Dual targeting of the protein disulfide isomerase RB60 to the chloroplast and the endoplasmic reticulum

Levitan, Alexander; Trebitsh, Tova; Kiss, Vladimir; Pereg, Yaron; Dangoor, Inbal; Danon, Avihai

doi:10.1073/pnas.0500676102

Cited by 93 publications

(83 citation statements)

References 48 publications

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“…the nucleus), whereas SRP binding would lead to co-translational insertion into the ER. This mechanism has been proposed for the dual localization of the PDI, RB60 (which contains a signal peptide and C-terminal KDEL), to the ER and chloroplast in Chlamydomonas (Levitan et al, 2005). Post-translational insertion of the signal peptide-containing polypeptide was observed in a few cases in animals, yeast and plants (Cramer et al, 1987;Plath et al, 1998;Rapoport et al, 1999).…”

Section: Discussionmentioning

confidence: 89%

Protein Disulfide Isomerase-2 of Arabidopsis Mediates Protein Folding and Localizes to Both the Secretory Pathway and Nucleus, Where It Interacts with Maternal Effect Embryo Arrest Factor

Cho

Yuen

Kang

et al. 2011

Molecules and Cells

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Protein disulfide isomerase (PDI) is a thiodisulfide oxidoreductase that catalyzes the formation, reduction and rearrangement of disulfide bonds in proteins of eukaryotes. The classical PDI has a signal peptide, two CXXCcontaining thioredoxin catalytic sites (a,a′), two noncatalytic thioredoxin fold domains (b,b′), an acidic domain (c) and a C-terminal endoplasmic reticulum (ER) retention signal. Although PDI resides in the ER where it mediates the folding of nascent polypeptides of the secretory pathway, we recently showed that PDI5 of Arabidopsis thaliana chaperones and inhibits cysteine proteases during trafficking to vacuoles prior to programmed cell death of the endothelium in developing seeds. Here we describe Arabidopsis PDI2, which shares a primary structure similar to that of classical PDI. Recombinant PDI2 is imported into ER-derived microsomes and complements the E. coli protein-folding mutant, dsbA. PDI2 interacted with proteins in both the ER and nucleus, including ER-resident protein folding chaperone, BiP1, and nuclear embryo transcription factor, MEE8. The PDI2-MEE8 interaction was confirmed to occur in vitro and in vivo. Transient expression of PDI2-GFP fusions in mesophyll protoplasts resulted in labeling of the ER, nucleus and vacuole. PDI2 is expressed in multiple tissues, with relatively high expression in seeds and root tips. Immunoelectron microscopy with GFP-and PDI2-specific antisera on transgenic seeds (PDI2-GFP) and wild type roots demonstrated that PDI2 was found in the secretory pathway (ER, Golgi, vacuole, cell wall) and the nuclei. Our results indicate that PDI2 mediates protein folding in the ER and has new functional roles in the nucleus.

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Section: Discussionmentioning

confidence: 89%

Protein Disulfide Isomerase-2 of Arabidopsis Mediates Protein Folding and Localizes to Both the Secretory Pathway and Nucleus, Where It Interacts with Maternal Effect Embryo Arrest Factor

Cho

Yuen

Kang

et al. 2011

Molecules and Cells

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“…As shown in Fig. 4D, a small proportion of MSC1 immunolabeling overlapped with labeling for KDEL, the endoplasmic reticulum retention signal sequence that is known to label punctate spots in the cytoplasm and chloroplast of Chlamydomonas (16). No MSC1 labeling colocalized with the markers for other organelles such as the phosphate body, Golgi apparatus, mitochondria, and lysosome (data not shown).…”

Section: Molecular Identification Of Msc1mentioning

confidence: 97%

Molecular and electrophysiological characterization of a mechanosensitive channel expressed in the chloroplasts of Chlamydomonas

Nakayama

Fujiu

Sokabe

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

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MscS is a mechanosensitive channel that is ubiquitous among bacteria. Recent progress in the genome projects has revealed that homologs of MscS are also present in eukaryotes, but whether they operate as ion channels is unknown. In this study we cloned MSC1, a homolog of MscS in Chlamydomonas, and examined its function when expressed in Escherichia coli. Full-length MSC1 was not functional when expressed in E. coli cells. However, removal of the N-terminal signal sequence (⌬N-MSC1) reversed this effect. ⌬N-MSC1 was found to open in response to membrane stretch and displayed a preference for anions over cations as permeable ions. ⌬N-MSC1 exhibited marked hysteretic behavior in response to ascending and descending stimuli. That is, channel gating occurred in response to significant stimuli but remained open until the stimulus was almost completely removed. Indirect immunofluorescence revealed that MSC1 is present as punctate spots in the cytoplasm and chloroplasts. Moreover, knockdown of MSC1 expression resulted in the abnormal localization of chlorophyll. These findings show that MSC1 is an intracellular mechanosensitive channel and is responsible for the organization of chloroplast in Chlamydomonas.MscS ͉ hysteresis ͉ heterogeneous expression ͉ knockdown ͉ green algae M echanosensation is typically involved in auditory perception, touch sensation, proprioception, and gravity perception. The mechanoreceptor potential in sensory cells is mediated by mechanosensitive channels, which are activated by stretching or deformation of the membrane. The patch-clamp technique has revealed that mechanosensitive channels are present in almost every cell type, not just sensory cells. In fact, mechanosensitive channels were first recorded with the patch-clamp method in the muscle cell (1). Mechanosensitive channels in nonsensory cells are believed to be responsible for monitoring cell deformation evoked by contact with surrounding materials and by changes in osmolarity.Bacteria harbor the mechanosensitive channels MscS and MscL, which act to protect against hypoosmotic downshock (2). The presence of MscS homologs in virtually all eubacteria and archaea suggests that MscS has an essential function in prokaryotes, but whether every MscS homolog serves as a mechanosensitive channel is uncertain. For instance, although there are at least six MscS homologs in the Escherichia coli genome, only two of them (MscS and MscK) have been detected by electrophysiological methods (3, 4). Recent genomic projects on eukaryotes have uncovered the presence of MscS homologs in some plants (Arabidopsis and Oryza), protists (Chlamydomonas), and fungi (Schizosaccharomyces). Curiously, MscS homologs have not been found in animals (5, 6). The MscS homologs of Arabidopsis (MSL2 and MSL3) have been observed as one or two foci on the plastid envelope, and their double knockout results in an abnormal size and shape of the plastids (6). This finding suggests that one of the possible functions of the MscS homologs is to control the size and shape of the intr...

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“…Moreover, administration of vitamin A, an 11-cis-retinal precursor, is beneficial to RP patients (Berson et al, 1993a,b;Berson, 2000). However, light-influenced changes in the expression of chaperones (Li and Guy, 2001;Levitan et al, 2005) or components of the ER-associated degradation (ERAD) pathway may also influence the equilibrium between folding, cleavage and degradation. Interestingly, this result also suggests that 11-cis-retinal is available to opsin in the RIS during biosynthesis and not only in the ROS.…”

Section: Discussionmentioning

confidence: 99%

Dark Rearing Rescues P23H Rhodopsin-Induced Retinal Degeneration in a TransgenicXenopus laevisModel of Retinitis Pigmentosa: A Chromophore-Dependent Mechanism Characterized by Production of N-Terminally Truncated Mutant Rhodopsin

Tam¹,

Moritz²

2007

J. Neurosci.

100

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To elucidate the molecular mechanisms underlying the light-sensitive retinal degeneration caused by the rhodopsin mutation P23H, which causes retinitis pigmentosa (RP) in humans, we expressed Xenopus laevis, bovine, human, and murine forms of P23H rhodopsin in transgenic X. laevis rod photoreceptors. All P23H rhodopsins caused aggressive retinal degeneration associated with low expression levels and retention of P23H rhodopsin in the endoplasmic reticulum (ER), suggesting involvement of protein misfolding and ER stress. However, light sensitivity varied dramatically between these RP models, with complete or partial rescue by dark rearing in the case of bovine and human P23H rhodopsin, and no rescue for X. laevis P23H rhodopsin. Rescue by dark rearing required an intact 11-cis-retinal chromophore binding site within the mutant protein and was associated with truncation of the P23H rhodopsin N terminus. This yielded an abundant nontoxic ϳ27 kDa form that escaped the ER and was transported to the rod outer segment. The truncated protein was produced in the greatest quantities in dark-reared retinas expressing bovine P23H rhodopsin and was not observed with X. laevis P23H rhodopsin. These results are consistent with a mechanism involving enhanced protein folding in the presence of 11-cis-retinal chromophore, with ER exit assisted by proteolytic truncation of the N terminus. This study provides a molecular mechanism for light sensitivity observed in other transgenic models of RP and for phenotypic variation among RP patients.

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Dual targeting of the protein disulfide isomerase RB60 to the chloroplast and the endoplasmic reticulum

Cited by 93 publications

References 48 publications

Protein Disulfide Isomerase-2 of Arabidopsis Mediates Protein Folding and Localizes to Both the Secretory Pathway and Nucleus, Where It Interacts with Maternal Effect Embryo Arrest Factor

Protein Disulfide Isomerase-2 of Arabidopsis Mediates Protein Folding and Localizes to Both the Secretory Pathway and Nucleus, Where It Interacts with Maternal Effect Embryo Arrest Factor

Molecular and electrophysiological characterization of a mechanosensitive channel expressed in the chloroplasts of Chlamydomonas

Dark Rearing Rescues P23H Rhodopsin-Induced Retinal Degeneration in a TransgenicXenopus laevisModel of Retinitis Pigmentosa: A Chromophore-Dependent Mechanism Characterized by Production of N-Terminally Truncated Mutant Rhodopsin

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