Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-22T22:15:39.610Z Has data issue: false hasContentIssue false
  • English
  • Français

Effect of arginine deficiency on arginine-dependent post-translational protein modifications in mice

Published online by Cambridge University Press:  08 March 2007

Karin L. Kwikkers ,
Jan M. Ruijter ,
Wil T. Labruyère ,
Kathryn K. McMahon  and
Wouter H. Lamers
Karin L. Kwikkers
Affiliation:
AMC Liver Center and Department of Anatomy and Embryology, Academic Medical Center, University of Amsterdam, Meibergdreef 69-71, 1105 BK, Amsterdam, The Netherlands
Jan M. Ruijter
Affiliation:
AMC Liver Center and Department of Anatomy and Embryology, Academic Medical Center, University of Amsterdam, Meibergdreef 69-71, 1105 BK, Amsterdam, The Netherlands
Wil T. Labruyère
Affiliation:
AMC Liver Center and Department of Anatomy and Embryology, Academic Medical Center, University of Amsterdam, Meibergdreef 69-71, 1105 BK, Amsterdam, The Netherlands
Kathryn K. McMahon
Affiliation:
Department of Pharmacology, Texas Tech University Health Sciences Center, Lubbock, USA
Wouter H. Lamers*
Affiliation:
AMC Liver Center and Department of Anatomy and Embryology, Academic Medical Center, University of Amsterdam, Meibergdreef 69-71, 1105 BK, Amsterdam, The Netherlands
*
*Corresponding author: Dr Wouter H. Lamers, fax +31 20 5669190, email [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Transgenic mice that overexpress arginase-I in their small-intestinal enterocytes suffer from a pronounced, but selective decrease in circulating arginine levels during the suckling period, resulting in impaired growth and development of hair, muscle and immune system. In the present study, we tested the hypothesis that the arginine-deficiency phenotype is caused by arginine-specific post-translational modifications, namely, an increase in the degree of mono-ADP-ribosylation of proteins because of reduced competition by free arginine residues and/or an increase in protein-tyrosine nitration because of an increased O2− production by NO synthases in the presence of limiting amounts of arginine. Arginine ADP-ribosylation and tyrosine nitration of proteins in the affected organs were assayed by Western blot analysis, using specific anti-ADP-ribosylarginine and protein-nitrotyrosine antisera. The composition of the group of proteins that were preferentially arginine ADP-ribosylated or tyrosine-nitrated in the respective organs was strikingly similar. Arginine-deficient mice differed from their controls in a reduced ADP-ribosylation of a 130 kDa and a 65 kDa protein in skin and an increased protein nitration of an 83 kDa protein in bone marrow and a 250 kDa protein in spleen. Since only 20 % of the visualised proteins were differentially modified in a subset of the affected organs, our findings appear to rule out these prominent arginine-dependent post-translational protein modifications as mediators of the characteristic phenotype of severely arginine-deficient mice.

Keywords

Transgenic miceMono-ADP-ribosylationTyrosine nitrationWestern blot analysis
Type
Research Article
Information
British Journal of Nutrition , Volume 93 , Issue 2 , February 2005 , pp. 183 - 189
Copyright
Copyright © The Nutrition Society 2005

References

Adriouch, S, Ohlrogge, W, Haag, F, Koch-Nolte, F & Seman, M (2001) Rapid induction of naive T cell apoptosis by ecto-nicotinamide adenine dinucleotide: requirement for mono(ADP-ribosyl)transferase 2 and a downstream effector. J Immunol 167, 196–203.CrossRefGoogle Scholar
Corda, D & Di Girolamo, M (2002) Mono-ADP-ribosylation: a tool for modulating immune response and cell signaling. Sci STKE 2002, E53CrossRefGoogle ScholarPubMed
Corda, D & Di Girolamo, M (2003) Functional aspects of protein mono-ADP-ribosylation. EMBO J 22, 1953–1958.CrossRefGoogle ScholarPubMed
Davis, TA, Fiorott, ML & Reeds, PJ (1993) Amino acid compositions of body and milk protein change during the suckling period in rats. J Nutr 123, 947–956.CrossRefGoogle ScholarPubMed
De Jonge, WJ, Dingemanse, MA, de Boer, PA, Lamers, WH & Moorman, AF (1998) Arginine-metabolizing enzymes in the developing rat small intestine. Pediatr Res 43, 442–451.CrossRefGoogle ScholarPubMed
De Jonge, WJ, Hallemeesch, MM, Kwikkers, KL, Ruijter, JM, Gier-de Vries, C, van Roon, MA, Meijer, AJ, Marescau, B, de Deyn, PP, Deutz, NE & Lamers, WH (2002a) Overexpression of arginase I in enterocytes of transgenic mice elicits a selective arginine deficiency and affects skin, muscle, and lymphoid development. Am J Clin Nutr 76, 128–140.CrossRefGoogle ScholarPubMed
De Jonge, WJ, Kwikkers, KL, te Velde, AA, van Deventer, SJ, Nolte, MA, Mebius, RE, Ruijter, JM, Lamers, MC & Lamers, WH (2002b) Arginine deficiency affects early B cell maturation and lymphoid organ development in transgenic mice. J Clin Invest 110, 1539–1548.CrossRefGoogle Scholar
Greenacre, SA & Ischiropoulos, H (2001) Tyrosine nitration: localisation, quantification, consequences for protein function and signal transduction. Free Radic Res 34, 541–581.CrossRefGoogle ScholarPubMed
Hallemeesch, MM, Dejonge, CHC, De Jonge, WJ, Soeters, PB, Lamers, WH & Deutz, NE (2003) Chronic reduction of circulating arginine by ornithine transcarbamylase deficiency causes a reduction of cNOS-mediated NO production. Am J Physiol 285, E871–E875.Google Scholar
Herzfeld, A & Raper, SM (1976) Enzymes of ornithine metabolism in adult and developing rat intestine. Biochim Biophys Acta 428, 600–610.CrossRefGoogle ScholarPubMed
Hilz, H, Fanick, W & Klapproth, K (1986) 2'-Phosphoadenylylation of eukaryotic proteins: a type of covalent modification. Proc Natl Acad Sci USA 83, 6267–6271.CrossRefGoogle ScholarPubMed
Hsia, JA, Tsai, SC, Adamik, R, Yost, DA, Hewlett, EL & Moss, J (1985) Amino acid-specific ADP-ribosylation. Sensitivity to hydroxylamine of [cysteine(ADP-ribose)]protein and [arginine(ADP-ribose)]protein linkages. J Biol Chem 260, 16187–16191.CrossRefGoogle ScholarPubMed
Hurwitz, R & Kretchmer, N (1986) Development of arginine-synthesizing enzymes in mouse intestine. Am J Physiol 251, G103–G110.Google ScholarPubMed
Klebl, BM, Gopel, SO & Pette, D (1997) Specificity and target proteins of arginine-specific mono-ADP-ribosylation in T-tubules of rabbit skeletal muscle. Arch Biochem Biophys 347, 155–162.CrossRefGoogle ScholarPubMed
Klotz, LO, Schroeder, P & Sies, H (2002) Peroxynitrite signaling: receptor tyrosine kinases and activation of stress-responsive pathways. Free Radic Biol Med 33, 737–743.CrossRefGoogle ScholarPubMed
Kurokawa, T, Fujimura, Y, Takahashi, K, Chono, E & Ishibashi, S (1995) Reduction of mono(ADP-ribosyl)ation of histones in rat testis by gonadotropin-testosterone system. Biochem Biophys Res Commun 215, 808–813.CrossRefGoogle ScholarPubMed
McDonald, LJ & Moss, J (1994) Enzymatic and nonenzymatic ADP-ribosylation of cysteine. Mol Cell Biochem 138, 221–226.CrossRefGoogle ScholarPubMed
Meyer, T & Hilz, H (1986) Production of anti-(ADP-ribose) antibodies with the aid of a dinucleotide-pyrophosphatase-resistant hapten and their application for the detection of mono(ADP-ribosyl)ated polypeptides. Eur J Biochem 155, 157–165.CrossRefGoogle ScholarPubMed
Minetti, M, Mallozzi, C, Di Stasi, AM (2002) Peroxynitrite activates kinases of the src family and upregulates tyrosine phosphorylation signaling. Free Radic Biol Med 33, 744–754.CrossRefGoogle ScholarPubMed
Moss, J, Stevens, LA, Cavanaugh, E, Okazaki, IJ, Bortell, R, Kanaitsuka, T, Mordes, JP, Greiner, DL & Rossini, AA (1997) Characterization of mouse Rt6.1 NAD:arginine ADP-ribosyltransferase. J Biol Chem 272, 4342–4346.CrossRefGoogle ScholarPubMed
Nagy, LE & Kretchmer, N (1988) Utilization of glutamine in the developing rat jejunum. J Nutr 118, 189–193.CrossRefGoogle ScholarPubMed
Nemoto, E, Yu, Y & Dennert, G (1996) Cell surface ADP-ribosyltransferase regulates lymphocyte function-associated molecule-1 (LFA-1) function in T cells. J Immunol 157, 3341–3349.CrossRefGoogle ScholarPubMed
Okamoto, S, Azhipa, O, Yu, Y, Russo, E & Dennert, G (1998) Expression of ADP-ribosyltransferase on normal T lymphocytes and effects of nicotinamide adenine dinucleotide on their function. J Immunol 160, 4190–4198.CrossRefGoogle ScholarPubMed
Okazaki, IJ & Moss, J (1999) Characterization of glycosylphosphatidylinositol-anchored, secreted, and intracellular vertebrate mono-ADP-ribosyltransferases. Annu Rev Nutr 19, 485–509.CrossRefGoogle Scholar
Riby, JE, Hurwitz, RE & Kretchmer, N (1990) Development of ornithine metabolism in the mouse intestine. Pediatr Res 28, 261–265.CrossRefGoogle ScholarPubMed
Schwab, CJ, Colville, MJ, Fullerton, AT & McMahon, KK (2000) Evidence of endogenous mono-ADP-ribosylation of cardiac proteins via anti-ADP-ribosylarginine immunoreactivity. Proc Soc Exp Biol Med 223, 389–396.Google ScholarPubMed
Tanny, JC, Dowd, GJ, Huang, J, Hilz, H & Moazed, D (1999) An enzymatic activity in the yeast Sir2 protein that is essential for gene silencing. Cell 99, 735–745.CrossRefGoogle ScholarPubMed
ter Steege, JC, Koster-Kamphuis, L, van Straaten, EA, Forget, PP & Buurman, WA (1998) Nitrotyrosine in plasma of celiac disease patients as detected by a new sandwich ELISA. Free Radic Biol Med 25, 953–963.CrossRefGoogle ScholarPubMed
Tsuchiya, M & Shimoyama, M (1994) Target protein for eucaryotic arginine-specific ADP-ribosyltransferase. Mol Cell Biochem 138, 113–118.CrossRefGoogle ScholarPubMed
Visek, WJ (1984) An update of concepts of essential amino acids. Annu Rev Nutr 4, 137–155.CrossRefGoogle ScholarPubMed
Wu, G (1997) Synthesis of citrulline and arginine from proline in enterocytes of postnatal pigs. Am J Physiol 272, G1382–G1390.Google ScholarPubMed
Wu, G & Knabe, DA (1995) Arginine synthesis in enterocytes of neonatal pigs. Am J Physiol 269, R621–R629.Google ScholarPubMed
Xia, Y, Dawson, VL, Dawson, TM, Snyder, SH & Zweier, JL (1996) Nitric oxide synthase generates superoxide and nitric oxide in arginine-depleted cells leading to peroxynitrite-mediated cellular injury. Proc Natl Acad Sci USA 93, 6770–6774.CrossRefGoogle ScholarPubMed
Xia, Y & Zweier, JL (1997) Superoxide and peroxynitrite generation from inducible nitric oxide synthase in macrophages. Proc Natl Acad Sci USA 94, 6954–6958.CrossRefGoogle ScholarPubMed
Ziegler, M (2000) New functions of a long-known molecule. Emerging roles of NAD in cellular signaling. Eur J Biochem 267, 1550–1564.CrossRefGoogle ScholarPubMed
Zolkiewska, A & Moss, J (1993) Integrin alpha 7 as substrate for a glycosylphosphatidylinositol-anchored ADP-ribosyltransferase on the surface of skeletal muscle cells. J Biol Chem 268, 25273–25276.CrossRefGoogle ScholarPubMed