Fibrin Scaffold Incorporating Platelet Lysate Enhance Follicle Survival and Angiogenesis in Cryopreserved Preantral Follicle Transplantation

Authors

  • Ali Talebi 3. School of Medicine, Shahroud University of Medical Sciences, Shahroud, Iran
  • Alireza Rajabzadeh 1. Department of Tissue Engineering and Applied Cell Science, School of Advanced Technologies in Medicine, Tehran University of Medical Sciences, Tehran, Iran
  • Fatemeh Jahanpeyma 2. Department of Medical Biotechnology, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran
  • Faezeh Moradi 4. Department of Tissue Engineering, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran
  • Hussein Eimani 6. Department of Embryology, Reproductive Biomedicine Research Center, Royan Institute for Reproductive Biomedicine, ACECR, Tehran, Iran
  • Amir Ali Hamidieh 5. Pediatric Stem Cell Transplant Department, Children’s Medical center, Tehran University of Medical Sciences, Tehran, Iran

DOI:

https://doi.org/10.31661/gmj.v9i.1558

Keywords:

Ovarian Follicle; Cryopreservation; Tissue Scaffolds; Fibrin

Abstract

Background: Transplantation of cryopreserved follicles can be regarded as a promising strategy for preserving fertility in cancer patients under chemotherapy and radiotherapy by reducing the risk of cancer recurrence. The present study aimed to evaluate whether fibrin hydrogel supplemented with platelet lysate (PL) could be applied to enhance follicular survival, growth, and angiogenesis in cryopreserved preantral follicle grafts. Materials and Methods: Preantral follicles were extracted from 15 four-week-old NMRI mice, cryopreserved by cryotop method, and encapsulated in fibrin-platelet lysate for subsequent heterotopic (subcutaneous) auto-transplantation into the neck. Transplants were assessed in three groups including fresh follicles in fibrin-15%PL, cryopreserved follicles in fibrin-15%PL, and cryopreserved follicles in fibrin-0% PL. Two weeks after transplantation, histological, and immunohistochemistry (CD31) analysis were applied to evaluate follicle morphology, survival rate, and vascular formation, respectively. Results: Based on the results, fibrin-15% PL significantly increased neovascularization and survival rate (SR) both in cryopreserved (SR=66.96%) and fresh follicle (SR=90.8%) grafts, compared to PL-less fibrin cryopreserved transplants (SR=28.46%). The grafts supplemented with PL included a significantly higher percentage of preantral and antral follicles. Also, no significant difference was observed in the percentage of preantral follicles between cryopreserved and fresh grafts of fibrin-15% PL. However, a significantly lower (P=0.03) percentage of follicles (23.37%) increased to the antral stage in cryopreserved grafts of fibrin-15%PL, compared to fresh grafts (35.01%). Conclusion: The findings demonstrated that fibrin-PL matrix could be a promising strategy to improve cryopreserved follicle transplantation and preserve fertility in cancer patients at the risk of ovarian failure. [GMJ.2020;9:e1558]

References

Luyckx V, Dolmans M-M, Vanacker J, Legat C, Moya CF, Donnez J, et al. A new step toward the artificial ovary: survival and proliferation of isolated murine follicles after autologous transplantation in a fibrin scaffold. Fertil Steril. 2014;101(4):1149-56. https://doi.org/10.1016/j.fertnstert.2013.12.025PMid:24462059 Kniazeva E, Hardy A, Boukaidi S, Woodruff T, Jeruss J, Shea L. Primordial follicle transplantation within designer biomaterial grafts produce live births in a mouse infertility model. Sci Rep. 2015;5:17709. https://doi.org/10.1038/srep17709PMid:26633657 PMCid:PMC4668556 Oktay K. Fertility preservation in cancer patients. LWW; 2017. https://doi.org/10.1097/01.COT.0000513308.74211.af Vanacker J, Luyckx V, Dolmans M-M, Des Rieux A, Jaeger J, Van Langendonckt A et al. Transplantation of an alginate-matrigel matrix containing isolated ovarian cells: first step in developing a biodegradable scaffold to transplant isolated preantral follicles and ovarian cells. Biomaterials. 2012;33(26):6079-85. https://doi.org/10.1016/j.biomaterials.2012.05.015PMid:22658800 Xu M, Banc A, Woodruff TK, Shea LD. Secondary follicle growth and oocyte maturation by culture in alginate hydrogel following cryopreservation of the ovary or individual follicles. Biotechnol Bioeng. 2009;103(2):378-86. https://doi.org/10.1002/bit.22250PMid:19191350 PMCid:PMC2778231 Itoh T, Kacchi M, Abe H, Sendai Y, Hoshi H. Growth, antrum formation, and estradiol production of bovine preantral follicles cultured in a serum-free medium. Biol Reprod. 2002;67(4):1099-105. https://doi.org/10.1095/biolreprod67.4.1099PMid:12297524 Liu J, Van der Elst J, Van den Broecke R, Dhont M. Live offspring by in vitro fertilization of oocytes from cryopreserved primordial mouse follicles after sequential in vivo transplantation and in vitro maturation. Biol Reprod. 2001;64(1):171-8. https://doi.org/10.1095/biolreprod64.1.171PMid:11133672 Eppig JJ. Maintenance of meiotic arrest and the induction of oocyte maturation in mouse oocyte-granulosa cell complexes developed in vitro from preantral follicles. Biol Reprod. 1991;45(6):824-30. https://doi.org/10.1095/biolreprod45.6.824PMid:1666849 Magalhães D, Duarte A, Araújo V, Brito I, Soares T, Lima I et al. In vitro production of a caprine embryo from a preantral follicle cultured in media supplemented with growth hormone. Theriogenology. 2011;75(1):182-8. https://doi.org/10.1016/j.theriogenology.2010.08.004PMid:20875671 Abir R, Franks S, Mobberley MA, Moore PA, Margara RA, Winston RM. Mechanical isolation and in vitro growth of preantral and small antral human follicles. Fertil Steril. 1997;68(4):682-8. https://doi.org/10.1016/S0015-0282(97)00264-1 Wu J, Emery BR, Carrell DT. In vitro growth, maturation, fertilization, and embryonic development of oocytes from porcine preantral follicles. Biol Reprod. 2001;64(1):375-81. https://doi.org/10.1095/biolreprod64.1.375PMid:11133696 Rajabzadeh AR, Eimani H, Koochesfahani HM, Shahvardi A-H, Fathi R. Morphological study of isolated ovarian preantral follicles using fibrin gel plus platelet lysate after subcutaneous transplantation. Cell J. 2015;17(1):145. Perka C, Schultz O, Spitzer R-S, Lindenhayn K, Burmester G-R, Sittinger M. Segmental bone repair by tissue-engineered periosteal cell transplants with bioresorbable fleece and fibrin scaffolds in rabbits. Biomaterials. 2000;21(11):1145-53. https://doi.org/10.1016/S0142-9612(99)00280-X Bensaıd W, Triffitt J, Blanchat C, Oudina K, Sedel L, Petite H. A biodegradable fibrin scaffold for mesenchymal stem cell transplantation. Biomaterials. 2003;24(14):2497-502. https://doi.org/10.1016/S0142-9612(02)00618-X Ronfard V, Rives J-M, Neveux Y, Carsin H, Barrandon Y. Long-term regeneration of human epidermis on third degree burns transplanted with autologous cultured epithelium grown on a fibrin matrix1, 2. Transplantation. 2000;70(11):1588-98. https://doi.org/10.1097/00007890-200012150-00009PMid:11152220 Rama P, Bonini S, Lambiase A, Golisano O, Paterna P, De Luca M, et al. Autologous fibrin-cultured limbal stem cells permanently restore the corneal surface of patients with total limbal stem cell deficiency1. Transplantation. 2001;72(9):1478-85. https://doi.org/10.1097/00007890-200111150-00002PMid:11707733 Chen S-J, Chang C-M, Tsai S-K, Chang Y-L, Chou S-J, Huang S-S et al. Functional improvement of focal cerebral ischemia injury by subdural transplantation of induced pluripotent stem cells with fibrin glue. Stem Cells Dev. 2010;19(11):1757-67. https://doi.org/10.1089/scd.2009.0452PMid:20192839 Zhang G, Hu Q, Braunlin EA, Suggs LJ, Zhang J. Enhancing efficacy of stem cell transplantation to the heart with a PEGylated fibrin biomatrix. Tissue Eng Part A. 2008;14(6):1025-36. https://doi.org/10.1089/ten.tea.2007.0289PMid:18476809 Vaquero J, Otero L, Bonilla C, Aguayo C, Rico MA, Rodriguez A, et al. Cell therapy with bone marrow stromal cells after intracerebral hemorrhage: impact of platelet-rich plasma scaffolds. Cytotherapy. 2013;15(1):33-43. https://doi.org/10.1016/j.jcyt.2012.10.005PMid:23260084 Burnouf T, Strunk D, Koh MB, Schallmoser K. Human platelet lysate: replacing fetal bovine serum as a gold standard for human cell propagation? Biomaterials. 2016;76:371-87. https://doi.org/10.1016/j.biomaterials.2015.10.065PMid:26561934 Liu B, Tan X-Y, Liu Y-P, Xu X-F, Li L, Xu H-Y, et al. The adjuvant use of stromal vascular fraction and platelet-rich fibrin for autologous adipose tissue transplantation. Tissue Eng Part C Methods. 2012;19(1):1-14. https://doi.org/10.1089/ten.tec.2012.0126PMid:22681647 Hasegawa A, Mochida N, Ogasawara T, Koyama K. Pup birth from mouse oocytes in preantral follicles derived from vitrified and warmed ovaries followed by in vitro growth, in vitro maturation, and in vitro fertilization. Fertil Steril. 2006;86(4):1182-92. https://doi.org/10.1016/j.fertnstert.2005.12.082PMid:16963048 Israely T, Dafni H, Granot D, Nevo N, Tsafriri A, Neeman M. Vascular remodeling and angiogenesis in ectopic ovarian transplants: a crucial role of pericytes and vascular smooth muscle cells in maintenance of ovarian grafts. Biol Rep. 2003;68(6):2055-64. https://doi.org/10.1095/biolreprod.102.011734PMid:12606340 Gumus E, Kaloglu C, Sari I, Yilmaz M, Cetin A. Effects of vitrification and transplantation on follicular development and expression of EphrinB1 and PDGFA in mouse ovaries. Cryobiology. 2018;80:101-13. https://doi.org/10.1016/j.cryobiol.2017.11.006PMid:29154909 Demirci B, Lornage J, Salle B, Frappart L, Franck M, Guerin JF. Follicular viability and morphology of sheep ovaries after exposure to cryoprotectant and cryopreservation with different freezing protocols. Fertil Steril. 2001;75(4):754-62. https://doi.org/10.1016/S0015-0282(00)01787-8 Chiti MC, Dolmans M-M, Mortiaux L, Zhuge F, Ouni E, Shahri PAK, et al. A novel fibrin-based artificial ovary prototype resembling human ovarian tissue in terms of architecture and rigidity. J Assist Reprod Genet. 2018;35(1):41-8. https://doi.org/10.1007/s10815-017-1091-3PMid:29236205 PMCid:PMC5758477 Rios PD, Kniazeva E, Lee HC, Xiao S, Oakes RS, Saito E, et al. Retrievable hydrogels for ovarian follicle transplantation and oocyte collection. Biotechnol Bioeng. 2018; 115(8):2075-2086 https://doi.org/10.1002/bit.26721PMid:29704433 PMCid:PMC6045426 Shikanov A, Xu M, Woodruff TK, Shea LD. A method for ovarian follicle encapsulation and culture in a proteolytically degradable 3 dimensional system. J Vis Exp. 2011(49). https://doi.org/10.3791/2695PMid:21445043 PMCid:PMC3197327 Johnson PJ, Parker SR, Sakiyama-Elbert SE. Fibrin-based tissue engineering scaffolds enhance neural fiber sprouting and delay the accumulation of reactive astrocytes at the lesion in a subacute model of spinal cord injury. J Biomed Mater Res A. 2010;92(1):152-63. https://doi.org/10.1002/jbm.a.32343PMid:19165795 PMCid:PMC2787862 Kolehmainen K, Willerth SM. Preparation of 3D fibrin scaffolds for stem cell culture applications. J Vis Exp. 2012(61). https://doi.org/10.3791/3641PMid:22415575 PMCid:PMC3399464 Shikanov A, Zhang Z, Xu M, Smith RM, Rajan A, Woodruff TK, et al. Fibrin encapsulation and vascular endothelial growth factor delivery promotes ovarian graft survival in mice. Tissue Eng Part A. 2011;17(23-24):3095-104. https://doi.org/10.1089/ten.tea.2011.0204PMid:21740332 PMCid:PMC3226061 Park CH, Oh J-H, Jung H-M, Choi Y, Rahman SU, Kim S, et al. Effects of the incorporation of ε-aminocaproic acid/chitosan particles to fibrin on cementoblast differentiation and cementum regeneration. Acta Biomater. 2017;61:134-43. https://doi.org/10.1016/j.actbio.2017.07.039PMid:28764948 Xu J, Lawson M, Yeoman R, Molskness T, Ting A, Stouffer R, et al. Fibrin promotes development and function of macaque primary follicles during encapsulated three-dimensional culture. Hum Reprod. 2013;28(8):2187-200. https://doi.org/10.1093/humrep/det093PMid:23608357 PMCid:PMC3712659 Grynberg M, Poulain M, Sebag-Peyrelevade S, le Parco S, Fanchin R, Frydman N. Ovarian tissue and follicle transplantation as an option for fertility preservation. Fertil Steril. 2012;97(6):1260-8. https://doi.org/10.1016/j.fertnstert.2012.04.042PMid:22656306 Sadr SZ, Fatehi R, Maroufizadeh S, Amorim CA, Ebrahimi B. Utilizing Fibrin-Alginate and Matrigel-Alginate for Mouse Follicle Development in Three-Dimensional Culture Systems. Biopreserv Biobank. 2018;16(2):120-7. https://doi.org/10.1089/bio.2017.0087PMid:29363997 Shikanov A, Xu M, Woodruff TK, Shea LD. Interpenetrating fibrin-alginate matrices for in vitro ovarian follicle development. Biomaterials. 2009;30(29):5476-85. https://doi.org/10.1016/j.biomaterials.2009.06.054PMid:19616843 PMCid:PMC2906124 Brito I, Silva G, Sales A, Lobo C, Rodrigues G, Sousa R, et al. Fibrin-alginate hydrogel supports steroidogenesis, in vitro maturation of oocytes and parthenotes production from caprine preantral follicles cultured in group. Reprod Domest Anim. 2016;51(6):997-1009. https://doi.org/10.1111/rda.12779PMid:27650787 Trapphoff T, El Hajj N, Zechner U, Haaf T, Eichenlaub-Ritter U. DNA integrity, growth pattern, spindle formation, chromosomal constitution and imprinting patterns of mouse oocytes from vitrified pre-antral follicles. Hum Reprod. 2010;25(12):3025-42. https://doi.org/10.1093/humrep/deq278PMid:20940142 Gassling V, Douglas T, Warnke PH, Açil Y, Wiltfang J, Becker ST. Platelet-rich fibrin membranes as scaffolds for periosteal tissue engineering. Clin Oral Implants Res. 2010;21(5):543-9. https://doi.org/10.1111/j.1600-0501.2009.01900.xPMid:20443805 Sykes J, Kuiper J, Richardson J, Wright K, Kuiper N. Impact of human platelet lysate on the expansion and chondrogenic capacity of cultured human chondrocytes for cartilage cell therapy. Osteoarthr. Cartil. 2018;26:S103. https://doi.org/10.1016/j.joca.2018.02.221 Lee KI, Olmer M, Baek J, D'Lima DD, Lotz MK. Platelet-derived growth factor-coated decellularized meniscus scaffold for integrative healing of meniscus tears. Acta Biomater. 2018;126-134 https://doi.org/10.1016/j.actbio.2018.06.021PMid:29908335 PMCid:PMC6090559 Samberg M, Stone II R, Natesan S, Kowalczewski A, Becerra S, Wrice N, et al. Platelet Rich Plasma Hydrogels Promote in vitro and in vivo Angiogenic Potential of Adipose-Derived Stem Cells. Acta biomater. 2019;87:76-87 https://doi.org/10.1016/j.actbio.2019.01.039PMid:30665019 Bindal P, Gnanasegaran N, Bindal U, Haque N, Ramasamy TS, Chai WL, et al. Angiogenic effect of platelet-rich concentrates on dental pulp stem cells in inflamed microenvironment. Clin Oral Investig. 2019;28:1-11. https://doi.org/10.1007/s00784-019-02811-5PMid:30687907 Kuwayama M. Highly efficient vitrification for cryopreservation of human oocytes and embryos: the Cryotop method. Theriogenology. 2007;67(1):73-80. https://doi.org/10.1016/j.theriogenology.2006.09.014PMid:17055564 Castelló D, Cobo A, Mestres E, Garcia M, Vanrell I, Remohí JA et al. Pre-clinical validation of a closed surface system (Cryotop SC) for the vitrification of oocytes and embryos in the mouse model. Cryobiology. 2018;81:107-16. https://doi.org/10.1016/j.cryobiol.2018.02.002PMid:29475071 Bottrel M, Ortiz I, Pereira B, Díaz-Jiménez M, Hidalgo M, Consuegra C et al. Cryopreservation of donkey embryos by the cryotop method: Effect of developmental stage, embryo quality, diameter and age of embryos. Theriogenology. 2018. https://doi.org/10.1016/j.theriogenology.2018.11.011PMid:30476757 Rajabi Z, Yazdekhasti H, Mugahi SMHN, Abbasi M, Kazemnejad S, Shirazi A, et al. Mouse preantral follicle growth in 3D co-culture system using human menstrual blood mesenchymal stem cell. Reprod Biol. 2018;18(1):122-31. https://doi.org/10.1016/j.repbio.2018.02.001PMid:29454805 Desai N, AbdelHafez F, Ali MY, Sayed EH, Abu-Alhassan AM, Falcone T, et al. Mouse ovarian follicle cryopreservation using vitrification or slow programmed cooling: Assessment of in vitro development, maturation, ultra-structure and meiotic spindle organization. J Obstet Gynaecol Res. 2011;37(1):1-12. https://doi.org/10.1111/j.1447-0756.2010.01215.xPMid:20731766 Taghavi SA, Valojerdi MR, Moghadam MF, Ebrahimi B. Vitrification of mouse preantral follicles versus slow freezing: Morphological and apoptosis evaluation. Animal Sci. J. 2015;86(1):37-44. https://doi.org/10.1111/asj.12244PMid:25041991 Bao R-M, Yamasaka E, Moniruzzaman M, Hamawaki A, Yoshikawa M, Miyano T. Development of vitrified bovine secondary and primordial follicles in xenografts. Theriogenology. 2010;74(5):817-27. https://doi.org/10.1016/j.theriogenology.2010.04.006PMid:20570334

Published

2020-07-08

How to Cite

Talebi, A., Rajabzadeh, A., Jahanpeyma, F., Moradi, F., Eimani, H., & Hamidieh, A. A. (2020). Fibrin Scaffold Incorporating Platelet Lysate Enhance Follicle Survival and Angiogenesis in Cryopreserved Preantral Follicle Transplantation: . Galen Medical Journal, 9, e1558. https://doi.org/10.31661/gmj.v9i.1558

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