12,029
Views
30
CrossRef citations to date
0
Altmetric
Research Paper

The GID ubiquitin ligase complex is a regulator of AMPK activity and organismal lifespan

, , , , ORCID Icon, , ORCID Icon, , & show all
Pages 1618-1634 | Received 20 Mar 2019, Accepted 07 Nov 2019, Published online: 03 Dec 2019

References

  • Hardie DG, Ross FA, Hawley SA. AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol. 2012;13(4):251–262. [Cited 2012 March 23]. PubMed PMID: 22436748.
  • Jansen M, Ten Klooster JP, Offerhaus GJ, et al. LKB1 and AMPK family signaling: the intimate link between cell polarity and energy metabolism. Physiol Rev. 2009;89(3):777–798. [Cited 2009 July 09]. PubMed PMID: 19584313.
  • Pickart CM, Eddins MJ. Ubiquitin: structures, functions, mechanisms. Biochim Biophys Acta. 2004;1695(1–3):55–72. [Cited 2004 December 02]. PubMed PMID: 15571809.
  • Sadowski M, Suryadinata R, Tan AR, et al. Protein monoubiquitination and polyubiquitination generate structural diversity to control distinct biological processes. IUBMB Life. 2012;64(2):136–142. [Cited 2011 December 02]. PubMed PMID: 22131221.
  • Hämmerle M, Bauer J, Rose M, et al. Proteins of newly isolated mutants and the amino-terminal proline are essential for ubiquitin-proteasome-catalyzed catabolite degradation of fructose-1,6-bisphosphatase of Saccharomyces cerevisiae. J Biol Chem. 1998;273(39):25000–25005. [Cited 1998 September 17]. PubMed PMID: 9737955.
  • Chen SJ, Wu X, Wadas B, et al. An N-end rule pathway that recognizes proline and destroys gluconeogenic enzymes. Science. 2017;355(6323):eaal3655. PubMed PMID: 28126757.
  • Francis O, Han F, Adams JC. Molecular phylogeny of a RING E3 ubiquitin ligase, conserved in eukaryotic cells and dominated by homologous components, the muskelin/RanBPM/CTLH complex. PLoS One. 2013;8(10):e75217. PubMed PMID: 24143168; PubMed Central PMCID: PMCPMC3797097.
  • Santt O, Pfirrmann T, Braun B, et al. The yeast GID complex, a novel ubiquitin ligase (E3) involved in the regulation of carbohydrate metabolism. Mol Biol Cell. 2008;19(8):3323–3333. [Cited 2008 May 30]. PubMed PMID: 18508925; PubMed Central PMCID: PMC2488282.
  • Liu H, Pfirrmann T. The Gid-complex: an emerging player in the ubiquitin ligase league. Biol Chem. 2019. [Cited 2019 March 21]. PubMed PMID: 30893051. DOI:10.1515/hsz-2019-0139
  • Texier Y, Toedt G, Gorza M, et al. Elution profile analysis of SDS-induced subcomplexes by quantitative mass spectrometry. Mol Cell Proteomics. 2014;13(5):1382–1391. PubMed PMID: 24563533; PubMed Central PMCID: PMC4014293.
  • Pfirrmann T, Villavicencio-Lorini P, Subudhi AK, et al. RMND5 from xenopus laevis is an E3 ubiquitin-ligase and functions in early embryonic forebrain development. PLoS One. 2015;10(3):e0120342. [Cited 2015 March 21]. PubMed PMID: 25793641; PubMed Central PMCID: PMC4368662.
  • Lampert F, Stafa D, Goga A, et al. The multi-subunit GID/CTLH E3 ubiquitin ligase promotes cell proliferation and targets the transcription factor Hbp1 for degradation. Elife. 2018;7. [Cited 2018 June 19]. PubMed PMID: 29911972; PubMed Central PMCID: PMCPMC6037477. DOI:10.7554/eLife.35528
  • Leal-Esteban LC, Rothe B, Fortier S, et al. Role of bicaudal C1 in renal gluconeogenesis and its novel interaction with the CTLH complex. PLoS Genet. 2018;14(7):e1007487. [Cited 2018 July 12]. PubMed PMID: 29995892; PubMed Central PMCID: PMCPMC6056059.
  • Snowdon C, Hlynialuk C, van der Merwe G. Components of the Vid30c are needed for the rapamycin-induced degradation of the high-affinity hexose transporter Hxt7p in saccharomyces cerevisiae. FEMS Yeast Res. 2008;8(2):204–216. [Cited 2007 November 08]. PubMed PMID: 17986252.
  • Klionsky DJ, Abdelmohsen K, Abe A, Abedin MJ, Abeliovich H, Acevedo Arozena A, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy. 2016;12(1):1–222. Epub 2016/01/23. doi:10.1080/15548627.2015.1100356. PubMed PMID: 26799652; PubMed Central PMCID: PMCPMC4835977
  • Betz C, Hall MN. Where is mTOR and what is it doing there? J Cell Biol. 2013;203(4):563–574. [Cited 2014 January 05]. PubMed PMID: 24385483; PubMed Central PMCID: PMCPMC3840941.
  • Hardie DG, Corton J, Ching YP, et al. Regulation of lipid metabolism by the AMP-activated protein kinase. Biochem Soc Trans. 1997;25(4):1229–1231. [Cited 1998 February 05]. PubMed PMID: 9449981.
  • Zhang CS, Hawley SA, Zong Y, et al. Fructose-1,6-bisphosphate and aldolase mediate glucose sensing by AMPK. Nature. 2017;548(7665):112–116. [Cited 2017 July 21]. PubMed PMID: 28723898; PubMed Central PMCID: PMCPMC5544942. DOI
  • Pampliega O, Cuervo AM, Autophagy and primary cilia: dual interplay. Curr Opin Cell Biol. 2016;39:1–7. [Cited 2016 January 31]. PubMed PMID: 26826446; PubMed Central PMCID: PMCPMC4733852.
  • Pampliega O, Orhon I, Patel B, et al. Functional interaction between autophagy and ciliogenesis. Nature. 2013;502(7470):194–200. [Cited 2013 October 04]. PubMed PMID: 24089209; PubMed Central PMCID: PMCPMC3896125. DOI
  • Tang Z, Lin MG, Stowe TR, et al. Autophagy promotes primary ciliogenesis by removing OFD1 from centriolar satellites. Nature. 2013;502(7470):254–257. [Cited 2013 October 04]. PubMed PMID: 24089205; PubMed Central PMCID: PMCPMC4075283.
  • Sherpa RT, Atkinson KF, Ferreira VP, et al. Rapamycin increases length and mechanosensory function of primary cilia in renal epithelial and vascular endothelial cells. Int Educ Res J. 2016;2(12):91–97. [Cited 2017 May 23]. PubMed PMID: 28529994; PubMed Central PMCID: PMCPMC5436805.
  • Thoreen CC, Kang SA, Chang JW, et al. An ATP-competitive mammalian target of rapamycin inhibitor reveals rapamycin-resistant functions of mTORC1. J Biol Chem. 2009;284(12):8023–8032. [Cited 2009 January 20]. PubMed PMID: 19150980; PubMed Central PMCID: PMCPMC2658096.
  • Corton JM, Gillespie JG, Hawley SA, et al. 5-aminoimidazole-4-carboxamide ribonucleoside. A specific method for activating AMP-activated protein kinase in intact cells? Eur J Biochem. 1995;229(2):558–565. [Cited 1995 April 15]. PubMed PMID: 7744080.
  • Gonzalez A, Hall MN. Nutrient sensing and TOR signaling in yeast and mammals. Embo J. 2017;36(4):397–408. [Cited 2017 January 18]. PubMed PMID: 28096180.
  • Uno M, Nishida E, Lifespan-regulating genes in C. elegans. NPJ Aging Mech Dis. 2016;2:16010. [Cited 2017 July 20]. PubMed PMID: 28721266; PubMed Central PMCID: PMCPMC5514992.
  • Lochhead PA, Salt IP, Walker KS, et al. 5-aminoimidazole-4-carboxamide riboside mimics the effects of insulin on the expression of the 2 key gluconeogenic genes PEPCK and glucose-6-phosphatase. Diabetes. 2000;49(6):896–903. [Cited 2000 June 24]. PubMed PMID: 10866040.
  • Menssen R, Schweiggert J, Schreiner J, et al. Exploring the topology of the gid complex, the E3 ubiquitin ligase involved in catabolite-induced degradation of gluconeogenic enzymes. J Biol Chem. 2012;287(30):25602–25614. [Cited 2012 May 31]. PubMed PMID: 22645139; PubMed Central PMCID: PMC3408164.
  • Deng M, Yang X, Qin B, et al. Deubiquitination and Activation of AMPK by USP10. Mol Cell. 2016;61(4):614–624. [Cited 2016 February 16]. PubMed PMID: 26876938; PubMed Central PMCID: PMCPMC4836875.
  • Al-Hakim AK, Zagorska A, Chapman L, et al. Control of AMPK-related kinases by USP9X and atypical Lys(29)/Lys(33)-linked polyubiquitin chains. Biochem J. 2008;411(2):249–260. [Cited 2008 February 08]. PubMed PMID: 18254724.
  • Pineda CT, Ramanathan S, Fon Tacer K, et al. Degradation of AMPK by a cancer-specific ubiquitin ligase. Cell. 2015;160(4):715–728. [Cited 2015 February 14]. PubMed PMID: 25679763.
  • Coughlan KA, Balon TW, Valentine RJ, et al. Nutrient excess and AMPK downregulation in incubated skeletal muscle and muscle of glucose infused rats. PLoS One. 2015;10(5):e0127388. [Cited 2015 May 23]. PubMed PMID: 25996822; PubMed Central PMCID: PMCPMC4440828.
  • Yu L, McPhee CK, Zheng L, et al. Termination of autophagy and reformation of lysosomes regulated by mTOR. Nature. 2010;465(7300):942–946. [Cited 2010 June 08]. PubMed PMID: 20526321; PubMed Central PMCID: PMCPMC2920749.
  • Mihaylova MM, Shaw RJ. The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nat Cell Biol. 2011;13(9):1016–1023. [Cited 2011 September 06]. PubMed PMID: 21892142; PubMed Central PMCID: PMCPMC3249400.
  • Greer EL, Dowlatshahi D, Banko MR, et al. An AMPK-FOXO pathway mediates longevity induced by a novel method of dietary restriction in C. elegans. Curr Biol. 2007;17(19):1646–1656. [Cited 2007 September 29]. PubMed PMID: 17900900; PubMed Central PMCID: PMCPMC2185793.
  • Ehninger D, Neff F, Xie K. Longevity, aging and rapamycin. Cell Mol Life Sci. 2014;71(22):4325–4346. [Cited 2014 July 13]. PubMed PMID: 25015322; PubMed Central PMCID: PMCPMC4207939.
  • Bitto A, Ito TK, Pineda VV, et al. Transient rapamycin treatment can increase lifespan and healthspan in middle-aged mice. Elife. 2016;5. [Cited 2016 August 24]. PubMed PMID: 27549339; PubMed Central PMCID: PMCPMC4996648. DOI:10.7554/eLife.16351
  • Huang X, Dixit VM. Drugging the undruggables: exploring the ubiquitin system for drug development. Cell Res. 2016;26(4):484–498. [Cited 2016 March 24]. PubMed PMID: 27002218; PubMed Central PMCID: PMCPMC4822129.
  • Fantus D, Rogers NM, Grahammer F, et al., Roles of mTOR complexes in the kidney: implications for renal disease and transplantation. Nat Rev Nephrol. 2016;12(10):587–609. [Cited 2016 August 02]. PubMed PMID: 27477490.
  • Coughlan KA, Valentine RJ, Ruderman NB, et al., AMPK activation: a therapeutic target for type 2 diabetes? Diabetes Metab Syndr Obes. 2014;7:241–253. [Cited 2014 July 16]. PubMed PMID: 25018645; PubMed Central PMCID: PMCPMC4075959.
  • Zhou G, Myers R, Li Y, et al. Role of AMP-activated protein kinase in mechanism of metformin action. J Clin Invest. 2001;108(8):1167–1174. [Cited 2001 October 17]. PubMed PMID: 11602624; PubMed Central PMCID: PMCPMC209533.
  • Johnson SC, Rabinovitch PS, Kaeberlein M. mTOR is a key modulator of ageing and age-related disease. Nature. 2013;493(7432):338–345. [Cited 2013 January 18]. PubMed PMID: 23325216; PubMed Central PMCID: PMCPMC3687363.
  • Fraser AG, Kamath RS, Zipperlen P, et al. Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature. 2000;408(6810):325–330. [Cited 2000 December 01]. PubMed PMID: 11099033.
  • Rual JF, Ceron J, Koreth J, et al. Toward improving caenorhabditis elegans phenome mapping with an ORFeome-based RNAi library. Genome Res. 2004;14(10B):2162–2168. [Cited 2004 October 19]. PubMed PMID: 15489339; PubMed Central PMCID: PMCPMC528933.
  • Pfirrmann T, Lokapally A, Andreasson C, et al. SOMA: a single oligonucleotide mutagenesis and cloning approach. PLoS One. 2013;8(6):e64870. PubMed PMID: 23750217; PubMed Central PMCID: PMC3672168.
  • Brenner S. The genetics of caenorhabditis elegans. Genetics. 1974;77(1):71–94. [Cited 1974 May 01]. PubMed PMID: 4366476; PubMed Central PMCID: PMCPMC1213120.
  • Urban N, Tsitsipatis D, Hausig F, et al. Non-linear impact of glutathione depletion on C. elegans life span and stress resistance. Redox Biol. 2017;11:502–515. [Cited 2017 January 14]. PubMed PMID: 28086197; PubMed Central PMCID: PMCPMC5228094.
  • Cox J, Neuhauser N, Michalski A, et al. Andromeda: a peptide search engine integrated into the MaxQuant environment. J Proteome Res. 2011;10(4):1794–1805. [Cited 2011 January 25]. PubMed PMID: 21254760.
  • Cox J, Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol. 2008;26(12):1367–1372. [Cited 2008 November 26]. PubMed PMID: 19029910.
  • Elias JE, Gygi SP. Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat Methods. 2007;4(3):207–214. [Cited 2007 March 01]. PubMed PMID: 17327847.
  • Mackmull MT, Klaus B, Heinze I, et al. Landscape of nuclear transport receptor cargo specificity. Mol Syst Biol. 2017;13(12):962. [Cited 2017 December 20]. PubMed PMID: 29254951; PubMed Central PMCID: PMCPMC5740495.
  • Gatto L, Lilley KS. MSnbase-an R/Bioconductor package for isobaric tagged mass spectrometry data visualization, processing and quantitation. Bioinformatics. 2012;28(2):288–289. [Cited 2011 November 25]. PubMed PMID: 22113085.
  • Ritchie ME, Phipson B, Wu D, et al. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 2015;43(7):e47. [Cited 2015 January 22]. PubMed PMID: 25605792; PubMed Central PMCID: PMCPMC4402510. DOI
  • Perez-Riverol Y, Csordas A, Bai J, et al. The PRIDE database and related tools and resources in 2019: improving support for quantification data. Nucleic Acids Res. 2019;47(D1):D442–D50. [Cited 2018 November 06]. PubMed PMID: 30395289; PubMed Central PMCID: PMCPMC6323896.