Evolutionary roots of arginase expression and regulation

Frontiers in Immunology

Volumn 5, Issue NOV, 2014, Pages

  Dzik, Jolanta Maria ^a  

^a WARSAW UNIVERSITY OF LIFE SCIENCES   (Poland)

Author keywords

Arginase; Evolution; Hemocytes; M1 M2 macrophages; Nitric oxide synthase; Parasites; TGF ; Wound healing

Indexed keywords

ARGINASE; BACTERIAL ENZYME; BONE MORPHOGENETIC PROTEIN; GAMMA INTERFERON; INTERLEUKIN 1BETA; INTERLEUKIN 4 RECEPTOR ALPHA; LIPOPOLYSACCHARIDE; NITRIC OXIDE SYNTHASE; PROTEIN SERINE THREONINE KINASE; SMAD2 PROTEIN; SMAD3 PROTEIN; STAT6 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ADAPTIVE IMMUNITY; BACTERIAL INFECTION; BLOOD CELL; CYTOTOXICITY; EMBRYO DEVELOPMENT; ENZYME INDUCTION; EVOLUTION; HUMAN; IMMUNE RESPONSE; INVERTEBRATE; MACROPHAGE; MACROPHAGE ACTIVATION; MACROPHAGE MIGRATION; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; TISSUE INJURY; WOUND HEALING;

EID: 84919427210     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2014.00544     Document Type: Review

References (132)

1. 2 paradigm. J Immunol (2000) 164:6166-73. doi: 10.4049/jimmunol.164.12.6166
2. Mosser DM. The many faces of macrophage activation. J Leukoc Biol (2003) 73:209-12. doi:10.1189/jlb.0602325
3. Ottaviani E. Immunocyte: the invertebrate counterpart of the vertebrate macrophage. Inv Surv J (2011) 8:1-4.
4. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol (2008) 8:958-69. doi:10.1038/nri2448
5. Mylonas KJ, Nair MG, Prieto-Lafuente L, Paape D, Allen JE. Alternatively activated macrophages elicited by helminth infection can be reprogrammed to enable microbial killing. J Immunol (2009) 182:3084-94. doi:10.4049/jimmunol.0803463
6. Hesse M, Modolell M, La Flamme AC, Schito M, Fuentes JM, Cheever AW, et al. Differential regulation of nitric oxide synthase-2 and arginase-1 by type 1/type 2 cytokines in vivo: granulomatous pathology is shaped by the pattern of L-arginine metabolism. J Immunol (2001) 167:6533-44. doi:10.4049/jimmunol.167.11.6533
7. Chen H, McCaig BC, Melotto M, He SY, Howe GA. Regulation of plant arginase by wounding, jasmonate, and the phytotoxin coronatine. J Biol Chem (2004) 279:45998-6007. doi:10.1074/jbc. M407151200
8. Sekowska A, Danchin A, Risler JL. Phylogeny of related functions: the case of polyamine biosynthetic enzymes. Microbiology (2000) 146:1815-28.
9. Samson ML. Drosophila arginase is produced from a nonvital gene that contains the elav locus within its third intron. J Biol Chem (2000) 275:31107-14. doi:10.1074/jbc. M001346200
10. Morris SM. Regulation of enzymes of the urea cycle and arginine metabolism. Annu Rev Nutr (2002) 22:87-105. doi:10.1146/annurev.nutr.22.110801.140547
11. Jenkinson CP, Grody WW, Cederbaum SD. Comparative properties of arginases. Comp Biochem Physiol (1996) 114B:107-32. doi:10.1016/0305-0491(95)02138-8
12. 2 cells: kinetics, pharmacology and dependence on the plasma membrane proton gradient. Biochem J (2006) 393:583-9. doi:10.1042/BJ20050981
13. Massagué J. TGF-β signal transduction. Annu Rev Biochem (1998) 67:753-91. doi:10.1146/annurev.biochem.67.1.753
14. Gitelman SE, Derynck R. Transforming growth factor-β. In: Nicola NA, editor. Guidebook to Cytokines and their Receptors. Oxford: A Sambrook and Tooze Publication at Oxford University Press (1994). p. 223-6.
15. Magor BG, Magor KE. Evolution of effectors and receptors of innate immunity. Dev Comp Immunol (2001) 25:651-82. doi:10.1016/S0145-305X(01)00029-5
16. Wang EA, Rosen V, Cordes P, Hewick RM, Kriz MJ, Luxenberg DP, et al. Purification and characterization of other distinct bone-inducing factors. Proc Natl Acad Sci U S A (1988) 85:9484-8. doi:10.1073/pnas.85.24.9484
17. Wozney JM, Rosen V, Celeste AJ, Mitsock LM, Whitters MJ, Kriz RW, et al. Novel regulators of bone formation: molecular clones and activities. Science (1988) 242:1528-34. doi:10.1126/science.3201241
18. Hogan BL. Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev (1996) 10:1580-94. doi:10.1101/gad.10.13.1580
19. Zhao GQ. Consequences of knocking out BMP signaling in the mouse. Genesis (2003) 35:43-56. doi:10.1002/gene.10167
20. Khalsa O, Yoon JW, Torres-Schumann S, Wharton KA. TGF-β/BMP superfamily members, Gbb-60A and Dpp, cooperate to provide pattern information and establish cell identity in the Drosophila wing. Development (1998) 125:2723-34.
21. Lelong C, Mathieu M, Favrel P. Identification of new bone morphogenetic protein-related members in invertebrates. Biochimie (2001) 83:423-6. doi:10.1016/S0300-9084(01)01260-3
22. Matus DQ, Magie CR, Pang K, Martindale MQ, Thomsen GH. The Hedgehog gene family of the cnidarian, Nematostella vectensis, and implications for understanding metazoan Hedgehog pathway evolution. Dev Biol (2008) 313:501-18. doi:10.1016/j.ydbio.2007.09.032
23. Matus DQ, Thomsen GH, Martin Dale MQ. Dorso/ventral genes are asymmetrically expressed and involved in germ-layer demarcation during cnidarian gastrulation. Curr Biol (2006) 16:499-505. doi:10.1016/j.cub.2006.01.052
24. Wrana JL, Attisano L, Wieser R, Ventura F, Massagué J. Mechanism of activation of the TGF-beta receptor. Nature (1994) 370:341-7. doi:10.1038/370341a0
25. Heldin CH, Miyazono K, ten Dijke P. TGF-β signalling from cell membrane to nucleus through SMAD proteins. Nature (1997) 390:465-71. doi:10.1038/37284
26. Attisano L, Wrana JL. Signal transduction by the TGF-β superfamily. Science (2002) 296:1646-7. doi:10.1126/science.1071809
27. Miyazawa K, Shinozaki M, Hara T, Furuya T, Miyazono K. Two major Smad pathways in TGF-β superfamily signalling. Genes Cells (2002) 7:1191-204. doi:10.1046/j.1365-2443.2002.00599.x
28. Qin BY, Chacko BM, Lam SS, de Caestecker MP, Correia JJ, Lin K. Structural basis of Smad1 activation by receptor kinase phosphorylation. Mol Cell (2001) 8:303-12. doi:10.1016/S1097-2765(01)00417-8
29. Massagué J, Seoane J, Wotton D. Smad transcription factors. Genes Dev (2005) 19:2783-810. doi:10.1101/gad.1350705
30. Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier ME, Mitros T, et al. The Amphimedon queenslandica genome and the evolution of animal complexity. Nature (2010) 466:720-6. doi:10.1038/nature09201
31. 7 is essential for specific inhibition of transforming growth factor-β signaling. J Cell Biol (2001) 155:1017-27. doi:10.1083/jcb.200106023
32. Richards GS, Degnan BM. The dawn of developmental signaling in the metazoa. Cold Spring Harb Symp Quant Biol (2009) 74:81-90. doi:10.1101/sqb.2009.74.028
33. Yokota Y, Mori S. Role of Id family proteins in growth control. J Cell Physiol (2002) 190:21-8. doi:10.1002/jcp.10042
34. Balinski A, Sun Y, Dzik J. Traces of marine nematodes from 470 million years old early Ordovician rocks in China. Nematology (2013) 15:567-74. doi:10.1163/15685411-00002702
35. Schulenburg H, Kurz CL, Ewbank JJ. Evolution of the innate immune system: the worm perspective. Immunol Rev (2004) 198:36-58. doi:10.1111/j.0105-2896.2004.0125.x
36. Tan MW. Genetic and genomic dissection of host-pathogen interactions using a P. aeruginosa-C. elegans pathogenesis model. Pediatr Pulmonol (2001) 32:96-7.
37. Mochii M, Yoshida S, Morita K, Kohara Y, Ueno N. Identification of transforming growth factor-β regulated genes in Caenorhabditis elegans by differential hybridization of arrayed cDNAs. Proc Natl Acad Sci U S A (1999) 96:15020-5. doi:10.1073/pnas.96.26.15020
38. Irving P, Troxler L, Heuer TS, Belvin M, Kopczynski C, Reichhart JM, et al. A genome-wide analysis of immune responses in Drosophila. Proc Natl Acad Sci U S A (2001) 98:15119-24. doi:10.1073/pnas.261573998
39. De Gregorio E, Spellman PT, Rubin GM, Lemaitre B. Genome-wide analysis of the Drosophila immune response by using oligonucleotide microarrays. Proc Natl Acad Sci U S A (2001) 98:12590-5. doi:10.1073/pnas.221458698
40. Newfeld SJ, Wisotzkey RG, Kumar S. Molecular evolution of a developmental pathway: phylogenetic analyses of transforming growth factor-b family ligands, receptors and Smad signal transducers. Genetics (1999) 152:783-95.
41. Letterio JJ, Roberts AB. Regulation of immune responses by TGF-β. Annu Rev Immunol (1998) 16:137-61. doi:10.1146/annurev.immunol.16.1.137
42. Morita K, Flemming AJ, Sugihara Y, Mochii M, Suzuki Y, Yoshida S, et al. A Caenorhabditis elegans TGF-β, DBL-1, controls the expression of LON-1, a PR-related protein, that regulates polyploidization and body length. EMBO J (2002) 21:1063-73. doi:10.1093/emboj/21.5.1063
43. Maduzia LL, Gumienny TL, Zimmerman CM, Wang H, Shetgiri P, Krishna S, et al. lon-1 regulates Caenorhabditis elegans body size downstream of the dbl-1TGF-β signaling pathway. Dev Biol (2002) 246:418-28. doi:10.1006/dbio.2002.0662
44. Fessler JH, Fessler LI. Drosophila extracellular matrix. Annu Rev Cell Biol (1989) 5:309-39. doi:10.1146/annurev.cellbio.5.1.309
45. Wood W, Faria C, Jacinto A. Distinct mechanisms regulate hemocyte chemotaxis during development and wound healing in Drosophila melanogaster. J Cell Biol (2006) 173:405-16. doi:10.1083/jcb.200508161
46. Grabher C, Cliffe A, Miura K, Hayflick J, Pepperkok R, Rørth P, et al. Birth and life of tissue macrophages and their migration in embryogenesis and inflammation in medaka. J Leukoc Biol (2007) 81:263-71. doi:10.1189/jlb.0806526
47. Stramer B, Wood W, Galko MJ, Redd MJ, Jacinto A, Parkhurst SM, et al. Live imaging of wound inflammation in Drosophila embryos reveals key roles for small GTPases during in vivo cell migration. J Cell Biol (2005) 168:567-73. doi:10.1083/jcb.200405120
48. Sminia T, Pietersma K, Scheerboom JE. Histological and ultrastructural observations on wound healing in the freshwater pulmonate Lymnaea stagnalis. Z Zellforsch Mikrosk Anat (1973) 141:561-73. doi:10.1007/BF00307125
49. Franchini A, Ottaviani E. Repair of molluscan tissue injury: role of PDGF and TGF-beta1. Tissue Cell (2000) 32:312-21.
50. Rudolph R, Vande Berg J, Ehrlich PH. Wound contraction and scar contracture. In: Cohen IK, Diegelmann RF, Lindblad WJ, editors. Wound Healing; Biochemical and Clinical Aspects. (Vol. 6), Philadelphia, PA: Saunders (1992). p. 96-114.
51. Leibovich SJ, Ross R. The role of the macrophage in wound repair. Am J Pathol (1975) 78:71-100.
52. Pierce GF, Vande Berg J, Rudolph R, Tarpley J, Mustoe TA. Platelet-derived growth factor-BB and transforming growth factor β-1 selectively modulate glycosaminoglycans, collagen, and myofibroblasts in excisional wounds. Am J Pathol (1991) 138:629-46.
53. Quaglino D, Nanney LB, Ditesheim JA, Davidson JM. Transforming growth factor-β stimulates wound healing and modulates extracellular matrix gene expression in pig skin. Incisional wound model. J Invest Dermatol (1991) 97:34-42.
54. Pongsomboon S, Tang S, Boonda S, Aoki T, Hirono I, Yasuike M, Tassanakajon A. Differentially expressed genes in Penaeus monodon hemocytes following infection with yellow head virus. BMB Rep (2008) 41:670-7. doi:10.5483/BMBRep.2008.41.9.670
55. Cutroneo KR. TGF-β-induced fibrosis and SMAD signaling: oligo decoys as natural therapeutics for inhibition of tissue fibrosis and scarring. Wound Repair Regen (2007) 15(Suppl 1):S54-60. doi:10.1111/j.1524-475X.2007.00226.x
56. Jacobs W, Kumar-Singh S, Bogers J, Van de Vijver K, Deelder A, Van Marck E. Transforming growth factor-β, basement membrane components and heparan sulphate proteoglycans in experimental hepatic schistosomiasis mansoni. Cell Tissue Res (1998) 292:101-6. doi:10.1007/s004410051039
57. Blaxter ML. Molecular analysis of nematode evolution. In: Kennedy MW, Harnett W, editors. Parasitic Nematodes: Molecular Biology, Biochemistry and Immunology. St. Albans: CAB International (2001). p. 1-24.
58. Wu G. Synthesis of citrulline and arginine from proline in enterocytes of postnatal pigs. Am J Physiol Gastrointest Liver Physiol (1997) 272:G1382-90.
59. Hamana K, Hamana H, Shinozawa T. Alterations in polyamine levels of nematode, earthworm, leech and planarian during regeneration, temperature and osmotic stresses. Comp Biochem Physiol B Biochem Mol Biol (1995) 111:91-7. doi:10.1016/0305-0491(94)00222-G
60. Zhang M, Wang H, Tracey KJ. Regulation of macrophage activation and inflammation by spermine: a new chapter in an old story. Crit Care Med (2000) 28(4 Suppl):N60-6. doi:10.1097/00003246-200004001-00007
61. Lockyer AE, Emery AM, Kane RA, Walker AJ, Mayer CD, Mitta G, et al. Early differential gene expression in haemocytes from resistant and susceptible Biomphalaria glabrata strains in response to Schistosoma mansoni. PLoS One (2012) 7(12):e51102. doi:10.1371/journal.pone.0051102
62. Albina JE, Caldwell MD, Henry WL, Mills CD. Regulation of macrophage functions by L-arginine. J Exp Med (1989) 169:1021-9. doi:10.1084/jem.169.3.1021
63. Witte MB, Barbul A. Arginine physiology and its implication for wound healing. Wound Repair Regen (2003) 11:419-23. doi:10.1046/j.1524-475X.2003.11605.x
64. Kinne O. Diseases of Marine Animals. Hamburg: Biologische Anstalt Helgoland (1983).
65. Ford SE, Kanaley SA, Littlewood DT. Cellular responses of oysters infected with Haplosporidium nelsoni: changes in circulating and tissue-infiltrating hemocytes. J Invertebr Pathol (1993) 61:49-57. doi:10.1006/jipa.1993.1009
66. Roberts AB, Heine UI, Flanders KC, Sporn MB. Transforming growth-factor-β - major role in regulation of extracellular-matrix. Ann N Y Acad Sci (1990) 580:225-32. doi:10.1111/j.1749-6632.1990.tb17931.x
67. Skugor S, Glover KA, Nilsen F, Krasnov A. Local and systemic gene expression responses of Atlantic salmon (Salmo salar) to infection with the salmon louse. BMC Genomics (2008) 9:498. doi:10.1186/1471-2164-9-498
68. McDowell IC, Nikapitiya C, Aguiar D, Lane CE, Istrail S, et al. Transcriptome of american oysters, Crassostrea virginica, in response to bacterial challenge: insights into potential mechanisms of disease resistance. PLoS One (2014) 9(8):e105097. doi:10.1371/journal.pone.0105097
69. Loke P, Gallagher I, Nair MG, Zang X, Brombacher F, Mohrs M, et al. Alternative activation is an innate response to injury that requires CD4+ T cells to be sustained during chronic infection. J Immunol (2007) 179:3926-36. doi:10.4049/jimmunol.179.6.3926
70. Wynn TA. Fibrotic disease and the TH1/TH2 paradigm. Nat Rev Immunol (2004) 4:583-94. doi:10.1038/nri1412
71. Allen JE, Wynn T. Evolution of Th2 immunity: a rapid repair response to tissue destructive pathogens. PLoS Pathog (2011) 7(5):e1002003. doi:10.1371/journal.ppat.1002003
72. Patel N, Kreider T, Urban JF Jr, Gause WC. Characterisation of effector mechanisms at the host: parasite interface during the immune response to tissue-dwelling intestinal nematode parasites. Int J Parasitol (2009) 39:13-21. doi:10.1016/j.ijpara.2008.08.003
73. Pearce EJ, Vasconcelos JP, Brunet LR, Sabin EA. IL-4 in schistosomiasis. Exp Parasitol (1996) 84:295-9. doi:10.1006/expr.1996.0116
74. Dzik JM, Gołos B, Jagielska E, Zielinski Z, Wałajtys-Rode E. A non-classical type of alveolar macrophage response to Trichinella spiralis infection. Parasite Immunol (2004) 26:197-205. doi:10.1111/j.0141-9838.2004.00700.x
75. Bai X, Wu X, Wang X, Guan Z, Gao F, Yu J, et al. Regulation of cytokine expression in murine macrophages stimulated by excretory/secretory products from Trichinella spiralis in vitro. Mol Cell Biochem (2012) 360:79-88. doi:10.1007/s11010-011-1046-4
76. Du L, Wei H, Li L, Shan H, Yu Y, Wang Y, et al. Regulation of recombinant Trichinella spiralis 53-kDa protein (rTsP53) on alternatively activated macrophages via STAT6 but not IL-4Rα in vitro. Cell Immunol (2014) 288:1-7. doi:10.1016/j.cellimm.2014.01.010
77. Donnelly S, Stack CM, O'Neill SM, Sayed AA, Williams DL, Dalton JP. Helminth 2-Cys peroxiredoxin drives Th2 responses through a mechanism involving alternatively activated macrophages. FASEB J (2008) 22:4022-32. doi:10.1096/fj.08-106278
78. Tanabe M, Kaneko N, Takeuchi T. Schistosoma mansoni: higher free proline levels in the livers of infected mice. Exp Parasitol (1991) 72:134-44. doi:10.1016/0014-4894(91)90131-F
79. Atochina O, Da'dara AA, Walker M, Harn DA. The immunomodulatory glycan LNFPIII initiates alternative activation of murine macrophages in vivo. Immunology (2008) 125:111-21. doi:10.1111/j.1365-2567.2008.02826.x
80. Thomas PG, Carter MR, Da'dara AA, DeSimone TM, Harn DA. A helminth glycan induces APC maturation via alternative NF-κB activation independent of I κBα degradation. J Immunol (2005) 175:2082-90. doi:10.4049/jimmunol.175.4.2082
81. Jensen KD, Wang Y, Wojno ED, Shastri AJ, Hu K, Cornel L, et al. Toxoplasma polymorphic effectors determine macrophage polarization and intestinal inflammation. Cell Host Microbe (2011) 9:472-83. doi:10.1016/j.chom.2011.04.015
82. Clark RI, Woodcock KJ, Geissmann F, Trouillet C, Dionne MS. Multiple TGF-β superfamily signals modulate the adult Drosophila immune response. Curr Biol (2011) 21:1672-7. doi:10.1016/j.cub.2011.08.048
83. Bootcov MR, Bauskin AR, Valenzuela SM, Moore AG, Bansal M, He XY. MIC-1, a novel macrophage inhibitory cytokine, is a divergent member of the TGF-β superfamily. Proc Natl Acad Sci U S A (1997) 94:11514-9. doi:10.1073/pnas.94.21.11514
84. Shull MM, Ormsby I, Kier AB, Pawlowski S, Diebold RJ, Yin M, et al. Targeted disruption of the mouse transforming growth factor-β1 gene results in multifocal inflammatory disease. Nature (1992) 359:693-9. doi:10.1038/359693a0
85. Mallo GV, Kurz CL, Couillault C, Pujol N, Granjeaud S, Kohara Y, et al. Inducible antibacterial defense system in C. elegans. Curr Biol (2002) 12:1209-14. doi:10.1016/S0960-9822(02)00928-4
86. Gong D, Shi W, Yi SJ, Chen H, Groffen J, Heisterkamp N. TGF-β signaling plays a critical role in promoting alternative macrophage activation. BMC Immunol (2012) 13:31. doi:10.1186/1471-2172-13-31
87. Mu Y, Gudey SK, Landstrom M. Non-Smad signaling pathways. Cell Tissue Res (2012) 347:11-20. doi:10.1007/s00441-011-1201-y
88. Rocher C, Singla DK. SMAD-PI3K-Akt-mTOR pathway mediates BMP-7 polarization of monocytes into M2 macrophages. PLoS One (2013) 8(12):e84009. doi:10.1371/journal.pone.0084009
89. Rauh MJ, Ho V, Pereira C, Sham A, Sly LM, Lam V, et al. SHIP represses the generation of alternatively activated macrophages. Immunity (2005) 23:361-74. doi:10.1016/j.immuni.2005.09.003
90. Weichhart T, Säemann MD. The PI3K/Akt/mTOR pathway in innate immune cells: emerging therapeutic applications. Ann Rheum Dis (2008) 67(Suppl 3):iii70-4. doi:10.1136/ard.2008.098459
91. Miyazono K, Maeda S, Imamura T. BMP receptor signaling: transcriptional targets, regulation of signals, and signaling cross-talk. Cytokine Growth Factor Rev (2005) 16:251-63. doi:10.1016/j.cytogfr.2005.01.009
92. Lu M, Lin SC, Huang Y, Kang YJ, Rich R, Lo YC, et al. XIAP induces NF-κB activation via the BIR1/TAB1 interaction and BIR1 dimerization. Mol Cell (2007) 26:689-702. doi:10.1016/j.molcel.2007.05.006
93. Hong JH, Lee GT, Lee JH, Kwon SJ, Park SH, Kim SJ, et al. Effect of bone morphogenetic protein-6 on macrophages. Immunology (2009) 128(1 Suppl):e442-50. doi:10.1111/j.1365-2567.2008.02998.x
94. Fujihara M, Muroi M, Tanamoto K, Suzuki T, Azuma H, Ikeda H. Molecular mechanisms of macrophage activation and deactivation by lipopolysaccharide: roles of the receptor complex. Pharmacol Ther (2003) 100:171-94. doi:10.1016/j.pharmthera.2003.08.003
95. Kwon SJ, Lee GT, Lee JH, Kim WJ, Kim IY. Bone morphogenetic protein-6 induces the expression of inducible nitric oxide synthase in macrophages. Immunology (2009) 128(1 Suppl):e758-65. doi:10.1111/j.1365-2567.2009.03079.x
96. Shibuya H, Iwata H, Masuyama N, Gotoh Y, Yamaguchi K, Irie K, et al. Role of TAK1 and TAB1 in BMP signaling in early Xenopus development. EMBO J (1998) 17:1019-28. doi:10.1093/emboj/17.4.1019
97. Jadrich JL, O'Connor MB, Coucouvanis E. Expression of TAK1, a mediator of TGF-β and BMP signaling, during mouse embryonic development. Gene Expr Patterns (2003) 3:131-4. doi:10.1016/S1567-133X(03)00012-7
98. Wang C, Deng L, Hong M, Akkaraju GR, Inoue J, Chen ZJ. TAK1 is a ubiquitin-dependent kinase of MKK and IKK. Nature (2001) 412:346-51. doi:10.1038/35083684
99. Mills CD. M1 and M2 Macrophages: Oracles of Health and Disease. Crit Rev Immunol (2012) 32(6):463-88. doi:10.1615/CritRevImmunol.v32.i6.10
100. Kleinert H, Schwarz PM, Forstermann U. Regulation of the expression of inducible nitric oxide synthase. Biol Chem (2003) 384:1343-64. doi:10.1515/BC.2003.152
101. Knowles RG, Moncada S. Nitric oxide synthases in mammals. Biochem J (1994) 298:249-58.
102. Zemojtel T, Wade RC, Dandekar T. In search of the prototype of nitric oxide synthase. FEBS Lett (2003) 554:1-5. doi:10.1016/S0014-5793(03)01081-0
103. Adak S, Aulak KS, Stuehr DJ. Direct evidence for nitric oxide production by a nitric-oxide synthase-like protein from Bacillus subtilis. J Biol Chem (2002) 277:16167-71. doi:10.1074/jbc. M201136200
104. Moroz LL, Meech RW, Sweedler JV, Mackie GO. Nitric oxide regulates swimming in the jellyfish Aglantha digitale. J Comp Neurol (2004) 471:26-36. doi:10.1002/cne.20023
105. Cristino L, Guglielmotti V, Cotugno A, Musio C, Santillo S. Nitric oxide signaling pathways at neural level in invertebrates: functional implications in cnidarians. Brain Res (2008) 1225:17-25. doi:10.1016/j.brainres.2008.04.056
106. Trimmer BA, Aprille J, Modica-Napolitano J. Nitric oxide signalling: insect brains and photocytes. Biochem Soc Symp (2004) 71:65-83.
107. Kohn AB, Lea JM, Moroz LL, Greenberg RM. Schistosoma mansoni: use of a fluorescent indicator to detect nitric oxide and related species in living parasites. Exp Parasitol (2006) 113:130-3. doi:10.1016/j.exppara.2005.12.013
108. Elofsson R, Carlberg M, Moroz L, Nezlin L, Sakharov D. Is nitric oxide (NO) produced by invertebrate neurones? Neuroreport (1993) 4:279-82. doi:10.1097/00001756-199303000-00013
109. Yuda M, Hirai M, Miura K, Matsumura H, Ando K, Chinzei Y. cDNA cloning, expression and characterization of nitric-oxide synthase from the salivary glands of the blood-sucking insect Rhodnius prolixus. Eur J Biochem (1996) 242:807-12. doi:10.1111/j.1432-1033.1996.0807r.x
110. Nighorn A, Gibson NJ, Rivers DM, Hildebrand JG, Morton DB. The nitric oxide-cGMP pathway may mediate communication between sensory afferents and projection neurons in the antennal lobe of Manduca sexta. J Neurosci (1998) 18:7244-55.
111. Regulski M, Tully T. Molecular and biochemical characterization of dNOS: a Drosophila Ca2+/calmodulin-dependent nitric oxide synthase. Proc Natl Acad Sci U S A (1995) 92:9072-6. doi:10.1073/pnas.92.20.9072
112. Korneev SA, Piper MR, Picot J, Phillips R, Korneeva EI, O'Shea M. Molecular characterization of NOS in a mollusc: expression in a giant modulatory neuron. J Neurobiol (1998) 35:65-76. doi:10.1002/(SICI)1097-4695(199804)35:1<65::AID-NEU6>3.0.CO;2-9
113. Moroz LL, Kohn AB. Parallel evolution of nitric oxide signaling: diversity of synthesis & memory pathways. Front Biosci (2014) 16:2008-51. doi:10.2741/3837
114. Golderer G, Werner ER, Leitner S, Grobner P, Werner-Felmayer G. Nitric oxide synthase is induced in sporulation of Physarum polycephalum. Genes Dev (2001) 15:1299-309. doi:10.1101/gad.890501
115. Dzik JM. The ancestry and cumulative evolution of immune reactions. Acta Biochim Pol (2010) 57:443-66.
116. Yeh FC, Wu SH, Lai CY, Lee CY. Demonstration of nitric oxide synthase activity in crustacean hemocytes and anti-microbial activity of hemocyte-derived nitric oxide. Comp Biochem Physiol B Biochem Mol Biol (2006) 144:11-7. doi:10.1016/j.cbpb.2006.01.007
117. Palumbo A. Nitric oxide in marine invertebrates: a comparative perspective. Comp Biochem Physiol A Mol Integr Physiol (2005) 142:241-8. doi:10.1016/j.cbpb.2005.05.043
118. Nappi AJ, Vass E, Frey F, Carton Y. Nitric oxide involvement in Drosophila immunity. Nitric Oxide (2000) 4:423-30. doi:10.1006/niox.2000.0294
119. Foley E, O'Farrell PH. Nitric oxide contributes to induction of innate immune responses to gram-negative bacteria in Drosophila. Genes Dev (2003) 17:115-25. doi:10.1101/gad.1018503
120. Dimopoulos G, Seeley D, Wolf A, Kafatos FC. Malaria infection of the mosquito Anopheles gambiae activates immune-responsive genes during critical transition stages of the parasite life cycle. EMBO J (1998) 17:6115-23. doi:10.1093/emboj/17.21.6115
121. Luckhart S, Rosenberg R. Gene structure and polymorphism of an invertebrate nitric oxide synthase gene. Gene (1999) 232:25-34. doi:10.1016/S0378-1119(99)00121-3
122. Beschin A, Bilej M, Torreele E, De Baetselier P. On the existence of cytokines in invertebrates. Cell Mol Life Sci (2001) 58(5-6):801-14. doi:10.1007/PL00000901
123. Lowenstein CJ, Alley EW, Raval P, Snowman AM, Snyder SH, Russell SW, et al. Macrophage nitric oxide synthase gene: two upstream regions mediate induction by interferon gamma and lipopolysaccharide. Proc Natl Acad Sci U S A (1993) 90:9730-4. doi:10.1073/pnas.90.20.9730
124. Xie QW, Whisnant R, Nathan C. Promoter of the mouse gene encoding calcium-independent nitric oxide synthase confers inducibility by interferon gamma and bacterial lipopolysaccharide. J Exp Med (1993) 177:1779-84. doi:10.1084/jem.177.6.1779
125. Sengupta R, Sahoo R, Mukherjee S, Regulski M, Tully T, Stuehr DJ, et al. Characterization of Drosophila nitric oxide synthase: a biochemical study. Biochem Biophys Res Commun (2003) 306:590-7. doi:10.1016/S0006-291X(03)01003-9
126. Ghosh DK, Wu C, Pitters ER, Mayer B, Stuehr DJ. Characterization of the inducible nitric oxide synthase oxygenase domain identifies a 49-amino acid segment required for subunit dimerization and tetrahydrobiopterin interaction. Biochemistry (1997) 36:10609-19. doi:10.1021/bi9702290
127. Pace JL, Lowenstein CJ, Phillips TA, Chen LC, Morrison DC, Hunt JS, et al. Population dynamics of inducible nitric oxide synthase production by LPS- and LPS/IFN-gamma-stimulated mouse macrophages. J Endotoxin Res (1994) 1:227-33.
128. Xie QW, Kashiwabara Y, Nathan C. Role of transcription factor NF-κ B/Rel in induction of nitric oxide synthase. J Biol Chem (1994) 269:4705-8.
129. Vodovotz Y. Control of nitric oxide production by transforming growth factor-beta1: mechanistic insights and potential relevance to human disease. Nitric Oxide (1997) 1:3-17. doi:10.1006/niox.1996.0105
130. Sugiyama Y, Kakoi K, Kimura A, Takada I, Kashiwagi I, Wakabayashi Y. Smad2 and Smad3 are redundantly essential for the suppression of iNOS synthesis in macrophages by regulating IRF3 and STAT1 pathways. Int Immunol (2012) 24:253-65. doi:10.1093/intimm/dxr126
131. Vodovotz Y, Chesler L, Chong H, Kim SJ, Simpson JT, De GraffW, et al. Regulation of transforming growth factor beta1 by nitric oxide. Cancer Res (1999) 59:2142-9.
132. Forlenza M, Fink IR, Raes G, Wiegertjes GF. Heterogeneity of macrophage activation in fish. Dev Comp Immunol (2011) 35:1246-55. doi:10.1016/j.dci.2011.03.008