CyrA, a matricellular protein that modulates cell motility in Dictyostelium discoideum

Matrix Biology

Volumn 31, Issue 4, 2012, Pages 271-280

  Huber, Robert J ^a   Suarez, Andres ^a   O'Day, Danton H ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Calmodulin binding protein; Cell motility; Cysteine rich; Dictyostelium; EGF like repeats; Extracellular matrix; Matricellular

Indexed keywords

CALCIUM ION; CALMODULIN; CALMODULIN BINDING PROTEIN; CELL PROTEIN; CYRA PROTEIN; GREEN FLUORESCENT PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTOZOAL PROTEIN; UNCLASSIFIED DRUG; VINCULIN;

ARTICLE; CELL MOTILITY; CHEMOTAXIS; CONTROLLED STUDY; DICTYOSTELIUM DISCOIDEUM; ENDOPLASMIC RETICULUM; IMMUNOLOCALIZATION; IMMUNOPRECIPITATION; INTRACELLULAR SPACE; NONHUMAN; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; WESTERN BLOTTING;

ANTIBODY SPECIFICITY; CALCIUM; CALMODULIN; CALMODULIN-BINDING PROTEINS; CELL MEMBRANE; CHEMOTAXIS; CONCANAVALIN A; CYCLIC AMP; DICTYOSTELIUM; ENDOPLASMIC RETICULUM; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX PROTEINS; GREEN FLUORESCENT PROTEINS; IMMUNOPRECIPITATION; PHOSPHATIDYLINOSITOL 3-KINASES; PROTOZOAN PROTEINS; RECEPTORS, CELL SURFACE; SEQUENCE ANALYSIS, PROTEIN; SIGNAL TRANSDUCTION; TIME FACTORS; VINCULIN;

DICTYOSTELIUM; DICTYOSTELIUM DISCOIDEUM; GASTROPODA;

EID: 84860305485     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2012.02.003     Document Type: Article

References (49)

1. Anjard C., Loomis W.F. Peptide signaling during terminal differentiation of Dictyostelium. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:7607-7611.
2. Bakthavatsalam D., Gomer R.H. The secreted proteome profile of developing Dictyostelium discoideum cells. Proteomics 2010, 10:2556-2559.
3. Bornstein P., Sage E.H. Matricellular proteins: extracellular modulators of cell function. Curr. Opin. Cell Biol. 2002, 14:608-616.
4. Bourguignon L.Y., Rozek R.J. Capping of concanavalin A receptors and their association with microfilaments in monolayer grown human fibroblastoid cells. Cell Tissue Res. 1980, 205:77-84.
5. Brekken R.A., Sage E.H. SPARC, a matricellular protein: at the crossroads of cell-matrix communication. Matrix Biol. 2000, 19:569-580.
6. Campbell I., Bork P. Epidermal growth factor-like modules. Curr. Opin. Struct. Biol. 1993, 3:385-392.
7. Carboni J.M., Condeelis J.S. Ligand-induced changes in the location of actin, myosin, 95K (alpha-actinin), and 120K protein in amebae of Dictyostelium discoideum. J. Cell Biol. 1985, 100:1884-1893.
8. Chen L.F., Iijima M., Tang M., Landree M.A., Huang Y.E., Xiong Y., Iglesias P.A., Devreotes P.N. PLA2 and PI3K/PTEN pathways act in parallel to mediate chemotaxis. Dev. Cell 2007, 12:603-614.
9. Emanuelsson O., Nielsen H., Brunak S., von Heijne G. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 2000, 300:1005-1016.
10. Giannelli G., Falk-Marzillier J., Schiraldi O., Stetler-Stevenson W.G., Quaranta V. Induction of cell migration by matrix metalloprotease-2 cleavage of laminin-5. Science 1997, 277:225-228.
11. Gillette M.U., Dengler R.E., Filosa M.F. The localization and fate of concanavalin A in amoebae of the cellular slime mold, Dictyostelium discoideum. J. Exp. Zool. 1974, 190:243-248.
12. Huber, R.J., O'Day, D.H., submitted for publication. Identification of vinculin B as a mediator of EGF-like peptide-enhanced cell movement in Dictyostelium discoideum.
13. Huber R.J., O'Day D.H. An EGF-like peptide sequence from Dictyostelium enhances cell motility and chemotaxis. Biochem. Biophys. Res. Commun. 2009, 379:470-475.
14. 2+/calmodulin signaling. Cell. Signal. 2011, 23:731-738.
15. Huber R.J., O'Day D.H. Nucleocytoplasmic transfer of Cdk5 and its binding to puromycin-sensitive aminopeptidase in Dictyostelium discoideum. Histochem. Cell Biol. 2011, 136:177-189.
16. Hulen D., Baron A., Salisbury J., Clarke M. Production and specificity of monoclonal antibodies against calmodulin from Dictyostelium discoideum. Cell Motil. Cytoskeleton 1991, 18:113-122.
17. Ikezaki H., Patel M., Onyuksel H., Akhter S.R., Gao X.P., Rubenstein I. Exogenous calmodulin potentiates vasodilation elicited by phospholipid-associated VIP in vivo. Am. J. Physiol. Regul. Integr. Comp. Physiol. 1999, 276:1359-1365.
18. Iyer A.K.V., Kien T.T., Borysenko C.W., Cascio M., Camacho C.J., Balir H.C., Bahar L., Wells A. Tenascin cytotactin epidermal growth factor-like repeat binds epidermal growth factor receptor with low affinity. J. Cell. Physiol. 2007, 211:748-758.
19. Iyer A.K.V., Tran K.T., Griffith L., Wells A. Cell surface restriction of EGFR by a tenascin cytotactin-encoded EGF-like repeat is preferential for motility-regulated signaling. J. Cell. Physiol. 2008, 214:504-512.
20. Khan A.A., Steiner J.P., Klein M.G., Schneider M.F., Snyder S.H. IP3 receptor: localization to plasma membrane of T cells and cocapping with the T cell receptor. Science 1992, 257:815-818.
21. Kim M.G., Lee G., Lee S.K., Lolkema M., Yim J., Hong S.H., Schwartz R.H. Epithelial cell-specific laminin 5 is required for survival of early thymocytes. J. Immunol. 2000, 165:192-201.
22. Krogh A., Larsson B., von Heijne G., Sonnhammer E.L.L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 2001, 305:567-580.
23. Libby R.T., Champliaud M.F., Claudepierre T., Xu Y., Gibbons E.P., Koch M., Burgeson R.E., Hunter D.D., Brunken W.J. Laminin expression in adult and developing retinae: evidence of two novel CNS laminins. J. Neurosci. 2000, 20:6517-6528.
24. Liu A., Garg P., Yang S., Gong P., Pallero M.A., Annis D.S., Liu Y., Passaniti A., Mann D., Mosher D.F., Murphy-Ullrich J.E., Goldblum S.E. Epidermal growth factor-like repeats of thrombospondins activate phospholipase Cgamma and increase epithelial cell migration through indirect epidermal growth factor receptor activation. J. Biol. Chem. 2009, 284:6389-6402.
25. Ma L., Xu X., Sun D. The presence of a heterotrimeric G protein and its role in signal transduction of extracellular calmodulin in pollen germination and tube growth. Plant Cell 1999, 11:1351-1362.
26. Müller-Taubenberger A., Lupas A.N., Li H., Ecke M., Simmeth E., Gerisch G. Calreticulin and calnexin in the endoplasmic reticulum are important for phagocytosis. EMBO J. 2001, 20:6772-6782.
27. Murphy-Ullrich J.E. The de-adhesive activity of matricellular proteins: is intermediate cell adhesion an adaptive state?. J. Clin. Invest. 2001, 107:785-790.
28. Nikolaeva I., Huber R.J., O'Day D.H. EGF-like peptide of Dictyostelium discoideum is not a chemoattractant but it does restore folate-mediated chemotaxis in the presence of signal transduction inhibitors. Peptides. 2012, 34:145-149.
29. O'Day D.H. CaMBOT: profiling and characterizing calmodulin binding proteins. Cell. Signal. 2003, 15:347-355.
30. Patton W.F., Dhanak M.R., Jacobson B.S. Analysis of plasma membrane protein changes in Dictyostelium discoideum during concanavalin A induced receptor redistribution using two-dimensional gel electrophoresis. Electrophoresis 1990, 11:79-85.
31. Petersen T.N., Brunak S., von Heijne G., Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 2011, 8:785-786.
32. Reddy G.P., Barrack E.R., Dou Q.P., Menon M., Pelley R., Sarkar F.H., Shijie S. Regulatory processes affecting androgen receptor expression, stability, and function: potential targets to treat hormone-refractory prostate cancer. J. Cell. Biochem. 2006, 98:1408-1423.
33. Remgard P., Ekstrom P.A.R., Wiklund P., Edstrom A. Calmodulin and in vitro regenerating frog sciatic nerves: release and extracellular effects. Eur. J. Neurosci. 1995, 7:1386-1392.
34. Roberts D.D. Emerging functions of matricellular proteins. Cell. Mol. Life Sci. 2011, 68:3133-3136.
35. Rot G., Parikh A., Curk T., Kuspa A., Shaulsky G., Zupan B. dictyExpress: a Dictyostelium discoideum gene expression database with an explorative data analysis web-based interface. BMC Bioinform. 2009, 10:256.
36. Schaap P. Evolutionary crossroads in developmental biology: Dictyostelium discoideum. Development 2011, 138:387-396.
37. Schenk S., HIntermann E., Bilban M., Koshikawa N., Hojilla C., Khokha R., Quaranta V. Binding to EGF receptor of a laminin-5 EGF-like fragment liberated during MMP-dependent mammary gland involution. J. Cell Biol. 2003, 161:197-209.
38. Somesh B.P., Neffgen C., Iijima M., Devreotes P., Rivero F. Dictyostelium RacH regulates endocytic vesicular trafficking and is required for localization of vacuolin. Traffic 2006, 7:1194-1212.
39. Suarez A., Huber R.J., Myre M.A., O'Day D.H. An extracellular matrix, calmodulin-binding protein from Dictyostelium with EGF-like repeats that enhance cell motility. Cell. Signal. 2011, 23:1197-1206.
40. Swindle S.C., Tran K.T., Johnson T.D., Banerjee P., Mayes A.M., Griffith L., Wells A. Epidermal growth factor (EGF)-like repeats of human tenascin-C as ligands for EGF receptor. J. Cell Biol. 2001, 154:459-468.
41. Tsuruta D., Kobayashi H., Imanishi H., Sugawara K., Ishii M., Jones J.C. Laminin-332-integrin interaction: a target for cancer therapy?. Curr. Med. Chem. 2008, 15:1968-1975.
42. Van Haastert P.J.M., Keizer-Gunnink I., Kortholt A. Essential role of PI3-kinase and phospholipase A2 in Dictyostelium discoideum chemotaxis. J. Cell Biol. 2007, 177:809-816.
43. Wallner K., Li C., Shah P.K., Wu K.J., Schwartz S.M., Sharifi B.G. EGF-like domain of tenascin-C is proapoptotic for cultured smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 2004, 24:1416-1421.
44. Weaver M.S., Workman G., Cardo-Vila M., Arap W., Pasqualini R., Sage E.H. Processing of the matricellular protein hevin in mouse brain is dependent on ADAMTS4. J. Biol. Chem. 2010, 285:5868-5877.
45. Wilkins M.R., Williams K.L. The extracellular matrix of the Dictyostelium discoideum slug. Experientia 1995, 51:1189-1196.
46. Williams J.G. Dictyostelium finds new roles to model. Genetics 2010, 185:717-726.
47. Yanagisawa H., Schluterman M.K., Brekken R.A. Fibulin-5, an integrin-binding matricellular protein: its function in development and disease. J. Cell Commun. Signal 2009, 3:337-347.
48. Zakharov V.V., Mosevitsky M.I. M-calpain-mediated cleavage of GAP-43 near Ser41 is negatively regulated by protein kinase C, calmodulin and calpain-inhibiting fragment GAP-43-3. J. Neurochem. 2007, 101:1539-1551.
49. Zhang Z., Majava V., Greffier A., Hayes R.L., Kursula P., Wang K.K.W. Collapsin response mediator protein-2 is a calmodulin binding protein. Cell. Mol. Life Sci. 2009, 66:526-536.