Lessons from natural cold-induced dormancy to organ preservation in medicine and biotechnology: From the "backwoods to the bedside"

Topics in Current Genetics

Volumn 21, Issue , 2010, Pages 253-278

  Fuller, Barry ^a   Guibert, Edgardo ^a,b   Rodríguez, Joaquín ^a,b  

^a ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

^b UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 77955955971     PISSN: 16102096     EISSN: 16106970     Source Type: Book Series    
DOI: 10.1007/978-3-642-12422-8_14     Document Type: Article

References (124)

1. Alijani MR, Cutler JA, Del Valle C, Morres D, Fawzy A, Pechan B, Helfrich G (1985) Single donor cold storage versus machine perfusion in cadaver kidney preservation. Transplantation 40:659-661
2. Andrews M (2007) Advances in molecular biology of hibernation in mammals. BioEssays 29:431-440
3. Arrhenius SA (1915) Quantitative laws in biological chemistry. G Bell & Sons, London
4. Baicu SC, Taylor MJ, Brockbank KG (2006) The role of preservation solution on acid-base regulation during machine perfusion of kidneys. Clin Transplant 20:113-121
5. Bartels-Stringer M, Wetzels JF, Wouterse AC, Steenbergen E, Russel FG, Kramers C (2005) Iron chelators do not reduce cold-induced cell injury in the isolated perfused rat kidney model. Nephrol Dial Transplant 20:2646-2653
6. Belzer FO, May R, Berry M, Lee JC (1970) Short term preservation of porcine livers. J Surg Res 10:55-61
7. Bennett LE, Glascock R, Breen T, Ellison M, Daily OP (1993) Organ donation in the United States: 1988 through 1992. Clin Transpl 5:85-93
8. Bessems M, Doorschodt BM, van Vliet AK, van Gulik TM (2005a) Improved machine perfusion preservation of the non-heart-beating donor rat liver using polysol: a new machine perfusion preservation solution. Liver Transpl 11:1379-1388
9. Bessems M, Doorschodt BM, van Marle J, Vreeling H, Meijer AJ, van Gulik TM (2005b) Improved rat liver preservation by hypothermic continuous machine perfusion using polysol, a new, enriched preservation solution. Liver Transpl 11:539-546
10. Bickford RG, Winton FR (1937) The influence of temperature on the isolated kidney of the dog. J Physiol (Lond) 89:198-219
11. Bickler P, Buck L (2007) Hypoxia tolerance in reptiles, amphibians, and fishes: life with variable oxygen availability. Annu Rev Physiol 69:145-170
12. Blackstone E, Roth MB (2007) Suspended animation-like state protects mice from lethal hypoxia. Shock 27:370-372
13. Blackstone E, Morrison M, Roth MB (2005) H2S induces a suspended animation-like state in mice. Science 308:518
14. Borgmann U (1974) A theoretical description of biological rates. J Theor Biol 45:171-182
15. Boyle R (1683) New experiments and observations touching cold. R. Davis, London
16. Breton S, Brown D (1998) Cold-induced microtubule disruption and relocalization of membrane proteins in kidney epithelial cells. J Am Soc Nephrol 9:155-166
17. Brodie T (1903) The perfusion of surviving organs. J Physiol (Lond) 29:266-275
18. Brooks SP, Storey K (1994) cGMP-stimulated protein kinase phosphorylates protein kinase in an anoxia-tolerant marine mollusc. J Comp Physiol B 160:309-316
19. Calne RY, Pegg DE, Pryse-Davies J, Brown FL (1963) Renal preservation by ice-cooling: an experimental study relating to kidney transplantation from cadavers. Br Med J 2:651-655
20. Carrel A, Lindbergh CA (1935) The culture of whole organs. Science 81:621-623
21. Carrel A, Lindbergh CA (1938) The culture of organs. Hoeber, NewYork
22. Casillas-Ramírez A, Mosbah IB, Ramalho F, Roselló-Catafau J, Peralta C (2006) Past and future approaches to ischemia-reperfusion lesion associated with liver transplantation. Life Sci 79:1181-1194
23. Changani KK, Fuller BJ, Bryant DJ, Bell JD, Ala-Korpela M, Taylor-Robinson SD, Moore DP, Davidson BR (1997) Non-invasive assessment of ATP regeneration potential of the preserved donor liver. A 31P MRS study in pig liver. J Hepatol 26:336-342
24. Changani KK, Davidson BR, Bell J, Taylor-Robinson S, Fuller B (1998) Enhanced energy metabolism at hypothermia following addition of a prostacyclin derivative in porcine liver. CryoLetters 19:131-140
25. Churchill TA, Cheetham KM, Fuller BJ (1994) Glycolysis and energy metabolism in rat liver during warm and cold ischemia: evidence of an activation of the regulatory enzyme phosphofructokinase. Cryobiology 31:441-452
26. Collins GM, Bravo-Shugarman M, Terasaki PI (1969) Kidney preservation for transportation. Initial perfusion and 30 hours' ice storage. Lancet 2:1219-1222
27. Collins L, Sawyer GJ, Zhang XH, Gustafsson K, Fabre JW (2000) In vitro investigation of factors important for the delivery of an integrin-targeted nonviral DNA vector in organ transplantation. Transplantation 69:1168-1176
28. Crowe JH, Hoekstra FA, Crowe LM, Anchordoguy TJ, Drobnis E (1989) Lipid phase transitions measured in intact cells with Fourier transform infrared spectroscopy. Cryobiology 26:76-84
29. Daemen MA, de Vries B, Buurman WA (2003) Apoptosis and inflammation in renal reperfusion injury. Transplantation 73:1693-1700
30. Dutkowski P, Schönfeld S, Heinrich T, Watzka M, Winkelbach V, Krysiak M, Odermatt B, Junginger T (1999) Reduced oxidative stress during acellular reperfusion of the rat liver after hypothermic oscillating perfusion. Transplantation 68:44-50
31. Dutkowski P, Graf R, Clavien PA (2006) Rescue of the cold preserved rat liver by hypothermic oxygenated machine perfusion. Am J Transplant 6:903-912
32. Ellermann J, Gewiese B, David H, Stiller D, Plötz M, Wolf KJ, L€uning M (1992) Electron microscopic and 31-P NMR studies of ischemic injured rat livers during preservation and reflow. Exp Toxicol Pathol 44:245-253
33. Faenza A, Catena F, Nardo B, Montalti R, Capocasale E, Busi N, Boggi U, Vistoli F, Di Naro A, Albertazzi A, Mosca F, Cavallari A (2001) Kidney preservation with university ofWisconsin and Celsior solution: a prospective multicenter randomized study. Transplantation 72:1274-1277
34. Farr DA, Fuhrman FA (1965) Role of diffusion of oxygen in the respiration of tissues at different temperatures. J Appl Physiol 20:637-646
35. Feltkamp CA, van der Waerden AW (1982) Low temperature -induced displacement of cholesterol and intramembrane particles in nuclear membranes of mouse leukemia cells. Cell Biol Int Rep 6:137-145
36. Fuhrman FA (1956) Oxygen consumption of mammalian tissues at reduced temperatures. Proc Natl Acad Sci USA 451:50-51
37. Fujita S, Hamamoto I, Nakamura K, Tanaka K, Ozawa K (1993a) Evaluation of oxygen necessity during hypothermic liver perfusion. Nippon Geka Hokan 62:228-240
38. Fujita S, Hamamoto I, Nakamura K, Tanaka K, Ozawa K (1993b) Isolated perfusion of rat livers: effect of temperature on O2 consumption, enzyme release, energy store, and morphology. Nippon Geka Hokan 62:58-70
39. Fuller BJ (1999) Organ preservation: the profit and loss account of using hypothermia to maintain viability. Transplant Rev 13:55-66
40. Fuller BJ (2003) Gene expression in response to low temperatures in mammalian cells: a review of current ideas. CryoLetters 24:95-102
41. Fuller BJ, So P-W (2001) Hepatic uptake of solutes from the preservation solution during hypothermic storage: a (1)H NMR study in rat liver. Cryobiology 42:307-313
42. Fuller BJ, Marley S, Green CJ (1985) Gluconeogenesis in stored kidneys from normal and coldacclimated rats. CryoLetters 6:91-98
43. Fuller BJ, Gower J, Green CJ (1988) Free radical damage and organ preservation: fact or fiction? A review of the interrelationship between oxidative stress and physiological ion disbalance. Cryobiology 25:377-393
44. Fuller BJ, Busza AL, Proctor E (1990) Possible resuscitation of liver function by hypothermic reperfusion in vitro after prolonged (24-hour) cold preservation - a 31P NMR study. Transplantation 50:511-513
45. Halloran PF, Aprile M (1987) A randomised prospective trial of cold-storage versus pulsatile perfusion for cadaveric kidney preservation. Transplantation 43:827-831
46. Hansen TN, D'Alessandro A, Southard JH (1997) Reduced renal vascular injury following warm ischemia and preservation by hypothermic machine perfusion. Transplant Proc 29: 3577-3579
47. Heilbrunn LV (1937) An outline of general physiology. WB Saunders, Philadelphia, USA
48. Henry ML, Sommer B, Ferguson R (1988) M. Improved immediate function of renal allografts with Belzer perfusate. Transplantation 45:73-75
49. Hobbs KE, Hunt A, Palmer D, Badrick F, Morris A, Mitra S, Peacock J, Immelman E, Riddell AG (1968) Hypothermic low flow liver perfusion as a means of porcine hepatic storage for 6 hours. Br J Surg 55:696-703
50. Hochachka P (1986) Defense strategies against hypoxia and hypothermia. Science 231:234-241
51. Hochachka PW, Buck LT, Doll CJ, Land SC (1996) Unifying theory of hypoxia tolerance: molecular/metabolic defense and rescue mechanisms for surviving oxygen lack. Proc Natl Acad Sci USA 93:9493-9498
52. Holden C, Storey K (1997) Second messenger and c-AMP dependent protein kinase responses to dehydration and anoxia stress in frogs. J Comp Physiol B 167:305-312
53. Hume DM, Merrill J, Miller BF, Thorn GW (1955) Experiences with renal homotransplantation in the human: report of nine cases. J Clin Invest 34:327-382
54. Humphries AL, Russell R, Christopher P, Goodrich S, Stoddard L, Moretz WH (1964a) Succesful reimplantation of twenty-four-hour stored kidney to nephrectomized dog. Ann N Y Acad Sci 120:496-505
55. Humphries AL, Russell R, Gregory J, Carter R, Moretz WH (1964b) Hypothermic perfusion of the canine kidney for 48 hours followed by reimplantation. Am Surg 30:748-752
56. Humphries AL Jr, Russell R, Stoddard L, Moretz WH (1968a) Successful five-day kidney preservation. Perfusion with hypothermic, plasma. Invest Urol 5:609-618
57. Humphries AL, Russell R, Stoddard LD, Moretz WH (1968b) Perfusion of dog kidneys with cooled medium 199 followed by auto or allotransplantation. In: Norman JC (ed) Organ perfusion and preservation. Appleton Century Crofts, NewYork, pp 13-26
58. Jassem W, Heaton ND (2004) The role of mitochondria in ischemia/reperfusion injury in organ transplantation. Kidney Int 66:514-517
59. Jassem W, Fuggle SV, Rela M, Koo DD, Heaton ND (2002) The role of mitochondria in ischemia/ reperfusion injury. Transplantation 73:493-499
60. Johansson BW (1996) The hibernator heart - nature's model of resistance to ventricular fibrillation. Cardiovasc Res 31:826-832
61. Johnson CP, Roza A, Adams MB (1990) Local procurement with pulsatile perfusion gives excellent results and minimises initial cost associated with renal transplantation. Transplant Proc 22:385
62. Keeler R, Swinney J, Taylor R, Uldall MB (1966) The problem of renal preservation. Br J Urol 38:653-655
63. Kupiec-Weglinski JW, Busuttil RW (2005) Ischemia and reperfusion injury in liver transplantation. Transplant Proc 37:1653-1656
64. Lee CY, Jain S, Duncan H, Zhang JX, Jones J, Southard JH, Clemens M (2003) Survival transplantation of preserved non-heart-beating donor rat livers. Transplantation 76:1432-1436
65. Lemaster JJ, Thurman RG (1993) Hypoxia and reperfusion injury to liver. Prog Liver Dis 11:85-114
66. Light JA (1998) A 25 year history of kidney transplantation in the Washington Hospital Centre. In: Cecka D, Terasaki PI (eds) Chapter 13, Clinical Transplants 1998, UCLA Tissue Typing Laboratory, pp 159-168
67. Lindell SL, Compagnon P, Mangino MJ, Southard JH (2005) UW solution for hypothermic machine perfusion of warm ischemic kidneys. Transplantation 79:1358-1361
68. Locke FS, Rosenheim O (1907) Contributions to the physiology of the isolated heart: the consumption of dextrose by mammalian cardiac muscle. J Physiol (Lond) 36:205-220
69. Lockett CJ, Busza AL, Toffa SK, Proctor E, Fuller BJ (1995) Resuscitation of cardiac energy metabolism in the rabbit heart by brief hypothermic reperfusion after preservation studied by 31P NMR spectroscopy. Transpl Int 8:8-12
70. Lopez-Neblina F, Toledo AH, Toledo-Pereyra LH (2005) Molecular biology of apoptosis in ischemia and reperfusion. J Invest Surg 18:335-350
71. Lyman CP (1982) The hibernating state. In: Willis JS, Malan A, Wang LCH (eds) Hibernation and torpor in mammals and birds. Academic Press, NewYork, pp 12-53
72. Lyman CP, Willis JS, Malan A, Wang LCH (1982) Hibernation and torpor in mammals and birds. Academic Press, New York
73. McAnulty JF (1998) The effect of calcium on hypothermia-facilitated resuscitation of warm ischemic kidney tissue slices: a role for the mitochondrial permeability transition pore? Cryobiology 36:12-19
74. McAnulty JF, Foley JD, Reid TW, Heath TD, Waller KR, Murphy CJ (2004) Suppression of cold ischemic injury in stored kidneys by the antimicrobial peptide bactenecin. Cryobiology 49:230-240
75. McCabe M, Maguire DJ (2005) Effects of temperature on oxygen transport in sheets and spheres of respiring tissues. Adv Exp Med Biol 566:105-109
76. Merion RM, Oh H, Port F, Toledo-Pereyra LH, Turcotte JG (1991) A prospective controlled trial of cold storage versus machine perfusion preservation in cadaveric renal transplantation. Transplantation 50:230-233
77. Milsom W, Beth Zimmer M, Harris B (1999) Regulation of cardiac rhythm in hibernating mammals. Comp Biochem Physiol 124:383-391
78. Minor T, Sitzia M, Dombrowski F (2005) Kidney transplantation from non-heart-beating donors after oxygenated low-flow machine perfusion preservation with histidine-tryptophanketoglutarate solution. Transpl Int 17:707-712
79. Moers C, Smits JM, Maathuis MH, Treckmann J, van Gelder F, Napieralski BP, van Kasterop-Kutz M, van der Heide JJ, Squifflet JP, van Heurn E, Kirste GR, Rahmel A, Leuvenink HG, Paul A, Pirenne J, Ploeg RJ (2009) Machine perfusion or cold storage in deceased-donor kidney transplantation. N Engl J Med 360:7-19
80. NHS Blood and Transplant (2008) Transplant activity in the UK: 2007-2008 http://www.organdonation. nhs.uk/ukt/
81. NHS Blood and Transplant Annual Activity Report 2008-2009, http://www.organdonation.nhs. uk/ukt/
82. Palmer JF (1825) The works of John Hunter FRS with notes. Longman, Reese, Orme, Brwon, Green & Longman, London
83. Pegg DE (1978) An approach to hypothermic renal preservation. Cryobiology 15:1-17
84. Pegg D, Wusteman MC, Foreman J (1981) Metabolism of normal and ischemically injured rabbit kidneys during perfusion for 48 hours at 10 C. Transplantation 32:437-443
85. Peltz M, He TT, Adams GA 4th, Koshy S, Burgess SC, Chao RY, Meyer DM, Jessen ME (2005) Perfusion preservation maintains myocardial ATP levels and reduces apoptosis in an ex vivo rat heart transplantation model. Surgery 138:795-805
86. Pinsky DJ, Yan SF, Lawson C, Naka Y, Chen JX, Connolly ES Jr, Stern DM (1995) Hypoxia and modification of the endothelium: implications for regulation of vascular homeostatic properties. Semin Cell Biol 6:283-294
87. Piper HM, Meuter K, Sch€afer C (2003) Cellular mechanisms of ischemia-reperfusion injury. Ann Thorac Surg 75:S644-S648
88. Pizzaro MD, Rodriguez JV, Mamprin M, Fuller B, Mann B, Motterlini M, Guibert E (2009) Protective effects of a carbon monoxide-releasing molecule (CORM-3) during hepatic cold preservation. Cryobiology 58:248-256
89. Polyak MM, Arrington BO, Stubenbord WT, Kapur S, Kinkhabwala M (1999) Prostaglandin E1 influences pulsatile preservation characteristics and early graft function in expanded criteria donor kidneys. J Surg Res 85:17-25
90. Rauen U, de Groot H (2002) Mammalian cell injury induced by hypothermia - the emerging role for reactive oxygen species. Biol Chem 383:477-488
91. Rauen U, de Groot H (2004) New insights into the cellular and molecular mechanisms of cold storage injury. J Investig Med 52:299-309
92. Rodriguez JV, Federico MB, Pizarro MD, Guibert EE, Scandizzi AL (2008) A device to measure oxygen consumption during the hypothermic perfusion of the liver. V Latin American Congress of Artificial Organs and Biomaterials, Ouro Preto, Brasil, N504
93. Rosenthal J, Danovitch G, Wilkinson A, Ettenger RB (1991) The high cost of delayed graft function in cadaveric renal transplantation. Transplantation 51:1115-1118
94. Ruiz J, Lillihie RC (1974) Pancreas. In: Karow A, Abouna G, Humphries AL (eds) Organ preservation for transplantation. Little Brown & Co, Boston, pp 372-382
95. Salahudeen AK, Huang H, Patel P, Jenkins JK (2000) Mechanism and prevention of cold storageinduced human renal tubular cell injury. Transplantation 70:1424-1431
96. Salehi P, Bigam DL, Ewaschuk JB, Madsen KL, Sigurdson GT, Jewell LD, Churchill TA (2008) Alleviating intestinal ischemia-reperfusion injury in an in vivo large animal model: developing an organ-specific preservation solution. Transplantation 85:878-884
97. Sandouka A, Fuller BJ, Mann BE, Green CJ, Foresti R, Motterlini R (2006) Treatment with CO-RMs during cold storage improves renal function at reperfusion. Kidney Int 69:239-247
98. Savolainen H, Tenhunen R, Elovaara E, Tossavainen A (1980) Cumulative biochemical effects of repeated subclinical hydrogen sulfide intoxication in mouse brain. Int Arch Occup Environ Health 46:87-92
99. Schloerb PR, Waldorf R, Welsh JS (1959) The protective effect of kidney hypothermia on total renal ischemia. Surg Gynecol Obstet 109:561-565
100. Silacci P, Desgeorges A, Mazzolai L, Chambaz C, Hayoz D (2001) Flow pulsatility is a critical determinant of oxidative stress in endothelial cells. Hypertension 38:1162-1166
101. Southard J, Belzer FO (1995) Organ preservation. Annu Rev Med 46:235-247
102. Southard JH, Van der Laan NC, Lutz M, Pavlock GS, Belzer JP, Belzer FO (1983) Comparison of the effect of temperature on kidney cortex mitochondria from rabbit, dog, pig, and human: Arrhenius plots of ADP-stimulated respiration. Cryobiology 20:395-400
103. Southard JH, Lutz M, Ametani M, Belzer FO (1984) Stimulation of ATP synthesis in hypothermically perfused dog kidneys by adenosine and PO4. Cryobiology 21:13-19
104. Starzl TE (2000) History of clinical transplantation. World J Surg 24:759-782
105. Starzl TE, Hakala TR, Shaw BW Jr, Hardesty RL, Rosenthal TJ, Griffith BP, Iwatsuki S, Bahnson HT (1984) A flexible procedure for multiple cadaveric organ procurement. Surg Gynecol Obstet 158:223-230
106. Stefanovich P, Ezzell RM, Sheehan SJ, Tompkins RG, Yarmush ML, Toner M (1996) Effects of hypothermia on the function, membrane integrity, and cytoskeletal structure of hepatocytes. Cryobiology 32:389-403
107. Stickel DL, Chen KM, Robinson R (1968) The effects of organ perfusion and other factors on the immediate function of canaine renal autografts. In: Norman JC (ed) Organ perfusion for preservation. Appleton-Century-Crofts, NewYork, pp 61-69
108. Storey K (2002) Life in the slow lane: molecular mechanisms of aestivation. Comp Biochem Physiol 133A:733-754
109. Storey K (2004) Cold ischemic organ preservation: lessons from natural systems. JInvestMed 52:315-322
110. Storey K, Storey J (1990) Facultative metabolic rate depression: molecular regulation and biochemical adaptation in anaerobiosis, hibernation and estivation. Q Rev Biol 65:145-174
111. Storey K, Storey J (2004a) Strategies for exploration of freeze responsive gene expression: advances in vertebrate freeze tolerance. Cryobiology 48:134-145
112. Storey K, Storey J (2004b) Metabolic rate depression in animals: transcriptional and translational controls. Biol Rev Camb Philos Soc 79:207-233
113. Storey K, Storey J (2007) Tribute to P. L. Lutz: putting life on 'pause' - molecular regulation of hypometabolism. J Exp Biol 210:1700-1714
114. Storey KB, Heldmaier G, Rider MH (2010) Mammalian Hibernation: Physiology, Cell Signaling, and Gene Controls on Metabolic Rate Depression XX-XX
115. T' Hart NA, van der Plaats A, Faber A, Leuvenink HG, Olinga P, Wiersema-Buist J, Verkerke GJ, Rakhorst G, Ploeg RJ (2005) Oxygenation during hypothermic rat liver preservation: an in vitro slice study to demonstrate beneficial or toxic oxygenation effects. Liver Transpl 11:1403-1411
116. Tamaki T, Kamada N, Wight D, Pegg D (1987) Successful 48-hour preservation of the rat liver by continuous hypothermic perfusion with haemaccel-isotonic citrate solution. Transplantation 43:468-471
117. Teoh NC, Farrell GC (2003) Hepatic ischemia reperfusion injury: pathogenic mechanisms and basis for hepatoprotection. J Gastroenterol Hepatol 18:891-902
118. Tesi R, Elkhammas E, Davies E, Henry M (1994) Pulsatile kidney perfusion for evaluation of high-risk kidney donors safely expands the donor pool. Transplant Proc 26:241-242
119. van der Plaatz A, 'T Hart NA, Verkerke GJ, Leuvenink HG, Ploeg RJ, Rakhorst G (2004) The Groningen hypothermic liver perfusion pump: functional evaluation of a new machine perfusion system. Ann Biomed Eng 32:623-631
120. Vardanian A, Busuttil R, Kupiec-Weglinski J (2008) Molecular mediators of liver ischemia and reperfusion injury: a brief review. Mol Med 14:337-345
121. Wight J, Chilcott J, Holmes M, Brewer N (2003) The clinical cost effectiveness of pulsatile machine perfusion versus cold storage of kidneys for transplantation retreived from heartbeating and non-heart beating donors. Health Technol Assess 7:1-94
122. Williams GM (1986) Kidney preservation and early function in the cyclosporine era: an overview. Transplant Proc 18(Suppl 1):38-40
123. Willis JS, Ellory JC, Becker JH (1978) Na-K pump and Na-K-ATPase: disparity of their temperature sensitivity. Am J Physiol 235:C159-C167
124. Zimmermann F, Diettz H, Kohler CH, Kilian N, Kosterhon J, Scholz R (1982) Effects of hypothermia on anabolic and catabolic processes and on oxygen consumption in perfused rat livers. In: Pegg DE, Jacobsen IA, Halasz N (eds) Organ preservation: basic and applied aspects. MTP Press, Lancaster, pp 121-126