Temperature-induced cardiac remodeling in fish

Keen, A.; Klaiman, Jordan M.; Shiels, Holly A.; Gillis, Todd E.

doi:10.1242/jeb.128496

Cited by 70 publications

(103 citation statements)

References 124 publications

(215 reference statements)

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…Some candidate genes for T PEAK are well‐known for their roles in cardiac function. For example, TITIN is involved in passive tension and plays a key role in contraction of muscle cells (Keen, Klaiman, Shiels, & Gillis, ). ADA1B (alpha 1B‐adrenergic receptor) has been shown to be involved in cardiac hypertrophy (Milano et al., ) and the regulation of vasoconstriction in mammals (Adefurin et al., ).…”

Section: Discussionmentioning

confidence: 99%

Physiological and genomic signatures of evolutionary thermal adaptation in redband trout from extreme climates

Chen

Farrell

Matala

et al. 2018

Evolutionary Applications

View full text Add to dashboard Cite

Temperature is a master environmental factor that limits the geographical distribution of species, especially in ectotherms. To address challenges in biodiversity conservation under ongoing climate change, it is essential to characterize relevant functional limitations and adaptive genomic content at population and species levels. Here, we present evidence for adaptive divergence in cardiac function and genomic regions in redband trout (Oncorhynchus mykiss gairdneri) populations from desert and montane streams. Cardiac phenotypes of individual fish were measured in the field with a custom‐built electrocardiogram apparatus. Maximum heart rate and its rate limiting temperature during acute warming were significantly higher in fish that have evolved in the extreme of a desert climate compared to a montane climate. Association mapping with 526,301 single nucleotide polymorphisms (SNPs) across the genome revealed signatures of thermal selection both within and among ecotypes. Among desert and montane populations, 435 SNPs were identified as putative outliers under natural selection and 20 of these loci showed significant association with average summer water temperatures among populations. Phenotypes for cardiac performance were variable within each ecotype, and 207 genomic regions were strongly associated with either maximum heart rate or rate limiting temperatures among individuals. Annotation of significant loci provided candidate genes that underlie thermal adaptation, including pathways associated with cardiac function (IRX5, CASQ1, CAC1D, and TITIN), neuroendocrine system (GPR17 and NOS), and stress response (SERPH). By integrating comparative physiology and population genomics, results here advance our knowledge on evolutionary processes of thermal adaptation in aquatic ectotherms.

show abstract

Section: Discussionmentioning

confidence: 99%

Physiological and genomic signatures of evolutionary thermal adaptation in redband trout from extreme climates

Chen

Farrell

Matala

et al. 2018

Evolutionary Applications

View full text Add to dashboard Cite

show abstract

“…The fish heart remodels with seasonal temperature change [23, 36, 39, 40, 11, 13, 19, 43, 42, 30]. Here, we focused on the passive properties of the rainbow trout atrium across multiple levels of biological organisation following chronic cooling and warming.…”

Section: Discussionmentioning

confidence: 99%

Macro- and micromechanical remodelling in the fish atrium is associated with regulation of collagen 1 alpha 3 chain expression

Keen

Fenna

McConnell

et al. 2018

Pflugers Arch - Eur J Physiol

Self Cite

View full text Add to dashboard Cite

Numerous pathologies lead to remodelling of the mammalian ventricle, often associated with fibrosis. Recent work in fish has shown that fibrotic remodelling of the ventricle is ‘reversible’, changing seasonally as temperature-induced changes in blood viscosity alter haemodynamic load on the heart. The atrial response to varying haemodynamic load is less understood in mammals and completely unexplored in non-mammalian vertebrates. To investigate atrial remodelling, rainbow trout were chronically cooled (from 10 ± 1 to 5 ± 1 °C) and chronically warmed (from 10 ± 1 to 18 ± 1 °C) for a minimum of 8 weeks. We assessed the functional effects on compliance using ex vivo heart preparations and atomic force microscopy nano-indentation and found chronic cold increased passive stiffness of the whole atrium and micromechanical stiffness of tissue sections. We then performed histological, biochemical and molecular assays to probe the mechanisms underlying functional remodelling of the atrial tissue. We found cooling resulted in collagen deposition which was associated with an upregulation of collagen-promoting genes, including the fish-specific collagen I alpha 3 chain, and a reduction in gelatinase activity of collagen-degrading matrix metalloproteinases (MMPs). Finally, we found that cooling reduced mRNA expression of cardiac growth factors and hypertrophic markers. Following long-term warming, there was an opposing response to that seen with cooling; however, these changes were more moderate. Our findings suggest that chronic cooling causes atrial dilation and increased myocardial stiffness in trout atria analogous to pathological states defined by changes in preload or afterload of the mammalian atria. The reversal of this phenotype following chronic warming is particularly interesting as it suggests that typically pathological features of mammalian atrial remodelling may oscillate seasonally in the fish, revealing a more dynamic and plastic atrial remodelling response.Electronic supplementary materialThe online version of this article (10.1007/s00424-018-2140-1) contains supplementary material, which is available to authorized users.

show abstract

“…These authors also propose a novel hypothesis, Hierarchical Mechanisms of Thermal Limitation, that integrates thermal effects on subcellular components and organ systems to better understand thermal tolerance at the whole organism level. Moreover, cells, tissues, organs, and whole organisms are dynamic systems that can sense and respond to their thermal environment through physiological acclimation (Somero, 2005;Keen et al, 2017;Rohr et al, 2018).…”

Section: Biophysical Effects Of Temperaturementioning

confidence: 99%

Embryonic Temperature Programs Phenotype in Reptiles

2020

View full text Add to dashboard Cite

Reptiles are critically affected by temperature throughout their lifespan, but especially so during early development. Temperature-induced changes in phenotype are a specific example of a broader phenomenon called phenotypic plasticity in which a single individual is able to develop different phenotypes when exposed to different environments. With climate change occurring at an unprecedented rate, it is important to study temperature effects on reptiles. For example, the potential impact of global warming is especially pronounced in species with temperature-dependent sex determination (TSD) because temperature has a direct effect on a key phenotypic (sex) and demographic (population sex ratios) trait. Reptiles with TSD also serve as models for studying temperature effects on the development of other traits that display continuous variation. Temperature directly influences metabolic and developmental rate of embryos and can have permanent effects on phenotype that last beyond the embryonic period. For instance, incubation temperature programs post-hatching hormone production and growth physiology, which can profoundly influence fitness. Here, we review current knowledge of temperature effects on phenotypic and developmental plasticity in reptiles. First, we examine the direct effect of temperature on biophysical processes, the concept of thermal performance curves, and the process of thermal acclimation. After discussing these reversible temperature effects, we focus the bulk of the review on developmental programming of phenotype by temperature during embryogenesis (i.e., permanent developmental effects). We focus on oviparous species because eggs are especially susceptible to changes in ambient temperature. We then discuss recent work probing the role of epigenetic mechanisms in mediating temperature effects on phenotype. Based on phenotypic effects of temperature, we return to the potential impact of global warming on reptiles. Finally, we highlight key areas for future research, including the identification of temperature sensors and assessment of genetic variation for thermosensitivity.

show abstract

Temperature-induced cardiac remodeling in fish

Cited by 70 publications

References 124 publications

Physiological and genomic signatures of evolutionary thermal adaptation in redband trout from extreme climates

Physiological and genomic signatures of evolutionary thermal adaptation in redband trout from extreme climates

Macro- and micromechanical remodelling in the fish atrium is associated with regulation of collagen 1 alpha 3 chain expression

Embryonic Temperature Programs Phenotype in Reptiles

Contact Info

Product

Resources

About