Making heads or tails of mitochondrial membranes in longevity and aging: A role for comparative studies

Longevity and Healthspan

Volumn 3, Issue 1, 2014, Pages

  Valencak, Teresa G ^a,b   Azzu, Vian ^c  

^a UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^b INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^c CHRIST S COLLEGE   (United Kingdom)

Author keywords

Comparative biology; Ectotherm; Endotherm; Fatty acid membrane composition; Longevity; Maximum lifespan; Mitochondria

Indexed keywords

CARDIOLIPIN; FATTY ACID; GLYCEROPHOSPHOLIPID; MITOCHONDRIAL DNA; REACTIVE OXYGEN METABOLITE; SPHINGOLIPID; STEROL;

AGAPORNIS; AGING; ALLOMETRY; APOPTOSIS; BUFO MARINUS; COCKATIEL; COLUMBA LIVIA; COMPARATIVE STUDY; COTURNIX CHINENSIS; COTURNIX JAPONICA; DNA DAMAGE; GENE EXPRESSION; HOMEOSTASIS; LIPID COMPOSITION; LONGEVITY; METABOLIC RATE; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; MUS MUSCULUS; NONHUMAN; OXIDATIVE STRESS; PEROMYSCUS MANICULATUS; PHYLOGENY; POGONA VITTICEPS; PRIORITY JOURNAL; RATTUS NORVEGICUS; REVIEW; SYSTEMATIC REVIEW; TAMIAS;

EID: 84992367521     PISSN: None     EISSN: 20462395     Source Type: Journal    
DOI: 10.1186/2046-2395-3-3     Document Type: Review

References (101)

1. Rubner M: Das Problem der Lebensdauer und seiner Beziehungen zu Wachstum und Ernährung. Munich: Oldenburg; 1908
2. Kleiber M: Body size and metabolism. Hilgardia 1932, 6:315-351
3. Pearl R: The Rate of Living, Being an Account of Some Experimental Studies on the Biology of Life Duration. New York: Alfred A. Knopf; 1928
4. Gerschman R, Gilbert DL, Nye SW, Dwyer P, Fenn WO: Oxygen poisoning and x-irradiation: a mechanism in common. Science 1954, 119:623-626
5. Harman D: Aging: a theory based on free radical and radiation chemistry. J Gerontol 1956, 11:298-300
6. Metchnikoff E: The Prolongation of Life; Optimistic Studies. GP Putnam's Sons: New York, London; 1908
7. Montgomery MK, Hulbert AJ, Buttemer WA: Metabolic rate and membrane fatty acid composition in birds: a comparison between long-living parrots and short-living fowl. J Comp Physiol B 2012, 182:127-137
8. Montgomery MK, Hulbert AJ, Buttemer WA: The long life of birds: the rat-pigeon comparison revisited. PLoS One 2011, 6:e24138
9. Brand MD, Couture P, Else PL, Withers KW, Hulbert AJ: Evolution of energy metabolism. Proton permeability of the inner membrane of liver mitochondria is greater in a mammal than in a reptile. Biochem J 1991, 275(Pt 1):81-86
10. Brookes PS, Buckingham JA, Tenreiro AM, Hulbert AJ, Brand MD: The proton permeability of the inner membrane of liver mitochondria from ectothermic and endothermic vertebrates and from obese rats: correlations with standard metabolic rate and phospholipid fatty acid composition. Comp Biochem Physiol B Biochem Mol Biol 1998, 119:325-334
11. Hulbert AJ, Else PL: Membranes as possible pacemakers of metabolism. J Theor Biol 1999, 199:257-274
12. Hulbert AJ: Life, death and membrane bilayers. J Exp Biol 2003, 206:2303-2311
13. Pamplona R, Barja G, Portero-Otin M: Membrane fatty acid unsaturation, protection against oxidative stress, and maximum life span: a homeoviscous-longevity adaptation? Ann N Y Acad Sci 2002, 959:475-490
14. Hulbert AJ: On the importance of fatty acid composition of membranes for aging. J Theor Biol 2005, 234:277-288
15. Valencak TG, Ruf T: N-3 polyunsaturated fatty acids impair lifespan but have no role for metabolism. Aging Cell 2007, 6:15-25
16. Speakman JR: Body size, energy metabolism and lifespan. J Exp Biol 2005, 208:1717-1730
17. Kowaltowski AJ: Alternative mitochondrial functions in cell physiopathology: beyond ATP production. Braz J Med Biol Res 2000, 33:241-250
18. Lanza IR, Nair KS: Mitochondrial function as a determinant of life span. Pflugers Arch 2010, 459:277-289
19. Barja G, Herrero A: Oxidative damage to mitochondrial DNA is inversely related to maximum life span in the heart and brain of mammals. FASEB J 2000, 14:312-318
20. Daum G: Lipids of mitochondria. Biochim Biophys Acta 1985, 822:1-42
21. Daum G, Vance JE: Import of lipids into mitochondria. Prog Lipid Res 1997, 36:103-130
22. Horvath SE, Daum G: Lipids of mitochondria. Prog Lipid Res 2013, 52:590-614
23. Bottema CK, Parks LW: Sterol analysis of the inner and outer mitochondrial membranes in yeast. Lipids 1980, 15:987-992
24. Petrescu AD, Gallegos AM, Okamura Y, Strauss JF 3rd, Schroeder F: Steroidogenic acute regulatory protein binds cholesterol and modulates mitochondrial membrane sterol domain dynamics. J Biol Chem 2001, 276:36970-36982
25. van den Brink-van der Laan E, Killian JA, de Kruijff B: Nonbilayer lipids affect peripheral and integral membrane proteins via changes in the lateral pressure profile. Biochim Biophys Acta 2004, 1666:275-288
26. Valencak TG, Ruf T: Feeding into old age: long-term effects of dietary fatty acid supplementation on tissue composition and life span in mice. J Comp Physiol B 2011, 181:289-298
27. Couture P, Hulbert AJ: Membrane fatty acid composition of tissues is related to body mass of mammals. J Membr Biol 1995, 148:27-39
28. Porter RK, Brand MD: Cellular oxygen consumption depends on body mass. Am J Physiol 1995, 269:R226-R228
29. Porter RK, Hulbert AJ, Brand MD: Allometry of mitochondrial proton leak: influence of membrane surface area and fatty acid composition. Am J Physiol 1996, 271:R1550-R1560
30. Else PL, Wu BJ: What role for membranes in determining the higher sodium pump molecular activity of mammals compared to ectotherms? J Comp Physiol B 1999, 169:296-302
31. Hazel JR: The effect of temperature acclimation upon succinic dehydrogenase activity from the epaxial muscle of the common goldfish (Carassius auratus L.)-II. Lipid reactivation of the soluble enzyme. Comp Biochem Physiol B 1972, 43:863-882
32. Wodtke E: Temperature adaptation of biological membranes. Compensation of the molar activity of cytochrome c oxidase in the mitochondrial energy-transducing membrane during thermal acclimation of the carp (Cyprinus carpio L.). Biochim Biophys Acta 1981, 640:710-720
33. Hulbert AJ, Else PL: Basal metabolic rate: history, composition, regulation, and usefulness. Physiol Biochem Zool 2004, 77:869-876
34. Clausen T, Van Hardeveld C, Everts ME: Significance of cation transport in control of energy metabolism and thermogenesis. Physiol Rev 1991, 71:733-774
35. Wu BJ, Else PL, Storlien LH, Hulbert AJ: Molecular activity of Na+/K+-ATPase from different sources is related to the packing of membrane lipids. J Exp Biol 2001, 204:4271-4280
36. Mitchell P: Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 1961, 191:144-148
37. Abrahams JP, Leslie AG, Lutter R, Walker JE: Structure at 2.8 Å resolution of F1-ATPase from bovine heart mitochondria. Nature 1994, 370:621-628
38. Wojtczak L, Bogucka K, Duszynski J, Zablocka B, Zolkiewska A: Regulation of mitochondrial resting state respiration: slip, leak, heterogeneity? Biochim Biophys Acta 1990, 1018:177-181
39. Azzu V, Brand MD: The on-off switches of the mitochondrial uncoupling proteins. Trends Biochem Sci 2010, 35:298-307
40. Brookes PS, Hulbert AJ, Brand MD: The proton permeability of liposomes made from mitochondrial inner membrane phospholipids: no effect of fatty acid composition. Biochim Biophys Acta 1997, 1330:157-164
41. Brookes PS, Rolfe DF, Brand MD: The proton permeability of liposomes made from mitochondrial inner membrane phospholipids: comparison with isolated mitochondria. J Membr Biol 1997, 155:167-174
42. Beck V, Jaburek M, Demina T, Rupprecht A, Porter RK, Jezek P, Pohl EE: Polyunsaturated fatty acids activate human uncoupling proteins 1 and 2 in planar lipid bilayers. FASEB J 2007, 21:1137-1144
43. Murphy MP, Echtay KS, Blaikie FH, Asin-Cayuela J, Cocheme HM, Green K, Buckingham JA, Taylor ER, Hurrell F, Hughes G, Miwa S, Cooper CE, Svistunenko DA, Smith RA, Brand MD: Superoxide activates uncoupling proteins by generating carbon-centered radicals and initiating lipid peroxidation: studies using a mitochondria-targeted spin trap derived from alpha-phenyl-N-tert-butylnitrone. J Biol Chem 2003, 278:48534-48545
44. Brand MD: Uncoupling to survive? The role of mitochondrial inefficiency in ageing. Exp Gerontol 2000, 35:811-820
45. 2 production of heart mitochondria and aging rate are slower in canaries and parakeets than in mice: sites of free radical generation and mechanisms involved. Mech Ageing Dev 1998, 103:133-146
46. Bevilacqua L, Ramsey JJ, Hagopian K, Weindruch R, Harper ME: Long-term caloric restriction increases UCP3 content but decreases proton leak and reactive oxygen species production in rat skeletal muscle mitochondria. Am J Physiol Endocrinol Metab 2005, 289:E429-E438
47. 2 production in liver. Comp Biochem Physiol B Biochem Mol Biol 2005, 140:99-108
48. Mookerjee SA, Divakaruni AS, Jastroch M, Brand MD: Mitochondrial uncoupling and lifespan. Mech Ageing Dev 2010, 131:463-472
49. Pamplona R, Prat J, Cadenas S, Rojas C, Perez-Campo R, Lopez Torres M, Barja G: Low fatty acid unsaturation protects against lipid peroxidation in liver mitochondria from long-lived species: the pigeon and human case. Mech Ageing Dev 1996, 86:53-66
50. Pamplona R, Portero-Otin M, Ruiz C, Gredilla R, Herrero A, Barja G: Double bond content of phospholipids and lipid peroxidation negatively correlate with maximum longevity in the heart of mammals. Mech Ageing Dev 2000, 112:169-183
51. AnAge database. http://genomics.senescence.info/species
52. Hulbert AJ, Turner N, Hinde J, Else P, Guderley H: How might you compare mitochondria from different tissues and different species? J Comp Physiol B 2006, 176:93-105
53. Geiser F: Influence of polyunsaturated and saturated dietary lipids on adipose tissue, brain and mitochondrial membrane fatty acid composition of a mammalian hibernator. Biochim Biophys Acta 1990, 1046:159-166
54. Valencak TG, Ruf T: Phospholipid composition and longevity: lessons from Ames dwarf mice. Age (Dordr) 2013, 35:2303-2313
55. Geiser F: The effect of unsaturated and saturated dietary lipids on the pattern of daily torpor and the fatty acid composition of tissues and membranes of the deer mouse Peromyscus maniculatus. J Comp Physiol B 1991, 161:590-597
56. Winczura A, Zdzalik D, Tudek B: Damage of DNA and proteins by major lipid peroxidation products in genome stability. Free Radic Res 2012, 46:442-459
57. Pamplona R, Portero-Otin M, Riba D, Ruiz C, Prat J, Bellmunt MJ, Barja G: Mitochondrial membrane peroxidizability index is inversely related to maximum life span in mammals. J Lipid Res 1998, 39:1989-1994
58. DeLany JP, Windhauser MM, Champagne CM, Bray GA: Differential oxidation of individual dietary fatty acids in humans. Am J Clin Nutr 2000, 72:905-911
59. Esterbauer H, Schaur RJ, Zollner H: Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 1991, 11:81-128
60. Richard D, Kefi K, Barbe U, Bausero P, Visioli F: Polyunsaturated fatty acids as antioxidants. Pharmacol Res 2008, 57:451-455
61. Andziak B, O'Connor TP, Qi W, DeWaal EM, Pierce A, Chaudhuri AR, Van Remmen H, Buffenstein R: High oxidative damage levels in the longestliving rodent, the naked mole-rat. Aging Cell 2006, 5:463-471
62. Andziak B, Buffenstein R: Disparate patterns of age-related changes in lipid peroxidation in long-lived naked mole-rats and shorter-lived mice. Aging Cell 2006, 5:525-532
63. Buffenstein R: The naked mole-rat: a new long-living model for human aging research. J Gerontol A Biol Sci Med Sci 2005, 60:1369-1377
64. Lambert AJ, Boysen HM, Buckingham JA, Yang T, Podlutsky A, Austad SN, Kunz TH, Buffenstein R, Brand MD: Low rates of hydrogen peroxide production by isolated heart mitochondria associate with long maximum lifespan in vertebrate homeotherms. Aging Cell 2007, 6:607-618
65. Mitchell TW, Buffenstein R, Hulbert AJ: Membrane phospholipid composition may contribute to exceptional longevity of the naked mole-rat (Heterocephalus glaber): a comparative study using shotgun lipidomics. Exp Gerontol 2007, 42:1053-1062
66. Brosche T, Platt D: The biological significance of plasmalogens in defense against oxidative damage. Exp Gerontol 1998, 33:363-369
67. Zoeller RA, Morand OH, Raetz CR: A possible role for plasmalogens in protecting animal cells against photosensitized killing. J Biol Chem 1988, 263:11590-11596
68. Schmid PC, Deli E, Schmid HH: Generation and remodeling of phospholipid molecular species in rat hepatocytes. Arch Biochem Biophys 1995, 319:168-176
69. Frank CL: The influence of dietary fatty acids on hibernation by golden-mantled ground squirrels (Spermophilus lateralis). Physiol Zool 1992, 65:906-920
70. Geiser F, Baudinette RV: The daily torpor and thermoregulation in the small dasyurid marsupials Planigale gilesi and Ningaui yvonneae. Aust J Zool 1988, 36:473-481
71. Geiser F, Kenagy GJ: Polyunsaturated lipid diet lengthens torpor and reduces body temperature in a hibernator. Am J Physiol 1987, 252:R897-R901
72. Aloia RC: Lipid, fluidity, and functional studies of the membranes of hibernating mammals. In Advances in Membrane Fluidity. Edited by Aloia RC, Curtain CC, Gordon LM. New York: Alan R Liss; 1988:1-39
73. Paradies G, Ruggiero FM, Dinoi P, Petrosillo G, Quagliariello E: Decreased cytochrome oxidase activity and changes in phospholipids in heart mitochondria from hypothyroid rats. Arch Biochem Biophys 1993, 307:91-95
74. Ruf T, Arnold W: Effects of polyunsaturated fatty acids on hibernation and torpor: a review and hypothesis. Am J Physiol Regul Integr Comp Physiol 2008, 294:R1044-R1052
75. Gerson AR, Brown JC, Thomas R, Bernards MA, Staples JF: Effects of dietary polyunsaturated fatty acids on mitochondrial metabolism in mammalian hibernation. J Exp Biol 2008, 211:2689-2699
76. Brown JC, Chung DJ, Belgrave KR, Staples JF: Mitochondrial metabolic suppression and reactive oxygen species production in liver and skeletal muscle of hibernating thirteen-lined ground squirrels. Am J Physiol Regul Integr Comp Physiol 2012, 302:R15-R28
77. Price ER, Valencak TG: Changes in fatty acid composition during starvation in vertebrates: mechanisms and questions. In Comparative Physiology of Fasting, Starvation, and Food Limitation. New York, Dordrecht, London: Springer Heidelberg; 2012:237-255. ISBN 978-3-642-29055-8 doi:10.1007/978-3-642-29056-5
78. Schlame M, Brody S, Hostetler KY: Mitochondrial cardiolipin in diverse eukaryotes. Comparison of biosynthetic reactions and molecular acyl species. Eur J Biochem 1993, 212:727-735
79. Pfeiffer K, Gohil V, Stuart RA, Hunte C, Brandt U, Greenberg ML, Schagger H: Cardiolipin stabilizes respiratory chain supercomplexes. J Biol Chem 2003, 278:52873-52880
80. Pebay-Peyroula E, Dahout-Gonzalez C, Kahn R, Trezeguet V, Lauquin GJ, Brandolin G: Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside. Nature 2003, 426:39-44
81. Claypool SM, Oktay Y, Boontheung P, Loo JA, Koehler CM: Cardiolipin defines the interactome of the major ADP/ATP carrier protein of the mitochondrial inner membrane. J Cell Biol 2008, 182:937-950
82. Osman C, Voelker DR, Langer T: Making heads or tails of phospholipids in mitochondria. J Cell Biol 2011, 192:7-16
83. Gonzalvez F, Schug ZT, Houtkooper RH, MacKenzie ED, Brooks DG, Wanders RJ, Petit PX, Vaz FM, Gottlieb E: Cardiolipin provides an essential activating platform for caspase-8 on mitochondria. J Cell Biol 2008, 183:681-696
84. Choi SY, Gonzalvez F, Jenkins GM, Slomianny C, Chretien D, Arnoult D, Petit PX, Frohman MA: Cardiolipin deficiency releases cytochrome c from the inner mitochondrial membrane and accelerates stimuli-elicited apoptosis. Cell Death Differ 2007, 14:597-606
85. Paradies G, Paradies V, Ruggiero FM, Petrosillo G: Changes in the mitochondrial permeability transition pore in aging and age-associated diseases. Mech Ageing Dev 2013, 134:1-9
86. Petrosillo G, De Benedictis V, Ruggiero FM, Paradies G: Decline in cytochrome c oxidase activity in rat-brain mitochondria with aging. Role of peroxidized cardiolipin and beneficial effect of melatonin. J Bioenerg Biomembr 2013, 45:431-440
87. Zhou J, Zhong Q, Li G, Greenberg ML: Loss of cardiolipin leads to longevity defects that are alleviated by alterations in stress response signaling. J Biol Chem 2009, 284:18106-18114
88. Gruber J, Ng LF, Fong S, Wong YT, Koh SA, Chen CB, Shui G, Cheong WF, Schaffer S, Wenk MR, Halliwell B: Mitochondrial changes in ageing Caenorhabditis elegans-what do we learn from superoxide dismutase knockouts? PLoS One 2011, 6:e19444
89. Lee HJ, Mayette J, Rapoport SI, Bazinet RP: Selective remodeling of cardiolipin fatty acids in the aged rat heart. Lipids Health Dis 2006, 5:2
90. Jobson RW, Nabholz B, Galtier N: An evolutionary genome scan for longevity-related natural selection in mammals. Mol Biol Evol 2010, 27:840-847
91. Speakman JR: Correlations between physiology and lifespan-two widely ignored problems with comparative studies. Aging Cell 2005, 4:167-175
92. R project. www.R-project.org
93. Felsenstein J: Phylogenies and the comparative method. Am Nat 1985, 125:1-15
94. Sohal RS, Weindruch R: Oxidative stress, caloric restriction, and aging. Science 1996, 273:59-63
95. Lambert AJ, Portero-Otin M, Pamplona R, Merry BJ: Effect of ageing and caloric restriction on specific markers of protein oxidative damage and membrane peroxidizability in rat liver mitochondria. Mech Ageing Dev 2004, 125:529-538
96. Faulks SC, Turner N, Else PL, Hulbert AJ: Calorie restriction in mice: effects on body composition, daily activity, metabolic rate, mitochondrial reactive oxygen species production, and membrane fatty acid composition. J Gerontol A Biol Sci Med Sci 2006, 61:781-794
97. Shmookler Reis RJ, Xu L, Lee H, Chae M, Thaden JJ, Bharill P, Tazearslan C, Siegel E, Alla R, Zimniak P, Ayyadevara S: Modulation of lipid biosynthesis contributes to stress resistance and longevity of C. elegans mutants. Aging (Albany NY) 2011, 3:125-147
98. Abbott SK, Else PL, Atkins TA, Hulbert AJ: Fatty acid composition of membrane bilayers: importance of diet polyunsaturated fat balance. Biochim Biophys Acta 1818, 2012:1309-1317
99. Hu FB, Willett WC: Optimal diets for prevention of coronary heart disease. JAMA 2002, 288:2569-2578
100. Hu FB, Stampfer MJ, Manson JE, Ascherio A, Colditz GA, Speizer FE, Hennekens CH, Willett WC: Dietary saturated fats and their food sources in relation to the risk of coronary heart disease in women. Am J Clin Nutr 1999, 70:1001-1008
101. Wilson PW: Established risk factors and coronary artery disease: the Framingham study. Am J Hypertens 1994, 7:7S-12S