Generation of male differentiated germ cells from various types of stem cells.

Infertility is a major and largely incurable disease caused by disruption and loss of germ cells. It affects 10-15% of couples, and male factor accounts for half of the cases. To obtain human male germ cells 'especially functional spermatids' is essential for treating male infertility. Currently, much progress has been made on generating male germ cells, including spermatogonia, spermatocytes, and spermatids, from various types of stem cells. These germ cells can also be used in investigation of the pathology of male infertility. In this review, we focused on advances on obtaining male differentiated germ cells from different kinds of stem cells, with an emphasis on the embryonic stem (ES) cells, the induced pluripotent stem (iPS) cells, and spermatogonial stem cells (SSCs). We illustrated the generation of male differentiated germ cells from ES cells, iPS cells and SSCs, and we summarized the phenotype for these stem cells, spermatocytes and spermatids. Moreover, we address the differentiation potentials of ES cells, iPS cells and SSCs. We also highlight the advantages, disadvantages and concerns on derivation of the differentiated male germ cells from several types of stem cells. The ability of generating mature and functional male gametes from stem cells could enable us to understand the precise etiology of male infertility and offer an invaluable source of autologous male gametes for treating male infertility of azoospermia patients.

[1]  H. Okano,et al.  Differentiation Of Induced Pluripotent Stem Cells-Derived Neural Crest Cells Into Corneal Keratocytes In Vivo , 2013 .

[2]  Zuping He,et al.  In vitro and in vivo differentiation of induced pluripotent stem cells into male germ cells. , 2013, Biochemical and biophysical research communications.

[3]  M. van Wely,et al.  Parental attitudes toward fertility preservation in boys with cancer: context of different risk levels of infertility and success rates of fertility restoration. , 2013, Fertility and sterility.

[4]  S. Repping,et al.  Restoring Fertility in Sterile Childhood Cancer Survivors by Autotransplanting Spermatogonial Stem Cells: Are We There Yet? , 2013, BioMed research international.

[5]  Peng Li,et al.  Differentiation of Induced Pluripotent Stem Cells into Male Germ Cells In Vitro through Embryoid Body Formation and Retinoic Acid or Testosterone Induction , 2012, BioMed research international.

[6]  Karen A. Peters,et al.  Spermatogonial stem cell transplantation into rhesus testes regenerates spermatogenesis producing functional sperm. , 2012, Cell stem cell.

[7]  K. Jahnukainen,et al.  Clinical review: Present and future prospects of male fertility preservation for children and adolescents. , 2012, The Journal of clinical endocrinology and metabolism.

[8]  G. Schatten,et al.  Direct differentiation of human pluripotent stem cells into haploid spermatogenic cells. , 2012, Cell reports.

[9]  C. Simón,et al.  In vitro production of haploid cells after coculture of CD49f+ with Sertoli cells from testicular sperm extraction in nonobstructive azoospermic patients. , 2012, Fertility and sterility.

[10]  Zheng Li,et al.  Generation of male germ cells from induced pluripotent stem cells (iPS cells): an in vitro and in vivo study. , 2012, Asian journal of andrology.

[11]  X. Guo,et al.  Derivation of male germ cells from induced pluripotent stem cells in vitro and in reconstituted seminiferous tubules , 2012, Cell proliferation.

[12]  C. Simón,et al.  Divergent RNA‐binding Proteins, DAZL and VASA, Induce Meiotic Progression in Human Germ Cells Derived in Vitro , 2012, Stem Cells.

[13]  Eitan Lunenfeld,et al.  Differentiation of murine male germ cells to spermatozoa in a soft agar culture system. , 2012, Asian journal of andrology.

[14]  Takehiko Ogawa,et al.  In vitro production of fertile sperm from murine spermatogonial stem cell lines. , 2011, Nature communications.

[15]  H. Ohta,et al.  Reconstitution of the Mouse Germ Cell Specification Pathway in Culture by Pluripotent Stem Cells , 2011, Cell.

[16]  N. Montserrat,et al.  Complete Meiosis from Human Induced Pluripotent Stem Cells , 2011, Stem cells.

[17]  Haifan Lin,et al.  Pinpointing the expression of piRNAs and function of the PIWI protein subfamily during spermatogenesis in the mouse. , 2011, Developmental Biology.

[18]  J. Rao,et al.  Identification and characterization of repopulating spermatogonial stem cells from the adult human testis. , 2011, Human reproduction.

[19]  N. Ogonuki,et al.  In vitro production of functional sperm in cultured neonatal mouse testes , 2011, Nature.

[20]  C. Simón,et al.  Human germ cell differentiation from fetal- and adult-derived induced pluripotent stem cells , 2010, Human molecular genetics.

[21]  M. Matzuk,et al.  Mendelian genetics of male infertility , 2010, Annals of the New York Academy of Sciences.

[22]  S. Yamanaka,et al.  Induction of primordial germ cells from mouse induced pluripotent stem cells derived from adult hepatocytes , 2010, Molecular reproduction and development.

[23]  Y. Hosoi,et al.  Leukemia inhibitory factor (LIF) enhances germ cell differentiation from primate embryonic stem cells. , 2010, Cellular Reprogramming.

[24]  A. Shelling Premature ovarian failure. , 2010, Reproduction.

[25]  P. Froment,et al.  An engineered 3D blood-testis barrier model for the assessment of reproductive toxicity potential. , 2010, Biomaterials.

[26]  Zuping He,et al.  Isolation, Characterization, and Culture of Human Spermatogonia1 , 2010, Biology of reproduction.

[27]  Krishanu Saha,et al.  Technical challenges in using human induced pluripotent stem cells to model disease. , 2009, Cell stem cell.

[28]  A. Fazeli,et al.  In vitro post-meiotic germ cell development from human embryonic stem cells. , 2009, Human reproduction.

[29]  H. N. Nguyen,et al.  Human DAZL, DAZ and BOULE genes modulate primordial germ cell and haploid gamete formation , 2009, Nature.

[30]  M. Simoni,et al.  New horizons for in vitro spermatogenesis? An update on novel three-dimensional culture systems as tools for meiotic and post-meiotic differentiation of testicular germ cells. , 2009, Molecular human reproduction.

[31]  Shaorong Gao,et al.  iPS cells can support full-term development of tetraploid blastocyst-complemented embryos. , 2009, Cell stem cell.

[32]  L. Zoloth,et al.  iPS cells can support full-term development of tetraploid blastocyst-complemented embryos, by L Kang, J Wang, Y Zhang, Z Kou, S Gao: Cell Stem Cell , 2009 .

[33]  Prashant Mali,et al.  Gene targeting of a disease-related gene in human induced pluripotent stem and embryonic stem cells. , 2009, Cell stem cell.

[34]  N. Nakatsuji,et al.  In Vitro Germ Cell Differentiation from Cynomolgus Monkey Embryonic Stem Cells , 2009, PloS one.

[35]  Wei Wang,et al.  piggyBac transposition reprograms fibroblasts to induced pluripotent stem cells , 2009, Nature.

[36]  K. Plath,et al.  Derivation of Primordial Germ Cells from Human Embryonic and Induced Pluripotent Stem Cells Is Significantly Improved by Coculture with Human Fetal Gonadal Cells , 2009, Stem cells.

[37]  Jiji Jiang,et al.  Pluripotent stem cells derived from adult human testes. , 2009, Stem cells and development.

[38]  Zuping He,et al.  Spermatogonial stem cells: mouse and human comparisons. , 2009, Birth defects research. Part C, Embryo today : reviews.

[39]  A. Hayek,et al.  A Novel Approach for the Derivation of Putative Primordial Germ Cells and Sertoli Cells from Human Embryonic Stem Cells , 2009, Stem cells.

[40]  R. Reijo-Pera,et al.  Isolation and Characterization of Pluripotent Human Spermatogonial Stem Cell-Derived Cells , 2009, Stem cells.

[41]  Meng Liu,et al.  Generation of induced pluripotent stem cells from adult rhesus monkey fibroblasts. , 2008, Cell stem cell.

[42]  M. Stojkovic,et al.  Isolation of Primordial Germ Cells from Differentiating Human Embryonic Stem Cells , 2008, Stem cells.

[43]  S. Stice,et al.  Enrichment and Differentiation of Human Germ‐Like Cells Mediated by Feeder Cells and Basic Fibroblast Growth Factor Signaling , 2008, Stem cells.

[44]  A. Consiglio,et al.  Efficient and rapid generation of induced pluripotent stem cells from human keratinocytes , 2008, Nature Biotechnology.

[45]  George Q. Daley,et al.  Disease-Specific Induced Pluripotent Stem Cells , 2008, Cell.

[46]  Hynek Wichterle,et al.  Induced Pluripotent Stem Cells Generated from Patients with ALS Can Be Differentiated into Motor Neurons , 2008, Science.

[47]  J. Thomson,et al.  Pluripotent stem cell lines. , 2008, Genes & development.

[48]  P. Mali,et al.  Improved Efficiency and Pace of Generating Induced Pluripotent Stem Cells from Human Adult and Fetal Fibroblasts , 2008, Stem cells.

[49]  Shinya Yamanaka,et al.  Pluripotency and nuclear reprogramming , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[50]  I. Kerkis,et al.  In vitro differentiation of male mouse embryonic stem cells into both presumptive sperm cells and oocytes. , 2007, Cloning and stem cells.

[51]  Shulan Tian,et al.  Induced Pluripotent Stem Cell Lines Derived from Human Somatic Cells , 2007, Science.

[52]  J. Dadoune Generation of functional multipotent adult stem cells from GPR125 + germline progenitors. , 2007 .

[53]  S. Rafii,et al.  Generation of functional multipotent adult stem cells from GPR125+ germline progenitors. , 2007, Nature.

[54]  T. Ichisaka,et al.  Generation of germline-competent induced pluripotent stem cells , 2007, Nature.

[55]  A. Iritani,et al.  Primate embryonic stem cells proceed to early gametogenesis in vitro. , 2007, Cloning and stem cells.

[56]  S. Yamanaka Strategies and new developments in the generation of patient-specific pluripotent stem cells. , 2007, Cell stem cell.

[57]  Jae-Ho Lee,et al.  In vitro differentiation of germ cells from nonobstructive azoospermic patients using three-dimensional culture in a collagen gel matrix. , 2007, Fertility and sterility.

[58]  C. Shun,et al.  Derivation, characterization and differentiation of human embryonic stem cells: comparing serum-containing versus serum-free media and evidence of germ cell differentiation. , 2007, Human reproduction.

[59]  A. Clark,et al.  Bone morphogenetic proteins induce germ cell differentiation from human embryonic stem cells. , 2006, Stem cells and development.

[60]  G. Daley,et al.  In vitro generation of germ cells from murine embryonic stem cells , 2006, Nature Protocols.

[61]  S. Yamanaka,et al.  Induction of Pluripotent Stem Cells from Mouse Embryonic and Adult Fibroblast Cultures by Defined Factors , 2006, Cell.

[62]  S. Knuutila,et al.  Distinct differentiation characteristics of individual human embryonic stem cell lines , 2006, BMC Developmental Biology.

[63]  T. Haaf,et al.  In vitro-differentiated embryonic stem cells give rise to male gametes that can generate offspring mice. , 2006, Developmental cell.

[64]  D. D. de Rooij,et al.  Rapid expansion of the spermatogonial stem cell tool box. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[65]  Myung Chan Gye,et al.  In vitro spermatogenesis by three-dimensional culture of rat testicular cells in collagen gel matrix. , 2006, Biomaterials.

[66]  Eric Johnson,et al.  Immortalization of Mouse Germ Line Stem Cells , 2005, Stem cells.

[67]  A. Clark,et al.  Spontaneous differentiation of germ cells from human embryonic stem cells in vitro. , 2004, Human molecular genetics.

[68]  George Q. Daley,et al.  Derivation of embryonic germ cells and male gametes from embryonic stem cells , 2004, Nature.

[69]  A. Honaramooz,et al.  Fertility and Germline Transmission of Donor Haplotype Following Germ Cell Transplantation in Immunocompetent Goats1 , 2003, Biology of reproduction.

[70]  N. Tsunekawa,et al.  Embryonic stem cells can form germ cells in vitro , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[71]  R. Brinster,et al.  Spermatogonial stem cells share some, but not all, phenotypic and functional characteristics with other stem cells , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[72]  W. Ryder,et al.  Semen cryopreservation, utilisation and reproductive outcome in men treated for Hodgkin's disease , 2002, British Journal of Cancer.

[73]  R. Brinster Germline Stem Cell Transplantation and Transgenesis , 2002, Science.

[74]  Yali Chen,et al.  Generation and in Vitro Differentiation of a Spermatogonial Cell Line , 2002, Science.

[75]  C. Staub A century of research on mammalian male germ cell meiotic differentiation in vitro. , 2001, Journal of andrology.

[76]  Hiroshi Kusunoki,et al.  Completion of meiosis in human primary spermatocytes through in vitro coculture with Vero cells. , 2001, Fertility and sterility.

[77]  C. Staub,et al.  The whole meiotic process can occur in vitro in untransformed rat spermatogenic cells. , 2000, Experimental cell research.

[78]  H. Baker,et al.  Infertility in men: recent advances and continuing controversies. , 1999, The Journal of clinical endocrinology and metabolism.

[79]  T. Shinohara,et al.  β1- and α6-integrin are surface markers on mouse spermatogonial stem cells , 1999 .

[80]  J. Thomson,et al.  Embryonic stem cell lines derived from human blastocysts. , 1998, Science.

[81]  C. Staub,et al.  Meiotic differentiation of germinal cells in three-week cultures of whole cell population from rat seminiferous tubules. , 1998, Biology of reproduction.

[82]  D. G. Rooij,et al.  Stem Cells in the Testis , 1998, International journal of experimental pathology.

[83]  R. Brinster,et al.  Spermatogenesis following male germ-cell transplantation. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[84]  S. Takahara,et al.  Clinical study of azoospermia. , 1994, International journal of andrology.

[85]  A. Kierszenbaum Mammalian spermatogenesis in vivo and in vitro: a partnership of spermatogenic and somatic cell lineages. , 1994, Endocrine reviews.

[86]  D. G. Rooij,et al.  A quantitative study of spermatogonial multiplication and stem cell renewal in the C3H/101 F1 hybrid mouse , 1993 .

[87]  E. Balbinder Multiple pathways of deletion formation in Escherichia coli. , 1993, Mutation research.

[88]  A. Bradley,et al.  Formation of germ-line chimaeras from embryo-derived teratocarcinoma cell lines , 1984, Nature.

[89]  G. Martin,et al.  Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[90]  HighWire Press Philosophical Transactions of the Royal Society of London , 1781, The London Medical Journal.

[91]  Seon-Woo Lee,et al.  Isolation and Characterization , 2016 .

[92]  F. Tomita,et al.  ISOLATION AND CHARACTERIZATION OF FLAVONOID COMPOUND FROM FERONIA LIMONIA , 2015 .

[93]  F. Abolhasani,et al.  Co-culture of spermatogonial stem cells with sertoli cells in the presence of testosterone and FSH improved differentiation via up-regulation of post meiotic genes. , 2013, Acta medica Iranica.

[94]  T. D. de Reijke,et al.  Embryonic stem cell-like cells derived from adult human testis. , 2010, Human reproduction.

[95]  M. Bonin,et al.  Generation of pluripotent stem cells from adult human testis , 2009, Nature.

[96]  Takashi Aoi,et al.  Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts , 2008, Nature Biotechnology.

[97]  V. Gatta,et al.  Male infertility: role of genetic background. , 2007, Reproductive biomedicine online.

[98]  T. Ichisaka,et al.  GENERATION OF GERMLINECOMPETENT INDUCED PLURIPOTENT STEM CELLS , 2007 .

[99]  R. Brinster,et al.  Spermatogonial stem cells. , 2006, Methods in enzymology.

[100]  S. Toyokuni,et al.  CD9 Is a Surface Marker on Mouse and Rat Male Germline Stem Cells1 , 2004, Biology of reproduction.

[101]  M. Sousa,et al.  Developmental potential of human spermatogenic cells co-cultured with Sertoli cells. , 2002, Human reproduction.

[102]  D. D. de Rooij,et al.  A quantitative study of spermatogonial multiplication and stem cell renewal in the C3H/101 F1 hybrid mouse. , 1993, Mutation research.

[103]  Y. Clermont Kinetics of spermatogenesis in mammals: seminiferous epithelium cycle and spermatogonial renewal. , 1972, Physiological reviews.