Temperature-Dependent Alternative Splicing of Precursor mRNAs and Its Biological Significance: A Review Focused on Post-Transcriptional Regulation of a Cold Shock Protein Gene in Hibernating Mammals

Shiina, Takahiko; Shimizu, Yasutake

doi:10.3390/ijms21207599

Cited by 11 publications

(7 citation statements)

References 147 publications

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“…Increasing temperatures induced upregulation of transcripts associated with posttranscriptional modifications in both populations of lake sturgeon, enhancing translational plasticity. Conserved responses of alternative splicing and gene silencing via miRNA suggest that these mechanisms are part of the inducible stress response of sturgeons, similar to other studied fishes, and likely play a role in environmental adaptation (Somero, 2018;Healy & Schulte, 2019;Tan et al, 2019;Shiina and Shimizu, 2020;Verta and Jacobs, 2021;Thorstensen et al, 2022;Steward et al, 2022). However, these processes were ultimately downregulated as temperatures increased to 24 °C, indicating thermal thresholds on post-translational as well as transcriptional responsiveness.…”

Section: Plasticity As An Adaptive Traitmentioning

confidence: 89%

Elevated temperatures reduce population-specific transcriptional plasticity in developing lake sturgeon (Acipenser fulvescens)

Bugg

Thorstensen

Marshall

et al. 2022

Preprint

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Rising mean and variance in temperatures elevate threats to endangered freshwater species like the lake sturgeon, Acipenser fulvescens. Previous research has demonstrated that higher temperatures in early development result in physiological consequences for lake sturgeon populations throughout Manitoba, Canada, with alteration of metabolic rate, thermal tolerance, transcriptional responses, growth, and mortality. In the present study, we acclimated lake sturgeon from northern and southern populations within Manitoba to current and future projected environmental temperatures of 16, 20, and 24C for 30 days, and measured gill transcriptional responses using RNAseq. We found population-specific and acclimation-specific responses to the thermal treatments, as well as conserved molecular responses between northern and southern sturgeon populations. Expression profiles revealed a gradient in transcriptional responses consistent with acclimation temperature, with a higher number of differentially expressed transcripts observed in the southern compared to the northern lake sturgeon population as temperatures increase, indicating enhanced transcriptional plasticity. Overall lake sturgeon populations responded to thermal acclimation by upregulating the expression of transcripts involved in transcriptional and translational regulation, mitochondrial function, pathogen responses, and DNA damage, as well as genes associated with pre- and post-transcriptional processes (i.e., methylation, alternative splicing). Further, both populations upregulated transcript expression related to cell structural damage as temperatures increased to 20C, but the northern population also responded with increases in damage signaling and recruitment of mitochondrial processes involved in ATP production. Ultimately, these transcriptional responses highlight molecular consequences of increasing temperatures for divergent lake sturgeon populations during vulnerable early developmental periods and the critical influence of transcriptome plasticity on acclimation capacity.

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Section: Plasticity As An Adaptive Traitmentioning

confidence: 89%

Elevated temperatures reduce population-specific transcriptional plasticity in developing lake sturgeon (Acipenser fulvescens)

Bugg

Thorstensen

Marshall

et al. 2022

Preprint

View full text Add to dashboard Cite

show abstract

“…Unlike plants and reptiles, wherein cellular temperature is largely reflective of external environmental conditions, mammalian cells are less sensitive to endogenous temperature changes due to homeostatic control (Tansey & Johnson, 2015; Shiina & Shimizu, 2020). Despite this, fluctuations within a comparatively narrow physiological range (maintained within 1–4 °C) (Refinetti & Menaker, 1992) do still occur and are sufficient to trigger differential splicing of particular transcripts (Fig.…”

Section: Proposed Models For Effects Of Testicular Hyperthermia On Sp...mentioning

confidence: 99%

Testicular heat stress, a historical perspective and two postulates for why male germ cells are heat sensitive

et al. 2022

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Herein, we compare the different experimental regimes used to induce testicular heat stress and summarise their impact on sperm production and male fertility. Irrespective of the protocol used, scrotal heat stress causes loss of sperm production. This is first seen 1-2 weeks post heat stress, peaking 4-5 weeks thereafter. The higher the temperature, or the longer the duration of heat, the more pronounced germ cell loss becomes, within extreme cases this leads to azoospermia. The second, and often underappreciated impact of testicular hyperthermia is the production of poor-quality spermatozoa. Typically, those cells that survive hyperthermia develop into morphologically abnormal and poorly motile spermatozoa. While both apoptotic and non-apoptotic pathways are known to contribute to hyperthermic germ cell loss, the mechanisms leading to formation of poor-quality sperm remain unclear. Mechanistically, it is unlikely that testicular hyperthermia affects messenger RNA (mRNA) abundance, as a comparison of four different mammalian studies shows no consistent single gene changes. Using available evidence, we propose two novel models to explain how testicular hyperthermia impairs sperm formation. Our first model suggests aberrant alternative splicing, while the second model proposes a loss of RNA repression. Importantly, neither model requires consistent changes in RNA species.

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“…RNA thermometers that regulate temperature-dependent splicing in plants, however, have not been reported. In general, the molecular mechanisms of temperature-dependent alternative splicing of genes are poorly understood [ 16 ].…”

Section: Introductionmentioning

confidence: 99%

Structural analysis of temperature-dependent alternative splicing of HsfA2 pre-mRNA from tomato plants

et al. 2022

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Temperature-dependent alternative splicing was recently demonstrated for intron 2 of the gene coding for heat shock factor HsfA2 of the tomato plant Solanum lycopersicum , but the molecular mechanism regulating the abundance of such temperature-dependent splice variants is still unknown. We report here on regulatory pre-mRNA structures that could function as regulators by controlling the use of splice sites in a temperature-dependent manner. We investigate pre-mRNA structures at the splice sites of intron 2 of the gene coding for HsfA2 from S. lycopersicum using NMR- and CD-spectroscopy as well as in-line probing. The pre-mRNA undergoes conformational changes between two different secondary structures at the 3ʹ splice site of the intron in a temperature-dependent manner. Previously, it was shown that three single nucleotide polymorphisms (SNPs) in intron 2 of the HsfA2 pre-mRNA affect the splicing efficiency of its pre-mRNA and are linked to the thermotolerance in different tomato species. By comparing pre-mRNA fragments of the tomato species S. lycopersicum and S. peruvianum , we show that these SNPs result in substantial structural differences between the pre-mRNAs of the two species.

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Temperature-Dependent Alternative Splicing of Precursor mRNAs and Its Biological Significance: A Review Focused on Post-Transcriptional Regulation of a Cold Shock Protein Gene in Hibernating Mammals

Cited by 11 publications

References 147 publications

Elevated temperatures reduce population-specific transcriptional plasticity in developing lake sturgeon (Acipenser fulvescens)

Elevated temperatures reduce population-specific transcriptional plasticity in developing lake sturgeon (Acipenser fulvescens)

Testicular heat stress, a historical perspective and two postulates for why male germ cells are heat sensitive

Structural analysis of temperature-dependent alternative splicing of HsfA2 pre-mRNA from tomato plants

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