A critical role of PUMA in maintenance of genomic integrity of murine spermatogonial stem cell precursors after genotoxic stress

Cell Research

Volumn 19, Issue 8, 2009, Pages 1018-1030

  Forand, Anne ^a,b,c   Bernardino Sgherri, J ^a,b,c  

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

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c INSERM   (France)

Author keywords

Apoptosis; Caspase; Cell death; Gonocyte; PUMA; Radiation

Indexed keywords

APOPTOSIS REGULATORY PROTEIN; CASPASE 9; CYTOCHROME C; PROTEIN P53; PUMA PROTEIN, MOUSE; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND RECEPTOR; TUMOR SUPPRESSOR PROTEIN;

ANIMAL; APOPTOSIS; ARTICLE; CYTOLOGY; GAMMA RADIATION; GENETICS; GENOMIC INSTABILITY; MALE; METABOLISM; MOUSE; MOUSE MUTANT; PHOSPHORYLATION; PHYSIOLOGY; PRENATAL DEVELOPMENT; SPERMATOGONIUM; STEM CELL; TESTIS;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CASPASE 9; CYTOCHROMES C; GAMMA RAYS; GENOMIC INSTABILITY; MALE; MICE; MICE, KNOCKOUT; PHOSPHORYLATION; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; SPERMATOGONIA; STEM CELLS; TESTIS; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

MURINAE; MUS;

EID: 68749104399     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2009.50     Document Type: Article

References (61)

1. Wyllie AH, Kerr JF, Currie AR. Cell death: the signifcance of apoptosis. Int Rev Cytol 1980; 68:251-306.
2. Muzio M. Signalling by proteolysis: death receptors induce apoptosis. Int J Clin Lab Res 1998; 28:141-147.
3. Boldin MP, Goncharov TM, Goltsev YV, Wallach D. Involvement of MACH, a novel MORT1/FADD-interacting protease, in Fas/APO-1- and TNF receptor-induced cell death. Cell 1996; 85:803-815.
4. Muzio M, Chinnaiyan AM, Kischkel FC, et al. FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death--inducing signaling complex. Cell 1996; 85:817-827.
5. Chen M, Orozco A, Spencer DM, Wang J. Activation of initiator caspases through a stable dimeric intermediate. J Biol Chem 2002; 277:50761-50767.
6. Muzio M, Stockwell BR, Stennicke HR, Salvesen GS, Dixit VM. An induced proximity model for caspase-8 activation. J Biol Chem 1998; 273:2926-2930.
7. Muzio M, Salvesen GS, Dixit VM. FLICE induced apoptosis in a cell-free system. Cleavage of caspase zymogens. J Biol Chem 1997; 272:2952-2956.
8. Irmler M, Thome M, Hahne M, et al. Inhibition of death receptor signals by cellular FLIP. Nature 1997; 388:190-195.
9. Scaffdi C, Schmitz I, Krammer PH, Peter ME. The role of c-FLIP in modulation of CD95-induced apoptosis. J Biol Chem 1999; 274:1541-1548.
10. Chang DW, Xing Z, Pan Y, et al. c-FLIP(L) is a dual function regulator for caspase-8 activation and CD95-mediated apop-tosis. EMBO J 2002; 21:3704-3714.
11. Gross A, Jockel J, Wei MC, Korsmeyer SJ. Enforced dimerization of BAX results in its translocation, mitochondrial dysfunction and apoptosis. EMBO J 1998; 17:3878-3885.
12. Srinivasula SM, Ahmad M, Fernandes-Alnemri T, Alnemri ES. Autoactivation of procaspase-9 by Apaf-1-mediated oli-gomerization. Mol Cell 1998; 1:949-957.
13. Michalak E, Villunger A, Erlacher M, Strasser A. Death squads enlisted by the tumour suppressor p53. Biochem Biophys Res Commun 2005; 331:786-798.
14. Susin SA, Lorenzo HK, Zamzami N, et al. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 1999; 397:441-446.
15. Ye H, Cande C, Stephanou NC, et al. DNA binding is required for the apoptogenic action of apoptosis inducing factor. Nat Struct Biol 2002; 9:680-684.
16. Rodriguez I, Ody C, Araki K, Garcia I, Vassalli P. An early and massive wave of germinal cell apoptosis is required for the development of functional spermatogenesis. EMBO J 1997; 16:2262-2270.
17. de Rooij DG, Grootegoed JA. Spermatogonial stem cells. Curr Opin Cell Biol 1998; 10:694-701.
18. Wang RA, Nakane PK, Koji T. Autonomous cell death of mouse male germ cells during fetal and postnatal period. Biol Reprod 1998; 58:1250-1256.
19. Furuchi T, Masuko K, Nishimune Y, Obinata M, Matsui Y. Inhibition of testicular germ cell apoptosis and differentiation in mice misexpressing Bcl-2 in spermatogonia. Development 1996; 122:1703-1709.
20. Knudson CM, Tung KS, Tourtellotte WG, Brown GA, Korsmeyer SJ. Bax-defcient mice with lymphoid hyperplasia and male germ cell death. Science 1995; 270:96-99.
21. Lizama C, Alfaro I, Reyes JG, Moreno RD. Up-regulation of CD95 (Apo-1/Fas) is associated with spermatocyte apoptosis during the frst round of spermatogenesis in the rat. Apoptosis 2007; 12:499-512.
22. Lee J, Richburg JH, Shipp EB, Meistrich ML, Boekelheide K. The Fas system, a regulator of testicular germ cell apoptosis, is differentially up-regulated in Sertoli cell versus germ cell injury of the testis. Endocrinology 1999; 140:852-858.
23. Hikim AP, Lue Y, Yamamoto CM, et al. Key apoptotic pathways for heat-induced programmed germ cell death in the testis. Endocrinology 2003; 144:3167-3175.
24. Hasegawa M, Wilson G, Russell LD, Meistrich ML. Radiation-induced cell death in the mouse testis: relationship to apoptosis. Radiat Res 1997; 147:457-467.
25. Moreno SG, Dutrillaux B, Coffgny H. High sensitivity of rat foetal germ cells to low dose-rate irradiation. Int J Radiat Biol 2001; 77:529-538.
26. Vergouwen RP, Huiskamp R, Bas RJ, et al. Radiosensitivity of testicular cells in the fetal mouse. Radiat Res 1995; 141:66-73.
27. Beumer TL, Roepers-Gajadien HL, Gademan IS, et al. The role of the tumor suppressor p53 in spermatogenesis. Cell Death Differ 1998; 5:669-677.
28. Hasegawa M, Zhang Y, Niibe H, Terry NH, Meistrich ML. Resistance of differentiating spermatogonia to radiation-induced apoptosis and loss in p53-defcient mice. Radiat Res 1998; 149:263-270.
29. Embree-Ku M, Venturini D, Boekelheide K. Fas is involved in the p53-dependent apoptotic response to ionizing radiation in mouse testis. Biol Reprod 2002; 66:1456-1461.
30. Grataroli R, Vindrieux D, Gougeon A, Benahmed M. Expression of tumor necrosis factor-alpha-related apoptosis-inducing ligand and its receptors in rat testis during development. Biol Reprod 2002; 66:1707-1715.
31. Grataroli R, Vindrieux D, Selva J, et al. Characterization of tumour necrosis factor-alpha-related apoptosis-inducing ligand and its receptors in the adult human testis. Mol Hum Reprod 2004; 10:123-128.
32. McKee CM, Ye Y, Richburg JH. Testicular germ cell sensitivity to TRAIL-induced apoptosis is dependent upon p53 expression and is synergistically enhanced by DR5 agonistic antibody treatment. Apoptosis 2006; 11:2237-2250.
33. Selby PB. X-ray-induced specifc-locus mutation rate in newborn male mice. Mutat Res 1973; 18:63-75.
34. Finnberg N, Gruber JJ, Fei P, et al. DR5 knockout mice are compromised in radiation-induced apoptosis. Mol Cell Biol 2005; 25:2000-2013.
35. Jeffers JR, Parganas E, Lee Y, et al. Puma is an essential mediator of p53-dependent and -independent apoptotic pathways. Cancer Cell 2003; 4:321-328.
36. Forand A, Fouchet P, Lahaye JB, Chicheportiche A, Habert R, Bernardino-Sgherri J. Similarities and differences in the in vivo response of mouse neonatal gonocytes and sper-matogonia to genotoxic stress. Biol Reprod 2009 Jan 14; [ DOI:10.1095/biolreprod.108.072884]
37. Komarov PG, Komarova EA, Kondratov RV, et al. A chemical inhibitor of p53 that protects mice from the side effects of cancer therapy. Science 1999; 285:1733-1737.
38. Ferber D. Cancer research. A new way to combat therapy side effects. Science 1999; 285:1651, 1653.
39. Hudson JM, Frade R, Bar-Eli M. Wild-type p53 regulates its own transcription in a cell-type specific manner. DNA Cell Biol 1995; 14:759-766.
40. Giampietri C, Petrungaro S, Coluccia P, et al. c-Flip(L) is expressed in undifferentiated mouse male germ cells. FEBS Lett 2006; 580:6109-6114.
41. Wu GS, Burns TF, Zhan Y, Alnemri ES, El-Deiry WS. Molec- ular cloning and functional analysis of the mouse homologue of the KILLER/DR5 tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) death receptor. Cancer Res 1999; 59:2770-2775.
42. Chater S, Amara S, Moussata D, et al. Differential effects of ionizing radiation and platinum-derivative chemotherapy on apoptotic pathways in testicular germ cells. Int J Radiat Biol 2007; 83:269-278.
43. Hamer G, Gademan IS, Kal HB, de Rooij DG. Role for c-Abl and p73 in the radiation response of male germ cells. Oncogene 2001; 20:4298-4304.
44. Suh EK, Yang A, Kettenbach A, et al. p63 protects the female germ line during meiotic arrest. Nature 2006; 444:624-628.
45. Petre-Lazar B, Livera G, Moreno SG, et al. The role of p63 in germ cell apoptosis in the developing testis. J Cell Physiol 2007; 210:87-98.
46. Petre-Lazar B, Moreno SG, Livera G, et al. p63 expression pattern in foetal and neonatal gonocytes after irradiation and role in the resulting apoptosis by using p63 knockout mice. Int J Radiat Biol 2006; 82:771-780.
47. Giampietri C, Petrungaro S, Klinger FG, et al. c-Flip expression and function in fetal mouse gonocytes. Faseb J 2006; 20:124-126.
48. Zhang Z, Shao S, Meistrich ML. The radiation-induced block in spermatogonial differentiation is due to damage to the somatic environment, not the germ cells. J Cell Physiol 2007; 211:149-158.
49. Thon L, Mathieu S, Kabelitz D, Adam D. The murine TRAIL receptor signals caspase-independent cell death through cera-mide. Exp Cell Res 2006; 312:3808-3821.
50. Lambrot R, Coffgny H, Pairault C, et al. High radiosensitiv-ity of germ cells in human male fetus. J Clin Endocrinol Me-tab 2007; 92:2632-2639.
51. Cory S, Huang DC, Adams JM. The Bcl-2 family: roles in cell survival and oncogenesis. Oncogene 2003; 22:8590-8607.
52. Chen L, Willis SN, Wei A, et al. Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function. Mol Cell 2005; 17:393-403.
53. Kim H, Rafuddin-Shah M, Tu HC, et al. Hierarchical regulation of mitochondrion-dependent apoptosis by BCL-2 subfamilies. Nat Cell Biol 2006; 8:1348-1358.
54. Chipuk JE, Bouchier-Hayes L, Kuwana T, Newmeyer DD, Green DR. PUMA couples the nuclear and cytoplasmic proa-poptotic function of p53. Science 2005; 309:1732-1735.
55. Villunger A, Michalak EM, Coultas L, et al. p53- and drug-induced apoptotic responses mediated by BH3-only proteins puma and noxa. Science 2003; 302:1036-1038.
56. Erster S, Mihara M, Kim RH, Petrenko O, Moll UM. In vivo mitochondrial p53 translocation triggers a rapid frst wave of cell death in response to DNA damage that can precede p53 target gene activation. Mol Cell Biol 2004; 24:6728-6741.
57. Michalak EM, Villunger A, Adams JM, Strasser A. In several cell types tumour suppressor p53 induces apoptosis largely via Puma but Noxa can contribute. Cell Death Differ 2008; 15:1019-1029
58. Western PS, Miles DC, van den Bergen JA, Burton M, Sinclair AH. Dynamic regulation of mitotic arrest in fetal male germ cells. Stem Cells 2008; 26:339-347.
59. Delbes G, Levacher C, Pairault C, et al. Estrogen receptor beta-mediated inhibition of male germ cell line development in mice by endogenous estrogens during perinatal life. Endocrinology 2004; 145:3395-3403.
60. Hanoux V, Pairault C, Bakalska M, Habert R, Livera G. Cas-pase-2 involvement during ionizing radiation-induced oocyte death in the mouse ovary. Cell Death Differ 2007; 14:671-681.
61. Abercrombie M. Estimation of nuclear population from microtome sections. Anat Rec 1946; 94:338-348.