Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2017 (2017), Article ID 8254289, 14 pages
https://doi.org/10.1155/2017/8254289
Review Article

Modulatory Mechanism of Polyphenols and Nrf2 Signaling Pathway in LPS Challenged Pregnancy Disorders

1National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Key Laboratory of Agro-Ecological Processes in Subtropical Region, Institute of Subtropical Agriculture Chinese Academy of Sciences, Changsha, Hunan 410125, China
2University of the Chinese Academy of Sciences, Beijing 10008, China
3Hunan Collaborative Innovation Center for Utilization of Botanical Functional Ingredients and Hunan Collaborative Innovation Center of Animal Production Safety, Changsha, Hunan 410000, China
4Shaheed Benazir Bhutto University of Veterinary & Animal Sciences, Sakrand, Sindh 67210, Pakistan
5Department of Veterinary Microbiology, Faculty of Animal Husbandry and Veterinary Sciences, Sindh Agriculture University, Tandojam, Sindh 70050, Pakistan
6Food Engineering and Bioprocess Technology, Asian Institute of Technology, Bangkok 12120, Thailand

Correspondence should be addressed to Bie Tan; nc.ca.asi@nateib

Received 7 April 2017; Accepted 16 July 2017; Published 23 August 2017

Academic Editor: Alessandro Venditti

Copyright © 2017 Tarique Hussain 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. X. F. Zeng, F. Wang, X. Fan et al., “Dietary arginine supplementation during early pregnancy enhances embryonic survival in rats,” Journal of Nutrition, vol. 138, pp. 1421–1425, 2008. View at Google Scholar
  2. K. McNamee, F. Dawood, and R. Farquharson, “Recurrent miscarriage and thrombophilia: an update,” Current Opinion in Obstetrics and Gynecology, vol. 24, no. 4, pp. 229–234, 2012. View at Publisher · View at Google Scholar · View at Scopus
  3. A. K. Goff, “Embryonic signals and survival,” Reproduction Domestic Animals, vol. 37, no. 1, pp. 133–139, 2002. View at Google Scholar
  4. D. D. Neubourg, J. Gerris, K. Mangelschots, E. Van Royen, M. Vercruyssen, and M. Elseviers, “Single top quality embryo transfer as a model for prediction of early pregnancy outcome,” Human Reproduction, vol. 19, pp. 1476–1479, 2004. View at Publisher · View at Google Scholar · View at Scopus
  5. Z. Zhou, L. Wang, Z. Song, J. C. Lambert, C. J. McClain, and Y. J. Kang, “A critical involvement of oxidative stress in acute alcohol-induced hepatic TNF-alpha production,” American Journal of Pathology, vol. 163, pp. 1137–1146, 2003. View at Google Scholar
  6. A. Kunnen, M. G. van Pampus, J. G. Aarnoudse, C. P. van der Schans, F. Abbas, and M. M. Faas, “The effect of Porphyromonas gingivalis lipopolysaccharide on pregnancy in the rat,” Oral Diseases, vol. 20, no. 6, pp. 591–601, 2014. View at Publisher · View at Google Scholar · View at Scopus
  7. P. Xue, M. Zheng, P. Gong et al., “Single administration of ultra-low-dose lipopolysaccharide in rat early pregnancy induces TLR4 activation in the placenta contributing to preeclampsia,” PLoS One, vol. 10, no. 4, article e0124001, 2015. View at Publisher · View at Google Scholar · View at Scopus
  8. J. M. Bowen, L. Chamley, M. D. Mitchell, and J. A. Keelan, “Cytokines of the placenta and extraplacental membranes: biosynthesis, secretion and roles in establishment of pregnancy in women,” Placenta, vol. 23, pp. 239–256, 2002. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Collins, M. Ramsay, M. P. Slack et al., “Risk of invasive Haemophilus influenzae infection during pregnancy and association with adverse fetal outcomes,” The Journal of the American Medical Association, vol. 311, no. 11, pp. 1125–1132, 2014. View at Publisher · View at Google Scholar · View at Scopus
  10. D. X. Xu, H. Wang, H. Ning, L. Zhao, and Y. H. Chen, “Maternally administered melatonin differentially regulates lipopolysaccharide-induced proinflammatory and anti-inflammatory cytokines in maternal serum, amniotic fluid, fetal liver, and fetal brain,” Journal of Pineal Research, vol. 43, pp. 74–79, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. A. Ornoy, “Embryonic oxidative stress as a mechanism of teratogenesis with special emphasis on diabetic embryopathy,” Reproductive Toxicology, vol. 24, pp. 31–41, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. P. G. Wells, G. P. McCallum, K. C. Lam, J. T. Henderson, and S. L. Ondovcik, “Oxidative DNA damage and repair in teratogenesis and neurodevelopmental deficits,” Birth Defects Research Part C, Embryo Today, vol. 90, pp. 103–109, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. I. A. Buhimschi, C. S. Buhimschi, and C. P. Weiner, “Protective effect of N-acetylcysteine against fetal death and preterm labor induced by maternal inflammation,” American Journal of Obstetrics & Gynecology, vol. 188, pp. 203–208, 2003. View at Google Scholar
  14. Y. Zhao, K. Koga, Y. Osuga et al., “Cyclic stretch augments production of neutrophil chemokines and matrix metalloproteinase-1 in human uterine smooth muscle cells,” American Journal of Reproductive Immunology, vol. 69, pp. 240–247, 2013. View at Publisher · View at Google Scholar · View at Scopus
  15. D. L. Rivera, S. M. Olister, X. Liu et al., “Interleukin-10 attenuates experimental fetal growth restriction and demise,” Federation of American Societies of Experimental Biology Journal, vol. 12, pp. 189–197, 1998. View at Google Scholar
  16. D. G. Ogando, D. Paz, M. Cella, and A. M. Franchi, “The fundamental role of increased production of nitric oxide in lipopolysaccharide-induced embryonic resorption in mice,” Reproduction, vol. 125, pp. 95–110, 2003. View at Publisher · View at Google Scholar
  17. S. J. Chapple, R. C. Siow, and G. E. Mann, “Crosstalk between Nrf2 and the proteasome: therapeutic potential of Nrf2 inducers in vascular disease and aging,” International Journal of Biochemistry and Cell Biology, vol. 44, pp. 1315–1320, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. R. Howden, “Nrf2 and cardiovascular defense,” Oxidative Medicine and Cellular Longevity, vol. 2013, Article ID 104308, 10 pages, 2013. View at Publisher · View at Google Scholar
  19. N. Kweider, A. Fragoulis, C. Rosen et al., “Interplay between vascular endothelial growth factor (VEGF) and nuclear factor erythroid 2-related factor-2 (Nrf2): implications for preeclampsia,” The Journal of Biological Chemistry, vol. 286, pp. 42863–42872, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. R. Lim, G. Barker, and M. Lappas, “The transcription factor Nrf2 is decreased after spontaneous term labour in human fetal membranes where it exerts anti-inflammatory properties,” Placenta, vol. 36, pp. 7–17, 2015. View at Publisher · View at Google Scholar · View at Scopus
  21. Y. Gan, S. Zheng, J. P. Baak et al., “Prediction of the anti-inflammatory mechanisms of curcumin by module-based protein interaction network analysis,” Acta Pharmaceutica Sinica-B, vol. 5, no. 6, pp. 590–595, 2015. View at Publisher · View at Google Scholar · View at Scopus
  22. B. Rajitha, A. Belalcazar, G. P. Nagaraju et al., “Inhibition of NF-KB translocation by curcumin analogs induces G0/G1 arrest and downregulates thymidylate synthase in colorectal cancer,” Cancer Letters, vol. 373, no. 2, pp. 227–233, 2016. View at Publisher · View at Google Scholar · View at Scopus
  23. Y. D. Hsuuw, C. K. Chang, W. H. Chan, and J. S. Yu, “Curcumin prevents methylglyoxal-induced oxidative stress and apoptosis in mouse embryonic stem cells and blastocysts,” Journal of Cellular Physiology, vol. 205, no. 3, pp. 379–386, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. D. Barrera, L. Díaz, N. Noyola-Martínez, and A. Halhali, “Vitamin D and inflammatory cytokines in healthy and preeclamptic pregnancies,” Nutrients, vol. 7, no. 8, pp. 6465–6490, 2015. View at Publisher · View at Google Scholar · View at Scopus
  25. L. Verstrepen, T. Bekaert, T. L. Chau, J. Tavernier, A. Chariot, and R. Beyaert, “TLR-4, IL-1R and TNF-R signaling to NF-kappaB: variations on a common theme. Cellular and molecular life sciences,” Cellular and Molecular Life Sciences, vol. 65, no. 19, pp. 2964–2978, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. D. Ribeiro, M. Freitas, J. L. Lima, and E. Fernandes, “Pro-inflammatory pathways: the modulation by flavonoids,” Medicinal Research Review, vol. 35, no. 5, pp. 877–936, 2015. View at Publisher · View at Google Scholar · View at Scopus
  27. E. Bognár, The critical role of MAP-kinases and PI3K-Akt signaling pathways in inflammation and oxidative stress, [Ph.D. Thesis], University of Pécs, Medical School Department of Biochemistry and Medical Chemistry, Hungary, 2013.
  28. M. Zhao, Y. H. Chen, X. Chen et al., “Folic acid supplementation during pregnancy protects against lipopolysaccharide-induced neural tube defects in mice,” Toxicology Letters, vol. 224, pp. 201–208, 2014. View at Publisher · View at Google Scholar · View at Scopus
  29. J. Yui, M. Garcia-Lloret, T. G. Wegmann, and L. I. Guilbert, “Cytotoxicity of tumour necrosis factor-alpha and gamma-interferon against primary human placental trophoblasts,” Placenta, vol. 15, no. 8, pp. 819–835, 1994. View at Google Scholar
  30. O. Dammann and A. Leviton, “Maternal intrauterine infection, cytokines, and brain damage in the preterm newborn,” Pediatric Research, vol. 42, pp. 1–8, 1997. View at Publisher · View at Google Scholar
  31. D. A. Clark, G. Chaouat, P. C. Arck, H. W. Mittruecker, and G. A. Levy, “Cutting edge: ctokine-dependent abortion in CBA × DBA/2 mice is mediated by the procoagulant fgl2 prothombinase,” The Journal of Immunology, vol. 160, no. 2, pp. 545–549, 1998. View at Google Scholar
  32. D. A. Clark, G. Yu, P. C. Arck, G. A. Levy, and R. M. Gorczynski, “MD-1 is a critical part of the mechanism causing Th1-cytokine-triggered murine fetal loss syndrome,” American Journal of Reproductive Immunology, vol. 49, pp. 297–307, 2003. View at Google Scholar
  33. D. A. Clark, J. W. Ding, G. Yu, G. A. Levy, and R. M. Gorczynski, “Fgl2 prothrombinase expression in mouse trophoblast and decidua triggers abortion but may be countered by OX-2,” Molecular Human Reproduction, vol. 7, pp. 185–194, 2001. View at Google Scholar
  34. K. W. Moore, R. de Waal Malefyt, R. L. Coffman, and A. O’Garra, “Interleukin-10 and the interleukin-10 receptor,” Annual Reviews in Immunology, vol. 19, pp. 683–765, 2001. View at Publisher · View at Google Scholar · View at Scopus
  35. M. F. Miller and R. Loch-Caruso, “Comparison of LPS-stimulated release of cytokines in punch versus transwell tissue culture systems of human gestational membranes,” Reproductive Biology and Endocrinology, vol. 8, p. 121, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. W. T. Schaiff, M. G. Carlson, S. D. Smith, R. Levy, D. M. Nelson, and Y. Sadovsky, “Peroxisome proliferator-activated receptor-gamma modulates differentiation of human trophoblast in a ligand-specific manner,” Journal of Clinical Endocrinology and Metabolism, vol. 85, pp. 3874–3881, 2000. View at Publisher · View at Google Scholar
  37. Y. Barak, M. C. Nelson, E. S. Ong et al., “PPAR gamma is required for placental, cardiac, and adipose tissue development,” Molecular Cell, vol. 4, pp. 585–595, 1999. View at Google Scholar
  38. L. L. Waite, E. C. Person, Y. Zhou, K. H. Lim, T. S. Scanlan, and R. N. Taylor, “Placental peroxisome proliferator-activated receptor-gamma is up-regulated by pregnancy serum,” Journal of Clinical Endocrinology & Metabolism, vol. 85, pp. 3808–3814, 2000. View at Publisher · View at Google Scholar
  39. F. Wieser, L. Waite, C. Depoix, and R. N. Taylor, “PPAR action in human placental development and pregnancy and its complications,” PPAR Research, vol. 2008, Article ID 527048, 14 pages, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. H. Martin, “Role of PPAR-gamma in inflammation. Prospects for therapeutic intervention by food components,” Mutation Research, vol. 690, no. 1-2, pp. 57–63, 2010. View at Google Scholar
  41. F. P. McCarthy, S. Drewlo, F. A. English et al., “Evidence implicating peroxisome proliferator-activated receptor-γ in the pathogenesis of preeclampsia,” Hypertension, vol. 58, pp. 882–887, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. G. Mor and I. Cardenas, “The immune system in pregnancy: a unique complexity,” American Journal of Reproductive Immunology, vol. 63, pp. 425–433, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. R. W. Kelly, A. E. King, and H. O. Critchley, “Cytokine control in human endometrium,” Reproduction, vol. 121, pp. 3–19, 2001. View at Google Scholar
  44. M. S. van Mourik, N. S. Macklon, and C. J. Heijnen, “Embryonic implantation: cytokines, adhesion molecules, and immune cells in establishing an implantation environment,” Journal of Leukocyte Biology, vol. 85, no. 1, pp. 4–19, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. J. Hanna, D. Goldman-Wohl, Y. Hamani et al., “Decidual NK cells regulate key developmental processes at the human fetal-maternal interface,” Natural Medicines, vol. 12, pp. 1065–1074, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. S. Fest, P. B. Aldo, V. M. Abrahams et al., “Trophoblast-macrophage interactions: a regulatory network for the protection of pregnancy,” American Journal of Reproductive Immunology, vol. 57, pp. 55–66, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. Z. M. David Dong, A. C. Aplin, and R. F. Nicosia, “Regulation of angiogenesis by macrophages, dendritic cells, and circulating myelomonocytic cells,” Current Pharmaceutical Desigen, vol. 15, no. 4, pp. 365–379, 2009. View at Google Scholar
  48. V. Plaks, T. Birnberg, T. Berkutzki et al., “Uterine DCs are crucial for decidua formation during embryo implantation in mice,” Journal of Clinical Investigation, vol. 118, no. 12, pp. 3954–3965, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. T. Nagamatsu and D. J. Schust, “The immunomodulatory roles of macrophages at the maternal-fetal interface,” Reproductive Sciences, vol. 17, no. 3, pp. 209–218, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. R. Romero, J. Espinoza, J. P. Kusanovic et al., “The preterm parturition syndrome,” BJOG: An International Journal of Obstetrics and Gynecology, vol. 113, no. 3, pp. 17–42, 2006. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Sola, M. R. Rogido, and R. Deulofeut, “Oxygen as a neonatal health hazard: call for detente in clinical practice,” Acta Paediatrica, vol. 96, no. 6, pp. 801–812, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. G. Burton, H. W. Yung, T. Cindrova-Davies, and D. Charnock-Jones, “Placental endoplasmic reticulum stress and oxidative stress in the pathophysiology of unexplained intrauterine growth restriction and early onset preeclampsia,” Placenta, vol. 30, pp. 43–48, 2009. View at Google Scholar
  53. J. G. Eriksson, T. Forsen, J. Tuomilehto, P. D. Winter, C. Osmond, and D. J. Barker, “Catch-up growth in childhood and death from coronary heart disease: longitudinal study,” British Medical Journal, vol. 318, pp. 427–431, 1999. View at Google Scholar
  54. Z. J. Hagay, Y. Weiss, I. Zusman et al., “Prevention of diabetes-associated embryopathy by overexpression of the free radical scavenger copper zinc superoxide dismutase in transgenic mouse embryos,” American Journal of Obstetrics, & Gynecology, vol. 173, pp. 1036–1041, 1995. View at Google Scholar
  55. F. Lackman, V. Capewell, R. Gagnon, and B. Richardson, “Umbilical cord oxygen values and birth to placental weight ratio in relation to size at birth,” American Journal of Obstetrics and Gynecology, vol. 185, pp. 674–682, 2011. View at Publisher · View at Google Scholar · View at Scopus
  56. J. M. Soos, P. S. Subramaniam, A. C. Hobeika, J. Schiffenbauer, and H. M. Johnson, “The IFN pregnancy recognition hormone IFN-tau blocks both development and superantigen reactivation of experimental allergic encephalomyelitis without associated toxicity,” Journal of Immunology, vol. 155, pp. 2747–2753, 1995. View at Google Scholar
  57. H. C. Do-Umehara, C. Chen, D. Urich et al., “Suppression of inflammation and acute lung injury by Miz1 via repression of C/EBP-delta,” Nature Immunology, vol. 14, pp. 461–469, 2013. View at Publisher · View at Google Scholar · View at Scopus
  58. T. Cotechini, M. Komisarenko, A. Sperou, S. Macdonald-Goodfellow, M. A. Adams, and C. H. Graham, “Inflammation in rat pregnancy inhibits spiral artery remodeling leading to fetal growth restriction and features of preeclampsia,” Journal of Experimental Medicine, vol. 211, no. 1, pp. 165–179, 2014. View at Publisher · View at Google Scholar · View at Scopus
  59. J. Zhou, H. Miao, X. Li, Y. Hu, H. Sun, and Y. Hou, “Curcumin inhibits placental inflammation to ameliorate LPS-induced adverse pregnancy outcomes in mice via upregulation of phosphorylated Akt,” Inflammatory Research, vol. 66, no. 2, pp. 177–185, 2017. View at Publisher · View at Google Scholar · View at Scopus
  60. X. Xu, P. Yin, C. Wan et al., “Punicalagin inhibits inflammation in LPS-induced RAW264.7 macrophages via the suppression of TLR4-mediated MAPKs and NF-kappaB activation,” Inflammation, vol. 37, pp. 956–965, 2014. View at Publisher · View at Google Scholar · View at Scopus
  61. R. G. Osmers, B. C. Adelmann-Grill, W. Rath, H. W. Stuhlsatz, H. Tschesche, and W. Kuhn, “Biochemical events in cervical ripening dilatation during pregnancy and parturition,” Journal of Obstetrics and Gynecology, vol. 21, no. 2, pp. 185–194, 1995. View at Google Scholar
  62. J. C. Condon, P. Jeyasuria, J. M. Faust, and C. R. Mendelson, “Surfactant protein secreted by the maturing mouse fetal lung acts as a hormone that signals the initiation of parturition,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 14, pp. 4978–4983, 2004. View at Publisher · View at Google Scholar · View at Scopus
  63. W. Liu, C. Xu, X. You et al., “Hydrogen sulfide delays LPS-induced preterm birth in mice via anti-inflammatory pathways,” PLoS One, vol. 11, no. 4, article e0152838, 2016. View at Publisher · View at Google Scholar · View at Scopus
  64. D. A. MacIntyre, Y. S. Lee, R. Migale et al., “Protein 1 is a key terminal mediator of inflammation-induced preterm labor in mice,” Federation of American Societies of Experimental Biology Journal, vol. 28, pp. 2358–2368, 2014. View at Publisher · View at Google Scholar · View at Scopus
  65. M. Qin, R. Wang, C. Li, X. L. Liu, L. H. Qin, and H. P. Liu, “Establishment of decidual cell apoptotic models induced by tumor necrosis factor alpha and effects of baicalin on decidual cell apoptosis,” Journal of Clinical Rehabilitative Tissue Engineering Research, vol. 11, no. 19, pp. 3793–3796, 2007. View at Google Scholar
  66. D. A. Clark, J. Manuel, L. Lee, G. Chaouat, R. M. Gorczynski, and G. A. Levy, “Ecology of danger-dependent cytokine-boosted spontaneous abortion in the CBA x DBA/2 mouse model. I. Synergistic effect of LPS (TNF-α + IFN-γ) on pregnancy loss,” American Journal of Reproductive Immunology, vol. 52, no. 6, pp. 370–378, 2004. View at Publisher · View at Google Scholar
  67. S. Daher, K. Arruda Geraldes Denardi, M. H. Blotta et al., “Cytokines in recurrent pregnancy loss,” Journal of Reproductive Immunology, vol. 62, no. 1-2, pp. 151–157, 2004. View at Publisher · View at Google Scholar · View at Scopus
  68. X. Wang, Y. Zhao, and X. Zhong, “Protective effects of baicalin on decidua cells of LPS-induced mice abortion,” Journal of Immunology Research, vol. 2014, Article ID 859812, 6 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  69. J. S. Chua, A. M. Rofe, and P. Coyle, “Dietary zinc supplementation ameliorates LPS-induced teratogenicity in mice,” Pediatric Research, vol. 59, no. 3, pp. 355–358, 2006. View at Publisher · View at Google Scholar · View at Scopus
  70. T. M. Leazer, B. Barbee, M. Ebron-McCoy, G. A. Henry-Sam, and J. M. Rogers, “Role of the maternal acute phase response and tumor necrosis factor alpha in the developmental toxicity of lipopolysaccharide in the CD-1 mouse,” Reproductive Toxicology, vol. 16, pp. 173–179, 2002. View at Google Scholar
  71. H. Ning, H. Wang, L. Zhao et al., “Maternally-administered lipopolysaccharide (LPS) increases tumor necrosis factor alpha in fetal liver and fetal brain: its suppression by low-dose LPS pretreatment,” Toxicology Letters, vol. 176, pp. 13–19, 2008. View at Publisher · View at Google Scholar · View at Scopus
  72. H. Ashdown, Y. Dumont, M. Ng, S. Poole, P. Boksa, and G. N. Luheshi, “The role of cytokines in mediating effects of prenatal infection on the fetus: implications for schizophrenia,” Molecular Psychiatry, vol. 11, pp. 47–55, 2006. View at Publisher · View at Google Scholar · View at Scopus
  73. M. D. Shah and S. R. Shah, “Nutrient deficiencies in the premature infant,” Pediatric Clinics of North America, vol. 56, no. 5, pp. 1069–1083, 2009. View at Publisher · View at Google Scholar · View at Scopus
  74. N. G. Than, R. Romero, A. L. Tarca et al., “Mitochondrial manganese superoxide dismutase mRNA expression in human chorioamniotic membranes and its association with labor, inflammation, and infection,” Journal of Maternal and Fetal Neonatal Medicine, vol. 22, no. 11, pp. 1000–1013, 2009. View at Publisher · View at Google Scholar · View at Scopus
  75. J. Lorenz, E. Seebach, G. Hackmayer et al., “Melanocortin 1 receptor-signaling deficiency results in an articular cartilage phenotype and accelerates pathogenesis of surgically induced murine osteoarthritis,” PLoS One, vol. 9, no. 9, article e105858, 2014. View at Publisher · View at Google Scholar · View at Scopus
  76. J. F. Ge, Y. Ji, and Y. Zhang, “Clinical analysis of 81 premature infants with early-onset sepsis,” Chinese Journal of Practical Medicine, vol. 43, no. 17, pp. 77–79, 2016. View at Google Scholar
  77. S. P. Zhen, S. Lu, and Z. H. Wang, “Review on screening of cervical lesions and pregnancy outcome by using liquid based cytology and HPV joint fractal detection in gestation period,” Chinese Foreign Medical Research, vol. 14, no. 11, pp. 44-45, 2016. View at Google Scholar
  78. C. Y. Yuan, “Analysis the effect of diabetes in gestation period on puerperal and newborn,” Women's Health Research, vol. 11, no. 14, p. 230, 2016. View at Google Scholar
  79. Y. Z. Guo, P. He, and A. M. Feng, “Effect of curcumin on expressions of NF-kBp65, TNF-a and IL-8 in placental tissue of premature birth of infected mice,” Asian Pacific Journal of Tropical Medicine, vol. 10, no. 2, pp. 175–178, 2017. View at Publisher · View at Google Scholar
  80. American College of Obstetricians and Gynecologists, “Hypertension in pregnancy: report of the American College of Obstetricians and Gynecologists’ task force on hypertension in pregnancy,” Obstetrics and Gynecology, vol. 122, p. 1122, 2013. View at Publisher · View at Google Scholar · View at Scopus
  81. C. W. Redman and I. L. Sargent, “Latest advances in understanding preeclampsia,” Science, vol. 308, pp. 1592–1594, 2005. View at Publisher · View at Google Scholar · View at Scopus
  82. J. M. Roberts and C. A. Hubel, “Oxidative stress in preeclampsia,” American Journal of Obstetrics and Gynecology, vol. 190, pp. 1177-1178, 2004. View at Publisher · View at Google Scholar · View at Scopus
  83. G. J. Burton, H. W. Yung, T. Cindrova-Davies, and D. S. Charnock-Jones, “Placental endoplasmic reticulum stress and oxidative stress in the pathophysiology of unexplained intrauterine growth restriction and early onset preeclampsia,” Placenta, vol. 30, pp. 43–48, 2009. View at Google Scholar
  84. J. M. Roberts and C. A. Hubel, “Is oxidative stress the link in the two-stage model of pre-eclampsia?” Lancet, vol. 354, pp. 788-789, 1999. View at Publisher · View at Google Scholar · View at Scopus
  85. X. J. Liu, B. W. Wang, M. Zhao et al., “Effects of maternal LPS exposure during pregnancy on metabolic phenotypes in female offspring,” PLoS One, vol. 9, no. 12, article e114780, 2014. View at Publisher · View at Google Scholar · View at Scopus
  86. P. Saenger, P. Czernichow, I. Hughes, and E. O. Reiter, “Small for gestational age: short stature and beyond,” Endocrine Reviews, vol. 28, pp. 219–251, 2007. View at Publisher · View at Google Scholar · View at Scopus
  87. Y. Seki, L. Williams, P. M. Vuguin, and M. J. Charron, “Minireview: epigenetic programming of diabetes and obesity: animal models,” Endocrinology, vol. 153, pp. 1031–1038, 2012. View at Publisher · View at Google Scholar · View at Scopus
  88. V. V. Bol, A. I. Delattre, B. Reusens, M. Raes, and C. Remacle, “Forced catch-up growth after fetal protein restriction alters the adipose tissue gene expression program leading to obesity in adult mice,” American Journal of Physiology and Regulatory Integrative and Comparative Physiology, vol. 297, pp. R291–R299, 2009. View at Publisher · View at Google Scholar · View at Scopus
  89. U. Kamath, G. Rao, S. U. Kamath, and L. Rai, “Maternal and fetal indicators of oxidative stress during intrauterine growth retardation (IUGR),” Indian Journal of Clinical Biochemistry, vol. 21, pp. 111–115, 2006. View at Publisher · View at Google Scholar · View at Scopus
  90. Z. Hracsko, H. Orvos, Z. Novak, A. Pal, and I. S. Varga, “Evaluation of oxidative stress markers in neonates with intra-uterine growth retardation,” Redox Reports, vol. 13, pp. 11–16, 2008. View at Publisher · View at Google Scholar · View at Scopus
  91. S. J. Chapple, X. Cheng, and G. E. Mann, “Effects of 4-hydroxynonenal on vascular endothelial and smooth muscle cell redox signaling and function in health and disease,” Redox Biology, vol. 1, pp. 319–331, 2013. View at Publisher · View at Google Scholar · View at Scopus
  92. S. J. Chapple, R. C. Siow, and G. E. Mann, “Crosstalk between Nrf2 and the proteasome: therapeutic potential of Nrf2 inducers in vascular disease and aging,” International Journal of Biochemistry and Cellular Biology, vol. 44, pp. 1315–1320, 2012. View at Publisher · View at Google Scholar · View at Scopus
  93. T. Ishii, K. Itoh, E. Ruiz et al., “Role of Nrf2 in the regulation of CD36 and stress protein expression in murine macrophages: activation by oxidatively modified LDL and 4-hydroxynonenal,” Circulatory Research, vol. 94, pp. 609–616, 2004. View at Publisher · View at Google Scholar · View at Scopus
  94. S. B. Cullinan, J. D. Gordan, J. Jin, J. W. Harper, and J. A. Diehl, “The Keap1-BTB protein is an adaptor that bridges Nrf2 to a Cul3-based E3 ligase: oxidative stress sensing by a Cul3-Keap1 ligase,” Molecular and Cellular Biology, vol. 24, pp. 8477–8486, 2004. View at Publisher · View at Google Scholar · View at Scopus
  95. K. Taguchi, H. Motohashi, and M. Yamamoto, “Molecular mechanisms of the Keap1-Nrf2 pathway in stress response and cancer evolution,” Genes to Cells, vol. 16, pp. 123–140, 2011. View at Publisher · View at Google Scholar · View at Scopus
  96. A. T. Dinkova-Kostova and P. Talalay, “NAD(P)H:quinone acceptor oxidoreductase 1 (NQO1), a multifunctional antioxidant enzyme and exceptionally versatile cytoprotector,” Archives of Biochemistry and Biophysics, vol. 501, pp. 116–123, 2010. View at Publisher · View at Google Scholar · View at Scopus
  97. R. C. Siow, H. Sato, and G. E. Mann, “Heme oxygenase-carbon monoxide signalling pathway in atherosclerosis: anti-atherogenic actions of bilirubin and carbon monoxide?” Cardiovascular Research, vol. 41, pp. 385–394, 1999. View at Google Scholar
  98. C. C. Franklin, D. S. Backos, I. Mohar, C. C. White, H. J. Forman, and T. J. Kavanagh, “Structure, function, and post-translational regulation of the catalytic and modifier subunits of glutamate cysteine ligase,” Molecular Aspects of Medicine, vol. 30, pp. 86–98, 2009. View at Publisher · View at Google Scholar · View at Scopus
  99. H. Sato, M. Tamba, K. Kuriyama-Matsumura, S. Okuno, and S. Bannai, “Molecular cloning and expression of human xCT, the light chain of amino acid transport system xc,” Antioxidant and Redox Signaling, vol. 2, pp. 665–671, 2000. View at Publisher · View at Google Scholar
  100. L. E. Tebay, S. T. Durant, S. R. Vitale, T. Penning, A. T. Dinkova-Kostova, and J. D. Hayes, “Mechanisms of activation of the transcription factor Nrf2 by redox stressors, nutrient cues, and energy status and the pathways through it attenuates degenerative disease,” Free Radicals Biology and Medicines, vol. 88, pp. 108–146, 2015. View at Google Scholar
  101. N. Kweider, J. Lambertz, T. Pufe, C. J. Wruck, and W. Rath, “[125-POS]: Nrf2 deficiency interferes with trophoblast differentiation and affects the placental development in mice,” Pregnancy Hypertension, vol. 5, pp. 66-67, 2015. View at Publisher · View at Google Scholar
  102. A. Ramkissoon and P. G. Wells, “Developmental role of nuclear factor E2-related factor 2 in mitigating methamphetamine fetal toxicity and postnatal neurodevelopmental deficits,” Free Radical Biology & Medicine, vol. 65, pp. 620–631, 2013. View at Publisher · View at Google Scholar · View at Scopus
  103. A. Zheng, H. Li, K. Cao et al., “Maternal hydroxytyrosol administration improves neurogenesis and cognitive function in prenatally stressed offspring,” Journal of Nutritional Biochemistry, vol. 26, pp. 190–199, 2015. View at Publisher · View at Google Scholar · View at Scopus
  104. X. Chen, J. Liu, and S. Y. Chen, “Sulforaphane protects against ethanol-induced oxidative stress and apoptosis in neural crest cells by the induction of Nrf2-mediated antioxidant response,” British Journal of Pharmacology, vol. 169, pp. 437–448, 2013. View at Publisher · View at Google Scholar · View at Scopus
  105. F. Lin, X. Yu, X. Zhang et al., “A synthetic analog of lipoxin A4 partially alleviates dexamethasone-induced fetal growth restriction in rats,” Placenta, vol. 34, pp. 941–948, 2013. View at Publisher · View at Google Scholar · View at Scopus
  106. A. J. Huebner, D. Dai, M. Morasso et al., “Amniotic fluid activates the Nrf2/keap1 pathway to repair an epidermal barrier defect in utero,” Developmental Cell, vol. 23, pp. 1238–1246, 2012. View at Publisher · View at Google Scholar · View at Scopus
  107. P. Wentzel and U. J. Eriksson, “Altered gene expression in rat cranial neural crest cells exposed to a teratogenic glucose concentration in vitro: paradoxical downregulation of antioxidative defense genes,” Birth Defects Research Part B, Developmental and Reproductive Toxicology, vol. 92, pp. 487–497, 2011. View at Publisher · View at Google Scholar · View at Scopus
  108. S. Y. Chang, Y. W. Chen, X. P. Zhao et al., “Catalase prevents maternal diabetes-induced perinatal programming via the Nrf2-HO-1 defense system,” Diabetes, vol. 61, pp. 2565–2574, 2012. View at Publisher · View at Google Scholar · View at Scopus
  109. N. Acar, H. Soylu, I. Edizer et al., “Expression of nuclear factor erythroid 2-related factor 2 (Nrf2) and peroxiredoxin 6 (Prdx6) proteins in healthy and pathologic placentas of human and rat,” Acta Histochemica, vol. 116, pp. 1289–1300, 2014. View at Publisher · View at Google Scholar · View at Scopus
  110. Y. Chigusa, K. Tatsumi, E. Kondoh et al., “Decreased lectin-like oxidized LDL receptor 1 (LOX-1) and low Nrf2 activation in placenta are involved in preeclampsia,” Journal of Clinical Endocrinology and Metabolism, vol. 97, pp. E1862–E1870, 2012. View at Publisher · View at Google Scholar · View at Scopus
  111. A. Maebayashi Asanuma, T. Yamamoto, H. Azuma et al., “Expression of placenta growth factor, soluble fms-like tyrosine kinase-1, metal-responsive transcription factor-1, heme oxygenase 1 and hypoxia inducible factor-1alpha mRNAs in pre-eclampsia placenta and the effect of pre-eclampsia sera on their expression of choriocarcinoma cells,” The Journal of Obstetrics and Gynaecology Research, vol. 40, pp. 2095–2103, 2014. View at Publisher · View at Google Scholar · View at Scopus
  112. X. Cheng, S. J. Chapple, B. Patel et al., “Gestational diabetes mellitus impairs Nrf2-mediated adaptive antioxidant defenses and redox signaling in fetal endothelial cells in utero,” Diabetes, vol. 62, pp. 4088–4097, 2013. View at Publisher · View at Google Scholar · View at Scopus
  113. A. Zheng, H. Li, K. Cao et al., “Maternal hydroxytyrosol administration improves neurogenesis and cognitive function in prenatally stressed offspring,” Journal of Nutritional Biochemistry, vol. 26, pp. 190–199, 2015. View at Publisher · View at Google Scholar · View at Scopus
  114. Y. J. Wan, Y. Y. Li, W. Xia et al., “Alterations in tumor biomarker GSTP gene methylation patterns induced by prenatal exposure to PFOS,” Toxicology, vol. 274, pp. 57–64, 2010. View at Publisher · View at Google Scholar · View at Scopus
  115. S. A. McGrath-Morrow, T. Lauer, J. M. Collaco et al., “Transcriptional responses of neonatal mouse lung to hyperoxia by Nrf2 status,” Cytokine, vol. 65, pp. 4–9, 2014. View at Publisher · View at Google Scholar · View at Scopus
  116. J. Dong, K. K. Sulik, and S. Y. Chen, “Nrf2-mediated transcriptional induction of antioxidant response in mouse embryos exposed to ethanol in vivo: implications for the prevention of fetal alcohol spectrum disorders,” Antioxidants and Redox Signaling, vol. 10, pp. 2023–2033, 2008. View at Publisher · View at Google Scholar · View at Scopus
  117. C. Harris and J. M. Hansen, “Nrf2-mediated resistance to oxidant-induced redox disruption in embryos,” Birth Defects Research Part B, Developmental Reproductive Toxicology, vol. 95, pp. 213–218, 2012. View at Publisher · View at Google Scholar · View at Scopus
  118. G. Agati, E. Azzarell, S. Pollastri, and M. Tattini, “Flavonoids as antioxidants in plants: location and functional significance,” Plant Science, vol. 196, pp. 67–76, 2012. View at Publisher · View at Google Scholar · View at Scopus
  119. P. V. Babu, D. Liu, and E. R. Gilbert, “Recent advances in understanding the anti-diabetic actions of dietary flavonoids,” Journal of Nutritional Biochemistry, vol. 24, pp. 1777–1789, 2013. View at Publisher · View at Google Scholar · View at Scopus
  120. W. Jiang, H. Wei, and B. He, “Dietary flavonoids intake and the risk of coronary heart disease: a dose-response meta-analysis of 15 prospective studies,” Thrombosis Research, vol. 135, pp. 459–463, 2015. View at Publisher · View at Google Scholar · View at Scopus
  121. S. Venturelli, M. Burkard, M. Biendl, U. M. Lauer, J. Frank, and C. Busch, “Prenylated chalcones and flavonoids for the prevention and treatment of cancer,” Nutrition, vol. 32, no. 11-12, pp. 1171–1178, 2016. View at Publisher · View at Google Scholar · View at Scopus
  122. V. Kumar, A. K. Abbas, N. Fausto, and R. N. Mitchell, Robbins Basic Pathology, Elsevier Health Sciences, Philadephia, PA, USA, 2012.
  123. M. Proell, S. J. Riedl, J. H. Fritz, A. M. Rojas, and R. Schwarzenbacher, “The nod-like receptor (NLR) family: a tale of similarities and differences,” PLoS One, vol. 3, p. 921, 2008. View at Publisher · View at Google Scholar · View at Scopus
  124. T. Cotechini, M. Komisarenko, A. Sperou, S. Macdonald-Goodfellow, M. A. Adams, and C. H. Graham, “Inflammation in rat pregnancy inhibits spiral artery remodeling leading to fetal growth restriction and features of preeclampsia,” Journal of Experimental Medicine, vol. 211, no. 1, pp. 165–179, 2014. View at Publisher · View at Google Scholar · View at Scopus
  125. A. Sharma, A. Satyam, and J. B. Sharma, “Leptin, IL-10 and inflammatory markers (TNF-a, IL-6 and IL-8) in pre-eclamptic, normotensive pregnant and healthy non-pregnant women,” American Journal of Reproductive Immunology, vol. 58, pp. 21–30, 2007. View at Publisher · View at Google Scholar · View at Scopus
  126. R. L. Prior, L. Gu, X. Wu et al., “Plasma antioxidant capacity changes following a meal as a measure of the ability of a food to alter in vivo antioxidant status,” Journal of American College of Nutrition, vol. 26, pp. 170–181, 2007. View at Google Scholar
  127. Y. H. Chen, M. Zhao, X. Chen et al., “Zinc supplementation during pregnancy protects against lipopolysaccharide-induced fetal growth restriction and demise through its anti-inflammatory effect,” Journal of Immunology, vol. 189, pp. 454–463, 2012. View at Publisher · View at Google Scholar · View at Scopus
  128. S. Kumar and A. K. Pandey, “Chemistry and biological activities of flavonoids: an overview,” Scientific World Journal, vol. 2013, Article ID 162750, 16 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  129. Y. L. Lin, C. Y. Cheng, Y. P. Lin, Y. W. Lau, I. M. Juan, and J. K. Lin, “Hypolipidemic effect of green tea leaves through induction of antioxidant and phase II enzymes including superoxide dismutase, catalase, and glutathione-S-transferase in rats,” Journal of Agriculture and Food Chemistry, vol. 46, pp. 1893–1899, 1998. View at Publisher · View at Google Scholar · View at Scopus
  130. K. H. Al-Gubory, P. A. Fowler, and C. Garrel, “The roles of cellular reactive oxygen species, oxidative stress and antioxidants in pregnancy outcomes,” International Journal of Biochemistry and Cellular Biology, vol. 42, no. 10, pp. 1634–1650, 2010. View at Publisher · View at Google Scholar · View at Scopus
  131. K. Vanhees, F. J. van Schooten, S. B. van Waalwijk van Doorn-Khosrovani et al., “Intrauterine exposure to flavonoids modifies antioxidant status at adulthood and decreases oxidative stress-induced DNA damage,” Free Radicals Biology and Medicine, vol. 57, pp. 154–161, 2013. View at Publisher · View at Google Scholar · View at Scopus
  132. J. D. Hartley, B. J. Ferguson, and A. Moffett, “The role of shed placental DNA in the systemic inflammatory syndrome of preeclampsia,” American Journal of Obstetrics and Gynecology, vol. 213, no. 3, pp. 268–277, 2015. View at Publisher · View at Google Scholar · View at Scopus
  133. V. Shalini, C. K. Pushpan, G. Sindhu, and A. Helen, “Tricin, flavonoid from Njavara reduces inflammatory responses in hPBMCs by modulating the p38MAPK and PI3K/Akt pathway and prevents inflammation associated endothelial dysfunction in HUVECs,” Immunobiology, vol. 221, no. 2, pp. 137–144, 2016. View at Publisher · View at Google Scholar · View at Scopus
  134. G. Scapagnini, V. Sonya, A. G. Nader, C. Calogero, D. Zella, and G. Fabio, “Modulation of Nrf2/ARE pathway by food polyphenols: a nutritional neuroprotective strategy for cognitive and neurodegenerative disorders,” Molecular Neurobiology, vol. 44, no. 2, pp. 192–201, 2011. View at Publisher · View at Google Scholar · View at Scopus
  135. H. K. Na, E. H. Kim, J. H. Jung, H. H. Lee, J. W. Hyun, and Y. J. Surh, “(−)-Epigallocatechin gallate induces Nrf2-mediated antioxidant enzyme expression via activation of PI3K and ERK in human mammary epithelial cells,” Archives of Biochemistry and Biophysics, vol. 476, pp. 171–177, 2008. View at Publisher · View at Google Scholar · View at Scopus
  136. X. Wang, A. Ma, W. Shi, M. Geng, X. Zhong, and Y. Zhao, “Quercetin and bornyl acetate regulate T-lymphocyte subsets and INF-/IL-4 ratio in utero in pregnant mice,” Evidence-Based Complementary and Alternative Medicine, vol. 2011, Article ID 745262, 7 pages, 2011. View at Publisher · View at Google Scholar · View at Scopus
  137. X. H. Zhong, W. Y. Shi, A. T. Ma et al., “Effects of Radix Scutellariae and Rhizoma Atractylodis on LPS-induced abortion and the uterine IL-10 contents in mice,” American Journal of Chinese Medicine, vol. 36, pp. 141–148, 2008. View at Publisher · View at Google Scholar · View at Scopus
  138. C. Li, G. Lin, and Z. Zuo, “Pharmacological effects and pharmacokinetics properties of Radix Scutellariae and its bioactive flavones,” Biopharmaceutics & Drug Disposition, vol. 32, no. 8, pp. 427–445. View at Publisher · View at Google Scholar · View at Scopus
  139. X. Zhong and Y. Zhao, “Anti-abortive effects of Bao Tai Wu You, Tai Shan Pan Shi and Bai Zhu San in a murine mode,” American Journal of Traditional Chinese Veterinary Medicine, vol. 8, no. 2, 2013. View at Google Scholar