Age-dependent FOXO regulation of p27Kip1 expression via a conserved binding motif in rat muscle precursor cells

American Journal of Physiology - Cell Physiology

Volumn 295, Issue 5, 2008, Pages

  Lees, Simon J ^a,d   Childs, Tom E ^a   Booth, Frank W ^a,b,c  

^a UNIVERSITY OF MISSOURI   (United States)

^b University of Missouri   (United States)

^c UNIVERSITY OF MISSOURI   (United States)

^d Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

5 untranslated region; Daf 16 family protein binding element; Forkhead box O; Proliferation; Satellite cell; Skeletal muscle

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1B; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR FKHRL1;

ANIMAL CELL; ARTICLE; CELL CYCLE ARREST; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DRUG PROTEIN BINDING; MALE; MUSCLE CELL; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RAT;

5' UNTRANSLATED REGIONS; AGE FACTORS; AGING; ANIMALS; BINDING SITES; CELL DIFFERENTIATION; CELLS, CULTURED; CONSERVED SEQUENCE; CREATINE KINASE, MM FORM; CYCLIN-DEPENDENT KINASE INHIBITOR P27; FORKHEAD TRANSCRIPTION FACTORS; GENES, REPORTER; MALE; MUTATION; MYOBLASTS, SKELETAL; NF-KAPPA B; PROMOTER REGIONS, GENETIC; RATS; RATS, INBRED BN; RATS, INBRED F344; TRANSCRIPTIONAL ACTIVATION; TRANSFECTION;

ANIMALIA; RATTUS;

EID: 57349141975     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00349.2008     Document Type: Article

References (40)

1. Adams GR, Caiozzo VJ, Haddad F, Baldwin KM. Cellular and molecular responses to increased skeletal muscle loading after irradiation. Am J Physiol Cell Physiol 283: C1182-C1195, 2002.
2. Allen RE, Temm-Grove CJ, Sheehan SM, Rice G. Skeletal muscle satellite cell cultures. Methods Cell Biol 52: 155-176, 1997.
3. Alway SE, Degens H, Krishnamurthy G, Smith CA. Potential role for Id myogenic repressors in apoptosis and attenuation of hypertrophy in muscles of aged rats. Am J Physiol Cell Physiol 283: C66-C76, 2002.
4. Barani AE, Durieux AC, Sabido O, Freyssenet D. Age-related changes in the mitotic and metabolic characteristics of muscle-derived cells. J Appl Physiol 95: 2089-2098, 2003.
5. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, Poueymirou WT, Panaro FJ, Na E, Dharmarajan K, Pan ZQ, Valenzuela DM, DeChiara TM, Stitt TN, Yancopoulos GD, Glass DJ. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294: 1704-1708, 2001.
6. Brooks SV, Faulkner JA. Contraction-induced injury: recovery of skeletal muscles in young and old mice. Am J Physiol Cell Physiol 258: C436-C442, 1990.
7. Brownawell AM, Kops GJ, Macara IG, Burgering BM. Inhibition of nuclear import by protein kinase B (Akt) regulates the subcellular distribution and activity of the forkhead transcription factor AFX. Mol Cell Biol 21: 3534-3546, 2001.
8. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96: 857-868, 1999.
9. Burgering BM. A brief introduction to FOXOlogy. Oncogene 27: 2258-2262, 2008.
10. Carlson ME, Hsu M, Conboy IM. Imbalance between pSmad3 and Notch induces CDK inhibitors in old muscle stem cells. Nature 454: 528-532, 2008.
11. Chakravarthy MV, Davis BS, Booth FW. IGF-I restores satellite cell proliferative potential in immobilized old skeletal muscle. J Appl Physiol 89: 1365-1379, 2000.
12. Conboy IM, Conboy MJ, Smythe GM, Rando TA. Notch-mediated restoration of regenerative potential to aged muscle. Science 302: 1575-1577, 2003.
13. Conboy IM, Conboy MJ, Wagers AJ, Girma ER, Weissman IL, Rando TA. Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 433: 760-764, 2005.
14. Dijkers PF, Medema RH, Pals C, Banerji L, Thomas NS, Lam EW, Burgering BM, Raaijmakers JA, Lammers JW, Koenderman L, Coffer PJ. Forkhead transcription factor FKHR-L1 modulates cytokine-dependent transcriptional regulation of p27(KIP1). Mol Cell Biol 20: 9138-9148, 2000.
15. Edstrom E, Altun M, Hagglund M, Ulfhake B. Atrogin-1/MAFbx and MuRF1 are downregulated in aging-related loss of skeletal muscle. J Gerontol A Biol Sci Med Sci 61: 663-674, 2006.
16. Furuyama T, Kitayama K, Yamashita H, Mori N. Forkhead transcription factor FOXO1 (FKHR)-dependent induction of PDK4 gene expression in skeletal muscle during energy deprivation. Biochem J 375: 365-371, 2003.
17. Furuyama T, Nakazawa T, Nakano I, Mori N. Identification of the differential distribution patterns of mRNAs and consensus binding sequences for mouse DAF-16 homologues. Biochem J 349: 629-634, 2000.
18. Greer EL, Brunet A. FOXO transcription factors at the interface between longevity and tumor suppression. Oncogene 24: 7410-7425, 2005.
19. Honda Y, Honda S. The daf-2 gene network for longevity regulates oxidative stress resistance and Mn-superoxide dismutase gene expression in Caenorhabditis elegans. FASEB J 13: 1385-1393, 1999.
20. Kim DH, Kim JY, Yu BP, Chung HY. The activation of NF-kappaB through Akt-induced FOXO1 phosphorylation during aging and its modulation by calorie restriction. Biogerontology 9: 33-47, 2008.
21. Kimball SR, O'Malley JP, Anthony JC, Crozier SJ, Jefferson LS. Assessment of biomarkers of protein anabolism in skeletal muscle during the life span of the rat: sarcopenia despite elevated protein synthesis. Am J Physiol Endocrinol Metab 287: E772-E780, 2004.
22. Klein D, Kern RM, Sokol RZ. A method for quantification and correction of proteins after transfer to immobilization membranes. Biochem Mol Biol Int 36: 59-66, 1995.
23. Kops GJ, de Ruiter ND, De Vries-Smits AM, Powell DR, Bos JL, Burgering BM. Direct control of the Forkhead transcription factor AFX by protein kinase B. Nature 398: 630-634, 1999.
24. Lees SJ, Childs TE, Booth FW. p21(Cip1) expression is increased in ambient oxygen, compared to estimated physiological (5%) levels in rat muscle precursor cell culture. Cell Prolif 41: 193-207, 2008.
25. Lees SJ, Rathbone CR, Booth FW. Age-associated decrease in muscle precursor cell differentiation. Am J Physiol Cell Physiol 290: C609-C615, 2006.
26. Lin L, Hron JD, Peng SL. Regulation of NF-kappaB, Th activation, and autoinflammation by the forkhead transcription factor Foxo3a. Immunity 21: 203-213, 2004.
27. Machida S, Booth FW. Increased nuclear proteins in muscle satellite cells in aged animals as compared to young growing animals. Exp Gerontol 39: 1521-1525, 2004.
28. Machida S, Spangenburg EE, Booth FW. Forkhead transcription factor FoxO1 transduces insulin-like growth factor's signal to p27Kip1 in primary skeletal muscle satellite cells. J Cell Physiol 196: 523-531, 2003.
29. Medema RH, Kops GJ, Bos JL, Burgering BM. AFX-like Forkhead transcription factors mediate cell-cycle regulation by Ras and PKB through p27kip1. Nature 404: 782-787, 2000.
30. Nakae J, Park BC, Accili D. Insulin stimulates phosphorylation of the forkhead transcription factor FKHR on serine 253 through a wortmannin-sensitive pathway. J Biol Chem 274: 15982-15985, 1999.
31. Rathbone CR, Booth FW, Lees SJ. FoxO3a preferentially induces p27Kip1 expression while impairing muscle precursor cell-cycle progression. Muscle Nerve 37: 84-89, 2008.
32. Raue U, Slivka D, Jemiolo B, Hollon C, Trappe S. Proteolytic gene expression differs at rest and after resistance exercise between young and old women. J Gerontol A Biol Sci Med Sci 62: 1407-1412, 2007.
33. Rena G, Guo S, Cichy SC, Unterman TG, Cohen P. Phosphorylation of the transcription factor forkhead family member FKHR by protein kinase B. J Biol Chem 274: 17179-17183, 1999.
34. Sandri M, Sandri C, Gilbert A, Skurk C, Calabria E, Picard A, Walsh K, Schiaffino S, Lecker SH, Goldberg AL. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117: 399-412, 2004.
35. Schultz E, McCormick KM. Skeletal muscle satellite cells. Rev Physiol Biochem Pharmacol 123: 213-257, 1994.
36. Tokuda Y, Crane S, Yamaguchi Y, Zhou L, Falanga V. The levels and kinetics of oxygen tension detectable at the surface of human dermal fibroblast cultures. J Cell Physiol 182: 414-420, 2000.
37. Van Der Heide LP, Hoekman MF, Smidt MP. The ins and outs of FoxO shuttling: mechanisms of FoxO translocation and transcriptional regulation. Biochem J 380: 297-309, 2004.
38. Yeh PY, Kuo SH, Yeh KH, Chuang SE, Hsu CH, Chang WC, Lin HI, Gao M, Cheng AL. A pathway for tumor necrosis factor-alpha-induced Bcl10 nuclear translocation. Bcl10 is up-regulated by NF-kappaB and phosphorylated by Akt1 and then complexes with Bcl3 to enter the nucleus. J Biol Chem 281: 167-175, 2006.
39. 2+ dependence, and differential half-site recognition. J Biol Chem 266: 252-260, 1991.
40. Zabludoff SD, Csete M, Wagner R, Yu X, Wold BJ. p27Kip1 is expressed transiently in developing myotomes and enhances myogenesis. Cell Growth Differ 9: 1-11, 1998.