The Effects of Type III Antifreeze Protein and Human Heat Shock Protein 70 Added to the Vitrification Medium of Mouse Embryos on in Vitro Embryonic Development Rates

The effect of antifreeze protein type III (AFPIII) and human heat shock protein 70 (HHSP70), added to the vitrification medium of mouse embryos, on post-freeze/thaw in vitro embryonic growth rates and cell numbers were investigated. In total 20 female mice were synchronized. After synchronization, 2 females and 1 male were mated in the same cage. Twenty-four h after mating, the embryos were collected at the pronuclear stage. In total 8 groups were established, including a positive control group (C+), a negative control group (C-), and treatment groups that were vitrified in a medium added with 200, 400 and 800 ng/ml of AFPIII (AFPIII200, AFPIII400, AFPIII800), and 1, 2 and 4 μg/ml of HHSP70 (HHSP70-1, HHSP70-2, HHSP70-4). Solid surface vitrification (SSV) medium was prepared for the vitrification of the embryos. Once thawed, in vitro development rates of embryos were followed at 24, 48, 72 and 96 h. Four embryos, which progressed to the full blastocyst stage, were taken from each group and stained with the Hoeschst 33258 and propidium iodine (PI) dyes to determine the inner cell mass (ICM), trophectoderm (TE) and total cell numbers. The groups showed statistically significant difference for in vitro embryonic development rates at 48, 72 and 96 h (p

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Alvarez-Rodríguez, Manuel, Mercedes Alvarez, Santiago Borragan, Felipe Martinez-Pastor, William Vincent Holt, Alireza Fazeli, Paulino de Paz, and Luis Anel. 2013. The addition of heat shock protein HSPA8 to cryoprotective media improves the survival of brown bear (Ursus arctos) spermatozoa during chilling and after cryopreservation. Theriogenology. 79: 541-50. https://doi.org/10.1016/ j.theriogenology.2012.11.006
Arakawa, Akihiko, Noriko Handa, Mikako Shirouzu, and Shigeyuki Yokoyama. 2011. Biochemical and structural studies on the high affinity of Hsp70 for ADP. Protein Science, 20: 1367-79. https://doi.org/10.1002/pro.663 Başpınar, Nuri. 2010. Biyofiziksel Kimya, In: Biyokimya.
Kalaycıoğlı L, Serpek B, Nizamlıoğlu M, Başpınar N, Tiftik AM (editors), 4. Baskı, Ankara, pp. 1-29. ISBN 978-605-133- 450-9 (print)
Beere, Helen M, Beni B Wolf, Kelvin Cain, Dick D Mosser, Artin Mahboubi, Tomomi Kuwana, Pankaj Tailor, Richard I Morimoto, Gerald M Cohen, and Douglas R Green. 2000.
Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the Apaf-1 apoptosome. Nature Cell Biology, 2: 469-75. https://doi.org/ 10.1038/35019501
Caglar, Kubra, Ahmet Kocabay, Ali Cihan Taskin, and Sezen Arat. 2020. Treatment with Melatonin Enhances the Embryo Quality and the Development of Vitrified/Warmed Eight Cell Mouse Embryos by Solid Surface Vitrification (SSV). CryoLetters, 41: 62-67.
Chao, Heman, Carl I DeLuca, Peter L Davies, Brian D Sykes, and Frank D Sönnichsen. 1994. Structure‐function relationship in the globular type III antifreeze protein: identification of a cluster of surface residues required for binding to ice. Protein Science, 3: 1760-69. https://doi.org/10.1002/pro.5560031016
Chen, Guangju, and Zongchao Jia. 1999. Ice-binding surface of fish type III antifreeze. Biophysical journal, 77: 1602-08. https://doi.org/10.1016/S0006-3495(99)77008-6
Crevel, RWR, JK Fedyk, and MJ Spurgeon. 2002. Antifreeze proteins: characteristics, occurrence and human exposure. Food and Chemical Toxicology, 40: 899-903. https://doi.org/10.1016/S0278-6915(02)00042-X
Cuello, C, Françoise Berthelot, Bernadette Delaleu, Eric Venturi, Luis Miguel Pastor, JM Vazquez, J Roca, Françoise Martinat- Botte, and EA Martinez. 2007. The effectiveness of the stereomicroscopic evaluation of embryo quality in vitrified– warmed porcine blastocysts: An ultrastructural and cell death study. Theriogenology, 67: 970-82. https://doi.org/ 10.1016/j.theriogenology.2006.11.011
DeLuca, Carl I, Peter L Davies, Qilu Ye, and Zongchao Jia. 1998. The effects of steric mutations on the structure of type III antifreeze protein and its interaction with ice. Journal of molecular biology, 275: 515-25. https://doi.org/ 10.1006/jmbi.1997.1482
Ding, Xuan Z, Robert Christian Smallridge, Richard J Galloway, and G Juliann. 1996. Increases in HSF1 translocation and synthesis in human epidermoid A-431 cells: role of protein kinase C and [Ca2+] i. Journal of investigative medicine, 44: 144-53.
Dinnyés, András, Yunping Dai, Shie Jiang, and Xiangzhong Yang. 2000. High developmental rates of vitrified bovine oocytes following parthenogenetic activation, in vitro fertilization, and somatic cell nuclear transfer. Biology of Reproduction, 63: 513-18. https://doi.org/10.1095/ biolreprod63.2.513
Do, Hackwon, Jun Hyuck Lee, Sung Gu Lee, and Hak Jun Kim. 2012. Crystallization and preliminary X-ray crystallographic analysis of an ice-binding protein (FfIBP) from Flavobacterium frigoris PS1. Acta Crystallographica Section F: Structural Biology and Crystallization Communications, 68: 806-09. https://doi.org/10.1107/S1744309112020465
Esfandiari, Navid, Tommaso Falcone, Jeffrey M Goldberg, Ashok Agarwal, and Rakesh K Sharma. 2007. Heat-shock proteins modulate the incidence of apoptosis and oxidative stress in preimplantation mouse embryos. Fertility and sterility, 87: 1214-17. https://doi.org/10.1016/ j.fertnstert.2006.07.1536
Evans, Mark D, Miral Dizdaroglu, and Marcus S Cooke. 2004. Oxidative DNA damage and disease: induction, repair and significance. Mutation Research/Reviews in Mutation Research, 567: 1-61. https://doi.org/10.1016/ j.mrrev.2003.11.001
Graether, Steffen P, Carl I DeLuca, Jason Baardsnes, Gregory A Hill, Peter L Davies, and Zongchao Jia. 1999. Quantitative and qualitative analysis of type III antifreeze protein structure and function. Journal of Biological Chemistry, 274: 11842- 47. https://doi.org/10.1074/jbc.274.17.11842
Gupta, Mukesh Kumar, Sang Jun Uhm, and Hoon Taek Lee. 2010. Effect of vitrification and beta-mercaptoethanol on reactive oxygen species activity and in vitro development of oocytes vitrified before or after in vitro fertilization. Fertility and sterility, 93: 2602-07. https://doi.org/10.1016/ j.fertnstert.2010.01.043
Hassas-Roudsari, Majid, and H Douglas Goff. 2012. Ice structuring proteins from plants: Mechanism of action and food application. Food Research International, 46: 425-36. https://doi.org/10.1016/j.foodres.2011.12.018
Holt, WV, I Del Valle, and A Fazeli. 2015. Heat shock protein A8 stabilizes the bull sperm plasma membrane during cryopreservation: effects of breed, protein concentration, and mode of use. Theriogenology, 84: 693-701.
https://doi.org/10.1016/j.theriogenology.2015.05.004 Ikwegbue, Paul Chukwudi, Priscilla Masamba, Babatunji Emmanuel Oyinloye, and Abidemi Paul Kappo. 2018. Roles of heat shock proteins in apoptosis, oxidative stress, human inflammatory diseases, and cancer. Pharmaceuticals, 11 (1): 2-18. https://doi.org/10.3390/ph11010002
Jia, Zongchao, Carl I DeLuca, Heman Chao, and Peter L Davies. 1996. Structural basis for the binding of a globular antifreeze protein to ice. Nature, 384: 285-88. https://doi.org/ 10.1038/384285a0
Jinyao, LI, MA Ji, and Fuchun Zhang. 2005. Recent advances in research of antifreeze proteins. Chinese Journal of biochemistry and molecular biology, 21: 717-22.
Jo, Jun Woo, Byung Chul Jee, Jung Ryeol Lee, and Chang Suk Suh. 2011. Effect of antifreeze protein supplementation in vitrification medium on mouse oocyte developmental competence. Fertility and sterility, 96: 1239-45.
Johnston, Donald, Hermann Oppermann, Jean Jackson, and W t Levinson. 1980. Induction of four proteins in chick embryo cells by sodium arsenite. Journal of Biological Chemistry, 255: 6975- 80. https://doi.org/10.1016/j.fertnstert.2011.08.023
Kelley, Philip M, and Milton J Schlesinger. 1978. The effect of amino acid analogues and heat shock on gene expression in chicken embryo fibroblasts. Cell, 15: 1277-86. https://doi.org/10.1016/0092-8674(78)90053-3
Kiang, Juliann G, and George C Tsokos. 1998. Heat shock protein 70 kDa: molecular biology, biochemistry, and physiology. Pharmacology & therapeutics, 80: 183-201. https://doi.org/10.1016/S0163-7258(98)00028-X
Leibo, SP, A Martino, S Kobayashi, and JW Pollard. 1996. Stagedependent sensitivity of oocytes and embryos to low temperatures. Animal reproduction science, 42: 45-53. https://doi.org/10.1016/0378-4320(96)01543-6
Levinson, Warren, Hermann Oppermann, and Jean Jackson. 1980. Transition series metals and sulfhydryl reagents induce the synthesis of four proteins in eukaryotic cells. Biochimica et Biophysica Acta (BBA)-Nucleic Acids and Protein Synthesis, 606: 170-80. https://doi.org/10.1016/0005- 2787(80)90108-2
Li, Gloria C, and Andrei Laszlo. 1985. Amino acid analogs while inducing heat shock proteins sensitize CHO cells to thermal damage. Journal of cellular physiology, 122: 91-97. https://doi.org/10.1002/jcp.1041220114
Lim, JM, Y Fukui, and H Ono. 1992. Developmental competence of bovine oocytes frozen at various maturation stages followed by in vitro maturation and fertilization. Theriogenology, 37: 351-61. https://doi.org/10.1016/0093- 691X(92)90193-U
Mazur, Peter. 1996. Principles of medical cryobiology: The freezing of living cells, tissues, and organs. in, Principles of Medical Biology (Elsevier).pp.355-384. ISBN 978-0-7623- 1124-8 (online).
Morató, Roser, Dolors Izquierdo, José Luis Albarracín, Begoña Anguita, María Jesús Palomo, Ana Raquel Jiménez‐Macedo, María Teresa Paramio, and Teresa Mogas. 2008. Effects of pre‐treating in vitro‐matured bovine oocytes with the cytoskeleton stabilizing agent taxol prior to vitrification. Molecular Reproduction and Development: Incorporating Gamete Research, 75: 191-201. https://doi.org/ 10.1002/mrd.20725
Nishijima, Kazutoshi, Mai Tanaka, Yusuke Sakai, Chihiro Koshimoto, Masatoshi Morimoto, Teruo Watanabe, Jianglin Fan, and Shuji Kitajima. 2014. Effects of type III antifreeze protein on sperm and embryo cryopreservation in rabbit. Cryobiology, 69: 22-25. https://doi.org/10.1016/ j.cryobiol.2014.04.014
Pouysségur, Jacques, Robert PC Shiu, and Ira Pastan. 1977. Induction of two transformation-sensitive membrane polypeptides in normal fibroblasts by a block in glycoprotein synthesis or glucose deprivation. Cell, 11: 941-47. https://doi.org/10.1016/0092-8674(77)90305-1
Somfai, Tamás, Manabu Ozawa, Junko Noguchi, Hiroyuki Kaneko, Ni Wayan Kuriani Karja, Mokhamad Farhudin, András Dinnyés, Takashi Nagai, and Kazuhiro Kikuchi. 2007. Developmental competence of in vitro-fertilized porcine oocytes after in vitro maturation and solid surface vitrification: effect of cryopreservation on oocyte antioxidative system and cell cycle stage. Cryobiology, 55: 115-26. https://doi.org/10.1016/j.cryobiol.2007.06.008
Succu, Sara, Giovanni Giuseppe Leoni, Fiammetta Berlinguer, Manuela Madeddu, Daniela Bebbere, Francesca Mossa, Luisa Bogliolo, Sergio Ledda, and Salvatore Naitana. 2007. Effect of vitrification solutions and cooling upon in vitro matured prepubertal ovine oocytes. Theriogenology, 68: 107- 14. https://doi.org/10.1016/j.theriogenology.2007.04.035
Sun, Wu-Sheng, Hoon Jang, Hyo Jin Kwon, Ki Young Kim, Soo Bin Ahn, Seongsoo Hwang, Sung Gu Lee, Jun Hyuck Lee, In-Sul Hwang, and Jeong-Woong Lee. 2020. The protective effect of Leucosporidium-derived ice-binding protein (LeIBP) on bovine oocytes and embryos during vitrification. Theriogenology, 151: 137-43. https://doi.org/10.1016/ j.theriogenology.2020.04.016
Trott, Amy, James D West, Lada Klaić, Sandy D Westerheide, Richard B Silverman, Richard I Morimoto, and Kevin A Morano. 2008. Activation of heat shock and antioxidant responses by the natural product celastrol: transcriptional signatures of a thiol-targeted molecule. Molecular biology of the cell, 19: 1104-12. https://doi.org/10.1091/mbc.e07-10-1004
Üstün, Nebahat Sule, and Sadettin Turhan. 2015. Antifreeze proteins: Characteristics, function, mechanism of action, sources and application to foods. Journal of food processing and preservation, 39: 3189-97. https://doi.org/ 10.1111/jfpp.12476
Vladimirov, Iavor K, Desislava Tacheva, and Vladislav Dobrinov. 2018. The Present and Future of Embryo Cryopreservation. in, Embryology-Theory and Practice (IntechOpen). pp. 1-20. ISBN 978-1-78985-306-3. Witt, Dariusz. 2008. Recent developments in disulfide bond formation. Synthesis, 2008: 2491-509. Doi: 10.1055/s-2008- 1067188
Esfandiari, Navid, Tommaso Falcone, Jeffrey M Goldberg, Ashok Agarwal, and Rakesh K Sharma. 2007. Heat-shock proteins modulate the incidence of apoptosis and oxidative stress in preimplantation mouse embryos. Fertility and sterility, 87: 1214-17. https://doi.org/10.1016/ j.fertnstert.2006.07.1536
Evans, Mark D, Miral Dizdaroglu, and Marcus S Cooke. 2004. Oxidative DNA damage and disease: induction, repair and significance. Mutation Research/Reviews in Mutation Research, 567: 1-61. https://doi.org/10.1016/ j.mrrev.2003.11.001
Graether, Steffen P, Carl I DeLuca, Jason Baardsnes, Gregory A Hill, Peter L Davies, and Zongchao Jia. 1999. Quantitative and qualitative analysis of type III antifreeze protein structure and function. Journal of Biological Chemistry, 274: 11842- 47. https://doi.org/10.1074/jbc.274.17.11842
Gupta, Mukesh Kumar, Sang Jun Uhm, and Hoon Taek Lee. 2010. Effect of vitrification and beta-mercaptoethanol on reactive oxygen species activity and in vitro development of oocytes vitrified before or after in vitro fertilization. Fertility and sterility, 93: 2602-07. https://doi.org/10.1016/ j.fertnstert.2010.01.043
Hassas-Roudsari, Majid, and H Douglas Goff. 2012. Ice structuring proteins from plants: Mechanism of action and food application. Food Research International, 46: 425-36. https://doi.org/10.1016/j.foodres.2011.12.018
Holt, WV, I Del Valle, and A Fazeli. 2015. Heat shock protein A8 stabilizes the bull sperm plasma membrane during cryopreservation: effects of breed, protein concentration, and mode of use. Theriogenology, 84: 693-701. https://doi.org/10.1016/j.theriogenology.2015.05.004
Ikwegbue, Paul Chukwudi, Priscilla Masamba, Babatunji Emmanuel Oyinloye, and Abidemi Paul Kappo. 2018. Roles of heat shock proteins in apoptosis, oxidative stress, human inflammatory diseases, and cancer. Pharmaceuticals, 11 (1): 2-18. https://doi.org/10.3390/ph11010002
Jia, Zongchao, Carl I DeLuca, Heman Chao, and Peter L Davies. 1996. Structural basis for the binding of a globular antifreeze protein to ice. Nature, 384: 285-88. https://doi.org/ 10.1038/384285a0
Jinyao, LI, MA Ji, and Fuchun Zhang. 2005. Recent advances in research of antifreeze proteins. Chinese Journal of biochemistry and molecular biology, 21: 717-22.
Jo, Jun Woo, Byung Chul Jee, Jung Ryeol Lee, and Chang Suk Suh. 2011. Effect of antifreeze protein supplementation in vitrification medium on mouse oocyte developmental competence. Fertility and sterility, 96: 1239-45.
Johnston, Donald, Hermann Oppermann, Jean Jackson, and W t Levinson. 1980. Induction of four proteins in chick embryo cells by sodium arsenite. Journal of Biological Chemistry, 255: 6975- 80. https://doi.org/10.1016/j.fertnstert.2011.08.023
Kelley, Philip M, and Milton J Schlesinger. 1978. The effect of amino acid analogues and heat shock on gene expression in chicken embryo fibroblasts. Cell, 15: 1277-86. https://doi.org/10.1016/0092-8674(78)90053-3
Kiang, Juliann G, and George C Tsokos. 1998. Heat shock protein 70 kDa: molecular biology, biochemistry, and physiology. Pharmacology & therapeutics, 80: 183-201. https://doi.org/10.1016/S0163-7258(98)00028-X
Leibo, SP, A Martino, S Kobayashi, and JW Pollard. 1996. Stagedependent sensitivity of oocytes and embryos to low temperatures. Animal reproduction science, 42: 45-53. https://doi.org/10.1016/0378-4320(96)01543-6
Levinson, Warren, Hermann Oppermann, and Jean Jackson. 1980. Transition series metals and sulfhydryl reagents induce the synthesis of four proteins in eukaryotic cells. Biochimica et Biophysica Acta (BBA)-Nucleic Acids and Protein Synthesis, 606: 170-80. https://doi.org/10.1016/0005- 2787(80)90108-2
Li, Gloria C, and Andrei Laszlo. 1985. Amino acid analogs while inducing heat shock proteins sensitize CHO cells to thermal damage. Journal of cellular physiology, 122: 91-97. https://doi.org/10.1002/jcp.1041220114
Lim, JM, Y Fukui, and H Ono. 1992. Developmental competence of bovine oocytes frozen at various maturation stages followed by in vitro maturation and fertilization. Theriogenology, 37: 351-61. https://doi.org/10.1016/0093- 691X(92)90193-U
Mazur, Peter. 1996. Principles of medical cryobiology: The freezing of living cells, tissues, and organs. in, Principles of Medical Biology (Elsevier).pp.355-384. ISBN 978-0-7623- 1124-8 (online).
Morató, Roser, Dolors Izquierdo, José Luis Albarracín, Begoña Anguita, María Jesús Palomo, Ana Raquel Jiménez‐Macedo, María Teresa Paramio, and Teresa Mogas. 2008. Effects of pre‐treating in vitro‐matured bovine oocytes with the cytoskeleton stabilizing agent taxol prior to vitrification. Molecular Reproduction and Development: Incorporating Gamete Research, 75: 191-201. https://doi.org/ 10.1002/mrd.20725
Nishijima, Kazutoshi, Mai Tanaka, Yusuke Sakai, Chihiro Koshimoto, Masatoshi Morimoto, Teruo Watanabe, Jianglin Fan, and Shuji Kitajima. 2014. Effects of type III antifreeze protein on sperm and embryo cryopreservation in rabbit. Cryobiology, 69: 22-25. https://doi.org/10.1016/ j.cryobiol.2014.04.014
Pouysségur, Jacques, Robert PC Shiu, and Ira Pastan. 1977. Induction of two transformation-sensitive membrane polypeptides in normal fibroblasts by a block in glycoprotein synthesis or glucose deprivation. Cell, 11: 941-47. https://doi.org/10.1016/0092-8674(77)90305-1
Somfai, Tamás, Manabu Ozawa, Junko Noguchi, Hiroyuki Kaneko, Ni Wayan Kuriani Karja, Mokhamad Farhudin, András Dinnyés, Takashi Nagai, and Kazuhiro Kikuchi. 2007. Developmental competence of in vitro-fertilized porcine oocytes after in vitro maturation and solid surface vitrification: effect of cryopreservation on oocyte antioxidative system and cell cycle stage. Cryobiology, 55: 115-26. https://doi.org/10.1016/j.cryobiol.2007.06.008
Succu, Sara, Giovanni Giuseppe Leoni, Fiammetta Berlinguer, Manuela Madeddu, Daniela Bebbere, Francesca Mossa, Luisa Bogliolo, Sergio Ledda, and Salvatore Naitana. 2007. Effect of vitrification solutions and cooling upon in vitro matured prepubertal ovine oocytes. Theriogenology, 68: 107- 14. https://doi.org/10.1016/j.theriogenology.2007.04.035
Sun, Wu-Sheng, Hoon Jang, Hyo Jin Kwon, Ki Young Kim, Soo Bin Ahn, Seongsoo Hwang, Sung Gu Lee, Jun Hyuck Lee, In-Sul Hwang, and Jeong-Woong Lee. 2020. The protective effect of Leucosporidium-derived ice-binding protein (LeIBP) on bovine oocytes and embryos during vitrification. Theriogenology, 151: 137-43. https://doi.org/10.1016/ j.theriogenology.2020.04.016
Trott, Amy, James D West, Lada Klaić, Sandy D Westerheide, Richard B Silverman, Richard I Morimoto, and Kevin A Morano. 2008. Activation of heat shock and antioxidant responses by the natural product celastrol: transcriptional signatures of a thiol-targeted molecule. Molecular biology of the cell, 19: 1104-12. https://doi.org/10.1091/mbc.e07-10-1004 Üstün, Nebahat Sule, and Sadettin Turhan. 2015. Antifreeze proteins: Characteristics, function, mechanism of action, sources and application to foods. Journal of food processing and preservation, 39: 3189-97. https://doi.org/ 10.1111/jfpp.12476
Vladimirov, Iavor K, Desislava Tacheva, and Vladislav Dobrinov. 2018. The Present and Future of Embryo Cryopreservation. in, Embryology-Theory and Practice (IntechOpen). pp. 1-20. ISBN 978-1-78985-306-3.
Witt, Dariusz. 2008. Recent developments in disulfide bond formation. Synthesis, 2008: 2491-509. Doi: 10.1055/s-2008- 1067188
Yang, Jie, Hong Zhang, Weibin Gong, Zhenyan Liu, Huiwen Wu, Wanhui Hu, Xinxin Chen, Lei Wang, Si Wu, and Chang Chen. 2020. S-Glutathionylation of human inducible Hsp70 reveals a regulatory mechanism involving the C-terminal α- helical lid. Journal of Biological Chemistry, 295: 8302-24. https://doi.org/10.1074/jbc.RA119.012372
Zhao, Xue‐Ming, Xiang‐Wei Fu, Yun‐Peng Hou, Chang‐Liang Yan, LUN Suo, Yan‐Ping Wang, Hua‐Bin Zhu, Andras Dinnyés, and Shi‐En Zhu. 2009. Effect of vitrification on mitochondrial distribution and membrane potential in mouse two pronuclear (2‐PN) embryos. Molecular Reproduction and Development: Incorporating Gamete Research, 76: 1056-63. https://doi.org/10.1002/mrd.21064