BUBR1 expression in benign oral lesions and squamous cell carcinomas: Correlation with human papillomavirus

Oncology Reports

Volumn 23, Issue 4, 2010, Pages 1027-1036

  Lira, Régia C P ^a   Miranda, Fabiana A ^a   Guimarães, Márcia C M ^a   Simões, Renata T ^c   Donadi, Eduardo A ^a   Soares, Christiane P ^b   Soares, Edson Garcia ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^c Santa Casa de Belo Horizonte   (Brazil)

Author keywords

BUBR1; HPV; Oral squamous cell carcinoma

Indexed keywords

ANTINEOPLASTIC AGENT; BUB1 RELATED PROTEIN; VIRUS DNA;

ADULT; ARTICLE; BENIGN TUMOR; CANCER CHEMOTHERAPY; CANCER INVASION; CANCER RADIOTHERAPY; CLINICAL FEATURE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN PAPILLOMAVIRUS TYPE 18; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LYMPH NODE; MAJOR CLINICAL STUDY; MALE; METASTASIS; MOUTH CARCINOMA; MOUTH LESION; ORAL BIOPSY; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; SQUAMOUS CELL CARCINOMA; VIRUS INFECTION;

CARCINOMA IN SITU; CARCINOMA, SQUAMOUS CELL; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MIDDLE AGED; MOUTH NEOPLASMS; PAPILLOMAVIRUS INFECTIONS; PREVALENCE; PROTEIN-SERINE-THREONINE KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 77949426000     PISSN: 1021335X     EISSN: 17912431     Source Type: Journal    
DOI: 10.3892/or_00000729     Document Type: Article

References (61)

1. Arduino PG, Carrozzo M, Chiecchio A, Broccoletti R, Tirone F, Borra E, Bertolusso G and Gandolfo S: Clinical and histopathologic independent prognostic factors in oral squamous cell carcinoma: a retrospective study of 334 cases. J Oral Maxillofac Surg 66: 1570-1579, 2008.
2. Scully C and Bagan J: Oral squamous cell carcinoma: overview of current understanding of aetiopathogenesis and clinical implications. Oral diseases: doi:10.1111/j.1601-0825. 2009.01563.x, 2009.
3. Ferlay J, Bray F, Pisani P and Parkin DM: GLOBOCAN 2002: Cancer Incidence, Mortality and Prevalence Worldwide. IARCPress, Lyon, 2004.
4. INCA, Instituto Nacional de Câncer: Estimativas 2008: Incidência de Câncer no Brasil. Rio de Janeiro, p94, 2007.
5. Goldenberg D, Brooksby C and Hollenbeak CS: Age as a determinant of outcomes for patients with oral cancer. Oral Oncol 45: e57-e61, 2009.
6. Massano J, Regateiro FS, Januario G and Ferreira A: Oral squamous cell carcinoma: review of prognostic and predictive factors. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 102: 67-76, 2006.
7. Andrews E, Seaman WT and Webster-Cyriaque J: Oropharyngeal carcinoma in non-smokers and non-drinkers: a role for HPV. Oral Oncol 45: 486-491, 2009.
8. Llamas-Martinez S, Esparza-Gomez G, Campo-Trapero J, Cancela-Rodriguez P, Bascones-Martinez A, Moreno-Lopez LA, Garcia-Nunez JA and Cerero-Lapiedra R: Genotypic determination by PCR-RFLP of human papillomavirus in normal oral mucosa, oral leukoplakia and oral squamous cell carcinoma samples in Madrid (Spain). Anticancer Res 28: 3733-3741, 2008.
9. Wunsch-Filho V: The epidemiology of oral and pharynx cancer in Brazil. Oral Oncol 38: 737-746, 2002.
10. Termine N, Panzarella V, Falaschini S, Russo A, Matranga D, Lo Muzio L and Campisi G: HPV in oral squamous cell carcinoma vs head and neck squamous cell carcinoma biopsies: a meta-analysis (1988-2007). Ann Oncol 19: 1681-1690, 2008.
11. Herrero R, Castellsague X, Pawlita M, Lissowska J, Kee F, Balaram P, Rajkumar T, Sridhar H, Rose B, Pintos J, Fernandez L, Idris A, Sanchez MJ, Nieto A, Talamini R, Tavani A, Bosch FX, Reidel U, Snijders PJ, Meijer CJ, Viscidi R, Munoz N and Franceschi S: Human papillomavirus and oral cancer: the International Agency for Research on Cancer multicenter study. J Natl Cancer Inst 95: 1772-1783, 2003.
12. Furrer VE, Benitez MB, Furnes M, Lanfranchi HE and Modesti NM: Biopsy vs. superficial scraping: detection of human papillomavirus 6, 11, 16, and 18 in potentially malignant and malignant oral lesions. J Oral Pathol Med 35: 338-344, 2006.
13. Bouda M, Gorgoulis VG, Kastrinakis NG, Giannoudis A, Tsoli E, Danassi-Afentaki D, Foukas P, Kyroudi A, Laskaris G, Herrington CS and Kittas C: 'High risk' HPV types are frequently detected in potentially malignant and malignant oral lesions, but not in normal oral mucosa. Mod Pathol 13: 644-653, 2000.
14. Giovannelli L, Campisi G, Lama A, Giambalvo O, Osborn J, Margiotta V and Ammatuna P: Human papillomavirus DNA in oral mucosal lesions. J Infec Dis 185: 833-836, 2002.
15. Luo CW, Roan CH and Liu CJ: Human papillomaviruses in oral squamous cell carcinoma and pre-cancerous lesions detected by PCR-based gene-chip array. Int J Oral Maxillofac Surg 36: 153-158, 2007.
16. Sugiyama M, Bhawal UK, Dohmen T, Ono S, Miyauchi M and Ishikawa T: Detection of human papillomavirus-16 and HPV-18 DNA in normal, dysplastic, and malignant oral epithelium. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 95: 594-600, 2003.
17. Lavia P, Mileo AM, Giordano A and Paggi MG: Emerging roles of DNA tumor viruses in cell proliferation: new insights into genomic instability. Oncogene 22: 6508-6516, 2003.
18. Reshmi SC, Saunders WS, Kudla DM, Ragin CR and Gollin SM: Chromosomal instability and marker chromosome evolution in oral squamous cell carcinoma. Genes Chromosomes Cancer 41: 38-46, 2004.
19. Saunders WS, Shuster M, Huang X, Gharaibeh B, Enyenihi AH, Petersen I and Gollin SM: Chromosomal instability and cytoskeletal defects in oral cancer cells. Proc Natl Acad Sci USA 97: 303-308, 2000.
20. Reing JE, Gollin SM and Saunders WS: The occurrence of chromosome segregational defects is an intrinsic and heritable property of oral squamous cell carcinoma cell lines. Cancer Genet Cytogenet 150: 57-61, 2004.
21. Rao CV, Yamada HY, Yao Y and Dai W: Enhanced genomic instabilities caused by deregulated microtubule dynamics and chromosome segregation: a perspective from genetic studies in mice. Carcinogenesis (In press).
22. Kim S, Park SY, Yong H, Famulski JK, Chae S, Lee JH, Kang CM, Saya H, Chan GK and Cho H: HBV X protein targets hBubR1, which induces dysregulation of the mitotic checkpoint. Oncogene 27: 3457-3464, 2008.
23. Yamamoto Y, Matsuyama H, Chochi Y, Okuda M, Kawauchi S, Inoue R, Furuya T, Oga A, Naito K and Sasaki K: Overexpression of BUBR1 is associated with chromosomal instability in bladder cancer. Cancer Genet Cytogenet 174: 42-47, 2007.
24. Shigeishi H, Yoneda S, Taki M, Nobumori T, Ohta K, Higashikawa K, Yasui W and Kamata N: Correlation of human Bub1 expression with tumor-proliferating activity in salivary gland tumors. Oncol Rep 15: 933-938, 2006.
25. Yuan B, Xu Y, Woo JH, Wang Y, Bae YK, Yoon DS, Wersto RP, Tully E, Wilsbach K and Gabrielson E: Increased expression of mitotic checkpoint genes in breast cancer cells with chromosomal instability. Clin Cancer Res 12: 405-410, 2006.
26. Grabsch H, Takeno S, Parsons WJ, Pomjanski N, Boecking A, Gabbert HE and Mueller W: Overexpression of the mitotic checkpoint genes BUB1, BUBR1, and BUB3 in gastric cancerassociation with tumour cell proliferation. J Pathol 200: 16-22, 2003.
27. Ying B and Wold WS: Adenovirus ADP protein (E3-11.6K), which is required for efficient cell lysis and virus release, interacts with human MAD2B. Virology 313: 224-234, 2003.
28. Burum-Auensen E, De Angelis PM, Schjolberg AR, Kravik KL, Aure M and Clausen OP: Subcellular localization of the spindle proteins Aurora A, Mad2, and BUBR1 assessed by immunohistochemistry. J Histochem Cytochem 55: 477-486, 2007.
29. Bettini JS, Soares EG, Duarte G, Simoes RT and Simoes AL: PCR diagnosis of HPV in cervical biopsies of CIN and invasive neoplasia formerly diagnosed as HPV negative. Acta Cytol 47: 545-549, 2003.
30. De Roda Husman AM, Walboomers JM, van den Brule AJ, Meijer CJ and Snijders PJ: The use of general primers GP5 and GP6 elongated at their 3' ends with adjacent highly conserved sequences improves human papillomavirus detection by PCR. J Gen Virol 76 (Pt 4): 1057-1062, 1995.
31. Saiki RK, Scharf S, Faloona F, Mullis KB, Horn GT, Erlich HA and Arnheim N: Enzymatic amplification of beta-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. Science (New York) 230: 1350-1354, 1985.
32. Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, Snijders PJ, Peto J, Meijer CJ and Munoz N: Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 189: 12-19, 1999.
33. Sanguinetti CJ, Dias Neto E and Simpson AJ: Rapid silver staining and recovery of PCR products separated on polyacrylamide gels. Biotechniques 17: 914-921, 1994.
34. Choi KK, Kim MJ, Yun PY, Lee JH, Moon HS, Lee TR and Myoung H: Independent prognostic factors of 861 cases of oral squamous cell carcinoma in Korean adults. Oral Oncol 42: 208-217, 2006.
35. Carvalho AL, Singh B, Spiro RH, Kowalski LP and Shah JP: Cancer of the oral cavity: a comparison between institutions in a developing and a developed nation. Head Neck 26: 31-38, 2004.
36. Ghoshal S, Mallick I, Panda N and Sharma SC: Carcinoma of the buccal mucosa: analysis of clinical presentation, outcome and prognostic factors. Oral Oncol 42: 533-539, 2006.
37. Nemes JA, Redl P, Boda R, Kiss C and Marton IJ: Oral cancer report from Northeastern Hungary. Pathol Oncol Res 14: 85-92, 2008.
38. Rodriguez T, Altieri A, Chatenoud L, Gallus S, Bosetti C, Negri E, Franceschi S, Levi F, Talamini R and La Vecchia C: Risk factors for oral and pharyngeal cancer in young adults. Oral Oncol 40: 207-213, 2004.
39. Simonato LE, Garcia JF, Sundefeld ML, Mattar NJ, Veronese LA and Miyahara GI: Detection of HPV in mouth floor squamous cell carcinoma and its correlation with clinicopathologic variables, risk factors and survival. J Oral Pathol Med 37: 593-598, 2008.
40. Nair S and Pillai MR: Human papillomavirus and disease mechanisms: relevance to oral and cervical cancers. Oral Dis 11: 350-359, 2005.
41. Zhang ZY, Sdek P, Cao J and Chen WT: Human papillomavirus type 16 and 18 DNA in oral squamous cell carcinoma and normal mucosa. Int J Oral Maxillofacial Surg 33: 71-74, 2004.
42. Ostwald C, Rutsatz K, Schweder J, Schmidt W, Gundlach K and Barten M: Human papillomavirus 6/11, 16 and 18 in oral carcinomas and benign oral lesions. Med Microbiol Immunol 192: 145-148, 2003.
43. Ritchie JM, Smith EM, Summersgill KF, Hoffman HT, Wang D, Klussmann JP, Turek LP and Haugen TH: Human papillomavirus infection as a prognostic factor in carcinomas of the oral cavity and oropharynx. Int J Cancer 104: 336-344, 2003.
44. Oliveira MC, Soares RC, Pinto LP, Souza LB, Medeiros SR and Costa Ade L: High-risk human papillomavirus (HPV) is not associated with p53 and bcl-2 expression in oral squamous cell carcinomas. Auris Nasus Larynx 36: 450-456, 2009.
45. Anaya-Saavedra G, Ramirez-Amador V, Irigoyen-Camacho ME, Garcia-Cuellar CM, Guido-Jimenez M, Mendez-Martinez R and Garcia-Carranca A: High association of human papillomavirus infection with oral cancer: a case-control study. Arch Med Res 39: 189-197, 2008.
46. Soares RC, Oliveira MC, de Souza LB, Costa Ade L and Pinto LP: Detection of HPV DNA and immunohistochemical expression of cell cycle proteins in oral carcinoma in a population of Brazilian patients. J Appl Oral Sci 16: 340-344, 2008.
47. Nagpal JK, Patnaik S and Das BR: Prevalence of high-risk human papilloma virus types and its association with P53 codon 72 polymorphism in tobacco addicted oral squamous cell carcinoma (OSCC) patients of Eastern India. Int J Cancer 97: 649-653, 2002.
48. De Reynies A, Assie G, Rickman DS, Tissier F, Groussin L, Rene-Corail F, Dousset B, Bertagna X, Clauser E and Bertherat J: Gene expression profiling reveals a new classification of adrenocortical tumors and identifies molecular predictors of malignancy and survival. J Clin Oncol 27: 1108-1115, 2009.
49. Haruki N, Saito H, Harano T, Nomoto S, Takahashi T, Osada H, Fujii Y and Takahashi T: Molecular analysis of the mitotic checkpoint genes BUB1, BUBR1 and BUB3 in human lung cancers. Cancer Lett 162: 201-205, 2001.
50. Ouyang B, Knauf JA, Ain K, Nacev B and Fagin JA: Mechanisms of aneuploidy in thyroid cancer cell lines and tissues: evidence for mitotic checkpoint dysfunction without mutations in BUB1 and BUBR1. Clin Endocrinol 56: 341-350, 2002.
51. Reis RM, Nakamura M, Masuoka J, Watanabe T, Colella S, Yonekawa Y, Kleihues P and Ohgaki H: Mutation analysis of hBUB1, hBUBR1 and hBUB3 genes in glioblastomas. Acta Neuropathol 101: 297-304, 2001.
52. Saeki A, Tamura S, Ito N, Kiso S, Matsuda Y, Yabuuchi I, Kawata S and Matsuzawa Y: Frequent impairment of the spindle assembly checkpoint in hepatocellular carcinoma. Cancer 94: 2047-2054, 2002.
53. Burum-Auensen E, Deangelis PM, Schjolberg AR, Roislien J, Andersen SN and Clausen OP: Spindle proteins Aurora A and BUB1B, but not Mad2, are aberrantly expressed in dysplastic mucosa of patients with longstanding ulcerative colitis. J Clin Pathol 60: 1403-1408, 2007.
54. Cotsiki M, Lock RL, Cheng Y, Williams GL, Zhao J, Perera D, Freire R, Entwistle A, Golemis EA, Roberts TM, Jat PS and Gjoerup OV: Simian virus 40 large T antigen targets the spindle assembly checkpoint protein Bub1. Proc Natl Acad Sci USA 101: 947-952, 2004.
55. Jin DY, Spencer F and Jeang KT: Human T cell leukemia virus type 1 oncoprotein Tax targets the human mitotic checkpoint protein MAD1. Cell 93: 81-91, 1998.
56. Pan SH, Tai CC, Lin CS, Hsu WB, Chou SF, Lai CC, Chen JY, Tien HF, Lee FY and Wang WB: Epstein-Barr virus nuclear antigen 2 disrupts mitotic checkpoint and causes chromosomal instability. Carcinogenesis 30: 366-375, 2009.
57. Chien CY, Su CY, Fang FM, Huang HY, Chuang HC, Chen CM and Huang CC: Lower prevalence but favorable survival for human papillomavirus-related squamous cell carcinoma of tonsil in Taiwan. Oral Oncol 44: 174-179, 2008.
58. Armas GL, Su CY, Huang CC, Fang FM, Chen CM and Chien CY: The impact of virus in N3 node dissection for head and neck cancer. Eur Arch Otorhinolaryngol 265: 1379-1384, 2008.
59. Ha GH, Baek KH, Kim HS, Jeong SJ, Kim CM, McKeon F and Lee CW: p53 activation in response to mitotic spindle damage requires signaling via BubR1-mediated phosphorylation. Cancer Res 67: 7155-7164, 2007.
60. Mammas IN, Sourvinos G, Giannoudis A and Spandidos DA: Human papilloma virus (HPV) and host cellular interactions. Pathol Oncol Res 14: 345-354, 2008.
61. Narisawa-Saito M and Kiyono T: Basic mechanisms of highrisk human papillomavirus-induced carcinogenesis: roles of E6 and E7 proteins. Cancer Sci 98: 1505-1511, 2007.