Photoperiodic conditions as a factor modulating leptin influence on pro-inflammatory cytokines and their receptors gene expression in ewe’s aorta
More details
Hide details
The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences, Department of Genetic Engineering, Instytucka 3, 05-110 Jabłonna
Agricultural University of Krakow, Department of Animal Biotechnology, Laboratory of Biotechnology and Genomics, 30-248 Krakow, Poland
A. Krawczyńska   

The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences, Department of Genetic Engineering, Instytucka 3, 05-110 Jabłonna
Publication date: 2019-06-19
J. Anim. Feed Sci. 2019;28(2):128–137
Atherosclerosis, a chronic inflammation state of the aorta, is characterised by increased levels of pro-inflammatory cytokines (tumour necrosis factor alpha (TNFα), interleukin (IL)-1β, IL-6). Sheep is used in both cardiovascular and immunological studies; besides, ‘long-day’ ewe can be a model of leptin resistance state. The aim of the study was to examine whether photoperiodic conditions (long-day (LD) and short-day (SD) seasons) are a key factor modulating exogenous leptin influence on pro-inflammatory cytokines and their receptors gene expression in aorta of ewe’s with or without prior induction of acute inflammation. The experiment was conducted on 48 ewes during SD and LD seasons which were randomly divided into 4 groups: control; with LPS injection (400 ng/kg of body weight (BW)); with leptin injection (20 μg/kg BW); and with LPS and 30-min later leptin injection. Three hours after LPS/control treatment animals were euthanized to collect the thoracic aorta samples. In both seasons leptin injection intensified LPS-induced increase in IL1B gene expression but only in SD season leptin injection increased IL1R1 and IL1R2 gene expressions. The leptin injection increased IL6 gene expression but only in SD season. In the LD season leptin enhanced the LPS effect on IL6 gene expression. Neither TNFA nor its receptors gene expression was influenced by leptin regardless of season. In the thoracic aorta tissue an exogenous leptin exerts effect on pro-inflammatory cytokines and their receptors gene expression; however in ewe this influence depends on photoperiodic conditions. Moreover, leptin can moderate progression of the inflammation reaction in this tissue
Azevedo L. (Editor), 2012. Sepsis – an Ongoing and Significant Challenge. InTech London (UK), https://doi.org/10.5772/2958.
Batra A, Pietsch J., Fedke I., Glauben R., Okur B., Stroh T., Zeitz M., Siegmund B., 2007. Leptin-dependent toll-like receptor expression and responsiveness in preadipocytes and adipocytes. Am. J. Pathol. 170, 1931–1941, https://doi.org/10.2353/ajpath....
Beltowski J., 2006. Leptin and atherosclerosis. Atherosclerosis 189, 47–60, https://doi.org/10.1016/j.athe....
Beręsewicz A. (Editor), 2011. Pathophysiology of atherosclerosis and ischemic heart disease (in Polish: Patofizjologia miażdżycy i choroby niedokrwiennej serca). Centrum Medycznego Kształcenia Podyplomowego Wydawnictwo. Warsaw (Poland).
Camacho P., Fan H., Liu Z et al., 2016. Large mammalian animal models of heart disease. J. Cardiovas. Develop. Dis. 3, 30, https://doi.org/10.3390/jcdd30....
Chilliard Y., Delavaud C., Bonnet M., 2005. Leptin expression in ruminants: Nutritional and physiological regulations in relation with energy metabolism. Domestic Anim. Endocrinol. 29, 3–22, https://doi.org/10.1016/j.doma....
DeVallance E., Branyan K.W., Lemaster K., Olfert I.M., Smith D.M., Pistilli E.E., Frisbee J.C., Chantler P.D., 2018. Aortic dysfunction in metabolic syndrome mediated by perivascular adipose tissue TNFα- and NOX2-dependent pathway. Exp. Physiol. 103, 590–603, https://doi.org/10.1113/EP0868....
Duchenne J., Claus P., Pagourelias E.D., Mada R.O., Van Puyvelde J., Vunckx K., Verbeken E., Gheysens O., Rega F., Voigt J.U., 2018. Sheep can be used as animal model of regional myocardial remodelling and controllable work. Cardiol. J. https://doi.org/10.5603/CJ.a20....
Frantz S., Ertl G., Bauersachs J., 2007. Mechanism of disease: Tolllike receptors in cardiovascular disease. Nat. Clin. Pract. Cardiovasc. Med. 4, 444–454, https://doi.org/10.1038/ncpcar....
Harden L.M., du Plessis I., Poole S., Laburn H.P., 2006. Interleukin-6 and leptin mediate lipopolysaccharide-induced fever and sickness behavior. Physiol. Behavior 89, 146–155, https://doi.org/10.1016/j.phys....
Hartman J., Frishman W.H., 2014. Inflammation and atherosclerosis: a review of the role of interleukin-6 in the development of atherosclerosis and the potential for targeted drug therapy. Cardiol. Rev. 22, 147–151, https://doi.org/10.1097/CRD.00....
Herman A., Misztal T., Herman A., Tomaszewska-Zaremba D., 2010. Expression of interleukin (IL)-1β and IL-1 receptors genes in the hypothalamus of anoestrous ewes after lipopolysaccharide treatment. Reprod. Domest. Anim. 45, e426–e433, https://doi.org/10.1111/j.1439....
Herman A.P., Krawczyńska A., Bochenek J., Antushevich H., Herman A., Tomaszewska-Zaremba D., 2014. Peripheral injection of SB203580 inhibits the inflammatorydependent synthesis of proinflammatory cytokines in the hypothalamus. BioMed Res. Int. 2014, 1–10, https://doi.org/10.1155/2014/4....
Herman A.P., Tomaszewska-Zaremba D., 2010. Effect of endotoxin on the expression of GnRH and GnRHR genes in the hypothalamus and anterior pituitary gland of anestrous ewes. Anim. Reprod. Sci. 120, 105–111, https://doi.org/10.1016/j.anir....
Hosoi T., Okuma Y., Nomura Y., 2002. Leptin regulates interleukin1beta expression in the brain via the STAT3-independent mechanisms. Brain Res. 949, 139–146, https://doi.org/10.1016/S0006-....
Howell K.W., Meng X., FullertonD.A., JinC., ReeceT.B., Cleveland J.C. Jr., 2011. Toll-like receptor 4 mediates oxidized LDL-induced macrophage differentiation to foam cells. J. Surg. Res. 171, e27–e31, https://doi.org/10.1016/j.jss.....
Katsargyris A., Theocharis S.E., Tsiodras S., Giaginis K., Bastounis E., Klonaris C., 2010. Enhanced TLR4 endothelial cell immunohistochemical expression in symptomatic carotid atherosclerotic plaques. Expert Opin. Ther. Targets 14, 1–10, https://doi.org/10.1517/147282....
Krawczyńska A., Olczak E., Rembiszewska A., GromadzkaOstrowska J., 2013. High-fat, cholesterol-rich diet affects leptin expression in the aortic layers. Exp Biol Med 238, 47–56, https://doi.org/10.1258/ebm.20....
Krawczyńska A., Olczak E., Rembiszewska A., Herman A.P., Gromadzka-Ostrowska J., 2014. Time-dependent supplementation of vitamin E influences leptin expression in the aortic layers of rats fed atherogenic diet. J. Physiol. Pharmacol. 65, 33–39.
Król K., Tomaszewska-Zaremba D., Herman A., 2016. Photoperioddependent effect of inflammation on nocturnal gene expression of proinflammatory cytokines and their receptors in pars tuberalis of ewe. J. Anim. Feed Sci. 25, 3–11, https://doi.org/10.22358/jafs/....
Kumar H., Kawai T., Akira S., 2011. Pathogen recognition by the innate immune system. Int. Rev. Immunol. 30, 16–34, https://doi.org/10.3109/088301....
Lee S.-M., Choi H.-J., Oh C.-H., Oh J.-W., Han J.-S., 2014. Leptin increases TNF-α expression and production through phospholipase D1 in Raw 264.7 cells. PLoS ONE 9, e102373, https://doi.org/10.1371/journa....
Libby P., 2017. Interleukin-1 beta as a target for atherosclerosis therapy. J. Am. Coll. Cardiol. 70, 2278–2289, https://doi.org/10.1016/j.jacc....
LuheshiG.N., Gardner J.D., RushforthD.A., LoudonA.S., RothwellN.J., 1999. Leptin actions on food intake and body temperature are mediated by IL-1. Proc. Natl. Acad. Sci. U.S.A. 96, 7047–7052, https://doi.org/10.1073/pnas.9....
Maciel M.N., Zieba D.A., Amstalden M., Keisler D.H., Neves J.P., Williams G.L., 2004. Chronic administration of recombinant ovine leptin in growing beef heifers: effects on secretion of LH, metabolic hormones, and timing of puberty. J. Anim. Sci. 82, 2930–2936, https://doi.org/10.2527/2004.8....
Michelsen K.S., WongM.H., Shah P.K., Zhang W., Yano J., Doherty TM., Akira S., Rajavashisth T.B., Arditi M., 2004. Lack of Tolllike receptor 4 or myeloid differentiation factor 88 reduces atherosclerosis and alters plaque phenotype in mice deficient in apolipoprotein E. Proc. Natl. Acad. Sci. U. S. A. 101, 10679–10684, https://doi.org/10.1073/pnas.0....
Milani-Nejad N., Janssen P.M.L., 2014. Small and large animal models in cardiac contraction research: advantages and disadvantages. Pharmacol. Therap. 141, 235–249, https://doi.org/10.1016/j.phar....
Mohamed-Ali V., Goodrick S., Bulmer K., Holly J.M.P., Yudkin J.S., Coppack S.W., 1999. Production of soluble tumor necrosis factor receptors by human subcutaneous adipose tissue in vivo. Am. J. Physiol. 277, E971–E975, https://doi.org/10.1152/ajpend....
Protogerou A.D., Zampeli E., Fragiadaki K., Stamatelopoulos K., PapamichaelC., Sfikakis P.P., 2011. A pilot study of endothelial dysfunction and aortic stiffness after interleukin-6 receptor inhibition in rheumatoid arthritis. Atherosclerosis 219, 734–736, https://doi.org/10.1016/j.athe....
Sachot C., Poole S., Luheshi G.N., 2004. Circulating leptin mediates lipopolysaccharide-induced anorexia and fever in rats: Leptin, a circulating mediator of inflammation. J. Physiol. 561, 263–272, https://doi.org/10.1113/jphysi....
Scheiermann C., Kunisaki Y., Frenette P.S., 2013. Circadian control of the immune system. Nat. Rev. Immunol. 13, 190–198, https://doi.org/10.1038/nri338....
Schroeter M.R., Schneiderman J., Schumann B., Glückermann R., Grimmas P., Buchwald A.B., Tirilomis T., Schöndube F.A., Konstantinides S.V., Schäfer K., 2007. Expression of the leptin receptor in different types of vascular lesions. Histochem. Cell Biol. 128, 323–333, https://doi.org/10.1007/s00418....
Shen J., Sakaida I., Uchida K., Terai S., Okita K., 2005. Leptin enhances TNF-α production via p38 and JNK MAPK in LPSstimulated Kupffer cells. Life Sci. 77, 1502–1515, https://doi.org/10.1016/j.lfs.....
Sikka G., Yang R., Reid S., Benjo A., Koitabashi N., Camara A., Baraban E., O’Donnell C.P., Berkowitz D.E., Barouch L.A., Leptin is essential in maintaining normal vascular compliance independent of body weight. Int. J. Obesity 2010, 34, 203–206, https://doi.org/10.1038/ijo.20...
Strzetelski J.A., Brzóska F., Kowalski Z.M., Osięgłowski S., 2014. Feeding Recommendation for Ruminants and Feed Tables (in Polish: Zalecenia Żywieniowe dla Przeżuwaczy i Tabele wartości pokarmowej pasz). National Research Institute of Animal Production. Krakow (Poland).
Su X., Ao L., Shi Y., Johnson T.R., Fullerton D.A., Meng X., 2011. Oxidized low density lipoprotein induces bone morphogenetic protein-2 in coronary artery endothelial cells via Toll-like receptors 2 and 4. J. Biol. Chem. 286, 12213–12220, https://doi.org/10.1074/jbc.M1....
Szczesna M., Zieba D.A., 2015. Phenomenon of leptin resistance in seasonal animals: the failure of leptin action in the brain. Domest. Anim. Endocrinol. 52, 60–70, https://doi.org/10.1016/j.doma....
Taleb S., Haaften R., Henegar C. et al., 2006. Microarray profiling of human white adipose tissue after exogenous leptin injection. Eur. J. Clin. Invest. 36, 153–163, https://doi.org/10.1111/j.1365....
Tousoulis D., Oikonomou E., Economou E.K., Crea F., Kaski J.C., 2016. Inflammatory cytokines in atherosclerosis: current therapeutic approaches. Eur. Heart J. 37, 1723–1732, https://doi.org/10.1093/eurhea....
World Health Organization (WHO), 2011. Global status report on noncommunicable disaeses 2010. Geneva (Switzerland).
Yen T.T., Allan J.A., Pearson D.V., Schinitsky M.R., 1977. Dissociation of obesity, hypercholesterolemia and diabetes from atherosclerosis in ob/ob mice. Experientia 33, 995–996, https://doi.org/10.1007/BF0194....
Yin K., Tang S.L., Yu X.H. et al., 2013. Apolipoprotein A-I inhibits LPS-induced atherosclerosis in ApoE(-/-) mice possibly via activated STAT3-mediated upregulation of tristetraprolin. Acta Pharmacol. Sin. 34, 837–846, https://doi.org/10.1038/aps.20....
Zieba D.A., Szczesna M., Klocek-Gorka B., Williams G.L., 2008. Leptin as a nutritional signal regulating appetite and reproductive processes in seasonally-breeding ruminants. J. Physiol. Pharmacol. 59, Suppl. 9, 7–18.
Effect of Central Injection of Neostigmine on the Bacterial Endotoxin Induced Suppression of GnRH/LH Secretion in Ewes during the Follicular Phase of the Estrous Cycle
Andrzej Herman, Janina Skipor, Agata Krawczyńska, Joanna Bochenek, Karolina Wojtulewicz, Bartosz Pawlina, Hanna Antushevich, Anna Herman, Dorota Tomaszewska-Zaremba
International Journal of Molecular Sciences
The Influence of Photoperiod on the Action of Exogenous Leptin on Gene Expression of Proinflammatory Cytokines and Their Receptors in the Thoracic Perivascular Adipose Tissue (PVAT) in Ewes
Agata Krawczyńska, Andrzej Herman, Hanna Antushevich, Joanna Bochenek, Karolina Wojtulewicz, Dorota Zięba
Mediators of Inflammation
The Impact of Photoperiod on the Leptin Sensitivity and Course of Inflammation in the Anterior Pituitary
Maciej Wójcik, Andrzej Herman, Dorota Zieba, Agata Krawczyńska
International Journal of Molecular Sciences
Interplays between inflammasomes and viruses, bacteria (pathogenic and probiotic), yeasts and parasites
Hanna Antushevich
Immunology Letters
Photoperiod Affects Leptin Action on the Choroid Plexus in Ewes Challenged with Lipopolysaccharide—Study on the mRNA Level
Aleksandra Szczepkowska, Marta Kowalewska, Agata Krawczyńska, Andrzej Herman, Janina Skipor
International Journal of Molecular Sciences
Anandamide Influences Interleukin-1β Synthesis and IL-1 System Gene Expressions in the Ovine Hypothalamus during Endo-Toxin-Induced Inflammation
Monika Tomczyk, Dorota Tomaszewska-Zaremba, Joanna Bochenek, Anna Herman, Andrzej Herman
Photoperiod alters the choroid plexus response to LPS-induced acute inflammation in ewes
Janina Skipor, Aleksandra Szczepkowska, Marta Kowalewska, Małgorzata Domżalska, Andrzej Herman, Agata Krawczyńska
Annals of Animal Science