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Relationship between salivary/pancreatic amylase and body mass index: a systems biology approach

Identifieur interne : 000462 ( Main/Exploration ); précédent : 000461; suivant : 000463

Relationship between salivary/pancreatic amylase and body mass index: a systems biology approach

Auteurs : Amélie Bonnefond [France] ; Loïc Yengo [France, Australie] ; Aurélie Dechaume [France] ; Mickaël Canouil [France] ; Maxime Castelain [France] ; Estelle Roger [France] ; Frédéric Allegaert [France] ; Robert Caiazzo [France] ; Violeta Raverdy [France] ; Marie Pigeyre [France] ; Abdelilah Arredouani [Qatar] ; Jean-Michel Borys [France] ; Claire Lévy-Marchal [France] ; Jacques Weill [France] ; Ronan Roussel [France] ; Beverley Balkau [France] ; Michel Marre [France] ; François Pattou [France] ; Thierry Brousseau [France] ; Philippe Froguel [France]

Source :

RBID : PMC:5322607

Descripteurs français

English descriptors

Abstract

Background

Salivary (AMY1) and pancreatic (AMY2) amylases hydrolyze starch. Copy number of AMY1A (encoding AMY1) was reported to be higher in populations with a high-starch diet and reduced in obese people. These results based on quantitative PCR have been challenged recently. We aimed to re-assess the relationship between amylase and adiposity using a systems biology approach.

Methods

We assessed the association between plasma enzymatic activity of AMY1 or AMY2, and several metabolic traits in almost 4000 French individuals from D.E.S.I.R. longitudinal study. The effect of the number of copies of AMY1A (encoding AMY1) or AMY2A (encoding AMY2) measured through droplet digital PCR was then analyzed on the same parameters in the same study. A Mendelian randomization analysis was also performed. We subsequently assessed the association between AMY1A copy number and obesity risk in two case-control studies (5000 samples in total). Finally, we assessed the association between body mass index (BMI)-related plasma metabolites and AMY1 or AMY2 activity.

Results

We evidenced strong associations between AMY1 or AMY2 activity and lower BMI. However, we found a modest contribution of AMY1A copy number to lower BMI. Mendelian randomization identified a causal negative effect of BMI on AMY1 and AMY2 activities. Yet, we also found a significant negative contribution of AMY1 activity at baseline to the change in BMI during the 9-year follow-up, and a significant contribution of AMY1A copy number to lower obesity risk in children, suggesting a bidirectional relationship between AMY1 activity and adiposity. Metabonomics identified a BMI-independent association between AMY1 activity and lactate, a product of complex carbohydrate fermentation.

Conclusions

These findings provide new insights into the involvement of amylase in adiposity and starch metabolism.

Electronic supplementary material

The online version of this article (doi:10.1186/s12916-017-0784-x) contains supplementary material, which is available to authorized users.


Url:
DOI: 10.1186/s12916-017-0784-x
PubMed: 28228143
PubMed Central: 5322607


Affiliations:


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Doha, 5825 Qatar</nlm:aff>
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Sorbonne Paris-Cité, Paris, 75013 France</nlm:aff>
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Villejuif, 94807 France</nlm:aff>
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Sorbonne Paris-Cité, Paris, 75013 France</nlm:aff>
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Lille, 59000 France</nlm:aff>
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Lille, 59000 France</nlm:aff>
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<term>Male</term>
<term>Obesity (enzymology)</term>
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<term>Salivary alpha-Amylases (metabolism)</term>
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<term>Biologie des systèmes</term>
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<front>
<div type="abstract" xml:lang="en">
<sec>
<title>Background</title>
<p>Salivary (AMY1) and pancreatic (AMY2) amylases hydrolyze starch. Copy number of
<italic>AMY1A</italic>
(encoding AMY1) was reported to be higher in populations with a high-starch diet and reduced in obese people. These results based on quantitative PCR have been challenged recently. We aimed to re-assess the relationship between amylase and adiposity using a systems biology approach.</p>
</sec>
<sec>
<title>Methods</title>
<p>We assessed the association between plasma enzymatic activity of AMY1 or AMY2, and several metabolic traits in almost 4000 French individuals from D.E.S.I.R. longitudinal study. The effect of the number of copies of
<italic>AMY1A</italic>
(encoding AMY1) or
<italic>AMY2A</italic>
(encoding AMY2) measured through droplet digital PCR was then analyzed on the same parameters in the same study. A Mendelian randomization analysis was also performed. We subsequently assessed the association between
<italic>AMY1A</italic>
copy number and obesity risk in two case-control studies (5000 samples in total). Finally, we assessed the association between body mass index (BMI)-related plasma metabolites and AMY1 or AMY2 activity.</p>
</sec>
<sec>
<title>Results</title>
<p>We evidenced strong associations between AMY1 or AMY2 activity and lower BMI. However, we found a modest contribution of
<italic>AMY1A</italic>
copy number to lower BMI. Mendelian randomization identified a causal negative effect of BMI on AMY1 and AMY2 activities. Yet, we also found a significant negative contribution of AMY1 activity at baseline to the change in BMI during the 9-year follow-up, and a significant contribution of
<italic>AMY1A</italic>
copy number to lower obesity risk in children, suggesting a bidirectional relationship between AMY1 activity and adiposity. Metabonomics identified a BMI-independent association between AMY1 activity and lactate, a product of complex carbohydrate fermentation.</p>
</sec>
<sec>
<title>Conclusions</title>
<p>These findings provide new insights into the involvement of amylase in adiposity and starch metabolism.</p>
</sec>
<sec>
<title>Electronic supplementary material</title>
<p>The online version of this article (doi:10.1186/s12916-017-0784-x) contains supplementary material, which is available to authorized users.</p>
</sec>
</div>
</front>
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</TEI>
<affiliations>
<list>
<country>
<li>Australie</li>
<li>France</li>
<li>Qatar</li>
</country>
<region>
<li>Hauts-de-France</li>
<li>Nord-Pas-de-Calais</li>
<li>Île-de-France</li>
</region>
<settlement>
<li>Lille</li>
<li>Paris</li>
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</list>
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<country name="France">
<region name="Hauts-de-France">
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<name sortKey="Balkau, Beverley" sort="Balkau, Beverley" uniqKey="Balkau B" first="Beverley" last="Balkau">Beverley Balkau</name>
<name sortKey="Borys, Jean Michel" sort="Borys, Jean Michel" uniqKey="Borys J" first="Jean-Michel" last="Borys">Jean-Michel Borys</name>
<name sortKey="Brousseau, Thierry" sort="Brousseau, Thierry" uniqKey="Brousseau T" first="Thierry" last="Brousseau">Thierry Brousseau</name>
<name sortKey="Caiazzo, Robert" sort="Caiazzo, Robert" uniqKey="Caiazzo R" first="Robert" last="Caiazzo">Robert Caiazzo</name>
<name sortKey="Caiazzo, Robert" sort="Caiazzo, Robert" uniqKey="Caiazzo R" first="Robert" last="Caiazzo">Robert Caiazzo</name>
<name sortKey="Canouil, Mickael" sort="Canouil, Mickael" uniqKey="Canouil M" first="Mickaël" last="Canouil">Mickaël Canouil</name>
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<name sortKey="Levy Marchal, Claire" sort="Levy Marchal, Claire" uniqKey="Levy Marchal C" first="Claire" last="Lévy-Marchal">Claire Lévy-Marchal</name>
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<name sortKey="Marre, Michel" sort="Marre, Michel" uniqKey="Marre M" first="Michel" last="Marre">Michel Marre</name>
<name sortKey="Marre, Michel" sort="Marre, Michel" uniqKey="Marre M" first="Michel" last="Marre">Michel Marre</name>
<name sortKey="Pattou, Francois" sort="Pattou, Francois" uniqKey="Pattou F" first="François" last="Pattou">François Pattou</name>
<name sortKey="Pattou, Francois" sort="Pattou, Francois" uniqKey="Pattou F" first="François" last="Pattou">François Pattou</name>
<name sortKey="Pigeyre, Marie" sort="Pigeyre, Marie" uniqKey="Pigeyre M" first="Marie" last="Pigeyre">Marie Pigeyre</name>
<name sortKey="Pigeyre, Marie" sort="Pigeyre, Marie" uniqKey="Pigeyre M" first="Marie" last="Pigeyre">Marie Pigeyre</name>
<name sortKey="Raverdy, Violeta" sort="Raverdy, Violeta" uniqKey="Raverdy V" first="Violeta" last="Raverdy">Violeta Raverdy</name>
<name sortKey="Raverdy, Violeta" sort="Raverdy, Violeta" uniqKey="Raverdy V" first="Violeta" last="Raverdy">Violeta Raverdy</name>
<name sortKey="Roger, Estelle" sort="Roger, Estelle" uniqKey="Roger E" first="Estelle" last="Roger">Estelle Roger</name>
<name sortKey="Roussel, Ronan" sort="Roussel, Ronan" uniqKey="Roussel R" first="Ronan" last="Roussel">Ronan Roussel</name>
<name sortKey="Roussel, Ronan" sort="Roussel, Ronan" uniqKey="Roussel R" first="Ronan" last="Roussel">Ronan Roussel</name>
<name sortKey="Roussel, Ronan" sort="Roussel, Ronan" uniqKey="Roussel R" first="Ronan" last="Roussel">Ronan Roussel</name>
<name sortKey="Weill, Jacques" sort="Weill, Jacques" uniqKey="Weill J" first="Jacques" last="Weill">Jacques Weill</name>
<name sortKey="Yengo, Loic" sort="Yengo, Loic" uniqKey="Yengo L" first="Loïc" last="Yengo">Loïc Yengo</name>
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<country name="Australie">
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<name sortKey="Yengo, Loic" sort="Yengo, Loic" uniqKey="Yengo L" first="Loïc" last="Yengo">Loïc Yengo</name>
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<country name="Qatar">
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<name sortKey="Arredouani, Abdelilah" sort="Arredouani, Abdelilah" uniqKey="Arredouani A" first="Abdelilah" last="Arredouani">Abdelilah Arredouani</name>
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