Liver mitochondrial membrane crosslinking and destruction in a rat model of Wilson disease

Journal of Clinical Investigation

Volumn 121, Issue 4, 2011, Pages 1508-1518

  Zischka, Hans ^a   Lichtmannegger, Josef ^a   Schmitt, Sabine ^a   Jägemann, Nora ^a   Schulz, Sabine ^a   Wartini, Daniela ^a   Jennen, Luise ^a   Rust, Christian ^b   Larochette, Nathanael ^c   Galluzzi, Lorenzo ^c,d,e   Chajes, Veronique ^d,f   Bandow, Nathan ^g   Gilles, Valérie S ^g   DiSpirito, Alan A ^g   Esposito, Irene ^a,h   Goettlicher, Martin ^a,h   Summer, Karl H ^a   Kroemer, Guido ^c,d,i,j,k  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c Institut Gustave Roussy   (France)

^d INSTITUT GUSTAVE ROUSSY   (France)

^e UNIVERSITÉ PARIS SACLAY   (France)

^f INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

^g IOWA STATE UNIVERSITY   (United States)

^h TECHNICAL UNIVERSITY OF MUNICH   (Germany)

ⁱ CENTRE DE RECHERCHE DES CORDELIERS   (France)

^j HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^k UNIVERSITÉ PARIS DESCARTES   (France)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ATP7B ENZYME; COPPER; THIOL; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CROSS LINKING; GENE; LIVER FAILURE; MITOCHONDRIAL MEMBRANE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; WILSON DISEASE;

ADENOSINE TRIPHOSPHATASES; ANIMALS; CATION TRANSPORT PROTEINS; CELL-FREE SYSTEM; CHELATING AGENTS; COPPER; CROSS-LINKING REAGENTS; DISEASE MODELS, ANIMAL; GENE KNOCKOUT TECHNIQUES; HEPATOLENTICULAR DEGENERATION; HUMANS; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA, LIVER; MITOCHONDRIAL PROTEINS; RATS; SULFHYDRYL COMPOUNDS;

EID: 79953302399     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI45401     Document Type: Article

References (56)

1. Sternlieb I. Wilson's disease. Clin Liver Dis. 2000;4(1):229-239. (Pubitemid 33041495)
2. Bull PC, Thomas GR, Rommens JM, Forbes JR, Cox DW. The Wilson disease gene is a putative copper transporting P-type ATPase similar to the Menkes gene. Nat Genet. 1993;5(4):327-337.
3. Tanzi RE, et al. The Wilson disease gene is a copper transporting ATPase with homology to the Menkes disease gene. Nat Genet. 1993;5(4):344-350. (Pubitemid 23351304)
4. Gitlin JD. Wilson disease. Gastroenterology. 2003;125(6):1868-1877. (Pubitemid 37500450)
5. Walshe JM. Penicillamine, a new oral therapy for Wilson's disease. Am J Med. 1956;21(4):487-495.
6. Walshe JM. Wilson's disease; new oral therapy. Lancet. 1956;270(6906):25-26.
7. Wilson SAK. Progressive lenticular degeneration: a familial nervous disease associated with cirrhosis of the liver. Lancet. 1912;179(4626):1115- 1119.
8. Cumings JN. The copper and iron content of brain and liver in the normal and in hepato-lenticular degeneration. Brain. 1948;71(pt. 4):410-415.
9. Sokol RJ, Devereaux MW, O'Brien K, Khandwala RA, Loehr JP. Abnormal hepatic mitochondrial respiration and cytochrome C oxidase activity in rats with long-term copper overload. Gastroenterology. 1993;105(1):178-187. (Pubitemid 23234034)
10. Gu M, et al. Oxidative-phosphorylation defects in liver of patients with Wilson's disease. Lancet. 2000;356(9228):469-474. (Pubitemid 30496819)
11. Britton RS. Metal-induced hepatotoxicity. Semin Liver Dis. 1996;16(1):3-12. (Pubitemid 26130097)
12. Luza SC, Speisky HC. Liver copper storage and transport during development: implications for cytotoxicity. Am J Clin Nutr. 1996;63(5):812S- 820S.
13. Rossi L, Lombardo MF, Ciriolo MR, Rotilio G. Mitochondrial dysfunction in neurodegenerative diseases associated with copper imbalance. Neurochem Res. 2004;29(3):493-504. (Pubitemid 38295000)
14. Mansouri A, et al. Premature oxidative aging of hepatic mitochondrial DNA in Wilson's disease. Gastroenterology. 1997;113(2):599-605. (Pubitemid 27351789)
15. Sokol RJ, et al. Oxidant injury to hepatic mitochondria in patients with Wilson's disease and Bedlington terriers with copper toxicosis. Gastroenterology. 1994;107(6):1788-1798. (Pubitemid 24357635)
16. Rae TD, Schmidt PJ, Pufahl RA, Culotta VC, O'Halloran TV. Undetectable intracellular free copper: the requirement of a copper chaperone for superoxide dismutase. Science. 1999;284(5415):805-808. (Pubitemid 29291346)
17. Lippard SJ. Free copper ions in the cell? Science. 1999;284(5415):748- 749.
18. Cobine PA, Ojeda LD, Rigby KM, Winge DR. Yeast contain a non-proteinaceous pool of copper in the mitochondrial matrix. J Biol Chem. 2004;279(14):14447-14455. (Pubitemid 38468987)
19. Cobine PA, Pierrel F, Bestwick ML, Winge DR. Mitochondrial matrix copper complex used in metallation of cytochrome oxidase and superoxide dismutase. J Biol Chem. 2006;281(48):36552-36559. (Pubitemid 46042122)
20. Galluzzi L, Blomgren K, Kroemer G. Mitochondrial membrane permeabilization in neuronal injury. Nat Rev Neurosci. 2009;10(7):481-494.
21. Kroemer G, Galluzzi L, Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol Rev. 2007;87(1):99-163. (Pubitemid 46209992)
22. Green DR, Kroemer G. The pathophysiology of mitochondrial cell death. Science. 2004;305(5684):626-629. (Pubitemid 39006738)
23. Sternlieb I. Mitochondrial and fatty changes in hepatocytes of patients with Wilson's disease. Gastroenterology. 1968;55(3):354-367.
24. Sternlieb I. Fraternal concordance of types of abnormal hepatocellular mitochondria in Wilson's disease. Hepatology. 1992;16(3):728-732.
25. Sternlieb I. Electron microscopy of mitochondria and peroxisomes of human hepatocytes. Prog Liver Dis. 1979;6:81-104.
26. Wu J, Forbes JR, Chen HS, Cox DW. The LEC rat has a deletion in the copper transporting ATPase gene homologous to the Wilson disease gene. Nat Genet. 1994;7(4):541-545.
27. Fuentealba IC, Aburto EM. Animal models of copper-associated liver disease. Comp Hepatol. 2003;2(1):5.
28. Sternlieb I, Quintana N, Volenberg I, Schilsky ML. An array of mitochondrial alterations in the hepatocytes of Long-Evans Cinnamon rats. Hepatology. 1995;22(6):1782-1787.
29. Sokol RJ, Devereaux M, Mierau GW, Hambidge KM, Shikes RH. Oxidant injury to hepatic mitochondrial lipids in rats with dietary copper overload. Modification by vitamin E deficiency. Gastroenterology. 1990;99(4):1061-1071.
30. Roberts EA, Robinson BH, Yang S. Mitochondrial structure and function in the untreated Jackson toxic milk (tx-j) mouse, a model for Wilson disease. Mol Genet Metab. 2008;93(1):54-65. (Pubitemid 350236005)
31. Orrenius S, Gogvadze V, Zhivotovsky B. Mitochondrial oxidative stress: implications for cell death. Annu Rev Pharmacol Toxicol. 2007;47:143-183.
32. Ott M, Gogvadze V, Orrenius S, Zhivotovsky B. Mitochondria, oxidative stress and cell death. Apoptosis. 2007;12(5):913-922. (Pubitemid 46653300)
33. Ahmed S, Deng J, Borjigin J. A new strain of rat for functional analysis of PINA. Brain Res Mol Brain Res. 2005;137(1-2):63-69. (Pubitemid 40798887)
34. Zischka H, et al. Isolation of highly pure rat liver mitochondria with the aid of zone-electrophoresis in a free flow device (ZE-FFE). Methods Mol Biol. 2008;424:333-348.
35. Nair J, et al. Apoptosis and age-dependant induction of nuclear and mitochondrial etheno-DNA adducts in Long-Evans Cinnamon (LEC) rats: enhanced DNA damage by dietary curcumin upon copper accumulation. Carcinogenesis. 2005;26(7):1307-1315. (Pubitemid 41417910)
36. Cobine PA, Pierrel F, Winge DR. Copper trafficking to the mitochondrion and assembly of copper metalloenzymes. Biochim Biophys Acta. 2006;1763(7):759-772. (Pubitemid 44189537)
37. Behling LA, et al. NMR, mass spectrometry and chemical evidence reveal a different chemical structure for methanobactin that contains oxazolone rings. J Am Chem Soc. 2008;130(38):12604-12605.
38. Kachur AV, Koch CJ, Biaglow JE. Mechanism of copper-catalyzed autoxidation of cysteine. Free Radic Res. 1999;31(1):23-34. (Pubitemid 29425339)
39. Kachur AV, Koch CJ, Biaglow JE. Mechanism of copper-catalyzed oxidation of glutathione. Free Radic Res. 1998;28(3):259-269. (Pubitemid 28325573)
40. Kachur AV, Held KD, Koch CJ, Biaglow JE. Mechanism of production of hydroxyl radicals in the copper-catalyzed oxidation of dithiothreitol. Radiat Res. 1997;147(4):409-415. (Pubitemid 27150370)
41. Hochgrafe F, Mostertz J, Albrecht D, Hecker M. Fluorescence thiol modification assay: oxidatively modified proteins in Bacillus subtilis. Mol Microbiol. 2005;58(2):409-425. (Pubitemid 41476158)
42. Braun RJ, Kinkl N, Zischka H, Ueffing M. 16-BAC/SDS-PAGE analysis of membrane proteins of yeast mitochondria purified by free flow electrophoresis. Methods Mol Biol. 2009;528:83-107.
43. Zischka H, et al. Electrophoretic analysis of the mitochondrial outer membrane rupture induced by permeability transition. Anal Chem. 2008;80(13):5051-5058. (Pubitemid 351956314)
44. Schilsky ML. Diagnosis and treatment of Wilson's disease. Pediatr Transplant. 2002;6(1):15-19. (Pubitemid 34269730)
45. Togashi Y, et al. D-penicillamine prevents the development of hepatitis in Long-Evans Cinnamon rats with abnormal copper metabolism. Hepatology. 1992;15(1):82-87.
46. Valko M, Rhodes CJ, Moncol J, Izakovic M, Mazur M. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact. 2006;160(1):1-40. (Pubitemid 43227479)
47. Hurd TR, et al. Glutathionylation of mitochondrial proteins. Antioxid Redox Signal. 2005;7(7-8):999-1010. (Pubitemid 40967150)
48. Halestrap AP, Brenner C. The adenine nucleotide translocase: a central component of the mitochondrial permeability transition pore and key player in cell death. Curr Med Chem. 2003;10(16):1507-1525. (Pubitemid 36896553)
49. Kim HJ, et al. Methanobactin, a copper-acquisition compound from methane-oxidizing bacteria. Science. 2004;305(5690):1612-1615. (Pubitemid 39296354)
50. Fleischer S. Long-term storage of mitochondria to preserve energy-linked functions. Methods Enzymol. 1979;55:28-32.
51. Kiebish MA, et al. Lipidomic analysis and electron transport chain activities in C57BL/6J mouse brain mitochondria. J Neurochem. 2008;106(1):299-312. (Pubitemid 351840212)
52. Zamzami N, Metivier D, Kroemer G. Quantitation of mitochondrial transmembrane potential in cells and in isolated mitochondria. Methods Enzymol. 2000;322:208-213. (Pubitemid 30482057)
53. Shevchenko A, Wilm M, Vorm O, Mann M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem. 1996;68(5):850-858.
54. Gharahdaghi F, Weinberg CR, Meagher DA, Imai BS, Mische SM. Mass spectrometric identification of proteins from silver-stained polyacrylamide gel: a method for the removal of silver ions to enhance sensitivity. Electrophoresis. 1999;20(3):601-605. (Pubitemid 29183427)
55. Bandow NL, et al. Isolation of methanobactin from the spent media of methane oxidizing bacteria. Meth Enzymol. In press.
56. Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979;76(9):4350-4354. (Pubitemid 9256559)