L-Arginine and tetrahydrobiopterin supported nitric oxide production is crucial for the microbicidal activity of neutrophils

References

• Gabay JE. Microbicidal mechanisms of phagocytes. Curr Opin Immunol. 1988;1(1):36–40.
   PubMed Web of Science ®Google Scholar
• Smith JA. Neutrophils, host defense, and inflammation: a double-edged sword. J Leukoc Biol. 1994;56(6):672–686.
   PubMed Web of Science ®Google Scholar
• Crowley MT, Costello PS, Fitzer-Attas CJ, et al. A critical role for Syk in signal transduction and phagocytosis mediated by Fcgamma receptors on macrophages. J Exp Med. 1997;186(7):1027–1039.
   PubMed Web of Science ®Google Scholar
• Brinkmann V, Reichard U, Goosmann C, et al. Neutrophil extracellular traps kill bacteria. Science. 2004;303(5663):1532–1535.
   PubMed Web of Science ®Google Scholar
• Segal AW. How neutrophils kill microbes. Annu Rev Immunol. 2005;23:197–223.
   PubMed Web of Science ®Google Scholar
• Jackson SH, Gallin JI, Holland SM. The p47phox mouse knock-out model of chronic granulomatous disease. J Exp Med. 1995;182(3):751–758.
   PubMed Web of Science ®Google Scholar
• Pollock JD, Williams DA, Gifford MA, et al. Mouse model of X-linked chronic granulomatous disease, an inherited defect in phagocyte superoxide production. Nat Genet. 1995;9(2):202–209.
   PubMed Web of Science ®Google Scholar
• Mittal M, Siddiqui MR, Tran K, et al. Reactive oxygen species in inflammation and tissue injury. Antioxid Redox Signal. 2014;20(7):1126–1167.
   PubMed Web of Science ®Google Scholar
• Saini R, Patel S, Saluja R, et al. Nitric oxide synthase localization in the rat neutrophils: immunocytochemical, molecular, and biochemical studies. J Leukoc Biol. 2006;79(3):519–528.
   PubMed Web of Science ®Google Scholar
• Jyoti A, Singh AK, Dubey M, et al. Interaction of inducible nitric oxide synthase with rac2 regulates reactive oxygen and nitrogen species generation in the human neutrophil phagosomes: implication in microbial killing. Antioxid Redox Signal. 2014;20(3):417–431.
   PubMed Web of Science ®Google Scholar
• Diefenbach A, Schindler H, Röllinghoff M, et al. Requirement for type 2 NO synthase for IL-12 signaling in innate immunity. Science. 1999;284(5416):951–955.
   PubMed Web of Science ®Google Scholar
• Mannick JB, Hausladen A, Liu L, et al. Fas-induced caspase denitrosylation. Science. 1999;284(5414):651–654.
   PubMed Web of Science ®Google Scholar
• Hierholzer C, Harbrecht B, Menezes JM, et al. Essential role of induced nitric oxide in the initiation of the inflammatory response after hemorrhagic shock. J Exp Med. 1998;187(6):917–928.
   PubMed Web of Science ®Google Scholar
• Moldogazieva NT, Mokhosoev IM, Feldman NB, et al. ROS and RNS signalling: adaptive redox switches through oxidative/nitrosative protein modifications. Free Radic Res. 2018;52(5):507–543.
   PubMed Web of Science ®Google Scholar
• Moncada S, Palmer RM, Higgs EA. Biosynthesis of nitric oxide from L-arginine. A pathway for the regulation of cell function and communication. Biochem Pharmacol. 1989;38(11):1709–1715.
   PubMed Web of Science ®Google Scholar
• Alderton WK, Cooper CE, Knowles RG. Nitric oxide synthases: structure, function and inhibition. Biochem J. 2001;357(3):593–615.
   PubMedGoogle Scholar
• Malawista SE, Montgomery RR, van Blaricom G. Evidence for reactive nitrogen intermediates in killing of staphylococci by human neutrophil cytoplasts. A new microbicidal pathway for polymorphonuclear leukocytes. J Clin Invest. 1992;90(2):631–636.
   PubMed Web of Science ®Google Scholar
• Tümer C, Bilgin HM, Obay BD, et al. Effect of nitric oxide on phagocytic activity of lipopolysaccharide-induced macrophages: possible role of exogenous L-arginine. Cell Biol Int. 2007;31(6):565–569.
   PubMed Web of Science ®Google Scholar
• Crabtree MJ, Tatham AL, Hale AB, et al. Critical role for tetrahydrobiopterin recycling by dihydrofolate reductase in regulation of endothelial nitric-oxide synthase coupling: relative importance of the de novo biopterin synthesis versus salvage pathways. J Biol Chem. 2009;284(41):28128–28136.
   PubMed Web of Science ®Google Scholar
• Crabtree MJ, Channon KM. Synthesis and recycling of tetrahydrobiopterin in endothelial function and vascular disease. Nitric Oxide. 2011;25(2):81–88.
   PubMed Web of Science ®Google Scholar
• Bendall JK, Douglas G, McNeill E, et al. Tetrahydrobiopterin in cardiovascular health and disease. Antioxid Redox Signal. 2014;20(18):3040–3077.
   PubMed Web of Science ®Google Scholar
• Zhang W, Kuncewicz T, Yu ZY, et al. Protein–protein interactions involving inducible nitric oxide synthase. Acta Physiol Scand. 2003;179(2):137–142.
   PubMedGoogle Scholar
• Luo S, Wang T, Qin H, et al. Obligatory role of heat shock protein 90 in iNOS induction. Am J Physiol Cell Physiol. 2011;301(1):C227–C233.
   PubMed Web of Science ®Google Scholar
• Nagarkoti S, Dubey M, Awasthi D, et al. S-Glutathionylation of p47phox sustains superoxide generation in activated neutrophils. Biochim Biophys Acta. 2018;1865(2):444–454.
   Web of Science ®Google Scholar
• Nathan C. Inducible nitric oxide synthase: what difference does it make? J Clin Invest. 1997;100(10):2417–2423.
   PubMed Web of Science ®Google Scholar
• Bogdan C, Röllinghoff M, Diefenbach A. Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity. Curr Opin Immunol. 2000;12(1):64–76.
   PubMed Web of Science ®Google Scholar
• Shiloh MU, MacMicking JD, Nicholson S, et al. Phenotype of mice and macrophages deficient in both phagocyte oxidase and inducible nitric oxide synthase. Immunity. 1999;10(1):29–38.
   PubMed Web of Science ®Google Scholar
• Gozalo AS, Hoffmann VJ, Brinster LR, et al. Spontaneous Staphylococcus xylosus infection in mice deficient in NADPH oxidase and comparison with other laboratory mouse strains. J Am Assoc Lab Anim Sci. 2010;49(4):480–486.
   PubMed Web of Science ®Google Scholar
• Zhou X, Potoka DA, Boyle P, et al. Aminoguanidine renders inducible nitric oxide synthase knockout mice more susceptible to Salmonella typhimurium infection. FEMS Microbiol Lett. 2002;206(1):93–97.
   PubMed Web of Science ®Google Scholar
• Sethi S, Dikshit M. Modulation of polymorphonuclear leukocytes function by nitric oxide. Thromb Res. 2000;100(3):223–247.
   PubMed Web of Science ®Google Scholar
• Cowland JB, Borregaard N. Isolation of neutrophil precursors from bone marrow for biochemical and transcriptional analysis. J Immunol Methods. 1999;232(1–2):191–200.
   PubMed Web of Science ®Google Scholar
• Kumar S, Jyoti A, Keshari RS, et al. Functional and molecular characterization of NOS isoforms in rat neutrophil precursor cells. Cytometry A. 2010;77(5):467–477.
   PubMed Web of Science ®Google Scholar
• Chatterjee M, Saluja R, Kumar V, et al. Ascorbate sustains neutrophil NOS expression, catalysis, and oxidative burst. Free Radic Biol Med. 2008;45(8):1084–1093.
   PubMed Web of Science ®Google Scholar
• Cai S, Alp NJ, McDonald D, et al. GTP cyclohydrolase I gene transfer augments intracellular tetrahydrobiopterin in human endothelial cells: effects on nitric oxide synthase activity, protein levels and dimerisation. Cardiovasc Res. 2002;55(4):838–849.
   PubMed Web of Science ®Google Scholar
• Zhang WZ, Kaye DM. Simultaneous determination of arginine and seven metabolites in plasma by reversed-phase liquid chromatography with a time-controlled ortho-phthaldialdehyde precolumn derivatization. Anal Biochem. 2004;326(1):87–92.
   PubMed Web of Science ®Google Scholar
• Kobzik L, Godleski JJ, Brain JD. Selective down-regulation of alveolar macrophage oxidative response to opsonin-independent phagocytosis. J Immunol. 1990;144(11):4312–4319.
   PubMed Web of Science ®Google Scholar
• Jaiswal A, Reddy SS, Maurya M, et al. MicroRNA-99a mimics inhibit M1 macrophage phenotype and adipose tissue inflammation by targeting TNFα. Cell Mol Immunol. 2018. DOI:10.1038/s41423-018-0038-7.
   PubMed Web of Science ®Google Scholar
• Perskvist N, Roberg K, Kulyté A, et al. Rab5a GTPase regulates fusion between pathogen-containing phagosomes and cytoplasmic organelles in human neutrophils. J Cell Sci. 2002;115(6):1321–1330.
   PubMed Web of Science ®Google Scholar
• Shui W, Sheu L, Liu J, et al. Membrane proteomics of phagosomes suggests a connection to autophagy. Proc Natl Acad Sci USA. 2008;105(44):16952–16957.
   PubMed Web of Science ®Google Scholar
• Lehrer RI, Ganz T. Antimicrobial polypeptides of human neutrophils. Blood. 1990;76(11):2169–2181.
   PubMed Web of Science ®Google Scholar
• Hampton MB, Kettle AJ, Winterbourn CC. Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing. Blood. 1998;92(9):3007–3017.
   PubMed Web of Science ®Google Scholar
• Tsuji S, Iharada A, Taniuchi S, et al. Increased production of nitric oxide by phagocytic stimulated neutrophils in patients with chronic granulomatous disease. J Pediatr Hematol Oncol. 2012;34(7):500–502.
   PubMed Web of Science ®Google Scholar
• Tsuji S, Taniuchi S, Hasui M, et al. Increased nitric oxide production by neutrophils from patients with chronic granulomatous disease on trimethoprim-sulfamethoxazole. Nitric Oxide. 2002;7(4):283–288.
   PubMed Web of Science ®Google Scholar
• Roos D, Winterbourn CC. Immunology. Lethal weapons. Science. 2002;296(5568):669–671.
   PubMed Web of Science ®Google Scholar
• Malawista SE, Van Blaricom G, Cretella SB. Cytokineplasts from human blood polymorphonuclear leukocytes. Lack of oxidase activity and extended functional longevity. Inflammation. 1985;9(1):99–106.
   PubMed Web of Science ®Google Scholar
• Malawista SE, Van Blaricom G. Phagocytic capacity of cytokineplasts from human blood polymorphonuclear leukocytes. Blood Cells. 1986;12(1):167–177.
   PubMedGoogle Scholar
• Seth P, Kumari R, Dikshit M. Alterations in the free radical generation and nitric oxide release from rat peripheral polymorphonuclear leukocytes following thrombosis. Thromb Res. 1997;87(3):279–288.
   PubMed Web of Science ®Google Scholar
• Sethi S, Singh MP, Dikshit M. Nitric oxide-mediated augmentation of polymorphonuclear free radical generation after hypoxia-reoxygenation. Blood. 1999;93(1):333–340.
   PubMed Web of Science ®Google Scholar
• Kumar S, Patel S, Jyoti A, et al. Nitric oxide-mediated augmentation of neutrophil reactive oxygen and nitrogen species formation: critical use of probes. Cytometry A. 2010;77(11):1038–1048.
   PubMedGoogle Scholar
• Patel S, Kumar S, Jyoti A, et al. Nitric oxide donors release extracellular traps from human neutrophils by augmenting free radical generation. Nitric Oxide. 2010;22(3):226–234.
   PubMed Web of Science ®Google Scholar
• Keshari RS, Jyoti A, Kumar S, et al. Neutrophil extracellular traps contain mitochondrial as well as nuclear DNA and exhibit inflammatory potential. Cytometry A. 2012;81(3):238–247.
   PubMedGoogle Scholar
• Mayer B, John M, Heinzel B, et al. Brain nitric oxide synthase is a biopterin- and flavin-containing multi-functional oxido-reductase. FEBS Lett. 1991;288(1–2):187–191.
   PubMedGoogle Scholar
• Kwon NS, Nathan CF, Stuehr DJ. Reduced biopterin as a cofactor in the generation of nitrogen oxides by murine macrophages. J Biol Chem. 1989;264(34):20496–20501.
   PubMed Web of Science ®Google Scholar
• Yeo TW, Lampah DA, Kenangalem E, et al. Impaired systemic tetrahydrobiopterin bioavailability and increased dihydrobiopterin in adult falciparum malaria: association with disease severity, impaired microvascular function and increased endothelial activation. PLoS Pathog. 2015;11(3):e1004667.
   PubMed Web of Science ®Google Scholar
• Rubach MP, Mukemba J, Florence S, et al. Impaired systemic tetrahydrobiopterin bioavailability and increased oxidized biopterins in pediatric falciparum malaria: association with disease severity. PLoS Pathog. 2015;11(3):e1004655.
   PubMed Web of Science ®Google Scholar
• Yeo TW, Lampah DA, Tjitra E, et al. Increased asymmetric dimethylarginine in severe falciparum malaria: association with impaired nitric oxide bioavailability and fatal outcome. PLoS Pathog. 2010;6(4):e1000868.
   PubMed Web of Science ®Google Scholar
• Watters K, O’Dwyer TP, Rowley H. Cost and morbidity of MRSA in head and neck cancer patients: what are the consequences? J Laryngol Otol. 2004;118(9):694–699.
   PubMed Web of Science ®Google Scholar
• Hallemeesch MM, Lamers WH, Deutz NE. Reduced arginine availability and nitric oxide production. Clin Nutr. 2002;21(4):273–279.
   PubMed Web of Science ®Google Scholar
• Moffat FL, Han T, Li ZM, et al. Supplemental L-arginine HCl augments bacterial phagocytosis in human polymorphonuclear leukocytes. J Cell Physiol. 1996;168(1):26–33.
   PubMed Web of Science ®Google Scholar
• Xia Y, Roman LJ, Masters BS, et al. Inducible nitric-oxide synthase generates superoxide from the reductase domain. J Biol Chem. 1998;273(35):22635–22639.
   PubMed Web of Science ®Google Scholar
• Munder M, Mollinedo F, Calafat J, et al. Arginase I is constitutively expressed in human granulocytes and participates in fungicidal activity. Blood. 2005;105(6):2549–2556.
   PubMed Web of Science ®Google Scholar
• Luiking YC, Poeze M, Ramsay G, et al. The role of arginine in infection and sepsis. JPEN J Parenter Enter Nutr. 2005;29(1):S70–S74.
   PubMed Web of Science ®Google Scholar
• Wang YY, Shang HF, Lai YN, et al. Arginine supplementation enhances peritoneal macrophage phagocytic activity in rats with gut-derived sepsis. JPEN J Parenter Enter Nutr. 2003;27(4):235–240.
   PubMed Web of Science ®Google Scholar
• Cui XL, Iwasa M, Iwasa Y, et al. Arginine-supplemented diet decreases expression of inflammatory cytokines and improves survival in burned rats. JPEN J Parenter Enter Nutr. 2000;24(2):89–96.
   PubMed Web of Science ®Google Scholar
• Vinet AF, Descoteaux A. Large scale phagosome preparation. Methods Mol Biol. 2009;531:329–346.
   PubMedGoogle Scholar
• Jahraus A, Tjelle TE, Berg T, et al. In vitro fusion of phagosomes with different endocytic organelles from J774 macrophages. J Biol Chem. 1998;273(46):30379–30390.
   PubMed Web of Science ®Google Scholar
• Desjardins M, Griffiths G. Phagocytosis: latex leads the way. Curr Opin Cell Biol. 2003;15(4):498–503.
   PubMed Web of Science ®Google Scholar