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A History of Deimination Research in Japan: The Founding Fathers

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Protein Deimination in Human Health and Disease

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Abstract

The research on protein deimination and the enzymes responsible for catalyzing this posttranslational modification started from investigations of the hair follicle and myelin in central nerve system. About 60 years ago, in 1958, the presence of protein-bound citrulline was first reported by Dr. George Rogers (Adelaide University, Australia) in the protein of the inner root sheath (IRS) of hair follicles (Rogers 1958). In order to obtain information about the protein composition of the IRS, he conducted a quantitative amino acid analysis of an acid hydrolysate on sufficient amounts of IRS that were dissected from the vibrissae follicle of rats. At that time, the common method for separating amino acids was paper chromatography, and when applied to the IRS hydrolysates, citrulline was discovered as a distinct ninhydrin-positive spot in an area adjacent to the basic amino acids. About 10 years after Rogers’s discovery, Dr. Mario Moscarello (Toronto University, Canada) started an intensive investigation of myelin sheath proteins in the central nerve system. In 1971, he also found the presence of peptide-bound citrulline in myelin basic protein (MBP) using similar methods to Rogers (Finch et al. 1971). Moscarello continued the investigation of MBP until he passed away in 2013, publishing many papers concerning the hyper-deimination of MBP in the pathology of multiple sclerosis. His research career involving the deimination of MBP was described in a eulogy in the first volume of this book series (Nicholas and Bhattacharya 2014).

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References

  • Arita, K., et al. (2004). Structural basis for Ca(2+)-induced activation of human PAD4. Nature Structural & Molecular Biology, 11(8), 777–783.

    Article  CAS  Google Scholar 

  • Asaga, H., Yamada, M., & Senshu, T. (1998). Selective deimination of vimentin in calcium ionophore-induced apoptosis of mouse peritoneal macrophages. Biochemical and Biophysical Research Communications, 243(3), 641–646.

    Article  CAS  PubMed  Google Scholar 

  • Chavanas, S., et al. (2004). Comparative analysis of the mouse and human peptidylarginine deiminase gene clusters reveals highly conserved non-coding segments and a new human gene, PADI6. Gene, 330, 19–27.

    Article  CAS  PubMed  Google Scholar 

  • Finch, P. R., Wood, D. D., & Moscarello, M. A. (1971). The presence of citrulline in a myelin protein fraction. FEBS Letters, 15(2), 145–148.

    Article  CAS  PubMed  Google Scholar 

  • Fujisaki, M., & Sugawara, K. (1981). Properties of peptidylarginine deiminase from the epidermis of newborn rats. Journal of Biochemistry, 89(1), 257–263.

    Article  CAS  PubMed  Google Scholar 

  • Girbal-Neuhauser, E., et al. (1999). The epitopes targeted by the rheumatoid arthritis-associated antifilaggrin autoantibodies are posttranslationally generated on various sites of (pro)filaggrin by deimination of arginine residues. Journal of Immunology, 162(1), 585–594.

    CAS  Google Scholar 

  • Guerrin, M., Ishigami, A., Mechin, M. C., Nachat, R., Valmary, S., Sebbag, M., Simon, M., Senshu, T., & Serre, G. (2003). cDNA cloning, gene organization and expression analysis of human peptidylarginine deiminase type I. Biochemical Journal, 370(Pt 1), 167–174.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsu, P. C., et al. (2014). Vimentin is involved in peptidylarginine deiminase 2-induced apoptosis of activated Jurkat cells. Molecules and Cells, 37(5), 426–434.

    Article  PubMed  PubMed Central  Google Scholar 

  • Inagaki, M., et al. (1989). Ca2+-dependent deimination-induced disassembly of intermediate filaments involves specific modification of the amino-terminal head domain. The Journal of Biological Chemistry, 264(30), 18119–18127.

    CAS  PubMed  Google Scholar 

  • Ishigami, A., et al. (1998). Molecular cloning of two novel types of peptidylarginine deiminase cDNAs from retinoic acid-treated culture of a newborn rat keratinocyte cell line. FEBS Letters, 433(1–2), 113–118.

    Article  CAS  PubMed  Google Scholar 

  • Ishigami, A., et al. (2002). Human peptidylarginine deiminase type II: Molecular cloning, gene organization, and expression in human skin. Archives of Biochemistry and Biophysics, 407(1), 25–31.

    Article  CAS  PubMed  Google Scholar 

  • Ishigami, A., et al. (2005). Abnormal accumulation of citrullinated proteins catalyzed by peptidylarginine deiminase in hippocampal extracts from patients with Alzheimer’s disease. Journal of Neuroscience Research, 80(1), 120–128.

    Article  CAS  PubMed  Google Scholar 

  • Kanno, T., et al. (2000). Human peptidylarginine deiminase type III: Molecular cloning and nucleotide sequence of the cDNA, properties of the recombinant enzyme, and immunohistochemical localization in human skin. The Journal of Investigative Dermatology, 115(5), 813–823.

    Article  CAS  PubMed  Google Scholar 

  • Masson-Bessière, C., et al. (2001). The major synovial targets of the rheumatoid arthritis-specific antifilaggrin autoantibodies are deiminated forms of the alpha- and beta-chains of fibrin. Journal of Immunology, 166(6), 4177–4184.

    Article  Google Scholar 

  • Nakashima, K., et al. (1999). Molecular characterization of peptidylarginine deiminase in HL-60 cells induced by retinoic acid and 1alpha,25-dihydroxyvitamin D(3). The Journal of Biological Chemistry, 274(39), 27786–27792.

    Article  CAS  PubMed  Google Scholar 

  • Nakashima, K., Hagiwara, T., & Yamada, M. (2002). Nuclear localization of peptidylarginine deiminase V and histone deimination in granulocytes. The Journal of Biological Chemistry, 277(51), 49562–49568.

    Article  CAS  PubMed  Google Scholar 

  • Nicholas, A. P., & Bhattacharya, S. K. (Eds.). (2014). Protein deimination in human health and disease. New York: Springer.

    Google Scholar 

  • Nishijyo, T., et al. (1997). Isolation and molecular cloning of epidermal- and hair follicle-specific peptidylarginine deiminase (type III) from rat. Journal of Biochemistry, 121(5), 868–875.

    Article  CAS  PubMed  Google Scholar 

  • Ohsugi, I., et al. (1995). Expression of mouse uterine peptidylarginine deiminase in Escherichia coli: Construction of expression plasmid and properties of the recombinant enzyme. Archives of Biochemistry and Biophysics, 317(1), 62–68.

    Article  CAS  PubMed  Google Scholar 

  • Rogers, G. E. (1958). Some observations on the proteins of the inner root sheath cells of hair follicles. Biochimica et Biophysica Acta, 29(1), 33–43.

    Article  CAS  PubMed  Google Scholar 

  • Rogers, G. E., Harding, H. W., & Llewellyn-Smith, I. J. (1977). The origin of citrulline-containing proteins in the hair follicle and the chemical nature of trichohyalin, an intracellular precursor. Biochimica et Biophysica Acta, 495(1), 159–175.

    Article  CAS  PubMed  Google Scholar 

  • Rus’d, A. A., et al. (1999). Molecular cloning of cDNAs of mouse peptidylarginine deiminase type I, type III and type IV, and the expression pattern of type I in mouse. European Journal of Biochemistry, 259(3), 660–669.

    Article  PubMed  Google Scholar 

  • Senshu, T., et al. (1989). Peptidylarginine deiminase in rat pituitary: Sex difference, estrous cycle-related changes, and estrogen dependence. Endocrinology, 124(6), 2666–2670.

    Article  CAS  PubMed  Google Scholar 

  • Senshu, T., et al. (1992). Detection of citrulline residues in deiminated proteins on polyvinylidene difluoride membrane. Analytical Biochemistry, 203(1), 94–100.

    Article  CAS  PubMed  Google Scholar 

  • Senshu, T., et al. (1995). Detection of deiminated proteins in rat skin: Probing with a monospecific antibody after modification of citrulline residues. The Journal of Investigative Dermatology, 105(2), 163–169.

    Article  CAS  PubMed  Google Scholar 

  • Sugawara, K. (1979). Presence of citrulline in the membranous proteins of stratum corneum of newborn rat and cow snout. Agricultural and Biological Chemistry, 43(12), 2215–2217.

    CAS  Google Scholar 

  • Suzuki, A., et al. (2003). Functional haplotypes of PADI4, encoding citrullinating enzyme peptidylarginine deiminase 4, are associated with rheumatoid arthritis. Nature Genetics, 34(4), 395–402.

    Article  CAS  PubMed  Google Scholar 

  • Takahara, H., Oikawa, Y., & Sugawara, K. (1983). Purification and characterization of peptidylarginine deiminase from rabbit skeletal muscle. Journal of Biochemistry, 94(6), 1945–1953.

    Article  CAS  PubMed  Google Scholar 

  • Takahara, H., Okamoto, H., & Sugawara, K. (1985). Specific modification of the functional arginine residue in soybean trypsin inhibitor (Kunitz) by peptidylarginine deiminase. The Journal of Biological Chemistry, 260(14), 8378–8383.

    CAS  PubMed  Google Scholar 

  • Takahara, H., Okamoto, H., & Sugawara, K. (1986). Affinity chromatography of peptidylarginine deiminase from rabbit skeletal muscle on a column of soybean trypsin inhibitor (Kunitz)-Sepharose. Journal of Biochemistry, 99(5), 1417–1424.

    Article  CAS  PubMed  Google Scholar 

  • Takahara, H., et al. (1989). Peptidylarginine deiminase of the mouse. Distribution, properties, and immunocytochemical localization. The Journal of Biological Chemistry, 264(22), 13361–13368.

    CAS  PubMed  Google Scholar 

  • Takahara, H., et al. (1992). Expression of peptidylarginine deiminase in the uterine epithelial cells of mouse is dependent on estrogen. The Journal of Biological Chemistry, 267(1), 520–525.

    CAS  PubMed  Google Scholar 

  • Terakawa, H., Takahara, H., & Sugawara, K. (1991). Three types of mouse peptidylarginine deiminase: Characterization and tissue distribution. Journal of Biochemistry, 110(4), 661–666.

    Article  CAS  PubMed  Google Scholar 

  • Tsuchida, M., et al. (1993). cDNA nucleotide sequence and primary structure of mouse uterine peptidylarginine deiminase. Detection of a 3′-untranslated nucleotide sequence common to the mRNA of transiently expressed genes and rapid turnover of this enzyme’s mRNA in the estrous cycle. European Journal of Biochemistry, 215(3), 677–685.

    Article  CAS  PubMed  Google Scholar 

  • Watanabe, K., & Senshu, T. (1989). Isolation and characterization of cDNA clones encoding rat skeletal muscle peptidylarginine deiminase. The Journal of Biological Chemistry, 264(26), 15255–15260.

    CAS  PubMed  Google Scholar 

  • Watanabe, K., et al. (1988). Combined biochemical and immunochemical comparison of peptidylarginine deiminases present in various tissues. Biochimica et Biophysica Acta, 966(3), 375–383.

    Article  CAS  PubMed  Google Scholar 

  • Wright, P. W., et al. (2003). ePAD, an oocyte and early embryo-abundant peptidylarginine deiminase-like protein that localizes to egg cytoplasmic sheets. Developmental Biology, 256(1), 73–88.

    Article  CAS  PubMed  Google Scholar 

  • Yamakoshi, A., et al. (1998). Cloning of cDNA encoding a novel isoform (type IV) of peptidylarginine deiminase from rat epidermis. Biochimica et Biophysica Acta, 1386(1), 227–232.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. College of Agriculture, Ibaraki University, 3-21-1, Chuuo, Ami, Inashiki, 300-0393, Ibaraki, Japan

    Hidenari Takahara

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  1. Hidenari Takahara
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Correspondence to Hidenari Takahara .

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Editors and Affiliations

  1. Department of Neurology, University of Alabama at Birmingham and The Birmingham Veterans Administration Medical Center, Birmingham, Alabama, USA

    Anthony P. Nicholas

  2. Bascom Palmer Eye Institute, University of Miami, Miami, Florida, USA

    Sanjoy K. Bhattacharya

  3. Department of Biochemistry and Molecular Pharmacology, UMASS Medical School, Worcester, Massachusetts, USA

    Paul R. Thompson

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Takahara, H. (2017). A History of Deimination Research in Japan: The Founding Fathers. In: Nicholas, A., Bhattacharya, S., Thompson, P. (eds) Protein Deimination in Human Health and Disease. Springer, Cham. https://doi.org/10.1007/978-3-319-58244-3_1

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