Temperature-activated ion channels in neural crest cells confer maternal fever–associated birth defects

Hutson, Mary Redmond; Keyte, Anna L.; Hernández-Morales, Miriam; Gibbs, Eric; Kupchinsky, Zachary A.; Argyridis, Ioannis; Erwin, Kyle N.; Pegram, Kelly; Kneifel, Margaret; Rosenberg, Paul B.; Matak, Pavle; Xie, Luke; Grandl, Jörg; Davis, Erica E.; Katsanis, Nicholas; Liu, Chunlei; Benner, Eric J.

doi:10.1126/scisignal.aal4055

Cited by 64 publications

(92 citation statements)

References 80 publications

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“…To study the effects of thermal stress on morphogenesis, dissection and direct observation of embryos is critical. Based on our results and comparisons with mammals (Walsh et al., ; Edwards, ; Hutson et al., ), these may be the most thermally sensitive stages of embryonic development for diverse vertebrate species. Within mammals and birds, thermal stress during morphogenesis may cause craniofacial abnormalities, neural tube defects, or mental retardation (Webster & Edwards, ; Shiota, ; Walsh et al., ; Edwards, ; Edwards, Saunders, & Shiota, ).…”

Section: Discussionmentioning

confidence: 99%

The effects of thermal stress on the early development of the lizard Anolis sagrei

et al. 2018

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Across the globe terrestrial ectotherms-amphibians and non-avian reptiles-are facing a range of emerging challenges. Increasing global temperatures, in particular, are affecting all aspects of ectotherm biology and life history. Embryonic development is a thermally sensitive period of the organismal lifecycle, yet the impacts of thermal stress on the early development of ectotherms have significantly lagged behind studies of later stages and adult thermal physiology. Morphogenesis, the stage where the major anatomical systems are actively forming, is particularly sensitive to thermal stress, yet is not studied as often as later stages where growth is the primary process happening within the egg. Here, we focus on the effects of thermal stress on the first 12 days of development, the stages of morphogenesis, in the lizard Anolis sagrei. We examine the resiliency of the early developmental stages to heat stress by incubating eggs at temperatures that parallel conditions observed today and predicted over the next 50-100 years of projected climate change. Our results suggest that some anole nests are currently at the thermal limits for which the early embryonic stages can properly develop. Our results emphasize the importance of studying early embryonic stages of development and the importance of studying stage-specific effects of thermal stress on squamate development.

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Section: Discussionmentioning

confidence: 99%

The effects of thermal stress on the early development of the lizard Anolis sagrei

et al. 2018

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“…Supporting their theoretical calculations, Duret et al (2017) show that the calcium response to magnetic field treatment is lost in cells expressing a temperature-insensitive TRPV4-ferritin construct. Similarly, Hutson et al (2017) show that the calcium response to oscillating magnetic field treatment is also lost in cells expressing a temperature-insensitive TRPV1 fused to a ferritin-binding domain. Although this mechanism is plausible, additional magnetomechanical and magnetothermal mechanisms of ion channel activation by iron-loaded ferritin are under consideration (M Barbic, in prep.).…”

Section: Genetically Encoded Particlesmentioning

confidence: 80%

“…Electromagnetic fields can penetrate tissue and in birds and other animals will guide migration, although the precise mechanism is unknown (Freake et al 2006). More recently, it has been shown that electromagnetic fields can be used to regulate the activity of cells in proximity to external metal nanoparticles (Huang et al 2010;Chen et al 2015), or that express genetically encoded intracellular metal nanoparticles (ferritin) (Stanley et al 2015;Wheeler et al 2016;Duret et al 2017;Hutson et al 2017). In both cases, the particles transduce electromagnetic fields that gate ion channels, although the field strength that is required is much larger than that required for magnetic sensing by biologic systems.…”

Section: Electromagnetic Control Of Cell Activitymentioning

confidence: 99%

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Electromagnetic Regulation of Cell Activity

Stanley

Friedman

2018

Cold Spring Harb Perspect Med

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The ability to observe the effects of rapidly and reversibly regulating cell activity in targeted cell populations has provided numerous physiologic insights. Over the last decade, a wide range of technologies have emerged for regulating cellular activity using optical, chemical, and, more recently, electromagnetic modalities. Electromagnetic fields can freely penetrate cells and tissue and their energy can be absorbed by metal particles. When released, the absorbed energy can in turn gate endogenous or engineered receptors and ion channels to regulate cell activity. In this manner, electromagnetic fields acting on external nanoparticles have been used to exert mechanical forces on cell membranes and organelles to generate heat and interact with thermally activated proteins or to induce receptor aggregation and intracellular signaling. More recently, technologies using genetically encoded nanoparticles composed of the iron storage protein, ferritin, have been used for targeted, temporal control of cell activity in vitro and in vivo. These tools provide a means for noninvasively modulating gene expression, intracellular organelles, such as endosomes, and whole-cell activity both in vitro and in freely moving animals. The use of magnetic fields interacting with external or genetically encoded nanoparticles thus provides a rapid noninvasive means for regulating cell activity.

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“…17 However, our results support assumption that increasing the duration of temperature elevation may lower threshold for malformations to 40-41°C 19 as has been recently published for the chick embryo. 74 Other in vitro studies on mammalian skeletal muscle cells have shown that hyperthermia at 41°C for 72 hours inhibited myotube formation. 75…”

Section: Discussionmentioning

confidence: 99%

Influence of hyperthermal regimes on experimental teratoma development in vitro

Bojanac

Rogosic

Sinčić

et al. 2018

Int J Experimental Path

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SummaryWe screened for the impact of hyperthermal regimes varying in the cumulative equivalent minutes at 43°C (CEM43°C) and media composition on tumour development using an original teratoma in vitro model. Rat embryos (three germ layers) were microsurgically isolated and cultivated at the air‐liquid interface. During a two week period, ectodermal, mesodermal and endodermal derivatives developed within trilaminar teratomas. Controls were grown at 37°C. Overall growth was measured, and teratoma survival and differentiation were histologically assessed. Cell proliferation was stereologically quantified by the volume density of Proliferating Cell Nuclear Antigen. Hyperthermia of 42°C, applied for 15 minutes after plating (CEM43°C 3.75 minutes), diminished cell proliferation (P ˂ .0001) and enhanced differentiation of both myotubes (P ˂ .01) and cylindrical epithelium (P ˂ .05). Hyperthermia of 43°C applied each day for 30 minutes during the first week (CEM43°C 210 minutes) impaired overall growth (P ˂ .01) and diminished cell proliferation (P ˂ .0001). Long‐term hyperthermia of 40.5°C applied for two weeks (CEM43°C 630 minutes) significantly impaired survival (P ˂ .005). Long‐term hyperthermia of 40.5°C applied from the second day when differentiation of tissues begins (CEM43°C 585 minutes) impaired survival (P ˂ .0001), overall growth (P ˂ .01) and cartilage differentiation (P ˂ .05). No teratomas survived extreme regimes: 43°C for 24 hours (CEM43°C 1440 minutes), hyperthermia in the scant serum‐free medium (CEM43°C 630 minutes) or treatment with an anti‐HSP70 antibody before long‐term hyperthermia 40.5°C from the second day (CEM43°C 585 minutes). This in vitro research provided novel insights into the impact of hyperthermia on the development of experimental teratomas from their undifferentiated sources and are thus of potential interest for future therapeutic strategies in corresponding in vivo models.

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Temperature-activated ion channels in neural crest cells confer maternal fever–associated birth defects

Cited by 64 publications

References 80 publications

The effects of thermal stress on the early development of the lizard Anolis sagrei

The effects of thermal stress on the early development of the lizard Anolis sagrei

Electromagnetic Regulation of Cell Activity

Influence of hyperthermal regimes on experimental teratoma development in vitro

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