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Maternal diet and gut microbiota influence predisposition to cardiovascular disease in the offspring

Hamdi Jama, Malathi S.I. Dona, Evany Dinakis, Michael Nakai, Madeleine R. Paterson, Waled Shihata, Crisdion Krstevski, Charles. D. Cohen, Kate L. Weeks, Gabriella E. Farrugia, Chad Johnson, Ekaterina Salimova, Daniel Donner, Helen Kiriazis, Harikrishnan Kaipananickal, Jun Okabe, Dovile Anderson, Darren J. Creek, Charles R. Mackay, Assam El-Osta, Alexander R. Pinto, David M. Kaye, Francine Z Marques
doi: https://doi.org/10.1101/2022.03.12.480450
Hamdi Jama
1Hypertension Research Laboratory, School of Biological Sciences, Monash University, Melbourne, VIC., Australia
2Heart Failure Research Group Baker Heart and Diabetes Institute, Melbourne, VIC., Australia
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Malathi S.I. Dona
3Cardiac Cellular Systems, Baker Heart and Diabetes Institute, Melbourne, VIC, Australia
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Evany Dinakis
1Hypertension Research Laboratory, School of Biological Sciences, Monash University, Melbourne, VIC., Australia
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Michael Nakai
1Hypertension Research Laboratory, School of Biological Sciences, Monash University, Melbourne, VIC., Australia
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Madeleine R. Paterson
1Hypertension Research Laboratory, School of Biological Sciences, Monash University, Melbourne, VIC., Australia
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Waled Shihata
2Heart Failure Research Group Baker Heart and Diabetes Institute, Melbourne, VIC., Australia
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Crisdion Krstevski
3Cardiac Cellular Systems, Baker Heart and Diabetes Institute, Melbourne, VIC, Australia
4Centre for Cardiovascular Biology and Disease Research, La Trobe University, Melbourne, Victoria, Australia
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Charles. D. Cohen
3Cardiac Cellular Systems, Baker Heart and Diabetes Institute, Melbourne, VIC, Australia
4Centre for Cardiovascular Biology and Disease Research, La Trobe University, Melbourne, Victoria, Australia
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Kate L. Weeks
5Department of Anatomy & Physiology, The University of Melbourne, Parkville, VIC, Australia
6Baker Department of Cardiometabolic Health, The University of Melbourne, Parkville, VIC, Australia
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Gabriella E. Farrugia
3Cardiac Cellular Systems, Baker Heart and Diabetes Institute, Melbourne, VIC, Australia
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Chad Johnson
7Monash Micro Imaging, Monash University, Melbourne, Australia
8La Trobe Institute of Molecular Science, La Trobe University, Melbourne, Victoria, Australia
9Burnet Institute, Melbourne, VIC, Australia
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Ekaterina Salimova
10Monash Biomedical Imaging, Monash University, Melbourne, Australia
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Daniel Donner
5Department of Anatomy & Physiology, The University of Melbourne, Parkville, VIC, Australia
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Helen Kiriazis
5Department of Anatomy & Physiology, The University of Melbourne, Parkville, VIC, Australia
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Harikrishnan Kaipananickal
11Epigenetics in Human Health and Disease, Central Clinical School, Alfred Centre, Monash University Melbourne, VIC, Australia
12Department of Clinical Pathology, University of Melbourne, VIC, Australia
13Department of Diabetes, Central Clinical School, Monash University, Melbourne, VIC, Australia
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Jun Okabe
11Epigenetics in Human Health and Disease, Central Clinical School, Alfred Centre, Monash University Melbourne, VIC, Australia
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Dovile Anderson
14Monash Institute of Pharmaceutical Sciences, Monash University, Melbourne, Australia
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Darren J. Creek
14Monash Institute of Pharmaceutical Sciences, Monash University, Melbourne, Australia
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Charles R. Mackay
14Monash Institute of Pharmaceutical Sciences, Monash University, Melbourne, Australia
16Department of Biochemistry and Molecular Biology, Monash University, Melbourne, Australia
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Assam El-Osta
11Epigenetics in Human Health and Disease, Central Clinical School, Alfred Centre, Monash University Melbourne, VIC, Australia
12Department of Clinical Pathology, University of Melbourne, VIC, Australia
13Department of Diabetes, Central Clinical School, Monash University, Melbourne, VIC, Australia
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Alexander R. Pinto
3Cardiac Cellular Systems, Baker Heart and Diabetes Institute, Melbourne, VIC, Australia
4Centre for Cardiovascular Biology and Disease Research, La Trobe University, Melbourne, Victoria, Australia
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David M. Kaye
2Heart Failure Research Group Baker Heart and Diabetes Institute, Melbourne, VIC., Australia
17Department of Cardiology, Alfred Hospital, Melbourne, Australia
18Central Clinical School, Faculty of Medicine Nursing and Health Sciences, Monash University, Melbourne, Australia
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Francine Z Marques
1Hypertension Research Laboratory, School of Biological Sciences, Monash University, Melbourne, VIC., Australia
2Heart Failure Research Group Baker Heart and Diabetes Institute, Melbourne, VIC., Australia
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  • For correspondence: francine.marques@monash.edu
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Abstract

Cardiovascular disease is one of the most significant causes of death globally, especially in regions where unhealthy diets are prevalent and dietary fibre intake is low.1,2 Fibre, particularly prebiotic types that feed gut microbes, is essential for maintaining healthy gut microbial ecosystems.3 One assumption has been that cardiovascular health relates directly to lifestyle choices in adult life. Here, we show in mice that some of these benefits operate from the prenatal stage and relate to the diet and gut microbiome of the mother. Intake of fibre during pregnancy shaped the mothers’ gut microbiome, which had a lasting founding effect on the offspring’s microbial composition and function. Maternal fibre intake during pregnancy significantly changed the cardiac cellular and molecular landscape in the offspring, protecting them against the development of cardiac hypertrophy, remodelling, and inflammation. These suggest a role for foetal exposure to maternal-derived gut microbial metabolites, which are known to cross the placenta and drive epigenetic changes. Maternal fibre intake led to foetal epigenetic reprogramming of the atrial natriuretic peptide gene (Nppa), protective against heart failure. These results underscore the importance of dietary intake and the gut microbiome of the mother during pregnancy for cardiovascular disease in the offspring.

Competing Interest Statement

DMK (GNT2008017) and AEO (GTN1154650) are supported by fellowships from the National Health & Medical Research Council of Australia (NHMRC). FZM is supported by a Senior Medical Research Fellowship from the Sylvia and Charles Viertel Charitable Foundation Fellowship. FZM (101185, 105663) and KLW (102539) are supported by National Heart Foundation Future Leader Fellowships. The Baker Heart & Diabetes Institute is supported in part by the Victorian Government's Operational Infrastructure Support Program.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Maternal diet and gut microbiota influence predisposition to cardiovascular disease in the offspring
Hamdi Jama, Malathi S.I. Dona, Evany Dinakis, Michael Nakai, Madeleine R. Paterson, Waled Shihata, Crisdion Krstevski, Charles. D. Cohen, Kate L. Weeks, Gabriella E. Farrugia, Chad Johnson, Ekaterina Salimova, Daniel Donner, Helen Kiriazis, Harikrishnan Kaipananickal, Jun Okabe, Dovile Anderson, Darren J. Creek, Charles R. Mackay, Assam El-Osta, Alexander R. Pinto, David M. Kaye, Francine Z Marques
bioRxiv 2022.03.12.480450; doi: https://doi.org/10.1101/2022.03.12.480450
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Maternal diet and gut microbiota influence predisposition to cardiovascular disease in the offspring
Hamdi Jama, Malathi S.I. Dona, Evany Dinakis, Michael Nakai, Madeleine R. Paterson, Waled Shihata, Crisdion Krstevski, Charles. D. Cohen, Kate L. Weeks, Gabriella E. Farrugia, Chad Johnson, Ekaterina Salimova, Daniel Donner, Helen Kiriazis, Harikrishnan Kaipananickal, Jun Okabe, Dovile Anderson, Darren J. Creek, Charles R. Mackay, Assam El-Osta, Alexander R. Pinto, David M. Kaye, Francine Z Marques
bioRxiv 2022.03.12.480450; doi: https://doi.org/10.1101/2022.03.12.480450

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