The Influence of Oncogenic Viruses in Renal Carcinogenesis: Pros and Cons
Abstract
:1. Introduction
2. Renal Cell Carcinoma: Carcinogenesis Mechanisms of Oncogenic Viruses
2.1. Polyomaviridae Family
BKPyV Carcinogenesis
2.2. Herpesviridae Family
2.2.1. EBV Carcinogenesis
2.2.2. KSHV Carcinogenesis in RCC
2.3. Flaviviridae Family
HCV Carcinogenesis
2.4. Papillomaviridae Family
HPV Carcinogenesis
3. Discussion
3.1. Towards a Standardized Approach for Testing Oncogenic Viruses in Kidney and Bladder Malignancies
3.2. The Benefit of Oncolytic Viral Therapy
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Authors, Year, Country | Sample Type | BKPyV Detection Assay/Status | Results | Novelty |
---|---|---|---|---|
Loria SJ et al., 2022 New York, NY, USA [60] | Cadaveric renal transplant | Persistent BKPyV viruria | Invasive small cell bladder carcinoma, with prominent adenocarcinoma component | Molecular evidence of BKPyV DNA in the bladder cancer cells |
Chen JM et al., 2021 New York, NY, USA [61] | Kidney transplantation | High-grade UCa | Tumor had metastasized to one left obturator lymph node but spared the two native kidneys and ureters |
|
Meier RPH et al., 2021 Geneva, Switzerland [19] | Kidney–pancreas female recipient with a history of BKPyV nephritis | Whole-genome sequencing of the tumor confirmed multiple BKPyV genome integrations; persistently elevated anti-BKPyV IgG titres and a specific anti-BKPyV T cell response | Presence of BKPyV oncogenic large tumor antigen (LT-Ag) was identified in large amount within the kidney tumor | Potential oncogenic role of BKPyV in collecting duct carcinoma in renal allografts |
Borgogna C et al., 2021 Novara, Italy [15] | ccRCC and UCa | IHC and fluorescent in situ hybridization (FISH) for detection of BKPyV infection |
| Highlighting the association between BKPyV reactivation and cancer development in KTRs |
Cuenca AG et al., 2020 Boston, USA [62] | BKPyV-associated nephropathy and, 6 years later, locally advanced UCa | Bioptic confirmation of BKPyV nephropathy | BKPyV DNA was detected in urine at values greater than 500 × 106 copies/mL | IHC for BKPyV LT-Ag |
Wang Y et al., 2020 Guangzhou, China [20] | BKPyV-associated UCa after renal transplantation | Next-generation virome capture sequencing | 332 viral integration sites were identified in the six tumors | Integration of BKPyV was a continuous process occurring in both primary and metastatic tumors, generating heterogenous tumor cell populations |
Querido S et al., 2020 Lisbon, Portugal [63] | KTR who developed a high-grade UCa 5 years after a diagnosis of JCV nephropathy and 9 years after kidney transplantation | Neoplastic tissue was positive for JCPyV DNA by RT-PCR | IHC staining showed strong positivity for early viral protein JCV LT-ag, using a broad polyomavirus antibody | The first report of high-grade UCa associated with JCPyV nephropathy in a KTR |
Chu YH et al., 2020 Madison, WI, USA [64] | Post-transplantation UCa and RCC | LT-Ag-expressing UCas were high-grade, with p16 and p53 overexpression | Tumor genome sequencing revealed BKPyV integration | Post-renal transplantation BKPyV-associated UCas are aggressive and genetically distinct from most non-BKPyV-related UCas |
Singh G et al., 2019 New Delhi, India [65] | Plasma urine kidney biopsy | IHC qPCR |
| Rare scenario of the development of a pelvic BK polyoma virus-associated UCa in the nonfunctioning graft of the recipient of a second kidney |
Odetola OE et al., 2018 Maywood, IL, USA [24] | Case 1: serum BKPyV titers | BKPyV viremia recurred and peaked at 1 year post-transplantation | Both on the smears and resection specimens, the neoplastic cells were found to be positive for SV40 |
|
Case 2: serum BKPyV titers | Bladder barbotage urine specimen showed decoy cells | Tumor cells were positive for SV40 | ||
Fu F et al., 2018 Guangzhou, China [66] |
Urine FFPE frozen graft tumor tissue | qPCR IHC Deep sequencing and sequence analysis | Integration of genotype IV BKPyV genome into the non-coding RNA (ncRNA) intronic region of human chromosome 18 | BKPyV integrated into human genome at new breakpoints and revealed the potential oncogenic mechanism of BKPyV |
Csoma E et al., 2016 Debrecen, Hungary [67] | FFPE renal neoplasms, bladder cancer and kidney biopsy | RT and nested PCR | Malignant renal tumors (0/89); urinary bladder carcinoma (0/76) | There is no evidence that WUPyV, KIPyV or HPyV9 have any role in oncogenesis |
Kenan DJ et al., 2015 Chapel Hill, NC, USA [21] | FFPE high-grade UCa arising in a renal allograft | Laser capture microdissection RT-PCR Deep sequencing and sequence analysis |
| First evidence for a high-grade UCa arising in a renal allograft associated with BKPyV fully integrated into the tumor genome at a single location |
Saleeb R et al., 2015 Toronto, Canada [68] | High-grade UCa in allograft kidney and bladder | PCR | BKPyV genome present in tumor | A significant proportion of malignancies developed in a renal transplant cohort (4 out of 106 patients, 3.8%) |
Bulut Y et al., 2013 Elazig, Turkey [16] | FFPE RCC | Nested PCR for detection of BKPyV DNA and real-time RT-PCR for determining mRNA levels of BKPyV | BKPyV VP1 was present in 69.5% of the BKPyV DNA positive samples | Presence of BKPyV DNA resulted in a fivefold increase in the risk of development of RCC |
Neirynck V et al., 2012 Brussels, Belgium [69] | FFPE RCC | IHC of SV40 | SV40-positive RCC in allograft | BKPyV plays a role in the occurrence of RCC |
Authors Year, Country | Sample Type | Herpes Viruses Detection Assay/Status | Results | Novelty |
---|---|---|---|---|
Farhadi A et al., 2022 Shiraz, Iran [36] | FFPE RCC | Nested PCR for EBV DNA amplification | EBV was found to be significantly associated with RCC | p65 NF-κB signaling pathway is involved in EBV-mediated RCC pathogenesis |
Dornieden T et al., 2021 Berlin, Germany [70] | Lymphocytes derived from blood FFPE RCC | Flow cytometry; highly advanced histology (multi-epitope ligand cartography) methods |
| Extensive overview of tissue-resident memory T cells’ phenotypes and functions in the human kidney presented for the first time, pointing toward their potential relevance in kidney transplantation |
Kryst P et al., 2020 Warsaw, Poland [33] | Partial or radical nephrectomy FFPE RCC | Isolation of the nucleic acids from plasma | Viral infections were diagnosed in ten patients (37.0%):
| EBV and ADV infections are common in RCC patients and increase the risk of high-grade RCC |
Karaarslan S et al., 2018 Izmir, Turkey [71] | FFPE RCC | EBV-encoded early RNA EBER—in situ hybridization EBER probe |
| EBV may contribute to tumor development as an etiological factor in patients with RCC |
Kang MJ et al., 2013 Jeonbuk, Korea [72] | FFPE ccRCC | EBER—in situ hybridization EBER probe | EBV positivity in 67/140 ccRCCs | EBV infection was significantly associated with poor survival of ccRCC patients |
Hesser CR et al., 2018 Berkeley, CA, USA [73] | KSHV-positive RCC cell line | Cell culture siRNA experiments RT-qPCR | Methylation at the N6 position of adenosine is centrally involved in regulating KSHV gene expression | KSHV reactivation |
Ghaninejad H et al., 2009 Tehran, Iran [74] | Renal transplantation | Dermatological examination | 2 cases of Kaposi’s sarcoma | Kaposi’s sarcoma described as most common post-transplant cancer in developing countries |
Authors Year, Country | Sample Type | Hepatitis Virus Detection Assay/Status | Results | Novelty |
---|---|---|---|---|
Ma Y et al., 2021 Sichuan, China [46] | FFPE RCC | Positive for anti-HCV and HCV-RNA analysis by RT-PCR | The association of HCV with RCC was most strong (RR = 1.71) in the USA | HCV infection was significantly associated with increased RCC risk |
Rangel JCA et al., 2021 Rio de Janeiro, Brazil [48] | FFPE RCC | Antibodies against HCV | 4.1% HCV infection from all RCC tested samples | A 3-fold higher prevalence of HCV infection identified among patients with RCC, compared to the general Brazilian population |
Liţescu M et al., 2020 Bucharest, Romania [75] | * Primary renal lymphoma | Initiation of direct-acting antiviral therapy | Child–Pugh class A HCV cirrhosis | Discovered incidentally in a patient investigated for HCV |
Cormio L et al., 2017 Foggia, Italy [76] | Uca plasmocytoid variant bladder metastasis | 74-year-old woman with HCV-related liver cirrhosis | Ascites and no urinary or other symptoms | First reported case of asymptomatic UCa and associated metastasis of hepatocellular carcinoma |
Akar E et al., 2019 Istanbul, Turkey [77] | Metastatic RCC | 60-year-old man, 16 months after sunitinib initiation | Elevated liver enzymes and hepatitis D virus infection reactivation in the HBsAg-positive patient | Cancer patients should be screened for viral hepatitis prior to immunosuppressive therapy or chemotherapy |
Authors Year, Country | Sample Type | HPV Detection Assay/Status | Results | Novelty |
---|---|---|---|---|
Henley JK et al., 2017 Danville, PA, USA [78] | Skin biopsy | Enlarged keratinocytes with blue cytoplasm and hypergranulosis characteristic of epidermodysplasia verruciformis (EDV)—features suggestive for HPV infection | Renal transplantation 7 years prior | Rare case of acquired EDV in a solid organ transplant recipient |
Farhadi A et al., 2014 Serdang, Malaysia [79] | FFPE RCC | MY/GP+ consensus primers and HPV-16/18 type specific nested PCRs followed by direct sequencing | HPV genome was detected in 37 cases (30.3%) HPV-18 was the most common viral type identified followed by HPV-16 and HPV-58 | Results indicate an association of HR-HPV types with RCC |
Virus Type | Tumor Type in Renal Allograft | IHC Viral Marker | IHC Associated Markers | References |
---|---|---|---|---|
BKPyV | RCC—collecting duct carcinoma | SV40 | PAX8, E-cadherin, CK7, INI1, CA9, vimentin, CK20, GATA3, p504S | Dao M et al., 2018 [80] |
RCC | SV40 | Pankeratin, CK7, vimentin, EMA, CK20, S100, HMB45, CD45 | Narayanan M et al., 2007 [18] | |
RCC | SV40 | p53 | Singh G et al., 2019 [65] | |
Bladder adenocarcinoma UCa | SV40 | PAX8, CK7, p53, p16 | Odetola OE et al., 2018 [24] | |
EBV | RCC | EBV LMP-1; EBNA-2; BZLF1 | CD79a, CD3, CD68, CD56, CD21, VS38 | Kim KH et al., 2005 [35] |
RCC | p53, p16, Ki-67, NF-κB | Farhadi A, 2022 [36] | ||
HCV | RCC | NS3, NS5A | p53, p21 | Ahmed et al., 2016 [81] |
HPV | RCC | HPLV1 capsid protein | p16 | Farhadi A et al., 2014 [79] |
RCC | PCNA, p53 CM-1, p53 DO-7 | Kamel D et al., 1994 [82] | ||
HHV-8 | Kaposi sarcoma | HHV8 | CD34, CD8, CD19, CD69 | Dudderidge TJ et al., 2007 [83] |
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Manole, B.; Damian, C.; Giusca, S.-E.; Caruntu, I.D.; Porumb-Andrese, E.; Lunca, C.; Dorneanu, O.S.; Iancu, L.S.; Ursu, R.G. The Influence of Oncogenic Viruses in Renal Carcinogenesis: Pros and Cons. Pathogens 2022, 11, 757. https://doi.org/10.3390/pathogens11070757
Manole B, Damian C, Giusca S-E, Caruntu ID, Porumb-Andrese E, Lunca C, Dorneanu OS, Iancu LS, Ursu RG. The Influence of Oncogenic Viruses in Renal Carcinogenesis: Pros and Cons. Pathogens. 2022; 11(7):757. https://doi.org/10.3390/pathogens11070757
Chicago/Turabian StyleManole, Bianca, Costin Damian, Simona-Eliza Giusca, Irina Draga Caruntu, Elena Porumb-Andrese, Catalina Lunca, Olivia Simona Dorneanu, Luminita Smaranda Iancu, and Ramona Gabriela Ursu. 2022. "The Influence of Oncogenic Viruses in Renal Carcinogenesis: Pros and Cons" Pathogens 11, no. 7: 757. https://doi.org/10.3390/pathogens11070757
APA StyleManole, B., Damian, C., Giusca, S.-E., Caruntu, I. D., Porumb-Andrese, E., Lunca, C., Dorneanu, O. S., Iancu, L. S., & Ursu, R. G. (2022). The Influence of Oncogenic Viruses in Renal Carcinogenesis: Pros and Cons. Pathogens, 11(7), 757. https://doi.org/10.3390/pathogens11070757