Cholesterol depletion induces anoikis-like apoptosis via FAK down-regulation and caveolae internalization

Journal of Pathology

Volumn 218, Issue 3, 2009, Pages 337-349

  Park, Eun Kyung ^a   Mi, Jung Park ^a,b   Lee, Seong Hee ^a   Ying, Chun Li ^a   Kim, Jungeun ^a   Lee, Jae Seon ^c   Jung, Weon Lee ^b   Ye, Sang Kyu ^b   Park, Jong Wan ^b   Kim, Chul Woo ^b   Park, Byung Kiu ^a   Kim, Yong Nyun ^a  

^a National Cancer Center   (South Korea)

^b Seoul National University College of Medicine   (South Korea)

^c Korea Institute of Radiation and Medical Science   (South Korea)

Author keywords

Adhesion; Anoikis; Caveolin 1; Cholesterol; FAK; Lipid rafts caveolae; Src

Indexed keywords

CAVEOLIN 1; CHOLESTEROL; FOCAL ADHESION KINASE; METHYL BETA CYCLODEXTRIN; PROTEIN KINASE B; PROTEIN TYROSINE KINASE; SMALL INTERFERING RNA;

ANOIKIS; APOPTOSIS; ARTICLE; CAVEOLA; CELL ADHESION; CELL MEMBRANE; CELL SPREADING; CELL SURVIVAL; CHOLESTEROL TRANSPORT; HUMAN; HUMAN CELL; LIPID RAFT; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

ANOIKIS; BETA-CYCLODEXTRINS; CAVEOLAE; CAVEOLIN 1; CELL SHAPE; CELL SURVIVAL; CHOLESTEROL; DOWN-REGULATION; FOCAL ADHESION KINASE 1; HUMANS; MICROSCOPY, CONFOCAL; TUMOR CELLS, CULTURED;

EID: 67650097014     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.2531     Document Type: Article

References (55)

1. Pike LJ. Lipid rafts: heterogeneity on the high seas. Biochem J 2004;378:281-292.
2. Anderson RG. The caveolae membrane system. Annu Rev Biochem 1998;67:199-225.
3. Silvius JR. Role of cholesterol in lipid raft formation: lessons from lipid model systems. Biochim Biophys Acta 2003;1610:174-183.
4. Muppidi JR, Siegel RM. Ligand-independent redistribution of Fas (CD95) into lipid rafts mediates clonotypic T cell death. Nat Immunol 2004;5:182-189.
5. Nichols BJ, Lippincott-Schwartz J. Endocytosis without clathrin coats. Trends Cell Biol 2001;11:406-412.
6. Kirkham M, Parton RG. Clathrin-independent endocytosis: new insights into caveolae and non-caveolar lipid raft carriers. Biochim Biophys Acta 2005;1746:349-363.
7. Reddig PJ, Juliano RL. Clinging to life: cell to matrix adhesion and cell survival. Cancer Metast Rev 2005;24:425-439.
8. Mitra SK, Hanson DA, Schlaepfer DD. Focal adhesion kinase: in command and control of cell motility. Nat Rev Mol Cell Biol 2005;6:56-68.
9. Mitra SK, Schlaepfer DD. Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr Opin Cell Biol 2006;18:516-523.
10. Wozniak MA, Modzelewska K, Kwong L, Keely PJ. Focal adhesion regulation of cell behavior. Biochim Biophys Acta 2004;1692:103-119.
11. Owens LV, Xu L, Craven RJ, Dent GA, Weiner TM, Kornberg L, et al. Overexpression of the focal adhesion kinase (p125FAK) in invasive human tumors. Cancer Res 1995;55:2752-2755.
12. Leitinger B, Hogg N. The involvement of lipid rafts in the regulation of integrin function. J Cell Sci 2002;115(Pt 5):963-972.
13. Wei Y, Yang X, Liu Q, Wilkins JA, Chapman HA. A role for caveolin and the urokinase receptor in integrin-mediated adhesion and signaling. J Cell Biol 1999;144:1285-1294.
14. del Pozo MA, Alderson NB, Kiosses WB, Chiang HH, Anderson RG, Schwartz MA. Integrins regulate Rac targeting by internalization of membrane domains. Science 2004;303:839-842.
15. Li YC, Park MJ, Ye SK, Kim CW, Kim YN. 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.
16. Kim YN, Wiepz GJ, Guadarrama AG, Bertics PJ. Epidermal growth factor-stimulated tyrosine phosphorylation of caveolin-1. Enhanced caveolin-1 tyrosine phosphorylation following aberrant epidermal growth factor receptor status. J Biol Chem 2000;275:7481-7491.
17. Grande-Garcia A, Echarri A, Del Pozo MA. Integrin regulation of membrane domain trafficking and Rac targeting. Biochem Soc Trans 2005;33(4):609-613.
18. Grimmer S, van Deurs B, Sandvig K. Membrane ruffling and macropinocytosis in A431 cells require cholesterol. J Cell Sci 2002;115(14):2953- 2962.
19. Gervais FG, Thornberry NA, Ruffolo SC, Nicholson DW, Roy S. Caspases cleave focal adhesion kinase during apoptosis to generate a FRNK-like polypeptide. J Biol Chem 1998;273:17102-17108.
20. Kim YN, Dam P, Bertics PJ. Caveolin-1 phosphorylation in human squamous and epidermoid carcinoma cells: dependence on ErbB1 expression and Src activation. Exp Cell Res 2002;280:134-147.
21. Kim YN, Bertics PJ. The endocytosis-linked protein dynamin associates with caveolin-1 and is tyrosine phosphorylated in response to the activation of a noninternalizing epidermal growth factor receptor mutant. Endocrinology 2002;143:1726-1731.
22. del Pozo MA, Balasubramanian N, Alderson NB, Kiosses WB, Grande-García A, Anderson RG, et al. Phospho-caveolin-1 mediates integrin-regulated membrane domain internalization. Nat Cell Biol 2005;7:901-908.
23. Subtil A, Gaidarov I, Kobylarz K, Lampson MA, Keen JH, McGraw TE. Acute cholesterol depletion inhibits clathrin-coated pit budding. Proc Natl Acad Sci USA 1999;96:6775-6780.
24. Rodal SK, Skretting G, Garred O, Vilhardt F, van Deurs B, Sandvig K. Extraction of cholesterol with methyl-beta-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles. Mol Biol Cell 1999;10:961-974.
25. Huang Q, Shen HM, Shui G, Wenk MR, Ong CN. Emodin inhibits tumor cell adhesion through disruption of the membrane lipid raft-associated integrin signaling pathway. Cancer Res 2006;66:5807-5815.
26. Swaney JS, Patel HH, Yokoyama U, Head BP, Roth DM, Insel PA. Focal adhesions in (myo)fibroblasts scaffold adenylyl cyclase with phosphorylated caveolin. J Biol Chem 2006;281:17173-17179.
27. Lee H, Volonte D, Galbiati F, Iyengar P, Lublin DM, Bregman DB, et al. Constitutive and growth factor-regulated phosphorylation of caveolin-1 occurs at the same site (Tyr-14) in vivo: identification of a c-Src/Cav-1/Grb7 signaling cassette. Mol Endocrinol 2000;14:1750- 1775.
28. Adam RM, Mukhopadhyay NK, Kim J, Di Vizio D, Cinar B, Boucher K, et al. Cholesterol sensitivity of endogenous and myristoylated Akt. Cancer Res 2007;67:6238-6246.
29. Zhuang L, Kim J, Adam RM, Solomon KR, Freeman MR. Cholesterol targeting alters lipid raft composition and cell survival in prostate cancer cells and xenografts. J Clin Invest 2005;115:959-968.
30. Zhuang L, Lin J, Lu ML, Solomon KR, Freeman MR. Cholesterol-rich lipid rafts mediate akt-regulated survival in prostate cancer cells. Cancer Res 2002;62:2227-2231.
31. Le Roy C, Wrana JL. Clathrin- and non-clathrin-mediated endocytic regulation of cell signalling. Nat Rev Mol Cell Biol 2005;6:112- 126.
32. Freeman MR, Solomon KR. Cholesterol and prostate cancer. J Cell Biochem 2004;91:54-69.
33. Wary KK, Mariotti A, Zurzolo C, Giancotti FG. A requirement for caveolin-1 and associated kinase Fyn in integrin signaling and anchorage-dependent cell growth. Cell 1998;94:625-634.
34. Gaus K, Le Lay S, Balasubramanian N, Schwartz MA. Integrin-mediated adhesion regulates membrane order. J Cell Biol 2006;174:725-734.
35. Gopalakrishna P, Chaubey SK, Manogaran PS, Pande G. Modulation of α5β1 integrin functions by the phospholipid and cholesterol contents of cell membranes. J Cell Biochem 2000;77:517-528.
36. Pankov R, Markovska T, Hazarosova R, Antonov P, Ivanova L, Momchilova A. Cholesterol distribution in plasma membranes of β1 integrin-expressing and β1 integrin-deficient fibroblasts. Arch Biochem Biophys 2005;442:160-168.
37. Ramprasad OG, Srinivas G, Rao KS, Joshi P, Thiery JP, Dufour S, et al. Changes in cholesterol levels in the plasma membrane modulate cell signaling and regulate cell adhesion and migration on fibronectin. Cell Motil Cytoskel 2007;64:199-216.
38. Hannigan G, Troussard AA, Dedhar S. Integrin-linked kinase: a cancer therapeutic target unique among its ILK. Nat Rev Cancer 2005;5:51-63.
39. Hess F, Estrugo D, Fischer A, Belka C, Cordes N. Integrin-linked kinase interacts with caspase-9 and -8 in an adhesion-dependent manner for promoting radiation-induced apoptosis in human leukemia cells. Oncogene 2007;26:1372-1384.
40. McLean GW, Carragher NO, Avizienyte E, Evans J, Brunton VG, Frame MC. The role of focal-adhesion kinase in cancer - a new therapeutic opportunity. Nat Rev Cancer 2005;5:505-515.
41. Frisch SM, Vuori K, Ruoslahti E, Chan-Hui PY. Control of adhesion-dependent cell survival by focal adhesion kinase. J Cell Biol 1996;134:793-799.
42. Hungerford JE, Compton MT, Matter ML, Hoffstrom BG, Otey CA. Inhibition of pp125FAK in cultured fibroblasts results in apoptosis. J Cell Biol 1996;135:1383-1390.
43. Golubovskaya VM, Finch R, Kweh F, Massoll NA, Campbell-Thompson M, Wallace MR, et al. p53 regulates FAK expression in human tumor cells. Mol Carcinogen 2008;47:373-382.
44. Lim ST, Chen XL, Lim Y, Hanson DA, Vo TT, Howerton K, et al. Nuclear FAK promotes cell proliferation and survival through FERM-enhanced p53 degradation. Mol Cell 2008;29:9-22.
45. Palazzo AF, Eng CH, Schlaepfer DD, Marcantonio EE, Gundersen GG. Localized stabilization of microtubules by integrin- and FAK-facilitated Rho signaling. Science 2004;303:836-839.
46. Guan JL. Cell biology. Integrins, rafts, Rac, and Rho. Science 2004;303:773-774.
47. Pietïainen V, Marjom̈aki V, Upla P, Pelkmans L, Helenius A, Hyypïa T Echovirus 1 endocytosis into caveosomes requires lipid rafts, dynamin II, and signaling events. Mol Biol Cell 2004;15:4911-4925.
48. Shajahan AN, Timblin BK, Sandoval R, Tiruppathi C, Malik AB, Minshall RD. Role of Src-induced dynamin-2 phosphorylation in caveolae-mediated endocytosis in endothelial cells. J Biol Chem 2004;279:20392-20400.
49. Nomura R, Fujimoto T. Tyrosine-phosphorylated caveolin-1: immunolocalization and molecular characterization. Mol Biol Cell 1999;10:975-986.
50. Glenney JR Jr. Tyrosine phosphorylation of a 22 kDa protein is correlated with transformation by Rous sarcoma virus. J BiolChem 1989;264:20163-20166.
51. Lasserre R, Guo XJ, Conchonaud F, Hamon Y, Hawchar O, Bernard AM, et al. Raft nanodomains contribute to Akt/PKB plasma membrane recruitment and activation. Nat Chem Biol 2008;4:538-547.
52. Loza-Coll MA, Perera S, Shi W, Filmus J. A transient increase in the activity of Src-family kinases induced by cell detachment delays anoikis of intestinal epithelial cells. Oncogene 2005;24:1727-1737.
53. Gilmore AP, Metcalfe AD, Romer LH, Streuli CH. Integrin-mediated survival signals regulate the apoptotic function of Bax through its conformation and subcellular localization. J Cell Biol 2000;149:431-446.
54. Carver LA, Schnitzer JE. Caveolae: mining little caves for new cancer targets. Nat Rev Cancer 2003;3:571-581.
55. Fedida-Metula S, Elhyany S, Tsory S, Segal S, Hershfinkel M, Sekler I, et al. Targeting lipid rafts inhibits protein kinase B by disrupting calcium homeostasis and attenuates malignant properties of melanoma cells. Carcinogenesis 2008;29:1546-1554.