NKp30 isoforms and NKp30 ligands are predictive biomarkers of response to imatinib mesylate in metastatic GIST patients

OncoImmunology

Volumn 6, Issue 1, 2017, Pages

  Rusakiewicz, Sylvie ^a,b,c   Perier, Aurélie ^a,b   Semeraro, Michaela ^a,b,d   Pitt, Jonathan M ^a,b   von Strandmann, Elke Pogge ^e   Reiners, Katrin S ^e   Aspeslagh, Sandrine ^a,b,d   Pipéroglou, Christelle ^f   Vély, Frédéric ^f,g   Ivagnes, Alexandre ^a,b   Jegou, Sarah ^a,b   Halama, Niels ^h,i   Chaigneau, Loic ^j   Validire, Pierre ^k   Christidis, Christos ^k   Perniceni, Thierry ^k   Landi, Bruno ^l   Berger, Anne ^l   Isambert, Nicolas ^m   Domont, Julien ^a,n   Bonvalot, Sylvie ^a,d,n   Terrier, Philippe ^a,d,n   Adam, Julien ^a,d   Coindre, Jean Michel ^o   Emile, Jean François ^p   Poirier Colame, Vichnou ^a,b   Chaba, Kariman ^b,q,r   Rocha, Benedita ^b,s   Caignard, Anne ^b,t   Toubert, Antoine ^b,t   Enot, David ^a,b,d,q   Koch, Joachim ^u   Marabelle, Aurélien ^a,b,d   Lambert, Marion ^v   Zucman, Sophie Caillat ^v   Leyvraz, Serge ^w   Auclair, Christian ^x   Vivier, Eric ^g,y   Eggermont, Alexander ^a   Borg, Christophe ^z   Blay, Jean Yves ^aa   Cesne, Axel Le ^a,n   Mir, Olivier ^a,n   Zitvogela, Laurence ^a,b,c,ab   more..

^a INSTITUT GUSTAVE ROUSSY   (France)

^b INSERM   (France)

^c Center of Clinical Investigations in Biotherapies of Cancer   (France)

^d GRCC   (France)

^e UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

^f HÔPITAL DE LA CONCEPTION   (France)

^g CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^h UNIVERSITY OF HEIDELBERG   (Germany)

ⁱ UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^j UNIVERSITY HOSPITAL JEAN MINJOZ   (France)

^k INSTITUT MUTUALISTE MONTSOURIS   (France)

^l HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^m CENTRE GEORGES FRANÇOIS LECLERC   (France)

ⁿ University of Paris Descartes ^*  (France)

^o INSTITUT BERGONIÉ   (France)

^p HÔPITAL AMBROISE PARÉ   (France)

^q CENTRE DE RECHERCHE DES CORDELIERS   (France)

^r UNIVERSITÉ PARIS DESCARTES   (France)

^s Institut de Virologie   (France)

^t Saint Louis Lariboisière University Hospitals   (France)

^u UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^v HÔPITAL ROBERT DEBRÉ   (France)

^w LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^x Ecole Normale Superieure de Cachan   (France)

^y AIX MARSEILLE UNIVERSITY   (France)

^z UNIVERSITÉ DE FRANCHE COMTÉ   (France)

^aa UNIVERSITÉ LYON 1   (France)

^ab UNIVERSITÉ PARIS SACLAY   (France)

more..

Author keywords

B7 H6; Cancer; GIST; Immunity; NK cells; NKp30 NCR3

Indexed keywords

COLONY STIMULATING FACTOR 1; CUTANEOUS T CELL ATTRACTING CHEMOKINE; GAMMA INTERFERON; GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IMATINIB; INTERLEUKIN 12P40; INTERLEUKIN 17; LYMPHOTOXIN; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3A; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3B; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3C; STROMAL CELL DERIVED FACTOR 1ALPHA; TUMOR MARKER; UNCLASSIFIED DRUG;

ARTICLE; BLOOD SAMPLING; CANCER PATIENT; CANCER PROGNOSIS; CELL PROLIFERATION; CONTROLLED STUDY; DNA TRANSCRIPTION; ENZYME LINKED IMMUNOSORBENT ASSAY; EVENT FREE SURVIVAL; GASTROINTESTINAL STROMAL TUMOR; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; OVERALL SURVIVAL; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PREDICTIVE VALUE; PROSPECTIVE STUDY; PROTEIN EXPRESSION; PROTEIN MICROARRAY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; T LYMPHOCYTE; TREATMENT RESPONSE; TUMOR MICROENVIRONMENT; VISCERAL METASTASIS;

EID: 85020486355     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2015.1137418     Document Type: Article

References (42)

1. Corless CL. Assessing the prognosis of gastrointestinal stromal tumors: a growing role for molecular testing. Am J Clin Pathol 2004; 122:11-3; PMID:15272524; http://dx.doi.org/10.1309/BUVLRQBVGU0N0L42
2. Corless CL, Barnett CM, Heinrich MC. Gastrointestinal stromal tumours: origin and molecular oncology. Nat Rev Cancer 2011; 11:865-78; PMID:22089421; http://dx.doi.org/10.1038/nrc3143
3. Hirota S, Isozaki K, Moriyama Y, Hashimoto K, Nishida T, Ishiguro S, Kawano K, Hanada M, Kurata A, Takeda M et al. Gain-of-function mutations of c-kit in human gastrointestinal stromal tumors. Science 1998; 279:577-80; PMID:9438854; http://dx.doi.org/10.1126/science.279.5350.577
4. Wozniak A, Rutkowski P, Schoffski P, Ray-Coquard I, Hostein I, Schildhaus HU, Le Cesne A, Bylina E, Limon J, Blay JY et al. Tumor genotype is an independent prognostic factor in primary gastrointestinal stromal tumors of gastric origin: a european multicenter analysis based on ConticaGIST. Clin Cancer Res 2014; 20:6105-16; PMID:25294914; http://dx.doi.org/10.1158/1078-0432.CCR-14-1677
5. Demetri GD, von Mehren M, Blanke CD, Van den Abbeele AD, Eisenberg B, Roberts PJ, Heinrich MC, Tuveson DA, Singer S, Janicek M et al. Efficacy and safety of imatinib mesylate in advanced gastrointestinal stromal tumors. N Engl J Med 2002; 347:472-80; PMID:12181401; http://dx.doi.org/10.1056/NEJMoa020461
6. ESMO. Gastrointestinal stromal tumours: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 2014; 25 Suppl 3:iii21-6; PMID:25210085; http://dx.doi.org/10.1093/annonc/mdu255
7. Pierotti MA, Tamborini E, Negri T, Pricl S, Pilotti S. Targeted therapy in GIST: in silico modeling for prediction of resistance. Nat Rev Clin Oncol 2011; 8:161-70; PMID:21364689; http://dx.doi.org/10.1038/nrclinonc.2011.3
8. Borg C, Terme M, Taieb J, Menard C, Flament C, Robert C, Maruyama K, Wakasugi H, Angevin E, Thielemans K et al. Novel mode of action of c-kit tyrosine kinase inhibitors leading to NK cell-dependent antitumor effects. J Clin Invest 2004; 114:379-88; PMID:15286804; http://dx.doi.org/10.1172/JCI21102
9. Menard C, Blay JY, Borg C, Michiels S, Ghiringhelli F, Robert C, Nonn C, Chaput N, Taïeb J, Delahaye NF et al. Natural killer cell IFN-gamma levels predict long-term survival with imatinib mesylate therapy in gastrointestinal stromal tumor-bearing patients. Cancer Res 2009; 69:3563-9; PMID:19351841; http://dx.doi.org/10.1158/0008-5472.CAN-08-3807
10. Delahaye NF, Rusakiewicz S, Martins I, Menard C, Roux S, Lyonnet L, Paul P, Sarabi M, Chaput N, Semeraro M et al. Alternatively spliced NKp30 isoforms affect the prognosis of gastrointestinal stromal tumors. Nat Med 2011; 17:700-7; PMID:21552268; http://dx.doi.org/10.1038/nm.2366
11. Rusakiewicz S, Semeraro M, Sarabi M, Desbois M, Locher C, Mendez R, Vimond N, Concha A, Garrido F, Isambert N et al. Immune infiltrates are prognostic factors in localized gastrointestinal stromal tumors. Cancer Res 2013; 73:3499-510; PMID:23592754; http://dx.doi.org/10.1158/0008-5472.CAN-13-0371
12. Cameron S, Haller F, Dudas J, Moriconi F, Gunawan B, Armbrust T, Langer C, Füzesi L, Ramadori G. Immune cells in primary gastrointestinal stromal tumors. Eur J Gastroenterol Hepatol 2008; 20:327-34; PMID:18334877; http://dx.doi.org/10.1097/MEG.0b013e3282f3a403
13. van Dongen M, Savage ND, Jordanova ES, Briaire-de Bruijn IH, Walburg KV, Ottenhoff TH, Hogendoorn PC, van der Burg SH, Gelderblom H, van Hall T. Anti-inflammatory M2 type macrophages characterize metastasized and tyrosine kinase inhibitor-treated gastrointestinal stromal tumors. Int J Cancer 2010; 127:899-909; PMID:20013807; http://dx.doi.org/10.1002/ijc.25113
14. Balachandran VP, Cavnar MJ, Zeng S, Bamboat ZM, Ocuin LM, Obaid H, Sorenson EC, Popow R, Ariyan C, Rossi F et al. Imatinib potentiates antitumor T cell responses in gastrointestinal stromal tumor through the inhibition of Ido. Nat Med 2011; 17:1094-100; PMID:21873989; http://dx.doi.org/10.1038/nm.2438
15. Reiners KS, Topolar D, Henke A, Simhadri VR, Kessler J, Sauer M, Bessler M, Hansen HP, Tawadros S, Herling M et al. Soluble ligands for NK cell receptors promote evasion of chronic lymphocytic leukemia cells from NK cell anti-tumor activity. Blood 2013; 121:3658-65; PMID:23509156; http://dx.doi.org/10.1182/blood-2013-01-476606
16. Baumgartner JM, Palmer BE, Banerjee A, McCarter MD. Role of Melanoma Secreted Thrombospondin-1 on Induction of Immunosuppressive Regulatory T Cells through CD47. J Cancer Mol 2008; 4:145-52
17. Lee HJ, Yeon JE, Suh SJ, Lee SJ, Yoon EL, Kang K, Yoo YJ, Kim JH, Seo YS, Yim HJ et al. Clinical utility of plasma glypican-3 and osteopontin as biomarkers of hepatocellular carcinoma. Gut Liver 2014; 8:177-85; PMID:24672660; http://dx.doi.org/10.5009/gnl.2014.8.2.177
18. Semeraro M, Rusakiewicz S, Minard-Colin V, Delahaye NF, Enot D, Vely F, Marabelle A, Papoular B, Piperoglou C, Ponzoni M et al. Clinical impact of the NKp30/B7-H6 axis in high-risk neuroblastoma patients. Sci Transl Med 2015; 7:283ra55; PMID:25877893; http://dx.doi.org/10.1126/scitranslmed.aaa2327
19. Schlecker E, Fiegler N, Arnold A, Altevogt P, Rose-John S, Moldenhauer G, Sucker A, Paschen A, von Strandmann EP, Textor S et al. Metalloprotease-mediated tumor cell shedding of B7-H6, the ligand of the natural killer cell-activating receptor NKp30. Cancer Res 2014; 74:3429-40; PMID:24780758; http://dx.doi.org/10.1158/0008-5472.CAN-13-3017
20. Seliger B, Ritz U, Ferrone S. Molecular mechanisms of HLA class I antigen abnormalities following viral infection and transformation. Int J Cancer 2006; 118:129-38; PMID:16003759; http://dx.doi.org/10.1002/ijc.21312
21. Aboud M, Kingsmore S, Segal S. Role of natural killer cells in controlling local tumor formation and metastatic manifestation of different 3LL Lewis lung carcinoma cell clones. Nat Immun 1993; 12:17-24; PMID:8431660
22. Smyth MJ, Thia KY, Street SE, MacGregor D, Godfrey DI, Trapani JA. Perforin-mediated cytotoxicity is critical for surveillance of spontaneous lymphoma. J Exp Med 2000; 192:755-60; PMID:10974040; http://dx.doi.org/10.1084/jem.192.5.755
23. Imai K, Matsuyama S, Miyake S, Suga K, Nakachi K. Natural cytotoxic activity of peripheral-blood lymphocytes and cancer incidence: an 11-year follow-up study of a general population. Lancet 2000; 356:1795-9; PMID:11117911; http://dx.doi.org/10.1016/S0140-6736(00)03231-1
24. Desbois M, Rusakiewicz S, Locher C, Zitvogel L, Chaput N. Natural killer cells in non-hematopoietic malignancies. Front Immunol 2012; 3:395; PMID:23269924; http://dx.doi.org/10.3389/fimmu.2012.00395
25. Sconocchia G, Zlobec I, Lugli A, Calabrese D, Iezzi G, Karamitopoulou E, Patsouris ES, Peros G, Horcic M, Tornillo L et al. Tumor infiltration by FcgammaRIII (CD16)+ myeloid cells is associated with improved survival in patients with colorectal carcinoma. Int J Cancer 2011; 128:2663-72; PMID:20715106; http://dx.doi.org/10.1002/ijc.25609
26. Platonova S, Cherfils-Vicini J, Damotte D, Crozet L, Vieillard V, Validire P, Validire P, André P, Dieu-Nosjean MC, Alifano M et al. Profound coordinated alterations of intratumoral NK cell phenotype and function in lung carcinoma. Cancer Res 2011; 71:5412-22; PMID:21708957; http://dx.doi.org/10.1158/0008-5472.CAN-10-4179
27. Fregni G, Messaoudene M, Fourmentraux-Neves E, Mazouz-Dorval S, Chanal J, Maubec E, Marinho E, Scheer-Senyarich I, Cremer I, Avril MF et al. Phenotypic and functional characteristics of blood natural killer cells from melanoma patients at different clinical stages. PLoS One 2013; 8:e76928; PMID:24204708; http://dx.doi.org/10.1371/journal.pone.0076928
28. Mamessier E, Sylvain A, Thibult ML, Houvenaeghel G, Jacquemier J, Castellano R, Gonçalves A, André P, Romagné F, Thibault G et al. Human breast cancer cells enhance self tolerance by promoting evasion from NK cell antitumor immunity. J Clin Invest 2011; 121:3609-22; PMID:21841316; http://dx.doi.org/10.1172/JCI45816
29. Carrega P, Morandi B, Costa R, Frumento G, Forte G, Altavilla G, Ratto GB, Mingari MC, Moretta L, Ferlazzo G. Natural killer cells infiltrating human nonsmall-cell lung cancer are enriched in CD56 bright CD16(−) cells and display an impaired capability to kill tumor cells. Cancer 2008; 112:863-75; PMID:18203207; http://dx.doi.org/10.1002/cncr.23239
30. Gannon PO, Poisson AO, Delvoye N, Lapointe R, Mes-Masson AM, Saad F. Characterization of the intra-prostatic immune cell infiltration in androgen-deprived prostate cancer patients. J Immunol Methods 2009; 348:9-17; PMID:19552894; http://dx.doi.org/10.1016/j.jim.2009.06.004
31. Marechal R, De Schutter J, Nagy N, Demetter P, Lemmers A, Deviere J, Salmon I, Tejpar S, Van Laethem JL. Putative contribution of CD56 positive cells in cetuximab treatment efficacy in first-line metastatic colorectal cancer patients. BMC Cancer 2010; 10:340; PMID:20591136; http://dx.doi.org/10.1186/1471-2407-10-340
32. Jin S, Deng Y, Hao JW, Li Y, Liu B, Yu Y, Shi FD, Zhou QH. NK cell phenotypic modulation in lung cancer environment. PLoS One 2014; 9:e109976; PMID:25299645; http://dx.doi.org/10.1371/journal.pone.0109976
33. Remark R, Alifano M, Cremer I, Lupo A, Dieu-Nosjean MC, Riquet M, Crozet L, Ouakrim H, Goc J, Cazes A et al. Characteristics and clinical impacts of the immune environments in colorectal and renal cell carcinoma lung metastases: influence of tumor origin. Clin Cancer Res 2013; 19:4079-91; PMID:23785047; http://dx.doi.org/10.1158/1078-0432.CCR-12-3847
34. Ruggeri L, Capanni M, Urbani E, Perruccio K, Shlomchik WD, Tosti A, Posati S, Rogaia D, Frassoni F, Aversa F et al. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 2002; 295:2097-100; PMID:11896281; http://dx.doi.org/10.1126/science.1068440
35. Ferrari de Andrade L, Ngiow SF, Stannard K, Rusakiewicz S, Kalimutho M, Khanna KK, Tey SK, Takeda K, Zitvogel L, Martinet L et al. Natural killer cells are essential for the ability of BRAF inhibitors to control BRAFV600E-mutant metastatic melanoma. Cancer Res 2014; 74:7298-308; PMID:25351955; http://dx.doi.org/10.1158/0008-5472.CAN-14-1339
36. Pogge von Strandmann E, Simhadri VR, von Tresckow B, Sasse S, Reiners KS, Hansen HP, Rothe A, Böll B, Simhadri VL, Borchmann P et al. Human leukocyte antigen-B-associated transcript 3 is released from tumor cells and engages the NKp30 receptor on natural killer cells. Immunity 2007; 27:965-74; PMID:18055229; http://dx.doi.org/10.1016/j.immuni.2007.10.010
37. Reiners KS, Kessler J, Sauer M, Rothe A, Hansen HP, Reusch U, Hucke C, Köhl U, Dürkop H, Engert A et al. Rescue of impaired NK cell activity in hodgkin lymphoma with bispecific antibodies in vitro and in patients. Mol Ther 2013; 21:895-903; PMID:23459515; http://dx.doi.org/10.1038/mt.2013.14
38. Wu MR, Zhang T, Gacerez AT, Coupet TA, DeMars LR, Sentman CL. B7H6-Specific Bispecific T Cell Engagers Lead to Tumor Elimination and Host Antitumor Immunity. J Immunol 2015; 194:5305-11; PMID:25911747; http://dx.doi.org/10.4049/jimmunol.1402517
39. Cavnar MJ, Zeng S, Kim TS, Sorenson EC, Ocuin LM, Balachandran VP, Seifert AM, Greer JB, Popow R, Crawley MH et al. KIT oncogene inhibition drives intratumoral macrophage M2 polarization. J Exp Med 2013; 210:2873-86; PMID:24323358; http://dx.doi.org/10.1084/jem.20130875
40. Chen LL, Chen X, Choi H, Sang H, Chen LC, Zhang H, Gouw L, Andtbacka RH, Chan BK, Rodesch CK et al. Exploiting antitumor immunity to overcome relapse and improve remission duration. Cancer Immunol Immunother 2012; 61:1113-24; PMID:22198309; http://dx.doi.org/10.1007/s00262-011-1185-1
41. Therasse P, Arbuck SG, Eisenhauer EA, Wanders J, Kaplan RS, Rubinstein L, Verweij J, Van Glabbeke M, van Oosterom AT, Christian MC et al. New guidelines to evaluate the response to treatment in solid tumors. European Organization for Research and Treatment of Cancer, National Cancer Institute of the United States, National Cancer Institute of Canada. J Natl Cancer Inst 2000; 92:205-16; PMID:10655437; http://dx.doi.org/10.1093/jnci/92.3.205
42. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods 2001; 25:402-8; PMID:11846609; http://dx.doi.org/10.1006/meth.2001.1262