Skip to main content
Top
Published in: Reproductive Biology and Endocrinology 1/2017

Open Access 01-12-2017 | Research

Mesenchymal stem cell-derived angiogenin promotes primodial follicle survival and angiogenesis in transplanted human ovarian tissue

Authors: Yaoyao Zhang, Xi Xia, Jie Yan, Liying Yan, Cuilin Lu, Xiaohui Zhu, Tianren Wang, Tailang Yin, Rong Li, Hsun-Ming Chang, Jie Qiao

Published in: Reproductive Biology and Endocrinology | Issue 1/2017

Login to get access

Abstract

Background

We have recently reported that human bone marrow-derived mesenchymal stem cells (MSCs) facilitate angiogenesis and prevent follicle loss in xenografted human ovarian tissues. However, the mechanism underlying this effect remains to be elucidated. Thus, determining the paracrine profiles and identifying the key secreted factors in MSCs co-transplanted with ovarian grafts are essential for the future application of MSCs.

Methods

In this study, we used cytokine microarrays to identify differentially expressed proteins associated with angiogenesis in frozen-thawed ovarian tissues co-transplanted with MSCs. The function of specific secreted factors in MSCs co-transplanted with human ovarian tissues was studied via targeted blockade with short-hairpin RNAi and the use of monoclonal neutralizing antibodies.

Results

Our results showed that angiogenin (ANG) was one of the most robustly up-regulated proteins (among 42 protein we screened, 37 proteins were up-regulated). Notably, the targeted depletion of ANG with short-hairpin RNAi (shANG) or the addition of anti-ANG monoclonal neutralizing antibodies (ANG Ab) significantly reversed the MSC-stimulated angiogenesis, increased follicle numbers and protective effect on follicle apoptosis.

Conclusion

Our results indicate that ANG plays a critical role in regulating angiogenesis and follicle survival in xenografted human ovarian tissues. Our findings provide important insights into the molecular mechanism by which MSCs promote angiogenesis and follicle survival in transplanted ovarian tissues, thus providing a theoretical basis for their further application.
Appendix
Available only for authorised users
Literature
1.
2.
go back to reference Bastings L, Beerendonk CC, Westphal JR, Massuger LF, Kaal SE, van Leeuwen FE, Braat DD, Peek R. Autotransplantation of cryopreserved ovarian tissue in cancer survivors and the risk of reintroducing malignancy: a systematic review. Hum Reprod Update. 2013;19:483–506.CrossRefPubMed Bastings L, Beerendonk CC, Westphal JR, Massuger LF, Kaal SE, van Leeuwen FE, Braat DD, Peek R. Autotransplantation of cryopreserved ovarian tissue in cancer survivors and the risk of reintroducing malignancy: a systematic review. Hum Reprod Update. 2013;19:483–506.CrossRefPubMed
3.
go back to reference 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;97:1260–8.CrossRefPubMed 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;97:1260–8.CrossRefPubMed
4.
go back to reference Gracia CR, Chang J, Kondapalli L, Prewitt M, Carlson CA, Mattei P, Jeffers S, Ginsberg JP. Ovarian tissue cryopreservation for fertility preservation in cancer patients: successful establishment and feasibility of a multidisciplinary collaboration. J Assist Reprod Genet. 2012;29:495–502.CrossRefPubMedPubMedCentral Gracia CR, Chang J, Kondapalli L, Prewitt M, Carlson CA, Mattei P, Jeffers S, Ginsberg JP. Ovarian tissue cryopreservation for fertility preservation in cancer patients: successful establishment and feasibility of a multidisciplinary collaboration. J Assist Reprod Genet. 2012;29:495–502.CrossRefPubMedPubMedCentral
5.
go back to reference Fabbri R, Vicenti R, Magnani V, Pasquinelli G, Macciocca M, Parazza I, Paradisi R, Battaglia C, Venturoli S. Cryopreservation of ovarian tissue in breast cancer patients: 10 years of experience. Future Oncol. 2012;8:1613–9.CrossRefPubMed Fabbri R, Vicenti R, Magnani V, Pasquinelli G, Macciocca M, Parazza I, Paradisi R, Battaglia C, Venturoli S. Cryopreservation of ovarian tissue in breast cancer patients: 10 years of experience. Future Oncol. 2012;8:1613–9.CrossRefPubMed
6.
go back to reference Lambertini M, Del Mastro L, Pescio MC, Andersen CY, Azim Jr HA, Peccatori FA, Costa M, Revelli A, Salvagno F, Gennari A, et al. Cancer and fertility preservation: international recommendations from an expert meeting. BMC Med. 2016;14:1.CrossRefPubMedPubMedCentral Lambertini M, Del Mastro L, Pescio MC, Andersen CY, Azim Jr HA, Peccatori FA, Costa M, Revelli A, Salvagno F, Gennari A, et al. Cancer and fertility preservation: international recommendations from an expert meeting. BMC Med. 2016;14:1.CrossRefPubMedPubMedCentral
7.
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.CrossRefPubMed 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.CrossRefPubMed
8.
go back to reference Van Eyck AS, Bouzin C, Feron O, Romeu L, Van Langendonckt A, Donnez J, Dolmans MM. Both host and graft vessels contribute to revascularization of xenografted human ovarian tissue in a murine model. Fertil Steril. 2010;93:1676–85.CrossRefPubMed Van Eyck AS, Bouzin C, Feron O, Romeu L, Van Langendonckt A, Donnez J, Dolmans MM. Both host and graft vessels contribute to revascularization of xenografted human ovarian tissue in a murine model. Fertil Steril. 2010;93:1676–85.CrossRefPubMed
9.
go back to reference Abtahi NS, Eimani H, Vosough A, Shahverdi A, Fathi R, Hayati N, Nasiri N. Effect of therapeutic ultrasound on folliculogenesis, angiogenesis and apoptosis after heterotopic mouse ovarian transplantation. Ultrasound Med Biol. 2014;40:1535–44.CrossRefPubMed Abtahi NS, Eimani H, Vosough A, Shahverdi A, Fathi R, Hayati N, Nasiri N. Effect of therapeutic ultrasound on folliculogenesis, angiogenesis and apoptosis after heterotopic mouse ovarian transplantation. Ultrasound Med Biol. 2014;40:1535–44.CrossRefPubMed
10.
go back to reference Hu H, Zou C. Mesenchymal stem cells in renal ischemia-reperfusion injury: Biological and therapeutic perspectives. Curr Stem Cell Res Ther. 2016;24. [Epub ahead of print] Hu H, Zou C. Mesenchymal stem cells in renal ischemia-reperfusion injury: Biological and therapeutic perspectives. Curr Stem Cell Res Ther. 2016;24. [Epub ahead of print]
12.
go back to reference Sherman LS, Shaker M, Mariotti V, Rameshwar P. Mesenchymal stromal/stem cells in drug therapy: New perspective. Cytotherapy. 2017;19(1):19–27.CrossRefPubMed Sherman LS, Shaker M, Mariotti V, Rameshwar P. Mesenchymal stromal/stem cells in drug therapy: New perspective. Cytotherapy. 2017;19(1):19–27.CrossRefPubMed
13.
go back to reference Xia X, Yin T, Yan J, Yan L, Jin C, Lu C, Wang T, Zhu X, Zhi X, Wang J, et al. Mesenchymal Stem Cells Enhance Angiogenesis and Follicle Survival in Human Cryopreserved Ovarian Cortex Transplantation. Cell Transplant. 2015;24:1999–2010.CrossRefPubMed Xia X, Yin T, Yan J, Yan L, Jin C, Lu C, Wang T, Zhu X, Zhi X, Wang J, et al. Mesenchymal Stem Cells Enhance Angiogenesis and Follicle Survival in Human Cryopreserved Ovarian Cortex Transplantation. Cell Transplant. 2015;24:1999–2010.CrossRefPubMed
14.
go back to reference Foronjy RF, Majka SM. The potential for resident lung mesenchymal stem cells to promote functional tissue regeneration: understanding microenvironmental cues. Cells. 2012;1:874.CrossRefPubMedPubMedCentral Foronjy RF, Majka SM. The potential for resident lung mesenchymal stem cells to promote functional tissue regeneration: understanding microenvironmental cues. Cells. 2012;1:874.CrossRefPubMedPubMedCentral
15.
go back to reference Au P, Tam J, Fukumura D, Jain RK. Bone marrow-derived mesenchymal stem cells facilitate engineering of long-lasting functional vasculature. Blood. 2008;111:4551–8.CrossRefPubMedPubMedCentral Au P, Tam J, Fukumura D, Jain RK. Bone marrow-derived mesenchymal stem cells facilitate engineering of long-lasting functional vasculature. Blood. 2008;111:4551–8.CrossRefPubMedPubMedCentral
16.
go back to reference Lee RH, Seo MJ, Reger RL, Spees JL, Pulin AA, Olson SD, Prockop DJ. Multipotent stromal cells from human marrow home to and promote repair of pancreatic islets and renal glomeruli in diabetic NOD/scid mice. Proc Natl Acad Sci U S A. 2006;103:17438–43.CrossRefPubMedPubMedCentral Lee RH, Seo MJ, Reger RL, Spees JL, Pulin AA, Olson SD, Prockop DJ. Multipotent stromal cells from human marrow home to and promote repair of pancreatic islets and renal glomeruli in diabetic NOD/scid mice. Proc Natl Acad Sci U S A. 2006;103:17438–43.CrossRefPubMedPubMedCentral
17.
go back to reference Liu SH, Huang JP, Lee RK, Huang MC, Wu YH, Chen CY, Chen CP. Paracrine factors from human placental multipotent mesenchymal stromal cells protect endothelium from oxidative injury via STAT3 and manganese superoxide dismutase activation. Biol Reprod. 2010;82:905–13.CrossRefPubMed Liu SH, Huang JP, Lee RK, Huang MC, Wu YH, Chen CY, Chen CP. Paracrine factors from human placental multipotent mesenchymal stromal cells protect endothelium from oxidative injury via STAT3 and manganese superoxide dismutase activation. Biol Reprod. 2010;82:905–13.CrossRefPubMed
18.
19.
go back to reference Duffy GP, Ahsan T, O’Brien T, Barry F, Nerem RM. Bone marrow-derived mesenchymal stem cells promote angiogenic processes in a time- and dose-dependent manner in vitro. Tissue Eng Part A. 2009;15:2459–70.CrossRefPubMed Duffy GP, Ahsan T, O’Brien T, Barry F, Nerem RM. Bone marrow-derived mesenchymal stem cells promote angiogenic processes in a time- and dose-dependent manner in vitro. Tissue Eng Part A. 2009;15:2459–70.CrossRefPubMed
20.
go back to reference Wu Y, Chen L, Scott PG, Tredget EE. Mesenchymal stem cells enhance wound healing through differentiation and angiogenesis. Stem Cells. 2007;25:2648–59.CrossRefPubMed Wu Y, Chen L, Scott PG, Tredget EE. Mesenchymal stem cells enhance wound healing through differentiation and angiogenesis. Stem Cells. 2007;25:2648–59.CrossRefPubMed
22.
go back to reference Kupcova Skalnikova H. Proteomic techniques for characterisation of mesenchymal stem cell secretome. Biochimie. 2013;95:2196–211.CrossRefPubMed Kupcova Skalnikova H. Proteomic techniques for characterisation of mesenchymal stem cell secretome. Biochimie. 2013;95:2196–211.CrossRefPubMed
23.
go back to reference Bronckaers A, Hilkens P, Martens W, Gervois P, Ratajczak J, Struys T, Lambrichts I. Mesenchymal stem/stromal cells as a pharmacological and therapeutic approach to accelerate angiogenesis. Pharmacol Ther. 2014;143:181–96.CrossRefPubMed Bronckaers A, Hilkens P, Martens W, Gervois P, Ratajczak J, Struys T, Lambrichts I. Mesenchymal stem/stromal cells as a pharmacological and therapeutic approach to accelerate angiogenesis. Pharmacol Ther. 2014;143:181–96.CrossRefPubMed
24.
go back to reference Hsieh JY, Wang HW, Chang SJ, Liao KH, Lee IH, Lin WS, Wu CH, Lin WY, Cheng SM. Mesenchymal stem cells from human umbilical cord express preferentially secreted factors related to neuroprotection, neurogenesis, and angiogenesis. PLoS One. 2013;8:e72604.CrossRefPubMedPubMedCentral Hsieh JY, Wang HW, Chang SJ, Liao KH, Lee IH, Lin WS, Wu CH, Lin WY, Cheng SM. Mesenchymal stem cells from human umbilical cord express preferentially secreted factors related to neuroprotection, neurogenesis, and angiogenesis. PLoS One. 2013;8:e72604.CrossRefPubMedPubMedCentral
25.
go back to reference Aranha AM, Zhang Z, Neiva KG, Costa CA, Hebling J, Nor JE. Hypoxia enhances the angiogenic potential of human dental pulp cells. J Endod. 2010;36:1633–7.CrossRefPubMed Aranha AM, Zhang Z, Neiva KG, Costa CA, Hebling J, Nor JE. Hypoxia enhances the angiogenic potential of human dental pulp cells. J Endod. 2010;36:1633–7.CrossRefPubMed
26.
go back to reference Xia X, Wang T, Yin T, Yan L, Yan J, Lu C, Zhao L, Li M, Zhang Y, Jin H, et al. Mesenchymal Stem Cells Facilitate In Vitro Development of Human Preantral Follicle. Reprod Sci. 2015;22:1367–76.CrossRefPubMed Xia X, Wang T, Yin T, Yan L, Yan J, Lu C, Zhao L, Li M, Zhang Y, Jin H, et al. Mesenchymal Stem Cells Facilitate In Vitro Development of Human Preantral Follicle. Reprod Sci. 2015;22:1367–76.CrossRefPubMed
27.
go back to reference Ernst E, Bergholdt S, Jorgensen JS, Andersen CY. The first woman to give birth to two children following transplantation of frozen/thawed ovarian tissue. Hum Reprod. 2010;25:1280–1.CrossRefPubMed Ernst E, Bergholdt S, Jorgensen JS, Andersen CY. The first woman to give birth to two children following transplantation of frozen/thawed ovarian tissue. Hum Reprod. 2010;25:1280–1.CrossRefPubMed
28.
go back to reference Yoshimatsu G, Sakata N, Tsuchiya H, Minowa T, Takemura T, Morita H, Hata T, Fukase M, Aoki T, Ishida M, et al. The co-transplantation of bone marrow derived mesenchymal stem cells reduced inflammation in intramuscular islet transplantation. PLoS One. 2015;10:e0117561.CrossRefPubMedPubMedCentral Yoshimatsu G, Sakata N, Tsuchiya H, Minowa T, Takemura T, Morita H, Hata T, Fukase M, Aoki T, Ishida M, et al. The co-transplantation of bone marrow derived mesenchymal stem cells reduced inflammation in intramuscular islet transplantation. PLoS One. 2015;10:e0117561.CrossRefPubMedPubMedCentral
29.
go back to reference Ahn SY, Chang YS, Sung DK, Sung SI, Yoo HS, Im GH, Choi SJ, Park WS. Optimal Route for Mesenchymal Stem Cells Transplantation after Severe Intraventricular Hemorrhage in Newborn Rats. PLoS One. 2015;10:e0132919.CrossRefPubMedPubMedCentral Ahn SY, Chang YS, Sung DK, Sung SI, Yoo HS, Im GH, Choi SJ, Park WS. Optimal Route for Mesenchymal Stem Cells Transplantation after Severe Intraventricular Hemorrhage in Newborn Rats. PLoS One. 2015;10:e0132919.CrossRefPubMedPubMedCentral
30.
go back to reference Gougeon A, Testart J. Germinal vesicle breakdown in oocytes of human atretic follicles during the menstrual cycle. J Reprod Fertil. 1986;78:389–401.CrossRefPubMed Gougeon A, Testart J. Germinal vesicle breakdown in oocytes of human atretic follicles during the menstrual cycle. J Reprod Fertil. 1986;78:389–401.CrossRefPubMed
31.
go back to reference Gao JM, Yan J, Li R, Li M, Yan LY, Wang TR, Zhao HC, Zhao Y, Yu Y, Qiao J. Improvement in the quality of heterotopic allotransplanted mouse ovarian tissues with basic fibroblast growth factor and fibrin hydrogel. Hum Reprod. 2013;28:2784–93.CrossRefPubMed Gao JM, Yan J, Li R, Li M, Yan LY, Wang TR, Zhao HC, Zhao Y, Yu Y, Qiao J. Improvement in the quality of heterotopic allotransplanted mouse ovarian tissues with basic fibroblast growth factor and fibrin hydrogel. Hum Reprod. 2013;28:2784–93.CrossRefPubMed
32.
go back to reference Niu G, Sun X, Cao Q, Courter D, Koong A, Le QT, Gambhir SS, Chen X. Cetuximab-based immunotherapy and radioimmunotherapy of head and neck squamous cell carcinoma. Clin Cancer Res. 2010;16:2095–105.CrossRefPubMedPubMedCentral Niu G, Sun X, Cao Q, Courter D, Koong A, Le QT, Gambhir SS, Chen X. Cetuximab-based immunotherapy and radioimmunotherapy of head and neck squamous cell carcinoma. Clin Cancer Res. 2010;16:2095–105.CrossRefPubMedPubMedCentral
33.
go back to reference Kishimoto K, Liu S, Tsuji T, Olson KA, Hu GF. Endogenous angiogenin in endothelial cells is a general requirement for cell proliferation and angiogenesis. Oncogene. 2005;24:445–56.CrossRefPubMed Kishimoto K, Liu S, Tsuji T, Olson KA, Hu GF. Endogenous angiogenin in endothelial cells is a general requirement for cell proliferation and angiogenesis. Oncogene. 2005;24:445–56.CrossRefPubMed
34.
35.
go back to reference Chen J, Liu Z, Hong MM, Zhang H, Chen C, Xiao M, Wang J, Yao F, Ba M, Liu J, et al. Proangiogenic compositions of microvesicles derived from human umbilical cord mesenchymal stem cells. PLoS One. 2014;9:e115316.CrossRefPubMedPubMedCentral Chen J, Liu Z, Hong MM, Zhang H, Chen C, Xiao M, Wang J, Yao F, Ba M, Liu J, et al. Proangiogenic compositions of microvesicles derived from human umbilical cord mesenchymal stem cells. PLoS One. 2014;9:e115316.CrossRefPubMedPubMedCentral
36.
go back to reference Du W, Li X, Chi Y, Ma F, Li Z, Yang S, Song B, Cui J, Ma T, Li J, et al. VCAM-1+ placenta chorionic villi-derived mesenchymal stem cells display potent pro-angiogenic activity. Stem Cell Res Ther. 2016;7:49.CrossRefPubMedPubMedCentral Du W, Li X, Chi Y, Ma F, Li Z, Yang S, Song B, Cui J, Ma T, Li J, et al. VCAM-1+ placenta chorionic villi-derived mesenchymal stem cells display potent pro-angiogenic activity. Stem Cell Res Ther. 2016;7:49.CrossRefPubMedPubMedCentral
37.
go back to reference Liu XH, Bai CG, Xu ZY, Huang SD, Yuan Y, Gong DJ, Zhang JR. Therapeutic potential of angiogenin modified mesenchymal stem cells: angiogenin improves mesenchymal stem cells survival under hypoxia and enhances vasculogenesis in myocardial infarction. Microvasc Res. 2008;76:23–30.CrossRefPubMed Liu XH, Bai CG, Xu ZY, Huang SD, Yuan Y, Gong DJ, Zhang JR. Therapeutic potential of angiogenin modified mesenchymal stem cells: angiogenin improves mesenchymal stem cells survival under hypoxia and enhances vasculogenesis in myocardial infarction. Microvasc Res. 2008;76:23–30.CrossRefPubMed
38.
go back to reference Huang SD, Lu FL, Xu XY, Liu XH, Zhao XX, Zhao BZ, Wang L, Gong DJ, Yuan Y, Xu ZY. Transplantation of angiogenin-overexpressing mesenchymal stem cells synergistically augments cardiac function in a porcine model of chronic ischemia. J Thorac Cardiovasc Surg. 2006;132:1329–38.CrossRefPubMed Huang SD, Lu FL, Xu XY, Liu XH, Zhao XX, Zhao BZ, Wang L, Gong DJ, Yuan Y, Xu ZY. Transplantation of angiogenin-overexpressing mesenchymal stem cells synergistically augments cardiac function in a porcine model of chronic ischemia. J Thorac Cardiovasc Surg. 2006;132:1329–38.CrossRefPubMed
39.
go back to reference Fett JW, Strydom DJ, Lobb RR, Alderman EM, Bethune JL, Riordan JF, Vallee BL. Isolation and characterization of angiogenin, an angiogenic protein from human carcinoma cells. Biochemistry. 1985;24:5480–6.CrossRefPubMed Fett JW, Strydom DJ, Lobb RR, Alderman EM, Bethune JL, Riordan JF, Vallee BL. Isolation and characterization of angiogenin, an angiogenic protein from human carcinoma cells. Biochemistry. 1985;24:5480–6.CrossRefPubMed
40.
go back to reference Subramanian V, Feng Y. A new role for angiogenin in neurite growth and pathfinding: implications for amyotrophic lateral sclerosis. Hum Mol Genet. 2007;16:1445–53.CrossRefPubMed Subramanian V, Feng Y. A new role for angiogenin in neurite growth and pathfinding: implications for amyotrophic lateral sclerosis. Hum Mol Genet. 2007;16:1445–53.CrossRefPubMed
41.
go back to reference Hooper LV, Stappenbeck TS, Hong CV, Gordon JI. Angiogenins: a new class of microbicidal proteins involved in innate immunity. Nat Immunol. 2003;4:269–73.CrossRefPubMed Hooper LV, Stappenbeck TS, Hong CV, Gordon JI. Angiogenins: a new class of microbicidal proteins involved in innate immunity. Nat Immunol. 2003;4:269–73.CrossRefPubMed
42.
go back to reference Malamitsi-Puchner A, Sarandakou A, Baka S, Hasiakos D, Kouskouni E, Creatsas G. In vitro fertilization: angiogenic, proliferative, and apoptotic factors in the follicular fluid. Ann N Y Acad Sci. 2003;997:124–8.CrossRefPubMed Malamitsi-Puchner A, Sarandakou A, Baka S, Hasiakos D, Kouskouni E, Creatsas G. In vitro fertilization: angiogenic, proliferative, and apoptotic factors in the follicular fluid. Ann N Y Acad Sci. 2003;997:124–8.CrossRefPubMed
43.
go back to reference Kawano Y, Zeineh Hasan K, Fukuda J, Mine S, Miyakawa I. Production of vascular endothelial growth factor and angiogenic factor in human follicular fluid. Mol Cell Endocrinol. 2003;202:19–23.CrossRefPubMed Kawano Y, Zeineh Hasan K, Fukuda J, Mine S, Miyakawa I. Production of vascular endothelial growth factor and angiogenic factor in human follicular fluid. Mol Cell Endocrinol. 2003;202:19–23.CrossRefPubMed
44.
go back to reference Stouffer RL, Martinez-Chequer JC, Molskness TA, Xu F, Hazzard TM. Regulation and action of angiogenic factors in the primate ovary. Arch Med Res. 2001;32:567–75.CrossRefPubMed Stouffer RL, Martinez-Chequer JC, Molskness TA, Xu F, Hazzard TM. Regulation and action of angiogenic factors in the primate ovary. Arch Med Res. 2001;32:567–75.CrossRefPubMed
45.
go back to reference Malamitsi-Puchner A, Sarandakou A, Baka SG, Tziotis J, Rizos D, Hassiakos D, Creatsas G. Concentrations of angiogenic factors in follicular fluid and oocyte-cumulus complex culture medium from women undergoing in vitro fertilization: association with oocyte maturity and fertilization. Fertil Steril. 2001;76:98–101.CrossRefPubMed Malamitsi-Puchner A, Sarandakou A, Baka SG, Tziotis J, Rizos D, Hassiakos D, Creatsas G. Concentrations of angiogenic factors in follicular fluid and oocyte-cumulus complex culture medium from women undergoing in vitro fertilization: association with oocyte maturity and fertilization. Fertil Steril. 2001;76:98–101.CrossRefPubMed
46.
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.CrossRefPubMed 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.CrossRefPubMed
47.
go back to reference Wu D, Lei Y, Tong Y, Tang F, Qian Y, Zhou Y. Angiogenesis of the frozen-thawed human fetal ovarian tissue at the early stage after xenotransplantation and the positive effect of Salviae miltiorrhizae. Anat Rec (Hoboken). 2010;293:2154–62.CrossRef Wu D, Lei Y, Tong Y, Tang F, Qian Y, Zhou Y. Angiogenesis of the frozen-thawed human fetal ovarian tissue at the early stage after xenotransplantation and the positive effect of Salviae miltiorrhizae. Anat Rec (Hoboken). 2010;293:2154–62.CrossRef
48.
go back to reference Kim SS. Assessment of long term endocrine function after transplantation of frozen-thawed human ovarian tissue to the heterotopic site: 10 year longitudinal follow-up study. J Assist Reprod Genet. 2012;29:489–93.CrossRefPubMedPubMedCentral Kim SS. Assessment of long term endocrine function after transplantation of frozen-thawed human ovarian tissue to the heterotopic site: 10 year longitudinal follow-up study. J Assist Reprod Genet. 2012;29:489–93.CrossRefPubMedPubMedCentral
49.
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.CrossRefPubMed 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.CrossRefPubMed
50.
go back to reference Dath C, Dethy A, Van Langendonckt A, Van Eyck AS, Amorim CA, Luyckx V, Donnez J, Dolmans MM. Endothelial cells are essential for ovarian stromal tissue restructuring after xenotransplantation of isolated ovarian stromal cells. Hum Reprod. 2011;26:1431–9.CrossRefPubMed Dath C, Dethy A, Van Langendonckt A, Van Eyck AS, Amorim CA, Luyckx V, Donnez J, Dolmans MM. Endothelial cells are essential for ovarian stromal tissue restructuring after xenotransplantation of isolated ovarian stromal cells. Hum Reprod. 2011;26:1431–9.CrossRefPubMed
51.
go back to reference Poirot C, Abirached F, Prades M, Coussieu C, Bernaudin F, Piver P. Induction of puberty by autograft of cryopreserved ovarian tissue. Lancet. 2012;379:588.CrossRefPubMed Poirot C, Abirached F, Prades M, Coussieu C, Bernaudin F, Piver P. Induction of puberty by autograft of cryopreserved ovarian tissue. Lancet. 2012;379:588.CrossRefPubMed
52.
go back to reference Lee DM, Yeoman RR, Battaglia DE, Stouffer RL, Zelinski-Wooten MB, Fanton JW, Wolf DP. Live birth after ovarian tissue transplant. Nature. 2004;428:137–8.CrossRefPubMed Lee DM, Yeoman RR, Battaglia DE, Stouffer RL, Zelinski-Wooten MB, Fanton JW, Wolf DP. Live birth after ovarian tissue transplant. Nature. 2004;428:137–8.CrossRefPubMed
53.
go back to reference Labied S, Delforge Y, Munaut C, Blacher S, Colige A, Delcombel R, Henry L, Fransolet M, Jouan C, Perrier d’Hauterive S, et al. Isoform 111 of vascular endothelial growth factor (VEGF111) improves angiogenesis of ovarian tissue xenotransplantation. Transplantation. 2013;95:426–33.CrossRefPubMed Labied S, Delforge Y, Munaut C, Blacher S, Colige A, Delcombel R, Henry L, Fransolet M, Jouan C, Perrier d’Hauterive S, et al. Isoform 111 of vascular endothelial growth factor (VEGF111) improves angiogenesis of ovarian tissue xenotransplantation. Transplantation. 2013;95:426–33.CrossRefPubMed
Metadata
Title
Mesenchymal stem cell-derived angiogenin promotes primodial follicle survival and angiogenesis in transplanted human ovarian tissue
Authors
Yaoyao Zhang
Xi Xia
Jie Yan
Liying Yan
Cuilin Lu
Xiaohui Zhu
Tianren Wang
Tailang Yin
Rong Li
Hsun-Ming Chang
Jie Qiao
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2017
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/s12958-017-0235-8

Other articles of this Issue 1/2017

Reproductive Biology and Endocrinology 1/2017 Go to the issue