Sex-specific regulation of prolactin secretion by pituitary activins in postnatal development

in Journal of Endocrinology
Authors:
Alejandra Abeledo-Machado Instituto de Biología y Medicina Experimental (IBYME), CONICET, Buenos Aires, Argentina

Search for other papers by Alejandra Abeledo-Machado in
Current site
Google Scholar
PubMed
Close
,
Dana Bornancini Instituto de Biología y Medicina Experimental (IBYME), CONICET, Buenos Aires, Argentina

Search for other papers by Dana Bornancini in
Current site
Google Scholar
PubMed
Close
,
Milagros Peña-Zanoni Instituto de Biología y Medicina Experimental (IBYME), CONICET, Buenos Aires, Argentina

Search for other papers by Milagros Peña-Zanoni in
Current site
Google Scholar
PubMed
Close
,
María Andrea Camilletti Instituto de Biología y Medicina Experimental (IBYME), CONICET, Buenos Aires, Argentina

Search for other papers by María Andrea Camilletti in
Current site
Google Scholar
PubMed
Close
,
Erika Yanil Faraoni Instituto de Biología y Medicina Experimental (IBYME), CONICET, Buenos Aires, Argentina

Search for other papers by Erika Yanil Faraoni in
Current site
Google Scholar
PubMed
Close
, and
Graciela Díaz-Torga Instituto de Biología y Medicina Experimental (IBYME), CONICET, Buenos Aires, Argentina

Search for other papers by Graciela Díaz-Torga in
Current site
Google Scholar
PubMed
Close
https://orcid.org/0000-0001-7373-6893

Correspondence should be addressed to G Diaz-Torga: gdiaz@ibyme.conicet.gov.ar
Restricted access
Rent on DeepDyve

Sign up for journal news

Serum prolactin increases from birth to adulthood in rats, being higher in females from birth. The maturation of hypothalamic/gonadal prolactin-releasing and -inhibiting factors does not explain some sex differences observed. During the first weeks of life, prolactin secretion increases, even when lactotrophs are isolated in vitro, in the absence of those controls, suggesting the participation of intra-pituitary factors in this control. The present work aimed to study the involvement of pituitary activins in the regulation of prolactin secretion during post-natal development. Sex differences were also highlighted. Female and male Sprague–Dawley rats at 11, 23 and 45postnatal days were used. Pituitary expression of activin subunits and activin receptors was maximum in p11 female pituitaries, being even higher than that observed in males. Those expressions decrease with age in females, and then the gender differences disappear at p23. Inhbb expression strongly increases at p45 in males, being the predominant subunit in this sex in adulthood. Activin inhibition of prolactin is mediated by the inhibition of Pit-1 expression. This action involves not only the canonical pSMAD pathway but also the phosphorylation of p38MAPK. At p11, almost all lactotrophs express p-p38MAPK in females, and its expression decreases with age with a concomitant increase in Pit-1. Our findings suggest that the inhibitory regulation of pituitary activins on prolactin secretion is sex specific; this regulation is more relevant in females during the first week of life and decreases with age; this intra-pituitary regulation is involved in the sex differences observed in serum prolactin levels during postnatal development.

 

  • Collapse
  • Expand
  • Abeledo-Machado A, Pérez PA, Camilletti MA, Faraoni EY, Picech F, Petiti JP, Gutiérrez S & & Diaz-Torga G 2020 TGFβ1 regulates prolactin secretion during postnatal development: gender differences. Journal of Endocrinology 246 2939. (https://doi.org/10.1530/JOE-20-0041)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Becú-Villalobos D, Lacau-Mengido IM, Díaz-Torga GS & & Libertun C 1992 Ontogenic studies of the neural control of adenohypophyseal hormones in the rat. II. prolactin. Cellular and Molecular Neurobiology 12 119. (https://doi.org/10.1007/BF00711635)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ben-Jonathan N & & Hnasko R 2001 Dopamine as a prolactin (PRL) inhibitor. Endocrine Reviews 22 724763. (https://doi.org/10.1210/edrv.22.6.0451)

  • Bilezikjian LM, Justice NJ, Blackler AN, Wiater E & & Vale WW 2012 2012 cell-type specific modulation of pituitary cells by activin, inhibin and follistatin. Molecular and Cellular Endocrinology 359 4352. (https://doi.org/10.1016/j.mce.2012.01.025)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Camilletti MAMA, Abeledo-Machado A, Ferraris J, Pérez PAPA, Faraoni EYEY, Pisera D, Gutierrez S & & Díaz-Torga G 2019a Role of GPER in the anterior pituitary gland focusing on lactotroph function. Journal of Endocrinology 240 99110. (https://doi.org/10.1530/JOE-18-0402)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Camilletti MA, Abeledo-Machado A, Faraoni EY, Thomas P & & Díaz-Torga G 2019b New insights into progesterone actions on prolactin secretion and prolactinoma development. Steroids 152 108496. (https://doi.org/10.1016/j.steroids.2019.108496)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Chen HT 1987 Postnatal development of pituitary lactotropes in the rat measured by reverse hemolytic plaque assay. Endocrinology 120 247253. (https://doi.org/10.1210/endo-120-1-247)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • De Guise C, Lacerte A, Rafiei S, Reynaud R, Roy M, Brue T & & Lebrun JJ 2006 Activin inhibits the human Pit-1 gene promoter through the p38 kinase pathway in a smad-independent manner. Endocrinology 147 43514362. (https://doi.org/10.1210/en.2006-0444)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Derynck R & & Zhang YE 2003 Smad-dependent and Smad-independent pathways in TGF-β family signalling. Nature 425 577584. (https://doi.org/10.1038/nature02006)

  • Díaz-Torga GS, Becú-Villalobos D & & Libertun C 1994 Ontogeny of angiotensin-II-induced prolactin release in vivo and in vitro in female and male rats. Neuroendocrinology 59 5762. (https://doi.org/10.1159/000126638)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Faraoni EY, Abeledo Machado AI, Pérez PA, Marcial López CA, Camilletti MA, Peña-Zanoni M, Rulli SB, Gutiérrez S & & Díaz-Torga G 2020 Activin-inhibitory action on lactotrophs is decreased in lactotroph hyperplasia. Journal of Endocrinology 244 415429. (https://doi.org/10.1530/JOE-19-0326)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Grattan DR 2015 60 years of neuroendocrinology: the hypothalamo-prolactin axis. Journal of Endocrinology 226 T101T122. (https://doi.org/10.1530/JOE-15-0213)

  • Gu Z, Nomura M, Simpson BB, Lei H, Feijen A, Van Den Eijnden-Van Raaij J, Donahoe PK & & Li E 1998 The type I activin receptor ActRIB is required for egg cylinder organization and gastrulation in the mouse. Genes and Development 12 844857. (https://doi.org/10.1101/gad.12.6.844)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kansra S, Yamagata S, Sneade L, Foster L & & Ben-Jonathan N 2005 Differential effects of estrogen receptor antagonists on pituitary lactotroph proliferation and prolactin release. Molecular and Cellular Endocrinology 239 2736. (https://doi.org/10.1016/j.mce.2005.04.008)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Karanth S, Dutt A & & Juneja HS 1987 Age-related release of prolactin by the pituitary and the pituitary-hypothalamic complex in vitro: an attempt to describe the development of the hypothalamic prolactin-inhibiting and -releasing activities in male rats. Journal of Endocrinology 115 405409. (https://doi.org/10.1677/joe.0.1150405)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Keogh EJ, Lee VW, Rennie GC, Burger HG, Hudson B & & De Kretser DM 1976 Selective suppression of FSH by testicular extracts. Endocrinology 98 9971004. (https://doi.org/10.1210/endo-98-4-997)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Lacerte A, Lee EH, Reynaud R, Canaff L, De Guise C, Devost D, Ali S, Hendy GN & & Lebrun JJ 2004 Activin inhibits pituitary prolactin expression and cell growth through Smads, Pit-1 and menin. Molecular Endocrinology 18 15581569. (https://doi.org/10.1210/me.2003-0470)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Leong DA, Frawley LS & & Neill JD 1983 Neuroendocrine control of prolactin secretion. Annual Review of Physiology 45 109127. (https://doi.org/10.1146/annurev.ph.45.030183.000545)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Makanji Y, Zhu J, Mishra R, Holmquist C, Wong WPS, Schwartz NB, Mayo KE & & Woodruff TK 2014 Inhibin at 90: from discovery to clinical application, a historical review. Endocrine Reviews 35 747794. (https://doi.org/10.1210/er.2014-1003)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Matzuk MM, Kumar TR, Vassalli A, Bickenbach JR, Roop DR, Jaenisch R & & Bradley A 1995a Functional analysis of activins during mammalian development. Nature 374 354356. (https://doi.org/10.1038/374354a0)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Matzuk MM, Kumar TR & & Bradley A 1995b Different phenotypes for mice deficient in either activins or activin receptor type II. Nature 374 356360. (https://doi.org/10.1038/374356a0)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Minami S & & Sarkar DK 1997 Transforming growth factor-beta 1 inhibits prolactin secretion and lactotropic cell proliferation in the pituitary of oestrogen-treated Fischer 344 rats. Neurochemistry International 30 499506. (https://doi.org/10.1016/s0197-0186(9600087-3)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Nazian SJ 1983 Pituitary function during the sexual maturation of the male rat: inhibition of prolactin secretion by exogenous dopamine. Biology of Reproduction 28 645651. (https://doi.org/10.1095/biolreprod28.3.645)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Oh SP & & Li E 1997 The signaling pathway mediated by the type IIB activin receptor controls axial patterning and lateral asymmetry in the mouse. Genes and Development 11 18121826. (https://doi.org/10.1101/gad.11.14.1812)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Recouvreux MV, Guida MC, Rifkin DB, Becu-Villalobos D & & Díaz-Torga G 2011 Active and total transforming growth factor-β1 are differentially regulated by dopamine and estradiol in the pituitary. Endocrinology 152 27222730. (https://doi.org/10.1210/en.2010-1464)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Sarkar DK, Pastorcic M, De A, Engel M, Moses H & & Ghasemzadeh MB 1998 Role of transforming growth factor (TGF)-beta Type I and TGF-beta type II receptors in the TGF-beta1-regulated gene expression in pituitary prolactin-secreting lactotropes. Endocrinology 139 36203628. (https://doi.org/10.1210/endo.139.8.6135)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Schang G, Ongaro L, Schultz H, Wang Y, Zhou X, Brûlé E, Boehm U, Lee SJ & & Bernard DJ 2020 Murine FSH production depends on the activin Type II receptors ACVR2A and ACVR2B. Endocrinology 161. (https://doi.org/10.1210/endocr/bqaa056)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Thompson TB, Lerch TF, Cook RW, Woodruff TK & & Jardetzky TS 2005 The structure of the follistatin:activin complex reveals antagonism of both type I and type II receptor binding. Developmental Cell 9 535543. (https://doi.org/10.1016/j.devcel.2005.09.008)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Vale W, Rivier J, Vaughan J, McClintock R, Corrigan A, Woo W, Karr D & & Spiess J 1986 Purification and characterization of an FSH releasing protein from porcine ovarian follicular fluid. Nature 321 776779. (https://doi.org/10.1038/321776a0)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Vassalli A, Matzuk MM, Gardner HAR, Lee KF & & Jaenisch R 1994 Activin/inhibin βB subunit gene disruption leads to defects in eyelid development and female reproduction. Genes and Development 8 414427. (https://doi.org/10.1101/gad.8.4.414)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Walker DM, Kirson D, Perez LF & & Gore AC 2012 Molecular profiling of postnatal development of the hypothalamus in female and male Rats1. Biology of Reproduction 87 129. (https://doi.org/10.1095/biolreprod.112.102798)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Welt C, Sidis Y, Keutmann H & & Schneyer A 2002 Activins, inhibins, and follistatins: from endocrinology to signaling. A paradigm for the new millennium. Experimental Biology and Medicine 227 724752. (https://doi.org/10.1177/153537020222700905)

    • PubMed
    • Search Google Scholar
    • Export Citation