S6K1 plays a critical role in early adipocyte differentiation

Developmental Cell

Volumn 18, Issue 5, 2010, Pages 763-774

  Carnevalli, Larissa S ^a   Masuda, Kouhei ^a   Frigerio, Francesca ^b   Le Bacquer, Olivier ^c   Um, Sung Hee ^a   Gandin, Valentina ^c   Topisirovic, Ivan ^c   Sonenberg, Nahum ^c   Thomas, George ^a   Kozma, Sara C ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

Devbio; Humdisease; Stemcell

Indexed keywords

PROTEIN SERINE THREONINE KINASE; S6 KINASE 1; UNCLASSIFIED DRUG;

ADIPOCYTE; ADIPOGENESIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL SIZE; CONTROLLED STUDY; EMBRYONIC STEM CELL; LIPID DIET; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; WILD TYPE;

ADIPOCYTES; ADIPOGENESIS; ADIPOSE TISSUE, WHITE; ANIMALS; CELL DIFFERENTIATION; HUMANS; HYPERPLASIA; MALE; MICE; MICE, KNOCKOUT; OBESITY; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; RIBOSOMAL PROTEIN S6 KINASES, 90-KDA; RNA, MESSENGER;

MUS;

EID: 77952893054     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devcel.2010.02.018     Document Type: Article

References (67)

1. Aguilar V., Alliouachene S., Sotiropoulos A., Sobering A., Athea Y., Djouadi F., Miraux S., Thiaudiere E., Foretz M., Viollet B., et al. S6 kinase deletion suppresses muscle growth adaptations to nutrient availability by activating AMP kinase. Cell Metab. 2007, 5:476-487.
2. Banko J.L., Poulin F., Hou L., DeMaria C.T., Sonenberg N., Klann E. The translation repressor 4E-BP2 is critical for eIF4F complex formation, synaptic plasticity, and memory in the hippocampus. J. Neurosci. 2005, 25:9581-9590.
3. Biondi R.M., Kieloch A., Currie R.A., Deak M., Alessi D.R. The PIF-binding pocket in PDK1 is essential for activation of S6K and SGK, but not PKB. EMBO J. 2001, 20:4380-4390.
4. Birsoy K., Chen Z., Friedman J. Transcriptional regulation of adipogenesis by KLF4. Cell Metab. 2008, 7:339-347.
5. Bone H.K., Welham M.J. Phosphoinositide 3-kinase signalling regulates early development and developmental haemopoiesis. J. Cell Sci. 2007, 120:1752-1762.
6. Bost F., Caron L., Marchetti I., Dani C., Le Marchand-Brustel Y., Binetruy B. Retinoic acid activation of the ERK pathway is required for embryonic stem cell commitment into the adipocyte lineage. Biochem. J. 2002, 361:621-627.
7. Calle E.E., Kaaks R. Overweight, obesity and cancer: epidemiological evidence and proposed mechanisms. Nat. Rev. Cancer 2004, 4:579-591.
8. Chang G.R., Chiu Y.S., Wu Y.Y., Chen W.Y., Liao J.W., Chao T.H., Mao F.C. Rapamycin protects against high fat diet-induced obesity in C57BL/6J mice. J. Pharmacol. Sci. 2009, 109:496-503.
9. Chen Z., Torrens J.I., Anand A., Spiegelman B.M., Friedman J.M. Krox20 stimulates adipogenesis via C/EBPbeta-dependent and -independent mechanisms. Cell Metab. 2005, 1:93-106.
10. da Silva Meirelles L., Caplan A.I., Nardi N.B. In search of the in vivo identity of mesenchymal stem cells. Stem Cells 2008, 26:2287-2299.
11. Dani C., Smith A.G., Dessolin S., Leroy P., Staccini L., Villageois P., Darimont C., Ailhaud G. Differentiation of embryonic stem cells into adipocytes in vitro. J. Cell Sci. 1997, 110:1279-1285.
12. Dann S.G., Selvaraj A., Thomas G. mTOR Complex1-S6K1 signaling: at the crossroads of obesity, diabetes and cancer. Trends Mol. Med. 2007, 13:252-259.
13. de Groot R.P., Ballou L.M., Sassone-Corsi P. Positive regulation of the cAMP-responsive activator CREM by the p70 S6 kinase: an alternative route to mitogen-induced gene expression. Cell 1994, 79:81-91.
14. El-Chaar D., Gagnon A., Sorisky A. Inhibition of insulin signaling and adipogenesis by rapamycin: effect on phosphorylation of p70 S6 kinase vs eIF4E-BP1. Int. J. Obes. Relat. Metab. Disord. 2004, 28:191-198.
15. Feldman M.E., Apsel B., Uotila A., Loewith R., Knight Z.A., Ruggero D., Shokat K.M. Active-site inhibitors of mTOR target rapamycin-resistant outputs of mTORC1 and mTORC2. PLoS Biol. 2009, 7:e38.
16. Gangloff Y.G., Mueller M., Dann S.G., Svoboda P., Sticker M., Spetz J.F., Um S.H., Brown E.J., Cereghini S., Thomas G., et al. Disruption of the mouse mTOR gene leads to early postimplantation lethality and prohibits embryonic stem cell development. Mol. Cell. Biol. 2004, 24:9508-9516.
17. Garmy-Susini B., Jin H., Zhu Y., Sung R.J., Hwang R., Varner J. Integrin alpha4beta1-VCAM-1-mediated adhesion between endothelial and mural cells is required for blood vessel maturation. J. Clin. Invest. 2005, 115:1542-1551.
18. Gesta S., Tseng Y.H., Kahn C.R. Developmental origin of fat: tracking obesity to its source. Cell 2007, 131:242-256.
19. Gulati P., Gaspers L.D., Dann S.G., Joaquin M., Nobukuni T., Natt F., Kozma S.C., Thomas A.P., Thomas G. Amino acids activate mTOR complex 1 via Ca2+/CaM signaling to hVps34. Cell Metab. 2008, 7:456-465.
20. Hannan K.M., Brandenburger Y., Jenkins A., Sharkey K., Cavanaugh A., Rothblum L., Moss T., Poortinga G., McArthur G.A., Pearson R.B., et al. mTOR-dependent regulation of ribosomal gene transcription requires S6K1 and is mediated by phosphorylation of the carboxy-terminal activation domain of the nucleolar transcription factor UBF. Mol. Cell. Biol. 2003, 23:8862-8877.
21. Hara K., Yonezawa K., Weng Q.P., Kozlowski M.T., Belham C., Avruch J. Amino acid sufficiency and mTOR regulate p70 S6 kinase and eIF-4E BP1 through a common effector mechanism. J. Biol. Chem. 1998, 273:14484-14494.
22. Hishida T., Nishizuka M., Osada S., Imagawa M. The role of C/EBPdelta in the early stages of adipogenesis. Biochimie 2009, 91:654-657.
23. Isakson P., Hammarstedt A., Gustafson B., Smith U. Impaired preadipocyte differentiation in human abdominal obesity: role of Wnt, tumor necrosis factor-alpha, and inflammation. Diabetes 2009, 58:1550-1557.
24. James W.P., Rigby N., Leach R. Obesity and the metabolic syndrome: the stress on society. Ann. NY Acad. Sci. 2006, 1083:1-10.
25. Jo J., Gavrilova O., Pack S., Jou W., Mullen S., Sumner A.E., Cushman S.W., Periwal V. Hypertrophy and/or hyperplasia: dynamics of adipose tissue growth. PLoS Comput. Biol. 2009, 5:e1000324.
26. Kim J.E., Chen J. Regulation of peroxisome proliferator-activated receptor-gamma activity by mammalian target of rapamycin and amino acids in adipogenesis. Diabetes 2004, 53:2748-2756.
27. Kissebah A.H., Krakower G.R. Regional adiposity and morbidity. Physiol. Rev. 1994, 74:761-811.
28. Koh Y.K., Lee M.Y., Kim J.W., Kim M., Moon J.S., Lee Y.J., Ahn Y.H., Kim K.S. Lipin1 is a key factor for the maturation and maintenance of adipocytes in the regulatory network with CCAAT/enhancer-binding protein alpha and peroxisome proliferator-activated receptor gamma 2. J. Biol. Chem. 2008, 283:34896-34906.
29. Le Bacquer O., Petroulakis E., Paglialunga S., Poulin F., Richard D., Cianflone K., Sonenberg N. Elevated sensitivity to diet-induced obesity and insulin resistance in mice lacking 4E-BP1 and 4E-BP2. J. Clin. Invest. 2007, 117:387-396.
30. Ma X.M., Yoon S.O., Richardson C.J., Julich K., Blenis J. SKAR links pre-mRNA splicing to mTOR/S6K1-mediated enhanced translation efficiency of spliced mRNAs. Cell 2008, 133:303-313.
31. Montagne J., Thomas G. S6K integrates nutrient and mitogenic signals to control cell growth. In Cell Growth: Control of Cell Size. Cold Spring Harbor Monograph Series #42 2004, 265-298. Cold Spring Laboratory Press, Cold Spring Harbor, NY. M. Hall, M. Raff, G. Thomas (Eds.).
32. Monteiro M.C., Wdziekonski B., Villageois P., Vernochet C., Iehle C., Billon N., Dani C. Commitment of mouse embryonic stem cells to the adipocyte lineage requires retinoic acid receptor beta and active GSK3. Stem Cells Dev. 2009, 18:457-463.
33. Morgan K.P., Kapur A., Beatt K.J. Anatomy of coronary disease in diabetic patients: an explanation for poorer outcomes after percutaneous coronary intervention and potential target for intervention. Heart 2004, 90:732-738.
34. Murakami M., Ichisaka T., Maeda M., Oshiro N., Hara K., Edenhofer F., Kiyama H., Yonezawa K., Yamanaka S. mTOR is essential for growth and proliferation in early mouse embryos and embryonic stem cells. Mol. Cell. Biol. 2004, 24:6710-6718.
35. Murry C.E., Keller G. Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell 2008, 132:661-680.
36. Noel D., Caton D., Roche S., Bony C., Lehmann S., Casteilla L., Jorgensen C., Cousin B. Cell specific differences between human adipose-derived and mesenchymal-stromal cells despite similar differentiation potentials. Exp. Cell Res. 2008, 314:1575-1584.
37. Nueda M.L., Garcia-Ramirez J.J., Laborda J., Baladron V. dlk1 specifically interacts with insulin-like growth factor binding protein 1 to modulate adipogenesis of 3T3-L1 cells. J. Mol. Biol. 2008, 379:428-442.
38. Oishi Y., Manabe I., Tobe K., Tsushima K., Shindo T., Fujiu K., Nishimura G., Maemura K., Yamauchi T., Kubota N., et al. Kruppel-like transcription factor KLF5 is a key regulator of adipocyte differentiation. Cell Metab. 2005, 1:27-39.
39. Panasyuk G., Nemazanyy I., Zhyvoloup A., Bretner M., Litchfield D.W., Filonenko V., Gout I.T. Nuclear export of S6K1 II is regulated by protein kinase CK2 phosphorylation at Ser-17. J. Biol. Chem. 2006, 281:31188-31201.
40. Phillips B.W., Vernochet C., Dani C. Differentiation of embryonic stem cells for pharmacological studies on adipose cells. Pharmacol. Res. 2003, 47:263-268.
41. Picard F., Gehin M., Annicotte J., Rocchi S., Champy M.F., O'Malley B.W., Chambon P., Auwerx J. SRC-1 and TIF2 control energy balance between white and brown adipose tissues. Cell 2002, 111:931-941.
42. Polak P., Cybulski N., Feige J.N., Auwerx J., Ruegg M.A., Hall M.N. Adipose-specific knockout of raptor results in lean mice with enhanced mitochondrial respiration. Cell Metab. 2008, 8:399-410.
43. Prunet-Marcassus B., Cousin B., Caton D., Andre M., Penicaud L., Casteilla L. From heterogeneity to plasticity in adipose tissues: site-specific differences. Exp. Cell Res. 2006, 312:727-736.
44. Pullen N., Dennis P.B., Andjelkovic M., Dufner A., Kozma S.C., Hemmings B.A., Thomas G. Phosphorylation and activation of p70s6k by PDK1. Science 1998, 279:707-710.
45. Riley J.K., Carayannopoulos M.O., Wyman A.H., Chi M., Moley K.H. Phosphatidylinositol 3-kinase activity is critical for glucose metabolism and embryo survival in murine blastocysts. J. Biol. Chem. 2006, 281:6010-6019.
46. Rodeheffer M.S., Birsoy K., Friedman J.M. Identification of white adipocyte progenitor cells in vivo. Cell 2008, 135:240-249.
47. Rosen E.D., MacDougald O.A. Adipocyte differentiation from the inside out. Nat. Rev. Mol. Cell Biol. 2006, 7:885-896.
48. Rosen E.D., Hsu C.H., Wang X., Sakai S., Freeman M.W., Gonzalez F.J., Spiegelman B.M. C/EBPalpha induces adipogenesis through PPARgamma: a unified pathway. Genes Dev. 2002, 16:22-26.
49. Sampath P., Pritchard D.K., Pabon L., Reinecke H., Schwartz S.M., Morris D.R., Murry C.E. A hierarchical network controls protein translation during murine embryonic stem cell self-renewal and differentiation. Cell Stem Cell 2008, 2:448-460.
50. Schalm S.S., Blenis J. Identification of a conserved motif required for mTOR signaling. Curr. Biol. 2002, 12:632-639.
51. Schwartz M.W., Woods S.C., Seeley R.J., Barsh G.S., Baskin D.G., Leibel R.L. Is the energy homeostasis system inherently biased toward weight gain?. Diabetes 2003, 52:232-238.
52. Selman C., Tullet J.M., Wieser D., Irvine E., Lingard S.J., Choudhury A.I., Claret M., Al-Qassab H., Carmignac D., Ramadani F., et al. Ribosomal protein S6 kinase 1 signaling regulates mammalian life span. Science 2009, 326:140-144.
53. s6k gene reveals a small mouse phenotype and a new functional S6 kinase. EMBO J. 1998, 17:6649-6659.
54. Singha U.K., Jiang Y., Yu S., Luo M., Lu Y., Zhang J., Xiao G. Rapamycin inhibits osteoblast proliferation and differentiation in MC3T3-E1 cells and primary mouse bone marrow stromal cells. J. Cell. Biochem. 2008, 103:434-446.
55. Spalding K.L., Arner E., Westermark P.O., Bernard S., Buchholz B.A., Bergmann O., Blomqvist L., Hoffstedt J., Naslund E., Britton T., et al. Dynamics of fat cell turnover in humans. Nature 2008, 453:783-787.
56. Takahashi K., Murakami M., Yamanaka S. Role of the phosphoinositide 3-kinase pathway in mouse embryonic stem (ES) cells. Biochem. Soc. Trans. 2005, 33:1522-1525.
57. Tang W., Zeve D., Suh J.M., Bosnakovski D., Kyba M., Hammer R.E., Tallquist M.D., Graff J.M. White fat progenitor cells reside in the adipose vasculature. Science 2008, 322:583-586.
58. Tsukiyama-Kohara K., Kohara P.F., De M., Maria C.T., Cheng A., Wu Z., Gingras A.C., Katsume A., Elchebly M., Spiegelman B.M., et al. Adipose tissue reduction in mice lacking the translational inhibitor 4E-BP1. Nat. Med. 2001, 7:1128-1132.
59. Um S.H., Frigerio F., Watanabe M., Picard F., Joaquin M., Sticker M., Fumagalli S., Allegrini P.R., Kozma S.C., Auwerx J., et al. Absence of S6K1 protects against age- and diet-induced obesity while enhancing insulin sensitivity. Nature 2004, 431:200-205.
60. Um S.H., D'Alessio D., Thomas G. Nutrient overload, insulin resistance, and ribosomal protein S6 kinase 1, S6K1. Cell Metab. 2006, 3:393-402.
61. von Manteuffel S.R., Dennis P.B., Pullen N., Gingras A.C., Sonenberg N., Thomas G. The insulin-induced signalling pathway leading to S6 and initiation factor 4E binding protein 1 phosphorylation bifurcates at a rapamycin-sensitive point immediately upstream of p70s6k. Mol. Cell. Biol. 1997, 17:5426-5436.
62. Wang W., Huang L., Huang Y., Yin J.W., Berk A.J., Friedman J.M., Wang G. Mediator MED23 links insulin signaling to the adipogenesis transcription cascade. Dev. Cell 2009, 16:764-771.
63. Xu Y., Shi Y., Ding S. A chemical approach to stem-cell biology and regenerative medicine. Nature 2008, 453:338-344.
64. Yamnik R.L., Digilova A., Davis D.C., Brodt Z.N., Murphy C.J., Holz M.K. S6 kinase 1 regulates estrogen receptor alpha in control of breast cancer cell proliferation. J. Biol. Chem. 2009, 284:6361-6369.
65. Yeh W.C., Bierer B.E., McKnight S.L. Rapamycin inhibits clonal expansion and adipogenic differentiation of 3T3-L1 cells. Proc. Natl. Acad. Sci. USA 1995, 92:11086-11090.
66. Zhang H.H., Huang J., Duvel K., Boback B., Wu S., Squillace R.M., Wu C.L., Manning B.D. Insulin stimulates adipogenesis through the Akt-TSC2-mTORC1 pathway. PLoS ONE 2009, 4:e6189.
67. Zhou J., Su P., Wang L., Chen J., Zimmermann M., Genbacev O., Afonja O., Horne M.C., Tanaka T., Duan E., et al. mTOR supports long-term self-renewal and suppresses mesoderm and endoderm activities of human embryonic stem cells. Proc. Natl. Acad. Sci. USA 2009, 106:7840-7845.