The transition from stem cell to progenitor spermatogonia and male fertility requires the SHP2 protein tyrosine phosphatase

Stem Cells

Volumn 32, Issue 3, 2014, Pages 741-753

  Puri, Pawan ^a   Phillips, Bart T ^a   Suzuki, Hitomi ^a   Orwig, Kyle E ^a   Rajkovic, Aleksandar ^a   Lapinski, Philip E ^b   King, Philip D ^b   Feng, Gen Sheng ^c   Walker, William H ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Germ cell; Male fertility; Sertoli cell; Signaling pathways; Spermatogenesis; Sterilization; Testis

Indexed keywords

GERM CELL; MALE FERTILITY; SERTOLI CELL; SIGNALING PATHWAYS; SPERMATOGENESIS; STERILIZATION; TESTIS;

AGING; ANIMALS; CELL ADHESION; CELL COUNT; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; FERTILITY; GENE DELETION; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; MICE, KNOCKOUT; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 11; SIGNAL TRANSDUCTION; SPERMATOGENESIS; SPERMATOGONIA; STEM CELLS;

EID: 84894274891     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.1572     Document Type: Article

References (48)

1. Yoshida S, Sukeno M, Nakagawa T, et al. The first round of mouse spermatogenesis is a distinctive program that lacks the self-renewing spermatogonia stage. Development 2006; 133: 1495-1505.
2. Bellve AR, Cavicchia JC, Millette CF, et al. Spermatogenic cells of the prepuberal mouse. Isolation and morphological characterization. J Cell Biol 1977; 74: 68-85.
3. 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.
4. Kluin PM, de Rooij DG,. A comparison between the morphology and cell kinetics of gonocytes and adult type undifferentiated spermatogonia in the mouse. Int J Androl 1981; 4: 475-493.
5. Meng X, Lindahl M, Hyvonen ME, et al. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science 2000; 287: 1489-1493.
6. Nagano M, Ryu BY, Brinster CJ, et al. Maintenance of mouse male germ line stem cells in vitro. Biol Reprod 2003; 68: 2207-2214.
7. Kubota H, Avarbock MR, Brinster RL,. Growth factors essential for self-renewal and expansion of mouse spermatogonial stem cells. Proc Natl Acad Sci USA 2004; 101: 16489-16494.
8. Perrinjaquet M, Vilar M, Ibanez CF,. Protein-tyrosine phosphatase SHP2 contributes to GDNF neurotrophic activity through direct binding to phospho-Tyr687 in the RET receptor tyrosine kinase. J Biol Chem 2010; 285: 31867-31875.
9. Cai Z, Feng GS, Zhang X,. Temporal requirement of the protein tyrosine phosphatase Shp2 in establishing the neuronal fate in early retinal development. J Neurosci 2010; 30: 4110-4119.
10. Mohi MG, Neel BG,. The role of Shp2 (PTPN11) in cancer. Curr Opin Genet Dev 2007; 17: 23-30.
11. Zhang SS, Hao E, Yu J, et al. Coordinated regulation by Shp2 tyrosine phosphatase of signaling events controlling insulin biosynthesis in pancreatic beta-cells. Proc Natl Acad Sci USA 2009; 106: 7531-7536.
12. Dance M, Montagner A, Salles JP, et al. The molecular functions of Shp2 in the Ras/Mitogen-activated protein kinase (ERK1/2) pathway. Cell Signal 2008; 20: 453-459.
13. Xu D, Qu CK,. Protein tyrosine phosphatases in the JAK/STAT pathway. Front Biosci 2008; 13: 4925-4932.
14. Edouard T, Montagner A, Dance M et al. How do Shp2 mutations that oppositely influence its biochemical activity result in syndromes with overlapping symptoms? Cell Mol Life Sci 2007; 64: 1585-1590.
15. Saxton TM, Henkemeyer M, Gasca S, et al. Abnormal mesoderm patterning in mouse embryos mutant for the SH2 tyrosine phosphatase Shp-2. EMBO J 1997; 16: 2352-2364.
16. Tartaglia M, Niemeyer CM, Fragale A, et al. Somatic mutations in PTPN11 in juvenile myelomonocytic leukemia, myelodysplastic syndromes and acute myeloid leukemia. Nat Genet 2003; 34: 148-150.
17. Chan RJ, Feng GS,. PTPN11 is the first identified proto-oncogene that encodes a tyrosine phosphatase. Blood 2007; 109: 862-867.
18. van der Burgt I, Berends E, Lommen E, et al. Clinical and molecular studies in a large Dutch family with Noonan syndrome. Am J Med Genet 1994; 53: 187-191.
19. Puri P, Walker WH,. The tyrosine phosphatase SHP2 regulates Sertoli cell junction complexes. Biol Reprod 2013; 88: 59.
20. Ruzankina Y, Pinzon-Guzman C, Asare A, et al. Deletion of the developmentally essential gene ATR in adult mice leads to age-related phenotypes and stem cell loss. Cell Stem Cell 2007; 1: 113-126.
21. Zhang EE, Chapeau E, Hagihara K, et al. Neuronal Shp2 tyrosine phosphatase controls energy balance and metabolism. Proc Natl Acad Sci USA 2004; 101: 16064-16069.
22. Bauler TJ, Kamiya N, Lapinski PE, et al. Development of severe skeletal defects in induced SHP-2-deficient adult mice: A model of skeletal malformation in humans with SHP-2 mutations. Dis Model Mech 2011; 4: 228-239.
23. Gallardo T, Shirley L, John GB, et al. Generation of a germ cell-specific mouse transgenic Cre line, Vasa-Cre. Genesis 2007; 45: 413-417.
24. Oatley JM, Brinster RL,. Spermatogonial stem cells. Methods Enzymol 2006; 419: 259-282.
25. Metzger D, Chambon P,. Site- and time-specific gene targeting in the mouse. Methods 2001; 24: 71-80.
26. Russell LD, Bartke A, Goh JC,. Postnatal development of the Sertoli cell barrier, tubular lumen, and cytoskeleton of Sertoli and myoid cells in the rat, and their relationship to tubular fluid secretion and flow. Am J Anat 1989; 184: 179-189.
27. Buaas FW, Kirsh AL, Sharma M, et al. Plzf is required in adult male germ cells for stem cell self-renewal. Nat Genet 2004; 36: 647-652.
28. Costoya JA, Hobbs RM, Barna M, et al. Essential role of Plzf in maintenance of spermatogonial stem cells. Nat Genet 2004; 36: 653-659.
29. Kanatsu-Shinohara M, Miki H, Inoue K, et al. Long-term culture of mouse male germline stem cells under serum-or feeder-free conditions. Biol Reprod 2005; 72: 985-991.
30. Ryu BY, Kubota H, Avarbock MR, et al. Conservation of spermatogonial stem cell self-renewal signaling between mouse and rat. Proc Natl Acad Sci USA 2005; 102: 14302-14307.
31. Braydich-Stolle L, Kostereva N, Dym M, et al. Role of Src family kinases and N-Myc in spermatogonial stem cell proliferation. Dev Biol 2007; 304: 34-45.
32. Savitt J, Singh D, Zhang C, et al. The in vivo response of stem and other undifferentiated spermatogonia to the reversible inhibition of glial cell line-derived neurotrophic factor signaling in the adult. Stem Cells 2012; 30: 732-740.
33. He Z, Jiang J, Kokkinaki M, et al. Gdnf upregulates c-Fos transcription via the Ras/Erk1/2 pathway to promote mouse spermatogonial stem cell proliferation. Stem Cells 2008; 26: 266-278.
34. Ishii K, Kanatsu-Shinohara M, Toyokuni S, et al. FGF2 mediates mouse spermatogonial stem cell self-renewal via upregulation of Etv5 and Bcl6b through MAP2K1 activation. Development 2012; 139: 1734-1743.
35. Ke Y, Zhang EE, Hagihara K, et al. Deletion of Shp2 in the brain leads to defective proliferation and differentiation in neural stem cells and early postnatal lethality. Mol Cell Biol 2007; 27: 6706-6717.
36. Nagano M, Avarbock MR, Brinster RL,. Pattern and kinetics of mouse donor spermatogonial stem cell colonization in recipient testes. Biol Reprod 1999; 60: 1429-1436.
37. Yoshida S, Sukeno M, Nabeshima Y,. A vasculature-associated niche for undifferentiated spermatogonia in the mouse testis. Science 2007; 317: 1722-1726.
38. de Rooij DG, Russell LD,. All you wanted to know about spermatogonia but were afraid to ask. J Androl 2000; 21: 776-798.
39. Schlesser HN, Simon L, Hofmann MC, et al. Effects of ETV5 (ets variant gene 5) on testis and body growth, time course of spermatogonial stem cell loss, and fertility in mice. Biol Reprod 2008; 78: 483-489.
40. Zhu HH, Ji K, Alderson N, et al. Kit-Shp2-Kit signaling acts to maintain a functional hematopoietic stem and progenitor cell pool. Blood 2011; 117: 5350-5361.
41. Chan G, Cheung LS, Yang W, et al. Essential role for Ptpn11 in survival of hematopoietic stem and progenitor cells. Blood 2011; 117: 4253-4261.
42. Yang W, Klaman LD, Chen B, et al. An Shp2/SFK/Ras/Erk signaling pathway controls trophoblast stem cell survival. Dev Cell 2006; 10: 317-327.
43. Chen C, Ouyang W, Grigura V, et al. ERM is required for transcriptional control of the spermatogonial stem cell niche. Nature 2005; 436: 1030-1034.
44. Goertz MJ, Wu Z, Gallardo TD, et al. Foxo1 is required in mouse spermatogonial stem cells for their maintenance and the initiation of spermatogenesis. J Clin Invest 2011; 121: 3456-3466.
45. Gallagher SJ, Kofman AE, Huszar JM, et al. Distinct requirements for Sin3a in perinatal male gonocytes and differentiating spermatogonia. Dev Biol 2013; 373: 83-94.
46. Willecke R, Heuberger J, Grossmann K, et al. The tyrosine phosphatase Shp2 acts downstream of GDNF/Ret in branching morphogenesis of the developing mouse kidney. Dev Biol 2011; 360: 310-317.
47. Mansukhani A, Bellosta P, Sahni M, et al. Signaling by fibroblast growth factors (FGF) and fibroblast growth factor receptor 2 (FGFR2)-activating mutations blocks mineralization and induces apoptosis in osteoblasts. J Cell Biol 2000; 149: 1297-1308.
48. Yoon SR, Choi SK, Eboreime J, et al. Age-dependent germline mosaicism of the most common Noonan Syndrome mutation shows the signature of germline selection. Am J Hum Genetics 2013; 92: 917-926.