Cryopreservation of human hepatocytes alters the mitochondrial respiratory chain complex 1

Cell Transplantation

Volumn 16, Issue 4, 2007, Pages 409-419

  Stéphenne, Xavier ^a   Najimi, Mustapha ^a   Dung, Khuu Ngoc ^a   Smets, Françoise ^a   Hue, Louis ^a   Guigas, Bruno ^a   Sokal, Etienne M ^a,b  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b CLINIQUES UNIVERSITAIRES SAINT LUC   (Belgium)

Author keywords

Complex; Cryopreservation; Hepatocyte; Liver cell transplantation; Mitochondria

Indexed keywords

2,4 DINITROPHENOL; ADENOSINE TRIPHOSPHATE; CASPASE 3; CASPASE 9; CYTOCHROME C; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); CASPASE; UNCOUPLING PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL ISOLATION; CELL PERMEABILIZATION; CONTROLLED STUDY; CRYOPRESERVATION; CYTOSOL; ELECTRON MICROSCOPY; ENZYME RELEASE; HUMAN; HUMAN CELL; IMAGE ANALYSIS; LIVER CELL; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; THAWING; ANIMAL; C57BL MOUSE; CELL SURVIVAL; CYTOLOGY; ENZYME ACTIVATION; IN VITRO STUDY; LIVER MITOCHONDRION; METABOLISM; PHYSIOLOGY; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

MUS;

2,4-DINITROPHENOL; ADENOSINE TRIPHOSPHATE; ANIMALS; CASPASES; CELL SURVIVAL; CRYOPRESERVATION; CYTOCHROMES C; ELECTRON TRANSPORT COMPLEX I; ENZYME ACTIVATION; HEPATOCYTES; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA, LIVER; OXYGEN CONSUMPTION; UNCOUPLING AGENTS;

EID: 38349070819     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/000000007783464821     Document Type: Article

References (45)

1. Baccarani, U.; Donini, A.; Sanna, A.; Risaliti, A.; Cariani, A.; Nardo, B.; Cavallari, A.; Martinelli, G.; Ridolfi, L.; Bellini, G.; Scalamogna, M.; Bresadola, F. First report of cryopreserved human hepatocytes based bioartificial liver successfully used as a bridge to liver transplantation. Am. J. Transplant. 4:286-289; 2004.
2. Bernardi, P. Mitochondrial transport of cations: Channels, exchangers, and permeability transition. Physiol. Rev. 79:1127-1155; 1999.
3. Berry, M. N.; Friend, D. S. High-yield preparation of isolated rat liver parenchymal cells: A biochemical and fine structural study. J. Cell Biol. 43:506-520; 1969.
4. Carroll, J.; Fearnley, I. M.; Shannon, R. J.; Hirst, J.; Walker, J. E. Analysis of the subunit composition of complex I from bovine heart mitochondria. Mol. Cell. Proteomics 2:117-126; 2003.
5. Dhawan, A.; Mitry, R. R.; Hughes, R. D.; Lehec, S.; Terry, C.; Bansal, S.; Arya, R.; Wade, J. J.; Verma, A.; Heaton, N. D.; Rela, M.; Mieli-Vergani, G. Hepatocyte transplantation for inherited factor VII deficiency. Transplantation 78:1812-1814; 2004.
6. Fox, I. J.; Chowdhury, J. R.; Kaufman, S. S.; Goertzen, T. C.; Chowdhury, N. R.; Warkentin, P. I.; Dorko, K.; Sauter, B. V.; Strom, S. C. Treatment of the Crigler-Najjar syndrome type I with hepatocyte transplantation. N. Engl. J. Med. 338:1422-1426; 1998.
7. Freitas, I.; Bertone, V.; Guarnaschelli, C.; Ferrigno, A.; Boncompagni, E.; Rizzo, V.; Reiter, R. J.; Barni, S.; Vairetti, M. In situ demonstration of improvement of liver mitochondria function by melatonin after cold ischemia. In Vivo 20:229-237; 2006.
8. Fu, T.; Guo, D.; Huang, X.; O'Gorman, M. R.; Huang, L.; Crawford, S. E.; Soriano, H. E. Apoptosis occurs in isolated and banked primary mouse hepatocytes. Cell Transplant. 10:59-66; 2001.
9. Fujita, R.; Hui, T.; Chelly, M.; Demetriou, A. A. The effect of antioxidants and a caspase inhibitor on cryopreserved rat hepatocytes. Cell Transplant. 14:391-396; 2005.
10. Giraudi, P. J.; Almada, L. L.; Mamprin, M. E.; Guibert, E. E.; Furno, G.; Rodriguez, J. V. The assessment of viability in isolated rat hepatocytes subjected to cold or sub-zero non-freezing preservation protocols using a propidium iodide modified test. Cryo Lett. 26:169-184; 2005.
11. Grattagliano, I.; Vendemiale, G.; Lauterburg, B. H. Reperfusion injury of the liver: Role of mitochondria and protection by glutathione ester. J. Surg. Res. 86:2-8; 1999.
12. Groen, A. K.; Sips, H. J.; Vervoorn, R. C.; Tager, J. M. Intracellular compartmentation and control of alanine metabolism in rat liver parenchymal cells. Eur. J. Biochem. 122:87-93; 1982.
13. Guigas, B.; Detaille, D.; Chauvin, C.; Batandier, C.; De Oliveira, F.; Fontaine, E.; Leverve, X. Metformin inhibits mitochondrial permeability transition and cell death: A pharmacological in vitro study. Biochem. J. 382:877-884; 2004.
14. Hanstein, W. G. Uncoupling of oxidative phosphorylation. Biochim. Biophys. Acta 456:129-148; 1976.
15. Hengartner, M. O. The biochemistry of apoptosis. Nature 407:770-776; 2000.
16. Ilan, Y. Towards a bank of cryopreserved hepatocytes: Which cell to freeze? J. Hepatol. 37:145-146; 2002.
17. Jamal, H. Z.; Weglarz, T. C.; Sandgren, E. P. Cryopreserved mouse hepatocytes retain regenerative capacity in vivo. Gastroenterology 118:390-394; 2000.
18. Janssens, D.; Delaive, E.; Remade, J.; Michiels, C. Protection by bilobalide of the ischaemia-induced alterations of the mitochondrial respiratory activity. Fundam. Clin. Pharmacol. 14:193-201; 2000.
19. Kuznetsov, A. V.; Schneeberger, S.; Seiler, R.; Brandacher, G.; Mark, W.; Steurer, W.; Saks, V.; Usson, Y.; Margreiter, R.; Gnaiger, E. Mitochondrial defects and heterogeneous cytochrome c release after cardiac cold ischemia and reperfusion. Am. J. Physiol. Heart Circ. Physiol. 286:H1633-1641; 2004.
20. Kwong, L. K.; Sohal, R. S. Substrate and site specificity of hydrogen peroxide generation in mouse mitochondria. Arch. Biochem. Biophys. 350:118-126; 1998.
21. Lloyd, T. D.; Orr, S.; Skett, P.; Berry, D. P.; Dennison, A. R. Cryopreservation of hepatocytes: A review of current methods for banking. Cell Tissue Bank 4:3-15; 2003.
22. Lloyd, T. D.; Orr, S.; Berry, D. P.; Dennison, A. R. Development of a protocol for cryopreservation of hepatocytes for use in bioartificial liver systems. Ann. Clin. Lab. Sci. 34:165-174; 2004.
23. Mahler, S.; Desille, M.; Fremond, B.; Chesne, C.; Guillouzo, A.; Campion, J. P.; Clement, B. Hypothermic storage and cryopreservation of hepatocytes: The protective effect of alginate gel against cell damages. Cell Transplant. 12:579-592; 2003.
24. Matsushita, T.; Yagi, T.; Hardin, J. A.; Cragun, J. D.; Crow, F. W.; Bergen, 3rd, H. R.; Gores, G. J.; Nyberg, S. L. Apoptotic cell death and function of cryopreserved porcine hepatocytes in a bioartificial liver. Cell Transplant. 12:109-121; 2003.
25. Mosmann, T. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J. Immunol. Methods 65:55-63; 1983.
26. Nicolli, A.; Basso, E.; Petronilli, V.; Wenger, R. M.; Bernardi, P. Interactions of cyclophilin with the mitochondrial inner membrane and regulation of the permeability transition pore, and cyclosporin A-sensitive channel. J. Biol. Chem. 271:2185-2192; 1996.
27. Nogueira, V.; Piquet, M. A.; Devin, A.; Fiore, C.; Fontaine, E.; Brandolin, G.; Rigoulet, M.; Leverve, X. M. Mitochondrial adaptation to in vivo polyunsaturated fatty acid deficiency: increase in phosphorylation efficiency. J. Bioenerg. Biomembr. 33:53-61; 2001.
28. Palmeira, C. M.; Moreno, A. J.; Madeira, V. M.; Wallace, K. B. Continuous monitoring of mitochondrial membrane potential in hepatocyte cell suspensions. J. Pharmacol. Toxicol. Methods 35:35-43; 1996.
29. Petronilli, V.; Nicolli, A.; Costantini, P.; Colonna, R.; Bernardi, P. Regulation of the permeability transition pore, a voltage-dependent mitochondrial channel inhibited by cyclosporin A. Biochim. Biophys. Acta 1187:255-259; 1994.
30. Piquet, M. A.; Nogueira, V.; Devin, A.; Sibille, B.; Filippi, C.; Fontaine, E.; Roulet, M.; Rigoulet, M.; Leverve, X. M. Chronic ethanol ingestion increases efficiency of oxidative phosphorylation in rat liver mitochondria. FEBS Lett. 468:239-242; 2000.
31. Sammut, I. A.; Thorniley, M. S.; Simpkin, S.; Fuller, B. J.; Bates, T. E.; Green, C. J. Impairment of hepatic mitochondrial respiratory function following storage and orthotopic transplantation of rat livers. Cryobiology 36:49-60; 1998.
32. Sammut, I. A.; Burton, K.; Balogun, E.; Sarathchandra, P.; Brooks, K. J.; Bates, T. E.; Green, C. J. Time-dependent impairment of mitochondrial function after storage and transplantation of rabbit kidneys. Transplantation 69:1265-1275; 2000.
33. Sazanov, L. A.; Hinchliffe, P. Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus. Science 311:1430-1436; 2006.
34. Skulachev, V. P. Bioenergetic aspects of apoptosis, necrosis and mitoptosis. Apoptosis 11:473-485; 2006.
35. Sokal, E. M.; Smets, F.; Bourgois, A.; Van Maldergem, L.; Buts, J. P.; Reding, R.; Otte, J. B.; Evrard, V.; Latinne, D.; Vincent, M. F.; Moser, A.; Soriano, H. E. Hepatocyte transplantation in a 4-year-old girl with peroxisomal biogenesis disease: Technique, safety, and metabolic follow-up. Transplantation 76:735-738; 2003.
36. Steinberg, P.; Fischer, T.; Kiulies, S.; Biefang, K.; Platt, K. L.; Oesch, F.; Bottger, T.; Bulitta, C.; Kempf, P.; Hengstler, J. Drug metabolizing capacity of cryopreserved human, rat, and mouse liver parenchymal cells in suspension. Drug Metab. Dispos. 27:1415-1422; 1999.
37. Stephenne, X.; Najimi, M.; Smets, F.; Reding, R.; de Ville de Goyet, J.; Sokal, E. M. Cryopreserved liver cell transplantation controls ornithine transcarbamylase deficient patient while awaiting liver transplantation. Am. J. Transplant. 5:2058-2061; 2005.
38. Stephenne, X.; Najimi, M.; Sibille, C.; Nassogne, M. C.; Smets, F.; Sokal, E. M. Sustained engraftment and tissue enzyme activity after liver cell transplantation for argininosuccinate lyase deficiency. Gastroenterology 130:1317-1323; 2006.
39. Terada, H. Uncouplers of oxidative phosphorylation. Environ. Health Perspect. 87:213-218; 1990.
40. Terry, C.; Mitry, R. R.; Lehec, S. C.; Muiesan, P.; Rela, M.; Heaton, N. D.; Hughes, R. D.; Dhawan, A. The effects of cryopreservation on human hepatocytes obtained from different sources of liver tissue. Cell Transplant. 14:585-594; 2005.
41. Terry, C.; Dhawan, A.; Mitry, R. R.; Lehec, S. C.; Hughes, R. D. Preincubation of rat and human hepatocytes with cytoprotectants prior to cryopreservation can improve viability and function upon thawing. Liver Transpl. 12:165-177; 2006.
42. Vanhulle, V. P.; Martiat, G. A.; Bontemps, F.; Vincent, M. F.; Pycke, J. M.; Verbeeck, R. K.; Horsmans, Y.; Delzenne, N. Cryopreservation of rat precision-cut liver slices is associated with major metabolic stress and ionic perturbations. Cell Physiol. Biochem. 13:103-112; 2003.
43. Veitch, K.; Hombroeckx, A.; Caucheteux, D.; Pouleur, H.; Hue, L. Global ischaemia induces a biphasic response of the mitochondrial respiratory chain. Anoxic pre-perfusion protects against ischaemic damage. Biochem. J. 281(Pt. 3):709-715; 1992.
44. Weyermann, J.; Lochmann, D.; Zimmer, A. A practical note on the use of cytotoxicity assays. Int. J. Pharm. 288:369-376; 2005.
45. Yagi, T.; Hardin, J. A.; Valenzuela, Y. M.; Miyoshi, H.; Gores, G. J.; Nyberg, S. L. Caspase inhibition reduces apoptotic death of cryopreserved porcine hepatocytes. Hepatology 33:1432-1440; 2001.