Time course and role of luteinizing hormone and follicle-stimulating hormone in the expansion of the Leydig cell population at the time of puberty in the rhesus monkey (Macaca mulatta)

I. Verhagen, S. Ramaswamy, K.J. Teerds, J. Keijer, T.M. Plant

Research output: Contribution to journalArticleAcademicpeer-review

6 Citations (Scopus)

Abstract

In higher primates, development of the adult population of Leydig cells has received little attention. Here, the emergence of 3beta-hydroxysteroid dehydrogenase (HSD3B) positive cells in the testis of the rhesus monkey was examined during spontaneous puberty, and correlated with S-phase labeling in the interstitium at this critical stage of development. In addition, the relative role of luteinizing hormone (LH) and follicle-stimulating hormone (FSH) in initiating the pubertal expansion of Leydig cells was studied by precociously stimulating the juvenile testis in vivo with pulsatile 11-day infusions of recombinant LH and FSH, either alone or in combination. At the time of castration, testes were immersion fixed in Bouin's, embedded in paraffin, and sectioned at 5mum. Leydig cells/testis were enumerated using HSD3B as a Leydig cell marker. Leydig cell number per testis increased progressively during puberty to reach values in the adult approximately 10 fold greater than in early-pubertal animals. The rise in cell number was associated with an increase in nuclear diameter. That the pubertal expansion of Leydig cell number was driven primarily by the increase in LH secretion at this stage of development was suggested by the finding that precocious stimulation of mid-juvenile monkeys with LH, either alone or in combination with that of FSH, resulted in a 20-30 fold increase in the number of HSD3B-positive cells. Interestingly, precocious FSH stimulation, alone, also resulted in appearance of Leydig cells as indicated by the occasional HSD3B-positive cell in the interstitium. The nuclear diameter of these Leydig cells, however, was less than that of those generated in response to LH.
Original languageEnglish
Pages (from-to)924-930
JournalAndrology
Volume2
Issue number6
DOIs
Publication statusPublished - 2014

Fingerprint

Leydig Cells
Follicle Stimulating Hormone
Puberty
Luteinizing Hormone
Macaca mulatta
Testis
Population
Cell Count
Hydroxysteroid Dehydrogenases
Castration
Immersion
S Phase
Paraffin
Primates
Haplorhini

Keywords

  • gonadotropin-secretion
  • postnatal-development
  • human testis
  • proliferation
  • testosterone
  • fsh
  • differentiation
  • fascicularis
  • spermatogonia
  • localization

Cite this

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title = "Time course and role of luteinizing hormone and follicle-stimulating hormone in the expansion of the Leydig cell population at the time of puberty in the rhesus monkey (Macaca mulatta)",
abstract = "In higher primates, development of the adult population of Leydig cells has received little attention. Here, the emergence of 3beta-hydroxysteroid dehydrogenase (HSD3B) positive cells in the testis of the rhesus monkey was examined during spontaneous puberty, and correlated with S-phase labeling in the interstitium at this critical stage of development. In addition, the relative role of luteinizing hormone (LH) and follicle-stimulating hormone (FSH) in initiating the pubertal expansion of Leydig cells was studied by precociously stimulating the juvenile testis in vivo with pulsatile 11-day infusions of recombinant LH and FSH, either alone or in combination. At the time of castration, testes were immersion fixed in Bouin's, embedded in paraffin, and sectioned at 5mum. Leydig cells/testis were enumerated using HSD3B as a Leydig cell marker. Leydig cell number per testis increased progressively during puberty to reach values in the adult approximately 10 fold greater than in early-pubertal animals. The rise in cell number was associated with an increase in nuclear diameter. That the pubertal expansion of Leydig cell number was driven primarily by the increase in LH secretion at this stage of development was suggested by the finding that precocious stimulation of mid-juvenile monkeys with LH, either alone or in combination with that of FSH, resulted in a 20-30 fold increase in the number of HSD3B-positive cells. Interestingly, precocious FSH stimulation, alone, also resulted in appearance of Leydig cells as indicated by the occasional HSD3B-positive cell in the interstitium. The nuclear diameter of these Leydig cells, however, was less than that of those generated in response to LH.",
keywords = "gonadotropin-secretion, postnatal-development, human testis, proliferation, testosterone, fsh, differentiation, fascicularis, spermatogonia, localization",
author = "I. Verhagen and S. Ramaswamy and K.J. Teerds and J. Keijer and T.M. Plant",
year = "2014",
doi = "10.1111/andr.275",
language = "English",
volume = "2",
pages = "924--930",
journal = "Andrology",
issn = "2047-2927",
publisher = "Wiley",
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Time course and role of luteinizing hormone and follicle-stimulating hormone in the expansion of the Leydig cell population at the time of puberty in the rhesus monkey (Macaca mulatta). / Verhagen, I.; Ramaswamy, S.; Teerds, K.J.; Keijer, J.; Plant, T.M.

In: Andrology, Vol. 2, No. 6, 2014, p. 924-930.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Time course and role of luteinizing hormone and follicle-stimulating hormone in the expansion of the Leydig cell population at the time of puberty in the rhesus monkey (Macaca mulatta)

AU - Verhagen, I.

AU - Ramaswamy, S.

AU - Teerds, K.J.

AU - Keijer, J.

AU - Plant, T.M.

PY - 2014

Y1 - 2014

N2 - In higher primates, development of the adult population of Leydig cells has received little attention. Here, the emergence of 3beta-hydroxysteroid dehydrogenase (HSD3B) positive cells in the testis of the rhesus monkey was examined during spontaneous puberty, and correlated with S-phase labeling in the interstitium at this critical stage of development. In addition, the relative role of luteinizing hormone (LH) and follicle-stimulating hormone (FSH) in initiating the pubertal expansion of Leydig cells was studied by precociously stimulating the juvenile testis in vivo with pulsatile 11-day infusions of recombinant LH and FSH, either alone or in combination. At the time of castration, testes were immersion fixed in Bouin's, embedded in paraffin, and sectioned at 5mum. Leydig cells/testis were enumerated using HSD3B as a Leydig cell marker. Leydig cell number per testis increased progressively during puberty to reach values in the adult approximately 10 fold greater than in early-pubertal animals. The rise in cell number was associated with an increase in nuclear diameter. That the pubertal expansion of Leydig cell number was driven primarily by the increase in LH secretion at this stage of development was suggested by the finding that precocious stimulation of mid-juvenile monkeys with LH, either alone or in combination with that of FSH, resulted in a 20-30 fold increase in the number of HSD3B-positive cells. Interestingly, precocious FSH stimulation, alone, also resulted in appearance of Leydig cells as indicated by the occasional HSD3B-positive cell in the interstitium. The nuclear diameter of these Leydig cells, however, was less than that of those generated in response to LH.

AB - In higher primates, development of the adult population of Leydig cells has received little attention. Here, the emergence of 3beta-hydroxysteroid dehydrogenase (HSD3B) positive cells in the testis of the rhesus monkey was examined during spontaneous puberty, and correlated with S-phase labeling in the interstitium at this critical stage of development. In addition, the relative role of luteinizing hormone (LH) and follicle-stimulating hormone (FSH) in initiating the pubertal expansion of Leydig cells was studied by precociously stimulating the juvenile testis in vivo with pulsatile 11-day infusions of recombinant LH and FSH, either alone or in combination. At the time of castration, testes were immersion fixed in Bouin's, embedded in paraffin, and sectioned at 5mum. Leydig cells/testis were enumerated using HSD3B as a Leydig cell marker. Leydig cell number per testis increased progressively during puberty to reach values in the adult approximately 10 fold greater than in early-pubertal animals. The rise in cell number was associated with an increase in nuclear diameter. That the pubertal expansion of Leydig cell number was driven primarily by the increase in LH secretion at this stage of development was suggested by the finding that precocious stimulation of mid-juvenile monkeys with LH, either alone or in combination with that of FSH, resulted in a 20-30 fold increase in the number of HSD3B-positive cells. Interestingly, precocious FSH stimulation, alone, also resulted in appearance of Leydig cells as indicated by the occasional HSD3B-positive cell in the interstitium. The nuclear diameter of these Leydig cells, however, was less than that of those generated in response to LH.

KW - gonadotropin-secretion

KW - postnatal-development

KW - human testis

KW - proliferation

KW - testosterone

KW - fsh

KW - differentiation

KW - fascicularis

KW - spermatogonia

KW - localization

U2 - 10.1111/andr.275

DO - 10.1111/andr.275

M3 - Article

VL - 2

SP - 924

EP - 930

JO - Andrology

JF - Andrology

SN - 2047-2927

IS - 6

ER -