Maternal chromium restriction leads to glucose metabolism imbalance in mice offspring through insulin signaling and wnt signaling pathways

International Journal of Molecular Sciences

Volumn 17, Issue 10, 2016, Pages

  Zhang, Qian ^a   Sun, Xiaofang ^b   Xiao, Xinhua ^a   Zheng, Jia ^a   Li, Ming ^a   Yu, Miao ^a   Ping, Fan ^a   Wang, Zhixin ^a   Qi, Cuijuan ^a   Wang, Tong ^a   Wang, Xiaojing ^a  

^a PEKING UNION MEDICAL COLLEGE HOSPITAL   (China)

^b QINGDAO UNIVERSITY   (China)

Author keywords

Development programming; Gene expression; Glucose metabolism; Insulin signaling pathway; Wnt pathway

Indexed keywords

CHROMIUM; GLUCOSE; INSULIN; WNT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AREA UNDER THE CURVE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; FEMALE; FOOD INTAKE; GENE EXPRESSION; GENE ONTOLOGY; GENE REGULATORY NETWORK; GLUCOSE METABOLISM; HYPERGLYCEMIA; HYPERINSULINEMIA; INSULIN RESISTANCE; LACTATION; MALE; MATERNAL NUTRITION; MOUSE; NONHUMAN; OBESITY; ORAL GLUCOSE TOLERANCE TEST; PREGNANCY; PROGENY; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING; WNT SIGNALING PATHWAY; ADVERSE EFFECTS; ANIMAL; C57BL MOUSE; DEFICIENCY; DIET; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HYPERINSULINISM; LIVER; MATERNAL EXPOSURE; METABOLISM; PATHOLOGY; PRENATAL EXPOSURE;

ANIMALS; CHROMIUM; DIET; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLUCOSE; HYPERGLYCEMIA; HYPERINSULINISM; INSULIN; INSULIN RESISTANCE; LIVER; MALE; MATERNAL EXPOSURE; MICE; MICE, INBRED C57BL; OBESITY; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; REAL-TIME POLYMERASE CHAIN REACTION; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 84992507453     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms17101767     Document Type: Article

References (46)

1. Whincup, P.H.; Kaye, S.J.; Owen, C.G.; Huxley, R.; Cook, D.G.; Anazawa, S.; Barrett-Connor, E.; Bhargava, S.K.; Birgisdottir, B.E.; Carlsson, S.; et al. Birth weight and risk of type 2 diabetes: A systematic review. JAMA 2008, 300, 2886–2897.
2. Vaag, A.A.; Grunnet, L.G.; Arora, G.P.; Brons, C. The thrifty phenotype hypothesis revisited. Diabetologia 2012, 55, 2085–2088.
3. Hales, C.N.; Barker, D.J.; Clark, P.M.; Cox, L.J.; Fall, C.; Osmond, C.; Winter, P.D. Fetal and infant growth and impaired glucose tolerance at age 64. BMJ 1991, 303, 1019–1022.
4. Molendi-Coste, O.; Laborie, C.; Scarpa, M.C.; Montel, V.; Vieau, D.; Breton, C. Maternal perinatal undernutrition alters postnatal development of chromaffin cells in the male rat adrenal medulla. Neuroendocrinology 2009, 90, 54–66.
5. Kimani-Murage, E.W.; Kahn, K.; Pettifor, J.M.; Tollman, S.M.; Dunger, D.B.; Gomez-Olive, X.F.; Norris, S.A. The prevalence of stunting, overweight and obesity, and metabolic disease risk in rural south african children. BMC Public Health 2010, 10, 158.
6. Sawaya, A.L.; Roberts, S. Stunting and future risk of obesity: Principal physiological mechanisms. Cadernos de Saúde Pública 2003, 19, S21–S28.
7. Lesage, J.; Sebaai, N.; Leonhardt, M.; Dutriez-Casteloot, I.; Breton, C.; Deloof, S.; Vieau, D. Perinatal maternal undernutrition programs the offspring hypothalamo-pituitary-adrenal (HPA) axis. Stress 2006, 9, 183–198.
8. Moura, A.S.; Carpinelli, A.R.; Barbosa, F.B.; Gravena, C.; Mathias, P.C. Undernutrition during early lactation as an alternative model to study the onset of diabetes mellitus type II. Res. Commun. Mol. Pathol. Pharmacol. 1996, 92, 73–84.
9. De Oliveira, J.C.; Scomparin, D.X.; Andreazzi, A.E.; Branco, R.C.; Martins, A.G.; Gravena, C.; Grassiolli, S.; Rinaldi, W.; Barbosa, F.B.; Mathias, P.C. Metabolic imprinting by maternal protein malnourishment impairs vagal activity in adult rats. J. Neuroendocrinol. 2011, 23, 148–157.
10. Candilish, D.J. Minerals. J. Am. Coll. Nutr. 2000, 17, 286–310.
11. Feng, W.; Mao, G.; Li, Q.; Wang, W.; Chen, Y.; Zhao, T.; Li, F.; Zou, Y.; Wu, H.; Yang, L. et al. 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 Investig. 2015, 6, 396–407.
12. Rhodes, N.R.; McAdory, D.; Love, S.; Di Bona, K.R.; Chen, Y.; Ansorge, K.; Hira, J.; Kern, N.; Kent, J.; Lara, P. et al. Urinary chromium loss associated with diabetes is offset by increases in absorption. J. Inorg. Biochem. 2010, 104, 790–797.
13. Morris, B.W.; Kemp, G.J.; Hardisty, C.A. Plasma chromium and chromium excretion in diabetes. Clin. Chem. 1985, 31, 334–335.
14. Morris, B.W.; MacNeil, S.; Hardisty, C.A.; Heller, S.; Burgin, C.; Gray, T.A. Chromium homeostasis in patients with type II (NIDDM) diabetes. J. Trace Elem. Med. Biol. 1999, 13, 57–61.
15. Rajendran, K.; Manikandan, S.; Nair, L.D.; Karuthodiyil, R.; Vijayarajan, N.; Gnanasekar, R.; Kapil, V.V.; Mohamed, A.S. Serum chromium levels in type 2 diabetic patients and its association with glycaemic control. J. Clin. Diagn. Res. 2015, 9, OC05–OC08.
16. Padmavathi, I.J.; Rao, K.R.; Raghunath, M. Impact of maternal chromium restriction on glucose tolerance, plasma insulin and oxidative stress in wnin rat offspring. J. Mol. Endocrinol. 2011, 47, 261–271.
17. Krol, E.; Krejpcio, Z. Chromium(III) propionate complex supplementation improves carbohydrate metabolism in insulin-resistance rat model. Food Chem. Toxicol. 2010, 48, 2791–2796.
18. Hao, C.; Hao, J.; Wang, W.; Han, Z.; Li, G.; Zhang, L.; Zhao, X.; Yu, G. Insulin sensitizing effects of oligomannuronate-chromium (III) complexes in C2C12 skeletal muscle cells. PLoS ONE 2011, 6, e24598.
19. Feng, W.; Zhao, T.; Mao, G.; Wang, W.; Feng, Y.; Li, F.; Zheng, D.; Wu, H.; Jin, D.; Yang, L. et al. Type 2 diabetic rats on diet supplemented with chromium malate show improved glycometabolism, glycometabolism-related enzyme levels and lipid metabolism. PLoS ONE 2015, 10, e0125952.
20. Racek, J.; Sindberg, C.D.; Moesgaard, S.; Mainz, J.; Fabry, J.; Muller, L.; Racova, K. Effect of chromium-enriched yeast on fasting plasma glucose, glycated haemoglobin and serum lipid levels in patients with type 2 diabetes mellitus treated with insulin. Biol. Trace Elem. Res. 2013, 155, 1–4.
21. Onakpoya, I.; Posadzki, P.; Ernst, E. Chromium supplementation in overweight and obesity: A systematic review and meta-analysis of randomized clinical trials. Obes. Rev. 2013, 14, 496–507.
22. 12 restrictions alter body composition (adiposity) and lipid metabolism in wistar rat offspring. J. Nutr. Biochem. 2013, 24, 25–31.
23. Vo, T.X.; Revesz, A.; Sohi, G.; Ma, N.; Hardy, D.B. Maternal protein restriction leads to enhanced hepatic gluconeogenic gene expression in adult male rat offspring due to impaired expression of the liver X receptor. J. Endocrinol. 2013, 218, 85–97.
24. Venu, L.; Kishore, Y.D.; Raghunath, M. Maternal and perinatal magnesium restriction predisposes rat pups to insulin resistance and glucose intolerance. J. Nutr. 2005, 135, 1353–1358.
25. Taniguchi, C.M.; Emanuelli, B.; Kahn, C.R. Critical nodes in signalling pathways: Insights into insulin action. Nat. Rev. Mol. Cell Biol. 2006, 7, 85–96.
26. Ye, J.; Zheng, R.; Wang, Q.; Liao, L.; Ying, Y.; Lu, H.; Cianflone, K.; Ning, Q.; Luo, X. Downregulating SOCS3 with sirna ameliorates insulin signaling and glucose metabolism in hepatocytes of iugr rats with catch-up growth. Pediatr. Res. 2012, 72, 550–559.
27. Wang, Z.Q.; Zhang, X.H.; Russell, J.C.; Hulver, M.; Cefalu, W.T. Chromium picolinate enhances skeletal muscle cellular insulin signaling in vivo in obese, insulin-resistant JCR:LA-cp rats. J. Nutr. 2006, 136, 415–420.
28. 3. J. Inorg. Biochem. 2006, 100, 1187–1193.
29. Zhang, Q.; Xiao, X.H.; Li, M.; Li, W.H.; Yu, M.; Zhang, H.B.; Ping, F.; Wang, Z.X.; Zheng, J. Chromium-containing traditional Chinese medicine, Tianmai Xiaoke tablet improves blood glucose through activating insulin-signaling pathway and inhibiting PTP1B and PCK2 in diabetic rats. J. Integr. Med. 2014, 12, 162–170.
30. Krebs, M.; Roden, M. Molecular mechanisms of lipid-induced insulin resistance in muscle, liver and vasculature. Diabetes Obes. Metab. 2005, 7, 621–632.
31. Bringhenti, I.; Ornellas, F.; Mandarim-de-Lacerda, C.A.; Aguila, M.B. The insulin-signaling pathway of the pancreatic islet is impaired in adult mice offspring of mothers fed a high-fat diet. Nutrition 2016, 32, 1138–1143.
32. Maia-Ceciliano, T.C.; Barreto-Vianna, A.R.; Barbosa-da-Silva, S.; Aguila, M.B.; Faria, T.S.; Mandarim-de-Lacerda, C.A. Maternal vitamin D-restricted diet has consequences in the formation of pancreatic islet/insulin-signaling in the adult offspring of mice. Endocrine 2016.
33. Krebs, D.L.; Hilton, D.J. SOCS: Physiological suppressors of cytokine signaling. J. Cell Sci. 2000, 113, 2813–2819.
34. Emanuelli, B.; Peraldi, P.; Filloux, C.; Chavey, C.; Freidinger, K.; Hilton, D.J.; Hotamisligil, G.S.; van Obberghen, E. SOCS-3 inhibits insulin signaling and is up-regulated in response to tumor necrosis factor-alpha in the adipose tissue of obese mice. J. Biol. Chem. 2001, 276, 47944–47949.
35. Ueki, K.; Kondo, T.; Kahn, C.R. Suppressor of cytokine signaling 1 (SOCS-1) and SOCS-3 cause insulin resistance through inhibition of tyrosine phosphorylation of insulin receptor substrate proteins by discrete mechanisms. Mol. Cell. Biol. 2004, 24, 5434–5446.
36. Lebrun, P.; van Obberghen, E. SOCS proteins causing trouble in insulin action. Acta Physiol. 2008, 192, 29–36.
37. Clevers, H. Wnt/β-catenin signaling in development and disease. Cell 2006, 127, 469–480.
38. Kanazawa, A.; Tsukada, S.; Sekine, A.; Tsunoda, T.; Takahashi, A.; Kashiwagi, A.; Tanaka, Y.; Babazono, T.; Matsuda, M.; Kaku, K. et al. Association of the gene encoding wingless-type mammary tumor virus integration-site family member 5B (WNT5B) with type 2 diabetes. Am. J. Hum. Genet. 2004, 75, 832–843.
39. Neve, B.; Le Bacquer, O.; Caron, S.; Huyvaert, M.; Leloire, A.; Poulain-Godefroy, O.; Lecoeur, C.; Pattou, F.; Staels, B.; Froguel, P. Alternative human liver transcripts of TCF7L2 bind to the gluconeogenesis regulator HNF4α at the protein level. Diabetologia 2014, 57, 785–796.
40. Abiola, M.; Favier, M.; Christodoulou-Vafeiadou, E.; Pichard, A.L.; Martelly, I.; Guillet-Deniau, I. Activation of wnt/beta-catenin signaling increases insulin sensitivity through a reciprocal regulation of wnt10b and srebp-1c in skeletal muscle cells. PLoS ONE 2009, 4, e8509.
41. Liu, H.; Fergusson, M.M.; Wu, J.J.; Rovira, I.I.; Liu, J.; Gavrilova, O.; Lu, T.; Bao, J.; Han, D.; Sack, M.N. et al. Wnt signaling regulates hepatic metabolism. Sci. Signal. 2011.
42. Yokomizo, H.; Inoguchi, T.; Sonoda, N.; Sakaki, Y.; Maeda, Y.; Inoue, T.; Hirata, E.; Takei, R.; Ikeda, N.; Fujii, M. et al. Maternal high-fat diet induces insulin resistance and deterioration of pancreatic β-cell function in adult offspring with sex differences in mice. Am. J. Physiol. Endocrinol. Metab. 2014, 306, E1163–E1175.
43. Dennis, G., Jr.; Sherman, B.T.; Hosack, D.A.; Yang, J.; Gao, W.; Lane, H.C.; Lempicki, R.A. David: Database for annotation, visualization, and integrated discovery. Genome Biol. 2003.
44. Ashburner, M.; Ball, C.A.; Blake, J.A.; Botstein, D.; Butler, H.; Cherry, J.M.; Davis, A.P.; Dolinski, K.; Dwight, S.S.; Eppig, J.T. et al. Gene ontology: Tool for the unification of biology. The gene ontology consortium. Nat. Genet. 2000, 25, 25–29.
45. Kanehisa, M.; Araki, M.; Goto, S.; Hattori, M.; Hirakawa, M.; Itoh, M.; Katayama, T.; Kawashima, S.; Okuda, S.; Tokimatsu, T. et al. Kegg for linking genomes to life and the environment. Nucleic Acids Res. 2008, 36, D480–D484.
46. Szklarczyk, D.; Franceschini, A.; Wyder, S.; Forslund, K.; Heller, D.; Huerta-Cepas, J.; Simonovic, M.; Roth, A.; Santos, A.; Tsafou, K.P. et al. STRING v10: Protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res. 2015, 43, D447–D452.