A therapeutic chemical chaperone inhibits cholera intoxication and unfolding/translocation of the cholera toxin a1 subunit

PLoS ONE

Volumn 6, Issue 4, 2011, Pages

  Taylor, Michael ^a   Banerjee, Tuhina ^a   Navarro Garcia, Fernando ^b   Huerta, Jazmin ^b   Massey, Shane ^a   Burlingame, Mansfield ^a   Pande, Abhay H ^a   Tatulian, Suren A ^c   Teter, Ken ^a  

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

^b DEPARTAMENTO DE FÍSICA   (Mexico)

^c UNIVERSITY OF CENTRAL FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 PHENYLBUTYRIC ACID; CHOLERA TOXIN; CHOLERA TOXIN A1 SUBUNIT; CHOLERA TOXIN A2 SUBUNIT; UNCLASSIFIED DRUG; 4-PHENYLBUTYRIC ACID; ARYLBUTYRIC ACID DERIVATIVE; DISULFIDE; PROTEIN DISULFIDE ISOMERASE; PROTEIN SUBUNIT;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CELLULAR DISTRIBUTION; CHOLERA; CIRCULAR DICHROISM; CONTROLLED STUDY; CYTOSOL; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; FLUORESCENCE SPECTROSCOPY; ILEUM; NONHUMAN; PROTEIN FOLDING; RAT; THERMAL UNFOLDING; ANIMAL; DRUG EFFECT; HELA CELL; HUMAN; METABOLISM; PATHOLOGY; PROTEIN BINDING; PROTEIN TRANSPORT; PROTEIN UNFOLDING; TEMPERATURE;

RATTUS;

ANIMALS; CHOLERA; CHOLERA TOXIN; CYTOSOL; DISULFIDES; ENDOPLASMIC RETICULUM; HELA CELLS; HUMANS; ILEUM; PHENYLBUTYRATES; PROTEIN BINDING; PROTEIN DISULFIDE-ISOMERASES; PROTEIN SUBUNITS; PROTEIN TRANSPORT; PROTEIN UNFOLDING; RATS; TEMPERATURE;

EID: 79955421850     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0018825     Document Type: Article

References (50)

1. Sandvig K, van Deurs B, (2002) Membrane traffic exploited by protein toxins. Annu Rev Cell Dev Biol 18: 1-24.
2. Watson P, Spooner RA, (2006) Toxin entry and trafficking in mammalian cells. Adv Drug Deliv Rev 58: 1581-1596.
3. Lord JM, Roberts LM, Lencer WI, (2005) Entry of protein toxins into mammalian cells by crossing the endoplasmic reticulum membrane: co-opting basic mechanisms of endoplasmic reticulum-associated degradation. Curr Top Microbiol Immunol 300: 149-168.
4. Hazes B, Read RJ, (1997) Accumulating evidence suggests that several AB-toxins subvert the endoplasmic reticulum-associated protein degradation pathway to enter target cells. Biochemistry 36: 11051-11054.
5. Deeks ED, Cook JP, Day PJ, Smith DC, Roberts LM, et al. (2002) The low lysine content of ricin A chain reduces the risk of proteolytic degradation after translocation from the endoplasmic reticulum to the cytosol. Biochemistry 41: 3405-3413.
6. Rodighiero C, Tsai B, Rapoport TA, Lencer WI, (2002) Role of ubiquitination in retro-translocation of cholera toxin and escape of cytosolic degradation. EMBO Rep 3: 1222-1227.
7. Worthington ZE, Carbonetti NH, (2007) Evading the proteasome: absence of lysine residues contributes to pertussis toxin activity by evasion of proteasome degradation. Infect Immun 75: 2946-2953.
8. De Haan L, Hirst TR, (2004) Cholera toxin: a paradigm for multi-functional engagement of cellular mechanisms (Review). Mol Membr Biol 21: 77-92.
9. Sanchez J, Holmgren J, (2008) Cholera toxin structure, gene regulation and pathophysiological and immunological aspects. Cell Mol Life Sci 65: 1347-1360.
10. Massey S, Banerjee T, Pande AH, Taylor M, Tatulian SA, et al. (2009) Stabilization of the tertiary structure of the cholera toxin A1 subunit inhibits toxin dislocation and cellular intoxication. J Mol Biol 393: 1083-1096.
11. Pande AH, Scaglione P, Taylor M, Nemec KN, Tuthill S, et al. (2007) Conformational instability of the cholera toxin A1 polypeptide. J Mol Biol 374: 1114-1128.
12. Surewicz WK, Leddy JJ, Mantsch HH, (1990) Structure, stability, and receptor interaction of cholera toxin as studied by Fourier-transform infrared spectroscopy. Biochemistry 29: 8106-8111.
13. Goins B, Freire E, (1988) Thermal stability and intersubunit interactions of cholera toxin in solution and in association with its cell-surface receptor ganglioside GM1. Biochemistry 27: 2046-2052.
14. Murayama T, Tsai SC, Adamik R, Moss J, Vaughan M, (1993) Effects of temperature on ADP-ribosylation factor stimulation of cholera toxin activity. Biochemistry 32: 561-566.
15. Ampapathi RS, Creath AL, Lou DI, Craft JW, Blanke SR, et al. (2008) Order-disorder-order transitions mediate the activation of cholera toxin. J Mol Biol 377: 748-760.
16. Banerjee T, Pande A, Jobling MG, Taylor M, Massey S, et al. (2010) Contribution of subdomain structure to the thermal stability of the cholera toxin A1 subunit. Biochemistry, 49: 8839-8846.
17. Perlmutter DH, (2002) Chemical chaperones: a pharmacological strategy for disorders of protein folding and trafficking. Pediatr Res 52: 832-836.
18. Maestri NE, Brusilow SW, Clissold DB, Bassett SS, (1996) Long-term treatment of girls with ornithine transcarbamylase deficiency. N Engl J Med 335: 855-859.
19. Homola J, (2003) Present and future of surface plasmon resonance biosensors. Anal Bioanal Chem 377: 528-539.
20. Majoul I, Ferrari D, Soling HD, (1997) Reduction of protein disulfide bonds in an oxidizing environment. The disulfide bridge of cholera toxin A-subunit is reduced in the endoplasmic reticulum. FEBS Lett 401: 104-108.
21. Orlandi PA, (1997) Protein-disulfide isomerase-mediated reduction of the A subunit of cholera toxin in a human intestinal cell line. J Biol Chem 272: 4591-4599.
22. Tsai B, Rodighiero C, Lencer WI, Rapoport TA, (2001) Protein disulfide isomerase acts as a redox-dependent chaperone to unfold cholera toxin. Cell 104: 937-948.
23. Teter K, Jobling MG, Sentz D, Holmes RK, (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.
24. Lencer WI, de Almeida JB, Moe S, Stow JL, Ausiello DA, et al. (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.
25. Orlandi PA, Curran PK, Fishman PH, (1993) Brefeldin A blocks the response of cultured cells to cholera toxin. Implications for intracellular trafficking in toxin action. J Biol Chem 268: 12010-12016.
26. Teter K, Allyn RL, Jobling MG, Holmes RK, (2002) Transfer of the cholera toxin A1 polypeptide from the endoplasmic reticulum to the cytosol is a rapid process facilitated by the endoplasmic reticulum-associated degradation pathway. Infect Immun 70: 6166-6171.
27. Ryu H, Smith K, Camelo SI, Carreras I, Lee J, et al. (2005) Sodium phenylbutyrate prolongs survival and regulates expression of anti-apoptotic genes in transgenic amyotrophic lateral sclerosis mice. J Neurochem 93: 1087-1098.
28. Vilatoba M, Eckstein C, Bilbao G, Smyth CA, Jenkins S, et al. (2005) Sodium 4-phenylbutyrate protects against liver ischemia reperfusion injury by inhibition of endoplasmic reticulum-stress mediated apoptosis. Surgery 138: 342-351.
29. Petri S, Kiaei M, Kipiani K, Chen J, Calingasan NY, et al. (2006) Additive neuroprotective effects of a histone deacetylase inhibitor and a catalytic antioxidant in a transgenic mouse model of amyotrophic lateral sclerosis. Neurobiol Dis 22: 40-49.
30. Welch WJ, Brown CR, (1996) Influence of molecular and chemical chaperones on protein folding. Cell Stress Chaperones 1: 109-115.
31. Rubenstein RC, Zeitlin PL, (2000) Sodium 4-phenylbutyrate downregulates Hsc70: implications for intracellular trafficking of DeltaF508-CFTR. Am J Physiol Cell Physiol 278: C259-267.
32. Choo-Kang LR, Zeitlin PL, (2001) Induction of HSP70 promotes DeltaF508 CFTR trafficking. Am J Physiol Lung Cell Mol Physiol 281: L58-68.
33. Basseri S, Lhotak S, Sharma AM, Austin RC, (2009) The chemical chaperone 4-phenylbutyrate inhibits adipogenesis by modulating the unfolded protein response. J Lipid Res 50: 2486-2501.
34. Bonapace G, Waheed A, Shah GN, Sly WS, (2004) Chemical chaperones protect from effects of apoptosis-inducing mutation in carbonic anhydrase IV identified in retinitis pigmentosa 17. Proc Natl Acad Sci U S A 101: 12300-12305.
35. Loffing J, Moyer BD, Reynolds D, Stanton BA, (1999) PBA increases CFTR expression but at high doses inhibits Cl(-) secretion in Calu-3 airway epithelial cells. Am J Physiol 277: L700-708.
36. Teter K, Holmes RK, (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.
37. Teter K, Jobling MG, Holmes RK, (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.
38. Taylor M, Navarro-Garcia F, Huerta J, Burress H, Massey S, et al. (2010) Hsp90 is required for transfer of the cholera toxin A1 subunit from the endoplasmic reticulum to the cytosol. J Biol Chem 285: 31261-31267.
39. Stechmann B, Bai SK, Gobbo E, Lopez R, Merer G, et al. (2010) Inhibition of retrograde transport protects mice from lethal ricin challenge. Cell 141: 231-242.
40. Collins AF, Pearson HA, Giardina P, McDonagh KT, Brusilow SW, et al. (1995) Oral sodium phenylbutyrate therapy in homozygous beta thalassemia: a clinical trial. Blood 85: 43-49.
41. Teckman JH, (2004) Lack of effect of oral 4-phenylbutyrate on serum alpha-1-antitrypsin in patients with alpha-1-antitrypsin deficiency: a preliminary study. J Pediatr Gastroenterol Nutr 39: 34-37.
42. Chang FH, Bourne HR, (1989) Cholera toxin induces cAMP-independent degradation of Gs. J Biol Chem 264: 5352-5357.
43. Kato J, Zhu J, Liu C, Moss J, (2007) Enhanced sensitivity to cholera toxin in ADP-ribosylarginine hydrolase-deficient mice. Mol Cell Biol 27: 5534-5543.
44. Wernick NL, De Luca H, Kam WR, Lencer WI, (2010) N-terminal Extension of the Cholera Toxin A1-chain Causes Rapid Degradation after Retrotranslocation from Endoplasmic Reticulum to Cytosol. J Biol Chem 285: 6145-6152.
45. Paton JC, Paton AW, (2006) Shiga toxin 'goes retro' in human primary kidney cells. Kidney Int 70: 2049-2051.
46. Hilger H, Pust S, von Figura G, Kaiser E, Stiles BG, et al. (2009) The long-lived nature of Clostridium perfringens iota toxin in mammalian cells induces delayed apoptosis. Infect Immun 77: 5593-5601.
47. Bech E, Jakobsen J, Orntoft TF, (1994) ELISA-type titertray assay of IgM anti-GM1 autoantibodies. Clin Chem 40: 1331-1334.
48. Lin LP, Huang LS, Lin CW, Lee CK, Chen JL, et al. (2005) Determination of binding constant of DNA-binding drug to target DNA by surface plasmon resonance biosensor technology. Curr Drug Targets Immune Endocr Metabol Disord 5: 61-72.
49. Teter K, Jobling MG, Holmes RK, (2004) Vesicular transport is not required for the cytoplasmic pool of cholera toxin to interact with the stimulatory alpha subunit of the heterotrimeric G protein. Infect Immun 72: 6826-6835.
50. Cantor CR, Schimmel PR, (1980) Biophysical chemistry part II: Techniques for the study of biological structure and function New York W.H. Freeman and Co.