Amino Acids

, 29:177 | Cite as

Almost all about citrulline in mammals

  • E. Curis
  • I. Nicolis
  • C. Moinard
  • S. Osowska
  • N. Zerrouk
  • S. Bénazeth
  • L. Cynober
Review Article

Summary.

Citrulline (Cit, C6H13N3O3), which is a ubiquitous amino acid in mammals, is strongly related to arginine. Citrulline metabolism in mammals is divided into two fields: free citrulline and citrullinated proteins. Free citrulline metabolism involves three key enzymes: NO synthase (NOS) and ornithine carbamoyltransferase (OCT) which produce citrulline, and argininosuccinate synthetase (ASS) that converts it into argininosuccinate. The tissue distribution of these enzymes distinguishes three “orthogonal” metabolic pathways for citrulline. Firstly, in the liver, citrulline is locally synthesized by OCT and metabolized by ASS for urea production. Secondly, in most of the tissues producing NO, citrulline is recycled into arginine via ASS to increase arginine availability for NO production. Thirdly, citrulline is synthesized in the gut from glutamine (with OCT), released into the blood and converted back into arginine in the kidneys (by ASS); in this pathway, circulating citrulline is in fact a masked form of arginine to avoid liver captation. Each of these pathways has related pathologies and, even more interestingly, citrulline could potentially be used to monitor or treat some of these pathologies. Citrulline has long been administered in the treatment of inherited urea cycle disorders, and recent studies suggest that citrulline may be used to control the production of NO. Recently, citrulline was demonstrated as a potentially useful marker of short bowel function in a wide range of pathologies. One of the most promising research directions deals with the administration of citrulline as a more efficient alternative to arginine, especially against underlying splanchnic sequestration of amino acids. Protein citrullination results from post-translational modification of arginine; that occurs mainly in keratinization-related proteins and myelins, and insufficiencies in this citrullination occur in some auto-immune diseases such as rheumatoid arthritis, psoriasis or multiple sclerosis.

Keywords: Citrulline metabolism – Urea cycle – Citrullinated proteins – Nitric oxide metabolism – Argininosuccinate synthetase – Ornithine carbamoyltransferase 

References

  1. Akashi, K, Miyake, C, Yokota, A 2001Citrulline, a novel compatible solute in drought-tolerant wild watermelon leaves, is an efficient hydroxyl radical scavenger.FEBS Lett508438442PubMedCrossRefGoogle Scholar
  2. Alteheld B, Stehle P, Fürst P (2004) Measurement of amino acid concentrations in biological fluids and tissues using reversed-phase HPLC-based methods. In: Cynober L (ed) Metabolic and therapeutic aspects of amino acids in clinical nutrition, chap. 2, 2nd edn. CRC Press, Boca Raton, pp 29–44Google Scholar
  3. Aoki, E, Takeuchi, IK 1997Immunohistochemical localization of arginine and citrulline in rat renal tissue.J Histochem Cytochem45875881PubMedGoogle Scholar
  4. Aoki, Y, Sunaga, H, Suzuki, KT 1988A cadmium-binding protein in rat liver identified as ornithine carbamoyltransferase.Biochem J250735742PubMedGoogle Scholar
  5. Arai, T, Kusubata, M, Kohsaka, T, Shiraiwa, M, Sugawara, K, Takahara, H 1995Mouse uterus peptidylarginine deiminase is expressed in decidual cells during pregnancy.J Cell Biochem58269278PubMedCrossRefGoogle Scholar
  6. Asaga, H, Yamada, M, Senshu, T 1998Selective deimination of vimentin in calcium ionophore-induced apoptosis of mouse peritoneal macrophages.Biochem Res Commun243641646Google Scholar
  7. Ashida, T, Fumakoshi, K, Tsukihara, T, Ueki, T, Kakudo, M 1972The crystal structures of L-citrulline hydrochloride and L-homocitrulline hydrochloride.Acta Cryst B2813671374Google Scholar
  8. Awrich, AE, Stackhouse, WJ, Cantrell, JE, Patterson, JH, Rudman, D 1975Hyperdibasicaminoaciduria, hyperammonemia, and growth retardation: treatment with arginine, lysine, and citrulline.J Pediatr87731738PubMedGoogle Scholar
  9. Bansal, V, Rodriguez, P, Wu, G, Eichler, DC, Zabaletta, J, Taheri, F, Ochoa, JB 2004Citrulline can preserve proliferation and prevent the loss of CD3 ζ chain under conditions of low arginine.J Parenter Enteral Nutr28423430Google Scholar
  10. Baur, H, Stalon, V, Falmagne, P, Luethi, E, Haas, D 1987Primary and quaternary structure of the catabolic ornithine carbamoyltransferase from Pseudomonas aeruginosa. Extensive sequence homology with the anabolic ornithine carbamoyltransferases of Escherichia coli.Eur J Biochem166111117PubMedCrossRefGoogle Scholar
  11. Baydoun, AR, Bogle, RG, Pearson, JD, Mann, GE 1994Discrimination between citrulline and arginine transport in activated murine macrophages: inefficient synthesis of NO from recycling of citrulline to arginine.Br J Pharmacol112487492PubMedGoogle Scholar
  12. Bendahan, D, Mattei, JP, Ghattas, B, Confort-Gouny, S, Guern, MEL, Cozzone, PJ 2002Citrulline/malate promotes aerobic energy production in human exercising muscle.Br J Sports Med36282289PubMedCrossRefGoogle Scholar
  13. Berendsen, HJC, Postma, JPM, van Gunsteren, WF, DiNola, A, Haak, JR 1984Molecular dynamics with coupling to an external bath.J Chem Phys8136843690CrossRefGoogle Scholar
  14. Berendsen, HJC, van der Spoel, D, van Drunen, R 1995GROMACS: a message-passing parallel molecular dynamics implementation.Comp Phys Comm914356Google Scholar
  15. Blijlevens, NMA, Lutgens, LCHW, Schattenberg, AVMB, Donnelly, JP 2004Citrulline: a potentially simple quantitative marker of intestinal epithelial damage following myeloablative therapy.Bone Marrow Transplant34193196PubMedCrossRefGoogle Scholar
  16. Boirie, Y, Gachon, P, Beaufrre, B 1997Splanchnic and whole-body leucine kinetics in young and elderly men.Am J Clin Nutr65489495PubMedGoogle Scholar
  17. Buckingham J (ed) (1994) Dictionary of natural products, vol 1, 1st edn Chapman & Hall, Chemical Database, London, p 1046Google Scholar
  18. Budavari S, O’Neil MJ, Heckelman PE, Kinneary JF (eds) (2001) The Merck Index: an encyclopedia of chemicals, drugs, and biologicals, 13th edn. CRC Press, Whitehouse StationGoogle Scholar
  19. Burns, SP, Woolf, DA, Leonard, JV, Iles, RA 1992Investigation of urea cycle enzyme disorders by 1H-NMR spectroscopy.Clin Chim Acta2094760PubMedCrossRefGoogle Scholar
  20. Callis, A, Magnan de Bornier, B, J-J, S, Bellet, H, Saumade, R 1991Activity of citrulline malate on acid-base balance and blood ammonia and amino acid levels. Study in the animal and in man.Arzneimittelforschung41660663PubMedGoogle Scholar
  21. Camacho, JA, Obie, C, Biery, B, Goodman, BK, Hu, CA, Almashanu, S, Steel, G, Casey, R, Lambert, M, Mitchell, GA, Valle, D 1999Hyperornithinaemia-hyperammonaemia-homocitrullinuria syndrome is caused by mutations in a gene encoding a mitochondrial ornithine transporter.Nat Genet22151158PubMedGoogle Scholar
  22. Carmeli, E, Reznick, AZ, Coleman, R, Carmeli, V 2000Muscle strength and mass of lower extremities in relation to functional abilities in elderly adults.Gerontology46249257PubMedCrossRefGoogle Scholar
  23. Carmeli, E, Coleman, R, Reznick, AZ 2002The biochemistry of aging muscle.Exp Gerontol37477489PubMedCrossRefGoogle Scholar
  24. Carritt, B, Povey, S 1979Regional asssignments of the loci AK3, ACONS, and ASS on human chromosome 9.Cytogenet Cell Genet23171181PubMedGoogle Scholar
  25. Carritt, B, Goldfarb, PS, Hooper, ML, Slack, C 1977Chromosome assignment of a human gene for argininosuccinate synthetase expression in Chinese hamster × human somatic cell hybrids.Exp Cell Res1067178PubMedCrossRefGoogle Scholar
  26. Castillo, L, Chapman, TE, Sanchez, M, Yu, YM, Burke, JF, Ajami, AM, Vogt, J, Young, VR 1993Plasma arginine and citrulline kinetics in adults given adequate and arginine-free diets.Proc Natl Acad Sci USA9077497753PubMedGoogle Scholar
  27. Ceballos, I, Chauveau, P, Guerin, V, Bardet, J, Parvy, P, Kamoun, P, Jungers, P 1990Early alterations of plasma amino acids in chronic renal failure.Clin Chim Acta188101108PubMedCrossRefGoogle Scholar
  28. Cheung, CW, Cohen, NS, Raijman, L 1989Channeling of urea cycle intermediates in situ in permeabilized hepatocytes.J Biol Chem26440384044PubMedGoogle Scholar
  29. Chih-Kuang, C, Shuan-Pei, L, Shyue-Jye, L, Tuan-Jen, W 2002Plasma free amino acids in Taiwan Chinese: the effect of age.Clin Chem Lab Med40378382PubMedCrossRefGoogle Scholar
  30. Clarke, ER, Martell, AE 1970Metal chelates of arginine and related ligands.J Inorg Nuc Chem32911926Google Scholar
  31. Collective (1997) The Aldrich Library of FT-IR Spectra. Aldrich Chemical Co., Milwaukee, Refs. 464B, 464DGoogle Scholar
  32. Crenn, P, Coudray-Lucas, C, Thuillier, F, Cynober, L, Messing, B 2000Postabsorptive plasma citrulline concentration is a marker of absorptive enterocyte mass and intestinal failure in humans.Gastroenterology11914951505CrossRefGoogle Scholar
  33. Crenn, P, Vahedi, K, Lavergne-Slove, A, Cynober, L, Matuchansky, C, Messing, B 2003Plasma citrulline: a marker of enterocyte mass in villous atrophy-associated small bowel disease.Gastroenterology12412101219PubMedCrossRefGoogle Scholar
  34. Cynober, L 2002Plasma amino acid levels with a note on membrane transport: characteristics, regulation, and metabolic significance.Nutrition18761766PubMedGoogle Scholar
  35. Cynober, L, Le Boucher, J, Vasson, MP 1995Arginine metabolism in mammals.J Nutr Biochem6402413CrossRefGoogle Scholar
  36. Demarquoy, J, Fairand, A, Gautier, C, Vaillant, R 1994Demonstration of argininosuccinate synthetase activity associated with mitochondrial membrane: characterization and hormonal regulation.Mol Cell Biol136145155Google Scholar
  37. Dickinson, JC, Rosenblum, H, Hamilton, PB 1965Ion exchange chromatography of the free amino acid in the plasma of newborn infants.Pediatrics36213PubMedGoogle Scholar
  38. Dillon, EL, Knabe, DA, Wu, G 1999Lactate inhibits citrulline and arginine synthesis from proline in pig enterocytes.Am J Physiol Gastrointest Liver Physiol276G1079G1086Google Scholar
  39. Duchemann, T, Osowska, S, Walrand, S, Paillard, A, Boirie, Y, Cynober, L, Moinard, C 2004La Citrulline améliore l’accrétion protéique musculaire chez le rat âgé dénutri via une stimulation de la synthèse protéique.Nut Clin Metabol18S20(abstract)Google Scholar
  40. Ellenbogen, E 1952Dissociation constants of peptides. I. A survey of the effect of optical configuration.J Am Chem Soc7451985201CrossRefGoogle Scholar
  41. Engelke, UF, van Sambeek, MLL, de Jong, JG, Leroy, JG, Morava, É, Smeitink, JA, Wevers, RA 2004N-Acetylated metabolites in urine: proton nuclear magnetic resonance spectroscopic study on patients with inborn errors of metabolism.Clin Chem505866PubMedGoogle Scholar
  42. Eronina, TB, Livanova, NB, Chebotareva, NA, Kurganov, BI, Luo, S, Graves, DJ 1996Deimination of glycogen phosphorylase b by peptidylarginine deiminase. Influence on the kinetical characteristics and dimer-tetramer transition.Biochimie78253258PubMedCrossRefGoogle Scholar
  43. Essmann, U, Perera, L, Berkowitz, ML, Darden, T, Lee, H, Pedersen, LG 1995A smooth particle mesh Ewald method.J Chem Phys10385778593Google Scholar
  44. Fekkes, D, van Dalen, A, Edelman, M, Voskuilen, A 1995Validation of the determination of amino acids in plasma by high-performance liquid chromatography using automated pre-column derivatization with o-phthaldialdehyde.J Chromatogr B Biomed Sci Appl669177186CrossRefGoogle Scholar
  45. Feste, AS 1992Reversed-phase chromatography of phenylthiocarbamyl amino acid derivatives of physiological amino acids: an evaluation and a comparison with analysis by ion-exchange chromatography.J Chromatogr5742324PubMedGoogle Scholar
  46. Fornaris, E, Vanuxem, D, Duflot, J, Bernasconi, P, Grimaud, C 1984Approche pharmacoclinique de l’activité du malate de citrulline: étudedes taux de lactates sanguins lors d’un exercice musculaire standardisé.Gaz Méd Fr91125127Google Scholar
  47. Freytag, SO, Beaudet, AL, Bock, HG, O’Brien, WE 1984Molecular structure of the human argininosuccinate synthetase gene: occurrence of alternative mRNA splicing.Mol Cell Biol419781984PubMedGoogle Scholar
  48. Ganadu, ML, Leoni, V, Crisponi, G, Nurchi, V 1991An investigation on the interaction between Palladium(II) and L-citrulline by 1H and 13C NMR spectroscopy and potentiometry.Polyhedron10333336CrossRefGoogle Scholar
  49. Ghose, C, Raushel, FM 1985Determination of the mechanism of the argininosuccinate synthetase reaction by static and dynamic quench experiments.Biochemistry2458945898PubMedCrossRefGoogle Scholar
  50. Girbal-Neuhauser, E, Durieux, JJ, Arnaud, M, Dalbon, P, Sebbag, M, Vincent, C, Simon, M, Senshu, T, Masson-Bessière, C, Jolivet-Reynaud, C, Jolivet, M, Serre, G 1999The epitopes targeted by the rheumatoid arthritis-associated antifilaggrin autoantibodies are posttranslationally generated on various sites of (Pro)filaggrin by deimination of arginine residues.J Immunol162585594PubMedGoogle Scholar
  51. Goldsmith, JO, Kuo, LC 1993Utilization of conformational flexibility in enzyme action-linkage between binding, isomerization, and catalysis.J Biol Chem2681848118484PubMedGoogle Scholar
  52. Gondolesi, G, Fishbein, T, Chehade, M, Tschernia, A, Magid, M, Kaufman, S, Raymond, K, Sansaricq, C, LeLeiko, N 2002Serum citrulline is a potential marker for rejection of intestinal allografts.Transplant Proc34918920PubMedGoogle Scholar
  53. Gondolesi, GE, Kaufman, SS, Sansaricq, C, Magid, MS, Raymond, K, Iledan, LP, Tao, Y, Florman, SS, LeLeiko, NS, Fishbein, TM 2004Defining normal plasma citrulline in intestinal transplant recipients.Am J Transplant4414418PubMedCrossRefGoogle Scholar
  54. Goto, M, Nakajima, Y, Hirotsu, K 2002Crystal structure of argininosuccinate synthetase from Thermus thermophilus HB8. Structural basis for the catalytic action.J Biol Chem2771589015896PubMedGoogle Scholar
  55. Goto, M, Omi, R, Miyahara, I, Sugahara, M, Hirotsu, K 2003Structures of argininosuccinate synthetase in enzyme-ATP substrates and enzyme-AMP product forms: stereochemistry of the catalytic reaction.J Biol Chem2782296422971PubMedGoogle Scholar
  56. Häberle, J, Pauli, S, Linnebank, M, Kleijer, WJ, Bakker, HD, Wanders, RJA, Harms, E, Koch, HG 2002Structure of the human argininosuccinate synthetase gene and an improved system for molecular diagnostics in patients with classical and mild citrullinemia.Hum Genet110327333PubMedGoogle Scholar
  57. Hagiwara, T, Nakashima, K, Hirano, H, Senshu, T, Yamada, M 2002Deimination of arginine residues in nucleophosmin/B23 and histones in HL-60 granulocytes.Biochem Biophys Res Commun290979983PubMedCrossRefGoogle Scholar
  58. Hamano Y, Kodama H, Yanagisawa M, Haraguchi Y, Mori M, Yokota S (1988) Immunocytochemical localization of ornithine transcarbamylase in rat intestinal mucosa. Light and electron microscopic study. J Histochem Cytochem 36: 29–35 [LR: 20031114; JID: 9815334; 0 (Staphylococcal Protein A); 7440-57-5 (Gold); EC 2.1.3.3 (Ornithine Carbamoyltransferase); ppublish]Google Scholar
  59. Hao, G, Xie, L, Gross, SS 2004Argininosuccinate synthetase is reversibly inactivated by S-nitrosylation in vitro and in vivo.J Biol Chem2793619236200PubMedGoogle Scholar
  60. Hartman, WJ, Torre, PM, Prior, RL 1994Dietary citrulline but not ornithine counteracts dietary arginine deficiency in rats by increasing splanchnic release of citrulline.J Nutr12419501960PubMedGoogle Scholar
  61. Hebuterne, X, Broussard, JF, Rampal, P 1995Acute renutrition by cyclic enteral nutrition in elderly and younger patients.JAMA273638643PubMedCrossRefGoogle Scholar
  62. Hilderman, RH, Casey, TE, Pojoga, LH 2000P1, P4-Diadenosine 5′-tetraphosphate modulates L-arginine and L-citrulline uptake by bovine aortic endothelial cells.Arch Biochem Biophys375124130PubMedCrossRefGoogle Scholar
  63. Hoogenraad, N, Totino, N, Elmer, H, Wraight, C, Alewood, P, Johns, RB 1985Inhibition of intestinal citrulline synthesis causes severe growth retardation in rats.Am J Physiol Gastrointest Liver Physiol249G792G799Google Scholar
  64. Houghton, JE, Bencini, DA, O’Donovan, GA, Wild, JR 1984Protein differentiation: a comparison of aspartate transcarbamoylase and ornithine transcarbamoylase from Escherichia coli K-12.Proc Natl Acad Sci US8148644868Google Scholar
  65. Husson, A, Brasse-Lagnel, C, Fairand, A, Renouf, S, Lavoinne, A 2003Argininosuccinate synthetase from the urea cycle to the citrulline-NO cycle.Eur J Biochem27018871899PubMedCrossRefGoogle Scholar
  66. Imparl, JM, Senshu, T, J, GD 1995Studies of calcineurin-calmodulin interaction: probing the role of arginine residues using peptidylarginine deiminase.Arch Biochem Biophys318370377PubMedCrossRefGoogle Scholar
  67. Ishida-Yamamoto, A, Senshu, T, Takahashi, H, Akiyama, K, Nomura, K, Iizuka, H 2000Decreased deiminated keratin K1 in psoriatic hyperproliferative epidermis.J Invest Dermatol114701705PubMedCrossRefGoogle Scholar
  68. Ishigami, A, Ohsawa, T, Asaga, H, Akiyama, K, Kuramoto, M, Maruyama, N 2002Human peptidylarginine deiminase type II: molecular cloning, gene organization, and expression in human skin.Arch Biochem Biophys3822531Google Scholar
  69. Ishiyama, N, Bates, IR, Hill, CM, Wood, DD, Matharu, P, Viner, NJ, Moscarello, MA, Harauz, G 2001The effects of deimination of myelin basic protein on structures formed by its interaction with phosphoinositide-containing lipid monolayers.J Struct Biol1363045PubMedCrossRefGoogle Scholar
  70. Janeira, MA, Maia, JR, Santos, PJ 1998Citrulline malate effects on the aerobic–anaerobic threshold and in post-exercise blood lactate recovery.Med Sci Sports Exerc30155(abstract)Google Scholar
  71. Kamoun, P, Parvy, P, Cathelineau, L 1983A rapid and simple method for citrulline determination in plasma.Clin Chem29398400PubMedGoogle Scholar
  72. Kanno, T, Kawada, A, Yamanouchi, J, Yosida-Noro, C, Yoshiki, A, Shiraiwa, M, Kusakabe, M, Manabe, M, Tezuka, T, Takahara, H 2000Human peptidylarginine deiminase Type III: molecular cloning and nucleotide sequence of the cDNA, properties of the recombinant enzyme, and immunohistochemical localization in human skin.J Invest Dermatol115813823PubMedCrossRefGoogle Scholar
  73. Ke, HM, Honzatko, RB, Lipscomb, WN 1984Structure of unligated aspartate carbamoyltransferase of Escherichia coli at 2.6-A resolution.Proc Natl Acad Sci USA8140374040PubMedGoogle Scholar
  74. Keilhoff, G, Wolf, G 2003Citrulline immunohistochemistry may not necessarily identify nitric oxide synthase activity: the pitfall of peptidylarginine deiminase.Nitric Oxide83138PubMedCrossRefGoogle Scholar
  75. Keilhoff, G, Reiser, M, Stanarius, A, Aoki, E, Wolf, G 2000Citrulline immunochemistry for demonstration of NOS activity in vivo and in vitro.Nitric Oxide4343353PubMedCrossRefGoogle Scholar
  76. Knipp, M, Vašák, M 2000A colorimetric 96-well microtiter plate assay for the determination of enzymatically formed citrulline.Anal Biochem286257264PubMedCrossRefGoogle Scholar
  77. Kobayashi, K, Saheki, T, Imamura, Y, Noda, T, Inoue, I, Matuo, S, Hagihara, S, Nomiyama, H, Jinno, Y, Shimada, K 1986Messenger RNA coding for argininosuccinate synthetase in citrullinemia.Am J Hum Genet38667680PubMedGoogle Scholar
  78. Kobayashi, K, Sinasac, DS, Iijima, M, Boright, AP, Begum, L, Lee, JR, Yasuda, T, Ikeda, S, Hirano, R, Terazono, H, Crackower, MA, Kondo, I, Tsui, LC, Scherer, SW, Saheki, T 1999The gene mutated in adult-onset type II citrullinaemia encodes a putative mitochondrial carrier protein.Nat Genet22159163PubMedCrossRefGoogle Scholar
  79. Kone, BC 2004Nitric oxide synthesis in the kidney: isoforms, biosynthesis, and functions in health.Semin Nephrol24299315PubMedCrossRefGoogle Scholar
  80. Kuo LC, Caron C, Lee S, Herzberg W 1990. Zn2+ regulation of ornithine transcarbamoylase. II. Metal binding site. J Mol Biol 211: 271–280 [LR: 20001218; JID: 2985088R; 6600-40-4 (norvaline); 7004-03-7 (Valine); 7440-66-6 (Zinc); EC 2.1.3.3 (Ornithine Carbamoyltransferase); ppublish]Google Scholar
  81. Lau, T, Owen, W, Yu, YM, Noviski, N, Lyons, J, Zurakowski, D, Tsay, R, Ajami, A, Young, VR, Castillo, L 2000Arginine, citrulline, and nitric oxide metabolism in end-stage renal disease patients.J Clin Invest10512171225PubMedCrossRefGoogle Scholar
  82. Le Boucher, J, Charret, C, Coudray-Lucas, C, Giboudeau, J, Cynober, L 1997Amino acid determination in biological fluids by automated ion-exchange chromatography: performance of Hitachi L-8500A.Clin Chem4314211428PubMedGoogle Scholar
  83. Le Floc’h, N, Seve, B 2000Le Devenir des protéines et des acides aminés dans l’intestin du porc: de la digestion à l’apparition dans la veine porte.INRA Prod Anim13303314Google Scholar
  84. Legerton, TL, Kanamori, K, Weiss, RL, Roberts, JD 198115N NMR studies of nitrogen metabolism in intact mycelia of Neurospora crassa.Proc Natl Acad Sci USA7814951498PubMedGoogle Scholar
  85. Lemke, CT, Howell, PL 2001The 1.6 Å crystal structure of E. coli argininosuccinate synthetase suggests a conformational change during catalysis.Structure911531164PubMedCrossRefGoogle Scholar
  86. Lemke, CT, Howell, PL 2002Substrate induced conformational changes in argininosuccinate synthetase.J Biol Chem2771307413081PubMedCrossRefGoogle Scholar
  87. Lepage, N, McDonald, N, Dallaire, L, Lambert, M 1997Age-specific distribution of plasma amino acid concentrations in a healthy pediatric population.Clin Chem4323972402PubMedGoogle Scholar
  88. Levillain, O, Hus-Citharel, A, Morel, F, Bankir, L 1990Localization of arginine synthesis along rat nephron.Am J Physiol Renal Physiol259F916F923Google Scholar
  89. Levillain, O, Parvy, P, Hassler, C 1997Amino acid handling in uremic rats: citrulline, a reliable marker of renal insufficiency and proximal tubular dysfunction.Metabolism46611618PubMedCrossRefGoogle Scholar
  90. Lide DR (ed) (2004) CRC handbook of chemistry and physics, 85th edn. CRC Press, Boca RatonGoogle Scholar
  91. Lindahl, E, Hess, B, van der Spoel, D 2001GROMACS 3.0: a package for molecular simulation and trajectory analysis.J Mol Mod7306317Google Scholar
  92. Lindgren, V, de Martinville, B, Horwich, AL, Rosenberg, LE, Francke, U 1984Human ornithine transcarbamylase locus mapped to band Xp21.1 near the Duchenne muscular dystrophy locus.Science226698700PubMedGoogle Scholar
  93. Lirk, P, Hoffmann, G, Rieder, J 2002Inducible nitric oxide synthase – time for reappraisal.Curr Drug Targets Inflamm Allergy189108PubMedCrossRefGoogle Scholar
  94. Ludwig, RA 1993Arabidopsis chloroplasts dissimilate L-arginine and L-citrulline for use as N source.Plant Physiol101429434PubMedCrossRefGoogle Scholar
  95. Lundberg, P, Lundquist, PO 2004Primary metabolism in N2-fixing Alnus incana-Frankia symbiotic root nodules studied with 15N and 31P nuclear magnetic resonance spectroscopy.Planta219661672PubMedCrossRefGoogle Scholar
  96. Lutgens, LCHW, Deutz, NEP, Gueulette, J, Cleutjens, JPM, Berger, MPF, Wouters, BG, von Meyenfeldt, MF, Lambin, P 2003Citrulline: A physiologic marker enabling quantitation and monitoring of epithelial radiation-induced small bowel damage.Int J Radiat Oncol Biol Phys5710671074PubMedCrossRefGoogle Scholar
  97. Lutgens, LCHW, Blijlevens, NMA, Deutz, NEP, Donnelly, JP, Lambin, P, de Pauw, BE 2004aMonitoring myeloablative therapy-induced small bowel toxicity by serum citrulline concentration. A comparision with sugar permeability tests.Cancer103191199Google Scholar
  98. Lutgens, LCHW, Deutz, NEP, Granzier-Peeters, M, Beets-Tan, R, de Ruysscher, D, Gueulette, J, Cleutjens, JPM, Berger, MPF, Wouters, BG, von Meyenfeldt, MF, Lambin, P 2004bPlasma citrulline concentration: a surrogate end point for radiation-induced mucosal atrophy of the small bowel. A feasibility study in 23 patients.Int J Radiat Oncol Biol Phys60275285CrossRefGoogle Scholar
  99. Martens-Lobenhoffer, J, Bode-Böger, SM 2003Simultaneous detection of arginine, asymmetric dimethylarginine, symmetric dimethylarginine and citrulline in human plasma and urine applying liquid chromatography-mass spectrometry with very straightforward sample preparation.J Chromatogr B Analyt Technol Biomed Life Sci798231239PubMedGoogle Scholar
  100. Meijer, AJ, Lamers, WH, Chamuleau, RAFM 1990Nitrogen metabolism and ornithine cycle function.Physiol Rev70701748PubMedGoogle Scholar
  101. Meulemans, A 2000Electrochemical detection of nitroso-arginine as an intermediate between N-hydroxy-arginine and citrulline. An in vitro versus in vivo study using microcarbon electrodes in neuronal nitric oxide synthase and mice brain.Neurosci Lett294125129PubMedCrossRefGoogle Scholar
  102. Mistry, SK, Greenfeld, Z, Morris, SM,Jr, Baylis, C 2002The ‘intestinal-renal’ arginine biosynthetic axis in the aging rat.Mech Ageing Dev12311591165PubMedCrossRefGoogle Scholar
  103. Mizutani, N, Kato, T, Maehara, M, Watanabe, K, Ban, M 1984Oral administration of arginine and citrulline in the treatment of lysinuric protein intolearnce.Tohoku J Exp Med1421524PubMedGoogle Scholar
  104. Morris SM Jr (2000) Regulation of arginine availability and its impact on NO synthesis. In: Ignarro LJ (ed) Nitric oxide: biology and pathobiology, chap 11. Academic Press, San Diego, pp 187–197Google Scholar
  105. Moscarello, MA, Pritzker, L, Mastronardi, FG, Wood, DD 2002Peptidylarginine deiminase: a candidate factor in demyelinating disease.J Neurochem81335343PubMedCrossRefGoogle Scholar
  106. Mosoni, L, Valluy, MC, Serrurier, B, Prugnaud, J, Obled, C, Guezennec, CY, Mirand, PP 1995Altered response of protein synthesis to nutritional state and endurance training in old rats.Am J Physiol Endocrinol Metab268E328E335Google Scholar
  107. Murphy, C, Newsholme, P 1998Importance of glutamine metabolism in murine macrophages and human monocytes to L-arginine biosynthesis and rates of nitrite or urea production.Clin Sci95397407PubMedCrossRefGoogle Scholar
  108. Muscaritoli, M, Conversano, L, Petti, MC, Cascino, A, Mecarocci, S, Annicchiarico, MA, Rossi Fanelli, F 1999Plasma amino acid concentrations in patients with acute myelogenous leukemia.Nutrition15195199PubMedCrossRefGoogle Scholar
  109. Naganathan, PS, Venkatesan, K 1971The crystal and molecular structure of L-citrulline hydrochloride.Acta Cryst B271079Google Scholar
  110. Nair, KS 1995Muscle protein turnover: methodological issues and the effect of aging.J Gerontol A Biol Sci Med Sci50107112PubMedGoogle Scholar
  111. Nair, KS 2000Age-related changes in muscle.Mayo Clin Proc75S14S18PubMedGoogle Scholar
  112. Nakashima, K, Hagiwara, T, Ishigami, A, Nagata, S, Asaga, H, Kuramoto, M, Senshu, T, Yamada, M 1999Molecular characterization of peptidylarginine deiminase in HL-60 cells induced by retinoic acid and 1α, 25-dihydroxyvitamin D3.J Biol Chem2742778627792PubMedGoogle Scholar
  113. Neveux N, David P, Cynober L (2004) Measurement of amino acids concentrations in biological fluids and tissues using ion exchange chromatography. In: Cynober L (ed) Metabolic and therapeutic aspects of amino acids in clinical nutrition, chap 1, 2nd edn. CRC Press, Boca Raton, pp 17–28Google Scholar
  114. Nicholas, AP, Sambandam, T, Echols, JD, Tourtellotte, WW 2004Increased citrullinated glial fibrillary acidic protein in secondary progressive multiple sclerosis.J Comp Neurol473128136PubMedCrossRefGoogle Scholar
  115. Nieto, R, Cruz, F, Tejedor, JM, Baroso, G, Cerdán, S 1992Origin of the ammonia used for mitochondrial citrulline synthesis as revealed by 13C – 15N spin coupling patterns observed by 13C NMR.Biochimie74903911PubMedCrossRefGoogle Scholar
  116. Norris, KA, Schrimpf, JE, Flynn, JL, Morris, SM,Jr 1995Enhancement of macrophage microbicidal activity: supplemental arginine and citrulline augment nitric oxide production in murine peritoneal macrophages and promote intracellular killing of Trypanosoma cruzi.Infect Immun6327932796PubMedGoogle Scholar
  117. Noszál, B, Kassai-Tánczos, R 1991Microscopic acid-base equilibria of arginine.Talanta3814391444PubMedGoogle Scholar
  118. Oknin, VI, Fedotova, AV, Vein, AM 1999Use of citrulline malate (stimol) in patients with autonomic dystonia associated with arterial hypotension.Zh Nevrol Psikhiatr Im S S Korsakova993033PubMedGoogle Scholar
  119. OMIM (2000) Online Mendelian Inheritance in Man World Wide Web URL: http://www.ncbi.nlm.nih.gov/omim/. McKusick-Nathans Institute for Genetic Medicine, Johns Hopkins University (Baltimore, MD) and National Center for Biotechnology Information, National Library of Medicine (Bethesda, MD)Google Scholar
  120. Osowska, S, Moinard, C, Neveux, N, Loï, C, Cynober, L 2004Citrulline increases arginine pools and restores nitrogen balance after massive intestinal resection.Gut5317811786PubMedCrossRefGoogle Scholar
  121. Oyanagi, K, Sogawa, H, Minami, R, Nakao, T, Karube, K, Tsugawa, S 1981A new transport interaction of dibasic amino acids and citrulline in human kidney.Tohoku J Exp Med1345558PubMedCrossRefGoogle Scholar
  122. Pacy, PJ, Price, GM, Halliday, D, Quevedo, MR, Millward, DJ 1994Nitrogen homeostasis in man: the diurnal responses of protein synthesis and degradation and amino acid oxidation to diets with increasing protein intakes.Clin Sci (Lond)86103116Google Scholar
  123. Palmieri, L, Pardo, B, Lasorsa, FM, del Arco, A, Kobayashi, K, Iijima, M, Runswick, M, Walker, J, Saheki, T, Satrústegui, J, Ferdinando, P 2001Citrin and aralarl are Ca2+-stimulated aspartate/glutamate transporters in mitochondria.EMBO J2050605069PubMedGoogle Scholar
  124. Pappas, PA, Saudubray, JM, Tzakis, AG, Rabier, D, Carreno, MR, Gomez-Marin, O, Huijing, F, Gelman, B, Levi, DM, Nery, JR, Kato, T, Mittal, N, Nishida, S, Thompson, JF, Ruiz, P 2002Serum citrulline as a marker of acute cellular rejection for intestinal transplantation.Transplant Proc34915917PubMedCrossRefGoogle Scholar
  125. Pappas, PA, Tzakis, AG, Saudubray, JM, Gaynor, JJ, Carreno, MR, Huijing, F, Kleiner, G, Rabier, D, Kato, T, Levi, DM, Nishida, S, Gelman, B, Thompson, JF, Mittal, N, Ruiz, P 2004Trends in serum citrulline and acute rejection among recipients of small bowel transplants.Transplant Proc36345347PubMedGoogle Scholar
  126. Pasqualotto, BA, Hope, BT, Vincent, SR 1991Citrulline in the rat brain: Immunohistochemistry and coexistence with NADPH-diaphorase.Neurosci Lett128155160PubMedCrossRefGoogle Scholar
  127. Pendleton, LC, Goodwin, BL, Flam, BR, Solomonson, LP, Eichler, DC 2002Endothelial argininosuccinate synthase mRNA 5′-untranslated region diversity. Infrastructure for tissue-specific expression.J Biol Chem2772536325369PubMedCrossRefGoogle Scholar
  128. Perkins, DJ 1953A study of the effect of amino-acid structure on the stabilities of the complexes formed with metals of group II of the periodic classification.Biochem J55649652PubMedGoogle Scholar
  129. Perry (1982) In: Lajtha A (ed) Handbook of neurochemistry – Chemical and cellular architecture. Plenum Press, New YorkGoogle Scholar
  130. Perry, TL, Hansen, S 1969Technical pitfalls leading to errors in the quantitation of plasma amino acids.Clin Chim Acta255358PubMedCrossRefGoogle Scholar
  131. Peters, JA, Lin, SC, Berridge, BJJ, Cummings, JG, Chao, WR 1969Amino acids including aspartate and glutamine in plasma and urine of normal human subjects.Proc Soc Exp Biol Med131281288PubMedGoogle Scholar
  132. Plauth, M, Schneider, BH, Raible, A, Hartmann, F 1999Effects of vascular or luminal administration and of simultaneous glucose availability on glutamine utilization by isolated rat small intestine.Int J Colorectal Dis1495100PubMedGoogle Scholar
  133. Pliška, V, Schmidt, M, Fauchère, JL 1981Partition coefficients of amino acids and hydrophobic parameters of their side-chains as measured by thin-layer chromatography.J Chromatogr2167992Google Scholar
  134. Porter, RK 2000Mammalian mitochondrial inner membrane cationic and neutral amino acid carriers.Biochim Biophys Acta Bioenergetics1459356362Google Scholar
  135. Porter, RW, Modebe, MO, Stark, GR 1969Aspartate transcarbamylase. Kinetic studies of the catalytic subunit.J Biol Chem24418461859PubMedGoogle Scholar
  136. Pouchert CJ (1983) The Aldrich Library of NMR Spectra, 2nd edn. Aldrich Chemical Co., Milwaukee, Ref. 658BGoogle Scholar
  137. Rabier, D, Kamoun, P 1995Metabolism of citrulline in man.Amino Acids9299316CrossRefGoogle Scholar
  138. Raghavan, SAV, Dikshit, M 2001L-Citrulline mediated relaxation in the control and lipopolysaccharide-treated rat aortic rings.Eur J Pharmacol4316169PubMedCrossRefGoogle Scholar
  139. Rajantie, J, Simell, O, Rapola, J, Perheentupa, J 1980Lysinuric protein intolerance: a two-year trial of dietary supplementation therapy with citrulline and lysine.J Pediatr97927932PubMedGoogle Scholar
  140. Raushel, FM, Seiglie, JL 1983Kinetic mechanism of argininosuccinate synthetase.Arch Biochem Biophys225979985PubMedCrossRefGoogle Scholar
  141. Ray, EC, Avissar, NE, Sax, HC 2002Growth factor regulation of enterocyte nutrient transport during intestinal adaptation.Am J Surg183361371PubMedCrossRefGoogle Scholar
  142. Reichard, P 1957Ornithine carbamyl transferase from rat liver.Acta Chem Scand11523536Google Scholar
  143. Richmonds, CR, Boonyapisit, K, Kusner, LL, Kaminski, HJ 1999Nitric oxide synthase in aging rat skeletal muscle.Mech Ageing Dev109177189PubMedCrossRefGoogle Scholar
  144. Rogers, G, Winter, B, McLaughlan, C, Powell, B, Nesci, T 1997Peptidylarginine deiminase of the hair follicle: characterization, localization, and function in keratinizing tissues.J Invest Dermatol108700707PubMedCrossRefGoogle Scholar
  145. Rosbe, KW, Mims, JW, Prazma, J, Petrusz, P, Rose, A, Drake, AF 1996Immunohistochemical localization of nitric oxide synthase activity in upper respiratory epithelium.Laryngoscope10610751079PubMedGoogle Scholar
  146. Roubenoff, R, Castaneda, C 2001Sarcopenia-understanding the dynamics of aging muscle.JAMA28612301231PubMedCrossRefGoogle Scholar
  147. Ryall J, Nguyen M, Bendayan M, Shore GC (1985) Expression of nuclear genes encoding the urea cycle enzymes, carbamoyl-phosphate synthetase I and ornithine carbamoyl transferase, in rat liver and intestinal mucosa. Eur J Biochem 152: 287–292 [LR: 20031114; JID: 0107600; 0 (RNA, Messenger); 24937-83-5 (Poly A); 57-13-6 (Urea); 9007-49-2 (DNA); EC 2.1.3.3 (Ornithine Carbamoyltransferase); EC 6. (Ligases); EC 6.3.4.16 (Carbamoyl-Phosphate Synthase (Ammonia)); ppublish]Google Scholar
  148. Samitz, MH, Katz, S 1964The chemical reactions between chromium and skin.J Invest Dermatol343544Google Scholar
  149. Schmidlin, A, Fischer, S, Wiesinger, H 2000Transport of L-citrulline in neural cell cultures.Dev Neurosci22393398PubMedCrossRefGoogle Scholar
  150. Schuegraf, A, Ratner, S, Warner, RC 1960Free energy changes of the argininosuccinate synthetase reaction and of the hydrolysis of the inner pyrophosphate bond of adenosine triphosphate.J Biol Chem2353597PubMedGoogle Scholar
  151. Scriver, GR, Davies, E 1965Endogenous renal clearance rate of free amino acid in pre-pubertal children (Employing an accelerated procedure for elution chromatography of basic amino acids on ion exchange resin).Pediatrics36592598PubMedGoogle Scholar
  152. Shi, D, Morizono, H, Ha, Y, Aoyagi, M, Tuchman, M, Allewell, NM 19981.85 Å resolution crystal structure of human ornithine transcarbamoylase complexed with N-phosphonacetyl-L-ornithine. Catalytic mechanism and correlation with inherited deficiency.J Biol Chem2733424734254PubMedGoogle Scholar
  153. Shi, D, Morizono, H, Aoyagi, M, Tuchman, M, Allewell, NM 2000Crystal structure of human ornithine transcarbamylase complexed with carbamoyl phosphate and L-norvaline at 1.9 Å resolution.Proteins: Structure, Function, and Genetics39271277CrossRefGoogle Scholar
  154. Shi, D, Morizono, H, Yu, X, Tong, L, Allewell, NM, Tuchman, M 2001Crystallization and preliminary X-ray crystallographic studies of wild-type human ornithine transcarbamylase and two naturally occurring mutants at position 277.Acta Cryst D57719721CrossRefGoogle Scholar
  155. Shigesada, K, Tatibana, M 1971Enzymatic synthesis of acetylglutamate by mammalian liver preparations and its stimulation by arginine.Biochem Biophys Res Commun4411171124PubMedCrossRefGoogle Scholar
  156. Shigesada, K, Tatibana, M 1978N-Acetylglutamate synthetase from rat-liver mitochondria. Partial purification and catalytic properties.Eur J Biochem84285291PubMedCrossRefGoogle Scholar
  157. Siest, G, Vigneron, C, Palaszewski, D, Marchal, D 1968Étude du dosage de l’urée et de la citrulline en milieu protéique. Méthode manuelle et automatique à la diacétylmonoxime.Clin Chim Acta20373379PubMedCrossRefGoogle Scholar
  158. Silberstein, M, Lane, D, Dodd, S, Opeskin, K 2002Identification of a by-product of nitric oxide synthase activity in human acute brain injury with in vivo proton magnetic resonance spectroscopy.Am J Neuroradiol23389392PubMedGoogle Scholar
  159. Sridhar, B, Srinivasan, N, Dalhus, B, Rajaram, RK 2002L-Citrullinium perchlorate.Acta Cryst E58o1177o1179Google Scholar
  160. Steglich W, Fugmann B, Lang-Fugmann S (2000) Römpp encyclopedia of natural products. Thieme Medical Publishers, Stuttgart New YorkGoogle Scholar
  161. Stephens, J, Levy, R 1994Effects of valproate and citrulline on ammonium-induced encephalopathy.Epilepsia35164171PubMedGoogle Scholar
  162. Su, TS, Lin, LH 1990Analysis of a splice acceptor site mutation which produces multiple splicing abnormalities in the human argininosuccinate synthetase locus.J Biol Chem2651971619720PubMedGoogle Scholar
  163. Su, TS, Beaudet, AL, O’Brien, WE 1981Increased translatable messenger ribonucleic acid for argininosuccinate synthetase in canavanine-resistant human cells.Biochemistry2029562960PubMedCrossRefGoogle Scholar
  164. Sugawara, K, Yoshizawa, Y, Tzeng, S, Epstein, WL, Fukuyama, K 1998Colorimetric determination of citrulline residues in proteins.Anal Biochem2659296PubMedCrossRefGoogle Scholar
  165. Surh, LC, Beaudet, AL, O’Brien, WE 1991Molecular characterization of the murine argininosuccinate synthetase locus.Gene99181189PubMedCrossRefGoogle Scholar
  166. Suyan, KM, Sachan, NP, Shah, SK, Gupta, CM 1979Polarographic behaviour of CdII-L-citrulline system in aqueous DMF and DMSO.Indian J Chem A188182Google Scholar
  167. Suzuki, T, Yamaguchi, T, Imanari, M 197415N FT NMR spectra of amino acids in natural abundance. pH dependence of 15N chemical shifts for L-arginine.Tetrahedron Lett1518091812Google Scholar
  168. Takiguchi, M, Mori, M 1995Transcriptional regulation of genes for ornithine cycle enzymes.Biochem J312649659PubMedGoogle Scholar
  169. Takiguchi, M, Matsubasa, T, Amaya, Y, Mori, M 1989Evolutionary aspects of urea cycle enzyme genes.Bioessays10163166PubMedCrossRefGoogle Scholar
  170. Tesmer, JJ, Klem, TJ, Deras, ML, Davisson, VJ, Smith, JL 1996The crystal structure of GMP synthetase reveals a novel catalytic triad and is a structural paradigm for two enzyme families.Nat Struct Mol Biol37486CrossRefGoogle Scholar
  171. Tewari, YB, Kishore, N, Margolis, SA, Goldberg, RN, Shibatani, T 1993Thermochemistry of the Hydrolysis of L-arginine to (L-citrulline + ammonia) and of the hydrolysis of L-arginine to (L-ornithine + urea).J Chem Thermodyn25293305Google Scholar
  172. Toffoli, P, Rodier, N, Astoin, J 1986Structure cristalline de l’acide L-amino-2-uréido-5-pentanoïque dihydrate (L-citrulline dihydrate).Bull Soc Chim Fr1116123Google Scholar
  173. Toffoli, P, Khodada, P, Rodier, N, Astoin, J 1987Structure de l’acide L-amino-2 Uréido-5 Pentanoïque (L-Citrulline).Acta Cryst C43945947Google Scholar
  174. Toffoli, P, Rodier, N, Céolin, R, Lepage, F, Astoin, J 1988Composé moléculaire acide L-malique–Citrulline(1/1).Acta Cryst C4421282131Google Scholar
  175. Trikha, KC, Nair, BC, Singh, RP 1968Complexation of bivalent metal ions with aminoacids: Part I – L-Citrulline complexes.Indian J Chem6532533Google Scholar
  176. Tsao, TS, Burcelin, R, Charron, MJ 1996Regulation of hexokinase II gene expression by glucose flux in skeletal muscle.J Biol Chem2711495914963PubMedCrossRefGoogle Scholar
  177. Vadgama, JV, Evered, DF 1992Characteristics of L-citrulline transport across rat small intestine in vitro.Pediatr Res32472478PubMedGoogle Scholar
  178. Valentini, G, De Gregorio, A, Di Salvo, C, Grimm, R, Bellocco, E, Cuzzocrea, G, Iadarola, P 1996An essential lysine in the substrate-binding site of ornithine carbamoyltransferase.Eur J Biochem239397402PubMedCrossRefGoogle Scholar
  179. van de Poll, MCG, Soeters, PB, Deutz, NEP, Fearon, KCH, Dejong, CHC 2004Renal metabolism of amino acids: its role in interorgan amino acis exchange.Am J Clin Nutr79185197PubMedGoogle Scholar
  180. Vandervoort, AA, Symons, TB 2001Functional and metabolic consequences of sarcopenia.Can J Appl Physiol2690101Google Scholar
  181. Vanuxem, D, Duflot, JC, Prevot, H, Bernasconi, P, Blehaut, H, Fornaris, E, Vanuxem, P 1990Influence d’un anti-asthénique: le malate de citrulline, sur la cinétique de lactatémie et d’ammoniémie au cours d’une épreuve d’effort maximal chez des sujets sédentaires.Sem Hôp Paris66477481Google Scholar
  182. Viner, RI, Ferrington, DA, Williams, TD, Bigelow, DJ, Schöneich, C 1999Protein modification during biological aging: selective tyrosine nitration of the SERCA2a isoform of the sarcoplasmic reticulum Ca2+-ATPase in skeletal muscle.Biochem J340657669PubMedCrossRefGoogle Scholar
  183. Wakabayashi, Y, Yamada, E, Yoshida, T, Takahashi, H 1994Arginine becomes an essential amino acid after massive resection of rat small intestine.J Biol Chem2693266732671PubMedGoogle Scholar
  184. Wakabayashi, Y, Yamada, E, Yoshida, T, Takahashi, N 1995Effect of intestinal resection and arginine-free diet on rat physiology.Am J Physiol Gastrointest Liver Physiol269G313G318Google Scholar
  185. Wanagat, J, Cao, Z, Pathare, P, Aiken, JM 2001Mitochondrial DNA deletion mutations colocalize with segmental electron transport system abnormalities, muscle fiber atrophy, fiber splitting, and oxidative damage in sarcopenia.FASEB J15322332PubMedCrossRefGoogle Scholar
  186. Waugh WH (1998) Utilisation de L-citrulline en médecine orthomoléculaire pour la vasoprotection, le tonus relaxatif des muscles lisses et la protection cellulaires Brevet d’invention 9802433 Institut national de la propriété industrielle ParisGoogle Scholar
  187. Waugh, WH, Daeschner, CWR, Files, BA, McConnell, ME, Strandjord, SE 2001Oral citrulline as arginine precursor may be beneficial in sickle cell disease: early phase two results.J Natl Med Assoc90363371Google Scholar
  188. Wick, H, Brechbuhler, T, Girard, J 1970Citrullinemia: elevated serum citrulline levels in healthy siblings.Experientia70823824Google Scholar
  189. Wiesinger, H 2001Arginine metabolism and the synthesis of nitric oxide in the nervous system.Prog Neurobiol64365391PubMedCrossRefGoogle Scholar
  190. Wileman, SM, Mann, GE, Pearson, JD, Baydoun, AR 2003Role of L-citrulline transport in nitric oxide synthesis in rat aortic smooth muscle cells activated with LPS and interferon-γ.Br J Pharmacol140179185PubMedCrossRefGoogle Scholar
  191. Windmueller, HG, Spaeth, AE 1981Source and fate of circulating citrulline.Am J Physiol Endocrinol Metab241E473E480Google Scholar
  192. Wood, DD, Moscarello, MA 1989The isolation, characterization, and lipid-aggregating properties of a citrulline containing myelin basic protein.J Biol Chem26451215127PubMedGoogle Scholar
  193. Wu, G 1998Intestinal mucosal amino acid catabolism.J Nutr12812491252PubMedGoogle Scholar
  194. Wu, GY, Brosnan, JT 1992Macrophages can convert citrulline into arginine.Biochem J2814548PubMedGoogle Scholar
  195. Xianglin J, Zuohua P, Ronghan G, Qichen H, (1985) Huaxue Xuebao (Acta Chim Sinica) 43: 5. From CIF file dataGoogle Scholar
  196. Yamauchi, O, Takaba, T, Sakurai, T 1980Solution equilibria of histidine-containing ternary amino acid-copper(II) complexes in 20v/v% dioxane-water.Bull Chem Soc Jpn53106111Google Scholar
  197. Yu, YM, Burke, JF, Tompkins, RG, Martin, R, Young, VR 1996Quantitative aspects of interorgan relationships among arginine and citrulline metabolism.Am J Physiol Endocrinol Metab271E1098E1109Google Scholar
  198. Zhang, WZ, Kaye, DM 2004Simultaneous determination of arginine and seven metabolites in plasma by reversed-phase liquid chromatography with a time-controlled ortho-phthaldialdehyde precolumn derivatization.Anal Biochem3268792PubMedCrossRefGoogle Scholar
  199. Zheng, C, Lin, J 1998The role of L-arginine and L-citrulline in activated macrophage against Toxoplasma gondii infection in vitro.Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi16326330In chinese: abstract was usedPubMedGoogle Scholar
  200. Ziegler, F, Le Boucher, J, Coudray-Lucas, C, Cynober, L 1992Plasma amino acid determinations by reversed-phase HPLC: improvement of the orthophthalaldehyde method and comparison with ion exchange chromatography.J Automat Chem14145149PubMedGoogle Scholar

Copyright information

© Springer-Verlag/Wien 2005

Authors and Affiliations

  • E. Curis
    • 1
  • I. Nicolis
    • 1
  • C. Moinard
    • 2
  • S. Osowska
    • 2
  • N. Zerrouk
    • 3
  • S. Bénazeth
    • 1
  • L. Cynober
    • 2
    • 4
  1. 1.Laboratoire de Biomathématiques, E.A. 2498, Faculté de Pharmacie, Université René DescartesParisFrance
  2. 2.Laboratoire de Biologie de la Nutrition, E.A. 2498, Faculté de Pharmacie, Université René DescartesParisFrance
  3. 3.Laboratoire de Pharmacotechnie, E.A. 2498, Faculté de Pharmacie, Université René DescartesParisFrance
  4. 4.Laboratoire de Biochimie, Hôtel-Dieu, Assistance Publique – Hôpitaux de ParisParisFrance

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