Phagosome-lysosome fusion hijack - An art of intracellular pathogens

  • Rameshwaram Nagender Rao Centre for DNA Fingerprinting & Diagnostics
  • Rohini Shrivastava Centre for DNA Fingerprinting & Diagnostics
  • Gourango Pradhan Centre for DNA Fingerprinting & Diagnostics
  • Parul Singh Centre for DNA Fingerprinting & Diagnostics
  • Sangita Mukhopadhyay Centre for DNA Fingerprinting & Diagnostics
Keywords: Phagosome-lysosome fusion, host signaling, cytokines, Rab GTPases, Lipid bodies

Abstract

Phagosome-lysosome fusion is an important innate-effector immune response of host macrophages. After entering the macrophages through phagocytosis, intracellular bacteria and parasites reside inside the phagosomes. In many cases, these pathogens prevent maturation of phagosomes and its fusion with lysosomes. Several signaling cascades are shown to be associated with blocking of phagosome maturation process. Understanding the mechanism of phagosome-lysosome fusion and factors regulating this process as well as the strategies adopted by the intracellular pathogens to prevent phagosome-lysosome fusion might provide insights for the development of new drugs and more effective treatment options to combat infectious diseases

Author Biographies

Rameshwaram Nagender Rao, Centre for DNA Fingerprinting & Diagnostics

Project Investigator (DST-SERB)

Laboratory of Molecular Cell Biology, CDFD

Rohini Shrivastava, Centre for DNA Fingerprinting & Diagnostics

Senior Research Fellow (CSIR)

Laboratory of Molecular Cell Biology, CDFD

Gourango Pradhan, Centre for DNA Fingerprinting & Diagnostics

Senior Research Fellow (ICMR)

Laboratory of Molecular Cell Biology, CDFD

Parul Singh, Centre for DNA Fingerprinting & Diagnostics

Senior Research Fellow (UGC)

Laboratory of Molecular Cell Biology, CDFD

Sangita Mukhopadhyay, Centre for DNA Fingerprinting & Diagnostics

Staff Scientist - VI & Group Head

Laboratory of Molecular Cell Biology, CDFD

References

Aderem A and Underhill D M (1999) Mechanisms of phagocytosis in macrophages. Annu Rev Immunol 17 593-623

Ahearn J M and Fearon D T (1989) Structure and function of the complement receptors, CR1 (CD35) and CR2 (CD21). Adv Immunol 46 183-219

An H, Xu H, Zhang M, Zhou J, Feng T, Qian C, Qi R and Cao X (2005) Src homology 2 domain-containing inositol-5-phosphatase 1 (SHIP1) negatively regulates TLR4-mediated LPS response primarily through a phosphatase activity- and PI-3K-independent mechanism. Blood 105 4685-4692

Appelmelk B J, den Dunnen J, Driessen NN, Ummels R, Pak M, Nigou J, Larrouy-Maumus G, Gurcha SS, Movahedzadeh F, Geurtsen J, Brown EJ, Eysink Smeets MM, Besra GS, Willemsen PT, Lowary TL, van Kooyk Y, Maaskant JJ, Stoker NG, van der Ley P, Puzo G, Vandenbroucke-Grauls CM, Wieland CW, van der Poll T, Geijtenbeek TB, van der Sar AM and Bitter W (2008) The mannose cap of mycobacterial lipoarabinomannan does not dominate the Mycobacterium-host interaction. Cell Microbiol 10 930-944

Barbero P, Bittova L and Pfeffer SR (2002) Visualization of Rab9-mediated vesicle transport from endosomes to the trans-Golgi in living cells. J Cell Biol 156 511-518

Barry AO, Mege JL and Ghigo E (2011) Hijacked phagosomes and leukocyte activation: an intimate relationship. J Leukoc Biol 89 373-382

Beauregard KE, Lee KD, Collier RJ and Swanson JA (1997) pH-dependent perforation of macrophage phagosomes by listeriolysin O from Listeria monocytogenes. J Exp Med 186 1159-1163

Bhattacharya M, Ojha N, Solanki S, Mukhopadhyay CK, Madan R, Patel N, Krishnamurthy G, Kumar S, Basu SK and Mukhopadhyay A (2006) IL-6 and IL-12 specifically regulate the expression of Rab5 and Rab7 via distinct signaling pathways. EMBO J 25 2878-2888

Blander J M and Medzhitov R (2004) Regulation of phagosome maturation by signals from toll-like receptors. Science 304 1014-1018

Bougnères L, Helft J, Tiwari S, Vargas P, Chang BH, Chan L, Campisi L, Lauvau G, Hugues S, Kumar P, Kamphorst AO, Dumenil AM, Nussenzweig M, MacMicking JD, Amigorena S and Guermonprez P (2009) A role for lipid bodies in the cross-presentation of phagocytosed antigens by MHC class I in dendritic cells. Immunity 31 232-244

Brzoza KL, Rockel AB and Hiltbold EM (2004) Cytoplasmic entry of Listeria monocytogenes enhances dendritic cell maturation and T cell differentiation and function. J Immunol 173 2641-2651

Bucci C, Thomsen P, Nicoziani P, McCarthy J and van Deurs B (2000) Rab7: a key to lysosome biogenesis. Mol Biol Cell 11 467-480

Bui M, Gilady SY, Fitzsimmons RE, Benson MD, Lynes EM, Gesson K, Alto NM, Strack S, Scott JD and Simmen T (2010) Rab32 modulates apoptosis onset and mitochondria-associated membrane (MAM) properties. J Biol Chem 285 31590-31602

Burgdorf S, Kautz A, Bohnert V, Knolle PA and Kurts C (2007) Distinct pathways of antigen uptake and intracellular routing in CD4 and CD8 T cell activation. Science 316 612-616

Burgoyne RD and Clague MJ (2003) Calcium and calmodulin in membrane fusion. Biochim Biophys Acta 164 1137-1143

Callaghan J, Simonsen A, Gaullier JM, Toh BH and Stenmark H (1999) The endosome fusion regulator early-endosomal autoantigen 1 (EEA1) is a dimer. Biochem J 338 539-543

Camandaroba E, Thé TS, Pessina DH and Andrade SG (2006) Trypanosoma cruzi: clones isolated from the Colombian strain, reproduce the parental strain characteristics, with ubiquitous histotropism. Int J ExpPathol 87 209-217

Campbell-Valois FX, Sachse M, Sansonetti PJ and Parsot C (2015) Escape of actively secreting Shigella flexneri from ATG8/LC3-positive vacuoles formed during cell-to-cell spread is facilitated by IcsB and VirA. MBio 6 e02567-14

Caparros E, Munoz P, Sierra-Filardi E, Serrano-Gomez D, Puig-Kroger A, Rodriguez-Fernandez J L, Mellado M, Sancho J, Zubiaur M and Corbi A L (2006) DC-SIGN ligation on dendritic cells results in ERK and PI3K activation and modulates cytokine production. Blood 107 3950-3958

Capo C, Zaffran Y, Zugun F, Houpikian P, Raoult D and Mege JL (1996) Production of interleukin-10 and transforming growth factor beta by peripheral blood mononuclear cells in Q fever endocarditis. Infect Immun 64 4143-4147

Cardona PJ, Llatjós R, Gordillo S, Díaz J, Ojanguren I, Ariza A and Ausina V (2000) Evolution of granulomas in lungs of mice infected aerogenically with Mycobacterium tuberculosis. Scand J Immunol 52 156-163

Carroll M C (1998) The role of complement and complement receptors in induction and regulation of immunity. Annu Rev Immunol 16 545-568

Chen YT, Holcomb C and Moore HP (1993) Expression and localization of two low molecular weight GTP-binding proteins, Rab8 and Rab10, by epitope tag. Proc Natl Acad Sci U S A 190 6508-6512

Clemens DL, Lee BY and Horwitz MA (2002) The Mycobacterium tuberculosis phagosome in human macrophages is isolated from the host cell cytoplasm. Infect Immun 70 5800-5807

Cocchiaro JL, Kumar Y, Fischer ER, Hackstadt T and Valdivia RH (2008) Cytoplasmic lipid droplets are translocated into the lumen of the Chlamydia trachomatis parasitophorous vacuole. Proc Natl Acad Sci U S A 105 9379-9384

Coyne C B, Shen L, Turner JR and Bergelson JM (2007) Coxsackievirus entry across epithelial tight junctions requires occludin and the small GTPases Rab34 and Rab5. Cell Host Microbe 2 181-192

D'Avila H, Melo RC, Parreira GG, Werneck-Barroso E, Castro-Faria-Neto HC and Bozza PT (2006) Mycobacterium bovis bacillus Calmette-Guerin induces TLR2-mediated formation of lipid bodies: intracellular domains for eicosanoid synthesis in vivo. J Immunol 176 3087-3097

Daniel J, Maamar H, Deb C, Sirakova TD and Kolattukudy PE (2011) Mycobacterium tuberculosis uses host triacylglycerol to accumulate lipid droplets and acquires a dormancy-like phenotype in lipid-loaded macrophages. PLoS Pathog 7 e1002093

Desjardins M, Huber L A, Parton R G and Griffiths G (1994) Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus. J Cell Biol 124 677-688

Dhiman R, Indramohan M, Barnes PF, Nayak RC, Paidipally P, Rao LV and Vankayalapati R (2009) IL-22 produced by human NK cells inhibits growth of Mycobacterium tuberculosis by enhancing phagolysosomal fusion. J Immunol 183 6639-6645

Dkhar HK, Nanduri R, Mahajan S, Dave S, Saini A, Somavarapu AK, Arora A, Parkesh R, Thakur KG, Mayilraj S and Gupta P (2014) Mycobacterium tuberculosis keto-mycolic acid and macrophage nuclear receptor TR4 modulate foamy biogenesis in granulomas: a case of a heterologous and noncanonical ligand-receptor pair. J Immunol 193 295-305

Evering T and Weiss LM (2006) The immunology of parasite infections in immunocompromised hosts. Parasite Immunol 28 549-565

Ezekowitz RA, Sastry K, Bailly P and Warner A (1990) Molecular characterization of the human macrophage mannose receptor: demonstration of multiple carbohydrate recognition-like domains and phagocytosis of yeasts in Cos-1 cells. J Exp Med 172 1785-1794

Flannagan RS, Cosío G, Grinstein S (2009) Antimicrobial mechanisms of phagocytes and bacterial evasion strategies. Nat Rev Microbiol 7 355-66

Fratti RA, Backer JM, Gruenberg J, Corvera S and Deretic V (2001) Role of phosphatidylinositol 3-kinase and Rab5 effectors in phagosomal biogenesis and mycobacterial phagosome maturation arrest. J Cell Biol 154 631-644

Fratti RA, Chua J, Vergne I and Deretic V (2003) Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest. Proc Natl Acad Sci U S A 100 5437-5442

Frehel C and Rastogi N (1987) Mycobacterium leprae surface components intervene in the early phagosome-lysosome fusion inhibition event. Infect Immun 55 2916-2921

Futter CE, Collinson LM, Backer JM and Hopkins CR (2001) Human VPS34 is required for internal vesicle formation within multivesicular endosomes. J Cell Biol 155 1251-1264

Garin J, Diez R, Kieffer S, Dermine J F, Duclos S, Gagnon E, Sadoul R, Rondeau C and Desjardins M (2001) The phagosome proteome: insight into phagosome functions. J Cell Biol 152 165-180

Gazi U and Martinez-Pomares L (2009) Influence of the mannose receptor in host immune responses. Immunobiology 214 554-561

Ghigo E, Capo C, Tung CH, Raoult D, Gorvel JP and Mege JL (2002) Coxiella burnetii survival in THP-1 monocytes involves the impairment of phagosome maturation: IFN-gamma mediates its restoration and bacterial killing. J Immunol 169 4488-4495

Ghigo E, Honstettre A, Capo C, Gorvel JP, Raoult D and Mege JL (2004) Link between impaired maturation of phagosomes and defective Coxiella burnetii killing in patients with chronic Q fever. J Infect Dis 190 1767-1772

Ghigo E, Colombo MI and Heinzen RA (2012) The Coxiella burnetii parasitophorous vacuole. Adv Exp Med Biol 984 141-169

Gorvel J P, Chavrier P, Zerial M and Gruenberg J (1991) rab5 controls early endosome fusion in vitro. Cell 64 915-925

Greenberg S and Grinstein S (2002) Phagocytosis and innate immunity. Curr Opin Immunol 14 136-145

Hackstadt T (2000) Redirection of host vesicle trafficking pathways by intracellular parasites. Traffic 1 93-99

Hirsch CS, Ellner JJ, Russell DG and Rich EA (1994) Complement receptor-mediated uptake and tumor necrosis factor-alpha-mediated growth inhibition of Mycobacterium tuberculosis by human alveolar macrophages. J Immunol 152 743-753

Honstettre A, Imbert G, Ghigo E, Gouriet F, Capo C, Raoult D and Mege JL (2003) Dysregulation of cytokines in acute Q fever: role of interleukin-10 and tumor necrosis factor in chronic evolution of Q fever. J Infect Dis 187 956-962

Horiuchi H, Lippe R, McBride HM, Rubino M, Woodman P, Stenmark H, Rybin V, Wilm M, Ashman K, Mann M and Zerial M (1997) A novel Rab5 GDP/GTP exchange factor complexed to Rabaptin-5 links nucleotide exchange to effector recruitment and function. Cell 90 1149-1159

Hu C, Mayadas-Norton T, Tanaka K, Chan J and Salgame P (2000) Mycobacterium tuberculosis infection in complement receptor 3-deficient mice. J Immunol 165 2596-2602

Hussain Bhat K, Mukhopadhyay S (2015) Macrophage takeover and the host-bacilli interplay during tuberculosis. Future Microbiol 10 853-872

Ishibashi Y and Arai T (1990) Roles of the complement receptor type 1 (CR1) and type 3 (CR3) on phagocytosis and subsequent phagosome-lysosome fusion in Salmonella-infected murine macrophages. FEMS Microbiol Immunol 2 89-96

Itoh T, Fujita N, Kanno E, Yamamoto A, Yoshimori T and Fukuda M (2008) Golgi-resident small GTPase Rab33B interacts with Atg16L and modulates autophagosome formation. Mol Biol Cell 19 2916-2925

Jahraus A, Egeberg M, Hinner B, Habermann A, Sackman E, Pralle A, Faulstich H, Rybin V, Defacque H and Griffiths G (2001) ATP-dependent membrane assembly of F-actin facilitates membrane fusion. Mol Biol Cell 12 155-170

Jehl SP, Nogueira CV, Zhang X and Starnbach MN (2012) IFNγ inhibits the cytosolic replication of Shigella flexneri via the cytoplasmic RNA sensor RIG-I. PloS Pathog 8 e1002809

Jouanguy E, Altare F, Lamhamedi S, Revy P, Emile JF, Newport M, Levin M, Blanche S, Seboun E, Fischer A and Casanova JL (1996) Interferon-gamma-receptor deficiency in an infant with fatal bacille Calmette-Guérin infection. N Engl J Med 335 1956-1961

Junutula JR, De Maziére AM, Peden AA, Ervin KE, Advani RJ, van Dijk SM, Klumperman J and Scheller RH (2004) Rab14 is involved in membrane trafficking between the Golgi complex and endosomes. Mol Biol Cell 15 2218-2229

Kang PB, Azad AK, Torrelles JB, Kaufman TM, Beharka A, Tibesar E, Desjardin LE and Schlesinger LS (2005) The human macrophage mannose receptor directs Mycobacterium tuberculosis lipoarabinomannan-mediated phagosome biogenesis. J Exp Med 202 987-999

Kelley VA and Schorey J S (2003) Mycobacterium's arrest of phagosome maturation in macrophages requires Rab5 activity and accessibility to iron. Mol Biol Cell 14 3366-3377

Kobayashi K, Hernandez LD, Galan JE, Janeway CA, Jr. Medzhitov R and Flavell RA (2002) IRAK-M is a negative regulator of Toll-like receptor signaling. Cell 110 191-202

Kouranti I, Sachse M, Arouche N, Goud B and Echard A (2006) Rab35 regulates an endocytic recycling pathway essential for the terminal steps of cytokinesis. Curr Biol 16 1719-1725

Kumar Y, Cocchiaro J and Valdivia RH (2006) The obligate intracellular pathogen Chlamydia trachomatis targets host lipid droplets. CurrBiol 16 1646-1651

Kyei GB, Vergne I, Chua J, Roberts E, Harris J, Junutula JR and Deretic V (2006) Rab14 is critical for maintenance of Mycobacterium tuberculosis phagosome maturation arrest. EMBO J 25 5250-5259

Lebreton A, Stavru F and Cossart P (2015) Organelle targeting during bacterial infection: insights from Listeria. Trends Cell Biol 25 330-338

Li Y, Wang Y, Zou L, Tang X, Yang Y, Ma L, Jia Q, Ni Q, Liu S, Tang L, Lin R, Wong E, Sun W, Wang L, Wei Q, Ran H, Zhang L, Lian H, Huang W, Wu Y, Li QJ and Wan Y (2016) Analysis of the Rab GTPase interactome in dendritic cells reveals anti-microbial functions of the Rab32 complex in bacterial containment. Immunity 44 422-437

Loftus SK, Larson DM, Baxter LL, Antonellis A, Chen Y, Wu X, Jiang Y, Bittner M, Hammer JA 3rd and Pavan WJ (2002) Mutation of melanosome protein RAB38 in chocolate mice. Proc Natl Acad Sci U S A 99 4471-4476

Lugering N, Kucharzik T, Stein H, Winde G, Lugering A, Hasilik A, Domschke W and Stoll R (1998) IL-10 synergizes with IL-4 and IL-13 in inhibiting lysosomal enzyme secretion by human monocytes and lamina propria mononuclear cells from patients with inflammatory bowel disease. Dig Dis Sci 43 706-714

Luo M, Fadeev EA and Groves JT (2005) Mycobactin-mediated iron acquisition within macrophages. Nat ChemBiol 1 149-153

Markgraf D F, Peplowska K and Ungermann C (2007) Rab cascades and tethering factors in the endomembrane system. FEBS Lett 581 2125-2130

Mariño G, Niso-Santano M, Baehrecke EH and Kroemer G (2014) Self-consumption: the interplay of autophagy and apoptosis. Nat Rev Mol Cell Biol 15 81-94

Martinez FO and Gordon S (2014) The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep 6 13

Mattos KA, D'Avila H, Rodrigues LS, Oliveira VG, Sarno EN, Atella GC, Pereira GM, Bozza PT and Pessolani MC (2010) Lipid droplet formation in leprosy: Toll-like receptor-regulated organelles involved in eicosanoid formation and Mycobacterium leprae pathogenesis. J Leukoc Biol 87 371-384

Mattos KA, Lara FA, Oliveira VG, Rodrigues LS, D'Avila H, Melo RC, Manso PP, Sarno EN, Bozza PT and Pessolani (2011) Modulation of lipid droplets by Mycobacterium leprae in Schwann cells: a putative mechanism for host lipid acquisition and bacterial survival in phagosomes. Cell Microbiol 13 259-273

Mattos KA, Oliveira VG, D'Avila H, Rodrigues LS, Pinheiro RO, Sarno EN, Pessolani MC and Bozza PT (2011b) TLR6-driven lipid droplets in Mycobacterium leprae-infected Schwann cells: immunoinflammatory platforms associated with bacterial persistence. J Immunol 187 2548-2558

McBride HM, Rybin V, Murphy C, Giner A, Teasdale R and Zerial M (1999) Oligomeric complexes link Rab5 effectors with NSF and drive membrane fusion via interactions between EEA1 and syntaxin 13. Cell 98 377-386

McCoy CE, Sheedy FJ, Qualls JE, Doyle SL, Quinn SR., Murray PJ and O'Neill LA (2010) IL-10 inhibits miR-155 induction by toll-like receptors. J Biol Chem 285 20492-20498

Medzhitov R., Preston-Hurlburt P and Janeway C A Jr (1997) A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388 394-397

Melo RCN, D'Avila H, Fabrino DL, Almeida PE and Bozza PT (2003) Macrophage lipid body induction by Chagas disease in vivo: putative intracellular domains for eicosanoid formation during infection. Tissue Cell 35 59-67

Mesa R, Magadán J, Barbieri A, López C, Stahl PD and Mayorga LS (2005) Overexpression of Rab22a hampers the transport between endosomes and the Golgi apparatus. Exp Cell Res 304 339-353

Mia S, Warnecke A, Zhang X M, Malmstrom V and Harris R A (2014) An optimized protocol for human M2 macrophages using M-CSF and IL-4/IL-10/TGF-beta yields a dominant immunosuppressive phenotype. Scand J Immunol 79 305-314

Miinea C P, Sano H, Kane S, Sano E, Fukuda M, Peranen J, Lane WS and Lienhard GE (2005) AS160, the Akt substrate regulating GLUT4 translocation, has a functional Rab GTPase-activating protein domain. Biochem J 391 87-93

Mills C D (2012) M1 and M2 Macrophages: Oracles of Health and Disease. Crit Rev Immunol 32 463-488

Mitchell G, Chen C and Portnoy DA (2016) Strategies used by bacteria to grow in macrophages. Microbiol Spectr 4 10.1128

Montaner LJ, da Silva RP, Sun J, Sutterwala S, Hollinshead M, Vaux D and Gordon S (1999) Type 1 and type 2 cytokine regulation of macrophage endocytosis: differential activation by IL-4/IL-13 as opposed to IFN-gamma or IL-10. J Immunol 162 4606-4613

Mosser DM and Edelson PJ (1987) The third component of complement (C3) is responsible for the intracellular survival of Leishmania major. Nature 327 329-331

Munafo DB and Colombo MI (2002) Induction of autophagy causes dramatic changes in the subcellular distribution of GFP-Rab24. Traffic 3 472-482

Murray P J and Wynn T A (2011) Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol 11 723-737

Nair S (2014) Immunomodulatory role of mycobacterial PE/PPE family of proteins. Proc Indian Natn Sci Acad 80 1055-1072

Ng EL, Wang Y and Tang BL (2007) Rab22B's role in trans-Golgi network membrane dynamics. Biochem Biophys Res Commun 361 751-757

Ng Yan Hing JD, Desjardins M and Descoteaux A (2004) Proteomic analysis reveals a role for protein kinase C-alpha in phagosome maturation. Biochem Biophys Res Commun 319 810-816

O'Leary S, O'Sullivan MP and Keane J (2011) IL-10 blocks phagosome maturation in mycobacterium tuberculosis-infected human macrophages. Am J Respir Cell Mol Biol 45 172-180

Pandey AK and Sassetti CM (2008) Mycobacterial persistence requires the utilization of host cholesterol. Proc Natl Acad Sci U S A 105 4376-4380

Pathak SK, Basu S, Bhattacharyya A, Pathak S, Kundu M and Basu J (2005) Mycobacterium tuberculosis lipoarabinomannan-mediated IRAK-M induction negatively regulates Toll-like receptor-dependent interleukin-12 p40 production in macrophages. J Biol Chem 280 42794-42800

Pellinen T, Arjonen A, Vuoriluoto K, Kallio K, Fransen JA and Ivaska J (2006) Small GTPase Rab21 regulates cell adhesion and controls endosomal traffic of β1-integrins. J Cell Biol 173 767-780

Peyron P, Vaubourgeix J, Poquet Y, Levillain F, Botanch C, Bardou F, Daffé M, Emile JF, Marchou B, Cardona PJ, de Chastellier C and Altare F (2008) Foamy macrophages from tuberculous patients' granulomas constitute a nutrient-rich reservoir for M. tuberculosis persistence. PLoS Pathog 4 e1000204

Polando R, Dixit UG, Carter CR, Jones B, Whitcomb JP, Ballhorn W, Harintho M, Jerde CL, Wilson ME and McDowell MA (2013) The roles of complement receptor 3 and Fcgamma receptors during Leishmania phagosome maturation. J Leukoc Biol 93 921-932

Poteryaev D, Datta S, Ackema K, Zerial M and Spang A (2010) Identification of the switch in early-to-late endosome transition. Cell 141 497-508

Prada-Delgado A, Carrasco-Marin E, Bokoch GM and Alvarez-Dominguez C (2001) Interferon-gamma listericidal action is mediated by novel Rab5a functions at the phagosomal environment. J Biol Chem 276 19059-19065

Pryor PR, Mullock BM, Bright NA, Gray SR and Luzio JP (2000) The role of intraorganellar Ca2+ in late endosome-lysosome heterotypic fusion and in the reformation of lysosomes from hybrid organelles. J Cell Biol 149 1053-1062

Rank RG, Whittimore J, Bowlin AK and Wyrick PB (2011) In vivo ultrastructural analysis of the intimate relationship between polymorphonuclear leukocytes and the chlamydial developmental cycle. Infect Immun 79 3291-3301

Redford PS, Murray PJ and O'Garra A (2011) The role of IL-10 in immune regulation during M. tuberculosis infection. Mucosal Immunol 4 261-270

Riggs B, Rothwell W, Mische S, Hickson GR, Matheson J, Hays TS, Gould GW and Sullivan W (2003) Actin cytoskeleton remodeling during early Drosophila furrow formation requires recycling endosomal components Nuclear-fallout and Rab11. J Cell Biol 163 143-154

Rink J, Ghigo E, Kalaidzidis Y and Zerial M (2005) Rab conversion as a mechanism of progression from early to late endosomes. Cell 122 735-749

Roberts EA, Chua J, Kyei GB and Deretic V (2006) Higher order Rab programming in phagolysosome biogenesis. J Cell Biol 174 923-929
Robinson MS, Watts C and Zerial M (1996) Membrane dynamics in endocytosis. Cell 84 13-21

Rubino M, Miaczynska M, Lippé R and Zerial M (2000) Selective membrane recruitment of EEA1 suggests a role in directional transport of clathrin-coated vesicles to early endosomes. J Biol Chem 275 3745-3748

Russell DG, Cardona PJ, Kim MJ, Allain S and Altare F (2009) Foamy macrophages and the progression of the human tuberculosis granuloma. Nat Immunol 10 943-948

Sanger JM and Sanger JW (2012) Insights into cell division using Listeria monocytogenes of PtK2 renal epithelial cells. Cytoskeleton 69 992-999

Sano H, Roach WG, Peck GR, Fukuda M and Lienhard GE (2008) Rab10 in insulin-stimulated GLUT4 translocation. Biochem J 411 89-95

Santic M, Molmere M and Abu Kwaik Y (2005) Maturation of the Legionella pneumophila-containing phagosome into a phagolysosome within gamma interferon-activated macrophages. Infect Immun 73 3166-3171

Schaible UE, Sturgill-Koszycki S, Schlesinger PH and Russell DG (1998) Cytokine activation leads to acidification and increases maturation of Mycobacterium avium-containing phagosomes in murine macrophages. J Immunol 160 1290-1296

Schlesinger LS, Bellinger-Kawahara CG, Payne NR and Horwitz MA (1990) Phagocytosis of Mycobacterium tuberculosis is mediated by human monocyte complement receptors and complement component C3. J Immunol 144 2771-2780

Schlesinger LS (1993) Macrophage phagocytosis of virulent but not attenuated strains of Mycobacterium tuberculosis is mediated by mannose receptors in addition to complement receptors. J Immunol 150 2920-2930

Schlesinger LS, Hull SR and Kaufman TM (1994) Binding of the terminal mannosyl units of lipoarabinomannan from a virulent strain of Mycobacterium tuberculosis to human macrophages. J Immunol 152 4070-4079

Schlesinger LS, Kaufman TM, Iyer S, Hull SR and Marchiando LK (1996) Differences in mannose receptor-mediated uptake of lipoarabinomannan from virulent and attenuated strains of Mycobacterium tuberculosis by human macrophages. J Immunol 157 4568-4575

Schorey JS, Carroll MC and Brown EJ (1997) A macrophage invasion mechanism of pathogenic mycobacteria. Science 277 1091-1093

Schreiber S, Perkins SL, Teitelbaum SL, Chappel J, Stahl PD and Blum JS (1993) Regulation of mouse bone marrow macrophage mannose receptor expression and activation by prostaglandin E and IFN-gamma. J Immunol 151 4973-4981

Schwartz SL, Cao C, Pylypenko O, Rak A and Wandinger-Ness A (2007) Rab GTPases at a glance. J Cell Sci 120 3905-3910

Seto S, Matsumoto S, Ohta I, Tsujimura K and Koide Y (2009) Dissection of Rab7 localization on Mycobacterium tuberculosis phagosome. Biochem Biophys Res Commun 387 272-277

Sheff DR, Daro EA, Hull M and Mellman I (1999) The receptor recycling pathway contains two distinct populations of early endosomes with different sorting functions. J Cell Biol 145 123-139

Shimada K, Takimoto H, Yano I and Kumazawa Y (2006) Involvement of mannose receptor in glycopeptidolipid-mediated inhibition of phagosome-lysosome fusion. Microbiol Immunol 50 243-251

Sibley LD (2013) Invasion and intracellular survival by protozoan parasites. Immunol Rev 240 72-91

Simonsen A, Lippe R, Christoforidis S, Gaullier JM, Brech A, Callaghan J, Toh BH, Murphy C, Zerial M and Stenmark H (1998) EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature 394 494-498

Smith A C, Heo W D, Braun V, Jiang X, Macrae C, Casanova J E, Scidmore M A, Grinstein S, Meyer T and Brumell J H (2007) A network of Rab GTPases controls phagosome maturation and is modulated by Salmonella enterica serovar Typhimurium. J Cell Biol 176 263-268

Stenmark H, Vitale G, Ullrich O and Zerial M (1995) Rabaptin-5 is a direct effector of the small GTPase Rab5 in endocytic membrane fusion. Cell 83 423-432

Sweet L, Singh PP, Azad AK, Rajaram MV, Schlesinger LS and Schorey JS (2010) Mannose receptor-dependent delay in phagosome maturation by Mycobacterium avium glycopeptidolipids. Infect Immun 78 518-526

Tanigawa K, Suzuki K, Nakamura K, Akama T, Kawashima A, Wu H, Hayashi M, Takahashi S, Ikuyama S, Ito T and Ishii N (2008) Expression of adipose differentiation-related protein (ADRP) and perilipin in macrophages infected with Mycobacterium leprae. FEMS Microbiol Lett 289 72-79

Thi EP, Lambertz U and Reiner, NE (2012) Sleeping with the enemy: how intracellular pathogens cope with a macrophage lifestyle. PLoS Pathog 8 e1002551

Torrelles JB, Schlesinger LS (2010) Diversity in Mycobacterium tuberculosis mannosylated cell wall determinants impacts adaptation to the host. Tuberculosis 90 84-93

Torrelles JB, Azad AK and Schlesinger LS (2006) Fine discrimination in the recognition of individual species of phosphatidyl-myo-inositol mannosides from Mycobacterium tuberculosis by C-type lectin pattern recognition receptors. J Immunol 177 1805-1816

Trost M, English L, Lemieux S, Courcelles M, Desjardins M and Thibault P (2009) The phagosomal proteome in interferon-gamma-activated macrophages. Immunity 30 143-154

van der Sluijs P, Hull M, Webster P, Mâle P, Goud B and Mellman I (1992) The small GTP-binding protein rab4 controls an early sorting event on the endocytic pathway. Cell 70 729-740

van Manen HJ, Kraan YM, Roos D and Otto C (2005) Single-cell Raman and fluorescence microscopy reveal the association of lipid bodies with phagosomes in leukocytes. Proc Natl Acad Sci U S A 102 10159-10164

Vergne I, Chua J and Deretic V (2003) Tuberculosis toxin blocking phagosome maturation inhibits a novel Ca2+/calmodulin-PI3K hVPS34 cascade. J Exp Med 198 653-659

Via LE, Deretic D, Ulmer RJ, Hibler NS, Huber LA and Deretic V (1997) Arrest of mycobacterial phagosome maturation is caused by a block in vesicle fusion between stages controlled by rab5 and rab7. J Biol Chem 272 13326-13331

Via LE, Fratti RA, McFalone M, Pagan-Ramos E, Deretic D and Deretic, V (1998) Effects of cytokines on mycobacterial phagosome maturation. J Cell Sci 111 897-905

Vieira OV, Botelho RJ and Grinstein S (2002) Phagosome maturation: aging gracefully. Biochem J 366 689-704

Vinet AF, Fukuda M, Turco SJ and Descoteaux A (2009) The Leishmania donovani lipophosphoglycan excludes the vesicular proton-ATPase from phagosomes by impairing the recruitment of synaptotagmin V. PLoS Pathog 5 e1000628

Wasmeier C, Romao M, Plowright L, Bennett DC, Raposo G and Seabra MC (2006) Rab38 and Rab32 control post-Golgi trafficking of melanogenic enzymes. J Cell Biol 175 271-281

Wright, SD and Silverstein SC (1983) Receptors for C3b and C3bi promote phagocytosis but not the release of toxic oxygen from human phagocytes. J Exp Med 158 2016-2023

Yam PT and Theriot JA (2004) Repeated cycles of rapid actin assembly and disassembly on epithelial cell phagosomes. Mol Biol Cell 15 5647-5658

Yates RM and Russell DG (2005) Phagosome maturation proceeds independently of stimulation of toll-like receptors 2 and 4. Immunity 23 409-417

Yoshimura S, Egerer J, Fuchs E, Haas AK and Barr FA (2007) Functional dissection of Rab GTPases involved in primary cilium formation. J Cell Biol 178 363-369

Zhang J, Tachado SD, Patel N, Zhu J, Imrich A, Manfruelli P, Cushion M, Kinane T B and Koziel H (2005) Negative regulatory role of mannose receptors on human alveolar macrophage proinflammatory cytokine release in vitro. J Leukoc Biol 78 665-674
Published
2017-09-20
Section
Review Articles