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Environmental Exposures around Conception: Developmental Pathways Leading to Lifetime Disease Risk

Author

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  • Tom P. Fleming

    (Biological Sciences, Southampton General Hospital, University of Southampton, Southampton SO16 6YD, UK)

  • Congshan Sun

    (Departments of Neurology and Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA
    Center for Genetic Muscle Disorders, Hugo W. Moser Research Institute at Kennedy Krieger Institute, Baltimore, MD 21205, USA)

  • Oleg Denisenko

    (Department of Medicine, University of Washington, 850 Republican St., Rm 242, Seattle, WA 98109, USA)

  • Laura Caetano

    (Biological Sciences, Southampton General Hospital, University of Southampton, Southampton SO16 6YD, UK)

  • Anan Aljahdali

    (Biological Sciences, Southampton General Hospital, University of Southampton, Southampton SO16 6YD, UK
    Department of Biological Sciences, Faculty of Science, Alfaisaliah campus, University of Jeddah, Jeddah 23442, Saudi Arabia)

  • Joanna M. Gould

    (Clinical Neurosciences and Psychiatry, Clinical and Experimental Sciences, Faculty of Medicine, University of Southampton, Southampton SO16 6YD, UK)

  • Pooja Khurana

    (Biological Sciences, Southampton General Hospital, University of Southampton, Southampton SO16 6YD, UK
    Institute for Biogenesis Research, Research Corporation of the University of Hawaii, Manoa, Honolulu, HI 96822, USA)

Abstract

Environment around conception can influence the developmental programme with lasting effects on gestational and postnatal phenotype and with consequences for adult health and disease risk. Peri-conception exposure comprises a crucial part of the ‘Developmental Origins of Health and Disease’ (DOHaD) concept. In this review, we consider the effects of maternal undernutrition experienced during the peri-conception period in select human models and in a mouse experimental model of protein restriction. Human datasets indicate that macronutrient deprivation around conception affect the epigenome, with enduring effects on cardiometabolic and neurological health. The mouse model, comprising maternal low protein diet exclusively during the peri-conception period, has revealed a stepwise progression in altered developmental programming following induction through maternal metabolite deficiency. This progression includes differential effects in extra-embryonic and embryonic cell lineages and tissues, leading to maladaptation in the growth trajectory and increased chronic disease comorbidities. The timeline embraces an array of mechanisms across nutrient sensing and signalling, cellular, metabolic, epigenetic and physiological processes with a coordinating role for mTORC1 signalling proposed. Early embryos appear active participants in environmental sensing to optimise the developmental programme for survival but with the trade-off of later disease. Similar adverse health outcomes may derive from other peri-conception environmental experiences, including maternal overnutrition, micronutrient availability, pollutant exposure and assisted reproductive treatments (ART) and support the need for preconception health before pregnancy.

Suggested Citation

  • Tom P. Fleming & Congshan Sun & Oleg Denisenko & Laura Caetano & Anan Aljahdali & Joanna M. Gould & Pooja Khurana, 2021. "Environmental Exposures around Conception: Developmental Pathways Leading to Lifetime Disease Risk," IJERPH, MDPI, vol. 18(17), pages 1-19, September.
    • Handle: RePEc:gam:jijerp:v:18:y:2021:i:17:p:9380-:d:629630
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    References listed on IDEAS

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    1. Lon J. Van Winkle & Vasiliy Galat & Philip M. Iannaccone, 2020. "Lysine Deprivation during Maternal Consumption of Low-Protein Diets Could Adversely Affect Early Embryo Development and Health in Adulthood," IJERPH, MDPI, vol. 17(15), pages 1-9, July.
    2. Sophie E. Moore & Timothy J. Cole & Elizabeth M. E. Poskitt & Bakary J. Sonko & Roger G. Whitehead & Ian A. McGregor & Andrew M. Prentice, 1997. "Season of birth predicts mortality in rural Gambia," Nature, Nature, vol. 388(6641), pages 434-434, July.
    3. Ekamper, P. & van Poppel, F. & Stein, A.D. & Lumey, L.H., 2014. "Independent and additive association of prenatal famine exposure and intermediary life conditions with adult mortality between age 18–63 years," Social Science & Medicine, Elsevier, vol. 119(C), pages 232-239.
    4. Nastaran Salavati & Marian K Bakker & Fraser Lewis & Petra C Vinke & Farya Mubarik & JanJaap H M Erwich & Eline M van der Beek, 2020. "Associations between preconception macronutrient intake and birth weight across strata of maternal BMI," PLOS ONE, Public Library of Science, vol. 15(12), pages 1-19, December.
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    Cited by:

    1. Prachand Issarapu & Manisha Arumalla & Hannah R. Elliott & Suraj S. Nongmaithem & Alagu Sankareswaran & Modupeh Betts & Sara Sajjadi & Noah J. Kessler & Swati Bayyana & Sohail R. Mansuri & Maria Derak, 2023. "DNA methylation at the suppressor of cytokine signaling 3 (SOCS3) gene influences height in childhood," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    2. Rebecca Jean Ryznar & Lacie Phibbs & Lon J. Van Winkle, 2021. "Epigenetic Modifications at the Center of the Barker Hypothesis and Their Transgenerational Implications," IJERPH, MDPI, vol. 18(23), pages 1-12, December.

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