Differential cell surface recruitment of the superoxide-producing NADPH oxidases Nox1, Nox2 and Nox5: The role of the small GTPase Sar1

Genes Cells. 2018 Jun;23(6):480-493. doi: 10.1111/gtc.12590. Epub 2018 May 2.

Abstract

Transmembrane glycoproteins, synthesized at the endoplasmic reticulum (ER), generally reach the Golgi apparatus in COPII-coated vesicles en route to the cell surface. Here, we show that the bona fide nonglycoprotein Nox5, a transmembrane superoxide-producing NADPH oxidase, is transported to the cell surface in a manner resistant to co-expression of Sar1 (H79G), a GTP-fixed mutant of the small GTPase Sar1, which blocks COPII vesicle fission from the ER. In contrast, Sar1 (H79G) effectively inhibits ER-to-Golgi transport of glycoproteins including the Nox5-related oxidase Nox2. The trafficking of Nox2, but not that of Nox5, is highly sensitive to over-expression of syntaxin 5 (Stx5), a t-SNARE required for COPII ER-to-Golgi transport. Thus, Nox2 and Nox5 mainly traffic via the Sar1/Stx5-dependent and -independent pathways, respectively. Both participate in Nox1 trafficking, as Nox1 advances to the cell surface in two differentially N-glycosylated forms, one complex and one high mannose, in a Sar1/Stx5-dependent and -independent manner, respectively. Nox2 and Nox5 also can use both pathways: a glycosylation-defective mutant Nox2 is weakly recruited to the plasma membrane in a less Sar1-dependent manner; N-glycosylated Nox5 mutants reach the cell surface in part as the complex form Sar1-dependently, albeit mainly as the high-mannose form in a Sar1-independent manner.

Keywords: N-linked glycosylation; NADPH oxidase; Nox1; Nox2; Nox5; Sar1; plasma membrane; protein targeting; reactive oxygen species.

MeSH terms

  • Amino Acid Sequence
  • Cell Membrane / metabolism*
  • Endoplasmic Reticulum / metabolism
  • Glycosylation
  • Golgi Apparatus / metabolism
  • HeLa Cells
  • Humans
  • Monomeric GTP-Binding Proteins / metabolism*
  • Mutation
  • NADPH Oxidase 1 / genetics
  • NADPH Oxidase 1 / metabolism
  • NADPH Oxidase 2 / genetics
  • NADPH Oxidase 2 / metabolism
  • NADPH Oxidase 5 / metabolism*
  • Protein Transport
  • Sequence Homology
  • Superoxides / metabolism*

Substances

  • Superoxides
  • CYBB protein, human
  • NADPH Oxidase 1
  • NADPH Oxidase 2
  • NADPH Oxidase 5
  • NOX1 protein, human
  • NOX5 protein, human
  • SAR1A protein, human
  • Monomeric GTP-Binding Proteins