Oropharyngeal malignant epithelial cell, lymphocyte and macrophage CD44 surface receptors for hyaluronate are expressed in sustained EBV infection: Immunohistochemical data and EBV DNA tissue indices

Pathology Research and Practice

Volumn 208, Issue 9, 2012, Pages 518-526

  Groma, Valerija ^a   Kazanceva, Anna ^b   Nora Krukle, Zaiga ^a   Murovska, Modra ^a  

^a RIGA STRADINS UNIVERSITY   (Latvia)

^b RIGA EAST UNIVERSITY HOSPITAL   (Latvia)

Author keywords

CD44 surface receptor; EBV; Immunohistochemistry; Nasopharyngeal carcinoma; Oral squamous cell carcinoma

Indexed keywords

CD19 ANTIGEN; CD68 ANTIGEN; CELL SURFACE RECEPTOR; HERMES ANTIGEN; HYALURONIC ACID; LATENT MEMBRANE PROTEIN; PROTEIN S 100; UNCLASSIFIED DRUG; VIRUS DNA; VIRUS PROTEIN;

ADULT; AGED; ANTIGEN EXPRESSION; ARTICLE; B LYMPHOCYTE; BLOOD SAMPLING; CANCER CELL; CELL LABELING; CHEEK MUCOSA; CLINICAL ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; DISEASE COURSE; EPITHELIUM CELL; EPSTEIN BARR VIRUS INFECTION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; LYMPHOCYTE; LYMPHOEPITHELIOMA; MACROPHAGE; MALE; MOUTH SQUAMOUS CELL CARCINOMA; NASOPHARYNX CARCINOMA; OROPHARYNX CANCER; PROTEIN EXPRESSION; SALIVARY GLAND;

ADULT; AGED; ANTIGENS, CD44; CARCINOMA, SQUAMOUS CELL; DENDRITIC CELLS; DNA, VIRAL; EPITHELIAL CELLS; EPSTEIN-BARR VIRUS INFECTIONS; FEMALE; HERPESVIRUS 4, HUMAN; HUMANS; HYALURONIC ACID; LYMPHOCYTES; MACROPHAGES; MALE; MIDDLE AGED; MOUTH MUCOSA; MOUTH NEOPLASMS; NASOPHARYNGEAL NEOPLASMS; SALIVARY GLANDS; SIGNAL TRANSDUCTION; TUMOR MARKERS, BIOLOGICAL; VIRAL LOAD; VIRAL MATRIX PROTEINS;

EID: 84865297440     PISSN: 03440338     EISSN: 16180631     Source Type: Journal    
DOI: 10.1016/j.prp.2012.05.017     Document Type: Article

References (65)

1. Abdulmajeed A., Stein S., Chan A., et al. Immunoexpression of putative cancer stem cell markers in oral epithelial dysplasia and squamous cell carcinoma. Third World Congr. Intern. Acad. Oral Oncol. 2011, 46S. (Abstract).
2. Anagnostopoulos I., Herbst H., Niedobitek G., et al. Demonstration of monoclonal EBV genomes in Hodgkin's disease and Ki-1 positive anaplastic large cell lymphoma by combined Southern blot and in situ hybridization. Blood 1989, 74:810-816.
3. Assimakopoulos D., Kolettas E., Patrikakos G., et al. The role of CD44 in the development and prognosis of head and neck squamous cell carcinomas. Histol. Histopathol. 2002, 17:1269-1281.
4. Bagan J., Jimenez Y., Murillo J., et al. Epstein-Barr virus in oral proliferative verrucous leukoplakia and squamous cell carcinoma: a preliminary study. Med. Oral Patol. Oral Cir. Bucal. 2008, 13:110-113.
5. Bánkfalvi A., Kraßort M., Buchwalow I.B., et al. Gains and losses of adhesion molecules (CD44, E-cadherin, and β-catenin) during oral carcinogenesis and tumour progression. J. Pathol. 2002, 198:343-351.
6. Benders A.A., Tang W., Jaap M., et al. Epstein-Barr virus latent membrane protein 1 is not associated with vessel density nor with hypoxia inducible factor 1 alpha expression in nasopharyngeal carcinoma tissue. Head Neck Pathol. 2009, 3:276-282.
7. Biddle A., Liang X., Gammon L., Fazil B., Harper L.J., Emich H., Costea D.E., Mackenzie I.C. Cancer stem cells in squamous cell carcinoma switch between two distinct phenotypes that are preferentially migratory or proliferative. Cancer Res. 2011, 71:5317-5326.
8. Carinci F., Stabellini G., Calvitti M., et al. CD44 as prognostic factor in oral and oropharyngeal squamous cell carcinoma. J. Craniofac. Surg. 2002, 13:85-89.
9. Cruz I., Van Der Brule A.J.C., Steenbergen R.D.N., et al. Prevalence of Epstein-Barr virus in oral squamous cell carcinomas, premalignant lesions and normal mucosa. A study using the polymerase chain reaction. Eur. J. Cancer B: Oral Oncol. 1997, 33:182-188.
10. Cummings B.J., Clark R.M. Squamous cell carcinoma of the oral cavity. J. Otolaryngol. 1982, 11:359-364.
11. D'Costa J., Saranath D., Sanghvi V., et al. Epstein-Barr virus in tobacco-induced oral cancer and oral lesions in patients from India. J. Oral Pathol. Med. 1998, 27:78-82.
12. Franchi A., Moroni M., Paglierani M., et al. Expression of CD44 standard and variant isoforms in parotid gland and parotid gland tumours. J. Oral Pathol. Med. 2001, 30:564-568.
13. Georgolios A., Batistatou A., Charalabopoulos A., et al. The role of CD44 adhesion molecule in oral cavity cancer. Exp. Oncol. 2006, 28:94-98.
14. Goldenberg D., Benoit N.E., Begum S., et al. Epstein-Barr virus in head and neck cancer assessed by quantitative polymerase chain reaction. Laryngoscope 2004, 114:1027-1031.
15. González-Moles M., Gutiérrez J., Ruiz I., et al. Epstein-Barr virus and oral squamous cell carcinoma in patients without HIV infection: viral detection by polymerase chain reaction. Microbios 1998, 96:23-31.
16. Gonzalez-Moles M., Gutiérrez J., Rodriguez M., et al. Epstein-Barr virus latent membrane protein-1 (LMP-1) expression in oral squamous cell carcinoma. Laryngoscope 2002, 112:482-487.
17. Gonzalez-Moles M., Bravo M., Ruiz-Avila I., et al. Adhesion molecule CD44 as a prognostic factor in tongue cancer. Anticancer Res. 2003, 23:5197-5202.
18. Gonzalez-Moles M., Bravo M., Ruiz-Avila I., et al. Adhesion molecule CD44 expression in non-tumour epithelium adjacent to tongue cancer. Oral Oncol. 2004, 40:281-286.
19. González X., Correnti M., Rivera H., et al. Epstein-Barr virus detection and latent membrane protein 1 in oral hairy leukoplakia in HIV+ Venezuelan patients. Med. Oral Patol. Oral Cir. Bucal. 2010, 15:297-302.
20. Gourzones C., Gelin A., Bombik I., et al. Extra-cellular release and blood diffusion of BART viral micro-RNAs produced by EBV-infected nasopharyngeal carcinoma cells. Virol. J. 2010, 7:271-282.
21. Grinstein S., Preciado M.V., Gattuso P., et al. Demonstration of Epstein-Barr virus in carcinomas of various sites. Cancer Res. 2002, 62:4876-4878.
22. Gulley M.L. Molecular Diagnosis of Epstein-Barr virus-related diseases. J. Mol. Diag. 2001, 3:1-10.
23. Hausen H., Schulte-Holthausen H., Klein G., et al. EBV DNA in biopsies of Burkitt tumours and anaplastic carcinoma of the nasopharynx. Nature 1970, 228:1056-1058.
24. Horiuchi K., Mishima K., Ichijima K., et al. Epstein-Barr virus in the proliferative disease of squamous epithelium in the oral cavity. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Oral Radiol. Endod. 1995, 79:57-63.
25. Houali K., Wang X., Shimizu Y., et al. New diagnostic marker for secreted Epstein-Barr virus encoded LMP1 and BARF1 oncoproteins in the serum and saliva of patients with nasopharyngeal carcinoma. Clin. Cancer Res. 2007, 13:4993-5000.
26. Jiang R., Gu X., Nathan C.O., et al. Laser-capture microdissection of oropharyngeal epithelium indicates restriction of Epstein-Barr virus receptor/CD21 mRNA to tonsil epithelial cells. J. Oral Pathol. Med. 2008, 37:626-633.
27. Keryer-Bibens C., Pioche-Durieu C., Villemant C., et al. Exosomes released by EBV-infected nasopharyngeal carcinoma cells convey the viral latent membrane protein 1 and the immunomodulatory protein galectin 9. BMC Cancer 2006, 6:283-290.
28. Kis A., Fehér E., Gáll T., et al. Epstein-Barr virus prevalence in oral squamous cell cancer and in potentially malignant oral disorders in an eastern Hungarian population. Eur. J. Oral Sci. 2009, 117:536-540.
29. Kobayashi I., Shima K., Saito I., et al. Prevalence of Epstein-Barr virus in oral squamous cell carcinoma. J. Pathol. 1999, 189:34-39.
30. Kokko L.L., Hurme S., Maula S.M., et al. Significance of site-specific prognosis of cancer stem cell marker CD44 in head and neck squamous-cell carcinoma. Oral Oncol. 2011, 47:510-516.
31. Landgren M., Kyllerman M., Bergström T., et al. Diagnosis of Epstein-Barr virus-induced central nervous system infections by DNA amplification from cerebrospinal fluid. Ann. Neurol. 1994, 35:631-635.
32. Lawrence S., Rickinsos B. Role of Epstein-Barr virus in the pathogenesis of nasopharyngeal carcinoma. Nat. Rev. Cancer 2004, 4:757-768.
33. Le A., Saverin M., Hand A.R. Distribution of dendritic cells in normal human salivary glands. Acta Histochem. Cytochem. 2011, 44:165-173.
34. Lo K.W., To K.F., Huang D.P. Focus on nasopharyngeal carcinoma. Cancer Cell 2004, 5:423-428.
35. Mao E.J., Smith C.J. Detection of Epstein-Barr virus (EBV) DNA by the polymerase chain reaction (PCR) in oral smears from healthy individuals and patients with squamous cell carcinoma. J. Oral Pathol. Med. 1993, 22:12-17.
36. Margaritescu Cl., Pirici D., Simionescu C., et al. The utility of CD44, CD117 and CD133 in identification of cancer stem cell (CSC) in oral squamous cell carcinomas (OSCC). Romanian J. Morphol. Embriol. 2011, 52:985-993.
37. Marhaba R., Zöller M. CD44 in cancer progression: adhesion, migration and growth regulation. J. Mol. Histol. 2004, 35:211-231.
38. Mesquita R.A., Araujo V.C., Paes R.A., et al. Immunohistochemical analysis for CD21, CD35, caldesmon and S100 protein on dendritic cells types in oral lymphomas. J. Appl. Oral Sci. 2009, 17:248-253.
39. Murray P.G., Young L.S., Rowe M., et al. Immunohistochemical demonstration of the Epstein-Barr virus encoded latent membrane protein in paraffin sections of Hodgkin's disease. J. Pathol. 1992, 166:1-5.
40. Nagano O., Saya H. Mechanism and biological significance of CD44 cleavage. Cancer Sci. 2004, 95:930-935.
41. Negishi A., Mogi K., Yamaguchi T. Histopathological study on the distribution of Langerhans Cells in Oral Mucosa. Kitakanto Med. J. 2007, 57:307-310.
42. Oliveira L.R., Oliveira-Costa J.P., Araujo I.M., et al. Cancer stem cell immunophenotypes in oral squamous cell carcinoma. J. Oral Pathol. Med. 2011, 40:135-142.
43. özer E., Kuyucuo-Lu F. Correlation of CD44 expression with prognostic factors in oral squamous carcinoma. Eastern J. Med. 1999, 4:61-64.
44. Prince M.E., Sivanandan R., Kaczorowski A., 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, 104:973-978.
45. Rajarajan A., Stokes A., Bloor B.K., et al. CD44 expression in oro-pharyngeal carcinoma tissues and cell lines. PLoS One 2012, 7:e28776.
46. Reategui E.P., de Mayolo A.A., Das P.M., et al. Characterization of CD44v3-containing isoforms in head and neck cancer. Cancer Biol. Ther. 2006, 5:1163-1168.
47. Richard V., Pillai M.R. The stem cell code in oral tumorigenesis: 'the cancer stem cell shift hypothesis'. Biochim. Biophys. Acta 2010, 1806:146-162.
48. Sand L.P., Jalouli J., Larsson P.A., et al. Prevalence of Epstein-Barr virus in oral squamous cell carcinoma, oral lichen planus, and normal oral mucosa. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 2002, 93:586-592.
49. Sato S., Miyauchi M., Takekoshi T., et al. Reduced expression of CD44 variant 9 is related to lymph node metastasis and poor survival in squamous cell carcinoma of tongue. Oral Oncol. 2000, 36:545-549.
50. Scully C., Bagan J.V. Oral squamous cell carcinoma: overview of current understanding of aetiopathogenesis and clinical implication. Oral Diseases 2009, 15:388-399.
51. Simionescu C., Margaritescu Cl., Surpateanu M., et al. The study of E-cadherine and CD44 immunoexpression in oral squamous cell carcinoma. Romanian J. Morphol. Embriol. 2008, 49:189-193.
52. Shamaa A.A., Zyada M.M., Wagner M., et al. The significance of Epstein-Barr virus (EBV) & DNA Topoisomerase II alpha (DNA-Topo II alpha) immnoreactivity in normal oral mucosa, oral epithelial dysplasia (OED) and oral squamous cell carcinoma (OSCC). Diagnostic Pathol. 2008, 3:45-57.
53. Shannon-Lowe C., Rowe M. Epstein-Barr virus infection of polarized epithelial cells via the basolateral surface by memory B cell-mediated transfer infection. PLoS. Pathog. 2011, 7:e1001338.
54. Shimakage M., Horii K., Tempaku A., et al. Association of Epstein-Barr virus with oral cancers. Hum. Pathol. 2002, 33:608-614.
55. Sterz C.M., Kulle C., Dakic B., 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, 46:116-122.
56. Taheri-Kadkhoda Z., Magnusson B., Svensson M., et al. Expression modes and clinical manifestations of latent membrane protein 1, Ki-67, cyclin-B1, and epidermal growth factor receptor in nonendemic nasopharyngeal carcinoma. Head Neck 2009, 31:482-549.
57. Tugizov S., Herrera R., Veluppillai P., et al. Epstein-Barr virus (EBV)-infected monocytes facilitate dissemination of EBV within the oral mucosal epithelium. J. Virol. 2007, 81:5484-5496.
58. Van Weering D.H., Baas P.D., Bos J.L. A PCR-based method for the analysis of human CD44 splice products. PCR Methods Appl. 1993, 3:100-106.
59. Walling D.M., Flaitz C.M., Nichols C.M., et al. Persistent productive Epstein-Barr virus replication in normal epithelial cells in vivo. J. Infect. Dis. 2001, 184:1499-1507.
60. Walling D.M., Ray A.J., Nichols J.E., et al. Epstein-Barr virus infection of langerhans cell precursors as a mechanism of oral epithelial entry, persistence, and reactivation. J. Virol. 2007, 81:7249-7268.
61. Wang S.J., Wreesmann V.B., Bourguignon L.Y. Association of CD44 V3-containing isoforms with tumor cell growth, migration, matrix metalloproteinase expression, and lymph node metastasis in head and neck cancer. Head Neck 2007, 29:550-558.
62. Wang S.J., Wong G., De Heer A.M., et al. CD44 variant isoforms in head and neck squamous cell carcinoma progression. Laryngoscope 2009, 119:1518-1530.
63. Wang S.J., Bourguignon L.Y. Role of hyaluronan-mediated CD44 signaling in head and neck squamous cell carcinoma progression and chemoresistance. Am. J. Pathol. 2011, 178:956-963.
64. Young L.S., Rickinson A.B. Epstein-Barr virus: 40 years on. Nat. Rev. Cancer 2004, 4:757-768.
65. Zheng H., Li L.L., Hu D.S., et al. Role of Epstein-Barr virus encoded latent membrane protein 1 in the carcinogenesis of nasopharyngeal carcinoma. Cell. Mol. Immunol. 2007, 4:185-196.