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Article

The Ubiquitin Ligase CHIP Prevents SirT6 Degradation through Noncanonical Ubiquitination

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Pages 4461-4472 | Received 22 Apr 2013, Accepted 05 Sep 2013, Published online: 20 Mar 2023

REFERENCES

  • Fontana L, Partridge L, Longo VD. 2010. Extending healthy life span—from yeast to humans. Science 328:321–326.
  • Johnson FB, Sinclair DA, Guarente L. 1999. Molecular biology of aging. Cell 96:291–302.
  • Kenyon CJ. 2010. The genetics of ageing. Nature 464:504–512.
  • McDonough H, Patterson C. 2003. CHIP: a link between the chaperone and proteasome systems. Cell Stress Chaperones 8:303–308.
  • Min JN, Whaley RA, Sharpless NE, Lockyer P, Portbury AL, Patterson C. 2008. CHIP deficiency decreases longevity, with accelerated aging phenotypes accompanied by altered protein quality control. Mol. Cell. Biol. 28:4018–4025.
  • Morimoto RI. 2008. Proteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging. Genes Dev. 22:1427–1438.
  • Dai Q, Zhang C, Wu Y, McDonough H, Whaley RA, Godfrey V, Li HH, Madamanchi N, Xu W, Neckers L, Cyr D, Patterson C. 2003. CHIP activates HSF1 and confers protection against apoptosis and cellular stress. EMBO J. 22:5446–5458.
  • Jiang J, Ballinger CA, Wu Y, Dai Q, Cyr DM, Hohfeld J, Patterson C. 2001. CHIP is a U-box-dependent E3 ubiquitin ligase: identification of Hsc70 as a target for ubiquitylation. J. Biol. Chem. 276:42938–42944.
  • Qian SB, McDonough H, Boellmann F, Cyr DM, Patterson C. 2006. CHIP-mediated stress recovery by sequential ubiquitination of substrates and Hsp70. Nature 440:551–555.
  • Meacham GC, Patterson C, Zhang W, Younger JM, Cyr DM. 2001. The Hsc70 co-chaperone CHIP targets immature CFTR for proteasomal degradation. Nat. Cell Biol. 3:100–105.
  • Xu W, Marcu M, Yuan X, Mimnaugh E, Patterson C, Neckers L. 2002. Chaperone-dependent E3 ubiquitin ligase CHIP mediates a degradative pathway for c-ErbB2/Neu. Proc. Natl. Acad. Sci. U. S. A. 99:12847–12852.
  • Li L, Xin H, Xu X, Huang M, Zhang X, Chen Y, Zhang S, Fu XY, Chang Z. 2004. CHIP mediates degradation of Smad proteins and potentially regulates Smad-induced transcription. Mol. Cell. Biol. 24:856–864.
  • Shin Y, Klucken J, Patterson C, Hyman BT, McLean PJ. 2005. The co-chaperone carboxyl terminus of Hsp70-interacting protein (CHIP) mediates alpha-synuclein degradation decisions between proteasomal and lysosomal pathways. J. Biol. Chem. 280:23727–23734.
  • Dickey CA, Kamal A, Lundgren K, Klosak N, Bailey RM, Dunmore J, Ash P, Shoraka S, Zlatkovic J, Eckman CB, Patterson C, Dickson DW, Nahman NSJr, Hutton M, Burrows F, Petrucelli L. 2007. The high-affinity HSP90-CHIP complex recognizes and selectively degrades phosphorylated tau client proteins. J. Clin. Invest. 117:648–658.
  • Kim HT, Kim KP, Lledias F, Kisselev AF, Scaglione KM, Skowyra D, Gygi SP, Goldberg AL. 2007. Certain pairs of ubiquitin-conjugating enzymes (E2s) and ubiquitin-protein ligases (E3s) synthesize nondegradable forked ubiquitin chains containing all possible isopeptide linkages. J. Biol. Chem. 282:17375–17386.
  • Komander D, Rape M. 2012. The ubiquitin code. Annu. Rev. Biochem. 81:203–229.
  • McDonough H, Charles PC, Hilliard EG, Qian SB, Min JN, Portbury A, Cyr DM, Patterson C. 2009. Stress-dependent Daxx-CHIP interaction suppresses the p53 apoptotic program. J. Biol. Chem. 284:20649–20659.
  • North BJ, Marshall BL, Borra MT, Denu JM, Verdin E. 2003. The human Sir2 ortholog, SIRT2, is an NAD+-dependent tubulin deacetylase. Mol. Cell 11:437–444.
  • Hallows WC, Lee S, Denu JM. 2006. Sirtuins deacetylate and activate mammalian acetyl-CoA synthetases. Proc. Natl. Acad. Sci. U. S. A. 103:10230–10235.
  • Dai Q, Qian SB, Li HH, McDonough H, Borchers C, Huang D, Takayama S, Younger JM, Ren HY, Cyr DM, Patterson C. 2005. Regulation of the cytoplasmic quality control protein degradation pathway by BAG2. J. Biol. Chem. 280:38673–38681.
  • Zhou P. 2004. Determining protein half-lives. Methods Mol. Biol. 284:67–77.
  • Homma S, Jin X, Wang G, Tu N, Min J, Yanasak N, Mivechi NF. 2007. Demyelination, astrogliosis, and accumulation of ubiquitinated proteins, hallmarks of CNS disease in hsf1-deficient mice. J. Neurosci. 27:7974–7986.
  • Xiao X, Zuo X, Davis AA, McMillan DR, Curry BB, Richardson JA, Benjamin IJ. 1999. HSF1 is required for extra-embryonic development, postnatal growth and protection during inflammatory responses in mice. EMBO J. 18:5943–5952.
  • Yan LJ, Christians ES, Liu L, Xiao X, Sohal RS, Benjamin IJ. 2002. Mouse heat shock transcription factor 1 deficiency alters cardiac redox homeostasis and increases mitochondrial oxidative damage. EMBO J. 21:5164–5172.
  • Mostoslavsky R, Chua KF, Lombard DB, Pang WW, Fischer MR, Gellon L, Liu P, Mostoslavsky G, Franco S, Murphy MM, Mills KD, Patel P, Hsu JT, Hong AL, Ford E, Cheng HL, Kennedy C, Nunez N, Bronson R, Frendewey D, Auerbach W, Valenzuela D, Karow M, Hottiger MO, Hursting S, Barrett JC, Guarente L, Mulligan R, Demple B, Yancopoulos GD, Alt FW. 2006. Genomic instability and aging-like phenotype in the absence of mammalian SIRT6. Cell 124:315–329.
  • Sundaresan NR, Vasudevan P, Zhong L, Kim G, Samant S, Parekh V, Pillai VB, Ravindra PV, Gupta M, Jeevanandam V, Cunningham JM, Deng CX, Lombard DB, Mostoslavsky R, Gupta MP. 2012. The sirtuin SIRT6 blocks IGF-Akt signaling and development of cardiac hypertrophy by targeting c-Jun. Nat. Med. 18:1643–1650.
  • Xiao C, Kim HS, Lahusen T, Wang RH, Xu X, Gavrilova O, Jou W, Gius D, Deng CX. 2010. SIRT6 deficiency results in severe hypoglycemia by enhancing both basal and insulin-stimulated glucose uptake in mice. J. Biol. Chem. 285:36776–36784.
  • Haigis MC, Sinclair DA. 2010. Mammalian sirtuins: biological insights and disease relevance. Annu. Rev. Pathol. 5:253–295.
  • Tennen RI, Berber E, Chua KF. 2010. Functional dissection of SIRT6: identification of domains that regulate histone deacetylase activity and chromatin localization. Mech. Ageing Dev. 131:185–192.
  • Michishita E, McCord RA, Berber E, Kioi M, Padilla-Nash H, Damian M, Cheung P, Kusumoto R, Kawahara TL, Barrett JC, Chang HY, Bohr VA, Ried T, Gozani O, Chua KF. 2008. SIRT6 is a histone H3 lysine 9 deacetylase that modulates telomeric chromatin. Nature 452:492–496.
  • Kawahara TL, Michishita E, Adler AS, Damian M, Berber E, Lin M, McCord RA, Ongaigui KC, Boxer LD, Chang HY, Chua KF. 2009. SIRT6 links histone H3 lysine 9 deacetylation to NF-kappaB-dependent gene expression and organismal life span. Cell 136:62–74.
  • Zhong L, D'Urso A, Toiber D, Sebastian C, Henry RE, Vadysirisack DD, Guimaraes A, Marinelli B, Wikstrom JD, Nir T, Clish CB, Vaitheesvaran B, Iliopoulos O, Kurland I, Dor Y, Weissleder R, Shirihai OS, Ellisen LW, Espinosa JM, Mostoslavsky R. 2010. The histone deacetylase Sirt6 regulates glucose homeostasis via Hif1alpha. Cell 140:280–293.
  • Xiao C, Wang RH, Lahusen TJ, Park O, Bertola A, Maruyama T, Reynolds D, Chen Q, Xu X, Young HA, Chen WJ, Gao B, Deng CX. 2012. Progression of chronic liver inflammation and fibrosis driven by activation of c-JUN signaling in Sirt6 mutant mice. J. Biol. Chem. 287:41903–41913.
  • Kaidi A, Weinert BT, Choudhary C, Jackson SP. 2010. Human SIRT6 promotes DNA end resection through CtIP deacetylation. Science 329:1348–1353.
  • Mao Z, Hine C, Tian X, Van Meter M, Au M, Vaidya A, Seluanov A, Gorbunova V. 2011. SIRT6 promotes DNA repair under stress by activating PARP1. Science 332:1443–1446.
  • McCord RA, Michishita E, Hong T, Berber E, Boxer LD, Kusumoto R, Guan S, Shi X, Gozani O, Burlingame AL, Bohr VA, Chua KF. 2009. SIRT6 stabilizes DNA-dependent protein kinase at chromatin for DNA double-strand break repair. Aging 1:109–121.
  • Lombard DB, Chua KF, Mostoslavsky R, Franco S, Gostissa M, Alt FW. 2005. DNA repair, genome stability, and aging. Cell 120:497–512.
  • Adler AS, Sinha S, Kawahara TL, Zhang JY, Segal E, Chang HY. 2007. Motif module map reveals enforcement of aging by continual NF-kappaB activity. Genes Dev. 21:3244–3257.
  • Holt SJ, Riddle DL. 2003. SAGE surveys C. elegans carbohydrate metabolism: evidence for an anaerobic shift in the long-lived dauer larva. Mech. Ageing Dev. 124:779–800.
  • Alberti S, Demand J, Esser C, Emmerich N, Schild H, Hohfeld J. 2002. Ubiquitylation of BAG-1 suggests a novel regulatory mechanism during the sorting of chaperone substrates to the proteasome. J. Biol. Chem. 277:45920–45927.

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