Development of the gubernaculum and processus vaginalis in freemartinism: Further evidence in support of a specific fetal testis hormone governing male-specific gubernacular development

Authors

  • Pieter Van Der Schoot,

    Corresponding author
    1. Department of Endocrinology & Reproduction, Faculty of Medicine and Health Sciences, Erasmus University, The Netherlands
    • Dept. of Endocrinology & REproduction, Faculty of Medicine and Health Sciences, Erasmus University Roterdam, P.O. Box 1738, 3000 DR Rotterdam, The Netherlands
    Search for more papers by this author
  • Bernard Vigier,

    1. INSERM unité 293, endocrinologie du Development, Ecole Normale Supérieure Départment de Biologie, Montrouge
    Search for more papers by this author
  • Jaques Prepin,

    1. UFR-Biomédicale des Saint-Pères, Department de Cytologie et d'Histologie, Ecole de Médicine, Université René Descartes, Paris, France
    Search for more papers by this author
  • Jean-Pierre Perchellet,

    1. Division of Biology, Kanas State University, Manhattan, Kansas
    Search for more papers by this author
  • Adriana Gittenberger-De Groot

    1. Department of Anatomy and Embryology, State University of Leidon, Leidon The Netherlands
    Search for more papers by this author

Abstract

Background: Freemartinism occurs in some speices of ruminants and affects most female bovine fetuses in hterrosexual, multiple pregnancies owing of susion of the chorionic blood circulations soon after implantation. Maldevelopment of the ovaries and Müllerian ducts have been described and recognized as resulting from exposure of their respective primoridia to an excess of anti-Müllerian hormone. The Present study aimed to analyse the prenatal growth the development of the gubernaculum in freemartins to find out its pssible affliction through foetal testis hormones derived from their male co-twin.

Methods: Histolgical sections of young and frawings and photographs of further developed freemartins and conrol male and female bovine foeuses were analysed. The specimens had been collected ealier for analsis of the time course of male and female gonadal and gential development and its impairment associated with freemartinism.

Results: The gubernaculum of 35–40 day-old male and female fetuses was in the intial stage of development and of similar appearance in all specimens. Gubenacula of 60–70-day-old male fetuss differed from those of females of similar age in various respects: the male gubernaculum size was larger and extension of the processus vaginalis was deeper. Freemartins showd and intermediate development with some individuals resembling male and othes resembling female agemates. During furher development, gubernacula in males developed into muscular cremaster sacs, whereas those in females generally did not develop beyond the size and structural complexity of 70-day-old foetuses. Beyond day 70 of fetal life, gubernaculum development in freemartins definitly showed male characteristics with respect to size and growth of a processus vaginalis with a cremaster muscular wall. The male-like pattern of the outgrowth of the processus vainalis changed during the second half of prenatal life. Rather than its further deepening as in mals, this structure became inveted to become emerging as a papilla-like structure from the inguinal abdomen bottom. An explanation is proposed for this unprecedented inversion, taking into account: (1) the faster and higher reaching rightsided ascent of the kidneys and gonads, (2) the femalelike outgrowth of the cranial gonadal suspensory ligaments, and (3) the absence of scrotum development. The ovaries and mesonephric remnants in developing freemartins, during their ascent together with the kidneys while remaining attached to the bottom of the developing processus vaginalis sacs via the gubernaculum ligament, are proposed to act together to pull up the bottom of the processus vaginalis sacs. From this action, “inverted hernia sacs” result as the irreversible consequence.

Conclusion: The data support the concept that foetal testes act, via as an yet unidentified third hormone, to establish malelike development of gubernacula into muscular cremaster sacs. Further work is required to reveal the identity of this hormone. Furthermore, the apparent similarity of the freemartins' inverted processus vaginalis sacs and the fetal rodents' gubernacular cones suggests that the ruminants' and rodents' processus vaginalis are essentially similar structures. Thus there is no longer an urgent need to distinguish between two different types of gubernaculum development and testis descent in rodents and ruminants, respectively, and involving or not fetal gubernacular cones. The present observations may thus contribute to the development of a unified hypothesis for sexually dimorphic development of the gubernaculum throughout the mammalian class. © 1995 Wiley-Liss, Inc.

Ancillary