Puma and Trail/Dr5 pathways control radiation-induced apoptosis in distinct populations of testicular progenitors

PLoS ONE

Volumn 5, Issue 8, 2010, Pages

  Coureuil, Mathieu ^a,c   Ugolin, Nicolas ^b   Tavernier, Marie ^a   Chevillard, Sylvie ^b   Barroca, Vilma ^a   Fouchet, Pierre ^a   Allemand, Isabelle ^a  

^a INSERM   (France)

^b INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA6 INTEGRIN; DEATH RECEPTOR 5; PROTEIN P53; PUMA PROTEIN; STEM CELL FACTOR; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; APOPTOSIS REGULATORY PROTEIN; PUMA PROTEIN, MOUSE; TUMOR SUPPRESSOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL FRACTIONATION; CELL SUBPOPULATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FLOW CYTOMETRY; GAMMA RADIATION; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCATION; GENOTOXICITY; IMMUNOMAGNETIC SEPARATION; MALE; MOUSE; NICK END LABELING; NONHUMAN; RADIATION INJURY; RADIOSENSITIVITY; SPERMATOGONIUM; STEM CELL; UPREGULATION; ADULT STEM CELL; ANIMAL; CYTOLOGY; GENE EXPRESSION REGULATION; METABOLISM; MITOCHONDRION; RADIATION EXPOSURE; SIGNAL TRANSDUCTION; TESTIS;

ADULT STEM CELLS; ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CELL DIFFERENTIATION; GAMMA RAYS; GENE EXPRESSION REGULATION; MALE; MICE; MITOCHONDRIA; SIGNAL TRANSDUCTION; SPERMATOGONIA; TESTIS; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

EID: 77957912444     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0012134     Document Type: Article

References (41)

1. Hasegawa M, Zhang Y, Niibe H, Terry N, Meistrich M (1998) Resistance of differentiating spermatogonia to radiation-induced apoptosis and loss in p53-deficient mice. Radiation Res 149: 263-270.
2. Beumer TL, Roepers-Gajadien HL, Gademan IS, van Buul PP, Gil-Gomez G, et al. (1998) The role of the tumor suppressor p53 in spermatogenesis. Cell Death Differ 5: 669-677.
3. Coureuil M, Fouchet P, Prat M, Letallec B, Barroca V, et al. (2006) Caspase-independent death of meiotic and postmeiotic cells overexpressing p53: calpain involvement. Cell Death Differ 13: 1927-1937.
4. Owen-Schaub LB, Zhang W, Cusack JC, Angelo LS, Santee SM, et al. (1995) Wild-type human p53 and a temperature-sensitive mutant induce Fas/APO-1 expression. Mol Cell Biol 15: 3032-3040.
5. Richburg JH, Nanez A, Williams LR, Embree ME, Boekelheide K (2000) Sensitivity of testicular germ cells to toxicant-induced apoptosis in gld mice that express a nonfunctional form of Fas ligand. Endocrinology 141: 787-793.
6. Embree-Ku M, Venturini D, Boekelheide K (2002) Fas is involved in the p53-dependent apoptotic response to ionizing radiation in mouse testis. Biol Reprod 66: 1456-1461.
7. Johnstone RW, Frew AJ, Smyth MJ (2008) The TRAIL apoptotic pathway in cancer onset, progression and therapy. Nat Rev Cancer 8: 782-798.
8. Wu GS, Burns TF, McDonald ER, 3rd, Jiang W, Meng R, et al. (1997) KILLER/DR5 is a DNA damage-inducible p53-regulated death receptor gene. Nat Genet 17: 141-143.
9. Finnberg N, Gruber JJ, Fei P, Rudolph D, Bric A, et al. (2005) DR5 knockout mice are compromised in radiation-induced apoptosis. Mol Cell Biol 25: 2000-2013.
10. McKee CM, Ye Y, Richburg JH (2006) Testicular germ cell sensitivity to TRAIL-induced apoptosis is dependent upon p53 expression and is synergis-tically enhanced by DR5 agonistic antibody treatment. Apoptosis 11: 2237-2250.
11. Russell LD, Chiarini-Garcia H, Korsmeyer SJ, Knudson CM (2002) Bax-dependent spermatogonia apoptosis is required for testicular development and spermatogenesis. Biol Reprod 66: 950-958.
12. Kasai S, Chuma S, Motoyama N, Nakatsuji N (2003) Haploinsufficiency of Bcl-x leads to male-specific defects in fetal germ cells: differential regulation of germ cell apoptosis between the sexes. Dev Biol 264: 202-216.
13. Coultas L, Bouillet P, Loveland KL, Meachem S, Perlman H, et al. (2005) Concomitant loss of proapoptotic BH3-only Bcl-2 antagonists Bik and Bim arrests spermatogenesis. Embo J 24: 3963-3973.
14. Chiarini-Garcia H, Russell LD (2001) High-resolution light microscopic characterization of mouse spermatogonia. Biol Reprod 65: 1170-1178.
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: 653-659.
16. Shinohara T, Avarbock MR, Brinster RL (1999) beta1- and alpha6-integrin are surface markers on mouse spermatogonial stem cells. Proc Natl Acad Sci U S A 96: 5504-5509.
17. Falciatori I, Borsellino G, Haliassos N, Boitani C, Corallini S, et al. (2004) Identification and enrichment of spermatogonial stem cells displaying side-population phenotype in immature mouse testis. Faseb J 18: 376-378.
18. Lassalle B, Bastos H, Louis JP, Riou L, Testart J, et al. (2004) 'Side Population' cells in adult mouse testis express Bcrp1 gene and are enriched in spermatogonia and germinal stem cells. Development 131: 479-487.
19. Schrans-Stassen BH, van de Kant HJ, de Rooij DG, van Pelt AM (1999) Differential expression of c-kit in mouse undifferentiated and differentiating type A spermatogonia. Endocrinology 140: 5894-5900.
20. Takubo K, Ohmura M, Azuma M, Nagamatsu G, Yamada W, et al. (2008) Stem cell defects in ATM-deficient undifferentiated spermatogonia through DNA damage-induced cell-cycle arrest. Cell Stem Cell 2: 170-182.
21. 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: 190-196.
22. Nakano K, Vousden KH (2001) PUMA, a novel proapoptotic gene, is induced by p53. Mol Cell 7: 683-694.
23. Yu J, Zhang L, Hwang PM, Kinzler KW, Vogelstein B (2001) PUMA induces the rapid apoptosis of colorectal cancer cells. Mol Cell 7: 673-682.
24. Yu J, Zhang L (2008) PUMA, a potent killer with or without p53. Oncogene 27: S71-83.
25. Erlacher M, Michalak EM, Kelly PN, Labi V, Niederegger H, et al. (2005) BH3-only proteins Puma and Bim are rate-limiting for gamma-radiation- and glucocorticoid-induced apoptosis of lymphoid cells in vivo. Blood 106: 4131-4138.
26. Akhtar RS, Geng Y, Klocke BJ, Latham CB, Villunger A, et al. (2006) BH3-only proapoptotic Bcl-2 family members Noxa and Puma mediate neural precursor cell death. J Neurosci 26: 7257-7264.
27. Qiu W, Carson-Walter EB, Liu H, Epperly M, Greenberger JS, et al. (2008) PUMA regulates intestinal progenitor cell radiosensitivity and gastrointestinal syndrome. Cell Stem Cell 2: 576-583.
28. Jeffers JR, Parganas E, Lee Y, Yang C, Wang J, et al. (2003) Puma is an essential mediator of p53-dependent and -independent apoptotic pathways. Cancer Cell 4: 321-328.
29. Jiang M, Wei Q, Wang J, Du Q, Yu J, et al. (2006) Regulation of PUMA-alpha by p53 in cisplatin-induced renal cell apoptosis. Oncogene 25: 4056-4066.
30. Gallenne T, Gautier F, Oliver L, Hervouet E, Nöel B, et al. (2009) Bax activation by the BH3-only protein Puma promotes cell dependence on antiapoptotic Bcl-2 family members. J Cell Biol 185: 279-290.
31. Ravi R, Bedi A (2002) Requirement of BAX for TRAIL/Apo2L-induced apoptosis of colorectal cancers: synergism with sulindac-mediated inhibition of Bcl-x(L). Cancer Res 62: 1583-1587.
32. Lamhamedi-Cherradi SE, Zheng SJ, Maguschak KA, Peschon J, Chen YH (2003) Defective thymocyte apoptosis and accelerated autoimmune diseases in TRAIL-/- mice. Nat Immunol 4: 255-260.
33. O'Flaherty J, Mei Y, Freer M, Weyman CM (2006) Signaling through the TRAIL receptor DR5/FADD pathway plays a role in the apoptosis associated with skeletal myoblast differentiation. Apoptosis 11: 2103-2113.
34. Zauli G, Secchiero P (2006) The role of the TRAIL/TRAIL receptors system in hematopoiesis and endothelial cell biology. Cytokine Growth Factor Rev 17: 245-257.
35. Brunetti G, Oranger A, Mori G, Tamma R, Di Benedetto A, et al. (2007) TRAIL is involved in human osteoclast apoptosis. Ann N Y Acad Sci 1116: 316-322.
36. Adachi M, Suematsu S, Kondo T, Ogasawara J, Tanaka T, et al. (1995) Targeted mutation in the Fas gene causes hyperplasia in peripheral lymphoid organs and liver. Nat Genet 11: 294-300.
37. Sedger LM, Glaccum MB, Schuh JC, Kanaly ST, Williamson E, et al. (2002) Characterization of the in vivo function of TNF-alpha-related apoptosis-inducing ligand, TRAIL/Apo2L, using TRAIL/Apo2L gene-deficient mice. Eur J Immunol 32: 2246-2254.
38. Villunger A, Michalak EM, Coultas L, Mullauer F, Bock G, et al. (2003) p53-and drug-induced apoptotic responses mediated by BH3-only proteins puma and noxa. Science 302: 1036-1038.
39. Donehower LA, Harvey M, Slagle BL, McArthur MJ, Montgomery CA, Jr., et al. (1999) Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356: 215-221.
40. Braghiroli L, Silvestrini B, Sorrentino C, Grima J, Mruk D, et al. (1998) Regulation of a2-macroglobulin expression in rat Sertoli cells and hepatocytes by germ cells in vitro. Biol Reprod 59: 111-123.
41. Callus BA, Moujallad DM, Silke J, Gerl R, Jabbour AM, et al. (2008) Triggering of apoptosis by Puma is determined by the threshold set by prosurvival Bcl-2 family proteins. J Mol Biol 384: 313-323.