Lower Expression of Inducible Nitric Oxide Synthase and Higher Expression of Arginase in Rat Alveolar Macrophages Are Linked to Their Susceptibility to Toxoplasma gondii Infection

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Zhao, Zhi Jun ^a,b   Zhang, Jia ^a   Wei, Jun ^b   Li, Zhi ^a   Wang, Tao ^a   Yi, Si Qi ^a   Shen, Ji Long ^c   Yang, Ting Bao ^a   Hide, Geoff ^d   Lun, Zhao Rong ^a,d  

^a SUN YAT SEN UNIVERSITY   (China)

^b NINGXIA MEDICAL UNIVERSITY   (China)

^c ANHUI MEDICAL UNIVERSITY   (China)

^d UNIVERSITY OF SALFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINASE 1; INDUCIBLE NITRIC OXIDE SYNTHASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; IN VITRO STUDY; IN VIVO STUDY; INFECTION RESISTANCE; INFECTION SENSITIVITY; LUNG ALVEOLUS MACROPHAGE; MOUSE; NONHUMAN; PARASITE VIRULENCE; PERITONEUM MACROPHAGE; PROTEIN EXPRESSION; RAT; TOXOPLASMA GONDII; TOXOPLASMOSIS;

ANIMALS; ARGINASE; DISEASE SUSCEPTIBILITY; MACROPHAGES, ALVEOLAR; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; RATS; TOXOPLASMA; TOXOPLASMOSIS;

EID: 84877728078     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0063650     Document Type: Article

References (87)

1. Montoya JG, Liesenfeld O, (2004) Toxoplasmosis. Lancet 363: 1965-1976.
2. Ruskin J, Remington JS, (1976) Toxoplasmosis in the compromised host. Ann Intern Med 84: 193-199.
3. Mendelson MH, Finkel LJ, Meyers BR, Lieberman JP, Hirschman SZ, (1987) Pulmonary toxoplasmosis in AIDS. Scand J Infect Dis 19: 703-706.
4. Tourani JM, Israël-Biet D, Venet A, Andrieu JM, (1985) Unusual pulmonary infection in a puzzling presentation of AIDS. Lancet 1: 989.
5. Catterall JR, Hofflin JM, Remington JS, (1986) Pulmonary toxoplasmosis. Am Rev Respir Dis 133: 704-705.
6. Oksenhendler E, Cadranel J, Sarfati C, Katlama C, Datry A, et al. (1990) Toxoplasma gondii pneumonia in patients with the acquired immunodeficiency syndrome. Am J Med 88: 18N-21N.
7. Pomeroy C, Filice GA, (1992) Pulmonary toxoplasmosis: a review. Clin Infect Dis 14: 863-870.
8. Rottenberg GT, Miszkiel K, Shaw P, Miller RF, (1997) Case report: fulminant Toxoplasma gondii pneumonia in a patient with AIDS. Clin Radiol 52: 472-474.
9. Delhaes L, Mraz JC, Fréalle E, Durand-Joly I, Magro L, et al. (2010) Severe pulmonary toxoplasmosis after allo-SCT in two patients: from Toxoplasma genotyping to clinical management. Bone Marrow Transplant 45: 580-583.
10. Monaco SE, Monaghan SA, Stamm JA, Khalbuss WE, Nichols L, et al. (2012) Toxoplasmosis in a post-transplant bronchoalveolar lavage: a case report. Diagn Cytopathol 40: 629-634.
11. Candolfi E, de Blay F, Rey D, Christmann D, Treisser A, et al. (1993) A parasitologically proven case of Toxoplasma pneumonia in an immunocompetent pregnant woman. J Infect 26: 79-81.
12. Bossi P, Caumes E, Paris L, Dardé ML, Bricaire F, (1998) Toxoplasma gondii-associated Guillain-Barré syndrome in an immunocompetent patient. J Clin Microbiol 36: 3724-3725.
13. Carme B, Aznar C, Motard A, Demar M, de Thoisy B, (2002) Serologic survey of Toxoplasma gondii in noncarnivorous free-ranging neotropical mammals in French Guiana. Vector Borne Zoonotic Dis 2: 11-17.
14. Bossi P, Bricaire F, (2004) Severe acute disseminated toxoplasmosis. Lancet 364: 579.
15. Leal FE, Cavazzana CL, de Andrade HF Jr, Galisteo AJ Jr, de Mendonça JS, et al. (2007) Toxoplasma gondii pneumonia in immunocompetent subjects: case report and review. Clinical infectious diseases 44: e62-66.
16. Carme B, Demar M, Ajzenberg D, Dardé ML, (2009) Severe acquired toxoplasmosis caused by wild cycle of Toxoplasma gondii, French Guiana. Emerg Infect Dis 15: 656-658.
17. Simanaityte D, Le Gouellec N, Ajana F, Baclet N, Poissy J, et al. (2010) Primary pulmonary toxoplasmosis in an immunocompetent patient. Med Mal Infect. 40: 713-715.
18. Ferguson HW, Ellis WA, (1979) Toxoplasmosis in a calf. Vet Rec 104: 392-393.
19. Foster SF, Martin P, Allan GS, Barrs VR, Malik R, (2004) Lower respiratory tract infections in cats: 21 cases (1995-2000). J Feline Med Surg 6: 167-180.
20. Thiptara A, Kongkaew W, Bilmad U, Bhumibhamon T, Anan S, (2006) Toxoplasmosis in piglets. Ann N Y Acad Sci 1081: 336-338.
21. Juránková J, Opsteegh M, Neumayerová H, Kovařčík K, Frencová A,et al. (2012) Quantification of Toxoplasma gondii in tissue samples of experimentally infected goats by magnetic capture and real-time PCR. Vet Parasitol doi:pii: S0304-4017(12)00600-0.10.1016/j.vetpar.2012.11.016.
22. Kovari H, Ebnöther C, Schweiger A, Berther N, Kuster H, (2010) Pulmonary toxoplasmosis, a rare but severe manifestation of a common opportunistic infection in late HIV presenters: report of two cases. Infection 38: 141-144.
23. Knani L, Bouslama K, Varette C, Gonzalez Canali G, Cabane J, et al. (1990) Pulmonary toxoplasmosis in AIDS. Report of 3 cases. Ann Med Interne (Paris) 141: 469-471.
24. Luong ML, Morrissey O, Husain S, (2010) Assessment of infection risks prior to lung transplantation. Curr Opin Infect Dis 23: 578-583.
25. Herscowitz HB, (1985) In defense of the lung: paradoxical role of the pulmonary alveolar macrophage. Ann Allergy 55: 634-650.
26. Fels AO, Cohn ZA, (1986) The alveolar macrophage. J Appl Physiol 60: 353-369.
27. Badger AM, Hutchman JS, Sung CP, Bugelski PJ, (1987) Activation of rat alveolar macrophages by gamma interferon to inhibit Toxoplasma gondii in vitro. J Leukoc Biol 42: 447-454.
28. Lambrecht BN, (2006) Alveolar macrophage in the driver's seat. Immunity 24: 366-368.
29. Chinchilla M, Guerrero OM, Solano E, (1982) Lack of multiplication of toxoplasma in macrophages of rats in vitro. J Parasitol 68: 952-955.
30. Catterall JR, Sharma SD, Remington JS, (1986) Oxygen-independent killing by alveolar macrophages. J Exp Med 163: 1113-1131.
31. Catterall JR, Black CM, Leventhal JP, Rizk NW, Wachtel JS, et al. (1987) Nonoxidative microbicidal activity in normal human alveolar and peritoneal macrophages. Infect Immun 55: 1635-1640.
32. Alexander J, Scharton-Kersten TM, Yap G, Roberts CW, Liew FY, et al. (1997) Mechanism of innate resistance to Toxoplasma gondii infection. Philos Trans R Soc Lon B, Biol Sci 352: 1355-1359.
33. Adams LB, Hibbs JB Jr, Taintor RR, Krahenbuhl JL, (1990) Microbiostatic effect of murine-activated macrophages for Toxoplasma gondii. Role for synthesis of inorganic nitrogen oxides from L-arginine. J Immunol 144: 2725-2729.
34. Langermans JA, Van der Hulst ME, Nibbering PH, Hiemstra PS, Fransen L, et al. (1992) IFN-gamma-induced L-arginine-dependent toxoplasmastatic activity in murine peritoneal macrophages is mediated by endogenous tumor necrosis factor-alpha. J Immunol 148: 568-574.
35. Wang WW, Jenkinson CP, Griscavage JM, Kern RM, et al. (1995) Co-induction of arginase and nitric oxide synthase in murine macrophages activated by lipopolysaccharide. Biochem Biophys Res Commun 210: 1009-1016.
36. Fang FC, (1997) Perspectives series: host/pathogen interactions. Mechanisms of nitric oxide-related antimicrobial activity. J Clin Invest 99: 2818-2825.
37. Munder M, Eichmann K, Modolell M, (1998) Alternative metabolic states in murine macrophages reflected by the nitric oxide synthase/arginase balance: competitive regulation by CD4+ T cells correlates with Th1/Th2 phenotype. J Immunol 160: 5347-5354.
38. Yap GS, Sher A, (1999) Effector cells of both nonhemopoietic and hemopoietic origin are required for interferon (IFN)-gamma- and tumor necrosis factor (TNF)-alpha-dependent host resistance to the intracellular pathogen, Toxoplasma gondii. J Exp Med 189: 1083-1092.
39. Gobert AP, Mersey BD, Cheng Y, Blumberg DR, Newton JC, et al. (2002) Cutting edge: urease release by Helicobacter pylori stimulates macrophage inducible nitric oxide synthase. J Immunol 168: 6002-6006.
40. Seabra SH, de Souza W, DaMatta RA, (2002) Toxoplasma gondii partially inhibits nitric oxide production of activated murine macrophages. Exp Parasitol 100: 62-70.
41. Seabra SH, DaMatta RA, de Mello FG, de Souza W, (2004) Endogenous polyamine levels in macrophages is sufficient to support growth of Toxoplasma gondii. J Parasitol 90: 455-460.
42. Lüder CG, Algner M, Lang C, Bleicher N, Gross U, (2003) Reduced expression of the inducible nitric oxide synthase after infection with Toxoplasma gondii facilitates parasite replication in activated murine macrophages. Int J Parasitol 33: 833-844.
43. Koschorreck S, Wenzel F, Fuhrmann M, Racké K, (2003) Effects of phosphodiesterase inhibitors on L-arginine pathways in rat alveolar macrophages. Eur J Pharmacol 471: 229-236.
44. El Kasmi KC, Qualls JE, Pesce JT, Smith AM, Thompson RW, et al. (2008) Toll-like receptor-induced arginase 1 in macrophages thwarts effective immunity against intracellular pathogens. Nat Immunol 9: 1399-1406.
45. Das P, Lahiri A, Lahiri A, Chakravortty D, (2010) Modulation of the arginase pathway in the context of microbial pathogenesis: a metabolic enzyme moonlighting as an immune modulator. PLoS Pathog. 6: e1000899.
46. Abdallahi OM, Bensalem H, Augier R, Diagana M, De Reggi M, et al. (2001) Arginase expression in peritoneal macrophages and increase in circulating polyamine levels in mice infected with Schistosoma mansoni. Cell Mol Life Sci 58: 1350-1357.
47. Igarashi K, Kashiwagi K, (2000) Polyamines: mysterious modulators of cellular functions. Biochem Biophys Res Commun 271: 559-564.
48. Roberts SC, Tancer MJ, Polinsky MR, Gibson KM, Heby O, et al. (2004) Arginase plays a pivotal role in polyamine precursor metabolism in Leishmania. Characterization of gene deletion mutants. J Biol Chem 279: 23668-23678.
49. Li Z, Zhao ZJ, Zhu XQ, Ren QS, Nie FF, et al. (2012) Differences in iNOS and arginase expression and activity in the macrophages of rats are responsible for the resistance against T. gondii infection. PLoS ONE 7: e35834.
50. Krahenbuhl JL, Blazkovec AA, (1975) Toxoplasma gondii: immunopathology of cutaneous hypersensitivityreactions in guinea pigs injected with living parasites. Exp Parasitol 37: 83-91.
51. Chinchilla M, Frenkel JK, (1978) Mediation of immunity to intracellular infection (Toxoplasma and Besnoitia) within somatic cells. Infect Immun. 19: 999-1012.
52. Dubey JP, Frenkel JK, (1998) Toxoplasmosis of rats: a review, with considerations of their value as an animal model and their possible role in epidemiology. Vet Parasitol 77: 31-32.
53. Dubey JP, Shen SK, Kwok OC, Frenkel JK, (1999) Infection and immunity with the RH strain of Toxoplasma gondii in rats and mice. J Parasitol 85: 657-662.
54. Santoro F, Auriault C, Leite P, Darcy F, Capron A, (1987) Infection of the athymic rat by Toxoplasma gondii. C R Acad Sci III 304: 297-300.
55. Darcy F, Zenner L, (1993) Experimental models of toxoplasmosis. Res Immunol 144: 16-23.
56. Zenner L, Darcy F, Capron A, Cesbron-Delauw MF, (1998) Toxoplasma gondii: kinetics of the dissemination in the host tissues during the acute phase of infection of mice and rats. Exp Parasitol 90: 86-94.
57. Zenner L, Foulet A, Caudrelier Y, Darcy F, Gosselin B, et al. (1999) Infection with Toxoplasma gondii RH and Prugniaud strains in mice, rats and nude rats: kinetics of infection in blood and tissues related to pathology in acute and chronic infection. Pathol Res Pract 195: 475-485.
58. Freyre A, Falcón J, Méndez J, González M, (2008) Toxoplasma gondii: an improved rat model of congenital infection. Exp Parasitol 120: 142-146.
59. Freyre A, Falcón J, Mendez J, Gonzalez M, (2008) Toxoplasma gondii: protection against colonization of the brain and muscles in a rat model. Exp Parasitol 119: 252-255.
60. Badger AM, Meunier PC, Weiss RA, Bugelski PJ, (1988) Modulation of rat bronchoalveolar lavage cell function by the intratracheal delivery of interferon-gamma. J Interferon Res 8: 251-260.
61. Carrera NJ, Carmona MC, Guerrero OM, Castillo AC, (2009) The immunosuppressant effect of T lewisi (Kinetoplastidae) infection on the multiplication of Toxoplasma gondii (Sarcocystidae) on alveolar and peritoneal macrophages of the white rat. Rev Biol Trop 57: 13-22.
62. Murakami Y, Hoshi M, Hara A, Takemura M, Arioka Y, et al. (2012) Inhibition of increased indoleamine 2,3-dioxygenase activity attenuates Toxoplasma gondii replication in the lung during acute infection. Cytokine 59: 245-251.
63. Lovchik JA, Lyons CR, Lipscomb MF, (1995) A role for gamma interferon-induced nitric oxide in pulmonary clearance of Cryptococcus neoformans. Am J Respir Cell Mol Biol 13: 116-124.
64. Holt PG, Oliver J, Bilyk N, McMenamin C, McMenamin PG, et al. (1993) Down regulation of the antigen presenting cell function(s) of pulmonary dendritic cells in vivo by resident alveolar macrophages. J Exp Med 177: 397-407.
65. Lacraz S, Nicod L, Galve-de Rochemonteix B, Baumberger C, Dayer JM, et al. (1992) Suppression of metalloproteinase biosynthesis in human alveolar macrophages by interleukin-4. J Clin Invest 90: 382-388.
66. Bunn HJ, Hewitt CR, Grigg J, (2002) Suppression of autologous peripheral blood mononuclear cell proliferation by alveolar macrophages from young infants. Clin Exp Immunol 128: 313-317.
67. Munder M, Eichmann K, Morán JM, Centeno F, Soler G, Modolell M, (1999) Th1/Th2-regulated expression of arginase isoforms in murine macrophages and dendritic cells. J Immunol 163: 3771-3777.
68. Pauleau AL, Rutschman R, Lang R, Pernis A, Watowich SS, et al. (2004) Enhancer-mediated control of macrophage-specific arginase I expression. J Immunol 172: 7565-7573.
69. Brunet LR, (2001) Nitric oxide in parasitic infections. Int Immunopharmacol 1: 1457-1467.
70. Nathan C, Shiloh MU, (2000) Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc Natl Acad Sci USA 97: 8841-8848.
71. Qualls JE, DeFreitas A, Smith AM, Watowich SS, Murray PJ, (2009) Direct and indirect type-1 arginase (Arg1) induction following Mycobacterium bovis (BCG) infection. J Immunol 182: 43.1.
72. Butcher BA, Fox BA, Rommereim LM, Kim SG, Maurer KJ, et al. (2011) Toxoplasma gondii rhoptry kinase ROP16 activates STAT3 and STAT6 resulting in cytokineinhibition and arginase-1-dependent growth control. PLoS Pathog 7: e1002236.
73. Naito M, (2008) Macrophage differentiation and function in health and disease. Pathol Int 58: 143-155.
74. Schulz C, Gomez Perdiguero E, Chorro L, Szabo-Rogers H, Cagnard N, et al. (2012) A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science 336: 86-90.
75. Simon LM, Robin ED, Phillips JR, Acevedo J, Axline SG, et al. (1977) Enzymatic basis for bioenergetic differences of alveolar versus peritoneal macrophages and enzyme regulation by molecular O2. J Clin Invest 59: 443-448.
76. Boltz-Nitulescu G, Foerster O, (1979) Antigenic differences between alveolar and peritoneal macrophages of the rat. Lack of population-specific determinants. Immunology 38: 621-630.
77. Dörger M, Münzing S, Allmeling AM, Messmer K, Krombach F, (2001) Phenotypic and functional differences between rat alveolar, pleural, and peritoneal macrophages. Exp Lung Res 27: 65-76.
78. Guth AM, Janssen WJ, Bosio CM, Crouch EC, Henson PM, et al. (2009) Lung environment determines unique phenotype of alveolar macrophages. Am J Physiol Lung Cell Mol Physiol 296: L936-946.
79. Müllner N, Lázár A, Hrabák A, (2002) Enhanced utilization and altered metabolism of arginine in inflammatory macrophages caused by raised nitric oxide synthesis. Int J Biochem Cell Biol 34: 1080-1090.
80. Hrabák A, Bajor T, Csuka I, (2006) The effect of various inflammatory agents on the alternative metabolic pathways of arginine in mouse and rat macrophages. Inflamm Res 55: 23-31.
81. Wang L, Chen H, Liu D, Huo X, Gao J, et al. (2013) Genotypes and Mouse Virulence of Toxoplasma gondii Isolates from Animals and Humans in China. PLoS One 8: e53483.
82. Dubremetz JF, Lebrun M, (2012) Virulence factors of Toxoplasma gondii. Microbes Infect 14: 1403-1410.
83. Schneemann M, Schoedon G, Hofer S, Blau N, Guerrero L, et al. (1993) Nitric oxide synthase is not a constituent of the antimicrobial armature of human mononuclear phagocytes. J Infect Dis 167: 1358-1363.
84. Kempf MC, Cesbron-Delauw MF, Deslee D, Gross U, Herrmann T, et al. (1999) Different manifestations of Toxoplasma gondii infection in F344 and LEW rats. Med Microbiol Immunol 187: 137-142.
85. Myrvik Q, Leake ES, Fariss B, (1961) Studies on pulmonary alveolar macrophages from the normal rabbit: a technique to procure them in a high state of purity. J Immunol 86: 128-132.
86. Ding AH, Nathan CF, Stuehr DJ, (1988) Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. J Immunol 141: 2407-2412.
87. Corraliza IM, Campo ML, Soler G, Modolell M, (1994) Determination of arginase activity in macrophages: a micromethod. J Immunol Methods 174: 231-235.