Gene expression ontogeny of spermatogenesis in the marmoset uncovers primate characteristics during testicular development

Zachary Yu Ching Lin, Takamasa Hirano, Shinsuke Shibata, Naomi M. Seki, Ryunosuke Kitajima, Ayako Sedohara, Mikiko C. Siomi, Erika Sasaki, Haruhiko Siomi, Masanori Imamura, Hideyuki Okano

Research output: Contribution to journalArticle

7 Citations (Scopus)

Abstract

Mammalian spermatogenesis has been investigated extensively in rodents and a strictly controlled developmental process has been defined at cellular and molecular levels. In comparison, primate spermatogenesis has been far less well characterized. However, important differences between primate and rodent spermatogenesis are emerging so it is not always accurate to extrapolate findings in rodents to primate systems. Here, we performed an extensive immunofluorescence study of spermatogenesis in neonatal, juvenile, and adult testes in the common marmoset (Callithrix jacchus) to determine primate-specific patterns of gene expression that underpin primate germ cell development. Initially we characterized adult spermatogonia into two main classes; mitotically active C-KIT+Ki67+ cells and mitotically quiescent SALL4+PLZF+LIN28+DPPA4+ cells. We then explored the expression of a set of markers, including PIWIL1/MARWI, VASA, DAZL, CLGN, RanBPM, SYCP1 and HAPRIN, during germ cell differentiation from early spermatocytes through round and elongating spermatids, and a clear program of gene expression changes was determined as development proceeded. We then examined the juvenile marmoset testis. Markers of gonocytes demonstrated two populations; one that migrates to the basal membrane where they form the SALL4+ or C-KIT+ spermatogonia, and another that remains in the lumen of the seminiferous tubule. This later population, historically identified as pre-spermatogonia, expressed meiotic and apoptotic markers and were eliminated because they appear to have failed to correctly migrate. Our findings provide the first platform of gene expression dynamics in adult and developing germ cells of the common marmoset. Although we have characterized a limited number of genes, these results will facilitate primate spermatogenesis research and understanding of human reproduction.

Original languageEnglish
Pages (from-to)43-58
Number of pages16
JournalDevelopmental Biology
Volume400
Issue number1
DOIs
Publication statusPublished - 2015 Apr 1

Fingerprint

Callithrix
Spermatogenesis
Primates
Gene Expression
Spermatogonia
Germ Cells
Rodentia
Testis
Seminiferous Tubules
Spermatocytes
Spermatids
Population
Fluorescent Antibody Technique
Reproduction
Cell Differentiation
Membranes
Research
Genes

Keywords

  • Common marmoset
  • Germ cell
  • Gonocyte
  • Spermatocyte
  • Spermatogenesis
  • Spermatogonia

ASJC Scopus subject areas

  • Developmental Biology
  • Cell Biology
  • Molecular Biology
  • Medicine(all)

Cite this

Gene expression ontogeny of spermatogenesis in the marmoset uncovers primate characteristics during testicular development. / Lin, Zachary Yu Ching; Hirano, Takamasa; Shibata, Shinsuke; Seki, Naomi M.; Kitajima, Ryunosuke; Sedohara, Ayako; Siomi, Mikiko C.; Sasaki, Erika; Siomi, Haruhiko; Imamura, Masanori; Okano, Hideyuki.

In: Developmental Biology, Vol. 400, No. 1, 01.04.2015, p. 43-58.

Research output: Contribution to journalArticle

Lin, Zachary Yu Ching ; Hirano, Takamasa ; Shibata, Shinsuke ; Seki, Naomi M. ; Kitajima, Ryunosuke ; Sedohara, Ayako ; Siomi, Mikiko C. ; Sasaki, Erika ; Siomi, Haruhiko ; Imamura, Masanori ; Okano, Hideyuki. / Gene expression ontogeny of spermatogenesis in the marmoset uncovers primate characteristics during testicular development. In: Developmental Biology. 2015 ; Vol. 400, No. 1. pp. 43-58.
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