Isoform-Specific SCFFbw7 ubiquitination mediates differential regulation of PGC-1α

Journal of Cellular Physiology

Volumn 230, Issue 4, 2015, Pages 842-852

  Trausch Azar, Julie S ^a   Abed, Mona ^b   Orian, Amir ^b   Schwartz, Alan L ^a  

^a ST LOUIS CHILDREN S HOSPITAL   (United States)

^b TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

E3 UBIQUITIN LIGASE SCF FBW7ALPHA; E3 UBIQUITIN LIGASE SCF FBW7BETA; ISOENZYME; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEASOME; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; F BOX PROTEIN; FBXW7 PROTEIN, HUMAN; ISOPROTEIN; PPARGC1A PROTEIN, HUMAN; TRANSCRIPTION FACTOR; UBIQUITIN PROTEIN LIGASE;

ARTICLE; CATALYSIS; CELL LEVEL; CONJUGATION; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVITY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN STABILITY; UBIQUITINATION; CELL CULTURE; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY;

CELL CYCLE PROTEINS; CELLS, CULTURED; CYTOPLASM; F-BOX PROTEINS; HUMANS; PHOSPHORYLATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN ISOFORMS; TRANSCRIPTION FACTORS; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84919772749     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24812     Document Type: Article

References (42)

1. Anderson RM, Barger JL, Edwards MG, Braun KH, O'Connor CE, Prolla TA, Weindruch R. 2008. Dynamic regulation of PGC-1alpha localization and turnover implicates mitochondrial adaptation in calorie restriction and the stress response. Aging Cell 7:101-111.
2. Arany Z, Foo SY, Ma Y, Ruas JL, Bommi-Reddy A, Girnun G, Cooper M, Laznik D, Chinsomboon J, Rangwala SM, Baek KH, Rosenzweig A, Spiegelman BM. 2008. HIF-independent regulation of VEGF and angiogenesis by the transcriptional coactivator PGC-1 alpha. Nature 451:1008-1012.
3. Aviram S, Kornitzer D. 2010. The ubiquitin ligase Hul5 promotes proteasomal processivity. Mol Cell Biol 30:985-994.
4. Bhaskaran N, van Drogen F, Ng HF, Kumar R, Ekholm-Reed S, Peter M, Sangfelt O, Reed SI. 2013. Fbw7α and Fbw7γ collaborate to shuttle cyclin E1 into the nucleolus for multiubiquitylation. Mol Cell Biol 33:85-97.
5. Blondel M, Galan JM, Chi Y, Lafourcade C, Longaretti C, Deshaies RJ, Peter M. 2000. Nuclear-specific degradation of Far1 is controlled by the localization of the F-box protein Cdc4. EMBO J 19:6085-6097.
6. Boutet S C, Disatnik M H, Chan L S, Iori K, Rando T A. 2007. Regulation of Pax3 by proteasomal degradation of monoubiquitinated protein in skeletal muscle progenitors. Cell 130:349-362.
7. Dominy J E Jr, Lee Y, Gerhart-Hines Z, Puigserver P. 2010. Nutrient-dependent regulation of PGC-1alpha's acetylation state and metabolic function through the enzymatic activities of Sirt1/GCN5. Biochim Biophys Acta 1804:1676-1683.
8. Finck BN, Kelly DP. 2006. PGC-1 coactivators: Inducible regulators of energy metabolism in health and disease. J Clin Invest 116:615-622.
9. Finley D. 2009. Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu Rev Biochem 78:477-513.
10. Finley D, Ulrich HD, Sommer T, Kaiser P. 2012. The ubiquitin-proteasome system of Saccharomyces cerevisiae. Genetics 192:319-360.
11. Grim JE, Gustafson MP, Hirata RK, Hagar AC, Swanger J, Welcker M, Ericsson J, Russell DW, Clurman BE. 2008. Isoform- and cell cycle-dependent substrate degradation by the Fbw7 ubiquitin ligase. J Cell Biol 181:913-920.
12. Handschin C, Spiegelman BM. 2006. Peroxisome proliferator-activated receptor gamma coactivator 1 coactivators, energy homeostasis, and metabolism. Endocr Rev 27:728-735.
13. Henchoz S, Chi Y, Catarin B, Herskowitz I, Deshaies RJ, Peter M. 1997. Phosphorylation- and ubiquitin-dependent degradation of the cyclin-dependent kinase inhibitor Far1p in budding yeast. Genes Dev 11:3046-3060.
14. Huss JM, Kopp RP, Kelly DP. 2002. Peroxisome proliferator-activated receptor coactivator-1alpha (PGC-1alpha) coactivates the cardiac-enriched nuclear receptors estrogen-related receptor-alpha and -gamma. Identification of novel leucine-rich interaction motif within PGC-1alpha. J Biol Chem 277:40265-40274.
15. Kelly DP, Scarpulla RC. 2004. Transcriptional regulatory circuits controlling mitochondrial biogenesis and function. Genes Dev 18:357-368.
16. Lin J, Handschin C, Spiegelman B M. 2005. Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab 1:361-370.
17. Lingbeck JM, Trausch-Azar JS, Ciechanover A, Schwartz AL. 2003. Determinants of nuclear and cytoplasmic ubiquitin-mediated degradation of MyoD. J Biol Chem 278:1817-1823.
18. Lingbeck JM, Trausch-Azar JS, Ciechanover A, Schwartz AL. 2005. E12 and E47 modulate cellular localization and proteasome-mediated degradation of MyoD and Id1. Oncogene 24:6376-6384.
19. Min S H, Lau A W, Lee T H, Inuzuka H, Wei S, Huang P, Shaik S, Lee D Y, Finn G, Balastik M, Chen C H, Luo M, Tron A E, Decaprio J A, Zhou X Z, Wei W, Lu K P. 2012. Negative regulation of the stability and tumor suppressor function of Fbw7 by the Pin1 prolyl isomerase. Mol Cell 46:771-783.
20. Moberg KH, Mukherjee A, Veraksa A, Artavanis-Tsakonas S, Hariharan IK. 2004. The Drosophila F box protein archipelago regulates dMyc protein levels in vivo. Curr Biol 14:965-974.
21. Olson BL, Hock MB, Ekholm-Reed S, Wohlschlegel JA, Dev KK, Kralli A, Reed SI. 2008. SCFCdc4 acts antagonistically to the PGC-1alpha transcriptional coactivator by targeting it for ubiquitin-mediated proteolysis. Genes Dev 22:252-264.
22. Puigserver P, Rhee J, Lin J Z, Yoon J C, Zhang C Y, Krauss S, Mootha V K, Lowell B B, Spiegelman B M. 2001. Cytokine stimulation of energy expenditure through p38 MAP kinase activation of PPARgamma coactivator-1. Mol Cell 8:971-982.
23. Puigserver P, Spiegelman BM. 2003. Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1 alpha): Transcriptional coactivator and metabolic regulator. Endocr Rev 24:78-90.
24. Puigserver P, Wu Z, Park C W, Graves R, Wright M, Spiegelman B M. 1998. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92:829-839.
25. Putters J, Slotman JA, Gerlach JP, Strous GJ. 2011. Specificity, location and function of βTrCP isoforms and their splice variants. Cell Signal 23:641-647.
26. Rajagopalan H, Jallepalli PV, Rago C, Velculescu VE, Kinzler KW, Vogelstein B, Lengauer C. 2004. Inactivation of hCDC4 can cause chromosomal instability. Nature 428:77-81.
27. Sancho R, Blake SM, Tendeng C, Clurman BE, Lewis J, Behrens A. 2013. Fbw7 Repression by hes5 creates a feedback loop that modulates Notch-mediated intestinal and neural stem cell fate decisions. PLoS Biol 11:e1001586.
28. Sano M, Tokudome S, Shimizu N, Yoshikawa N, Ogawa C, Shirakawa K, Endo J, Katayama T, Yuasa S, Ieda M, Makino S, Hattori F, Tanaka H, Fukuda K. 2007. Intramolecular control of protein stability, subnuclear compartmentalization, and coactivator function of peroxisome proliferator-activated receptor gamma coactivator 1alpha. J Biol Chem 282:25970-25980.
29. Schwartz AL, Ciechanover A. 2009. Targeting proteins for destruction by the ubiquitin system: Implications for human pathobiology. Annu Rev Pharmacol Toxicol 48:73-96.
30. Shabek N, Herman-Bachinsky Y, Buchsbaum S, Lewinson O, Haj-Yahya M, Hejjaoui M, Lashuel HA, Sommer T, Brik A, Ciechanover A. 2012. The size of the proteasomal substrate determines whether its degradation will be mediated by mono- or polyubiquitylation. Mol Cell 48:87-97.
31. Sionov RV, Netzer E, Shaulian E. 2013. Differential regulation of FBXW7 isoforms by various stress stimuli. Cell Cycle 12:3547-3554.
32. Sun L, Trausch-Azar JS, Ciechanover A, Schwartz AL. 2005. Ubiquitin-proteasome-mediated degradation, intracellular localization, and protein synthesis of MyoD and Id1 during muscle differentiation. J Biol Chem 280:26448-26456.
33. Sun L, Trausch-Azar JS, Muglia LJ, Schwartz AL. 2008. Glucocorticoids differentially regulate degradation of MyoD and Id1 by N-terminal ubiquitination to promote muscle protein catabolism. Proc Natl Acad Sci U S A 105:3339-3344.
34. Thrower JS, Hoffman L, Rechsteiner M, Pickart CM. 2000. Recognition of the polyubiquitin proteolytic signal. EMBO J 19:94-102.
35. Trausch-Azar J, Leone TC, Kelly DP, Schwartz AL. 2010. Ubiquitin proteasome-dependent degradation of the transcriptional coactivator PGC-1{alpha} via the N-terminal pathway. J Biol Chem 285:40192-40200.
36. Wei W, Jin J, Schlisio S, Harper JW, Kaelin WG, Jr. 2005. The v-Jun point mutation allows c-Jun to escape GSK3-dependent recognition and destruction by the Fbw7 ubiquitin ligase. Cancer Cell 8:25-33.
37. Welcker M, Clurman BE. 2008. FBW7 ubiquitin ligase: A tumour suppressor at the crossroads of cell division, growth and differentiation. Nat Rev Cancer 8:83-93.
38. Welcker M, Larimore EA, Swanger J, Bengoechea-Alonso MT, Grim JE, Ericsson J, Zheng N, Clurman BE. 2013. Fbw7 dimerization determines the specificity and robustness of substrate degradation. Genes Dev 27:2531-2536.
39. Welcker M, Orian A, Grim JE, Eisenman RN, Clurman BE. 2004. A nucleolar isoform of the Fbw7 ubiquitin ligase regulates c-Myc and cell size. Curr Biol 14:1852-1857.
40. Welcker M, Orian A, Jin J, Grim JE, Harper JW, Eisenman RN. 2004. The Fbw7 tumor suppressor regulates glycogen synthase kinase 3 phosphorylation-dependent c-Myc protein degradation. Proc Natl Acad Sci USA 101:9085-9090.
41. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, Troy A, Cinti S, Lowell B, Scarpulla R C, Spiegelman B M. 1999. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98:115-124.
42. Zhang Y, Huypens P, Adamson A W, Chang J S, Henagan T M, Boudreau A, Lenard N R, Burk D, Klein J, Perwitz N, Shin J, Fasshauer M, Kralli A, Gettys T W. 2009. Alternative mRNA splicing produces a novel biologically active short isoform of PGC-1 alpha. J Biol Chem 284:32813-32826.