deltaPKC participates in the endoplasmic reticulum stress-induced response in cultured cardiac myocytes and ischemic heart - PubMed (original) (raw)
deltaPKC participates in the endoplasmic reticulum stress-induced response in cultured cardiac myocytes and ischemic heart
Xin Qi et al. J Mol Cell Cardiol. 2007 Oct.
Abstract
The cellular response to excessive endoplasmic reticulum (ER) stress includes the activation of signaling pathways, which lead to apoptotic cell death. Here we show that treatment of cultured cardiac myocytes with tunicamycin, an agent that induces ER stress, causes the rapid translocation of deltaPKC to the ER. We further demonstrate that inhibition of deltaPKC using the deltaPKC-specific antagonist peptide, deltaV1-1, reduces tunicamycin-induced apoptotic cell death, and inhibits expression of specific ER stress response markers such as CHOP, GRP78 and phosphorylation of JNK. The physiological importance of deltaPKC in this event is further supported by our findings that the ER stress response is also induced in hearts subjected to ischemia and reperfusion injury and that this response also involves deltaPKC translocation to the ER. We found that the levels of the ER chaperone, GRP78, the spliced XBP-1 and the phosphorylation of JNK are all increased following ischemia and reperfusion and that deltaPKC inhibition by deltaV1-1 blocks these events. Therefore, ischemia-reperfusion injury induces ER stress in the myocardium in a mechanism that requires deltaPKC activity. Taken together, our data show for the first time that deltaPKC activation plays a critical role in the ER stress-mediated response and the resultant cell death.
Figures
Fig 1. δPKC activation modulates tunicamycin-induced cell death and apoptosis in cardiac myocytes
A. Cell death after Tm-treatment (3μg/ml, 40 hours) was measured by LDH release in the presence of the δPKC antagonist peptide, δV1-1, or the TAT control peptide (1 μM). Data are mean ± S.E of four independent experiments. Student t test; * p<0.05 vs. Tm treatment. B. Untreated or tunicamycin-treated cardiac myocytes (3 μg/ml, 24 hours) in the presence of control peptide (Tm+TAT) or the δPKC inhibitor, δV1-1 (Tm + δV1-1) were co-stained with the TUNEL method, to identify apoptotic cells, and with the nuclear dye, Hoechst, to identify the cells in the field. Arrows point out some of the TUNEL-positive cells. C. TUNEL-positive cells were counted in a total of more than 300 myocytes over 3 random fields and expressed as percentages of the total number of nuclei. Data are expressed as mean ± S.E. of three independent experiments. Student t test; ** p<0.01 vs. Tm treatment. D. δV1-1 inhibits caspase-3 activation induced by Tm treatment. Procaspase-3 was detected 24 hours after Tm treatment. The data are expressed as mean ± S.E of three independent experiments.
Fig 2. δPKC activation regulates signals triggered by tunicamycin-induced ER stress in cardiac myocytes
After 6 hours (A) and 24 hours (B, C) of Tm treatment (3μg/ml) in the presence of TAT or δV1-1, total lysates of myocytes were analyzed by Western blot for the presence of the pro-apoptotic ER stress-induced protein, CHOP (A), the ER chaperone, GRP78 (B) and phosphorylation of the apoptotic kinase, JNK (C). Shown are representative blots of three independent experiments. Data are expressed as mean ± S.E. Student t test; * p < 0.05 vs. Tm treatment. GAPDH and JNK were used as internal normalization standards.
Fig 3. δPKC translocates to the ER of Tm-treated cardiac myocytes
A. ER fractions from Tm-treated myocytes were subjected to Western blot analysis with an anti-δPKC antibody. The ER-specific calnexin protein was used as an internal loading control for normalization. Purity of ER fractions was confirmed using the mitochondrial marker, ANT, and the cytoplasmic marker, enolase. Data represent mean ± S.E. of three independent experiments. Student t test; * p<0.05 vs. no treatment (Con). B. Representative confocal pictures of δPKC (red) and PDI (green, an ER marker) demonstrating increased co-localization (yellow) in Tm-treated cardiac myocytes. Data are representative of three independent experiments. C. ER fractions from cells treated with Tm in the presence of δV1-1 or TAT were subjected to Western blot with an anti-Phospho-Ser643-δPKC (p-δPKC, a marker of active δPKC) antibody. An anti-δPKC antibody or anti-calnexin were used as internal controls for normalization. D. The ER, mitochondria and cytosol were probed with the fraction specific markers, calnexin, ANT and enolase, respectively.
Fig 4. δPKC modulates the ER stress response of the myocardium in a model of cardiac ischemia and reperfusion injury
A. Normoxic control hearts and hearts that underwent ischemia and reperfusion were homogenized and total extracts were isolated. The levels of GRP78, spliced XBP1 and phospho-JNK were determined by Western blot. B. Quantitative data of the hearts described in (A). Values represent mean ± S.E. of three animals in each group (N: normoxia; I/R: ischemia/reperfusion). Student t test; * p<0.05 vs. TAT treatment, # p< 0.05 vs. control. C. Hearts were subjected to ischemia-reperfusion and treated at the onset of reperfusion with TAT control peptide or δV1-1 and the infarct size (left panel) and cell survival, as demonstrated by the decrease in CPK release (right panel), were determined. Data are expressed as mean ± S.E. of three animals in each group. Student t test; * p<0.05 vs. TAT treatment.
Fig 5. δPKC translocates to the ER in an ex vivo model of ischemia-reperfusion injury
A. ER fractions of normoxic and ischemia-reperfusion injured hearts were subjected to Western blot analysis with an anti-δPKC antibody. Whereas ischemia (0 min reperfusion) did not induce translocation of δPKC to the ER as compared with normoxic control hearts (N), reperfusion significantly induced δPKC translocation to the ER by 5 minutes. Shown are representative Western blots (bottom) and a histogram depicting the amount of δPKC associated with the ER in heart samples (top). δPKC levels were normalized to the ER marker, calnexin. Purity of the ER fractions was confirmed by the lack of the mitochondrial marker, ANT. Student t test; * p < 0.05 vs. control normoxia. B. ER localization of δPKC as evidenced by immuno-electron microscopy. Representative electron micrographs of δPKC staining in the ER fractions from normoxic control hearts (N) and hearts subjected to 35 min of ischemia followed by 15 min of reperfusion (I/R). (magnification: × 35000). Samples were probed in the presence (+) or absence (-) of δPKC antibody. Arrows indicate δPKC-positive staining with gold particles. Quantitative data of gold particles associated with ER lumen are provided in the right histogram. Five random fields of each section from two animals were counted. The data represent mean ± SD of two animals in each group. Student t test; * p < 0.05 vs. control normoxia.
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References
- Boyce M, Yuan J. Cellular response to endoplasmic reticulum stress: a matter of life or death. Cell Death Differ. 2006;13:363–73. - PubMed
- Oyadomari S, Mori M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ. 2004;11:381–9. - PubMed
- Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA, et al. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature. 2000;403:98–103. - PubMed
- Thuerauf DJ, Marcinko M, Gude N, Rubio M, Sussman MA, Glembotski CC. Activation of the unfolded protein response in infarcted mouse heart and hypoxic cultured cardiac myocytes. Circ Res. 2006;99:275–82. - PubMed
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