ADP-ribosylation factor 6 acts as an allosteric activator for the folded but not disordered cholera toxin A1 polypeptide

Molecular Microbiology

Volumn 94, Issue 4, 2014, Pages 898-912

  Banerjee, Tuhina ^a,c   Taylor, Michael ^c   Jobling, Michael G ^d   Burress, Helen ^c   Yang, Zhijie ^b,d   Serrano, Albert ^c   Holmes, Randall K ^d   Tatulian, Suren A ^e   Teter, Ken ^c  

^a PITTSBURG STATE UNIVERSITY   (United States)

^b Atila Biosystems Inc   (United States)

^c UNIVERSITY OF CENTRAL FLORIDA COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF CENTRAL FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; CHOLERA TOXIN; CHOLERA TOXIN A1; PROTEINASE; UNCLASSIFIED DRUG; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; ADP-RIBOSYLATION FACTOR 6;

ALLOSTERISM; ARTICLE; CONTROLLED STUDY; INFRARED SPECTROSCOPY; LIPID RAFT; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STABILITY; TEMPERATURE DEPENDENCE; TOXIN ANALYSIS; CELL MEMBRANE; CHEMISTRY; METABOLISM; STRUCTURE ACTIVITY RELATION; TEMPERATURE;

ADP-RIBOSYLATION FACTORS; ALLOSTERIC REGULATION; CHOLERA TOXIN; MEMBRANE MICRODOMAINS; PROTEIN CONFORMATION; PROTEIN FOLDING; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; STRUCTURE-ACTIVITY RELATIONSHIP; TEMPERATURE;

EID: 84912126924     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12807     Document Type: Article

References (57)

1. Allen, J.A., Halverson-Tamboli, R.A., and Rasenick, M.M. (2007) Lipid raft microdomains and neurotransmitter signaling. Nat Rev Neurosci 8: 128-140.
2. Ampapathi, R.S., Creath, A.L., Lou, D.I., Craft, J.W., Jr, Blanke, S.R., and Legge, G.B. (2008) Order-disorder-order transitions mediate the activation of cholera toxin. J Mol Biol 377: 748-760.
3. Banerjee, T., Pande, A., Jobling, M.G., Taylor, M., Massey, S., Holmes, R.K., etal. (2010) Contribution of subdomain structure to the thermal stability of the cholera toxin A1 subunit. Biochemistry 49: 8839-8846.
4. Bernardi, K.M., Forster, M.L., Lencer, W.I., and Tsai, B. (2008) Derlin-1 facilitates the retro-translocation of cholera toxin. Mol Biol Cell 19: 877-884.
5. Bernardi, K.M., Williams, J.M., Kikkert, M., van Voorden, S., Wiertz, E.J., Ye, Y., and Tsai, B. (2010) The E3 ubiquitin ligases Hrd1 and gp78 bind to and promote cholera toxin retro-translocation. Mol Biol Cell 21: 140-151.
6. Bobak, D.A., Bliziotes, M.M., Noda, M., Tsai, S.C., Adamik, R., and Moss, J. (1990) Mechanism of activation of cholera toxin by ADP-ribosylation factor (ARF): both low- and high-affinity interactions of ARF with guanine nucleotides promote toxin activation. Biochemistry 29: 855-861.
7. Cho, J.A., Chinnapen, D.J., Aamar, E., Welscher, Y.M., Lencer, W.I., and Massol, R. (2012) Insights on the trafficking and retro-translocation of glycosphingolipid-binding bacterial toxins. Front Cell Infect Microbiol 2: 51. doi:10.3389/fcimb.2012.00051
8. Dixit, G., Mikoryak, C., Hayslett, T., Bhat, A., and Draper, R.K. (2008) Cholera toxin up-regulates endoplasmic reticulum proteins that correlate with sensitivity to the toxin. Exp Biol Med (Maywood) 233: 163-175.
9. 2+ levels. J Biol Chem 270: 1337-1341.
10. Haun, R.S., Tsai, S.C., Adamik, R., Moss, J., and Vaughan, M. (1993) Effect of myristoylation on GTP-dependent binding of ADP-ribosylation factor to Golgi. J Biol Chem 268: 7064-7068.
11. Hazes, B., and Read, R.J. (1997) Accumulating evidence suggests that several AB-toxins subvert the endoplasmic reticulum-associated protein degradation pathway to enter target cells. Biochemistry 36: 11051-11054.
12. Honda, A., Al-Awar, O.S., Hay, J.C., and Donaldson, J.G. (2005) Targeting of Arf-1 to the early Golgi by membrin, an ER-Golgi SNARE. J Cell Biol 168: 1039-1051.
13. Horton, R.M., Cai, Z.L., Ho, S.N., and Pease, L.R. (1990) Gene splicing by overlap extension: tailor-made genes using the polymerase chain reaction. Biotechniques 8: 528-535.
14. Jobling, M.G., and Holmes, R.K. (2000) Identification of motifs in cholera toxin A1 polypeptide that are required for its interaction with human ADP-ribosylation factor 6 in a bacterial two-hybrid system. Proc Natl Acad Sci USA 97: 14662-14667.
15. Jobling, M.G., and Holmes, R.K. (2001) Biological and biochemical characterization of variant A subunits of cholera toxin constructed by site-directed mutagenesis. J Bacteriol 183: 4024-4032.
16. Kahn, R.A., and Gilman, A.G. (1984) Purification of a protein cofactor required for ADP-ribosylation of the stimulatory regulatory component of adenylate cyclase by cholera toxin. J Biol Chem 259: 6228-6234.
17. Kahn, R.A., and Gilman, A.G. (1986) The protein cofactor necessary for ADP-ribosylation of Gs by cholera toxin is itself a GTP binding protein. J Biol Chem 261: 7906-7911.
18. Kamata, K., Manno, S., Ozaki, M., and Takakuwa, Y. (2008) Functional evidence for presence of lipid rafts in erythrocyte membranes: Gsalpha in rafts is essential for signal transduction. Am J Hematol 83: 371-375.
19. Lai, C.Y., Xia, Q.C., and Salotra, P.T. (1983) Location and amino acid sequence around the ADP-ribosylation site in the cholera toxin active subunit A1. Biochem Biophys Res Commun 116: 341-348.
20. Lencer, W.I., de Almeida, J.B., Moe, S., Stow, J.L., Ausiello, D.A., and Madara, J.L. (1993) Entry of cholera toxin into polarized human intestinal epithelial cells. Identification of an early brefeldin A sensitive event required for A1-peptide generation. J Clin Invest 92: 2941-2951.
21. Massey, S., Banerjee, T., Pande, A.H., Taylor, M., Tatulian, S.A., and Teter, K. (2009) Stabilization of the tertiary structure of the cholera toxin A1 subunit inhibits toxin dislocation and cellular intoxication. J Mol Biol 393: 1083-1096.
22. Menetrey, J., Macia, E., Pasqualato, S., Franco, M., and Cherfils, J. (2000) Structure of Arf6-GDP suggests a basis for guanine nucleotide exchange factors specificity. Nat Struct Biol 7: 466-469.
23. Morinaga, N., Kaihou, Y., Vitale, N., Moss, J., and Noda, M. (2001) Involvement of ADP-ribosylation factor 1 in cholera toxin-induced morphological changes of Chinese hamster ovary cells. J Biol Chem 276: 22838-22843.
24. Moss, J., and Vaughan, M. (1995) Structure and function of ARF proteins: activators of cholera toxin and critical components of intracellular vesicular transport processes. J Biol Chem 270: 12327-12330.
25. Murayama, T., Tsai, S.C., Adamik, R., Moss, J., and Vaughan, M. (1993) Effects of temperature on ADP-ribosylation factor stimulation of cholera toxin activity. Biochemistry 32: 561-566.
26. Oh, P., and Schnitzer, J.E. (2001) Segregation of heterotrimeric G proteins in cell surface microdomains. G(q) binds caveolin to concentrate in caveolae, whereas G(i) and G(s) target lipid rafts by default. Mol Biol Cell 12: 685-698.
27. O'Neal, C.J., Amaya, E.I., Jobling, M.G., Holmes, R.K., and Hol, W.G. (2004) Crystal structures of an intrinsically active cholera toxin mutant yield insight into the toxin activation mechanism. Biochemistry 43: 3772-3782.
28. O'Neal, C.J., Jobling, M.G., Holmes, R.K., and Hol, W.G. (2005) Structural basis for the activation of cholera toxin by human ARF6-GTP. Science 309: 1093-1096.
29. Pande, A.H., Scaglione, P., Taylor, M., Nemec, K.N., Tuthill, S., Moe, D., etal. (2007) Conformational instability of the cholera toxin A1 polypeptide. J Mol Biol 374: 1114-1128.
30. Pasqualato, S., Menetrey, J., Franco, M., and Cherfils, J. (2001) The structural GDP/GTP cycle of human Arf6. EMBO Rep 2: 234-238.
31. Price, S.R., Welsh, C.F., Haun, R.S., Stanley, S.J., Moss, J., and Vaughan, M. (1992) Effects of phospholipid and GTP on recombinant ADP-ribosylation factors (ARFs). Molecular basis for differences in requirements for activity of mammalian ARFs. J Biol Chem 267: 17766-17772.
32. Ray, S., Taylor, M., Banerjee, T., Tatulian, S.A., and Teter, K. (2012) Lipid rafts alter the stability and activity of the cholera toxin A1 subunit. J Biol Chem 287: 30395-30405.
33. Reddy, S., Taylor, M., Zhao, M., Cherubin, P., Geden, S., Ray, S., etal. (2013) Grape extracts inhibit multiple events in the cell biology of cholera intoxication. PLoS ONE 8: e73390.
34. Richards, A.A., Stang, E., Pepperkok, R., and Parton, R.G. (2002) Inhibitors of COP-mediated transport and cholera toxin action inhibit simian virus 40 infection. Mol Biol Cell 13: 1750-1764.
35. Rodighiero, C., Tsai, B., Rapoport, T.A., and Lencer, W.I. (2002) Role of ubiquitination in retro-translocation of cholera toxin and escape of cytosolic degradation. EMBO Rep 3: 1222-1227.
36. Saslowsky, D.E., Cho, J.A., Chinnapen, H., Massol, R.H., Chinnapen, D.J., Wagner, J.S., etal. (2010) Intoxication of zebrafish and mammalian cells by cholera toxin depends on the flotillin/reggie proteins but not Derlin-1 or -2. J Clin Invest 120: 4399-4409.
37. Schmitz, A., Herrgen, H., Winkeler, A., and Herzog, V. (2000) Cholera toxin is exported from microsomes by the Sec61p complex. J Cell Biol 148: 1203-1212.
38. Soman, G., Narayanan, J., Martin, B.L., and Graves, D.J. (1986) Use of substituted (benzylidineamino)guanidines in the study of guanidino group specific ADP-ribosyltransferase. Biochemistry 25: 4113-4119.
39. Swaisgood, H.E. (1993) Review and update of casein chemistry. J Dairy Sci 76: 3054-3061.
40. Tatulian, S.A. (2010) Structural analysis of proteins by isotope-edited FTIR spectroscopy. Spectrosc Int J 24: 37-43.
41. Tatulian, S.A. (2013) Structural characterization of membrane proteins and peptides by FTIR and ATR-FTIR spectroscopy. In Lipid-Protein Interactions: Methods and Protocols. Kleinschmidt, J.H. (ed.). New York: Humana Press, pp. 177-218.
42. Tatulian, S.A., Chen, B., Li, J., Negash, S., Middaugh, C.R., Bigelow, D.J., and Squier, T.C. (2002) The inhibitory action of phospholamban involves stabilization of alpha-helices within the Ca-ATPase. Biochemistry 41: 741-751.
43. Tatulian, S.A., Qin, S., Pande, A.H., and He, X. (2005) Positioning membrane proteins by novel protein engineering and biophysical approaches. J Mol Biol 351: 939-947.
44. Taylor, M., Banerjee, T., Navarro-Garcia, F., Huerta, J., Massey, S., Burlingame, M., etal. (2011a) A therapeutic chemical chaperone inhibits cholera intoxication and unfolding/translocation of the cholera toxin A1 subunit. PLoS ONE 6: e18825.
45. Taylor, M., Banerjee, T., Ray, S., Tatulian, S.A., and Teter, K. (2011b) Protein disulfide isomerase displaces the cholera toxin A1 subunit from the holotoxin without unfolding the A1 subunit. J Biol Chem 286: 22090-22100.
46. Taylor, M., Banerjee, T., VanBennekom, N., and Teter, K. (2012) Detection of toxin translocation into the host cytosol by surface plasmon resonance. J Vis Exp (59): e3686. doi:10.3791/3686
47. Taylor, M., Burress, H., Banerjee, T., Ray, S., Curtis, D., Tatulian, S.A., and Teter, K. (2014) Substrate-induced unfolding of protein disulfide isomerase displaces the cholera toxin A1 subunit from its holotoxin. PLoS Pathog 10: e1003925.
48. Teter, K., and Holmes, R.K. (2002) Inhibition of endoplasmic reticulum-associated degradation in CHO cells resistant to cholera toxin, Pseudomonas aeruginosa exotoxin A, and ricin. Infect Immun 70: 6172-6179.
49. Teter, K., Jobling, M.G., and Holmes, R.K. (2003) A class of mutant CHO cells resistant to cholera toxin rapidly degrades the catalytic polypeptide of cholera toxin and exhibits increased endoplasmic reticulum-associated degradation. Traffic 4: 232-242.
50. Teter, K., Jobling, M.G., Sentz, D., and Holmes, R.K. (2006) The cholera toxin A13 subdomain is essential for interaction with ADP-ribosylation factor 6 and full toxic activity but is not required for translocation from the endoplasmic reticulum to the cytosol. Infect Immun 74: 2259-2267.
51. Tsai, B., Rodighiero, C., Lencer, W.I., and Rapoport, T.A. (2001) Protein disulfide isomerase acts as a redox-dependent chaperone to unfold cholera toxin. Cell 104: 937-948.
52. Tsai, S.C., Noda, M., Adamik, R., Moss, J., and Vaughan, M. (1987) Enhancement of choleragen ADP-ribosyltransferase activities by guanyl nucleotides and a 19-kDa membrane protein. Proc Natl Acad Sci USA 84: 5139-5142.
53. Tsai, S.C., Noda, M., Adamik, R., Chang, P.P., Chen, H.C., Moss, J., and Vaughan, M. (1988) Stimulation of choleragen enzymatic activities by GTP and two soluble proteins purified from bovine brain. J Biol Chem 263: 1768-1772.
54. Vembar, S.S., and Brodsky, J.L. (2008) One step at a time: endoplasmic reticulum-associated degradation. Nat Rev Mol Cell Biol 9: 944-957.
55. Weiss, O., Holden, J., Rulka, C., and Kahn, R.A. (1989) Nucleotide binding and cofactor activities of purified bovine brain and bacterially expressed ADP-ribosylation factor. J Biol Chem 264: 21066-21072.
56. Welsh, C.F., Moss, J., and Vaughan, M. (1994) ADP-ribosylation factors: a family of approximately 20-kDa guanine nucleotide-binding proteins that activate cholera toxin. Mol Cell Biochem 138: 157-166.
57. Wernick, N.L.B., Chinnapen, D.J.-F., Cho, J.A., and Lencer, W.I. (2010) Cholera toxin: an intracellular journey into the cytosol by way of the endoplasmic reticulum. Toxins 2: 310-325.