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      The Male Fetal Biomarker INSL3 Reveals Substantial Hormone Exchange between Fetuses in Early Pig Gestation

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          Abstract

          The peptide hormone INSL3 is uniquely produced by the fetal testis to promote the transabdominal phase of testicular descent. Because it is fetal sex specific, and is present in only very low amounts in the maternal circulation, INSL3 acts as an ideal biomarker with which to monitor the movement of fetal hormones within the pregnant uterus of a polytocous species, the pig. INSL3 production by the fetal testis begins at around GD30. At GD45 of the ca. 114 day gestation, a time at which testicular descent is promoted, INSL3 evidently moves from male to female allantoic compartments, presumably impacting also on the female fetal circulation. At later time-points (GD63, GD92) there is less inter-fetal transfer, although there still appears to be significant INSL3, presumably of male origin, in the plasma of female fetuses. This study thus provides evidence for substantial transfer of a peptide hormone between fetuses, and probably also across the placenta, emphasizing the vulnerability of the fetus to extrinsic hormonal influences within the uterus.

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          Cryptorchidism in mice mutant for Insl3.

          L Parada, S Nef (1999)
          Impaired testicular descent (cryptorchidism) is one of the most frequent congenital abnormalities in humans, involving 2% of male births. Cryptorchidism can result in infertility and increases risk for development of germ-cell tumours. Testicular descent from abdomen to scrotum occurs in two distinct phases: the trans-abdominal phase and the inguino-scrotal phase. Currently, little is known about the factors that regulate the trans-abdominal phase of testicular descent. Leydig insulin-like hormone (Insl3) is a member of the insulin hormone superfamily expressed in the developing testis. We show here that mice mutant for Insl3 are viable, but exhibit bilateral cryptorchidism due to developmental abnormalities of the gubernaculum, resulting in abnormal spermatogenesis and infertility. Female homozygotes have impaired fertility associated with deregulation of the oestrus cycle. These findings reveal roles for Insl3 in the development of the urogenital tract and in female fertility. Insl3 may act as a hormone to regulate the growth and differentiation of the gubernaculum, thereby mediating intra-abdominal testicular descent.
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            Targeted disruption of the Insl3 gene causes bilateral cryptorchidism.

            I Adham, W J ENGEL, A Holstein … (1999)
            The sexual dimorphic position of the gonads in mammals is dependent on differential development of two ligaments, the cranial suspensory ligament (CSL) and the gubernaculum. During male embryogenesis, outgrowth of the gubernaculum and regression of the CSL result in transabdominal descent of the testes, whereas in the female, development of the CSL in conjunction with failure of the gubernaculum development holds the ovaries in a position lateral to the kidneys. Several lines of evidence suggest that regression of the CSL and induction of gubernaculum development are mediated by testosterone and a yet unidentified testicular factor, respectively. The Insl3 gene (originally designated Ley I-L), a member of the insulin-like superfamily, is specifically expressed in Leydig cells of the fetal and postnatal testis and in theca cells of the postnatal ovary. Here we show that male mice homozygous for a targeted deletion of the Insl3 locus exhibit bilateral cryptorchidism with free moving testes and genital ducts. These malformations are due to failure of gubernaculum development during embryogenesis. In double-mutant male mice for Insl3 and androgen receptor genes, testes are positioned adjacent to the kidneys and steadied in the abdomen by the CSL. These findings demonstrate, that the Insl3 induces gubernaculum development in an androgen-independent way, while androgen-mediated regression of the CSL occurs independently from Insl3.
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              Reproductive cycles in pigs.

              N.M. Soede, P. Langendijk, B. Kemp (2011)
              The oestrous cycle in pigs spans a period of 18-24 days. It consists of a follicular phase of 5-7 days and a luteal phase of 13-15 days. During the follicular phase, small antral follicles develop into large, pre-ovulatory follicles. Being a polytocous species, the pig may ovulate from 15 to 30 follicles, depending on age, nutritional status and other factors. During the luteal phase, follicle development is less pronounced, although there is probably a considerable turnover of primordial to early antral follicles that fail to further develop due to progesterone inhibition of gonadotrophic hormones. Nevertheless, formation of the early antral follicle pool during this stage probably has a major impact on follicle dynamics in the follicular phase in terms of number and quality of follicles. Generally, gilts are mated at their second or third estrous cycle after puberty. After farrowing, pigs experience a lactational anoestrus period, until they are weaned and the follicular phase is initiated, resulting in oestrus and ovulation 4-7 days after weaning. This paper describes the major endocrine processes during the follicular and luteal phases that precede and follow ovulation. The role of nutrition and metabolic status on these processes are briefly discussed.
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                Author and article information

                Contributors
                Elissa Z. Cameron: Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (iso-abbrev): PLoS ONE
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, CA USA )
                ISSN (Electronic): 1932-6203
                Publication date (Electronic): 31 March 2016
                Publication date Collection: 2016
                Volume: 11
                Issue: 3
                Electronic Location Identifier: e0152689
                Affiliations
                [1 ]FBN Leibniz Institute for Farm Animal Biology, 18196 Dummerstorf, Germany
                [2 ]School of Biosciences, University of Nottingham, Sutton Bonington, LE12 5RD, United Kingdom
                University of Tasmania, AUSTRALIA
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: AV RA-I RI. Performed the experiments: AV KH RA-I. Analyzed the data: AV KH RA-I RI. Contributed reagents/materials/analysis tools: AV RA-I RI. Wrote the paper: AV RA-I KH RI.

                Article
                Publisher ID: PONE-D-15-53081
                DOI: 10.1371/journal.pone.0152689
                PMC ID: 4816311
                PubMed ID: 27031644
                SO-VID: 417faf60-9908-4ed9-a622-d49510d543b1
                Copyright © © 2016 Vernunft et al
                License:

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                Date received : 12 December 2015
                Date accepted : 17 March 2016
                Page count
                Figures: 4, Tables: 0, Pages: 14
                Funding
                This project was funded by incidental support from the Leibniz Institute for Farm Animal Biology, Dummerstorf, and by the School of Biosciences, University of Nottingham. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Subject: Research Article
                Subject: Biology and Life Sciences
                Subject: Developmental Biology
                Subject: Embryology
                Subject: Fetuses
                Subject: Biology and Life Sciences
                Subject: Anatomy
                Subject: Body Fluids
                Subject: Amniotic Fluid
                Subject: Medicine and Health Sciences
                Subject: Anatomy
                Subject: Body Fluids
                Subject: Amniotic Fluid
                Subject: Biology and Life Sciences
                Subject: Physiology
                Subject: Body Fluids
                Subject: Amniotic Fluid
                Subject: Medicine and Health Sciences
                Subject: Physiology
                Subject: Body Fluids
                Subject: Amniotic Fluid
                Subject: Biology and Life Sciences
                Subject: Agriculture
                Subject: Livestock
                Subject: Swine
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Animals
                Subject: Vertebrates
                Subject: Amniotes
                Subject: Mammals
                Subject: Swine
                Subject: Biology and Life Sciences
                Subject: Biochemistry
                Subject: Hormones
                Subject: Peptide Hormones
                Subject: Medicine and Health Sciences
                Subject: Women's Health
                Subject: Maternal Health
                Subject: Pregnancy
                Subject: Medicine and Health Sciences
                Subject: Women's Health
                Subject: Obstetrics and Gynecology
                Subject: Pregnancy
                Subject: Biology and Life Sciences
                Subject: Anatomy
                Subject: Body Fluids
                Subject: Blood
                Subject: Blood Plasma
                Subject: Medicine and Health Sciences
                Subject: Anatomy
                Subject: Body Fluids
                Subject: Blood
                Subject: Blood Plasma
                Subject: Biology and Life Sciences
                Subject: Physiology
                Subject: Body Fluids
                Subject: Blood
                Subject: Blood Plasma
                Subject: Medicine and Health Sciences
                Subject: Physiology
                Subject: Body Fluids
                Subject: Blood
                Subject: Blood Plasma
                Subject: Medicine and Health Sciences
                Subject: Hematology
                Subject: Blood
                Subject: Blood Plasma
                Subject: Biology and Life Sciences
                Subject: Biochemistry
                Subject: Hormones
                Subject: Medicine and Health Sciences
                Subject: Endocrinology
                Subject: Endocrine Physiology
                Subject: Hormone Transport
                Subject: Biology and Life Sciences
                Subject: Physiology
                Subject: Endocrine Physiology
                Subject: Hormone Transport
                Subject: Medicine and Health Sciences
                Subject: Physiology
                Subject: Endocrine Physiology
                Subject: Hormone Transport
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                Data Availability All relevant data are within the paper.

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