Clioquinol attenuates zinc-dependent β-cell death and the onset of insulitis and hyperglycemia associated with experimental type I diabetes in mice

European Journal of Pharmacology

Volumn 565, Issue 1-3, 2007, Pages 232-239

  Priel, Tsvia ^a   Aricha Tamir, Barak ^a   Sekler, Israel ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

Clioquinol; Diabetes; MLD STZ; Zinc chelation; Zinc homeostasis

Indexed keywords

CLIOQUINOL; STREPTOZOCIN; ZINC; ZINC ION;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DEATH; CONTROLLED STUDY; DRUG ANTAGONISM; DRUG EFFICACY; DRUG HALF LIFE; EXPERIMENTAL DIABETES MELLITUS; GLUCOSE TOLERANCE TEST; HOMEOSTASIS; HYPERGLYCEMIA; IN VIVO STUDY; INSULIN DEPENDENT DIABETES MELLITUS; INSULINOMA; INSULITIS; LOW DRUG DOSE; MALE; MONOTHERAPY; MOUSE; NONHUMAN; PANCREAS ISLET; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; STATISTICAL SIGNIFICANCE; STREPTOZOCIN DIABETES; TUMOR CELL LINE;

ANIMALS; CATION TRANSPORT PROTEINS; CELL DEATH; CELL LINE, TUMOR; CHELATING AGENTS; CLIOQUINOL; DIABETES MELLITUS, TYPE 1; HYPERGLYCEMIA; INSULIN-SECRETING CELLS; MALE; MICE; MICE, INBRED ICR; SODIUM; STREPTOZOCIN; ZINC;

EID: 34249097722     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2007.02.064     Document Type: Article

References (48)

1. Aizenman E., Stout A.K., Hartnett K.A., Dineley K.E., McLaughlin B., and Reynolds I.J. Induction of neuronal apoptosis by thiol oxidation: putative role of intracellular zinc release. J. Neurochem. 75 (2000) 1878-1888
2. Andrews G.K. Cellular zinc sensors: MTF-1 regulation of gene expression. Biometals 14 (2001) 223-237
3. Atar D., Backx P.H., Appel M.M., Gao W.D., and Marban E. Excitation-transcription coupling mediated by zinc influx through voltage-dependent calcium channels. J. Biol. Chem. 270 (1995) 2473-2477
4. Azriel-Tamir H., Sharir H., Schwartz B., and Hershfinkel M. Extracellular zinc triggers ERK-dependent activation of Na+/H+ exchange in colonocytes mediated by the zinc-sensing receptor. J. Biol. Chem. 279 (2004) 51804-51816
5. Bush A.I. Metal complexing agents as therapies for Alzheimer's disease. Neurobiol. Aging 23 (2002) 1031-1038
6. Chang I., Cho N., Koh J.Y., and Lee M.S. Pyruvate inhibits zinc-mediated pancreatic islet cell death and diabetes. Diabetologia 46 (2003) 1220-1227
7. Cherny R.A., Atwood C.S., Xilinas M.E., Gray D.N., Jones W.D., McLean C.A., Barnham K.J., Volitakis I., Fraser F.W., Kim Y., Huang X., Goldstein L.E., Moir R.D., Lim J.T., Beyreuther K., Zheng H., Tanzi R.E., Masters C.L., and Bush A.I. Treatment with a copper-zinc chelator markedly and rapidly inhibits beta-amyloid accumulation in Alzheimer's disease transgenic mice. Neuron 30 (2001) 665-676
8. Choi D.W., and Koh J.Y. Zinc and brain injury. Annu. Rev. Neurosci. 21 (1998) 347-375
9. Choi D.W., Yokoyama M., and Koh J. Zinc neurotoxicity in cortical cell culture. Neuroscience 24 (1988) 67-79
10. Cote A., Chiasson M., Peralta III M.R., Lafortune K., Pellegrini L., and Toth K. Cell type-specific action of seizure-induced intracellular zinc accumulation in the rat hippocampus. J. Physiol. 566 (2005) 821-837
11. Crivat G., Kikuchi K., Nagano T., Priel T., Hershfinkel M., Sekler I., Rosenzweig N., and Rosenzweig Z. Fluorescence-based zinc ion sensor for zinc ion release from pancreatic cells. Anal. Chem. 78 (2006) 5799-5804
12. Cuajungco M.P., Faget K.Y., Huang X., Tanzi R.E., and Bush A.I. Metal chelation as a potential therapy for Alzheimer's disease. Ann. N.Y. Acad. Sci. 920 (2000) 292-304
13. Dunn M.F. Zinc-ligand interactions modulate assembly and stability of the insulin hexamer - a review. Biometals 18 (2005) 295-303
14. Formby B., Schmid-Formby F., and Grodsky G.M. Relationship between insulin release and 65zinc efflux from rat pancreatic islets maintained in tissue culture. Diabetes 33 (1984) 229-234
15. Frederickson C.J., Suh S.W., Koh J.Y., Cha Y.K., Thompson R.B., LaBuda C.J., Balaji R.V., and Cuajungco M.P. Depletion of intracellular zinc from neurons by use of an extracellular chelator in vivo and in vitro. J. Histochem. Cytochem. 50 (2002) 1659-1662
16. Frederickson C.J., Koh J.Y., and Bush A.I. The neurobiology of zinc in health and disease. Nat. Rev., Neurosci. 6 (2005) 449-462
17. Gee K.R., Zhou Z.L., Qian W.J., and Kennedy R. Detection and imaging of zinc secretion from pancreatic beta-cells using a new fluorescent zinc indicator. J. Am. Chem. Soc. 124 (2002) 776-778
18. Gyulkhandanyan A.V., Lee S.C., Bikopoulos G., Dai F., and Wheeler M.B. The Zn2+ transporting pathways in pancreatic beta-cells: A role for the L-type voltage-gated Ca2+ channel. J. Biol. Chem. 281 (2006) 9361-9372
19. Herold K.C., Bloch T.N., Vezys V., and Sun Q. Diabetes induced with low doses of streptozotocin is mediated by V beta 8.2+ T-cells. Diabetes 44 (1995) 354-359
20. Hershfinkel M., Moran A., Grossman N., and Sekler I. A zinc-sensing receptor triggers the release of intracellular Ca2+ and regulates ion transport. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 11749-11754
21. Huang X.F., and Arvan P. Intracellular transport of proinsulin in pancreatic beta-cells. Structural maturation probed by disulfide accessibility. J. Biol. Chem. 270 (1995) 20417-20423
22. Hyun H.J., Sohn J.H., Ha D.W., Ahn Y.H., Koh J.Y., and Yoon Y.H. Depletion of intracellular zinc and copper with TPEN results in apoptosis of cultured human retinal pigment epithelial cells. Invest. Ophthalmol. Vis. Sci. 42 (2001) 460-465
23. Ishihara H., Maechler P., Gjinovci A., Herrera P.L., and Wollheim C.B. Islet beta-cell secretion determines glucagon release from neighbouring alpha-cells. Nat. Cell Biol. 5 (2003) 330-335
24. Kim B.J., Kim Y.H., Kim S., Kim J.W., Koh J.Y., Oh S.H., Lee M.K., Kim K.W., and Lee M.S. Zinc as a paracrine effector in pancreatic islet cell death. Diabetes 49 (2000) 367-372
25. Koh J.Y., Suh S.W., Gwag B.J., He Y.Y., Hsu C.Y., and Choi D.W. The role of zinc in selective neuronal death after transient global cerebral ischemia. Science 272 (1996) 1013-1016
26. Komatsu K., Kikuchi K., Kojima H., Urano Y., and Nagano T. Selective zinc sensor molecules with various affinities for Zn2+, revealing dynamics and regional distribution of synaptically released Zn2+ in hippocampal slices. J. Am. Chem. Soc. 127 (2005) 10197-10204
27. Liuzzi J.P., Bobo J.A., Lichten L.A., Samuelson D.A., and Cousins R.J. Responsive transporter genes within the murine intestinal-pancreatic axis form a basis of zinc homeostasis. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 14355-14360
28. Maret W. Cellular zinc and redox states converge in the metallothionein/thionein pair. J. Nutr. 133 (2003) 1460S-1462S
29. Nguyen T., Hamby A., and Massa S.M. Clioquinol down-regulates mutant huntingtin expression in vitro and mitigates pathology in a Huntington's disease mouse model. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 11840-11845
30. Nitzan Y.B., Sekler I., Hershfinkel M., Moran A., and Silverman W.F. Postnatal regulation of ZnT-1 expression in the mouse brain. Brain Res. Dev. Brain Res. 137 (2002) 149-157
31. Nitzan Y.B., Sekler I., Frederickson C.J., Coulter D.A., Balaji R.V., Liang S.L., Margulis A., Hershfinkel M., and Silverman W.F. Clioquinol effects on tissue chelatable zinc in mice. J. Mol. Med. 81 (2003) 637-644
32. Nolte C., Gore A., Sekler I., Kresse W., Hershfinkel M., Hoffmann A., Kettenmann H., and Moran A. ZnT-1 expression in astroglial cells protects against zinc toxicity and slows the accumulation of intracellular zinc. Glia 48 (2004) 145-155
33. Ogata M., Watanabe S., Tateishi J., Kuroda S., and Otsuki S. Accumulation of clioquinol in mice. Lancet 1 (1973) 1325
34. Ohana E., Segal D., Palty R., Ton-That D., Moran A., Sensi S.L., Weiss J.H., Hershfinkel M., and Sekler I. A sodium zinc exchange mechanism is mediating extrusion of zinc in Mammalian cells. J. Biol. Chem. 279 (2004) 4278-4284
35. Ohana E., Sekler I., Kaisman T., Kahn N., Cove J., Silverman W.F., Amsterdam A., and Hershfinkel M. Silencing of ZnT-1 expression enhances heavy metal influx and toxicity. J. Mol. Med. 84 (2006) 753-763
36. Ohly P., Dohle C., Abel J., Seissler J., and Gleichmann H. Zinc sulphate induces metallothionein in pancreatic islets of mice and protects against diabetes induced by multiple low doses of streptozotocin. Diabetologia 43 (2000) 1020-1030
37. Park K.S., Ahn Y., Kim J.A., Yun M.S., Seong B.L., and Choi K.Y. Extracellular zinc stimulates ERK-dependent activation of p21(Cip/WAF1) and inhibits proliferation of colorectal cancer cells. Br. J. Pharmacol. 137 (2002) 597-607
38. Priel T., and Hershfinkel M. Zinc influx and physiological consequences in the beta-insulinoma cell line, Min6. Biochem. Biophys. Res. Commun. 346 (2006) 205-212
39. Schott-Ohly P., Lgssiar A., Partke H.J., Hassan M., Friesen N., and Gleichmann H. Prevention of spontaneous and experimentally induced diabetes in mice with zinc sulfate-enriched drinking water is associated with activation and reduction of NF-kappa B and AP-1 in islets, respectively. Exp. Biol. Med. (Maywood) 229 (2004) 1177-1185
40. Segal D., Ohana E., Besser L., Hershfinkel M., Moran A., and Sekler I. A role for ZnT-1 in regulating cellular cation influx. Biochem. Biophys. Res. Commun. 323 (2004) 1145-1150
41. Sekler I., Moran A., Hershfinkel M., Dori A., Margulis A., Birenzweig N., Nitzan Y., and Silverman W.F. Distribution of the zinc transporter ZnT-1 in comparison with chelatable zinc in the mouse brain. J. Comp. Neurol. 447 (2002) 201-209
42. Sensi S.L., Ton-That D., Sullivan P.G., Jonas E.A., Gee K.R., Kaczmarek L.K., and Weiss J.H. Modulation of mitochondrial function by endogenous Zn2+ pools. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 6157-6162
43. Strandell E., Eizirik D.L., Korsgren O., and Sandler S. Functional characteristics of cultured mouse pancreatic islets following exposure to different streptozotocin concentrations. Mol. Cell. Endocrinol. 59 (1988) 83-91
44. Toyokura Y., Takasu T., and Matsuoka O. Experimental studies utilizing radionuclide-labelled clioquinol as tracer in vivo. Jpn. J. Med. Sci. Biol. 28 (1975) 79-86
45. Wang Z., and Gleichmann H. GLUT2 in pancreatic islets: crucial target molecule in diabetes induced with multiple low doses of streptozotocin in mice. Diabetes 47 (1998) 50-56
46. Weiss J.H., Sensi S.L., and Koh J.Y. Zn(2+): a novel ionic mediator of neural injury in brain disease. Trends Pharmacol. Sci. 21 (2000) 395-401
47. White A.R., Du T., Laughton K.M., Volitakis I., Sharples R.A., Xilinas M.E., Hoke D.E., Holsinger R.M., Evin G., Cherny R.A., Hill A.F., Barnham K.J., Li Q.X., Bush A.I., and Masters C.L. Degradation of the Alzheimer disease amyloid beta-peptide by metal-dependent up-regulation of metalloprotease activity. J. Biol. Chem. 281 (2006) 17670-17680
48. Zalewski P.D., Millard S.H., Forbes I.J., Kapaniris O., Slavotinek A., Betts W.H., Ward A.D., Lincoln S.F., and Mahadevan I. Video image analysis of labile zinc in viable pancreatic islet cells using a specific fluorescent probe for zinc. J. Histochem. Cytochem. 42 (1994) 877-884