MicroRNAs in the growth plate are responsive to nutritional cues: Association between miR-140 and SIRT1

Journal of Nutritional Biochemistry

Volumn 23, Issue 11, 2012, Pages 1474-1481

  Pando, Rakefet ^a,b   Even Zohar, Naomi ^a,b   Shtaif, Biana ^a,b   Edry, Liat ^b   Shomron, Noam ^b   Phillip, Moshe ^a,b   Gat Yablonski, Galia ^a  

^a SCHNEIDER CHILDREN S MEDICAL CENTER OF ISRAEL   (Israel)

^b TEL AVIV UNIVERSITY   (Israel)

Author keywords

Catch up growth; Growth plate; MicroRNA; MiR 140; SIRT1

Indexed keywords

MICRORNA; MICRORNA 140; SIRTUIN 1; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ARTICLE; DIET RESTRICTION; EPIGENETICS; EPIPHYSIS; GENE CONTROL; GENE EXPRESSION; GROWTH PLATE; IMMUNOBLOTTING; MALE; MICROARRAY ANALYSIS; NONHUMAN; NUTRITIONAL ASSESSMENT; POLYMERASE CHAIN REACTION; PROTEIN TARGETING; RAT;

3' UNTRANSLATED REGIONS; ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; CHONDROCYTES; EPIGENESIS, GENETIC; GROWTH PLATE; HISTONE DEACETYLASES; HUMANS; INSULIN-LIKE GROWTH FACTOR BINDING PROTEINS; INSULIN-LIKE GROWTH FACTOR I; MALE; MICRORNAS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, IGF TYPE 1; SIRTUIN 1;

ANIMALIA; RATTUS;

EID: 84867708109     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2011.09.010     Document Type: Article

References (55)

1. Holness M.J., Caton P.W., Sugden M.C. Acute and long-term nutrient-led modifications of gene expression: potential role of SIRT1 as a central co-ordinator of short and longer-term programming of tissue function. Nutrition 2010, 26:491-501.
2. He Z., Sontheimer E.J. "siRNAs and miRNAs": a meeting report on RNA silencing. RNA 2004, 10:1165-1173.
3. Chen K., Rajewsky N. The evolution of gene regulation by transcription factors and microRNAs. Nature reviews 2007, 8:93-103.
4. Cuellar T.L., McManus M.T. MicroRNAs and endocrine biology. J Endocrinol 2005, 187:327-332.
5. Schickel R., Boyerinas B., Park S.M., Peter M.E. MicroRNAs: key players in the immune system, differentiation, tumorigenesis and cell death. Oncogene 2008, 27:5959-5974.
6. Baltimore D., Boldin M.P., O'Connell R.M., Rao D.S., Taganov K.D. MicroRNAs: new regulators of immune cell development and function. Nat Immunol 2008, 9:839-845.
7. Kim J., Inoue K., Ishii J., Vanti W.B., Voronov S.V., Murchison E., et al. A microRNA feedback circuit in midbrain dopamine neurons. Science 2007, 317:1220-1224.
8. Esau C., Kang X., Peralta E., Hanson E., Marcusson E.G., Ravichandran L.V., et al. MicroRNA-143 regulates adipocyte differentiation. J Biol Chem 2004, 279:52361-52365.
9. Zhang J., Jima D.D., Jacobs C., Fischer R., Gottwein E., Huang G., et al. Patterns of microRNA expression characterize stages of human B-cell differentiation. Blood 2009, 113:4586-4594.
10. Poy M.N., Eliasson L., Krutzfeldt J., Kuwajima S., Ma X., Macdonald P.E., et al. A pancreatic islet-specific microRNA regulates insulin secretion. Nature 2004, 432:226-230.
11. Papagiannakopoulos T., Kosik K.S. MicroRNAs: regulators of oncogenesis and stemness. BMC Med 2008, 6:15.
12. Calin G.A., Croce C.M. MicroRNA signatures in human cancers. Nat Rev Cancer 2006, 6:857-866.
13. Pauley K.M., Cha S., Chan E.K. MicroRNA in autoimmunity and autoimmune diseases. J Autoimmun 2009, 32:189-194.
14. Boersma B., Wit J.M. Catch-up growth. Endocr Rev 1997, 18:646-661.
15. Gafni R.I., Baron J. Catch-up growth: possible mechanisms. Pediatr Nephrol 2000, 14:616-619.
16. Gat-Yablonski G., Shtaif B., Abraham E., Phillip M. Nutrition-induced catch-up growth at the growth plate. J Pediatr Endocrinol Metab 2008, 21:879-893.
17. Maor G., Rochwerger M., Segev Y., Phillip M. Leptin acts as a growth factor on the chondrocytes of skeletal growth centers. J Bone Miner Res 2002, 17:1034-1043.
18. Gat-Yablonski G., Ben-Ari T., Shtaif B., Potievsky O., Moran O., Eshet R., et al. Leptin reverses the inhibitory effect of caloric restriction on longitudinal growth. Endocrinology 2004, 145:343-350.
19. Ben-Eliezer M., Phillip M., Gat-Yablonski G. Leptin regulates chondrogenic differentiation in ATDC5 cell-line through JAK/STAT and MAPK pathways. Endocrine 2007, 32:235-244.
20. Schipani E., Ryan H.E., Didrickson S., Kobayashi T., Knight M., Johnson R.S. Hypoxia in cartilage: HIF-1alpha is essential for chondrocyte growth arrest and survival. Genes Dev 2001, 15:2865-2876.
21. Even-Zohar N., Jacob J., Amariglio N., Rechavi G., Potievsky O., Phillip M., et al. Nutrition-induced catch-up growth increases hypoxia inducible factor 1alpha RNA levels in the growth plate. Bone 2008, 42:505-515.
22. Tuddenham L., Wheeler G., Ntounia-Fousara S., Waters J., Hajihosseini M.K., Clark I., et al. The cartilage specific microRNA-140 targets histone deacetylase 4 in mouse cells. FEBS letters 2006, 580:4214-4217.
23. Rosenfeld N., Aharonov R., Meiri E., Rosenwald S., Spector Y., Zepeniuk M., et al. MicroRNAs accurately identify cancer tissue origin. Nat Biotechnol 2008, 26:462-469.
24. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods (San Diego, Calif. 2001, 25:402-408.
25. Nicolas F.E., Pais H., Schwach F., Lindow M., Kauppinen S., Moulton V., et al. Experimental identification of microRNA-140 targets by silencing and overexpressing miR-140. RNA 2008, 14:2513-2520.
26. Vizioli M.G., Sensi M., Miranda C., Cleris L., Formelli F., Anania M.C., et al. IGFBP7: an oncosuppressor gene in thyroid carcinogenesis. Oncogene 2010, 29:3835-3844.
27. Cohen H.Y., Miller C., Bitterman K.J., Wall N.R., Hekking B., Kessler B., et al. Calorie restriction promotes mammalian cell survival by inducing the SIRT1 deacetylase. Science 2004, 305:390-392.
28. Voorhoeve P.M., le Sage C., Schrier M., Gillis A.J., Stoop H., Nagel R., et al. A genetic screen implicates miRNA-372 and miRNA-373 as oncogenes in testicular germ cell tumors. Cell 2006, 124:1169-1181.
29. Kanfi Y., Peshti V., Gozlan Y.M., Rathaus M., Gil R., Cohen H.Y. Regulation of SIRT1 protein levels by nutrient availability. FEBS letters 2008, 582:2417-2423.
30. Chen D., Bruno J., Easlon E., Lin S.J., Cheng H.L., Alt F.W., et al. Tissue-specific regulation of SIRT1 by calorie restriction. Genes Dev 2008, 22:1753-1757.
31. McBurney M.W., Yang X., Jardine K., Hixon M., Boekelheide K., Webb J.R., et al. The mammalian SIR2alpha protein has a role in embryogenesis and gametogenesis. Mol Cell Biol 2003, 23:38-54.
32. Jin Q., Yan T., Ge X., Sun C., Shi X., Zhai Q. Cytoplasm-localized SIRT1 enhances apoptosis. J Cell Physiol 2007, 213:88-97.
33. Bernstein E., Kim S.Y., Carmell M.A., Murchison E.P., Alcorn H., Li M.Z., et al. Dicer is essential for mouse development. Nat Genet 2003, 35:215-217.
34. Kobayashi T., Lu J., Cobb B.S., Rodda S.J., McMahon A.P., Schipani E., et al. Dicer-dependent pathways regulate chondrocyte proliferation and differentiation. Proc Natl Acad Sci U S A 2008, 105:1949-1954.
35. Harfe B.D., McManus M.T., Mansfield J.H., Hornstein E., Tabin C.J. The RNaseIII enzyme Dicer is required for morphogenesis but not patterning of the vertebrate limb. Proc Natl Acad Sci U S A 2005, 102:10898-10903.
36. Wienholds E., Kloosterman W.P., Miska E., Alvarez-Saavedra E., Berezikov E., de Bruijn E., et al. MicroRNA expression in zebrafish embryonic development. Science 2005, 309:310-311.
37. Vega R.B., Matsuda K., Oh J., Barbosa A.C., Yang X., Meadows E., et al. Histone deacetylase 4 controls chondrocyte hypertrophy during skeletogenesis. Cell 2004, 119:555-566.
38. Colnot C., Romero D.M., Huang S., Helms J.A. Mechanisms of action of demineralized bone matrix in the repair of cortical bone defects. Clin Orthop Relat Res 2005, 69-78.
39. Eberhart J.K., He X., Swartz M.E., Yan Y.L., Song H., Boling T.C., et al. MicroRNA Mirn140 modulates Pdgf signaling during palatogenesis. Nat Genet 2008, 40:290-298.
40. Tavazoie S.F., Alarcon C., Oskarsson T., Padua D., Wang Q., Bos P.D., et al. Endogenous human microRNAs that suppress breast cancer metastasis. Nature 2008, 451:147-152.
41. Chan J.A., Krichevsky A.M., Kosik K.S. MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res 2005, 65:6029-6033.
42. Pais H., Nicolas F.E., Soond S.M., Swingler T.E., Clark I.M., Chantry A., et al. Analyzing mRNA expression identifies Smad3 as a microRNA-140 target regulated only at protein level. RNA 2010, 16:489-494.
43. Colnot C. Cellular and molecular interactions regulating skeletogenesis. J Cell Biochem 2005, 95:688-697.
44. Picard F., Kurtev M., Chung N., Topark-Ngarm A., Senawong T., Machado De Oliveira R., et al. Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-gamma. Nature 2004, 429:771-776.
45. Rodgers J.T., Lerin C., Gerhart-Hines Z., Puigserver P. Metabolic adaptations through the PGC-1 alpha and SIRT1 pathways. FEBS letters 2008, 582:46-53.
46. Nemoto S., Fergusson M.M., Finkel T. Nutrient availability regulates SIRT1 through a forkhead-dependent pathway. Science 2004, 306:2105-2108.
47. Jing E., Gesta S., Kahn C.R. SIRT2 regulates adipocyte differentiation through FoxO1 acetylation/deacetylation. Cell Metab 2007, 6:105-114.
48. Blander G., Guarente L. The Sir2 family of protein deacetylases. Annu Rev Biochem 2004, 73:417-435.
49. Cheng H.L., Mostoslavsky R., Saito S., Manis J.P., Gu Y., Patel P., et al. Developmental defects and p53 hyperacetylation in Sir2 homolog (SIRT1)-deficient mice. Proc Natl Acad Sci U S A 2003, 100:10794-10799.
50. Lim J.H., Lee Y.M., Chun Y.S., Chen J., Kim J.E., Park J.W. Sirtuin 1 modulates cellular responses to hypoxia by deacetylating hypoxia-inducible factor 1alpha. Mol Cell 2010, 38:864-878.
51. Tokunaga C., Yoshino K., Yonezawa K. mTOR integrates amino acid- and energy-sensing pathways. Biochem Biophys Res Commun 2004, 313:443-446.
52. Yamanaka Y., Wilson E.M., Rosenfeld R.G., Oh Y. Inhibition of insulin receptor activation by insulin-like growth factor binding proteins. J Biol Chem 1997, 272:30729-30734.
53. Lui J.C., Andrade A.C., Forcinito P., Hegde A., Chen W., Baron J., et al. Spatial and temporal regulation of gene expression in the mammalian growth plate. Bone 2010, 46:1380-1390.
54. Maes M., Maiter D., Thissen J.P., Underwood L.E., Ketelslegers J.M. Contributions of growth hormone receptor and postreceptor defects to growth hormone resistance in malnutrition. Trends Endocrinol Metab 1991, 2:92-97.
55. Hernandez-Sanchez C., Werner H., Roberts C.T., Woo E.J., Hum D.W., Rosenthal S.M., et al. Differential regulation of insulin-like growth factor-I (IGF-I) receptor gene expression by IGF-I and basic fibroblastic growth factor. J Biol Chem 1997, 272:4663-4670.