Serum profiling of healthy aging identifies phospho- and sphingolipid species as markers of human longevity

Aging

Volumn 6, Issue 1, 2014, Pages 9-25

  Montoliu, Ivan ^a   Scherer, Max ^a   Beguelin, Fiona ^a   DaSilva, Laeticia ^a   Mari, Daniela ^b,c   Salvioli, Stefano ^d   Martin, François Pierre J ^a   Capri, Miriam ^d   Bucci, Laura ^d   Ostan, Rita ^d   Garagnani, Paolo ^d   Monti, Daniela ^e   Biagi, Elena ^d   Brigidi, Patrizia ^d   Kussmann, Martin ^a,f,g   Rezzi, Serge ^a   Franceschi, Claudio ^d   Collino, Sebastiano ^a  

^a NESTLÉ RESEARCH CENTER   (Switzerland)

^b UNIVERSITY OF MILAN   (Italy)

^c FONDAZIONE IRCCS CA GRANDA OSPEDALE MAGGIORE POLICLINICO   (Italy)

^d UNIVERSITY OF BOLOGNA   (Italy)

^e UNIVERSITY OF FLORENCE   (Italy)

^f EPFL   (Switzerland)

^g AARHUS UNIVERSITY   (Denmark)

Author keywords

Biomarkers; Healthy aging; Inflammageing; Lipidomics; Metabolomics

Indexed keywords

AMINO ACID; BIOLOGICAL MARKER; PHOSPHOLIPID; SPHINGOLIPID;

AGE; AGED; AGING; ARTICLE; BLOOD; FEMALE; HUMAN; LONGEVITY; MALE; METABOLOMICS; METHODOLOGY; MIDDLE AGED; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; VERY ELDERLY;

AGE FACTORS; AGED; AGED, 80 AND OVER; AGING; AMINO ACIDS; BIOLOGICAL MARKERS; FEMALE; HEALTHY VOLUNTEERS; HUMANS; LONGEVITY; MAGNETIC RESONANCE SPECTROSCOPY; MALE; METABOLOMICS; MIDDLE AGED; PHOSPHOLIPIDS; SPHINGOLIPIDS;

EID: 84893485982     PISSN: 19454589     EISSN: None     Source Type: Journal    
DOI: 10.18632/aging.100630     Document Type: Article

References (55)

1. Sansoni P, Vescovini R, Fagnoni F, Biasini C, Zanni F, Zanlari L, Telera A, Lucchini G, Passeri G, Monti D, Franceschi C, Passeri M. The immune system in extreme longevity. Exp Gerontol. 2008;43:61-65.
2. Franceschi C, Capri M, Monti D, Giunta S, Olivieri F, Sevini F, Panourgia MP, Invidia L, Celani L, Scurti M, Cevenini E, Castellani GC, Salvioli S. Inflammaging and anti-inflammaging: a systemic perspective on aging and longevity emerged from studies in humans. Mech Ageing Dev. 2007;128:92-105.
3. Franceschi C. Inflammaging as a major characteristic of old people: can it be prevented or cured? Nutr Rev. 2007;65:S173-S176.
4. Burkle A, Caselli G, Franceschi C, Mariani E, Sansoni P, Santoni A, Vecchio G, Witkowski JM, Caruso C. Pathophysiology of ageing, longevity and age related diseases. Immun Ageing. 2007;4:4.
5. Franceschi C, Capri M, Monti D, Giunta S, Olivieri F, Sevini F, Panourgia MP, Invidia L, Celani L, Scurti M, Cevenini E, Castellani GC, Salvioli S: Inflammaging and anti-inflammaging: a systemic perspective on aging and longevity emerged from studies in humans. Mech Ageing Dev. 2007;128:92-105.
6. Franceschi C, Bonafe M. Centenarians as a model for healthy aging. Biochem Soc Trans. 2003;31:457-461.
7. Nicholson JK, Holmes E, Wilson ID. Gut microorganisms, mammalian metabolism and personalized health care. Nat Rev Microbiol. 2005;3:431-438.
8. Li M, Wang B, Zhang M, Rantalainen M, Wang S, Zhou H, Zhang Y, Shen J, Pang X, Zhang M, Wei H, Chen Y, Lu H, Zuo J, Su M, Qiu Y, Jia W, Xiao C, Smith LM, Yang S, Holmes E, Tang H, Zhao G, Nicholson JK, Li L, Zhao L. Symbiotic gut microbes modulate human metabolic phenotypes. Proc Natl Acad Sci U S A. 2008;105:2117-2122.
9. Martin F-PJ, Wang Y, Sprenger N, Yap IKS, Rezzi S, Ramadan Z, Pere-Trepat E, Rochat F, Cherbut C, van Bladeren P, Fay LB, Kochhar S, Lindon JC, Holmes E, Nicholson JK. Top-down Systems Biology Integration of Conditional Prebiotic Transgenomic Interactions in a Humanized Microbiome Mouse Model. Mol Syst Biol. 2008;4:205.
10. Selman C, Kerrison ND, Cooray A, Piper MD, Lingard SJ, Barton RH, Schuster EF, Blanc E, Gems D, Nicholson JK, Thornton JM, Partridge L, Withers DJ. Coordinated multi-tissue transcriptional and plasma metabonomic profiles following acute caloric restriction in mice. Physiol Genomics 2006.
11. Wang Y, Lawler D, Larson B, Ramadan Z, Kochhar S, Holmes E, Nicholson JK. Metabonomic Investigations of Aging and Caloric Restriction in a Life-Long Dog Study. J Proteome Res. 2007;6:1846-1854.
12. Rezzi S, Martin FP, Shanmuganayagam D, Colman RJ, Nicholson JK, Weindruch R. Metabolic shifts due to long-term caloric restriction revealed in nonhuman primates. Exp Gerontol. 2009;44:356-362.
13. Ejsing CS, Sampaio JL, Surendranath V, Duchoslav E, Ekroos K, Klemm RW, Simons K, Shevchenko A. Global analysis of the yeast lipidome by quantitative shotgun mass spectrometry. Proc Natl Acad Sci U S A. 2009;106:2136-2141.
14. Gonzalez-Covarrubias V, Beekman M, Uh HW, Dane A, Troost J, Paliukhovich I, van der Kloet FM, Houwing-Duistermaat J, Vreeken RJ, Hankemeier T, Slagboom EP. Lipidomics of familial longevity. Aging Cell. 2013;12:426-434.
15. Collino S, Montoliu I, Martin FP, Scherer M, Mari D, Salvioli S, Bucci L, Ostan R, Monti D, Biagi E, Brigidi P, Franceschi C, Rezzi S. Metabolic signatures of extreme longevity in northern italian centenarians reveal a complex remodeling of lipids, amino acids, and gut microbiota metabolism. PLoS One. 2013;8:e56564.
16. Cloarec O, Dumas ME, Craig A, Barton RH, Trygg J, Hudson J, Blancher C, Gauguier D, Lindon JC, Holmes E, Nicholson J. Statistical total correlation spectroscopy: an exploratory approach for latent biomarker identification from metabolic 1H NMR data sets. Anal Chem. 2005;77:1282-1289.
17. Passarino G, Calignano C, Vallone A, Franceschi C, Jeune B, Robine JM, Yashin AI, Cavalli Sforza LL, De BG. Male/female ratio in centenarians: a possible role played by population genetic structure. Exp Gerontol. 2002;37:1283-1289.
18. Dejong CH, van de Poll MC, Soeters PB, Jalan R, Olde Damink SW. Aromatic amino acid metabolism during liver failure. J Nutr. 2007;137:1579S-1585S.
19. Dillon EL, Sheffield-Moore M, Paddon-Jones D, Gilkison C, Sanford AP, Casperson SL, Jiang J, Chinkes DL, Urban RJ. Amino acid supplementation increases lean body mass, basal muscle protein synthesis, and insulin-like growth factor-I expression in older women. J Clin Endocrinol Metab. 2009;94:1630-1637.
20. Chen J, Herrup K. Glutamine acts as a neuroprotectant against DNA damage, beta-amyloid and H2O2-induced stress. PLoS One. 2012;7:e33177.
21. Folstein MF, Folstein SE, McHugh PR. "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12:189-198.
22. Magni E, Binetti G, Bianchetti A, Rozzini R, Trabucchi M. Mini-Mental State Examination: a normative study in Italian elderly population. Eur J Neurol. 1996;3:198-202.
23. Franceschi C, Motta L, Valensin S, Rapisarda R, Franzone A, Berardelli M, Motta M, Monti D, Bonafe M, Ferrucci L, Deiana L, Pes GM, Carru C, Desole MS, Barbi C, Sartoni G, Gemelli C, Lescai F, Olivieri F, Marchegiani F, Cardelli M, Cavallone L, Gueresi P, Cossarizza A, Troiano L, Pini G, Sansoni P, Passeri G, Lisa R, Spazzafumo L, Amadio L, Giunta S, Stecconi R, Morresi R, Viticchi C, Mattace R, De BG, Baggio G. Do men and women follow different trajectories to reach extreme longevity? Italian Multicenter Study on Centenarians (IMUSCE). Aging (Milano). 2000;12:77-84.
24. Hubert-Buron A, Leblond J, Jacquot A, Ducrotte P, Dechelotte P, Coeffier M. Glutaminepretreatment reduces IL-8 production in human intestinal epithelial cells by limiting IkappaBalpha ubiquitination. J Nutr.2006;136:1461-1465.
25. Ingram DK, Roth GS. Glycolytic inhibition as a strategy for developing calorie restriction mimetics. Exp Gerontol. 2011;46:148-154.
26. Salvioli S, Monti D, Lanzarini C, Conte M, Pirazzini C, Bacalini MG, Garagnani P, Giuliani C, Fontanesi E, Ostan R, Bucci L, Sevini F, Yani SL, Barbieri A, Lomartire L, Borelli V, Vianello D, Bellavista E, Martucci M, Cevenini E, Pini E, Scurti M, Biondi F, Santoro A, Capri M, Franceschi C. Immune system, cell senescence, aging and longevity--inflamm-aging reappraised. Curr Pharm Des. 2013;19:1675-1679.
27. Grootveld M, Claxson AW, Chander CL, Haycock P, Blake DR, Hawkes GE. High resolution proton NMR investigations of rat blood plasma. Assignment of resonances for the molecularly mobile carbohydrate side-chains of 'acute-phase' glycoproteins. FEBS Lett. 1993;322:266-276.
28. Baumann H, Jahreis GP, Gaines KC. Synthesis and regulation of acute phase plasma proteins in primary cultures of mouse hepatocytes. J Cell Biol. 1983;97:866-876.
29. Wyss M, Kaddurah-Daouk R. Creatine and creatinine metabolism. Physiol Rev. 2000;80:1107-1213.
30. Gey C, Seeger K. Metabolic changes during cellular senescence investigated by proton NMR-spectroscopy. Mech Ageing Dev. 2013;134:130-138.
31. Tang WH, Wang Z, Levison BS, Koeth RA, Britt EB, Fu X, Wu Y, Hazen SL. Intestinal microbial metabolism of phosphatidylcholine and cardiovascular risk. N Engl J Med. 2013;368:1575-1584.
32. Bennett BJ, de Aguiar Vallim TQ, Wang Z, Shih DM, Meng Y, Gregory J, Allayee H, Lee R, Graham M, Crooke R, Edwards PA, Hazen SL, Lusis AJ. Trimethylamine-N-oxide, a metabolite associated with atherosclerosis, exhibits complex genetic and dietary regulation. Cell Metab. 2013;17:49-60.
33. Piccinini M, Scandroglio F, Prioni S, Buccinna B, Loberto N, Aureli M, Chigorno V, Lupino E, DeMarco G, Lomartire A, Rinaudo MT, Sonnino S, Prinetti A. Deregulated sphingolipid metabolism and membrane organization in neurodegenerative disorders. Mol Neurobiol. 2010;41:314-340.
34. Nelson JC, Jiang XC, Tabas I, Tall A, Shea S. Plasma sphingomyelin and subclinical atherosclerosis: findings from the multi-ethnic study of atherosclerosis. Am J Epidemiol. 2006;163:903-912.
35. Holland WL, Summers SA. Sphingolipids, insulin resistance, and metabolic disease: new insights from in vivo manipulation of sphingolipid metabolism. Endocr Rev. 2008;29:381-402.
36. Smith AR, Visioli F, Frei B, Hagen TM. Age-related changes in endothelial nitric oxide synthase phosphorylation and nitric oxide dependent vasodilation: evidence for a novel mechanism involving sphingomyelinase and ceramide-activated phosphatase 2A. Aging Cell. 2006;5:391-400.
37. Schmitz G, Grandl M. Role of redox regulation and lipid rafts in macrophages during Ox-LDL-mediated foam cell formation. Antioxid Redox Signal. 2007;9:1499-1518.
38. Grandl M, Bared SM, Liebisch G, Werner T, Barlage S, Schmitz G. E-LDL and Ox-LDL differentially regulate ceramide and cholesterol raft microdomains in human Macrophages. Cytometry A. 2006;69:189-191.
39. Bismuth J, Lin P, Yao Q, Chen C. Ceramide: a common pathway for atherosclerosis? Atherosclerosis. 2008;196:497-504.
40. Vitale G, Salvioli S, Franceschi C. Oxidative stress and the ageing endocrine system. Nat Rev Endocrinol. 2013;9:228-240.
41. Salvioli S, Monti D, Lanzarini C, Conte M, Pirazzini C, Bacalini MG, Garagnani P, Giuliani C, Fontanesi E, Ostan R, Bucci L, Sevini F, Yani SL, Barbieri A, Lomartire L, Borelli V, Vianello D, Bellavista E, Martucci M, Cevenini E, Pini E, Scurti M, Biondi F, Santoro A, Capri M, Franceschi C. Immune system, cell senescence, aging and longevity--inflamm-aging reappraised. Curr Pharm Des. 2013;19:1675-1679.
42. Wiesner P, Leidl K, Boettcher A, Schmitz G, Liebisch G. Lipid profiling of FPLC-separated lipoprotein fractions by electrospray ionization tandem mass spectrometry. J Lipid Res. 2009;50:574-585.
43. Li Z, Agellon LB, Allen TM, Umeda M, Jewell L, Mason A, Vance DE. The ratio of phosphatidylcholine to phosphatidylethanolamine influences membrane integrity and steatohepatitis. Cell Metab. 2006;3:321-331.
44. Farooqui AA, Ong WY, Horrocks LA. Biochemical aspects of neurodegeneration in human brain: involvement of neural membrane phospholipids and phospholipases A2. Neurochem Res. 2004;29:1961-1977.
45. Rabini RA, Moretti N, Staffolani R, Salvolini E, Nanetti L, Franceschi C, Mazzanti L. Reduced susceptibility to peroxidation of erythrocyte plasma membranes from centenarians. Exp Gerontol. 2002;37:657-663.
46. Maskrey BH, Bermudez-Fajardo A, Morgan AH, Stewart-Jones E, Dioszeghy V, Taylor GW, Baker PR, Coles B, Coffey MJ, Kuhn H, O'Donnell VB. Activated platelets and monocytes generate four hydroxyphosphatidylethanolamines via lipoxygenase. J Biol Chem. 2007;282:20151-20163.
47. van Dieren JM, Simons-Oosterhuis Y, Raatgeep HC, Lindenbergh-Kortleve DJ, Lambers ME, van der Woude CJ, Kuipers EJ, Snoek GT, Potman R, Hammad H, Lambrecht BN, Samsom JN, Nieuwenhuis EE. Anti-inflammatory actions of phosphatidylinositol. Eur J Immunol. 2011;41:1047-1057.
48. Rhee EP, Cheng S, Larson MG, Walford GA, Lewis GD, McCabe E, Yang E, Farrell L, Fox CS, O'Donnell CJ, Carr SA, Vasan RS, Florez JC, Clish CB, Wang TJ, Gerszten RE. Lipid profiling identifies a triacylglycerol signature of insulin resistance and improves diabetes prediction in humans. J Clin Invest. 2011;121:1402-1411.
49. Erion DM, Shulman GI: Diacylglycerol-mediated insulin resistance. Nat Med. 2010;16:400-402.
50. Rezzi S, Ramadan Z, Martin FP, Fay LB, Van BP, Lindon JC, Nicholson JK, Kochhar S. Human metabolic phenotypes link directly to specific dietary preferences in healthyindividuals. J Proteome Res. 2007;6:4469-4477.
51. Siddiqui N, Sim J, Silwood CJ, Toms H, Iles RA, Grootveld M. Multicomponent analysis of encapsulated marine oil supplements using high-resolution 1H and 13C NMR techniques. J Lipid Res. 2003;44:2406-2427.
52. Oostendorp M, Engelke UF, Willemsen MA, Wevers RA. Diagnosing inborn errors of lipid metabolism with proton nuclear magnetic resonance spectroscopy. Clin Chem. 2006;52:1395-1405.
53. Matyash V, Liebisch G, Kurzchalia TV, Shevchenko A, Schwudke D. Lipid extraction by methyl-tert-butyl ether for highthroughput lipidomics. J Lipid Res. 2008;49:1137-1146.
54. Schuhmann K, Herzog R, Schwudke D, Metelmann-Strupat W, Bornstein SR, Shevchenko A. Bottom-up shotgun lipidomics by higher energy collisional dissociation on LTQ Orbitrap mass spectrometers. Anal Chem. 2011;83:5480-5487.
55. Herzog R, Schwudke D, Schuhmann K, Sampaio JL, Bornstein SR, Schroeder M, Shevchenko A. A novel informatics concept for high-throughput shotgun lipidomics based on the molecular fragmentation query language. Genome Biol. 2011;12:R8.