Advertisement

Transabdominal Migration of the Testis

  • John M. Hutson
  • Jørgen M. Thorup
  • Spencer W. Beasley
Chapter

Abstract

The first phase of testicular descent, where its location is different from the developing ovary, is called the transabdominal phase, and occurs in humans between 8 and 15 weeks’ gestation. Transabdominal migration is controlled by changes in the supporting ligaments of the gonad, namely the cranial suspensory ligament and the genitoinguinal ligament, or ‘gubernaculum’. In the male the cranial ligament regresses (under the action of testosterone) while the gubernaculum enlarges and remains short (the so-called swelling reaction) under the influence of a newly discovered Leydig cell hormone, insulin-like hormone 3 (INSL3). INSL3 is inhibited by oestrogen in animal models and probably by endocrine disruptors in humans, while there is some indirect evidence for a minor role for maintaining the gubernacular cord short by the Sertoli cell hormone, anti-Mullerian hormone (AMH).

Keywords

Leydig Cell Testicular Descent Transverse Testicular Ectopia Relaxin Family Peptide Duct Regression 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. 1.
    Hutson JM. A biphasic model for the hormonal control of testicular descent. Lancet. 1985;2(8452):419–21.PubMedCrossRefGoogle Scholar
  2. 2.
    Hutson JM, Donahoe PK. The hormonal control of testicular descent. Endocr Rev. 1986;7(3):270–83.PubMedCrossRefGoogle Scholar
  3. 3.
    Rajfer J, Walsh PC. Hormonal regulation of testicular descent: experimental and clinical observations. J Urol. 1977;118(6):985–90.PubMedGoogle Scholar
  4. 4.
    Rajfer J. Hormonal regulation of testicular descent. Eur J Pediatr. 1987;146(2):56–7.Google Scholar
  5. 5.
    Newbold RR, Suzuki Y, McLachlan JA. Mullerian duct maintenance in heterotypic organ culture after in vivo exposure to diethylstilbestrol. Endocrinology. 1984;115(5):1863–8.PubMedCrossRefGoogle Scholar
  6. 6.
    Jean C. Croissance et structure des testicules cryptorchides chez les souris nees de meres traitees a l’oestradiol pendant a la gestation. Ann Endocrinol. 1973;34:669–87.Google Scholar
  7. 7.
    Hutson J. Exogenous oestrogens prevent transabdominal, testicular descent in mice with complete androgen resistance (testicular feminisation). Pediatr Surg Int. 1987;2:242–6.Google Scholar
  8. 8.
    Green RR, Burrill MW, Ivy AC. The effects of estrogens on the antenatal sexual development of the rat. Am J Anal. 1940;67:305–45.CrossRefGoogle Scholar
  9. 9.
    Hadziselimovic F, Herzog B, Kruslin E. Estrogen-induced cryptorchidism in animals. Clin Androl. 1980;3:166–74.Google Scholar
  10. 10.
    Habenicht UF, Neumann F. Hormonal regulation of testicular descent. Adv Anat Embryol Cell Biol. 1983;81:1–54.PubMedCrossRefGoogle Scholar
  11. 11.
    Wensing CJ, Colenbrander B. Normal and abnormal testicular descent. Oxf Rev Reprod Biol. 1986;8:130–64.PubMedGoogle Scholar
  12. 12.
    Barteczko KJ, Jacob MI. The testicular descent in human. Origin, development and fate of the gubernaculum Hunteri, processus vaginalis peritonei, and gonadal ligaments. Adv Anat Embryol Cell Biol. 2000;156:III–X, 1–98.PubMedGoogle Scholar
  13. 13.
    Wensing CJG. Testicular descent in some domestic mammals. III. Search for the factors that regulate the gubernacular reaction. Proc K Ned Akad Van Wet. 2000;x:196–202.Google Scholar
  14. 14.
    Wensing CJ. Testicular descent in the rat and a comparison of this process in the rat with that in the pig. Anat Rec. 1986;214(2):154–60.PubMedCrossRefGoogle Scholar
  15. 15.
    Shono T, Ramm-Anderson S, Hutson JM. Transabdominal testicular descent is really ovarian ascent. J Urol. 1994;152(2 Pt 2):781–4.PubMedGoogle Scholar
  16. 16.
    Wells L. Descent of the testis: anatomical and hormonal considerations. Surgery. 1943;14:436–68.Google Scholar
  17. 17.
    Lewis LG. Cryptorchism. J Urol. 1948;60:345–56.PubMedGoogle Scholar
  18. 18.
    Backhouse KM, Butler H. The gubernaculum testis of the pig (Sus scropha). J Anat. 1960;94:107–20.PubMedCentralPubMedGoogle Scholar
  19. 19.
    Backhouse KM. Embryology of testicular descent and maldescent. Urol Clin North Am. 1982;9(3):315–25.PubMedGoogle Scholar
  20. 20.
    Heyns CF, Human HJ, De Klerk DP. Hyperplasia and hypertrophy of the gubernaculum during testicular descent in the fetus. J Urol. 1986;135(5):1043–7.PubMedGoogle Scholar
  21. 21.
    Fentener van Vlissingen JM, Colenbrander B, Verbruggen A, et al. Testicular feminized males (TFM) in Nyctereutes procyonoides (Raccoon dog). In: Recent progress in cellular endocrinology of the testis. Elsevier: Amsterdam; 1984. p. 335–40.Google Scholar
  22. 22.
    Baumans V, Dijkstra G, Wensing CJ. The effect of orchidectomy on gubernacular outgrowth and regression in the dog. Int J Androl. 1982;5(4):387–400.PubMedCrossRefGoogle Scholar
  23. 23.
    Wensing CJ, Colenbrander B. The process of normal and abnormal testicular descent. In: Bierich JR, Ranke MB, editors. Maldescensus testis. Baltimore: Urban and Schwarzenberg; 1977. p. 193–7.Google Scholar
  24. 24.
    Wensing CJ, Colenbrander B, Bosma AA. Testicular feminisation syndrome and gubernacular development in a pig. Proc K Ned Akad Wet. 1975;78:402–5.Google Scholar
  25. 25.
    Hutson J. Testicular feminisation – a model for testicular descent in mice and men. J Pediatr Surg. 1986;21:195–8.PubMedCrossRefGoogle Scholar
  26. 26.
    Husmann DA, McPhaul MJ. Localization of the androgen receptor in the developing rat gubernaculum. Endocrinology. 1991;128(1):383–7.PubMedCrossRefGoogle Scholar
  27. 27.
    Welsh M, Saunders PT, Fisken M, et al. Identification in rats of a programming window for reproductive tract masculinization, disruption of which leads to hypospadias and cryptorchidism. J Clin Invest. 2008;118(4):1479–90.PubMedCentralPubMedCrossRefGoogle Scholar
  28. 28.
    Heyns CF, Pape VC. Presence of a low capacity androgen receptor in the gubernaculum of the pig fetus. J Urol. 1991;145(1):161–7.PubMedGoogle Scholar
  29. 29.
    Spencer JR, Torrado T, Sanchez RS, et al. Effects of flutamide and finasteride on rat testicular descent. Endocrinology. 1991;129(2):741–8.PubMedCrossRefGoogle Scholar
  30. 30.
    Zimmermann S, Steding G, Emmen JM, et al. Targeted disruption of the Insl3 gene causes bilateral cryptorchidism. Mol Endocrinol. 1999;13(5):681–91.PubMedCrossRefGoogle Scholar
  31. 31.
    Nef S, Parada LF. Cryptorchidism in mice mutant for Insl3. Nat Genet. 1999;22(3):295–9.PubMedCrossRefGoogle Scholar
  32. 32.
    Bay K, Andersson AM. Human testicular insulin-like factor 3: in relation to development, reproductive hormones and andrological disorders. Int J Androl. 2010;34(2):97–109.CrossRefGoogle Scholar
  33. 33.
    Fu P, Layfield S, Ferraro T, et al. Synthesis, conformation, receptor binding and biological activities of monobiotinylated human insulin-like peptide 3. J Pept Res. 2004;63(2):91–8.PubMedCrossRefGoogle Scholar
  34. 34.
    Bay K, Anand-Ivell R. Human testicular insulin-like factor 3 and endocrine disrupters. Vitam Horm. 2014;94:327–48.PubMedCrossRefGoogle Scholar
  35. 35.
    Kubota Y, Temelcos C, Bathgate RA, et al. The role of insulin 3, testosterone, Mullerian inhibiting substance and relaxin in rat gubernacular growth. Mol Hum Reprod. 2002;8(10):900–5.PubMedCrossRefGoogle Scholar
  36. 36.
    Adham IM, Steding G, Thamm T, et al. The overexpression of the insl3 in female mice causes descent of the ovaries. Mol Endocrinol. 2002;16(2):244–52.PubMedCrossRefGoogle Scholar
  37. 37.
    Chen N, Harisis GN, Farmer P, et al. Gone with the Wnt: the canonical Wnt signaling axis is present and androgen dependent in the rodent gubernaculum. J Pediatr Surg. 2011;46(12):2363–9.PubMedCrossRefGoogle Scholar
  38. 38.
    Kaftanovskaya EM, Feng S, Huang Z, et al. Suppression of insulin-like3 receptor reveals the role of beta-catenin and Notch signaling in gubernaculum development. Mol Endocrinol. 2011;25(1):170–83.PubMedCentralPubMedCrossRefGoogle Scholar
  39. 39.
    Harisis GN, Chen N, Farmer PJ, et al. Wnt signalling in testicular descent: a candidate mechanism for cryptorchidism in Robinow syndrome. J Pediatr Surg. 2013;48(7):1573–7.PubMedCrossRefGoogle Scholar
  40. 40.
    Mamoulakis C, Georgiou I, Dimitriadis F, et al. Genetic analysis of the human Insulin-like 3 gene: absence of mutations in a Greek paediatric cohort with testicular maldescent. Andrologia. 2014;46(9):986–96.PubMedCrossRefGoogle Scholar
  41. 41.
    Robinow M, Silverman FN, Smith HD. A newly recognized dwarfing syndrome. Am J Dis Child. 1969;117(6):645–51.PubMedGoogle Scholar
  42. 42.
    van Bokhoven H, Celli J, Kayserili H, et al. Mutation of the gene encoding the ROR2 tyrosine kinase causes autosomal recessive Robinow syndrome. Nat Genet. 2000;25(4):423–6.PubMedCrossRefGoogle Scholar
  43. 43.
    Mazzeu JF, Krepischi-Santos AC, Rosenberg C, et al. Chromosome abnormalities in two patients with features of autosomal dominant Robinow syndrome. Am J Med Genet A. 2007;143A(15):1790–5.PubMedCrossRefGoogle Scholar
  44. 44.
    Minami Y, Oishi I, Endo M, et al. Ror-family receptor tyrosine kinases in noncanonical Wnt signaling: their implications in developmental morphogenesis and human diseases. Dev Dyn. 2010;239(1):1–15.PubMedGoogle Scholar
  45. 45.
    Ivell R, Hartung S. The molecular basis of cryptorchidism. Mol Hum Reprod. 2003;94(4):175–81.CrossRefGoogle Scholar
  46. 46.
    Virtanen HE, Toppari J. Embryology and physiology of testicular development and descent. Pediatr Endocrinol Rev PER. 2014;11 Suppl 2:206–13.Google Scholar
  47. 47.
    Yuan FP, Lin DX, Rao CV, et al. Cryptorchidism in LhrKO animals and the effect of testosterone-replacement therapy. Hum Reprod. 2006;21(4):936–42.PubMedCrossRefGoogle Scholar
  48. 48.
    Hadziselimovic F, Kruslin E. The role of the epididymis in descensus testis and the topographical relationship between the testis and epididymis from the sixth month of pregnancy until immediately after birth. Anat Embryol (Berl). 1979;155(2):191–6.CrossRefGoogle Scholar
  49. 49.
    Hutson JM, Williams MP, Attah A, et al. Undescended testes remain a dilemma despite recent advances in research. Aust N Z J Surg. 1990;60(6):429–39.PubMedCrossRefGoogle Scholar
  50. 50.
    Hutson JM, Williams MPL, Fallat ME, et al. Testicular descent: new insights into its hormonal control. In: Milligan S, editor. Oxford reviews of reproductive biology, vol. 12. Oxford: Clarendon Press; 1990. p. 1–56.Google Scholar
  51. 51.
    Josso N, Fekete C, Cachin O, et al. Persistence of Mullerian ducts in male pseudohermaphroditism, and its relationship to cryptorchidism. Clin Endocrinol (Oxf). 1983;19(2):247–58.CrossRefGoogle Scholar
  52. 52.
    Luthra M, Hutson J. Late gestation exogenous oestrogen inhibits testicular descent in fetal mice despite mullerian duct regression. Pediatr Surg Int. 1989;4:260–4.Google Scholar
  53. 53.
    Beheshti M, Churchill BM, Hardy BE, et al. Familial persistent mullerian duct syndrome. J Urol. 1984;131(5):968–9.PubMedGoogle Scholar
  54. 54.
    Brook CGD. Persistent mullerian duct syndrome. Pediatr Adolesc Endocrinol. 1981;8:100–4.Google Scholar
  55. 55.
    Sloan WR, Walsh PC. Familial persistent Mullerian duct syndrome. J Urol. 1976;115(4):459–61.PubMedGoogle Scholar
  56. 56.
    Keukens L, Zijp G, Mul D. Persistent Mullerian duct syndrome: a rare cause of unilateral cryptorchidism. BMJ Case Rep. 2012.Google Scholar
  57. 57.
    Morikawa S, Moriya K, Ishizu K, et al. Two heterozygous mutations of the AMH gene in a Japanese patient with persistent Mullerian duct syndrome. J Pediatr Endocrinol Metab. 2014;27(11–12):1223–6.PubMedGoogle Scholar
  58. 58.
    Josso N, Tran D. Biochemical aspects of prenatal testicular development: relationship to testicular descent. Pediatr Androl Endocrinol. 1979;6:37–46.Google Scholar
  59. 59.
    Hutson JM, Chow CW, Ng W-D. Persistent mullerian duct syndrome with transverse testicular ectopia. Pediatr Surg Int. 1987;2:191–4.Google Scholar
  60. 60.
    Scott JES. The Hutson hypothesis. A clinical study. Br J Urology. 1987;60:74–6.CrossRefGoogle Scholar
  61. 61.
    Hutson JM, Warne GL, Grover SR. Disorders of sex development: an integrated approach to management. Berlin: Springer; 2012.CrossRefGoogle Scholar
  62. 62.
    Picard JY, Tran D, Vigier B, et al. Maintien des canaux de Muller chez le lapin male par immunisation passive contre l’hormone anti-mullerienne pendant la vie foetale. C R Seances Acad Sci. 1983;297(Series III):567–70.Google Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • John M. Hutson
    • 1
  • Jørgen M. Thorup
    • 2
  • Spencer W. Beasley
    • 3
  1. 1.Royal Children’s Hospital University of MelbourneParkvilleAustralia
  2. 2.Univ. Hospital of Copenhagen RigshospitaletKøbenhavnDenmark
  3. 3.University of OtagoChristchurchNew Zealand

Personalised recommendations