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Perinatal Exposure to Western Diet Programs Autonomic Dysfunction in the Male Offspring

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Abstract

Although the deleterious influence of protein deficiency on fetal programming is well documented, the impact of a Western diet on epigenetic mechanisms is less clear. We hypothesized that high-fat high-sucrose diet (HFHSD) consumption during pregnancy leads to epigenetic modifications within the progeny’s compensatory renin–angiotensin system (RAS), affecting autonomic and metabolic functions. Dams were fed HFHSD (45% fat and 30% sucrose) or regular chow (RD) from mating until weaning of the pups (~7 weeks). Offspring from both groups were then maintained on chow and studied in adulthood (3–7 months). Offspring from HFHSD-exposed dams (OH) exhibited no difference in body weight or fasting blood glucose compared to controls (OR). In 3-month-old offspring, DNA methylation was significantly lower for the ACE2 gene (P < 0.05) in the brainstem, kidney and cecum. Moreover, ACE2 activity in the hypothalamus was increased at 7 months (OH: 91 ± 1 vs. OR: 74 ± 4 AFU/mg/min, P < 0.05). Although baseline blood pressure was not different between groups, vagal tone in OH was significantly impaired compared to OR. At the same time, OH offspring had a 1.7-fold increase in AT1a receptor expression and a 1.3-fold increase in ADAM17 mRNA. DOCA-salt treatment further revealed and exacerbated hypertensive response in the OH progeny (OH: 130 ± 6 vs. OR: 108 ± 3 mmHg, P < 0.05). Taken together, our data suggest that perinatal exposure to HFHSD resulted in epigenetic modifications of the compensatory brain RAS, potentially affecting plasticity of neuronal networks leading to autonomic dysfunction in the male offspring.

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Acknowledgements

The authors would like to thank Dr. Weining Tang (Omega Bio-tek, Norcross, GA) for providing technical expertise regarding the design of the methylation array.

Funding

This work was supported by an Established Investigator Award from the American Heart Association (12EIA8030004 to E.L.), the National Center for Research Resources (RR018766), and the National Institute of General Medical Sciences (GM103514 and GM106392).

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Authors and Affiliations

  1. Department of Pharmacology and Experimental Therapeutics and Cardiovascular Center of Excellence, Louisiana State University Health Sciences Center, New Orleans, LA, USA

    Snigdha Mukerjee & Eric Lazartigues

  2. Department of Epidemiology, University of Florida, Gainesville, FL, USA

    Yun Zhu & Jinying Zhao

  3. Department of Physiology, Tulane University, New Orleans, LA, USA

    Andrea Zsombok

  4. Department of Medicine, Tulane University, New Orleans, LA, USA

    Franck Mauvais-Jarvis

  5. Department of Pharmacology and Experimental Therapeutics, School of Medicine, Louisiana State University Health Sciences Center, 1901 Perdido Street, Room 5218, New Orleans, LA, 70112, USA

    Eric Lazartigues

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  1. Snigdha Mukerjee
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Mukerjee, S., Zhu, Y., Zsombok, A. et al. Perinatal Exposure to Western Diet Programs Autonomic Dysfunction in the Male Offspring. Cell Mol Neurobiol 38, 233–242 (2018). https://doi.org/10.1007/s10571-017-0502-4

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