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Improvement in glucose tolerance and insulin sensitivity by probiotic strains of Indian gut origin in high-fat diet-fed C57BL/6J mice

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Abstract

Purpose

Diabetes and obesity are characterized by glucose intolerance, fat deposition, inflammation, and dyslipidemia. Recent reports postulated that distinct gut microbiota alterations were observed in obese/diabetic subjects and modulating gut microbiota beneficially through specific probiotics could be a potential therapeutic option for type 2 diabetes/obesity. Therefore, we attempted to study the efficacy of probiotics of Indian gut origin (Lactobacillus plantarum MTCC5690 and Lactobacillus fermentum MTCC5689) along with a positive control, Lactobacillus rhamnosus (LGG) on glucose/lipid homeostasis in high-fat-diet-induced diabetic animal model.

Methods

C57BL/6J male mice were divided into seven groups (n = 6 per group) comprising feeding on: (1) Normal Pellet Diet (NPD), (2) High-Fat Diet (HFD), (3) HFD with LGG, (4) HFD with MTCC5690, (5) HFD with MTCC5689, (6) HFD with metformin, and 7) HFD with vildagliptin for a period of 6 months. Biochemical markers, glucose tolerance, insulin resistance, and GLP-1 and LPS levels were assessed by standard protocols. Gut integrity was measured by intestinal permeability test. Transcriptional levels of tight junction proteins (TJPs) were probed in small intestinal tissues while inflammatory signals and other pathway specific genes were profiled in liver, visceral adipose tissue, and skeletal muscle.

Results

Mice fed with HFD became insulin resistant, glucose intolerant, hyperglycemic, and dyslipidemic. Diabetic mice were characterized to exhibit decreased levels of GLP-1, increased gut permeability, increased circulatory levels of LPS, decrease in the gene expression patterns of intestinal tight junction markers (occludin and ZO-1), and increased proinflammatory gene markers (TNFα and IL6) in visceral fat along with decreased mRNA expression of FIAF and adiponectin. Diabetic mice also exhibited increased mRNA expression of ER stress markers in skeletal muscle. In addition, liver from HFD-fed diabetic mice showed increased gene expressions of proinflammation, lipogenesis, and gluconeogenesis. Probiotic interventions (most prominently the MTCC5689) resisted insulin resistance and development of diabetes in mice under HFD feeding and beneficially modulated all the biochemical and molecular alterations in a mechanistic way in several tissues. The metabolic benefits offered by the probiotics were also more or less similar to that of standard drugs such as metformin and vildagliptin.

Conclusion

Native probiotic strains MTCC 5690 and MTCC 5689 appear to have potential against insulin resistance and type 2 diabetes with mechanistic, multiple tissue-specific mode of actions.

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Abbreviations

MTCC 5690:

Lactobacillus plantarum Lp91

MTCC 5689:

Lactobacillus fermentum Lf1

LGG:

Lactobacillus rhamnosus GG

FIAF:

Fasting-induced adipocyte factor

ZO-1:

Zonula occludens-1

NPD:

Normal pellet diet

HFD:

High-fat diet

IL6:

Interleukin 6

TNFα:

Tumor necrosis factor alpha

LPS:

Lipopolysaccharide

GRP78:

Glucose-regulated protein 78

PERK:

Protein kinase R (PKR)-like endoplasmic reticulum kinase

IRE1-α:

Inositol-requiring enzyme 1 alpha

XBP1:

X-box-binding protein 1

CHOP:

CCAAT-enhancer-binding protein homologous protein

SREBP-1c:

Sterol regulatory element-binding protein 1 (SREBP-1)

GLUT4:

Glucose transporter, member 4

MCP1:

Monocyte chemoattractant protein-1

GCK:

Glucokinase

PEPCK:

Phosphoenolpyruvate carboxykinase

G6Pc:

Glucose-6-phosphatase catalytic subunit

FOXO1:

Forkhead box protein O1

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Acknowledgments

Financial assistance from Department of Biotechnology (DBT, New Delhi, Government of India) is greatly acknowledged. BM acknowledges Council of Scientific and Industrial Research (CSIR), New Delhi for Research Associateship.

Authors contributions

MB conceived, designed, supervised, and commented on all drafts of this paper. BM, DP, PP, CS, SR, AS, NR and RK coordinated the animal study, conducted the overall experiments and participated in the data collection and analysis, molecular investigations and helped in the drafts. VM, SG, VKB, and MB contributed to data interpretation and manuscript completion.

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Authors and Affiliations

  1. Department of Cell and Molecular Biology, Dr. Rema Mohan High-Throughput Screening (HTS) Lab, Madras Diabetes Research Foundation and Dr. Mohan’s Diabetes Specialties Centre, 4, Conran Smith Road, Gopalapuram, Chennai, 600 086, India

    Mahalingam Balakumar, Durai Prabhu, Chandrakumar Sathishkumar, Paramasivam Prabu, Ramesh Kumar, Srividhya Raghavan, Avinash Soundarajan, Viswanathan Mohan & Muthuswamy Balasubramanyam

  2. National Dairy Research Institute (NDRI), Karnal, Haryana, 132001, India

    Namita Rokana, Sunita Grover & Virender Kumar Batish

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  1. Mahalingam Balakumar
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This study was conducted as per the compliance of Committee for the Purpose of Control And Supervision of Experiments on Animals (CPCSEA) guidelines, Government of India.

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Balakumar, M., Prabhu, D., Sathishkumar, C. et al. Improvement in glucose tolerance and insulin sensitivity by probiotic strains of Indian gut origin in high-fat diet-fed C57BL/6J mice. Eur J Nutr 57, 279–295 (2018). https://doi.org/10.1007/s00394-016-1317-7

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