Looking Beyond Structure: Membrane Phospholipids of Skeletal Muscle Mitochondria

Trends in Endocrinology and Metabolism

Volumn 27, Issue 8, 2016, Pages 553-562

  Heden, Timothy D ^a   Neufer, P Darrell ^a,b   Funai, Katsuhiko ^a,b  

^a EAST CAROLINA UNIVERSITY   (United States)

^b EAST CAROLINA UNIVERSITY   (United States)

Author keywords

aerobic capacity.; membrane phospholipids; mitochondria; phospholipid biosynthesis; skeletal muscle

Indexed keywords

CARDIOLIPIN; MEMBRANE PHOSPHOLIPID; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLINOSITOL; PHOSPHOLIPID; MEMBRANE LIPID;

AEROBIC CAPACITY; AEROBIC METABOLISM; DIET; EXERCISE; HUMAN; LIPID COMPOSITION; LIPOGENESIS; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; MUSCLE MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SKELETAL MUSCLE; SKELETAL MUSCLE CELL; ANIMAL; METABOLISM;

ANIMALS; HUMANS; MEMBRANE LIPIDS; MITOCHONDRIA, MUSCLE; MITOCHONDRIAL MEMBRANES; MUSCLE, SKELETAL; PHOSPHOLIPIDS;

EID: 84979687694     PISSN: 10432760     EISSN: 18793061     Source Type: Journal    
DOI: 10.1016/j.tem.2016.05.007     Document Type: Review

References (80)

1. 1 Myers, J., et al. Exercise capacity and mortality among men referred for exercise testing. N. Engl. J. Med. 346 (2002), 793–801.
2. 2 Wisloff, U., et al. Cardiovascular risk factors emerge after artificial selection for low aerobic capacity. Science 307 (2005), 418–420.
3. 3 Zurlo, F., et al. Skeletal muscle metabolism is a major determinant of resting energy expenditure. J. Clin. Invest. 86 (1990), 1423–1427.
4. 4 Muoio, D.M., Neufer, P.D., Lipid-induced mitochondrial stress and insulin action in muscle. Cell Metab. 15 (2012), 595–605.
5. 5 Carter, H.N., et al. Mitochondria, muscle health, and exercise with advancing age. Physiology 30 (2015), 208–223.
6. 6 Holloszy, J.O., Biochemical adaptations in muscle. Effects of exercise on mitochondrial oxygen uptake and respiratory enzyme activity in skeletal muscle. J. Biol. Chem. 242 (1967), 2278–2282.
7. 7 Hancock, C.R., et al. High-fat diets cause insulin resistance despite an increase in muscle mitochondria. Proc. Natl. Acad. Sci. U.S.A. 105 (2008), 7815–7820.
8. 8 Henriksson, J., Reitman, J.S., Time course of changes in human skeletal muscle succinate dehydrogenase and cytochrome oxidase activities and maximal oxygen uptake with physical activity and inactivity. Acta Physiol. Scand. 99 (1977), 91–97.
9. 9 Mejia, E.M., Hatch, G.M., Mitochondrial phospholipids: role in mitochondrial function. J. Bioenerg. Biomembr. 48 (2015), 99–112.
10. 10 Stefanyk, L.E., et al. Skeletal muscle type comparison of subsarcolemmal mitochondrial membrane phospholipid fatty acid composition in rat. J. Membr. Biol. 234 (2010), 207–215.
11. 11 Tsalouhidou, S., et al. Mitochondrial phospholipids of rat skeletal muscle are less polyunsaturated than whole tissue phospholipids: implications for protection against oxidative stress. J. Anim. Sci. 84 (2006), 2818–2825.
12. 12 Daum, G., Lipids of mitochondria. Biochim. Biophys. Acta. 822 (1985), 1–42.
13. 13 Daum, G., Vance, J.E., Import of lipids into mitochondria. Prog. Lipid Res. 36 (1997), 103–130.
14. 14 Kennedy, E.P., Weiss, S.B., The function of cytidine coenzymes in the biosynthesis of phospholipides. J. Biol. Chem. 222 (1956), 193–214.
15. 15 Vance, D.E., Vance, J.E., Physiological consequences of disruption of mammalian phospholipid biosynthetic genes. J. Lipid Res. 50:Suppl. (2009), S132–S137.
16. 16 Arikketh, D., et al. Defining the importance of phosphatidylserine synthase-1 (PSS1): unexpected viability of PSS1-deficient mice. J. Biol. Chem. 283 (2008), 12888–12897.
17. 17 Sousa, S.B., et al. Gain-of-function mutations in the phosphatidylserine synthase 1 (PTDSS1) gene cause Lenz–Majewski syndrome. Nat. Genet. 46 (2014), 70–76.
18. 18 Hishikawa, D., et al. Discovery of a lysophospholipid acyltransferase family essential for membrane asymmetry and diversity. Proc. Natl. Acad. Sci. U.S.A. 105 (2008), 2830–2835.
19. 19 Horvath, S.E., Daum, G., Lipids of mitochondria. Prog. Lipid Res. 52 (2013), 590–614.
20. 20 Vance, J.E., MAM (mitochondria-associated membranes) in mammalian cells: lipids and beyond. Biochim. Biophys. Acta. 1841 (2014), 595–609.
21. 21 Michel, V., et al. The impact of choline availability on muscle lipid metabolism. Food Funct. 2 (2011), 53–62.
22. 22 da Costa, K.A., et al. Elevated serum creatine phosphokinase in choline-deficient humans: mechanistic studies in C2C12 mouse myoblasts. Am. J. Clin. Nutr. 80 (2004), 163–170.
23. 23 Wu, G., et al. Early embryonic lethality caused by disruption of the gene for choline kinase alpha, the first enzyme in phosphatidylcholine biosynthesis. J. Biol. Chem. 283 (2008), 1456–1462.
24. 24 Wu, G., et al. Understanding the muscular dystrophy caused by deletion of choline kinase beta in mice. Biochim. Biophys. Acta. 1791 (2009), 347–356.
25. 25 Sher, R.B., et al. A rostrocaudal muscular dystrophy caused by a defect in choline kinase beta, the first enzyme in phosphatidylcholine biosynthesis. J. Biol. Chem. 281 (2006), 4938–4948.
26. 26 Mitsuhashi, S., et al. Muscle choline kinase beta defect causes mitochondrial dysfunction and increased mitophagy. Hum. Mol. Genet. 20 (2011), 3841–3851.
27. 27 Wang, L., et al. Early embryonic lethality in mice with targeted deletion of the CTP:phosphocholine cytidylyltransferase alpha gene (Pcyt1a). Mol. Cell. Biol. 25 (2005), 3357–3363.
28. 28 Jackowski, S., et al. Disruption of CCTbeta2 expression leads to gonadal dysfunction. Mol. Cell. Biol. 24 (2004), 4720–4733.
29. 29 Shaikh, S.R., et al. Increasing mitochondrial membrane phospholipid content lowers the enzymatic activity of electron transport complexes. Biochemistry 53 (2014), 5589–5591.
30. 30 Steenbergen, R., et al. Disruption of the phosphatidylserine decarboxylase gene in mice causes embryonic lethality and mitochondrial defects. J. Biol. Chem. 280 (2005), 40032–40040.
31. 31 Bergo, M.O., et al. Defining the importance of phosphatidylserine synthase 2 in mice. J. Biol. Chem. 277 (2002), 47701–47708.
32. 32 Shiao, Y.J., et al. Evidence that phosphatidylserine is imported into mitochondria via a mitochondria-associated membrane and that the majority of mitochondrial phosphatidylethanolamine is derived from decarboxylation of phosphatidylserine. J. Biol. Chem. 270 (1995), 11190–11198.
33. 33 Tasseva, G., et al. Phosphatidylethanolamine deficiency in Mammalian mitochondria impairs oxidative phosphorylation and alters mitochondrial morphology. J. Biol. Chem. 288 (2013), 4158–4173.
34. 34 Fullerton, M.D., et al. Developmental and metabolic effects of disruption of the mouse CTP:phosphoethanolamine cytidylyltransferase gene (Pcyt2). Mol. Cell. Biol. 27 (2007), 3327–3336.
35. 35 Selathurai, A., et al. The CDP-ethanolamine pathway regulates skeletal muscle diacylglycerol content and mitochondrial biogenesis without altering insulin sensitivity. Cell Metab. 21 (2015), 718–730.
36. 36 Funai, K., et al. Skeletal muscle phospholipid Metabolism regulates insulin sensitivity and contractile function. Diabetes 65 (2016), 358–370.
37. 37 Cao, J., et al. A novel cardiolipin-remodeling pathway revealed by a gene encoding an endoplasmic reticulum-associated acyl-CoA:lysocardiolipin acyltransferase (ALCAT1) in mouse. J. Biol. Chem. 279 (2004), 31727–31734.
38. 38 Fry, M., Green, D.E., Cardiolipin requirement for electron transfer in complex I and III of the mitochondrial respiratory chain. J. Biol. Chem. 256 (1981), 1874–1880.
39. 39 Zhang, M., et al. Gluing the respiratory chain together. Cardiolipin is required for supercomplex formation in the inner mitochondrial membrane. J. Biol. Chem. 277 (2002), 43553–43556.
40. 2+ in mitochondrial dysfunction and disease. Cell Calcium 45 (2009), 643–650.
41. 41 Barth, P.G., et al. An X-linked mitochondrial disease affecting cardiac muscle, skeletal muscle and neutrophil leucocytes. J. Neurol. Sci. 62 (1983), 327–355.
42. 2 utilization mediate exercise intolerance in Barth syndrome. Am. J. Physiol. Heart Circ. Physiol. 301 (2011), H2122–H2129.
43. 43 Powers, C., et al. Diminished exercise capacity and mitochondrial bc1 complex deficiency in tafazzin-knockdown mice. Front Physiol., 4, 2013, 74.
44. 44 Soustek, M.S., et al. Endurance training ameliorates complex 3 deficiency in a mouse model of Barth syndrome. J. Inherit. Metab. Dis. 38 (2015), 915–922.
45. 45 Sengers, R.C., et al. Congenital cataract and mitochondrial myopathy of skeletal and heart muscle associated with lactic acidosis after exercise. J. Pediatr. 86 (1975), 873–880.
46. 46 Mayr, J.A., et al. Lack of the mitochondrial protein acylglycerol kinase causes Sengers syndrome. Am. J. Hum. Genet. 90 (2012), 314–320.
47. 47 Das, S., et al. ATP citrate lyase improves mitochondrial function in skeletal muscle. Cell Metab. 21 (2015), 868–876.
48. 48 Carper, M.J., et al. Skeletal muscle group VIA phospholipase A2 (iPLA2beta): expression and role in fatty acid oxidation. Biochemistry 47 (2008), 12241–12249.
49. 49 Song, H., et al. Mice deficient in group VIB phospholipase A2 (iPLA2gamma) exhibit relative resistance to obesity and metabolic abnormalities induced by a Western diet. Am. J. Physiol. Endocrinol. Metab. 298 (2010), E1097–E1114.
50. 50 Gardocki, M.E., et al. Phosphatidylinositol biosynthesis: biochemistry and regulation. Biochim. Biophys. Acta. 1735 (2005), 89–100.
51. 51 Kim, Y.J., et al. A highly dynamic ER-derived phosphatidylinositol-synthesizing organelle supplies phosphoinositides to cellular membranes. Dev. Cell 21 (2011), 813–824.
52. 52 Rosivatz, E., Woscholski, R., Removal or masking of phosphatidylinositol(4,5)bisphosphate from the outer mitochondrial membrane causes mitochondrial fragmentation. Cell. Signal. 23 (2011), 478–486.
53. 53 Cortie, C.H., et al. Of mice, pigs and humans: an analysis of mitochondrial phospholipids from mammals with very different maximal lifespans. Exp. Gerontol. 70 (2015), 135–143.
54. 54 Hulbert, A.J., Metabolism and longevity: is there a role for membrane fatty acids?. Integr. Comp. Biol. 50 (2010), 808–817.
55. 55 Mitchell, T.W., et al. Membrane phospholipid composition may contribute to exceptional longevity of the naked mole-rat (Heterocephalus glaber): a comparative study using shotgun lipidomics. Exp. Gerontol. 42 (2007), 1053–1062.
56. 56 Hulbert, A.J., et al. The exceptional longevity of an egg-laying mammal, the short-beaked echidna (Tachyglossus aculeatus) is associated with peroxidation-resistant membrane composition. Exp. Gerontol. 43 (2008), 729–733.
57. 57 Gonzalez-Freire, M., et al. Reconsidering the role of mitochondria in aging. J. Gerontol. A Biol. Sci. Med. Sci. 70 (2015), 1334–1342.
58. 58 Nomura, K., et al. Mitochondrial phospholipid hydroperoxide glutathione peroxidase inhibits the release of cytochrome c from mitochondria by suppressing the peroxidation of cardiolipin in hypoglycaemia-induced apoptosis. Biochem. J. 351 (2000), 183–193.
59. 59 Lopez-Dominguez, J.A., et al. The influence of dietary fat source on life span in calorie restricted mice. J. Gerontol. A Biol. Sci. Med. Sci. 70 (2015), 1181–1188.
60. 60 Valencak, T.G., Azzu, V., Making heads or tails of mitochondrial membranes in longevity and aging: a role for comparative studies. Longev. Healthspan, 3, 2014, 3.
61. 61 Goto-Inoue, N., et al. Lipidomics analysis revealed the phospholipid compositional changes in muscle by chronic exercise and high-fat diet. Sci. Rep., 3, 2013, 3267.
62. 62 Mitchell, T.W., et al. Exercise alters the profile of phospholipid molecular species in rat skeletal muscle. J. Appl. Physiol. 97 (2004), 1823–1829.
63. 63 Senoo, N., et al. PGC-1alpha-mediated changes in phospholipid profiles of exercise-trained skeletal muscle. J. Lipid Res. 56 (2015), 2286–2296.
64. 64 Liang, M.T., et al. Effects of exercise training and anabolic steroids on plantaris and soleus phospholipids: a 31P nuclear magnetic resonance study. Int. J. Biochem. 25 (1993), 337–347.
65. 65 Dohm, G.L., et al. Changes in muscle mitochondrial lipid composition resulting from training and exhaustive exercise. Life Sci. 17 (1975), 1075–1080.
66. 66 Toledo, F.G., et al. Effects of physical activity and weight loss on skeletal muscle mitochondria and relationship with glucose control in type 2 diabetes. Diabetes 56 (2007), 2142–2147.
67. 67 Takahashi, M., Hood, D.A., Chronic stimulation-induced changes in mitochondria and performance in rat skeletal muscle. J. Appl. Physiol. 74 (1993), 934–941.
68. 68 Ostojic, O., et al. The effects of chronic muscle use and disuse on cardiolipin metabolism. J. Appl. Physiol. 114 (2013), 444–452.
69. 69 Lai, L., et al. A role for peroxisome proliferator-activated receptor gamma coactivator 1 (PGC-1) in the regulation of cardiac mitochondrial phospholipid biosynthesis. J. Biol. Chem. 289 (2014), 2250–2259.
70. 70 Athea, Y., et al. AMP-activated protein kinase alpha2 deficiency affects cardiac cardiolipin homeostasis and mitochondrial function. Diabetes 56 (2007), 786–794.
71. 71 Romanello, V., Sandri, M., Mitochondrial quality control and Muscle mass maintenance. Front Physiol., 6, 2015, 422.
72. 72 Mayr, J.A., Lipid metabolism in mitochondrial membranes. J. Inherit. Metab. Dis. 38 (2015), 137–144.
73. 73 de Wilde, J., et al. Short-term high fat-feeding results in morphological and metabolic adaptations in the skeletal muscle of C57BL/6J mice. Physiol. Genomics 32 (2008), 360–369.
74. 74 Hoeks, J., et al. High fat diet-induced changes in mouse muscle mitochondrial phospholipids do not impair mitochondrial respiration despite insulin resistance. PloS One, 6, 2011, e27274.
75. 75 Martin, N., et al. Dietary fatty acid composition and the homeostatic regulation of mitochondrial phospholipid classes in red muscle of rainbow trout (Oncorhynchus mykiss). J. Exp. Zool. A Ecol. Genet. Physiol. 323 (2015), 60–71.
76. 76 Martin, N., et al. Dietary lipid quality and mitochondrial membrane composition in trout: responses of membrane enzymes and oxidative capacities. J. Comp. Physiol. B. 183 (2013), 393–408.
77. 77 Fajardo, V.A., et al. Cardiolipin linoleic acid content and mitochondrial cytochrome c oxidase activity are associated in rat skeletal muscle. Chem. Phys. Lipids 187 (2015), 50–55.
78. 78 Lanza, I.R., et al. Influence of fish oil on skeletal muscle mitochondrial energetics and lipid metabolites during high-fat diet. Am. J. Physiol. Endocrinol. Metab. 304 (2013), E1391–E1403.
79. 79 Herbst, E.A., et al. Omega-3 supplementation alters mitochondrial membrane composition and respiration kinetics in human skeletal muscle. J. Physiol. 592 (2014), 1341–1352.
80. 80 Funai, K., Semenkovich, C.F., Skeletal muscle lipid flux: running water carries no poison. Am. J. Physiol. Endocrinol. Metab. 301 (2011), E245–E251.