Hypothermic preconditioning of endothelial cells attenuates cold-induced injury by a ferritin-dependent process

Free Radical Biology and Medicine

Volumn 46, Issue 5, 2009, Pages 680-691

  Zieger, Michael A J ^a,b   Gupta, Mahesh P ^a  

^a METHODIST RESEARCH INSTITUTE   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Endothelial cells; Ferritin; Free radicals; Heme oxygenase; Hypothermia; Preconditioning

Indexed keywords

BLEOMYCIN; DEFEROXAMINE; FERRITIN; GLUTATHIONE; HEME OXYGENASE 1; IRON;

ARTICLE; CELL PROTECTION; CELL VIABILITY; COLD INJURY; CONTROLLED STUDY; CORONARY ARTERY; ENDOTHELIUM CELL; ENZYME RELEASE; HUMAN; HUMAN CELL; HYPOTHERMIA; OXIDATIVE STRESS; PRIORITY JOURNAL;

CELL PROLIFERATION; CELLS, CULTURED; COLD TEMPERATURE; CORONARY VESSELS; DEFEROXAMINE; ENDOTHELIAL CELLS; FERRITINS; GLUTATHIONE; HEME OXYGENASE-1; HUMANS; HYPOTHERMIA, INDUCED; IRON; ISCHEMIC PRECONDITIONING; L-LACTATE DEHYDROGENASE; MYOCARDIAL REPERFUSION INJURY; OXIDATIVE STRESS;

EID: 59249092359     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2008.12.004     Document Type: Article

References (56)

1. Kevelaitis E., Nyborg N.C., and Menasche P. Coronary endothelial dysfunction of isolated hearts subjected to prolonged cold storage: patterns and contributing factors. J. Heart Lung Transplant. 18 (1999) 239-247
2. Perrault L.P., Nickner C., Desjardins N., Dumont E., Thai P., and Carrier M. Improved preservation of coronary endothelial function with Celsior compared with blood and crystalloid solutions in heart transplantation. J. Heart Lung Transplant. 20 (2001) 549-558
3. Hiramatsu T., Forbess J.M., Miura T., Nomura F., and Mayer Jr. J.E. Additive effects of l-arginine infusion and leukocyte depletion on recovery after hypothermic ischemia in neonatal lamb hearts. J. Thorac. Cardiovasc. Surg. 110 (1995) 172-179
4. Day J.D., Rayburn B.K., Gaudin P.B., Baldwin III W.M., Lowenstein C.J., Kasper E.K., Baughman K.L., Baumgartner W.A., Hutchins G.M., and Hruban R.H. Cardiac allograft vasculopathy: the central pathogenetic role of ischemia-induced endothelial cell injury. J. Heart Lung Transplant. 14 (1995) S142-149
5. Kristek F., Torok J., and Sikulova J. Morphological and functional alterations in endothelium, smooth muscle, and nerve fibers in rabbit aorta after storage at 4 degrees C. Cryobiology 30 (1993) 376-385
6. Baric D., Cebotari S., Mertsching H., Leyh R., and Haverich A. Could 37 degrees C storage temperature extend homovital valve allograft viability?. J. Heart Valve Dis. 13 (2004) 494-499 discussion 499-500
7. Crowe D.M., Hurley J.V., Mitchell G.M., Niazi Z., and Morrison W.A. Long-term studies of cold-stored rabbit femoral artery and vein autografts. Br. J. Plast. Surg. 51 (1998) 291-299
8. Redondo J., Manso A.M., Pacheco M.E., Hernandez L., Salaices M., and Marin J. Hypothermic storage of coronary endothelial cells reduces nitric oxide synthase activity and expression. Cryobiology 41 (2000) 292-300
9. Roberts J.R., Rowe P.A., and Demaine A.G. Activation of NF-kappaB and MAP kinase cascades by hypothermic stress in endothelial cells. Cryobiology 44 (2002) 161-169
10. Dahdah N.S., Russo P., and Wagerle L.C. Phosphorylation in coronary artery cold-induced contraction in the newborn lamb. Cryobiology 42 (2001) 40-48
11. Rauen U., Polzar B., Stephan H., Mannherz H.G., and de Groot H. Cold-induced apoptosis in cultured hepatocytes and liver endothelial cells: mediation by reactive oxygen species. FASEB J. 13 (1999) 155-168
12. 2 formation. FASEB J. 14 (2000) 1953-1964
13. Zieger M.A.J., and Gupta M.P. Endothelial cell preservation at 10 degrees C minimizes catalytic iron, oxidative stress, and cold-induced injury. Cell Transplant. 15 (2006) 499-510
14. Zieger M.A., Glofcheski D.J., Lepock J.R., and Kruuv J. Factors influencing survival of mammalian cells exposed to hypothermia. IV. Effects of iron chelation. Cryobiology 27 (1990) 452-464
15. Salahudeen A.A., Jenkins J.K., Huang H., Ndebele K., and Salahudeen A.K. Overexpression of heme oxygenase protects renal tubular cells against cold storage injury: studies using hemin induction and HO-1 gene transfer. Transplantation 72 (2001) 1498-1504
16. Ely D., Dunphy G., Dollwet H., Richter H., Sellke F., and Azodi M. Maintenance of left ventricular function (90%) after twenty-four-hour heart preservation with deferoxamine. Free Radic. Biol. Med. 12 (1992) 479-485
17. Wille T., de Groot H., and Rauen U. Improvement of the cold storage of blood vessels with a vascular preservation solution: study in porcine aortic segments. J. Vasc. Surg. 47 (2008) 422-431
18. Menasche P., Grousset C., Mouas C., and Piwnica A. A promising approach for improving the recovery of heart transplants: prevention of free radical injury through iron chelation by deferoxamine. J. Thorac. Cardiovasc. Surg. 100 (1990) 13-21
19. Myers C.L., Weiss S.J., Kirsh M.M., Shepard B.M., and Shlafer M. Effects of supplementing hypothermic crystalloid cardioplegic solution with catalase, superoxide dismutase, allopurinol, or deferoxamine on functional recovery of globally ischemic and reperfused isolated hearts. J. Thorac. Cardiovasc. Surg. 91 (1986) 281-289
20. Pohlman T.H., and Harlan J.M. Adaptive responses of the endothelium to stress. J. Surg. Res. 89 (2000) 85-119
21. Culic O., Decking U.K., and Schrader J. Metabolic adaptation of endothelial cells to substrate deprivation. Am. J. Physiol. 276 (1999) C1061-1068
22. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65 (1983) 55-63
23. Rauen U., Noll T., Piper H.M., Lauchart W., Becker H.D., and De Groot H. Endothelial cell toxicity of preservation solutions: comparison of endothelial cells of different origin and dependence on growth state. Cryobiology 31 (1994) 144-153
24. Ou R., Gavin J.B., Esmore D.S., and Rosenfeldt F.L. Increased temperature reduces the protective effect of University of Wisconsin solution in the heart. Ann. Thorac. Surg. 68 (1999) 1628-1634 discussion 1634-1625
25. Mankad P., Slavik Z., and Yacoub M. Endothelial dysfunction caused by University of Wisconsin preservation solution in the rat heart: the importance of temperature. J. Thorac. Cardiovasc. Surg. 104 (1992) 1618-1624
26. Gutteridge J.M., and Hou Y.Y. Iron complexes and their reactivity in the bleomycin assay for radical-promoting loosely-bound iron. Free Radic. Res. Commun. 2 (1986) 143-151
27. 2. J. Clin. Invest. 89 (1992) 794-802
28. Kuross S.A., Rank B.H., and Hebbel R.P. Excess heme in sickle erythrocyte inside-out membranes: possible role in thiol oxidation. Blood 71 (1988) 876-882
29. Zieger M.A., Tredget E.E., and McGann L.E. A simple, effective system for assessing viability in split-thickness skin with the use of oxygen consumption. J. Burn Care Rehabil. 14 (1993) 310-318
30. Goessling L.S., Mascotti D.P., Bhattacharyya-Pakrasi M., Gang H., and Thach R.E. Irreversible steps in the ferritin synthesis induction pathway. J. Biol. Chem. 269 (1994) 4343-4348
31. Haile D.J., Rouault T.A., Harford J.B., Kennedy M.C., Blondin G.A., Beinert H., and Klausner R.D. Cellular regulation of the iron-responsive element binding protein: disassembly of the cubane iron-sulfur cluster results in high-affinity RNA binding. Proc. Natl. Acad. Sci. USA 89 (1992) 11735-11739
32. Eisenstein R.S., Tuazon P.T., Schalinske K.L., Anderson S.A., and Traugh J.A. Iron-responsive element-binding protein: phosphorylation by protein kinase C. J. Biol. Chem. 268 (1993) 27363-27370
33. Huang H., and Salahudeen A.K. Cold induces catalytic iron release of cytochrome P-450 origin: a critical step in cold storage-induced renal injury. Am. J. Transplant. 2 (2002) 631-639
34. Arthur P.G., Niu X., Rigby P., Steer J.H., and Jeffrey G.P. Oxidative stress causes a decline in lysosomal integrity during hypothermic incubation of rat hepatocytes. Free Radic. Biol. Med. 44 (2008) 24-33
35. Balla G., Jacob H.S., Balla J., Rosenberg M., Nath K., Apple F., Eaton J.W., and Vercellotti G.M. Ferritin: a cytoprotective antioxidant stratagem of endothelium. J. Biol. Chem. 267 (1992) 18148-18153
36. Khaliulin I., Clarke S.J., Lin H., Parker J., Suleiman M.S., and Halestrap A.P. Temperature preconditioning of isolated rat hearts-a potent cardioprotective mechanism involving a reduction in oxidative stress and inhibition of the mitochondrial permeability transition pore. J. Physiol. (London) 581 (2007) 1147-1161
37. Ning X.-H., Chi E.Y., Buroker N.E., Chen S.-H., Xu C.S., Tien Y.-T., Hyyti O.M., Ge M., and Portman M.A. Moderate hypothermia (30 degrees C) maintains myocardial integrity and modifies response of cell survival proteins after reperfusion. Am. J. Physiol. Heart Circ. Physiol. 293 (2007) H2119-2128
38. Yunoki M., Nishio S., Ukita N., Anzivino M.J., and Lee K.S. Hypothermic preconditioning induces rapid tolerance to focal ischemic injury in the rat. Exp. Neurol. 181 (2003) 291-300
39. Yunoki M., Nishio S., Ukita N., Anzivino M.J., and Lee K.S. Characteristics of hypothermic preconditioning influencing the induction of delayed ischemic tolerance. J. Neurosurg. 97 (2002) 650-657
40. Sun S., and Chasteen N.D. Ferroxidase kinetics of horse spleen apoferritin. J. Biol. Chem. 267 (1992) 25160-25166
41. Mignogna G., Chiaraluce R., Consalvi V., Cavallo S., Stefanini S., and Chiancone E. Ferritin from the spleen of the Antarctic teleost Trematomus bernacchii is an M-type homopolymer. Eur. J. Biochem. 269 (2002) 1600-1606
42. Yamashita M., Ojima N., and Sakamoto T. Molecular cloning and cold-inducible gene expression of ferritin H subunit isoforms in rainbow trout cells. J. Biol. Chem. 271 (1996) 26908-26913
43. Vairetti M., Ferrigno A., Bertone R., Richelmi P., Berte F., and Freitas I. Apoptosis vs. necrosis: glutathione-mediated cell death during rewarming of rat hepatocytes. Biochim. Biophys. Acta 1740 (2005) 367-374
44. Stefanutti G., Pierro A., Vinardi S., Spitz L., and Eaton S. Moderate hypothermia protects against systemic oxidative stress in a rat model of intestinal ischemia and reperfusion injury. Shock 24 (2005) 159-164
45. Slikker III W., Desai V.G., Duhart H., Feuers R., and Imam S.Z. Hypothermia enhances bcl-2 expression and protects against oxidative stress-induced cell death in Chinese hamster ovary cells. Free Radic. Biol. Med. 31 (2001) 405-411
46. Khar A., Pardhasaradhi B.V.V., Ali A.M., and Kumari A.L. Protection conferred by Bcl-2 expression involves reduced oxidative stress and increased glutathione production during hypothermia-induced apoptosis in AK-5 tumor cells. Free Radic. Biol. Med. 35 (2003) 949-957
47. Xu L., Koumenis I.L., Tilly J.L., and Giffard R.G. Overexpression of bcl-xL protects astrocytes from glucose deprivation and is associated with higher glutathione, ferritin, and iron levels. Anesthesiology 91 (1999) 1036-1046
48. Fujita J. Cold shock response in mammalian cells. J. Mol. Microbiol. Biotechnol. 1 (1999) 243-255
49. Sonna L.A., Fujita J., Gaffin S.L., and Lilly C.M. Effects of heat and cold stress on mammalian gene expression. J. Appl. Physiol. 92 (2002) 1725-1742
50. Fuller B.J. Gene expression in response to low temperatures in mammalian cells: a review of current ideas. Cryo Lett. 24 (2003) 95-102
51. Al-Fageeh M.B., and Smales C.M. Control and regulation of the cellular responses to cold shock: the responses in yeast and mammalian systems. Biochem. J. 397 (2006) 247-259
52. Glofcheski D.J., Borrelli M.J., Stafford D.M., and Kruuv J. Induction of tolerance to hypothermia and hyperthermia by a common mechanism in mammalian cells. J. Cell Physiol. 156 (1993) 104-111
53. Otterbein L.E., and Choi A.M. Heme oxygenase: colors of defense against cellular stress. Am. J. Physiol. Lung Cell Mol. Physiol. 279 (2000) L1029-1037
54. Balogun E., Foresti R., Green C.J., and Motterlini R. Changes in temperature modulate heme oxygenase-1 induction by curcumin in renal epithelial cells. Biochem. Biophys. Res. Commun. 308 (2003) 950-955
55. Steinlechner-Maran R., Eberl T., Kunc M., Schrocksnadel H., Margreiter R., and Gnaiger E. Respiratory defect as an early event in preservation-reoxygenation injury of endothelial cells. Transplantation 63 (1997) 136-142
56. Fuckert O., Rauen U., and De Groot H. A role for sodium in hypoxic but not in hypothermic injury to hepatocytes and LLC-PK1 cells. Transplantation 70 (2000) 723-730