A novel mechanism of regulating breast cancer cell migration via palmitoylation-dependent alterations in the lipid raft affiliation of CD44

Breast Cancer Research

Volumn 16, Issue 1, 2014, Pages

  Babina, Irina S ^a   McSherry, Elaine A ^a   Donatello, Simona ^a   Hill, Arnold D K ^a   Hopkins, Ann M ^a  

^a BEAUMONT HOSPITAL   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

BIOTIN; CD44V ANTIGEN; EZRIN; TRITON X 100; CD44 PROTEIN, HUMAN; CYTOSKELETON PROTEIN; HERMES ANTIGEN; PROTEIN BINDING;

ARTICLE; BREAST CARCINOMA; BREAST METASTASIS; CANCER CELL CULTURE; CANCER MORTALITY; CANCER PATIENT; CELL ADHESION; CELL FRACTIONATION; CELL MIGRATION; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; LIPID RAFT; PALMITOYLATION; POINT MUTATION; PRIMARY CELL CULTURE; SITE DIRECTED MUTAGENESIS; SUCROSE GRADIENT; TUMOR CELL; WESTERN BLOTTING; BREAST; BREAST TUMOR; CELL MEMBRANE; CELL MOTION; CYTOLOGY; GENETICS; LIPOYLATION; METABOLISM; PAGET NIPPLE DISEASE; PATHOLOGY; PHYSIOLOGY; PROTEIN PROCESSING; TUMOR CELL LINE; TUMOR INVASION;

ANTIGENS, CD44; BREAST; BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; CYTOSKELETAL PROTEINS; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HUMANS; LIPOYLATION; MEMBRANE MICRODOMAINS; MUTAGENESIS, SITE-DIRECTED; NEOPLASM INVASIVENESS; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84896721663     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/bcr3614     Document Type: Article

References (42)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011, 61:69-90. 10.3322/caac.20107, 21296855.
2. Platt VM, Szoka FC. Anticancer therapeutics: targeting macromolecules and nanocarriers to hyaluronan or CD44, a hyaluronan receptor. Mol Pharm 2008, 5:474-486. 10.1021/mp800024g, 2772999, 18547053.
3. Herrera-Gayol A, Jothy S. Adhesion proteins in the biology of breast cancer: contribution of CD44. Exp Mol Pathol 1999, 66:149-156. 10.1006/exmp.1999.2251, 10409443.
4. Orian-Rousseau V, Chen L, Sleeman JP, Herrlich P, Ponta H. CD44 is required for two consecutive steps in HGF/c-Met signaling. Genes Dev 2002, 16:3074-3086. 10.1101/gad.242602, 187488, 12464636.
5. Ponta H, Sherman L, Herrlich PA. CD44: from adhesion molecules to signalling regulators. Nat Rev Mol Cell Biol 2003, 4:33-45. 10.1038/nrm1004, 12511867.
6. Ostapkowicz A, Inai K, Smith L, Kreda S, Spychala J. Lipid rafts remodeling in estrogen receptor-negative breast cancer is reversed by histone deacetylase inhibitor. Mol Cancer Ther 2006, 5:238-245.
7. Olsson E, Honeth G, Bendahl PO, Saal LH, Gruvberger-Saal S, Ringner M, Vallon-Christersson J, Jonsson G, Holm K, Lovgren K, Fernö M, Grabau D, Borg A, Hegardt C. CD44 isoforms are heterogeneously expressed in breast cancer and correlate with tumor subtypes and cancer stem cell markers. BMC Cancer 2011, 11:418. 10.1186/1471-2407-11-418, 3196967, 21957977.
8. Gao AC, Lou W, Dong JT, Isaacs JT. CD44 is a metastasis suppressor gene for prostatic cancer located on human chromosome 11p13. Cancer Res 1997, 57:846-849.
9. Horak CE, Lee JH, Marshall JC, Shreeve SM, Steeg PS. The role of metastasis suppressor genes in metastatic dormancy. APMIS 2008, 116:586-601. 10.1111/j.1600-0463.2008.01027.x, 3508681, 18834404.
10. Louderbough JM, Schroeder JA. Understanding the dual nature of CD44 in breast cancer progression. Mol Cancer Res 2011, 9:1573-1586. 10.1158/1541-7786.MCR-11-0156, 21970856.
11. Neame SJ, Uff CR, Sheikh H, Wheatley SC, Isacke CM. CD44 exhibits a cell type dependent interaction with triton X-100 insoluble, lipid rich, plasma membrane domains. J Cell Sci 1995, 108:3127-3135.
12. Babina IS, Donatello S, Nabi IR, Hopkins AM. Lipid Rafts as Master Regulators of Breast Cancer Cell Function. Breast Cancer - Carcinogenesis, Cell Growth and Signalling Pathways 2011, 401-428. Croatia: InTech, Gunduz MGE, doi:10.5772/21324.
13. Staubach S, Hanisch FG. Lipid rafts: signaling and sorting platforms of cells and their roles in cancer. Expert Rev Proteomics 2011, 8:263-277. 10.1586/epr.11.2, 21501018.
14. Diaz LK, Zhou X, Wright ET, Cristofanilli M, Smith T, Yang Y, Sneige N, Sahin A, Gilcrease MZ. CD44 expression is associated with increased survival in node-negative invasive breast carcinoma. Clin Cancer Res 2005, 11:3309-3314. 10.1158/1078-0432.CCR-04-2184, 15867228.
15. Naor D, Wallach-Dayan SB, Zahalka MA, Sionov RV. Involvement of CD44, a molecule with a thousand faces, in cancer dissemination. Semin Cancer Biol 2008, 18:260-267. 10.1016/j.semcancer.2008.03.015, 18467123.
16. Bourguignon LY. Hyaluronan-mediated CD44 activation of RhoGTPase signaling and cytoskeleton function promotes tumor progression. Semin Cancer Biol 2008, 18:251-259. 10.1016/j.semcancer.2008.03.007, 2505114, 18450475.
17. Morrison H, Sperka T, Manent J, Giovannini M, Ponta H, Herrlich P. Merlin/neurofibromatosis type 2 suppresses growth by inhibiting the activation of Ras and Rac. Cancer Res 2007, 67:520-527. 10.1158/0008-5472.CAN-06-1608, 17234759.
18. Donatello S, Babina IS, Hazelwood LD, Hill AD, Nabi IR, Hopkins AM. Lipid Raft Association Restricts CD44-Ezrin Interaction and Promotion of Breast Cancer Cell Migration. Am J Pathol 2012, 181:2172-2187. 10.1016/j.ajpath.2012.08.025, 3502863, 23031255.
19. Donatello S, Hudson L, Cottell DC, Blanco A, Aurrekoetxea I, Shelly MJ, Dervan PA, Kell MR, Stokes M, Hill AD, Hopkins AM. An imbalance in progenitor cell populations reflects tumour progression in breast cancer primary culture models. J Exp Clin Cancer Res 2011, 30:45. 10.1186/1756-9966-30-45, 3094256, 21521500.
20. Chao JI, Kuo PC, Hsu TS. Down-regulation of survivin in nitric oxide-induced cell growth inhibition and apoptosis of the human lung carcinoma cells. J Biol Chem 2004, 279:20267-20276. 10.1074/jbc.M312381200, 14988404.
21. Bowie RV, Donatello S, Lyes C, Owens MB, Babina IS, Hudson L, Walsh SV, O'Donoghue DP, Amu S, Barry SP, Fallon PG, Hopkins AM. Lipid rafts are disrupted in mildly inflamed intestinal microenvironments without overt disruption of the epithelial barrier. Am J Physiol Gastrointest Liver Physiol 2012, 302:G781-G793. 10.1152/ajpgi.00002.2011, 22241861.
22. Fairbank M, Huang K, El-Husseini A, Nabi IR. RING finger palmitoylation of the endoplasmic reticulum Gp78 E3 ubiquitin ligase. FEBS Lett 2012, 586:2488-2493. 10.1016/j.febslet.2012.06.011, 22728137.
23. Hughes L, Malone C, Chumsri S, Burger AM, McDonnell S. Characterisation of breast cancer cell lines and establishment of a novel isogenic subclone to study migration, invasion and tumourigenicity. Clin Exp Metastasis 2008, 25:549-557. 10.1007/s10585-008-9169-z, 18386134.
24. Sheridan C, Kishimoto H, Fuchs RK, Mehrotra S, Bhat-Nakshatri P, Turner CH, Goulet R, Badve S, Nakshatri H. CD44+/CD24- breast cancer cells exhibit enhanced invasive properties: an early step necessary for metastasis. Breast Cancer Res 2006, 8:R59. 10.1186/bcr1610, 1779499, 17062128.
25. Klingbeil P, Natrajan R, Everitt G, Vatcheva R, Marchio C, Palacios J, Buerger H, Reis-Filho JS, Isacke CM. CD44 is overexpressed in basal-like breast cancers but is not a driver of 11p13 amplification. Breast Cancer Res Treat 2010, 120:95-109. 10.1007/s10549-009-0380-7, 19350388.
26. Ilangumaran S, Hoessli DC. Effects of cholesterol depletion by cyclodextrin on the sphingolipid microdomains of the plasma membrane. Biochem J 1998, 335:433-440. 1219799, 9761744.
27. Tarone G, Ferracini R, Galetto G, Comoglio P. A cell surface integral membrane glycoprotein of 85,000 mol wt (gp85) associated with triton X-100-insoluble cell skeleton. J Cell Biol 1984, 99:512-519. 10.1083/jcb.99.2.512, 2113253, 6378925.
28. Bourguignon LY, Wong G, Earle C, Krueger K, Spevak CC. Hyaluronan-CD44 interaction promotes c-Src-mediated twist signaling, microRNA-10b expression, and RhoA/RhoC up-regulation, leading to Rho-kinase-associated cytoskeleton activation and breast tumor cell invasion. J Biol Chem 2010, 285:36721-36735. 10.1074/jbc.M110.162305, 2978601, 20843787.
29. Manes S, Mira E, Gomez-Mouton C, Lacalle RA, Keller P, Labrador JP, Martinez AC. Membrane raft microdomains mediate front-rear polarity in migrating cells. EMBO J 1999, 18:6211-6220. 10.1093/emboj/18.22.6211, 1171684, 10562533.
30. Oliferenko S, Paiha K, Harder T, Gerke V, Schwarzler C, Schwarz H, Beug H, Gunthert U, Huber LA. Analysis of CD44-containing lipid rafts: Recruitment of annexin II and stabilization by the actin cytoskeleton. J Cell Biol 1999, 146:843-854. 10.1083/jcb.146.4.843, 2156143, 10459018.
31. Murai T, Miyazaki Y, Nishinakamura H, Sugahara KN, Miyauchi T, Sako Y, Yanagida T, Miyasaka M. Engagement of CD44 promotes Rac activation and CD44 cleavage during tumor cell migration. J Biol Chem 2004, 279:4541-4550.
32. Murai T, Maruyama Y, Mio K, Nishiyama H, Suga M, Sato C. Low cholesterol triggers membrane microdomain-dependent CD44 shedding and suppresses tumor cell migration. J Biol Chem 2011, 286:1999-2007. 10.1074/jbc.M110.184010, 3023496, 21087933.
33. Lee JL, Wang MJ, Sudhir PR, Chen JY. CD44 engagement promotes matrix-derived survival through the CD44-SRC-integrin axis in lipid rafts. Mol Cell Biol 2008, 28:5710-5723. 10.1128/MCB.00186-08, 2546932, 18644869.
34. Elliott BE, Meens JA, SenGupta SK, Louvard D, Arpin M. The membrane cytoskeletal crosslinker ezrin is required for metastasis of breast carcinoma cells. Breast Cancer Res 2005, 7:R365-R373. 10.1186/bcr1006, 1143558, 15987432.
35. Singleton PA, Bourguignon LY. CD44 interaction with ankyrin and IP3 receptor in lipid rafts promotes hyaluronan-mediated Ca2+ signaling leading to nitric oxide production and endothelial cell adhesion and proliferation. Exp Cell Res 2004, 295:102-118. 10.1016/j.yexcr.2003.12.025, 15051494.
36. Thankamony SP, Knudson W. Acylation of CD44 and its association with lipid rafts are required for receptor and hyaluronan endocytosis. J Biol Chem 2006, 281:34601-34609. 10.1074/jbc.M601530200, 3039921, 16945930.
37. Simons K, Ikonen E. Functional rafts in cell membranes. Nature 1997, 387:569-572. 10.1038/42408, 9177342.
38. Liu D, Sy MS. Phorbol myristate acetate stimulates the dimerization of CD44 involving a cysteine in the transmembrane domain. J Immunol 1997, 159:2702-2711.
39. Wakahara K, Kobayashi H, Yagyu T, Matsuzaki H, Kondo T, Kurita N, Sekino H, Inagaki K, Suzuki M, Kanayama N, Terao T. Bikunin down-regulates heterodimerization between CD44 and growth factor receptors and subsequently suppresses agonist-mediated signaling. J Cell Biochem 2005, 94:995-1009. 10.1002/jcb.20364, 15597342.
40. Skube SB, Chaverri JM, Goodson HV. Effect of GFP tags on the localization of EB1 and EB1 fragments in vivo. Cytoskeleton (Hoboken) 2010, 67:1-12. 10.1002/cm.20409, 2909448, 19701929.
41. Roetger A, Merschjann A, Dittmar T, Jackisch C, Barnekow A, Brandt B. Selection of potentially metastatic subpopulations expressing c-erbB-2 from breast cancer tissue by use of an extravasation model. Am J Pathol 1998, 153:1797-1806. 10.1016/S0002-9440(10)65694-5, 1866322, 9846970.
42. Brown RL, Reinke LM, Damerow MS, Perez D, Chodosh LA, Yang J, Cheng C. CD44 splice isoform switching in human and mouse epithelium is essential for epithelial-mesenchymal transition and breast cancer progression. J Clin Invest 2011, 121:1064-1074. 10.1172/JCI44540, 3049398, 21393860.