FREE SHIPPING over $40
OVER 10000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Animal reproduction science2007; 106(1-2); 65-76; doi: 10.1016/j.anireprosci.2007.03.026

Xenografting of adult mammalian testis tissue.

Abstract: Xenografting of testis tissue from immature males from several mammalian species to immunodeficient mouse hosts results in production of fertilization-competent sperm. However, the efficiency of testis tissue xenografting from adult donors has not been critically evaluated. Testis tissue xenografting from sexually mature animals could provide an option to preserve the genetic material from valuable males when semen for cryopreservation cannot be collected. To assess the potential use of this technique for adult individuals, testes from adult animals of six species (pig, goat, cattle, donkey, horse and rhesus monkey) were ectopically grafted to host mice. Grafts were recovered and analyzed at three time points: less than 12 weeks, between 12 and 24 weeks and more than 24 weeks after grafting. Histological analysis of the grafts revealed effects of species and donor tissue maturity: all grafts from species with greater daily sperm production (pig and goat) were found to have degenerated tubules or grafts were completely degenerated. None of the xenografts from mature adult bull and monkeys contained differentiated spermatogenic cells when examined more than 12 weeks post-grafting but tubules with Sertoli cells only remained. In grafts from a young adult bull, Sertoli cells persisted much longer than with the mature adult grafts. In grafts from a young adult horse, spermatogenesis proceeded to meiosis. In grafts from a young adult donkey and monkey, however, complete spermatogenesis was found in the grafts. These results show that testis tissue grafts from mature adult donors did not support germ cell differentiation but seminiferous tubules with Sertoli cells only survived in some species. The timing and progression of tubular degeneration after grafting of adult testis tissue appear to be related to the intensity of spermatogenesis at the time of grafting. Testis tissue from sub-adult donors survives better as xenograft than tissue from mature adult donors, and complete spermatogenesis can occur albeit with species-specific differences.
Get Full Text
Publication Date: 2007-04-08 PubMed ID: 17512146PubMed Central: PMC2386512DOI: 10.1016/j.anireprosci.2007.03.026Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Evaluation Study
  • Journal Article
  • Research Support
  • N.I.H.
  • Extramural
  • Research Support
  • Non-U.S. Gov't
  • Research Support
  • U.S. Gov't
  • Non-P.H.S.

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This study investigates the potential of xenografting, or transplanting tissue between different species, using testis tissue from mature adult male mammals into immunodeficient mice. The results show varying success across different species and suggest that the donor’s level of sexual maturity and sperm production rates may significantly impact the success of such grafts.

Objective of the Study

  • The study sought to evaluate the efficiency of xenografting testis tissue from mature male animals into a different species. The technique could represent a method for preserving genetic material from valued male animals, particularly when the collection of semen for cryopreservation is not possible.

Methodology

  • Tissue from adult testes of six animal species—pig, goat, cattle, donkey, horse, and rhesus monkey—was grafted into mouse hosts.
  • The study retrieved and analyzed the grafts at three different stages: less than 12 weeks, between 12 and 24 weeks, and more than 24 weeks after grafting.
  • Using histological analysis, researchers observed the results of the grafts and noted the effects related to the species and maturity of the donor tissue.

Findings

  • Grafts from species with higher daily sperm production (pigs and goats) demonstrated degenerated tubules, or the grafts were completely degenerated.
  • None of the grafts from mature adult bulls and monkeys contained differentiated spermatogenic cells when examined after 12 weeks post-grafting, but tubules with Sertoli cells (which help in sperm formation) only, survived.
  • Grafts taken from a young adult bull showed that Sertoli cells lived longer than with mature adult grafts.
  • In grafts from a young adult horse, spermatogenesis (the process of producing sperm) proceeded to meiosis, a process that halves the number of chromosomes and results in the creation of sperm.
  • Full spermatogenesis was found in the grafts from young adult donkeys and monkeys.

Conclusion

  • Testis tissue grafts from mature adult donors did not support germ cell differentiation, a necessary process for sperm production. However, seminiferous tubules with only Sertoli cells survived in some species.
  • The timing and progression of tubular degeneration after grafting of adult testis tissue appeared to correlate with the intensity of spermatogenesis at the time of grafting.
  • The survival rate of testis tissue from sub-adult donors was higher as a xenograft than mature adult donors. Further, complete spermatogenesis could occur, albeit with variations across different species.

Cite This Article

APA
Arregui L, Rathi R, Zeng W, Honaramooz A, Gomendio M, Roldan ER, Dobrinski I. (2007). Xenografting of adult mammalian testis tissue. Anim Reprod Sci, 106(1-2), 65-76. https://doi.org/10.1016/j.anireprosci.2007.03.026

Publication

Animal reproduction science
ISSN: 0378-4320
NlmUniqueID: 7807205
Country: Netherlands
Language: English
Volume: 106
Issue: 1-2
Pages: 65-76

Researcher Affiliations

Arregui, Lucía
  • Center for Animal Transgenesis and Germ Cell Research, University of Pennsylvania, Kennet Square, PA 19348, USA.
Rathi, Rahul
    Zeng, Wenxian
      Honaramooz, Ali
        Gomendio, Montserrat
          Roldan, Eduardo R S
            Dobrinski, Ina

              MeSH Terms

              • Age Factors
              • Animals
              • Cattle
              • Equidae / physiology
              • Goats / physiology
              • Graft Survival
              • Horses / physiology
              • Macaca mulatta / physiology
              • Male
              • Mammals / physiology
              • Mice
              • Organ Size
              • Seminal Vesicles / anatomy & histology
              • Spermatogenesis / physiology
              • Swine / physiology
              • Testis / transplantation
              • Transplantation, Heterologous / methods
              • Transplantation, Heterologous / physiology
              • Transplantation, Heterologous / veterinary

              Grant Funding

              • R01 RR017359 / NCRR NIH HHS
              • R01 RR017359-05 / NCRR NIH HHS
              • 5R01 RR 17359-05 / NCRR NIH HHS

              References

              This article includes 22 references
              1. Bajpai M, Gupta G, Setty BS. Changes in carbohydrate metabolism of testicular germ cells during meiosis in the rat.. Eur J Endocrinol 1998 Mar;138(3):322-7.
                pubmed: 9539308doi: 10.1530/eje.0.1380322google scholar: lookup
              2. Blottner S, Hingst O, Meyer HH. Inverse relationship between testicular proliferation and apoptosis in mammalian seasonal breeders.. Theriogenology 1995 Aug;44(3):321-8.
                pubmed: 16727732doi: 10.1016/0093-691x(95)00187-dgoogle scholar: lookup
              3. Geens M, De Block G, Goossens E, Frederickx V, Van Steirteghem A, Tournaye H. Spermatogonial survival after grafting human testicular tissue to immunodeficient mice.. Hum Reprod 2006 Feb;21(2):390-6.
                pubmed: 16311289doi: 10.1093/humrep/dei412google scholar: lookup
              4. Honaramooz A, Snedaker A, Boiani M, Schöler H, Dobrinski I, Schlatt S. Sperm from neonatal mammalian testes grafted in mice.. Nature 2002 Aug 15;418(6899):778-81.
                pubmed: 12181567doi: 10.1038/nature00918google scholar: lookup
              5. Honaramooz A, Li MW, Penedo MC, Meyers S, Dobrinski I. Accelerated maturation of primate testis by xenografting into mice.. Biol Reprod 2004 May;70(5):1500-3.
                pubmed: 14736818doi: 10.1095/biolreprod.103.025536google scholar: lookup
              6. Jahnukainen K, Ehmcke J, Schlatt S. Testicular xenografts: a novel approach to study cytotoxic damage in juvenile primate testis.. Cancer Res 2006 Apr 1;66(7):3813-8.
                pubmed: 16585208doi: 10.1158/0008-5472.can-05-3754google scholar: lookup
              7. Johnson L, Thompson DL Jr. Age-related and seasonal variation in the Sertoli cell population, daily sperm production and serum concentrations of follicle-stimulating hormone, luteinizing hormone and testosterone in stallions.. Biol Reprod 1983 Oct;29(3):777-89.
                pubmed: 6414546doi: 10.1095/biolreprod29.3.777google scholar: lookup
              8. Johnson AD, Gomes WR, Vandermark NL. The testis. Academic Press; London: 1970.
              9. Meachem SJ, Stanton PG, Schlatt S. Follicle-stimulating hormone regulates both Sertoli cell and spermatogonial populations in the adult photoinhibited Djungarian hamster testis.. Biol Reprod 2005 May;72(5):1187-93.
                pubmed: 15659702doi: 10.1095/biolreprod.104.039321google scholar: lookup
              10. Oatley JM, de Avila DM, Reeves JJ, McLean DJ. Spermatogenesis and germ cell transgene expression in xenografted bovine testicular tissue.. Biol Reprod 2004 Aug;71(2):494-501.
                pubmed: 15070832doi: 10.1095/biolreprod.104.027953google scholar: lookup
              11. O'Donnell L, Meachem SJ, Stanton PG, McLachlan RI. Endocrine regulation of spermatogenesis. In: Neill JD, editor. Knobil and Neill's physiology of reproduction. Third. Elsevier Academic Press; 2006. pp. 1017–1069.
              12. Orwig KE, Schlatt S. Cryopreservation and transplantation of spermatogonia and testicular tissue for preservation of male fertility.. J Natl Cancer Inst Monogr 2005;(34):51-6.
                pubmed: 15784824doi: 10.1093/jncimonographs/lgi029google scholar: lookup
              13. Pukazhenthi B, Comizzoli P, Travis AJ, Wildt DE. Applications of emerging technologies to the study and conservation of threatened and endangered species.. Reprod Fertil Dev 2006;18(1-2):77-90.
                pubmed: 16478605doi: 10.1071/rd05117google scholar: lookup
              14. Rathi R, Honaramooz A, Zeng W, Turner R, Dobrinski I. Germ cell development in equine testis tissue xenografted into mice.. Reproduction 2006 Jun;131(6):1091-8.
                pubmed: 16735548doi: 10.1530/rep.1.01101google scholar: lookup
              15. Russell LD. Sertoli cell structure and function in seasonally breeding mammals. In: Russell LD, Griswold MD, editors. The sertoli cell. Clearwater: Cache River Press; 1993. pp. 350–364.
              16. Schmidt JA, de Avila JM, McLean DJ. Effect of vascular endothelial growth factor and testis tissue culture on spermatogenesis in bovine ectopic testis tissue xenografts.. Biol Reprod 2006 Aug;75(2):167-75.
                pubmed: 16571874doi: 10.1095/biolreprod.105.049817google scholar: lookup
              17. Schlatt S, Kim SS, Gosden R. Spermatogenesis and steroidogenesis in mouse, hamster and monkey testicular tissue after cryopreservation and heterotopic grafting to castrated hosts.. Reproduction 2002 Sep;124(3):339-46.
                pubmed: 12201807doi: 10.1530/rep.0.1240339google scholar: lookup
              18. Schlatt S, Honaramooz A, Ehmcke J, Goebell PJ, Rübben H, Dhir R, Dobrinski I, Patrizio P. Limited survival of adult human testicular tissue as ectopic xenograft.. Hum Reprod 2006 Feb;21(2):384-9.
                pmc: PMC1361612pubmed: 16239313doi: 10.1093/humrep/dei352google scholar: lookup
              19. Shinohara T, Inoue K, Ogonuki N, Kanatsu-Shinohara M, Miki H, Nakata K, Kurome M, Nagashima H, Toyokuni S, Kogishi K, Honjo T, Ogura A. Birth of offspring following transplantation of cryopreserved immature testicular pieces and in-vitro microinsemination.. Hum Reprod 2002 Dec;17(12):3039-45.
                pubmed: 12456600doi: 10.1093/humrep/17.12.3039google scholar: lookup
              20. Siegel S, Castellan NJ. Nonparametric statistics for the behavioural sciences. Second. McGraw-Hill College; London: 1988.
              21. Snedaker AK, Honaramooz A, Dobrinski I. A game of cat and mouse: xenografting of testis tissue from domestic kittens results in complete cat spermatogenesis in a mouse host.. J Androl 2004 Nov-Dec;25(6):926-30.
                pubmed: 15477365doi: 10.1002/j.1939-4640.2004.tb03163.xgoogle scholar: lookup
              22. Turner RM, Rathi R, Zeng W, Honaramooz A, Dobrinski I. Xenografting to study testis function in stallions. Anim Reprod Sci 2006;94:161–164.

              Citations

              This article has been cited 25 times.
              1. Farias TO, Figueiredo AFA, Wnuk NT, Talamoni SA, Costa GMJ. Testis and brown adipose tissue xenografts from yellowish myotis (Myotis levis). Reprod Fertil 2022 Nov 1;3(4):287-300.
                doi: 10.1530/RAF-22-0056pubmed: 36331914google scholar: lookup
              2. Bolton RL, Mooney A, Pettit MT, Bolton AE, Morgan L, Drake GJ, Appeltant R, Walker SL, Gillis JD, Hvilsom C. Resurrecting biodiversity: advanced assisted reproductive technologies and biobanking. Reprod Fertil 2022 Jul 1;3(3):R121-R146.
                doi: 10.1530/RAF-22-0005pubmed: 35928671google scholar: lookup
              3. Awang-Junaidi AH, Fayaz MA, Goldstein S, Honaramooz A. Using a testis regeneration model, FGF9, LIF, and SCF improve testis cord formation while RA enhances gonocyte survival. Cell Tissue Res 2022 Aug;389(2):351-370.
                doi: 10.1007/s00441-022-03641-wpubmed: 35596812google scholar: lookup
              4. Awang-Junaidi AH, Fayaz MA, Goldstein S, Honaramooz A. Brief exposure of neonatal testis cells to EGF or GDNF alters the regenerated tissue. Reprod Fertil 2022 Jan 1;3(1):39-56.
                doi: 10.1530/RAF-21-0057pubmed: 35441148google scholar: lookup
              5. Tran KTD, Valli-Pulaski H, Colvin A, Orwig KE. Male fertility preservation and restoration strategies for patients undergoing gonadotoxic therapies†. Biol Reprod 2022 Aug 9;107(2):382-405.
                doi: 10.1093/biolre/ioac072pubmed: 35403667google scholar: lookup
              6. Bîcă O, Sârbu I, Ciongradi CI. Pediatric and Adolescent Oncofertility in Male Patients-From Alpha to Omega. Genes (Basel) 2021 May 8;12(5).
                doi: 10.3390/genes12050701pubmed: 34066795google scholar: lookup
              7. Sharma S, Sandhowe-Klaverkamp R, Schlatt S. Differentiation of Testis Xenografts in the Prepubertal Marmoset Depends on the Sex and Status of the Mouse Host. Front Endocrinol (Lausanne) 2018;9:467.
                doi: 10.3389/fendo.2018.00467pubmed: 30210448google scholar: lookup
              8. Devi L, Pothana L, Goel S. Dysregulation of angiogenesis-specific signalling in adult testis results in xenograft degeneration. Sci Rep 2017 Jun 1;7(1):2605.
                doi: 10.1038/s41598-017-02604-4pubmed: 28572601google scholar: lookup
              9. Zeng W, Alpaugh W, Stefanovski D, Schlingmann K, Dobrinski I, Turner RM. Xenografting of isolated equine (Equus caballus) testis cells results in de novo morphogenesis of seminiferous tubules but not spermatogenesis. Andrology 2017 Mar;5(2):336-346.
                doi: 10.1111/andr.12308pubmed: 28160442google scholar: lookup
              10. Sato T, Katagiri K, Kojima K, Komeya M, Yao M, Ogawa T. In Vitro Spermatogenesis in Explanted Adult Mouse Testis Tissues. PLoS One 2015;10(6):e0130171.
                doi: 10.1371/journal.pone.0130171pubmed: 26065832google scholar: lookup
              11. Pukazhenthi BS, Nagashima J, Travis AJ, Costa GM, Escobar EN, França LR, Wildt DE. Slow freezing, but not vitrification supports complete spermatogenesis in cryopreserved, neonatal sheep testicular xenografts. PLoS One 2015;10(4):e0123957.
                doi: 10.1371/journal.pone.0123957pubmed: 25923660google scholar: lookup
              12. Wyns C. Male fertility preservation before gonadotoxic therapies. Facts Views Vis Obgyn 2010;2(2):88-108.
                pubmed: 25302103
              13. Arregui L, Dobrinski I. Xenografting of testicular tissue pieces: 12 years of an in vivo spermatogenesis system. Reproduction 2014 Nov;148(5):R71-84.
                doi: 10.1530/REP-14-0249pubmed: 25150043google scholar: lookup
              14. Arregui L, Dobrinski I, Roldan ER. Germ cell survival and differentiation after xenotransplantation of testis tissue from three endangered species: Iberian lynx (Lynx pardinus), Cuvier's gazelle (Gazella cuvieri) and Mohor gazelle (G. dama mhorr). Reprod Fertil Dev 2014;26(6):817-26.
                doi: 10.1071/RD12411pubmed: 23763851google scholar: lookup
              15. Arregui L, Rathi R, Modelski M, Zeng W, Roldan ER, Dobrinski I. Suppression of spermatogenesis before grafting increases survival and supports resurgence of spermatogenesis in adult mouse testis. Fertil Steril 2012 Jun;97(6):1422-9.
                doi: 10.1016/j.fertnstert.2012.03.009pubmed: 22464084google scholar: lookup
              16. Tang L, Rodriguez-Sosa JR, Dobrinski I. Germ cell transplantation and testis tissue xenografting in mice. J Vis Exp 2012 Feb 6;(60).
                doi: 10.3791/3545pubmed: 22330955google scholar: lookup
              17. Lo KC, Domes T. Can we grow sperm? A translational perspective on the current animal and human spermatogenesis models. Asian J Androl 2011 Sep;13(5):677-82.
                doi: 10.1038/aja.2011.88pubmed: 21765440google scholar: lookup
              18. Gourdon JC, Travis AJ. Spermatogenesis in ferret testis xenografts: a new model. Comp Med 2011 Apr;61(2):145-9.
                pubmed: 21535925
              19. Fortier LA, Travis AJ. Stem cells in veterinary medicine. Stem Cell Res Ther 2011 Feb 23;2(1):9.
                doi: 10.1186/scrt50pubmed: 21371354google scholar: lookup
              20. Mota PC, Ramalho-Santos J, Schlatt S. Xenografting as a tool to preserve endangered species: outcomes and challenges in model systems. Vet Med Int 2010 Sep 2;2011.
                doi: 10.4061/2011/629409pubmed: 20885939google scholar: lookup
              21. Schlatt S, Westernströer B, Gassei K, Ehmcke J. Donor-host involvement in immature rat testis xenografting into nude mouse hosts. Biol Reprod 2010 May;82(5):888-95.
                doi: 10.1095/biolreprod.109.082073pubmed: 20107205google scholar: lookup
              22. Dobrinski I. De novo morphogenesis of functional testis tissue after ectopic transplantation of isolated cells. Organogenesis 2007 Oct;3(2):79-82.
                doi: 10.4161/org.3.2.4944pubmed: 19279705google scholar: lookup
              23. Honaramooz A, Cui XS, Kim NH, Dobrinski I. Porcine embryos produced after intracytoplasmic sperm injection using xenogeneic pig sperm from neonatal testis tissue grafted in mice. Reprod Fertil Dev 2008;20(7):802-7.
                doi: 10.1071/rd08093pubmed: 18842182google scholar: lookup
              24. Pereira AG, Matos TM, de Albuquerque JLC, da Silva AM, Silva AR. Testicular cryopreservation: From technical aspects to practical applications. Histol Histopathol 2025 Jul;40(7):967-978.
                doi: 10.14670/HH-18-869pubmed: 39810720google scholar: lookup
              25. Damyanova KB, Nixon B, Johnston SD, Gambini A, Benitez PP, Lord T. Spermatogonial stem cell technologies: applications from human medicine to wildlife conservation†. Biol Reprod 2024 Oct 14;111(4):757-779.
                doi: 10.1093/biolre/ioae109pubmed: 38993049google scholar: lookup
              Subscribe to our newsletter
              Join 99,780 horse owners like you who receive our email updates on horse health and nutrition.