Home LiteratureArticle Details
PMID: 19995913 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, P.H.S.

Structural insights into Nox4 and Nox2: motifs involved in function and cellular localization.

Molecular and cellular biology ·Vol. 30 ·No. 4 ·2010-02-00 ·Pages 961-75

von Löhneysen K, Noack D, Wood MR, Friedman JS, Knaus UG

Abstract

Regulated generation of reactive oxygen species (ROS) is primarily accomplished by NADPH oxidases (Nox). Nox1 to Nox4 form a membrane-associated heterodimer with p22(phox), creating the docking site for assembly of the activated oxidase. Signaling specificity is achieved by interaction with a complex network of cytosolic components. Nox4, an oxidase linked to cardiovascular disease, carcinogenesis, and pulmonary fibrosis, deviates from this model by displaying constitutive H(2)O(2) production without requiring known regulators. Extensive Nox4/Nox2 chimera screening was initiated to pinpoint structural motifs essential for ROS generation and Nox subcellular localization. In summary, a matching B loop was crucial for catalytic activity of both Nox enzymes. Substitution of the carboxyl terminus was sufficient for converting Nox4 into a phorbol myristate acetate (PMA)-inducible phenotype, while Nox2-based chimeras never gained constitutive activity. Changing the Nox2 but not the Nox4 amino terminus abolished ROS generation. The unique heterodimerization of a functional Nox4/p22(phox) Y121H complex was dependent on the D loop. Nox4, Nox2, and functional Nox chimeras translocated to the plasma membrane. Cell surface localization of Nox4 or PMA-inducible Nox4 did not correlate with O(2)(-) generation. In contrast, Nox4 released H(2)O(2) and promoted cell migration. Our work provides insights into Nox structure, regulation, and ROS output that will aid inhibitor design.

MeSH Terms
Amino Acid Motifs Biocatalysis Cell Line Cell Movement Cell Survival Humans Membrane Glycoproteins/chemistry,genetics,metabolism Microscopy, Electron NADPH Oxidase 2 NADPH Oxidase 4 NADPH Oxidases/chemistry,genetics,metabolism Reactive Oxygen Species/metabolism
Chemicals
Membrane Glycoproteins Reactive Oxygen Species CYBB protein, human NADPH Oxidase 2 NADPH Oxidase 4 NADPH Oxidases NOX4 protein, human
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
von Löhneysen Katharina
Department of Immunology and Microbial Science, Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, California 92037, USA.
Noack Deborah
Wood Malcolm R
Friedman Jeffrey S
Knaus Ulla G
References (37)
37 references, click to expand
  1. Mutation of the Cyba gene encoding p22phox causes vestibular and immune defects in mice.
    J Clin Invest. 2008 Mar;118(3):1176-85 PMID: 18292807
  2. 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
  3. Leu505 of Nox2 is crucial for optimal p67phox-dependent activation of the flavocytochrome b558 during phagocytic NADPH oxidase assembly.
    J Leukoc Biol. 2007 Jan;81(1):238-49 PMID: 17060362
  4. Mutational analysis reveals distinct features of the Nox4-p22 phox complex.
    J Biol Chem. 2008 Dec 12;283(50):35273-82 PMID: 18849343
  5. Structure, regulation and evolution of Nox-family NADPH oxidases that produce reactive oxygen species.
    FEBS J. 2008 Jul;275(13):3249-77 PMID: 18513324
  6. Dual oxidase-2 has an intrinsic Ca2+-dependent H2O2-generating activity.
    J Biol Chem. 2005 Aug 26;280(34):30046-54 PMID: 15972824
  7. Distinct subcellular localizations of Nox1 and Nox4 in vascular smooth muscle cells.
    Arterioscler Thromb Vasc Biol. 2004 Apr;24(4):677-83 PMID: 14670934
  8. Redox changes of cultured endothelial cells and actin dynamics.
    Circ Res. 2000 Mar 17;86(5):549-57 PMID: 10720417
  9. 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
  10. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology.
    Physiol Rev. 2007 Jan;87(1):245-313 PMID: 17237347
  11. Topological mapping of neutrophil cytochrome b epitopes with phage-display libraries.
    J Biol Chem. 1995 Jul 14;270(28):16974-80 PMID: 7622517
  12. Heterodimerization controls localization of Duox-DuoxA NADPH oxidases in airway cells.
    J Cell Sci. 2009 Apr 15;122(Pt 8):1238-47 PMID: 19339556
  13. Monoclonal antibody 7D5 raised to cytochrome b558 of human neutrophils: immunocytochemical detection of the antigen in peripheral phagocytes of normal subjects, patients with chronic granulomatous disease, and their carrier mothers.
    Blood. 1987 May;69(5):1404-8 PMID: 3552074
  14. Critical roles for p22phox in the structural maturation and subcellular targeting of Nox3.
    Biochem J. 2007 Apr 1;403(1):97-108 PMID: 17140397
  15. NADPH oxidase.
    Curr Opin Immunol. 2004 Feb;16(1):42-7 PMID: 14734109
  16. Involvement of Rac1 in activation of multicomponent Nox1- and Nox3-based NADPH oxidases.
    Mol Cell Biol. 2006 Mar;26(6):2160-74 PMID: 16507994
  17. Point mutations in the proline-rich region of p22phox are dominant inhibitors of Nox1- and Nox2-dependent reactive oxygen generation.
    J Biol Chem. 2005 Sep 9;280(36):31859-69 PMID: 15994299
  18. NOX4 activity is determined by mRNA levels and reveals a unique pattern of ROS generation.
    Biochem J. 2007 Aug 15;406(1):105-14 PMID: 17501721
  19. Functional analysis of Nox4 reveals unique characteristics compared to other NADPH oxidases.
    Cell Signal. 2006 Jan;18(1):69-82 PMID: 15927447
  20. Crucial role of two potential cytosolic regions of Nox2, 191TSSTKTIRRS200 and 484DESQANHFAVHHDEEKD500, on NADPH oxidase activation.
    J Biol Chem. 2005 Apr 15;280(15):14962-73 PMID: 15684431
  21. The superoxide-generating NADPH oxidase: structural aspects and activation mechanism.
    Cell Mol Life Sci. 2002 Sep;59(9):1428-59 PMID: 12440767
  22. Direct involvement of the small GTPase Rac in activation of the superoxide-producing NADPH oxidase Nox1.
    J Biol Chem. 2006 Aug 4;281(31):21857-21868 PMID: 16762923
  23. 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
  24. Regulated hydrogen peroxide production by Duox in human airway epithelial cells.
    Am J Respir Cell Mol Biol. 2005 May;32(5):462-9 PMID: 15677770
  25. Characterization of two monoclonal antibodies against cytochrome b558 of human neutrophils.
    Blood. 1989 May 1;73(6):1686-94 PMID: 2469497
  26. Identification of structural elements in Nox1 and Nox4 controlling localization and activity.
    Antioxid Redox Signal. 2009 Jun;11(6):1279-87 PMID: 19061439
  27. Molecular evolution of the reactive oxygen-generating NADPH oxidase (Nox/Duox) family of enzymes.
    BMC Evol Biol. 2007 Jul 06;7:109 PMID: 17612411
  28. Cloning and sequencing of the bovine flavocytochrome b subunit proteins, gp91-phox and p22-phox: comparison with other known flavocytochrome b sequences.
    J Leukoc Biol. 1998 Jul;64(1):114-23 PMID: 9665285
  29. Identification of a conserved Rac-binding site on NADPH oxidases supports a direct GTPase regulatory mechanism.
    J Biol Chem. 2008 May 9;283(19):12736-46 PMID: 18347018
  30. The superoxide-producing NAD(P)H oxidase Nox4 in the nucleus of human vascular endothelial cells.
    Genes Cells. 2005 Dec;10(12):1139-51 PMID: 16324151
  31. Regulation of Nox and Duox enzymatic activity and expression.
    Free Radic Biol Med. 2007 Aug 1;43(3):319-31 PMID: 17602947
  32. A novel superoxide-producing NAD(P)H oxidase in kidney.
    J Biol Chem. 2001 Jan 12;276(2):1417-23 PMID: 11032835
  33. 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
  34. Deletion mutagenesis of p22phox subunit of flavocytochrome b558: identification of regions critical for gp91phox maturation and NADPH oxidase activity.
    J Biol Chem. 2006 Oct 13;281(41):30336-46 PMID: 16895900
  35. 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
  36. The NADPH oxidase Nox3 constitutively produces superoxide in a p22phox-dependent manner: its regulation by oxidase organizers and activators.
    J Biol Chem. 2005 Jun 17;280(24):23328-39 PMID: 15824103
  37. 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
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
1098-5549
Published
2010-02-00
Epub
2009-00-07
Pages
961-75
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC2815567
Subset
IM
Grants
NIAID NIH HHS · R21 AI077042 · United States
NCPDCID CDC HHS · CI000095 · United States
NIAID NIH HHS · R01 AI024838 · United States
NIAID NIH HHS · AI077042 · United States
NCPDCID CDC HHS · P01 CI000095 · United States
NIAID NIH HHS · AI024838 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]