Tumor suppressor gene Rb is required for self-renewal of spermatogonial stem cells in mice

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 31, 2013, Pages 12685-12690

  Hu, Yueh Chiang ^a   De Rooij, Dirk G ^a   Page, David C ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Fertility; Spermatogenesis; Testis

Indexed keywords

RETINOBLASTOMA PROTEIN;

ANIMAL CELL; ARTICLE; CELL DENSITY; CELL DIFFERENTIATION; CELL LOSS; CELL PROLIFERATION; CELL RENEWAL; CONTROLLED STUDY; GERM CELL; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROGENY; PROTEIN FUNCTION; SPERMATOGONIUM; TESTIS;

FERTILITY; SPERMATOGENESIS; TESTIS;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR RECEPTORS; MALE; MICE; MICE, TRANSGENIC; RETINOBLASTOMA PROTEIN; SPERMATOGONIA; STEM CELLS;

EID: 84881098478     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1311548110     Document Type: Article

References (49)

1. Chinnam M, Goodrich DW (2011) RB1, development, and cancer. Curr Top Dev Biol 94: 129-169.
2. Manning AL, Dyson NJ (2012) RB: Mitotic implications of a tumour suppressor. Nat Rev Cancer 12(3):220-226.
3. Sage J (2012) The retinoblastoma tumor suppressor and stem cell biology. Genes Dev 26(13):1409-1420.
4. Orford KW, Scadden DT (2008) Deconstructing stem cell self-renewal: Genetic insights into cell-cycle regulation. Nat Rev Genet 9(2):115-128.
5. Viatour P, et al. (2008) Hematopoietic stem cell quiescence is maintained by compound contributions of the retinoblastoma gene family. Cell Stem Cell 3(4):416-428.
6. Viatour P, et al. (2011) Notch signaling inhibits hepatocellular carcinoma following inactivation of the RB pathway. J Exp Med 208(10):1963-1976.
7. Hosoyama T, Nishijo K, Prajapati SI, Li G, Keller C (2011) Rb1 gene inactivation expands satellite cell and postnatal myoblast pools. J Biol Chem 286(22):19556-19564.
8. Ruiz S, et al. (2004) Unique and overlapping functions of pRb and p107 in the control of proliferation and differentiation in epidermis. Development 131(11):2737-2748.
9. Walkley CR, Orkin SH (2006) Rb is dispensable for self-renewal and multilineage differentiation of adult hematopoietic stem cells. Proc Natl Acad Sci USA 103(24): 9057-9062.
10. Thomas DM, et al. (2001) The retinoblastoma protein acts as a transcriptional coactivator required for osteogenic differentiation. Mol Cell 8(2):303-316.
11. Haigis K, Sage J, Glickman J, Shafer S, Jacks T (2006) The related retinoblastoma (pRb) and p130 proteins cooperate to regulate homeostasis in the intestinal epithelium. J Biol Chem 281(1):638-647.
12. Calo E, et al. (2010) Rb regulates fate choice and lineage commitment in vivo. Nature 466(7310):1110-1114.
13. Jiang Z, et al. (2010) Rb deletion in mouse mammary progenitors induces luminal-B or basal-like/EMT tumor subtypes depending on p53 status. J Clin Invest 120(9): 3296-3309.
14. Chen D, et al. (2004) Cell-specific effects of RB or RB/p107 loss on retinal development implicate an intrinsically death-resistant cell-of-origin in retinoblastoma. Cancer Cell 5(6):539-551.
15. Grisanti L, et al. (2009) Identification of spermatogonial stem cell subsets by morphological analysis and prospective isolation. Stem Cells 27(12):3043-3052.
16. Lok D, Jansen MT, de Rooij DG (1984) Spermatogonial multiplication in the Chinese hamster. IV. Search for long cycling stem cells. Cell Tissue Kinet 17(2):135-143.
17. 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(2):214-224.
18. Huckins C (1971) The spermatogonial stem cell population in adult rats. I. Their morphology, proliferation and maturation. Anat Rec 169(3):533-557.
19. Oakberg EF (1971) Spermatogonial stem-cell renewal in the mouse. Anat Rec 169(3): 515-531.
20. de Rooij DG (1973) Spermatogonial stem cell renewal in the mouse. I. Normal situation. Cell Tissue Kinet 6(3):281-287.
21. Nakagawa T, Sharma M, Nabeshima Y, Braun RE, Yoshida S (2010) Functional hierarchy and reversibility within the murine spermatogenic stem cell compartment. Science 328(5974):62-67.
22. Sada A, Hasegawa K, Pin PH, Saga Y (2012) NANOS2 acts downstream of glial cell linederived neurotrophic factor signaling to suppress differentiation of spermatogonial stem cells. Stem Cells 30(2):280-291.
23. De Rooij DG, Griswold MD (2012) Questions about spermatogonia posed and answered since 2000. J Androl 22(6):1085-1095.
24. Ahmed EA, de Rooij DG (2009) Staging of mouse seminiferous tubule cross-sections. Methods Mol Biol 558:263-277.
25. Phillips BT, Gassei K, Orwig KE (2010) Spermatogonial stem cell regulation and spermatogenesis. Philos Trans R Soc Lond B Biol Sci 365(1546):1663-1678.
26. Oatley JM, Brinster RL (2012) The germline stem cell niche unit in mammalian testes. Physiol Rev 92(2):577-595.
27. Sada A, Suzuki A, Suzuki H, Saga Y (2009) The RNA-binding protein NANOS2 is required to maintain murine spermatogonial stem cells. Science 325(5946):1394-1398.
28. Sage J, Miller AL, Pérez-Mancera PA, Wysocki JM, Jacks T (2003) Acute mutation of retinoblastoma gene function is sufficient for cell cycle reentry. Nature 424(6945): 223-228.
29. Soriano P (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21(1):70-71.
30. de Rooij DG, Grootegoed JA (1998) Spermatogonial stem cells. Curr Opin Cell Biol 10 (6):694-701.
31. Spiller CM, Wilhelm D, Koopman P (2010) Retinoblastoma 1 protein modulates XY germ cell entry into G1/G0 arrest during fetal development in mice. Biol Reprod 82(2): 433-443.
32. 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(2): 193-200.
33. Grasso M, et al. (2012) Distribution of GFRA1-expressing spermatogonia in adult mouse testis. Reproduction 143(3):325-332.
34. 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 cellspecific proteins Nanos2 and Nanos3. Dev Biol 336(2):222-231.
35. McLean DJ, Friel PJ, Johnston DS, Griswold MD (2003) Characterization of spermatogonial stem cell maturation and differentiation in neonatal mice. Biol Reprod 69(6):2085-2091.
36. De Rooij DG, Lok D (1987) Regulation of the density of spermatogonia in the seminiferous epithelium of the Chinese hamster: II. Differentiating spermatogonia. Anat Rec 217(2):131-136.
37. Russell LD, Chiarini-Garcia H, Korsmeyer SJ, Knudson CM (2002) Bax-dependent spermatogonia apoptosis is required for testicular development and spermatogenesis. Biol Reprod 66(4):950-958.
38. Wikenheiser-Brokamp KA (2006) Retinoblastoma family proteins: Insights gained through genetic manipulation of mice. Cell Mol Life Sci 63(7-8):767-780.
39. Spradling A, Fuller MT, Braun RE, Yoshida S (2011) Germline stem cells. Cold Spring Harb Perspect Biol 3(11):a002642.
40. Oatley MJ, Kaucher AV, Racicot KE, Oatley JM (2011) 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 85(2):347-356.
41. Iavarone A, Garg P, Lasorella A, Hsu J, Israel MA (1994) The helix-loop-helix protein Id-2 enhances cell proliferation and binds to the retinoblastoma protein. Genes Dev 8(11):1270-1284.
42. Lasorella A, Noseda M, Beyna M, Yokota Y, Iavarone A (2000) Id2 is a retinoblastoma protein target and mediates signalling by Myc oncoproteins. Nature 407(6804): 592-598.
43. Tyagi G, et al. (2009) Loss of Etv5 decreases proliferation and RET levels in neonatal mouse testicular germ cells and causes an abnormal first wave of spermatogenesis. Biol Reprod 81(2):258-266.
44. 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(2):314-321.
45. Costoya JA, et al. (2004) Essential role of Plzf in maintenance of spermatogonial stem cells. Nat Genet 36(6):653-659.
46. Buageaw A, et al. (2005) GDNF family receptor alpha1 phenotype of spermatogonial stem cells in immature mouse testes. Biol Reprod 73(5):1011-1016.
47. Shaner NC, et al. (2008) Improving the photostability of bright monomeric orange and red fluorescent proteins. Nat Methods 5(6):545-551.
48. Gill ME, Hu YC, Lin Y, Page DC (2011) Licensing of gametogenesis, dependent on RNA binding protein DAZL, as a gateway to sexual differentiation of fetal germ cells. Proc Natl Acad Sci USA 108(18):7443-7448.
49. Buganim Y, et al. (2012) Direct reprogramming of fibroblasts into embryonic Sertolilike cells by defined factors. Cell Stem Cell 11(3):373-386.