A Bacterial Pathogen Targets a Host Rab-Family GTPase Defense Pathway with a GAP

Cell Host and Microbe

Volumn 19, Issue 2, 2016, Pages 216-226

  Spanò, Stefania ^a   Gao, Xiang ^a   Hannemann, Sebastian ^a   Lara Tejero, María ^a   Galán, Jorge E ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

bacterial pathogenesis; cell autonomous defense; innate immunity; lysosome related organelles; lysosomes; macrophages; membrane traffic; Rab GTPases; Rab32; Salmonella pathogenesis; Salmonella Typhi; type III secretion; typhoid fever

Indexed keywords

GUANOSINE TRIPHOSPHATASE; RAB PROTEIN; BACTERIAL PROTEIN; RAB32 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL VIRULENCE; CONTROLLED STUDY; HOST RESISTANCE; INFECTION SENSITIVITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN SECRETION; PROTEIN TARGETING; SALMONELLA ENTERICA SEROVAR TYPHI; TYPE III SECRETION SYSTEM; ANIMAL; ENZYMOLOGY; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; PROTEIN DEGRADATION; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SALMONELLOSIS; VIRULENCE;

ANIMALS; BACTERIAL PROTEINS; HOST-PATHOGEN INTERACTIONS; HUMANS; MICE; PROTEOLYSIS; RAB GTP-BINDING PROTEINS; SALMONELLA INFECTIONS; SALMONELLA TYPHI; SALMONELLA TYPHIMURIUM; VIRULENCE;

EID: 85012004937     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2016.01.004     Document Type: Article

References (63)

1. Albert, S., Gallwitz, D., Two new members of a family of Ypt/Rab GTPase activating proteins. Promiscuity of substrate recognition. J. Biol. Chem. 274 (1999), 33186–33189.
2. Alix, E., Mukherjee, S., Roy, C.R., Subversion of membrane transport pathways by vacuolar pathogens. J. Cell Biol. 195 (2011), 943–952.
3. Aspengren, S., Hedberg, D., Sköld, H.N., Wallin, M., New insights into melanosome transport in vertebrate pigment cells. Int. Rev. Cell Mol. Biol. 272 (2009), 245–302.
4. Asrat, S., de Jesús, D.A., Hempstead, A.D., Ramabhadran, V., Isberg, R.R., Bacterial pathogen manipulation of host membrane trafficking. Annu. Rev. Cell Dev. Biol. 30 (2014), 79–109.
5. Barr, F., Lambright, D.G., Rab GEFs and GAPs. Curr. Opin. Cell Biol. 22 (2010), 461–470.
6. Benado, A., Nasagi-Atiya, Y., Sagi-Eisenberg, R., Protein trafficking in immune cells. Immunobiology 214 (2009), 507–525.
7. Broz, P., Monack, D.M., Newly described pattern recognition receptors team up against intracellular pathogens. Nat. Rev. Immunol. 13 (2013), 551–565.
8. Brumell, J.H., Kujat-Choy, S., Brown, N.F., Vallance, B.A., Knodler, L.A., Finlay, B.B., SopD2 is a novel type III secreted effector of Salmonella typhimurium that targets late endocytic compartments upon delivery into host cells. Traffic 4 (2003), 36–48.
9. Bruno, V.M., Hannemann, S., Lara-Tejero, M., Flavell, R.A., Kleinstein, S.H., Galán, J.E., Salmonella Typhimurium type III secretion effectors stimulate innate immune responses in cultured epithelial cells. PLoS Pathog., 5, 2009, e1000538.
10. Bultema, J.J., Ambrosio, A.L., Burek, C.L., Di Pietro, S.M., BLOC-2, AP-3, and AP-1 proteins function in concert with Rab38 and Rab32 proteins to mediate protein trafficking to lysosome-related organelles. J. Biol. Chem. 287 (2012), 19550–19563.
11. Collazo, C.M., Galán, J.E., The invasion-associated type III system of Salmonella typhimurium directs the translocation of Sip proteins into the host cell. Mol. Microbiol. 24 (1997), 747–756.
12. Creasey, E.A., Isberg, R.R., Maintenance of vacuole integrity by bacterial pathogens. Curr. Opin. Microbiol. 17 (2014), 46–52.
13. Crump, J.A., Mintz, E.D., Global trends in typhoid and paratyphoid Fever. Clin. Infect. Dis. 50 (2010), 241–246.
14. D'Costa, V.M., Braun, V., Landekic, M., Shi, R., Proteau, A., McDonald, L., Cygler, M., Grinstein, S., Brumell, J.H., Salmonella disrupts host endocytic trafficking by SopD2-mediated inhibition of Rab7. Cell Rep. 12 (2015), 1508–1518.
15. Dell'Angelica, E.C., The building BLOC(k)s of lysosomes and related organelles. Curr. Opin. Cell Biol. 16 (2004), 458–464.
16. Denat, L., Kadekaro, A.L., Marrot, L., Leachman, S.A., Abdel-Malek, Z.A., Melanocytes as instigators and victims of oxidative stress. J. Invest. Dermatol. 134 (2014), 1512–1518.
17. Deretic, V., Autophagy in immunity and cell-autonomous defense against intracellular microbes. Immunol. Rev. 240 (2011), 92–104.
18. Diacovich, L., Gorvel, J.P., Bacterial manipulation of innate immunity to promote infection. Nat. Rev. Microbiol. 8 (2010), 117–128.
19. Dixit, E., Kagan, J.C., Intracellular pathogen detection by RIG-I-like receptors. Adv. Immunol. 117 (2013), 99–125.
20. Fukuda, M., TBC proteins: GAPs for mammalian small GTPase Rab?. Biosci. Rep. 31 (2011), 159–168.
21. Galán, J.E., Curtiss, R. 3rd, Distribution of the invA, -B, -C, and -D genes of Salmonella typhimurium among other Salmonella serovars: invA mutants of Salmonella typhi are deficient for entry into mammalian cells. Infect. Immun. 59 (1991), 2901–2908.
22. Gerondopoulos, A., Langemeyer, L., Liang, J.R., Linford, A., Barr, F.A., BLOC-3 mutated in Hermansky-Pudlak syndrome is a Rab32/38 guanine nucleotide exchange factor. Curr. Biol. 22 (2012), 2135–2139.
23. Grassl, G.A., Finlay, B.B., Pathogenesis of enteric Salmonella infections. Curr. Opin. Gastroenterol. 24 (2008), 22–26.
24. Harris, R.S., Dudley, J.P., APOBECs and virus restriction. Virology 479-480 (2015), 131–145.
25. Hensel, M., Shea, J.E., Gleeson, C., Jones, M.D., Dalton, E., Holden, D.W., Simultaneous identification of bacterial virulence genes by negative selection. Science 269 (1995), 400–403.
26. Hoiseth, S.K., Stocker, B.A., Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291 (1981), 238–239.
27. Hunn, J.P., Feng, C.G., Sher, A., Howard, J.C., The immunity-related GTPases in mammals: a fast-evolving cell-autonomous resistance system against intracellular pathogens. Mamm. Genome 22 (2011), 43–54.
28. Jarczak, J., Kościuczuk, E.M., Lisowski, P., Strzałkowska, N., Jóźwik, A., Horbańczuk, J., Krzyżewski, J., Zwierzchowski, L., Bagnicka, E., Defensins: natural component of human innate immunity. Hum. Immunol. 74 (2013), 1069–1079.
29. Jiang, H., Vilcinskas, A., Kanost, M.R., Immunity in lepidopteran insects. Adv. Exp. Med. Biol. 708 (2010), 181–204.
30. Kaniga, K., Bossio, J.C., Galán, J.E., The Salmonella typhimurium invasion genes invF and invG encode homologues of the AraC and PulD family of proteins. Mol. Microbiol. 13 (1994), 555–568.
31. Kim, B.H., Shenoy, A.R., Kumar, P., Bradfield, C.J., MacMicking, J.D., IFN-inducible GTPases in host cell defense. Cell Host Microbe 12 (2012), 432–444.
32. Lee, M.T., Mishra, A., Lambright, D.G., Structural mechanisms for regulation of membrane traffic by rab GTPases. Traffic 10 (2009), 1377–1389.
33. Liu, X., Gao, B., Novik, V., Galán, J.E., Quantitative Proteomics of Intracellular Campylobacter jejuni Reveals Metabolic Reprogramming. PLoS Pathog., 8, 2012, e1002562.
34. Lu, A., Zhang, Q., Zhang, J., Yang, B., Wu, K., Xie, W., Luan, Y.X., Ling, E., Insect prophenoloxidase: the view beyond immunity. Front. Physiol., 5, 2014, 252, 10.3389/fphys.2014.00252.
35. Luzio, J.P., Hackmann, Y., Dieckmann, N.M., Griffiths, G.M., The biogenesis of lysosomes and lysosome-related organelles. Cold Spring Harb. Perspect. Biol., 6, 2014, a016840, 10.011101/cshperspect.a016840.
36. Medzhitov, R., Recognition of microorganisms and activation of the immune response. Nature 449 (2007), 819–826.
37. Nairz, M., Haschka, D., Demetz, E., Weiss, G., Iron at the interface of immunity and infection. Front. Pharmacol., 5, 2014, 152.
38. Nish, S., Medzhitov, R., Host defense pathways: role of redundancy and compensation in infectious disease phenotypes. Immunity 34 (2011), 629–636.
39. Ochman, H., Soncini, F.C., Solomon, F., Groisman, E.A., Identification of a pathogenicity island required for Salmonella survival in host cells. Proc. Natl. Acad. Sci. USA 93 (1996), 7800–7804.
40. Ohl, M.E., Miller, S.I., Salmonella: a model for bacterial pathogenesis. Annu. Rev. Med. 52 (2001), 259–274.
41. Orchard, R.C., Alto, N.M., Mimicking GEFs: a common theme for bacterial pathogens. Cell. Microbiol. 14 (2012), 10–18.
42. Parkhill, J., Dougan, G., James, K.D., Thomson, N.R., Pickard, D., Wain, J., Churcher, C., Mungall, K.L., Bentley, S.D., Holden, M.T., et al. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 413 (2001), 848–852.
43. Parry, C.M., Hien, T.T., Dougan, G., White, N.J., Farrar, J.J., Typhoid fever. N. Engl. J. Med. 347 (2002), 1770–1782.
44. Raffatellu, M., Wilson, R.P., Winter, S.E., Bäumler, A.J., Clinical pathogenesis of typhoid fever. J. Infect. Dev. Ctries. 2 (2008), 260–266.
45. Rajsbaum, R., García-Sastre, A., Versteeg, G.A., TRIMmunity: the roles of the TRIM E3-ubiquitin ligase family in innate antiviral immunity. J. Mol. Biol. 426 (2014), 1265–1284.
46. Randow, F., MacMicking, J.D., James, L.C., Cellular self-defense: how cell-autonomous immunity protects against pathogens. Science 340 (2013), 701–706.
47. Raposo, G., Marks, M.S., Melanosomes—dark organelles enlighten endosomal membrane transport. Nat. Rev. Mol. Cell Biol. 8 (2007), 786–797.
48. Reddick, L.E., Alto, N.M., Bacteria fighting back: how pathogens target and subvert the host innate immune system. Mol. Cell 54 (2014), 321–328.
49. Sanjuan, M.A., Milasta, S., Green, D.R., Toll-like receptor signaling in the lysosomal pathways. Immunol. Rev. 227 (2009), 203–220.
50. Sato, T., Iwano, T., Kunii, M., Matsuda, S., Mizuguchi, R., Jung, Y., Hagiwara, H., Yoshihara, Y., Yuzaki, M., Harada, R., Harada, A., Rab8a and Rab8b are essential for several apical transport pathways but insufficient for ciliogenesis. J. Cell Sci. 127 (2014), 422–431.
51. Schroeder, N., Henry, T., de Chastellier, C., Zhao, W., Guilhon, A.A., Gorvel, J.P., Méresse, S., The virulence protein SopD2 regulates membrane dynamics of Salmonella-containing vacuoles. PLoS Pathog., 6, 2010, e1001002, 10.1371/journal.ppat.1001002.
52. Spanò, S., Galán, J.E., A Rab32-dependent pathway contributes to Salmonella typhi host restriction. Science 338 (2012), 960–963.
53. Spanò, S., Liu, X., Galán, J.E., Proteolytic targeting of Rab29 by an effector protein distinguishes the intracellular compartments of human-adapted and broad-host Salmonella. Proc. Natl. Acad. Sci. USA 108 (2011), 18418–18423.
54. Stebbins, C.E., Galán, J.E., Modulation of host signaling by a bacterial mimic: structure of the Salmonella effector SptP bound to Rac1. Mol. Cell 6 (2000), 1449–1460.
55. Stebbins, C.E., Galán, J.E., Structural mimicry in bacterial virulence. Nature 412 (2001), 701–705.
56. Stenmark, H., Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol. 10 (2009), 513–525.
57. Tsolis, R.M., Townsend, S.M., Miao, E.A., Miller, S.I., Ficht, T.A., Adams, L.G., Bäumler, A.J., Identification of a putative Salmonella enterica serotype typhimurium host range factor with homology to IpaH and YopM by signature-tagged mutagenesis. Infect. Immun. 67 (1999), 6385–6393.
58. Voehringer, D., Protective and pathological roles of mast cells and basophils. Nat. Rev. Immunol. 13 (2013), 362–375.
59. Wasmeier, C., Romao, M., Plowright, L., Bennett, D.C., Raposo, G., Seabra, M.C., Rab38 and Rab32 control post-Golgi trafficking of melanogenic enzymes. J. Cell Biol. 175 (2006), 271–281.
60. Wood, M.W., Jones, M.A., Watson, P.R., Siber, A.M., McCormick, B.A., Hedges, S., Rosqvist, R., Wallis, T.S., Galyov, E.E., The secreted effector protein of Salmonella dublin, SopA, is translocated into eukaryotic cells and influences the induction of enteritis. Cell. Microbiol. 2 (2000), 293–303.
61. Yang, Y., Bazhin, A.V., Werner, J., Karakhanova, S., Reactive oxygen species in the immune system. Int. Rev. Immunol. 32 (2013), 249–270.
62. Zhang, F., Liu, H., Chen, S., Low, H., Sun, L., Cui, Y., Chu, T., Li, Y., Fu, X., Yu, Y., et al. Identification of two new loci at IL23R and RAB32 that influence susceptibility to leprosy. Nat. Genet. 43 (2011), 1247–1251.
63. Zhou, D., Chen, L.M., Hernandez, L., Shears, S.B., Galán, J.E., A Salmonella inositol polyphosphatase acts in conjunction with other bacterial effectors to promote host cell actin cytoskeleton rearrangements and bacterial internalization. Mol. Microbiol. 39 (2001), 248–259.