Hormonal components of altered developmental pathways in the annual killifish, Austrofundulus limnaeus

Pri-Tal, Benjamin M.; Blue, Steven W.; Pau, Francis K.-Y.; Podrabsky, Jason E.

doi:10.1016/j.ygcen.2011.08.016

Cited by 20 publications

(23 citation statements)

References 75 publications

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“…However, the embryonic incubation environment can alter this initial programming, and, for example, a 5°C increase in incubation temperature can force 100% of the embryos to bypass diapause II and develop directly to diapause III (145). The molecular mechanisms that control maternal influences on diapause II appear to be related to the age of the female at the time of oviposition and not environmental cues, and may be regulated by maternal steroid hormone levels (152). How hormonal cues may alter gene expression during oogenesis, and what exactly is packaged into the oocytes are still open questions.…”

Section: Fishmentioning

confidence: 99%

“…However, evidence is mounting that maternally packaged proteins and perhaps RNAs may play key roles in the maternal regulation of entrance into diapause. Recent evidence from comparative studies of closely related species of killifish that differ in their production of diapause II embryos suggest that microRNAs may play a pivotal role in the regulation of diapause (152). However, mechanistic studies have yet to be reported to support the importance of these findings.…”

Section: Fishmentioning

confidence: 99%

See 1 more Smart Citation

Mechanisms of animal diapause: recent developments from nematodes, crustaceans, insects, and fish

Hand

Denlinger

Podrabsky

et al. 2016

American Journal of Physiology-Regulatory, Integrative and Comp

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222

224

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Life cycle delays are beneficial for opportunistic species encountering suboptimal environments. Many animals display a programmed arrest of development (diapause) at some stage(s) of their development, and the diapause state may or may not be associated with some degree of metabolic depression. In this review, we will evaluate current advancements in our understanding of the mechanisms responsible for the remarkable phenotype, as well as environmental cues that signal entry and termination of the state. The developmental stage at which diapause occurs dictates and constrains the mechanisms governing diapause. Considerable progress has been made in clarifying proximal mechanisms of metabolic arrest and the signaling pathways like insulin/Foxo that control gene expression patterns. Overlapping themes are also seen in mechanisms that control cell cycle arrest. Evidence is emerging for epigenetic contributions to diapause regulation via small RNAs in nematodes, crustaceans, insects, and fish. Knockdown of circadian clock genes in selected insect species supports the importance of clock genes in the photoperiodic response that cues diapause. A large suite of chaperone-like proteins, expressed during diapause, protects biological structures during long periods of energy-limited stasis. More information is needed to paint a complete picture of how environmental cues are coupled to the signal transduction that initiates the complex diapause phenotype, as well as molecular explanations for how the state is terminated. Excellent examples of molecular memory in post-dauer animals have been documented in Caenorhabditis elegans It is clear that a single suite of mechanisms does not regulate diapause across all species and developmental stages.

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Section: Fishmentioning

confidence: 99%

Section: Fishmentioning

confidence: 99%

Mechanisms of animal diapause: recent developments from nematodes, crustaceans, insects, and fish

Hand

Denlinger

Podrabsky

et al. 2016

American Journal of Physiology-Regulatory, Integrative and Comp

Self Cite

222

224

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“…U0126 inhibits the activity of Mek1/2 proteins, which are key components of the MAP kinase signaling cascade (Duncia et al, 1998). Embryos of A. limnaeus are known to be highly impermeable to exogenous substances, and thus higher than expected external concentrations and dimethyl sulfoxide (DMSO) in the medium are required to achieve biologically active concentrations within the embryos (Podrabsky and Hand, 2000;Pri-Tal et al, 2011). Lyophilized pharmacological agents were reconstituted in 100% DMSO stock solutions that were diluted in embryo medium (Podrabsky, 1999) without antibiotics.…”

Section: Pharmacological Inhibition Of Igf Signalingmentioning

confidence: 99%

Insulin-like growth factor signaling regulates developmental trajectory associated with diapause in embryos of the annual killifish Austrofundulus limnaeus

Woll

Podrabsky

2017

Journal of Experimental Biology

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Annual killifishes exhibit a number of unique life history characters including the occurrence of embryonic diapause, unique cell movements associated with dispersion and subsequent reaggregation of the embryonic blastomeres, and a short postembryonic life span. Insulin-like growth factor (IGF) signaling is known to play a role in the regulation of metabolic dormancy in a number of animals but has not been explored in annual killifishes. The abundance of IGF proteins during development and the developmental effects of blocking IGF signaling by pharmacological inhibition of the insulin-like growth factor I receptor (IGF1R) were explored in embryos of the annual killifish Austrofundulus limnaeus. Blocking of IGF signaling in embryos that would normally escape entrance into diapause resulted in a phenotype that was remarkably similar to that of embryos entering diapause. IGF-I protein abundance spikes during early development in embryos that will not enter diapause. In contrast, IGF-I levels remain low during early development in embryos that will enter diapause II. IGF-II protein is packaged at higher levels in escape-bound embryos compared with diapause-bound embryos. However, IGF-II levels quickly decrease and remain low during early development and only increase substantially during late development in both developmental trajectories. Developmental patterns of IGF-I and IGF-II protein abundance under conditions that would either induce or bypass entrance into diapause are consistent with a role for IGF signaling in the regulation of developmental trajectory and entrance into diapause in this species. We propose that IGF signaling may be a unifying regulatory pathway that explains the larger suite of characters that are associated with the complex life history of annual killifishes.

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“…In a recent study, Pri-Tal et al [103] reported that A. limnaeus embryos that escape diapause II show higher levels of androstenedione (estrogen precursor) and estradiol that embryos entering diapause, suggesting that that steroid hormonal signaling is involved in the regulation of developmental trajectories in this species. Sulfatation of the 3β-hydroxyl group of a steroid may transforms a liposoluble steroid into a water soluble molecule, and therefore modifies its subcellular localization and biological activities [104].…”

Section: Resultsmentioning

confidence: 99%

A Rapid Transcriptome Response Is Associated with Desiccation Resistance in Aerially-Exposed Killifish Embryos

et al. 2013

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Delayed hatching is a form of dormancy evolved in some amphibian and fish embryos to cope with environmental conditions transiently hostile to the survival of hatchlings or larvae. While diapause and cryptobiosis have been extensively studied in several animals, very little is known concerning the molecular mechanisms involved in the sensing and response of fish embryos to environmental cues. Embryos of the euryhaline killifish Fundulus heteroclitus advance dvelopment when exposed to air but hatching is suspended until flooding with seawater. Here, we investigated how transcriptome regulation underpins this adaptive response by examining changes in gene expression profiles of aerially incubated killifish embryos at ∼100% relative humidity, compared to embryos continuously flooded in water. The results confirm that mid-gastrula embryos are able to stimulate development in response to aerial incubation, which is accompanied by the differential expression of at least 806 distinct genes during a 24 h period. Most of these genes (∼70%) appear to be differentially expressed within 3 h of aerial exposure, suggesting a broad and rapid transcriptomic response. This response seems to include an early sensing phase, which overlaps with a tissue remodeling and activation of embryonic development phase involving many regulatory and metabolic pathways. Interestingly, we found fast (0.5–1 h) transcriptional differences in representatives of classical “stress” proteins, such as some molecular chaperones, members of signalling pathways typically involved in the transduction of sensor signals to stress response genes, and oxidative stress-related proteins, similar to that described in other animals undergoing dormancy, diapause or desiccation. To our knowledge, these data represent the first transcriptional profiling of molecular processes associated with desiccation resistance during delayed hatching in non-mammalian vertebrates. The exceptional transcriptomic plasticity observed in killifish embryos provides an important insight as to how the embryos are able to rapidly adapt to non-lethal desiccation conditions.

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Hormonal components of altered developmental pathways in the annual killifish, Austrofundulus limnaeus

Cited by 20 publications

References 75 publications

Mechanisms of animal diapause: recent developments from nematodes, crustaceans, insects, and fish

Mechanisms of animal diapause: recent developments from nematodes, crustaceans, insects, and fish

Insulin-like growth factor signaling regulates developmental trajectory associated with diapause in embryos of the annual killifish Austrofundulus limnaeus

A Rapid Transcriptome Response Is Associated with Desiccation Resistance in Aerially-Exposed Killifish Embryos

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