Information de reference pour ce titreAccession Number: | 00076208-201309100-00009.
|
Author: | Krzewski, Konrad a; Cullinane, Andrew R. b,*
|
Institution: | (a)Receptor Cell Biology Section, Laboratory of Immunogenetics, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Rockville, MD 20852, USA (b)Medical Genetics Branch, National Human Genome Research Institute, National Institutes of Health, Building 10, Room 10C107A, 10 Center Drive, Bethesda, MD 20892, USA
|
Title: | Evidence for defective Rab GTPase-dependent cargo traffic in immune disorders.[Review]
|
Source: | Experimental Cell Research. 319(15):2360-2367, September 10, 2013.
|
Abstract: | A fully functional immune system is essential to protect the body against pathogens and other diseases, including cancer. Vesicular trafficking provides the correct localization of proteins within all cell types, but this process is most exquisitely controlled and coordinated in immune cells because of their specialized organelles and their requirement to respond to selected stimuli. More than 60 Rab GTPases play important roles in protein trafficking, but only five Rab-encoding genes have been associated with inherited human disorders, and only one of these (Rab27a) causes an immune defect. Mutations in RAB27A cause Griscelli Syndrome type 2 (GS2), an autosomal recessive disorder of pigmentation and severe immune deficiency. In lymphocytes, Munc13-4 is an effector of Rab27a, and mutations in the gene encoding this protein (UNC13D) cause Familial Hemophagocytic Lymphohistiocytosis Type 3 (FHL3). The immunological features of GS2 and FHL3 include neutropenia, thrombocytopenia, and immunodeficiency due to impaired function of cytotoxic lymphocytes. The small number of disorders caused by mutations in genes encoding Rabs could be due to their essential functions, where defects in these genes could be lethal. However, with the increasing use of next generation sequencing technologies, more mutations in genes encoding Rabs may be identified in the near future.
* Precise protein trafficking is required for the immune system to function properly.
* Rab5, Rab7, Rab13, Rab14, Rab27a, and Rab38 are associated with immune disorders.
* Mutations in RAB27A cause Griscelli Syndrome Type 2, a pigment and immune disorder.
* UNC13D, encoding Munc13-4, is mutated in FHL Type 3 and is an effector of Rab27a.
(C) 2013Elsevier, Inc.
|
Author Keywords: | Rab GTPases; Immunodeficiencies; Griscelli Syndrome Type 2; Rab27a; Familial Hemophagocytic Lymphohistiocytosis Type 3; Muc13-4.
|
References: | [1]. A.Q. Gomes, B.R. Ali, J.S. Ramalho, R.F. Godfrey, D.C. Barral, A.N. Hume, M.C. Seabra. Membrane targeting of Rab GTPases is influenced by the prenylation motif. Mol. Biol. Cell. 14 (2003) 1882-1899.
[2]. M. Zerial, H. McBride. Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2 (2001) 107-117.
[3]. S. Pfeffer, D. Aivazian. Targeting Rab GTPases to distinct membrane compartments. Nat. Rev. Mol. Cell Biol. 5 (2004) 886-896.
[4]. A.K. Haas, E. Fuchs, R. Kopajtich, F.A. Barr. A GTPase-activating protein controls Rab5 function in endocytic trafficking. Nat. Cell Biol. 7 (2005) 887-893.
[5]. A. Benado, Y. Nasagi-Atiya, R. Sagi-Eisenberg. Protein trafficking in immune cells. Immunobiology. 214 (2009) 507-525.
[6]. A.J. Smith, J.R. Pfeiffer, J. Zhang, A.M. Martinez, G.M. Griffiths, B.S. Wilson. Microtubule-dependent transport of secretory vesicles in RBL-2H3 cells. Traffic. 4 (2003) 302-312.
[7]. G. Bossi, G.M. Griffiths. Degranulation plays an essential part in regulating cell surface expression of Fas ligand in T cells and natural killer cells. Nat. Med. 5 (1999) 90-96.
[8]. S. Kornfeld, I. Mellman. The biogenesis of lysosomes. Annu. Rev. Cell Biol. 5 (1989) 483-525.
[9]. G. Raposo, M.S. Marks, D.F. Cutler. Lysosome-related organelles: driving post-Golgi compartments into specialisation. Curr. Opin. Cell Biol. 19 (2007) 394-401.
[10]. M. Huizing, A. Helip-Wooley, W. Westbroek, M. Gunay-Aygun, W.A. Gahl. Disorders of lysosome-related organelle biogenesis: clinical and molecular genetics. Annu. Rev. Genomics Hum. Genet. 9 (2008) 359-386.
[11]. J.S. Bonifacino, B.S. Glick. The mechanisms of vesicle budding and fusion. Cell. 116 (2004) 153-166.
[12]. J. Gruenberg. The endocytic pathway: a mosaic of domains. Nat. Rev. Mol. Cell Biol. 2 (2001) 721-730.
[13]. S.A. Tooze. Biogenesis of secretory granules in the trans-Golgi network of neuroendocrine and endocrine cells. Biochim. Biophys. Acta. 1404 (1998) 231-244.
[14]. D. Bem, S. Yoshimura, R. Nunes-Bastos, F.C. Bond, M.A. Kurian, F. Rahman, M.T. Handley, Y. Hadzhiev, I. Masood, A.A. Straatman-Iwanowska, A.R. Cullinane, A. McNeill, S.S. Pasha, G.A. Kirby, K. Foster, Z. Ahmed, J.E. Morton, D. Williams, J.M. Graham, W.B. Dobyns, L. Burglen, J.R. Ainsworth, P. Gissen, F. Muller, E.R. Maher, F.A. Barr, I.A. Aligianis. Loss-of-function mutations in RAB18 cause Warburg micro-syndrome. Am. J. Hum. Genet. 88 (2011) 499-507.
[15]. K. Verhoeven, P. De Jonghe, K. Coen, N. Verpoorten, M. Auer-Grumbach, J.M. Kwon, D. FitzPatrick, E. Schmedding, E. De Vriendt, A. Jacobs, V. Van Gerwen, K. Wagner, H.P. Hartung, V. Timmerman. Mutations in the small GTP-ase late endosomal protein RAB7 cause Charcot-Marie-Tooth type 2B neuropathy. Am. J. Hum. Genet. 72 (2003) 722-727.
[16]. D. Jenkins, D. Seelow, F.S. Jehee, C.A. Perlyn, L.G. Alonso, D.F. Bueno, D. Donnai, D. Josifova, I.M. Mathijssen, J.E. Morton, K.H. Orstavik, E. Sweeney, S.A. Wall, J.L. Marsh, P. Nurnberg, M.R. Passos-Bueno, A.O. Wilkie. RAB23 mutations in Carpenter syndrome imply an unexpected role for hedgehog signaling in cranial-suture development and obesity. Am. J. Hum. Genet. 80 (2007) 1162-1170.
[17]. G. Menasche, E. Pastural, J. Feldmann, S. Certain, F. Ersoy, S. Dupuis, N. Wulffraat, D. Bianchi, A. Fischer, F. Le Deist, G. de Saint Basile. Mutations in RAB27A cause Griscelli syndrome associated with haemophagocytic syndrome. Nat. Genet. 25 (2000) 173-176.
[18]. M. Giannandrea, V. Bianchi, M.L. Mignogna, A. Sirri, S. Carrabino, E. D'Elia, M. Vecellio, S. Russo, F. Cogliati, L. Larizza, H.H. Ropers, A. Tzschach, V. Kalscheuer, B. Oehl-Jaschkowitz, C. Skinner, C.E. Schwartz, J. Gecz, H. Van Esch, M. Raynaud, J. Chelly, A.P. de Brouwer, D. Toniolo, P. D'Adamo. Mutations in the small GTPase gene RAB39B are responsible for X-linked mental retardation associated with autism, epilepsy, and macrocephaly. Am. J. Hum. Genet. 86 (2010) 185-195.
[19]. C. Griscelli, A. Durandy, D. Guy-Grand, F. Daguillard, C. Herzog, M. Prunieras. A syndrome associating partial albinism and immunodeficiency. Am. J. Med. 65 (1978) 691-702.
[20]. C. Griscelli, M. Prunieras. Pigment dilution and immunodeficiency: a new syndrome. Int. J. Dermatol. 17 (1978) 788-791.
[21]. X.S. Wu, K. Rao, H. Zhang, F. Wang, J.R. Sellers, L.E. Matesic, N.G. Copeland, N.A. Jenkins, J.A. Hammer 3rd. Identification of an organelle receptor for myosin-Va. Nat. Cell Biol. 4 (2002) 271-278.
[22]. J.C. Stinchcombe, D.C. Barral, E.H. Mules, S. Booth, A.N. Hume, L.M. Machesky, M.C. Seabra, G.M. Griffiths. Rab27a is required for regulated secretion in cytotoxic T lymphocytes. J. Cell Biol. 152 (2001) 825-834.
[23]. A.N. Hume, L.M. Collinson, C.R. Hopkins, M. Strom, D.C. Barral, G. Bossi, G.M. Griffiths, M.C. Seabra. The leaden gene product is required with Rab27a to recruit myosin Va to melanosomes in melanocytes. Traffic. 3 (2002) 193-202.
[24]. J. Pachlopnik Schmid, C.H. Ho, J. Diana, G. Pivert, A. Lehuen, F. Geissmann, A. Fischer, G. de Saint Basile. A Griscelli syndrome type 2 murine model of hemophagocytic lymphohistiocytosis (HLH). Eur. J. Immunol. 38 (2008) 3219-3225.
[25]. M. Miyata, Y. Kishimoto, M. Tanaka, K. Hashimoto, N. Hirashima, Y. Murata, M. Kano, Y. Takagishi. A role for myosin Va in cerebellar plasticity and motor learning: a possible mechanism underlying neurological disorder in myosin Va disease. J. Neurosci. 31 (2011) 6067-6078.
[26]. E.K. Haddad, X. Wu, J.A. Hammer 3rd, P.A. Henkart. Defective granule exocytosis in Rab27a-deficient lymphocytes from Ashen mice. J. Cell Biol. 152 (2001) 835-842.
[27]. S.M. Wood, M. Meeths, S.C. Chiang, A.G. Bechensteen, J.J. Boelens, C. Heilmann, H. Horiuchi, S. Rosthoj, O. Rutynowska, J. Winiarski, J.L. Stow, M. Nordenskjold, J.I. Henter, H.G. Ljunggren, Y.T. Bryceson. Different NK cell-activating receptors preferentially recruit Rab27a or Munc13-4 to perforin-containing granules for cytotoxicity. Blood. 114 (2009) 4117-4127.
[28]. M. Neeft, M. Wieffer, A.S. de Jong, G. Negroiu, C.H. Metz, A. van Loon, J. Griffith, J. Krijgsveld, N. Wulffraat, H. Koch, A.J. Heck, N. Brose, M. Kleijmeer, P. van der Sluijs. Munc13-4 is an effector of rab27a and controls secretion of lysosomes in hematopoietic cells. Mol. Biol. Cell. 16 (2005) 731-741.
[29]. G. Menasche, M.M. Menager, J.M. Lefebvre, E. Deutsch, R. Athman, N. Lambert, N. Mahlaoui, M. Court, J. Garin, A. Fischer, G. de Saint Basile. A newly identified isoform of Slp2a associates with Rab27a in cytotoxic T cells and participates to cytotoxic granule secretion. Blood. 112 (2008) 5052-5062.
[30]. Y. Sanchez-Ruiz, S. Valitutti, L. Dupre. Stepwise maturation of lytic granules during differentiation and activation of human CD8+ T lymphocytes. PLoS One. 6 (2011) e27057.
[31]. G. de Saint Basile, G. Menasche, A. Fischer. Molecular mechanisms of biogenesis and exocytosis of cytotoxic granules, Nat. Rev. Immunol., 10, 568-579.
[32]. M.M. Menager, G. Menasche, M. Romao, P. Knapnougel, C.H. Ho, M. Garfa, G. Raposo, J. Feldmann, A. Fischer, G. de Saint Basile. Secretory cytotoxic granule maturation and exocytosis require the effector protein hMunc13-4. Nat. Immunol. 8 (2007) 257-267.
[33]. D. Liu, T. Meckel, E.O. Long. Distinct role of rab27a in granule movement at the plasma membrane and in the cytosol of NK cells. PLoS One. 5 (2010) e12870.
[34]. M. Kurowska, N. Goudin, N.T. Nehme, M. Court, J. Garin, A. Fischer, G. de Saint Basile, G. Menasche. Terminal transport of lytic granules to the immune synapse is mediated by the kinesin-1/Slp3/Rab27a complex. Blood. 119 (2012) 3879-3889.
[35]. M.M. Andzelm, X. Chen, K. Krzewski, J.S. Orange, J.L. Strominger. Myosin IIA is required for cytolytic granule exocytosis in human NK cells. J. Exp. Med. 204 (2007) 2285-2291.
[36]. G.E. Janka. Familial hemophagocytic lymphohistiocytosis. Eur. J. Pediatr. 140 (1983) 221-230.
[37]. S.E. Stepp, R. Dufourcq-Lagelouse, F. Le Deist, S. Bhawan, S. Certain, P.A. Mathew, J.I. Henter, M. Bennett, A. Fischer, G. de Saint Basile, V. Kumar. Perforin gene defects in familial hemophagocytic lymphohistiocytosis. Science. 286 (1999) 1957-1959.
[38]. J. Feldmann, I. Callebaut, G. Raposo, S. Certain, D. Bacq, C. Dumont, N. Lambert, M. Ouachee-Chardin, G. Chedeville, H. Tamary, V. Minard-Colin, E. Vilmer, S. Blanche, F. Le Deist, A. Fischer, G. de Saint Basile. Munc13-4 is essential for cytolytic granules fusion and is mutated in a form of familial hemophagocytic lymphohistiocytosis (FHL3). Cell. 115 (2003) 461-473.
[39]. U. zur Stadt, S. Schmidt, B. Kasper, K. Beutel, A.S. Diler, J.I. Henter, H. Kabisch, R. Schneppenheim, P. Nurnberg, G. Janka, H.C. Hennies. Linkage of familial hemophagocytic lymphohistiocytosis (FHL) type-4 to chromosome 6q24 and identification of mutations in syntaxin 11. Hum. Mol. Genet. 14 (2005) 827-834.
[40]. U. zur Stadt, J. Rohr, W. Seifert, F. Koch, S. Grieve, J. Pagel, J. Strauss, B. Kasper, G. Nurnberg, C. Becker, A. Maul-Pavicic, K. Beutel, G. Janka, G. Griffiths, S. Ehl, H.C. Hennies. Familial hemophagocytic lymphohistiocytosis type 5 (FHL-5) is caused by mutations in Munc18-2 and impaired binding to syntaxin 11. Am. J. Hum. Genet. 85 (2009) 482-492.
[41]. S. Marcenaro, F. Gallo, S. Martini, A. Santoro, G.M. Griffiths, M. Arico, L. Moretta, D. Pende. Analysis of natural killer-cell function in familial hemophagocytic lymphohistiocytosis (FHL): defective CD107a surface expression heralds Munc13-4 defect and discriminates between genetic subtypes of the disease. Blood. 108 (2006) 2316-2323.
[42]. J. Rohr, K. Beutel, A. Maul-Pavicic, T. Vraetz, J. Thiel, K. Warnatz, I. Bondzio, U. Gross-Wieltsch, M. Schundeln, B. Schutz, W. Woessmann, A.H. Groll, B. Strahm, J. Pagel, C. Speckmann, G. Janka, G. Griffiths, K. Schwarz, U. zur Stadt, S. Ehl. Atypical familial hemophagocytic lymphohistiocytosis due to mutations in UNC13D and STXBP2 overlaps with primary immunodeficiency diseases. Haematologica. 95 (2010) 2080-2087.
[43]. M. Meeths, S.C. Chiang, S.M. Wood, M. Entesarian, H. Schlums, B. Bang, E. Nordenskjold, C. Bjorklund, G. Jakovljevic, J. Jazbec, H. Hasle, B.M. Holmqvist, L. Rajic, S. Pfeifer, S. Rosthoj, M. Sabel, T.T. Salmi, T. Stokland, J. Winiarski, H.G. Ljunggren, B. Fadeel, M. Nordenskjold, J.I. Henter, Y.T. Bryceson. Familial hemophagocytic lymphohistiocytosis type 3 (FHL3) caused by deep intronic mutation and inversion in UNC13D. Blood. 118 (2011) 5783-5793.
[44]. E.D. Elstak, M. Neeft, N.T. Nehme, J. Voortman, M. Cheung, M. Goodarzifard, H.C. Gerritsen, P.M. van Bergen En Henegouwen, I. Callebaut, G. de Saint Basile, P. van der Sluijs. The munc13-4-rab27 complex is specifically required for tethering secretory lysosomes at the plasma membrane. Blood. 118 (2011) 1570-1578.
[45]. K. Krzewski, J.E. Coligan. Human NK cell lytic granules and regulation of their exocytosis. Front. Immunol. 3 (2012) 335.
[46]. J.S. Orange. Formation and function of the lytic NK-cell immunological synapse. Nat. Rev. Immunol. 8 (2008) 713-725.
[47]. L.C. Schneider, R.S. Berman, C.R. Shea, A.R. Perez-Atayde, H. Weinstein, R.S. Geha. Bone marrow transplantation (BMT) for the syndrome of pigmentary dilution and lymphohistiocytosis (Griscelli's syndrome). J. Clin. Immunol. 10 (1990) 146-153.
[48]. A.H. Wei, W. Li. Hermansky-Pudlak syndrome: pigmentary and non-pigmentary defects and their pathogenesis. Pigment Cell Melanoma Res. 26 (2013) 176-192.
[49]. M. Huizing, W.A. Gahl. Disorders of vesicles of lysosomal lineage: the Hermansky-Pudlak syndromes. Curr. Mol. Med. 2 (2002) 451-467.
[50]. B.R. Gochuico, M. Huizing, G.A. Golas, C.D. Scher, M. Tsokos, S.D. Denver, M.J. Frei-Jones, W.A. Gahl. Interstitial lung disease and pulmonary fibrosis in Hermansky-Pudlak syndrome type 2, an adaptor protein-3 complex disease. Mol. Med. 18 (2012) 56-64.
[51]. J.C. Detter, Q. Zhang, E.H. Mules, E.K. Novak, V.S. Mishra, W. Li, E.B. McMurtrie, V.T. Tchernev, M.R. Wallace, M.C. Seabra, R.T. Swank, S.F. Kingsmore. Rab geranylgeranyl transferase alpha mutation in the gunmetal mouse reduces Rab prenylation and platelet synthesis. Proc. Natl. Acad. Sci. USA. 97 (2000) 4144-4149.
[52]. Q. Zhang, L. Zhen, W. Li, E.K. Novak, L.M. Collinson, E.K. Jang, R.J. Haslam, R.W. Elliott, R.T. Swank. Cell-specific abnormal prenylation of Rab proteins in platelets and melanocytes of the gunmetal mouse. Br. J. Haematol. 117 (2002) 414-423.
[53]. M.C. Seabra, E.H. Mules, A.N. Hume. Rab GTPases intracellular traffic and disease. Trends Mol. Med. 8 (2002) 23-30.
[54]. L. Zhang, K. Yu, K.W. Robert, K.M. DeBolt, N. Hong, J.Q. Tao, M. Fukuda, A.B. Fisher, S. Huang. Rab38 targets to lamellar bodies and normalizes their sizes in lung alveolar type II epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 301 (2011) L461-477.
[55]. J.R. Wright. Immunoregulatory functions of surfactant proteins. Nat. Rev. Immunol. 5 (2005) 58-68.
[56]. K. Osanai, R. Oikawa, J. Higuchi, M. Kobayashi, K. Tsuchihara, M. Iguchi, H. Jongsu, H. Toga, D.R. Voelker. A mutation in Rab38 small GTPase causes abnormal lung surfactant homeostasis and aberrant alveolar structure in mice. Am. J. Pathol. 173 (2008) 1265-1274.
[57]. K. Osanai, J. Higuchi, R. Oikawa, M. Kobayashi, K. Tsuchihara, M. Iguchi, J. Huang, D.R. Voelker, H. Toga. Altered lung surfactant system in a Rab38-deficient rat model of Hermansky-Pudlak syndrome. Am. J. Physiol. Lung Cell. Mol. Physiol. 298 (2010) L243-251.
[58]. K. Osanai, D.R. Voelker. Analysis and expression of Rab38 in oculocutaneous lung disease. Methods Enzymol. 438 (2008) 203-215.
[59]. A. Gerondopoulos, L. Langemeyer, J.R. Liang, A. Linford, F.A. Barr. BLOC-3 mutated in Hermansky-Pudlak syndrome is a Rab32/38 guanine nucleotide exchange factor. Curr. Biol. CB. 22 (2012) 2135-2139.
[60]. J.J. Bultema, A.L. Ambrosio, C.L. Burek, S.M. Di Pietro. 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.
[61]. A.L. Ambrosio, J.A. Boyle, S.M. Di Pietro. Mechanism of platelet dense granule biogenesis: study of cargo transport and function of Rab32 and Rab38 in a model system. Blood. 120 (2012) 4072-4081.
[62]. E.C. Dell'Angelica, V. Shotelersuk, R.C. Aguilar, W.A. Gahl, J.S. Bonifacino. Altered trafficking of lysosomal proteins in Hermansky-Pudlak syndrome due to mutations in the beta 3A subunit of the AP-3 adaptor. Mol. Cell. 3 (1999) 11-21.
[63]. J.R. Turner. Molecular basis of epithelial barrier regulation: from basic mechanisms to clinical application. Am. J. Pathol. 169 (2006) 1901-1909.
[64]. A.M. Marzesco, I. Dunia, R. Pandjaitan, M. Recouvreur, D. Dauzonne, E.L. Benedetti, D. Louvard, A. Zahraoui. The small GTPase Rab13 regulates assembly of functional tight junctions in epithelial cells. Mol. Biol. Cell. 13 (2002) 1819-1831.
[65]. K. Kohler, D. Louvard, A. Zahraoui. Rab13 regulates PKA signaling during tight junction assembly. J. Cell Biol. 165 (2004) 175-180.
[66]. R. Yamamura, N. Nishimura, H. Nakatsuji, S. Arase, T. Sasaki. The interaction of JRAB/MICAL-L2 with Rab8 and Rab13 coordinates the assembly of tight junctions and adherens junctions. Mol. Biol. Cell. 19 (2008) 971-983.
[67]. M. Ohira, N. Oshitani, S. Hosomi, K. Watanabe, H. Yamagami, K. Tominaga, T. Watanabe, Y. Fujiwara, K. Maeda, K. Hirakawa, T. Arakawa. Dislocation of Rab13 and vasodilator-stimulated phosphoprotein in inactive colon epithelium in patients with Crohn's disease. Int. J. Mol. Med. 24 (2009) 829-835.
[68]. W. Introne, R.E. Boissy, W.A. Gahl. Clinical, molecular, and cell biological aspects of Chediak-Higashi syndrome. Mol. Genet. Metab. 68 (1999) 283-303.
[69]. E. Kypri, K. Falkenstein, A.D. Lozanne. Antagonistic control of lysosomal fusion by Rab14 and the Lyst-related protein LvsB. Traffic. 14 (2013) 599-609.
[70]. J.M. Kinchen, K.S. Ravichandran. Phagosome maturation: going through the acid test. Nat. Rev. Mol. Cell Biol. 9 (2008) 781-795.
[71]. K. Mukherjee, S. Parashuraman, M. Raje, A. Mukhopadhyay. 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. 276 (2001) 23607-23615.
[72]. A. Prada-Delgado, E. Carrasco-Marin, C. Pena-Macarro, E. Del Cerro-Vadillo, M. Fresno-Escudero, F. Leyva-Cobian, C. Alvarez-Dominguez. Inhibition of Rab5a exchange activity is a key step for Listeria monocytogenes survival. Traffic. 6 (2005) 252-265.
[73]. C. Alvarez-Dominguez, F. Madrazo-Toca, L. Fernandez-Prieto, J. Vandekerckhove, E. Pareja, R. Tobes, M.T. Gomez-Lopez, E. Del Cerro-Vadillo, M. Fresno, F. Leyva-Cobian, E. Carrasco-Marin. Characterization of a Listeria monocytogenes protein interfering with Rab5a. Traffic. 9 (2008) 325-337.
[74]. M.R. Terebiznik, C.L. Vazquez, K. Torbicki, D. Banks, T. Wang, W. Hong, S.R. Blanke, M.I. Colombo, N.L. Jones. Helicobacter pylori VacA toxin promotes bacterial intracellular survival in gastric epithelial cells. Infect. Immun. 74 (2006) 6599-6614.
[75]. J.L. Murray, M. Mavrakis, N.J. McDonald, M. Yilla, J. Sheng, W.J. Bellini, L. Zhao, J.M. Le Doux, M.W. Shaw, C.C. Luo, J. Lippincott-Schwartz, A. Sanchez, D.H. Rubin, T.W. Hodge. Rab9 GTPase is required for replication of human immunodeficiency virus type 1, filoviruses, and measles virus. J. Virol. 79 (2005) 11742-11751.
[76]. S. Nydegger, M. Foti, A. Derdowski, P. Spearman, M. Thali. HIV-1 egress is gated through late endosomal membranes. Traffic. 4 (2003) 902-910.
[77]. A. Ono, E.O. Freed. Cell-type-dependent targeting of human immunodeficiency virus type 1 assembly to the plasma membrane and the multivesicular body. J. Virol. 78 (2004) 1552-1563.
|
Language: | English.
|
Document Type: | Review Article.
|
Journal Subset: | Clinical Medicine. Life & Biomedical Sciences.
|
ISSN: | 0014-4827
|
DOI Number: | https://dx.doi.org/10.1016/j.yex...- ouverture dans une nouvelle fenêtre
|
Annotation(s) | |
|
|