Natural antisense transcript for hyaluronan synthase 2 (HAS2-AS1) induces transcription of HAS2 via protein O-GlcNAcylation

Journal of Biological Chemistry

Volumn 289, Issue 42, 2014, Pages 28816-28826

  Vigetti, Davide ^a   Deleonibus, Sara ^a   Moretto, Paola ^a   Bowen, Timothy ^b   Fischer, Jens W ^c   Grandoch, Maria ^c   Oberhuber, Alexander ^c   Love, Dona C ^d   Hanover, John A ^d   Cinquetti, Raffaella ^a   Karousou, Eugenia ^a   Viola, Manuela ^a   D'Angelo, Maria Luisa ^a   Hascall, Vincent C ^e   De Luca, Giancarlo ^a   Passi, Alberto ^a  

^a UNIVERSITY OF INSUBRIA   (Italy)

^b CARDIFF UNIVERSITY   (United Kingdom)

^c UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

^d NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^e LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLATION; CHROMOSOMES; DISEASES; ENZYMES; GLUCOSE; HYALURONIC ACID; MUSCLE; PROTEINS;

BIOSYNTHETIC PATHWAY; CHROMATIN STRUCTURE; CYTOSOLIC PROTEINS; EPIGENETIC MODIFICATION; HUMAN AORTIC SMOOTH MUSCLE CELLS; MICROENVIRONMENTS; N-ACETYLGLUCOSAMINE; VASCULAR PATHOLOGY;

TRANSCRIPTION;

COMPLEMENTARY RNA; HYALURONAN SYNTHASE 2; HYALURONAN SYNTHASE 3; N ACETYLGLUCOSAMINE; N ACETYLLACTOSAMINE SYNTHASE; SYNAPTOTAGMIN I; SYNTHETASE; UNCLASSIFIED DRUG; CHROMATIN; GLUCURONOSYLTRANSFERASE; HAS2 PROTEIN, HUMAN; HAS2 PROTEIN, MOUSE; MESSENGER RNA; MONOSACCHARIDE; N ACETYLGLUCOSAMINYLTRANSFERASE; O-GLCNAC TRANSFERASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHROMATIN STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME BINDING; ENZYME INDUCTION; ENZYME INHIBITION; GENE; GENE EXPRESSION; GENE INTERACTION; GENETIC TRANSCRIPTION; HAS2 GENE; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; RNA STABILITY; TRANSCRIPTION INITIATION; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; AORTA; BIOLOGICAL MODEL; CELL NUCLEUS; CHEMISTRY; CHROMATIN; CYTOPLASM; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC EPIGENESIS; GENETICS; KNOCKOUT MOUSE; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROMOTER REGION; SMOOTH MUSCLE FIBER;

ACETYLGLUCOSAMINE; ANIMALS; AORTA; BASE SEQUENCE; CELL NUCLEUS; CHROMATIN; CYTOPLASM; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE SILENCING; GLUCURONOSYLTRANSFERASE; HUMANS; MALE; MICE; MICE, KNOCKOUT; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; MONOSACCHARIDES; MYOCYTES, SMOOTH MUSCLE; N-ACETYLGLUCOSAMINYLTRANSFERASES; PROMOTER REGIONS, GENETIC; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

EID: 84908052393     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.597401     Document Type: Article

References (56)

1. Jiang, D., Liang, J., and Noble, P. W. (2011) Hyaluronan as an immune regulator in human diseases. Physiol. Rev. 91, 221-264
2. Vigetti, D., Karousou, E., Viola, M., Deleonibus, S., De Luca, G., and Passi, A. (2014) Hyaluronan: biosynthesis and signaling. Biochim. Biophys. Acta 1840, 2452-2459
3. Tammi, R. H., Passi, A. G., Rilla, K., Karousou, E., Vigetti, D., Makkonen, K., and Tammi, M. I. (2011) Transcriptional and post-translational regulation of hyaluronan synthesis. FEBS J. 278, 1419-1428
4. Vigetti, D., Viola, M., Karousou, E., De Luca, G., and Passi, A. (2014) Metabolic control of hyaluronan synthases. Matrix Biol. 35, 8-13
5. Ross, R. (1999) Atherosclerosis: an inflammatory disease. N. Engl. J. Med. 340, 115-126
6. Vigetti, D., Moretto, P., Viola, M., Genasetti, A., Rizzi, M., Karousou, E., Pallotti, F., De Luca, G., and Passi, A. (2006) Matrix metalloproteinase 2 and tissue inhibitors of metalloproteinases regulate human aortic smooth muscle cell migration during in vitro aging. FASEB J. 20, 1118-1130
7. Riessen, R., Wight, T. N., Pastore, C., Henley, C., and Isner, J. M. (1996) Distribution of hyaluronan during extracellular matrix remodeling in human restenotic arteries and balloon-injured rat carotid arteries. Circulation 93, 1141-1147
8. Chai, S., Chai, Q., Danielsen, C. C., Hjorth, P., Nyengaard, J. R., Ledet, T., Yamaguchi, Y., Rasmussen, L. M., and Wogensen, L. (2005) Overexpression of hyaluronan in the tunica media promotes the development of atherosclerosis. Circ. Res. 96, 583-591
9. Cuff, C. A., Kothapalli, D., Azonobi, I., Chun, S., Zhang, Y., Belkin, R., Yeh, C., Secreto, A., Assoian, R. K., Rader, D. J., and Puré, E. (2001) The adhesion receptor CD44 promotes atherosclerosis by mediating inflammatory cell recruitment and vascular cell activation. J. Clin. Invest. 108, 1031-1040
10. Vigetti, D., Viola, M., Karousou, E., Genasetti, A., Rizzi, M., Clerici, M., Bartolini, B., Moretto, P., De Luca, G., and Passi, A. (2008) Vascular pathology and the role of hyaluronan. Scientific World Journal 8, 1116-1118
11. Vigetti, D., Rizzi, M., Moretto, P., Deleonibus, S., Dreyfuss, J. M., Karousou, E., Viola, M., Clerici, M., Hascall, V. C., Ramoni, M. F., De Luca, G., and Passi, A. (2011) Glycosaminoglycans and glucose prevent apoptosis in 4-methylumbelliferone-treated human aortic smooth muscle cells. J. Biol. Chem. 286, 34497-34503
12. Vigetti, D., Rizzi, M., Viola, M., Karousou, E., Genasetti, A., Clerici, M., Bartolini, B., Hascall, V. C., De Luca, G., and Passi, A. (2009) The effects of 4-methylumbelliferone on hyaluronan synthesis, MMP2 activity, proliferation, and motility of human aortic smooth muscle cells. Glycobiology 19, 537-546
13. Nigro, J., Osman, N., Dart, A. M., and Little, P. J. (2006) Insulin resistance and atherosclerosis. Endocr. Rev. 27, 242-259
14. Brownlee, M. (2001) Biochemistry and molecular cell biology of diabetic complications. Nature 414, 813-820
15. Copeland, R. J., Bullen, J. W., and Hart, G. W. (2008) Cross-talk between GlcNAcylation and phosphorylation: roles in insulin resistance and glucose toxicity. Am. J. Physiol. Endocrinol. Metab. 295, E17-E28
16. Vigetti, D., Deleonibus, S., Moretto, P., Karousou, E., Viola, M., Bartolini, B., Hascall, V. C, Tammi, M., De Luca, G., and Passi, A. (2012) Role of UDP-N-acetylglucosamine (GlcNAc) and O-GlcNAcylation of hyaluronan synthase 2 in the control of chondroitin sulfate and hyaluronan synthesis. J. Biol. Chem. 287, 35544-35555
17. Vigetti, D., Ori, M., Viola, M., Genasetti, A., Karousou, E., Rizzi, M., Pallotti, F., Nardi, I., Hascall, V. C., De Luca, G., and Passi, A. (2006) Molecular cloning and characterization of UDP-glucose dehydrogenase from the amphibian Xenopus laevis and its involvement in hyaluronan synthesis. J. Biol. Chem. 281, 8254-8263
18. Jokela, T. A., Makkonen, K. M., Oikari, S., Kärnä, R., Koli, E., Hart, G. W., Tammi, R. H, Carlberg, C., and Tammi, M. I. (2011) Cellular content of UDP-N-acetylhexosamines controls hyaluronan synthase 2 expression and correlates with O-GlcNAc modification of transcription factors YY1 and SP1. J. Biol. Chem. 286, 33632-33640
19. Hart, G. W., Housley, M. P., and Slawson, C. (2007) Cycling of O-linked β-N-acetylglucosamine on nucleocytoplasmic proteins. Nature 446, 1017-1022
20. Buse, M. G. (2006) Hexosamines, insulin resistance, and the complications of diabetes: current status. Am. J. Physiol. Endocrinol. Metab. 290, E1-E8
21. Slawson, C, Copeland, R. J., and Hart, G. W. (2010) O-GlcNAc signaling: a metabolic link between diabetes and cancer? Trends Biochem. Sci. 35, 547-555
22. Hanover, J. A., Krause, M. W., and Love, D. C. (2012) Bittersweet memories: linking metabolism to epigenetics through O-GlcNAcylation. Nat. Rev. Mol. Cell Biol. 13, 312-321
23. Chao, H., and Spicer, A. P. (2005) Natural antisense mRNAs to hyaluronan synthase 2 inhibit hyaluronan biosynthesis and cell proliferation. J. Biol. Chem. 280, 27513-27522
24. Magistri, M., Faghihi, M. A., St Laurent, G., 3rd, and Wahlestedt, C (2012) Regulation of chromatin structure by long noncoding RNAs: focus on natural antisense transcripts. Trends Genet. 28, 389-396
25. Rinn, J. L., and Chang, H. Y. (2012) Genome regulation by long noncoding RNAs. Annu. Rev. Biochem. 81, 145-166
26. Wang, K. C, and Chang, H. Y. (2011) Molecular mechanisms of long noncoding RNAs. Mol. Cell 43, 904-914
27. Yoon, J. H, Abdelmohsen, K., and Gorospe, M. (2013) Posttranscriptional gene regulation by long noncoding RNA. J. Mol. Biol. 425, 3723-3730
28. Mercer, T. R., and Mattick, J. S. (2013) Structure and function of long noncoding RNAs in epigenetic regulation. Nat. Struct. Mol. Biol. 20, 300-307
29. Lee, J. T. (2012) Epigenetic regulation by long noncoding RNAs. Science 338, 1435-1439
30. Faghihi, M. A., and Wahlestedt, C (2009) Regulatory roles of natural antisense transcripts. Nat Rev. Mol. Cell Biol. 10, 637-643
31. Michael, D. R., Phillips, A. O., Krupa, A., Martin, J., Redman, J. E., Altaher, A., Neville, R. D., Webber, J., Kim, M. Y., and Bowen, T. (2011) The human hyaluronan synthase 2 (HAS2) gene and its natural antisense RNA exhibit coordinated expression in the renal proximal tubular epithelial cell. J. Biol. Chem. 286, 19523-19532
32. Faghihi, M. A., Modarresi, F., Khalil, A. M., Wood, D. E., Sahagan, B. G., Morgan, T. E., Finch, C. E., St Laurent, G., 3rd, Kenny, P. J., and Wahlestedt, C. (2008) Expression of a noncoding RNA is elevated in Alzheimer's disease and drives rapid feed-forward regulation of β-secretase. Nat. Med. 14, 723-730
33. Vigetti, D., Clerici, M., Deleonibus, S., Karousou, E., Viola, M., Moretto, P., Heldin, P., Hascall, V. C, De Luca, G., and Passi, A. (2011) Hyaluronan synthesis is inhibited by adenosine monophosphate-activated protein kinase through the regulation of HAS2 activity in human aortic smooth muscle cells. J. Biol. Chem. 286, 7917-7924
34. Raman, P., Krukovets, I., Marinic, T. E., Bornstein, P., and Stenina, O. I. (2007) Glycosylation mediates up-regulation of a potent antiangiogenic and proatherogenic protein, thrombospondin-1, by glucose in vascular smooth muscle cells. J. Biol. Chem. 282, 5704-5714
35. Schreck, R., Meier, B., Männel, D. N., Dröge, W., and Baeuerle, P. A. (1992) Dithiocarbamates as potent inhibitors of nuclear factor "B activation in intact cells. J. Exp. Med. 175, 1181-1194
36. Vigetti, D., Genasetti, A., Karousou, E., Viola, M., Moretto, P., Clerici, M., Deleonibus, S., De Luca, G., Hascall, V C, and Passi, A. (2010) Proinflammatory cytokines induce hyaluronan synthesis and monocyte adhesion in human endothelial cells through hyaluronan synthase 2 (HAS2) and the nuclear factor-"B (NF-kB) pathway. J. Biol. Chem. 285, 24639-24645
37. Yang, Y. R., Song, M., Lee, H., Jeon, Y., Choi, E. J., Jang, H. J., Moon, H. Y., Byun, H. Y., Kim, E. K., Kim, D. H., Lee, M. N., Koh, A., Ghim, J., Choi, J. H, Lee-Kwon, W., Kim, K. T., Ryu, S. H, and Suh, P. G. (2012) O-GlcNAcase is essential for embryonic development and maintenance of genomic stability. Aging Cell 11, 439-448
38. Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-AAC (T)) method. Methods 25, 402-408
39. Makkonen, K. M., Pasonen-Seppänen, S., Törrönen, K., Tammi, M. I., and Carlberg, C. (2009) Regulation of the hyaluronan synthase 2 gene by convergence in cyclic AMP response element-binding protein and retinoid acid receptor signaling. J. Biol. Chem. 284, 18270-18281
40. Love, D. C, Ghosh, S., Mondoux, M. A., Fukushige, T., Wang, P., Wilson, M. A., Iser, W. B., Wolkow, C. A., Krause, M. W., and Hanover, J. A. (2010) Dynamic O-GlcNAc cycling at promoters of Caenorhabditis elegans genes regulating longevity, stress, and immunity. Proc. Natl. Acad. Sci. U. S. A. 107, 7413-7418
41. Wang, I. C, Chen, Y. J., Hughes, D., Petrovic, V., Major, M. L., Park, H. J., Tan, Y., Ackerson, T., and Costa, R. H. (2005) Forkhead box M1 regulates the transcriptional network of genes essential for mitotic progression and genes encoding the SCF (Skp2-Cks1) ubiquitin ligase. Mol. Cell. Biol. 25, 10875-10894
42. Rao, S., Procko, E., and Shannon, M. F. (2001) Chromatin remodeling, measured by a novel real-time polymerase chain reaction assay, across the proximal promoter region of the IL-2 gene. J. Immunol. 167, 4494-4503
43. Yuan, W., Wu, T., Fu, H, Dai, C, Wu, H, Liu, N., Li, X., Xu, M., Zhang, Z., Niu, T., Han, Z., Chai, J., Zhou, X. J., Gao, S., and Zhu, B. (2012) Dense chromatin activates Polycomb repressive complex 2 to regulate H3 lysine 27 methylation. Science 337, 971-975
44. Ozcan, S., Andrali, S. S., and Cantrell, J. E. (2010) Modulation of transcription factor function by O-GlcNAc modification. Biochim. Biophys. Acta 1799, 353-364
45. Allison, D. F., Wamsley, J. J., Kumar, M., Li, D., Gray, L. G., Hart, G. W., Jones, D. R., and Mayo, M. W. (2012) Modification of RelA by O-linked N-acetylglucosamine links glucose metabolism to NF-kB acetylation and transcription. Proc. Natl. Acad. Sci. U. S. A. 109, 16888-16893
46. Slawson, C, and Hart, G. W. (2011) O-GlcNAc signalling: implications for cancer cell biology. Nat. Rev. Cancer 11, 678-684
47. Sakabe, K., Wang, Z., and Hart, G. W. (2010) β-N-Acetylglucosamine (O-GlcNAc) is part of the histone code. Proc. Natl. Acad. Sci. U. S. A. 107, 19915-19920
48. Zhang, S., Roche, K., Nasheuer, H. P., and Lowndes, N. F. (2011) Modification of histones by sugar β-N-acetylglucosamine (GlcNAc) occurs on multiple residues, including histone H3 serine 10, and is cell cycle-regulated. J. Biol. Chem. 286, 37483-37495
49. Chi, P., Allis, C. D., and Wang, G. G. (2010) Covalent histone modifications: miswritten, misinterpreted and mis-erased in human cancers. Nat. Rev. Cancer 10, 457-469
50. Bannister, A. J., and Kouzarides, T. (2011) Regulation of chromatin by histone modifications. Cell Res. 21, 381-395
51. Chen, Q., Chen, Y., Bian, C, Fujiki, R., and Yu, X. (2013) TET2 promotes histone O-GlcNAcylation during gene transcription. Nature 493, 561-564
52. Deplus, R., Delatte, B., Schwinn, M. K., Defrance, M., Méndez, J., Murphy, N., Dawson, M. A., Volkmar, M., Putmans, P., Calonne, E., Shih, A. H., Levine, R. L., Bernard, O., Mercher, T., Solary, E., Urh, M., Daniels, D. L., and Fuks, F. (2013) TET2 and TET3 regulate GlcNAcylation and H3K4 methylation through OGT and SET1/COM-PASS. EMBOJ. 32, 645-655
53. Tahiliani, M., Koh, K. P., Shen, Y., Pastor, W. A., Bandukwala, H., Brudno, Y., Agarwal, S., Iyer, L. M., Liu, D. R., Aravind, L., and Rao, A. (2009) Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324, 930-935
54. Bernstein, E., and Allis, C. D. (2005) RNA meets chromatin. Genes Dev. 19, 1635-1655
55. Du, Z., Fei, T., Verhaak, R. G., Su, Z., Zhang, Y., Brown, M., Chen, Y., and Liu, X. S. (2013) Integrative genomic analyses reveal clinically relevant long noncoding RNAs in human cancer. Nat. Struct. Mol. Biol. 20, 908-913
56. Yang, W. H., Park, S. Y., Nam, H. W., Kim do, H., Kang, J. G., Kang, E. S., Kim, Y. S., Lee, H. C, Kim, K. S., and Cho, J. W. (2008) NFkB activation is associated with its O-GlcNAcylation state under hyperglycemic conditions. Proc. Natl. Acad. Sci. U. S. A. 105, 17345-17350