Hypothermic preservation of rat hearts using antifreeze glycoprotein

. 2020 Dec 22 ; 69 (6) : 1029-1038. [epub] 20201125

Jazyk angličtina Země Česko Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid33251809

Antifreeze proteins are an effective additive for low-temperature preservation of solid organs. Here, we compared static hypothermic preservation with and without antifreeze glycoprotein (AFGP), followed by nonfreezing cryopreservation of rat hearts. The heart was surgically extracted and immersed in one of the cardioplegia solutions after cardiac arrest. Control rat hearts (n=6) were immersed in University of Wisconsin (UW) solution whereas AFGP-treated hearts (AFGP group) (n=6) were immersed in UW solution containing 500 ?g/ml AFGP. After static hypothermic preservation, a Langendorff apparatus was used to reperfuse the coronary arteries with oxygenated Krebs-Henseleit solution. After 30, 60, 90, and 120 min, the heart rate (HR), coronary flow (CF), cardiac contractile force (max dP/dt), and cardiac diastolic force (min dP/dt) were measured. Tissue water content (TWC) and tissue adenosine triphosphate (ATP) levels in the reperfused preserved hearts were also assessed. All the parameters were compared between the control and AFGP groups. Compared with the control group, the AFGP group had significantly (p<0.05) higher values of the following parameters: HR at 60, 90, and 120 min; CF at all four time points; max dP/dt at 90 min; min dP/dt at 90 and 120 min; and tissue ATP levels at 120 min. TWC did not differ significantly between the groups. The higher HR, CF, max dP/dt, min dP/dt, and tissue ATP levels in the AFGP compared with those in control hearts suggested that AFGP conferred superior hemodynamic and metabolic functions. Thus, AFGP might be a useful additive for the static/nonfreezing hypothermic preservation of hearts.

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AMIR G, HOROWITZ L, RUBINSKY B, YOUSIF BS, LAVEE J, SMOLINSKY AK. Subzero nonfreezing cryopresevation of rat hearts using antifreeze protein I and antifreeze protein III. Cryobiology. 2004;48:273–282. doi: 10.1016/j.cryobiol.2004.02.009. PubMed DOI

AMIR G, RUBINSKY B, BASHEER SY, HOROWITZ L, JONATHAN L, FEINBERG MS, SMOLINSKY AK, LAVEE J. Improved viability and reduced apoptosis in sub-zero 21-hour preservation of transplanted rat hearts using anti-freeze proteins. J Heart and Lung Transplant. 2005;24:1915–1929. doi: 10.1016/j.healun.2004.11.003. PubMed DOI

BELZER FO, SOUTHARD JH. Principles of solid-organ preservation by cold storage. Transplantation. 1988;45:673–676. doi: 10.1097/00007890-198804000-00001. PubMed DOI

BURCHAM TS, OSUGA DT, RAO BN, BUSH CA, FEENEY RE. Purification and primary sequences of the major arginine-containing antifreeze glycopeptides from the fish eeginus gracilis. J Biol Chem. 1986;261:6384–6389. PubMed

DEVRIES AL, WOHLSCHLAG DE. Freezing resistance in some Antarctic fishes. Science. 1969;163:1073–1075. doi: 10.1126/science.163.3871.1073. PubMed DOI

ETO TK, RUBINSKY B. Antifreeze glycoproteins increase solution viscosity. Biochem Biophys Res Commun. 1993;197:927–931. doi: 10.1006/bbrc.1993.2568. PubMed DOI

GEORGE TJ, ARNAOUTAKIS GJ, BAUMGARTNER WA, SHAH AS, CONTE JV. Organ storage with University of Wisconsin solution is associated with improved outcomes after orthotopic heart transplantation. J Heart Lung Transplant. 2011;30:1033–1043. doi: 10.1016/j.healun.2011.05.005. PubMed DOI

HARDING MM, ANDERBERG PI, HAYMET AD. ‘Antifreeze’ glycoproteins from polar fish. Eur J Biochem. 2003;270:1381–1392. doi: 10.1046/j.1432-1033.2003.03488.x. PubMed DOI

HIRANO Y, NISHIMIYA Y, MATSUMOTO S, MATSUSHITA M, TODO S, MIURA A, KOMATSU Y, TSUDA S. Hypothermic preservation effect on mammalian cells of type III antifreeze proteins from notched-fin eelpout. Cryobiology. 2008;57:46–51. doi: 10.1016/j.cryobiol.2008.05.006. PubMed DOI

HUELSZ-PRINCE G, DEVRIES AL, BAKKER HJ, Van ZON JS, MEISTER K. Effect of antifreeze glycoproteins on organoid survival during and after hypothermic storage. Biomolecules. 2019;9:E110. doi: 10.3390/biom9030110. PubMed DOI PMC

JAHANIA MS, SANCHEZ JA, NARAYAN P, LASLEY RD, MENTZER RM., JR Heart preservation for transplantation: principles and strategies. Ann Thorac Surg. 1999;68:1983–1987. PubMed

KATO H, TOMITA S, YAMAGUCHI S, OHTAKE H, WATANABE G. Subzero 24-hr nonfreezing rat heart preservation: a novel preservation method in a variable magnetic field. Transplantation. 2012;94:473–477. doi: 10.1097/TP.0b013e3182637054. PubMed DOI

KAMIJIMA T, SAKASHITA M, MIURA A, NISHIMIYA Y, TSUDA S. Antifreeze protein prolongs the life-time of insulinoma cells during hypothermic preservation. PLoS One. 2013;8:e73643. doi: 10.1371/journal.pone.0073643. PubMed DOI PMC

KANDA Y. Investigation of the freely available easy-to-use software ‘EZR’ for medical statistics. Bone Marrow Transplant. 2013;48:452–458. doi: 10.1038/bmt.2012.244. PubMed DOI PMC

MANKAD P, SLAVIK Z, YACOUB M. Endothelial dysfunction caused by University of Wisconsin preservation solution in the rat heart. The importance of temperature. J Thorac Cardiovasc Surg. 1992;104:1618–1624. doi: 10.1016/S0022-5223(19)33892-9. PubMed DOI

MATSUMOTO S, MATSUSITA M, MORITA T, KAMACHI H, TSUKIYAMA S, FURUKAWA Y, KOSHIDA S, TACHIBANA Y, NISHIMURA S, TODO S. Effects of synthetic antifreeze glycoprotein analogue on islet cell survival and function during cryopreservation. Cryobiology. 2006;52:90–98. doi: 10.1016/j.cryobiol.2005.10.010. PubMed DOI

MICHEL SG, LA MURAGLIA GM, 2ND, MADARIAGA ML, TITUS JS, SELIG MK, FARKASH EA, ALLAN JS, ANDERSON LM, MADSEN JC. Twelve-hour hypothermic machine perfusion for donor heart preservation leads to improved ultrastructural characteristics compared to conventional cold storage. Ann Transplant. 2015;20:461–468. doi: 10.12659/AOT.893784. PubMed DOI

MUGNANO JA, WANG T, LAYNE JR, JR, DEVRIES AL, LEE RE., JR Antifreeze glycoproteins promote intracellular freezing of rat cardiomyocytes at high subzero temperatures. Am J Physiol. 1995;269:474–479. doi: 10.1152/ajpregu.1995.269.2.R474. PubMed DOI

NISHIMIYA Y, MIE Y, HIRANO Y, KONDO H, MIMURA A, TSUDA S. Mass preparation and technological development of an antifreeze protein. Synthesiology. 2008;1:7–14. doi: 10.5571/syntheng.1.7. DOI

PERNOT AC, INGWALL JS, MENASCHE P, GROUSSET C, BERCOT M, PIWNICA A, FOSSEL ET. Evaluation of high energy phosphate metabolism during cardioplegic arrest and reperfusion: a phosphorus-31 nuclear magnetic resonance study. Circulation. 1983;67:1296–1303. doi: 10.1161/01.CIR.67.6.1296. PubMed DOI

PRATHALINGAM NS, HOLT WV, REVELL SG, MIRCZUK S, FLECK RA, WATSON PF. Impact of antifreeze proteins and antifreeze glycoproteins on bovine sperm during freeze-thaw. Theriogenology. 2006;66:1894–1900. doi: 10.1016/j.theriogenology.2006.04.041. PubMed DOI

PROKUDINA ES, NARYZHNAYA NV, MUKHOMEDZYANOV AV, GORBUNOV AS, ZHANG Y, JAGGI AS, TSIBULNIKOV SY, NESTEROV EA, LISHMANOV YB, SULEIMAN MS, OELTGEN PR, MASLOV LN. Effect of chronic continuous normobaric hypoxia on functional state of cardiac mitochondria and tolerance of isolated rat heart to ischemia and reperfusion: Role of μ and δ2 opioid receptors. Physiol Res. 2019;68:909–920. doi: 10.3938/NPSM.68.909. PubMed DOI

QADEER S, KHAN MA, ANSARI MS, RAKHA BA, EJAZ R, IQBAL R, YOUNIS M, ULLAH N, DEVRIES AL, AKHTER S. Efficiency of antifreeze glycoproteins for cryopreservation of Nili-Ravi (Bubalus bubalis) buffalo bull sperm. Anim Reprod Sci. 2015;157:56–62. doi: 10.1016/j.anireprosci.2015.03.015. PubMed DOI

RUBINSKY B. Principles of Low Temperature Cell Preservation. Heart Fail Rev. 2003;8:277–284. doi: 10.1023/A:1024734003814. PubMed DOI

RUBINSKY B, ARAV A, FLETCHER GL. Hypothermic protection - a fundamental property of "antifreeze" proteins. Biochem Biophys Res Commun. 1991;180:566–571. doi: 10.1016/S0006-291X(05)81102-7. PubMed DOI

RUBINSKY B, ARAV A, MATTIOLI M, DEVRIES AL. The effect of antifreeze glycopeptides on membrane potential changes at hypothermic temperatures. Biochem Biophys Res Commun. 1990;173:1369–1374. doi: 10.1016/S0006-291X(05)80939-8. PubMed DOI

RUBINSKY B, MATTIOLI M, ARAV A, BARBONI B, FLETCHER GL. Inhibition of Ca2+ and K+ currents by "antifreeze" proteins. Am J Physiol. 1992;262:542–545. doi: 10.1152/ajpregu.1992.262.3.R542. PubMed DOI

SAKAGUCHI H, KITAMURA S, KAWACHI K, KOBAYASHI S, YOSHIDA Y, NIWAYA K, GOJO S. Preservation of myocardial function and metabolism at subzero nonfreezing temperature storage of the heart. J Heart Lung Transplant. 1996;15:1101–1107. PubMed

SAKAGUCHI H, TANIGUCHI S, KOBAYASHI S, TSUJI T, ABE T, KITAMURA S. Subzero nonfreezing storage (−1 degree C) of the heart with University of Wisconsin solution and 2,3-butanediol. Transplant Proc. 1998;30:58–59. doi: 10.1016/S0041-1345(97)01178-0. PubMed DOI

SOLTYS KA, BATTA AK, KONERU B. Successful nonfreezing, subzero preservation of rat liver with 2,3-butanediol and type I antifreeze protein. J Surg Res. 2001;96:30–34. doi: 10.1006/jsre.2000.6053. PubMed DOI

STEHLIK J, EDWARDS LB, KUCHERYAVAYA AY, BENDEN C, CHRISTIE JD, DOBBELS F, KIRK R, RAHMEL AO, HERTZ MI. The Registry of the International Society for Heart and Lung Transplantation: twenty-eighth adult heart transplant report-2011. J Heart Lung Transplant. 2011;30:1078–1094. doi: 10.1016/j.healun.2011.08.003. PubMed DOI

STRINGHAM JC, SOUTHARD JH, HEGGE J, TRIEMSTRA L, FIELDS BL, BELZER FO. Limitations of heart preservation by cold storage. Transplantation. 1992;53:287–294. doi: 10.1097/00007890-199202010-00007. PubMed DOI

TOMCZAK MM, HINCHA DK, ESTRADA SD, WOLKERS WF, CROWE LM, FEENEY RE, TABLIN F, CROWE JH. A mechanism for stabilization of membranes at low temperatures by an antifreeze protein. Biophys J. 2002;82:874–881. doi: 10.1016/S0006-3495(02)75449-0. PubMed DOI PMC

WANG T, ZHU Q, YANG X, LAYNE JR, JR, DEVRIES AL. Antifreeze glycoproteins from antarctic notothenioid fishes fail to protect the rat cardiac explant during hypothermic and freezing preservation. Cryobiology. 1994;31:185–192. doi: 10.1006/cryo.1994.1022. PubMed DOI

YANG X, ZHU Q, LAYNE JR, JR, CLAYDON M, HICKS GL, JR, WANG T. Subzero nonfreezing storage of the mammalian cardiac explant. I. Methanol, ethanol, ethylene glycol, and propylene glycol as colligative cryoprotectants. Cryobiology. 1993;30:366–375. doi: 10.1006/cryo.1993.1036. PubMed DOI

ZHANG F, MO A, WEN Z, ZHOU Y, LIANG S, LIN H. Continuous perfusion of donor hearts with oxygenated blood cardioplegia improves graft function. Transpl Int. 2010;23:1164–1170. doi: 10.1111/j.1432-2277.2010.01112.x. PubMed DOI

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