Skip to main content
SpringerLink
Log in

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

  • Research
  • Published:
Probiotics and Antimicrobial Proteins Aims and scope Submit manuscript

Abstract

Type 2 diabetes (T2D) is known as adult-onset diabetes, but recently, T2D has increased in the number of younger people, becoming a major clinical burden in human society. The objective of this study was to determine the effects of Bifidobacterium and Lactiplantibacillus strains derived from the feces of 20 healthy humans on T2D development and to understand the mechanism underlying any positive effects of probiotics. We found that Bifidobacterium longum NBM7-1 (Chong Kun Dang strain 1; CKD1) and Lactiplantibacillus rhamnosus NBM17-4 (Chong Kun Dang strain 2; CKD2) isolated from the feces of healthy Korean adults (n = 20) have anti-diabetic effects based on the insulin sensitivity. During the oral gavage for 8 weeks, T2D mice were supplemented with anti-diabetic drugs (1.0–10 mg/kg body weight) to four positive and negative control groups or four probiotics (200 uL; 1 × 109 CFU/mL) to groups separately or combined to the four treatment groups (n = 6 per group). While acknowledging the relatively small sample size, this study provides valuable insights into the potential benefits of B. longum NBM7-1 and L. rhamnosus NBM17-4 in mitigating T2D development. The animal gene expression was assessed using a qRT-PCR, and metabolic parameters were assessed using an ELISA assay. We demonstrated that B. longum NBM7-1 in the CKD1 group and L. rhamnosus NBM17-4 in the CKD2 group alleviate T2D development through the upregulation of IL-22, which enhances insulin sensitivity and pancreatic functions while reducing liver steatosis. These findings suggest that B. longum NBM7-1 and L. rhamnosus NBM17-4 could be the candidate probiotics for the therapeutic treatments of T2D patients as well as the prevention of type 2 diabetes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data Availability

The datasets generated during the current study are available in the GenBank (Web link: https://www.ncbi.nlm.nih.gov/genbank/).

References

  1. Zheng Y, Ley SH, Hu FB (2018) Global aetiology and epidemiology of type 2 diabetes mellitus and its complications. Nat Rev Endocrinol 14(2):88–98. https://doi.org/10.1038/nrendo.2017.151

    Article  PubMed  Google Scholar 

  2. Wang X, Yang J, Qiu X, Wen Q, Liu M, Zhou D et al (2021) Probiotics, pre-biotics and synbiotics in the treatment of pre-diabetes: a systematic review of randomized controlled trials. Front Public Health 9:645035. https://doi.org/10.3389/fpubh.2021.645035

    Article  PubMed  PubMed Central  Google Scholar 

  3. Mambiya M, Shang M, Wang Y, Li Q, Liu S, Yang L et al (2019) The play of genes and non-genetic factors on type 2 diabetes. Front Public Health 7:349. https://doi.org/10.3389/fpubh.2019.00349

    Article  PubMed  PubMed Central  Google Scholar 

  4. Foretz M, Guigas B, Bertrand L, Pollak M, Viollet B (2014) Metformin: from mechanisms of action to therapies. Cell Metab 20(6):953–966. https://doi.org/10.1016/j.cmet.2014.09.018

    Article  CAS  PubMed  Google Scholar 

  5. Bösenberg LH, van Zyl DG (2014) The mechanism of action of oral antidiabetic drugs: a review of recent literature. J Endocrinol Metab Diabetes S Afr 13(3):80–88. https://doi.org/10.1080/22201009.2008.10872177

    Article  Google Scholar 

  6. Bischoff H (1995) The mechanism of alpha-glucosidase inhibition in the management of diabetes. Clin Invest Med 18(4):303–311

    CAS  PubMed  Google Scholar 

  7. Hauner H (2002) The mode of action of thiazolidinediones. Diabetes Metab Res Rev 18(Suppl 2):S10-15. https://doi.org/10.1002/dmrr.249

    Article  CAS  PubMed  Google Scholar 

  8. Thornberry NA, Gallwitz B (2009) Mechanism of action of inhibitors of dipeptidyl-peptidase–4 (DPP–4). Best Pract Res Clin Endocrinol Metab 23(4):479–486. https://doi.org/10.1016/j.beem.2009.03.004

    Article  CAS  PubMed  Google Scholar 

  9. Kalra S (2014) Sodium Glucose Co-Transporter-2 (SGLT2) Inhibitors: a review of their basic and clinical pharmacology. Diabetes Ther 5(2):355–366. https://doi.org/10.1007/s13300-014-0089-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Drucker DJ (2018) Mechanisms of action and therapeutic application of glucagon-like peptide-1. Cell Metab 27(4):740–756. https://doi.org/10.1016/j.cmet.2018.03.001

    Article  CAS  PubMed  Google Scholar 

  11. McGuckin MA, Eri R, Simms LA, Florin TH, Radford-Smith G (2009) Intestinal barrier dysfunction in inflammatory bowel diseases. Inflamm Bowel Dis 15(1):100–113. https://doi.org/10.1002/ibd.20539

    Article  PubMed  Google Scholar 

  12. Boroni Moreira AP, Teixeira FS, T., do, C. G. P. M., & de Cássia Gonçalves Alfenas, R. (2012) Gut microbiota and the development of obesity. Nutr Hosp 27(5):1408–1414. https://doi.org/10.3305/nh.2012.27.5.5887

    Article  CAS  PubMed  Google Scholar 

  13. Archer AC, Muthukumar SP, Halami PM (2021) Lactobacillus fermentum MCC2759 and MCC2760 alleviate inflammation and intestinal function in high-fat diet-fed and streptozotocin-induced diabetic rats. Probiotics Antimicrob Proteins 13(4):1068–1080. https://doi.org/10.1007/s12602-021-09744-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Wu T, Zhang Y, Li W, Zhao Y, Long H, Muhindo EM et al (2021) Lactobacillus rhamnosus LRa05 ameliorate hyperglycemia through a regulating glucagon-mediated signaling pathway and gut microbiota in type 2 diabetic mice. J Agric Food Chem 69(31):8797–8806. https://doi.org/10.1021/acs.jafc.1c02925

    Article  CAS  PubMed  Google Scholar 

  15. Toejing P, Khat-Udomkiri N, Intakhad J, Sirilun S, Chaiyasut C, Lailerd N (2020) Putative mechanisms responsible for the antihyperglycemic action of Lactobacillus paracasei HII01 in experimental type 2 diabetic rats. Nutrients 12(10). https://doi.org/10.3390/nu12103015

  16. Zheng F, Wang Z, Stanton C, Ross RP, Zhao J, Zhang H et al (2021) Lactobacillus rhamnosus FJSYC4–1 and Lactobacillus reuteri FGSZY33L6 alleviate metabolic syndrome via gut microbiota regulation. Food Funct 12(9):3919–3930. https://doi.org/10.1039/D0FO02879G

  17. Muganga L, Liu X, Tian F, Zhao J, Zhang H, Chen W (2015) Screening for lactic acid bacteria based on antihyperglycaemic and probiotic potential and application in synbiotic set yoghurt. Journal of Functional Foods 16:125–136. https://doi.org/10.1016/j.jff.2015.04.030

    Article  CAS  Google Scholar 

  18. Ankolekar C, Johnson D, Pinto Mda S, Johnson K, Labbe R, Shetty K (2011) Inhibitory potential of tea polyphenolics and influence of extraction time against Helicobacter pylori and lack of inhibition of beneficial lactic acid bacteria. J Med Food 14(11):1321–1329. https://doi.org/10.1089/jmf.2010.0237

    Article  CAS  PubMed  Google Scholar 

  19. Chelakkot C, Ghim J, Ryu SH (2018) Mechanisms regulating intestinal barrier integrity and its pathological implications. Exp Mol Med 50(8):1–9. https://doi.org/10.1038/s12276-018-0126-x

    Article  CAS  PubMed  Google Scholar 

  20. Cunningham AL, Stephens JW, Harris DA (2021) Gut microbiota influence in type 2 diabetes mellitus (T2DM). Gut Pathog 13(1):50. https://doi.org/10.1186/s13099-021-00446-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Zhao L, Lou H, Peng Y, Chen S, Zhang Y, Li X (2019) Comprehensive relationships between gut microbiome and faecal metabolome in individuals with type 2 diabetes and its complications. Endocrine 66(3):526–537. https://doi.org/10.1007/s12020-019-02103-8

    Article  CAS  PubMed  Google Scholar 

  22. Liu C, Shao W, Gao M, Liu J, Guo Q, Jin J et al (2020) Changes in intestinal flora in patients with type 2 diabetes on a low-fat diet during 6 months of follow-up. Exp Ther Med 20(5):40. https://doi.org/10.3892/etm.2020.9167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Zhao L, Zhang F, Ding X, Wu G, Lam YY, Wang X et al (2018) Gut bacteria selectively promoted by dietary fibers alleviate type 2 diabetes. 359(6380):1151–1156. https://doi.org/10.1126/science.aao5774

  24. Tennoune N, Andriamihaja M, Blachier F (2022) Production of indole and indole-related compounds by the intestinal microbiota and consequences for the host: the good, the bad, and the ugly. Microorganisms 10(5). https://doi.org/10.3390/microorganisms10050930

  25. Thomas C, Pellicciari R, Pruzanski M, Auwerx J, Schoonjans K (2008) Targeting bile-acid signalling for metabolic diseases. Nat Rev Drug Discov 7(8):678–693. https://doi.org/10.1038/nrd2619

    Article  CAS  Google Scholar 

  26. Blaut M (2015) Gut microbiota and energy balance: role in obesity. Proc Nutr Soc 74(3):227–234. https://doi.org/10.1017/S0029665114001700

    Article  CAS  PubMed  Google Scholar 

  27. Brooks L, Viardot A, Tsakmaki A, Stolarczyk E, Howard JK, Cani PD et al (2017) Fermentable carbohydrate stimulates FFAR2-dependent colonic PYY cell expansion to increase satiety. Mol Metab 6(1):48–60. https://doi.org/10.1016/j.molmet.2016.10.011

    Article  CAS  PubMed  Google Scholar 

  28. Ghosh S, Whitley CS, Haribabu B, Jala VR (2021) Regulation of intestinal barrier function by microbial metabolites. Cell Mol Gastroenterol Hepatol 11(5):1463–1482. https://doi.org/10.1016/j.jcmgh.2021.02.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Okumura R, Takeda K (2018) Maintenance of intestinal homeostasis by mucosal barriers. Inflamm Regen 38:5. https://doi.org/10.1186/s41232-018-0063-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Keir M, Yi Y, Lu T, Ghilardi N (2020) The role of IL-22 in intestinal health and disease. J Exp Med 217(3):e20192195. https://doi.org/10.1084/jem.20192195

    Article  PubMed  PubMed Central  Google Scholar 

  31. Avitabile S, Odorisio T, Madonna S, Eyerich S, Guerra L, Eyerich K et al (2015) Interleukin-22 promotes wound repair in diabetes by improving keratinocyte pro-healing functions. J Invest Dermatol 135(11):2862–2870. https://doi.org/10.1038/jid.2015.278

    Article  CAS  PubMed  Google Scholar 

  32. Wang X, Ota N, Manzanillo P, Kates L, Zavala-Solorio J, Eidenschenk C et al (2014) Interleukin-22 alleviates metabolic disorders and restores mucosal immunity in diabetes. Nature 514(7521):237–241. https://doi.org/10.1038/nature13564

    Article  CAS  PubMed  Google Scholar 

  33. Zhang C-X, Wang H-Y, Chen T-X (2019) Interactions between intestinal microflora/probiotics and the immune system. Biomed Res Int 2019:6764919. https://doi.org/10.1155/2019/6764919

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Hou Q, Ye L, Liu H, Huang L, Yang Q, Turner JR et al (2018) Lactobacillus accelerates ISCs regeneration to protect the integrity of intestinal mucosa through activation of STAT3 signaling pathway induced by LPLs secretion of IL-22. Cell Death Differ 25(9):1657–1670. https://doi.org/10.1038/s41418-018-0070-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Vlavcheski F, Tsiani E (2018) Attenuation of free fatty acid-induced muscle insulin resistance by rosemary extract. Nutrients 10(11). https://doi.org/10.3390/nu10111623

  36. Artasensi A, Pedretti A, Vistoli G, Fumagalli L (2020) Type 2 diabetes mellitus: a review of multi-target drugs. Molecules 25(8). https://doi.org/10.3390/molecules25081987

  37. Firouzi S, Majid HA, Ismail A, Kamaruddin NA, Barakatun-Nisak MY (2017) Effect of multi-strain probiotics (multi-strain microbial cell preparation) on glycemic control and other diabetes-related outcomes in people with type 2 diabetes: a randomized controlled trial. Eur J Nutr 56(4):1535–1550. https://doi.org/10.1007/s00394-016-1199-8

    Article  CAS  PubMed  Google Scholar 

  38. Wa Y, Yin B, He Y, Xi W, Huang Y, Wang C et al (2019) Effects of single probiotic- and combined probiotic-fermented milk on lipid metabolism in hyperlipidemic rats. [Original Research]. 10. https://doi.org/10.3389/fmicb.2019.01312

  39. Luo M, Yan J, Wu L, Wu J, Chen Z, Jiang J et al (2021) Probiotics alleviated nonalcoholic fatty liver disease in high-fat diet-fed rats via gut microbiota/FXR/FGF15 signaling pathway. J Immunol Res 2021:2264737. https://doi.org/10.1155/2021/2264737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Xia Y, Chen Y, Wang G, Yang Y, Song X, Xiong Z et al (2020) Lactobacillus plantarum AR113 alleviates DSS-induced colitis by regulating the TLR4/MyD88/NF-κB pathway and gut microbiota composition. J Functional Foods 67. https://doi.org/10.1016/j.jff.2020.103854

  41. Lee Y-S, Lee D, Park G-S, Ko S-H, Park J, Lee Y-K et al (2021) Lactobacillus plantarum HAC01 ameliorates type 2 diabetes in high-fat diet and streptozotocin-induced diabetic mice in association with modulating the gut microbiota. Food Funct 12(14):6363–6373. https://doi.org/10.1039/D1FO00698C

    Article  CAS  PubMed  Google Scholar 

  42. Ai X, Wu C, Yin T, Zhur O, Liu C, Yan X et al (2021) Antidiabetic function of Lactobacillus fermentum MF423-fermented rice bran and its effect on gut microbiota structure in type 2 diabetic mice. Front Microbiol 12:682290. https://doi.org/10.3389/fmicb.2021.682290

    Article  PubMed  PubMed Central  Google Scholar 

  43. Farida E, Nuraida L, Giriwono PE, Jenie BSL (2020) Lactobacillus rhamnosus reduces blood glucose level through downregulation of gluconeogenesis gene expression in streptozotocin-induced diabetic rats. Int J Food Sci 2020:6108575. https://doi.org/10.1155/2020/6108575

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Putt KK, Pei R, White HM, Bolling BW (2017) Yogurt inhibits intestinal barrier dysfunction in Caco-2 cells by increasing tight junctions. Food Funct 8(1):406–414. https://doi.org/10.1039/c6fo01592a

    Article  CAS  PubMed  Google Scholar 

  45. Kim E, Cui J, Kang I, Zhang G, Lee Y (2021) Potential antidiabetic effects of seaweed extracts by upregulating glucose utilization and alleviating inflammation in C2C12 myotubes. Int J Environ Res Public Health 18(3). https://doi.org/10.3390/ijerph18031367

  46. Kim SH, Huh CS, Choi ID, Jeong JW, Ku HK, Ra JH et al (2014) The anti-diabetic activity of Bifidobacterium lactis HY8101 in vitro and in vivo. J Appl Microbiol 117(3):834–845. https://doi.org/10.1111/jam.12573

    Article  CAS  PubMed  Google Scholar 

  47. Leahy JL, Hirsch IB, Peterson KA, Schneider D (2010) Targeting beta-cell function early in the course of therapy for type 2 diabetes mellitus. J Clin Endocrinol Metab 95(9):4206–4216. https://doi.org/10.1210/jc.2010-0668

    Article  CAS  PubMed  Google Scholar 

  48. Kwon MJ, Lee YJ, Jung HS, Shin HM, Kim TN, Lee SH et al (2019) The direct effect of lobeglitazone, a new thiazolidinedione, on pancreatic beta cells: a comparison with other thiazolidinediones. Diabetes Res Clin Pract 151:209–223. https://doi.org/10.1016/j.diabres.2019.04.006

    Article  CAS  PubMed  Google Scholar 

  49. Manaer T, Yu L, Nabi XH, Dilidaxi D, Liu L, Sailike J (2021) The beneficial effects of the composite probiotics from camel milk on glucose and lipid metabolism, liver and renal function and gut microbiota in db/db mice. BMC Complement Med Ther 21(1):127. https://doi.org/10.1186/s12906-021-03303-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Hsieh PS, Ho HH, Tsao SP, Hsieh SH, Lin WY, Chen JF et al (2021) Multi-strain probiotic supplement attenuates streptozotocin-induced type-2 diabetes by reducing inflammation and β-cell death in rats. PLoS ONE 16(6):e0251646. https://doi.org/10.1371/journal.pone.0251646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Li C, Li X, Han H, Cui H, Peng M, Wang G et al (2016) Effect of probiotics on metabolic profiles in type 2 diabetes mellitus: a meta-analysis of randomized, controlled trials. Medicine 95(26):e4088. https://doi.org/10.1097/md.0000000000004088

    Article  PubMed  PubMed Central  Google Scholar 

  52. Bae UJ, Park SH, Jung SY, Park BH, Chae SW (2015) Hypoglycemic effects of aqueous persimmon leaf extract in a murine model of diabetes. Mol Med Rep 12(2):2547–2554. https://doi.org/10.3892/mmr.2015.3766

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Gross DN, van den Heuvel APJ, Birnbaum MJ (2008) The role of FoxO in the regulation of metabolism. Oncogene 27(16):2320–2336. https://doi.org/10.1038/onc.2008.25

    Article  CAS  PubMed  Google Scholar 

  54. Altomonte J, Richter A, Harbaran S, Suriawinata J, Nakae J, Thung SN et al (2003) Inhibition of Foxo1 function is associated with improved fasting glycemia in diabetic mice. Am J Physiol Endocrinol Metab 285(4):E718–728. https://doi.org/10.1152/ajpendo.00156.2003

    Article  CAS  PubMed  Google Scholar 

  55. Honma M, Sawada S, Ueno Y, Murakami K, Yamada T, Gao J et al (2018) Selective insulin resistance with differential expressions of IRS-1 and IRS-2 in human NAFLD livers. Int J Obes 42(9):1544–1555. https://doi.org/10.1038/s41366-018-0062-9

    Article  CAS  Google Scholar 

  56. Ryu R, Kwon E-Y, Choi J-Y, Shon JC, Liu K-H, Choi M-S (2019) Chrysanthemum leaf ethanol extract prevents obesity and metabolic disease in diet-induced obese mice via lipid mobilization in white adipose tissue 11(6):1347

    CAS  Google Scholar 

  57. Wahli W, Michalik L (2012) PPARs at the crossroads of lipid signaling and inflammation. Trends Endocrinol Metab 23(7):351–363. https://doi.org/10.1016/j.tem.2012.05.001

    Article  CAS  PubMed  Google Scholar 

  58. Inoue M, Ohtake T, Motomura W, Takahashi N, Hosoki Y, Miyoshi S et al (2005) Increased expression of PPARgamma in high fat diet-induced liver steatosis in mice. Biochem Biophys Res Commun 336(1):215–222. https://doi.org/10.1016/j.bbrc.2005.08.070

    Article  CAS  PubMed  Google Scholar 

  59. Lee YH, Kim JH, Kim SR, Jin HY, Rhee EJ, Cho YM et al (2017) Lobeglitazone, a novel thiazolidinedione, improves non-alcoholic fatty liver disease in type 2 diabetes: its efficacy and predictive factors related to responsiveness. J Korean Med Sci 32(1):60–69. https://doi.org/10.3346/jkms.2017.32.1.60

    Article  CAS  PubMed  Google Scholar 

  60. Zai W, Chen W, Liu H, Ju D (2021) Therapeutic opportunities of IL-22 in non-alcoholic fatty liver disease: from molecular mechanisms to clinical applications. Biomedicines 9(12). https://doi.org/10.3390/biomedicines9121912

  61. Abadpour S, Halvorsen B, Sahraoui A, Korsgren O, Aukrust P, Scholz H (2018) Interleukin-22 reverses human islet dysfunction and apoptosis triggered by hyperglycemia and LIGHT. J Mol Endocrinol 60(3):171–183. https://doi.org/10.1530/JME-17-0182

    Article  CAS  PubMed  Google Scholar 

  62. Xuan X, Tian Z, Zhang M, Zhou J, Gao W, Zhang Y et al (2018) Diverse effects of interleukin-22 on pancreatic diseases. Pancreatology 18(3):231–237. https://doi.org/10.1016/j.pan.2018.02.014

    Article  CAS  PubMed  Google Scholar 

  63. Parks OB, Pociask DA, Hodzic Z, Kolls JK, Good M (2015) Interleukin-22 signaling in the regulation of intestinal health and disease. Front Cell Dev Biol 3:85. https://doi.org/10.3389/fcell.2015.00085

    Article  PubMed  Google Scholar 

  64. Vazquez-Gutierrez P, Lacroix C, Jaeggi T, Zeder C, Zimmerman MB, Chassard C (2015) Bifidobacteria strains isolated from stools of iron deficient infants can efficiently sequester iron. BMC Microbiol 15(1):3. https://doi.org/10.1186/s12866-014-0334-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Wang H, Li L (2022) Comprehensive evaluation of probiotic property, hypoglycemic ability and antioxidant activity of lactic acid bacteria. Foods (Basel, Switzerland) 11(9). https://doi.org/10.3390/foods11091363

  66. Wu P, Wu D, Ni C, Ye J, Chen W, Hu G et al (2014) gammadeltaT17 cells promote the accumulation and expansion of myeloid-derived suppressor cells in human colorectal cancer. Immunity 40(5):785–800. https://doi.org/10.1016/j.immuni.2014.03.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Kyoko OO, Kono H, Ishimaru K, Miyake K, Kubota T, Ogawa H et al (2014) Expressions of tight junction proteins Occludin and Claudin-1 are under the circadian control in the mouse large intestine: implications in intestinal permeability and susceptibility to colitis. PLoS ONE 9(5):e98016. https://doi.org/10.1371/journal.pone.0098016

    Article  CAS  PubMed  Google Scholar 

  68. Gallego FQ, Sinzato YK, Miranda CA, Iessi IL, Dallaqua B, Volpato GT et al (2018) Pancreatic islet response to diabetes during pregnancy in rats. Life Sci 214:1–10. https://doi.org/10.1016/j.lfs.2018.10.046

    Article  CAS  PubMed  Google Scholar 

  69. Song I, Patel O, Himpe E, Muller CJ, Bouwens L (2015) Beta cell mass restoration in alloxan-diabetic mice treated with EGF and Gastrin. PLoS ONE 10(10):e0140148. https://doi.org/10.1371/journal.pone.0140148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Shimizu T, Kida Y, Kuwano K (2008) Mycoplasma pneumoniae-derived lipopeptides induce acute inflammatory responses in the lungs of mice. Infect Immun 76(1):270–277. https://doi.org/10.1128/iai.00955-07

    Article  CAS  PubMed  Google Scholar 

  71. Sugimoto K, Ogawa A, Mizoguchi E, Shimomura Y, Andoh A, Bhan AK et al (2008) IL-22 ameliorates intestinal inflammation in a mouse model of ulcerative colitis. J Clin Invest 118(2):534–544. https://doi.org/10.1172/jci33194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Yang Z-H, Miyahara H, Takeo J, Katayama M (2012) Diet high in fat and sucrose induces rapid onset of obesity-related metabolic syndrome partly through rapid response of genes involved in lipogenesis, insulin signalling and inflammation in mice. Diabetol Metab Syndr 4(1):32. https://doi.org/10.1186/1758-5996-4-32

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Laaksonen H, Guerreiro-Cacais AO, Adzemovic MZ, Parsa R, Zeitelhofer M, Jagodic M et al (2014) The multiple sclerosis risk gene IL22RA2 contributes to a more severe murine autoimmune neuroinflammation. Genes Immun 15(7):457–465. https://doi.org/10.1038/gene.2014.36

    Article  CAS  PubMed  Google Scholar 

  74. Almohazey D, Lo Y-H, Vossler CV, Simmons AJ, Hsieh JJ, Bucar EB et al (2017) The ErbB3 receptor tyrosine kinase negatively regulates Paneth cells by PI3K-dependent suppression of Atoh1. Cell Death Differ 24(5):855–865. https://doi.org/10.1038/cdd.2017.27

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Kwon E-Y, Kim SY, Choi M-S (2018) Luteolin-enriched artichoke leaf extract alleviates the metabolic syndrome in mice with high-fat diet-induced obesity 10(8):979

    Google Scholar 

  76. Monmai C, Park SH, You S, Park WJ (2018) Immuno-enhancement effect of polysaccharide extracted from Stichopus japonicus on cyclophosphamide-induced immunosuppression mice. Food science and biotechnology 27(2):565–573. https://doi.org/10.1007/s10068-017-0248-2

    Article  CAS  PubMed  Google Scholar 

  77. Kim TK, Lee J-C, Im S-H, Lee M-S (2020) Amelioration of autoimmune diabetes of NOD mice by immunomodulating probiotics. [Original Research]. 11. https://doi.org/10.3389/fimmu.2020.01832

Download references

Acknowledgements

Our sincere thanks are also extended to Dr. Seung-Young Park, a senior research scientist of the Institute of GBST in the SNU for their invaluable assistance in proofreading and editing the revised manuscript.

Funding

This work was supported financially by Chong Kun Dang Bio Co. Ltd.

Author information

Authors and Affiliations

  1. Department of Agricultural Biotechnology, College of Agriculture Sciences, Seoul National University, Seoul, South Korea

    Won Jun Kim & Heebal Kim

  2. Institute of Green-Bio Science & Technology, Seoul National University, Pyeongchang, South Korea

    Ri Ryu, Eun-Hee Doo & Chul Sung Huh

  3. Department of Yuhan Biotechnology, School of Bio-Health Sciences, Yuhan University, Bucheon, 14780, South Korea

    Eun-Hee Doo

  4. Research Institute, Chong Kun Dang Bio Co. Ltd, Ansan, South Korea

    Yukyung Choi, Kyunghwan Kim & Byoung Kook Kim

  5. Department of Animal Science and Biotechnology, Seoul National University, Seoul, South Korea

    Heebal Kim

  6. Department of Animal Science, Pusan National University, Miryang, South Korea

    Myunghoo Kim

  7. Graduate School of International Agricultural Technology, Seoul National University, Pyeongchang, South Korea

    Chul Sung Huh

Authors
  1. Won Jun Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ri Ryu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eun-Hee Doo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yukyung Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kyunghwan Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Byoung Kook Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Heebal Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Myunghoo Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Chul Sung Huh
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

WJK, RR, YKC, KHK, BKK, HBK and CSH conceived and designed the experiments; WJK, and RR performed the experiments; WJK, RR, and CSH analyzed the data; WJK, RR, EHD, and CSH contributed data or analysis tools; MHK and CSH wrote the paper; WJK, MHK, and CSH reviewed and edited the paper.

Corresponding authors

Correspondence to Myunghoo Kim or Chul Sung Huh.

Ethics declarations

Conflicts of Interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Wonjun Kim and Ri Ryu contributed equally to this work

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kim, W.J., Ryu, R., Doo, EH. et al. 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 & Antimicro. Prot. (2023). https://doi.org/10.1007/s12602-023-10156-5

Download citation

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12602-023-10156-5

Keywords

Search

Navigation