Article information
Abstract
Nitric oxide (NO) is a free radical synthesized from L-arginine by different isoforms NO-synthases. NO possesses multiple and complex biological functions. NO is an important mediator of homeostasis, and changes in its generation or actions can contribute or not to pathological states. The knowledge of effects of NO has been not only important to our understanding of immune response, but also to new tools for research and treatment of various diseases. Knowing the importance of NO as inflammatory mediator in diverse infectious diseases, we decided to develop a revision that shows the participation/effect of this mediator in immune response induced against Giardia spp. Several studies already demonstrated the participation of NO with microbicidal and microbiostatic activity in giardiasis. On the other hand, some works report that Giardia spp. inhibit NO production by consuming the intermediate metabolite arginine. In fact, studies in vitro showed that G. lamblia infection of human intestinal epithelial cells had reduced NO production. This occurs due to limited offer of the crucial substrate arginine (essential aminoacid for NO production), consequently reducing NO production. Therefore, the balance between giardial arginine consumption and epithelial NO production could contribute to the variability of the duration and severity of infections by this ubiquitous parasite.
Keywords:
nitric oxide
immune system
giardiasis
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References
[1.]
R.F. Furchgott, J.V. Zawadzki.
The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine.
Nature, 288 (1980), pp. 373-376
[2.]
S. Moncada, M.W. Radomski, R.M. Palmer.
Endothelium-derived relaxing factor. Identification as nitric oxide and role in the control of vascular tone and platelet function.
Biochem Pharmacol, 37 (1988), pp. 2495-2501
[3.]
S. Moncada, R.M. Palmer, E.A. Higgs.
Nitric oxide: physiology, pathophysiology, and pharmacology.
Pharmacol Rev, 43 (1991), pp. 109-142
[4.]
J.R. Lancaster Jr.
Simulation of the diffusion and reaction of endogenously produced nitric oxide.
Proc Natl Acad Sci USA, 91 (1994), pp. 8137-8141
[5.]
C. Nathan, Q.W. Xie.
Regulation of biosynthesis of nitric oxide.
J Biol Chem, 269 (1994), pp. 13725-13728
[6.]
M. Regulski, T. Tully.
Molecular and biochemical characterization of dNOS: a Drosophila Ca2+/calmodulin-dependent nitric oxide synthase.
Proc Natl Acad Sci U S A, 92 (1995), pp. 9072-9076
[7.]
J.M. Ribeiro, J.M. Hazzard, R.H. Nussenzveig, et al.
Reversible binding of nitric oxide by a salivary heme protein from a bloodsucking insect.
Science, 260 (1993), pp. 539-541
[8.]
Y.J. Sung, J.H. Hotchkiss, R.E. Austic, R.R. Dietert.
L-arginine-dependent production of a reactive nitrogen intermediate by macrophages of a uricotelic species.
J Leukoc Biol, 50 (1991), pp. 49-56
[9.]
A.W. Lin, C.C. Chang, C.C. McCormick.
Molecular cloning and expression of an avian macrophage nitric-oxide synthase cDNA and the analysis of the genomic 5-flanking region.
J Biol Chem, 271 (1996), pp. 11911-11919
[10.]
B.I. Holmqvist, T. Ostholm, P. Alm, P. Ekstrom.
Nitric oxide synthase in the brain of a teleost.
Neurosci Lett, 171 (1994), pp. 205-208
[11.]
F.Y. Liew, X.Q. Wei, L. Proudfoot.
Cytokines and nitric oxide as effector molecules against parasitic infections.
Philos Trans R Soc Lond B Biol Sci, 352 (1997), pp. 1311-1315
[12.]
W.K. Alderton, C.E. Cooper, R.G. Knowles.
Nitric oxide synthases: structure, function and inhibition.
Biochem J, 357 (2001), pp. 593-615
[13.]
C. Nathan.
Nitric oxide as a secretory product of mammalian cells.
Faseb J, 6 (1992), pp. 3051-3064
[14.]
H.H. Schmidt, H. Hofmann, U. Schindler, et al.
NO from NO synthase.
Proc Natl Acad Sci USA, 93 (1996), pp. 14492-14497
[15.]
A. Barbul, D.A. Sisto, H.L. Wasserkrug, G. Efron.
Arginine stimulates lymphocyte immune response in healthy human beings.
Surgery, 90 (1981), pp. 244-251
[16.]
J.B. Ochoa, J. Strange, P. Kearney, et al.
Effects of L-arginine on the proliferation of T lymphocyte subpopulations.
JPEN J Parenter Enteral Nutr, 25 (2001), pp. 23-29
[17.]
S.M. Morris Jr., D. Kepka-Lenhart, L.C. Chen.
Differential regulation of arginases and inducible nitric oxide synthase in murine macrophage cells.
Am J Physiol, 275 (1998), pp. E740-E747
[18.]
H. Li, C.J. Meininger, J.R. Hawker Jr., T.E. Haynes, D. Kepka-Lenhart, S.K. Mistry, et al.
Regulatory role of arginase I and II in nitric oxide, polyamine, and proline syntheses in endothelial cells.
Am J Physiol Endocrinol Metab, 280 (2001), pp. E75-E82
[19.]
F. Taheri, J.B. Ochoa, Z. Faghiri, et al.
L-Arginine regulates the expression of the T-cell receptor zeta chain (CD3zeta) in Jurkat cells.
Clin Cancer Res, 7 (2001), pp. 958s-965s
[20.]
M. Munder, K. Eichmann, J.M. Moran, et al.
Th1/Th2-regulated expression of arginase isoforms in murine macrophages and dendritic cells.
J Immunol, 163 (1999), pp. 3771-3777
[21.]
W. Durante, F.K. Johnson, R.A. Johnson.
Arginase: a critical regulator of nitric oxide synthesis and vascular function.
Clin Exp Pharmacol Physiol, 34 (2007), pp. 906-911
[22.]
L. Kobzik, D.S. Bredt, C.J. Lowenstein, et al.
Nitric oxide synthase in human and rat lung: immunocytochemical and histochemical localization.
Am J Respir Cell Mol Biol, 9 (1993), pp. 371-377
[23.]
J.B. Hibbs Jr., R.R. Taintor, Z. Vavrin, E.M. Rachlin.
Nitric oxide: a cytotoxic activated macrophage effector molecule.
Biochem Biophys Res Commun, 157 (1988), pp. 87-94
[24.]
H.D. Brightbill, D.H. Libraty, S.R. Krutzik, et al.
Host defense mechanisms triggered by microbial lipoproteins through toll-like receptors.
Science, 285 (1999), pp. 732-736
[25.]
R.L. Tarleton.
Immune system recognition of Trypanosoma cruzi.
Curr Opin Immunol, 19 (2007), pp. 430-434
[26.]
J. Marks-Konczalik, S.C. Chu, J. Moss.
Cytokine-mediated transcriptional induction of the human inducible nitric oxide synthase gene requires both activator protein 1 and nuclear factor kappaB-binding sites.
J Biol Chem, 273 (1998), pp. 22201-22208
[27.]
M.G. Cifone, L. Cironi, M.A. Meccia, et al.
Role of nitric oxide in cell-mediated tumor cytotoxicity.
Adv Neuroimmunol, 5 (1995), pp. 443-461
[28.]
T. Utsumi, T. Mizuta, Y. Fujii, et al.
Nitric oxide production by bronchoalveolar cells during allograft rejection in the rat.
Transplantation, 67 (1999), pp. 1622-1626
[29.]
D.E. Heck, V.E. Kagan, A.A. Shvedova, J.D. Laskin.
An epigrammatic (abridged) recounting of the myriad tales of astonishing deeds and dire consequences pertaining to nitric oxide and reactive oxygen species in mitochondria with an ancillary missive concerning the origins of apoptosis.
Toxicology, 208 (2005), pp. 259-271
[30.]
J. Sun, C. Steenbergen, E. Murphy.
S-nitrosylation: NO-related redox signaling to protect against oxidative stress.
Antioxid Redox Signal, 8 (2006), pp. 1693-1705
[31.]
D.T. Hess, A. Matsumoto, R. Nudelman, J.S. Stamler.
S-nitrosylation: spectrum and specificity.
Nat Cell Biol, 3 (2001), pp. E46-E49
[32.]
D.T. Hess, A. Matsumoto, S.O. Kim, et al.
S-nitrosylation: purview and parameters.
Nat Rev Mol Cell Biol, 6 (2005), pp. 150-166
[33.]
G. Melino, F. Bernassola, R.A. Knight, et al.
S-nitrosylation regulates apoptosis.
Nature, 388 (1997), pp. 432-433
[34.]
L. Thomson, F.R. Gadelha, G. Peluffo, A.E. Vercesi, R. Radi.
Peroxynitrite affects Ca2+ transport in Trypanosoma cruzi.
Mol Biochem Parasitol, 98 (1999), pp. 81-91
[35.]
H. Rubbo, A. Denicola, R. Radi.
Peroxynitrite inactivates thiol-containing enzymes of Trypanosoma cruzi energetic metabolism and inhibits cell respiration.
Arch Biochem Biophys, 308 (1994), pp. 96-102
[36.]
P. Ascenzi, L. Salvati, M. Bolognesi, et al.
Inhibition of cysteine protease activity by NO-donors.
Curr Protein Pept Sci, 2 (2001), pp. 137-153
[37.]
J.H. McKerrow.
Development of cysteine protease inhibitors as chemotherapy for parasitic diseases: insights on safety, target validation, and mechanism of action.
Int J Parasitol, 29 (1999), pp. 833-837
[38.]
M.B. Rao, A.M. Tanksale, M.S. Ghatge, V.V. Deshpande.
Molecular and biotechnological aspects of microbial proteases.
Microbiol Mol Biol Rev, 62 (1998), pp. 597-635
[39.]
L. Liaudet, F.G. Soriano, C. Szabo.
Biology of nitric oxide signaling.
Crit Care Med, 28 (2000), pp. N37-N52
[40.]
A. Abulencia, J. Adelman, T. Affolder, et al.
Measurement of sigma Lambda b0/sigma B0 x B(Lambda b0-->Lambda c+pi-)/B(B0-- >D+pi-) in pp collisions at square root s=1.96 TeV.
Phys Rev Lett, 98 (2007), pp. 1220-1222
[41.]
C. Szabo, H. Ischiropoulos, R. Radi.
Peroxynitrite: biochemistry, pathophysiology and development of therapeutics.
Nat Rev Drug Discov, 6 (2007), pp. 662-680
[42.]
L.J. Marnett, J.N. Riggins, J.D. West.
Endogenous generation of reactive oxidants and electrophiles and their reactions with DNA and protein.
J Clin Invest, 111 (2003), pp. 583-593
[43.]
R.E. Bundy, N. Marczin, A.H. Chester, M. Yacoub.
A redox-based mechanism for nitric oxide-induced inhibition of DNA synthesis in human vascular smooth muscle cells.
Br J Pharmacol, 129 (2000), pp. 1513-1521
[44.]
Y.M. Kim, K. Son, S.J. Hong, et al.
Inhibition of protein synthesis by nitric oxide correlates with cytostatic activity: nitric oxide induces phosphorylation of initiation factor eIF-2 alpha.
Mol Med, 4 (1998), pp. 179-190
[45.]
K. Roxstrom-Lindquist, D. Palm, D. Reiner, et al.
Giardia immunity--an update.
Trends Parasitol, 22 (2006), pp. 26-31
[46.]
P.A. Flanagan.
Giardia diagnosis, clinical course and epidemiology. A review.
Epidemiol Infect, 109 (1992), pp. 1-22
[47.]
T.E. Nash, D.A. Herrington, G.A. Losonsky, M.M. Levine.
Experimental human infections with Giardia lamblia.
J Infect Dis, 156 (1987), pp. 974-984
[48.]
E. Li, P. Zhou, S.M. Singer.
Neuronal nitric oxide synthase is necessary for elimination of Giardia lamblia infections in mice.
J Immunol, 176 (2006), pp. 516-521
[49.]
Y.S. Andersen, F.D. Gillin, L. Eckmann.
Adaptive immunity-dependent intestinal hypermotility contributes to host defense against Giardia spp.
Infection and Immunity, 74 (2006), pp. 2473-2476
[50.]
G. Faubert.
Immune response to Giardia duodenalis.
Clin Microbiol Rev, 13 (2000), pp. 35-54
[52.]
F.C. Fang.
Perspectives series: host/pathogen interactions. Mechanisms of nitric oxide-related antimicrobial activity.
J Clin Invest, 99 (1997), pp. 2818-2825
[53.]
C. Nathan, M.U. Shiloh.
Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens.
Proc Natl Acad Sci U S A, 97 (2000), pp. 8841-8848
[54.]
M.A. De Groote, F.C. Fang.
NO inhibitions: antimicrobial properties of nitric oxide.
Clin Infect Dis, 21 (1995), pp. S162-S165
[55.]
H.W. Murray, C.F. Nathan.
Macrophage microbicidal mechanisms in vivo: reactive nitrogen versus oxygen intermediates in the killing of intracellular visceral Leishmania donovani.
J Exp Med, 189 (1999), pp. 741-746
[56.]
S. Stenger, N. Donhauser, H. Thuring, M. Rollinghoff, C. Bogdan.
Reactivation of latent leishmaniasis by inhibition of inducible nitric oxide synthase.
J Exp Med, 183 (1996), pp. 1501-1514
[57.]
L.B. Adams, J.B. Hibbs Jr., R.R. Taintor, J.L. Krahenbuhl.
Microbiostatic effect of murine-activated macrophages for Toxoplasma gondii. Role for synthesis of inorganic nitrogen oxides from L-arginine.
J Immunol, 144 (1990), pp. 2725-2729
[58.]
L.R. Brunet.
Nitric oxide in parasitic infections.
Int Immunopharmacol, 1 (2001), pp. 1457-1467
[59.]
S.L. James.
Role of nitric oxide in parasitic infections.
Microbiol Rev, 59 (1995), pp. 533-547
[60.]
T.A. Wynn, I.P. Oswald, I.A. Eltoum, et al.
Elevated expression of Th1 cytokines and nitric oxide synthase in the lungs of vaccinated mice after challenge infection with Schistosoma mansoni.
J Immunol, 153 (1994), pp. 5200-5209
[61.]
C.F. Nathan, J.B. Hibbs Jr..
Role of nitric oxide synthesis in macrophage antimicrobial activity.
Curr Opin Immunol, 3 (1991), pp. 65-70
[62.]
C. Nathan, Q.W. Xie.
Nitric oxide synthases: roles, tolls, and controls.
Cell, 78 (1994), pp. 915-918
[63.]
G.N. Vespa, F.Q. Cunha, J.S. Silva.
Nitric oxide is involved in control of Trypanosoma cruzi-induced parasitemia and directly kills the parasite in vitro.
Infect Immun, 62 (1994), pp. 5177-5182
[64.]
J.S. Silva, F.S. Machado, G.A. Martins.
The role of nitric oxide in the pathogenesis of Chagas disease.
Front Biosci, 8 (2003), pp. s314-s325
[65.]
D. Chakravortty, M. Hensel.
Inducible nitric oxide synthase and control of intracellular bacterial pathogens.
Microbes Infect, 5 (2003), pp. 621-627
[66.]
I.A. Clark, K.A. Rockett.
Nitric oxide and parasitic disease.
Adv Parasitol, 37 (1996), pp. 1-56
[67.]
P. Chaves Mdel, J.A. Fernandez, I. Ospina, et al.
Giardia duodenalis prevalence and associated risk factors in preschool and school-age children of rural Colombia.
Biomedica, 27 (2007), pp. 345-351
[68.]
L. Eckmann, F. Laurent, T.D. Langford, et al.
Nitric oxide production by human intestinal epithelial cells and competition for arginine as potential determinants of host defense against the lumen-dwelling pathogen Giardia lamblia.
J Immunol, 164 (2000), pp. 1478-1487
[69.]
A.T. Islam, A. Kuraoka, M. Kawabuchi.
Morphological basis of nitric oxide production and its correlation with the polysialylated precursor cells in the dentate gyrus of the adult guinea pig hippocampus.
Anat Sci Int, 78 (2003), pp. 98-103
[70.]
R.A. Hoffman, J.M. Langrehr, K.E. Dull, R.L. Simmons.
Nitric oxide production by mouse sponge matrix allograft-infiltrating cells. Comparison with the rat species.
Transplantation, 55 (1993), pp. 591-596
[71.]
P.D. Fernandes, J. Assreuy.
Role of nitric oxide and superoxide in Giardia lamblia killing.
Braz J Med Biol Res, 30 (1997), pp. 93-99
[72.]
H.G. Morrison, A.G. McArthur, F.D. Gillin, et al.
Genomic minimalism in the early diverging intestinal parasite Giardia lamblia.
Science, 317 (2007), pp. 1921-1926
[73.]
D.M. Brown, J.A. Upcroft, P. Upcroft.
Free radical detoxification in Giardia duodenalis.
Mol Biochem Parasitol, 72 (1995), pp. 47-56
[74.]
E. Ringqvist, J.E. Palm, H. Skarin, et al.
Release of metabolic enzymes by Giardia in response to interaction with intestinal epithelial cells.
Mol Biochem Parasitol, 159 (2008), pp. 85-91
[75.]
G. Oberhuber, N. Kastner, M. Stolte.
Giardiasis: a histologic analysis of 567 cases.
Scandinavian Journal of Gastroenterology, 32 (1997), pp. 48
[76.]
S.M. Singer, T.E. Nash.
T-cell-dependent control of acute Giardia lamblia infections in mice.
Infection and Immunity, 68 (2000), pp. 170
[77.]
T.D. Langford, M.P. Housley, Boes, et al.
Central importance of immunoglobulin A in host defense against Giardia spp.
Infection and Immunity, 70 (2002), pp. 11
[78.]
C.W. Daniels, M. Belosevic.
Serum antibody responses by male and female C57BL / 6 mice infected with Giardia muris.
Clinical and Experimental Immunology, 97 (1994), pp. 424
[79.]
S. Char, N. Shetty, M. Narasimha.
Serum antobidy response in children with Giardia lamblia and infection of an immunodominant 57-kilodalton antigen.
Parasite Immunol, 13 (1991), pp. 329-337
[80.]
S. Char, A.M. Cevallo, P. Yamson.
Impaired IgA response to Giardia heat-shock antigen in children with persistent diarrhoea and giardiasis.
Gut, 34 (1993), pp. 38-40
[81.]
K. Djamiatun, G.M. Faubert.
Exogenous cytokines released by spleen and Peyer's patch cells removed from mice infected with Giardia muris.
Parasite Immunol, 20 (1998), pp. 27-36
[82.]
M.S. Mahmoud, A.A. Salem, M.M. Rifaat.
Human giardiasis as an etiology of skin allergy: the role of adhesion molecules and interleukin-6.
J Egypt Soc Parasitol, 34 (2004), pp. 723-737
[83.]
M.R. Bayraktar, N. Mehmetb, R. Durmaza.
Serum cytokine changes in Turkish children infected with Giardia lamblia with and without allergy: Effect of metronidazole treatment.
Acta Tropica, 95 (2005), pp. 116-122
[84.]
E. Sonoda, R. Matsumoto, Y. Hitoshi, et al.
Transforming growth factorb induces IgA production and acts additively with interleukin 5 for IgA production.
Journal of Experimental Medicine, 170 (1989), pp. 1415-1423
[85.]
R.L. Coffman, D.A. Lebman, B. Shrader.
Transforming growth factor-b specifically enhances IgA production by lipopolysaccharide-stimulated murine B lymphocytes.
Journal of Experimental Medicine, 170 (1998), pp. 1039-1047
[86.]
H. Taherkhani, M. Hajilooi, M. Fallah, et al.
Gene polymorphism in transforming growth factor-beta codon 10 is associated with susceptibility to Giardiasis.
Int J Immunogenet, 36 (2009), pp. 345-349
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