231
Views
24
CrossRef citations to date
0
Altmetric
Research Paper

Restoration of ovarian tissue function and estrous cycle in rat after autotransplantation using hyaluronic acid hydrogel scaffold containing VEGF and bFGF

, , &
Pages 97-106 | Received 14 Mar 2016, Accepted 24 May 2016, Published online: 30 Jun 2016

References

  • Abir R, Fisch B, Jessel S, Felz C, Ben-Haroush A, Orvieto R. 2011. Improving posttransplantation survival of human ovarian tissue by treating the host and graft. Fertil Steril 95:1205–1210
  • Agca C, Lucy MC, Agca Y. 2009. Gene expression profile of rat ovarian tissue following xenotransplantation into immune-deficient mice. Reproduction 137:957–967
  • Ährlund-Richter L, De Luca M, Marshak DR, Munsie M, Veiga A, Rao M. 2009. Isolation and production of cells suitable for human therapy: Challenges ahead. Cell Stem Cell 4:20–26
  • Akhavan Taheri M, Rezazadeh Valojerdi M, Ebrahimi B. 2016. Intramuscular autotransplantation of vitrified rat ovary encapsulated with hyaluronic acid hydrogel. Biopreserv Biobank 14:114–121
  • Amorim EMGd, Damous LL, Durando MCS, Saraiva MVA, Koike MK, Montero EFdS. 2014. N-acetylcysteine improves morphologic and functional aspects of ovarian grafts in rats. Acta Cir Bras 29:22–27
  • Anderson SM, Chen TT, Iruela-Arispe ML, Segura T. 2009. The phosphorylation of vascular endothelial growth factor receptor-2 (VEGFR-2) by engineered surfaces with electrostatically or covalently immobilized VEGF. Biomaterials 30:4618–4628
  • Barros FS, de Oliveira RM, Alves FM, Sampaio M, Geber S. 2008. Successful ovarian autotransplant with no vascular reanastomosis in rats. Transplantation 86:1628–1630
  • Bruno J, Celestino J, Lima-Verde I, Lima L, Matos M, AraÃojo V, Saraiva M, et al. 2009. Expression of vascular endothelial growth factor (VEGF) receptor in goat ovaries and improvement of in vitro caprine preantral follicle survival and growth with VEGF. Reprod Fertil Dev 21:679–687
  • Carmeliet P, Jain RK. 2011. Molecular mechanisms and clinical applications of angiogenesis. Nature 473:298–307
  • Cha SK, Shin DH, Kim BY, Yoon SY, Yoon TK, Lee WS, Chung HM, et al. 2014. Effect of human endothelial progenitor cell (EPC)- or mouse vascular endothelial growth factor-derived vessel formation on the survival of vitrified/warmed mouse ovarian grafts. Reprod Sci 21:859–868
  • Chan AT, Karakas MF, Vakrou S, Afzal J, Rittenbach A, Lin X, Wahl RL, et al. 2015. Hyaluronic acid-serum hydrogels rapidly restore metabolism of encapsulated stem cells and promote engraftment. Biomaterials 73:1–11
  • Chow LW, Bitton R, Webber MJ, Carvajal D, Shull KR, Sharma AK, Stupp SI. 2011. A bioactive self-assembled membrane to promote angiogenesis. Biomaterials 32:1574–1582
  • Cohen Y, Dafni H, Avni R, Raz T, Biton I, Hemmings B, Neeman M. 2014. In search of signaling pathways critical for ovarian graft reception: Akt1 is essential for long-term survival of ovarian grafts. Fertil Steril 101:536–544
  • Damous L, Silva S, Carbonel A, SimÃμes R, SimÃμes M, Montero E. 2009. Effect of remote ischemic preconditioning on rat estradiol serum levels and follicular development after ovarian transplantation. Transplant Proc 41:830–833
  • Damous L, Silva S, SimÃμes R, Morello R, Carbonel A, SimÃμes M, Montero E. 2008. Remote ischemic preconditioning on neovascularization and follicle viability on ovary autotransplantation in rats. Transplant Proc 40:861–864
  • Damous LL, Nakamuta JS, de Carvalho AETS, Carvalho KC, Soares JM Jr, de Jesus Simões M, Krieger JE, et al. 2015. Scaffold-based delivery of adipose tissue-derived stem cells in rat frozen-thawed ovarian autografts: Preliminary studies in a rat model. J Assist Reprod Genet 32:1285–1294
  • Damous LL, Nakamuta JS, de Carvalho AE, Soares JM, Jr de Jesus SimÃμes M, Krieger JE, Baracat EC. 2015. Adipose tissue-derived stem cell therapy in rat cryopreserved ovarian grafts. Stem Cell Res Ther 6:1–6
  • Damous LL, Nakamuta JS, Soares JM, Jr, Maciel GAR, dos Santos SimÃμes R, de Souza Montero EF, Krieger JE, et al. 2014. Females transplanted with ovaries subjected to hypoxic preconditioning show impair of ovarian function. J Ovarian Res 7:1–7
  • Evanko SP, Tammi MI, Tammi RH, Wight TN. 2007. Hyaluronan-dependent pericellular matrix. Adv Drug Deliv Rev 59:1351–1365
  • Friedman O, Orvieto R, Fisch B, Felz C, Freud E, Ben-Haroush A, Abir R. 2012. Possible improvements in human ovarian grafting by various host and graft treatments. Hum Reprod 27:474–482
  • Gao F, Liu Y, He Y, Yang C, Wang Y, Shi X, Wei G. 2010. Hyaluronan oligosaccharides promote excisional wound healing through enhanced angiogenesis. Matrix Biol 29:107–116
  • Gao JM, Yan J, Li R, Li M, Yan LY, Wang TR, Zhao HC, et al. 2013. Improvement in the quality of heterotopic allotransplanted mouse ovarian tissues with basic fibroblast growth factor and fibrin hydrogel. Hum Reprod 28:2784–2793
  • Gao J, Huang Y, Li M, Zhao H, Zhao Y, Li R, Yan J, et al. 2015. Effect of local basic fibroblast growth factor and vascular endothelial growth factor on subcutaneously allotransplanted ovarian tissue in ovariectomized mice. PLoS One 10:e0134035
  • Henry L, Labied S, Fransolet M, Kirschvink N, Blacher S, Noel A, Foidart JM, et al. 2015. Isoform 165 of vascular endothelial growth factor in collagen matrix improves ovine cryopreserved ovarian tissue revascularisation after xenotransplantation in mice. Reprod Biol Endocrinol 13:12–22
  • Hussein MR. 2005. Apoptosis in the ovary: Molecular mechanisms. Hum Reprod Update 11:162–178
  • Ikehara S. 2013. Grand challenges in stem cell treatments. Front Cell Dev Biol 1:2–3
  • Kosaka N, Sudo N, Miyamoto A, Shimizu T. 2007. Vascular endothelial growth factor (VEGF) suppresses ovarian granulosa cell apoptosis in vitro. Biochem Biophys Res Commun 363:733–737
  • La Marca A, Sighinolfi G, Radi D, Argento C, Baraldi E, Artenisio AC, Stabile G, et al. 2010. Anti-Mullerian hormone (AMH) as a predictive marker in assisted reproductive technology (ART). Hum Reprod Update 16:113–130
  • Labied S, Delforge Y, Munaut C, Blacher S, Colige A, Delcombel R, Henry L, et al. 2013. Isoform 111 of vascular endothelial growth factor (VEGF111) improves angiogenesis of ovarian tissue xenotransplantation. Transplantation 95:426–433
  • Li F, Tao Y, Zhang Y, Li Y, Fang F, Liu Y, Cao H, et al. 2010. Follicle growth and oocyte development after ovary transplantation into back muscle of immune-intact adult castrated male mice. Reproduction 140:465–476
  • Liu J, Van der Elst J, Van den Broecke R, Dhont M. 2002. Early massive follicle loss and apoptosis in heterotopically grafted newborn mouse ovaries. Hum Reprod 17:605–611
  • Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25:402–408
  • Marcondes F, Bianchi F, Tanno A. 2002. Determination of the estrous cycle phases of rats: Some helpful considerations. Braz J Biol 62:609–614
  • Marshall OJ. 2004. PerlPrimer: Cross-platform, graphical primer design for standard, bisulphite and real-time PCR. Bioinformatics 20:2471–2472
  • Nilsson E, Parrott JA, Skinner MK. 2001. Basic fibroblast growth factor induces primordial follicle development and initiates folliculogenesis. Mol Cell Endocrinol 175:123–130
  • Oh EJ, Park K, Kim KS, Kim J, Yang JA, Kong JH, Lee MY, et al. 2010. Target specific and long-acting delivery of protein, peptide, and nucleotide therapeutics using hyaluronic acid derivatives. J Control Release 141:2–12
  • Oktay K, Schenken RS, Nelson JF. 1995. Proliferating cell nuclear antigen marks the initiation of follicular growth in the rat. Biol Reprod 53:295–301
  • Otani N, Minami S, Yamoto M, Shikone T, Otani H, Nishiyama R, Otani T, et al. 1999. The vascular endothelial growth factor/fms-like tyrosine kinase system in human ovary during the menstrual cycle and early pregnancy. J Clin Endocrinol Metab 84:3845–3851
  • Pardue EL, Ibrahim S, Ramamurthi A. 2008. Role of hyaluronan in angiogenesis and its utility to angiogenic tissue engineering. Organogenesis 4:203–214
  • Pasquinelli G, Vinci MC, Gamberini C, Orrico C, Foroni L, Guarnieri C, Parenti A, et al. 2009. Architectural organization and functional features of early endothelial progenitor cells cultured in a hyaluronan-based polymer scaffold. Tissue Eng Part A 15:2751–2762
  • Pike DB, Cai S, Pomraning KR, Firpo MA, Fisher RJ, Shu XZ, Prestwich GD, et al. 2006. Heparin-regulated release of growth factors in vitro and angiogenic response in vivo to implanted hyaluronan hydrogels containing VEGF and bFGF. Biomaterials 27:5242–5251
  • Prestwich GD. 2011. Hyaluronic acid-based clinical biomaterials derived for cell and molecule delivery in regenerative medicine. J Control Release 155:193–199
  • Riley CM, Fuegy PW, Firpo MA, Shu XZ, Prestwich GD, Peattie RA. 2006. Stimulation of in vivo angiogenesis using dual growth factor-loaded crosslinked glycosaminoglycan hydrogels. Biomaterials 27:5935–5943
  • Saito H, Kaneko T, Takahashi T, Kawachiya S, Saito T, Hiroi M. 2000. Hyaluronan in follicular fluids and fertilization of oocytes. Fertil Steril 74:1148–1152
  • Shikanov A, Zhang Z, Xu M, Smith RM, Rajan A, Woodruff TK, Shea LD. 2011. Fibrin encapsulation and vascular endothelial growth factor delivery promotes ovarian graft survival in mice. Tissue Eng Part A 17:3095–3104
  • Shin SY, Lee JY, Lee E, Choi J, Yoon BK, Bae D, Choi D. 2006. Protective effect of vascular endothelial growth factor (VEGF) in frozen-thawed granulosa cells is mediated by inhibition of apoptosis. Eur J Obstet Gynecol Reprod Biol 125:233–238
  • Skaznik-Wikiel ME, Sharma RK, Selesniemi K, Lee HJ, Tilly JL, Falcone T. 2011. Granulocyte colony-stimulating factor in conjunction with vascular endothelial growth factor maintains primordial follicle numbers in transplanted mouse ovaries. Fertil Steril 95:1405–1409
  • Smith RM, Shikanov A, Kniazeva E, Ramadurai D, Woodruff TK, Shea LD. 2014. Fibrin-mediated delivery of an ovarian follicle pool in a mouse model of infertility. Tissue Eng Part A 20:3021–3030
  • Soleimani R, Heytens E, Van den Broecke R, Rottiers I, Dhont M, Cuvelier C, De Sutter P. 2010. Xenotransplantation of cryopreserved human ovarian tissue into murine back muscle. Hum Reprod 25:1458–1470
  • Sun XT, Ding YT, Yan XG, Wu LY, Li Q, Cheng N, Qiu YD, et al. 2004. Angiogenic synergistic effect of basic fibroblast growth factor and vascular endothelial growth factor in an in vitro quantitative microcarrier-based three-dimensional fibrin angiogenesis system. World J Gastroenterol 10:2524–2528
  • Tang ZC, Liao WY, Tang AC, Tsai SJ, Hsieh PC. 2011. The enhancement of endothelial cell therapy for angiogenesis in hindlimb ischemia using hyaluronan. Biomaterials 32:75–86
  • Van den Broecke R, Liu J, Handyside A, Van der Elst JC, Krausz T, Dhont M, Winston RM, et al. 2001. Follicular growth in fresh and cryopreserved human ovarian cortical grafts transplanted to immunodeficient mice. Eur J Obstet Gynecol Reprod Biol 97:193–201
  • Vanacker J, Luyckx V, Dolmans MM, Des Rieux A, Jaeger J, Van Langendonckt A, Donnez J, et al. 2012. 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 33:6079–6085
  • Visser JA, Schipper I, Laven JS, Themmen AP. 2012. Anti-Müllerian hormone: an ovarian reserve marker in primary ovarian insufficiency. Nat Rev Endocrinol 8:331–341
  • Visser JA, Themmen AP. 2005. Anti-Müllerian hormone and folliculogenesis. Mol Cell Endocrinol 234:81–86
  • Wang L, Ying Yf, Ouyang Yl, Wang Jf, Xu J. 2013. VEGF and bFGF increase survival of xenografted human ovarian tissue in an experimental rabbit model. J Assist Reprod Genet 30:1301–1311
  • Yang H, Lee HH, Lee HC, Ko DS, Kim SS. 2008. Assessment of vascular endothelial growth factor expression and apoptosis in the ovarian graft: can exogenous gonadotropin promote angiogenesis after ovarian transplantation? Fertil Steril 90:1550–1558
  • Yoshiji H, Kuriyama S, Yoshii J, Ikenaka Y, Noguchi R, Hicklin DJ, Huber J, et al. 2002. Synergistic effect of basic fibroblast growth factor and vascular endothelial growth factor in murine hepatocellular carcinoma. Hepatology 35:834–842

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.