title: Gene expression ontogeny of spermatogenesis in the marmoset uncovers primate characteristics during testicular development.
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.
authors.affiliation: Department of Physiology, School of Medicine, Keio University, 35 Shinanomachi, Shinjuku-ku, Tokyo 160-8582, Japan.
authors.forename: Zachary Yu-Ching
authors.initials: ZY
authors.lastname: Lin
authors.affiliation: Department of Molecular Biology, School of Medicine, Keio University, 35 Shinanomachi, Shinjuku-ku, Tokyo 160-8582, Japan.
authors.forename: Takamasa
authors.initials: T
authors.lastname: Hirano
authors.affiliation: Department of Physiology, School of Medicine, Keio University, 35 Shinanomachi, Shinjuku-ku, Tokyo 160-8582, Japan.
authors.forename: Shinsuke
authors.initials: S
authors.lastname: Shibata
authors.affiliation: Department of Molecular Biology, School of Medicine, Keio University, 35 Shinanomachi, Shinjuku-ku, Tokyo 160-8582, Japan; Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan.
authors.forename: Naomi M
authors.initials: NM
authors.lastname: Seki
authors.affiliation: Molecular Biology Section, Department of Cellular and Molecular Biology, Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan.
authors.forename: Ryunosuke
authors.initials: R
authors.lastname: Kitajima
authors.affiliation: Department of Applied Developmental Biology, Central Institute for Experimental Animals, 3-25-12 Tonomachi, Kawasaki 210-0821, Japan.
authors.forename: Ayako
authors.initials: A
authors.lastname: Sedohara
authors.affiliation: Department of Molecular Biology, School of Medicine, Keio University, 35 Shinanomachi, Shinjuku-ku, Tokyo 160-8582, Japan; Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan.
authors.forename: Mikiko C
authors.initials: MC
authors.lastname: Siomi
authors.affiliation: Department of Physiology, School of Medicine, Keio University, 35 Shinanomachi, Shinjuku-ku, Tokyo 160-8582, Japan; Department of Applied Developmental Biology, Central Institute for Experimental Animals, 3-25-12 Tonomachi, Kawasaki 210-0821, Japan; PRESTO Japan Science and Technology Agency, Japan.
authors.forename: Erika
authors.initials: E
authors.lastname: Sasaki
authors.affiliation: Department of Molecular Biology, School of Medicine, Keio University, 35 Shinanomachi, Shinjuku-ku, Tokyo 160-8582, Japan.
authors.forename: Haruhiko
authors.initials: H
authors.lastname: Siomi
authors.affiliation: Department of Physiology, School of Medicine, Keio University, 35 Shinanomachi, Shinjuku-ku, Tokyo 160-8582, Japan; Molecular Biology Section, Department of Cellular and Molecular Biology, Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan. Electronic address: imamura.masanori.2m@kyoto-u.ac.jp.
authors.forename: Masanori
authors.initials: M
authors.lastname: Imamura
authors.affiliation: Department of Physiology, School of Medicine, Keio University, 35 Shinanomachi, Shinjuku-ku, Tokyo 160-8582, Japan. Electronic address: hidokano@a2.keio.jp.
authors.forename: Hideyuki
authors.initials: H
authors.lastname: Okano
mesh_terms: D000818:Animals; D017209:Apoptosis / Q000502:physiology; D015153:Blotting, Western; D002144:Callithrix / Q000254:growth & development*; D018507:Gene Expression Regulation, Developmental / Q000502:physiology*; D005819:Genetic Markers / Q000235:genetics; D008297:Male; D008856:Microscopy, Fluorescence; D016253:Microscopy, Immunoelectron; D020133:Reverse Transcriptase Polymerase Chain Reaction; D013045:Species Specificity; D013091:Spermatogenesis / Q000502:physiology*; D013737:Testis / Q000166:cytology / Q000254:growth & development*
chemical_list: D005819:Genetic Markers
keywords: Common marmoset; Germ cell; Gonocyte; Spermatocyte; Spermatogenesis; Spermatogonia