2,463
Views
25
CrossRef citations to date
0
Altmetric
Research Paper

RNA-binding proteins regulate cell respiration and coenzyme Q biosynthesis by post-transcriptional regulation of COQ7

, , , , , ORCID Icon, , ORCID Icon, , , & show all
Pages 622-634 | Received 09 Sep 2015, Accepted 09 Nov 2015, Published online: 22 Jun 2016

References

  • Bentinger M, Tekle M, Dallner G. Coenzyme Q – Biosynthesis and functions. Biochem Biophys Res Commun 2010; 396:74-9; PMID:20494114; http://doi.dx.org/10.1016/j.bbrc.2010.02.147
  • Cramer WA, Hasan SS, Yamashita E. The Q cycle of cytochrome bc complexes: A structure perspective. Biochim Biophys Acta - Bioenerg 2011; 1807:788-802; http://doi.dx.org/10.1016/j.bbabio.2011.02.006
  • Padilla S, Jonassen T, Jimenez-Hidalgo MA, Fernandez-Ayala DJM, Lopez-Lluch G, Marbois B, Navas P, Clarke CF, Santos-Ocana C. Demethoxy-Q, an intermediate of coenzyme Q biosynthesis, fails to support respiration in saccharomyces cerevisiae and lacks antioxidant activity. J Biol Chem 2004; 279:25995-6004; PMID:15078893; http://doi.dx.org/10.1074/jbc.M400001200
  • Lapuente-Brun E, Moreno-Loshuertos R, Acin-Perez R, Latorre-Pellicer A, Colas C, Balsa E, Perales-Clemente E, Quiros PM, Calvo E, Rodriguez-Hernandez MA, et al. Supercomplex Assembly Determines Electron Flux in the Mitochondrial Electron Transport Chain. Science (80-) 2013; 340:1567-70; PMID:23812712; http://doi.dx.org/10.1126/science.1230381
  • Genova ML, Lenaz G. The Interplay Between Respiratory Supercomplexes and ROS in Aging. Antioxid Redox Signal 2015; 23:208-38; PMID:25711676; http://doi.dx.org/10.1089/ars.2014.6214
  • Doimo M, Desbats MA, Cerqua C, Cassina M, Trevisson E, Salviati L. Genetics of coenzyme q10 deficiency. Mol Syndromol 2014; 5:156-62; PMID:25126048; http://doi.dx.org/10.1159/000362826
  • Laredj LN, Licitra F, Puccio HM. The molecular genetics of coenzyme Q biosynthesis in health and disease. Biochimie 2014; 100:78-87; PMID:24355204; http://doi.dx.org/10.1016/j.biochi.2013.12.006
  • Desbats MA, Lunardi G, Doimo M, Trevisson E, Salviati L. Genetic bases and clinical manifestations of coenzyme Q10 (CoQ 10) deficiency. J Inherit Metab Dis 2014; 38:145-56; PMID:25091424; http://doi.dx.org/10.1007/s10545-014-9749-9
  • Desbats MA, Vetro A, Limongelli I, Lunardi G, Casarin A, Doimo M, Spinazzi M, Angelini C, Cenacchi G, Burlina A, et al. Primary coenzyme Q10 deficiency presenting as fatal neonatal multiorgan failure. Eur J Hum Genet 2015; 23:1254-8; PMID:25564041; http://doi.dx.org/10.1038/ejhg.2014.277
  • Cornelius N, Byron C, Hargreaves I, Guerra PF, Furdek AK, Land J, Radford WW, Frerman F, Corydon TJ, Gregersen N, et al. Secondary coenzyme Q10 deficiency and oxidative stress in cultured fibroblasts from patients with riboflavin responsive multiple Acyl-CoA dehydrogenation deficiency. Hum Mol Genet 2013; 22:3819-27; PMID:23727839; http://doi.dx.org/10.1093/hmg/ddt232
  • Asencio C, Rodríguez-Hernandez MA, Briones P, Montoya J, Cortés A, Emperador S, Gavilán A, Ruiz-Pesini E, Yubero D, Montero R, et al. Severe encephalopathy associated to pyruvate dehydrogenase mutations and unbalanced coenzyme Q10 content. Eur J Hum Genet 2015; PMID:26014431; http://doi.dx.org/10.1038/ejhg.2015.112.
  • Baur JA, Pearson KJ, Price NL, Jamieson HA, Lerin C, Kalra A, Prabhu V V, Allard JS, Lopez-Lluch G, Lewis K, et al. Resveratrol improves health and survival of mice on a high-calorie diet. Nature 2006; 444:337-42; PMID:17086191; http://doi.dx.org/10.1038/nature05354
  • L pez-Lluch G, Hunt N, Jones B, Zhu M, Jamieson H, Hilmer S, Cascajo M V, Allard J, Ingram DK, Navas P, et al. Calorie restriction induces mitochondrial biogenesis and bioenergetic efficiency. Proc Natl Acad Sci 2006; 103:1768-73; PMID:16446459; http://doi.dx.org/10.1073/pnas.0510452103
  • Asencio C, Rodriguez-Aguilera JC, Ruiz-Ferrer M, Vela J, Navas P. Silencing of ubiquinone biosynthesis genes extends life span in Caenorhabditis elegans. FASEB J 2003; 17:1135-7; PMID:12709403; http://doi.dx.org/10.1096/fj.02-1022fje
  • Wang Y, Oxer D, Hekimi S. Mitochondrial function and lifespan of mice with controlled ubiquinone biosynthesis. Nat Commun 2015; 6:6393; PMID:25744659; http://doi.dx.org/10.1038/ncomms7393
  • Turunen M, Peters JM, Gonzalez FJ, Schedin S, Dallner G. Influence of peroxisome proliferator-activated receptor α on ubiquinone biosynthesis. J Mol Biol 2000; 297:607-14; PMID:10731415; http://doi.dx.org/10.1006/jmbi.2000.3596
  • Bentinger M, Tekle M, Brismar K, Chojnacki T, Swiezewska E, Dallner G. Stimulation of coenzyme Q synthesis. BioFactors 2008; 32:99-111; PMID:19096105; http://doi.dx.org/10.1002/biof.5520320112
  • Brea-Calvo G, Siendones E, Sánchez-Alcázar JA, de Cabo R, Navas P. Cell survival from chemotherapy depends on NF-kappaB transcriptional up-regulation of coenzyme Q biosynthesis. PLoS One 2009; 4:e5301; PMID:19390650; http://doi.dx.org/10.1371/journal.pone.0005301
  • Martín-Montalvo A, González-Mariscal I, Padilla S, Ballesteros M, Brautigan DL, Navas P, Santos-Ocaña C. Respiratory-induced coenzyme Q biosynthesis is regulated by a phosphorylation cycle of Cat5p/Coq7p. Biochem J 2011; 440:107-14; PMID:21812761; http://doi.dx.org/10.1042/BJ20101422
  • Martin-Montalvo A, Gonzalez-Mariscal I, Pomares-Viciana T, Padilla-Lopez S, Ballesteros M, Vazquez-Fonseca L, Gandolfo P, Brautigan DL, Navas P, Santos-Ocana C. The Phosphatase Ptc7 Induces Coenzyme Q Biosynthesis by Activating the Hydroxylase Coq7 in Yeast. J Biol Chem 2013; 288:28126-37; PMID:23940037; http://doi.dx.org/10.1074/jbc.M113.474494
  • Lohman DC, Forouhar F, Beebe ET, Stefely MS, Minogue CE, Ulbrich A, Stefely JA, Sukumar S, Luna-Sánchez M, Jochem A, et al. Mitochondrial COQ9 is a lipid-binding protein that associates with COQ7 to enable coenzyme Q biosynthesis. Proc Natl Acad Sci U S A 2014; 111:E4697-705; PMID:25339443; http://doi.dx.org/10.1073/pnas.1413128111
  • Mata J, Marguerat S, Bähler J. Post-transcriptional control of gene expression: A genome-wide perspective. Trends Biochem Sci 2005; 30:506-14; PMID:16054366; http://doi.dx.org/10.1016/j.tibs.2005.07.005
  • Pascale A, Govoni S. The complex world of post-transcriptional mechanisms: is their deregulation a common link for diseases? Focus on ELAV-like RNA-binding proteins. Cell Mol life Sci C 2011; 69:501-17; PMID:21909784; http://doi.dx.org/10.1007/s00018-011-0810-7
  • López de Silanes I, Zhan M, Lal A, Yang X, Gorospe M. Identification of a target RNA motif for RNA-binding protein HuR. Proc Natl Acad Sci U S A 2004; 101:2987-92; PMID:14981256; http://doi.dx.org/10.1073/pnas.0306453101
  • Hinman MN, Lou H. Diverse molecular functions of Hu proteins. Cell Mol Life Sci 2008; 65:3168-81; PMID:18581050; http://doi.dx.org/10.1007/s00018-008-8252-6
  • Atasoy U, Watson J, Patel D, Keene JD. ELAV protein HuA (HuR) can redistribute between nucleus and cytoplasm and is upregulated during serum stimulation and T cell activation. J Cell Sci 1998; 111 ( Pt 2:3145-56; PMID:9763509.
  • Figueroa A, Cuadrado A, Fan J, Atasoy U, Muscat GE, Munoz-Canoves P, Gorospe M, Munoz A. Role of HuR in Skeletal Myogenesis through Coordinate Regulation of Muscle Differentiation Genes. Mol Cell Biol 2003; 23:4991-5004; PMID:12832484; http://doi.dx.org/10.1128/MCB.23.14.4991-5004.2003
  • Kullmann M. ELAV/Hu proteins inhibit p27 translation via an IRES element in the p27 5′UTR. Genes Dev 2002; 16:3087-99; PMID:12464637; http://doi.dx.org/10.1101/gad.248902
  • Wang W, Caldwell MC, Lin S, Furneaux H, Gorospe M. HuR regulates cyclin A and cyclin B1 mRNA stability during cell proliferation. EMBO J 2000; 19:2340-50; PMID:10811625; http://doi.dx.org/10.1093/emboj/19.10.2340
  • Chang N, Yi J, Guo G, Liu X, Shang Y, Tong T, Cui Q, Zhan M, Gorospe M, Wang W. HuR uses AUF1 as a cofactor to promote p16INK4 mRNA decay. Mol Cell Biol 2010; 30:3875-86; PMID:20498276; http://doi.dx.org/10.1128/MCB.00169-10
  • Lal A, Mazan-Mamczarz K, Kawai T, Yang X, Martindale JL, Gorospe M. Concurrent versus individual binding of HuR and AUF1 to common labile target mRNAs. EMBO J 2004; 23:3092-102; PMID:15257295; http://doi.dx.org/10.1038/sj.emboj.7600305
  • Pan Y-X, Chen H, Kilberg MS. Interaction of RNA-binding Proteins HuR and AUF1 with the Human ATF3 mRNA 3′-Untranslated Region Regulates Its Amino Acid Limitation-induced Stabilization. J Biol Chem 2005; 280:34609-16; PMID:16109718; http://doi.dx.org/10.1074/jbc.M507802200
  • Zou T, Rao JN, Liu L, Xiao L, Yu T-X, Jiang P, Gorospe M, Wang J-Y. Polyamines Regulate the Stability of JunD mRNA by Modulating the Competitive Binding of Its 3′ Untranslated Region to HuR and AUF1. Mol Cell Biol 2010; 30:5021-32; PMID:20805360; http://doi.dx.org/10.1128/MCB.00807-10
  • Herzig RP. Sequential Serum-dependent Activation of CREB and NRF-1 Leads to Enhanced Mitochondrial Respiration through the Induction of Cytochrome c. J Biol Chem 2000; 275:13134-41; PMID:10777619; http://doi.dx.org/10.1074/jbc.275.17.13134
  • Golpour M, Akhavan Niaki H, Khorasani HR, Hajian A, Mehrasa R, Mostafazadeh A. Human fibroblast switches to anaerobic metabolic pathway in response to serum starvation: a mimic of warburg effect. Int J Mol Cell Med 2014; 3:74-80; PMID:25035856.
  • López-Martín JM, Salviati L, Trevisson E, Montini G, DiMauro S, Quinzii C, Hirano M, Rodriguez-Hernandez A, Cordero MD, Sánchez-Alcázar JA, et al. Missense mutation of the COQ2 gene causes defects of bioenergetics and de novo pyrimidine synthesis. Hum Mol Genet 2007; 16:1091-7; PMID:17374725; http://doi.dx.org/10.1093/hmg/ddm058
  • Allan CM, Awad AM, Johnson JS, Shirasaki DI, Wang C, Blaby-Haas CE, Merchant SS, Loo JA, Clarke CF. Identification of Coq11, a New Coenzyme Q Biosynthetic Protein in the CoQ-Synthome in Saccharomyces cerevisiae. J Biol Chem 2015; 290:7517-34; PMID:25631044; http://doi.dx.org/10.1074/jbc.M114.633131
  • Parrado-Fernández C, López-Lluch G, Rodríguez-Bies E, Santa-Cruz S, Navas P, Ramsey JJ, Villalba JM. Calorie restriction modifies ubiquinone and COQ transcript levels in mouse tissues. Free Radic Biol Med 2011; 50:1728-36; PMID:21447381; http://doi.dx.org/10.1016/j.freeradbiomed.2011.03.024
  • González-Mariscal I, García-Testón E, Padilla S, Martín-Montalvo A, Pomares Viciana T, Vazquez-Fonseca L, Gandolfo Domínguez P, Santos-Ocaña C. The Regulation of Coenzyme Q Biosynthesis in Eukaryotic Cells: All That Yeast Can Tell Us. Mol Syndromol 2014; 5:107-18; PMID:25126044; http://doi.dx.org/10.1159/000362897
  • He CH, Xie LX, Allan CM, Tran UC, Clarke CF. Coenzyme Q supplementation or over-expression of the yeast Coq8 putative kinase stabilizes multi-subunit Coq polypeptide complexes in yeast coq null mutants. Biochim Biophys Acta - Mol Cell Biol Lipids 2014; 1841:630-44; PMID:24406904; http://doi.dx.org/10.1016/j.bbalip.2013.12.017
  • Padilla S, Tran UC, Jiménez-Hidalgo M, López-Martín JM, Martín-Montalvo A, Clarke CF, Navas P, Santos-Ocaña C. Hydroxylation of demethoxy-Q6 constitutes a control point in yeast coenzyme Q6 biosynthesis. Cell Mol Life Sci 2009; 66:173-86; PMID:19002377; http://doi.dx.org/10.1007/s00018-008-8547-7
  • Miyadera H, Amino H, Hiraishi A, Taka H, Murayama K, Miyoshi H, Sakamoto K, Ishii N, Hekimi S, Kita K. Altered Quinone Biosynthesis in the Long-lived clk-1Mutants of Caenorhabditis elegans. J Biol Chem 2001; 276:7713-6; PMID:11244089; http://doi.dx.org/10.1074/jbc.C000889200
  • Gao J, Schatton D, Martinelli P, Hansen H, Pla-Martin D, Barth E, Becker C, Altmueller J, Frommolt P, Sardiello M, et al. CLUH regulates mitochondrial biogenesis by binding mRNAs of nuclear-encoded mitochondrial proteins. J Cell Biol 2014; 207:213-23; PMID:25349259; http://doi.dx.org/10.1083/jcb.201403129
  • Pullmann R, Kim HH, Abdelmohsen K, Lal A, Martindale JL, Yang X, Gorospe M. Analysis of Turnover and Translation Regulatory RNA-Binding Protein Expression through Binding to Cognate mRNAs. Mol Cell Biol 2007; 27:6265-78; PMID:17620417; http://doi.dx.org/10.1128/MCB.00500-07
  • Romano M, Buratti E. Targeting RNA Binding Proteins Involved in Neurodegeneration. J Biomol Screen 2013; 18:967-83; PMID:23954928; http://doi.dx.org/10.1177/1087057113497256
  • Szostak E, Gebauer F. Translational control by 3′-UTR-binding proteins. Brief Funct Genomics 2013; 12:58-65; PMID:23196851; http://doi.dx.org/10.1093/bfgp/els056
  • Richman TR, Davies SMK, Shearwood A-MJ, Ermer JA, Scott LH, Hibbs ME, Rackham O, Filipovska A. A bifunctional protein regulates mitochondrial protein synthesis. Nucleic Acids Res 2014; 42:5483-94; PMID:24598254; http://doi.dx.org/10.1093/nar/gku179
  • Svoboda P, Cara AD. Hairpin RNA: a secondary structure of primary importance. Cell Mol Life Sci 2006; 63:901-8; PMID:16568238; http://doi.dx.org/10.1007/s00018-005-5558-5
  • Mignone F, Gissi C, Liuni S, Pesole G. No Title. Genome Biol 2002; 3:reviews0004.1; PMID:11897027; http://doi.dx.org/10.1186/gb-2002-3-3-reviews0004
  • Izquierdo JM, Cuezva JM. Control of the translational efficiency of β-F1-ATPase mRNA depends on the regulation of a protein that binds the 3′ untranslated region of the mRNA. Mol Cell Biol 1997; 17:5255-68; PMID:9271403.
  • Gorospe M, Baglioni C. Degradation of unstable interleukin-1α mRNA in a rabbit reticulocyte cell-free system: Localization of an instability determinant to a cluster of AUUUA motifs. J Biol Chem 1994; 269:11845-51; PMID:8163483.
  • Trevisson E, Dimauro S, Navas P, Salviati L. Coenzyme Q deficiency in muscle. Curr Opin Neurol 2011; 24:449-56; PMID:21844807; http://doi.dx.org/10.1097/WCO.0b013e32834ab528
  • Blaxall BC, Pende A, Wu SC, Port JD. No Title. Mol Cell Biochem 2002; 232:1-11; PMID:12030365; http://doi.dx.org/10.1023/A:1014819016552
  • David PS, Tanveer R, Port JD. FRET-detectable interactions between the ARE binding proteins, HuR and p37AUF1. RNA 2007; 13:1453-68; PMID:17626845; http://doi.dx.org/10.1261/rna.501707
  • Barker A, Epis MR, Porter CJ, Hopkins BR, Wilce MCJ, Wilce JA, Giles KM, Leedman PJ. Sequence requirements for RNA binding by HuR and AUF1. J Biochem 2012; 151:423-37; PMID:22368252; http://doi.dx.org/10.1093/jb/mvs010
  • Masuda K, Marasa B, Martindale JL, Halushka MK, Gorospe M. Tissue- and age-dependent expression of RNA-binding proteins that influence mRNA turnover and translation. Aging (Albany NY) 2009; 1:681-98; PMID:20157551.
  • Izquierdo JM. Heterogeneous ribonucleoprotein C displays a repressor activity mediated by T-cell intracellular antigen-1-related/like protein to modulate Fas exon 6 splicing through a mechanism involving Hu antigen R. Nucleic Acids Res 2010; 38:8001-14; PMID:20699271; http://doi.dx.org/10.1093/nar/gkq698
  • Papadopoulou C, Patrinou-Georgoula M, Guialis A. Extensive association of HuR with hnRNP proteins within immunoselected hnRNP and mRNP complexes. Biochim Biophys Acta - Proteins Proteomics 2010; 1804:692-703; PMID:19931428; http://doi.dx.org/10.1016/j.bbapap.2009.11.007
  • Fan XC, Steitz JA. HNS, a nuclear-cytoplasmic shuttling sequence in HuR. Proc Natl Acad Sci U S A 1998; 95:15293-8; PMID:9860962; http://doi.dx.org/10.1073/pnas.95.26.15293
  • Keene JD. Why is Hu where? Shuttling of early-response-gene messenger RNA subsets. Proc Natl Acad Sci 1999; 96:5-7; PMID:9874760; http://doi.dx.org/10.1073/pnas.96.1.5
  • Lal A, Abdelmohsen K, Pullmann R, Kawai T, Galban S, Yang X, Brewer G, Gorospe M. Posttranscriptional Derepression of GADD45α by Genotoxic Stress. Mol Cell 2006; 22:117-28; PMID:16600875; http://doi.dx.org/10.1016/j.molcel.2006.03.016
  • Wang W, Furneaux H, Cheng H, Caldwell MC, Hutter D, Liu Y, Holbrook N, Gorospe M. HuR Regulates p21 mRNA Stabilization by UV Light. Mol Cell Biol 2000; 20:760-9; PMID:10629032; http://doi.dx.org/10.1128/MCB.20.3.760-769.2000
  • Ortega AD, Sala S, Espinosa E, Gonzalez-Baron M, Cuezva JM. HuR and the bioenergetic signature of breast cancer: a low tumor expression of the RNA-binding protein predicts a higher risk of disease recurrence. Carcinogenesis 2008; 29:2053-61; PMID:18687667; http://doi.dx.org/10.1093/carcin/bgn185
  • Abdelmohsen K, Lal A, Kim HH, Gorospe M. Posttranscriptional Orchestration of an Anti-Apoptotic Program by HuR. Cell Cycle 2007; 6:1288-92; PMID:17534146; http://doi.dx.org/10.4161/cc.6.11.4299
  • Durie D, Hatzoglou M, Chakraborty P, Holcik M. HuR controls mitochondrial morphology through the regulation of BclxL translation. Transl (Austin, Tex) 2013; 1:e23980; PMID:25328858; http://doi.dx.org/10.4161/trla.23980
  • Montero R, Grazina M, López-Gallardo E, Montoya J, Briones P, Navarro-Sastre A, Land JM, Hargreaves IP, Artuch R, del Mar O'Callaghan M, et al. Coenzyme Q10 deficiency in mitochondrial DNA depletion syndromes. Mitochondrion 2013; 13:337-41; PMID:23583954; http://doi.dx.org/10.1016/j.mito.2013.04.001
  • Larsson O. Role of biosynthesis of cholesterol and isoprenoid derivatives in regulation of G1 progression and cell proliferation of 3T6 cells. J Cell Physiol 1987; 133:163-8; PMID:3667703; http://doi.dx.org/10.1002/jcp.1041330121
  • Abdelmohsen K, Pullmann R, Lal A, Kim HH, Galban S, Yang X, Blethrow JD, Walker M, Shubert J, Gillespie DA, et al. Phosphorylation of HuR by Chk2 Regulates SIRT1 Expression. Mol Cell 2007; 25:543-57; PMID:17317627; http://doi.dx.org/10.1016/j.molcel.2007.01.011