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. 2018 Apr 23:9:161.
doi: 10.3389/fendo.2018.00161. eCollection 2018.

Maternal Diet, Metabolic State, and Inflammatory Response Exert Unique and Long-Lasting Influences on Offspring Behavior in Non-Human Primates

Jacqueline R Thompson  1   2 , Hanna C Gustafsson  3 , Madison DeCapo  1   2 , Diana L Takahashi  2 , Jennifer L Bagley  1   2 , Tyler A Dean  2 , Paul Kievit  2 , Damien A Fair  3   4 , Elinor L Sullivan  1   2   3   5
Affiliations

Maternal Diet, Metabolic State, and Inflammatory Response Exert Unique and Long-Lasting Influences on Offspring Behavior in Non-Human Primates

Jacqueline R Thompson et al. Front Endocrinol (Lausanne). .

Abstract

Nutritional status influences brain health and gestational exposure to metabolic disorders (e.g. obesity and diabetes) increases the risk of neuropsychiatric disorders. The aim of the present study was to further investigate the role of maternal Western-style diet (WSD), metabolic state, and inflammatory factors in the programming of Japanese macaque offspring behavior. Utilizing structural equation modeling, we investigated the relationships between maternal diet, prepregnancy adiposity, third trimester insulin response, and plasma cytokine levels on 11-month-old offspring behavior. Maternal WSD was associated with greater reactive and ritualized anxiety in offspring. Maternal adiposity and third trimester macrophage-derived chemokine (MDC) exerted opposing effects on offspring high-energy outbursts. Elevated levels of this behavior were associated with low maternal MDC and increased prepregnancy adiposity. This is the first study to show that maternal MDC levels influence offspring behavior. We found no evidence suggesting maternal peripheral inflammatory response mediated the effect of maternal diet and metabolic state on aberrant offspring behavior. Additionally, the extent of maternal metabolic impairment differentially influenced chemokine response. Elevated prepregnancy adiposity suppressed third trimester chemokines, while obesity-induced insulin resistance augmented peripheral chemokine levels. WSD also directly increased maternal interleukin-12. This is the first non-human primate study to delineate the effects of maternal diet and metabolic state on gestational inflammatory environment and subsequent offspring behavior. Our findings give insight to the complex mechanisms by which diet, metabolic state, and inflammation during pregnancy exert unique influences on offspring behavioral regulation.

Keywords: Western-style; adiposity; behavior; development; diet; inflammation; macaque; macrophage-derived chemokine (MDC); maternal.

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Figures

Figure 1
Figure 1
Perinatal environmental influences on offspring behavioral response. This figure presents the consolidated results of five different offspring behavior models, identical in every aspect except for the outcome behavior variable. Solid black lines were significant (p < 0.05) in every behavior model and gray dashed lines were not significant in any model. Magenta lines (labeled a–d) were significant in some behavior models; the inset table details the significant direct effects of the corresponding model. Paths were also estimated from maternal age to prepregnancy adiposity, third trimester IAUC, and third trimester MDC and were consistent across all behavior models but were not depicted for ease of readability. WSD, Western-style diet; IAUC, insulin area under the curve. *p < 0.05 and **p < 0.01.
Figure 2
Figure 2
Gestational MDC and IL-12 response and degree of metabolic impairment. (A) In the presented model for maternal third trimester MDC, paths were also estimated from maternal age at birth to prepregnancy adiposity (β = 0.54, p < 0.001), third trimester IAUC (β = −0.02, p = 0.80), and maternal third trimester MDC (β = 0.03, p = 0.80), but were not visually depicted for ease of readability. (B) In the presented model for maternal third trimester, IL-12 paths were also estimated from maternal age at birth to prepregnancy adiposity (β = 0.54, p < 0.001), third trimester IAUC (β = −0.03, p = 0.74), and maternal third trimester IL-12 (β = −0.08, p = 0.58), but were not visually depicted for ease of readability. Black lines indicate significant direct effects (p < 0.05) and are labeled with β value. See results for further details on model fit and indirect effects. Gray dashed lines indicate paths that were estimated but were not statistically significant. WSD, Western-style diet; IAUC, insulin area under the curve; IL, interleukin. *p < 0.05 and **p < 0.01.
Figure 3
Figure 3
Gestational chemokine response and degree of metabolic impairment. The model for chemokine latent variable is presented with constituent chemokine protein markers and the corresponding standardized factor loadings. Paths were also estimated from maternal age at birth to prepregnancy adiposity (β = 0.53, p < 0.001), third trimester IAUC (β = −0.02, p = 0.83), and maternal third trimester chemokines (β = 0.24, p = 0.04) but were not visually depicted for ease of readability. Black lines indicate significant direct effects (p < 0.05) and are labeled with β value. See results for further details on model fit and indirect effects. Gray dashed lines indicate paths that were estimated but were not statistically significant. WSD, Western-style diet; IAUC, insulin area under the curve. *p < 0.05 and **p < 0.01.
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