Journal of Shandong University (Health Sciences) ›› 2018, Vol. 56 ›› Issue (7): 7-14.doi: 10.6040/j.issn.1671-7554.0.2017.929

Previous Articles    

Effects of Fusobacterium nucleatum gavage on the intestinal microbiota of rats

SONG Lijin, GU Xiang, LI Lixiang, LI Ming, ZUO Xiuli, LI Yanqing   

  1. Department of Gastroenterology, Qilu Hospital of Shandong University, Jinan 250012, Shandong, China
  • Published:2022-09-27

PDF (PC)

100

Abstract: Objective To investigate the effects of Fusobacterium nucleatum(F. nucleatum)gavage on the intestinal microbiota of rats. Methods A total of 16 male SD rats were randomly divided into 2 groups: intervention group(n=8)and control group(n=8). The intervention group was treated with F. nucleatum when the rats were 4, 5, 6, 7 and 8 weeks old. The control group was treated with the same dosage of normal saline at the same time. Feces was collected at the end of week 3, 8 and 12 to extract DNA, and then Illumina Miseq platform was used for 16S rRNA gene sequencing. Specific IgA against F. nucleatum in stool was detected with Western blotting. Results There were no significant differences between the two groups in terms of fecal microbial diversity and relative abundance of main phyla in week 3. The microbial diversity of the intervention group was significantly lower than that of the control group in week 8(P=0.009). The relative abundances of Firmicutes and Proteobacteriodes in the intervention group were significantly less than those in the control group(P<0.05), while the relative abundance of Bacteriodes in the intervention group was significantly higher than that in the control group in week 8(P<0.05). In week 12, the intervention group showed higher diversity(P=0.021), and there was no significant difference in the relative abundance of main phyla. Moreover, the treatment of F. nucleatum stimulated the production of specific IgA. Conclusion The F. nucleatum can interfere with intestinal microbiota independent on colonization, and this effect can last for some time. The production of specific IgA induced by F. nucleatum may explain why this bacterium does not colonize in the intestine.

Key words: Fusobacterium nucleatum, Intestinal microbiota, High-throughput sequencing, Rats

CLC Number: 

  • R574
[1] Han YW. Fusobacterium nucleatum: a commensal-turned pathogen[J]. Curr Opin Microbiol, 2015, 23:141-147.doi:10.1016/j.mib.2014.11.013.
[2] Strauss J, Kaplan GG, Beck PL, et al. Invasive potential of gut mucosa-derived Fusobacterium nucleatum positively correlates with IBD status of the host[J]. Inflamm Bowel Dis, 2011, 17(9):1971-1978.
[3] Han YW, Fardini Y, Chen C, et al. Term stillbirth caused by oral Fusobacterium nucleatum[J]. Obstet Gynecol, 2010, 115(2 Pt 2):442-445.
[4] Yang Y, Weng W, Peng J, et al. Fusobacterium nucleatum increases proliferation of colorectal cancer cells and tumor development in mice by activating Toll-like receptor 4 signaling to nuclear factor-kappaB, and up-regulating expression of microRNA-21[J]. Gastroenterology, 2017, 152(4):851-866.
[5] Swidsinski A, Dorffel Y, Loening-Baucke V, et al. Acute appendicitis is characterised by local invasion with Fusobacterium nucleatum/necrophorum[J]. Gut, 2011, 60(1):34-40.
[6] Gur C, Ibrahim Y, Isaacson B, et al. Binding of the Fap2 protein of Fusobacterium nucleatum to human inhibitory receptor TIGIT protects tumors from immune cell attack[J]. Immunity, 2015, 42(2):344-355.
[7] Rubinstein MR, Wang X, Liu W, et al. Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/beta-catenin signaling via its FadA adhesin[J]. Cell Host Microbe, 2013, 14(2):195-206.
[8] Nakagaki H, Sekine S, Terao Y, et al. Fusobacterium nucleatum envelope protein FomA is immunogenic and binds to the salivary statherin-derived peptide[J]. Infect Immun, 2010, 78(3):1185-1192.
[9] Abed J, Emgard JE, Zamir G, et al. Fap2 mediates Fusobacterium nucleatum colorectal adenocarcinoma enrichment by binding to tumor-expressed Gal-GalNAc[J]. Cell Host Microbe, 2016, 20(2):215-225.
[10] Yu T, Guo F, Yu Y, et al. Fusobacterium nucleatum promotes chemoresistance to colorectal cancer by modulating autophagy[J]. Cell, 2017, 170(3):548-563.e16.
[11] Stecher B, Hardt WD. Mechanisms controlling pathogen colonization of the gut[J]. Curr Opin Microbiol, 2011, 14(1):82-91.
[12] Levy M, Kolodziejczyk AA, Thaiss CA, et al. Dysbiosis and the immune system[J]. Nat Rev Immunol, 2017, 17(4):219-232.
[13] Simren M, Barbara G, Flint HJ, et al. Intestinal microbiota in functional bowel disorders: a Rome foundation report[J]. Gut, 2013, 62(1):159-176.
[14] Marchesi JR, Adams DH, Fava F, et al. The gut microbiota and host health: a new clinical frontier[J]. Gut, 2016, 65(2):330-339.
[15] Arumugam M, Raes J, Pelletier E, et al. Enterotypes of the human gut microbiome[J]. Nature, 2011, 473(7346):174-180.
[16] Tettamanti L, Gaudio RM, Cura F, et al. Prevalence of periodontal pathogens among italian patients with chronic periodontitis: a retrospective study on 2992 patients[J]. Oral Implantol(Rome), 2017, 10(1):28-36.
[17] Wang HF, Li LF, Guo SH, et al. Evaluation of antibody level against Fusobacterium nucleatum in the serological diagnosis of colorectal cancer[J]. Sci Rep, 2016, 6:33440. doi: 10.1038/srep33440.
[18] Edgar RC. Search and clustering orders of magnitude faster than BLAST[J]. Bioinformatics, 2010, 26(19):2460-2461.
[19] Lan Y, Wang Q, Cole JR, et al. Using the RDP classifier to predict taxonomic novelty and reduce the search space for finding novel organisms[J]. PLoS One, 2012, 7(3):e32491. doi: 10.1371/journal.pone.0032491
[20] Lundberg DS, Yourstone S, Mieczkowski P, et al. Practical innovations for high-throughput amplicon sequencing[J]. Nat Methods, 2013, 10(10):999-1002.
[21] Zhang C, Li S, Yang L, et al. Structural modulation of gut microbiota in life-long calorie-restricted mice[J]. Nat Commun, 2013, 4:2163. doi: 10.1038/ncomms3163.
[22] Kaplan CW, Lux R, Haake SK, et al. The Fusobacterium nucleatum outer membrane protein RadD is an arginine-inhibitable adhesin required for inter-species adherence and the structured architecture of multispecies biofilm[J]. Mol Microbiol, 2009, 71(1):35-47.
[23] Nwizu NN, Marshall JR, Moysich K, et al. Periodontal disease and incident cancer risk among postmenopausal women: results from the Womens Health Initiative Observational Cohort[J]. Cancer Epidemiol Biomarkers Prev, 2017, 26(8):1255-1265.
[24] Michaud DS, Liu Y, Meyer M, et al. Periodontal disease, tooth loss, and cancer risk in male health professionals: a prospective cohort study[J]. Lancet Oncol, 2008, 9(6):550-558.
[25] Barton MK. Evidence accumulates indicating periodontal disease as a risk factor for colorectal cancer or lymphoma[J]. CA Cancer J Clin, 2017, 67(3):173-174.
[26] Momen-Heravi F, Babic A, Tworoger SS, et al. Periodontal disease, tooth loss and colorectal cancer risk: results from the nurses’ health study[J]. Int J Cancer, 2017, 140(3):646-652.
[27] Bertrand KA, Shingala J, Evens A, et al. Periodontal disease and risk of non-Hodgkin lymphoma in the health professionals follow-up Study[J]. Int J Cancer, 2017, 140(5):1020-1026.
[28] 束蓉. 牙周病病因及治疗研究进展[J]. 上海交通大学学报(医学版), 2007,27(6):625-628. SHU Rong. Research advances in etiology and treatment of periodontal disease[J]. Journal of Shanghai Jiaotong University(Medical Science), 2007, 27(6):625-628.
[29] Saygun I, Nizam N, Keskiner I, et al. Salivary infectious agents and periodontal disease status[J]. J Periodontal Res, 2011, 46(2):235-239.
[30] Nakajima M, Arimatsu K, Kato T, et al. Oral administration of P. gingivalis induces dysbiosis of gut microbiota and impaired barrier function leading to dissemination of enterobacteria to the liver[J]. PLoS One, 2015, 10(7):e0134234. doi:10.1371/journal.pone.0134234.
[31] 赵力, 李理想, 陈飞雪, 等. 枯草芽孢杆菌灌胃对小鼠肠道菌群的影响[J]. 山东大学学报(医学版), 2017,55(10):28-35. ZHAO Li, LI Lixiang, CHEN Feixue, et al. Effect of Bacillus subtilis gavage on the intestinal microbiota of mice[J]. Journal of Shandong University(Health Sciences), 2017, 55(10):28-35.
[32] Dethlefsen L, McFall-Ngai M, Relman DA. An ecological and evolutionary perspective on human-microbe mutualism and disease[J]. Nature, 2007, 449(7164):811-818.
[33] Stecher B, Hardt WD. The role of microbiota in infectious disease[J]. Trends Microbiol, 2008, 16(3):107-114.
[34] Kabat AM, Srinivasan N, Maloy KJ. Modulation of immune development and function by intestinal microbiota[J]. Trends Immunol, 2014, 35(11):507-517.
[35] Macpherson AJ, Uhr T. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria[J]. Science, 2004, 303(5664):1662-1665.
[36] Norman JM, Handley SA, Baldridge MT, et al. Disease-specific alterations in the enteric virome in inflammatory bowel disease[J]. Cell, 2015, 160(3):447-460.
[37] Shah MS, DeSantis TZ, Weinmaier T, et al. Leveraging sequence-based faecal microbial community survey data to identify a composite biomarker for colorectal cancer[J]. Gut, 2018, 67(5):882-891.
[38] Monaco CL, Gootenberg DB, Zhao G, et al. Altered virome and bacterial microbiome in human immunodeficiency virus-associated acquired immunodeficiency syndrome[J]. Cell Host Microbe, 2016, 19(3):311-322.
[39] Kostic AD, Gevers D, Siljander H, et al. The dynamics of the human infant gut microbiome in development and in progression toward type 1 diabetes[J]. Cell Host Microbe, 2015, 17(2):260-273.
[40] Wright EK, Kamm MA, Teo SM, et al. Recent advances in characterizing the gastrointestinal microbiome in Crohn's disease: a systematic review[J]. Inflamm Bowel Dis, 2015, 21(6):1219-1228.
[41] 谢莉敏, 李丹, 程秀芳, 等. 益生菌的种类及其在人体营养保健中的应用研究[J]. 安徽农业科学, 2013(17):7694-7695. XIE Limin, LI Dan, CHENG Xiufang, et al. On species and application of probiotics in human nutrition and health care [J]. Journal of Anhui Agri, 2013, 41(17):7694-7695.
[1] ZHU Lin, HU San-Yuan, ZHANG Guang-Yong, DING Xiang-Jiu. Protection of PGE2 against intestinal mucosa injuries in obstructed jaundice rats [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2209, 47(6): 12-.
[2] SUN Tao, ZHANG Dao-Lai, XIE Shan-Shan, WANG Yu-Zhuo, FENG Yu-Xin, XIN Hua. Effect of ethanol on expression of connexin 43 in primary culture of neural precursor cells [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2209, 47(6): 20-.
[3] ZHANG Dao-Lai, SUN Tao, XIE Shan-Shan, WANG Yu-Zhuo, ZHAO Ling, FENG Yu-Xin, XIN Hua. Developmental expression of NMDAR1 subunit on cultured cerebral cortical neurons of fetal rats in vitro [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2209, 47(6): 28-32.
[4] HU Na, SUN Miao, XING Shasha, XU Danxia, HAI Xiaoming, MA Ling, YANG Li, MIAN Yuchen, HE Rui, CHEN Dongmei, MA Huiming. Evening primrose oil resists oxidative stress in the ovaries of rats with polycystic ovary syndrome [J]. Journal of Shandong University (Health Sciences), 2022, 60(5): 22-30.
[5] ZHAO Huiwen, XU Lin, SHAN Shan, ZHAO Xiulan. Protective effect of taurine on cognitive deficit induced by 1-bromopropane [J]. Journal of Shandong University (Health Sciences), 2022, 60(2): 14-21.
[6] WANG Haipeng, ZOU Juanjuan, GAO Chunmiao, WANG Xiao, WANG Yan, LI Yanzhong. Construction and significance of a rat model of OSAHS with chronic intermittent hypoxia [J]. Journal of Shandong University (Health Sciences), 2021, 59(2): 7-13.
[7] ZHANG Jijuan, YU Hancheng, WANG Lan, CHEN Nuo, CUI Shumeng, Gao Xibao. Effects of high-fat diet and selenium concentration on antioxidant function in rats [J]. Journal of Shandong University (Health Sciences), 2021, 59(1): 95-101.
[8] ZHANG Dandan, XIE Hongqiang, WU Qianqian, LI Hongchang, ZHU Yueting, LU Juanjuan, JIANG Wenjie, YAN Junhao. Clinical treatment value of preimplantation genetic screening for unexplained repeated implantation failure [J]. Journal of Shandong University (Health Sciences), 2018, 56(4): 64-69.
[9] WANG Qianqian, WANG Xuxia, QIAO Qingfang, WANG Yingzi, YANG Panpan, ZHANG Jun. Effects of sympathetic signals on orthodontic root resorption in rats [J]. Journal of Shandong University (Health Sciences), 2018, 56(1): 76-80.
[10] ZHANG Liang, XU Min, ZHUANG Xianghua, LOU Fuchen, LOU Nengjun, LÜ Li, GUO Wenjuan, ZHENG Fengjie, CHEN Shihong. An investigation of endoplasmic reticulum stress and apoptosis in diabetic peripheral neuropathy [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2017, 55(8): 13-17.
[11] ZHAO Li, LI Lixiang, CHEN Feixue, ZUO Xiuli, LI Yanqing. Effect of Bacillus subtilis gavage on the intestinal microbiota of mice [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2017, 55(10): 28-35.
[12] XIE Haibin, WU Qunzheng, LIU Shaozhuang, HUANG Xin, CHENG Yugang, HU Sanyuan, ZHANG Guangyong. Role of mitochondria-associated membranes in the improvement of insulin sensitivity in diabetic rats after sleeve gastrectomy [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2017, 55(10): 36-40.
[13] CHEN Yihui, LIU Xuewei, HOU Xuhao, SUN Qinfeng. Study of mouse alveolar bone defect reparation by dialdehyde bletilla striata glucomanna / hydroxypropyl chitosan / nano-nacre powder composited scaffolds [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2016, 54(6): 7-11.
[14] LI Hongzhi, LIU Jing, SONG Yan, CHI Lingyi, LIU Yuguang. Role of liraglutide in the repair of spinal cord injury [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2016, 54(4): 1-5.
[15] REN Baoxin, MA Yunfeng, LIU Dianwei, LI Zhuo, JIANG Yong. Effects of Wnt3a on neuronal autophagy and apoptosis in early brain injury after subarachnoid hemorrhage in rats [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2016, 54(10): 11-15.
Viewed
Full text


Abstract

Cited
  Shared   
  Discussed   
No Suggested Reading articles found!
Copyright 2018 © Editorial office of Journal of Shandong University (Health Sciences)
Supported by Beijing Magtech Co.Ltd