Induction of genes encoding NADPH oxidase components and activation of IFN regulatory factor-1 by prolactin in fish macrophages

Innate Immunity

Volumn 19, Issue 6, 2013, Pages 644-654

  Olavarría, Víctor H ^a   Figueroa, Jaime E ^a,b   Mulero, Victoriano ^c  

^a UNIVERSIDAD AUSTRAL DE CHILE   (Chile)

^b Interdisciplinary Center for Aquaculture Research   (Chile)

^c UNIVERSITY OF MURCIA   (Spain)

Author keywords

cell signaling; evolution; inflammation; Reactive oxygen species; respiratory burst; salmon; teleosts

Indexed keywords

INTERFERON REGULATORY FACTOR 1; JANUS KINASE; N BENZYL 2 CYANO 3 (3,4 DIHYDROXYPHENYL)ACRYLAMIDE; P47PHOX PROTEIN; P67PHOX PROTEIN; PROLACTIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; STAT PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; ATLANTIC SALMON; CONTROLLED STUDY; DNA BINDING; GENE EXPRESSION; GENE INDUCTION; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; MACROPHAGE; NONHUMAN; PROTEIN PHOSPHORYLATION; RAT; RESPIRATORY BURST; SIGNAL TRANSDUCTION;

CELL SIGNALING; EVOLUTION; INFLAMMATION; REACTIVE OXYGEN SPECIES; RESPIRATORY BURST; SALMON; TELEOSTS;

ANIMALS; CELL LINE; FISH PROTEINS; GENE EXPRESSION REGULATION; INTERFERON REGULATORY FACTOR-1; JANUS KINASES; MONOCYTES; NADPH OXIDASE; NUCLEOTIDE MOTIFS; PROLACTIN; REACTIVE OXYGEN SPECIES; SALMO SALAR; SIGNAL TRANSDUCTION; STAT TRANSCRIPTION FACTORS; TILAPIA; TRANSCRIPTIONAL ACTIVATION; TYRPHOSTINS;

EID: 84884983127     PISSN: 17534259     EISSN: 17534267     Source Type: Journal    
DOI: 10.1177/1753425913479148     Document Type: Article

References (54)

1. Kooijman R, Hooghe-Peters EL, Hooghe R. Prolactin, growth hormone, and insulin-like growth factor-1 in the immune system. Adv Immunol. 1996 ; 63: 377-454
2. McMurray RW. Estrogen, prolactin, and autoimmunity: actions and interactions. Intl Immunopharmacol. 2001 ; 1: 995-1008
3. Balm M, Iwama K, Pickerling D, Sumpter P, Schreck B Fish stress and health in aquaculture. Iwama GK Pickering AD Sumpter JP Schreck CB, ed. Cambridge: Cambridge University Press ; 1997: 195-221.
4. Clark R. The somatogenic hormones and insulin-like growth factor-1: stimulators of lymphopoiesis and immune function. Endocr Rev. 1997 ; 18: 157-179
5. Harris J, Bird DJ. Modulation of the fish immune system by hormones. Vet Immunol Immunopathol. 2000 ; 77: 163-176
6. Sakai M, Kobayashi M, Kawauchi H. In vitro activation of fish phagocytic cells by GH, prolactin and somatolactin. J Endocrinol. 1996 ; 151: 113-118
7. Yada T, Nagae M, Moriyama S, Azuma T. Effects of prolactin and growth hormone on plasma immunoglobulin M levels of hypophysectomized rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol. 1999 ; 115: 46-52
8. Ushio-Fukai M. Compartmentalization of redox signaling through NADPH oxidase-derived ROS. Antioxid Redox Signal. 2009 ; 11: 1289-1299
9. Olavarría VH, Sepulcre MP, Figueroa JE, Mulero V. Prolactin-induced production of reactive oxygen species and IL-1β in leukocytes from the bony fish gilthead seabream involves Jak/Stat and NF-κB signaling pathways. J Immunol. 2010 ; 185: 3873-3883
10. Olavarría VH, Figueroa JE, Mulero V. Prolactin-induced activation of phagocyte NADPH oxidase in the teleost fish gilthead seabream involves the phosphorylation of p47phox by protein kinase C. Dev Comp Immunol. 2012 ; 36: 216-221
11. Huang B, Qi ZT, Xu Z, Nie P. Global characterization of IFN regulatory factor (IRF) genes in vertebrates: glimpse of the diversification in evolution. BMC Immunol. 2010 ; 5: 11-22
12. Nguyen H, Hiscott J, Pitha PM. The growing family of IFN regulatory factors. Cytokine Growth Factor Rev. 1997 ; 8: 293-312
13. Taniguchi T, Ogasawara K, Takaoka A, Tanaka N. IRF family of transcription factors as regulators of host defense. Annu Rev Immunol. 2001 ; 19: 623-655
14. Wang Y, O'Neal KD, Yu-Lee Ly. Multiple prolactin receptor cytoplasmic residues and Stat1 mediate prolactin signaling to the IRF-1 promoter. Mol Endocrinol. 1997 ; 11: 1353-1364
15. Goffin V, Binart N, Clement-Lacroix P, Bouchard B, Bole-Feysot C, Edery M, et al. From the molecular biology of prolactin and its receptor to the lessons learned from knockout mice models. Genet Anal Biomol Engin. 1999 ; 15: 189-201
16. Dogusan Z, Book ML, Verdood P, Yu-Lee Ly, Hooghe-Peters E. Prolactin activates IFN regulatory factor-1 expression in normal lympho-hemopoietic cells. Eur Cytokine Netwk. 2000 ; 11: 435-442
17. Dogusan Z, Hooghe R, Verdood P, Hooghe-Peters EL. Cytokine-like effects of prolactin in human mononuclear and polymorphonuclear leukocytes. J Neuroimmunol. 2001 ; 120: 58-66
18. Newburger PE, Ezekowitz RA, Whitney C, Wright J, Orkin SH. Induction of phagocyte cytochrome b heavy chain gene expression by IFN gamma. Proc Natl Acad Sci U S A. 1988 ; 85: 5215-5219
19. Cassatella MA, Hartman L, Perussia B, Trinchieri G. Tumor necrosis factor and immune IFN synergistically induce cytochrome b-245 heavy-chain gene expression and nicotinamide-adenine dinucleotide phosphate hydrogenase oxidase in human leukemic myeloid cells. J Clin Invest. 1989 ; 83: 1570-1579
20. Kumatori A, Yang D, Suzuki S, Nakamura M. Cooperation of STAT-1 and IRF-1 in IFN-gamma-induced transcription of the gp91(phox) gene. J Biol Chem. 2002 ; 15: 9103-9111
21. Thomas V, Samanta S, Wu C, Berliner N, Fikrig E. Anaplasma phagocytophilum modulates gp91phox gene expression through altered IFN regulatory factor 1 and PU.1 levels and binding of CCAAT displacement protein. Infect Immun. 2005 ; 73: 208-218
22. Yabu T, Hirose H, Hirono I, Katagiri T, Aoki T, Yamamoto E. Molecular cloning of a novel IFN regulatory factor in Japanese flounder, Paralichthys olivaceus. Mol Mar Biol Biotechnol. 1998 ; 7: 138-144
23. Richardson MP, Tay BH, Goh BY, Venkatesh B, Brenner S. Molecular cloning and genomic structure of a gene encoding IFN regulatory factor in the Pufferfish (Fugu rubripes). Mar Biotechnol (NY). 2001 ; 3: 145-151
24. Collet B, Secombes CJ. The rainbow trout (Oncorhynchus mykiss) Mx1 promoter Structural and functional characterization. Eur J Biochem. 2001 ; 268: 1577-1584
25. Ordás MC, Abollo E, Costa MM, Figueras A, Novoa B. Molecular cloning and expression analysis of IFN regulatory factor-1 (IRF-1) of turbot and sea bream. Mol Immunol. 2006 ; 43: 882-890
26. Jia W, Guo Q. Gene structures and promoter characteristics of IFN regulatory factor 1 (IRF-1), IRF-2 and IRF-7 from snakehead Channa argus. Mol Immunol. 2008 ; 45: 2419-2428
27. Yao CL, Kong P, Huang XN, Wang ZY. Molecular cloning and expression of IRF1 in large yellow croaker, Pseudosciaena crocea. Fish Shellfish Immunol. 2010 ; 28: 654-660
28. Bergan V, Steinsvik S, Xu H, Kileng Ø, Robertsen B. Promoters of type I IFN genes from Atlantic salmon contain two main regulatory regions. FEBS J. 2006 ; 273: 3893-3906
29. Dannevig BH, Brudeseth BE, Gjoen T, Rode M, Wergeland HI, Evensen Ø. Characterisation of a long-term cell line (SHK-1) developed from the head kidney of Atlantic salmon (Salmo salar). Fish Shellfish Immunol. 1997 ; 7: 213-226
30. Ma AC, Ward AC, Liang R, Leung AY. The role of jak2a in zebrafish hematopoiesis. Blood. 2007 ; 110: 1824-1830
31. Wang HD, Pagano PJ, Du Y. Superoxide anion from the adventitia of the rat thoracic aorta inactivates nitric oxide. Circ Res. 1998 ; 82: 810-818
32. Suh YA, Arnold RS, Lassegue B. Cell transformation by the superoxide generating oxidase Mox1. Nature. 1999 ; 401: 79-81
33. Sambrook J, Fritsch EF, Maniatis T Molecular cloning: a laboratory manual. 2 nd ed. Cold Spring Harbor, NY: Cold Spring Harbor, 1989. Cold Spring Harbor, NY: Cold Spring Harbor ; 1989 :
34. Sadowski HB, Shuai K, Darnell JE, Gilman MZ. A common nuclear signal transduction pathway activated by growth factor and cytokine receptors. Science. 1993 ; 261: 1739-1744
35. Nakajima K, Kusafuka T, Takeda T, Fujitani Y, Nakae K, Hirano T. Identification of a novel interleukin-6 response element containing an Ets binding site and a CRE-like site in the junB promoter. Mol Cell Biol. 1993 ; 13: 3027-3041
36. Olavarría VH, Gallardo L, Figueroa JE, Mulero V. Lipopolysaccharide primes the respiratory burst of Atlantic salmon SHK-1 cells through protein kinase C-mediated phosphorylation of p47phox. Dev Comp Immunol. 2010 ; 34: 1242-1253
37. Clevenger CV. Role of prolactin/prolactin receptor signaling in human breast cancer. Breast Dis. 2003 ; 18: 75-86
38. Boutet P, Sulon J, Closset R, Detilleux J, Beckers JF, Bureau F, Lekeux P. Prolactin-induced activation of nuclear factor kappaB in bovine mammary epithelial cells: role in chronic mastitis. J Dairy Sci. 2007 ; 90: 155-164
39. Quinn MT, Gauss KA. Structure and regulation of the neutrophil respiratory burst oxidase: comparison with nonphagocyte oxidases. J Leukoc Biol. 2004 ; 76: 760-778
40. El-Benna J, Dang PM, Gougerot-Pocidalo MA, Elbim C. Phagocyte NADPH oxidase: a multicomponent enzyme essential for host defenses. Arch Immunol Ther Exp. 2005 ; 53: 199-206
41. Groemping Y, Rittinger K. Activation and assembly of the NADPH oxidase: a structural perspective. Biochem J. 2005 ; 386: 401-416
42. Lai HL, Yang TH, Messing RO, Ching YH, Lin SC, Chern YJ. Protein kinase C inhibits adenylyl cyclase type VI activity during desensitization of the A2a-adenosine receptor-mediated cAMP response. J Biol Chem. 1997 ; 272: 4970-4977
43. Bole-Feysot C, Goffin V, Edery M, Binart N, Kelly PA. Prolactin (PRL) and its receptor: actions, signal transduction pathways and phenotypes observed in prl receptor knockout mice. Endocr Rev. 1998 ; 19: 225-268
44. Murakami M, Narazaki M, Hibi M, Yawata H, Yasukawa K, Hamaguchi M, et al. Critical cytoplasmic region of the interleukin-6 signal transducer, gp130, is conserved in the cytokine receptor family. Proc Natl Acad Sci U S A. 1991 ; 88: 11349-11353
45. Goffin V, Ferrag F, Kelly PA Advances in molecular and cellular endocrinology. Leroith D, ed. London: Jai ; 1998: 1-33.
46. Sandra O, Sohm F, de Luze A, Prunet P, Edery M, Kelly PA. Expression cloning of a cDNA encoding a fish prolactin receptor. Proc Natl Acad Sci U S A. 1995 ; 92: 6037-6041
47. Huang X, Jiao B, Fung CK, Zhang Y, Ho WK, Chan CB, et al. The presence of two distinct prolactin receptors in seabream with different tissue distribution patterns, signal transduction pathways and regulation of gene expression by steroid hormones. J Endocrinol. 2007 ; 194: 373-392
48. Campbell GS, Argetsinger LS, Ihle JN, Kelly PA, Rillema JA, Carter-Su C. Activation of jak2 tyrosine kinase by prolactin receptors in nb2 cells and mouse mammary gland explants. Proc Natl Acad Sci U S A. 1994 ; 91: 5232-5236
49. Ferrag F, Pezet A, Chiarenza A, Buteau H, Nelson BH, Goffin V, Kelly PA. Homodimerization of IL-2 receptor beta chain is necessary and sufficient to activate Jak2 and downstream signaling pathways. FEBS Lett. 1998 ; 421: 32-36
50. Tanaka N, Kawakami T, Taniguchi T. Recognition DNA sequences of IFN regulatory factor-1 (IRF-1) and IRF-2, regulators of cell growth and the IFN system. Mol Cell Biol. 1993 ; 13: 4531-4538
51. Yu-Lee L-Y. Molecular actions of prolactin in the immune system. Proc Soc Exp Biol Med. 1997 ; 215: 35-52
52. Li SL, Schlegel W, Valente AJ, Clark RA. Critical flanking sequences of PU.1 binding sites in myeloid-specific promoters. J Biol Chem. 1999 ; 274: 32453-32460
53. Suzuki S, Kumatori A, Haagen IA, Fujii Y, Sadat MA, Jun HL, et al. PU.1 as an essential activator for the expression of gp91 (phox) gene in human peripheral neutrophils, monocytes, and B lymphocytes. Proc Natl Acad Sci U S A. 1998 ; 95: 6085-6090
54. Eklund EA, Kakar R. Recruitment of CREB-binding protein by PU.1, IFN-regulatory factor-1, and the IFN consensus sequence-binding protein is necessary for IFN-gamma-induced p67phox and gp91phox expression. J Immunol. 1999 ; 163: 6095-6105