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Published in: Medical Microbiology and Immunology 1/2014

01-02-2014 | Original Investigation

Differential influenza H1N1-specific humoral and cellular response kinetics in kidney transplant patients

Authors: Vinay Rambal, Karin Müller, Chantip Dang-Heine, Arne Sattler, Mikalai Dziubianau, Benjamin Weist, Si-Hong Luu, Alexandra Stoyanova, Peter Nickel, Andreas Thiel, Avidan Neumann, Brunhilde Schweiger, Petra Reinke, Nina Babel

Published in: Medical Microbiology and Immunology | Issue 1/2014

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Abstract

Renal transplant recipients (RTR) are considered at high risk for influenza-associated complications due to immunosuppression. The efficacy of standard influenza vaccination in RTRs is unclear. Hence, we evaluated activation of the adaptive immunity by the pandemic influenza A(H1N1) 2009 (A(H1N1)pdm09) vaccine in RTRs as compared to healthy controls. To determine cross-reactivity and/or bystander activation, seasonal trivalent influenza vaccine and tetanus/diphteria toxoid (TT/DT) vaccine-specific T cells along with allospecific T cells were quantified before and after A(H1N1)pdm09 vaccination. Vaccination-induced alloimmunity was additionally determined by quantifying serum creatinine and proinflammatory protein IP-10. Contrary to healthy controls, RTRs required a booster vaccination to achieve seroconversion (13.3 % day 21; 90 % day 90). In contrast to humoral immunity, sufficient A(H1N1)pdm09-specific T-cell responses were mounted in RTRs already after the first immunization with a magnitude comparable with healthy controls. Interestingly, vaccination simultaneously boosted T cells reacting to seasonal flu but not to TT/DT, suggesting cross-activation. No alloimmune effects were recorded. In conclusion, protective antibody responses required booster vaccination. However, sufficient cellular immunity is established already after the first vaccination, demonstrating differential kinetics of humoral and cellular immunity.
Literature
1.
go back to reference Ljungman P, Andersson J, Aschan J, Barkholt L, Ehrnst A, Johansson M, Weiland O (1993) Influenza A in immunocompromised patients. Clin Infect Dis 17(2):244–247PubMedCrossRef Ljungman P, Andersson J, Aschan J, Barkholt L, Ehrnst A, Johansson M, Weiland O (1993) Influenza A in immunocompromised patients. Clin Infect Dis 17(2):244–247PubMedCrossRef
2.
go back to reference Vilchez RA, McCurry K, Dauber J, Lacono A, Griffith B, Fung J, Kusne S (2002) Influenza virus infection in adult solid organ transplant recipients. Am J Transplant 2(3):287–291PubMedCrossRef Vilchez RA, McCurry K, Dauber J, Lacono A, Griffith B, Fung J, Kusne S (2002) Influenza virus infection in adult solid organ transplant recipients. Am J Transplant 2(3):287–291PubMedCrossRef
3.
go back to reference Kumar D, Michaels MG, Morris MI, Green M, Avery RK, Liu C, Danziger-Isakov L, Stosor V, Estabrook M, Gantt S, Marr KA, Martin S, Silveira FP, Razonable RR, Allen UD, Levi ME, Lyon GM, Bell LE, Huprikar S, Patel G, Gregg KS, Pursell K, Helmersen D, Julian KG, Shiley K, Bono B, Dharnidharka VR, Alavi G, Kalpoe JS, Shoham S, Reid GE, Humar A (2010) Outcomes from pandemic influenza A H1N1 infection in recipients of solid-organ transplants: a multicentre cohort study. Lancet Infect Dis 10(8):521–526PubMedCentralPubMedCrossRef Kumar D, Michaels MG, Morris MI, Green M, Avery RK, Liu C, Danziger-Isakov L, Stosor V, Estabrook M, Gantt S, Marr KA, Martin S, Silveira FP, Razonable RR, Allen UD, Levi ME, Lyon GM, Bell LE, Huprikar S, Patel G, Gregg KS, Pursell K, Helmersen D, Julian KG, Shiley K, Bono B, Dharnidharka VR, Alavi G, Kalpoe JS, Shoham S, Reid GE, Humar A (2010) Outcomes from pandemic influenza A H1N1 infection in recipients of solid-organ transplants: a multicentre cohort study. Lancet Infect Dis 10(8):521–526PubMedCentralPubMedCrossRef
4.
go back to reference Fiore AE, Shay DK, Broder K, Iskander JK, Uyeki TM, Mootrey G, Bresee JS, Cox NJ (2009) Prevention and control of seasonal influenza with vaccines: recommendations of the advisory committee on immunization practices (ACIP). MMWR Recomm Rep 58(RR-8):1–52PubMed Fiore AE, Shay DK, Broder K, Iskander JK, Uyeki TM, Mootrey G, Bresee JS, Cox NJ (2009) Prevention and control of seasonal influenza with vaccines: recommendations of the advisory committee on immunization practices (ACIP). MMWR Recomm Rep 58(RR-8):1–52PubMed
5.
go back to reference Smith KG, Isbel NM, Catton MG, Leydon JA, Becker GJ, Walker RG (1998) Suppression of the humoral immune response by mycophenolate mofetil. Nephrol Dial Transplant 13(1):160–164PubMedCrossRef Smith KG, Isbel NM, Catton MG, Leydon JA, Becker GJ, Walker RG (1998) Suppression of the humoral immune response by mycophenolate mofetil. Nephrol Dial Transplant 13(1):160–164PubMedCrossRef
6.
go back to reference Sanchez-Fructuoso AI, Prats D, Naranjo P, Fernandez-Perez C, Gonzalez MJ, Mariano A, Gonzalez J, Figueredo MA, Martin JM, Paniagua V, Fereres J, Gomez de la Concha E, Barrientos A (2000) Influenza virus immunization effectivity in kidney transplant patients subjected to two different triple-drug therapy immunosuppression protocols: mycophenolate versus azathioprine. Transplantation 69(3):436–439PubMedCrossRef Sanchez-Fructuoso AI, Prats D, Naranjo P, Fernandez-Perez C, Gonzalez MJ, Mariano A, Gonzalez J, Figueredo MA, Martin JM, Paniagua V, Fereres J, Gomez de la Concha E, Barrientos A (2000) Influenza virus immunization effectivity in kidney transplant patients subjected to two different triple-drug therapy immunosuppression protocols: mycophenolate versus azathioprine. Transplantation 69(3):436–439PubMedCrossRef
7.
go back to reference Wyzgal J, Brydak LB, Zygier D, Paczek L, Rowinski W, Grochowiecki T (2002) Study on efficacy of influenza vaccination in renal allograft recipients. Transplant Proc 34(2):572–575PubMedCrossRef Wyzgal J, Brydak LB, Zygier D, Paczek L, Rowinski W, Grochowiecki T (2002) Study on efficacy of influenza vaccination in renal allograft recipients. Transplant Proc 34(2):572–575PubMedCrossRef
8.
go back to reference Birdwell KA, Ikizler MR, Sannella EC, Wang L, Byrne DW, Ikizler TA, Wright PF (2009) Decreased antibody response to influenza vaccination in kidney transplant recipients: a prospective cohort study. Am J Kidney Dis 54(1):112–121PubMedCentralPubMedCrossRef Birdwell KA, Ikizler MR, Sannella EC, Wang L, Byrne DW, Ikizler TA, Wright PF (2009) Decreased antibody response to influenza vaccination in kidney transplant recipients: a prospective cohort study. Am J Kidney Dis 54(1):112–121PubMedCentralPubMedCrossRef
9.
go back to reference Carroll RN, Marsh SD, O’Donoghue EP, Breeze DC, Shackman R (1974) Response to influenza vaccine by renal transplant patients. Br Med J 2(5921):701–703PubMedCentralPubMedCrossRef Carroll RN, Marsh SD, O’Donoghue EP, Breeze DC, Shackman R (1974) Response to influenza vaccine by renal transplant patients. Br Med J 2(5921):701–703PubMedCentralPubMedCrossRef
10.
go back to reference Scharpe J, Evenepoel P, Maes B, Bammens B, Claes K, Osterhaus AD, Vanrenterghem Y, Peetermans WE (2008) Influenza vaccination is efficacious and safe in renal transplant recipients. Am J Transplant 8(2):332–337PubMedCrossRef Scharpe J, Evenepoel P, Maes B, Bammens B, Claes K, Osterhaus AD, Vanrenterghem Y, Peetermans WE (2008) Influenza vaccination is efficacious and safe in renal transplant recipients. Am J Transplant 8(2):332–337PubMedCrossRef
11.
go back to reference Candon S, Thervet E, Lebon P, Suberbielle C, Zuber J, Lima C, Charron D, Legendre C, Chatenoud L (2009) Humoral and cellular immune responses after influenza vaccination in kidney transplant recipients. Am J Transplant 9(10):2346–2354PubMedCrossRef Candon S, Thervet E, Lebon P, Suberbielle C, Zuber J, Lima C, Charron D, Legendre C, Chatenoud L (2009) Humoral and cellular immune responses after influenza vaccination in kidney transplant recipients. Am J Transplant 9(10):2346–2354PubMedCrossRef
12.
go back to reference Ridao-Cano N, Sanchez-Fructuoso AI, Rodriguez-Moreno A, Barrientos A (2009) H1N1 2009 influenza in kidney transplant patients. Transplantation 90(2):224–225CrossRef Ridao-Cano N, Sanchez-Fructuoso AI, Rodriguez-Moreno A, Barrientos A (2009) H1N1 2009 influenza in kidney transplant patients. Transplantation 90(2):224–225CrossRef
13.
go back to reference Camargo LF, de Sandes-Freitas TV, Silva CD, Bittante CD, Ono G, Correa L, Silva M Jr, Bellei NC, Goto JM, Medeiros EA, Gomes PS, Medina-Pestana JO (2012) Morbimortality of pandemic influenza A H1N1 infection in kidney transplant recipients requiring hospitalization: a comparative analysis with nonimmunocompromised patients. Transplantation 93(1):69–72PubMedCrossRef Camargo LF, de Sandes-Freitas TV, Silva CD, Bittante CD, Ono G, Correa L, Silva M Jr, Bellei NC, Goto JM, Medeiros EA, Gomes PS, Medina-Pestana JO (2012) Morbimortality of pandemic influenza A H1N1 infection in kidney transplant recipients requiring hospitalization: a comparative analysis with nonimmunocompromised patients. Transplantation 93(1):69–72PubMedCrossRef
14.
go back to reference Keane WR, Helderman JH, Luby J, Gailiunas P, Hull AR, Kokko JP (1978) Epidemic renal transplant rejection associated with influenza A Victoria. Proc Clin Dial Transplant Forum 8:232–236PubMed Keane WR, Helderman JH, Luby J, Gailiunas P, Hull AR, Kokko JP (1978) Epidemic renal transplant rejection associated with influenza A Victoria. Proc Clin Dial Transplant Forum 8:232–236PubMed
15.
go back to reference Kunisaki KM, Janoff EN (2009) Influenza in immunosuppressed populations: a review of infection frequency, morbidity, mortality, and vaccine responses. Lancet Infect Dis 9(8):493–504PubMedCentralPubMedCrossRef Kunisaki KM, Janoff EN (2009) Influenza in immunosuppressed populations: a review of infection frequency, morbidity, mortality, and vaccine responses. Lancet Infect Dis 9(8):493–504PubMedCentralPubMedCrossRef
16.
go back to reference Danziger-Isakov L, Cherkassky L, Siegel H, McManamon M, Kramer K, Budev M, Sawinski D, Augustine JJ, Hricik DE, Fairchild R, Heeger PS, Poggio ED (2010) Effects of influenza immunization on humoral and cellular alloreactivity in humans. Transplantation 89(7):838–844PubMedCentralPubMedCrossRef Danziger-Isakov L, Cherkassky L, Siegel H, McManamon M, Kramer K, Budev M, Sawinski D, Augustine JJ, Hricik DE, Fairchild R, Heeger PS, Poggio ED (2010) Effects of influenza immunization on humoral and cellular alloreactivity in humans. Transplantation 89(7):838–844PubMedCentralPubMedCrossRef
17.
go back to reference Poggio ED, Clemente M, Riley J, Roddy M, Greenspan NS, Dejelo C, Najafian N, Sayegh MH, Hricik DE, Heeger PS (2004) Alloreactivity in renal transplant recipients with and without chronic allograft nephropathy. J Am Soc Nephrol 15(7):1952–1960PubMedCrossRef Poggio ED, Clemente M, Riley J, Roddy M, Greenspan NS, Dejelo C, Najafian N, Sayegh MH, Hricik DE, Heeger PS (2004) Alloreactivity in renal transplant recipients with and without chronic allograft nephropathy. J Am Soc Nephrol 15(7):1952–1960PubMedCrossRef
18.
go back to reference Heeger PS (2003) T-cell allorecognition and transplant rejection: a summary and update. Am J Transplant 3(5):525–533PubMedCrossRef Heeger PS (2003) T-cell allorecognition and transplant rejection: a summary and update. Am J Transplant 3(5):525–533PubMedCrossRef
19.
go back to reference Matl I, Hribova P, Honsova E, Brabcova I, Viklicky O (2010) Potential predictive markers in protocol biopsies for premature renal graft loss. Kidney Blood Press Res 33(1):7–14PubMedCrossRef Matl I, Hribova P, Honsova E, Brabcova I, Viklicky O (2010) Potential predictive markers in protocol biopsies for premature renal graft loss. Kidney Blood Press Res 33(1):7–14PubMedCrossRef
20.
go back to reference Matz M, Beyer J, Wunsch D, Mashreghi MF, Seiler M, Pratschke J, Babel N, Volk HD, Reinke P, Kotsch K (2006) Early post-transplant urinary IP-10 expression after kidney transplantation is predictive of short- and long-term graft function. Kidney Int 69(9):1683–1690PubMedCrossRef Matz M, Beyer J, Wunsch D, Mashreghi MF, Seiler M, Pratschke J, Babel N, Volk HD, Reinke P, Kotsch K (2006) Early post-transplant urinary IP-10 expression after kidney transplantation is predictive of short- and long-term graft function. Kidney Int 69(9):1683–1690PubMedCrossRef
21.
go back to reference Hricik DE, Rodriguez V, Riley J, Bryan K, Tary-Lehmann M, Greenspan N, Dejelo C, Schulak JA, Heeger PS (2003) Enzyme linked immunosorbent spot (ELISPOT) assay for interferon-gamma independently predicts renal function in kidney transplant recipients. Am J Transplant 3(7):878–884PubMedCrossRef Hricik DE, Rodriguez V, Riley J, Bryan K, Tary-Lehmann M, Greenspan N, Dejelo C, Schulak JA, Heeger PS (2003) Enzyme linked immunosorbent spot (ELISPOT) assay for interferon-gamma independently predicts renal function in kidney transplant recipients. Am J Transplant 3(7):878–884PubMedCrossRef
22.
go back to reference Meyer S, Adam M, Schweiger B, Ilchmann C, Eulenburg C, Sattinger E, Runte H, Schluter M, Deuse T, Reichenspurner H, Costard-Jackle A (2011) Antibody response after a single dose of an AS03-adjuvanted split-virion Influenza A(H1N1) vaccine in heart transplant recipients. Transplantation 91(9):1031–1035PubMedCrossRef Meyer S, Adam M, Schweiger B, Ilchmann C, Eulenburg C, Sattinger E, Runte H, Schluter M, Deuse T, Reichenspurner H, Costard-Jackle A (2011) Antibody response after a single dose of an AS03-adjuvanted split-virion Influenza A(H1N1) vaccine in heart transplant recipients. Transplantation 91(9):1031–1035PubMedCrossRef
23.
go back to reference Andree H, Nickel P, Nasiadko C, Hammer MH, Schonemann C, Pruss A, Volk HD, Reinke P (2006) Identification of dialysis patients with panel-reactive memory T cells before kidney transplantation using an allogeneic cell bank. J Am Soc Nephrol 17(2):573–580PubMedCrossRef Andree H, Nickel P, Nasiadko C, Hammer MH, Schonemann C, Pruss A, Volk HD, Reinke P (2006) Identification of dialysis patients with panel-reactive memory T cells before kidney transplantation using an allogeneic cell bank. J Am Soc Nephrol 17(2):573–580PubMedCrossRef
24.
go back to reference Wrammert J, Koutsonanos D, Li GM, Edupuganti S, Sui J, Morrissey M, McCausland M, Skountzou I, Hornig M, Lipkin WI, Mehta A, Razavi B, Del Rio C, Zheng NY, Lee JH, Huang M, Ali Z, Kaur K, Andrews S, Amara RR, Wang Y, Das SR, O’Donnell CD, Yewdell JW, Subbarao K, Marasco WA, Mulligan MJ, Compans R, Ahmed R, Wilson PC (2011) Broadly cross-reactive antibodies dominate the human B cell response against 2009 pandemic H1N1 influenza virus infection. J Exp Med 208(1):181–193PubMedCentralPubMedCrossRef Wrammert J, Koutsonanos D, Li GM, Edupuganti S, Sui J, Morrissey M, McCausland M, Skountzou I, Hornig M, Lipkin WI, Mehta A, Razavi B, Del Rio C, Zheng NY, Lee JH, Huang M, Ali Z, Kaur K, Andrews S, Amara RR, Wang Y, Das SR, O’Donnell CD, Yewdell JW, Subbarao K, Marasco WA, Mulligan MJ, Compans R, Ahmed R, Wilson PC (2011) Broadly cross-reactive antibodies dominate the human B cell response against 2009 pandemic H1N1 influenza virus infection. J Exp Med 208(1):181–193PubMedCentralPubMedCrossRef
25.
go back to reference Fairhead T, Hendren E, Tinckam K, Rose C, Sherlock CH, Shi L, Crowcroft NS, Gubbay JB, Landsberg D, Knoll G, Gill J, Kumar D (2012) Poor seroprotection but allosensitization after adjuvanted pandemic influenza H1N1 vaccine in kidney transplant recipients. Transpl Infect Dis 14(6):575–583PubMedCrossRef Fairhead T, Hendren E, Tinckam K, Rose C, Sherlock CH, Shi L, Crowcroft NS, Gubbay JB, Landsberg D, Knoll G, Gill J, Kumar D (2012) Poor seroprotection but allosensitization after adjuvanted pandemic influenza H1N1 vaccine in kidney transplant recipients. Transpl Infect Dis 14(6):575–583PubMedCrossRef
26.
go back to reference Ott U, Sauerbrei A, Lange J, Schafler A, Walther M, Wolf G, Wutzler P, Zell R, Krumbholz A (2012) Serological response to influenza A H1N1 vaccine (Pandemrix®) and seasonal influenza vaccine 2009/2010 in renal transplant recipients and in hemodialysis patients. Med Microbiol Immunol 201(3):297–302PubMedCrossRef Ott U, Sauerbrei A, Lange J, Schafler A, Walther M, Wolf G, Wutzler P, Zell R, Krumbholz A (2012) Serological response to influenza A H1N1 vaccine (Pandemrix®) and seasonal influenza vaccine 2009/2010 in renal transplant recipients and in hemodialysis patients. Med Microbiol Immunol 201(3):297–302PubMedCrossRef
27.
go back to reference Quintana LF, Serra N, De Molina-Llaurado P, Blasco M, Martinez M, Campos B, Bayas JM, Pumarola T, Campistol JM (2012) Influence of renal replacement therapy on immune response after one and two doses of the A(H1N1) pdm09 vaccine. Influenza Other Respi Viruses Quintana LF, Serra N, De Molina-Llaurado P, Blasco M, Martinez M, Campos B, Bayas JM, Pumarola T, Campistol JM (2012) Influence of renal replacement therapy on immune response after one and two doses of the A(H1N1) pdm09 vaccine. Influenza Other Respi Viruses
28.
go back to reference Manuel O, Pascual M, Hoschler K, Giulieri S, Alves D, Ellefsen K, Bart PA, Venetz JP, Calandra T, Cavassini M (2011) Humoral response to the influenza A H1N1/09 monovalent AS03-adjuvanted vaccine in immunocompromised patients. Clin Infect Dis 52(2):248–256PubMedCrossRef Manuel O, Pascual M, Hoschler K, Giulieri S, Alves D, Ellefsen K, Bart PA, Venetz JP, Calandra T, Cavassini M (2011) Humoral response to the influenza A H1N1/09 monovalent AS03-adjuvanted vaccine in immunocompromised patients. Clin Infect Dis 52(2):248–256PubMedCrossRef
29.
go back to reference Brakemeier S, Schweiger B, Lachmann N, Glander P, Schonemann C, Diekmann F, Neumayer HH, Budde K (2011) Immune response to an adjuvanted influenza A H1N1 vaccine (Pandemrix®) in renal transplant recipients. Nephrol Dial Transplant 27(1):423–428PubMedCrossRef Brakemeier S, Schweiger B, Lachmann N, Glander P, Schonemann C, Diekmann F, Neumayer HH, Budde K (2011) Immune response to an adjuvanted influenza A H1N1 vaccine (Pandemrix®) in renal transplant recipients. Nephrol Dial Transplant 27(1):423–428PubMedCrossRef
30.
go back to reference Esposito S, Meregalli E, Daleno C, Ghio L, Tagliabue C, Valzano A, Serra D, Galeone C, Edefonti A, Principi N (2011) An open-label, randomized clinical trial assessing immunogenicity, safety and tolerability of pandemic influenza A/H1N1 MF59-adjuvanted vaccine administered sequentially or simultaneously with seasonal virosomal-adjuvanted influenza vaccine to paediatric kidney transplant recipients. Nephrol Dial Transplant 26(6):2018–2024PubMedCrossRef Esposito S, Meregalli E, Daleno C, Ghio L, Tagliabue C, Valzano A, Serra D, Galeone C, Edefonti A, Principi N (2011) An open-label, randomized clinical trial assessing immunogenicity, safety and tolerability of pandemic influenza A/H1N1 MF59-adjuvanted vaccine administered sequentially or simultaneously with seasonal virosomal-adjuvanted influenza vaccine to paediatric kidney transplant recipients. Nephrol Dial Transplant 26(6):2018–2024PubMedCrossRef
31.
go back to reference de Lavallade H, Garland P, Sekine T, Hoschler K, Marin D, Stringaris K, Loucaides E, Howe K, Szydlo R, Kanfer E, Macdonald D, Kelleher P, Cooper N, Khoder A, Gabriel IH, Milojkovic D, Pavlu J, Goldman JM, Apperley JF, Rezvani K (2011) Repeated vaccination is required to optimize seroprotection against H1N1 in the immunocompromised host. Haematologica 96(2):307–314PubMedCrossRef de Lavallade H, Garland P, Sekine T, Hoschler K, Marin D, Stringaris K, Loucaides E, Howe K, Szydlo R, Kanfer E, Macdonald D, Kelleher P, Cooper N, Khoder A, Gabriel IH, Milojkovic D, Pavlu J, Goldman JM, Apperley JF, Rezvani K (2011) Repeated vaccination is required to optimize seroprotection against H1N1 in the immunocompromised host. Haematologica 96(2):307–314PubMedCrossRef
32.
go back to reference Muller K, Schachtner T, Sattler A, Meier S, Friedrich P, Trydzenskaya H, Hinrichs C, Trappe R, Thiel A, Reinke P, Babel N (2011) BK-VP3 as a new target of cellular immunity in BK virus infection. Transplantation 91(1):100–107CrossRef Muller K, Schachtner T, Sattler A, Meier S, Friedrich P, Trydzenskaya H, Hinrichs C, Trappe R, Thiel A, Reinke P, Babel N (2011) BK-VP3 as a new target of cellular immunity in BK virus infection. Transplantation 91(1):100–107CrossRef
33.
go back to reference Bunde T, Kirchner A, Hoffmeister B, Habedank D, Hetzer R, Cherepnev G, Proesch S, Reinke P, Volk HD, Lehmkuhl H, Kern F (2005) Protection from cytomegalovirus after transplantation is correlated with immediate early 1-specific CD8 T cells. J Exp Med 201(7):1031–1036PubMedCentralPubMedCrossRef Bunde T, Kirchner A, Hoffmeister B, Habedank D, Hetzer R, Cherepnev G, Proesch S, Reinke P, Volk HD, Lehmkuhl H, Kern F (2005) Protection from cytomegalovirus after transplantation is correlated with immediate early 1-specific CD8 T cells. J Exp Med 201(7):1031–1036PubMedCentralPubMedCrossRef
34.
go back to reference Harari A, Petitpierre S, Vallelian F, Pantaleo G (2004) Skewed representation of functionally distinct populations of virus-specific CD4 T cells in HIV-1-infected subjects with progressive disease: changes after antiretroviral therapy. Blood 103(3):966–972PubMedCrossRef Harari A, Petitpierre S, Vallelian F, Pantaleo G (2004) Skewed representation of functionally distinct populations of virus-specific CD4 T cells in HIV-1-infected subjects with progressive disease: changes after antiretroviral therapy. Blood 103(3):966–972PubMedCrossRef
35.
go back to reference Kumar D, Campbell P, Humar A (2011) Donor-specific alloantibody upregulation after influenza vaccination in transplant recipients. Am J Transplant 11(11):2538PubMedCrossRef Kumar D, Campbell P, Humar A (2011) Donor-specific alloantibody upregulation after influenza vaccination in transplant recipients. Am J Transplant 11(11):2538PubMedCrossRef
36.
go back to reference Lee VJ, Tay JK, Chen MI, Phoon MC, Xie ML, Wu Y, Lee CX, Yap J, Sakharkar KR, Sakharkar MK, Lin RT, Cui L, Kelly PM, Leo YS, Tan YJ, Chow VT (2010) Inactivated trivalent seasonal influenza vaccine induces limited cross-reactive neutralizing antibody responses against 2009 pandemic and 1934 PR8 H1N1 strains. Vaccine 28(42):6852–6857PubMedCrossRef Lee VJ, Tay JK, Chen MI, Phoon MC, Xie ML, Wu Y, Lee CX, Yap J, Sakharkar KR, Sakharkar MK, Lin RT, Cui L, Kelly PM, Leo YS, Tan YJ, Chow VT (2010) Inactivated trivalent seasonal influenza vaccine induces limited cross-reactive neutralizing antibody responses against 2009 pandemic and 1934 PR8 H1N1 strains. Vaccine 28(42):6852–6857PubMedCrossRef
37.
go back to reference Xing Z, Cardona CJ (2009) Preexisting immunity to pandemic (H1N1). Emerg Infect Dis 15(11):1847–1849PubMedCrossRef Xing Z, Cardona CJ (2009) Preexisting immunity to pandemic (H1N1). Emerg Infect Dis 15(11):1847–1849PubMedCrossRef
38.
go back to reference Duvvuri VR, Moghadas SM, Guo H, Duvvuri B, Heffernan JM, Fisman DN, Wu GE, Wu J (2010) Highly conserved cross-reactive CD4 + T-cell HA-epitopes of seasonal and the 2009 pandemic influenza viruses. Influenza Other Respi Viruses 4(5):249–258CrossRef Duvvuri VR, Moghadas SM, Guo H, Duvvuri B, Heffernan JM, Fisman DN, Wu GE, Wu J (2010) Highly conserved cross-reactive CD4 + T-cell HA-epitopes of seasonal and the 2009 pandemic influenza viruses. Influenza Other Respi Viruses 4(5):249–258CrossRef
39.
go back to reference Greenbaum JA, Kotturi MF, Kim Y, Oseroff C, Vaughan K, Salimi N, Vita R, Ponomarenko J, Scheuermann RH, Sette A, Peters B (2009) Pre-existing immunity against swine-origin H1N1 influenza viruses in the general human population. Proc Natl Acad Sci USA 106(48):20365–20370PubMedCrossRef Greenbaum JA, Kotturi MF, Kim Y, Oseroff C, Vaughan K, Salimi N, Vita R, Ponomarenko J, Scheuermann RH, Sette A, Peters B (2009) Pre-existing immunity against swine-origin H1N1 influenza viruses in the general human population. Proc Natl Acad Sci USA 106(48):20365–20370PubMedCrossRef
40.
go back to reference Allwinn R, Geiler J, Berger A, Cinatl J, Doerr HW (2010) Determination of serum antibodies against swine-origin influenza A virus H1N1/09 by immunofluorescence, haemagglutination inhibition, and by neutralization tests: how is the prevalence rate of protecting antibodies in humans? Med Microbiol Immunol 199(2):117–121PubMedCrossRef Allwinn R, Geiler J, Berger A, Cinatl J, Doerr HW (2010) Determination of serum antibodies against swine-origin influenza A virus H1N1/09 by immunofluorescence, haemagglutination inhibition, and by neutralization tests: how is the prevalence rate of protecting antibodies in humans? Med Microbiol Immunol 199(2):117–121PubMedCrossRef
41.
go back to reference Gueller S, Allwinn R, Mousset S, Martin H, Wieters I, Herrmann E, Serve H, Bickel M, Bug G (2011) Enhanced immune response after a second dose of an AS03-adjuvanted H1N1 influenza A vaccine in patients after hematopoietic stem cell transplantation. Biol Blood Marrow Transplant 17(10):1546–1550PubMedCrossRef Gueller S, Allwinn R, Mousset S, Martin H, Wieters I, Herrmann E, Serve H, Bickel M, Bug G (2011) Enhanced immune response after a second dose of an AS03-adjuvanted H1N1 influenza A vaccine in patients after hematopoietic stem cell transplantation. Biol Blood Marrow Transplant 17(10):1546–1550PubMedCrossRef
42.
go back to reference Kamperschroer C, Dibble JP, Meents DL, Schwartzberg PL, Swain SL (2006) SAP is required for Th cell function and for immunity to influenza. J Immunol 177(8):5317–5327PubMed Kamperschroer C, Dibble JP, Meents DL, Schwartzberg PL, Swain SL (2006) SAP is required for Th cell function and for immunity to influenza. J Immunol 177(8):5317–5327PubMed
43.
go back to reference Mozdzanowska K, Furchner M, Maiese K, Gerhard W (1997) CD4 + T cells are ineffective in clearing a pulmonary infection with influenza type A virus in the absence of B cells. Virology 239(1):217–225PubMedCrossRef Mozdzanowska K, Furchner M, Maiese K, Gerhard W (1997) CD4 + T cells are ineffective in clearing a pulmonary infection with influenza type A virus in the absence of B cells. Virology 239(1):217–225PubMedCrossRef
44.
go back to reference van de Berg PJ, van Leeuwen EM, ten Berge IJ, van Lier R (2008) Cytotoxic human CD4(+) T cells. Curr Opin Immunol 20(3):339–343PubMedCrossRef van de Berg PJ, van Leeuwen EM, ten Berge IJ, van Lier R (2008) Cytotoxic human CD4(+) T cells. Curr Opin Immunol 20(3):339–343PubMedCrossRef
46.
go back to reference Brown DM, Lee S, Garcia-Hernandez Mde L, Swain SL (2012) Multifunctional CD4 cells expressing gamma interferon and perforin mediate protection against lethal influenza virus infection. J Virol 86(12):6792–6803PubMedCentralPubMedCrossRef Brown DM, Lee S, Garcia-Hernandez Mde L, Swain SL (2012) Multifunctional CD4 cells expressing gamma interferon and perforin mediate protection against lethal influenza virus infection. J Virol 86(12):6792–6803PubMedCentralPubMedCrossRef
47.
go back to reference Wilkinson TM, Li CK, Chui CS, Huang AK, Perkins M, Liebner JC, Lambkin-Williams R, Gilbert A, Oxford J, Nicholas B, Staples KJ, Dong T, Douek DC, McMichael AJ, Xu XN (2012) Preexisting influenza-specific CD4 + T cells correlate with disease protection against influenza challenge in humans. Nat Med 18(2):274–280PubMedCrossRef Wilkinson TM, Li CK, Chui CS, Huang AK, Perkins M, Liebner JC, Lambkin-Williams R, Gilbert A, Oxford J, Nicholas B, Staples KJ, Dong T, Douek DC, McMichael AJ, Xu XN (2012) Preexisting influenza-specific CD4 + T cells correlate with disease protection against influenza challenge in humans. Nat Med 18(2):274–280PubMedCrossRef
48.
go back to reference Ballet C, Roussey-Kesler G, Aubin JT, Brouard S, Giral M, Miqueu P, Louis S, van der Werf S, Soulillou JP (2006) Humoral and cellular responses to influenza vaccination in human recipients naturally tolerant to a kidney allograft. Am J Transplant 6(11):2796–2801PubMedCrossRef Ballet C, Roussey-Kesler G, Aubin JT, Brouard S, Giral M, Miqueu P, Louis S, van der Werf S, Soulillou JP (2006) Humoral and cellular responses to influenza vaccination in human recipients naturally tolerant to a kidney allograft. Am J Transplant 6(11):2796–2801PubMedCrossRef
49.
go back to reference Ghendon Y (1990) The immune response to influenza vaccines. Acta Virol 34(3):295–304PubMed Ghendon Y (1990) The immune response to influenza vaccines. Acta Virol 34(3):295–304PubMed
50.
go back to reference Sant AJ, Chaves FA, Krafcik FR, Lazarski CA, Menges P, Richards K, Weaver JM (2007) Immunodominance in CD4 T-cell responses: implications for immune responses to influenza virus and for vaccine design. Expert Rev Vaccines 6(3):357–368PubMedCrossRef Sant AJ, Chaves FA, Krafcik FR, Lazarski CA, Menges P, Richards K, Weaver JM (2007) Immunodominance in CD4 T-cell responses: implications for immune responses to influenza virus and for vaccine design. Expert Rev Vaccines 6(3):357–368PubMedCrossRef
51.
go back to reference Teijaro JR, Verhoeven D, Page CA, Turner D, Farber DL (2010) Memory CD4 T cells direct protective responses to influenza virus in the lungs through helper-independent mechanisms. J Virol 84(18):9217–9226PubMedCentralPubMedCrossRef Teijaro JR, Verhoeven D, Page CA, Turner D, Farber DL (2010) Memory CD4 T cells direct protective responses to influenza virus in the lungs through helper-independent mechanisms. J Virol 84(18):9217–9226PubMedCentralPubMedCrossRef
52.
go back to reference Miesegaes G, Lute S, Brorson K (2010) Analysis of viral clearance unit operations for monoclonal antibodies. Biotechnol Bioeng 106(2):238–246PubMed Miesegaes G, Lute S, Brorson K (2010) Analysis of viral clearance unit operations for monoclonal antibodies. Biotechnol Bioeng 106(2):238–246PubMed
53.
go back to reference Neuzil KM, Jackson LA, Nelson J, Klimov A, Cox N, Bridges CB, Dunn J, DeStefano F, Shay D (2006) Immunogenicity and reactogenicity of 1 versus 2 doses of trivalent inactivated influenza vaccine in vaccine-naive 5-8-year-old children. J Infect Dis 194(8):1032–1039PubMedCrossRef Neuzil KM, Jackson LA, Nelson J, Klimov A, Cox N, Bridges CB, Dunn J, DeStefano F, Shay D (2006) Immunogenicity and reactogenicity of 1 versus 2 doses of trivalent inactivated influenza vaccine in vaccine-naive 5-8-year-old children. J Infect Dis 194(8):1032–1039PubMedCrossRef
54.
go back to reference Englund JA, Walter E, Black S, Blatter M, Nyberg J, Ruben FL, Decker MD (2010) Safety and immunogenicity of trivalent inactivated influenza vaccine in infants: a randomized double-blind placebo-controlled study. Pediatr Infect Dis J 29(2):105–110PubMedCrossRef Englund JA, Walter E, Black S, Blatter M, Nyberg J, Ruben FL, Decker MD (2010) Safety and immunogenicity of trivalent inactivated influenza vaccine in infants: a randomized double-blind placebo-controlled study. Pediatr Infect Dis J 29(2):105–110PubMedCrossRef
55.
go back to reference Bickel M, Lassmann C, Wieters I, Doerr HW, Herrmann E, Wicker S, Brodt HR, Stephan C, Allwinn R, Jung O (2013) Immune response after a single dose of the 2010/11 Trivalent, seasonal influenza vaccine in HIV-1-infected patients and healthy controls. HIV Clin Trials 14(4):175–184PubMedCrossRef Bickel M, Lassmann C, Wieters I, Doerr HW, Herrmann E, Wicker S, Brodt HR, Stephan C, Allwinn R, Jung O (2013) Immune response after a single dose of the 2010/11 Trivalent, seasonal influenza vaccine in HIV-1-infected patients and healthy controls. HIV Clin Trials 14(4):175–184PubMedCrossRef
56.
go back to reference Walker WT, Faust SN (2010) Monovalent inactivated split-virion AS03-adjuvanted pandemic influenza A (H1N1) vaccine. Expert Rev Vaccines 9(12):1385–1398PubMedCrossRef Walker WT, Faust SN (2010) Monovalent inactivated split-virion AS03-adjuvanted pandemic influenza A (H1N1) vaccine. Expert Rev Vaccines 9(12):1385–1398PubMedCrossRef
57.
go back to reference Skowronski DM, Janjua NZ, De Serres G, Hottes TS, Dickinson JA, Crowcroft N, Kwindt TL, Tang P, Charest H, Fonseca K, Gubbay JB, Bastien N, Li Y, Petric M (2011) Effectiveness of AS03 adjuvanted pandemic H1N1 vaccine: case-control evaluation based on sentinel surveillance system in Canada, autumn 2009. BMJ 342:c7297PubMedCentralPubMedCrossRef Skowronski DM, Janjua NZ, De Serres G, Hottes TS, Dickinson JA, Crowcroft N, Kwindt TL, Tang P, Charest H, Fonseca K, Gubbay JB, Bastien N, Li Y, Petric M (2011) Effectiveness of AS03 adjuvanted pandemic H1N1 vaccine: case-control evaluation based on sentinel surveillance system in Canada, autumn 2009. BMJ 342:c7297PubMedCentralPubMedCrossRef
Metadata
Title
Differential influenza H1N1-specific humoral and cellular response kinetics in kidney transplant patients
Authors
Vinay Rambal
Karin Müller
Chantip Dang-Heine
Arne Sattler
Mikalai Dziubianau
Benjamin Weist
Si-Hong Luu
Alexandra Stoyanova
Peter Nickel
Andreas Thiel
Avidan Neumann
Brunhilde Schweiger
Petra Reinke
Nina Babel
Publication date
01-02-2014
Publisher
Springer Berlin Heidelberg
Published in
Medical Microbiology and Immunology / Issue 1/2014
Print ISSN: 0300-8584
Electronic ISSN: 1432-1831
DOI
https://doi.org/10.1007/s00430-013-0312-3

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