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

Alireza Rajabzadeh, Fatemeh Jahanpeyma, Ali Talebi, Faezeh Moradi, Hussein Eimani

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]

Ovarian Follicle; Cryopreservation; Tissue Scaffolds; Fibrin
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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.2013.12.025

PMid: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/srep17709

PMid: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.2012.05.015

PMid: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.22250

PMid: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/biolreprod67.4.1099

PMid: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/biolreprod64.1.171

PMid: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/biolreprod45.6.824

PMid: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.2010.08.004

PMid: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/biolreprod64.1.375

PMid: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/10.1097/00007890-200012150-00009

PMid: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/10.1097/00007890-200111150-00002

PMid: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.2009.0452

PMid: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.2007.0289

PMid: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.2012.10.005

PMid: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.2015.10.065

PMid: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.2012.0126

PMid: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.2005.12.082

PMid: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.102.011734

PMid: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.2017.11.006

PMid: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/s10815-017-1091-3

PMid: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.26721

PMid: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/10.3791/2695

PMid: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.32343

PMid: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/10.3791/3641

PMid: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.2011.0204

PMid: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.2017.07.039

PMid: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/det093

PMid: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.2012.04.042

PMid: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.2017.0087

PMid: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.2009.06.054

PMid: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.12779

PMid: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/deq278

PMid: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.x

PMid: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.2018.06.021

PMid: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.2019.01.039

PMid: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/s00784-019-02811-5

PMid: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.2006.09.014

PMid: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.2018.02.002

PMid: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.2018.11.011

PMid: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.2018.02.001

PMid: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.x

PMid: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.12244

PMid: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.2010.04.006

PMid:20570334

DOI: http://dx.doi.org/10.31661/gmj.v9i0.1558

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