CD24 interacts with and promotes the activity of c-src within lipid rafts in breast cancer cells, thereby increasing integrin-dependent adhesion

Cellular and Molecular Life Sciences

Volumn 69, Issue 3, 2012, Pages 435-448

  Baumann, Petra ^a   Thiele, Wilko ^a,b   Cremers, Natascha ^a,b   Muppala, Santoshi ^b   Krachulec, Justyna ^b   Diefenbacher, Markus ^a   Kassel, Olivier ^a   Mudduluru, Giridhar ^b   Allgayer, Heike ^b   Frame, Margaret ^c   Sleeman, Jonathan P ^a,b,d  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

C src; CD24; Heat stable antigen; Integrin; Motility

Indexed keywords

CD24 ANTIGEN; FOCAL ADHESION KINASE; PAXILLIN; PROTEIN TYROSINE KINASE;

ANIMAL CELL; ARTICLE; BREAST CANCER; CANCER CELL; CELL ADHESION; CELL INVASION; CELL PROLIFERATION; CELL SPREADING; CONTROLLED STUDY; ENZYME ACTIVITY; GAIN OF FUNCTION MUTATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LIPID RAFT; LOSS OF FUNCTION MUTATION; NONHUMAN; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION;

ANTI-BACTERIAL AGENTS; ANTIGENS, CD24; BREAST NEOPLASMS; CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; DOXYCYCLINE; FEMALE; FIBRONECTINS; FOCAL ADHESION KINASE 1; HUMANS; INTEGRINS; MEMBRANE MICRODOMAINS; PAXILLIN; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN-TYROSINE KINASES; PYRIMIDINES;

EID: 84856209716     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-011-0756-9     Document Type: Article

References (48)

1. AJ Henniker 2001 Cd24 J Biol Regul Homeost Agents 15 182 184 11501979 1:CAS:528:DC%2BD3MXovFSgtbg%3D (Pubitemid 32720386)
2. S Aigner CL Ramos A Hafezi-Moghadam MB Lawrence J Friederichs P Altevogt K Ley 1998 CD24 mediates rolling of breast carcinoma cells on P-selectin FASEB J 12 1241 1251 9737727 1:CAS:528:DyaK1cXlvFWrsrY%3D (Pubitemid 28418954)
3. G Kadmon BA Imhof P Altevogt M Schachner 1995 Adhesive hierarchy involving the cell adhesion molecules L1, CD24, and alpha 6 integrin in murine neuroblastoma N2A cells Biochem Biophys Res Commun 214 94 101 7669058 10.1006/bbrc.1995.2261 1:CAS:528:DyaK2MXnvFahs70%3D
4. M Sammar S Aigner P Altevogt 1997 Heat-stable antigen (mouse CD24) in the brain: dual but distinct interaction with P-selectin and L1 Biochim Biophys Acta 1337 287 294 9048906 10.1016/S0167-4838(96)00177-X 1:CAS:528: DyaK2sXnsFyitg%3D%3D (Pubitemid 27073499)
5. PJ Nielsen B Lorenz AM Muller RH Wenger F Brombacher M Simon T von der Weid WJ Langhorne H Mossmann G Kohler 1997 Altered erythrocytes and a leaky block in B-cell development in CD24/HSA-deficient mice Blood 89 1058 1067 9028339 1:CAS:528:DyaK2sXptFOisg%3D%3D (Pubitemid 27121301)
6. G Kadmon F von Bohlen und Halbach M Schachner P Altevogt 1994 Differential, LFA-1-sensitive effects of antibodies to nectadrin, the heat-stable antigen, on B lymphoblast aggregation and signal transduction Biochem Biophys Res Commun 198 1209 1215 8117278 10.1006/bbrc.1994.1171 1:CAS:528:DyaK2cXhs1Wls7w%3D (Pubitemid 24172825)
7. R Belvindrah G Rougon G Chazal 2002 Increased neurogenesis in adult mCD24-deficient mice J Neurosci 22 3594 3607 11978835 1:CAS:528: DC%2BD38Xjs1Sgs7Y%3D (Pubitemid 37465764)
8. D Shewan V Calaora P Nielsen J Cohen G Rougon H Moreau 1996 mCD24, a glycoprotein transiently expressed by neurons, is an inhibitor of neurite outgrowth J Neurosci 16 2624 2634 8786438 1:CAS:528:DyaK28XitFKhu78%3D (Pubitemid 26122680)
9. R Kleene H Yang M Kutsche M Schachner 2001 The neural recognition molecule L1 is a sialic acid-binding lectin for CD24, which induces promotion and inhibition of neurite outgrowth J Biol Chem 276 21656 21663 11283023 10.1074/jbc.M101790200 1:CAS:528:DC%2BD3MXksFGks78%3D
10. N Cremers MA Deugnier J Sleeman 2010 Loss of CD24 expression promotes ductal branching in the murine mammary gland Cell Mol Life Sci 67 2311 2322 20352469 10.1007/s00018-010-0342-6 1:CAS:528:DC%2BC3cXntF2gsbY%3D
11. G Kristiansen M Sammar P Altevogt 2004 Tumour biological aspects of CD24, a mucin-like adhesion molecule J Mol Histol 35 255 262 15339045 10.1023/B:HIJO.0000032357.16261.c5 1:CAS:528:DC%2BD2cXltVWqs7c%3D (Pubitemid 40585311)
12. GP Yang DT Ross WW Kuang PO Brown RJ Weigel 1999 Combining SSH and cDNA microarrays for rapid identification of differentially expressed genes Nucleic Acids Res 27 1517 1523 10037815 10.1093/nar/27.6.1517 1:CAS:528: DyaK1MXitFentLs%3D (Pubitemid 29206295)
13. A Nestl OD Von Stein K Zatloukal WG Thies P Herrlich M Hofmann JP Sleeman 2001 Gene expression patterns associated with the metastatic phenotype in rodent and human tumors Cancer Res 61 1569 1577 11245467 1:CAS:528: DC%2BD3MXhvVeltbk%3D (Pubitemid 34292589)
14. MW Pedersen T Thykjaer TF Orntoft L Damstrup HS Poulsen 2001 Profile of differentially expressed genes mediated by the type III epidermal growth factor receptor mutation expressed in a small-cell lung cancer cell line Br J Cancer 85 1211 1218 11710837 10.1054/bjoc.2001.2053 1:CAS:528:DC%2BD3MXoslalsro%3D (Pubitemid 33052323)
15. K Boon JB Edwards IM Siu D Olschner CG Eberhart MA Marra RL Strausberg GJ Riggins 2003 Comparison of medulloblastoma and normal neural transcriptomes identifies a restricted set of activated genes Oncogene 22 7687 7694 14576832 10.1038/sj.onc.1207043 1:CAS:528:DC%2BD3sXotlaisrk%3D (Pubitemid 37464103)
16. KG Kohlgraf AJ Gawron M Higashi JL Meza MD Burdick S Kitajima DL Kelly TC Caffrey MA Hollingsworth 2003 Contribution of the MUC1 tandem repeat and cytoplasmic tail to invasive and metastatic properties of a pancreatic cancer cell line Cancer Res 63 5011 5020 12941828 1:CAS:528:DC%2BD3sXms12nsLY%3D (Pubitemid 37022639)
17. JP Sleeman N Cremers 2007 New concepts in breast cancer metastasis: tumor initiating cells and the microenvironment Clin Exp Metastasis 24 707 715 17972145 10.1007/s10585-007-9122-6 1:CAS:528:DC%2BD1cXhvFGgtrY%3D (Pubitemid 50000183)
18. V Senner A Sturm I Baur UH Schrell L Distel W Paulus 1999 CD24 promotes invasion of glioma cells in vivo J Neuropathol Exp Neurol 58 795 802 10446804 10.1097/00005072-199908000-00002 1:CAS:528:DyaK1MXls1Wgs74%3D (Pubitemid 29372834)
19. H Schabath S Runz S Joumaa P Altevogt 2006 CD24 affects CXCR4 function in pre-B lymphocytes and breast carcinoma cells J Cell Sci 119 314 325 16390867 10.1242/jcs.02741 1:CAS:528:DC%2BD28Xhs1eitLc%3D (Pubitemid 43210700)
20. P Baumann N Cremers F Kroese G Orend R Chiquet-Ehrismann T Uede H Yagita JP Sleeman 2005 CD24 expression causes the acquisition of multiple cellular properties associated with tumor growth and metastasis Cancer Res 65 10783 10793 16322224 10.1158/0008-5472.CAN-05-0619 1:CAS:528:DC%2BD2MXht1Kjsr7J (Pubitemid 41715227)
21. VG Brunton MC Frame 2008 Src and focal adhesion kinase as therapeutic targets in cancer Curr Opin Pharmacol 8 427 432 18625340 10.1016/j.coph.2008.06. 012 1:CAS:528:DC%2BD1cXhtFCktL%2FN
22. RH Alvarez HM Kantarjian JE Cortes 2006 The role of Src in solid and hematologic malignancies: development of new-generation Src inhibitors Cancer 107 1918 1929 16986126 10.1002/cncr.22215 1:CAS:528:DC%2BD28Xht1Cms7fL (Pubitemid 44582963)
23. P Timpson GE Jones MC Frame VG Brunton 2001 Coordination of cell polarization and migration by the Rho family GTPases requires Src tyrosine kinase activity Curr Biol 11 1836 1846 11728306 10.1016/S0960-9822(01)00583-8 1:CAS:528:DC%2BD3MXovVCns78%3D (Pubitemid 33136523)
24. MG Paulick CR Bertozzi 2008 The glycosylphosphatidylinositol anchor: a complex membrane-anchoring structure for proteins Biochemistry 47 6991 7000 18557633 10.1021/bi8006324 1:CAS:528:DC%2BD1cXntF2rsr4%3D (Pubitemid 351956348)
25. S Runz CT Mierke S Joumaa J Behrens B Fabry P Altevogt 2008 CD24 induces localization of beta1 integrin to lipid raft domains Biochem Biophys Res Commun 365 35 41 17980703 10.1016/j.bbrc.2007.10.139 1:CAS:528:DC%2BD2sXhtlalsL7E (Pubitemid 350110573)
26. P Keller K Simons 1998 Cholesterol is required for surface transport of influenza virus hemagglutinin J Cell Biol 140 1357 1367 9508769 10.1083/jcb.140.6.1357 1:CAS:528:DyaK1cXitFChs7w%3D (Pubitemid 28152985)
27. EP Kilsdonk PG Yancey GW Stoudt FW Bangerter WJ Johnson MC Phillips GH Rothblat 1995 Cellular cholesterol efflux mediated by cyclodextrins J Biol Chem 270 17250 17256 7615524 10.1074/jbc.270.29.17250 1:CAS:528:DyaK2MXntVOrtr4%3D
28. P Scheiffele MG Roth K Simons 1997 Interaction of influenza virus haemagglutinin with sphingolipid-cholesterol membrane domains via its transmembrane domain EMBO J 16 5501 5508 9312009 10.1093/emboj/16.18.5501 1:CAS:528:DyaK2sXmsFWnurc%3D (Pubitemid 27399842)
29. JA Zarn SM Zimmermann MK Pass R Waibel RA Stahel 1996 Association of CD24 with the kinase c-fgr in a small cell lung cancer cell line and with the kinase lyn in an erythroleukemia cell line Biochem Biophys Res Commun 225 384 391 8753773 10.1006/bbrc.1996.1184 1:CAS:528:DyaK28XltVels74%3D (Pubitemid 26355612)
30. M Sammar E Gulbins K Hilbert F Lang P Altevogt 1997 Mouse CD24 as a signaling molecule for integrin-mediated cell binding: functional and physical association with src-kinases Biochem Biophys Res Commun 234 330 334 9177270 10.1006/bbrc.1997.6639 1:CAS:528:DyaK2sXjsFCjur8%3D (Pubitemid 27243902)
31. D Lingwood K Simons 2010 Lipid rafts as a membrane-organising principle Science 327 46 50 20044567 10.1126/science.1174621 1:CAS:528:DC%2BD1MXhs1WksrfJ
32. K Simons D Toomre 2000 Lipid rafts and signal transduction Nat Rev Mol Cell Biol 1 31 39 11413487 10.1038/35036052 1:CAS:528:DC%2BD3MXivVGjtbo%3D
33. M Narisawa-Saito Y Yamanashi T Morioka T Oite F Shimizu 1996 Thy-1 molecule associates with protein tyrosine kinase(s) in rat mesangial cells Clin Exp Immunol 106 86 90 8870703 10.1046/j.1365-2249.1996.d01-800.x 1:CAS:528:DyaK28XmsFChsbY%3D (Pubitemid 26329384)
34. TA Rege MA Pallero C Gomez HE Grenett JE Murphy-Ullrich JS Hagood 2006 Thy-1, via its GPI anchor, modulates Src family kinase and focal adhesion kinase phosphorylation and subcellular localization, and fibroblast migration, in response to thrombospondin-1/hep I Exp Cell Res 312 3752 3767 17027000 10.1016/j.yexcr.2006.07.029 1:CAS:528:DC%2BD28XhtFCjs7fK (Pubitemid 44633878)
35. EM Kramer C Klein T Koch M Boytinck J Trotter 1999 Compartmentation of Fyn kinase with glycosylphosphatidylinositol-anchored molecules in oligodendrocytes facilitates kinase activation during myelination J Biol Chem 274 29042 29049 10506155 10.1074/jbc.274.41.29042 1:CAS:528:DyaK1MXmslWqtr0%3D (Pubitemid 29477064)
36. K Kasahara K Watanabe K Takeuchi H Kaneko A Oohira T Yamamoto Y Sanai 2000 Involvement of gangliosides in glycosylphosphatidylinositol-anchored neuronal cell adhesion molecule TAG-1 signaling in lipid rafts J Biol Chem 275 34701 34709 10944523 10.1074/jbc.M003163200 1:CAS:528:DC%2BD3cXotFWltLc%3D
37. T Suzuki N Kiyokawa T Taguchi T Sekino YU Katagiri J Fujimoto 2001 CD24 induces apoptosis in human B cells via the glycolipid-enriched membrane domains/rafts-mediated signaling system J Immunol 166 5567 5577 11313396 1:CAS:528:DC%2BD3MXjtFyrur0%3D (Pubitemid 32374179)
38. KG Suzuki TK Fujiwara F Sanematsu R Iino M Edidin A Kusumi 2007 GPI-anchored receptor clusters transiently recruit Lyn and G alpha for temporary cluster immobilization and Lyn activation: single-molecule tracking study 1 J Cell Biol 177 717 730 17517964 10.1083/jcb.200609174 1:CAS:528: DC%2BD2sXls1ygs78%3D (Pubitemid 46799842)
39. S Lu M Ouyang J Seong J Zhang S Chien Y Wang 2008 The spatiotemporal pattern of Src activation at lipid rafts revealed by diffusion-corrected FRET imaging PLoS Comput Biol 4 e1000127 18711637 10.1371/journal.pcbi.1000127
40. RM Young D Holowka B Baird 2003 A lipid raft environment enhances Lyn kinase activity by protecting the active site tyrosine from dephosphorylation J Biol Chem 278 20746 20752 12670955 10.1074/jbc.M211402200 1:CAS:528: DC%2BD3sXkt1Wis74%3D (Pubitemid 36806378)
41. C Oneyama T Hikita K Enya MW Dobenecker K Saito S Nada A Tarakhovsky M Okada 2008 The lipid raft-anchored adaptor protein Cbp controls the oncogenic potential of c-Src Mol Cell 30 426 436 18498747 10.1016/j.molcel.2008.03.026 1:CAS:528:DC%2BD1cXmslOitb8%3D (Pubitemid 351672379)
42. NK Williams IS Lucet SP Klinken E Ingley J Rossjohn 2009 Crystal structures of the Lyn protein tyrosine kinase domain in its Apo- and inhibitor-bound state J Biol Chem 284 284 291 18984583 10.1074/jbc.M807850200 1:CAS:528:DC%2BD1cXhsFCjtLzK
43. KF Harris I Shoji EM Cooper S Kumar H Oda PM Howley 1999 Ubiquitin-mediated degradation of active Src tyrosine kinase Proc Natl Acad Sci U S A 96 13738 13743 10570142 10.1073/pnas.96.24.13738 1:CAS:528: DyaK1MXns1Oqtr0%3D
44. T Hitosugi M Sato K Sasaki Y Umezawa 2007 Lipid raft specific knockdown of SRC family kinase activity inhibits cell adhesion and cell cycle progression of breast cancer cells Cancer Res 67 8139 8148 17804726 10.1158/0008-5472.CAN- 06-4539 1:CAS:528:DC%2BD2sXpvFKjtb8%3D (Pubitemid 47395149)
45. XH Zhang Q Wang W Gerald CA Hudis L Norton M Smid JA Foekens J Massague 2009 Latent bone metastasis in breast cancer tied to Src-dependent survival signals Cancer Cell 16 67 78 19573813 10.1016/j.ccr.2009.05.017 1:CAS:528:DC%2BD1MXhtVWnsL7I
46. R Ishizawar SJ Parsons 2004 c-Src and cooperating partners in human cancer Cancer Cell 6 209 214 15380511 10.1016/j.ccr.2004.09.001 1:CAS:528:DC%2BD2cXot1Kis7w%3D (Pubitemid 39222033)
47. E Sagiv A Starr U Rozovski R Khosravi P Altevogt T Wang N Arber 2008 Targeting CD24 for treatment of colorectal and pancreatic cancer by monoclonal antibodies or small interfering RNA Cancer Res 68 2803 2812 18413748 10.1158/0008-5472.CAN-07-6463 1:CAS:528:DC%2BD1cXks1Giuro%3D (Pubitemid 351556279)
48. LC Kim L Song EB Haura 2009 Src kinases as therapeutic targets for cancer Nat Rev Clin Oncol 6 587 595 19787002 10.1038/nrclinonc.2009.129