Rac and Rab GTPases dual effector Nischarin regulates vesicle maturation to facilitate survival of intracellular bacteria

EMBO Journal

Volumn 32, Issue 5, 2013, Pages 713-727

  Kuijl, Coenraad ^a   Pilli, Manohar ^a,b   Alahari, Suresh K ^c   Janssen, Hans ^d   Khoo, Poh Sim ^a   Ervin, Karen E ^a   Calero, Monica ^a   Jonnalagadda, Sobhanaditya ^b   Scheller, Richard H ^a   Neefjes, Jacques ^d   Junutula, Jagath R ^a  

^a GENENTECH INC   (United States)

^b OSMANIA UNIVERSITY   (India)

^c LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

Nischarin; Rab14; Rab9; Rac1; Salmonella

Indexed keywords

NISCHARIN; PROTEIN; RAB PROTEIN; RAB14 PROTEIN; RAB9 PROTEIN; RAC1 PROTEIN; UNCLASSIFIED DRUG;

ACIDIFICATION; BACTERIAL SURVIVAL; CELL MATURATION; CELL VACUOLE; CONTROLLED STUDY; ENDOSOME; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REVIEW; SALMONELLA;

BIOLOGICAL TRANSPORT; BLOTTING, WESTERN; ENDOSOMES; GUANOSINE TRIPHOSPHATE; HELA CELLS; HUMANS; IMIDAZOLINE RECEPTORS; IMMUNOPRECIPITATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LYSOSOMES; PHOSPHATIDYLINOSITOL PHOSPHATES; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; RAC GTP-BINDING PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM; TWO-HYBRID SYSTEM TECHNIQUES; VACUOLES;

BACTERIA (MICROORGANISMS); SALMONELLA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; STRAWBERRY CRINKLE VIRUS;

EID: 84875211797     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2013.10     Document Type: Review

References (63)

1. Alahari SK, Nasrallah H (2004) A membrane proximal region of the integrin alpha5 subunit is important for its interaction with nischarin. Biochem J 377: 449-457
2. Alahari SK, Reddig PJ, Juliano RL (2004) The integrin-binding protein Nischarin regulates cell migration by inhibiting PAK. EMBO J 23: 2777-2788
3. Bakowski MA, Braun V, Lam GY, Yeung T, Heo WD, Meyer T, Finlay BB, Grinstein S, Brumell JH (2011) The phosphoinositide phosphatase SopB manipulates membrane surface charge and trafficking of the salmonella-containing vacuole. Cell Host Microbe 7: 453-462
4. Baust T, Czupalla C, Krause E, Bourel-Bonnet L, Hoflack B (2006) Proteomic analysis of adaptor protein 1A coats selectively assembled on liposomes. Proc Natl Acad Sci USA 103: 3159-3164
5. Beuzón CR, Banks G, Deiwick J, Hensel M, Holden DW (1999) pH-dependent secretion of SseB, a product of the SPI-2 type III secretion system of Salmonella typhimurium. Mol Microbiol 33: 806-816
6. Brumell JH, Scidmore MA (2007) Manipulation of rab GTPase function by intracellular bacterial pathogens. Microbiol Mol Biol Rev 71: 636-652
7. Bueno SM, González PA, Carreño LJ, Tobar JA, Mora GC, Pereda CJ, Salazar-Onfray F, Kalergis AM (2008) The capacity of Salmonella to survive inside dendritic cells and prevent antigen presentation to T cells is host specific. Immunology 124: 522-533
8. Carpenter AE, Jones TR, Lamprecht MR, Clarke C, Kang IH, Friman O, Guertin DA, Chang JH, Lindquist RA, Moffat J, Golland P, Sabatini DM (2006) CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol 7: R100.
9. Chen LM, Bagrodia S, Cerione RA, Galán JE (1999) Requirement of p21-activated kinase (PAK) for Salmonella typhimurium-induced nuclear responses. J Exp Med 189: 1479-1488
10. Christoforidis S, Miaczynska M, Ashman K, Wilm M, Zhao L, Yip SC, Waterfield MD, Backer JM, Zerial M (1999) Phosphatidylinositol-3-OH kinases are Rab5 effectors. Nat Cell Biol 1: 249-252
11. Cormack BP, Valdivia RH, Falkow S (1996) FACS-optimized mutants of the green fluorescent protein (GFP). Gene 173: 33-38
12. Darie CC, Deinhardt K, Zhang G, Cardasis HS, Chao MV, Neubert TA (2011) Identifying transient protein-protein interactions in EphB2 signaling by Blue Native PAGE and Mass Spectrometry. Proteomics 11: 4514-4528
13. Drecktrah D, Knodler LA, Howe D, Steele-Mortimer O (2007) Salmonella trafficking is defined by continuous dynamic interactions with the endolysosomal system. Traffic 8: 212-225
14. Eathiraj S, Pan X, Ritacco C, Lambright DG (2005) Structural basis of family-wide Rab GTPase recognition by rabenosyn-5. Nature 436: 415-419
15. Ganley IG, Carroll K, Bittova L, Pfeffer S (2004) Rab9 GTPase regulates late endosome size and requires effector interaction for its stability. Mol Biol Cell 15: 5420-5430
16. Garcia-del Portillo F, Finlay BB (1995) Targeting of Salmonella typhimurium to vesicles containing lysosomal membrane glycoproteins bypasses compartments with mannose 6-phosphate receptors. J Cell Biol 129: 81-97
17. Garcia-del Portillo F, Zwick MB, Leung KY, Finlay BB (1993) Intracellular replication of Salmonella within epithelial cells is associated with filamentous structures containing lysosomal membrane glycoproteins. Infect Agents Dis 2: 227-231
18. Haraga A, Ohlson MB, Miller SI (2008) Salmonellae interplay with host cells. Nat Rev Microbiol 6: 53-66
19. Hardt WD, Chen LM, Schuebel KE, Bustelo XR, Galán JE (1998) S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 93: 815-826
20. Hensel M, Shea JE, Waterman SR, Mundy R, Nikolaus T, Banks G, Vazquez-Torres A, Gleeson C, Fang FC, Holden DW (1998) Genes encoding putative effector proteins of the type III secretion system of Salmonella pathogenicity island 2 are required for bacterial virulence and proliferation in macrophages. Mol Microbiol 30: 163-174
21. Hernandez LD, Hueffer K, Wenk MR, Galán JE (2004) Salmonella modulates vesicular traffic by altering phosphoinositide metabolism. Science 304: 1805-1807
22. Jefferies HBJ, Cooke FT, Jat P, Boucheron C, Koizumi T, Hayakawa M, Kaizawa H, Ohishi T, Workman P, Waterfield MD, Parker PJ (2008) A selective PIKfyve inhibitor blocks PtdIns(3,5)P(2) production and disrupts endomembrane transport and retroviral budding. EMBO Rep 9: 164-170
23. Jones BD, Ghori N, Falkow S (1994) Salmonella typhimurium initiates murine infection by penetrating and destroying the specialized epithelial M cells of the Peyer's patches. J Exp Med 180: 15-23
24. Jordens I, Fernandez-Borja M, Marsman M, Dusseljee S, Janssen L, Calafat J, Janssen H, Wubbolts R, Neefjes J (2001) The Rab7 effector protein RILP controls lysosomal transport by inducing the recruitment of dynein-dynactin motors. Curr Biol 11: 1680-1685
25. Junutula JR, De Maziére AM, Peden AA, Ervin KE, Advani RJ, van Dijk SM, Klumperman J, Scheller RH (2004) Rab14 is involved in membrane trafficking between the Golgi complex and endosomes. Mol Biol Cell 15: 2218-2229
26. Jäger D, Stockert E, Jäger E, Güre AO, Scanlan MJ, Knuth A, Old LJ, Chen YT (2000) Serological cloning of a melanocyte rab guanosine 5'-triphosphate-binding protein and a chromosome condensation protein from a melanoma complementary DNA library. Cancer Res 60: 3584-3591
27. Kinchen JM, Ravichandran KS (2010) Identification of two evolutionarily conserved genes regulating processing of engulfed apoptotic cells. Nature 464: 778-782
28. Kohbata S, Yokoyama H, Yabuuchi E (1986) Cytopathogenic effect of Salmonella typhi GIFU 10007 on M cells of murine ileal Peyer's patches in ligated ileal loops: an ultrastructural study. Microbiol Immunol 30: 1225-1237
29. Kremers G-J, Goedhart J, van den Heuvel DJ, Gerritsen HC, Gadella TWJ (2007) Improved green and blue fluorescent proteins for expression in bacteria and mammalian cells. Biochemistry 46: 3775-3783
30. Kuijl C, Savage NDL, Marsman M, Tuin AW, Janssen L, Egan DA, Ketema M, van den Nieuwendijk R, van den Eeden SJF, Geluk A, Poot A, van der Marel G, Beijersbergen RL, Overkleeft H, Ottenhoff THM, Neefjes J (2007) Intracellular bacterial growth is controlled by a kinase network around PKB/AKT1. Nature 450: 725-730
31. Kyei GB, Vergne I, Chua J, Roberts E, Harris J, Junutula JR, Deretic V (2006) Rab14 is critical for maintenance of Mycobacterium tuberculosis phagosome maturation arrest. EMBO J 25: 5250-5259
32. Larance M, Ramm G, Stöckli J, van Dam EM, Winata S, Wasinger V, Simpson F, Graham M, Junutula JR, Guilhaus M, James DE (2005) Characterization of the role of the Rab GTPase-activating protein AS160 in insulin-regulated GLUT4 trafficking. J Biol Chem 280: 37803-37813
33. Lim K-P, Hong W (2004) Human Nischarin/imidazoline receptor antisera-selected protein is targeted to the endosomes by a combined action of a PX domain and a coiled-coil region. J Biol Chem 279: 54770-54782
34. Lindmo K, Stenmark H (2006) Regulation of membrane traffic by phosphoinositide 3-kinases. J Cell Sci 119: 605-614
35. Lombardi D, Soldati T, Riederer MA, Goda Y, Zerial M, Pfeffer SR (1993) Rab9 functions in transport between late endosomes and the trans Golgi network. EMBO J 12: 677-682
36. Lostroh CP, Lee CA (2001) The Salmonella pathogenicity island-1 type III secretion system. Microbes Infect 3: 1281-1291
37. Mallo GV, Espina M, Smith AC, Terebiznik MR, Alemán A, Finlay BB, Rameh LE, Grinstein S, Brumell JH (2008) SopB promotes phosphatidylinositol 3-phosphate formation on Salmonella vacuoles by recruiting Rab5 and Vps34. J Cell Biol 182: 741-752
38. Manser E, Leung T, Salihuddin H, Zhao ZS, Lim L (1994) A brain serine/threonine protein kinase activated by Cdc42 and Rac1. Nature 367: 40-46
39. McGhie EJ, Brawn LC, Hume PJ, Humphreys D, Koronakis V (2009) Salmonella takes control: effector-driven manipulation of the host. Curr Opin Microbiol 12: 117-124
40. Méresse S, Steele-Mortimer O, Finlay BB, Gorvel JP (1999) The rab7 GTPase controls the maturation of Salmonella typhimuriumcontaining vacuoles in HeLa cells. EMBO J 18: 4394-4403
41. M?̂inea CP, Sano H, Kane S, Sano E, Fukuda M, Peränen J, Lane WS, Lienhard GE (2005) AS160, the Akt substrate regulating GLUT4 translocation, has a functional Rab GTPase-activating protein domain. Biochem J 391: 87-93
42. Palamidessi A, Frittoli E, Garré M, Faretta M, Mione M, Testa I, Diaspro A, Lanzetti L, Scita G, Di Fiore PP (2008) Endocytic trafficking of Rac is required for the spatial restriction of signaling in cell migration. Cell 134: 135-147
43. Pavlova B, Volf J, Ondrackova P, Matiasovic J, Stepanova H, Crhanova M, Karasova D, Faldyna M, Rychlik I (2011) SPI-1-encoded type III secretion system of Salmonella enterica is required for the suppression of porcine alveolar macrophage cytokine expression. Vet Res 42: 16
44. Pfeffer S (2003) Membrane domains in the secretory and endocytic pathways. Cell 112: 507-517
45. Poteryaev D, Datta S, Ackema K, Zerial M, Spang A (2010) Identification of the switch in early-to-late endosome transition. Cell 141: 497-508
46. Rathman M, Sjaastad MD, Falkow S (1996) Acidification of phagosomes containing Salmonella typhimurium in murine macrophages. Infect Immun 64: 2765-2773
47. Reddig PJ, Xu D, Juliano RL (2005) Regulation of p21-activated kinase-independent Rac1 signal transduction by nischarin. J Biol Chem 280: 30994-31002
48. Rescigno M, Urbano M, Valzasina B, Francolini M, Rotta G, Bonasio R, Granucci F, Kraehenbuhl JP, Ricciardi-Castagnoli P (2001) Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol 2: 361-367
49. Riederer MA, Soldati T, Shapiro AD, Lin J, Pfeffer SR (1994) Lysosome biogenesis requires Rab9 function and receptor recycling from endosomes to the trans-Golgi network. J Cell Biol 125: 573-582
50. Rink J, Ghigo E, Kalaidzidis Y, Zerial M (2005) Rab conversion as a mechanism of progression from early to late endosomes. Cell 122: 735-749
51. Sano H, Liu SCH, Lane WS, Piletz JE, Lienhard GE (2002) Insulin receptor substrate 4 associates with the protein IRAS. J Biol Chem 277: 19439-19447
52. Smith AC, Heo WD, Braun V, Jiang X, Macrae C, Casanova JE, Scidmore MA, Grinstein S, Meyer T, Brumell JH (2007) A network of Rab GTPases controls phagosome maturation and is modulated by Salmonella enterica serovar Typhimurium. J Cell Biol 176: 263-268
53. Souwer Y, Griekspoor A, Jorritsma T, de Wit J, Janssen H, Neefjes J, van Ham SM (2009) B cell receptor-mediated internalization of salmonella: a novel pathway for autonomous B cell activation and antibody production. J Immunol 182: 7473-7481
54. Steele-Mortimer O (2000) Activation of Akt/Protein Kinase B in Epithelial Cells by the Salmonella typhimurium Effector SigD. J Biol Chem 275: 37718-37724
55. Steele-Mortimer O, Méresse S, Gorvel JP, Toh BH, Finlay BB (1999a) Biogenesis of Salmonella typhimurium-containing vacuoles in epithelial cells involves interactions with the early endocytic pathway. Cell Microbiol 1: 33-49
56. Steele-Mortimer O, Méresse S, Gorvel JP, Toh BH, Finlay BB (1999b) Biogenesis of Salmonella typhimurium-containing vacuoles in epithelial cells involves interactions with the early endocytic pathway. Cell Microbiol 1: 33-49
57. Stöckli J, Davey JR, Hohnen-Behrens C, Xu A, James DE, Ramm G (2008) Regulation of glucose transporter 4 translocation by the Rab guanosine triphosphatase-activating protein AS160/TBC1D4: role of phosphorylation and membrane association. Mol Endocrinol 22: 2703-2715
58. Vennegoor C, Calafat J, Hageman P, van Buitenen F, Janssen H, Kolk A, Rümke P (1985) Biochemical characterization and cellular localization of a formalin-resistant melanoma-associated antigen reacting with monoclonal antibody NKI/C-3. Int J Cancer 35: 287-295
59. Wells CM, Abo A, Ridley AJ (2002) PAK4 is activated via PI3K in HGF-stimulated epithelial cells. J Cell Sci 115: 3947-3956
60. Yamamoto H, Koga H, Katoh Y, Takahashi S, Nakayama K, Shin HW (2010) Functional cross-talk between Rab14 and Rab4 through a dual effector, RUFY1/Rabip4. Mol Biol Cell 21: 2746-2755
61. Yeung T, Grinstein S (2007) Lipid signaling and the modulation of surface charge during phagocytosis. Immunol Rev 219: 17-36
62. Yu X-J, McGourty K, Liu M, Unsworth KE, Holden DW (2010) pH sensing by intracellular Salmonella induces effector translocation. Science 328: 1040-1043
63. Zerial M, McBride H (2001) Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2: 107-117