The plasma membrane as a capacitor for energy and metabolism

American Journal of Physiology - Cell Physiology

Volumn 310, Issue 3, 2016, Pages C181-C192

  Ray, Supriyo ^a,b   Kassan, Adam ^a,b   Busija, Anna R ^a,b   Rangamani, Padmini ^c   Patel, Hemal H ^a,b  

^a VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^b University of California   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Caveolae; Cholesterol; Energy; Membrane; Metabolism; Rafts

Indexed keywords

CHOLESTEROL; LIPID; OXYGEN; MEMBRANE LIPID; MEMBRANE PROTEIN;

CELL COMMUNICATION; CELL ENERGY; CELL FUNCTION; CELL MEMBRANE; CELL METABOLISM; COEVOLUTION; ELASTICITY; MOLECULAR EVOLUTION; PRIORITY JOURNAL; REVIEW; ANIMAL; BIOLOGICAL MODEL; ELECTRIC CAPACITANCE; ENERGY METABOLISM; EVOLUTION; HUMAN; MEMBRANE FLUIDITY; METABOLISM; OXIDATION REDUCTION REACTION; SIGNAL TRANSDUCTION;

ANIMALS; BIOLOGICAL EVOLUTION; CELL MEMBRANE; ELASTICITY; ELECTRIC CAPACITANCE; ENERGY METABOLISM; HUMANS; MEMBRANE FLUIDITY; MEMBRANE LIPIDS; MEMBRANE MICRODOMAINS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; OXIDATION-REDUCTION; OXYGEN; SIGNAL TRANSDUCTION;

EID: 84956920738     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00087.2015     Document Type: Review

References (163)

1. Bae MK, Jeong DK, Park NS, Lee CH, Cho BH, Jang HO, Yun I. The effect of ethanol on the physical properties of neuronal membranes. Mol Cells 19: 356–364, 2005.
2. Baggetto LG, Clottes E, Vial C. Low mitochondrial proton leak due to high membrane cholesterol content and cytosolic creatine kinase as two features of the deviant bioenergetics of Ehrlich and AS30-D tumor cells. Cancer Res 52: 4935–4941, 1992.
3. Banerjee T, Taylor M, Jobling MG, Burress H, Yang Z, Serrano A, Holmes RK, Tatulian SA, Teter K. ADP-ribosylation factor 6 acts as an allosteric activator for the folded but not disordered cholera toxin A1 polypeptide. Mol Microbiol 94: 898–912, 2014.
4. Bissig C, Gruenberg J. Lipid sorting and multivesicular endosome biogenesis. Cold Spring Harb Perspect Biol 5: a016816, 2013.
5. Blobel G. Intracellular protein topogenesis. Proc Natl Acad Sci USA 77: 1496–1500, 1980.
6. Bogdanov M, Dowhan W. Lipid-assisted protein folding. J Biol Chem 274: 36827–36830, 1999.
7. Bogdanov M, Dowhan W. Phospholipid-assisted protein folding: phosphatidylethanolamine is required at a late step of the conformational maturation of the polytopic membrane protein lactose permease. EMBO J 17: 5255–5264, 1998.
8. Bogdanov M, Umeda M, Dowhan W. Phospholipid-assisted refolding of an integral membrane protein. Minimum structural features for phosphatidylethanolamine to act as a molecular chaperone. J Biol Chem 274: 12339–12345, 1999.
9. Bosch M, Mari M, Herms A, Fernandez A, Fajardo A, Kassan A, Giralt A, Colell A, Balgoma D, Barbero E, Gonzalez-Moreno E, Matias N, Tebar F, Balsinde J, Camps M, Enrich C, Gross SP, Garcia-Ruiz C, Perez-Navarro E, Fernandez-Checa JC, Pol A. Caveolin-1 deficiency causes cholesterol-dependent mitochondrial dysfunction and apoptotic susceptibility. Curr Biol 21: 681–686, 2011.
10. Botto L, Beretta E, Daffara R, Miserocchi G, Palestini P. Biochemical and morphological changes in endothelial cells in response to hypoxic interstitial edema. Respir Res 7: 7, 2006.
11. Brash AR. Arachidonic acid as a bioactive molecule. J Clin Invest 107: 1339–1345, 2001.
12. Brette F, Orchard C. Resurgence of cardiac t-tubule research. Physiology (Bethesda) 22: 167–173, 2007.
13. Brown AJ, Galea AM. Cholesterol as an evolutionary response to living with oxygen. Evolution 64: 2179–2183, 2010.
14. Brown DA, London E. Structure of detergent-resistant membrane domains: does phase separation occur in biological membranes? Biochem Biophys Res Commun 240: 1–7, 1997.
15. Brown DA, Rose JK. Sorting of GPI-anchored proteins to glycolipidenriched membrane subdomains during transport to the apical cell surface. Cell 68: 533–544, 1992.
16. Brown JR, Doolittle WF. Root of the universal tree of life based on ancient aminoacyl-tRNA synthetase gene duplications. Proc Natl Acad Sci USA 92: 2441–2445, 1995.
17. Canham PB. The minimum energy of bending as a possible explanation of the biconcave shape of the human red blood cell. J Theor Biol 26: 61–81, 1970.
18. Cao TB, Saier MH Jr. The general protein secretory pathway: phylogenetic analyses leading to evolutionary conclusions. Biochim Biophys Acta 1609: 115–125, 2003.
19. Carrasco S, Meyer T. STIM proteins and the endoplasmic reticulumplasma membrane junctions. Annu Rev Biochem 80: 973–1000, 2011.
20. Cavalier-Smith T. The origin of cells: a symbiosis between genes, catalysts, and membranes. Cold Spring Harb Symp Quant Biol 52: 805–824, 1987.
21. Cavalier-Smith T. The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int J Syst Evol Microbiol 52: 297–354, 2002.
22. Chandler D. Interfaces and the driving force of hydrophobic assembly. Nature 437: 640–647, 2005.
23. Chevallet M, Lescuyer P, Diemer H, van Dorsselaer A, Leize- Wagner E, Rabilloud T. Alterations of the mitochondrial proteome caused by the absence of mitochondrial DNA: a proteomic view. Electrophoresis 27: 1574–1583, 2006.
24. Christie DA, Kirchhof MG, Vardhana S, Dustin ML, Madrenas J. Mitochondrial and plasma membrane pools of stomatin-like protein 2 coalesce at the immunological synapse during T cell activation. PLoS One 7: e37144, 2012.
25. Cooper GM. The Cell: A Molecular Approach. Sunderland, MA: Sinauer, 2000.
26. Cooper RA. Influence of increased membrane cholesterol on membrane fluidity and cell function in human red blood cells. J Supramol Struct 8: 413–430, 1978.
27. Csordas G, Varnai P, Golenar T, Roy S, Purkins G, Schneider TG, Balla T, Hajnoczky G. Imaging interorganelle contacts and local calcium dynamics at the ER-mitochondrial interface. Mol Cell 39: 121–132, 2010.
28. Da Cruz S, Xenarios I, Langridge J, Vilbois F, Parone PA, Martinou JC. Proteomic analysis of the mouse liver mitochondrial inner membrane. J Biol Chem 278: 41566–41571, 2003.
29. Daleke DL. Regulation of transbilayer plasma membrane phospholipid asymmetry. J Lipid Res 44: 233–242, 2003.
30. Davies SS, Guo L. Lipid peroxidation generates biologically active phospholipids including oxidatively N-modified phospholipids. Chem Phys Lipids 181: 1–33, 2014.
31. De Duve C. Evolution of the peroxisome. Ann NY Acad Sci 168: 369–381, 1969.
32. Deamer DW. Origins of life: how leaky were primitive cells? Nature 454: 37–38, 2008.
33. Debnath D, Bhattacharya S, Chakrabarti A. Phospholipid assisted folding of a denatured heme protein: effect of phosphatidylethanolamine. Biochem Biophys Res Commun 301: 979–984, 2003.
34. DeBose-Boyd RA. Feedback regulation of cholesterol synthesis: sterolaccelerated ubiquitination and degradation of HMG CoA reductase. Cell Res 18: 609–621, 2008.
35. Demchenko AP, Yesylevskyy SO. Nanoscopic description of biomembrane electrostatics: results of molecular dynamics simulations and fluorescence probing. Chem Phys Lipids 160: 63–84, 2009.
36. Derenyi I, Julicher F, Prost J. Formation and interaction of membrane tubes. Phys Rev Lett 88: 238101, 2002.
37. Deserno M. Fluid lipid membranes: from differential geometry to curvature stresses. Chem Phys Lipids 185: 11–45, 2015.
38. Deuling HJ, Helfrich W. Red blood cell shapes as explained on the basis of curvature elasticity. Biophys J 16: 861–868, 1976.
39. Devos D, Dokudovskaya S, Alber F, Williams R, Chait BT, Sali A, Rout MP. Components of coated vesicles and nuclear pore complexes share a common molecular architecture. PLoS Biol 2: e380, 2004.
40. Evans EA. Bending resistance and chemically induced moments in membrane bilayers. Biophys J 14: 923–931, 1974.
41. Fischer TM. Is the surface area of the red cell membrane skeleton locally conserved? Biophys J 61: 298–305, 1992.
42. Flucher BE. Structural analysis of muscle development: transverse tubules, sarcoplasmic reticulum, and the triad. Dev Biol 154: 245–260, 1992.
43. Fowler SL, Akins M, Zhou H, Figeys D, Bennett SA. The liver connexin32 interactome is a novel plasma membrane-mitochondrial signaling nexus. J Proteome Res 12: 2597–2610, 2013.
44. Franzini-Armstrong C, Jorgensen AO. Structure and development of E-C coupling units in skeletal muscle. Annu Rev Physiol 56: 509–534, 1994.
45. Fridolfsson HN, Kawaraguchi Y, Ali SS, Panneerselvam M, Niesman IR, Finley JC, Kellerhals SE, Migita MY, Okada H, Moreno AL, Jennings M, Kidd MW, Bonds JA, Balijepalli RC, Ross RS, Patel PM, Miyanohara A, Chen Q, Lesnefsky EJ, Head BP, Roth DM, Insel PA, Patel HH. Mitochondria-localized caveolin in adaptation to cellular stress and injury. FASEB J 26: 4637–4649, 2012.
46. Fridolfsson HN, Patel HH. Caveolin and caveolae in age associated cardiovascular disease. J Geriatr Cardiol 10: 66–74, 2013.
47. 2+- ATPases. J Biol Chem 280: 43198–43208, 2005.
48. Furt F, Simon-Plas F, Mongrand S. Lipids of the plant plasma membrane. Plant Plasma Membr 19: 3–30, 2011.
49. Garrigues A, Escargueil AE, Orlowski S. The multidrug transporter, P-glycoprotein, actively mediates cholesterol redistribution in the cell membrane. Proc Natl Acad Sci USA 99: 10347–10352, 2002.
50. Gattinger A, Schloter M, Munch JC. Phospholipid etherlipid and phospholipid fatty acid fingerprints in selected euryarchaeotal monocultures for taxonomic profiling. FEMS Microbiol Lett 213: 133–139, 2002.
51. Grafmuller A, Shillcock J, Lipowsky R. The fusion of membranes and vesicles: pathway and energy barriers from dissipative particle dynamics. Biophys J 96: 2658–2675, 2009.
52. Grafmuller A, Shillcock J, Lipowsky R. Pathway of membrane fusion with two tension-dependent energy barriers. Phys Rev Lett 98: 218101, 2007.
53. Grzelczyk A, Gendaszewska-Darmach E. Novel bioactive glycerolbased lysophospholipids: new data—new insight into their function. Biochimie 95: 667–679, 2013.
54. Hannun YA, Obeid LM. Principles of bioactive lipid signalling: lessons from sphingolipids. Nat Rev Mol Cell Biol 9: 139–150, 2008.
55. Head BP, Peart JN, Panneerselvam M, Yokoyama T, Pearn ML, Niesman IR, Bonds JA, Schilling JM, Miyanohara A, Headrick J, Ali SS, Roth DM, Patel PM, Patel HH. Loss of caveolin-1 accelerates neurodegeneration and aging. PLoS One 5: e15697, 2010.
56. Helfrich W. Elastic properties of lipid bilayers: theory and possible experiments. Z Naturforsch C 28: 693–703, 1973.
57. Helle SC, Kanfer G, Kolar K, Lang A, Michel AH, Kornmann B. Organization and function of membrane contact sites. Biochim Biophys Acta 1833: 2526–2541, 2013.
58. Henkart M, Landis DM, Reese TS. Similarity of junctions between plasma membranes and endoplasmic reticulum in muscle and neurons. J Cell Biol 70: 338–347, 1976.
59. Hilario E, Gogarten JP. The prokaryote-to-eukaryote transition reflected in the evolution of the V/F/A-ATPase catalytic and proteolipid subunits. J Mol Evol 46: 703–715, 1998.
60. Horikawa YT, Panneerselvam M, Kawaraguchi Y, Tsutsumi YM, Ali SS, Balijepalli RC, Murray F, Head BP, Niesman IR, Rieg T, Vallon V, Insel PA, Patel HH, Roth DM. Cardiac-specific overexpression of caveolin-3 attenuates cardiac hypertrophy and increases natriuretic peptide expression and signaling. J Am Coll Cardiol 57: 2273–2283, 2011.
61. Huber R, Eder W, Heldwein S, Wanner G, Huber H, Rachel R, Stetter KO. Thermocrinis ruber gen. nov., sp. nov., a pink-filamentforming hyperthermophilic bacterium isolated from Yellowstone National Park. Appl Environ Microbiol 64: 3576–3583, 1998.
62. Hughes AL, Todd BL, Espenshade PJ. SREBP pathway responds to sterols and functions as an oxygen sensor in fission yeast. Cell 120: 831–842, 2005.
63. Igbavboa U, Avdulov NA, Chochina SV, Wood WG. Transbilayer distribution of cholesterol is modified in brain synaptic plasma membranes of knockout mice deficient in the low-density lipoprotein receptor, apolipoprotein E, or both proteins. J Neurochem 69: 1661–1667, 1997.
64. Igbavboa U, Avdulov NA, Schroeder F, Wood WG. Increasing age alters transbilayer fluidity and cholesterol asymmetry in synaptic plasma membranes of mice. J Neurochem 66: 1717–1725, 1996.
65. Igbavboa U, Eckert GP, Malo TM, Studniski AE, Johnson LN, Yamamoto N, Kobayashi M, Fujita SC, Appel TR, Muller WE, Wood WG, Yanagisawa K. Murine synaptosomal lipid raft protein and lipid composition are altered by expression of human apoE 3 and 4 and by increasing age. J Neurol Sci 229–230: 225–232, 2005.
66. Igbavboa U, Hamilton J, Kim HY, Sun GY, Wood WG. A new role for apolipoprotein E: modulating transport of polyunsaturated phospholipid molecular species in synaptic plasma membranes. J Neurochem 80: 255–261, 2002.
67. Igbavboa U, Sun GY, Weisman GA, He Y, Wood WG. Amyloid beta-protein stimulates trafficking of cholesterol and caveolin-1 from the plasma membrane to the Golgi complex in mouse primary astrocytes. Neuroscience 162: 328–338, 2009.
68. Iglic A. A possible mechanism determining the stability of spiculated red blood cells. J Biomech 30: 35–40, 1997.
69. Inoue T, Tsai B. How viruses use the endoplasmic reticulum for entry, replication, and assembly. Cold Spring Harb Perspect Biol 5: a013250, 2013.
70. Jaric M, Seifert U, Wintz W, Wortis M. Vesicular instabilities: the prolate-to-oblate transition and other shape instabilities of fluid bilayer membranes. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 52: 6623–6634, 1995.
71. Jekely G. Did the last common ancestor have a biological membrane? Biol Direct 1: 35, 2006.
72. Jekely G. Small GTPases and the evolution of the eukaryotic cell. Bioessays 25: 1129–1138, 2003.
73. Kates M, Yengoyan LS, Sastry PS. A diether analog of phosphatidyl glycerophosphate in Halobacterium cutirubrum. Biochim Biophys Acta 98: 252–268, 1965.
74. Khan N, Shen J, Chang TY, Chang CC, Fung PC, Grinberg O, Demidenko E, Swartz H. Plasma membrane cholesterol: a possible barrier to intracellular oxygen in normal and mutant CHO cells defective in cholesterol metabolism. Biochemistry 42: 23–29, 2003.
75. Kiessling V, Wan C, Tamm LK. Domain coupling in asymmetric lipid bilayers. Biochim Biophys Acta 1788: 64–71, 2009.
76. Kirchhof MG, Chau LA, Lemke CD, Vardhana S, Darlington PJ, Marquez ME, Taylor R, Rizkalla K, Blanca I, Dustin ML, Madrenas J. Modulation of T cell activation by stomatin-like protein 2. J Immunol 181: 1927–1936, 2008.
77. Klecker T, Scholz D, Fortsch J, Westermann B. The yeast cell cortical protein Num1 integrates mitochondrial dynamics into cellular architecture. J Cell Sci 126: 2924–2930, 2013.
78. Koga Y. Early evolution of membrane lipids: how did the lipid divide occur? J Mol Evol 72: 274–282, 2011.
79. Koga Y, Kyuragi T, Nishihara M, Sone N. Did archaeal and bacterial cells arise independently from noncellular precursors? A hypothesis stating that the advent of membrane phospholipid with enantiomeric glycerophosphate backbones caused the separation of the two lines of descent. J Mol Evol 46: 54–63, 1998.
80. Koga Y, Morii H. Biosynthesis of ether-type polar lipids in archaea and evolutionary considerations. Microbiol Mol Biol Rev 71: 97–120, 2007.
81. Koonin EV. Comparative genomics, minimal gene-sets and the last universal common ancestor. Nat Rev Microbiol 1: 127–136, 2003.
82. Kurzchalia TV, Dupree P, Parton RG, Kellner R, Virta H, Lehnert M, Simons K. VIP21, a 21-kD membrane protein is an integral component of trans-Golgi-network-derived transport vesicles. J Cell Biol 118: 1003–1014, 1992.
83. Lackner LL, Ping H, Graef M, Murley A, Nunnari J. Endoplasmic reticulum-associated mitochondria-cortex tether functions in the distribution and inheritance of mitochondria. Proc Natl Acad Sci USA 110: E458–E467, 2013.
84. Lane N. Oxygen: The Molecule That Made the World. Oxford, UK: Oxford Univ. Press, 2002.
85. Langworthy TA, Smith PF, Mayberry WR. Lipids of Thermoplasma acidophilum. J Bacteriol 112: 1193–1200, 1972.
86. Lenz O, Schmid F. Structure of symmetric and asymmetric “ripple” phases in lipid bilayers. Phys Rev Lett 98: 058104, 2007.
87. Levine T, Loewen C. Inter-organelle membrane contact sites: through a glass, darkly. Curr Opin Cell Biol 18: 371–378, 2006.
88. Lingwood D, Simons K. Lipid rafts as a membrane-organizing principle. Science 327: 46–50, 2010.
89. Lipowsky R. Spontaneous tubulation of membranes and vesicles reveals membrane tension generated by spontaneous curvature. Faraday Discuss 161: 305–331, 2013.
90. Liu P, Anderson RG. Compartmentalized production of ceramide at the cell surface. J Biol Chem 270: 27179–27185, 1995.
91. Mandyam CD, Schilling JM, Cui W, Egawa J, Niesman IR, Kellerhals SE, Staples MC, Busija AR, Risbrough VB, Posadas E, Grogman GC, Chang JW, Roth DM, Patel PM, Patel HH, Head BP. Neuron-targeted caveolin-1 improves molecular signaling, plasticity, and behavior dependent on the hippocampus in adult and aged mice. Biol Psychiatry (October 7, 2015). doi:10.1016/j.biopsych.2015.09.020.
92. Mansy SS, Schrum JP, Krishnamurthy M, Tobe S, Treco DA, Szostak JW. Template-directed synthesis of a genetic polymer in a model protocell. Nature 454: 122–125, 2008.
93. Marrink SJ, Mark AE. The mechanism of vesicle fusion as revealed by molecular dynamics simulations. J Am Chem Soc 125: 11144–11145, 2003.
94. Martin W, Muller M. The hydrogen hypothesis for the first eukaryote. Nature 392: 37–41, 1998.
95. Martin W, Russell MJ. On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. Philos Trans R Soc Lond B Biol Sci 358: 59–83, 2003.
96. Massey KA, Schnitzer JE. Caveolae and cancer. Recent Results Cancer Res 180: 217–231, 2010.
97. Mouritsen OG, Zuckermann MJ. What’s so special about cholesterol? Lipids 39: 1101–1113, 2004.
98. Mulkidjanian AY, Galperin MY, Koonin EV. Co-evolution of primordial membranes and membrane proteins. Trends Biochem Sci 34: 206–215, 2009.
99. Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74: 1124–1136, 1986.
100. Murry CE, Richard VJ, Reimer KA, Jennings RB. Ischemic preconditioning slows energy metabolism and delays ultrastructural damage during a sustained ischemic episode. Circ Res 66: 913–931, 1990.
101. Nelson P, Powers T, Seifert U. Dynamical theory of the Pearling instability in cylindrical vesicles. Phys Rev Lett 74: 3384–3387, 1995.
102. Nishizuka Y. Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C. Science 258: 607–614, 1992.
103. Palade GE. Fine structure of blood capillaries. J Appl Phys 24: 1424, 1953.
104. Palade GE, Bruns RR. Structural modulations of plasmalemmal vesicles. J Cell Biol 37: 633–649, 1968.
105. Papa S, Skulachev VP. Reactive oxygen species, mitochondria, apoptosis and aging. Mol Cell Biochem 174: 305–319, 1997.
106. Papackova Z, Cahova M. Fatty acid signaling: the new function of intracellular lipases. Int J Mol Sci 16: 3831–3855, 2015.
107. Parlo RA, Coleman PS. Enhanced rate of citrate export from cholesterol- rich hepatoma mitochondria. The truncated Krebs cycle and other metabolic ramifications of mitochondrial membrane cholesterol. J Biol Chem 259: 9997–10003, 1984.
108. Parton RG, Molero JC, Floetenmeyer M, Green KM, James DE. Characterization of a distinct plasma membrane macrodomain in differentiated adipocytes. J Biol Chem 277: 46769–46778, 2002.
109. Parton RG, Way M, Zorzi N, Stang E. Caveolin-3 associates with developing T-tubules during muscle differentiation. J Cell Biol 136: 137–154, 1997.
110. Patel HH, Insel PA. Lipid rafts and caveolae and their role in compartmentation of redox signaling. Antioxid Redox Signal 11: 1357–1372, 2009.
111. Patel HH, Murray F, Insel PA. Caveolae as organizers of pharmacologically relevant signal transduction molecules. Annu Rev Pharmacol Toxicol 48: 359–391, 2008.
112. Payne JL, Boyer AG, Brown JH, Finnegan S, Kowalewski M, Krause RA Jr, Lyons SK, McClain CR, McShea DW, Novack-Gottshall PM, Smith FA, Stempien JA, Wang SC. Two-phase increase in the maximum size of life over 35 billion years reflects biological innovation and environmental opportunity. Proc Natl Acad Sci USA 106: 24–27, 2009.
113. Payne JL, McClain CR, Boyer AG, Brown JH, Finnegan S, Kowalewski M, Krause RA Jr, Lyons SK, McShea DW, Novack-Gottshall PM, Smith FA, Spaeth P, Stempien JA, Wang SC. The evolutionary consequences of oxygenic photosynthesis: a body size perspective. Photosynth Res 107: 37–57, 2011.
114. Peart JN, Pepe S, Reichelt ME, Beckett N, See Hoe L, Ozberk V, Niesman IR, Patel HH, Headrick JP. Dysfunctional survival-signaling and stress-intolerance in aged murine and human myocardium. Exp Gerontol 50: 72–81, 2014.
115. Pelkmans L, Burli T, Zerial M, Helenius A. Caveolin-stabilized membrane domains as multifunctional transport and sorting devices in endocytic membrane traffic. Cell 118: 767–780, 2004.
116. Pelkmans L, Helenius A. Endocytosis via caveolae. Traffic 3: 311–320, 2002.
117. Pereto J, Lopez-Garcia P, Moreira D. Ancestral lipid biosynthesis and early membrane evolution. Trends Biochem Sci 29: 469–477, 2004.
118. Philips R, Kondev J, Theriot J, Orme N, Garcia H. Physical Biology of the Cell. New York: Garland Science, 2009.
119. Pichler H, Gaigg B, Hrastnik C, Achleitner G, Kohlwein SD, Zellnig G, Perktold A, Daum G. A subfraction of the yeast endoplasmic reticulum associates with the plasma membrane and has a high capacity to synthesize lipids. Eur J Biochem 268: 2351–2361, 2001.
120. Pike LJ. Lipid rafts: bringing order to chaos. J Lipid Res 44: 655–667, 2003.
121. Pike LJ, Casey L. Localization and turnover of phosphatidylinositol 4,5-bisphosphate in caveolin-enriched membrane domains. J Biol Chem 271: 26453–26456, 1996.
122. Pike LJ, Han X, Chung KN, Gross RW. Lipid rafts are enriched in arachidonic acid and plasmenylethanolamine and their composition is independent of caveolin-1 expression: a quantitative electrospray ionization/ mass spectrometric analysis. Biochemistry 41: 2075–2088, 2002.
123. Rajendran L, Simons K. Lipid rafts and membrane dynamics. J Cell Sci 118: 1099–1102, 2005.
124. Rangamani P, Benjamini A, Agrawal A, Smit B, Steigmann DJ, Oster G. Small scale membrane mechanics. Biomech Model Mechanobiol 13: 697–711, 2014.
125. Rao AM, Igbavboa U, Semotuk M, Schroeder F, Wood WG. Kinetics and size of cholesterol lateral domains in synaptosomal membranes: modification by sphingomyelinase and effects on membrane enzyme activity. Neurochem Int 23: 45–52, 1993.
126. Raucher D, Sheetz MP. Characteristics of a membrane reservoir buffering membrane tension. Biophys J 77: 1992–2002, 1999.
127. Ray S, Taylor M, Banerjee T, Tatulian SA, Teter K. Lipid rafts alter the stability and activity of the cholera toxin A1 subunit. J Biol Chem 287: 30395–30405, 2012.
128. Ray S, Taylor M, Burlingame M, Tatulian SA, Teter K. Modulation of toxin stability by 4-phenylbutyric acid and negatively charged phospholipids. PLoS One 6: e23692, 2011.
129. Rezaul K, Wu L, Mayya V, Hwang SI, Han D. A systematic characterization of mitochondrial proteome from human T leukemia cells. Mol Cell Proteomics 4: 169–181, 2005.
130. Rosen GM. Free Radicals: Biology and Detection by Spin Trapping. New York: Oxford Univ. Press, 1999.
131. Rossy J, Ma Y, Gaus K. The organisation of the cell membrane: do proteins rule lipids? Curr Opin Chem Biol 20C: 54–59, 2014.
132. Rothberg KG, Heuser JE, Donzell WC, Ying YS, Glenney JR, Anderson RG. Caveolin, a protein component of caveolae membrane coats. Cell 68: 673–682, 1992.
133. Rothman JE, Lenard J. Membrane asymmetry. Science 195: 743–753, 1977.
134. Rouslin W, MacGee J, Wesselman AR, Adams RJ, Gupte S. Canine myocardial ischemia: increased mitochondrial cholesterol, a marker of mitochondrial membrane injury. J Mol Cell Cardiol 12: 1475–1482, 1980.
135. Saenz JP, Sezgin E, Schwille P, Simons K. Functional convergence of hopanoids and sterols in membrane ordering. Proc Natl Acad Sci USA 109: 14236–14240, 2012.
136. Sandow A. Excitation-contraction coupling in muscular response. Yale J Biol Med 25: 176–201, 1952.
137. Sarnataro D, Campana V, Paladino S, Stornaiuolo M, Nitsch L, Zurzolo C. PrPC association with lipid rafts in the early secretory pathway stabilizes its cellular conformation. Mol Biol Cell 15: 4031–4042, 2004.
138. Schroeder F, Morrison WJ, Gorka C, Wood WG. Transbilayer effects of ethanol on fluidity of brain membrane leaflets. Biochim Biophys Acta 946: 85–94, 1988.
139. Seifert U, Berndl K, Lipowsky R. Shape transformations of vesicles: phase diagram for spontaneous-curvature and bilayer-coupling models. Phys Rev A 44: 1182–1202, 1991.
140. Simons K, Ikonen E. Functional rafts in cell membranes. Nature 387: 569–572, 1997.
141. Simons K, Toomre D. Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1: 31–39, 2000.
142. Slotte JP, Hedstrom G, Rannstrom S, Ekman S. Effects of sphingomyelin degradation on cell cholesterol oxidizability and steady-state distribution between the cell surface and the cell interior. Biochim Biophys Acta 985: 90–96, 1989.
143. Stefan CJ, Manford AG, Emr SD. ER-PM connections: sites of information transfer and inter-organelle communication. Curr Opin Cell Biol 25: 434–442, 2013.
144. Sun J, Nguyen T, Aponte AM, Menazza S, Kohr MJ, Roth DM, Patel HH, Murphy E, Steenbergen C. Ischaemic preconditioning preferentially increases protein S-nitrosylation in subsarcolemmal mitochondria. Cardiovasc Res 106: 227–236, 2015.
145. Szostak JW, Bartel DP, Luisi PL. Synthesizing life. Nature 409: 387–390, 2001.
146. Taylor SW, Fahy E, Zhang B, Glenn GM, Warnock DE, Wiley S, Murphy AN, Gaucher SP, Capaldi RA, Gibson BW, Ghosh SS. Characterization of the human heart mitochondrial proteome. Nat Biotechnol 21: 281–286, 2003.
147. Teter K, Jobling MG, Sentz D, Holmes RK. The cholera toxin A13 subdomain is essential for interaction with ADP-ribosylation factor 6 and full toxic activity but is not required for translocation from the endoplasmic reticulum to the cytosol. Infect Immun 74: 2259–2267, 2006.
148. Thomas JA, Rana FR. The influence of environmental conditions, lipid composition, and phase behavior on the origin of cell membranes. Orig Life Evol Biosph 37: 267–285, 2007.
149. Toulmay A, Prinz WA. Lipid transfer and signaling at organelle contact sites: the tip of the iceberg. Curr Opin Cell Biol 23: 458–463, 2011.
150. Tristram-Nagle S, Zhang R, Suter RM, Worthington CR, Sun WJ, Nagle JF. Measurement of chain tilt angle in fully hydrated bilayers of gel phase lecithins. Biophys J 64: 1097–1109, 1993.
151. Tsutsumi YM, Horikawa YT, Jennings MM, Kidd MW, Niesman IR, Yokoyama U, Head BP, Hagiwara Y, Ishikawa Y, Miyanohara A, Patel PM, Insel PA, Patel HH, Roth DM. Cardiac-specific overexpression of caveolin-3 induces endogenous cardiac protection by mimicking ischemic preconditioning. Circulation 118: 1979–1988, 2008.
152. van Meer G, Simons K. Lipid polarity and sorting in epithelial cells. J Cell Biochem 36: 51–58, 1988.
153. Vinten J, Johnsen AH, Roepstorff P, Harpoth J, Tranum-Jensen J. Identification of a major protein on the cytosolic face of caveolae. Biochim Biophys Acta 1717: 34–40, 2005.
154. Vinten J, Voldstedlund M, Clausen H, Christiansen K, Carlsen J, Tranum-Jensen J. A 60-kDa protein abundant in adipocyte caveolae. Cell Tissue Res 305: 99–106, 2001.
155. Wachtershauser G. From pre-cells to Eukarya—a tale of two lipids. Mol Microbiol 47: 13–22, 2003.
156. Wang CH, Popel AS. Effect of red blood cell shape on oxygen transport in capillaries. Math Biosci 116: 89–110, 1993.
157. Wang J, Schilling JM, Niesman IR, Headrick JP, Finley JC, Kwan E, Patel PM, Head BP, Roth DM, Yue Y, Patel HH. Cardioprotective trafficking of caveolin to mitochondria is Gi-protein dependent. Anesthesiology 121: 538–548, 2014.
158. Watkins EB, Miller CE, Majewski J, Kuhl TL. Membrane texture induced by specific protein binding and receptor clustering: active roles for lipids in cellular function. Proc Natl Acad Sci USA 108: 6975–6980, 2011.
159. Widomska J, Raguz M, Subczynski WK. Oxygen permeability of the lipid bilayer membrane made of calf lens lipids. Biochim Biophys Acta 1768: 2635–2645, 2007.
160. Woese CR, Kandler O, Wheelis ML. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA 87: 4576–4579, 1990.
161. Woese CR, Magrum LJ, Fox GE. Archaebacteria. J Mol Evol 11: 245–251, 1978.
162. Wood WG, Gorka C, Schroeder F. Acute and chronic effects of ethanol on transbilayer membrane domains. J Neurochem 52: 1925–1930, 1989.
163. Yesylevskyy SO, Demchenko AP, Kraszewski S, Ramseyer C. Cholesterol induces uneven curvature of asymmetric lipid bilayers. ScientificWorldJournal 2013: 965230, 2013.