Differential proteomic and oxidative profiles unveil dysfunctional protein import to adipocyte mitochondria in obesity-associated aging and diabetes

Redox Biology - Tập 11 - Trang 415-428 - 2017
María Gómez‐Serrano1,2, Emilio Camafeita3, Juan Antonio López3, Miguel A. Rubio4, Irene Bretón Lesmes5, Inés García‐Consuegra6,7, Eva García‐Santos1,2, Jesús Lago8, Andrés Sánchez-Pernaute9, Antonio Torres9, Jesús Vázquez3, Belén Peral1,2
1Consejo Superior de Investigaciones Científicas & Universidad Autónoma de Madrid (CSIC-UAM), Madrid 28029, Spain
2Instituto de Investigaciones Biomédicas, Alberto Sols, (IIBM)
3Laboratory of Cardiovascular Proteomics, Centro Nacional de Investigaciones Cardiovasculares (CNIC), Madrid 28029, Spain
4Department of Endocrinology, Hospital Clínico San Carlos (IDISSC), Facultad de Medicina, Universidad Complutense, Madrid 28040, Spain
5Department of Endocrinology and Nutrition, Hospital General Universitario Gregorio Marañón (IISGM), Madrid 28007, Spain
6Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER), U723, Madrid 28029, Spain
7Instituto de Investigación, Hospital Universitario 12 de Octubre (i+12), Madrid 28041, Spain
8Department of Surgery, Hospital General Universitario Gregorio Marañón (IISGM), Madrid 28007, Spain
9Department of Surgery, Hospital Clínico San Carlos (IDISSC), Facultad de Medicina, Universidad Complutense, Madrid 28040, Spain

Tóm tắt

Từ khóa


Tài liệu tham khảo

Starkov, 2008, The role of mitochondria in reactive oxygen species metabolism and signaling, Ann. N.Y. Acad. Sci., 1147, 37, 10.1196/annals.1427.015

Cheng, 2013, Mitochondria and metabolic homeostasis, Antioxid. Redox Signal., 19, 240, 10.1089/ars.2013.5255

Murphy, 2012, Mitochondrial thiols in antioxidant protection and redox signaling: distinct roles for glutathionylation and other thiol modifications, Antioxid. Redox Signal., 16, 476, 10.1089/ars.2011.4289

James, 2012, Mitochondrial oxidative stress and the metabolic syndrome, Trends Endocrinol. Metab.: TEM, 23, 429, 10.1016/j.tem.2012.06.008

James, 2008, The epidemiology of obesity: the size of the problem, J. Intern. Med., 263, 336, 10.1111/j.1365-2796.2008.01922.x

Kershaw, 2004, Adipose tissue as an endocrine organ, J. Clin. Endocrinol. Metab., 89, 2548, 10.1210/jc.2004-0395

Neeland, 2012, Dysfunctional adiposity and the risk of prediabetes and type 2 diabetes in obese adults, JAMA: J. Am. Med. Assoc., 308, 1150, 10.1001/2012.jama.11132

Ahima, 2011, Digging deeper into obesity, J. Clin. Investig., 121, 2076, 10.1172/JCI58719

Gao, 2014, Mitochondrial response to nutrient availability and its role in metabolic disease, EMBO Mol. Med., 6, 580, 10.1002/emmm.201303782

Petersen, 2003, Mitochondrial dysfunction in the elderly: possible role in insulin resistance, Science, 300, 1140, 10.1126/science.1082889

Patti, 2010, The role of mitochondria in the pathogenesis of type 2 diabetes, Endocr. Rev., 31, 364, 10.1210/er.2009-0027

Wang, 2015, redox modulation of adipocyte differentiation: hypothesis of "redox chain" and novel insights into intervention of adipogenesis and obesity, Free Radic. Biol. Med., 89, 99, 10.1016/j.freeradbiomed.2015.07.012

Jankovic, 2015, Redox implications in adipose tissue (dys)function – a new look at old acquaintances, Redox Biol., 6, 19, 10.1016/j.redox.2015.06.018

Holmstrom, 2012, Tissue-specific control of mitochondrial respiration in obesity-related insulin resistance and diabetes, Am. J. Physiol. Endocrinol. Metab., 302, E731, 10.1152/ajpendo.00159.2011

Kusminski, 2012, Mitochondrial dysfunction in white adipose tissue, Trends Endocrinol. Metab.: TEM, 23, 435, 10.1016/j.tem.2012.06.004

Boudina, 2014, Mitochondrial function/dysfunction in white adipose tissue, Exp. Physiol., 99, 1168, 10.1113/expphysiol.2014.081414

Perez-Perez, 2012, Attenuated metabolism is a hallmark of obesity as revealed by comparative proteomic analysis of human omental adipose tissue, J. Proteom., 75, 783, 10.1016/j.jprot.2011.09.016

Rabilloud, 1998, Two-dimensional electrophoresis of human placental mitochondria and protein identification by mass spectrometry: toward a human mitochondrial proteome, Electrophoresis, 19, 1006, 10.1002/elps.1150190616

Taylor, 2003, Characterization of the human heart mitochondrial proteome, Nat. Biotechnol., 21, 281, 10.1038/nbt793

Lindinger, 2015, Important mitochondrial proteins in human omental adipose tissue show reduced expression in obesity, J. Proteom., 124, 79, 10.1016/j.jprot.2015.03.037

Lefort, 2009, Proteome profile of functional mitochondria from human skeletal muscle using one-dimensional gel electrophoresis and HPLC-ESI-MS/MS, J. Proteom., 72, 1046, 10.1016/j.jprot.2009.06.011

Winterbourn, 2008, Thiol chemistry and specificity in redox signaling, Free Radic. Biol. Med., 45, 549, 10.1016/j.freeradbiomed.2008.05.004

Ckless, 2014, Redox proteomics: from bench to bedside, Adv. Exp. Med. Biol., 806, 301, 10.1007/978-3-319-06068-2_13

Wojdyla, 2015, Differential alkylation-based redox proteomics – lessons learnt, Redox Biol., 6, 240, 10.1016/j.redox.2015.08.005

Bak, 2015, Cysteine-mediated redox signalling in the mitochondria, Mol. Biosyst., 11, 678, 10.1039/C4MB00571F

Holmstrom, 2014, Cellular mechanisms and physiological consequences of redox-dependent signalling, Nat. Rev. Mol. Cell Biol., 15, 411, 10.1038/nrm3801

Martinez-Acedo, 2012, A novel strategy for global analysis of the dynamic thiol redox proteome, Mol. Cell. Proteom.: MCP, 11, 800, 10.1074/mcp.M111.016469

Martinez-Bartolome, 2008, Properties of average score distributions of SEQUEST: the probability ratio method, Mol. Cell. Proteom.: MCP, 7, 1135, 10.1074/mcp.M700239-MCP200

Navarro, 2009, A refined method to calculate false discovery rates for peptide identification using decoy databases, J. Proteome Res., 8, 1792, 10.1021/pr800362h

Lopez-Ferrer, 2006, Quantitative proteomics using 16O/18O labeling and linear ion trap mass spectrometry, Proteomics, 6, S4, 10.1002/pmic.200500375

Ramos-Fernandez, 2007, Improved method for differential expression proteomics using trypsin-catalyzed 18O labeling with a correction for labeling efficiency, Mol. Cell. Proteom.: MCP, 6, 1274, 10.1074/mcp.T600029-MCP200

Navarro, 2014, General statistical framework for quantitative proteomics by stable isotope labeling, J. Proteome Res., 13, 1234, 10.1021/pr4006958

Luo, 2012, Protein quantitation using iTRAQ: review on the sources of variations and analysis of nonrandom missingness, Stat. Interface, 5, 99, 10.4310/SII.2012.v5.n1.a9

F. Garcia-Marques, M. Trevisan-Herraz, S. Martinez-Martinez, E. Camafeita, I. Jorge, J.A. Lopez, N. Mendez-Barbero, S. Mendez-Ferrer, M.A. Del Pozo, B. Ibanez, V. Andres, F. Sanchez-Madrid, J.M. Redondo, E. Bonzon-Kulichenko, J. VazquezA novel systems-biology algorithm for the analysis of coordinated protein responses using quantitative proteomics, Mol. Cell. Proteom.: MCP, 2016

Huang da, 2009, Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists, Nucleic Acids Res., 37, 1, 10.1093/nar/gkn923

Calvo, 2016, MitoCarta2.0: an updated inventory of mammalian mitochondrial proteins, Nucleic Acids Res., 44, D1251, 10.1093/nar/gkv1003

Huang da, 2009, Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources, Nat. Protoc., 4, 44, 10.1038/nprot.2008.211

Gomez-Serrano, 2016, Proteome-wide alterations on adipose tissue from obese patients as age-, diabetes- and gender-specific hallmarks, Sci. Rep., 6, 25756, 10.1038/srep25756

Pagliarini, 2008, A mitochondrial protein compendium elucidates complex I disease biology, Cell, 134, 112, 10.1016/j.cell.2008.06.016

Smith, 2016, MitoMiner v3.1, an update on the mitochondrial proteomics database, Nucleic Acids Res., 44, D1258, 10.1093/nar/gkv1001

Uhlen, 2015, Proteomics. Tissue-based map of the human proteome, Science, 347, 1260419, 10.1126/science.1260419

B. Alberts, A. Johnson, J. Lewis, P. Walter, M. Raff, K. Roberts. Molecular Biology of the Cell 4th Edition edition: International Student Edition, 2002, Routledge

Abdulhag, 2015, Mitochondrial complex IV deficiency, caused by mutated COX6B1, is associated with encephalomyopathy, hydrocephalus and cardiomyopathy, Eur. J. Hum. Genet, 23, 159, 10.1038/ejhg.2014.85

Massa, 2008, Severe infantile encephalomyopathy caused by a mutation in COX6B1, a nucleus-encoded subunit of cytochrome c oxidase, Am. J. Hum. Genet, 82, 1281, 10.1016/j.ajhg.2008.05.002

Garcia-Marques, 2016, A novel systems-biology algorithm for the analysis of coordinated protein responses using quantitative proteomics, Mol. Cell. Proteom.: MCP, 15, 1740, 10.1074/mcp.M115.055905

Sprinzak, 2009, Detecting coordinated regulation of multi-protein complexes using logic analysis of gene expression, BMC Syst. Biol., 3, 115, 10.1186/1752-0509-3-115

Aguer, 1832, Increased proton leak and SOD2 expression in myotubes from obese non-diabetic subjects with a family history of type 2diabetes, Biochim. Biophys. Acta, 1624–1633, 2013

Han, 2016, Adipocyte-specific deletion of manganese superoxide dismutase protects from diet-induced obesity through increased mitochondrial uncoupling and biogenesis, Diabetes, 65, 2639, 10.2337/db16-0283

Mimaki, 1817, Understanding mitochondrial complex I assembly in health and disease, Biochim. Biophys. Acta, 851–862, 2012

D.A. Stroud, E.E. Surgenor, L.E. Formosa, B. Reljic, A.E. Frazier, M.G. Dibley, L.D. Osellame, T. Stait, T.H. Beilharz, D.R. Thorburn, A. Salim, M.T. Ryan, Accessory subunits are integral for assembly and function of human mitochondrial complex I. Nature 538 (2016) 123-126.

Zickermann, 2015, Structural biology. Mechanistic insight from the crystal structure of mitochondrial complex I, Science, 347, 44, 10.1126/science.1259859

Srinivasan, 2012, Cytochrome c oxidase dysfunction in oxidative stress, Free Radic. Biol. Med., 53, 1252, 10.1016/j.freeradbiomed.2012.07.021

Mick, 2011, Inventory control: cytochrome c oxidase assembly regulates mitochondrial translation, Nat. Rev. Mol. Cell Biol., 12, 14, 10.1038/nrm3029

Sanchez-Caballero, 1857, Unraveling the complexity of mitochondrial complex I assembly: a dynamic process, Biochim. Et. Biophys. Acta, 980–990, 2016

Larsson, 1998, Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice, Nat. Genet, 18, 231, 10.1038/ng0398-231

Campbell, 1819, Mitochondrial transcription factor A regulates mitochondrial transcription initiation, DNA packaging, and genome copy number, Biochim. Biophys. Acta, 921–929, 2012

Picca, 2013, Aging and calorie restriction oppositely affect mitochondrial biogenesis through TFAM binding at both origins of mitochondrial DNA replication in rat liver, PLoS One, 8, e74644, 10.1371/journal.pone.0074644

Pesce, 2005, Age-related changes of mitochondrialDNA content and mitochondrial genotypic and phenotypic alterations in rat hind-limb skeletal muscles, J. Gerontol. Ser. A Biol. Sci. Med. Sci., 60, 715, 10.1093/gerona/60.6.715

Heinonen, 2015, Impaired mitochondrial biogenesis in adipose tissue in acquired obesity, Diabetes, 64, 3135, 10.2337/db14-1937

Vernochet, 2012, Adipose-specific deletion of TFAM increases mitochondrial oxidation and protects mice against obesity and insulin resistance, Cell Metab., 16, 765, 10.1016/j.cmet.2012.10.016

Villarroya, 2009, Mitochondrial DNA: an up-and-coming actor in white adipose tissue pathophysiology, Obesity (Silver Spring), 17, 1814, 10.1038/oby.2009.152

Young, 2003, Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70, Cell, 112, 41, 10.1016/S0092-8674(02)01250-3

Schmidt, 2010, Mitochondrial protein import: from proteomics to functional mechanisms, Nat. Rev. Mol. Cell Biol., 11, 655, 10.1038/nrm2959

Lindinger, 2010, Mitochondrial DNA content in human omental adipose tissue, Obes. Surg., 20, 84, 10.1007/s11695-009-9987-3

Hsieh, 2011, Tissue-specific differences in mitochondrial DNA content in type 2 diabetes, Diabetes Res. Clin. Pract., 92, 106, 10.1016/j.diabres.2011.01.010

Harman, 1956, Aging: a theory based on free radical and radiation chemistry, J. Gerontol., 11, 298, 10.1093/geronj/11.3.298

Stojanovski, 1823, The MIA pathway: a tight bond between protein transport and oxidative folding in mitochondria, Biochim. Biophys. Acta, 1142–1150, 2012

Szklarczyk, 2011, NDUFB7 and NDUFA8 are located at the intermembrane surface of complex I, FEBS Lett., 585, 737, 10.1016/j.febslet.2011.01.046

Modjtahedi, 2016, Mitochondrial proteins containing, Trends Biochem. Sci., 41, 245, 10.1016/j.tibs.2015.12.004

Barzilai, 2012, The critical role of metabolic pathways in aging, Diabetes, 61, 1315, 10.2337/db11-1300

Fink, 1983, Mechanisms of insulin resistance in aging, J. Clin. Investig., 71, 1523, 10.1172/JCI110908

Go, 2015, The cysteine proteome, Free Radic. Biol. Med., 84, 227, 10.1016/j.freeradbiomed.2015.03.022

Lapuente-Brun, 2013, Supercomplex assembly determines electron flux in the mitochondrial electron transport chain, Science, 340, 1567, 10.1126/science.1230381

Antoun, 2015, Impaired mitochondrial oxidative phosphorylation and supercomplex assembly in rectus abdominis muscle of diabetic obese individuals, Diabetologia, 58, 2861, 10.1007/s00125-015-3772-8