ROS-generating oxidase Nox3 regulates the self-renewal of mouse spermatogonial stem cells

Biology of Reproduction

Volumn 92, Issue 6, 2015, Pages

  Morimoto, Hiroko ^a   Kanatsu Shinohara, Mito ^a,b   Shinohara, Takashi ^a  

^a KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Spermatogenesis; Spermatogonia; Spermatogonial stem cells; Stem cells; Testis

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; CYTOKINE; DIMETHYL SULFOXIDE; FIBROBLAST GROWTH FACTOR 2; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; MESSENGER RNA; N (2,3 DIHYDROXYPROPOXY) 3,4 DIFLUORO 2 (2 FLUORO 4 IODOANILINO)BENZAMIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 3; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; RHODAMINE; RNA; SHORT HAIRPIN RNA; TRYPSIN; UNCLASSIFIED DRUG; NOX3 PROTEIN, MOUSE; OXIDOREDUCTASE;

ACROSOME; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL ISOLATION; CELL PROLIFERATION; CELL RENEWAL; CELL STIMULATION; CELL STRUCTURE; CONTROLLED STUDY; ENZYME INHIBITION; FLOW CYTOMETRY; GENE DOSAGE; GENETIC TRANSFECTION; IMMUNOHISTOCHEMISTRY; IMMUNOHISTOLOGY; MALE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; SEMINIFEROUS TUBULE; SPERMATOGONIAL STEM CELL; SPERMATOGONIUM; STEM CELL; TESTIS CELL; TUNEL ASSAY; UPREGULATION; ANIMAL; CELL CULTURE; CYTOLOGY; GENETICS; METABOLISM; PHYSIOLOGY; SPERMATOGENESIS;

ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; MALE; MICE; NADH, NADPH OXIDOREDUCTASES; NADPH OXIDASE; REACTIVE OXYGEN SPECIES; SPERMATOGENESIS; SPERMATOGONIA; STEM CELLS;

EID: 84936929543     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.114.127647     Document Type: Article

References (31)

1. de Rooij DG, Russell LD. All you wanted to know about spermatogonia but were afraid to ask. J Androl 2000; 21:776-798.
2. Meistrich ML, van Beek MEAB. Spermatogonial stem cells. In: Desjardins CC, Ewing LL (eds.), Cell and Molecular Biology of the Testis. New York: Oxford University Press; 1993:266-295.
3. Meng X, Lindahl M, Hyvönen 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.
4. Kanatsu-Shinohara M, Ogonuki N, Inoue K, Miki H, Ogura A, Toyokuni S, Shinohara T. Long-term proliferation in culture and germline transmission of mouse male germline stem cells. Biol Reprod 2003; 69: 612-616.
5. Kanatsu-Shinohara M, Shinohara T. Spermatogonial stem cell selfrenewal and development. Annu Rev Cell Dev Biol 2013; 29:163-187.
6. Lee J, Kanatsu-Shinohara M, Morimoto H, Kazuki Y, Takashima S, Oshimura M, Toyokuni S, Shinohara T. Genetic reconstruction of mouse spermatogonial stem cell self-renewal in vitro by Ras-cyclin D2 activation. Cell Stem Cell 2009; 5:76-86.
7. Lee J, Kanatsu-Shinohara M, Inoue K, Ogonuki N, Miki H, Toyokuni S, Kimura T, Nakano T, Ogura A, Shinohara T. Akt mediates self-renewal division of mouse spermatogonial stem cells. Development 2007; 134: 1853-1859.
8. Oatley JM, Avarbock MR, Brinster RL. Gial cell line-derived neurotrophic factor regulation of genes essential for self-renewal of mouse spermatogonial stem cells is dependent on Src family kinase signaling. J Biol Chem 2007; 282:25842-25851.
9. Braydich-Stolle L, Kostereva N, Dym M, Hofmann MC. Role of Src family kinases and N-Myc in spermatogonial stem cell proliferation. Dev Biol 2007; 304:34-45.
10. Ishii K, Kanatsu-Shinohara M, Toyokuni S, Shinohara T. FGF2 mediates mouse spermatogonial stem cell self-renewal via upregulation of Etv5 and Bcl6b through MAP2K1 activation. Development 2012; 139:1734-1743.
11. Oatley JM, Avarbock MR, Telaranta AI, Fearon DT, Brinster RL. Identifying genes important for spermatogonial stem cell self-renewal and survival. Proc Natl Acad Sci U S A 2006; 103:9524-9529.
12. Morimoto H, Iwata K, Ogonuki N, Inoue K, Ogura A, Kanatsu-Shinohara M, Morimoto T, Yabe-Nishimura C, Shinohara T. ROS are required for mouse spermatogonial stem cell self-renewal. Cell Stem Cell 2013; 12: 774-786.
13. Bedard K, Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 2007; 87: 245-313.
14. Saalu LC. The incriminating role of reactive oxygen species in idiopathic male infertility: an evidence based evaluation. Pak J Biol Sci 2010; 13: 413-422.
15. Chen G, Cao Z, Xu X, van Meir EG, Lambeth JD. Homologs of gp91 phox: cloning and tissue expression of Nox3, Nox4, and Nox5. Gene 2001; 269:131-140.
16. Ueyama T, Geiszt M, Leto TL. Involvement of Rac1 in activation of multicomponent Nox1-and Nox3-based NADPH oxidases. Mol Cell Biol 2006; 26:2160-2174.
17. Ogawa T, Aréchaga JM, Avarbock MR, Brinster RL. Transplantation of testis germinal cells into mouse seminiferous tubules. Int J Dev Biol 1997; 41:111-122.
18. Kanatsu-Shinohara M, Muneto T, Lee J, Takenaka M, Chuma S, Nakatsuji N, Horiuchi T, Shinohara T. Long-term culture of male germline stem cells from hamster testes. Biol Reprod 2008; 78:611-617.
19. Lee SH, Park DW, Park SC, Park YK, Hong SY, Kim JR, Lee CH, Baek SH. Calcium-independent phospholipase A2β-Akt signaling is involved in lipopolysaccharide-induced NADPH oxidase 1 expression and foam cell formation. J Immunol 2009; 183:7497-7504.
20. Adachi Y, Shibai Y, Mitsushita J, Shang WH, Hirose K, Kamata T. Oncogenic Ras upregulates NADPH oxidase 1 gene expression through MEK-ERK-dependent phosphorylation of GATA-6. Oncogene 2008; 27: 4921-4932.
21. Brinster RL, Zimmermann JW. Spermatogenesis following male germ-cell transplantation. Proc Natl Acad Sci U S A 1994; 91:11298-11302.
22. Shinohara T, Orwig KE, Avarbock MR, Brinster RL. Remodeling of the postnatal mouse testis is accompanied by dramatic changes in stem cell number and niche accessibility. Proc Natl Acad Sci U S A 2001; 98: 6186-6191.
23. Peterson JR, Burmeister MA, Tian X, Zhou Y, Guruju MR, Stupinski JA, Sharma RV, Davisson EL. Genetic silencing of Nox2 and Nox4 reveals differential roles of these NADPH oxidase homologues in the vasopressor and dipsogenic effects of brain angiotensin II. Hypertention 2009; 54: 1106-1114.
24. Piccoli C, D'Aprile A, Ripoli M, Scrima R, Lecce L, Boffoli D, Tabilio A, Capitanio N. Bone-marrow derived hematopoietic stem/progenitor cells express multiple isoforms of NADPH oxidase and produce constitutively reactive oxygen species. Biochem Biophys Res Commun 2007; 353: 965-972.
25. Bánfi B, Malgrange B, Knisz J, Steger K, Dubois-Dauphin M, Krause KH. NOX3, a superoxide-generating NADPH oxidase of the inner ear. J Biol Chem 2004; 279:46065-46072.
26. Paffenholz R, Bergstrom RA, Pasutto F, Wabnitz P, Munroe RJ, Jagia W, Heinzmann U, Marquardt A, Bareiss A, Laufs J, Russ A, Stumm G, et al. Vestibular defects in head-tilt mice result from mutations in Nox3, encoding an NADPH oxidase. Genes Dev 2004; 18:486-491.
27. Kiss PJ, Knisz J, Zhang Y, Baltrusaitis J, Sigmund CD, Thalmann R, Smith RJH, Verpy E, Bánfi B. Inactivation of NADPH oxidase organizer 1 results in severe imbalance. Curr Biol 2006; 16:208-213.
28. Gao D, Nong S, Huang X, Lu Y, Zhao H, Lin Y, Man Y, Wang S, Yang J, Li J. The effects of palmitate on hepatic insulin resistance are mediated by NADPH Oxidase 3-derived reactive oxygen species through JNK and p38MAPK pathways. J Biol Chem 2010; 285:29965-29973.
29. Takubo K, Ohmura M, Azuma M, Nagamatsu G, Yamada W, Arai F, Hirao A, Suda T. Stem cell defects in ATM-deficient undifferentiated spermatogonia through DNA damage-induced cell-cycle arrest. Cell Stem Cell 2008; 2:170-182.
30. Goertz MJ, Wu Z, Gallardo TD, Hamra FK, Castrillon DH. Foxo1 is required in mouse spermatogonial stem cells for their maintenance and the initiation of spermatogenesis. J Clin Invest 2011; 121:3456-3466.
31. Gruber M, Mathew LK, Runge AC, Garcia JA, Simon MC. EPAS1 is required for spermatogenesis in the postnatal mouse testis. Biol Reprod 2010; 82:1227-1236.