Characterization, Cryopreservation, and Ablation of Spermatogonial Stem Cells in Adult Rhesus Macaques

Hermann, Brian P.; Sukhwani, Meena; Lin, Che‐Chern; Yi, Sheng; Tomko, Jamie; Rodriguez, Mario; Shuttleworth, Jennifer J.; McFarland, David; Hobbs, Robin M.; Pandolfi, Pier Paolo; Schatten, Gerald; Orwig, Kyle E.

doi:10.1634/stemcells.2007-0143

Cited by 197 publications

(210 citation statements)

References 51 publications

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“…On the basis of oligonucleotide microarray analyses and qRT-PCR, the expression of Dazl, Vasa, Zbtb16, and Uchl1 are all enriched in these prepubertal germ cells of both species as they are in mouse SSCs (20,21,(23)(24)(25). Rhesus monkey spermatogonia have also been shown to express Dazl, Vasa, and Zbtb16 (40). While Taf4b expression showed enrichment on the microarray in prepubertal human spermatogonia but not mouse gonocytes, it is known to be important for mouse SSC maintenance (32).…”

Section: Discussionmentioning

confidence: 99%

Prepubertal human spermatogonia and mouse gonocytes share conserved gene expression of germline stem cell regulatory molecules

Schmidt

Avarbock

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

177

137

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In the human testis, beginning at Ϸ2 months of age, gonocytes are replaced by adult dark (Ad) and pale (Ap) spermatogonia that make up the spermatogonial stem cell (SSC) pool. In mice, the SSC pool arises from gonocytes Ϸ6 days after birth. During puberty in both species, complete spermatogenesis is established by cells that differentiate from SSCs. Essentially pure populations of prepubertal human spermatogonia and mouse gonocytes were selected from testis biopsies and validated by confirming the presence of specific marker proteins in cells. Stem cell potential of germ cells was demonstrated by transplantation to mouse testes, following which the cells migrated to the basement membrane of the seminiferous tubule and were maintained similar to SSCs. Differential gene expression profiles generated between germ cells and testis somatic cells demonstrated that expression of genes previously identified as SSC and spermatogonial-specific markers (e.g., zinc-finger and BTB-domain containing 16, ZBTB16) was greatly elevated in both human spermatogonia and mouse gonocytes compared to somatic cells. Several genes were expressed at significantly higher levels in germ cells of both species. Most importantly, genes known to be essential for mouse SSC self-renewal (e.g., Ret proto-oncogene, Ret; GDNF-family receptor ␣1, Gfr␣1; and B-cell CLL/lymphoma 6, member B, Bcl6b) were more highly expressed in both prepubertal human spermatogonia and mouse gonocytes than in somatic cells. The results indicate remarkable conservation of gene expression, notably for self-renewal genes, in these prepubertal germline cells between two species that diverged phylogenetically Ϸ75 million years ago. mouse spermatogonia ͉ spermatogenesis

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Section: Discussionmentioning

confidence: 99%

Prepubertal human spermatogonia and mouse gonocytes share conserved gene expression of germline stem cell regulatory molecules

Schmidt

Avarbock

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

177

137

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“…Quantification of PLZF immunopositive cells per seminiferous cross section showed that 1.84±0.59 cells were positive, which is slightly less than the combined number of A dark and A pale spermatogonia per cross section, indicating that this marker is expressed by a subpopulation of undifferentiated spermatogonia in rhesus monkey as shown in Fig. 1 (Hermann et al, 2007(Hermann et al, , 2009.…”

Section: Comparative Expression Analyses Of Spermatogonial Markersmentioning

confidence: 91%

Male germline stem cells in non-human primates

Sharma¹,

Portela

Langenstroth-Röwer³

et al. 2017

Primate Biol.

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Abstract.Over the past few decades, several studies have attempted to decipher the biology of mammalian germline stem cells (GSCs). These studies provide evidence that regulatory mechanisms for germ cell specification and migration are evolutionarily conserved across species. The characteristics and functions of primate GSCs are highly distinct from rodent species; therefore the findings from rodent models cannot be extrapolated to primates. Due to limited availability of human embryonic and testicular samples for research purposes, two non-human primate models (marmoset and macaque monkeys) are extensively employed to understand human germline development and differentiation. This review provides a broader introduction to the in vivo and in vitro germline stem cell terminology from primordial to differentiating germ cells. Primordial germ cells (PGCs) are the most immature germ cells colonizing the gonad prior to sex differentiation into testes or ovaries. PGC specification and migratory patterns among different primate species are compared in the review. It also reports the distinctions and similarities in expression patterns of pluripotency markers (OCT4A, NANOG, SALL4 and LIN28) during embryonic developmental stages, among marmosets, macaques and humans. This review presents a comparative summary with immunohistochemical and molecular evidence of germ cell marker expression patterns during postnatal developmental stages, among humans and non-human primates. Furthermore, it reports findings from the recent literature investigating the plasticity behavior of germ cells and stem cells in other organs of humans and monkeys. The use of non-human primate models would enable bridging the knowledge gap in primate GSC research and understanding the mechanisms involved in germline development. Reported similarities in regulatory mechanisms and germ cell expression profile in primates demonstrate the preclinical significance of monkey models for development of human fertility preservation strategies.

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“…Certain rodent markers for germ cells and SSCs such as VASA, DAZL, PLZF, and GFR1are also of monkey (Hermann et al, 2007) and in other species. VASA expression marks spermatogonia in sheep (Borjigin et al, 2010), buffalo (Goel et al, 2010b) and bull (Fujihara et al, 2011) testis.…”

Section: Markers Of Sscsmentioning

confidence: 99%

“…PLZF is characterized as a hallmark for mouse spermatogonial stem/progenitor cells (Buaas et al, 2004;Costoya et al, 2004). In adult monkey, the expression of PLZF is confined to the A dark and/or A pale spermatogonia (Hermann et al, 2007). GPR125 has been demonstrated to be expressed in mouse spermatogonia and their progenitors (Seandel et al, 2007), and it is recently reported that GPR125 is also present in human spermatogonia ).…”

Section: Markers Of Sscsmentioning

confidence: 99%