PLU-1/JARID1B overexpression predicts proliferation properties in head and neck squamous cell carcinoma

Cui,Zhibin; Song,Liwei; Hou,Zhaoyuan; Han,Yifan; Hu,Yuhua; Wu,Yadi; Chen,Wantao; Mao,Li

doi:10.3892/or.2015.3849

PLU-1/JARID1B overexpression predicts proliferation properties in head and neck squamous cell carcinoma

Authors:
- Zhibin Cui
- Liwei Song
- Zhaoyuan Hou
- Yifan Han
- Yuhua Hu
- Yadi Wu
- Wantao Chen
- Li Mao
View Affiliations

Affiliations: Department of Oral and Maxillofacial Surgery, Ninth People's Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200011, P.R. China, Department of General Surgery, Ninth People's Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200011, P.R. China, Department of Biochemistry and Molecular and Cellular Biology, Shanghai Jiao Tong University School of Medicine, Shanghai, P.R. China, Department of Oral Pathology, Ninth People's Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai 200011, P.R. China, Department of Oncology and Diagnostic Sciences, University of Maryland School of Dentistry, Baltimore, MD 20201, USA, Shanghai Key Laboratory of Stomatology, Shanghai 200011, P.R. China
Published online on: March 12, 2015 https://doi.org/10.3892/or.2015.3849
Pages: 2454-2460

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

PLU-1/JARID1B (jumonji AT rich interactive domain 1B) is one of the testis cancer antigens and functions as a histone demethylase in the regulation of various human types of cancers. However, its functions in head and neck squamous cell carcinoma (HNSCC) are rarely reported. The aim of the present study was to examine PLU-1/JARID1B expression levels in HNSCCs and to investigate its role in cancer cell proliferation. In the present study, we found that PLU-1/JARID1B mRNA was upregulated in all tested HNSCC cell lines. Immunohistochemical staining showed that PLU-1/JARID1B protein expression was detected in 87.8% (87/99) of the HNSCC cases. A positive association was observed between high PLU-1/JARID1B expression and higher Ki-67 labeling in the HNSCC samples (Pearson r=0.6514, P=0.0003). Stable PLU-1/JARID1B knockdown by PLU-1-shRNAs in the HNSCC cell lines suppressed cell growth both in the in vitro and in vivo studies. Moreover, PLU-1/JARID1B knockdown resulted in G1 arrest and early apoptosis by suppressing Bcl-2 family members in the HNSCCs. These data indicate that PLU-1/JARID1B is overexpressed in HNSCCs and is associated with tumor proliferation and apoptosis. Therefore, PLU-1/JARID1B represents a candidate proliferation biomarker for HNSCC diagnosis and treatment.

View Figures

View References

1	Sun Q, Zhang J, Cao W, Wang X, Xu Q, Yan M, Wu X and Chen W: Dysregulated miR-363 affects head and neck cancer invasion and metastasis by targeting podoplanin. Int J Biochem Cell Biol. 45:513–520. 2013. View Article : Google Scholar
2	Amente S, Lania L and Majello B: The histone LSD1 demeth-ylase in stemness and cancer transcription programs. Biochim Biophys Acta. 1829:981–986. 2013. View Article : Google Scholar : PubMed/NCBI
3	Jithesh PV, Risk JM, Schache AG, Dhanda J, Lane B, Liloglou T and Shaw RJ: The epigenetic landscape of oral squamous cell carcinoma. Br J Cancer. 108:370–379. 2013. View Article : Google Scholar : PubMed/NCBI
4	Huang PH, Chen CH, Chou CC, Sargeant AM, Kulp SK, Teng CM, Byrd JC and Chen CS: Histone deacetylase inhibitors stimulate histone H3 lysine 4 methylation in part via transcriptional repression of histone H3 lysine 4 demethylases. Mol Pharmacol. 79:197–206. 2011. View Article : Google Scholar :
5	Yamane K, Tateishi K, Klose RJ, Fang J, Fabrizio LA, Erdjument-Bromage H, Taylor-Papadimitriou J, Tempst P and Zhang Y: PLU-1 is an H3K4 demethylase involved in transcriptional repression and breast cancer cell proliferation. Mol Cell. 25:801–812. 2007. View Article : Google Scholar : PubMed/NCBI
6	Barrett A, Santangelo S, Tan K, Catchpole S, Roberts K, Spencer-Dene B, Hall D, Scibetta A, Burchell J, Verdin E, et al: Breast cancer associated transcriptional repressor PLU-1/JARID1B interacts directly with histone deacetylases. Int J Cancer. 121:265–275. 2007. View Article : Google Scholar : PubMed/NCBI
7	Lu PJ, Sundquist K, Baeckstrom D, Poulsom R, Hanby A, Meier-Ewert S, Jones T, Mitchell M, Pitha-Rowe P, Freemont P and Taylor-Papadimitriou J: A novel gene (PLU-1) containing highly conserved putative DNA/chromatin binding motifs is specifically up-regulated in breast cancer. J Biol Chem. 274:15633–15645. 1999. View Article : Google Scholar : PubMed/NCBI
8	Madsen B, Spencer-Dene B, Poulsom R, Hall D, Lu PJ, Scott K, Shaw AT, Burchell JM, Freemont P and Taylor-Papadimitriou J: Characterisation and developmental expression of mouse Plu-1, a homologue of a human nuclear protein (PLU-1) which is specifically up-regulated in breast cancer. Mech Dev. 119(Suppl 1): S239–S246. 2002. View Article : Google Scholar
9	Catchpole S, Spencer-Dene B, Hall D, Santangelo S, Rosewell I, Guenatri M, Beatson R, Scibetta AG, Burchell JM and Taylor-Papadimitriou J: PLU-1/JARID1B/KDM5B is required for embryonic survival and contributes to cell proliferation in the mammary gland and in ER⁺ breast cancer cells. Int J Oncol. 38:1267–1277. 2011.PubMed/NCBI
10	Coleman JA, Correa I, Cooper L, Bohnenkamp HR, Poulsom R, Burchell JM and Taylor-Papadimitriou J: T cells reactive with HLA-A*0201 peptides from the histone demethylase JARID1B are found in the circulation of breast cancer patients. Int J Cancer. 128:2114–2124. 2011. View Article : Google Scholar
11	Ohta K, Haraguchi N, Kano Y, Kagawa Y, Konno M, Nishikawa S, Hamabe A, Hasegawa S, Ogawa H, Fukusumi T, et al: Depletion of JARID1B induces cellular senescence in human colorectal cancer. Int J Oncol. 42:1212–1218. 2013.PubMed/NCBI
12	Hayami S, Yoshimatsu M, Veerakumarasivam A, Unoki M, Iwai Y, Tsunoda T, Field HI, Kelly JD, Neal DE, Yamaue H, et al: Overexpression of the JmjC histone demethylase KDM5B in human carcinogenesis: involvement in the proliferation of cancer cells through the E2F/RB pathway. Mol Cancer. 9:592010. View Article : Google Scholar : PubMed/NCBI
13	Roesch A, Fukunaga-Kalabis M, Schmidt EC, Zabierowski SE, Brafford PA, Vultur A, Basu D, Gimotty P, Vogt T and Herlyn M: A temporarily distinct subpopulation of slow-cycling melanoma cells is required for continuous tumor growth. Cell. 141:583–594. 2010. View Article : Google Scholar : PubMed/NCBI
14	Schmitz SU, Albert M, Malatesta M, Morey L, Johansen JV, Bak M, Tommerup N, Abarrategui I and Helin K: Jarid1b targets genes regulating development and is involved in neural differentiation. EMBO J. 30:4586–4600. 2011. View Article : Google Scholar : PubMed/NCBI
15	Stalker L and Wynder C: Evaluation of histone-modifying enzymes in stem cell populations. Methods Mol Biol. 809:411–426. 2012. View Article : Google Scholar
16	Zhong LP, Pan HY, Zhou XJ, Ye DX, Zhang L, Yang X, Chen WT and Zhang ZY: Characteristics of a cancerous cell line, HIOEC-B(a)P-96, induced by benzo(a)pyrene from human immortalized oral epithelial cell line. Arch Oral Biol. 53:443–452. 2008. View Article : Google Scholar : PubMed/NCBI
17	Cao W, Feng Z, Cui Z, Zhang C, Sun Z, Mao L and Chen W: Up-regulation of enhancer of zeste homolog 2 is associated positively with cyclin D1 overexpression and poor clinical outcome in head and neck squamous cell carcinoma. Cancer. 118:2858–2871. 2012. View Article : Google Scholar
18	Oda D and Watson E: Human oral epithelial cell culture. I Improved conditions for reproducible culture in serum-free medium. In Vitro Cell Dev Biol. 26:589–595. 1990. View Article : Google Scholar : PubMed/NCBI
19	Cao W, Zhang ZY, Xu Q, Sun Q, Yan M, Zhang J, Zhang P, Han ZG and Chen WT: Epigenetic silencing of MAL, a putative tumor suppressor gene, can contribute to human epithelium cell carcinoma. Mol Cancer. 9:2962010. View Article : Google Scholar : PubMed/NCBI
20	Cui Z, Cao W, Li J, Song X, Mao L and Chen W: TRIM24 overexpression is common in locally advanced head and neck squamous cell carcinoma and correlates with aggressive malignant phenotypes. PLoS One. 8:e638872013. View Article : Google Scholar : PubMed/NCBI
21	Barrett A, Madsen B, Copier J, Lu PJ, Cooper L, Scibetta AG, Burchell J and Taylor-Papadimitriou J: PLU-1 nuclear protein, which is upregulated in breast cancer, shows restricted expression in normal human adult tissues: a new cancer/testis antigen? Int J Cancer. 101:581–588. 2002. View Article : Google Scholar : PubMed/NCBI
22	Glazer CA, Smith IM, Ochs MF, Begum S, Westra W, Chang SS, Sun W, Bhan S, Khan Z, Ahrendt S and Califano JA: Integrative discovery of epigenetically derepressed cancer testis antigens in NSCLC. PLoS One. 4:e81892009. View Article : Google Scholar : PubMed/NCBI
23	Yegnasubramanian S, Haffner MC, Zhang Y, Gurel B, Cornish TC, Wu Z, Irizarry RA, Morgan J, Hicks J, DeWeese TL, et al: DNA hypomethylation arises later in prostate cancer progression than CpG island hypermethylation and contributes to metastatic tumor heterogeneity. Cancer Res. 68:8954–8967. 2008. View Article : Google Scholar : PubMed/NCBI
24	Kim SG, Kim AS, Jeong JH, Choi JY and Kweon H: 4-Hexyl-resorcinol stimulates the differentiation of SCC-9 cells through the suppression of E2F2, E2F3 and Sp3 expression and the promotion of Sp1 expression. Oncol Rep. 28:677–681. 2012.PubMed/NCBI
25	Kulkarni P, Shiraishi T, Rajagopalan K, Kim R, Mooney SM and Getzenberg RH: Cancer/testis antigens and urological malignancies. Nat Rev Urol. 9:386–396. 2012. View Article : Google Scholar : PubMed/NCBI
26	Zhao WF, Wang HB, Xie B, Hu LJ, Xu LH, Kuang BH, Li MZ and Zhang X: Sp1 and Sp3 are involved in the full transcriptional activity of centromere protein H in human nasopharyngeal carcinoma cells. FEBS J. 279:2714–2726. 2012. View Article : Google Scholar : PubMed/NCBI
27	Clahsen PC, van de Velde CJ, Duval C, Pallud C, Mandard AM, Delobelle-Deroide A, van den Broek L and van de Vijver MJ: The utility of mitotic index, oestrogen receptor and Ki-67 measurements in the creation of novel prognostic indices for node-negative breast cancer. Eur J Surg Oncol. 25:356–363. 1999. View Article : Google Scholar : PubMed/NCBI
28	Colozza M, Azambuja E, Cardoso F, Sotiriou C, Larsimont D and Piccart MJ: Proliferative markers as prognostic and predictive tools in early breast cancer: where are we now? Ann Oncol. 16:1723–1739. 2005. View Article : Google Scholar : PubMed/NCBI
29	Trihia H, Murray S, Price K, Gelber RD, Golouh R, Goldhirsch A, Coates AS, Collins J, Castiglione-Gertsch M and Gusterson BA: International Breast Cancer Study Group: Ki-67 expression in breast carcinoma: its association with grading systems, clinical parameters, and other prognostic factors - a surrogate marker? Cancer. 97:1321–1331. 2003. View Article : Google Scholar : PubMed/NCBI
30	Raman V, Martensen SA, Reisman D, Evron E, Odenwald WF, Jaffee E, Marks J and Sukumar S: Compromised HOXA5 function can limit p53 expression in human breast tumours. Nature. 405:974–978. 2000. View Article : Google Scholar : PubMed/NCBI