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Research Paper

Doxycycline-induced exogenous Bmi-1 expression enhances tumor formation in a murine model of oral squamous cell carcinoma

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 400-411 | Received 30 Jul 2019, Accepted 17 Jan 2020, Published online: 09 Feb 2020

References

  • Siegel RL, Miller KD, Jemal A. Cancer statistics, 2018. CA Cancer J Clin. 2018;68:7–30. doi:10.3322/caac.21442.
  • Markopoulos AK. Current aspects on oral squamous cell carcinoma. Open Dent J. 2012;6:126–130. doi:10.2174/1874210601206010126.
  • Society AC. Cancer facts & figures. American Cancer Society; 2018.
  • Gao Z, Zhang J, Bonasio R, Strino F, Sawai A, Parisi F, Kluger Y, Reinberg D. Pcgf homologs, cbx proteins, and rybp define functionally distinct prc1 family complexes. Mol Cell. 2012;45:344–356.
  • Sauvageau M, Sauvageau G. Polycomb group proteins: multi-faceted regulators of somatic stem cells and cancer. Cell Stem Cell. 2010;7:299–313. doi:10.1016/j.stem.2010.08.002.
  • Zhu S, Zhao D, Yan L, Jiang W, Kim JS, Gu B, Liu Q, Wang R, Xia B, Zhao JC, Song G. Bmi1 regulates androgen receptor in prostate cancer independently of the polycomb repressive complex 1. Nat Commun. 2018;9:500. doi:10.1038/s41467-018-02863-3.
  • Xin Q, Kong S, Yan J, Qiu J, He B, Zhou C, Ni Z, Bao H, Huang L, Lu J, et al. Polycomb subunit bmi1 determines uterine progesterone responsiveness essential for normal embryo implantation. J Clin Invest. 2018;128:175–189. doi:10.1172/JCI92862.
  • Banerjee Mustafi S, Aznar N, Dwivedi SK, Chakraborty PK, Basak R, Mukherjee P, Ghosh P, Bhattacharya R. Mitochondrial bmi1 maintains bioenergetic homeostasis in cells. Faseb J. 2016;30:4042–4055. doi:10.1096/fj.201600321R.
  • van der Lugt NM, Domen J, Linders K, van Roon M, Robanus-Maandag E, Te Riele H, van der Valk M, Deschamps J, Sofroniew M, van Lohuizen M, et al. Posterior transformation, neurological abnormalities, and severe hematopoietic defects in mice with a targeted deletion of the bmi-1 proto-oncogene. Genes Dev. 1994;8:757–769. doi:10.1101/gad.8.7.757.
  • Park I-K, Qian D, Kiel M, Becker MW, Pihalja M, Weissman IL, Morrison SJ, Clarke MF. Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature. 2003;423:302–305. doi:10.1038/nature01587.
  • Montagnani S, Rueger MA, Hosoda T, Nurzynska D. Adult stem cells in tissue maintenance and regeneration. Stem Cells Int. 2016;2016:7362879. doi:10.1155/2016/7362879.
  • Tanaka T, Komai Y, Tokuyama Y, Yanai H, Ohe S, Okazaki K, Ueno H. Identification of stem cells that maintain and regenerate lingual keratinized epithelial cells. Nat Cell Biol. 2013;15:511–518. doi:10.1038/ncb2719.
  • Jones KB, Furukawa S, Marangoni P, Ma H, Pinkard H, D’Urso R, Zilionis R, Klein AM, Klein OD. Quantitative clonal analysis and single-cell transcriptomics reveal division kinetics, hierarchy, and fate of oral epithelial progenitor cells. Cell Stem Cell. 2019;24:183–192.e188. doi:10.1016/j.stem.2018.10.015.
  • Wang MC, Li CL, Cui J, JIAO M, WU T, JING LI, NAN K-J. Bmi-1, a promising therapeutic target for human cancer. Oncol Lett. 2015;10:583–588. doi:10.3892/ol.2015.3361.
  • Zeuner A. The secret life of quiescent cancer stem cells. Mol Cell Oncol. 2015;2:e968067. doi:10.4161/23723548.2014.968067.
  • Chen YC, Chang CJ, Hsu HS, Chen Y-W, Tai L-K, Tseng L-M, Chiou G-Y, Chang S-C, Kao S-Y, Chiou S-H, et al. 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. doi:10.1016/j.oraloncology.2009.11.007.
  • Han J, Fujisawa T, Husain SR, Puri RK. Identification and characterization of cancer stem cells in human head and neck squamous cell carcinoma. BMC Cancer. 2014;14:173. doi:10.1186/1471-2407-14-173.
  • Prince ME, Sivanandan R, Kaczorowski A, Wolf GT, Kaplan MJ, Dalerba P, Weissman IL, Clarke MF, Ailles LE. 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;104:973–978. doi:10.1073/pnas.0610117104.
  • Tang XH, Knudsen B, Bemis D, Tickoo S, Gudas LJ. Oral cavity and esophageal carcinogenesis modeled in carcinogen-treated mice. Clin Cancer Res. 2004;10:301–313. doi:10.1158/1078-0432.CCR-0999-3.
  • Chen D, Wu M, Li Y, Chang I, Yuan Q, Ekimyan-Salvo M, Deng P, Yu B, Yu Y, Dong J, et al. Targeting bmi1+ cancer stem cells overcomes chemoresistance and inhibits metastases in squamous cell carcinoma. Cell Stem Cell. 2017;20:621–634.e626. doi:10.1016/j.stem.2017.02.003.
  • Rivera C, Venegas B. Histological and molecular aspects of oral squamous cell carcinoma (review). Oncol Lett. 2014;8:7–11. doi:10.3892/ol.2014.2103.
  • Tang XH, Osei-Sarfo K, Urvalek AM. Combination of bexarotene and the retinoid cd1530 reduces murine oral-cavity carcinogenesis induced by the carcinogen 4-nitroquinoline 1-oxide. Proc Natl Acad Sci U S A. 2014;111:8907–8912. doi:10.1073/pnas.1404828111.
  • Tang XH, Albert M, Scognamiglio T, Gudas LJ. A dna methyltransferase inhibitor and all-trans retinoic acid reduce oral cavity carcinogenesis induced by the carcinogen 4-nitroquinoline 1-oxide. Cancer Prev Res (Phila). 2009;2:1100–1110. doi:10.1158/1940-6207.CAPR-09-0136.
  • Osei-Sarfo K, Tang XH, Urvalek AM, Scognamiglio T, Gudas LJ, Xin Q, Kong S, Yan J, Qiu J, He B. The molecular features of tongue epithelium treated with the carcinogen 4-nitroquinoline-1-oxide and alcohol as a model for hnscc. Carcinogenesis. 2013;34:2673–2681. doi:10.1093/carcin/bgt223.
  • Laursen KB, Mongan NP, Zhuang Y, Ng MM, Benoit YD, Gudas LJ. Polycomb recruitment attenuates retinoic acid-induced transcription of the bivalent nr2f1 gene. Nucleic Acids Res. 2013;41:6430–6443. doi:10.1093/nar/gkt367.
  • Xia J, Gill EE, Hancock RE. Networkanalyst for statistical, visual and network-based meta-analysis of gene expression data. Nat Protoc. 2015;10:823–844. doi:10.1038/nprot.2015.052.
  • Tang XH, Scognamiglio T, Gudas LJ. Basal stem cells contribute to squamous cell carcinomas in the oral cavity. Carcinogenesis. 2013;34:1158–1164. doi:10.1093/carcin/bgt021.
  • Cao R, Tsukada Y, Zhang Y. Role of bmi-1 and ring1a in h2a ubiquitylation and hox gene silencing. Mol Cell. 2005;20:845–854. doi:10.1016/j.molcel.2005.12.002.
  • Nakamura S, Oshima M, Yuan J, Saraya A, Miyagi S, Konuma T, Yamazaki S, Osawa M, Nakauchi H, Koseki H et al. Bmi1 confers resistance to oxidative stress on hematopoietic stem cells. PLoS One. 2012;7:e36209. doi:10.1371/journal.pone.0036209.
  • Kimball SR. Eukaryotic initiation factor eif2. Int J Biochem Cell Biol. 1999;31:25–29. doi:10.1016/S1357-2725(98)00128-9.
  • Santos CX, Hafstad AD, Beretta M, Zhang M, Molenaar C, Kopec J, Fotinou D, Murray TV, Cobb AM, Martin D, et al. Targeted redox inhibition of protein phosphatase 1 by nox4 regulates eif2α-mediated stress signaling. Embo J. 2016;35:319–334. doi:10.15252/embj.201592394.
  • Ma XM, Blenis J. Molecular mechanisms of mtor-mediated translational control. Nat Rev Mol Cell Biol. 2009;10:307–318. doi:10.1038/nrm2672.
  • Gingras AC, Raught B, Sonenberg N. Eif4 initiation factors: effectors of mrna recruitment to ribosomes and regulators of translation. Annu Rev Biochem. 1999;68:913–963. doi:10.1146/annurev.biochem.68.1.913.
  • Larsson O, Li S, Issaenko OA, Avdulov S, Peterson M, Smith K, Bitterman PB, Polunovsky VA. Eukaryotic translation initiation factor 4e induced progression of primary human mammary epithelial cells along the cancer pathway is associated with targeted translational deregulation of oncogenic drivers and inhibitors. Cancer Res. 2007;67:6814–6824. doi:10.1158/0008-5472.CAN-07-0752.
  • MF O, Choesmel V, Faubladier M, Fichant G, Gleizes PE. Functional dichotomy of ribosomal proteins during the synthesis of mammalian 40s ribosomal subunits. J Cell Biol. 2010;190:853–866.
  • Liemburg-Apers DC, Willems PH, Koopman WJ, Grefte S. Interactions between mitochondrial reactive oxygen species and cellular glucose metabolism. Arch Toxicol. 2015;89:1209–1226. doi:10.1007/s00204-015-1520-y.
  • Stefková J, Poledne R, Hubácek JA. Atp-binding cassette (abc) transporters in human metabolism and diseases. Physiol Res. 2004;53:235–243.
  • Jiang YJ, Lu B, Kim P, Elias PM, Feingold KR. Regulation of abca1 expression in human keratinocytes and murine epidermis. J Lipid Res. 2006;47:2248–2258. doi:10.1194/jlr.M600163-JLR200.
  • Shah FD, Begum R, Vajaria BN, Patel KR, Patel JB, Shukla SN, Patel PS. A review on salivary genomics and proteomics biomarkers in oral cancer. Indian J Clin Biochem. 2011;26:326–334. doi:10.1007/s12291-011-0149-8.
  • Laplante M, Sabatini DM. Mtor signaling at a glance. J Cell Sci. 2009;122:3589–3594. doi:10.1242/jcs.051011.
  • Gao R, Chen S, Kobayashi M, Yu H, Zhang Y, Wan Y, Young SK, Soltis A, Yu M, Vemula S, et al. Bmi1 promotes erythroid development through regulating ribosome biogenesis. Stem Cells. 2015;33:925–938. doi:10.1002/stem.1896.
  • De Faveri LE, Hurst CD, Roulson JA, Wood H, Sanchez-Carbayo M, Knowles MA, Chapman EJ. Polycomb repressor complex 1 member, bmi1 contributes to urothelial tumorigenesis through p16-independent mechanisms. Transl Oncol. 2015;8:387–399. doi:10.1016/j.tranon.2015.08.002.
  • Baser A, Skabkin M, Martin-Villalba A, Mira Aparicio H, Lie DC. Neural stem cell activation and the role of protein synthesis. Brain Plast. 2017;3:27–41. doi:10.3233/BPL-160038.
  • Tahmasebi S, Amiri M, Sonenberg N. Translational control in stem cells. Front Genet. 2018;9:709. doi:10.3389/fgene.2018.00709.
  • Liu J, Cao L, Chen J, Song S, Lee IH, Quijano C, Liu H, Keyvanfar K, Chen H, Cao L-Y, et al. Bmi1 regulates mitochondrial function and the dna damage response pathway. Nature. 2009;459:387–392. doi:10.1038/nature08040.
  • Dong Q, Oh JE, Chen W, Kim R, Kim RH, Shin K-H, McBride WH, Park N-H, Kang MK. Radioprotective effects of bmi-1 involve epigenetic silencing of oxidase genes and enhanced dna repair in normal human keratinocytes. J Invest Dermatol. 2011;131:1216–1225. doi:10.1038/jid.2011.11.
  • Lee K, Adhikary G, Balasubramanian S, Gopalakrishnan R, McCormick T, Dimri GP, Eckert RL, Rorke EA. Expression of bmi-1 in epidermis enhances cell survival by altering cell cycle regulatory protein expression and inhibiting apoptosis. J Invest Dermatol. 2008;128:9–17. doi:10.1038/sj.jid.5700949.
  • Chou CH, Yang NK, Liu TY, Tai S-K, Hsu DSS, Chen Y-W, Chen Y-J, Chang -C-C, Tzeng C-H, Yang M-H, et al. Chromosome instability modulated by bmi1-aurka signaling drives progression in head and neck cancer. Cancer Res. 2013;73:953–966. doi:10.1158/0008-5472.CAN-12-2397.
  • Kang MK, Kim RH, Kim SJ, Yip FK, Shin K-H, Dimri GP, Christensen R, Han T, Park N-H. 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. doi:10.1038/sj.bjc.6603529.
  • 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;3:273–283. doi:10.1002/cam4.182.
  • Ween MP, Armstrong MA, Oehler MK, Ricciardelli C. The role of abc transporters in ovarian cancer progression and chemoresistance. Crit Rev Oncol Hematol. 2015;96:220–256. doi:10.1016/j.critrevonc.2015.05.012.
  • Paranjape AN, Balaji SA, Mandal T, Krushik EV, Nagaraj P, Mukherjee G, Rangarajan A. Bmi1 regulates self-renewal and epithelial to mesenchymal transition in breast cancer cells through nanog. BMC Cancer. 2014;14:785. doi:10.1186/1471-2407-14-785.

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