Emerging Roles of Arf-Like GTP-Binding Proteins: From Membrane Trafficking to Cytoskeleton Dynamics and Beyond
Keywords:
Arl GTPase, Membrane trafficking, Lysosome, Cilia
Abstract
Arf-like (Arl) GTPases belong to the Ras superfamily of small GTPases with nearly 20 known members. As the name suggests, Arl GTPases were identified as proteins having a structure similar to ADP ribosylation factor (Arf) GTP-binding proteins. Despite having structurally resemblance to Arfs, Arl family members exhibit amazing diversity in mediating different cellular functions which makes them an attractive class of GTPases to study. Some of the examples include Arl3, Arl6 and Arl13b that are reported to be important for cilia biogenesis; Arl1 and Arl8 regulate the membrane trafficking pathways in cells; Arl11, a previously characterized tumor suppressor gene, is recently shown to be important for macrophage upon pathogen encounter. This review focuses on the known functions of Arl GTPases but there still remains a large gap in our understanding of how these Arls are regulated as well as the function of several Arl GTPases remains unknown.
References
Akhmanova A, Steinmetz M O (2015) Control of microtubule organization and dynamics: two ends in the limelight Nature Reviews Molecular Cell Biology 16 711
Amor J C, Horton J R, Zhu X, Wang Y, Sullards C, et al. (2001) Structures of yeast ARF2 and ARL1: distinct roles for the N terminus in the structure and function of ARF family GTPases J Biol Chem 276 42477-42484
Antonny B, Beraud-Dufour S, Chardin P, Chabre M (1997) N-terminal hydrophobic residues of the G-protein ADP-ribosylation factor-1 insert into membrane phospholipids upon GDP to GTP exchange Biochemistry 36 4675-4684
Antoshechkin I, Han M (2002) The C. elegans evl-20 gene is a homolog of the small GTPase ARL2 and regulates cytoskeleton dynamics during cytokinesis and morphogenesis Dev Cell 2 579-591
Arisi I, D'Onofrio M, Brandi R, Felsani A, Capsoni S, et al. (2011) Gene expression biomarkers in the brain of a mouse model for Alzheimer's disease: mining of microarray data by logic classification and feature selection J Alzheimers Dis 24 721-738
Arya S B, Kumar G, Kaur H, Kaur A, Tuli A (2018) ARL11 regulates lipopolysaccharide-stimulated macrophage activation by promoting mitogen-activated protein kinase (MAPK) signaling J Biol Chem 293 9892-9909
Avidor-Reiss T, Maer A M, Koundakjian E, Polyanovsky A, Keil T, et al. (2004) Decoding cilia function: defining specialized genes required for compartmentalized cilia biogenesis Cell 117 527-539
Badano J L, Mitsuma N, Beales P L, Katsanis N (2006) The ciliopathies: an emerging class of human genetic disorders Annu Rev Genomics Hum Genet 7 125-148
Bagshaw R D, Callahan J W, Mahuran D J (2006) The Arf-family protein, Arl8b, is involved in the spatial distribution of lysosomes Biochem Biophys Res Commun 344 1186-1191
Barral D C, Garg S, Casalou C, Watts G F M, Sandoval J L, et al. (2012) Arl13b regulates endocytic recycling traffic Proceedings of the National Academy of Sciences 109 21354-21359
Behar S M, Divangahi M, Remold H G (2010) Evasion of innate immunity by Mycobacterium tuberculosis: is death an exit strategy? Nat Rev Microbiol 8 668-674
Bestman J E, Huang L C, Lee-Osbourne J, Cheung P, Cline H T (2015) An in vivo screen to identify candidate neurogenic genes in the developing Xenopus visual system Dev Biol 408 269-291
Bhamidipati A, Lewis S A, Cowan N J (2000) ADP ribosylation factor-like protein 2 (Arl2) regulates the interaction of tubulin-folding cofactor D with native tubulin J Cell Biol 149 1087-1096
Blacque O E, Reardon M J, Li C, McCarthy J, Mahjoub M R, et al. (2004) Loss of C. elegans BBS-7 and BBS-8 protein function results in cilia defects and compromised intraflagellar transport Genes Dev 18 1630-1642
Boucrot E, Henry T, Borg J P, Gorvel J P, Meresse S (2005) The intracellular fate of Salmonella depends on the recruitment of kinesin Science 308 1174-1178
Breiner M, Schurmann A, Becker W, Joost H G (1996) Cloning of a novel member (ARL5) of the ARF-family of Ras-related GTPases Biochim Biophys Acta 1308 1-6
Breitfeld J, Stumvoll M, Kovacs P (2012) Genetics of adiponectin Biochimie 94 2157-2163
Calin G A, Trapasso F, Shimizu M, Dumitru C D, Yendamuri S, et al. (2005) Familial cancer associated with a polymorphism in ARLTS1 N Engl J Med 352 1667-1676
Cantagrel V, Silhavy J L, Bielas S L, Swistun D, Marsh S E, et al. (2008) Mutations in the Cilia Gene ARL13B Lead to the Classical Form of Joubert Syndrome American Journal of Human Genetics 83 170-179
Cavenagh M M, Breiner M, Schurmann A, Rosenwald A G, Terui T, et al. (1994) ADP-ribosylation factor (ARF)-like 3, a new member of the ARF family of GTP-binding proteins cloned from human and rat tissues J Biol Chem 269 18937-18942
Cevik S, Hori Y, Kaplan O I, Kida K, Toivenon T, et al. (2010) Joubert syndrome Arl13b functions at ciliary membranes and stabilizes protein transport in <em>Caenorhabditis elegans</em> The Journal of Cell Biology 188 953
Chang L, Kreko-Pierce T, Eaton B A (2015) The guanine exchange factor Gartenzwerg and the small GTPase Arl1 function in the same pathway with Arfaptin during synapse growth Biol Open 4 947-953
Chen B, Zhu Z, Wang Y, Ding X, Guo X, et al. (2018) Nature vs. nurture in human sociality: multi-level genomic analyses of social conformity J Hum Genet 63 605-619
Chen K, Koe C T, Xing Z B, Tian X, Rossi F, et al. (2016) Arl2- and Msps-dependent microtubule growth governs asymmetric division J Cell Biol 212 661-676
Chiang A P, Nishimura D, Searby C, Elbedour K, Carmi R, et al. (2004) Comparative genomic analysis identifies an ADP-ribosylation factor-like gene as the cause of Bardet-Biedl syndrome (BBS3) Am J Hum Genet 75 475-484
Clark J, Moore L, Krasinskas A, Way J, Battey J, et al. (1993) Selective amplification of additional members of the ADP-ribosylation factor (ARF) family: cloning of additional human and Drosophila ARF-like genes Proc Natl Acad Sci U S A 90 8952-8956
Cruz-Garcia D, Ortega-Bellido M, Scarpa M, Villeneuve J, Jovic M, et al. (2013) Recruitment of arfaptins to the trans-Golgi network by PI(4)P and their involvement in cargo export EMBO J 32 1717-1729
Cuvillier A, Redon F, Antoine J C, Chardin P, DeVos T, et al. (2000) LdARL-3A, a Leishmania promastigote-specific ADP-ribosylation factor-like protein, is essential for flagellum integrity J Cell Sci 113 ( Pt 11) 2065-2074
Dahlman I, Arner P (2010) Genetics of adipose tissue biology Prog Mol Biol Transl Sci 94 39-74
Divangahi M, Chen M, Gan H, Desjardins D, Hickman T T, et al. (2009) Mycobacterium tuberculosis evades macrophage defenses by inhibiting plasma membrane repair Nat Immunol 10 899-906
Donaldson J G, Jackson C L (2011) ARF family G proteins and their regulators: roles in membrane transport, development and disease Nat Rev Mol Cell Biol 12 362-375
Duldulao N A, Lee S, Sun Z (2009) Cilia localization is essential for in vivo functions of the Joubert syndrome protein Arl13b/Scorpion Development 136 4033
Dykes S S, Gray A L, Coleman D T, Saxena M, Stephens C A, et al. (2016) The Arf-like GTPase Arl8b is essential for three-dimensional invasive growth of prostate cancer in vitro and xenograft formation and growth in vivo Oncotarget 7 31037-31052
Eiseler T, Wille C, Koehler C, Illing A, Seufferlein T (2016) Protein Kinase D2 Assembles a Multiprotein Complex at the Trans-Golgi Network to Regulate Matrix Metalloproteinase Secretion J Biol Chem 291 462-477
Engel T, Lueken A, Bode G, Hobohm U, Lorkowski S, et al. (2004) ADP-ribosylation factor (ARF)-like 7 (ARL7) is induced by cholesterol loading and participates in apolipoprotein AI-dependent cholesterol export FEBS Lett 566 241-246
Evans R J, Schwarz N, Nagel-Wolfrum K, Wolfrum U, Hardcastle A J, et al. (2010) The retinitis pigmentosa protein RP2 links pericentriolar vesicle transport between the Golgi and the primary cilium Human Molecular Genetics 19 1358-1367
Fan Y, Esmail M A, Ansley S J, Blacque O E, Boroevich K, et al. (2004) Mutations in a member of the Ras superfamily of small GTP-binding proteins causes Bardet-Biedl syndrome Nat Genet 36 989-993
Fansa E K, Kosling S K, Zent E, Wittinghofer A, Ismail S (2016) PDE6delta-mediated sorting of INPP5E into the cilium is determined by cargo-carrier affinity Nat Commun 7 11366
Farias G G, Guardia C M, De Pace R, Britt D J, Bonifacino J S (2017) BORC/kinesin-1 ensemble drives polarized transport of lysosomes into the axon Proc Natl Acad Sci U S A 114 E2955-E2964
Filipek P A, de Araujo M E G, Vogel G F, De Smet C H, Eberharter D, et al. (2017) LAMTOR/Ragulator is a negative regulator of Arl8b- and BORC-dependent late endosomal positioning J Cell Biol 216 4199-4215
Francis J W, Goswami D, Novick S J, Pascal B D, Weikum E R, et al. (2017a) Nucleotide Binding to ARL2 in the TBCDARL2beta-Tubulin Complex Drives Conformational Changes in beta-Tubulin J Mol Biol 429 3696-3716
Francis J W, Newman L E, Cunningham L A, Kahn R A (2017b) A Trimer Consisting of the Tubulin-specific Chaperone D (TBCD), Regulatory GTPase ARL2, and beta-Tubulin Is Required for Maintaining the Microtubule Network J Biol Chem 292 4336-4349
Garg S, Sharma M, Ung C, Tuli A, Barral D C, et al. (2011) Lysosomal trafficking, antigen presentation, and microbial killing are controlled by the Arf-like GTPase Arl8b Immunity 35 182-193
Gehart H, Goginashvili A, Beck R, Morvan J, Erbs E, et al. (2012) The BAR domain protein Arfaptin-1 controls secretory granule biogenesis at the trans-Golgi network Dev Cell 23 756-768
Glessner J T, Bradfield J P, Wang K, Takahashi N, Zhang H, et al. (2010) A genome-wide study reveals copy number variants exclusive to childhood obesity cases Am J Hum Genet 87 661-666
Goetz S C, Anderson K V (2010) The primary cilium: a signalling centre during vertebrate development Nat Rev Genet 11 331-344
Goitre L, Trapani E, Trabalzini L, Retta S F (2014) The Ras superfamily of small GTPases: the unlocked secrets Methods Mol Biol 1120 1-18
Gotthardt K, Lokaj M, Koerner C, Falk N, Gießl A, et al. (2015) A G-protein activation cascade from Arl13B to Arl3 and implications for ciliary targeting of lipidated proteins eLife 4 e11859
Grayson C, Bartolini F, Chapple J P, Willison K R, Bhamidipati A, et al. (2002) Localization in the human retina of the X-linked retinitis pigmentosa protein RP2, its homologue cofactor C and the RP2 interacting protein Arl3 Hum Mol Genet 11 3065-3074
Guardia C M, Farias G G, Jia R, Pu J, Bonifacino J S (2016) BORC Functions Upstream of Kinesins 1 and 3 to Coordinate Regional Movement of Lysosomes along Different Microtubule Tracks Cell Rep 17 1950-1961
Hofmann I, Munro S (2006) An N-terminally acetylated Arf-like GTPase is localised to lysosomes and affects their motility J Cell Sci 119 1494-1503
Hofmann I, Thompson A, Sanderson C M, Munro S (2007) The Arl4 family of small G proteins can recruit the cytohesin Arf6 exchange factors to the plasma membrane Curr Biol 17 711-716
Hong C, Walczak R, Dhamko H, Bradley M N, Marathe C, et al. (2011) Constitutive activation of LXR in macrophages regulates metabolic and inflammatory gene expression: identification of ARL7 as a direct target J Lipid Res 52 531-539
Horner V L, Caspary T (2011) Disrupted dorsal neural tube BMP signaling in the cilia mutant Arl13bhnn stems from abnormal Shh signaling Developmental Biology 355 43-54
Houghton F J, Bellingham S A, Hill A F, Bourges D, Ang D K, et al. (2012) Arl5b is a Golgi-localised small G protein involved in the regulation of retrograde transport Exp Cell Res 318 464-477
Hoyt M A, Stearns T, Botstein D (1990) Chromosome instability mutants of Saccharomyces cerevisiae that are defective in microtubule-mediated processes Mol Cell Biol 10 223-234
Huotari J, Helenius A (2011) Endosome maturation EMBO J 30 3481-3500
Ishida M, Ohbayashi N, Fukuda M (2015) Rab1A regulates anterograde melanosome transport by recruiting kinesin-1 to melanosomes through interaction with SKIP Sci Rep 5 8238
Ivanova A A, Caspary T, Seyfried N T, Duong D M, West A B, et al. (2017) Biochemical characterization of purified mammalian ARL13B protein indicates that it is an atypical GTPase and ARL3 guanine nucleotide exchange factor (GEF) Journal of Biological Chemistry 292 11091-11108
Jacobs S, Schilf C, Fliegert F, Koling S, Weber Y, et al. (1999) ADP-ribosylation factor (ARF)-like 4, 6, and 7 represent a subgroup of the ARF family characterization by rapid nucleotide exchange and a nuclear localization signal FEBS Lett 456 384-388
Jacobs S, Schurmann A, Becker W, Bockers T M, Copeland N G, et al. (1998) The mouse ADP-ribosylation factor-like 4 gene: two separate promoters direct specific transcription in tissues and testicular germ cell Biochem J 335 ( Pt 2) 259-265
Jin H, White S R, Shida T, Schulz S, Aguiar M, et al. (2010) The Conserved Bardet-Biedl Syndrome Proteins Assemble a Coat that Traffics Membrane Proteins to Cilia Cell 141 1208-1219
Kahn R A, Cherfils J, Elias M, Lovering R C, Munro S, et al. (2006) Nomenclature for the human Arf family of GTP-binding proteins: ARF, ARL, and SAR proteins The Journal of Cell Biology 172 645
Kaniuk N A, Canadien V, Bagshaw R D, Bakowski M, Braun V, et al. (2011) Salmonella exploits Arl8B-directed kinesin activity to promote endosome tubulation and cell-to-cell transfer Cell Microbiol 13 1812-1823
Khatter D, Raina V B, Dwivedi D, Sindhwani A, Bahl S, et al. (2015a) The small GTPase Arl8b regulates assembly of the mammalian HOPS complex on lysosomes J Cell Sci 128 1746-1761
Khatter D, Sindhwani A, Sharma M (2015b) Arf-like GTPase Arl8: Moving from the periphery to the center of lysosomal biology Cell Logist 5 e1086501
Kitai Y, Takeuchi O, Kawasaki T, Ori D, Sueyoshi T, et al. (2015) Negative regulation of melanoma differentiation-associated gene 5 (MDA5)-dependent antiviral innate immune responses by Arf-like protein 5B J Biol Chem 290 1269-1280
Klassen M P, Wu Y E, Maeder C I, Nakae I, Cueva J G, et al. (2010) An Arf-like small G protein, ARL-8, promotes the axonal transport of presynaptic cargoes by suppressing vesicle aggregation Neuron 66 710-723
Kobayashi T, Hori Y, Ueda N, Kajiho H, Muraoka S, et al. (2009) Biochemical characterization of missense mutations in the Arf/Arl-family small GTPase Arl6 causing Bardet-Biedl syndrome Biochem Biophys Res Commun 381 439-442
Korolchuk V I, Saiki S, Lichtenberg M, Siddiqi F H, Roberts E A, et al. (2011) Lysosomal positioning coordinates cellular nutrient responses Nat Cell Biol 13 453-460
Lai C K, Gupta N, Wen X, Rangell L, Chih B, et al. (2011) Functional characterization of putative cilia genes by high-content analysis Mol Biol Cell 22 1104-1119
Larkins C E, Aviles G D G, East M P, Kahn R A, Caspary T (2011) Arl13b regulates ciliogenesis and the dynamic localization of Shh signaling proteins Molecular Biology of the Cell 22 4694-4703
Li C C, Wu T S, Huang C F, Jang L T, Liu Y T, et al. (2012a) GTP-binding-defective ARL4D alters mitochondrial morphology and membrane potential PLoS One 7 e43552
Li Y, Wei Q, Zhang Y, Ling K, Hu J (2010) The small GTPases ARL-13 and ARL-3 coordinate intraflagellar transport and ciliogenesis The Journal of Cell Biology 189 1039
Li Y, Zhang Q, Wei Q, Zhang Y, Ling K, et al. (2012b) SUMOylation of the small GTPase ARL-13 promotes ciliary targeting of sensory receptors The Journal of Cell Biology 199 589
Liem K F, Ashe A, He M, Satir P, Moran J, et al. (2012) The IFT-A complex regulates Shh signaling through cilia structure and membrane protein trafficking The Journal of Cell Biology 197 789
Liew Gerald M, Ye F, Nager Andrew R, Murphy J P, Lee Jaclyn S, et al. (2014) The Intraflagellar Transport Protein IFT27 Promotes BBSome Exit from Cilia through the GTPase ARL6/BBS3 Developmental Cell 31 265-278
Lin C Y, Huang P H, Liao W L, Cheng H J, Huang C F, et al. (2000) ARL4, an ARF-like protein that is developmentally regulated and localized to nuclei and nucleoli J Biol Chem 275 37815-37823
Lin Y C, Chiang T C, Liu Y T, Tsai Y T, Jang L T, et al. (2011) ARL4A acts with GCC185 to modulate Golgi complex organization J Cell Sci 124 4014-4026
Long L M, He B F, Huang G Q, Guo Y H, Liu Y S, et al. (2015) microRNA-214 functions as a tumor suppressor in human colon cancer via the suppression of ADP-ribosylation factor-like protein 2 Oncol Lett 9 645-650
Louro R, Nakaya H I, Paquola A C, Martins E A, da Silva A M, et al. (2004) RASL11A, member of a novel small monomeric GTPase gene family, is down-regulated in prostate tumors Biochem Biophys Res Commun 316 618-627
Lu H, Toh M T, Narasimhan V, Thamilselvam S K, Choksi S P, et al. (2015) A function for the Joubert syndrome protein Arl13b in ciliary membrane extension and ciliary length regulation Developmental Biology 397 225-236
Lu L, Tai G, Hong W (2004) Autoantigen Golgin-97, an effector of Arl1 GTPase, participates in traffic from the endosome to the trans-golgi network Mol Biol Cell 15 4426-4443
Maresova L, Vydareny T, Sychrova H (2012) Comparison of the influence of small GTPases Arl1 and Ypt6 on yeast cells' tolerance to various stress factors FEMS Yeast Res 12 332-340
Marion V, Stutzmann F, Gérard M, De Melo C, Schaefer E, et al. (2012) Exome sequencing identifies mutations in LZTFL, a BBSome and smoothened trafficking regulator, in a family with Bardet–Biedl syndrome with situs inversus and insertional polydactyly Journal of Medical Genetics 49 317
Marwaha R, Arya S B, Jagga D, Kaur H, Tuli A, et al. (2017) The Rab7 effector PLEKHM1 binds Arl8b to promote cargo traffic to lysosomes J Cell Biol 216 1051-1070
Michelet X, Garg S, Wolf B J, Tuli A, Ricciardi-Castagnoli P, et al. (2015) MHC class II presentation is controlled by the lysosomal small GTPase, Arl8b J Immunol 194 2079-2088
Michelet X, Tuli A, Gan H, Geadas C, Sharma M, et al. (2018) Lysosome-Mediated Plasma Membrane Repair Is Dependent on the Small GTPase Arl8b and Determines Cell Death Type in Mycobacterium tuberculosis Infection J Immunol 200 3160-3169
Mori R, Toda T (2013) The dual role of fission yeast Tbc1/cofactor C orchestrates microtubule homeostasis in tubulin folding and acts as a GAP for GTPase Alp41/Arl2 Mol Biol Cell 24 1713-1724, S1711-1718
Mourão A, Nager A R, Nachury M V, Lorentzen E (2014) Structural basis for membrane targeting of the BBSome by ARL6 Nat Struct Mol Biol 21 1035-1041
Mrakovic A, Kay J G, Furuya W, Brumell J H, Botelho R J (2012) Rab7 and Arl8 GTPases are necessary for lysosome tubulation in macrophages Traffic 13 1667-1679
Munro S (2005) The Arf-like GTPase Arl1 and its role in membrane traffic Biochem Soc Trans 33 601-605
Nakae I, Fujino T, Kobayashi T, Sasaki A, Kikko Y, et al. (2010) The arf-like GTPase Arl8 mediates delivery of endocytosed macromolecules to lysosomes in Caenorhabditis elegans Mol Biol Cell 21 2434-2442
Nakamura K, Man Z, Xie Y, Hanai A, Makyio H, et al. (2012) Structural basis for membrane binding specificity of the Bin/Amphiphysin/Rvs (BAR) domain of Arfaptin-2 determined by Arl1 GTPase J Biol Chem 287 25478-25489
Negi S, Juyal G, Senapati S, Prasad P, Gupta A, et al. (2013) A genome-wide association study reveals ARL15, a novel non-HLA susceptibility gene for rheumatoid arthritis in North Indians Arthritis Rheum 65 3026-3035
Newman L E, Schiavon C R, Zhou C, Kahn R A (2017) The abundance of the ARL2 GTPase and its GAP, ELMOD2, at mitochondria are modulated by the fusogenic activity of mitofusins and stressors PLoS One 12 e0175164
Newman L E, Zhou C J, Mudigonda S, Mattheyses A L, Paradies E, et al. (2014) The ARL2 GTPase is required for mitochondrial morphology, motility, and maintenance of ATP levels PLoS One 9 e99270
Nishikiori M, Mori M, Dohi K, Okamura H, Katoh E, et al. (2011) A host small GTP-binding protein ARL8 plays crucial roles in tobamovirus RNA replication PLoS Pathog 7 e1002409
Nithianantham S, Le S, Seto E, Jia W, Leary J, et al. (2015) Tubulin cofactors and Arl2 are cage-like chaperones that regulate the soluble alphabeta-tubulin pool for microtubule dynamics eLife 4
Niwa S, Lipton D M, Morikawa M, Zhao C, Hirokawa N, et al. (2016) Autoinhibition of a Neuronal Kinesin UNC-104/KIF1A Regulates the Size and Density of Synapses Cell Rep 16 2129-2141
Novick P (2016) Regulation of membrane traffic by Rab GEF and GAP cascades Small GTPases 7 252-256
Okai T, Araki Y, Tada M, Tateno T, Kontani K, et al. (2004) Novel small GTPase subfamily capable of associating with tubulin is required for chromosome segregation J Cell Sci 117 4705-4715
Otto E A, Hurd T W, Airik R, Chaki M, Zhou W, et al. (2010) Candidate exome capture identifies mutation of SDCCAG8 as the cause of a retinal-renal ciliopathy Nat Genet 42 840-850
Ozdemir E S, Jang H, Gursoy A, Keskin O, Nussinov R (2018) Arl2-Mediated Allosteric Release of Farnesylated KRas4B from Shuttling Factor PDEdelta J Phys Chem B 122 7503-7513
Panic B, Perisic O, Veprintsev D B, Williams R L, Munro S (2003a) Structural basis for Arl1-dependent targeting of homodimeric GRIP domains to the Golgi apparatus Mol Cell 12 863-874
Panic B, Whyte J R, Munro S (2003b) The ARF-like GTPases Arl1p and Arl3p act in a pathway that interacts with vesicle-tethering factors at the Golgi apparatus Curr Biol 13 405-410
Pasqualato S, Renault L, Cherfils J (2002) Arf, Arl, Arp and Sar proteins: a family of GTP-binding proteins with a structural device for 'front-back' communication EMBO Rep 3 1035-1041
Patel M, Chiang T C, Tran V, Lee F J, Cote J F (2011) The Arf family GTPase Arl4A complexes with ELMO proteins to promote actin cytoskeleton remodeling and reveals a versatile Ras-binding domain in the ELMO proteins family J Biol Chem 286 38969-38979
Paul P, van den Hoorn T, Jongsma M L, Bakker M J, Hengeveld R, et al. (2011) A Genome-wide multidimensional RNAi screen reveals pathways controlling MHC class II antigen presentation Cell 145 268-283
Platko K, Lebeau P, Austin R C (2018) MAPping the kinase landscape of macrophage activation J Biol Chem 293 9910-9911
Price H P, Peltan A, Stark M, Smith D F (2010) The small GTPase ARL2 is required for cytokinesis in Trypanosoma brucei Mol Biochem Parasitol 173 123-131
Pruski M, Rajnicek A, Yang Z, Clancy H, Ding Y-Q, et al. (2016) The ciliary GTPase Arl13b regulates cell migration and cell cycle progression Cell Adhesion & Migration 10 393-405
Pu J, Keren-Kaplan T, Bonifacino J S (2017) A Ragulator-BORC interaction controls lysosome positioning in response to amino acid availability J Cell Biol 216 4183-4197
Pu J, Schindler C, Jia R, Jarnik M, Backlund P, et al. (2015) BORC, a multisubunit complex that regulates lysosome positioning Dev Cell 33 176-188
Radcliffe P A, Vardy L, Toda T (2000) A conserved small GTP-binding protein Alp41 is essential for the cofactor-dependent biogenesis of microtubules in fission yeast FEBS Lett 468 84-88
Richards J B, Waterworth D, O'Rahilly S, Hivert M F, Loos R J, et al. (2009) A genome-wide association study reveals variants in ARL15 that influence adiponectin levels PLoS Genet 5 e1000768
Rosa-Ferreira C, Christis C, Torres I L, Munro S (2015) The small G protein Arl5 contributes to endosome-to-Golgi traffic by aiding the recruitment of the GARP complex to the Golgi Biol Open 4 474-481
Rosa-Ferreira C, Munro S (2011) Arl8 and SKIP act together to link lysosomes to kinesin-1 Dev Cell 21 1171-1178
Schiefermeier N, Scheffler J M, de Araujo M E, Stasyk T, Yordanov T, et al. (2014) The late endosomal p14-MP1 (LAMTOR2/3) complex regulates focal adhesion dynamics during cell migration J Cell Biol 205 525-540
Schrick J J, Vogel P, Abuin A, Hampton B, Rice D S (2006) ADP-ribosylation factor-like 3 is involved in kidney and photoreceptor development Am J Pathol 168 1288-1298
Schurmann A, Breiner M, Becker W, Huppertz C, Kainulainen H, et al. (1994) Cloning of two novel ADP-ribosylation factor-like proteins and characterization of their differential expression in 3T3-L1 cells J Biol Chem 269 15683-15688
Schurmann A, Koling S, Jacobs S, Saftig P, Krauss S, et al. (2002) Reduced sperm count and normal fertility in male mice with targeted disruption of the ADP-ribosylation factor-like 4 (Arl4) gene Mol Cell Biol 22 2761-2768
Seixas C, Choi S Y, Polgar N, Umberger N L, East M P, et al. (2016) Arl13b and the exocyst interact synergistically in ciliogenesis Molecular Biology of the Cell 27 308-320
Shao J, Xu L, Chen L, Lu Q, Xie X, et al. (2017) Arl13b Promotes Gastric Tumorigenesis by Regulating Smo Trafficking and Activation of the Hedgehog Signaling Pathway Cancer Research 77 4000
Sharer J D, Shern J F, Van Valkenburgh H, Wallace D C, Kahn R A (2002) ARL2 and BART enter mitochondria and bind the adenine nucleotide transporter Mol Biol Cell 13 71-83
Sindhwani A, Arya S B, Kaur H, Jagga D, Tuli A, et al. (2017) Salmonella exploits the host endolysosomal tethering factor HOPS complex to promote its intravacuolar replication PLoS Pathog 13 e1006700
Song P, Dudinsky L, Fogerty J, Gaivin R, Perkins B D (2016) Arl13b Interacts With Vangl2 to Regulate Cilia and Photoreceptor Outer Segment Length in ZebrafishArl13b/Vangl2 Epistasis Regulates Photoreceptor Cilia Investigative Ophthalmology & Visual Science 57 4517-4526
Spasic M, Jacobs C R (2017) Primary cilia: Cell and molecular mechanosensors directing whole tissue function Semin Cell Dev Biol 71 42-52
Sun Z, Amsterdam A, Pazour G J, Cole D G, Miller M S, et al. (2004) A genetic screen in zebrafish identifies cilia genes as a principal cause of cystic kidney Development 131 4085
Tamkun J W, Kahn R A, Kissinger M, Brizuela B J, Rulka C, et al. (1991) The arflike gene encodes an essential GTP-binding protein in Drosophila Proceedings of the National Academy of Sciences 88 3120-3124
Torres I L, Rosa-Ferreira C, Munro S (2014) The Arf family G protein Arl1 is required for secretory granule biogenesis in Drosophila J Cell Sci 127 2151-2160
Tuli A, Thiery J, James A M, Michelet X, Sharma M, et al. (2013) Arf-like GTPase Arl8b regulates lytic granule polarization and natural killer cell-mediated cytotoxicity Mol Biol Cell 24 3721-3735
Wang I H, Chen Y J, Hsu J W, Lee F J (2017a) The Arl3 and Arl1 GTPases co-operate with Cog8 to regulate selective autophagy via Atg9 trafficking Traffic 18 580-589
Wang J, Qi X, Zhang X, Yan W, You C (2017b) [Genetic polymorphisms of ARL15 and HLA-DMA are associated with rheumatoid arthritis in Han population from northwest China] Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi 33 1681-1685
Wei S M, Xie C G, Abe Y, Cai J T (2009) ADP-ribosylation factor like 7 (ARL7) interacts with alpha-tubulin and modulates intracellular vesicular transport Biochem Biophys Res Commun 384 352-356
Wiens C J, Tong Y, Esmail M A, Oh E, Gerdes J M, et al. (2010) Bardet-Biedl Syndrome-associated Small GTPase ARL6 (BBS3) Functions at or near the Ciliary Gate and Modulates Wnt Signaling Journal of Biological Chemistry 285 16218-16230
Wright K J, Baye L M, Olivier-Mason A, Mukhopadhyay S, Sang L, et al. (2011) An ARL3–UNC119–RP2 GTPase cycle targets myristoylated NPHP3 to the primary cilium Genes & Development 25 2347-2360
Wu M, Lu L, Hong W, Song H (2004) Structural basis for recruitment of GRIP domain golgin-245 by small GTPase Arl1 Nat Struct Mol Biol 11 86-94
Wu Y E, Huo L, Maeder C I, Feng W, Shen K (2013) The balance between capture and dissociation of presynaptic proteins controls the spatial distribution of synapses Neuron 78 994-1011
Yang Y K, Qu H, Gao D, Di W, Chen H W, et al. (2011) ARF-like protein 16 (ARL16) inhibits RIG-I by binding with its C-terminal domain in a GTP-dependent manner J Biol Chem 286 10568-10580
Ye F, Nager A R, Nachury M V (2018) BBSome trains remove activated GPCRs from cilia by enabling passage through the transition zone The Journal of Cell Biology
Yendamuri S, Trapasso F, Calin G A (2008) ARLTS1 - a novel tumor suppressor gene Cancer Lett 264 11-20
Yendamuri S, Trapasso F, Ferracin M, Cesari R, Sevignani C, et al. (2007) Tumor suppressor functions of ARLTS1 in lung cancers Cancer Res 67 7738-7745
Yu C J, Lee F J (2017) Multiple activities of Arl1 GTPase in the trans-Golgi network J Cell Sci 130 1691-1699
Yu J, Ka S O, Kwon K B, Lee S M, Park J W, et al. (2011) Overexpression of the small GTPase Arl4D suppresses adipogenesis Int J Mol Med 28 793-798
Zaghloul N A, Katsanis N (2009) Mechanistic insights into Bardet-Biedl syndrome, a model ciliopathy The Journal of Clinical Investigation 119 428-437
Zhang Q, Li Y, Zhang Y, Torres V E, Harris P C, et al. (2016) GTP-binding of ARL-3 is activated by ARL-13 as a GEF and stabilized by UNC-119 Scientific Reports 6 24534
Zhang Q, Nishimura D, Seo S, Vogel T, Morgan D A, et al. (2011) Bardet-Biedl syndrome 3 (Bbs3) knockout mouse model reveals common BBS-associated phenotypes and Bbs3 unique phenotypes Proceedings of the National Academy of Sciences 108 20678-20683
Zhao J, Wang M, Deng W, Zhong D, Jiang Y, et al. (2017) ADP-ribosylation factor-like GTPase 15 enhances insulin-induced AKT phosphorylation in the IR/IRS1/AKT pathway by interacting with ASAP2 and regulating PDPK1 activity Biochem Biophys Res Commun 486 865-871
Zhou C X, Shi L Y, Li R C, Liu Y H, Xu B Q, et al. (2017) GTPase-activating protein Elmod2 is essential for meiotic progression in mouse oocytes Cell Cycle 16 852-860
Acknowledgements
Amor J C, Horton J R, Zhu X, Wang Y, Sullards C, et al. (2001) Structures of yeast ARF2 and ARL1: distinct roles for the N terminus in the structure and function of ARF family GTPases J Biol Chem 276 42477-42484
Antonny B, Beraud-Dufour S, Chardin P, Chabre M (1997) N-terminal hydrophobic residues of the G-protein ADP-ribosylation factor-1 insert into membrane phospholipids upon GDP to GTP exchange Biochemistry 36 4675-4684
Antoshechkin I, Han M (2002) The C. elegans evl-20 gene is a homolog of the small GTPase ARL2 and regulates cytoskeleton dynamics during cytokinesis and morphogenesis Dev Cell 2 579-591
Arisi I, D'Onofrio M, Brandi R, Felsani A, Capsoni S, et al. (2011) Gene expression biomarkers in the brain of a mouse model for Alzheimer's disease: mining of microarray data by logic classification and feature selection J Alzheimers Dis 24 721-738
Arya S B, Kumar G, Kaur H, Kaur A, Tuli A (2018) ARL11 regulates lipopolysaccharide-stimulated macrophage activation by promoting mitogen-activated protein kinase (MAPK) signaling J Biol Chem 293 9892-9909
Avidor-Reiss T, Maer A M, Koundakjian E, Polyanovsky A, Keil T, et al. (2004) Decoding cilia function: defining specialized genes required for compartmentalized cilia biogenesis Cell 117 527-539
Badano J L, Mitsuma N, Beales P L, Katsanis N (2006) The ciliopathies: an emerging class of human genetic disorders Annu Rev Genomics Hum Genet 7 125-148
Bagshaw R D, Callahan J W, Mahuran D J (2006) The Arf-family protein, Arl8b, is involved in the spatial distribution of lysosomes Biochem Biophys Res Commun 344 1186-1191
Barral D C, Garg S, Casalou C, Watts G F M, Sandoval J L, et al. (2012) Arl13b regulates endocytic recycling traffic Proceedings of the National Academy of Sciences 109 21354-21359
Behar S M, Divangahi M, Remold H G (2010) Evasion of innate immunity by Mycobacterium tuberculosis: is death an exit strategy? Nat Rev Microbiol 8 668-674
Bestman J E, Huang L C, Lee-Osbourne J, Cheung P, Cline H T (2015) An in vivo screen to identify candidate neurogenic genes in the developing Xenopus visual system Dev Biol 408 269-291
Bhamidipati A, Lewis S A, Cowan N J (2000) ADP ribosylation factor-like protein 2 (Arl2) regulates the interaction of tubulin-folding cofactor D with native tubulin J Cell Biol 149 1087-1096
Blacque O E, Reardon M J, Li C, McCarthy J, Mahjoub M R, et al. (2004) Loss of C. elegans BBS-7 and BBS-8 protein function results in cilia defects and compromised intraflagellar transport Genes Dev 18 1630-1642
Boucrot E, Henry T, Borg J P, Gorvel J P, Meresse S (2005) The intracellular fate of Salmonella depends on the recruitment of kinesin Science 308 1174-1178
Breiner M, Schurmann A, Becker W, Joost H G (1996) Cloning of a novel member (ARL5) of the ARF-family of Ras-related GTPases Biochim Biophys Acta 1308 1-6
Breitfeld J, Stumvoll M, Kovacs P (2012) Genetics of adiponectin Biochimie 94 2157-2163
Calin G A, Trapasso F, Shimizu M, Dumitru C D, Yendamuri S, et al. (2005) Familial cancer associated with a polymorphism in ARLTS1 N Engl J Med 352 1667-1676
Cantagrel V, Silhavy J L, Bielas S L, Swistun D, Marsh S E, et al. (2008) Mutations in the Cilia Gene ARL13B Lead to the Classical Form of Joubert Syndrome American Journal of Human Genetics 83 170-179
Cavenagh M M, Breiner M, Schurmann A, Rosenwald A G, Terui T, et al. (1994) ADP-ribosylation factor (ARF)-like 3, a new member of the ARF family of GTP-binding proteins cloned from human and rat tissues J Biol Chem 269 18937-18942
Cevik S, Hori Y, Kaplan O I, Kida K, Toivenon T, et al. (2010) Joubert syndrome Arl13b functions at ciliary membranes and stabilizes protein transport in <em>Caenorhabditis elegans</em> The Journal of Cell Biology 188 953
Chang L, Kreko-Pierce T, Eaton B A (2015) The guanine exchange factor Gartenzwerg and the small GTPase Arl1 function in the same pathway with Arfaptin during synapse growth Biol Open 4 947-953
Chen B, Zhu Z, Wang Y, Ding X, Guo X, et al. (2018) Nature vs. nurture in human sociality: multi-level genomic analyses of social conformity J Hum Genet 63 605-619
Chen K, Koe C T, Xing Z B, Tian X, Rossi F, et al. (2016) Arl2- and Msps-dependent microtubule growth governs asymmetric division J Cell Biol 212 661-676
Chiang A P, Nishimura D, Searby C, Elbedour K, Carmi R, et al. (2004) Comparative genomic analysis identifies an ADP-ribosylation factor-like gene as the cause of Bardet-Biedl syndrome (BBS3) Am J Hum Genet 75 475-484
Clark J, Moore L, Krasinskas A, Way J, Battey J, et al. (1993) Selective amplification of additional members of the ADP-ribosylation factor (ARF) family: cloning of additional human and Drosophila ARF-like genes Proc Natl Acad Sci U S A 90 8952-8956
Cruz-Garcia D, Ortega-Bellido M, Scarpa M, Villeneuve J, Jovic M, et al. (2013) Recruitment of arfaptins to the trans-Golgi network by PI(4)P and their involvement in cargo export EMBO J 32 1717-1729
Cuvillier A, Redon F, Antoine J C, Chardin P, DeVos T, et al. (2000) LdARL-3A, a Leishmania promastigote-specific ADP-ribosylation factor-like protein, is essential for flagellum integrity J Cell Sci 113 ( Pt 11) 2065-2074
Dahlman I, Arner P (2010) Genetics of adipose tissue biology Prog Mol Biol Transl Sci 94 39-74
Divangahi M, Chen M, Gan H, Desjardins D, Hickman T T, et al. (2009) Mycobacterium tuberculosis evades macrophage defenses by inhibiting plasma membrane repair Nat Immunol 10 899-906
Donaldson J G, Jackson C L (2011) ARF family G proteins and their regulators: roles in membrane transport, development and disease Nat Rev Mol Cell Biol 12 362-375
Duldulao N A, Lee S, Sun Z (2009) Cilia localization is essential for in vivo functions of the Joubert syndrome protein Arl13b/Scorpion Development 136 4033
Dykes S S, Gray A L, Coleman D T, Saxena M, Stephens C A, et al. (2016) The Arf-like GTPase Arl8b is essential for three-dimensional invasive growth of prostate cancer in vitro and xenograft formation and growth in vivo Oncotarget 7 31037-31052
Eiseler T, Wille C, Koehler C, Illing A, Seufferlein T (2016) Protein Kinase D2 Assembles a Multiprotein Complex at the Trans-Golgi Network to Regulate Matrix Metalloproteinase Secretion J Biol Chem 291 462-477
Engel T, Lueken A, Bode G, Hobohm U, Lorkowski S, et al. (2004) ADP-ribosylation factor (ARF)-like 7 (ARL7) is induced by cholesterol loading and participates in apolipoprotein AI-dependent cholesterol export FEBS Lett 566 241-246
Evans R J, Schwarz N, Nagel-Wolfrum K, Wolfrum U, Hardcastle A J, et al. (2010) The retinitis pigmentosa protein RP2 links pericentriolar vesicle transport between the Golgi and the primary cilium Human Molecular Genetics 19 1358-1367
Fan Y, Esmail M A, Ansley S J, Blacque O E, Boroevich K, et al. (2004) Mutations in a member of the Ras superfamily of small GTP-binding proteins causes Bardet-Biedl syndrome Nat Genet 36 989-993
Fansa E K, Kosling S K, Zent E, Wittinghofer A, Ismail S (2016) PDE6delta-mediated sorting of INPP5E into the cilium is determined by cargo-carrier affinity Nat Commun 7 11366
Farias G G, Guardia C M, De Pace R, Britt D J, Bonifacino J S (2017) BORC/kinesin-1 ensemble drives polarized transport of lysosomes into the axon Proc Natl Acad Sci U S A 114 E2955-E2964
Filipek P A, de Araujo M E G, Vogel G F, De Smet C H, Eberharter D, et al. (2017) LAMTOR/Ragulator is a negative regulator of Arl8b- and BORC-dependent late endosomal positioning J Cell Biol 216 4199-4215
Francis J W, Goswami D, Novick S J, Pascal B D, Weikum E R, et al. (2017a) Nucleotide Binding to ARL2 in the TBCDARL2beta-Tubulin Complex Drives Conformational Changes in beta-Tubulin J Mol Biol 429 3696-3716
Francis J W, Newman L E, Cunningham L A, Kahn R A (2017b) A Trimer Consisting of the Tubulin-specific Chaperone D (TBCD), Regulatory GTPase ARL2, and beta-Tubulin Is Required for Maintaining the Microtubule Network J Biol Chem 292 4336-4349
Garg S, Sharma M, Ung C, Tuli A, Barral D C, et al. (2011) Lysosomal trafficking, antigen presentation, and microbial killing are controlled by the Arf-like GTPase Arl8b Immunity 35 182-193
Gehart H, Goginashvili A, Beck R, Morvan J, Erbs E, et al. (2012) The BAR domain protein Arfaptin-1 controls secretory granule biogenesis at the trans-Golgi network Dev Cell 23 756-768
Glessner J T, Bradfield J P, Wang K, Takahashi N, Zhang H, et al. (2010) A genome-wide study reveals copy number variants exclusive to childhood obesity cases Am J Hum Genet 87 661-666
Goetz S C, Anderson K V (2010) The primary cilium: a signalling centre during vertebrate development Nat Rev Genet 11 331-344
Goitre L, Trapani E, Trabalzini L, Retta S F (2014) The Ras superfamily of small GTPases: the unlocked secrets Methods Mol Biol 1120 1-18
Gotthardt K, Lokaj M, Koerner C, Falk N, Gießl A, et al. (2015) A G-protein activation cascade from Arl13B to Arl3 and implications for ciliary targeting of lipidated proteins eLife 4 e11859
Grayson C, Bartolini F, Chapple J P, Willison K R, Bhamidipati A, et al. (2002) Localization in the human retina of the X-linked retinitis pigmentosa protein RP2, its homologue cofactor C and the RP2 interacting protein Arl3 Hum Mol Genet 11 3065-3074
Guardia C M, Farias G G, Jia R, Pu J, Bonifacino J S (2016) BORC Functions Upstream of Kinesins 1 and 3 to Coordinate Regional Movement of Lysosomes along Different Microtubule Tracks Cell Rep 17 1950-1961
Hofmann I, Munro S (2006) An N-terminally acetylated Arf-like GTPase is localised to lysosomes and affects their motility J Cell Sci 119 1494-1503
Hofmann I, Thompson A, Sanderson C M, Munro S (2007) The Arl4 family of small G proteins can recruit the cytohesin Arf6 exchange factors to the plasma membrane Curr Biol 17 711-716
Hong C, Walczak R, Dhamko H, Bradley M N, Marathe C, et al. (2011) Constitutive activation of LXR in macrophages regulates metabolic and inflammatory gene expression: identification of ARL7 as a direct target J Lipid Res 52 531-539
Horner V L, Caspary T (2011) Disrupted dorsal neural tube BMP signaling in the cilia mutant Arl13bhnn stems from abnormal Shh signaling Developmental Biology 355 43-54
Houghton F J, Bellingham S A, Hill A F, Bourges D, Ang D K, et al. (2012) Arl5b is a Golgi-localised small G protein involved in the regulation of retrograde transport Exp Cell Res 318 464-477
Hoyt M A, Stearns T, Botstein D (1990) Chromosome instability mutants of Saccharomyces cerevisiae that are defective in microtubule-mediated processes Mol Cell Biol 10 223-234
Huotari J, Helenius A (2011) Endosome maturation EMBO J 30 3481-3500
Ishida M, Ohbayashi N, Fukuda M (2015) Rab1A regulates anterograde melanosome transport by recruiting kinesin-1 to melanosomes through interaction with SKIP Sci Rep 5 8238
Ivanova A A, Caspary T, Seyfried N T, Duong D M, West A B, et al. (2017) Biochemical characterization of purified mammalian ARL13B protein indicates that it is an atypical GTPase and ARL3 guanine nucleotide exchange factor (GEF) Journal of Biological Chemistry 292 11091-11108
Jacobs S, Schilf C, Fliegert F, Koling S, Weber Y, et al. (1999) ADP-ribosylation factor (ARF)-like 4, 6, and 7 represent a subgroup of the ARF family characterization by rapid nucleotide exchange and a nuclear localization signal FEBS Lett 456 384-388
Jacobs S, Schurmann A, Becker W, Bockers T M, Copeland N G, et al. (1998) The mouse ADP-ribosylation factor-like 4 gene: two separate promoters direct specific transcription in tissues and testicular germ cell Biochem J 335 ( Pt 2) 259-265
Jin H, White S R, Shida T, Schulz S, Aguiar M, et al. (2010) The Conserved Bardet-Biedl Syndrome Proteins Assemble a Coat that Traffics Membrane Proteins to Cilia Cell 141 1208-1219
Kahn R A, Cherfils J, Elias M, Lovering R C, Munro S, et al. (2006) Nomenclature for the human Arf family of GTP-binding proteins: ARF, ARL, and SAR proteins The Journal of Cell Biology 172 645
Kaniuk N A, Canadien V, Bagshaw R D, Bakowski M, Braun V, et al. (2011) Salmonella exploits Arl8B-directed kinesin activity to promote endosome tubulation and cell-to-cell transfer Cell Microbiol 13 1812-1823
Khatter D, Raina V B, Dwivedi D, Sindhwani A, Bahl S, et al. (2015a) The small GTPase Arl8b regulates assembly of the mammalian HOPS complex on lysosomes J Cell Sci 128 1746-1761
Khatter D, Sindhwani A, Sharma M (2015b) Arf-like GTPase Arl8: Moving from the periphery to the center of lysosomal biology Cell Logist 5 e1086501
Kitai Y, Takeuchi O, Kawasaki T, Ori D, Sueyoshi T, et al. (2015) Negative regulation of melanoma differentiation-associated gene 5 (MDA5)-dependent antiviral innate immune responses by Arf-like protein 5B J Biol Chem 290 1269-1280
Klassen M P, Wu Y E, Maeder C I, Nakae I, Cueva J G, et al. (2010) An Arf-like small G protein, ARL-8, promotes the axonal transport of presynaptic cargoes by suppressing vesicle aggregation Neuron 66 710-723
Kobayashi T, Hori Y, Ueda N, Kajiho H, Muraoka S, et al. (2009) Biochemical characterization of missense mutations in the Arf/Arl-family small GTPase Arl6 causing Bardet-Biedl syndrome Biochem Biophys Res Commun 381 439-442
Korolchuk V I, Saiki S, Lichtenberg M, Siddiqi F H, Roberts E A, et al. (2011) Lysosomal positioning coordinates cellular nutrient responses Nat Cell Biol 13 453-460
Lai C K, Gupta N, Wen X, Rangell L, Chih B, et al. (2011) Functional characterization of putative cilia genes by high-content analysis Mol Biol Cell 22 1104-1119
Larkins C E, Aviles G D G, East M P, Kahn R A, Caspary T (2011) Arl13b regulates ciliogenesis and the dynamic localization of Shh signaling proteins Molecular Biology of the Cell 22 4694-4703
Li C C, Wu T S, Huang C F, Jang L T, Liu Y T, et al. (2012a) GTP-binding-defective ARL4D alters mitochondrial morphology and membrane potential PLoS One 7 e43552
Li Y, Wei Q, Zhang Y, Ling K, Hu J (2010) The small GTPases ARL-13 and ARL-3 coordinate intraflagellar transport and ciliogenesis The Journal of Cell Biology 189 1039
Li Y, Zhang Q, Wei Q, Zhang Y, Ling K, et al. (2012b) SUMOylation of the small GTPase ARL-13 promotes ciliary targeting of sensory receptors The Journal of Cell Biology 199 589
Liem K F, Ashe A, He M, Satir P, Moran J, et al. (2012) The IFT-A complex regulates Shh signaling through cilia structure and membrane protein trafficking The Journal of Cell Biology 197 789
Liew Gerald M, Ye F, Nager Andrew R, Murphy J P, Lee Jaclyn S, et al. (2014) The Intraflagellar Transport Protein IFT27 Promotes BBSome Exit from Cilia through the GTPase ARL6/BBS3 Developmental Cell 31 265-278
Lin C Y, Huang P H, Liao W L, Cheng H J, Huang C F, et al. (2000) ARL4, an ARF-like protein that is developmentally regulated and localized to nuclei and nucleoli J Biol Chem 275 37815-37823
Lin Y C, Chiang T C, Liu Y T, Tsai Y T, Jang L T, et al. (2011) ARL4A acts with GCC185 to modulate Golgi complex organization J Cell Sci 124 4014-4026
Long L M, He B F, Huang G Q, Guo Y H, Liu Y S, et al. (2015) microRNA-214 functions as a tumor suppressor in human colon cancer via the suppression of ADP-ribosylation factor-like protein 2 Oncol Lett 9 645-650
Louro R, Nakaya H I, Paquola A C, Martins E A, da Silva A M, et al. (2004) RASL11A, member of a novel small monomeric GTPase gene family, is down-regulated in prostate tumors Biochem Biophys Res Commun 316 618-627
Lu H, Toh M T, Narasimhan V, Thamilselvam S K, Choksi S P, et al. (2015) A function for the Joubert syndrome protein Arl13b in ciliary membrane extension and ciliary length regulation Developmental Biology 397 225-236
Lu L, Tai G, Hong W (2004) Autoantigen Golgin-97, an effector of Arl1 GTPase, participates in traffic from the endosome to the trans-golgi network Mol Biol Cell 15 4426-4443
Maresova L, Vydareny T, Sychrova H (2012) Comparison of the influence of small GTPases Arl1 and Ypt6 on yeast cells' tolerance to various stress factors FEMS Yeast Res 12 332-340
Marion V, Stutzmann F, Gérard M, De Melo C, Schaefer E, et al. (2012) Exome sequencing identifies mutations in LZTFL, a BBSome and smoothened trafficking regulator, in a family with Bardet–Biedl syndrome with situs inversus and insertional polydactyly Journal of Medical Genetics 49 317
Marwaha R, Arya S B, Jagga D, Kaur H, Tuli A, et al. (2017) The Rab7 effector PLEKHM1 binds Arl8b to promote cargo traffic to lysosomes J Cell Biol 216 1051-1070
Michelet X, Garg S, Wolf B J, Tuli A, Ricciardi-Castagnoli P, et al. (2015) MHC class II presentation is controlled by the lysosomal small GTPase, Arl8b J Immunol 194 2079-2088
Michelet X, Tuli A, Gan H, Geadas C, Sharma M, et al. (2018) Lysosome-Mediated Plasma Membrane Repair Is Dependent on the Small GTPase Arl8b and Determines Cell Death Type in Mycobacterium tuberculosis Infection J Immunol 200 3160-3169
Mori R, Toda T (2013) The dual role of fission yeast Tbc1/cofactor C orchestrates microtubule homeostasis in tubulin folding and acts as a GAP for GTPase Alp41/Arl2 Mol Biol Cell 24 1713-1724, S1711-1718
Mourão A, Nager A R, Nachury M V, Lorentzen E (2014) Structural basis for membrane targeting of the BBSome by ARL6 Nat Struct Mol Biol 21 1035-1041
Mrakovic A, Kay J G, Furuya W, Brumell J H, Botelho R J (2012) Rab7 and Arl8 GTPases are necessary for lysosome tubulation in macrophages Traffic 13 1667-1679
Munro S (2005) The Arf-like GTPase Arl1 and its role in membrane traffic Biochem Soc Trans 33 601-605
Nakae I, Fujino T, Kobayashi T, Sasaki A, Kikko Y, et al. (2010) The arf-like GTPase Arl8 mediates delivery of endocytosed macromolecules to lysosomes in Caenorhabditis elegans Mol Biol Cell 21 2434-2442
Nakamura K, Man Z, Xie Y, Hanai A, Makyio H, et al. (2012) Structural basis for membrane binding specificity of the Bin/Amphiphysin/Rvs (BAR) domain of Arfaptin-2 determined by Arl1 GTPase J Biol Chem 287 25478-25489
Negi S, Juyal G, Senapati S, Prasad P, Gupta A, et al. (2013) A genome-wide association study reveals ARL15, a novel non-HLA susceptibility gene for rheumatoid arthritis in North Indians Arthritis Rheum 65 3026-3035
Newman L E, Schiavon C R, Zhou C, Kahn R A (2017) The abundance of the ARL2 GTPase and its GAP, ELMOD2, at mitochondria are modulated by the fusogenic activity of mitofusins and stressors PLoS One 12 e0175164
Newman L E, Zhou C J, Mudigonda S, Mattheyses A L, Paradies E, et al. (2014) The ARL2 GTPase is required for mitochondrial morphology, motility, and maintenance of ATP levels PLoS One 9 e99270
Nishikiori M, Mori M, Dohi K, Okamura H, Katoh E, et al. (2011) A host small GTP-binding protein ARL8 plays crucial roles in tobamovirus RNA replication PLoS Pathog 7 e1002409
Nithianantham S, Le S, Seto E, Jia W, Leary J, et al. (2015) Tubulin cofactors and Arl2 are cage-like chaperones that regulate the soluble alphabeta-tubulin pool for microtubule dynamics eLife 4
Niwa S, Lipton D M, Morikawa M, Zhao C, Hirokawa N, et al. (2016) Autoinhibition of a Neuronal Kinesin UNC-104/KIF1A Regulates the Size and Density of Synapses Cell Rep 16 2129-2141
Novick P (2016) Regulation of membrane traffic by Rab GEF and GAP cascades Small GTPases 7 252-256
Okai T, Araki Y, Tada M, Tateno T, Kontani K, et al. (2004) Novel small GTPase subfamily capable of associating with tubulin is required for chromosome segregation J Cell Sci 117 4705-4715
Otto E A, Hurd T W, Airik R, Chaki M, Zhou W, et al. (2010) Candidate exome capture identifies mutation of SDCCAG8 as the cause of a retinal-renal ciliopathy Nat Genet 42 840-850
Ozdemir E S, Jang H, Gursoy A, Keskin O, Nussinov R (2018) Arl2-Mediated Allosteric Release of Farnesylated KRas4B from Shuttling Factor PDEdelta J Phys Chem B 122 7503-7513
Panic B, Perisic O, Veprintsev D B, Williams R L, Munro S (2003a) Structural basis for Arl1-dependent targeting of homodimeric GRIP domains to the Golgi apparatus Mol Cell 12 863-874
Panic B, Whyte J R, Munro S (2003b) The ARF-like GTPases Arl1p and Arl3p act in a pathway that interacts with vesicle-tethering factors at the Golgi apparatus Curr Biol 13 405-410
Pasqualato S, Renault L, Cherfils J (2002) Arf, Arl, Arp and Sar proteins: a family of GTP-binding proteins with a structural device for 'front-back' communication EMBO Rep 3 1035-1041
Patel M, Chiang T C, Tran V, Lee F J, Cote J F (2011) The Arf family GTPase Arl4A complexes with ELMO proteins to promote actin cytoskeleton remodeling and reveals a versatile Ras-binding domain in the ELMO proteins family J Biol Chem 286 38969-38979
Paul P, van den Hoorn T, Jongsma M L, Bakker M J, Hengeveld R, et al. (2011) A Genome-wide multidimensional RNAi screen reveals pathways controlling MHC class II antigen presentation Cell 145 268-283
Platko K, Lebeau P, Austin R C (2018) MAPping the kinase landscape of macrophage activation J Biol Chem 293 9910-9911
Price H P, Peltan A, Stark M, Smith D F (2010) The small GTPase ARL2 is required for cytokinesis in Trypanosoma brucei Mol Biochem Parasitol 173 123-131
Pruski M, Rajnicek A, Yang Z, Clancy H, Ding Y-Q, et al. (2016) The ciliary GTPase Arl13b regulates cell migration and cell cycle progression Cell Adhesion & Migration 10 393-405
Pu J, Keren-Kaplan T, Bonifacino J S (2017) A Ragulator-BORC interaction controls lysosome positioning in response to amino acid availability J Cell Biol 216 4183-4197
Pu J, Schindler C, Jia R, Jarnik M, Backlund P, et al. (2015) BORC, a multisubunit complex that regulates lysosome positioning Dev Cell 33 176-188
Radcliffe P A, Vardy L, Toda T (2000) A conserved small GTP-binding protein Alp41 is essential for the cofactor-dependent biogenesis of microtubules in fission yeast FEBS Lett 468 84-88
Richards J B, Waterworth D, O'Rahilly S, Hivert M F, Loos R J, et al. (2009) A genome-wide association study reveals variants in ARL15 that influence adiponectin levels PLoS Genet 5 e1000768
Rosa-Ferreira C, Christis C, Torres I L, Munro S (2015) The small G protein Arl5 contributes to endosome-to-Golgi traffic by aiding the recruitment of the GARP complex to the Golgi Biol Open 4 474-481
Rosa-Ferreira C, Munro S (2011) Arl8 and SKIP act together to link lysosomes to kinesin-1 Dev Cell 21 1171-1178
Schiefermeier N, Scheffler J M, de Araujo M E, Stasyk T, Yordanov T, et al. (2014) The late endosomal p14-MP1 (LAMTOR2/3) complex regulates focal adhesion dynamics during cell migration J Cell Biol 205 525-540
Schrick J J, Vogel P, Abuin A, Hampton B, Rice D S (2006) ADP-ribosylation factor-like 3 is involved in kidney and photoreceptor development Am J Pathol 168 1288-1298
Schurmann A, Breiner M, Becker W, Huppertz C, Kainulainen H, et al. (1994) Cloning of two novel ADP-ribosylation factor-like proteins and characterization of their differential expression in 3T3-L1 cells J Biol Chem 269 15683-15688
Schurmann A, Koling S, Jacobs S, Saftig P, Krauss S, et al. (2002) Reduced sperm count and normal fertility in male mice with targeted disruption of the ADP-ribosylation factor-like 4 (Arl4) gene Mol Cell Biol 22 2761-2768
Seixas C, Choi S Y, Polgar N, Umberger N L, East M P, et al. (2016) Arl13b and the exocyst interact synergistically in ciliogenesis Molecular Biology of the Cell 27 308-320
Shao J, Xu L, Chen L, Lu Q, Xie X, et al. (2017) Arl13b Promotes Gastric Tumorigenesis by Regulating Smo Trafficking and Activation of the Hedgehog Signaling Pathway Cancer Research 77 4000
Sharer J D, Shern J F, Van Valkenburgh H, Wallace D C, Kahn R A (2002) ARL2 and BART enter mitochondria and bind the adenine nucleotide transporter Mol Biol Cell 13 71-83
Sindhwani A, Arya S B, Kaur H, Jagga D, Tuli A, et al. (2017) Salmonella exploits the host endolysosomal tethering factor HOPS complex to promote its intravacuolar replication PLoS Pathog 13 e1006700
Song P, Dudinsky L, Fogerty J, Gaivin R, Perkins B D (2016) Arl13b Interacts With Vangl2 to Regulate Cilia and Photoreceptor Outer Segment Length in ZebrafishArl13b/Vangl2 Epistasis Regulates Photoreceptor Cilia Investigative Ophthalmology & Visual Science 57 4517-4526
Spasic M, Jacobs C R (2017) Primary cilia: Cell and molecular mechanosensors directing whole tissue function Semin Cell Dev Biol 71 42-52
Sun Z, Amsterdam A, Pazour G J, Cole D G, Miller M S, et al. (2004) A genetic screen in zebrafish identifies cilia genes as a principal cause of cystic kidney Development 131 4085
Tamkun J W, Kahn R A, Kissinger M, Brizuela B J, Rulka C, et al. (1991) The arflike gene encodes an essential GTP-binding protein in Drosophila Proceedings of the National Academy of Sciences 88 3120-3124
Torres I L, Rosa-Ferreira C, Munro S (2014) The Arf family G protein Arl1 is required for secretory granule biogenesis in Drosophila J Cell Sci 127 2151-2160
Tuli A, Thiery J, James A M, Michelet X, Sharma M, et al. (2013) Arf-like GTPase Arl8b regulates lytic granule polarization and natural killer cell-mediated cytotoxicity Mol Biol Cell 24 3721-3735
Wang I H, Chen Y J, Hsu J W, Lee F J (2017a) The Arl3 and Arl1 GTPases co-operate with Cog8 to regulate selective autophagy via Atg9 trafficking Traffic 18 580-589
Wang J, Qi X, Zhang X, Yan W, You C (2017b) [Genetic polymorphisms of ARL15 and HLA-DMA are associated with rheumatoid arthritis in Han population from northwest China] Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi 33 1681-1685
Wei S M, Xie C G, Abe Y, Cai J T (2009) ADP-ribosylation factor like 7 (ARL7) interacts with alpha-tubulin and modulates intracellular vesicular transport Biochem Biophys Res Commun 384 352-356
Wiens C J, Tong Y, Esmail M A, Oh E, Gerdes J M, et al. (2010) Bardet-Biedl Syndrome-associated Small GTPase ARL6 (BBS3) Functions at or near the Ciliary Gate and Modulates Wnt Signaling Journal of Biological Chemistry 285 16218-16230
Wright K J, Baye L M, Olivier-Mason A, Mukhopadhyay S, Sang L, et al. (2011) An ARL3–UNC119–RP2 GTPase cycle targets myristoylated NPHP3 to the primary cilium Genes & Development 25 2347-2360
Wu M, Lu L, Hong W, Song H (2004) Structural basis for recruitment of GRIP domain golgin-245 by small GTPase Arl1 Nat Struct Mol Biol 11 86-94
Wu Y E, Huo L, Maeder C I, Feng W, Shen K (2013) The balance between capture and dissociation of presynaptic proteins controls the spatial distribution of synapses Neuron 78 994-1011
Yang Y K, Qu H, Gao D, Di W, Chen H W, et al. (2011) ARF-like protein 16 (ARL16) inhibits RIG-I by binding with its C-terminal domain in a GTP-dependent manner J Biol Chem 286 10568-10580
Ye F, Nager A R, Nachury M V (2018) BBSome trains remove activated GPCRs from cilia by enabling passage through the transition zone The Journal of Cell Biology
Yendamuri S, Trapasso F, Calin G A (2008) ARLTS1 - a novel tumor suppressor gene Cancer Lett 264 11-20
Yendamuri S, Trapasso F, Ferracin M, Cesari R, Sevignani C, et al. (2007) Tumor suppressor functions of ARLTS1 in lung cancers Cancer Res 67 7738-7745
Yu C J, Lee F J (2017) Multiple activities of Arl1 GTPase in the trans-Golgi network J Cell Sci 130 1691-1699
Yu J, Ka S O, Kwon K B, Lee S M, Park J W, et al. (2011) Overexpression of the small GTPase Arl4D suppresses adipogenesis Int J Mol Med 28 793-798
Zaghloul N A, Katsanis N (2009) Mechanistic insights into Bardet-Biedl syndrome, a model ciliopathy The Journal of Clinical Investigation 119 428-437
Zhang Q, Li Y, Zhang Y, Torres V E, Harris P C, et al. (2016) GTP-binding of ARL-3 is activated by ARL-13 as a GEF and stabilized by UNC-119 Scientific Reports 6 24534
Zhang Q, Nishimura D, Seo S, Vogel T, Morgan D A, et al. (2011) Bardet-Biedl syndrome 3 (Bbs3) knockout mouse model reveals common BBS-associated phenotypes and Bbs3 unique phenotypes Proceedings of the National Academy of Sciences 108 20678-20683
Zhao J, Wang M, Deng W, Zhong D, Jiang Y, et al. (2017) ADP-ribosylation factor-like GTPase 15 enhances insulin-induced AKT phosphorylation in the IR/IRS1/AKT pathway by interacting with ASAP2 and regulating PDPK1 activity Biochem Biophys Res Commun 486 865-871
Zhou C X, Shi L Y, Li R C, Liu Y H, Xu B Q, et al. (2017) GTPase-activating protein Elmod2 is essential for meiotic progression in mouse oocytes Cell Cycle 16 852-860
Acknowledgements
Published
2019-04-04
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Copyright (c) 2019 Mahak Sharma, Rituraj Rituraj Marwaha, Devashish Dwivedi
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