Targeted ex vivo reduction of CD64-positive monocytes in chronic myelomonocytic leukemia and acute myelomonocytic leukemia using human granzyme B-based cytolytic fusion proteins

International Journal of Cancer

Volumn 135, Issue 6, 2014, Pages 1497-1508

  Schiffer, Sonja ^a,b   Rosinke, Reinhard ^b   Jost, Edgar ^a   Hehmann Titt, Grit ^c   Huhn, Michael ^a   Melmer, Georg ^c   Barth, Stefan ^a,b   Thepen, Theo ^b  

^a UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^b FRAUNHOFER INSTITUTE FOR MOLECULAR BIOLOGY AND APPLIED ECOLOGY IME   (Germany)

^c PharmedArtis GmbH   (Germany)

Author keywords

immunotoxin; leukemia; serpin B9; therapy resistance

Indexed keywords

ANTILEUKEMIC AGENT; CD14 ANTIGEN; CD33 ANTIGEN; CD56 ANTIGEN; CD64 ANTIGEN; CYTOLYTIC FUSION PROTEIN; GRANZYME B; IMMUNOTOXIN; MUTANT PROTEIN; PEPTIDES AND PROTEINS; PROTEIN PI9; UNCLASSIFIED DRUG;

ACUTE MYELOMONOCYTIC LEUKEMIA; ADULT; AGED; ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; CANCER IMMUNOTHERAPY; CHRONIC MYELOMONOCYTIC LEUKEMIA; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG BLOOD LEVEL; DRUG CYTOTOXICITY; DRUG STABILITY; ENZYME ACTIVITY; EX VIVO STUDY; FEMALE; HUMAN; HUMAN CELL; MALE; MONOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; WILD TYPE;

IMMUNOTOXIN; LEUKEMIA; SERPIN B9; THERAPY-RESISTANCE;

AGED; AGED, 80 AND OVER; DRUG STABILITY; FEMALE; GRANZYMES; HL-60 CELLS; HUMANS; IMMUNOTOXINS; LEUKEMIA, MYELOMONOCYTIC, ACUTE; LEUKEMIA, MYELOMONOCYTIC, CHRONIC; MALE; MIDDLE AGED; RECEPTORS, IGG; RECOMBINANT FUSION PROTEINS; SINGLE-CHAIN ANTIBODIES;

EID: 84903956915     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.28786     Document Type: Article

References (51)

1. Vardiman JW, Imbert M, Pierre R, et al. Chronic myelomonocytic leukaemia. In:, Jaffe ES, Harris NL, Sten H, Vardiman JW, eds. World Health Organization Classification of Tumors: Pathology and Genetics of Tumours of Haematopoietic and Lymphoid Tissues. Lyon: IARC Press, 2001. 49-52.
2. Vardiman JW, Harris NL, Brunning RD,. The World Health Organization (WHO) classification of the myeloid neoplasms. Blood 2002; 100: 2292-302.
3. Hall J, Foucar K,. Diagnosing myelodysplastic/myeloproliferative neoplasms: laboratory testing strategies to exclude other disorders. Int J Lab Hematol 2010; 32: 559-71.
4. Orazi A, Germing U,. The myelodysplastic/myeloproliferative neoplasms: myeloproliferative diseases with dysplastic features. Leukemia 2008; 22: 1308-19.
5. Xu Y, McKenna RW, Karandikar NJ, et al. Flow cytometric analysis of monocytes as a tool for distinguishing chronic myelomonocytic leukemia from reactive monocytosis. Am J Clin Pathol 2005; 124: 799-806.
6. Vuckovic S, Fearnley DB, Gunningham S, et al. Dendritic cells in chronic myelomonocytic leukaemia. Brit J Haematol 1999; 105: 974-85.
7. Orazi A, Chiu R, O'Malley DP, et al. Chronic myelomonocytic leukemia: the role of bone marrow biopsy immunohistology. Mod Pathol 2006; 19: 1536-45.
8. Fenaux P, Beuscart R, Lai JL, et al. Prognostic factors in adult chronic myelomonocytic leukemia: an analysis of 107 cases. J Clin Oncol 1988; 6: 1417-24.
9. Onida F, Ball G, Kantarjian HM, et al. Characteristics and outcome of patients with Philadelphia chromosome negative, bcr/abl negative chronic myelogenous leukemia. Cancer 2002; 95: 1673-84.
10. Itzykson R, Kosmider O, Renneville A, et al. Clonal architecture of chronic myelomonocytic leukemias. Blood 2013; 121: 2186-98.
11. Germing U, Neukirchen J,. How to treat patients with CMML? Leuk Res 2013; 37: 605-606.
12. Fenaux P, Mufti GJ, Hellstrom-Lindberg E, et al. Efficacy of azacitidine compared with that of conventional care regimens in the treatment of higher-risk myelodysplastic syndromes: a randomised, open-label, phase III study. Lancet Oncol 2009; 10: 223-232.
13. Rollins-Raval MA, Roth CG,. The value of immunohistochemistry for CD14, CD123, CD33, myeloperoxidase and CD68R in the diagnosis of acute and chronic myelomonocytic leukaemias. Histopathology 2012; 60: 933-42.
14. Kreitman RJ,. Immunotoxins for targeted cancer therapy. AAPS J 2006; 8: E532-51.
15. Walter RB, Appelbaum FR, Estey EH, et al. Acute myeloid leukemia stem cells and CD33-targeted immunotherapy. Blood 2012; 119: 6198-208.
16. Mathew M, Verma RS,. Humanized immunotoxins: a new generation of immunotoxins for targeted cancer therapy. Cancer Sci 2009; 100: 1359-65.
17. Kurschus FC, Jenne DE,. Delivery and therapeutic potential of human granzyme B. Immunol Rev 2010; 235: 159-71.
18. Liu Y, Cheung LH, Hittelman WN, et al. Targeted delivery of human pro-apoptotic enzymes to tumor cells: in vitro studies describing a novel class of recombinant highly cytotoxic agents. Mol Cancer Ther 2003; 2: 1341-50.
19. Kurschus FC, Fellows E, Stegmann E, et al. Granzyme B delivery via perforin is restricted by size, but not by heparan sulfate-dependent endocytosis. Proc Natl Acad Sci U S A 2008; 105: 13799-804.
20. Zhang L, Zhao J, Wang T, et al. HER2-targeting recombinant protein with truncated pseudomonas exotoxin A translocation domain efficiently kills breast cancer cells. Cancer Biol Therapy 2008; 7: 1226-31.
21. Clement MV, Haddad P, Soulie A, et al. Involvement of granzyme B and perforin gene expression in the lytic potential of human natural killer cells. Nouv Rev Fr Hematol 1990; 32: 349-52.
22. Raja SM, Wang B, Dantuluri M, et al. Cytotoxic cell granule-mediated apoptosis. Characterization of the macromolecular complex of granzyme B with serglycin. J Biol Chem 2002; 277: 49523-30.
23. Barry M, Heibein JA, Pinkoski MJ, et al. Granzyme B short-circuits the need for caspase 8 activity during granule-mediated cytotoxic T-lymphocyte killing by directly cleaving Bid. Mol Cell Biol 2000; 20: 3781-94.
24. Metkar SS, Wang B, Ebbs ML, et al. Granzyme B activates procaspase-3 which signals a mitochondrial amplification loop for maximal apoptosis. J Cell Biol 2003; 160: 875-85.
25. Trapani JA, Jans DA, Jans PJ, et al. Efficient nuclear targeting of granzyme B and the nuclear consequences of apoptosis induced by granzyme B and perforin are caspase-dependent, but cell death is caspase-independent. J Biol Chem 1998; 273: 27934-8.
26. Andrade F, Roy S, Nicholson D, et al. Granzyme B directly and efficiently cleaves several downstream caspase substrates: implications for CTL-induced apoptosis. Immunity 1998; 8: 451-60.
27. Ray M, Hostetter DR, Loeb CR, et al. Inhibition of Granzyme B by PI-9 protects prostate cancer cells from apoptosis. Prostate, in press.
28. Rousalova I, Krepela E, Prochazka J, et al. Expression of proteinase inhibitor-9/serpinB9 in non-small cell lung carcinoma cells and tissues. Int J Oncol 2010; 36: 275-83.
29. ten Berge RL, Meijer CJ, Dukers DF, et al. Expression levels of apoptosis-related proteins predict clinical outcome in anaplastic large cell lymphoma. Blood 2002; 99: 4540-6.
30. Bladergroen BA, Meijer CJ, ten Berge RL, et al. Expression of the granzyme B inhibitor, protease inhibitor 9, by tumor cells in patients with non-Hodgkin and Hodgkin lymphoma: a novel protective mechanism for tumor cells to circumvent the immune system? Blood 2002; 99: 232-7.
31. Losasso V, Schiffer S, Barth S, et al. Design of human granzyme B variants resistant to serpin B9. Proteins 2012; 80: 2514-22.
32. Stahnke B, Thepen T, Stocker M, et al. Granzyme B-H22(scFv), a human immunotoxin targeting CD64 in acute myeloid leukemia of monocytic subtypes. Mol Cancer Ther 2008; 7: 2924-32.
33. van de Winkel JG, Anderson CL,. Biology of human immunoglobulin G Fc receptors. J Leukoc Biol 1991; 49: 511-24.
34. Tur MK, Huhn M, Thepen T, et al. Recombinant CD64-specific single chain immunotoxin exhibits specific cytotoxicity against acute myeloid leukemia cells. Cancer Res 2003; 63: 8414-9.
35. Kampmeier F, Niesen J, Koers A, et al. Rapid optical imaging of EGF receptor expression with a single-chain antibody SNAP-tag fusion protein. Eur J Nucl Med Mol Imaging 2010; 37: 1926-34.
36. Hetzel C, Bachran C, Fischer R, et al. Small cleavable adapters enhance the specific cytotoxicity of a humanized immunotoxin directed against CD64-positive cells. J Immunother 2008; 31: 370-6.
37. Schiffer S, Letzian S, Jost E, et al. Granzyme M as a novel effector molecule for human cytolytic fusion proteins: CD64-specific cytotxicity of Gm-H22(scFv) against leukemic cells. Cancer Lett. 2013; 341: 178-85.
38. Silverman GA, Bird PI, Carrell RW, et al. The serpins are an expanding superfamily of structurally similar but functionally diverse proteins. Evolution, mechanism of inhibition, novel functions, and a revised nomenclature. J Biol Chem 2001; 276: 33293-6.
39. Schiffer S, Hansen H, Hehmann-Titt G, et al. Efficacy of an adapted Granzyme B-based anti-CD30 cytolytic fusion protein against PI-9-positive classical Hodgkin lymphoma cells in a murine model. Blood Cancer J 2013; 3: e106.
40. Thepen T, Huhn M, Melmer G, et al. Fcgamma receptor 1 (CD64), a target beyond cancer. Curr Pharm Des 2009; 15: 2712-8.
41. ten Cate B, Bremer E, de Bruyn M, et al. A novel AML-selective TRAIL fusion protein that is superior to Gemtuzumab Ozogamicin in terms of in vitro selectivity, activity and stability. Leukemia 2009; 23: 1389-97.
42. Schwemmlein M, Peipp M, Barbin K, et al. A CD33-specific single-chain immunotoxin mediates potent apoptosis of cultured human myeloid leukaemia cells. Br J Haematol 2006; 133: 141-51.
43. Zhong RK, van de Winkel JG, Thepen T, et al. Cytotoxicity of anti-CD64-ricin a chain immunotoxin against human acute myeloid leukemia cells in vitro and in SCID mice. J Hematother Stem Cell Res 2001; 10: 95-105.
44. Santos IM, Franzon CM, Koga AH,. Laboratory diagnosis of chronic myelomonocytic leukemia and progression to acute leukemia in association with chronic lymphocytic leukemia: morphological features and immunophenotypic profile. Rev Bras Hematol Hemoter 2012; 34: 242-4.
45. Nordigarden A, Zetterblad J, Trinks C, et al. Irreversible pan-ERBB inhibitor canertinib elicits anti-leukaemic effects and induces the regression of FLT3-ITD transformed cells in mice. Br J Haematol 2011; 155: 198-208.
46. Krauter J, Wagner K, Schafer I, et al. Prognostic factors in adult patients up to 60 years old with acute myeloid leukemia and translocations of chromosome band 11q23: individual patient data-based meta-analysis of the German Acute Myeloid Leukemia Intergroup. J Clin Oncol 2009; 27: 3000-6.
47. Tur MK, Huhn M, Jost E, et al. In vivo efficacy of the recombinant anti-CD64 immunotoxin H22(scFv)-ETA' in a human acute myeloid leukemia xenograft tumor model. Int J Cancer 2011; 129: 1277-82.
48. Jedema I, Barge RM, Frankel AE, et al. Acute myeloid leukemia cells in G0 phase of the cell cycle that are unresponsive to conventional chemotherapy are sensitive to treatment with granulocyte-macrophage colony-stimulating factor/diphtheria toxin fusion proteins. Exp Hematol 2004; 32: 188-94.
49. Wei H, Bera TK, Wayne AS, et al. A modified form of diphthamide causes immunotoxin resistance in a lymphoma cell line with a deletion of the WDR85 gene. J Biol Chem 2013; 288: 12305-12.
50. Classen CF, Bird PI, Debatin KM,. Modulation of the granzyme B inhibitor proteinase inhibitor 9 (PI-9) by activation of lymphocytes and monocytes in vitro and by Epstein-Barr virus and bacterial infection. Clin Exp Immunol 2006; 143: 534-42.
51. Graziano RF, Tempest PR, White P, et al. Construction and characterization of a humanized anti-gamma-Ig receptor type I (Fc gamma RI) monoclonal antibody. J Immunol 1995; 155: 4996-5002.