Arf6-dependent intracellular trafficking of pasteurella multocida toxin and pH-dependent translocation from late endosomes

Toxins

Volumn 3, Issue 3, 2011, Pages 218-241

  Repella, Tana L ^a   Ho, Mengfei ^a   Chong, Tracy P M ^a   Bannai, Yuka ^a   Wilson, Brenda A ^a,b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Endocytosis; Intoxication; Translocation

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; BACTERIAL TOXIN; BREFELDIN A; CHOLERA TOXIN; CYTOCHALASIN D; NOCODAZOLE; PHOSPHATIDYLINOSITOL 3 KINASE; TRANSFERRIN;

ACIDIFICATION; ACTIN FILAMENT; BACTERIAL VIRULENCE; CONTROLLED STUDY; CYTOTOXICITY; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENDOSOME; ENZYME ACTIVITY; INTERNALIZATION; INTRACELLULAR SIGNALING; INTRACELLULAR TRANSPORT; MICROTUBULE; PASTEURELLA MULTOCIDA; PH MEASUREMENT; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; REVIEW; TOXIN ANALYSIS;

3T3 CELLS; ADP-RIBOSYLATION FACTORS; ANIMALS; BACTERIAL PROTEINS; BACTERIAL TOXINS; BLOTTING, WESTERN; CELL CULTURE TECHNIQUES; CHOLERA TOXIN; ENDOCYTOSIS; ENDOSOMES; HEK293 CELLS; HUMANS; HYDROGEN-ION CONCENTRATION; MICE; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; PASTEURELLA MULTOCIDA; PROTEIN TRANSPORT; TRANSFERRIN;

PASTEURELLA MULTOCIDA;

EID: 79953245323     PISSN: None     EISSN: 20726651     Source Type: Journal    
DOI: 10.3390/toxins3030218     Document Type: Review

References (65)

1. Wilson, B.A.; Ho, M. Pasteurella multocida toxin. In The Comprehensive Sourcebook of Bacterial Protein Toxins; Alouf, J.E., Popoff, M.R., Eds.; Elsevier Science Publishers B.V.: Amsterdam, The Netherlands, 2006; pp. 430-447.
2. Harper, M.; Boyce, J.D.; Adler, B. Pasteurella multocida pathogenesis: 125 years after Pasteur. FEMS Microbiol. Lett. 2006, 265, 1-10.
3. Arashima, Y.; Kumasaka, K. Pasteurellosis as zoonosis. Intern. Med. 2005, 44, 692-693.
4. Lax, A.J.; Chanter, N. Cloning of the toxin gene from Pasteurella multocida and its role in atrophic rhinitis. J. Gen. Microbiol. 1990, 136, 81-87.
5. Foged, N.T. Pasteurella multocida toxin. The characterisation of the toxin and its significance in the diagnosis and prevention of progressive atrophic rhinitis in pigs. APMIS Suppl. 1992, 25, 1-56.
6. Cheville, N.F.; Rimler, R.B. A protein toxin from Pasteurella multocida type D causes acute and chronic hepatic toxicity in rats. Vet. Pathol. 1989, 26, 148-157.
7. Thurston, J.R.; Rimler, R.B.; Ackermann, M.R.; Cheville, N.F. Use of rats to compare atrophic rhinitis vaccines for protection against effects of heat-labile protein toxin produced by Pasteurella multocida serogroup D. Vet. Immunol. Immunopathol. 1992, 33, 155-162.
8. Aminova, L.R.; Wilson, B.A. Calcineurin-independent inhibition of 3T3-L1 adipogenesis by Pasteurella multocida toxin: Suppression of Notch1, stabilization of beta-catenin and pre-adipocyte factor 1. Cell Microbiol. 2007, 9, 2485-2496.
9. Bagley, K.C.; Abdelwahab, S.F.; Tuskan, R.G.; Lewis, G.K. Pasteurella multocida toxin activates human monocyte-derived and murine bone marrow-derived dendritic cells in vitro but suppresses antibody production in vivo. Infect. Immun. 2005, 73, 413-421.
10. Lax, A.J. Opinion: Bacterial toxins and cancer-a case to answer? Nat. Rev. Microbiol. 2005, 3, 343-349.
11. Wilson, B.A.; Ho, M. Pasteurella multocida toxin as a tool for studying Gq signal transduction. Rev. Physiol. Biochem. Pharmacol. 2004, 152, 93-109.
12. Kitadokoro, K.; Kamitani, S.; Miyazawa, M.; Hanajima-Ozawa, M.; Fukui, A.; Miyake, M.; Horiguchi, Y. Crystal structures reveal a thiol protease-like catalytic triad in the C-terminal region of Pasteurella multocida toxin. Proc. Natl. Acad. Sci. USA 2007, 104, 5139-5144.
13. Aminova, L.R.; Luo, S.; Bannai, Y.; Ho, M.; Wilson, B.A. The C3 domain of Pasteurella multocida toxin is the minimal domain responsible for activation of Gq-dependent calcium and mitogenic signaling. Protein Sci. 2008, 17, 945-949.
14. Orth, J.H.; Preuss, I.; Fester, I.; Schlosser, A.; Wilson, B.A.; Aktories, K. Pasteurella multocida toxin activation of heterotrimeric G proteins by deamidation. Proc. Natl. Acad. Sci. USA 2009, 106, 7179-7184.
15. Fromm, C.; Coso, O.A.; Montaner, S.; Xu, N.; Gutkind, J.S. The small GTP-binding protein Rho links G protein-coupled receptors and Galpha12 to the serum response element and to cellular transformation. Proc. Natl. Acad. Sci. USA 1997, 94, 10098-10103.
16. Hill, C.S.; Wynne, J.; Treisman, R. The Rho family GTPases RhoA, Rac1, and CDC42Hs regulate transcriptional activation by SRF. Cell 1995, 81, 1159-1170.
17. Wilson, B.A.; Ho, M. Recent insights into Pasteurella multocida toxin and other G-protein-modulating bacterial toxins. Future Microbiol. 2010, 5, 1185-1201.
18. Rozengurt, E.; Higgins, T.; Chanter, N.; Lax, A.J.; Staddon, J.M. Pasteurella multocida toxin: Potent mitogen for cultured fibroblasts. Proc. Natl. Acad. Sci. USA 1990, 87, 123-127.
19. Bowman, E.J.; Siebers, A.; Altendorf, K. Bafilomycins: A class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc. Natl. Acad. Sci. USA 1988, 85, 7972-7976.
20. Baldwin, M.R.; Lakey, J.H.; Lax, A.J. Identification and characterization of the Pasteurella multocida toxin translocation domain. Mol. Microbiol. 2004, 54, 239-250.
21. Smyth, M.G.; Pickersgill, R.W.; Lax, A.J. The potent mitogen Pasteurella multocida toxin is highly resistant to proteolysis but becomes susceptible at lysosomal pH. FEBS Lett. 1995, 360, 62-66.
22. Maranda, B.; Brown, D.; Bourgoin, S.; Casanova, J.E.; Vinay, P.; Ausiello, D.A.; Marshansky, V. Intra-endosomal pH-sensitive recruitment of the Arf-nucleotide exchange factor ARNO and Arf6 from cytoplasm to proximal tubule endosomes. J. Biol. Chem. 2001, 276, 18540-18550.
23. Hurtado-Lorenzo, A.; Skinner, M.; El Annan, J.; Futai, M.; Sun-Wada, G.H.; Bourgoin, S.; Casanova, J.; Wildeman, A.; Bechoua, S.; Ausiello, D.A.; Brown, D.; Marshansky, V. V-ATPase interacts with ARNO and Arf6 in early endosomes and regulates the protein degradative pathway. Nat. Cell Biol. 2006, 8, 124-136.
24. Peters, P.J.; Hsu, V.W.; Ooi, C.E.; Finazzi, D.; Teal, S.B.; Oorschot, V.; Donaldson, J.G.; Klausner, R.D. Overexpression of wild-type and mutant ARF1 and ARF6: Distinct perturbations of nonoverlapping membrane compartments. J. Cell Biol. 1995, 128, 1003-1017.
25. Christoforidis, S.; McBride, H.M.; Burgoyne, R.D.; Zerial, M. The Rab5 effector EEA1 is a core component of endosome docking. Nature 1999, 397, 621-625.
26. Zerial, M.; McBride, H. Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2001, 2, 107-117.
27. Maxfield, F.R.; McGraw, T.E. Endocytic recycling. Nat. Rev. Mol. Cell Biol. 2004, 5, 121-132.
28. Naslavsky, N.; Weigert, R.; Donaldson, J.G. Convergence of non-clathrin- and clathrin-derived endosomes involves Arf6 inactivation and changes in phosphoinositides. Mol. Biol. Cell 2003, 14, 417-431.
29. Widera, A.; Kim, K.J.; Crandall, E.D.; Shen, W.C. Transcytosis of GCSF-transferrin across rat alveolar epithelial cell monolayers. Pharm. Res. 2003, 20, 1231-1238.
30. Brown, F.D.; Rozelle, A.L.; Yin, H.L.; Balla, T.; Donaldson, J.G. Phosphatidylinositol 4,5-bisphosphate and Arf6-regulated membrane traffic. J. Cell Biol. 2001, 154, 1007-1017.
31. Chies, R.; Nobbio, L.; Edomi, P.; Schenone, A.; Schneider, C.; Brancolini, C. Alterations in the Arf6-regulated plasma membrane endosomal recycling pathway in cells overexpressing the tetraspan protein Gas3/PMP22. J. Cell Sci. 2003, 116, 987-999.
32. D'Souza-Schorey, C.; van Donselaar, E.; Hsu, V.W.; Yang, C.; Stahl, P.D.; Peters, P.J. ARF6 targets recycling vesicles to the plasma membrane: Insights from an ultrastructural investigation. J. Cell Biol. 1998, 140, 603-616.
33. D'Souza-Schorey, C.; Li, G.; Colombo, M.I.; Stahl, P.D. A regulatory role for ARF6 in receptor-mediated endocytosis. Science 1995, 267, 1175-1178.
34. El Hage, T.; Merlen, C.; Fabrega, S.; Authier, F. Role of receptor-mediated endocytosis, endosomal acidification and cathepsin D in cholera toxin cytotoxicity. FEBS J. 2007, 274, 2614-2629.
35. Kahn, R.A.; Gilman, A.G. The protein cofactor necessary for ADP-ribosylation of Gs by cholera toxin is itself a GTP binding protein. J. Biol. Chem. 1986, 261, 7906-7911.
36. Noda, M.; Tsai, S.C.; Adamik, R.; Moss, J.; Vaughan, M. Mechanism of cholera toxin activation by a guanine nucleotide-dependent 19 kDa protein. Biochim. Biophys. Acta 1990, 1034, 195-199.
37. O'Neal, C.J.; Jobling, M.G.; Holmes, R.K.; Hol, W.G. Structural basis for the activation of cholera toxin by human ARF6-GTP. Science 2005, 309, 1093-1096.
38. Merlen, C.; Fayol-Messaoudi, D.; Fabrega, S.; El Hage, T.; Servin, A.; Authier, F. Proteolytic activation of internalized cholera toxin within hepatic endosomes by cathepsin D. Febs J. 2005, 272, 4385-4397.
39. Lencer, W.I.; Constable, C.; Moe, S.; Jobling, M.G.; Webb, H.M.; Ruston, S.; Madara, J.L.; Hirst, T.R.; Holmes, R.K. Targeting of cholera toxin and Escherichia coli heat labile toxin in polarized epithelia: role of COOH-terminal KDEL. J. Cell Biol. 1995, 131, 951-962.
40. Fujiwara, T.; Oda, K.; Yokota, S.; Takatsuki, A.; Ikehara, Y., Brefeldin A causes disassembly of the Golgi complex and accumulation of secretory proteins in the endoplasmic reticulum. J. Biol. Chem. 1988, 263, 18545-18552.
41. Orlandi, P.A.; Curran, P.K.; Fishman, P.H. Brefeldin A blocks the response of cultured cells to cholera toxin. Implications for intracellular trafficking in toxin action. J. Biol. Chem. 1993, 268, 12010-12016.
42. Bomsel, M.; Parton, R.; Kuznetsov, S.A.; Schroer, T.A.; Gruenberg, J. Microtubule- and motor-dependent fusion in vitro between apical and basolateral endocytic vesicles from MDCK cells. Cell 1990, 62, 719-731.
43. Kingston, R.E.; Chen, C.A.; Rose, J.K. Calcium phosphate transfection. Curr. Protoc. Mol. Biol. 2003, 9, 1-11.
44. Hsu, V.W.; Prekeris, R. Transport at the recycling endosome. Curr. Opin. Cell Biol. 2010, 22, 528-534.
45. Pullinger, G.D.; Sowdhamini, R.; Lax, A.J. Localization of functional domains of the mitogenic toxin of Pasteurella multocida. Infect. Immun. 2001, 69, 7839-7850.
46. Vlahos, C.J.; Matter, W.F.; Hui, K.Y.; Brown, R.F. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phensyl-4H-1-benzopyran-4-one (LY294002). J. Biol. Chem. 1994, 269, 5241-5248.
47. Ohkuma, S.; Poole, B. Fluorescence probe measurement of the intralysosomal pH in living cells and the perturbation of pH by various agents. Proc. Natl. Acad. Sci. USA 1978, 75, 3327-3331.
48. van Weert, A.W.; Dunn, K.W.; Gueze, H.J.; Maxfield, F.R.; Stoorvogel, W. Transport from late endosomes to lysosomes, but not sorting of integral membrane proteins in endosomes, depends on the vacuolar proton pump. J. Cell Biol. 1995, 130, 821-834.
49. Lencer, W.I.; Strohmeier, G.; Moe, S.; Carlson, S.L.; Constable, C.T.; Madara, J.L. Signal transduction by cholera toxin: Processing in vesicular compartments does not require acidification. Am. J. Physiol. 1995, 269, G548-G557.
50. Sugimoto, Y.; Ninomiya, H.; Ohsaki, Y.; Higaki, K.; Davies, J.P.; Ioannou, Y.A.; Ohno, K. Accumulation of cholera toxin and GM1 ganglioside in the early endosome of Niemann-Pick C1-deficient cells. Proc. Natl. Acad. Sci. USA 2001, 98, 12391-12396.
51. Macia, E.; Luton, F.; Partisani, M.; Cherfils, J.; Chardin, P.; Franco, M. The GDP-bound form of Arf6 is located at the plasma membrane. J. Cell Sci. 2004, 117, 2389-2398.
52. D'Souza-Schorey, C.; Stahl, P.D. Myristoylation is required for the intracellular localization and endocytic function of ARF6. Exp. Cell Res. 1995, 221, 153-159.
53. Massol, R.H.; Larsen, J.E.; Fujinaga, Y.; Lencer, W.I.; Kirchhausen, T. Cholera toxin toxicity does not require functional Arf6- and dynamin-dependent endocytic pathways. Mol. Biol. Cell 2004, 15, 3631-3641.
54. Misumi, Y.; Misumi, Y.; Miki, K.; Takatsuki, A.; Tamura, G.; Ikehara, Y. Novel blockade by brefeldin A of intracellular transport of secretory proteins in cultured rat hepatocytes. J. Biol. Chem. 1986, 261, 11398-11403.
55. Donaldson, J.G.; Lippincott-Schwartz, J.; Bloom, G.S.; Kreis, T.E.; Klausner, R.D. Dissociation of a 110-kD peripheral membrane protein from the Golgi apparatus is an early event in brefeldin A action. J. Cell Biol. 1990, 111, 2295-2306.
56. Lippincott-Schwartz, J.; Donaldson, J.G.; Schweizer, A.; Berger, E.G.; Hauri, H.P.; Yuan, L.C.; Klausner, R.D. Microtubule-dependent retrograde transport of proteins into the ER in the presence of brefeldin A suggests an ER recycling pathway. Cell 1990, 60, 821-836.
57. Lippincott-Schwartz, J.; Yuan, L.; Tipper, C.; Amherdt, M.; Orci, L.; Klausner, R.D. Brefeldin A's effects on endosomes, lysosomes, and the TGN suggest a general mechanism for regulating organelle structure and membrane traffic. Cell 1991, 67, 601-616.
58. Zhang, Q.; Cox, D.; Tseng, C.C.; Donaldson, J.G.; Greenberg, S. A requirement for ARF6 in Fcgamma receptor-mediated phagocytosis in macrophages. J. Biol. Chem. 1998, 273, 19977-19981.
59. Santy, L.C. Characterization of a fast cycling ADP-ribosylation factor 6 mutant. J. Biol. Chem. 2002, 277, 40185-40188.
60. Sandvig, K.; Olsnes, S. Diphtheria toxin entry into cells is facilitated by low pH. J. Cell Biol. 1980, 87, 828-832.
61. Skretting, G.; Torgersen, M.L.; van Deurs, B.; Sandvig, K. Endocytic mechanisms responsible for uptake of GPI-linked diphtheria toxin receptor. J. Cell Sci. 1999, 112, 3899-3909.
62. Antignani, A.; Youle, R.J. Endosome fusion induced by diphtheria toxin translocation domain. Proc. Natl. Acad. Sci. USA 2008, 105, 8020-8025.
63. Argent, R.H.; McGarr, C.; Atherton, J.C. Brefeldin A enhances Helicobacter pylori vacuolating cytotoxin-induced vacuolation of epithelial cells. FEMS Microbiol. Lett. 2004, 237, 163-170.
64. Wood, S.A.; Brown, W.J. The morphology but not the function of endosomes and lysosomes is altered by brefeldin A. J. Cell Biol. 1992, 119, 273-285.
65. Wood, S.A.; Park, J.E.; Brown, W.J. Brefeldin A causes a microtubule-mediated fusion of the trans-Golgi network and early endosomes. Cell 1991, 67, 591-600.