Human β cell transcriptome analysis uncovers lncRNAs that are tissue-specific, dynamically regulated, and abnormally expressed in type 2 diabetes

Cell Metabolism

Volumn 16, Issue 4, 2012, Pages 435-448

  Morán, Ignasi ^a   Akerman, Ildem ^a   Van De Bunt, Martijn ^c,d   Xie, Ruiyu ^e   Benazra, Marion ^f   Nammo, Takao ^a,b,g   Arnes, Luis ^h   Nakić, Nikolina ^a,b   García Hurtado, Javier ^a,b   Rodríguez Seguí, Santiago ^a,b   Pasquali, Lorenzo ^a,b   Sauty Colace, Claire ^f   Beucher, Anthony ^a,b   Scharfmann, Raphael ⁱ   Van Arensbergen, Joris ^a,b   Johnson, Paul R ^d,j   Berry, Andrew ^k   Lee, Clarence ^l   Harkins, Timothy ^l   Gmyr, Valery ^m   Pattou, François ^m   Kerr Conte, Julie ^m   Piemonti, Lorenzo ⁿ   Berney, Thierry ^o   Hanley, Neil ^k   Gloyn, Anna L ^d   Sussel, Lori ^h   Langman, Linda ^p   Brayman, Kenneth L ^p   Sander, Maike ^e   McCarthy, Mark I ^c,d,n   Ravassard, Philippe ^f   Ferrer, Jorge ^a,b,q   more..

^a INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d CHURCHILL HOSPITAL   (United Kingdom)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f INSTITUT DU CERVEAU ET DE LA MOELLE ÉPINIÈRE   (France)

^g Research Institute   (Japan)

^h Columbia University ^*  (United States)

ⁱ INSERM   (France)

^j JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^k UNIVERSITY OF MANCHESTER   (United Kingdom)

^l Life Technologies   (United States)

^m UNIV LILLE   (France)

ⁿ SAN RAFFAELE HOSPITAL   (Italy)

^o Cell Isolation and Transplantation Center   (Switzerland)

^p UNIVERSITY OF VIRGINIA   (United States)

^q HOSPITAL CLÍNIC   (Spain)

more..

Author keywords

[No Author keywords available]

Indexed keywords

HEPATOCYTE NUCLEAR FACTOR 1ALPHA; HEPATOCYTE NUCLEAR FACTOR 3BETA; LONG NONCODING RNA; MESSENGER RNA; NEUROGENIC DIFFERENTIATION FACTOR; TRANSCRIPTION FACTOR GATA 6; TRANSCRIPTION FACTOR MAFB; TRANSCRIPTION FACTOR NKX2.2; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR PDX 1; TRANSCRIPTOME; UNCLASSIFIED DRUG; UNTRANSLATED RNA;

ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; DISEASE PREDISPOSITION; DOWN REGULATION; GENE CONTROL; GENE LOCUS; GENE MAPPING; HUMAN; HUMAN CELL; HUMAN TISSUE; INTERSPERSED REPEAT; NON INSULIN DEPENDENT DIABETES MELLITUS; PANCREAS ISLET BETA CELL; PANCREAS ISLET CELL; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RNA SEQUENCE;

ANIMALS; CHROMATIN; DIABETES MELLITUS, TYPE 2; DOWN-REGULATION; GENE EXPRESSION PROFILING; GENETIC LOCI; HUMANS; INSULIN-SECRETING CELLS; MICE; REPRESSOR PROTEINS; RNA, LONG UNTRANSLATED; RNA, MESSENGER; TRANS-ACTIVATORS;

EID: 84867070330     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2012.08.010     Document Type: Article

References (54)

1. H.L. Allen, S.E. Flanagan, C. Shaw-Smith, E. De Franco, I. Akerman, R. Caswell, J. Ferrer, A.T. Hattersley, and S. Ellard GATA6 haploinsufficiency causes pancreatic agenesis in humans Nat. Genet. 44 2012 20 22
2. I. Artner, B. Blanchi, J.C. Raum, M. Guo, T. Kaneko, S. Cordes, M. Sieweke, and R. Stein MafB is required for islet beta cell maturation Proc. Natl. Acad. Sci. USA 104 2007 3853 3858
3. G.I. Bell, and K.S. Polonsky Diabetes mellitus and genetically programmed defects in beta-cell function Nature 414 2001 788 791
4. M. Bensellam, L. Van Lommel, L. Overbergh, F.C. Schuit, and J.C. Jonas Cluster analysis of rat pancreatic islet gene mRNA levels after culture in low-, intermediate- and high-glucose concentrations Diabetologia 52 2009 463 476
5. P. Bertone, V. Stolc, T.E. Royce, J.S. Rozowsky, A.E. Urban, X. Zhu, J.L. Rinn, W. Tongprasit, M. Samanta, and S. Weissman Global identification of human transcribed sequences with genome tiling arrays Science 306 2004 2242 2246
6. E. Birney, J.A. Stamatoyannopoulos, A. Dutta, R. Guigó, T.R. Gingeras, E.H. Margulies, Z. Weng, M. Snyder, E.T. Dermitzakis, R.E. Thurman ENCODE Project Consortium NISC Comparative Sequencing Program Baylor College of Medicine Human Genome Sequencing Center Washington University Genome Sequencing Center Broad Institute Children's Hospital Oakland Research Institute Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project Nature 447 2007 799 816
7. S.F. Boj, J.M. Servitja, D. Martin, M. Rios, I. Talianidis, R. Guigo, and J. Ferrer Functional targets of the monogenic diabetes transcription factors HNF-1alpha and HNF-4alpha are highly conserved between mice and humans Diabetes 58 2009 1245 1253
8. P. Bucher, Z. Mathe, P. Morel, D. Bosco, A. Andres, M. Kurfuest, O. Friedrich, N. Raemsch-Guenther, L.H. Buhler, and T. Berney Assessment of a novel two-component enzyme preparation for human islet isolation and transplantation Transplantation 79 2005 91 97
9. M.N. Cabili, C. Trapnell, L. Goff, M. Koziol, B. Tazon-Vega, A. Regev, and J.L. Rinn Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses Genes Dev. 25 2011 1915 1927
10. P. Carninci, T. Kasukawa, S. Katayama, J. Gough, M.C. Frith, N. Maeda, R. Oyama, T. Ravasi, B. Lenhard, C. Wells FANTOM Consortium RIKEN Genome Exploration Research Group and Genome Science Group (Genome Network Project Core Group) The transcriptional landscape of the mammalian genome Science 309 2005 1559 1563
11. M. Castaing, B. Duvillié, E. Quemeneur, A. Basmaciogullari, and R. Scharfmann Ex vivo analysis of acinar and endocrine cell development in the human embryonic pancreas Dev. Dyn. 234 2005 339 345
12. Y.S. Cho, C.H. Chen, C. Hu, J. Long, R.T. Ong, X. Sim, F. Takeuchi, Y. Wu, M.J. Go, T. Yamauchi DIAGRAM Consortium MuTHER Consortium Meta-analysis of genome-wide association studies identifies eight new loci for type 2 diabetes in east Asians Nat. Genet. 44 2012 67 72
13. P. Collombat, X. Xu, P. Ravassard, B. Sosa-Pineda, S. Dussaud, N. Billestrup, O.D. Madsen, P. Serup, H. Heimberg, and A. Mansouri The ectopic expression of Pax4 in the mouse pancreas converts progenitor cells into alpha and subsequently beta cells Cell 138 2009 449 462
14. C. Dorrell, J. Schug, C.F. Lin, P.S. Canaday, A.J. Fox, O. Smirnova, R. Bonnah, P.R. Streeter, C.J. Stoeckert Jr., K.H. Kaestner, and M. Grompe Transcriptomes of the major human pancreatic cell types Diabetologia 54 2011 2832 2844
15. J. Dupuis, C. Langenberg, I. Prokopenko, R. Saxena, N. Soranzo, A.U. Jackson, E. Wheeler, N.L. Glazer, N. Bouatia-Naji, A.L. Gloyn DIAGRAM Consortium GIANT Consortium Global BPgen Consortium Anders Hamsten on behalf of Procardis Consortium MAGIC investigators New genetic loci implicated in fasting glucose homeostasis and their impact on type 2 diabetes risk Nat. Genet. 42 2010 105 116
16. K.J. Gaulton, T. Nammo, L. Pasquali, J.M. Simon, P.G. Giresi, M.P. Fogarty, T.M. Panhuis, P. Mieczkowski, A. Secchi, and D. Bosco A map of open chromatin in human pancreatic islets Nat. Genet. 42 2010 255 259
17. A.L. Gloyn, E.R. Pearson, J.F. Antcliff, P. Proks, G.J. Bruining, A.S. Slingerland, N. Howard, S. Srinivasan, J.M. Silva, and J. Molnes Activating mutations in the gene encoding the ATP-sensitive potassium-channel subunit Kir6.2 and permanent neonatal diabetes N. Engl. J. Med. 350 2004 1838 1849
18. R.A. Gupta, N. Shah, K.C. Wang, J. Kim, H.M. Horlings, D.J. Wong, M.C. Tsai, T. Hung, P. Argani, and J.L. Rinn Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis Nature 464 2010 1071 1076
19. M. Guttman, I. Amit, M. Garber, C. French, M.F. Lin, D. Feldser, M. Huarte, O. Zuk, B.W. Carey, and J.P. Cassady Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals Nature 458 2009 223 227
20. M. Guttman, J. Donaghey, B.W. Carey, M. Garber, J.K. Grenier, G. Munson, G. Young, A.B. Lucas, R. Ach, and L. Bruhn lincRNAs act in the circuitry controlling pluripotency and differentiation Nature 477 2011 295 300
21. M. Guttman, and J.L. Rinn Modular regulatory principles of large non-coding RNAs Nature 482 2012 339 346
22. P.A. Halban, S.E. Kahn, Lernmark A., and C.J. Rhodes Gene and cell-replacement therapy in the treatment of type 1 diabetes: how high must the standards be set? Diabetes 50 2001 2181 2191
23. I.M. Heid, A.U. Jackson, J.C. Randall, T.W. Winkler, L. Qi, V. Steinthorsdottir, G. Thorleifsson, M.C. Zillikens, E.K. Speliotes, R. Mägi MAGIC Meta-analysis identifies 13 new loci associated with waist-hip ratio and reveals sexual dimorphism in the genetic basis of fat distribution Nat. Genet. 42 2010 949 960
24. W. Hu, B. Yuan, J. Flygare, and H.F. Lodish Long noncoding RNA-mediated anti-apoptotic activity in murine erythroid terminal differentiation Genes Dev. 25 2011 2573 2578
25. J.S. Kooner, D. Saleheen, X. Sim, J. Sehmi, W. Zhang, P. Frossard, L.F. Been, K.S. Chia, A.S. Dimas, N. Hassanali DIAGRAM MuTHER Genome-wide association study in individuals of South Asian ancestry identifies six new type 2 diabetes susceptibility loci Nat. Genet. 43 2011 984 989
26. E. Kroon, L.A. Martinson, K. Kadoya, A.G. Bang, O.G. Kelly, S. Eliazer, H. Young, M. Richardson, N.G. Smart, and J. Cunningham Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo Nat. Biotechnol. 26 2008 443 452
27. H. Lango Allen, K. Estrada, G. Lettre, S.I. Berndt, M.N. Weedon, F. Rivadeneira, C.J. Willer, A.U. Jackson, S. Vedantam, and S. Raychaudhuri Hundreds of variants clustered in genomic loci and biological pathways affect human height Nature 467 2010 832 838
28. S. Loewer, M.N. Cabili, M. Guttman, Y.-H. Loh, K. Thomas, I.H. Park, M. Garber, M. Curran, T. Onder, and S. Agarwal Large intergenic non-coding RNA-RoR modulates reprogramming of human induced pluripotent stem cells Nat. Genet. 42 2010 1113 1117
29. J.S. Mattick, and I.V. Makunin Non-coding RNA Hum. Mol. Genet. 15 Spec No 1 2006 R17 R29
30. M.I. McCarthy Genomics, type 2 diabetes, and obesity N. Engl. J. Med. 363 2010 2339 2350
31. T.R. Mercer, M.E. Dinger, S.M. Sunkin, M.F. Mehler, and J.S. Mattick Specific expression of long noncoding RNAs in the mouse brain Proc. Natl. Acad. Sci. USA 105 2008 716 721
32. A. Pauli, E. Valen, M.F. Lin, M. Garber, N.L. Vastenhouw, J.Z. Levin, L. Fan, A. Sandelin, J.L. Rinn, A. Regev, and A.F. Schier Systematic identification of long noncoding RNAs expressed during zebrafish embryogenesis Genome Res. 22 2012 577 591
33. G.D. Penny, G.F. Kay, S.A. Sheardown, S. Rastan, and N. Brockdorff Requirement for Xist in X chromosome inactivation Nature 379 1996 131 137
34. K. Piper, S. Brickwood, L.W. Turnpenny, I.T. Cameron, S.G. Ball, D.I. Wilson, and N.A. Hanley Beta cell differentiation during early human pancreas development J. Endocrinol. 181 2004 11 23
35. J. Ponjavic, P.L. Oliver, G. Lunter, and C.P. Ponting Genomic and transcriptional co-localization of protein-coding and long non-coding RNA pairs in the developing brain PLoS Genet. 5 2009 e1000617
36. P. Ravassard, Y. Hazhouz, S. Pechberty, E. Bricout-Neveu, M. Armanet, P. Czernichow, and R. Scharfmann A genetically engineered human pancreatic β cell line exhibiting glucose-inducible insulin secretion J. Clin. Invest. 121 2011 3589 3597
37. J.L. Rinn, M. Kertesz, J.K. Wang, S.L. Squazzo, X. Xu, S.A. Brugmann, L.H. Goodnough, J.A. Helms, P.J. Farnham, E. Segal, and H.Y. Chang Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs Cell 129 2007 1311 1323
38. R. Scharfmann, X. Xiao, H. Heimberg, J. Mallet, and P. Ravassard Beta cells within single human islets originate from multiple progenitors PLoS ONE 3 2008 e3559
39. F. Schuit, D. Flamez, A. De Vos, and D. Pipeleers Glucose-regulated gene expression maintaining the glucose-responsive state of beta-cells Diabetes 51 Suppl 3 2002 S326 S332
40. A.V. Segrè, L. Groop, V.K. Mootha, M.J. Daly, D. Altshuler DIAGRAM Consortium MAGIC investigators Common inherited variation in mitochondrial genes is not enriched for associations with type 2 diabetes or related glycemic traits PLoS Genet. 6 2010 6
41. V. Senée, C. Chelala, S. Duchatelet, D. Feng, H. Blanc, J.C. Cossec, C. Charon, M. Nicolino, P. Boileau, and D.R. Cavener Mutations in GLIS3 are responsible for a rare syndrome with neonatal diabetes mellitus and congenital hypothyroidism Nat. Genet. 38 2006 682 687
42. J.M. Servitja, and J. Ferrer Transcriptional networks controlling pancreatic development and beta cell function Diabetologia 47 2004 597 613
43. F. Sleutels, R. Zwart, and D.P. Barlow The non-coding Air RNA is required for silencing autosomal imprinted genes Nature 415 2002 810 813
44. R.J. Strawbridge, J. Dupuis, I. Prokopenko, A. Barker, E. Ahlqvist, D. Rybin, J.R. Petrie, M.E. Travers, N. Bouatia-Naji, A.S. Dimas DIAGRAM Consortium GIANT Consortium MuTHER Consortium CARDIoGRAM Consortium C4D Consortium Genome-wide association identifies nine common variants associated with fasting proinsulin levels and provides new insights into the pathophysiology of type 2 diabetes Diabetes 60 2011 2624 2634
45. I. Ulitsky, A. Shkumatava, C.H. Jan, H. Sive, and D.P. Bartel Conserved function of lincRNAs in vertebrate embryonic development despite rapid sequence evolution Cell 147 2011 1537 1550
46. J. van Arensbergen, J. García-Hurtado, I. Moran, M.A. Maestro, X. Xu, M. Van de Casteele, A.L. Skoudy, M. Palassini, H. Heimberg, and J. Ferrer Derepression of Polycomb targets during pancreatic organogenesis allows insulin-producing beta-cells to adopt a neural gene activity program Genome Res. 20 2010 722 732
47. M. van de Bunt, and A.L. Gloyn From genetic association to molecular mechanism Curr. Diab. Rep. 10 2010 452 466
48. D. Van Hoof, K.A. D'Amour, and M.S. German Derivation of insulin-producing cells from human embryonic stem cells Stem Cell Res. (Amst.) 3 2009 73 87
49. B.F. Voight, L.J. Scott, V. Steinthorsdottir, A.P. Morris, C. Dina, R.P. Welch, E. Zeggini, C. Huth, Y.S. Aulchenko, G. Thorleifsson MAGIC investigators GIANT Consortium Twelve type 2 diabetes susceptibility loci identified through large-scale association analysis Nat. Genet. 42 2010 579 589
50. K.C. Wang, and H.Y. Chang Molecular mechanisms of long noncoding RNAs Mol. Cell 43 2011 904 914
51. J.E. Wilusz, H. Sunwoo, and D.L. Spector Long noncoding RNAs: functional surprises from the RNA world Genes Dev. 23 2009 1494 1504
52. Z. Xu, W. Wei, J. Gagneur, S. Clauder-Münster, M. Smolik, W. Huber, and L.M. Steinmetz Antisense expression increases gene expression variability and locus interdependency Mol. Syst. Biol. 7 2011 468
53. E. Zeggini, M.N. Weedon, C.M. Lindgren, T.M. Frayling, K.S. Elliott, H. Lango, N.J. Timpson, J.R. Perry, N.W. Rayner, R.M. Freathy Wellcome Trust Case Control Consortium (WTCCC) Replication of genome-wide association signals in UK samples reveals risk loci for type 2 diabetes Science 316 2007 1336 1341
54. Q. Zhou, J. Brown, A. Kanarek, J. Rajagopal, and D.A. Melton In vivo reprogramming of adult pancreatic exocrine cells to beta-cells Nature 455 2008 627 632