Phosphorylation of DARPP-32 regulates breast cancer cell migration downstream of the receptor tyrosine kinase DDR1

Experimental Cell Research

Volumn 312, Issue 20, 2006, Pages 4011-4018

  Hansen, Christian ^a   Greengard, Paul ^b   Nairn, Angus C ^c   Andersson, Tommy ^a   Vogel, Wolfgang F ^d  

^a LUND UNIVERSITY   (Sweden)

^b ROCKEFELLER UNIVERSITY   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

Breast cancer; Cell invasion; Cell migration; Collagen; Discoidin domain; Phosphorylation; Tyrosine kinase

Indexed keywords

DISCOIDIN DOMAIN RECEPTOR 1; PHOSPHOPROTEIN DARPP 32; PROTEIN TYROSINE KINASE; THREONINE;

ARTICLE; BREAST CANCER; CANCER CELL; CELL MIGRATION; CELL STRAIN MCF 7; CONTROLLED STUDY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION;

EID: 34447651165     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2006.09.003     Document Type: Article

References (38)

1. Wiseman B.S., and Werb Z. Stromal effects on mammary gland development and breast cancer. Science 296 (2002) 1046-1049
2. Johnson J.D., Edman J.C., and Rutter W.J. A receptor tyrosine kinase found in breast carcinoma cells has an extracellular discoidin I-like domain. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 5677-5681
3. Di Marco E., Cutuli N., Guerra L., Cancedda R., and De Luca M. 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 (1993) 24290-24295
4. Alves F., Vogel W., Mossie K., Millauer B., Hofler H., and Ullrich A. Distinct structural characteristics of discoidin I subfamily receptor tyrosine kinases and complementary expression in human cancer. Oncogene 10 (1995) 609-618
5. Vogel W.F., Abdulhussein R., and Ford C.E. Sensing extracellular matrix: an update on DDR function. Cell Signal. 18 (2006) 1108-1116
6. Vogel W.F., Aszodi A., Alves F., and Pawson T. Discoidin domain receptor 1 tyrosine kinase has an essential role in mammary gland development. Mol. Cell. Biol. 21 (2001) 2906-2917
7. Faraci-Orf E., McFadden C., and Vogel W.F. DDR1 signaling is essential to sustain Stat5 function during lactogenesis. J. Cell. Biochem. 97 (2006) 109-121
8. Vogel W.F. Collagen-receptor signaling in health and disease. Eur. J. Dermatol. 11 (2001) 506-514
9. Dejmek J., Leandersson K., Manjer J., Bjartell A., Emdin S.O., Vogel W.F., Landberg G., and Andersson T. 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 (2005) 520-528
10. Davies H., Hunter C., Smith R., Stephens P., Greenman C., Bignell G., Teague J., Butler A., Edkins S., Stevens C., Parker A., O'Meara S., Avis T., Barthorpe S., Brackenbury L., Buck G., Clements J., Cole J., Dicks E., Edwards K., Forbes S., Gorton M., Gray K., Halliday K., Harrison R., Hills K., Hinton J., Jones D., Kosmidou V., Laman R., Lugg R., Menzies A., Perry J., Petty R., Raine K., Shepherd R., Small A., Solomon H., Stephens Y., Tofts C., Varian J., Webb A., West S., Widaa S., Yates A., Brasseur F., Cooper C.S., Flanagan A.M., Green A., Knowles M., Leung S.Y., Looijenga L.H., Malkowicz B., Pierotti M.A., Teh B.T., Yuen S.T., Lakhani S.R., Easton D.F., Weber B.L., Goldstraw P., Nicholson A.G., Wooster R., Stratton M.R., and Futreal P.A. Somatic mutations of the protein kinase gene family in human lung cancer. Cancer Res. 65 (2005) 7591-7595
11. Vogel W., Gish G.D., Alves F., and Pawson T. The discoidin domain receptor tyrosine kinases are activated by collagen. Mol. Cell 1 (1997) 13-23
12. Hou G., Vogel W.F., and Bendeck M.P. Tyrosine kinase activity of discoidin domain receptor 1 is necessary for smooth muscle cell migration and matrix metalloproteinase expression. Circ. Res. 90 (2002) 1147-1149
13. Wang C.Z., Hsu Y.M., and Tang M.J. Function of discoidin domain receptor I in HGF-induced branching tubulogenesis of MDCK cells in collagen gel. J. Cell. Physiol. 203 (2005) 295-304
14. Kamohara H., Yamashiro S., Galligan C., and Yoshimura T. Discoidin domain receptor 1 isoform-a (DDR1alpha) promotes migration of leukocytes in three-dimensional collagen lattices. FASEB J. 15 (2001) 2724-2726
15. Jonsson M., and Andersson T. Repression of Wnt-5a impairs DDR1 phosphorylation and modifies adhesion and migration of mammary cells. J. Cell. Sci. 114 (2001) 2043-2053
16. Koo D.H., McFadden C., Huang Y., Abdulhussein R., Friese-Hamim M., and Vogel W.F. Pinpointing phosphotyrosine-dependent interactions downstream of the collagen receptor DDR1. FEBS Lett. 580 (2006) 15-22
17. Matsuyama W., Wang L., Farrar W.L., Faure M., and Yoshimura T. Activation of discoidin domain receptor 1 isoform b with collagen up-regulates chemokine production in human macrophages: role of p38 mitogen-activated protein kinase and NF-kappa B. J. Immunol. 172 (2004) 2332-2340
18. Foehr E.D., Tatavos A., Tanabe E., Raffioni S., Goetz S., Dimarco E., De Luca M., and Bradshaw R.A. Discoidin domain receptor 1 (DDR1) signaling in PC12 cells: activation of juxtamembrane domains in PDGFR/DDR/TrkA chimeric receptors. FASEB J. 14 (2000) 973-981
19. Walaas S.I., Aswad D.W., and Greengard P. A dopamine- and cyclic AMP-regulated phosphoprotein enriched in dopamine-innervated brain regions. Nature 301 (1983) 69-71
20. Svenningsson P., Nishi A., Fisone G., Girault J.A., Nairn A.C., and Greengard P. DARPP-32: an integrator of neurotransmission. Annu. Rev. Pharmacol. Toxicol. 44 (2004) 269-296
21. Fienberg A.A., Hiroi N., Mermelstein P.G., Song W., Snyder G.L., Nishi A., Cheramy A., O'Callaghan J.P., Miller D.B., Cole D.G., Corbett R., Haile C.N., Cooper D.C., Onn S.P., Grace A.A., Ouimet C.C., White F.J., Hyman S.E., Surmeier D.J., Girault J., Nestler E.J., and Greengard P. DARPP-32: regulator of the efficacy of dopaminergic neurotransmission. Science 281 (1998) 838-842
22. Hemmings Jr. H.C., Greengard P., Tung H.Y., and Cohen P. DARPP-32, a dopamine-regulated neuronal phosphoprotein, is a potent inhibitor of protein phosphatase-1. Nature 310 (1984) 503-505
23. Bibb J.A., Snyder G.L., Nishi A., Yan Z., Meijer L., Fienberg A.A., Tsai L.H., Kwon Y.T., Girault J.A., Czernik A.J., Huganir R.L., Hemmings Jr. H.C., Nairn A.C., and Greengard P. Phosphorylation of DARPP-32 by Cdk5 modulates dopamine signalling in neurons. Nature 402 (1999) 669-671
24. El-Rifai W., Smith Jr. M.F., Li G., Beckler A., Carl V.S., Montgomery E., Knuutila S., Moskaluk C.A., Frierson Jr. H.F., and Powell S.M. Gastric cancers overexpress DARPP-32 and a novel isoform, t-DARPP. Cancer Res. 62 (2002) 4061-4064
25. Varis A., Zaika A., Puolakkainen P., Nagy B., Madrigal I., Kokkola A., Vayrynen A., Karkkainen P., Moskaluk C., El-Rifai W., and Knuutila S. Coamplified and overexpressed genes at ERBB2 locus in gastric cancer. Int. J. Cancer 109 (2004) 548-553
26. Beckler A., Moskaluk C.A., Zaika A., Hampton G.M., Powell S.M., Frierson Jr. H.F., and El-Rifai W. Overexpression of the 32-kilodalton dopamine and cyclic adenosine 3′,5′-monophosphate-regulated phosphoprotein in common adenocarcinomas. Cancer 98 (2003) 1547-1551
27. Ebihara Y., Miyamoto M., Fukunaga A., Kato K., Shichinohe T., Kawarada Y., Kurokawa T., Cho Y., Murakami S., Uehara H., Kaneko H., Hashimoto H., Murakami Y., Itoh T., Okushiba S., Kondo S., and Katoh H. DARPP-32 expression arises after a phase of dysplasia in oesophageal squamous cell carcinoma. Br. J. Cancer 91 (2004) 119-123
28. Keegan K., and Cooper J.A. Use of the two hybrid system to detect the association of the protein-tyrosine-phosphatase, SHPTP2, with another SH2-containing protein, Grb7. Oncogene 12 (1996) 1537-1544
29. Gietz R.D., and Woods R.A. Screening for protein-protein interactions in the yeast two-hybrid system. Methods Mol. Biol. 185 (2002) 471-486
30. Muniz M., Martin M.E., Hidalgo J., and Velasco A. Protein kinase A activity is required for the budding of constitutive transport vesicles from the trans-Golgi network. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 14461-14466
31. Snyder G.L., Girault J.A., Chen J.Y., Czernik A.J., Kebabian J.W., Nathanson J.A., and Greengard P. Phosphorylation of DARPP-32 and protein phosphatase inhibitor-1 in rat choroid plexus: regulation by factors other than dopamine. J. Neurosci. 12 (1992) 3071-3083
32. Valjent E., Pascoli V., Svenningsson P., Paul S., Enslen H., Corvol J.C., Stipanovich A., Caboche J., Lombroso P.J., Nairn A.C., Greengard P., Herve D., and Girault J.A. Regulation of a protein phosphatase cascade allows convergent dopamine and glutamate signals to activate ERK in the striatum. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 491-496
33. Lewis R.M., Wallace W.C., Kanazir S.D., and Greengard P. Expression of cell-type-specific neuronal phosphoproteins. Cold Spring Harbor Symp. Quant. Biol. 48 Pt 1 (1983) 347-354
34. Andersson M., Usiello A., Borgkvist A., Pozzi L., Dominguez C., Fienberg A.A., Svenningsson P., Fredholm B.B., Borrelli E., Greengard P., and Fisone G. Cannabinoid action depends on phosphorylation of dopamine- and cAMP-regulated phosphoprotein of 32 kDa at the protein kinase A site in striatal projection neurons. J. Neurosci. 25 (2005) 8432-8438
35. Howe A.K., Hogan B.P., and Juliano R.L. Regulation of vasodilator-stimulated phosphoprotein phosphorylation and interaction with Abl by protein kinase A and cell adhesion. J. Biol. Chem. 277 (2002) 38121-38126
36. Howe A.K., and Juliano R.L. Regulation of anchorage-dependent signal transduction by protein kinase A and p21-activated kinase. Nat. Cell Biol. 2 (2000) 593-600
37. Lundell L. Re: "DRD2/DARPP-32 expression correlates with lymph node metastasis and tumor progression in patients with esophageal squamous cell carcinoma". World J. Surg. 30 (2006) 1672-1681
38. Garcia-Jimenez C., Zaballos M.A., and Santisteban P. DARPP-32 (dopamine and 3′,5′-cyclic adenosine monophosphate-regulated neuronal phosphoprotein) is essential for the maintenance of thyroid differentiation. Mol. Endocrinol. 19 (2005) 3060-3072