Abr and Bcr, Two Homologous Rac GTPase-Activating Proteins, Control Multiple Cellular Functions of Murine Macrophages

REFERENCES

• Aghazadeh, B., K. Zhu, T. J. Kubiseski, G. A. Liu, T. Pawson, Y. Zheng, and M. K. Rosen. 1998. Structure and mutagenesis of the Dbl homology domain. Nat. Struct. Biol. 5:1098–1107.
   PubMedGoogle Scholar
• Allen, W. E., G. E. Jones, J. W. Pollard, and A. J. Ridley. 1997. Rho, Rac and Cdc42 regulate actin organization and cell adhesion in macrophages. J. Cell Sci. 110:707–720.
   PubMed Web of Science ®Google Scholar
• Allen, W. E., D. Zicha, A. J. Ridley, and G. E. Jones. 1998. A role for Cdc42 in macrophage chemotaxis. J. Cell Biol. 141:1147–1157.
   PubMed Web of Science ®Google Scholar
• Benard, V., and G. M. Bokoch. 2002. Assay of Cdc42, Rac, and Rho GTPase activation by affinity methods. Methods Enzymol. 345:349–359.
   PubMed Web of Science ®Google Scholar
• Bernards, A. 2003. GAPs galore! A survey of putative Ras superfamily GTPase activating proteins in man and Drosophila. Biochim. Biophys. Acta 1603:47–82.
   PubMed Web of Science ®Google Scholar
• Bernards, A., and J. Settleman. 2004. GAP control: regulating the regulators of small GTPases. Trends Cell Biol. 14:377–385.
   PubMed Web of Science ®Google Scholar
• Bokoch, G. M. 2005. Regulation of innate immunity by Rho GTPases. Trends Cell Biol. 15:163–171.
   PubMed Web of Science ®Google Scholar
• Castellano, F., P. Montcourrier, and P. Chavrier. 2000. Membrane recruitment of Rac1 triggers phagocytosis. J. Cell Sci. 113:2955–2961.
   PubMedGoogle Scholar
• Cho, S. Y., and R. L. Klemke. 2002. Purification of pseudopodia from polarized cells reveals redistribution and activation of Rac through assembly of a CAS/Crk scaffold. J. Cell Biol. 156:725–736.
   PubMed Web of Science ®Google Scholar
• Chuang, T. H., X. Xu, V. Kaartinen, N. Heisterkamp, J. Groffen, and G. M. Bokoch. 1995. Abr and Bcr are multifunctional regulators of the Rho GTP-binding protein family. Proc. Natl. Acad. Sci. USA 92:10282–10286.
   PubMed Web of Science ®Google Scholar
• Cougoule, C., S. Hoshino, A. Dart, J. Lim, and E. Caron. 2006. Dissociation of recruitment and activation of the small G-protein Rac during Fcγ receptor-mediated phagocytosis. J. Biol. Chem. 281:8756–8764.
   PubMedGoogle Scholar
• Cunnick, J., P. Kaur, Y. Cho, J. Groffen, and N. Heisterkamp. 2006. Use of bone marrow-derived macrophages to model murine innate immune responses. J. Immunol. Methods 311:96–105.
   PubMedGoogle Scholar
• del Pozo, M. A., L. S. Price, N. B. Alderson, X. D. Ren, and M. A. Schwartz. 2000. Adhesion to the extracellular matrix regulates the coupling of the small GTPase Rac to its effector PAK. EMBO J. 19:2008–2014.
   PubMed Web of Science ®Google Scholar
• Diakonova, M., G. Bokoch, and J. A. Swanson. 2002. Dynamics of cytoskeletal proteins during Fcγ receptor-mediated phagocytosis in macrophages. Mol. Biol. Cell 13:402–411.
   PubMed Web of Science ®Google Scholar
• Etienne-Manneville, S., and A. Hall. 2002. Rho GTPases in cell biology. Nature 420:629–635.
   PubMed Web of Science ®Google Scholar
• Gardiner, E. M., K. N. Pestonjamasp, B. P. Bohl, C. Chamberlain, K. M. Hahn, and G. M. Bokoch. 2002. Spatial and temporal analysis of Rac activation during live neutrophil chemotaxis. Curr. Biol. 12:2029–2034.
   PubMedGoogle Scholar
• Haataja, L., V. Kaartinen, J. Groffen, and N. Heisterkamp. 2002. The small GTPase Rac3 interacts with the integrin-binding protein CIB and promotes integrin α(IIb)β(3)-mediated adhesion and spreading. J. Biol. Chem. 277:8321–8328.
   PubMed Web of Science ®Google Scholar
• Hall, A. B., M. A. Gakidis, M. Glogauer, J. L. Wilsbacher, S. Gao, W. Swat, and J. S. Brugge. 2006. Requirements for Vav guanine nucleotide exchange factors and Rho GTPases in FcγR- and complement-mediated phagocytosis. Immunity 24:305–316.
   PubMedGoogle Scholar
• Heisterkamp, N., and J. Groffen. 2002. Philadelphia-positive leukemia: a personal perspective. Oncogene 21:8536–8540.
   PubMed Web of Science ®Google Scholar
• Heisterkamp, N., V. Kaartinen, S. van Soest, G. M. Bokoch, and J. Groffen. 1993. Human ABR encodes a protein with GAPrac activity and homology to the DBL nucleotide exchange factor domain. J. Biol. Chem. 268:16903–16906.
   PubMed Web of Science ®Google Scholar
• Heisterkamp, N., C. Morris, and J. Groffen. 1989. ABR, an active BCR-related gene. Nucleic Acids Res. 17:8821–8831.
   PubMedGoogle Scholar
• Hemmeryckx, B., A. van Wijk, A. Reichert, V. Kaartinen, R. de Jong, P. K. Pattengale, I. Gonzalez-Gomez, J. Groffen, and N. Heisterkamp. 2001. Crkl enhances leukemogenesis in BCR/ABL P190 transgenic mice. Cancer Res. 61:1398–1405.
   PubMedGoogle Scholar
• Hirose, K., T. Kawashima, I. Iwamoto, T. Nosaka, and T. Kitamura. 2001. MgcRacGAP is involved in cytokinesis through associating with mitotic spindle and midbody. J. Biol. Chem. 276:5821–5828.
   PubMedGoogle Scholar
• Hoppe, A. D., and J. A. Swanson. 2004. Cdc42, Rac1, and Rac2 display distinct patterns of activation during phagocytosis. Mol. Biol. Cell 15:3509–3519.
   PubMed Web of Science ®Google Scholar
• Jaffe, A. B., and A. Hall. 2005. Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21:247–269.
   PubMed Web of Science ®Google Scholar
• Jones, G. E., W. E. Allen, and A. J. Ridley. 1998. The Rho GTPases in macrophage motility and chemotaxis. Cell Adhes. Commun. 6:237–245.
   PubMed Web of Science ®Google Scholar
• Kaartinen, V., I. Gonzalez-Gomez, J. W. Voncken, L. Haataja, E. Faure, A. Nagy, J. Groffen, and N. Heisterkamp. 2001. Abnormal function of astroglia lacking Abr and Bcr RacGAPs. Development 128:4217–4227.
   PubMed Web of Science ®Google Scholar
• Kaartinen, V., A. Nagy, I. Gonzalez-Gomez, J. Groffen, and N. Heisterkamp. 2002. Vestibular dysgenesis in mice lacking Abr and Bcr Cdc42/RacGAPs. Dev. Dyn. 223:517–525.
   PubMedGoogle Scholar
• Lee, J. S., K. Kamijo, N. Ohara, T. Kitamura, and T. Miki. 2004. MgcRacGAP regulates cortical activity through RhoA during cytokinesis. Exp. Cell Res. 293:275–282.
   PubMedGoogle Scholar
• Leeuwen, F. N., H. E. Kain, R. A. Kammen, F. Michiels, O. W. Kranenburg, and J. G. Collard. 1997. The guanine nucleotide exchange factor Tiam1 affects neuronal morphology; opposing roles for the small GTPases Rac and Rho. J. Cell Biol. 139:797–807.
   PubMed Web of Science ®Google Scholar
• Li, Y. M., G. Baviello, H. Vlassara, and T. Mitsuhashi. 1997. Glycation products in aged thioglycollate medium enhance the elicitation of peritoneal macrophages. J. Immunol. Methods 201:183–188.
   PubMed Web of Science ®Google Scholar
• Liang, X., N. A. Draghi, and M. D. Resh. 2004. Signaling from integrins to Fyn to Rho family GTPases regulates morphologic differentiation of oligodendrocytes. J. Neurosci. 24:7140–7149.
   PubMed Web of Science ®Google Scholar
• Ligeti, E., and J. Settleman. 2006. Regulation of RhoGAP specificity by phospholipids and prenylation. Methods Enzymol. 406:104–117.
   PubMedGoogle Scholar
• Malmberg, E. K., C. X. Andersson, M. Gentzsch, J. H. Chen, A. Mengos, L. Cui, G. C. Hansson, and J. R. Riordan. 2004. Bcr (breakpoint cluster region) protein binds to PDZ-domains of scaffold protein PDZK1 and vesicle coat protein Mint3. J. Cell Sci. 117:5535–5541.
   PubMedGoogle Scholar
• Massol, P., P. Montcourrier, J. C. Guillemot, and P. Chavrier. 1998. Fc receptor-mediated phagocytosis requires CDC42 and Rac1. EMBO J. 17:6219–6229.
   PubMed Web of Science ®Google Scholar
• Moon, S. Y., and Y. Zheng. 2003. Rho GTPase-activating proteins in cell regulation. Trends Cell Biol. 13:13–22.
   PubMed Web of Science ®Google Scholar
• National Research Council. 1996. Guide for the care and use of laboratory animals. National Academy Press, Washington, D.C.
   Google Scholar
• Nobes, C. D., and A. Hall. 1999. Rho GTPases control polarity, protrusion, and adhesion during cell movement. J. Cell Biol. 144:1235–1244.
   PubMed Web of Science ®Google Scholar
• Nobes, C. D., and A. Hall. 1995. Rho, Rac, and Cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81:53–62.
   PubMed Web of Science ®Google Scholar
• Patel, J. C., A. Hall, and E. Caron. 2002. Vav regulates activation of Rac but not Cdc42 during FcγR-mediated phagocytosis. Mol. Biol. Cell 13:1215–1226.
   PubMed Web of Science ®Google Scholar
• Post, P. L., G. M. Bokoch, and M. S. Mooseker. 1998. Human myosin-IXb is a mechanochemically active motor and a GAP for rho. J. Cell Sci. 111:941–950.
   PubMedGoogle Scholar
• Prieto-Sanchez, R. M., I. M. Berenjeno, and X. R. Bustelo. 2006. Involvement of the Rho/Rac family member RhoG in caveolar endocytosis. Oncogene 25:2961–2973.
   PubMed Web of Science ®Google Scholar
• Radziwill, G., R. A. Erdmann, U. Margelisch, and K. Moelling. 2003. The Bcr kinase downregulates Ras signaling by phosphorylating AF-6 and binding to its PDZ domain. Mol. Cell. Biol. 23:4663–4672.
   PubMed Web of Science ®Google Scholar
• Ren, X. D., and M. A. Schwartz. 2000. Determination of GTP loading on Rho. Methods Enzymol. 325:264–272.
   PubMed Web of Science ®Google Scholar
• Ridley, A. J. 2001. Rho GTPases and cell migration. J. Cell Sci. 114:2713–2722.
   PubMed Web of Science ®Google Scholar
• Ridley, A. J. 2001. Rho proteins, PI 3-kinases, and monocyte/macrophage motility. FEBS Lett. 498:168–171.
   PubMedGoogle Scholar
• Ridley, A. J. 2004. Pulling back to move forward. Cell 116:357–358.
   PubMedGoogle Scholar
• Schmidt, A., and A. Hall. 2002. Guanine nucleotide exchange factors for Rho GTPases: turning on the switch. Genes Dev. 16:1587–1609.
   PubMed Web of Science ®Google Scholar
• Servant, G., O. D. Weiner, P. Herzmark, T. Balla, J. W. Sedat, and H. R. Bourne. 2000. Polarization of chemoattractant receptor signaling during neutrophil chemotaxis. Science 287:1037–1040.
   PubMed Web of Science ®Google Scholar
• Sordella, R., M. Classon, K. Q. Hu, S. F. Matheson, M. R. Brouns, B. Fine, L. Zhang, H. Takami, Y. Yamada, and J. Settleman. 2002. Modulation of CREB activity by the Rho GTPase regulates cell and organism size during mouse embryonic development. Dev. Cell 2:553–565.
   PubMedGoogle Scholar
• Stanley, E. R. 1997. Murine bone marrow-derived macrophages. Methods Mol. Biol. 75:301–304.
   PubMedGoogle Scholar
• Swanson, J. A., M. T. Johnson, K. Beningo, P. Post, M. Mooseker, and N. Araki. 1999. A contractile activity that closes phagosomes in macrophages. J. Cell Sci. 112:307–316.
   PubMed Web of Science ®Google Scholar
• Tan, E. C., T. Leung, E. Manser, and L. Lim. 1993. The human active breakpoint cluster region-related gene encodes a brain protein with homology to guanine nucleotide exchange proteins and GTPase-activating proteins. J. Biol. Chem. 268:27291–27298.
   PubMed Web of Science ®Google Scholar
• Thompson, C. D., M. R. Frazier-Jessen, R. Rawat, R. P. Nordan, and R. T. Brown. 1999. Evaluation of methods for transient transfection of a murine macrophage cell line, RAW 264.7. BioTechniques 27:824–830, 832.
   PubMedGoogle Scholar
• Vedham, V., H. Phee, and K. M. Coggeshall. 2005. Vav activation and function as a rac guanine nucleotide exchange factor in macrophage colony-stimulating factor-induced macrophage chemotaxis. Mol. Cell. Biol. 25:4211–4220.
   PubMed Web of Science ®Google Scholar
• Vincent, S., and J. Settleman. 1999. Inhibition of RhoGAP activity is sufficient for the induction of Rho-mediated actin reorganization. Eur. J. Cell Biol. 78:539–548.
   PubMedGoogle Scholar
• Voncken, J. W., H. van Schaick, V. Kaartinen, K. Deemer, T. Coates, B. Landing, P. Pattengale, O. Dorseuil, G. M. Bokoch, J. Groffen, et al. 1995. Increased neutrophil respiratory burst in bcr-null mutants. Cell 80:719–728.
   PubMed Web of Science ®Google Scholar
• Wang, L., L. Yang, K. Burns, C. Y. Kuan, and Y. Zheng. 2005. Cdc42GAP regulates c-Jun N-terminal kinase (JNK)-mediated apoptosis and cell number during mammalian perinatal growth. Proc. Natl. Acad. Sci. USA 102:13484–13489.
   PubMedGoogle Scholar
• Wang, L., L. Yang, M. D. Filippi, D. A. Williams, and Y. Zheng. 2006. Genetic deletion of Cdc42GAP reveals a role of Cdc42 in erythropoiesis and hematopoietic stem/progenitor cell survival, adhesion, and engraftment. Blood 107:98–105.
   PubMedGoogle Scholar
• Watanabe, T., J. Noritake, and K. Kaibuchi. 2005. Regulation of microtubules in cell migration. Trends Cell Biol. 15:76–83.
   PubMed Web of Science ®Google Scholar
• Wells, C. M., P. J. Bhavsar, I. R. Evans, E. Vigorito, M. Turner, V. Tybulewicz, and A. J. Ridley. 2005. Vav1 and Vav2 play different roles in macrophage migration and cytoskeletal organization. Exp. Cell Res. 310:303–310.
   PubMed Web of Science ®Google Scholar
• Wells, C. M., M. Walmsley, S. Ooi, V. Tybulewicz, and A. J. Ridley. 2004. Rac1-deficient macrophages exhibit defects in cell spreading and membrane ruffling but not migration. J. Cell Sci. 117:1259–1268.
   PubMed Web of Science ®Google Scholar
• Wennerberg, K., and C. J. Der. 2004. Rho-family GTPases: it's not only Rac and Rho (and I like it). J. Cell Sci. 117:1301–1312.
   PubMed Web of Science ®Google Scholar
• Wennerberg, K., S. M. Ellerbroek, R. Y. Liu, A. E. Karnoub, K. Burridge, and C. J. Der. 2002. RhoG signals in parallel with Rac1 and Cdc42. J. Biol. Chem. 277:47810–47817.
   PubMed Web of Science ®Google Scholar
• Yamauchi, A., C. Kim, S. Li, C. C. Marchal, J. Towe, S. J. Atkinson, and M. C. Dinauer. 2004. Rac2-deficient murine macrophages have selective defects in superoxide production and phagocytosis of opsonized particles. J. Immunol. 173:5971–5979.
   PubMedGoogle Scholar
• Zhang, Q., J. Calafat, H. Janssen, and S. Greenberg. 1999. ARF6 is required for growth factor- and Rac-mediated membrane ruffling in macrophages at a stage distal to rac membrane targeting. Mol. Cell. Biol. 19:8158–8168.
   PubMedGoogle Scholar