Control of stress-induced apoptosis by freezing tolerance-associated wheat proteins during cryopreservation of rat hepatocytes

Cell Stress and Chaperones - Tập 25 - Trang 869-886 - 2020
Mélanie Chow-shi-yée1, Melanie Grondin1, Francois Ouellet1, Diana A. Averill-Bates1
1Département des Sciences Biologiques, Université du Québec à Montréal, Montréal, Canada

Tóm tắt

Cryopreservation is used for long-term storage of cells and tissues. Cryoprotectants such as dimethyl disulfoxide (DMSO) are used to protect cells against freeze-thaw damage. Despite the use of cryoprotectants, hepatocytes are sensitive to stresses imposed by freeze and thaw processes, which cause physical damage, loss of functionality, or cell death. As an alternative, we have developed new technology using several recombinant wheat proteins as cryoprotectants: TaENO (enolase), TaBAS1 (2-Cys peroxiredoxin), and a combination of WCS120 (dehydrin) with TaIRI-2 (inhibitor of ice recrystallization). This study aims to understand the mechanisms by which these plant proteins protect rat hepatocytes against cell death incurred during cryopreservation. Our analysis revealed that for cells cryopreserved with DMSO, cell death occurred by apoptosis and necrosis. Apoptosis was detected by activation of effector caspases-3 and -7, PARP cleavage, and nuclear chromatin condensation. These apoptotic events were inhibited when hepatocytes were cryopreserved with the different plant proteins. Cryopreservation with DMSO activated apoptosis through the mitochondrial pathway: the Bax/Bcl-2 protein ratio increased, mitochondrial membrane potential decreased, and initiator caspase-9 was activated. Furthermore, the endoplasmic reticulum pathway of apoptosis was activated: levels of the chaperone Bip/GRP78 decreased, pro-apoptotic transcription factor CHOP was induced, and initiator caspase-12 was activated. Activation of the mitochondrial and endoplasmic reticulum pathways of apoptosis was attenuated when hepatocytes were cryopreserved with the different recombinant proteins. This study improves understanding of mechanisms of cryoprotection provided by these plant proteins during freezing stress. These proteins are natural products and show promising potential by decreasing cell death during cryopreservation of hepatocytes.

Tài liệu tham khảo

Arias IM, Wolkoff AW, Boyer JL, Shafritz DA, Fausto N, Alter HJ, Cohen DE (eds) (2009) The liver: biology and pathobiology. 5th edition. John Wiley & Sons, Ltd, New York. doi:https://doi.org/10.1002/9780470747919 Baust JM, Buskirk V, Baust JG (2000) Cell viability improves following inhibition of cryopreservation-induced apoptosis. In Vitro Cell Dev Biol Anim 36:262–270 Baust JM, Van Buskirk RG, Baust JG (2002) Gene activation of the apoptotic caspase cascade following cryogenic storage. Cell Preserv Tech 1:63–80. https://doi.org/10.1089/15383440260073301 Baust JG, Gao D, Baust JM (2009) Cryopreservation: an emerging paradigm change. Organogenesis 5:90–96. https://doi.org/10.4161/org.5.3.10021 Bendall LJ, Green DR (2014) Autopsy of a cell. Leukemia. 28:1341–1343. https://doi.org/10.1038/leu.2014.17 Best BP (2015) Cryoprotectant toxicity: facts, issues, and questions. Rejuvenation Res 18:422–436. https://doi.org/10.1089/rej.2014.1656 Bhardwaj PK, Mala D, Kumar S (2014) 2-Cys peroxiredoxin responds to low temperature and other cues in Caragana jubata, a plant species of cold desert of Himalaya. Mol Biol Rep 41:2951–2961. https://doi.org/10.1007/s11033-014-3151-4 Bissoyi A, Nayak B, Pramanik K, Sarangi SK (2014) Targeting cryopreservation-induced cell death: a review. Biopreserv Biobank 12:23–34. https://doi.org/10.1089/bio.2013.0032 Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254. https://doi.org/10.1006/abio.1976.9999 Cardoso LMDF, Moreira LFP, Pinto MA, Henriques-Pons A, Alves LA (2018) Domino hepatocyte transplantation: a therapeutic alternative for the treatment of acute liver failure. Can J Gastroenterol Hepatol 2018:2593745–2593749. https://doi.org/10.1155/2018/2593745 Cho C-W, Chung E, Heo J-E, So H-A, Choi H-K, Kim DH, Chung YS, Chae HZ, Lee J-H (2012) Molecular characterization of a 2-Cys peroxiredoxin induced by abiotic stress in mungbean. Plant Cell Tissue Organ Cult 108:473–484. https://doi.org/10.1007/s11240-011-0061-1 Choi YJ, Morel L, Le François T, Bourque D, Bourget L, Groleau D, Massie B, Míguez CB (2010) Novel, versatile, and tightly regulated expression system for Escherichia coli strains. Appl Environ Microbiol 76:5058–5066. https://doi.org/10.1128/AEM.00413-10 Chow-shi-yée M, Grondin M, Averill-Bates DA, Ouellet F (2016) Plant protein 2-Cys peroxiredoxin TaBAS1 alleviates oxidative and nitrosative stresses incurred during cryopreservation of mammalian cells. Biotechnol Bioeng 113:1511–1521. https://doi.org/10.1002/bit.25921 Crowley LC, Marfell BJ, Scott AP, Waterhouse NJ (2016) Quantitation of apoptosis and necrosis by annexin V binding, propidium iodide uptake, and flow cytometry. Cold Spring Harb Protoc 2016(11):pdb.prot087288. https://doi.org/10.1101/pdb.prot087288 Czabotar PE, Lessene G, Strasser A, Adams JM (2014) Control of apoptosis by the BCL-2 protein family: implications for physiology and therapy. Nat Rev Mol Cell Biol 15:49–63. https://doi.org/10.1038/nrm3722 Dludla PV, Jack B, Viraragavan A, Pheiffer C, Johnson R, Louw J, Muller CJF (2018) A dose-dependent effect of dimethyl sulfoxide on lipid content, cell viability and oxidative stress in 3T3-L1 adipocytes. Toxicol Rep 5:1014–1020. https://doi.org/10.1016/j.toxrep.2018.10.002 Elliott GD, Wang S, Fuller BJ (2017) Cryoprotectants: a review of the actions and applications of cryoprotective solutes that modulate cell recovery from ultra-low temperatures. Cryobiology 76:74–91. https://doi.org/10.1016/j.cryobiol.2017.04.004 Fu T, Guo D, Huang X, O'gorman MR, Huang L, Crawford SE, Soriano HE (2001) Apoptosis occurs in isolated and banked primary mouse hepatocytes. Cell Transplant 10:59–66. https://doi.org/10.3727/000000001783987043 Fujita R, Hui T, Chelly M, Demetriou AA (2005) The effect of antioxidants and a caspase inhibitor on cryopreserved rat hepatocytes. Cell Transplant 14:391–396. https://doi.org/10.3727/000000005783982981 Fulda S, Gorman AM, Hori O, Samali A (2010) Cellular stress responses: cell survival and cell death. Int J Cell Biol 2010:214074–214023. https://doi.org/10.1155/2010/214074 Gómez-Lechón MJ, Castell JV, Donato MT (2010) The use of hepatocytes to investigate drug toxicity. Methods Mol Biol 640:389–415. https://doi.org/10.1007/978-1-60761-688-7_21 Grondin M, Marion M, Denizeau F, Averill-Bates DA (2007) Tributyltin induces apoptotic signaling in hepatocytes through pathways involving the endoplasmic reticulum and mitochondria. Toxicol Appl Pharmacol 222:57–68. https://doi.org/10.1016/j.taap.2007.03.028 Grondin M, Hamel F, Averill-Bates DA, Sarhan F (2009a) Wheat proteins enhance stability and function of adhesion molecules in cryopreserved hepatocytes. Cell Transplant 18:79–88. https://doi.org/10.3727/096368909788237104 Grondin M, Hamel F, Averill-Bates DA, Sarhan F (2009b) Wheat proteins improve cryopreservation of rat hepatocytes. Biotechnol Bioeng 103:582–591. https://doi.org/10.1002/bit.22270 Grondin M, Chow-Shi-Yée M, Ouellet F, Averill-Bates DA (2015) Wheat enolase demonstrates potential as a non-toxic cryopreservation agent for liver and pancreatic cells. Biotechnol J 10:801–810. https://doi.org/10.1002/biot.201400562 Guguen-Guillouzo C, Guillouzo A (2010) General review on in vitro hepatocyte models and their applications. Methods Mol Biol 640:1–40. https://doi.org/10.1007/978-1-60761-688-7_1 Haidara K, Marion M, Gascon-Barré M, Denizeau F, Averill-Bates DA (2008) Implication of caspases and subcellular compartments in tert-butylhydroperoxide induced apoptosis. Toxicol Appl Pharmacol 229:65–76. https://doi.org/10.1016/j.taap.2008.01.010 Hamel F, Grondin M, Denizeau F, Averill-Bates DA, Sarhan F (2006) Wheat extracts as an efficient cryoprotective agent for primary cultures of rat hepatocytes. Biotechnol Bioeng 95:661–670 Hanslick JL, Lau K, Noguchi KK, Olney JW, Zorumski CF, Mennerick S, Farber N (2009) Dimethyl sulfoxide (DMSO) produces widespread apoptosis in the developing central nervous system. Neurobiol Dis 34:1–10. https://doi.org/10.1016/j.nbd.2008.11.006 Häussinger D, Lamers WH, Moorman A (1992) Hepatocyte heterogeneity in the metabolism of amino acids and ammonia. Enzyme 46:72–93 Heath-Engel HM, Chang NC, Shore GC (2008) The endoplasmic reticulum in apoptosis and autophagy: role of the BCL-2 protein family. Oncogene 27:6419–6433. https://doi.org/10.1038/onc.2008.309 Heng BC, Liu H, Toh WS, Rufaihah AJ, Yang Z, Bay BH, Ge Z, Quang HW, Lee EH, Cao T (2005) Loss of viability during freeze-thaw of intact and adherent human embryonic stem cells with conventional slow-cooling protocols is predominantly due to apoptosis rather than cellular necrosis. J Biomed Sci 13:433–445. https://doi.org/10.1007/s11373-005-9051-9 Houde M, Daniel C, Lachapelle M, Allard F, Laliberté S, Sarhan F (1995) Immunolocalization of freezing-tolerance-associated proteins in the cytoplasm and nucleoplasm of wheat crown tissues. Plant J 8:583–593. https://doi.org/10.1046/j.1365-313x.1995.8040583.x Hughes RD, Mitry RR, Dhawan A (2012) Current status of hepatocyte transplantation. Transplantation 93:342–347. https://doi.org/10.1097/TP.0b013e31823b72d6 Review Jitraruch S, Dhawan A, Hughes RD, Filippi C, Lehec SC, Glover L, Mitry RR (2017) Cryopreservation of hepatocyte microbeads for clinical transplantation. Cell Transplant 8:1341–1354. https://doi.org/10.1177/0963689717720050 Joza N, Pospisilik JA, Hangen E, Hanada T, Modjtahedi N, Penninger JM, Kroemer G (2009) AIF: not just an apoptosis-inducing factor. Ann N Y Acad Sci 1171:2–11. https://doi.org/10.1111/j.1749-6632.2009.04681.xReview Kaufmann T, Strasser A, Jost PJ (2012) Fas death receptor signalling: roles of Bid and XIAP. Cell Death Differ 19:42–50. https://doi.org/10.1038/cdd.2011.121 Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–885. https://doi.org/10.1038/227680a0 Lee H, Guo Y, Ohta M, Xiong L, Stevenson B, Zhu JK (2002) LOS2, a genetic locus required for cold-responsive gene transcription encodes a bi-functional enolase. EMBO J 21:2692–2702. https://doi.org/10.1093/emboj/21.11.2692 Leibowitz B, Yu J (2010) Mitochondrial signaling in cell death via the Bcl-2 family. Cancer Biol Ther 9:417–422. https://doi.org/10.4161/cbt.9.6.11392 Li AP (2014) In vitro human hepatocyte-based experimental systems for the evaluation of human drug metabolism, drug-drug interactions, and drug toxicity in drug development. Curr Top Med Chem 14:1325–1338. Review. https://doi.org/10.2174/1568026614666140506114411 Li Y, Guo Y, Tang J, Jiang J, Chen Z (2014) New insights into the roles of CHOP-induced apoptosis in ER stress. Acta Biochim Biophys Sin 46:629–640. https://doi.org/10.1093/abbs/gmu128 Lord CJ, Ashworth A (2017) PARP inhibitors: synthetic lethality in the clinic. Science 355:1152–1158. https://doi.org/10.1126/science.aam7344 Matsushita T, Yagi T, Hardin JA, Cragun JD, Crow FW, Bergen HR, Gores GJ, Nyberg SL (2003) Apoptotic cell death and function of cryopreserved porcine hepatocytes in a bioartificial liver. Cell Transplant 12:109–121. https://doi.org/10.3727/000000003108746696 Mazur P (1984) Freezing of living cells: mechanisms and implications. Am J Phys 247:C125–C142. https://doi.org/10.1152/ajpcell.1984.247.3.C125 McCullough KD, Martindale JL, Klotz L-O, Aw T-Y, Holbrook NJ (2001) Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol Cell Biol 21:1249–1259. https://doi.org/10.1128/MCB.21.4.1249-1259.2001 Notman R, Noro M, O’Malley B, Anwar J (2006) Molecular basis for dimethylsulfoxide (DMSO) action on lipid membranes. J Am Chem Soc 128:13982–13983. https://doi.org/10.1021/ja063363t Oakes SA, Scorrano L, Opferman JT, Bassik M, Nishino MC, Pozzan T, Korsmeyer SJ (2005) Proapoptotic BAX and BAK regulate the type 1 inositol trisphosphate receptor and calcium leak from the endoplasmic reticulum. Proc Natl Acad Sci U S A 102:105–110. https://doi.org/10.1073/pnas.0408352102 Orrenius S, Gogvadze V, Zhivotovsky B (2015) Calcium and mitochondria in the regulation of cell death. Biochem Biophys Res Commun 460:72–81. https://doi.org/10.1016/j.bbrc.2015.01.137 Review Ott M, Gogvadze V, Orrenius S, Zhivotovsky B (2007) Mitochondria, oxidative stress and cell death. Apoptosis 12:913–922. https://doi.org/10.1007/s10495-007-0756-2 Review Pallepati P, Averill-Bates DA (2010) Mild thermotolerance induced at 40 degrees C increases antioxidants and protects HeLa cells against mitochondrial apoptosis induced by hydrogen peroxide: role of p53. Arch Biochem Biophys 495:97–111. https://doi.org/10.1016/j.abb.2009.12.014 Pallepati P, Averill-Bates DA (2011) Activation of ER stress and apoptosis by hydrogen peroxide in HeLa cells: protective role of mild heat preconditioning at 40°C. Biochim Biophys Acta 1813:1987–1999. https://doi.org/10.1016/j.bbamcr.2011.07.021 Pegg DE (2015) Principles of cryopreservation. Methods Mol Biol 1257:3–19. https://doi.org/10.1007/978-1-4939-2193-5_1 Perelman A, Wachtel C, Cohen M, Haupt S, Shapiro H, Tzur A (2012) JC-1: alternative excitation wavelengths facilitate mitochondrial membrane potential cytometry. Cell Death Dis 3:e430. https://doi.org/10.1038/cddis.2012.171 Pincus D, Chevalier MW, Aragón T, van Anken E, Vidal SE, El-Samad H, Walter P (2010) BiP binding to the ER-stress sensor Ire1 tunes the homeostatic behavior of the unfolded protein response. PLoS Biol 8(7):e1000415. https://doi.org/10.1371/journal.pbio.1000415 Qi W, Ding D, Salvi RJ (2008) Cytotoxic effects of dimethyl sulphoxide (DMSO) on cochlear organotypic cultures. Hear Res 236:52–60. https://doi.org/10.1016/j.heares.2007.12.002 Redza-Dutordoir M, Averill-Bates DA (2016) Activation of apoptosis signalling pathways by reactive oxygen species. Biochim Biophys Acta 1863:2977–2992. https://doi.org/10.1016/j.bbamcr.2016.09.012 Rozpedek W, Pytel D, Mucha B, Leszczynska H, Diehl JA, Majsterek I (2016) The role of the PERK/eIF2α/ATF4/CHOP signaling pathway in tumor progression during endoplasmic reticulum stress. Curr Mol Med 16:533–544. https://doi.org/10.2174/1566524016666160523143937 Sano R, Reed JC (2013) ER stress-induced cell death mechanisms. Biochim Biophys Acta 1833:3460–3470. https://doi.org/10.1016/j.bbamcr.2013.06.028 Sauvat A, Wang Y, Segura F, Spaggiari S, Müller K, Zhou H, Galluzzi L, Kepp O, Kroemer G (2015) Quantification of cellular viability by automated microscopy and flow cytometry. Oncotarget 6:9467–9475. https://doi.org/10.18632/oncotarget.3266 Shalini S, Dorstyn L, Dawar S, Kumar S (2015) Old, new and emerging functions of caspases. Cell Death Differ 22:526–539. https://doi.org/10.1038/cdd.2014.216 Shore GC, Papa FR, Oakes SA (2011) Signaling cell death from the endoplasmic reticulum stress response. Curr Opin Cell Biol 23:143–149. https://doi.org/10.1016/j.ceb.2010.11.003 Soldani C, Scovassi AI (2002) Poly (ADP-ribose) polymerase-1 cleavage during apoptosis: an update. Apoptosis 7:321-328 Review Stéphenne X, Najimi M, Ngoc DK, Smets F, Hue L, Guigas B, Sokal EM (2007) Cryopreservation of human hepatocytes alters the mitochondrial respiratory chain complex 1. Cell Transplant 16:409–419. https://doi.org/10.3727/000000007783464821 Tan Y, Dourdin N, Wu C, De Veyra T, Elce JS, Greer PA (2006) Ubiquitous calpains promote caspase-12 and JNK activation during endoplasmic reticulum stress induced apoptosis. J Biol Chem 281:16016–16024. https://doi.org/10.1074/jbc.M601299200 Tchir J, Acker JP (2010) Mitochondria and membrane cryoinjury in micropatterned cells: effects of cell-cell interactions. Cryobiology 61:100–107. https://doi.org/10.1016/j.cryobiol.2010.05.007 Terry C, Hughes RD, Mitry RR, Lehec SC, Dhawan A (2007) Cryopreservation-induced nonattachment of human hepatocytes: role of adhesion molecules. Cell Transplant 16:639–647. https://doi.org/10.3727/000000007783465000 Tremblay K, Ouellet F, Fournier J, Sarhan F (2005) Molecular characterization and origin of novel bipartite cold-regulated ice recrystallization inhibition proteins from cereals. Plant Cell Physiol 46:884–891. https://doi.org/10.1093/pcp/pci093 Wang M, Kaufman RJ (2016) Protein misfolding in the endoplasmic reticulum as a conduit to human disease. Nature 529:326–335. https://doi.org/10.1038/nature17041 Wyllie AH (2010) “Where, O death, is thy sting?” a brief review of apoptosis biology. Mol Neurobiol 42:4–9. https://doi.org/10.1007/s12035-010-8125-5 Xu X, Cowley S, Flaim CJ, James W, Seymour L, Cui Z (2010) The roles of apoptotic pathways in the low recovery rate after cryopreservation of dissociated human embryonic stem cells. Biotechnol Prog 26:827–837. https://doi.org/10.1002/btpr.368 Yagi T, Hardin JA, Valenzuela YM, Miyoshi H, Gores GJ, Nyberg SL (2001) Caspase inhibition reduces apoptotic death of cryopreserved porcine hepatocytes. Hepatology 33:1432–1440. https://doi.org/10.1053/jhep.2001.24560 Yuan C, Gao J, Guo J, Bai L, Marshall C, Cai WL, Xiao M (2014) Dimethyl sulfoxide damages mitochondrial integrity and membrane potential in cultured astrocytes. PLoS One 9(9):e107447. https://doi.org/10.1371/journal.pone.0107447