Membrane fluidity matters: Hyperthermia from the aspects of lipids and membranes

International Journal of Hyperthermia

Volumn 29, Issue 5, 2013, Pages 491-499

  Csoboz, Balint ^a   Balogh, Gabor E ^a   Kusz, Erzsebet ^a   Gombos, Imre ^a   Peter, Maria ^a   Crul, Tim ^a   Gungor, Burcin ^a   Haracska, Lajos ^a   Bogdanovics, Gordana ^b   Torok, Zsolt ^a   Horvath, Ibolya ^a   Vigh, Laszlo ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b ONCOLOGY INSTITUTE OF VOJVODINA   (Serbia)

Author keywords

Cancer therapy; Heat shock protein; Hyperthermia; Lipid raft; Membrane fluidity; Thermotolerance

Indexed keywords

CISPLATIN; DEOXYRIBODIPYRIMIDINE PHOTOLYASE; HEAT SHOCK PROTEIN; LIPID; PHOSPHOLIPASE A2; PHOSPHOLIPASE C; POLYUNSATURATED FATTY ACID;

APOPTOSIS; CELL DEATH; CELL DENSITY; CELL MEMBRANE; CELL MEMBRANE FLUIDITY; CELL STRESS; FLUIDIZATION; HEAT SENSITIVITY; HEAT SHOCK RESPONSE; HEAT TOLERANCE; HUMAN; HYPERTHERMIC THERAPY; INDEPENDENT VARIABLE; INTRACELLULAR SIGNALING; LETHALITY; LIPID MEMBRANE; LIPID METABOLISM; LIPID RAFT; LIPIDOMICS; MELANOMA B16; NONHUMAN; PHYSICAL CHEMISTRY; PLEIOTROPY; REVIEW; STOICHIOMETRY; TUMOR CELL;

EID: 84881121802     PISSN: 02656736     EISSN: 14645157     Source Type: Journal    
DOI: 10.3109/02656736.2013.808765     Document Type: Review

References (91)

1. Pallepati P, Averill-Bates D. Mild thermotolerance induced at 40 °C increases antioxidants and protects HeLa cells against mitochondrial apoptosis induced by hydrogen peroxide: Role of p53. Arch Biochem Biophys 2010;495:97-111.
2. Issels RD. Hyperthermia adds to chemotherapy. Eur J Cancer 2008; 44:2546-54.
3. Ostberg JR, Repasky EA. Emerging evidence indicates that physiologically relevant thermal stress regulates dendritic cell function. Cancer Immunol Immunother 2006;55:292-8. (Pubitemid 41682578)
4. Peer AJ, Grimm MJ, Zynda ER, Repasky EA. Diverse immune mechanisms may contribute to the survival benefit seen in cancer patients receiving hyperthermia. Immunol Res 2010;46:137-54.
5. Mace TA, Zhong L, Kilpatrick C, Zynda E, Lee C-T, Capitano M, et al. Differentiation of CD8+ T cells into effector cells is enhanced by physiological range hyperthermia. J Leukoc Biol 2011;90: 951-62.
6. Takahashi A, Yamakawa N, Mori E, Ohnishi K, Yokota S, Sugo N, et al. Development of thermotolerance requires interaction between polymerase-beta and heat shock proteins. Cancer Sci 2008;99: 973-8. (Pubitemid 351997600)
7. Nivon M, Richet E, Codogno P, Arrigo A-P, Kretz-Remy C. Autophagy activation by NFkappaB is essential for cell survival after heat shock. Autophagy 2009;5:766-83.
8. Heilbrunn, LV. The colloid chemistry of protoplasm. IV. The heat coagulation of protoplasm. Am J Physiol 1924;69:190-9.
9. Yatvin MB, Clifton KH, Dennis WH. Hyperthermia and local anesthetics: Potentiation of survival of tumor-bearing mice. Science 1979;205:195-6. (Pubitemid 9224693)
10. Balogh G, Péter M, Liebisch G, Horváth I, Török Z, Nagy E, et al. Lipidomics reveals membrane lipid remodelling and release of potential lipid mediators during early stress responses in a murine melanoma cell line. Biochim Biophys Acta 2010;1801: 1036-47.
11. Péter M, Balogh G, Gombos I, Liebisch G, Horváth I, Török Z, et al. Nutritional lipid supply can control the heat shock response of B16 melanoma cells in culture. Mol Membr Biol 2012;29:274-89.
12. Baritaki S, Apostolakis S, Kanellou P, Dimanche-Boitrel M-T, Spandidos DA, Bonavida B. Reversal of tumor resistance to apoptotic stimuli by alteration of membrane fluidity: Therapeutic implications. Adv Cancer Res 2007;98:149-90. (Pubitemid 46566453)
13. Zhang F, Du G. Dysregulated lipid metabolism in cancer. World J Biol Chem 2012;3:167-74.
14. Nomura DK, Long JZ, Niessen S, Hoover HS, Ng S-W, Cravatt BF. Monoacylglycerol lipase regulates a fatty acid network that promotes cancer pathogenesis. Cell 2010;140:49-61.
15. Cadenas C, Vosbeck S, Hein E-M, Hellwig B, Langer A, Hayen H, et al. Glycerophospholipid profile in oncogene-induced senescence. Biochim Biophys Acta 2012;1821:1256-68.
16. Funaki N, Tanaka J, Kono Y, Nonaka A, Yotsumoto F, Lee J-U, et al. Combination of alpha-fetoprotein mRNA-based detection of hematogenously disseminating hepatocellular carcinoma cells and analysis of cancer cell membrane fluidity is more accurate in screening patients at risk of postoperative recurrence. Oncol Rep 2004;11:637-9.
17. Sok M, Sentjurc M, Schara M, Stare J, Rott T. Cell membrane fluidity and prognosis of lung cancer. Ann Thorac Surg 2002;73: 1567-71. (Pubitemid 34596594)
18. Yukihara M, Komizu Y, Tanoue O, Matsushita T, Matsumoto Y, Ueoka R. Specific accumulation and antitumor effects of hybrid liposomes on the growth of lung tumor cells. Yakugaku Zasshi 2010;130:1581-7.
19. Batko J, Plotast-Necas B, Warchol T, Karoń H. The effect of an experimental neoplastic disease on the flux of sodium and potassium ions across red blood cells and on the lipid composition of their membranes. Acta Biochim Pol 1992;39:317-26.
20. Barker CJ, Bowler K. Lipid composition of the membranes from cells of two rat tumors and its relationship to tumor thermosensitivity. Radiat Res 1991;125:48-55.
21. Gonda K, Watanabe TM, Ohuchi N, Higuchi H. In vivo nanoimaging of membrane dynamics in metastatic tumor cells using quantum dots. J Biol Chem 2010;285:2750-7.
22. Zeisig R, Koklic T, Wiesner B, Fichtner I, Sentjurc M. Increase in fluidity in the membrane of MT3 breast cancer cells correlates with enhanced cell adhesion in vitro and increased lung metastasis in NOD/SCID mice. Arch Biochem Biophys 2007;459:98-106.
23. Taraboletti G, Perin L, Bottazzi B, Mantovani A, Giavazzi R, Salmona M. Membrane fluidity affects tumor-cell motility, invasion and lung-colonizing potential. Int J Cancer 1989;44:707-13. (Pubitemid 19258749)
24. Sherbet G V. Membrane fluidity and cancer metastasis. Exp Cell Biol 1989;57:198-205. (Pubitemid 19261731)
25. Benkö S, Hilkmann H, Vigh L, Van Blitterswijk WJ. Catalytic hydrogenation of fatty acyl chains in plasma membranes: Effect on membrane lipid fluidity and expression of cell surface antigens. Biochim Biophys Acta 1987;896:129-35. (Pubitemid 17002006)
26. Angelucci C, Maulucci G, Lama G, Proietti G, Colabianchi A, Papi M, et al. Epithelial-stromal interactions in human breast cancer: Effects on adhesion, plasma membrane fluidity and migration speed and directness. PloS One 2012;7:e50804.
27. Segui B, Legembre P. Redistribution of CD95 into the lipid rafts to treat cancer cells? Recent Pat Anticancer Drug Discov 2010;5: 22-8.
28. Miller RC, Richards M, Baird C, Martin S, Hall EJ. Interaction of hyperthermia and chemotherapy agents: Cell lethality and oncogenic potential. Int J Hyperthermia 1994;10:89-99. (Pubitemid 24030725)
29. Horváth I, Glatz A, Varvasovszki V, Török Z, Páli T, Balogh G, et al. Membrane physical state controls the signaling mechanism of the heat shock response in Synechocystis PCC 6803: Identification of hsp17 as a 'fluidity gene'. Proc Natl Acad Sci USA 1998;95: 3513-18.
30. Shigapova N, Török Z, Balogh G, Goloubinoff P, Vígh L, Horváth I. Membrane fluidization triggers membrane remodeling which affects the thermotolerance in Escherichia coli. Biochem Biophys Res Commun 2005;328:1216-23. (Pubitemid 40238763)
31. Horváth I, Glatz A, Nakamoto H, Mishkind ML, Munnik T, Saidi Y, et al. Heat shock response in photosynthetic organisms: Membrane and lipid connections. Prog Lipid Res 2012;51:208-20.
32. Vigh L, Horváth I, Horváth LI, Dudits D, Farkas T. Protoplast plasmalemma fluidity of hardened wheats correlates with frost resistance. FEBS Lett 1979;107:291-4.
33. Vigh L, Horváth I, Farkas T, Horvátht LI, Belea A. Adaptation of membrane fluidity of rye wheat seedlings according to temperature. Phytochemistry 1979;18:787-9.
34. Vigh L, Maresca B, Harwood JL. Does the membrane's physical state control the expression of heat shock and other genes? Trends Biochem Sci 1998;23:369-74. (Pubitemid 28511372)
35. Vigh L, Escribá P V, Sonnleitner A, Sonnleitner M, Piotto S, Maresca B, et al. The significance of lipid composition for membrane activity: New concepts and ways of assessing function. Prog Lipid Res 2005;44:303-44. (Pubitemid 41429298)
36. Vigh L, Horváth I, Maresca B, Harwood JL. Can the stress protein response be controlled by 'membrane-lipid therapy'? Trends Biochem Sci 2007;32:357-63. (Pubitemid 47126860)
37. Vigh L, Los DA, Horváth I, Murata N. The primary signal in the biological perception of temperature: Pd-catalyzed hydrogenation of membrane lipids stimulated the expression of the desA gene in Synechocystis PCC6803. Proc Natl Acad Sci USA 1993;90: 9090-4. (Pubitemid 23306457)
38. Simons K, Sampaio JL. Membrane organization and lipid rafts. Cold Spring Harb Perspect Biol 2011;3(10):a004697.
39. Olivera-Couto A, Aguilar PS. Eisosomes and plasma membrane organization. Mol Genet Genomics 2012;287:607-20.
40. Balogh G, Péter M, Glatz A, Gombos I, Török Z, Horváth I, et al. Key role of lipids in heat stress management. FEBS Lett 2013;587:1970-80.
41. Brameshuber M, Weghuber J, Ruprecht V, Gombos I, Horváth I, Vigh L, et al. Imaging of mobile long-lived nanoplatforms in the live cell plasma membrane. J Biol Chem 2010;285:41765-71.
42. Balogh G, Horváth I, Nagy E, Hoyk Z, Benko S, Bensaude O, et al. The hyperfluidization of mammalian cell membranes acts as a signal to initiate the heat shock protein response. FEBS J 2005;272: 6077-86. (Pubitemid 41713697)
43. Nagy E, Balogi Z, Gombos I, Akerfelt M, Björkbom A, Balogh G, et al. Hyperfluidization-coupled membrane microdomain reorganization is linked to activation of the heat shock response in a murine melanoma cell line. Proc Natl Acad Sci USA 2007;104: 7945-50. (Pubitemid 47185856)
44. Giocondi M-C, Besson F, Dosset P, Milhiet P-E, Le Grimellec C. Temperature-dependent localization of GPI-anchored intestinal alkaline phosphatase in model rafts. J Mol Recognit 2007;20: 531-7.
45. Chung J, Nguyen A-K, Henstridge DC, Holmes AG, Chan MHS, Mesa JL, et al. HSP72 protects against obesity-induced insulin resistance. Proc Natl Acad Sci USA 2008;105:1739-44. (Pubitemid 351346584)
46. Gombos I, Crul T, Piotto S, Güngör B, Török Z, Balogh G, et al. Membrane-lipid therapy in operation: The HSP co-inducer BGP-15 activates stress signal transduction pathways by remodeling plasma membrane rafts. PLOS One 2011;6(12):e28818.
47. Crul T, Toth N, Piotto S, Literati-Nagy P, Tory K, Haldimann P, et al. Hydroximic acid derivatives: Pleiotropic HSP co-inducers restoring homeostasis and robustness. Curr Pharm Des 2013;19: 309-46.
48. Mukherjee S, Maxfield FR. Membrane domains. Annu Rev Cell Dev Biol 2004;20:839-66. (Pubitemid 39488660)
49. Grassme H, Riethmuller J, Gulbins E, Grassmé H, Riethmüller J. Biological aspects of ceramide-enriched membrane domains. Prog Lipid Res 2007;46:161-70. (Pubitemid 46962121)
50. Patra SK. Dissecting lipid raft facilitated cell signaling pathways in cancer. Biochim Biophys Acta 2008;1785:182-206.
51. Vigh L, Nakamoto H, Landry J, Gomez-Munoz A, Harwood JL, Horvath I. Membrane regulation of the stress response from prokaryotic models to mammalian cells. Ann N Y Acad Sci 2007; 1113:40-51. (Pubitemid 350015023)
52. Balboa MA, Balsinde J. Oxidative stress and arachidonic acid mobilization. Biochim Biophys Acta 2006;1761:385-91. (Pubitemid 43776462)
53. Balsinde J, Winstead M V, Dennis EA. Phospholipase A(2) regulation of arachidonic acid mobilization. FEBS Lett 2002; 531:2-6. (Pubitemid 35232775)
54. Hirabayashi T, Murayama T, Shimizu T. Regulatory mechanism and physiological role of cytosolic phospholipase A2. Biol Pharm Bull 2004;27:1168-73. (Pubitemid 41701705)
55. Hønger T, Jørgensen K, Biltonen RL, Mouritsen OG. Systematic relationship between phospholipase A2 activity and dynamic lipid bilayer microheterogeneity. Biochemistry 1996;35:9003-6. (Pubitemid 26249845)
56. Ahyayauch H, Villar A V, Alonso A, Goñi FM. Modulation of PI-specific phospholipase C by membrane curvature and molecular order. Biochemistry 2005;44:11592-600. (Pubitemid 41209095)
57. Calderwood SK, Stevenson MA, Price BD. Activation of phospholipase C by heat shock requires GTP analogs and is resistant to pertussis toxin. J Cell Physiol 1993;156:153-9. (Pubitemid 23211274)
58. Samples BL, Pool GL, Lumb RH. Polyunsaturated fatty acids enhance the heat induced stress response in rainbow trout (Oncorhynchus mykiss) leukocytes. Comp Biochem Physiol B Biochem Mol Biol 1999;123:389-97. (Pubitemid 29414778)
59. Corda D, Zizza P, Varone A, Filippi BM, Mariggiò S. The glycerophosphoinositols: Cellular metabolism and biological functions. Cell Mol Life Sci 2009;66:3449-67.
60. Wymann MP, Schneiter R. Lipid signalling in disease. Nat Rev Mol Cell Biol 2008;9:162-76. (Pubitemid 351158917)
61. Calderwood SK, Stevenson MA, Hahn GM. Heat stress stimulates inositol trisphosphate release and phosphorylation of phosphoinositides in CHO and Balb C 3T3 cells. J Cell Physiol 1987;130: 369-76. (Pubitemid 17051288)
62. Kiang JG, Tsokos GC. Heat shock protein 70 kDa: Molecular biology, biochemistry, and physiology. Pharmacol Ther 1998;80: 183-201. (Pubitemid 28498227)
63. Wakelam MJ. Diacylglycerol - When is it an intracellular messenger? Biochim Biophys Acta 1998;1436:117-26.
64. Escribá P V, González-Ros JM, Goñ i FM, Kinnunen PKJ, Vigh L, Sánchez-Magraner L, et al. Membranes: A meeting point for lipids, proteins and therapies. J Cell Mol Med 2008;12:829-75. (Pubitemid 351718066)
65. Griner EM, Kazanietz MG. Protein kinase C and other diacylglycerol effectors in cancer. Nat Rev Cancer 2007;7:281-94. (Pubitemid 46480971)
66. Shimizu T, Yokotani K. Bidirectional roles of the brain 2-arachidonoyl-sn-glycerol in the centrally administered vasopressin-induced adrenomedullary outflow in rats. Eur J Pharmacol 2008;582:62-9.
67. Tang X, Edwards EM, Holmes BB, Falck JR, Campbell WB. Role of phospholipase C and diacylglyceride lipase pathway in arachidonic acid release and acetylcholine-induced vascular relaxation in rabbit aorta. Am J Physiol Heart Circ Physiol 2006;290: H37-45.
68. Chau LY, Tai HH. Release of arachidonate from diglyceride in human platelets requires the sequential action of a diglyceride lipase and a monoglyceride lipase. Biochem Biophys Res Commun 1981;100:1688-95. (Pubitemid 11026067)
69. Jurivich DA, Pachetti C, Qiu L, Welk JF. Salicylate triggers heat shock factor differently than heat. J Biol Chem 1995;270:24489-95.
70. Noonan EJ, Place RF, Rasoulpour RJ, Giardina C, Hightower LE. Cell number-dependent regulation of Hsp70B' expression: Evidence of an extracellular regulator. J Cell Physiol 2007;210: 201-11. (Pubitemid 44904716)
71. Koklic T, Pirs M, Zeisig R, Abramović Z, Sentjurc M. Membrane switch hypothesis. 1. Cell density influences lateral domain structure of tumor cell membranes. J Chem Inf Model 2005;45: 1701-7. (Pubitemid 41784743)
72. Menendez JA, Lupu R. Fatty acid synthase and the lipogenic phenotype in cancer pathogenesis. Nat Rev Cancer 2007;7:763-77. (Pubitemid 47469806)
73. Hønger T, Jørgensen K, Biltonen RL, Mouritsen OG. Systematic relationship between phospholipase A2 activity and dynamic lipid bilayer microheterogeneity. Biochemistry 1996;35:9003-6. (Pubitemid 26249845)
74. Fernandis AZ, Wenk MR. Lipid-based biomarkers for cancer. J Chromatogr B Analyt Technol Biomed Life Sci 2009;877:2830-5.
75. Klose C, Surma MA, Simons K. Organellar lipidomics-background and perspectives. Curr Opin Cell Biol 2013. doi: 10.1016/j.ceb.2013.03.005.
76. Anderson RL, Tao TW, Betten DA, Hahn GM. Heat shock protein levels are not elevated in heat-resistant B16 melanoma cells. Radiat Res 1986;105:240-6. (Pubitemid 16125008)
77. Swan TM, Watson K. Stress tolerance in a yeast lipid mutant: membrane lipids influence tolerance to heat and ethanol independently of heat shock proteins and trehalose. Can J Microbiol 1999; 45:472-9.
78. Redman CA, Kennington S, Spathopoulou T, Kusel JR. Interconversion of sphingomyelin and ceramide in adult Schistosoma mansoni. Mol Biochem Parasitol 1997;90:145-53. (Pubitemid 28044384)
79. Nakamoto H, Vigh L. The small heat shock proteins and their clients. Cell Mol Life Sci 2007;64:294-306. (Pubitemid 46440201)
80. Horváth I, Multhoff G, Sonnleitner A, Vígh L. Membraneassociated stress proteins: More than simply chaperones. Biochim Biophys Acta 2008;1778:1653-64.
81. Horváth I, Vígh L. Cell biology: Stability in times of stress. Nature 2010;463:436-8.
82. Török Z, Horváth I, Goloubinoff P, Kovács E, Glatz A, Balogh G, et al. Evidence for a lipochaperonin: Association of active protein-folding GroESL oligomers with lipids can stabilize membranes under heat shock conditions. Proc Natl Acad Sci USA 1997; 94:2192-7. (Pubitemid 27136850)
83. Török Z, Goloubinoff P, Horváth I, Tsvetkova NM, Glatz A, Balogh G, et al. Synechocystis Hsp17 is an amphitropic protein that stabilizes heat-stressed membranes and binds denatured proteins for subsequent chaperone-mediated refolding. Proc Natl Acad Sci USA 2001;98:3098-103. (Pubitemid 32220805)
84. Balogi Z, Török Z, Balogh G, Jósvay K, Shigapova N, Vierling E, et al. Heat shock lipid in cyanobacteria during heat/ lightacclimation. Arch Biochem Biophys 2005;436:346-54. (Pubitemid 40576274)
85. Balogi Z, Cheregi O, Giese KC, Juhász K, Vierling E, Vass I, et al. A mutant small heat shock protein with increased thylakoid association provides an elevated resistance against UV-B damage in Synechocystis 6803. J Biol Chem 2008;283:22983-91.
86. Tsvetkova NM, Horváth I, Török Z, Wolkers WF, Balogi Z, Shigapova N, et al. Small heat-shock proteins regulate membrane lipid polymorphism. Proc Natl Acad Sci USA 2002;99:13504-9. (Pubitemid 35215411)
87. Török Z, Pilbat AM, Gombos I, Hocsák E, Sümegi B, Horváth I, et al. Evidence on cholesterol-controlled lipid raft interaction of the small heat shock protein HSPB11. In: Henderson B, Pockley AG, editors. Cellular Trafficking of Cell Stress Proteins in Health and Disease. Dordrecht: Springer; 2012.
88. Kirkegaard T, Roth AG, Petersen NHT, Mahalka AK, Olsen OD, Moilanen I, et al. Hsp70 stabilizes lysosomes and reverts Niemann-Pick disease-associated lysosomal pathology. Nature 2010;463: 549-53.
89. Juhász K, Thuenauer R, Spachinger A, Duda E, Horváth I, Vígh L, et al. Lysosomal rerouting of Hsp70 trafficking as a potential immune activating tool for targeting melanoma. Curr Pharm Des 2013;19:430-40.
90. Carracedo A, Cantley LC, Pandolfi PP. Cancer metabolism: Fatty acid oxidation in the limelight. Nat Rev Cancer 2013;13:227-32.
91. Gabai VL, Sherman MY. Invited review: Interplay between molecular chaperones and signaling pathways in survival of heat shock. J Appl Physiol 2002;92:1743-8. (Pubitemid 34670933)