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Reproductive Biology and Endocrinology
Published in: Reproductive Biology and Endocrinology 1/2009

Open Access 01-12-2009 | Review

Potential biological role of poly (ADP-ribose) polymerase (PARP) in male gametes

Authors: Ashok Agarwal, Reda Z Mahfouz, Rakesh K Sharma, Oli Sarkar, Devna Mangrola, Premendu P Mathur

Published in: Reproductive Biology and Endocrinology | Issue 1/2009

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Abstract

Maintaining the integrity of sperm DNA is vital to reproduction and male fertility. Sperm contain a number of molecules and pathways for the repair of base excision, base mismatches and DNA strand breaks. The presence of Poly (ADP-ribose) polymerase (PARP), a DNA repair enzyme, and its homologues has recently been shown in male germ cells, specifically during stage VII of spermatogenesis. High PARP expression has been reported in mature spermatozoa and in proven fertile men. Whenever there are strand breaks in sperm DNA due to oxidative stress, chromatin remodeling or cell death, PARP is activated. However, the cleavage of PARP by caspase-3 inactivates it and inhibits PARP's DNA-repairing abilities. Therefore, cleaved PARP (cPARP) may be considered a marker of apoptosis. The presence of higher levels of cPARP in sperm of infertile men adds a new proof for the correlation between apoptosis and male infertility. This review describes the possible biological significance of PARP in mammalian cells with the focus on male reproduction. The review elaborates on the role played by PARP during spermatogenesis, sperm maturation in ejaculated spermatozoa and the potential role of PARP as new marker of sperm damage. PARP could provide new strategies to preserve fertility in cancer patients subjected to genotoxic stresses and may be a key to better male reproductive health.
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Literature
1.
Ogawa T, Ito C, Nakamura T, Tamura Y, Yamamoto T, Noda T, Kubota Y, Toshimori K: Abnormal sperm morphology caused by defects in Sertoli cells of Cnot7 knockout mice. Archives of histology and cytology. 2004, 67 (4): 307-314. 10.1679/aohc.67.307.PubMed
2.
Suzuki-Toyota F, Ito C, Toyama Y, Maekawa M, Yao R, Noda T, Iida H, Toshimori K: Factors maintaining normal sperm tail structure during epididymal maturation studied in Gopc-/- mice. Biol Reprod. 2007, 77 (1): 71-82. 10.1095/biolreprod.106.058735.PubMed
3.
Toshimori K, Ito C, Maekawa M, Toyama Y, Suzuki-Toyota F, Saxena DK: Impairment of spermatogenesis leading to infertility. Anatomical science international/Japanese Association of Anatomists. 2004, 79 (3): 101-111.
4.
Aitken RJ, De Iuliis GN: Origins and consequences of DNA damage in male germ cells. Reproductive biomedicine online. 2007, 14 (6): 727-733.PubMed
5.
Amiri I, Sheikh N, Najafi R: Nitric oxide level in seminal plasma and its relation with sperm DNA damages. Iran Biomed J. 2007, 11 (4): 259-264.PubMed
6.
Kappes F, Fahrer J, Khodadoust MS, Tabbert A, Strasser C, Mor-Vaknin N, Moreno-Villanueva M, Burkle A, Markovitz DM, Ferrando-May E: DEK is a poly(ADP-ribose) acceptor in apoptosis and mediates resistance to genotoxic stress. Mol Cell Biol. 2008, 28 (10): 3245-3257. 10.1128/MCB.01921-07.PubMedCentralPubMed
7.
Tripathi DN, Jena GB: Astaxanthin inhibits cytotoxic and genotoxic effects of cyclophosphamide in mice germ cells. Toxicology. 2008, 248 (2-3): 96-103. 10.1016/j.tox.2008.03.015.PubMed
8.
Sakkas D, Moffatt O, Manicardi GC, Mariethoz E, Tarozzi N, Bizzaro D: Nature of DNA damage in ejaculated human spermatozoa and the possible involvement of apoptosis. Biol Reprod. 2002, 66 (4): 1061-1067. 10.1095/biolreprod66.4.1061.PubMed
9.
Patrizio P, Sanguineti F, Sakkas D: Modern andrology: from semen analysis to postgenomic studies of the male gametes. Annals of the New York Academy of Sciences. 2008, 1127: 59-63. 10.1196/annals.1434.021.PubMed
10.
Seli E, Sakkas D: Spermatozoal nuclear determinants of reproductive outcome: implications for ART. Human reproduction update. 2005, 11 (4): 337-349. 10.1093/humupd/dmi011.PubMed
11.
Tesarik J, Mendoza-Tesarik R, Mendoza C: Sperm nuclear DNA damage: update on the mechanism, diagnosis and treatment. Reproductive biomedicine online. 2006, 12 (6): 715-721.PubMed
12.
El-Domyati MM, Al-Din AB, Barakat MT, El-Fakahany HM, Honig S, Xu J, Sakkas D: The expression and distribution of deoxyribonucleic acid repair and apoptosis markers in testicular germ cells of infertile varicocele patients resembles that of old fertile men. Fertility and sterility. 2008,
13.
Laberge RM, Boissonneault G: Chromatin remodeling in spermatids: a sensitive step for the genetic integrity of the male gamete. Arch Androl. 2005, 51 (2): 125-133. 10.1080/014850190518134.PubMed
14.
Laberge RM, Boissonneault G: On the nature and origin of DNA strand breaks in elongating spermatids. Biol Reprod. 2005, 73 (2): 289-296. 10.1095/biolreprod.104.036939.PubMed
15.
Leduc F, Nkoma GB, Boissonneault G: Spermiogenesis and DNA repair: a possible etiology of human infertility and genetic disorders. Systems biology in reproductive medicine. 2008, 54 (1): 3-10. 10.1080/19396360701876823.PubMed
16.
Sharma RK, Said T, Agarwal A: Sperm DNA damage and its clinical relevance in assessing reproductive outcome. Asian journal of andrology. 2004, 6 (2): 139-148.PubMed
17.
Agarwal A, Said TM: Carnitines and male infertility. Reproductive biomedicine online. 2004, 8 (4): 376-384.PubMed
18.
Agarwal A, Ranganathan P, Kattal N, Pasqualotto F, Hallak J, Khayal S, Mascha E: Fertility after cancer: a prospective review of assisted reproductive outcome with banked semen specimens. Fertil Steril. 2004, 81 (2): 342-348. 10.1016/j.fertnstert.2003.07.021.PubMed
19.
Agarwal A, Allamaneni SS: Sperm DNA damage assessment: a test whose time has come. Fertil Steril. 2005, 84 (4): 850-853. 10.1016/j.fertnstert.2005.03.080.PubMed
20.
Agarwal A, Said TM: Oxidative stress, DNA damage and apoptosis in male infertility: a clinical approach. BJU international. 2005, 95 (4): 503-507. 10.1111/j.1464-410X.2005.05328.x.PubMed
21.
Bungum M, Humaidan P, Axmon A, Spano M, Bungum L, Erenpreiss J, Giwercman A: Sperm DNA integrity assessment in prediction of assisted reproduction technology outcome. Hum Reprod. 2007, 22 (1): 174-179. 10.1093/humrep/del326.PubMed
22.
Erenpreiss J, Spano M, Erenpreisa J, Bungum M, Giwercman A: Sperm chromatin structure and male fertility: biological and clinical aspects. Asian J Androl. 2006, 8 (1): 11-29. 10.1111/j.1745-7262.2006.00112.x.PubMed
23.
Muratori M, Luconi M, Marchiani S, Forti G, Baldi E: Molecular markers of human sperm functions. International journal of andrology. 2009, 32 (1): 25-45. 10.1111/j.1365-2605.2008.00875.x.PubMed
24.
Lewis SE, Aitken RJ: DNA damage to spermatozoa has impacts on fertilization and pregnancy. Cell Tissue Res. 2005, 322 (1): 33-41. 10.1007/s00441-005-1097-5.PubMed
25.
Tremellen K: Oxidative stress and male infertility--a clinical perspective. Human reproduction update. 2008, 14 (3): 243-258. 10.1093/humupd/dmn004.PubMed
26.
Schmid TE, Eskenazi B, Baumgartner A, Marchetti F, Young S, Weldon R, Anderson D, Wyrobek AJ: The effects of male age on sperm DNA damage in healthy non-smokers. Hum Reprod. 2007, 22 (1): 180-187. 10.1093/humrep/del338.PubMed
27.
Chitra KC, Latchoumycandane C, Mathur PP: Effect of nonylphenol on the antioxidant system in epididymal sperm of rats. Arch Toxicol. 2002, 76 (9): 545-551. 10.1007/s00204-002-0372-4.PubMed
28.
Mathur P, Saradha B, Vaithinathan S: Impact of environmental toxicants on testicular function. Immun Endoc Metab Agents Med Chem. 2008, 8: 79-90.
29.
Olsen AK, Lindeman B, Wiger R, Duale N, Brunborg G: How do male germ cells handle DNA damage?. Toxicol Appl Pharmacol. 2005, 207 (2 Suppl): 521-531. 10.1016/j.taap.2005.01.060.PubMed
30.
Rockett JC, Mapp FL, Garges JB, Luft JC, Mori C, Dix DJ: Effects of hyperthermia on spermatogenesis, apoptosis, gene expression, and fertility in adult male mice. Biol Reprod. 2001, 65 (1): 229-239. 10.1095/biolreprod65.1.229.PubMed
31.
Saradha B, Mathur P: Effect of environmental contaminants on male reproduction. Environ Toxicol Pharmacol. 2006, 21: 34-41. 10.1016/j.etap.2005.06.004.PubMed
32.
Desai N, Sabanegh E, Kim T, Agarwal A: Free Radical Theory of Aging: Implications in Male Infertility. Urology. 2009,
33.
Agarwal A, Desai NR, Ruffoli R, Carpi A: Lifestyle and testicular dysfunction: a brief update. Biomed Pharmacother. 2008, 62 (8): 550-553. 10.1016/j.biopha.2008.07.052.PubMed
34.
Gero D, Szabo C: Poly(ADP-ribose) polymerase: a new therapeutic target?. Curr Opin Anaesthesiol. 2008, 21 (2): 111-121. 10.1097/ACO.0b013e3282f63c15.PubMed
35.
Gagne JP, Moreel X, Gagne P, Labelle Y, Droit A, Chevalier-Pare M, Bourassa S, McDonald D, Hendzel MJ, Prigent C, Poirier GG: Proteomic Investigation of Phosphorylation Sites in Poly(ADP-ribose) Polymerase-1 and Poly(ADP-ribose) Glycohydrolase. J Proteome Res. 2009, 8 (2): 1014-1029. 10.1021/pr800810n.PubMed
36.
Reed AM, Fishel ML, Kelley MR: Small-molecule inhibitors of proteins involved in base excision repair potentiate the anti-tumorigenic effect of existing chemotherapeutics and irradiation. Future Oncology. 2009, 5 (5): 713-726. 10.2217/fon.09.31.PubMedCentralPubMed
37.
Di Meglio S, Tramontano F, Cimmino G, Jones R, Quesada P: Dual role for poly(ADP-ribose)polymerase-1 and -2 and poly(ADP-ribose)glycohydrolase as DNA-repair and pro-apoptotic factors in rat germinal cells exposed to nitric oxide donors. Biochim Biophys Acta. 2004, 1692 (1): 35-44. 10.1016/S0167-4889(04)00073-4.PubMed
38.
Sinha Hikim AP, Lue Y, Diaz-Romero M, Yen PH, Wang C, Swerdloff RS: Deciphering the pathways of germ cell apoptosis in the testis. J Steroid Biochem Mol Biol. 2003, 85 (2-5): 175-182. 10.1016/S0960-0760(03)00193-6.PubMed
39.
Meyer-Ficca ML, Scherthan H, Burkle A, Meyer RG: Poly(ADP-ribosyl)ation during chromatin remodeling steps in rat spermiogenesis. Chromosoma. 2005, 114 (1): 67-74. 10.1007/s00412-005-0344-6.PubMed
40.
Atorino L, Di Meglio S, Farina B, Jones R, Quesada P: Rat germinal cells require PARP for repair of DNA damage induced by gamma-irradiation and H2O2 treatment. Eur J Cell Biol. 2001, 80 (3): 222-229. 10.1078/0171-9335-00153.PubMed
41.
Sakkas D, Mariethoz E, Manicardi G, Bizzaro D, Bianchi PG, Bianchi U: Origin of DNA damage in ejaculated human spermatozoa. Rev Reprod. 1999, 4 (1): 31-37. 10.1530/ror.0.0040031.PubMed
42.
Stahl O, Eberhard J, Jepson K, Spano M, Cwikiel M, Cavallin-Stahl E, Giwercman A: Sperm DNA integrity in testicular cancer patients. Hum Reprod. 2006, 21 (12): 3199-3205. 10.1093/humrep/del292.PubMed
43.
Mahfouz RZ, Sharma RK, Said TM, Erenpreiss J, Agarwal A: Association of sperm apoptosis and DNA ploidy with sperm chromatin quality in human spermatozoa. Fertility and sterility. 2009, 91 (4): 1110-1118. 10.1016/j.fertnstert.2008.01.047.PubMed
44.
Lewis SE: Is sperm evaluation useful in predicting human fertility?. Reproduction. 2007, 134 (1): 31-40. 10.1530/REP-07-0152.PubMed
45.
Zini A, Boman JM, Belzile E, Ciampi A: Sperm DNA damage is associated with an increased risk of pregnancy loss after IVF and ICSI: systematic review and meta-analysis. Hum Reprod. 2008, 23 (12): 2663-2668. 10.1093/humrep/den321.PubMed
46.
Horak S, Olejek A, Widlak P: Sperm DNA adducts impair fertilization during ICSI but not during IVF. Folia Histochem Cytobiol. 2007, 45 (Suppl 1): S99-104.PubMed
47.
Li Z, Wang L, Cai J, Huang H: Correlation of sperm DNA damage with IVF and ICSI outcomes: a systematic review and meta-analysis. J Assist Reprod Genet. 2006, 23 (9-10): 367-376. 10.1007/s10815-006-9066-9.PubMedCentralPubMed
48.
Nasr-Esfahani MH, Salehi M, Razavi S, Anjomshoa M, Rozbahani S, Moulavi F, Mardani M: Effect of sperm DNA damage and sperm protamine deficiency on fertilization and embryo development post-ICSI. Reproductive biomedicine online. 2005, 11 (2): 198-205.PubMed
49.
Niederberger C: Efficient treatment of infertility due to sperm DNA damage by ICSI with testicular spermatozoa. J Urol. 2005, 174 (3): 1048-
50.
Paul C, Melton DW, Saunders PT: Do heat stress and deficits in DNA repair pathways have a negative impact on male fertility?. Mol Hum Reprod. 2008, 14 (1): 1-8. 10.1093/molehr/gam089.PubMed
51.
Schreiber V, Ame JC, Dolle P, Schultz I, Rinaldi B, Fraulob V, Menissier-de Murcia J, de Murcia G: Poly(ADP-ribose) polymerase-2 (PARP-2) is required for efficient base excision DNA repair in association with PARP-1 and XRCC1. J Biol Chem. 2002, 277 (25): 23028-23036. 10.1074/jbc.M202390200.PubMed
52.
Flohr C, Burkle A, Radicella JP, Epe B: Poly(ADP-ribosyl)ation accelerates DNA repair in a pathway dependent on Cockayne syndrome B protein. Nucleic Acids Res. 2003, 31 (18): 5332-5337. 10.1093/nar/gkg715.PubMedCentralPubMed
53.
Ame JC, Spenlehauer C, de Murcia G: The PARP superfamily. Bioessays. 2004, 26 (8): 882-893. 10.1002/bies.20085.PubMed
54.
Hassa PO, Hottiger MO: The diverse biological roles of mammalian PARPS, a small but powerful family of poly-ADP-ribose polymerases. Front Biosci. 2008, 13: 3046-3082. 10.2741/2909.PubMed
55.
Wacker DA, Frizzell KM, Zhang T, Kraus WL: Regulation of chromatin structure and chromatin-dependent transcription by poly(ADP-ribose) polymerase-1: possible targets for drug-based therapies. Subcell Biochem. 2007, 41: 45-69. full_text.PubMed
56.
Schreiber V, Dantzer F, Ame JC, de Murcia G: Poly(ADP-ribose): novel functions for an old molecule. Nat Rev Mol Cell Biol. 2006, 7 (7): 517-528. 10.1038/nrm1963.PubMed
57.
Augustin A, Spenlehauer C, Dumond H, Menissier-De Murcia J, Piel M, Schmit AC, Apiou F, Vonesch JL, Kock M, Bornens M, De Murcia G: PARP-3 localizes preferentially to the daughter centriole and interferes with the G1/S cell cycle progression. J Cell Sci. 2003, 116 (Pt 8): 1551-1562. 10.1242/jcs.00341.PubMed
58.
Baumgartner M, Schneider R, Auer B, Herzog H, Schweiger M, Hirsch-Kauffmann M: Fluorescence in situ mapping of the human nuclear NAD+ ADP-ribosyltransferase gene (ADPRT) and two secondary sites to human chromosomal bands 1q42, 13q34, and 14q24. Cytogenet Cell Genet. 1992, 61 (3): 172-174. 10.1159/000133400.PubMed
59.
Cherney BW, McBride OW, Chen DF, Alkhatib H, Bhatia K, Hensley P, Smulson ME: cDNA sequence, protein structure, and chromosomal location of the human gene for poly(ADP-ribose) polymerase. Proc Natl Acad Sci USA. 1987, 84 (23): 8370-8374. 10.1073/pnas.84.23.8370.PubMedCentralPubMed
60.
Woodhouse BC, Dianova II, Parsons JL, Dianov GL: Poly(ADP-ribose) polymerase-1 modulates DNA repair capacity and prevents formation of DNA double strand breaks. DNA Repair (Amst). 2008, 7 (6): 932-940. 10.1016/j.dnarep.2008.03.017.
61.
D'Amours D, Desnoyers S, D'Silva I, Poirier GG: Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem J. 1999, 342 (Pt 2): 249-268. 10.1042/0264-6021:3420249.PubMedCentralPubMed
62.
Hassa PO, Haenni SS, Elser M, Hottiger MO: Nuclear ADP-ribosylation reactions in mammalian cells: where are we today and where are we going?. Microbiol Mol Biol Rev. 2006, 70 (3): 789-829. 10.1128/MMBR.00040-05.PubMedCentralPubMed
63.
Langelier MF, Servent KM, Rogers EE, Pascal JM: A third zinc-binding domain of human poly(ADP-ribose) polymerase-1 coordinates DNA-dependent enzyme activation. The Journal of biological chemistry. 2008, 283 (7): 4105-4114. 10.1074/jbc.M708558200.PubMed
64.
Tao Z, Gao P, Hoffman DW, Liu HW: Domain C of human poly(ADP-ribose) polymerase-1 is important for enzyme activity and contains a novel zinc-ribbon motif. Biochemistry. 2008, 47 (21): 5804-5813. 10.1021/bi800018a.PubMed
65.
Schreiber V, Molinete M, Boeuf H, de Murcia G, Menissier-de Murcia J: The human poly(ADP-ribose) polymerase nuclear localization signal is a bipartite element functionally separate from DNA binding and catalytic activity. EMBO J. 1992, 11 (9): 3263-3269.PubMedCentralPubMed
66.
Pion E, Ullmann GM, Ame JC, Gerard D, de Murcia G, Bombarda E: DNA-induced dimerization of poly(ADP-ribose) polymerase-1 triggers its activation. Biochemistry. 2005, 44 (44): 14670-14681. 10.1021/bi050755o.PubMed
67.
Altmeyer M, Messner S, Hassa PO, Fey M, Hottiger MO: Molecular mechanism of poly(ADP-ribosyl)ation by PARP1 and identification of lysine residues as ADP-ribose acceptor sites. Nucleic acids research. 2009, 37 (11): 3723-3738. 10.1093/nar/gkp229.PubMedCentralPubMed
68.
Zaremba T, Ketzer P, Cole M, Coulthard S, Plummer ER, Curtin NJ: Poly(ADP-ribose) polymerase-1 polymorphisms, expression and activity in selected human tumour cell lines. Br J Cancer. 2009, 101 (2): 256-262. 10.1038/sj.bjc.6605166.PubMedCentralPubMed
69.
Ogata N, Ueda K, Kagamiyama H, Hayaishi O: ADP-ribosylation of histone H1. Identification of glutamic acid residues 2, 14, and the COOH-terminal lysine residue as modification sites. The Journal of biological chemistry. 1980, 255 (16): 7616-7620.PubMed
70.
Diefenbach J, Burkle A: Introduction to poly(ADP-ribose) metabolism. Cell Mol Life Sci. 2005, 62 (7-8): 721-730. 10.1007/s00018-004-4503-3.PubMed
71.
Mendoza-Alvarez H, Alvarez-Gonzalez R: Poly(ADP-ribose) polymerase is a catalytic dimer and the automodification reaction is intermolecular. J Biol Chem. 1993, 268 (30): 22575-22580.PubMed
72.
Adamietz P, Rudolph A: ADP-ribosylation of nuclear proteins in vivo. Identification of histone H2B as a major acceptor for mono- and poly(ADP-ribose) in dimethyl sulfate-treated hepatoma AH 7974 cells. J Biol Chem. 1984, 259 (11): 6841-6846.PubMed
73.
Poirier GG, de Murcia G, Jongstra-Bilen J, Niedergang C, Mandel P: Poly(ADP-ribosyl)ation of polynucleosomes causes relaxation of chromatin structure. Proc Natl Acad Sci USA. 1982, 79 (11): 3423-3427. 10.1073/pnas.79.11.3423.PubMedCentralPubMed
74.
Atorino L, Alvarez-Gonzalez R, Cardone A, Lepore I, Farina B, Quesada P: Metabolic changes in the poly(ADP-ribosyl)ation pathway of differentiating rat germinal cells. Arch Biochem Biophys. 2000, 381 (1): 111-118. 10.1006/abbi.2000.1926.PubMed
75.
Mendoza-Alvarez H, Alvarez-Gonzalez R: Regulation of p53 sequence-specific DNA-binding by covalent poly(ADP-ribosyl)ation. J Biol Chem. 2001, 276 (39): 36425-36430. 10.1074/jbc.M105215200.PubMed
76.
Yoshihara K, Itaya A, Tanaka Y, Ohashi Y, Ito K, Teraoka H, Tsukada K, Matsukage A, Kamiya T: Inhibition of DNA polymerase alpha, DNA polymerase beta, terminal deoxynucleotidyl transferase, and DNA ligase II by poly(ADP-ribosyl)ation reaction in vitro. Biochem Biophys Res Commun. 1985, 128 (1): 61-67. 10.1016/0006-291X(85)91644-4.PubMed
77.
Scovassi AI, Mariani C, Negroni M, Negri C, Bertazzoni U: ADP-ribosylation of nonhistone proteins in HeLa cells: modification of DNA topoisomerase II. Exp Cell Res. 1993, 206 (1): 177-181. 10.1006/excr.1993.1135.PubMed
78.
Kameoka M, Ota K, Tetsuka T, Tanaka Y, Itaya A, Okamoto T, Yoshihara K: Evidence for regulation of NF-kappaB by poly(ADP-ribose) polymerase. Biochem J. 2000, 346 (Pt 3): 641-649. 10.1042/0264-6021:3460641.PubMedCentralPubMed
79.
Huang K, Tidyman WE, Le KU, Kirsten E, Kun E, Ordahl CP: Analysis of nucleotide sequence-dependent DNA binding of poly(ADP-ribose) polymerase in a purified system. Biochemistry. 2004, 43 (1): 217-223. 10.1021/bi0301800.PubMed
80.
Bauer PI, Kenesi E, Mendeleyev J, Kun E: The influence of ATP on poly(ADP-ribose) metabolism. Int J Mol Med. 2005, 16 (2): 321-324.PubMed
81.
Kolthur-Seetharam U, Dantzer F, McBurney MW, de Murcia G, Sassone-Corsi P: Control of AIF-mediated cell death by the functional interplay of SIRT1 and PARP-1 in response to DNA damage. Cell Cycle. 2006, 5 (8): 873-877.PubMed
82.
Ermak G, Davies KJ: Calcium and oxidative stress: from cell signaling to cell death. Mol Immunol. 2002, 38 (10): 713-721. 10.1016/S0161-5890(01)00108-0.PubMed
83.
Schwerdtle T, Hamann I, Jahnke G, Walter I, Richter C, Parsons JL, Dianov GL, Hartwig A: Impact of copper on the induction and repair of oxidative DNA damage, poly(ADP-ribosyl)ation and PARP-1 activity. Mol Nutr Food Res. 2007, 51 (2): 201-210. 10.1002/mnfr.200600107.PubMed
84.
Midorikawa R, Takei Y, Hirokawa N: KIF4 motor regulates activity-dependent neuronal survival by suppressing PARP-1 enzymatic activity. Cell. 2006, 125 (2): 371-383. 10.1016/j.cell.2006.02.039.PubMed
85.
Mocchegiani E, Muzzioli M, Giacconi R, Cipriano C, Gasparini N, Franceschi C, Gaetti R, Cavalieri E, Suzuki H: Metallothioneins/PARP-1/IL-6 interplay on natural killer cell activity in elderly: parallelism with nonagenarians and old infected humans. Effect of zinc supply. Mech Ageing Dev. 2003, 124 (4): 459-468. 10.1016/S0047-6374(03)00023-X.PubMed
86.
Kun E, Kirsten E, Ordahl CP: Coenzymatic activity of randomly broken or intact double-stranded DNAs in auto and histone H1 trans-poly(ADP-ribosylation), catalyzed by poly(ADP-ribose) polymerase (PARP I). The Journal of biological chemistry. 2002, 277 (42): 39066-39069. 10.1074/jbc.C200410200.PubMed
87.
Geraets L, Moonen HJ, Wouters EF, Bast A, Hageman GJ: Caffeine metabolites are inhibitors of the nuclear enzyme poly(ADP-ribose)polymerase-1 at physiological concentrations. Biochem Pharmacol. 2006, 72 (7): 902-910. 10.1016/j.bcp.2006.06.023.PubMed
88.
Kauppinen TM, Chan WY, Suh SW, Wiggins AK, Huang EJ, Swanson RA: Direct phosphorylation and regulation of poly(ADP-ribose) polymerase-1 by extracellular signal-regulated kinases 1/2. Proc Natl Acad Sci USA. 2006, 103 (18): 7136-7141. 10.1073/pnas.0508606103.PubMedCentralPubMed
89.
Ariumi Y, Masutani M, Copeland TD, Mimori T, Sugimura T, Shimotohno K, Ueda K, Hatanaka M, Noda M: Suppression of the poly(ADP-ribose) polymerase activity by DNA-dependent protein kinase in vitro. Oncogene. 1999, 18 (32): 4616-4625. 10.1038/sj.onc.1202823.PubMed
90.
Audebert M, Salles B, Calsou P: Effect of double-strand break DNA sequence on the PARP-1 NHEJ pathway. Biochem Biophys Res Commun. 2008, 369 (3): 982-988. 10.1016/j.bbrc.2007.11.132.PubMed
91.
Chen J, Tomkinson AE, Ramos W, Mackey ZB, Danehower S, Walter CA, Schultz RA, Besterman JM, Husain I: Mammalian DNA ligase III: molecular cloning, chromosomal localization, and expression in spermatocytes undergoing meiotic recombination. Mol Cell Biol. 1995, 15 (10): 5412-5422.PubMedCentralPubMed
92.
Kotoglou P, Kalaitzakis A, Vezyraki P, Tzavaras T, Michalis LK, Dantzer F, Jung JU, Angelidis C: Hsp70 translocates to the nuclei and nucleoli, binds to XRCC1 and PARP-1, and protects HeLa cells from single-strand DNA breaks. Cell Stress Chaperones. 2009, 14 (4): 391-406. 10.1007/s12192-008-0093-6.PubMedCentralPubMed
93.
Leppard JB, Dong Z, Mackey ZB, Tomkinson AE: Physical and functional interaction between DNA ligase IIIalpha and poly(ADP-Ribose) polymerase 1 in DNA single-strand break repair. Mol Cell Biol. 2003, 23 (16): 5919-5927. 10.1128/MCB.23.16.5919-5927.2003.PubMedCentralPubMed
94.
Dantzer F, de La Rubia G, Menissier-De Murcia J, Hostomsky Z, de Murcia G, Schreiber V: Base excision repair is impaired in mammalian cells lacking Poly(ADP-ribose) polymerase-1. Biochemistry. 2000, 39 (25): 7559-7569. 10.1021/bi0003442.PubMed
95.
Parsons JL, Dianova II, Allinson SL, Dianov GL: Poly(ADP-ribose) polymerase-1 protects excessive DNA strand breaks from deterioration during repair in human cell extracts. FEBS J. 2005, 272 (8): 2012-2021. 10.1111/j.1742-4658.2005.04628.x.PubMed
96.
Sagan D, Muller R, Kroger C, Hematulin A, Mortl S, Eckardt-Schupp F: The DNA repair protein NBS1 influences the base excision repair pathway. Carcinogenesis. 2009, 30 (3): 408-415. 10.1093/carcin/bgp004.PubMed
97.
Quenet D, El Ramy R, Schreiber V, Dantzer F: The role of poly(ADP-ribosyl)ation in epigenetic events. Int J Biochem Cell Biol. 2009, 41 (1): 60-65. 10.1016/j.biocel.2008.07.023.PubMed
98.
Mortusewicz O, Ame JC, Schreiber V, Leonhardt H: Feedback-regulated poly(ADP-ribosyl)ation by PARP-1 is required for rapid response to DNA damage in living cells. Nucleic Acids Res. 2007, 35 (22): 7665-7675. 10.1093/nar/gkm933.PubMedCentralPubMed
99.
Ullrich O, Reinheckel T, Sitte N, Hass R, Grune T, Davies KJ: Poly-ADP ribose polymerase activates nuclear proteasome to degrade oxidatively damaged histones. Proc Natl Acad Sci USA. 1999, 96 (11): 6223-6228. 10.1073/pnas.96.11.6223.PubMedCentralPubMed
100.
Mathieu J, Flexor M, Lanotte M, Besancon F: A PARP-1/JNK1 cascade participates in the synergistic apoptotic effect of TNFalpha and all-trans retinoic acid in APL cells. Oncogene. 2008, 27 (24): 3361-3370. 10.1038/sj.onc.1210997.PubMed
101.
Heeres JT, Hergenrother PJ: Poly(ADP-ribose) makes a date with death. Curr Opin Chem Biol. 2007, 11 (6): 644-653. 10.1016/j.cbpa.2007.08.038.PubMed
102.
Oliver FJ, Menissier-de Murcia J, Nacci C, Decker P, Andriantsitohaina R, Muller S, de la Rubia G, Stoclet JC, de Murcia G: Resistance to endotoxic shock as a consequence of defective NF-kappaB activation in poly (ADP-ribose) polymerase-1 deficient mice. EMBO J. 1999, 18 (16): 4446-4454. 10.1093/emboj/18.16.4446.PubMedCentralPubMed
103.
Zerfaoui M, Suzuki Y, Naura AS, Hans CP, Nichols C, Boulares AH: Nuclear translocation of p65 NF-kappaB is sufficient for VCAM-1, but not ICAM-1, expression in TNF-stimulated smooth muscle cells: Differential requirement for PARP-1 expression and interaction. Cell Signal. 2008, 20 (1): 186-194. 10.1016/j.cellsig.2007.10.007.PubMedCentralPubMed
104.
Kaufmann SH, Desnoyers S, Ottaviano Y, Davidson NE, Poirier GG: Specific proteolytic cleavage of poly(ADP-ribose) polymerase: an early marker of chemotherapy-induced apoptosis. Cancer Res. 1993, 53 (17): 3976-3985.PubMed
105.
D'Amours D, Sallmann FR, Dixit VM, Poirier GG: Gain-of-function of poly(ADP-ribose) polymerase-1 upon cleavage by apoptotic proteases: implications for apoptosis. J Cell Sci. 2001, 114 (Pt 20): 3771-3778.PubMed
106.
Yu SW, Wang H, Poitras MF, Coombs C, Bowers WJ, Federoff HJ, Poirier GG, Dawson TM, Dawson VL: Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science. 2002, 297 (5579): 259-263. 10.1126/science.1072221.PubMed
107.
Tramontano F, Malanga M, Quesada P: Differential contribution of poly(ADP-ribose)polymerase-1 and -2 (PARP-1 and -2) to the poly(ADP-ribosyl)ation reaction in rat primary spermatocytes. Mol Hum Reprod. 2007, 13 (11): 821-828. 10.1093/molehr/gam062.PubMed
108.
Tulin A, Chinenov Y, Spradling A: Regulation of chromatin structure and gene activity by poly(ADP-ribose) polymerases. Curr Top Dev Biol. 2003, 56: 55-83. full_text.PubMed
109.
Berger NA, Sims JL, Catino DM, Berger SJ: Poly(ADP-ribose) polymerase mediates the suicide response to massive DNA damage: studies in normal and DNA-repair defective cells. Princess Takamatsu Symp. 1983, 13: 219-226.PubMed
110.
Andrabi SA, Dawson TM, Dawson VL: Mitochondrial and Nuclear Cross Talk in Cell Death Parthanatos. Annals of the New York Academy of Sciences. 2008, 1147: 233-241.PubMedCentralPubMed
111.
Kanai M, Uchida M, Hanai S, Uematsu N, Uchida K, Miwa M: Poly(ADP-ribose) polymerase localizes to the centrosomes and chromosomes. Biochem Biophys Res Commun. 2000, 278 (2): 385-389. 10.1006/bbrc.2000.3801.PubMed
112.
Chang P, Jacobson MK, Mitchison TJ: Poly(ADP-ribose) is required for spindle assembly and structure. Nature. 2004, 432 (7017): 645-649. 10.1038/nature03061.PubMed
113.
Kanai M, Tong WM, Sugihara E, Wang ZQ, Fukasawa K, Miwa M: Involvement of poly(ADP-Ribose) polymerase 1 and poly(ADP-Ribosyl)ation in regulation of centrosome function. Mol Cell Biol. 2003, 23 (7): 2451-2462. 10.1128/MCB.23.7.2451-2462.2003.PubMedCentralPubMed
114.
Earle E, Saxena A, MacDonald A, Hudson DF, Shaffer LG, Saffery R, Cancilla MR, Cutts SM, Howman E, Choo KH: Poly(ADP-ribose) polymerase at active centromeres and neocentromeres at metaphase. Hum Mol Genet. 2000, 9 (2): 187-194. 10.1093/hmg/9.2.187.PubMed
115.
Saxena A, Wong LH, Kalitsis P, Earle E, Shaffer LG, Choo KH: Poly(ADP-ribose) polymerase 2 localizes to mammalian active centromeres and interacts with PARP-1, Cenpa, Cenpb and Bub3, but not Cenpc. Hum Mol Genet. 2002, 11 (19): 2319-2329. 10.1093/hmg/11.19.2319.PubMed
116.
Faraone-Mennella MR: Chromatin architecture and functions: the role(s) of poly(ADP-RIBOSE) polymerase and poly(ADPribosyl)ation of nuclear proteins. Biochem Cell Biol. 2005, 83 (3): 396-404. 10.1139/o05-042.PubMed
117.
Kraus WL, Lis JT: PARP goes transcription. Cell. 2003, 113 (6): 677-683. 10.1016/S0092-8674(03)00433-1.PubMed
118.
Kraus WL: Transcriptional control by PARP-1: chromatin modulation, enhancer-binding, coregulation, and insulation. Curr Opin Cell Biol. 2008, 20 (3): 294-302. 10.1016/j.ceb.2008.03.006.PubMedCentralPubMed
119.
Quenet D, Gasser V, Fouillen L, Cammas F, Sanglier-Cianferani S, Losson R, Dantzer F: The histone subcode: poly(ADP-ribose) polymerase-1 (Parp-1) and Parp-2 control cell differentiation by regulating the transcriptional intermediary factor TIF1beta and the heterochromatin protein HP1alpha. FASEB J. 2008, 22 (11): 3853-3865. 10.1096/fj.08-113464.PubMed
120.
Huang JY, Chen WH, Chang YL, Wang HT, Chuang WT, Lee SC: Modulation of nucleosome-binding activity of FACT by poly(ADP-ribosyl)ation. Nucleic Acids Res. 2006, 34 (8): 2398-2407. 10.1093/nar/gkl241.PubMedCentralPubMed
121.
Poirier GG, de Murcia G, Jongstra-Bilen J, Niedergang C, Mandel P: Poly(ADP-ribosyl)ation of polynucleosomes causes relaxation of chromatin structure. Proc Natl Acad Sci USA. 1982, 79 (11): 3423-3427. 10.1073/pnas.79.11.3423.PubMedCentralPubMed
122.
Rouleau M, Aubin RA, Poirier GG: Poly(ADP-ribosyl)ated chromatin domains: access granted. J Cell Sci. 2004, 117 (Pt 6): 815-825. 10.1242/jcs.01080.PubMed
123.
Krishnakumar R, Gamble MJ, Frizzell KM, Berrocal JG, Kininis M, Kraus WL: Reciprocal binding of PARP-1 and histone H1 at promoters specifies transcriptional outcomes. Science. 2008, 319 (5864): 819-821. 10.1126/science.1149250.PubMed
124.
Oei SL, Griesenbeck J, Schweiger M, Ziegler M: Regulation of RNA polymerase II-dependent transcription by poly(ADP-ribosyl)ation of transcription factors. The Journal of biological chemistry. 1998, 273 (48): 31644-31647. 10.1074/jbc.273.48.31644.PubMed
125.
Yazawa T, Fujimoto K, Yamamoto T, Abe SI: Caspase activity in newt spermatogonial apoptosis induced by prolactin and cycloheximide. Mol Reprod Dev. 2001, 59 (2): 209-214. 10.1002/mrd.1024.PubMed
126.
Ye K: PARP inhibitor tilts cell death from necrosis to apoptosis in cancer cells. Cancer Biol Ther. 2008, 7 (6): 942-944.PubMed
127.
Mizuno K, Hayashi Y, Kojima Y, Nakane A, Tozawa K, Kohri K: Activation of NF-kappaB associated with germ cell apoptosis in testes of experimentally induced cryptorchid rat model. Urology. 2009, 73 (2): 389-393. 10.1016/j.urology.2008.09.019.PubMed
128.
Varisli O, Uguz C, Agca C, Agca Y: Various physical stress factors on rat sperm motility, integrity of acrosome, and plasma membrane. J Androl. 2009, 30 (1): 75-86. 10.2164/jandrol.107.004333.PubMed
129.
Tanori M, Mancuso M, Pasquali E, Leonardi S, Rebessi S, Di Majo V, Guilly MN, Giangaspero F, Covelli V, Pazzaglia S, Saran A: PARP-1 cooperates with Ptc1 to suppress medulloblastoma and basal cell carcinoma. Carcinogenesis. 2008, 29 (10): 1911-1919. 10.1093/carcin/bgn174.PubMed
130.
Spina-Purrello V, Patti D, Giuffrida-Stella AM, Nicoletti VG: Parp and cell death or protection in rat primary astroglial cell cultures under LPS/IFNgamma induced proinflammatory conditions. Neurochem Res. 2008, 33 (12): 2583-2592. 10.1007/s11064-008-9835-1.PubMed
131.
Yu W, Ginjala V, Pant V, Chernukhin I, Whitehead J, Docquier F, Farrar D, Tavoosidana G, Mukhopadhyay R, Kanduri C, Oshimura M, Feinberg AP, Lobanenkov V, Klenova E, Ohlsson R: Poly(ADP-ribosyl)ation regulates CTCF-dependent chromatin insulation. Nat Genet. 2004, 36 (10): 1105-1110. 10.1038/ng1426.PubMed
132.
Thornberry NA, Lazebnik Y: Caspases: enemies within. Science. 1998, 281 (5381): 1312-1316. 10.1126/science.281.5381.1312.PubMed
133.
Ullrich O, Reinheckel T, Sitte N, Hass R, Grune T, Davies KJ: Poly-ADP ribose polymerase activates nuclear proteasome to degrade oxidatively damaged histones. Proc Natl Acad Sci USA. 1999, 96 (11): 6223-6228. 10.1073/pnas.96.11.6223.PubMedCentralPubMed
134.
Klenova E, Ohlsson R: Poly(ADP-ribosyl)ation and epigenetics. Is CTCF PARt of the plot?. Cell Cycle. 2005, 4 (1): 96-101.PubMed
135.
Guastafierro T, Cecchinelli B, Zampieri M, Reale A, Riggio G, Sthandier O, Zupi G, Calabrese L, Caiafa P: CCCTC-binding factor activates PARP-1 affecting DNA methylation machinery. The Journal of biological chemistry. 2008, 283 (32): 21873-21880. 10.1074/jbc.M801170200.PubMedCentralPubMed
136.
Winstall E, Affar EB, Shah R, Bourassa S, Scovassi IA, Poirier GG: Preferential perinuclear localization of poly(ADP-ribose) glycohydrolase. Exp Cell Res. 1999, 251 (2): 372-378. 10.1006/excr.1999.4594.PubMed
137.
Davidovic L, Vodenicharov M, Affar EB, Poirier GG: Importance of poly(ADP-ribose) glycohydrolase in the control of poly(ADP-ribose) metabolism. Exp Cell Res. 2001, 268 (1): 7-13. 10.1006/excr.2001.5263.PubMed
138.
Koh DW, Lawler AM, Poitras MF, Sasaki M, Wattler S, Nehls MC, Stoger T, Poirier GG, Dawson VL, Dawson TM: Failure to degrade poly(ADP-ribose) causes increased sensitivity to cytotoxicity and early embryonic lethality. Proc Natl Acad Sci USA. 2004, 101 (51): 17699-17704. 10.1073/pnas.0406182101.PubMedCentralPubMed
139.
Blenn C, Althaus FR, Malanga M: Poly(ADP-ribose) glycohydrolase silencing protects against H2O2-induced cell death. Biochem J. 2006, 396 (3): 419-429. 10.1042/BJ20051696.PubMedCentralPubMed
140.
Fisher AE, Hochegger H, Takeda S, Caldecott KW: Poly(ADP-ribose) polymerase 1 accelerates single-strand break repair in concert with poly(ADP-ribose) glycohydrolase. Mol Cell Biol. 2007, 27 (15): 5597-5605. 10.1128/MCB.02248-06.PubMedCentralPubMed
141.
Baum JS, St George JP, McCall K: Programmed cell death in the germline. Semin Cell Dev Biol. 2005, 16 (2): 245-259. 10.1016/j.semcdb.2004.12.008.PubMed
142.
Print CG, Loveland KL: Germ cell suicide: new insights into apoptosis during spermatogenesis. Bioessays. 2000, 22 (5): 423-430. 10.1002/(SICI)1521-1878(200005)22:5<423::AID-BIES4>3.0.CO;2-0.PubMed
143.
Codelia VA, Cisternas P, Moreno RD: Relevance of caspase activity during apoptosis in pubertal rat spermatogenesis. Mol Reprod Dev. 2008, 75 (5): 881-889. 10.1002/mrd.20822.PubMed
144.
Ohashi Y, Ueda K, Kawaichi M, Hayaishi O: Activation of DNA ligase by poly(ADP-ribose) in chromatin. Proc Natl Acad Sci USA. 1983, 80 (12): 3604-3607. 10.1073/pnas.80.12.3604.PubMedCentralPubMed
145.
Spina-Purrello V, Patti D, Giuffrida-Stella AM, Nicoletti VG: Parp and Cell Death or Protection in Rat Primary Astroglial Cell Cultures Under LPS/IFNgamma Induced Proinflammatory Conditions. Neurochem Res. 2008
146.
Tewari M, Quan LT, O'Rourke K, Desnoyers S, Zeng Z, Beidler DR, Poirier GG, Salvesen GS, Dixit VM: Yama/CPP32 beta, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell. 1995, 81 (5): 801-809. 10.1016/0092-8674(95)90541-3.PubMed
147.
Pacher P, Szabo C: Role of the peroxynitrite-poly(ADP-ribose) polymerase pathway in human disease. Am J Pathol. 2008, 173 (1): 2-13. 10.2353/ajpath.2008.080019.PubMedCentralPubMed
148.
Duriez PJ, Shah GM: Cleavage of poly(ADP-ribose) polymerase: a sensitive parameter to study cell death. Biochem Cell Biol. 1997, 75 (4): 337-349. 10.1139/bcb-75-4-337.PubMed
149.
Hadziselimovic F, Geneto R, Emmons LR: Increased apoptosis in the contralateral testes of patients with testicular torsion as a factor for infertility. J Urol. 1998, 160 (3 Pt 2): 1158-1160.PubMed
150.
Lin WW, Lamb DJ, Wheeler TM, Lipshultz LI, Kim ED: In situ end-labeling of human testicular tissue demonstrates increased apoptosis in conditions of abnormal spermatogenesis. Fertil Steril. 1997, 68 (6): 1065-1069. 10.1016/S0015-0282(97)00372-5.PubMed
151.
Kim SK, Yoon YD, Park YS, Seo JT, Kim JH: Involvement of the Fas-Fas ligand system and active caspase-3 in abnormal apoptosis in human testes with maturation arrest and Sertoli cell-only syndrome. Fertility and sterility. 2007, 87 (3): 547-553. 10.1016/j.fertnstert.2006.07.1524.PubMed
152.
Tesarik J, Greco E, Cohen-Bacrie P, Mendoza C: Germ cell apoptosis in men with complete and incomplete spermiogenesis failure. Mol Hum Reprod. 1998, 4 (8): 757-762. 10.1093/molehr/4.8.757.PubMed
153.
Maymon BB, Cohen-Armon M, Yavetz H, Yogev L, Lifschitz-Mercer B, Kleiman SE, Botchan A, Hauser R, Paz G: Role of poly(ADP-ribosyl)ation during human spermatogenesis. Fertil Steril. 2006, 86 (5): 1402-1407. 10.1016/j.fertnstert.2006.03.063.PubMed
154.
Dantzer F, Ame JC, Schreiber V, Nakamura J, Menissier-de Murcia J, de Murcia G: Poly(ADP-ribose) polymerase-1 activation during DNA damage and repair. Methods Enzymol. 2006, 409: 493-510. 10.1016/S0076-6879(05)09029-4.PubMed
155.
Hikim AP, Vera Y, Vernet D, Castanares M, Diaz-Romero M, Ferrini M, Swerdloff RS, Gonzalez-Cadavid NF, Wang C: Involvement of nitric oxide-mediated intrinsic pathway signaling in age-related increase in germ cell apoptosis in male Brown-Norway rats. J Gerontol A Biol Sci Med Sci. 2005, 60 (6): 702-708.PubMed
156.
Miura M, Sasagawa I, Suzuki Y, Nakada T, Fujii J: Apoptosis and expression of apoptosis-related genes in the mouse testis following heat exposure. Fertil Steril. 2002, 77 (4): 787-793. 10.1016/S0015-0282(01)03255-1.PubMed
157.
Aguilar-Quesada R, Munoz-Gamez JA, Martin-Oliva D, Peralta-Leal A, Quiles-Perez R, Rodriguez-Vargas JM, de Almodovar MR, Conde C, Ruiz-Extremera A, Oliver FJ: Modulation of transcription by PARP-1: consequences in carcinogenesis and inflammation. Curr Med Chem. 2007, 14 (11): 1179-1187. 10.2174/092986707780597998.PubMed
158.
Pentikainen V, Suomalainen L, Erkkila K, Martelin E, Parvinen M, Pentikainen MO, Dunkel L: Nuclear factor-kappa B activation in human testicular apoptosis. Am J Pathol. 2002, 160 (1): 205-218.PubMedCentralPubMed
159.
Chiarugi A: Poly(ADP-ribosyl)ation and stroke. Pharmacol Res. 2005, 52 (1): 15-24. 10.1016/j.phrs.2005.02.018.PubMed
160.
Di Meglio S, Denegri M, Vallefuoco S, Tramontano F, Scovassi AI, Quesada P: Poly(ADPR) polymerase-1 and poly(ADPR) glycohydrolase level and distribution in differentiating rat germinal cells. Mol Cell Biochem. 2003, 248 (1-2): 85-91. 10.1023/A:1024136927637.PubMed
161.
Quesada P, Atorino L, Cardone A, Ciarcia G, Farina B: Poly(ADPribosyl)ation system in rat germinal cells at different stages of differentiation. Exp Cell Res. 1996, 226 (1): 183-190. 10.1006/excr.1996.0217.PubMed
162.
Wouters-Tyrou D, Martinage A, Chevaillier P, Sautiere P: Nuclear basic proteins in spermiogenesis. Biochimie. 1998, 80 (2): 117-128. 10.1016/S0300-9084(98)80018-7.PubMed
163.
Ward WS, Coffey DS: DNA packaging and organization in mammalian spermatozoa: comparison with somatic cells. Biol Reprod. 1991, 44 (4): 569-574. 10.1095/biolreprod44.4.569.PubMed
164.
Marcon L, Boissonneault G: Transient DNA strand breaks during mouse and human spermiogenesis new insights in stage specificity and link to chromatin remodeling. Biol Reprod. 2004, 70 (4): 910-918. 10.1095/biolreprod.103.022541.PubMed
165.
Meyer-Ficca ML, Lonchar J, Credidio C, Ihara M, Li Y, Wang ZQ, Meyer RG: Disruption of poly(ADP-ribose) homeostasis affects spermiogenesis and sperm chromatin integrity in mice. Biology of reproduction. 2009, 81 (1): 46-55. 10.1095/biolreprod.108.075390.PubMedCentralPubMed
166.
Kaipia A, Toppari J, Mali P, Kangasniemi M, Alcivar AA, Hecht NB, Parvinen M: Stage- and cell-specific expression of the ornithine decarboxylase gene during rat and mouse spermatogenesis. Molecular and cellular endocrinology. 1990, 73 (1): 45-52. 10.1016/0303-7207(90)90043-8.PubMed
167.
Taylor SL, Weng SL, Fox P, Duran EH, Morshedi MS, Oehninger S, Beebe SJ: Somatic cell apoptosis markers and pathways in human ejaculated sperm: potential utility as indicators of sperm quality. Molecular human reproduction. 2004, 10 (11): 825-834. 10.1093/molehr/gah099.PubMed
168.
Jha R, Agarwal A, Mahfouz R, Paasch U, Grunewald S, Sabanegh E, Yadav SP, Sharma R: Determination of Poly (ADP-ribose) polymerase (PARP) homologues in human ejaculated sperm and its correlation with sperm maturation. Fertility and sterility. 2009, 91 (3): 782-790. 10.1016/j.fertnstert.2007.12.079.PubMed
169.
Benchaib M, Lornage J, Mazoyer C, Lejeune H, Salle B, Francois Guerin J: Sperm deoxyribonucleic acid fragmentation as a prognostic indicator of assisted reproductive technology outcome. Fertil Steril. 2007, 87 (1): 93-100. 10.1016/j.fertnstert.2006.05.057.PubMed
170.
Kopeika J, Kopeika E, Zhang T, Rawson DM, Holt WV: Effect of DNA repair inhibitor (3-aminobenzamide) on genetic stability of loach (Misgurnus fossilis) embryos derived from cryopreserved sperm. Theriogenology. 2004, 61 (9): 1661-1673. 10.1016/j.theriogenology.2003.09.010.PubMed
171.
Meseguer M, Santiso R, Garrido N, Fernandez JL: The effect of cancer on sperm DNA fragmentation as measured by the sperm chromatin dispersion test. Fertil Steril. 2008, 90 (1): 225-227. 10.1016/j.fertnstert.2007.06.026.PubMed
172.
O'Flaherty C, Vaisheva F, Hales BF, Chan P, Robaire B: Characterization of sperm chromatin quality in testicular cancer and Hodgkin's lymphoma patients prior to chemotherapy. Hum Reprod. 2008, 23 (5): 1044-1052. 10.1093/humrep/den081.PubMed
173.
Edelstein A, Yavetz H, Kleiman SE, Botchan A, Hauser R, Paz G, Yogev L: Deoxyribonucleic acid-damaged sperm in cryopreserved-thawed specimens from cancer patients and healthy men. Fertil Steril. 2008, 90 (1): 205-208. 10.1016/j.fertnstert.2007.05.060.PubMed
174.
Spermon JR, Ramos L, Wetzels AM, Sweep CG, Braat DD, Kiemeney LA, Witjes JA: Sperm integrity pre- and post-chemotherapy in men with testicular germ cell cancer. Hum Reprod. 2006, 21 (7): 1781-1786. 10.1093/humrep/del084.PubMed
175.
Mitchell RT, Saunders PT, Sharpe RM, Kelnar CJ, Wallace WH: Male fertility and strategies for fertility preservation following childhood cancer treatment. Endocr Dev. 2009, 15: 101-134. full_text.PubMed
176.
Wang T, Simbulan-Rosenthal CM, Smulson ME, Chock PB, Yang DC: Polyubiquitylation of PARP-1 through ubiquitin K48 is modulated by activated DNA, NAD+, and dipeptides. J Cell Biochem. 2008, 104 (1): 318-328. 10.1002/jcb.21624.PubMed
177.
Wang Y, Virji AS, Howard P, Sayani Y, Zhang J, Achu P, McArthur C: Detection of cleaved alpha-fodrin autoantigen in Sjogren's syndrome: apoptosis and co-localisation of cleaved alpha-fodrin with activated caspase-3 and cleaved poly(ADP-ribose) polymerase (PARP) in labial salivary glands. Arch Oral Biol. 2006, 51 (7): 558-566. 10.1016/j.archoralbio.2005.11.008.PubMed
178.
Olsen GJ: The history of life. Nat Genet. 2001, 28 (3): 197-198. 10.1038/90014.PubMed
179.
Kovtun IV, McMurray CT: Trinucleotide expansion in haploid germ cells by gap repair. Nat Genet. 2001, 27 (4): 407-411. 10.1038/86906.PubMed
180.
Kovtun IV, McMurray CT: Features of trinucleotide repeat instability in vivo. Cell research. 2008, 18 (1): 198-213. 10.1038/cr.2008.5.PubMed
181.
Kovtun IV, Welch G, Guthrie HD, Hafner KL, McMurray CT: CAG repeat lengths in X- and Y-bearing sperm indicate that gender bias during transmission of Huntington's disease gene is determined in the embryo. J Biol Chem. 2004, 279 (10): 9389-9391. 10.1074/jbc.M313080200.PubMed
182.
Trushina E, Heldebrant MP, Perez-Terzic CM, Bortolon R, Kovtun IV, Badger JD, Terzic A, Estevez A, Windebank AJ, Dyer RB, Yao J, McMurray CT: Microtubule destabilization and nuclear entry are sequential steps leading to toxicity in Huntington's disease. Proc Natl Acad Sci USA. 2003, 100 (21): 12171-12176. 10.1073/pnas.2034961100.PubMedCentralPubMed
183.
Rybaczek D, Bodys A, Maszewski J: H2AX foci in late S/G2- and M-phase cells after hydroxyurea- and aphidicolin-induced DNA replication stress in Vicia. Histochemistry and cell biology. 2007, 128 (3): 227-241. 10.1007/s00418-007-0311-9.PubMed
184.
Leduc F, Maquennehan V, Nkoma GB, Boissonneault G: DNA damage response during chromatin remodeling in elongating spermatids of mice. Biol Reprod. 2008, 78 (2): 324-332. 10.1095/biolreprod.107.064162.PubMed
185.
Quesada P, Tramontano F, Faraone-Mennella MR, Farina B: The analysis of the poly(ADPR) polymerase mode of action in rat testis nuclear fractions defines a specific poly(ADP-ribosyl)ation system associated with the nuclear matrix. Mol Cell Biochem. 2000, 205 (1-2): 91-99. 10.1023/A:1007005715848.PubMed
186.
Tramontano F, Malanga M, Farina B, Jones R, Quesada P: Heat stress reduces poly(ADPR)polymerase expression in rat testis. Mol Hum Reprod. 2000, 6 (7): 575-581. 10.1093/molehr/6.7.575.PubMed
187.
Jaroudi S, SenGupta S: DNA repair in mammalian embryos. Mutat Res. 2007, 635 (1): 53-77. 10.1016/j.mrrev.2006.09.002.PubMed
188.
Marchetti C, Gallego MA, Defossez A, Formstecher P, Marchetti P: Staining of human sperm with fluorochrome-labeled inhibitor of caspases to detect activated caspases: correlation with apoptosis and sperm parameters. Hum Reprod. 2004, 19 (5): 1127-1134. 10.1093/humrep/deh222.PubMed
189.
Paasch U, Grunewald S, Agarwal A, Glandera HJ: Activation pattern of caspases in human spermatozoa. Fertility and sterility. 2004, 81 (Suppl 1): 802-809. 10.1016/j.fertnstert.2003.09.030.PubMed
190.
Grunewald S, Sharma R, Paasch U, Glander HJ, Agarwal A: Impact of caspase activation in human spermatozoa. Microsc Res Tech. 2009,
191.
Almeida C, Cardoso MF, Sousa M, Viana P, Goncalves A, Silva J, Barros A: Quantitative study of caspase-3 activity in semen and after swim-up preparation in relation to sperm quality. Hum Reprod. 2005, 20 (5): 1307-1313. 10.1093/humrep/deh727.PubMed
192.
Weng SL, Taylor SL, Morshedi M, Schuffner A, Duran EH, Beebe S, Oehninger S: Caspase activity and apoptotic markers in ejaculated human sperm. Molecular human reproduction. 2002, 8 (11): 984-991. 10.1093/molehr/8.11.984.PubMed
193.
Paasch U, Grunewald S, Fitzl G, Glander HJ: Deterioration of plasma membrane is associated with activated caspases in human spermatozoa. J Androl. 2003, 24 (2): 246-252.PubMed
194.
Faleiro L, Lazebnik Y: Caspases disrupt the nuclear-cytoplasmic barrier. J Cell Biol. 2000, 151 (5): 951-959. 10.1083/jcb.151.5.951.PubMedCentralPubMed
195.
Buelow B, Song Y, Scharenberg AM: The Poly(ADP-ribose) Polymerase PARP-1 Is Required for Oxidative Stress-induced TRPM2 Activation in Lymphocytes. J Biol Chem. 2008, 283 (36): 24571-24583. 10.1074/jbc.M802673200.PubMedCentralPubMed
196.
Xu B, Chiu J, Feng B, Chen S, Chakrabarti S: PARP activation and the alteration of vasoactive factors and extracellular matrix protein in retina and kidney in diabetes. Diabetes Metab Res Rev. 2008, 24 (5): 404-412. 10.1002/dmrr.842.PubMed
197.
Blanc-Layrac G, Bringuier AF, Guillot R, Feldmann G: Morphological and biochemical analysis of cell death in human ejaculated spermatozoa. Cell Mol Biol (Noisy-le-grand). 2000, 46 (1): 187-197.
198.
El-Domyati MM, Al-Din AB, Barakat MT, El-Fakahany HM, Xu J, Sakkas D: Deoxyribonucleic acid repair and apoptosis in testicular germ cells of aging fertile men: the role of the poly(adenosine diphosphate-ribosyl)ation pathway. Fertility and sterility. 2009, 91 (5 Suppl): 2221-2229. 10.1016/j.fertnstert.2008.03.027.PubMed
199.
Mahfouz RZ, Sharma RK, Poenicke K, Jha R, Paasch U, Grunewald S, Agarwal A: Evaluation of poly(ADP-ribose) polymerase cleavage (cPARP) in ejaculated human sperm fractions after induction of apoptosis. Fertility and sterility. 2009, 91 (5 Suppl): 2210-2220. 10.1016/j.fertnstert.2008.02.173.PubMed
200.
Kefer JC, Agarwal A, Sabanegh E: Role of antioxidants in the treatment of male infertility. Int J Urol. 2009, 16 (5): 449-457. 10.1111/j.1442-2042.2009.02280.x.PubMed
201.
Makker K, Agarwal A, Sharma R: Oxidative stress & male infertility. Indian J Med Res. 2009, 129 (4): 357-367.PubMed
202.
Reddy M, Mahipal S, Subhashini J, Reddy M, Roy K, Reddy G, Reddy P, Reddanna P: Bacterial lipopolysaccharide-induced oxidative stress in the impairment of steroidogenesis and spermatogenesis in rats. Reprod Toxicol. 2006, 22: 493-500. 10.1016/j.reprotox.2006.03.003.PubMed
203.
Mahfouz R, Sharma R, Sharma D, Sabanegh E, Agarwal A: Diagnostic value of the total antioxidant capacity (TAC) in human seminal plasma. Fertility and sterility. 2009, 91 (3): 805-811. 10.1016/j.fertnstert.2008.01.022.PubMed
204.
Vaithinathan S, Saradha B, Mathur PP: Transient inhibitory effect of methoxychlor on testicular steroidogenesis in rat: an in vivo study. Arch Toxicol. 2008, 82 (11): 833-839. 10.1007/s00204-008-0301-2.PubMed
205.
Sarkar O, Mathur PP: Adjudin-mediated germ cell depletion alters the anti-oxidant status of adult rat testis. Mol Reprod Dev. 2009, 76 (1): 31-37. 10.1002/mrd.20928.PubMed
206.
Saradha B, Vaithinathan S, Mathur PP: Lindane induces testicular apoptosis in adult Wistar rats through the involvement of Fas-FasL and mitochondria-dependent pathways. Toxicology. 2009, 255 (3): 131-139. 10.1016/j.tox.2008.10.016.PubMed
207.
Sarkar O, Mathur P, Cheng C, Mruk D: Interleukin 1 alpha (IL1A) is a novel regulator of the blood-testis barrier in the rat. Biol Reprod. 2008, 78: 445-454. 10.1095/biolreprod.107.064501.PubMedCentralPubMed
208.
Erdelyi K, Bakondi E, Gergely P, Szabo C, Virag L: Pathophysiologic role of oxidative stress-induced poly(ADP-ribose) polymerase-1 activation: focus on cell death and transcriptional regulation. Cell Mol Life Sci. 2005, 62 (7-8): 751-759. 10.1007/s00018-004-4506-0.PubMed
209.
Chen H, Jia W, Xu X, Fan Y, Zhu D, Wu H, Xie Z, Zheng Z: Upregulation of PEDF expression by PARP inhibition contributes to the decrease in hyperglycemia-induced apoptosis in HUVECs. Biochem Biophys Res Commun. 2008, 369 (2): 718-724. 10.1016/j.bbrc.2008.02.100.PubMed
210.
Chandak PG, Gaikwad AB, Tikoo K: Gallotannin ameliorates the development of streptozotocin-induced diabetic nephropathy by preventing the activation of PARP. Phytother Res. 2009, 23 (1): 72-77. 10.1002/ptr.2559.PubMed
211.
El-Khamisy SF, Masutani M, Suzuki H, Caldecott KW: A requirement for PARP-1 for the assembly or stability of XRCC1 nuclear foci at sites of oxidative DNA damage. Nucleic Acids Res. 2003, 31 (19): 5526-5533. 10.1093/nar/gkg761.PubMedCentralPubMed
212.
Liang Y, Lin SY, Brunicardi FC, Goss J, Li K: DNA damage response pathways in tumor suppression and cancer treatment. World J Surg. 2009, 33 (4): 661-666. 10.1007/s00268-008-9840-1.PubMed
213.
Ljungman M, Hanawalt PC: Efficient protection against oxidative DNA damage in chromatin. Mol Carcinog. 1992, 5 (4): 264-269. 10.1002/mc.2940050406.PubMed
214.
Huang SH, Xiong M, Chen XP, Xiao ZY, Zhao YF, Huang ZY: PJ34, an inhibitor of PARP-1, suppresses cell growth and enhances the suppressive effects of cisplatin in liver cancer cells. Oncol Rep. 2008, 20 (3): 567-572.PubMed
215.
Lin P, Lin C, Huang C, Fang J, Chuang M: 2,3,7,8-Tetrachlorodibenzo-p-dioxin modulates the induction of DNA strand breaks and poly(ADP-ribose) polymerase-1 activation by 17beta-estradiol in human breast carcinoma cells through alteration of CYP1A1 and CYP1B1 expression. Chem Res Toxicol. 2008, 21 (7): 1337-1347. 10.1021/tx700396d.PubMed
216.
Ma Q, Baldwin K, Renzelli A, McDaniel A, Dong L: TCDD-inducible poly(ADP-ribose) polymerase: a novel response to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Biochem Biophys Res Commun. 2001, 289 (2): 499-506. 10.1006/bbrc.2001.5987.PubMed
217.
Beneke S, Burkle A: Poly(ADP-ribosyl)ation in mammalian ageing. Nucleic Acids Res. 2007, 35 (22): 7456-7465. 10.1093/nar/gkm735.PubMedCentralPubMed
218.
Cohausz O, Althaus FR: Role of PARP-1 and PARP-2 in the expression of apoptosis-regulating genes in HeLa cells. Cell Biol Toxicol. 2009, 25 (4): 379-391. 10.1007/s10565-008-9092-8.PubMed
219.
Chiu HJ, Fischman DA, Hammerling U: Vitamin A depletion causes oxidative stress, mitochondrial dysfunction, and PARP-1-dependent energy deprivation. FASEB J. 2008, 22 (11): 3878-3887. 10.1096/fj.08-112375.PubMedCentralPubMed
220.
Dantzer F, Giraud-Panis MJ, Jaco I, Ame JC, Schultz I, Blasco M, Koering CE, Gilson E, Menissier-de Murcia J, de Murcia G, Schreiber V: Functional interaction between poly(ADP-Ribose) polymerase 2 (PARP-2) and TRF2: PARP activity negatively regulates TRF2. Mol Cell Biol. 2004, 24 (4): 1595-1607. 10.1128/MCB.24.4.1595-1607.2004.PubMedCentralPubMed
221.
Gomez M, Wu J, Schreiber V, Dunlap J, Dantzer F, Wang Y, Liu Y: PARP1 Is a TRF2-associated poly(ADP-ribose)polymerase and protects eroded telomeres. Mol Biol Cell. 2006, 17 (4): 1686-1696. 10.1091/mbc.E05-07-0672.PubMedCentralPubMed
222.
Smith S, Giriat I, Schmitt A, de Lange T: Tankyrase, a poly(ADP-ribose) polymerase at human telomeres. Science. 1998, 282 (5393): 1484-1487. 10.1126/science.282.5393.1484.PubMed
223.
Simbulan-Rosenthal CM, Haddad BR, Rosenthal DS, Weaver Z, Coleman A, Luo R, Young HM, Wang ZQ, Ried T, Smulson ME: Chromosomal aberrations in PARP(-/-) mice: genome stabilization in immortalized cells by reintroduction of poly(ADP-ribose) polymerase cDNA. Proc Natl Acad Sci USA. 1999, 96 (23): 13191-13196. 10.1073/pnas.96.23.13191.PubMedCentralPubMed
224.
d'Adda di Fagagna F, Hande MP, Tong WM, Lansdorp PM, Wang ZQ, Jackson SP: Functions of poly(ADP-ribose) polymerase in controlling telomere length and chromosomal stability. Nat Genet. 1999, 23 (1): 76-80. 10.1038/12680.PubMed
225.
Aitken RJ, Gordon E, Harkiss D, Twigg JP, Milne P, Jennings Z, Irvine DS: Relative impact of oxidative stress on the functional competence and genomic integrity of human spermatozoa. Biol Reprod. 1998, 59 (5): 1037-1046. 10.1095/biolreprod59.5.1037.PubMed
226.
Aitken RJ, Krausz C: Oxidative stress, DNA damage and the Y chromosome. Reproduction. 2001, 122 (4): 497-506. 10.1530/rep.0.1220497.PubMed
227.
Mahfouz RZ, Said TM, Mangrola D, Agarwal A: Potential roles of poly (ADP-ribose) polymerase in male reproduction. Archives of Medical Science. 2009, 5 (1A): S92-S98.
228.
Adhikari S, Choudhury S, Mitra PS, Dubash JJ, Sajankila SP, Roy R: Targeting base excision repair for chemosensitization. Anticancer Agents Med Chem. 2008, 8 (4): 351-357.PubMed
229.
de la Lastra CA, Villegas I, Sanchez-Fidalgo S: Poly(ADP-ribose) polymerase inhibitors: new pharmacological functions and potential clinical implications. Curr Pharm Des. 2007, 13 (9): 933-962. 10.2174/138161207780414241.PubMed
230.
Zhang P, Li H, Chen D, Ni J, Kang Y, Wang S: Oleanolic acid induces apoptosis in human leukemia cells through caspase activation and poly(ADP-ribose) polymerase cleavage. Acta Biochim Biophys Sin (Shanghai). 2007, 39 (10): 803-809. 10.1111/j.1745-7270.2007.00335.x.
Metadata
Title
Potential biological role of poly (ADP-ribose) polymerase (PARP) in male gametes
Authors
Ashok Agarwal
Reda Z Mahfouz
Rakesh K Sharma
Oli Sarkar
Devna Mangrola
Premendu P Mathur
Publication date
01-12-2009
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2009
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/1477-7827-7-143

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