Enhanced ADCC activity of affinity maturated and Fc-engineered mini-antibodies directed against the AML stem cell antigen CD96

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Mohseni Nodehi, Sahar ^a   Repp, Roland ^a   Kellner, Christian ^a   Bräutigam, Joachim ^a   Staudinger, Matthias ^a   Schub, Natalie ^a   Peipp, Matthias ^a   Gramatzki, Martin ^a   Humpe, Andreas ^a  

^a UNIVERSITY OF KIEL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CD16A ANTIGEN; CD96 ANTIGEN; CELL ANTIGEN; IMMUNOGLOBULIN G1; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY CD96; SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; ANTIBODY AFFINITY; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIGEN ANTIBODY COMPLEX; ANTIGEN SPECIFICITY; ARTICLE; BIOENGINEERING; CANCER STEM CELL; CELL ISOLATION; CONTROLLED STUDY; CYTOLYSIS; DRUG MECHANISM; DRUG SYNTHESIS; EFFECTOR CELL; HUMAN; HUMAN CELL; HYBRIDOMA; MUTAGENESIS; NONHUMAN; PHAGE DISPLAY; TUMOR CELL; WILD TYPE;

AMINO ACID SEQUENCE; ANTIBODY AFFINITY; ANTIBODY SPECIFICITY; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; ANTIGENS, CD; ANTIGENS, NEOPLASM; CELL LINE, TUMOR; DOSE-RESPONSE RELATIONSHIP, IMMUNOLOGIC; HUMANS; HYBRIDOMAS; IMMUNOGLOBULIN G; LEUKEMIA, MYELOID, ACUTE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; MUTATION; NEOPLASTIC STEM CELLS; PROTEIN BINDING; PROTEIN ENGINEERING; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, FC; SEQUENCE ALIGNMENT; SINGLE-CHAIN ANTIBODIES;

EID: 84864561123     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042426     Document Type: Article

References (53)

1. Bonnet D, Dick J, (1997) Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 3: 730-737.
2. Wang J, Dick J, (2005) Cancer stem cells: lessons from leukemia. Trends Cell Biol 15: 494-501.
3. Goardon N, Marchi E, Atzberger A, Quek L, Schuh A, et al. (2011) Coexistence of LMPP-like and GMP-like leukemia stem cells in acute myeloid leukemia. Cancer Cell 19: 138-152.
4. Kamel-Reid S, Dick J, (1988) Engraftment of immune-deficient mice with human hematopoietic stem cells. Science 242: 1706.
5. Gilliland D, Jordan C, Felix C, (2004) The molecular basis of leukemia. Hematology 2004: 80.
6. Guan Y, Gerhard B, Hogge D, (2003) Detection, isolation, and stimulation of quiescent primitive leukemic progenitor cells from patients with acute myeloid leukemia (AML). Blood 101: 3142.
7. Passegué E, Jamieson C, Ailles L, Weissman I, (2003) Normal and leukemic hematopoiesis: Are leukemias a stem cell disorder or a reacquisition of stem cell characteristics? Proc Natl Acad Sci U S A 100: 11842.
8. Reya T, Morrison S, Clarke M, Weissman I, (2001) Stem cells, cancer, and cancer stem cells. Nature. pp. 105-111.
9. Guan Y, Hogge D, (2000) Proliferative status of primitive hematopoietic progenitors from patients with acute myelogenous leukemia(AML). Leukemia 14: 2135-2141.
10. Jordan C, Guzman M, Noble M, (2006) Cancer stem cells. N Engl J Med 355: 1253.
11. Majeti R, (2011) Monoclonal antibody therapy directed against human acute myeloid leukemia stem cells. Oncogene 30: 1009-1019.
12. Hauswirth A, Florian S, Printz D, (2007) Expression of the target receptor CD33 in and chemotherapy synergistically kill infant and childhood MLL-rearranged CD34+/CD38-/CD123+ AML stem cells. Eur J Clin Invest 37: 73-82.
13. Vercauteren S, Zapf R, Sutherland D, (2007) Primitive AML progenitors from most CD34+ patients lack CD33 expression but progenitors from many CD34- AML patients express CD33. Cytotherapy 9: 194-204.
14. Jin L, Hope K, Zhai Q, Smadja-Joffe F, Dick J, (2006) Targeting of CD44 eradicates human acute myeloid leukemic stem cells. Nat Med 12: 1167-1174.
15. Munoz L, Nomdedeu J, Lopez O, Carnicer M, Bellido M, et al. (2001) Interleukin-3 receptor alpha chain (CD123) is widely expressed in hematologic malignancies. Haematologica 86: 1261.
16. Kugler M, Stein C, Kellner C, Mentz K, Saul D, et al. (2010) A recombinant trispecific single-chain Fv derivative directed against CD123 and CD33 mediates effective elimination of acute myeloid leukaemia cells by dual targeting. Br J Haematol 150: 574-586.
17. Bakker A, van den Oudenrijn S, Bakker A, Feller N, van Meijer M, et al. (2004) C-type lectin-like molecule-1: a novel myeloid cell surface marker associated with acute myeloid leukemia. Cancer Res 64: 8443.
18. Zhao X, Singh S, Pardoux C, Zhao J, Hsi ED, et al. (2010) Targeting C-type lectin-like molecule-1 for antibody-mediated immunotherapy in acute myeloid leukemia. Haematologica 95: 71-78.
19. Majeti R, Chao M, Alizadeh A, Pang W, Jaiswal S, et al. (2009) CD47 is an adverse prognostic factor and therapeutic antibody target on human acute myeloid leukemia stem cells. Cell 138: 286-299.
20. Jan M, Chao MP, Cha AC, Alizadeh AA, Gentles AJ, et al. (2011) Prospective separation of normal and leukemic stem cells based on differential expression of TIM3, a human acute myeloid leukemia stem cell marker. Proc Natl Acad Sci U S A 108: 5009-5014.
21. Hosen N, Park C, Tatsumi N, Oji Y, Sugiyama H, et al. (2007) CD96 is a leukemic stem cell-specific marker in human acute myeloid leukemia. Proc Natl Acad Sci U S A 104: 11008.
22. Gramatzki M, Ludwig W, Burger R, Moos P, Rohwer P, et al. (1998) Antibodies TC-12 ("unique") and TH-111 (CD96) characterize T-cell acute lymphoblastic leukemia and a subgroup of acute myeloid leukemia. Exp Hematol 26: 1209.
23. Wang P, O'Farrell S, Clayberger C, Krensky A, (1992) Identification and molecular cloning of tactile. A novel human T cell activation antigen that is a member of the Ig gene superfamily. J Immunol 148: 2600.
24. Burger R, Hansen-Hagge T, Drexler H, Gramatzki M, (1999) Heterogeneity of T-acute lymphoblastic leukemia (T-ALL) cell lines: suggestion for classification by immunophenotype and T-cell receptor studies. Leukemia Res 23: 19-27.
25. Fuchs A, Cella M, Giurisato E, Shaw A, Colonna M, (2004) Cutting edge: CD96 (tactile) promotes NK cell-target cell adhesion by interacting with the poliovirus receptor (CD155). J Immunol 172: 3994.
26. Lafrenie R, Buckner C, Bewick M, (2007) Cell adhesion and cancer: is there a potential for therapeutic intervention? Expert Opin Ther Tar 11: 727-731.
27. Adams G, McCartney J, Tai M, Oppermann H, Huston J, et al. (1993) Highly specific in vivo tumor targeting by monovalent and divalent forms of 741F8 anti-c-erbB-2 single-chain Fv. Cancer Res 53: 4026.
28. Carter PJ, (2006) Potent antibody therapeutics by design. Nat Review Immunol 6: 343-357.
29. Clynes RA, Towers TL, Presta LG, Ravetch JV, (2000) Inhibitory Fc receptors modulate in vivo cytoxicity against tumor targets. Nat Med 6: 443-446.
30. de Haij S, Jansen JH, Boross P, Beurskens FJ, Bakema JE, et al. (2010) In vivo Cytotoxicity of Type I CD20 Antibodies Critically Depends on Fc Receptor ITAM Signaling. Cancer Res 70: 3209-3217.
31. Weng WK, Levy R, (2003) Two immunoglobulin G fragment C receptor polymorphisms independently predict response to rituximab in patients with follicular lymphoma. J Clin Oncol 21: 3940-3947.
32. Desjarlais JR, Lazar GA, Zhukovsky EA, Chu SY, (2007) Optimizing engagement of the immune system by anti-tumor antibodies: an engineer's perspective. Drug Discov Today 12: 898-910.
33. Nimmerjahn F, Ravetch JV, (2005) Divergent immunoglobulin g subclass activity through selective Fc receptor binding. Science 310: 1510-1512.
34. Tang Y, Lou J, Alpaugh RK, Robinson MK, Marks JD, et al. (2007) Regulation of antibody-dependent cellular cytotoxicity by IgG intrinsic and apparent affinity for target antigen. J Immunol 179: 2815-2823.
35. Hayden-Ledbetter MS, Cerveny CG, Espling E, Brady WA, Grosmaire LS, et al. (2009) CD20-directed small modular immunopharmaceutical, TRU-015, depletes normal and malignant B cells. Clin Cancer Res 15: 2739-2746.
36. Zhao X, Lapalombella R, Joshi T, Cheney C, Gowda A, et al. (2007) Targeting CD37-positive lymphoid malignancies with a novel engineered small modular immunopharmaceutical. Blood 110: 2569-2577.
37. Lazar GA, Dang W, Karki S, Vafa O, Peng JS, et al. (2006) Engineered antibody Fc variants with enhanced effector function. Proc Natl Acad Sci U S A 103: 4005-4010.
38. Shields R, Namenuk A, Hong K, Meng Y, Rae J, et al. (2001) High resolution mapping of the binding site on human IgG1 for Fcgamma RI, Fcgamma RII, Fcgamma RIII, and FcRn and design of IgG1 variants with improved binding to the Fcgamma R. J Biol Chem. 276: 6591.
39. Okazaki A, Shoji-Hosaka E, Nakamura K, Wakitani M, Uchida K, et al. (2004) Fucose depletion from human IgG1 oligosaccharide enhances binding enthalpy and association rate between IgG1 and Fc [gamma] RIIIa. J Mol Biol 336: 1239-1249.
40. Shields R, Lai J, Keck R, O'Connell L, Hong K, et al. (2002) Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human Fcgamma RIII and antibody-dependent cellular toxicity. J Biol Chem 277: 26733.
41. Peipp M, van Bueren L, Jeroen J, Schneider-Merck T, Bleeker W, et al. (2008) Antibody fucosylation differentially impacts cytotoxicity mediated by NK and PMN effector cells. Blood 112: 2390.
42. Repp R, Kellner C, Muskulus A, Staudinger M, Mohsni Nodehi S, et al. (2011) Combined Fc-protein- and Fc-glyco-engineering of scFv-Fc fusion proteins synergistically enhances CD16a binding but does not further enhance NK-cell mediated ADCC. J Immunol Methods epub.
43. Laemmli U, (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
44. Krebber A, Bornhauser S, Burmester J, Honegger A, Willuda J, et al. (1997) Reliable cloning of functional antibody variable domains from hybridomas and spleen cell repertoires employing a reengineered phage display system. J Immunol Methods 201: 35-55.
45. Kipriyanov S, Moldenhauer G, Little M, (1997) High level production of soluble single chain antibodies in small-scale Escherichia coli cultures. J Immunol Methods 200: 69-77.
46. Sircar A, Kim ET, Gray JJ, (2009) RosettaAntibody: antibody variable region homology modeling server. Nucleic Acids Res 37: W474-479.
47. Carroll WL, Mendel E, Levy S, (1988) Hybridoma fusion cell lines contain an aberrant kappa transcript. Mol Immunol 25: 991-995.
48. Vidarsson G, van de Winkel JG, van Dijk MA, (2001) Multiplex screening for functionally rearranged immunoglobulin variable regions reveals expression of hybridoma-specific aberrant V-genes. J Immunol Methods 249: 245-252.
49. Toleikis L, Broders O, Dubel S, (2004) Cloning single-chain antibody fragments (scFv) from hybridoma cells. Methods Mol Med 94: 447-458.
50. Kellner C, Bruenke J, Stieglmaier J, Schwemmlein M, Schwenkert M, et al. (2008) A novel CD19-directed recombinant bispecific antibody derivative with enhanced immune effector functions for human leukemic cells. J Immunother 31: 871-884.
51. McCall AM, Shahied L, Amoroso AR, Horak EM, Simmons HH, et al. (2001) Increasing the affinity for tumor antigen enhances bispecific antibody cytotoxicity. J Immunol 166: 6112-6117.
52. Wang J, Palzkill T, Chow D, (2009) Structural Insight into the Kinetics and Cp of Interactions between TEM-1-Lactamase and-Lactamase Inhibitory Protein (BLIP). J Biol Chem 284: 595.
53. Kabat EA, Wu TT, Perry HM, Gottesman KS, Foeller C (1991) Sequences of proteins of immunological interest. Bethesda: MD: US Depatment of Health and Human Services, National Institutes of Health.