Skip to main content

Advertisement

SpringerLink
Log in

Restoring Fertility with Cryopreserved Prepubertal Testicular Tissue: Perspectives with Hydrogel Encapsulation, Nanotechnology, and Bioengineered Scaffolds

  • Reproductive Tissue Engineering
  • Published:
Annals of Biomedical Engineering Aims and scope Submit manuscript

An Erratum to this article was published on 06 February 2017

Abstract

New and improved oncological therapies are now able to cure more than 80% of cancer-affected children in Europe. However, such treatments are gonadotoxic and result in fertility issues, especially in boys who are not able to provide a sperm sample before starting chemo/radiotherapy because of their prepubertal state. For these boys, cryopreservation of immature testicular tissue (ITT) is the only available option, aiming to preserve spermatogonial stem cells (SSCs). Both slow-freezing and vitrification have been investigated to this end and are now applied in a clinical setting for SSC cryopreservation. Research now has to focus on methods that will allow fertility restoration. This review discusses different studies that have been conducted on ITT transplantation, including those using growth factor supplementation like free molecules, or tissue encapsulation with or without nanoparticles, as well as the possibility of developing a bioartificial testis that can be used for in vitro gamete production or in vivo transplantation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

ITT:

Immature testicular tissue

SSC:

Spermatogonial stem cell

SC:

Sertoli cell

LC:

Leydig cell

ST:

Seminiferous tubule

ICSI:

Intracytoplasmic sperm injection

VEGF:

Vascular endothelial growth factor

ROS:

Reactive oxygen species

NAC:

N-Acetylcystein

NP:

Nanoparticle

ECM:

Extracellular matrix

PDGF:

Platelet-derived growth factor

EDTA:

Ethylenediaminetetraacetic acid

Gal-KO:

α1,3-Galactosyltransferase knockout

References

  1. Abrishami, M., M. Anzar, Y. Yang, and A. Honaramooz. Cryopreservation of immature porcine testis tissue to maintain its developmental potential after xenografting into recipient mice. Theriogenology 73:86–96, 2010.

    Article  CAS  PubMed  Google Scholar 

  2. Aktas, B. K., S. Bulut, S. Bulut, M. M. Baykam, C. Ozden, M. Senes, D. Yucel, and A. Memis. The effects of N-acetylcysteine on testicular damage in experimental testicular ischemia/reperfusion injury. Pediatr. Surg. Int. 26:293–298, 2010.

    Article  PubMed  Google Scholar 

  3. Amorim, C. A., and A. Shikanov. The artificial ovary: current status and future perspectives. Future Oncol. 12:2323–2332, 2016.

    Article  CAS  PubMed  Google Scholar 

  4. Artel, A., H. Mehdizadeh, Y. C. Chiu, E. M. Brey, and A. Cinar. An agent-based model for the investigation of neovascularization within porous scaffolds. Tissue Eng. Part A 17:2133–2141, 2011.

    Article  CAS  PubMed  Google Scholar 

  5. Awada, H. K., N. R. Johnson, and Y. Wang. Sequential delivery of angiogenic growth factors improves revascularization and heart function after myocardial infarction. J. Control Release 207:7–17, 2015.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Ayinde, O. C., S. Ogunnowo, and R. A. Ogedegbe. Influence of Vitamin C and Vitamin E on testicular zinc content and testicular toxicity in lead exposed albino rats. BMC Pharmacol. Toxicol. 13:17, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Baert, Y., E. Goossens, D. van Saen, L. Ning, P. In’t Veld, and H. Tournaye. Orthotopic grafting of cryopreserved prepubertal testicular tissue: in search of a simple yet effective cryopreservation protocol. Fertil. Steril. 97:1152–1157, 2012.

    Article  PubMed  Google Scholar 

  8. Baert, Y., J. B. Stukenborg, M. Landreh, J. De Kock, H. Jornvall, O. Soder, and E. Goossens. Derivation and characterization of a cytocompatible scaffold from human testis. Hum. Reprod. 30:256–267, 2015.

    Article  CAS  PubMed  Google Scholar 

  9. Bahadur, G., R. Chatterjee, and D. Ralph. Testicular tissue cryopreservation in boys. Ethical and legal issues: case report. Hum. Reprod. 15:1416–1420, 2000.

    Article  CAS  PubMed  Google Scholar 

  10. Bahadur, G., and D. Ralph. Gonadal tissue cryopreservation in boys with paediatric cancers. Hum. Reprod. 14:11–17, 1999.

    Article  CAS  PubMed  Google Scholar 

  11. Bonandrini, B., M. Figliuzzi, E. Papadimou, M. Morigi, N. Perico, F. Casiraghi, C. Dipl, F. Sangalli, S. Conti, A. Benigni, A. Remuzzi, and G. Remuzzi. Recellularization of well-preserved acellular kidney scaffold using embryonic stem cells. Tissue Eng. Part A 20:1486–1498, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Caires, K. C., J. de Avila, and D. J. McLean. Vascular endothelial growth factor regulates germ cell survival during establishment of spermatogenesis in the bovine testis. Reproduction 138:667–677, 2009.

    Article  CAS  PubMed  Google Scholar 

  13. Campbell, G. R., G. Turnbull, L. Xiang, M. Haines, S. Armstrong, B. E. Rolfe, and J. H. Campbell. The peritoneal cavity as a bioreactor for tissue engineering visceral organs: bladder, uterus and vas deferens. J. Tissue Eng. Regen. Med. 2:50–60, 2008.

    Article  CAS  PubMed  Google Scholar 

  14. Cao, Y., A. Hong, H. Schulten, and M. J. Post. Update on therapeutic neovascularization. Cardiovasc. Res. 65:639–648, 2005.

    Article  CAS  PubMed  Google Scholar 

  15. Cay, A., A. Alver, M. Kucuk, O. Isik, M. S. Eminagaoglu, S. C. Karahan, and O. Deger. The effects of N-acetylcysteine on antioxidant enzyme activities in experimental testicular torsion. J. Surg. Res. 131:199–203, 2006.

    Article  CAS  PubMed  Google Scholar 

  16. Chen, K. L., D. Eberli, J. J. Yoo, and A. Atala. Bioengineered corporal tissue for structural and functional restoration of the penis. Proc. Natl Acad. Sci. U.S.A. 107:3346–3350, 2010.

    Article  CAS  PubMed  Google Scholar 

  17. Chen, R. R., E. A. Silva, W. W. Yuen, and D. J. Mooney. Spatio-temporal VEGF and PDGF delivery patterns blood vessel formation and maturation. Pharm. Res. 24:258–264, 2007.

    Article  PubMed  Google Scholar 

  18. Cheng, C. Y., E. W. Wong, H. H. Yan, and D. D. Mruk. Regulation of spermatogenesis in the microenvironment of the seminiferous epithelium: new insights and advances. Mol. Cell. Endocrinol. 315:49–56, 2010.

    Article  CAS  PubMed  Google Scholar 

  19. Crapo, P. M., T. W. Gilbert, and S. F. Badylak. An overview of tissue and whole organ decellularization processes. Biomaterials 32:3233–3243, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Curaba, M., J. Poels, A. van Langendonckt, J. Donnez, and C. Wyns. Can prepubertal human testicular tissue be cryopreserved by vitrification? Fertil. Steril. 95:2123.e9–2123.e12, 2011.

    Google Scholar 

  21. de Michele, F., J. Poels, L. Weerens, C. Petit, Z. Evrard, J. Ambroise, D. Gruson, and C. Wyns. Preserved seminiferous tubule integrity with spermatogonial survival and induction of Sertoli and Leydig cell maturation after long-term organotypic culture of prepubertal human testicular tissue. Hum. Reprod. 97:143–150, 2016.

    Google Scholar 

  22. des Rieux, A., P. De Berdt, E. Ansorena, B. Ucakar, J. Damien, O. Schakman, E. Audouard, C. Bouzin, D. Auhl, T. Simon-Yarza, O. Feron, M. J. Blanco-Prieto, P. Carmeliet, C. Bailly, F. Clotman, and V. Preat. Vascular endothelial growth factor-loaded injectable hydrogel enhances plasticity in the injured spinal cord. J Biomed Mater Res A 102:2345–2355, 2013.

    Article  PubMed  Google Scholar 

  23. des Rieux, A., B. Ucakar, B. P. Mupendwa, D. Colau, O. Feron, P. Carmeliet, and V. Preat. 3D systems delivering VEGF to promote angiogenesis for tissue engineering. J Control Release 150:272–278, 2011.

    Article  PubMed  Google Scholar 

  24. Dhandayuthapani, B., Y. Yoshida, T. Maekawa, and D. S. Kumar. Polymeric scaffolds in tissue engineering application: a review. Int. J. Polym. Sci. 1–19:2011, 2011.

    Google Scholar 

  25. Eberli, D., R. Susaeta, J. J. Yoo, and A. Atala. A method to improve cellular content for corporal tissue engineering. Tissue Eng. Part A 14:1581–1589, 2008.

    Article  PubMed  Google Scholar 

  26. Enders, G. C., J. H. Henson, and C. F. Millette. Sertoli cell binding to isolated testicular basement membrane. J. Cell Biol. 103:1109–1119, 1986.

    Article  CAS  PubMed  Google Scholar 

  27. Gatta, G., G. Zigon, R. Capocaccia, J. W. Coebergh, E. Desandes, P. Kaatsch, G. Pastore, R. Peris-Bonet, C. A. Stiller, and EUROCARE Working Group. Survival of European children and young adults with cancer diagnosed 1995–2002. Eur. J. Cancer 45: 992–1005, 2009.

  28. Gerdprasert, O., M. K. O’Bryan, J. A. Muir, A. M. Caldwell, S. Schlatt, D. M. de Kretser, and M. P. Hedger. The response of testicular leukocytes to lipopolysaccharide-induced inflammation: further evidence for heterogeneity of the testicular macrophage population. Cell Tissue Res. 308:277–285, 2002.

    Article  CAS  PubMed  Google Scholar 

  29. Ginsberg, J. P., C. A. Carlson, K. Lin, W. L. Hobbie, E. Wigo, X. Wu, R. L. Brinster, and T. F. Kolon. An experimental protocol for fertility preservation in prepubertal boys recently diagnosed with cancer: a report of acceptability and safety. Hum. Reprod. 25:37–41, 2010.

    Article  CAS  PubMed  Google Scholar 

  30. Hadley, M. A., S. W. Byers, C. A. Suarez-Quian, H. K. Kleinman, and M. Dym. Extracellular matrix regulates Sertoli cell differentiation, testicular cord formation, and germ cell development in vitro. J. Cell Biol. 101:1511–1522, 1985.

    Article  CAS  PubMed  Google Scholar 

  31. Han, F., X. Jia, D. Dai, X. Yang, J. Zhao, Y. Zhao, Y. Fan, and X. Yuan. Performance of a multilayered small-diameter vascular scaffold dual-loaded with VEGF and PDGF. Biomaterials 34:7302–7313, 2013.

    Article  CAS  PubMed  Google Scholar 

  32. Hao, X., E. A. Silva, A. Mansson-Broberg, K. H. Grinnemo, A. J. Siddiqui, G. Dellgren, E. Wardell, L. A. Brodin, D. J. Mooney, and C. Sylven. Angiogenic effects of sequential release of VEGF-A165 and PDGF-BB with alginate hydrogels after myocardial infarction. Cardiovasc. Res. 75:178–185, 2007.

    Article  CAS  PubMed  Google Scholar 

  33. Hemadi, M., S. Shokri, F. Moramezi, R. Nikbakht, and A. Sobhani. Potential use of melatonin supplementation to protect vitrified testicular grafts from hypoxic-ischaemic damage. Andrologia 46:513–521, 2014.

    Article  CAS  PubMed  Google Scholar 

  34. Hemadi, M., M. Zargar, A. Sobhani, and A. Sobhani. Assessment of morphological and functional changes in neonate vitrified testis grafts after host treatment with melatonin. Folia Morphol. (Warsz) 70:95–102, 2011.

    CAS  Google Scholar 

  35. Henry, L., S. Labied, M. Fransolet, N. Kirschvink, S. Blacher, A. Noel, J. M. Foidart, M. Nisolle, and C. Munaut. 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, 2015.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Hoare, T. R., and D. S. Kohane. Hydrogels in drug delivery: progress and challenges. Polymer 49:1993–2007, 2008.

    Article  CAS  Google Scholar 

  37. Honaramooz, A., A. Snedaker, M. Boiani, H. Scholer, I. Dobrinski, and S. Schlatt. Sperm from neonatal mammalian testes grafted in mice. Nature 418:778–781, 2002.

    Article  CAS  PubMed  Google Scholar 

  38. House, M., C. C. Sanchez, W. L. Rice, S. Socrate, and D. L. Kaplan. Cervical tissue engineering using silk scaffolds and human cervical cells. Tissue Eng. Part A 16:2101–2112, 2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Howlader, N., A. M. Noone, M. Krapcho, J. Garshell, N. Neyman, S. F. Altekruse, C. L. Kosary, M. Yu, J. Ruhl, Z. Tatalovich, H. Cho, A. Mariotto, D. R. Lewis, H. S. Chen, E. J. Feuer, and K. A. Cronin. SEER Cancer Statistics Review, 1975–2010. Bethesda, MD: National Cancer Institute, 2014.

    Google Scholar 

  40. Huang, M., S. N. Vitharana, L. J. Peek, T. Coop, and C. Berkland. Polyelectrolyte complexes stabilize and controllably release vascular endothelial growth factor. Biomacromolecules 8:1607–1614, 2007.

    Article  CAS  PubMed  Google Scholar 

  41. Hussein, K. H., K. M. Park, K. S. Kang, and H. M. Woo. Biocompatibility evaluation of tissue-engineered decellularized scaffolds for biomedical application. Mater. Sci. Eng. C Mater. Biol. Appl. 67:766–778, 2016.

    Article  CAS  PubMed  Google Scholar 

  42. Hynes, R. O. The extracellular matrix: not just pretty fibrils. Science 326:1216–1219, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Jafari, M., Z. Paknejad, M. R. Rad, S. R. Motamedian, M. J. Eghbal, N. Nadjmi, and A. Khojasteh. Polymeric scaffolds in tissue engineering: a literature review. J Biomed Mater Res B Appl Biomater 104(11):2843–2853, 2015.

    Google Scholar 

  44. Kaneko, H., K. Kikuchi, M. Nakai, T. Somfai, J. Noguchi, F. Tanihara, J. Ito, and N. Kashiwazaki. Generation of live piglets for the first time using sperm retrieved from immature testicular tissue cryopreserved and grafted into nude mice. PLoS ONE 8:e70989, 2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Keros, V., K. Hultenby, B. Borgstrom, M. Fridstrom, K. Jahnukainen, and O. Hovatta. Methods of cryopreservation of testicular tissue with viable spermatogonia in pre-pubertal boys undergoing gonadotoxic cancer treatment. Hum. Reprod. 22:1384–1395, 2007.

    Article  CAS  PubMed  Google Scholar 

  46. Kim, T. H., H. K. Hargreaves, R. K. Brynes, H. K. Hawkins, V. K. Lui, J. Woodard, and A. H. Ragab. Pretreatment testicular biopsy in childhood acute lymphocytic leukaemia. Lancet 2:657–658, 1981.

    Article  CAS  PubMed  Google Scholar 

  47. Kim, T. H., H. K. Hargreaves, W. C. Chan, R. K. Brynes, C. Alvarado, J. Woodard, and A. H. Ragab. Sequential testicular biopsies in childhood acute lymphocytic leukemia. Cancer 57:1038–1041, 1986.

    Article  CAS  PubMed  Google Scholar 

  48. Labied, S., Y. Delforge, C. Munaut, S. Blacher, A. Colige, R. Delcombel, L. Henry, M. Fransolet, C. Jouan, S. Perrier d’Hauterive, A. Noel, M. Nisolle, and J. M. Foidart. Isoform 111 of vascular endothelial growth factor (VEGF111) improves angiogenesis of ovarian tissue xenotransplantation. Transplantation 95:426–433, 2013.

    Article  CAS  PubMed  Google Scholar 

  49. Laronda, M. M., A. E. Jakus, K. A. Whelan, J. A. Wertheim, R. N. Shah, and T. K. Woodruff. Initiation of puberty in mice following decellularized ovary transplant. Biomaterials 50:20–29, 2015.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Lee, D. R., M. T. Kaproth, and J. E. Parks. In vitro production of haploid germ cells from fresh or frozen-thawed testicular cells of neonatal bulls. Biol. Reprod. 65:873–878, 2001.

    Article  CAS  PubMed  Google Scholar 

  51. Lee, J., and K. Y. Lee. Local and sustained vascular endothelial growth factor delivery for angiogenesis using an injectable system. Pharm. Res. 26:1739–1744, 2009.

    Article  CAS  PubMed  Google Scholar 

  52. Lee, J. H., M. C. Gye, K. W. Choi, J. Y. Hong, Y. B. Lee, D. W. Park, S. J. Lee, and C. K. Min. In vitro differentiation of germ cells from nonobstructive azoospermic patients using three-dimensional culture in a collagen gel matrix. Fertil. Steril. 87:824–833, 2007.

    Article  CAS  PubMed  Google Scholar 

  53. Lee, J. H., H. J. Kim, H. Kim, S. J. Lee, and M. C. Gye. In vitro spermatogenesis by three-dimensional culture of rat testicular cells in collagen gel matrix. Biomaterials 27:2845–2853, 2006.

    Article  CAS  PubMed  Google Scholar 

  54. Lee, J. H., J. H. Oh, J. H. Lee, M. R. Kim, and C. K. Min. Evaluation of in vitro spermatogenesis using poly(d,l-lactic-co-glycolic acid) (PLGA)-based macroporous biodegradable scaffolds. J. Tissue Eng. Regen. Med. 5:130–137, 2011.

    Article  CAS  PubMed  Google Scholar 

  55. Liu, J., K. M. Cheng, and F. G. Silversides. Production of live offspring from testicular tissue cryopreserved by vitrification procedures in Japanese quail (Coturnix japonica). Biol. Reprod. 88:124, 2013.

    Article  PubMed  Google Scholar 

  56. Liu, Z., Y. H. Nie, C. C. Zhang, Y. J. Cai, Y. Wang, H. P. Lu, Y. Z. Li, C. Cheng, Z. L. Qiu, and Q. Sun. Generation of macaques with sperm derived from juvenile monkey testicular xenografts. Cell Res. 26:139–142, 2016.

    Article  PubMed  Google Scholar 

  57. Luyckx, V., M. M. Dolmans, J. Vanacker, C. Legat, C. Fortuno Moya, J. Donnez, and C. A. Amorim. A new step toward the artificial ovary: survival and proliferation of isolated murine follicles after autologous transplantation in a fibrin scaffold. Fertil. Steril. 101:1149–1156, 2014.

    Article  PubMed  Google Scholar 

  58. Luyckx, V., M. M. Dolmans, J. Vanacker, S. R. Scalercio, J. Donnez, and C. A. Amorim. First step in developing a 3D biodegradable fibrin scaffold for an artificial ovary. J. Ovarian Res. 6:83, 2013.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Milazzo, J. P., A. Travers, A. Bironneau, A. Safsaf, E. Gruel, C. Arnoult, B. Mace, O. Boyer, and N. Rives. Rapid screening of cryopreservation protocols for murine prepubertal testicular tissue by histology and PCNA immunostaining. J. Androl. 31:617–630, 2010.

    Article  CAS  PubMed  Google Scholar 

  60. Murphy, S. V., and A. Atala. 3D bioprinting of tissues and organs. Nat. Biotechnol. 32:773–785, 2014.

    Article  CAS  PubMed  Google Scholar 

  61. Nicodemus, G. D., and S. J. Bryant. Cell encapsulation in biodegradable hydrogels for tissue engineering applications. Tissue Eng. Part B Rev. 14:149–165, 2008.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Nomi, M., A. Atala, P. D. Coppi, and S. Soker. Principals of neovascularization for tissue engineering. Mol. Aspects Med. 23:463–483, 2002.

    Article  CAS  PubMed  Google Scholar 

  63. Ohta, H., and T. Wakayama. Generation of normal progeny by intracytoplasmic sperm injection following grafting of testicular tissue from cloned mice that died postnatally. Biol. Reprod. 73:390–395, 2005.

    Article  CAS  PubMed  Google Scholar 

  64. Patel, H., M. Bonde, and G. Srinivasan. Biodegradable polymer scaffold for tissue engineering. Trends Biomater. Artif. Organs 25:20–29, 2011.

    Google Scholar 

  65. Pati, F., J. Jang, D. H. Ha, S. Won Kim, J. W. Rhie, J. H. Shim, D. H. Kim, and D. W. Cho. Printing three-dimensional tissue analogues with decellularized extracellular matrix bioink. Nat Commun 5:3935, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Pelliniemi, L. J., J. Paranko, S. K. Grund, K. Frojdman, J. M. Foidart, and T. Lakkala-Paranko. Extracellular matrix in testicular differentiation. Ann. N. Y. Acad. Sci. 438:405–416, 1984.

    Article  CAS  PubMed  Google Scholar 

  67. Poels, J., G. Abou-Ghannam, S. Herman, A. Van Langendonckt, F. X. Wese, and C. Wyns. In search of better spermatogonial preservation by supplementation of cryopreserved human immature testicular tissue xenografts with N-acetylcysteine and testosterone. Front. Surg. 1:47, 2014.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Poels, J., A. Van Langendonckt, M. C. Many, F. X. Wese, and C. Wyns. Vitrification preserves proliferation capacity in human spermatogonia. Hum. Reprod. 28:578–589, 2013.

    Article  CAS  PubMed  Google Scholar 

  69. Pollanen, P. P., M. Kallajoki, L. Risteli, J. Risteli, and J. J. Suominen. Laminin and type IV collagen in the human testis. Int. J. Androl. 8:337–347, 1985.

    Article  CAS  PubMed  Google Scholar 

  70. Rao, A. V., and C. Shaha. N-acetylcysteine prevents MAA induced male germ cell apoptosis: role of glutathione and cytochrome c. FEBS Lett. 527:133–137, 2002.

    Article  CAS  PubMed  Google Scholar 

  71. Rathi, R., W. Zeng, S. Megee, A. Conley, S. Meyers, and I. Dobrinski. Maturation of testicular tissue from infant monkeys after xenografting into mice. Endocrinology 149:5288–5296, 2008.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Raya-Rivera, A. M., D. Esquiliano, R. Fierro-Pastrana, E. Lopez-Bayghen, P. Valencia, R. Ordorica-Flores, S. Soker, J. J. Yoo, and A. Atala. Tissue-engineered autologous vaginal organs in patients: a pilot cohort study. Lancet 384:329–336, 2014.

    Article  PubMed  Google Scholar 

  73. Reuter, K., J. Ehmcke, J. B. Stukenborg, M. Simoni, O. S. Damm, K. Redmann, S. Schlatt, and J. Wistuba. Reassembly of somatic cells and testicular organogenesis in vitro. Tissue Cell 46:86–96, 2014.

    Article  CAS  PubMed  Google Scholar 

  74. Richardson, T. P., M. C. Peters, A. B. Ennett, and D. J. Mooney. Polymeric system for dual growth factor delivery. Nat. Biotechnol. 19:1029–1034, 2001.

    Article  CAS  PubMed  Google Scholar 

  75. Rutz, A., M. M. Laronda, S. Xiao, K. A. Whelan, T. K. Woodruff, and R. N. Shah. Engineering a functional ovary with 3D biomaterial printing. Front. Bioeng. Biotechnol. 2016. doi:10.3389/conf.FBIOE.2016.01.02633.

    Google Scholar 

  76. Sadri-Ardekani, H., C. H. Homburg, T. M. van Capel, H. van den Berg, F. van der Veen, C. E. van der Schoot, A. M. van Pelt, and S. Repping. Eliminating acute lymphoblastic leukemia cells from human testicular cell cultures: a pilot study. Fertil Steril 101:1072–1078.e1, 2014.

    Article  PubMed  Google Scholar 

  77. Sasaki, T., R. Fassler, and E. Hohenester. Laminin: the crux of basement membrane assembly. J. Cell Biol. 164:959–963, 2004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Schlatt, S., B. Westernstroer, K. Gassei, and J. Ehmcke. Donor-host involvement in immature rat testis xenografting into nude mouse hosts. Biol. Reprod. 82:888–895, 2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Schmidt, J. A., J. M. de Avila, and D. J. McLean. Effect of vascular endothelial growth factor and testis tissue culture on spermatogenesis in bovine ectopic testis tissue xenografts. Biol. Reprod. 75:167–175, 2006.

    Article  CAS  PubMed  Google Scholar 

  80. Schover, L. R., K. Brey, A. Lichtin, L. I. Lipshultz, and S. Jeha. Knowledge and experience regarding cancer, infertility, and sperm banking in younger male survivors. J. Clin. Oncol. 20:1880–1889, 2002.

    Article  PubMed  Google Scholar 

  81. Shetty, G., and M. L. Meistrich. The missing niche for spermatogonial stem cells: do blood vessels point the way? Cell Stem Cell 1:361–363, 2007.

    Article  CAS  PubMed  Google Scholar 

  82. Shikanov, A., Z. Zhang, M. Xu, R. M. Smith, A. Rajan, T. K. Woodruff, and L. D. Shea. Fibrin encapsulation and vascular endothelial growth factor delivery promotes ovarian graft survival in mice. Tissue Eng. Part A 17:3095–3104, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Shinohara, T., K. Inoue, N. Ogonuki, M. Kanatsu-Shinohara, H. Miki, K. Nakata, M. Kurome, H. Nagashima, S. Toyokuni, K. Kogishi, T. Honjo, and A. Ogura. Birth of offspring following transplantation of cryopreserved immature testicular pieces and in vitro microinsemination. Hum. Reprod. 17:3039–3045, 2002.

    Article  CAS  PubMed  Google Scholar 

  84. Silva, E. A., and D. J. Mooney. Effects of VEGF temporal and spatial presentation on angiogenesis. Biomaterials 31:1235–1241, 2010.

    Article  CAS  PubMed  Google Scholar 

  85. Simon-Yarza, T., F. R. Formiga, E. Tamayo, B. Pelacho, F. Prosper, and M. J. Blanco-Prieto. Vascular endothelial growth factor-delivery systems for cardiac repair: an overview. Theranostics 2:541–552, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Taylor, K. R., and R. L. Gallo. Glycosaminoglycans and their proteoglycans: host-associated molecular patterns for initiation and modulation of inflammation. FASEB J. 20:9–22, 2006.

    Article  CAS  PubMed  Google Scholar 

  87. Turkmen, S., A. Mentese, E. Karaguzel, Y. Karaca, A. Kucuk, A. Uzun, E. Yulug, and S. Turedi. A comparison of the effects of N-acetylcysteine and ethyl pyruvate on experimental testicular ischemia-reperfusion injury. Fertil. Steril. 98:626–631, 2012.

    Article  CAS  PubMed  Google Scholar 

  88. Van Eyck, A. S., C. Bouzin, O. Feron, L. Romeu, A. Van Langendonckt, J. Donnez, and M. M. Dolmans. Both host and graft vessels contribute to revascularization of xenografted human ovarian tissue in a murine model. Fertil. Steril. 93:1676–1685, 2010.

    Article  PubMed  Google Scholar 

  89. Van Saen, D., E. Goossens, C. Bourgain, A. Ferster, and H. Tournaye. Meiotic activity in orthotopic xenografts derived from human postpubertal testicular tissue. Hum. Reprod. 26:282–293, 2011.

    Article  PubMed  Google Scholar 

  90. Van Saen, D., E. Goossens, P. Haentjens, Y. Baert, and H. Tournaye. Exogenous administration of recombinant human FSH does not improve germ cell survival in human prepubertal xenografts. Reprod. Biomed. Online 26:286–298, 2013.

    Article  PubMed  Google Scholar 

  91. Vanacker, J., M. M. Dolmans, V. Luyckx, J. Donnez, and C. A. Amorim. First transplantation of isolated murine follicles in alginate. Regen. Med. 9:609–619, 2014.

    Article  CAS  PubMed  Google Scholar 

  92. Vanacker, J., V. Luyckx, M. M. Dolmans, A. Des Rieux, J. Jaeger, A. Van Langendonckt, J. Donnez, and C. A. Amorim. 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, 2012.

    Article  CAS  PubMed  Google Scholar 

  93. Wang, P., X. Jiang, Y. Jiang, X. Hu, H. Mou, M. Li, and H. Guan. In vitro antioxidative activities of three marine oligosaccharides. Nat. Prod. Res. 21:646–654, 2007.

    Article  PubMed  Google Scholar 

  94. Wyns, C., M. Curaba, B. Martinez-Madrid, A. Van Langendonckt, W. Francois-Xavier, and J. Donnez. Spermatogonial survival after cryopreservation and short-term orthotopic immature human cryptorchid testicular tissue grafting to immunodeficient mice. Hum. Reprod. 22:1603–1611, 2007.

    Article  PubMed  Google Scholar 

  95. Wyns, C., M. Curaba, S. Petit, B. Vanabelle, P. Laurent, J. F. Wese, and J. Donnez. Management of fertility preservation in prepubertal patients: 5 years’ experience at the Catholic University of Louvain. Hum. Reprod. 26:737–747, 2011.

    Article  CAS  PubMed  Google Scholar 

  96. Wyns, C., M. Curaba, B. Vanabelle, A. Van Langendonckt, and J. Donnez. Options for fertility preservation in prepubertal boys. Hum. Reprod. Update 16:312–328, 2010.

    Article  PubMed  Google Scholar 

  97. Wyns, C., A. Van Langendonckt, F. X. Wese, J. Donnez, and M. Curaba. Long-term spermatogonial survival in cryopreserved and xenografted immature human testicular tissue. Hum. Reprod. 23:2402–2414, 2008.

    Article  PubMed  Google Scholar 

  98. Yildiz, C., B. Mullen, K. Jarvi, C. McKerlie, and K. C. Lo. Effect of different cryoprotectant agents on spermatogenesis efficiency in cryopreserved and grafted neonatal mouse testicular tissue. Cryobiology 67:70–75, 2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Zhang, Y. S., K. Yue, J. Aleman, K. Mollazadeh-Moghaddam, S. M. Bakht, J. Yang, W. Jia, V. Dell’Erba, P. Assawes, S. R. Shin, M. R. Dokmeci, R. Oklu, and A. Khademhosseini. 3D bioprinting for tissue and organ fabrication. Ann. Biomed. Eng. 43(3):730–746, 2016.

    Google Scholar 

Download references

Acknowledgments

The authors thank Mira Hryniuk, B.A., for reviewing the English language of the manuscript.

Funding

Studies conducted at the UCL were supported by grants from the Fonds National de la Recherche Scientifique de Belgique (Télévie Grants 7.4619.05; 7. 4.572.09.F; 7.4616.11.F; 7.4596.13; 7.4512.15) and the Fondation Salus Sanguinis. Anne des Rieux is a research associate from the FRS-FNRS (Fonds de la Recherche Scientifique, Belgique) and is a recipient of subsidies from the Fonds Spéciaux de Recherche Scientifique (FSR, UCL).

Author information

Authors and Affiliations

  1. Gynecology-Andrology Research Unit, Medical School, Institut de Recherche Expérimentale et Clinique, Université Catholique de Louvain, 1200, Brussels, Belgium

    Maxime Vermeulen, Jonathan Poels, Francesca de Michele & Christine Wyns

  2. Department of Gynecology-Andrology, Université Catholique de Louvain, Cliniques Universitaires Saint-Luc, Avenue Hippocrate 10, 1200, Brussels, Belgium

    Jonathan Poels, Francesca de Michele & Christine Wyns

  3. Advanced Drug Delivery and Biomaterials Unit, Louvain Drug Research Institute, Université Catholique de Louvain, 1200, Brussels, Belgium

    Anne des Rieux

  4. Institute of Condensed Matter and Nanosciences, Université Catholique de Louvain, 1348, Louvain-la-Neuve, Belgium

    Anne des Rieux

Authors
  1. Maxime Vermeulen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jonathan Poels
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Francesca de Michele
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anne des Rieux
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Christine Wyns
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christine Wyns.

Additional information

Associate Editor Christiani Amorim oversaw the review of this article.

An erratum to this article is available at http://dx.doi.org/10.1007/s10439-017-1807-7.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vermeulen, M., Poels, J., de Michele, F. et al. Restoring Fertility with Cryopreserved Prepubertal Testicular Tissue: Perspectives with Hydrogel Encapsulation, Nanotechnology, and Bioengineered Scaffolds. Ann Biomed Eng 45, 1770–1781 (2017). https://doi.org/10.1007/s10439-017-1789-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-017-1789-5

Keywords

Search

Navigation