Top

International Journal of Colorectal Disease

Published in:

Open Access 01-12-2024 | Colorectal Cancer | RESEARCH

Analysis of the differential expression of serum miR-21-5p, miR-135-5p, and miR-155-5p by Bifidobacterium triplex viable capsules during the perioperative stage of colorectal cancer

Authors: Jing Zhang, Ji Guo, Ruochong He, Ji Li, Bingyi Du, Yi Zhang, Rongliang He, Haixia Cheng

Published in: International Journal of Colorectal Disease | Issue 1/2024

Abstract

Objective

In this study, we investigated the impact of perioperative administration of Bifidobacterium triplex viable capsules on the serum levels of circulating miR-21-5p, miR-135-5p, and miR-155-5p in patients with colorectal cancer (CRC). The purpose of this study is to provide a foundation for future research on the use of Bifidobacterium triplex viable capsules to enhance postoperative recovery in patients with CRC.

Methods

A total of 60 patients with primary CRC admitted to the Department of General Surgery at Shanxi Bethune Hospital between June 2020 and December 2020 were selected and randomly divided into two groups: 20 cases in the control group and 40 cases in the experimental group. The experimental group was administered oral Bifidobacterium triplex viable capsules during the perioperative period, while the control group was administered oral placebo. Before and after the perioperative period, the expression levels of miR-21-5p, miR-135-5p, and miR-155-5p were compared in the serum of both groups of patients. Furthermore, we established the prognostic value of these three miRNAs in CRC patients.

Results

After surgery, the expression levels of miR-21-5p, miR-135-5p, and miR-155-5p decreased in both groups of patients (P < 0.05). Significantly greater differences were observed between miR-21-5p and miR-135-5p (P < 0.001). Expression levels of serum miR-21-5p (P = 0.020) and miR-135-5p (P = 0.023) decreased significantly more in the experimental group than in the control group. The levels of the above three miRNAs after surgery did not correlate with 3-year OS (HR = 4.21; 95% CI 0.37–47.48; log-rank P = 0.20) or 3-year DFS (HR = 1.57; 95% CI 0.32–7.66; log-rank P = 0.55) in two groups.

Conclusion

Radical surgery reduces the levels of serum miR-21-5p, miR-135-5p, and miR-155-5p expression in patients with CRC. The use of Bifidobacterium triplex viable capsules assists in achieving quicker perioperative recovery from radical surgery in CRC patients, and this underlying mechanism may be associated with the regulation of serum miR-21-5p, miR-135-5p, and miR-155-5p expression levels.

Tilg H, Adolph TE, Gerner RR, Moschen AR (2018) The intestinal microbiota in colorectal cancer. Cancer Cell 33(6):954–964. https://doi.org/10.1016/j.ccell.2018.03.004CrossRefPubMed

Wong SH, Yu J (2019) Gut microbiota in colorectal cancer: mechanisms of action and clinical applications. Nat Rev Gastroenterol Hepatol 16(11):690–704. https://doi.org/10.1038/s41575-019-0209-8CrossRefPubMed

Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A et al (2021) Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 71(3):209–249. https://doi.org/10.3322/caac.21660CrossRefPubMed

Krezalek MA, Hyoju S, Zaborin A, Okafor E, Chandrasekar L, Bindokas V et al (2018) Can methicillin-resistant Staphylococcus aureus silently travel from the gut to the wound and cause postoperative infection? Modeling the “Trojan horse hypothesis.” Ann Surg 267(4):749–758. https://doi.org/10.1097/SLA.0000000000002173CrossRefPubMed

Yang J, Yu J (2018) The association of diet, gut microbiota and colorectal cancer: what we eat may imply what we get. Protein Cell 9(5):474–487. https://doi.org/10.1007/s13238-018-0543-6CrossRefPubMedPubMedCentral

Lavelle A, Hoffmann TW, Pham HP, Langella P, Guédon E, Sokol H (2019) Baseline microbiota composition modulates antibiotic-mediated effects on the gut microbiota and host. Microbiome 7(1):111. https://doi.org/10.1186/s40168-019-0725-3CrossRefPubMedPubMedCentral

Kong C, Gao R, Yan X, Huang L, He J, Li H et al (2019) Alterations in intestinal microbiota of colorectal cancer patients receiving radical surgery combined with adjuvant CapeOx therapy. Sci China Life Sci 62(9):1178–1193. https://doi.org/10.1007/s11427-018-9456-xCrossRefPubMed

Colov EP, Degett TH, Raskov H, Gögenur I (2020) The impact of the gut microbiota on prognosis after surgery for colorectal cancer - a systematic review and meta-analysis. APMIS 128(2):162–176. https://doi.org/10.1111/apm.13032CrossRefPubMed

Lauka L, Reitano E, Carra MC, Gaiani F, Gavriilidis P, Brunetti F et al (2019) Role of the intestinal microbiome in colorectal cancer surgery outcomes. World J Surg Oncol 17(1):204. https://doi.org/10.1186/s12957-019-1754-xCrossRefPubMedPubMedCentral

10.

Ouyang X, Li Q, Shi M, Niu D, Song W, Nian Q et al (2019) Probiotics for preventing postoperative infection in colorectal cancer patients: a systematic review and meta-analysis. Int J Colorectal Dis 34(3):459–469. https://doi.org/10.1007/s00384-018-3214-4CrossRefPubMed

11.

Eslami M, Yousefi B, Kokhaei P, Hemati M, Nejad ZR, Arabkari V et al (2019) Importance of probiotics in the prevention and treatment of colorectal cancer. J Cell Physiol 234(10):17127–17143. https://doi.org/10.1002/jcp.28473CrossRefPubMed

12.

Ding S, Hu C, Fang J, Liu G (2020) The protective role of probiotics against colorectal cancer. Oxid Med Cell Longev 2020:8884583. https://doi.org/10.1155/2020/8884583CrossRefPubMedPubMedCentral

13.

Zununi Vahed S, Barzegari A, Rahbar Saadat Y, Goreyshi A, Omidi Y (2017) Leuconostoc mesenteroides-derived anticancer pharmaceuticals hinder inflammation and cell survival in colon cancer cells by modulating NF-κB/AKT/PTEN/MAPK pathways. Biomed Pharmacother 94:1094–1100. https://doi.org/10.1016/j.biopha.2017.08.033CrossRefPubMed

14.

Peng Y, Croce CM (2016) The role of microRNAs in human cancer. Signal Transduct Target Ther 1:15004. https://doi.org/10.1038/sigtrans.2015.4CrossRefPubMedPubMedCentral

15.

Ulivi P, Canale M, Passardi A, Marisi G, Valgiusti M, Frassineti GL, Calistri D, Amadori D, Scarpi E (2018) Circulating plasma levels of miR-20b, miR-29b and miR-155 as predictors of bevacizumab efficacy in patients with metastatic colorectal cancer. Int J Mol Sci 19(1):307. https://doi.org/10.3390/ijms19010307CrossRefPubMedPubMedCentral

16.

McKenna LB, Schug J, Vourekas A, McKenna JB, Bramswig NC, Friedman JR et al (2010) MicroRNAs control intestinal epithelial differentiation, architecture, and barrier function. Gastroenterology 139(5):1654–64. https://doi.org/10.1053/j.gastro.2010.07.040CrossRefPubMed

17.

Bi K, Zhang X, Chen W, Diao H (2020) MicroRNAs regulate intestinal immunity and gut microbiota for gastrointestinal health: a comprehensive review. Genes (Basel) 11(9):1075. https://doi.org/10.3390/genes11091075CrossRefPubMed

18.

Teodori L, Petrignani I, Giuliani A, Prattichizzo F, Gurău F, Matacchione G et al (2019) Inflamm-aging microRNAs may integrate signals from food and gut microbiota by modulating common signalling pathways. Mech Ageing Dev 182:111127. https://doi.org/10.1016/j.mad.2019.111127CrossRefPubMed

19.

Han TS, Voon DC, Oshima H, Nakayama M, Echizen K, Sakai E et al (2019) Interleukin 1 Up-regulates microRNA 135b to promote inflammation-associated gastric carcinogenesis in mice. Gastroenterology 156(4):1140-1155.e4. https://doi.org/10.1053/j.gastro.2018.11.059CrossRefPubMed

20.

Toiyama Y, Takahashi M, Hur K, Nagasaka T, Tanaka K, Inoue Y et al (2013) Serum miR-21 as a diagnostic and prognostic biomarker in colorectal cancer. J Natl Cancer Inst 105(12):849–859. https://doi.org/10.1093/jnci/djt101CrossRefPubMedPubMedCentral

21.

Li G, Wang Q, Li Z, Shen Y (2020) Serum miR-21 and miR-210 as promising non-invasive biomarkers for the diagnosis and prognosis of colorectal cancer. Rev Esp Enferm Dig 112(11):832–837. https://doi.org/10.17235/reed.2020.6801/2019CrossRefPubMed

22.

Li L, Wang A, Cai M, Tong M, Chen F, Huang L (2020) Identification of stool miR-135b-5p as a non-invasive diaognostic biomarker in later tumor stage of colorectal cancer. Life Sci 260:118417. https://doi.org/10.1016/j.lfs.2020.118417CrossRefPubMed

23.

Bocchetti M, Ferraro MG, Ricciardiello F, Ottaiano A, Luce A, Cossu AM et al (2021) The role of microRNAs in development of colitis-associated colorectal cancer. Int J Mol Sci 22(8):3967. https://doi.org/10.3390/ijms22083967CrossRefPubMedPubMedCentral

24.

Tsukamoto M, Iinuma H, Yagi T, Matsuda K, Hashiguchi Y (2017) Circulating exosomal microRNA-21 as a biomarker in each tumor stage of colorectal cancer. Oncology 92(6):360–370. https://doi.org/10.1159/000463387CrossRefPubMed

25.

Babaei-Jadidi R, Kashfi H, Alelwani W, Karimi Bakhtiari A, Kattan SW, Mansouri OA, Mukherjee A, Lobo DN, Nateri AS (2022) Anti-miR-135/SPOCK1 axis antagonizes the influence of metabolism on drug response in intestinal/colon tumour organoids. Oncogenesis 11(1):4. https://doi.org/10.1038/s41389-021-00376-1CrossRefPubMedPubMedCentral

26.

Liang G, Zhu Y, Ali DJ, Tian T, Xu H, Si K et al (2020) Engineered exosomes for targeted co-delivery of miR-21 inhibitor and chemotherapeutics to reverse drug resistance in colon cancer. J Nanobiotechnology 18(1):10. https://doi.org/10.1186/s12951-019-0563-2CrossRefPubMedPubMedCentral

27.

Li Y, Duo Y, Bi J, Zeng X, Mei L, Bao S et al (2018) Targeted delivery of anti-miR-155 by functionalized mesoporous silica nanoparticles for colorectal cancer therapy. Int J Nanomedicine 13:1241–1256. https://doi.org/10.2147/IJN.S158290CrossRefPubMedPubMedCentral

28.

Percario R, Panaccio P, di Mola FF, Grottola T, Di Sebastiano P (2021) The complex network between inflammation and colorectal cancer: a systematic review of the literature. Cancers (Basel) 13(24):6237. https://doi.org/10.3390/cancers13246237CrossRefPubMed

29.

Kaźmierczak-Siedlecka K, Roviello G, Catalano M, Polom K (2021) Gut microbiota modulation in the context of immune-related aspects of Lactobacillus spp. and Bifidobacterium spp. in gastrointestinal cancers. Nutrients 13(8):2674. https://doi.org/10.3390/nu13082674CrossRefPubMedPubMedCentral

30.

Wei H, Chen L, Lian G, Yang J, Li F, Zou Y et al (2018) Antitumor mechanisms of bifidobacteria. Oncol Lett 16(1):3–8. https://doi.org/10.3892/ol.2018.8692CrossRefPubMedPubMedCentral

31.

Heydari Z, Rahaie M, Alizadeh AM, Agah S, Khalighfard S, Bahmani S (2019) Effects of Lactobacillus acidophilus and Bifidobacterium bifidum probiotics on the expression of microRNAs 135b, 26b, 18a and 155, and Their Involving Genes in Mice Colon Cancer. Probiotics Antimicrob Proteins 11(4):1155–1162. https://doi.org/10.1007/s12602-018-9478-8CrossRefPubMed

32.

Lai CY, Yeh KY, Liu BF, Chang TM, Chang CH, Liao YF et al (2021) MicroRNA-21 plays multiple oncometabolic roles in colitis-associated carcinoma and colorectal cancer via the PI3K/AKT, STAT3, and PDCD4/TNF-α signaling pathways in zebrafish. Cancers (Basel) 13(21):5565. https://doi.org/10.3390/cancers13215565CrossRefPubMed

33.

Valeri N, Braconi C, Gasparini P, Murgia C, Lampis A, Paulus-Hock V et al (2014) MicroRNA-135b promotes cancer progression by acting as a downstream effector of oncogenic pathways in colon cancer. Cancer Cell 25(4):469–483. https://doi.org/10.1016/j.ccr.2014.03.006CrossRefPubMedPubMedCentral

34.

Zhang Y, Zhang Z, Yi Y, Wang Y, Fu J (2020) CircNOL10 acts as a sponge of miR-135a/b-5p in suppressing colorectal cancer progression via regulating KLF9. Onco Targets Ther 13:5165–5176. https://doi.org/10.2147/OTT.S242001CrossRefPubMedPubMedCentral

35.

Guo J, Liao M, Wang J (2021) TLR4 signaling in the development of colitis-associated cancer and its possible interplay with microRNA-155. Cell Commun Signal 19(1):90. https://doi.org/10.1186/s12964-021-00771-6CrossRefPubMedPubMedCentral

36.

Chen K, Collins G, Wang H, Toh JWT (2021) Pathological features and prognostication in colorectal cancer. Curr Oncol 28(6):5356–5383. https://doi.org/10.3390/curroncol28060447CrossRefPubMedPubMedCentral

37.

Zhou H, Zhu L, Song J, Wang G, Li P, Li W, Luo P, Sun X, Wu J, Liu Y, Zhu S, Zhang Y (2022) Liquid biopsy at the frontier of detection, prognosis and progression monitoring in colorectal cancer. Mol Cancer 21(1):86. https://doi.org/10.1186/s12943-022-01556-2CrossRefPubMedPubMedCentral

38.

Chen B, Xia Z, Deng YN, Yang Y, Zhang P, Zhu H, Xu N, Liang S (2019) Emerging microRNA biomarkers for colorectal cancer diagnosis and prognosis. Open Biol 9(1):180212. https://doi.org/10.1098/rsob.180212CrossRefPubMedPubMedCentral

Title: Analysis of the differential expression of serum miR-21-5p, miR-135-5p, and miR-155-5p by Bifidobacterium triplex viable capsules during the perioperative stage of colorectal cancer
Authors: Jing Zhang
Ji Guo
Ruochong He
Ji Li
Bingyi Du
Yi Zhang
Rongliang He
Haixia Cheng
Publication date: 01-12-2024
Publisher: Springer Berlin Heidelberg
Keywords: Colorectal Cancer
Colorectal Cancer
Probiotics
Published in: International Journal of Colorectal Disease / Issue 1/2024
Print ISSN: 0179-1958
Electronic ISSN: 1432-1262
DOI: https://doi.org/10.1007/s00384-024-04617-8

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Analysis of the differential expression of serum miR-21-5p, miR-135-5p, and miR-155-5p by Bifidobacterium triplex viable capsules during the perioperative stage of colorectal cancer

Abstract

Objective

Methods

Results

Conclusion

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Objective

Methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 1/2024

Single-incision plus one-port laparoscopy surgery versus conventional multi-port laparoscopy surgery for colorectal cancer: a systematic review and meta-analysis

The utility of synoptic operation reports in colorectal surgery: a systematic review

Prediction of 30-day, 90-day, and 1-year mortality after colorectal cancer surgery using a data-driven approach

A novel classification of posterior pelvic exenteration to assess prognosis in female patients with locally advanced primary rectal cancer: a retrospective cohort study from China PelvEx collaborative

Developing a multivariable prediction model of global health-related quality of life in patients treated for rectal cancer: a prospective study in five countries

Fistula development after anal abscess drainage—a multicentre retrospective cohort study