Skip to main content
Top
Published in: Chinese Medicine 1/2018

Open Access 01-12-2018 | Research

Metabonomic study of the protective effect of Fukeqianjin formula on multi-pathogen induced pelvic inflammatory disease in rats

Authors: Yan Zhang, Wei Li, Liang Zou, Yun Gong, Peng Zhang, Shasha Xing, Hang Yang

Published in: Chinese Medicine | Issue 1/2018

Login to get access

Abstract

Background

Fukeqianjin formula has been effectively used in the treatment of pelvic inflammatory disease (PID) and the related complications in clinic. Although there have been some studies about the underlying mechanism that focus on its anti-inflammatory and immunoregulatory activities. But the mechanism is still not fully understood. The aim of this study was to investigate the alteration of plasma metabolic profiles in PID rats and the regulatory effect of Fukeqianjin formula on potential biomarkers.

Methods

Pelvic inflammatory model was established by intrauterine inoculation of multiple pathogens combined with mechanical injury of endometrium. Rats were randomly divided into normal group, model group, azithromycin group, high-and low-dose of Fukeqianjin formula treatment group (FF-H, and FF-L, respectively). After 14 days of intragastric administration, the plasm levels of interleukin-1β (IL-1β) and nitric oxide (NO) were measured. To further recognize and identify potential biomarkers and metabolic pathways, an ultra-performance liquid chromatography-quadrupole-Exactive Orbitrap-mass spectrometry (UPLC-Q-Exactive Orbitrap-MS) metabonomic method combined with multivariate analyses including principal component analysis (PCA), partial least squares discriminant analysis (PLS-DA) and orthogonal partial least squares discriminant analysis (OPLS-DA), was employed to analyze the metabolic profiling.

Results

Compared with normal group, the plasma levels of IL-1β and NO were significantly increased in the PID model group (P < 0. 05), and obviously decreased after high-dose intervention of Fukeqianjin formula (P < 0. 01). The PCA, PLS-DA and OPLS-DA analysis showed that PID rats were clearly separated from normal rats. Compared with the PID model group, the metabolite profiles of Fukeqianjin formula treatment group was gradually restored to normal. Meanwhile, 14 potential metabolite biomarkers, which were mainly related to the metabolic pathways of intervening glycerophospholipid metabolism, linoleic acid metabolism/alpha-linolenic acid metabolism, amino acid metabolism, arachidonic acid metabolism, and unsaturated fatty acids biosynthesis, have been identified. Fukeqianjin formula exerts good regulatory effect on the abnormal metabolism of PID rats.

Conclusions

Intrauterine inoculation of multiple pathogens combined with mechanical injury of endometrium could significantly disturb the plasma metabolic profiles of rats. Fukeqianjin formula has potential therapeutic effect on multi-pathogen-induced PID by ameliorating metabolism disorders and alleviating the inflammatory response.
Appendix
Available only for authorised users
Literature
1.
go back to reference Mitchell C, Prabhu M. Pelvic inflammatory disease: current concepts in pathogenesis, diagnosis and treatment. Infect Dis Clin N Am. 2013;27(4):793–809.CrossRef Mitchell C, Prabhu M. Pelvic inflammatory disease: current concepts in pathogenesis, diagnosis and treatment. Infect Dis Clin N Am. 2013;27(4):793–809.CrossRef
2.
go back to reference Haggerty CL, Schulz R, Ness RB. Lower quality of life among women with chronic pelvic pain after pelvic inflammatory disease. Obstet Gynecol. 2003;102(5 Pt 1):934–9.PubMed Haggerty CL, Schulz R, Ness RB. Lower quality of life among women with chronic pelvic pain after pelvic inflammatory disease. Obstet Gynecol. 2003;102(5 Pt 1):934–9.PubMed
3.
go back to reference Zhou Z, Zeng F, Yuan J, Tang J, Colditz GA, Tworoger SS, et al. Pelvic inflammatory disease and the risk of ovarian cancer: a meta-analysis. Cancer Causes Control. 2017;28(5):415–28.CrossRefPubMedPubMedCentral Zhou Z, Zeng F, Yuan J, Tang J, Colditz GA, Tworoger SS, et al. Pelvic inflammatory disease and the risk of ovarian cancer: a meta-analysis. Cancer Causes Control. 2017;28(5):415–28.CrossRefPubMedPubMedCentral
5.
go back to reference Haggerty CL, Totten PA, Tang G, Astete SG, Ferris MJ, Norori J, et al. Identification of novel microbes associated with pelvic inflammatory disease and infertility. Sex Transm Infect. 2016;92(6):441–6.CrossRefPubMedPubMedCentral Haggerty CL, Totten PA, Tang G, Astete SG, Ferris MJ, Norori J, et al. Identification of novel microbes associated with pelvic inflammatory disease and infertility. Sex Transm Infect. 2016;92(6):441–6.CrossRefPubMedPubMedCentral
6.
go back to reference Spencer TH, Umeh PO, Irokanulo E, Baba MM, Spencer BB, Umar AI, et al. Bacterial isolates associated with pelvic inflammatory disease among female patients attending some hospitals in Abuja, Nigeria. Afr J Infect Dis. 2014;8(1):9–13.PubMedPubMedCentral Spencer TH, Umeh PO, Irokanulo E, Baba MM, Spencer BB, Umar AI, et al. Bacterial isolates associated with pelvic inflammatory disease among female patients attending some hospitals in Abuja, Nigeria. Afr J Infect Dis. 2014;8(1):9–13.PubMedPubMedCentral
7.
go back to reference Bevan CD, Ridgway GL, Rothermel CD. Efficacy and safety of azithromycin as monotherapy or combined with metronidazole compared with two standard multidrug regimens for the treatment of acute pelvic inflammatory disease. J Int Med Res. 2003;31(1):45–54.CrossRefPubMed Bevan CD, Ridgway GL, Rothermel CD. Efficacy and safety of azithromycin as monotherapy or combined with metronidazole compared with two standard multidrug regimens for the treatment of acute pelvic inflammatory disease. J Int Med Res. 2003;31(1):45–54.CrossRefPubMed
8.
go back to reference Piyadigamage A, Wilson J. Improvement in the clinical cure rate of outpatient management of pelvic inflammatory disease following a change in therapy. Sex Transm Infect. 2005;81(3):233–5.CrossRefPubMedPubMedCentral Piyadigamage A, Wilson J. Improvement in the clinical cure rate of outpatient management of pelvic inflammatory disease following a change in therapy. Sex Transm Infect. 2005;81(3):233–5.CrossRefPubMedPubMedCentral
9.
go back to reference Ness RB, Soper DE, Holley RL, Peipert J, Randall H, Sweet RL, et al. Effectiveness of inpatient and outpatient treatment strategies for women with pelvic inflammatory disease: results from the pelvic inflammatory disease evaluation and clinical health (peach) randomized trial. Am J Obstet Gynecol. 2002;186(5):929–37.CrossRefPubMed Ness RB, Soper DE, Holley RL, Peipert J, Randall H, Sweet RL, et al. Effectiveness of inpatient and outpatient treatment strategies for women with pelvic inflammatory disease: results from the pelvic inflammatory disease evaluation and clinical health (peach) randomized trial. Am J Obstet Gynecol. 2002;186(5):929–37.CrossRefPubMed
10.
go back to reference Zhou J, Qu F. Treating gynaecological disorders with traditional Chinese medicine: a review. Afr J Tradit Complement Altern Med. 2009;6(4):494–517.PubMedPubMedCentral Zhou J, Qu F. Treating gynaecological disorders with traditional Chinese medicine: a review. Afr J Tradit Complement Altern Med. 2009;6(4):494–517.PubMedPubMedCentral
11.
go back to reference Zheng Y, Jin Y, Zhu HB, Xu ST, Xia YX, Huang Y. The anti-inflammatory and anti-nociceptive activities of Patrinia villosa and its mechanism on the proinflammatory cytokines of rats with pelvic inflammation. Afr J Tradit Complement Altern Med. 2012;9(3):295–302.PubMedPubMedCentral Zheng Y, Jin Y, Zhu HB, Xu ST, Xia YX, Huang Y. The anti-inflammatory and anti-nociceptive activities of Patrinia villosa and its mechanism on the proinflammatory cytokines of rats with pelvic inflammation. Afr J Tradit Complement Altern Med. 2012;9(3):295–302.PubMedPubMedCentral
12.
go back to reference Bu X, Liu Y, Lu Q, Jin Z. Effects of “danzhi decoction” on chronic pelvic pain, hemodynamics, and proinflammatory factors in the murine model of sequelae of pelvic inflammatory disease. Evid Based Complement Altern Med. 2015;2015:547251.CrossRef Bu X, Liu Y, Lu Q, Jin Z. Effects of “danzhi decoction” on chronic pelvic pain, hemodynamics, and proinflammatory factors in the murine model of sequelae of pelvic inflammatory disease. Evid Based Complement Altern Med. 2015;2015:547251.CrossRef
13.
go back to reference Oh Y, Kwon YS, Jung BD. Anti-inflammatory effects of the natural compounds cortex Phellodendri and Humulus japonicus on pelvic inflammatory disease in mice. Int J Med Sci. 2017;14(8):729–34.CrossRefPubMedPubMedCentral Oh Y, Kwon YS, Jung BD. Anti-inflammatory effects of the natural compounds cortex Phellodendri and Humulus japonicus on pelvic inflammatory disease in mice. Int J Med Sci. 2017;14(8):729–34.CrossRefPubMedPubMedCentral
14.
go back to reference Li Y, Liu Y, Yang Q, Shi Z, Xie Y, Wang S. Anti-inflammatory effect of Feiyangchangweiyan capsule on rat pelvic inflammatory disease through JNK/NF-κB pathway. Evid Based Complement Altern Med. 2018;2018:8476147. Li Y, Liu Y, Yang Q, Shi Z, Xie Y, Wang S. Anti-inflammatory effect of Feiyangchangweiyan capsule on rat pelvic inflammatory disease through JNK/NF-κB pathway. Evid Based Complement Altern Med. 2018;2018:8476147.
15.
go back to reference Yuan J, Guo J, Wu C, Yue Z, Zeng G. Effect of Qianjin tablets on serum IgA, IgG and IgM in acute pelvic inflammation in rats. J TCM Univ Hunan. 2010;30(9):87–9 (In Chinese). Yuan J, Guo J, Wu C, Yue Z, Zeng G. Effect of Qianjin tablets on serum IgA, IgG and IgM in acute pelvic inflammation in rats. J TCM Univ Hunan. 2010;30(9):87–9 (In Chinese).
16.
go back to reference Lu Y, Qu J, Guo J, Zuo Z, Shi Z, Wang X, Gui L. Effect of Fuke Qianjin tablet on TNF-α and IL-2 mRNA transcription in the uteri and ovary tissues of acute pelvic inflammatory disease in rats. Chin Tradit Patent Med. 2012;34(1):29–33 (In Chinese). Lu Y, Qu J, Guo J, Zuo Z, Shi Z, Wang X, Gui L. Effect of Fuke Qianjin tablet on TNF-α and IL-2 mRNA transcription in the uteri and ovary tissues of acute pelvic inflammatory disease in rats. Chin Tradit Patent Med. 2012;34(1):29–33 (In Chinese).
17.
go back to reference Li X, Guo J, Shi Z, Nie J. Effect of Fuke Qianjin tablets on inflammatory cytokines in blood serum in rats with chronic pelvic inflammatory disease. Chin J Exp Tradit Med Formulae. 2013;19(10):226–8 (In Chinese). Li X, Guo J, Shi Z, Nie J. Effect of Fuke Qianjin tablets on inflammatory cytokines in blood serum in rats with chronic pelvic inflammatory disease. Chin J Exp Tradit Med Formulae. 2013;19(10):226–8 (In Chinese).
18.
go back to reference Nie J, Li X, Shi Z, Guo J. Influence of FukeQianjin tablets to rat’s caspase-3 and caspase-8 expression of ovary with chronic pelvic inflammatory disease. Northwest Pharm J. 2014;29(4):385–7 (In Chinese). Nie J, Li X, Shi Z, Guo J. Influence of FukeQianjin tablets to rat’s caspase-3 and caspase-8 expression of ovary with chronic pelvic inflammatory disease. Northwest Pharm J. 2014;29(4):385–7 (In Chinese).
19.
go back to reference Wang X, Sun H, Zhang A, Sun W, Wang P, Wang Z. Potential role of metabolomics apporoaches in the area of traditional Chinese medicine: as pillars of the bridge between Chinese and Western medicine. J Pharm Biomed Anal. 2011;55(5):859–68.CrossRefPubMed Wang X, Sun H, Zhang A, Sun W, Wang P, Wang Z. Potential role of metabolomics apporoaches in the area of traditional Chinese medicine: as pillars of the bridge between Chinese and Western medicine. J Pharm Biomed Anal. 2011;55(5):859–68.CrossRefPubMed
20.
go back to reference Dai M, Wang F, Zou Z, Xiao G, Chen H, Yang H. Metabolic regulations of a decoction of Hedyotis diffusa in acute liver injury of mouse models. Chin Med. 2017;12:35.CrossRefPubMedPubMedCentral Dai M, Wang F, Zou Z, Xiao G, Chen H, Yang H. Metabolic regulations of a decoction of Hedyotis diffusa in acute liver injury of mouse models. Chin Med. 2017;12:35.CrossRefPubMedPubMedCentral
21.
go back to reference Jiang H, Qin XJ, Li WP, Ma R, Wang T, Li ZQ. Effects of Shu Gan Jian Pi formula on rats with carbon tetrachloride-induced liver fibrosis using serum metabonomics based on gas chromatography-time of flight mass spectrometry. Mol Med Rep. 2017;16(4):3901–9.CrossRefPubMedPubMedCentral Jiang H, Qin XJ, Li WP, Ma R, Wang T, Li ZQ. Effects of Shu Gan Jian Pi formula on rats with carbon tetrachloride-induced liver fibrosis using serum metabonomics based on gas chromatography-time of flight mass spectrometry. Mol Med Rep. 2017;16(4):3901–9.CrossRefPubMedPubMedCentral
22.
go back to reference Zou W, Wen X, Sheng X, Zheng YI, Xiao Z, Luo J, et al. Gas chromatography-mass spectrometric method-based urine metabolomic profile of rats with pelvic inflammatory disease. Exp Ther Med. 2016;11(5):1653–60.CrossRefPubMedPubMedCentral Zou W, Wen X, Sheng X, Zheng YI, Xiao Z, Luo J, et al. Gas chromatography-mass spectrometric method-based urine metabolomic profile of rats with pelvic inflammatory disease. Exp Ther Med. 2016;11(5):1653–60.CrossRefPubMedPubMedCentral
23.
go back to reference Zou W, Wen X, Zheng Y, Xiao Z, Luo J, Chen S, et al. Metabolomic study on the preventive effect of Patrinia scabiosaefolia Fisch on multipathogen induced pelvic inflammatory disease in rats. Evid Based Complement Altern Med. 2015;2015:170792.CrossRef Zou W, Wen X, Zheng Y, Xiao Z, Luo J, Chen S, et al. Metabolomic study on the preventive effect of Patrinia scabiosaefolia Fisch on multipathogen induced pelvic inflammatory disease in rats. Evid Based Complement Altern Med. 2015;2015:170792.CrossRef
24.
go back to reference Niedbala W, Alves-Filho JC, Fukada SY, Vieira SM, Mitani A, Sonego F, et al. Regulation of type 17 helper T-cell function by nitric oxide during inflammation. Proc Natl Acad Sci USA. 2011;108(22):9220–5.CrossRefPubMed Niedbala W, Alves-Filho JC, Fukada SY, Vieira SM, Mitani A, Sonego F, et al. Regulation of type 17 helper T-cell function by nitric oxide during inflammation. Proc Natl Acad Sci USA. 2011;108(22):9220–5.CrossRefPubMed
25.
go back to reference Xu L, Zhu J, Yin W, Ding X. Astaxanthin improves cognitive deficits from oxidative stress, nitric oxide synthase and inflammation through upregulation of PI3K/Akt in diabetes rat. Int J Clin Exp Pathol. 2015;8(6):6083–94.PubMedPubMedCentral Xu L, Zhu J, Yin W, Ding X. Astaxanthin improves cognitive deficits from oxidative stress, nitric oxide synthase and inflammation through upregulation of PI3K/Akt in diabetes rat. Int J Clin Exp Pathol. 2015;8(6):6083–94.PubMedPubMedCentral
26.
go back to reference Zhou MX, Wei X, Li AL, Wang AM, Lu LZ, Yang Y, et al. Screening of traditional Chinese medicines with therapeutic potential on chronic obstructive pulmonary disease through inhibiting oxidative stress and inflammatory response. BMC Complement Altern Med. 2016;16:360.CrossRefPubMedPubMedCentral Zhou MX, Wei X, Li AL, Wang AM, Lu LZ, Yang Y, et al. Screening of traditional Chinese medicines with therapeutic potential on chronic obstructive pulmonary disease through inhibiting oxidative stress and inflammatory response. BMC Complement Altern Med. 2016;16:360.CrossRefPubMedPubMedCentral
27.
go back to reference Ying X, Chen X, Cheng S, Shen Y, Peng L, Xu HZ. Piperine inhibits IL-β induced expression of inflammatory mediators in human osteoarthritis chondrocyte. Int Immunopharmacol. 2013;17(2):293–9.CrossRefPubMed Ying X, Chen X, Cheng S, Shen Y, Peng L, Xu HZ. Piperine inhibits IL-β induced expression of inflammatory mediators in human osteoarthritis chondrocyte. Int Immunopharmacol. 2013;17(2):293–9.CrossRefPubMed
28.
go back to reference Wu MY, Chao KH, Yang JH, Lee TH, Yang YS, Ho HN. Nitric oxide synthesis is increased in the endometrial tissue of women with endometriosis. Hum Reprod. 2003;18(12):2668–71.CrossRefPubMed Wu MY, Chao KH, Yang JH, Lee TH, Yang YS, Ho HN. Nitric oxide synthesis is increased in the endometrial tissue of women with endometriosis. Hum Reprod. 2003;18(12):2668–71.CrossRefPubMed
29.
go back to reference Rocha MG, Gomes VA, Tanus-Santos JE, Rosa-e-Silva JC, Candido-dos-Reis FJ, Nogueira AA, et al. Reduction of blood nitric oxide levels is associated with clinical improvement of the chronic pelvic pain related to endometriosis. Braz J Med Biol Res. 2015;48(4):363–9.CrossRefPubMedPubMedCentral Rocha MG, Gomes VA, Tanus-Santos JE, Rosa-e-Silva JC, Candido-dos-Reis FJ, Nogueira AA, et al. Reduction of blood nitric oxide levels is associated with clinical improvement of the chronic pelvic pain related to endometriosis. Braz J Med Biol Res. 2015;48(4):363–9.CrossRefPubMedPubMedCentral
30.
go back to reference Cheng W, Shivshankar P, Li Z, Chen L, Yeh IT, Zhong G. Caspase-1 contributes to Chlamydia trachomatis-induced upper urogenital tract inflammatory pathologies without affecting the course of infection. Infect Immun. 2008;76(2):515–22.CrossRefPubMed Cheng W, Shivshankar P, Li Z, Chen L, Yeh IT, Zhong G. Caspase-1 contributes to Chlamydia trachomatis-induced upper urogenital tract inflammatory pathologies without affecting the course of infection. Infect Immun. 2008;76(2):515–22.CrossRefPubMed
31.
go back to reference Hu XY, Wu RH, Logue M, Blondel C, Lai LYW, Stuart B, et al. Andrographis paniculata (Chuān Xīn Lián) for symptomatic relief of acute respiratory tract infections in adults and children: a systematic review and meta-analysis. PLoS ONE. 2017;12(8):e0181780.CrossRefPubMedPubMedCentral Hu XY, Wu RH, Logue M, Blondel C, Lai LYW, Stuart B, et al. Andrographis paniculata (Chuān Xīn Lián) for symptomatic relief of acute respiratory tract infections in adults and children: a systematic review and meta-analysis. PLoS ONE. 2017;12(8):e0181780.CrossRefPubMedPubMedCentral
32.
go back to reference Jayakumar T, Hsieh CY, Lee JJ, Sheu JR. Experimental and clinical pharmacology of Andrographis paniculata and its major bioactive phytoconstituent andrographolide. Evid Based Complement Altern Med. 2013;2013:846740. Jayakumar T, Hsieh CY, Lee JJ, Sheu JR. Experimental and clinical pharmacology of Andrographis paniculata and its major bioactive phytoconstituent andrographolide. Evid Based Complement Altern Med. 2013;2013:846740.
33.
go back to reference Pholphana N, Rangkadilok N, Saehun J, Ritruechai S, Satayavivad J. Changes in the contents of four active diterpenoids at different growth stages in Andrographis paniculata (Burm.f.) Nees (Chuanxinlian). Chin Med. 2013;8(1):2.CrossRefPubMedPubMedCentral Pholphana N, Rangkadilok N, Saehun J, Ritruechai S, Satayavivad J. Changes in the contents of four active diterpenoids at different growth stages in Andrographis paniculata (Burm.f.) Nees (Chuanxinlian). Chin Med. 2013;8(1):2.CrossRefPubMedPubMedCentral
34.
go back to reference Arifullah M, Namsa ND, Mandal M, Chiruvella KK, Vikrama P, Gopal GR. Evaluation of anti-bacterial and anti-oxidant potential of andrographolide and echiodinin isolated from callus culture of Andrographis paniculata Nees. Asian Pac J Trop Biomed. 2013;3(8):604–10.CrossRefPubMedPubMedCentral Arifullah M, Namsa ND, Mandal M, Chiruvella KK, Vikrama P, Gopal GR. Evaluation of anti-bacterial and anti-oxidant potential of andrographolide and echiodinin isolated from callus culture of Andrographis paniculata Nees. Asian Pac J Trop Biomed. 2013;3(8):604–10.CrossRefPubMedPubMedCentral
35.
go back to reference Hua Z, Frohlich KM, Zhang Y, Feng X, Zhang J, Shen L. Andrographolide inhibits intracellular Chlamydia trachomatis multiplication and reduces secretion of proinflammatory mediators produced by human epithelial cells. Pathog Dis. 2015;73(1):1–11.CrossRefPubMed Hua Z, Frohlich KM, Zhang Y, Feng X, Zhang J, Shen L. Andrographolide inhibits intracellular Chlamydia trachomatis multiplication and reduces secretion of proinflammatory mediators produced by human epithelial cells. Pathog Dis. 2015;73(1):1–11.CrossRefPubMed
36.
go back to reference Shen T, Yang WS, Yi YS, Sung GH, Rhee MH, Poo H, et al. AP-1/IRF-3 targeted anti-inflammatory activity of andrographolide isolated from Andrographis paniculata. Evid Based Complement Altern Med. 2013;2013:210736. Shen T, Yang WS, Yi YS, Sung GH, Rhee MH, Poo H, et al. AP-1/IRF-3 targeted anti-inflammatory activity of andrographolide isolated from Andrographis paniculata. Evid Based Complement Altern Med. 2013;2013:210736.
37.
go back to reference Zou W, Xiao Z, Wen X, Luo J, Chen S, Cheng Z, et al. The anti-inflammatory effect of Andrographis paniculata (Burm. f.) Nees on pelvic inflammatory disease in rats through down-regulation of the NF-κB pathway. BMC Complement Altern Med. 2016;16(1):483.CrossRefPubMedPubMedCentral Zou W, Xiao Z, Wen X, Luo J, Chen S, Cheng Z, et al. The anti-inflammatory effect of Andrographis paniculata (Burm. f.) Nees on pelvic inflammatory disease in rats through down-regulation of the NF-κB pathway. BMC Complement Altern Med. 2016;16(1):483.CrossRefPubMedPubMedCentral
38.
go back to reference Tao X, Sun X, Xu L, Yin L, Han X, Qi Y, et al. Total flavonoids from Rosa laevigata Michx fruit ameliorates hepatic ischemia/reperfusion injury through inhibition of oxidative stress and inflammation in rats. Nutrients. 2016;8(7):E418.CrossRefPubMed Tao X, Sun X, Xu L, Yin L, Han X, Qi Y, et al. Total flavonoids from Rosa laevigata Michx fruit ameliorates hepatic ischemia/reperfusion injury through inhibition of oxidative stress and inflammation in rats. Nutrients. 2016;8(7):E418.CrossRefPubMed
39.
go back to reference Zhao L, Xu L, Tao X, Han X, Yin L, Qi Y, Peng J. Protective effect of the total flavonoids from Rosa laevigata Michx fruit on renal ischemia-reperfusion injury through suppression of oxidative stress and inflammation. Molecules. 2016;21(7):E952.CrossRefPubMed Zhao L, Xu L, Tao X, Han X, Yin L, Qi Y, Peng J. Protective effect of the total flavonoids from Rosa laevigata Michx fruit on renal ischemia-reperfusion injury through suppression of oxidative stress and inflammation. Molecules. 2016;21(7):E952.CrossRefPubMed
40.
go back to reference Liu L, Chen L, Jiang C, Guo J, Xie Y, Kang L, et al. Berberine inhibits the LPS-induced proliferation and inflammatory response of stromal cells of adenomyosis tissues mediated by the LPS/TLR4 signaling pathway. Exp Ther Med. 2017;14(6):6125–30.PubMedPubMedCentral Liu L, Chen L, Jiang C, Guo J, Xie Y, Kang L, et al. Berberine inhibits the LPS-induced proliferation and inflammatory response of stromal cells of adenomyosis tissues mediated by the LPS/TLR4 signaling pathway. Exp Ther Med. 2017;14(6):6125–30.PubMedPubMedCentral
41.
go back to reference Ma X, Chen Z, Wang L, Wang G, Wang Z, Dong X, et al. The pathogenesis of diabetes mellitus by oxidative stress and inflammation: its inhibition by berberine. Front Pharmacol. 2018;9:782.CrossRefPubMedPubMedCentral Ma X, Chen Z, Wang L, Wang G, Wang Z, Dong X, et al. The pathogenesis of diabetes mellitus by oxidative stress and inflammation: its inhibition by berberine. Front Pharmacol. 2018;9:782.CrossRefPubMedPubMedCentral
42.
go back to reference Jin H, Jin X, Cao B, Wang W. Berberine affects osteosarcoma via downregulating the caspase-1/IL-1β signaling axis. Oncol Rep. 2017;37(2):729–36.CrossRefPubMed Jin H, Jin X, Cao B, Wang W. Berberine affects osteosarcoma via downregulating the caspase-1/IL-1β signaling axis. Oncol Rep. 2017;37(2):729–36.CrossRefPubMed
46.
go back to reference Liu C, Li J, Meng FY, Liang SX, Deng R, Li CK, et al. Polysaccharides from the root of Angelica sinensis promotes hematopoiesis and thrombopoiesis through the PI3K/AKT pathway. BMC Complement Altern Med. 2010;10:79.CrossRefPubMedPubMedCentral Liu C, Li J, Meng FY, Liang SX, Deng R, Li CK, et al. Polysaccharides from the root of Angelica sinensis promotes hematopoiesis and thrombopoiesis through the PI3K/AKT pathway. BMC Complement Altern Med. 2010;10:79.CrossRefPubMedPubMedCentral
47.
go back to reference Huang Y, Chen L, Feng L, Guo F, Li Y. Characterization of total phenolic constituents from the stems of Spatholobus suberectus using LC-DAD-MS(n) and their inhibitory effect on human neutrophil elastase activity. Molecules. 2013;18(7):7549–56.CrossRefPubMed Huang Y, Chen L, Feng L, Guo F, Li Y. Characterization of total phenolic constituents from the stems of Spatholobus suberectus using LC-DAD-MS(n) and their inhibitory effect on human neutrophil elastase activity. Molecules. 2013;18(7):7549–56.CrossRefPubMed
48.
go back to reference Fu YF, Jiang LH, Zhao WD, Xi-Nan M, Huang SQ, Yang J, et al. Immunomodulatory and antioxidant effects of total flavonoids of Spatholobus suberectus Dunn on PCV2 infected mice. Sci Rep. 2017;7(1):8676.CrossRefPubMedPubMedCentral Fu YF, Jiang LH, Zhao WD, Xi-Nan M, Huang SQ, Yang J, et al. Immunomodulatory and antioxidant effects of total flavonoids of Spatholobus suberectus Dunn on PCV2 infected mice. Sci Rep. 2017;7(1):8676.CrossRefPubMedPubMedCentral
49.
go back to reference Yue R, Zhao L, Hu Y, Jiang P, Wang S, Xiang L, et al. Rapid-resolution liquid chromatography TOF-MS for urine metabolomic analysis of collagen-induced arthritis in rats and its applications. J Ethnopharmacol. 2013;145(2):465–75.CrossRefPubMed Yue R, Zhao L, Hu Y, Jiang P, Wang S, Xiang L, et al. Rapid-resolution liquid chromatography TOF-MS for urine metabolomic analysis of collagen-induced arthritis in rats and its applications. J Ethnopharmacol. 2013;145(2):465–75.CrossRefPubMed
50.
go back to reference Ahn JK, Kim S, Hwang J, Kim J, Lee YS, Koh EM, et al. Metabolomic elucidation of the effects of curcumin on fibroblast-like synoviocytes in rheumatoid arthritis. PLoS ONE. 2015;10(12):e0145539.CrossRefPubMedPubMedCentral Ahn JK, Kim S, Hwang J, Kim J, Lee YS, Koh EM, et al. Metabolomic elucidation of the effects of curcumin on fibroblast-like synoviocytes in rheumatoid arthritis. PLoS ONE. 2015;10(12):e0145539.CrossRefPubMedPubMedCentral
51.
go back to reference Dai D, Gao Y, Chen J, Huang Y, Zhang Z, Xu F. Time-resolved metabolomics analysis of individual differences during the early stage of lipopolysaccharide-treated rats. Sci Rep. 2016;6:34136.CrossRefPubMedPubMedCentral Dai D, Gao Y, Chen J, Huang Y, Zhang Z, Xu F. Time-resolved metabolomics analysis of individual differences during the early stage of lipopolysaccharide-treated rats. Sci Rep. 2016;6:34136.CrossRefPubMedPubMedCentral
52.
go back to reference Qi Y, Jiang C, Cheng J, Krausz KW, Li T, Ferrell JM, et al. Bile acid signaling in lipid metabolism: metabolomic and lipidomic analysis of lipid and bile acid markers linked to anti-obesity and anti-diabetes in mice. Biochim Biophys Acta. 2015;1851(1):19–29.CrossRefPubMed Qi Y, Jiang C, Cheng J, Krausz KW, Li T, Ferrell JM, et al. Bile acid signaling in lipid metabolism: metabolomic and lipidomic analysis of lipid and bile acid markers linked to anti-obesity and anti-diabetes in mice. Biochim Biophys Acta. 2015;1851(1):19–29.CrossRefPubMed
53.
go back to reference Mariette C, Perrais M, Leteurtre E, Jonckheere N, Hémon B, Pigny P, et al. Transcriptional regulation of human mucin MUC4 by bile acids in oesophageal cancer cells is promoter-dependent and involves activation of the phosphatidylinositol 3-kinase signalling pathway. Biochem J. 2004;377(Pt 3):701–8.CrossRefPubMedPubMedCentral Mariette C, Perrais M, Leteurtre E, Jonckheere N, Hémon B, Pigny P, et al. Transcriptional regulation of human mucin MUC4 by bile acids in oesophageal cancer cells is promoter-dependent and involves activation of the phosphatidylinositol 3-kinase signalling pathway. Biochem J. 2004;377(Pt 3):701–8.CrossRefPubMedPubMedCentral
54.
go back to reference Carraway KL, Ramsauer VP, Haq B, Carothers Carraway CA. Cell signaling through membrane mucins. BioEssays. 2003;25(1):66–71.CrossRefPubMed Carraway KL, Ramsauer VP, Haq B, Carothers Carraway CA. Cell signaling through membrane mucins. BioEssays. 2003;25(1):66–71.CrossRefPubMed
55.
go back to reference Guijas C, Astudillo AM, Gil-de-Gómez L, Rubio JM, Balboa MA, Balsinde J. Phospholipid sources for adrenic acid mobilization in RAW 264.7 macrophages. Comparison with arachidonic acid. Biochim Biophys Acta. 2012;1821(11):1386–93.CrossRefPubMed Guijas C, Astudillo AM, Gil-de-Gómez L, Rubio JM, Balboa MA, Balsinde J. Phospholipid sources for adrenic acid mobilization in RAW 264.7 macrophages. Comparison with arachidonic acid. Biochim Biophys Acta. 2012;1821(11):1386–93.CrossRefPubMed
56.
go back to reference Wu X, Cao H, Zhao L, Song J, She Y, Feng Y. Metabolomic analysis of glycerophospholipid signatures of inflammation treated with non-steroidal anti-inflammatory drugs-induced-RAW264.7 cells using (1)H NMR and U-HPLC/Q-TOF-MS. J Chromatogr B Analyt Technol Biomed Life Sci. 2016;1028:199–215.CrossRefPubMed Wu X, Cao H, Zhao L, Song J, She Y, Feng Y. Metabolomic analysis of glycerophospholipid signatures of inflammation treated with non-steroidal anti-inflammatory drugs-induced-RAW264.7 cells using (1)H NMR and U-HPLC/Q-TOF-MS. J Chromatogr B Analyt Technol Biomed Life Sci. 2016;1028:199–215.CrossRefPubMed
57.
go back to reference Dong L, Han X, Tao X, Xu L, Xu Y, Fang L, et al. Protection by the total flavonoids from Rosa laevigata Michx fruit against lipopolysaccharide-induced liver injury in mice via modulation of FXR signaling. Foods. 2018;7(6):E88.CrossRefPubMed Dong L, Han X, Tao X, Xu L, Xu Y, Fang L, et al. Protection by the total flavonoids from Rosa laevigata Michx fruit against lipopolysaccharide-induced liver injury in mice via modulation of FXR signaling. Foods. 2018;7(6):E88.CrossRefPubMed
58.
go back to reference Hu XY, Qin FY, Lu XF, Zhang LS, Cheng YX. Three new polyynes from Codonopsis pilosula and their activities on lipid metabolism. Molecules. 2018;23(4):E887.CrossRefPubMed Hu XY, Qin FY, Lu XF, Zhang LS, Cheng YX. Three new polyynes from Codonopsis pilosula and their activities on lipid metabolism. Molecules. 2018;23(4):E887.CrossRefPubMed
Metadata
Title
Metabonomic study of the protective effect of Fukeqianjin formula on multi-pathogen induced pelvic inflammatory disease in rats
Authors
Yan Zhang
Wei Li
Liang Zou
Yun Gong
Peng Zhang
Shasha Xing
Hang Yang
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Chinese Medicine / Issue 1/2018
Electronic ISSN: 1749-8546
DOI
https://doi.org/10.1186/s13020-018-0217-6

Other articles of this Issue 1/2018

Chinese Medicine 1/2018 Go to the issue