Rapid intracellular acidification and cell death by H2O2 and alloxan in pancreatic β cells

Free Radical Biology and Medicine

Volumn 40, Issue 11, 2006, Pages 2047-2055

  Nakamura, Udai ^a   Iwase, Masanori ^a   Uchizono, Yuji ^a   Sonoki, Kazuo ^a   Sasaki, Nobuhiro ^a   Imoto, Hirofumi ^a   Goto, Daisuke ^a   Iida, Mitsuo ^a  

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

Apoptosis; Diabetes mellitus; Na+ H+ exchanger; Nigericin; Oxidative stress

Indexed keywords

ALLOXAN; AMMONIUM CHLORIDE; ANTIOXIDANT; CASPASE 3; DYE; HYDROGEN PEROXIDE; LIPOCORTIN 5; NIGERICIN; PROPIDIUM IODIDE; PROTEIN BAX; SODIUM PROTON EXCHANGE PROTEIN;

ACIDIFICATION; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DAMAGE; CELL DEATH; CELL PH; CLAMP; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVITY; FLOW CYTOMETRY; INTRACELLULAR SPACE; MOUSE; NECROSIS; NONHUMAN; PANCREAS ISLET BETA CELL; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; STAINING;

ANIMALS; BCL-2-ASSOCIATED X PROTEIN; CASPASE 3; CASPASES; CELL DEATH; CELL LINE; FLOW CYTOMETRY; HYDROGEN PEROXIDE; HYDROGEN-ION CONCENTRATION; ISLETS OF LANGERHANS; MICE; MICE, INBRED NOD;

EID: 33646585770     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2006.01.038     Document Type: Article

References (46)

1. Kloppel G., Drenck C.R., Oberholzer M., and Heitz P.U. Morphometric evidence for a striking B-cell reduction at the clinical onset of type 1 diabetes. Virchows Arch. 403 (1984) 441-452
2. Sakuraba H., Mizukami H., Yagihashi N., Wada R., Hanyu C., and Yagihashi S. Reduced beta-cell mass and expression of oxidative stress-related DNA damage in the islet of Japanese Type II diabetic patients. Diabetologia 45 (2002) 85-96
3. Butler A.E., Janson J., Bonner-Weir S., Ritzel R., Rizza R.A., and Butler P.C. Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 52 (2003) 102-110
4. Robertson R.P. Consequences on beta-cell function and reserve after long-term pancreas transplantation. Diabetes 53 (2004) 633-644
5. Mandrup-Poulsen T., Helqvist S., Wogensen L.D., Molvig J., Pociot F., Johannesen J., and Nerup J. Cytokine and free radicals as effector molecules in the destruction of pancreatic beta cells. Curr. Top. Microbiol. Immunol. 164 (1990) 169-193
6. Lortz S., and Tiedge M. Sequential inactivation of reactive oxygen species by combined overexpression of SOD isoforms and catalase in insulin-producing cells. Free Radic. Biol. Med. 34 (2003) 683-688
7. Olcott A.P., Tocco G., Tian J., Zekzer D., Fukuto J., Ignarro L., and Kaufman D.L. A salen-manganese catalytic free radical scavenger inhibits type 1 diabetes and islet allograft rejection. Diabetes 53 (2004) 2574-2580
8. Fridlyand L.E., and Philipson L.H. Does the glucose-dependent insulin secretion mechanism itself cause oxidative stress in pancreatic beta-cells?. Diabetes 53 (2004) 1942-1948
9. Boron W.F. Regulation of intracellular pH. Adv. Physiol. Educ. 28 (2004) 160-179
10. McLean L.A., Roscoe J., Jorgensen N.K., Gorin F.A., and Cala P.M. Malignant gliomas display altered pH regulation by NHE1 compared with nontransformed astrocytes. Am. J. Physiol. Cell Physiol. 278 (2000) C676-C688
11. Fabiato A., and Fabiato F. Effects of pH on the myofilaments and the sarcoplasmic reticulum of skinned cells from cardiac and skeletal muscles. J. Physiol. (London) 276 (1978) 233-255
12. Trudeau L.E., Parpura V., and Haydon P.G. Activation of neurotransmitter release in hippocampal nerve terminals during recovery from intracellular acidification. J. Neurophysiol. 81 (1999) 2627-2635
13. Gottlieb R.A., Nordberg J., Skowronski E., and Babior B.M. Apoptosis induced in Jurkat cells by several agents is preceded by intracellular acidification. Proc. Natl. Acad. Sci. USA 93 (1996) 654-658
14. Wolf C.M., Reynolds J.E., Morana S.J., and Eastman A. The temporal relationship between protein phosphatase, ICE/CED-3 proteases, intracellular acidification, and DNA fragmentation in apoptosis. Exp. Cell Res. 230 (1997) 22-27
15. Furlong I.J., Ascaso R., Lopez Rivas A., and Collins M.K. Intracellular acidification induces apoptosis by stimulating ICE-like protease activity. J. Cell Sci. 110 (1997) 653-661
16. 2 in renal epithelial cells. Arch. Biochem. Biophys. 302 (1993) 245-254
17. Wu M.L., Tsai K.L., Wang S.M., Wu J.C., Wang B.S., and Lee Y.T. Mechanism of hydrogen peroxide and hydroxyl free radical-induced intracellular acidification in cultured rat cardiac myoblasts. Circ. Res. 78 (1996) 564-572
18. Tsai K.L., Wang S.M., Chen C.C., Fong T.H., and Wu M.L. Mechanism of oxidative stress-induced intracellular acidosis in rat cerebellar astrocytes and C6 glioma cells. J. Physiol. (London) 502 (1997) 161-174
19. + exchange. Circ. Res. 83 (1998) 644-651
20. Affar e.B., Shah R.G., Dallaire A.K., Castonguay V., and Shah G.M. Role of poly(ADP-ribose) polymerase in rapid intracellular acidification induced by alkylating DNA damage. Proc. Natl. Acad. Sci. USA 99 (2002) 245-250
21. Mulkey D.K., Henderson III R.A., Ritucci N.A., Putnam R.W., and Dean J.B. Oxidative stress decreases pHi and Na(+)/H(+) exchange and increases excitability of solitary complex neurons from rat brain slices. Am. J. Physiol. Cell Physiol. 286 (2004) C940-C951
22. Gunawardana S.C., and Sharp G.W. Intracellular pH plays a critical role in glucose-induced time-dependent potentiation of insulin release in rat islets. Diabetes 51 (2002) 105-113
23. Hamaguchi K., Gaskins H.R., and Leiter E.H. NIT-1, a pancreatic beta-cell line established from a transgenic NOD/Lt mouse. Diabetes 40 (1991) 842-849
24. Pressman B.C. Biological applications of ionophores. Annu. Rev. Biochem. 45 (1976) 501-530
25. Thomas J.A., Buchsbaum R.N., Zimniak A., and Racker E. Intracellular pH measurements in Ehrlich ascites tumor cells utilizing spectroscopic probes generated in situ. Biochemistry 18 (1979) 2210-2218
26. Roos A., and Boron W.F. Intracellular pH. Physiol. Rev. 61 (1981) 296-434
27. Vermes I., Haanen C., Steffens-Nakken H., and Reutelingsperger C. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V. J. Immunol. Methods 184 (1995) 39-51
28. Anderson R. A peroxidase-independent method for the quantitation of extracellular hydrogen peroxide generated by activated phagocytes in vitro. J. Immunol. Methods 155 (1992) 49-55
29. Cohen G., and Heikkila R.E. The generation of hydrogen peroxide, superoxide radical, and hydroxyl radical by 6-hydroxydopamine, dialuric acid, and related cytotoxic agents. J. Biol. Chem. 249 (1974) 2447-2452
30. Malaisse W.J. Alloxan toxicity to the pancreatic B-cell. A new hypothesis. Biochem. Pharmacol. 31 (1982) 3527-3534
31. Grapengiesser E., Gylfe E., and Hellman B. Regulation of pH in individual pancreatic beta-cells as evaluated by fluorescence ratio microscopy. Biochim. Biophys. Acta 1014 (1989) 219-224
32. 2+, and pH-regulating exchangers in glucose-induced rise of cytoplasmic pH in normal mouse pancreatic islets. J. Biol. Chem. 270 (1995) 7915-7921
33. Hyslop P.A., Hinshaw D.B., Halsey Jr. W.A., Schraufstatter I.U., Sauerheber R.D., Spragg R.G., Jackson J.H., and Cochrane C.G. Mechanisms of oxidant-mediated cell injury. The glycolytic and mitochondrial pathways of ADP phosphorylation are major intracellular targets inactivated by hydrogen peroxide. J. Biol. Chem. 263 (1988) 1665-1675
34. Krippeit-Drews P., Kramer C., Welker S., Lang F., Ammon H.P., and Drews G. Interference of H2O2 with stimulus-secretion coupling in mouse pancreatic beta-cells. J. Physiol. (Lond.) 514 (1999) 471-481
35. Maechler P., Jornot L., and Wollheim C.B. Hydrogen peroxide alters mitochondrial activation and insulin secretion in pancreatic beta cells. J. Biol. Chem. 274 (1999) 27905-27913
36. + antiporter. Analysis of phosphorylation and subcellular localization. J. Biol. Chem. 269 (1994) 8741-8748
37. Boquist L. A new hypothesis for alloxan diabetes. Acta Pathol. Microbiol. Scand. 88 (1980) 201-209
38. Elsner M., Tiedge M., Guldbakke B., Munday R., and Lenzen S. Importance of the GLUT2 glucose transporter for pancreatic beta cell toxicity of alloxan. Diabetologia 45 (2002) 1542-1549
39. Harned R.L., Hidy P.H., Corum C.J., and Jones K.L. Nigericin, a new crystalline antibiotic from an unidentified Streptomyces. Antibiot. Chemother. 1 (1951) 594-596
40. Tartakoff A.M., and Vassalli P. Plasma cell immunoglobulin secretion: arrest is accompanied by alterations of the Golgi complex. J. Exp. Med. 146 (1977) 1332-1345
41. Ohkuma S., and 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 75 (1978) 3327-3331
42. Watanabe N., Kawaguchi M., and Kobayashi Y. Activation of interleukin-1beta-converting enzyme by nigericin is independent of apoptosis. Cytokine 10 (1998) 645-653
43. Varnes M.E., Glazier K.G., and Gray C. pH-dependent effects of the ionophore nigericin on response of mammalian cells to radiation and heat treatment. Radiat. Res. 117 (1989) 282-292
44. Ray B., and Wu H.C. Enhancement of cytotoxicities of ricin and Pseudomonas toxin in Chinese hamster ovary cells by nigericin. Mol. Cell. Biol. 1 (1981) 552-559
45. Chu C.Y., Kao Y.S., and Fong J.C. Nigericin inhibits insulin-stimulated glucose transport in 3T3-L1 adipocytes. J. Cell. Biochem. 85 (2002) 83-91
46. Sakurai K., Katoh M., Someno K., and Fujimoto Y. Apoptosis and mitochondrial damage in INS-1 cells treated with alloxan. Biol. Pharm. Bull. 24 (2001) 876-882