Methylated trivalent arsenicals are potent inhibitors of glucose stimulated insulin secretion by murine pancreatic islets

Toxicology and Applied Pharmacology

Volumn 267, Issue 1, 2013, Pages 11-15

  Douillet, Christelle ^a   Currier, Jenna ^b   Saunders, Jesse ^a   Bodnar, Wanda M ^c   Matoušek, Tomáš ^d   Stýblo, Miroslav ^a  

^a University of North Carolina   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c University of North Carolina at Chapel Hill   (United States)

^d INSTITUTE OF ANALYTICAL CHEMISTRY   (Czech Republic)

Author keywords

Cells; Arsenic; Diabetes; Insulin secretion; Isolated pancreatic islets

Indexed keywords

ARSENIC; ARSENIC TRIOXIDE; DIMETHYLARSINITE; GLUCOSE; INSULIN; METHYLARSONITE; ORGANOARSENIC DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE; CELL VACUOLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; IC 50; INCUBATION TIME; INSULIN RELEASE; MALE; METABOLITE; MOUSE; NONHUMAN; PANCREAS ISLET; PANCREAS ISLET BETA CELL;

ANIMALS; ARSENICALS; CELLS, CULTURED; GLUCOSE; INSULIN; ISLETS OF LANGERHANS; MALE; METHYLATION; MICE; MICE, INBRED C57BL;

MURINAE; MUS;

EID: 84872203817     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2012.12.007     Document Type: Article

References (33)

1. ATSDR (Agency for Toxic Substances, Disease Registry) Toxicological Profile for Arsenic 2007, U.S. Department of Health and Human Services, Public Health Service, (August 2007. http://www.atsdr.cdc.gov/toxprofiles/tp.asp?id=22&tid=3).
2. BGS, DPHE Arsenic contamination of groundwater in Bangladesh. Final report. British Geological Survey Report WC/00/19 2001, vol. 2. D.G. Kinniburgh, P.L. Smedley (Eds.).
3. Boucher A., Lu D., Burgess S.C., Telemaque-Potts S., Jensen M.V., Mulder H., Wang M.Y., Unger R.H., Sherry A.D., Newgard C.B. Biochemical mechanisms of lipid-induced impairment of glucose-stimulated insulin secretion and reversal with a malate analog. J. Biol. Chem. 2004, 279:27,263-27,271.
4. Del Razo L.M., García-Vargas G.G., Valenzuela O.L., Hernandez-Castellanos E., Sánchez-Peña L.C., Drobná Z., Loomis D., Stýblo M. Exposure to arsenic in drinking water is associated with increased prevalence of diabetes: a cross-sectional study in the Zimapán and Lagunera regions in Mexico. Environ. Health 2011, 10:73.
5. Díaz-Villaseñor A., Sánchez-Soto M.C., Cebrián M.E., Ostrosky-Wegman P., Hiriart M. Sodium arsenite impairs insulin secretion and transcription in pancreatic beta-cells. Toxicol. Appl. Pharmacol. 2006, 214:30-34.
6. Díaz-Villaseñor A., Burns A.L., Salazar A.M., Sordo M., Hiriart M., Cebrián M.E., Ostrosky-Wegman P. Arsenite reduces insulin secretion in rat pancreatic beta-cells by decreasing the calcium-dependent calpain-10 proteolysis of SNAP-25. Toxicol. Appl. Pharmacol. 2008, 231:291-299.
7. Drobná Z., Waters S.B., Devesa V., Harmon A.W., Thomas D.J., Stýblo M. Metabolism and toxicity of As in human urothelial cells expressing rat arsenic (+3 oxidation state) methyltransferase. Toxicol. Appl. Pharmacol. 2005, 207:147-159.
8. Fu J., Woods C.G., Yehuda-Shnaidman E., Zhang Q., Wong V., Collins S., Sun G., Andersen M.E., Pi J. Low-level arsenic impairs glucose-stimulated insulin secretion in pancreatic beta cells: involvement of cellular adaptive response to oxidative stress. Environ. Health Perspect. 2010, 118:864-870.
9. Gresser M.J. ADP-arsenate. Formation by submitochondrial particles under phosphorylating conditions. J. Biol. Chem. 1981, 256:5981-5983.
10. Haller M.J., Atkinson M.A., Schatz D. Type 1 diabetes mellitus: etiology, presentation, and management. Pediatr. Clin. North Am. 2005, 52:1553-1578.
11. Hernández-Zavala A., Matoušek T., Drobná Z., Adair B.M., Dědina J., Thomas D.J., Stýblo M. Speciation of arsenic in biological matrices by automated hydride generation-cryotrapping-atomic absorption spectrometry with multiple microflame quartz tube atomizer (multiatomizer). J. Anal. At. Spectrom. 2008, 23:342-351.
12. Hughes M.F., Edward B.C., Herbin-Davis K.M., Saunders R.J., Styblo M., Thomas D.J. Arsenic (+3 oxidation state) methyltransferase genotype affects steady-state distribution and clearance of arsenic in arsenate-treated mice. Toxicol. Appl. Pharmacol. 2010, 249:217-223.
13. Liang Y., Matschinsky F.M. Mechanisms of action of nonglucose insulin secretagogues. Annu. Rev. Nutr. 1994, 14:59-81.
14. Liu Z., Sanchez M.A., Jiang X., Boles E., Landfear S.M., Rosen B.P. Mammalian glucose permease GLUT1 facilitates transport of arsenic trioxide and methylarsonous acid. Biochem. Biophys. Res. Commun. 2006, 351:424-430.
15. Longnecker M.P., Daniels J.L. Environmental contaminants as etiologic factors for diabetes. Environ. Health Perspect. 2001, 109:871-876.
16. Matoušek T., Hernández-Zavala A., Svoboda M., Langerová L., Adair B.M., Drobná Z., Thomas D.J., Stýblo M., Dědina J. Oxidation state specific generation of arsines from methylated arsenicals based on l-cysteine treatment in buffered media for speciation analysis by hydride generation-automated cryotrapping-gas chromatography-atomic absorption spectrometry with the multiatomizer. Spetrochim. Acta Part B 2008, 63:396-406.
17. Maull E.A., Ahsan H., Edwards J., Longnecker M.P., Navas-Acien A., Pi J., Silbergeld E.K., Styblo M., Tseng C.H., Thayer K.A., Loomis D. Evaluation of the Association between Arsenic and Diabetes: A National Toxicology Program Workshop Review. Environ. Health Perspect. 2012, 120:1658-1670.
18. Navas-Acien A., Silbergeld E.K., Streeter R.A., Clark J.M., Burke T.A., Guallar E. Arsenic exposure and type 2 diabetes: a systematic review of the experimental and epidemiological evidence. Environ. Health Perspect. 2006, 114:641-648.
19. Paul D.S., Harmon A.W., Devesa V., Thomas D.J., Styblo M. Molecular mechanisms of diabetogenic effects of arsenic: inhibition of insulin signaling by arsenite and methylarsonous acid. Environ. Health Perspect. 2007, 115:734-742.
20. Paul D.S., Hernández-Zavala A., Walton F.S., Adair B.M., Dědina J., Matoušek T., Styblo M. Examination of the effects of arsenic on glucose homeostasis in cell culture and animal studies: development of a mouse model for arsenic-induced diabetes. Toxicol. Appl. Pharmacol. 2007, 222:305-314.
21. Paul D.S., Devesa V., Hernández-Zavala A., Adair B.M., Walton F.S., Drobná Z., Thomas D.J., Styblo M. Environmental arsenic as a disruptor of insulin signaling. Metal Ions in Biology and Medicine 2008, vol. 10:1-7. John Libbey, Eurotext, Paris. P. Collery, I. Maymard, T. Theophanides, L. Khasanova, T. Collery (Eds.).
22. Paul D.S., Walton F.S., Saunders R.J., Styblo M. Characterization of the impaired glucose homeostasis produced in C57BL/6 mice by chronic exposure to arsenic and high-fat diet. Environ. Health Perspect. 2011, 119:1104-1109.
23. Prentki M., Nolan C.J. Islet beta cell failure in type 2 diabetes. J. Clin. Invest. 2006, 116:1802-1812.
24. Pysher M.D., Sollome J.J., Regan S., Cardinal T.R., Hoying J.B., Brooks H.L., Vaillancourt R.R. Increased hexokinase II expression in the renal glomerulus of mice in response to arsenic. Toxicol. Appl. Pharmacol. 2007, 224:39-48.
25. Rorsman P., Eliasson L., Renstrom E., Gromada J., Barg S., Gopel S. The cell physiology of biphasic insulin secretion. News Physiol. Sci. 2000, 15:72-77.
26. Styblo M., Del Razo L.M., Vega L., Germolec D.R., LeCluyse E.L., Hamilton G.A., Reed W., Wang C., Cullen W.R., Thomas D.J. Comparative toxicity of trivalent and pentavalent inorganic and methylated arsenicals in human cells. Arch. Toxicol. 2000, 74:289-299.
27. Stýblo M., Drobná Z., Jaspers I., Lin S., Thomas D.J. The role of biomethylation in toxicity and carcinogenicity of arsenic: a research update. Environ. Health Perspect. 2002, 110(Suppl. 5):767-771.
28. Szot G.L., Koudria P., Bluestone J.A. Murine pancreatic isolation. J. Viz. Exp. 2007, (7):255.
29. The World Bank Arsenic contamination of groundwater in Asia. A World Bank and Water and Sanitation Program Report 2005, (March 2005. http://siteresources.worldbank.org/INTSAREGTOPWATRES/Resources/ARSENIC_BRIEF.pdf).
30. Thomas D.J., Styblo M., Lin S. The cellular metabolism and systemic toxicity of arsenic. Toxicol. Appl. Pharmacol. 2001, 176:127-144.
31. Tseng C.H. The potential biological mechanisms of arsenic-induced diabetes mellitus. Toxicol. Appl. Pharmacol. 2004, 197:67-83.
32. Turner M.D. Coordinated control of both insulin secretion and insulin action through calpain-10-mediated regulation of exocytosis?. Mol. Genet. Metab. 2007, 91:305-307.
33. Walton F.S., Harmon A.W., Paul D.S., Drobna Z., Patel Y.M., Styblo M. Inhibition of insulin-dependent glucose uptake by trivalent arsenicals: possible mechanism of arsenic-induced diabetes. Toxicol. Appl. Pharmacol. 2004, 198:424-433.