Analysis of the effect of the mitochondrial prohibitin complex, a context-dependent modulator of longevity, on the C. elegans metabolome

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1847, Issue 11, 2015, Pages 1457-1468

  Lourenço, Artur B ^a   Muñoz Jiménez, Celia ^a   Venegas Calerón, Mónica ^b   Artal Sanz, Marta ^a  

^a UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

^b INSTITUTO DE LA GRASA   (Spain)

Author keywords

C. elegans; Insulin signalling; Longevity; Metabolomics; Mitochondria; Prohibitin

Indexed keywords

ALANINE; AMINO ACID; CARBOHYDRATE; FATTY ACID; GLUTAMIC ACID; GLUTAMINE; GLYCEROL; INSULIN; LACTIC ACID; LEUCINE; PROHIBITIN; TREHALOSE; VALINE; REPRESSOR PROTEIN;

AMINO ACID METABOLISM; ARTICLE; CAENORHABDITIS ELEGANS; CARBOHYDRATE METABOLISM; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DIAPAUSE; FATTY ACID METABOLISM; GAS CHROMATOGRAPHY; GENE MUTATION; LARVAL STAGE; LIPID COMPOSITION; LONGEVITY; METABOLOME; MITOCHONDRIAL PROHIBITIN COMPLEX; MITOCHONDRION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTON NUCLEAR MAGNETIC RESONANCE; SIGNAL TRANSDUCTION; WILD TYPE; ANIMAL; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHYSIOLOGY;

ANIMALS; CAENORHABDITIS ELEGANS; FATTY ACIDS; LONGEVITY; MAGNETIC RESONANCE SPECTROSCOPY; METABOLOME; MITOCHONDRIA; REPRESSOR PROTEINS;

EID: 84941747977     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2015.06.003     Document Type: Article

References (70)

1. W.B. Wood, and T.E. Johnson Aging. Stopping the clock Curr. Biol. 4 1994 151 153
2. C.J. Kenyon The genetics of ageing Nature 464 2010 504 512
3. K.D. Kimura, H.A. Tissenbaum, Y. Liu, and G. Ruvkun daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans Science 277 1997 942 946
4. S.B. Roberts, and I. Rosenberg Nutrition and aging: changes in the regulation of energy metabolism with aging Physiol. Rev. 86 2006 651 667
5. R.S. Balaban, S. Nemoto, and T. Finkel Mitochondria, oxidants, and aging Cell 120 2005 483 495
6. M. Artal-Sanz, and N. Tavernarakis Prohibitin couples diapause signalling to mitochondrial metabolism during ageing in C. elegans Nature 461 2009 793 797
7. J.W. Back, M.A. Sanz, L. De Jong, L.J. De Koning, L.G. Nijtmans, and et al. A structure for the yeast prohibitin complex: structure prediction and evidence from chemical crosslinking and mass spectrometry Protein Sci. 11 2002 2471 2478
8. M. Artal-Sanz, W.Y. Tsang, E.M. Willems, L.A. Grivell, B.D. Lemire, and et al. The mitochondrial prohibitin complex is essential for embryonic viability and germline function in Caenorhabditis elegans J. Biol. Chem. 278 2003 32091 32099
9. C. Merkwirth, S. Dargazanli, T. Tatsuta, S. Geimer, B. Lower, and et al. Prohibitins control cell proliferation and apoptosis by regulating OPA1-dependent cristae morphogenesis in mitochondria Genes Dev. 22 2008 476 488
10. K.H. Berger, and M.P. Yaffe Prohibitin family members interact genetically with mitochondrial inheritance components in Saccharomyces cerevisiae Mol. Cell. Biol. 18 1998 4043 4052
11. M. Artal-Sanz, and N. Tavernarakis Opposing function of mitochondrial prohibitin in aging Aging (Albany NY) 2 2010 1004 1011
12. M. Artal-Sanz, and N. Tavernarakis Prohibitin and mitochondrial biology Trends Endocrinol. Metab. 20 2009 394 401
13. L.G. Nijtmans, L. de Jong, M. Artal Sanz, P.J. Coates, J.A. Berden, and et al. Prohibitins act as a membrane-bound chaperone for the stabilization of mitochondrial proteins EMBO J. 19 2000 2444 2451
14. L.G. Nijtmans, S.M. Artal, L.A. Grivell, and P.J. Coates The mitochondrial PHB complex: roles in mitochondrial respiratory complex assembly, ageing and degenerative disease Cell. Mol. Life Sci. 59 2002 143 155
15. C. Osman, M. Haag, C. Potting, J. Rodenfels, P.V. Dip, and et al. The genetic interactome of prohibitins: coordinated control of cardiolipin and phosphatidylethanolamine by conserved regulators in mitochondria J. Cell Biol. 184 2009 583 596
16. R. Richter-Dennerlein, A. Korwitz, M. Haag, T. Tatsuta, S. Dargazanli, and et al. DNAJC19, a mitochondrial cochaperone associated with cardiomyopathy, forms a complex with prohibitins to regulate cardiolipin remodeling Cell Metab. 20 2014 158 171
17. J. Schleit, S.C. Johnson, C.F. Bennett, M. Simko, N. Trongtham, and et al. Molecular mechanisms underlying genotype-dependent responses to dietary restriction Aging Cell 12 2013 1050 1061
18. J. McElwee, K. Bubb, and J.H. Thomas Transcriptional outputs of the Caenorhabditis elegans forkhead protein DAF-16 Aging Cell 2 2003 111 121
19. C. Kenyon, J. Chang, E. Gensch, A. Rudner, and R. Tabtiang A C. elegans mutant that lives twice as long as wild type Nature 366 1993 461 464
20. S.B. Pierce, M. Costa, R. Wisotzkey, S. Devadhar, S.A. Homburger, and et al. Regulation of DAF-2 receptor signaling by human insulin and ins-1, a member of the unusually large and diverse C. elegans insulin gene family Genes Dev. 15 2001 672 686
21. W. Li, S.G. Kennedy, and G. Ruvkun daf-28 encodes a C. elegans insulin superfamily member that is regulated by environmental cues and acts in the DAF-2 signaling pathway Genes Dev. 17 2003 844 858
22. P. Ruzanov, D.L. Riddle, M.A. Marra, S.J. McKay, and S.M. Jones Genes that may modulate longevity in C. elegans in both dauer larvae and long-lived daf-2 adults Exp. Gerontol. 42 2007 825 839
23. M. Artal-Sanz, and N. Tavernarakis Mechanisms of aging and energy metabolism in Caenorhabditis elegans IUBMB Life 60 2008 315 322
24. K. Ashrafi Mapping out starvation responses Cell Metab. 3 2006 235 236
25. E.J. O'Rourke, A.A. Soukas, C.E. Carr, and G. Ruvkun C. elegans major fats are stored in vesicles distinct from lysosome-related organelles Cell Metab. 10 2009 430 435
26. G.A. Lemieux, and K. Ashrafi Insights and challenges in using C. elegans for investigation of fat metabolism Crit. Rev. Biochem. Mol. Biol. 2014 1 16
27. W.B. Dunn, N.J. Bailey, and H.E. Johnson Measuring the metabolome: current analytical technologies Analyst 130 2005 606 625
28. V. Matyash, G. Liebisch, T.V. Kurzchalia, A. Shevchenko, and D. Schwudke Lipid extraction by methyl-tert-butyl ether for high-throughput lipidomics J. Lipid Res. 49 2008 1137 1146
29. B. Gonzalez, J. Francois, and M. Renaud A rapid and reliable method for metabolite extraction in yeast using boiling buffered ethanol Yeast 13 1997 1347 1355
30. D.S. Wishart, T. Jewison, A.C. Guo, M. Wilson, C. Knox, and et al. HMDB 3.0 - The Human Metabolome Database in 2013 Nucleic Acids Res. 41 2013 D801 D807
31. Q. Cui, I.A. Lewis, A.D. Hegeman, M.E. Anderson, J. Li, and et al. Metabolite identification via the Madison Metabolomics Consortium Database Nat. Biotechnol. 26 2008 162 164
32. W.A. Van Voorhies The influence of metabolic rate on longevity in the nematode Caenorhabditis elegans Aging Cell 1 2002 91 101
33. C. Castro, J. Krumsiek, N.J. Lehrbach, S.A. Murfitt, E.A. Miska, and et al. A study of Caenorhabditis elegans DAF-2 mutants by metabolomics and differential correlation networks Mol. BioSyst. 9 2013 1632 1642
34. S.L. Yu, Y.J. An, H.J. Yang, M.S. Kang, H.Y. Kim, and et al. Alanine-metabolizing enzyme Alt1 is critical in determining yeast life span, as revealed by combined metabolomic and genetic studies J. Proteome Res. 12 2013 1619 1627
35. S. Mishra, L.C. Murphy, and L.J. Murphy The prohibitins: emerging roles in diverse functions J. Cell. Mol. Med. 10 2006 353 363
36. L.M. Raamsdonk, B. Teusink, D. Broadhurst, N. Zhang, A. Hayes, and et al. A functional genomics strategy that uses metabolome data to reveal the phenotype of silent mutations Nat. Biotechnol. 19 2001 45 50
37. R.J. Bino, R.D. Hall, O. Fiehn, J. Kopka, K. Saito, and et al. Potential of metabolomics as a functional genomics tool Trends Plant Sci. 9 2004 418 425
38. R.J. Shmookler Reis, L. Xu, H. Lee, M. Chae, J.J. Thaden, and et al. Modulation of lipid biosynthesis contributes to stress resistance and longevity of C. elegans mutants Aging (Albany NY) 3 2011 125 147
39. E.J. O'Rourke, P. Kuballa, R. Xavier, and G. Ruvkun omega-6 polyunsaturated fatty acids extend life span through the activation of autophagy Genes Dev. 27 2013 429 440
40. M.R. Van Gilst, H. Hadjivassiliou, A. Jolly, and K.R. Yamamoto Nuclear hormone receptor NHR-49 controls fat consumption and fatty acid composition in C. elegans PLoS Biol. 3 2005 e53
41. C. Edwards, J. Canfield, N. Copes, A. Brito, M. Rehan, and et al. Mechanisms of amino acid-mediated lifespan extension in Caenorhabditis elegans BMC Genet. 16 2015 8
42. F.P. Martin, B. Spanier, S. Collino, I. Montoliu, C. Kolmeder, and et al. Metabotyping of Caenorhabditis elegans and their culture media revealed unique metabolic phenotypes associated to amino acid deficiency and insulin-like signaling J. Proteome Res. 10 2011 990 1003
43. S. Fuchs, J.G. Bundy, S.K. Davies, J.M. Viney, J.S. Swire, and et al. A metabolic signature of long life in Caenorhabditis elegans BMC Biol. 8 2010 14
44. S.N. Reinke, X. Hu, B.D. Sykes, and B.D. Lemire Caenorhabditis elegans diet significantly affects metabolic profile, mitochondrial DNA levels, lifespan and brood size Mol. Genet. Metab. 100 2010 274 282
45. P. Newsholme, J. Procopio, M.M. Lima, T.C. Pithon-Curi, and R. Curi Glutamine and glutamate - their central role in cell metabolism and function Cell Biochem. Funct. 21 2003 1 9
46. R.M. Chin, X. Fu, M.Y. Pai, L. Vergnes, H. Hwang, and et al. The metabolite alpha-ketoglutarate extends lifespan by inhibiting ATP synthase and TOR Nature 510 2014 397 401
47. S. Schrier Vergano, M. Rao, S. McCormack, J. Ostrovsky, C. Clarke, and et al. In vivo metabolic flux profiling with stable isotopes discriminates sites and quantifies effects of mitochondrial dysfunction in C. elegans Mol. Genet. Metab. 111 2014 331 341
48. J.R. Vanfleteren, and B.P. Braeckman Mechanisms of life span determination in Caenorhabditis elegans Neurobiol. Aging 20 1999 487 502
49. M. Kunze, I. Pracharoenwattana, S.M. Smith, and A. Hartig A central role for the peroxisomal membrane in glyoxylate cycle function Biochim. Biophys. Acta 1763 2006 1441 1452
50. M.E. Forsythe, D.C. Love, B.D. Lazarus, E.J. Kim, W.A. Prinz, and et al. Caenorhabditis elegans ortholog of a diabetes susceptibility locus: oga-1 (O-GlcNAcase) knockout impacts O-GlcNAc cycling, metabolism, and dauer Proc. Natl. Acad. Sci. U. S. A. 103 2006 11952 11957
51. J.J. McElwee, E. Schuster, E. Blanc, J. Thornton, and D. Gems Diapause-associated metabolic traits reiterated in long-lived daf-2 mutants in the nematode Caenorhabditis elegans Mech. Ageing Dev. 127 2006 458 472
52. R.K. Chaudhary, J. Kardani, K. Singh, R. Banerjee, and I. Roy Deciphering the roles of trehalose and Hsp104 in the inhibition of aggregation of mutant huntingtin in a yeast model of Huntington's disease Neruomol. Med. 16 2014 280 291
53. J.E. Purvis, L.P. Yomano, and L.O. Ingram Enhanced trehalose production improves growth of Escherichia coli under osmotic stress Appl. Environ. Microbiol. 71 2005 3761 3769
54. A. Hedoux, L. Paccou, S. Achir, and Y. Guinet Mechanism of protein stabilization by trehalose during freeze-drying analyzed by in situ micro-raman spectroscopy J. Pharm. Sci. 102 2013 2484 2494
55. G. Depuydt, F. Xie, V.A. Petyuk, A. Smolders, H.M. Brewer, and et al. LC-MS proteomics analysis of the insulin/IGF-1-deficient Caenorhabditis elegans daf-2(e1370) mutant reveals extensive restructuring of intermediary metabolism J. Proteome Res. 13 2014 1938 1956
56. S. Rea, and T.E. Johnson A metabolic model for life span determination in Caenorhabditis elegans Dev. Cell 5 2003 197 203
57. K. Houthoofd, M.A. Fidalgo, D. Hoogewijs, B.P. Braeckman, I. Lenaerts, and et al. Metabolism, physiology and stress defense in three aging Ins/IGF-1 mutants of the nematode Caenorhabditis elegans Aging Cell 4 2005 87 95
58. M. Hansen, T. Flatt, and H. Aguilaniu Reproduction, fat metabolism, and life span: what is the connection? Cell Metab. 17 2013 10 19
59. R. Ratnappan, F.R. Amrit, S.W. Chen, H. Gill, K. Holden, and et al. Germline signals deploy NHR-49 to modulate fatty-acid beta-oxidation and desaturation in somatic tissues of C. elegans PLoS Genet. 10 2014 e1004829
60. H. Hsin, and C. Kenyon Signals from the reproductive system regulate the lifespan of C. elegans Nature 399 1999 362 366
61. C.B. Edwards, N. Copes, A.G. Brito, J. Canfield, and P.C. Bradshaw Malate and fumarate extend lifespan in Caenorhabditis elegans PLoS One 8 2013 e58345
62. W.G. Wadsworth, and D.L. Riddle Developmental regulation of energy metabolism in Caenorhabditis elegans Dev. Biol. 132 1989 167 173
63. D. Cristina, M. Cary, A. Lunceford, C. Clarke, and C. Kenyon A regulated response to impaired respiration slows behavioral rates and increases lifespan in Caenorhabditis elegans PLoS Genet. 5 2009 e1000450
64. M. Schleicher, B.R. Shepherd, Y. Suarez, C. Fernandez-Hernando, J. Yu, and et al. Prohibitin-1 maintains the angiogenic capacity of endothelial cells by regulating mitochondrial function and senescence J. Cell Biol. 180 2008 101 112
65. P. Zhou, L. Qian, M. D'Aurelio, S. Cho, G. Wang, and et al. Prohibitin reduces mitochondrial free radical production and protects brain cells from different injury modalities J. Neurosci. 32 2012 583 592
66. S. Supale, F. Thorel, C. Merkwirth, A. Gjinovci, P.L. Herrera, and et al. Loss of prohibitin induces mitochondrial damages altering beta-cell function and survival and is responsible for gradual diabetes development Diabetes 62 2013 3488 3499
67. R. Vartak, C.A. Porras, and Y. Bai Respiratory supercomplexes: structure, function and assembly Protein Cell 4 2013 582 590
68. I. Gohring, and H. Mulder Glutamate dehydrogenase, insulin secretion, and type 2 diabetes: a new means to protect the pancreatic beta-cell? J. Endocrinol. 212 2012 239 242
69. C.A. Stanley, J. Fang, K. Kutyna, B.Y. Hsu, J.E. Ming, and et al. Molecular basis and characterization of the hyperinsulinism/hyperammonemia syndrome: predominance of mutations in exons 11 and 12 of the glutamate dehydrogenase gene. HI/HA contributing investigators Diabetes 49 2000 667 673
70. T. Yorifuji, J. Muroi, A. Uematsu, H. Hiramatsu, and T. Momoi Hyperinsulinism-hyperammonemia syndrome caused by mutant glutamate dehydrogenase accompanied by novel enzyme kinetics Hum. Genet. 104 1999 476 479