The ganglioside antigen G D2 is surface-expressed in Ewing sarcoma and allows for MHC-independent immune targeting

British Journal of Cancer

Volumn 106, Issue 6, 2012, Pages 1123-1133

  Kailayangiri, S ^a   Altvater, B ^a   Meltzer, J ^a   Pscherer, S ^a   Luecke, A ^a   Dierkes, C ^b   Titze, U ^b   Leuchte, K ^a   Landmeier, S ^a   Hotfilder, M ^a   Dirksen, U ^a   Hardes, J ^a   Gosheger, G ^a   Juergens, H ^a   Rossig, C ^a  

^a UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^b UNIVERSITY HOSPITAL MÜNSTER   (Germany)

Author keywords

cancer targets; cellular immunotherapy; Ewing sarcoma; GD2; gene transfer

Indexed keywords

CYTOKINE; GANGLIOSIDE GD2;

ADOLESCENT; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CHILD; CLINICAL ARTICLE; CYTOLYSIS; EWING SARCOMA; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SARCOMA CELL; SCHOOL CHILD; T LYMPHOCYTE; TUMOR CELL; TUMOR XENOGRAFT;

ADOLESCENT; ADULT; ANIMALS; ANTIGENS, SURFACE; BONE NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; CHILD; COCULTURE TECHNIQUES; CYTOTOXICITY, IMMUNOLOGIC; FEMALE; GANGLIOSIDES; GRANZYMES; HUMANS; MALE; MICE; MICE, INBRED NOD; MICE, SCID; NEOPLASM TRANSPLANTATION; RECEPTORS, ANTIGEN, T-CELL; RECOMBINANT FUSION PROTEINS; SARCOMA, EWING; SINGLE-CHAIN ANTIBODIES; SPHEROIDS, CELLULAR; T-LYMPHOCYTES; YOUNG ADULT;

EID: 84858290569     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2012.57     Document Type: Article

References (49)

1. Agrawal V, Frankel AE (2010) 14G2a anti-GD2 crossreactivity with the CD166 antigen. J Immunother 33: 1014-1015
2. Ahmed N, Salsman VS, Yvon E, Louis CU, Perlaky L, Wels WS, Dishop MK, Kleinerman EE, Pule M, Rooney CM, Heslop HE, Gottschalk S (2009) Immunotherapy for osteosarcoma: genetic modification of T cells overcomes low levels of tumor antigen expression. Mol Ther 17: 1779-1787
3. Altvater B, Pscherer S, Landmeier S, Niggemeier V, Juergens H, Vormoor J, Rossig C (2006) CD28 co-stimulation via tumour-specific chimaeric receptors induces an incomplete activation response in Epstein-Barr virus-specific effector memory T cells. Clin Exp Immunol 144: 447-457 (Pubitemid 43799928)
4. Berghuis D, de Hooge AS, Santos SJ, Horst D, Wiertz EJ, van Eggermond MC, van den Elsen PJ, Taminiau AH, Ottaviano L, Schaefer KL, Dirksen U, Hooijberg E, Mulder A, Melief CJ, Egeler RM, Schilham MW, Jordanova ES, Hogendoorn PC, Lankester AC (2009) Reduced human leukocyte antigen expression in advanced-stage Ewing sarcoma: implications for immune recognition. J Pathol 218: 222-231
5. Berghuis D, Santos SJ, Baelde HJ, Taminiau AH, Egeler RM, Schilham MW, Hogendoorn PC, Lankester AC (2011) Pro-inflammatory chemokinechemokine receptor interactions within the Ewing sarcoma microenvironment determine CD8 (+) T-lymphocyte infiltration and affect tumour progression. J Pathol 223: 347-357
6. Bollard CM, Gottschalk S, Leen AM, Weiss H, Straathof KC, Carrum G, Khalil M, Wu MF, Huls MH, Chang CC, Gresik MV, Gee AP, Brenner MK, Rooney CM, Heslop HE (2007) Complete responses of relapsed lymphoma following genetic modification of tumor-antigen presenting cells and T-lymphocyte transfer. Blood 110: 2838-2845 (Pubitemid 350006936)
7. Castillero-Trejo Y, Eliazer S, Xiang L, Richardson JA, Ilaria Jr RL (2005) Expression of the EWS/FLI-1 oncogene in murine primary bone-derived cells Results in EWS/FLI-1-dependent, ewing sarcoma-like tumors. Cancer Res 65: 8698-8705 (Pubitemid 41377357)
8. Chang HR, Cordon-Cardo C, Houghton AN, Cheung NK, Brennan MF (1992) Expression of disialogangliosides GD2 and GD3 on human soft tissue sarcomas. Cancer 70: 633-638
9. Cheresh DA, Pierschbacher MD, Herzig MA, Mujoo K (1986) Disialogangliosides GD2 and GD3 are involved in the attachment of human melanoma and neuroblastoma cells to extracellular matrix proteins. J Cell Biol 102: 688-696 (Pubitemid 16021888)
10. Cheung NKV, Neely JE, Landmeier B, Nelson D, Miraldi F (1987) Targeting of Ganglioside-Gd2 Monoclonal-Antibody to Neuroblastoma. J Nucl Med 28: 1577-1583
11. Cho D, Shook DR, Shimasaki N, Chang YH, Fujisaki H, Campana D (2010) Cytotoxicity of activated natural killer cells against pediatric solid tumors. Clin Cancer Res 16: 3901-3909
12. Coiffier B, Thieblemont C, Van Den NE, Lepeu G, Plantier I, Castaigne S, Lefort S, Marit G, Macro M, Sebban C, Belhadj K, Bordessoule D, Ferme C, Tilly H (2010) Long-term outcome of patients in the LNH-98.5 trial, the first randomized study comparing rituximab-CHOP to standard CHOP chemotherapy in DLBCL patients: a study by the Groupe d'Etudes des Lymphomes de l'Adulte. Blood 116: 2040-2045
13. Coles EG, Lawlor ER, Bronner-Fraser M (2008) EWS-FLI1 causes neuroepithelial defects and abrogates emigration of neural crest stem cells. Stem Cells 26: 2237-2244
14. Dudley ME, Wunderlich JR, Robbins PF, Yang JC, Hwu P, Schwartzentruber DJ, Topalian SL, Sherry R, Restifo NP, Hubicki AM, Robinson MR, Raffeld M, Duray P, Seipp CA, Rogers-Freezer L, Morton KE, Mavroukakis SA, White DE, Rosenberg SA (2002) Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 298: 850-854 (Pubitemid 35231542)
15. Heiner JP, Miraldi F, Kallick S, Makley J, Neely J, Smithmensah WH, Cheung NKV (1987) Localization of Gd2-specific monoclonal-antibody 3F8 in human osteosarcoma. Cancer Res 47: 5377-5381 (Pubitemid 17152948)
16. Holmes TD, El Sherbiny YM, Davison A, Clough SL, Blair GE, Cook GP (2011) A human NK cell activation/inhibition threshold allows small changes in the target cell surface phenotype to dramatically alter susceptibility to NK cells. J Immunol 186: 1538-1545
17. Kramer K, Gerald WL, Kushner BH, Larson SM, Hameed M, Cheung NK (1998) Disialoganglioside G (D2) loss following monoclonal antibody therapy is rare in neuroblastoma. Clin Cancer Res 4: 2135-2139 (Pubitemid 28415659)
18. Ladenstein R, Potschger U, Le Deley MC, Whelan J, Paulussen M, Oberlin O, van den BH, Dirksen U, Hjorth L, Michon J, Lewis I, Craft A, Jurgens H (2010) Primary disseminated multifocal Ewing sarcoma: results of the Euro-EWING 99 trial. J Clin Oncol 28: 3284-3291
19. Lawlor ER, Scheel C, Irving J, Sorensen PH (2002) Anchorage-independent multi-cellular spheroids as an in vitro model of growth signaling in Ewing tumors. Oncogene 21: 307-318 (Pubitemid 34102139)
20. Lipinski M, Braham K, Philip I, Wiels J, Philip T, Goridis C, Lenoir GM, Tursz T (1987) Neuroectoderm-associated antigens on Ewing's sarcoma cell lines. Cancer Res 47: 183-187 (Pubitemid 17002120)
21. Louis CU, Savoldo B, Dotti G, Pule M, Yvon E, Myers GD, Rossig C, Russell HV, Diouf O, Liu E, Liu H, Wu MF, Gee AP, Mei Z, Rooney CM, Heslop HE, Brenner MK (2011) Anti-tumor activity and long-term fate of chimeric antigen receptor positive T-cells in patients with neuroblastoma. Blood 118(23): 6050-6056
22. Mackall CL, Rhee EH, Read EJ, Khuu HM, Leitman SF, Bernstein D, Tesso M, Long LM, Grindler D, Merino M, Kopp W, Tsokos M, Berzofsky JA, Helman LJ (2008) A pilot study of consolidative immunotherapy in patients with high-risk pediatric sarcomas. Clin Cancer Res 14: 4850-4858
23. Martinez C, Hofmann TJ, Marino R, Dominici M, Horwitz EM (2007) Human bone marrow mesenchymal stromal cells express the neural ganglioside GD2: a novel surface marker for the identification of MSCs. Blood 109: 4245-4248 (Pubitemid 46743389)
24. Meyer-Wentrup F, Richter G, Burdach S (2005) Identification of an immunogenic EWS-FLI1-derived HLA-DR-restricted T helper cell epitope. Pediatr Hematol Oncol 22: 297-308 (Pubitemid 40770481)
25. Modak S, Gerald W, Cheung NK (2002) Disialoganglioside GD2 and a novel tumor antigen: potential targets for immunotherapy of desmoplastic small round cell tumor. Med Pediatr Oncol 39: 547-551 (Pubitemid 35191435)
26. Morgan RA, Dudley ME, Wunderlich JR, Hughes MS, Yang JC, Sherry RM, Royal RE, Topalian SL, Kammula US, Restifo NP, Zheng ZL, Nahvi A, de Vries CR, Rogers-Freezer LJ, Mavroukakis SA, Rosenberg SA (2006) Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 314: 126-129 (Pubitemid 44547756)
27. Mujoo K, Kipps TJ, Yang HM, Cheresh DA, Wargalla U, Sander DJ, Reisfeld RA (1989) Functional properties and effect on growth suppression of human neuroblastoma tumors by isotype switch variants of monoclonal antiganglioside GD2 antibody 14.18. Cancer Res 49: 2857-2861 (Pubitemid 19148615)
28. Ottaviano L, Schaefer KL, Gajewski M, Huckenbeck W, Baldus S, Rogel U, Mackintosh C, de Alava E, Myklebost O, Kresse SH, Meza-Zepeda LA, Serra M, Cleton-Jansen AM, Hogendoorn PC, Buerger H, Aigner T, Gabbert HE, Poremba C (2010) Molecular characterization of commonly used cell lines for bone tumor research: a trans-European EuroBoNet effort. Genes Chromosomes Cancer 49: 40-51
29. Porter DL, Levine BL, Kalos M, Bagg A, June CH (2011) Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med 365: 725-733
30. Pule MA, Savoldo B, Myers GD, Rossig C, Russell HV, Dotti G, Huls MH, Liu EL, Gee AP, Mei Z, Yvon E, Weiss HL, Liu H, Rooney CM, Heslop HE, Brenner MK (2008) Virus-specific T cells engineered to coexpress tumor-specific receptors: persistence and antitumor activity in individuals with neuroblastoma. Nat Med 14: 1264-1270
31. Rapoport AP, Aqui NA, Stadtmauer EA, Vogl DT, Fang HB, Cai L, Janofsky S, Chew A, Storek J, Akpek G, Badros A, Yanovich S, Tan MT, Veloso E, Pasetti MF, Cross A, Philip S, Murphy H, Bhagat R, Zheng Z, Milliron T, Cotte J, Cannon A, Levine BL, Vonderheide RH, June CH (2011) Combination immunotherapy using adoptive T-cell transfer and tumor antigen vaccination on the basis of hTERT and survivin after ASCT for myeloma. Blood 117: 788-797
32. Riggi N, Cironi L, Provero P, Suva ML, Kaloulis K, Garcia-Echeverria C, Hoffmann F, Trumpp A, Stamenkovic I (2005) Development of Ewing's sarcoma from primary bone marrow-derived mesenchymal progenitor cells. Cancer Res 65: 11459-11468 (Pubitemid 41821703)
33. Rossig C, Bar A, Pscherer S, Altvater B, Pule M, Rooney CM, Brenner MK, Jurgens H, Vormoor J (2006) Target antigen expression on a professional antigen-presenting cell induces superior proliferative antitumor T-cell responses via chimeric T-cell receptors. J Immunother 29: 21-31
34. Rossig C, Bollard CM, Nuchtern JG, Merchant DA, Brenner MK (2001) Targeting of G (D2)-positive tumor cells by human T lymphocytes engineered to express chimeric T-cell receptor genes. Int J Cancer 94: 228-236 (Pubitemid 32911418)
35. Rossig C, Bollard CM, Nuchtern JG, Rooney CM, Brenner MK (2002) Epstein-Barr virus-specific human T lymphocytes expressing antitumor chimeric T-cell receptors: potential for improved immunotherapy. Blood 99: 2009-2016 (Pubitemid 34525482)
36. Schulz G, Cheresh DA, Varki NM, Yu A, Staffileno LK, Reisfeld RA (1984) Detection of ganglioside GD2 in tumor tissues and sera of neuroblastoma patients. Cancer Res 44: 5914-5920 (Pubitemid 15183611)
37. Shusterman S, London WB, Gillies SD, Hank JA, Voss SD, Seeger RC, Reynolds CP, Kimball J, Albertini MR, Wagner B, Gan J, Eickhoff J, DeSantes KB, Cohn SL, Hecht T, Gadbaw B, Reisfeld RA, Maris JM, Sondel PM (2010) Antitumor activity of hu14.18-IL2 in patients with relapsed/refractory neuroblastoma: a Children's Oncology Group (COG) phase II study. J Clin Oncol 28: 4969-4975
38. Sorkin LS, Otto M, Baldwin III WM, Vail E, Gillies SD, Handgretinger R, Barfield RC, Ming YH, Yu AL (2010) Anti-GD (2) with an FC point mutation reduces complement fixation and decreases antibody-induced allodynia. Pain 149: 135-142
39. Suzuki Y, Yanagisawa M, Ariga T, Yu RK (2011) Histone acetylationmediated glycosyltransferase gene regulation in mouse brain during development. J Neurochem 116: 874-880
40. Takashima Y, Era T, Nakao K, Kondo S, Kasuga M, Smith AG, Nishikawa S (2007) Neuroepithelial cells supply an initial transient wave of MSC differentiation. Cell 129: 1377-1388 (Pubitemid 46970707)
41. Tirode F, Laud-Duval K, Prieur A, Delorme B, Charbord P, Delattre O (2007) Mesenchymal stem cell features of Ewing tumors. Cancer Cell 11: 421-429 (Pubitemid 46680428)
42. Tsuchida T, Saxton RE, Morton DL, Irie RF (1989) Gangliosides of human melanoma. Cancer 63: 1166-1174 (Pubitemid 19074749)
43. Verhoeven DH, de Hooge AS, Mooiman EC, Santos SJ, ten Dam MM, Gelderblom H, Melief CJ, Hogendoorn PC, Egeler RM, van Tol MJ, Schilham MW, Lankester AC (2008) NK cells recognize and lyse Ewing sarcoma cells through NKG2D and DNAM-1 receptor dependent pathways. Mol Immunol 45: 3917-3925
44. Vormoor J, Baersch G, Decker S, Hotfilder M, Schafer KL, Pelken L, Rube C, Van Valen F, Jurgens H, Dockhorn-Dworniczak B (2001) Establishment of an in vivo model for pediatric Ewing tumors by transplantation into NOD/scid mice. Pediatr Res 49: 332-341 (Pubitemid 32205231)
45. Wahl J, Bogatyreva L, Boukamp P, Rojewski M, Van Valen F, Fiedler J, Hipp N, Debatin KM, Beltinger C (2010) Ewing's sarcoma cells with CD57-associated increase of tumorigenicity and with neural crest-like differentiation capacity. Int J Cancer 127: 1295-1307
46. Wierzbicki A, Gil M, Ciesielski M, Fenstermaker RA, Kaneko Y, Rokita H, Lau JT, Kozbor D (2008) Immunization with a mimotope of GD2 ganglioside induces CD8+ T cells that recognize cell adhesion molecules on tumor cells. J Immunol 181: 6644-6653
47. Xu J, Liao W, Gu D, Liang L, Liu M, Du W, Liu P, Zhang L, Lu S, Dong C, Zhou B, Han Z (2009) Neural ganglioside GD2 identifies a subpopulation of mesenchymal stem cells in umbilical cord. Cell Physiol Biochem 23: 415-424
48. Yu AL, Gilman AL, Ozkaynak MF, London WB, Kreissman SG, Chen HX, Smith M, Anderson B, Villablanca JG, Matthay KK, Shimada H, Grupp SA, Seeger R, Reynolds CP, Buxton A, Reisfeld RA, Gillies SD, Cohn SL, Maris JM, Sondel PM (2010) Anti-GD2 antibody with GM-CSF, interleukin-2, and isotretinoin for neuroblastoma. N Engl J Med 363: 1324-1334
49. Yvon E, Del Vecchio M, Savoldo B, Hoyos V, Dutour A, Anichini A, Dotti G, Brenner MK (2009) Immunotherapy of metastatic melanoma using genetically engineered GD2-specific T cells. Clin Cancer Res 15: 5852-5860