Polyomavirus BK-Specific CD4+ T Cells Response to VP1 Stimulation in Kidney Transplant Recipients
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Abstract
Reactivation of Polyomavirus BK (BKPyV) is related to reduction of T cells response in kidney transplant recipients (KTRs). Here, we examined the differentiation of CD4+ T cells subsets in response to BKPyV KTRs, using the BKPyV VP1 (viral capsid protein 1) as a stimulator.
We categorized our samples into three distinct groups: 1. Reactive BKPyV (BKPyV+), 2. non-reactive (BKPyV-) KTRs and 3. Healthy controls. BKPyV- KTRs and healthy controls stimulated with VP1 and BKPyV+ unstimulated with VP1. The human CD4+ T cells was stimulation with VP1-Ag. The proportion of CD4+ T lymphocytes and their various subsets, including naive T cells, central memory T cells (TCM), and effector memory T cells (TEM) was measured using flowcytometry.
BKPyV- KTRs VP1+ indicated significantly lower TCM CD4+ T cells in contrast with both BKPyV+ KTRs VP1-, and healthy controls VP1+. This indicates that VP1 stimulation may reduce TCM cell levels in these patients. The percentage of TEM in the BKPyV- KTRs VP1+ group was significantly less prevalent than the BKPyV+ KTRs VP1- group. The percentage of TEM cells in BKPyV+ KTRs VP1- was significantly lower than the healthy controls VP1+. Stimulation with VP1 protein significantly increased the frequency of cytotoxic CD4+ T cells in BKPyV- KTRs VP1+ compared to BKPyV+ KTRs VP1-.
The present research has shown that the VP1 stimulation of CD4+ T cells can induce cytotoxic CD4+ T cells responses that may help overcome BKPyV infection in KTRs. However, VP1 stimulation may also differentially affect TCM and TEM CD4+ T cells subsets.
1. Cohen-Bucay A, Ramirez S, Gordon CE, Francis JM, Chitalia V. Advances in BK Virus Complications in Organ Transplantation and Beyond. Kidney Med. 2020;2(6):771-6.
2. Shen CL, Wu BS, Lien TJ, Yang AH, Yang CY. BK polyomavirus nephropathy in kidney transplantation: balancing rejection and infection. Viruses. 2021;16;13(3):487.
3. Yogo Y, Sugimoto C, Zhong S, Homma Y. Evolution of the BK polyomavirus: epidemiological, anthropological and clinical implications. Rev Med Virol. 2009;19(4):185-99.
4. Flægstad T, Rönne K, Filipe AR, Traavik T. Prevalence of anti BK virus antibody in Portugal and Norway. Scand J Infect Dis. 1989;21(2):145-7.
5. Stolt A, Sasnauskas K, Koskela P, Lehtinen M, Dillner J. Seroepidemiology of the human polyomaviruses. Journal of General Virology. 2003;84(6):1499-504.
6. Pakfetrat M, Yaghobi R, Salmanpoor Z, Roozbeh J, Torabinezhad S, Kadkhodaei S. Frequency of polyomavirus BK infection in kidney transplant patients suspected to nephropathy. Int J Organ Transplant Med. 2015;6(2):77.
7. Hurdiss DL, Morgan EL, Thompson RF, Prescott EL, Panou MM, Macdonald A, et al. New structural insights into the genome and minor capsid proteins of BK polyomavirus using cryo-electron microscopy. Structure. 2016;24(4):528-36.
8. Noshadi N, Yaghoubi R, Afshari A, Forouzanfar M. Impaired CD4+ Cytotoxic T Lymphocyte Activity in Polyomavirus BK Infected Kidney Transplant Recipients. Iranian J AllergyBAsthma Immunol. 2023:1-11.
9. Yang L, Chen H, Liu L, Song J, Feng T, Li Y, et al. Foot-and-mouth disease virus VP1 promotes viral replication by regulating the expression of chemokines and GBP1. Frontiers in Veterinary Science. 2022 Jul 22; 9:937409.
10. Foroudi MR, Yaghobi R, Afshari A, Roozbeh J, Miresmaeili SM, Javid A. The effect of BK polyomavirus large T antigen on CD4 and CD8 T cells in kidney transplant recipients. Transplant Immunol. 2022; 74:101655.
11. Seemayer CA, Seemayer NH, Dürmüller U, Gudat F, Schaub S, Hirsch HH, et al. BK virus large T and VP-1 expression in infected human renal allografts. Nephrol Dialysis Transplant. 2008 Dec 1;23(12):3752-61.
12. Hale AD, Dargevičiūt A, Jin L, Knowles W, Staniulis J, Brown DW, et al. Expression and antigenic characterization of the major capsid proteins of human polyomaviruses BK and JC in Saccharomyces cerevisiae. J Virol Methods. 2002;104(1):93-8.
13. Jozpanahi M, Ramezani A, Ossareh S, Banifazl M, Bavand A, Mamishi S, et al. BK viremia among Iranian Renal transplant candidates. Iranian J Pathol. 2016;11(3):210.
14. Rahimi Z, Yaghobi R, Afshari A, Roozbeh J, Mokhtari MJ, Hosseini AM. The effect of BKV reactivation on cytokines behavior in kidney transplanted patients. BMC Nephrol. 2022;23(1):20.
15. Foroudi MR, Yaghobi R, Afshari A, Roozbeh J, Miresmaeili SM, Javid A. The effect of the BK polyomavirus large T antigen on the function and maturity of the CD4+ T cell subsets in kidney transplant recipients. Transplant Immunol. 2023;80(14):101884.
16. Cimbaluk D, Pitelka L, Kluskens L, Gattuso P. Update on human polyomavirus BK nephropathy. Diagnostic cytopathology. 2009;37(10):773-9.
17. Van Aalderen M, Heutinck K, Huisman C, Ten Berge I. BK virus infection in transplant recipients: clinical manifestations, treatment options and the immune response. Neth J Med. 2012;70(4):172-83.
18. Gupta N, Lawrence RM, Nguyen C, Modica RF. BK virus in systemic lupus erythematosus. Pediatric Rheumatol. 2015;13(1):1-11.
19. Kariminik A, Yaghobi R, Dabiri S. Association of BK Virus Infection with CXCL11 Gene Expression and Protein Levels in Kidney Transplant Patients. Experimental and clinical transplantation: official journal of the Middle East Society for Organ Transplant. 2016;16(1):50-4.
20. Malekshahi SS, Soleimanjahi H, Dorostkar F, Salimi V, Farahmand M. Survey of BK Virus in Renal Transplant Recipients in Iran: A Systematic Review and Meta-Analysis. Intervirology. 2021;64(1):27-35.
21. Zareei N, Miri HR, Karimi MH, Afshari A, Geramizadeh B, Roozbeh J, et al. Increasing of the interferon-γ gene expression during polyomavirus BK infection in kidney transplant patients. Microbial pathogenesis. 2019; 129:187-94.
22. Blyth E, Clancy L, Simms R, Gaundar S, O'Connell P, Micklethwaite K, et al. BK virus-specific T cells for use in cellular therapy show specificity to multiple antigens and polyfunctional cytokine responses. Transplantation. 2011;92(10):1077-84.
23. Comoli P, Basso S, Azzi A, Moretta A, De Santis R, Del Galdo F, et al. Dendritic cells pulsed with polyomavirus BK antigen induce ex vivo polyoma BK virus–specific cytotoxic T-cell lines in seropositive healthy individuals and renal transplant recipients. J Am Society Nephrol. 2003;14(12):3197-204.
24. Weist B, Schmueck M, Fuehrer H, Sattler A, Reinke P, Babel N. The role of CD4+ T cells in BKV-specific T cell immunity. Med Microbiol Immunol. 2014; 203:395-408.
25. Okada R, Kondo T, Matsuki F, Takata H, Takiguchi M. Phenotypic classification of human CD4+ T cell subsets and their differentiation. Int Immunol. 2008;20(9):1189-99.
26. Zhou W, Sharma M, Martinez J, Srivastava T, Diamond DJ, Knowles W, et al. Functional characterization of BK virus-specific CD4+ T cells with cytotoxic potential in seropositive adults. Viral immunology. 2007;20(3):379-88.
27. Pachnio A, Ciaurriz M, Begum J, Lal N, Zuo J, Beggs A, et al. Cytomegalovirus infection leads to development of high frequencies of cytotoxic virus-specific CD4+ T cells targeted to vascular endothelium. PLoS pathogens. 2016;12(9): e1005832.
28. Liechti T, Roederer M. OMIP‐060: 30‐parameter flow cytometry panel to assess T cell effector functions and regulatory T cells. Cytometry Part A. 2019;95(11):1129-34.
29. Trapani JA, Smyth MJ. Functional significance of the perforin/granzyme cell death pathway. Nat Rev Immunol. 2002;2(10):735-47.
30. Parajuli S, Jorgenson M, Meyers RO, Djamali A, Galipeau J. Role of Virus-Specific T cell therapy for Cytomegalovirus and BK infections in kidney transplant recipients. Kidney360. 2021;2(5):905.
31. Li P, Cheng D, Wen J, Ni X, Li X, Xie K, et al. The immunophenotyping of different stages of BK virus allograft nephropathy. Renal failure. 2019;41(1):855-61.
32. Snyder LD, Chan C, Kwon D, Yi JS, Martissa JA, Copeland CAF, et al. Polyfunctional T-cell signatures to predict protection from cytomegalovirus after lung transplantation. Am J Res Critical Care Med. 2016;193(1):78-85.
33. Stervbo U, Nienen M, Weist BJ, Kuchenbecker L, Hecht J, Wehler P, et al. BKV clearance time correlates with exhaustion state and T-cell receptor repertoire shape of BKV-specific T-cells in renal transplant patients. Front Immunol. 2019;10:767.
34. van Aalderen MC, Remmerswaal EB, Heutinck KM, Ten Brinke A, Feltkamp MC, van der Weerd NC, et al. Clinically relevant reactivation of polyomavirus BK (BKPyV) in HLA-A02-positive renal transplant recipients is associated with impaired effector-memory differentiation of BKPyV-specific CD8+ T cells. PLoS Pathogens. 2016;12(10): e1005903.
35. Dekeyser M, François H, Beaudreuil S, Durrbach A. Polyomavirus-specific cellular immunity: from BK-virus-specific cellular immunity to BK-virus-associated nephropathy? Front Immunol. 2015; 6:307.
36. Binggeli S, Egli A, Schaub S, Binet I, Mayr M, Steiger J, et al. Polyomavirus BK‐specific cellular immune response to VP1 and large T‐antigen in kidney transplant recipients. Am J Transplant. 2007;7(5):1131-9.
37. Fan Y, Bai H, Qian Y, Sun Z, Shi B. CD4+ T cell immune response to VP1 and VP3 in BK virus infected recipients of renal transplantation. Surgical Infect. 2019;20(3):236-43.
38. Bruminhent J, Srisala S, Klinmalai C, Pinsai S, Watcharananan SP, Kantachuvesiri S, et al. BK Polyomavirus-specific T cell immune responses in kidney transplant recipients diagnosed with BK Polyomavirus-associated nephropathy. BMC Infect Dis. 2019;19:1-8.
39. Ahrends T, Busselaar J, Severson TM, Bąbała N, de Vries E, Bovens A, et al. CD4+ T cell help creates memory CD8+ T cells with innate and help-independent recall capacities. Nat Commun. 2019;10(1):5531.
40. Weist BJ, Wehler P, El Ahmad L, Schmueck-Henneresse M, Millward JM, Nienen M, et al. A revised strategy for monitoring BKV-specific cellular immunity in kidney transplant patients. Kidney International. 2015;88(6):1293-303.
41. Letsch A, Knoedler M, Na IK, Kern F, Asemissen AM, Keilholz U, et al. CMV‐specific central memory T cells reside in bone marrow. Europ J Immunol. 2007 Nov;37(11):3063-8.
42. van Doesum WB, Abdulahad WH, van Dijk MC, Dolff S, van son WJ, Stegeman CA, et al. Characterization of urinary CD 4+ and CD 8+ T cells in kidney transplantation patients with polyomavirus BK infection and allograft rejection. Transplant Infectious Disease. 2014 Oct;16(5):733-43.
43. Ambalathingal GR, Francis RS, Corvino D, Srihari S, Aftab BT, Smith C, et al. Proteome‐wide analysis of T‐cell response to BK polyomavirus in healthy virus carriers and kidney transplant recipients reveals a unique transcriptional and functional profile. Clin Trans Immunol. 2020;9(1):e01102.
44. Alonso Arias R, Moro-García MA, Echeverria A, Solano-Jaurrieta JJ, Suárez-García FM, López-Larrea C. Intensity of the humoral response to cytomegalovirus is associated with the phenotypic and functional status of the immune system. J Virol. 2013;87(8):4486-95.
45. Zhang W, Morris AB, Peek EV, Karadkhele G, Kissick HT, Larsen CP. CMV status drives distinct trajectories of CD4+ T cell differentiation. Front Immunol. 2021 Apr 15; 12:620386.
46. Palma JP, Yauch RL, Lang S, Kim BS. Potential role of CD4+ T cell-mediated apoptosis of activated astrocytes in Theiler’s virus-induced demyelination. J Immunology. 1999;162(11):6543-51.
47. Comoli P, Hirsch HH, Ginevri F. Cellular immune responses to BK virus. Curr Opin Organ Transplann. 2008;13(6):569-74.
48. Espada E, Cheng MP, Kim HT, Woolley AE, Avigan JI, Forcade E, et al. BK virus–specific T-cell immune reconstitution after allogeneic hematopoietic cell transplantation. Blood Advances. 2020;4(9):1881-93.
49. Schaenman JM, Korin Y, Sidwell T, Kandarian F, Harre N, Gjertson D, et al. Increased frequency of BK virus-specific polyfunctional CD8+ T cells predict successful control of BK viremia after kidney transplantation. Transplantation. 2017;101(6):1479.
2. Shen CL, Wu BS, Lien TJ, Yang AH, Yang CY. BK polyomavirus nephropathy in kidney transplantation: balancing rejection and infection. Viruses. 2021;16;13(3):487.
3. Yogo Y, Sugimoto C, Zhong S, Homma Y. Evolution of the BK polyomavirus: epidemiological, anthropological and clinical implications. Rev Med Virol. 2009;19(4):185-99.
4. Flægstad T, Rönne K, Filipe AR, Traavik T. Prevalence of anti BK virus antibody in Portugal and Norway. Scand J Infect Dis. 1989;21(2):145-7.
5. Stolt A, Sasnauskas K, Koskela P, Lehtinen M, Dillner J. Seroepidemiology of the human polyomaviruses. Journal of General Virology. 2003;84(6):1499-504.
6. Pakfetrat M, Yaghobi R, Salmanpoor Z, Roozbeh J, Torabinezhad S, Kadkhodaei S. Frequency of polyomavirus BK infection in kidney transplant patients suspected to nephropathy. Int J Organ Transplant Med. 2015;6(2):77.
7. Hurdiss DL, Morgan EL, Thompson RF, Prescott EL, Panou MM, Macdonald A, et al. New structural insights into the genome and minor capsid proteins of BK polyomavirus using cryo-electron microscopy. Structure. 2016;24(4):528-36.
8. Noshadi N, Yaghoubi R, Afshari A, Forouzanfar M. Impaired CD4+ Cytotoxic T Lymphocyte Activity in Polyomavirus BK Infected Kidney Transplant Recipients. Iranian J AllergyBAsthma Immunol. 2023:1-11.
9. Yang L, Chen H, Liu L, Song J, Feng T, Li Y, et al. Foot-and-mouth disease virus VP1 promotes viral replication by regulating the expression of chemokines and GBP1. Frontiers in Veterinary Science. 2022 Jul 22; 9:937409.
10. Foroudi MR, Yaghobi R, Afshari A, Roozbeh J, Miresmaeili SM, Javid A. The effect of BK polyomavirus large T antigen on CD4 and CD8 T cells in kidney transplant recipients. Transplant Immunol. 2022; 74:101655.
11. Seemayer CA, Seemayer NH, Dürmüller U, Gudat F, Schaub S, Hirsch HH, et al. BK virus large T and VP-1 expression in infected human renal allografts. Nephrol Dialysis Transplant. 2008 Dec 1;23(12):3752-61.
12. Hale AD, Dargevičiūt A, Jin L, Knowles W, Staniulis J, Brown DW, et al. Expression and antigenic characterization of the major capsid proteins of human polyomaviruses BK and JC in Saccharomyces cerevisiae. J Virol Methods. 2002;104(1):93-8.
13. Jozpanahi M, Ramezani A, Ossareh S, Banifazl M, Bavand A, Mamishi S, et al. BK viremia among Iranian Renal transplant candidates. Iranian J Pathol. 2016;11(3):210.
14. Rahimi Z, Yaghobi R, Afshari A, Roozbeh J, Mokhtari MJ, Hosseini AM. The effect of BKV reactivation on cytokines behavior in kidney transplanted patients. BMC Nephrol. 2022;23(1):20.
15. Foroudi MR, Yaghobi R, Afshari A, Roozbeh J, Miresmaeili SM, Javid A. The effect of the BK polyomavirus large T antigen on the function and maturity of the CD4+ T cell subsets in kidney transplant recipients. Transplant Immunol. 2023;80(14):101884.
16. Cimbaluk D, Pitelka L, Kluskens L, Gattuso P. Update on human polyomavirus BK nephropathy. Diagnostic cytopathology. 2009;37(10):773-9.
17. Van Aalderen M, Heutinck K, Huisman C, Ten Berge I. BK virus infection in transplant recipients: clinical manifestations, treatment options and the immune response. Neth J Med. 2012;70(4):172-83.
18. Gupta N, Lawrence RM, Nguyen C, Modica RF. BK virus in systemic lupus erythematosus. Pediatric Rheumatol. 2015;13(1):1-11.
19. Kariminik A, Yaghobi R, Dabiri S. Association of BK Virus Infection with CXCL11 Gene Expression and Protein Levels in Kidney Transplant Patients. Experimental and clinical transplantation: official journal of the Middle East Society for Organ Transplant. 2016;16(1):50-4.
20. Malekshahi SS, Soleimanjahi H, Dorostkar F, Salimi V, Farahmand M. Survey of BK Virus in Renal Transplant Recipients in Iran: A Systematic Review and Meta-Analysis. Intervirology. 2021;64(1):27-35.
21. Zareei N, Miri HR, Karimi MH, Afshari A, Geramizadeh B, Roozbeh J, et al. Increasing of the interferon-γ gene expression during polyomavirus BK infection in kidney transplant patients. Microbial pathogenesis. 2019; 129:187-94.
22. Blyth E, Clancy L, Simms R, Gaundar S, O'Connell P, Micklethwaite K, et al. BK virus-specific T cells for use in cellular therapy show specificity to multiple antigens and polyfunctional cytokine responses. Transplantation. 2011;92(10):1077-84.
23. Comoli P, Basso S, Azzi A, Moretta A, De Santis R, Del Galdo F, et al. Dendritic cells pulsed with polyomavirus BK antigen induce ex vivo polyoma BK virus–specific cytotoxic T-cell lines in seropositive healthy individuals and renal transplant recipients. J Am Society Nephrol. 2003;14(12):3197-204.
24. Weist B, Schmueck M, Fuehrer H, Sattler A, Reinke P, Babel N. The role of CD4+ T cells in BKV-specific T cell immunity. Med Microbiol Immunol. 2014; 203:395-408.
25. Okada R, Kondo T, Matsuki F, Takata H, Takiguchi M. Phenotypic classification of human CD4+ T cell subsets and their differentiation. Int Immunol. 2008;20(9):1189-99.
26. Zhou W, Sharma M, Martinez J, Srivastava T, Diamond DJ, Knowles W, et al. Functional characterization of BK virus-specific CD4+ T cells with cytotoxic potential in seropositive adults. Viral immunology. 2007;20(3):379-88.
27. Pachnio A, Ciaurriz M, Begum J, Lal N, Zuo J, Beggs A, et al. Cytomegalovirus infection leads to development of high frequencies of cytotoxic virus-specific CD4+ T cells targeted to vascular endothelium. PLoS pathogens. 2016;12(9): e1005832.
28. Liechti T, Roederer M. OMIP‐060: 30‐parameter flow cytometry panel to assess T cell effector functions and regulatory T cells. Cytometry Part A. 2019;95(11):1129-34.
29. Trapani JA, Smyth MJ. Functional significance of the perforin/granzyme cell death pathway. Nat Rev Immunol. 2002;2(10):735-47.
30. Parajuli S, Jorgenson M, Meyers RO, Djamali A, Galipeau J. Role of Virus-Specific T cell therapy for Cytomegalovirus and BK infections in kidney transplant recipients. Kidney360. 2021;2(5):905.
31. Li P, Cheng D, Wen J, Ni X, Li X, Xie K, et al. The immunophenotyping of different stages of BK virus allograft nephropathy. Renal failure. 2019;41(1):855-61.
32. Snyder LD, Chan C, Kwon D, Yi JS, Martissa JA, Copeland CAF, et al. Polyfunctional T-cell signatures to predict protection from cytomegalovirus after lung transplantation. Am J Res Critical Care Med. 2016;193(1):78-85.
33. Stervbo U, Nienen M, Weist BJ, Kuchenbecker L, Hecht J, Wehler P, et al. BKV clearance time correlates with exhaustion state and T-cell receptor repertoire shape of BKV-specific T-cells in renal transplant patients. Front Immunol. 2019;10:767.
34. van Aalderen MC, Remmerswaal EB, Heutinck KM, Ten Brinke A, Feltkamp MC, van der Weerd NC, et al. Clinically relevant reactivation of polyomavirus BK (BKPyV) in HLA-A02-positive renal transplant recipients is associated with impaired effector-memory differentiation of BKPyV-specific CD8+ T cells. PLoS Pathogens. 2016;12(10): e1005903.
35. Dekeyser M, François H, Beaudreuil S, Durrbach A. Polyomavirus-specific cellular immunity: from BK-virus-specific cellular immunity to BK-virus-associated nephropathy? Front Immunol. 2015; 6:307.
36. Binggeli S, Egli A, Schaub S, Binet I, Mayr M, Steiger J, et al. Polyomavirus BK‐specific cellular immune response to VP1 and large T‐antigen in kidney transplant recipients. Am J Transplant. 2007;7(5):1131-9.
37. Fan Y, Bai H, Qian Y, Sun Z, Shi B. CD4+ T cell immune response to VP1 and VP3 in BK virus infected recipients of renal transplantation. Surgical Infect. 2019;20(3):236-43.
38. Bruminhent J, Srisala S, Klinmalai C, Pinsai S, Watcharananan SP, Kantachuvesiri S, et al. BK Polyomavirus-specific T cell immune responses in kidney transplant recipients diagnosed with BK Polyomavirus-associated nephropathy. BMC Infect Dis. 2019;19:1-8.
39. Ahrends T, Busselaar J, Severson TM, Bąbała N, de Vries E, Bovens A, et al. CD4+ T cell help creates memory CD8+ T cells with innate and help-independent recall capacities. Nat Commun. 2019;10(1):5531.
40. Weist BJ, Wehler P, El Ahmad L, Schmueck-Henneresse M, Millward JM, Nienen M, et al. A revised strategy for monitoring BKV-specific cellular immunity in kidney transplant patients. Kidney International. 2015;88(6):1293-303.
41. Letsch A, Knoedler M, Na IK, Kern F, Asemissen AM, Keilholz U, et al. CMV‐specific central memory T cells reside in bone marrow. Europ J Immunol. 2007 Nov;37(11):3063-8.
42. van Doesum WB, Abdulahad WH, van Dijk MC, Dolff S, van son WJ, Stegeman CA, et al. Characterization of urinary CD 4+ and CD 8+ T cells in kidney transplantation patients with polyomavirus BK infection and allograft rejection. Transplant Infectious Disease. 2014 Oct;16(5):733-43.
43. Ambalathingal GR, Francis RS, Corvino D, Srihari S, Aftab BT, Smith C, et al. Proteome‐wide analysis of T‐cell response to BK polyomavirus in healthy virus carriers and kidney transplant recipients reveals a unique transcriptional and functional profile. Clin Trans Immunol. 2020;9(1):e01102.
44. Alonso Arias R, Moro-García MA, Echeverria A, Solano-Jaurrieta JJ, Suárez-García FM, López-Larrea C. Intensity of the humoral response to cytomegalovirus is associated with the phenotypic and functional status of the immune system. J Virol. 2013;87(8):4486-95.
45. Zhang W, Morris AB, Peek EV, Karadkhele G, Kissick HT, Larsen CP. CMV status drives distinct trajectories of CD4+ T cell differentiation. Front Immunol. 2021 Apr 15; 12:620386.
46. Palma JP, Yauch RL, Lang S, Kim BS. Potential role of CD4+ T cell-mediated apoptosis of activated astrocytes in Theiler’s virus-induced demyelination. J Immunology. 1999;162(11):6543-51.
47. Comoli P, Hirsch HH, Ginevri F. Cellular immune responses to BK virus. Curr Opin Organ Transplann. 2008;13(6):569-74.
48. Espada E, Cheng MP, Kim HT, Woolley AE, Avigan JI, Forcade E, et al. BK virus–specific T-cell immune reconstitution after allogeneic hematopoietic cell transplantation. Blood Advances. 2020;4(9):1881-93.
49. Schaenman JM, Korin Y, Sidwell T, Kandarian F, Harre N, Gjertson D, et al. Increased frequency of BK virus-specific polyfunctional CD8+ T cells predict successful control of BK viremia after kidney transplantation. Transplantation. 2017;101(6):1479.
| Files | ||
| Issue | Vol 23 No 3 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijaai.v23i3.15637 | |
| Keywords | ||
| CD4 T cell Kidney transplant Polyomavirus BK VP1 protein | ||
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How to Cite
1.
Noshadi N, Yaghoubi R, afshari A, Forouzanfar M, Soleimanian S. Polyomavirus BK-Specific CD4+ T Cells Response to VP1 Stimulation in Kidney Transplant Recipients. Iran J Allergy Asthma Immunol. 2024;23(3):272-287.
