A-single spermatogonia heterogeneity and cell cycles synchronize with rat seminiferous epithelium stages VIII-IX

Biology of Reproduction

Volumn 90, Issue 2, 2014, Pages

  Abid, Shadaan N ^a   Richardson, Timothy E ^a   Powell, Heather M ^a   Jaichander, Priscilla ^a   Chaudhary, Jaideep ^a   Chapman, Karen M ^a   Hamra, F Kent ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

A single spermatogonia; Epithelial cycle; ERBB3; Germline stemcell; HER3; Seminiferous; SNAP91; Spermatogenesis; Spermatogonia; Spermatogonial stem cells; Stem cell niche; Stem cells; Testis

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; BASEMENT MEMBRANE; BLOOD TESTIS BARRIER; CELL CYCLE; CELL HETEROGENEITY; CONTROLLED STUDY; GERM CELL; IMMUNOFLUORESCENCE; MALE; MICROENVIRONMENT; NONHUMAN; PRIORITY JOURNAL; RAT; SEMINIFEROUS TUBULE; SEMINIFEROUS TUBULE EPITHELIUM; SPERM; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOGONIUM; STEM CELL; STEM CELL NICHE; TESTIS; ANIMAL; CELL DIFFERENTIATION; CELL SEPARATION; CLASSIFICATION; CYTOLOGY; METABOLISM; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; CELL CYCLE; CELL DIFFERENTIATION; CELL SEPARATION; MALE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, ERBB-3; SEMINIFEROUS EPITHELIUM; SPERMATOGENESIS; SPERMATOGONIA; TESTIS;

EID: 84899978248     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.113.113555     Document Type: Article

References (76)

1. Regaud C. Some biological aspects of the radiation therapy of cancer. Am J Roentgen Radium Ther 1924; 12:97-101.
2. Phillips BT, Gassei K, Orwig KE. Spermatogonial stem cell regulation and spermatogenesis. Philos Trans R Soc Lond B Biol Sci 2010; 365: 1663-1678.
3. Oatley JM, Brinster RL. The germline stem cell niche unit in mammalian testes. Physiol Rev 2012; 92:577-595.
4. Brinster RL, Zimmermann JW. Spermatogenesis following male germ-cell transplantation. Proc Natl Acad Sci U S A 1994; 91:11298-11302.
5. Clermont Y. Kinetics of spermatogenesis in mammals: seminiferous epithelium cycle and spermatogonial renewal. Physiol Rev 1972; 52: 198-236.
6. Franca LR, Ogawa T, Avarbock MR, Brinster RL, Russell LD. Germ cell genotype controls cell cycle during spermatogenesis in the rat. Biol Reprod 1998; 59:1371-1377.
7. Russell LD, Ettlin RA, Hikim APS, Clegg ED (eds.). Histological and Histopathological Evaluation of the Testes. Clearwater, FL: Cache River Press; 1990.
8. Oakberg EF. Spermatogonial stem-cell renewal in the mouse. Anat Rec 1971; 169:515-531.
9. Huckins C. The spermatogonial stem cell population in adult rats. I. Their morphology, proliferation and maturation. Anat Rec 1971; 169:533-557.
10. Lok D, Weenk D, De Rooij DG. Morphology, proliferation, and differentiation of undifferentiated spermatogonia in the Chinese hamster and the ram. Anat Rec 1982; 203:83-99.
11. Nakagawa T, Sharma M, Nabeshima Y, Braun RE, Yoshida S. Functional hierarchy and reversibility within the murine spermatogenic stem cell compartment. Science 2010; 328:62-67.
12. Monesi V. Autoradiographic study of DNA synthesis and the cell cycle in spermatogonia and spermatocytes of mouse testis using tritiated thymidine. J Cell Biol 1962; 14:1-18.
13. Spradling A, Fuller MT, Braun RE, Yoshida S. Germline stem cells. Cold Spring Harb Perspect Biol 2011; 3:a002642.
14. Zheng K, Wu X, Kaestner KH, Wang PJ. The pluripotency factor LIN28 marks undifferentiated spermatogonia in mouse. BMC Dev Biol 2009; 9: 38.
15. Nakagawa T, Nabeshima Y, Yoshida S. Functional identification of the actual and potential stem cell compartments in mouse spermatogenesis. Dev Cell 2007; 12:195-206.
16. Sada A, Suzuki A, Suzuki H, Saga Y. The RNA-binding protein NANOS2 is required to maintain murine spermatogonial stem cells. Science 2009; 325:1394-1398.
17. Sheng XR, Matunis E. Live imaging of the Drosophila spermatogonial stem cell niche reveals novel mechanisms regulating germline stem cell output. Development 2011; 138:3367-3376.
18. Morrison SJ, Spradling AC. Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 2008; 132:598-611.
19. Meng X, Lindahl M, Hyvonen ME, Parvinen M, de Rooij DG, Hess MW, Raatikainen-Ahokas A, Sainio K, Rauvala H, Lakso M, Pichel JG, Westphal H, et al. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science 2000; 287:1489-1493.
20. Oatley MJ, Racicot KE, Oatley JM. Sertoli cells dictate spermatogonial stem cell niches in the mouse testis. Biol Reprod 2011; 84:639-645.
21. Kai T, Spradling A. Differentiating germ cells can revert into functional stem cells in Drosophila melanogaster ovaries. Nature 2004; 428: 564-569.
22. Brawley C, Matunis E. Regeneration of male germline stem cells by spermatogonial dedifferentiation in vivo. Science 2004; 304:1331-1334.
23. Cronkhite JT, Norlander C, Furth JK, Levan G, Garbers DL, Hammer RE. Male and female germline specific expression of an EGFP reporter gene in a unique strain of transgenic rats. Dev Biol 2005; 284:171-183.
24. Meijering E, Jacob M, Sarria JC, Steiner P, Hirling H, Unser M. Design and validation of a tool for neurite tracing and analysis in fluorescence microscopy images. Cytometry A 2004; 58:167-176.
25. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 2012; 9:671-675.
26. Perry B, Clermont Y, Leblond CP. The wave of the seminiferous epithelium in the rat. Am J Anat 1961; 108:47-78.
27. Clermont Y, Perey B. Quantitative study of the cell population of the seminiferous tubules in immature rats. Am J Anat 1957; 100:241-267.
28. Leblond CP, Clermont Y. Spermiogenesis of rat, mouse, hamster and guinea pig as revealed by the periodic acid-fuchsin sulfurous acid technique. Am J Anat 1952; 90:167-215.
29. Chapman KM, Powell HM, Chaudhary J, Shelton JM, Richardson JA, Richardson TE, Hamra FK. Linking spermatid RNA binding protein and retrogene diversity to reproductive success. Mol Cell Proteomics 2013; 12: 3221-3236.
30. Leblond CP, Clermont Y. Definition of the stages of the cycle of the seminiferous epithelium in the rat. Ann N Y Acad Sci 1952; 55:548-573.
31. Hamra FK, Schultz N, Chapman KM, Grellhesl DM, Cronkhite JT, Hammer RE, Garbers DL. Defining the spermatogonial stem cell. Dev Biol 2004; 269:393-410.
32. McGuinness MP, Linder CC, Morales CR, Heckert LL, Pikus J, Griswold MD. Relationship of a mouse Sertoli cell line (MSC-1) to normal Sertoli cells. Biol Reprod 1994; 51:116-124.
33. Hamra FK, Chapman KM, Nguyen D, Garbers DL. Identification of neuregulin as a factor required for formation of aligned spermatogonia. J Biol Chem 2007; 282:721-730.
34. Costoya JA, Hobbs RM, Barna M, Cattoretti G, Manova K, Sukhwani M, Orwig KE, Wolgemuth DJ, Pandolfi PP. Essential role of Plzf in maintenance of spermatogonial stem cells. Nat Genet 2004; 36:653-659.
35. Buaas FW, Kirsh AL, Sharma M, McLean DJ, Morris JL, Griswold MD, de Rooij DG, Braun RE. Plzf is required in adult male germ cells for stem cell self-renewal. Nat Genet 2004; 36:647-652.
36. Hamra FK, Chapman KM, Nguyen DM, Williams-Stephens AA, Hammer RE, Garbers DL. Self renewal, expansion, and transfection of rat spermatogonial stem cells in culture. Proc Natl Acad Sci U S A 2005; 102: 17430-17435.
37. Kanatsu-Shinohara M, Toyokuni S, Shinohara T. CD9 is a surface marker on mouse and rat male germline stem cells. Biol Reprod 2004; 70:70-75.
38. Bartles JR, Wierda A, Zheng L. Identification and characterization of espin, an actin-binding protein localized to the F-actin-rich junctional plaques of Sertoli cell ectoplasmic specializations. J Cell Sci 1996; 109(pt 6):1229-1239.
39. Kohtz DS, Puszkin S. A neuronal protein (NP185) associated with clathrin-coated vesicles. Characterization of NP185 with monoclonal antibodies. J Biol Chem 1988; 263:7418-7425.
40. Suzuki H, Sada A, Yoshida S, Saga Y. 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 2009; 336:222-231.
41. Suzuki A, Saga Y. Nanos2 suppresses meiosis and promotes male germ cell differentiation. Genes Dev 2008; 22:430-435.
42. Tsuda M, Sasaoka Y, Kiso M, Abe K, Haraguchi S, Kobayashi S, Saga Y. Conserved role of nanos proteins in germ cell development. Science 2003; 301:1239-1241.
43. Sada A, Hasegawa K, Pin PH, Saga Y. NANOS2 acts downstream of glial cell line-derived neurotrophic factor signaling to suppress differentiation of spermatogonial stem cells. Stem Cells 2012; 30:280-291.
44. Naughton CK, Jain S, Strickland AM, Gupta A, Milbrandt J. Glial cell-line derived neurotrophic factor-mediated RET signaling regulates spermatogonial stem cell fate. Biol Reprod 2006; 74:314-321.
45. Hofmann MC, Braydich-Stolle L, Dym M. Isolation of male germ-line stem cells; influence of GDNF. Dev Biol 2005; 279:114-124.
46. Suzuki H, Ahn HW, Chu T, Bowden W, Gassei K, Orwig K, Rajkovic A. SOHLH1 and SOHLH2 coordinate spermatogonial differentiation. Dev Biol 2012; 361:301-312.
47. Gassei K, Orwig KE. SALL4 expression in gonocytes and spermatogonial clones of postnatal mouse testes. PLoS ONE 2013; 8:e53976.
48. Hermann BP, Sukhwani M, Hansel MC, Orwig KE. Spermatogonial stem cells in higher primates: are there differences from those in rodents? Reproduction 2010; 139:479-493.
49. Campos-Junior PH, Costa GM, Lacerda SM, Rezende-Neto JV, de Paula AM, Hofmann MC, de Franca LR. The spermatogonial stem cell niche in the collared peccary (Tayassu tajacu). Biol Reprod 2012; 86:155.
50. Grasso M, Fuso A, Dovere L, de Rooij DG, Stefanini M, Boitani C, Vicini E. Distribution of GFRA1-expressing spermatogonia in adult mouse testis. Reproduction 2012; 143:325-332.
51. Oatley MJ, Kaucher AV, Racicot KE, Oatley JM. Inhibitor of DNA binding 4 is expressed selectively by single spermatogonia in the male germline and regulates the self-renewal of spermatogonial stem cells in mice. Biol Reprod 2011; 85:347-356.
52. Huckins C. The spermatogonial stem cell population in adult rats. II. A radioautographic analysis of their cell cycle properties.Cell Tissue Kinet 1971; 4:313-334.
53. Huckins C. The spermatogonial stem cell population in adult rats. 3. Evidence for a long-cycling population.Cell Tissue Kinet 1971; 4: 335-349.
54. Lok D, de Rooij DG. Spermatogonial multiplication in the Chinese hamster. III. Labelling indices of undifferentiated spermatogonia throughout the cycle of the seminiferous epithelium.Cell Tissue Kinet 1983; 16: 31-40.
55. Lok D, Jansen MT, de Rooij DG. Spermatogonial multiplication in the Chinese hamster. II. Cell cycle properties of undifferentiated spermatogonia. Cell Tissue Kinet 1983; 16:19-29.
56. Lok D, Jansen MT, de Rooij DG. Spermatogonial multiplication in the Chinese hamster. IV. Search for long cycling stem cells.Cell Tissue Kinet 1984; 17:135-143.
57. Hu YC, de Rooij DG, Page DC. Tumor suppressor gene Rb is required for self-renewal of spermatogonial stem cells in mice. Proc Natl Acad Sci U S A 2013; 110:12685-12690.
58. Yang QE, Gwost I, Oatley MJ, Oatley JM. Retinoblastoma protein (RB1) controls fate determination in stem cells and progenitors of the mouse male germline. Biol Reprod 2013; 89:113.
59. Sage J. The retinoblastoma tumor suppressor and stem cell biology. Genes Dev 2012; 26:1409-1420.
60. Chen D, McKearin D. Gene circuitry controlling a stem cell niche. Curr Biol 2005; 15:179-184.
61. Decotto E, Spradling AC. The Drosophila ovarian and testis stem cell niches: similar somatic stem cells and signals. Dev Cell 2005; 9:501-510.
62. Yamashita YM, Fuller MT. Asymmetric stem cell division and function of the niche in the Drosophila male germ line. Int J Hematol 2005; 82: 377-380.
63. de Cuevas M, Matunis EL. The stem cell niche: lessons from the Drosophila testis. Development 2011; 138:2861-2869.
64. Goriely A, McVean GA, van Pelt AM, O'Rourke AW, Wall SA, de Rooij DG, Wilkie AO. Gain-of-function amino acid substitutions drive positive selection of FGFR2 mutations in human spermatogonia. Proc Natl Acad Sci U S A 2005; 102:6051-6056.
65. Chen C, Ouyang W, Grigura V, Zhou Q, Carnes K, Lim H, Zhao GQ, Arber S, Kurpios N, Murphy TL, Cheng AM, Hassell JA, et al. ERM is required for transcriptional control of the spermatogonial stem cell niche. Nature 2005; 436:1030-1034.
66. Ryu BY, Orwig KE, Avarbock MR, Brinster RL. Stem cell and niche development in the postnatal rat testis. Dev Biol 2003; 263:253-263.
67. Chiarini-Garcia H, Hornick JR, Griswold MD, Russell LD. Distribution of type A spermatogonia in the mouse is not random. Biol Reprod 2001; 65: 1179-1185.
68. Yoshida S, Sukeno M, Nabeshima Y. A vasculature-associated niche for undifferentiated spermatogonia in the mouse testis. Science 2007; 317: 1722-1726.
69. Chiarini-Garcia H, Raymer AM, Russell LD. Non-random distribution of spermatogonia in rats: evidence of niches in the seminiferous tubules. Reproduction 2003; 126:669-680.
70. Huckins C. Cell cycle properties of differentiating spermatogonia in adult Sprague-Dawley rats. Cell Tissue Kinet 1971; 4:139-154.
71. Shetty G, Meistrich ML. The missing niche for spermatogonial stem cells: do blood vessels point the way? Cell Stem Cell 2007; 1:361-363.
72. de Rooij DG, Griswold MD. Questions about spermatogonia posed and answered since 2000. J Androl 2012; 33:1085-1095.
73. de Rooij DG, van Beek ME. Computer simulation of the rodent spermatogonial stem cell niche. Biol Reprod 2013; 88:131.
74. Tegelenbosch RA, de Rooij DG. A quantitative study of spermatogonial multiplication and stem cell renewal in the C3H/101 F1 hybrid mouse. Mutat Res 1993; 290:193-200.
75. De Rooij DG, Janssen JM. Regulation of the density of spermatogonia in the seminiferous epithelium of the Chinese hamster: I. Undifferentiated spermatogonia. Anat Rec 1987; 217:124-130.
76. De Rooij DG, Lok D. Regulation of the density of spermatogonia in the seminiferous epithelium of the Chinese hamster: II. Differentiating spermatogonia. Anat Rec 1987; 217:131-136.