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“Ficus johannis Boiss. leaves ethanolic extract ameliorate streptozotocin-induced diabetes in rats by upregulating the expressions of GCK, GLUT4, and IGF and downregulating G6P”

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Abstract

The leaves of Ficus johannis Boiss (F. johannis), commonly known as Fig tree, Anjir, and Teen, are used by the folk medicinal practitioners in Iran for controlling hyperglycemia in diabetic patients. This study investigated the pharmacological basis for antidiabetic effect of the ethanolic extract of F. johannis leaves using in vitro and in vivo experimental models. Qualitative screening of phytochemicals, estimation of total phenolic and flavonoid contents, and in vitro antioxidant and α-amylase inhibition assays were performed. Moreover, the High-performance liquid chromatography (HPLC) quantification, acute toxicity, glucose tolerance, and in vivo antidiabetic effect along with the evaluation of gene expressions involved in diabetes mellitus were carried out. Significant quantities of phenolic (71.208 ± 2.89 mgg−1 GAE) and flavonoid (26.38 ± 3.53 mgg−1 QE) were present. Inhibitory concentration (IC50) of the plant extract exhibited an excellent in vitro antioxidant (IC50 = 33.81 µg/mL) and α-amylase (IC50 = 12.18 µg/mL) inhibitory potential. The HPLC analysis confirmed the gallic acid (257.79 mgg−1) as main constituent of the extract followed by kaempferol (22.86 mgg−1), myricetin (0.16 mgg−1), and quercetin (3.22 mgg−1). Ethanolic extract displayed glucose tolerance in normo-glycemic rats. Streptozotocin-induced hyperglycemia declined dose dependently in the extract treated rats with improvement in lipid profile and liver and renal function biomarkers. The F. johannis-treated groups showed an increase in mRNA expressions of glucose transporter 4 (GLUT-4), glucokinase, insulin growth like factor 1 and peroxisomal proliferator activating receptor gamma in pancreas. However, the Glucose-6-phosphatase was downregulated. Present study suggests that the ethanolic extract of F. johannis leaves demonstrates a good anti-diabetic profile by improving insulin sensitivity, GLUT-4 translocation, and carbohydrate metabolism while inhibiting lipogenesis.

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Data availability

The data that support the findings of this study are available and submitted in form of supplementary file along with the manuscript.

Abbreviations

ALT:

Aalanine aminotransferase

ALP:

Alkaline phosphatase

AlCl3:

Aluminium chloride

AST:

Aspartate aminotransferase

DC:

Diabetic control

DM:

Diabetes mellitus

DMSO:

Dimethylsulfoxide

EDTA:

Ethylenediaminetetraacetic acid

F. johannis :

Ficus johannis Boiss.

FJ 125:

Ficus johannis 125 Mg/kg

FJ 250:

Ficus johannis 250 Mg/kg

FJ 500:

Ficus johannis 500 Mg/kg

FC:

Folin-Ciocalteu’s

G6P:

Glucose-6-Phosphatase

GCK:

Glucokinase

GLUT4:

Glucose transporter 4

GAPDH:

Glyceraldehyde-3-phosphate dehydrogenase

GAE:

Gallic acid equivalent

HDL:

High density lipoproteins

H&E:

Haematoxylin and eosin

HPLC:

High-performance liquid chromatography

IC:

Inhibitor concentration

IREC:

Institutional Research Ethics Committee

IGF:

Insulin growth like factor

LDL:

Low density lipoproteins

NIDDM:

Non-insulin-dependent diabetes mellitus

NA:

Nicotinamide

NC:

Normal control

NFJ:

Normal + Ficus johannis

OGTT:

Oral glucose tolerance test

OECD:

Organization for Economic and Co-operation and Development

PPAR-γ:

Peroxisomal proliferator activating receptor gamma

PC:

Positive control

CH3CO2K:

Potassium acetate

PCNA:

Proliferating cell nuclear antigen

RT-PCR:

Reverse transcriptase polymerase chain reaction

PPN:

Parts per million

RNA:

Ribonucleic acid

Na2CO3 :

Sodium carbonate

STZ:

Streptozotocin

TOP2A:

Topoisomerase 2 alpha

TC:

Total cholesterol level

TG:

Triglyceride level

UV:

Ultraviolet

v-LDL:

Very low-density lipoproteins

WHO:

World Health Organization

DPPH:

2,2-Diphenyl-1-picrylhydrazyl

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Authors and Affiliations

  1. Faculty of Pharmacy, The University of Lahore, 1Km- Off Defense Road, Lahore, Pakistan

    Afshan Asghar

  2. Department of Pharmacology, Institute of Pharmacy, Faculty of Pharmaceutical and Allied Health Sciences, Lahore College for Women University, Jail Road, Lahore, Pakistan

    Ali Sharif

  3. Department of Zoology, Kinnaird College for Women Lahore, 1Km- Off Defense Road, Lahore, Pakistan

    Sana Javaid Awan

  4. Department of Pharmacy, University of Agriculture, Faisalabad, Pakistan

    Bushra Akhtar

  5. Riphah Institute of Pharmaceutical Sciences, Riphah International University, Lahore Campus, Lahore, Pakistan

    Muhammad Furqan Akhtar

  6. Department of Chemistry - Ångström Laboratory, Physical Chemistry, Uppsala University, Uppsala, Sweden

    Sajid Ali

  7. Department of Chemistry, Lahore College for Women University, Jail Road, Lahore, Pakistan

    Shahnaz

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  1. Afshan Asghar
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  2. Ali Sharif
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  3. Sana Javaid Awan
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  4. Bushra Akhtar
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  5. Muhammad Furqan Akhtar
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  6. Sajid Ali
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  7. Shahnaz
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Contributions

Afshan Asghar performed most of the experimental work and participated in data interpretation. Bushra Akhtar and Muhammad Furqan Akhtar participated in the data analysis and statistical analysis. Ali Sharif and Sana Javaid Awan conceived the study and carried out the experimental design and data interpretation. Ali Sharif, Shahnaz, and Sajid Ali prepared and revised the manuscript. All authors read and approved the final manuscript.

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Correspondence to Ali Sharif.

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The study was conducted followed by the approval of Animal Ethical Committee (IREC-2019–87) in accordance with the NC3Rs ARRIVE Guidelines, adhere to ethical guidelines of The Basel Declaration, the International Council for Laboratory Animal Science (ICLAS) ethical guidelines, and Directive 2010/63/EU.

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Asghar, A., Sharif, A., Awan, S.J. et al. “Ficus johannis Boiss. leaves ethanolic extract ameliorate streptozotocin-induced diabetes in rats by upregulating the expressions of GCK, GLUT4, and IGF and downregulating G6P”. Environ Sci Pollut Res 30, 49108–49124 (2023). https://doi.org/10.1007/s11356-023-25765-4

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