Cell biology of Mycobacterium tuberculosis phagosome

Annual Review of Cell and Developmental Biology

Volumn 20, Issue , 2004, Pages 367-394

  Vergne, Isabelle ^a   Chua, Jennifer ^a   Singh, Sudha B ^a   Deretic, Vojo ^a  

^a UNIVERSITY OF NEW MEXICO HEALTH SCIENCES CENTER   (United States)

Author keywords

Calcium; Endosome; Lysosome; Phosphatidylinositol; Rab

Indexed keywords

ACTIN; CALCIUM ION; CALMODULIN; CORD FACTOR; CYTOKINE; GUANINE NUCLEOTIDE BINDING PROTEIN; LIPOARABINOMANNAN; MANNOSIDE; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL; RAB PROTEIN; SULFATIDE; TREHALOSE;

ANTIGEN PRESENTATION; CELL MATURATION; CYTOLOGY; ENZYME INHIBITION; HOMEOSTASIS; LYSOSOME; MEMBRANE FUSION; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; ORGANOGENESIS; PARASITISM; PHAGOCYTOSIS; PHAGOSOME; PRIORITY JOURNAL; REVIEW;

BIOLOGICAL TRANSPORT; CALCIUM; HUMANS; MACROPHAGES; MYCOBACTERIUM TUBERCULOSIS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHAGOCYTOSIS; PHAGOSOMES;

MYCOBACTERIUM; MYCOBACTERIUM TUBERCULOSIS;

EID: 8444225798     PISSN: 10810706     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.cellbio.20.010403.114015     Document Type: Review

References (116)

1. Al-Haddad A, Shonn MA, Redlich B, Blocker A, Burkhardt JK, et al. 2001. Myosin va bound to phagosomes binds to f-actin and delays microtubule- dependent motility. Mol. Biol. Cell 12:2742-55
2. Anes E, Kuhnel MP, Bos E, Moniz-Pereira J, Habermann A, Griffiths G. 2003. Selected lipids activate phagosome actin assembly and maturation resulting in killing of pathogenic mycobacteria. Nat. Cell Biol. 5:793-802
3. Armstrong JA, Hart PD. 1971. Response of cultured macrophages to M. tuberculosis with observations of fusion of lysosomes with phagosomes. J. Exp. Med. 134:713-40
4. Armstrong JA, Hart PD. 1975. Phagosome-lysosome interactions in cultured macrophages infected with virulent tubercle bacilli. Reversal of the usual nonfusion pattern and observations of bacterial survival. J. Exp. Med. 142:1-16
5. Barker LP, George KM, Falkow S, Small PL. 1997. Differential trafficking of live and dead Mycobacterium marinum organisms in macrophages. Infect. Immun. 65:1497-504
6. Beatty WL, Rhoades ER, Ullrich H-J, Chatterjee D, Heuser JE, Russell DG. 2000. Trafficking and release of mycobacterial lipids from infected macrophages. Traffic 1:235-47
7. Blocker A, Severin FF, Burkhardt JK, Bingham JB, Yu H, et al. 1997. Molecular requirements for bi-directional movement of phagosomes along microtubules. J. Cell Biol. 137:113-29
8. Botelho RJ, Teruel M, Dierckman R, Anderson R, Wells A, et al. 2000. Localized biphasic changes in phosphatidylinositol-4,5-bisphosphate at sites of phagocytosis. J. Cell Biol. 151:1353-68
9. Cavalli V, Vilbois F, Corti M, Marcote MJ, Tamura K, et al. 2001. The stress-induced MAP kinase p38 regulates endocytic trafficking via the GDI:Rab5 complex. Mol. Cell 7:421-32
10. Christoforidis S, McBride HM, Burgoyne RD, Zerial M. 1999a. The Rab5 effector EEA1 is a core component of endosome docking. Nature 397:621-5
11. Christoforidis S, Miaczynska M, Ashman K, Wilm M, Zhao L, et al. 1999b. Phosphatidylinositol-3-OH kinases are Rab5 effectors. Nat. Cell Biol. 1:249-52
12. Chua J, Vergne I, Master S, Deretic V. 2004. A tale of two lipids: Mycobacterium tuberculosis phagosome maturation arrest. Curr. Opin. Microbiol. 7:71-77
13. Clemens DL, Horwitz MA. 1995. Characterization of the Mycobacterium tuberculosis phagosome and evidence that phagosomal maturation is inhibited. J. Exp. Med. 181:257-70
14. Clemens DL, Horwitz MA. 1996. The Mycobacterium tuberculosis phagosome interacts with early endosomes and is accessible to exogenously administered transferrin. J. Exp. Med. 184:1349-55
15. Clemens DL, Lee BY, Horwitz MA. 2000a. Deviant expression of rab5 on phagosomes containing the intracellular pathogens Mycobacterium tuberculosis and Legionella pneumophila is associated with altered phagosomal fate. Infect. Immun. 68:2671-84
16. Clemens DL, Lee BY, Horwitz MA. 2000b. Mycobacterium tuberculosis and Legionella pneumophila phagosomes exhibit arrested maturation despite acquisition of Rab7. Infect. Immun. 68:5154-66
17. Clemens DL, Lee BY, Horwitz MA. 2002c. The Mycobacterium tuberculosis phagosome in human macrophages is isolated from the host cell cytoplasm. Infect. Immun. 70:5800-7
18. Crowle A, Dahl R, Ross E, May M. 1991. Evidence that vesicles containing living virulent M. tuberculosis or M. avium in cultured human macrophages are not acidic. Infect. Immun. 59:1823-31
19. Cywes C, Godenir NL, Hoppe HC, Scholle RR, Steyn LM, et al. 1996. Nonopsonic binding of Mycobacterium tuberculosis to human complement receptor type 3 expressed in Chinese hamster ovary cells. Infect. Immun. 64:5373-83
20. Daffe M, Etienne G. 1999. The capsule of Mycobacterium tuberculosis and its implications for pathogenicity. Tuber. Lung. Dis. 79:153-69
21. de Chastellier C, Thilo L. 1997. Phagosome maturation and fusion with lysosomes in relation to surface property and size of the phagocytic particle. Eur. J. Cell Biol. 74:49-62
22. De Cock KM, Soro B, Coulibaly IM, Lucas SB. 1992. Tuberculosis and HIV infection in sub-Saharan Africa. JAMA 268:1581-87
23. Defacque H, Egeberg M, Habermann A, Diakonova M, Roy C, et al. 2000. Involvement of ezrin/moesin in de novo actin assembly on phagosomal membranes. EMBO. J. 19:199-212
24. Diakonova M, Gerke V, Ernst J, Liautard JP, van der Vusse G, Griffiths G. 1997. Localization of five annexins in J774 macrophages and on isolated phagosomes. J. Cell Sci. 110:1199-213
25. Ernst JD. 1998. Macrophage receptors for Mycobacterium tuberculosis. Infect. Immun. 66:1277-81
26. Flynn JL, Chan J. 2003. Immune evasion by Mycobacterium tuberculosis: living with the enemy. Curr. Opin. Immunol. 15:450-55
27. Fratti RA, Backer JM, Gruenberg J, Corvera S, Deretic V. 2001. Role of phosphatidylinositol 3-kinase and Rab5 effectors in phagosomal biogenesis and mycobacterial phagosome maturation arrest. J. Cell Biol. 154:631-44
28. Fratti RA, Chua J, Deretic V. 2002. Cellubrevin alterations and Mycobacterium tuberculosis phagosome maturation arrest. J. Biol. Chem. 277:17320-26
29. Fratti RA, Chua J, Deretic V. 2003a. Induction of p38 mitogen-activated protein kinase reduces EEA1 recruitment to phagosomal membranes. J. Biol. Chem. 278:46961-67
30. Fratti RA, Chua J, Vergne I, Deretic V. 2003b. Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest. Proc. Natl. Acad. Sci. USA 100:5437-42
31. Gagnon E, Duclos S, Rondeau C, Chevet E, Cameron PH, et al. 2002. Endoplasmic reticulum-mediated phagocytosis is a mechanism of entry into macrophages. Cell 110:119-31
32. Garin J, Diez R, Kieffer S, Dermine JF, Duclos S, et al. 2001. The phagosome proteome: insight into phagosome functions. J. Cell Biol. 152:165-80
33. Gatfield J, Pieters J. 2000. Essential role for cholesterol in entry of mycobacteria into macrophages. Science 288:1647-50
34. Gaynor CD, McCormack FX, Voelker DR, McGowan SE, Schlesinger LS. 1995. Pulmonary surfactant protein A mediates enhanced phagocytosis of Mycobacterium tuberculosis by a direct interaction with human macrophages. J. Immunol. 155:5343-51
35. Goren MB, D'Arcy Hart P, Young MR, Armstrong JA. 1976. Prevention of phagosome-lysosome fusion in cultured macrophages by sulfatides of Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 73:2510-14
36. Goren MB, Vatter AE, Fiscus J. 1987. Polyanionic agents as inhibitors of phagosome-lysosome fusion in cultured macrophages: evolution of an alternative interpretation. J. Leukoc. Biol. 41:111-21
37. Guerin I, de Chastellier C. 2000a. Disruption of the actin filament network affects delivery of endocytic contents marker to phagosomes with early endosome characteristics: the case of phagosomes with pathogenic mycobacteria. Eur. J. Cell Biol. 79:735-49
38. Guerin I, de Chastellier C. 2000b. Pathogenic mycobacteria disrupt the macrophage actin filament network. Infect. Immun. 68:2655-62
39. Guermonprez P, Saveanu L, Kleijmeer M, Davoust J, Van Endert P, Amigorena S. 2003. ER-phagosome fusion defines an MHC class I cross-presentation compartment in dendritic cells. Nature 425:397-402
40. Guyader M, Kiyokawa E, Abrami L, Turelli P, Trono D. 2002. Role for human immunodeficiency virus type 1 membrane cholesterol in viral internalization. J. Virol. 76:10356-64
41. Hanekom WA, Mendillo M, Manca C, Haslett PA, Siddiqui MR, et al. 2003. Mycobacterium tuberculosis inhibits maturation of human monocyte-derived dendritic cells in vitro. J. Infect. Dis. 188:257-66
42. Harrison RE, Bucci C, Vieira OV, Schroer TA, Grinstein S. 2003. Phagosomes fuse with late endosomes and/or lysosomes by extension of membrane protrusions along microtubules: role of Rab7 and RILP. Mol. Cell Biol. 23:6494-506
43. Hart PD, Young MR, Gordon AH, Sullivan KH. 1987. Inhibition of phagosome-lysosome fusion in macrophages by certain mycobacteria can be explained by inhibition of lysosomal movements observed after phagocytosis. J. Exp. Med. 166:933
44. Henry RM, Hoppe AD, Joshi N, Swanson JA. 2004. The uniformity of phagosome maturation in macrophages. J. Cell Biol. 164:185-94
45. Hmama Z, Gabathuler R, Jefferies WA, de Jong G, Reiner NE. 1998. Attenuation of HLA-DR expression by mononuclear phagocytes infected with Mycobacterium tuberculosis is related to intracellular sequestration of immature class II heterodimers. J. Immunol. 161:4882-93
46. Indrigo J, Hunter RL Jr, Actor JK. 2003. Cord factor trehalose 6,6′-dimycolate (TDM) mediates trafficking events during mycobacterial infection of murine macrophages. Microbiology 149:2049-59
47. Juffermans NP, Dekkers PE, Peppelenbosch MP, Speelman P, van Deventer SJ, van Der Poll T. 2000. Expression of the chemokine receptors CXCR1 and CXCR2 on granulocytes in human endotoxemia and tuberculosis: involvement of the p38 mitogen-activated protein kinase pathway. J. Infect. Dis. 182:888-94
48. Kang BK, Schlesinger LS. 1998. Characterization of mannose receptor-dependent phagocytosis mediated by Mycobacterium tuberculosis lipoarabinomannan. Infect. Immun. 66:2769-77
49. Karlsson K, Carlsson SR. 1998. Sorting of lysosomal membrane glycoproteins lamp-1 and lamp-2 into vesicles distinct from mannose 6-phosphate receptor/gamma-adaptin vesicles at the trans-Golgi network. J. Biol. Chem. 273:18966-73
50. Katzmann DJ, Odorizzi G, Emr SD. 2002. Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell Biol. 3:893-905
51. Kelley VA, Schorey JS. 2003. Mycobacterium's arrest of phagosome maturation in macrophages requires Rab5 activity and accessibility to iron. Mol. Biol. Cell 14:3366-77
52. Kincaid EZ, Ernst JD. 2003. Mycobacterium tuberculosis exerts gene-selective inhibition of transcriptional responses to IFN-gamma without inhibiting STAT1 function. J. Immunol. 171:2042-49
53. Knutson KL, Hmama Z, Herrera-Velit P, Rochford R, Reiner NE. 1998. Lipoarabinomannan of Mycobacterium tuberculosis promotes protein tyrosine dephosphorylation and inhibition of mitogen-activated protein kinase in human mononuclear phagocytes. Role of the Src homology 2 containing tyrosine phosphatase 1. J. Biol. Chem. 273:645-52
54. Le Cabec V, Cols C, Maridonneau-Parini I. 2000. Nonopsonic phagocytosis of zymosan and Mycobacterium kansasii by CR3 (CD11b/CD18) involves distinct molecular determinants and is or is not coupled with NADPH oxidase activation. Infect. Immun. 68:4736-45
55. Lee RE, Brennan PJ, Besra GS. 1996. Mycobacterium tuberculosis cell envelope. Curr. Top. Microbiol. Immunol. 215:1-27
56. Lopez JP, Clark E, Shepherd VL. 2003. Surfactant protein A enhances Mycobacterium avium ingestion but not killing by rat macrophages. J. Leukoc. Biol. 74:523-30
57. MacMicking JD, Taylor GA, McKinney JD. 2003. Immune control of tuberculosis by IFN-gamma-inducible LRG-47. Science 302:654-59
58. 2+ signaling by Mycobacterium tuberculosis is associated with reduced phagosome-lysosome fusion and increased survival within human macrophages. J. Exp. Med. 191:287-302
59. Malik ZA, Iyer SS, Kusner DJ. 2001. Mycobacterium tuberculosis phagosomes exhibit altered calmodulin-dependent signal transduction: contribution to inhibition of phagosome-lysosome fusion and intracellular survival in human macrophages. J. Immunol. 166:3392-401
60. 2+ signaling and phagosome maturation in human macrophages via specific inhibition of sphingosine kinase. J. Immunol. 170:2811-15
61. Maniak M, Rauchenberger R, Albrecht R, Murphy J, Gerisch G. 1995. Coronin involved in phagocytosis: dynamics of particle-induced relocalization visualized by a green fluorescent protein Tag. Cell 83:915-24
62. Marshall JG, Booth JW, Stambolic V, Mak T, Balla T, et al. 2001. Restricted accumulation of phosphatidylinositol 3-kinase products in a plasmalemmal subdomain during Fc gamma receptor-mediated phagocytosis. J. Cell Biol. 153:1369-80
63. McDonough KA, Kress Y, Bloom BR. 1993. Pathogenesis of tuberculosis: interaction of Mycobacterium tuberculosis with macrophages. Infect. Immun. 61:2763-73
64. Miller BH, Fratti RA, Poschet JF, Master S, Timmins G, et al. 2004. Mycobacteria inhibit nitric oxide synthase recruitment to phagosomes during macrophage infection. Infect. Immun. 72:2872-78
65. Moreira AL, Wang J, Tsenova-Berkova L, Hellmann W, Freedman VH, Kaplan G. 1997. Sequestration of Mycobacterium tuberculosis in tight vacuoles in vivo in lung macrophages of mice infected by the respiratory route. Infect. Immun. 65:305-8
66. Mustafa T, Phyu S, Nilsen R, Bjune G, Jonsson R. 1999. Increased expression of Fas ligand on Mycobacterium tuberculosis infected macrophages: a potential novel mechanism of immune evasion by Mycobacterium tuberculosis? Inflammation 23:507-21
67. Mwandumba HC, Russell DG, Nyirenda MH, Anderson J, White SA, et al. 2004. Mycobacterium tuberculosis resides in non-acidified vacuoles in endocytically competent alveolar macrophages from patients with tuberculosis and HIV-infection. J. Immunol. 172:4592-98
68. Niedergang F, Colucci-Guyon E, Dubois T, Raposo G, Chavrier P. 2003. ADP ribosylation factor 6 is activated and controls membrane delivery during phagocytosis in macrophages. J. Cell Biol. 161:1143-50
69. Oh Y-K, Starubinger RM. 1996. Intracellular fate of Mycobacterium avium: use of dual-label spectrofluorometry to investigate the influence of bacterial viability and opsonization on phagosomal pH and phagosome-lysosome interaction. Infect. Immun. 64:319-25
70. Ono M, Okada H, Holland S, Yanagi S, Kurosaki T, Ravetch JV. 1997. Deletion of SHIP or SHP-1 reveals two distinct pathways for inhibitory signaling. Cell 90:293-301
71. Pancholi P, Mirza A, Bhardwaj N, Steinman RM. 1993. Sequestration from immune CD4+ T cells of mycobacteria growing in human macrophages. Science 260:984-86
72. Pelchen-Matthews A, Kramer B, Marsh M. 2003. Infectious HIV-1 assembles in late endosomes in primary macrophages. J. Cell Biol. 162:443-55
73. Perskvist N, Zheng L, Stendahl O. 2000. Activation of human neutrophils by Mycobacterium tuberculosis H37Ra involves phospholipase C gamma 2, Shc adapter protein, and p38 mitogen-activated protein kinase. J. Immunol. 164:959-65
74. Peterson PK, Gekker G, Hu S, Sheng WS, Anderson WR, et al. 1995. CD14 receptor-mediated uptake of nonopsonized Mycobacterium tuberculosis by human microglia. Infect. Immun. 63:1598-602
75. Peyron P, Bordier C, N'Diaye EN, Maridonneau-Parini I. 2000. Nonopsonic phagocytosis of Mycobacterium kansasii by human neutrophils depends on cholesterol and is mediated by CR3 associated with glycosylphosphatidylinositol- anchored proteins. J. Immunol. 165:5186-91
76. Pieters J. 2001. Entry and survival of pathogenic mycobacteria in macrophages. Microbes Infect. 3:249-55
77. Pieters J, Gatfield J. 2002. Hijacking the host: survival of pathogenic mycobacteria inside macrophages. Trends Microbiol. 10:142-46
78. Pittis MG, Muzzolin L, Giulianini PG, Garcia RC. 2003. Mycobacteria-containing phagosomes associate less annexins I, VI, VII and XI, but not II, concomitantly with a diminished phagolysosomal fusion. Eur. J. Cell Biol. 82:9-17
79. 2+-dependent cell signaling. J. Infect. Dis. 182:240-51
80. Rousseau C, Turner OC, Rush E, Bordat Y, Sirakova TD, et al. 2003. Sulfolipid deficiency does not affect the virulence of Mycobacterium tuberculosis H37Rv in mice and guinea pigs. Infect. Immun. 71:4684-90
81. Russell DG, Dant J, Sturgill-Koszycki S. 1996. Mycobacterium avium- and Mycobacterium tuberculosis-containing vacuoles are dynamic, fusion-competent vesicles that are accessible to glycosphingolipids from the host cell plasmalemma. J. Immunol. 156:4764-73
82. Russell DG, Mwandumba HC, Rhoades EE. 2002. Mycobacterium and the coat of many lipids. J. Cell Biol. 158:421-26
83. Schaible UE, Collins HL, Priem F, Kaufmann SH. 2002. Correction of the iron overload defect in beta-2-microglobulin knockout mice by lactoferrin abolishes their increased susceptibility to tuberculosis. J. Exp. Med. 196:1507-13
84. Schaible UE, Hagens K, Fischer K, Collins HL, Kaufmann SH. 2000. Intersection of group I CD1 molecules and mycobacteria in different intracellular compartments of dendritic cells. J. Immunol. 164:4843-52
85. Schaible UE, Sturgill-Koszycki S, Schlesinger PH, Russell DG. 1998. Cytokine activation leads to acidification and increases maturation of Mycobacterium avium-containing phagosomes in murine macrophages. J. Immunol. 160:1290-96
86. 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. 150:2920-30
87. Schorey JS, Carroll MC, Brown EJ. 1997. A macrophage invasion mechanism of pathogenic mycobacteria. Science 277:1091-93
88. Schuller S, Neefjes J, Ottenhoff T, Thole J, Young D. 2001. Coronin is involved in uptake of Mycobacterium bovis BCG in human macrophages but not in phagosome maintenance. Cell. Microbiol. 3:785-93
89. 3K function to Rab5 regulation of endosome fusion. Nature 394:494-98
90. Solomon JM, Leung GS, Isberg RR. 2003. Intracellular replication of Mycobacterium marinum within Dictyostelium discoideum: efficient replication in the absence of host coronin. Infect. Immun. 71:3578-86
91. Spargo BJ, Crowe LM, Ioneda T, Beaman BL, Crowe JH. 1991. Cord factor (alpha,alpha-trehalose 6,6′-dimycolate) inhibits fusion between phospholipid vesicles. Proc. Natl. Acad. Sci. USA 88:737-40
92. Stamm LM, Morisaki JH, Gao LY, Jeng RL, McDonald KL, et al. 2003. Mycobacterium marinum escapes from phagosomes and is propelled by actin-based motility. J. Exp. Med. 198:1361-68
93. Stenger S, Niazi KR, Modlin RL. 1998. Downregulation of CD1 on antigen-presenting cells by infection with Mycobacterium tuberculosis. J. Immunol. 161:3582-88
94. Stober CB, Lammas DA, Li CM, Kumararatne DS, Lightman SL, McArdle CA. 2001. ATP-mediated killing of Mycobacterium bovis bacille Calmette-Guerin within human macrophages is calcium dependent and associated with the acidification of mycobacteria-containing phagosomes. J. Immunol. 166:6276-86
95. Strack B, Calistri A, Craig S, Popova E, Gottlinger HG. 2003. AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding. Cell 114:689-99
96. Sturgill-Koszycki S, Schaible UE, Russell DG. 1996. Mycobacterium- containing phagosomes are accessible to early endosomes and reflect a transitional state in normal phagosome biogenesis. EMBO J. 15:6960-68
97. Sturgill-Koszycki S, Schlesinger PH, Chakraborty P, Haddix PL, Collins HL, et al. 1994a. Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 263:678-81
98. Tailleux L, Neyrolles O, Honore-Bouakline S, Perret E, Sanchez F, et al. 2003. Constrained intracellular survival of Mycobacterium tuberculosis in human dendritic cells. J. Immunol. 170:1939-48
99. Teis D, Huber LA. 2003. The odd couple: signal transduction and endocytosis. Cell. Mol. Life Sci. 60:2020-33
100. Teitelbaum R, Cammer M, Maitland ML, Freitag NE, Condeelis J, Bloom BR. 1999. Mycobacterial infection of macrophages results in membrane-permeable phagosomes. Proc. Natl. Acad. Sci. USA 96:15190-95
101. Ting LM, Kim AC, Cattamanchi A, Ernst JD. 1999. Mycobacterium tuberculosis inhibits IFN-gamma transcriptional responses without inhibiting activation of STAT1. J. Immunol. 163:3898-906
102. Tse HM, Josephy SI, Chan ED, Fouts D, Cooper AM. 2002. Activation of the mitogen-activated protein kinase signaling pathway is instrumental in determining the ability of Mycobacterium avium to grow in murine macrophages. J. Immunol. 168:825-33
103. Ullrich HJ, Beatty WL, Russell DG. 1999. Direct delivery of procathepsin D to phagosomes: implications for phagosome biogenesis and parasitism by Mycobacterium. Eur. J. Cell Biol. 78:739-48
104. Ullrich HJ, Beatty WL, Russell DG. 2000. Interaction of Mycobacterium avium-containing phagosomes with the antigen presentation pathway. J. Immunol. 165:6073-80
105. Underhill DM, Ozinsky A, Hajjar AM, Stevens A, Wilson CB, et al. 1999. The Toll-like receptor 2 is recruited to macrophage phagosomes and discriminates between pathogens. Nature 401:811-15
106. Vercellone A, Nigou J, Puzo G. 1998. Relationships between the structure and the roles of lipoarabinomannans and related glycoconjugates in tuberculosis pathogenesis. Front Biosci. 3:e149-63
107. 2+/calmodulin-PI3K hVPS34 ascade. J. Exp. Med. 198:653-59
108. Vergne I, Fratti RA, Hill PJ, Chua J, Belisle J, Deretic V. 2004. Mycobacterium tuberculosis phagosome maturation arrest: mycobacterial phosphatidylinositol analog phosphatidylinositol mannoside stimulates early endosomal fusion. Mol. Biol. Cell 15:751-60
109. Via LE, Deretic D, Ulmer RJ, Hibler NS, Huber LA, 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. 272:13326-31
110. Via LE, Fratti RA, McFalone M, Pagan-Ramos E, Deretic D, Deretic V. 1998. Effects of cytokines on mycobacterial phagosome maturation. J Cell Sci. 111:897-905
111. Vieira OV, Botelho RJ, Grinstein S. 2002. Phagosome maturation: aging gracefully. Biochem. J. 366:689-704
112. Vieira OV, Botelho RJ, Rameh L, Brachmann SM, Matsuo T, et al. 2001. Distinct roles of class I and class III phosphatidylinositol 3-kinase in phagosome formation and maturation. J. Cell Biol. 155:19-25
113. Weikert LF, Edwards K, Chroneos ZC, Hager C, Hoffman L, Shepherd VL. 1997. SP-A enhances uptake of bacillus Calmette-Guerin by macrophages through a specific SP-A receptor. Am. J. Physiol. Lung Cell Mol. Physiol. 272:L989-95
114. Xu S, Cooper A, Sturgill-Koszycki S, van Heyningen T, Chatterjee D, et al. 1994. Intracellular trafficking in Mycobacterium tuberculosis and Mycobacterium avium-infected macrophages. J. Immunol. 153:2568-78
115. Zimmerli S, Edwards S, Ernst JD. 1996a. Selective receptor blockade during phagocytosis does not alter the survival and growth of Mycobacterium tuberculosis in human macrophages. Am. J. Respir. Cell Mol. Biol. 15:760-70
116. Zimmerli S, Majeed M, Gustavsson M, Stenahl O, Sanan DA, Ernst JD. 1996b. Phagosome-lysosome fusion is a calcium-independent event in macrophages. J. Cell Biol. 132:49-61