Metabolic Signatures of Extreme Longevity in Northern Italian Centenarians Reveal a Complex Remodeling of Lipids, Amino Acids, and Gut Microbiota Metabolism

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Collino, Sebastiano ^a   Montoliu, Ivan ^a   Martin, François Pierre J ^a   Scherer, Max ^a   Mari, Daniela ^b,c   Salvioli, Stefano ^d   Bucci, Laura ^d   Ostan, Rita ^d   Monti, Daniela ^e   Biagi, Elena ^d   Brigidi, Patrizia ^d   Franceschi, Claudio ^d   Rezzi, Serge ^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)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ARACHIDONIC ACID; CYTOCHROME P450; GLYCEROPHOSPHOLIPID; LINOLEIC ACID; LIPID; LIPIDOME; SPHINGOLIPID; TRYPTOPHAN;

ADULT; AGED; AGING; ARTICLE; BACTERIAL CELL; CENTENARIAN; COHORT ANALYSIS; CONTROLLED STUDY; DETOXIFICATION; ENZYME ACTIVITY; ETHNIC GROUP; FEMALE; HUMAN; INFLAMMATION; INTESTINE FLORA; ITALIAN; LIPID BLOOD LEVEL; LIPID PEROXIDATION; LONGEVITY; MALE; MASS SPECTROMETRY; METABOLOMICS; METABONOMICS; MICROBIAL METABOLISM; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PROTEIN ASSEMBLY; PROTON NUCLEAR MAGNETIC RESONANCE;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; AMINO ACIDS; BIOLOGICAL MARKERS; CHILD; CHROMATOGRAPHY, LIQUID; COHORT STUDIES; DEMOGRAPHY; EICOSANOIDS; FEMALE; GASTROINTESTINAL TRACT; HUMANS; ITALY; LIPID METABOLISM; LONGEVITY; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MASS SPECTROMETRY; METABOLOME; METABOLOMICS; METAGENOME; MIDDLE AGED; PHENOTYPE; YOUNG ADULT;

EID: 84874593878     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0056564     Document Type: Article

References (61)

1. Weinert BT, Timiras PS, (2003) Invited review: Theories of aging. J Appl Physiol 95: 1706-1716.
2. De BG, Carotenuto L, Carrieri G, De LM, Falcone E, et al. (1998) Gene/longevity association studies at four autosomal loci (REN, THO, PARP, SOD2). Eur J Hum Genet 6: 534-541.
3. Radak Z, Zhao Z, Goto S, Koltai E, (2011) Age-associated neurodegeneration andoxidative damage to lipids, proteins and DNA. Mol Aspects Med 32: 305-315.
4. Xue H, Xian B, Dong D, Xia K, Zhu S, et al. (2007) A modular network model of aging. Mol Syst Biol 3: 147.
5. Sansoni P, Vescovini R, Fagnoni F, Biasini C, Zanni F, et al. (2008) The immune system in extreme longevity. Exp Gerontol 43: 61-65.
6. Franceschi C, (2007) Inflammaging as a major characteristic of old people: can it be prevented or cured? Nutr Rev 65: S173-S176.
7. Burkle A, Caselli G, Franceschi C, Mariani E, Sansoni P, et al. (2007) Pathophysiology of ageing, longevity and age related diseases. Immun Ageing 4: 4.
8. Li M, Wang B, Zhang M, Rantalainen M, Wang S, et al. (2008) Symbiotic gut microbes modulate human metabolic phenotypes. Proc Natl Acad Sci U S A 105: 2117-2122.
9. Wijeyesekera A, Selman C, Barton RH, Holmes E, Nicholson JK, et al. (2012) Metabotyping of Long-Lived Mice using (1)H NMR Spectroscopy. J Proteome Res 11: 2224-2235.
10. Wang Y, Lawler D, Larson B, Ramadan Z, Kochhar S, et al. (2007) Metabonomic Investigations of Aging and Caloric Restriction in a Life-Long Dog Study. J Proteome Res 6: 1846-1854.
11. Rezzi S, Martin FP, Shanmuganayagam D, Colman RJ, Nicholson JK, et al. (2009) Metabolic shifts due to long-term caloric restriction revealed in nonhuman primates. Exp Gerontol 44: 356-362.
12. Passarino G, Calignano C, Vallone A, Franceschi C, Jeune B, et al. (2002) Male/female ratio in centenarians: a possible role played by population genetic structure. Exp Gerontol 37: 1283-1289.
13. Cevenini E, Invidia L, Lescai F, Salvioli S, Tieri P, et al. (2008) Human models of aging and longevity. Expert Opin Biol Ther 8: 1393-1405.
14. Atzmon G, Rincon M, Rabizadeh P, Barzilai N, (2005) Biological evidence for inheritance of exceptional longevity. Mech Ageing Dev 126: 341-345.
15. Patterson D, Cabelof DC, (2011) Down syndrome as a model of DNA polymerase beta haploinsufficiency and accelerated aging. Mech Ageing Dev.
16. Biagi E, Nylund L, Candela M, Ostan R, Bucci L, et al. (2010) Through ageing, and beyond: gut microbiota and inflammatory status in seniors and centenarians. PLoS One 5: e10667.
17. Baur P, Martin FP, Gruber L, Bosco N, Brahmbhatt V, et al. (2011) Metabolic Phenotyping of the Crohn's Disease-like IBD Etiopathology in the TNF(DeltaARE/WT) Mouse Model. J Proteome Res.
18. Deems R, Buczynski MW, Bowers-Gentry R, Harkewicz R, Dennis EA, (2007) Detection and quantitation of eicosanoids via high performance liquid chromatography electrospray ionization-mass spectrometry. Methods Enzymol 432: 59-82.
19. Cloarec O, Dumas ME, Craig A, Barton RH, Trygg J, et al. (2005) Statistical total correlation spectroscopy: an exploratory approach for latent biomarker identification from metabolic 1H NMR data sets. Anal Chem 77: 1282-1289.
20. Liaw A, Wiener M, (2002) Classification and regression by randomForest. R News 3: 18-22.
21. Magni E, Binetti G, Bianchetti A, Rozzini R, Trabucchi M, (1996) Mini-Mental State Examination: a normative study in Italian elderly population. Eur J Neurol 3: 198-202.
22. Byrne GI, Lehmann LK, Kirschbaum JG, Borden EC, Lee CM, et al. (1986) Induction of tryptophan degradation in vitro and in vivo: a gamma-interferon-stimulated activity. J Interferon Res 6: 389-396.
23. Gupta NK, Thaker AI, Kanuri N, Riehl TE, Rowley CW, et al. (2011) Serum analysis of tryptophan catabolism pathway: Correlation with Crohn's disease activity. Inflamm Bowel Dis.
24. Huang A, Fuchs D, Widner B, Glover C, Henderson DC, et al. (2002) Serum tryptophan decrease correlates with immune activation and impaired quality of life in colorectal cancer. Br J Cancer 86: 1691-1696.
25. Aiyar N, Disa J, Ao Z, Ju H, Nerurkar S, et al. (2007) Lysophosphatidylcholine induces inflammatory activation of human coronary artery smooth muscle cells. Mol Cell Biochem 295: 113-120.
26. Schmitz G, Ruebsaamen K, (2010) Metabolism and atherogenic disease association of lysophosphatidylcholine. Atherosclerosis 208: 10-18.
27. Fuchs B, Schiller J, Wagner U, Hantzschel H, Arnold K, (2005) The phosphatidylcholine/lysophosphatidylcholine ratio in human plasma is an indicator of the severity of rheumatoid arthritis: investigations by 31P NMR and MALDI-TOF MS. Clin Biochem 38: 925-933.
28. Wijeyesekera A, Selman C, Barton RH, Holmes E, Nicholson JK, et al. (2012) Metabotyping of long-lived mice using 1H NMR spectroscopy. J Proteome Res 11: 2224-2235.
29. Perls TT, Wilmoth J, Levenson R, Drinkwater M, Cohen M, et al. (2002) Life-long sustained mortality advantage of siblings of centenarians. Proc Natl Acad Sci U S A 99: 8442-8447.
30. Suliman ME, Qureshi AR, Stenvinkel P, Pecoits-Filho R, Barany P, et al. (2005) Inflammation contributes to low plasma amino acid concentrations in patients with chronic kidney disease. Am J Clin Nutr 82: 342-349.
31. Dillon EL, Sheffield-Moore M, Paddon-Jones D, Gilkison C, Sanford AP, et al. (2009) 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 94: 1630-1637.
32. Kummerow FA, Cook LS, Wasowicz E, Jelen H, (2001) Changes in the phospholipid composition of the arterial cell can result in severe atherosclerotic lesions. J Nutr Biochem 12: 602-607.
33. Yeboah J, McNamara C, Jiang XC, Tabas I, Herrington DM, et al. (2010) Association of plasma sphingomyelin levels and incident coronary heart disease events in an adult population: Multi-Ethnic Study of Atherosclerosis. Arterioscler Thromb Vasc Biol 30: 628-633.
34. Nagan N, Zoeller RA, (2001) Plasmalogens: biosynthesis and functions. Prog Lipid Res 40: 199-229.
35. Pereira SP, Cassell TB, Engelman JL, Sladen GE, Murphy GM, et al. (1996) Plasma arachidonic acid-rich phospholipids in Crohn's disease: response to treatment. Clin Sci (Lond) 91: 509-512.
36. Hsieh CC, Papaconstantinou J, (2004) Akt/PKB and p38 MAPK signaling, translational initiation and longevity in Snell dwarf mouse livers. Mech Ageing Dev 125: 785-798.
37. Laplante M, Sabatini DM, (2009) An emerging role of mTOR in lipid biosynthesis. Curr Biol 19: R1046-R1052.
38. Schieke SM, Finkel T, (2007) TOR and aging: less is more. Cell Metab 5: 233-235.
39. Sharp ZD, Strong R, (2010) The role of mTOR signaling in controlling mammalian life span: what a fungicide teaches us about longevity. J Gerontol A Biol Sci Med Sci 65: 580-589.
40. Maeba R, Maeda T, Kinoshita M, Takao K, Takenaka H, et al. (2007) Plasmalogens in human serum positively correlate with high- density lipoprotein and decrease with aging. J Atheroscler Thromb 14: 12-18.
41. Radmark O, (2003) 5-lipoxygenase-derived leukotrienes: mediators also of atherosclerotic inflammation. Arterioscler Thromb Vasc Biol 23: 1140-1142.
42. Takata S, Papayianni A, Matsubara M, Jimenez W, Pronovost PH, et al. (1994) 15-Hydroxyeicosatetraenoic acid inhibits neutrophil migration across cytokine-activated endothelium. Am J Pathol 145: 541-549.
43. Seubert JM, Zeldin DC, Nithipatikom K, Gross GJ, (2007) Role of epoxyeicosatrienoic acids in protecting the myocardium following ischemia/reperfusion injury. Prostaglandins Other Lipid Mediat 82: 50-59.
44. Campbell WB, (2000) New role for epoxyeicosatrienoic acids as anti-inflammatory mediators. Trends Pharmacol Sci 21: 125-127.
45. Jira W, Spiteller G, Richter A, (1997) Increased levels of lipid oxidation products in low density lipoproteins of patients suffering from rheumatoid arthritis. Chem Phys Lipids 87: 81-89.
46. Gaskins AJ, Rovner AJ, Mumford SL, Yeung E, Browne RW, et al. (2010) Adherence to a Mediterranean diet and plasma concentrations of lipid peroxidation in premenopausal women. Am J Clin Nutr 92: 1461-1467.
47. Jira W, Spiteller G, Richter A, (1997) Increased levels of lipid oxidation products in low density lipoproteins of patients suffering from rheumatoid arthritis. Chem Phys Lipids 87: 81-89.
48. Jira W, Spiteller G, Carson W, Schramm A, (1998) Strong increase in hydroxy fatty acids derived from linoleic acid in human low density lipoproteins of atherosclerotic patients. Chem Phys Lipids 91: 1-11.
49. Davinelli S, Willcox DC, Scapagnini G, (2012) Extending healthy ageing: nutrient sensitive pathway and centenarian population. Immun Ageing 9: 9.
50. Calder PC, (2008) Polyunsaturated fatty acids, inflammatory processes and inflammatory bowel diseases. Mol Nutr Food Res 52: 885-897.
51. Guigoz Y, Dore J, Schiffrin EJ, (2008) The inflammatory status of old age can be nurtured from the intestinal environment. Curr Opin Clin Nutr Metab Care 11: 13-20.
52. Claesson MJ, Cusack S, O'Sullivan O, Greene-Diniz R, de WH, et al. (2011) Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proc Natl Acad Sci U S A 108 Suppl 1: 4586-4591.
53. Clayton TA, Baker D, Lindon JC, Everett JR, Nicholson JK, (2009) Pharmacometabonomic identification of a significant host-microbiome metabolic interaction affecting human drug metabolism. Proc Natl Acad Sci U S A 106: 14728-14733.
54. Smith EA, Macfarlane GT, (1997) Formation of Phenolic and Indolic Compounds by Anaerobic Bacteria in the Human Large Intestine. Microb Ecol 33: 180-188.
55. Xu XM, Sansores-Garcia L, Chen XM, Matijevic-Aleksic N, Du M, et al. (1999) Suppression of inducible cyclooxygenase 2 gene transcription by aspirin and sodium salicylate. Proc Natl Acad Sci U S A 96: 5292-5297.
56. Elsden SR, Hilton MG, Waller JM, (1976) The end products of the metabolism of aromatic amino acids by Clostridia. Arch Microbiol 107: 283-288.
57. Baumgart M, Dogan B, Rishniw M, Weitzman G, Bosworth B, et al. (2007) Culture independent analysis of ileal mucosa reveals a selective increase in invasive Escherichia coli of novel phylogeny relative to depletion of Clostridiales in Crohn's disease involving the ileum. ISME J 1: 403-418.
58. Peng L, He Z, Chen W, Holzman IR, Lin J, (2007) Effects of butyrate on intestinal barrier function in a Caco-2 cell monolayer model of intestinal barrier. Pediatr Res 61: 37-41.
59. Oostendorp M, Engelke UF, Willemsen MA, Wevers RA, (2006) Diagnosing inborn errors of lipid metabolism with proton nuclear magnetic resonance spectroscopy. Clin Chem 52: 1395-1405.
60. Rezzi S, Ramadan Z, Martin FP, Fay LB, Van BP, et al. (2007a) Human metabolic phenotypes link directly to specific dietary preferences in healthy individuals. J Proteome Res 6: 4469-4477.
61. Siddiqui N, Sim J, Silwood CJ, Toms H, Iles RA, et al. (2003) Multicomponent analysis of encapsulated marine oil supplements using high-resolution 1H and 13C NMR techniques. J Lipid Res 44: 2406-2427.