Citrullination – small change with a great consequence

Authors

  • Mariusz Gogól Jagiellonian University, Faculty of Biochemistry, Biophysics and Biotechnology, Department of Analytical Biochemistry

DOI:

https://doi.org/10.2478/fobio-2013-0003

Keywords:

deimination, peptidylarginine deiminase, citrulline, post-translational modification

Abstract

Citrullination is one of the possible post-translational modifications of proteins. It is based on a conversion of L-arginine residue (L-Arg) to L-citrulline residue (L-Cit). The reaction is catalyzed by peptidylarginine deiminases (PAD). The change of L-Arg imino moiety results in a loss of a positive charge. This slight modification can contribute to significant changes in physicochemical properties of proteins, which may also cause a change of their functions. Citrullination is the modification observed in physiological processes such as epidermal keratinization, regulation of gene expression and the reorganization of myelin sheaths. The changes in the efficacy of citrullination may contribute to the pathogenesis of many different diseases including: psoriasis, multiple sclerosis, rheumatoid arthritis and cancer.

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References

Arita, K., Hashimoto, H., Shimizu, T. et al. 2004. Structural basis for Ca(2+)-induced activation of human PAD4. Nature structural & molecular biology, 11: 777–783. http://dx.doi.org/10.1038/nsmb799
Google Scholar

Asaga, H., Yamada, M. & Senshu, T. 1998. Selective deimination of vimentin in calcium ionophoreinduced apoptosis of mouse peritoneal macrophages. Biochemical and biophysical research communications, 243: 641–646. http://dx.doi.org/10.1006/bbrc.1998.8148
Google Scholar

Beniac, D.R., Wood, D.D., Palaniyar, N. et al. 2000. Cryoelectron microscopy of protein-lipid complexes of human myelin basic protein charge isomers differing in degree of citrullination. Journal of structural biology, 129: 80–95. http://dx.doi.org/10.1006/jsbi.1999.4200
Google Scholar

Berlet, H.H. 1987. Cation-dependent extraction of basic protein from isolated human myelin. Independence of endogenous acid proteolysis. Neurochemical pathology, 7: 263–274.
Google Scholar

Blombäck, B., Hessel, B., Hogg, D. & Therkildsen, L. 1978. A two-step fibrinogen--fibrin transition in blood coagulation. Nature, 275: 501–505.
Google Scholar

Boggs, J.M., Rangaraj, G., Koshy, K.M. et al. 1999. Highly deiminated isoform of myelin basic protein from multiple sclerosis brain causes fragmentation of lipid vesicles. Journal of neuroscience research, 57: 529–535.
Google Scholar

Cao, L., Goodin, R., Wood, D., et al. 1999. Rapid release and unusual stability of immunodominant peptide, 45–89 from citrullinated myelin basic protein. Biochemistry, 38: 6157–6163. http://dx.doi.org/10.1021/bi982960s
Google Scholar

Chang, X., Hou, X., Pan, J. et al. 2011. Investigating the pathogenic role of PADI4 in oesophageal cancer. International journal of biological sciences, 7: 769–781.
Google Scholar

Chang, X., Yamada, R., Suzuki, A. et al. 2005. Citrullination of fibronectin in rheumatoid arthritis synovial tissue. Rheumatology (Oxford, England), 44: 1374–1382. http://dx.doi.org/10.1093/rheumatology/kei023
Google Scholar

Chavanas, S., Méchin, M-C., Nachat, R. et al. 2006. Peptidylarginine deiminases and deimination in biology and pathology: relevance to skin homeostasis. Journal of dermatological science, 44: 63–72. http://dx.doi.org/10.1016/j.jdermsci.2006.07.004
Google Scholar

Cherrington, B.D., Morency, E., Struble, A.M. et al. 2010. Potential role for peptidylarginine deiminase 2 (PAD2) in citrullination of canine mammary epithelial cell histones. PloS one, 5: e11768. http://dx.doi.org/10.1371/journal.pone.0011768
Google Scholar

Cherrington, B.D., Zhang, X., McElwee, J.L. et al. 2012. Potential role for PAD2 in gene regulation in breast cancer cells. PloS one, 7: e41242. http://dx.doi.org/10.1371/journal.pone.0041242
Google Scholar

Curis, E., Nicolis, I., Moinard, C., et al. 2005. Almost all about citrulline in mammals. Amino acids, 29: 177–205. http://dx.doi.org/10.1007/s00726-005-0235-4
Google Scholar

Ferreiro, E., Resende, R., Costa, R. et al. 2006. An endoplasmic-reticulum-specific apoptotic pathway is involved in prion and amyloid-beta peptides neurotoxicity. Neurobiology of disease 23: 669–678. http://dx.doi.org/10.1016/j.nbd.2006.05.011
Google Scholar

Firestein, G.S. 2003. Evolving concepts of rheumatoid arthritis. Nature, 423: 356–361. http://dx.doi.org/10.1038/nature01661
Google Scholar

Furie, B. & Furie, B.C. 1988. The molecular basis of blood coagulation. Cell, 53: 505–518.
Google Scholar

György, B., Tóth, E., Tarcsa, E. et al. 2006. Citrullination: a posttranslational modification in health and disease. The international journal of biochemistry & cell biology, 38: 1662–1677. http://dx.doi.org/10.1016/j.biocel.2006.03.008
Google Scholar

Hagiwara, T., Hidaka, Y. & Yamada, M. 2005. Deimination of histone H2A and H4 at arginine 3 in HL-60 granulocytes. Biochemistry, 44: 5827–5834. http://dx.doi.org/10.1021/bi047505c
Google Scholar

Harding, C.R. & Scott, I.R. 1983. Histidine-rich proteins (filaggrins): structural and functional heterogeneity during epidermal differentiation. Journal of molecular biology, 170: 651–673.
Google Scholar

Ishida-Yamamoto, A., Senshu, T., Takahashi, H. et al. 2000. Decreased deiminated keratin K1 in psoriatic hyperproliferative epidermis. The Journal of investigative dermatology, 114: 701–705. http://dx.doi.org/10.1046/j.1523-1747.2000.00936.x
Google Scholar

Jang, B., Kim, E., Choi, J-K. et al. 2008. Accumulation of citrullinated proteins by up-regulated peptidylarginine deiminase 2 in brains of scrapieinfected mice: a possible role in pathogenesis. The American journal of pathology, 173: 1129–1142. http://dx.doi.org/10.2353/ajpath.2008.080388
Google Scholar

Karlić, R., Chung, H-R., Lasserre, J., et al. 2010. Histone modification levels are predictive for gene expression. Proceedings of the National Academy of Sciences of the United States of America, 107: 2926–2931. http://dx.doi.org/10.1073/pnas.0909344107
Google Scholar

Kubilus, J. & Badenm, H.P. 1983. Purification and properties of a brain enzyme which deiminates proteins. Biochimica et biophysica acta, 745: 285–291.
Google Scholar

Kursula, P. 2008. Structural properties of proteins specific to the myelin sheath. Amino acids, 34: 175–185. http://dx.doi.org/10.1007/s00726-006-0479-7
Google Scholar

Lee, S.C., Kim, I.G., Marekov, L.N. et al. 1993. The structure of human trichohyalin. Potential multiple roles as a functional EF-hand-like calcium-binding protein, a cornified cell envelope precursor, and an intermediate filament-associated (cross-linking) protein. The Journal of biological chemistry, 268: 12164–12176.
Google Scholar

Masson-Bessière, C., Sebbag, M., Girbal-Neuhauser, E. et al. 2001. The major synovial targets of the rheumatoid arthritis-specific antifilaggrin autoantibodies are deiminated forms of the alphaand beta-chains of fibrin. Journal of immunology (Baltimore, Md : 1950), 166: 4177–4184.
Google Scholar

Mastronardi, F.G., Wood, D.D., Mei, J. et al. 2006. 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. The Journal of neuroscience: the official journal of the Society for Neuroscience, 26: 11387–1396. http://dx.doi.org/10.1523/JNEUROSCI.3349-06.2006
Google Scholar

Mohanan, S., Cherrington, B.D., Horibata, S. et al. 2012. Potential role of peptidylarginine deiminase enzymes and protein citrullination in cancer pathogenesis. Biochemistry research international, 2012: 1–11. http://dx.doi.org/10.1155/2012/895343
Google Scholar

Moscarello, M. A., Pritzker, L., Mastronardi, F.G. & Wood, D.D. 2002. Peptidylarginine deiminase: a candidate factor in demyelinating disease. Journal of neurochemistry, 81: 335–343.
Google Scholar

Moscarello, M a, Wood, D.D., Ackerley, C. & Boulias, C. 1994. Myelin in multiple sclerosis is developmentally immature. The Journal of clinical investigation, 94: 146–154. http://dx.doi.org/10.1172/JCI117300
Google Scholar

Méchin, M-C., Sebbag, M., Arnaud, J. et al. 2007. Update on peptidylarginine deiminases and deimination in skin physiology and severe human diseases. International journal of cosmetic science, 29: 147–168. http://dx.doi.org/10.1111/j.1467-2494.2007.00377.x
Google Scholar

Nachat, R., Méchin, M-C., Takahara, H. et al. 2005. Peptidylarginine deiminase isoforms 1-3 are expressed in the epidermis and involved in the deimination of K1 and filaggrin. The Journal of investigative dermatology, 124: 384–93. http://dx.doi.org/10.1111/j.0022-202X.2004.23568.x
Google Scholar

Nakayama-Hamada, M., Suzuki, A., Furukawa, H. et al. 2008. Citrullinated fibrinogen inhibits thrombincatalysed fibrin polymerization. Journal of biochemistry, 144: 393–398. http://dx.doi.org/10.1093/jb/mvn079
Google Scholar

Okumura, N., Haneishi, A. & Terasawa, F. 2009. Citrullinated fibrinogen shows defects in FPA and FPB release and fibrin polymerization catalyzed by thrombin. Clinica chimica acta; international journal of clinical chemistry 401: 119–123. http://dx.doi.org/10.1016/j.cca.2008.12.002
Google Scholar

O’Donovan, C.N., Tobin, D. & Cotter, T.G. 2001. Prion protein fragment PrP-(106-126) induces apoptosis via mitochondrial disruption in human neuronal SH-SY5Y cells. The Journal of biological chemistry, 276: 43516–43523. http://dx.doi.org/10.1074/jbc.M103894200
Google Scholar

Pearton, D.J., Dale, B.A. & Presland, R.B. 2002. Functional Analysis of the Pro®laggrin N-Terminal Peptide: Identi®cation of Domains that Regulate Nuclear and Cytoplasmic Distribution. 661–669.
Google Scholar

Pritzker, L.B., Joshi, S., Harauz, G. & Moscarello, M.A. 2000. Deimination of myelin basic protein. 2. Effect of methylation of MBP on its deimination by peptidylarginine deiminase. Biochemistry, 39: 5382–5388.
Google Scholar

Rodenburg, R.J., Ganga, A., Van Lent, P.L. et al. 2000. The antiinflammatory drug sulfasalazine inhibits tumor necrosis factor alpha expression in macrophages by inducing apoptosis. Arthritis and rheumatism, 43: 1941–1950. http://dx.doi.org/10.1002/1529-0131(200009)43:9<1941::AID-ANR4>3.0.CO;2-O
Google Scholar

Rodríguez, S.B., Stitt, B.L. & Ash, D.E. 2010. Cysteine 351 is an essential nucleophile in catalysis by Porphyromonas gingivalis peptidylarginine deiminase. Archives of biochemistry and biophysics, 504: 190–196. http://dx.doi.org/10.1016/j.abb.2010.09.008
Google Scholar

Rubin, B. & Sønderstrup, G. 2004. Citrullination of self-proteins and autoimmunity. Scandinavian journal of immunology, 60: 112–120. http://dx.doi.org/10.1111/j.0300-9475.2004.01457.x
Google Scholar

Sebbag, M., Chapuy-Regaud, S., Auger, I. et al. 2004. Clinical and pathophysiological significance of the autoimmune response to citrullinated proteins in rheumatoid arthritis. Joint, bone, spine: revue du rhumatisme, 71: 493–502. http://dx.doi.org/10.1016/j.jbspin.2004.07.004
Google Scholar

Senshu, T., Akiyama, K. & Nomura, K. 1999. Identification of citrulline residues in the V subdomains of keratin K1 derived from the cornified layer of newborn mouse epidermis. Experimental dermatology, 8: 392–401.
Google Scholar

Senshu, T., Kan, S., Ogawa, H. et al. 1996. Preferential Deimination of Keratin K1 and Filaggrin during the Terminal Differentiation of Human Epidermis The process of normal epidermal differentiation is characterized by a series of morphologic changes as keratinocytes progress from the germinative, 719: 712–719.
Google Scholar

So, A.K., Varisco, P-A., Kemkes-Matthes, B. et al. 2003. Arthritis is linked to local and systemic activation of coagulation and fibrinolysis pathways. Journal of thrombosis and haemostasis: JTH, 1: 2510–2515.
Google Scholar

Staquet, M.J., Haftek, M., Cordier, G. & Thivolet, J. 1987. Keratin filament composition of human epidermal spinous and granular cell fractions selected by flow cytometric sorting. Archives of dermatological research, 279: 273–275.
Google Scholar

Steinert, P.M., Mack, J.W., Korge, B.P. et al. 1991. Glycine loops in proteins: their occurrence in certain intermediate filament chains, loricrins and single-stranded RNA binding proteins. International journal of biological macromolecules, 13: 130–139.
Google Scholar

Suzuki, A., Yamada, R. & Yamamoto, K. 2007. Citrullination by Peptidylarginine Deiminase in Rheumatoid Arthritis. Annals of the New York Academy of Sciences, 1108: 323–339. http://dx.doi.org/10.1196/annals.1422.034
Google Scholar

Takahara, H., Okamoto, H. & Sugawara, K. 1986. Calcium-dependent Properties of Peptidylarginine from Rabbit Skeletal Muscle. Agricultural and biological chemistry, 50: 2899–2904.
Google Scholar

Takizawa, Y., Suzuki, A., Sawada, T. et al. 2006. Citrullinated fibrinogen detected as a soluble citrullinated autoantigen in rheumatoid arthritis synovial fluids. Annals of the rheumatic diseases, 65: 1013–1020. http://dx.doi.org/10.1136/ard.2005.044743
Google Scholar

Tarcsa, E., Marekov, L.N., Andreoli, J. et al. 1997. The Fate of Trichohyalin. 272: 27893–27901.
Google Scholar

Tarcsa, E., Marekov, L.N., Mei, G. et al. 1996a. Protein unfolding by peptidylarginine deiminase. Substrate specificity and structural relationships of the natural substrates trichohyalin and filaggrin. The Journal of biological chemistry, 271: 30709–30716.
Google Scholar

Thompson, P.R. & Fast, W. 2006. Histone citrullination by protein arginine deiminase: is arginine methylation a green light or a roadblock? ACS chemical biology, 1: 433–441. http://dx.doi.org/10.1021/cb6002306
Google Scholar

Vossenaar, E.R. 2004. Expression and activity of citrullinating peptidylarginine deiminase enzymes in monocytes and macrophages. Annals of the Rheumatic Diseases, 63: 373–381. http://dx.doi.org/10.1136/ard.2003.012211
Google Scholar

Vossenaar, E.R., Zendman, A.J.W., Van Venrooij, W.J. & Pruijn, G.J.M. 2003. PAD, a growing family of citrullinating enzymes: genes, features and involvement in disease. BioEssays: news and reviews in molecular, cellular and developmental biology, 25: 1106–1118. http://dx.doi.org/10.1002/bies.10357
Google Scholar

Wang, L., Chang, X., Yuan, G. et al. 2010. Expression of peptidylarginine deiminase type 4 in ovarian tumors. International journal of biological sciences, 6: 454–464.
Google Scholar

Whitaker, J.N., Bashir, R.M., Chou, C.H. & Kibler, R.F. 1980. Antigenic features of myelin basic protein-like material in cerebrospinal fluid. Journal of immunology (Baltimore, Md : 1950), 124: 1148–1153.
Google Scholar

Wood, D.D., Bilbao, J.M., O’Connors, P. & Moscarello, M.A. 1996. Acute multiple sclerosis (Marburg type) is associated with developmentally immature myelin basic protein. Annals of neurology, 40: 18–24. http://dx.doi.org/10.1002/ana.410400106
Google Scholar

Wysocka, J., Allis, C.D. & Coonrod, S. 2006. Histone arginine methylation and its dynamic regulation. Frontiers in bioscience : a journal and virtual library, 11: 344–355.
Google Scholar

Ying, S., Simon, M., Serre, G. & Takahara, H. 2012. Peptidylarginine Deiminases and Protein Deimination in Skin Physiopathology. In: O'Daly J. (ed.), Psoriasis - A Systemic Disease, 118–132, InTech.
Google Scholar

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Published

2013-12-31

How to Cite

Gogól, M. (2013). Citrullination – small change with a great consequence. Acta Universitatis Lodziensis. Folia Biologica Et Oecologica, 9, 17–25. https://doi.org/10.2478/fobio-2013-0003

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