DSPP-MMP20 gene silencing downregulates cancer stem cell markers in human oral cancer cells

• Autorzy: Nikitakis N.G. , Gkouveris I. , Aseervatham J. , Barahona K. , Ogbureke K.
• Języki publikacji: EN

Abstrakty

EN

Background: Recent findings indicate that dentin sialophosphoprotein (DSPP) and matrix metalloproteinase (MMP) 20 interact in oral squamous cell carcinoma (OSCC). The objective of this study was to determine the effects of DSPP/MMP20 gene silencing on oral cancer stem cell (OCSC) markers. Methods: The expression of well-established OCSC markers: ABCG2; ALDH1; CD133; CD44; BMI1; LGR4, and Podoplanin in DSPP/MMP20-silenced OSCC cell line, OSC2, and controls were assayed by western blot (WB), and flow cytometry techniques. The sensitivity of OSC2 cells to cisplatin following DSPP/MMP20 silencing was also determined. Results: DSPP/MMP20 silencing resulted in downregulation of OCSC markers, more profoundly ABCG2 (84%) and CD44 (81%), following double silencing. Furthermore, while treatment of parent (pre-silenced) OSC2 cells with cisplatin resulted in upregulation of OCSC markers, DSPP/MMP20-silenced OSC2 cells similarly treated resulted in profound downregulation of OCSC markers (72 to 94% at 50 μM of cisplatin), and a marked reduction in the proportion of ABCG2 and ALDH1 positive cells (~ 1%). Conclusions: We conclude that the downregulation of OCSC markers may signal a reduction in OCSC population following MMP20/DSPP silencing in OSCC cells, while also increasing their sensitivity to cisplatin. Thus, our findings suggest a potential role for DSPP and MMP20 in sustaining OCSC population in OSCCs, possibly, through mechanism(s) that alter OCSC sensitivity to treatment with chemotherapeutic agents such as cisplatin.

• Wydawca: -
• Czasopismo: Cellular and Molecular Biology Letters
• Rocznik: 2018
• Tom: 23
• Opis fizyczny: p.1-14,fig.,ref.

Twórcy

autor

Nikitakis N.G.

• Department of Diagnostic and Biomedical Sciences, University of Texas Health Sciences Center at Houston School of Dentistry, 7500 Cambridge Street, Houston, TX 77054, USA

autor

Gkouveris I.

• Department of Diagnostic and Biomedical Sciences, University of Texas Health Sciences Center at Houston School of Dentistry, 7500 Cambridge Street, Houston, TX 77054, USA

autor

Aseervatham J.

• Department of Diagnostic and Biomedical Sciences, University of Texas Health Sciences Center at Houston School of Dentistry, 7500 Cambridge Street, Houston, TX 77054, USA

autor

Barahona K.

• Department of Diagnostic and Biomedical Sciences, University of Texas Health Sciences Center at Houston School of Dentistry, 7500 Cambridge Street, Houston, TX 77054, USA

autor

Ogbureke K.

• Department of Diagnostic and Biomedical Sciences, University of Texas Health Sciences Center at Houston School of Dentistry, 7500 Cambridge Street, Houston, TX 77054, USA

Bibliografia

• 1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61:69–90.
• 2. Tang X, Hu Y-J, Ju W-T, et al. Elevated growth differentiating factor 15 expression predicts long-term benefit of docetaxel, cisplatin and 5-fluorouracil induction chemotherapy in patients with oral cancer. Oncol Lett. 2018;15:8118–24.
• 3. Zhang SK, Zheng R, Chen Q, et al. Oral cancer incidence and mortality in China, 2011. Chin J Cancer Res. 2015;27:44–51.
• 4. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin. 2015;65:87–108.
• 5. Méry B, Guy JB, Espenel S, Wozny AS, Simonet S, Vallard A, et al. Targeting head and neck tumoral stem cells: from biological aspects to therapeutic perspectives. World J Stem Cells. 2016;8:13–21.
• 6. Qian X, Tan C, Wang F, Yang B, Ge Y, Guan Z, Cai J. Esophageal cancer stem cells and implications for future therapeutics. Onco Targets Ther. 2016;92:247–54.
• 7. Xu L, Huang TJ, Hu H, Wang MY, Shi SM, Yang Q, et al. The developmental transcription factor IRF6 attenuates ABCG2 gene expression and distinctively reverses stemness phenotype in nasopharyngeal carcinoma. Cancer Lett. 2017;
• 8. Nakata S, Phillips E, Goidts V. Emerging role for leucine-rich repeat-containing G-protein-coupled receptors LGR5 and LGR4 in cancer stem cells. Cancer Manag Res. 2014;6:171–80.
• 9. Shah A, Patel S, Pathak J, Swain N, Kumar S. The evolving concepts of cancer stem cells in head and neck squamous cell carcinoma. Sci World J. 2014;2014:842491.
• 10. Patel SS, Shah KA, Shah MJ, Kothari KC, Rawal RM. Cancer stem cells and stemness markers in oral squamous cell carcinomas. Asian Pac J Cancer Prev. 2014;15:8549–56.
• 11. Allegra E, Trapasso S, Pisani D, Puzzo L. The role of BMI1 as a biomarker of cancer stem cells in head and neck cancer a review. Oncology. 2014;86:199–205.
• 12. Chinn SB, Darr OA, Owen JH, Bellile E, McHugh JB, Spector ME, et al. Cancer stem cells: mediators of tumorigenesis and metastasis in head and neck squamous cell carcinoma. Head Neck. 2015;37:317–26.
• 13. Prince ME, Sivanandan R, Kaczorowski A, Wolf GT, Kaplan MJ, Dalerba P, et al. Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proc Natl Acad Sci U S A. 2007;104:973–8.
• 14. Fan Z, Li M, Chen X, et al. Prognostic value of Cancer stem cell markers in head and neck squamous cell carcinoma: a meta-analysis. Sci Rep. 2017;7:43008.
• 15. McDermott SC, Rodriguez-Ramirez C, McDermott SP, Wicha MS, Nör JE. FGFR signaling regulates resistance of head and neck cancer stem cells to cisplatin. Oncotarget. 2018;9(38):25148–65.
• 16. Fisher LW, Jain A, Tayback M, Fedarko NS. Small integrin binding ligand N-linked glycoprotein gene family expression in different cancers. Clin Cancer Res. 2004;10:8501–11.
• 17. Ogbureke KU, Nikitakis NG, Warburton G, Ord RA, Sauk JJ, Waller JL, Fisher LW. Up-regulation of SIBLING proteins and correlation with cognate MMP expression in oral cancer. Oral Oncol. 2007;43:920–32.
• 18. Ogbureke KU, Weinberger PM, Looney SW, Li L, Fisher LW. Expressions of matrix metalloproteinase-9 (MMP-9), dentin sialophosphoprotein (DSPP), and osteopontin (OPN) at histologically negative surgical margins may predict recurrence of oral squamous cell carcinoma. Oncotarget. 2012;3:286–98.
• 19. Anunobi CC, Koli K, Saxena G, Banjo AA, Ogbureke KU. Expression of the SIBLINGs and their MMP partners in human benign and malignant prostate neoplasms. Oncotarget. 2016;7:48038–49.
• 20. Joshi R, Tawfik A, Edeh N, McCloud V, Looney S, Lewis J, et al. Dentin sialophosphoprotein (DSPP) gene-silencing inhibits key tumorigenic activities in human oral cancer cell line. OSC2 PLoS One. 2010;5:e13974.
• 21. Ha NH, Park DG, Woo BH, Kim DJ, Choi JI, et al. Porphyromonas gingivalis increases the invasiveness of oral cancer cells by upregulating IL-8 and MMPs. Cytokine. 2016;86:64–72.
• 22. Gkouveris I, Nikitakis N, Aseervatham J, Rao N, Ogbureke KUE. Matrix metalloproteinases in head and neck cancer: current perspectives. Metalloproteinases Med. 2017;4:47–61.
• 23. Saxena G, Koli K, de la Garza J, Ogbureke KU. Matrix metalloproteinase 20-dentin sialophosphoprotein interaction in oral cancer. J Dent Res. 2015;94:584–93.
• 24. Qian X, Ma C, Nie X, Lu J, Lenarz M, Kaufmann AM, Albers AE. Biology and immunology of cancer stem (−like) cells in head and neck cancer. Crit Rev Oncol Hematol. 2015;95:337–45.
• 25. Dalley AJ, Pitty LP, Major AG, Abdulmajeed AA, Farah CS. Expression of ABCG2 and Bmi-1 in oral potentially malignant lesions and oral squamous cell carcinoma. Cancer Med. 2014;3:273–83.
• 26. Huang L, Lu Q, Han Y, Li Z, Zhang Z, Li X. ABCG2/V-ATPase was associated with the drug resistance and tumor metastasis of esophageal squamous cancer cells. Diagn Pathol. 2012;7:180.
• 27. Lim YC, Kang HJ, Moon JH. C-met pathway promotes self-renewal and tumorigenecity of head and neck squamous cell carcinoma stem-like cell. Oral Oncol. 2014;50:633–9.
• 28. Chen C, Wei Y, Hummel M, Hoffmann TK, Gross M, Kaufmann AM, Albers AE. Evidence for epithelial-mesenchymal transition in cancer stem cells of head and neck squamous cell carcinoma. PLoS One. 2011;6:e16466.
• 29. Davis SJ, Divi V, Owen JH, Bradford CR, Carey TE, Papagerakis S, Prince ME. Metastatic potential of cancer stem cells in head and neck squamous cell carcinoma. Arch Otolaryngol Head Neck Surg. 2010;136:1260–6.
• 30. Vormittag L, Thurnher D, Geleff S, Pammer J, Heiduschka G, Brunner M, et al. Co-expression of BMI1 and podoplanin predicts overall survival in patients with squamous cell carcinoma of the head and neck treated with radio(chemo) therapy. Int J Radiat Oncol Biol Phys. 2009;73:913–8.
• 31. Hsieh JC, Lin HC, Huang CY, Hsu HL, Wu TM, Lee CL, et al. Prognostic value of circulating tumor cells with podoplanin expression in patients with locally advanced or metastatic head and neck squamous cell carcinoma. Head Neck. 2015;37:1448–55.
• 32. Mannelli G, Magnelli L, Deganello A, Busoni M, Meccariello G, Parrinello G, Gallo O. Detection of putative stem cell markers, CD44/CD133, in primary and lymph node metastases in head and neck squamous cell carcinomas. A preliminary immunohistochemical and in vitro study. Clin Otolaryngol. 2015;40:312–20.
• 33. Qiu H, Wang H, Che N, et al. Identification and characterization of CD133pos subpopulation cells from a human laryngeal Cancer cell line. Med Sci Monit. 2016;22:1146–51.
• 34. Zhang Q, Shi S, Yen Y, Brown J, Ta JQ. Le AD. A subpopulation of CD133(+) cancer stem-like cells characterized in human oral squamous cell carcinoma confer resistance to |chemotherapy. Cancer Lett. 2010;289:151–60.
• 35. Xu P, Dang Y, Wang L, Liu X, Ren X, Gu J, et al. Lgr4 is crucial for skin carcinogenesis by regulating MEK/ERK and Wnt/β-catenin signaling pathways. Cancer Lett. 2016;383:161–70.
• 36. Kwon T, Bak Y, Park YH, Jang GB, Nam JS, Yoo JE, et al. Peroxiredoxin II is essential for maintaining Stemness by redox regulation in liver Cancer cells. Stem Cells. 2016;34:1188–97.
• 37. Goel HL, Chang C, Pursell B, Leav I, Lyle S, Xi HS, et al. VEGF/neuropilin-2 regulation of Bmi-1 and consequent repression of IGF-IR define a novel mechanism of aggressive prostate cancer. Cancer Discov. 2012;2:906–21.
• 38. Adini A, Adini I, Ghosh K, Benny O, Pravda E, Hu R, et al. The stem cell marker prominin-/CD133 interacts with vascular endothelial growth factor and potentiates its action. Angiogenesis. 2013;16:405–16.
• 39. Liebscher CA, Prinzler J, Sinn BV, Budczies J, Denkert C, Noske A, et al. Aldehyde dehydrogenase 1/epidermal growth factor receptor coexpression is characteristic of a highly aggressive, poor-prognosis subgroup of highgrade serous ovarian carcinoma. Hum Pathol. 2013;44:1465–71.
• 40. Nalwoga H, Arnes JB, Wabinga H, Akslen LA. Expression of aldehyde dehydrogenase 1 (ALDH1) is associated with basal-like markers and features of aggressive tumours in African breast cancer. Br J Cancer. 2010;102:369–75.
• 41. Li YY, Zhou CX, Gao Y. Podoplanin promotes the invasion of oral squamous cell carcinoma in coordination with MT1-MMP and rho GTPases. Am J Cancer Res. 2015;5:514–29.
• 42. Sterz CM, Kulle C, Dakic B, Makarova G, Böttcher MC, Bette M, et al. A basal-cell-like compartment in head and neck squamous cell carcinomas represents the invasive front of the tumor and is expressing MMP-9. Oral Oncol. 2010;46:116–22.
• 43. Chetty C, Vanamala SK, Gondi CS, Dinh DH, Gujrati M, Rao JS. MMP-9 induces CD44 cleavage and CD44 mediated cell migration in glioblastoma xenograft cells. Cell Signal. 2012;24:549–59.
• 44. Zhang Y, Thant AA, Machida K, Ichigotani Y, Naito Y, Hiraiwa Y, et al. Hyaluronan-CD44s signaling regulates matrix metalloproteinase-2 secretion in a human lung carcinoma cell line QG90. Cancer Res. 2002;62:3962–5.
• 45. Zarrabi K, Dufour A, Li J, Kuscu C, Pulkoski-Gross A, Zhi J, et al. Inhibition of matrix metalloproteinase 14 (MMP-14)- mediated cancer cell migration. J Biol Chem. 2011;286:33167–77.
• 46. Li L, Liu HC, Wang C, Liu X, Hu FC, Xie N, et al. Overexpression of β-catenin induces cisplatin resistance in oral squamous cell carcinoma. Biomed Res Int. 2016;2016:5378567.
• 47. Hardie ME, Kava HW, Murray V. Cisplatin analogues with an increased interaction with DNA: prospects for therapy. Curr Pharm Des. 2016;22:6645–64.
• 48. Nör C, Zhang Z, Warner KA, Bernardi L, Visioli F, Helman JI, et al. Cisplatin induces Bmi-1 and enhances the stem cell fraction in head and neck cancer. Neoplasia. 2014;16:137–46.
• 49. Zhou Y, Zhang L, Pan H, Wang B, Yan F, Fang X, et al. Bmi1 essentially mediates podocalyxin-enhanced cisplatin chemoresistance in oral tongue squamous cell carcinoma. PLoS One. 2015;10:e0123208.
• 50. Kumar B, Yadav A, Lang JC, Cipolla MJ, Schmitt AC, Arradaza N, et al. YM155 reverses cisplatin resistance in head and neck cancer by decreasing cytoplasmic survivin levels. Mol Cancer Ther. 2012;11:1988–98.
• 51. Chang CW, Chen YS, Chen CC, Chan IO, Chen CC, Sheu SJ, et al. Targeting cancer initiating cells by promoting cell differentiation and restoring chemosensitivity via dual inactivation of STAT3 and src activity using an active component of antrodia cinnamomea mycelia. Oncotarget. 2016;7:73016–31.
• 52. Zhao L, Ren Y, Tang H, Wang W, He Q, Sun J, et al. Deregulation of the miR-222-ABCG2 regulatory module in tongue squamous cell carcinoma contributes to chemoresistance and enhanced migratory/invasive potential. Oncotarget. 2015;6:44538–50.

Identyfikatory

DOI

10.1186/s11658-018-0096-y