仿生控冰材料用于细胞及组织的冷冻保存
收稿日期: 2021-02-03
网络出版日期: 2021-03-19
基金资助
国家自然科学基金(51925307); 国家自然科学基金(21733010); 国家重点研发计划项目(2018YFA0208502); 中国科学院前沿科学重点研究项目(ZDBS-LYSLH031)
Bio-inspired Ice-controlling Materials for Cryopreservation of Cells and Tissues
Received date: 2021-02-03
Online published: 2021-03-19
Supported by
National Natural Science Foundation of China(51925307); National Natural Science Foundation of China(21733010); National Key R&D Program of China(2018YFA0208502); Key Research Program of Frontier Sciences, CAS(ZDBS-LYSLH031)
冷冻保存是将细胞、组织或器官等生物样品置于超低温环境中, 使其代谢速率大大降低甚至停止, 以达到长期存储的目的, 并能在解冻后恢复其生理功能的科学与技术. 冷冻保存是当前实现生物样品长期存储的唯一有效手段, 是细胞治疗、再生医学以及器官移植等先进医疗技术充分发展的关键瓶颈之一. 然而, 由于细胞、组织中的含水量可高达70%~90%, 在不添加冷冻保护剂的情况下, 降温及复苏过程中伴随的冰晶损伤、渗透压失衡及溶质过度积累等必然会导致冻存失败. 传统冷冻保存策略通过大量使用二甲基亚砜(dimethyl sulfoxide, DMSO)等能与水形成氢键的有机小分子置换出部分胞内水分, 有效避免了胞内形成大冰晶及溶质过度积累等不利因素, 使细胞得以成功冻存. 然而, 该类小分子已被证实破坏蛋白质结构、胞间连接, 并且具有表观遗传毒性; 同时, 传统的冻存策略很难用于组织器官冻存. 因此冷冻保存科学与技术急需冷冻保护材料(剂)的创新, 以摒弃有毒小分子的大量使用, 实现细胞、组织及器官的安全高效冻存. 控冰蛋白是在极寒地区生物体内发现的一类高效冰晶成核与生长控制剂, 可以保护生物不受冰冻损伤. 揭示控冰蛋白作用机制将为仿生构筑高效控冰材料, 开发新型控冰冷冻保存剂提供全新的思路. 本综述将简单回顾冷冻保存的发展历史, 评述传统冷冻保存策略的优缺点; 从新型仿生控冰冷冻保护剂的研究出发, 重点阐述近几十年来控冰蛋白控冰机制的研究进展、仿生控冰材料的创制及其在冷冻保存中的应用; 最后将进一步展望仿生控冰冻存材料未来的发展方向.
郑夏 , 刘建亭 , 刘樟 , 王健君 . 仿生控冰材料用于细胞及组织的冷冻保存[J]. 化学学报, 2021 , 79(6) : 729 -741 . DOI: 10.6023/A21020043
Cryopreservation is a science and technology of using ultra-low temperatures for the long-term storage of cells, tissues, or organs; also it ensures a recovery in function after thawing. Cryopreservation is currently the only effective method to realize long-term storage of biological samples, and it plays a critical role in areas of biomedicine such as cell therapy, regenerative medicine and organ transplantation. As the water content of cells and tissues can be as high as 70%~90%, ice formation inevitably occurs both intracellularly and extracellularly, which can be lethal because of the mechanical damage, the osmotic shock and excessive solute accumulations. Therefore, the scientific challenge of cryopreservation is to inhibit or control ice formation in the freezing/thawing processes. Traditional cryopreservation strategies use large amounts of small molecules, such as dimethyl sulfoxide (DMSO), as cryoprotectant (CPA) to permeate into the cells and prevent intracellular ice formation; which to some extends are successful in the cryopreservation of cells. However, these molecules are chemically and epigenetically toxic to cells. Meanwhile, these strategies have proved refractory for the cryopreservation of tissues and organs. Therefore, great efforts have been made for effective ice-controlling materials to regulate the ice formation during cryopreservation. In nature, many cold-acclimated species can avoid cold damage and survive in the subzero environment due to the existence of ice-regulating proteins, i.e., ice nucleating proteins (INPs) and antifreeze (glyco) proteins (AF(G)Ps). Inspired by these proteins, intensive investigations have been made to reveal the protection mechanism of the ice-regulating proteins in order to develop their mimics. It has been reported that the bio-inspired ice-controlling materials are more effective and safer CPA in cryopreservation in comparison to small organic molecules. Therefore, the present review will briefly summarize the history of cryopreservation for cells and tissues, and focus on the development of bio-inspired ice-controlling materials and their application in the cryopreservation of cells and tissues. At last, the challenges and possible directions of bio-inspired ice-controlling materials as cryoprotective agents will be briefed.
[1] | Giwa, S.; Lewis, J. K.; Alvarez, L.; Langer, R.; Roth, A. E.; Church, G. M.; Markmann, J. F.; Sachs, D. H.; Chandraker, A.; Wertheim, J. A.; Rothblatt, M.; Boyden, E. S.; Eidbo, E.; Lee, W. P. A.; Pomahac, B.; Brandacher, G.; Weinstock, D. M.; Elliott, G.; Nelson, D.; Acker, J. P.; Uygun, K.; Schmalz, B.; Weegman, B. P.; Tocchio, A.; Fahy, G. M.; Storey, K. B.; Rubinsky, B.; Bischof, J.; Elliott, J. A. W.; Woodruff, T. K.; Morris, G. J.; Demirci, U.; Brockbank, K. G. M.; Woods, E. J.; Ben, R. N.; Baust, J. G.; Gao, D.; Fuller, B.; Rabin, Y.; Kravitz, D. C.; Taylor, M. J.; Toner, M. Nat. Biotechnol. 2017, 35, 530. |
[2] | Takahashi, K.; Ohnuki, M.; Narita, M.; Ichisaka, T.; Tomoda, K.; Yamanaka, S. Cell 2007, 131, 861. |
[3] | Wakeman, D. R.; Hiller, B. M.; Marmion, D. J.; McMahon, C. W.; Corbett, G. T.; Mangan, K. P.; Ma, J. Y.; Little, L. E.; Xie, Z.; Perez-Rosello, T.; Guzman, J. N.; Surmeier, D. J.; Kordower, J. H. Stem Cell Rep. 2017, 9, 149. |
[4] | Maranda, E. L.; Rodriguez-Menocal, L.; Badiavas, E. V. Curr. Stem Cell Res. Ther. 2017, 12, 61. |
[5] | Valipour, B.; Abedelahic, A.; Naderalia, E.; Velaeic, K.; Movassaghpourd, A.; Talebid, M.; Montazersahebe, S.; Karimipourc, M.; Darabif, M.; Chavoshid, H.; Charoudeh, H. N. Life Sci. 2020, 242, 1. |
[6] | Kriks, S.; Shim, J. W.; Piao, J.; Ganat, Y. M.; Wakeman, D. R.; Xie, Z.; Carrillo-Reid, L.; Auyeung, G.; Antonacci, C.; Buch, A.; Yang, L.; Beal, M. F.; Surmeier, D. J.; Kordower, J. H.; Tabar, V.; Studer, L. Nature 2011, 480, 547. |
[7] | Najafi, M.; Farhood, B.; Mortezaee, K. J. Cell Physiol. 2019, 234, 8381. |
[8] | Starzl, T. E. J. Surg. Res. 1970, 10, 291. |
[9] | Elliott, G. D.; Wang, S.; Fuller, B. J. Cryobiology 2017, 76, 74. |
[10] | Pegg, D. E. Methods Mol. Biol. 2015, 1257, 3. |
[11] | Hunt, C. J. Stem Cell Banking: Concepts and Protocols, Vol. 1590, Eds.: Crook, J. M.; Ludwig, T.E., Humana Press, New York, 2017, p.41. |
[12] | Polge, C.; Smith, A. U.; Parkes, A. S. Nature 1949, 164, 666. |
[13] | Lovelock, J. E.; Bishop, M. W. H. Nature 1959, 183, 1394. |
[14] | Ein, L.; Naseri, M.; Karimi-Busheri, F.; Bozorgmehr, M.; Ghods, R.; Madjd, Z. J. Cell Physiol. 2020, 235, 2452. |
[15] | Ishizukaa, Y.; Bramham, C. R. J. Neurosci. Methods 2020, 333, 1. |
[16] | Madrigal-Valverde, M.; Bittencourt, R. F.; Lisboa Ribeiro Filho, A.; Araujo, G. R.; Lents, M. P.; Santos, E. S.; Lima, A. S.; Mattos, P. Cryobiology 2020, 97, 138. |
[17] | Amorim, C. A.; Curaba, M.; Van Langendonckt, A.; Dolmans, M. M.; Donnez, J. Reprod. Biomed. Online 2011, 23, 160. |
[18] | Towey, J. J.; Soper, A. K.; Dougan, L. Faraday Discuss. 2013, 167, 159. |
[19] | Gurtovenko, A. A.; Anwar, J. Phys. Chem. B 2007, 111, 10453. |
[20] | Rasmussen, D. H.; MacKenzie, A. P. Nature 1968, 220, 1315. |
[21] | Fahy, G. M.; Wowk, B.; Wu, J.; Phan, J.; Rasch, C.; Chang, A.; Zendejas, E. Cryobiology 2004, 48, 157. |
[22] | Bunge, R. G.; Sherman, J. K. Nature 1953, 172, 767. |
[23] | Chen, C. Lancet 1986, 1, 884. |
[24] | Reubinoff, B. E.; Pera, M. F.; Vajta, G.; Trounson, A. O. Hum. Reprod. 2001, 16, 2187. |
[25] | Berz, D.; McCormack, E. M.; Winer, E. S.; Colvin, G. A.; Quesenberry, P. J. Am. J. Hematol. 2007, 82, 463. |
[26] | Holm, F.; Strom, S.; Inzunza, J.; Baker, D.; Stromberg, A. M.; Rozell, B.; Feki, A.; Bergstrom, R.; Hovatta, O. Hum. Reprod. 2010, 25, 1271. |
[27] | Niclis, J. C.; Gantner, C. W.; Alsanie, W. F.; McDougall, S. J.; Bye, C. R.; Elefanty, A. G.; Stanley, E. G.; Haynes, J. M.; Pouton, C. W.; Thompson, L. H.; Parish, C. L. Stem Cells Transl. Med. 2017, 6, 937. |
[28] | Cheng, C. Y.; Song, J.; Pas, J.; Meijer, L. H.; Han, S. Biophys. J. 2015, 109, 330. |
[29] | Fahy, G. M. Cryobiology 2010, 60, S45. |
[30] | Kang, M. H.; You, S. Y.; Hong, K.; Kim, J. H. Biomaterials 2020, 230, 119604. |
[31] | Whittingham, D. G.; Leibo, S. P.; Mazur, P. Science 1972, 178, 411. |
[32] | Trounson, A.; Mohr, L. Nature 1983, 305, 707. |
[33] | Hovatta, O.; Silye, R.; Krausz, T.; Abir, R.; Margara, R.; Trew, G.; Lass, A.; Winston, R. M. L. Hum. Reprod. 1996, 11, 1268. |
[34] | Donnez, J.; Dolmans, M. M.; Demylle, D.; Jadoul, P.; Pirard, C.; Squifflet, J.; Martinez-Madrid, B.; Van Langendonckt, A. Lancet 2004, 364, 1405. |
[35] | Rivas Leonel, E. C.; Lucci, C. M.; Amorim, C. A. Transfus. Med. Hemother. 2019, 46, 173. |
[36] | Courbiere, B.; Caquant, L.; Mazoyer, C.; Franck, M.; Lornage, J.; Salle, B. Fertil. Steril. 2009, 91, 2697. |
[37] | Qiao, J.; Su, P. Reproductive engineering, People's Medical Publishing House, Beijing, 2007, p.5. (in Chinese) |
[37] | (乔杰, 苏萍, 生殖工程学, 人民卫生出版社, 北京, 2007, p. 5) |
[38] | Lu, G. X.; Dai, Z. Y.; Wang, Y. Z.; Xue, Q. M.; Peng, Y. X.; Zhu, J. Z. J. Hunan Med. Univ. 1983, 8, 219. (in Chinese) |
[38] | (卢光琇, 戴中原, 王炎之, 薛启明, 彭挹勋, 朱敬璋, 湖南医学院学报, 1983, 8, 219.) |
[39] | Manuchehrabadi, N.; Gao, Z.; Zhang, J. J.; Ring, H. L.; Shao, Q.; Liu, F.; McDermott, M.; Fok, A.; Rabin, Y.; Brockbank, K. G. M.; Garwood, M.; Haynes, C. L.; Bischof, J. C. Sci. Transl. Med. 2017, 9, eaah4586. |
[40] | Storey, K. B.; Storey, J. M. Sci. Am. 1990, 263, 92. |
[41] | Taylor, M. J.; Weegman, B. P.; Baicu, S. C.; Giwa, S. E. Transfus. Med. Hemother. 2019, 46, 197. |
[42] | DeVries, A. L. Science 1969, 163, 1073. |
[43] | Duman, J. G.; Bennett, V.; Sformo, T.; Hochstrasser, R.; Barnes, B. M. J. Insect Physiol. 2004, 50, 259. |
[44] | Griffith, M.; Yaish, M. W. Trends Plant Sci. 2004, 9, 399. |
[45] | Villarreal, P.; Carrasco, M.; Barahona, S.; Alcaino, J.; Cifuentes, V.; Baeza, M. BMC Microbiol. 2018, 18, 1. |
[46] | Bar Dolev, M.; Braslavsky, I.; Davies, P. L. Annu. Rev. Biochem. 2016, 85, 515. |
[47] | Kim, M.; Gwak, Y.; Jung, W.; Jin, E. Mar. Drugs 2017, 15, 1. |
[48] | Mao, X.; Liu, Z.; Ma, J.; Pang, H.; Zhang, F. Cryobiology 2011, 62, 91. |
[49] | Haji-Akbari, A. Proc. Natl. Acad. Sci. U. S. A. 2016, 113, 3714. |
[50] | Davies, P. L. Trends Biochem. Sci. 2014, 39, 548. |
[51] | Duman, J. G. Annu. Rev. Physiol. 2001, 63, 327. |
[52] | Balcerzak, A. K.; Capicciotti, C. J.; Briard, J. G.; Ben, R. N. RSC Adv. 2014, 4, 42682. |
[53] | Deller, R. C.; Vatish, M.; Mitchell, D. A.; Gibson, M. I. Nat. Commun. 2014, 5, 3244. |
[54] | Geng, H. Y.; Liu, X.; Shi, G. S.; Bai, G. Y.; Ma, J.; Chen, J. B.; Wu, Z. Y.; Song, Y. L.; Fang, H. P.; Wang, J. J. Angew. Chem. Int. Ed. 2017, 56, 997. |
[55] | Qin, Q. Y.; Zhao, L. S.; Liu, Z.; Liu, T.; Qu, J. X.; Zhang, X. W.; Li, R.; Yan, L. Y.; Yan, J.; Jin, S. L.; Wang, J. J.; Qiao, J. ACS Appl. Mater. Interfaces 2020, 12, 18352. |
[56] | Lovelock, J. E. Biochim. Biophys. Acta 1953, 10, 414. |
[57] | Mazur, P. J. Gen. Physiol. 1963, 47, 347. |
[58] | Mazur, P. Science 1970, 168, 939. |
[59] | Leibo, S. P.; Mazur, P. Cryobiology 1971, 8, 447. |
[60] | Jang, T. H.; Park, S. C.; Yang, J. H.; Kim, J. Y.; Seok, J. H.; Park, U. S.; Choi, C. W.; Lee, S. R.; Han, J. Integr. Med. Res. 2017, 6, 12. |
[61] | Fowler, A.; Toner, M. Ann. N. Y. Acad. Sci. 2005, 1066, 119. |
[62] | Pegg, D. E. Cryobiology 2010, 60, S36. |
[63] | Kopeika, J.; Thornhill, A.; Khalaf, Y. Hum. Reprod. Update 2015, 21, 209. |
[64] | Pegg, D. E. Hum. Fertil. 2009, 8, 231. |
[65] | Luyet, B. J.; Gibbs, M. C. Biochim. Biophys. Acta 1937, 25, 1. |
[66] | Yavin, S.; Arva, A. Theriogenology 2007, 67, 81. |
[67] | Fahy, G. M.; Wowk, B. Cryopreservation and Freeze-Drying Protocols, Vol. 1257, Eds.: Wolkers, W. F.; Harri?tte, O., Humana Press, New York, 2015, p.21. |
[68] | Fahy, G. M.; Wowk, B.; Wu, J.; Paynter, S. Cryobiology 2004, 48, 22. |
[69] | Rall, W. F.; Fahy, G. M. Nature 1985, 313, 573. |
[70] | Xu, H. F.; Liu, B. L.; Gao, Z. X. Cryogenics 2010, 5, 59. (in Chinese) |
[70] | (徐海峰, 刘宝林, 高志新, 低温工程, 2010, 5, 59.) |
[71] | Fahy, G. M.; Wowk, B.; Pagotan, R.; Chang, A.; Phan, J.; Thomson, B.; Phan, L. Organogenesis 2009, 5, 167. |
[72] | Argyle, C. E.; Harper, J. C.; Davies, M. C. Hum. Reprod. Update 2016, 22, 440. |
[73] | Chinnadurai, R.; Garcia, M. A.; Sakurai, Y.; Lam, W. A.; Kirk, A. D.; Galipeau, J.; Copland, I. B. Stem Cell Rep. 2014, 3, 60. |
[74] | Kashino, G.; Liu, Y.; Suzuki, M.; Masunaga, S.; Kinashi, Y.; Ono, K.; Tano, K. J. Radiat. Res. 2010, 51, 73. |
[75] | Watanabe, M.; Kaiser, J. Science 2002, 295, 1015. |
[76] | Pegg, D. E.; Wusteman, M. C.; Boylan, S. Cryobiology 1997, 34, 183. |
[77] | Spindler, R.; Wolkers, W. F.; Glasmacher, B. J. Biomech. Eng. 2009, 131, 074517-1. |
[78] | Giugliarelli, A.; Urbanelli, L.; Ricci, M.; Paolantoni, M.; Emiliani, C.; Saccardi, R.; Mazzanti, B.; Lombardini, L.; Morresi, A.; Sassi, P. J. Phys. Chem. A 2016, 120, 5065. |
[79] | Galvao, J.; Davis, B.; Tilley, M.; Normando, E.; Duchen, M. R.; Cordeiro, M. F. FASEB J. 2014, 28, 1317. |
[80] | Boiso, I.; Martí, M.; Santaló, J.; Ponsá, M.; Pere N.; Barri, P. N.; Veiga, A. Hum. Reprod. 2001, 17, 1885. |
[81] | Eroglu, A.; Toth, T. L.; Toner, M. Fertil. Steril. 1998, 69, 944. |
[82] | Alam, M. H.; Miyano, T. Reprod. Med. Biol. 2020, 19, 13. |
[83] | Trapphoff, T.; El Hajj, N.; Zechner, U.; Haaf, T.; Eichenlaub-Ritter, U. Hum. Reprod. 2010, 25, 3025. |
[84] | Okumura, N.; Kagami, T.; Watanabe, K.; Kadoya, S.; Sato, M.; Koizumi, N. PLoS One 2019, 14, e0218431. |
[85] | Iwatani, M.; Ikegami, K.; Kremenska, Y.; Hattori, N.; Tanaka, S.; Yagi, S.; Shiota, K. Stem Cells 2006, 24, 2549. |
[86] | Weng, L. D.; Beauchesne, P. R. Cryobiology 2020, 94, 9. |
[87] | Gallardo, M.; Paulini, F.; Corral, A.; Balcerzyk, M.; Lucci, C. M.; Ambroise, J.; Merola, M.; Fernandez-Maza, L.; Risco, R.; Dolmans, M.; Amorim, C. A. Reprod. BioMed. Online 2018, 37, 653. |
[88] | Song, Y. S.; Adler, D.; Xu, F.; Kayaalp, E.; Nureddin, A.; Anchan, R. M.; Maas, R. L.; Demirci, U. Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 4596. |
[89] | Seki, S.; Mazur, P. Cryobiology 2009, 59, 75. |
[90] | Campbell, B. K.; Hernandez-Medrano, J.; Onions, V.; Pincott-Allen, C.; Aljaser, F.; Fisher, J.; McNeilly, A. S.; Webb, R.; Picton, H. M. Hum. Reprod. 2014, 29, 1749. |
[91] | Wang, X.; Chen, H. F.; Yin, H.; Kim, S. S.; Tan, S. L.; Gosden, R. G. Nature 2002, 415, 385. |
[92] | Nasralla, D.; Coussios, C. C.; Mergental, H.; Akhtar, M. Z.; Butler, A. J.; Ceresa, C. D. L.; Chiocchia, V.; Dutton, S. J.; García-Valdecasas, J. C.; Heaton, N.; Imber, C.; Jassem, W.; Jochmans, I.; Karani, J.; Knight, S. R.; Kocabayoglu, P.; Malagò, M.; Mirza, D.; Morris, P. J.; Pallan, A.; Paul, A.; Pavel, M.; Perera, M. T. P. R.; Pirenne, J.; Ravikumar, R.; Russell, L.; Upponi, S.; Watson, C. J. E.; Weissenbacher, A.; Ploeg, R. J.; Friend, P. J.. Nature 2018, 557, 50. |
[93] | Rosania, K. Lab Anim. 2013, 42, 343. |
[94] | Miller, L. K. J. Insect Physiol. 1978, 24, 791. |
[95] | Storey, K. B.; Storey, J. M. Physiol. Rev. 1988, 68, 27. |
[96] | Raymond, J. A.; DeVries, A. L. Proc. Natl. Acad. Sci. U. S. A. 1977, 74, 2589. |
[97] | Qiu, L. M.; Ma, J.; Wang, J.; Zhang, F. C.; Wang, Y. Cryobiology 2010, 60, 192. |
[98] | Graham, L. A.; Liou, Y.; Walker, V. K.; Davies, P. L. Nature 1997, 388, 727. |
[99] | Graham, L. A.; Davies, P. L. Science 2005, 310, 461. |
[100] | Davies, P. L. Trends Biochem. Sci. 2014, 39, 548. |
[101] | Capicciotti, C. J.; Doshi, M.; Ben, R. N. In Recent Development in the Study of Recrystallization, Ed.: Peter, W., IntechOpen, 2013,Chapter 7. |
[102] | Carpenter, J. F.; Hansen, T. N. Proc. Natl. Acad. Sci. U. S. A. 1992, 89, 8953. |
[103] | Liang, S.; Yuan, B.; Kwon, J.-W.; Ahn, M.; Cui, X.-S.; Bang, J. K.; Kim, N.-H. Theriogenology 2016, 86, 485. |
[104] | Rubinsky, B.; Arav, A.; Mattioli, M.; DeVries, A. L. Biochem. Biophys. Res. Commun. 1990, 173, 1369. |
[105] | Prathalingam, N. S.; Holt, W. V.; Revell, S. G.; Mirczuk, S.; Fleck, R. A.; Watson, P. F. Theriogenology 2006, 66, 1894. |
[106] | Toma?s, R. M. F.; Bailey, T. L.; Hasan, M.; Gibson, M. I. Biomacromolecules 2019, 20, 3864. |
[107] | Liang, S.; Yuan, B.; Jin, Y.-X.; Zhang, J.-B.; Bang, J. K.; Kim, N.-H. Reprod. Fertil. Dev. 2017, 29, 2140. |
[108] | Chow-Shi-Yée, M.; Briard, J. G.; Grondin, M.; Averill-Bates, D. A.; Ben, R. N.; Ouellet, F. Protein Sci. 2016, 25, 974. |
[109] | Lee, S. G.; Koh, H. Y.; Lee, J. H.; Kang, S.-H.; Kim, H. J. Appl. Biochem. Biotechnol. 2012, 167, 824. |
[110] | Wen, Y.; Zhao, S. Q.; Chao, L.; Yu, H. L.; Song, C. Z.; Shen, Y. J.; Chen, H. L.; Deng, X. H. Cryobiology 2014, 69, 94. |
[111] | Six, K. R.; Lyssens, S.; Devloo, R.; Compernolle, V.; Feys, H. B. Transfusion 2019, 59, 3029. |
[112] | Knight, C. A. Nature 2000, 406, 249. |
[113] | Bar Dolev, M.; Braslavsky, I.; Davies, P. L. Annu. Rev. Biochem. 2016, 85, 515. |
[114] | Nada, H.; Furukawa, Y. Polym. J. 2012, 44, 690. |
[115] | Olijve, L. L.; Meister, K.; DeVries, A. L.; Duman, J. G.; Guo, S.; Bakker, H. J.; Voets, I. K. Proc. Natl. Acad. Sci. U. S. A. 2016, 113, 3740. |
[116] | Tyshenko, M. G.; Doucet, D.; Davies, P. L.; Walker, V. K. Nature 1997, 15, 887. |
[117] | Olsen, T. M.; Duman, J. G. J. Comp. Physiol., B 1997, 167, 105. |
[118] | Davies, P. L.; Hew, C. L. FASEB J. 1990, 4, 2460. |
[119] | Sidebottom, C.; Buckley, S.; Pudney, P.; Twigg, S.; Jarman, C.; Holt, C.; Telford, J.; McArthur, A.; Worrall, D.; Hubbard, R.; Lillford, P. Nature 2000, 406, 256. |
[120] | Berger, T.; Meister, K.; DeVries, A. L.; Eves, R.; Davies, P. L.; Drori, R. J. Am. Chem. Soc. 2019, 141, 19144. |
[121] | Celik, Y.; Drori, R.; Pertaya-Braun, N.; Altan, A.; Barton, T.; Bar-Dolev, M.; Groisman, A.; Davies, P. L.; Braslavsky, I. Proc. Natl. Acad. Sci. U. S. A. 2013, 110, 1309. |
[122] | Nada, H.; Furukawa, Y. Polym. J. 2012, 44, 690. |
[123] | Kim, H. J.; Lee, J. H.; Hur, Y. B.; Lee, C. W.; Park, S.-H.; Koo, B.-W. Mar. Drugs 2017, 15, 27. |
[124] | Liu, S. H.; Wang, W. J.; von Moos, E.; Jackman, J.; Mealing, G.; Monette, R.; Ben, R. N. Biomacromolecules 2007, 8, 1456. |
[125] | Liou, Y.; Tocilj, A.; Davies, P. L.; Jia, Z. C. Nature 2000, 406, 322. |
[126] | Graether, S. P.; Kuiper, J. K.; Gagné, S. M.; Walker, V. K.; Jia, Z. C.; Sykes, B. D.; Davies, P. L. Nature 2000, 406, 325. |
[127] | Hudait, A.; Qiu, Y.; Odendahl, N.; Molinero, V. J. Am. Chem. Soc. 2019, 141, 7887. |
[128] | Davies, P. L. Trends Biochem. Sci. 2014, 39, 548. |
[129] | Liu, K.; Wang, C. L.; Ma, J.; Shi, G. S.; Yao, X.; Fang, H. P.; Song, Y. L; Wang, J. J. Proc. Natl. Acad. Sci. U. S. A. 2016, 113, 14739. |
[130] | Jin, S. L.; Yin, L. K.; Kong, B.; Wu, S. W.; He, Z. Y.; Xue, H.; Liu, Z.; Cheng, Q.; Zhou, X.; Wang, J. J. Sci. China: Chem. 2019, 62, 909. |
[131] | He, Z. Y.; Liu, K.; Wang, J. J. Acc. Chem. Res. 2018, 51, 1082. |
[132] | Matsumoto, M.; Saito, S.; Ohmine, I. Nature 2002, 416, 409. |
[133] | Bai, G. Y.; Gao, D.; Liu, Z.; Zhou, X.; Wang, J. J. Nature 2019, 576, 437. |
[134] | Graham, B.; Fayter, A. E. R.; Houston, J. E.; Evans, R. C.; Gibson, M. I. J. Am. Chem. Soc. 2018, 140, 5682. |
[135] | Biggs, C. I.; Stubbs, C.; Graham, B.; Fayter, A. E. R.; Hasan, M.; Gibson, M. I. Macromol. Biosci. 2019, 19, e1900082. |
[136] | Drori, R.; Li, C.; Hu, C. H.; Raiteri, P.; Rohl, A. L.; Ward, M. D.; Kahr, B. J. Am. Chem. Soc. 2016, 138, 13396. |
[137] | Deville, S.; Viazzi, C.; Leloup, J.; Lasalle, A.; Guizard, C.; Maire, E.; Adrien, J.; Gremillard, L. PLoS One 2011, 6, e26474. |
[138] | Mitchell, D. E.; Clarkson, G.; Fox, D. J.; Vipond, R. A.; Scott, P.; Gibson, M. I. J. Am. Chem. Soc. 2017, 139, 9835. |
[139] | Graham, B.; Bailey, T. L.; Healey, J. R. J.; Marcellini, M.; Deville, S.; Gibson, M. I. Angew. Chem. Int. Ed. 2017, 56, 15941. |
[140] | Congdon, T.; Notman, R.; Gibson, M. I. Biomacromolecules 2013, 14, 1578. |
[141] | Matsumura, K.; Bae, J. Y.; Kim, H. H.; Hyon, S. H. Cryobiology 2011, 63, 76. |
[142] | Naullage, P. M.; Molinero, V. J. Am. Chem. Soc. 2020, 142, 4356. |
[143] | Rajan, R.; Hayashi, F.; Nagashima, T.; Matsumura, K. Biomacromolecules 2016, 17, 1882. |
[144] | Mitchell, D. E.; Lilliman, M.; Spain, S. G.; Gibson, M. I. Biomater. Sci. 2014, 2, 1787. |
[145] | Biggs, C. I.; Bailey, T. L.; Graham, B.; Stubbs, C.; Fayter, A.; Gibson, M. I. Nat. Commun. 2017, 8, 1546. |
[146] | Liu, X.; Geng, H. Y.; Sheng, N.; Wang, J. J.; Shi, G. S. J. Mater. Chem. A 2020, 8, 23555. |
[147] | Bai, G. Y.; Song, Z. P.; Geng, H. Y.; Gao, D.; Liu, K.; Wu, S. W.; Rao, W.; Guo, L. Q.; Wang, J. J. Adv. Mater. 2017, 29, 1606843. |
[148] | Bain, B. J. Medicine 2017, 45, 187. |
[149] | Li, T.; Zhao, Y.; Zhong, Q. X.; Wu, T. Biomacromolecules 2019, 20, 1667. |
[150] | Liang, H.; Mo?hler, H.; Griffiths, S.; Zou, L. J. Phys. Chem. C 2019, 124, 677. |
[151] | Zhu, W.; Guo, J.; Agola, J. O.; Croissant, J. G.; Wang, Z.; Shang, J.; Coker, E.; Motevalli, B.; Zimpel, A.; Wuttke, S.; Brinker, C. J. J. Am. Chem. Soc. 2019, 141, 7789. |
[152] | Naitana, S.; Ledda, S.; Loi, P.; Leoni, G.; Bogliolo, L.; Dattena, M.; Cappai, P. Anim. Reprod. Sci. 1997, 48, 247. |
[153] | Knight, C. A.; Wen, D.; Laursen, R. A. Cryobiology 1995, 32, 23. |
[154] | Rogers, S. C.; Dosier, L. B.; McMahon, T. J.; Zhu, H. M.; Timm, D.; Zhang, H. T.; Herbert, J.; Atallah, J.; Palmer, G. M.; Cook, A.; Ernst, M.; Prakash, J.; Terng, M.; Towfighi, P.; Doctor, R.; Said, A.; Joens, M. S.; Fitzpatrick, J. A. J.; Hanna, G.; Lin, X.; Reisz, J. A.; Nemkov, T.; D’Alessandro, A.; Doctor, A. PLoS One 2018, 13, e0209201. |
[155] | Briard, J. G.; Poisson, J. S.; Turner, T. R.; Capicciotti, C. J.; Acker, J. P.; Ben, R. N. Sci. Rep. 2015, 6, 23619. |
[156] | Sui, X. J.; Wen, C. Y.; Yang, J.; Guo, H. S.; Zhao, W. Q.; Li, Q. S.; Zhang, J. M.; Zhu, Y. N.; Zhang, L. ACS Biomater. Sci. Eng. 2019, 5, 1083. |
[157] | Mitchell, D. E.; Lovett, J. R.; Armes, S. P.; Gibson, M. I. Angew. Chem., Int. Ed. 2016, 55, 2801. |
[158] | Wang, Z. H.; Yang, B.; Chen, Z.; Liu, D.; Jing, L. H.; Gao, C.; Li, J.; He, Z. Y.; Wang, J. J. ACS Appl. Bio Mater. 2020, 3, 3785. |
[159] | Lecle?re, M.; Kwok, B. K.; Wu, L. K.; Allan, D. S.; Ben, R. N. Bioconjugate Chem. 2011, 22, 1804. |
[160] | Liu, M.; Zhang, X. Y.; Guo, H. S.; Zhu, Y. N.; Wen, C. Y.; Sui, X. J.; Yang, J.; Zhang, L. Biomacromolecules 2019, 20, 3980. |
[161] | Capicciotti, C. J.; Mancini, R. S.; Turner, T. R.; Koyama, T.; Alteen, M. G.; Doshi, M.; Inada, T.; Acker, J. P.; Ben, R. N. ACS Omega 2016, 1, 656. |
[162] | Briard, J. G.; Jahan, S.; Chandran, P.; Allan, D.; Pineault, N.; Ben, R. N. ACS Omega 2016, 1, 1010. |
[163] | William, N.; Acker, J. P. Cryobiology 2020, 97, 250. |
[164] | Poisson, J. S.; Acker, J. P.; Briard, J. G.; Meyer, J. E.; Ben, R. N. Langmuir 2018, 35, 7452. |
[165] | Yan, L.; Ren, Y. S.; Wang, X. J.; Mu, W.; Han, X. J. Acta Chim. Sinica 2020, 78, 1150. (in Chinese) |
[165] | (闫琳, 任永硕, 王雪靖, 穆韡, 韩晓军, 化学学报, 2020, 78, 1150.) |
/
〈 |
|
〉 |