Testicular germ cells can colonize sexually undifferentiated embryonic gonad and produce functional eggs in fish

Okutsu, Tomoyuki; Suzuki, Kensuke; Takeuchi, Yutaka; Takeuchi, Toshio; Yoshizaki, Goro

doi:10.1073/pnas.0509218103

Cited by 243 publications

(227 citation statements)

References 20 publications

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“…In both rainbow trout and medaka, vasa expression in gonia does not show sex dimorphism. Data for rainbow trout are from the present study and (Li et al, 2011 In press), and data for medaka are according to Together with transplantation data (Okutsu et al, 2006;Yoshizaki et al, 2010), our finding suggests the plasticity of gonial sexuality for reprogramming into both sexes under the influence of the gonadal sex. Our findings suggest that sperm/ egg decision and mitosis/meiosis decision are two independent events, and that sperm/egg decision appears to precede mitosis/meiosis decision.…”

Section: Resultssupporting

confidence: 73%

“…We chose trout as a test-organism to study the sexuality of germ cells prior to meiosis, because in this organism, spermatogonia and oogonia have been demonstrated to take the male or female pathway according to the sex of a host gonad but irrespective of the sex of their origin (Okutsu et al, 2006;Yoshizaki et al, 2010). Recently, we have established that boule and dazl encoding RNA binding proteins of the DAZ family are germ cell markers in rainbow trout (Li et al, 2011).…”

Section: Resultsmentioning

confidence: 99%

“…Gonia within a testis (spermatogonia) or an ovary (oogonia) contain germ stem cells capable of self-renewal and differentiation even in culture (Hong et al, 2004). Transplantation data in fish support that gonia are sexually indeterminate or plastic (Okutsu et al, 2006;Okutsu et al, 2007;Yoshizaki et al, 2010). However, there is no evidence for the absence or presence of gonial sex (Kocer et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

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Germ cell sex prior to meiosis in the rainbow trout

Li¹,

Shen²,

Wong³

et al. 2011

Protein Cell

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Germ cells make two major decisions when they move from an indeterminate state to their final stage of gamete production. One decision is sexual commitment for sperm or egg production, and the other is to maintain mitotic division or entry into meiosis. It is unclear whether the two decisions are made as a single event or separate events, because there has been no evidence for the presence of germ cell sex prior to meiosis. Here we report direct evidence in the fish rainbow trout that gonia have distinct sexuality. We show that dazl expression occurs in both male and female gonia but exhibits differential intracellular distribution. More strikingly, we show that boule is highly expressed in male gonia but absent in female gonia. Therefore, mitotic gonia possess sex, sperm/egg decision and mitosis/meiosis decision are two independent events, and sperm/egg decision precedes mitosis/meiosis decision in rainbow trout, making this organism a unique vertebrate model for mechanistic understanding of germ cell sex differentiation and relationship between the two decisions.

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Section: Resultssupporting

confidence: 73%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Germ cell sex prior to meiosis in the rainbow trout

Li¹,

Shen²,

Wong³

et al. 2011

Protein Cell

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“…Regardless of donor trout sex, germ cells that were transplanted into larva assumed the sexual fate of the recipient gonad 18, 19. We also transplanted GFP‐labelled germ cells isolated from adult testis into the coelomic cavity of larva and found that GFP‐germ cells developed into oocytes (unpublished results).…”

Section: Introductionmentioning

confidence: 86%

Germline stem cells are critical for sexual fate decision of germ cells

Tanaka

2016

BioEssays

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Egg or sperm? The mechanism of sexual fate decision in germ cells has been a long‐standing issue in biology. A recent analysis identified foxl3 as a gene that determines the sexual fate decision of germ cells in the teleost fish, medaka. foxl3/Foxl3 acts in female germline stem cells to repress commitment into male fate (spermatogenesis), indicating that the presence of mitotic germ cells in the female is critical for continuous sexual fate decision of germ cells in medaka gonads. Interestingly, foxl3 is found in most vertebrate genomes except for mammals. This provides the interesting possibility that the sexual fate of germ cells in mammals is determined in a different way compared to foxl3‐possessing vertebrates. Considering the fact that germline stem cells are the cells where foxl3 begins to express and sexual fate decision initiates and mammalian ovary does not have typical germline stem cells, the mechanism in mammals may have been co‐evolved with germline stem cell loss in mammalian ovary.

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“…Although most studies have been performed in rodents, germ cell transplantation has also been applied to non-rodent species as pigs, goats, cattle, monkeys and recently fish and chickens (Honaramooz et al, 2002a(Honaramooz et al, ,b, 2003Schlatt et al, 2002;Izadyar et al, 2003b;Takeuchi et al, 2003;Yoshizaki et al, 2005;Lee et al, 2006;Mikkola et al, 2006;Okutsu et al 2006;Trefil et al 2006), as reviewed by Dobrinski, (2008). The first hurdle found when germ cell transplantation was applied to livestock species was the differences in testicular anatomy and physiology.…”

Section: Sscs Transplantation and Transgenesismentioning

confidence: 99%