Neomorphic effects of recurrent somatic mutations in yin yang 1 in insulin-producing adenomas

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 13, 2015, Pages 4062-4067

  Cromer, M Kyle ^a,b   Choi, Murim ^a,b   Nelson Williams, Carol ^a,b   Fonseca, Annabelle L ^a,c,d   Kunstman, John W ^a,c,d   Korah, Reju M ^a,c,d   Overton, John D ^a,c   Mane, Shrikant ^a,c   Kenneyg, Barton ^a   Malchoff, Carl D ^e,f   Stalbergj, Peter ^g   Akerströmj, Göran ^g   Westin, Gunnar ^g   Hellman, Per ^g   Carling, Tobias ^a,c,d   Björklund, Peyman ^g   Lifton, Richard P ^a,b,c  

^a Department of Genetics ^*  (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d YALE CANCER CENTER   (United States)

^e Division of Endocrinology   (United States)

^f UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^g UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CYCLIC AMP; DNA; GLUCOSE; INSULIN; TRANSCRIPTION FACTOR YY1; ADENYLATE CYCLASE; ADENYLYL CYCLASE 1; CACNA2D2 PROTEIN, HUMAN; CALCIUM; CALCIUM CHANNEL; GLUCOSE BLOOD LEVEL; PROTEIN BINDING; YY1 PROTEIN, HUMAN;

ADENOMA; ADENYLYL CYCLASE 1 GENE; ANIMAL CELL; ARTICLE; CACNA2D2 GENE; CANCER SURGERY; CHROMATIN IMMUNOPRECIPITATION; CLINICAL ARTICLE; CONTROLLED STUDY; DNA BINDING MOTIF; GENE; GENE EXPRESSION; GIPC2 GENE; GLUCOSE BLOOD LEVEL; HUMAN; HUMAN TISSUE; HYPOGLYCEMIA; INSULIN RELEASE; INSULINOMA; MEN1 GENE; MISSENSE MUTATION; NONHUMAN; PANCREAS ISLET CELL TUMOR; PANCREAS TUMOR; PRIORITY JOURNAL; RAT; SOMATIC MUTATION; ADOLESCENT; ADULT; AGED; BINDING SITE; COHORT ANALYSIS; CYTOLOGY; FEMALE; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; MIDDLE AGED; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PANCREAS ISLET BETA CELL; VERY ELDERLY;

RATTUS;

ADENYLYL CYCLASES; ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; BASE SEQUENCE; BINDING SITES; BLOOD GLUCOSE; CALCIUM; CALCIUM CHANNELS; COHORT STUDIES; CYCLIC AMP; FEMALE; GENE EXPRESSION REGULATION; HUMANS; INSULIN; INSULIN-SECRETING CELLS; INSULINOMA; MALE; MIDDLE AGED; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; PANCREATIC NEOPLASMS; PROTEIN BINDING; YY1 TRANSCRIPTION FACTOR;

EID: 84961291596     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1503696112     Document Type: Article

References (54)

1. Batcher E, Madaj P, Gianoukakis AG (2011) Pancreatic neuroendocrine tumors. Endocr Res 36(1):35-43.
2. Perry RR, Vinik AI (1995) Clinical review 72: Diagnosis and management of functioning islet cell tumors. J Clin Endocrinol Metab 80(8):2273-2278.
3. Li L, Rojas A, Wu J, Jiang C (2004) Disruption of glucose sensing and insulin secretion by ribozyme Kir6.2-gene targeting in insulin-secreting cells. Endocrinology 145(9): 4408-4414.
4. Scrocchi LA, Marshall BA, Cook SM, Brubaker PL, Drucker DJ (1998) Identification of glucagon-like peptide 1 (GLP-1) actions essential for glucose homeostasis in mice with disruption of GLP-1 receptor signaling. Diabetes 47(4):632-639.
5. Holst JJ (2007) The physiology of glucagon-like peptide 1. Physiol Rev 87(4):1409-1439.
6. Doyle ME, Egan JM (2007) Mechanisms of action of glucagon-like peptide 1 in the pancreas. Pharmacol Ther 113(3):546-593.
7. Roger B, et al. (2011) Adenylyl cyclase 8 is central to glucagon-like peptide 1 signalling and effects of chronically elevated glucose in rat and human pancreatic beta cells. Diabetologia 54(2):390-402.
8. Ozaki N, et al. (2000) cAMP-GEFII is a direct target of cAMP in regulated exocytosis. Nat Cell Biol 2(11):805-811.
9. Drucker DJ, Nauck MA (2006) The incretin system: Glucagon-like peptide-1 receptor agonists and dipeptidyl peptidase-4 inhibitors in type 2 diabetes. Lancet 368(9548): 1696-1705.
10. Sjöholm A (1995) Regulation of insulinoma cell proliferation and insulin accumulation by peptides and second messengers. Ups J Med Sci 100(3):201-216.
11. Klinger S, et al. (2008) Increasing GLP-1-induced beta-cell proliferation by silencing the negative regulators of signaling cAMP response element modulator-alpha and DUSP14. Diabetes 57(3):584-593.
12. Choi M, et al. (2011) K+ channel mutations in adrenal aldosterone-producing adenomas and hereditary hypertension. Science 331(6018):768-772.
13. Scholl UI, et al. (2013) Somatic and germline CACNA1D calcium channel mutations in al-dosterone-producing adenomas and primary aldosteronism. Nat Genet 45(9):1050-1054.
14. Azizan EA, et al. (2013) Somatic mutations in ATP1A1 and CACNA1D underlie a common subtype of adrenal hypertension. Nat Genet 45(9):1055-1060.
15. Goh G, et al. (2014) Recurrent activating mutation in PRKACA in cortisol-producing adrenal tumors. Nat Genet 46(6):613-617.
16. Cao Y, et al. (2014) Activating hotspot L205R mutation in PRKACA and adrenal Cushing's syndrome. Science 344(6186):913-917.
17. Larsson C, Skogseid B, Oberg K, Nakamura Y, Nordenskjöld M (1988) Multiple endocrine neoplasia type 1 gene maps to chromosome 11 and is lost in insulinoma. Nature 332(6159):85-87.
18. Zhuang Z, et al. (1997) Somatic mutations of the MEN1 tumor suppressor gene in sporadic gastrinomas and insulinomas. Cancer Res 57(21):4682-4686.
19. Cao Y, et al. (2013) Whole exome sequencing of insulinoma reveals recurrent T372R mutations in YY1. Nat Commun 4:2810.
20. Shi Y, Lee JS, Galvin KM (1997) Everything you have ever wanted to know about Yin Yang 1...... Biochim Biophys Acta 1332(2):F49-F66.
21. Thorvaldsen JL, Weaver JR, Bartolomei MS (2011) A YY1 bridge for X inactivation. Cell 146(1):11-13.
22. Jeon Y, Lee JT (2011) YY1 tethers Xist RNA to the inactive X nucleation center. Cell 146(1):119-133.
23. Chandrasekharappa SC, et al. (1997) Positional cloning of the gene for multiple endocrine neoplasia-type 1. Science 276(5311):404-407.
24. Wu G, et al.; St. Jude Children's Research Hospital-Washington University Pediatric Cancer Genome Project (2012) Somatic histone H3 alterations in pediatric diffuse intrinsic pontine gliomas and non-brainstem glioblastomas. Nat Genet 44(3):251-253.
25. Kim JD, Kim J (2009) YY1's longer DNA-binding motifs. Genomics 93(2):152-158.
26. Houbaviy HB, Usheva A, Shenk T, Burley SK (1996) Cocrystal structure of YY1 bound to the adeno-associated virus P5 initiator. Proc Natl Acad Sci USA 93(24):13577-13582.
27. Bailey TL, Williams N, Misleh C, Li WW (2006) MEME: Discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34(Web Server issue):W369-W373.
28. Zhang Y, et al. (2008) Model-based analysis of ChIP-Seq (MACS). Genome Biol 9(9): R137.
29. Grant CE, Bailey TL, Noble WS (2011) FIMO: Scanning for occurrences of a given motif. Bioinformatics 27(7):1017-1018.
30. Xi H, et al. (2007) Analysis of overrepresented motifs in human core promoters reveals dual regulatory roles of YY1. Genome Res 17(6):798-806.
31. Pagliarini DJ, et al. (2008) A mitochondrial protein compendium elucidates complex I disease biology. Cell 134(1):112-123.
32. Wang H, Ferguson GD, Pineda VV, Cundiff PE, Storm DR (2004) Overexpression of type-1 adenylyl cyclase in mouse forebrain enhances recognition memory and LTP. Nat Neurosci 7(6):635-642.
33. Leech CA, Castonguay MA, Habener JF (1999) Expression of adenylyl cyclase subtypes in pancreatic beta-cells. Biochem Biophys Res Commun 254(3):703-706.
34. Kutlu B, et al. (2009) Detailed transcriptome atlas of the pancreatic beta cell. BMC Med Genomics 2:3.
35. Delmeire D, et al. (2003) Type VIII adenylyl cyclase in rat beta cells: Coincidence signal detector/generator for glucose and GLP-1. Diabetologia 46(10):1383-1393.
36. Nguidjoe E, et al. (2011) Heterozygous inactivation of the Na/Ca exchanger increases glucose-induced insulin release, β-cell proliferation, and mass. Diabetes 60(8):2076-2085.
37. Carboni GL, et al. (2003) CACNA2D2-mediated apoptosis in NSCLC cells is associated with alterations of the intracellular calcium signaling and disruption of mitochondria membrane integrity. Oncogene 22(4):615-626.
38. Hanoune J, Defer N (2001) Regulation and role of adenylyl cyclase isoforms. Annu Rev Pharmacol Toxicol 41:145-174.
39. Cooper DM, Mons N, Karpen JW (1995) Adenylyl cyclases and the interaction between calcium and cAMP signalling. Nature 374(6521):421-424.
40. Kitaguchi T, Oya M, Wada Y, Tsuboi T, Miyawaki A (2013) Extracellular calcium influx activates adenylate cyclase 1 and potentiates insulin secretion in MIN6 cells. Biochem J 450(2):365-373.
41. Asfari M, et al. (1992) Establishment of 2-mercaptoethanol-dependent differentiated insulin-secreting cell lines. Endocrinology 130(1):167-178.
42. Dames P, et al. (2012) Suppression of the nuclear factor Eny2 increases insulin secretion in poorly functioning INS-1E insulinoma cells. Exp Diabetes Res 2012:460869.
43. Popiela H, Moore W (1991) Tolbutamide stimulates proliferation of pancreatic beta cells in culture. Pancreas 6(4):464-469.
44. Hussain MA, et al. (2006) Increased pancreatic beta-cell proliferation mediated by CREB binding protein gene activation. Mol Cell Biol 26(20):7747-7759.
45. Hui H, Nourparvar A, Zhao X, Perfetti R (2003) Glucagon-like peptide-1 inhibits apoptosis of insulin-secreting cells via a cyclic 5″-adenosine monophosphate-dependent protein kinase A- and a phosphatidylinositol 3-kinase-dependent pathway. Endocrinology 144(4):1444-1455.
46. Munaron L, Antoniotti S, Lovisolo D (2004) Intracellular calcium signals and control of cell proliferation: How many mechanisms? J Cell Mol Med 8(2):161-168.
47. Olofsson MH, Havelka AM, Brnjic S, Shoshan MC, Linder S (2008) Charting calciumregulated apoptosis pathways using chemical biology: Role of calmodulin kinase II. BMC Chem Biol 8:2.
48. Scholl UI, et al. (2012) Hypertension with or without adrenal hyperplasia due to different inherited mutations in the potassium channel KCNJ5. Proc Natl Acad Sci USA 109(7):2533-2538.
49. Jones S, et al. (2008) Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 321(5897):1801-1806.
50. Jiao Y, et al. (2011) DAXX/ATRX, MEN1, and mTOR pathway genes are frequently altered in pancreatic neuroendocrine tumors. Science 331(6021):1199-1203.
51. Beuschlein F, et al. (2013) Somatic mutations in ATP1A1 and ATP2B3 lead to aldo-sterone-producing adenomas and secondary hypertension. Nat Genet 45(4):440-444.
52. Reddy TE, et al. (2009) Genomic determination of the glucocorticoid response reveals unexpected mechanisms of gene regulation. Genome Res 19(12):2163-2171.
53. Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10(3):R25.
54. Giardine B, et al. (2005) Galaxy: A platform for interactive large-scale genome analysis. Genome Res 15(10):1451-1455.