Loss of oral mucosal stem cell markers in oral submucous fibrosis and their reactivation in malignant transformation

Mohit Sharma , Felipe Paiva Fonseca , Keith D. Hunter , Raghu Radhakrishnan

International Journal of Oral Science ›› 2020, Vol. 12 ›› Issue (1) : 23

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International Journal of Oral Science ›› 2020, Vol. 12 ›› Issue (1) : 23 DOI: 10.1038/s41368-020-00090-5
Review Article

Loss of oral mucosal stem cell markers in oral submucous fibrosis and their reactivation in malignant transformation

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Abstract

The integrity of the basal stem cell layer is critical for epithelial homoeostasis. In this paper, we review the expression of oral mucosal stem cell markers (OM-SCMs) in oral submucous fibrosis (OSF), oral potentially malignant disorders (OPMDs) and oral squamous cell carcinoma (OSCC) to understand the role of basal cells in potentiating cancer stem cell behaviour in OSF. While the loss of basal cell clonogenicity triggers epithelial atrophy in OSF, the transition of the epithelium from atrophic to hyperplastic and eventually neoplastic involves the reactivation of basal stemness. The vacillating expression patterns of OM-SCMs confirm the role of keratins 5, 14, 19, CD44, β1-integrin, p63, sex-determining region Y box (SOX2), octamer-binding transcription factor 4 (Oct-4), c-MYC, B-cell-specific Moloney murine leukaemia virus integration site 1 (Bmi-1) and aldehyde dehydrogenase 1 (ALDH1) in OSF, OPMDs and OSCC. The downregulation of OM-SCMs in the atrophic epithelium of OSF and their upregulation during malignant transformation are illustrated with relevant literature in this review.

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Mohit Sharma, Felipe Paiva Fonseca, Keith D. Hunter, Raghu Radhakrishnan. Loss of oral mucosal stem cell markers in oral submucous fibrosis and their reactivation in malignant transformation. International Journal of Oral Science, 2020, 12(1): 23 DOI:10.1038/s41368-020-00090-5

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References

[1]

Ray JG, Chatterjee R, Chaudhuri K. Oral submucous fibrosis: a global challenge. Rising incidence, risk factors, management, and research priorities. Periodontol 2000, 2019, 80: 200-212.

[2]

Sharma M, Shetty SS, Radhakrishnan R. Oral submucous fibrosis as an overhealing wound: implications in malignant transformation. Recent Pat. Anticancer Drug Discov., 2018, 13: 272-291.

[3]

Shih YH, Wang TH, Shieh TM, Tseng YH. Oral submucous fibrosis: a review on etiopathogenesis, diagnosis, and therapy. Int. J. Mol. Sci., 2019, 20: 2940.

[4]

Khan I, . Epithelial atrophy in oral submucous fibrosis is mediated by copper (II) and arecoline of areca nut. J. Cell. Mol. Med., 2015, 19: 2397-2412.

[5]

Jones RE, Foster DS, Hu MS, Longaker MT. Wound healing and fibrosis: current stem cell therapies. Transfusion, 2019, 59: 884-892.

[6]

Ge Y, . Stem cell lineage infidelity drives wound repair and cancer. Cell, 2017, 169: 636-650.

[7]

Rajendran R, Sunil, Twinkle SP, Anikumar TV, Annie J. Cell death does not herald epithelial involution (“atrophy”) in oral sub mucous fibrosis: a TEM study. Indian J. Dent. Res., 2004, 15: 13-19.

[8]

Li N, . Discovery of novel biomarkers in oral submucous fibrosis by microarray analysis. Cancer Epidemiol. Biomark. Prev., 2008, 17: 2249-2259.

[9]

Veeravarmal V, Austin RD, Nagini S, Nassar MHM. Expression of β1integrin in normal epithelium, oral submucous fibrosis and oral squamous cell carcinoma. Pathol. Res. Pract., 2018, 214: 273-280.

[10]

Bazarsad S, . Identification of a combined biomarker for malignant transformation in oral submucous fibrosis. J. Oral. Pathol. Med., 2017, 46: 431-438.

[11]

Rajendran R, Varkey S. Inducible nitric oxide synthase expression is upregulated in oral submucous fibrosis. Indian J. Dent. Res., 2007, 18: 94-100.

[12]

Das RK, . Epithelio-mesenchymal transitional attributes in oral sub-mucous fibrosis. Exp. Mol. Pathol., 2013, 95: 259-269.

[13]

Anura A, . Endorsing cellular competitiveness in aberrant epithelium of oral submucous fibrosis progression: neighbourhood analysis of immunohistochemical attributes. Histochem. Cell Biol., 2018, 150: 61-75.

[14]

Das RK, . Assessment of malignant potential of oral submucous fibrosis through evaluation of p63, E-cadherin and CD105 expression. J. Clin. Pathol., 2010, 63: 894-899.

[15]

Overstreet JM, Samarakoon R, Meldrum KK, Higgins PJ. Redox control of p53 in the transcriptional regulation of TGF-beta1 target genes through SMAD cooperativity. Cell Signal., 2014, 26: 1427-1436.

[16]

Kawarada Y, . TGF-β induces p53/Smads complex formation in the PAI-1 promoter to activate transcription. Sci. Rep., 2016, 6

[17]

Sachdeva M, . p53 represses c-Myc through induction of the tumor suppressor miR-145. Proc. Natl Acad. Sci. USA, 2009, 106: 3207-3212.

[18]

Wang TY, . Acquisition cancer stemness, mesenchymal transdifferentiation, and chemoresistance properties by chronic exposure of oral epithelial cells to arecoline. Oncotarget, 2016, 7: 84072-84081.

[19]

Baillie R, Tan ST, Itinteang T. Cancer stem cells in oral cavity squamous cell carcinoma: a review. Front. Oncol., 2017, 7: 112.

[20]

Feng JQ, . Expression of cancer stem cell markers ALDH1 and Bmi1 in oral erythroplakia and the risk of oral cancer. J. Oral. Pathol. Med., 2013, 42: 148-153.

[21]

Rodini CO, Lopes NM, Lara VS, Mackenzie IC. Oral cancer stem cells—properties and consequences. J. Appl. Oral. Sci., 2017, 25: 708-715.

[22]

Jones KB, Klein OD. Oral epithelial stem cells in tissue maintenance and disease: the first steps in a long journey. Int. J. Oral. Sci., 2013, 5: 121-129.

[23]

Batlle E, Clevers H. Cancer stem cells revisited. Nat. Med., 2017, 23: 1124-1134.

[24]

Rich JN. Cancer stem cells: understanding tumor hierarchy and heterogeneity. Medicine, 2016, 95: S2-S7.

[25]

Hu FW, . Impairment of tumor-initiating stem-like property and reversal of epithelial-mesenchymal transdifferentiation in head and neck cancer by resveratrol treatment. Mol. Nutr. Food Res., 2012, 56: 1247-1258.

[26]

Sinha N, Mukhopadhyay S, Das DN, Panda PK, Bhutia SK. Relevance of cancer initiating/stem cells in carcinogenesis and therapy resistance in oral cancer. Oral. Oncol., 2013, 49: 854-862.

[27]

Chen YC, . Inhibition of tumorigenicity and enhancement of radiochemosensitivity in head and neck squamous cell cancer-derived ALDH1-positive cells by knockdown of Bmi-1. Oral. Oncol., 2010, 46: 158-165.

[28]

Costea DE, Tsinkalovsky O, Vintermyr OK, Johannessen AC, Mackenzie IC. Cancer stem cells—new and potentially important targets for the therapy of oral squamous cell carcinoma. Oral. Dis., 2006, 12: 443-454.

[29]

De Boeck A, . Resident and bone marrow-derived mesenchymal stem cells in head and neck squamous cell carcinoma. Oral. Oncol., 2010, 46: 336-342.

[30]

Schneider S, . Expression of the sonic hedgehog pathway in squamous cell carcinoma of the skin and the mucosa of the head and neck. Head. Neck, 2011, 33: 244-250.

[31]

Prince ME, . Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proc. Natl Acad. Sci. USA, 2007, 104: 973-978.

[32]

Fu TY, . Association of OCT4, SOX2, and NANOG expression with oral squamous cell carcinoma progression. J. Oral. Pathol. Med., 2016, 45: 89-95.

[33]

Rodrigues M, . Prognostic implications of CD44, NANOG, OCT4, and BMI1 expression in tongue squamous cell carcinoma. Head Neck, 2018, 40: 1759-1773.

[34]

Ortiz RC, . CD44 and ALDH1 immunoexpression as prognostic indicators of invasion and metastasis in oral squamous cell carcinoma. J. Oral. Pathol. Med., 2018, 47: 740-747.

[35]

Lobo NA, Shimono Y, Qian D, Clarke MF. The biology of cancer stem cells. Annu. Rev. Cell Dev. Biol., 2007, 23: 675-699.

[36]

Katoh M, Katoh M. WNT signaling pathway and stem cell signaling network. Clin. Cancer Res., 2007, 13: 4042-4045.

[37]

Milosevic M, . Characterization of stem-like cancer cells in basal cell carcinoma and its surgical margins. Exp. Dermatol., 2018, 27: 1160-1165.

[38]

Lazarevic M, . Putative cancer stem cells are present in surgical margins of oral squamous cell carcinoma. J. BUON, 2018, 23: 1686-1692.

[39]

Lazarevic M, . Marked epithelial to mesenchymal transition in surgical margins of oral canceran in vitro study. Oncol. Lett., 2020, 19: 3743-3750.

[40]

Kobayashi CI, Suda T. Regulation of reactive oxygen species in stem cells and cancer stem cells. J. Cell. Physiol., 2012, 227: 421-430.

[41]

Xu Q, . EGF induces epithelial-mesenchymal transition and cancer stem-like cell properties in human oral cancer cells via promoting Warburg effect. Oncotarget, 2017, 8: 9557-9571.

[42]

Zhao H, Hu CY, Chen WM, Huang P. Lactate promotes cancer stem-like property of oral sequamous cell carcinoma. Curr. Med. Sci., 2019, 39: 403-409.

[43]

Chen YC, . Aldehyde dehydrogenase 1 is a putative marker for cancer stem cells in head and neck squamous cancer. Biochem. Biophys. Res. Commun., 2009, 385: 307-313.

[44]

Bertrand G, . Targeting head and neck cancer stem cells to overcome resistance to photon and carbon ion radiation. Stem Cell Rev., 2014, 10: 114-126.

[45]

Masui T, . Snail-induced epithelial-mesenchymal transition promotes cancer stem cell-like phenotype in head and neck cancer cells. Int. J. Oncol., 2014, 44: 693-699.

[46]

Seino S, . CD44(high) /ALDH1(high) head and neck squamous cell carcinoma cells exhibit mesenchymal characteristics and GSK3beta-dependent cancer stem cell properties. J. Oral. Pathol. Med., 2016, 45: 180-188.

[47]

Hildebrand LC, . Spatial distribution of cancer stem cells in head and neck squamous cell carcinomas. J. Oral. Pathol. Med., 2014, 43: 499-506.

[48]

Visus C, . Identification of human aldehyde dehydrogenase 1 family member A1 as a novel CD8+ T-cell-defined tumor antigen in squamous cell carcinoma of the head and neck. Cancer Res., 2007, 67: 10538-10545.

[49]

Li YC, Cheng AJ, Lee LY, Huang YC, Chang JT. Multifaceted mechanisms of areca nuts in oral carcinogenesis: the molecular pathology from precancerous condition to malignant transformation. J. Cancer, 2019, 10: 4054-4062.

[50]

Li YC, . Areca nut contributes to oral malignancy through facilitating the conversion of cancer stem cells. Mol. Carcinog., 2016, 55: 1012-1023.

[51]

Liu W, . Two stem cell markers, ATP-binding cassette, G2 subfamily (ABCG2) and BMI-1, predict the transformation of oral leukoplakia to cancer: a long-term follow-up study. Cancer, 2012, 118: 1693-1700.

[52]

Liu W, . Expression patterns of cancer stem cell markers ALDH1 and CD133 correlate with a high risk of malignant transformation of oral leukoplakia. Int. J. Cancer, 2013, 132: 868-874.

[53]

Feng J, Zhou Z, Shi L, Yang X, Liu W. Cancer stem cell markers ALDH1 and Bmi1 expression in oral erythroplakia revisited: implication for driving the process of field cancerization. J. Oral. Pathol. Med., 2020, 49: 96-99.

[54]

Yang X, Shi L, Zhou Z, Liu W. Podoplanin and ABCG2 expression in oral erythroplakia revisited: potential evidence for cancer stem cells driving the process of field cancerization. Oral. Oncol., 2020, 101: 104368.

[55]

Calenic B, Greabu M, Caruntu C, Tanase C, Battino M. Oral keratinocyte stem/progenitor cells: specific markers, molecular signaling pathways and potential uses. Periodontol 2000, 2015, 69: 68-82.

[56]

Li N, Li X, Chen K, Dong H, Kagami H. Characterization of spontaneous spheroids from oral mucosa-derived cells and their direct comparison with spheroids from skin-derived cells. Stem Cell Res. Ther., 2019, 10: 184.

[57]

Hisha H, Tanaka T, Ueno H. Lingual epithelial stem cells and organoid culture of them. Int. J. Mol. Sci., 2016, 17: 168.

[58]

Moses MA, . Molecular mechanisms of p63-mediated squamous cancer pathogenesis. Int. J. Mol. Sci., 2019, 20: 3590.

[59]

Bose A, . Two mechanisms regulate keratin K15 expression in keratinocytes: role of PKC/AP-1 and FOXM1 mediated signalling. PLoS ONE, 2012, 7: e38599.

[60]

Ishii A, . Expression of p75(NGFR), a proliferative and basal cell marker, in the buccal mucosa epithelium during re-epithelialization. Acta Histochem. Cytochem., 2014, 47: 145-153.

[61]

Cherukuri P, . Phosphorylation of DeltaNp63alpha via a novel TGFbeta/ALK5 signaling mechanism mediates the anti-clonogenic effects of TGFbeta. PLoS ONE, 2012, 7: e50066.

[62]

Hildesheim J, . Gadd45a regulates matrix metalloproteinases by suppressing ΔNp63α and β-catenin via p38 MAP kinase and APC complex activation. Oncogene, 2004, 23: 1829-1837.

[63]

Cojoc M, . Aldehyde dehydrogenase is regulated by β-catenin/TCF and promotes radioresistance in prostate cancer progenitor cells. Cancer Res., 2015, 75: 1482-1494.

[64]

Alam H, Sehgal L, Kundu ST, Dalal SN, Vaidya MM. Novel function of keratins 5 and 14 in proliferation and differentiation of stratified epithelial cells. Mol. Biol. Cell, 2011, 22: 4068-4078.

[65]

Dmello C, . Vimentin regulates differentiation switch via modulation of keratin 14 levels and their expression together correlates with poor prognosis in oral cancer patients. PLoS ONE, 2017, 12: e0172559.

[66]

Xia H, . Pathologic caveolin-1 regulation of PTEN in idiopathic pulmonary fibrosis. Am. J. Pathol., 2010, 176: 2626-2637.

[67]

Lin HC, . High-level beta1-integrin expression in a subpopulation of highly tumorigenic oral cancer cells. Clin. Oral. Investig., 2014, 18: 1277-1284.

[68]

Barkan D, Chambers AF. β1-integrin: a potential therapeutic target in the battle against cancer recurrence. Clin. Cancer Res., 2011, 17: 7219-7223.

[69]

Shishido S, Bonig H, Kim YM. Role of integrin alpha4 in drug resistance of leukemia. Front. Oncol., 2014, 4: 99.

[70]

Zhang HF, . The PI3K/AKT/c-MYC axis promotes the acquisition of cancer stem-like features in esophageal squamous cell carcinoma. Stem Cells, 2016, 34: 2040-2051.

[71]

Ha L, Ponnamperuma RM, Jay S, Ricci MS, Weinberg WC. Dysregulated DeltaNp63alpha inhibits expression of Ink4a/arf, blocks senescence, and promotes malignant conversion of keratinocytes. PLoS ONE, 2011, 6: e21877.

[72]

Chang MC, . Areca nut components affect COX-2, cyclin B1/cdc25C and keratin expression, PGE2 production in keratinocyte is related to reactive oxygen species, CYP1A1, Src, EGFR and Ras signaling. PLoS ONE, 2014, 9: e101959.

[73]

Mognetti B, . ΔNp63α as early indicator of malignancy in surgical margins of an oral squamous cell carcinoma. Oral. Oncol. Extras, 2005, 41: 129-131.

[74]

Candi E, . TAp63 and DeltaNp63 in cancer and epidermal development. Cell Cycle, 2007, 6: 274-285.

[75]

Wang GX, . DeltaNp63 inhibits oxidative stress-induced cell death, including ferroptosis, and cooperates with the BCL-2 family to promote clonogenic survival. Cell Rep., 2017, 21: 2926-2939.

[76]

Compagnone M, . DeltaNp63-mediated regulation of hyaluronic acid metabolism and signaling supports HNSCC tumorigenesis. Proc. Natl Acad. Sci. USA, 2017, 114: 13254-13259.

[77]

Keyes WM, . DeltaNp63alpha is an oncogene that targets chromatin remodeler Lsh to drive skin stem cell proliferation and tumorigenesis. Cell Stem Cell, 2011, 8: 164-176.

[78]

Viticchie G, . p63 supports aerobic respiration through hexokinase II. Proc. Natl Acad. Sci. USA, 2015, 112: 11577-11582.

[79]

Roberts DJ, Miyamoto S. Hexokinase II integrates energy metabolism and cellular protection: akting on mitochondria and TORCing to autophagy. Cell Death Differ., 2015, 22: 248-257.

[80]

Victorelli S, Passos JF. Reactive oxygen species detection in senescent cells. Methods Mol. Biol., 2019, 1896: 21-29.

[81]

He X, . Chromatin remodeling factor LSH drives cancer progression by suppressing the activity of fumarate hydratase. Cancer Res., 2016, 76: 5743-5755.

[82]

Yang M, Soga T, Pollard PJ, Adam J. The emerging role of fumarate as an oncometabolite. Front. Oncol., 2012, 2: 85-85.

[83]

Courtnay R, . Cancer metabolism and the Warburg effect: the role of HIF-1 and PI3K. Mol. Biol. Rep., 2015, 42: 841-851.

[84]

Bourguignon LYW. Matrix hyaluronan-CD44 interaction activates MicroRNA and LncRNA signaling associated with chemoresistance, invasion, and tumor progression. Front. Oncol., 2019, 9: 492.

[85]

Yoh K, Prywes R. Pathway regulation of p63, a director of epithelial cell fate. Front. Endocrinol., 2015, 6: 51.

[86]

Chu WK, Dai PM, Li HL, Chen JK. Transcriptional activity of the DeltaNp63 promoter is regulated by STAT3. J. Biol. Chem., 2008, 283: 7328-7337.

[87]

Wong WJ, Qiu B, Nakazawa MS, Qing G, Simon MC. MYC degradation under low O2 tension promotes survival by evading hypoxia-induced cell death. Mol. Cell. Biol., 2013, 33: 3494-3504.

[88]

Wang L, Xue M, Chung DC. c-Myc is regulated by HIF-2alpha in chronic hypoxia and influences sensitivity to 5-FU in colon cancer. Oncotarget, 2016, 7: 78910-78917.

[89]

Wang LH, Xu M, Fu LQ, Chen XY, Yang F. The antihelminthic niclosamide inhibits cancer stemness, extracellular matrix remodeling, and metastasis through dysregulation of the nuclear beta-catenin/c-Myc axis in OSCC. Sci. Rep., 2018, 8

[90]

Kim MJ, . PAF-Myc-controlled cell stemness is required for intestinal regeneration and tumorigenesis. Dev. Cell, 2018, 44: 582-596. e4

[91]

Huang H, . NF-kappaB1 inhibits c-Myc protein degradation through suppression of FBW7 expression. Oncotarget, 2014, 5: 493-505.

[92]

Sawant S, . Prognostic role of Oct4, CD44 and c-Myc in radio-chemo-resistant oral cancer patients and their tumourigenic potential in immunodeficient mice. Clin. Oral. Investig., 2016, 20: 43-56.

[93]

Itahana K, Campisi J, Dimri GP. Mechanisms of cellular senescence in human and mouse cells. Biogerontology, 2004, 5: 1-10.

[94]

Jacobs JJ, Kieboom K, Marino S, DePinho RA, van Lohuizen M. The oncogene and polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature, 1999, 397: 164-168.

[95]

Kang MK, . Elevated Bmi-1 expression is associated with dysplastic cell transformation during oral carcinogenesis and is required for cancer cell replication and survival. Br. J. Cancer, 2007, 96: 126-133.

[96]

Nacerddine K, . Akt-mediated phosphorylation of Bmi1 modulates its oncogenic potential, E3 ligase activity, and DNA damage repair activity in mouse prostate cancer. J. Clin. Investig., 2012, 122: 1920-1932.

[97]

Yu CC, . Bmi-1 regulates snail expression and promotes metastasis ability in head and neck squamous cancer-derived ALDH1 positive cells. J. Oncol., 2011, 2011: 609259.

[98]

Sawant SS, . Clinical significance of aberrant vimentin expression in oral premalignant lesions and carcinomas. Oral. Dis., 2014, 20: 453-465.

[99]

Zheng L, . miR-203 inhibits arecoline-induced epithelial-mesenchymal transition by regulating secreted frizzled-related protein 4 and transmembrane-4 L six family member 1 in oral submucous fibrosis. Oncol. Rep., 2015, 33: 2753-2760.

[100]

Rajkumar K, . Salivary and serum level of CYFRA 21-1 in oral precancer and oral squamous cell carcinoma. Oral. Dis., 2015, 21: 90-96.

[101]

Dohmoto K, . The role of caspase 3 in producing cytokeratin 19 fragment (CYFRA21-1) in human lung cancer cell lines. Int. J. Cancer, 2001, 91: 468-473.

[102]

Garnier P, . Hypoxia induces caspase-9 and caspase-3 activation without neuronal death in gerbil brains. Eur. J. Neurosci., 2004, 20: 937-946.

[103]

Veeravarmal V, Austin RD, Siddavaram N, Thiruneelakandan S, Nassar MH. Caspase-3 expression in normal oral epithelium, oral submucous fibrosis and oral squamous cell carcinoma. J. Oral. Maxillofac. Pathol., 2016, 20: 445-452.

[104]

Safadi RA, Musleh AS, Al-Khateeb TH, Hamasha AA. Analysis of immunohistochemical expression of k19 in oral epithelial dysplasia and oral squamous cell carcinoma using color deconvolution-image analysis method. Head. Neck Pathol., 2010, 4: 282-289.

[105]

Khanom R, . Expression of basal cell keratin 15 and keratin 19 in oral squamous neoplasms represents diverse pathophysiologies. Histol. Histopathol., 2012, 27: 949-959.

[106]

Ernst J, . Expression of CK19 is an independent predictor of negative outcome for patients with squamous cell carcinoma of the tongue. Oncotarget, 2016, 7: 76151-76158.

[107]

Carafoli F, Hohenester E. Collagen recognition and transmembrane signalling by discoidin domain receptors. Biochim. Biophys. Acta, 2013, 1834: 2187-2194.

[108]

Zhou Q, . Characterization of in vivo keratin 19 phosphorylation on tyrosine-391. PLoS ONE, 2010, 5: e13538.

[109]

Matte BF, . Matrix stiffness mechanically conditions EMT and migratory behavior of oral squamous cell carcinoma. J. Cell Sci., 2019, 132: jcs224360.

[110]

Hiemer SE, . A YAP/TAZ-regulated molecular signature is associated with oral squamous cell carcinoma. Mol. Cancer Res., 2015, 13: 957-968.

[111]

Nukuda A, . Stiff substrates increase YAP-signaling-mediated matrix metalloproteinase-7 expression. Oncogenesis, 2015, 4

[112]

Fisher ML, Ciavattone N, Grun D, Adhikary G, Eckert RL. Sulforaphane reduces YAP/Np63alpha signaling to reduce cancer stem cell survival and tumor formation. Oncotarget, 2017, 8: 73407-73418.

[113]

Li J, . The hippo effector TAZ promotes cancer stemness by transcriptional activation of SOX2 in head neck squamous cell carcinoma. Cell Death Dis., 2019, 10

[114]

Chen X, . C-MYC and BCL-2 mediate YAP-regulated tumorigenesis in OSCC. Oncotarget, 2018, 9: 668-679.

[115]

Zhou ZT, Jiang WW. Cancer stem cell model in oral squamous cell carcinoma. Curr. Stem Cell Res. Ther., 2008, 3: 17-20.

[116]

Yu CC, Liao YW, Yu CH, Chang YC. STRO-1 confers myofibroblast transdifferentiation in fibroblasts derived from oral submucous fibrosis. J. Oral. Pathol. Med., 2018, 47: 299-305.

[117]

Ye MY, . Growth-regulated oncogene-alpha from oral submucous fibrosis fibroblasts promotes malignant transformation of oral precancerous cells. J. Oral. Pathol. Med., 2018, 47: 880-886.

[118]

Ritchie KE, Nor JE. Perivascular stem cell niche in head and neck cancer. Cancer Lett., 2013, 338: 41-46.

[119]

Campos MS, Neiva KG, Meyers KA, Krishnamurthy S, Nor JE. Endothelial derived factors inhibit anoikis of head and neck cancer stem cells. Oral. Oncol., 2012, 48: 26-32.

[120]

Winquist RJ, Boucher DM, Wood M, Furey BF. Targeting cancer stem cells for more effective therapies: taking out cancer’s locomotive engine. Biochem. Pharmacol., 2009, 78: 326-334.

[121]

Ishii H, . Cancer stem cells and chemoradiation resistance. Cancer Sci., 2008, 99: 1871-1877.

[122]

Frank NY, Schatton T, Frank MH. The therapeutic promise of the cancer stem cell concept. J. Clin. Investig., 2010, 120: 41-50.

[123]

Trumpp A, Wiestler OD. Mechanisms of disease: cancer stem cells-targeting the evil twin. Nat. Clin. Pract. Oncol., 2008, 5: 337-347.

[124]

Glavinas H, Krajcsi P, Cserepes J, Sarkadi B. The role of ABC transporters in drug resistance, metabolism and toxicity. Curr. Drug Deliv., 2004, 1: 27-42.

[125]

Hatina J, . Tumour stem cells-a new concept in tumour biology. Dtsch. Med. Wochenschr., 2007, 132: 1629-1632.

[126]

Epa AP, . Normal human lung epithelial cells inhibit transforming growth factor-beta induced myofibroblast differentiation via prostaglandin E2. PLoS ONE, 2015, 10: e0135266.

[127]

Varga J, Greten FR. Cell plasticity in epithelial homeostasis and tumorigenesis. Nat. Cell Biol., 2017, 19: 1133-1141.

[128]

Gottipamula S, Sundarrajan S, Moorthy A, Padmanabhan S, Sridhar NK. Buccal mucosal epithelial cells downregulate CTGF expression in buccal submucosal fibrosis fibroblasts. J. Maxillofac. Oral. Surg., 2018, 17: 254-259.

[129]

Wang X, . Inhibition of dermal fibrosis in self-assembled skin equivalents by undifferentiated keratinocytes. J. Dermatol. Sci., 2009, 53: 103-111.

Funding

DST | Science and Engineering Research Board (SERB)(EMR/2017/002792)

Science and Engineering Board (SERB), Department of Science and Technology (DST), Government of India Grant Reference Number - EMR/2017/002792

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