ER membrane-localized oxidoreductase Ero1 is required for disulfide bond formation in the rice endosperm

Onda, Yayoi; Kumamaru, Toshihiro; Kawagoe, Yasuhiro

doi:10.1073/pnas.0904429106

Cited by 96 publications

(165 citation statements)

References 36 publications

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“…It is worth noting that a huge amount of Zera-ECFP enters the ER in the transient expression system used and that the ER needs to accommodate the redox homeostasis by maintaining sufficient oxidizing conditions within the lumen. This is achieved by interplay between the enzyme proteindisulfide isomerase (50,51), oxidoreductases, such as the flavoprotein Ero1 recently described in rice (52), and glutathione as the redox buffer.…”

Section: Discussionmentioning

confidence: 99%

Relevant Elements of a Maize γ-Zein Domain Involved in Protein Body Biogenesis

Llop‐Tous

Madurga

Giralt

et al. 2010

Journal of Biological Chemistry

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The N-terminal proline-rich domain of ␥-zein (Zera) plays an important role in protein body (PB) formation not only in the original host (maize seeds) but in a broad spectrum of eukaryotic cells. However, the elements within the Zera sequence that are involved in the biogenesis of PBs have not been clearly identified. Here, we focused on amino acid sequence motifs that could be involved in Zera oligomerization, leading to PB-like structures in Nicotiana benthamiana leaves. By using fusions of Zera with fluorescent proteins, we found that the lack of the repeat region (PPPVHL) 8 of Zera resulted in the secretion of the fusion protein but that this repeat by itself did not form PBs. Although the repeat region containing eight units was the most efficient for Zera self-assembly, shorter repeats of 4 -6 units still formed small multimers. Based on site-directed mutagenesis of Zera cysteine residues and analysis of multimer formation, we conclude that the two N-terminal Cys residues of Zera (Cys 7 and Cys 9 ) are critical for oligomerization. Immunoelectron microscopy and confocal studies on PB development over time revealed that early, small, Zera-derived oligomers were sequestered in buds along the rough ER and that the mature size of the PBs could be attained by both cross-linking of preformed multimers and the incorporation of new chains of Zera fusions synthesized by active membrane-bound ribosomes. Based on these results and on the behavior of the Zera structure determined by molecular dynamics simulation studies, we propose a model of Zera-induced PB biogenesis.The mechanisms by which prolamins, which lack the ER 3 retention (H/K)DEL motif, are retained and assembled in the ER-derived PBs are only partially understood. Different factors act as determinants of PB biogenesis, some of them derived from cis-cargo properties and others with a cellular trans-origin (1). It has been proposed that the physico-chemical properties of prolamins, such as hydrophobicity and disulfide bond formation, promote specific interactions resulting in the formation of large self-assemblies that are responsible for their retention in the ER and PB formation (2-4). These polymers could be excluded because of their size from being carried by the COP II vesicles that transport cargo proteins to the Golgi complex (5). However, the generic COPII vesicles are flexible enough for large cargo loading, including that of procollagen (more than 300 nm in size) (6) and the collagen VII trimer (900 kDa) (7).In maize, four distinct types of prolamins (␣-, ␤-, ␥-, and ␦-zein) coexist in the PBs (8) and play distinct roles in PB formation. Recently, maize storage protein mutants created through RNAi showed that ␥-RNAi maize mutant lines exhibited slightly altered protein body formation and that a more drastic effect was observed in the ␤-␥ combined mutant, where protein bodies showed an irregular shape, particularly in their periphery (9).Various studies on zein accumulation in heterologous expression systems suggest that ␥-zein and ␤-zein mediate t...

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Section: Discussionmentioning

confidence: 99%

Relevant Elements of a Maize γ-Zein Domain Involved in Protein Body Biogenesis

Llop‐Tous

Madurga

Giralt

et al. 2010

Journal of Biological Chemistry

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“…Another possibility could be a tight association of Ero1α with the MAM membrane, which has been shown to exhibit specific lipid composition (Sano et al 2009). Similar to the characterization of the rice Ero1α ER targeting mechanism (Onda et al 2009), we expect a detailed analysis of the Ero1α peptide sequence to yield information concerning a novel targeting mechanism for ER oxidoreductases and chaperones to the MAM. We further expect such a targeting mechanism to have important implications on cell survival and protein secretion.…”

Section: Discussionmentioning

confidence: 99%

“…Another factor that impacts on the catalytic activity of Ero1 proteins is their correct localization to the ER. Both yeast and rice Ero1 proteins require association with the ER membrane for their functioning (Onda et al 2009;Pagani et al 2001). Human Ero1α requires the interaction with PDI and another oxidoreductase, ERp44, for its retention within the ER (Anelli et al 2003;Otsu et al 2006).…”

Section: Introductionmentioning

confidence: 99%

Ero1α requires oxidizing and normoxic conditions to localize to the mitochondria-associated membrane (MAM)

Gilady

Bui

Lynes

et al. 2010

Cell Stress and Chaperones

159

115

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Protein secretion from the endoplasmic reticulum (ER) requires the enzymatic activity of chaperones and oxidoreductases that fold polypeptides and form disulfide bonds within newly synthesized proteins. The best-characterized ER redox relay depends on the transfer of oxidizing equivalents from molecular oxygen through ER oxidoreductin 1 (Ero1) and protein disulfide isomerase to nascent polypeptides. The formation of disulfide bonds is, however, not the sole function of ER oxidoreductases, which are also important regulators of ER calcium homeostasis. Given the role of human Ero1α in the regulation of the calcium release by inositol 1,4,5-trisphosphate receptors during the onset of apoptosis, we hypothesized that Ero1α may have a redox-sensitive localization to specific domains of the ER. Our results show that within the ER, Ero1α is almost exclusively found on the mitochondria-associated membrane (MAM). The localization of Ero1α on the MAM is dependent on oxidizing conditions within the ER. Chemical reduction of the ER environment, but not ER stress in general leads to release of Ero1α from the MAM. In addition, the correct localization of Ero1α to the MAM also requires normoxic conditions, but not ongoing oxidative phosphorylation.

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“…For localization analysis of TIP3 protein, we made a translational fusion between the full-length TIP3 and GFP driven by TIP3's native promoter (PTIP3:TIP3-GFP) according to a previous report (Onda et al, 2009). The construct was introduced into the EHA105 strain and used to infect calli of the indica var N22 and recessive gpa3 lines isolated from a gpa3/02428 F3 population.…”

Section: Vector Construction and Rice Transformationmentioning

confidence: 99%

GLUTELIN PRECURSOR ACCUMULATION3Encodes a Regulator of Post-Golgi Vesicular Traffic Essential for Vacuolar Protein Sorting in Rice Endosperm

et al. 2014

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In seed plants, a major pathway for sorting of storage proteins to the protein storage vacuole (PSV) depends on the Golgi-derived dense vesicles (DVs). However, the molecular mechanisms regulating the directional trafficking of DVs to PSVs remain largely elusive. Here, we report the functional characterization of the rice (Oryza sativa) glutelin precursor accumulation3 (gpa3) mutant, which exhibits a floury endosperm phenotype and accumulates excess proglutelins in dry seeds. Cytological and immunocytochemistry studies revealed that in the gpa3 mutant, numerous proglutelin-containing DVs are misrouted to the plasma membrane and, via membrane fusion, release their contents into the apoplast to form a new structure named the paramural body. Positional cloning of GPA3 revealed that it encodes a plant-specific kelch-repeat protein that is localized to the trans-Golgi networks, DVs, and PSVs in the developing endosperm. In vitro and in vivo experiments verified that GPA3 directly interacts with the rice Rab5a-guanine exchange factor VPS9a and forms a regulatory complex with Rab5a via VPS9a. Furthermore, our genetic data support the notion that GPA3 acts synergistically with Rab5a and VPS9a to regulate DV-mediated post-Golgi traffic in rice. Our findings provide insights into the molecular mechanisms regulating the plant-specific PSV pathway and expand our knowledge of vesicular trafficking in eukaryotes.

show abstract

ER membrane-localized oxidoreductase Ero1 is required for disulfide bond formation in the rice endosperm

Cited by 96 publications

References 36 publications

Relevant Elements of a Maize γ-Zein Domain Involved in Protein Body Biogenesis

Relevant Elements of a Maize γ-Zein Domain Involved in Protein Body Biogenesis

Ero1α requires oxidizing and normoxic conditions to localize to the mitochondria-associated membrane (MAM)

GLUTELIN PRECURSOR ACCUMULATION3Encodes a Regulator of Post-Golgi Vesicular Traffic Essential for Vacuolar Protein Sorting in Rice Endosperm

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