Overnutrition and maternal obesity in sheep pregnancy alter the JNK-IRS-1 signaling cascades and cardiac function in the fetal heart

FASEB Journal

Volumn 24, Issue 6, 2010, Pages 2066-2076

  Wang, Jingying ^a,b   Ma, Heng ^b   Tong, Chao ^a,b   Zhang, Hanying ^b   Lawlis, Gavin B ^b   Li, Yuanda ^b   Zang, Mengwei ^c   Ren, Jun ^b   Nijland, Mark J ^d   Ford, Stephen P ^b   Nathanielsz, Peter W ^d   Li, Ji ^a,b  

^a UNIVERSITY AT BUFFALO   (United States)

^b UNIVERSITY OF WYOMING   (United States)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF TEXAS AT SAN ANTONIO   (United States)

Author keywords

Cardiac dysfunction; Insulin resistance; Signaling transduction

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; GLUCOSE; INSULIN; INSULIN RECEPTOR SUBSTRATE 1; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPSY; CONTROLLED STUDY; FEMALE; FETUS; FETUS BLOOD; FETUS HEART; GLUCOSE BLOOD LEVEL; HEART FUNCTION; INSULIN BLOOD LEVEL; MATERNAL OBESITY; NONHUMAN; OBESITY; OVERNUTRITION; PREGNANCY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SHEEP; UPREGULATION;

ANIMALS; FEMALE; FETAL HEART; IMMUNOBLOTTING; IMMUNOPRECIPITATION; INSULIN; INSULIN RECEPTOR SUBSTRATE PROTEINS; INSULIN RESISTANCE; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE SIGNALING SYSTEM; OBESITY; OVERNUTRITION; PHENOTYPE; PHOSPHORYLATION; PREGNANCY; PROTO-ONCOGENE PROTEINS C-AKT; SHEEP; SIGNAL TRANSDUCTION;

OVIS ARIES;

EID: 77953508427     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-142315     Document Type: Article

References (60)

1. Ehrenberg, H. M., Dierker, L., Milluzzi, C., and Mercer, B. M. (2002) Prevalence of maternal obesity in an urban center. Am. J. Obstet. Gynecol. 187, 1189-1193
2. Reece, E. A. (2008) Perspectives on obesity, pregnancy and birth outcomes in the United States: the scope of the problem. Am. J. Obstet. Gynecol. 198, 23-27
3. Nohr, E. A., Vaeth, M., Bech, B. H., Henriksen, T. B., Cnattingius, S., and Olsen, J. (2007) Maternal obesity and neonatal mortality according to subtypes of preterm birth. Obstet. Gynecol. 110, 1083-1090
4. Hull, H. R., Dinger, M. K., Knehans, A. W., Thompson, D. M., and Fields, D. A. (2008) Impact of maternal body mass index on neonate birthweight and body composition. Am. J. Obstet. Gynecol. 198, 416 e411-416
5. Barker, D. J. (2002) Fetal programming of coronary heart disease. Trends Endocrinol. Metab. 13, 364-368
6. Mighty, H. E., and Fahey, A. J. (2007) Obesity and pregnancy complications. Curr. Diabetes Reports 7, 289-294
7. Woods, L. L. (2000) Fetal origins of adult hypertension: a renal mechanism? Curr. Opin. Nephrol. Hypertens. 9, 419-425
8. Hintz, K. K., Aberle, N. S., and Ren, J. (2003) Insulin resistance induces hyperleptinemia, cardiac contractile dysfunction but not cardiac leptin resistance in ventricular myocytes. Int. J. Obes. Relat. Metab. Disord. 27, 1196-1203
9. Yu, Y. R., Li, H. L., Yu, H. L., Wang, C., and Pu, S. (2003) The relationship between insulin resistance and endothelium-dependent vasodilatation in obese subjects. Zhonghua Yi Xue Za Zhi 83, 1467-1470
10. Ginsberg, H. N. (2000) Insulin resistance and cardiovascular disease. J. Clin. Invest. 106, 453-458
11. Rapp, J. H., Lespine, A., Hamilton, R. L., Colyvas, N., Chaumeton, A. H., Tweedie-Hardman, J., Kotite, L., Kunitake, S. T., Havel, R. J., and Kane, J. P. (1994) Triglyceride-rich lipoproteins isolated by selected-affinity anti-apolipoprotein B immunosorption from human atherosclerotic plaque. Arterioscler. Thromb. 14, 1767-1774 (Pubitemid 2164784)
12. Rodrigues, B., and McNeill, J. H. (1992) The diabetic heart: metabolic causes for the development of a cardiomyopathy. Cardiovasc. Res. 26, 913-922
13. Kenchaiah, S., Evans, J. C., Levy, D., Wilson, P. W., Benjamin, E. J., Larson, M. G., Kannel, W. B., and Vasan, R. S. (2002) Obesity and the risk of heart failure. N. Engl. J. Med. 347, 305-313
14. Trovato, G. M., Catalano, D., Caruso, G., Squatrito, R., Venturino, M., Degano, C., and Fazzio, S. D. (2001) Relationship between cardiac function and insulin resistance in obese patients. Diabetes Nutr. Metab. 14, 325-328 (Pubitemid 34071380)
15. Peterson, L. R. (2006) Obesity and insulin resistance: effects on cardiac structure, function, and substrate metabolism. Curr. Hypertens. Rep. 8, 451-456
16. Bennett, B. L., Satoh, Y., and Lewis, A. J. (2003) JNK: a new therapeutic target for diabetes. Curr. Opin. Pharm. 3, 420-425
17. Hirosumi, J., Tuncman, G., Chang, L., Gorgun, C. Z., Uysal, K. T., Maeda, K., Karin, M., and Hotamisligil, G. S. (2002) A central role for JNK in obesity and insulin resistance. Nature 420, 333-336
18. Aguirre, V., Uchida, T., Yenush, L., Davis, R., and White, M. F. (2000) The c-Jun NH(2)-terminal kinase promotes insulin resistance during association with insulin receptor substrate-1 and phosphorylation of Ser(307). J. Biol. Chem. 275, 9047-9054
19. Kaneto, H., Matsuoka, T. A., Nakatani, Y., Kawamori, D., Miyatsuka, T., Matsuhisa, M., and Yamasaki, Y. (2005) Oxidative stress, ER stress, and the JNK pathway in type 2 diabetes. J. Mol. Med. 83, 429-439 (Pubitemid 40922165)
20. Kaneto, H., Xu, G., Fujii, N., Kim, S., Bonner-Weir, S., and Weir, G. C. (2002) Involvement of c-Jun N-terminal kinase in oxidative stress-mediated suppression of insulin gene expression. J. Biol. Chem. 277, 30010-30018
21. Skalicky, J., Muzakova, V., Kandar, R., Meloun, M., Rousar, T., and Palicka, V. (2008) Evaluation of oxidative stress and inflammation in obese adults with metabolic syndrome. Clin. Chem. Lab. Med. 46, 499-505
22. Zhu, M. J., Han, B., Tong, J., Ma, C., Kimzey, J. M., Underwood, K. R., Xiao, Y., Hess, B. W., Ford, S. P., Nathanielsz, P. W., and Du, M. (2008) AMP-activated protein kinase signalling pathways are down regulated and skeletal muscle development impaired in fetuses of obese, over-nourished sheep. J. Physiol. 586, 2651-2664
23. Sanson, D. W., West, T. R., Tatman, W. R., Riley, M. L., Judkins, M. B., and Moss, G. E. (1993) Relationship of body composition of mature ewes with condition score and body weight. J. Anim. Sci. 71, 1112-1116
24. Ford, S. P., Zhang, L., Zhu, M., Miller, M. M., Smith, D. T., Hess, B. W., Moss, G. E., Nathanielsz, P. W., and Nijland, M. J. (2009) Maternal obesity accelerates fetal pancreatic β cell but not α cell development in the sheep: prenatal and postnatal consequences. Am. J. Physiol. 297, 835-843
25. Miller, E. J., Li, J., Leng, L., McDonald, C., Atsumi, T., Bucala, R., and Young, L. H. (2008) Macrophage migration inhibitory factor stimulates AMP-activated protein kinase in the ischaemic heart. Nature 451, 578-582
26. Zhao, P., Wang, J., Ma, H., Xiao, Y., He, L., Tong, C., Wang, Z., Zheng, Q., Dolence, E. K., Nair, S., Ren, J., and Li, J. (2009) A newly synthetic chromium complex-chromium (d-phenylalanine) (3) activates AMP-activated protein kinase and stimulates glucose transport. Biochem. Pharm. 77, 1002-1010
27. Li, J., Miller, E. J., Ninomiya-Tsuji, J., Russell, R. R., 3rd, and Young, L. H. (2005) AMP-activated protein kinase activates p38 mitogen-activated protein kinase by increasing recruitment of p38 MAPK to TAB1 in the ischemic heart. Circ. Res. 97, 872-879
28. Hiromura, M., Okada, F., Obata, T., Auguin, D., Shibata, T., Roumestand, C., and Noguchi, M. (2004) Inhibition of Akt kinase activity by a peptide spanning the betaA strand of the proto-oncogene TCL1. J. Biol. Chem. 279, 53407-53418
29. Furukawa, S., Fujita, T., Shimabukuro, M., Iwaki, M., Yamada, Y., Nakajima, Y., Nakayama, O., Makishima, M., Matsuda, M., and Shimomura, I. (2004) Increased oxidative stress in obesity and its impact on metabolic syndrome. J. Clin. Invest. 114, 1752-1761
30. Li, J., and Holbrook, N. J. (2003) Common mechanisms for declines in oxidative stress tolerance and proliferation with aging. Free Radic. Biol. Med. 35, 292-299
31. Shiojima, I., Yefremashvili, M., Luo, Z., Kureishi, Y., Takahashi, A., Tao, J., Rosenzweig, A., Kahn, C. R., Abel, E. D., and Walsh, K. (2002) Akt signaling mediates postnatal heart growth in response to insulin and nutritional status. J. Biol. Chem. 277, 37670-37677
32. Dyck, J. R., Kudo, N., Barr, A. J., Davies, S. P., Hardie, D. G., and Lopaschuk, G. D. (1999) Phosphorylation control of cardiac acetyl-CoA carboxylase by cAMP-dependent protein kinase and 5′-AMP activated protein kinase. Eur. J. Biochem. 262, 184-190
33. Li, J., Hu, X., Selvakumar, P., Russell, R. R., 3rd, Cushman, S. W., Holman, G. D., and Young, L. H. (2004) Role of the nitric oxide pathway in AMPK-mediated glucose uptake and GLUT4 translocation in heart muscle. Am. J. Physiol. Endocrinol. Metab. 287, E834-E841
34. Cong, L. N., Chen, H., Li, Y., Zhou, L., McGibbon, M. A., Taylor, S. I., and Quon, M. J. (1997) Physiological role of Akt in insulin-stimulated translocation of GLUT4 in transfected rat adipose cells. Mol. Endocrin. 11, 1881-1890 (Pubitemid 27524872)
35. Lopaschuk, G. D., Spafford, M. A., and Marsh, D. R. (1991) Glycolysis is predominant source of myocardial ATP production immediately after birth. Am. J. Physiol. Heart Circ. Physiol. 261, H1698-H1705
36. Opie, L. H. (1968) Metabolism of the heart in health and disease. I. Am. Heart J. 76, 685-698
37. Stanley, W. C., Recchia, F. A., and Lopaschuk, G. D. (2005) Myocardial substrate metabolism in the normal and failing heart. Physiol. Rev. 85, 1093-1129
38. Okamoto, F., Tanaka, T., Sohmiya, K., and Kawamura, K. (1998) CD36 abnormality and impaired myocardial long-chain fatty acid uptake in patients with hypertrophic cardiomyopathy. Jpn. Circ. J. 62, 499-504 (Pubitemid 128543304)
39. Watanabe, K., Toba, K., Ogawa, Y., Kodama, M., Hirono, S., Ohkura, Y., Hanawa, H., Nakamura, Y., Aoki, Y., Fuse, I., Aizawa, Y., Miyajima, S., Kusano, Y., Nagatomo, T., Hasegawa, G., and Naito, M. (1998) Hypertrophic cardiomyopathy with type I CD36 deficiency. Jpn. Circ. J. 62, 541-542
40. Tong, J., Zhu, M. J., Underwood, K. R., Hess, B. W., Ford, S. P., and Du, M. (2008) AMP-activated protein kinase and adipogenesis in sheep fetal skeletal muscle and 3T3-L1 cells. J. Animal. Sci. 86, 1296-1305
41. Taylor, P. D., and Poston, L. (2007) Developmental programming of obesity in mammals. Exp. Physiol. 92, 287-298
42. Virkamaki, A., Ueki, K., and Kahn, C. R. (1999) Protein-protein interaction in insulin signaling and the molecular mechanisms of insulin resistance. J. Clin. Invest. 103, 931-943 (Pubitemid 29169600)
43. Steinberg, G. R. (2007) Inflammation in obesity is the common link between defects in fatty acid metabolism and insulin resistance. Cell Cycle 6, 888-894
44. Schmatz, M., Madan, J., Marino, T., and Davis, J. (2009) Maternal obesity: the interplay between inflammation, mother and fetus. [E-pub ahead of print] J. Perinatol. doi: 10.1038/jp.2009.182
45. Young, L. H., Li, J., Baron, S. J., and Russell, R. R. (2005) AMP-activated protein kinase: a key stress signaling pathway in the heart. Trends Cardiovasc. Med. 15, 110-118
46. Ma, H., Li, J., Gao, F., and Ren, J. (2009) Aldehyde dehydrogenase 2 ameliorates acute cardiac toxicity of ethanol role of protein phosphatase and forkhead transcription factor. J. Am. Coll. Cardiol. 54, 2187-2196
47. Steinberg, G. R., Michell, B. J., van Denderen, B. J., Watt, M. J., Carey, A. L., Fam, B. C., Andrikopoulos, S., Proietto, J., Gorgun, C. Z., Carling, D., Hotamisligil, G. S., Febbraio, M. A., Kay, T. W., and Kemp, B. E. (2006) Tumor necrosis factor alpha-induced skeletal muscle insulin resistance involves suppression of AMP-kinase signaling. Cell Metab. 4, 465-474
48. Wang, M. Y., and Unger, R. H. (2005) Role of PP2C in cardiac lipid accumulation in obese rodents and its prevention by troglitazone. Am. J. Physiol. Endocrinol. Metab. 288, E216-E221
49. Peterson, L. R., Herrero, P., Schechtman, K. B., Racette, S. B., Waggoner, A. D., Kisrieva-Ware, Z., Dence, C., Klein, S., Marsala, J., Meyer, T., and Gropler, R. J. (2004) Effect of obesity and insulin resistance on myocardial substrate metabolism and efficiency in young women. Circulation 109, 2191-2196
50. Srinivasan, M., Aalinkeel, R., Song, F., Mitrani, P., Pandya, J. D., Strutt, B., Hill, D. J., and Patel, M. S. (2006) Maternal hyperinsulinemia predisposes rat fetuses for hyperinsulinemia, and adult-onset obesity and maternal mild food restriction reverses this phenotype. Am. J. Physiol. Endocrinol. Metab. 290, E129-E134
51. Sobngwi, E., Boudou, P., Mauvais-Jarvis, F., Leblanc, H., Velho, G., Vexiau, P., Porcher, R., Hadjadj, S., Pratley, R., Tataranni, P. A., Calvo, F., and Gautier, J. F. (2003) Effect of a diabetic environment in utero on predisposition to type 2 diabetes. Lancet 361, 1861-1865
52. Whitaker, R. C., Wright, J. A., Pepe, M. S., Seidel, K. D., and Dietz, W. H. (1997) Predicting obesity in young adulthood from childhood and parental obesity. N. Engl. J. Med. 337, 869-873
53. Calvert, J. W., Lefer, D. J., Gundewar, S., Poston, L., and Coetzee, W. A. (2009) Developmental programming resulting from maternal obesity in mice: effects on myocardial ischaemia-reperfusion injury. Exp. Physiol. 94, 805-814
54. Corrigan, N., Brazil, D. P., and McAuliffe, F. (2009) Fetal cardiac effects of maternal hyperglycemia during pregnancy. Birth Defects Res. A. Clin. Mol. Teratol. 85, 523-530
55. Napoli, C., D'Armiento, F. P., Mancini, F. P., Postiglione, A., Witztum, J. L., Palumbo, G., and Palinski, W. (1997) Fatty streak formation occurs in human fetal aortas and is greatly enhanced by maternal hypercholesterolemia. Intimal accumulation of low density lipoprotein and its oxidation precede monocyte recruitment into early atherosclerotic lesions. J. Clin. Invest. 100, 2680-2690
56. Palinski, W., Nicolaides, E., Liguori, A., and Napoli, C. (2009) Influence of maternal dysmetabolic conditions during pregnancy on cardiovascular disease. J. Cardiovasc. Transl. Res. 2, 277-285
57. Napoli, C., Glass, C. K., Witztum, J. L., Deutsch, R., D'Armiento, F. P., and Palinski, W. (1999) Influence of maternal hypercholesterolaemia during pregnancy on progression of early atherosclerotic lesions in childhood: fate of early lesions in children (FELIC) study. Lancet 354, 1234-1241
58. Kristensen, J., Vestergaard, M., Wisborg, K., Kesmodel, U., and Secher, N. J. (2005) Pre-pregnancy weight and the risk of stillbirth and neonatal death. BJOG 112, 403-408
59. Chen, A., Feresu, S. A., Fernandez, C., and Rogan, W. J. (2009) Maternal obesity and the risk of infant death in the United States. Epidemiology 20, 74-81
60. Cnattingius, S., Bergstrom, R., Lipworth, L., and Kramer, M. S. (1998) Prepregnancy weight and the risk of adverse pregnancy outcomes. N. Engl. J. Med. 338, 147-152