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Polyomavirus Jcpyv Infrequently Detectable in Adenoid Cystic Carcinoma of the Oral Cavity and the Airways

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Polyomavirus Jcpyv Infrequently Detectable in Adenoid Cystic Carcinoma of the Oral Cavity and the Airways Virchows Archiv (2019) 475:609–616 https://doi.org/10.1007/s00428-019-02617-6 ORIGINAL ARTICLE Polyomavirus JCPyV infrequently detectable in adenoid cystic carcinoma of the oral cavity and the airways Hanna Hämetoja1,2 & Jaana Hagström2,3 & Caj Haglund3,4 & Leif Bäck5 & Antti Mäkitie5,6,7 & Stina Syrjänen1 Received: 29 March 2019 /Revised: 13 June 2019 /Accepted: 25 June 2019 /Published online: 1 July 2019 # The Author(s) 2019 Abstract Our objective was to assess the presence of three polyomaviruses, namely SV40, JCPyV, and BKPyV, and human papilloma- viruses (HPV) in adenoid cystic carcinomas (ACC) of the minor salivary glands (MiSG) in the head and neck region. The study comprised 68 MiSG ACC patients operated during 1974–2012 at the Helsinki University Hospital (Helsinki, Finland). Medical records and 68 histological samples were reviewed. Polyomaviruses were detected with quantitative PCR and the DNA-positive samples were further analyzed for the presence of viral tumor T antigen (T-ag) with immunohistochemistry. HPV genotyping was performed with a Multiplex HPV Genotyping Kit. Only JCPyV DNAwas found in ACC samples, being present in 7 (10.3%) out of the 68 samples. The viral load of JCPyV was low varying between 1 to 226 copies/μg DNA. The JCPyV-positive samples originated from trachea (two samples), paranasal sinuses (one), and oral cavity (two). Additionally, JCPyV positivity was found in one lung metastasis of a tracheal tumor and one local disease failure of an oral cavity tumor. Three JCPyV DNA-positive samples showed weak nuclear staining for large T-ag. In conclusion, only JCPyV but not SV40, BKPyV, or HPV was found in ACC from the upper and lower airways. JCPyV copy numbers were low which might support its role as a “hit and run agent” in ACC carcinogenesis. Keywords Adenoid cystic carcinoma . Polyomavirus . Oral cancer . Oncogenes . Human papillomavirus Introduction Adenoid cystic carcinoma (ACC) is a rare malignancy of glan- dular structures, which most commonly (70%) appears in sal- * Hanna Hämetoja [email protected] ivary glands [1]. Minor glands (MiSGs) are involved more often than major glands (MaSGs) [1, 2]. Etiopathogenesis for ACC as well as for many other salivary gland tumors is still 1 Department of Oral Pathology, University of Turku and Turku University Hospital, Turku, Finland unknown. In ACC, genetic studies have found MYB/NFIB translocations and this fusion oncogene is overexpressed [3]. 2 Department of Pathology, University of Helsinki and Helsinki University Hospital, Helsinki, Finland In addition, studies have provided evidence for Notch-pathway alterations in 11 to 29% of patients [4]. As the pathogenesis of 3 Research Programs Unit, Translational Cancer Biology Program, University of Helsinki, Helsinki, Finland ACC remains unknown, even viral background should be con- sidered. Distinguished viral etiological factors among head and 4 Department of Surgery, University of Helsinki and Helsinki University Hospital, Helsinki, Finland neck cancers are Epstein-Barr virus (EBV) in nasopharyngeal carcinoma and human papilloma virus (HPV) 16 in oropha- 5 Department of Otorhinolaryngology - Head and Neck Surgery, University of Helsinki and Helsinki University Hospital, ryngeal squamous cell carcinoma [5, 6]. Helsinki, Finland Furthermore, head and neck cancer studies have gained 6 Division of Ear, Nose and Throat Diseases, Department of Clinical new knowledge on polyomaviruses (HPyVs) and their coin- Sciences, Intervention and Technology, Karolinska Institutet and fection with other viruses [7–11]. A recent study on oncogenic Karolinska University Hospital, Stockholm, Sweden DNA viruses in salivary gland tumors increases the interest on 7 Research Programme in Systems Oncology, Faculty of Medicine, possible role of HPyVs in the pathogenesis of salivary gland University of Helsinki, Helsinki, Finland tumors [12]. 610 Virchows Arch (2019) 475:609–616 Currently, 13 human HPyVs have been identified [13, 14]. Table 1 Characterization of the 68 patients with an adenoid cystic Among them, Merkel cell polyomavirus (MCPyV), BK poly- carcinoma of minor salivary and mucous glands omavirus (BKPyV), and JC polyomavirus (JCPyV) have been N % associated with human cancers [13]. MCPyV is classified as a grade 2A carcinogen (probable carcinogen) by IARC while Sex BKPyV and JCPyV are grade 2B carcinogens (possibly carci- Male 29 42.6 nogenic to humans) [13]. Simian vacuolating virus 40 (SV40) Female 39 57.4 has an ability to cause cancer in animal models but clinical Female/male ratio 1.35 consequences to humans are controversial although SV40 con- Median age, years (range) 58 (24–88) taminated polio vaccine was used during the years 1955–1963 Tumor site [13, 15, 16]. HPyVs are small non-enveloped viruses Oral cavity 41 60.3 consisting of circular double-stranded DNA genome (5.2 kb) Paranasal cavities 6 8.8 that has two transcriptional units, early and late region [13]. Trachea 6 8.8 The former encodes large T antigen (T-ag) (90–100 kDA nu- Nasopharynx 5 7.4 clear protein) and the latter, small T-ag (17–22 kDa) viral cap- Oropharynx 3 4.4 sidproteinsVP1,VP2,andVP3[13]. Large T-ag acts similarly Ear 4 5.9 as many other known oncoproteins of tumor viruses by inter- Larynx 2 2.9 fering with tumor suppressor proteins pRb and p53 [8, 11]. Esophagus 1 1.5 Roughly 80–90% of the population are latent carriers of Tclass JCPyV and BKPyV and primary infections are usually mani- T1 18 26.5 fested subclinically during early childhood [11, 15, 17]. In T2 12 17.6 healthy individuals, secretion of JCPyV and BKPyV might T3 6 8.8 occasionally be detected in urine and saliva [18]. In the case T4 22 32.4 of immunocompromised patients, however, polyomavirus re- N/A 4 5.9 activation may cause severe complications. These include N class polyomavirus-associated nephropathy due to BKPyV reactiva- N0 54 79.4 tion in kidney transplant recipients and JCPyV-related progres- N1 1 1.5 sive multifocal leukoencephalopathy [15]. HPVs are widely N2 3 4.4 studied and the causality of HPV type 16 and squamous cell N/A 4 5.9 carcinoma (SCC) has been classified as grade 1 (IARC vol Stage 100, 2009) [19]. The etiological link between HPV and SCC I1623.5 has specially been shown in cancers of uterine cervix and oro- II 12 17.6 pharynx [6, 20]. HPV has also been detected in salivary gland III 7 10.3 ACC although the connection between HPV and ACC does IV 23 33.8 not seem to be strong [21–23]. According to the “hit and run N/A 4 5.9 theory,” different viruses may contribute to tumorigenesis, for instance, polyomaviruses could augment the oncogenic prop- N/A, not available erties of HPV during their co-infections [8]. TNM and stage classification for 62 tumors (trachea excluded) Altogether, studies on HPyVs, HPVs, and salivary gland tumors are sparse and as far as we know, there are no previous Department of Otorhinolaryngology – Head and Neck publications on the presence of polyomaviruses in ACC. The Surgery, Helsinki University Hospital (Helsinki, Finland) be- aim of this study was to assess the prevalence of the three tween 1974 and 2012. The referral area for this tertiary care polyomaviruses, SV40, JCPyV, and BKPyV, and HPV in center currently is 1.6 M. The clinical data of this series have ACC samples of minor salivary and mucous glands. been characterized in our previous study [24] and the Ki67 immunostaining results collected from the same hospital data were now added. The tumor samples were re-evaluated and Materials and methods validated according to the diagnostic criteria by the classifica- tion of the World Health Organization classification (both Patient and tumor characteristics 2005 and 2017) [3, 25]. The present tumor, node, metastasis (TNM) classification does not include tracheal tumors, and Table 1 summarizes the demographic data and tumor charac- thus, the TNM classes on six (8.8%) tracheal ACCs are not teristics in a retrospective series on 68 patients with MiSG given. Additionally, in four cases (5.9%), the TNM class could ACC. The patients were diagnosed and treated at the not be defined. Virchows Arch (2019) 475:609–616 611 Altogether, 68 paraffin blocks of tumor samples were avail- Quantitative detection of SV40, JCPyV, and BKPyV able. Samples included 48 samples from primary tumors and 20 disease failures from 15 patients; altogether, we were able Presence of SV40, JCPyV and BKPyV DNA in the samples to study samples from 53 patients. In addition, ten normal was detected by quantitative polymerase chain reaction salivary gland tissue samples from the same patients were (qPCR) (Roche, Light Cycler 96) targeting their oncogenic used as normal controls. large T-ag as described by McNees and coworkers, with slight The study comprised MiSG and mucous excreting gland modification [15]. RNase P was used as a reference gene samples from the head and neck area including trachea and (TaqMan® Copy Number Reference Assay RNase, Applied esophagus. These gland types in the upper gastrointestinal Biosystems, Foster City, CA, USA) to a relative expression of tract and in the respiratory tract have similar structure and the target genes. function. They maintain the overall moisturizing of the muco- The primers and probes were designed as described earlier sa. MaSGs on the other hand are activated mainly during [15] and produced by Life Technologies as given in Table 2. eating when they produce serous saliva. Due to the location The probes for the target genes SV40, JCPyV, and BKPyV of MiSGs, just beneath the epithelium, different carcinogenic were labeled with 6-carboxyfluorescein (FAM) and (VIC) was agents and oncoviruses might have easier access to MiSGs used for labeling the probe for the reference gene RNase P. compared with MaSGs. The qPCR reactions were performed in 20 μlvolumeinmicro Institutional Research Ethics Board approved the study titer plate.
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