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Oxidative Medicine and Cellular Longevity Volume 2019 ,2019-10-01
Maternal Diet-Induced Obesity Compromises Oxidative Stress Status and Angiogenesis in the Porcine Placenta by Upregulating Nox2 Expression
Research Article
Chengjun Hu 1 Yunyu Yang 1 Jiaying Li 1 Hao Wang 1 Chuanhui Cheng 1 Linfang Yang 2 Qiqi Li 1 Jinping Deng 1 , 3 Zuman Liang 4 Yulong Yin 1 , 5 Zhengjun Xie 6 Chengquan Tan 1 , 3
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DOI:10.1155/2019/2481592
Received 2019-03-11, accepted for publication 2019-07-18, Published 2019-07-18
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摘要

Maternal obesity is associated with placental oxidative stress. However, the mechanism underlying this association remains poorly understood. In the present study, a gilt obesity model was developed by exposure to different energy diets and used to investigate the role of NADPH oxidase 2 (Nox2) in the placenta. Specifically, 99 gilts (Guangdong Small-ear Spotted pig) at day 60 of gestation were randomly assigned to one of the following three treatments: low-energy group (L, DE=11.50 MJ/kg), medium-energy group (M, DE=12.41 MJ/kg), and high-energy group (H, DE=13.42 MJ/kg), with 11 replicate pens per treatment and 3 gilts per pen. At the start of the study, maternal body weight and backfat thickness were not significantly different in the three treatments. After the study, data indicated that the H group had higher body weight and backfat thickness gain for gilts during gestation and lower piglet birth weight compared with the other two groups. Additionally, the H group showed glucolipid metabolic disorders and increased triglyceride and nonesterified fatty acid contents in the placenta of gilts. Compared with the L group, the H group exhibited lower mitochondrial biogenesis and increased oxidative damage in the placenta. Importantly, increased mRNA expression and protein abundance of Nox2 were observed for the first time in H group placentae. Furthermore, compared with the L group, the H group showed a decrease in the density of placental vessels and the protein levels of vascular endothelial cadherin (VE-cadherin), vascular endothelial growth factor A (VEGF-A), and phosphorylation of vascular endothelial growth factor receptor 2 (p-VEGFR2) as well as the immunostaining intensity of platelet endothelial cell adhesion molecule-1 (CD31). Our findings suggest that maternal high-energy diet-induced obesity increases placental oxidative stress and decreases placental angiogenesis possibly through the upregulation of Nox2.

授权许可

Copyright © 2019 Chengjun Hu et al. 2019
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.

通讯作者

1. Yulong Yin.Guangdong Provincial Key Laboratory of Animal Nutrition Control, Institute of Subtropical Animal Nutrition and Feed, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong 510642, China, scau.edu.cn;National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, Hunan 410125, China, cas.cn.yinyulong@isa.ac.cn
2. Chengquan Tan.Guangdong Provincial Key Laboratory of Animal Nutrition Control, Institute of Subtropical Animal Nutrition and Feed, College of Animal Science, South China Agricultural University, Guangzhou, Guangdong 510642, China, scau.edu.cn;College of Animal Science and National Engineering Research Center for Breeding Swine Industry, South China Agricultural University, Guangzhou, Guangdong 510642, China, scau.edu.cn.tanchengquan@scau.edu.cn

推荐引用方式

Chengjun Hu,Yunyu Yang,Jiaying Li,Hao Wang,Chuanhui Cheng,Linfang Yang,Qiqi Li,Jinping Deng,Zuman Liang,Yulong Yin,Zhengjun Xie,Chengquan Tan. Maternal Diet-Induced Obesity Compromises Oxidative Stress Status and Angiogenesis in the Porcine Placenta by Upregulating Nox2 Expression. Oxidative Medicine and Cellular Longevity ,Vol.2019(2019)

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参考文献
[1] M. Chen, R. E. Lacey. (2018). Adverse childhood experiences and adult inflammation: findings from the 1958 British birth cohort. Brain, Behavior, and Immunity.69:582-590. DOI: 10.1016/S0140-6736(14)60460-8.
[2] S.-I. Shimizu, M. Nomoto, T. Yamamoto, K. Momose. et al.(1994). Reduction by N-nitro-L-arginine of HO-induced endothelial cell injury. British Journal of Pharmacology.113(2):564-568. DOI: 10.1016/S0140-6736(14)60460-8.
[3] K. A. Vonnahme, S. P. Ford. (2004). Differential expression of the vascular endothelial growth factor-receptor system in the gravid uterus of Yorkshire and Meishan pigs. Biology of Reproduction.71(1):163-169. DOI: 10.1016/S0140-6736(14)60460-8.
[4] C. Tan, H. Wei, J. Ao, G. Long. et al.(2016). Inclusion of konjac flour in the gestation diet changes the gut microbiota, alleviates oxidative stress, and improves insulin sensitivity in sows. Applied and Environmental Microbiology.82(19):5899-5909. DOI: 10.1016/S0140-6736(14)60460-8.
[5] M. Ng, T. Fleming, M. Robinson, B. Thomson. et al.(2014). Global, regional, and national prevalence of overweight and obesity in children and adults during 1980-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet.384(9945):766-781. DOI: 10.1016/S0140-6736(14)60460-8.
[6] H. Yang, D. Fu, H. Shao, X. Kong. et al.(2012). Impacts of birth weight on plasma, liver and skeletal muscle neutral amino acid profiles and intestinal amino acid transporters in suckling Huanjiang mini-piglets. PLoS One.7(12, article e50921). DOI: 10.1016/S0140-6736(14)60460-8.
[7] C. Tan, H. Wei, H. Sun, J. Ao. et al.(2015). Effects of dietary supplementation of oregano essential oil to sows on oxidative stress status, lactation feed intake of sows, and piglet performance. BioMed Research International.2015-9. DOI: 10.1016/S0140-6736(14)60460-8.
[8] B. Tan, Y. Yin, Z. Liu, W. Tang. et al.(2011). Dietary L-arginine supplementation differentially regulates expression of lipid-metabolic genes in porcine adipose tissue and skeletal muscle. Journal of Nutritional Biochemistry.22(5):441-445. DOI: 10.1016/S0140-6736(14)60460-8.
[9] P. Gonzalez-Añover, T. Encinas, L. Torres-Rovira, P. Pallares. et al.(2011). Ovulation rate, embryo mortality and intrauterine growth retardation in obese swine with gene polymorphisms for leptin and melanocortin receptors. Theriogenology.75(1):34-41. DOI: 10.1016/S0140-6736(14)60460-8.
[10] F. Violi, P. Pignatelli, C. Pignata, A. Plebani. et al.(2013). Reduced atherosclerotic burden in subjects with genetically determined low oxidative stress. Arteriosclerosis, Thrombosis, and Vascular Biology.33(2):406-412. DOI: 10.1016/S0140-6736(14)60460-8.
[11] Y. Zhou, T. Xu, A. Cai, Y. Wu. et al.(2018). Excessive backfat of sows at 109 d of gestation induces lipotoxic placental environment and is associated with declining reproductive performance. Journal of Animal Science.96(1):250-257. DOI: 10.1016/S0140-6736(14)60460-8.
[12] F. Violi, V. Sanguigni, R. Carnevale, A. Plebani. et al.(2009). Hereditary deficiency of gp91 is associated with enhanced arterial dilatation: results of a multicenter study. Circulation.120(16):1616-1622. DOI: 10.1016/S0140-6736(14)60460-8.
[13] C. M. Lynch, D. A. Kinzenbaw, X. Chen, S. Zhan. et al.(2013). Nox2-derived superoxide contributes to cerebral vascular dysfunction in diet-induced obesity. Stroke.44(11):3195-3201. DOI: 10.1016/S0140-6736(14)60460-8.
[14] Y. H. Zhang, D. W. Wang, S. F. Xu, S. Zhang. et al.(2018). -Lipoic acid improves abnormal behavior by mitigation of oxidative stress, inflammation, ferroptosis, and tauopathy in P301S tau transgenic mice. Redox Biology.14:535-548. DOI: 10.1016/S0140-6736(14)60460-8.
[15] C. Liang, K. DeCourcy, M. R. Prater. (2010). High-saturated-fat diet induces gestational diabetes and placental vasculopathy in C57BL/6 mice. Metabolism.59(7):943-950. DOI: 10.1016/S0140-6736(14)60460-8.
[16] N. Parajuli, V. B. Patel, W. Wang, R. Basu. et al.(2014). Loss of NOX2 (gp91) prevents oxidative stress and progression to advanced heart failure. Clinical Science.127(5):331-340. DOI: 10.1016/S0140-6736(14)60460-8.
[17] T. Zou, B. Yu, J. Yu, X. Mao. et al.(2016). Moderately decreased maternal dietary energy intake during pregnancy reduces fetal skeletal muscle mitochondrial biogenesis in the pigs. Genes & Nutrition.11(1). DOI: 10.1016/S0140-6736(14)60460-8.
[18] K. M. Godfrey, R. M. Reynolds, S. L. Prescott, M. Nyirenda. et al.(2017). Influence of maternal obesity on the long-term health of offspring. The Lancet Diabetes & Endocrinology.5(1):53-64. DOI: 10.1016/S0140-6736(14)60460-8.
[19] N. J. Sebire, M. Jolly, J. P. Harris, J. Wadsworth. et al.(2001). Maternal obesity and pregnancy outcome: a study of 287,213 pregnancies in London. International Journal of Obesity and Related Metabolic Disorders.25(8):1175-1182. DOI: 10.1016/S0140-6736(14)60460-8.
[20] M. S. Baker, G. Li, J. J. Kohorst, R. A. Waterland. et al.(2015). Fetal growth restriction promotes physical inactivity and obesity in female mice. International Journal of Obesity.39(1):98-104. DOI: 10.1016/S0140-6736(14)60460-8.
[21] J. L. Rains, S. K. Jain. (2011). Oxidative stress, insulin signaling, and diabetes. Free Radical Biology & Medicine.50(5):567-575. DOI: 10.1016/S0140-6736(14)60460-8.
[22] C. Bonnard, A. Durand, S. Peyrol, E. Chanseaume. et al.(2008). Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice. Journal of Clinical Investigation.118(2):789-800. DOI: 10.1016/S0140-6736(14)60460-8.
[23] X. Zhou, L. He, S. Zuo, Y. Zhang. et al.(2018). Serine prevented high-fat diet-induced oxidative stress by activating AMPK and epigenetically modulating the expression of glutathione synthesis-related genes. Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease.1864(2):488-498. DOI: 10.1016/S0140-6736(14)60460-8.
[24] I. Dalle-Donne, R. Rossi, D. Giustarini, A. Milzani. et al.(2003). Protein carbonyl groups as biomarkers of oxidative stress. Clinica Chimica Acta.329(1-2):23-38. DOI: 10.1016/S0140-6736(14)60460-8.
[25] E. Jarvie, S. Hauguel-de-Mouzon, S. M. Nelson, N. Sattar. et al.(2010). Lipotoxicity in obese pregnancy and its potential role in adverse pregnancy outcome and obesity in the offspring. Clinical Science.119(3):123-129. DOI: 10.1016/S0140-6736(14)60460-8.
[26] S. Furukawa, T. Fujita, M. Shimabukuro, M. Iwaki. et al.(2004). Increased oxidative stress in obesity and its impact on metabolic syndrome. The Journal of Clinical Investigation.114(12):1752-1761. DOI: 10.1016/S0140-6736(14)60460-8.
[27] N. Suematsu, H. Tsutsui, J. Wen, D. Kang. et al.(2003). Oxidative stress mediates tumor necrosis factor--induced mitochondrial DNA damage and dysfunction in cardiac myocytes. Circulation.107(10):1418-1423. DOI: 10.1016/S0140-6736(14)60460-8.
[28] J. Mele, S. Muralimanoharan, A. Maloyan, L. Myatt. et al.(2014). Impaired mitochondrial function in human placenta with increased maternal adiposity. American Journal of Physiology Endocrinology and Metabolism.307(5):E419-E425. DOI: 10.1016/S0140-6736(14)60460-8.
[29] T. Song, J. Lu, Z. Deng, T. Xu. et al.(2018). Maternal obesity aggravates the abnormality of porcine placenta by increasing N6-methyladenosine. International Journal of Obesity.42(10):1812-1820. DOI: 10.1016/S0140-6736(14)60460-8.
[30] J. E. Kokoszka, P. Coskun, L. A. Esposito, D. C. Wallace. et al.(2001). Increased mitochondrial oxidative stress in the Sod2 (+/-) mouse results in the age-related decline of mitochondrial function culminating in increased apoptosis. Proceedings of the National Academy of Sciences of the United States of America.98(5):2278-2283. DOI: 10.1016/S0140-6736(14)60460-8.
[31] P. Haddad, S. Dussault, J. Groleau, J. Turgeon. et al.(2011). Nox2-derived reactive oxygen species contribute to hypercholesterolemia-induced inhibition of neovascularization: effects on endothelial progenitor cells and mature endothelial cells. Atherosclerosis.217(2):340-349. DOI: 10.1016/S0140-6736(14)60460-8.
[32] H. Liu, J. Wang, Y. Chen, Y. Chen. et al.(2017). NPC-EXs alleviate endothelial oxidative stress and dysfunction through the miR-210 downstream Nox2 and VEGFR2 pathways. Oxidative Medicine and Cellular Longevity.2017-11. DOI: 10.1016/S0140-6736(14)60460-8.
[33] Y. Takagi, T. Nikaido, T. Toki, N. Kita. et al.(2004). Levels of oxidative stress and redox-related molecules in the placenta in preeclampsia and fetal growth restriction. Virchows Archiv.444(1):49-55. DOI: 10.1016/S0140-6736(14)60460-8.
[34] S. Pitkanen, B. H. Robinson. (1996). Mitochondrial complex I deficiency leads to increased production of superoxide radicals and induction of superoxide dismutase. Journal of Clinical Investigation.98(2):345-351. DOI: 10.1016/S0140-6736(14)60460-8.
[35] D. S. Torry, M. Hinrichs, R. J. Torry. (2004). Determinants of placental vascularity. American Journal of Reproductive Immunology.51(4):257-268. DOI: 10.1016/S0140-6736(14)60460-8.
[36] Y. W. Kim, T. V. Byzova. (2014). Oxidative stress in angiogenesis and vascular disease. Blood.123(5):625-631. DOI: 10.1016/S0140-6736(14)60460-8.
[37] R. M. Reynolds, K. M. Allan, E. A. Raja, S. Bhattacharya. et al.(2013). Maternal obesity during pregnancy and premature mortality from cardiovascular event in adult offspring: follow-up of 1 323 275 person years. BMJ.347:f4539. DOI: 10.1016/S0140-6736(14)60460-8.
[38] T. Nishikawa, D. Kukidome, K. Sonoda, K. Fujisawa. et al.(2007). Impact of mitochondrial ROS production on diabetic vascular complications. Diabetes Research and Clinical Practice.77(3):S41-S45. DOI: 10.1016/S0140-6736(14)60460-8.
[39] T. J. Stuart, K. O’Neill, D. Condon, I. Sasson. et al.(2018). Diet-induced obesity alters the maternal metabolome and early placenta transcriptome and decreases placenta vascularity in the mouse. Biology of Reproduction.98(6):795-809. DOI: 10.1016/S0140-6736(14)60460-8.
[40] H. Yang, F. Li, X. Kong, X. Yuan. et al.(2012). Molecular cloning, tissue distribution and ontogenetic expression of Xiang pig chemerin and its involvement in regulating energy metabolism through Akt and ERK1/2 signaling pathways. Molecular Biology Reports.39(2):1887-1894. DOI: 10.1016/S0140-6736(14)60460-8.
[41] C. Chen, Z. Wang, J. Li, Y. Li. et al.(2019). Dietary vitamin E affect small intestinal histomorphology, digestive enzyme activity and the expression of nutrient transporters by inhibiting proliferation of intestinal epithelial cells within jejunum in weaned piglets. Journal of Animal Science.97(3):1212-1221. DOI: 10.1016/S0140-6736(14)60460-8.
[42] K. A. Vonnahme, M. E. Wilson, S. P. Ford. (2001). Relationship between placental vascular endothelial growth factor expression and placental/endometrial vascularity in the pig. Biology of Reproduction.64(6):1821-1825. DOI: 10.1016/S0140-6736(14)60460-8.
[43] P. Zhou, Y. Zhao, P. Zhang, Y. Li. et al.(2017). Microbial mechanistic insight into the role of inulin in improving maternal health in a pregnant sow model. Frontiers in Microbiology.8(2242). DOI: 10.1016/S0140-6736(14)60460-8.
[44] M. E. Wilson, N. J. Biensen, S. P. Ford. (1999). Novel insight into the control of litter size in pigs, using placental efficiency as a selection tool. Journal of Animal Science.77(7):1654-1658. DOI: 10.1016/S0140-6736(14)60460-8.
[45] S. Aldosari, M. Awad, E. Harrington, F. Sellke. et al.(2018). Subcellular reactive oxygen species (ROS) in cardiovascular pathophysiology. Antioxidants.7(1):14. DOI: 10.1016/S0140-6736(14)60460-8.
[46] M. S. Hernandes, J. C. D’Avila, S. C. Trevelin, P. A. Reis. et al.(2014). The role of Nox2-derived ROS in the development of cognitive impairment after sepsis. Journal of Neuroinflammation.11(1):36. DOI: 10.1016/S0140-6736(14)60460-8.
[47] U. Bergström, C. Grundtman, I. E. Lundberg, L. T. Jacobsson. et al.(2014). Effects of adalimumab treatment on endothelial cell activation markers in the skeletal muscle of patients with rheumatoid arthritis. Clinical and Experimental Rrheumatology.32:883-890. DOI: 10.1016/S0140-6736(14)60460-8.
[48] J. Turgeon, P. Haddad, S. Dussault, J. Groleau. et al.(2012). Protection against vascular aging in Nox2-deficient mice: impact on endothelial progenitor cells and reparative neovascularization. Atherosclerosis.223(1):122-129. DOI: 10.1016/S0140-6736(14)60460-8.
[49] C. Óvilo, A. González-Bulnes, R. Benítez, M. Ayuso. et al.(2014). Prenatal programming in an obese swine model: sex-related effects of maternal energy restriction on morphology, metabolism and hypothalamic gene expression. British Journal of Nutrition.111(4):735-746. DOI: 10.1016/S0140-6736(14)60460-8.
[50] T. L. Bach, C. Barsigian, D. G. Chalupowicz, D. Busler. et al.(1998). VE-cadherin mediates endothelial cell capillary tube formation in fibrin and collagen gels. Experimental Cell Research.238(2):324-334. DOI: 10.1016/S0140-6736(14)60460-8.
[51] L. C. Joseph, E. Barca, P. Subramanyam, M. Komrowski. et al.(2016). Inhibition of NAPDH oxidase 2 (NOX2) prevents oxidative stress and mitochondrial abnormalities caused by saturated fat in cardiomyocytes. PloS One.11(1, article e0145750). DOI: 10.1016/S0140-6736(14)60460-8.
[52] C. Xia, Q. Meng, L. Z. Liu, Y. Rojanasakul. et al.(2007). Reactive oxygen species regulate angiogenesis and tumor growth through vascular endothelial growth factor. Cancer Research.67(22):10823-10830. DOI: 10.1016/S0140-6736(14)60460-8.
[53] T. Sato, J. I. Takino, K. Nagamine, K. Nishio. et al.(2019). RASGRP2 suppresses apoptosis via inhibition of ROS production in vascular endothelial cells. The Scientific World Journal.2019-8. DOI: 10.1016/S0140-6736(14)60460-8.
[54] F. Wu, F. J. Tian, Y. Lin, W. M. Xu. et al.(2016). Oxidative stress: placenta function and dysfunction. American Journal of Reproductive Immunology.76(4):258-271. DOI: 10.1016/S0140-6736(14)60460-8.
[55] C. Jiang, L. Jiang, Q. Li, X. Liu. et al.(2018). Acrolein induces NLRP3 inflammasome-mediated pyroptosis and suppresses migration via ROS-dependent autophagy in vascular endothelial cells. Toxicology.410:26-40. DOI: 10.1016/S0140-6736(14)60460-8.
[56] K. Bedard, K. H. Krause. (2007). The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiological Reviews.87(1):245-313. DOI: 10.1016/S0140-6736(14)60460-8.
[57] C. J. Hu, Q. Y. Jiang, T. Zhang, Y. L. Yin. et al.(2017). Dietary supplementation with arginine and glutamic acid modifies growth performance, carcass traits, and meat quality in growing-finishing pigs. Journal of Animal Science.95(6):2680-2689. DOI: 10.1016/S0140-6736(14)60460-8.
[58] I. Mert, A. Sargın Oruc, S. Yuksel, E. S. Cakar. et al.(2012). Role of oxidative stress in preeclampsia and intrauterine growth restriction. Journal of Obstetrics and Gynaecology Research.38(4):658-664. DOI: 10.1016/S0140-6736(14)60460-8.
[59] C. J. Hu, Q. Y. Jiang, T. Zhang, Y. L. Yin. et al.(2017). Dietary supplementation with arginine and glutamic acid enhances key lipogenic gene expression in growing pigs. Journal of Animal Science.95(12):5507-5515. DOI: 10.1016/S0140-6736(14)60460-8.
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