1,625
Views
0
CrossRef citations to date
0
Altmetric
Research Paper

B. longum CKD1 enhances the efficacy of anti-diabetic medicines through upregulation of IL- 22 response in type 2 diabetic mice

, , , , , , , , , , & ORCID Icon show all
Article: 2319889 | Received 27 Oct 2023, Accepted 12 Feb 2024, Published online: 23 Feb 2024

References

  • Sun X, Yu W, Hu C. Genetics of type 2 diabetes: insights into the pathogenesis and its clinical application. Biomed Res Int. 2014;2014:926713. doi:10.1155/2014/926713.
  • Zheng Y, Ley SH, Hu FB. Global aetiology and epidemiology of type 2 diabetes mellitus and its complications. Nat Rev Endocrinol. 2018;14(2):88–26. doi:10.1038/nrendo.2017.151.
  • Edward Michieka O, Benjamin Moranga O. The rise of noncommunicable diseases in Kenya: an examination of the time trends and contribution of the changes in diet and physical inactivity. J Epidemiol Glob Health. 2018;8(1–2):1–7. doi:10.2991/j.jegh.2017.11.004.
  • Saeedi P, Petersohn I, Salpea P, Malanda B, Karuranga S, Unwin N, Colagiuri S, Guariguata L, Motala AA, Ogurtsova K. et al. Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: results from the international diabetes federation diabetes atlas, 9(th) edition. Diabetes Res Clin Pract. 2019;157:107843. doi:10.1016/j.diabres.2019.107843.
  • Thrasher J. Pharmacologic management of type 2 diabetes mellitus: available therapies. Am J Med. 2017;130(6):S4–S17. doi:10.1016/j.amjmed.2017.04.004.
  • Whang A, Nagpal R, Yadav H. Bi-directional drug-microbiome interactions of anti-diabetics. EBioMedicine. 2019;39:591–602. doi:10.1016/j.ebiom.2018.11.046
  • Horii T, Iwasawa M, Kabeya Y, Atuda K. Polypharmacy and oral antidiabetic treatment for type 2 diabetes characterised by drug class and patient characteristics: a Japanese database analysis. Sci Rep. 2019;9(1):12992. doi:10.1038/s41598-019-49424-2.
  • Wu H, Esteve E, Tremaroli V, Khan MT, Caesar R, Mannerås-Holm L, Ståhlman M, Olsson LM, Serino M, Planas-Fèlix M. et al. Metformin alters the gut microbiome of individuals with treatment-naive type 2 diabetes, contributing to the therapeutic effects of the drug. Nat Med. 2017;23(7):850–858. doi:10.1038/nm.4345.
  • Liao X, Song L, Zeng B, Liu B, Qiu Y, Qu H, Zheng Y, Long M, Zhou H, Wang Y. et al. Alteration of gut microbiota induced by DPP-4i treatment improves glucose homeostasis. EBioMedicine. 2019;44:665–674. doi:10.1016/j.ebiom.2019.03.057.
  • Chan CW, Yu C-L, Lin J-C, Hsieh Y-C, Lin C-C, Hung C-Y, Li C-H, Liao Y-C, Lo C-P, Huang J-L. et al. Glitazones and alpha-glucosidase inhibitors as the second-line oral anti-diabetic agents added to metformin reduce cardiovascular risk in type 2 diabetes patients: a nationwide cohort observational study. Cardiovasc Diabetol. 2018;17(1):20. doi:10.1186/s12933-018-0663-6.
  • Tomas J, Mulet C, Saffarian A, Cavin J-B, Ducroc R, Regnault B, Kun Tan C, Duszka K, Burcelin R, Wahli W. et al. High-fat diet modifies the PPAR-γ pathway leading to disruption of microbial and physiological ecosystem in murine small intestine. Proc Natl Acad Sci USA. 2016;113(40):E5934–e5943. doi:10.1073/pnas.1612559113.
  • Xavier-Santos D, Bedani R, Lima ED, Saad SMI. Impact of probiotics and prebiotics targeting metabolic syndrome. J Funct Foods. 2020;64:103666. doi:10.1016/j.jff.2019.103666
  • Mazziotta C, Tognon M, Martini F, Torreggiani E, Rotondo JC. Probiotics mechanism of action on immune cells and beneficial effects on human health. Cells. 2023;12(1):184. doi:10.3390/cells12010184.
  • Ejtahed HS, Mohtadi-Nia J, Homayouni-Rad A, Niafar M, Asghari-Jafarabadi M, Mofid V, Akbarian-Moghari A. Effect of probiotic yogurt containing Lactobacillus acidophilus and Bifidobacterium lactis on lipid profile in individuals with type 2 diabetes mellitus. J Dairy Sci. 2011;94(7):3288–3294. doi:10.3168/jds.2010-4128.
  • Qian X, Si Q, Lin G, Zhu M, Lu J, Zhang H, Wang G, Chen W. Bifidobacterium adolescentis is effective in relieving type 2 diabetes and May Be related to its dominant core genome and gut microbiota modulation capacity. Nutrients. 2022;14(12):2479. doi:10.3390/nu14122479.
  • Yan F, Li N, Shi J, Li H, Yue Y, Jiao W, Wang N, Song Y, Huo G, Li B. et al. Lactobacillus acidophilus alleviates type 2 diabetes by regulating hepatic glucose, lipid metabolism and gut microbiota in mice. Food Funct. 2019;10(9):5804–5815. doi:10.1039/C9FO01062A.
  • Abenavoli L, Scarlata GGM, Scarpellini E, Boccuto L, Spagnuolo R, Tilocca B, Roncada P, Luzza F. Metabolic- Dysfunction-Associated Fatty liver disease and gut microbiota: from Fatty liver to dysmetabolic syndrome. Med (Kaunas). 2023;59(3):594. doi:10.3390/medicina59030594.
  • Yan X, Feng B, Li P, Tang Z, Wang L. Microflora disturbance during progression of glucose intolerance and effect of Sitagliptin: an animal study. J Diabetes Res. 2016;2016:2093171. doi:10.1155/2016/2093171.
  • Zhao L, Chen Y, Xia F, Abudukerimu B, Zhang W, Guo Y, Wang N, Lu Y. A glucagon-like peptide-1 receptor agonist lowers weight by modulating the structure of gut microbiota. Front Endocrinol. 2018;9. doi:10.3389/fendo.2018.00233.
  • Pryor R, Martinez-Martinez D, Quintaneiro L, Cabreiro F. The role of the microbiome in drug response. Annu Rev Pharmacol Toxicol. 2020;60(1):417–435. doi:10.1146/annurev-pharmtox-010919-023612.
  • Wang D, Liu J, Zhong L, Ding L, Zhang Q, Yu M, Li M, Xiao X. Potential benefits of metformin and pioglitazone combination therapy via gut microbiota and metabolites in high-fat diet-fed mice. Front Pharmacol. 2022;13:1004617. doi:10.3389/fphar.2022.1004617.
  • Koh A, Mannerås-Holm L, Yunn N-O, Nilsson PM, Ryu SH, Molinaro A, Perkins R, Smith JG, Bäckhed F. Microbial imidazole propionate affects responses to metformin through p38γ-dependent inhibitory AMPK phosphorylation. Cell Metab. 2020;32(4):643–653.e644. doi:10.1016/j.cmet.2020.07.012.
  • Sato J, Kanazawa A, Azuma K, Ikeda F, Goto H, Komiya K, Kanno R, Tamura Y, Asahara T, Takahashi T. et al. Probiotic reduces bacterial translocation in type 2 diabetes mellitus: a randomised controlled study. Sci Rep. 2017;7(1):12115. doi:10.1038/s41598-017-12535-9.
  • Kocsis T, Molnár B, Németh D, Hegyi P, Szakács Z, Bálint A, Garami A, Soós A, Márta K, Solymár M. et al. Probiotics have beneficial metabolic effects in patients with type 2 diabetes mellitus: a meta- analysis of randomized clinical trials. Sci Rep. 2020;10(1):11787. doi:10.1038/s41598-020-68440-1.
  • Zhang Y, Gu Y, Ren H, Wang S, Zhong H, Zhao X, Ma J, Gu X, Xue Y, Huang S. et al. Gut microbiome-related effects of berberine and probiotics on type 2 diabetes (the PREMOTE study). Nat Commun. 2020;11(1):5015. doi:10.1038/s41467-020-18414-8.
  • Gai Z, Liao W, Huang Y, Dong Y, Feng H, Han M. Effects of bifidobacterium BL21 and lacticaseibacillus LRa05 on gut microbiota in type 2 diabetes mellitus mice. AMB Express. 2023;13(1):97. doi:10.1186/s13568-023-01603-1.
  • Ferreira JP, Rossignol P, Bakris G, Mehta C, White WB, Zannad F. Body weight changes in patients with type 2 diabetes and a recent acute coronary syndrome: an analysis from the EXAMINE trial. Cardiovasc Diabetol. 2021;20(1):187. doi:10.1186/s12933-021-01382-8.
  • Choi H-M, Kim HR, Kim E-K, Byun YS, Won Y-S, Yoon W-K, Kim H-C, Kang J-G, Nam K-H. An age-dependent alteration of the respiratory exchange ratio in the db/db mouse. Lar. 2015;31(1):1–6. doi:10.5625/lar.2015.31.1.1.
  • Ko KY, Wu YW, Liu CW, Cheng MF, Yen RF, Yang WS. Longitudinal evaluation of myocardial glucose metabolism and contractile function in obese type 2 diabetic db/db mice using small-animal dynamic (18)F-FDG PET and echocardiography. Oncotarget. 2017;8(50):87795–87808. doi:10.18632/oncotarget.21202.
  • Suriano F, Vieira-Silva S, Falony G, Roumain M, Paquot A, Pelicaen R, Régnier M, Delzenne NM, Raes J, Muccioli GG. et al. Novel insights into the genetically obese (ob/ob) and diabetic (db/db) mice: two sides of the same coin. Microbiome. 2021;9(1):147. doi:10.1186/s40168-021-01097-8.
  • Utzschneider KM, Kahn SE. The role of Insulin Resistance in nonalcoholic fatty liver disease. J Clin Endocrinol Metab. 2006;91(12):4753–4761. doi:10.1210/jc.2006-0587.
  • Tilg H, Moschen AR. Inflammatory mechanisms in the regulation of insulin resistance. Mol Med. 2008;14(3–4):222–231. doi:10.2119/2007-00119.Tilg.
  • Rehman K, Akash MSH. Mechanisms of inflammatory responses and development of insulin resistance: how are they interlinked? J Biomed Sci. 2016;23(1):87. doi:10.1186/s12929-016-0303-y.
  • Kitade H, Chen G, Ni Y, Ota T. Nonalcoholic fatty liver disease and insulin resistance: new insights and potential new treatments. Nutrients. 2017;9(4):387. doi:10.3390/nu9040387.
  • Sargent J. IL-22 and metabolic disease. Nat Rev Endocrinol. 2014;10(11):639–639. doi:10.1038/nrendo.2014.148.
  • Wang X, Ota N, Manzanillo P, Kates L, Zavala-Solorio J, Eidenschenk C, Zhang J, Lesch J, Lee WP, Ross J. et al. Interleukin-22 alleviates metabolic disorders and restores mucosal immunity in diabetes. Nature. 2014;514(7521):237–241. doi:10.1038/nature13564.
  • Chen H, Sun L, Feng L, Yin Y, Zhang W. Role of innate lymphoid cells in obesity and insulin resistance. Front Endocrinol. 2022;13. doi:10.3389/fendo.2022.855197.
  • Kalyesubula M, Mopuri R, Rosov A, Alon T, Edery N, Moallem U, Dvir H. Hyperglycemia-stimulating diet induces liver steatosis in sheep. Sci Rep. 2020;10(1):12189. doi:10.1038/s41598-020-68909-z.
  • Thaiss CA, Levy M, Grosheva I, Zheng D, Soffer E, Blacher E, Braverman S, Tengeler AC, Barak O, Elazar M. et al. Hyperglycemia drives intestinal barrier dysfunction and risk for enteric infection. Science. 2018;359(6382):1376–1383. doi:10.1126/science.aar3318.
  • Tanase DM, Gosav EM, Costea CF, Ciocoiu M, Lacatusu CM, Maranduca MA, Ouatu A, Floria M. The intricate relationship between type 2 diabetes mellitus (T2DM), insulin resistance (IR), and nonalcoholic fatty liver disease (NAFLD). J Diabetes Res. 2020;2020:3920196. doi:10.1155/2020/3920196.
  • Sharma BR, Jaiswal S, Ravindra PV. Modulation of gut microbiota by bioactive compounds for prevention and management of type 2 diabetes. Biomed Pharmacother. 2022;152:113148. doi:10.1016/j.biopha.2022.113148
  • Jayashree B, Bibin YS, Prabhu D, Shanthirani CS, Gokulakrishnan K, Lakshmi BS, Mohan V, Balasubramanyam M. Increased circulatory levels of lipopolysaccharide (LPS) and zonulin signify novel biomarkers of proinflammation in patients with type 2 diabetes. Mol Cell Biochem. 2014;388(1–2):203–210. doi:10.1007/s11010-013-1911-4.
  • Sakura T, Morioka T, Shioi A, Kakutani Y, Miki Y, Yamazaki Y, Motoyama K, Mori K, Fukumoto S, Shoji T. et al. Lipopolysaccharide-binding protein is associated with arterial stiffness in patients with type 2 diabetes: a cross-sectional study. Cardiovasc Diabetol. 2017;16(1):62. doi:10.1186/s12933-017-0545-3.
  • Khondkaryan L, Margaryan S, Poghosyan D, Manukyan G. Impaired inflammatory response to LPS in type 2 diabetes mellitus. Int J Inflam. 2018;2018:2157434. doi:10.1155/2018/2157434.
  • Armandi A, Rosso C, Caviglia GP, Bugianesi E. Insulin resistance across the spectrum of nonalcoholic fatty liver disease. Metabolites. 2021;11(3):155. doi:10.3390/metabo11030155.
  • Muzurović E, Mikhailidis DP, Mantzoros C. Non-alcoholic fatty liver disease, insulin resistance, metabolic syndrome and their association with vascular risk. Metabolism. 2021;119:154770. doi:10.1016/j.metabol.2021.154770.
  • Gallwitz B. Review of sitagliptin phosphate: a novel treatment for type 2 diabetes. Vasc Health Risk Manag. 2007;3(2):203–210. doi:10.2147/vhrm.2007.3.2.203.
  • Rena G, Hardie DG, Pearson ER. The mechanisms of action of metformin. Diabetologia. 2017;60(9):1577–1585. doi:10.1007/s00125-017-4342-z.
  • Shen J, Fang Y, Zhu H, Ge W. Plasma interleukin-22 levels are associated with prediabetes and type 2 diabetes in the Han Chinese population. J Diabetes Investig. 2018;9(1):33–38. doi:10.1111/jdi.12640.
  • Hendrikx T, Schnabl B. Indoles: metabolites produced by intestinal bacteria capable of controlling liver disease manifestation. J Intern Med. 2019;286(1):32–40. doi:10.1111/joim.12892.
  • Gong F, Wu J, Zhou P, Zhang M, Liu J, Liu Y, Lu X, Liu Z. Interleukin-22 might act as a double-edged sword in type 2 diabetes and coronary artery disease. Mediators Inflamm. 2016;2016:8254797. doi:10.1155/2016/8254797.
  • Zai W, Chen W, Liu H, Ju D. Therapeutic opportunities of IL-22 in Non-Alcoholic Fatty liver disease: from molecular mechanisms to clinical applications. Biomedicines. 2021;9(12):1912. doi:10.3390/biomedicines9121912.
  • Chen W, Zai W, Fan J, Zhang X, Zeng X, Luan J, Wang Y, Shen Y, Wang Z, Dai S. et al. Interleukin-22 drives a metabolic adaptive reprogramming to maintain mitochondrial fitness and treat liver injury. Theranostics. 2020;10(13):5879–5894. doi:10.7150/thno.43894.
  • Abadpour S, Halvorsen B, Sahraoui A, Korsgren O, Aukrust P, Scholz H. Interleukin-22 reverses human islet dysfunction and apoptosis triggered by hyperglycemia and LIGHT. J Mol Endocrinol. 2018;60(3):171–183. doi:10.1530/jme-17-0182.
  • Ma Q, Luan J, Bai Y, Xu C, Liu F, Chen B, Ju D, Xu H. Interleukin-22 in renal protection and its pathological role in kidney diseases. Front Immunol. 2022;13:851818. doi:10.3389/fimmu.2022.851818.
  • Gulhane M, Murray L, Lourie R, Tong H, Sheng YH, Wang R, Kang A, Schreiber V, Wong KY, Magor G. et al. High fat diets induce colonic epithelial cell stress and inflammation that is reversed by IL- 22. Sci Rep. 2016;6(1):28990. doi:10.1038/srep28990.
  • Yang W, Yu T, Huang X, Bilotta AJ, Xu L, Lu Y, Sun J, Pan F, Zhou J, Zhang W. et al. Intestinal microbiota-derived short-chain fatty acids regulation of immune cell IL-22 production and gut immunity. Nat Commun. 2020;11(1):4457. doi:10.1038/s41467-020-18262-6.
  • Cunningham AL, Stephens JW, Harris DA. Intestinal microbiota and their metabolic contribution to type 2 diabetes and obesity. J Diabetes Metab Disord. 2021;20(2):1855–1870. doi:10.1007/s40200-021-00858-4.
  • Tang R, Li L. Modulation of short-chain fatty acids as potential therapy method for type 2 diabetes mellitus. Can J Infect Dis Med Microbiol. 2021;2021:6632266. doi:10.1155/2021/9756586.
  • Chun E, Lavoie S, Fonseca-Pereira D, Bae S, Michaud M, Hoveyda HR, Fraser GL, Gallini Comeau CA, Glickman JN, Fuller MH. et al. Metabolite-sensing receptor Ffar2 regulates colonic group 3 Innate Lymphoid Cells and gut immunity. Immunity. 2019;51(5):871–884.e876. doi:10.1016/j.immuni.2019.09.014.
  • Sivaprakasam S, Prasad PD, Singh N. Benefits of short-chain fatty acids and their receptors in inflammation and carcinogenesis. Pharmacol Ther. 2016;164:144–151. doi:10.1016/j.pharmthera.2016.04.007.
  • Zenewicz LA, Yin X, Wang G, Elinav E, Hao L, Zhao L, Flavell RA. IL-22 Deficiency Alters Colonic Microbiota To Be Transmissible and Colitogenic. J Immunol. 2013;190(10):5306–5312. doi:10.4049/jimmunol.1300016.
  • Peralta G, Sánchez MB, Roiz MP, Garrido JC, Teira R, Mateos F. Diabetes does not affect outcome in patients with Enterobacteriaceae bacteremia. BMC Infect Dis. 2009;9(1):94. doi:10.1186/1471-2334-9-94.
  • Chen YR, Jing QL, Chen FL, Zheng H, Chen LD, Yang ZC. Desulfovibrio is not always associated with adverse health effects in the Guangdong gut microbiome project. PeerJ. 2021;9:e12033. doi:10.7717/peerj.12033
  • Kaur H, Bose C, Mande SS. Tryptophan metabolism by gut microbiome and gut-Brain-Axis: an in silico analysis. Front Neurosci. 2019;13. doi:10.3389/fnins.2019.01365.
  • Almugadam BS, Ibrahim MK, Liu Y, Chen SM, Wang CH, Shao CY, Ren BW, Tang L. Association of urogenital and intestinal parasitic infections with type 2 diabetes individuals: a comparative study. BMC Infect Dis. 2021;21(1):20. doi:10.1186/s12879-020-05629-9.
  • Yoshida M, Funasaka Y, Saeki H, Yamamoto M, Kanda N. Dietary Fiber Inulin Improves Murine Imiquimod- Induced Psoriasis-like Dermatitis. Int J Mol Sci. 2023;24(18):14197. https://www.mdpi.com/1422-0067/24/18/14197.
  • Su X, Zhang M, Qi H, Gao Y, Yang Y, Yun H, Zhang Q, Yang X, Zhang Y, He J. et al. Gut microbiota–derived metabolite 3-idoleacetic acid together with LPS induces IL-35+ B cell generation. Microbiome. 2022;10(1):13. doi:10.1186/s40168-021-01205-8.
  • Dupraz L, Magniez A, Rolhion N, Richard ML, Da Costa G, Touch S, Mayeur C, Planchais J, Agus A, Danne C. et al. Gut microbiota-derived short-chain fatty acids regulate IL-17 production by mouse and human intestinal γδ T cells. Cell Rep. 2021;36(1):109332. doi:10.1016/j.celrep.2021.109332.
  • WJ RR K, Doo EH, Choi YK, Kim KH, Kim BK, Kim BK, Kim H, Kim M, Huh CS. Supplementation with the probiotic strains Bifidobacterium longum and lactiplantibacillus rhamnosus alleviates glucose intolerance by restoring the IL-22 response and pancreatic beta cell dysfunction in type 2 diabetic mice. Probiotics Antimicrob Proteins. 2023. doi:10.1007/s12602-023-10156-5.
  • Song I, Patel O, Himpe E, Muller CJ, Bouwens L, Rooman I. Beta cell Mass restoration in alloxan-diabetic mice treated with EGF and Gastrin. PLoS One. 2015;10(10):e0140148. doi:10.1371/journal.pone.0140148.
  • Kwon EY, Kim SY, Choi MS. Luteolin-enriched artichoke leaf extract alleviates the metabolic syndrome in mice with high-fat diet-induced obesity. Nutrients. 2018;10(8):979. doi:10.3390/nu10080979.
  • Yao B, Dong T, Fu A, Li H, Jiang C, Li N, Cai S. Quantification and characterization of mouse and human tissue- resident microbiota by qPCR and 16S sequencing. STAR Protoc. 2022;3(4):101765. doi:10.1016/j.xpro.2022.101765.
  • Illumina. 16S Metagenomic Sequencing Library Preparation_Preparing 16S ribosomal RNA gene amplicons for the Illumina MiSeq system. https://support.illumina.com/documents/documentation/chemistry_documentation/16s/16s-metagenomic-library-prep-guide-15044223-b.pdf.
  • Wang H, Song W, Wu Q, Gao X, Li J, Tan C, Zhou H, Zhu J, He Y, Yin J. et al. Fecal transplantation from db/db mice treated with sodium butyrate attenuates ischemic stroke injury. Microbiol Spectr. 2021;9(2):e0004221. doi:10.1128/Spectrum.00042-21.