Top

Published in:

Open Access 01-12-2019 | Influenza | Research

Effect of feeding Chinese herb medicine ageratum-liquid on intestinal bacterial translocations induced by H9N2 AIV in mice

Authors: Haoran Lu, Luxuan Zhang, Junfang Xiao, Che Wu, Huanmin Zhang, Yihu Chen, Zhengyong Hu, Wencheng Lin, Qingmei Xie, Hongxin Li

Published in: Virology Journal | Issue 1/2019

Abstract

Background

As a low pathogenic influenza virus, avian influenza virus subtype H9N2 (H9N2 AIV) often induces high morbidity in association with secondary bacterial infections in chickens or mammals. To explore this phenomenon, the relationship between intestinal microflora changes and bacterial translocations was studied post H9N2 AIV challenge and post AIV infection plus Ageratum-liquid treatment.

Methods

Illumina sequencing, histological examination and Neongreen-tagged bacteria were used in this study to research the microbiota composition, intestinal barrier, and bacterial translocation in six weeks of BALB/c mice.

Results

H9N2 AIV infection caused intestinal dysbacteriosis and mucosal barrier damages. Notably, the villus length was significantly reduced (p < 0.01) at 12 dpi and the crypt depth was significantly increased (p < 0.01) at 5 dpi and 12 dpi with infection, resulting in the mucosal regular villus-length/crypt-depth (V/C) was significantly reduced (p < 0.01) at 5 dpi and 12 dpi. Moreover, degeneration and dissolution of the mucosal epithelial cells, loose of the connective tissue and partial glandular atrophy were found in infection group, indicating that intestinal barrier function was weakened. Eventually, intestinal microbiota (Staphylococcus, E. coli, etc.) overrun the intestinal barrier and migrated to liver and lung tissues of the mice at 5 and 12 dpi. Furthermore, the bacteria transferred in mesentery tissue sites from intestine at 36 h through tracking the Neongreen-tagged bacteria. Then the Neongreen-tagged bacteria were isolated from liver at 48 h post intragastrical administration. Simultaneously, Ageratum-liquid could inhibit the intestinal microbiota disorder post H9N2 AIV challenge via the respiratory tract. In addition, this study also illustrated that Ageratum-liquid could effectively prevent intestinal bacterial translocation post H9N2 AIV infection in mice.

Conclusion

In this study, we report the discovery that H9N2 AIV infection could damage the ileal mucosal barrier and induce the disturbance of the intestinal flora in BALB/c mice resulting in translocation of intestinal bacteria. In addition, this study indicated that Ageratum-liquid can effectively prevent bacterial translocation following H9N2 infection. These findings are of important theoretical and practical significance in prevention and control of H9N2 AIV infection.

Available only for authorised users

Gu M, Xu L, Wang X, Liu X. Current situation of H9N2 subtype avian influenza in China. Vet Res. 2017;48(1):49. https://doi.org/10.1186/s13567-017-0453-2.CrossRefPubMedPubMedCentral

Peiris M, Yuen KY, Leung CW, Chan KH, Ip PLS, Lai RWM, et al. Human infection with influenza H9N2. Lancet (North American Edition). 1999; 354(9182):916. doi: https://doi.org/10.1016/S0140-6736(99)03311-5.

Nagy A, Mettenleiter TC, Abdelwhab EM. A brief summary of the epidemiology and genetic relatedness of avian influenza H9N2 virus in birds and mammals in the Middle East and North Africa. Epidemiol Infect. 2017;145(16):3320–33. https://doi.org/10.1017/S0950268817002576.CrossRefPubMed

Barbour EK, Mastori FA, Nour AMA, Shaib HA, Jaber LS, Yaghi RH, et al. Standardisation of a new model of H9N2/Escherichia coli challenge in broilers in the Lebanon. Vet Ital. 2009;45:317–22.PubMed

Heidari A, Mancin M, Nili H, Pourghanbari GH, Lankarani KB, Leardini S, et al. Serological evidence of H9N2 avian influenza virus exposure among poultry workers from Fars province of Iran. Virol J. 2016; 13(16). doi: https://doi.org/10.1186/s12985-016-0472-z.

Li S, Zhou Y, Song W, Pang Q, Miao Z. Avian influenza virus H9N2 seroprevalence and risk factors for infection in occupational poultry-exposed workers in Tai'an of China. J Med Virol. 2016;88(8):1453–6. https://doi.org/10.1002/jmv.24483.CrossRefPubMed

Li H, Liu X, Chen F, Zuo K, Wu C, Yan Y, et al. Avian influenza virus subtype H9N2 affects intestinal microbiota, barrier structure injury, and inflammatory intestinal disease in the chicken ileum. Viruses. 2018; 10(5). doi: https://doi.org/10.3390/v10050270.

Qu B, Li X, Gao W, Sun W, Jin Y, Cardona CJ, et al. Human intestinal epithelial cells are susceptible to influenza virus subtype H9N2. Virus Res. 2012;163(1):151–9. https://doi.org/10.1016/j.virusres.2011.09.007.CrossRefPubMed

Lu Y, Li D, Tang F. Mechanism of huoxiang zhengqi extract for regulating the intestinal motility in rat model of diarrhea-predominant irritable bowel syndrome. Zhongguo Zhong Xi Yi Jie He Za Zhi. 2011;31(7):941–5.PubMed

10.

Liu Y, Liu W, Peng QX, Peng JL, Yu LZ, Hu JL. Protective effect of huoxiang zhengqi oral liquid on intestinal mucosal mechanical barrier of rats with postinfectious irritable bowel syndrome induced by acetic acid. Evid Based Complement Alternat Med. 2014;2014:218383. https://doi.org/10.1155/2014/218383.CrossRefPubMedPubMedCentral

11.

Zhao HJ, Guo LP, Yang FW, Zhang MY, Zhang LS, Liu Z, et al. Huoxiang Zhengqi formulas for treatment of gastrointestinal type cold:a systematic review and Meta-analysis. Zhongguo Zhong Yao Za Zhi. 2017; 42(8):1495–1499. doi: https://doi.org/10.19540/j.cnki.cjcmm.2017.0047.

12.

Chen W, Lewith G, Wang LQ, Ren J, Xiong WJ, Lu F, et al. Chinese proprietary herbal medicine listed in 'China national essential drug list' for common cold: a systematic literature review. PLoS One. 2014;9(10):e110560. https://doi.org/10.1371/journal.pone.0110560.CrossRefPubMedPubMedCentral

13.

Pritchett K, Corrow D, Stockwell J, Smith A. Euthanasia of neonatal mice with carbon dioxide. Comp Med. 2005;55:275–81.PubMed

14.

He C, Yang Z, Cheng D, Xie C, Zhu Y, Ge Z, et al. Helicobacter pylori infection aggravates diet-induced insulin resistance in association with gut microbiota of mice. EBioMedicine. 2016;12:247–54. https://doi.org/10.1016/j.ebiom.2016.09.010.CrossRefPubMedPubMedCentral

15.

Maines TR, Szretter KJ, Perrone L, Belser JA, Bright RA, Zeng H, et al. Pathogenesis of emerging avian influenza viruses in mammals and the host innate immune response. Immunol Rev. 2008;225:68–84. https://doi.org/10.1111/j.1600-065X.2008.00690.x.CrossRefPubMed

16.

Pawar SD, Tandale BV, Raut CG, Parkhi SS, Barde TD, Gurav YK, et al. Avian influenza H9N2 seroprevalence among poultry workers in Pune, India, 2010. PLoS One. 2012; 7(e363745). doi: https://doi.org/10.1371/journal.pone.0036374.

17.

Jiang Y, Yang G, Wang Q, Wang Z, Yang W, Gu W, et al. Molecular mechanisms underlying protection against H9N2 influenza virus challenge in mice by recombinant lactobacillus plantarum with surface displayed HA2-LTB. J Biotechnol. 2017;259:6–14. https://doi.org/10.1016/j.jbiotec.2017.08.011.CrossRefPubMed

18.

Ren W, Wang P, Yan J, Liu G, Zeng B, Hussain T, et al. Melatonin alleviates weanling stress in mice: Involvement of intestinal microbiota. J Pineal Res. 2018; 64(2). doi: https://doi.org/10.1111/jpi.12448.

19.

Du W, Xu H, Mei X, Cao X, Gong L, Wu Y, et al. Probiotic Bacillus enhance the intestinal epithelial cell barrier and immune function of piglets. Benef Microbes. 2018;9(5):743–54. https://doi.org/10.3920/BM2017.0142.CrossRefPubMed

20.

Xie Q, Haoran LU, Zhang L, Chen Y. Intestinal flora and mucosal barrier function in mice infected with subtype H9N2 AIV. China Poultry. 2017; (In Chinese).

21.

Yitbarek A, Weese JS, Alkie TN, Parkinson J, Sharif S. Influenza A virus subtype H9N2 infection disrupts the composition of intestinal microbiota of chickens. FEMS Microbiol Ecol. 2018; 94(1). doi: https://doi.org/10.1093/femsec/fix165.

22.

Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444(7122):1027–31. https://doi.org/10.1038/nature05414.CrossRefPubMed

23.

Garrett WS, Lord GM, Punit S, Lugo-Villarino G, Mazmanian SK, Ito S, et al. Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system. Cell. 2007;131(1):33–45. https://doi.org/10.1016/j.cell.2007.08.017.CrossRefPubMedPubMedCentral

24.

Wu H, Li B, Wang X, Jin M, Wang G. Inhibitory effect and possible mechanism of action of patchouli alcohol against influenza a (H2N2) virus. Molecules. 2011;16(8):6489–501. https://doi.org/10.3390/molecules16086489.CrossRefPubMedPubMedCentral

25.

Yu XD, Xie JH, Wang YH, Li YC, Mo ZZ, Zheng YF, et al. Selective antibacterial activity of patchouli alcohol against helicobacter pylori based on inhibition of urease. Phytother Res. 2015;29(1):67–72. https://doi.org/10.1002/ptr.5227.CrossRefPubMed

26.

Lin XM, Wu ZX, Lai JQ, Tao HL, Wei WH, Zhuang HL, et al. Mechanism of lysosome-mediated eradication activity of macrophages on specific anti-Helicobacter pylori of patchouli alcohol. Zhongguo Zhong Yao Za Zhi. 2018; 43(15):3171–3175. doi: https://doi.org/10.19540/j.cnki.cjcmm.20180608.001.

27.

Wu XN, Chen XG, Hu ZD. High-performance liquid simultaneous determination chromatographic method for of honokiol and magnolol in rat plasma. TALANTA. 2003;59(1):115–21. https://doi.org/10.1016/S0039-9140(02)00470-8.CrossRefPubMed

28.

Yang X, Gao M, Hu H, Zhang H. Electrochemical detection of honokiol and magnolol in traditional chinese medicines using acetylene black nanoparticle-modified electrode. Phytochem Anal. 2011; 22(4):291–295. doi: https://doi.org/10.1002/pca.1279 PMID: 21204152.

29.

Syu WJ, Shen CC, Lu JJ, Lee GH, Sun CM. Antimicrobial and cytotoxic activities of neolignans from Magnolia officinalis. Chem Biodivers. 2004;1(3):530–7. https://doi.org/10.1002/cbdv.200490046.CrossRefPubMed

30.

Haraguchi H, Ishikawa H, Shirataki N, Fukuda A. Antiperoxidative activity of neolignans from Magnolia obovata. J Pharm Pharmacol. 1997;49(2):209–12. https://doi.org/10.1111/j.2042-7158.1997.tb06781.x.CrossRefPubMed

31.

Chilampalli S, Zhang X, Fahmy H, Kaushik RS, Zeman D, Hildreth MB, et al. Chemopreventive effects of honokiol on UVB-induced skin cancer development. Anticancer Res. 2010;30(3):777–83.PubMed

32.

Dikalov S, Losik T, Arbiser JL. Honokiol is a potent scavenger of superoxide and peroxyl radicals. Biochem Pharmacol. 2008;76(5):589–96. https://doi.org/10.1016/j.bcp.2008.06.012.CrossRefPubMedPubMedCentral

33.

Fried LE, Arbiser JL. Honokiol, a multifunctional antiangiogenic and antitumor agent. Antioxid Redox Signal. 2009;11(5):1139–48. https://doi.org/10.1089/ars.2009.2440.CrossRefPubMedPubMedCentral

34.

Son HJ, Lee HJ, Yun-Choi HS, Ryu J. Inhibitors of nitric oxide synthesis and TNF-alpha expression from Magnolia obovata in activated macrophages. Planta Med. 2000;66(5):469–71. https://doi.org/10.1055/s-2000-8592.CrossRefPubMed

35.

Tominaga K, Arakawa T. Kampo medicines for gastrointestinal tract disorders: a review of basic science and clinical evidence and their future application. J Gastroenterol. 2013;48(4):452–62. https://doi.org/10.1007/s00535-013-0788-z.CrossRefPubMedPubMedCentral

36.

Ko SJ, Ryu B, Kim J, Hong BG, Yeo I, Lee BJ, et al. Effect of herbal extract granules combined with probiotic mixture on irritable bowel syndrome with diarrhea: study protocol for a randomized controlled trial. Trials. 2011;12:219. https://doi.org/10.1186/1745-6215-12-219.CrossRefPubMedPubMedCentral

37.

Chen F, Wen Q, Jiang J, Li HL, Tan YF, Li YH, et al. Could the gut microbiota reconcile the oral bioavailability conundrum of traditional herbs? J Ethnopharmacol. 2016;179:253–64. https://doi.org/10.1016/j.jep.2015.12.031.CrossRefPubMed

38.

He YH, Zhao HY, Liu ZL, Lu C, Luo XJ, Lin SQ, et al. Effects of huoxiangzhengqi liquid on enteric mucosal immune responses in mice with Bacillus dysenteriae and Salmonella typhimurium induced diarrhea. World J Gastroenterol. 2006;12(45):7346–9. https://doi.org/10.3748/wjg.v12.i45.7346.CrossRefPubMedPubMedCentral

Title: Effect of feeding Chinese herb medicine ageratum-liquid on intestinal bacterial translocations induced by H9N2 AIV in mice
Authors: Haoran Lu
Luxuan Zhang
Junfang Xiao
Che Wu
Huanmin Zhang
Yihu Chen
Zhengyong Hu
Wencheng Lin
Qingmei Xie
Hongxin Li
Publication date: 01-12-2019
Publisher: BioMed Central
Keywords: Influenza
Respiratory Microbiota
Published in: Virology Journal / Issue 1/2019
Electronic ISSN: 1743-422X
DOI: https://doi.org/10.1186/s12985-019-1131-y

ACC 2024 Congress Coverage

Heart Failure Video

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Effect of feeding Chinese herb medicine ageratum-liquid on intestinal bacterial translocations induced by H9N2 AIV in mice

Abstract

Background

Methods

Results

Conclusion

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Background

Methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 1/2019

The effects of autophagy on the replication of Nelson Bay orthoreovirus

Full genome sequence analysis and putative host-shifting of Milk vetch dwarf virus infecting tobacco (Nicotiana tabacum) in China

Alpha, Beta, gamma human PapillomaViruses (HPV) detection with a different sets of primers in oropharyngeal swabs, anal and cervical samples

Construction and characterization of an infectious cDNA clone of coxsackievirus A 10

Distribution of human papillomavirus infection: a population-based study of cervical samples from Jiangsu Province

Intra-species recombination among strains of the ampelovirus Grapevine leafroll-associated virus 4

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page