PRMT4 is involved in insulin secretion via the methylation of histone H3 in pancreatic β cells

Journal of Molecular Endocrinology

Volumn 54, Issue 3, 2015, Pages 315-324

  Kim, Joong Kwan ^a   Lim, Yongchul ^b   Lee, Jung Ok ^a   Lee, Young Sun ^c   Won, Nam Hee ^a   Kim, Hyun ^a   Kim, Hyeon Soo ^a  

^a Korea University College of Medicine   (South Korea)

^b Samsung Medical Center   (South Korea)

^c Gachon University   (South Korea)

Author keywords

Histone H3R17; Insulin secretion; Insulin synthesis; PRMT4

Indexed keywords

BETA ACTIN; GLUCOSE; HISTONE H3; INSULIN; PROTEIN ARGININE METHYLTRANSFERASE; PROTEIN ARGININE METHYLTRANSFERASE 4; UNCLASSIFIED DRUG; COACTIVATOR-ASSOCIATED ARGININE METHYLTRANSFERASE 1; HISTONE;

ANIMAL CELL; ARTICLE; CELL LYSATE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE SILENCING; HISTONE METHYLATION; INS 1 CELL LINE; INSULIN RELEASE; INSULIN SYNTHESIS; MALE; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; C57BL MOUSE; ENZYME INDUCTION; ENZYMOLOGY; GENETICS; HAMSTER; METABOLISM; METHYLATION; PROTEIN PROCESSING; RAT; SECRETION (PROCESS); TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CRICETINAE; ENZYME INDUCTION; GLUCOSE; HISTONES; INSULIN; INSULIN-SECRETING CELLS; MALE; METHYLATION; MICE; MICE, INBRED C57BL; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-ARGININE N-METHYLTRANSFERASES; RATS;

EID: 84938526863     PISSN: 09525041     EISSN: 14796813     Source Type: Journal    
DOI: 10.1530/JME-14-0325     Document Type: Article

References (41)

1. An W, Kim J & Roeder RG 2004 Ordered cooperative functions of PRMT1, p300, and CARM1 in transcriptional activation by p53. Cell 117 735-748. (doi:10. 1016/j. cell. 2004. 05. 009)
2. Andersson AK & Sandler S 2001 Melatonin protects against streptozotocin, but not interleukin-1β-induced damage of rodent pancreatic β-cells. Journal of Pineal Research 30 157-165. (doi:10. 1034/j. 1600-079X. 2001. 300304. x). ?
3. Bauer UM, Daujat S, Nielsen SJ, Nightingale K & Kouzarides T 2002 Methylation at arginine 17 of histone H3 is linked to gene activation. EMBO Reports 3 39-44. (doi:10. 1093/embo-reports/kvf013)
4. Bedford MT & Clarke SG 2009 Protein arginine methylation in mammals: who, what, and why. Molecular Cell 33 1-13. (doi:10. 1016/j. molcel. 2008. 12. 013)
5. Carter JD, Dula SB, Corbin KL, Wu R & Nunemaker CS 2009 A practical guide to rodent islet isolation and assessment. Biological Procedures Online 11 3-31. (doi:10. 1007/s12575-009-9021-0)
6. Casadio F, Lu X, Pollock SB, LeRoy G, Garcia BA, Muir TW, Roeder RG & Allis CD 2013 H3R42me2a is a histone modification with positive transcriptional effects. PNAS 110 14894-14899. (doi:10. 1073/ pnas. 1312925110). ?
7. Chakrabarti SK, Francis J, Ziesmann SM, Garmey JC & Mirmira RG 2003 Covalent histone modifications underlie the developmental regulation of insulin gene transcription in pancreatic β cells. Journal of Biological Chemistry 278 23617-23623. (doi:10. 1074/jbc. M303423200)
8. Chen Y, Xu X, Sheng M, Zhang X, Gu Q & Zheng Z 2009 PRMT-1 and DDAHs-induced ADMA upregulation is involved in ROS-and RAS-mediated diabetic retinopathy. Experimental Eye Research 89 1028-1034. (doi:10. 1016/j. exer. 2009. 09. 004)
9. Cheng D, Côté J, Shaaban S & Bedford MT 2007 The arginine methyltransferase CARM1 regulates the coupling of transcription and mRNA processing. Molecular Cell 25 71-83. (doi:10. 1016/j. molcel. 2006. 11. 019). ?
10. Daujat S, Bauer UM, Shah V, Turner B, Berger S & Kouzarides T 2002 Crosstalk between CARM1 methylation and CBP acetylation on histone H3. Current Biology 12 2090-2097. (doi:10. 1016/S0960-9822(02)01387-8)
11. Dean PM 1973 Ultrastructural morphometry of the pancreatic β-cell. Diabetologia 9 115-119. (doi:10. 1007/BF01230690)
12. El Messaoudi S, Fabbrizio E, Rodriguez C, Chuchana P, Fauquier L, Cheng D, Theillet C, Vandel L, BedfordMT&SardetC2006 Coactivator-associated arginine methyltransferase 1 (CARM1) is a positive regulator of the cyclin E1 gene. PNAS 103 13351-13356. (doi:10. 1073/pnas. 0605692103)
13. Francis J, Chakrabarti SK, Garmey JC & Mirmira RG 2005 Pdx-1 links histone H3-Lys-4 methylation to RNA polymerase II elongation during activation of insulin transcription. Journal of Biological Chemistry 280 36244-36253. (doi:10. 1074/jbc. M505741200)
14. Frietze S, Lupien M, Silver PA & Brown M 2008 CARM1 regulates estrogenstimulated breast cancer growth through up-regulation of E2F1. Cancer Research 68 301-306. (doi:10. 1158/0008-5472. CAN-07-1983)
15. Grill V, Adamson U & Cerasi E 1978 Immediate and time-dependent effects of glucose on insulin release from rat pancreatic tissue. Evidence for different mechanisms of action. Journal of Clinical Investigation 61 1034-1043. (doi:10. 1172/JCI109002)
16. Guccione E, Bassi C, Casadio F, Martinato F, Cesaroni M, Schuchlautz H, Lüscher B & Amati B 2007 Methylation of histone H3R2 by PRMT6 and H3K4 by an MLL complex are mutually exclusive. Nature 449 933-937. (doi:10. 1038/nature06166)
17. HamidM, McCluskey JT, McClenaghan NH & Flatt PR 2002 Comparison of the secretory properties of four insulin-secreting cell lines. Endocrine Research 28 35-47. (doi:10. 1081/ERC-120004536)
18. Henquin JC 2000 Triggering and amplifying pathways of regulation of insulin secretion by glucose. Diabetes 49 1751-1760. (doi:10. 2337/ diabetes. 49. 11. 1751)
19. Hill RS & Boyd AE III 1985 Perifusion of a clonal cell line of Simian virus 40-transformed beta cells. Insulin secretory dynamics in response to glucose, 3-isobutyl-1-methylxanthine, and potassium. Diabetes 34115-120. (doi:10. 2337/diab. 34. 2. 115)
20. Iberg AN, Espejo A, Cheng D, Kim D, Michaud-Levesque J, Richard S & Bedford MT 2008 Arginine methylation of the histone H3 tail impedes effector binding. Journal of Biological Chemistry 283 3006-3010. (doi:10. 1074/jbc. C700192200)
21. Irwin N, McClean PL, Harriott P & Flatt PR 2007 Beneficial effects of sub-chronic activation of glucagon-like peptide-1 (GLP-1) receptors on deterioration of glucose homeostasis and insulin secretion in aging mice. Experimental Gerontology 42 296-300. (doi:10. 1016/j. exger. 2006. 10. 017)
22. Iwasaki H 2009 Impaired PRMT1 activity in the liver and pancreas of type 2 diabetic Goto-Kakizaki rats. Life Sciences 85 161-166. (doi:10. 1016/ j. lfs. 2009. 05. 007)
23. Komatsu M, Yajima H, Yamada S, Kaneko T, Sato Y, Yamauchi K, Hashizume K & Aizawa T 1999 Augmentation of Ca2C-stimulated insulin release by glucose and long-chain fatty acids in rat pancreatic islets: free fatty acids mimic ATP-sensitive KC channel-independent insulinotropic action of glucose. Diabetes 48 1543-1549. (doi:10. 2337/ diabetes. 48. 8. 1543)
24. Leibiger B, Moede T, Schwarz T, Brown GR, Köhler M, Leibiger IB & Berggren PO 1998 Short-term regulation of insulin gene transcription by glucose. PNAS 95 9307-9312. (doi:10. 1073/pnas. 95. 16. 9307). ?
25. Li Y, Wang P, Xu J, Gorelick F, Yamazaki H, Andrews N & Desir GV 2007 Regulation of insulin secretion and GLUT4 trafficking by the calcium sensor synaptotagmin VII. Biochemical and Biophysical Research Communications 362 658-664. (doi:10. 1016/j. bbrc. 2007. 08. 023)
26. Lim Y, Shin JS, Paik WK & Kim S 2003 Increased methylation of endogenous 20-kDa protein in HIT β-cell during insulin secretion. Biochemical and Biophysical Research Communications 305 292-298. (doi:10. 1016/S0006-291X(03)00733-2)
27. Ma H, Baumann CT, Li H, Strahl BD, Rice R, Jelinek MA, Aswad DW, Allis CD, Hager GL & Stallcup MR 2001 Hormone-dependent, CARM1-directed, arginine-specific methylation of histone H3 on a steroid-regulated promoter. Current Biology 11 1981-1985. (doi:10. 1016/S0960-9822(01)00600-5)
28. Mizutani A, Fukuda M, Ibata K, Shiraishi Y &Mikoshiba K 2000 SYNCRIP, a cytoplasmic counterpart of heterogeneous nuclear ribonucleoprotein R, interacts with ubiquitous synaptotagmin isoforms. Journal of Biological Chemistry 275 9823-9831. (doi:10. 1074/jbc. 275. 13. 9823). ?
29. Moran A, Zhang HJ, Olson LK, Harmon JS, Poitout V & Robertson RP 1997 Differentiation of glucose toxicity from beta cell exhaustion during the evolution of defective insulin gene expression in the pancreatic islet cell line, HIT-T15. Journal of Clinical Investigation 99 534-549. (doi:10. 1172/JCI119190)
30. Newsholme P & Krause M 2012 Nutritional regulation of insulin secretion: implications for diabetes. Clinical Biochemist. Reviews 33 35-47.
31. Ort T, Voronov S, Guo J, Zawalich K, Froehner SC, ZawalichW&SolimenaM 2001 Dephosphorylation of β2-syntrophin and Ca2C/μ-calpainmediated cleavage of ICA512 upon stimulation of insulin secretion. EMBO Journal 20 4013-4023. (doi:10. 1093/emboj/20. 15. 4013). ?
32. Ren J, Jin P, Wang E, Liu E, Harlan DM, Li X & Stroncek DF 2007 Pancreatic islet cell therapy for type I diabetes: understanding the effects of glucose stimulation on islets in order to produce better islets for transplantation. Journal of Translational Medicine 3 1-15. (doi:10. 1186/1479-5876-5-1)
33. Robertson RP, Zhang HJ, Pyzdrowski KL &Walseth TF 1992 Preservation of insulin mRNA levels and insulin secretion in HIT cells by avoidance of chronic exposure to high glucose concentrations. Journal of Clinical Investigation 90 320-325. (doi:10. 1172/JCI115865)
34. Schneider R, Bannister AJ, Myers FA, Thorne AW, Crane-Robinson C & Kouzarides T 2004 Histone H3 lysine 4 methylation patterns in higher eukaryotic genes. Nature Cell Biology 6 73-77. (doi:10. 1038/ncb1076)
35. Schurter BT, Koh SS, Chen D, Bunick GJ, Harp JM, Hanson BL, Henschen-Edman A, Mackay DR, Stallcup MR & Aswad DW 2001 Methylation of histone H3 by coactivator-associated arginine methyltransferase 1. Biochemistry 40 5747-5756. (doi:10. 1021/bi002631b)
36. Shalev A, Blair PJ, Hoffmann SC, Hirshberg B, Peculis BA & Harlan DM 2002 A proinsulin gene splice variant with increased translation efficiency is expressed in human pancreatic islets. Endocrinology 143 2541-2547. (doi:10. 1210/endo. 143. 7. 8920)
37. Straub SG & Sharp GW 2002 Glucose-stimulated signaling pathways in biphasic insulin secretion. Diabetes/Metabolism Research and Reviews 18451-463. (doi:10. 1002/dmrr. 329)
38. Tanaka Y, Gleason CE, Tran PO, Harmon JS & Robertson RP 1999 Prevention of glucose toxicity in HIT-T15 cells and Zucker diabetic fatty rats by antioxidants. PNAS 96 10857-10862. (doi:10. 1073/ pnas. 96. 19. 10857)
39. Wada K, Inoue K & HagiwaraM2002 Identification of methylated proteins by protein arginine N-methyltransferase 1, PRMT1, with a new expression cloning strategy. Biochimica et Biophysica Acta 1591 1-10. (doi:10. 1016/S0167-4889(02)00202-1)
40. Webb GC, Akbar MS, Zhao C & Steiner DF 2000 Expression profiling of pancreatic β cells: glucose regulation of secretory and metabolic pathway genes. PNAS 97 5773-5778. (doi:10. 1073/pnas. 100126597)
41. Wu Q, Bruce AW, Jedrusik A, Ellis PD, Andrews RM, Langford CF, Glover DM & Zernicka-Goetz M 2009 CARM1 is required in embryonic stem cells to maintain pluripotency and resist differentiation. Stem Cells 11 2637-2645. (doi:10. 1002/stem. 131)