Migration inhibition of mammary epithelial cells by Syk is blocked in the presence of DDR1 receptors

Cellular and Molecular Life Sciences

Volumn 68, Issue 22, 2011, Pages 3757-3770

  Neuhaus, Brit ^a   Bühren, Sebastian ^a   Böck, Barbara ^a   Alves, Frauke ^b,c   Vogel, Wolfgang F ^d   Kiefer, Friedemann ^a  

^a MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

^b UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^c MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

Cancer; DDR1; Epithelial cells; Migration; Syk

Indexed keywords

DISCOIDIN; DISCOIDIN DOMAIN RECEPTOR TYROSINE KINASE 1; MESSENGER RNA; PROTEIN KINASE SYK; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BREAST CARCINOMA; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; ENZYME ACTIVITY; EPITHELIUM CELL; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MIGRATION INHIBITION; MOUSE; MYOEPITHELIUM CELL; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RECEPTOR BLOCKING; SKIN EPITHELIUM;

EID: 85027929832     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-011-0676-8     Document Type: Article

References (46)

1. Comoglio PM, Trusolino L (2005) Cancer: the matrix is now in control. Nat Med 11:1156-1159 (Pubitemid 43093657)
2. Sada K, Takano T, Yanagi S, Yamamura H (2001) Structure and function of Syk protein-tyrosine kinase. J Biochem 130:177-186 (Pubitemid 32785863)
3. Fluck M, Zurcher G, Andres AC, Ziemiecki A (1995) Molecular characterization of the murine Syk protein tyrosine kinase cDNA, transcripts and protein. Biochem Biophys Res Commun 213:273-281
4. Coopman PJ, Mueller SC (2006) The Syk tyrosine kinase: a new negative regulator in tumor growth and progression. Cancer Lett 241:159-173 (Pubitemid 44163045)
5. Mocsai A, Ruland J, Tybulewicz VL (2010) The SYK tyrosine kinase: a crucial player in diverse biological functions. Nat Rev Immunol 10:387-402
6. Moroni M, Soldatenkov V, Zhang L, Zhang Y, Stoica G, Gehan E, Rashidi B, Singh B, Ozdemirli M, Mueller SC (2004) Progressive loss of Syk and abnormal proliferation in breast cancer cells. Cancer Res 64:7346-7354 (Pubitemid 39372073)
7. Yuan Y, Liu H, Sahin A, Dai JL (2005) Reactivation of SYK expression by inhibition of DNA methylation suppresses breast cancer cell invasiveness. Int J Cancer 113:654-659 (Pubitemid 40038744)
8. Dejmek J, Leandersson K, Manjer J, Bjartell A, Emdin SO, Vogel WF, Landberg G, Andersson T (2005) Expression and signaling activity of Wnt-5a/discoidin domain receptor-1 and Syk plays distinct but decisive roles in breast cancer patient survival. Clin Cancer Res 11:520-528 (Pubitemid 40116875)
9. Toyama T, Iwase H, Yamashita H, Hara Y, Omoto Y, Sugiura H, Zhang Z, Fujii Y (2003) Reduced expression of the Syk gene is correlated with poor prognosis in human breast cancer. Cancer Lett 189:97-102 (Pubitemid 35351524)
10. Coopman PJ, Do MT, Barth M, Bowden ET, Hayes AJ, Basyuk E, Blancato JK, Vezza PR, McLeskey SW, Mangeat PH, Mueller SC (2000) The Syk tyrosine kinase suppresses malignant growth of human breast cancer cells. Nature 406:742-747
11. Li J, Sidell N (2005) Growth-related oncogene produced in human breast cancer cells and regulated by Syk protein-tyrosine kinase. Int JCancer 117:14-20 (Pubitemid 41262755)
12. Wang L, Devarajan E, He J, Reddy SP, Dai JL (2005) Transcription repressor activity of spleen tyrosine kinase mediates breast tumor suppression. Cancer Res 65:10289-10297 (Pubitemid 41743721)
13. Zyss D, Montcourrier P, Vidal B, Anguille C, Merezegue F, Sahuquet A, Mangeat PH, Coopman PJ (2005) The Syk tyrosine kinase localizes to the centrosomes and negatively affects mitotic progression. Cancer Res 65:10872-10880 (Pubitemid 41713355)
14. Vogel W, Gish GD, Alves F, Pawson T (1997) The discoidin domain receptor tyrosine kinases are activated by collagen. Mol Cell 1:13-23 (Pubitemid 127376389)
15. Di ME, Cutuli N, Guerra L, Cancedda R, De LM (1993) Molecular cloning of trkE, a novel trk-related putative tyrosine kinase receptor isolated from normal human keratinocytes and widely expressed by normal human tissues. J Biol Chem 268:24290-24295 (Pubitemid 23335418)
16. Alves F, Vogel W, Mossie K, Millauer B, Hofler H, Ullrich A (1995) Distinct structural characteristics of discoidin I subfamily receptor tyrosine kinases and complementary expression in human cancer. Oncogene 10:609-618
17. Vogel WF, Abdulhussein R, Ford CE (2006) Sensing extracellular matrix: an update on discoidin domain receptor function. Cell Signal 18:1108-1116 (Pubitemid 43674043)
18. Alves F, Saupe S, Ledwon M, Schaub F, Hiddemann W, Vogel WF (2001) Identification of two novel, kinase-deficient variants of discoidin domain receptor 1: differential expression in human colon cancer cell lines. FASEB J 15:1321-1323
19. Mullenbach E, Walter L, Dressel R (2006) A novel discoidin domain receptor 1 (Ddr1) transcript is expressed in postmeiotic germ cells of the rat testis depending on the major histocompatibility complex haplotype. Gene 372:53-61
20. Curat CA, Vogel WF (2002) Discoidin domain receptor 1 controls growth and adhesion of mesangial cells. J Am Soc Nephrol 13:2648-2656 (Pubitemid 35216033)
21. Ongusaha PP, Kim JI, Fang L, Wong TW, Yancopoulos GD, Aaronson SA, Lee SW (2003) p53 induction and activation of DDR1 kinase counteract p53-mediated apoptosis and influence p53 regulation through a positive feedback loop. EMBO J 22:1289-1301 (Pubitemid 36362693)
22. Hou G, Vogel W, Bendeck MP (2001) The discoidin domain receptor tyrosine kinase DDR1 in arterial wound repair. J Clin Invest 107:727-735 (Pubitemid 32225358)
23. Kamohara H, Yamashiro S, Galligan C, Yoshimura T (2001) Discoidin domain receptor 1 isoform-a (DDR1alpha) promotes migration of leukocytes in three-dimensional collagen lattices. FASEB J 15:2724-2726
24. Yoshimura T, Matsuyama W, Kamohara H (2005) Discoidin domain receptor 1: a new class of receptor regulating leukocytecollagen interaction. Immunol Res 31:219-230
25. Weiner HL, Huang H, Zagzag D, Boyce H, Lichtenbaum R, Ziff EB (2000) Consistent and selective expression of the discoidin domain receptor-1 tyrosine kinase in human brain tumors. Neurosurgery 47:1400-1409
26. Wang L, Duke L, Zhang PS, Arlinghaus RB, Symmans WF, Sahin A, Mendez R, Dai JL (2003) Alternative splicing disrupts a nuclear localization signal in spleen tyrosine kinase that is required for invasion suppression in breast cancer. Cancer Res 63:4724-4730 (Pubitemid 36951053)
27. Gatalica Z, Bing Z (2005) Syk tyrosine kinase expression during multistep mammary carcinogenesis. Croat Med J 46:372-376 (Pubitemid 40686479)
28. Ulanova M, Puttagunta L, Marcet-Palacios M, Duszyk M, Steinhoff U, Duta F, Kim MK, Indik ZK, Schreiber AD, Befus AD (2005) Syk tyrosine kinase participates in beta1-integrin signaling and inflammatory responses in airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 288:L497-L507 (Pubitemid 40229515)
29. Nakashima H, Natsugoe S, Ishigami S, Okumura H, Matsumoto M, Hokita S, Aikou T (2006) Clinical significance of nuclear expression of spleen tyrosine kinase (Syk) in gastric cancer. Cancer Lett 236:89-94
30. Bohmer R, Neuhaus B, Buhren S, Zhang D, Stehling M, Bock B, Kiefer F (2010) Regulation of developmental lymphangiogenesis by Syk (+) leukocytes. Dev Cell 18:437-449
31. Srinivas S, Watanabe T, Lin CS, William CM, Tanabe Y, Jessell TM, Costantini F (2001) Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol 1:4
32. Saouaf SJ, Mahajan S, Rowley RB, Kut SA, Fargnoli J, Burkhardt AL, Tsukada S, Witte ON, Bolen JB (1994) Temporal differences in the activation of three classes of non-transmembrane protein tyrosine kinases following B-cell antigen receptor surface engagement. Proc Natl Acad Sci USA 91:9524-9528
33. Luangdilok S, Box C, Patterson L, Court W, Harrington K, Pitkin L, Rhys-Evans P, Charoenrat P, Eccles S (2007) Syk tyrosine kinase is linked to cell motility and progression in squamous cell carcinomas of the head and neck. Cancer Res 67:7907-7916 (Pubitemid 47281387)
34. Mahabeleshwar GH, Kundu GC (2003) Syk, a protein-tyrosine kinase, suppresses the cell motility and nuclear factor kappa B-mediated secretion of urokinase type plasminogen activator by inhibiting the phosphatidylinositol 3'-kinase activity in breast cancer cells. J Biol Chem 278:6209-6221 (Pubitemid 36800876)
35. Zhang X, Shrikhande U, Alicie BM, Zhou Q, Geahlen RL (2009) Role of the protein tyrosine kinase Syk in regulating cell-cell adhesion and motility in breast cancer cells. Mol Cancer Res 7:634-644
36. Law DA, Nannizzi-Alaimo L, Ministri K, Hughes PE, Forsyth J, Turner M, Shattil SJ, Ginsberg MH, Tybulewicz VL, Phillips DR (1999) Genetic and pharmacological analyses of Syk function in alphaIIbbeta3 signaling in platelets. Blood 93:2645-2652 (Pubitemid 29181197)
37. Inoue O, Suzuki-Inoue K, Dean WL, Frampton J, Watson SP (2003) Integrin alpha2beta1 mediates outside-in regulation of platelet spreading on collagen through activation of Src kinases and PLCgamma2. J Cell Biol 160:769-780 (Pubitemid 36298271)
38. Larive RM, Urbach S, Poncet J, Jouin P, Mascre G, Sahuquet A, Mangeat PH, Coopman PJ, Bettache N (2009) Phosphoproteomic analysis of Syk kinase signaling in human cancer cells reveals its role in cell-cell adhesion. Oncogene 28:2337-2347
39. Singh A, Greninger P, Rhodes D, Koopman L, Violette S, Bardeesy N, Settleman J (2009) A gene expression signature associated with "K-Ras addiction" reveals regulators of EMT and tumor cell survival. Cancer Cell 15:489-500
40. Jonsson M, Andersson T (2001) Repression of Wnt-5a impairs DDR1 phosphorylation and modifies adhesion and migration of mammary cells. J Cell Sci 114:2043-2053 (Pubitemid 32586629)
41. Hou G, Vogel WF, Bendeck MP (2002) Tyrosine kinase activity of discoidin domain receptor 1 is necessary for smooth muscle cell migration and matrix metalloproteinase expression. Circ Res 90:1147-1149 (Pubitemid 34786897)
42. Katz E, Dubois-Marshall S, Sims AH, Faratian D, Li J, Smith ES, Quinn JA, Edward M, Meehan RR, Evans EE, Langdon SP, Harrison DJ (2010) A gene on the HER2 amplicon, C35, is an oncogene in breast cancer whose actions are prevented by inhibition of Syk. Br J Cancer 103:401-410
43. Evans EE, Henn AD, Jonason A, Paris MJ, Schiffhauer LM, Borrello MA, Smith ES, Sahasrabudhe DM, Zauderer M (2006) C35 (C17orf37) is a novel tumor biomarker abundantly expressed in breast cancer. Mol Cancer Ther 5:2919-2930 (Pubitemid 44849020)
44. Katz E, Lareef MH, Rassa JC, Grande SM, King LB, Russo J, Ross SR, Monroe JG (2005) MMTV Env encodes an ITAM responsible for transformation of mammary epithelial cells in three-dimensional culture. J Exp Med 201:431-439 (Pubitemid 40229417)
45. Grande SM, Katz E, Crowley JE, Bernardini MS, Ross SR, Monroe JG (2006) Cellular ITAM-containing proteins are oncoproteins in nonhematopoietic cells. Oncogene 25:2748-2757
46. Kiefer F, Tibbles LA, Anafi M, Janssen A, Zanke BW, Lassam N, Pawson T, Woodgett JR, Iscove NN (1996) HPK1, a hematopoietic protein kinase activating the SAPK/JNK pathway. EMBO J 15:7013-7025 (Pubitemid 27023272)