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Deciphering the multi-functional role of Indian propolis for the management of Alzheimer’s disease by integrating LC–MS/MS, network pharmacology, molecular docking, and in-vitro studies

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Abstract

The conventional one-drug-one-disease theory has lost its sheen in multigenic diseases such as Alzheimer’s disease (AD). Propolis, a honeybee-derived product has ethnopharmacological evidence of antioxidant, anti-inflammatory, antimicrobial and neuroprotective properties. However, the chemical composition is complex and highly variable geographically. So, to leverage the potential of propolis as an effective treatment modality, it is essential to understand the role of each phytochemical in the AD pathophysiology. Therefore, the present study was aimed at investigating the anti-Alzheimer effect of bioactive in Indian propolis (IP) by combining LC–MS/MS fingerprinting, with network-based analysis and experimental validation. First, phytoconstituents in IP extract were identified using an in-house LC–MS/MS method. The drug likeness and toxicity were assessed, followed by identification of AD targets. The constituent–target–gene network was then constructed along with protein–protein interactions, gene pathway, ontology, and enrichment analysis. LC–MS/MS analysis identified 16 known metabolites with druggable properties except for luteolin-5-methyl ether. The network pharmacology-based analysis revealed that the hit propolis constituents were majorly flavonoids, whereas the main AD-associated targets were MAOB, ESR1, BACE1, AChE, CDK5, GSK3β, and PTGS2. A total of 18 gene pathways were identified to be associated, with the pathways related to AD among the topmost enriched. Molecular docking analysis against top AD targets resulted in suitable binding interactions at the active site of target proteins. Further, the protective role of IP in AD was confirmed with cell-line studies on PC-12, in situ AChE inhibition, and antioxidant assays.

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Abbreviations

AD:

Alzheimer’s disease

LC-MS:

Liquid chromatography hyphenated to mass spectrophotometer

ARIA:

Amyloid-related imaging abnormalities

IP:

Indian propolis

HAR_PRP:

Haryana propolis

PPI:

Protein–protein interaction

KEGG:

Kyoto encyclopedia of genes and genomes

DAVID:

Database for annotation visualization and integrated discovery

Aβ:

Amyloid beta

PC-12 cell line:

Rat pheochromocytoma cell line

AChE:

Acetylcholinesterase

BBB:

Blood–brain barrier

BA:

Bioavailability score

FDR:

False discovery rate

PDB:

Protein data bank

IC50 :

half maximal inhibitory concentration

RMSD:

Root mean square deviation

TIC:

Total ion chromatogram

GO:

Gene ontology

BP:

Biological process

CC:

Cellular component

MF:

Molecular function

APP:

Amyloid precursor protein

BACE1:

Beta-secretase 1

GSK3β:

Glycogen synthase kinase-3 beta

CDK5:

Cyclin-dependent kinase 5

PTGS2:

Prostaglandin endoperoxide synthase 2

AA:

Ascorbic acid

mgEAA/g:

Milli gram equivalent of ascorbic acid/gram

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Acknowledgements

The authors are grateful to the All-India Council for Technical Education (AICTE) for providing financial assistance to Sandeep Sankaran through the AICTE Doctoral Fellowship Scheme (ADF). The authors would like to acknowledge Dr Sangram Patil, Mr Amol Kadam, and the Centre of Food Testing Laboratories, Pune for their support in LC-MS/MS work. The authors are thankful to Dr Amol Jadhav, and Nirav BioSolutions, Pune for their help in carrying out the cell viability assay.

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This research did not receive any specific grant from funding agencies for carrying out this work.

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Authors and Affiliations

  1. Department of Quality Assurance Techniques, Poona College of Pharmacy, Bharati Vidyapeeth (Deemed to be) University, Pune, Maharashtra, 411038, India

    Sandeep Sankaran

  2. Department of Pharmaceutical Chemistry, Poona College of Pharmacy, Bharati Vidyapeeth (Deemed to be) University, Pune, Maharashtra, 411038, India

    Rahul Dubey, Ashwini Kshirsagar & Sathiyanarayanan Lohidasan

  3. Department of Pharmaceutical Chemistry, Bombay College of Pharmacy, Mumbai, Maharashtra, 400098, India

    Anish Gomatam

  4. Department of Pharmaceutics, Poona College of Pharmacy, Bharati Vidyapeeth (Deemed to be) University, Pune, Maharashtra, 411038, India

    Rishikesh Chakor

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Contributions

S.S: performed LC-MS/MS, network pharmacology, molecular docking, in-vitro experiments, and wrote the manuscript. R.D: helped in LC-MS/MS and in-vitro experiments. A.G: assisted in molecular docking studies, Writing - review. RC: helped in network pharmacology analysis. A.K: helped in in-vitro experiments. S.L: conceptualized and designed the work, provided reagents and facilities, Supervision, Writing - review and editing.

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Correspondence to Sathiyanarayanan Lohidasan.

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Sankaran, S., Dubey, R., Gomatam, A. et al. Deciphering the multi-functional role of Indian propolis for the management of Alzheimer’s disease by integrating LC–MS/MS, network pharmacology, molecular docking, and in-vitro studies. Mol Divers (2024). https://doi.org/10.1007/s11030-024-10818-8

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