Autoinhibition and phosphorylation-induced activation of phospholipase C-γ isozymes

Biochemistry

Volumn 52, Issue 28, 2013, Pages 4810-4819

  Hajicek, Nicole ^a   Charpentier, Thomas H ^a   Rush, Jeremy R ^a,b   Harden, T Kendall ^a   Sondek, John ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b BOEHRINGER INGELHEIM VETMEDICA INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRITICAL DETERMINANT; EXTRACELLULAR STIMULI; INTRAMOLECULAR INTERACTIONS; MOLECULAR MECHANISM; PHOSPHOLIPASE ACTIVITY; PHOSPHORYLATED TYROSINE; SIGNALING CASCADES; TYROSINE PHOSPHORYLATION;

AMINO ACIDS; ISOENZYMES; PHOSPHORYLATION;

PEPTIDES;

PHOSPHOLIPASE C GAMMA; PROTEIN SH2; TYROSINE;

ARTICLE; CONTROLLED STUDY; CRYSTALLIZATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; CRYSTALLOGRAPHY, X-RAY; ENZYME ACTIVATION; ISOENZYMES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHOSPHOLIPASE C GAMMA; PHOSPHORYLATION; SEQUENCE HOMOLOGY, AMINO ACID; SRC HOMOLOGY DOMAINS;

EID: 84880548414     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi400433b     Document Type: Article

References (39)

1. Harden, T. K. and Sondek, J. (2006) Regulation of phospholipase C isozymes by Ras superfamily GTPases Annu. Rev. Pharmacol. Toxicol. 46, 355-379
2. Rhee, S. G. (2001) Regulation of phosphoinositide-specific phospholipase C Annu. Rev. Biochem. 70, 281-312
3. Hicks, S. N., Jezyk, M. R., Gershburg, S., Seifert, J. P., Harden, T. K., and Sondek, J. (2008) General and versatile autoinhibition of PLC isozymes Mol. Cell 31, 383-394
4. Jezyk, M. R., Snyder, J. T., Gershberg, S., Worthylake, D. K., Harden, T. K., and Sondek, J. (2006) Crystal structure of Rac1 bound to its effector phospholipase C-β2 Nat. Struct. Mol. Biol. 13, 1135-1140
5. q signaling complex Science 330, 974-980
6. Nishibe, S., Wahl, M. I., Hernandez-Sotomayor, S. M., Tonks, N. K., Rhee, S. G., and Carpenter, G. (1990) Increase of the catalytic activity of phospholipase C-γ1 by tyrosine phosphorylation Science 250, 1253-1256
7. Kim, H. K., Kim, J. W., Zilberstein, A., Margolis, B., Kim, J. G., Schlessinger, J., and Rhee, S. G. (1991) PDGF stimulation of inositol phospholipid hydrolysis requires PLC-γ1 phosphorylation on tyrosine residues 783 and 1254 Cell 65, 435-441
8. Ozdener, F., Dangelmaier, C., Ashby, B., Kunapuli, S. P., and Daniel, J. L. (2002) Activation of phospholipase Cγ2 by tyrosine phosphorylation Mol. Pharmacol. 62, 672-679
9. Gresset, A., Hicks, S. N., Harden, T. K., and Sondek, J. (2010) Mechanism of phosphorylation-induced activation of phospholipase C-γ isozymes J. Biol. Chem. 285, 35836-35847
10. Serrano, C. J., Graham, L., DeBell, K., Rawat, R., Veri, M. C., Bonvini, E., Rellahan, B. L., and Reischl, I. G. (2005) A new tyrosine phosphorylation site in PLCγ1: The role of tyrosine 775 in immune receptor signaling J. Immunol. 174, 6233-6237
11. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276, 307-326
12. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software J. Appl. Crystallogr. 40, 658-674
13. Winn, M. D., Ballard, C. C., Cowtan, K. D., Dodson, E. J., Emsley, P., Evans, P. R., Keegan, R. M., Krissinel, E. B., Leslie, A. G., McCoy, A., McNicholas, S. J., Murshudov, G. N., Pannu, N. S., Potterton, E. A., Powell, H. R., Read, R. J., Vagin, A., and Wilson, K. S. (2011) Overview of the CCP4 suite and current developments Acta Crystallogr. D67, 235-242
14. Murshudov, G. N., Skubak, P., Lebedev, A. A., Pannu, N. S., Steiner, R. A., Nicholls, R. A., Winn, M. D., Long, F., and Vagin, A. A. (2011) REFMAC5 for the refinement of macromolecular crystal structures Acta Crystallogr. D67, 355-367
15. Emsley, P. and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics Acta Crystallogr. D60, 2126-2132
16. Adams, P. D., Afonine, P. V., Bunkoczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D66, 213-221
17. Chen, V. B., Arendall, W. B., III, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: All-atom structure validation for macromolecular crystallography Acta Crystallogr. D66, 12-21
18. Kelley, L. A. and Sternberg, M. J. (2009) Protein structure prediction on the Web: A case study using the Phyre server Nat. Protoc. 4, 363-371
19. Baker, N. A., Sept, D., Joseph, S., Holst, M. J., and McCammon, J. A. (2001) Electrostatics of nanosystems: Application to microtubules and the ribosome Proc. Natl. Acad. Sci. U.S.A. 98, 10037-10041
20. The PyMOL Molecular Graphics System, Version 1.5.0.4, Schrödinger, LLC.
21. Lee, C. H., Kominos, D., Jacques, S., Margolis, B., Schlessinger, J., Shoelson, S. E., and Kuriyan, J. (1994) Crystal structures of peptide complexes of the amino-terminal SH2 domain of the Syp tyrosine phosphatase Structure 2, 423-438
22. Pascal, S. M., Singer, A. U., Gish, G., Yamazaki, T., Shoelson, S. E., Pawson, T., Kay, L. E., and Forman-Kay, J. D. (1994) Nuclear magnetic resonance structure of an SH2 domain of phospholipase C-γ1 complexed with a high affinity binding peptide Cell 77, 461-472
23. Yu, J., Zhang, Y., McIlroy, J., Rordorf-Nikolic, T., Orr, G. A., and Backer, J. M. (1998) Regulation of the p85/p110 phosphatidylinositol 3′-kinase: Stabilization and inhibition of the p110α catalytic subunit by the p85 regulatory subunit Mol. Cell. Biol. 18, 1379-1387
24. Yu, J., Wjasow, C., and Backer, J. M. (1998) Regulation of the p85/p110α phosphatidylinositol 3′-kinase. Distinct roles for the N-terminal and C-terminal SH2 domains J. Biol. Chem. 273, 30199-30203
25. Vadas, O., Burke, J. E., Zhang, X., Berndt, A., and Williams, R. L. (2011) Structural basis for activation and inhibition of class I phosphoinositide 3-kinases Sci. Signaling 4, re2
26. Huang, C. H., Mandelker, D., Schmidt-Kittler, O., Samuels, Y., Velculescu, V. E., Kinzler, K. W., Vogelstein, B., Gabelli, S. B., and Amzel, L. M. (2007) The structure of a human p110α/p85α complex elucidates the effects of oncogenic PI3Kα mutations Science 318, 1744-1748
27. Mandelker, D., Gabelli, S. B., Schmidt-Kittler, O., Zhu, J., Cheong, I., Huang, C. H., Kinzler, K. W., Vogelstein, B., and Amzel, L. M. (2009) A frequent kinase domain mutation that changes the interaction between PI3Kα and the membrane Proc. Natl. Acad. Sci. U.S.A. 106, 16996-17001
28. Miled, N., Yan, Y., Hon, W. C., Perisic, O., Zvelebil, M., Inbar, Y., Schneidman-Duhovny, D., Wolfson, H. J., Backer, J. M., and Williams, R. L. (2007) Mechanism of two classes of cancer mutations in the phosphoinositide 3-kinase catalytic subunit Science 317, 239-242
29. Nolte, R. T., Eck, M. J., Schlessinger, J., Shoelson, S. E., and Harrison, S. C. (1996) Crystal structure of the PI 3-kinase p85 amino-terminal SH2 domain and its phosphopeptide complexes Nat. Struct. Biol. 3, 364-374
30. Backer, J. M., Myers, M. G., Jr., Shoelson, S. E., Chin, D. J., Sun, X. J., Miralpeix, M., Hu, P., Margolis, B., Skolnik, E. Y., and Schlessinger, J. (1992) Phosphatidylinositol 3′-kinase is activated by association with IRS-1 during insulin stimulation EMBO J. 11, 3469-3479
31. Carpenter, C. L., Auger, K. R., Chanudhuri, M., Yoakim, M., Schaffhausen, B., Shoelson, S., and Cantley, L. C. (1993) Phosphoinositide 3-kinase is activated by phosphopeptides that bind to the SH2 domains of the 85-kDa subunit J. Biol. Chem. 268, 9478-9483
32. Samuels, Y., Wang, Z., Bardelli, A., Silliman, N., Ptak, J., Szabo, S., Yan, H., Gazdar, A., Powell, S. M., Riggins, G. J., Willson, J. K., Markowitz, S., Kinzler, K. W., Vogelstein, B., and Velculescu, V. E. (2004) High frequency of mutations of the PIK3CA gene in human cancers Science 304, 554
33. Ikenoue, T., Kanai, F., Hikiba, Y., Obata, T., Tanaka, Y., Imamura, J., Ohta, M., Jazag, A., Guleng, B., Tateishi, K., Asaoka, Y., Matsumura, M., Kawabe, T., and Omata, M. (2005) Functional analysis of PIK3CA gene mutations in human colorectal cancer Cancer Res. 65, 4562-4567
34. Isakoff, S. J., Engelman, J. A., Irie, H. Y., Luo, J., Brachmann, S. M., Pearline, R. V., Cantley, L. C., and Brugge, J. S. (2005) Breast cancer-associated PIK3CA mutations are oncogenic in mammary epithelial cells Cancer Res. 65, 10992-11000
35. Kang, S., Bader, A. G., and Vogt, P. K. (2005) Phosphatidylinositol 3-kinase mutations identified in human cancer are oncogenic Proc. Natl. Acad. Sci. U.S.A. 102, 802-807
36. Ombrello, M. J., Remmers, E. F., Sun, G., Freeman, A. F., Datta, S., Torabi-Parizi, P., Subramanian, N., Bunney, T. D., Baxendale, R. W., Martins, M. S., Romberg, N., Komarow, H., Aksentijevich, I., Kim, H. S., Ho, J., Cruse, G., Jung, M. Y., Gilfillan, A. M., Metcalfe, D. D., Nelson, C., O'Brien, M., Wisch, L., Stone, K., Douek, D. C., Gandhi, C., Wanderer, A. A., Lee, H., Nelson, S. F., Shianna, K. V., Cirulli, E. T., Goldstein, D. B., Long, E. O., Moir, S., Meffre, E., Holland, S. M., Kastner, D. L., Katan, M., Hoffman, H. M., and Milner, J. D. (2012) Cold urticaria, immunodeficiency, and autoimmunity related to PLCG2 deletions N. Engl. J. Med. 366, 330-338
37. Zhou, Q., Lee, G. S., Brady, J., Datta, S., Katan, M., Sheikh, A., Martins, M. S., Bunney, T. D., Santich, B. H., Moir, S., Kuhns, D. B., Long Priel, D. A., Ombrello, A., Stone, D., Ombrello, M. J., Khan, J., Milner, J. D., Kastner, D. L., and Aksentijevich, I. (2012) A hypermorphic missense mutation in PLCG2, encoding phospholipase Cγ2, causes a dominantly inherited autoinflammatory disease with immunodeficiency Am. J. Hum. Genet. 91, 713-720
38. 2+ entry Immunity 22, 451-465
39. Everett, K. L., Bunney, T. D., Yoon, Y., Rodrigues-Lima, F., Harris, R., Driscoll, P. C., Abe, K., Fuchs, H., de Angelis, M. H., Yu, P., Cho, W., and Katan, M. (2009) Characterization of phospholipase Cγ enzymes with gain-of-function mutations J. Biol. Chem. 284, 23083-23093