Skip to main content
Erschienen in: Inflammation 5/2018

09.07.2018 | ORIGINAL ARTICLE

Luteoloside Protects the Uterus from Staphylococcus aureus-Induced Inflammation, Apoptosis, and Injury

verfasst von: Xiaoyan Wang, Ting Yuan, Nannan Yin, Xiaofei Ma, Zhenbiao Zhang, Zhe Zhu, Aftab Shaukat, Ganzhen Deng

Erschienen in: Inflammation | Ausgabe 5/2018

Einloggen, um Zugang zu erhalten

Abstract

Luteoloside is a flavonoid extracted from several natural herbs that exhibits anti-microbial and anti-inflammation properties. Our study mainly identified the anti-inflammatory mechanism of action of luteoloside in Staphylococcus aureus-induced endometritis. Histopathological observations and myeloperoxidase (MPO) activity showed that luteoloside could protect the uterus from S. aureus-induced damage and ameliorate the infiltration of inflammatory cells. Quantitative PCR (qPCR) and ELISA analysis also revealed that luteoloside could decrease the expression of the pro-inflammatory cytokines TNF-α, IL-1β, and IL-6 and increase the expression of the anti-inflammatory cytokine IL-10 both in vivo and in vitro. However, western blot analysis revealed that luteoloside inhibited the expression of TLR2 and IL-8 and inhibited the phosphorylation of IκBα and NF-κB p65. Moreover, luteoloside inhibited the apoptosis of endometrial epithelial cells (EECs), suppressed the phosphorylation of p53, and decreased the expression of caspase-3 induced by S. aureus. Furthermore, this study showed that luteoloside inhibited the expression of Bax but increased the expression of Bcl-2. These results indicate that luteoloside has anti-inflammatory properties by inhibiting the TLR2 and NF-κB signaling pathways and plays an anti-apoptotic role in S. aureus-induced endometritis, which may be valuable for the clinical treatment of S. aureus-induced inflammation.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
1.
Zurück zum Zitat Turner, M.L., G.D. Healey, and I.M. Sheldon. 2012. Immunity and inflammation in the uterus. Reproduction in Domestic Animals. 47: 402–409.CrossRefPubMed Turner, M.L., G.D. Healey, and I.M. Sheldon. 2012. Immunity and inflammation in the uterus. Reproduction in Domestic Animals. 47: 402–409.CrossRefPubMed
2.
Zurück zum Zitat Arlt, S., W. Padberg, M. Drillich, and W. Heuwieser. 2009. Efficacy of homeopathic remedies as prophylaxis of bovine endometritis. Journal of Dairy Science. 92: 4945–4953.CrossRefPubMed Arlt, S., W. Padberg, M. Drillich, and W. Heuwieser. 2009. Efficacy of homeopathic remedies as prophylaxis of bovine endometritis. Journal of Dairy Science. 92: 4945–4953.CrossRefPubMed
3.
Zurück zum Zitat Sheldon, I.M., and J.J. Bromfield. 2011. Innate immunity in the human endometrium and ovary. American Journal of Reproductive Immunology. 66: 63–71.CrossRefPubMed Sheldon, I.M., and J.J. Bromfield. 2011. Innate immunity in the human endometrium and ovary. American Journal of Reproductive Immunology. 66: 63–71.CrossRefPubMed
4.
Zurück zum Zitat Carneiro, L.C., A.F. Ferreira, M. Padua, J.P. Saut, A.S. Ferraudo, and R.M. Santos. 2014. Incidence of subclinical endometritis and its effects on reproductive performance of crossbred dairy cows. Tropical Animal Health and Production. 46: 1435–1439.CrossRefPubMed Carneiro, L.C., A.F. Ferreira, M. Padua, J.P. Saut, A.S. Ferraudo, and R.M. Santos. 2014. Incidence of subclinical endometritis and its effects on reproductive performance of crossbred dairy cows. Tropical Animal Health and Production. 46: 1435–1439.CrossRefPubMed
5.
Zurück zum Zitat Fábián, K., L. Makrai, K. Sachse, L. Szeredi, and L. Egyed. 2008. An investigation of the aetiological role of bovine herpesvirus 4 in bovine endometritis. The Veterinary Journal. 177: 289–292.CrossRefPubMed Fábián, K., L. Makrai, K. Sachse, L. Szeredi, and L. Egyed. 2008. An investigation of the aetiological role of bovine herpesvirus 4 in bovine endometritis. The Veterinary Journal. 177: 289–292.CrossRefPubMed
6.
Zurück zum Zitat Sheldon, I.M., and H. Dobson. 2004. Postpartum uterine health in cattle. Animal Reproduction Science 82–83: 295–306.CrossRefPubMed Sheldon, I.M., and H. Dobson. 2004. Postpartum uterine health in cattle. Animal Reproduction Science 82–83: 295–306.CrossRefPubMed
7.
Zurück zum Zitat Williams, E.J., D.P. Fischer, D.U. Pfeiffer, G.C.W. England, D.E. Noakes, H. Dobson, and I.M. Sheldon. 2005. Clinical evaluation of postpartum vaginal mucus reflects uterine bacterial infection and the immune response in cattle. Theriogenology 63: 102–117.CrossRefPubMed Williams, E.J., D.P. Fischer, D.U. Pfeiffer, G.C.W. England, D.E. Noakes, H. Dobson, and I.M. Sheldon. 2005. Clinical evaluation of postpartum vaginal mucus reflects uterine bacterial infection and the immune response in cattle. Theriogenology 63: 102–117.CrossRefPubMed
8.
Zurück zum Zitat Jadon, R.S., G.S. Dhaliwal, and S.K. Jand. 2005. Prevalence of aerobic and anaerobic uterine bacteria during peripartum period in normal and dystocia-affected buffaloes. Animal Reproduction Science 88: 215–224.CrossRefPubMed Jadon, R.S., G.S. Dhaliwal, and S.K. Jand. 2005. Prevalence of aerobic and anaerobic uterine bacteria during peripartum period in normal and dystocia-affected buffaloes. Animal Reproduction Science 88: 215–224.CrossRefPubMed
9.
Zurück zum Zitat Veni, J.K., G. Bhat, S.M. Shalini, P. Kumar, M. Chakrapani, and S. Baliga. 2015. Community-acquired methicillin resistant staphylococcus aureus bacteremia: case series. Kathmandu University Medical Journal (KUMJ). 13: 77–79.CrossRefPubMed Veni, J.K., G. Bhat, S.M. Shalini, P. Kumar, M. Chakrapani, and S. Baliga. 2015. Community-acquired methicillin resistant staphylococcus aureus bacteremia: case series. Kathmandu University Medical Journal (KUMJ). 13: 77–79.CrossRefPubMed
10.
Zurück zum Zitat Ghasemi, F., P. Gonzalez-Cano, P.J. Griebel, and C. Palmer. 2012. Proinflammatory cytokine gene expression in endometrial cytobrush samples harvested from cows with and without subclinical endometritis. Theriogenology 78: 1538–1547.CrossRefPubMed Ghasemi, F., P. Gonzalez-Cano, P.J. Griebel, and C. Palmer. 2012. Proinflammatory cytokine gene expression in endometrial cytobrush samples harvested from cows with and without subclinical endometritis. Theriogenology 78: 1538–1547.CrossRefPubMed
11.
Zurück zum Zitat Lien, E., T.J. Sellati, A. Yoshimura, T.H. Flo, G. Rawadi, R.W. Finberg, J.D. Carroll, T. Espevik, R.R. Ingalls, J.D. Radolf, and D.T. Golenbock. 1999. Toll-like receptor 2 functions as a pattern recognition receptor for diverse bacterial products. Journal of Biological Chemistry. 274: 33419–33425.CrossRefPubMed Lien, E., T.J. Sellati, A. Yoshimura, T.H. Flo, G. Rawadi, R.W. Finberg, J.D. Carroll, T. Espevik, R.R. Ingalls, J.D. Radolf, and D.T. Golenbock. 1999. Toll-like receptor 2 functions as a pattern recognition receptor for diverse bacterial products. Journal of Biological Chemistry. 274: 33419–33425.CrossRefPubMed
12.
Zurück zum Zitat Liu, Y., C. Qiu, W. Li, W. Mu, C. Li, and M. Guo. 2016. Selenium plays a protective role in Staphylococcus aureus-induced endometritis in the uterine tissue of rats. Biological Trace Element Research. 173: 1–9.CrossRef Liu, Y., C. Qiu, W. Li, W. Mu, C. Li, and M. Guo. 2016. Selenium plays a protective role in Staphylococcus aureus-induced endometritis in the uterine tissue of rats. Biological Trace Element Research. 173: 1–9.CrossRef
13.
Zurück zum Zitat Guo, M.Y., W.Y. Li, Z. Zhang, C. Qiu, C. Li, and G. Deng. 2015. Betulin suppresses S. aureus-induced mammary gland inflammatory injury by regulating PPAR-γ in mice. International Immunopharmacology 29: 824–831.CrossRefPubMed Guo, M.Y., W.Y. Li, Z. Zhang, C. Qiu, C. Li, and G. Deng. 2015. Betulin suppresses S. aureus-induced mammary gland inflammatory injury by regulating PPAR-γ in mice. International Immunopharmacology 29: 824–831.CrossRefPubMed
14.
Zurück zum Zitat Sabroe, I., S.K. Dower, and M.K. Whyte. 2005. The role of Toll-like receptors in the regulation of neutrophil migration, activation, and apoptosis. Clinical Infectious Diseases. 41 (Suppl 7): S421–S426.CrossRefPubMed Sabroe, I., S.K. Dower, and M.K. Whyte. 2005. The role of Toll-like receptors in the regulation of neutrophil migration, activation, and apoptosis. Clinical Infectious Diseases. 41 (Suppl 7): S421–S426.CrossRefPubMed
15.
Zurück zum Zitat Sun, X., G.B. Sun, M. Wang, J. Xiao, and X.B. Sun. 2011. Protective effects of cynaroside against H(2)O(2)-induced apoptosis in H9c2 cardiomyoblasts. Journal of Cellular Biochemistry 112: 2019–2029.CrossRefPubMed Sun, X., G.B. Sun, M. Wang, J. Xiao, and X.B. Sun. 2011. Protective effects of cynaroside against H(2)O(2)-induced apoptosis in H9c2 cardiomyoblasts. Journal of Cellular Biochemistry 112: 2019–2029.CrossRefPubMed
16.
Zurück zum Zitat Xiong, J., S. Li, W. Wang, Y. Hong, K. Tang, and Q. Luo. 2013. Screening and identification of the antibacterial bioactive compounds from Lonicera japonica Thunb. Leaves. Food chemistry. 138: 327–333.CrossRefPubMed Xiong, J., S. Li, W. Wang, Y. Hong, K. Tang, and Q. Luo. 2013. Screening and identification of the antibacterial bioactive compounds from Lonicera japonica Thunb. Leaves. Food chemistry. 138: 327–333.CrossRefPubMed
17.
Zurück zum Zitat Baskar, A.A., S. Ignacimuthu, G.P. Michael, and K.S. Al Numair. 2011. Cancer chemopreventive potential of luteolin-7-O-glucoside isolated from Ophiorrhiza mungos Linn. Nutrition and cancer. 63: 130–138.PubMed Baskar, A.A., S. Ignacimuthu, G.P. Michael, and K.S. Al Numair. 2011. Cancer chemopreventive potential of luteolin-7-O-glucoside isolated from Ophiorrhiza mungos Linn. Nutrition and cancer. 63: 130–138.PubMed
18.
Zurück zum Zitat Park, C.M., and Y.S. Song. 2013. Luteolin and luteolin-7-O-glucoside inhibit lipopolysaccharide-induced inflammatory responses through modulation of NF-kappaB/AP-1/PI3K-Akt signaling cascades in RAW 264.7 cells. Nutrition Research and Practice. 7: 423–429.CrossRefPubMedPubMedCentral Park, C.M., and Y.S. Song. 2013. Luteolin and luteolin-7-O-glucoside inhibit lipopolysaccharide-induced inflammatory responses through modulation of NF-kappaB/AP-1/PI3K-Akt signaling cascades in RAW 264.7 cells. Nutrition Research and Practice. 7: 423–429.CrossRefPubMedPubMedCentral
19.
Zurück zum Zitat Song, Y.S., and C.M. Park. 2014. Luteolin and luteolin-7-O-glucoside strengthen antioxidative potential through the modulation of Nrf2/MAPK mediated HO-1 signaling cascade in RAW 264.7 cells. Food and Chemical Toxicology: An International Journal Published for the British Industrial Biological Research Association. 65: 70–75.CrossRef Song, Y.S., and C.M. Park. 2014. Luteolin and luteolin-7-O-glucoside strengthen antioxidative potential through the modulation of Nrf2/MAPK mediated HO-1 signaling cascade in RAW 264.7 cells. Food and Chemical Toxicology: An International Journal Published for the British Industrial Biological Research Association. 65: 70–75.CrossRef
20.
Zurück zum Zitat Josse, J., F. Velard, and S.C. Gangloff. 2015. Staphylococcus aureus vs. osteoblast: relationship and consequences in osteomyelitis. Frontiers in Cellular and Infection Microbiology. 5: 85.CrossRefPubMedPubMedCentral Josse, J., F. Velard, and S.C. Gangloff. 2015. Staphylococcus aureus vs. osteoblast: relationship and consequences in osteomyelitis. Frontiers in Cellular and Infection Microbiology. 5: 85.CrossRefPubMedPubMedCentral
21.
Zurück zum Zitat Jiang K, Chen X, Zhao G, Wu H, Mi J, Qiu C, et al. 2017. IFN-τ plays an anti-inflammatory role in Staphylococcus aureus-induced endometritis in mice through the suppression of NF-κB pathway and MMP9 expression. Journal of Interferon & Cytokine Research the Official Journal of the International Society for Interferon & Cytokine Research 37. Jiang K, Chen X, Zhao G, Wu H, Mi J, Qiu C, et al. 2017. IFN-τ plays an anti-inflammatory role in Staphylococcus aureus-induced endometritis in mice through the suppression of NF-κB pathway and MMP9 expression. Journal of Interferon & Cytokine Research the Official Journal of the International Society for Interferon & Cytokine Research 37.
22.
Zurück zum Zitat Dolezel, R., T. Palenik, S. Cech, L. Kohoutova, and M. Vyskocil. 2010. Bacterial contamination of the uterus in cows with various clinical types of metritis and endometritis and use of hydrogen peroxide for intrauterine treatment. Veterinární Medicína 55: 504–511.CrossRef Dolezel, R., T. Palenik, S. Cech, L. Kohoutova, and M. Vyskocil. 2010. Bacterial contamination of the uterus in cows with various clinical types of metritis and endometritis and use of hydrogen peroxide for intrauterine treatment. Veterinární Medicína 55: 504–511.CrossRef
23.
Zurück zum Zitat Zahid, I.A. 2004. Culture and sensitivity of bacterial growth from exotic cows suffering from endometritis under Pakistani conditions. Pakistan Veterinary Journal. 24: 107–108. Zahid, I.A. 2004. Culture and sensitivity of bacterial growth from exotic cows suffering from endometritis under Pakistani conditions. Pakistan Veterinary Journal. 24: 107–108.
24.
Zurück zum Zitat Cotton, J.A., J.-P. Motta, L.P. Schenck, S.A. Hirota, P.L. Beck, and A.G. Buret. 2014. Giardia duodenalis infection reduces granulocyte infiltration in an in vivo model of bacterial toxin-induced colitis and attenuates inflammation in human intestinal tissue. PLoS One 9: e109087.CrossRefPubMedPubMedCentral Cotton, J.A., J.-P. Motta, L.P. Schenck, S.A. Hirota, P.L. Beck, and A.G. Buret. 2014. Giardia duodenalis infection reduces granulocyte infiltration in an in vivo model of bacterial toxin-induced colitis and attenuates inflammation in human intestinal tissue. PLoS One 9: e109087.CrossRefPubMedPubMedCentral
25.
Zurück zum Zitat Shav, D., R. Gotlieb, U. Zaretsky, D. Elad, and S. Einav. 2014. Wall shear stress effects on endothelial-endothelial and endothelial-smooth muscle cell interactions in tissue engineered models of the vascular wall. PLoS One 9: e88304.CrossRefPubMedPubMedCentral Shav, D., R. Gotlieb, U. Zaretsky, D. Elad, and S. Einav. 2014. Wall shear stress effects on endothelial-endothelial and endothelial-smooth muscle cell interactions in tissue engineered models of the vascular wall. PLoS One 9: e88304.CrossRefPubMedPubMedCentral
26.
Zurück zum Zitat Pande, M., G.K. Das, F.A. Khan, M. Sarkar, M.C. Pathak, J.K. Prasad, and H. Kumar. 2013. Endometritis impairs luteal development, function, and nitric oxide and ascorbic acid concentrations in buffalo (Bubalus bubalis). Tropical Animal Health and Production. 45: 805–810.CrossRefPubMed Pande, M., G.K. Das, F.A. Khan, M. Sarkar, M.C. Pathak, J.K. Prasad, and H. Kumar. 2013. Endometritis impairs luteal development, function, and nitric oxide and ascorbic acid concentrations in buffalo (Bubalus bubalis). Tropical Animal Health and Production. 45: 805–810.CrossRefPubMed
27.
Zurück zum Zitat Potter, T.J., J. Guitian, J. Fishwick, P.J. Gordon, and I.M. Sheldon. 2010. Risk factors for clinical endometritis in postpartum dairy cattle. Theriogenology 74: 127–134.CrossRefPubMed Potter, T.J., J. Guitian, J. Fishwick, P.J. Gordon, and I.M. Sheldon. 2010. Risk factors for clinical endometritis in postpartum dairy cattle. Theriogenology 74: 127–134.CrossRefPubMed
28.
Zurück zum Zitat Lembo, A., C. Kalis, C.J. Kirschning, V. Mitolo, E. Jirillo, H. Wagner, C. Galanos, and M.A. Freudenberg. 2003. Differential contribution of Toll-like receptors 4 and 2 to the cytokine response to Salmonella enterica serovar Typhimurium and Staphylococcus aureus in mice. Infection and Immunity. 71: 6058–6062.CrossRefPubMedPubMedCentral Lembo, A., C. Kalis, C.J. Kirschning, V. Mitolo, E. Jirillo, H. Wagner, C. Galanos, and M.A. Freudenberg. 2003. Differential contribution of Toll-like receptors 4 and 2 to the cytokine response to Salmonella enterica serovar Typhimurium and Staphylococcus aureus in mice. Infection and Immunity. 71: 6058–6062.CrossRefPubMedPubMedCentral
29.
Zurück zum Zitat Liang, Y., Y. Zhou, and P. Shen. 2004. NF-kappaB and its regulation on the immune system. Cellular & Molecular Immunology 1: 343–350. Liang, Y., Y. Zhou, and P. Shen. 2004. NF-kappaB and its regulation on the immune system. Cellular & Molecular Immunology 1: 343–350.
30.
Zurück zum Zitat Gao X, Zhang Z, Li Y, Hu X, Shen P, Fu Y, et al. 2015. Selenium deficiency deteriorate the inflammation of S. aureus infection via regulating NF-kappaB and PPAR-gamma in mammary gland of mice. Biological Trace Element Research. Gao X, Zhang Z, Li Y, Hu X, Shen P, Fu Y, et al. 2015. Selenium deficiency deteriorate the inflammation of S. aureus infection via regulating NF-kappaB and PPAR-gamma in mammary gland of mice. Biological Trace Element Research.
31.
Zurück zum Zitat Guo, M.Y., W.Y. Li, Z. Zhang, C. Qiu, C. Li, and G. Deng. 2015. Betulin suppresses S. aureus-induced mammary gland inflammatory injury by regulating PPAR-gamma in mice. International Immunopharmacology 29: 824–831.CrossRefPubMed Guo, M.Y., W.Y. Li, Z. Zhang, C. Qiu, C. Li, and G. Deng. 2015. Betulin suppresses S. aureus-induced mammary gland inflammatory injury by regulating PPAR-gamma in mice. International Immunopharmacology 29: 824–831.CrossRefPubMed
32.
Zurück zum Zitat Bi CL, Wang H, Wang YJ, Sun J, Dong JS, Meng X, et al. 2016. Selenium inhibits Staphylococcus aureus-induced inflammation by suppressing the activation of the NF-kappaB and MAPK signalling pathways in RAW264.7 macrophages. European Journal of Pharmacology. Bi CL, Wang H, Wang YJ, Sun J, Dong JS, Meng X, et al. 2016. Selenium inhibits Staphylococcus aureus-induced inflammation by suppressing the activation of the NF-kappaB and MAPK signalling pathways in RAW264.7 macrophages. European Journal of Pharmacology.
33.
Zurück zum Zitat Culmsee, C., and M.P. Mattson. 2005. p53 in neuronal apoptosis. Biochemical and Biophysical Research Communications. 331: 761–777.CrossRefPubMed Culmsee, C., and M.P. Mattson. 2005. p53 in neuronal apoptosis. Biochemical and Biophysical Research Communications. 331: 761–777.CrossRefPubMed
34.
Zurück zum Zitat Arroyo, D.S., Soria, J.A., Gaviglio, E.A., Garcia-Keller, C., Cancela, L.M., Rodriguez-Galan, M.C., Wang, J.M. and Iribarren, P. (2013). Toll-like receptor 2 ligands promote microglial cell death by inducing autophagy. FASEB J 27, 299–312. Arroyo, D.S., Soria, J.A., Gaviglio, E.A., Garcia-Keller, C., Cancela, L.M., Rodriguez-Galan, M.C., Wang, J.M. and Iribarren, P. (2013). Toll-like receptor 2 ligands promote microglial cell death by inducing autophagy. FASEB J 27, 299–312.
35.
Zurück zum Zitat Chipuk, J.E., Kuwana, T., Bouchier-Hayes, L., Droin, N.M., Newmeyer, D.D., Schuler, M. and Green, D.R. (2004). Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 303, 1010-4. Chipuk, J.E., Kuwana, T., Bouchier-Hayes, L., Droin, N.M., Newmeyer, D.D., Schuler, M. and Green, D.R. (2004). Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 303, 1010-4.
36.
Zurück zum Zitat Shi, L., Chen, J., Yang, J., Pan, T., Zhang, S. and Wang, Z. (2010). MiR-21 protected human glioblastoma U87MG cells from chemotherapeutic drug temozolomide induced apoptosis by decreasing Bax/Bcl-2 ratio and caspase-3 activity. Brain Res 1352, 255–64. Shi, L., Chen, J., Yang, J., Pan, T., Zhang, S. and Wang, Z. (2010). MiR-21 protected human glioblastoma U87MG cells from chemotherapeutic drug temozolomide induced apoptosis by decreasing Bax/Bcl-2 ratio and caspase-3 activity. Brain Res 1352, 255–64.
37.
Zurück zum Zitat Harburg, G.C., Hall, F.S., Harrist, A.V., Sora, I., Uhl, G.R. and Eisch, A.J. (2007). Knockout of the mu opioid receptor enhances the survival of adult-generated hippocampal granule cell neurons. Neuroscience 144, 77–87. Harburg, G.C., Hall, F.S., Harrist, A.V., Sora, I., Uhl, G.R. and Eisch, A.J. (2007). Knockout of the mu opioid receptor enhances the survival of adult-generated hippocampal granule cell neurons. Neuroscience 144, 77–87.
Metadaten
Titel
Luteoloside Protects the Uterus from Staphylococcus aureus-Induced Inflammation, Apoptosis, and Injury
verfasst von
Xiaoyan Wang
Ting Yuan
Nannan Yin
Xiaofei Ma
Zhenbiao Zhang
Zhe Zhu
Aftab Shaukat
Ganzhen Deng
Publikationsdatum
09.07.2018
Verlag
Springer US
Erschienen in
Inflammation / Ausgabe 5/2018
Print ISSN: 0360-3997
Elektronische ISSN: 1573-2576
DOI
https://doi.org/10.1007/s10753-018-0814-7

Weitere Artikel der Ausgabe 5/2018

Inflammation 5/2018 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.