Prevalence of human cytomegalovirus, polyomaviruses, and oncogenic viruses in glioblastoma among Japanese subjects

Infectious Agents and Cancer

Masanori Daibata¹  Tetsuya Ueba³  Makoto Hiroi⁴  Masanao Murakami¹  Sena Hosokawa¹  Toshio Yawata³  Ayuko Taniguchi²  Yumiko Hashida¹ 

[1] Department of Microbiology and Infection, Kochi Medical School, Kochi University, Nankoku, Kochi 783-8505, Japan;Division of Hematology and Respiratory Medicine, Kochi Medical School, Kochi University, Nankoku, Kochi 783-8505, Japan;Department of Neurosurgery, Kochi Medical School, Kochi University, Nankoku, Kochi 783-8505, Japan;Laboratory of Diagnostic Pathology, Kochi Medical School, Kochi University, Nankoku, Kochi 783-8505, Japan

关键词: Epidemiology;    Glioblastoma;    Polyomaviruses;    HPV;    HCMV;    Oncogenic viruses;   

Others  :  1133736
DOI  :  10.1186/1750-9378-10-3

 received in 2014-10-29, accepted in 2015-01-21,  发布年份 2015

【 摘 要 】

Background

The association between human cytomegalovirus (HCMV) and glioblastoma multiforme (GBM) is becoming a new concept. However, information on the geographic variability of HCMV prevalence in GBM remains scarce. Moreover, the potential roles of various viruses, such as polyomaviruses and oncogenic viruses, in gliomagenesis remain unclear. Our aim was to investigate the prevalence of HCMV in GBM among Japanese patients. Furthermore, this was the first study that evaluated infection with four new human polyomaviruses in GBMs. This study also provided the first data on the detection of human papillomavirus (HPV) in GBM in the Eastern world.

Methods

We measured the number of various viral genomes in GBM samples from 39 Japanese patients using real-time quantitative PCR. The tested viruses included HCMV, Merkel cell polyomavirus, human polyomavirus (HPyV) 6, HPyV7, HPyV9, Epstein–Barr virus, human herpesvirus 8, and HPV. Our quantitative PCR analysis led to the detection of eight copies of the HCMV DNA mixed with DNA extracted from 10⁴ HCMV-negative cells. The presence of HCMV and HPV genomes was also assessed by nested PCR. Immunohistochemical study was also carried out to detect HPV-derived protein in GBM tissues.

Results

The viral DNAs were not detectable, with the exception of HPV, which was present in eight out of 39 (21%) GBMs. All HPV-positive cases harbored high-risk-type HPV (HPV16 and HPV18). Moreover, the HPV major capsid protein was detected in GBM tumor cells.

Conclusions

In contrast with previous reports from Caucasian patients, we did not obtain direct evidence in support of the association between HCMV and GBM. However, high-risk-type HPV infection may play a potential etiological role in gliomagenesis in a subset of patients. These findings should prompt further worldwide epidemiological studies aimed at defining the pathogenicity of virus-associated GBM.

【 授权许可】

   
2015 Hashida et al.; licensee BioMed Central.

【 图 表 】

Figure 1.

【 参考文献 】

• [1]White MK, Pagano JS, Khalili K: Viruses and human cancers: a long road of discovery of molecular paradigms. Clin Microbiol Rev 2014, 27:463-81.
• [2]Cobbs CS, Harkins L, Samanta M, Gillespie GY, Bharara S, King PH, et al.: Human cytomegalovirus infection and expression in human malignant glioma. Cancer Res 2002, 62:3347-50.
• [3]Mitchell DA, Xie W, Schmittling R, Learn C, Friedman A, McLendon RE, et al.: Sensitive detection of human cytomegalovirus in tumors and peripheral blood of patients diagnosed with glioblastoma. Neuro Oncol 2008, 10:10-8.
• [4]Scheurer ME, Bondy ML, Aldape KD, Albrecht T, El-Zein R: Detection of human cytomegalovirus in different histological types of gliomas. Acta Neuropathol 2008, 116:79-86.
• [5]Lucas KG, Bao L, Bruggeman R, Dunham K, Specht C: The detection of CMV pp 65 and IE1 in glioblastoma multiforme. J Neurooncol 2011, 103:231-8.
• [6]dos Santos CJ, Stangherlin LM, Figueiredo EG, Corrêa C, Teixeira MJ, da Silva MC: High prevalence of HCMV and viral load in tumor tissues and peripheral blood of glioblastoma multiforme patients. J Med Virol 2014, 86:1953-61.
• [7]Rahbar A, Orrego A, Peredo I, Dzabic M, Wolmer-Solberg N, Strååt K, et al.: Human cytomegalovirus infection levels in glioblastoma multiforme are of prognostic value for survival. J Clin Virol 2013, 57:36-42.
• [8]Rahbar A, Stragliotto G, Orrego A, Peredo I, Taher C, Willems J, et al.: Low levels of human cytomegalovirus infection in glioblastoma multiforme associates with patient survival: a case-control study. Herpesviridae 2012, 3:3. BioMed Central Full Text
• [9]Stragliotto G, Rahbar A, Solberg NW, Lilja A, Taher C, Orrego A, et al.: Effects of valganciclovir as an add-on therapy in patients with cytomegalovirus-positive glioblastoma: a randomized, double-blind, hypothesis-generating study. Int J Cancer 2013, 133:1204-13.
• [10]Söderberg-Nauclér C, Rahbar A, Stragliotto G: Survival in patients with glioblastoma receiving valganciclovir. N Engl J Med 2013, 369:985-6.
• [11]Lau SK, Chen YY, Chen WG, Diamond DJ, Mamelak AN, Zaia JA, et al.: Lack of association of cytomegalovirus with human brain tumors. Mod Pathol 2005, 18:838-43.
• [12]Sabatier J, Uro-Coste E, Pommepuy I, Labrousse F, Allart S, Trémoulet M, et al.: Detection of human cytomegalovirus genome and gene products in central nervous system tumours. Br J Cancer 2005, 92:747-50.
• [13]Poltermann S, Schlehofer B, Steindorf K, Schnitzler P, Geletneky K, Schlehofer JR: Lack of association of herpesviruses with brain tumors. J Neurovirol 2006, 12:90-9.
• [14]Cimino PJ, Zhao G, Wang D, Sehn JK, Lewis JS Jr, Duncavage EJ: Detection of viral pathogens in high grade gliomas from unmapped next-generation sequencing data. Exp Mol Pathol 2014, 96:310-5.
• [15]Yamashita Y, Ito Y, Isomura H, Takemura N, Okamoto A, Motomura K, et al.: Lack of presence of the human cytomegalovirus in human glioblastoma. Mod Pathol 2014, 27:922-9.
• [16]Mazzoni E, Gerosa M, Lupidi F, Corallini A, Taronna AP, D’Agostino A, et al.: Significant prevalence of antibodies reacting with simian virus 40 mimotopes in sera from patients affected by glioblastoma multiforme. Neuro Oncol 2014, 16:513-9.
• [17]Piña-Oviedo S, De León-Bojorge B, Cuesta-Mejías T, White MK, Ortiz-Hidalgo C, Khalili K, et al.: Glioblastoma multiforme with small cell neuronal-like component: association with human neurotropic JC virus. Acta Neuropathol 2006, 111:388-96.
• [18]Feng H, Shuda M, Chang Y, Moore PS: Clonal integration of a polyomavirus in human Merkel cell carcinoma. Science 2008, 319:1096-100.
• [19]Imajoh M, Hashida Y, Nemoto Y, Oguri H, Maeda N, Furihata M, et al.: Detection of Merkel cell polyomavirus in cervical squamous cell carcinomas and adenocarcinomas from Japanese patients. Virol J 2012, 9:154. BioMed Central Full Text
• [20]Hashida Y, Imajoh M, Nemoto Y, Kamioka M, Taniguchi A, Taguchi T, et al.: Detection of Merkel cell polyomavirus with a tumour-specific signature in non-small cell lung cancer. Br J Cancer 2013, 108:629-37.
• [21]Isomura H, Stinski MF: The human cytomegalovirus major immediate-early enhancer determines the efficiency of immediate-early gene transcription and viral replication in permissive cells at low multiplicity of infection. J Virol 2003, 77:3602-14.
• [22]Wada K, Kubota N, Ito Y, Yagasaki H, Kato K, Yoshikawa T, et al.: Simultaneous quantification of Epstein-Barr virus, cytomegalovirus, and human herpesvirus 6 DNA in samples from transplant recipients by multiplex real-time PCR assay. J Clin Microbiol 2007, 45:1426-32.
• [23]Tafvizi F, Fard ZT: Detection of human cytomegalovirus in patients with colorectal cancer by nested-PCR. Asian Pac J Cancer Prev 2014, 15:1453-7.
• [24]Vidone M, Alessandrini F, Marucci G, Farnedi A, de Biase D, Ricceri F, et al.: Evidence of association of human papillomavirus with prognosis worsening in glioblastoma multiforme. Neuro Oncol 2014, 16:298-302.
• [25]de Roda Husman AM, Walboomers JM, van den Brule AJ, Meijer CJ, 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 1995, 76:1057-62.
• [26]Gravitt PE, Peyton CL, Alessi TQ, Wheeler CM, Coutlée F, Hildesheim A, et al.: Improved amplification of genital human papillomaviruses. J Clin Microbiol 2000, 38:357-61.
• [27]Iwasaki T, Sata T, Sugase M, Sato Y, Kurata T, Suzuki K, et al.: Detection of capsid antigen of human papillomavirus (HPV) in benign lesions of female genital tract using anti-HPV monoclonal antibody. J Pathol 1992, 168:293-300.
• [28]Morshed K: Association between human papillomavirus infection and laryngeal squamous cell carcinoma. J Med Virol 2010, 82:1017-23.
• [29]Dziurzynski K, Chang SM, Heimberger AB, Kalejta RF, McGregor Dallas SR, Smit M, et al.: Consensus on the role of human cytomegalovirus in glioblastoma. Neuro Oncol 2012, 14:246-55.
• [30]Wöhrer A, Waldhör T, Heinzl H, Hackl M, Feichtinger J, Gruber-Mösenbacher U, et al.: The Austrian brain tumour registry: a cooperative way to establish a population-based brain tumour registry. J Neurooncol 2009, 95:401-11.
• [31]Stiller CA, Nectoux J: International incidence of childhood brain and spinal tumours. Int J Epidemiol 1994, 23:458-64.
• [32]Fan KJ, Pezeshkpour GH: Ethnic distribution of primary central nervous system tumors in Washington, DC, 1971 to 1985. J Natl Med Assoc 1992, 84:858-63.
• [33]Pignatelli S, Dal Monte P, Rossini G, Landini MP: Genetic polymorphisms among human cytomegalovirus (HCMV) wild-type strains. Rev Med Virol 2004, 14:383-410.
• [34]Navarro D, Paz P, Tugizov S, Topp K, La Vail J, Pereira L: Glycoprotein B of human cytomegalovirus promotes virion penetration into cells, transmission of infection from cell to cell, and fusion of infected cells. Virology 1993, 197:143-58.
• [35]Pignatelli S, Dal Monte P, Rossini G, Chou S, Gojobori T, Hanada K, et al.: Human cytomegalovirus glycoprotein N (gpUL73-gN) genomic variants: identification of a novel subgroup, geographical distribution and evidence of positive selective pressure. J Gen Virol 2003, 84:647-55.
• [36]Pagano JS, Blaser M, Buendia MA, Damania B, Khalili K, Raab-Traub N, et al.: Infectious agents and cancer: criteria for a causal relation. Semin Cancer Biol 2004, 14:453-71.
• [37]Martini F, Corallini A, Balatti V, Sabbioni S, Pancaldi C, Tognon M: Simian virus 40 in humans. Infect Agent Cancer 2007, 2:13. BioMed Central Full Text
• [38]Moens U, Van Ghelue M, Song X, Ehlers B: Serological cross-reactivity between human polyomaviruses. Rev Med Virol 2013, 23:250-64.
• [39]Moens U, Van Ghelue M, Ehlers B: Are human polyomaviruses co-factors for cancers induced by other oncoviruses? Rev Med Virol 2014, 24:343-60.
• [40]Bhatia K, Goedert JJ, Modali R, Preiss L, Ayers LW: Merkel cell carcinoma subgroups by Merkel cell polyomavirus DNA relative abundance and oncogene expression. Int J Cancer 2010, 126:2240-6.
• [41]Duncavage EJ, Pfeifer JD: Human polyomaviruses 6 and 7 are not detectable in Merkel cell polyomavirus-negative Merkel cell carcinoma. J Cutan Pathol 2011, 38:790-6.
• [42]Imajoh M, Hashida Y, Taniguchi A, Kamioka M, Daibata M: Novel human polyomaviruses, Merkel cell polyomavirus and human polyomavirus 9, in Japanese chronic lymphocytic leukemia cases. J Hematol Oncol 2012, 5:25. BioMed Central Full Text
• [43]Sato T, Fujieda M, Tanaka E, Miyamura M, Chikamoto H, Hisano M, et al.: Monitoring of Epstein-Barr virus load and antibody in pediatric renal transplant patients. Pediatr Int 2008, 50:454-8.
• [44]Yu D, Chen Y, Wu S, Wang B, Tang YW, Li L: Simultaneous detection and differentiation of human papillomavirus genotypes 6, 11, 16 and 18 by AllGlo quadruplex quantitative PCR. PLoS One 2012, 7:e48972.
• [45]Hiatt KM, Nelson AM, Lichy JH, Fanburg-Smith JC: Classic Kaposi Sarcoma in the United States over the last two decades: a clinicopathologic and molecular study of 438 non-HIV-related Kaposi Sarcoma patients with comparison to HIV-related Kaposi Sarcoma. Mod Pathol 2008, 21:572-82.