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Mitogen-activated protein kinases contribute to temperature-induced cardiac remodelling in rainbow trout (Oncorhynchus mykiss)

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Abstract

Rainbow trout (Oncorhynchus mykiss) live in environments where water temperatures range between 4 °C and 20 °C. Laboratory studies demonstrate that cold and warm acclimations of male trout can have oppositional effects on cardiac hypertrophy and the collagen content of the heart. The cellular mechanisms behind temperature-induced cardiac remodelling are unclear, as is why this response differs between male and female fish. Studies with cultured trout cardiac fibroblasts suggests that collagen deposition is regulated, at least in part, by mitogen-activated protein kinase (MAPK) cell signalling pathways. We, therefore, hypothesized that temperature-dependent cardiac remodelling is regulated by these signalling pathways. To test this, male and female trout were acclimated to 18 °C (warm) in the summer and to 4 °C (cold) in the winter and the activation of MAPK pathways in the hearts were characterized and compared to that of control fish maintained at 12 °C. In addition, cardiac collagen content, cardiac morphology and the expression of gene transcripts for matrix metalloproteinases (MMP) -9, MMP-2, tissue inhibitor of matrix metalloproteinases and collagen 1α were characterized. p38 MAPK phosphorylation increased in the hearts of female fish with cold acclimation and the phosphorylation of extracellular signal-regulated kinase increased in the hearts of male fish with warm acclimation. However, there was no effect of thermal acclimation on cardiac morphology or collagen content in either male or female fish. These results indicate that thermal acclimation has transient and sex-specific effects on the phosphorylation of MAPKs but also how variable the response of the trout heart is to thermal acclimation.

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Funding

Y.D. was supported by an Ontario Graduate Scholarship. This work in the Gillis Lab is supported by a Discovery Grant, and a Discovery Accelerator Supplement, from the National Sciences and Engineering Research Council of Canada.

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  1. Department of Integrative Biology, University of Guelph, Guelph, ON, N1G-2W1, Canada

    Y. Ding, E. F. Johnston & T. E. Gillis

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  1. Y. Ding
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  2. E. F. Johnston
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Correspondence to T. E. Gillis.

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Appendix

Appendix

See Tables 1, 2 and Figs. 5, 6

Table 1 Effect of cold and warm acclimation on the collagen composition of rainbow trout (Oncorhynchus mykiss) ventricles
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Table 2 Summary of initial, final, and delta quantitative measurements (Mean ± SEM) taken during sampling
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Fig. 5
figure 5

Representative western blot from the cold acclimation experiment. Each different antibody corresponds to different blots that were loaded and run simultaneously. Antibodies were from cell signalling technology and are as follows: phosphorylated p38 (p-p38), total p38, phosphorylated ERK (p-ERK), total ERK. The sample group of each lane is listed along the top: E experimental; C control; numbers indicate the sampling week (E8, experimental group sampled at W8). The same internal control sample was loaded with every blot

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Fig. 6
figure 6

Relative ventricular collagen content, standardized to actin, measured by western blotting in rainbow trout (Oncorhynchus mykiss) at the initial (W-1/2) and final (W8) sampling periods. (A) Cold acclimated male heart, (B) cold acclimated female heart. (C) Warm acclimated male heart, (D) warm acclimated female heart. No statistically significant differences found (N = 4–8). There are no statistically significant differences between the plotted means

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Ding, Y., Johnston, E.F. & Gillis, T.E. Mitogen-activated protein kinases contribute to temperature-induced cardiac remodelling in rainbow trout (Oncorhynchus mykiss). J Comp Physiol B 192, 61–76 (2022). https://doi.org/10.1007/s00360-021-01406-5

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