Skip to main content
Top
Published in: Journal of Assisted Reproduction and Genetics 10/2013

01-10-2013 | Fertility Preservation

VEGF and bFGF increase survival of xenografted human ovarian tissue in an experimental rabbit model

Authors: Lin Wang, Ying-fen Ying, Yin-luan Ouyang, Jing-fen Wang, Jian Xu

Published in: Journal of Assisted Reproduction and Genetics | Issue 10/2013

Login to get access

Abstract

Purpose

The aim of this study is to determine whether vascular endothelial growth factor (VEGF) and basic fibroblast growth factor (bFGF) could increase the survival of xenografted human ovarian tissue in an experimental rabbit model.

Methods

Fresh human ovarian tissue was xenotransplanted into the back muscle of 25 castrated female New Zealand rabbits for 6 weeks with the immunosuppression of FTY720 (2 mg/kg/d). Rabbits were randomly divided into five experimental groups: (A) graft and host treatment with VEGF (50 ng/ml); (B) graft and host treatment with bFGF (100 ng/ml); (C) graft and host treatment with VEGF(50 ng/ml) + bFGF (100 ng/ml); (D) graft and host treatment with normal saline; (E) control group, no treatment. 4 weeks after transplantation, human menopausal gonadotropin (HMG) 10 IU was administered every second day in group A, group B, group C and group D for 2 weeks. Graft survival was assessed by graft recovery rate, histological analysis, immunohistochemical staining for CD31 and Ki-67expression, TUNEL assay.

Results

After 6 weeks of grafting, the number of CD31-positive stained cells increased significantly in group A, group B and group C compared to the control group. All groups showed strong Ki-67 immunostaining in ovarian stroma. Only one rabbit in group C retained the grafts’ follicles. Grafting resulted in relative lower fibrosis in group A and group C compared to the control group. Apoptosis was significantly lower in group C compared to the control group.

Conclusions

Fresh human ovarian cortex grafted into the back muscle of rabbit can sustain part of ovarian tissue function with the immunosuppression of FTY720, although follicle number diminishes significantly after grafting. The administration of VEGF and bFGF, especially the combination of them, may trigger angiogenesis, reduce apoptosis and fibrosis, increase survival in transplanted human ovarian tissue.
Literature
1.
go back to reference McLaren JF, Bates GW. Fertility preservation in women of reproductive age with cancer. Am J Obstet Gynecol. 2012;207:455–62.PubMedCrossRef McLaren JF, Bates GW. Fertility preservation in women of reproductive age with cancer. Am J Obstet Gynecol. 2012;207:455–62.PubMedCrossRef
2.
go back to reference Lee SJ, Schover LR, Partridge AH, Patrizio P, Wallace WH, Hagerty K, et al. American Society of Clinical Oncology recommendations on fertility preservation in cancer patients. J Clin Oncol. 2006;24:2917–31.PubMedCrossRef Lee SJ, Schover LR, Partridge AH, Patrizio P, Wallace WH, Hagerty K, et al. American Society of Clinical Oncology recommendations on fertility preservation in cancer patients. J Clin Oncol. 2006;24:2917–31.PubMedCrossRef
3.
go back to reference Baka SG, Toth TL, Veeck LL, Jones HJ, Muasher SJ, Lanzendorf SE. Evaluation of the spindle apparatus of in-vitro matured human oocytes following cryopreservation. Hum Reprod. 1995;10:1816–20.PubMed Baka SG, Toth TL, Veeck LL, Jones HJ, Muasher SJ, Lanzendorf SE. Evaluation of the spindle apparatus of in-vitro matured human oocytes following cryopreservation. Hum Reprod. 1995;10:1816–20.PubMed
4.
go back to reference Silber SJ. Ovary cryopreservation and transplantation for fertility preservation. Mol Hum Reprod. 2012;18:59–67.PubMedCrossRef Silber SJ. Ovary cryopreservation and transplantation for fertility preservation. Mol Hum Reprod. 2012;18:59–67.PubMedCrossRef
5.
go back to reference Donnez J, Jadoul P, Pirard C, Hutchings G, Demylle D, Squifflet J, et al. Live birth after transplantation of frozen-thawed ovarian tissue after bilateral oophorectomy for benign disease. Fertil Steril. 2012;98:720–5.PubMedCrossRef Donnez J, Jadoul P, Pirard C, Hutchings G, Demylle D, Squifflet J, et al. Live birth after transplantation of frozen-thawed ovarian tissue after bilateral oophorectomy for benign disease. Fertil Steril. 2012;98:720–5.PubMedCrossRef
6.
go back to reference Revelli A, Marchino G, Dolfin E, Molinari E, Delle PL, Salvagno F, et al. Live birth after orthotopic grafting of autologous cryopreserved ovarian tissue and spontaneous conception in Italy. Fertil Steril. 2013;99:227–30.PubMedCrossRef Revelli A, Marchino G, Dolfin E, Molinari E, Delle PL, Salvagno F, et al. Live birth after orthotopic grafting of autologous cryopreserved ovarian tissue and spontaneous conception in Italy. Fertil Steril. 2013;99:227–30.PubMedCrossRef
7.
go back to reference Dolmans MM, Marinescu C, Saussoy P, Van Langendonckt A, Amorim C, Donnez J. Reimplantation of cryopreserved ovarian tissue from patients with acute lymphoblastic leukemia is potentially unsafe. Blood. 2010;116:2908–14.PubMedCrossRef Dolmans MM, Marinescu C, Saussoy P, Van Langendonckt A, Amorim C, Donnez J. Reimplantation of cryopreserved ovarian tissue from patients with acute lymphoblastic leukemia is potentially unsafe. Blood. 2010;116:2908–14.PubMedCrossRef
8.
go back to reference Nugent D, Newton H, Gallivan L, Gosden RG. Protective effect of vitamin E on ischaemia-reperfusion injury in ovarian grafts. J Reprod Fertil. 1998;114:341–6.PubMedCrossRef Nugent D, Newton H, Gallivan L, Gosden RG. Protective effect of vitamin E on ischaemia-reperfusion injury in ovarian grafts. J Reprod Fertil. 1998;114:341–6.PubMedCrossRef
9.
go back to reference Israely T, Dafni H, Nevo N, Tsafriri A, Neeman M. Angiogenesis in ectopic ovarian xenotransplantation: multiparameter characterization of the neovasculature by dynamic contrast-enhanced MRI. Magn Reson Med. 2004;52:741–50.PubMedCrossRef Israely T, Dafni H, Nevo N, Tsafriri A, Neeman M. Angiogenesis in ectopic ovarian xenotransplantation: multiparameter characterization of the neovasculature by dynamic contrast-enhanced MRI. Magn Reson Med. 2004;52:741–50.PubMedCrossRef
10.
go back to reference Van Eyck AS, Jordan BF, Gallez B, Heilier JF, Van Langendonckt A, Donnez J. Electron paramagnetic resonance as a tool to evaluate human ovarian tissue reoxygenation after xenografting. Fertil Steril. 2009;92:374–81.PubMedCrossRef Van Eyck AS, Jordan BF, Gallez B, Heilier JF, Van Langendonckt A, Donnez J. Electron paramagnetic resonance as a tool to evaluate human ovarian tissue reoxygenation after xenografting. Fertil Steril. 2009;92:374–81.PubMedCrossRef
11.
go back to reference Demeestere I, Simon P, Emiliani S, Delbaere A, Englert Y. Orthotopic and heterotopic ovarian tissue transplantation. Hum Reprod Update. 2009;15:649–65.PubMedCrossRefPubMedCentral Demeestere I, Simon P, Emiliani S, Delbaere A, Englert Y. Orthotopic and heterotopic ovarian tissue transplantation. Hum Reprod Update. 2009;15:649–65.PubMedCrossRefPubMedCentral
12.
go back to reference Zhou XH, Wu YJ, Shi J, Xia YX, Zheng SS. Cryopreservation of human ovarian tissue: comparison of novel direct cover vitrification and conventional vitrification. Cryobiology. 2010;60:101–5.PubMedCrossRef Zhou XH, Wu YJ, Shi J, Xia YX, Zheng SS. Cryopreservation of human ovarian tissue: comparison of novel direct cover vitrification and conventional vitrification. Cryobiology. 2010;60:101–5.PubMedCrossRef
13.
go back to reference Hazzard TM, Stouffer RL. Angiogenesis in ovarian follicular and luteal development. Baillieres Best Pract Res Clin Obstet Gynaecol. 2000;14:883–900.PubMedCrossRef Hazzard TM, Stouffer RL. Angiogenesis in ovarian follicular and luteal development. Baillieres Best Pract Res Clin Obstet Gynaecol. 2000;14:883–900.PubMedCrossRef
14.
go back to reference Kaczmarek MM, Schams D, Ziecik AJ. Role of vascular endothelial growth factor in ovarian physiology - an overview. Reprod Biol. 2005;5:111–36.PubMed Kaczmarek MM, Schams D, Ziecik AJ. Role of vascular endothelial growth factor in ovarian physiology - an overview. Reprod Biol. 2005;5:111–36.PubMed
15.
go back to reference Ravindranath N, Little-Ihrig L, Phillips HS, Ferrara N, Zeleznik AJ. Vascular endothelial growth factor messenger ribonucleic acid expression in the primate ovary. Endocrinology. 1992;131:254–60.PubMedCrossRef Ravindranath N, Little-Ihrig L, Phillips HS, Ferrara N, Zeleznik AJ. Vascular endothelial growth factor messenger ribonucleic acid expression in the primate ovary. Endocrinology. 1992;131:254–60.PubMedCrossRef
16.
go back to reference Seli E, Zeyneloglu HB, Senturk LM, Bahtiyar OM, Olive DL, Arici A. Basic fibroblast growth factor: peritoneal and follicular fluid levels and its effect on early embryonic development. Fertil Steril. 1998;69:1145–8.PubMedCrossRef Seli E, Zeyneloglu HB, Senturk LM, Bahtiyar OM, Olive DL, Arici A. Basic fibroblast growth factor: peritoneal and follicular fluid levels and its effect on early embryonic development. Fertil Steril. 1998;69:1145–8.PubMedCrossRef
17.
go back to reference Reynolds LP, Redmer DA. Expression of the angiogenic factors, basic fibroblast growth factor and vascular endothelial growth factor, in the ovary. J Anim Sci. 1998;76:1671–81.PubMed Reynolds LP, Redmer DA. Expression of the angiogenic factors, basic fibroblast growth factor and vascular endothelial growth factor, in the ovary. J Anim Sci. 1998;76:1671–81.PubMed
18.
go back to reference Imthurn B, Cox SL, Jenkin G, Trounson AO, Shaw JM. Gonadotrophin administration can benefit ovarian tissue grafted to the body wall: implications for human ovarian grafting. Mol Cell Endocrinol. 2000;163:141–6.PubMedCrossRef Imthurn B, Cox SL, Jenkin G, Trounson AO, Shaw JM. Gonadotrophin administration can benefit ovarian tissue grafted to the body wall: implications for human ovarian grafting. Mol Cell Endocrinol. 2000;163:141–6.PubMedCrossRef
19.
go back to reference Chiba K, Yanagawa Y, Masubuchi Y, Kataoka H, Kawaguchi T, Ohtsuki M, et al. FTY720, a novel immunosuppressant, induces sequestration of circulating mature lymphocytes by acceleration of lymphocyte homing in rats. I. FTY720 selectively decreases the number of circulating mature lymphocytes by acceleration of lymphocyte homing. J Immunol. 1998;160:5037–44.PubMed Chiba K, Yanagawa Y, Masubuchi Y, Kataoka H, Kawaguchi T, Ohtsuki M, et al. FTY720, a novel immunosuppressant, induces sequestration of circulating mature lymphocytes by acceleration of lymphocyte homing in rats. I. FTY720 selectively decreases the number of circulating mature lymphocytes by acceleration of lymphocyte homing. J Immunol. 1998;160:5037–44.PubMed
20.
go back to reference Dath C, Van Eyck AS, Dolmans MM, Romeu L, Delle VL, Donnez J, et al. Xenotransplantation of human ovarian tissue to nude mice: comparison between four grafting sites. Hum Reprod. 2010;25:1734–43.PubMedCrossRef Dath C, Van Eyck AS, Dolmans MM, Romeu L, Delle VL, Donnez J, et al. Xenotransplantation of human ovarian tissue to nude mice: comparison between four grafting sites. Hum Reprod. 2010;25:1734–43.PubMedCrossRef
21.
go back to reference Meirow D, Hardan I, Dor J, Fridman E, Elizur S, Ra’Anani H, et al. Searching for evidence of disease and malignant cell contamination in ovarian tissue stored from hematologic cancer patients. Hum Reprod. 2008;23:1007–13.PubMedCrossRef Meirow D, Hardan I, Dor J, Fridman E, Elizur S, Ra’Anani H, et al. Searching for evidence of disease and malignant cell contamination in ovarian tissue stored from hematologic cancer patients. Hum Reprod. 2008;23:1007–13.PubMedCrossRef
22.
go back to reference Lotz L, Montag M, van der Ven H, von Wolff M, Mueller A, Hoffmann I, et al. Xenotransplantation of cryopreserved ovarian tissue from patients with ovarian tumors into SCID mice–no evidence of malignant cell contamination. Fertil Steril. 2011;95:2612–4.PubMedCrossRef Lotz L, Montag M, van der Ven H, von Wolff M, Mueller A, Hoffmann I, et al. Xenotransplantation of cryopreserved ovarian tissue from patients with ovarian tumors into SCID mice–no evidence of malignant cell contamination. Fertil Steril. 2011;95:2612–4.PubMedCrossRef
23.
go back to reference Chambers EL, Gosden RG, Yap C, Picton HM. In situ identification of follicles in ovarian cortex as a tool for quantifying follicle density, viability and developmental potential in strategies to preserve female fertility. Hum Reprod. 2010;25:2559–68.PubMedCrossRef Chambers EL, Gosden RG, Yap C, Picton HM. In situ identification of follicles in ovarian cortex as a tool for quantifying follicle density, viability and developmental potential in strategies to preserve female fertility. Hum Reprod. 2010;25:2559–68.PubMedCrossRef
24.
go back to reference Amorim CA, Dolmans MM, David A, Jaeger J, Vanacker J, Camboni A, et al. Vitrification and xenografting of human ovarian tissue. Fertil Steril. 2012;98:1291–8.PubMedCrossRef Amorim CA, Dolmans MM, David A, Jaeger J, Vanacker J, Camboni A, et al. Vitrification and xenografting of human ovarian tissue. Fertil Steril. 2012;98:1291–8.PubMedCrossRef
25.
go back to reference David A, Dolmans MM, Van Langendonckt A, Donnez J, Amorim CA. Immunohistochemical localization of growth factors after cryopreservation and 3 weeks’ xenotransplantation of human ovarian tissue. Fertil Steril. 2011;95:1241–6.PubMedCrossRef David A, Dolmans MM, Van Langendonckt A, Donnez J, Amorim CA. Immunohistochemical localization of growth factors after cryopreservation and 3 weeks’ xenotransplantation of human ovarian tissue. Fertil Steril. 2011;95:1241–6.PubMedCrossRef
26.
go back to reference Soleimani R, Heytens E, Oktay K. Enhancement of neoangiogenesis and follicle survival by sphingosine-1-phosphate in human ovarian tissue xenotransplants. PLoS One. 2011;6:e19475.PubMedCrossRefPubMedCentral Soleimani R, Heytens E, Oktay K. Enhancement of neoangiogenesis and follicle survival by sphingosine-1-phosphate in human ovarian tissue xenotransplants. PLoS One. 2011;6:e19475.PubMedCrossRefPubMedCentral
27.
go back to reference Friedman O, Orvieto R, Fisch B, Felz C, Freud E, Ben-Haroush A, et al. Possible improvements in human ovarian grafting by various host and graft treatments. Hum Reprod. 2012;27:474–82.PubMedCrossRef Friedman O, Orvieto R, Fisch B, Felz C, Freud E, Ben-Haroush A, et al. Possible improvements in human ovarian grafting by various host and graft treatments. Hum Reprod. 2012;27:474–82.PubMedCrossRef
28.
go back to reference Israely T, Nevo N, Harmelin A, Neeman M, Tsafriri A. Reducing ischaemic damage in rodent ovarian xenografts transplanted into granulation tissue. Hum Reprod. 2006;21:1368–79.PubMedCrossRef Israely T, Nevo N, Harmelin A, Neeman M, Tsafriri A. Reducing ischaemic damage in rodent ovarian xenografts transplanted into granulation tissue. Hum Reprod. 2006;21:1368–79.PubMedCrossRef
29.
go back to reference Donnez J, Dolmans MM, Demylle D, Jadoul P, Pirard C, Squifflet J, et al. Livebirth after orthotopic transplantation of cryopreserved ovarian tissue. Lancet. 2004;364:1405–10.PubMedCrossRef Donnez J, Dolmans MM, Demylle D, Jadoul P, Pirard C, Squifflet J, et al. Livebirth after orthotopic transplantation of cryopreserved ovarian tissue. Lancet. 2004;364:1405–10.PubMedCrossRef
30.
go back to reference Donnez J, Dolmans MM, Demylle D, Jadoul P, Pirard C, Squifflet J, et al. Restoration of ovarian function after orthotopic (intraovarian and periovarian) transplantation of cryopreserved ovarian tissue in a woman treated by bone marrow transplantation for sickle cell anaemia: case report. Hum Reprod. 2006;21:183–8.PubMedCrossRef Donnez J, Dolmans MM, Demylle D, Jadoul P, Pirard C, Squifflet J, et al. Restoration of ovarian function after orthotopic (intraovarian and periovarian) transplantation of cryopreserved ovarian tissue in a woman treated by bone marrow transplantation for sickle cell anaemia: case report. Hum Reprod. 2006;21:183–8.PubMedCrossRef
31.
go back to reference Abir R, Fisch B, Jessel S, Felz C, Ben-Haroush A, Orvieto R. Improving posttransplantation survival of human ovarian tissue by treating the host and graft. Fertil Steril. 2011;95:1205–10.PubMedCrossRef Abir R, Fisch B, Jessel S, Felz C, Ben-Haroush A, Orvieto R. Improving posttransplantation survival of human ovarian tissue by treating the host and graft. Fertil Steril. 2011;95:1205–10.PubMedCrossRef
32.
go back to reference Yang H, Lee HH, Lee HC, Ko DS, Kim SS. Assessment of vascular endothelial growth factor expression and apoptosis in the ovarian graft: can exogenous gonadotropin promote angiogenesis after ovarian transplantation? Fertil Steril. 2008;90:1550–8.PubMedCrossRef Yang H, Lee HH, Lee HC, Ko DS, Kim SS. Assessment of vascular endothelial growth factor expression and apoptosis in the ovarian graft: can exogenous gonadotropin promote angiogenesis after ovarian transplantation? Fertil Steril. 2008;90:1550–8.PubMedCrossRef
33.
go back to reference Nilsson E, Parrott JA, Skinner MK. Basic fibroblast growth factor induces primordial follicle development and initiates folliculogenesis. Mol Cell Endocrinol. 2001;175:123–30.PubMedCrossRef Nilsson E, Parrott JA, Skinner MK. Basic fibroblast growth factor induces primordial follicle development and initiates folliculogenesis. Mol Cell Endocrinol. 2001;175:123–30.PubMedCrossRef
34.
go back to reference Lund EL, Thorsen C, Pedersen MW, Junker N, Kristjansen PE. Relationship between vessel density and expression of vascular endothelial growth factor and basic fibroblast growth factor in small cell lung cancer in vivo and in vitro. Clin Cancer Res. 2000;6:4287–91.PubMed Lund EL, Thorsen C, Pedersen MW, Junker N, Kristjansen PE. Relationship between vessel density and expression of vascular endothelial growth factor and basic fibroblast growth factor in small cell lung cancer in vivo and in vitro. Clin Cancer Res. 2000;6:4287–91.PubMed
35.
go back to reference Skinner MK. Regulation of primordial follicle assembly and development. Hum Reprod Update. 2005;11:461–71.PubMedCrossRef Skinner MK. Regulation of primordial follicle assembly and development. Hum Reprod Update. 2005;11:461–71.PubMedCrossRef
36.
go back to reference Van Eyck AS, Bouzin C, Feron O, Romeu L, Van Langendonckt A, Donnez J, et al. Both host and graft vessels contribute to revascularization of xenografted human ovarian tissue in a murine model. Fertil Steril. 2010;93:1676–85.PubMedCrossRef Van Eyck AS, Bouzin C, Feron O, Romeu L, Van Langendonckt A, Donnez J, et al. Both host and graft vessels contribute to revascularization of xenografted human ovarian tissue in a murine model. Fertil Steril. 2010;93:1676–85.PubMedCrossRef
37.
go back to reference Tille JC, Wood J, Mandriota SJ, Schnell C, Ferrari S, Mestan J, et al. Vascular endothelial growth factor (VEGF) receptor-2 antagonists inhibit VEGF- and basic fibroblast growth factor-induced angiogenesis in vivo and in vitro. J Pharmacol Exp Ther. 2001;299:1073–85.PubMed Tille JC, Wood J, Mandriota SJ, Schnell C, Ferrari S, Mestan J, et al. Vascular endothelial growth factor (VEGF) receptor-2 antagonists inhibit VEGF- and basic fibroblast growth factor-induced angiogenesis in vivo and in vitro. J Pharmacol Exp Ther. 2001;299:1073–85.PubMed
38.
go back to reference Stavri GT, Zachary IC, Baskerville PA, Martin JF, Erusalimsky JD. Basic fibroblast growth factor upregulates the expression of vascular endothelial growth factor in vascular smooth muscle cells. Synergistic interaction with hypoxia. Circulation. 1995;92:11–4.PubMedCrossRef Stavri GT, Zachary IC, Baskerville PA, Martin JF, Erusalimsky JD. Basic fibroblast growth factor upregulates the expression of vascular endothelial growth factor in vascular smooth muscle cells. Synergistic interaction with hypoxia. Circulation. 1995;92:11–4.PubMedCrossRef
39.
go back to reference Mattern J, Koomagi R, Volm M. Coexpression of VEGF and bFGF in human epidermoid lung carcinoma is associated with increased vessel density. Anticancer Res. 1997;17:2249–52.PubMed Mattern J, Koomagi R, Volm M. Coexpression of VEGF and bFGF in human epidermoid lung carcinoma is associated with increased vessel density. Anticancer Res. 1997;17:2249–52.PubMed
40.
go back to reference 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;17:3095–104.PubMedCrossRefPubMedCentral 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;17:3095–104.PubMedCrossRefPubMedCentral
41.
go back to reference Laschke MW, Menger MD, Vollmar B. Ovariectomy improves neovascularization and microcirculation of freely transplanted ovarian follicles. J Endocrinol. 2002;172:535–44.PubMedCrossRef Laschke MW, Menger MD, Vollmar B. Ovariectomy improves neovascularization and microcirculation of freely transplanted ovarian follicles. J Endocrinol. 2002;172:535–44.PubMedCrossRef
42.
go back to reference Dissen GA, Lara HE, Fahrenbach WH, Costa ME, Ojeda SR. Immature rat ovaries become revascularized rapidly after autotransplantation and show a gonadotropin-dependent increase in angiogenic factor gene expression. Endocrinology. 1994;134:1146–54.PubMedCrossRef Dissen GA, Lara HE, Fahrenbach WH, Costa ME, Ojeda SR. Immature rat ovaries become revascularized rapidly after autotransplantation and show a gonadotropin-dependent increase in angiogenic factor gene expression. Endocrinology. 1994;134:1146–54.PubMedCrossRef
43.
go back to reference Soleimani R, Heytens E, Van den Broecke R, Rottiers I, Dhont M, Cuvelier CA, et al. Xenotransplantation of cryopreserved human ovarian tissue into murine back muscle. Hum Reprod. 2010;25:1458–70.PubMedCrossRef Soleimani R, Heytens E, Van den Broecke R, Rottiers I, Dhont M, Cuvelier CA, et al. Xenotransplantation of cryopreserved human ovarian tissue into murine back muscle. Hum Reprod. 2010;25:1458–70.PubMedCrossRef
44.
go back to reference von Wolff M, Donnez J, Hovatta O, Keros V, Maltaris T, Montag M, et al. Cryopreservation and autotransplantation of human ovarian tissue prior to cytotoxic therapy–a technique in its infancy but already successful in fertility preservation. Eur J Cancer. 2009;45:1547–53.CrossRef von Wolff M, Donnez J, Hovatta O, Keros V, Maltaris T, Montag M, et al. Cryopreservation and autotransplantation of human ovarian tissue prior to cytotoxic therapy–a technique in its infancy but already successful in fertility preservation. Eur J Cancer. 2009;45:1547–53.CrossRef
45.
go back to reference Amorim CA, David A, Dolmans MM, Camboni A, Donnez J, Van Langendonckt A. Impact of freezing and thawing of human ovarian tissue on follicular growth after long-term xenotransplantation. J Assist Reprod Genet. 2011;28:1157–65.PubMedCrossRefPubMedCentral Amorim CA, David A, Dolmans MM, Camboni A, Donnez J, Van Langendonckt A. Impact of freezing and thawing of human ovarian tissue on follicular growth after long-term xenotransplantation. J Assist Reprod Genet. 2011;28:1157–65.PubMedCrossRefPubMedCentral
46.
go back to reference 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;64:171–8.PubMedCrossRef 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;64:171–8.PubMedCrossRef
47.
go back to reference Fujita T, Hirose R, Yoneta M, Sasaki S, Inoue K, Kiuchi M, et al. Potent immunosuppressants, 2-alkyl-2-aminopropane-1,3-diols. J Med Chem. 1996;39:4451–9.PubMedCrossRef Fujita T, Hirose R, Yoneta M, Sasaki S, Inoue K, Kiuchi M, et al. Potent immunosuppressants, 2-alkyl-2-aminopropane-1,3-diols. J Med Chem. 1996;39:4451–9.PubMedCrossRef
48.
go back to reference Yagi H, Kamba R, Chiba K, Soga H, Yaguchi K, Nakamura M, et al. Immunosuppressant FTY720 inhibits thymocyte emigration. Eur J Immunol. 2000;30:1435–44.PubMedCrossRef Yagi H, Kamba R, Chiba K, Soga H, Yaguchi K, Nakamura M, et al. Immunosuppressant FTY720 inhibits thymocyte emigration. Eur J Immunol. 2000;30:1435–44.PubMedCrossRef
49.
go back to reference Zelinski MB, Murphy MK, Lawson MS, Jurisicova A, Pau KY, Toscano NP, et al. In vivo delivery of FTY720 prevents radiation-induced ovarian failure and infertility in adult female nonhuman primates. Fertil Steril. 2011;95:1440–5.PubMedCrossRefPubMedCentral Zelinski MB, Murphy MK, Lawson MS, Jurisicova A, Pau KY, Toscano NP, et al. In vivo delivery of FTY720 prevents radiation-induced ovarian failure and infertility in adult female nonhuman primates. Fertil Steril. 2011;95:1440–5.PubMedCrossRefPubMedCentral
Metadata
Title
VEGF and bFGF increase survival of xenografted human ovarian tissue in an experimental rabbit model
Authors
Lin Wang
Ying-fen Ying
Yin-luan Ouyang
Jing-fen Wang
Jian Xu
Publication date
01-10-2013
Publisher
Springer US
Published in
Journal of Assisted Reproduction and Genetics / Issue 10/2013
Print ISSN: 1058-0468
Electronic ISSN: 1573-7330
DOI
https://doi.org/10.1007/s10815-013-0043-9

Other articles of this Issue 10/2013

Journal of Assisted Reproduction and Genetics 10/2013 Go to the issue