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Published in: BMC Cancer 1/2014

Open Access 01-12-2014 | Research article

Significance of CD44 expression in head and neck cancer: a systemic review and meta-analysis

Authors: Jianqiang Chen, Jianding Zhou, Jie Lu, Hua Xiong, Xueli Shi, Liang Gong

Published in: BMC Cancer | Issue 1/2014

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Abstract

Background

CD44 has been reported to be involved with tumor growth and metastasis and has also been implicated as a CSC marker in head and neck squamous cell cancer (HNSCC). However, the prognostic value of CD44 still remains controversial; hence, we investigated the correlation between CD44 and the clinicopathological features of HNSCC by meta-analysis.

Methods

A comprehensive search was performed using PubMed, ISI web of Science and China National Knowledge Infrastructure (CNKI) up to April 2013. Only studies with immunohistochemical staining of HNSCC were considered. Data on TNM classification, tumor grade, disease free survival and 3- or 5-year overall survival rate were extracted.

Results

Thirty studies with 2102 patients met the inclusion criteria for the meta-analysis. Fifteen studies used anti-pan-CD44 antibody, 9 used anti-CD44-v6 antibody, 2 used anti-CD44-v3 and 2 used anti-CD44s antibody, 1 used anti-CD44-v9, and 1 used anti-CD44-v6,-v3 and -v4-5 simultaneously. The total percentage of CD44 expression was 57.8%, with 49.3% in oral cancer patients, 66.4% in pharynx and 54.7% in larynx cancer patients expressing CD44. No significant correlation between clinical features and CD44 expression was revealed for oral cancer patients, but CD44 was shown to be associated with advanced T categories (larynx: RR = 1.33, 95% CI 1.01-1.76; larynx & pharynx RR = 1.21, 95% CI 1.08-1.35), worse N categories (larynx: RR = 2.53, 95% CI 1.99-3.21; larynx & pharynx RR = 1.95, 95% CI 1.35-2.82), higher tumor grades (larynx & pharynx RR = 1.71, 95% CI 1.04-2.79) and 5-year OS rates (larynx: RR = 0.62, 95% CI 0.47-0.83; larynx & pharynx RR = 0.66, 95% CI 0.47-0.94) in patients with laryngeal and pharyngolaryngeal cancer. In stratified analysis, pan-CD44 and CD44-v6 expression were both correlated with 5-year OS rate of patients with laryngeal (CD44: RR = 0.66, 95% CI 0.46-0.95; CD44-v6 RR = 0.53, 95% CI 0.37-0.77) and pharyngolaryngeal cancer (CD44: RR = 0.56, 95% CI 0.34-0.93; CD44-v6 RR = 0.53, 95% CI 0.37-0.77).

Conclusions

Our analysis suggested that CD44 is related to worse T category, N category, tumor grade and prognosis, in pharyngeal and laryngeal cancer, but no clear association was revealed between CD44 expression and oral cancer.
Appendix
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Literature
1.
go back to reference Siegel R, Naishadham D, Jemal A: Cancer statistics, 2012. CA: Canc J Clinician. 2012, 62 (1): 10-29. 10.3322/caac.20138. Siegel R, Naishadham D, Jemal A: Cancer statistics, 2012. CA: Canc J Clinician. 2012, 62 (1): 10-29. 10.3322/caac.20138.
2.
go back to reference Kokko LL, Hurme S, Maula SM, Alanen K, Grenman R, Kinnunen I, Ventela S: Significance of site-specific prognosis of cancer stem cell marker CD44 in head and neck squamous-cell carcinoma. Oral Oncol. 2011, 47 (6): 510-516. 10.1016/j.oraloncology.2011.03.026.CrossRefPubMed Kokko LL, Hurme S, Maula SM, Alanen K, Grenman R, Kinnunen I, Ventela S: Significance of site-specific prognosis of cancer stem cell marker CD44 in head and neck squamous-cell carcinoma. Oral Oncol. 2011, 47 (6): 510-516. 10.1016/j.oraloncology.2011.03.026.CrossRefPubMed
3.
go back to reference Lobo NA, Shimono Y, Qian D, Clarke MF: The biology of cancer stem cells. Ann Rev Dev Biol. 2007, 23: 675-699. 10.1146/annurev.cellbio.22.010305.104154.CrossRef Lobo NA, Shimono Y, Qian D, Clarke MF: The biology of cancer stem cells. Ann Rev Dev Biol. 2007, 23: 675-699. 10.1146/annurev.cellbio.22.010305.104154.CrossRef
4.
go back to reference Bomken S, Fiser K, Heidenreich O, Vormoor J: Understanding the cancer stem cell. Br J Canc. 2010, 103 (4): 439-445. 10.1038/sj.bjc.6605821.CrossRef Bomken S, Fiser K, Heidenreich O, Vormoor J: Understanding the cancer stem cell. Br J Canc. 2010, 103 (4): 439-445. 10.1038/sj.bjc.6605821.CrossRef
5.
go back to reference Chiou SH, Yu CC, Huang CY, Lin SC, Liu CJ, Tsai TH, Chou SH, Chien CS, Ku HH, Lo JF: Positive correlations of Oct-4 and Nanog in oral cancer stem-like cells and high-grade oral squamous cell carcinoma. Clin Canc Res: Offic J Am Assoc Canc Res. 2008, 14 (13): 4085-4095. 10.1158/1078-0432.CCR-07-4404.CrossRef Chiou SH, Yu CC, Huang CY, Lin SC, Liu CJ, Tsai TH, Chou SH, Chien CS, Ku HH, Lo JF: Positive correlations of Oct-4 and Nanog in oral cancer stem-like cells and high-grade oral squamous cell carcinoma. Clin Canc Res: Offic J Am Assoc Canc Res. 2008, 14 (13): 4085-4095. 10.1158/1078-0432.CCR-07-4404.CrossRef
6.
go back to reference Yu CC, Chang YC: Enhancement of cancer stem-like and epithelial-mesenchymal transdifferentiation property in oral epithelial cells with long-term nicotine exposure: reversal by targeting SNAIL. Toxicol Appl Pharmacol. 2013, 266 (3): 459-469. 10.1016/j.taap.2012.11.023.CrossRefPubMed Yu CC, Chang YC: Enhancement of cancer stem-like and epithelial-mesenchymal transdifferentiation property in oral epithelial cells with long-term nicotine exposure: reversal by targeting SNAIL. Toxicol Appl Pharmacol. 2013, 266 (3): 459-469. 10.1016/j.taap.2012.11.023.CrossRefPubMed
7.
go back to reference Chen YS, Wu MJ, Huang CY, Lin SC, Chuang TH, Yu CC, Lo JF: CD133/Src axis mediates tumor initiating property and epithelial-mesenchymal transition of head and neck cancer. PloS One. 2011, 6 (11): e28053-10.1371/journal.pone.0028053.CrossRefPubMedPubMedCentral Chen YS, Wu MJ, Huang CY, Lin SC, Chuang TH, Yu CC, Lo JF: CD133/Src axis mediates tumor initiating property and epithelial-mesenchymal transition of head and neck cancer. PloS One. 2011, 6 (11): e28053-10.1371/journal.pone.0028053.CrossRefPubMedPubMedCentral
8.
go back to reference Trapasso S, Allegra E: Role of CD44 as a marker of cancer stem cells in head and neck cancer. Biol: Targets Ther. 2012, 6: 379-383. Trapasso S, Allegra E: Role of CD44 as a marker of cancer stem cells in head and neck cancer. Biol: Targets Ther. 2012, 6: 379-383.
9.
go back to reference Joshua B, Kaplan MJ, Doweck I, Pai R, Weissman IL, Prince ME, Ailles LE: Frequency of cells expressing CD44, a head and neck cancer stem cell marker: correlation with tumor aggressiveness. Head Neck. 2012, 34 (1): 42-49. 10.1002/hed.21699.CrossRefPubMed Joshua B, Kaplan MJ, Doweck I, Pai R, Weissman IL, Prince ME, Ailles LE: Frequency of cells expressing CD44, a head and neck cancer stem cell marker: correlation with tumor aggressiveness. Head Neck. 2012, 34 (1): 42-49. 10.1002/hed.21699.CrossRefPubMed
10.
go back to reference Chikamatsu K, Takahashi G, Sakakura K, Ferrone S, Masuyama K: Immunoregulatory properties of CD44+ cancer stem-like cells in squamous cell carcinoma of the head and neck. Head & neck. 2011, 33 (2): 208-215. 10.1002/hed.21420.CrossRef Chikamatsu K, Takahashi G, Sakakura K, Ferrone S, Masuyama K: Immunoregulatory properties of CD44+ cancer stem-like cells in squamous cell carcinoma of the head and neck. Head & neck. 2011, 33 (2): 208-215. 10.1002/hed.21420.CrossRef
11.
go back to reference van der Windt GJ, Schouten M, Zeerleder S, Florquin S, van der Poll T: CD44 is protective during hyperoxia-induced lung injury. Am J Respir Mol Biol. 2011, 44 (3): 377-383. 10.1165/rcmb.2010-0158OC.CrossRef van der Windt GJ, Schouten M, Zeerleder S, Florquin S, van der Poll T: CD44 is protective during hyperoxia-induced lung injury. Am J Respir Mol Biol. 2011, 44 (3): 377-383. 10.1165/rcmb.2010-0158OC.CrossRef
12.
go back to reference Zoller M: CD44: can a cancer-initiating cell profit from an abundantly expressed molecule?. Nat Rev Canc. 2011, 11 (4): 254-267. 10.1038/nrc3023.CrossRef Zoller M: CD44: can a cancer-initiating cell profit from an abundantly expressed molecule?. Nat Rev Canc. 2011, 11 (4): 254-267. 10.1038/nrc3023.CrossRef
13.
go back to reference Negi LM, Talegaonkar S, Jaggi M, Ahmad FJ, Iqbal Z, Khar RK: Role of CD44 in tumour progression and strategies for targeting. J Drug Target. 2012, 20 (7): 561-573. 10.3109/1061186X.2012.702767.CrossRefPubMed Negi LM, Talegaonkar S, Jaggi M, Ahmad FJ, Iqbal Z, Khar RK: Role of CD44 in tumour progression and strategies for targeting. J Drug Target. 2012, 20 (7): 561-573. 10.3109/1061186X.2012.702767.CrossRefPubMed
14.
go back to reference Aruffo A, Stamenkovic I, Melnick M, Underhill CB, Seed B: CD44 is the principal cell surface receptor for hyaluronate. Cell. 1990, 61 (7): 1303-1313. 10.1016/0092-8674(90)90694-A.CrossRefPubMed Aruffo A, Stamenkovic I, Melnick M, Underhill CB, Seed B: CD44 is the principal cell surface receptor for hyaluronate. Cell. 1990, 61 (7): 1303-1313. 10.1016/0092-8674(90)90694-A.CrossRefPubMed
15.
go back to reference Orian-Rousseau V: CD44, a therapeutic target for metastasising tumours. Eur J Canc. 2010, 46 (7): 1271-1277. 10.1016/j.ejca.2010.02.024.CrossRef Orian-Rousseau V: CD44, a therapeutic target for metastasising tumours. Eur J Canc. 2010, 46 (7): 1271-1277. 10.1016/j.ejca.2010.02.024.CrossRef
16.
go back to reference Wibulswas A, Croft D, Pitsillides AA, Bacarese-Hamilton I, McIntyre P, Genot E, Kramer IM: Influence of epitopes CD44v3 and CD44v6 in the invasive behavior of fibroblast-like synoviocytes derived from rheumatoid arthritic joints. Arthritis Rheum. 2002, 46 (8): 2059-2064. 10.1002/art.10421.CrossRefPubMed Wibulswas A, Croft D, Pitsillides AA, Bacarese-Hamilton I, McIntyre P, Genot E, Kramer IM: Influence of epitopes CD44v3 and CD44v6 in the invasive behavior of fibroblast-like synoviocytes derived from rheumatoid arthritic joints. Arthritis Rheum. 2002, 46 (8): 2059-2064. 10.1002/art.10421.CrossRefPubMed
17.
go back to reference Fehon RG, McClatchey AI, Bretscher A: Organizing the cell cortex: the role of ERM proteins. Nat Rev Mol Cell Biol. 2010, 11 (4): 276-287. 10.1038/nrm2866.CrossRefPubMedPubMedCentral Fehon RG, McClatchey AI, Bretscher A: Organizing the cell cortex: the role of ERM proteins. Nat Rev Mol Cell Biol. 2010, 11 (4): 276-287. 10.1038/nrm2866.CrossRefPubMedPubMedCentral
18.
go back to reference Lamontagne CA, Grandbois M: PKC-induced stiffening of hyaluronan/CD44 linkage; local force measurements on glioma cells. Exp Cell Res. 2008, 314 (2): 227-236. 10.1016/j.yexcr.2007.07.013.CrossRefPubMed Lamontagne CA, Grandbois M: PKC-induced stiffening of hyaluronan/CD44 linkage; local force measurements on glioma cells. Exp Cell Res. 2008, 314 (2): 227-236. 10.1016/j.yexcr.2007.07.013.CrossRefPubMed
19.
go back to reference Gonzalez-Moles MA, Bravo M, Ruiz-Avila I, Esteban F, Rodriguez-Archilla A, Gonzalez-Moles S, Arias B: Adhesion molecule CD44 as a prognostic factor in tongue cancer. Anticancer Res. 2003, 23 (6D): 5197-5202.PubMed Gonzalez-Moles MA, Bravo M, Ruiz-Avila I, Esteban F, Rodriguez-Archilla A, Gonzalez-Moles S, Arias B: Adhesion molecule CD44 as a prognostic factor in tongue cancer. Anticancer Res. 2003, 23 (6D): 5197-5202.PubMed
20.
go back to reference Esteban F, Bravo JJ, Gonzalez-Moles MA, Bravo M, Ruiz-Avila I, Gil-Montoya JA: Adhesion molecule CD44 as a prognostic factor in laryngeal cancer. Anticancer Res. 2005, 25 (2A): 1115-1121.PubMed Esteban F, Bravo JJ, Gonzalez-Moles MA, Bravo M, Ruiz-Avila I, Gil-Montoya JA: Adhesion molecule CD44 as a prognostic factor in laryngeal cancer. Anticancer Res. 2005, 25 (2A): 1115-1121.PubMed
21.
go back to reference Kosunen A, Pirinen R, Ropponen K, Pukkila M, Kellokoski J, Virtaniemi J, Sironen R, Juhola M, Kumpulainen E, Johansson R, et al: CD44 expression and its relationship with MMP-9, clinicopathological factors and survival in oral squamous cell carcinoma. Oral Oncol. 2007, 43 (1): 51-59. 10.1016/j.oraloncology.2006.01.003.CrossRefPubMed Kosunen A, Pirinen R, Ropponen K, Pukkila M, Kellokoski J, Virtaniemi J, Sironen R, Juhola M, Kumpulainen E, Johansson R, et al: CD44 expression and its relationship with MMP-9, clinicopathological factors and survival in oral squamous cell carcinoma. Oral Oncol. 2007, 43 (1): 51-59. 10.1016/j.oraloncology.2006.01.003.CrossRefPubMed
22.
go back to reference Wang SJ, Earle C, Wong G, Bourguignon LY: Role of hyaluronan synthase 2 to promote CD44-dependent oral cavity squamous cell carcinoma progression. Head Neck. 2013, 35 (4): 511-520. 10.1002/hed.22991.CrossRefPubMed Wang SJ, Earle C, Wong G, Bourguignon LY: Role of hyaluronan synthase 2 to promote CD44-dependent oral cavity squamous cell carcinoma progression. Head Neck. 2013, 35 (4): 511-520. 10.1002/hed.22991.CrossRefPubMed
23.
go back to reference Mori S, Nose M, Morikawa H, Sato A, Saito T, Song ST, Tanda N, Teshima T: A novel evaluation system of metastatic potential of oral squamous cell carcinoma according to the histopathological and histochemical grading. Oral Oncol. 1998, 34 (6): 549-557. 10.1016/S1368-8375(98)00048-7.CrossRefPubMed Mori S, Nose M, Morikawa H, Sato A, Saito T, Song ST, Tanda N, Teshima T: A novel evaluation system of metastatic potential of oral squamous cell carcinoma according to the histopathological and histochemical grading. Oral Oncol. 1998, 34 (6): 549-557. 10.1016/S1368-8375(98)00048-7.CrossRefPubMed
24.
go back to reference Wang S, Qiang Y, Xiao K, Jiang S, Chen E: Expression of CD44s and CD44v6 in laryngeal squamous cell carcinoma and their significance. J Clin Oto (China). 2000, 14 (10): 3- Wang S, Qiang Y, Xiao K, Jiang S, Chen E: Expression of CD44s and CD44v6 in laryngeal squamous cell carcinoma and their significance. J Clin Oto (China). 2000, 14 (10): 3-
25.
go back to reference Rong XZ, Zhi WS, Ming CX: The immunohistochemical expression of CD44s and CD44v6 in oral squamous cell carcinomas. J Oral Maxillofac Surg. 2001, 11 (3): 208-211. Rong XZ, Zhi WS, Ming CX: The immunohistochemical expression of CD44s and CD44v6 in oral squamous cell carcinomas. J Oral Maxillofac Surg. 2001, 11 (3): 208-211.
26.
go back to reference Zhao SW, Sun BC, He J, Ye Q, Lin SZ, Sun A: The expression of CD44 and its significance in human laryngeal carcinoma. J Clin Oto (China). 2003, 17 (3): 3- Zhao SW, Sun BC, He J, Ye Q, Lin SZ, Sun A: The expression of CD44 and its significance in human laryngeal carcinoma. J Clin Oto (China). 2003, 17 (3): 3-
27.
go back to reference Qiu XX, Huang JF, Zhang ZX, Da P, Zhou R: The expression of CD44 and its clinical significance in human laryngeal carcinoma. Med J Comm. 2006, 20 (6): 670-671. Qiu XX, Huang JF, Zhang ZX, Da P, Zhou R: The expression of CD44 and its clinical significance in human laryngeal carcinoma. Med J Comm. 2006, 20 (6): 670-671.
28.
go back to reference Lu S, Tian J, Lv Z, Wang H, Bai X, Liu W, Li J, Xu W: The probable role of tumor stem cells for lymph node metastasis in supraglottic carcinoma. Pathol Oncol Res: POR. 2011, 17 (1): 33-38. 10.1007/s12253-010-9271-9.CrossRefPubMed Lu S, Tian J, Lv Z, Wang H, Bai X, Liu W, Li J, Xu W: The probable role of tumor stem cells for lymph node metastasis in supraglottic carcinoma. Pathol Oncol Res: POR. 2011, 17 (1): 33-38. 10.1007/s12253-010-9271-9.CrossRefPubMed
29.
go back to reference Uwa N, Kataoka TR, Torii I, Sato A, Nishigami T, Song M, Daimon T, Saeki N, Sagawa K, Mouri T, et al: CD44 expression is related to poor prognosis of hypopharyngeal squamous cell carcinoma. Acta Oto-laryngologica. 2011, 131 (3): 323-329. 10.3109/00016489.2010.528792.CrossRefPubMed Uwa N, Kataoka TR, Torii I, Sato A, Nishigami T, Song M, Daimon T, Saeki N, Sagawa K, Mouri T, et al: CD44 expression is related to poor prognosis of hypopharyngeal squamous cell carcinoma. Acta Oto-laryngologica. 2011, 131 (3): 323-329. 10.3109/00016489.2010.528792.CrossRefPubMed
30.
go back to reference Yuce I, Bayram A, Cagli S, Canoz O, Bayram S, Guney E: The role of CD44 and matrix metalloproteinase-9 expression in predicting neck metastasis of supraglottic laryngeal carcinoma. Am J Otolaryngol. 2011, 32 (2): 141-146. 10.1016/j.amjoto.2010.01.001.CrossRefPubMed Yuce I, Bayram A, Cagli S, Canoz O, Bayram S, Guney E: The role of CD44 and matrix metalloproteinase-9 expression in predicting neck metastasis of supraglottic laryngeal carcinoma. Am J Otolaryngol. 2011, 32 (2): 141-146. 10.1016/j.amjoto.2010.01.001.CrossRefPubMed
31.
go back to reference Lindquist D, Ahrlund-Richter A, Tarjan M, Tot T, Dalianis T: Intense CD44 expression is a negative prognostic factor in tonsillar and base of tongue cancer. Anticancer Res. 2012, 32 (1): 153-161.PubMed Lindquist D, Ahrlund-Richter A, Tarjan M, Tot T, Dalianis T: Intense CD44 expression is a negative prognostic factor in tonsillar and base of tongue cancer. Anticancer Res. 2012, 32 (1): 153-161.PubMed
32.
go back to reference Wang M, Xing L, Zhang C: Study in the Expression of CD44 in Nasopharyngeal Neoplasms and the Clinical Relationship. Tianjin Med J. 2004, 32 (9): 3- Wang M, Xing L, Zhang C: Study in the Expression of CD44 in Nasopharyngeal Neoplasms and the Clinical Relationship. Tianjin Med J. 2004, 32 (9): 3-
33.
go back to reference Song X, Peng J, Cai X, Hou F, Lin Q: Expression of CD44v6 protein in laryngeal squamous cell carcinoma. Chin J Otorhinolaryngol-Skull Base Surg. 1999, 5 (2): 4- Song X, Peng J, Cai X, Hou F, Lin Q: Expression of CD44v6 protein in laryngeal squamous cell carcinoma. Chin J Otorhinolaryngol-Skull Base Surg. 1999, 5 (2): 4-
34.
go back to reference Xu YP, Zhao XQ, Sommer K, Moubayed P: Correlation of matrix metalloproteinase-2, -9, tissue inhibitor-1 of matrix metalloproteinase and CD44 variant 6 in head and neck cancer metastasis. J Zhejiang Univ (Sci). 2003, 4 (4): 491-501. 10.1631/jzus.2003.0491.CrossRef Xu YP, Zhao XQ, Sommer K, Moubayed P: Correlation of matrix metalloproteinase-2, -9, tissue inhibitor-1 of matrix metalloproteinase and CD44 variant 6 in head and neck cancer metastasis. J Zhejiang Univ (Sci). 2003, 4 (4): 491-501. 10.1631/jzus.2003.0491.CrossRef
35.
go back to reference Liqun X, Lijia S, Huiyong J, Liu Q: Tissue microarray assay of CD44v6 and PCNA expression for oral squamous cell carcinomas and precancerous lesions and it sclinical significance. J Jinan Univ. 2006, 27 (6): 8- Liqun X, Lijia S, Huiyong J, Liu Q: Tissue microarray assay of CD44v6 and PCNA expression for oral squamous cell carcinomas and precancerous lesions and it sclinical significance. J Jinan Univ. 2006, 27 (6): 8-
36.
go back to reference Staibano S, Merolla F, Testa D, Iovine R, Mascolo M, Guarino V, Castellone MD, Di Benedetto M, Galli V, Motta S, et al: OPN/CD44v6 overexpression in laryngeal dysplasia and correlation with clinical outcome. Brit J Canc. 2007, 97 (11): 1545-1551. 10.1038/sj.bjc.6604070.CrossRef Staibano S, Merolla F, Testa D, Iovine R, Mascolo M, Guarino V, Castellone MD, Di Benedetto M, Galli V, Motta S, et al: OPN/CD44v6 overexpression in laryngeal dysplasia and correlation with clinical outcome. Brit J Canc. 2007, 97 (11): 1545-1551. 10.1038/sj.bjc.6604070.CrossRef
37.
go back to reference Huang S, Luo W, Wu S, Wang W, Chen X: Expression of PCNA and CD44V6 in laryngeal carcinoma. J Guangdong Medical Coll. 2007, 2 (2): 3- Huang S, Luo W, Wu S, Wang W, Chen X: Expression of PCNA and CD44V6 in laryngeal carcinoma. J Guangdong Medical Coll. 2007, 2 (2): 3-
38.
go back to reference Lu J, Gao Y, Xiao Y, Jin D: Expression and clinical significance of CD44v6 in tissues of laryngeal and hypopharyngeal squamous cell carcinoma. J Harbin Med Univ. 2008, 42 (2): 5- Lu J, Gao Y, Xiao Y, Jin D: Expression and clinical significance of CD44v6 in tissues of laryngeal and hypopharyngeal squamous cell carcinoma. J Harbin Med Univ. 2008, 42 (2): 5-
39.
go back to reference Gao Y: The expression and its significance of CD44v6 in human laryngeal and hypopharyngeal squamous cell carcinoma. Chi Med Herald. 2009, 6 (1): 2- Gao Y: The expression and its significance of CD44v6 in human laryngeal and hypopharyngeal squamous cell carcinoma. Chi Med Herald. 2009, 6 (1): 2-
40.
go back to reference Guo X, Li F X, Feng S, Li X, Pan Z, Guan C, Wang Y, Yang H, Jiang X: Expression of gene BRMS1 and CD44v6 protein in supraglottic laryngeal carcinoma and its clinical significance. J Clin Otorhinolaryngol Head Neck Surg (China). 2009, 23 (6): 6- Guo X, Li F X, Feng S, Li X, Pan Z, Guan C, Wang Y, Yang H, Jiang X: Expression of gene BRMS1 and CD44v6 protein in supraglottic laryngeal carcinoma and its clinical significance. J Clin Otorhinolaryngol Head Neck Surg (China). 2009, 23 (6): 6-
41.
go back to reference Zhang R, Fan LV, Mu S, Xie X, Zhang M, Zhao C, Chang Q: Expression of CD44v6 in human oral squamous cell carcinoma. J Oral Sci Res. 2011, 27 (9): 4- Zhang R, Fan LV, Mu S, Xie X, Zhang M, Zhao C, Chang Q: Expression of CD44v6 in human oral squamous cell carcinoma. J Oral Sci Res. 2011, 27 (9): 4-
42.
go back to reference Masuda M, Kuratomi Y, Shiratsuchi H, Nakashima T, Naonobu K, Komiyama S: Decreased CD44H expression in early-stage tongue carcinoma associates with late nodal metastases following interstitial brachytherapy. Head Neck. 2000, 22 (7): 662-665. 10.1002/1097-0347(200010)22:7<662::AID-HED4>3.0.CO;2-O.CrossRefPubMed Masuda M, Kuratomi Y, Shiratsuchi H, Nakashima T, Naonobu K, Komiyama S: Decreased CD44H expression in early-stage tongue carcinoma associates with late nodal metastases following interstitial brachytherapy. Head Neck. 2000, 22 (7): 662-665. 10.1002/1097-0347(200010)22:7<662::AID-HED4>3.0.CO;2-O.CrossRefPubMed
43.
go back to reference Kawano T, Nakamura Y, Yanoma S, Kubota A, Furukawa M, Miyagi Y, Tsukuda M: Expression of E-cadherin, and CD44s and CD44v6 and its association with prognosis in head and neck cancer. Auris Nasus Larynx. 2004, 31 (1): 35-41. 10.1016/j.anl.2003.09.005.CrossRefPubMed Kawano T, Nakamura Y, Yanoma S, Kubota A, Furukawa M, Miyagi Y, Tsukuda M: Expression of E-cadherin, and CD44s and CD44v6 and its association with prognosis in head and neck cancer. Auris Nasus Larynx. 2004, 31 (1): 35-41. 10.1016/j.anl.2003.09.005.CrossRefPubMed
44.
go back to reference Bankfalvi A, Krassort M, Buchwalow IB, Vegh A, Felszeghy E, Piffko J: Gains and losses of adhesion molecules (CD44, E-cadherin, and beta-catenin) during oral carcinogenesis and tumour progression. J Pathol. 2002, 198 (3): 343-351. 10.1002/path.1204.CrossRefPubMed Bankfalvi A, Krassort M, Buchwalow IB, Vegh A, Felszeghy E, Piffko J: Gains and losses of adhesion molecules (CD44, E-cadherin, and beta-catenin) during oral carcinogenesis and tumour progression. J Pathol. 2002, 198 (3): 343-351. 10.1002/path.1204.CrossRefPubMed
45.
go back to reference Ma D, Yuan L, Zhao Y, Zhou X, Li C, Liu L: Relationship study between KAI1, CD44v3 expressions and laryngeal carcinoma. J Shandong Med Coll. 2009, 31 (2): 4- Ma D, Yuan L, Zhao Y, Zhou X, Li C, Liu L: Relationship study between KAI1, CD44v3 expressions and laryngeal carcinoma. J Shandong Med Coll. 2009, 31 (2): 4-
46.
go back to reference Ue T, Yokozaki H, Kagai K, Higashikawa K, Yasui W, Sugiyama M, Tahara E, Ishikawa T: Reduced expression of the CD44 variant exons in oral squamous cell carcinoma and its relationship to metastasis. J Oral Pathol Med: offi Publ Int Assoc Oral Pathol Am Acad Pathol. 1998, 27 (5): 197-201.CrossRef Ue T, Yokozaki H, Kagai K, Higashikawa K, Yasui W, Sugiyama M, Tahara E, Ishikawa T: Reduced expression of the CD44 variant exons in oral squamous cell carcinoma and its relationship to metastasis. J Oral Pathol Med: offi Publ Int Assoc Oral Pathol Am Acad Pathol. 1998, 27 (5): 197-201.CrossRef
47.
go back to reference Fonseca I, Pereira T, Rosa-Santos J, Soares J: Expression of CD44 isoforms in squamous cell carcinoma of the border of the tongue: A correlation with histological grade, pattern of stromal invasion, and cell differentiation. J Surg Oncol. 2001, 76 (2): 115-120. 10.1002/1096-9098(200102)76:2<115::AID-JSO1021>3.0.CO;2-9.CrossRefPubMed Fonseca I, Pereira T, Rosa-Santos J, Soares J: Expression of CD44 isoforms in squamous cell carcinoma of the border of the tongue: A correlation with histological grade, pattern of stromal invasion, and cell differentiation. J Surg Oncol. 2001, 76 (2): 115-120. 10.1002/1096-9098(200102)76:2<115::AID-JSO1021>3.0.CO;2-9.CrossRefPubMed
49.
go back to reference Biddle A, Gammon L, Fazil B, Mackenzie IC: CD44 staining of cancer stem-like cells is influenced by down-regulation of CD44 variant isoforms and up-regulation of the standard CD44 isoform in the population of cells that have undergone epithelial-to-mesenchymal transition. PloS one. 2013, 8 (2): e57314-10.1371/journal.pone.0057314.CrossRefPubMedPubMedCentral Biddle A, Gammon L, Fazil B, Mackenzie IC: CD44 staining of cancer stem-like cells is influenced by down-regulation of CD44 variant isoforms and up-regulation of the standard CD44 isoform in the population of cells that have undergone epithelial-to-mesenchymal transition. PloS one. 2013, 8 (2): e57314-10.1371/journal.pone.0057314.CrossRefPubMedPubMedCentral
50.
go back to reference Brown RL, Reinke LM, Damerow MS, Perez D, Chodosh LA, Yang J, Cheng C: CD44 splice isoform switching in human and mouse epithelium is essential for epithelial-mesenchymal transition and breast cancer progression. J Clin Investig. 2011, 121 (3): 1064-1074. 10.1172/JCI44540.CrossRefPubMedPubMedCentral Brown RL, Reinke LM, Damerow MS, Perez D, Chodosh LA, Yang J, Cheng C: CD44 splice isoform switching in human and mouse epithelium is essential for epithelial-mesenchymal transition and breast cancer progression. J Clin Investig. 2011, 121 (3): 1064-1074. 10.1172/JCI44540.CrossRefPubMedPubMedCentral
51.
go back to reference Krishnamachary B, Penet MF, Nimmagadda S, Mironchik Y, Raman V, Solaiyappan M, Semenza GL, Pomper MG, Bhujwalla ZM: Hypoxia regulates CD44 and its variant isoforms through HIF-1alpha in triple negative breast cancer. PloS One. 2012, 7 (8): e44078-10.1371/journal.pone.0044078.CrossRefPubMedPubMedCentral Krishnamachary B, Penet MF, Nimmagadda S, Mironchik Y, Raman V, Solaiyappan M, Semenza GL, Pomper MG, Bhujwalla ZM: Hypoxia regulates CD44 and its variant isoforms through HIF-1alpha in triple negative breast cancer. PloS One. 2012, 7 (8): e44078-10.1371/journal.pone.0044078.CrossRefPubMedPubMedCentral
52.
go back to reference Rodrigo JP, Dominguez F, Alvarez C, Herrero A, Suarez C: Expression of E-cadherin, CD44s, and CD44v6 in laryngeal and pharyngeal carcinomas. Am J Otolaryngol. 2003, 24 (6): 384-389. 10.1016/S0196-0709(03)00082-6.CrossRefPubMed Rodrigo JP, Dominguez F, Alvarez C, Herrero A, Suarez C: Expression of E-cadherin, CD44s, and CD44v6 in laryngeal and pharyngeal carcinomas. Am J Otolaryngol. 2003, 24 (6): 384-389. 10.1016/S0196-0709(03)00082-6.CrossRefPubMed
53.
go back to reference Piffko J, Bankfalvi A, Klauke K, Dreier R, Joos U, Bocker W, Schmid KW: Unaltered strong immunohistochemical expression of CD44-v6 and -v5 isoforms during development and progression of oral squamous cell carcinomas. J Oral Pathol Med: Offic Publ Int Ass Oral Pathologists Am Acad Oral Pathol. 1996, 25 (9): 502-506. 10.1111/j.1600-0714.1996.tb00305.x.CrossRef Piffko J, Bankfalvi A, Klauke K, Dreier R, Joos U, Bocker W, Schmid KW: Unaltered strong immunohistochemical expression of CD44-v6 and -v5 isoforms during development and progression of oral squamous cell carcinomas. J Oral Pathol Med: Offic Publ Int Ass Oral Pathologists Am Acad Oral Pathol. 1996, 25 (9): 502-506. 10.1111/j.1600-0714.1996.tb00305.x.CrossRef
54.
go back to reference Rajarajan A, Stokes A, Bloor BK, Ceder R, Desai H, Grafstrom RC, Odell EW: CD44 expression in oro-pharyngeal carcinoma tissues and cell lines. PloS One. 2012, 7 (1): e28776-10.1371/journal.pone.0028776.CrossRefPubMedPubMedCentral Rajarajan A, Stokes A, Bloor BK, Ceder R, Desai H, Grafstrom RC, Odell EW: CD44 expression in oro-pharyngeal carcinoma tissues and cell lines. PloS One. 2012, 7 (1): e28776-10.1371/journal.pone.0028776.CrossRefPubMedPubMedCentral
55.
go back to reference Lin JT, Chang TH, Chang CS, Wang WH, Su BW, Lee KD, Chang PJ: Prognostic value of pretreatment CD44 mRNA in peripheral blood of patients with locally advanced head and neck cancer. Oral Oncol. 2010, 46 (5): e29-e33. 10.1016/j.oraloncology.2010.02.011.CrossRefPubMed Lin JT, Chang TH, Chang CS, Wang WH, Su BW, Lee KD, Chang PJ: Prognostic value of pretreatment CD44 mRNA in peripheral blood of patients with locally advanced head and neck cancer. Oral Oncol. 2010, 46 (5): e29-e33. 10.1016/j.oraloncology.2010.02.011.CrossRefPubMed
56.
go back to reference Okamoto I, Tsuiki H, Kenyon LC, Godwin AK, Emlet DR, Holgado-Madruga M, Lanham IS, Joynes CJ, Vo KT, Guha A, et al: Proteolytic cleavage of the CD44 adhesion molecule in multiple human tumors. Am J Pathol. 2002, 160 (2): 441-447. 10.1016/S0002-9440(10)64863-8.CrossRefPubMedPubMedCentral Okamoto I, Tsuiki H, Kenyon LC, Godwin AK, Emlet DR, Holgado-Madruga M, Lanham IS, Joynes CJ, Vo KT, Guha A, et al: Proteolytic cleavage of the CD44 adhesion molecule in multiple human tumors. Am J Pathol. 2002, 160 (2): 441-447. 10.1016/S0002-9440(10)64863-8.CrossRefPubMedPubMedCentral
57.
go back to reference Stamenkovic I, Yu Q: Shedding light on proteolytic cleavage of CD44: the responsible sheddase and functional significance of shedding. J Investig Dermatol. 2009, 129 (6): 1321-1324. 10.1038/jid.2009.13.CrossRefPubMedPubMedCentral Stamenkovic I, Yu Q: Shedding light on proteolytic cleavage of CD44: the responsible sheddase and functional significance of shedding. J Investig Dermatol. 2009, 129 (6): 1321-1324. 10.1038/jid.2009.13.CrossRefPubMedPubMedCentral
58.
go back to reference Okamoto I, Kawano Y, Murakami D, Sasayama T, Araki N, Miki T, Wong AJ, Saya H: Proteolytic release of CD44 intracellular domain and its role in the CD44 signaling pathway. J Cell Biol. 2001, 155 (5): 755-762. 10.1083/jcb.200108159.CrossRefPubMedPubMedCentral Okamoto I, Kawano Y, Murakami D, Sasayama T, Araki N, Miki T, Wong AJ, Saya H: Proteolytic release of CD44 intracellular domain and its role in the CD44 signaling pathway. J Cell Biol. 2001, 155 (5): 755-762. 10.1083/jcb.200108159.CrossRefPubMedPubMedCentral
59.
go back to reference Lammich S, Okochi M, Takeda M, Kaether C, Capell A, Zimmer AK, Edbauer D, Walter J, Steiner H, Haass C: Presenilin-dependent intramembrane proteolysis of CD44 leads to the liberation of its intracellular domain and the secretion of an Abeta-like peptide. J Biol Chem. 2002, 277 (47): 44754-44759. 10.1074/jbc.M206872200.CrossRefPubMed Lammich S, Okochi M, Takeda M, Kaether C, Capell A, Zimmer AK, Edbauer D, Walter J, Steiner H, Haass C: Presenilin-dependent intramembrane proteolysis of CD44 leads to the liberation of its intracellular domain and the secretion of an Abeta-like peptide. J Biol Chem. 2002, 277 (47): 44754-44759. 10.1074/jbc.M206872200.CrossRefPubMed
60.
go back to reference Anderegg U, Eichenberg T, Parthaune T, Haiduk C, Saalbach A, Milkova L, Ludwig A, Grosche J, Averbeck M, Gebhardt C, et al: ADAM10 is the constitutive functional sheddase of CD44 in human melanoma cells. J Investig Dermatol. 2009, 129 (6): 1471-1482. 10.1038/jid.2008.323.CrossRefPubMed Anderegg U, Eichenberg T, Parthaune T, Haiduk C, Saalbach A, Milkova L, Ludwig A, Grosche J, Averbeck M, Gebhardt C, et al: ADAM10 is the constitutive functional sheddase of CD44 in human melanoma cells. J Investig Dermatol. 2009, 129 (6): 1471-1482. 10.1038/jid.2008.323.CrossRefPubMed
61.
go back to reference Takamune Y, Ikebe T, Nagano O, Nakayama H, Ota K, Obayashi T, Saya H, Shinohara M: ADAM-17 associated with CD44 cleavage and metastasis in oral squamous cell carcinoma. Virchows Archiv: Int J Pathol. 2007, 450 (2): 169-177. 10.1007/s00428-006-0350-y.CrossRef Takamune Y, Ikebe T, Nagano O, Nakayama H, Ota K, Obayashi T, Saya H, Shinohara M: ADAM-17 associated with CD44 cleavage and metastasis in oral squamous cell carcinoma. Virchows Archiv: Int J Pathol. 2007, 450 (2): 169-177. 10.1007/s00428-006-0350-y.CrossRef
62.
go back to reference Takamune Y, Ikebe T, Nagano O, Shinohara M: Involvement of NF-kappaB-mediated maturation of ADAM-17 in the invasion of oral squamous cell carcinoma. Biochem Biophys Res Commun. 2008, 365 (2): 393-398. 10.1016/j.bbrc.2007.11.010.CrossRefPubMed Takamune Y, Ikebe T, Nagano O, Shinohara M: Involvement of NF-kappaB-mediated maturation of ADAM-17 in the invasion of oral squamous cell carcinoma. Biochem Biophys Res Commun. 2008, 365 (2): 393-398. 10.1016/j.bbrc.2007.11.010.CrossRefPubMed
63.
go back to reference Ko SY, Lin SC, Wong YK, Liu CJ, Chang KW, Liu TY: Increase of disintergin metalloprotease 10 (ADAM10) expression in oral squamous cell carcinoma. Canc lett. 2007, 245 (1–2): 33-43.CrossRef Ko SY, Lin SC, Wong YK, Liu CJ, Chang KW, Liu TY: Increase of disintergin metalloprotease 10 (ADAM10) expression in oral squamous cell carcinoma. Canc lett. 2007, 245 (1–2): 33-43.CrossRef
64.
go back to reference Cromer A, Carles A, Millon R, Ganguli G, Chalmel F, Lemaire F, Young J, Dembele D, Thibault C, Muller D, et al: Identification of genes associated with tumorigenesis and metastatic potential of hypopharyngeal cancer by microarray analysis. Oncogene. 2004, 23 (14): 2484-2498. 10.1038/sj.onc.1207345.CrossRefPubMed Cromer A, Carles A, Millon R, Ganguli G, Chalmel F, Lemaire F, Young J, Dembele D, Thibault C, Muller D, et al: Identification of genes associated with tumorigenesis and metastatic potential of hypopharyngeal cancer by microarray analysis. Oncogene. 2004, 23 (14): 2484-2498. 10.1038/sj.onc.1207345.CrossRefPubMed
65.
go back to reference Oliveira DT, Odell EW: Expression of CD44 variant exons by normal oral epithelia. Oral Oncol. 1997, 33 (4): 260-262. 10.1016/S0964-1955(97)00081-X.CrossRefPubMed Oliveira DT, Odell EW: Expression of CD44 variant exons by normal oral epithelia. Oral Oncol. 1997, 33 (4): 260-262. 10.1016/S0964-1955(97)00081-X.CrossRefPubMed
66.
go back to reference Franzmann EJ, Reategui EP, Pedroso F, Pernas FG, Karakullukcu BM, Carraway KL, Hamilton K, Singal R, Goodwin WJ: Soluble CD44 is a potential marker for the early detection of head and neck cancer. Canc Epidemiol Biomark Preve: Publ Am Assoc Canc Res, Cosponsored Am Soc Prev Oncol. 2007, 16 (7): 1348-1355.CrossRef Franzmann EJ, Reategui EP, Pedroso F, Pernas FG, Karakullukcu BM, Carraway KL, Hamilton K, Singal R, Goodwin WJ: Soluble CD44 is a potential marker for the early detection of head and neck cancer. Canc Epidemiol Biomark Preve: Publ Am Assoc Canc Res, Cosponsored Am Soc Prev Oncol. 2007, 16 (7): 1348-1355.CrossRef
67.
go back to reference Pereira LH, Adebisi IN, Perez A, Wiebel M, Reis I, Duncan R, Goodwin WJ, Hu JJ, Lokeshwar VB, Franzmann EJ: Salivary markers and risk factor data: a multivariate modeling approach for head and neck squamous cell carcinoma detection. Canc Biomarkers : Dection A of Dis markers. 2011, 10 (5): 241-249. Pereira LH, Adebisi IN, Perez A, Wiebel M, Reis I, Duncan R, Goodwin WJ, Hu JJ, Lokeshwar VB, Franzmann EJ: Salivary markers and risk factor data: a multivariate modeling approach for head and neck squamous cell carcinoma detection. Canc Biomarkers : Dection A of Dis markers. 2011, 10 (5): 241-249.
68.
go back to reference Hsu KH, Tsai HW, Lin PW, Hsu YS, Shan YS, Lu PJ: Clinical implication and mitotic effect of CD44 cleavage in relation to osteopontin/CD44 interaction and dysregulated cell cycle protein in gastrointestinal stromal tumor. Ann Surg Oncol. 2010, 17 (8): 2199-2212. 10.1245/s10434-010-0927-1.CrossRefPubMed Hsu KH, Tsai HW, Lin PW, Hsu YS, Shan YS, Lu PJ: Clinical implication and mitotic effect of CD44 cleavage in relation to osteopontin/CD44 interaction and dysregulated cell cycle protein in gastrointestinal stromal tumor. Ann Surg Oncol. 2010, 17 (8): 2199-2212. 10.1245/s10434-010-0927-1.CrossRefPubMed
69.
go back to reference Margaritescu C, Pirici D, Simionescu C, Stepan A: The utility of CD44, CD117 and CD133 in identification of cancer stem cells (CSC) in oral squamous cell carcinomas (OSCC). Romanian journal of morphology and embryology = Revue roumaine de morphologie et embryologie . 2011, 52 (3 Suppl): 985-993.PubMed Margaritescu C, Pirici D, Simionescu C, Stepan A: The utility of CD44, CD117 and CD133 in identification of cancer stem cells (CSC) in oral squamous cell carcinomas (OSCC). Romanian journal of morphology and embryology = Revue roumaine de morphologie et embryologie . 2011, 52 (3 Suppl): 985-993.PubMed
70.
go back to reference Su J, Xu XH, Huang Q, Lu MQ, Li DJ, Xue F, Yi F, Ren JH, Wu YP: Identification of cancer stem-like CD44+ cells in human nasopharyngeal carcinoma cell line. Arch Med Res. 2011, 42 (1): 15-21. 10.1016/j.arcmed.2011.01.007.CrossRefPubMed Su J, Xu XH, Huang Q, Lu MQ, Li DJ, Xue F, Yi F, Ren JH, Wu YP: Identification of cancer stem-like CD44+ cells in human nasopharyngeal carcinoma cell line. Arch Med Res. 2011, 42 (1): 15-21. 10.1016/j.arcmed.2011.01.007.CrossRefPubMed
71.
go back to reference Lun SW, Cheung ST, Cheung PF, To KF, Woo JK, Choy KW, Chow C, Cheung CC, Chung GT, Cheng AS, et al: CD44+ cancer stem-like cells in EBV-associated nasopharyngeal carcinoma. PloS one. 2012, 7 (12): e52426-10.1371/journal.pone.0052426.CrossRefPubMedPubMedCentral Lun SW, Cheung ST, Cheung PF, To KF, Woo JK, Choy KW, Chow C, Cheung CC, Chung GT, Cheng AS, et al: CD44+ cancer stem-like cells in EBV-associated nasopharyngeal carcinoma. PloS one. 2012, 7 (12): e52426-10.1371/journal.pone.0052426.CrossRefPubMedPubMedCentral
72.
go back to reference Janisiewicz AM, Shin JH, Murillo-Sauca O, Kwok S, Le QT, Kong C, Kaplan MJ, Sunwoo JB: CD44(+) cells have cancer stem cell-like properties in nasopharyngeal carcinoma. Int Forum Allergy & Rhinology. 2012, 2 (6): 465-470. 10.1002/alr.21068.CrossRef Janisiewicz AM, Shin JH, Murillo-Sauca O, Kwok S, Le QT, Kong C, Kaplan MJ, Sunwoo JB: CD44(+) cells have cancer stem cell-like properties in nasopharyngeal carcinoma. Int Forum Allergy & Rhinology. 2012, 2 (6): 465-470. 10.1002/alr.21068.CrossRef
Metadata
Title
Significance of CD44 expression in head and neck cancer: a systemic review and meta-analysis
Authors
Jianqiang Chen
Jianding Zhou
Jie Lu
Hua Xiong
Xueli Shi
Liang Gong
Publication date
01-12-2014
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2014
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/1471-2407-14-15

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