Skip to main content
Top
Published in: European Journal of Medical Research 1/2023

Open Access 01-12-2023 | Leukoplakia | Review

The potential roles of cigarette smoke-induced extracellular vesicles in oral leukoplakia

Authors: Qiao Peng, Ning Duan, Xiang Wang, Wenmei Wang

Published in: European Journal of Medical Research | Issue 1/2023

Login to get access

Abstract

Background

The onset of oral leukoplakia (OLK), the most common oral lesion with a high risk of malignant transformation, is closely associated with the exposure of cigarette smoke. Cigarette smoke is a complicated mixture of more than 4500 different chemicals including various oxidants and free radical, which contributes to the onset of immune and inflammatory response or even carcinogenesis. Recent studies have proved that the exposure of cigarette smoke leads to the onset and aggravation of many diseases via significantly changed the production and components of extracellular vesicles. The extracellular vesicles are membrane-enclosed nanosized particles secreted by diverse cells and involved in cell–cell communication because of their ability to deliver a number of bioactive molecules including proteins, lipids, DNAs and RNAs. Getting insight into the mechanisms of extracellular vesicles in regulating OLK upon cigarette smoke stimulation contributes to unravel the pathophysiology of OLK in-depth. However, evidence done on the role of extracellular vesicles in cigarette smoke-induced OLK is still in its infancy.

Materials and methods

Relevant literatures on cigarette smoke, oral leukoplakia and extracellular vesicles were searched in PubMed database.

Conclusions

In this review, we summarize the recent findings about the function of extracellular vesicles in the pathogenesis of cigarette smoke-induced diseases, and to infer their potential utilizations as diagnostic biomarkers, prognostic evaluation, and therapeutic targets of OLK in the future.
Literature
1.
go back to reference Lugg ST, Scott A, Parekh D, Naidu B, Thickett DR. Cigarette smoke exposure and alveolar macrophages: mechanisms for lung disease. Thorax. 2022;77:94–101.PubMedCrossRef Lugg ST, Scott A, Parekh D, Naidu B, Thickett DR. Cigarette smoke exposure and alveolar macrophages: mechanisms for lung disease. Thorax. 2022;77:94–101.PubMedCrossRef
2.
go back to reference Prieux R, Eeman M, Rothen-Rutishauser B, Valacchi G. Mimicking cigarette smoke exposure to assess cutaneous toxicity. Toxicol In Vitro. 2020;62: 104664.PubMedCrossRef Prieux R, Eeman M, Rothen-Rutishauser B, Valacchi G. Mimicking cigarette smoke exposure to assess cutaneous toxicity. Toxicol In Vitro. 2020;62: 104664.PubMedCrossRef
3.
go back to reference Rezk-Hanna M, Benowitz NL. Cardiovascular effects of hookah smoking: potential implications for cardiovascular risk. Nicotine Tob Res. 2019;21:1151–61.PubMedCrossRef Rezk-Hanna M, Benowitz NL. Cardiovascular effects of hookah smoking: potential implications for cardiovascular risk. Nicotine Tob Res. 2019;21:1151–61.PubMedCrossRef
4.
go back to reference Mravec B, Tibensky M, Horvathova L, Babal P. E-cigarettes and cancer risk. Cancer Prev Res. 2020;13:137–44.CrossRef Mravec B, Tibensky M, Horvathova L, Babal P. E-cigarettes and cancer risk. Cancer Prev Res. 2020;13:137–44.CrossRef
5.
go back to reference Rohde P, Kahler CW, Lewinsohn PM, Brown RA. Psychiatric disorders, familial factors, and cigarette smoking: II. Associations with progression to daily smoking. Nicotine Tob Res. 2004;6:119–32.PubMedCrossRef Rohde P, Kahler CW, Lewinsohn PM, Brown RA. Psychiatric disorders, familial factors, and cigarette smoking: II. Associations with progression to daily smoking. Nicotine Tob Res. 2004;6:119–32.PubMedCrossRef
6.
go back to reference Kerr DMI, Brooksbank KJM, Taylor RG, Pinel K, Rios FJ, Touyz RM, et al. Acute effects of electronic and tobacco cigarettes on vascular and respiratory function in healthy volunteers: a cross-over study. J Hypertens. 2019;37:154–66.PubMedCrossRef Kerr DMI, Brooksbank KJM, Taylor RG, Pinel K, Rios FJ, Touyz RM, et al. Acute effects of electronic and tobacco cigarettes on vascular and respiratory function in healthy volunteers: a cross-over study. J Hypertens. 2019;37:154–66.PubMedCrossRef
7.
go back to reference Yang SR, Wright J, Bauter M, Seweryniak K, Kode A, Rahman I. Sirtuin regulates cigarette smoke-induced proinflammatory mediator release via RelA/p65 NF-kappaB in macrophages in vitro and in rat lungs in vivo: implications for chronic inflammation and aging. Am J Physiol Lung Cell Mol Physiol. 2007;292:L567–76.PubMedCrossRef Yang SR, Wright J, Bauter M, Seweryniak K, Kode A, Rahman I. Sirtuin regulates cigarette smoke-induced proinflammatory mediator release via RelA/p65 NF-kappaB in macrophages in vitro and in rat lungs in vivo: implications for chronic inflammation and aging. Am J Physiol Lung Cell Mol Physiol. 2007;292:L567–76.PubMedCrossRef
8.
go back to reference Mossina A, Lukas C, Merl-Pham J, Uhl FE, Mutze K, Schamberger A, et al. Cigarette smoke alters the secretome of lung epithelial cells. Proteomics. 2017;17:1600243.CrossRef Mossina A, Lukas C, Merl-Pham J, Uhl FE, Mutze K, Schamberger A, et al. Cigarette smoke alters the secretome of lung epithelial cells. Proteomics. 2017;17:1600243.CrossRef
10.
go back to reference Sepand MR, Maghsoudi AS, Shadboorestan A, Mirnia K, Aghsami M, Raoufi M. Cigarette smoke-induced toxicity consequences of intracellular iron dysregulation and ferroptosis. Life Sci. 2021;281: 119799.PubMedCrossRef Sepand MR, Maghsoudi AS, Shadboorestan A, Mirnia K, Aghsami M, Raoufi M. Cigarette smoke-induced toxicity consequences of intracellular iron dysregulation and ferroptosis. Life Sci. 2021;281: 119799.PubMedCrossRef
11.
go back to reference Kono Y, Colley T, To M, Papaioannou AI, Mercado N, Baker JR, et al. Cigarette smoke-induced impairment of autophagy in macrophages increases galectin-8 and inflammation. Sci Rep. 2021;11:335.PubMedPubMedCentralCrossRef Kono Y, Colley T, To M, Papaioannou AI, Mercado N, Baker JR, et al. Cigarette smoke-induced impairment of autophagy in macrophages increases galectin-8 and inflammation. Sci Rep. 2021;11:335.PubMedPubMedCentralCrossRef
12.
go back to reference Asthana S, Labani S, Kailash U, Sinha DN, Mehrotra R. Association of smokeless tobacco use and oral cancer: a systematic global review and meta-analysis. Nicotine Tob Res. 2019;21:1162–71.PubMedCrossRef Asthana S, Labani S, Kailash U, Sinha DN, Mehrotra R. Association of smokeless tobacco use and oral cancer: a systematic global review and meta-analysis. Nicotine Tob Res. 2019;21:1162–71.PubMedCrossRef
13.
go back to reference Aredo JV, Luo SJ, Gardner RM, Sanyal N, Choi E, Hickey TP, et al. Tobacco smoking and risk of second primary lung cancer. J Thorac Oncol. 2021;16:968–79.PubMedPubMedCentralCrossRef Aredo JV, Luo SJ, Gardner RM, Sanyal N, Choi E, Hickey TP, et al. Tobacco smoking and risk of second primary lung cancer. J Thorac Oncol. 2021;16:968–79.PubMedPubMedCentralCrossRef
14.
16.
go back to reference Olsson P, Bodewes ILA, Nilsson AM, Turesson C, Jacobsson LTH, Theander E, et al. Associations of cigarette smoking with disease phenotype and type I interferon expression in primary Sjogren’s syndrome. Rheumatol Int. 2019;39:1575–84.PubMedCrossRef Olsson P, Bodewes ILA, Nilsson AM, Turesson C, Jacobsson LTH, Theander E, et al. Associations of cigarette smoking with disease phenotype and type I interferon expression in primary Sjogren’s syndrome. Rheumatol Int. 2019;39:1575–84.PubMedCrossRef
17.
go back to reference Leite FRM, Nascimento GG, Scheutz F, Lopez R. Effect of smoking on periodontitis: a systematic review and meta-regression. Am J Prev Med. 2018;54:831–41.PubMedCrossRef Leite FRM, Nascimento GG, Scheutz F, Lopez R. Effect of smoking on periodontitis: a systematic review and meta-regression. Am J Prev Med. 2018;54:831–41.PubMedCrossRef
18.
19.
go back to reference Warnakulasuriya S. Oral potentially malignant disorders: a comprehensive review on clinical aspects and management. Oral Oncol. 2020;102: 104550.PubMedCrossRef Warnakulasuriya S. Oral potentially malignant disorders: a comprehensive review on clinical aspects and management. Oral Oncol. 2020;102: 104550.PubMedCrossRef
20.
go back to reference Carrard VC, van der Waal I. A clinical diagnosis of oral leukoplakia; a guide for dentists. Med Oral Patol Oral Cir Bucal. 2018;23:e59–64.PubMed Carrard VC, van der Waal I. A clinical diagnosis of oral leukoplakia; a guide for dentists. Med Oral Patol Oral Cir Bucal. 2018;23:e59–64.PubMed
21.
go back to reference Lodi G, Franchini R, Warnakulasuriya S, Varoni EM, Sardella A, Kerr AR, et al. Interventions for treating oral leukoplakia to prevent oral cancer. Cochrane Database Syst Rev. 2016;7:Cd001829.PubMed Lodi G, Franchini R, Warnakulasuriya S, Varoni EM, Sardella A, Kerr AR, et al. Interventions for treating oral leukoplakia to prevent oral cancer. Cochrane Database Syst Rev. 2016;7:Cd001829.PubMed
22.
23.
go back to reference Aguirre-Urizar JM, Lafuente-Ibáñez de Mendoza I, Warnakulasuriya S. Malignant transformation of oral leukoplakia: systematic review and meta-analysis of the last 5 years. Oral Dis. 2021;27:1881–95.PubMedCrossRef Aguirre-Urizar JM, Lafuente-Ibáñez de Mendoza I, Warnakulasuriya S. Malignant transformation of oral leukoplakia: systematic review and meta-analysis of the last 5 years. Oral Dis. 2021;27:1881–95.PubMedCrossRef
24.
go back to reference Kumar S, Muniyandi M. Tobacco use and oral leukoplakia: cross-sectional study among the Gond tribe in Madhya Pradesh. Asian Pac J Cancer Prev. 2015;16:1515–8.PubMedCrossRef Kumar S, Muniyandi M. Tobacco use and oral leukoplakia: cross-sectional study among the Gond tribe in Madhya Pradesh. Asian Pac J Cancer Prev. 2015;16:1515–8.PubMedCrossRef
25.
26.
go back to reference Dietrich T, Reichart PA, Scheifele C. Clinical risk factors of oral leukoplakia in a representative sample of the US population. Oral Oncol. 2004;40:158–63.PubMedCrossRef Dietrich T, Reichart PA, Scheifele C. Clinical risk factors of oral leukoplakia in a representative sample of the US population. Oral Oncol. 2004;40:158–63.PubMedCrossRef
27.
go back to reference Ye P, Chen W, Huang F, Liu Q, Zhu YN, Wang X, et al. Smoking increases oral mucosa susceptibility to Candida albicans infection via the Nrf2 pathway: in vitro and animal studies. J Cell Mol Med. 2021;25:7948–60.PubMedPubMedCentralCrossRef Ye P, Chen W, Huang F, Liu Q, Zhu YN, Wang X, et al. Smoking increases oral mucosa susceptibility to Candida albicans infection via the Nrf2 pathway: in vitro and animal studies. J Cell Mol Med. 2021;25:7948–60.PubMedPubMedCentralCrossRef
28.
go back to reference Sekar D. Extracellular vesicles are involved in oxidative stress and mitochondrial homeostasis in pulmonary arterial hypertension. Hypertens Res. 2021;44:1028–9.PubMedCrossRef Sekar D. Extracellular vesicles are involved in oxidative stress and mitochondrial homeostasis in pulmonary arterial hypertension. Hypertens Res. 2021;44:1028–9.PubMedCrossRef
29.
go back to reference Chiaradia E, Tancini B, Emiliani C, Delo F, Pellegrino RM, Tognoloni A, et al. Extracellular vesicles under oxidative stress conditions: biological properties and physiological roles. Cells. 2021;10:1763.PubMedPubMedCentralCrossRef Chiaradia E, Tancini B, Emiliani C, Delo F, Pellegrino RM, Tognoloni A, et al. Extracellular vesicles under oxidative stress conditions: biological properties and physiological roles. Cells. 2021;10:1763.PubMedPubMedCentralCrossRef
30.
32.
go back to reference Cocucci E, Meldolesi J. Ectosomes and exosomes: shedding the confusion between extracellular vesicles. Trends Cell Biol. 2015;25:364–72.PubMedCrossRef Cocucci E, Meldolesi J. Ectosomes and exosomes: shedding the confusion between extracellular vesicles. Trends Cell Biol. 2015;25:364–72.PubMedCrossRef
34.
go back to reference Zhu L, Sun HT, Wang S, Huang SL, Zheng Y, Wang CQ, et al. Isolation and characterization of exosomes for cancer research. J Hematol Oncol. 2020;13:152.PubMedPubMedCentralCrossRef Zhu L, Sun HT, Wang S, Huang SL, Zheng Y, Wang CQ, et al. Isolation and characterization of exosomes for cancer research. J Hematol Oncol. 2020;13:152.PubMedPubMedCentralCrossRef
35.
go back to reference Pitt JM, Kroemer G, Zitvogel L. Extracellular vesicles: masters of intercellular communication and potential clinical interventions. J Clin Invest. 2016;126:1139–43.PubMedPubMedCentralCrossRef Pitt JM, Kroemer G, Zitvogel L. Extracellular vesicles: masters of intercellular communication and potential clinical interventions. J Clin Invest. 2016;126:1139–43.PubMedPubMedCentralCrossRef
36.
go back to reference O’Brien K, Breyne K, Ughetto S, Laurent LC, Breakefield XO. RNA delivery by extracellular vesicles in mammalian cells and its applications. Nat Rev Mol Cell Biol. 2020;21:585–606.PubMedPubMedCentralCrossRef O’Brien K, Breyne K, Ughetto S, Laurent LC, Breakefield XO. RNA delivery by extracellular vesicles in mammalian cells and its applications. Nat Rev Mol Cell Biol. 2020;21:585–606.PubMedPubMedCentralCrossRef
37.
go back to reference Macias M, Alegre E, Diaz-Lagares A, Patino A, Perez-Gracia JL, Sanmamed M, et al. Liquid biopsy: from basic research to clinical practice. Adv Clin Chem. 2018;83:73–119.PubMedCrossRef Macias M, Alegre E, Diaz-Lagares A, Patino A, Perez-Gracia JL, Sanmamed M, et al. Liquid biopsy: from basic research to clinical practice. Adv Clin Chem. 2018;83:73–119.PubMedCrossRef
38.
go back to reference Yu W, Hurley J, Roberts D, Chakrabortty SK, Enderle D, Noerholm M, et al. Exosome-based liquid biopsies in cancer: opportunities and challenges. Ann Oncol. 2021;32:466–77.PubMedCrossRef Yu W, Hurley J, Roberts D, Chakrabortty SK, Enderle D, Noerholm M, et al. Exosome-based liquid biopsies in cancer: opportunities and challenges. Ann Oncol. 2021;32:466–77.PubMedCrossRef
40.
41.
go back to reference Skog J, Wurdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 2008;10:1470–6.PubMedPubMedCentralCrossRef Skog J, Wurdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 2008;10:1470–6.PubMedPubMedCentralCrossRef
42.
go back to reference Zhou B, Xu K, Zheng X, Chen T, Wang J, Song Y, et al. Application of exosomes as liquid biopsy in clinical diagnosis. Signal Transduct Target Ther. 2020;5:144.PubMedPubMedCentralCrossRef Zhou B, Xu K, Zheng X, Chen T, Wang J, Song Y, et al. Application of exosomes as liquid biopsy in clinical diagnosis. Signal Transduct Target Ther. 2020;5:144.PubMedPubMedCentralCrossRef
43.
go back to reference Ma YS, Yang XL, Xin R, Liu JB, Fu D. Power and promise of exosomes as clinical biomarkers and therapeutic vectors for liquid biopsy and cancer control. Biochim et Biophys Acta Rev Cancer. 2021;1875: 188497.CrossRef Ma YS, Yang XL, Xin R, Liu JB, Fu D. Power and promise of exosomes as clinical biomarkers and therapeutic vectors for liquid biopsy and cancer control. Biochim et Biophys Acta Rev Cancer. 2021;1875: 188497.CrossRef
44.
go back to reference Tkach M, Thery C. Communication by extracellular vesicles: where we are and where we need to go. Cell. 2016;164:1226–32.PubMedCrossRef Tkach M, Thery C. Communication by extracellular vesicles: where we are and where we need to go. Cell. 2016;164:1226–32.PubMedCrossRef
45.
go back to reference Benedikter BJ, Weseler AR, Wouters EFM, Savelkoul PHM, Rohde GGU, Stassen FRM. Redox-dependent thiol modifications: implications for the release of extracellular vesicles. Cell Mol Life Sci. 2018;75:2321–37.PubMedPubMedCentralCrossRef Benedikter BJ, Weseler AR, Wouters EFM, Savelkoul PHM, Rohde GGU, Stassen FRM. Redox-dependent thiol modifications: implications for the release of extracellular vesicles. Cell Mol Life Sci. 2018;75:2321–37.PubMedPubMedCentralCrossRef
46.
go back to reference Benedikter BJ, Koenen RR. Vaping, vapor, vesicles! Electronic cigarettes provoke vascular extracellular vesicle release in healthy volunteers. Atherosclerosis. 2020;301:79–81.PubMedCrossRef Benedikter BJ, Koenen RR. Vaping, vapor, vesicles! Electronic cigarettes provoke vascular extracellular vesicle release in healthy volunteers. Atherosclerosis. 2020;301:79–81.PubMedCrossRef
47.
go back to reference Serban KA, Rezania S, Petrusca DN, Poirier C, Cao D, Justice MJ, et al. Structural and functional characterization of endothelial microparticles released by cigarette smoke. Sci Rep. 2016;6:31596.PubMedPubMedCentralCrossRef Serban KA, Rezania S, Petrusca DN, Poirier C, Cao D, Justice MJ, et al. Structural and functional characterization of endothelial microparticles released by cigarette smoke. Sci Rep. 2016;6:31596.PubMedPubMedCentralCrossRef
48.
go back to reference Benedikter BJ, Volgers C, van Eijck PH, Wouters EFM, Savelkoul PHM, Reynaert NL, et al. Cigarette smoke extract induced exosome release is mediated by depletion of exofacial thiols and can be inhibited by thiol-antioxidants. Free Radic Biol Med. 2017;108:334–44.PubMedCrossRef Benedikter BJ, Volgers C, van Eijck PH, Wouters EFM, Savelkoul PHM, Reynaert NL, et al. Cigarette smoke extract induced exosome release is mediated by depletion of exofacial thiols and can be inhibited by thiol-antioxidants. Free Radic Biol Med. 2017;108:334–44.PubMedCrossRef
49.
go back to reference Benedikter BJ, Bouwman FG, Heinzmann ACA, Vajen T, Mariman EC, Wouters EFM, et al. Proteomic analysis reveals procoagulant properties of cigarette smoke-induced extracellular vesicles. J Extracell Vesicles. 2019;8:1585163.PubMedPubMedCentralCrossRef Benedikter BJ, Bouwman FG, Heinzmann ACA, Vajen T, Mariman EC, Wouters EFM, et al. Proteomic analysis reveals procoagulant properties of cigarette smoke-induced extracellular vesicles. J Extracell Vesicles. 2019;8:1585163.PubMedPubMedCentralCrossRef
50.
go back to reference Baek R, Varming K, Jorgensen MM. Does smoking, age or gender affect the protein phenotype of extracellular vesicles in plasma? Transfus Apher Sci. 2016;55:44–52.PubMedCrossRef Baek R, Varming K, Jorgensen MM. Does smoking, age or gender affect the protein phenotype of extracellular vesicles in plasma? Transfus Apher Sci. 2016;55:44–52.PubMedCrossRef
51.
go back to reference Mobarrez F, Antoniewicz L, Bosson JA, Kuhl J, Pisetsky DS, Lundback M. The effects of smoking on levels of endothelial progenitor cells and microparticles in the blood of healthy volunteers. PLoS ONE. 2014;9: e90314.PubMedPubMedCentralCrossRef Mobarrez F, Antoniewicz L, Bosson JA, Kuhl J, Pisetsky DS, Lundback M. The effects of smoking on levels of endothelial progenitor cells and microparticles in the blood of healthy volunteers. PLoS ONE. 2014;9: e90314.PubMedPubMedCentralCrossRef
52.
go back to reference Feller D, Kun J, Ruzsics I, Rapp J, Sarosi V, Kvell K, et al. Cigarette smoke-induced pulmonary inflammation becomes systemic by circulating extracellular vesicles containing wnt5a and inflammatory cytokines. Front Immunol. 2018;9:1724.PubMedPubMedCentralCrossRef Feller D, Kun J, Ruzsics I, Rapp J, Sarosi V, Kvell K, et al. Cigarette smoke-induced pulmonary inflammation becomes systemic by circulating extracellular vesicles containing wnt5a and inflammatory cytokines. Front Immunol. 2018;9:1724.PubMedPubMedCentralCrossRef
53.
go back to reference Tanaka T, Narazaki M, Masuda K, Kishimoto T. Regulation of IL-6 in immunity and diseases. Adv Exp Med Biol. 2016;941:79–88.PubMedCrossRef Tanaka T, Narazaki M, Masuda K, Kishimoto T. Regulation of IL-6 in immunity and diseases. Adv Exp Med Biol. 2016;941:79–88.PubMedCrossRef
54.
go back to reference Sharma M, Bairy I, Pai K, Satyamoorthy K, Prasad S, Berkovitz B, et al. Salivary IL-6 levels in oral leukoplakia with dysplasia and its clinical relevance to tobacco habits and periodontitis. Clin Oral Investig. 2011;15:705–14.PubMedCrossRef Sharma M, Bairy I, Pai K, Satyamoorthy K, Prasad S, Berkovitz B, et al. Salivary IL-6 levels in oral leukoplakia with dysplasia and its clinical relevance to tobacco habits and periodontitis. Clin Oral Investig. 2011;15:705–14.PubMedCrossRef
55.
go back to reference Rhodus NL, Ho V, Miller CS, Myers S, Ondrey F. NF-kappaB dependent cytokine levels in saliva of patients with oral preneoplastic lesions and oral squamous cell carcinoma. Cancer Detect Prev. 2005;29:42–5.PubMedCrossRef Rhodus NL, Ho V, Miller CS, Myers S, Ondrey F. NF-kappaB dependent cytokine levels in saliva of patients with oral preneoplastic lesions and oral squamous cell carcinoma. Cancer Detect Prev. 2005;29:42–5.PubMedCrossRef
56.
go back to reference Kumar A, Sinha N, Haque S, Kodidela S, Wang T, Martinez AG, et al. Nicotine self-administration with menthol and audiovisual cue facilitates differential packaging of CYP2A6 and cytokines/chemokines in rat plasma extracellular vesicles. Sci Rep. 2021;11:17393.PubMedPubMedCentralCrossRef Kumar A, Sinha N, Haque S, Kodidela S, Wang T, Martinez AG, et al. Nicotine self-administration with menthol and audiovisual cue facilitates differential packaging of CYP2A6 and cytokines/chemokines in rat plasma extracellular vesicles. Sci Rep. 2021;11:17393.PubMedPubMedCentralCrossRef
57.
go back to reference Charrin S, le Naour F, Silvie O, Milhiet PE, Boucheix C, Rubinstein E. Lateral organization of membrane proteins: tetraspanins spin their web. Biochem J. 2009;420:133–54.PubMedCrossRef Charrin S, le Naour F, Silvie O, Milhiet PE, Boucheix C, Rubinstein E. Lateral organization of membrane proteins: tetraspanins spin their web. Biochem J. 2009;420:133–54.PubMedCrossRef
60.
go back to reference Singh KP, Maremanda KP, Li D, Rahman I. Exosomal microRNAs are novel circulating biomarkers in cigarette, waterpipe smokers, E-cigarette users and dual smokers. BMC Med Genom. 2020;13:128.CrossRef Singh KP, Maremanda KP, Li D, Rahman I. Exosomal microRNAs are novel circulating biomarkers in cigarette, waterpipe smokers, E-cigarette users and dual smokers. BMC Med Genom. 2020;13:128.CrossRef
61.
go back to reference Sundar IK, Li D, Rahman I. Small RNA-sequence analysis of plasma-derived extracellular vesicle miRNAs in smokers and patients with chronic obstructive pulmonary disease as circulating biomarkers. J Extracell Vesicles. 2019;8:1684816.PubMedPubMedCentralCrossRef Sundar IK, Li D, Rahman I. Small RNA-sequence analysis of plasma-derived extracellular vesicle miRNAs in smokers and patients with chronic obstructive pulmonary disease as circulating biomarkers. J Extracell Vesicles. 2019;8:1684816.PubMedPubMedCentralCrossRef
62.
go back to reference Xu H, Ling M, Xue J, Dai X, Sun Q, Chen C, et al. Exosomal microRNA-21 derived from bronchial epithelial cells is involved in aberrant epithelium-fibroblast cross-talk in COPD induced by cigarette smoking. Theranostics. 2018;8:5419–33.PubMedPubMedCentralCrossRef Xu H, Ling M, Xue J, Dai X, Sun Q, Chen C, et al. Exosomal microRNA-21 derived from bronchial epithelial cells is involved in aberrant epithelium-fibroblast cross-talk in COPD induced by cigarette smoking. Theranostics. 2018;8:5419–33.PubMedPubMedCentralCrossRef
63.
go back to reference Kaunein N, Ramani RS, Koo K, Moore C, Celentano A, McCullough M, et al. A systematic review of microRNA signatures associated with the progression of leukoplakia with and without epithelial dysplasia. Biomolecules. 2021;11:1879.PubMedPubMedCentralCrossRef Kaunein N, Ramani RS, Koo K, Moore C, Celentano A, McCullough M, et al. A systematic review of microRNA signatures associated with the progression of leukoplakia with and without epithelial dysplasia. Biomolecules. 2021;11:1879.PubMedPubMedCentralCrossRef
64.
go back to reference Chen H, Liu X, Jin Z, Gou C, Liang M, Cui L, et al. A three miRNAs signature for predicting the transformation of oral leukoplakia to oral squamous cell carcinoma. Am J Cancer Res. 2018;8:1403–13.PubMedPubMedCentral Chen H, Liu X, Jin Z, Gou C, Liang M, Cui L, et al. A three miRNAs signature for predicting the transformation of oral leukoplakia to oral squamous cell carcinoma. Am J Cancer Res. 2018;8:1403–13.PubMedPubMedCentral
65.
go back to reference Roy R, Singh R, Chattopadhyay E, Ray A, Sarkar N, Aich R, et al. MicroRNA and target gene expression based clustering of oral cancer, precancer and normal tissues. Gene. 2016;593:58–63.PubMedCrossRef Roy R, Singh R, Chattopadhyay E, Ray A, Sarkar N, Aich R, et al. MicroRNA and target gene expression based clustering of oral cancer, precancer and normal tissues. Gene. 2016;593:58–63.PubMedCrossRef
66.
go back to reference Brito JA, Gomes CC, Guimaraes AL, Campos K, Gomez RS. Relationship between microRNA expression levels and histopathological features of dysplasia in oral leukoplakia. J Oral Pathol Med. 2014;43:211–6.PubMedCrossRef Brito JA, Gomes CC, Guimaraes AL, Campos K, Gomez RS. Relationship between microRNA expression levels and histopathological features of dysplasia in oral leukoplakia. J Oral Pathol Med. 2014;43:211–6.PubMedCrossRef
67.
go back to reference Niklander S, Guerra D, Contreras F, Gonzalez-Arriagada W, Marin C. MicroRNAs and their role in the malignant transformation of oral leukoplakia: a scoping review. Med Oral Patol Oral Cir Bucal. 2022;27:e77–84.PubMedCrossRef Niklander S, Guerra D, Contreras F, Gonzalez-Arriagada W, Marin C. MicroRNAs and their role in the malignant transformation of oral leukoplakia: a scoping review. Med Oral Patol Oral Cir Bucal. 2022;27:e77–84.PubMedCrossRef
68.
go back to reference Grammatikakis I, Lal A. Significance of lncRNA abundance to function. Mamm Genome. 2022;33:271–80.PubMedCrossRef Grammatikakis I, Lal A. Significance of lncRNA abundance to function. Mamm Genome. 2022;33:271–80.PubMedCrossRef
69.
go back to reference Ferrè F, Colantoni A, Helmer-Citterich M. Revealing protein-lncRNA interaction. Brief Bioinform. 2016;17:106–16.PubMedCrossRef Ferrè F, Colantoni A, Helmer-Citterich M. Revealing protein-lncRNA interaction. Brief Bioinform. 2016;17:106–16.PubMedCrossRef
70.
72.
go back to reference Sun Z, Yang S, Zhou Q, Wang G, Song J, Li Z, et al. Emerging role of exosome-derived long non-coding RNAs in tumor microenvironment. Mol Cancer. 2018;17:82.PubMedPubMedCentralCrossRef Sun Z, Yang S, Zhou Q, Wang G, Song J, Li Z, et al. Emerging role of exosome-derived long non-coding RNAs in tumor microenvironment. Mol Cancer. 2018;17:82.PubMedPubMedCentralCrossRef
73.
go back to reference Dai J, Su Y, Zhong S, Cong L, Liu B, Yang J, et al. Exosomes: key players in cancer and potential therapeutic strategy. Signal Transduct Target Ther. 2020;5:145.PubMedPubMedCentralCrossRef Dai J, Su Y, Zhong S, Cong L, Liu B, Yang J, et al. Exosomes: key players in cancer and potential therapeutic strategy. Signal Transduct Target Ther. 2020;5:145.PubMedPubMedCentralCrossRef
74.
go back to reference Kaur G, Singh K, Maremanda KP, Li D, Chand HS, Rahman I. Differential plasma exosomal long non-coding RNAs expression profiles and their emerging role in E-cigarette users, cigarette, waterpipe, and dual smokers. PLoS ONE. 2020;15: e0243065.PubMedPubMedCentralCrossRef Kaur G, Singh K, Maremanda KP, Li D, Chand HS, Rahman I. Differential plasma exosomal long non-coding RNAs expression profiles and their emerging role in E-cigarette users, cigarette, waterpipe, and dual smokers. PLoS ONE. 2020;15: e0243065.PubMedPubMedCentralCrossRef
75.
go back to reference Humpton TJ, Alagesan B, DeNicola GM, Lu D, Yordanov GN, Leonhardt CS, et al. Oncogenic KRAS induces NIX-mediated mitophagy to promote pancreatic cancer. Cancer Discov. 2019;9:1268–87.PubMedPubMedCentralCrossRef Humpton TJ, Alagesan B, DeNicola GM, Lu D, Yordanov GN, Leonhardt CS, et al. Oncogenic KRAS induces NIX-mediated mitophagy to promote pancreatic cancer. Cancer Discov. 2019;9:1268–87.PubMedPubMedCentralCrossRef
76.
go back to reference Li Y, Zheng W, Lu Y, Zheng Y, Pan L, Wu X, et al. BNIP3L/NIX-mediated mitophagy: molecular mechanisms and implications for human disease. Cell Death Dis. 2021;13:14.PubMedPubMedCentralCrossRef Li Y, Zheng W, Lu Y, Zheng Y, Pan L, Wu X, et al. BNIP3L/NIX-mediated mitophagy: molecular mechanisms and implications for human disease. Cell Death Dis. 2021;13:14.PubMedPubMedCentralCrossRef
77.
go back to reference Zhang T, Liu Q, Gao W, Sehgal SA, Wu H. The multifaceted regulation of mitophagy by endogenous metabolites. Autophagy. 2022;18:1216–39.PubMedCrossRef Zhang T, Liu Q, Gao W, Sehgal SA, Wu H. The multifaceted regulation of mitophagy by endogenous metabolites. Autophagy. 2022;18:1216–39.PubMedCrossRef
78.
go back to reference Liu Q, Zhao M, Chen W, Xu K, Huang F, Qu J, et al. Mainstream cigarette smoke induces autophagy and promotes apoptosis in oral mucosal epithelial cells. Arch Oral Biol. 2020;111: 104646.PubMedCrossRef Liu Q, Zhao M, Chen W, Xu K, Huang F, Qu J, et al. Mainstream cigarette smoke induces autophagy and promotes apoptosis in oral mucosal epithelial cells. Arch Oral Biol. 2020;111: 104646.PubMedCrossRef
79.
go back to reference de Lima TB, Paz AHR, Rados PV, Leonardi R, Bufo P, Pedicillo MC, et al. Autophagy analysis in oral carcinogenesis. Pathol Res Pract. 2017;213:1072–7.PubMedCrossRef de Lima TB, Paz AHR, Rados PV, Leonardi R, Bufo P, Pedicillo MC, et al. Autophagy analysis in oral carcinogenesis. Pathol Res Pract. 2017;213:1072–7.PubMedCrossRef
80.
go back to reference Liu W, Yao Y, Shi L, Tang G, Wu L. A novel lncRNA LOLA1 may predict malignant progression and promote migration, invasion, and EMT of oral leukoplakia via the AKT/GSK-3beta pathway. J Cell Biochem. 2021;122:1302–12.PubMedCrossRef Liu W, Yao Y, Shi L, Tang G, Wu L. A novel lncRNA LOLA1 may predict malignant progression and promote migration, invasion, and EMT of oral leukoplakia via the AKT/GSK-3beta pathway. J Cell Biochem. 2021;122:1302–12.PubMedCrossRef
81.
go back to reference Shi L, Yang Y, Li M, Li C, Zhou Z, Tang G, et al. LncRNA IFITM4P promotes immune escape by up-regulating PD-L1 via dual mechanism in oral carcinogenesis. Mol Ther. 2022;30:1564–77.PubMedPubMedCentralCrossRef Shi L, Yang Y, Li M, Li C, Zhou Z, Tang G, et al. LncRNA IFITM4P promotes immune escape by up-regulating PD-L1 via dual mechanism in oral carcinogenesis. Mol Ther. 2022;30:1564–77.PubMedPubMedCentralCrossRef
82.
go back to reference Corsello T, Kudlicki AS, Garofalo RP, Casola A. Cigarette smoke condensate exposure changes RNA content of extracellular vesicles released from small airway epithelial cells. Cells. 2019;8:1652.PubMedPubMedCentralCrossRef Corsello T, Kudlicki AS, Garofalo RP, Casola A. Cigarette smoke condensate exposure changes RNA content of extracellular vesicles released from small airway epithelial cells. Cells. 2019;8:1652.PubMedPubMedCentralCrossRef
83.
go back to reference Chen Z, Wu H, Shi R, Fan W, Zhang J, Su W, et al. miRNAomics analysis reveals the promoting effects of cigarette smoke extract-treated Beas-2B-derived exosomes on macrophage polarization. Biochem Biophys Res Commun. 2021;572:157–63.PubMedCrossRef Chen Z, Wu H, Shi R, Fan W, Zhang J, Su W, et al. miRNAomics analysis reveals the promoting effects of cigarette smoke extract-treated Beas-2B-derived exosomes on macrophage polarization. Biochem Biophys Res Commun. 2021;572:157–63.PubMedCrossRef
84.
go back to reference Zhu Y, Zhang S, Sun J, Wang T, Liu Q, Wu G, et al. Cigarette smoke promotes oral leukoplakia via regulating glutamine metabolism and M2 polarization of macrophage. Int J Oral Sci. 2021;13:25.PubMedPubMedCentralCrossRef Zhu Y, Zhang S, Sun J, Wang T, Liu Q, Wu G, et al. Cigarette smoke promotes oral leukoplakia via regulating glutamine metabolism and M2 polarization of macrophage. Int J Oral Sci. 2021;13:25.PubMedPubMedCentralCrossRef
85.
go back to reference Fujita Y, Araya J, Ito S, Kobayashi K, Kosaka N, Yoshioka Y, et al. Suppression of autophagy by extracellular vesicles promotes myofibroblast differentiation in COPD pathogenesis. J Extracell Vesicles. 2015;4:28388.PubMedCrossRef Fujita Y, Araya J, Ito S, Kobayashi K, Kosaka N, Yoshioka Y, et al. Suppression of autophagy by extracellular vesicles promotes myofibroblast differentiation in COPD pathogenesis. J Extracell Vesicles. 2015;4:28388.PubMedCrossRef
86.
go back to reference Xia H, Wu Y, Zhao J, Li W, Lu L, Ma H, et al. The aberrant cross-talk of epithelium-macrophages via METTL3-regulated extracellular vesicle miR-93 in smoking-induced emphysema. Cell Biol Toxicol. 2022;38:167–83.PubMedCrossRef Xia H, Wu Y, Zhao J, Li W, Lu L, Ma H, et al. The aberrant cross-talk of epithelium-macrophages via METTL3-regulated extracellular vesicle miR-93 in smoking-induced emphysema. Cell Biol Toxicol. 2022;38:167–83.PubMedCrossRef
87.
go back to reference Mondal S, Adhikari N, Banerjee S, Amin SA, Jha T. Matrix metalloproteinase-9 (MMP-9) and its inhibitors in cancer: a minireview. Eur J Med Chem. 2020;194: 112260.PubMedCrossRef Mondal S, Adhikari N, Banerjee S, Amin SA, Jha T. Matrix metalloproteinase-9 (MMP-9) and its inhibitors in cancer: a minireview. Eur J Med Chem. 2020;194: 112260.PubMedCrossRef
89.
go back to reference Shin YJ, Vu H, Lee JH, Kim HD. Diagnostic and prognostic ability of salivary MMP-9 for oral squamous cell carcinoma: a pre-/post-surgery case and matched control study. PLoS ONE. 2021;16: e0248167.PubMedPubMedCentralCrossRef Shin YJ, Vu H, Lee JH, Kim HD. Diagnostic and prognostic ability of salivary MMP-9 for oral squamous cell carcinoma: a pre-/post-surgery case and matched control study. PLoS ONE. 2021;16: e0248167.PubMedPubMedCentralCrossRef
90.
go back to reference Nanda DP, Dutta K, Ganguly KK, Hajra S, Mandal SS, Biswas J, et al. MMP-9 as a potential biomarker for carcinoma of oral cavity: a study in eastern India. Neoplasma. 2014;61:747–57.PubMedCrossRef Nanda DP, Dutta K, Ganguly KK, Hajra S, Mandal SS, Biswas J, et al. MMP-9 as a potential biomarker for carcinoma of oral cavity: a study in eastern India. Neoplasma. 2014;61:747–57.PubMedCrossRef
91.
go back to reference Enășescu DA, Moisescu MG, Imre M, Greabu M, Ripszky Totan A, Stanescu-Spinu I, et al. Lutein treatment effects on the redox status and metalloproteinase-9 (MMP-9) in oral cancer squamous cells-are there therapeutical hopes? Materials. 2021;14:2968.PubMedPubMedCentralCrossRef Enășescu DA, Moisescu MG, Imre M, Greabu M, Ripszky Totan A, Stanescu-Spinu I, et al. Lutein treatment effects on the redox status and metalloproteinase-9 (MMP-9) in oral cancer squamous cells-are there therapeutical hopes? Materials. 2021;14:2968.PubMedPubMedCentralCrossRef
92.
go back to reference Chang PY, Kuo YB, Wu TL, Liao CT, Sun YC, Yen TC, et al. Association and prognostic value of serum inflammation markers in patients with leukoplakia and oral cavity cancer. Clin Chem Lab Med. 2013;51:1291–300.PubMedCrossRef Chang PY, Kuo YB, Wu TL, Liao CT, Sun YC, Yen TC, et al. Association and prognostic value of serum inflammation markers in patients with leukoplakia and oral cavity cancer. Clin Chem Lab Med. 2013;51:1291–300.PubMedCrossRef
93.
go back to reference de Carvalho Fraga CA, Farias LC, de Oliveira MV, Domingos PL, Pereira CS, Silva TF, et al. Increased VEGFR2 and MMP9 protein levels are associated with epithelial dysplasia grading. Pathol Res Pract. 2014;210:959–64.PubMedCrossRef de Carvalho Fraga CA, Farias LC, de Oliveira MV, Domingos PL, Pereira CS, Silva TF, et al. Increased VEGFR2 and MMP9 protein levels are associated with epithelial dysplasia grading. Pathol Res Pract. 2014;210:959–64.PubMedCrossRef
94.
go back to reference Smith J, Rattay T, McConkey C, Helliwell T, Mehanna H. Biomarkers in dysplasia of the oral cavity: a systematic review. Oral Oncol. 2009;45:647–53.PubMedCrossRef Smith J, Rattay T, McConkey C, Helliwell T, Mehanna H. Biomarkers in dysplasia of the oral cavity: a systematic review. Oral Oncol. 2009;45:647–53.PubMedCrossRef
95.
go back to reference Li CJ, Liu Y, Chen Y, Yu D, Williams KJ, Liu ML. Novel proteolytic microvesicles released from human macrophages after exposure to tobacco smoke. Am J Pathol. 2013;182:1552–62.PubMedPubMedCentralCrossRef Li CJ, Liu Y, Chen Y, Yu D, Williams KJ, Liu ML. Novel proteolytic microvesicles released from human macrophages after exposure to tobacco smoke. Am J Pathol. 2013;182:1552–62.PubMedPubMedCentralCrossRef
96.
go back to reference Gonzalez-Molina J, Gramolelli S, Liao Z, Carlson JW, Ojala PM, Lehti K. MMP14 in sarcoma: a regulator of tumor microenvironment communication in connective tissues. Cells. 2019;8:991.PubMedPubMedCentralCrossRef Gonzalez-Molina J, Gramolelli S, Liao Z, Carlson JW, Ojala PM, Lehti K. MMP14 in sarcoma: a regulator of tumor microenvironment communication in connective tissues. Cells. 2019;8:991.PubMedPubMedCentralCrossRef
97.
98.
go back to reference Bourdonnay E, Zaslona Z, Penke LR, Speth JM, Schneider DJ, Przybranowski S, et al. Transcellular delivery of vesicular SOCS proteins from macrophages to epithelial cells blunts inflammatory signaling. J Exp Med. 2015;212:729–42.PubMedPubMedCentralCrossRef Bourdonnay E, Zaslona Z, Penke LR, Speth JM, Schneider DJ, Przybranowski S, et al. Transcellular delivery of vesicular SOCS proteins from macrophages to epithelial cells blunts inflammatory signaling. J Exp Med. 2015;212:729–42.PubMedPubMedCentralCrossRef
99.
go back to reference Donate PB, Alves de Lima K, Peres RS, Almeida F, Fukada SY, Silva TA, et al. Cigarette smoke induces miR-132 in Th17 cells that enhance osteoclastogenesis in inflammatory arthritis. Proc Natl Acad Sci USA. 2021;118: e2017120118.PubMedCrossRef Donate PB, Alves de Lima K, Peres RS, Almeida F, Fukada SY, Silva TA, et al. Cigarette smoke induces miR-132 in Th17 cells that enhance osteoclastogenesis in inflammatory arthritis. Proc Natl Acad Sci USA. 2021;118: e2017120118.PubMedCrossRef
100.
go back to reference Cordazzo C, Petrini S, Neri T, Lombardi S, Carmazzi Y, Pedrinelli R, et al. Rapid shedding of proinflammatory microparticles by human mononuclear cells exposed to cigarette smoke is dependent on Ca2+ mobilization. Inflamm Res. 2014;63:539–47.PubMedCrossRef Cordazzo C, Petrini S, Neri T, Lombardi S, Carmazzi Y, Pedrinelli R, et al. Rapid shedding of proinflammatory microparticles by human mononuclear cells exposed to cigarette smoke is dependent on Ca2+ mobilization. Inflamm Res. 2014;63:539–47.PubMedCrossRef
101.
go back to reference Li M, Yu D, Williams KJ, Liu ML. Tobacco smoke induces the generation of procoagulant microvesicles from human monocytes/macrophages. Arterioscler Thromb Vasc Biol. 2010;30:1818–24.PubMedPubMedCentralCrossRef Li M, Yu D, Williams KJ, Liu ML. Tobacco smoke induces the generation of procoagulant microvesicles from human monocytes/macrophages. Arterioscler Thromb Vasc Biol. 2010;30:1818–24.PubMedPubMedCentralCrossRef
Metadata
Title
The potential roles of cigarette smoke-induced extracellular vesicles in oral leukoplakia
Authors
Qiao Peng
Ning Duan
Xiang Wang
Wenmei Wang
Publication date
01-12-2023
Publisher
BioMed Central
Published in
European Journal of Medical Research / Issue 1/2023
Electronic ISSN: 2047-783X
DOI
https://doi.org/10.1186/s40001-023-01217-0

Other articles of this Issue 1/2023

European Journal of Medical Research 1/2023 Go to the issue