Skip to main content
Top
Published in: Virology Journal 1/2022

Open Access 01-12-2022 | Polymerase Chain Reaction | Research

Traces of JC polyomavirus in papillary thyroid cancer: a comprehensive study in Iran

Authors: Amir Ali Karimi, Rahil Tarharoudi, Zahra Kianmehr, Fatemeh Sakhaee, Fatemeh Rahimi Jamnani, Seyed Davar Siadat, Abolfazl Fateh

Published in: Virology Journal | Issue 1/2022

Login to get access

Abstract

Background

JC polyomavirus (JCPyV) is known to induce solid tumors such as astrocytomas, glioblastomas, and neuroblastomas in experimental animals, and recent studies have shown that the virus may be correlated with carcinogenesis. This study aimed to evaluate the impact of JCPyV on the progression of papillary thyroid cancer (PTC).

Methods

A total of 1057 samples, including 645 paraffin-embedded PTC biopsy samples (PEBS) and 412 fresh biopsy samples (FBS), and 1057 adjacent non-cancerous samples were evaluated for the presence of JCPyV DNA and RNA.

Results

We observed that 10.8% (114/1057) samples, including 17.5% (72/412) FBS and 6.5% (42/645) PEBS were positive for the JCPyV DNA. Among the JCPyV-positive samples, the mean JCPyV copy number was lower in patients with PEBS (0.3 × 10–4 ± 0.1 × 10–4 copies/cell) compared to FBS (1.8 × 10–1 ± 0.4 × 10–1 copies/cell) and non-PTC normal samples (0.2 × 10–5 ± 0.01 × 10–5 copies/cell), with a statistically significant difference (P < 0.001). The LT-Ag RNA expression was lower in PEBS than in FBS, while no VP1 gene transcript expression was found.

Conclusions

Although our results confirmed the presence of JCPyV in some Iranian patients with PTC, more research is needed to verify these results.
Literature
1.
go back to reference Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71:209–49.CrossRef Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71:209–49.CrossRef
2.
go back to reference Crnčić TB, Tomaš MI, Girotto N, Ivanković SG. Risk factors for thyroid cancer: What do we know so far? Acta Clin Croat. 2020;59:66. Crnčić TB, Tomaš MI, Girotto N, Ivanković SG. Risk factors for thyroid cancer: What do we know so far? Acta Clin Croat. 2020;59:66.
3.
go back to reference Mostafaei S, Keshavarz M, Nahand JS, Hassankiadeh RF, Moradinazar M, Nouri M, Babaei F, Ahadi M, Payandeh M, Esker AS. Viral infections and risk of thyroid Cancer: a systematic review and empirical Bayesian meta-analysis. Pathol Res Pract. 2020;216:152855.CrossRef Mostafaei S, Keshavarz M, Nahand JS, Hassankiadeh RF, Moradinazar M, Nouri M, Babaei F, Ahadi M, Payandeh M, Esker AS. Viral infections and risk of thyroid Cancer: a systematic review and empirical Bayesian meta-analysis. Pathol Res Pract. 2020;216:152855.CrossRef
4.
go back to reference Ghanghareh M, Mosayebi Amroabadi J, Tavangar SM, Irani S, Sakhaee F, Ghazanfari Jajin M, Vaziri F, Siadat SD, Fateh A. Evidencing the presence of merkel cell polyomavirus in papillary thyroid cancer. Sci Rep. 2021;11:1–6.CrossRef Ghanghareh M, Mosayebi Amroabadi J, Tavangar SM, Irani S, Sakhaee F, Ghazanfari Jajin M, Vaziri F, Siadat SD, Fateh A. Evidencing the presence of merkel cell polyomavirus in papillary thyroid cancer. Sci Rep. 2021;11:1–6.CrossRef
5.
go back to reference Tan CS, Ghofrani J, Geiger E, Koralnik IJ, Jost S. Decreased JC virus-specific antibody-dependent cellular cytotoxicity in HIV-seropositive PML survivors. J Acquir Immune Defic Syndr. 1999;2019(82):220. Tan CS, Ghofrani J, Geiger E, Koralnik IJ, Jost S. Decreased JC virus-specific antibody-dependent cellular cytotoxicity in HIV-seropositive PML survivors. J Acquir Immune Defic Syndr. 1999;2019(82):220.
6.
go back to reference Saribaş AS, Özdemir A, Lam C, Safak M. JC virus-induced progressive multifocal leukoencephalopathy. Futur Virol. 2010;5:313–23.CrossRef Saribaş AS, Özdemir A, Lam C, Safak M. JC virus-induced progressive multifocal leukoencephalopathy. Futur Virol. 2010;5:313–23.CrossRef
7.
go back to reference Assetta B, Atwood WJ. The biology of JC polyomavirus. Biol Chem. 2017;398:839–55.CrossRef Assetta B, Atwood WJ. The biology of JC polyomavirus. Biol Chem. 2017;398:839–55.CrossRef
8.
go back to reference Tyagarajan SK, Frisque RJ. Stability and function of JC virus large T antigen and T′ proteins are altered by mutation of their phosphorylated threonine 125 residues. J Virol. 2006;80:2083–91.CrossRef Tyagarajan SK, Frisque RJ. Stability and function of JC virus large T antigen and T′ proteins are altered by mutation of their phosphorylated threonine 125 residues. J Virol. 2006;80:2083–91.CrossRef
9.
go back to reference Prado JCM, Monezi TA, Amorim AT, Lino V, Paladino A, Boccardo E. Human polyomaviruses and cancer: an overview. Clinics 2018, 73. Prado JCM, Monezi TA, Amorim AT, Lino V, Paladino A, Boccardo E. Human polyomaviruses and cancer: an overview. Clinics 2018, 73.
10.
go back to reference Sinagra E, Raimondo D, Gallo E, Stella M, Cottone M, Rossi F, Messina M, Spada M, Tomasello G, Ferrara G. JC virus and lung adenocarcinoma: fact or myth? Anticancer Res. 2017;37:3311–4.PubMed Sinagra E, Raimondo D, Gallo E, Stella M, Cottone M, Rossi F, Messina M, Spada M, Tomasello G, Ferrara G. JC virus and lung adenocarcinoma: fact or myth? Anticancer Res. 2017;37:3311–4.PubMed
11.
go back to reference Sinagra E, Raimondo D, Gallo E, Stella M, Cottone M, Orlando A, Rossi F, Orlando E, Messina M, Tomasello G. Could JC virus provoke metastasis in colon cancer? World J Gastroenterol. 2014;20:15745.CrossRef Sinagra E, Raimondo D, Gallo E, Stella M, Cottone M, Orlando A, Rossi F, Orlando E, Messina M, Tomasello G. Could JC virus provoke metastasis in colon cancer? World J Gastroenterol. 2014;20:15745.CrossRef
12.
go back to reference McNees AL, White ZS, Zanwar P, Vilchez RA, Butel JS. Specific and quantitative detection of human polyomaviruses BKV, JCV, and SV40 by real time PCR. J Clin Virol. 2005;34:52–62.CrossRef McNees AL, White ZS, Zanwar P, Vilchez RA, Butel JS. Specific and quantitative detection of human polyomaviruses BKV, JCV, and SV40 by real time PCR. J Clin Virol. 2005;34:52–62.CrossRef
13.
go back to reference Sadeghi F, Salehi-Vaziri M, Ghodsi SM, Alizadeh A, Bokharaei-Salim F, Saroukalaei ST, Mirbolouk M, Monavari SH, Keyvani H. Prevalence of JC polyomavirus large T antigen sequences among Iranian patients with central nervous system tumors. Adv Virol. 2015;160:61–8. Sadeghi F, Salehi-Vaziri M, Ghodsi SM, Alizadeh A, Bokharaei-Salim F, Saroukalaei ST, Mirbolouk M, Monavari SH, Keyvani H. Prevalence of JC polyomavirus large T antigen sequences among Iranian patients with central nervous system tumors. Adv Virol. 2015;160:61–8.
14.
go back to reference Sadeghi F, Salehi-Vaziri M, Alizadeh A, Ghodsi SM, Bokharaei-Salim F, Fateh A, Monavari SH, Keyvani H. Detection of Merkel cell polyomavirus large T-antigen sequences in human central nervous system tumors. J Med Virol. 2015;87:1241–7.CrossRef Sadeghi F, Salehi-Vaziri M, Alizadeh A, Ghodsi SM, Bokharaei-Salim F, Fateh A, Monavari SH, Keyvani H. Detection of Merkel cell polyomavirus large T-antigen sequences in human central nervous system tumors. J Med Virol. 2015;87:1241–7.CrossRef
15.
go back to reference Chiang C, Dvorkin S, Chiang JJ, Potter RB, Gack MU. The small t antigen of JC virus antagonizes RIG-I-mediated innate immunity by inhibiting TRIM25’s RNA binding ability. MBio. 2021;12:e00620-00621.CrossRef Chiang C, Dvorkin S, Chiang JJ, Potter RB, Gack MU. The small t antigen of JC virus antagonizes RIG-I-mediated innate immunity by inhibiting TRIM25’s RNA binding ability. MBio. 2021;12:e00620-00621.CrossRef
16.
go back to reference Shapiro SS, Wilk MB. An analysis of variance test for normality (complete samples). Biometrika. 1965;52:591–611.CrossRef Shapiro SS, Wilk MB. An analysis of variance test for normality (complete samples). Biometrika. 1965;52:591–611.CrossRef
17.
go back to reference Zheng H-c, Cui Z-g, Zhao S, Zhang Y. The oncogenic roles of JC virus T antigen in breast carcinogenesis. Front Mol Biosci 2021:713. Zheng H-c, Cui Z-g, Zhao S, Zhang Y. The oncogenic roles of JC virus T antigen in breast carcinogenesis. Front Mol Biosci 2021:713.
18.
go back to reference Ahye N, Bellizzi A, May D, Wollebo HS. The role of the JC virus in central nervous system tumorigenesis. Int J Mol Sci. 2020;21:6236.CrossRef Ahye N, Bellizzi A, May D, Wollebo HS. The role of the JC virus in central nervous system tumorigenesis. Int J Mol Sci. 2020;21:6236.CrossRef
19.
go back to reference Del Valle L, Gordon J, Enam S, Delbue S, Croul S, Abraham S, Radhakrishnan S, Assimakopoulou M, Katsetos CD, Khalili K. Expression of human neurotropic polyomavirus JCV late gene product agnoprotein in human medulloblastoma. J Natl Cancer Inst. 2002;94:267–73.CrossRef Del Valle L, Gordon J, Enam S, Delbue S, Croul S, Abraham S, Radhakrishnan S, Assimakopoulou M, Katsetos CD, Khalili K. Expression of human neurotropic polyomavirus JCV late gene product agnoprotein in human medulloblastoma. J Natl Cancer Inst. 2002;94:267–73.CrossRef
20.
go back to reference Enam S, Del Valle L, Lara C, Gan D-D, Ortiz-Hidalgo C, Palazzo JP, Khalili K. Association of human polyomavirus JCV with colon cancer: evidence for interaction of viral T-antigen and β-catenin. Can Res. 2002;62:7093–101. Enam S, Del Valle L, Lara C, Gan D-D, Ortiz-Hidalgo C, Palazzo JP, Khalili K. Association of human polyomavirus JCV with colon cancer: evidence for interaction of viral T-antigen and β-catenin. Can Res. 2002;62:7093–101.
21.
go back to reference Pacini F, Vivaldi A, Santoro M, Fedele M, Fusco A, Romei C, Basolo F, Pinchera A. Simian virus 40-like DNA sequences in human papillary thyroid carcinomas. Oncogene. 1998;16:665–9.CrossRef Pacini F, Vivaldi A, Santoro M, Fedele M, Fusco A, Romei C, Basolo F, Pinchera A. Simian virus 40-like DNA sequences in human papillary thyroid carcinomas. Oncogene. 1998;16:665–9.CrossRef
22.
go back to reference Vivaldi A, Pacini F, Martini F, Iaccheri L, Pezzetti F, Elisei R, Pinchera A, Faviana P, Basolo F, Tognon M. Simian virus 40-like sequences from early and late regions in human thyroid tumors of different histotypes. J Clin Endocrinol Metab. 2003;88:892–9.CrossRef Vivaldi A, Pacini F, Martini F, Iaccheri L, Pezzetti F, Elisei R, Pinchera A, Faviana P, Basolo F, Tognon M. Simian virus 40-like sequences from early and late regions in human thyroid tumors of different histotypes. J Clin Endocrinol Metab. 2003;88:892–9.CrossRef
23.
go back to reference Ozdarendeli A, Camci C, Aygen E, Kirkil C, Toroman Z, Dogru O, Doymaz M. SV40 in human thyroid nodules. J Clin Virol. 2004;30:337–40.CrossRef Ozdarendeli A, Camci C, Aygen E, Kirkil C, Toroman Z, Dogru O, Doymaz M. SV40 in human thyroid nodules. J Clin Virol. 2004;30:337–40.CrossRef
24.
go back to reference Stamatiou D, Derdas SP, Symvoulakis EK, Sakorafas GH, Zoras O, Spandidos DA. Investigation of BK virus, Epstein–Barr virus and human papillomavirus sequences in postoperative thyroid gland specimens. Int J Biol Mark. 2015;30:104–10.CrossRef Stamatiou D, Derdas SP, Symvoulakis EK, Sakorafas GH, Zoras O, Spandidos DA. Investigation of BK virus, Epstein–Barr virus and human papillomavirus sequences in postoperative thyroid gland specimens. Int J Biol Mark. 2015;30:104–10.CrossRef
25.
go back to reference Fredericks D, Relman DA. Sequence-based identification of microbial pathogens: a reconsideration of Koch’s postulates. Clin Microbiol Rev. 1996;9:18–33.CrossRef Fredericks D, Relman DA. Sequence-based identification of microbial pathogens: a reconsideration of Koch’s postulates. Clin Microbiol Rev. 1996;9:18–33.CrossRef
26.
go back to reference Hill AB. The environment and disease: Association or causation? J R Soc Med. 2015;108:32–7.CrossRef Hill AB. The environment and disease: Association or causation? J R Soc Med. 2015;108:32–7.CrossRef
27.
go back to reference Sarid R, Gao S-J. Viruses and human cancer: from detection to causality. Cancer Lett. 2011;305:218–27.CrossRef Sarid R, Gao S-J. Viruses and human cancer: from detection to causality. Cancer Lett. 2011;305:218–27.CrossRef
28.
go back to reference Gao XH, Li J, Gong HF, Yu GY, Liu P, Hao LQ, Liu LJ, Bai CG, Zhang W. Comparison of fresh frozen tissue with formalin-fixed paraffin-embedded tissue for mutation analysis using a multi-gene panel in patients with colorectal cancer. Front Oncol. 2020;10:310.CrossRef Gao XH, Li J, Gong HF, Yu GY, Liu P, Hao LQ, Liu LJ, Bai CG, Zhang W. Comparison of fresh frozen tissue with formalin-fixed paraffin-embedded tissue for mutation analysis using a multi-gene panel in patients with colorectal cancer. Front Oncol. 2020;10:310.CrossRef
29.
go back to reference Mohebbi E, Noormohamadi Z, Sadeghi-Rad H, Sadeghi F, Yahyapour Y, Vaziri F, Rahimi A, Rahimi Jamnani F, Mehrabi S, Siadat SD. Low viral load of Merkel cell polyomavirus in Iranian patients with head and neck squamous cell carcinoma: Is it clinically important? J Med Virol. 2018;90:344–50.CrossRef Mohebbi E, Noormohamadi Z, Sadeghi-Rad H, Sadeghi F, Yahyapour Y, Vaziri F, Rahimi A, Rahimi Jamnani F, Mehrabi S, Siadat SD. Low viral load of Merkel cell polyomavirus in Iranian patients with head and neck squamous cell carcinoma: Is it clinically important? J Med Virol. 2018;90:344–50.CrossRef
30.
go back to reference Behdarvand A, Zamani MS, Sadeghi F, Yahyapour Y, Vaziri F, Jamnani FR, Nowruzi B, Fateh A, Siadat SD. Evaluation of Merkel cell polyomavirus in non-small cell lung cancer and adjacent normal cells. Microb Pathog. 2017;108:21–6.CrossRef Behdarvand A, Zamani MS, Sadeghi F, Yahyapour Y, Vaziri F, Jamnani FR, Nowruzi B, Fateh A, Siadat SD. Evaluation of Merkel cell polyomavirus in non-small cell lung cancer and adjacent normal cells. Microb Pathog. 2017;108:21–6.CrossRef
31.
go back to reference Niller HH, Wolf H, Minarovits J. Viral hit and run-oncogenesis: genetic and epigenetic scenarios. Cancer Lett. 2011;305:200–17.CrossRef Niller HH, Wolf H, Minarovits J. Viral hit and run-oncogenesis: genetic and epigenetic scenarios. Cancer Lett. 2011;305:200–17.CrossRef
32.
go back to reference Jung WT, Li MS, Goel A, Boland CR. JC virus T-antigen expression in sporadic adenomatous polyps of the colon. Cancer Interdiscip Int J Am Cancer Soc. 2008;112:1028–36. Jung WT, Li MS, Goel A, Boland CR. JC virus T-antigen expression in sporadic adenomatous polyps of the colon. Cancer Interdiscip Int J Am Cancer Soc. 2008;112:1028–36.
33.
go back to reference zur Hausen H. A specific signature of Merkel cell polyomavirus persistence in human cancer cells. Proc Natl Acad Sci. 2008;105:16063–4.CrossRef zur Hausen H. A specific signature of Merkel cell polyomavirus persistence in human cancer cells. Proc Natl Acad Sci. 2008;105:16063–4.CrossRef
34.
go back to reference Feng H, Shuda M, Chang Y, Moore PS. Clonal integration of a polyomavirus in human Merkel cell carcinoma. Science. 2008;319:1096–100.CrossRef Feng H, Shuda M, Chang Y, Moore PS. Clonal integration of a polyomavirus in human Merkel cell carcinoma. Science. 2008;319:1096–100.CrossRef
35.
go back to reference Rotondo JC, Mazziotta C, Lanzillotti C, Tognon M, Martini F. Epigenetic dysregulations in merkel cell polyomavirus-driven merkel cell carcinoma. Int J Mol Sci. 2021;22:11464.CrossRef Rotondo JC, Mazziotta C, Lanzillotti C, Tognon M, Martini F. Epigenetic dysregulations in merkel cell polyomavirus-driven merkel cell carcinoma. Int J Mol Sci. 2021;22:11464.CrossRef
36.
go back to reference Hashida Y, Imajoh M, Nemoto Y, Kamioka M, Taniguchi A, Taguchi T, Kume M, Orihashi K, Daibata M. Detection of Merkel cell polyomavirus with a tumour-specific signature in non-small cell lung cancer. Br J Cancer. 2013;108:629–37.CrossRef Hashida Y, Imajoh M, Nemoto Y, Kamioka M, Taniguchi A, Taguchi T, Kume M, Orihashi K, Daibata M. Detection of Merkel cell polyomavirus with a tumour-specific signature in non-small cell lung cancer. Br J Cancer. 2013;108:629–37.CrossRef
37.
go back to reference Abdel-Aziz HO, Murai Y, Hong M, Kutsuna T, Takahashi H, Nomoto K, Murata S, Tsuneyama K, Takano Y. Detection of the JC virus genome in lung cancers: possible role of the T-antigen in lung oncogenesis. Appl Immunohistochem Mol Morphol. 2007;15:394–400.CrossRef Abdel-Aziz HO, Murai Y, Hong M, Kutsuna T, Takahashi H, Nomoto K, Murata S, Tsuneyama K, Takano Y. Detection of the JC virus genome in lung cancers: possible role of the T-antigen in lung oncogenesis. Appl Immunohistochem Mol Morphol. 2007;15:394–400.CrossRef
Metadata
Title
Traces of JC polyomavirus in papillary thyroid cancer: a comprehensive study in Iran
Authors
Amir Ali Karimi
Rahil Tarharoudi
Zahra Kianmehr
Fatemeh Sakhaee
Fatemeh Rahimi Jamnani
Seyed Davar Siadat
Abolfazl Fateh
Publication date
01-12-2022
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2022
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-022-01881-4

Other articles of this Issue 1/2022

Virology Journal 1/2022 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.