The PCH family member MAYP/PSTPIP2 directly regulates F-actin bundling and enhances filopodia formation and motility in macrophages

Molecular Biology of the Cell

Volumn 16, Issue 6, 2005, Pages 2947-2959

  Chitu, Violeta ^a   Pixley, Fiona J ^a   Macaluso, Frank ^a   Larson, Daniel R ^a   Condeelis, John ^a   Yeung, Yee Guide ^a   Stanley, E Richard ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; COLONY STIMULATING FACTOR 1; F ACTIN; PROTEIN MAYP; UNCLASSIFIED DRUG;

ACTIN POLYMERIZATION; ANIMAL CELL; ARTICLE; CELL ELONGATION; CELL MEMBRANE; CELL MOTILITY; CELL STRUCTURE; CHEMOTAXIS; CONTROLLED STUDY; FILOPODIUM; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; MOUSE; NONHUMAN; PHENOTYPE; POLARIZATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN METABOLISM; PROTEIN PURIFICATION; PROTEIN STABILITY; WESTERN BLOTTING;

ACTINS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL LINE; CELL POLARITY; CHEMOTAXIS; CYTOSKELETAL PROTEINS; DOSE-RESPONSE RELATIONSHIP, DRUG; FLUORESCENT ANTIBODY TECHNIQUE; FLUORESCENT DYES; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; KINETICS; MACROPHAGE COLONY-STIMULATING FACTOR; MACROPHAGES; MICE; MICROSCOPY, VIDEO; PHALLOIDINE; PHOSPHORYLATION; PRECIPITIN TESTS; PSEUDOPODIA; RECEPTOR, MACROPHAGE COLONY-STIMULATING FACTOR; RETROVIRIDAE; RHODAMINES; SUBCELLULAR FRACTIONS;

EID: 19644380374     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E04-10-0914     Document Type: Article

References (46)

1. Allen, W. E., Zicha, D., Ridley, A. J., and Jones, G. E. (1998). A role for Cdc42 in macrophage chemotaxis. J. Cell Biol. 141, 1147-1157.
2. Angers-Loustau, A., Cote, J.-F., Charest, A., Dowbenko, D., Spencer, S., Lasky, L. A., and Tremblay, M. L. (1999). Protein tyrosine phosphatase-PEST regulates focal adhesion disassembly, migration and cytokinesis in fibroblasts. J. Cell Biol. 144, 1019-1031.
3. Aspenström, P. (1997). A Cdc42 target protein with homology to the non-kinase domain of FER has a potential role in regulating the actin cytoskeleton, Curr. Biol. 7, 479-487.
4. Bailly, M., Macaluso, F., Cammer, M., Chan, A., Segall, J. E., and Condeelis, J. S. (1999). Relationship between Arp2/3 complex and the barbed ends of actin filaments at the leading edge of carcinoma cells after epidermal growth factor stimulation. J. Cell Biol. 145, 331-345.
5. Bailly, M., Yan, L., Whitesides, G. M., Condeelis, J. S., and Segall, J. E. (1998). Regulation of protrusion shape and adhesion to the substratum during chemotactic responses of mammalian carcinoma cells. Exp. Cell Res. 241, 285-299.
6. Boocock, C. A., Jones, G. E., Stanley, E. R., and Pollard, J. W. (1989). Colony-stimulating factor-1 induces rapid behavioural responses in the mouse macrophage cell line, BAC1.2F5. J. Cell Sci. 93, 447-456.
7. Bryant, P. (1999). Filopodia: fickle fingers of cell fate? Curr. Biol. 9, R655-R657.
8. Cecchini, M. G., Dominguez, M. G., Mocci, S., Wetterwald, A., Felix, R., Fleisch, H., Chisholm, O., Hofstetter, W., Pollard, J. W., and Stanley, E. R. (1994). Role of colony stimulating factot-1 in the establishment and regulation of tissue macrophages during postnatal development of the mouse. Development 120, 1357-1372.
9. Coussens, L. M., and Werb, Z. (2001). Inflammatory cells and cancer: think different! J. Exp. Med. 193, F23-F26.
10. Demma, M., Warren, V., Hock, R., Dharmawardhane, S., and Condeelis, J. (1990). Isolation of an abundant 50,000-dalton actin filament bundling protein from Dictyostelium amoebae. J. Biol. Chem. 265, 2286-2291.
11. DesMarais, V., Ichetovkin, I., Condeelis, J., and Hitchcock-DeGregori, S. E. (2002). Spatial regulation of actin dynamics: a tropomyosin-free, actin-rich compartment at the leading edge. J. Cell Sci. 115, 4649-4660.
12. Edmonds, B. T., Wyckoff, J., Yeung, Y.-G., Wang, Y., Stanley, E. R., Jones, J., Segall, J., and Condeelis, J. (1996). Elongation factor-1α is an overexpressed actin binding protein in metastatic rat mammary adenocarcinoma. J. Cell Sci. 109, 2705-2714.
13. Ho, H. Y., Rohatgi, R., Lebensohn, A. M., Le, M., Li, J., Gygi, S. P., and Kirschner, M. W. (2004). Toca-1 mediates Cdc42-dependent actin nucleation by activating the N-WASP-WIP complex. Cell 118, 203-216.
14. Jones, G., Allen, W., and Ridley, A. (1998). The Rho GTPases in macrophage motility and chemotaxis. Cell Adhes. Commun. 6, 237-245.
15. Lewis, C. E., Leek, R., Harris, A., and McGee, J. O. (1995). Cytokine regulation of angiogenesis in breast cancer: the role of tumor-associated macrophages. J. Leukoc. Biol. 57, 747-751.
16. Lin, E. Y., Nguyen, A. V., Russell, R. G., and Pollard, J. W. (2001). Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy. J. Exp. Med. 193, 727-739.
17. Lippincott, J., and Li, R. (2000). Involvement of PCH family proteins in cytokinesis and actin distribution. Microsc. Res. Tech. 49, 168-172.
18. Modregger, J., Ritter, B., Witter, B., Paulsson, M., and Plomann, M. (2000). All three PACSIN isoforms bind to endocytic proteins and inhibit endocytosis. J. Cell Sci. 113, 4511-4521.
19. Morgan, C. J., Pollard, J. W., and Stanley, E. R. (1987). Isolation and characterization of a cloned growth factor dependent macrophage cell line, BAC12F5. J. Cell. Physiol. 130, 420-427.
20. Muller, A. J., Young, J. C., Pendergast, A. M., Pondel, M., Landau, N. R., Littman, D. R., and Witte, O. (1991). BCR first exon sequences specifically activate the BCR/ABL tyrosine kinase oncogene of Philadelphia chromosome-positive human leukemias. Mol. Cell. Biol. 11, 1785-1792.
21. Murray, J. W., Edmonds, B. T., Liu, C., and Condeelis, J. (1997). Elongation factor-1α alters the initial rates and final extent of actin polymerization and depolymerization. J. Cell Biol. 135, 1309-1321.
22. Nikki, M., Merilainen, J., and Lehto, V. P. (2002). Focal adhesion protein FAP52 self-associates through a sequence conserved among members of the PCH family of proteins. Biochemistry 41, 6320-6329.
23. Persons, D. A., Allay, J. A., Allay, E. R., Ashmun, R. A., Orlic, D., Jane, S. M., Cunningham, J. M., and Nienhuis, A. W. (1999). Enforced expression of the GATA-2 transcription factor blocks normal hematopoiesis. Blood 93, 488-499.
24. Pixley, F. J., Lee, P.S.W., Condeelis, J. S., and Stanley, E. R. (2001). Protein tyrosine phosphataseφ regulates paxillin tyrosine phosphorylation and mediates colony-stimulating-factor 1-induced morphological changes in macrophages. Mol. Cell. Biol. 21, 1795-1809.
25. Pixley, F. J., and Stanley, E. R. (2004). CSF-1 regulation of the wandering macrophage: complexity in action. Trends Cell Biol. 14, 628-638.
26. Pollard, J. W., and Stanley, E. R. (1996). Pleiotropic roles for CSF-1 in development defined by the mouse mutation osteopetrotic. Adv. Dev. Biochem. 4, 153-193.
27. Qualmann, B., and Kelly, R. B. (2000). Syndapin isoforms participate in receptor-mediated endocytosis and actin organization. J. Cell Biol. 148, 1047-1062.
28. Rust, W. L., Huff, J. L., and Plopper, G. E. (2000). Screening assay for promigratory/antimigratory compounds. Anal Biochem. 280, 11-19.
29. Sherr, C. J., Rettenmier, C. W., Sacca, R., Roussel, M. F., Look, A. T., and Stanley, E. R. (1985). The c-fms proto-oncogene product is related to the receptor for the mononuclear phagocyte growth factor, CSF-1. Cell 41, 665-676.
30. Stanley, E. R., Chen, D. M., and Lin, H.-S. (1978). Induction of macrophage production and proliferation by a purified colony stimulating factor, Nature 274, 168-170.
31. Stoy, N. (2001). Macrophage biology and pathobiology in the evolution of immune responses: a functional analysis. Pathobiology 69, 179-211.
32. Svitkina, T. M., Bulanova, E. A., Chaga, O. Y., Vignjevic, D. M., Kojima, S., Vasiliev, J. M., and Borisy, G. (2003). Mechanism of filopodia initiation by reorganization of a dendritic network. J. Cell Biol. 160, 409-421.
33. Takenawa, T., and Miki, H. (2001). WASP and WAVE family proteins: key molecules for rapid rearrangement of cortical actin filaments and cell movement. J. Cell Sci. 114, 1801-1809.
34. Tian, L., Nelson, D. L., and Stewart, D. M. (2000). Cdc42-interacting protein 4 mediates binding of the Wiskott-Aldrich syndrome protein to microtubules. J. Biol. Chem. 275, 7854-7861.
35. Tushinski, R. J., Oliver, I. T., Guilbert, L. J., Tynan, P. W., Warner, J. R., and Stanley, E. R. (1982). Survival of mononuclear phagocytes depends on a lineage-specific growth factor that the differentiated cells selectively destroy. Cell 28, 71-81.
36. Vignjevic, D., Yarar, D., Welch, M. D., Peloquin, J., Svitkina, T., and Borisy, G. (2003). Formation of filopodia-like bundles in vitro from a dendritic network. J. Cell Biol. 160, 951-962.
37. Webb, S. E., Pollard, J. W., and Jones, G. E. (1996). Direct observation and quantification of macrophage chemoattraction to the growth factor CSF-1. J. Cell Sci. 109, 793-803.
38. Wise, C. A., Gillum, J. D., Seidman, C. E., Lindor, N. M., Veile, R., Bashiardes, S., and Lovett, M. (2002). Mutations in CD2BP1 disrupt binding to FTP PEST and are responsible for PAPA syndrome, an autoinflammatory disorder. Hum. Mol. Genet. 11, 961-969.
39. Wu, Y., Dowbenko, D., and Lasky, L. K. (1998a). PSTPIP 2, a second tyrosine phosphorylated, cytoskeletal associated protein that binds a PEST-type protein-tyrosine phosphatase. J. Biol. Chem. 273, 30487-30496.
40. Wu, Y., Spencer, S. D., and Lasky, L. A. (1998b). Tyrosine phosphorylation regulates the SH3-mediated binding of the Wiskott-Aldrich syndrome protein to PSTPIP, a cytoskeletal-associated protein. J. Biol. Chem. 273, 5765-5770.
41. Wyckoff, J., Wang, W., Lin, E. L., Wang, Y., Pixley, F., Stanley, E. R., Graf, T., Pollard, J. W., Segall, J., and Condeelis, J. (2004). A paracrine loop between tumor cells and macrophages is required for tumor cell migration in mammary tumors. Cancer Res. 64, 7022-7029.
42. Yeung, Y.-G., Berg, K. L., Pixley, F. J., Angeletti, R. H., and Stanley, E. R. (1992). Protein tyrosine phosphatase-1C is rapidly phosphorylated in tyrosine in macrophages in response to colony stimulating factor-1, J. Biol. Chem. 267, 23447-23450.
43. Yeung, Y.-G., and Stanley, E. R. (1990). Colony stimulating factor-1 receptor. In: Receptor Purification, ed. G. Litwack, Clifton, NJ: Humana Press, 315-328.
44. Yeung, Y.-G., and Stanley, E. R. (2003). Proteomic approaches to the analysis of early events in colony-stimulating factor-1 signal transduction. Mol. Cell Proteomics 2, 1143-1155.
45. Yeung, Y.-G., Wang, Y., Einstein, D. B., Lee, P.S.W., and Stanley, E. R. (1998a). Colony-stimulating factor-1 stimulates the formation of multimeric cytosolic complexes of signaling proteins and cytoskeletal components in macrophages. J. Biol. Chem. 273, 17128-17137.
46. Yeung, Y. G., Soldera, S., and Stanley, E. R. (1998b). A novel macrophage actin-associated protein (MAYP) is tyrosine- phosphorylated after colony stimulating factor-1 stimulation. J. Biol. Chem. 273, 30638-30642.