CD52 is a molecular target in advanced systemic mastocytosis

FASEB Journal

Volumn 28, Issue 8, 2014, Pages 3540-3551

  Hoermann, Gregor ^a   Blatt, Katharina ^a   Greiner, Georg ^a   Putz, Eva Maria ^b   Berger, Angelika ^b   Herrmann, Harald ^c   Cerny Reiterer, Sabine ^a,c   Gleixner, Karoline V ^a   Walz, Christoph ^d   Hoetzenecker, Konrad ^a   Müllauer, Leonhard ^a   Reiter, Andreas ^e   Sotlar, Karl ^d   Sexl, Veronika ^b   Valent, Peter ^a,c   Mayerhofer, Matthias ^f  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^c LUDWIG BOLTZMANN INSTITUTE FOR LUNG VASCULAR RESEARCH   (Austria)

^d UNIVERSITY OF MUNICH   (Germany)

^e UNIVERSITY OF HEIDELBERG   (Germany)

^f HANUSCH HOSPITAL   (Austria)

Author keywords

Alemtuzumab; CAMPATH 1; Mast cell leukemia; RAS G12V

Indexed keywords

ALEMTUZUMAB; CD52 ANTIGEN; LENTIVIRUS VECTOR;

ADULT; AGED; ARTICLE; CANCER CELL LINE; CELL DEATH; CELL IMMORTALIZATION; CELL SURVIVAL; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MOLECULARLY TARGETED THERAPY; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL; SYSTEMIC MASTOCYTOSIS; UMBILICAL CORD BLOOD; XENOTRANSPLANTATION;

ALEMTUZUMAB; CAMPATH-1; MAST CELL LEUKEMIA; RAS G12V;

ADULT; AGED; ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIGENS, CD; ANTIGENS, NEOPLASM; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CELLS, CULTURED; FEMALE; FETAL BLOOD; GENES, RAS; GLYCOPROTEINS; GTP PHOSPHOHYDROLASES; HUMANS; MALE; MAP KINASE SIGNALING SYSTEM; MAST CELLS; MASTOCYTOSIS, SYSTEMIC; MEMBRANE PROTEINS; MICE; MICE, INBRED NOD; MICE, SCID; MIDDLE AGED; MOLECULAR TARGETED THERAPY; MUTATION, MISSENSE; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-KIT; RAS PROTEINS; TRANSDUCTION, GENETIC; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84905233373     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-250894     Document Type: Article

References (55)

1. Akin, C., and Metcalfe, D. D. (2004) Systemic mastocytosis. Annu. Rev. Med. 55, 419-432 (Pubitemid 38316735)
2. Arock, M., and Valent, P. (2010) Pathogenesis, classification and treatment of mastocytosis: state of the art in 2010 and future perspectives. Expert Rev. Hematol. 3, 497-516
3. Horny, H. P., Metcalfe, D. D., Bennett, J. M., B.J., B., Akin, C., Escribano, L., and Valent, P. (2008) Mastocytosis. In WHO Classification of Tumours of Haematopoietic and Lymphoid Tissues (Swerdlow, S., Campo, E., Harris, N., Jaffe, E., Stefano, A., Stein, H., Thiele, J., and Vardiman, J., eds) pp. 54-63, International Agency for Research on Cancer (IARC), Lyon, France
4. Valent, P., Akin, C., Sperr, W. R., Escribano, L., Arock, M., Horny, H. P., Bennett, J. M., and Metcalfe, D. D. (2003) Aggressive systemic mastocytosis and related mast cell disorders: current treatment options and proposed response criteria. Leukemia Res. 27, 635-641 (Pubitemid 36398099)
5. Georgin-Lavialle, S., Lhermitte, L., Dubreuil, P., Chandesris, M. O., Hermine, O., and Damaj, G. (2013) Mast cell leukemia. Blood 121, 1285-1295
6. Valent, P., Ghannadan, M., Akin, C., Krauth, M. T., Selzer, E., Mayerhofer, M., Sperr, W. R., Arock, M., Samorapoompichit, P., Horny, H. P., and Metcalfe, D. D. (2004) On the way to targeted therapy of mast cell neoplasms: identification of molecular targets in neoplastic mast cells and evaluation of arising treatment concepts. Eur. J. Clin. Invest. 34(Suppl. 2), 41-52 (Pubitemid 39331488)
7. Nagata, H., Worobec, A. S., Oh, C. K., Chowdhury, B. A., Tannenbaum, S., Suzuki, Y., and Metcalfe, D. D. (1995) Identification of a point mutation in the catalytic domain of the protooncogene c-kit in peripheral blood mononuclear cells of patients who have mastocytosis with an associated hematologic disorder. Proc. Natl. Acad. Sci. U. S. A. 92, 10560-10564
8. Longley, B. J., Jr., Metcalfe, D. D., Tharp, M., Wang, X., Tyrrell, L., Lu, S. Z., Heitjan, D., and Ma, Y. (1999) Activating and dominant inactivating c-KIT catalytic domain mutations in distinct clinical forms of human mastocytosis. Proc. Natl. Acad. Sci. U. S. A. 96, 1609-1614 (Pubitemid 29098499)
9. Longley, B. J., Tyrrell, L., Lu, S. Z., Ma, Y. S., Langley, K., Ding, T. G., Duffy, T., Jacobs, P., Tang, L. H., and Modlin, I. (1996) Somatic c-KIT activating mutation in urticaria pigmentosa and aggressive mastocytosis: establishment of clonality in a human mast cell neoplasm. Nat. Genetics 12, 312-314 (Pubitemid 26080092)
10. Fritsche-Polanz, R., Jordan, J. H., Feix, A., Sperr, W. R., Sunder- Plassmann, G., Valent, P., and Fodinger, M. (2001) Mutation analysis of C-KIT in patients with myelodysplastic syndromes without mastocytosis and cases of systemic mastocytosis. Br. J. Haematol. 113, 357-364 (Pubitemid 32523138)
11. Feger, F., Ribadeau Dumas, A., Leriche, L., Valent, P., and Arock, M. (2002) Kit and c-kit mutations in mastocytosis: a short overview with special reference to novel molecular and diagnostic concepts. Int. Arch. Allergy Immunol. 127, 110-114 (Pubitemid 34264196)
12. Mayerhofer, M., Gleixner, K. V., Hoelbl, A., Florian, S., Hoermann, G., Aichberger, K. J., Bilban, M., Esterbauer, H., Krauth, M. T., Sperr, W. R., Longley, J. B., Kralovics, R., Moriggl, R., Zappulla, J., Liblau, R. S., Schwarzinger, I., Sexl, V., Sillaber, C., and Valent, P. (2008) Unique effects of KIT D816V in BaF3 cells: induction of cluster formation, histamine synthesis, and early mast cell differentiation antigens. J. Immunol. 180, 5466-5476
13. Schwaab, J., Schnittger, S., Sotlar, K., Walz, C., Fabarius, A., Pfirrmann, M., Kohlmann, A., Grossmann, V., Meggendorfer, M., Horny, H. P., Valent, P., Jawhar, M., Teichmann, M., Metzgeroth, G., Erben, P., Ernst, T., Hochhaus, A., Haferlach, T., Hofmann, W. K., Cross, N. C., and Reiter, A. (2013) Comprehensive mutational profiling in advanced systemic mastocytosis. Blood 122, 2460-2466
14. Wilson, T. M., Maric, I., Simakova, O., Bai, Y., Chan, E. C., Olivares, N., Carter, M., Maric, D., Robyn, J., and Metcalfe, D. D. (2011) Clonal analysis of NRAS activating mutations in KITD816V systemic mastocytosis. Haematologica 96, 459-463
15. Hale, C., Bartholomew, M., Taylor, V., Stables, J., Topley, P., and Tite, J. (1996) Recognition of CD52 allelic gene products by CAMPATH-1H antibodies. Immunology 88, 183-190 (Pubitemid 26189299)
16. Hale, G. (2001) CD52 (CAMPATH1). J. Biol. Regul. Homeost. Agents 15, 386-391
17. Osterborg, A., Dyer, M. J., Bunjes, D., Pangalis, G. A., Bastion, Y., Catovsky, D., and Mellstedt, H. (1997) Phase II multicenter study of human CD52 antibody in previously treated chronic lymphocytic leukemia. European Study Group of CAM-PATH-1H Treatment in Chronic Lymphocytic Leukemia. J. Clin. Oncol. 15, 1567-1574 (Pubitemid 27167394)
18. Osterborg, A., Fassas, A. S., Anagnostopoulos, A., Dyer, M. J., Catovsky, D., and Mellstedt, H. (1996) Humanized CD52 monoclonal antibody Campath-1H as first-line treatment in chronic lymphocytic leukaemia. Br. J. Haematol. 93, 151-153 (Pubitemid 26132394)
19. Coles, A. J., Compston, D. A., Selmaj, K. W., Lake, S. L., Moran, S., Margolin, D. H., Norris, K., and Tandon, P. K. (2008) Alemtuzumab vs. interferon beta-1a in early multiple sclerosis. N. Engl. J. Med. 359, 1786-1801
20. Matteson, E. L., Yocum, D. E., St Clair, E. W., Achkar, A. A., Thakor, M. S., Jacobs, M. R., Hays, A. E., Heitman, C. K., and Johnston, J. M. (1995) Treatment of active refractory rheumatoid arthritis with humanized monoclonal antibody CAM-PATH-1H administered by daily subcutaneous injection. Arthritis Rheum. 38, 1187-1193
21. Hu, Y., Turner, M. J., Shields, J., Gale, M. S., Hutto, E., Roberts, B. L., Siders, W. M., and Kaplan, J. M. (2009) Investigation of the mechanism of action of alemtuzumab in a human CD52 transgenic mouse model. Immunology 128, 260-270
22. Rao, S. P., Sancho, J., Campos-Rivera, J., Boutin, P. M., Severy, P. B., Weeden, T., Shankara, S., Roberts, B. L., and Kaplan, J. M. (2012) Human peripheral blood mononuclear cells exhibit heterogeneous CD52 expression levels and show differential sensitivity to alemtuzumab mediated cytolysis. PLoS One 7, e39416
23. Hoermann, G., Cerny-Reiterer, S., Perne, A., Klauser, M., Hoetzenecker, K., Klein, K., Mullauer, L., Groger, M., Nijman, S. M., Klepetko, W., Valent, P., and Mayerhofer, M. (2011) Identification of oncostatin M as a STAT5-dependent mediator of bone marrow remodeling in KIT D816V-positive systemic mastocytosis. Am. J. Pathol. 178, 2344-2356
24. Valent, P., Ashman, L. K., Hinterberger, W., Eckersberger, F., Majdic, O., Lechner, K., and Bettelheim, P. (1989) Mast cell typing: demonstration of a distinct hematopoietic cell type and evidence for immunophenotypic relationship to mononuclear phagocytes. Blood 73, 1778-1785 (Pubitemid 19145106)
25. Malbec, O., Roget, K., Schiffer, C., Iannascoli, B., Dumas, A. R., Arock, M., and Daeron, M. (2007) Peritoneal cell-derived mast cells: an in vitro model of mature serosal-type mouse mast cells. J. Immunol. 178, 6465-6475 (Pubitemid 46717430)
26. Butterfield, J. H., Weiler, D., Dewald, G., and Gleich, G. J. (1988) Establishment of an immature mast cell line from a patient with mast cell leukemia. Leukemia Res. 12, 345-355
27. Hoermann, G., Cerny-Reiterer, S., Herrmann, H., Blatt, K., Bilban, M., Gisslinger, H., Gisslinger, B., Mullauer, L., Kralovics, R., Mannhalter, C., Valent, P., and Mayerhofer, M. (2012) Identification of oncostatin M as a JAK2 V617F-dependent amplifier of cytokine production and bone marrow remodeling in myeloproliferative neoplasms. FASEB J. 26, 894-906
28. Salmon, P., Oberholzer, J., Occhiodoro, T., Morel, P., Lou, J., and Trono, D. (2000) Reversible immortalization of human primary cells by lentivector-mediated transfer of specific genes. Mol. Ther. 2, 404-414
29. Elad-Sfadia, G., Haklai, R., Ballan, E., Gabius, H. J., and Kloog, Y. (2002) Galectin-1 augments Ras activation and diverts Ras signals to Raf-1 at the expense of phosphoinositide 3-kinase. J. Biol. Chem. 277, 37169-37175
30. Kondo, R., Gleixner, K. V., Mayerhofer, M., Vales, A., Gruze, A., Samorapoompichit, P., Greish, K., Krauth, M. T., Aichberger, K. J., Pickl, W. F., Esterbauer, H., Sillaber, C., Maeda, H., and Valent, P. (2007) Identification of heat shock protein 32 (Hsp32) as a novel survival factor and therapeutic target in neoplastic mast cells. Blood 110, 661-669 (Pubitemid 47105405)
31. Wiznerowicz, M., and Trono, D. (2003) Conditional suppression of cellular genes: lentivirus vector-mediated drug-inducible RNA interference. J. Virol. 77, 8957-8961 (Pubitemid 36936105)
32. Szulc, J., Wiznerowicz, M., Sauvain, M. O., Trono, D., and Aebischer, P. (2006) A versatile tool for conditional gene expression and knockdown. Nat. Methods 3, 109-116 (Pubitemid 43173309)
33. Fiordalisi, J. J., Johnson, R. L., 2nd, Ulku, A. S., Der, C. J., and Cox, A. D. (2001) Mammalian expression vectors for Ras family proteins: generation and use of expression constructs to analyze Ras family function. Methods Enzymol. 332, 3-36 (Pubitemid 32275369)
34. Khosravi-Far, R., White, M. A., Westwick, J. K., Solski, P. A., Chrzanowska-Wodnicka, M., Van Aelst, L., Wigler, M. H., and Der, C. J. (1996) Oncogenic Ras activation of Raf/mitogen-activated protein kinase-independent pathways is sufficient to cause tumorigenic transformation. Mol. Cell. Biol. 16, 3923-3933
35. Rangarajan, A., Hong, S. J., Gifford, A., and Weinberg, R. A. (2004) Species- and cell type-specific requirements for cellular transformation. Cancer Cell 6, 171-183 (Pubitemid 39485689)
36. Rodriguez-Viciana, P., Warne, P. H., Khwaja, A., Marte, B. M., Pappin, D., Das, P., Waterfield, M. D., Ridley, A., and Downward, J. (1997) Role of phosphoinositide 3-OH kinase in cell transformation and control of the actin cytoskeleton by Ras. Cell 89, 457-467 (Pubitemid 27220890)
37. Beillard, E., Pallisgaard, N., van der Velden, V. H., Bi, W., Dee, R., van der Schoot, E., Delabesse, E., Macintyre, E., Gottardi, E., Saglio, G., Watzinger, F., Lion, T., van Dongen, J. J., Hokland, P., and Gabert, J. (2003) Evaluation of candidate control genes for diagnosis and residual disease detection in leukemic patients using 'real-time' quantitative reverse-transcriptase polymerase chain reaction (RQ-PCR) - a Europe against cancer program. Leukemia 17, 2474-2486 (Pubitemid 38072587)
38. Akin, C., Brockow, K., D'Ambrosio, C., Kirshenbaum, A. S., Ma, Y., Longley, B. J., and Metcalfe, D. D. (2003) Effects of tyrosine kinase inhibitor STI571 on human mast cells bearing wild-type or mutated c-kit. Exp. Hematol. 31, 686-692 (Pubitemid 36945381)
39. Hahn, W. C., Counter, C. M., Lundberg, A. S., Beijersbergen, R. L., Brooks, M. W., and Weinberg, R. A. (1999) Creation of human tumour cells with defined genetic elements. Nature 400, 464-468 (Pubitemid 29361801)
40. Zhang, P. L., Pennington, J. R., Prichard, J. W., Blasick, T. M., Brown, A. M., and Potdar, S. (2007) CD52 antigen may be a therapeutic target for eosinophilic rhinosinusitis. Ann. Clin. Lab. Sci. 37, 148-151
41. Santos, D. D., Hatjiharissi, E., Tournilhac, O., Chemaly, M. Z., Leleu, X., Xu, L., Patterson, C., Branagan, A. R., Manning, R. J., Ho, A. W., Hunter, Z. R., Dimmock, E. A., Kutok, J. L., Churchill, W. H., Castells, M. C., Tai, Y. T., Anderson, K. C., and Treon, S. P. (2006) CD52 is expressed on human mast cells and is a potential therapeutic target in Waldenstrom's macroglobulinemia and mast cell disorders. Clin. Lymphoma Myeloma 6, 478-483 (Pubitemid 44043538)
42. Teodosio, C., Garcia-Montero, A. C., Jara-Acevedo, M., Sanchez-Munoz, L., Pedreira, C. E., Alvarez-Twose, I., Matarraz, S., Morgado, J. M., Barcena, P., Matito, A., Mayado, A., Sanchez, M. L., Diez-Campelo, M., Escribano, L., and Orfao, A. (2013) Gene expression profile of highly purified bone marrow mast cells in systemic mastocytosis. J. Allergy Clin. Immunol. 131, 1213-1224, 1224 e1211-1214
43. Sobering, A. K., Watanabe, R., Romeo, M. J., Yan, B. C., Specht, C. A., Orlean, P., Riezman, H., and Levin, D. E. (2004) Yeast Ras regulates the complex that catalyzes the first step in GPI-anchor biosynthesis at the ER. Cell 117, 637-648 (Pubitemid 38692529)
44. Saito, Y., Nakahata, S., Yamakawa, N., Kaneda, K., Ichihara, E., Suekane, A., and Morishita, K. (2011) CD52 as a molecular target for immunotherapy to treat acute myeloid leukemia with high EVI1 expression. Leukemia 25, 921-931
45. Gao, J. S., Zhang, Y., Tang, X., Tucker, L. D., Tarwater, P. M., Quesenberry, P. J., Rigoutsos, I., and Ramratnam, B. (2011) The evi1, microRNA-143, K-Ras axis in colon cancer. FEBS Lett. 585, 693-699
46. Kitayama, H., Kanakura, Y., Furitsu, T., Tsujimura, T., Oritani, K., Ikeda, H., Sugahara, H., Mitsui, H., Kanayama, Y., Kitamura, Y., and Matsuzawa, Y. (1995) Constitutively activating mutations of c-kit receptor tyrosine kinase confer factor-independent growth and tumorigenicity of factor-dependent hematopoietic cell lines. Blood 85, 790-798
47. Piao, X., Paulson, R., van der Geer, P., Pawson, T., and Bernstein, A. (1996) Oncogenic mutation in the Kit receptor tyrosine kinase alters substrate specificity and induces degradation of the protein tyrosine phosphatase SHP-1. Proc. Natl. Acad. Sci. U. S. A. 93, 14665-14669
48. Tsujimura, T., Hashimoto, K., Kitayama, H., Ikeda, H., Sugahara, H., Matsumura, I., Kaisho, T., Terada, N., Kitamura, Y., and Kanakura, Y. (1999) Activating mutation in the catalytic domain of c-kit elicits hematopoietic transformation by receptor self-association not at the ligand-induced dimerization site. Blood 93, 1319-1329 (Pubitemid 29076147)
49. Zappulla, J. P., Dubreuil, P., Desbois, S., Letard, S., Hamouda, N. B., Daeron, M., Delsol, G., Arock, M., and Liblau, R. S. (2005) Mastocytosis in mice expressing human Kit receptor with the activating Asp816Val mutation. J. Exp. Med. 202, 1635-1641 (Pubitemid 41815869)
50. Hanssens, K., Brenet, F., Agopian, J., Georgin-Lavialle, S., Damaj, G., Cabaret, L., Chandesris, M. O., de Sepulveda, P., Hermine, O., Dubreuil, P., and Soucie, E. (2014) SRSF2-P95 hotspot mutation is highly associated with advanced forms of mastocytosis and mutations in epigenetic regulator genes. [E-pub ahead of print] Haematologica 10.3324/haematol.2013.095133
51. Siders, W. M., Shields, J., Garron, C., Hu, Y., Boutin, P., Shankara, S., Weber, W., Roberts, B., and Kaplan, J. M. (2010) Involvement of neutrophils and natural killer cells in the anti-tumor activity of alemtuzumab in xenograft tumor models. Leukemia Lymphoma 51, 1293-1304
52. Golay, J., Manganini, M., Rambaldi, A., and Introna, M. (2004) Effect of alemtuzumab on neoplastic B cells. Haematologica 89, 1476-1483
53. Zent, C. S., Secreto, C. R., LaPlant, B. R., Bone, N. D., Call, T. G., Shanafelt, T. D., Jelinek, D. F., Tschumper, R. C., and Kay, N. E. (2008) Direct and complement dependent cytotoxicity in CLL cells from patients with high-risk early-intermediate stage chronic lymphocytic leukemia (CLL) treated with alemtuzumab and rituximab. Leukemia Res. 32, 1849-1856
54. Mone, A. P., Cheney, C., Banks, A. L., Tridandapani, S., Mehter, N., Guster, S., Lin, T., Eisenbeis, C. F., Young, D. C., and Byrd, J. C. (2006) Alemtuzumab induces caspase-independent cell death in human chronic lymphocytic leukemia cells through a lipid raft-dependent mechanism. Leukemia 20, 272-279 (Pubitemid 43148665)
55. Stanglmaier, M., Reis, S., and Hallek, M. (2004) Rituximab and alemtuzumab induce a nonclassic, caspase-independent apoptotic pathway in B-lymphoid cell lines and in chronic lymphocytic leukemia cells. Ann. Hematol. 83, 634-645 (Pubitemid 39317488)