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Erschienen in: Archives of Virology 1/2015

01.01.2015 | Original Article

Prevalence of JC polyomavirus large T antigen sequences among Iranian patients with central nervous system tumors

verfasst von: Farzin Sadeghi, Mostafa Salehi-Vaziri, Seyed Mohammad Ghodsi, Ahad Alizadeh, Farah Bokharaei-Salim, Sedigheh Taghinezhad Saroukalaei, Mohammadhossein Mirbolouk, Seyed Hamidreza Monavari, Hossein Keyvani

Erschienen in: Archives of Virology | Ausgabe 1/2015

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Abstract

The human neurotropic JC virus (JCV) is of significant interest due to its experimental neuro- oncogenic potential. In clinical samples from human central nervous system (CNS) tumors, detection of JCV sequences suggests a possible association with CNS neoplasms, but the results are discrepant worldwide. To assess the prevalence of JCV sequences in Iranian patients with primary and metastatic CNS malignancies, a total of 58 fresh CNS tumors were examined by quantitative real-time PCR targeting the JCV large T antigen (LT-Ag) gene, and JCV DNA load was determined as viral copy number per cell. All patients were immunocompetent, and none of them had received immunosuppressive therapy before surgical operation. JC virus LT-Ag sequences were found in a total of 15 (25.9 %) out of the 58 tested samples. In primary CNS tumors, JCV sequences were identified more frequently in meningiomas (50.0 %) and schwannomas (35.7 %). In metastatic CNS tumors, JCV LT-Ag was identified in one case with brain adenocarcinoma originating from lung cancer. No statistically significant association between JCV positivity and various types of CNS malignancies was observed (P = 0.565). The mean JCV LT-Ag copy number in 15 positive cases was 1.8 × 10−4 ± 4.5 × 10−4 copies per cell (range 1.0 × 10−5-1.78 × 10−3 copies per cell). An inverse correlation between white blood cell (WBC) count and JCV copy number was observed, but this correlation was not statistically significant (R = −0.198, P = 0.480). This study provides the first data on the prevalence of JCV in primary and metastatic CNS tumors from Iranian patients.
Literatur
1.
2.
3.
4.
Zurück zum Zitat White MK, Gordon J, Reiss K, Del Valle L, Croul S, Giordano A, Darbinyan A, Khalili K (2005) Human polyomaviruses and brain tumors. Brain Res Brain Res Rev 50:69–85PubMedCrossRef White MK, Gordon J, Reiss K, Del Valle L, Croul S, Giordano A, Darbinyan A, Khalili K (2005) Human polyomaviruses and brain tumors. Brain Res Brain Res Rev 50:69–85PubMedCrossRef
5.
Zurück zum Zitat Bofill-Mas S, Pina S, Girones R (2000) Documenting the epidemiologic patterns of polyomaviruses in human populations by studying their presence in urban sewage. Appl Environ Microbiol 66:238–245PubMedCrossRefPubMedCentral Bofill-Mas S, Pina S, Girones R (2000) Documenting the epidemiologic patterns of polyomaviruses in human populations by studying their presence in urban sewage. Appl Environ Microbiol 66:238–245PubMedCrossRefPubMedCentral
6.
Zurück zum Zitat Bofill-Mas S, Rodriguez-Manzano J, Calgua B, Carratala A, Girones R (2010) Newly described human polyomaviruses Merkel cell, KI and WU are present in urban sewage and may represent potential environmental contaminants. Virol J 7:141PubMedCrossRefPubMedCentral Bofill-Mas S, Rodriguez-Manzano J, Calgua B, Carratala A, Girones R (2010) Newly described human polyomaviruses Merkel cell, KI and WU are present in urban sewage and may represent potential environmental contaminants. Virol J 7:141PubMedCrossRefPubMedCentral
7.
Zurück zum Zitat Moens U, Van Ghelue M, Ehlers B (2014) Are human polyomaviruses co-factors for cancers induced by other oncoviruses? Rev Med Virol. doi:10.1002/rmv.1798 Moens U, Van Ghelue M, Ehlers B (2014) Are human polyomaviruses co-factors for cancers induced by other oncoviruses? Rev Med Virol. doi:10.​1002/​rmv.​1798
8.
Zurück zum Zitat Padgett BL, Walker DL, ZuRhein GM, Eckroade RJ, Dessel BH (1971) Cultivation of papova-like virus from human brain with progressive multifocal leucoencephalopathy. Lancet 1:1257–1260PubMedCrossRef Padgett BL, Walker DL, ZuRhein GM, Eckroade RJ, Dessel BH (1971) Cultivation of papova-like virus from human brain with progressive multifocal leucoencephalopathy. Lancet 1:1257–1260PubMedCrossRef
9.
Zurück zum Zitat Gardner SD, Field AM, Coleman DV, Hulme B (1971) New human papovavirus (B.K.) isolated from urine after renal transplantation. Lancet 1:1253–1257PubMedCrossRef Gardner SD, Field AM, Coleman DV, Hulme B (1971) New human papovavirus (B.K.) isolated from urine after renal transplantation. Lancet 1:1253–1257PubMedCrossRef
10.
Zurück zum Zitat Markowitz RB, Thompson HC, Mueller JF, Cohen JA, Dynan WS (1993) Incidence of BK virus and JC virus viruria in human immunodeficiency virus-infected and -uninfected subjects. J Infect Dis 167:13–20PubMedCrossRef Markowitz RB, Thompson HC, Mueller JF, Cohen JA, Dynan WS (1993) Incidence of BK virus and JC virus viruria in human immunodeficiency virus-infected and -uninfected subjects. J Infect Dis 167:13–20PubMedCrossRef
11.
Zurück zum Zitat Gjoerup O, Chang Y (2010) Update on human polyomaviruses and cancer. Adv Cancer Res 106:1–51PubMedCrossRef Gjoerup O, Chang Y (2010) Update on human polyomaviruses and cancer. Adv Cancer Res 106:1–51PubMedCrossRef
12.
Zurück zum Zitat Khalili K, Del Valle L, Otte J, Weaver M, Gordon J (2003) Human neurotropic polyomavirus, JCV, and its role in carcinogenesis. Oncogene 22:5181–5191PubMedCrossRef Khalili K, Del Valle L, Otte J, Weaver M, Gordon J (2003) Human neurotropic polyomavirus, JCV, and its role in carcinogenesis. Oncogene 22:5181–5191PubMedCrossRef
13.
Zurück zum Zitat Koralnik IJ (2006) Progressive multifocal leukoencephalopathy revisited: Has the disease outgrown its name? Ann Neurol 60:162–173PubMedCrossRef Koralnik IJ (2006) Progressive multifocal leukoencephalopathy revisited: Has the disease outgrown its name? Ann Neurol 60:162–173PubMedCrossRef
14.
Zurück zum Zitat Arthur RR, Shah KV, Baust SJ, Santos GW, Saral R (1986) Association of BK viruria with hemorrhagic cystitis in recipients of bone marrow transplants. N Engl J Med 315:230–234PubMedCrossRef Arthur RR, Shah KV, Baust SJ, Santos GW, Saral R (1986) Association of BK viruria with hemorrhagic cystitis in recipients of bone marrow transplants. N Engl J Med 315:230–234PubMedCrossRef
15.
18.
Zurück zum Zitat Del Valle L, Wang JY, Lassak A, Peruzzi F, Croul S, Khalili K, Reiss K (2002) Insulin-like growth factor I receptor signaling system in JC virus T antigen-induced primitive neuroectodermal tumors–medulloblastomas. J Neurovirol 8(Suppl 2):138–147PubMedCrossRef Del Valle L, Wang JY, Lassak A, Peruzzi F, Croul S, Khalili K, Reiss K (2002) Insulin-like growth factor I receptor signaling system in JC virus T antigen-induced primitive neuroectodermal tumors–medulloblastomas. J Neurovirol 8(Suppl 2):138–147PubMedCrossRef
19.
Zurück zum Zitat Gan DD, Reiss K, Carrill T, Del Valle L, Croul S, Giordano A, Fishman P, Khalili K (2001) Involvement of Wnt signaling pathway in murine medulloblastoma induced by human neurotropic JC virus. Oncogene 20:4864–4870PubMedCrossRef Gan DD, Reiss K, Carrill T, Del Valle L, Croul S, Giordano A, Fishman P, Khalili K (2001) Involvement of Wnt signaling pathway in murine medulloblastoma induced by human neurotropic JC virus. Oncogene 20:4864–4870PubMedCrossRef
20.
Zurück zum Zitat London WT, Houff SA, Madden DL, Fuccillo DA, Gravell M, Wallen WC, Palmer AE, Sever JL, Padgett BL, Walker DL, ZuRhein GM, Ohashi T (1978) Brain tumors in owl monkeys inoculated with a human polyomavirus (JC virus). Science 201:1246–1249PubMedCrossRef London WT, Houff SA, Madden DL, Fuccillo DA, Gravell M, Wallen WC, Palmer AE, Sever JL, Padgett BL, Walker DL, ZuRhein GM, Ohashi T (1978) Brain tumors in owl monkeys inoculated with a human polyomavirus (JC virus). Science 201:1246–1249PubMedCrossRef
21.
Zurück zum Zitat London WT, Houff SA, McKeever PE, Wallen WC, Sever JL, Padgett BL, Walker DL (1983) Viral-induced astrocytomas in squirrel monkeys. Prog Clin Biol Res 105:227–237PubMed London WT, Houff SA, McKeever PE, Wallen WC, Sever JL, Padgett BL, Walker DL (1983) Viral-induced astrocytomas in squirrel monkeys. Prog Clin Biol Res 105:227–237PubMed
22.
Zurück zum Zitat Walker DL, Padgett BL, ZuRhein GM, Albert AE, Marsh RF (1973) Human papovavirus (JC): induction of brain tumors in hamsters. Science 181:674–676PubMedCrossRef Walker DL, Padgett BL, ZuRhein GM, Albert AE, Marsh RF (1973) Human papovavirus (JC): induction of brain tumors in hamsters. Science 181:674–676PubMedCrossRef
23.
Zurück zum Zitat Frisque RJ, Rifkin DB, Walker DL (1980) Transformation of primary hamster brain cells with JC virus and its DNA. J Virol 35:265–269PubMedPubMedCentral Frisque RJ, Rifkin DB, Walker DL (1980) Transformation of primary hamster brain cells with JC virus and its DNA. J Virol 35:265–269PubMedPubMedCentral
24.
Zurück zum Zitat Mandl C, Walker DL, Frisque RJ (1987) Derivation and characterization of POJ cells, transformed human fetal glial cells that retain their permissivity for JC virus. J Virol 61:755–763PubMedPubMedCentral Mandl C, Walker DL, Frisque RJ (1987) Derivation and characterization of POJ cells, transformed human fetal glial cells that retain their permissivity for JC virus. J Virol 61:755–763PubMedPubMedCentral
25.
Zurück zum Zitat Atwood WJ, Amemiya K, Traub R, Harms J, Major EO (1992) Interaction of the human polyomavirus, JCV, with human B-lymphocytes. Virology 190:716–723PubMedCrossRef Atwood WJ, Amemiya K, Traub R, Harms J, Major EO (1992) Interaction of the human polyomavirus, JCV, with human B-lymphocytes. Virology 190:716–723PubMedCrossRef
26.
Zurück zum Zitat Randhawa P, Shapiro R, Vats A (2005) Quantitation of DNA of polyomaviruses BK and JC in human kidneys. J Infect Dis 192:504–509PubMedCrossRef Randhawa P, Shapiro R, Vats A (2005) Quantitation of DNA of polyomaviruses BK and JC in human kidneys. J Infect Dis 192:504–509PubMedCrossRef
27.
Zurück zum Zitat Tan CS, Dezube BJ, Bhargava P, Autissier P, Wuthrich C, Miller J, Koralnik IJ (2009) Detection of JC virus DNA and proteins in the bone marrow of HIV-positive and HIV-negative patients: implications for viral latency and neurotropic transformation. J Infect Dis 199:881–888PubMedCrossRefPubMedCentral Tan CS, Dezube BJ, Bhargava P, Autissier P, Wuthrich C, Miller J, Koralnik IJ (2009) Detection of JC virus DNA and proteins in the bone marrow of HIV-positive and HIV-negative patients: implications for viral latency and neurotropic transformation. J Infect Dis 199:881–888PubMedCrossRefPubMedCentral
28.
Zurück zum Zitat Sabath BF, Major EO (2002) Traffic of JC virus from sites of initial infection to the brain: the path to progressive multifocal leukoencephalopathy. J Infect Dis 186(Suppl 2):S180–S186PubMedCrossRef Sabath BF, Major EO (2002) Traffic of JC virus from sites of initial infection to the brain: the path to progressive multifocal leukoencephalopathy. J Infect Dis 186(Suppl 2):S180–S186PubMedCrossRef
29.
Zurück zum Zitat Perez-Liz G, Del Valle L, Gentilella A, Croul S, Khalili K (2008) Detection of JC virus DNA fragments but not proteins in normal brain tissue. Ann Neurol 64:379–387PubMedCrossRefPubMedCentral Perez-Liz G, Del Valle L, Gentilella A, Croul S, Khalili K (2008) Detection of JC virus DNA fragments but not proteins in normal brain tissue. Ann Neurol 64:379–387PubMedCrossRefPubMedCentral
30.
Zurück zum Zitat Bayliss J, Karasoulos T, McLean CA (2013) Immunosuppression increases JC polyomavirus large T antigen DNA load in the brains of patients without progressive multifocal leukoencephalopathy. J Infect Dis 207:133–136PubMedCrossRef Bayliss J, Karasoulos T, McLean CA (2013) Immunosuppression increases JC polyomavirus large T antigen DNA load in the brains of patients without progressive multifocal leukoencephalopathy. J Infect Dis 207:133–136PubMedCrossRef
31.
Zurück zum Zitat Tan CS, Ellis LC, Wuthrich C, Ngo L, Broge TA Jr, Saint-Aubyn J, Miller JS, Koralnik IJ (2010) JC virus latency in the brain and extraneural organs of patients with and without progressive multifocal leukoencephalopathy. J Virol 84:9200–9209PubMedCrossRefPubMedCentral Tan CS, Ellis LC, Wuthrich C, Ngo L, Broge TA Jr, Saint-Aubyn J, Miller JS, Koralnik IJ (2010) JC virus latency in the brain and extraneural organs of patients with and without progressive multifocal leukoencephalopathy. J Virol 84:9200–9209PubMedCrossRefPubMedCentral
32.
Zurück zum Zitat Richardson EP Jr (1961) Progressive multifocal leukoencephalopathy. N Engl J Med 265:815–823PubMedCrossRef Richardson EP Jr (1961) Progressive multifocal leukoencephalopathy. N Engl J Med 265:815–823PubMedCrossRef
33.
Zurück zum Zitat Del Valle L, Gordon J, Assimakopoulou M, Enam S, Geddes JF, Varakis JN, Katsetos CD, Croul S, Khalili K (2001) Detection of JC virus DNA sequences and expression of the viral regulatory protein T-antigen in tumors of the central nervous system. Cancer Res 61:4287–4293PubMed Del Valle L, Gordon J, Assimakopoulou M, Enam S, Geddes JF, Varakis JN, Katsetos CD, Croul S, Khalili K (2001) Detection of JC virus DNA sequences and expression of the viral regulatory protein T-antigen in tumors of the central nervous system. Cancer Res 61:4287–4293PubMed
34.
Zurück zum Zitat Delbue S, Pagani E, Guerini FR, Agliardi C, Mancuso R, Borghi E, Rossi F, Boldorini R, Veggiani C, Car PG, Ferrante P (2005) Distribution, characterization and significance of polyomavirus genomic sequences in tumors of the brain and its covering. J Med Virol 77:447–454PubMedCrossRef Delbue S, Pagani E, Guerini FR, Agliardi C, Mancuso R, Borghi E, Rossi F, Boldorini R, Veggiani C, Car PG, Ferrante P (2005) Distribution, characterization and significance of polyomavirus genomic sequences in tumors of the brain and its covering. J Med Virol 77:447–454PubMedCrossRef
35.
Zurück zum Zitat Tsekov I, Ferdinandov D, Bussarsky V, Hristova S, Kalvatchev Z (2011) Prevalence of JC polyomavirus genomic sequences from the large T-antigen and non-coding control regions among Bulgarian patients with primary brain tumors. J Med Virol 83:1608–1613PubMedCrossRef Tsekov I, Ferdinandov D, Bussarsky V, Hristova S, Kalvatchev Z (2011) Prevalence of JC polyomavirus genomic sequences from the large T-antigen and non-coding control regions among Bulgarian patients with primary brain tumors. J Med Virol 83:1608–1613PubMedCrossRef
36.
Zurück zum Zitat Bozorgi SM, Tahaei SM, Mohebbi SR, Sahba N, Damavand B, Romani S, Azimzadeh P, Naghoosi H, Milanizadeh S, Mohebbi A, Zali MR (2012) Molecular prevalence of JC virus in Tehran, Iran. Gastroenterol Hepatol Bed Bench 5:84–89PubMedPubMedCentral Bozorgi SM, Tahaei SM, Mohebbi SR, Sahba N, Damavand B, Romani S, Azimzadeh P, Naghoosi H, Milanizadeh S, Mohebbi A, Zali MR (2012) Molecular prevalence of JC virus in Tehran, Iran. Gastroenterol Hepatol Bed Bench 5:84–89PubMedPubMedCentral
37.
Zurück zum Zitat McNees AL, White ZS, Zanwar P, Vilchez RA, Butel JS (2005) Specific and quantitative detection of human polyomaviruses BKV, JCV, and SV40 by real time PCR. J Clin Virol 34:52–62PubMedCrossRef McNees AL, White ZS, Zanwar P, Vilchez RA, Butel JS (2005) Specific and quantitative detection of human polyomaviruses BKV, JCV, and SV40 by real time PCR. J Clin Virol 34:52–62PubMedCrossRef
38.
Zurück zum Zitat MacKenzie J, Wilson KS, Perry J, Gallagher A, Jarrett RF (2003) Association between simian virus 40 DNA and lymphoma in the United Kingdom. J Natl Cancer Inst 95:1001–1003PubMedCrossRef MacKenzie J, Wilson KS, Perry J, Gallagher A, Jarrett RF (2003) Association between simian virus 40 DNA and lymphoma in the United Kingdom. J Natl Cancer Inst 95:1001–1003PubMedCrossRef
39.
Zurück zum Zitat Imajoh M, Hashida Y, Taniguchi A, Kamioka M, Daibata M (2012) Novel human polyomaviruses, Merkel cell polyomavirus and human polyomavirus 9, in Japanese chronic lymphocytic leukemia cases. J Hematol Oncol 5:25PubMedCrossRefPubMedCentral Imajoh M, Hashida Y, Taniguchi A, Kamioka M, Daibata M (2012) Novel human polyomaviruses, Merkel cell polyomavirus and human polyomavirus 9, in Japanese chronic lymphocytic leukemia cases. J Hematol Oncol 5:25PubMedCrossRefPubMedCentral
40.
Zurück zum Zitat Jazayeri SB, Rahimi-Movaghar V, Shokraneh F, Saadat S, Ramezani R (2013) Epidemiology of primary CNS tumors in Iran: a systematic review. Asian Pac J Cancer Prev 14:3979–3985PubMedCrossRef Jazayeri SB, Rahimi-Movaghar V, Shokraneh F, Saadat S, Ramezani R (2013) Epidemiology of primary CNS tumors in Iran: a systematic review. Asian Pac J Cancer Prev 14:3979–3985PubMedCrossRef
41.
Zurück zum Zitat Zheng H, Abdel Aziz HO, Nakanishi Y, Masuda S, Saito H, Tsuneyama K, Takano Y (2007) Oncogenic role of JC virus in lung cancer. J Pathol 212:306–315PubMedCrossRef Zheng H, Abdel Aziz HO, Nakanishi Y, Masuda S, Saito H, Tsuneyama K, Takano Y (2007) Oncogenic role of JC virus in lung cancer. J Pathol 212:306–315PubMedCrossRef
42.
Zurück zum Zitat Behren A, Simon C, Schwab RM, Loetzsch E, Brodbeck S, Huber E, Stubenrauch F, Zenner HP, Iftner T (2005) Papillomavirus E2 protein induces expression of the matrix metalloproteinase-9 via the extracellular signal-regulated kinase/activator protein-1 signaling pathway. Cancer Res 65:11613–11621PubMedCrossRef Behren A, Simon C, Schwab RM, Loetzsch E, Brodbeck S, Huber E, Stubenrauch F, Zenner HP, Iftner T (2005) Papillomavirus E2 protein induces expression of the matrix metalloproteinase-9 via the extracellular signal-regulated kinase/activator protein-1 signaling pathway. Cancer Res 65:11613–11621PubMedCrossRef
43.
Zurück zum Zitat Gou XM, Chen Y, Chen XY, Arrand JR (2003) Effects of Epstein-Barr virus latent membrane protein 1 (EBV-LMP1) on related factors of metastasis of nasopharyngeal carcinoma cell line CNE1. Ai Zheng 22:481–485PubMed Gou XM, Chen Y, Chen XY, Arrand JR (2003) Effects of Epstein-Barr virus latent membrane protein 1 (EBV-LMP1) on related factors of metastasis of nasopharyngeal carcinoma cell line CNE1. Ai Zheng 22:481–485PubMed
44.
Zurück zum Zitat Link A, Shin SK, Nagasaka T, Balaguer F, Koi M, Jung B, Boland CR, Goel A (2009) JC virus mediates invasion and migration in colorectal metastasis. PLoS One 4:e8146PubMedCrossRefPubMedCentral Link A, Shin SK, Nagasaka T, Balaguer F, Koi M, Jung B, Boland CR, Goel A (2009) JC virus mediates invasion and migration in colorectal metastasis. PLoS One 4:e8146PubMedCrossRefPubMedCentral
45.
Zurück zum Zitat Krynska B, Gordon J, Otte J, Franks R, Knobler R, DeLuca A, Giordano A, Khalili K (1997) Role of cell cycle regulators in tumor formation in transgenic mice expressing the human neurotropic virus, JCV, early protein. J Cell Biochem 67:223–230PubMedCrossRef Krynska B, Gordon J, Otte J, Franks R, Knobler R, DeLuca A, Giordano A, Khalili K (1997) Role of cell cycle regulators in tumor formation in transgenic mice expressing the human neurotropic virus, JCV, early protein. J Cell Biochem 67:223–230PubMedCrossRef
46.
Zurück zum Zitat White MK, Khalili K (2006) Interaction of retinoblastoma protein family members with large T-antigen of primate polyomaviruses. Oncogene 25:5286–5293PubMedCrossRef White MK, Khalili K (2006) Interaction of retinoblastoma protein family members with large T-antigen of primate polyomaviruses. Oncogene 25:5286–5293PubMedCrossRef
Metadaten
Titel
Prevalence of JC polyomavirus large T antigen sequences among Iranian patients with central nervous system tumors
verfasst von
Farzin Sadeghi
Mostafa Salehi-Vaziri
Seyed Mohammad Ghodsi
Ahad Alizadeh
Farah Bokharaei-Salim
Sedigheh Taghinezhad Saroukalaei
Mohammadhossein Mirbolouk
Seyed Hamidreza Monavari
Hossein Keyvani
Publikationsdatum
01.01.2015
Verlag
Springer Vienna
Erschienen in
Archives of Virology / Ausgabe 1/2015
Print ISSN: 0304-8608
Elektronische ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-014-2230-0

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