Adiponectin deficiency and high fat and sucrose diets impair pancreatic islet adaptations to pregnancy and contribute to gestational hyperglycemia

脂联素缺乏以及高脂肪和高蔗糖饮食会损害胰岛对妊娠的适应性,并导致妊娠期高血糖。

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Abstract

Gestational diabetes mellitus is characterized by hyperglycemia and impaired glucose tolerance with first onset in pregnancy. Clinical research shows an association between low circulating adiponectin levels and gestational diabetes mellitus diagnosis. Adiponectin is a fat-derived cytokine which is postulated to improve insulin secretion and survival of pancreatic β-cells; however, the role of adiponectin in the regulation of late pregnancy glucose homeostasis requires investigation. We investigated metabolic, morphological, and functional adaptations of pancreatic islets to pregnancy in adiponectin knockout and wild-type female mice and the interaction with low fat (LF) or high fat and sucrose (HFS) diets. Pregnant wild-type mice fed a HFS diet exhibited elevated fasting glycemia and glucose intolerance, accompanied by impaired insulinogenic index at gestational day 18.5 compared to LF-fed controls, and interestingly both LF and HFS-fed adiponectin knockout mice exhibited similar impairments. Pregnancy-induced pancreatic β-cell expansion was largely preserved during late pregnancy, though the HFS diet attenuated β-cell mass at gestational day 18.5 and adiponectin deficiency triggered a similar level of impairment. Glucose stimulated insulin secretion was significantly attenuated in islets isolated from pregnant wild-type mice fed HFS diet and both LF and HFS-fed pregnant adiponectin knockout mice showed a similar level of impaired despite similar basal secretion and insulin content. Gene expression analysis of islets from pregnant mice revealed reduced Nkx6.1 and downregulation of metabolism genes (Ppargc1a, Cpt1a) and Adipor1, without changes in insulin synthesis/secretion genes or mitochondrial electron transport chain components in both the HFS-fed wild-type and both LF- and HFS-fed adiponectin knockout mice compared to wild-type LF-fed controls. These findings demonstrate that HFS feeding and adiponectin deficiency trigger a similar level of impaired insulin secretion during pregnancy that contributes to hyperglycemia, which suggests increasing adiponectin levels during pregnancy has potential therapeutic benefit. SIGNIFICANCE STATEMENT: We show that in late pregnancy, the absence of adiponectin elicits a similar level of impaired insulin secretion as high fat/sucrose diet-induced obesity, but without a synergistic effect. This suggests interventions to enhance adiponectin could improve insulin secretion and prevent gestational diabetes mellitus.

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