Whole Genome SNP Genotyping and Exome Sequencing Reveal Novel Genetic Variants and Putative Causative Genes in Congenital Hyperinsulinism

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Proverbio, Maria Carla ^a   Mangano, Eleonora ^b   Gessi, Alessandra ^a   Bordoni, Roberta ^b   Spinelli, Roberta ^b   Asselta, Rosanna ^a   Valin, Paola Sogno ^c   Di Candia, Stefania ^c   Zamproni, Ilaria ^c   Diceglie, Cecilia ^c   Mora, Stefano ^c   Caruso Nicoletti, Manuela ^d   Salvatoni, Alessandro ^e   De Bellis, Gianluca ^b   Battaglia, Cristina ^a,b  

^a UNIVERSITY OF MILAN   (Italy)

^b INSTITUTE OF BIOMEDICAL TECHNOLOGIES   (Italy)

^c SAN RAFFAELE HOSPITAL   (Italy)

^d UNIVERSITY OF CATANIA   (Italy)

^e UNIVERSITY OF INSUBRIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; INSULIN; MEMBRANE PROTEIN; MITOCHONDRIAL ENZYME;

ACACB GENE; ARTICLE; CACNA1A GENE; CAMK2D GENE; CDKAL1 GENE; CLINICAL ARTICLE; CSMD1 GENE; FAMILY; FEMALE; GENE; GENE IDENTIFICATION; GENE LINKAGE DISEQUILIBRIUM; GENE MUTATION; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOTYPE; GNAS GENE; HUMAN; INSULIN RELEASE; KCNH6 GENE; KCNJ10 GENE; MALE; NOS2 GENE; NOTCH2 GENE; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PC GENE; PDE4C GENE; PERSISTENT HYPERINSULINEMIC HYPOGLYCEMIA OF INFANCY; PIK3R3 GENE; RYR3 GENE; SCN8A GENE; SINGLE NUCLEOTIDE POLYMORPHISM; SLC24A6 GENE; SLC37A3 GENE; SULF1 GENE; TLL1 GENE; TRPC5 GENE; TRPV3 GENE;

CONGENITAL HYPERINSULINISM; EXOME; FEMALE; GENETIC PREDISPOSITION TO DISEASE; GENOME, HUMAN; GENOTYPING TECHNIQUES; HUMANS; INSULIN; MALE; POLYMORPHISM, SINGLE NUCLEOTIDE;

EID: 84880310418     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068740     Document Type: Article

References (61)

1. Hussain K (2008) Diagnosis and management of hyperinsulinaemic hypoglycaemia of infancy. Hormone research 69: 2-13. Available: http://www.ncbi.nlm.nih.gov/pubmed/18059080. Accessed 16 September 2012.
2. Arnoux J-B, Verkarre V, Saint-Martin C, Montravers F, Brassier A, et al. (2011) Congenital hyperinsulinism: current trends in diagnosis and therapy. Orphanet journal of rare diseases 6: 63 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3199232&tool=pmcentrez&rendertype=abstract.
3. Senniappan S, Shanti B, James C, Hussain K (2012) Hyperinsulinaemic hypoglycaemia: genetic mechanisms, diagnosis and management. Journal of inherited metabolic disease 35: 589-601.Available: http://www.ncbi.nlm.nih.gov/pubmed/22231386. Accessed 26 September 2012.
4. Flanagan SE, Kapoor RR, Hussain K (2011) Genetics of congenital hyperinsulinemic hypoglycemia. Seminars in pediatric surgery 20: 13-17.Available: http://www.ncbi.nlm.nih.gov/pubmed/21185998. Accessed 9 August 2012.
5. Hojlund K, Hansen T, Lajer M, Henriksen JE, Levin K, et al. (2004) A Novel Syndrome of Autosomal-Dominant Hyperinsulinemic Hypoglycemia Linked to a Mutation in the Human Insulin Receptor Gene. Diabetes 53: 1592-1598.Available: http://diabetes.diabetesjournals.org/content/53/6/1592.short. Accessed 13 March 2013.
6. Stanescu DE, Hughes N, Kaplan B, Stanley CA, De León DD (2012) Novel Presentations of Congenital Hyperinsulinism due to Mutations in the MODY genes: HNF1A and HNF4A. The Journal of clinical endocrinology and metabolism 97: 1-5. Available: http://www.ncbi.nlm.nih.gov/pubmed/22802087. Accessed 3 August 2012.
7. Snider KE, Becker S, Boyajian L, Shyng S-L, Macmullen C, et al. (2013) Genotype and phenotype correlations in 417 children with congenital hyperinsulinism. The Journal of clinical endocrinology and metabolism 98: E355-63. Available: http://www.ncbi.nlm.nih.gov/pubmed/23275527. Accessed 16 February 2013.
8. Rorsman P, Braun M (2012) Regulation of Insulin Secretion in Human Pancreatic Islets. Annual review of physiology: 1-25. Available: http://www.ncbi.nlm.nih.gov/pubmed/22974438. Accessed 31 October 2012.
9. Colsoul B, Vennekens R, Nilius B, (2011) Transient Receptor Potential cation channels in Pancreatic β Cells. Rev Physiol Biochem Pharmacol 161: 87-111 doi:10.1007/112.
10. Jitrapakdee S, Wutthisathapornchai A, Wallace JC, MacDonald MJ, (2010) Regulation of insulin secretion: role of mitochondrial signalling. Diabetologia 53: 1019-1032 doi:10.1007/s00125-010-1685-0.Regulation.
11. Dipple KM, McCabe ER, (2000) Phenotypes of patients with simple Mendelian disorders are complex traits: thresholds, modifiers, and systems dynamics. American journal of human genetics 66: 1729-1735 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1378056&tool=pmcentrez&rendertype=abstract.
12. Ott J, Kamatani Y, Lathrop M (2011) Family-based designs for genome-wide association studies. Nature reviews Genetics 12: 465-474. Available: http://www.ncbi.nlm.nih.gov/pubmed/21629274. Accessed 16 October 2012.
13. Bailey-Wilson JE, Wilson AF (2011) Linkage analysis in the next-generation sequencing era. Human heredity 72: 228-236. Available: http://www.ncbi.nlm.nih.gov/pubmed/22189465. Accessed 31 October 2012.
14. Ng SB, Buckingham KJ, Lee C, Bigham AW, Tabor HK, et al. (2010) Exome sequencing identifies the cause of a Mendelian disorder. Nature genetics 42: 30-35 doi:10.1038/ng.499.Exome.
15. Bamshad MJ, Ng SB, Bigham AW, Tabor HK, Emond MJ, et al. (2011) Exome sequencing as a tool for Mendelian disease gene discovery. Nature reviews Genetics 12: 745-755. Available: http://www.ncbi.nlm.nih.gov/pubmed/21946919. Accessed 13 July 2012.
16. Johansson S, Irgens H, Chudasama KK, Molnes J, Aerts J, et al. (2012) Exome sequencing and genetic testing for MODY. PloS one 7: e38050. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3360646&tool=pmcentrez&rendertype=abstract. Accessed 31 July 2012.
17. Bonnefond A, Philippe J, Durand E, Dechaume A, Huyvaert M, et al. (2012) Whole-Exome Sequencing and High Throughput Genotyping Identified KCNJ11 as the Thirteenth MODY Gene. PloS one 7: e37423. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3372463&tool=pmcentrez&rendertype=abstract. Accessed 3 August 2012.
18. Lehne B, Lewis CM, Schlitt T (2011) From SNPs to genes: disease association at the gene level. PloS one 6: e20133. Available: http://dx.plos.org/10.1371/journal.pone.0020133. Accessed 13 March 2013.
19. Nestorowicz A, Glaser B, Wilson BA, Shyng SL, Nichols CG, et al. (1998) Genetic heterogeneity in familial hyperinsulinism. Human molecular genetics 7: 1119-1128 Available: http://www.ncbi.nlm.nih.gov/pubmed/9618169.
20. Parappil HA, Rahman SA, Soliman AB, Ismail AC, Al-Bozom I, et al. (2009) Congenital Hyperinsulinism in a Neonate Due to a Novel Homozygous Mutation (ABCC8): A case report. Int J Endocrinol Metab 2: 95-100.
21. Chevre JC, Hani EH, Boutin P, Vaxillaire M, Blanché H, et al. (1998) Mutation screening in 18 Caucasian families suggest the existence of other MODY genes. Diabetologia 41: 1017-1023 Available: http://www.ncbi.nlm.nih.gov/pubmed/9754819.
22. Stanescu DE, Hughes N, Kaplan B, Stanley CA, De León DD (2012) Novel Presentations of Congenital Hyperinsulinism due to Mutations in the MODY genes: HNF1A and HNF4A. The Journal of clinical endocrinology and metabolism 97: 1-5. Available: http://www.ncbi.nlm.nih.gov/pubmed/22802087. Accessed 3 August 2012.
23. Rorsman P, Braun M, Zhang Q (2011) Regulation of calcium in pancreatic α- and β-cells in health and disease. Cell calcium 51: 300-308. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3334273&tool=pmcentrez&rendertype=abstract. Accessed 7 September 2012.
24. Dunne MJ, Shepherd RM, Cosgrove KE, Macfarlane WM, Lindley KJ, et al. (2000) Persistent hyperinsulinaemic hyperglycaemia of infancy-derived cells; implications for beta-cells that replicate in vitro. Journal of molecular endocrinology 24: 313-320 Available: http://www.ncbi.nlm.nih.gov/pubmed/10828824.
25. Rosati B, Marchetti P, Crociani O, Lecchi M, Lupi R, et al. (2000) Glucose- and arginine-induced insulin secretion by human pancreatic β-cells: the role of HERG K+ channels in firing and relase. FASEB journal 14: 2601-2610.
26. Scholl UI, Choi M, Liu T, Ramaekers VT, Häusler MG, et al. (2009) Seizures, sensorineural deafness, ataxia, mental retardation, and electrolyte imbalance (SeSAME syndrome) caused by mutations in KCNJ10. Proceedings of the National Academy of Sciences of the United States of America 106: 5842-5847. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2656559&tool=pmcentrez&rendertype=abstract. Accessed 13 March 2013.
27. Lammert E, Brown J, Melton DA (2000) Notch gene expression during pancreatic organogenesis. Mechanisms of development 94: 199-203. Available: http://www.ncbi.nlm.nih.gov/pubmed/10842072. Accessed 13 March 2013.
28. Kim W, Shin Y-K, Kim B-J, Egan JM (2010) Notch signaling in pancreatic endocrine cell and diabetes. Biochemical and biophysical research communications 392: 247-251. Available: http://www.ncbi.nlm.nih.gov/pubmed/20035712. Accessed 31 October 2012.
29. Vionnet N, Stoffel M, Takeda J, Yasuda K, Bell GI, et al. (1992) Nonsense mutation in the glucokinase gene causes early-onset non-insulin-dependent diabetes mellitus. Nature 356: 721-722. Available: http://www.ncbi.nlm.nih.gov/pubmed/1570017. Accessed 13 March 2013.
30. Yamagata K, Furuta H, Oda N, Kaisaki PJ, Menzel S, et al. (1996) Mutations in the hepatocyte nuclear factor-4alpha gene in maturity-onset diabetes of the young (MODY1). Nature 384: 458-460. Available: http://www.ncbi.nlm.nih.gov/pubmed/8945471. Accessed 13 March 2013.
31. Yamagata K, Oda N, Kaisaki PJ, Menzel S, Furuta H, et al. (1996) Mutations in the hepatocyte nuclear factor-1alpha gene in maturity-onset diabetes of the young (MODY3). Nature 384: 455-458. Available: http://www.ncbi.nlm.nih.gov/pubmed/8945470. Accessed 13 March 2013.
32. Johnson JD, Kuang S, Misler S, Polonsky KS, (2004) Ryanodine receptors in human pancreatic beta cells: localization and effects on insulin secretion. FASEB journal 18: 878-880 Available: http://www.ncbi.nlm.nih.gov/pubmed/15033925.
33. Bartoloni L, Antonarakis SE (2004) The human sugar-phosphate/phosphate exchanger family SLC37. European journal of physiology 447: 780-783. Available: http://www.ncbi.nlm.nih.gov/pubmed/12811562. Accessed 26 September 2012.
34. Braun M, Ramracheya R, Bengtsson M, Zhang Q, Karanauskaite J, et al. (2008) Voltage-Gated Ion Channels in Human Pancreatic β-Cells: Electrophysiological Characterization and Role in Insulin Secretion. Diabetes 57: 1618-1628 doi:10.2337/db07-0991.M.B.
35. Prentki M, Vischer S, Glennon MC, Regazzi R, Deeney JT, et al. (1992) Malonyl-CoA and long chain acyl-CoA esters as metabolic coupling factors in nutrient-induced insulin secretion. The Journal of biological chemistry 267: 5802-5810 Available: http://www.ncbi.nlm.nih.gov/pubmed/1556096.
36. Zhang S, Kim K-H (1995) Glucose activation of acetyl-CoA carboxylase in association with insulin secretion in a pancreatic β-cell line. Journal of Endocrinology 147: 33-41. Available: http://joe.endocrinology-journals.org/content/147/1/33.abstract?ijkey=8a76ed9c70df96aeae6c97c33f117d4df096fb6e&keytype2=tf_ipsecsha. Accessed 6 November 2012.
37. Osterhoff M, Möhlig M, Schwanstecher M, Seufert J, Ortmann J, et al. (2003) Ca2+/calmodulin-dependent protein kinase II δ2 regulates gene expression of insulin in INS-1 rat insulinoma cells. Cell Calcium 33: 175-184. Available: http://linkinghub.elsevier.com/retrieve/pii/S0143416002002270. Accessed 31 October 2012.
38. Rochlitz H, Voigt A, Lankat-Buttgereit B, Göke B, Heimberg H, et al. (2000) Cloning and quantitative determination of the human Ca2+/calmodulin-dependent protein kinase II (CaMK II) isoforms in human beta cells. Diabetologia 43: 465-473 Available: http://www.ncbi.nlm.nih.gov/pubmed/10819240.
39. Brambillasca S, Altkrueger A, Colombo SF, Friederich A, Eickelmann P, et al. (2012) CDK5 regulatory subunit-associated protein 1-like 1 (CDKAL1) is a tail-anchored protein in the endoplasmic reticulum (ER) of insulinoma cells. The Journal of biological chemistry 287: 41808-41819. Available: http://www.ncbi.nlm.nih.gov/pubmed/23048041. Accessed 13 March 2013.
40. Ohara-Imaizumi M, Yoshida M, Aoyagi K, Saito T, Okamura T, et al. (2010) Deletion of CDKAL1 affects mitochondrial ATP generation and first-phase insulin exocytosis. PloS one 5: e15553. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3000340&tool=pmcentrez&rendertype=abstract. Accessed 31 October 2012.
41. Xie T, Chen M, Zhang Q-H, Ma Z, Weinstein LS, (2007) Beta cell-specific deficiency of the stimulatory G protein alpha-subunit Gsalpha leads to reduced beta cell mass and insulin-deficient diabetes. Proceedings of the National Academy of Sciences of the United States of America 104: 19601-19606 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2148335&tool=pmcentrez&rendertype=abstract.
42. Bastepe M, (2007) The GNAS Locus: Quintessential Complex Gene Encoding Gsalpha, XLalphas, and other Imprinted Transcripts. Current genomics 8: 398-414 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2671723&tool=pmcentrez&rendertype=abstract.
43. Corbett BJA, Mcdaniel ML (1995) Intraislet Release of Interleukin 1 Inhibits 3 Cell Function by Inducing 3 Cell Expression of Inducible Nitric Oxide Synthase. J Exp Med 181.
44. Tanioka T, Tamura Y, Fukaya M, Shinozaki S, Mao J, et al. (2011) Inducible nitric-oxide synthase and nitric oxide donor decrease insulin receptor substrate-2 protein expression by promoting proteasome-dependent degradation in pancreatic beta-cells: involvement of glycogen synthase kinase-3beta. The Journal of biological chemistry 286: 29388-29396. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3190744&tool=pmcentrez&rendertype=abstract. Accessed 31 October 2012.
45. Waddleton D, Wu W, Feng Y, Thompson C, Wu M, et al. (2008) Phosphodiesterase 3 and 4 comprise the major cAMP metabolizing enzymes responsible for insulin secretion in INS-1 (832/13) cells and rat islets. Biochemical pharmacology 76: 884-893. Available: http://www.ncbi.nlm.nih.gov/pubmed/18706893. Accessed 9 September 2012.
46. Heimann E, Jones HA, Resjö S, Manganiello VC, Stenson L, et al. (2010) Expression and regulation of cyclic nucleotide phosphodiesterases in human and rat pancreatic islets. PloS one 5: e14191. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2995729&tool=pmcentrez&rendertype=abstract. Accessed 26 September 2012.
47. Hirsch E, Costa C, Ciraolo E (2007) Phosphoinositide 3-kinases as a common platform for multi-hormone signaling. The Journal of endocrinology 194: 243-256. Available: http://www.ncbi.nlm.nih.gov/pubmed/17641274. Accessed 7 November 2012.
48. Li J, Kleeff J, Abiatari I, Kayed H, Giese NA, et al. (2005) Enhanced levels of Hsulf-1 interfere with heparin-binding growth factor signaling in pancreatic cancer. Molecular cancer 4: 14. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1087876&tool=pmcentrez&rendertype=abstract. Accessed 5 November 2012.
49. Chao LC, Bensinger SJ, Villanueva CJ, Wroblewski K, Tontonoz P (2008) Inhibition of adipocyte differentiation by Nur77, Nurr1, and Nor1. Molecular endocrinology (Baltimore, Md) 22: 2596-2608. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2610364&tool=pmcentrez&rendertype=abstract. Accessed 5 November 2012.
50. Pineda M, Campistol J, Vilaseca MA, Briones P, Ribes A, et al. (1995) An atypical French form of pyruvate carboxylase deficiency. Brain & development 17: 276-279. Available: http://www.ncbi.nlm.nih.gov/pubmed/7503391. Accessed 5 November 2012.
51. Palty R, Ohana E, Hershfinkel M, Volokita M, Elgazar V, et al. (2004) Lithium-calcium exchange is mediated by a distinct potassium-independent sodium-calcium exchanger. The Journal of biological chemistry 279: 25234-25240. Available: http://www.ncbi.nlm.nih.gov/pubmed/15060069. Accessed 8 March 2013.
52. Biagiotti L, Proverbio MC, Bosio L, Gervasi F, Rovida E, et al. (2007) Identification of two novel frameshift mutations in the KCNJ11 gene in two Italian patients affected by Congenital Hyperinsulinism of Infancy. Experimental and molecular pathology 83: 59-64. Available: http://www.ncbi.nlm.nih.gov/pubmed/17316607. Accessed 31 October 2012.
53. Cazzaniga G, Lo Nigro L, Cifola I, Milone G, Schnittger S, et al. (2009) Simultaneous occurrence of acute myeloid leukaemia with mutated nucleophosmin (NPM1) in the same family. Leukemia 23: 199-203. Available: http://www.ncbi.nlm.nih.gov/pubmed/18596743. Accessed 31 October 2012.
54. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, et al. (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. American journal of human genetics 81: 559-575. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1950838&tool=pmcentrez&rendertype=abstract. Accessed 12 July 2012.
55. Dudbridge F, Gusnanto A (2008) Estimation of significance thresholds for genomewide association scans. Genetic epidemiology 32: 227-234. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2573032&tool=pmcentrez&rendertype=abstract. Accessed 28 February 2013.
56. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics (Oxford, England) 25: 1754-1760. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2705234&tool=pmcentrez&rendertype=abstract. Accessed 4 October 2012.
57. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics (Oxford, England) 25: 2078-2079. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2723002&tool=pmcentrez&rendertype=abstract. Accessed 13 July 2012.
58. Twigger SN, Shimoyama M, Bromberg S, Kwitek AE, Jacob HJ (2007) The Rat Genome Database, update 2007-easing the path from disease to data and back again. Nucleic acids research 35: D658-62. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1761441&tool=pmcentrez&rendertype=abstract. Accessed 31 October 2012.
59. Kumar P, Henikoff S, Ng PC (2009) Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nature protocols 4: 1073-1081. Available: http://www.ncbi.nlm.nih.gov/pubmed/19561590. Accessed 16 July 2012.
60. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, et al. (2010) A method and server for predicting damaging missense mutations. Nature methods 7: 248-249. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2855889&tool=pmcentrez&rendertype=abstract. Accessed 8 October 2012.
61. Szklarczyk D, Franceschini A, Kuhn M, Simonovic M, Roth A, et al. (2011) The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic acids research 39: D561-8. Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3013807&tool=pmcentrez&rendertype=abstract. Accessed 26 October 2012.