Cd2+-induced cytochrome c release in apoptotic proximal tubule cells: Role of mitochondrial permeability transition pore and Ca2+ uniporter

American Journal of Physiology - Renal Physiology

Volumn 288, Issue 1 57-1, 2005, Pages

  Lee, Wing Kee ^a,b   Bork, Ulrich ^a   Gholamrezaei, Fatemeh ^a   Thévenod, Frank ^a  

^a UNIVERSITY OF WITTEN HERDECKE   (Germany)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Apoptosis inducing factor; Aquaporin; Cadmium; Cyclosporin A

Indexed keywords

APOPTOSIS INDUCING FACTOR; AQUAPORIN; AQUAPORIN 8; BONGKREKIC ACID; CADMIUM; CALCIUM ION; CYCLOSPORIN A; CYTOCHROME C; HOE 33342; LANTHANUM; RUTHENIUM RED; SILVER NITRATE;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME RELEASE; FLUORESCENCE; INTRACELLULAR SPACE; KIDNEY CELL; KIDNEY CORTEX; KIDNEY PROXIMAL TUBULE; MALE; MEMBRANE PERMEABILITY; MITOCHONDRIAL MEMBRANE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; RAT; TIME;

EID: 11144283124     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00224.2004     Document Type: Article

References (60)

1. Almofti MR, Ichikawa T, Yamashita K, Terada H, and Shinohara Y. Silver ion induces a cyclosporine a-insensitive permeability transition in rat liver mitochondria and release of apoptogenic cytochrome c. J Biochem (Tokyo) 134: 43-49, 2003.
2. Al-Nasser IA. Cadmium hepatotoxicity and alterations of the mitochondrial function. J Toxicol Clin Toxicol 38: 407-413, 2000.
3. Beavis AD, Brannan RD, and Garlid KD. Swelling and contraction of the mitochondrial matrix. I. A structural interpretation of the relationship between light scattering and matrix volume. J Biol Chem 260: 13424-13433, 1985.
4. Bernardi P. Mitochondrial transport of cations: channels, exchangers, and permeability transition. Physiol Rev 79: 1127-1155, 1999.
5. Bernardi P and Azzone GF. Cytochrome c as an electron shuttle between the outer and inner mitochondrial membranes. J Biol Chem 256: 7187-7192, 1981.
6. Bernardi P, Petronilli V, Di Lisa F, and Forte M. A mitochondrial perspective on cell death. Trends Biochem Sci 26: 112-117, 2001.
7. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254, 1976.
8. Cortese JD, Voglino AL, and Hackenbrock CR. Multiple conformations of physiological membrane-bound cytochrome c. Biochemistry 37: 6402-6409, 1998.
9. 2+-dependent pore in heart mitochondria activated by inorganic phosphate and oxidative stress. Biochem J 255: 357-360, 1988.
10. De Ceaurriz J, Payan JP, Morel G, and Brondeau MT. Role of extracellular glutathione and γ-glutamyltranspeptidase in the disposition and kidney toxicity of inorganic mercury in rats. J Appl Toxicol 14: 201-206, 1994.
11. Denizot F and Lang R. Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J Immunol Methods 89: 271-277, 1986.
12. Desagher S and Martinou JC. Mitochondria as the central control point of apoptosis. Trends Cell Biol 10: 369-377, 2000.
13. Dorta DJ, Leite S, DeMarco KC, Prado IM, Rodrigues T, Mingatto FE, Uyemura SA, Santos AC, and Curti C. A proposed sequence of events for cadmium-induced mitochondrial impairment. J Inorg Biochem 97: 251-257, 2003.
14. Du C, Fang M, Li Y, Li L, and Wang X. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 102: 33-42, 2000.
15. Elkjær ML, Nejsum LN, Gresz V, Kwon TH, Jensen UB, Frøkiær J, and Nielsen S. Immunolocalization of aquaporin-8 in rat kidney, gastrointestinal tract, testis, and airways. Am J Physiol Renal Physiol 281: F1047-F1057, 2001.
16. 2+ or CdMT in proximal tubule cells: different uptake routes and permissive role of endo/lysosomal CdMT uptake. Am J Physiol Cell Physiol 285: C1367-C1376, 2003.
17. Ferri D, Mazzone A, Liquori GE, Cassano G, Svelto M, and Calamita G. Ontogeny, distribution, and possible functional implications of an unusual aquaporin, AQP8, in mouse liver. Hepatology 38: 947-957, 2003.
18. Friberg L, Elinder CG, Kjellstrom T, and Nordberg GF. Cadmium and Health: A Toxicological and Epidemiological Approach. Boca Raton, FL: CRC, 1986.
19. Gee KR, Zhou ZL, Ton-That D, Sensi SL, and Weiss JH. Measuring zinc in living cells. A new generation of sensitive and selective fluorescent probes. Cell Calcium 31: 245-251, 2002.
20. 2+-independent mechanisms that are regulated by Bax. J Biol Chem 276: 19066-19071, 2001.
21. Greenawalt JW. The isolation of outer and inner mitochondrial membranes. Methods Enzymol 31: 310-323, 1974.
22. 2+-induced large-amplitude swelling of liver and heart mitochondria by cyclosporin is probably caused by the inhibitor binding to mitochondrial-matrix peptidyl-prolyl cis-trans isomerase and preventing it interacting with the adenine nucleotide translocase. Biochem J 268: 153-160, 1990.
23. Halestrap AP, McStay GP, and Clarke SJ. The permeability transition pore complex: another view. Biochimie 84: 153-166, 2002.
24. Haller T, Ortner M, and Gnaiger E. A respirometer for investigating oxidative cell metabolism: toward optimization of respiratory studies. Anal Biochem 218: 338-342, 1994.
25. Hayes RB. The carcinogenicity of metals in humans. Cancer Causes Control 8: 371-385, 1997.
26. Kaufmann SH and Hengartner MO. Programmed cell death: alive and well in the new millennium. Trends Cell Biol 11: 526-534, 2001.
27. Kim MS, Kim BJ, Woo HN, Kim KW, Kim KB, Kim IK, and Jung YK. Cadmium induces caspase-mediated cell death: suppression by Bcl-2. Toxicology 145: 27-37, 2000.
28. Kim SC, Cho MK, and Kim SG. Cadmium-induced non-apoptotic cell death mediated by oxidative stress under the condition of sulfhydryl deficiency. Toxicol Lett 144: 325-336, 2003.
29. Kirichok Y, Krapivinsky G, and Clapham DE. The mitochondrial calcium uniporter is a highly selective ion channel. Nature 427: 360-364, 2004.
30. Klaassen CD. Casarett and Doull's Toxicology. New York: McGraw-Hill, 1999.
31. Klaassen CD, Liu J, and Choudhuri S. Metallothionein: an intracellular protein to protect against cadmium toxicity. Annu Rev Pharmacol Toxicol 39: 267-294, 1999.
32. Kokoszka JE, Waymire KG, Levy SE, Sligh JE, Cai J, Jones DP, MacGregor GR, and Wallace DC. The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore. Nature 427: 461-465, 2004.
33. Kroemer G. Mitochondrial control of apoptosis: an introduction. Biochem Biophys Res Commun 304: 433-435, 2003.
34. Lee WK, Bork U, and Thévenod F. Mitochondria as a target of cadmium nephrotoxicity: induction of swelling and cytochrome c release. Toxicol Mech Methods 14: 67-71, 2004.
35. 2+-calpain and caspase-mitochondria-dependent pathways. J Biol Chem 275: 39702-39709, 2000.
36. Li M, Xia T, Jiang CS, Li LJ, Fu JL, and Zhou ZC. Cadmium directly induced the opening of membrane permeability pore of mitochondria which possibly involved in cadmium-triggered apoptosis. Toxicology 194: 19-33, 2003.
37. 2-induced nephrotoxicity indicates that renal injury is not mediated by the CdMT complex. Toxicol Sci 46: 197-203, 1998.
38. Liu X, Kim CN, Yang J, Jemmerson R, and Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86: 147-157, 1996.
39. Martinou JC and Green DR. Breaking the mitochondrial barrier. Nat Rev Mol Cell Biol 2: 63-67, 2001.
40. Mosmann T. Rapid colorimetric assay for cellular growth and survival-application to proliferation and cytotoxicity assays. J Immunol Methods 65: 55-63, 1983.
41. Niemietz CM and Tyerman SD. New potent inhibitors of aquaporins: silver and gold compounds inhibit aquaporins of plant and human origin. FEBS Lett 531: 443-447, 2002.
42. O'Brien P and Salacinski HJ. Evidence that the reactions of cadmium in the presence of metallothionein can produce hydroxyl radicals. Arch Toxicol 72: 690-700, 1998.
43. Ott M, Robertson JD, Gogvadze V, Zhivotovsky B, and Orrenius S. Cytochrome c release from mitochondria proceeds by a two-step process. Proc Natl Acad Sci USA 99: 1259-1263, 2002.
44. Preston GM, Jung JS, Guggino WB, and Agre P. The mercury-sensitive residue at cysteine 189 in the CHIP28 water channel. J Biol Chem 268: 17-20, 1993.
45. Robertson JD, Gogvadze V, Zhivotovsky B, and Orrenius S. Distinct pathways for stimulation of cytochrome c release by etoposide. J Biol Chem 275: 32438-32443, 2000.
46. Shimizu S, Ide T, Yanagida T, and Tsujimoto Y. Electrophysiological study of a novel large pore formed by Bax and the voltage-dependent anion channel that is permeable to cytochrome c. J Biol Chem 275: 12321-12325, 2000.
47. Shimizu S, Narita M, and Tsujimoto Y. Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 399: 483-487, 1999.
48. Susin SA, Lorenzo HIC, Zamzami N, Marzo I, Snow BE, Brothers GM, Mangion J, Jacotot E, Costantini P, Loeffler M, Larochette N, Goodlett DR, Aebersold R, Siderovski DP, Penninger JM, and Kroemer G. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397: 441-446, 1999.
49. Takebayashi S, Jimi S, Segawa M, and Kiyoshi Y. Cadmium induces osteomalacia mediated by proximal tubular atrophy and disturbances of phosphate reabsorption. A study of 11 autopsies. Pathol Res Pract 196: 653-663, 2000.
50. Thévenod F. Nephrotoxicity and the proximal tubule. Insights from cadmium. Nephron Physiol 93: 87-93, 2003.
51. +-ATPase through proteasomal and endo-/lysosomal proteolytic pathways. FASEB J 13: 1751-1761, 1999.
52. Thévenod F, Friedmann JM, Katsen AD, and Hauser IA. Up-regulation of multidrug resistance P-glycoprotein via nuclear factor-κB activation protects kidney proximal tubule cells from cadmium- and reactive oxygen species-induced apoptosis. J Biol Chem 275: 1887-1896, 2000.
53. Verhagen AM, Ekert PG, Pakusch M, Silke J, Connolly LM, Reid GE, Moritz RL, Simpson RJ, and Vaux DL. Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell 102: 43-53, 2000.
54. Verroust PJ and Kozyraki R. The roles of cubilin and megalin, two multiligand receptors, in proximal tubule function: possible implication in the progression of renal disease. Curr Opin Nephrol Hypertens 10: 33-38, 2001.
55. Von Ahsen O, Renken C, Perkins G, Kluck RM, Bossy-Wetzel E, and Newmeyer DD. Preservation of mitochondrial structure and function after Bid- or Bax-mediated cytochrome c release. J Cell Biol 150: 1027-1036, 2000.
56. Wedeen RP and De Broe ME. Heavy metals and the kidney. Oxford Textbook of Clinical Nephrology, edited by Davison AM. Oxford, UK: Oxford University Press, 1998, chapt. 65, p. 1175-1189.
57. Woost PG, Orosz DE, Jin W, Frisa PS, Jacobberger JW, Douglas JG, and Hopfer U. Immortalization and characterization of proximal tubule cells derived from kidneys of spontaneously hypertensive and normotensive rats. Kidney Int 50: 125-134, 1996.
58. Zalups RK and Koropatnick J. Molecular Biology and Toxicology of Metals. London: Taylor and Francis, 2000.
59. Zazueta C, Sosa-Torres ME, Correa F, and Garza-Ortiz A. Inhibitory properties of ruthenium amine complexes on mitochondrial calcium uptake. J Bioenerg Biomembr 31: 551-557, 1999.
60. Zimmermann KC, Bonzon C, and Green DR. The machinery of programmed cell death. Pharmacol Ther 92: 57-70, 2001.