Suppression of colitis in mice by Cl-amidine: A novel peptidylarginine deiminase inhibitor

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 300, Issue 6, 2011, Pages

  Chumanevich, Alexander A ^a   Causey, Corey P ^a   Knuckley, Bryan A ^a,b   Jones, Justin E ^a,b   Poudyal, Deepak ^a   Chumanevich, Alena P ^a   Davis, Tia ^a   Matesic, Lydia E ^a   Thompson, Paul R ^a,b   Hofseth, Lorne J ^a  

^a UNIVERSITY OF SOUTH CAROLINA   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Apoptosis; Citrullination; Inflammation

Indexed keywords

ANTIINFLAMMATORY AGENT; CHLORAMIDINE; CYTOKINE; DEXTRAN SULFATE; PROTEIN ARGININE DEIMINASE; UNCLASSIFIED DRUG;

ABSENCE OF SIDE EFFECTS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; COLITIS; CONTROLLED STUDY; ENZYME BLOOD LEVEL; HUMAN; HUMAN TISSUE; HYPOTHESIS; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATORY CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ADMINISTRATION, ORAL; ANIMALS; ANTI-INFLAMMATORY AGENTS; APOPTOSIS; ARGININE; CITRULLINE; COLITIS; COLON; DEXTRAN SULFATE; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; GASTROINTESTINAL AGENTS; HT29 CELLS; HUMANS; HYDROLASES; MICE; MICE, INBRED C57BL; ORNITHINE; PROTEIN PROCESSING, POST-TRANSLATIONAL; UP-REGULATION;

EID: 79957951714     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00435.2010     Document Type: Article

References (41)

1. Causey CP, Thompson PR. An improved synthesis of haloaceteamidinebased inactivators of protein arginine deiminase 4 (PAD4). Tetrahedron Lett 49: 4383-4385, 2008.
2. Chang X, Han J. Expression of peptidylarginine deiminase type 4 (PAD4) in various tumors. Mol Carcinog 45: 183-196, 2006.
3. Chang X, Han J, Pang L, Zhao Y, Yang Y, Shen Z. Increased PADI4 expression in blood and tissues of patients with malignant tumors. BMC Cancer 9: 40, 2009.
4. Chen CC, Isomoto H, Narumi Y, Sato K, Oishi Y, Kobayashi T, Yanagihara K, Mizuta Y, Kohno S, Tsukamoto K. Haplotypes of PADI4 susceptible to rheumatoid arthritis are also associated with ulcerative colitis in the Japanese population. Clin Immunol 126: 165-171, 2008.
5. Cui X, Jin Y, Hofseth AB, Pena E, Habiger J, Chumanevich A, Poudyal D, Nagarkatti M, Nagarkatti PS, Singh UP, Hofseth LJ. Resveratrol suppresses colitis and colon cancer associated with colitis. Cancer Prev Res 3: 549-559, 2010.
6. De Rycke L, Peene I, Hoffman IE, Kruithof E, Union A, Meheus L, Lebeer K, Wyns B, Vincent C, Mielants H, Boullart L, Serre G, Veys EM, De Keyser F. Rheumatoid factor and anticitrullinated protein antibodies in rheumatoid arthritis: diagnostic value, associations with radiological progression rate, and extra-articular manifestations. Ann Rheum Dis 63: 1587-1593, 2004.
7. Denkert C, Koch I, von Keyserlingk N, Noske A, Niesporek S, Dietel M, Weichert W. Expression of the ELAV-like protein HuR in human colon cancer: association with tumor stage and cyclooxygenase-2. Mod Pathol 19: 1261-1269, 2006.
8. Foulquier C, Sebbag M, Clavel C, Chapuy-Regaud S, Al Badine R, Mechin MC, Vincent C, Nachat R, Yamada M, Takahara H, Simon M, Guerrin M, Serre G. Peptidyl arginine deiminase type 2 (PAD-2) and PAD-4 but not PAD-1, PAD-3, and PAD-6 are expressed in rheumatoid arthritis synovium in close association with tissue inflammation. Arthritis Rheum 56: 3541-3553, 2007.
9. Ishigami A, Ohsawa T, Hiratsuka M, Taguchi H, Kobayashi S, Saito Y, Murayama S, Asaga H, Toda T, Kimura N, Maruyama N. Abnormal accumulation of citrullinated proteins catalyzed by peptidylarginine deiminase in hippocampal extracts from patients with Alzheimer's disease. J Neurosci Res 80: 120-128, 2005.
10. Jin Y, Hofseth AB, Cui X, Windust AJ, Poudyal D, Chumanevich AA, Matesic LE, Singh NP, Nagarkatti M, Nagarkatti PS, Hofseth LJ. American ginseng suppresses colitis through p53-mediated apoptosis of inflammatory cells. Cancer Prev Res 3: 339-347, 2010.
11. Jin Y, Kotakadi VS, Ying L, Hofseth AB, Cui X, Wood PA, Windust A, Matesic LE, Pena EA, Chiuzan C, Singh NP, Nagarkatti M, Nagarkatti PS, Wargovich MJ, Hofseth LJ. American ginseng suppresses inflammation and DNA damage associated with mouse colitis. Carcinogenesis 29: 2351-2359, 2008.
12. Jones JE, Causey CP, Knuckley B, Slack-Noyes JL, Thompson PR. Protein arginine deiminase 4 (PAD4): current understanding and future therapeutic potential. Curr Opin Drug Discov Dev 12: 616-627, 2009.
13. Kearney PL, Bhatia M, Jones NG, Yuan L, Glascock MC, Catchings KL, Yamada M, Thompson PR. Kinetic characterization of protein arginine deiminase 4: a transcriptional corepressor implicated in the onset and progression of rheumatoid arthritis. Biochemistry 44: 10570-10582, 2005.
14. Knipp M, Vasak M. A colorimetric 96-well microtiter plate assay for the determination of enzymatically formed citrulline. Anal Biochem 286: 257-264, 2000.
15. Kotakadi VS, Jin Y, Hofseth AB, Ying L, Cui X, Volate S, Chumanevich A, Wood PA, Price RL, McNeal A, Singh UP, Singh NP, Nagarkatti M, Nagarkatti PS, Matesic LE, Auclair K, Wargovich MJ, Hofseth LJ. Ginkgo biloba extract EGb 761 has anti-inflammatory properties and ameliorates colitis in mice by driving effector T cell apoptosis. Carcinogenesis 29: 1799-1806, 2008.
16. Krieglstein CF, Cerwinka WH, Laroux FS, Grisham MB, Schurmann G, Bruwer M, Granger DN. Role of appendix and spleen in experimental colitis. J Surg Res 101: 166-175, 2001.
17. Kunckley B, Causey CP, Pellechia PJ, Cook PF, Thompson PR. Haloacetamidine-based inactivators of protein arginine deiminase 4 (PAD4): evidence that general acid catalysis promotes efficient inactivation. Chembiochem 11: 11, 2009.
18. Li P, Yao H, Zhang Z, Li M, Luo Y, Thompson PR, Gilmour DS, Wang Y. Regulation of p53 target gene expression by peptidylarginine deiminase 4. Mol Cell Biol 28: 4745-4758, 2008.
19. Lichtenstein GR, Abreu MT, Cohen R, Tremaine W. American Gastroenterological Association Institute technical review on corticosteroids, immunomodulators, and infliximab in inflammatory bowel disease. Gastroenterology 130: 940-987, 2006.
20. Lopez-Longo FJ, Sanchez-Ramon S, Carreno L. The value of anticyclic citrullinated peptide antibodies in rheumatoid arthritis: do they imply new risk factors? Drug News Perspect 22: 543-548, 2009.
21. Luo Y, Arita K, Bhatia M, Knuckley B, Lee YH, Stallcup MR, Sato M, Thompson PR. Inhibitors and inactivators of protein arginine deiminase 4: functional and structural characterization. Biochemistry 45: 11727- 11736, 2006.
22. Maines LW, Fitzpatrick LR, French KJ, Zhuang Y, Xia Z, Keller SN, Upson JJ, Smith CD. Suppression of ulcerative colitis in mice by orally available inhibitors of sphingosine kinase. Dig Dis Sci 53: 997-1012, 2008.
23. Makrygiannakis D, af Klint E, Lundberg IE, Lofberg R, Ulfgren AK, Klareskog L, Catrina AI. Citrullination is an inflammation-dependent process. Ann Rheum Dis 65: 1219-1222, 2006.
24. Mastronardi FG, Wood DD, Mei J, Raijmakers R, Tseveleki V, Dosch HM, Probert L, Casaccia-Bonnefil P, Moscarello MA. Increased citrullination of histone H3 in multiple sclerosis brain and animal models of demyelination: a role for tumor necrosis factor-induced peptidylarginine deiminase 4 translocation. J Neurosci 26: 11387-11396, 2006.
25. Moscarello MA, Mastronardi FG, Wood DD. The role of citrullinated proteins suggests a novel mechanism in the pathogenesis of multiple sclerosis. Neurochem Res 32: 251-256, 2007.
26. Moscarello MA, Pritzker L, Mastronardi FG, Wood DD. Peptidylarginine deiminase: a candidate factor in demyelinating disease. J Neurochem 81: 335-343, 2002.
27. Neuman MG. Immune dysfunction in inflammatory bowel disease. Transl Res 149: 173-186, 2007.
28. Nikfar S, Rahimi R, Rezaie A, Abdollahi M. A meta-analysis of the efficacy of sulfasalazine in comparison with 5-aminosalicylates in the induction of improvement and maintenance of remission in patients with ulcerative colitis. Dig Dis Sci 54: 1157-1170, 2009.
29. Reagan-Shaw S, Nihal M, Ahmad N. Dose translation from animal to human studies revisited. FASEB J 17: 659-661, 2007.
30. Sartor RB. Mechanisms of disease: pathogenesis of Crohn's disease and ulcerative colitis. Nat Clin Pract Gastroenterol Hepatol 3: 390-407, 2006.
31. Satoh K, Kawakami A, Shirabe S, Tamai M, Sato A, Tsujihata M, Nagasato K, Eguchi K. Anti-cyclic citrullinated peptide antibody (anti- CCP antibody) is present in the sera of patients with dementia of Alzheimer's type in Asian. Acta Neurol Scand 30: 338-341, 2009.
32. Shepela C. The safety of biologic agents in the treatment of inflammatory bowel disease. Minn Med 91: 42-45, 2008.
33. Siegel CA, Marden SM, Persing SM, Larson RJ, Sands BE. Risk of lymphoma associated with combination anti-tumor necrosis factor and immunomodulator therapy for the treatment of Crohn's disease: a metaanalysis. Clin Gastroenterol Hepatol 7: 874-881, 2009.
34. Skopek TR, Liber HL, Penman BW, Thilly WG. Isolation of a human lymphoblastoid line heterozygous at the thymidine kinase locus: possibility for a rapid human cell mutation assay. Biochem Biophys Res Commun 84: 411-416, 1978.
35. Snider AJ, Kawamori T, Bradshaw SG, Orr KA, Gilkeson GS, Hannun YA, Obeid LM. A role for sphingosine kinase 1 in dextran sulfate sodium-induced colitis. FASEB J 23: 143-152, 2009.
36. Struyf S, Noppen S, Loos T, Mortier A, Gouwy M, Verbeke H, Huskens D, Luangsay S, Parmentier M, Geboes K, Schols D, Van Damme J, Proost P. Citrullination of CXCL12 differentially reduces CXCR4 and CXCR7 binding with loss of inflammatory and anti-HIV-1 activity via CXCR4. J Immunol 182: 666-674, 2009.
37. Szodoray P, Szabo Z, Kapitany A, Gyetvai A, Lakos G, Szanto S, Szucs G, Szekanecz Z. Anti-citrullinated protein/peptide autoantibodies in association with genetic and environmental factors as indicators of disease outcome in rheumatoid arthritis. Autoimmun Rev 7: 140-143, 2009.
38. van Schaardenburg D, Dijkmans BA. Clinical approaches to early inflammatory arthritis. Nat Rev Rheumatol 5: 627-633, 2009.
39. Whiting PF, Smidt N, Sterne JA, Harbord R, Burton A, Burke M, Beynon R, Ben-Shlomo Y, Axford J, Dieppe P. Systematic review: accuracy of anti-citrullinated peptide antibodies for diagnosing rheumatoid arthritis. Ann Intern Med 152: W155-W466, 2010.
40. Yamada R, Suzuki A, Chang X, Yamamoto K. Peptidylarginine deiminase type 4: identification of a rheumatoid arthritis-susceptible gene. Trends Mol Med 9: 503-508, 2003.
41. Ying L, Hofseth AB, Browning DD, Nagarkatti M, Nagarkatti PS, Hofseth LJ. Nitric oxide inactivates the retinoblastoma pathway in chronic inflammation. Cancer Res 67: 9286-9293, 2007.