Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-22T17:19:20.639Z Has data issue: false hasContentIssue false

Oxidative stress caused by a dysregulated Wnt/β-catenin signalling pathway is involved in abnormal placenta formation in pregnant mice with chronic fatigue syndrome

Published online by Cambridge University Press:  15 October 2020

Hai Zhao*
Affiliation:
Institute of Laboratory Animal Science, Guizhou University of Traditional Chinese Medicine, Guiyang, Guizhou550025, China
Jian Zhang
Affiliation:
Institute of Laboratory Animal Science, Guizhou University of Traditional Chinese Medicine, Guiyang, Guizhou550025, China
Ning Qian
Affiliation:
Institute of Laboratory Animal Science, Guizhou University of Traditional Chinese Medicine, Guiyang, Guizhou550025, China
Shuguang Wu
Affiliation:
Institute of Laboratory Animal Science, Guizhou University of Traditional Chinese Medicine, Guiyang, Guizhou550025, China
Yanjun Wu
Affiliation:
Institute of Laboratory Animal Science, Guizhou University of Traditional Chinese Medicine, Guiyang, Guizhou550025, China
Gang Yao
Affiliation:
Institute of Laboratory Animal Science, Guizhou University of Traditional Chinese Medicine, Guiyang, Guizhou550025, China
*
Author for correspondence: Hai Zhao. Dongqing Road, Huaxi University Town, Guiyang, Guizhou550025, China. Tel: +86 0851 85652972. E-mail: [email protected]

Summary

Chronic fatigue syndrome (CFS) is characterized by extreme fatigue and disabling symptoms. Women with CFS often have a high risk of gynaecological problems such as irregular menstruation, endometriosis and pelvic pain and sexual dysfunction. Our previous results have shown that, in pregnant mice, CFS significantly decreased the progestational hormone level in serum, as well as learning and memory, and the function of the hypothalamus–pituitary–gonadal axis. In addition, the F1 generation also suffered from congenital hypothyroidism. At present, there has been no report about placenta formation and embryonic development in pregnant mice with CFS. The aim of the present study was to investigate the influence of CFS on the morphology, oxidative stress and Wnt/β-catenin signalling pathway during placenta formation. In this study, we found that CFS decreased the number of implantation sites for blastocysts, and increased the number of absorbed, stillborn and malformed fetuses. The morphology and structure of the placenta were abnormal in pregnant mice with CFS. Further study found that the oxidative stress in serum, uterus and placenta was increased in pregnant mice with CFS, while the levels of antioxidase were decreased. CFS also inhibited the Wnt/β-catenin signalling pathway in the placenta. These results suggested that inhibition of the Wnt/β-catenin signalling pathway and enhanced oxidative stress play an important role in abnormal placentation in pregnant mice with CFS.

Type
Research Article
Copyright
© The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Barrientos, G, Pussetto, M, Rose, M, Staff, AC, Blois, SM and Toblli (2017). Defective trophoblast invasion underlies fetal growth restriction and preeclampsia-like symptoms in the stroke-prone spontaneously hypertensive rat. Mol Hum Reprod 23, 509–19.CrossRefGoogle ScholarPubMed
Boneva, RS, Lin, JM and Unger, ER (2015). Early menopause and other gynecologic risk indicators for CFS in women. Menopause 22, 826–34.CrossRefGoogle ScholarPubMed
Cliff, JM, King, EC, Lee, JS, Sepúlveda, N, Wolf, AS, Kingdon, C, Bowman, E, Dockrell, HM, Nacul, L, Lacerda, E and Riley, EM. (2019). Cellular immune function in myalgic encephalomyelitis/chronic fatigue syndrome (ME/CFS). Front Immunol 16, 796.CrossRefGoogle Scholar
Collin, SM, Norris, T, Nuevo, R, Tilling, K, Joinson, C, Sterne, JAC and Crawley, E (2016). Chronic fatigue syndrome at age 16 years. Pediatrics 137, 110.CrossRefGoogle ScholarPubMed
Glassford, JAG (2017). The neuroinflammatory etiopathology of myalgic encephalomyelitis/chronic fatigue syndrome (ME/CFS). Front Physiol 2017; 8, 88.CrossRefGoogle Scholar
Herr, F, Horndasch, M, Howe, D, Baal, N, Goyal, P, Fischer, S, Zygmunt, M and Preissner, KT (2014). Human placenta-derived Wnt-5a induces the expression of ICAM-1 and VCAM-1 in CD133+CD34+-hematopoietic progenitor cells. Reprod Biol 14, 262–75.CrossRefGoogle ScholarPubMed
Jiang, SY, Yan, JT and Fang, M (2004). Progress in research on chronic fatigue syndrome. Zhong Xi Yi Jie He Xue Bao 2, 459–63.CrossRefGoogle ScholarPubMed
Josev, EK, Jackson, ML, Bei, B, Trinder, J, Harvey, A, Clarke, C, Snodgrass, K, Scheinberg, A and Knight, SJ (2017). Sleep quality in adolescents with chronic fatigue syndrome/myalgic encephalomyelitis (CFS/ME). J Clin Sleep Med 13, 1057–66.CrossRefGoogle Scholar
Katafuchi, T, Kondo, T, Yasaka, K, Kubo, K, Take, S and Yoshimura, M (2003). Prolonged effects of polyribocytidylic acid on spontaneous running wheel activity and brain interferon-α mRNA in rats: a model for immunologically induced fatigue. Neuroscience 120, 837–45.CrossRefGoogle Scholar
Liu, L and Qian, N (2011). Establishment of a pregnant rat model with chronic fatigue syndrome. J North Pharm 8, 67–8.Google Scholar
Logan, PC, Yango, P and Tran, ND (2018). Endometrial stromal and epithelial cells exhibit unique aberrant molecular defects in patients with endometriosis. Reprod Sci 25, 140–59.CrossRefGoogle ScholarPubMed
McInnis, OA, Matheson, K and Anisman, H (2014). Living with the unexplained: coping, distress, and depression among women with chronic fatigue syndrome and/or fibromyalgia compared with an autoimmune disorder. Anxiety Stress Coping 27, 601–18.CrossRefGoogle ScholarPubMed
Meinhardt, G, Haider, S, Haslinger, P, Proestling, K, Fiala, C, Pollheimer, J and Knoffler, M (2014). Wnt-dependent T-cell factor-4 controls human extravillous trophoblast motility. Endocrinology 155, 1908–20.CrossRefGoogle ScholarPubMed
Mensah, FFK, Armstrong, CW, Reddy, V, Bansal, AS, Berkovitz, S, Leandro, MJ and Cambridge, G (2018). CD24 expression and b cell maturation shows a novel link with energy metabolism: potential implications for patients with myalgic encephalomyelitis/chronic fatigue syndrome. Front Immunol 22, 2421.CrossRefGoogle Scholar
Nayeem, SB, Arfuso, F, Dharmarajan, A and Keelan, JA (2016). Role of Wnt signalling in early pregnancy. Reprod Fertil Dev 28, 525–44.CrossRefGoogle ScholarPubMed
Ohba, T, Domoto, S, Tanaka, M, Nakamura, S, Shimazawa, M and Hara, H (2019). Myalgic encephalomyelitis/chronic fatigue syndrome induced by repeated forced swimming in mice. Biol Pharm Bull 2019; 42, 1140–5.CrossRefGoogle ScholarPubMed
Pajediene, E, Bileviciute-Ljungar, I and Friberg, D (2018). Sleep patterns among patients with chronic fatigue: a polysomnography-based study. Clin Respir J 12, 1389–97.CrossRefGoogle ScholarPubMed
Partl, JZ, Fabijanovic, D, Skrtic, A, Vranic, S, Martic, TN and Serman, L (2014). Immunohistochemical expression of SFRP1 and SFRP3 proteins in normal and malignant reproductive tissues of rats and humans. Appl Immunohistochem Mol Morphol 22, 681–7.CrossRefGoogle ScholarPubMed
Polli, A, Van Oosterwijck, J, Nijs, J, Marusic, U, De WAndele, I, Paul, L, Meeus, M, Moorkens, G, Lambrecht, L and Ickmans, K (2019). Relationship between exercise-induced oxidative stress changes and parasympathetic activity in chronic fatigue syndrome: an observational study in patients and healthy subjects. Clin Ther 41, 641–55.CrossRefGoogle ScholarPubMed
Scheibenbogen, C, Loebel, M, Freitag, H, Krueger, A, Nauer, S, Antelmann, M, Doehner, W, Scherbakov, N, Heidecke, H, Reinke, P, Volk, H-D and Grabowski, P (2018). Immunoadsorption to remove 2 adrenergic receptor antibodies in chronic fatigue syndrome CFS/ME. PLoS One 13, e0193672.CrossRefGoogle ScholarPubMed
Shan, ZY, Finegan, K, Bhuta, S, Ireland, T, Staines, DR, Marshall-Gradisnik, SM and Barnden, LR (2018). Brain function characteristics of chronic fatigue syndrome: a task MRI study. Neuroimage Clin 25, 279–86.CrossRefGoogle Scholar
van der Schaaf, ME, Roelofs, K, de Lange, FP, Geurts, DEM, van der Meer, JWM, Knoop, H and Toni, I (2018). Fatigue is associated with altered monitoring and preparation of physical effort in patients with chronic fatigue syndrome. Biol Psych Cogn Neurosci Neuroimag 3, 392404.Google ScholarPubMed
Vergauwen, K, Huijnen, IP, Kos, D, Van de Velde, D, van Eupen, I and Meeus, M (2015). Assessment of activity limitations and participation restrictions with persons with chronic fatigue syndrome: a systematic review. Disabil Rehabil 37, 1706–116.CrossRefGoogle ScholarPubMed
Wang, X, Zhang, Z, Zeng, X, Wang, J, Zhang, L, Song, W and Shi, Y (2018). Wnt/β-catenin signaling pathway in severe preeclampsia. J Mol Histol 49, 317–27.CrossRefGoogle ScholarPubMed
Xu, P, Gu, Q and Zhang, M (2017). Research progress on the role of Wnt/β- catenin signaling pathway in disease and its regulatory mechanism. Zhonghua Lao Dong Wei Sheng Zhi Ye Bing Za Zhi 35, 946–9.Google ScholarPubMed
Yeh, CC, Su, FH, Tzeng, CR, Muo, C-H and Wang, W-C (2018). Women with adenomyosis are at higher risks of endometrial and thyroid cancers: a population-based historical cohort study. PLoS One 13, e0194011.CrossRefGoogle ScholarPubMed
Zhao, H, Yao, G, Qian, N, Chen, M, Yang, Z and Wu, S (2016a). The ability of spontaneous and exploratory behavior was observed in chronic fatigue syndrome mice. Lab Anim Sci 33, 3942.Google Scholar
Zhao, H, Yao, G, Qian, N, Chen, M, Yang, Z and Wu, S (2016b). The spatial learning and memory function were reduced in chronic fatigue syndrome. Sichuan J Zool 2016b, 35, 879–83.Google Scholar
Zhang, Z, Zhang, L, Zhang, L, Jia, L, Wang, P and Gap, Y (2013). Association of Wnt2 and sFRP4 expression in the third trimester placenta in women with severe preeclampsia. Reprod Sci 20, 981–9.CrossRefGoogle ScholarPubMed
Zhang, Z, Wang, X, Zhang, L, Shi, Y, Wang, J and Yan, H (2017). Wnt/β-catenin signaling pathway in trophoblasts and abnormal activation in preeclampsia. Mol Med Rep 16, 10071013.Google ScholarPubMed
Zhang, L, Leng, M, Li, Y, Yuan, Y, Yang, B, Li, Y, Yuan, E, Shi, W, Yan, S and Cui, S (2019). Altered DNA methylation and transcription of WNT2 and DKK1 genes in placentas associated with early-onset preeclampsia. Clin Chim Acta 490, 154–60.CrossRefGoogle ScholarPubMed
Zhuang, B, Luo, X, Rao, H, Li, Q, Shan, N, Liu, X and Qi, H (2015). Oxidative stress-induced C/EBPβ inhibits β-catenin signaling molecule involving in the pathology of preeclampsia. Placenta 36, 838–46.CrossRefGoogle ScholarPubMed
Zinn, MA, Zinn, ML, Valencia, I, Jason, LA and Montoya, JG (2018). Cortical hypoactivation during resting EEG suggests central nervous system pathology in patients with chronic fatigue syndrome. Biol Psychol 136, 8799.CrossRefGoogle ScholarPubMed
Zmijanac Partl, J, Karin, V, Skrtic, A, Nikuseva-Martic, T, Serman, A, Mlinareac, J, Curkovic-Perica, M, Vranic, S and Serman, L (2018). Negative regulators of Wnt signaling pathway SFRP1 and SFRP3 expression in preterm and term pathologic placentas. J Matern Fetal Neonatal Med 31, 2971–9.CrossRefGoogle ScholarPubMed