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A brief review of applications of antifreeze proteins in cryopreservation and metabolic genetic engineering

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Abstract

Antifreeze proteins (AFPs) confer the ability to survive at subzero temperatures and are found in many different organisms, including fish, plants, and insects. They prevent the formation of ice crystals by non-colligative adsorption to the ice surface and are essential for the survival of organisms in cold environments. These proteins are also widely used for cryopreservation, food technology, and metabolic genetic engineering over a range of sources and recipient cell types. This review summarizes successful applications of AFPs in the cryopreservation of animals, insects, and plants, and discusses challenges encountered in cryopreservation. Applications in metabolic genetic engineering are also described, specifically with the overexpression of AFP genes derived from different organisms to provide freeze protection to sensitive crops seasonally exposed to subzero temperatures. This review will provide information about potential applications of AFPs in the cryopreservation of animals and plants as well as in plant metabolic genetic engineering in hopes of furthering the development of cold-tolerant organisms.

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References

  • Adler S, Pellizer C, Paparella M, Hartung T, Bremer S (2006) The effects of solvents on embryonic stem cell differentiation. Toxicol Vitro 20:265–271

    CAS  Google Scholar 

  • Amir G, Rubinsky B, Horovitz L, Yousif BS, Leor J, Smolinsky AK, Lavee J (2004) Improved viability and reduced apoptosis in sub-zero 21 h preservation of transplanted rat hearts using antifreeze proteins. J Heart Lung Transpl 23:171–172

    Google Scholar 

  • Amir G, Rubinsky B, Basheer SY, Horowitz L, Jonathan L, Feinberg MS, Smolinsky AM, Lavee J (2005) Improved viability and reduced apoptosis in sub-zero 21 h preservation of transplanted rat hearts using anti-freeze proteins. J Heart Lung Transpl 24:1915–1929

    Google Scholar 

  • Arav A, Rubinsky B, Fletcher G, Seren E (1993) Cryogenic protection of oocytes with antifreeze proteins. Mol Reprod Dev 36:488–493

    CAS  PubMed  Google Scholar 

  • Bagis H, Aktoprakligil D, Mercan HO, Yurdusev N, Turgut G, Sekmen S, Arat S, Cetin S (2006) Stable transmission and transcription of newfoundland ocean pout type III fish antifreeze protein (AFP) gene in transgenic mice and hypothermic storage of transgenic ovary and testis. Mol Reprod Dev 73:1404–1411

    CAS  PubMed  Google Scholar 

  • Bagis H, Akkoc T, Tass A, Aktoprakligil D (2008) Cryogenic effect of antifreeze protein on transgenic mouse ovaries and the production of live offspring by orthotopic transplantation of cryopreserved mouse ovaries. Mol Reprod Dev 75:608–613

    CAS  PubMed  Google Scholar 

  • Baguisi A, Arav A, Crosby TF, Roche JF, Boland MP (1997) Hypothermic storage of sheep embryos with antifreeze proteins: development in vitro and in vivo. Theriogenology 48:1017–1024

    CAS  PubMed  Google Scholar 

  • Balamurugan S, Ann JS, Varghese IP, Murugan SB, Harish MC, Kumar SR, Sathishkumar R (2018) Heterologous expression of Lolium perenne antifreeze protein confers chilling tolerance in tomato. J Integr Agric 17:1128–1136

    CAS  Google Scholar 

  • Carpenter JF, Hansen TN (1992) Antifreeze protein modulates cell survival during cryopreservation: mediation through influence on ice crystal growth. Proc Natl Acad Sci USA 89:8953–8957

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cheung RC, Ng TB, Wong JH (2017) Antifreeze proteins from diverse organisms and their applications: an overview. Curr Protein Pept Sci 18:262–283

    CAS  PubMed  Google Scholar 

  • Christner B (2010) Bioprospecting for microbial products that affect ice crystal formation and growth. Appl Microbiol Biotechnol 85:481–489

    CAS  PubMed  Google Scholar 

  • Cutler AJ, Saleem M, Kendall E, Gusta LV, Georges F, Fletcher GL (1989) Winter flounder antifreeze protein improves the cold hardiness of plant tissues. J Plant Physiol 135:351–354

    CAS  Google Scholar 

  • Deng LQ, Yu HQ, Liu YP, Jiao PP, Zhou SF, Zhang SZ, Li WC, Fu FL (2014) Heterologous expression of antifreeze protein gene AnAFP from Ammopiptanthus nanus enhances cold tolerance in Escherichia coli and tobacco. Gene 539:132–140

    CAS  PubMed  Google Scholar 

  • DeVries AL, Wohlschlag DE (1969) Freezing resistance in some Antarctic fishes. Science 163:1073–1075

    CAS  PubMed  Google Scholar 

  • Drori R, Celik Y, Davies PL, Braslavsky I (2014) Ice-binding proteins that accumulate on different ice crystal planes produce distinct thermal hysteresis dynamics. J R Soc Interface 11:20140526

    PubMed  PubMed Central  Google Scholar 

  • Duman JG (1979) Thermal-hysteresis-factors in overwintering insects. J Insect Physiol 25(10):805–810

    CAS  Google Scholar 

  • Duman JG (2002) The inhibition of ice nucleators by insect antifreeze proteins is enhanced by glycerol and citrate. J Comp Physiol 172:163–168

    CAS  Google Scholar 

  • Duman JG, Olsen TM (1993) Thermal hysteresis protein activity in bacteria, fungi, and phylogenetically diverse plants. Cryobiology 30:322–328

    Google Scholar 

  • Duman JG, Serianni AS (2002) The role of endogenous antifreeze protein enhancers in the hemolymph thermal hysteresis activity of the beetle Dendroides canadensis. J Insect Physiol 48:103–111

    CAS  PubMed  Google Scholar 

  • Duman JG, Bennett T, Sformo T, Hochstrasser R, Barnes BM (2004) Antifreeze proteins in Alaskan insects and spiders. J Insect Physiol 50:259–266

    CAS  PubMed  Google Scholar 

  • Engelmann F (2011) Cryopreservation of embryos: an overview. In: Thorpe TA, Yeung EC (eds) In plant embryo culture. Methods in molecular biology. Humana Press, New York, pp 155–184

    Google Scholar 

  • Fan Y, Liu B, Wang H, Wang S, Wang J (2002) Cloning of an antifreeze protein gene from carrot and its influence on cold tolerance in transgenic tobacco plants. Plant Cell Rep 21:296–301

    CAS  Google Scholar 

  • Gehrken U, Somme L (1987) Increased cold hardiness in eggs of Arcynopteryx compacta (Plecoptera) by dehydration. J Insect Physiol 33(12):987–991

    Google Scholar 

  • Gilbert JA, Davies PL, Laybourn-Parry J (2005) A hyperactive, Ca2 + -dependent antifreeze protein in an Antarctic bacterium. FEMS Microbiol Lett 245(1):67–72

    CAS  PubMed  Google Scholar 

  • Graham LA, Liou YC, Walker VK, Davies PL (1997) Hyperactive antifreeze protein from beetles. Nature 388:727–728

    CAS  PubMed  Google Scholar 

  • Griffith M, Ewart KV (1995) Antifreeze proteins and their potential use in frozen foods. Biotechnol Adv 13:375–402

    CAS  PubMed  Google Scholar 

  • Griffith M, Yaish MW (2004) Antifreeze proteins in overwintering plants: a tale of two activities. Trends Plant Sci 9:399–405

    CAS  PubMed  Google Scholar 

  • Griffith M, Ala P, Yang DS, Hon WC, Moffatt BA (1992) Antifreeze protein produced endogenously in winter rye leaves. Plant Physiol 100:593–596

    CAS  PubMed  PubMed Central  Google Scholar 

  • Griffith M, Antikainen M, Hon WC, Pihakaski-Maunsbach K, Yu XM, Chun JU, Yang DSC (1997) Antifreeze proteins in winter rye. Physiol Plantarum 100:327–332

    CAS  Google Scholar 

  • Gupta R, Deswal R (2014) Antifreeze proteins enable plants to survive in freezing conditions. J Biosci 39(5):931–944

    CAS  PubMed  Google Scholar 

  • Hansen TN, Smith KM, Brockbank KG (1993) Type I antifreeze protein attenuates cell recoveries following cryopreservation. Transpl Proc 25:3182–3184

    CAS  Google Scholar 

  • Hew CL, Kao MH, So Y-P, Lim K-P (1983) Presence of cysteine containing antifreeze proteins in the spruce bud worm, Choristoneura fumiferana. Can J Zool 61(10):2324–2328

    CAS  Google Scholar 

  • Hew CL, Davies PL, Fletcher G (1992) Antifreeze protein gene transfer in Atlantic salmon. Mol Mar Biol Biotechnol 1:309–317

    CAS  PubMed  Google Scholar 

  • Hew C, Poon R, Xiong F, Gauthier S, Shears M, King M, Davies P, Fletcher G (1999) Liver-specific and seasonal expression of transgenic Atlantic salmon harboring the winter flounder antifreeze protein gene. Transgenic Res 8:405–414

    CAS  PubMed  Google Scholar 

  • Hightower R, Baden C, Penzes E, Lund P, Dunsmuir P (1991) Expression of antifreeze proteins in transgenic plants. Plant Mol Biol 17:1013–1021

    CAS  PubMed  Google Scholar 

  • Hobbs RS, Fletcher GL (2008) Tissue specific expression of antifreeze protein and growth hormone transgenes driven by the ocean pout (Macrozoarces americanus) antifreeze protein OP5a gene promoter in Atlantic salmon (Salmo salar). Transgenic Res 17:33–45

    CAS  PubMed  Google Scholar 

  • Holmberg N, Farr´es J, Bailey JE, Kallio PT (2001) Targeted expression of a synthetic codon optimized gene, encoding the spruce budworm antifreeze protein, leads to accumulation of antifreeze activity in the apoplasts of transgenic tobacco. Gene 275:115–124

    CAS  PubMed  Google Scholar 

  • Hoshino T, Odaira M, Yoshida M, Tsuda S (1999) Physiological and biochemical significance of antifreeze substances in plants. J Plant Res 112:255–261

    CAS  Google Scholar 

  • Hoshino T, Kiriaki M, Ohgiya S, Fujiwara M, Kondo H, Nishimiya Y, Yumoto I, Tsuda S (2003) Antifreeze proteins from snow mold fungi. Can J Bot Rev Can Bot 81:1175–1181

    CAS  Google Scholar 

  • Huang T, Nicodemus J, Zarka DG, Thomashow MF, Wisniewski M, Duman JG (2002) Expression of an insect (Dendroides canadensis) antifreeze protein in Arabidopsis thaliana results in a decrease in plant freezing temperature. Plant Mol Biol 50:333–344

    CAS  PubMed  Google Scholar 

  • Husby JA, Zachariassen KE (1980) Antifreeze agents in the body fluid of winter active insects and spiders. Experientia 36(8):963–964

    CAS  Google Scholar 

  • Ideta A, Aoyagi Y, Tsuchiya K, Nakamura Y, Hayama K, Shirasawa A, Sakaguchi K, Tominaga N, Nishimiya Y, Tsuda S (2014) Prolonging hypothermic storage (4 °C) of bovine embryos with fish antifreeze protein. J Reprod Dev 61:1–6

    PubMed  PubMed Central  Google Scholar 

  • Jarzabek M, Pukacki PM, Nuk K (2009) Cold-regulated proteins with potent antifreeze and cryoprotective activities in spruces (Picea spp.). Cryobiology 58:268–274. https://doi.org/10.1016/j.cryobiol.2009.01.007

    Article  CAS  PubMed  Google Scholar 

  • Jeon SM, Naing AH, Park KI, Kim CK (2015) The effect of antifreeze protein on the cryopreservation of chrysanthemums. Plant Cell Tissue Organ Cult 123:665–671

    CAS  Google Scholar 

  • Jia Z, Davies PL (2002) Antifreeze proteins: an unusual receptor-ligand interaction. Trends Biochem Sci 27(2):101–106

    CAS  PubMed  Google Scholar 

  • Jo JW, Jee BC, Lee JR, Suh CS (2011) Effect of antifreeze protein supplementation in vitrification medium on mouse oocyte developmental competence. Fertil Steril 96:1239–1245

    CAS  PubMed  Google Scholar 

  • Kawahara H, Iwanaka Y, Higa S, Muryoi N, Sato M, Honda M, Omura H, Obata H (2007) A novel, intracellular antifreeze protein in an antarctic bacterium, Flavobacterium xanthum. Cryo Lett 28:39–49

    CAS  Google Scholar 

  • Kawahara H, Fujii A, Inoue M, Kitao S, Fukuoka J, Obata H (2009) Antifreeze activity of cold acclimated Japanese radish and purification of antifreeze peptide. Cryo Lett 30:119–131

    CAS  Google Scholar 

  • Kenward KD, Altschuler M, Hilderbrand D, Davies PL (1993) Accumulation of type I fish antifreeze protein in transgenic tobacco in cold specific. Plant Mol Biol 23:377–385

    CAS  PubMed  Google Scholar 

  • Kenward KD, Brandle J, McPherson J, Davies PL (1999) Type II fish antifreeze protein accumulation in transgenic tobacco does not confer frost resistance. Transgenic Res 8:105–117

    CAS  PubMed  Google Scholar 

  • Khanna HK, Daggard GE (2006) Targeted expression of redesigned and codon optimized synthetic gene leads to recrystallisation inhibition and reduced electrolyte leakage in spring wheat at sub-zero temperatures. Plant Cell Rep 25:1336–1346

    CAS  PubMed  Google Scholar 

  • Kim HJ, Shim HE, Lee JH, Kang Y-C, Hur YB (2015) Ice-binding protein derived from Glaciozyma can improve the viability of cryopreserved mammalian cells. J Microbiol Biotechnol 25:1989–1996

    CAS  PubMed  Google Scholar 

  • Kim HJ, Lee JH, Hur YB, Lee CW, Park SH, Koo BW (2017) Marine antifreeze proteins: structure, function, and application to cryopreservation as a potential cryoprotectant. Mar Drugs 15:27

    PubMed Central  Google Scholar 

  • Knight CA, DeVries AL, Oolman LD (1984) Fish antifreeze protein and the freezing and recrystallization of ice. Nature 308:295–296

    CAS  PubMed  Google Scholar 

  • Knight CA, Hallett J, DeVries AL (1988) Solute effects on ice recrystallization: an assessment technique. Cryobiology 25:55–60

    CAS  PubMed  Google Scholar 

  • Knight CA, Cheng CC, DeVries AL (1991) Adsorption of alpha-helical antifreeze peptides on specific ice crystal surface planes. Biophys J 59:409–418

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kong CH, Hamid N, Liu T, Sarojini V (2016) Effect of antifreeze peptide pretreatment on ice crystal size, drip loss, texture, and volatile compounds of frozen carrots. J Agric Food Chem 64:4327–4335

    CAS  PubMed  Google Scholar 

  • Koushafar H, Rubinsky B (1997) Effect of antifreeze proteins on frozen primary prostatic adenocarcinoma cells. Urology 49:421–425

    CAS  PubMed  Google Scholar 

  • Lee CY, Rubinsky B, Fletcher GL (1992) Hypothermic preservation of whole mammalian organs with antifreeze proteins. Cryo Lett 13:59–66

    CAS  Google Scholar 

  • Lee JK, Park KS, Park S, Park H, Song YH, Kang SH, Kim HJ (2010) An extracellular ice-binding glycoprotein from an Arctic psychrophilic yeast. Cryobiology 60:222–228

    CAS  PubMed  Google Scholar 

  • Lee HH, Lee HJ, Kim HJ, Lee JH, Ko Y, Kim SM, Lee JR, Suh CS, Kim SH (2015a) Effects of antifreeze proteins on the vitrification of mouse oocytes: comparison of three different antifreeze proteins. Hum Reprod 30:2110–2119

    CAS  PubMed  Google Scholar 

  • Lee J, Kim SK, Youm HW, Kim HJ, Lee JR, Suh CS, Kim SH (2015b) Effects of three different types of antifreeze proteins on mouse ovarian tissue cryopreservation and transplantation. PLoS One 10:e0126252

    PubMed  PubMed Central  Google Scholar 

  • Lin X, O'Tousa JE, Duman JG (2010) Expression of two selfenhancing antifreeze proteins from the beetle Dendroides Canadensis in Drosophila melanogaster. J Insect Physiol 56(4):341–349

    CAS  PubMed  Google Scholar 

  • Lin X, Wisniewski M, Duman JG (2011) Expression of two self-enhancing antifreeze proteins from the beetle Dendroides canadensis in Arabidopsis thaliana. Plant Mol Biol Rep 29:802–813

    CAS  Google Scholar 

  • Liu M, Liang Y, Wange Y, Zhang H, Wu G, Wang L, Qian H, Qi X (2018) Effects of recombinant carrot antifreeze protein from Pichia pastoris GS115 on the physicochemical properties of hydrated gluten during freeze−thawed cycles. J Cereal Sci 83:245–251

    CAS  Google Scholar 

  • Martínez-Páramo S, Perez-Cerezales S, Barbosa V, Robles V, Herraez MP (2008a) Advances on fish embryo cryopreservation using antifreeze proteins. Biol Reprod 78:152

    Google Scholar 

  • Martínez-Páramo S, Perez-Cerezales S, Robles V, Anel L, Herraez MP (2008b) Incorporation of antifreeze proteins into zebrafish embryos by a non-invasive method. Cryobiology 56:216–222

    PubMed  Google Scholar 

  • Martínez-Páramo S, Barbosa V, Pérez-Cerezales S, Robles V, Herraez MP (2009) Cryoprotective effects of antifreeze proteins delivered into zebrafish embryos. Cryobiology 58:128–133

    PubMed  Google Scholar 

  • Maunsbach PK, Moffatt B, Testillano P, Risueno M, Yeh S, Griffith M, Maunsbach AB (2001) Genes encoding chitinase antifreeze proteins are regulated by cold and expressed by all cell types in winter rye shoots. Physiol Plantarum 112:359–371

    Google Scholar 

  • Meyer K, Keil M, Naldrett MJ (1999) A leucine-rich repeat protein of carrot that exhibits antifreeze activity. FEBS Lett 447:171–178

    CAS  PubMed  Google Scholar 

  • Muryoi N, Sato M, Kaneko S, Kawahara H, Obata H, Yaish MW, Griffith M, Glick BR (2004) Cloning and expression of afpA, a gene encoding an antifreeze protein from the arctic plant growth promoting rhizobacterium Pseudomonas putida GR12-2. J Bacteriol 186(17):5661–5671

    CAS  PubMed  PubMed Central  Google Scholar 

  • Naidenko T (1997) Cryopreservative of Crassostrea gigas oocytes embryo and larvae using antioxidants echinochromes A and antifreeze protein AFP–I. Cryo Lett 18:375–382

    Google Scholar 

  • Neelakanta G, Hudson AM, Sultana H, Cooley L, Fikrig E (2012) Expression of Ixodes scapularis antifreeze glycoprotein enhances cold tolerance in Drosophila melanogaster. PLoS One 7:e33447

    CAS  PubMed  PubMed Central  Google Scholar 

  • Newsted WJ, Polvi S, Papish B, Kendall E, Saleem M, Koch M, Hussain A, Cutler AJ, Georges F (1994) A low molecular weight peptide from snow mold with epitopic homology to the winter flounder antifreeze protein. Biochem Cell Biol 72(3−4):152–156

    CAS  PubMed  Google Scholar 

  • Nicodemus J, O’Tousa JE, Duman JG (2006) Expression of a beetle, Dendroides canadensis, antifreeze protein in Drosophila melanogaster. J Insect Physiol 52:888–896

    CAS  PubMed  Google Scholar 

  • Nishijima K, Tanaka M, Sakai Y, Koshimoto C, Morimoto M, Watanabe T, Fan J, Kitajima S (2014) Effects of type III antifreeze protein on sperm and embryo cryopreservation in rabbit. Cryobiology 69:22–25

    CAS  PubMed  Google Scholar 

  • Olsen TM, Duman JG (1997) Maintenance of the supercooled state in the gut of overwintering pyrochroid beetle larvae, Dendroides canadensis: role of gut ice nucleators and antifreeze proteins. J Comp Physiol B 167:114–122

    Google Scholar 

  • Park KS, Do H, Lee JH, Park SI, Kim EJ, Kim SJ, Kang SH, Kim HJ (2012) Characterization of the ice-binding protein from Arctic yeast Leucosporidium sp. AY30. Cryobiology 64:286–296

    CAS  PubMed  Google Scholar 

  • Patterson JL, Kelly TJ, Duman JG (1981) Purification and composition of a thermal hysteresis producing protein from the milkweed bug, Oncopeltus fasciatus. J Comp Physiol 142(4):539–542

    CAS  Google Scholar 

  • Pe PPW, Naing AH, Chung MY, Park KI, Kim CK (2019) The role of antifreeze proteins (AFPs) in the regulation of genes involved in response of Hosta capitate to cold. 3 Biotech. https://doi.org/10.1007/s13205-019-1859-5

  • Pertaya N, Marshall CB, Celik Y, Davies PL, Braslavsky I (2008) Direct visualization of spruce budworm antifreeze protein interacting with ice crystals: basal plane affinity confers hyperactivity. Biophys J 95:333–341

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pham L, Dahiya R, Rubinsky B (1999) An in vivo study of antifreeze protein adjuvant cryosurgery. Cryobiology 38:169–175

    CAS  PubMed  Google Scholar 

  • Prathalingam NS, Holt WV, Revell SG, Mirczuk S, Fleck RA, Watson PF (2006) Impact of antifreeze proteins and antifreeze glycoproteins on bovine sperm during freeze−thaw. Theriogenology 66:1894–1900

    CAS  PubMed  Google Scholar 

  • Raymond JA, Fritsen C, Shen K (2007) An ice-binding protein from an Antarctic sea ice bacterium. FEMS Microbiol Ecol 61:214–221

    CAS  PubMed  Google Scholar 

  • Regand A, Goff HD (2006) Ice recrystallization inhibition in ice cream as affected by ice structuring proteins from winter wheat grass. J Dairy Sci 89:49–57

    CAS  PubMed  Google Scholar 

  • Robles V, Cabrita E, Anelb L, Herraez MP (2006) Microinjection of the antifreeze protein type III (AFPIII) in turbot (Scophthalmus maximus) embryos: toxicity and protein distribution. Aquaculture 261:1299–1306

    CAS  Google Scholar 

  • Rubinsky B, Devries A, Arav A (1994) Interaction of thermal hysteresis protein with cells and cell membranes and associated applications. US Patent 5358931

  • Rubinsky B, Arav A, Fletcher GL (1991) Hypothermic protection—a fundamental property of “antifreeze” proteins. Biochem Biophys Res Comm 180:566–571

    CAS  PubMed  Google Scholar 

  • Rubinsky B, Mattioli M, Arav A, Barboni B, Fletcher GL (1992) Inhibition of Ca++ and K+ currents by “antifreeze” proteins. Am J Physiol 262:542–545

    Google Scholar 

  • Rubinsky B, Arav A, Hong JS, Lee CY (1994b) Freezing of mammalian livers with glycerol and antifreeze proteins. Biochem Biophys Res Commun 200:732–741

    CAS  PubMed  Google Scholar 

  • Scholander PF, van Dam L, Kanwisher JW, Hammel HT, Gordon MS (1957) Supercooling and osmoregulation in Arctic fish. J Cell Comp Physiol 49:5–24

    CAS  Google Scholar 

  • Seo JH, Naing AH, Jeon SM, Kim CK (2018) Anti-freezing-protein type III strongly influences the expression of relevant genes in cryopreserved potato shoot tips. Plant Mol Biol 97:347–355

    CAS  PubMed  Google Scholar 

  • Sicheri F, Yang DS (1995) Ice-binding structure and mechanism of an antifreeze protein from winter flounder. Nature 375:427–431

    CAS  PubMed  Google Scholar 

  • Sidebottom C, Buckley S, Pudney P, Twigg S, Jarman C, Holt C, Telford J, McArthur A, Worrall D, Hubbard R, Lillford P (2000) Heat-stable antifreeze protein from grass. Nature 406:256

    CAS  PubMed  Google Scholar 

  • Singh P, Hanada Y, Singh SM, Tsuda S (2014) Antifreeze protein activity in Arctic cryoconite bacteria. FEMS Microbiol Lett 351(1):14–22

    CAS  PubMed  Google Scholar 

  • Soltys KA, Batta AK, Koneru B (2001) Successful nonfreezing, sub-zero preservation of rat liver with 2, 3-butanediol and type I antifreeze protein. J Surg Res 96:30–34

    CAS  PubMed  Google Scholar 

  • Taylor R, Fletcher RL (1998) Cryopreservation of eukaryotic algae—a review of methodologies. J Appl Phycol 10:481–501

    Google Scholar 

  • Taylor R, Fletcher RL (1999) A simple method for the freeze-preservation of zoospores of the green macroalga Enteromorpha intestinalis. J Appl Phycol 11:257–262

    Google Scholar 

  • Thaler R, Spitzer S, Karlic H, Klaushofer K, Varga F (2012) DMSO is a strong inducer of DNA hydroxymethylation in pre-osteoblastic MC3T3-E1 cells. Epigenetics 7:635–651

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tomczak MM, Marshall CB, Gilbert JA, Davies PL (2003) A facile method for determining ice recrystallization inhibition by antifreeze proteins. Biochem Biophys Res Commun 311:1041–1046

    CAS  PubMed  Google Scholar 

  • Uhlig C, Kabisch J, Palm GJ, Valentin K, Schweder T, Krell A (2011) Heterologous expression, refolding and functional characterization of two antifreeze proteins from Fragilariopsis cylindrus (Bacillariophyceae). Cryobiology 63:220–228

    CAS  PubMed  Google Scholar 

  • Uperti GC, Payen SR, Duganzich DM, Oliver JE, Smith JF (1996) Enzyme leakage during cryopreservative of ram spermatozoa. Anim Reprod. Sci. 41:27–36

    Google Scholar 

  • Wallis JG, Wang H, Guerra DJ (1997) Expression of a synthetic antifreeze protein in potato reduces electrolyte release at freezing temperatures. Plant Mol Biol 35:323–330

    CAS  PubMed  Google Scholar 

  • Wang JH, Huang CN (1996) Antifreeze proteins: in hypothermic and cryogenic preservation. Chinese J Cell Biol 18:107–111

    CAS  Google Scholar 

  • Wang R, Zhang P, Gong Z, Hew CL (1995) Expression of the antifreeze protein gene in transgenic goldfish (Carassius auratus) and its implication in cold adaptation. Mol Mar Biol Biotechnol 4:20–26

    CAS  PubMed  Google Scholar 

  • Wang JH, Bian HW, Huang CN, Ge JG (1999) Studies on the application of antifreeze proteins in cryopreservation of rice embryogenic suspension cells. Acta Biol Exp Sinica 32:271–276

    CAS  PubMed  Google Scholar 

  • Wang JH, Bian HW, Zhang YX, Cheng HP (2001) The dual effect of antifreeze protein on cryopreservation of rice (Oryza sativa L.) embryogenic suspension cells. Cryo Lett 22:175–182

    Google Scholar 

  • Wang Y, Qiu L, Dai C, Wang J, Luo J, Zhang F, Ma J (2008) Expression of insect (Microdera puntipennis dzungarica) antifreeze protein MpAFP149 confers the cold tolerance to transgenic tobacco. Plant Cell Rep 27:1349–1358

    CAS  PubMed  Google Scholar 

  • Wisniewski M, Webb R, Balsamo R, Close TJ, Yu XM, Griffith M (1999) Purification, immunolocalization, cryoprotective, and antifreeze activity of PCA60: a dehydrin from peach (Prunus persica). Physiol Plant 105:600–608

    CAS  Google Scholar 

  • Worrall D, Elias L, Ashford D, Smallwood M, Sidebottom C, Lillford P, Telford J, Holt C, Bowles D (1998) A carrot leucine-rich-repeat protein that inhibits ice recrystallization. Science 282:115–117

    CAS  PubMed  Google Scholar 

  • Wu DW, Duman JG, Cheng CHC, Castellino FJ (1991) Purification and characterization of antifreeze proteins from larvae of the beetle Dendroides canadensis. J Comp Physiol B 161:271–278

    CAS  Google Scholar 

  • Yeh S, Moffatt BA, Griffith M, Xiong F, Yang DSC, Wiseman SB, Sarhan F, Danyluk J, Xue YQ, Hew CL, Doherty-Kirby A, Lajoie G (2000) Chitinase genes responsive to cold encode antifreeze proteins in winter cereals. Plant Physiol 124:1251–1263

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang D, Liu B, Feng D, He Y, Wang J (2004) Expression, purification, and antifreeze activity of carrot antifreeze protein and its mutants. Protein Expres Purif 35:257–263

    CAS  Google Scholar 

  • Zhu B, Xiong AS, Peng RH, Xu J, Jin XF, Meng XR, Yao QH (2010) Overexpression of ThpI from Choristoneura fumiferana enhances tolerance to cold in Arabidopsis. Mol Biol Rep 37:961–966

    CAS  PubMed  Google Scholar 

  • Zilli L, Beirao J, Schiavone R, Herraez MP, Gnoni A, Vilella S (2014) Comparative proteome analysis of cryopreserved flagella and head plasma membrane proteins from sea bream spermatozoa: effect of antifreeze proteins. PLoS One 9:e99992

    PubMed  PubMed Central  Google Scholar 

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Funding

This work was supported by the Korea Institute of Planning and Evaluation for Technology in Food, Agriculture, Forestry and Fisheries (IPET) through the Agri-Bio industry Technology Development Program, funded by the Ministry of Agriculture, Food and Rural Affairs (MAFRA) (Grant# 315002-5)

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AHN collected the literature and wrote the manuscript; CKK advised and assisted with the writing of the manuscript.

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Correspondence to Chang Kil Kim.

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Naing, A.H., Kim, C.K. A brief review of applications of antifreeze proteins in cryopreservation and metabolic genetic engineering. 3 Biotech 9, 329 (2019). https://doi.org/10.1007/s13205-019-1861-y

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