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PMID: 16025326 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

Characteristics of NADPH oxidase genes (Nox2, p22, p47, and p67) and Nox4 gene expressed in blood cells of juvenile Ciona intestinalis.

Immunogenetics ·Vol. 57 ·No. 7 ·2005-08-00 ·Pages 520-34

Inoue Y, Ogasawara M, Moroi T, Satake M, Azumi K, Moritomo T, Nakanishi T

Abstract

To illuminate the origins of NADPH oxidase (Nox), we identified cDNA clones encoding Nox2, Nox4, p22 phagocyte oxidase (phox), p47phox, and p67phox in a chordate phylogenetically distant to the vertebrates, the sea squirt Ciona intestinalis. We also examined the spatiotemporal expression of these genes in embryos and juveniles. The sequences of the Nox2, Nox4, p22phox, p47phox, and p67phox cDNAs contained open reading frames encoding 581, 811, 175, 461, and 515 amino acids, respectively. The level of identities between the deduced Nox2, Nox4, p22phox, p47phox, and p67phox amino acid sequences and their corresponding human components were 54.0, 31.0, 44.4, 36.0, and 26.2%, respectively. Despite these low identities, the functional domains of the C. intestinalis and human NADPH oxidase and Nox4 are highly conserved. The genomic organizations of the components of the NADPH oxidase gene except for p67phox (a single exon gene) and the Nox4 gene in C. intestinalis are highly similar to those of the corresponding human NADPH oxidase genes. Further, the analyzed part of the C. intestinalis genome and EST database do not seem to present p40phox and Nox5. The Nox2, p22phox, p47phox, and p67phox genes were specifically expressed in the blood cells of juveniles. The Nox4 gene was expressed in blood cells and endostyle of juveniles. These results suggest that C. intestinalis NADPH oxidase components possess potential functional activities similar to those of human, but the manner in which cytosolic phox proteins in C. intestinalis interact is different from that in human.

MeSH Terms
Amino Acid Sequence Animals Base Sequence Ciona intestinalis/enzymology,genetics,growth & development DNA, Complementary/genetics Gene Expression Regulation, Developmental Gene Expression Regulation, Enzymologic Genome Humans In Situ Hybridization Models, Biological Molecular Sequence Data NADPH Oxidase 4 NADPH Oxidases/blood,chemistry,genetics Phylogeny Sequence Homology, Amino Acid Species Specificity
Chemicals
DNA, Complementary NADPH Oxidase 4 NADPH Oxidases NOX4 protein, human
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Inoue Yuuki
Laboratory of Fish Pathology, Department of Veterinary Medicine, College of Bioresource Sciences, Nihon University, Kameino 1866, Fujisawa, Kanagawa, 252-8510, Japan, [email protected]
Ogasawara Michio
Moroi Takuma
Satake Masanobu
Azumi Kaoru
Moritomo Tadaaki
Nakanishi Teruyuki
References (49)
49 references, click to expand
  1. Tetratricopeptide repeat (TPR) motifs of p67(phox) participate in interaction with the small GTPase Rac and activation of the phagocyte NADPH oxidase.
    J Biol Chem. 1999 Aug 27;274(35):25051-60 PMID: 10455184
  2. Novel human homologues of p47phox and p67phox participate in activation of superoxide-producing NADPH oxidases.
    J Biol Chem. 2003 Jul 4;278(27):25234-46 PMID: 12716910
  3. Cell transformation by the superoxide-generating oxidase Mox1.
    Nature. 1999 Sep 2;401(6748):79-82 PMID: 10485709
  4. Novel modular domain PB1 recognizes PC motif to mediate functional protein-protein interactions.
    EMBO J. 2001 Aug 1;20(15):3938-46 PMID: 11483497
  5. NADPH oxidase activity is independent of p47phox in vitro.
    J Biol Chem. 1996 Sep 13;271(37):22578-82 PMID: 8798426
  6. Mapping sites of interaction of p47-phox and flavocytochrome b with random-sequence peptide phage display libraries.
    Proc Natl Acad Sci U S A. 1995 Jul 18;92(15):7110-4 PMID: 7624379
  7. The neighbor-joining method: a new method for reconstructing phylogenetic trees.
    Mol Biol Evol. 1987 Jul;4(4):406-25 PMID: 3447015
  8. Novel gp91(phox) homologues in vascular smooth muscle cells : nox1 mediates angiotensin II-induced superoxide formation and redox-sensitive signaling pathways.
    Circ Res. 2001 May 11;88(9):888-94 PMID: 11348997
  9. Mechanism for phosphorylation-induced activation of the phagocyte NADPH oxidase protein p47(phox). Triple replacement of serines 303, 304, and 328 with aspartates disrupts the SH3 domain-mediated intramolecular interaction in p47(phox), thereby activating the oxidase.
    J Biol Chem. 1999 Nov 19;274(47):33644-53 PMID: 10559253
  10. Functional analysis of two-amino acid substitutions in gp91 phox in a patient with X-linked flavocytochrome b558-positive chronic granulomatous disease by means of transgenic PLB-985 cells.
    Hum Genet. 2004 Oct;115(5):418-27 PMID: 15338276
  11. Gene expression profiles in young adult Ciona intestinalis.
    Dev Genes Evol. 2002 May;212(4):173-85 PMID: 12012232
  12. Creation of a genetic system for analysis of the phagocyte respiratory burst: high-level reconstitution of the NADPH oxidase in a nonhematopoietic system.
    Blood. 2002 Apr 15;99(8):2653-61 PMID: 11929750
  13. The phosphorylation of the respiratory burst oxidase component p47phox during neutrophil activation. Phosphorylation of sites recognized by protein kinase C and by proline-directed kinases.
    J Biol Chem. 1994 Sep 23;269(38):23431-6 PMID: 8089108
  14. Phosphorylation of p47phox directs phox homology domain from SH3 domain toward phosphoinositides, leading to phagocyte NADPH oxidase activation.
    Proc Natl Acad Sci U S A. 2003 Apr 15;100(8):4474-9 PMID: 12672956
  15. Inactivating mutations in the gene for thyroid oxidase 2 (THOX2) and congenital hypothyroidism.
    N Engl J Med. 2002 Jul 11;347(2):95-102 PMID: 12110737
  16. Reactive oxygen species generated by microbial NADPH oxidase NoxA regulate sexual development in Aspergillus nidulans.
    Mol Microbiol. 2003 Nov;50(4):1241-55 PMID: 14622412
  17. Tyrosine cross-linking of extracellular matrix is catalyzed by Duox, a multidomain oxidase/peroxidase with homology to the phagocyte oxidase subunit gp91phox.
    J Cell Biol. 2001 Aug 20;154(4):879-91 PMID: 11514595
  18. Site-specific inhibitors of NADPH oxidase activity and structural probes of flavocytochrome b: characterization of six monoclonal antibodies to the p22phox subunit.
    J Immunol. 2004 Dec 15;173(12):7349-57 PMID: 15585859
  19. Ciona intestinalis cDNA projects: expressed sequence tag analyses and gene expression profiles during embryogenesis.
    Gene. 2002 Apr 3;287(1-2):83-96 PMID: 11992726
  20. Zymosan induces production of superoxide anions by hemocytes of the solitary ascidian Halocynthia roretzi.
    Comp Biochem Physiol C Toxicol Pharmacol. 2002 Dec;133(4):567-74 PMID: 12458184
  21. Regulation of growth and apoptosis of cultured guinea pig gastric mucosal cells by mitogenic oxidase 1.
    Am J Physiol Gastrointest Liver Physiol. 2000 Dec;279(6):G1169-76 PMID: 11093939
  22. A point mutation in gp91-phox of cytochrome b558 of the human NADPH oxidase leading to defective translocation of the cytosolic proteins p47-phox and p67-phox.
    J Clin Invest. 1994 May;93(5):2120-6 PMID: 8182143
  23. Developmental expression of NADPH phagocytic oxidase components in mouse embryos.
    Pediatr Res. 1999 Aug;46(2):152-7 PMID: 10447107
  24. Intramembrane bis-heme motif for transmembrane electron transport conserved in a yeast iron reductase and the human NADPH oxidase.
    J Biol Chem. 1996 Dec 6;271(49):31021-4 PMID: 8940093
  25. Evaluation of the expression of NADPH oxidase components during maturation of HL-60 cells to neutrophil lineage.
    J Leukoc Biol. 2000 Aug;68(2):216-24 PMID: 10947066
  26. Direct interaction of the novel Nox proteins with p22phox is required for the formation of a functionally active NADPH oxidase.
    J Biol Chem. 2004 Oct 29;279(44):45935-41 PMID: 15322091
  27. Mapping of functional domains in the p22(phox) subunit of flavocytochrome b(559) participating in the assembly of the NADPH oxidase complex by "peptide walking".
    J Biol Chem. 2002 Mar 8;277(10):8421-32 PMID: 11733522
  28. Mutagenesis of an arginine- and lysine-rich domain in the gp91(phox) subunit of the phagocyte NADPH-oxidase flavocytochrome b558.
    J Biol Chem. 1999 Apr 9;274(15):10451-7 PMID: 10187835
  29. Mutagenesis of p22(phox) histidine 94. A histidine in this position is not required for flavocytochrome b558 function.
    J Biol Chem. 2002 Aug 16;277(33):30368-74 PMID: 12042318
  30. Solution structure of the PX domain, a target of the SH3 domain.
    Nat Struct Biol. 2001 Jun;8(6):526-30 PMID: 11373621
  31. Molecular cloning and sequencing of Japanese pufferfish (Takifugu rubripes) NADPH oxidase cDNAs.
    Dev Comp Immunol. 2004 Jul 1;28(9):911-25 PMID: 15183032
  32. Biosynthesis of the phagocyte NADPH oxidase cytochrome b558. Role of heme incorporation and heterodimer formation in maturation and stability of gp91phox and p22phox subunits.
    J Biol Chem. 1997 Oct 24;272(43):27288-94 PMID: 9341176
  33. Regulation of the neutrophil respiratory burst oxidase. Identification of an activation domain in p67(phox).
    J Biol Chem. 1998 Jul 3;273(27):16663-8 PMID: 9642219
  34. Phagocytosis in the colonial ascidian Botryllus schlosseri.
    Dev Comp Immunol. 1994 Nov-Dec;18(6):467-81 PMID: 7768314
  35. Homologs of gp91phox: cloning and tissue expression of Nox3, Nox4, and Nox5.
    Gene. 2001 May 16;269(1-2):131-40 PMID: 11376945
  36. Heme-ligating histidines in flavocytochrome b(558): identification of specific histidines in gp91(phox).
    J Biol Chem. 2001 Aug 17;276(33):31105-12 PMID: 11413138
  37. The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins.
    Science. 2002 Dec 13;298(5601):2157-67 PMID: 12481130
  38. Novel homologs of gp91phox.
    Trends Biochem Sci. 2000 Oct;25(10):459-61 PMID: 11050424
  39. Diverse recognition of non-PxxP peptide ligands by the SH3 domains from p67(phox), Grb2 and Pex13p.
    EMBO J. 2002 Aug 15;21(16):4268-76 PMID: 12169629
  40. NOX enzymes and the biology of reactive oxygen.
    Nat Rev Immunol. 2004 Mar;4(3):181-9 PMID: 15039755
  41. TreeView: an application to display phylogenetic trees on personal computers.
    Comput Appl Biosci. 1996 Aug;12(4):357-8 PMID: 8902363
  42. Cytochrome b558, a component of the phagocyte NADPH oxidase, is a flavoprotein.
    Biochem Biophys Res Commun. 1992 Aug 14;186(3):1368-75 PMID: 1324665
  43. p40phox, a third cytosolic component of the activation complex of the NADPH oxidase to contain src homology 3 domains.
    Biochem J. 1993 Dec 15;296 ( Pt 3):557-61 PMID: 8280052
  44. NOX3, a superoxide-generating NADPH oxidase of the inner ear.
    J Biol Chem. 2004 Oct 29;279(44):46065-72 PMID: 15326186
  45. Superoxide release and NADPH oxidase components in mature human phagocytes: correlation between functional capacity and amount of functional proteins.
    Biochem Biophys Res Commun. 1996 Nov 12;228(2):510-6 PMID: 8920944
  46. An SH3 domain and proline-rich sequence mediate an interaction between two components of the phagocyte NADPH oxidase complex.
    J Biol Chem. 1994 May 13;269(19):13752-5 PMID: 8188650
  47. A novel superoxide-producing NAD(P)H oxidase in kidney.
    J Biol Chem. 2001 Jan 12;276(2):1417-23 PMID: 11032835
  48. The superoxide-generating NADPH oxidase: structural aspects and activation mechanism.
    Cell Mol Life Sci. 2002 Sep;59(9):1428-59 PMID: 12440767
  49. Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91phox).
    Plant J. 1998 May;14(3):365-70 PMID: 9628030
Article Info
Journal
Immunogenetics
Abbr.
Immunogenetics
ISSN
0093-7711
Published
2005-08-00
Epub
2005-00-29
Pages
520-34
Language
English
Region
United States
NLM ID
0420404
Subset
IM
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