CD24 controls Src/STAT3 activity in human tumors

Cellular and Molecular Life Sciences

Volumn 69, Issue 22, 2012, Pages 3863-3879

  Bretz, Niko P ^a   Salnikov, Alexei V ^a   Perne, Claudia ^a   Keller, Sascha ^a   Wang, Xiaoli ^a   Mierke, Claudia T ^b   Fogel, Mina ^c   Erbe Hofmann, Natalie ^a   Schlange, Thomas ^d   Moldenhauer, Gerhard ^a   Altevogt, Peter ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY OF LEIPZIG   (Germany)

^c KAPLAN HOSPITAL   (Israel)

^d BAYER PHARMA AG   (Germany)

Author keywords

Cancer; CD24; Lipid rafts; Signaling; STAT3

Indexed keywords

CD24 ANTIGEN; FOCAL ADHESION KINASE; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY CD24; PROTEIN TYROSINE KINASE; SMALL INTERFERING RNA; STAT3 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; CANCER CELL; CANCER GROWTH; CELL ADHESION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME REGULATION; GENE EXPRESSION REGULATION; GENE TARGETING; HUMAN; HUMAN CELL; LIPID RAFT; LUNG CANCER; MALIGNANT NEOPLASTIC DISEASE; MOUSE; NONHUMAN; PANCREAS CANCER; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; TUMOR XENOGRAFT;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD24; APOPTOSIS; CELL ADHESION; CELL LINE, TUMOR; CELL PROLIFERATION; FOCAL ADHESION KINASE 1; GENE EXPRESSION REGULATION; HUMANS; MICE; MICE, INBRED NOD; MICE, SCID; NEOPLASM TRANSPLANTATION; NEOPLASMS; PHOSPHORYLATION; RNA INTERFERENCE; RNA, SMALL INTERFERING; SRC-FAMILY KINASES; STAT3 TRANSCRIPTION FACTOR; TRANSPLANTATION, HETEROLOGOUS;

MUS;

EID: 84867892211     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-012-1055-9     Document Type: Article

References (49)

1. Kay R, Rosten PM, Humphries RK (1991) CD24, a signal transducer modulating B cell activation responses, is a very short peptide with a glycosyl phosphatidylinositol membrane anchor. J Immunol 147(4):1412-1416
2. Kristiansen G, Sammar M, Altevogt P (2004) Tumour biological aspects of CD24, a mucin-like adhesion molecule. J Mol Histol 35(3):255-262
3. Kristiansen G, Machado E, Bretz N, Rupp C, Winzer KJ, Konig AK, Moldenhauer G, Marme F, Costa J, Altevogt P (2010) Molecular and clinical dissection of CD24 antibody specificity by a comprehensive comparative analysis. Lab Invest 90(7):1102-1116
4. Lim SC (2005) CD24 and human carcinoma: tumor biological aspects. Biomed Pharmacother 59(2):S351-S354
5. Woodward WA, Sulman EP (2008) Cancer stem cells: markers or biomarkers? Cancer Metastasis Rev 27(3):459-470
6. Fang X, Zheng P, Tang J, Liu Y (2010) CD24: from A to Z. Cell Mol Immunol 7(2):100-103
7. Nielsen PJ, Lorenz B, Muller AM, Wenger RH, Brombacher F, Simon M, von der Weid T, Langhorne WJ, Mossmann H, Kohler G (1997) Altered erythrocytes and a leaky block in B-cell development in CD24/HSA-deficient mice. Blood 89(3):1058-1067
8. Hahne M, Wenger RH, Vestweber D, Nielsen PJ (1994) The heatstable antigen can alter very late antigen 4-mediated adhesion. J Exp Med 179(4):1391-1395
9. Baumann P, Cremers N, Kroese F, Orend G, Chiquet-Ehrismann R, Uede T, Yagita H, Sleeman JP (2005) CD24 expression causes the acquisition of multiple cellular properties associated with tumor growth and metastasis. Cancer Res 65(23):10783-10793
10. Sagiv E, Starr A, Rozovski U, Khosravi R, Altevogt P, Wang T, Arber N (2008) Targeting CD24 for treatment of colorectal and pancreatic cancer by monoclonal antibodies or small interfering RNA. Cancer Res 68(8):2803-2812
11. Taniuchi K, Nishimori I, Hollingsworth MA (2011) Intracellular CD24 inhibits cell invasion by posttranscriptional regulation of BART through interaction with G3BP. Cancer Res 71(3):895-905
12. Ilangumaran S, Arni S, van Echten-Deckert G, Borisch B, Hoessli DC (1999) Microdomain-dependent regulation of Lck and Fyn protein-tyrosine kinases in T lymphocyte plasma membranes. Mol Biol Cell 10(4):891-905
13. Zarn JA, Zimmermann SM, Pass MK, Waibel R, Stahel RA (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(2):384-391
14. Sammar M, Gulbins E, Hilbert K, Lang F, Altevogt P (1997) Mouse CD24 as a signaling molecule for integrin-mediated cell binding: functional and physical association with src-kinases. Biochem Biophys Res Commun 234(2):330-334
15. Stefanova I, Horejsi V, Ansotegui IJ, Knapp W, Stockinger H (1991) GPI-anchored cell-surface molecules complexed to protein tyrosine kinases. Science 254(5034):1016-1019
16. Baumann P, Thiele W, Cremers N, Muppala S, Krachulec J, Diefenbacher M, Kassel O, Mudduluru G, Allgayer H, Frame M, Sleeman JP (2012) CD24 interacts with and promotes the activity of Src within lipid rafts in breast cancer cells, thereby increasing integrin-dependent adhesion. Cell Mol Life Sci 69(3):435-448
17. Bretz N, Noske A, Keller S, Erbe-Hofmann N, Schlange T, Salnikov A, Moldenhauer G, Kristiansen G, Altevogt P (2012) CD24 promotes tumor-cell invasion by suppressing tissue factor pathway inhibitor-2 (TFPI-2) in a Src-dependent fashion. Clin Exp Metast 29(1):27-38
18. Mierke CT, Bretz N, Altevogt P (2011) Contractile forces contribute to increased GPI-anchored receptor CD24 facilitated cancer cell invasion. J Biol Chem 286(40):34858-34871
19. Wolterink S, Moldenhauer G, Fogel M, Kiefel H, Pfeifer M, Luttgau S, Gouveia R, Costa J, Endell J, Moebius U, Altevogt P (2010) Therapeutic antibodies to human L1CAM: functional characterization and application in a mouse model for ovarian carcinoma. Cancer Res 70(6):2504-2515
20. Runz S, Mierke CT, Joumaa S, Behrens J, Fabry B, Altevogt P (2008) CD24 induces localization of beta1 integrin to lipid raft domains. Biochem Biophys Res Commun 365(1):35-41
21. Jackson D, Waibel R, Weber E, Bell J, Stahel RA (1992) CD24, a signal-transducing molecule expressed on human B cells, is a major surface antigen on small cell lung carcinomas. Cancer Res 52(19):5264-5270
22. Schabath H, Runz S, Joumaa S, Altevogt P (2006) CD24 affects CXCR4 function in pre-B lymphocytes and breast carcinoma cells. J Cell Sci 119(Pt 2):314-325
23. Riedle S, Kiefel H, Gast D, Bondong S, Wolterink S, Gutwein P, Altevogt P (2009) Nuclear translocation and signalling of L1- CAM in human carcinoma cells requires ADAM10 and presenilin/ gamma-secretase activity. Biochem J 420(3):391-402
24. Pfeifer M, Schirmer U, Geismann C, Schafer H, Sebens S, Altevogt P (2010) L1CAM expression in endometrial carcinomas is regulated by usage of two different promoter regions. BMC Mol Biol 11:64
25. Stoeck A, Gast D, Sanderson MP, Issa Y, Gutwein P, Altevogt P (2007) L1-CAM in a membrane-bound or soluble form augments protection from apoptosis in ovarian carcinoma cells. Gynecol Oncol 104(2):461-469
26. Kiefel H, Bondong S, Erbe-Hoffmann N, Hazin J, Riedle S, Wolf J, Pfeifer M, Arlt A, Schafer H, Muerkoster SS, Altevogt P (2010) L1CAM-integrin interaction induces constitutive NF-kappaB activation in pancreatic adenocarcinoma cells by enhancing IL- 1beta expression. Oncogene 29(34):4766-4778
27. Mechtersheimer S, Gutwein P, Agmon-Levin N, Stoeck A, Oleszewski M, Riedle S, Postina R, Fahrenholz F, Fogel M, Lemmon V, Altevogt P (2001) Ectodomain shedding of L1 adhesion molecule promotes cell migration by autocrine binding to integrins. J Cell Biol 155(4):661-673
28. Smith SC, Oxford G, Wu Z, Nitz MD, Conaway M, Frierson HF, Hampton G, Theodorescu D (2006) The metastasis-associated gene CD24 is regulated by Ral GTPase and is a mediator of cell proliferation and survival in human cancer. Cancer Res 66(4):1917-1922
29. Senner V, Sturm A, Baur I, Schrell UH, Distel L, Paulus W (1999) CD24 promotes invasion of glioma cells in vivo. J Neuropathol Exp Neurol 58(8):795-802
30. Dauer DJ, Ferraro B, Song L, Yu B, Mora L, Buettner R, Enkemann S, Jove R, Haura EB (2005) Stat3 regulates genes common to both wound healing and cancer. Oncogene 24(21):3397-3408
31. Yu H, Pardoll D, Jove R (2009) STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer 9(11):798-809
32. Cao X, Tay A, Guy GR, Tan YH (1996) Activation and association of Stat3 with Src in v-Src-transformed cell lines. Mol Cell Biol 16(4):1595-1603
33. Turkson J, Bowman T, Garcia R, Caldenhoven E, De Groot RP, Jove R (1998) Stat3 activation by Src induces specific gene regulation and is required for cell transformation. Mol Cell Biol 18(5):2545-2552
34. Schaller MD, Hildebrand JD, Shannon JD, Fox JW, Vines RR, Parsons JT (1994) Autophosphorylation of the focal adhesion kinase, pp 125FAK, directs SH2-dependent binding of pp60src. Mol Cell Biol 14(3):1680-1688
35. Calalb MB, Polte TR, Hanks SK (1995) Tyrosine phosphorylation of focal adhesion kinase at sites in the catalytic domain regulates kinase activity: a role for Src family kinases. Mol Cell Biol 15(2):954-963
36. Hitosugi T, Sato M, Sasaki K, Umezawa Y (2007) Lipid raft specific knockdown of SRC family kinase activity inhibits cell adhesion and cell cycle progression of breast cancer cells. Cancer Res 67(17):8139-8148
37. Overdevest JB, Thomas S, Kristiansen G, Hansel DE, Smith SC, Theodorescu D (2011) CD24 offers a therapeutic target for control of bladder cancer metastasis based on a requirement for lung colonization. Cancer Res 71(11):3802-3811
38. Ahmed MA, Jackson D, Seth R, Robins A, Lobo DN, Tomlinson IP, Ilyas M (2009) CD24 is upregulated in inflammatory bowel disease and stimulates cell motility and colony formation. Inflamm Bowel Dis 16(5):795-803
39. Fukushima T, Tezuka T, Shimomura T, Nakano S, Kataoka H (2007) Silencing of insulin-like growth factor-binding protein-2 in human glioblastoma cells reduces both invasiveness and expression of progression-associated gene CD24. J Biol Chem 282(25):18634-18644
40. Wang W, Wang X, Peng L, Deng Q, Liang Y, Qing H, Jiang B (2010) CD24-dependent MAPK pathway activation is required for colorectal cancer cell proliferation. Cancer Sci 101(1):112-119
41. Brunton VG, Avizienyte E, Fincham VJ, Serrels B, Metcalf CA 3rd, Sawyer TK, Frame MC (2005) Identification of Src-specific phosphorylation site on focal adhesion kinase: dissection of the role of Src SH2 and catalytic functions and their consequences for tumor cell behavior. Cancer Res 65(4):1335-1342
42. Holzer RG, Park EJ, Li N, Tran H, Chen M, Choi C, Solinas G, Karin M (2011) Saturated fatty acids induce Src clustering within membrane subdomains, leading to JNK activation. Cell 147(1):173-184
43. Rajendran L, Simons K (2005) Lipid rafts and membrane dynamics. J Cell Sci 118(Pt 6):1099-1102
44. Simons K, Toomre D (2000) Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1(1):31-39
45. Paulick MG, Bertozzi CR (2008) The glycosylphosphatidylinositol anchor: a complex membrane-anchoring structure for proteins. Biochemistry 47(27):6991-7000
46. Lee TK, Castilho A, Cheung VC, Tang KH, Ma S, Ng IO (2011) CD24(?) liver tumor-initiating cells drive self-renewal and tumor initiation through STAT3-mediated NANOG regulation. Cell Stem Cell 9(1):50-63
47. Marotta LL, Almendro V, Marusyk A, Shipitsin M, Schemme J, Walker SR, Bloushtain-Qimron N, Kim JJ, Choudhury SA, Maruyama R, Wu Z, Gonen M, Mulvey LA, Bessarabova MO, Huh SJ, Silver SJ, Kim SY, Park SY, Lee HE, Anderson KS, Richardson AL, Nikolskaya T, Nikolsky Y, Liu XS, Root DE, Hahn WC, Frank DA, Polyak K (2011) The JAK2/STAT3 signaling pathway is required for growth of CD44? CD24- stem cell-like breast cancer cells in human tumors. J Clin Invest. 121(7):2723-2735
48. Honeth G, Bendahl PO, Ringner M, Saal LH, Gruvberger-Saal SK, Lovgren K, Grabau D, Ferno M, Borg A, Hegardt C (2008) The CD44+/CD24- phenotype is enriched in basal-like breast tumors. Breast Cancer Res 10(3):R53
49. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 100(7):3983-3988