Poly(ADP-ribose) polymerase plays a differential role in DNA damage-response and cell death pathways in Trypanosoma cruzi

International Journal for Parasitology

Volumn 41, Issue 3, 2011, Pages 405-416

  Vilchez Larrea, Salomé C ^a   Alonso, Guillermo D ^a,b   Schlesinger, Mariana ^a   Torres, Héctor N ^a,b   Flawiá, Mirtha M ^a,b   Fernández Villamil, Silvia H ^a,b  

^a INSTITUTO DE INVESTIGACIONES EN INGENIERÍA GENÉTICA Y BIOLOGÍA MOLECULAR   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

Cell death; DNA repair; PARG; PARP; Trypanosoma cruzi

Indexed keywords

HYDROGEN PEROXIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE;

DNA; EUKARYOTE; GENOTOXICITY; INHIBITOR; METABOLISM; PARASITE; POLYMERASE CHAIN REACTION; PROTEIN;

APOPTOSIS; ARTICLE; CELL GROWTH; CELL NUCLEUS; CONTROLLED STUDY; CYTOSOL; DNA DAMAGE; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE TRANSLOCATION; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; TRYPANOSOMA CRUZI; ULTRAVIOLET RADIATION;

ANIMALS; CELL DEATH; CELL NUCLEUS; DNA DAMAGE; DNA REPAIR; GLYCOSIDE HYDROLASES; POLY(ADP-RIBOSE) POLYMERASES; PROTOZOAN PROTEINS; TRYPANOSOMA CRUZI;

EUKARYOTA; PROTISTA; TRYPANOSOMA CRUZI;

EID: 79951812211     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2010.11.008     Document Type: Article

References (82)

1. Ame J.C., Spenlehauer C., de Murcia G. The PARP superfamily. BioEssays 2004, 26:882-893.
2. Ame J.C., Fouquerel E., Gauthier L.R., Biard D., Boussin F.D., Dantzer F., de Murcia G., Schreiber V. Radiation-induced mitotic catastrophe in PARG-deficient cells. J. Cell Sci. 2009, 122:1990-2002.
3. Andrabi S.A., Kim N.S., Yu S.W., Wang H., Koh D.W., Sasaki M., Klaus J.A., Otsuka T., Zhang Z., Koehler R.C., Hurn P.D., Poirier G.G., Dawson V.L., Dawson T.M. Poly(ADP-ribose) (PAR) polymer is a death signal. Proc. Natl. Acad. Sci. USA 2006, 103:18308-18313.
4. Assuncao Guimaraes C., Linden R. Programmed cell deaths. Apoptosis and alternative deathstyles. Eur. J. Biochem. 2004, 271:1638-1650.
5. Augusto-Pinto L., Bartholomeu D.C., Teixeira S.M., Pena S.D., Machado C.R. Molecular cloning and characterization of the DNA mismatch repair gene class 2 from the Trypanosoma cruzi. Gene 2001, 272:323-333.
6. Augusto-Pinto L., Teixeira S.M., Pena S.D., Machado C.R. Single-nucleotide polymorphisms of the Trypanosoma cruzi MSH2 gene support the existence of three phylogenetic lineages presenting differences in mismatch-repair efficiency. Genetics 2003, 164:117-126.
7. Barry J.D., McCulloch R. Antigenic variation in trypanosomes: enhanced phenotypic variation in a eukaryotic parasite. Adv. Parasitol. 2001, 49:1-70.
8. Bell J.S., Harvey T.I., Sims A.M., McCulloch R. Characterization of components of the mismatch repair machinery in Trypanosoma brucei. Mol. Microbiol. 2004, 51:159-173.
9. Berriman M., Ghedin E., Hertz-Fowler C., Blandin G., Renauld H., Bartholomeu D.C., Lennard N.J., Caler E., Hamlin N.E., Haas B., Bohme U., Hannick L., Aslett M.A., Shallom J., Marcello L., Hou L., Wickstead B., Alsmark U.C., Arrowsmith C., Atkin R.J., Barron A.J., Bringaud F., Brooks K., Carrington M., Cherevach I., Chillingworth T.J., Churcher C., Clark L.N., Corton C.H., Cronin A., Davies R.M., Doggett J., Djikeng A., Feldblyum T., Field M.C., Fraser A., Goodhead I., Hance Z., Harper D., Harris B.R., Hauser H., Hostetler J., Ivens A., Jagels K., Johnson D., Johnson J., Jones K., Kerhornou A.X., Koo H., Larke N., Landfear S., Larkin C., Leech V., Line A., Lord A., Macleod A., Mooney P.J., Moule S., Martin D.M., Morgan G.W., Mungall K., Norbertczak H., Ormond D., Pai G., Peacock C.S., Peterson J., Quail M.A., Rabbinowitsch E., Rajandream M.A., Reitter C., Salzberg S.L., Sanders M., Schobel S., Sharp S., Simmonds M., Simpson A.J., Tallon L., Turner C.M., Tait A., Tivey A.R., Van Aken S., Walker D., Wanless D., Wang S., White B., White O., Whitehead S., Woodward J., Wortman J., Adams M.D., Embley T.M., Gull K., Ullu E., Barry J.D., Fairlamb A.H., Opperdoes F., Barrell B.G., Donelson J.E., Hall N., Fraser C.M., Melville S.E., El-Sayed N.M. The genome of the African trypanosome Trypanosoma brucei. Science 2005, 309:416-422.
10. Bonicalzi M.E., Haince J.F., Droit A., Poirier G.G. Regulation of poly(ADP-ribose) metabolism by poly(ADP-ribose) glycohydrolase: where and when?. Cell. Mol. Life Sci. 2005, 62:739-750.
11. Boothroyd C.E., Dreesen O., Leonova T., Ly K.I., Figueiredo L.M., Cross G.A., Papavasiliou F.N. A yeast-endonuclease-generated DNA break induces antigenic switching in Trypanosoma brucei. Nature 2009, 459:278-281.
12. Burkle A. Physiology and pathophysiology of poly(ADP-ribosyl)ation. BioEssays 2001, 23:795-806.
13. +. FEBS J. 2005, 272:4576-4589.
14. Caldecott K.W. Single-strand break repair and genetic disease. Nat. Rev. Genet. 2008, 9:619-631.
15. Cohausz O., Blenn C., Malanga M., Althaus F.R. The roles of poly(ADP-ribose)-metabolizing enzymes in alkylation-induced cell death. Cell. Mol. Life Sci. 2008, 65:644-655.
16. Cohausz O., Althaus F.R. Role of PARP-1 and PARP-2 in the expression of apoptosis-regulating genes in HeLa cells. Cell Biol. Toxicol. 2009, 25:379-391.
17. D'Amours D., Desnoyers S., D'Silva I., Poirier G.G. Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem. J. 1999, 342(Pt 2):249-268.
18. Dantzer F., Schreiber V., Niedergang C., Trucco C., Flatter E., De La Rubia G., Oliver J., Rolli V., Menissier-de Murcia J., de Murcia G. Involvement of poly(ADP-ribose) polymerase in base excision repair. Biochimie 1999, 81:69-75.
19. Davidovic L., Vodenicharov M., Affar E.B., Poirier G.G. Importance of poly(ADP-ribose) glycohydrolase in the control of poly(ADP-ribose) metabolism. Exp. Cell Res. 2001, 268:7-13.
20. de Murcia G., Menissier de Murcia J. Poly(ADP-ribose) polymerase: a molecular nick-sensor. Trends Biochem. Sci. 1994, 19:172-176.
21. De Souza W. Basic cell biology of Trypanosoma cruzi. Curr. Pharm. Des. 2002, 8:269-285.
22. Diefenbach J., Burkle A. Introduction to poly(ADP-ribose) metabolism. Cell. Mol. Life Sci. 2005, 62:721-730.
23. Donelson J.E. Antigenic variation and the African trypanosome genome. Acta Trop. 2003, 85:391-404.
24. Duszenko M., Figarella K., Macleod E.T., Welburn S.C. Death of a trypanosome: a selfish altruism. Trends Parasitol 2006, 22:536-542.
25. El-Sayed N.M., Myler P.J., Bartholomeu D.C., Nilsson D., Aggarwal G., Tran A.N., Ghedin E., Worthey E.A., Delcher A.L., Blandin G., Westenberger S.J., Caler E., Cerqueira G.C., Branche C., Haas B., Anupama A., Arner E., Aslund L., Attipoe P., Bontempi E., Bringaud F., Burton P., Cadag E., Campbell D.A., Carrington M., Crabtree J., Darban H., da Silveira J.F., de Jong P., Edwards K., Englund P.T., Fazelina G., Feldblyum T., Ferella M., Frasch A.C., Gull K., Horn D., Hou L., Huang Y., Kindlund E., Klingbeil M., Kluge S., Koo H., Lacerda D., Levin M.J., Lorenzi H., Louie T., Machado C.R., McCulloch R., McKenna A., Mizuno Y., Mottram J.C., Nelson S., Ochaya S., Osoegawa K., Pai G., Parsons M., Pentony M., Pettersson U., Pop M., Ramirez J.L., Rinta J., Robertson L., Salzberg S.L., Sanchez D.O., Seyler A., Sharma R., Shetty J., Simpson A.J., Sisk E., Tammi M.T., Tarleton R., Teixeira S., Van Aken S., Vogt C., Ward P.N., Wickstead B., Wortman J., White O., Fraser C.M., Stuart K.D., Andersson B. The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 2005, 309:409-415.
26. Erdelyi K., Bai P., Kovacs I., Szabo E., Mocsar G., Kakuk A., Szabo C., Gergely P., Virag L. Dual role of poly(ADP-ribose) glycohydrolase in the regulation of cell death in oxidatively stressed A549 cells. FASEB J. 2009, 23:3553-3563.
27. Fernandez Villamil S.H., Baltanas R., Alonso G.D., Vilchez Larrea S.C., Torres H.N., Flawia M.M. TcPARP: a DNA damage-dependent poly(ADP-ribose) polymerase from Trypanosoma cruzi. Int. J. Parasitol. 2008, 38:277-287.
28. Gagne J.P., Hendzel M.J., Droit A., Poirier G.G. The expanding role of poly(ADP-ribose) metabolism: current challenges and new perspectives. Curr. Opin. Cell Biol. 2006, 18:145-151.
29. Ghodgaonkar M.M., Zacal N., Kassam S., Rainbow A.J., Shah G.M. Depletion of poly(ADP-ribose) polymerase-1 reduces host cell reactivation of a UV-damaged adenovirus-encoded reporter gene in human dermal fibroblasts. DNA Repair (Amst.) 2008, 7:617-632.
30. Ha H.C., Snyder S.H. Poly(ADP-ribose) polymerase is a mediator of necrotic cell death by ATP depletion. Proc. Natl. Acad. Sci. USA 1999, 96:13978-13982.
31. Haince J.F., Ouellet M.E., McDonald D., Hendzel M.J., Poirier G.G. Dynamic relocation of poly(ADP-ribose) glycohydrolase isoforms during radiation-induced DNA damage. Biochim. Biophys. Acta 2006, 1763:226-237.
32. Hakem R. DNA-damage repair; the good, the bad, and the ugly. EMBO J. 2008, 27:589-605.
33. Hassa P.O., Haenni S.S., Elser M., Hottiger M.O. Nuclear ADP-ribosylation reactions in mammalian cells: where are we today and where are we going?. Microbiol. Mol. Biol. Rev. 2006, 70:789-829.
34. Hjertvik M., Erixon K., Ahnstrom G. Repair of DNA damage in mammalian cells after treatment with UV and dimethyl sulphate: discrimination between nucleotide and base excision repair by their temperature dependence. Mutat. Res. 1998, 407:87-96.
35. Huang Q., Wu Y.T., Tan H.L., Ong C.N., Shen H.M. A novel function of poly(ADP-ribose) polymerase-1 in modulation of autophagy and necrosis under oxidative stress. Cell Death Differ. 2009, 16:264-277.
36. Jeggo P., Lobrich M. Radiation-induced DNA damage responses. Radiat Prot Dosimetry 2006, 122:124-127.
37. Jeggo P.A., Lobrich M. Contribution of DNA repair and cell cycle checkpoint arrest to the maintenance of genomic stability. DNA Repair (Amst.) 2006, 5:1192-1198.
38. +-dependent modulation of chromatin structure and transcription by nucleosome binding properties of PARP-1. Cell 2004, 119:803-814.
39. + into a nuclear signal. Genes Dev. 2005, 19:1951-1967.
40. Leppard J.B., Dong Z., Mackey Z.B., Tomkinson A.E. Physical and functional interaction between DNA ligase III alpha and poly(ADP-Ribose) polymerase 1 in DNA single-strand break repair. Mol. Cell. Biol. 2003, 23:5919-5927.
41. Lockshin R.A., Zakeri Z. Apoptosis, autophagy, and more. Int. J. Biochem. Cell Biol. 2004, 36:2405-2419.
42. Lockshin R.A., Zakeri Z. Caspase-independent cell death?. Oncogene 2004, 23:2766-2773.
43. Machado-Silva A., Teixeira S.M., Franco G.R., Macedo A.M., Pena S.D., McCulloch R., Machado C.R. Mismatch repair in Trypanosoma brucei: heterologous expression of MSH2 from Trypanosoma cruzi provides new insights into the response to oxidative damage. Gene 2008, 411:19-26.
44. Malanga M., Althaus F.R. The role of poly(ADP-ribose) in the DNA damage signaling network. Biochem. Cell Biol. 2005, 83:354-364.
45. Maruta H., Matsumura N., Tanuma S. Role of (ADP-ribose)n catabolism in DNA repair. Biochem. Biophys. Res. Commun. 1997, 236:265-269.
46. McCulloch R., Barry J.D. A role for RAD51 and homologous recombination in Trypanosoma brucei antigenic variation. Genes Dev. 1999, 13:2875-2888.
47. McKean P.G., Keen J.K., Smith D.F., Benson F.E. Identification and characterisation of a RAD51 gene from Leishmania major. Mol. Biochem. Parasitol. 2001, 115:209-216.
48. Menna-Barreto R.F., Salomao K., Dantas A.P., Santa-Rita R.M., Soares M.J., Barbosa H.S., de Castro S.L. Different cell death pathways induced by drugs in Trypanosoma cruzi: an ultrastructural study. Micron 2009, 40:157-168.
49. Meyer-Ficca M.L., Meyer R.G., Coyle D.L., Jacobson E.L., Jacobson M.K. Human poly(ADP-ribose) glycohydrolase is expressed in alternative splice variants yielding isoforms that localize to different cell compartments. Exp. Cell Res. 2004, 297:521-532.
50. Militello K.T., Refour P., Comeaux C.A., Duraisingh M.T. Antisense RNA and RNAi in protozoan parasites: working hard or hardly working?. Mol. Biochem. Parasitol. 2008, 157:117-126.
51. Munoz-Gamez J.A., Rodriguez-Vargas J.M., Quiles-Perez R., Aguilar-Quesada R., Martin-Oliva D., de Murcia G., Menissier de Murcia J., Almendros A., Ruiz de Almodovar M., Oliver F.J. PARP-1 is involved in autophagy induced by DNA damage. Autophagy 2009, 5:61-74.
52. Niere M., Kernstock S., Koch-Nolte F., Ziegler M. Functional localization of two poly(ADP-ribose)-degrading enzymes to the mitochondrial matrix. Mol. Cell. Biol. 2008, 28:814-824.
53. O'Driscoll M., Jeggo P.A. The role of double-strand break repair - insights from human genetics. Nat. Rev. Genet. 2006, 7:45-54.
54. Ohashi S., Kanai M., Hanai S., Uchiumi F., Maruta H., Tanuma S., Miwa M. Subcellular localization of poly(ADP-ribose) glycohydrolase in mammalian cells. Biochem. Biophys. Res. Commun. 2003, 307:915-921.
55. Oka S., Kato J., Moss J. Identification and characterization of a mammalian 39-kDa poly(ADP-ribose) glycohydrolase. J. Biol. Chem. 2006, 281:705-713.
56. Otto H., Reche P.A., Bazan F., Dittmar K., Haag F., Koch-Nolte F. In silico characterization of the family of PARP-like poly(ADP-ribosyl)transferases (pARTs). BMC Genomics 2005, 6:139.
57. Podesta D., Garcia-Herreros M.I., Cannata J.J., Stoppani A.O., Fernandez Villamil S.H. Purification and properties of poly(ADP-ribose) polymerase from Crithidia fasciculata. Automodification and poly(ADP-ribosyl)ation of DNA topoisomerase I. Mol. Biochem. Parasitol. 2004, 135:211-219.
58. 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, 41:60-65.
59. Robinson N.P., McCulloch R., Conway C., Browitt A., Barry J.D. Inactivation of Mre11 does not affect VSG gene duplication mediated by homologous recombination in Trypanosoma brucei. J. Biol. Chem. 2002, 277:26185-26193.
60. Rossi M.N., Carbone M., Mostocotto C., Mancone C., Tripodi M., Maione R., Amati P. Mitochondrial localization of PARP-1 requires interaction with mitofilin and is involved in the maintenance of mitochondrial DNA integrity. J. Biol. Chem. 2009, 284:31616-31624.
61. Satoh M.S., Lindahl T. Role of poly(ADP-ribose) formation in DNA repair. Nature 1992, 356:356-358.
62. Schreiber V., Dantzer F., Ame J.C., de Murcia G. Poly(ADP-ribose): novel functions for an old molecule. Nat. Rev. Mol. Cell Biol. 2006, 7:517-528.
63. Shall S. ADP-ribosylation reactions. Biochimie 1995, 77:313-318.
64. Shi H., Tschudi C., Ullu E. An unusual Dicer-like1 protein fuels the RNA interference pathway in Trypanosoma brucei. RNA 2006, 12:2063-2072.
65. Shrivastav M., De Haro L.P., Nickoloff J.A. Regulation of DNA double-strand break repair pathway choice. Cell Res 2008, 18:134-147.
66. Son Y.O., Kook S.H., Jang Y.S., Shi X., Lee J.C. Critical role of poly(ADP-ribose) polymerase-1 in modulating the mode of cell death caused by continuous oxidative stress. J. Cell. Biochem. 2009, 108:989-997.
67. Stockdale C., Swiderski M.R., Barry J.D., McCulloch R. Antigenic variation in Trypanosoma brucei: joining the DOTs. PLoS Biol. 2008, 6:e185.
68. Szabó C. Cell Death. The Role of PARP 2000, CRC Press, Boca Raton, USA.
69. Tentori L., Balduzzi A., Portarena I., Levati L., Vernole P., Gold B., Bonmassar E., Graziani G. Poly (ADP-ribose) polymerase inhibitor increases apoptosis and reduces necrosis induced by a DNA minor groove binding methyl sulfonate ester. Cell Death Differ. 2001, 8:817-828.
70. Tulin A., Stewart D., Spradling A.C. The Drosophila heterochromatic gene encoding poly(ADP-ribose) polymerase (PARP) is required to modulate chromatin structure during development. Genes Dev. 2002, 16:2108-2119.
71. Ulbert S., Chaves I., Borst P. Expression site activation in Trypanosoma brucei with three marked variant surface glycoprotein gene expression sites. Mol. Biochem. Parasitol. 2002, 120:225-235.
72. Ullu E., Tschudi C., Chakraborty T. RNA interference in protozoan parasites. Cell. Microbiol. 2004, 6:509-519.
73. Vazquez M.P., Levin M.J. Functional analysis of the intergenic regions of TcP2beta gene loci allowed the construction of an improved Trypanosoma cruzi expression vector. Gene 1999, 239:217-225.
74. Virag L., Salzman A.L., Szabo C. Poly(ADP-ribose) synthetase activation mediates mitochondrial injury during oxidant-induced cell death. J. Immunol. 1998, 161:3753-3759.
75. Virag L., Szabo C. The therapeutic potential of poly(ADP-ribose) polymerase inhibitors. Pharmacol. Rev. 2002, 54:375-429.
76. Westergaard G.G., Bercovich N., Reinert M.D., Vazquez M.P. Analysis of a nuclear localization signal in the p14 splicing factor in Trypanosoma cruzi. Int. J. Parasitol. 2010, 40(9):1029-1035.
77. Whatcott C.J., Meyer-Ficca M.L., Meyer R.G., Jacobson M.K. A specific isoform of poly(ADP-ribose) glycohydrolase is targeted to the mitochondrial matrix by a N-terminal mitochondrial targeting sequence. Exp. Cell Res. 2009, 315:3477-3485.
78. Woodhouse B.C., Dianov G.L. Poly ADP-ribose polymerase-1: an international molecule of mystery. DNA Repair (Amst.) 2008, 7:1077-1086.
79. Woodhouse B.C., Dianova I.I., Parsons J.L., Dianov G.L. Poly(ADP-ribose) polymerase-1 modulates DNA repair capacity and prevents formation of DNA double strand breaks. DNA Repair (Amst.) 2008, 7:932-940.
80. Yu S.W., Wang H., Poitras M.F., Coombs C., Bowers W.J., Federoff H.J., Poirier G.G., Dawson T.M., Dawson V.L. Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 2002, 297:259-263.
81. Yu S.W., Andrabi S.A., Wang H., Kim N.S., Poirier G.G., Dawson T.M., Dawson V.L. Apoptosis-inducing factor mediates poly(ADP-ribose) (PAR) polymer-induced cell death. Proc. Natl. Acad. Sci. USA 2006, 103:18314-18319.
82. Ziegler M., Oei S.L. A cellular survival switch: poly(ADP-ribosyl)ation stimulates DNA repair and silences transcription. BioEssays 2001, 23:543-548.