Increasing evidence shows that maternal nutrition status has a vital effect on offspring susceptibility to obesity. MicroRNAs are related to lipid metabolism processes. This study aimed to evaluate whether maternal chromium restriction could affect miRNA expression involved in lipid metabolism in offspring. Weaning C57BL/6J mice born from mothers fed with normal control diet or chromium-restricted diet were fed for 13 weeks. The adipose miRNA expression profile was analyzed by miRNA array analysis. At 16 weeks old, pups from dams fed with chromium-restricted diet exhibit higher body weight, fat weight, and serum TC, TG levels. Six miRNAs were identified as upregulated in the RC group compared with the CC group, whereas eight miRNAs were lower than the threshold level set in the RC group. In the validated target genes of these differentially expressed miRNA, the MAPK signaling pathway serves an important role in the influence of early life chromium-restricted diet on lipid metabolism through miRNA. Long-term programming on various specific miRNA and MAPK signaling pathway may be involved in maternal chromium restriction in the adipose of female offspring.
Impact statement
For the first time, our study demonstrates important miRNA differences in the effect of maternal chromium restriction in offspring. These miRNAs may serve as “bridges” between the mother and the offspring by affecting the MAPK pathway.
HalesCNBarkerDJClarkPMCoxLJFallCOsmondCWinterPD. Fetal and infant growth and impaired glucose tolerance at age 64. BMJ1991; 303: 1019–22.
2.
RavelliACvan der MeulenJHMichelsRPOsmondCBarkerDJHalesCNBlekerOP. Glucose tolerance in adults after prenatal exposure to famine. Lancet1998; 351: 173–7.
3.
ZucchiFCYaoYMetzGA. The secret language of destiny: stress imprinting and transgenerational origins of disease. Front Genet2012; 3: 96–96.
4.
CohenJELeePRChenSLiWFieldsRD. MicroRNA regulation of homeostatic synaptic plasticity. Proc Natl Acad Sci U S A2011; 108: 11650–5.
5.
BoardFaN. Recommended dietary allowances, Washington, DC: National Academy Press, 2000.
6.
AndersonRA. Chromium, glucose intolerance and diabetes. J Am Coll Nutr1998; 17: 548–55.
7.
AndersonRAKozlovskyAS. Chromium intake, absorption and excretion of subjects consuming self-selected diets. Am J Clin Nutr1985; 41: 1177–83.
8.
AndersonRA. Chromium in the prevention and control of diabetes. Diabetes Metab2000; 26: 22–7.
9.
OffenbacherEGPi-SunyerFX. Beneficial effect of chromium-rich yeast on glucose tolerance and blood lipids in elderly subjects. Diabetes1980; 29: 919–25.
10.
SuksomboonNPoolsupNYuwanakornA. Systematic review and meta-analysis of the efficacy and safety of chromium supplementation in diabetes. J Clin Pharm Ther2014; 39: 292–306.
11.
LefaviRGAndersonRAKeithREWilsonGDMcMillanJLStoneMH. Efficacy of chromium supplementation in athletes: emphasis on anabolism. Int J Sport Nutr1992; 2: 111–22.
12.
FengWZhaoTMaoGWangWFengYLiFZhengDWuHJinDYangLWuX. Type 2 diabetic rats on diet supplemented with chromium malate show improved glycometabolism, glycometabolism-related enzyme levels and lipid metabolism. PLoS One2015; 10: e0125952–e0125952.
13.
FengWMaoGLiQWangWChenYZhaoTLiFZouYWuHYangLWuX. Effects of chromium malate on glycometabolism, glycometabolism-related enzyme levels and lipid metabolism in type 2 diabetic rats: a dose-response and curative effects study. J Diabetes Investig2015; 6: 396–407.
ZhangQSunXXiaoXZhengJLiMYuMPingFWangZQiCWangTWangX. Effects of maternal chromium restriction on the long-term programming in MAPK signaling pathway of lipid metabolism in mice. Nutrients2016; 8: 488–488.
16.
Najafi-ShoushtariSHKristoFLiYShiodaTCohenDEGersztenRENaarAM. MicroRNA-33 and the SREBP host genes cooperate to control cholesterol homeostasis. Science2010; 328: 1566–9.
17.
LiWQChenCXuMDGuoJLiYMXiaQMLiuHMHeJYuHYZhuL. The rno-miR-34 family is upregulated and targets ACSL1 in dimethylnitrosamine-induced hepatic fibrosis in rats. FEBS J2011; 278: 1522–32.
18.
TsaiWCHsuSDHsuCSLaiTCChenSJShenRHuangYChenHCLeeCHTsaiTFHsuMTWuJCHuangHDShiaoMSHsiaoMTsouAP. MicroRNA-122 plays a critical role in liver homeostasis and hepatocarcinogenesis. J Clin Invest2012; 122: 2884–97.
19.
AikenCEOzanneSE. Sex differences in developmental programming models. Reproduction2013; 145: R1–13.
20.
TaylorBAPhillipsSJ. Detection of obesity QTLs on mouse chromosomes 1 and 7 by selective DNA pooling. Genomics1996; 34: 389–98.
21.
ZhangQXiaoXLiMLiWYuMZhangHWangZXiangH. Acarbose reduces blood glucose by activating miR-10a-5p and miR-664 in diabetic rats. PloS one2013; 8: e79697–e79697.
ChouCHChangNWShresthaSHsuSDLinYLLeeWHYangCDHongHCWeiTYTuSJTsaiTRHoSYJianTYWuHYChenPRLinNCHuangHTYangTLPaiCYTaiCSChenWLHuangCYLiuCCWengSLLiaoKWHsuWLHuangHD. miRTarBase 2016: updates to the experimentally validated miRNA-target interactions database. Nucleic Acids Res2016; 44: D239–47.
24.
DennisGJrShermanBTHosackDAYangJGaoWLaneHCLempickiRA. DAVID: database for annotation, visualization, and integrated discovery. Genome Biol2003; 4: P3–P3.
25.
ShannonPMarkielAOzierOBaligaNSWangJTRamageDAminNSchwikowskiBIdekerT. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res2003; 13: 2498–504.
26.
KumarKALalithaAPavithraDPadmavathiIJGaneshanMRaoKRVenuLBalakrishnaNShankerNHReddySUChandakGRSenguptaSRaghunathM. Maternal dietary folate and/or vitamin B12 restrictions alter body composition (adiposity) and lipid metabolism in Wistar rat offspring. J Nutr Biochem2013; 24: 25–31.
27.
TinkovAAPopovaEVPolyakovaVSKwanOVSkalnyAVNikonorovAA. Adipose tissue chromium and vanadium disbalance in high-fat fed Wistar rats. J Trace Elem Med Biol2015; 29: 176–81.
28.
VenuLKishoreYDRaghunathM. Maternal and perinatal magnesium restriction predisposes rat pups to insulin resistance and glucose intolerance. J Nutrition2005; 135: 1353–8.
29.
BerendsLMFernandez-TwinnDSMartin-GronertMSCrippsRLOzanneSE. Catch-up growth following intra-uterine growth-restriction programmes an insulin-resistant phenotype in adipose tissue. Int J Obes2013; 37: 1051–7.
30.
PadmavathiIJKishoreYDVenuLGaneshanMHarishankarNGiridharanNVRaghunathM. Prenatal and perinatal zinc restriction: effects on body composition, glucose tolerance and insulin response in rat offspring. Exp Physiol2009; 94: 761–9.
31.
SharmaSAgrawalRPChoudharyMJainSGoyalSAgarwalV. Beneficial effect of chromium supplementation on glucose, HbA1C and lipid variables in individuals with newly onset type-2 diabetes. J Trace Elem Med Biol2011; 25: 149–53.
32.
LeeNAReasnerCA. Beneficial effect of chromium supplementation on serum triglyceride levels in NIDDM. Diabetes Care1994; 17: 1449–52.
33.
ElwoodJCNashDTStreetenDH. Effect of high-chromium brewer's yeast on human serum lipids. J Am Coll Nutr1982; 1: 263–74.
34.
DoddigarlaZAhmadJParwezI. Effect of chromium picolinate and melatonin either in single or in a combination in high carbohydrate diet-fed male Wistar rats. Biofactors2016; 42: 106–14.
35.
BringhentiISchultzARachidTBomfimMAMandarim-de-LacerdaCAAguilaMB. An early fish oil-enriched diet reverses biochemical, liver and adipose tissue alterations in male offspring from maternal protein restriction in mice. J Nutr Biochem2011; 22: 1009–14.
36.
MohamedJSHajiraAPardoPSBoriekAM. MicroRNA-149 inhibits PARP-2 and promotes mitochondrial biogenesis via SIRT-1/PGC-1alpha network in skeletal muscle. Diabetes2014; 63: 1546–59.
37.
JacovettiCAbderrahmaniAParnaudGJonasJCPeyotMLCornuMLaybuttRMeugnierERomeSThorensBPrentkiMBoscoDRegazziR. MicroRNAs contribute to compensatory beta cell expansion during pregnancy and obesity. J Clin Invest2012; 122: 3541–51.
38.
NescaVGuayCJacovettiCMenoudVPeyotMLLaybuttDRPrentkiMRegazziR. Identification of particular groups of microRNAs that positively or negatively impact on beta cell function in obese models of type 2 diabetes. Diabetologia2013; 56: 2203–12.
39.
HulsmansMSinnaevePVan der SchuerenBMathieuCJanssensSHolvoetP. Decreased miR-181a expression in monocytes of obese patients is associated with the occurrence of metabolic syndrome and coronary artery disease. J Clin Endocrinol Metab2012; 97: E1213–8.
40.
CuadradoANebredaAR. Mechanisms and functions of p38 MAPK signalling. Biochem J2010; 429: 403–17.
41.
ShimJHXiaoCPaschalAEBaileySTRaoPHaydenMSLeeKYBusseyCSteckelMTanakaNYamadaGAkiraSMatsumotoKGhoshS. TAK1, but not TAB1 or TAB2, plays an essential role in multiple signaling pathways in vivo. Genes Dev2005; 19: 2668–81.
42.
BiesemannNMendlerLKostinSWietelmannABorchardtTBraunT. Myostatin induces interstitial fibrosis in the heart via TAK1 and p38. Cell Tissue Res2015; 361: 779–87.
43.
KinugawaKJeongMYBristowMRLongCS. Thyroid hormone induces cardiac myocyte hypertrophy in a thyroid hormone receptor alpha1-specific manner that requires TAK1 and p38 mitogen-activated protein kinase. Mol Endocrinol2005; 19: 1618–28.
44.
MaekawaTJinWIshiiS. The role of ATF-2 family transcription factors in adipocyte differentiation: antiobesity effects of p38 inhibitors. Mol Cell Biol2010; 30: 613–25.
45.
Figuera-LosadaMLoGrassoPV. Enzyme kinetics and interaction studies for human JNK1beta1 and substrates activating transcription factor 2 (ATF2) and c-Jun N-terminal kinase (c-Jun). J Biol Chem2012; 287: 13291–302.
46.
HataKNishimuraRIkedaFYamashitaKMatsubaraTNokubiTYonedaT. Differential roles of Smad1 and p38 kinase in regulation of peroxisome proliferator-activating receptor gamma during bone morphogenetic protein 2-induced adipogenesis. Mol Biol Cell2003; 14: 545–55.
47.
XieXSongJLiG. MiR-21a-5p suppresses bisphenol A-induced pre-adipocyte differentiation by targeting map2k3 through MKK3/p38/MAPK. Biochem Biophys Res Commun2016; 473: 140–6.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
