Modulation of Rab5 and Rab7 recruitment to phagosomes by phosphatidylinositol 3-kinase

Molecular and Cellular Biology

Volumn 23, Issue 7, 2003, Pages 2501-2514

  Vieira, Otilia V ^a   Bucci, Cecilia ^b   Harrison, Rene E ^a   Trimble, William S ^a   Lanzetti, Letizia ^c   Gruenberg, Jean ^d   Schreiber, Alan D ^e   Stahl, Philip D ^f   Grinstein, Sergio ^a  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF SALENTO   (Italy)

^c EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

^d UNIVERSITY OF GENEVA   (Switzerland)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

^f WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; RAB PROTEIN; WORTMANNIN;

ANIMAL CELL; ANTIGEN BINDING; ANTIGEN PRESENTATION; ARTICLE; BIOGENESIS; BLEACHING; CELL FUSION; CELL MATURATION; CONTROLLED STUDY; ENDOSOME; ENZYME ACTIVITY; ENZYME INHIBITION; LEUKOCYTE; LYSOSOME; MICROBIAL DEGRADATION; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PHAGOCYTE; PHAGOSOME; PRIORITY JOURNAL;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANDROSTADIENES; ANIMALS; CARRIER PROTEINS; CELL LINE; CHO CELLS; CRICETINAE; ENZYME ACTIVATION; ENZYME INHIBITORS; FEMALE; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GREEN FLUORESCENT PROTEINS; LUMINESCENT PROTEINS; MACROPHAGES; MEMBRANE FUSION; MICE; ONCOGENE PROTEINS, FUSION; OVARY; PHAGOSOMES; PROTEIN BINDING; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; RAB5 GTP-BINDING PROTEINS; RECOMBINANT FUSION PROTEINS; TRANSFECTION;

ANIMALIA;

EID: 0037378608     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.7.2501-2514.2003     Document Type: Article

References (40)

1. Aderem, A., and D. M. Underhill. 1999. Mechanisms of phagocytosis in macrophages. Annu. Rev. Immunol. 17:593-623.
2. Alvarez-Dominguez, C., A. M. Barbieri, W. Beron, A. Wandinger-Ness, and P. D. Stahl. 1996. Phagocytosed live. Listeria monocytogenes influences Rab5-regulated in vitro phagosome-endosome fusion. J. Biol. Chem. 271:13834-13843.
3. Alvarez-Dominguez, C., and P. D. Stahl. 1998. Interferon-gamma selectively induces Rab5a synthesis and processing in mononuclear cells. J. Biol. Chem. 273:33901-33904.
4. Araki, N., M. T. Johnson, and J. A. Swanson. 1996. A role for phosphoinositide 3-kinase in the completion of macropinocytosis and phagocytosis by macrophages. J. Cell Biol. 135:1249-1260.
5. Bucci, C., R. G. Parton, I. H. Mather, H. Stunnenberg, K. Simons, B. Hoflack, and M. Zerial. 1992. The small, GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 70:715-728.
6. Bucci, C., P. Thomsen, P. Nicoziani, J. McCarthy, and B. van Deurs. 2000. Rab7: a key to lysosome biogenesis. Mol. Biol. Cell 11:467-480.
7. Callaghan, J., A. Simonsen, J. M. Gaullier, B. H. Toh, and H. Stenmark. 1999. The endosome fusion regulator early-endosomal autoantigen 1 (EEA1) is a dimer. Biochem J. 338:539-543.
8. Cantalupo, G., P. Alifano, V. Roberti, C. B. Bruni, and C. Bucci. 2001. Rab-interacting lysosomal protein (RILP): the Rab7 effector required for transport to lysosomes. EMBO J. 20:683-693.
9. Cheever, M. L., T. K. Sato, T. de Beer, T. G. Kutateladze, S. D. Emr, and M. Overduin. 2001. Phox domain interaction with PtdIns(3)P targets the Vam7 t-SNARE to vacuole membranes. Nat. Cell Biol. 3:613-618.
10. Chen, X., and Z. Wang. 2001. Regulation of epidermal growth factor receptor endocytosis by wortmannin through activation of Rab5 rather than inhibition of phosphatidylinositol 3-kinase. EMBO Rep. 2:842-849.
11. a. Collins, R. F., A. D. Schreiber, S. Grinstein, and W. S. Trimble. 2002. Syntaxins 13 and 7 function at distinct steps during phagocytosis. J. Immunol. 169:3250-3256.
12. Cox, D., C. C. Tseng, G. Bjekic, and S. Greenberg. 1999. A requirement for phosphatidylinositol 3-kinase in pseudopod extension. J. Biol. Chem. 274:1240-1247.
13. Desjardins, M., J. E. Celis, G. van Meer, H. Dieplinger, A. Jahraus, G. Griffiths, and L. A. Huber. 1994. Molecular characterization of phagosomes. J. Biol. Chem. 269:32194-32200.
14. Desjardins, M., L. A. Huber, R. G. Parton, and G. Griffiths. 1994. Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus. J. Cell Biol. 124:677-688.
15. Downey, G. P., R. J. Botelho, J. R. Butler, Y. Moltyaner, P. Chien, A. D. Schreiber, and S. Grinstein. 1999. Phagosomal maturation, acidification, and inhibition of bacterial growth in nonphagocytic cells transfected with FcγRIIA receptors. J. Biol. Chem. 274:28436-28444.
16. Duclos, S., R. Diez, J. Garin, B. Papadopoulou, A. Descoteaux, H. Stenmark, and M. Desjardins. 2000. Rab5 regulates the kiss and run fusion between phagosomes and endosomes and the acquisition of phagosome leishmanicidal properties in RAW 264.7 macrophages. J Cell Sci. 113:3531-3541.
17. Fratti, R. A., J. M. Backer, J. Gruenberg, S. Corvera, and V. Deretic. 2001. Role of phosphatidylinositol 3-kinase and Rab5 effectors in phagosomal biogenesis and mycobacterial phagosome maturation arrest. J. Cell Biol. 154:631-644.
18. Garin, J., R. Diez, S. Kieffer, J. F. Dermine, S. Duclos, E. Gagnon, R. Sadoul, C. Rondeau, and M. Desjardins. 2001. The phagosome proteome: insight into phagosome functions. J. Cell Biol. 152:165-180.
19. Gorvel, J. P., P. Chavrier, M. Zerial, and J. Gruenberg. 1991. rab5 controls early endosome fusion in vitro. Cell 64:915-925.
20. Indik, Z. K., J. G. Park, S. Hunter, and A. D. Schreiber. 1995. The molecular dissection of Fc gamma receptor mediated phagocytosis. Blood 86:4389-4399.
21. Jahraus, A., T. E. Tjelle, T. Berg, A. Habermann, B. Storrie, O. Ullrich, and G. Griffiths. 1998. In vitro fusion of phagosomes with different endocytic organelles from J774 macrophages. J. Biol. Chem. 273:30379-30390.
22. Jordens, I., M. Fernandez-Borja, M. Marsman, S. Dusseljee, L. Janssen, J. Calafat, H. Janssen, R. Wubbolts, and J. Neefjes. 2001. The Rab7 effector protein RILP controls lysosomal transport by inducing the recruitment of dynein-dynactin motors. Curr. Biol. 11:1680-1685.
23. Kobayashi, T, F. Gu, and J. Gruenberg. 1998. Lipids, lipid domains and lipid-protein interactions in endocytic membrane traffic. Semin. Cell. Dev. Biol. 9:517-526.
24. Kobayashi, T., M. H. Beuchat, M. Lindsay, S. Frias, R. D. Palmiter, H. Sakuraba, R. G. Parton, and J. Gruenberg. 1999. Late endosomal membranes rich in lysobisphosphatidic acid regulate cholesterol transport. Nat. Cell Biol. 1:113-118.
25. Lanzetti, L., V. Rybin, M. G. Malabarba, S. Christoforidis, G. Scita, M. Zerial, and P. P. Di Fiore. 2000. The Eps8 protein coordinates EGF receptor signalling through. Rac and trafficking through Rab5. Nature 408:374-377.
26. Li, G., C. D'Souza-Schorey, M. A. Barbieri, J. A. Cooper, and P. D. Stahl. 1997. Uncoupling of membrane ruffling and pinocytosis during Ras signal transduction. J. Biol. Chem. 272:10337-10340.
27. Li, G., M. A. Barbieri, M. I. Colombo, and P. D. Stahl. 1994. Structural features of the GTP-binding defective Rab5 mutants required for their inhibitory activity on endocytosis. J. Biol. Chem. 269:14631-14635.
28. Liu, K., and G. Li. 1998. Catalytic domain of the p120 Ras GAP binds to RAb5 and stimulates its GTPase activity. J. Biol. Chem. 273:10087-10090.
29. McBride, H. M., V. Rybin, C. Murphy, A. Giner, R. Teasdale, and M. Zerial. 1999. Oligomeric complexes link Rab5 effectors with NSF and drive membrane fusion via interactions between EEA1 and syntaxin 13. Cell 98:377-386.
30. Nielsen, E., S. Christoforidis, S. Uttenweiler-Joseph, M. Miaczynska, F. Dewitte, M. Wilm, B. Hoflack, and M. Zerial. 2000. Rabenosyn-5, a novel Rab5 effector, is complexed with hVPS45 and recruited to endosomes through a FYVE finger domain. J Cell Biol. 151:601-612.
31. Patki, V., J. Virbasius, W. S. Lane, B. H. Toh, H. S. Shpetner, and S. Corvera. 1997. Identification of an early endosomal protein regulated by phosphatidylinositol 3-kinase. Proc. Natl. Acad. Sci. USA 94:7326-7330.
32. Roberts, R. L., M. A. Barbieri, J. Ullrich, and P. D. Stahl. 2000. Dynamics of rab5 activation in endocytosis and phagocytosis. J. Leukoc. Biol. 68:627-632.
33. Roberts, R. L., M. A. Barbieri, K. M. Pryse, M. Chua, J. H. Morisaki, and P. D. Stahl. 1999. Endosome fusion in living cells overexpressing GFP-rab5. J. Cell Sci. 112:3667-3675.
34. Scott, C. C., P. Cuellar-Mata, T. Matsuo, H. W. Davidson, and S. Grinstein. 2002. Role of 3-phosphoinositides in the maturation of Salmonella-containing vacuoles within host cells. J. Biol. Chem. 277:12770-12776.
35. Simonsen, A., R. Lippe, S. Christoforidis, J. M. Gaullier, A. Brech, J. Callaghan, B. H. Toh, C. Murphy, M. Zerial, and H. Stenmark. 1998. EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature 394:494-498.
36. Tall, G. G., M. A. Barbieri, P. D. Stahl, and B. F. Horazdovsky. 2001. Ras-activated endocytosis is mediated by the Rab5 guanine nucleotide exchange activity of RIN1. Dev. Cell 1:73-82.
37. Underhill, D. M., and A. Ozinsky. 2002. Phagocytosis of microbes: complexity in action. Annu. Rev. Immunol. 20:825-852.
38. Vieira, O. V., R. J. Botelho, L. Rameh, S. M. Brachmann, T, Matsu, H. W. Davidson, A. Schreiber, J. M. Backer, L. C. Cantley, and S. Grinstein. 2001. Distinct roles of class I and class III phosphatidylinositol 3-kinases in phagosome formation and maturation. J. Cell Biol. 155:19-25.
39. Xiao, G. H., F. Shoarinejad, F. Jin, E. A. Golemis, and R. S. Yeung. 1997. The tuberous sclerosis 2 gene product, tuberin, functions as a Rab5 GTPase activating protein (GAP) in modulating endocytosis. J. Biol. Chem. 272:6097-6100.
40. Zerial, M., and H. McBride. 2001. Rab proteins as membrane organizers. Nat. Rev. Mol. Cell. Biol. 2:107-117.