Cholesterol lowering: Role in cancer prevention and treatment

Biological Chemistry

Volumn 396, Issue 1, 2015, Pages 1-11

  Murai, Toshiyuki ^a  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

lipid raft; membrane remodeling; metabolic reprogramming; microdomain; tumor invasion; statin

Indexed keywords

CHOLESTEROL; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; HYPOCHOLESTEROLEMIC AGENT;

APOPTOSIS; BREAST CANCER; CANCER CELL; CANCER PREVENTION; CANCER THERAPY; CELL INVASION; CELL MIGRATION; CHOLESTEROL METABOLISM; CHOLESTEROL SYNTHESIS; COLORECTAL CANCER; HUMAN; LIPID RAFT; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; PROSTATE CANCER; REVIEW; SYSTEMIC CIRCULATION; DISEASE COURSE; HYPERCHOLESTEROLEMIA; METABOLISM; NEOPLASMS;

CHOLESTEROL; DISEASE PROGRESSION; HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; HYPERCHOLESTEROLEMIA; NEOPLASMS;

EID: 84914693422     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2014-0194     Document Type: Review

References (100)

1. Adler, E.M. (2011). Lost without a raft. Sci. Signal. 4, ec24.
2. Azrolan, N.I. and Coleman, P.S. (1989). A discoordinate 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. 258, 421-425.
3. Babina, I.S., McSherry, E.A., Donatello, S., Hill, A.D., and Hopkins, A.M. (2014). A novel mechanism of regulating breast cancer cell migration via palmitoylation-dependent alterations in the lipid raft affiliation of CD44. Breast Cancer Res. 16, R19.
4. Baruthio, F., Quadroni, M., Rüegg, C., and Mariotti, A. (2008). Proteomic analysis of membrane rafts of melanoma cells identifies protein patterns characteristic of the tumor progression stage. Proteomics 8, 4733-4747.
5. Berger, T., Ueda, T., Arpaia, E., Chio, I.I.C., Shirdel, E.A., Jurisica, I., Hamada, K., You-Ten, A., Haight, J., Wakeham, A., et al. (2013). Flotillin-2 deficiency leads to reduced lung metastases in a mouse breast cancer model. Oncogene 32, 4989-4994.
6. Bernstein, H., Bernstein, C., Payne, C.M., Dvorakova, K., and Garewal, H. (2005). Bile acids as carcinogens in human gastrointestinal cancers. Mutat. Res. 589, 47-65.
7. Bowie, R.V., Donatello, S., Lyes, C., Owens, M.B., Babina, I.S., Hudson, L., Walsh, S.V., O'Donoghue, D.P., Amu, S., Barry, S.P., et al. (2012). Lipid rafts are disrupted in mildly inflamed intestinal microenvironments without overt disruption of the epithelial barrier. Am. J. Physiol. Gastrointest. Liver Physiol. 302, G781-793.
8. Brown, M.S. and Goldstein, J.L. (2009). Cholesterol feedback: from Schoenheimer's bottle to Scap's MELADL. J. Lipid Res. 50, S15-S27.
9. Brown, D.A. and London, E. (2000). Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J. Biol. Chem. 275, 17221-17224.
10. Causeret, M., Taulet, N., Comunale, F., Favard, C., and Gauthier- Rouvière, C. (2005). N-cadherin association with lipid rafts regulates its dynamic assembly at cell-cell junctions in C2C12 myoblasts. Mol. Biol. Cell 16, 2168-2180.
11. Chetty, C., Lakka, S.S., Bhoopathi, P., Gondi, C.S., Veeravalli, K.K., Fassett, D., Klopfenstein, J.D., Dinh, D.H., Gujrati, M., and Rao, J.S. (2010). Urokinase plasminogen activator receptor and/ or matrix metalloproteinase-9 inhibition induces apoptosis signaling through lipid rafts in glioblastoma xenograft cells. Mol. Cancer Ther. 9, 2605-2617.
12. Clendening, J.W., Pandyra, A., Boutros, P.C., El Ghamrasni, S., Khosravi, F., Trentin, G.A., Martirosyan, A., Hakem, A., Hakem, R., Jurisica, I., et al. (2010). Dysregulation of the mevalonate pathway promotes transformation. Proc. Natl. Acad. Sci. USA 107, 15051-15056.
13. Collins, R., Armitage, J., Parish, S., Sleigh, P., and Peto, R.; Heart Protection Study Collaborative Group (2002). MRC/BHF Heart Protection Study of cholesterol lowering with simvastatin in 20536 high-risk individuals: a randomised placebo-controlled trial. Lancet 360, 7-22.
14. DeBerardinis R.J., Mancuso, A., Daikhin, E., Nissim, I., Yudkoff, M., Wehrli, S., and Thompson, C.B. (2007). Beyond aerobic glycolysis: transformed cells can engage in glutamine metabolism that exceeds the requirement for protein and nucleotide synthesis. Proc. Natl. Acad. Sci. USA 104, 19345-19350.
15. Farwell, W.R., Scranton, R.E., Lawler, E.V., Lew, R.A., Brophy, M.T., Fiore, L.D., and Gaziano, J.M. (2008). The association between statins and cancer incidence in a veterans population. J. Natl. Cancer Inst. 100, 134-139.
16. Fessler, M.B. and Parks, J.S. (2011). Intracellular lipid flux and membrane microdomains as organizing principles in inflammatory cell signaling. J. Immunol. 187, 1529-1535.
17. Foster, L.J., de Hoog, C.L., and Mann, M. (2003). Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc. Natl. Acad. Sci. USA 100, 5813-5818.
18. Freed-Pastor, W.A., Mizuno, H., Zhao, X., Langerød, A., Moon, S.H., Rodriguez-Barrueco, R., Barsotti, A., Chicas, A., Li, W., Polotskaia, A., et al. (2012). Mutant p53 disrupts mammary tissue architecture via the mevalonate pathway. Cell 148, 244-258.
19. Freeman, M.R. and Solomon, K.R. (2004). Cholesterol and prostate cancer. J. Cell. Biochem. 91, 54-69.
20. Gajate, C. and Mollinedo, F. (2001). The antitumor ether lipid ET- 18-OCH3 induces apoptosis through translocation and capping of Fas/CD95 into membrane rafts in human leukemic cells. Blood 98, 3860-3863.
21. Gajate, C. and Mollinedo, F. (2007). Edelfosine and perifosine induce selective apoptosis in multiple myeloma by recruitment of death receptors and downstream signaling molecules into lipid rafts. Blood 109, 711-719.
22. Gajate, C., del Canto-Jañez, E., Acuña, A.U., Amat-Guerri, F., Geijo, E., Santos-Beneit, A.M., Veldman, R.J., and Mollinedo, F. (2004). Intracellular triggering of Fas aggregation and recruitment of apoptotic molecules into Fas-enriched rafts in selective tumor cell apoptosis. J. Exp. Med. 200, 353-365.
23. Gonzalez, R., Carlson, J.P., and Dempsey, M.E. (1979). Two major regulatory steps in cholesterol synthesis by human renal cancer cells. Arch. Biochem. Biophys. 196, 574-580.
24. Grivennikov, S.I. (2013). Inflammation and colorectal cancer: colitisassociated neoplasia. Semin. Immunopathol. 35, 229-244.
25. Hanahan, D. and Weinberg, R.A. (2011). Hallmarks of cancer: the next generation. Cell 144, 646-674.
26. Hanzal-Bayer, M.F. and Hancock, J.F. (2007). Lipid rafts and membrane traffic. FEBS Lett. 581, 2098-2104.
27. Hazarika, P., McCarty, M.F., Prieto, V.G., George, S., Babu, D., Koul, D., Bar-Eli, M., and Duvic, M. (2004). Up-regulation of Flotillin- 2 is associated with melanoma progression and modulates expression of the thrombin receptor protease activated receptor 1. Cancer Res. 64, 7361-7369.
28. Hirsch, H.A., Iliopoulos, D., Joshi, A., Zhang, Y., Jaeger, S.A., Bulyk, M., Tsichlis, P.N., Liu, S., and Struhl, K. (2010). A transcriptional signature and common gene networks link cancer with lipid metabolism and diverse human diseases. Cancer Cell 17, 348-361.
29. Ho, Y.K., Smith, R.G., Brown, M.S., and Goldstein, J.L. (1978). Lowdensity lipoprotein (LDL) receptor activity in human acute myelogenous leukemia cells. Blood 52, 1099-1114.
30. Holtzman, E.J., Yaari, S., and Goldbourt, U. (1987). Serum cholesterol and the risk of colorectal cancer. N. Engl. J. Med. 317, 114.
31. Hu, J., La Vecchia, C., de Groh, M., Negri, E., Morrison, H., and Mery, L.; Canadian Cancer Registries Epidemiology Research Group (2012). Dietary cholesterol intake and cancer. Ann. Oncol. 23, 491-500.
32. Huang, S. and He, X. (2011). The role of microRNAs in liver cancer progression. Br. J. Cancer 104, 235-240.
33. Ibrahim, A.F., Weirauch, U., Thomas, M., Grünweller, A., Hartmann, R.K., and Aigner, A. (2011). MicroRNA replacement therapy for miR-145 and miR-33a is efficacious in a model of colon carcinoma. Cancer Res. 71, 5214-5224.
34. Jiang, G., Freywald, T., Webster, J., Kozan, D., Geyer, R., DeCoteau, J., Narendran, A., and Freywald A. (2008). In human leukemia cells ephrin-B-induced invasive activity is supported by Lck and is associated with reassembling of lipid raft signaling complexes. Mol. Cancer Res. 6, 291-305.
35. Jick, H., Zornberg, G.L., Jick, S.S., Seshadri, S., and Drachman, D.A. (2000). Statins and the risk of dementia. Lancet 356, 1627-1631.
36. Jowett, M. (1931). The phosphatide and cholesterol contents of normal and malignant human tissues. Biochem. J. 25, 1991-1998.
37. Kiberstis, P.A. (2013). Cholesterol and cancer. Sci. Signal. 6, ec292.
38. Kojro, E., Gimpl, G., Lammich, S., März, W., and Fahrenholz, F. (2001). Proc. Natl. Acad. Sci. USA 98, 5815-5820.
39. Kritchevsky, S.B. and Kritchevsky, D. (1992). Serum cholesterol and cancer risk: an epidemiologic perspective. Annu. Rev. Nutr. 12, 391-416.
40. Lesley, J., Hyman, R., and Kincade, P.W. (1993). CD44 and its interaction with extracellular matrix. Adv. Immunol. 54, 271-335.
41. Li, Y.C., Park, M.J., Ye, S.K., Kim, C.W., and Kim, Y.N. (2006). Elevated levels of cholesterol-rich lipid rafts in cancer cells are correlated with apoptosis sensitivity induced by cholesteroldepleting agents. Am. J. Pathol. 168, 1107-1118.
42. Lin, C., Wu, Z., Lin, X., Yu, C., Shi, T., Zeng, Y., Wang, X., Li, J., and Song, L. (2011). Knockdown of FLOT1 impairs cell proliferation and tumorigenicity in breast cancer through upregulation of FOXO3a. Clin. Cancer Res. 17, 3089-3099.
43. Locke, J.A., Guns, E.S., Lubik, A.A., Adomat, H.H., Hendy, S.C., Wood, C.A., Ettinger, S.L., Gleave, M.E., and Nelson, C.C. (2008). Androgen levels increase by intratumoral de novo steroidogenesis during progression of castration-resistant prostate cancer. Cancer Res. 68, 6407-6415.
44. Mathupala, S.P., Ko, Y.H., and Pedersen, P.L. (2006). Hexokinase II: cancer's double-edged sword acting as both facilitator and gatekeeper of malignancy when bound to mitochondria. Oncogene 25, 4777-4786.
45. Matthews, V., Schuster, B., Schütze, S., Bussmeyer, I., Ludwig, A., Hundhausen, C., Sadowski, T., Saftig, P., Hartmann, D., Kallen, K.J., et al. (2003). J. Biol. Chem. 278, 38829-38839.
46. Matoba, S., Kang, J.G., Patino, W.D., Wragg, A., Boehm, M., Gavrilova, O., Hurley, P.J., Bunz, F., and Hwang, P.M. (2006). p53 regulates mitochondrial respiration. Science 312, 1650-1653.
47. Mechtersheimer, S., Gutwein, P., Agmon-Levin, N., Stoeck, A., Oleszewski, M., Riedle, S., Postina, R., Fahrenholz, F., Fogel, M., Lemmon, V., et al. (2001). Ectodomain shedding of L1 adhesion molecule promotes cell migration by autocrine binding to integrins. J. Cell Biol. 155, 661-673.
48. Menendez, J.A. and Lupu, R. (2007). Fatty acid synthase and the lipogenic phenotype in cancer pathogenesis. Nat. Rev. Cancer 7, 763-777.
49. Mollinedo, F., de la Iglesia-Vicente, J., Gajate, C., Estella-Hermoso de Mendoza, A., Villa-Pulgarin, J.A., Campanero, M.A., and Blanco-Prieto, M.J. (2010a). Lipid raft-targeted therapy in multiple myeloma. Oncogene 29, 3748-3757.
50. Mollinedo, F., de la Iglesia-Vicente, J., Gajate, C., Estella-Hermoso de Mendoza, A., Villa-Pulgarin, J.A., de Frias, M., Roué, G., Gil, J., Colomer, D., Campanero, M.A., et al. (2010b). In vitro and in vivo selective antitumor activity of Edelfosine against mantle cell lymphoma and chronic lymphocytic leukemia involving lipid rafts. Clin. Cancer Res. 16, 2046-2054.
51. Moore, K.J., Rayner, K.J., Suárez, Y., and Fandernández-Hernando, C. (2010). microRNAs and cholesterol metabolism. Trends Endocrinol. Metab. 21, 699-706.
52. Mullen, A.R., Wheaton, W.W., Jin, E.S., Chen, P.H., Sullivan, L.B., Cheng, T., Yang, Y., Linehan, W.M., Chandel, N.S., and DeBerardinis, R.J. (2012). Reductive carboxylation supports growth in tumour cells with defective mitochondria. Nature 481, 385-388.
53. Murai, T. (2012). The role of lipid rafts in cancer cell adhesion and migration. Int. J. Cell Biol. 2012, 763283.
54. Murai, T., Miyazaki, Y., Nishinakamura, H., Sugahara, K.N., Miyauchi, T., Sako, Y., Yanagida, T., and Miyasaka, M. (2004). Engagement of CD44 promotes Rac activation and CD44 cleavage during tumor cell migration. J. Biol. Chem. 279, 4541-4550.
55. Murai, T., Miyauchi, T., Yanagida, T., and Sako, Y. (2006). Epidermal growth factor-regulated activation of Rac GTPase enhances CD44 cleavage by metalloproteinase disintegrin ADAM10. Biochem. J. 395, 65-71.
56. Murai, T., Hokonohara, H., Takagi, A., and Kawai, T. (2009). Atomic force microscopy imaging of supramolecular organization of hyaluronan and its receptor CD44. IEEE Trans. NanoBiosci. 8, 294-299.
57. Murai, T., Maruyama, Y., Mio, K., Nishiyama, H., Suga, M., and Sato, C. (2011). Low cholesterol triggers membrane microdomaindependent CD44 shedding and suppresses tumor cell migration. J. Biol. Chem. 286, 1999-2007.
58. Murai, T., Sato, C., Sato, M., Nishiyama, H., Suga, M., Mio, K., and Kawashima, H. (2013a). Membrane cholesterol modulates the hyaluronan-binding ability of CD44 in T lymphocytes and controls rolling under shear flow. J. Cell Sci. 126, 3284-3294.
59. Murai, T., Sato, M., Nishiyama, H., Suga, M., and Sato, C. (2013b). Ultrastructural analysis of nanogold-labeled cell surface microvilli in liquid by atmospheric scanning electron microscopy and their relevance in cell adhesion. Int. J. Mol. Sci. 14, 20809-20819.
60. Nelson, E.R., Wardell, S.E., Jasper, J.S., Park, S., Suchindran, S., Howe, M.K., Carver, N.J., Pillai, R.V., Sullivan, P.M., Sondhi, V., et al. (2013). 27-Hydroxycholesterol links hypercholesterolemia and breast cancer pathophysiology. Science 342, 1094-1097.
61. Nieto-Miguel, T., Gajate, C., Gonzalez-Camacho, F., and Mollinedo, F. (2008). Proapoptotic role of Hsp90 by its interaction with c-Jun N-terminal kinase in lipid rafts in edelfosine-mediated antileukemic therapy. Oncogene 27, 1779-1787.
62. Oneyama, C., Hikita, T., Enya, K., Dobenecker, M.W., Saito, K., Nada, S., Tarakhovsky, A., and Okada, M. (2008). The lipid raftanchored adaptor protein Cbp controls the oncogenic potential of c-Src. Mol. Cell 30, 426-436.
63. Parks, S.K., Chiche, J., and Pouyssegur, J. (2011). pH control mechanisms of tumor survival and growth. J. Cell. Physiol. 226, 299-308.
64. Parton, R.G., Hanzal-Bayer, M., and Hancock, J.F. (2006). Biogenesis of caveolae: a structural model for caveolin-induced domain formation. J. Cell Sci. 119, 787-796.
65. Pelton, K., Freeman, M.R., and Solomon, K.R. (2012). Cholesterol and prostate cancer. Curr. Opin. Pharmacol. 12, 751-759.
66. Pike, L.J. (2006). Rafts defined: a report on the Keystone symposium on lipid rafts and cellular function. J. Lipid Res. 47, 1597-1598.
67. Platz, E.A., Clinton, S.K., and Giovannucci, E. (2008). Association between plasma cholesterol and prostate cancer in the PSA era. Int. J. Cancer 123, 1693-1698.
68. Poynter, J.N., Gruber, S.B., Higgins, P.D., Almog, R., Bonner, J.D., Rennert, H.S., Low, M., Greenson, J.K., and Rennert, G. (2005). Statins and the risk of colorectal cancer. New Engl. J. Med. 352, 2184-2192.
69. Rayner, K.J., Suárezm, Y., Dávalosm, A., Parathathm, S., Fitzgeraldm, M.L., Tamehirom, N., Fisherm, E.A., Moorem, K.J., and Fernández- Hernando, C. (2010). MiR-33 contributes to the regulation of cholesterol homeostasis. Science 328, 1570-1573.
70. Resh, M.D. (1999). Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins. Biochim. Biophys. Acta 1451, 1-16.
71. Rossi, S., Graner, E., Febbo, P., Weinstein, L., Bhattacharya, N., Onody, T., Bubley, G., Balk, S., and Loda, M. (2003). Fatty acid synthase expression defines distinct molecular signatures in prostate cancer. Mol. Cancer Res. 1, 707-715.
72. Roy, S., Luetterforst, R., Harding, A., Apolloni, A., Etheridge, M., Stang, E., Rolls, B., Hancock, J.F., and Parton, R.G. (1999). Dominant-negative caveolin inhibits H-Ras function by disrupting cholesterol-rich plasma membrane domains. Nat. Cell Biol. 1, 98-105.
73. Selvais, C., D'Auria, L., Tyteca, D., Perrot, G., Lemoine, P., Troeberg, L., Dedieu, S., Noël, A., Nagase, H., Henriet, P., et al. (2011). Cell cholesterol modulates metalloproteinase-dependent shedding of low-density lipoprotein receptor-related protein-1 (LRP-1) and clearance function. FASEB J. 25, 2770-2781.
74. Sharpe, L.J. and Brown, A.J. (2013). Controlling cholesterol synthesis beyond 3-hydroxy-3-methylglutaryl-CoA reductase (HMGCR). J. Biol. Chem. 288, 18707-18715.
75. Siegel, R., Naishadham, D., and Jemal, A. (2013). Cancer statistics, 2013. CA Cancer J. Clin. 63, 11-30.
76. Simons, K. and Ikonen, E. (1997). Functional rafts in cell membranes. Nature 387, 569-572.
77. Simons, K. and Toomre, D. (2000). Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1, 31-39.
78. Simons, K. and van Meer, G. (1988). Lipid sorting in epithelial cells. Biochemistry 27, 6197-6202.
79. Singer, S.J. and Nicolson, G.L. (1972). The fluid mosaic model of the structure of cell membranes. Science 175, 720-731.
80. Solomon, K.R. and Freeman, M.R. (2008). Do the cholesterol-lowering properties of statins affect cancer risk? Trends Endocrinol. Metab. 19, 113-121.
81. Solomon, K.R., Pelton, K., Boucher, K., Joo, J., Tully, C., Zurakowski, D., Schaffner, C.P., Kim, J., and Freeman, M.R. (2009). Ezetimibe is an inhibitor of tumor angiogenesis. Am. J. Pathol. 174, 1017-1026.
82. Sugahara, K.N., Murai, T., Nishinakamura, H., Kawashima, H., Saya, H., and Miyasaka, M. (2003). Hyaluronan oligosaccharides induce CD44 cleavage and promote cell migration in CD44- expressing tumor cells. J. Biol. Chem. 278, 32259-32265.
83. Swyer, G.I.M. (1942). The cholesterol content of normal and enlarged prostates. Cancer Res. 21, 372-375.
84. Trapani, L., Segatto, M., Ascenzi, P., and Pallottini, V. (2011). Potential role of nonstatin cholesterol lowering agents. IUBMB Life 63, 964-971.
85. Vander Heiden, M.G., Locasale, J.W., Swanson, K.D., Sharfi, H., Heffron, G.J., Amador-Noguez, D., Christofk, H.R., Wagner, G., Rabinowitz, J.D., Asara, J.M., et al. (2010). Evidence for an alternative glycolytic pathway in rapidly proliferating cells. Science 329, 1492-1499.
86. Veit, G., Zimina, E.P., Franzke, C.W., Kutsch, S., Siebolds, U., Gordon, M.K., Bruckner-Tuderman, L., and Koch, M. (2007). Shedding of collagen XXIII is mediated by furin and depends on the plasma membrane microenvironment. J. Biol. Chem. 282, 27424-27435.
87. Vogelstein, B. and Kinzler, K.W. (1993). The multistep nature of cancer. Trends Genet. 9, 138-141.
88. von Tresckow, B., Kallen, K.J., von Strandmann, E.P., Borchmann, P., Lange, H., Engert, A., and Hansen, H.P. (2004). Depletion of cellular cholesterol and lipid rafts increases shedding of CD30. J. Immunol. 172, 4324-4331.
89. Warburg, O. (1956). On the origin of cancer cells. Science 123, 309-314.
90. Warburg, O., Wind, F., and Negelein, E. (1927). The metabolism of tumors in the body. J. Gen. Physiol. 8, 519-530.
91. Wary, K.K., Mariotti, A., Zurzolo, C., and Giancotti, F.G. (1998). A requirement for caveolin-1 and associated kinase Fyn in integrin signaling and anchorage-dependent cell growth. Cell 94, 625-634.
92. Waugh, M.G., Lawson, D., and Hsuan, J.J. (1999). Epidermal growth factor receptor activation is localized within low-buoyant density, non-caveolar membrane domains. Biochem. J. 337, 591-597.
93. White, C.P. (1909). On the occurrence of crystals in tumours. J. Pathol. Bacteriol. 13, 3-10.
94. Williams, T.M. and Lisanti, M.P. (2005). Caveolin-1 in oncogenic transformation, cancer, and metastasis. Am. J. Physiol. Cell. Physiol. 288, C494-506.
95. Yager, J.D. and Davidson, N.E. (2006). Estrogen carcinogenesis in breast cancer. New Engl. J. Med. 354, 270-282.
96. Yasuda, M. and Bloor, W.R. (1932). Lipid content of tumors. J. Clin. Invest. 11, 677-682.
97. Young, R.M., Holowka, D., and Baird, B. (2003). A lipid raft environment enhances Lyn kinase activity by protecting the active site tyrosine from dephosphorylation. J. Biol. Chem. 278, 20746-20752.
98. Xue, T., Zhang, Y., Zhang, L., Yao, L., Hu, X., and Xu, L.X. (2013). Proteomic analysis of two metabolic proteins with potential to translocate to plasma membrane associated with tumor metastasis development and drug targets. J. Proteome Res. 12, 1754-1763.
99. Zhuang, L., Kim, J., Adam, R.M., Solomon, K.R., and Freeman, M.R. (2005). Cholesterol targeting alters lipid raft composition and cell survival in prostate cancer cells and xenografts. J. Clin. Invest. 115, 959-968.
100. Zimina, E.P., Bruckner-Tuderman, L., and Franzke, C.W. (2005). Shedding of collagen XVII ectodomain depends on plasma membrane microenvironment. J. Biol. Chem. 280, 34019-34024.