The Anaplasma phagocytophilum-occupied vacuole selectively recruits Rab-GTPases that are predominantly associated with recycling endosomes

Cellular Microbiology

Volumn 12, Issue 9, 2010, Pages 1292-1307

  Huang, Bernice ^a   Hubber, Andree ^b   McDonough, Justin A ^b   Roy, Craig R ^b   Scidmore, Marci A ^c   Carlyon, Jason A ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; GREEN FLUORESCENT PROTEIN; GUANOSINE TRIPHOSPHATASE; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; RAB PROTEIN; TETRACYCLINE;

ANAPLASMA PHAGOCYTOPHILUM; ARTICLE; CELL STRAIN HL 60; CELL SURVIVAL; CELL VACUOLE; CELLULAR DISTRIBUTION; ENDOPLASMIC RETICULUM; ENDOSOME; FLUORESCENCE; GOLGI COMPLEX; HOST CELL; INTRACELLULAR BACTERIUM; LYSOSOME; MEMBRANE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; WILD TYPE;

ANAPLASMA PHAGOCYTOPHILUM; BACTERIAL PROTEINS; EHRLICHIOSIS; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENDOSOMES; GOLGI APPARATUS; HL-60 CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; MEMBRANE PROTEINS; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; TETRACYCLINE; VACUOLES;

ANAPLASMA PHAGOCYTOPHILUM; BACTERIA (MICROORGANISMS);

EID: 77955427023     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2010.01468.x     Document Type: Article

References (55)

1. Amigorena S, Drake JR, Webster P, Mellman I. Transient accumulation of new class II MHC molecules in a novel endocytic compartment in B lymphocytes. Nature 1994, 369:113-120.
2. Borjesson DL, Kobayashi SD, Whitney AR, Voyich JM, Argue CM, Deleo FR. Insights into pathogen immune evasion mechanisms: Anaplasma phagocytophilum fails to induce an apoptosis differentiation program in human neutrophils. J Immunol 2005, 174:6364-6372.
3. Brown FD, Rozelle AL, Yin HL, Balla T, Donaldson JG. Phosphatidylinositol 4,5-bisphosphate and Arf6-regulated membrane traffic. J Cell Biol 2001, 154:1007-1017.
4. Brumell JH, Scidmore MA. Manipulation of rab GTPase function by intracellular bacterial pathogens. Microbiol Mol Biol Rev 2007, 71:636-652.
5. Carlyon JA, Abdel-Latif D, Pypaert M, Lacy P, Fikrig E. Anaplasma phagocytophilum utilizes multiple host evasion mechanisms to thwart NADPH oxidase-mediated killing during neutrophil infection. Infect Immun 2004, 72:4772-4783.
6. Chen SM, Dumler JS, Bakken JS, Walker DH. Identification of a granulocytotropic Ehrlichia species as the etiologic agent of human disease. J Clin Microbiol 1994, 32:589-595.
7. Cortes C, Rzomp KA, Tvinnereim A, Scidmore MA, Wizel B. Chlamydia pneumoniae inclusion membrane protein Cpn0585 interacts with multiple Rab GTPases. Infect Immun 2007, 75:5586-5596.
8. Derre I, Isberg RR. Legionella pneumophila replication vacuole formation involves rapid recruitment of proteins of the early secretory system. Infect Immun 2004, 72:3048-3053.
9. Eyster CA, Higginson JD, Huebner R, Porat-Shliom N, Weigert R, Wu WW. Discovery of new cargo proteins that enter cells through clathrin-independent endocytosis. Traffic 2009, 10:590-599.
10. Galan JE. Common themes in the design and function of bacterial effectors. Cell Host Microbe 2009, 5:571-579.
11. Geuze HJ, Stoorvogel W, Strous GJ, Slot JW, Bleekemolen JE, Mellman I. Sorting of mannose 6-phosphate receptors and lysosomal membrane proteins in endocytic vesicles. J Cell Biol 1988, 107:2491-2501.
12. Gokce HI, Ross G, Woldehiwet Z. Inhibition of phagosome-lysosome fusion in ovine polymorphonuclear leucocytes by Ehrlichia (Cytoecetes) phagocytophila. J Comp Pathol 1999, 120:369-381.
13. Grant BD, Donaldson JG. Pathways and mechanisms of endocytic recycling. Nat Rev Mol Cell Biol 2009, 10:597-608.
14. Gutierrez MG, Munafo DB, Beron W, Colombo MI. Rab7 is required for the normal progression of the autophagic pathway in mammalian cells. J Cell Sci 2004, 117:2687-2697.
15. Gutierrez MG, Vazquez CL, Munafo DB, Zoppino FC, Beron W, Rabinovitch M, Colombo MI. Autophagy induction favours the generation and maturation of the Coxiella-replicative vacuoles. Cell Microbiol 2005, 7:981-993.
16. Heuer D, Rejman Lipinski A, Machuy N, Karlas A, Wehrens A, Siedler F. Chlamydia causes fragmentation of the Golgi compartment to ensure reproduction. Nature 2009, 457:731-735.
17. Hotopp JC, Lin M, Madupu R, Crabtree J, Angiuoli SV, Eisen J. Comparative genomics of emerging human ehrlichiosis agents. PLoS Genet 2006, 2:e21.
18. Ijdo JW, Mueller AC. Neutrophil NADPH oxidase is reduced at the Anaplasma phagocytophilum phagosome. Infect Immun 2004, 72:5392-5401.
19. Ijdo JW, Sun W, Zhang Y, Magnarelli LA, Fikrig E. Cloning of the gene encoding the 44-kilodalton antigen of the agent of human granulocytic ehrlichiosis and characterization of the humoral response. Infect Immun 1998, 66:3264-3269.
20. Ingmundson A, Delprato A, Lambright DG, Roy CR. Legionella pneumophila proteins that regulate Rab1 membrane cycling. Nature 2007, 450:365-369.
21. Junutula JR, De Maziere AM, Peden AA, Ervin KE, Advani RJ, van Dijk SM. Rab14 is involved in membrane trafficking between the Golgi complex and endosomes. Mol Biol Cell 2004, 15:2218-2229.
22. Kagan JC, Stein MP, Pypaert M, Roy CR. Legionella subvert the functions of Rab1 and Sec22b to create a replicative organelle. J Exp Med 2004, 199:1201-1211.
23. Kelley VA, Schorey JS. Mycobacterium's arrest of phagosome maturation in macrophages requires Rab5 activity and accessibility to iron. Mol Biol Cell 2003, 14:3366-3377.
24. Kelly EE, Horgan CP, Adams C, Patzer TM, Ni Shuilleabhain DM, Norman JC, McCaffrey MW. Class I Rab11-Family interacting proteins are binding targets for the Rab14 GTPase. Biol Cell 2009, 102:51-62.
25. Kumar Y, Valdivia RH. Leading a sheltered life: intracellular pathogens and maintenance of vacuolar compartments. Cell Host Microbe 2009, 5:593-601.
26. Kyei GB, Vergne I, Chua J, Roberts E, Harris J, Junutula JR, Deretic V. Rab14 is critical for maintenance of Mycobacterium tuberculosis phagosome maturation arrest. EMBO J 2006, 25:5250-5259.
27. Lin M, Rikihisa Y. Ehrlichia chaffeensis and Anaplasma phagocytophilum lack genes for lipid A biosynthesis and incorporate cholesterol for their survival. Infect Immun 2003, 71:5324-5331.
28. Lipinski AR, Heymann J, Meissner C, Karlas A, Brinkmann V, Meyer TF, Heuer D. Rab6 and Rab11 regulate Chlamydia trachomatis development and golgin-84-dependent Golgi fragmentation. PLoS Pathog 2009, 5:e1000615.
29. Machner MP, Isberg RR. Targeting of host Rab GTPase function by the intravacuolar pathogen Legionella pneumophila. Dev Cell 2006, 11:47-56.
30. Mayor S, Pagano RE. Pathways of clathrin-independent endocytosis. Nat Rev Mol Cell Biol 2007, 8:603-612.
31. Moorhead AR, Rzomp KA, Scidmore MA. The Rab6 effector Bicaudal D1 associates with Chlamydia trachomatis inclusions in a biovar-specific manner. Infect Immun 2007, 75:781-791.
32. Mott J, Barnewall RE, Rikihisa Y. Human granulocytic ehrlichiosis agent and Ehrlichia chaffeensis reside in different cytoplasmic compartments in HL-60 cells. Infect Immun 1999, 67:1368-1378.
33. Mott J, Rikihisa Y, Tsunawaki S. Effects of Anaplasma phagocytophila on NADPH oxidase components in human neutrophils and HL-60 cells. Infect Immun 2002, 70:1359-1366.
34. Mukherjee K, Parashuraman S, Raje M, Mukhopadhyay A. SopE acts as an Rab5-specific nucleotide exchange factor and recruits non-prenylated Rab5 on Salmonella-containing phagosomes to promote fusion with early endosomes. J Biol Chem 2001, 276:23607-23615.
35. Murata T, Delprato A, Ingmundson A, Toomre DK, Lambright DG, Roy CR. The Legionella pneumophila effector protein DrrA is a Rab1 guanine nucleotide-exchange factor. Nat Cell Biol 2006, 8:971-977.
36. Neefjes JJ, Stollorz V, Peters PJ, Geuze HJ, Ploegh HL. The biosynthetic pathway of MHC class II but not class I molecules intersects the endocytic route. Cell 1990, 61:171-183.
37. Plutner H, Cox AD, Pind S, Khosravi-Far R, Bourne JR, Schwaninger R. Rab1b regulates vesicular transport between the endoplasmic reticulum and successive Golgi compartments. J Cell Biol 1991, 115:31-43.
38. Radhakrishna H, Donaldson JG. ADP-ribosylation factor 6 regulates a novel plasma membrane recycling pathway. J Cell Biol 1997, 139:49-61.
39. Roberts EA, Chua J, Kyei GB, Deretic V. Higher order Rab programming in phagolysosome biogenesis. J Cell Biol 2006, 174:923-929.
40. Romano PS, Gutierrez MG, Beron W, Rabinovitch M, Colombo MI. The autophagic pathway is actively modulated by phase II Coxiella burnetii to efficiently replicate in the host cell. Cell Microbiol 2007, 9:891-909.
41. Rzomp KA, Scholtes LD, Briggs BJ, Whittaker GR, Scidmore MA. Rab GTPases are recruited to chlamydial inclusions in both a species-dependent and species-independent manner. Infect Immun 2003, 71:5855-5870.
42. Rzomp KA, Moorhead AR, Scidmore MA. The GTPase Rab4 interacts with Chlamydia trachomatis inclusion membrane protein CT229. Infect Immun 2006, 74:5362-5373.
43. Sandvig K, Torgersen ML, Raa HA, van Deurs B. Clathrin-independent endocytosis: from nonexisting to an extreme degree of complexity. Histochem Cell Biol 2008, 129:267-276.
44. Schlumberger MC, Hardt WD. Triggered phagocytosis by Salmonella: bacterial molecular mimicry of RhoGTPase activation/deactivation. Curr Top Microbiol Immunol 2005, 291:29-42.
45. Shaner NC, Lin MZ, McKeown MR, Steinbach PA, Hazelwood KL, Davidson MW, Tsien RY. Improving the photostability of bright monomeric orange and red fluorescent proteins. Nat Methods 2008, 5:545-551.
46. Smith AC, Cirulis JT, Casanova JE, Scidmore MA, Brumell JH. Interaction of the Salmonella-containing vacuole with the endocytic recycling system. J Biol Chem 2005, 280:24634-24641.
47. Smith AC, Heo WD, Braun V, Jiang X, Macrae C, Casanova JE. A network of Rab GTPases controls phagosome maturation and is modulated by Salmonella enterica serovar Typhimurium. J Cell Biol 2007, 176:263-268.
48. Steele-Mortimer O, Meresse S, Gorvel JP, Toh BH, Finlay BB. Biogenesis of Salmonella typhimurium-containing vacuoles in epithelial cells involves interactions with the early endocytic pathway. Cell Microbiol 1999, 1:33-49.
49. Stenmark H. Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 2009, 10:513-525.
50. Thomas RJ, Dumler JS, Carlyon JA. Current management of human granulocytic anaplasmosis, human monocytic ehrlichiosis and Ehrlichia ewingii ehrlichiosis. Expert Rev Anti Infect Ther 2009, 7:709-722.
51. Tisdale EJ, Balch WE. Rab2 is essential for the maturation of pre-Golgi intermediates. J Biol Chem 1996, 271:29372-29379.
52. Troese MJ, Carlyon JA. Anaplasma phagocytophilum dense-cored organisms mediate cellular adherence through recognition of human P-selectin glycoprotein ligand 1. Infect Immun 2009, 77:4018-4027.
53. Via LE, Deretic D, Ulmer RJ, Hibler NS, Huber LA, Deretic V. Arrest of mycobacterial phagosome maturation is caused by a block in vesicle fusion between stages controlled by rab5 and rab7. J Biol Chem 1997, 272:13326-13331.
54. Webster P, IJdo JW, Chicoine LM, Fikrig E. The agent of Human Granulocytic Ehrlichiosis resides in an endosomal compartment. J Clin Invest 1998, 101:1932-1941.
55. Xiong Q, Lin M, Rikihisa Y. Cholesterol-dependent anaplasma phagocytophilum exploits the low-density lipoprotein uptake pathway. PLoS Pathog 2009, 5:e1000329.