Committing cytomegalovirus-specific CD8 T cells to eliminate tumor cells by bifunctional major histocompatibility class I antibody fusion molecules

Cancer Immunology Research

Volumn 3, Issue 7, 2015, Pages 764-776

  Schmittnaegel, Martina ^a   Levitsky, Victor ^b   Hoffmann, Eike ^a   Georges, Guy ^a   Mundigl, Olaf ^a   Klein, Christian ^b   Knoetgen, Hendrik ^a  

^a ROCHE INNOVATION CENTER MUNICH   (Germany)

^b Oncology Drug Discovery Unit   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; IMMUNOGLOBULIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; VIRUS PROTEIN; ANTIBODY; HLA A2 ANTIGEN; HLA ANTIGEN CLASS 1; HLA-A*02:01 ANTIGEN; PEPTIDE;

ANIMAL CELL; ANTIGEN SPECIFICITY; ANTIGENICITY; ARTICLE; BINDING AFFINITY; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; CYTOTOXIC T LYMPHOCYTE; DRUG EFFICACY; DRUG SAFETY; FEASIBILITY STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN EXPRESSION; T LYMPHOCYTE ACTIVATION; TARGET CELL; TUMOR CELL; ANIMAL; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MONONUCLEAR CELL; TUMOR CELL LINE;

ANIMALS; ANTIBODIES; CELL LINE, TUMOR; CYTOMEGALOVIRUS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HLA-A2 ANTIGEN; HUMANS; LEUKOCYTES, MONONUCLEAR; LYMPHOCYTE ACTIVATION; MICE; PEPTIDES; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84962020054     PISSN: 23266066     EISSN: 23266074     Source Type: Journal    
DOI: 10.1158/2326-6066.CIR-15-0037     Document Type: Article

References (61)

1. Kaech SM, Wherry RJ, Ahmed R. Effector and memory T-cell differentiation: implications for vaccine development. Nat Rev Immunol 2002;2:251-62.
2. Cannon MJ, Schmid DS, Hyde TB. Review of cytomegalovirus seroprevalence and demographic characteristics associated with infection. Rev Med Virol 2010;20:202-13.
3. Goodrum F, Caviness K, Zagallo P. Human cytomegalovirus persistence. Cell Microbiol 2012;14:644-55.
4. Seckert CK, Griessl M, Büttner JK, Scheller S, Simon CO, Kropp KA, et al. Viral latency drives 'memory inflation': a unifying hypothesis linking two hallmarks of cytomegalovirus infection. Med Microbiol Immunol 2012;201:551-66.
5. Snyder CM. Buffered memory: a hypothesis for the maintenance of functional, virus-specific CD8 (+) T cells during cytomegalovirus infection. Immunol Res 2011;51:195-204.
6. Hislop AD, Annels NE, Gudgeon NH, Leese AM, Rickinson AB. Epitopespecific evolution of human CD8 (+) T cell responses from primary to persistent phases of Epstein-Barr virus infection. J Exp Med 2002;195:893-905.
7. Khan N, Shariff N, Cobbold M, Bruton R, Ainsworth JA, Sinclair AJ, et al. Cytomegalovirus seropositivity drives the CD8 T cell repertoire toward greater clonality in healthy elderly individuals. J Immunol 2002;169:1984-92.
8. Wills MR, Carmichael AJ, Mynard K, Jin X, Weekes MP, Plachter B, et al. The human cytotoxic T-lymphocyte (CTL) response to cytomegalovirus is dominated by structural protein pp65: frequency, specificity, and T-cell receptor usage of pp65-specific CTL. J Virol 1996;70:7569-79.
9. Gratama JW, Brooimans RA, van der Holt B, Sintnicolaas K, van Doornum G, Niesters HG, et al. Monitoring cytomegalovirus IE-1 and pp65-specific CD4+ and CD8+ T-cell responses after allogeneic stem cell transplantation may identify patients at risk for recurrent CMV reactivations. Cytometry B Clin Cytom 2008;74:211-20.
10. Peggs KS, Thomson K, Samuel E, Dyer G, Armoogum J, Chakraverty R, et al. Directly selected cytomegalovirus-reactive donor T cells confer rapid and safe systemic reconstitution of virus-specific immunity following stem cell transplantation. Clin Infect Dis 2011;52:49-57.
11. Schuessler A, Smith C, Beagley L, Boyle GM, Rehan S, Matthews K, et al. Autologous T-cell therapy for cytomegalovirus as a consolidative treatment for recurrent glioblastoma. Cancer Res 2014;74:3466-76.
12. Derhovanessian E, Maier AB, Hähnel K, Beck R, de Craen AJ, Slagboom EP, et al. Infection with cytomegalovirus but not herpes simplex virus induces the accumulation of late-differentiatedCD4+ and CD8+ T-cells in humans. J Gen Virol 2011;92:2746-56.
13. Wills MR, Okecha G, Weekes MP, Gandhi MK, Sissons PJ, Carmichael AJ. Identification of naive or antigen-experienced human CD8 (+) T cells by expression of costimulation and chemokine receptors: analysis of the human cytomegalovirus-specific CD8 (+) T cell response. J Immunol 2002;168:5455-64.
14. van Leeuwen EM, de Bree GJ, ten Berge IJ, van Lier RA. Human virus-specific CD8+ T cells: diversity specialists. Immunol Rev 2006;211:225-35.
15. Khan N, Hislop A, Gudgeon N, Cobbold M, Khanna R, Nayak L, et al. Herpesvirus-specific CD8 T cell immunity in old age: cytomegalovirus impairs the response to a coresident EBV infection. J Immunol 2004;173:7481-9.
16. Powers C, DeFilippis V, Malouli D, Früh K. Cytomegalovirus immune evasion. Curr Top Microbiol Immunol 2008;325:333-59.
17. Baitsch L, Fuertes-Marraco SA, Legat A, Meyer C, Speiser DE. The three main stumbling blocks for anticancer T cells. Trends Immunol 2012;33:364-72.
18. Gilboa E. How tumors escape immune destruction and what we can do about it. Cancer Immunol Immunother 1999;48:382-5.
19. Lev A, Noy R, Oved K, Novak H, Segal D, Walden P, et al. Tumor-specific Abmediated targeting of MHC-peptide complexes induces regression of human tumor xenografts in vivo. Proc Natl Acad Sci U S A 2004;101:9051-6.
20. Cesson V, Stirnemann K, Robert B, Luescher I, Filleron T, Corradin G, et al. Active antiviral T-lymphocyte response can be redirected against tumor cells by antitumor antibody x MHC/viral peptide conjugates. Clin Cancer Res 2006;12:7422-30.
21. Aptsiauri N, Carretero R, Garcia-Lora A, Real LM, Cabrera T, Garrido F. Regressing and progressing metastatic lesions: resistance to immunotherapy is predetermined by irreversible HLA class I antigen alterations. Cancer Immunol Immunother 2008;57:1727-33.
22. Kim S, Li L, McMurtrey CP, Hildebrand WH, Weidanz JA, Gillanders WE, et al. Single-chain HLA-A2 MHC trimers that incorporate an immundominant peptide elicit protective T cell immunity against lethal West Nile virus infection. J Immunol 2010;184:4423-30.
23. Lev A, Novak H, Segal D, Reiter Y. Recruitment of CTL activity by tumorspecific antibody-mediated targeting of single-chain class I MHC-peptide complexes. J Immunol 2002;169:2988-96.
24. Novak H, Noy R, Oved K, Segal D, Wels WS, Reiter Y. Selective antibodymediated targeting of class I MHC to EGFR-expressing tumor cells induces potent antitumor CTL activity in vitro and in vivo. Int J Cancer 2007;120:329-36.
25. King BC, Hamblin AD, Savage PM, Douglas LR, Hansen TH, French RR, et al. Antibody-peptide-MHC fusion conjugates target non-cognate T cells to kill tumour cells. Cancer Immunol Immunother 2013;62:1093-105.
26. Ligensa T, Krauss S, Demuth D, Schumacher R, Camonis J, Jaques G, et al. A PDZ domain protein interacts with the C-terminal tail of the insulin-like growth factor-1 receptor but not with the insulin receptor. J Biol Chem 2001;276:33419-27.
27. Greten TF, Korangy F, Neumann G, Wedemeyer H, Schlote K, Heller A, et al. Peptide-beta2-microglobulin-MHC fusion molecules bind antigen-specific T cells and can be used for multivalent MHC-Ig complexes. J Immunol Methods 2002;271:125-35.
28. Truscott SM, Wang X, Lybarger L, Biddison WE, McBerry C, Martinko JM, et al. Human major histocompatibility complex (MHC) class I molecules with disulfide traps secure disease-related antigenic peptides and exclude competitor peptides. J Biol Chem 2008;283:7480-90.
29. Oved K, Lev A, Noy R, Segal D, Reiter Y. Antibody-mediated targeting of human single-chain class I MHC with covalently linked peptides induces efficient killing of tumor cells by tumor or viral-specific cytotoxic T lymphocytes. Cancer Immunol Immunother 2005;54:867-79.
30. Moessner E, Tuffin G, Colombetti S, Freytag O, Moser S, Dunn C, et al. M4-3-ML2, a novel glycoengineered humanized IgG1 antibody, targeting a membrane-proximal epitope of MCSP/CSPG4 exhibits potent ADCC induction in vitro and in vivo anti-tumoral efficacy in disseminated melanoma models Cancer Res 2012;72(8):Suppl LB-236.
31. Croasdale R, Wartha K, Schanzer JM, Kuenkele KP, Ries C, Mayer K, et al. Development of tetravalent IgG1 dual targeting IGF-1R-EGFR antibodies with potent tumor inhibition. Arch Biochem Biophy 2012;526:206-18.
32. Burns WR, Zhao Y, Frankel TL, Hinrichs CS, Zheng Z, Xu H, et al. A high molecular weight melanoma-associated antigen-specific chimeric antigen receptor redirects lymphocytes to target human melanomas. Cancer Res 2010;70:3027-33.
33. Tomlinson IM, Walter G, Marks JD, Llewelyn MB, Winter G. The repertoire of human germline VH sequences reveals about fifty groups of VH segments with different hypervariable loops. J Mol Biol 1992;227:776-98.
34. Merchant AM, Zhu Z, Yuan JQ, Goddard A, Adams CW, Presta LG, et al. An efficient route to human bispecific IgG. Nat Biotechnol 1998;16:677-81.
35. Ridgway JB, Presta LG, Carter P. 'Knobs-into-holes' engineering of antibody CH3 domains for heavy chain heterodimerization. Protein Eng 1996;9:617-21.
36. Baehner M, Jenewein S, Kubbies M, Moessner E, Schlothauer. T xsantibody Fc variants. US20120251531. Hoffmann-La Roche Inc. 2012.
37. Knoetgen H. Complexes comprising MHC class I fusion polypeptides and antigen-specific antibodies and methods of use. US20130011394. Hoffmann-La Roche Inc. 2013.
38. Lybarger L, Yu LYY, Miley MJ, Fremont DH, Myers N, Primeau T, et al. Enhanced immune presentation of a single-chain major histocompatibility complex class I molecule engineered to optimize linkage of a C-terminally extended peptide. J Biol Chem 2003;278:27105-11.
39. Wu C, Ying H, Grinnell C, Bryant S, Miller R, Clabbers A, et al. Simultaneous targeting of multiple disease mediators by a dual-variable-domain immunoglobulin. Nat Biotechnol 2007;25:1290-7.
40. Restifo NP, Dudley ME, Rosenberg SA. Adoptive immunotherapy for cancer: harnessing the T cell response. Nat Rev Immunol 2012;12:269-81.
41. Lilleri D, Fornara C, Revello MG, Gerna G. Human cytomegalovirusspecific memory CD8+ and CD4+ T cell differentiation after primary infection. J Infect Dis 2008;198:536-43.
42. Kaech SM, Tan JT, Wherry EJ, Konieczny BT, Surh CD, Ahmed R. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat Immunol 2003;4:1191-8.
43. Rea IM, McNerlan SE, Alexander HD. CD69, CD25, and HLA-DR activation antigen expression on CD3+ lymphocytes and relationship to serum TNF-alpha, IFN-gamma, and sIL-2R levels in aging. Exp Gerontol 1999;34:79-93.
44. Kobayashi N, Kondo T, Takata H, Yokota S, Takiguchi M. Functional and phenotypic analysis of human memory CD8+ T cells expressing CXCR3. J Leukoc Biol 2006;80:320-9.
45. Zimmermann C, Prévost-Blondel A, Blaser C, Pircher H. Kinetics of the response of naive and memory CD8 T cells to antigen: similarities and differences. Eur J Immunol 1999;29:284-90.
46. Mack M, Riethmuller G, Kufer P. A small bispecific antibody construct expressed as a functional single-chain molecule with high tumor cell cytotoxicity. Proc Natl Acad Sci U S A 1995;92:7021-5.
47. Teachey DT, Rheingold SR, Maude SL, Zugmaier G, Barrett DM, Seif AE, et al. Cytokine release syndrome after blinatumomab treatment related to abnormal macrophage activation and ameliorated with cytokine-directed therapy. Blood 2013;121:5154-7.
48. Cosmi L, Annunziato F, Galli MIG, Maggi RME, Nagata K, Romagnani S. CRTH2 is the most reliable marker for the detection of circulating human type 2 Th and type 2 T cytotoxic cells in health and disease. Eur J Immunol 2000;30:2972-9.
49. Corrigan-Curay J, Kiem HP, Baltimore D, O'Reilly M, Brentjens RJ, Cooper L, et al. T-cell immunotherapy: looking forward. Mol Ther 2014;22:1564-74.
50. Waller EC, McKinney N, Hicks R, Carmichael AJ, Sissons JG, Wills MR. Differential costimulation through CD137 (4-1BB) restores proliferation of human virus-specific "effector memory" (CD28 (-) CD45RA (HI)) CD8 (+) T cells. Blood 2007;110:4360-6.
51. te Raa GD, Pascutti MF, García-Vallejo JJ, Reinen E, Remmerswaal EB, ten Berge IJ, et al. CMV-specific CD8+ T-cell function is not impaired in chronic lymphocytic leukemia. Blood 2014;123:717-24.
52. Dziurzynski K, Chang SM, Heimberger AB, Kalejta RF, McGregor Dallas SR, Smit M, et al. Consensus on the role of human cytomegalovirus in glioblastoma. Neuro Oncol 2012;14:246-55.
53. Michaelis M, Doerr HW, Cinatl J. The story of human cytomegalovirus and cancer: increasing evidence and open questions. Neoplasia 2009;11:1-9.
54. Prins RM, Cloughesy TF, Liau LM. Cytomegalovirus immunity after vaccination with autologous glioblastoma lysate. N Engl J Med 2008;359:539-41.
55. Mous R, Savage P, Remmerswaal EB, van Lier RA, Eldering E, van Oers MH. Redirection of CMV-specific CTL towards B-CLL via CD20-targeted HLA/CMV complexes. Leukemia 2006;20:1096-102.
56. Matsui K, Boniface JJ, Reay PA, Schild H, Fazekas de St Groth B, Davis MM. Low affinity interaction of peptide-MHC complexes with T cell receptors. Science 1991;254:1788-91.
57. Solberg OD, Mack SJ, Lancaster AK, Single RM, Tsai Y, Sanchez-Mazas A, et al. Balancing selection and heterogeneity across the classical human leukocyte antigen loci: a meta-analytic review of 497 population studies. Hum Immunol 2008;69:443-64.
58. Dowd J, Aiello AE, Alley DE. Socioeconomic disparities in the seroprevalence of cytomegalovirus infection in the US population: NHANES III. Epidemiol Infect 2009;137:58-65.
59. Hecker M, Qiu D, Marquardt K, Bein G, Hackstein H. Continuous cytomegalovirus seroconversion in a large group of healthy blood donors. Vox Sang 2004;86:41-4.
60. Ross SA, Novak Z, Pati S, Boppana SB. Overview of the diagnosis of cytomegalovirus infection. Infect Disord Drug Targets 2011;11:466-74.
61. Azuma F, Kashiwase K. [HLA genotyping for molecular epidemiological analysis of humans]. Rinsho Byori 2013;61:1026-34.