Table of Contents Author Guidelines Submit a Manuscript
International Journal of Endocrinology
Volume 2014, Article ID 537603, 10 pages
http://dx.doi.org/10.1155/2014/537603
Research Article

Energy Balance Regulating Neuropeptides Are Expressed through Pregnancy and Regulated by Interleukin-6 Deficiency in Mouse Placenta

1Department of Physiology, Research Center of Molecular Medicine and Chronic Diseases (CIMUS), University of Santiago de Compostela, Avenida de Barcelona s/n, 15782 Santiago de Compostela, Spain
2Instituto de Investigación Sanitaria de Santiago de Compostela (IDIS), 15706 Santiago de Compostela, Spain
3CIBER Fisiopatología Obesidad y Nutrición (CB06/03), Instituto de Salud Carlos III (ISCIII), Ministerio de Economía y Competitividad (MINECO), 15706 Santiago de Compostela, Spain

Received 21 November 2013; Revised 21 January 2014; Accepted 2 February 2014; Published 12 March 2014

Academic Editor: Georgios Valsamakis

Copyright © 2014 Patricia Pazos 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. J. R. Speakman, D. A. Levitsky, D. B. Allison et al., “Set points, settling points and some alternative models: theoretical options to understand how genes and environments combine to regulate body adiposity,” Disease Models & Mechanisms, vol. 4, no. 6, pp. 733–745, 2011. View at Publisher · View at Google Scholar · View at Scopus
  2. K. W. Williams and J. K. Elmquist, “From neuroanatomy to behavior: central integration of peripheral signals regulating feeding behavior,” Nature Neuroscience, vol. 15, no. 10, pp. 1350–1355, 2012. View at Publisher · View at Google Scholar
  3. J. E. Schneider, C. M. Klingerman, and A. Abdulhay, “Sense and nonsense in metabolic control of reproduction,” Frontiers in Endocrinology, vol. 3, article 26, 2012. View at Publisher · View at Google Scholar
  4. D. Richard, B. Monge-Roffarello, K. Chechi, S. M. Labbe, and E. E. Turcotte, “Control and physiological determinants of sympathetically mediated brown adipose tissue thermogenesis,” Frontiers in Endocrinology, vol. 3, article 36, 2012. View at Publisher · View at Google Scholar
  5. M. G. Myers Jr. and D. P. Olson, “Central nervous system control of metabolism,” Nature, vol. 491, no. 7424, pp. 357–363, 2012. View at Publisher · View at Google Scholar
  6. M. Lopez, S. Tovar, M. J. Vazquez, L. M. Williams, and C. Dieguez, “Peripheral tissue-brain interactions in the regulation of food intake,” Proceedings of the Nutrition Society, vol. 66, no. 1, pp. 131–155, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. S. R. Ladyman, R. A. Augustine, and D. R. Grattan, “Hormone interactions regulating energy balance during pregnancy,” Journal of Neuroendocrinology, vol. 22, no. 7, pp. 805–817, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. K. Sinchak and E. J. Wagner, “Estradiol signaling in the regulation of reproduction and energy balance,” Frontiers in Endocrinology, vol. 33, no. 4, pp. 342–363, 2012. View at Publisher · View at Google Scholar
  9. A. Crown, D. K. Clifton, and R. A. Steiner, “Neuropeptide signaling in the integration of metabolism and reproduction,” Neuroendocrinology, vol. 86, no. 3, pp. 175–182, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. J. W. Hill, J. K. Elmquist, and C. F. Elias, “Hypothalamic pathways linking energy balance and reproduction,” American Journal of Physiology, vol. 294, no. 5, pp. E827–E832, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Kumar and G. Kaur, “Intermittent fasting dietary restriction regimen negatively influences reproduction in young rats: a study of hypothalamo-hypophysial-gonadal axis,” PLoS ONE, vol. 8, no. 1, Article ID e52416, 2013. View at Publisher · View at Google Scholar
  12. R. Senaris, T. Garcia-Caballero, X. Casabiell et al., “Synthesis of leptin in human placenta,” Endocrinology, vol. 138, no. 10, pp. 4501–4504, 1997. View at Publisher · View at Google Scholar · View at Scopus
  13. N. Hoogard, L. Hunter, J. S. Duncan, L. M. Williams, P. Trayhurn, and J. G. Mercer, “Leptin and leptin receptor mRNA and protein expression in the murine fetus and placenta,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 20, pp. 11073–11078, 1997. View at Publisher · View at Google Scholar · View at Scopus
  14. J. E. Caminos, R. Nogueiras, R. Gallego et al., “Expression and regulation of adiponectin and receptor in human and rat placenta,” The Journal of Clinical Endocrinology & Metabolism, vol. 90, no. 7, pp. 4276–4286, 2005. View at Publisher · View at Google Scholar · View at Scopus
  15. H. N. Jones, T. Jansson, and T. L. Powell, “Full-length adiponectin attenuates insulin signaling and inhibits insulin-stimulated amino acid transport in human primary trophoblast cells,” Diabetes, vol. 59, no. 5, pp. 1161–1170, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. N. di Simone, F. di Nicuolo, D. Marzioni et al., “Resistin modulates glucose uptake and glucose transporter-1 (GLUT-1) expression in trophoblast cells,” Journal of Cellular and Molecular Medicine, vol. 13, no. 2, pp. 388–397, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. S. Yura, N. Sagawa, H. Itoh et al., “Resistin is expressed in the human placenta,” The Journal of Clinical Endocrinology & Metabolism, vol. 88, no. 3, pp. 1394–1397, 2003. View at Publisher · View at Google Scholar · View at Scopus
  18. N. Noyola-Martíneza, L. Díaz, E. Avila, A. Halhali, F. Larrea, and D. Barrera, “Calcitriol downregulates TNF-α and IL-6 expression in cultured placental cells from preeclamptic women,” Cytokine, vol. 61, no. 1, pp. 245–250, 2013. View at Publisher · View at Google Scholar
  19. S. K. Munro, M. D. Mitchell, and A. P. Ponnampalam, “Histone deacetylase inhibition by trichostatin A mitigates LPS induced TNFα and IL-10 production in human placental explants,” Placenta, vol. 34, no. 7, pp. 567–573, 2013. View at Publisher · View at Google Scholar
  20. R. Beloosesky, D. A. Gayle, F. Amidi, S. N. Ahanya, M. Desai, and M. G. Ross, “Ontogenic expression of putative feeding peptides in the rat fetal brain and placenta,” Nutritional Neuroscience, vol. 9, no. 1-2, pp. 33–40, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. J. E. Caminos, S. B. Bravo, C. R. González et al., “Food intake regulating-neuropeptides are expressed and regulated through pregnancy and following food restriction in rat placenta,” Reproductive Biology and Endocrinology, vol. 6, article 14, 2008. View at Publisher · View at Google Scholar
  22. S. I. Grigorakis, E. Anastasiou, K. Dai, A. Souvatzoglou, and M. Alevizaki, “Three mRNA transcripts of the proopiomelanocortin gene in human placenta at term,” European Journal of Endocrinology, vol. 142, no. 5, pp. 533–536, 2000. View at Google Scholar · View at Scopus
  23. J. Robidoux, L. Simoneau, A. Masse, and J. Lafond, “Activation of L-type calcium channels induces corticotropin-releasing factor secretion from human placental trophoblasts,” The Journal of Clinical Endocrinology & Metabolism, vol. 85, no. 9, pp. 3356–3364, 2000. View at Google Scholar · View at Scopus
  24. C. L. Chen, C. C. Chang, D. T. Krieger, and C. W. Bardin, “Expression and regulation of proopiomelanocortin-like gene in the ovary and placenta: comparison with the testis,” Endocrinology, vol. 118, no. 6, pp. 2382–2389, 1986. View at Google Scholar · View at Scopus
  25. J. Dotsch, K.-D. Nusken, I. Knerr, M. Kirschbaum, R. Repp, and W. Rascher, “Leptin and neuropeptide Y gene expression in human placenta: ontogeny and evidence for similarities to hypothalamic regulation,” The Journal of Clinical Endocrinology & Metabolism, vol. 84, no. 8, pp. 2755–2758, 1999. View at Google Scholar · View at Scopus
  26. M. Erta, A. Quintana, and J. Hidalgo, “Interleukin-6, a major cytokine in the central nervous system,” International Journal of Biological Sciences, vol. 8, no. 9, pp. 1254–1266, 2012. View at Publisher · View at Google Scholar
  27. S. Lager, N. Jansson, A. L. Olsson, M. Wennergren, T. Jansson, and T. L. Powell, “Effect of IL-6 and TNF-α on fatty acid uptake in cultured human primary trophoblast cells,” Placenta, vol. 32, no. 2, pp. 121–127, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. R. Shao, M. Nutu, L. Karlsson-Lindahl et al., “Downregulation of cilia-localized Il-6Rα by 17β-estradiol in mouse and human fallopian tubes,” American Journal of Physiology, vol. 297, no. 1, pp. C140–C151, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. P. Pazos, L. Lima, F. F. Casanueva, C. Dieguez, and M. C. Garcia, “Interleukin 6 deficiency modulates the hypothalamic expression of energy balance regulating peptides during pregnancy in mice,” PLoS ONE, vol. 8, no. 8, Article ID e72339, 2013. View at Publisher · View at Google Scholar
  30. J.-O. Jansson, K. Wallenius, I. Wernstedt, C. Ohlsson, S. L. Dickson, and V. Wallenius, “On the site and mechanism of action of the anti-obesity effects of interleukin-6,” Growth Hormone and IGF Research, vol. 13, supplement A, pp. S28–S32, 2003. View at Publisher · View at Google Scholar · View at Scopus
  31. E. Schéle, A. Benrick, L. Grahnemo et al., “Inter-relation between interleukin (IL)-1, IL-6 and body fat regulating circuits of the hypothalamic arcuate nucleus,” Journal of Neuroendocrinology, vol. 25, no. 6, pp. 580–589, 2013. View at Publisher · View at Google Scholar
  32. K. Stenlof, I. Wernstedt, T. Fjallman, V. Wallenius, K. Wallenius, and J.-O. Jansson, “Interleukin-6 levels in the central nervous system are negatively correlated with fat mass in overweight/obese subjects,” The Journal of Clinical Endocrinology & Metabolism, vol. 88, no. 9, pp. 4379–4383, 2003. View at Publisher · View at Google Scholar · View at Scopus
  33. V. Wallenius, K. Wallenius, B. Ahrén et al., “Interleukin-6-deficient mice develop mature-onset obesity,” Nature Medicine, vol. 8, no. 1, pp. 75–79, 2002. View at Publisher · View at Google Scholar · View at Scopus
  34. C. T. de Souza, E. P. Araujo, S. Bordin et al., “Consumption of a fat-rich diet activates a proinflammatory response and induces insulin resistance in the hypothalamus,” Endocrinology, vol. 146, no. 10, pp. 4192–4199, 2005. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Milanski, G. Degasperi, A. Coope et al., “Saturated fatty acids produce an inflammatory response predominantly through the activation of TLR4 signaling in hypothalamus: implications for the pathogenesis of obesity,” The Journal of Neuroscience, vol. 29, no. 2, pp. 359–370, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. K. Wallenius, V. Wallenius, D. Sunter, S. L. Dickson, and J.-O. Jansson, “Intracerebroventricular interleukin-6 treatment decreases body fat in rats,” Biochemical and Biophysical Research Communications, vol. 293, no. 1, pp. 560–565, 2002. View at Publisher · View at Google Scholar · View at Scopus
  37. I. Wernstedt, A. Edgley, A. Berndtsson et al., “Reduced stress- and cold-induced increase in energy expenditure in interleukin-6-deficient mice,” American Journal of Physiology, vol. 291, no. 3, pp. R551–R557, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. J. Faldt, I. Wernstedt, S. M. Fitzgerald, K. Wallenius, G. Bergström, and J.-O. Jansson, “Reduced exercise endurance in interleukin-6-deficient mice,” Endocrinology, vol. 145, no. 6, pp. 2680–2686, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Hidalgo, S. Florit, M. Giralt, B. Ferrer, C. Keller, and H. Pilegaard, “Transgenic mice with astrocyte-targeted production of interleukin-6 are resistant to high-fat diet-induced increases in body weight and body fat,” Brain, Behavior, and Immunity, vol. 24, no. 1, pp. 119–126, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. M. B. Flores, M. F. Fernandes, E. R. Ropelle et al., “Exercise improves insulin and leptin sensitivity in hypothalamus of Wistar rats,” Diabetes, vol. 55, no. 9, pp. 2554–2561, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. B. C. Borges, R. Rorato, Y. Avraham et al., “Leptin resistance and desensitization of hypophagia during prolonged inflammatory challenge,” American Journal of Physiology, vol. 300, no. 5, pp. E858–E869, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. A. Benrick, E. Schele, S. B. Pinnock et al., “Interleukin-6 gene knockout influences energy balance regulating peptides in the hypothalamic paraventricular and supraoptic nuclei,” Journal of Neuroendocrinology, vol. 21, no. 7, pp. 620–628, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. E. Schéle, C. Fekete, P. Egri et al., “Interleukin-6 receptor α is co-localised with melanin-concentrating hormone in human and mouse hypothalamus,” Journal of Neuroendocrinology, vol. 24, no. 6, pp. 930–943, 2012. View at Publisher · View at Google Scholar
  44. S. Lager and T. L. Powell, “Regulation of nutrient transport across the placenta,” Journal of Pregnancy, vol. 2012, Article ID 179827, 14 pages, 2012. View at Publisher · View at Google Scholar
  45. M. Kopf, H. Baumann, G. Freer et al., “Impaired immune and acute-phase responses in interleukin-6-deficient mice,” Nature, vol. 368, no. 6469, pp. 339–342, 1994. View at Publisher · View at Google Scholar · View at Scopus
  46. M. J. Vazquez, C. R. Gonzalez, L. Varela et al., “Central resistin regulates hypothalamic and peripheral lipid metabolism in a nutritional-dependent fashion,” Endocrinology, vol. 149, no. 9, pp. 4534–4543, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. I. Rioja, K. A. Bush, J. B. Buckton, M. C. Dickson, and P. F. Life, “Joint cytokine quantification in two rodent arthritis models: kinetics of expression, correlation of mRNA and protein levels and response to prednisolone treatment,” Clinical & Experimental Immunology, vol. 137, no. 1, pp. 65–73, 2004. View at Publisher · View at Google Scholar · View at Scopus
  48. F. Isken, M. O. Weickert, M. H. Tschöp et al., “Metabolic effects of diets differing in glycaemic index depend on age and endogenous glucose-dependent insulinotrophic polypeptide in mice,” Diabetologia, vol. 52, no. 10, pp. 2159–2168, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. S. B. Bravo, J. E. Caminos, C. R. González et al., “Leptin and fasting regulate rat gastric glucose-regulated protein 58,” International Journal of Peptides, vol. 2011, Article ID 969818, 11 pages, 2011. View at Publisher · View at Google Scholar
  50. M. Garcia-Lavandeira, V. Quereda, I. Flores et al., “A GRFa2/Prop1/Stem (GPS) cell niche in the pituitary,” PLoS ONE, vol. 4, no. 3, Article ID e4815, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. S. B. Bravo, M. E. Garcia-Rendueles, A. R. Garcia-Rendueles et al., “Humanized medium (h7H) allows long-term primary follicular thyroid cultures from human normal thyroid, benign neoplasm, and cancer,” The Journal of Clinical Endocrinology & Metabolism, vol. 98, no. 6, pp. 2431–2441, 2013. View at Publisher · View at Google Scholar
  52. K. J. Livak and T. D. Schmittgen, “Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method,” Methods, vol. 25, no. 4, pp. 402–408, 2001. View at Publisher · View at Google Scholar · View at Scopus
  53. N. M. Orsi, N. Gopichandran, U. V. Ekbote, and J. J. Walker, “Murine serum cytokines throughout the estrous cycle, pregnancy and post partum period,” Animal Reproduction Science, vol. 96, no. 1-2, pp. 54–65, 2006. View at Publisher · View at Google Scholar · View at Scopus
  54. P. J. Mark, J. L. Lewis, M. L. Jones, J. A. Keelan, and B. J. Waddell, “The inflammatory state of the rat placenta increases in late gestation and is further enhanced by glucocorticoids in the labyrinth zone,” Placenta, vol. 34, no. 7, pp. 559–566, 2013. View at Publisher · View at Google Scholar
  55. S. Hauguel-de Mouzon and M. Guerre-Millo, “The placenta cytokine network and inflammatory signals,” Placenta, vol. 27, no. 8, pp. 794–798, 2006. View at Publisher · View at Google Scholar · View at Scopus
  56. R. Agarwal, A. Loganath, A. C. Roy, Y. C. Wong, C. Lindoff, and S. C. Ng, “Increased expression of interleukin 6 in term compared to the first trimester human placental villi,” Hormone and Metabolic Research, vol. 32, no. 5, pp. 164–168, 2000. View at Google Scholar · View at Scopus
  57. M. de, T. H. Sanford, and G. W. Wood, “Detection of interleukin-1, interleukin-6, and tumor necrosis factor-α in the uterus during the second half of pregnancy in the mouse,” Endocrinology, vol. 131, no. 1, pp. 14–20, 1992. View at Publisher · View at Google Scholar · View at Scopus
  58. L. Zhang, T. Sugiyama, N. Murabayashi et al., “The inflammatory changes of adipose tissue in late pregnant mice,” Journal of Molecular Endocrinology, vol. 47, no. 2, pp. 157–165, 2011. View at Publisher · View at Google Scholar · View at Scopus
  59. T. M. Reyes and P. E. Sawchenko, “Involvement of the arcuate nucleus of the hypothalamus in interleukin-1-induced anorexia,” The Journal of Neuroscience, vol. 22, no. 12, pp. 5091–5099, 2002. View at Google Scholar · View at Scopus
  60. B. C. Borges, J. Antunes-Rodrigues, M. Castro, J. C. Bittencourt, C. F. Elias, and L. L. K. Elias, “Expression of hypothalamic neuropeptides and the desensitization of pituitary-adrenal axis and hypophagia in the endotoxin tolerance,” Hormones and Behavior, vol. 52, no. 4, pp. 508–519, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. 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, Article ID e1000465, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. R. M. Senaris, M. L. Trujillo, B. Navia et al., “Interleukin-6 regulates the expression of hypothalamic neuropeptides involved in body weight in a gender-dependent way,” Journal of Neuroendocrinology, vol. 23, no. 8, pp. 675–686, 2011. View at Publisher · View at Google Scholar · View at Scopus
  63. V. Sergeyev, C. Broberger, and T. Hokfelt, “Effect of LPS administration on the expression of POMC, NPY, galanin, CART and MCH mRNAs in the rat hypothalamus,” Molecular Brain Research, vol. 90, no. 2, pp. 93–100, 2001. View at Publisher · View at Google Scholar · View at Scopus
  64. A. Malassine, J.-L. Frendo, and D. Evain-Brion, “A comparison of placental development and endocrine functions between the human and mouse model,” Human Reproduction Update, vol. 9, no. 6, pp. 531–539, 2003. View at Publisher · View at Google Scholar · View at Scopus