Lipid rafts as major platforms for signaling regulation in cancer

Advances in Biological Regulation

Volumn 57, Issue , 2015, Pages 130-146

  Mollinedo, Faustino ^a,b   Gajate, Consuelo ^a,b  

^a UNIVERSITY OF SALAMANCA   (Spain)

^b HOSPITAL UNIVERSITARIO DE SALAMANCA   (Spain)

Author keywords

Cancer; CASMER; Fas CD95; IGF I PI3K Akt signaling; Lipid rafts; Signal transduction

Indexed keywords

ANTINEOPLASTIC AGENT; EDELFOSINE; ETHER PHOSPHOLIPID; TUMOR PROTEIN;

ANIMAL; APOPTOSIS; CELL MEMBRANE; CELL SURVIVAL; DRUG EFFECTS; GENETICS; HUMAN; LYMPHOMA, MANTLE-CELL; METABOLISM; PATHOLOGY; PHYSIOLOGY; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL SURVIVAL; HUMANS; LYMPHOMA, MANTLE-CELL; MEMBRANE MICRODOMAINS; NEOPLASM PROTEINS; PHOSPHOLIPID ETHERS; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

EID: 84920916855     PISSN: 22124926     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jbior.2014.10.003     Document Type: Review

References (164)

1. Abroun S., Ishikawa H., Tsuyama N., Liu S., Li F.J., Otsuyama K., et al. Receptor synergy of interleukin-6 (IL-6) and insulin-like growth factor-I in myeloma cells that highly express IL-6 receptor alpha. Blood 2004, 103:2291-2298.
2. Adam R.M., Mukhopadhyay N.K., Kim J., Di Vizio D., Cinar B., Boucher K., et al. Cholesterol sensitivity of endogenous and myristoylated Akt. Cancer Res 2007, 67:6238-6246.
3. Ashcroft M., Ludwig R.L., Woods D.B., Copeland T.D., Weber H.O., MacRae E.J., et al. Phosphorylation of HDM2 by Akt. Oncogene 2002, 21:1955-1962.
4. Ashkenazi A., Dixit V.M. Death receptors: signaling and modulation. Science 1998, 281:1305-1308.
5. Azrolan N.I., Coleman P.S. Adiscoordinate increase in the cellular amount of 3-hydroxy-3-methylglutaryl-CoA reductase results in the loss of rate-limiting control over cholesterogenesis in a tumour cell-free system. Biochem J 1989, 258:421-425.
6. Bardou M., Barkun A., Martel M. Effect of statin therapy on colorectal cancer. Gut 2010, 59:1572-1585.
7. Baserga R., Peruzzi F., Reiss K. The IGF-1 receptor in cancer biology. Int J Cancer 2003, 107:873-877.
8. Beneteau M., Pizon M., Chaigne-Delalande B., Daburon S., Moreau P., De Giorgi F., et al. Localization of Fas/CD95 into the lipid rafts on down-modulation of the phosphatidylinositol 3-kinase signaling pathway. Mol Cancer Res 2008, 6:604-613.
9. Bodmer J.L., Holler N., Reynard S., Vinciguerra P., Schneider P., Juo P., et al. TRAIL receptor-2 signals apoptosis through FADD and caspase-8. Nat Cell Biol 2000, 2:241-243.
10. Boldin M.P., Goncharov T.M., Goltsev Y.V., Wallach D. Involvement of MACH, a novel MORT1/FADD-interacting protease, in Fas/APO-1- and TNF receptor-induced cell death. Cell 1996, 85:803-815.
11. Brazil D.P., Hemmings B.A. Ten years of protein kinase B signalling: a hard Akt to follow. Trends Biochem Sci 2001, 26:657-664.
12. Brown D.A., London E. Structure of detergent-resistant membrane domains: does phase separation occur in biological membranes?. Biochem Biophys Res Commun 1997, 240:1-7.
13. Brown D.A., London E. Functions of lipid rafts in biological membranes. Annu Rev Cell Dev Biol 1998, 14:111-136.
14. Brown D.A., London E. Structure and function of sphingolipid- and cholesterol-rich membrane rafts. JBiol Chem 2000, 275:17221-17224.
15. Brunet A., Bonni A., Zigmond M.J., Lin M.Z., Juo P., Hu L.S., et al. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 1999, 96:857-868.
16. Cardone M.H., Roy N., Stennicke H.R., Salvesen G.S., Franke T.F., Stanbridge E., et al. Regulation of cell death protease caspase-9 by phosphorylation. Science 1998, 282:1318-1321.
17. Courtney K.D., Corcoran R.B., Engelman J.A. The PI3K pathway as drug target in human cancer. JClin Oncol 2010, 28:1075-1083.
18. Crowell J.A., Steele V.E., Fay J.R. Targeting the AKT protein kinase for cancer chemoprevention. Mol Cancer Ther 2007, 6:2139-2148.
19. Cuesta-Marban A., Botet J., Czyz O., Cacharro L.M., Gajate C., Hornillos V., et al. Drug uptake, lipid rafts, and vesicle trafficking modulate resistance to an anticancer lysophosphatidylcholine analogue in yeast. JBiol Chem 2013, 288:8405-8418.
20. Czyz O., Bitew T., Cuesta-Marban A., McMaster C.R., Mollinedo F., Zaremberg V. Alteration of plasma membrane organization by an anticancer lysophosphatidylcholine analogue induces intracellular acidification and internalization of plasma membrane transporters in yeast. JBiol Chem 2013, 288:8419-8432.
21. Chan F.K., Chun H.J., Zheng L., Siegel R.M., Bui K.L., Lenardo M.J. Adomain in TNF receptors that mediates ligand-independent receptor assembly and signaling. Science 2000, 288:2351-2354.
22. Chapuis N., Tamburini J., Cornillet-Lefebvre P., Gillot L., Bardet V., Willems L., et al. Autocrine IGF-1/IGF-1R signaling is responsible for constitutive PI3K/Akt activation in acute myeloid leukemia: therapeutic value of neutralizing anti-IGF-1R antibody. Haematologica 2010, 95:415-423.
23. Chinnaiyan A.M., O'Rourke K., Tewari M., Dixit V.M. FADD, a novel death domain-containing protein, interacts with the death domain of Fas and initiates apoptosis. Cell 1995, 81:505-512.
24. Dal Col J., Zancai P., Terrin L., Guidoboni M., Ponzoni M., Pavan A., et al. Distinct functional significance of Akt and mTOR constitutive activation in mantle cell lymphoma. Blood 2008, 111:5142-5151.
25. Dan H.C., Sun M., Kaneko S., Feldman R.I., Nicosia S.V., Wang H.G., et al. Akt phosphorylation and stabilization of X-linked inhibitor of apoptosis protein (XIAP). JBiol Chem 2004, 279:5405-5412.
26. Delmas D., Rebe C., Lacour S., Filomenko R., Athias A., Gambert P., et al. Resveratrol-induced apoptosis is associated with Fas redistribution in the rafts and the formation of a death-inducing signaling complex in colon cancer cells. JBiol Chem 2003, 278:41482-41490.
27. Delmas D., Rebe C., Micheau O., Athias A., Gambert P., Grazide S., et al. Redistribution of CD95, DR4 and DR5 in rafts accounts for the synergistic toxicity of resveratrol and death receptor ligands in colon carcinoma cells. Oncogene 2004, 23:8979-8986.
28. Demierre M.F., Higgins P.D., Gruber S.B., Hawk E., Lippman S.M. Statins and cancer prevention. Nat Rev Cancer 2005, 5:930-942.
29. Dessi S., Batetta B., Pulisci D., Spano O., Anchisi C., Tessitore L., et al. Cholesterol content in tumor tissues is inversely associated with high-density lipoprotein cholesterol in serum in patients with gastrointestinal cancer. Cancer 1994, 73:253-258.
30. Di Vizio D., Solomon K.R., Freeman M.R. Cholesterol and cholesterol-rich membranes in prostate cancer: an update. Tumori 2008, 94:633-639.
31. Downward J. How BAD phosphorylation is good for survival. Nat Cell Biol 1999, 1:E33-E35.
32. Drab M., Verkade P., Elger M., Kasper M., Lohn M., Lauterbach B., et al. Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 2001, 293:2449-2452.
33. Eggeling C., Ringemann C., Medda R., Schwarzmann G., Sandhoff K., Polyakova S., et al. Direct observation of the nanoscale dynamics of membrane lipids in a living cell. Nature 2009, 457:1159-1162.
34. El-Shewy H.M., Luttrell L.M. Insulin-like growth factor-2/mannose-6 phosphate receptors. Vitam Horm 2009, 80:667-697.
35. Farwell W.R., Scranton R.E., Lawler E.V., Lew R.A., Brophy M.T., Fiore L.D., et al. The association between statins and cancer incidence in a veterans population. JNatl Cancer Inst 2008, 100:134-139.
36. Feldman M.E., Apsel B., Uotila A., Loewith R., Knight Z.A., Ruggero D., et al. Active-site inhibitors of mTOR target rapamycin-resistant outputs of mTORC1 and mTORC2. PLoS Biol 2009, 7:e38.
37. Franke T.F. PI3K/Akt: getting it right matters. Oncogene 2008, 27:6473-6488.
38. Frattali A.L., Pessin J.E. Relationship between alpha subunit ligand occupancy and beta subunit autophosphorylation in insulin/insulin-like growth factor-1 hybrid receptors. JBiol Chem 1993, 268:7393-7400.
39. Freeman M.R., Solomon K.R. Cholesterol and prostate cancer. JCell Biochem 2004, 91:54-69.
40. Gajate C., Fonteriz R.I., Cabaner C., Alvarez-Noves G., Alvarez-Rodriguez Y., Modolell M., et al. Intracellular triggering of Fas, independently of FasL, as a new mechanism of antitumor ether lipid-induced apoptosis. Int J Cancer 2000, 85:674-682.
41. 3 induces apoptosis through translocation and capping of Fas/CD95 into membrane rafts in human leukemic cells. Blood 2001, 98:3860-3863.
42. 3 (Edelfosine), a proapoptotic agent in tumor cells. Curr Drug Metab 2002, 3:491-525.
43. Gajate C., Del Canto-Janez E., Acuna A.U., Amat-Guerri F., Geijo E., Santos-Beneit A.M., et al. Intracellular triggering of Fas aggregation and recruitment of apoptotic molecules into Fas-enriched rafts in selective tumor cell apoptosis. JExp Med 2004, 200:353-365.
44. Gajate C., Mollinedo F. Cytoskeleton-mediated death receptor and ligand concentration in lipid rafts forms apoptosis-promoting clusters in cancer chemotherapy. JBiol Chem 2005, 280:11641-11647.
45. Gajate C., Mollinedo F. Edelfosine and perifosine induce selective apoptosis in multiple myeloma by recruitment of death receptors and downstream signaling molecules into lipid rafts. Blood 2007, 109:711-719.
46. Gajate C., Gonzalez-Camacho F., Mollinedo F. Lipid raft connection between extrinsic and intrinsic apoptotic pathways. Biochem Biophys Res Commun 2009, 380:780-784.
47. Gajate C., Gonzalez-Camacho F., Mollinedo F. Involvement of raft aggregates enriched in Fas/CD95 death-inducing signaling complex in the antileukemic action of edelfosine in Jurkat cells. PLoS ONE 2009, 4:e5044.
48. Gajate C., Mollinedo F. Lipid rafts, endoplasmic reticulum and mitochondria in the antitumor action of the alkylphospholipid analog edelfosine. Anticancer Agents Med Chem 2014, 14:509-527.
49. Gao X., Zhang J. Spatiotemporal analysis of differential Akt regulation in plasma membrane microdomains. Mol Biol Cell 2008, 19:4366-4373.
50. Gao X., Zhang J. Akt signaling dynamics in plasma membrane microdomains visualized by FRET-based reporters. Commun Integr Biol 2009, 2:32-34.
51. Gao X., Lowry P.R., Zhou X., Depry C., Wei Z., Wong G.W., et al. PI3K/Akt signaling requires spatial compartmentalization in plasma membrane microdomains. Proc Natl Acad Sci U S A 2011, 108:14509-14514.
52. Giovannucci E. Insulin, insulin-like growth factors and colon cancer: a review of the evidence. JNutr 2001, 131:3109S-3120S.
53. Gonyeau M.J., Yuen D.W. Aclinical review of statins and cancer: helpful or harmful?. Pharmacotherapy 2010, 30:177-194.
54. Graaf M.R., Beiderbeck A.B., Egberts A.C., Richel D.J., Guchelaar H.J. The risk of cancer in users of statins. JClin Oncol 2004, 22:2388-2394.
55. Hankinson S.E., Willett W.C., Colditz G.A., Hunter D.J., Michaud D.S., Deroo B., et al. Circulating concentrations of insulin-like growth factor-I and risk of breast cancer. Lancet 1998, 351:1393-1396.
56. Heerklotz H. Triton promotes domain formation in lipid raft mixtures. Biophys J 2002, 83:2693-2701.
57. Ho Y.K., Smith R.G., Brown M.S., Goldstein J.L. Low-density lipoprotein (LDL) receptor activity in human acute myelogenous leukemia cells. Blood 1978, 52:1099-1114.
58. Holtzman E.J., Yaari S., Goldbourt U. Serum cholesterol and the risk of colorectal cancer. NEngl J Med 1987, 317:114.
59. Hong S., Huo H., Xu J., Liao K. Insulin-like growth factor-1 receptor signaling in 3T3-L1 adipocyte differentiation requires lipid rafts but not caveolae. Cell Death Differ 2004, 11:714-723.
60. Hueber A.O., Bernard A.M., Herincs Z., Couzinet A., He H.T. An essential role for membrane rafts in the initiation of Fas/CD95-triggered cell death in mouse thymocytes. EMBO Rep 2002, 3:190-196.
61. Huo H., Guo X., Hong S., Jiang M., Liu X., Liao K. Lipid rafts/caveolae are essential for insulin-like growth factor-1 receptor signaling during 3T3-L1 preadipocyte differentiation induction. JBiol Chem 2003, 278:11561-11569.
62. Ikonen E. Roles of lipid rafts in membrane transport. Curr Opin Cell Biol 2001, 13:470-477.
63. Itoh N., Yonehara S., Ishii A., Yonehara M., Mizushima S., Sameshima M., et al. The polypeptide encoded by the cDNA for human cell surface antigen Fas can mediate apoptosis. Cell 1991, 66:233-243.
64. Itoh N., Nagata S. Anovel protein domain required for apoptosis. Mutational analysis of human Fas antigen. JBiol Chem 1993, 268:10932-10937.
65. Jhanwar-Uniyal M., Jeevan D., Neil J., Shannon C., Albert L., Murali R. Deconstructing mTOR complexes in regulation of Glioblastoma Multiforme and its stem cells. Adv Biol Regul 2013, 53:202-210.
66. Jones J.I., Clemmons D.R. Insulin-like growth factors and their binding proteins: biological actions. Endocr Rev 1995, 16:3-34.
67. Jowett M. The phosphatide and cholesterol contents of normal and malignant human tissues. Biochem J 1931, 25:1991-1998.
68. Karnovsky M.J., Kleinfeld A.M., Hoover R.L., Klausner R.D. The concept of lipid domains in membranes. JCell Biol 1982, 94:1-6.
69. Kato H., Faria T.N., Stannard B., Roberts C.T., LeRoith D. Essential role of tyrosine residues 1131, 1135, and 1136 of the insulin-like growth factor-I (IGF-I) receptor in IGF-I action. Mol Endocrinol 1994, 8:40-50.
70. Kischkel F.C., Hellbardt S., Behrmann I., Germer M., Pawlita M., Krammer P.H., et al. Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. Embo J 1995, 14:5579-5588.
71. Kischkel F.C., Lawrence D.A., Chuntharapai A., Schow P., Kim K.J., Ashkenazi A. Apo2L/TRAIL-dependent recruitment of endogenous FADD and caspase-8 to death receptors 4 and 5. Immunity 2000, 12:611-620.
72. Kolanjiappan K., Ramachandran C.R., Manoharan S. Biochemical changes in tumor tissues of oral cancer patients. Clin Biochem 2003, 36:61-65.
73. Kritchevsky S.B., Kritchevsky D. Serum cholesterol and cancer risk: an epidemiologic perspective. Annu Rev Nutr 1992, 12:391-416.
74. Kusumi A., Koyama-Honda I., Suzuki K. Molecular dynamics and interactions for creation of stimulation-induced stabilized rafts from small unstable steady-state rafts. Traffic 2004, 5:213-230.
75. Lacour S., Hammann A., Grazide S., Lagadic-Gossmann D., Athias A., Sergent O., et al. Cisplatin-induced CD95 redistribution into membrane lipid rafts of HT29 human colon cancer cells. Cancer Res 2004, 64:3593-3598.
76. Lasserre R., Guo X.J., Conchonaud F., Hamon Y., Hawchar O., Bernard A.M., et al. Raft nanodomains contribute to Akt/PKB plasma membrane recruitment and activation. Nat Chem Biol 2008, 4:538-547.
77. Laurent P.A., Severin S., Gratacap M.P., Payrastre B. Class I PI 3-kinases signaling in platelet activation and thrombosis: PDK1/Akt/GSK3 axis and impact of PTEN and SHIP1. Adv Biol Regul 2014, 54:162-174.
78. Lenne P.F., Wawrezinieck L., Conchonaud F., Wurtz O., Boned A., Guo X.J., et al. Dynamic molecular confinement in the plasma membrane by microdomains and the cytoskeleton meshwork. Embo J 2006, 25:3245-3256.
79. Li Y.C., Park M.J., Ye S.K., Kim C.W., Kim Y.N. Elevated levels of cholesterol-rich lipid rafts in cancer cells are correlated with apoptosis sensitivity induced by cholesterol-depleting agents. Am J Pathol 2006, 168:1107-1118. quiz 404-5.
80. Lichtenberg D., Goni F.M., Heerklotz H. Detergent-resistant membranes should not be identified with membrane rafts. Trends Biochem Sci 2005, 30:430-436.
81. Lingwood D., Simons K. Detergent resistance as a tool in membrane research. Nat Protoc 2007, 2:2159-2165.
82. Liu P., Rudick M., Anderson R.G. Multiple functions of caveolin-1. JBiol Chem 2002, 277:41295-41298.
83. Ma J., Pollak M.N., Giovannucci E., Chan J.M., Tao Y., Hennekens C.H., et al. Prospective study of colorectal cancer risk in men and plasma levels of insulin-like growth factor (IGF)-I and IGF-binding protein-3. JNatl Cancer Inst 1999, 91:620-625.
84. Malaguarnera R., Belfiore A. The emerging role of insulin and insulin-like growth factor signaling in cancer stem cells. Front Endocrinol (Lausanne) 2014, 5:10.
85. Marcella S.W., David A., Ohman-Strickland P.A., Carson J., Rhoads G.G. Statin use and fatal prostate cancer: a matched case-control study. Cancer 2012, 118:4046-4052.
86. Marguet D., Lenne P.F., Rigneault H., He H.T. Dynamics in the plasma membrane: how to combine fluidity and order. Embo J 2006, 25:3446-3457.
87. Matthews L.C., Taggart M.J., Westwood M. Effect of cholesterol depletion on mitogenesis and survival: the role of caveolar and noncaveolar domains in insulin-like growth factor-mediated cellular function. Endocrinology 2005, 146:5463-5473.
88. Maxfield F.R. Plasma membrane microdomains. Curr Opin Cell Biol 2002, 14:483-487.
89. Mesquita R.M., Melo E., Thompson T.E., Vaz W.L. Partitioning of amphiphiles between coexisting ordered and disordered phases in two-phase lipid bilayer membranes. Biophys J 2000, 78:3019-3025.
90. 3 (edelfosine): a selective antitumour lipid targeting apoptosis through intracellular activation of Fas/CD95 death receptor. Curr Med Chem 2004, 11:3163-3184.
91. Mollinedo F., Gajate C. Fas/CD95 death receptor and lipid rafts: new targets for apoptosis-directed cancer therapy. Drug Resist Updat 2006, 9:51-73.
92. Mollinedo F., Gajate C. FasL-independent activation of Fas. Fas signaling 2006, 13-27. Landes Bioscience and Springer Science, Georgetown, TX, [Chapter 2]. H. Wajant (Ed.).
93. Mollinedo F. Antitumor ether lipids: proapoptotic agents with multiple therapeutic indications. Expert Opin Ther Pat 2007, 17:385-405.
94. Mollinedo F., de la Iglesia-Vicente J., Gajate C., Estella-Hermoso de Mendoza A., Villa-Pulgarin J.A., Campanero M.A., et al. Lipid raft-targeted therapy in multiple myeloma. Oncogene 2010, 29:3748-3757.
95. Mollinedo F., de la Iglesia-Vicente J., Gajate C., Estella-Hermoso de Mendoza A., Villa-Pulgarin J.A., de Frias M., et al. Invitro and invivo selective antitumor activity of Edelfosine against mantle cell lymphoma and chronic lymphocytic leukemia involving lipid rafts. Clin Cancer Res 2010, 16:2046-2054.
96. Mollinedo F., Gajate C. Lipid rafts and clusters of apoptotic signaling molecule-enriched rafts in cancer therapy. Future Oncol 2010, 6:811-821.
97. Mollinedo F., Gajate C. Lipid rafts, death receptors and CASMERs: new insights for cancer therapy. Future Oncol 2010, 6:491-494.
98. Mollinedo F. Editorial: antitumor alkylphospholipid analogs: a promising and growing family of synthetic cell membrane-targeting molecules for cancer treatment. Anticancer Agents Med Chem 2014, 14:495-498.
99. Munro S. Lipid rafts: elusive or illusive?. Cell 2003, 115:377-388.
100. Nagata S. Apoptosis by death factor. Cell 1997, 88:355-365.
101. Norris P.C., Dennis E.A. Alipidomic perspective on inflammatory macrophage eicosanoid signaling. Adv Biol Regul 2014, 54:99-110.
102. Oates A.J., Schumaker L.M., Jenkins S.B., Pearce A.A., DaCosta S.A., Arun B., et al. The mannose 6-phosphate/insulin-like growth factor 2 receptor (M6P/IGF2R), a putative breast tumor suppressor gene. Breast Cancer Res Treat 1998, 47:269-281.
103. Okamoto T., Schlegel A., Scherer P.E., Lisanti M.P. Caveolins, a family of scaffolding proteins for organizing "preassembled signaling complexes" at the plasma membrane. JBiol Chem 1998, 273:5419-5422.
104. Ozes O.N., Mayo L.D., Gustin J.A., Pfeffer S.R., Pfeffer L.M., Donner D.B. NF-kappaB activation by tumour necrosis factor requires the Akt serine-threonine kinase. Nature 1999, 401:82-85.
105. Panetta D., Biedi C., Repetto S., Cordera R., Maggi D. IGF-I regulates caveolin 1 and IRS1 interaction in caveolae. Biochem Biophys Res Commun 2004, 316:240-243.
106. Patra S.K. Dissecting lipid raft facilitated cell signaling pathways in cancer. Biochim Biophys Acta 2008, 1785:182-206.
107. Pelton K., Freeman M.R., Solomon K.R. Cholesterol and prostate cancer. Curr Opin Pharmacol 2012, 12:751-759.
108. Pike L.J. Lipid rafts: heterogeneity on the high seas. Biochem J 2004, 378:281-292.
109. Pike L.J. Rafts defined: a report on the Keystone Symposium on Lipid Rafts and Cell Function. JLipid Res 2006, 47:1597-1598.
110. Pinaud F., Michalet X., Iyer G., Margeat E., Moore H.P., Weiss S. Dynamic partitioning of a glycosyl-phosphatidylinositol-anchored protein in glycosphingolipid-rich microdomains imaged by single-quantum dot tracking. Traffic 2009, 10:691-712.
111. Platz E.A., Leitzmann M.F., Visvanathan K., Rimm E.B., Stampfer M.J., Willett W.C., et al. Statin drugs and risk of advanced prostate cancer. JNatl Cancer Inst 2006, 98:1819-1825.
112. Pollak M.N., Schernhammer E.S., Hankinson S.E. Insulin-like growth factors and neoplasia. Nat Rev Cancer 2004, 4:505-518.
113. Qi X.J., Wildey G.M., Howe P.H. Evidence that Ser87 of BimEL is phosphorylated by Akt and regulates BimEL apoptotic function. JBiol Chem 2006, 281:813-823.
114. Raghu H., Sodadasu P.K., Malla R.R., Gondi C.S., Estes N., Rao J.S. Localization of uPAR and MMP-9 in lipid rafts is critical for migration, invasion and angiogenesis in human breast cancer cells. BMC Cancer 2010, 10:647.
115. Razani B., Engelman J.A., Wang X.B., Schubert W., Zhang X.L., Marks C.B., et al. Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities. JBiol Chem 2001, 276:38121-38138.
116. Reis-Sobreiro M., Gajate C., Mollinedo F. Involvement of mitochondria and recruitment of Fas/CD95 signaling in lipid rafts in resveratrol-mediated antimyeloma and antileukemia actions. Oncogene 2009, 28:3221-3234.
117. Reis-Sobreiro M., Roue G., Moros A., Gajate C., de la Iglesia-Vicente J., Colomer D., et al. Lipid raft-mediated Akt signaling as a therapeutic target in mantle cell lymphoma. Blood Cancer J 2013, 3:e118.
118. Remacle-Bonnet M., Garrouste F., Baillat G., Andre F., Marvaldi J., Pommier G. Membrane rafts segregate pro- from anti-apoptotic insulin-like growth factor-I receptor signaling in colon carcinoma cells stimulated by members of the tumor necrosis factor superfamily. Am J Pathol 2005, 167:761-773.
119. Rieder S., Michalski C.W., Friess H., Kleeff J. Insulin-like growth factor signaling as a therapeutic target in pancreatic cancer. Anticancer Agents Med Chem 2011, 11:427-433.
120. Romanelli R.J., Mahajan K.R., Fulmer C.G., Wood T.L. Insulin-like growth factor-I-stimulated Akt phosphorylation and oligodendrocyte progenitor cell survival require cholesterol-enriched membranes. JNeurosci Res 2009, 87:3369-3377.
121. Rossig L., Jadidi A.S., Urbich C., Badorff C., Zeiher A.M., Dimmeler S. Akt-dependent phosphorylation of p21(Cip1) regulates PCNA binding and proliferation of endothelial cells. Mol Cell Biol 2001, 21:5644-5657.
122. Rowinsky E.K., Youssoufian H., Tonra J.R., Solomon P., Burtrum D., Ludwig D.L. IMC-A12, a human IgG1 monoclonal antibody to the insulin-like growth factor I receptor. Clin Cancer Res 2007, 13:5549s-5555s.
123. Rudelius M., Pittaluga S., Nishizuka S., Pham T.H., Fend F., Jaffe E.S., et al. Constitutive activation of Akt contributes to the pathogenesis and survival of mantle cell lymphoma. Blood 2006, 108:1668-1676.
124. Ryan P.D., Goss P.E. The emerging role of the insulin-like growth factor pathway as a therapeutic target in cancer. Oncologist 2008, 13:16-24.
125. Scheel-Toellner D., Wang K., Singh R., Majeed S., Raza K., Curnow S.J., et al. The death-inducing signalling complex is recruited to lipid rafts in Fas-induced apoptosis. Biochem Biophys Res Commun 2002, 297:876-879.
126. Schroeder R.J., Ahmed S.N., Zhu Y., London E., Brown D.A. Cholesterol and sphingolipid enhance the Triton X-100 insolubility of glycosylphosphatidylinositol-anchored proteins by promoting the formation of detergent-insoluble ordered membrane domains. JBiol Chem 1998, 273:1150-1157.
127. Schuck S., Honsho M., Ekroos K., Shevchenko A., Simons K. Resistance of cell membranes to different detergents. Proc Natl Acad Sci U S A 2003, 100:5795-5800.
128. Sepp-Lorenzino L. Structure and function of the insulin-like growth factor I receptor. Breast Cancer Res Treat 1998, 47:235-253.
129. Sharma P., Varma R., Sarasij R.C., Ira, Gousset K., Krishnamoorthy G., et al. Nanoscale organization of multiple GPI-anchored proteins in living cell membranes. Cell 2004, 116:577-589.
130. Shukla S., Maclennan G.T., Hartman D.J., Fu P., Resnick M.I., Gupta S. Activation of PI3K-Akt signaling pathway promotes prostate cancer cell invasion. Int J Cancer 2007, 121:1424-1432.
131. Siegel R.M., Chan F.K., Chun H.J., Lenardo M.J. The multifaceted role of Fas signaling in immune cell homeostasis and autoimmunity. Nat Immunol 2000, 1:469-474.
132. Simons K., Ikonen E. Functional rafts in cell membranes. Nature 1997, 387:569-572.
133. Simons K., Toomre D. Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 2000, 1:31-39.
134. Simons K., Gerl M.J. Revitalizing membrane rafts: new tools and insights. Nat Rev Mol Cell Biol 2010, 11:688-699.
135. Singer S.J., Nicolson G.L. The fluid mosaic model of the structure of cell membranes. Science 1972, 175:720-731.
136. Sprick M.R., Weigand M.A., Rieser E., Rauch C.T., Juo P., Blenis J., et al. FADD/MORT1 and caspase-8 are recruited to TRAIL receptors 1 and 2 and are essential for apoptosis mediated by TRAIL receptor 2. Immunity 2000, 12:599-609.
137. Staubach S., Razawi H., Hanisch F.G. Proteomics of MUC1-containing lipid rafts from plasma membranes and exosomes of human breast carcinoma cells MCF-7. Proteomics 2009, 9:2820-2835.
138. Staubach S., Hanisch F.G. Lipid rafts: signaling and sorting platforms of cells and their roles in cancer. Expert Rev Proteomics 2011, 8:263-277.
139. Stel A.J., Ten Cate B., Jacobs S., Kok J.W., Spierings D.C., Dondorff M., et al. Fas receptor clustering and involvement of the death receptor pathway in rituximab-mediated apoptosis with concomitant sensitization of lymphoma B cells to fas-induced apoptosis. JImmunol 2007, 178:2287-2295.
140. Surmacz E. Growth factor receptors as therapeutic targets: strategies to inhibit the insulin-like growth factor I receptor. Oncogene 2003, 22:6589-6597.
141. Tai Y.T., Podar K., Catley L., Tseng Y.H., Akiyama M., Shringarpure R., et al. Insulin-like growth factor-1 induces adhesion and migration in human multiple myeloma cells via activation of beta1-integrin and phosphatidylinositol 3'-kinase/AKT signaling. Cancer Res 2003, 63:5850-5858.
142. Toker A. Achieving specificity in Akt signaling in cancer. Adv Biol Regul 2012, 52:78-87.
143. Toker A., Marmiroli S. Signaling specificity in the Akt pathway in biology and disease. Adv Biol Regul 2014, 55:28-38.
144. Tosi M.R., Bottura G., Lucchi P., Reggiani A., Trinchero A., Tugnoli V. Cholesteryl esters in human malignant neoplasms. Int J Mol Med 2003, 11:95-98.
145. Tosi M.R., Tugnoli V. Cholesteryl esters in malignancy. Clin Chim Acta 2005, 359:27-45.
146. Ullrich A., Gray A., Tam A.W., Yang-Feng T., Tsubokawa M., Collins C., et al. Insulin-like growth factor I receptor primary structure: comparison with insulin receptor suggests structural determinants that define functional specificity. EMBO J 1986, 5:2503-2512.
147. Valentinis B., Baserga R. IGF-I receptor signalling in transformation and differentiation. Mol Pathol 2001, 54:133-137.
148. van Zanten T.S., Cambi A., Garcia-Parajo M.F. Ananometer scale optical view on the compartmentalization of cell membranes. Biochim Biophys Acta 2010, 1798:777-787.
149. Viglietto G., Motti M.L., Bruni P., Melillo R.M., D'Alessio A., Califano D., et al. Cytoplasmic relocalization and inhibition of the cyclin-dependent kinase inhibitor p27(Kip1) by PKB/Akt-mediated phosphorylation in breast cancer. Nat Med 2002, 8:1136-1144.
150. Vyas N., Goswami D., Manonmani A., Sharma P., Ranganath H.A., VijayRaghavan K., et al. Nanoscale organization of hedgehog is essential for long-range signaling. Cell 2008, 133:1214-1227.
151. Wang T.Y., Leventis R., Silvius J.R. Fluorescence-based evaluation of the partitioning of lipids and lipidated peptides into liquid-ordered lipid microdomains: a model for molecular partitioning into "lipid rafts". Biophys J 2000, 79:919-933.
152. Wang T.Y., Silvius J.R. Different sphingolipids show differential partitioning into sphingolipid/cholesterol-rich domains in lipid bilayers. Biophys J 2000, 79:1478-1489.
153. Werner H., Le Roith D. New concepts in regulation and function of the insulin-like growth factors: implications for understanding normal growth and neoplasia. Cell Mol Life Sci 2000, 57:932-942.
154. Werner H. Tumor suppressors govern insulin-like growth factor signaling pathways: implications in metabolism and cancer. Oncogene 2012, 31:2703-2714.
155. Xu L., Qu X., Hu X., Zhu Z., Li C., Li E., et al. Lipid raft-regulated IGF-1R activation antagonizes TRAIL-induced apoptosis in gastric cancer cells. FEBS Lett 2013, 587:3815-3823.
156. Xu Z.X., Ding T., Haridas V., Connolly F., Gutterman J.U. Avicin D, a plant triterpenoid, induces cell apoptosis by recruitment of Fas and downstream signaling molecules into lipid rafts. PLoS One 2009, 4:e8532.
157. Yamaguchi H., Wang H.G. The protein kinase PKB/Akt regulates cell survival and apoptosis by inhibiting Bax conformational change. Oncogene 2001, 20:7779-7786.
158. Yasuda M., Bloor W.R. Lipid content of tumors. JClin Invest 1932, 11:677-682.
159. Yu H., Rohan T. Role of the insulin-like growth factor family in cancer development and progression. JNatl Cancer Inst 2000, 92:1472-1489.
160. Zaremberg V., Gajate C., Cacharro L.M., Mollinedo F., McMaster C.R. Cytotoxicity of an anti-cancer lysophospholipid through selective modification of lipid raft composition. JBiol Chem 2005, 280:38047-38058.
161. Zhang Q., Wakelam M.J. Lipidomics in the analysis of malignancy. Adv Biol Regul 2014, 54:93-98.
162. Zhong L., Zeng G., Lu X., Wang R.C., Gong G., Yan L., et al. NSOM/QD-based direct visualization of CD3-induced and CD28-enhanced nanospatial coclustering of TCR and coreceptor in nanodomains in T cell activation. PLoS ONE 2009, 4:e5945.
163. Zhuang L., Lin J., Lu M.L., Solomon K.R., Freeman M.R. Cholesterol-rich lipid rafts mediate akt-regulated survival in prostate cancer cells. Cancer Res 2002, 62:2227-2231.
164. Zhuang L., Kim J., Adam R.M., Solomon K.R., Freeman M.R. Cholesterol targeting alters lipid raft composition and cell survival in prostate cancer cells and xenografts. JClin Invest 2005, 115:959-968.