User menu

Accès à distance ? S'identifier sur le proxy UCLouvain

Tissue Engineering to Improve Immature Testicular Tissue and Cell Transplantation Outcomes: One Step Closer to Fertility Restoration for Prepubertal Boys Exposed to Gonadotoxic Treatments

Primary tabs

download
  • Open access
  • PDF
  • 2.82 M
Del Vento, Federico [UCL] Vermeulen, Maxime [UCL] de Michele, Francesca [UCL] Giudice, Maria [UCL] Poels, Jonathan [UCL] des Rieux, Anne [UCL] Wyns, Christine [UCL]

Despite their important contribution to the cure of both oncological and benign diseases, gonadotoxic therapies present the risk of a severe impairment of fertility. Sperm cryopreservation is not an option to preserve prepubertal boys’ reproductive potential, as their seminiferous tubules only contain spermatogonial stem cells (as diploid precursors of spermatozoa). Cryobanking of human immature testicular tissue (ITT) prior to gonadotoxic therapies is an accepted practice. Evaluation of cryopreserved ITT using xenotransplantation in nude mice showed the survival of a limited proportion of spermatogonia and their ability to proliferate and initiate differentiation. However, complete spermatogenesis could not be achieved in the mouse model. Loss of germ cells after ITT grafting points to the need to optimize the transplantation technique. Tissue engineering, a new branch of science that aims at improving cellular environment using scaffolds and molecules administration, might be an approach for further progress. In this review, after summarizing the lessons learned from human prepubertal testicular germ cells or tissue xenotransplantation experiments, we will focus on the benefits that might be gathered using bioengineering techniques to enhance transplantation outcomes by optimizing early tissue graft revascularization, protecting cells from toxic insults linked to ischemic injury and exploring strategies to promote cellular differentiation.

Document type Article de périodique (Journal article) – Synthèse de littérature
Access type Accès libre
Publication date 2018
Language Anglais
Journal information "International Journal of Molecular Sciences" - Vol. 19, no. 1, p. 286 [1-24] (2018)
Peer reviewed yes
Publisher MDPI AG ((Switzerland) Basel)
e-issn 1422-0067
Publication status Publié
Affiliations UCL - SSS/IREC/GYNE - Pôle de Gynécologie
UCL - (SLuc) Service de gynécologie et d'andrologie
Keywords Prepubertal ; Male fertility ; Fertility preservation ; Fertility after cancer ; Spermatogenesis ; Testicular tissue ; Spermatogonial stem cells ; Transplantation ; Tissue engineering ; Nanoparticles
Links
  1. Gatta Gemma, Zigon Giulia, Capocaccia Riccardo, Coebergh Jan Willem, Desandes Emmanuel, Kaatsch Peter, Pastore Guido, Peris-Bonet Rafael, Stiller Charles A., Survival of European children and young adults with cancer diagnosed 1995–2002, 10.1016/j.ejca.2008.11.042
  2. Jahnukainen Kirsi, Mitchell Rod T., Stukenborg Jan-Bernd, Testicular function and fertility preservation after treatment for haematological cancer : , 10.1097/med.0000000000000156
  3. Wyns C., Curaba M., Vanabelle B., Van Langendonckt A., Donnez J., Options for fertility preservation in prepubertal boys, 10.1093/humupd/dmp054
  4. Lukusa Aimé Kazadi, Vermylen Christiane, Vanabelle Bernard, Curaba Mara, Brichard Benedicte, Chantrain Christophe, Dupont Sophie, Ferrant Augustin, Wyns Christine, BONE MARROW TRANSPLANTATION OR HYDROXYUREA FOR SICKLE CELL ANEMIA: Long-Term Effects on Semen Variables and Hormone Profiles, 10.1080/07357900902892780
  5. Lee Stephanie J., Schover Leslie R., Partridge Ann H., Patrizio Pasquale, Wallace W. Hamish, Hagerty Karen, Beck Lindsay N., Brennan Lawrence V., Oktay Kutluk, American Society of Clinical Oncology Recommendations on Fertility Preservation in Cancer Patients, 10.1200/jco.2006.06.5888
  6. Schover Leslie R., Rybicki Lisa A., Martin Beth Anne, Bringelsen Karen A., Having children after cancer : A pilot survey of survivors' attitudes and experiences, 10.1002/(sici)1097-0142(19990815)86:4<697::aid-cncr20>3.0.co;2-j
  7. Wyns C., Collienne C., Shenfield F., Robert A., Laurent P., Roegiers L., Brichard B., Fertility preservation in the male pediatric population: factors influencing the decision of parents and children, 10.1093/humrep/dev161
  8. Ginsberg Jill P., Li Yimei, Carlson Claire A., Gracia Clarisa R., Hobbie Wendy L., Miller Victoria A., Mulhall John, Shnorhavorian Margarett, Brinster Ralph L., Kolon Thomas F., Testicular tissue cryopreservation in prepubertal male children: An analysis of parental decision-making : Testicular Tissue Cryopreservation, 10.1002/pbc.25078
  9. van den Berg H., Repping S., van der Veen F., Parental desire and acceptability of spermatogonial stem cell cryopreservation in boys with cancer, 10.1093/humrep/del375
  10. Clermont, Arch. Anat. Microsc. Morphol. Exp., 56, 7 (1967)
  11. Keros Victoria, Hultenby Kjell, Borgström Birgit, Fridström Margareta, Jahnukainen Kirsi, Hovatta Outi, Methods of cryopreservation of testicular tissue with viable spermatogonia in pre-pubertal boys undergoing gonadotoxic cancer treatment, 10.1093/humrep/del508
  12. Wyns Christine, Curaba Mara, Martinez-Madrid Belen, Van Langendonckt Anne, François-Xavier Wese, Donnez Jacques, Spermatogonial survival after cryopreservation and short-term orthotopic immature human cryptorchid testicular tissue grafting to immunodeficient mice, 10.1093/humrep/dem062
  13. Wyns C., Curaba M., Petit S., Vanabelle B., Laurent P., Wese J.-F.X., Donnez J., Management of fertility preservation in prepubertal patients: 5 years’ experience at the Catholic University of Louvain, 10.1093/humrep/deq387
  14. Picton Helen M., Wyns Christine, Anderson Richard A., Goossens Ellen, Jahnukainen Kirsi, Kliesch Sabine, Mitchell Rod T., Pennings G., Rives Natalie, Tournaye Herman, van Pelt Ans M.M., Eichenlaub-Ritter Ursula, Schlatt Stefan, A European perspective on testicular tissue cryopreservation for fertility preservation in prepubertal and adolescent boys, 10.1093/humrep/dev190
  15. Ogawa Takehiko, Ohmura Masako, Ohbo Kazuyuki, The Niche for Spermatogonial Stem Cells in the Mammalian Testis, 10.1532/ijh97.05088
  16. Wyns C., Van Langendonckt A., Wese F.-X., Donnez J., Curaba M., Long-term spermatogonial survival in cryopreserved and xenografted immature human testicular tissue, 10.1093/humrep/den272
  17. Kim Tae H., Hargreaves Hilary K., Chan Wing C., Brynes Russell K., Alvarado Carlos, Woodard John, Ragab Abdelsalam H., Sequential testicular biopsies in childhood acute lymphocytic leukemia, 10.1002/1097-0142(19860301)57:5<1038::aid-cncr2820570527>3.0.co;2-1
  18. Hou M., Andersson M., Eksborg S., Soder O., Jahnukainen K., Xenotransplantation of testicular tissue into nude mice can be used for detecting leukemic cell contamination, 10.1093/humrep/dem085
  19. de Michele Francesca, Vermeulen Maxime, Wyns Christine, Fertility restoration with spermatogonial stem cells : , 10.1097/med.0000000000000370
  20. de Michele F., Poels J., Weerens L., Petit C., Evrard Z., Ambroise J., Gruson D., Wyns C., 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, 10.1093/humrep/dew300
  21. Donnez J, Dolmans MM, Demylle D, Jadoul P, Pirard C, Squifflet J, Martinez-Madrid B, Van Langendonckt A, Livebirth after orthotopic transplantation of cryopreserved ovarian tissue, 10.1016/s0140-6736(04)17222-x
  22. Jadoul P., Guilmain A., Squifflet J., Luyckx M., Votino R., Wyns C., Dolmans M.M., Efficacy of ovarian tissue cryopreservation for fertility preservation: lessons learned from 545 cases, 10.1093/humrep/dex040
  23. Chiti M. C., Dolmans M. M., Donnez J., Amorim C. A., Fibrin in Reproductive Tissue Engineering: A Review on Its Application as a Biomaterial for Fertility Preservation, 10.1007/s10439-017-1817-5
  24. Demeestere Isabelle, Simon Philippe, Dedeken Laurence, Moffa Federica, Tsépélidis Sophie, Brachet Cecile, Delbaere Anne, Devreker Fabienne, Ferster Alina, Live birth after autograft of ovarian tissue cryopreserved during childhood: Figure 1, 10.1093/humrep/dev128
  25. Van Eyck Anne-Sophie, Jordan Bénédicte Francine, Gallez Bernard, Heilier Jean-François, Van Langendonckt Anne, Donnez Jacques, Electron paramagnetic resonance as a tool to evaluate human ovarian tissue reoxygenation after xenografting, 10.1016/j.fertnstert.2008.05.012
  26. Dolmans M.-M., Martinez-Madrid B., Gadisseux E., Guiot Y., Yuan W. Y., Torre A., Camboni A., Van Langendonckt A., Donnez J., Short-term transplantation of isolated human ovarian follicles and cortical tissue into nude mice, 10.1530/rep-07-0131
  27. Goossens Ellen, Geens Mieke, De Block Gert, Tournaye Herman, Spermatogonial survival in long-term human prepubertal xenografts, 10.1016/j.fertnstert.2007.09.044
  28. Sato Y., Nozawa S., Yoshiike M., Arai M., Sasaki C., Iwamoto T., Xenografting of testicular tissue from an infant human donor results in accelerated testicular maturation, 10.1093/humrep/deq001
  29. Van Saen Dorien, Goossens Ellen, Haentjens Patrick, Baert Yoni, Tournaye Herman, Exogenous administration of recombinant human FSH does not improve germ cell survival in human prepubertal xenografts, 10.1016/j.rbmo.2012.11.013
  30. Poels J., Van Langendonckt A., Many M.-C., Wese F.-X., Wyns C., Vitrification preserves proliferation capacity in human spermatogonia, 10.1093/humrep/des455
  31. Poels Jonathan, Abou-Ghannam Gaël, Herman Sophie, Van Langendonckt Anne, Wese François-Xavier, Wyns Christine, In Search of Better Spermatogonial Preservation by Supplementation of Cryopreserved Human Immature Testicular Tissue Xenografts with N-acetylcysteine and Testosterone, 10.3389/fsurg.2014.00047
  32. Schlatt S., Honaramooz A., Ehmcke J., Goebell P.J., Rübben H., Dhir R., Dobrinski I., Patrizio P., Limited survival of adult human testicular tissue as ectopic xenograft, 10.1093/humrep/dei352
  33. Benjamin, Development, 125, 1591 (1998)
  34. Geens Mieke, De Block Gert, Goossens Ellen, Frederickx Veerle, Van Steirteghem André, Tournaye Herman, Spermatogonial survival after grafting human testicular tissue to immunodeficient mice, 10.1093/humrep/dei412
  35. Van Saen D., Goossens E., Bourgain C., Ferster A., Tournaye H., Meiotic activity in orthotopic xenografts derived from human postpubertal testicular tissue, 10.1093/humrep/deq321
  36. Kuhn Howard E., The Onset of Sperm Production in Pubertal Boys : Relationship to Gonadotropin Excretion, 10.1001/archpedi.1989.02150140080024
  37. Honaramooz Ali, Snedaker Amy, Boiani Michele, Schöler Hans, Dobrinski Ina, Schlatt Stefan, Sperm from neonatal mammalian testes grafted in mice, 10.1038/nature00918
  38. Jahnukainen K., Ehmcke J., Nurmio M., Schlatt S., Autologous Ectopic Grafting of Cryopreserved Testicular Tissue Preserves the Fertility of Prepubescent Monkeys That Receive Sterilizing Cytotoxic Therapy, 10.1158/0008-5472.can-12-1317
  39. Shinohara T., Birth of offspring following transplantation of cryopreserved immature testicular pieces and in-vitro microinsemination, 10.1093/humrep/17.12.3039
  40. Snedaker Amy K., Honaramooz Ali, Dobrinski Ina, A Game of Cat and Mouse: Xenografting of Testis Tissue From Domestic Kittens Results in Complete Cat Spermatogenesis in a Mouse Host, 10.1002/j.1939-4640.2004.tb03163.x
  41. Abrishami M., Anzar M., Yang Y., Honaramooz A., Cryopreservation of immature porcine testis tissue to maintain its developmental potential after xenografting into recipient mice, 10.1016/j.theriogenology.2009.08.004
  42. Yildiz Cengiz, Mullen Brendan, Jarvi Keith, McKerlie Colin, Lo Kirk C., Effect of different cryoprotectant agents on spermatogenesis efficiency in cryopreserved and grafted neonatal mouse testicular tissue, 10.1016/j.cryobiol.2013.05.004
  43. Pukazhenthi Budhan S., Nagashima Jennifer, Travis Alexander J., Costa Guilherme M., Escobar Enrique N., França Luiz R., Wildt David E., Slow Freezing, but Not Vitrification Supports Complete Spermatogenesis in Cryopreserved, Neonatal Sheep Testicular Xenografts, 10.1371/journal.pone.0123957
  44. Liu Jianan, Cheng Kimberly M., Silversides Frederick G., Production of Live Offspring from Testicular Tissue Cryopreserved by Vitrification Procedures in Japanese Quail (Coturnix japonica)1, 10.1095/biolreprod.113.108951
  45. Ohta Hiroshi, Wakayama Teruhiko, Generation of Normal Progeny by Intracytoplasmic Sperm Injection Following Grafting of Testicular Tissue from Cloned Mice That Died Postnatally1, 10.1095/biolreprod.105.041673
  46. Kaneko Hiroyuki, Kikuchi Kazuhiro, Nakai Michiko, Somfai Tamas, Noguchi Junko, Tanihara Fuminori, Ito Junya, Kashiwazaki Naomi, Generation of Live Piglets for the First Time Using Sperm Retrieved from Immature Testicular Tissue Cryopreserved and Grafted into Nude Mice, 10.1371/journal.pone.0070989
  47. Liu Zhen, Nie Yan-Hong, Zhang Chen-Chen, Cai Yi-Jun, Wang Yan, Lu Hui-Ping, Li Yu-Zhuo, Cheng Cheng, Qiu Zi-Long, Sun Qiang, Generation of macaques with sperm derived from juvenile monkey testicular xenografts, 10.1038/cr.2015.112
  48. Vermeulen Maxime, Poels Jonathan, de Michele Francesca, des Rieux Anne, Wyns Christine, Restoring Fertility with Cryopreserved Prepubertal Testicular Tissue: Perspectives with Hydrogel Encapsulation, Nanotechnology, and Bioengineered Scaffolds, 10.1007/s10439-017-1789-5
  49. Schlatt S, Kim S., Gosden R, Spermatogenesis and steroidogenesis in mouse, hamster and monkey testicular tissue after cryopreservation and heterotopic grafting to castrated hosts, 10.1530/rep.0.1240339
  50. Arregui L., Dobrinski I., Xenografting of testicular tissue pieces: 12 years of an in vivo spermatogenesis system, 10.1530/rep-14-0249
  51. Schlatt Stefan, Westernströer Birgit, Gassei Kathrin, Ehmcke Jens, Donor-Host Involvement in Immature Rat Testis Xenografting into Nude Mouse Hosts1, 10.1095/biolreprod.109.082073
  52. Andrejecsk Jillian W., Cui Jiajia, Chang William G., Devalliere Julie, Pober Jordan S., Saltzman W. Mark, Paracrine exchanges of molecular signals between alginate-encapsulated pericytes and freely suspended endothelial cells within a 3D protein gel, 10.1016/j.biomaterials.2013.08.008
  53. Chan Frank, Allison John E., Stanley Allan J., Gumbreck Laurence G., Reciprocal Transplantation of Testes Between Normal and Pseudohermaphroditic Male Rats, 10.1016/s0015-0282(16)37037-6
  54. Johnson Larry, Suggs Lisa C., Norton Yvonne M., Zeh Wayne C., Effect of Developmental Age or Time after Transplantation on Sertoli Cell Number and Testicular Size in Inbred Fischer Rats1, 10.1095/biolreprod54.5.948
  55. Wistuba Joachim, Luetjens C. Marc, Wesselmann Ramona, Nieschlag Eberhard, Simoni Manuela, Schlatt Stefan, Meiosis in Autologous Ectopic Transplants of Immature Testicular Tissue Grafted to Callithrix jacchus1, 10.1095/biolreprod.105.048793
  56. Marc Luetjens C., Stukenborg Jan-Bernd, Nieschlag Eberhard, Simoni Manuela, Wistuba Joachim, Complete Spermatogenesis in Orthotopic But Not in Ectopic Transplants of Autologously Grafted Marmoset Testicular Tissue, 10.1210/en.2007-1325
  57. Van Saen Dorien, Goossens Ellen, De Block Gert, Tournaye Herman, Regeneration of spermatogenesis by grafting testicular tissue or injecting testicular cells into the testes of sterile mice: a comparative study, 10.1016/j.fertnstert.2008.02.100
  58. Oatley Jon M., Reeves Jerry J., McLean Derek J., Establishment of Spermatogenesis in Neonatal Bovine Testicular Tissue Following Ectopic Xenografting Varies with Donor Age1, 10.1095/biolreprod.104.030783
  59. Schmidt Jonathan A., de Avila Jeanene M., McLean Derek J., Grafting Period and Donor Age Affect the Potential for Spermatogenesis in Bovine Ectopic Testis Xenografts, 10.1095/biolreprod.105.049825
  60. Jahnukainen Kirsi, Ehmcke Jens, Hergenrother Scott D., Schlatt Stefan, Effect of cold storage and cryopreservation of immature non-human primate testicular tissue on spermatogonial stem cell potential in xenografts, 10.1093/humrep/del471
  61. Potter Sarah J, DeFalco Tony, Role of the testis interstitial compartment in spermatogonial stem cell function, 10.1530/rep-16-0588
  62. Schlatt Stefan, Honaramooz Ali, Boiani Michele, Schöler Hans R., Dobrinski Ina, Progeny from Sperm Obtained after Ectopic Grafting of Neonatal Mouse Testes1, 10.1095/biolreprod.102.014894
  63. Honaramooz Ali, Li Ming-Wen, Penedo M. Cecilia T., Meyers Stuart, Dobrinski Ina, Accelerated Maturation of Primate Testis by Xenografting into Mice1, 10.1095/biolreprod.103.025536
  64. Schlatt Stefan, Gassei Kathrin, Westernströer Birgit, Ehmcke Jens, Modulating Testicular Mass in Xenografting: A Model to Explore Testis Development and Endocrine Function, 10.1210/en.2010-0415
  65. Wistuba Joachim, Mundry Marvin, Luetjens C. Marc, Schlatt Stefan, CoGrafting of Hamster (Phodopus sungorus) and Marmoset (Callithrix jacchus) Testicular Tissues into Nude Mice Does Not Overcome Blockade of Early Spermatogenic Differentiation in Primate Grafts1, 10.1095/biolreprod.104.033431
  66. Rathi Rahul, Zeng Wenxian, Megee Susan, Conley Alan, Meyers Stuart, Dobrinski Ina, Maturation of Testicular Tissue from Infant Monkeys after Xenografting into Mice, 10.1210/en.2008-0311
  67. Ehmcke J., Gassei K., Westernströer B., Schlatt S., Immature rhesus monkey (Macaca mulatta) testis xenografts show increased growth, but not enhanced seminiferous differentiation, under human chorionic gonadotropin treatment of nude mouse recipients : Gonadotropin action on monkey xenografts, 10.1111/j.1365-2605.2011.01179.x
  68. Rathi R, Honaramooz A, Zeng W, Turner R, Dobrinski I, Germ cell development in equine testis tissue xenografted into mice, 10.1530/rep.1.01101
  69. Marchlewska Katarzyna, Kula Krzysztof, Walczak-Jedrzejowska Renata, Kula Wojciech, Oszukowska Elzbieta, Filipiak Eliza, Moszura Tomasz, Slowikowska-Hilczer Jolanta, Experimental research Maturational changes in connexin 43 expression in the seminiferous tubules may depend on thyroid hormone action, 10.5114/aoms.2013.33074
  70. Rodriguez-Sosa J. R., Costa G. M. J., Rathi R., Franca L. R., Dobrinski I., Endocrine modulation of the recipient environment affects development of bovine testis tissue ectopically grafted in mice, 10.1530/rep-12-0020
  71. Turner T. T., Tung Kenneth S.K., Tomomasa Hiroshi, Wilson Leigh W., Acute Testicular Ischemia Results in Germ Cell-Specific Apoptosis in the Rat1, 10.1095/biolreprod57.6.1267
  72. Yancopoulos George D., Davis Samuel, Gale Nicholas W., Rudge John S., Wiegand Stanley J., Holash Jocelyn, 10.1038/35025215
  73. Lee K., Silva E. A., Mooney D. J., Growth factor delivery-based tissue engineering: general approaches and a review of recent developments, 10.1098/rsif.2010.0223
  74. Mitchell Aaron C., Briquez Priscilla S., Hubbell Jeffrey A., Cochran Jennifer R., Engineering growth factors for regenerative medicine applications, 10.1016/j.actbio.2015.11.007
  75. Caires Kyle C., de Avila Jeanene M., Cupp Andrea S., McLean Derek J., VEGFA Family Isoforms Regulate Spermatogonial Stem Cell Homeostasisin Vivo, 10.1210/en.2011-1323
  76. Ergün S, Kiliç N, Fiedler W, Mukhopadhyay A.K, Vascular endothelial growth factor and its receptors in normal human testicular tissue, 10.1016/s0303-7207(97)00082-8
  77. Tian Ruhui, Yang Shi, Zhu Yong, Zou Shasha, Li Peng, Wang Junlong, Zhu Zijue, Huang Yiran, He Zuping, Li Zheng, VEGF/VEGFR2 Signaling Regulates Germ Cell Proliferation in vitro and Promotes Mouse Testicular Regeneration in vivo, 10.1159/000440949
  78. Schmidt Jonathan A., de Avila Jeanene M., McLean Derek J., Effect of Vascular Endothelial Growth Factor and Testis Tissue Culture on Spermatogenesis in Bovine Ectopic Testis Tissue Xenografts, 10.1095/biolreprod.105.049817
  79. Caires K. C, de Avila J., McLean D. J, Vascular endothelial growth factor regulates germ cell survival during establishment of spermatogenesis in the bovine testis, 10.1530/rep-09-0020
  80. Zafarullah M., Li W. Q., Sylvester J., Ahmad M., Molecular mechanisms of N -acetylcysteine actions, 10.1007/s000180300001
  81. Çay Ali, Alver Ahmet, Küçük Murat, Işik Osman, Eminağaoğlu M. Selçuk, Karahan S. Caner, Değer Orhan, The Effects of N-Acetylcysteine on Antioxidant Enzyme Activities in Experimental Testicular Torsion, 10.1016/j.jss.2005.11.572
  82. Turkmen Suha, Mentese Ahmet, Karaguzel Ersagun, Karaca Yunus, Kucuk Adem, Uzun Aysegul, Yulug Esin, Turedi Suleyman, A comparison of the effects of N-acetylcysteine and ethyl pyruvate on experimental testicular ischemia-reperfusion injury, 10.1016/j.fertnstert.2012.05.034
  83. Erkkila K., N-Acetyl-L-Cysteine Inhibits Apoptosis in Human Male Germ Cells in Vitro, 10.1210/jc.83.7.2523
  84. Poeggeler B., Reiter R. J., Hardeland R., Tan D. -X., Barlow-Walden L. R., Melatonin and structurally-related, endogenous indoles act as potent electron donors and radical scavengers in vitro, 10.1080/13510002.1996.11747046
  85. Gholami, Iran. J. Basic Med. Sci., 17, 93 (2014)
  86. Navid Shadan, Rastegar Tayebeh, Baazm Maryam, Alizadeh Rafieh, Talebi Ali, Gholami Keykavos, Khosravi-Farsani Somayeh, Koruji Morteza, Abbasi Mehdi, In vitro effects of melatonin on colonization of neonate mouse spermatogonial stem cells, 10.1080/19396368.2017.1358774
  87. Gholami, Iran. J. Basic Med. Sci., 16, 906 (2013)
  88. Kimsa Magdalena, Strzalka-Mrozik Barbara, Kimsa Malgorzata, Gola Joanna, Nicholson Peter, Lopata Krzysztof, Mazurek Urszula, Porcine Endogenous Retroviruses in Xenotransplantation—Molecular Aspects, 10.3390/v6052062
  89. Nomi Masashi, Atala Anthony, Coppi Paolo De, Soker Shay, Principals of neovascularization for tissue engineering, 10.1016/s0098-2997(02)00008-0
  90. Vajanto Ismo, Rissanen Tuomas T., Rutanen Juha, Hiltunen Mikko O., Tuomisto Tiina T., Arve Katja, Närvänen Outi, Manninen Hannu, Räsänen Heikki, Hippeläinen Mikko, Alhava Esko, Ylä-Herttuala Seppo, Evaluation of angiogenesis and side effects in ischemic rabbit hindlimbs after intramuscular injection of adenoviral vectors encoding VEGF andLacZ : Gene Therapy for Angiogenesis, 10.1002/jgm.287
  91. Ferrara Napoleone, Davis-Smyth Terri, The Biology of Vascular Endothelial Growth Factor, 10.1210/edrv.18.1.0287
  92. Folkman Judah, Role of angiogenesis in tumor growth and metastasis, 10.1053/sonc.2002.37263
  93. Moulisová Vladimíra, Gonzalez-García Cristina, Cantini Marco, Rodrigo-Navarro Aleixandre, Weaver Jessica, Costell Mercedes, Sabater i Serra Roser, Dalby Matthew J., García Andrés J., Salmerón-Sánchez Manuel, Engineered microenvironments for synergistic VEGF – Integrin signalling during vascularization, 10.1016/j.biomaterials.2017.02.024
  94. Brinster R. L., Zimmermann J. W., Spermatogenesis following male germ-cell transplantation., 10.1073/pnas.91.24.11298
  95. Brook Philip F, Radford John A, Shalet Steven M, Joyce Adrian D, Gosden Roger G, Isolation of germ cells from human testicular tissue for low temperature storage and autotransplantation, 10.1016/s0015-0282(00)01721-0
  96. Kanatsu-Shinohara M., Restoration of fertility in infertile mice by transplantation of cryopreserved male germline stem cells, 10.1093/humrep/deg483
  97. Schlatt S., Germ cell transfer into rat, bovine, monkey and human testes, 10.1093/humrep/14.1.144
  98. Ning Liang, Meng Jie, Goossens Ellen, Lahoutte Tony, Marichal Miriam, Tournaye Herman, In search of an efficient injection technique for future clinical application of spermatogonial stem cell transplantation: infusion of contrast dyes in isolated cadaveric human testes, 10.1016/j.fertnstert.2012.08.023
  99. Clouthier David E., Avarbock Mary R., Maika Shanna D., Hammer Robert E., Brinster Ralph L., Rat spermatogenesis in mouse testis, 10.1038/381418a0
  100. Ogawa Takehiko, Dobrinski Ina, Avarbock Mary R., Brinster Ralph L., Xenogeneic Spermatogenesis Following Transplantation of Hamster Germ Cells to Mouse Testes1, 10.1095/biolreprod60.2.515
  101. Russell, J. Androl., 17, 615 (1996)
  102. Nagano Makoto, Patrizio Pasquale, Brinster Ralph L, Long-term survival of human spermatogonial stem cells in mouse testes, 10.1016/s0015-0282(02)04345-5
  103. Wu X., Schmidt J. A., Avarbock M. R., Tobias J. W., Carlson C. A., Kolon T. F., Ginsberg J. P., Brinster R. L., Prepubertal human spermatogonia and mouse gonocytes share conserved gene expression of germline stem cell regulatory molecules, 10.1073/pnas.0912432106
  104. Sadri-Ardekani Hooman, In Vitro Propagation of Human Prepubertal Spermatogonial Stem Cells, 10.1001/jama.2011.791
  105. Radford J., Shalet S., Lieberman B., Fertility after treatment for cancer, 10.1136/bmj.319.7215.935
  106. Radford John, Restoration of Fertility after Treatment for Cancer, 10.1159/000067840
  107. Müller Jørn, Skakkebæk Niels E., Quantification of germ cells and seminiferous tubules by stereological examination of testicles from 50 boys who suffered from sudden death, 10.1111/j.1365-2605.1983.tb00333.x
  108. Dobrinski Ina, Ogawa Takehiko, Avarbock Mary R., Brinster Ralph L., Computer assisted image analysis to assess colonization of recipient seminiferous tubules by spermatogonial stem cells from transgenic donor mice, 10.1002/(sici)1098-2795(199906)53:2<142::aid-mrd3>3.0.co;2-o
  109. Sadri-Ardekani Hooman, Propagation of Human Spermatogonial Stem Cells In Vitro, 10.1001/jama.2009.1689
  110. Mirzapour T., Movahedin M., Koruji M., Nowroozi M. R., Xenotransplantation assessment: morphometric study of human spermatogonial stem cells in recipient mouse testes, 10.1111/and.12310
  111. Conrad Sabine, Azizi Hossein, Hatami Maryam, Kubista Mikael, Bonin Michael, Hennenlotter Jörg, Renninger Markus, Skutella Thomas, Differential Gene Expression Profiling of Enriched Human Spermatogonia after Short- and Long-Term Culture, 10.1155/2014/138350
  112. Gat Itai, Maghen Leila, Filice Melissa, Kenigsberg Shlomit, Wyse Brandon, Zohni Khaled, Saraz Peter, Fisher Andrée Gauthier, Librach Clifford, Initial germ cell to somatic cell ratio impacts the efficiency of SSC expansion in vitro, 10.1080/19396368.2017.1406013
  113. Ko Kinarm, Araúzo-Bravo Marcos J., Tapia Natalia, Kim Julee, Lin Qiong, Bernemann Christof, Han Dong Wook, Gentile Luca, Reinhardt Peter, Greber Boris, Schneider Rebekka K., Kliesch Sabine, Zenke Martin, Schöler Hans R., Human adult germline stem cells in question, 10.1038/nature09089
  114. Bar-Shira Maymon Batia, Yogev Leah, Marks Alexander, Hauser Ron, Botchan Amnon, Yavetz Haim, Sertoli cell inactivation by cytotoxic damage to the human testis after cancer chemotherapy, 10.1016/j.fertnstert.2003.09.078
  115. Howell S. J., Radford J. A., Ryder W.D.J., Shalet S. M., Testicular Function After Cytotoxic Chemotherapy: Evidence of Leydig Cell Insufficiency, 10.1200/jco.1999.17.5.1493
  116. Fujita Kazutoshi, Ohta Hiroshi, Tsujimura Akira, Takao Tetsuya, Miyagawa Yasushi, Takada Shingo, Matsumiya Kiyomi, Wakayama Teruhiko, Okuyama Akihiko, Transplantation of spermatogonial stem cells isolated from leukemic mice restores fertility without inducing leukemia, 10.1172/jci24189
  117. Fujita K., Tsujimura A., Miyagawa Y., Kiuchi H., Matsuoka Y., Takao T., Takada S., Nonomura N., Okuyama A., Isolation of Germ Cells from Leukemia and Lymphoma Cells in a Human In vitro Model: Potential Clinical Application for Restoring Human Fertility after Anticancer Therapy, 10.1158/0008-5472.can-06-2326
  118. Geens M., Van de Velde H., De Block G., Goossens E., Van Steirteghem A., Tournaye H., The efficiency of magnetic-activated cell sorting and fluorescence-activated cell sorting in the decontamination of testicular cell suspensions in cancer patients, 10.1093/humrep/del418
  119. Dovey Serena L., Valli Hanna, Hermann Brian P., Sukhwani Meena, Donohue Julia, Castro Carlos A., Chu Tianjiao, Sanfilippo Joseph S., Orwig Kyle E., Eliminating malignant contamination from therapeutic human spermatogonial stem cells, 10.1172/jci65822
  120. Hou M., Andersson M., Zheng C., Sundblad A., Soder O., Jahnukainen K., Decontamination of leukemic cells and enrichment of germ cells from testicular samples from rats with Roser's T-cell leukemia by flow cytometric sorting, 10.1530/rep-07-0240
  121. Hermann Brian P., Sukhwani Meena, Salati Jennifer, Sheng Yi, Chu Tianjiao, Orwig Kyle E., Separating spermatogonia from cancer cells in contaminated prepubertal primate testis cell suspensions, 10.1093/humrep/der343
  122. Sadri-Ardekani Hooman, Homburg Christa H., van Capel Toni M.M., van den Berg Henk, van der Veen Fulco, van der Schoot C. Ellen, van Pelt Ans M.M., Repping Sjoerd, Eliminating acute lymphoblastic leukemia cells from human testicular cell cultures: a pilot study, 10.1016/j.fertnstert.2014.01.014
  123. Kanatsu-Shinohara M., Genetic and epigenetic properties of mouse male germline stem cells during long-term culture, 10.1242/dev.02004
  124. Nickkholgh Bita, Mizrak S. Canan, van Daalen Saskia K.M., Korver Cindy M., Sadri-Ardekani Hooman, Repping Sjoerd, van Pelt Ans M.M., Genetic and epigenetic stability of human spermatogonial stem cells during long-term culture, 10.1016/j.fertnstert.2014.08.022
  125. Fleischer Sharon, Feiner Ron, Dvir Tal, Cardiac tissue engineering: from matrix design to the engineering of bionic hearts, 10.2217/rme-2016-0150
  126. O'Brien Fergal J., Biomaterials & scaffolds for tissue engineering, 10.1016/s1369-7021(11)70058-x
  127. Richardson Thomas P., Peters Martin C., Ennett Alessandra B., Mooney David J., Polymeric system for dual growth factor delivery, 10.1038/nbt1101-1029
  128. Gorain Bapi, Tekade Muktika, Kesharwani Prashant, Iyer Arun K., Kalia Kiran, Tekade Rakesh Kumar, The use of nanoscaffolds and dendrimers in tissue engineering, 10.1016/j.drudis.2016.12.007
  129. Lee Dong Ryul, Kaproth Michael T., Parks John E., In Vitro Production of Haploid Germ Cells from Fresh or Frozen-Thawed Testicular Cells of Neonatal Bulls1, 10.1095/biolreprod65.3.873
  130. Badylak Stephen F., The extracellular matrix as a biologic scaffold material☆, 10.1016/j.biomaterials.2007.04.043
  131. Janson Isaac A., Putnam Andrew J., Extracellular matrix elasticity and topography: Material-based cues that affect cell function via conserved mechanisms : ECM ELASTICITY AND TOPOGRAPHY, 10.1002/jbm.a.35254
  132. Qazi Taimoor H., Mooney David J., Duda Georg N., Geissler Sven, Biomaterials that promote cell-cell interactions enhance the paracrine function of MSCs, 10.1016/j.biomaterials.2017.06.019
  133. Li Eric, Chang C.C., Zhang Zhongpu, Li Qing, Characterization of tissue scaffolds for time-dependent biotransport criteria – a novel computational procedure, 10.1080/10255842.2015.1124268
  134. Cheng C. Yan, Wong Elissa W.P., Yan Helen H.N., Mruk Dolores D., Regulation of spermatogenesis in the microenvironment of the seminiferous epithelium: New insights and advances, 10.1016/j.mce.2009.08.004
  135. Pöllänen Pasi P., Kallajoki Markku, Risteli Leila, Risteli Juha, Suominen Jyrki J. O., Laminin and type IV collagen in the human testis, 10.1111/j.1365-2605.1985.tb00846.x
  136. Anderson James M., Rodriguez Analiz, Chang David T., Foreign body reaction to biomaterials, 10.1016/j.smim.2007.11.004
  137. Morris Aaron H., Stamer D.K., Kyriakides T.R., The host response to naturally-derived extracellular matrix biomaterials, 10.1016/j.smim.2017.01.002
  138. Chen Yuhang, Zhou Shiwei, Li Qing, Microstructure design of biodegradable scaffold and its effect on tissue regeneration, 10.1016/j.biomaterials.2011.03.064
  139. Pan Z., Ding J., Poly(lactide-co-glycolide) porous scaffolds for tissue engineering and regenerative medicine, 10.1098/rsfs.2011.0123
  140. Wu Linbo, Zhang Junchuan, Jing Dianying, Ding Jiandong, “Wet-state” mechanical properties of three-dimensional polyester porous scaffolds, 10.1002/jbm.a.30544
  141. Poels Jonathan, Abou-Ghannam Gaël, Decamps Aline, Leyman Mélanie, Rieux Anne des, Wyns Christine, Transplantation of testicular tissue in alginate hydrogel loaded with VEGF nanoparticles improves spermatogonial recovery, 10.1016/j.jconrel.2016.05.037
  142. Chan B. P., Leong K. W., Scaffolding in tissue engineering: general approaches and tissue-specific considerations, 10.1007/s00586-008-0745-3
  143. Xia Tingting, Liu Wanqian, Yang Li, A review of gradient stiffness hydrogels used in tissue engineering and regenerative medicine : GRADIENT STIFFNESS HYDROGELS USED IN TISSUE ENGINEERING AND REGENERATIVE MEDICINE, 10.1002/jbm.a.36034
  144. Crapo Peter M., Gilbert Thomas W., Badylak Stephen F., An overview of tissue and whole organ decellularization processes, 10.1016/j.biomaterials.2011.01.057
  145. Bayat Akbar, Dorkoosh Farid A., Dehpour Ahmad Reza, Moezi Leila, Larijani Bagher, Junginger Hans E., Rafiee-Tehrani Morteza, Nanoparticles of quaternized chitosan derivatives as a carrier for colon delivery of insulin: Ex vivo and in vivo studies, 10.1016/j.ijpharm.2007.12.037
  146. Letchford Kevin, Burt Helen, A review of the formation and classification of amphiphilic block copolymer nanoparticulate structures: micelles, nanospheres, nanocapsules and polymersomes, 10.1016/j.ejpb.2006.11.009
  147. Hamidi Mehrdad, Azadi Amir, Rafiei Pedram, Hydrogel nanoparticles in drug delivery, 10.1016/j.addr.2008.08.002
  148. Huang Min, Vitharana Samadhi N., Peek Laura J., Coop Tina, Berkland Cory, Polyelectrolyte Complexes Stabilize and Controllably Release Vascular Endothelial Growth Factor, 10.1021/bm061211k
  149. Baek Jong-Suep, Cho Cheong-Weon, A multifunctional lipid nanoparticle for co-delivery of paclitaxel and curcumin for targeted delivery and enhanced cytotoxicity in multidrug resistant breast cancer cells, 10.18632/oncotarget.16153
  150. Izadifar Mohammad, Kelly Michael E, Chen Xiongbiao, Regulation of sequential release of growth factors using bilayer polymeric nanoparticles for cardiac tissue engineering, 10.2217/nnm-2016-0220
  151. Najjar Mejdi, Manzoli Vita, Abreu Maria, Villa Chiara, Martino Mikaël M., Molano R. Damaris, Torrente Yvan, Pileggi Antonello, Inverardi Luca, Ricordi Camillo, Hubbell Jeffrey A., Tomei Alice A., Fibrin gels engineered with pro-angiogenic growth factors promote engraftment of pancreatic islets in extrahepatic sites in mice : Engineered Gels for Islet Transplantation, 10.1002/bit.25589
  152. Felice Betiana, Prabhakaran Molamma P., Rodríguez Andrea P., Ramakrishna Seeram, Drug delivery vehicles on a nano-engineering perspective, 10.1016/j.msec.2014.04.049
  153. Lee Jae-Ho, Gye Myung C., Choi Kyoo Wan, Hong Jae Yup, Lee Yong Bok, Park Dong-Wook, Lee Seung Jae, Min Churl K., In vitro differentiation of germ cells from nonobstructive azoospermic patients using three-dimensional culture in a collagen gel matrix, 10.1016/j.fertnstert.2006.09.015
  154. Reuter Karin, Ehmcke Jens, Stukenborg Jan-Bernd, Simoni Manuela, Damm Oliver S., Redmann Klaus, Schlatt Stefan, Wistuba Joachim, Reassembly of somatic cells and testicular organogenesis in vitro, 10.1016/j.tice.2013.12.001
  155. Jalayeri Maryam, Pirnia Afshin, Najafabad Elaheh Poorazizi, Varzi Ali Mohammad, Gholami Mohammadreza, Evaluation of alginate hydrogel cytotoxicity on three-dimensional culture of type A spermatogonial stem cells, 10.1016/j.ijbiomac.2016.10.074
  156. Artel Arsun, Mehdizadeh Hamidreza, Chiu Yu-Chieh, Brey Eric M., Cinar Ali, An Agent-Based Model for the Investigation of Neovascularization Within Porous Scaffolds, 10.1089/ten.tea.2010.0571
  157. Wang Peng, Jiang Xiaolu, Jiang Yanhua, Hu Xiaoke, Mou Haijin, Li Man, Guan Huashi, In vitroantioxidative activities of three marine oligosaccharides, 10.1080/14786410701371215
  158. Hsiao Chi-Hao, Ji Andrea Tung-Qian, Chang Chih-Cheng, Cheng Chien-Jui, Lee Liang-Ming, Ho Jennifer Hui-Chun, Local injection of mesenchymal stem cells protects testicular torsion-induced germ cell injury, 10.1186/s13287-015-0079-0
  159. , , , , , , Upregulated Autophagy in Sertoli Cells of Ethanol-Treated Rats Is Associated with Induction of Inducible Nitric Oxide Synthase (iNOS), Androgen Receptor Suppression and Germ Cell Apoptosis, 10.3390/ijms18051061
  160. Eid N., Kondo Y., Ethanol-induced mitophagy in rat Sertoli cells: Implications for male fertility, 10.1111/and.12820
  161. Baert Y., Stukenborg J.- B., Landreh M., De Kock J., Jornvall H., Soder O., Goossens E., Derivation and characterization of a cytocompatible scaffold from human testis, 10.1093/humrep/deu330
  162. Vermeulen Maxime, Del Vento Federico, de Michele Francesca, Poels Jonathan, Wyns Christine, Development of a Cytocompatible Scaffold from Pig Immature Testicular Tissue Allowing Human Sertoli Cell Attachment, Proliferation and Functionality, 10.3390/ijms19010227
  163. Baert Yoni, Rombaut Charlotte, Goossens Ellen, Scaffold-Based and Scaffold-Free Testicular Organoids from Primary Human Testicular Cells, Methods in Molecular Biology (2017), 10.1007/7651_2017_48
  164. Ciubotaru Anatol, Cebotari Serghei, Tudorache Igor, Beckmann Erik, Hilfiker Andres, Haverich Axel, Biological heart valves, 10.1515/bmt-2012-0148
  165. Takahashi Kazutoshi, Yamanaka Shinya, Induction of Pluripotent Stem Cells from Mouse Embryonic and Adult Fibroblast Cultures by Defined Factors, 10.1016/j.cell.2006.07.024
  166. Ishikura Yukiko, Yabuta Yukihiro, Ohta Hiroshi, Hayashi Katsuhiko, Nakamura Tomonori, Okamoto Ikuhiro, Yamamoto Takuya, Kurimoto Kazuki, Shirane Kenjiro, Sasaki Hiroyuki, Saitou Mitinori, In Vitro Derivation and Propagation of Spermatogonial Stem Cell Activity from Mouse Pluripotent Stem Cells, 10.1016/j.celrep.2016.11.026
  167. Chuma S., Spermatogenesis from epiblast and primordial germ cells following transplantation into postnatal mouse testis, 10.1242/dev.01555
  168. Hayashi Katsuhiko, Ohta Hiroshi, Kurimoto Kazuki, Aramaki Shinya, Saitou Mitinori, Reconstitution of the Mouse Germ Cell Specification Pathway in Culture by Pluripotent Stem Cells, 10.1016/j.cell.2011.06.052
  169. Sasaki Kotaro, Yokobayashi Shihori, Nakamura Tomonori, Okamoto Ikuhiro, Yabuta Yukihiro, Kurimoto Kazuki, Ohta Hiroshi, Moritoki Yoshinobu, Iwatani Chizuru, Tsuchiya Hideaki, Nakamura Shinichiro, Sekiguchi Kiyotoshi, Sakuma Tetsushi, Yamamoto Takashi, Mori Takahide, Woltjen Knut, Nakagawa Masato, Yamamoto Takuya, Takahashi Kazutoshi, Yamanaka Shinya, Saitou Mitinori, Robust In Vitro Induction of Human Germ Cell Fate from Pluripotent Stem Cells, 10.1016/j.stem.2015.06.014
  170. Botman Olivier, Wyns Christine, Induced Pluripotent Stem Cell Potential in Medicine, Specifically Focused on Reproductive Medicine, 10.3389/fsurg.2014.00005
Bibliographic reference Del Vento, Federico ; Vermeulen, Maxime ; de Michele, Francesca ; Giudice, Maria ; Poels, Jonathan ; et. al. Tissue Engineering to Improve Immature Testicular Tissue and Cell Transplantation Outcomes: One Step Closer to Fertility Restoration for Prepubertal Boys Exposed to Gonadotoxic Treatments. In: International Journal of Molecular Sciences, Vol. 19, no. 1, p. 286 [1-24] (2018)
Permanent URL http://hdl.handle.net/2078.1/193342