Галерея 3479468

Галерея 3479468
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Proc Natl Acad Sci U S A

v.109(42); 2012 Oct 16

PMC3479468

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Proc Natl Acad Sci U S A. 2012 Oct 16; 109(42): 16934–16938.
Published online 2012 Sep 10. doi: 10.1073/pnas.1211845109
a Department of Urology, Yokohama City University Graduate School of Medicine, Yokohama 236-0004, Japan;
b RIKEN, Bioresource Center, Ibaraki 305-0074, Japan;
c Division of Germ Cell Biology, National Institute for Basic Biology, National Institutes of Natural Sciences, Okazaki, 444-8787, Japan;
d Department of Basic Biology, School of Life Science, Graduate University for Advanced Studies (Sokendai), Okazaki, 444-8787, Japan;
e Department of Medical Life Science, Yokohama City University, Yokohama 236-0004, Japan; and
f Advanced Medical Research Center, Yokohama City University, Yokohama 236-0004, Japan
1 To whom correspondence should be addressed. E-mail: pj.ca.uc-amahokoy.dem@awago .
Edited by Ralph L. Brinster, University of Pennsylvania, Philadelphia, PA, and approved August 16, 2012 (received for review July 11, 2012)
See commentary " Making male gametes in culture " in volume 109 on page 16762.
GUID: B51F6FBA-BE91-4328-B2C3-4831EEC12004
GUID: B7093504-2A0D-48D2-BC33-993D125E1F6F
1. Russell LD, Ettlin RA, Sinha Hikim AP, Clegg ED. Histological and Histopathological Evaluation of the Testis. Clearwater, FL: Cache River; 1990. [ Google Scholar ]
2. Sugimoto R, Nabeshima Y, Yoshida S. Retinoic acid metabolism links the periodical differentiation of germ cells with the cycle of Sertoli cells in mouse seminiferous epithelium. Mech Dev. 2012; 128 :610–624. [ PubMed ] [ Google Scholar ]
3. Gohbara A, et al. In vitro murine spermatogenesis in an organ culture system. Biol Reprod. 2010; 83 :261–267. [ PubMed ] [ Google Scholar ]
4. Sato T, et al. In vitro production of functional sperm in cultured neonatal mouse testes. Nature. 2011; 471 :504–507. [ PubMed ] [ Google Scholar ]
5. Sato T, et al. In vitro production of fertile sperm from murine spermatogonial stem cell lines. Nat Commun. 2011; 2 :472. [ PubMed ] [ Google Scholar ]
6. Runyan C, et al. Steel factor controls midline cell death of primordial germ cells and is essential for their normal proliferation and migration. Development. 2006; 133 :4861–4869. [ PubMed ] [ Google Scholar ]
7. Flanagan JG, Chan DC, Leder P. Transmembrane form of the kit ligand growth factor is determined by alternative splicing and is missing in the Sld mutant. Cell. 1991; 64 :1025–1035. [ PubMed ] [ Google Scholar ]
8. Russell ES. Hereditary anemias of the mouse: A review for geneticists. Adv Genet. 1979; 20 :357–459. [ PubMed ] [ Google Scholar ]
9. Silvers WK. The Coat Colors of Mice: A Model for Mammalian Gene Action and Interaction. New York: Springer; 1979. [ Google Scholar ]
10. Broudy VC. Stem cell factor and hematopoiesis. Blood. 1997; 90 :1345–1364. [ PubMed ] [ Google Scholar ]
11. Vincent S, et al. Stage-specific expression of the Kit receptor and its ligand (KL) during male gametogenesis in the mouse: A Kit-KL interaction critical for meiosis. Development. 1998; 125 :4585–4593. [ PubMed ] [ Google Scholar ]
12. Ohta H, Yomogida K, Dohmae K, Nishimune Y. Regulation of proliferation and differentiation in spermatogonial stem cells: The role of c-kit and its ligand SCF. Development. 2000; 127 :2125–2131. [ PubMed ] [ Google Scholar ]
13. Heyworth CM, Whetton AD, Nicholls S, Zsebo K, Dexter TM. Stem cell factor directly stimulates the development of enriched granulocyte-macrophage colony-forming cells and promotes the effects of other colony-stimulating factors. Blood. 1992; 80 :2230–2236. [ PubMed ] [ Google Scholar ]
14. Lennartsson J, Shivakrupa R, Linnekin D. Synergistic growth of stem cell factor and granulocyte macrophage colony-stimulating factor involves kinase-dependent and -independent contributions from c-Kit. J Biol Chem. 2004; 279 :44544–44553. [ PubMed ] [ Google Scholar ]
15. Duarte RF, Franf DA. The synergy between stem cell factor (SCF) and granulocyte colony-stimulating factor (G-CSF): Molecular basis and clinical relevance. Leuk Lymphoma. 2002; 43 :1179–1187. [ PubMed ] [ Google Scholar ]
16. Pearson MA, et al. Investigation of the molecular mechanisms underlying growth factor synergy: The role of ERK 2 activation in synergy. Growth Factors. 1998; 15 :293–306. [ PubMed ] [ Google Scholar ]
17. Broudy VC, et al. Stem cell factor influences the proliferation and erythroid differentiation of the MB-02 human erythroleukemia cell line by binding to a high-affinity c-kit receptor. Blood. 1993; 82 :436–444. [ PubMed ] [ Google Scholar ]
18. Kokkinaki M, et al. The molecular signature of spermatogonial stem/progenitor cells in the 6-day-old mouse testis. Biol Reprod. 2009; 80 :707–717. [ PMC free article ] [ PubMed ] [ Google Scholar ]
19. Oatley JM, Oatley MJ, Avarbock MR, Tobias JW, Brinster RL. Colony stimulating factor 1 is an extrinsic stimulator of mouse spermatogonial stem cell self-renewal. Development. 2009; 136 :1191–1199. [ PMC free article ] [ PubMed ] [ Google Scholar ]
20. Ogawa T, Dobrinski I, Avarbock MR, Brinster RL. Transplantation of male germ line stem cells restores fertility in infertile mice. Nat Med. 2000; 6 :29–34. [ PMC free article ] [ PubMed ] [ Google Scholar ]
21. Kanatsu-Shinohara M, et al. Germline niche transplantation restores fertility in infertile mice. Hum Reprod. 2005; 20 :2376–2382. [ PubMed ] [ Google Scholar ]
22. Ikawa M, et al. Restoration of spermatogenesis by lentiviral gene transfer: Offspring from infertile mice. Proc Natl Acad Sci USA. 2002; 99 :7524–7529. [ PMC free article ] [ PubMed ] [ Google Scholar ]
23. Kanatsu-Shinohara M, et al. Adenovirus-mediated gene delivery and in vitro microinsemination produce offspring from infertile male mice. Proc Natl Acad Sci USA. 2002; 99 :1383–1388. [ PMC free article ] [ PubMed ] [ Google Scholar ]
24. Cohen PE, Chisholm O, Arceci RJ, Stanley ER, Pollard JW. Absence of colony-stimulating factor-1 in osteopetrotic (csfmop/csfmop) mice results in male fertility defects. Biol Reprod. 1996; 55 :310–317. [ PubMed ] [ Google Scholar ]
25. Krausz C. Male infertility: Pathogenesis and clinical diagnosis. Best Pract Res Clin Endocrinol Metab. 2011; 25 :271–285. [ PubMed ] [ Google Scholar ]
26. McLachlan RI, O’Bryan MK. Clinical Review#: State of the art for genetic testing of infertile men. J Clin Endocrinol Metab. 2010; 95 :1013–1024. [ PubMed ] [ Google Scholar ]
Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences
1. Russell LD, Ettlin RA, Sinha Hikim AP, Clegg ED. Histological and Histopathological Evaluation of the Testis. Clearwater, FL: Cache River; 1990. [ Google Scholar ] [ Ref list ]
2. Sugimoto R, Nabeshima Y, Yoshida S. Retinoic acid metabolism links the periodical differentiation of germ cells with the cycle of Sertoli cells in mouse seminiferous epithelium. Mech Dev. 2012; 128 :610–624. [ PubMed ] [ Google Scholar ] [ Ref list ]
3. Gohbara A, et al. In vitro murine spermatogenesis in an organ culture system. Biol Reprod. 2010; 83 :261–267. [ PubMed ] [ Google Scholar ] [ Ref list ]
4. Sato T, et al. In vitro production of functional sperm in cultured neonatal mouse testes. Nature. 2011; 471 :504–507. [ PubMed ] [ Google Scholar ] [ Ref list ]
5. Sato T, et al. In vitro production of fertile sperm from murine spermatogonial stem cell lines. Nat Commun. 2011; 2 :472. [ PubMed ] [ Google Scholar ] [ Ref list ]
6. Runyan C, et al. Steel factor controls midline cell death of primordial germ cells and is essential for their normal proliferation and migration. Development. 2006; 133 :4861–4869. [ PubMed ] [ Google Scholar ] [ Ref list ]
7. Flanagan JG, Chan DC, Leder P. Transmembrane form of the kit ligand growth factor is determined by alternative splicing and is missing in the Sld mutant. Cell. 1991; 64 :1025–1035. [ PubMed ] [ Google Scholar ] [ Ref list ]
8. Russell ES. Hereditary anemias of the mouse: A review for geneticists. Adv Genet. 1979; 20 :357–459. [ PubMed ] [ Google Scholar ] [ Ref list ]
9. Silvers WK. The Coat Colors of Mice: A Model for Mammalian Gene Action and Interaction. New York: Springer; 1979. [ Google Scholar ] [ Ref list ]
10. Broudy VC. Stem cell factor and hematopoiesis. Blood. 1997; 90 :1345–1364. [ PubMed ] [ Google Scholar ] [ Ref list ]
11. Vincent S, et al. Stage-specific expression of the Kit receptor and its ligand (KL) during male gametogenesis in the mouse: A Kit-KL interaction critical for meiosis. Development. 1998; 125 :4585–4593. [ PubMed ] [ Google Scholar ] [ Ref list ]
12. Ohta H, Yomogida K, Dohmae K, Nishimune Y. Regulation of proliferation and differentiation in spermatogonial stem cells: The role of c-kit and its ligand SCF. Development. 2000; 127 :2125–2131. [ PubMed ] [ Google Scholar ] [ Ref list ]
13. Heyworth CM, Whetton AD, Nicholls S, Zsebo K, Dexter TM. Stem cell factor directly stimulates the development of enriched granulocyte-macrophage colony-forming cells and promotes the effects of other colony-stimulating factors. Blood. 1992; 80 :2230–2236. [ PubMed ] [ Google Scholar ] [ Ref list ]
14. Lennartsson J, Shivakrupa R, Linnekin D. Synergistic growth of stem cell factor and granulocyte macrophage colony-stimulating factor involves kinase-dependent and -independent contributions from c-Kit. J Biol Chem. 2004; 279 :44544–44553. [ PubMed ] [ Google Scholar ] [ Ref list ]
15. Duarte RF, Franf DA. The synergy between stem cell factor (SCF) and granulocyte colony-stimulating factor (G-CSF): Molecular basis and clinical relevance. Leuk Lymphoma. 2002; 43 :1179–1187. [ PubMed ] [ Google Scholar ] [ Ref list ]
16. Pearson MA, et al. Investigation of the molecular mechanisms underlying growth factor synergy: The role of ERK 2 activation in synergy. Growth Factors. 1998; 15 :293–306. [ PubMed ] [ Google Scholar ] [ Ref list ]
17. Broudy VC, et al. Stem cell factor influences the proliferation and erythroid differentiation of the MB-02 human erythroleukemia cell line by binding to a high-affinity c-kit receptor. Blood. 1993; 82 :436–444. [ PubMed ] [ Google Scholar ] [ Ref list ]
18. Kokkinaki M, et al. The molecular signature of spermatogonial stem/progenitor cells in the 6-day-old mouse testis. Biol Reprod. 2009; 80 :707–717. [ PMC free article ] [ PubMed ] [ Google Scholar ] [ Ref list ]
19. Oatley JM, Oatley MJ, Avarbock MR, Tobias JW, Brinster RL. Colony stimulating factor 1 is an extrinsic stimulator of mouse spermatogonial stem cell self-renewal. Development. 2009; 136 :1191–1199. [ PMC free article ] [ PubMed ] [ Google Scholar ] [ Ref list ]
20. Ogawa T, Dobrinski I, Avarbock MR, Brinster RL. Transplantation of male germ line stem cells restores fertility in infertile mice. Nat Med. 2000; 6 :29–34. [ PMC free article ] [ PubMed ] [ Google Scholar ] [ Ref list ]
21. Kanatsu-Shinohara M, et al. Germline niche transplantation restores fertility in infertile mice. Hum Reprod. 2005; 20 :2376–2382. [ PubMed ] [ Google Scholar ] [ Ref list ]
22. Ikawa M, et al. Restoration of spermatogenesis by lentiviral gene transfer: Offspring from infertile mice. Proc Natl Acad Sci USA. 2002; 99 :7524–7529. [ PMC free article ] [ PubMed ] [ Google Scholar ] [ Ref list ]
23. Kanatsu-Shinohara M, et al. Adenovirus-mediated gene delivery and in vitro microinsemination produce offspring from infertile male mice. Proc Natl Acad Sci USA. 2002; 99 :1383–1388. [ PMC free article ] [ PubMed ] [ Google Scholar ] [ Ref list ]
24. Cohen PE, Chisholm O, Arceci RJ, Stanley ER, Pollard JW. Absence of colony-stimulating factor-1 in osteopetrotic (csfmop/csfmop) mice results in male fertility defects. Biol Reprod. 1996; 55 :310–317. [ PubMed ] [ Google Scholar ] [ Ref list ]
25. Krausz C. Male infertility: Pathogenesis and clinical diagnosis. Best Pract Res Clin Endocrinol Metab. 2011; 25 :271–285. [ PubMed ] [ Google Scholar ] [ Ref list ]
26. McLachlan RI, O’Bryan MK. Clinical Review#: State of the art for genetic testing of infertile men. J Clin Endocrinol Metab. 2010; 95 :1013–1024. [ PubMed ] [ Google Scholar ] [ Ref list ]

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a Department of Urology, Yokohama City University Graduate School of Medicine, Yokohama 236-0004, Japan;
a Department of Urology, Yokohama City University Graduate School of Medicine, Yokohama 236-0004, Japan;
a Department of Urology, Yokohama City University Graduate School of Medicine, Yokohama 236-0004, Japan;
a Department of Urology, Yokohama City University Graduate School of Medicine, Yokohama 236-0004, Japan;
a Department of Urology, Yokohama City University Graduate School of Medicine, Yokohama 236-0004, Japan;
b RIKEN, Bioresource Center, Ibaraki 305-0074, Japan;
b RIKEN, Bioresource Center, Ibaraki 305-0074, Japan;
b RIKEN, Bioresource Center, Ibaraki 305-0074, Japan;
c Division of Germ Cell Biology, National Institute for Basic Biology, National Institutes of Natural Sciences, Okazaki, 444-8787, Japan;
d Department of Basic Biology, School of Life Science, Graduate University for Advanced Studies (Sokendai), Okazaki, 444-8787, Japan;
a Department of Urology, Yokohama City University Graduate School of Medicine, Yokohama 236-0004, Japan;
e Department of Medical Life Science, Yokohama City University, Yokohama 236-0004, Japan; and
f Advanced Medical Research Center, Yokohama City University, Yokohama 236-0004, Japan
Author contributions: T.S., S.Y., and T.O. designed research; T.S., T.Y., M.K., K.K., S.M., N.O., and A.O. performed research; T.S., Y.K., and T.O. analyzed data; and T.S. and T.O. wrote the paper.
Male infertility is most commonly caused by spermatogenic defects or insufficiencies, the majority of which are as yet cureless. Recently, we succeeded in cultivating mouse testicular tissues for producing fertile sperm from spermatogonial stem cells. Here, we show that one of the most severe types of spermatogenic defect mutant can be treated by the culture method without any genetic manipulations. The Sl/Sl d mouse is used as a model of such male infertility. The testis of the Sl/Sl d mouse has only primitive spermatogonia as germ cells, lacking any sign of spermatogenesis owing to mutations of the c-kit ligand (KITL) gene that cause the loss of membrane-bound-type KITL from the surface of Sertoli cells. To compensate for the deficit, we cultured testis tissues of Sl/Sl d mice with a medium containing recombinant KITL and found that it induced the differentiation of spermatogonia up to the end of meiosis. We further discovered that colony stimulating factor-1 (CSF-1) enhances the effect of KITL and promotes spermatogenesis up to the production of sperm. Microinsemination of haploid cells resulted in delivery of healthy offspring. This study demonstrated that spermatogenic impairments can be treated in vitro with the supplementation of certain factors or substances that are insufficient in the original testes.
Spermatogenic impairments can be caused by malfunctions of either the germ cell itself or surrounding somatic cells, which collectively constitute the microenvironment for proper spermatogenesis. It is well known that the microenvironmental condition in the testis is under the body’s systemic control, particularly through hormones from the pituitary. It is also well recognized that testicular somatic cells, Sertoli cells in particular, play a pivotal role in spermatogenesis ( 1 , 2 ). Although it remains to be elucidated what molecules are essential constituents of that microenvironment and how they exert their role in spatial and temporal terms, it is a reasonable assumption that the spermatogenic impairments caused by microenvironmental factors are treatable by correcting the defect(s).
Recently, we succeeded in inducing complete spermatogenesis in mice using an organ culture method ( 3 – 5 ). In this culture system, germ cells developed from spermatogonial stem cells through mitotic differentiation of spermatogonia, meiosis in spermatocytes, and morphological transformation in haploid spermatids, to sperm. One of the greatest advantages of the in vitro system is that the culture medium can be modified freely to an extent that would be impossible to achieve in vivo. In the present study, we attempted to treat spermatogenic failure of a mutant mouse by culturing testis tissue fragments in media supplemented with combinations of growth factors.
For this experimental trial we chose the Steel ( Sl) mutant mouse, which has long been used to study spermatogenesis, hematopoiesis, and proliferation and differentiation of melanocytes. Sl mutants are caused by defects in Kitl and now comprise more than 40 kindred mutants (Mouse Genome Database, The Jackson Laboratory). The original Sl mutant lacks a wide range of genomic regions, including the entire Kitl along with eight other genes ( 6 ). Another well-known mutant named Sl d has a deletion in the domains of transmembrane and cytoplasmic Kitl . This partia
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