Small RNA sequencing reveals miR-642a-3p as a novel adipocyte-specific microRNA and miR-30 as a key regulator of human adipogenesis

Genome Biology

Volumn 12, Issue 7, 2011, Pages

  Zaragosi, Laure Emmanuelle ^a,b   Wdziekonski, Brigitte ^a,b   Brigand, Kevin L ^a,b   Villageois, Phi ^a,b   Mari, Bernard ^a,b   Waldmann, Rainer ^a,b   Dani, Christian ^a,b   Barbry, Pascal ^a,b  

^a CNRS   (France)

^b UNIVERSITÉ CÔTE D'AZUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 30; MICRORNA 30A; MICRORNA 30D; MICRORNA 378; MICRORNA 642A 3P; TRANSCRIPTION FACTOR RUNX2; UNCLASSIFIED DRUG; MIRN30 MICRORNA, HUMAN; MIRN642 MICRORNA, HUMAN;

ADIPOCYTE; ADIPOGENESIS; ADIPOSE TISSUE; ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME INHIBITION; GENE LOSS; GENE OVEREXPRESSION; GENE SILENCING; GENE TARGETING; GENETIC GAIN; HUMAN; HUMAN CELL; HUMAN TISSUE; MOLECULAR CLONING; RNA SEQUENCE; STEM CELL; UPREGULATION; ANTIBODY SPECIFICITY; CHEMISTRY; DRUG ANTAGONISM; GENE EXPRESSION REGULATION; GENETICS; HIGH THROUGHPUT SEQUENCING; METABOLISM; SEQUENCE ANALYSIS;

ADIPOCYTES; ADIPOGENESIS; CELL DIFFERENTIATION; CORE BINDING FACTOR ALPHA 1 SUBUNIT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MICRORNAS; ORGAN SPECIFICITY; OSTEOGENESIS; SEQUENCE ANALYSIS, RNA; UP-REGULATION;

EID: 79960565215     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2011-12-7-r64     Document Type: Article

References (42)

1. Rodriguez AM, Elabd C, Delteil F, Astier J, Vernochet C, Saint-Marc P, Guesnet J, Guezennec A, Amri EZ, Dani C. Adipocyte differentiation of multipotent cells established from human adipose tissue. Biochem Biophys Res Commun 2004, 315:255-263. 10.1016/j.bbrc.2004.01.053, 14766202.
2. Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H, Alfonso ZC, Fraser JK, Benhaim P, Hedrick MH. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 2002, 13:4279-4295. 10.1091/mbc.E02-02-0105, 138633, 12475952.
3. Spalding KL, Arner E, Westermark PO, Bernard S, Buchholz BA, Bergmann O, Blomqvist L, Hoffstedt J, Naslund E, Britton T, Concha H, Hassan M, Rydén M, Frisén J, Arner P. Dynamics of fat cell turnover in humans. Nature 2008, 453:783-787. 10.1038/nature06902, 18454136.
4. Rosen ED, Spiegelman BM. Molecular regulation of adipogenesis. Annu Rev Cell Dev Biol 2000, 16:145-171. 10.1146/annurev.cellbio.16.1.145, 11031233.
5. Guilak F, Lott KE, Awad HA, Cao Q, Hicok KC, Fermor B, Gimble JM. Clonal analysis of the differentiation potential of human adipose-derived adult stem cells. J Cell Physiol 2006, 206:229-237. 10.1002/jcp.20463, 16021633.
6. Muraglia A, Cancedda R, Quarto R. Clonal mesenchymal progenitors from human bone marrow differentiate in vitro according to a hierarchical model. J Cell Sci 2000, 113:1161-1166.
7. Ahdjoudj S, Fromigue O, Marie PJ. Plasticity and regulation of human bone marrow stromal osteoprogenitor cells: potential implication in the treatment of age-related bone loss. Histol Histopathol 2004, 19:151-157.
8. Pilat MJ, Ensor DS, Bosch JC. Cascade impactor for sizing particulates in emission sources. Am Ind Hyg Assoc J 1971, 32:508-511.
9. Gimble JM, Robinson CE, Wu X, Kelly KA. The function of adipocytes in the bone marrow stroma: an update. Bone 1996, 19:421-428. 10.1016/S8756-3282(96)00258-X, 8922639.
10. Meunier P, Aaron J, Edouard C, Vignon G. Osteoporosis and the replacement of cell populations of the marrow by adipose tissue. A quantitative study of 84 iliac bone biopsies. Clin Orthop Relat Res 1971, 80:147-154.
11. Muruganandan S, Roman AA, Sinal CJ. Adipocyte differentiation of bone marrow-derived mesenchymal stem cells: cross talk with the osteoblastogenic program. Cell Mol Life Sci 2009, 66:236-253. 10.1007/s00018-008-8429-z, 18854943.
12. Baulcombe D. RNA silencing. Trends Biochem Sci 2005, 30:290-293. 10.1016/j.tibs.2005.04.012, 15950871.
13. Xie X, Lu J, Kulbokas EJ, Golub TR, Mootha V, Lindblad-Toh K, Lander ES, Kellis M. Systematic discovery of regulatory motifs in human promoters and 3' UTRs by comparison of several mammals. Nature 2005, 434:338-345. 10.1038/nature03441, 2923337, 15735639.
14. Xie H, Lim B, Lodish HF. MicroRNAs induced during adipogenesis that accelerate fat cell development are downregulated in obesity. Diabetes 2009, 58:1050-1057. 10.2337/db08-1299, 2671055, 19188425.
15. Esau C, Kang X, Peralta E, Hanson E, Marcusson EG, Ravichandran LV, Sun Y, Koo S, Perera RJ, Jain R, Dean NM, Freier SM, Bennett CF, Lollo B, Griffey R. MicroRNA-143 regulates adipocyte differentiation. J Biol Chem 2004, 279:52361-52365. 10.1074/jbc.C400438200, 15504739.
16. Wang Q, Li YC, Wang J, Kong J, Qi Y, Quigg RJ, Li X. miR-17-92 cluster accelerates adipocyte differentiation by negatively regulating tumor-suppressor Rb2/p130. Proc Natl Acad Sci USA 2008, 105:2889-2894. 10.1073/pnas.0800178105, 2268555, 18287052.
17. Kim YJ, Hwang SJ, Bae YC, Jung JS. miR-21 regulates adipogenic differentiation through the modulation of TGF-beta signaling in mesenchymal stem cells derived from human adipose tissue. Stem Cells 2009, 27:3093-3102.
18. Huang J, Zhao L, Xing L, Chen D. MicroRNA-204 regulates Runx2 protein expression and mesenchymal progenitor cell differentiation. Stem Cells 2010, 28:357-364. 2837600, 20039258.
19. Lin Q, Gao Z, Alarcon RM, Ye J, Yun Z. A role of miR-27 in the regulation of adipogenesis. FEBS J 2009, 276:2348-2358. 10.1111/j.1742-4658.2009.06967.x, 19348006.
20. Li Z, Hassan MQ, Jafferji M, Garzon R, Croce CM, van Wijnen AJ, Stein JL, Stein GS, Lian JB. Biological functions of miR-29b contribute to positive regulation of osteoblast differentiation. J Biol Chem 2009, 284:15676-15684. 10.1074/jbc.M809787200, 2708864, 19342382.
21. Weaver RE, Donnelly D, Wabitsch M, Grant PJ, Balmforth AJ. Functional expression of glucose-dependent insulinotropic polypeptide receptors is coupled to differentiation in a human adipocyte model. Int J Obes (Lond) 2008, 32:1705-1711.
22. Hauner H, Glatting G, Kaminska D, Pfeiffer EF. Effects of gastric inhibitory polypeptide on glucose and lipid metabolism of isolated rat adipocytes. Ann Nutr Metab 1988, 32:282-288. 10.1159/000177467, 3076052.
23. Miyawaki K, Yamada Y, Ban N, Ihara Y, Tsukiyama K, Zhou H, Fujimoto S, Oku A, Tsuda K, Toyokuni S, Hiai H, Mizunoya W, Fushiki T, Holst JJ, Makino M, Tashita A, Kobara Y, Tsubamoto Y, Jinnouchi T, Jomori T, Seino Y. Inhibition of gastric inhibitory polypeptide signaling prevents obesity. Nat Med 2002, 8:738-742. 10.1038/nm727, 12068290.
24. Elabd C, Chiellini C, Massoudi A, Cochet O, Zaragosi LE, Trojani C, Michiels JF, Weiss P, Carle G, Rochet N, Dechesne CA, Ailhaud G, Dani C, Amri EZ. Human adipose tissue-derived multipotent stem cells differentiate in vitro and in vivo into osteocyte-like cells. Biochem Biophys Res Commun 2007, 361:342-348. 10.1016/j.bbrc.2007.06.180, 17651696.
25. White UA, Stephens JM. Transcriptional factors that promote formation of white adipose tissue. Mol Cell Endocrinol 2010, 318:10-14. 10.1016/j.mce.2009.08.023, 3079373, 19733624.
26. Hong JH, Hwang ES, McManus MT, Amsterdam A, Tian Y, Kalmukova R, Mueller E, Benjamin T, Spiegelman BM, Sharp PA, Hopkins N, Yaffe MB. TAZ, a transcriptional modulator of mesenchymal stem cell differentiation. Science 2005, 309:1074-1078. 10.1126/science.1110955, 16099986.
27. Le Brigand K, Robbe-Sermesant K, Mari B, Barbry P. MiRonTop: mining microRNAs targets across large scale gene expression studies. Bioinformatics 2010, 26:3131-3132. 10.1093/bioinformatics/btq589, 2995122, 20959382.
28. Komori T. Requisite roles of Runx2 and Cbfb in skeletal development. J Bone Miner Metab 2003, 21:193-197.
29. Kahai S, Lee SC, Lee DY, Yang J, Li M, Wang CH, Jiang Z, Zhang Y, Peng C, Yang BB. MicroRNA miR-378 regulates nephronectin expression modulating osteoblast differentiation by targeting GalNT-7. PLoS One 2009, 4:e7535. 10.1371/journal.pone.0007535, 2760121, 19844573.
30. Gerin I, Bommer GT, McCoin CS, Sousa KM, Krishnan V, Macdougald OA. Roles for miRNA-378/378 in adipocyte gene expression and lipogenesis. Am J Physiol Endocrinol Metab 2010, 299:E198-206. 2928515, 20484008.
31. Martinelli R, Nardelli C, Pilone V, Buonomo T, Liguori R, Castano I, Buono P, Masone S, Persico G, Forestieri P, Pastore L, Sacchetti L. miR-519d overexpression is associated with human obesity. Obesity (Silver Spring) 2010, 18:2170-2176.
32. Picard F, Gehin M, Annicotte J, Rocchi S, Champy MF, O'Malley BW, Chambon P, Auwerx J. SRC-1 and TIF2 control energy balance between white and brown adipose tissues. Cell 2002, 111:931-941. 10.1016/S0092-8674(02)01169-8, 12507421.
33. Lee YS, Shibata Y, Malhotra A, Dutta A. A novel class of small RNAs: tRNA-derived RNA fragments (tRFs). Genes Dev 2009, 23:2639-2649. 10.1101/gad.1837609, 2779758, 19933153.
34. Rodriguez A-M, Pisani D, Dechesne CA, Turc-Carel C, Kurzenne J-Y, Wdziekonski B, Villageois A, Bagnis C, Breittmayer J-P, Groux H, Ailhaud G, Dani C. Transplantation of a multipotent cell population from human adipose tissue induces dystrophin expression in the immunocompetent mdx mouse. J Exp Med 2005, 201:1397-1405. 10.1084/jem.20042224, 2213197, 15867092.
35. Wdziekonski B, Villageois P, Dani C. Development of adipocytes from differentiated ES cells. Methods Enzymol 2003, 365:268-277.
36. Massiera F, Saint-Marc P, Seydoux J, Murata T, Kobayashi T, Narumiya S, Guesnet P, Amri E-Z, Negrel R, Ailhaud G. Arachidonic acid and prostacyclin signaling promote adipose tissue development: a human health concern?. J Lipid Res 2003, 44:271-279. 10.1194/jlr.M200346-JLR200, 12576509.
37. NCBI Gene Expression Omnibus. , http://www.ncbi.nlm.nih.gov/geo/
38. Bioconductor. , http://www.bioconductor.org
39. Ortega FJ, Moreno-Navarrete JM, Pardo G, Sabater M, Hummel M, Ferrer A, Rodriguez-Hermosa JI, Ruiz B, Ricart W, Peral B, Fernández-Real JM. MiRNA expression profile of human subcutaneous adipose and during adipocyte differentiation. PLoS One 2010, 5:e9022. 10.1371/journal.pone.0009022, 2814866, 20126310.
40. Kajimoto K, Naraba H, Iwai N. MicroRNA and 3T3-L1 pre-adipocyte differentiation. RNA 2006, 12:1626-1632. 10.1261/rna.7228806, 1557704, 16870994.
41. Qin L, Chen Y, Niu Y, Chen W, Wang Q, Xiao S, Li A, Xie Y, Li J, Zhao X, He Z, Mo D. A deep investigation into the adipogenesis mechanism: profile of microRNAs regulating adipogenesis by modulating the canonical Wnt/beta-catenin signaling pathway. BMC Genomics 2010, 11:320. 10.1186/1471-2164-11-320, 2895628, 20492721.
42. Oskowitz AZ, Lu J, Penfornis P, Ylostalo J, McBride J, Flemington EK, Prockop DJ, Pochampally R. Human multipotent stromal cells from bone marrow and microRNA: Regulation of differentiation and leukemia inhibitory factor expression. Proc Natl Acad Sci USA 2008, 105:18372-18377. 10.1073/pnas.0809807105, 2587615, 19011087.