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BioMed Research International
Volume 2014, Article ID 917672, 13 pages
http://dx.doi.org/10.1155/2014/917672
Review Article

Programming of Fetal Insulin Resistance in Pregnancies with Maternal Obesity by ER Stress and Inflammation

1Cellular and Molecular Physiology Laboratory (CMPL), Division of Obstetrics and Gynecology, School of Medicine, Faculty of Medicine, Pontificia Universidad Católica de Chile, P.O. Box 114-D, 8330024 Santiago, Chile
2Facultad de Ciencia, Universidad San Sebastián, 7510157 Santiago, Chile
3Advanced Center for Chronic Diseases (ACCDiS), Faculty of Chemical & Pharmaceutical Sciences & Faculty of Medicine, University of Chile, 8380492 Santiago, Chile
4Facultad de Ciencias de la Salud, Universidad San Sebastián, 7510157 Santiago, Chile
5University of Queensland Centre for Clinical Research (UQCCR), Faculty of Medicine and Biomedical Sciences, University of Queensland, Herston, 4006 QLD, Australia

Received 13 April 2014; Accepted 4 June 2014; Published 30 June 2014

Academic Editor: Leslie Myatt

Copyright © 2014 Francisco Westermeier et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. WHO, “Diet, nutrition and the prevention of chronic diseases,” WHO Technical Report 916, World Health Organization, Geneva, Switzerland, 2003. View at Google Scholar
  2. WHO, WHO Global Database on Body Mass Index, World Health Organization, 2011.
  3. S. Triunfo and A. Lanzone, “Impact of overweight and obesity on obstetric outcomes,” Journal of Endocrinological Investigation, 2014. View at Google Scholar
  4. ACOG, “ACOG Committee Opinion number 315, September 2005. Obesity in pregnancy,” Obstetrics and Gynecology, vol. 106, no. 3, pp. 671–675, 2005. View at Google Scholar
  5. V. Flenady, L. Koopmans, P. Middleton et al., “Major risk factors for stillbirth in high-income countries: a systematic review and meta-analysis,” The Lancet, vol. 377, no. 9774, pp. 1331–1340, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. P. D. Taylor, A. M. Samuelsson, and L. Poston, “Maternal obesity and the developmental programming of hypertension: a role for leptin,” Acta Physiologica, vol. 2010, no. 3, pp. 508–523, 2014. View at Google Scholar
  7. M. Dong, Q. Zheng, S. P. Ford, P. W. Nathanielsz, and J. Ren, “Maternal obesity, lipotoxicity and cardiovascular diseases in offspring,” Journal of Molecular and Cellular Cardiology, vol. 55, no. 1, pp. 111–116, 2013. View at Publisher · View at Google Scholar · View at Scopus
  8. T. Deng, C. J. Lyon, L. J. Minze et al., “Class II major histocompatibility complex plays an essential role in obesity-induced adipose inflammation,” Cell Metabolism, vol. 17, no. 3, pp. 411–422, 2013. View at Publisher · View at Google Scholar · View at Scopus
  9. M. S. Han, D. Y. Jung, C. Morel et al., “JNK expression by macrophages promotes obesity-induced insulin resistance and inflammation,” Science, vol. 339, no. 6116, pp. 218–222, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Matsuda and I. Shimomura, “Increased oxidative stress in obesity: implications for metabolic syndrome, diabetes, hypertension, dyslipidemia, atherosclerosis, and cancer,” Obesity Research and Clinical Practice, vol. 7, no. 5, pp. e330–e341, 2013. View at Publisher · View at Google Scholar · View at Scopus
  11. W. P. Cawthorn and J. K. Sethi, “TNF-α and adipocyte biology,” FEBS Letters, vol. 582, no. 1, pp. 117–131, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. N. Ouchi, J. L. Parker, J. J. Lugus, and K. Walsh, “Adipokines in inflammation and metabolic disease,” Nature Reviews Immunology, vol. 11, no. 2, pp. 85–97, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. H. Cao, “Adipocytokines in obesity and metabolic disease,” Journal of Endocrinology, vol. 220, no. 2, pp. 47–59, 2014. View at Publisher · View at Google Scholar
  14. M. Flamment, E. Hajduch, P. Ferré, and F. Foufelle, “New insights into ER stress-induced insulin resistance,” Trends in Endocrinology and Metabolism, vol. 23, no. 8, pp. 381–390, 2012. View at Publisher · View at Google Scholar · View at Scopus
  15. U. Özcan, Q. Cao, E. Yilmaz et al., “Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes,” Science, vol. 306, no. 5695, pp. 457–461, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. P. A. Hansen, A. Waheed, and J. A. Corbett, “Chemically chaperoning the actions of insulin,” Trends in Endocrinology and Metabolism, vol. 18, no. 1, pp. 1–3, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. D. L. Eizirik, A. K. Cardozo, and M. Cnop, “The role for endoplasmic reticulum stress in diabetes mellitus,” Endocrine Reviews, vol. 29, no. 1, pp. 42–61, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. S. Schenk, M. Saberi, and J. M. Olefsky, “Insulin sensitivity: Modulation by nutrients and inflammation,” Journal of Clinical Investigation, vol. 118, no. 9, pp. 2992–3002, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Zeyda and T. M. Stulnig, “Obesity, inflammation, and insulin resistance—a mini-review,” Gerontology, vol. 55, no. 4, pp. 379–386, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. G. S. Hotamisligil, “Endoplasmic Reticulum Stress and the Inflammatory Basis of Metabolic Disease,” Cell, vol. 140, no. 6, pp. 900–917, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. A. Yalcin and G. S. Hotamisligil, “Impact of ER protein homeostasis on metabolism,” Diabetes, vol. 62, no. 3, pp. 691–693, 2013. View at Publisher · View at Google Scholar · View at Scopus
  22. J. Lee and U. Ozcan, “Unfolded protein response signaling and metabolic diseases,” The Journal of Biological Chemistry, vol. 289, no. 3, pp. 1203–1211, 2014. View at Google Scholar
  23. K. Tenenbaum-Gavish and M. Hod, “Impact of maternal obesity on fetal health,” Fetal Diagnosis and Therapy, vol. 34, no. 1, pp. 1–7, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. IOM, Institute of Medicine, and National Academy of Sciences, Nutrition during Pregnancy, National Academy Press, Washington, Wash, USA, 1990.
  25. E. Papachatzi, G. Dimitriou, K. Dimitropoulos, and A. Vantarakis, “Pre-pregnancy obesity: maternal, neonatal and childhood outcomes,” Journal of Neonatal- Perinatal Medicine, vol. 6, no. 3, pp. 203–216, 2013. View at Google Scholar
  26. P. M. Catalano, “Obesity and pregnancy—the propagation of a viscous cycle?” The Journal of Clinical Endocrinology & Metabolism, vol. 88, no. 8, pp. 3505–3506, 2003. View at Publisher · View at Google Scholar · View at Scopus
  27. P. M. Catalano, L. Mele, M. B. Landon et al., “Inadequate weight gain in overweight and obese pregnant women: what is the effect on fetal growth?” American Journal of Obstetrics and Gynecology, 2014. View at Publisher · View at Google Scholar
  28. G. C. Curhan, W. C. Willett, E. B. Rimm, D. Spiegelman, A. L. Ascherio, and M. J. Stampfer, “Birth weight and adult hypertension, diabetes mellitus, and obesity in US men,” Circulation, vol. 94, no. 12, pp. 3246–3250, 1996. View at Publisher · View at Google Scholar · View at Scopus
  29. E. Öken, S. L. Rifas-Shiman, A. E. Field, A. L. Frazier, and M. W. Gillman, “Maternal gestational weight gain and offspring weight in adolescence,” Obstetrics and Gynecology, vol. 112, no. 5, pp. 999–1006, 2008. View at Publisher · View at Google Scholar
  30. M. Birbilis, G. Moschonis, V. Mougios, and Y. Manios, “Obesity in adolescence is associated with perinatal risk factors, parental BMI and sociodemographic characteristics,” European Journal of Clinical Nutrition, vol. 67, no. 1, pp. 115–121, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. E. Oken, E. M. Taveras, K. P. Kleinman, J. W. Rich-Edwards, and M. W. Gillman, “Gestational weight gain and child adiposity at age 3 years,” The American Journal of Obstetrics and Gynecology, vol. 196, no. 4, pp. 322.e1–322.e8, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. B. H. Wrotniak, J. Shults, S. Butts, and N. Stettler, “Gestational weight gain and risk of overweight in the offspring at age 7 y in a multicenter, multiethnic cohort study,” The American Journal of Clinical Nutrition, vol. 87, no. 6, pp. 1818–1824, 2008. View at Google Scholar · View at Scopus
  33. A. Fraser, K. Tilling, C. MacDonald-Wallis et al., “Association of maternal weight gain in pregnancy with offspring obesity and metabolic and vascular traits in childhood,” Circulation, vol. 121, no. 23, pp. 2557–2564, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. A. A. Mamun, M. O'Callaghan, L. Callaway, G. Williams, J. Najman, and D. A. Lawlor, “Associations of gestational weight gain with offspring body mass index and blood pressure at 21 years of ageevidence from a birth cohort study,” Circulation, vol. 119, no. 13, pp. 1720–1727, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. B. M. Margetts, M. G. M. Rowland, F. A. Foord, A. M. Cruddas, T. J. Cole, and D. J. P. Barker, “The relation of maternal weight to the blood pressures of Gambian children,” International Journal of Epidemiology, vol. 20, no. 4, pp. 938–943, 1991. View at Publisher · View at Google Scholar · View at Scopus
  36. A. Laor, D. K. Stevenson, J. Shemer, R. Gale, and D. S. Seidman, “Size at birth, maternal nutritional status in pregnancy, and blood pressure at age 17: population based analysis,” British Medical Journal, vol. 315, no. 7106, pp. 449–453, 1997. View at Publisher · View at Google Scholar · View at Scopus
  37. R. Gaillard, E. A. Steegers, L. Duijts et al., “Childhood cardiometabolic outcomes of maternal obesity during pregnancy: The Generation R Study,” Hypertension, vol. 63, no. 4, pp. 683–691, 2014. View at Publisher · View at Google Scholar
  38. A. M. Stuebe, M. B. Landon, Y. Lai et al., “Maternal BMI, glucose tolerance, and adverse pregnancy outcomes,” American Journal of Obstetrics & Gynecology, vol. 207, no. 1, pp. 62.e1–62.e7, 2012. View at Publisher · View at Google Scholar · View at Scopus
  39. M. F. Sewell, L. Huston-Presley, D. M. Super, and P. Catalano, “Increased neonatal fat mass, not lean body mass, is associated with maternal obesity,” American Journal of Obstetrics and Gynecology, vol. 195, no. 4, pp. 1100–1103, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. P. M. Catalano, L. Presley, J. Minium, and S. Hauguel-de Mouzon, “Fetuses of obese mothers develop insulin resistance in utero,” Diabetes Care, vol. 32, no. 6, pp. 1076–1080, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. E. Öken and M. W. Gillman, “Fetal origins of obesity,” Obesity Research, vol. 11, no. 4, pp. 496–506, 2003. View at Publisher · View at Google Scholar · View at Scopus
  42. H. M. Ehrenberg, B. M. Mercer, and P. M. Catalano, “The influence of obesity and diabetes on the prevalence of macrosomia,” American Journal of Obstetrics & Gynecology, vol. 191, no. 3, pp. 964–968, 2004. View at Publisher · View at Google Scholar · View at Scopus
  43. G. Dörner and A. Plagemann, “Perinatal hyperinsulinism as possible predisposing factor for diabetes mellitus, obesity and enhanced cardiovascular risk in later life,” Hormone and Metabolic Research, vol. 26, no. 5, pp. 213–221, 1994. View at Publisher · View at Google Scholar · View at Scopus
  44. J. R. O'Reilly and R. M. Reynolds, “The risk of maternal obesity to the long-term health of the offspring,” Clinical Endocrinology, vol. 78, no. 1, pp. 9–16, 2013. View at Publisher · View at Google Scholar · View at Scopus
  45. K. M. Godfrey, T. Forrester, D. J. P. Barker et al., “Maternal nutritional status in pregnancy and blood pressure in childhood,” British Journal of Obstetrics and Gynaecology, vol. 101, no. 5, pp. 398–403, 1994. View at Publisher · View at Google Scholar · View at Scopus
  46. P. M. Clark, C. Atton, C. M. Law, A. Shiell, K. Godfrey, and D. J. P. Barker, “Weight gain in pregnancy, triceps skinfold thickness, and blood pressure, in offspring,” Obstetrics and Gynecology, vol. 91, no. 1, pp. 103–107, 1998. View at Publisher · View at Google Scholar · View at Scopus
  47. K. K. Ryckman, K. S. Borowski, N. I. Parikh, and A. F. Saftlas, “Pregnancy complications and the risk of metabolic syndrome for the offspring,” Current Cardiovascular Risk Reports, vol. 7, no. 3, pp. 217–223, 2013. View at Publisher · View at Google Scholar · View at Scopus
  48. A. M. Magarey, L. A. Daniels, T. J. Boulton, and R. A. Cockington, “Predicting obesity in early adulthood from childhood and parental obesity,” International Journal of Obesity and Related Metabolic Disorders, vol. 27, no. 4, pp. 505–513, 2003. View at Publisher · View at Google Scholar · View at Scopus
  49. S. Danielzik, M. Czerwinski-Mast, K. Langnäse, B. Dilba, and M. J. Müller, “Parental overweight, socioeconomic status and high birth weight are the major determinants of overweight and obesity in 5-7 y-old children: baseline data of the Kiel Obesity Prevention Study (KOPS),” International Journal of Obesity, vol. 28, no. 11, pp. 1494–1502, 2004. View at Publisher · View at Google Scholar · View at Scopus
  50. P. J. Salsberry and P. B. Reagan, “Dynamics of early childhood overweight,” Pediatrics, vol. 116, no. 6, pp. 1329–1338, 2005. View at Publisher · View at Google Scholar · View at Scopus
  51. K. B. Adamo, Z. M. Ferraro, G. Goldfield et al., “The Maternal Obesity Management (MOM) Trial Protocol: a lifestyle intervention during pregnancy to minimize downstream obesity,” Contemporary Clinical Trials, vol. 35, no. 1, pp. 87–96, 2013. View at Publisher · View at Google Scholar · View at Scopus
  52. H. Ainge, C. Thompson, S. E. Ozanne, and K. B. Rooney, “A systematic review on animal models of maternal high fat feeding and offspring glycaemic control,” International Journal of Obesity, vol. 35, no. 3, pp. 325–335, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. M. Li, D. M. Sloboda, and M. H. Vickers, “Maternal obesity and developmental programming of metabolic disorders in offspring: Evidence from animal models,” Experimental Diabetes Research, vol. 2011, Article ID 592408, 9 pages, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. F. Guo and K.-L. C. Jen, “High-fat feeding during pregnancy and lactation affects offspring metabolism in rats,” Physiology and Behavior, vol. 57, no. 4, pp. 681–686, 1995. View at Publisher · View at Google Scholar · View at Scopus
  55. A. Samuelsson, P. A. Matthews, M. Argenton et al., “Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance: a novel murine model of developmental programming,” Hypertension, vol. 51, no. 2, pp. 383–392, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. J. A. Oben, A. Mouralidarane, A. M. Samuelsson et al., “Maternal obesity during pregnancy and lactation programs the development of offspring non-alcoholic fatty liver disease in mice,” Journal of Hepatology, vol. 52, no. 6, pp. 913–920, 2010. View at Publisher · View at Google Scholar · View at Scopus
  57. J. Han, J. Xu, P. N. Epstein, and Y. Q. Liu, “Long-term effect of maternal obesity on pancreatic beta cells of offspring: reduced beta cell adaptation to high glucose and high-fat diet challenges in adult female mouse offspring,” Diabetologia, vol. 48, no. 9, pp. 1810–1818, 2005. View at Publisher · View at Google Scholar · View at Scopus
  58. H. Yamashita, J. Shao, L. Qiao, M. Pagliassotti, and J. E. Friedman, “Effect of spontaneous gestational diabetes on fetal and postnatal hepatic insulin resistance in Leprdb/+ mice,” Pediatric Research, vol. 53, no. 3, pp. 411–418, 2003. View at Publisher · View at Google Scholar · View at Scopus
  59. B. E. Metzger, B. L. Silverman, N. Freinkel, S. L. Dooley, E. S. Ogata, and O. C. Green, “Amniotic fluid insulin concentration as a predictor of obesity,” Archives of Disease in Childhood, vol. 65, no. 10, pp. 1050–1052, 1990. View at Publisher · View at Google Scholar · View at Scopus
  60. R. Boskovic, D. S. Feig, L. Derewlany, B. Knie, G. Portnoi, and G. Koren, “Transfer of insulin lispro across the human placenta: in vitro perfusion studies,” Diabetes Care, vol. 26, no. 5, pp. 1390–1394, 2003. View at Publisher · View at Google Scholar · View at Scopus
  61. G. Holcberg, M. Tsadkin-Tamir, O. Sapir et al., “Transfer of insulin lispro across the human placenta,” European Journal of Obstetrics Gynecology and Reproductive Biology, vol. 115, no. 1, pp. 117–118, 2004. View at Publisher · View at Google Scholar · View at Scopus
  62. G. J. Burton and A. L. Fowden, “Review: the placenta and developmental programming: Balancing fetal nutrient demands with maternal resource allocation,” Placenta, vol. 33, pp. S23–S27, 2012. View at Publisher · View at Google Scholar · View at Scopus
  63. J. Pedersen, The Pregnant Diabetic and Her Newborn, Williams & Wilkins, Baltimore, Md, USA, 2nd edition, 1977.
  64. F. Westermeier, C. Salomón, M. González et al., “Insulin restores gestational diabetes mellitus-reduced adenosine transport involving differential expression of insulin receptor isoforms in human umbilical vein endothelium,” Diabetes, vol. 60, no. 6, pp. 1677–1687, 2011. View at Publisher · View at Google Scholar · View at Scopus
  65. C. Salomón, F. Westermeier, C. Puebla et al., “Gestational diabetes reduces adenosine transport in human placental microvascular endothelium, an effect reversed by insulin,” PLoS ONE, vol. 7, no. 7, Article ID e40578, 2012. View at Google Scholar
  66. T. W. Leung and T. T. Lao, “Placental size and large-for-gestational-age infants in women with abnormal glucose tolerance in pregnancy,” Diabetic Medicine, vol. 17, no. 1, pp. 48–52, 2000. View at Publisher · View at Google Scholar · View at Scopus
  67. A. P. Jones, E. N. Pothos, P. Rada, D. H. Olster, and B. G. Hoebel, “Maternal hormonal manipulations in rats cause obesity and increase medial hypothalamic norepinephrine release in male offspring,” Developmental Brain Research, vol. 88, no. 2, pp. 127–131, 1995. View at Publisher · View at Google Scholar · View at Scopus
  68. A. Plagemann, I. Heidrich, F. Götz, W. Rohde, and G. Dorner, “Lifelong enhanced diabetes susceptibility and obesity after temporary intrahypothalamic hyperinsulinism during brain organization,” Experimental and Clinical Endocrinology, vol. 99, no. 2, pp. 91–95, 1992. View at Publisher · View at Google Scholar · View at Scopus
  69. S. Hauguel-de Mouzon, J. Lepercq, and P. Catalano, “The known and unknown of leptin in pregnancy,” American Journal of Obstetrics & Gynecology, vol. 194, no. 6, pp. 1537–1545, 2006. View at Publisher · View at Google Scholar · View at Scopus
  70. J. T. Smith and B. J. Waddell, “Leptin distribution and metabolism in the pregnant rat: transplacental leptin passage increases in late gestation but is reduced by excess glucocorticoids,” Endocrinology, vol. 144, no. 7, pp. 3024–3030, 2003. View at Publisher · View at Google Scholar · View at Scopus
  71. F. M. Stewart, D. J. Freeman, J. E. Ramsay, I. A. Greer, M. Caslake, and W. R. Ferrell, “Longitudinal assessment of maternal endothelial function and markers of inflammation and placental function throughout pregnancy in lean and obese mothers,” The Journal of Clinical Endocrinology and Metabolism, vol. 92, no. 3, pp. 969–975, 2007. View at Publisher · View at Google Scholar · View at Scopus
  72. R. Meshkani and K. Adeli, “Hepatic insulin resistance, metabolic syndrome and cardiovascular disease,” Clinical Biochemistry, vol. 42, no. 13-14, pp. 1331–1346, 2009. View at Publisher · View at Google Scholar · View at Scopus
  73. R. Muniyappa, M. Montagnani, K. K. Koh, and M. J. Quon, “Cardiovascular actions of insulin,” Endocrine Reviews, vol. 18, no. 5, pp. 463–491, 2007. View at Google Scholar
  74. A. Ullrich, J. R. Bell, E. Y. Chen et al., “Human insulin receptor and its relationship to the tyrosine kinase family of oncogenes,” Nature, vol. 313, no. 6005, pp. 756–761, 1985. View at Publisher · View at Google Scholar · View at Scopus
  75. Y. Ebina, M. Edery, L. Ellis et al., “Expression of a functional human insulin receptor from a cloned cDNA in Chinese hamster ovary cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 82, no. 23, pp. 8014–8018, 1985. View at Publisher · View at Google Scholar · View at Scopus
  76. A. Belfiore, F. Frasca, G. Pandini, L. Sciacca, and R. Vigneri, “Insulin receptor isoforms and insulin receptor/insulin-like growth factor receptor hybrids in physiology and disease,” Endocrine Reviews, vol. 30, no. 6, pp. 586–623, 2009. View at Publisher · View at Google Scholar · View at Scopus
  77. A. R. Saltiel and C. R. Kahn, “Insulin signalling and the regulation of glucose and lipid metabolism,” Nature, vol. 414, no. 6865, pp. 799–806, 2001. View at Publisher · View at Google Scholar · View at Scopus
  78. J.-A. Kim, M. Montagnani, K. K. Kwang, and M. J. Quon, “Reciprocal relationships between insulin resistance and endothelial dysfunction: molecular and pathophysiological mechanisms,” Circulation, vol. 113, no. 15, pp. 1888–1904, 2006. View at Publisher · View at Google Scholar · View at Scopus
  79. C. M. Taniguchi, B. Emanuelli, and C. R. Kahn, “Critical nodes in signalling pathways: insights into insulin action,” Nature Reviews. Molecular Cell Biology, vol. 7, no. 2, pp. 85–96, 2006. View at Publisher · View at Google Scholar · View at Scopus
  80. G. Desoye and S. Hauguel-de Mouzon, “The human placenta in gestational diabetes mellitus: the insulin and cytokine network,” Diabetes Care, vol. 30, supplement 2, pp. S120–S126, 2007. View at Publisher · View at Google Scholar · View at Scopus
  81. B. H. Goodpaster, “Mitochondrial deficiency is associated with insulin resistance,” Diabetes, vol. 62, no. 4, pp. 1032–1035, 2013. View at Publisher · View at Google Scholar · View at Scopus
  82. E. C. Eringa, C. D. A. Stehouwer, G. P. van Nieuw Amerongen, L. Ouwehand, N. Westerhof, and P. Sipkema, “Vasoconstrictor effects of insulin in skeletal muscle arterioles are mediated by ERK1/2 activation in endothelium,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 287, no. 5, pp. H2043–H2048, 2004. View at Publisher · View at Google Scholar · View at Scopus
  83. M. J. Czaja, “JNK regulation of hepatic manifestations of the metabolic syndrome,” Trends in Endocrinology and Metabolism, vol. 21, no. 12, pp. 707–713, 2010. View at Publisher · View at Google Scholar · View at Scopus
  84. J. I. Odegaard and A. Chawla, “The immune system as a sensor of the metabolic state,” Immunity, vol. 38, no. 4, pp. 644–654, 2013. View at Publisher · View at Google Scholar · View at Scopus
  85. I. L. M. H. Aye, T. L. Powell, and T. Jansson, “Review: adiponectin—The missing link between maternal adiposity, placental transport and fetal growth?” Placenta, vol. 34, pp. S40–S45, 2013. View at Publisher · View at Google Scholar · View at Scopus
  86. J. Hirosumi, G. Tuncman, L. Chang et al., “A central, role for JNK in obesity and insulin resistance,” Nature, vol. 420, no. 6913, pp. 333–336, 2002. View at Publisher · View at Google Scholar · View at Scopus
  87. S. J. Marciniak and D. Ron, “Endoplasmic reticulum stress signaling in disease,” Physiological Reviews, vol. 86, no. 4, pp. 1133–1149, 2006. View at Publisher · View at Google Scholar · View at Scopus
  88. M. Cnop, F. Foufelle, and L. A. Velloso, “Endoplasmic reticulum stress, obesity and diabetes,” Trends in Molecular Medicine, vol. 18, no. 1, pp. 59–68, 2012. View at Publisher · View at Google Scholar · View at Scopus
  89. D. Ron and P. Walter, “Signal integration in the endoplasmic reticulum unfolded protein response,” Nature Reviews Molecular Cell Biology, vol. 8, no. 7, pp. 519–529, 2007. View at Publisher · View at Google Scholar · View at Scopus
  90. K. Zhang and R. J. Kaufman, “Protein folding in the endoplasmic reticulum and the unfolded protein response,” Handbook of Experimental Pharmacology, no. 172, pp. 69–91, 2006. View at Google Scholar · View at Scopus
  91. C. Hetz, “The unfolded protein response: controlling cell fate decisions under ER stress and beyond,” Nature Reviews Molecular Cell Biology, vol. 13, no. 2, pp. 89–102, 2012. View at Publisher · View at Google Scholar · View at Scopus
  92. J. Y. Chan, J. Luzuriaga, M. Bensellam, T. J. Biden, and D. R. Laybutt, “Failure of the adaptive unfolded protein response in islets of obese mice is linked with abnormalities in β-cell gene expression and progression to diabetes,” Diabetes, vol. 62, no. 5, pp. 1557–1568, 2013. View at Publisher · View at Google Scholar · View at Scopus
  93. Y. Zhou, J. Lee, C. M. Reno et al., “Regulation of glucose homeostasis through a XBP-1-FoxO1 interaction,” Nature Medicine, vol. 17, no. 3, pp. 356–365, 2011. View at Publisher · View at Google Scholar · View at Scopus
  94. B. H. Cha, J. S. Kim, J. C. Ahn et al., “The role of tauroursodeoxycholic acid on adipogenesis of human adipose-derived stem cells by modulation of ER stress,” Biomaterials, vol. 35, no. 9, pp. 2851–2858, 2014. View at Publisher · View at Google Scholar
  95. H. Kono and K. L. Rock, “How dying cells alert the immune system to danger,” Nature Reviews Immunology, vol. 8, no. 4, pp. 279–289, 2008. View at Publisher · View at Google Scholar · View at Scopus
  96. C. A. Dinarello, “Historical insights into cytokines,” European Journal of Immunology, vol. 37, supplement 1, pp. S34–S45, 2007. View at Publisher · View at Google Scholar · View at Scopus
  97. G. S. Hotamisligil and E. Erbay, “Nutrient sensing and inflammation in metabolic diseases,” Nature Reviews Immunology, vol. 8, no. 12, pp. 923–934, 2008. View at Publisher · View at Google Scholar · View at Scopus
  98. C. N. Lumeng and A. R. Saltiel, “Inflammatory links between obesity and metabolic disease,” The Journal of Clinical Investigation, vol. 121, no. 6, pp. 2111–2117, 2011. View at Publisher · View at Google Scholar · View at Scopus
  99. J. E. Snyder-Cappione and B. S. Nikolajczyk, “When diet and exercise are not enough, think immunomodulation,” Molecular Aspects of Medicine, vol. 34, no. 1, pp. 30–38, 2013. View at Publisher · View at Google Scholar · View at Scopus
  100. S. Hummasti and G. S. Hotamisligil, “Endoplasmic reticulum stress and inflammation in obesity and diabetes,” Circulation Research, vol. 107, no. 5, pp. 579–591, 2010. View at Publisher · View at Google Scholar · View at Scopus
  101. G. S. Hotamisligil, N. S. Shargill, and B. M. Spiegelman, “Adipose expression of tumor necrosis factor-α: direct role in obesity-linked insulin resistance,” Science, vol. 259, no. 5091, pp. 87–91, 1993. View at Publisher · View at Google Scholar · View at Scopus
  102. A. D. Garg, A. Kaczmarek, O. Krysko, P. Vandenabeele, D. V. Krysko, and P. Agostinis, “ER stress-induced inflammation: does it aid or impede disease progression?” Trends in Molecular Medicine, vol. 18, no. 10, pp. 589–598, 2012. View at Publisher · View at Google Scholar · View at Scopus
  103. K. L. A. Souza, E. Gurgul-Convey, M. Elsner, and S. Lenzen, “Interaction between pro-inflammatory and anti-inflammatory cytokines in insulin-producing cells,” The Journal of Endocrinology, vol. 197, no. 1, pp. 139–150, 2008. View at Publisher · View at Google Scholar · View at Scopus
  104. A. K. Cardozo, F. Ortis, J. Storling et al., “Cytokines downregulate the sarcoendoplasmic reticulum pump Ca2+ ATPase 2b and deplete endoplasmic reticulum Ca2+, leading to induction of endoplasmic reticulum stress in pancreatic β-cells,” Diabetes, vol. 54, no. 2, pp. 452–461, 2005. View at Publisher · View at Google Scholar · View at Scopus
  105. C. M. O'Neill, C. Lu, K. L. Corbin et al., “Circulating levels of IL-1B+IL-6 cause ER stress and dysfunction in islets from prediabetic male mice,” Endocrinology, vol. 154, no. 9, pp. 3077–3088, 2013. View at Publisher · View at Google Scholar · View at Scopus
  106. N. Kawasaki, R. Asada, A. Saito, S. Kanemoto, and K. Imaizumi, “Obesity-induced endoplasmic reticulum stress causes chronic inflammation in adipose tissue,” Scientific Reports, vol. 2, article 799, 2012. View at Publisher · View at Google Scholar · View at Scopus
  107. T. Nakamura, M. Furuhashi, P. Li et al., “Double-stranded RNA-dependent protein kinase links pathogen sensing with stress and metabolic homeostasis,” Cell, vol. 140, no. 3, pp. 338–348, 2010. View at Publisher · View at Google Scholar · View at Scopus
  108. B. Sharma, J. K. Altman, D. J. Goussetis, A. K. Verma, and L. C. Platanias, “Protein kinase R as mediator of the effects of interferon (IFN) γ and tumor necrosis factor (TNF) α on normal and dysplastic hematopoiesis,” The Journal of Biological Chemistry, vol. 286, no. 31, pp. 27506–27514, 2011. View at Publisher · View at Google Scholar · View at Scopus
  109. X. Wang, R. Zhang, S. Zhang et al., “Interferon regulatory factor 7 deficiency prevents diet-induced obesity and insulin resistance,” American Journal of Physiology—Endocrinology and Metabolism, vol. 305, no. 4, pp. E485–E495, 2013. View at Publisher · View at Google Scholar · View at Scopus
  110. B. Lu, T. Nakamura, K. Inouye et al., “Novel role of PKR in inflammasome activation and HMGB1 release,” Nature, vol. 488, no. 7413, pp. 670–674, 2012. View at Publisher · View at Google Scholar · View at Scopus
  111. M. G. Netea, L. A. Joosten, E. Lewis et al., “Deficiency of interleukin-18 in mice leads to hyperphagia, obesity and insulin resistance,” Nature Medicine, vol. 12, no. 6, pp. 650–656, 2006. View at Publisher · View at Google Scholar · View at Scopus
  112. G. Boden, P. Cheung, S. Salehi et al., “Insulin regulates the unfolded protein response in human adipose tissue,” Diabetes, vol. 63, no. 3, pp. 912–922, 2014. View at Google Scholar
  113. A. Shkoda, P. A. Ruiz, H. Daniel et al., “Interleukin-10 blocked endoplasmic reticulum stress in intestinal epithelial cells: impact on chronic inflammation,” Gastroenterology, vol. 132, no. 1, pp. 190–207, 2007. View at Publisher · View at Google Scholar · View at Scopus
  114. S. Z. Hasnain, S. Tauro, I. Das et al., “IL-10 promotes production of intestinal mucus by suppressing protein misfolding and endoplasmic reticulum stress in goblet cells,” Gastroenterology, vol. 144, no. 2, pp. 357.e9–368.e9, 2013. View at Publisher · View at Google Scholar · View at Scopus
  115. E. R. Ropelle, M. B. Flores, D. E. Cintra et al., “IL-6 and IL-10 anti-inflammatory activity links exercise to hypothalamic insulin and leptin sensitivity through IKKβ and ER stress inhibition,” PLoS Biology, vol. 8, no. 8, 2010. View at Publisher · View at Google Scholar · View at Scopus
  116. D. Y. Oh, S. Talukdar, E. J. Bae et al., “GPR120 is an omega-3 fatty acid receptor mediating potent anti-inflammatory and insulin-sensitizing effects,” Cell, vol. 142, no. 5, pp. 687–698, 2010. View at Publisher · View at Google Scholar · View at Scopus
  117. M. Suragani, V. D. Aadinarayana, A. B. Pinjari et al., “Human resistin, a proinflammatory cytokine, shows chaperone-like activity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 51, pp. 20467–20472, 2013. View at Google Scholar
  118. M. Kuro-o, Y. Matsumura, H. Aizawa et al., “Mutation of the mouse klotho gene leads to a syndrome resembling ageing,” Nature, vol. 390, no. 6655, pp. 45–51, 1997. View at Publisher · View at Google Scholar · View at Scopus
  119. M. S. Razzaque, “The role of Klotho in energy metabolism,” Nature Reviews Endocrinology, vol. 8, no. 10, pp. 579–587, 2012. View at Publisher · View at Google Scholar · View at Scopus
  120. H. Kurosu, M. Yamamoto, J. D. Clark et al., “Physiology: suppression of aging in mice by the hormone Klotho,” Science, vol. 309, no. 5742, pp. 1829–1833, 2005. View at Publisher · View at Google Scholar · View at Scopus
  121. F. Liu, S. Wu, H. Ren, and J. Gu, “Klotho suppresses RIG-I-mediated senescence-associated inflammation,” Nature Cell Biology, vol. 13, no. 3, pp. 254–262, 2011. View at Publisher · View at Google Scholar · View at Scopus
  122. S. Banerjee, Y. Zhao, P. S. Sarkar, K. P. Rosenblatt, R. G. Tilton, and S. Choudhary, “Klotho ameliorates chemically induced endoplasmic reticulum (ER) stress signaling,” Cellular Physiology and Biochemistry, vol. 31, no. 4-5, pp. 659–672, 2013. View at Publisher · View at Google Scholar · View at Scopus
  123. J. Dahlgren, C. Nilsson, E. Jennische et al., “Prenatal cytokine exposure results in obesity and gender-specific programming,” American Journal of Physiology—Endocrinology and Metabolism, vol. 281, no. 2, pp. E326–E334, 2001. View at Google Scholar · View at Scopus
  124. J. C. Challier, S. Basu, T. Bintein et al., “Obesity in pregnancy stimulates macrophage accumulation and inflammation in the placenta,” Placenta, vol. 29, no. 3, pp. 274–281, 2008. View at Publisher · View at Google Scholar · View at Scopus
  125. M. R. Indra, S. Karyono, R. Ratnawati, and S. G. Malik, “Quercetin suppresses inflammation by reducing ERK1/2 phosphorylation and NF kappa B activation in Leptin-induced human umbilical vein endothelial cells (HUVECs),” BMC Research Notes, vol. 6, no. 1, article 275, 2013. View at Publisher · View at Google Scholar · View at Scopus
  126. Z. Wu, J. Zhao, H. Xu et al., “Maternal quercetin administration during gestation and lactation decrease endoplasmic reticulum stress and related inflammation in the adult offspring of obese female rats,” Europe Journal of Nutrition, 2014. View at Publisher · View at Google Scholar
  127. T. Nakamura, A. Arduini, B. Baccaro, M. Furuhashi, and G. S. Hotamisligil, “Small-molecule inhibitors of PKR improve glucose homeostasis in obese diabetic mice,” Diabetes, vol. 63, no. 2, pp. 526–534, 2014. View at Publisher · View at Google Scholar
  128. S. Entringer, C. Buss, J. M. Swanson et al., “Fetal programming of body composition, obesity, and metabolic function: the role of intrauterine stress and stress biology,” Journal of Nutrition and Metabolism, vol. 2012, Article ID 632548, 16 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  129. R. Dantzer, J. C. O'Connor, G. G. Freund, R. W. Johnson, and K. W. Kelley, “From inflammation to sickness and depression: when the immune system subjugates the brain,” Nature Reviews Neuroscience, vol. 9, no. 1, pp. 46–56, 2008. View at Publisher · View at Google Scholar · View at Scopus
  130. R. E. Fisher, M. Steele, and N. A. Karrow, “Fetal programming of the neuroendocrine-immune system and metabolic disease,” Journal of Pregnancy, vol. 2012, Article ID 792934, 10 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  131. E. Jarvie, S. Hauguel-de-Mouzon, S. M. Nelson, N. Sattar, P. M. Catalano, and D. J. Freeman, “Lipotoxicity in obese pregnancy and its potential role in adverse pregnancy outcome and obesity in the offspring,” Clinical Science, vol. 119, no. 3, pp. 123–129, 2010. View at Publisher · View at Google Scholar · View at Scopus
  132. P. M. Catalano and H. M. Ehrenberg, “The short- and long-term implications of maternal obesity on the mother and her offspring,” British Journal of Obstetrics and Gynaecology, vol. 113, no. 10, pp. 1126–1133, 2006. View at Publisher · View at Google Scholar · View at Scopus
  133. K. A. Roberts, S. C. Riley, R. M. Reynolds et al., “Placental structure and inflammation in pregnancies associated with obesity,” Placenta, vol. 32, no. 3, pp. 247–254, 2011. View at Publisher · View at Google Scholar · View at Scopus
  134. C. E. McCurdy, J. M. Bishop, S. M. Williams et al., “Maternal high-fat diet triggers lipotoxicity in the fetal livers of nonhuman primates,” The Journal of Clinical Investigation, vol. 119, no. 2, pp. 323–335, 2009. View at Publisher · View at Google Scholar · View at Scopus
  135. N. Anderson and J. Borlak, “Molecular mechanisms and therapeutic targets in steatosis and steatohepatitis,” Pharmacological Reviews, vol. 60, no. 3, pp. 311–357, 2008. View at Publisher · View at Google Scholar · View at Scopus
  136. M. Kars, L. Yang, M. F. Gregor et al., “Tauroursodeoxycholic acid may improve liver and muscle but not adipose tissue insulin sensitivity in obese men and women,” Diabetes, vol. 59, no. 8, pp. 1899–1905, 2010. View at Publisher · View at Google Scholar · View at Scopus
  137. M. G. Roma, F. D. Toledo, A. C. Boaglio et al., “Ursodeoxycholic acid in cholestasis: linking action mechanisms to therapeutic applications,” Clinical Science, vol. 121, no. 12, pp. 523–544, 2011. View at Google Scholar