Response of heterogeneous ribonuclear proteins (hnRNP) to ionising radiation and their involvement in DNA damage repair

International Journal of Radiation Biology

Volumn 85, Issue 8, 2009, Pages 643-655

  Haley, Benjamin ^a   Paunesku, Tatjana ^a   Protic, Miroslava ^c   Woloschak, Gayle E ^a,b,d  

^a NORTHWESTERN UNIVERSITY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c ARGONNE NATIONAL LABORATORY   (United States)

^d NORTHWESTERN UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

DNA DSB repair; HnRNP; Homologous recombination; Radiation; Transcription factors

Indexed keywords

DNA DEPENDENT PROTEIN KINASE; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN A1; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN A18; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN A2; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN B1; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN C; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN C1; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN C2; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN D; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN E1; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN E2; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN H1; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN K; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN L; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN M; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN P2; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN U; KU ANTIGEN; MESSENGER RNA; PROTEIN P53; SMALL INTERFERING RNA; TELOMERASE REVERSE TRANSCRIPTASE; THIOREDOXIN; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE ARREST; DNA DAMAGE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; GENE EXPRESSION; HUMAN; IONIZING RADIATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEFECT; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; RADIOSENSITIVITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR PROMOTION; ULTRAVIOLET RADIATION; WESTERN BLOTTING;

ANIMALS; DNA; DNA DAMAGE; DNA REPAIR; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEINS; HUMANS; RADIATION, IONIZING; RECOMBINATION, GENETIC;

MURINAE;

EID: 68649126316     PISSN: 09553002     EISSN: 13623095     Source Type: Journal    
DOI: 10.1080/09553000903009548     Document Type: Article

References (76)

1. Abraham RT. 2004. PI 3-kinase related kinases: 'Big' players in stress-induced signaling pathways. DNA Repair 3:883-887.
2. Barenco M, Tomescu D, Brewer D, Callard R, Stark J, Hubank M. 2006. Ranked prediction of p53 targets using hidden variable dynamic modeling. Genome Biology 7:R25. (Pubitemid 43871869)
3. Barker S, Weinfeld M, Sheng J, Li L, Murray D. 2005. Identification of mammalian proteins cross-linked to DNA by ionising radiation. Journal of Biological Chemistry 280:33826-33838. (Pubitemid 41443102)
4. Beals CR, Sheridan CM, Turck CW, Gardner P, Crabtree GR. 1997. Nuclear export of NF-ATc enhanced by glycogen synthase kinase-3. Science 275:1930-1934. (Pubitemid 27148814)
5. Berggren M, Gallegos A, Gasdaska JR, Gasdaska PY, Warneke J, Powis G. 1996. Thioredoxin and thioredoxin reductase gene expression in human tumors and cell lines, and the effects of serum stimulation and hypoxia. Anticancer Research 16:3459-3466. (Pubitemid 27084998)
6. Beyer AL, Christensen ME, Walker BW, Lestourgeon WM. 1977. Identification and characterisation of the packaging proteins of core 40S hnRNP particles. Cell 11:127-138. (Pubitemid 8126060)
7. Bomsstyk K, Van Seuningen I, Susuki H, Denisenko O, Ostrowski J. 1997. Diverse molecular interactions of the hnRNP K protein. FEBS Letters 403:113-115. (Pubitemid 27081476)
8. Bullock AN, Fersht AR. 2001. Rescuing the function of mutant p 53. Nature Reviews Cancer 1:68-76.
9. Burd CG, Swanson MS, Gorlach M, Dreyfuss G. 1989. Primary structures of the heterogeneous nuclear ribonucleoprotein A2, B1, and C2 proteins: A diversity of RNA binding proteins is generated by small peptide inserts. Proceedings of the National Academy of Sciences of the USA 86:9788-9792. (Pubitemid 20030719)
10. Caceres JF, Stamm S, Helfman DM, Krainer AR. 1994. Regulation of alternative splicing in vivo by overexpression of antagonistic splicing factors. Science 265:1706-1709. (Pubitemid 24314901)
11. Calvio C, Neubauer G, Mann M, Lamond AI. 1995. Identification of hnRNP P2 as TLS/FUS using electrospray mass spectrometry. RNA 1:724-733.
12. Crosat A, Aman P, Mandahl N, Ron D. 1993. Fusion of CHOP to a novel RNA-binding protein in human myxoid liposarcoma. Nature 363:640-644. (Pubitemid 23227627)
13. Dai JM, Sun DC, Lin RX, Yang J, Lou S, Wang SQ. 2006. Microarray analysis of differentially expressed genes in mouse bone marrow tissues after ionising radiation. International Journal of Radiation Biology 82:511-521. (Pubitemid 44174869)
14. Dallaire F, Dupuis S, Fiset S, Chabot B. 2000. Heterogeneous nuclear ribonucleoprotein A1 and UP1 protect mammalian telomeric repeats and modulate telomere replication in vitro. Journal of Biological Chemistry 275:14509-14516. (Pubitemid 30339738)
15. Delattre O, Sucman J, Plougastel B, Desmase C, Melot T, Peter M, Kovar H, Joubert I, De Jong P, Rouleau G. 1992. Gene fusion with an ETS DNA-binding domain caused by chromosome translocation in human tumours. Nature 359:162-165.
16. Denko N, Schindler C, Koong A, Laderoute K, Green C, Giaccia A. 2000. Epigenetic regulation of gene expression in cervical cancer cells by the tumor microenvironment. Clinical Cancer Research 6:480-487. (Pubitemid 30111467)
17. Dreyfuss G, Kim VN, Kataoka N. 2002. Messenger-RNA-binding proteins and the messages they carry. Nature Reviews Molecular Cell Biology 3:195-205. (Pubitemid 37237142)
18. Dreyfuss G, Matunis MJ, Pihol-Roma S. 1993. hnRNP proteins and the biogenesis of mNA. Annual Review of Biochemistry 62:289-321.
19. Edick MJ, Cheng C, Yang W, Cheok M, Wilkinson MR, Pei D, Evans WE, Kun LE, Pui CH, Relling MV. 2005. Lymphoid gene expression as a predictor of risk of secondary brain tumors. Genes Chromosomes and Cancer 42:107-116. (Pubitemid 40094094)
20. Efeyan A, Serrano M. 2007. p53: Guardian of the genome and policeman of the oncogenes. Cell Cycle 6:1006-1010. (Pubitemid 46708570)
21. Fanning E, Klimovich V, Nager AR. 2006. A dynamic model for replication protein A (RPA) function in DNA processing pathways. Nucleic Acids Research 34:4126. (Pubitemid 44542191)
22. Fiset S, Chabot B. 2001. hnRNP A1 may interact simultaneously with telomeric DNA and the human telomerase RNA in vitro. Nucleic Acids Research 29:2268-2275. (Pubitemid 32514929)
23. Ford LP, Suh JM, Wright WE, Shay JW. 2000. Heterogeneous nuclear ribonucleoproteins C1 and C2 associate with the RNA component of human telomerase. Molecular and Cellular Biology 20:9084-9091. (Pubitemid 32245937)
24. Fornace AJ, Alamo I, Hollander MC. 1988. DNA damage-inducible transcripts in mammalian cells. Proceedings of the National Academy of Sciences of the USA 85:8800-8804. (Pubitemid 19001796)
25. Funasaka Y, Ichihashi M. 1997. The effect of ultraviolet B induced adult T cell leukemia-derived factor/thioredoxin (ADF/TRX) on survival and growth of human melanocytes. Pigment Cell Research 10:68-73. (Pubitemid 127526197)
26. Gamble SC, Dunn MJ, Wheeler CH, Joiner MC, Adu-Poku A, Arrand JE. 2000. Expression of proteins coincident with inducible radioprotection in human lung epithelial cells. Cancer Research 60:2146-2151. (Pubitemid 30225176)
27. Goto Y, Sueoka E, Chiba H, Fujiki H. 1999. Significance of heterogeneous nuclear ribonucleoprotein B1 as a new early detection marker for oral squamous cell carcinoma. Japanese Journal of Cancer Research 90:1358-1363. (Pubitemid 30032075)
28. Grogan TM, Fenoglio-Prieser C, Seheb R, Bellamy W, Frutiger Y, Vela E, Stemmerman G, Macdonald J, Richter L, Gallegos A. 2000. Thioredoxin, a putative oncogene product, is overexpressed in gastric carcinoma and associated with increased proliferation and increased cell survival. Human Pathology 31:475-481. (Pubitemid 30262870)
29. Guil S, Long JC, Cáceres JF. 2006. hnRNP A1 Relocalisation to the stress granules reflects a role in the stress response. Molecular and Cellular Biology 26:5744-5758. (Pubitemid 44134331)
30. Hamasaki M, Kamma H, Wu W, Kaneko S, Fujiwara M, Satoh H, Haraoka S, Kikuchi M, Shirakusa T. 2001. Expression of hnRNP B1 in four major histological types of lung cancers. Anticancer Research 21:979-984. (Pubitemid 32494196)
31. Henning W, Stürsbecher HW. 2003. Homologous recombination and cell cycle checkpoints: Rad51 in tumour progression and therapy resistance. Toxicology 193:91-109. (Pubitemid 37340146)
32. Iwanaga K, Sueoka N, Sato A, Hayashi S, Sueoka E. 2005. Heterogeneous nuclear ribonucleoprotein B1 protein impairs DNA repair mediated through the inhibition of DNA-dependent protein kinase activity. Biochemical and Biophysical Research Communications 333:888-895. (Pubitemid 40854242)
33. Jen KY, Cheung VG. 2003. Transcriptional response of lymphoblastoid cells to ionising radiation. Genome Research 13:2092-2100. (Pubitemid 37161766)
34. Kamma H, Horiguchi H, Wan L, Matsui M, Fujiwara M, Fujimoto M, Yasawa T, Dreyfuss G. 1999. Molecular characterisation of the hnRNP A2/B1 proteins: Tissue-specific expression and novel isoforms. Experimental Cell Research 246:399-411. (Pubitemid 29394003)
35. Khodarev NN, Park JO, Yu J, Gupta N, Nodsenski E, Roisman B, Weichselbaum RR. 2001. Dose-dependent and independent temporal patterns of gene responses to ionising radiation in normal and tumor cells and tumor xenografts. Proceedings of the National Academy of Sciences of the USA 98:12665-12670. (Pubitemid 33020003)
36. Kiledjian M, Dreyfuss G. 1992. Primary structure and binding activity of the hnRNP U protein: Binding RNA through RGG box. EMBO Journal 11:2655-2664.
37. Kim L, Kimmel AR. 2000. GSK3, a master switch regulating cell-fate specification and tumorigenesis. Current Opinion Genetic Development 10:508-514. (Pubitemid 30683345)
38. Klimek-Tomcsak K, Wyrwics LS, Jain S, Bomsstyk K, Ostrowski J. 2004. Characterisation of hnRNP K protein-RNA interactions. Journal of Molecular Biology 342:1131-1141.
39. Krecic AM, Swanson MS. 1999. hnRNP complexes: Composition, structure, and function. Current Opinion Cell Biology 11:363-371. (Pubitemid 29273808)
40. Kuroda M, Sok J, Webb L, Baechtold H, Urano F, Yin Y, Chung P, De Rooij DG, Akhmedov A, Ashley T. 2000. Male sterility and enhanced radiation sensitivity in TLS-/-mice. EMBO Journal 19:453-462. (Pubitemid 30072615)
41. Labranche H, Dupuis S, Ben-David Y, Bani MR, Wellinger RJ, Chabot B. 1998. Telomere elongation by hnRNP A1 and a derivative that interacts with telomeric repeats and telomerase. Nature Genetics 19:199-202. (Pubitemid 28253328)
42. Lane DP. 1992. p 53, guardian of the genome. Nature 358:15-16.
43. Lécuyer E, Yoshida H, Parthasarathy N, Alm C, Babak T, Cerovina T, Hughes TR, Tomancak P, Krause HM. 2007. Global analysis of mRNA localisation reveals a prominent role in organising cellular architecture and function. Cell 131:174-187. (Pubitemid 47498530)
44. Lee SY, Park JH, Kim S, Park EJ, Yun Y, Kwon J. 2005. A proteomics approach for the identification of nucleophosmin and heterogeneous nuclear ribonucleoprotein C1/C2 as chromatin-binding proteins in response to DNA double-strand breaks. Biochemistry Journal 388:7-15. (Pubitemid 40732927)
45. Lin S, Lim S, Viani MA, Sapp M, Lim MS. 2001. Down-regulation of telomerase activity in malignant lymphomas by radiation and chemotherapeutic agents. American Journal of Pathology 159:711-719. (Pubitemid 32751101)
46. Ljungman M. 2007. The transcription stress response. Cell Cycle 6:2252-2257.
47. Matsuyama S, Goto Y, Sueoka N, Ohkura Y, Tanaka Y, Nakachi K, Sueoka E. 2000. Heterogeneous nuclear ribonucleoprotein B1 expressed in esophageal squamous cell carcinomas as a new biomarker for diagnosis. Cancer Science 91:658-663. (Pubitemid 30453795)
48. Mattick JS. 2003. Challenging the dogma: The hidden layer of non-protein-coding RNAs in complex organisms. BioEssays 25:930-939.
49. Mayeda A, Krainer AR. 1992. Regulation of alternative pre-mRNA splicing by hnRNP A1 and splicing factor SF2. Cell 68:365-375.
50. Moumen A, Masterson P, O'Connor MJ, Jackson SP. 2005. hnRNP K: An HDM2 target and transcriptional coactivator of p53 in response to DNA damage. Cell 123:1065-1078. (Pubitemid 41785421)
51. Nishiyama H, Itoh K, Kaneko Y, Kishishita M, Yoshida O, Fujita J. 1997. A Glycine-rich RNA-binding protein mediating cold-inducible suppression of mammalian cell growth. Journal of Cell Biology 137:899-908. (Pubitemid 27215512)
52. Pino I, Pio R, Toledo G, Sabalegui N, Vicent S, Rey N, Losano MD, Torre W, Garcia-Foncillas J, Montuenga LM. 2003. Altered patterns of expression of members of the heterogeneous nuclear ribonucleoprotein (hnRNP) family in lung cancer. Lung Cancer 41:131-143. (Pubitemid 36842776)
53. Pinol-Roma S, Dreyfuss G. 1992. Shuttling of pre-mRNA binding proteins between nucleus and cytoplasm. Nature 355:730-732.
54. Rabbitts TH, Forster A, Larson R, Nathan P. 1993. Fusion of the dominant negative transcription regulator CHOP with a novel gene FUS by translocation t (12; 16) in malignant liposarcoma. Nature Genetics 4:175-180. (Pubitemid 23179103)
55. Rundhaug JE, Hawkins KA, Pavone A, Gaddis S, Kil H, Klein RD, Berton TR, Mccauley E, Johnson DG, Lubet RA. 2005. SAGE profiling of UV-induced mouse skin squamous cell carcinomas, comparison with acute UV irradiation effects. Molecular Carcinogenesis 42:40-52. (Pubitemid 40041484)
56. San Filippo J, Sung P, Klein H. 2008. Mechanism of eukaryotic homologous recombination. Annual Review of Biochemistry 77:229-257.
57. Sheikh MS, Carrier F, Papathanasiou MA, Hollander MC, Shan Q, Yu K, Fornace AJ. 1997. Identification of several human homologs of hamster DNA damage-inducible transcripts cloning and characterisation of a novel UV-inducible cDNA that codes for a putative RNA-binding protein. Journal of Biological Chemistry 272:26720-26726. (Pubitemid 27458899)
58. Sheikh MS, Fornace AJ Jr. 1999. Regulation of translation initiation following stress. Oncogene 18:6121-6128.
59. Shiloh Y, Andegeko Y, Tsarfaty I. 2004. In search of drug treatment for genetic defects in the DNA damage response: The example of ataxia- telangiectasia. Seminal Cancer Biology 14:295-305.
60. Shyu AB, Wilkinson MF. 2000. The double lives of shuttling mRNA binding proteins. Cell 102:135-138.
61. Sonoda E, Hochegger H, Saberi A, Taniguchi Y, Takeda S. 2006. Differential usage of non-homologous end-joining and homologous recombination in double strand break repair. DNA Repair 5:1021-1029. (Pubitemid 44291617)
62. Sueoka E, Goto Y, Sueoka N, Kai Y, Kosu T, Fujiki H. 1999. Heterogeneous nuclear ribonucleoprotein B1 as a new marker of early detection for human lung cancers. Cancer Research 59:1404-1407. (Pubitemid 29160099)
63. Sueoka E, Sueoka N, Goto Y, Matsuyama S, Nishimura H, Sato M, Fujimura S, Chiba H, Fujiki H. 2001. Heterogeneous nuclear ribonucleoprotein B1 as early cancer biomarker for occult cancer of human lungs and bronchial dysplasia. Cancer Research 61:1896-1902. (Pubitemid 32692005)
64. Takao J, Ariisumi K, Dougherty II, Crus PD. 2002. Genomic scale analysis of the human keratinocyte response to broadband ultraviolet-B irradiation. Photodermatology Photoimmunology and Photomedicine 18:5-13. (Pubitemid 34555447)
65. Van Der Houven Van Oordt W, Dias-Meco MT, Losano J, Krainer AR, Moscat J, Caceres JF. 2000. The MKK3/6-p38-signaling cascade alters the subcellular distribution of hnRNP A1 and modulates alternative splicing regulation. Journal of Cell Biology 149:307-316. (Pubitemid 30227149)
66. Ward JF. 1988. DNA damage produced by ionising radiation in mammalian cells: Identities, mechanisms of formation, and reparability. Progress in Nucleic Acid Research and Molecular Biology 35:95-125.
67. Waterhouse N, Kumar S, Song Q, Strike P, Sparrow L, Dreyfuss G, Alnemri ES, Litwack G, Lavin M, Watters D. 1996. Heteronuclear ribonucleoproteins C1 and C2, components of the spliceosome, are specific targets of Interleukin 1 beta-converting ensyme-like proteases in apoptosis. Journal of Biological Chemistry 271:29335-29341. (Pubitemid 26382648)
68. Weinstock DM, Richardson CA, Elliott B, Jasin M. 2006. Modeling oncogenic translocations: Distinct roles for double-strand break repair pathways in translocation formation in mammalian cells. DNA Repair 5:1065-1074. (Pubitemid 44291619)
69. Weinstock GM. 2007. ENCODE: More genomic empowerment. Genome Research 17:667-668.
70. Weller GR, Brandt VL, Roth DB. 2004. Doing more with less in bacterial DNA repair. Nature Structural & Molecular Biology 11:1158-1159.
71. Yang C, Carrier F. 2001. The UV-inducible RNA-binding protein A18 (A18 hnRNP) plays a protective role in the genotoxic stress response. Journal of Biological Chemistry 276:47277-47284. (Pubitemid 37373107)
72. Yang R, Weber DJ, Carrier F. 2006. Post-transcriptional regulation of thioredoxin by the stress inducible heterogenous ribonucleoprotein A18. Nucleic Acids Research 34: 1224.
73. Yang X, Bani M, Lu S, Rowan S, Ben-David Y, Chabot B. 1994. The A1 and A1B proteins of heterogeneous nuclear ribonucleoparticles modulate 5′ splice site selection in vivo. Proceedings of the National Academy of Sciences of the USA 91:6924-6928. (Pubitemid 24984968)
74. Yim EK, Lee KH, Kim CJ, Park JS. 2006. Analysis of differential protein expression by cisplatin treatment in cervical carcinoma cells. International Journal of Gynecological Cancer 16:690-697.
75. Yokomiso A, Ono M, Nanri H, Makino Y, Ohga T, Wada M, Okamoto T, Yodoi J, Kuwano M, Kohno K. 1995. Cellular levels of thioredoxin associated with drug sensitivity to cisplatin, mitomycin C, doxorubicin, and etoposide. Cancer Research 55:4293-4296.
76. Shang S, Schlott B, Görlach M, Grosse F, Journals O. 2004. DNA-dependent protein kinase (DNA-PK) phosphorylates nuclear DNA helicase II/RNA helicase A and hnRNP proteins in an RNA-dependent manner. Nucleic Acids Research 32: 1-10.