CO-INHIBITORY MOLECULES IN NORMAL AND PATHOLOGICAL CONDITIONS. IMMONOLOGICAL CHECKPOINTS. Part 2. Co-inhibitory molecules part in oncology and infectious diseases. Checkpoints’ blockers monoclonal antibodies

Cover Page


Cite item

Full Text

Abstract

The differentiation and protective capacity of antigen‑specific T‑cells are regulated by both positive and negative signals. Molecules of the B7/CD28 family are very important for regulating T‑cell activation and peripheral tolerance. In particular, PD‑1, CTLA‑4 and other co‑inhibitory molecules play an active role in dampening of excessive immune activation which is critical for successful clearance of a pathogen without harm to the host. These co‑inhibitory molecules (immunological checkpoints) are essential for inducible Treg differentiation and function. On the other hand, overexpression of co‑inhibitory molecules can lead to T‑cell exhaustion, an adaptive property that occurs in T‑cells due to persistent systemic antigen exposure. Exhausted T‑cells are described as effector T‑cells with decreased cytokine expression and effector function. Here, we review a critical role of co‑inhibitory molecules which they play in immunopathogenesis of four immunological syndromes: allergy, autoimmune diseases, chronic infection, and cancer. Reversal of exhausted T‑cells by blocking co‑inhibitory pathways has become an important area due to its therapeutic applications in oncology and chronic viral infections.

About the authors

A. P. Toptygina

G.N. Gabrichevsky Research Institute for Epidemiology and Microbiology; Lomonosov Moscow State University

Author for correspondence.
Email: toptyginaanna@rambler.ru

PhD, MD (Medicine), Leading Research Associate, Laboratory of Cytokines; Professor Chair of Immunology, Faculty of Biology

125212 Moscow, Admirala Makarova ul., 10

Russian Federation

References

  1. Bonato V.L., Medeiros A.I., Lima V.M., Dias A.R., Faccioliti L.H., Silva C.L. Downmodulation of CD18 and CD86 on macrophages and VLA-4 on lymphocytes in experimental tuberculosis. Scand J Immunol. 2001, 54, 564–573.
  2. Murray R.A., Siddiqui M.R., Mendillo M., Krahenbuhl J., Kaplan G. Mycobacterium leprae inhibits dendritic cell activation and maturation. J Immunol. 2007, 178, 338–344.
  3. Chaudhry A., Das S.R., Hussain A., Mayor S., George A., Bal V., Jameel S., Rath S. The Nef protein of HIV-1 induces loss of cell surface costimulatory molecules CD80 and CD86 in APCs. J Immunol. 2005, 175, 4566–4574.
  4. Servet-Delprat C., Vidalain P.O., Bausinger H., Manié S., Le Deist F., Azocar O., Hanau D., Fischer A., Rabourdin-Combe C. Measles virus induces abnormal differentiation of CD40 ligand-activated human dendritic cells. J Immunol. 2000, 164, 1753–1760.
  5. Sakai S., Kawamura I., Okazaki T., Tsuchiya K., Uchiyama R., Mitsuyama M. PD-1-PD-L1 pathway impairs T(h)1 immune response in the late stage of infection with Mycobacterium bovis bacillus Calmette-Guerin. Int Immunol. 2010, 22, 915–925.
  6. Anderson K.M., Czinn S.J., Redline R.W., Blanchard T.G. Induction of CTLA-4-mediated anergy contributes to persistent colonization in the murine model of gastric Helicobacter pylori infection. J Immunol. 2006, 176. 5306–5313.
  7. Petrovas C., Casazza J.P., Brenchley J.M., Price D.A., Gostick E., Adams W.C., Precopio M.L., Schacker T., Roederer M., Douek D.C., Koup R.A. PD-1 is a regulator of virus-specific CD8+ T cell survival in HIV infection. J Exp Med. 2006, 203, 2281–2292.
  8. Bengsch B., Seigel B., Ruhl M., Timm J., Kuntz M., Blum H.E., Pircher H., Thimme R. Coexpression of PD-1, 2B4, CD160 and KLRG1 on exhausted HCV-specific CD8+ T cells is linked to antigen recognition and T cell differentiation. PLoS Pathog. 2010, 6, e1000947.
  9. Cornberg M., Kenney L.L., Chen A.T., Waggoner S.N., Kim S.-K., Dienes H.P., Welsh R.M., Selin L.K. Clonal Exhaustion as a Mechanism to Protect Against Severe Immunopathology and Death from an Overwhelming CD8 T Cell Response. Front Immunol. 2013, 4, 475–479.
  10. Akbar A.N., Henson S.M. Are senescence and exhaustion intertwined or unrelated processes that compromise immunity? Nat Rev Immunol. 2011. 11(4), 289–295.
  11. Plunkett F.J., Franzese O., Finney H.M., Fletcher J.M., Belaramani L.L., Salmon M., Dokal I., Webster D., Lawson A.D., Akbar A.N. The loss of telomerase activity in highly differentiated CD8+CD28-CD27-T cells is associated with decreased Akt (Ser473) phosphorylation. J Immunol. 2007, 178(12), 7710–7719.
  12. Wherry E.J. T cell exhaustion. Nat Immunol. 2011, 12(6), 492–499.
  13. Henson S.M., Franzese O., Macaulay R., Libri V., Azevedo R.I., Kiani-Alikhan S., Plunkett F.J., Masters J.E., Jackson S., Griffiths S.J., Pircher H.P., Soares M.V., Akbar A.N. KLRG1 signaling induces defective Akt (ser473) phosphorylation and proliferative dysfunction of highly differentiated CD8+ T cells. Blood 2009, 113(26), 6619–6628.
  14. Wherry E.J., Blattman J.N., Murali-Krishna K., van der Most R., Ahmed R. Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment. J Virol. 2003, 77(8), 4911–4927.
  15. Peretz Y., He Z., Shi Y., Yassine-Diab B., Goulet J.P., Bordi R., Filali-Mouhim A., Loubert J.B., El-Far M., Dupuy F.P., Boulassel M.R., Tremblay C., Routy J.P., Bernard N., Balderas R., Haddad E.K., Sékaly R.P. CD160 and PD-1 co-expression on HIV-specific CD8 T cells defines a subset with advanced dysfunction. PLoS Pathog. 2012, 8(8), e1002840.
  16. McLane L.M., Banerjee P.P., Cosma G.L., Makedonas G., Wherry E.J., Orange J.S., Betts M.R. Differential localization of T-bet and eomes in CD8 T cell memory populations. J Immunol. 2013, 190(7), 3207–3215.
  17. Shin H., Blackburn S.D., Intlekofer A.M., Kao C., Angelosanto J.M., Reiner S.L., Wherry E.J. A role for the transcriptional repressor Blimp-1 in CD8(+) T cell exhaustion during chronic viral infection. Immunity 2009, 31(2), 309–320.
  18. Paley M.A., Kroy D.C., Odorizzi P.M., Johnnidis J.B., Dolfi D.V., Barnett B.E., Bikoff E.K., Robertson E.J., Lauer G.M., Reiner S.L., Wherry E.J. Progenitor and terminal subsets of CD8 + T cells cooperate to contain chronic viral infection. Science. 2012, 338, 1220–1225.
  19. Crawford A., Angelosanto J.M., Kao C., Doering T.A., Odorizzi P.M., Barnett B.E., Wherry E.J. Molecular and transcriptional basis of CD4 + T cell dysfunction during chronic infection. Immunity. 2014, 40, 289–302.
  20. Kurktschiev P.D., Raziorrouh B., Schraut W., Backmund M., Wächtler M., Wendtner C.M., Bengsch B., Thimme R., Denk G., Zachoval R., Dick A., Spannagl M., Haas J., Diepolder H.M., Jung M.C., Gruener N.H. Dysfunctional CD8(+) T cells in hepatitis B and C are characterized by a lack of antigen-specific T-bet induction J Exp Med. 2014, 211, 2047–2059.
  21. Fuller M.J., Khanolkar A., Tebo A.E., Zajac A.J. Maintenance, loss, and resurgence of T cell responses during acute, protracted, and chronic viral infections. J. Immunol. 2004, 172, 4204–4214.
  22. Mackerness K.J., Cox M.A., Lilly L.M., Weaver C.T., Harrington L.E., Zajac A.J. Pronounced virus-dependent activation drives exhaustion but sustains IFN-γ transcript levels. J. Immunol. 2010, 185, 3643–3651.
  23. Angelosanto J.M., Blackburn S.D., Crawford A., Wherry E.J. Progressive Loss of Memory T Cell Potential and Commitment to Exhaustion during Chronic Viral Infection. J. Virol. 2012, 86, 8161–8170.
  24. Moorman J.P., Zhang C.L., Ni L., Ma C.J., Zhang Y., Wu X.Y., Thayer P., Islam T.M., Borthwick T., Yao Z.Q. Impaired hepatitis B vaccine response during chronic hepatitis C infection: involvement of the PD-1 pathway in regulating CD4 + T cell responses. Vaccine. 2011, 29, 3169–3176.
  25. McMahan R.H., Golden-Mason L., Nishimura M.I., McMahon B.J., Kemper M., Allen T.M., Gretch D.R., Rosen H.R. Tim-3 expression on PD-1 + HCV-specific human CTLs is associated with viral persistence, and its blockade restores hepatocyte-directed in vitro cytotoxicity. J. Clin. Invest. 2010, 1172, 4546–2557.
  26. Barber D.L., Wherry E.J., Masopust D., Zhu B., Allison J.P., Sharpe A.H., Freeman G.J., Ahmed R. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature. 2006, 439, 682–687.
  27. Penaloza-MacMaster P., Kamphorst A.O., Wieland A., Araki K., Iyer S.S., West E.E., O’Mara L., Yang S., Konieczny B.T., Sharpe A.H., Freeman G.J., Rudensky A.Y., Ahmed R. Interplay between regulatory T cells and PD-1 in modulating T cell exhaustion and viral control during chronic LCMV infection. J Exp Med. 2014, 211(9), 1905–1918.
  28. Day C.L., Kaufmann D.E., Kiepiela P., Brown J.A., Moodley E.S., Reddy S., Mackey E.W., Miller J.D., Leslie A.J., DePierres C., Mncube Z., Duraiswamy J., Zhu B., Eichbaum Q., Altfeld M., Wherry E.J., Coovadia H.M., Goulder P.J., Klenerman P., Ahmed R., Freeman G.J., Walker B.D. PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature 2006, 443(7109), 350–410.
  29. Boni C., Fisicaro P., Valdatta C., Amadei B., Di Vincenzo P., Giuberti T., Laccabue D., Zerbini A., Cavalli A., Missale G., Bertoletti A., Ferrari C. Characterization of hepatitis B virus (HBV)-specific T-cell dysfunction in chronic HBV infection. J Virol 2007, 81(8), 4215–4225.
  30. Bengsch B., Seigel B., Ruhl M., Timm J., Kuntz M., Blum H.E., Pircher H., Thimme R. Coexpression of PD-1, 2B4, CD160 and KLRG1 on exhausted HCV-specific CD8+ T cells is linked to antigen recognition and T cell differentiation. PLoS Pathog. 2010, 6(6), e1000947.
  31. Kared H., Fabre T., Bédard N., Bruneau J., Shoukry N.H. Galectin-9 and IL-21 mediate crossregulation between Th17 and Treg cells during acute hepatitis C. PLoS Pathog. 2013, 9(6), e1003422.
  32. Schurich A., Khanna P., Lopes A.R., Han K.J., Peppa D., Micco L., Nebbia G., Kennedy P.T., Geretti A.M., Dusheiko G., Maini M.K. Role of the coinhibitory receptor cytotoxic T lymphocyte antigen-4 on apoptosis-prone CD8 T cells in persistent hepatitis B virus infection. Hepatology 2011, 53(5), 1494–1503.
  33. Nebbia G., Peppa D., Schurich A., Khanna P., Singh H.D., Cheng Y., Rosenberg W., Dusheiko G., Gilson R., ChinAleong J., Kennedy P., Maini M.K. Upregulation of the Tim-3/galectin-9 pathway of T cell exhaustion in chronic hepatitis B virus infection. PLoS One 2012, 7(10), e47648.
  34. Klapper J.A., Downey S.G., Smith F.O., Yang J.C., Hughes M.S., Kammula U.S., Sherry R.M., Royal R.E., Steinberg S.M., Rosenberg S. High-dose interleukin-2 for the treatment of metastatic renal cell carcinoma: a retrospective analysis of response and survival in patients treated in the Surgery Branch at the National Cancer Institute between 1986 and 2006. Cancer. 2008, 113(2), 293–301.
  35. Su Z., Dannull J., Heiser A., Yancey D., Pruitt S., Madden J., Coleman D., Niedzwiecki D., Gilboa E., Vieweg J. Immunological and clinical responses in metastatic renal cancer patients vaccinated with tumor RNA-transfected dendritic cells. Cancer Research. 2003, 63(9), 2127–2133.
  36. Krane R.J., Carpinito G.A., Ross S.D., Lavin P.T., Osband M.E. Treatment of metastatic renal cell carcinoma with autolymphocyte therapy. Low toxicity outpatient approach to adoptive immunotherapy without use of in vivo interleukin-2. Urology. 1990, 35(5), 417–422.
  37. Ettinger D.S., Akerley W., Borghaei H., Chang A.C., Cheney R.T., Chirieac L.R., D’Amico T.A., Demmy T.L., Ganti A.K., Govindan R., Grannis Jr F.W., Horn L., Jahan T.M., Jahanzeb M., Kessinger A., Komaki R., Kong F.M., Kris M.G., Krug L.M., Lennes I.T., Loo Jr B.W., Martins R., O’Malley J., Osarogiagbon R.U., Otterson G.A., Patel J.D., Pinder-Schenck M.C., Pisters K.M., Reckamp K., Riely G.J., Rohren E., Swanson S.J., Wood D.E., Yang S.C., Hughes M., Gregory K.M. Non-small cell lung cancer. J Natl Compr Canc Netw. 2012, 10, 1236–1271.
  38. Mapara M., Sykes M. Tolerance and cancer: mechanisms of tumor evasion and strategies for breaking tolerance. J. Clin. Oncol. 2004, 22(6), 1136–1151.
  39. Liu Y., Zeng B., Zhang Z., Zhang Y., Yang R. B7-H1 on myeloid-derived suppressor cells in immune suppression by a mouse model of ovarian cancer. Clin Immunol. 2008, 129, 471–481.
  40. Nishikawa H., Sakaguchi S. Regulatory T cells in tumor immunity. Int J Cancer 2010, 127, 759–767.
  41. Lewis C.E., Pollard J.W. Distinct role of macrophages in different tumor microenvironments. Cancer Res. 2006, 66, 605–612.
  42. Katz L.H., Li Y., Chen J.S., Munoz N.M., Majumdar A., Chen J., Mishra L. Targeting TGF-beta signaling in cancer. Expert Opin Ther Targets 2013, 17, 743–760.
  43. Yamamoto R., Nishikori M., Kitawaki T., Sakai T., Hishizawa M., Tashima M., Kondo T., Ohmori K., Kurata M., Hayashi T., Uchiyama T. PD-1-PD-1 ligand interaction contributes to immunosuppressive microenvironment of Hodgkin lymphoma. Blood 2008, 111, 3220–3224.
  44. Fourcade J., Kudela P., Sun Z., Shen H., Land S.R., Lenzner D., Guillaume P., Luescher I.F., Sander C., Ferrone S., Kirkwood J.M., Zarour H.M. PD-1 is a regulator of NY-ESO-1-specific CD8+ T cell expansion in melanoma patients. J Immunol. 2009, 182, 5240–5249.
  45. Ahmadzadeh M., Johnson L.A., Heemskerk B., Wunderlich J.R., Dudley M.E., White D.E., Rosenberg S.A. Tumor antigen-specific CD8 T cells infiltrating the tumor express high levels of PD-1 and are functionally impaired. Blood 2009, 114, 1537–1544.
  46. Gehring A.J., Ho Z.Z., Tan A.T., Aung M.O., Lee K.H., Tan K.C., Lim S.G., Bertoletti A. Profile of tumor antigen-specific CD8 T cells in patients with hepatitis B virus-related hepatocellular carcinoma. Gastroenterology 2009, 137, 682–690.
  47. Saito H., Kuroda H., Matsunaga T., Osaki T., Ikeguchi M. Increased PD-1 expression on CD4+ and CD8+ T cells is involved in immune evasion in gastric cancer. J Surg Oncol. 2013, 107, 517–522.
  48. Fourcade J., Sun Z., Benallaoua M., Guillaume P., Luescher I.F., Sander C., Kirkwood J.M., Kuchroo V., Zarour H.M. Upregulation of Tim-3 and PD-1 expression is associated with tumor antigen-specific CD8+ T cell dysfunction in melanoma patients. J Exp Med. 2010, 207, 2175–2186.
  49. Woo S.R., Turnis M.E., Goldberg M.V., Bankoti J., Selby M., Nirschl C.J., Bettini M.L., Gravano D.M., Vogel P., Liu C.L., Tangsombatvisit S., Grosso J.F., Netto G., Smeltzer M.P., Chaux A., Utz P.J., Workman C.J., Pardoll D.M., Korman A.J., Drake C.G., Vignali D.A. Immune inhibitory molecules LAG-3 and PD-1 synergistically regulate T-cell function to promote tumoral immune escape. Cancer Res. 2012, 72, 917–927.
  50. Topalian S.L., Hodi F.S., Brahmer J.R., Gettinger S.N., Smith D.C., McDermott D.F., Powderly J.D., Carvajal R.D., Sosman J.A., Atkins M.B., Leming P.D., Spigel D.R., Antonia S.J., Horn L., Drake C.G., Pardoll D.M., Chen L., Sharfman W.H., Anders R.A., Taube J.M., McMiller T.L., Xu H., Korman A.J., Jure-Kunkel M., Agrawal S., McDonald D., Kollia G.D., Gupta A., Wigginton J.M., Sznol M. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med. 2012, 366, 2443–2454.
  51. Ghebeh H., Mohammed S., Al-Omair A., Qattan A., Lehe C., Al-Qudaihi G., Elkum N., Alshabanah M., Bin Amer S., Tulbah A., Ajarim D., Al-Tweigeri T., Dermime S. The B7-H1 (PD-L1) T lymphocyte-inhibitory molecule is expressed in breast cancer patients with infiltrating ductal carcinoma: correlation with important high-risk prognostic factors. Neoplasia 2006, 8, 190–198.
  52. Yang C.Y., Lin M.W., Chang Y.L., Wu C.T., Yang P.C. Programmed cell death-ligand 1 expression in surgically resected stage I pulmonary adenocarcinoma and its correlation with driver mutations and clinical outcomes. Eur J Cancer 2014, 50, 1361–1369.
  53. Thompson R.H., Kuntz S.M., Leibovich B.C., Dong H., Lohse C.M., Webster W.S., Sengupta S., Frank I., Parker A.S., Zincke H., Blute M.L., Sebo T.J., Cheville J.C., Kwon E.D. Tumor B7-H1 is associated with poor prognosis in renal cell carcinoma patients with long-term follow-up. Cancer Res. 2006, 66, 3381–3385.
  54. Nomi T., Sho M., Akahori T., Hamada K., Kubo A., Kanehiro H., Nakamura S., Enomoto K., Yagita H., Azuma M., Nakajima Y. Clinical significance and therapeutic potential of the programmed death-1 ligand/ programmed death-1 pathway in human pancreatic cancer. Clin Cancer Res. 2007, 13, 2151–2157.
  55. Taube J.M., Anders R.A., Young G.D., Xu H., Sharma R., McMiller T.L., Chen S., Klein A.P., Pardoll D.M., Topalian S.L., Chen L. Colocalization of inflammatory response with B7-h1 expression in human melanocytic lesions supports an adaptive resistance mechanism of immune escape. Sci Transl Med. 2012, 4, 127–137.
  56. Lin Y.-M., Sung W.-W., Hsieh M.-J., Tsai S.-C., Lai H.-W., Yang S.-M., Shen K.-H., Chen M.-K., Lee H., Yeh K.-T., Chen. C.-J. High PD-L1 Expression Correlates with Metastasis and Poor Prognosis in Oral Squamous Cell Carcinoma. PLoS One. 2015, 10(11), e0142656.
  57. Hodi F.S., O’Day S.J., McDermott D.F., Weber R.W., Sosman J.A., Haanen J.B., Gonzalez R., Robert C., Schadendorf D., Hassel J.C., Akerley W., van den Eertwegh A.J., Lutzky J., Lorigan P., Vaubel J.M., Linette G.P., Hogg D., Ottensmeier C.H., Lebbé C., Peschel C., Quirt I., Clark J.I., Wolchok J.D., Weber J.S., Tian J., Yellin M.J., Nichol G.M., Hoos A., Urba W.J. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med. 2010, 363, 711–723.
  58. Ribas A., Kefford R., Marshall M.A., Punt C.J., Haanen J.B., Marmol M., Garbe C., Gogas H., Schachter J., Linette G., Lorigan P., Kendra K.L., Maio M., Trefzer U., Smylie M., McArthur G.A., Dreno B., Nathan P.D., Mackiewicz J., Kirkwood J.M., Gomez-Navarro J., Huang B., Pavlov D., Hauschild A. Phas III randomized clinical trial comparing tremelimumab with standard-of-care chemotherapy in patient with advanced melanoma. J Clin Oncol. 2013, 31(5), 616–622.
  59. Yang J.C., Hughes M., Kammula U., Royal R., Sherry R.M., Topalian S.L., Suri K.B., Levy C., Allen T., Mavroukakis S., Lowy I., White D.E., Rosenberg S.A. Ipilimumab (anti-CTLA4 antibody) causes regression of metastatic renal cell cancer associated with enteritis and hypophysitis. J. Immunother. 2007, 30(8), 825–830.
  60. Truong P., Rahal A., Kallail K.J. Metastatic Hepatocellular Carcinoma Responsive to Pembrolizumab. Cureus. 2016, 8(6), e631.
  61. Motzer R.J., Escudier B., McDermott D.F., George S., Hammers H.J., Srinivas S., Tykodi S.S., Sosman J.A., Procopio G., Plimack E.R., Castellano D., Choueiri T.K., Gurney H., Donskov F., Bono P., Wagstaff J., Gauler T.C., Ueda T., Tomita Y., Schutz F.A., Kollmannsberger C., Larkin J., Ravaud A., Simon J.S., Xu L.A., Waxman I.M., Sharma P. Nivolumab versus everolimus in advanced renal-cell carcinoma. N Engl J Med. 2015. 373, 1803–1813.
  62. Reardon D.A., Gokhale P.C., Klein S.R., Ligon K.L., Rodig S.J., Ramkissoon S.H., Jones K.L., Conway A.S., Liao X., Zhou J., Wen P.Y., Van Den Abbeele A.D., Hodi F.S., Qin L., Kohl N.E., Sharpe A.H., Dranoff G., Freeman G.J. Glioblastoma Eradication Following Immune Checkpoint Blockade in an Orthotopic, Immunocompetent Model. Cancer Immunol Res. 2016, 4(2), 124–135.
  63. Armand P., Shipp M.A., Ribrag V., Michot J.M., Zinzani P.L., Kuruvilla J., Snyder E.S., Ricart A.D., Balakumaran A., Rose S., Moskowitz C.H. Programmed Death-1 Blockade With Pembrolizumab in Patients With Classical Hodgkin Lymphoma After Brentuximab Vedotin Failure. J Clin Oncol. 2016, 27, pii: JCO673467.
  64. Garon E.B., Rizvi N.A., Hui R., Leighl N., Balmanoukian A.S., Eder J.P., Patnaik A., Aggarwal C., Gubens M., Horn L., Carcereny E., Ahn M.J., Felip E., Lee J.S., Hellmann M.D., Hamid O., Goldman J.W., Soria J.C., Dolled-Filhart M., Rutledge R.Z., Zhang J., Lunceford J.K., Rangwala R., Lubiniecki G.M., Roach C., Emancipator K., Gandhi L. Pembrolizumab for the treatment of non-small-cell lung cancer. N Engl J Med. 2015, 372(21), 2018–2028.
  65. Fehrenbaher L., Spira A., Ballinger M., Kowanetz M., Vansteenkiste J., Mazieres J., Park K., Smith D., Artal-Cortes A., Lewanski C., Braiteh F., Waterkamp D., He P., Zou W., Chen D.S., Yi J., Sandler A., Rittmeyer A. Atezolizumab versus docetaxel for patients with previously treated non-small-cell lung cancer (POPLAR): a multicentre, open-label, phase 2 randomised controlled trial. Lancet. 2016. 387(10030), 1837–1846.
  66. Herbst R.S., Baas P., Kim D.W., Felip E., Pérez-Gracia J.L., Han J.Y., Molina J., Kim J.H., Arvis C.D., Ahn M.J., Majem M., Fidler M.J., de Castro Jr G., Garrido M., Lubiniecki G.M., Shentu Y., Im E., Dolled-Filhart M., Garon E.B. Pembrolizumab versus docetaxel for previously treated, PD-L1-positive, advanced non-small-cell lung cancer (KEYNOTE-010): a randomised controlled trial. Lancet. 2016, 387(10027), 1540–1550.
  67. Buchbinder E.I., Hodi F.S. Melanoma in 2015: Immune-checkpoint blockade – durable cancer control. Nat Rev Clin Oncol. 2016, 13(2), 77–78.
  68. Hofmann L., Forschner A., Loquai C., Goldinger S.M., Zimmer L., Ugurel S., Schmidgen M.I., Gutzmer R., Utikal J.S., Göppner D., Hassel J.C., Meier F., Tietze J.K., Thomas I., Weishaupt C., Leverkus M., Wahl R., Dietrich U., Garbe C., Kirchberger M.C., Eigentler T., Berking C., Gesierich A., Krackhardt A.M., Schadendorf D., Schuler G., Dummer R., Heinzerling L.M. Cutaneous, gastrointestinal, hepatic, endocrine, and renal side-effects of anti-PD-1 therapy. Eur J Cancer. 2016, 60, 190–209.
  69. Ludlow S.P., Kay N. Delayed dermatologic hypersensitivity reaction secondary to ipilimumab. J Immunother. 2015, 38(4), 165–166.
  70. Abdel-Wahab N., Shah M., Suarez-Almazor M.E. Adverse Events Associated with Immune Checkpoint Blockade in Patients with Cancer: A Systematic Review of Case Reports. PLoS One. 2016, 11(7), e0160221.
  71. Miyoshi Y., Ogawa O., Oyama Y. Nivolumab, an Anti-Programmed Cell Death-1 Antibody, Induces Fulminant Type 1 Diabetes. Tohoku J Exp Med. 2016, 239(2), 155–158.
  72. Min L., Hodi F.S., Giobbie-Hurder A., Ott P.A., Luke J.J., Donahue H., Davis M., Carroll R.S., Kaiser U.B. Systemic high-dose corticosteroid treatment does not improve the outcome of ipilimumab-related hypophysitis: a retrospective cohort study. Clin Cancer Res. 2015, 21(4), 749–755.
  73. Hsieh A.H., Ferman M., Brown M.P., Andrews J.M. Vedolizumab: a novel treatment for ipilimumabinduced colitis. BMJ Case Rep. 2016, 2016, pii: bcr2016216641.
  74. Kong B.Y., Micklethwaite K.P., Swaminathan S., Kefford R.F., Carlino M.S. Autoimmune hemolytic anemia induced by anti-PD-1 therapy in metastatic melanoma. Melanoma Res. 2016, 26(2), 202–204.
  75. Postow M.A., Chesney J., Pavlick A.C., Robert C., Grossmann K., McDermott D., Linette G.P., Meyer N., Giguere J.K., Agarwala S.S., Shaheen M., Ernstoff M.S., Minor D., Salama A.K., Taylor M., Ott P.A., Rollin L.M., Horak C., Gagnier P., Wolchok J.D., Hodi F.S. Nivolumab and ipilimumab versus ipilimumab in untreated melanoma. N Engl J Med. 2015, 372, 2006–2017.
  76. Larkin J., Hodi F.S., Wolchok J.D. Combined Nivolumab and Ipilimumab or Monotherapy in Untreated Melanoma. N Engl J Med. 2015, 373(13), 1270–1271.
  77. Yamazaki N., Uhara H., Fukushima S., Uchi H., Shibagaki N., Kiyohara Y., Tsutsumida A., Namikawa K., Okuyama R., Otsuka Y., Tokudome T. Phase II study of the immune-checkpoint inhibitor ipilimumab plus dacarbazine in Japanese patients with previously untreated, unresectable or metastatic melanoma. Cancer Chemother Pharmacol. 2015, 76(5), 969–975.
  78. de Velasco G., Krajewski K.M., Albiges L., Awad M.M., Bellmunt J., Hodi F.S., Choueiri T.K. Radiologic Heterogeneity in Responses to Anti-PD-1/PD-L1 Therapy in Metastatic Renal Cell Carcinoma. Cancer Immunol Res. 2016, 4(1), 12–17.
  79. Wightman F., Solomon A., Kumar S.S., Urriola N., Gallagher K., Hiener B., Palmer S., Mcneil C., Garsia R., Lewin S.R. Effect of ipilimumab on the HIV reservoir in an HIV-infected individual with metastatic melanoma. AIDS. 2015, 29(4), 504–506.
  80. Fuller M.J., Callendret B., Zhu B., Freeman G.J., Hasselschwert D.L., Satterfield W., Sharpe A.H., Dustin L.B., Rice C.M., Grakoui A., Ahmed R., Walker C.M. Immunotherapy of chronic hepatitis C virus infection with antibodies against programmed cell death-1 (PD-1). Proc. Natl. Acad. Sci. 2013, 110, 15001–15006.
  81. Davar D., Wilson M., Pruckner C., Kirkwood J.M. PD-1 Blockade in Advanced Melanoma in Patients with Hepatitis C and/or HIV. Case Rep Oncol Med. 2015, 2015, 737389.
  82. Gardiner D., Lalezari J., Lawitz E., DiMicco M., Ghalib R., Reddy K.R., Chang K.M., Sulkowski M., Marro S.O., Anderson J., He B., Kansra V., McPhee F., Wind-Rotolo M., Grasela D., Selby M., Korman A.J., Lowy I. A randomized, double-blind, placebo-controlled assessment of BMS-936558, a fully human monoclonal antibody to programmed death-1 (PD-1), in patients with chronic hepatitis C virus infection. PLoS One. 2013, 8, e63818.

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) 2018 Toptygina A.P.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № 77 - 11525 от 04.01.2002.


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies