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Review
. 2023 Dec 4;16(12):1684.
doi: 10.3390/ph16121684.

A Critical Interpretive Synthesis of the Role of Arecoline in Oral Carcinogenesis: Is the Local Cholinergic Axis a Missing Link in Disease Pathophysiology?

Affiliations
Review

A Critical Interpretive Synthesis of the Role of Arecoline in Oral Carcinogenesis: Is the Local Cholinergic Axis a Missing Link in Disease Pathophysiology?

Hakan Gocol et al. Pharmaceuticals (Basel). .

Abstract

Arecoline is the primary active carcinogen found in areca nut and has been implicated in the pathogenesis of oral squamous cell carcinoma (OSCC) and oral submucous fibrosis (OSF). For this study, we conducted a stepwise review process by combining iterative scoping reviews with a post hoc search, with the aim of identifying the specific mechanisms by which arecoline initiates and promotes oral carcinogenesis. Our initial search allowed us to define the current trends and patterns in the pathophysiology of arecoline-induced OSF and OSCC, which include the induction of cell proliferation, facilitation of invasion, adhesion, and migration, increased collagen deposition and fibrosis, imbalance in immune and inflammatory mechanisms, and genotoxicity. Key molecular pathways comprise the activation of NOTCH1, MYC, PRDX2, WNT, CYR61, EGFR/Pl3K, DDR1 signaling, and cytokine upregulation. Despite providing a comprehensive overview of potential pathogenic mechanisms of OSF, the involvement of molecules functioning as areca alkaloid receptors, namely, the muscarinic and nicotinic acetylcholine receptors (AChRs), was not elucidated with this approach. Accordingly, our search strategy was refined to reflect these evidence gaps. The results of the second round of reviews with the post hoc search highlighted that arecoline binds preferentially to muscarinic AChRs, which have been implicated in cancer. Consistently, AChRs activate the signaling pathways that partially overlap with those described in the context of arecoline-induced carcinogenesis. In summary, we used a theory-driven interpretive review methodology to inform, extend, and supplement the conventional systematic literature assessment workflow. On the one hand, the results of this critical interpretive synthesis highlighted the prevailing trends and enabled the consolidation of data pertaining to the molecular mechanisms involved in arecoline-induced carcinogenesis, and, on the other, brought up knowledge gaps related to the role of the local cholinergic axis in oral carcinogenesis, thus suggesting areas for further investigation.

Keywords: acetylcholine receptors; arecoline; mouth neoplasms; nicotine; oral cancer; oral submucous fibrosis.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
PRISMA flow diagram demonstrating the selection process for the initial scoping review. PRISMA: preferred reporting items for systematic reviews and meta-analysis.
Figure 2
Figure 2
Putative pathways involving the receptor-mediated signaling of arecoline. Arecoline binds preferentially to muscarinic acetylcholine receptors (mAChR) but can also serve as a partial agonist of nicotinic receptors (nAChR). Two key molecular pathways involve EGFR and integrins. mAChR activates EGFR signaling via a so-called “triple-membrane-passing” pathway, whereby metalloproteinases cleave and activate EGF-like ligands, which, in turn, bind to EGFR and trigger downstream kinase signaling, including the Ras/Raf/MEK/ERK pathway. MAPK signaling can also be activated via canonical second messenger-mediated signals, as well as via nAChR. The two receptors also work synergistically to promote survival and inhibit apoptosis via PI3K/Akt and p21, respectively. Together, these pathways promote the expression of proliferation and survival genes, as well as migration/invasion and fibrosis/senescence via integrins and TGF-beta signaling, respectively (brown arrow). See Abbreviations part for the abbreviations and acronyms.

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This research received no external funding.