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Induction of apoptosis in A431 cells via ROS generation and p53-mediated pathway by chloroform fraction of Argemone mexicana (Pepaveraceae)

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Abstract

Argemone mexicana(Pepaveraceae) is an important medicinal plant commonly known as ‘maxican prickly poppy’ and is traditionally used to treat skin diseases. In the present study, the extract/fractions of aerial parts of A. mexicana after carrying out the organoleptic characteristics were sequentially extracted with the solvents of increasing polarities. Total fractions were examined for their radical scavenging activities in DPPH and DNA nicking assays. Among all, maximum antioxidant activity was shown by chloroform fraction (AmC) in DPPH assay with IC50 of 26.12 μg/ml, and DNA nicking assay showed 80.91% protective potential. The AmC fraction was analyzed for its antibacterial, cytotoxic potential, cell cycle analysis, mitochondrial membrane potential (MMP) and accumulation of reactive oxygen species (ROS) using A431 cell line. The AmC fraction exhibited remarkable antibacterial activity against bacterial strains in the order Klebsiella pneumoniae> Bacillussubtilis> Salmonella typhi> Staphylococcus epidermidis. The cytotoxic potential of the AmC fraction was analyzed in skin epidermoid carcinoma (A431) cells, osteosarcoma (MG-63) and cervical (HeLa) cell lines with a GI50 value of 47.04 μg/ml, 91.46 μg/ml and 102.90 μg/ml, respectively. The AmC fraction was extended further to explore its role in cell death using A431 cell line. Phase contrast and scanning electron microscopic studies on A431 cells exhibited all the characteristics indicative of apoptosis, viz., viability loss, cell shrinkage, cell rounding-off, DNA fragmentation and formation of apoptotic bodies. Flow cytometric analysis revealed enhanced ROS level, decreased MMP and arrest cell cycle at the G0/G1 phase further strengthened cell death by apoptosis. Increased expressions of apoptotic markers (p53, PUMA, cyt c, Fas and Apaf-1) were confirmed by RT-qPCR analysis. Furthermore, the AmC fraction was subjected to ultra-high-performance liquid chromatography, which revealed the presence of different polyphenols in the order: caffeic acid> epicatechin> kaempferol> chlorogenic acid> gallic acid> catechin> ellagic acid >umbeliferone> quercetin> coumaric acid. A critical analysis of results revealed that the AmC fraction induced cell death in epidermoid carcinoma cells via ROS and p53-mediated apoptotic pathway which may be ascribed to the presence of polyphenols in it.

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Abbreviations

A431:

Skin epidermoid carcinoma cells

AO/EtBr:

Acridine orange/ethidium bromide

Apaf-1:

Apoptotic protease activating factor 1

Cyt c:

Cytochrome c

DCFH-DA:

2,7-Dichloroflourescein diacetate

DMEM:

Dulbecco’s modified Eagle’s medium

DPPH:

2,2-Diphenyl-1-picrylhydrazyl

EA:

Early apoptosis

ELISA:

Enzyme-linked immunosorbent assay

FBS:

Fetal bovine serum

GAE:

Gallic acid equivalent

HeLa:

Human cervical cancer

L:

Live

L929:

Human fibroblast

LA:

Late apoptosis

MEM:

Minimal essential media

MG-63:

Human osteosarcoma

MTT:

3-(4,5-Dimethylthiazol-2-yl)-2,5-diphenylte-trazolium bromide

NCCS:

National Centre for Cell Science

PI:

Propidium iodide

MMP:

Mitochondrial membrane potential

Rh123:

Rhodamine 123

ROS:

Reactive oxygen species

RT-qPCR:

Quantitative real-timepolymerase chain reaction

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Acknowledgements

We like to acknowledge DST-PURSE, DST-FIST programmer, UGC, New Delhi for the instrumentation facility provided under UGC-DRS V, CPEPA and UPE program and Centre of Emerging Life Sciences, Guru Nanak Dev University, Amritsar (India) for providing the required support and facilities.

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The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation, to any qualified researcher.

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The authors are thankful to the Council of Scientific and Industrial Research (CSIR), New Delhi India for providing financial assistance.

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Authors and Affiliations

  1. Department of Botanical & Environmental Sciences, Guru Nanak Dev University, Amritsar, Punjab, India

    Shivani Attri, Prabhjot Kaur, Davinder Singh, Harneetpal Kaur, Farhana Rashid, Avinash Kumar & Saroj Arora

  2. Department of Pharmaceutical Sciences, Guru Nanak Dev University, 143005, Amritsar, Punjab, India

    Balbir Singh & Neena Bedi

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  1. Shivani Attri
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SA: conceptualization, validation, methodology, formal analysis, writing—original draft, investigation, software; PK: conceptualization, investigation; DS: conceptualization; HK: investigation; FR: investigation, conceptualization; AK: conceptualization, formal analysis; BS: supervision, validation; NB: supervision, methodology; SA: supervision, validation, methodology, conceptualization, writing—original draft. All authors have read and approved the published version of the manuscript.

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Correspondence to Saroj Arora.

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Attri, S., Kaur, P., Singh, D. et al. Induction of apoptosis in A431 cells via ROS generation and p53-mediated pathway by chloroform fraction of Argemone mexicana (Pepaveraceae). Environ Sci Pollut Res 29, 17189–17208 (2022). https://doi.org/10.1007/s11356-021-16696-z

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