The miR-379/miR-410 cluster at the imprinted Dlk1-Dio3 domain controls neonatal metabolic adaptation

EMBO Journal

Volumn 33, Issue 19, 2014, Pages 2216-2230

  Labialle, Stéphane ^a   Marty, Virginie ^a   Bortolin Cavaillé, Marie Line ^a   Hoareau Osman, Magali ^a   Pradère, Jean Philippe ^b,c   Valet, Philippe ^b,c   Martin, Pascal G P ^a,d,e   Cavaillé, Jérôme ^a  

^a Université Paul Sabatier   (France)

^b INSERM   (France)

^c Departments of Clinical Biochemistry and Sports Medicine   (France)

^d TOXALIM RESEARCH CENTRE IN FOOD TOXICOLOGY   (France)

^e UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

Epigenetic; Genomic imprinting; Metabolic adaptation; MicroRNA; Mouse model

Indexed keywords

GLUCOSE; KETONE; MICRORNA; MICRORNA 379; MICRORNA 410; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; DLK1 PROTEIN, MOUSE; IODIDE PEROXIDASE; IODOTHYRONINE DEIODINASE TYPE III; MESSENGER RNA; MIRN379 MICRORNA, HUMAN; MIRN410 MICRORNA, HUMAN; SIGNAL PEPTIDE;

ADAPTATION; ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; ENERGY; FEMALE; GENE CONTROL; GENE DELETION; GENE DISRUPTION; GENE EXPRESSION; GLUCONEOGENESIS; GLUCOSE HOMEOSTASIS; GLYCOGENOLYSIS; HETEROZYGOTE; HYPOGLYCEMIA; LETHALITY; LIVER; LIVER CELL; MALE; METABOLIC REGULATION; MOLECULAR IMPRINTING; MOUSE; NEWBORN; NEWBORN DEATH; NEWBORN MORTALITY; NONHUMAN; PHYSIOLOGICAL PROCESS; PLACENTAL MAMMALS; ANIMAL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENETICS; GENOME IMPRINTING; HUMAN; KNOCKOUT MOUSE; METABOLISM; MULTIGENE FAMILY; NORTHERN BLOTTING; PATHOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANIMALS, NEWBORN; BIOMARKERS; BLOTTING, NORTHERN; CELLS, CULTURED; FEMALE; GENE EXPRESSION PROFILING; GENOMIC IMPRINTING; GLUCONEOGENESIS; GLYCOGENOLYSIS; HUMANS; HYPOGLYCEMIA; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; IODIDE PEROXIDASE; KETONES; LIVER; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICRORNAS; MULTIGENE FAMILY; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 84908110335     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201387038     Document Type: Article

References (64)

1. Ambros V (2011) MicroRNAs and developmental timing. Curr Opin Genet Dev 21: 511-517
2. Attane C, Foussal C, Le Gonidec S, Benani A, Daviaud D, Wanecq E, Guzman-Ruiz R, Dray C, Bezaire V, Rancoule C, Kuba K, Ruiz-Gayo M, Levade T, Penninger J, Burcelin R, Penicaud L, Valet P, Castan-Laurell I (2012) Apelin treatment increases complete Fatty Acid oxidation, mitochondrial oxidative capacity, and biogenesis in muscle of insulin-resistant mice. Diabetes 61: 310-320
3. Baek D, Villen J, Shin C, Camargo FD, Gygi SP, Bartel DP (2008) The impact of microRNAs on protein output. Nature 455: 64-71
4. Barlow DP, Bartolomei MS (2014) Genomic imprinting in mammals. Cold Spring Harb Perspect Biol 6: pii: a018382.
5. Barrans A, Collet X, Barbaras R, Jaspard B, Manent J, Vieu C, Chap H, Perret B (1994) Hepatic lipase induces the formation of pre-beta 1 high density lipoprotein (HDL) from triacylglycerol-rich HDL2. A study comparing liver perfusion to in vitro incubation with lipases. J Biol Chem 269: 11572-11577
6. Benetatos L, Voulgaris E, Vartholomatos G (2012) DLK1-MEG3 imprinted domain microRNAs in cancer biology. Crit Rev Eukaryot Gene Expr 22: 1-15
7. Bicker S, Khudayberdiev S, Weiss K, Zocher K, Baumeister S, Schratt G (2013) The DEAH-box helicase DHX36 mediates dendritic localization of the neuronal precursor-microRNA-134. Genes Dev 27: 991-996
8. Brennan AJ, Sharp JA, Digby MR, Nicholas KR (2007) The tammar wallaby: a model to examine endocrine and local control of lactation. IUBMB Life 59: 146-150
9. Bushati N, Cohen SM (2007) microRNA functions. Annu Rev Cell Dev Biol 23: 175-205
10. Cederbaum AI (2010) Role of CYP2E1 in ethanol-induced oxidant stress, fatty liver and hepatotoxicity. Dig Dis 28: 802-811
11. Charalambous M, da Rocha ST, Ferguson-Smith AC (2007) Genomic imprinting, growth control and the allocation of nutritional resources: consequences for postnatal life. Curr Opin Endocrinol Diabetes Obes 14: 3-12
12. Charalambous M, Ferron SR, da Rocha ST, Murray AJ, Rowland T, Ito M, Schuster-Gossler K, Hernandez A, Ferguson-Smith AC (2012) Imprinted gene dosage is critical for the transition to independent life. Cell Metab 15: 209-221
13. Charalambous M, da Rocha ST, Hernandez A, Ferguson-Smith AC (2014) Perturbations to the IGF1 growth pathway and adult energy homeostasis following disruption of mouse chromosome 12 imprinting. Acta Physiol (Oxf) 210: 174-187
14. Chiang HR, Schoenfeld LW, Ruby JG, Auyeung VC, Spies N, Baek D, Johnston WK, Russ C, Luo S, Babiarz JE, Blelloch R, Schroth GP, Nusbaum C, Bartel DP (2010) Mammalian microRNAs: experimental evaluation of novel and previously annotated genes. Genes & Development 24: 992-1009
15. Christensen M, Larsen LA, Kauppinen S, Schratt G (2010) Recombinant adeno-associated virus-mediated microRNA delivery into the postnatal mouse brain reveals a role for miR-134 in dendritogenesis in vivo. Front Neural Circuits 3: 16
16. Constancia M, Kelsey G, Reik W (2004) Resourceful imprinting. Nature 432: 53-57
17. Davis E, Caiment F, Tordoir X, Cavaille J, Ferguson-Smith A, Cockett N, Georges M, Charlier C (2005) RNAi-mediated allelic trans-interaction at the imprinted Rtl1/Peg11 locus. Curr Biol 15: 743-749
18. Dorn GW 2nd (2013) MicroRNAs and the butterfly effect. Cell Cycle 12: 707-708
19. Edwards CA, Mungall AJ, Matthews L, Ryder E, Gray DJ, Pask AJ, Shaw G, Graves JA, Rogers J, Dunham I, Renfree MB, Ferguson-Smith AC (2008) The evolution of the DLK1-DIO3 imprinted domain in mammals. PLoS Biol 6: e135
20. Fabian MR, Sonenberg N (2012) The mechanics of miRNA-mediated gene silencing: a look under the hood of miRISC. Nat Struct Mol Biol 19: 586-593
21. Fiore R, Khudayberdiev S, Christensen M, Siegel G, Flavell SW, Kim TK, Greenberg ME, Schratt G (2009) Mef2-mediated transcription of the miR379-410 cluster regulates activity-dependent dendritogenesis by fine-tuning Pumilio2 protein levels. EMBO J 28: 697-710
22. Frontera M, Dickins B, Plagge A, Kelsey G (2008) Imprinted genes, postnatal adaptations and enduring effects on energy homeostasis. Adv Exp Med Biol 626: 41-61
23. Gao J, Wang WY, Mao YW, Graff J, Guan JS, Pan L, Mak G, Kim D, Su SC, Tsai LH (2010) A novel pathway regulates memory and plasticity via SIRT1 and miR-134. Nature 466: 1105-1109
24. Giraldez AJ (2010) microRNAs, the cell's Nepenthe: clearing the past during the maternal-to-zygotic transition and cellular reprogramming. Curr Opin Genet Dev 20: 369-375
25. Girard J, Ferre P, Pegorier JP, Duee PH (1992) Adaptations of glucose and fatty acid metabolism during perinatal period and suckling-weaning transition. Physiol Rev 72: 507-562
26. Girardot M, Cavaille J, Feil R (2012) Small regulatory RNAs controlled by genomic imprinting and their contribution to human disease. Epigenetics 7: 1341-1348.
27. Gonzalez FJ (2007) The 2006 Bernard B. Brodie Award Lecture. Cyp2e1. Drug Metab Dispos 35: 1-8
28. Hart SN, Cui Y, Klaassen CD, Zhong XB (2009) Three patterns of cytochrome P450 gene expression during liver maturation in mice. Drug Metab Dispos 37: 116-121
29. Helwak A, Kudla G, Dudnakova T, Tollervey D (2013) Mapping the human miRNA interactome by CLASH reveals frequent noncanonical binding. Cell 153: 654-665
30. Hondares E, Rosell M, Gonzalez FJ, Giralt M, Iglesias R, Villarroya F (2010) Hepatic FGF21 expression is induced at birth via PPARalpha in response to milk intake and contributes to thermogenic activation of neonatal brown fat. Cell Metab 11: 206-212
31. Jimenez-Mateos EM, Engel T, Merino-Serrais P, McKiernan RC, Tanaka K, Mouri G, Sano T, O'Tuathaigh C, Waddington JL, Prenter S, Delanty N, Farrell MA, O'Brien DF, Conroy RM, Stallings RL, DeFelipe J, Henshall DC (2012) Silencing microRNA-134 produces neuroprotective and prolonged seizure-suppressive effects. Nat Med 18: 1087-1094
32. Kagami M, Sekita Y, Nishimura G, Irie M, Kato F, Okada M, Yamamori S, Kishimoto H, Nakayama M, Tanaka Y, Matsuoka K, Takahashi T, Noguchi M, Masumoto K, Utsunomiya T, Kouzan H, Komatsu Y, Ohashi H, Kurosawa K, Kosaki K et al (2008) Deletions and epimutations affecting the human 14q32.2 imprinted region in individuals with paternal and maternal upd(14)-like phenotypes. Nat Genet 40: 237-242
33. Kameswaran V, Bramswig NC, McKenna LB, Penn M, Schug J, Hand NJ, Chen Y, Choi I, Vourekas A, Won KJ, Liu C, Vivek K, Naji A, Friedman JR, Kaestner KH (2014) Epigenetic regulation of the DLK1-MEG3 microRNA cluster in human type 2 diabetic islets. Cell Metab 19: 135-145
34. Kaneko-Ishino T, Kohda T, Ishino F (2003) The regulation and biological significance of genomic imprinting in mammals. J Biochem 133: 699-711
35. Labialle S, Cavaille J (2011) Do repeated arrays of regulatory small-RNA genes elicit genomic imprinting?: Concurrent emergence of large clusters of small non-coding RNAs and genomic imprinting at four evolutionarily distinct eutherian chromosomal loci. Bioessays 33: 565-573
36. Labialle S, Vitali P, Cavaille J (2011) Imprinted Small Non-coding RNA Genes: Time to Decipher their Physiological Functions. In Non Coding RNAs and Epigenetic Regulation of Gene Expression-Drivers of Natural Selection, Morris KV (ed.), pp. 47-75. Norfolk, UK: Caister Academic Press.
37. Leung AK, Sharp PA (2010) MicroRNA functions in stress responses. Mol Cell 40: 205-215
38. Lewis A, Redrup L (2005) Genetic imprinting: conflict at the Callipyge locus. Curr Biol 15: R291-294
39. Lin SP, Youngson N, Takada S, Seitz H, Reik W, Paulsen M, Cavaille J, Ferguson-Smith AC (2003) Asymmetric regulation of imprinting on the maternal and paternal chromosomes at the Dlk1-Gtl2 imprinted cluster on mouse chromosome 12. Nat Genet 35: 97-102
40. Liu L, Luo GZ, Yang W, Zhao X, Zheng Q, Lv Z, Li W, Wu HJ, Wang L, Wang XJ, Zhou Q (2010) Activation of the imprinted Dlk1-Dio3 region correlates with pluripotency levels of mouse stem cells. J Biol Chem 285: 19483-19490
41. Medeiros LA, Dennis LM, Gill ME, Houbaviy H, Markoulaki S, Fu D, White AC, Kirak O, Sharp PA, Page DC, Jaenisch R (2011) Mir-290-295 deficiency in mice results in partially penetrant embryonic lethality and germ cell defects. Proc Natl Acad Sci USA 108: 14163-14168
42. Mendell JT, Olson EN (2012) MicroRNAs in stress signaling and human disease. Cell 148: 1172-1187
43. Moore T, Haig D (1991) Genomic imprinting in mammalian development: a parental tug-of-war. Trends Genet 7: 45-49
44. Noguer-Dance M, Abu-Amero S, Al-Khtib M, Lefevre A, Coullin P, Moore GE, Cavaille J (2010) The primate-specific microRNA gene cluster (C19MC) is imprinted in the placenta. Hum Mol Genet 19: 3566-3582
45. Park CY, Choi YS, McManus MT (2010) Analysis of microRNA knockouts in mice. Hum Mol Genet 19: R169-175
46. Park CY, Jeker LT, Carver-Moore K, Oh A, Liu HJ, Cameron R, Richards H, Li Z, Adler D, Yoshinaga Y, Martinez M, Nefadov M, Abbas AK, Weiss A, Lanier LL, de Jong PJ, Bluestone JA, Srivastava D, McManus MT (2012) A resource for the conditional ablation of microRNAs in the mouse. Cell Rep 1: 385-391
47. Poethig RS (2009) Small RNAs and developmental timing in plants. Curr Opin Genet Dev 19: 374-378
48. Potthoff MJ, Kliewer SA, Mangelsdorf DJ (2012) Endocrine fibroblast growth factors 15/19 and 21: from feast to famine. Genes Dev 26: 312-324
49. Rago L, Beattie R, Taylor V, Winter J (2014) miR379-410 cluster miRNAs regulate neurogenesis and neuronal migration by fine-tuning N-cadherin. EMBO J 33: 906-920
50. Raj A, Rifkin SA, Andersen E, van Oudenaarden A (2010) Variability in gene expression underlies incomplete penetrance. Nature 463: 913-918
51. da Rocha ST, Edwards CA, Ito M, Ogata T, Ferguson-Smith AC (2008) Genomic imprinting at the mammalian Dlk1-Dio3 domain. Trends Genet 24: 306-316
52. Schratt GM, Tuebing F, Nigh EA, Kane CG, Sabatini ME, Kiebler M, Greenberg ME (2006) A brain-specific microRNA regulates dendritic spine development. Nature 439: 283-289
53. Seitz H, Youngson N, Lin SP, Dalbert S, Paulsen M, Bachellerie JP, Ferguson-Smith AC, Cavaille J (2003) Imprinted microRNA genes transcribed antisense to a reciprocally imprinted retrotransposon-like gene. Nat Genet 34: 261-262
54. Sekita Y, Wagatsuma H, Nakamura K, Ono R, Kagami M, Wakisaka N, Hino T, Suzuki-Migishima R, Kohda T, Ogura A, Ogata T, Yokoyama M, Kaneko-Ishino T, Ishino F (2008) Role of retrotransposon-derived imprinted gene, Rtl1, in the feto-maternal interface of mouse placenta. Nat Genet 40: 243-248
55. Stadtfeld M, Apostolou E, Akutsu H, Fukuda A, Follett P, Natesan S, Kono T, Shioda T, Hochedlinger K (2010) Aberrant silencing of imprinted genes on chromosome 12qF1 in mouse induced pluripotent stem cells. Nature 465: 175-181
56. Thumelin S, Esser V, Charvy D, Kolodziej M, Zammit VA, McGarry D, Girard J, Pegorier JP (1994) Expression of liver carnitine palmitoyltransferase I and II genes during development in the rat. Biochem J 300(Pt 2): 583-587
57. Turgeon B, Meloche S (2009) Interpreting neonatal lethal phenotypes in mouse mutants: insights into gene function and human diseases. Physiol Rev 89: 1-26
58. Wallace C, Smyth DJ, Maisuria-Armer M, Walker NM, Todd JA, Clayton DG (2010) The imprinted DLK1-MEG3 gene region on chromosome 14q32.2 alters susceptibility to type 1 diabetes. Nat Genet 42: 68-71
59. Wang ND, Finegold MJ, Bradley A, Ou CN, Abdelsayed SV, Wilde MD, Taylor LR, Wilson DR, Darlington GJ (1995) Impaired energy homeostasis in C/EBP alpha knockout mice. Science 269: 1108-1112
60. Wang Q, Chow J, Hong J, Smith AF, Moreno C, Seaby P, Vrana P, Miri K, Tak J, Chung ED, Mastromonaco G, Caniggia I, Varmuza S (2011) Recent acquisition of imprinting at the rodent Sfmbt2 locus correlates with insertion of a large block of miRNAs. BMC Genomics 12: 204
61. Wilkins JF, Haig D (2003) What good is genomic imprinting: the function of parent-specific gene expression. Nat Rev Genet 4: 359-368
62. Wolf JB, Hager R (2006) A maternal-offspring coadaptation theory for the evolution of genomic imprinting. PLoS Biol 4: e380
63. Yubero P, Hondares E, Carmona MC, Rossell M, Gonzalez FJ, Iglesias R, Giralt M, Villarroya F (2004) The developmental regulation of peroxisome proliferator-activated receptor-gamma coactivator-1alpha expression in the liver is partially dissociated from the control of gluconeogenesis and lipid catabolism. Endocrinology 145: 4268-4277
64. Zhang Y, Hagedorn CH, Wang L (2011) Role of nuclear receptor SHP in metabolism and cancer. Biochim Biophys Acta 1812: 893-908