QKI-mediated alternative splicing of the histone variant MacroH2A1 regulates cancer cell proliferation

Molecular and Cellular Biology

Volumn 31, Issue 20, 2011, Pages 4244-4255

  Novikov, Leonid ^a   Park, Jong Woo ^a   Chen, Hongshan ^a   Klerman, Hadassa ^a   Jalloh, Abubakar S ^a   Gamble, Matthew J ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H2A; HISTONE H2A1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PROTEIN QKI; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; HISTONE; MACROH2A HISTONE; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PARP1 PROTEIN, HUMAN; QKI PROTEIN, HUMAN; RNA BINDING PROTEIN; RNA PRECURSOR;

ALTERNATIVE RNA SPLICING; ARTICLE; CANCER CELL; CANCER GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; GENE EXPRESSION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; HUMAN TISSUE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REGULATORY MECHANISM; RNA INTERFERENCE; CELL CULTURE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NEOPLASM; TUMOR CELL LINE;

ALTERNATIVE SPLICING; CELL LINE, TUMOR; CELL PROLIFERATION; CELLS, CULTURED; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONES; HUMANS; NAD; NEOPLASMS; POLY(ADP-RIBOSE) POLYMERASES; RNA INTERFERENCE; RNA PRECURSORS; RNA-BINDING PROTEINS;

EID: 80555157615     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.05244-11     Document Type: Article

References (51)

1. Abbott, D. W., et al. 2004. Structural characterization of macroH2A containing chromatin. Biochemistry 43:1352-1359.
2. Ahel, D., et al. 2009. Poly(ADP-ribose)-dependent regulation of DNA repair by the chromatin remodeling enzyme ALC1. Science 325:1240-1243.
3. Angelov, D., et al. 2006. Nucleolin is a histone chaperone with FACT-like activity and assists remodeling of nucleosomes. EMBO J. 25:1669-1679.
4. Angelov, D., et al. 2003. The histone variant macroH2A interferes with transcription factor binding and SWI/SNF nucleosome remodeling. Mol. Cell 11:1033-1041.
5. Bieche, I., G. de Murcia, and R. Lidereau. 1996. Poly(ADP-ribose) polymerase gene expression status and genomic instability in human breast cancer. Clin. Cancer Res. 2:1163-1167.
6. Buschbeck, M., et al. 2009. The histone variant macroH2A is an epigenetic regulator of key developmental genes. Nat. Struct. Mol. Biol. 16:1074-1079.
7. Carbone, M., et al. 2008. Poly(ADP-ribosyl)ation is implicated in the G0-G1 transition of resting cells. Oncogene 27:6083-6092.
8. Castle, J. C., et al. 2008. Expression of 24,426 human alternative splicing events and predicted cis regulation in 48 tissues and cell lines. Nat. Genet. 40:1416-1425.
9. Chakravarthy, S., et al. 2005. Structural characterization of the histone variant macroH2A. Mol. Cell. Biol. 25:7616-7624.
10. Chakravarthy, S., and K. Luger. 2006. The histone variant macro-H2A preferentially forms "hybrid nucleosomes." J. Biol. Chem. 281:25522-25531.
11. Chang, E. Y., et al. 2008. MacroH2A allows ATP-dependent chromatin remodeling by SWI/SNF and ACF complexes but specifically reduces recruitment of SWI/SNF. Biochemistry 47:13726-13732.
12. Changolkar, L. N., et al. 2007. Developmental changes in histone macroH2A1-mediated gene regulation. Mol. Cell. Biol. 27:2758-2764.
13. Changolkar, L. N., et al. 2010. Genome-wide distribution of macroH2A1 histone variants in mouse liver chromatin. Mol. Cell. Biol. 30:5473-5483.
14. Chen, M., J. Zhang, and J. L. Manley. 2010. Turning on a fuel switch of cancer: hnRNP proteins regulate alternative splicing of pyruvate kinase mRNA. Cancer Res. 70:8977-8980.
15. Chevanne, M., et al. 2010. Inhibition of PARP activity by PJ-34 leads to growth impairment and cell death associated with aberrant mitotic pattern and nucleolar actin accumulation in M14 melanoma cell line. J. Cell. Physiol. 222:401-410.
16. Cohen-Armon, M. 2007. PARP-1 activation in the ERK signaling pathway. Trends Pharmacol. Sci. 28:556-560.
17. Cohen-Armon, M., et al. 2007. DNA-independent PARP-1 activation by phosphorylated ERK2 increases Elk1 activity: a link to histone acetylation. Mol. Cell 25:297-308.
18. Costanzi, C., and J. R. Pehrson. 1998. Histone macroH2A1 is concentrated in the inactive X chromosome of female mammals. Nature 393:599-601.
19. Costanzi, C., and J. R. Pehrson. 2001. MACROH2A2, a new member of the MARCOH2A core histone family. J. Biol. Chem. 276:21776-21784.
20. Counter, C. M., et al. 1998. Dissociation among in vitro telomerase activity, telomere maintenance, and cellular immortalization. Proc. Natl. Acad. Sci. U. S. A. 95:14723-14728.
21. David, C. J., and J. L. Manley. 2010. Alternative pre-mRNA splicing regulation in cancer: pathways and programs unhinged. Genes Dev. 24:2343-2364.
22. De Blasio, A., et al. 2005. Differentiative pathway activated by 3-aminobenzamide, an inhibitor of PARP, in human osteosarcoma MG-63 cells. FEBS Lett. 579:615-620.
23. Gamble, M. J., K. M. Frizzell, C. Yang, R. Krishnakumar, and W. L. Kraus. 2010. The histone variant macroH2A1 marks repressed autosomal chromatin, but protects a subset of its target genes from silencing. Genes Dev. 24:21-32.
24. Gamble, M. J., and W. L. Kraus. 2010. Multiple facets of the unique histone variant macroH2A: from genomics to cell biology. Cell Cycle 9:2566-2572.
25. Ghabreau, L., et al. 2004. Poly(ADP-ribose) polymerase-1, a novel partner of progesterone receptors in endometrial cancer and its precursors. Int. J. Cancer 109:317-321.
26. Gottschalk, A. J., et al. 2009. Poly(ADP-ribosyl)ation directs recruitment and activation of an ATP-dependent chromatin remodeler. Proc. Natl. Acad. Sci. U. S. A. 106:13770-13774.
27. Hafner, M., et al. 2010. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 141:129-141.
28. Hernandez-Munoz, I., et al. 2005. Stable X chromosome inactivation involves the PRC1 polycomb complex and requires histone MACROH2A1 and the CULLIN3/SPOP ubiquitin E3 ligase. Proc. Natl. Acad. Sci. U. S. A. 102:7635-7640.
29. Kapoor, A., et al. 2010. The histone variant macroH2A suppresses melanoma progression through regulation of CDK8. Nature 468:1105-1109.
30. Karras, G. I., et al. 2005. The macro domain is an ADP-ribose binding module. EMBO J. 24:1911-1920.
31. Katoh, M. 2008. Cancer genomics and genetics of FGFR2 (review). Int. J. Oncol. 33:233-237.
32. Kaufmann, S. H., S. Desnoyers, Y. Ottaviano, N. E. Davidson, and G. G. Poirier. 1993. Specific proteolytic cleavage of poly(ADP-ribose) polymerase: an early marker of chemotherapy-induced apoptosis. Cancer Res. 53:3976-3985.
33. Kraus, W. L. 2009. New functions for an ancient domain. Nat. Struct. Mol. Biol. 16:904-907.
34. Krishnakumar, R., et al. 2008. Reciprocal binding of PARP-1 and histone H1 at promoters specifies transcriptional outcomes. Science 319:819-821.
35. Kustatscher, G., M. Hothorn, C. Pugieux, K. Scheffzek, and A. G. Ladurner. 2005. Splicing regulates NAD metabolite binding to histone macroH2A. Nat. Struct. Mol. Biol. 12:624-625.
36. Martzen, M. R., et al. 1999. A biochemical genomics approach for identifying genes by the activity of their products. Science 286:1153-1155.
37. Nosho, K., et al. 2006. Overexpression of poly(ADP-ribose) polymerase-1 (PARP-1) in the early stage of colorectal carcinogenesis. Eur. J. Cancer. 42:2374-2381.
38. Pehrson, J. R., C. Costanzi, and C. Dharia. 1997. Developmental and tissue expression patterns of histone macroH2A1 subtypes. J. Cell Biochem. 65:107-113.
39. Prasad, S. C., P. J. Thraves, K. G. Bhatia, M. E. Smulson, and A. Dritschilo. 1990. Enhanced poly(adenosine diphosphate ribose) polymerase activity and gene expression in Ewing's sarcoma cells. Cancer Res. 50:38-43.
40. Schefe, J. H., K. E. Lehmann, I. R. Buschmann, T. Unger, and H. Funke-Kaiser. 2006. Quantitative real-time RT-PCR data analysis: current concepts and the novel "gene expression's CT difference" formula. J. Mol. Med. 84:901-910.
41. Sharma, S., T. K. Kelly, and P. A. Jones. 2010. Epigenetics in cancer. Carcinogenesis 31:27-36.
42. Shimizu, S., et al. 2004. Expression of poly(ADP-ribose) polymerase in human hepatocellular carcinoma and analysis of biopsy specimens obtained under sonographic guidance. Oncol. Rep. 12:821-825.
43. Sporn, J. C., et al. 2009. Histone macroH2A isoforms predict the risk of lung cancer recurrence. Oncogene 28:3423-3428.
44. Svotelis, A., N. Gevry, and L. Gaudreau. 2009. Regulation of gene expression and cellular proliferation by histone H2A.Z. Biochem. Cell Biol. 87:179-188.
45. Svotelis, A., N. Gevry, G. Grondin, and L. Gaudreau. 2010. H2A.Z overexpression promotes cellular proliferation of breast cancer cells. Cell Cycle 9:364-370.
46. Talbert, P. B., and S. Henikoff. 2010. Histone variants-ancient wrap artists of the epigenome. Nat. Rev. Mol. Cell Biol. 11:264-275.
47. Timinszky, G., et al. 2009. A macrodomain-containing histone rearranges chromatin upon sensing PARP1 activation. Nat. Struct. Mol. Biol. 16:923-929.
48. Tomoda, T., et al. 1991. Enhanced expression of poly(ADP-ribose) synthetase gene in malignant lymphoma. Am. J. Hematol. 37:223-227.
49. Wutz, A., T. P. Rasmussen, and R. Jaenisch. 2002. Chromosomal silencing and localization are mediated by different domains of Xist RNA. Nat. Genet. 30:167-174.
50. Yang, G., et al. 2010. RNA-binding protein quaking, a critical regulator of colon epithelial differentiation and a suppressor of colon cancer. Gastroenterology 138:231-240.e5.
51. Yin, D., et al. 2009. High-resolution genomic copy number profiling of glioblastoma multiforme by single nucleotide polymorphism DNA microarray. Mol. Cancer Res. 7:665-677.