1932

Abstract

Stem cells are necessary for the maintenance of many adult tissues. Signals within the stem cell microenvironment, or niche, regulate the self-renewal and differentiation capability of these cells. Misregulation of these signals through mutation or damage can lead to overgrowth or depletion of different stem cell pools. In this review, we focus on the testis and ovary, both of which contain well-defined niches, as well as the mouse testis, which has become a more approachable stem cell system with recent technical advances. We discuss the signals that regulate gonadal stem cells in their niches, how these signals mediate self-renewal and differentiation under homeostatic conditions, and how stress, whether from mutations or damage, can cause changes in cell fate and drive stem cell competition.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-cellbio-100913-013344
2015-11-13
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/cellbio/31/1/annurev-cellbio-100913-013344.html?itemId=/content/journals/10.1146/annurev-cellbio-100913-013344&mimeType=html&fmt=ahah

Literature Cited

  1. Aloisio GM, Nakada Y, Saatcioglu HD, Pena CG, Baker MD. et al. 2014. PAX7 expression defines germline stem cells in the adult testis. J. Clin. Investig. 124:3929–44 [Google Scholar]
  2. Amoyel M, Sanny J, Burel M, Bach EA. 2013. Hedgehog is required for CySC self-renewal but does not contribute to the GSC niche in the Drosophila testis. Development 140:56–65 [Google Scholar]
  3. Amoyel M, Simons BD, Bach EA. 2014. Neutral competition of stem cells is skewed by proliferative changes downstream of Hh and Hpo. EMBO J. 33:2295–313 [Google Scholar]
  4. Baker AM, Cereser B, Melton S, Fletcher AG, Rodriguez-Justo M. et al. 2014. Quantification of crypt and stem cell evolution in the normal and neoplastic human colon. Cell Rep. 8:940–47 [Google Scholar]
  5. Barroca V, Lassalle B, Coureuil M, Louis JP, Le Page F. et al. 2009. Mouse differentiating spermatogonia can generate germinal stem cells in vivo. Nat. Cell Biol. 11:190–96 [Google Scholar]
  6. Bondar T, Medzhitov R. 2010. p53-mediated hematopoietic stem and progenitor cell competition. Cell Stem Cell 6:309–22 [Google Scholar]
  7. Brawley C, Matunis E. 2004. Regeneration of male germline stem cells by spermatogonial dedifferentiation in vivo. Science 304:1331–34 [Google Scholar]
  8. Buaas FW, Kirsh AL, Sharma M, McLean DJ, Morris JL. et al. 2004. Plzf is required in adult male germ cells for stem cell self-renewal. Nat. Genet. 36:647–52 [Google Scholar]
  9. Castanieto A, Johnston MJ, Nystul TG. 2014. EGFR signaling promotes self-renewal through the establishment of cell polarity in Drosophila follicle stem cells. eLife 3:e04437 [Google Scholar]
  10. Chan ST. 1970. Natural sex reversal in vertebrates. Philos. Trans. R. Soc. B 259:59–71 [Google Scholar]
  11. Chen D, McKearin D. 2003. Dpp signaling silences bam transcription directly to establish asymmetric divisions of germline stem cells. Curr. Biol. 13:1786–91 [Google Scholar]
  12. Chen S, Lewallen M, Xie T. 2013. Adhesion in the stem cell niche: biological roles and regulation. Development 140:255–65 [Google Scholar]
  13. Cheng J, Turkel N, Hemati N, Fuller MT, Hunt AJ, Yamashita YM. 2008. Centrosome misorientation reduces stem cell division during ageing. Nature 456:599–604 [Google Scholar]
  14. Clayton E, Doupe DP, Klein AM, Winton DJ, Simons BD, Jones PH. 2007. A single type of progenitor cell maintains normal epidermis. Nature 446:185–89 [Google Scholar]
  15. Costoya JA, Hobbs RM, Barna M, Cattoretti G, Manova K. et al. 2004. Essential role of Plzf in maintenance of spermatogonial stem cells. Nat. Genet. 36:653–59 [Google Scholar]
  16. de Cuevas M, Matunis EL. 2011. The stem cell niche: lessons from the Drosophila testis. Development 138:2861–69 [Google Scholar]
  17. de la Cova C, Abril M, Bellosta P, Gallant P, Johnston LA. 2004. Drosophila Myc regulates organ size by inducing cell competition. Cell 117:107–16 [Google Scholar]
  18. de Navascués J, Perdigoto CN, Bian Y, Schneider MH, Bardin AJ. et al. 2012. Drosophila midgut homeostasis involves neutral competition between symmetrically dividing intestinal stem cells. EMBO J. 31:2473–85 [Google Scholar]
  19. Dinardo S, Okegbe T, Wingert L, Freilich S, Terry N. 2011. lines and bowl affect the specification of cyst stem cells and niche cells in the Drosophila testis. Development 138:1687–96 [Google Scholar]
  20. Doupe DP, Alcolea MP, Roshan A, Zhang G, Klein AM. et al. 2012. A single progenitor population switches behavior to maintain and repair esophageal epithelium. Science 337:1091–93 [Google Scholar]
  21. Doupe DP, Klein AM, Simons BD, Jones PH. 2010. The ordered architecture of murine ear epidermis is maintained by progenitor cells with random fate. Dev. Cell 18:317–23 [Google Scholar]
  22. Eliazer S, Buszczak M. 2011. Finding a niche: studies from the Drosophila ovary. Stem Cell Res. Ther. 2:45 [Google Scholar]
  23. Eun SH, Shi Z, Cui K, Zhao K, Chen X. 2014. A non-cell autonomous role of E(z) to prevent germ cells from turning on a somatic cell marker. Science 343:1513–16 [Google Scholar]
  24. Fichelson P, Moch C, Ivanovitch K, Martin C, Sidor CM. et al. 2009. Live-imaging of single stem cells within their niche reveals that a U3snoRNP component segregates asymmetrically and is required for self-renewal in Drosophila. Nat. Cell Biol. 11:685–93 [Google Scholar]
  25. Flaherty MS, Salis P, Evans CJ, Ekas LA, Marouf A. et al. 2010. chinmo is a functional effector of the JAK/STAT pathway that regulates eye development, tumor formation, and stem cell self-renewal in Drosophila. Dev. Cell 18:556–68 [Google Scholar]
  26. Foley K, Cooley L. 1998. Apoptosis in late stage Drosophila nurse cells does not require genes within the H99 deficiency. Development 125:1075–82 [Google Scholar]
  27. Forbes AJ, Lin H, Ingham PW, Spradling AC. 1996. hedgehog is required for the proliferation and specification of ovarian somatic cells prior to egg chamber formation in Drosophila. Development 122:1125–35 [Google Scholar]
  28. Fox DT, Morris LX, Nystul T, Spradling AC. 2009. Lineage analysis of stem cells. StemBook The Stem Cell Research Community Cambridge, MA: Harvard Stem Cell Inst. [Google Scholar]
  29. Fuller MT. 1993. Spermatogenesis. The Development of Drosophila melanogaster 1 M Bate, A Martinez Arias 71–147 Cold Spring Harbor, NY: Cold Spring Harb. Lab. Press [Google Scholar]
  30. Gönczy P, DiNardo S. 1996. The germ line regulates somatic cyst cell proliferation and fate during Drosophila spermatogenesis. Development 122:2437–47 [Google Scholar]
  31. Goriely A, Wilkie AO. 2012. Paternal age effect mutations and selfish spermatogonial selection: causes and consequences for human disease. Am. J. Hum. Genet. 90:175–200 [Google Scholar]
  32. Grisanti L, Falciatori I, Grasso M, Dovere L, Fera S. et al. 2009. Identification of spermatogonial stem cell subsets by morphological analysis and prospective isolation. Stem Cells 27:3043–52 [Google Scholar]
  33. Hanna CB, Hennebold JD. 2014. Ovarian germline stem cells: an unlimited source of oocytes?. Fertil. Steril. 101:20–30 [Google Scholar]
  34. Hara K, Nakagawa T, Enomoto H, Suzuki M, Yamamoto M. et al. 2014. Mouse spermatogenic stem cells continually interconvert between equipotent singly isolated and syncytial states. Cell Stem Cell 14:658–72 [Google Scholar]
  35. Hardy RW, Tokuyasu KT, Lindsley DL, Garavito M. 1979. The germinal proliferation center in the testis of Drosophila melanogaster. J. Ultrastruct. Res. 69:180–90 [Google Scholar]
  36. Hartman TR, Zinshteyn D, Schofield HK, Nicolas E, Okada A, O'Reilly AM. 2010. Drosophila Boi limits Hedgehog levels to suppress follicle stem cell proliferation. J. Cell Biol. 191:943–52 [Google Scholar]
  37. Hasegawa K, Namekawa SH, Saga Y. 2013. MEK/ERK signaling directly and indirectly contributes to the cyclical self-renewal of spermatogonial stem cells. Stem Cells 31:2517–27 [Google Scholar]
  38. Hasegawa K, Saga Y. 2012. Retinoic acid signaling in Sertoli cells regulates organization of the blood-testis barrier through cyclical changes in gene expression. Development 139:4347–55 [Google Scholar]
  39. Hermann BP, Sukhwani M, Hansel MC, Orwig KE. 2010. Spermatogonial stem cells in higher primates: are there differences from those in rodents?. Reproduction 139:479–93 [Google Scholar]
  40. Hétié P, de Cuevas M, Matunis E. 2014. Conversion of quiescent niche cells to somatic stem cells causes ectopic niche formation in the Drosophila testis. Cell Rep. 7:715–21 [Google Scholar]
  41. Hudson AG, Parrott BB, Qian Y, Schulz C. 2013. A temporal signature of epidermal growth factor signaling regulates the differentiation of germline cells in testes of Drosophila melanogaster. PLOS ONE 8:e70678 [Google Scholar]
  42. Inaba M, Yuan H, Yamashita YM. 2011. String (Cdc25) regulates stem cell maintenance, proliferation and aging in Drosophila testis. Development 138:5079–86 [Google Scholar]
  43. Ishii K, Kanatsu-Shinohara M, Toyokuni S, Shinohara T. 2012. FGF2 mediates mouse spermatogonial stem cell self-renewal via upregulation of Etv5 and Bcl6b through MAP2K1 activation. Development 139:1734–43 [Google Scholar]
  44. Issigonis M, Tulina N, de Cuevas M, Brawley C, Sandler L, Matunis E. 2009. JAK-STAT signal inhibition regulates competition in the Drosophila testis stem cell niche. Science 326:153–56 [Google Scholar]
  45. Jin Z, Kirilly D, Weng C, Kawase E, Song X. et al. 2008. Differentiation-defective stem cells outcompete normal stem cells for niche occupancy in the Drosophila ovary. Cell Stem Cell 2:39–49 [Google Scholar]
  46. Johnston LA. 2009. Competitive interactions between cells: death, growth, and geography. Science 324:1679–82 [Google Scholar]
  47. Kai T, Spradling A. 2004. Differentiating germ cells can revert into functional stem cells in Drosophila melanogaster ovaries. Nature 428:564–69 [Google Scholar]
  48. Kanatsu-Shinohara M, Shinohara T. 2013. Spermatogonial stem cell self-renewal and development. Annu. Rev. Cell Dev. Biol. 29:163–87 [Google Scholar]
  49. Kanatsu-Shinohara M, Takehashi M, Takashima S, Lee J, Morimoto H. et al. 2008. Homing of mouse spermatogonial stem cells to germline niche depends on β1-integrin. Cell Stem Cell 3:533–42 [Google Scholar]
  50. Kawase E, Wong MD, Ding BC, Xie T. 2004. Gbb/Bmp signaling is essential for maintaining germline stem cells and for repressing bam transcription in the Drosophila testis. Development 131:1365–75 [Google Scholar]
  51. Kiger AA, Jones DL, Schulz C, Rogers MB, Fuller MT. 2001. Stem cell self-renewal specified by JAK-STAT activation in response to a support cell cue. Science 294:2542–45 [Google Scholar]
  52. Kiger AA, White-Cooper H, Fuller MT. 2000. Somatic support cells restrict germline stem cell self-renewal and promote differentiation. Nature 407:750–54 [Google Scholar]
  53. King RC. 1970. Ovarian Development in Drosophila melanogaster. New York: Academic [Google Scholar]
  54. King RS, Newmark PA. 2012. The cell biology of regeneration. J. Cell Biol. 196:553–62 [Google Scholar]
  55. Kirilly D, Spana EP, Perrimon N, Padgett RW, Xie T. 2005. BMP signaling is required for controlling somatic stem cell self-renewal in the Drosophila ovary. Dev. Cell 9:651–62 [Google Scholar]
  56. Klein AM, Nakagawa T, Ichikawa R, Yoshida S, Simons BD. 2010. Mouse germ line stem cells undergo rapid and stochastic turnover. Cell Stem Cell 7:214–24 [Google Scholar]
  57. Klein AM, Simons BD. 2011. Universal patterns of stem cell fate in cycling adult tissues. Development 138:3103–11 [Google Scholar]
  58. Kronen MR, Schoenfelder KP, Klein AM, Nystul TG. 2014. Basolateral junction proteins regulate competition for the follicle stem cell niche in the Drosophila ovary. PLOS ONE 9:e101085 [Google Scholar]
  59. Kubota H, Avarbock MR, Brinster RL. 2004. Growth factors essential for self-renewal and expansion of mouse spermatogonial stem cells. PNAS 101:16489–94 [Google Scholar]
  60. Lacerda SM, Costa GM, de Franca LR. 2014. Biology and identity of fish spermatogonial stem cell. Gen. Comp. Endocrinol. 207:56–65 [Google Scholar]
  61. Leatherman JL, Dinardo S. 2008. Zfh-1 controls somatic stem cell self-renewal in the Drosophila testis and nonautonomously influences germline stem cell self-renewal. Cell Stem Cell 3:44–54 [Google Scholar]
  62. Leatherman JL, Dinardo S. 2010. Germline self-renewal requires cyst stem cells, while stat regulates niche adhesion in Drosophila testes. Nat. Cell Biol. 12:806–11 [Google Scholar]
  63. Lee S, Zhou L, Kim J, Kalbfleisch S, Schock F. 2008. Lasp anchors the Drosophila male stem cell niche and mediates spermatid individualization. Mech. Dev. 125:768–76 [Google Scholar]
  64. Lei L, Spradling AC. 2013. Female mice lack adult germ-line stem cells but sustain oogenesis using stable primordial follicles. PNAS 110:8585–90 [Google Scholar]
  65. Li Y, Minor NT, Park JK, McKearin DM, Maines JZ. 2009. Bam and Bgcn antagonize Nanos-dependent germ-line stem cell maintenance. PNAS 106:9304–9 [Google Scholar]
  66. Lim JG, Fuller MT. 2012. Somatic cell lineage is required for differentiation and not maintenance of germline stem cells in Drosophila testes. PNAS 109:18477–81 [Google Scholar]
  67. Lopez-Garcia C, Klein AM, Simons BD, Winton DJ. 2010. Intestinal stem cell replacement follows a pattern of neutral drift. Science 330:822–25 [Google Scholar]
  68. Lopez-Onieva L, Fernandez-Minan A, Gonzalez-Reyes A. 2008. Jak/Stat signalling in niche support cells regulates dpp transcription to control germline stem cell maintenance in the Drosophila ovary. Development 135:533–40 [Google Scholar]
  69. Losick R, Desplan C. 2008. Stochasticity and cell fate. Science 320:65–68 [Google Scholar]
  70. Luo J, Megee S, Dobrinski I. 2009. Asymmetric distribution of UCH-L1 in spermatogonia is associated with maintenance and differentiation of spermatogonial stem cells. J. Cell. Physiol. 220:460–68 [Google Scholar]
  71. Ma Q, Wawersik M, Matunis EL. 2014. The Jak-STAT target Chinmo prevents sex transformation of adult stem cells in the Drosophila testis niche. Dev. Cell 31:474–86 [Google Scholar]
  72. Martin LA, Assif N, Gilbert M, Wijewarnasuriya D, Seandel M. 2014. Enhanced fitness of adult spermatogonial stem cells bearing a paternal age-associated FGFR2 mutation. Stem Cell Rep. 3:219–26 [Google Scholar]
  73. Masuyama H, Yamada M, Kamei Y, Fujiwara-Ishikawa T, Todo T. et al. 2012. Dmrt1 mutation causes a male-to-female sex reversal after the sex determination by Dmy in the medaka. Chromosome Res. 20:163–76 [Google Scholar]
  74. Matson CK, Murphy MW, Sarver AL, Griswold MD, Bardwell VJ, Zarkower D. 2011. DMRT1 prevents female reprogramming in the postnatal mammalian testis. Nature 476:101–4 [Google Scholar]
  75. Matunis E, Tran J, Gonczy P, Caldwell K, DiNardo S. 1997. punt and schnurri regulate a somatically derived signal that restricts proliferation of committed progenitors in the germline. Development 124:4383–91 [Google Scholar]
  76. Matunis EL, Stine RR, de Cuevas M. 2012. Recent advances in Drosophila male germline stem cell biology. Spermatogenesis 2:137–44 [Google Scholar]
  77. McCall K, Steller H. 1998. Requirement for DCP-1 caspase during Drosophila oogenesis. Science 279:230–34 [Google Scholar]
  78. Meng X, Lindahl M, Hyvonen ME, Parvinen M, de Rooij DG. et al. 2000. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science 287:1489–93 [Google Scholar]
  79. Michel M, Kupinski AP, Raabe I, Bokel C. 2012. Hh signalling is essential for somatic stem cell maintenance in the Drosophila testis niche. Development 139:2663–69 [Google Scholar]
  80. Michel M, Raabe I, Kupinski AP, Perez-Palencia R, Bokel C. 2011. Local BMP receptor activation at adherens junctions in the Drosophila germline stem cell niche. Nat. Commun. 2:415 [Google Scholar]
  81. Morris LX, Spradling AC. 2011. Long-term live imaging provides new insight into stem cell regulation and germline-soma coordination in the Drosophila ovary. Development 138:2207–15 [Google Scholar]
  82. Morrissey ER, Vermeulen L. 2014. Stem cell competition: how speeding mutants beat the rest. EMBO J. 33:2277–78 [Google Scholar]
  83. Mullaney BP, Skinner MK. 1992. Basic fibroblast growth factor (bFGF) gene expression and protein production during pubertal development of the seminiferous tubule: follicle-stimulating hormone-induced Sertoli cell bFGF expression. Endocrinology 131:2928–34 [Google Scholar]
  84. Nakagawa T, Nabeshima Y, Yoshida S. 2007. Functional identification of the actual and potential stem cell compartments in mouse spermatogenesis. Dev. Cell 12:195–206 [Google Scholar]
  85. Naughton CK, Jain S, Strickland AM, Gupta A, Milbrandt J. 2006. Glial cell-line derived neurotrophic factor-mediated RET signaling regulates spermatogonial stem cell fate. Biol. Reprod. 74:314–21 [Google Scholar]
  86. Noll JE, Williams SA, Purton LE, Zannettino AC. 2012. Tug of war in the haematopoietic stem cell niche: do myeloma plasma cells compete for the HSC niche?. Blood Cancer J. 2:e91 [Google Scholar]
  87. Oatley JM, Avarbock MR, Telaranta AI, Fearon DT, Brinster RL. 2006. Identifying genes important for spermatogonial stem cell self-renewal and survival. PNAS 103:9524–29 [Google Scholar]
  88. Oatley JM, Brinster RL. 2012. The germline stem cell niche unit in mammalian testes. Physiol. Rev. 92:577–95 [Google Scholar]
  89. Oatley JM, Oatley MJ, Avarbock MR, Tobias JW, Brinster RL. 2009. Colony stimulating factor 1 is an extrinsic stimulator of mouse spermatogonial stem cell self-renewal. Development 136:1191–99 [Google Scholar]
  90. Patel T, Tursun B, Rahe DP, Hobert O. 2012. Removal of Polycomb repressive complex 2 makes C. elegans germ cells susceptible to direct conversion into specific somatic cell types. Cell Rep. 2:1178–86 [Google Scholar]
  91. Resende LP, Boyle M, Tran D, Fellner T, Jones DL. 2013. Headcase promotes cell survival and niche maintenance in the Drosophila testis. PLOS ONE 8:e68026 [Google Scholar]
  92. Rhiner C, Diaz B, Portela M, Poyatos JF, Fernandez-Ruiz I. et al. 2009. Persistent competition among stem cells and their daughters in the Drosophila ovary germline niche. Development 136:995–1006 [Google Scholar]
  93. Riparbelli MG, Callaini G. 2011. Male gametogenesis without centrioles. Dev. Biol. 349:427–39 [Google Scholar]
  94. Russell LD. 1978. The blood-testis barrier and its formation relative to spermatocyte maturation in the adult rat: a lanthanum tracer study. Anat. Rec. 190:99–111 [Google Scholar]
  95. Ryu BY, Orwig KE, Oatley JM, Avarbock MR, Brinster RL. 2006. Effects of aging and niche microenvironment on spermatogonial stem cell self-renewal. Stem Cells 24:1505–11 [Google Scholar]
  96. Sahai-Hernandez P, Castanieto A, Nystul TG. 2012. Drosophila models of epithelial stem cells and their niches. Wiley Interdiscip. Rev. Dev. Biol. 1:447–57 [Google Scholar]
  97. Salzmann V, Inaba M, Cheng J, Yamashita YM. 2013. Lineage tracing quantification reveals symmetric stem cell division in Drosophila male germline stem cells. Cell. Mol. Bioeng. 6:441–48 [Google Scholar]
  98. Sánchez Alvarado A, Yamanaka S. 2014. Rethinking differentiation: stem cells, regeneration, and plasticity. Cell 157:110–19 [Google Scholar]
  99. Schulz C, Wood CG, Jones DL, Tazuke SI, Fuller MT. 2002. Signaling from germ cells mediated by the rhomboid homolog stet organizes encapsulation by somatic support cells. Development 129:4523–34 [Google Scholar]
  100. Sheng XR, Brawley CM, Matunis EL. 2009. Dedifferentiating spermatogonia outcompete somatic stem cells for niche occupancy in the Drosophila testis. Cell Stem Cell 5:191–203 [Google Scholar]
  101. Sheng XR, Matunis E. 2011. Live imaging of the Drosophila spermatogonial stem cell niche reveals novel mechanisms regulating germline stem cell output. Development 138:3367–76 [Google Scholar]
  102. Shinohara T, Avarbock MR, Brinster RL. 1999. β1- and α6-integrin are surface markers on mouse spermatogonial stem cells. PNAS 96:5504–9 [Google Scholar]
  103. Simon L, Ekman GC, Tyagi G, Hess RA, Murphy KM, Cooke PS. 2007. Common and distinct factors regulate expression of mRNA for ETV5 and GDNF, Sertoli cell proteins essential for spermatogonial stem cell maintenance. Exp. Cell Res. 313:3090–99 [Google Scholar]
  104. Singh SR, Zheng Z, Wang H, Oh SW, Chen X, Hou SX. 2010. Competitiveness for the niche and mutual dependence of the germline and somatic stem cells in the Drosophila testis are regulated by the JAK/STAT signaling. J. Cell. Physiol. 223:500–10 [Google Scholar]
  105. Slaidina M, Lehmann R. 2014. Translational control in germline stem cell development. J. Cell Biol. 207:13–21 [Google Scholar]
  106. Smith-Berdan S, Nguyen A, Hassanein D, Zimmer M, Ugarte F. et al. 2011. Robo4 cooperates with CXCR4 to specify hematopoietic stem cell localization to bone marrow niches. Cell Stem Cell 8:72–83 [Google Scholar]
  107. Snippert HJ, van der Flier LG, Sato T, van Es JH, van den Born M. et al. 2010. Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 143:134–44 [Google Scholar]
  108. Song X, Wong MD, Kawase E, Xi R, Ding BC. et al. 2004. Bmp signals from niche cells directly repress transcription of a differentiation-promoting gene, bag of marbles, in germline stem cells in the Drosophila ovary. Development 131:1353–64 [Google Scholar]
  109. Song X, Xie T. 2002. DE-cadherin-mediated cell adhesion is essential for maintaining somatic stem cells in the Drosophila ovary. PNAS 99:14813–18 [Google Scholar]
  110. Song X, Xie T. 2003. Wingless signaling regulates the maintenance of ovarian somatic stem cells in Drosophila. Development 130:3259–68 [Google Scholar]
  111. Song X, Zhu CH, Doan C, Xie T. 2002. Germline stem cells anchored by adherens junctions in the Drosophila ovary niches. Science 296:1855–57 [Google Scholar]
  112. Spradling AC. 1993. Developmental genetics of oogenesis. The Development of Drosophila melanogaster 1 M Bate, A Martinez Arias 1–70 Cold Spring Harbor, NY: Cold Spring Harbor Lab. Press [Google Scholar]
  113. Spradling A, Fuller MT, Braun RE, Yoshida S. 2011. Germline stem cells. Cold Spring Harb. Perspect. Biol. 3:a002642 [Google Scholar]
  114. Stine RR, Greenspan LJ, Ramachandran KV, Matunis EL. 2014. Coordinate regulation of stem cell competition by Slit-Robo and JAK-STAT signaling in the Drosophila testis. PLOS Genet. 10:e1004713 [Google Scholar]
  115. Stine RR, Matunis EL. 2013. Stem cell competition: finding balance in the niche. Trends Cell Biol. 23:357–64 [Google Scholar]
  116. Suzuki H, Sada A, Yoshida S, Saga Y. 2009. The heterogeneity of spermatogonia is revealed by their topology and expression of marker proteins including the germ cell-specific proteins Nanos2 and Nanos3. Dev. Biol. 336:222–31 [Google Scholar]
  117. Tadokoro Y, Yomogida K, Ohta H, Tohda A, Nishimune Y. 2002. Homeostatic regulation of germinal stem cell proliferation by the GDNF/FSH pathway. Mech. Dev. 113:29–39 [Google Scholar]
  118. Takatsu K, Miyaoku K, Roy SR, Murono Y, Sago T. et al. 2013. Induction of female-to-male sex change in adult zebrafish by aromatase inhibitor treatment. Sci. Rep. 3:3400 [Google Scholar]
  119. Tanentzapf G, Devenport D, Godt D, Brown NH. 2007. Integrin-dependent anchoring of a stem-cell niche. Nat. Cell Biol. 9:1413–18 [Google Scholar]
  120. Tegelenbosch RA, de Rooij DG. 1993. A quantitative study of spermatogonial multiplication and stem cell renewal in the C3H/101 F1 hybrid mouse. Mutat. Res. 290:193–200 [Google Scholar]
  121. Teixeira VH, Nadarajan P, Graham TA, Pipinikas CP, Brown JM. et al. 2013. Stochastic homeostasis in human airway epithelium is achieved by neutral competition of basal cell progenitors. eLife 2:e00966 [Google Scholar]
  122. Thorel F, Nepote V, Avril I, Kohno K, Desgraz R. et al. 2010. Conversion of adult pancreatic α-cells to β-cells after extreme β-cell loss. Nature 464:1149–54 [Google Scholar]
  123. Tran J, Brenner TJ, DiNardo S. 2000. Somatic control over the germline stem cell lineage during Drosophila spermatogenesis. Nature 407:754–57 [Google Scholar]
  124. Tran V, Lim C, Xie J, Chen X. 2012. Asymmetric division of Drosophila male germline stem cell shows asymmetric histone distribution. Science 338:679–82 [Google Scholar]
  125. Tulina N, Matunis E. 2001. Control of stem cell self-renewal in Drosophila spermatogenesis by JAK-STAT signaling. Science 294:2546–49 [Google Scholar]
  126. Tursun B, Patel T, Kratsios P, Hobert O. 2011. Direct conversion of C. elegans germ cells into specific neuron types. Science 331:304–8 [Google Scholar]
  127. Uhlenhaut NH, Jakob S, Anlag K, Eisenberger T, Sekido R. et al. 2009. Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation. Cell 139:1130–42 [Google Scholar]
  128. Vermeulen L, Morrissey E, van der Heijden M, Nicholson AM, Sottoriva A. et al. 2013. Defining stem cell dynamics in models of intestinal tumor initiation. Science 342:995–98 [Google Scholar]
  129. Voog J, D'Alterio C, Jones DL. 2008. Multipotent somatic stem cells contribute to the stem cell niche in the Drosophila testis. Nature 454:1132–36 [Google Scholar]
  130. Voog J, Sandall SL, Hime GR, Resende LP, Loza-Coll M. et al. 2014. Escargot restricts niche cell to stem cell conversion in the Drosophila testis. Cell Rep. 7:722–34 [Google Scholar]
  131. Wang L, Li Z, Cai Y. 2008. The JAK/STAT pathway positively regulates DPP signaling in the Drosophila germline stem cell niche. J. Cell Biol. 180:721–28 [Google Scholar]
  132. Wu X, Oatley JM, Oatley MJ, Kaucher AV, Avarbock MR, Brinster RL. 2010. The POU domain transcription factor POU3F1 is an important intrinsic regulator of GDNF-induced survival and self-renewal of mouse spermatogonial stem cells. Biol. Reprod. 82:1103–11 [Google Scholar]
  133. Yadlapalli S, Yamashita YM. 2013. Chromosome-specific nonrandom sister chromatid segregation during stem-cell division. Nature 498:251–54 [Google Scholar]
  134. Yamashita YM, Fuller MT. 2008. Asymmetric centrosome behavior and the mechanisms of stem cell division. J. Cell Biol. 180:261–66 [Google Scholar]
  135. Yamashita YM, Jones DL, Fuller MT. 2003. Orientation of asymmetric stem cell division by the APC tumor suppressor and centrosome. Science 301:1547–50 [Google Scholar]
  136. Yamashita YM, Mahowald AP, Perlin JR, Fuller MT. 2007. Asymmetric inheritance of mother versus daughter centrosome in stem cell division. Science 315:518–21 [Google Scholar]
  137. Yan D, Neumuller RA, Buckner M, Ayers K, Li H. et al. 2014. A regulatory network of Drosophila germline stem cell self-renewal. Dev. Cell 28:459–73 [Google Scholar]
  138. Yoshida S. 2012. Elucidating the identity and behavior of spermatogenic stem cells in the mouse testis. Reproduction 144:293–302 [Google Scholar]
  139. Zhang H, Zheng W, Shen Y, Adhikari D, Ueno H, Liu K. 2012. Experimental evidence showing that no mitotically active female germline progenitors exist in postnatal mouse ovaries. PNAS 109:12580–85 [Google Scholar]
  140. Zhang Q, Shalaby NA, Buszczak M. 2014. Changes in rRNA transcription influence proliferation and cell fate within a stem cell lineage. Science 343:298–301 [Google Scholar]
  141. Zhang Z, Lv X, Jiang J, Zhang L, Zhao Y. 2013. Dual roles of Hh signaling in the regulation of somatic stem cell self-renewal and germline stem cell maintenance in Drosophila testis. Cell Res. 23:573–76 [Google Scholar]
  142. Zhou Q, Brown J, Kanarek A, Rajagopal J, Melton DA. 2008. In vivo reprogramming of adult pancreatic exocrine cells to β-cells. Nature 455:627–32 [Google Scholar]
  143. Zoller R, Schulz C. 2012. The Drosophila cyst stem cell lineage: Partners behind the scenes?. Spermatogenesis 2:145–57 [Google Scholar]
/content/journals/10.1146/annurev-cellbio-100913-013344
Loading
/content/journals/10.1146/annurev-cellbio-100913-013344
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error