Embryonic diapause: Development on hold

Fenelon, Jane C.; Banerjee, Arnab; Murphy, Bruce D.

doi:10.1387/ijdb.140074bm

Cited by 148Reproductive Biology and FertilityDevelopmental Biology and Gene RegulationAnimal Genetics and Reproduction

Embryonic diapause: Development on hold

Fenelon, Jane C., Banerjee, Arnab, Murphy, Bruce D.·2014·The International Journal of Developmental Biology

DOI 10.1387/ijdb.140074bm

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Abstract

Embryonic diapause, the temporary suspension of development of the embryo, is a fascinating reproductive strategy that has been frequently exploited across the animal kingdom. It is characterized by an arrest in development that occurs at the blastocyst stage in over 130 species of mammals. Its presumed function is to uncouple mating from parturition, to ensure that both occur at the most propitious moment for survival of the species. Diapause can be facultative, i.e. induced by physiological conditions, or obligate, i.e. present in every gestation of a species. In the latter case, the proximal signals for regulation are related to photoperiod. Three diverse models, the mouse, the mustelid carnivores and the wallaby have been studied in detail. From these studies it can be discerned that, although the endocrine cues responsible for induction of diapause and re-initiation of development vary widely between species, there are a number of commonalities. Evidence to date indicates that the uterus exercises the proximal regulatory influence over whether an embryo enters into and when it exits from diapause. Some factors have been identified that appear crucial to this regulation, in particular, the polyamines. Recent studies indicate that diapause can be induced in species where it does not exist in nature. This suggests that the potential for diapause in mammals to be due to a single evolutionary event, to which control mechanisms adapted when the trait was beneficial to reproductive success. Further work at the molecular, cellular and organismic levels will be required before the physiological basis of diapause is resolved.

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Prolactin as a luteotrophin
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Uterine and embryonic metabolism after diapause in the tammar wallaby, Macropus eugenii
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Precocious Induction of Luteal Activation and Termination of Delayed Implantation in Mink with the Dopamine Antagonist Pimozide
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PROLACTIN AND LUTEINIZING HORMONE RECEPTORS IN MARSUPIAL CORPORA LUTEA: RELATIONSHIP TO CONTROL OF LUTEAL FUNCTION
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Initiation of Blastocyst Implantation by Luteinizing Hormone
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Luteotropic Hormone Receptors in the Ovary of the Mink (Mustela vison) during Delayed Implantation and Early-Postimplantation Gestation
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Seasonal Breeding in a Marsupial: Opportunities of a New Species for an Old Problem
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Colorectal Cancer Cells Enter a Diapause-like DTP State to Survive Chemotherapy
Rehman, S. K., Haynes, J., Collignon, E., Brown, K. R., Wang, Y., Nixon, A. M. L., Bruce, J. P., Wintersinger, J. A., Singh Mer, A., Lo, E. B. L., et al. (2021) · Cell · doi:10.1016/j.cell.2020.11.018 · Cited by 495 · see citing works
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Inhibition of mTOR induces a paused pluripotent state
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An Embryonic Diapause-like Adaptation with Suppressed Myc Activity Enables Tumor Treatment Persistence
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Cancer drug-tolerant persister cells: from biological questions to clinical opportunities
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mTOR signaling in stem and progenitor cells
Meng, D., Frank, A. R., & Jewell, J. L. (2018) · Development · doi:10.1242/dev.152595 · Cited by 191 · see citing works
Role of mTOR Signaling in Female Reproduction
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Metabolic Control over mTOR-Dependent Diapause-like State
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Principles of seed banks and the emergence of complexity from dormancy
Lennon, J. T., den Hollander, F., Wilke-Berenguer, M., & Blath, J. (2021) · Nature Communications · doi:10.1038/s41467-021-24733-1 · Cited by 121 · see citing works
Deconstructing the pluripotency gene regulatory network
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Understanding and targeting prostate cancer cell heterogeneity and plasticity
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The mammalian blastocyst
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Aminergic Signaling Controls Ovarian Dormancy in Drosophila
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Untangling Longevity, Dauer, and Healthspan in Caenorhabditis elegans Insulin/IGF-1-Signalling
Ewald, C. Y., Castillo-Quan, J. I., & Blackwell, T. K. (2017) · Gerontology · doi:10.1159/000480504 · Cited by 70 · see citing works
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Histone Acetyltransferase MOF Blocks Acquisition of Quiescence in Ground-State ESCs through Activating Fatty Acid Oxidation
Khoa, L. T. P., Tsan, Y.-C., Mao, F., Kremer, D. M., Sajjakulnukit, P., Zhang, L., Zhou, B. O., Tong, X., Bhanu, N. V., Choudhary, C., et al. (2020) · Cell stem cell · doi:10.1016/j.stem.2020.06.005 · Cited by 62 · see citing works
Corazonin signaling integrates energy homeostasis and lunar phase to regulate aspects of growth and sexual maturation in <i>Platynereis</i>
Andreatta, G., Broyart, C., Borghgraef, C., Vadiwala, K., Kozin, V., Polo, A., Bileck, A., Beets, I., Schoofs, L., Gerner, C., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1910262116 · Cited by 61 · see citing works
Research advances on embryonic diapause in mammals
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Wnt/Beta-catenin/Esrrb signalling controls the tissue-scale reorganization and maintenance of the pluripotent lineage during murine embryonic diapause
Fan, R., Kim, Y. S., Wu, J., Chen, R., Zeuschner, D., Mildner, K., Adachi, K., Wu, G., Galatidou, S., Li, J., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-19353-0 · Cited by 58 · see citing works
Blastocyst activation engenders transcriptome reprogram affecting X-chromosome reactivation and inflammatory trigger of implantation
He, B., Zhang, H., Wang, J., Liu, M., Sun, Y., Guo, C., Lu, J., Wang, H., & Kong, S. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1900401116 · Cited by 57 · see citing works
Facing Adversity: Dormant Embryos in Rotifers
García-Roger, E. M., Lubzens, E., Fontaneto, D., & Serra, M. (2019) · Biological Bulletin · doi:10.1086/705701 · Cited by 56 · see citing works
Rapid conceptus elongation in the pig: An interleukin 1 beta 2 and estrogen‐regulated phenomenon
Geisert, R. D., Whyte, J. J., Meyer, A. E., Mathew, D. J., Juárez, M. R., Lucy, M. C., Prather, R. S., & Spencer, T. E. (2017) · Molecular Reproduction and Development · doi:10.1002/mrd.22813 · Cited by 56 · see citing works
Recovery from cold-induced reproductive dormancy is regulated by temperature-dependent AstC signaling
Meiselman, M. R., Alpert, M. H., Cui, X., Shea, J., Gregg, I., Gallio, M., & Yapici, N. (2022) · Current Biology · doi:10.1016/j.cub.2022.01.061 · Cited by 55 · see citing works
Let-7 derived from endometrial extracellular vesicles is an important inducer of embryonic diapause in mice
Liu, W. M., Cheng, R. R., Niu, Z., Chen, A. C. H., Y., M., Li, T., Chiu, P. C. N., Pang, R. T., Lee, Y. L., Ou, J., et al. (2020) · Science Advances · doi:10.1126/sciadv.aaz7070 · Cited by 55 · see citing works
Polyamine-Mediated Effects of Prolactin Dictate Emergence from Mink Obligate Embryonic Diapause
Fenelon, J. C., Banerjee, A., Lefèvre, P. L. C., Gratian, F., & Murphy, B. D. (2016) · Biology of Reproduction · doi:10.1095/biolreprod.116.139204 · Cited by 47 · see citing works
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Embryo-endometrial interactions during early development after embryonic diapause in the marsupial tammar wallaby
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CNOT3-Dependent mRNA Deadenylation Safeguards the Pluripotent State
Zheng, X., Yang, P., Lackford, B. L., Bennett, B. D., Wang, L., Li, H., Wang, Y., Miao, Y., Foley, J. F., Fargo, D. C., et al. (2016) · Stem Cell Reports · doi:10.1016/j.stemcr.2016.09.007 · Cited by 40 · see citing works
Inhibition of polyamine synthesis causes entry of the mouse blastocyst into embryonic diapause†
Fenelon, J. C., & Murphy, B. D. (2017) · Biology of Reproduction · doi:10.1093/biolre/iox060 · Cited by 39 · see citing works
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Emergent Protective Organogenesis in Date Palms: A Morpho-Devo-Dynamic Adaptive Strategy during Early Development
Xiao, T. T., Aragón-Raygoza, A., Caballero-Pérez, J., Kirschner, G. K., Deng, Y., Atkinson, B. S., Sturrock, C. J., Lube, V., Wang, J. Y., Gilles Lubineau, A., et al. (2019) · The Plant Cell · doi:10.1105/tpc.19.00008 · Cited by 38 · see citing works
Arginine, Agmatine, and Polyamines: Key Regulators of Conceptus Development in Mammals
Halloran, K. M., Stenhouse, C., Wu, G., & Bazer, F. W. (2021) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-74180-8_6 · Cited by 38 · see citing works
Homeostatic regulation of lipid droplet content in mammalian oocytes and embryos
Ibayashi, M., Aizawa, R., Mitsui, J., & Tsukamoto, S. (2021) · Reproduction · doi:10.1530/rep-21-0238 · Cited by 38 · see citing works
Regulation of diapause in carnivores
Fenelon, J. C., Lefèvre, P. L. C., Banerjee, A., & Murphy, B. D. (2016) · Reproduction in Domestic Animals · doi:10.1111/rda.12835 · Cited by 33 · see citing works
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Fatty acid oxidation is required for embryonic stem cell survival during metabolic stress
Yan, H., Malik, N., Kim, Y., He, Y., Li, M., Dubois, W., Liu, H., Peat, T. J., Nguyen, J. T., Tseng, Y., et al. (2021) · EMBO Reports · doi:10.15252/embr.202052122 · Cited by 33 · see citing works
Epigenetic reprogramming by TET enzymes impacts co-transcriptional R-loops
Sabino, J. C., de Almeida, M. R., Abreu, P. L., Ferreira, A. M., Caldas, P., Domingues, M. M., Santos, N. C., Azzalin, C. M., Grosso, A. R., & de Almeida, S. F. (2022) · eLife · doi:10.7554/elife.69476 · Cited by 30 · see citing works
Embryo arrest and reactivation: potential candidates controlling embryonic diapause in the tammar wallaby and mink†
Fenelon, J. C., Shaw, G., Frankenberg, S., Murphy, B. D., & Renfree, M. B. (2017) · Biology of Reproduction · doi:10.1093/biolre/iox019 · Cited by 30 · see citing works
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Molecular Regulators of Embryonic Diapause and Cancer Diapause-like State
Hussein, A. M., Balachandar, N., Mathieu, J., & Ruohola‐Baker, H. (2022) · Cells · doi:10.3390/cells11192929 · Cited by 29 · see citing works
Epigenetic control of embryo–uterine crosstalk at peri-implantation
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Authors: Fenelon, J. C., Banerjee, A., & Murphy, B. D.
Affiliations: Université de Montréal (CA)
ORCID: Fenelon, Jane C.
Banerjee, Arnab
Murphy, Bruce D.
Venue: The International Journal of Developmental Biology
Publisher: EHU Press
Published: 2014
Volume: 58
Issue: 2-3-4
Pages: 163-174
ISSN: 0214-6282 (ISSN-L)
DOI: 10.1387/ijdb.140074bm
OpenAlex: W1976804823
Cited by: 147
References: 144
Citations by year: 2026: 4 · 2025: 16 · 2024: 17 · 2023: 11 · 2022: 13 · 2021: 15 · 2020: 16 · 2019: 14 · 2018: 8 · 2017: 16 · 2016: 10 · 2015: 6 · 2014: 1
FWCI: 10.89
Type: journal article
Language: en
Open access: closed
Locations: The International Journal of Developmental Biology (publishedVersion)
PubMed (publishedVersion)
Funders: Canadian Institutes of Health Research
Topics: Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Reproductive Biology and Fertility
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Animal Genetics and Reproduction
Keywords: delayed implantation, facultative diapause, photoperiod, uterus, polyamines, wallabies, mice
MeSH terms: Animals, Blastocyst, Embryo, Mammalian, Female, Humans, Embryo Implantation, Delayed, Reproduction, Uterus, Embryonic Development, Mice

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Embryonic diapause: Development on hold

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