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Published in: BMC Urology 1/2022

Open Access 01-12-2022 | Kidney Cancer | Research

Epstein–Barr virus infection is associated with the nuclear factor-kappa B p65 signaling pathway in renal cell carcinoma

Authors: Ali Farhadi, Sepide Namdari, Pei Pei Chong, Bita Geramizadeh, Abbas Behzad-Behbahani, Zamberi Sekawi, Sedigheh Sharifzadeh

Published in: BMC Urology | Issue 1/2022

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Abstract

Background

There have been few studies regarding viral involvement in the pathogenesis of renal cell carcinoma (RCC). The aim of this study was to examine the possible association of Epstein–Barr virus (EBV) infection with clinicopathological features and cellular biomarkers including p53, p16INK4a, Ki-67 and nuclear factor-kappa B (NF-κB) in RCC tumors.

Methods

In this prospective study, 122 histologically confirmed Formalin-fixed Paraffin-embedded RCC tissue specimens along with 96 specimens of their corresponding peritumoral tissues and 23 samples of blunt renal injuries were subjected to nested polymerase chain reaction (nPCR) in order to amplify EBV DNA sequences. The expression of p53, p16INK4a, Ki-67 and NF-κB was investigated by immunohistochemistry (IHC) assay. Statistical analysis was employed to demonstrate the possible associations.

Results

Infection with EBV was found to be significantly associated with RCC. Our results indicate that p65 NF-κB signaling pathway is probably involved in EBV-mediated RCC pathogenesis. Moreover, we found p53, Ki-67 and cytoplasmic NF-κB expression to be associated with tumor nuclear grade in RCC patients. The expression of p53 and Ki-67 was associated with primary tumor category as well. In addition, p53 overexpression was significantly more frequent among nonconventional RCC tumors than the conventional histologic type.

Conclusions

Infection with EBV is likely to play an important role in the development of RCC through the constitutive and permanent activation of NF-κB p65 signaling pathway. However, more experiments and supporting data are required to reach a decisive conclusion.
Literature
3.
go back to reference Koul H, Huh JS, Rove KO, et al. Molecular aspects of renal cell carcinoma: a review. Am J Cancer Res. 2011;1(2):240.PubMed Koul H, Huh JS, Rove KO, et al. Molecular aspects of renal cell carcinoma: a review. Am J Cancer Res. 2011;1(2):240.PubMed
6.
go back to reference Liao JB. Cancer issue: viruses and human cancer. Yale J Biol Med. 2006;79(3–4):115.PubMed Liao JB. Cancer issue: viruses and human cancer. Yale J Biol Med. 2006;79(3–4):115.PubMed
7.
go back to reference Hutt-Fletcher L. Cancers in people with HIV and AIDS: Epstein–Barr virus. 1st ed. New York: Springer; 2014. p. 75–85. Hutt-Fletcher L. Cancers in people with HIV and AIDS: Epstein–Barr virus. 1st ed. New York: Springer; 2014. p. 75–85.
8.
go back to reference Ponticelli C. Herpes viruses and tumours in kidney transplant recipients. The role of immunosuppression. Nephrol Dial Transplant. 2011;26(6):1769–75.PubMedCrossRef Ponticelli C. Herpes viruses and tumours in kidney transplant recipients. The role of immunosuppression. Nephrol Dial Transplant. 2011;26(6):1769–75.PubMedCrossRef
9.
go back to reference Iwama H, Horikoshi S, Shirato I, et al. Epstein–Barr virus detection in kidney biopsy specimens correlates with glomerular mesangial injury. Am J Kidney Dis. 1998;32(5):785–93.PubMedCrossRef Iwama H, Horikoshi S, Shirato I, et al. Epstein–Barr virus detection in kidney biopsy specimens correlates with glomerular mesangial injury. Am J Kidney Dis. 1998;32(5):785–93.PubMedCrossRef
10.
go back to reference Becker JL, Miller F, Nuovo GJ, et al. Epstein–Barr virus infection of renal proximal tubule cells: possible role in chronic interstitial nephritis. J Clin Invest. 1999;104(12):1673–81.PubMedPubMedCentralCrossRef Becker JL, Miller F, Nuovo GJ, et al. Epstein–Barr virus infection of renal proximal tubule cells: possible role in chronic interstitial nephritis. J Clin Invest. 1999;104(12):1673–81.PubMedPubMedCentralCrossRef
11.
go back to reference Törnell J, Farzad S, Espander-Jansson A, et al. Expression of Epstein–Barr nuclear antigen 2 in kidney tubule cells induce tumors in transgenic mice. Oncogene. 1996;12(7):1521–8.PubMed Törnell J, Farzad S, Espander-Jansson A, et al. Expression of Epstein–Barr nuclear antigen 2 in kidney tubule cells induce tumors in transgenic mice. Oncogene. 1996;12(7):1521–8.PubMed
12.
go back to reference Shimakage M, Kawahara K, Harada S, et al. Expression of Epstein–Barr virus in renal cell carcinoma. Oncol Rep. 2007;18(1):41–6.PubMed Shimakage M, Kawahara K, Harada S, et al. Expression of Epstein–Barr virus in renal cell carcinoma. Oncol Rep. 2007;18(1):41–6.PubMed
13.
go back to reference Karaarslan S, Şen N. Investigation of the relationship of Epstein–Barr virus with in situ hybridization in renal-cell carcinomas. Ann Diagn Pathol. 2018;34:45–9.PubMedCrossRef Karaarslan S, Şen N. Investigation of the relationship of Epstein–Barr virus with in situ hybridization in renal-cell carcinomas. Ann Diagn Pathol. 2018;34:45–9.PubMedCrossRef
14.
go back to reference Kryst P, Poletajew S, Wyczałkowska-Tomasik A, et al. Epstein–Barr virus and human adenovirus viremia in renal tumors is associated with histological features of malignancy. J Clin Med. 2020;9(10):3195.PubMedCentralCrossRef Kryst P, Poletajew S, Wyczałkowska-Tomasik A, et al. Epstein–Barr virus and human adenovirus viremia in renal tumors is associated with histological features of malignancy. J Clin Med. 2020;9(10):3195.PubMedCentralCrossRef
15.
go back to reference Hollstein M, Rice K, Greenblatt M, et al. Database of p53 gene somatic mutations in human tumors and cell lines. Nucleic Acids Res. 1994;22(17):3551.PubMedPubMedCentral Hollstein M, Rice K, Greenblatt M, et al. Database of p53 gene somatic mutations in human tumors and cell lines. Nucleic Acids Res. 1994;22(17):3551.PubMedPubMedCentral
16.
go back to reference Wang Z, Peng S, Jiang N, et al. Prognostic and clinicopathological value of p53 expression in renal cell carcinoma: a meta-analysis. Oncotarget. 2017;8(60):102361.PubMedPubMedCentralCrossRef Wang Z, Peng S, Jiang N, et al. Prognostic and clinicopathological value of p53 expression in renal cell carcinoma: a meta-analysis. Oncotarget. 2017;8(60):102361.PubMedPubMedCentralCrossRef
17.
go back to reference Kim HL, Seligson D, Liu X, et al. Using protein expressions to predict survival in clear cell renal carcinoma. Clin Cancer Res. 2004;10(16):5464–71.PubMedCrossRef Kim HL, Seligson D, Liu X, et al. Using protein expressions to predict survival in clear cell renal carcinoma. Clin Cancer Res. 2004;10(16):5464–71.PubMedCrossRef
18.
go back to reference Zubac DP, Bostad L, Kihl B, et al. The expression of thrombospondin-1 and p53 in clear cell renal cell carcinoma: its relationship to angiogenesis, cell proliferation and cancer specific survival. J Urol. 2009;182(5):2144–9.PubMedCrossRef Zubac DP, Bostad L, Kihl B, et al. The expression of thrombospondin-1 and p53 in clear cell renal cell carcinoma: its relationship to angiogenesis, cell proliferation and cancer specific survival. J Urol. 2009;182(5):2144–9.PubMedCrossRef
19.
go back to reference Kankaya D, Kiremitci S, Tulunay O, et al. NF-κB, and p53 expression in clear cell renal cell carcinoma: impact on outcome. Pathol Res Pract. 2015;211(7):505–12.PubMedCrossRef Kankaya D, Kiremitci S, Tulunay O, et al. NF-κB, and p53 expression in clear cell renal cell carcinoma: impact on outcome. Pathol Res Pract. 2015;211(7):505–12.PubMedCrossRef
20.
go back to reference Lok SS, Stewart JP, Kelly BG, et al. Epstein–Barr virus and wild p53 in idiopathic pulmonary fibrosis. Respir Med. 2001;95(10):787–91.PubMedCrossRef Lok SS, Stewart JP, Kelly BG, et al. Epstein–Barr virus and wild p53 in idiopathic pulmonary fibrosis. Respir Med. 2001;95(10):787–91.PubMedCrossRef
21.
go back to reference Yi F, Saha A, Murakami M, et al. Epstein–Barr virus nuclear antigen 3C targets p53 and modulates its transcriptional and apoptotic activities. Virology. 2009;388(2):236–47.PubMedCrossRef Yi F, Saha A, Murakami M, et al. Epstein–Barr virus nuclear antigen 3C targets p53 and modulates its transcriptional and apoptotic activities. Virology. 2009;388(2):236–47.PubMedCrossRef
22.
go back to reference Shao JY, Ernberg I, Biberfeld P, et al. Epstein–Barr virus LMP1 status in relation to apoptosis, p53 expression and leucocyte infiltration in nasopharyngeal carcinoma. Anticancer Res. 2004;24(4):2309–18.PubMed Shao JY, Ernberg I, Biberfeld P, et al. Epstein–Barr virus LMP1 status in relation to apoptosis, p53 expression and leucocyte infiltration in nasopharyngeal carcinoma. Anticancer Res. 2004;24(4):2309–18.PubMed
24.
go back to reference Liggett WH Jr, Sidransky D. Role of the p16 tumor suppressor gene in cancer. J Clin Oncol. 1998;16(3):1197–206.PubMedCrossRef Liggett WH Jr, Sidransky D. Role of the p16 tumor suppressor gene in cancer. J Clin Oncol. 1998;16(3):1197–206.PubMedCrossRef
25.
26.
go back to reference Kamb A, Gruis NA, Weaver-Feldhaus J, et al. A cell cycle regulator potentially involved in genesis of many tumor types. Science. 1994;264(5157):436–40.PubMedCrossRef Kamb A, Gruis NA, Weaver-Feldhaus J, et al. A cell cycle regulator potentially involved in genesis of many tumor types. Science. 1994;264(5157):436–40.PubMedCrossRef
27.
go back to reference Skalska L, White RE, Franz M, et al. Epigenetic repression of p16INK4A by latent Epstein–Barr virus requires the interaction of EBNA3A and EBNA3C with CtBP. PLoS Pathog. 2010;6(6):e1000951.PubMedPubMedCentralCrossRef Skalska L, White RE, Franz M, et al. Epigenetic repression of p16INK4A by latent Epstein–Barr virus requires the interaction of EBNA3A and EBNA3C with CtBP. PLoS Pathog. 2010;6(6):e1000951.PubMedPubMedCentralCrossRef
28.
go back to reference McGuire BB, Fitzpatrick JM. Biomarkers in renal cell carcinoma. Curr Opin Urol. 2009;19(5):441–6.PubMedCrossRef McGuire BB, Fitzpatrick JM. Biomarkers in renal cell carcinoma. Curr Opin Urol. 2009;19(5):441–6.PubMedCrossRef
29.
go back to reference Visapää H, Bui M, Huang Y, et al. Correlation of Ki-67 and gelsolin expression to clinical outcome in renal clear cell carcinoma. Urology. 2003;61(4):845–50.PubMedCrossRef Visapää H, Bui M, Huang Y, et al. Correlation of Ki-67 and gelsolin expression to clinical outcome in renal clear cell carcinoma. Urology. 2003;61(4):845–50.PubMedCrossRef
30.
go back to reference Xie Y, Chen L, Ma X, et al. Prognostic and clinicopathological role of high Ki-67 expression in patients with renal cell carcinoma: a systematic review and meta-analysis. Sci Rep. 2017;7(1):1–9. Xie Y, Chen L, Ma X, et al. Prognostic and clinicopathological role of high Ki-67 expression in patients with renal cell carcinoma: a systematic review and meta-analysis. Sci Rep. 2017;7(1):1–9.
31.
go back to reference Zheng X, Hu L, Chen F, et al. Expression of Ki67 antigen, epidermal growth factor receptor and Epstein–Barr virus-encoded latent membrane protein (LMP1) in nasopharyngeal carcinoma. Eur J Cancer B Oral Oncol. 1994;30b(5):290–5.PubMedCrossRef Zheng X, Hu L, Chen F, et al. Expression of Ki67 antigen, epidermal growth factor receptor and Epstein–Barr virus-encoded latent membrane protein (LMP1) in nasopharyngeal carcinoma. Eur J Cancer B Oral Oncol. 1994;30b(5):290–5.PubMedCrossRef
32.
go back to reference Gilmore TD. The Rel/NF-κB signal transduction pathway: introduction. Oncogene. 1999;18(49):6842–4.PubMedCrossRef Gilmore TD. The Rel/NF-κB signal transduction pathway: introduction. Oncogene. 1999;18(49):6842–4.PubMedCrossRef
33.
go back to reference Dolcet X, Llobet D, Pallares J, et al. NF-kB in development and progression of human cancer. Virchows Arch. 2005;446(5):475–82.PubMedCrossRef Dolcet X, Llobet D, Pallares J, et al. NF-kB in development and progression of human cancer. Virchows Arch. 2005;446(5):475–82.PubMedCrossRef
34.
go back to reference Matušan-Ilijaš K, Damante G, Fabbro D, et al. Osteopontin expression correlates with nuclear factor-κB activation and apoptosis downregulation in clear cell renal cell carcinoma. Pathol Res Pract. 2011;207(2):104–10.PubMedCrossRef Matušan-Ilijaš K, Damante G, Fabbro D, et al. Osteopontin expression correlates with nuclear factor-κB activation and apoptosis downregulation in clear cell renal cell carcinoma. Pathol Res Pract. 2011;207(2):104–10.PubMedCrossRef
35.
go back to reference Ng KL, Yap NY, Rajandram R, et al. Nuclear factor-kappa B subunits and their prognostic cancer-specific survival value in renal cell carcinoma patients. Pathology. 2018;50(5):511–8.PubMedCrossRef Ng KL, Yap NY, Rajandram R, et al. Nuclear factor-kappa B subunits and their prognostic cancer-specific survival value in renal cell carcinoma patients. Pathology. 2018;50(5):511–8.PubMedCrossRef
36.
go back to reference Yin H, Qu J, Peng Q, et al. Molecular mechanisms of EBV-driven cell cycle progression and oncogenesis. Med Microbiol Immunol. 2019;208(5):573–83.PubMedCrossRef Yin H, Qu J, Peng Q, et al. Molecular mechanisms of EBV-driven cell cycle progression and oncogenesis. Med Microbiol Immunol. 2019;208(5):573–83.PubMedCrossRef
37.
go back to reference Kovacs G, Akhtar M, Beckwith BJ, et al. The Heidelberg classification of renal cell tumours. J Pathol. 1997;183(2):131–3.PubMedCrossRef Kovacs G, Akhtar M, Beckwith BJ, et al. The Heidelberg classification of renal cell tumours. J Pathol. 1997;183(2):131–3.PubMedCrossRef
38.
go back to reference Fuhrman SA, Lasky LC, Limas C. Prognostic significance of morphologic parameters in renal cell carcinoma. Am J Surg Pathol. 1982;6(7):655–64.PubMedCrossRef Fuhrman SA, Lasky LC, Limas C. Prognostic significance of morphologic parameters in renal cell carcinoma. Am J Surg Pathol. 1982;6(7):655–64.PubMedCrossRef
39.
go back to reference Edge SB, Compton CC. The American Joint Committee on Cancer: the 7th edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol. 2010;17(6):1471–4.PubMedCrossRef Edge SB, Compton CC. The American Joint Committee on Cancer: the 7th edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol. 2010;17(6):1471–4.PubMedCrossRef
40.
go back to reference Guinan P, Sobin LH, Algaba F, et al. TNM staging of renal cell carcinoma: workgroup no. 3. Cancer. 1997;80(5):992–3.PubMedCrossRef Guinan P, Sobin LH, Algaba F, et al. TNM staging of renal cell carcinoma: workgroup no. 3. Cancer. 1997;80(5):992–3.PubMedCrossRef
41.
go back to reference Saiki RK, Gelfand DH, Stoffel S, et al. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988;239(4839):487–91.PubMedCrossRef Saiki RK, Gelfand DH, Stoffel S, et al. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988;239(4839):487–91.PubMedCrossRef
42.
go back to reference Espy MJ, Mitchell PS, Persing DH, et al. Diagnostic virology protocols: herpesviruses. 2nd ed. Totowa: Springer; 1998. p. 89–101.CrossRef Espy MJ, Mitchell PS, Persing DH, et al. Diagnostic virology protocols: herpesviruses. 2nd ed. Totowa: Springer; 1998. p. 89–101.CrossRef
43.
go back to reference Zigeuner R, Ratschek M, Rehak P, et al. Value of p53 as a prognostic marker in histologic subtypes of renal cell carcinoma: a systematic analysis of primary and metastatic tumor tissue. Urology. 2004;63(4):651–5.PubMedCrossRef Zigeuner R, Ratschek M, Rehak P, et al. Value of p53 as a prognostic marker in histologic subtypes of renal cell carcinoma: a systematic analysis of primary and metastatic tumor tissue. Urology. 2004;63(4):651–5.PubMedCrossRef
44.
go back to reference Kankuri M, Söderström KO, Pelliniemi TT, et al. The association of immunoreactive p53 and Ki-67 with T-stage, grade, occurrence of metastases and survival in renal cell carcinoma. Anticancer Res. 2006;26(5B):3825–33.PubMed Kankuri M, Söderström KO, Pelliniemi TT, et al. The association of immunoreactive p53 and Ki-67 with T-stage, grade, occurrence of metastases and survival in renal cell carcinoma. Anticancer Res. 2006;26(5B):3825–33.PubMed
45.
go back to reference Olumi AF, Weidner N, Presti JC Jr. p53 immunoreactivity correlates with Ki-67 and bcl-2 expression in renal cell carcinoma. Urol Oncol. 2001;6(2):63–7. Olumi AF, Weidner N, Presti JC Jr. p53 immunoreactivity correlates with Ki-67 and bcl-2 expression in renal cell carcinoma. Urol Oncol. 2001;6(2):63–7.
46.
go back to reference Gabrielli Fregonesi PA, Teresa DB, Duarte RA, et al. p16INK4A immunohistochemical overexpression in premalignant and malignant oral lesions infected with human papillomavirus. J Histochem Cytochem. 2003;51(10):1291–7.CrossRef Gabrielli Fregonesi PA, Teresa DB, Duarte RA, et al. p16INK4A immunohistochemical overexpression in premalignant and malignant oral lesions infected with human papillomavirus. J Histochem Cytochem. 2003;51(10):1291–7.CrossRef
47.
go back to reference Farhadi A, Behzad-Behbahani A, Geramizadeh B, et al. High-risk human papillomavirus infection in different histological subtypes of renal cell carcinoma. J Med Virol. 2014;86(7):1134–44.PubMedCrossRef Farhadi A, Behzad-Behbahani A, Geramizadeh B, et al. High-risk human papillomavirus infection in different histological subtypes of renal cell carcinoma. J Med Virol. 2014;86(7):1134–44.PubMedCrossRef
48.
go back to reference Zhou S, Ye W, Shao Q, et al. Prognostic significance of XIAP and NF-κB expression in esophageal carcinoma with postoperative radiotherapy. World J Surg Oncol. 2013;11(1):1–7.CrossRef Zhou S, Ye W, Shao Q, et al. Prognostic significance of XIAP and NF-κB expression in esophageal carcinoma with postoperative radiotherapy. World J Surg Oncol. 2013;11(1):1–7.CrossRef
50.
go back to reference Kim KH, Han EM, Lee ES, et al. Epstein–Barr virus infection in sarcomatoid renal cell carcinoma tissues. BJU Int. 2005;96(4):547–52.PubMedCrossRef Kim KH, Han EM, Lee ES, et al. Epstein–Barr virus infection in sarcomatoid renal cell carcinoma tissues. BJU Int. 2005;96(4):547–52.PubMedCrossRef
52.
go back to reference Hainaut P, Soussi T, Shomer B, et al. Database of p53 gene somatic mutations in human tumors and cell lines: updated compilation and future prospects. Nucleic Acids Res. 1997;25(1):151–7.PubMedPubMedCentralCrossRef Hainaut P, Soussi T, Shomer B, et al. Database of p53 gene somatic mutations in human tumors and cell lines: updated compilation and future prospects. Nucleic Acids Res. 1997;25(1):151–7.PubMedPubMedCentralCrossRef
53.
go back to reference Noon AP, Vlatković N, Polański R, et al. p53 and MDM2 in renal cell carcinoma: biomarkers for disease progression and future therapeutic targets? Cancer. 2010;116(4):780–90.PubMedCrossRef Noon AP, Vlatković N, Polański R, et al. p53 and MDM2 in renal cell carcinoma: biomarkers for disease progression and future therapeutic targets? Cancer. 2010;116(4):780–90.PubMedCrossRef
54.
go back to reference Hodges A, Talley L, Gokden N. Human Papillomavirus DNA and P16INK4A are not detected in renal tumors with immunohistochemistry and signal-amplified in situ hybridization in paraffin-embedded tissue. Appl Immunohistochem Mol Morphol. 2006;14(4):432–5.PubMedCrossRef Hodges A, Talley L, Gokden N. Human Papillomavirus DNA and P16INK4A are not detected in renal tumors with immunohistochemistry and signal-amplified in situ hybridization in paraffin-embedded tissue. Appl Immunohistochem Mol Morphol. 2006;14(4):432–5.PubMedCrossRef
55.
go back to reference Ikuerowo SO, Kuczyk MA, von Wasielewski R, et al. p16INK4a expression and clinicopathologic parameters in renal cell carcinoma. Eur Urol. 2007;51(3):732–8.PubMedCrossRef Ikuerowo SO, Kuczyk MA, von Wasielewski R, et al. p16INK4a expression and clinicopathologic parameters in renal cell carcinoma. Eur Urol. 2007;51(3):732–8.PubMedCrossRef
56.
go back to reference Yildiz E, Gokce G, Kilicarslan H, et al. Prognostic value of the expression of Ki-67, CD44 and vascular endothelial growth factor, and microvessel invasion, in renal cell carcinoma. BJU Int. 2004;93(7):1087–93.PubMedCrossRef Yildiz E, Gokce G, Kilicarslan H, et al. Prognostic value of the expression of Ki-67, CD44 and vascular endothelial growth factor, and microvessel invasion, in renal cell carcinoma. BJU Int. 2004;93(7):1087–93.PubMedCrossRef
57.
go back to reference Bui MH, Visapaa H, Seligson D, et al. Prognostic value of carbonic anhydrase IX and KI67 as predictors of survival for renal clear cell carcinoma. J Urol. 2004;171(6 Part 1):2461–6.PubMedCrossRef Bui MH, Visapaa H, Seligson D, et al. Prognostic value of carbonic anhydrase IX and KI67 as predictors of survival for renal clear cell carcinoma. J Urol. 2004;171(6 Part 1):2461–6.PubMedCrossRef
58.
go back to reference Phuoc NB, Ehara H, Gotoh T, et al. Immunohistochemical analysis with multiple antibodies in search of prognostic markers for clear cell renal cell carcinoma. Urology. 2007;69(5):843–8.PubMedCrossRef Phuoc NB, Ehara H, Gotoh T, et al. Immunohistochemical analysis with multiple antibodies in search of prognostic markers for clear cell renal cell carcinoma. Urology. 2007;69(5):843–8.PubMedCrossRef
59.
go back to reference Rioux-Leclercq N, Turlin B, Bansard JY, et al. Value of immunohistochemical Ki-67 and p53 determinations as predictive factors of outcome in renal cell carcinoma. Urology. 2000;55(4):501–5.PubMedCrossRef Rioux-Leclercq N, Turlin B, Bansard JY, et al. Value of immunohistochemical Ki-67 and p53 determinations as predictive factors of outcome in renal cell carcinoma. Urology. 2000;55(4):501–5.PubMedCrossRef
60.
go back to reference Luo Y, Liu Y, Wang C, et al. Signaling pathways of EBV-induced oncogenesis. Cancer Cell Int. 2021;21(1):1–11.CrossRef Luo Y, Liu Y, Wang C, et al. Signaling pathways of EBV-induced oncogenesis. Cancer Cell Int. 2021;21(1):1–11.CrossRef
61.
go back to reference Pakdel F, Farhadi A, Pakdel T, et al. The frequency of high-risk human papillomavirus types, HPV16 lineages, and their relationship with p16 INK4a and NF-κB expression in head and neck squamous cell carcinomas in Southwestern Iran. Braz J Microbiol. 2021;52(1):195–206.PubMedCrossRef Pakdel F, Farhadi A, Pakdel T, et al. The frequency of high-risk human papillomavirus types, HPV16 lineages, and their relationship with p16 INK4a and NF-κB expression in head and neck squamous cell carcinomas in Southwestern Iran. Braz J Microbiol. 2021;52(1):195–206.PubMedCrossRef
63.
go back to reference Chen C, Edelstein LC, Gélinas C. The Rel/NF-κB family directly activates expression of the apoptosis inhibitor Bcl-xL. Mol Cell Biol. 2000;20(8):2687–95.PubMedPubMedCentralCrossRef Chen C, Edelstein LC, Gélinas C. The Rel/NF-κB family directly activates expression of the apoptosis inhibitor Bcl-xL. Mol Cell Biol. 2000;20(8):2687–95.PubMedPubMedCentralCrossRef
64.
go back to reference Meteoglu I, Erdogdu IH, Meydan N, et al. NF-KappaB expression correlates with apoptosis and angiogenesis in clear cell renal cell carcinoma tissues. J Exp Clin Cancer Res. 2008;27(1):1–9.CrossRef Meteoglu I, Erdogdu IH, Meydan N, et al. NF-KappaB expression correlates with apoptosis and angiogenesis in clear cell renal cell carcinoma tissues. J Exp Clin Cancer Res. 2008;27(1):1–9.CrossRef
Metadata
Title
Epstein–Barr virus infection is associated with the nuclear factor-kappa B p65 signaling pathway in renal cell carcinoma
Authors
Ali Farhadi
Sepide Namdari
Pei Pei Chong
Bita Geramizadeh
Abbas Behzad-Behbahani
Zamberi Sekawi
Sedigheh Sharifzadeh
Publication date
01-12-2022
Publisher
BioMed Central
Published in
BMC Urology / Issue 1/2022
Electronic ISSN: 1471-2490
DOI
https://doi.org/10.1186/s12894-022-00964-2

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