A chemical biology approach demonstrates G protein βγ subunits are sufficient to mediate directional neutrophil chemotaxis

Journal of Biological Chemistry

Volumn 289, Issue 25, 2014, Pages 17791-17801

  Surve, Chinmay R ^a   Lehmann, David ^b   Smrcka, Alan V ^a,b  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b UNIVERSITY OF ROCHESTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL ACTIVATION; DIGITAL STORAGE; ENZYME ACTIVITY; MOLECULES; PEPTIDES;

CHEMICAL BIOLOGY; DOWNSTREAM TARGET; EXTRACELLULAR SIGNAL-REGULATED KINASE; G PROTEIN COUPLED RECEPTORS; NUCLEOTIDE EXCHANGE; PHOSPHOINOSITIDE 3-KINASE; PROTEIN KINASE B; SMALL MOLECULES;

BIOCHEMISTRY;

AGENTS AFFECTING PROTEIN METABOLISM; AMINOQUINURIDE; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN BETA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN GAMMA SUBUNIT; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE GAMMA; PHOSPHOLIPASE C; PROTEIN KINASE B; UNCLASSIFIED DRUG;

ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CONTROLLED STUDY; DISSOCIATION; ENZYME ACTIVATION; HL 60 CELL LINE; IN VITRO STUDY; NEUTROPHIL CHEMOTAXIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

CELL SIGNALING; CHEMICAL BIOLOGY; CHEMOTAXIS; G PROTEIN; G PROTEIN-COUPLED RECEPTOR (GPCR);

ANIMALS; CALCIUM; CHEMOTAXIS; CYCLOHEXANES; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; GTP-BINDING PROTEIN BETA SUBUNITS; GTP-BINDING PROTEIN GAMMA SUBUNITS; HL-60 CELLS; HUMANS; MICE; N-FORMYLMETHIONINE LEUCYL-PHENYLALANINE; NEUTROPHILS; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; XANTHENES;

EID: 84903484347     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.576827     Document Type: Article

References (36)

1. Gilman, A. G. (1987) G proteins: transducers of receptor-generated signals. Annu. Rev. Biochem. 56, 615-649
2. Oldham, W. M., and Hamm, H. E. (2006) Structural basis of function in heterotrimeric G proteins. Q. Rev. Biophys. 39, 117-166 (Pubitemid 44706968)
3. Lin, Y., and Smrcka, A. V. (2011) Understanding molecular recognition by G protein βγ subunits on the path to pharmacological targeting. Mol. Pharmacol. 80, 551-557
4. Bonacci, T. M., Mathews, J. L., Yuan, C., Lehmann, D. M., Malik, S., Wu, D., Font, J. L., Bidlack, J. M., and Smrcka, A. V. (2006) Differential targeting of Gβγ-subunit signaling with small molecules. Science 312, 443-446
5. Ford, C. E., Skiba, N. P., Bae, H., Daaka, Y., Reuveny, E., Shekter, L. R., Rosal, R., Weng, G., Yang, C. S., Iyengar, R., Miller, R. J., Jan, L. Y., Lefkowitz, R. J., and Hamm, H. E. (1998) Molecular basis for interactions of G protein βγ subunits with effectors. Science 280, 1271-1274 (Pubitemid 28269623)
6. Scott, J. K., Huang, S. F., Gangadhar, B. P., Samoriski, G. M., Clapp, P., Gross, R. A., Taussig, R., and Smrcka, A. V. (2001) Evidence that a protein-protein interaction "hot spot" on heterotrimeric G protein βγ subunits is used for recognition of a subclass of effectors. EMBO J. 20, 767-776 (Pubitemid 32167641)
7. Rossi, D., and Zlotnik, A. (2000) The biology of chemokines and their receptors. Annu. Rev. Immunol. 18, 217-242
8. s. Proc. Natl. Acad. Sci. U.S.A. 94, 14489-14494
9. Kölsch, V., Charest, P. G., and Firtel, R. A. (2008) The regulation of cell motility and chemotaxis by phospholipid signaling. J. Cell Sci. 121, 551-559 (Pubitemid 351524153)
10. Wu, D., Huang, C. K., and Jiang, H. (2000) Roles of phospholipid signaling in chemoattractant-induced responses. J. Cell Sci. 113, 2935-2940
11. Li, Z., Hannigan, M., Mo, Z., Liu, B., Lu, W., Wu, Y., Smrcka, A. V., Wu, G., Li, L., Liu, M., Huang, C.-K., and Wu, D. (2003) Directional sensing requires Gβγ-mediated PAK1 and PIXα-dependent activation of Cdc42. Cell 114, 215-227 (Pubitemid 36936915)
12. Yagi, H., Tan, W., Dillenburg-Pilla, P., Armando, S., Amornphimoltham, P., Simaan, M., Weigert, R., Molinolo, A. A., Bouvier, M., and Gutkind, J. S. (2011) A synthetic biology approach reveals a CXCR4-G13-Rho signaling axis driving transendothelial migration of metastatic breast cancer cells. Sci. Signal. 4, ra60
13. 13 is required for growth factor-induced cell migration. Dev. Cell 10, 707-718
14. Décaillot, F. M., Kazmi, M. A., Lin, Y., Ray-Saha, S., Sakmar, T. P., and Sachdev, P. (2011) CXCR7/CXCR4 heterodimer constitutively recruits β-arrestin to enhance cell migration. J. Biol. Chem. 286, 32188-32197
15. DeFea, K. A. (2007) Stop that cell! β-Arrestin-dependent chemotaxis: a tale of localized actin assembly and receptor desensitization. Annu. Rev. Physiol. 69, 535-560
16. Vroon, A., Heijnen, C. J., and Kavelaars, A. (2006) GRKs and arrestins: regulators of migration and inflammation. J. Leukocyte Biol. 80, 1214-1221 (Pubitemid 44904958)
17. Penela, P., Ribas, C., Aymerich, I., and Mayor, F. (2009) New roles of G protein-coupled receptor kinase 2 (GRK2) in cell migration. Cell Adh. Migr. 3, 19-23
18. 2 heterodimer. Biochemistry 44, 10593-10604
19. Kozasa, T., and Gilman, A. G. (1995) Purification of recombinant G proteins from Sf9 cells by hexahistidine tagging of associated subunits: characterization of α12 and inhibition of adenylyl cyclase by αz. J. Biol. Chem. 270, 1734-1741
20. Smrcka, A. V., and Scott, J. K. (2002) Discovery of ligands for βγ subunits from phage-displayed peptide libraries. Methods Enzymol. 344, 557-576
21. Seneviratne, A. M., Burroughs, M., Giralt, E., and Smrcka, A. V. (2011) Direct-reversible binding of small molecules to G protein βγ subunits. Biochim. Biophys. Acta 1814, 1210-1218
22. Bonacci, T. M., Ghosh, M., Malik, S., and Smrcka, A. V. (2005) Regulatory interactions between the amino terminus of G-protein βγ subunits and the catalytic domain of PLCβ2. J. Biol. Chem. 280, 10174-10181 (Pubitemid 40395871)
23. Goubaeva, F., Ghosh, M., Malik, S., Yang, J., Hinkle, P. M., Griendling, K. K., Neubig, R. R., and Smrcka, A. V. (2003) Stimulation of cellular signaling and G protein subunit dissociation by G protein βγ subunit-binding peptides. J. Biol. Chem. 278, 19634-19641 (Pubitemid 36799147)
24. i and βγ binding: measuring high affinity interactions in a lipid environment using flow cytometry. J. Biol. Chem. 273, 7934-7940
25. 35S]GTPγS binding. Methods Mol. Biol. 237, 135-143
26. Parish, C. A., Smrcka, A. V., and Rando, R. R. (1995) Functional significance of βγ subunit carboxymethylation for the activation of phospholipase C and phosphoinositide 3-kinase. Biochemistry 34, 7722-7727
27. Lehmann, D. M., Seneviratne, A. M., and Smrcka, A. V. (2008) Small molecule disruption of G protein βγ subunit signaling inhibits neutrophil chemotaxis and inflammation. Mol. Pharmacol. 73, 410-418 (Pubitemid 351159211)
28. Casey, L. M., Pistner, A. R., Belmonte, S. L., Migdalovich, D., Stolpnik, O., Nwakanma, F. E., Vorobiof, G., Dunaevsky, O., Matavel, A., Lopes, C. M., Smrcka, A. V., and Blaxall, B. C. (2010) Small molecule disruption of Gβγ signaling inhibits the progression of heart failure. Circ. Res. 107, 532-539
29. Mathews, J. L., Smrcka, A. V., and Bidlack, J. M. (2008) A novel Gβγ subunit inhibitor selectively modulates μ-opioid-dependent antinociception and attenuates acute morphine-induced antinociceptive tolerance and dependence. J. Neurosci. 28, 12183-12189
30. Inoue, T., and Meyer, T. (2008) Synthetic activation of endogenous PI3K and Rac identifies an AND gate switch for cell polarization and migration. PloS One 3, e3068
31. Ghosh, M., Peterson, Y. K., Lanier, S. M., and Smrcka, A. V. (2003) Receptor and nucleotide exchange independent mechanisms for promoting G protein subunit dissociation. J. Biol. Chem. 273, 34747-34750 (Pubitemid 37102232)
32. Kirui, J. K., Xie, Y., Wolff, D. W., Jiang, H., Abel, P. W., and Tu, Y. (2010) Gβγ signaling promotes breast cancer cell migration and invasion. J. Pharmacol. Exp. Ther. 333, 393-403
33. Schuksz, M., Fuster, M. M., Brown, J. R., Crawford, B. E., Ditto, D. P., Lawrence, R., Glass, C. A., Wang, L., Tor, Y., and Esko, J. D. (2008) Surfen, a small molecule antagonist of heparan sulfate. Proc. Natl. Acad. Sci. U.S.A. 105, 13075-13080
34. Roan, N. R., Sowinski, S., Münch, J., Kirchhoff, F., and Greene, W. C. (2010) Aminoquinoline surfen inhibits the action of SEVI (semen-derived enhancer of viral infection). J. Biol. Chem. 285, 1861-1869
35. Panchal, R. G., Hermone, A. R., Nguyen, T. L., Wong, T. Y., Schwarzenbacher, R., Schmidt, J., Lane, D., McGrath, C., Turk, B. E., Burnett, J., Aman, M. J., Little, S., Sausville, E. A., Zaharevitz, D. W., Cantley, L. C., Liddington, R. C., Gussio, R., and Bavari, S. (2004) Identification of small molecule inhibitors of anthrax lethal factor. Nat. Struct. Mol. Biol. 11, 67-72 (Pubitemid 38173443)
36. Kamakura, S., Nomura, M., Hayase, J., Iwakiri, Y., Nishikimi, A., Takayanagi, R., Fukui, Y., and Sumimoto, H. (2013) The cell polarity protein mInsc regulates neutrophil chemotaxis via a noncanonical G protein signaling pathway. Dev. Cell 26, 292-302