1932

Abstract

The demand for food will increase to an unprecedented level over the next 30 years owing to human population expansion, thus necessitating an evolution that improves the efficiency of livestock production. Genetic gain to improve production traits of domestic animal populations is most effectively achieved via selective use of gametes from animals deemed to be elite, and this principle has been the basis of selective breeding strategies employed by humans for thousands of years. In modern-day animal agriculture, artificial insemination (AI) has been the staple of selective breeding programs, but it has inherent limitations for applications in beef cattle and pig production systems. In this review, we discuss the potential and current state of development for a concept termed Surrogate Sires as a next-generation breeding tool in livestock production. The scheme capitalizes on the capacity of spermatogonial stem cells to regenerate sperm production after isolation from donor testicular tissue and transfer into the testes of a recipient male that lacks endogenous germline, thereby allowing the surrogate male to produce offspring with the donor haplotype via natural mating. This concept provides an effective selective breeding tool to achieve genetic gain that is conducive for livestock production systems in which AI is difficult to implement.

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/content/journals/10.1146/annurev-animal-020518-115239
2019-02-15
2024-04-27
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Literature Cited

  1. 1. 
    Food Agric. Organ 2006. Livestock's Long Shadow: Environmental Issues and Options Rome: Food Agric. Organ.
  2. 2. 
    Thornton PK 2010. Livestock production: recent trends, future prospects. Philos. Trans. R. Soc. B Biol. Sci. 365:15542853–67
    [Google Scholar]
  3. 3. 
    Food Agric. Organ 2015. World Agriculture: Towards 2015/2030 London: Food Agric. Organ.
  4. 4. 
    Food Agric. Organ 2006. FAO Statistical Databases Rome: Food Agric. Organ.
  5. 5. 
    Food Agric. Organ 2006. World Agriculture: Towards 2030/2050 Rome: Food Agric. Organ.
  6. 6. 
    Gonen S, Jenko J, Gorjanc G, Mileham AJ, Whitelaw CBA, Hickey JM 2017. Potential of gene drives with genome editing to increase genetic gain in livestock breeding programs. Genet. Sel. Evol. 49:31–14
    [Google Scholar]
  7. 7. 
    Natl. Anim. Health Monit. Syst. 1997. Part 1: Reference of 1997 Beef Cow-Calf Management Practices, Fort Collins, CO: US Dep. Agric., Anim. Plant Health Inspect. Serv., Vet. Serv.
  8. 8. 
    US Dep. Agric. 2015. Swine 2012: Part I: Baseline Reference of Swine Health and Management in the United States, 201244 Fort Collins, CO: US. Dep. Agric., Anim. Plant Health Inspect. Serv., Vet. Serv., Natl. Anim. Health Monit. Syst .
    [Google Scholar]
  9. 9. 
    Roca J, Vásquez JM, Gil MA, Cuello C, Parrilla I, Martínez EA 2006. Challenges in pig artificial insemination. Reprod. Domest. Anim. 41:Suppl. 243–53
    [Google Scholar]
  10. 10. 
    Wagner H, Thibier M 2000. World statistics for artificial insemination in small ruminant and swine. Proceedings of the 14th International Congress on Animal Reproduction, Stockholm, Swed., July 2–63 New York: Elsevier
    [Google Scholar]
  11. 11. 
    Oatley JM, Brinster RL 2012. The germline stem cell niche unit in mammalian testes. Physiol. Rev. 92:2577–95
    [Google Scholar]
  12. 12. 
    de Rooij DG 2017. The nature and dynamics of spermatogonial stem cells. Development 144:3022–30
    [Google Scholar]
  13. 13. 
    Berndtson WE, Igboeli G, Pickett BW 1987. Relationship of absolute numbers of Sertoli cells to testicular size and spermatogenesis in young beef bulls. J. Anim. Sci. 64:1241–46
    [Google Scholar]
  14. 14. 
    Berndtson WE, Thompson TL 1990. Changing relationships between testis size, Sertoli cell number and spermatogenesis in Sprague-Dawley rats. J. Androl. 11:5429–35
    [Google Scholar]
  15. 15. 
    Thompson TL, Berndtson WE 1993. Testicular weight, Sertoli cell number, daily sperm production, and sperm output of sexually mature rabbits after neonatal or prepubertal hemicastration. Biol. Reprod. 48:5952–57
    [Google Scholar]
  16. 16. 
    Kerkhofs S, Denayer S, Haelens A, Claessens F 2009. Androgen receptor knockout and knock-in mouse models. J. Mol. Endocrinol. 42:11–17
    [Google Scholar]
  17. 17. 
    Potter SJ, De Falco T 2017. Role of the testis interstitial compartment in spermatogonial stem cell function. Reproduction 153:4R151–62
    [Google Scholar]
  18. 18. 
    Chen L, Brown PR, Willis WB, Eddy EM 2014. Peritubular myoid cells participate in male mouse spermatogonial stem cell maintenance. Endocrinology 155:4964–74
    [Google Scholar]
  19. 19. 
    de Rooij DG, Grootegoed JA 1998. Spermatogonial stem cells. Curr. Opin. Cell Biol. 10:6694–701
    [Google Scholar]
  20. 20. 
    de Rooij DG, Russell LD 2000. All you wanted to know about spermatogonia but were afraid to ask. J. Androl. 21:6776–98
    [Google Scholar]
  21. 21. 
    Oatley JM, Brinster RL 2008. Regulation of spermatogonial stem cell self-renewal in mammals. Annu. Rev. Cell Dev. Biol. 24:263–86
    [Google Scholar]
  22. 22. 
    Oatley JM, Brinster RL 2012. The germline stem cell niche unit in mammalian testes. Physiol. Rev. 92:2577–95
    [Google Scholar]
  23. 23. 
    Lord T, Oatley JM 2017. A revised Asingle model to explain stem cell dynamics in the mouse male germline. Reproduction 154:R55–64
    [Google Scholar]
  24. 24. 
    Brinster RL, Avarbock MR 1994. Germline transmission of donor haplotype following spermatogonial transplantation. PNAS 91:2411303–7
    [Google Scholar]
  25. 25. 
    Brinster RL, Zimmermann JW 1994. Spermatogenesis following male germ-cell transplantation. PNAS 91:2411298–302
    [Google Scholar]
  26. 26. 
    Kanatsu-Shinohara M, Ogonuki N, Inoue K, Miki H, Ogura A et al. 2003. Long-term proliferation in culture and germline transmission of mouse male germline stem cells. Biol. Reprod. 69:2612–16
    [Google Scholar]
  27. 27. 
    Kubota H, Avarbock MR, Brinster RL 2004. Growth factors essential for self-renewal and expansion of mouse spermatogonial stem cells. PNAS 101:4716489–94
    [Google Scholar]
  28. 28. 
    Ogawa T, Arechaga T, Avarbock M, Brinster R 1997. Transplantation of testis germinal cells into mouse seminiferous tubules. Int. J. Dev. 122:111–22
    [Google Scholar]
  29. 29. 
    Kanatsu-Shinohara M, Shinohara T 2010. Germline modification using mouse spermatogonial stem cells. Methods Enzymol 477:17–36
    [Google Scholar]
  30. 30. 
    Zhang Z, Shao S, Meistrich ML 2006. Irradiated mouse testes efficiently support spermatogenesis derived from donor germ cells of mice and rats. J. Androl. 27:3365–75
    [Google Scholar]
  31. 31. 
    Shinohara T, Orwig KE, Avarbock MR, Brinster RL 2000. Remodeling of the postnatal mouse testis is accompanied by dramatic changes in stem cell number and niche accessibility. PNAS 98:116186–91
    [Google Scholar]
  32. 32. 
    Oatley MJ, Racicot KE, Oatley JM 2011. Sertoli cells dictate spermatogonial stem cell niches in the mouse testis. Biol. Reprod. 84:639–45
    [Google Scholar]
  33. 33. 
    Cooke Ps, Arambepola NK, Kirby JD, Hardy MP, Hess RA, Bunick D 1997. Thyroid hormone regulation of the development of the testis and its constituent cell types. J. Endocrinol. 48:43–58
    [Google Scholar]
  34. 34. 
    Holsberger DR, Jirawatnotai S, Kiyokawa H, Cooke PS 2003. Thyroid hormone regulates the cell cycle inhibitor p27 Kip1 in postnatal murine Sertoli cells. Endocrinology 144:3732–38
    [Google Scholar]
  35. 35. 
    Silva CG, Cunha ER, Blume GR, Malaquias JV, Báo SN, Martins CF 2015. Cryopreservation of boar sperm comparing different cryoprotectants associated in media based on powdered coconut water, lactose and trehalose. Cryobiology 70:290–94
    [Google Scholar]
  36. 36. 
    Izadyar F, Den Ouden K, Stout TA, Stout J, Coret J et al. 2003. Autologous and homologous transplantation of bovine spermatogonial stem cells. Reproduction 126:765–74
    [Google Scholar]
  37. 37. 
    Herrid M, Vignarajan S, Davey R, Dobrinski I, Hill JR 2006. Successful transplantation of bovine testicular cells to heterologous recipients. Reproduction 132:4617–24
    [Google Scholar]
  38. 38. 
    Stockwell S, Herrid M, Davey R, Brownlee A, Hutton K, Hill JR 2009. Microsatellite detection of donor-derived sperm DNA following germ cell transplantation in cattle. Reprod. Fertil. Dev. 21:3462–68
    [Google Scholar]
  39. 39. 
    Honaramooz A, Megee SO, Dobrinski I 2002. Germ cell transplantation in pigs. Biol. Reprod. 66:21–28
    [Google Scholar]
  40. 40. 
    Mikkola M, Sironen A, Kopp C, Taponen J, Sukura A et al. 2006. Transplantation of normal boar testicular cells resulted in complete focal spermatogenesis in a boar affected by the immotile short-tail sperm defect. Reprod. Domest. Anim. 41:2124–28
    [Google Scholar]
  41. 41. 
    Zeng W, Tang L, Bondareva A, Honaramooz A, Tanco V et al. 2013. Viral transduction of male germline stem cells results in transgene transmission after germ cell transplantation in pigs. Biol. Reprod. 88:27
    [Google Scholar]
  42. 42. 
    Guan K, Wolf F, Becker A, Engel W, Nayernia K, Hasenfuss G 2009. Isolation and cultivation of stem cells from adult mouse testes. Nat. Protoc. 4:143–54
    [Google Scholar]
  43. 43. 
    Meng X 2000. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science 287:54571489–93
    [Google Scholar]
  44. 44. 
    Oatley MJ, Kaucher AV, Yang Q-E, Waqas MS, Oatley JM 2016. Conditions for long-term culture of cattle undifferentiated spermatogonia. Biol. Reprod. 9514:11–10
    [Google Scholar]
  45. 45. 
    Aponte PM, Soda T, Teerds KJ, Mizrak SC, van de Kant HJG, de Rooij DG 2008. Propagation of bovine spermatogonial stem cells in vitro. Reproduction 136:5543–57
    [Google Scholar]
  46. 46. 
    Goel S, Sugimoto M, Minami N, Yamada M, Kume S, Imai H 2007. Identification, isolation, and in vitro culture of porcine gonocytes. Biol. Reprod. 77:1127–37
    [Google Scholar]
  47. 47. 
    Kuijk EW, Colenbrander B, Roelen BAJ 2009. The effects of growth factors on in vitro–cultured porcine testicular cells. Reproduction 138:4721–31
    [Google Scholar]
  48. 48. 
    Pramod RK, Mitra A 2014. In vitro culture and characterization of spermatogonial stem cells on Sertoli cell feeder layer in goat (Caprahircus). J. Assist. Reprod. Genet. 31:8993–1001
    [Google Scholar]
  49. 49. 
    Lee WY, Park HJ, Lee R, Lee KH, Kim YH et al. 2013. Establishment and in vitro culture of porcine spermatogonial germ cells in low temperature culture conditions. Stem Cell Res 11:31234–49
    [Google Scholar]
  50. 50. 
    Aponte PM, Soda T, van de Kant HJG, de Rooij DG 2006. Basic features of bovine spermatogonial culture and effects of glial cell line-derived neurotrophic factor. Theriogenology 65:1828–47
    [Google Scholar]
  51. 51. 
    Suyatno, Kitamura Y, Ikeda S, Minami N, Yamada M, Imai H 2018. Long-term culture of undifferentiated spermatogonia isolated from immature and adult bovine testes. Mol. Reprod. Dev. 85:236–49
    [Google Scholar]
  52. 52. 
    Zhao HM, Yang H, Luo FH, Li MX, Zhang S, Yang XG 2016. Isolation, proliferation, and induction of Bama mini-pig spermatogonial stem cells in vitro. Genet. Mol. Res. 15:3 https://doi.org/10.4238/gmr.15038602
    [Crossref] [Google Scholar]
  53. 53. 
    Zhang P, Chen X, Zheng Y, Zhu J, Qin Y et al. 2017. Long-term propagation of porcine undifferentiated spermatogonia. Stem Cells Dev 26:151121–31
    [Google Scholar]
  54. 54. 
    Ryu B, Kubota H, Avarbock MR, Brinster RL 2005. Conservation of spermatogonial stem cell self-renewal signaling between mouse and rat. PNAS 102:4014302–7
    [Google Scholar]
  55. 55. 
    Ogawa T, Dobrinski I, Avarbock MR, Brinster RL 2000. Transplantation of male germ line stem cells restores fertility in infertile mice. Nat. Med. 6:129–34
    [Google Scholar]
  56. 56. 
    Schrans-Stassen BHGJ, van de Kant HJG, de Rooij DG, van Pelt AMM 1999. Differential expression of c-kit in mouse undifferentiated and differentiating type A spermatogonia. Endocrinology 140:125894–900
    [Google Scholar]
  57. 57. 
    Kubota H, Avarbock MR, Schmidt JA, Brinster RL 2009. Spermatogonial stem cells derived from infertile WV/WV mice self-renew in vitro and generate progeny following transplantation. Biol. Reprod. 81:2293–301
    [Google Scholar]
  58. 58. 
    Kanatsu-Shinohara M, Morimoto H, Shinohara T 2016. Fertility of male germline stem cells following spermatogonial transplantation in infertile mouse models. Biol. Reprod. 94:51–11
    [Google Scholar]
  59. 59. 
    Park KE, Kaucher AV, Powell A, Waqas MS, Sandmaier SES et al. 2017. Generation of germline ablated male pigs by CRISPR/Cas9 editing of the NANOS2 gene. Sci. Rep. 7:40176
    [Google Scholar]
  60. 60. 
    Ephrussi A, Dickinson LK, Lehmann R 1991. oskar organizes the germ plasm and directs localization of the posterior determinant nanos. Cell 66:137–50
    [Google Scholar]
  61. 61. 
    Haraguchi S, Tsuda M, Kitajima S, Sasaoka Y, Nomura-Kitabayashi A et al. 2003. nanos1: a mouse nanos gene expressed in the central nervous system is dispensable for normal development. Mech. Dev. 120:721–31
    [Google Scholar]
  62. 62. 
    Tsuda M, Sasaoka Y, Kiso M, Abe K, Haraguchi S et al. 2003. Conserved role of nanos proteins in germ cell development. Science 301:56371239–41
    [Google Scholar]
  63. 63. 
    Suzuki A, Tsuda M, Saga Y 2007. Functional redundancy among Nanos proteins and a distinct role of Nanos2 during male germ cell development. Development 134:177–83
    [Google Scholar]
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