Circadian rhythms of factors involved in luteal regression are modified in p55 tumour necrosis factor receptor (TNFRp55)-deficient mice
Magali del C. de la Vega A , María B. Delsouc A , Ivana Ponce B , Vicente Ragusa A B , Sandra Vallcaneras A , Ana C. Anzulovich B C and Marilina Casais A C
+ Author Affiliations
- Author Affiliations
A Laboratorio de Biología de la Reproducción, Facultad de Química, Bioquímica y Farmacia, Instituto Multidisciplinario de Investigaciones Biológicas, San Luis, Universidad Nacional de San Luis, Ejército de los Andes 950, CP D5700HHW, San Luis, Argentina.
B Laboratorio de Cronobiología, Facultad de Química, Bioquímica y Farmacia, Instituto Multidisciplinario de Investigaciones Biológicas, San Luis, Universidad Nacional de San Luis, Ejército de los Andes 950, CP D5700HHW, San Luis, Argentina.
C Corresponding authors. Emails: mcasais@unsl.edu.ar; anzulova@gmail.com
Reproduction, Fertility and Development 30(12) 1651-1665 https://doi.org/10.1071/RD18058
Submitted: 9 February 2018 Accepted: 5 May 2018 Published: 15 June 2018
Abstract
The rhythm of factors involved in luteal regression is crucial in determining the physiological duration of the oestrous cycle. Given the role of tumour necrosis factor (TNF)-α in luteal function and circadian regulation and that most of the effects of TNF-α are mediated by p55 TNF receptor (TNFRp55), the aims of the present study were to analyse the following during the luteal regression phase in the ovary of mice: (1) whether the pattern of expression of progesterone (P4) and the enzymes involved in the synthesis and degradation of P4 is circadian and endogenous (the rhythm persists in constant conditions, (i.e., constant darkness) with a period of about 24 hours); (2) circadian oscillations in clock gene expression; (3) whether there are daily variations in the expression of key genes involved in apoptosis and antioxidant mechanisms; and (4) the consequences of TNFRp55 deficiency. P4 was found to oscillate circadianally following endogenous rhythms of clock factors. Of note, TNFRp55 deficiency modified the circadian oscillation in P4 concentrations and its enzymes involved in the synthesis and degradation of P4, probably as a consequence of changes in the circadian oscillations of brain and muscle ARNT-Like protein 1 (Bmal1) and Cryptochrome 1 (Cry1). Furthermore, TNFRp55 deficiency modified the circadian rhythms of apoptosis genes, as well as antioxidant enzymes and peroxidation levels in the ovary in dioestrus. The findings of the present study strengthen the hypothesis that dysregulation of TNF-α signalling may be a potential cause for altered circadian and menstrual cycling in some gynaecological diseases.
Additional keywords: clock, corpus luteum, ovary.
References
Abdo, M., Hisheh, S., Arfuso, F., and Dharmarajan, A. (2008). The expression of tumor necrosis factor-alpha, its receptors and steroidogenic acute regulatory protein during corpus luteum regression. Reprod. Biol. Endocrinol. 6, 50–61.| The expression of tumor necrosis factor-alpha, its receptors and steroidogenic acute regulatory protein during corpus luteum regression.Crossref | GoogleScholarGoogle Scholar |
Aebi, H. (1984). Catalase in vitro. Methods Enzymol. 105, 121–126.
| Catalase in vitro.Crossref | GoogleScholarGoogle Scholar |
Al-Gubory, K. H., Garrel, C., Faure, P., and Sugino, N. (2012). Roles of antioxidant enzymes in corpus luteum rescue from reactive oxygen species-induced oxidative stress. Reprod. Biomed. Online 25, 551–560.
| Roles of antioxidant enzymes in corpus luteum rescue from reactive oxygen species-induced oxidative stress.Crossref | GoogleScholarGoogle Scholar |
Arjona, A., and Sarkar, D. K. (2006). Evidence supporting a circadian control of natural killer cell function. Brain Behav. Immun. 20, 469–476.
| Evidence supporting a circadian control of natural killer cell function.Crossref | GoogleScholarGoogle Scholar |
Boden, M. J., Varcoe, T. J., Voultsios, A., and Kennaway, D. J. (2010). Reproductive biology of female Bmal1 null mice. Reproduction 139, 1077–1090.
| Reproductive biology of female Bmal1 null mice.Crossref | GoogleScholarGoogle Scholar |
Bollinger, T., Bollinger, A., Naujoks, J., Lange, T., and Solbach, W. (2010). The influence of regulatory T cells and diurnal hormone rhythms on T helper cell activity. Immunology 131, 488–500.
| The influence of regulatory T cells and diurnal hormone rhythms on T helper cell activity.Crossref | GoogleScholarGoogle Scholar |
Bowen-Shauver, J. M., and Telleria, C. M. (2003). Luteal regression: a redefinition of the terms. Reprod. Biol. Endocrinol. 1, 28.
| Luteal regression: a redefinition of the terms.Crossref | GoogleScholarGoogle Scholar |
Bussmann, L. E., and Deis, R. P. (1979). Studies concerning the hormonal induction of lactogenesis by prostaglandin F2 in pregnant rats. J. Steroid Biochem. 11, 1485–1489.
| Studies concerning the hormonal induction of lactogenesis by prostaglandin F2 in pregnant rats.Crossref | GoogleScholarGoogle Scholar |
Candolfi, M., Jaita, G., Zaldivar, V., Zárate, S., Ferrari, L., Pisera, D., Castro, M. G., and Seilicovich, A. (2005). Progesterone antagonizes the permissive action of estradiol on tumor necrosis factor-alpha-induced apoptosis of anterior pituitary cells. Endocrinology 146, 736–743.
| Progesterone antagonizes the permissive action of estradiol on tumor necrosis factor-alpha-induced apoptosis of anterior pituitary cells.Crossref | GoogleScholarGoogle Scholar |
Cartharius, K., Frech, K., Grote, K., Klocke, B., Haltmeier, M., Klingenhoff, A., Frisch, M., Bayerlein, M., and Werner, T. (2005). MatInspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics 21, 2933–2942.
| MatInspector and beyond: promoter analysis based on transcription factor binding sites.Crossref | GoogleScholarGoogle Scholar |
Cavadini, G., Petrzilka, S., Kohler, P., Jud, C., Tobler, I., Birchler, T., and Fontana, A. (2007). TNF-alpha suppresses the expression of clock genes by interfering with E-box-mediated transcription. Proc. Natl Acad. Sci. USA 104, 12843–12848.
| TNF-alpha suppresses the expression of clock genes by interfering with E-box-mediated transcription.Crossref | GoogleScholarGoogle Scholar |
Chang, W. T., Hsieh, B. S., Cheng, H. L., Lee, K. T., and Chang, K. L. (2014). Progesterone augments epirubicin-induced apoptosis in HA22T/VGH cells by increasing oxidative stress and upregulating Fas/FasL. J. Surg. Res. 188, 432–441.
| Progesterone augments epirubicin-induced apoptosis in HA22T/VGH cells by increasing oxidative stress and upregulating Fas/FasL.Crossref | GoogleScholarGoogle Scholar |
Chen, H., Zhao, L., Kumazawa, M., Yamauchi, N., Shigeyoshi, Y., Hashimoto, S., and Hattori, M. A. (2013). Downregulation of core clock gene Bmal1 attenuates expression of progesterone and prostaglandin biosynthesis-related genes in rat luteinizing granulosa cells. Am. J. Physiol. Cell Physiol. 304, C1131–C1140.
| Downregulation of core clock gene Bmal1 attenuates expression of progesterone and prostaglandin biosynthesis-related genes in rat luteinizing granulosa cells.Crossref | GoogleScholarGoogle Scholar |
Coogan, A. N., Papachatzaki, M. M., Clemens, C., Baird, A., Donev, R. M., Joosten, J., Zachariou, V., and Thome, J. (2011). Haloperidol alters circadian clock gene product expression in the mouse brain. World J. Biol. Psychiatry 12, 638–644.
| Haloperidol alters circadian clock gene product expression in the mouse brain.Crossref | GoogleScholarGoogle Scholar |
Corda, S., Laplace, C., Vicaut, E., and Duranteau, J. (2001). Rapid reactive oxygen species production by mitochondria in endothelial cells exposed to tumor necrosis factor-alpha is mediated by ceramide. Am. J. Respir. Cell Mol. Biol. 24, 762–768.
| Rapid reactive oxygen species production by mitochondria in endothelial cells exposed to tumor necrosis factor-alpha is mediated by ceramide.Crossref | GoogleScholarGoogle Scholar |
Davis, J. S., and Rueda, B. R. (2002). The corpus luteum: an ovarian structure with maternal instincts and suicidal tendencies. Front. Biosci. 7, d1949–d1978.
| The corpus luteum: an ovarian structure with maternal instincts and suicidal tendencies.Crossref | GoogleScholarGoogle Scholar |
Draper, H. H., and Hadley, M. (1990). Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol. 186, 421–431.
| Malondialdehyde determination as index of lipid peroxidation.Crossref | GoogleScholarGoogle Scholar |
Endo, T., Henmi, H., Goto, T., Kitajima, Y., Kiya, T., Nishikawa, A., Manase, K., Yamamoto, H., and Kudo, R. (1998). Effects of estradiol and an aromatase inhibitor on progesterone production in human cultured luteal cells. Gynecol. Endocrinol. 12, 29–34.
| Effects of estradiol and an aromatase inhibitor on progesterone production in human cultured luteal cells.Crossref | GoogleScholarGoogle Scholar |
Fahrenkrug, J., Georg, B., Hannibal, J., Hindersson, P., and Gras, S. (2006). Diurnal rhythmicity of the clock genes Per1 and Per2 in the rat ovary. Endocrinology 147, 3769–3776.
| Diurnal rhythmicity of the clock genes Per1 and Per2 in the rat ovary.Crossref | GoogleScholarGoogle Scholar |
Flohé, L., and Günzler, W. A. (1984). Assays of glutathione peroxidase. Methods Enzymol. 105, 114–120.
| Assays of glutathione peroxidase.Crossref | GoogleScholarGoogle Scholar |
Granda, T. G., Liu, X. H., Smaaland, R., Cermakian, N., Filipski, E., Sassone-Corsi, P., and Lévi, F. (2005). Circadian regulation of cell cycle and apoptosis proteins in mouse bone marrow and tumor. FASEB J. 19, 304–306.
| Circadian regulation of cell cycle and apoptosis proteins in mouse bone marrow and tumor.Crossref | GoogleScholarGoogle Scholar |
Hardeland, R., Coto-Montes, A., and Poeggeler, B. (2003). Circadian rhythms, oxidative stress, and antioxidative defense mechanisms. Chronobiol. Int. 20, 921–962.
| Circadian rhythms, oxidative stress, and antioxidative defense mechanisms.Crossref | GoogleScholarGoogle Scholar |
Leone, M. J., Marpegan, L., Duhart, J. M., and Golombek, D. A. (2012). Role of proinflammatory cytokines on lipopolysaccharide-induced phase shifts in locomotor activity circadian rhythm. Chronobiol. Int. 29, 715–723.
| Role of proinflammatory cytokines on lipopolysaccharide-induced phase shifts in locomotor activity circadian rhythm.Crossref | GoogleScholarGoogle Scholar |
Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. (1951). Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265–275.
Mukhopadhyay, R., Mishra, M. K., Basu, A., and Bishayi, B. (2009). Modulation of steroidogenic enzymes in murine lymphoid organs after immune activation. Immunol. Invest. 38, 14–30.
| Modulation of steroidogenic enzymes in murine lymphoid organs after immune activation.Crossref | GoogleScholarGoogle Scholar |
Nakamura, T. J., Sellix, M. T., Kudo, T., Nakao, N., Yoshimura, T., Ebihara, S., Colwell, C. S., and Block, G. D. (2010). Influence of the estrous cycle on clock gene expression in reproductive tissues: effects of fluctuating ovarian steroid hormone levels. Steroids 75, 203–212.
| Influence of the estrous cycle on clock gene expression in reproductive tissues: effects of fluctuating ovarian steroid hormone levels.Crossref | GoogleScholarGoogle Scholar |
Nakao, N., Yasuo, S., Nishimura, A., Yamamura, T., Watanabe, T., Anraku, T., Okano, T., Fukada, Y., Sharp, P. J., Ebihara, S., and Yoshimura, T. (2007). Circadian clock gene regulation of steroidogenic acute regulatory protein gene expression in preovulatory ovarian follicles. Endocrinology 148, 3031–3038.
| Circadian clock gene regulation of steroidogenic acute regulatory protein gene expression in preovulatory ovarian follicles.Crossref | GoogleScholarGoogle Scholar |
Navigatore-Fonzo, L., Castro, A., Pignataro, V., Garraza, M., Casais, M., and Anzulovich, A. C. (2017). Daily rhythms of cognition-related factors are modified in an experimental model of Alzheimer’s disease. Brain Res. 1660, 27–35.
| Daily rhythms of cognition-related factors are modified in an experimental model of Alzheimer’s disease.Crossref | GoogleScholarGoogle Scholar |
Okuda, K., and Sakumoto, R. (2003). Multiple roles of TNF super family members in corpus luteum function. Reprod. Biol. Endocrinol. 1, 95.
| Multiple roles of TNF super family members in corpus luteum function.Crossref | GoogleScholarGoogle Scholar |
Petrzilka, S., Taraborrelli, C., Cavadini, G., Fontana, A., and Birchler, T. (2009). Clock gene modulation by TNF-alpha depends on calcium and p38 MAP kinase signaling. J. Biol. Rhythms 24, 283–294.
| Clock gene modulation by TNF-alpha depends on calcium and p38 MAP kinase signaling.Crossref | GoogleScholarGoogle Scholar |
Ponce, I. T., Rezza, I. G., Delgado, S. M., Navigatore, L. S., Bonomi, M. R., Golini, R. L., Gimenez, M. S., and Anzulovich, A. C. (2012). Daily oscillation of glutathione redox cycle is dampened in the nutritional vitamin A deficiency. Biol. Rhythm Res. 43, 351–372.
| Daily oscillation of glutathione redox cycle is dampened in the nutritional vitamin A deficiency.Crossref | GoogleScholarGoogle Scholar |
Pru, J. K., Lynch, M. P., Davis, J. S., and Rueda, B. R. (2003). Signaling mechanisms in tumor necrosis factor alpha-induced death of microvascular endothelial cells of the corpus luteum. Reprod. Biol. Endocrinol. 1, 17.
| Signaling mechanisms in tumor necrosis factor alpha-induced death of microvascular endothelial cells of the corpus luteum.Crossref | GoogleScholarGoogle Scholar |
Redlin, U. (2001). Neural basis and biological function of masking by light in mammals: suppression of melatonin and locomotor activity. Chronobiol. Int. 18, 737–758.
| Neural basis and biological function of masking by light in mammals: suppression of melatonin and locomotor activity.Crossref | GoogleScholarGoogle Scholar |
Refinetti, R., Corné Lissen, G., and Halberg, F. (2007). Procedures for numerical analysis of circadian rhythms. Biol. Rhythm Res. 38, 275–325.
| Procedures for numerical analysis of circadian rhythms.Crossref | GoogleScholarGoogle Scholar |
Roby, K. F., Son, D. S., and Terranova, P. F. (1999). Alterations of events related to ovarian function in tumor necrosis factor receptor type I knockout mice. Biol. Reprod. 61, 1616–1621.
| Alterations of events related to ovarian function in tumor necrosis factor receptor type I knockout mice.Crossref | GoogleScholarGoogle Scholar |
Rojas-Cartagena, C., Appleyard, C. B., Santiago, O. I., and Flores, I. (2005). Experimental intestinal endometriosis is characterized by increased levels of soluble TNFRSF1B and downregulation of Tnfrsf1a and Tnfrsf1b gene expression. Biol. Reprod. 73, 1211–1218.
| Experimental intestinal endometriosis is characterized by increased levels of soluble TNFRSF1B and downregulation of Tnfrsf1a and Tnfrsf1b gene expression.Crossref | GoogleScholarGoogle Scholar |
Sander, V. A., Piehl, L., Facorro, G. B., Rubin de Celis, E., and Motta, A. B. (2008). Regulation of functional and regressing stages of corpus luteum development in mice. Role of reactive oxygen species. Reprod. Fertil. Dev. 20, 760–769.
| Regulation of functional and regressing stages of corpus luteum development in mice. Role of reactive oxygen species.Crossref | GoogleScholarGoogle Scholar |
Sellix, M. T., and Menaker, M. (2011). Circadian clocks in mammalian reproductive physiology: effects of the ‘other’ biological clock on fertility. Discov. Med. 11, 273–281.
Smith, M. S., Freeman, M. E., and Neill, J. D. (1975). The control of progesterone secretion during the estrous cycle and early pseudopregnancy in the rat: prolactin, gonadotropin and steroid levels associated with rescue of the corpus luteum of pseudopregnancy. Endocrinology 96, 219–226.
| The control of progesterone secretion during the estrous cycle and early pseudopregnancy in the rat: prolactin, gonadotropin and steroid levels associated with rescue of the corpus luteum of pseudopregnancy.Crossref | GoogleScholarGoogle Scholar |
Stocco, C., Telleria, C., and Gibori, G. (2007). The molecular control of corpus luteum formation, function, and regression. Endocr. Rev. 28, 117–149.
| The molecular control of corpus luteum formation, function, and regression.Crossref | GoogleScholarGoogle Scholar |
Sugino, N., Telleria, C. M., and Gibori, G. (1997). Progesterone inhibits 20alpha-hydroxysteroid dehydrogenase expression in the rat corpus luteum through the glucocorticoid receptor. Endocrinology 138, 4497–4500.
| Progesterone inhibits 20alpha-hydroxysteroid dehydrogenase expression in the rat corpus luteum through the glucocorticoid receptor.Crossref | GoogleScholarGoogle Scholar |
Tasaki, H., Zhao, L., Isayama, K., Chen, H., Yamauchi, N., Shigeyoshi, Y., Hashimoto, S., and Hattori, M. A. (2013). Profiling of circadian genes expressed in the uterus endometrial stromal cells of pregnant rats as revealed by DNA microarray coupled with RNA interference. Front. Endocrinol. (Lausanne) 4, 82.
| Profiling of circadian genes expressed in the uterus endometrial stromal cells of pregnant rats as revealed by DNA microarray coupled with RNA interference.Crossref | GoogleScholarGoogle Scholar |
Terranova, P. F., and Rice, V. M. (1997). Review: cytokine involvement in ovarian processes. Am. J. Reprod. Immunol. 37, 50–63.
| Review: cytokine involvement in ovarian processes.Crossref | GoogleScholarGoogle Scholar |
Terranova, P. F., Hunter, V. J., Roby, K. F., and Hunt, J. S. (1995). Tumor necrosis factor-α in the female reproductive tract. Proc. Soc. Exp. Biol. Med. 209, 325–342.
| Tumor necrosis factor-α in the female reproductive tract.Crossref | GoogleScholarGoogle Scholar |
Trinder, P. (1969). Determination of glucose in blood using glucose oxidase with an alternative oxygen acceptor. Ann. Clin. Biochem. 6, 24–27.
| Determination of glucose in blood using glucose oxidase with an alternative oxygen acceptor.Crossref | GoogleScholarGoogle Scholar |
Vallcaneras, S. S., De la Vega, M., Delgado, S. M., Motta, A., Telleria, C., Rastrilla, A. M., and Casais, M. (2016). Prolactin modulates luteal regression from the coeliac ganglion via the superior ovarian nerve in the late-pregnant rat. Reprod. Fertil. Dev. 28, 565–573.
| Prolactin modulates luteal regression from the coeliac ganglion via the superior ovarian nerve in the late-pregnant rat.Crossref | GoogleScholarGoogle Scholar |
Vallcaneras, S., Ghersa, F., Bastón, J., Delsouc, M. B., Meresman, G., and Casais, M. (2017). TNFRp55 deficiency promotes the development of ectopic endometriotic-like lesions in mice. J. Endocrinol. 234, 269–278.
| TNFRp55 deficiency promotes the development of ectopic endometriotic-like lesions in mice.Crossref | GoogleScholarGoogle Scholar |
Verma, D., Hashim, O. H., Jayapalan, J. J., and Subramanian, P. (2014). Effect of melatonin on antioxidant status and circadian activity rhythm during hepatocarcinogenesis in mice. J. Cancer Res. Ther. 10, 1040–1044.
| Effect of melatonin on antioxidant status and circadian activity rhythm during hepatocarcinogenesis in mice.Crossref | GoogleScholarGoogle Scholar |
Welsh, D. K., Takahashi, J. S., and Kay, S. A. (2010). Suprachiasmatic nucleus: cell autonomy and network properties. Annu. Rev. Physiol. 72, 551–577.
| Suprachiasmatic nucleus: cell autonomy and network properties.Crossref | GoogleScholarGoogle Scholar |
Yoshida, K., Hashiramoto, A., Okano, T., Yamane, T., Shibanuma, N., and Shiozawa, S. (2013). TNF-α modulates expression of the circadian clock gene Per2 in rheumatoid synovial cells. Scand. J. Rheumatol. 42, 276–280.
| TNF-α modulates expression of the circadian clock gene Per2 in rheumatoid synovial cells.Crossref | GoogleScholarGoogle Scholar |
Zhang, Z., Lai, S., Wang, Y., Li, L., Yin, H., Wang, Y., Zhao, X., Li, D., Yang, M., and Zhu, Q. (2017). Rhythmic expression of circadian clock genes in the preovulatory ovarian follicles of the laying hen. PLoS One 12, e0179019.
| Rhythmic expression of circadian clock genes in the preovulatory ovarian follicles of the laying hen.Crossref | GoogleScholarGoogle Scholar |
Zorov, D. B., Juhaszova, M., and Sollott, S. J. (2006). Mitochondrial ROS-induced ROS release: an update and review. Biochim. Biophys. Acta 1757, 509–517.
| Mitochondrial ROS-induced ROS release: an update and review.Crossref | GoogleScholarGoogle Scholar |
Zuther, P., Gorbey, S., and Lemmer, B. (2009). Chronos-Fit 1.06, http://www.ma.uni-heidelberg.de/inst/phar/lehre/chrono.html [verified 21 March 2017].
