Protein arginine deiminase 2 binds calcium in an ordered fashion: Implications for inhibitor design

ACS Chemical Biology

Volumn 10, Issue 4, 2015, Pages 1043-1053

  Slade, Daniel J ^a,f   Fang, Pengfei ^a   Dreyton, Christina J ^a,e   Zhang, Ying ^b   Fuhrmann, Jakob ^a   Rempel, Don ^b   Bax, Benjamin D ^c   Coonrod, Scott A ^d   Lewis, Huw D ^c   Guo, Min ^a   Gross, Michael L ^b   Thompson, Paul R ^a,e  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b WASHINGTON UNIVERSITY   (United States)

^c GLAXOSMITHKLINE   (United Kingdom)

^d Department of Molecular Biology and Genetics   (United States)

^e UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^f VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOPIPERIDINE; ARGININE; BENZIMIDAZOLE; CALCIUM ION; ENZYME INHIBITOR; HISTONE; PIPERIDINE DERIVATIVE; PROTEIN ARGININE DEIMINASE; PROTEIN ARGININE DEIMINASE 2; UNCLASSIFIED DRUG; BENZIMIDAZOLE DERIVATIVE; CALCIUM; CYSTEINE; GSK199; HYDROLASE; PROTEIN-ARGININE DEIMINASE;

ALLOSTERISM; ARTICLE; CALCIUM BINDING; CATALYSIS; CRYSTAL STRUCTURE; DEUTERIUM HYDROGEN EXCHANGE; ELECTROSPRAY MASS SPECTROMETRY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME KINETICS; MOLECULAR DOCKING; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEADY STATE; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY; AMINO ACID SEQUENCE; ANTAGONISTS AND INHIBITORS; CHEMISTRY; ENZYME ACTIVATION; ENZYME ACTIVE SITE; HUMAN; METABOLISM; MOLECULAR GENETICS; PROTEIN CONFORMATION;

AMINO ACID SEQUENCE; BENZIMIDAZOLES; CALCIUM; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; CYSTEINE; DEUTERIUM EXCHANGE MEASUREMENT; ENZYME ACTIVATION; ENZYME INHIBITORS; HUMANS; HYDROLASES; MOLECULAR DOCKING SIMULATION; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION;

EID: 84928157473     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb500933j     Document Type: Article

References (40)

1. Jones, J. E., Causey, C. P., Knuckley, B., Slack-Noyes, J. L., and Thompson, P. R. (2009) Protein arginine deiminase 4 (PAD4): Current understanding and future therapeutic potential Curr. Opin. Drug Discovery Dev. 12, 616-627
2. Vossenaar, E. R., Zendman, A. J., van Venrooij, W. J., and Pruijn, G. J. (2003) PAD, a growing family of citrullinating enzymes: genes, features and involvement in disease Bioessays 25, 1106-18
3. Christophorou, M. A., Castelo-Branco, G., Halley-Stott, R. P., Oliveira, C. S., Loos, R., Radzisheuskaya, A., Mowen, K. A., Bertone, P., Silva, J. C., Zernicka-Goetz, M., Nielsen, M. L., Gurdon, J. B., and Kouzarides, T. (2014) Citrullination regulates pluripotency and histone H1 binding to chromatin Nature 507, 104-8
4. Slade, D. J., Subramanian, V., and Thompson, P. R. (2014) Citrullination unravels stem cells Nat. Chem. Biol. 10, 327-328
5. Arita, K., Hashimoto, H., Shimizu, T., Nakashima, K., Yamada, M., and Sato, M. (2004) Structural basis for Ca(2+)-induced activation of human PAD4 Nat. Struct Mol. Biol. 11, 777-83
6. Dwivedi, N., Neeli, I., Schall, N., Wan, H., Desiderio, D. M., Csernok, E., Thompson, P. R., Dali, H., Briand, J. P., Muller, S., and Radic, M. (2014) Deimination of linker histones links neutrophil extracellular trap release with autoantibodies in systemic autoimmunity FASEB J. 28, 2840-2851
7. Moscarello, M. A., Pritzker, L., Mastronardi, F. G., and Wood, D. D. (2002) Peptidylarginine deiminase: a candidate factor in demyelinating disease J. Neurochem 81, 335-43
8. Zhang, X., Bolt, M., Guertin, M. J., Chen, W., Zhang, S., Cherrington, B. D., Slade, D. J., Dreyton, C. J., Subramanian, V., Bicker, K. L., Thompson, P. R., Mancini, M. A., Lis, J. T., and Coonrod, S. A. (2012) Peptidylarginine deiminase 2-catalyzed histone H3 arginine 26 citrullination facilitates estrogen receptor alpha target gene activation Proc. Natl. Acad. Sci. U. S. A. 109, 13331-6
9. Stadler, S. C., Vincent, C. T., Fedorov, V. D., Patsialou, A., Cherrington, B. D., Wakshlag, J. J., Mohanan, S., Zee, B. M., Zhang, X., Garcia, B. A., Condeelis, J. S., Brown, A. M., Coonrod, S. A., and Allis, C. D. (2013) Dysregulation of PAD4-mediated citrullination of nuclear GSK3beta activates TGF-beta signaling and induces epithelial-to-mesenchymal transition in breast cancer cells Proc. Natl. Acad. Sci. U. S. A. 110, 11851-6
10. Schellekens, G. A., de Jong, B. A., van den Hoogen, F. H., van de Putte, L. B., and van Venrooij, W. J. (1998) Citrulline is an essential constituent of antigenic determinants recognized by rheumatoid arthritis-specific autoantibodies J. Clin. Invest. 101, 273-81
11. Wang, Y., Li, M., Stadler, S., Correll, S., Li, P., Wang, D., Hayama, R., Leonelli, L., Han, H., Grigoryev, S. A., Allis, C. D., and Coonrod, S. A. (2009) Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation J. Cell Biol. 184, 205-213
12. Mohanan, S., Horibata, S., McElwee, J. L., Dannenberg, A. J., and Coonrod, S. A. (2013) Identification of macrophage extracellular trap-like structures in mammary gland adipose tissue: a preliminary study Front. Immunol. 4, 67
13. Bicker, K. L. and Thompson, P. R. (2013) The protein arginine deiminases: Structure, function, inhibition, and disease Biopolymers 99, 155-63
14. Chumanevich, A. A., Causey, C. P., Knuckley, B. A., Jones, J. E., Poudyal, D., Chumanevich, A. P., Davis, T., Matesic, L. E., Thompson, P. R., and Hofseth, L. J. (2011) Suppression of colitis in mice by Cl-amidine: a novel peptidylarginine deiminase inhibitor Am. J. Physiol. Gastrointest. Liver Physiol. 300, G929-38
15. Knight, J. S., Zhao, W., Luo, W., Subramanian, V., ODell, A. A., Yalavarthi, S., Hodgin, J. B., Eitzman, D. T., Thompson, P. R., and Kaplan, M. J. (2013) Peptidylarginine deiminase inhibition is immunomodulatory and vasculoprotective in murine lupus J. Clin. Invest. 123, 2981-93
16. Lange, S., Gogel, S., Leung, K. Y., Vernay, B., Nicholas, A. P., Causey, C. P., Thompson, P. R., Greene, N. D., and Ferretti, P. (2011) Protein deiminases: New players in the developmentally regulated loss of neural regenerative ability Dev. Biol. 355, 205-14
17. McElwee, J. L., Mohanan, S., Griffith, O. L., Breuer, H. C., Anguish, L. J., Cherrington, B. D., Palmer, A. M., Howe, L. R., Subramanian, V., Causey, C. P., Thompson, P. R., Gray, J. W., and Coonrod, S. A. (2012) Identification of PADI2 as a potential breast cancer biomarker and therapeutic target BMC Cancer 12, 500
18. Willis, V. C., Gizinski, A. M., Banda, N. K., Causey, C. P., Knuckley, B., Cordova, K. N., Luo, Y., Levitt, B., Glogowska, M., Chandra, P., Kulik, L., Robinson, W. H., Arend, W. P., Thompson, P. R., and Holers, V. M. (2011) N-alpha-benzoyl-N5-(2-chloro-1-iminoethyl)-L-ornithine amide, a protein arginine deiminase inhibitor, reduces the severity of murine collagen-induced arthritis J. Immunol. 186, 4396-404
19. Knight, J. S., Luo, W., ODell, A. A., Yalavarthi, S., Zhao, W., Subramanian, V., Guo, C., Grenn, R. C., Thompson, P. R., Eitzman, D. T., and Kaplan, M. J. (2014) Peptidylarginine deiminase inhibition reduces vascular damage and modulates innate immune responses in murine models of atherosclerosis Circ. Res. 114, 947-56
20. Knight, J. S., Subramanian, V., ODell, A. A., Yalavarthi, S., Zhao, W., Smith, C. K., Hodgin, J. B., Thompson, P. R., and Kaplan, M. J. (2014) Peptidylarginine deiminase inhibition disrupts NET formation and protects against kidney, skin and vascular disease in lupus-prone MRL/lpr mice Ann. Rheum Dis. 10.1136/annrheumdis-2014-205365
21. Symmans, W. F., Hatzis, C., Sotiriou, C., Andre, F., Peintinger, F., Regitnig, P., Daxenbichler, G., Desmedt, C., Domont, J., Marth, C., Delaloge, S., Bauernhofer, T., Valero, V., Booser, D. J., Hortobagyi, G. N., and Pusztai, L. (2010) Genomic index of sensitivity to endocrine therapy for breast cancer J. Clin Oncol 28, 4111-9
22. Bertucci, F., Borie, N., Ginestier, C., Groulet, A., Charafe-Jauffret, E., Adelaide, J., Geneix, J., Bachelart, L., Finetti, P., Koki, A., Hermitte, F., Hassoun, J., Debono, S., Viens, P., Fert, V., Jacquemier, J., and Birnbaum, D. (2004) Identification and validation of an ERBB2 gene expression signature in breast cancers Oncogene 23, 2564-75
23. Lewis, H. D., Liddle, J., Coote, J. E., Atkinson, S. J., Barker, M. D., Bax, B. D., Bicker, K. L., Bingham, R. P., Campbell, M., Chen, Y. H., Chung, C.-W., Craggs, P. D., Davis, R. P., Eberhard, D., Joberty, G., Lind, K. E., Locke, K., Maller, C., Martinod, K., Patten, C., Polyakova, O., Rise, C. E., Rudiger, M., Sheppard, R. J., Slade, D. J., Thomas, P., Thorpe, J., Yao, G., Drewes, G., Wagner, D. D., Thompson, P. R., Prinjha, R. K., and Wilson, D. M. (2015) Inhibition of PAD4 activity is sufficient to disrupt mouse and human NET formation Nat. Chem. Biol. 10.1038/nchembio.1735
24. Zheng, H., Chruszcz, M., Lasota, P., Lebioda, L., and Minor, W. (2008) Data mining of metal ion environments present in protein structures J. Inorg. Biochem. 102, 1765-76
25. Youn, H. D., Sun, L., Prywes, R., and Liu, J. O. (1999) Apoptosis of T cells mediated by Ca2+-induced release of the transcription factor MEF2 Science 286, 790-793
26. Darrah, E., Giles, J. T., Ols, M. L., Bull, H. G., Andrade, F., and Rosen, A. (2013) Erosive Rheumatoid Arthritis Is Associated with Antibodies That Activate PAD4 by Increasing Calcium Sensitivity Sci. Transl. Med. 5, 186ra65
27. Llinas, R., Sugimori, M., and Silver, R. B. (1992) Microdomains of high calcium concentration in a presynaptic terminal Science 256, 677-9
28. Tour, O., Adams, S. R., Kerr, R. A., Meijer, R. M., Sejnowski, T. J., Tsien, R. W., and Tsien, R. Y. (2007) Calcium Green FlAsH as a genetically targeted small-molecule calcium indicator Nat. Chem. Biol. 3, 423-31
29. Otwinowski, Z. M. W. (1997) Processing of X-ray Diffraction Data Collected in Oscillation Mode Methods Enzymol. 276, 307-326
30. 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., Sect. D: Biol. Crystallogr. 66, 213-21
31. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 2126-32
32. Harding, M. M. (2000) The geometry of metal-ligand interactions relevant to proteins. II. Angles at the metal atom, additional weak metal-donor interactions Acta Crystallogr., Sect. D: Biol. Crystallogr. 56, 857-67
33. Menard, H. A., Lapointe, E., Rochdi, M. D., and Zhou, Z. J. (2000) Insights into rheumatoid arthritis derived from the Sa immune system Arthritis Res. 2, 429-432
34. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera - a visualization system for exploratory research and analysis J. Comput. Chem. 25, 1605-12
35. Laskowski, R. A. and Swindells, M. B. (2011) LigPlot+: multiple ligand-protein interaction diagrams for drug discovery J. Chem. Inf. Model. 51, 2778-86
36. Kearney, P. L., Bhatia, M., Jones, N. G., Yuan, L., Glascock, M. C., Catchings, K. L., Yamada, M., and Thompson, P. R. (2005) Kinetic characterization of protein arginine deiminase 4: a transcriptional corepressor implicated in the onset and progression of rheumatoid arthritis Biochemistry 44, 10570-82
37. Knipp, M. and Vasak, M. (2000) A colorimetric 96-well microtiter plate assay for the determination of enzymatically formed citrulline Anal. Biochem. 286, 257-64
38. Leatherbarrow, R. J. Grafit, version 5; Erithacus Software Ltd.: Horley, U.K., 2001.
39. Zhang, H., Cui, W., Wen, J., Blankenship, R. E., and Gross, M. L. (2011) Native electrospray and electron-capture dissociation FTICR mass spectrometry for top-down studies of protein assemblies Anal. Chem. 83, 5598-606
40. Morris, G. M., Huey, R., Lindstrom, W., Sanner, M. F., Belew, R. K., Goodsell, D. S., and Olson, A. J. (2009) AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility J. Comput. Chem. 30, 2785-2791