The end of the road for the tryptophan depletion concept in pregnancy and infection

Clinical Science

Volumn 130, Issue 15, 2016, Pages 1327-1333

  Badawy, Abdulla A B ^a   Namboodiri, Aryan M A ^b   Moffett, John R ^b  

^a CARDIFF METROPOLITAN UNIVERSITY   (United Kingdom)

^b UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

Author keywords

Immunosuppression; Kynurenine metabolites; Plasma free tryptophan; Tryptophan utilization concept

Indexed keywords

KYNURENINE; TRYPTOPHAN; INDOLEAMINE 2,3 DIOXYGENASE; NICOTINAMIDE ADENINE DINUCLEOTIDE; PROTEIN BINDING; TRYPTOPHAN 2,3 DIOXYGENASE;

AMINO ACID METABOLISM; AMINO ACID TRANSPORT; ARTICLE; CATABOLISM; HUMAN; IMMUNE DEFICIENCY; INFECTION; METABOLITE; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROTEIN DEPLETION; ANTIGEN PRESENTING CELL; BLOOD; COMMUNICABLE DISEASE; DEFICIENCY; FEMALE; FETUS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; METABOLISM; OXIDATIVE STRESS; PREGNANCY COMPLICATION; T LYMPHOCYTE;

ANTIGEN-PRESENTING CELLS; COMMUNICABLE DISEASES; FEMALE; FETUS; HUMANS; IMMUNE TOLERANCE; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; KYNURENINE; NAD; OXIDATIVE STRESS; PREGNANCY; PREGNANCY COMPLICATIONS; PROTEIN BINDING; T-LYMPHOCYTES; TRYPTOPHAN; TRYPTOPHAN OXYGENASE;

EID: 84996780872     PISSN: 01435221     EISSN: 14708736     Source Type: Journal    
DOI: 10.1042/CS20160153     Document Type: Article

References (59)

1. Murray, H.W., Szuro-Sudol, A., Wellner, D., Oca, M.J., Granger, A.M., Libby, D.M., Rothermel, C.D. and Rubin, B.Y. (1989) Role of tryptophan degradation in respiratory burst-independent antimicrobial activity of gamma interferon-stimulated human macrophages. Infect. Immun. 57, 845-849.
2. Pfefferkorn, E.R., Eckel, M. and Rebhun, S. (1986) Interferon-gamma suppresses the growth of Toxoplasma gondii in human fibroblasts through starvation for tryptophan. Mol. Biochem. Parasitol. 20, 215-224.
3. Taylor, M.W. and Feng, G.S. (1991) Relationship between interferon-gamma, indoleamine 2,3-dioxygenase, and tryptophan catabolism. FASEB J. 5, 2516-2522.
4. Munn, D.H., Zhou, M., Attwood, J.T., Bondarev, I., Conway, S.J., Marshall, B., Brown, C. and Mellor, A.L. (1998) Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 281, 1191-1193.
5. Yeung, A. W., Terentis, A.C., King, N.J. and Thomas, S.R. (2015) Role of indoleamine 2,3-dioxygenase in health and disease. Clin. Sci. 129, 601-672.
6. Moffett, J.R. and Namboodiri, M.A. (2003) Tryptophan and the immune response. Immunol. Cell Biol. 81, 247-265.
7. Badawy, A.A.-B. (2014) The tryptophan utilization concept in pregnancy. Obstet. Gynecol. Sci. 57, 249-259.
8. Badawy, A.A.-B. (2015) Tryptophan metabolism, disposition and utilisation in pregnancy. Biosci. Rep. 35, e00261.
9. Sedlmayr, P., Blaschitz, A. and Stocker, R. (2014) The role of placental tryptophan catabolism. Front. Immunol. 5, article 230.
10. Varesio, L., Clayton, M., Blasi, E., Ruffman, R. and Radzioch, D. (1990) Picolinic acid, a catabolite of tryptophan, as the second signal in the activation of IFN-gamma-primed macrophages. J. Immunol. 145, 4265-4271.
11. Melillo, G., Cox, G.W., Radzioch, D. and Varesio, L. (1993) Picolinic acid, a catabolite of L-tryptophan, is a costimulus for the induction of reactive nitrogen intermediate production in murine macrophages. J. Immunol. 150, 4031-4040.
12. Moffett, J.R., Espey, M.G., Gaudet, S.J. and Namboodiri, M.A. (1993) Antibodies to quinolinic acid reveal localization in select immune cells rather than neurons or astroglia. Brain Res. 623, 337-340.
13. Moffett, J.R., Espey, M.G., Saito, K. and Namboodiri, M.A. (1994) Quinolinic acid immunoreactivity in cells within the choroid plexus, leptomeninges and brain vasculature of the immune stimulated gerbil. J. Neuroimmunol. 54, 69-73.
14. Moffett, J.R., Espey, M.G. and Namboodiri, M.A. (1994) Antibodies to quinolinic acid and the determination of its cellular distribution within the rat immune system. Cell Tissue Res. 278, 461-469.
15. Espey, M.G., Tang, Y., Morse, 3rd, H.C., Moffett, J.R. and Namboodiri, M.A. (1996) Localization of quinolinic acid in the murine AIDS model of retrovirus-induced immunodeficiency: implications for neurotoxicity and dendritic cell immunopathogenesis. AIDS 10, 151-158.
16. Namboodiri, M.A., Venkateshan, C.N., Narayanan, R., Blinder, K., Moffett, J.R., Gajdusek, D.C., Gravell, M. and Gibbs, Jr, C.J. (1996) Increased quinolinate immunoreactivity in the peripheral blood monocytes/macrophages from SIV-infected monkeys. J. Neurovirol. 2, 433-438.
17. Venkateshan, C.N., Narayanan, R., Espey, M.G., Moffett, J.R., Gajdusek, D.C., Gibbs, C.J. and Namboodiri, M.A. (1996) Immunocytochemical localization of the endogenous neuroexcitotoxin quinolinate in human peripheral blood monocytes/macrophages and the effect of human T-cell lymphotropic virus type I infection. Proc. Natl. Acad. Sci. U.S.A. 93, 1636-1641.
18. Sekkai, D., Guittet, O., Lemaire, G., Tenu, J.P. and Lepoivre, M. (1997) Inhibition of nitric oxide synthase expression and activity in macrophages by 3-hydroxyanthranilic acid, a tryptophan metabolite. Arch. Biochem. Biophys. 340, 117-123.
19. Hayaishi, O. (1993) My life with tryptophan-never a dull moment. Protein Sci. 2, 472-475.
20. Moffett, J.R., Els, T., Espey, M.G., Walter, S.A., Streit, W.J. and Namboodiri, M.A. (1997) Quinolinate immunoreactivity in experimental rat brain tumors is present in macrophages but not in astrocytes. Exp. Neurol. 144, 287-301.
21. Moffett, J.R., Blinder, K.L., Venkateshan, C.N. and Namboodiri, M.A. (1998) Differential effects of kynurenine and tryptophan treatment on quinolinate immunoreactivity in rat lymphoid and non-lymphoid organs. Cell Tissue Res. 293, 525-534.
22. Terness, P., Bauer, T.M., Rose, L., Dufter, C., Watzlik, A., Simon, H. and Opelz, G. (2002) Inhibition of allogeneic T cell proliferation by indoleamine 2,3-dioxygenase-expressing dendritic cells: mediation of suppression by tryptophan metabolites. J. Exp. Med. 196, 447-457.
23. Fallarino, F., Grohmann, U., Vacca, C., Bianchi, R., Orabona, C., Spreca, A., Fioretti, M.C. and Puccetti, P. (2002) T cell apoptosis by tryptophan catabolism. Cell Death Differ. 9, 1069-1077.
24. Clark, C.J., Mackay, G.M., Smythe, G.A., Bustamante, S., Stone, T.W. and Phillips, R.S. (2005) Prolonged survival of a murine model of cerebral malaria by kynurenine pathway inhibition. Infect. Immun. 73, 5249-5251.
25. Von Bubnoff, D., Matz, H., Frahnert, C., Rao, M.L., Hanau, D., de la, S.H. and Bieber, T. (2002) FcepsilonRI induces the tryptophan degradation pathway involved in regulating T cell responses. J. Immunol. 169, 1810-1816.
26. Wirthgen, E. and Hoeflich, A. (2015) Endotoxin-induced tryptophan degradation along the kynurenine pathway: the role of indolamine 2,3-dioxygenase and aryl hydrocarbon receptor-mediated immunosuppressive effects in endotoxin tolerance and cancer and its implications for immunoparalysis. J. Amino Acids 2015, 973548.
27. Efimov, I., Basran, J., Sun, X., Chauhan, N., Chapman, S.K., Mowat, C.G. and Raven, E.L. (2012) The mechanism of substrate inhibition in human indoleamine 2,3-dioxygenase. J. Am. Chem. Soc. 134, 3034-3041.
28. Kanai, M., Funakoshi, H., Takahashi, H., Hayakawa, T., Mizuno, S., Matsumoto, K. and Nakamura, T. (2009) Tryptophan 2,3-dioxygenase is a key modulator of physiological neurogenesis and anxiety-related behavior in mice. Mol. Brain 2,8.
29. Santillan, M.K., Pelham, C.J., Ketsawatsomkron, P., Santillan, D.A., Davis, D.R., Devor, E.J., Gibson-Corley, K.N., Scroggins, S.M., Grobe, J.L., Yang, B. et al. (2015) Pregnant mice lacking indoleamine 2,3-dioxygenase exhibit preeclampsia phenotypes. Physiol. Rep. 3, e12257.
30. Espey, M.G., Moffett, J.R. and Namboodiri, M.A. (1995) Temporal and spatial changes of quinolinic acid immunoreactivity in the immune system of lipopolysaccharide-stimulated mice. J. Leukoc. Biol. 57, 199-206.
31. Yoshida, R., Oku, T., Imanishi, J., Kishida, T. and Hayaishi, O. (1986) Interferon: a mediator of indoleamine 2,3-dioxygenase induction by lipopolysaccharide, poly(I) X poly(C), and pokeweed mitogen in mouse lung. Arch. Biochem. Biophys. 249, 596-604.
32. el-Azhary, R. and Mannering, G.J. (1979) Effects of interferon inducing agents (polyriboinosinic acid. Polyribocytidylic acid, tilorone) on hepatic hemoproteins (cytochrome P-450, catalase, tryptophan 2,3-dioxygenase, mitochondrial cytochromes), heme metabolism and cytochrome P-450-linked monooxygenase systems. Mol. Pharmacol. 15, 698-707.
33. Rizzardini, M., Carelli, M., Cabello Porras, M.R. and Cantoni, L. (1994) Mechanisms of endotoxin-induced haem oxygenase mRNA accumulation in mouse liver: synergism by glutathione depletion and protection by N-acetylcysteine. Biochem. J. 304, 477-483.
34. Berry, L.J. and Smythe, D.S. (1964) Effects of bacterial endotoxins on metabolism. VII. Enzyme induction and cortisone protection. J. Exp. Med. 120, 721-732.
35. Badawy, A.A.-B. and Morgan, C.J. (1982) Tryptophan and tryptophan pyrrolase in haem regulation. The role of lipolysis and direct displacement of serum-protein-bound tryptophan in the opposite effects of administration of endotoxin, morphine, palmitate, salicylate and theophylline on rat liver 5-aminolaevulinate synthase activity and the haem saturation of tryptophan pyrrolase. Biochem. J. 206, 451-460.
36. Moon, R.J. (1971) Tryptophan oxygenase and tryptophan metabolism in endotoxin-poisoned and allopurinol-treated mice. Biochim. Biophys. Acta 230, 342-348.
37. Farshtchi, D. and Lewis, V.J. (1968) Effects of three bacterial infections on serum lipids of rabbits. J. Bacteriol. 95, 1615-1621.
38. Cui, L., Lee, Y.H., Kumar, Y., Xu, F., Lu, K., Ooi, E.E., Tannenbaum, S.R. and Ong, C.N. (2013) Serum metabolome and lipidome changes in adult patients with primary dengue infection. PLoS Negl. Trop. Dis. 7, e2373.
39. Dusingize, J.C., Hoover, D.R., Shi, Q., Mutimura, E., Kiefer, E., Cohen, M. and Anastos, K. (2012) Association of serum albumin with markers of nutritional status among HIV-infected and uninfected Rwandan women. PLoS One 7, e35079.
40. Cangiano, C., Cascino, A., Ceci, F., Laviano, A., Mulieri, M., Muscaritoli, M. and Rossi-Fanelli, F. (1990) Plasma and CSF tryptophan in cancer anorexia. J. Neural Transm. Gen. Sect. 81, 225-233.
41. Iguchi, T., Takasugi, N., Nishimura, N. and Kusunoki, S. (1989) Correlation between mammary tumor and blood glucose, serum insulin, and free fatty acids in mice. Cancer Res. 49, 821-825.
42. Seve, P., Ray-Coquard, I., Trillet-Lenoir, V., Sawyer, M., Hanson, J., Broussolle, C., Negrier, S., Dumontet, C. and Mackey, J.R. (2006) Low serum albumin levels and liver metastasis are powerful prognostic markers for survival in patients with carcinomas of unknown primary site. Cancer 107, 2698-2705.
43. Mehraj, V. and Routy, J.P. (2015) Tryptophan catabolism in chronic viral infections: handling uninvited guests. Int. J. Tryptophan Res. 8, 41-48.
44. Sarsero, J.P., Merino, E. and Yanofsky, C. (2000) A Bacillus subtilis operon containing genes of unknown function senses tRNATrp charging and regulates expression of the genes of tryptophan biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 97, 2656-2661.
45. Bonner, C.A., Byrne, G.I. and Jensen, R.A. (2014) Chlamydia exploit the mammalian tryptophan-depletion defense strategy as a counter-defensive cue to trigger a survival state of persistence. Front. Cell. Infect. Microbiol. 4, 17.
46. Lo, C.C., Xie, G., Bonner, C.A. and Jensen, R.A. (2012) The alternative translational profile that underlies the immune-evasive state of persistence in Chlamydiaceae exploits differential tryptophan contents of the protein repertoire. Microbiol. Mol. Biol. Rev. 76, 405-443.
47. Hogan, R.J., Mathews, S.A., Mukhopadhyay, S., Summersgill, J.T. and Timms, P. (2004) Chlamydial persistence: beyond the biphasic paradigm. Infect. Immun. 72, 1843-1855.
48. Beatty, W.L., Morrison, R.P. and Byrne, G.I. (1994) Persistent chlamydiae: from cell culture to a paradigm for chlamydial pathogenesis. Microbiol. Rev. 58, 686-699.
49. Pfefferkorn, E.R. (1984) Interferon gamma blocks the growth of Toxoplasma gondii in human fibroblasts by inducing the host cells to degrade tryptophan. Proc. Natl. Acad. Sci. U.S.A. 81, 908-912.
50. Sanni, L.A., Thomas, S.R., Tattam, B.N., Moore, D.E., Chaudhri, G., Stocker, R. and Hunt, N.H. (1998) Dramatic changes in oxidative tryptophan metabolism along the kynurenine pathway in experimental cerebral and noncerebral malaria. Am. J. Pathol. 152, 611-619.
51. Fujigaki, S., Saito, K., Takemura, M., Maekawa, N., Yamada, Y., Wada, H. and Seishima, M. (2002) L-tryptophan-L-kynurenine pathway metabolism accelerated by Toxoplasma gondii infection is abolished in gamma interferon-gene-deficient mice: cross-regulation between inducible nitric oxide synthase and indoleamine-2,3-dioxygenase. Infect. Immun. 70, 779-786.
52. Kudo, Y. and Boyd, C.A. (2001) The role of L-tryptophan transport in L-tryptophan degradation by indoleamine 2,3-dioxygenase in human placental explants. J. Physiol. 531, 417-423.
53. Opitz, C.A., Litzenburger, U.M., Opitz, U., Sahm, F., Ochs, K., Lutz, C., Wick, W. and Platten, M. (2011) The indoleamine-2,3-dioxygenase (IDO) inhibitor 1-methyl-D-tryptophan upregulates IDO1 in human cancer cells. PLoS One 6, e19823.
54. Badawy, A.A.-B. (2010) Plasma free tryptophan revisited: what you need to know and do before measuring it. J. Psychopharmacol. 24, 809-815.
55. Desjardins-Proulx, P., White, E.P., Adamson, J.J., Ram, K., Poisot, T. and Gravel, D. (2013) The case for open preprints in biology. PLoS One Biol. 11, e1001563.
56. Fallarino, F., Grohmann, U. and Puccetti, P. (2012) Indoleamine 2,3-dioxygenase: from catalyst to signaling function. Eur. J. Immunol. 42, 1932-1937.
57. Bessede, A., Gargaro, M., Pallotta, M.T., Matino, D., Servillo, G., Brunacci, C., Bicciato, S., Mazza, E.M., Macchiarulo, A., Vacca, C. et al. (2014) Aryl hydrocarbon receptor control of a disease tolerance defence pathway. Nature 511, 184-190.
58. Mole, D.J., Webster, S.P., Uings, I., Zheng, X., Binnie, M., Wilson, K., Hutchinson, J.P., Mirguet, O., Walker, A., Beaufils, B. et al. (2016) Kynurenine-3-monooxygenase inhibition prevents multiple organ failure in rodent models of acute pancreatitis. Nat. Med. 22, 202-209.
59. Liu, H., Huang, L., Bradley, J., Liu, K., Bardhan, K., Ron, D., Mellor, A.L., Munn, D.H. and McGaha, T.L. (2014) GCN2-dependent metabolic stress is essential for endotoxemic cytokine induction and pathology. Mol. Cell. Biol. 34, 428-438.