Enhancement of NEIL1 protein-initiated oxidized DNA base excision repair by heterogeneous nuclear ribonucleoprotein U (hnRNP-U) via direct interaction

Journal of Biological Chemistry

Volumn 287, Issue 41, 2012, Pages 34202-34211

  Hegde, Muralidhar L ^a   Banerjee, Srijita ^a   Hegde, Pavana M ^a   Bellot, Larry J ^a   Hazra, Tapas K ^a,b   Boldogh, Istvan ^a,b   Mitra, Sankar ^a,b  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASE EXCISION REPAIRS; BASE REPAIR; C-TERMINAL DOMAINS; C-TERMINAL REGIONS; CIRCULAR DICHROISM SPECTRA; DIRECT INTERACTIONS; DISORDERED REGIONS; DNA GLYCOSYLASE; ENZYMATIC ACTIVITIES; EQUIMOLAR RATIO; HIGH AFFINITY; HUMAN CELLS; HUMAN GENOMES; IMMUNOPRECIPITATES; IN-VITRO; NATIVE PROTEINS; NUCLEAR RIBONUCLEOPROTEIN; PRODUCT RELEASE; SINGLE-STRANDED DNA;

CELLS; CYTOLOGY; DNA; GENES; OXIDATION; OXIDATIVE STRESS; PROTEINS;

REPAIR;

DNA BASE; DNA GLYCOSYLTRANSFERASE; DOUBLE STRANDED DNA; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN U; PROTEIN NEIL1; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CELL INTERACTION; CELL PROTECTION; CELL SURVIVAL; CIRCULAR DICHROISM; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; EXCISION REPAIR; GENETIC DAMAGE; HUMAN; HUMAN CELL; IN VITRO STUDY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; REGULATORY MECHANISM;

DNA GLYCOSYLASES; DNA REPAIR; HEK293 CELLS; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN U; HUMANS; OXIDATION-REDUCTION; OXIDATIVE STRESS; PROTEIN BINDING;

EID: 84867261398     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.384032     Document Type: Article

References (50)

1. Breen, A. P., and Murphy, J. A. (1995) Reactions of oxyl radicals with DNA. Free Radic. Biol. Med. 18, 1033-1077
2. Cadet, J. L., and Brannock, C. (1998) Free radicals and the pathobiology of brain dopamine systems. Neurochem. Int. 32, 117-131 (Pubitemid 28105298)
3. Grisham, M. B., Hernandez, L. A., and Granger, D. N. (1986) Xanthine oxidase and neutrophil infiltration in intestinal ischemia. Am. J. Physiol. 251, G567-G574
4. Ames, B. N., Shigenaga, M. K., and Hagen, T. M. (1993) Oxidants, antioxidants, and the degenerative diseases of aging. Proc. Natl. Acad. Sci. U.S.A. 90, 7915-7922 (Pubitemid 23260825)
5. Bozner, P., Grishko, V., LeDoux, S. P., Wilson, G. L., Chyan, Y. C., and Pappolla, M. A. (1997) The amyloid-β protein induces oxidative damage of mitochondrial DNA. J. Neuropathol. Exp. Neurol. 56, 1356-1362 (Pubitemid 28006581)
6. DeWeese, T. L., Shipman, J. M., Larrier, N. A., Buckley, N. M., Kidd, L. R., Groopman, J. D., Cutler, R. G., te Riele, H., and Nelson, W. G. (1998) Mouse embryonic stem cells carrying one or two defective Msh2 alleles respond abnormally to oxidative stress inflicted by low-level radiation. Proc. Natl. Acad. Sci. U.S.A. 95, 11915-11920
7. Meyer, T. E., Liang, H. Q., Buckley, A. R., Buckley, D. J., Gout, P. W., Green, E. H., and Bode, A. M. (1998) Changes in glutathione redox cycling and oxidative stress response in the malignant progression of NB2 lymphoma cells. Int. J. Cancer 77, 55-63 (Pubitemid 28308552)
8. Mukherjee, S. K., and Adams, J. D., Jr. (1997) The effects of aging and neurodegeneration on apoptosis-associated DNA fragmentation and the benefits of nicotinamide. Mol. Chem. Neuropathol. 32, 59-74 (Pubitemid 28028113)
9. Multhaup, G., Ruppert, T., Schlicksupp, A., Hesse, L., Beher, D., Masters, C. L., and Beyreuther, K. (1997) Reactive oxygen species and Alzheimer disease. Biochem. Pharmacol. 54, 533-539 (Pubitemid 27405186)
10. Hegde, M. L., Hazra, T. K., and Mitra, S. (2008) Early steps in the DNA base excision/single-strand interruption repair pathway in mammalian cells. Cell Res. 18, 27-47
11. Liu, M., Bandaru, V., Bond, J. P., Jaruga, P., Zhao, X., Christov, P. P., Burrows, C. J., Rizzo, C. J., Dizdaroglu, M., and Wallace, S. S. (2010) The mouse orthologue of NEIL3 is a functionalDNAglycosylase in vitro and in vivo. Proc. Natl. Acad. Sci. U.S.A. 107, 4925-4930
12. Wiederhold, L., Leppard, J. B., Kedar, P., Karimi-Busheri, F., Rasouli-Nia, A., Weinfeld, M., Tomkinson, A. E., Izumi, T., Prasad, R., Wilson, S. H., Mitra, S., and Hazra, T. K. (2004) AP endonuclease-independent DNA base excision repair in human cells. Mol. Cell 15, 209-220 (Pubitemid 38950968)
13. Matsumoto, Y. (2001) Molecular mechanism of PCNA-dependent base excision repair. Prog. Nucleic Acid Res. Mol. Biol. 68, 129-138
14. Klungland, A., and Lindahl, T. (1997) Second pathway for completion of human DNA base excision-repair: reconstitution with purified proteins and requirement for DNase IV (FEN1). EMBO J. 16, 3341-3348 (Pubitemid 27234971)
15. Garg, P., Stith, C. M., Sabouri, N., Johansson, E., and Burgers, P. M. (2004) Idling by DNA polymerase δ maintains a ligatable nick during laggingstrand DNA replication. Genes Dev. 18, 2764-2773 (Pubitemid 39507769)
16. Das, S., Chattopadhyay, R., Bhakat, K. K., Boldogh, I., Kohno, K., Prasad, R., Wilson, S. H., and Hazra, T. K. (2007) Stimulation of NEIL2-mediated oxidized base excision repair via YB-1 interaction during oxidative stress. J. Biol. Chem. 282, 28474-28484 (Pubitemid 47606000)
17. Prasad, R., Liu, Y., Deterding, L. J., Poltoratsky, V. P., Kedar, P. S., Horton, J. K., Kanno, S., Asagoshi, K., Hou, E. W., Khodyreva, S. N., Lavrik, O. I., Tomer, K. B., Yasui, A., and Wilson, S. H. (2007) HMGB1 is a cofactor in mammalian base excision repair. Mol. Cell 27, 829-841 (Pubitemid 47333218)
18. Marenstein, D. R., Ocampo, M. T., Chan, M. K., Altamirano, A., Basu, A. K., Boorstein, R. J., Cunningham, R. P., and Teebor, G. W. (2001) Stimulation of human endonuclease III by Y box-binding protein 1 (DNA-binding protein B): interaction between a base excision repair enzyme and a transcription factor. J. Biol. Chem. 276, 21242-21249
19. Banerjee, D., Mandal, S. M., Das, A., Hegde, M. L., Das, S., Bhakat, K. K., Boldogh, I., Sarkar, P. S., Mitra, S., and Hazra, T. K. (2011) Preferential repair of oxidized base damage in the transcribed genes of mammalian cells. J. Biol. Chem. 286, 6006-6016
20. Das, A., Boldogh, I., Lee, J. W., Harrigan, J. A., Hegde, M. L., Piotrowski, J., de Souza Pinto, N., Ramos, W., Greenberg, M. M., Hazra, T. K., Mitra, S., and Bohr, V. A. (2007) The human Werner syndrome protein stimulates repair of oxidative DNA base damage by the DNA glycosylase NEIL1. J. Biol. Chem. 282, 26591-26602 (Pubitemid 47443759)
21. Dou, H., Theriot, C. A., Das, A., Hegde, M. L., Matsumoto, Y., Boldogh, I., Hazra, T. K., Bhakat, K. K., and Mitra, S. (2008) Interaction of the human DNAglycosylase NEIL1 with proliferating cell nuclear antigen: the potential for replication-associated repair of oxidized bases in mammalian genomes. J. Biol. Chem. 283, 3130-3140
22. Hegde, M. L., Theriot, C. A., Das, A., Hegde, P. M., Guo, Z., Gary, R. K., Hazra, T. K., Shen, B., and Mitra, S. (2008) Physical and functional interaction between human oxidized base-specific DNA glycosylase NEIL1 and flap endonuclease 1. J. Biol. Chem. 283, 27028-27037
23. Theriot, C. A., Hegde, M. L., Hazra, T. K., and Mitra, S. (2010) RPA physically interacts with the human DNA glycosylase NEIL1 to regulate excision of oxidative DNA base damage in primer-template structures. DNA Repair (Amst.) 9, 643-652
24. Kiledjian, M., and Dreyfuss, G. (1992) Primary structure and binding activity of the hnRNP U protein: binding RNA through RGG box. EMBO J. 11, 2655-2664
25. Xiao, R., Tang, P., Yang, B., Huang, J., Zhou, Y., Shao, C., Li, H., Sun, H., Zhang, Y., and Fu, X. D. (2012) Nuclear matrix factor hnRNP U/SAF-A exerts a global control of alternative splicing by regulating U2 snRNP maturation. Mol. Cell 45, 656-668
26. Romig, H., Fackelmayer, F. O., Renz, A., Ramsperger, U., and Richter, A. (1992) Characterization of SAF-A, a novel nuclear DNA-binding protein from HeLa cells with high affinity for nuclear matrix/scaffold attachment DNA elements. EMBO J. 11, 3431-3440
27. Spraggon, L., Dudnakova, T., Slight, J., Lustig-Yariv, O., Cotterell, J., Hastie, N., and Miles, C. (2007) hnRNP-U directly interacts withWT1and modulates WT1 transcriptional activation. Oncogene 26, 1484-1491 (Pubitemid 46340810)
28. β-TrCP ubiquitin ligase by hn-RNP-U. Genes Dev. 16, 439-451
29. Britton, S., Froment, C., Frit, P., Monsarrat, B., Salles, B., and Calsou, P. (2009) Cell nonhomologous end joining capacity controls SAF-A phosphorylation by DNA-PK in response toDNAdouble-strand breaks inducers. Cell Cycle 8, 3717-3722
30. Berglund, F. M., and Clarke, P. R. (2009) hnRNP-U is a specific DNA-dependent protein kinase substrate phosphorylated in response to DNA double-strand breaks. Biochem. Biophys. Res. Commun. 381, 59-64
31. Hegde, M. L., Hegde, P. M., Holthauzen, L. M., Hazra, T. K., Rao, K. S., and Mitra, S. (2010) Specific Inhibition of NEIL-initiated repair of oxidized base damage in human genome by copper and iron: potential etiological linkage to neurodegenerative diseases. J. Biol. Chem. 285, 28812-28825
32. Das, A., Wiederhold, L., Leppard, J. B., Kedar, P., Prasad, R., Wang, H., Boldogh, I., Karimi-Busheri, F., Weinfeld, M., Tomkinson, A. E., Wilson, S. H., Mitra, S., and Hazra, T. K. (2006) NEIL2-initiated, APE-independent repair of oxidized bases in DNA: evidence for a repair complex in human cells. DNA Repair (Amst.) 5, 1439-1448 (Pubitemid 44768083)
33. Hazra, T. K., Izumi, T., Boldogh, I., Imhoff, B., Kow, Y. W., Jaruga, P., Dizdaroglu, M., and Mitra, S. (2002) Identification and characterization of a humanDNAglycosylase for repair of modified bases in oxidatively damaged DNA. Proc. Natl. Acad. Sci. U.S.A. 99, 3523-3528 (Pubitemid 34252141)
34. Hazra, T. K., Kow, Y. W., Hatahet, Z., Imhoff, B., Boldogh, I., Mokkapati, S. K., Mitra, S., and Izumi, T. (2002) Identification and characterization of a novel human DNA glycosylase for repair of cytosine-derived lesions. J. Biol. Chem. 277, 30417-30420 (Pubitemid 34970730)
35. Guan, X., Bai, H., Shi, G., Theriot, C. A., Hazra, T. K., Mitra, S., and Lu, A. L. (2007) The human checkpoint sensor Rad9-Rad1-Hus1 interacts with and stimulates NEIL1 glycosylase. Nucleic Acids Res. 35, 2463-2472 (Pubitemid 47073661)
36. Whitfield, M. L., Sherlock, G., Saldanha, A. J., Murray, J. I., Ball, C. A., Alexander, K. E., Matese, J. C., Perou, C. M., Hurt, M. M., Brown, P. O., and Botstein, D. (2002) Identification of genes periodically expressed in the human cell cycle and their expression in tumors. Mol. Biol. Cell 13, 1977-2000 (Pubitemid 34651487)
37. Chattopadhyay, R., Das, S., Maiti, A. K., Boldogh, I., Xie, J., Hazra, T. K., Kohno, K., Mitra, S., and Bhakat, K. K. (2008) Regulatory role of human AP-endonuclease (APE1/Ref-1) in YB-1-mediated activation of the multidrug resistance gene MDR1. Mol. Cell. Biol. 28, 7066-7080
38. Romero, P., Obradovic, Z., Li, X., Garner, E. C., Brown, C. J., and Dunker, A. K. (2001) Sequence complexity of disordered protein. Proteins 42, 38-48
39. Hegde, M. L., Hazra, T. K., and Mitra, S. (2010) Functions of disordered regions in mammalian early base excision repair proteins. Cell. Mol. Life Sci. 67, 3573-3587
40. Yang, J. T., Wu, C. S., and Martinez, H. M. (1986) Calculation of protein conformation from circular dichroism. Methods Enzymol. 130, 208-269
41. Johansson, H., Svensson, F., Runnberg, R., Simonsson, T., and Simonsson, S. (2010) Phosphorylated nucleolin interacts with translationally controlled tumor protein during mitosis and with Oct4 during interphase in ES cells. PloS One 5, e13678
42. Fredriksson, S., Gullberg, M., Jarvius, J., Olsson, C., Pietras, K., Gústafsdóttir, S. M., Ostman, A., and Landegren, U. (2002) Protein detection using proximity-dependent DNA ligation assays. Nat. Biotechnol. 20, 473-477 (Pubitemid 34495933)
43. Mandal, S. M., Hegde, M. L., Chatterjee, A., Hegde, P. M., Szczesny, B., Banerjee, D., Boldogh, I., Gao, R., Falkenberg, M., Gustafsson, C. M., Sarkar, P. S., and Hazra, T. K. (2012) Role of human DNA glycosylase Nei-like 2 (NEIL2) and single-strand break repair protein polynucleotide kinase 3′-phosphatase in maintenance of mitochondrial genome. J. Biol. Chem. 287, 2819-2829
44. Douki, T., Laporte, G., and Cadet, J. (2003) Interstrand photoproducts are produced in high yield within A-DNA exposed to UVC radiation. Nucleic Acids Res. 31, 3134-3142 (Pubitemid 37441773)
45. Cadet, J., Sage, E., and Douki, T. (2005) Ultraviolet radiation-mediated damage to cellular DNA. Mutat. Res. 571, 3-17 (Pubitemid 40313428)
46. Otterlei, M., Warbrick, E., Nagelhus, T. A., Haug, T., Slupphaug, G., Akbari, M., Aas, P. A., Steinsbekk, K., Bakke, O., and Krokan, H. E. (1999) Postreplicative base excision repair in replication foci. EMBO J. 18, 3834-3844 (Pubitemid 29308862)
47. Sengupta, S., Mantha, A. K., Mitra, S., and Bhakat, K. K. (2011) Human AP endonuclease (APE1/Ref-1) and its acetylation regulate YB-1-p300 recruitment and RNA polymerase II loading in the drug-induced activation of multidrug resistance gene MDR1. Oncogene 30, 482-493
48. Hill, J. W., Hazra, T. K., Izumi, T., and Mitra, S. (2001) Stimulation of human 8-oxoguanine-DNA glycosylase by AP-endonuclease: potential coordination of the initial steps in base excision repair. Nucleic Acids Res. 29, 430-438 (Pubitemid 32060930)
49. Vizlin-Hodzic, D., Runnberg, R., Ryme, J., Simonsson, S., and Simonsson, T. (2011) SAF-A forms a complex with BRG1, and both components are required for RNA polymerase II-mediated transcription. PloS One 6, e28049
50. Polo, S. E., Blackford, A. N., Chapman, J. R., Baskcomb, L., Gravel, S., Rusch, A., Thomas, A., Blundred, R., Smith, P., Kzhyshkowska, J., Dobner, T., Taylor, A. M., Turnell, A. S., Stewart, G. S., Grand, R. J., and Jackson, S. P. (2012) Regulation of DNA end resection by hnRNPU-like proteins promotes DNA double-strand break signaling and repair. Mol. Cell 45, 505-516