PD-L1 expression in metastatic neuroblastoma as an additional mechanism for limiting immune surveillance

OncoImmunology

Volumn 5, Issue 1, 2016, Pages

  Dondero, Alessandra ^a   Pastorino, Fabio ^b   Della Chiesa, Mariella ^a   Corrias, Maria Valeria ^b   Morandi, Fabio ^b   Pistoia, Vito ^b   Olive, Daniel ^c   Bellora, Francesca ^a   Locatelli, Franco ^d   Castellano, Aurora ^d   Moretta, Lorenzo ^b   Moretta, Alessandro ^a   Bottino, Cristina ^a,b   Castriconi, Roberta ^a  

^a UNIVERSITY OF GENOA   (Italy)

^b G GASLINI INSTITUTE   (Italy)

^c AIX MARSEILLE UNIVERSITY   (France)

^d UNIVERSITY OF PAVIA   (Italy)

Author keywords

Anti tumor immunity; Immune checkpoints; INF ; Natural killer cells; Neuroblastoma; PD 1; PD L1; PD L2; T cells; TNF

Indexed keywords

GAMMA INTERFERON; GANGLIOSIDE GD2; HLA ANTIGEN CLASS 1; MONOCLONAL ANTIBODY; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 LIGAND 2; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW BIOPSY; CONTROLLED STUDY; CYTOFLUOROMETRY; CYTOKINE RELEASE; FEMALE; GAMMA DELTA T LYMPHOCYTE; GENE EXPRESSION REGULATION; HIGH RISK PATIENT; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; IMMUNOSURVEILLANCE; METASTASIS; MOUSE; NATURAL KILLER T CELL; NEUROBLASTOMA; NEUROBLASTOMA CELL LINE; NONHUMAN; PROTEIN EXPRESSION; T LYMPHOCYTE ACTIVATION; TUMOR XENOGRAFT;

EID: 84954446803     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2015.1064578     Document Type: Article

References (57)

1. Cohn SL, Pearson AD, London WB, Monclair T, Ambros PF, Brodeur GM, Faldum A, Hero B, Iehara T, Machin D et al. The International Neuroblastoma Risk Group (INRG) classification system: an INRG Task Force report. J Clin Oncol 2009; 27:289-97; PMID:19047291; http://dx. doi. org/10. 1200/JCO. 2008. 16. 6785
2. Park JR, Eggert A, Caron H. Neuroblastoma: biology, prognosis, and treatment. Pediatr Clin North Am 2008; 55:97-120, x; PMID:18242317; http://dx. doi. org/10. 1016/j. pcl. 2007. 10. 014
3. Cheung NK, Dyer MA. Neuroblastoma: developmental biology, cancer genomics and immunotherapy. Nat Rev Cancer 2013; 13:397-411; PMID:23702928; http://dx. doi. org/10. 1038/nrc3526
4. Bottino C, Dondero A, Bellora F, Moretta L, Locatelli F, Pistoia V, Moretta A, Castriconi R. Natural Killer Cells and Neuroblastoma: tumor recognition, escape mechanisms and possible novel immunotherapeutic approaches. Front Immunol 2014; 5:56; PMID:24575100; http://dx. doi. org/10. 3389/fimmu. 2014. 0005
5. Castriconi R, Dondero A, Cilli M, Ognio E, Pezzolo A, De Giovanni B, Gambini C, Pistoia V, Moretta L, Moretta A et al. Human NK cell infusions prolong survival of metastatic human neuroblastoma-bearing NOD/scid mice. Cancer Immunol Immunother 2007; 56:1733-42; PMID:17426969; http://dx. doi. org/10. 1007/s00262-007-0317-0
6. Valteau-Couanet D, Leboulaire C, Maincent K, Tournier M, Hartmann O, Benard J, Beaujean F, Boccaccio C, Zitvogel L, Angevin E. Dendritic cells for NK/LAK activation: rationale for multicellular immunotherapy in neuroblastoma patients. Blood 2002; 100:2554-61; PMID:12239169; http://dx. doi. org/10. 1182/blood. V100. 7. 2554
7. Falco M, Moretta L, Moretta A, Bottino C. KIR and KIR ligand polymorphism: a new area for clinical applications? Tissue Antigens 2013; 82:363-73; PMID:24498992; http://dx. doi. org/10. 1111/tan. 12262
8. Bottino C, Castriconi R, Moretta L, Moretta A. Cellular ligands of activating NK receptors. Trends Immunol 2005; 26:221-6; PMID:15797513; http://dx. doi. org/10. 1016/j. it. 2005. 02. 007
9. Vivier E, Raulet DH, Moretta A, Caligiuri MA, Zitvogel L, Lanier LL, Yokoyama WM, Ugolini S. Innate or adaptive immunity? The example of natural killer cells. Science 2011; 331:44-9; PMID:21212348; http://dx. doi. org/10. 1126/science. 1198687
10. Castriconi R, Dondero A, Corrias MV, Lanino E, Pende D, Moretta L, Bottino C, Moretta A. Natural killer cell-mediated killing of freshly isolated neuroblastoma cells: critical role of DNAX accessory molecule-1-poliovirus receptor interaction. Cancer Res 2004; 64:9180-4; PMID:15604290; http://dx. doi. org/10. 1158/0008-5472. CAN-04-2682
11. Castriconi R, Dondero A, Augugliaro R, Cantoni C, Carnemolla B, Sementa AR, Negri F, Conte R, Corrias MV, Moretta L et al. Identification of 4Ig-B7-H3 as a neuroblastoma-associated molecule that exerts a protective role from an NK cell-mediated lysis. Proc Natl Acad Sci U S A 2004; 101:12640-5; PMID:15314238; http://dx. doi. org/ 10. 1073/pnas. 0405025101
12. Lemke D, Pfenning PN, Sahm F, Klein AC, Kempf T, Warnken U, Schnölzer M, Tudoran R, Weller M, Platten M et al. Costimulatory protein 4IgB7H3 drives the malignant phenotype of glioblastoma by mediating immune escape and invasiveness. Clin Cancer Res 2012; 18:105-17; PMID:22080438; http://dx. doi. org/10. 1158/1078-0432. CCR-11-0880
13. Yuan H, Wei X, Zhang G, Li C, Zhang X, Hou J. B7-H3 over expression in prostate cancer promotes tumor cell progression. J Urol 2011; 186:1093-9; PMID:21784485; http://dx. doi. org/10. 1016/j. juro. 2011. 04. 103
14. Suh WK, Gajewska BU, Okada H, Gronski MA, Bertram EM, Dawicki W, Schnölzer M, Tudoran R, Weller M, Platten M et al. The B7 family member B7-H3 preferentially down-regulates T helper type 1-mediated immune responses. Nat Immunol 2003; 4:899-906; PMID:12925852; http://dx. doi. org/10. 1038/ni967
15. Hu Y, Lv X, Wu Y, Xu J, Wang L, Chen W, Li J, Zhang S, Qiu H. Expression of costimulatory molecule B7-H3 and its prognostic implications in human acute leukemia. Hematology 2014; 20(4):187-95; PMID:25130683; http://dx. doi. org/10. 1179/1607845414Y. 0000000186
16. Roth TJ, Sheinin Y, Lohse CM, Kuntz SM, Frigola X, Inman BA, Krambeck AE, McKenney ME, Karnes RJ, Blute ML et al. B7-H3 ligand expression by prostate cancer: a novel marker of prognosis and potential target for therapy. Cancer Res 2007; 67:7893-900; PMID:17686830; http://dx. doi. org/10. 1158/0008-5472. CAN-07-1068
17. Gregorio A, Corrias MV, Castriconi R, Dondero A, Mosconi M, Gambini C, Moretta A, Moretta L, Bottino C. Small round blue cell tumours: diagnostic and prognostic usefulness of the expression of B7-H3 surface molecule. Histopathology 2008; 53:73-80; PMID:18613926; http://dx. doi. org/10. 1111/j. 1365-2559. 2008. 03070. x
18. Crispen PL, Sheinin Y, Roth TJ, Lohse CM, Kuntz SM, Frigola X, Thompson RH, Boorjian SA, Dong H, Leibovich BC et al. Tumor cell and tumor vasculature expression of B7-H3 predict survival in clear cell renal cell carcinoma. Clin Cancer Res 2008; 14:5150-7; PMID:18694993; http://dx. doi. org/10. 1158/1078-0432. CCR-08-0536
19. Sun TW, Gao Q, Qiu SJ, Zhou J, Wang XY, Yi Y, Shi JY, Xu YF, Shi YH, Song K et al. B7-H3 is expressed in human hepatocellular carcinoma and is associated with tumor aggressiveness and postoperative recurrence. Cancer Immunol Immunother 2012; 61:2171-82; PMID:22729558; http://dx. doi. org/10. 1007/s00262-012-1278-5
20. Zang X, Thompson RH, Al-Ahmadie HA, Serio AM, Reuter VE, Eastham JA, Scardino PT, Sharma P, Allison JP. B7-H3 and B7x are highly expressed in human prostate cancer and associated with disease spread and poor outcome. Proc Natl Acad Sci U S A 2007; 104:19458-63; PMID:18042703; http://dx. doi. org/10. 1073/pnas. 0709802104
21. Wang J, Chong KK, Nakamura Y, Nguyen L, Huang SK, Kuo C, Zhang W, Yu H, Morton DL, Hoon DS. B7-H3 associated with tumor progression and epigenetic regulatory activity in cutaneous melanoma. J Invest Dermatol 2013; 133:2050-8; PMID:23474948; http:// dx. doi. org/10. 1038/jid. 2013. 114
22. Wang L, Zhang Q, Chen W, Shan B, Ding Y, Zhang G, Cao N, Liu L, Zhang Y. B7-H3 is overexpressed in patients suffering osteosarcoma and associated with tumor aggressiveness and metastasis. PloS One 2013; 8:e70689; PMID:23940627; http://dx. doi. org/10. 1371/journal. pone. 0070689
23. Loo D, Alderson RF, Chen FZ, Huang L, Zhang W, Gorlatov S, Burke S, Ciccarone V, Li H, Yang Y et al. Development of an Fc-enhanced anti-B7-H3 monoclonal antibody with potent antitumor activity. Clin Cancer Res 2012; 18:3834-45; PMID:22615450; http://dx. doi. org/ 10. 1158/1078-0432. CCR-12-0715
24. Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 2012; 12:252-64; PMID:22437870; http:// dx. doi. org/10. 1038/nrc3239
25. Shin DS, Ribas A. The evolution of checkpoint blockade as a cancer therapy: what's here, what's next? Curr Opin Immunol 2015; 33C:23-35; http://dx. doi. org/10. 1016/j. coi. 2015. 01. 006
26. Benson DM, Jr., Bakan CE, Mishra A, Hofmeister CC, Efebera Y, Becknell B, Baiocchi RA, Zhang J, Yu J, Smith MK et al. The PD-1/ PD-L1 axis modulates the natural killer cell versus multiple myeloma effect: a therapeutic target for CT-011, a novel monoclonal anti-PD-1 antibody. Blood 2010; 116:2286-94; PMID:20460501; http://dx. doi. org/10. 1182/blood-2010-02-271874
27. Terme M, Ullrich E, Aymeric L, Meinhardt K, Desbois M, Delahaye N, Viaud S, Ryffel B, Yagita H, Kaplanski G et al. IL-18 induces PD-1-dependent immunosuppression in cancer. Cancer Res 2011; 71:5393-9; PMID:21724589; http://dx. doi. org/10. 1158/0008-5472. CAN-11-0993
28. Freeman GJ, Long AJ, Iwai Y, Bourque K, Chernova T, Nishimura H, Fitz LJ, Malenkovich N, Okazaki T, Byrne MC et al. Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J Exp Med 2000; 192:1027-34; PMID:11015443; http://dx. doi. org/10. 1084/ jem. 192. 7. 1027
29. Iwasaki M, Tanaka Y, Kobayashi H, Murata-Hirai K, Miyabe H, Sugie T, Toi M, Minato N. Expression and function of PD-1 in human gammadelta T cells that recognize phosphoantigens. Eur J Immunol 2011; 41:345-55; PMID:21268005; http://dx. doi. org/10. 1002/eji. 201040959
30. Ghiotto M, Gauthier L, Serriari N, Pastor S, Truneh A, Nunes JA, Olive D. PD-L1 and PD-L2 differ in their molecular mechanisms of interaction with PD-1. Int Immunol 2010; 22:651-60; PMID:20587542; http://dx. doi. org/10. 1093/intimm/dxq049
31. Zitvogel L, Kroemer G. Targeting PD-1/PD-L1 interactions for cancer immunotherapy. Oncoimmunology 2012; 1:1223-5; PMID:23243584; http://dx. doi. org/10. 4161/onci. 21335
32. Wilke CM, Wei S, Wang L, Kryczek I, Kao J, Zou W. Dual biological effects of the cytokines interleukin-10 and interferon-gamma. Cancer Immunol Immunother 2011; 60:1529-41; PMID:21918895; http://dx. doi. org/10. 1007/s00262-011-1104-5
33. Raffaghello L, Prigione I, Airoldi I, Camoriano M, Levreri I, Gambini C, Pende D, Steinle A, Ferrone S, Pistoia V. Downregulation and/or release of NKG2D ligands as immune evasion strategy of human neuroblastoma. Neoplasia 2004; 6:558-68; PMID:15548365; http://dx. doi. org/10. 1593/neo. 04316
34. Kramer K, Kushner BH, Modak S, Pandit-Taskar N, Smith-Jones P, Zanzonico P, Humm JL, Xu H, Wolden SL, Souweidane MM et al. Compartmental intrathecal radioimmunotherapy: results for treatment for metastatic CNS neuroblastoma. J Neuro Oncol 2010; 97:409-18; PMID:19890606; http://dx. doi. org/10. 1007/s11060-009-0038-7
35. Ritprajak P, Azuma M. Intrinsic and extrinsic control of expression of the immunoregulatory molecule PD-L1 in epithelial cells and squamous cell carcinoma. Oral Oncol 2015; 51:221-8; PMID:25500094; http://dx. doi. org/10. 1016/j. oraloncology. 2014. 11. 014
36. Boes M, Meyer-Wentrup F. TLR3 triggering regulates PD-L1 (CD274) expression in human neuroblastoma cells. Cancer Lett 2015; 361:49-56; PMID:25697485;http://dx. doi. org/10. 1016/j. canlet. 2015. 02. 027
37. Hamanishi J, Mandai M, Iwasaki M, Okazaki T, Tanaka Y, Yamaguchi K, Higuchi T, Yagi H, Takakura K, Minato N et al. Programmed cell death 1 ligand 1 and tumor-infiltrating CD8+ T lymphocytes are prognostic factors of human ovarian cancer. Proc Natl Acad Sci U S A 2007; 104:3360-5; PMID:17360651; http://dx. doi. org/10. 1073/pnas. 0611533104
38. Hino R, Kabashima K, Kato Y, Yagi H, Nakamura M, Honjo T, Okazaki T, Tokura Y. Tumor cell expression of programmed cell death-1 ligand 1 is a prognostic factor for malignant melanoma. Cancer 2010; 116:1757-66; PMID:20143437; http://dx. doi. org/10. 1002/cncr. 24899
39. Ohigashi Y, Sho M, Yamada Y, Tsurui Y, Hamada K, Ikeda N, Mizuno T, Yoriki R, Kashizuka H, Yane K et al. Clinical significance of programmed death-1 ligand-1 and programmed death-1 ligand-2 expression in human esophageal cancer. Clin Cancer Res 2005; 11:2947-53; PMID:15837746; http://dx. doi. org/10. 1158/1078-0432. CCR-04-1469
40. Thompson RH, Dong H, Kwon ED. Implications of B7-H1 expression in clear cell carcinoma of the kidney for prognostication and therapy. Clin Cancer Res 2007; 13:709s-15s; PMID:17255298; http://dx. doi. org/10. 1158/1078-0432. CCR-06-1868
41. Wu C, Zhu Y, Jiang J, Zhao J, Zhang XG, Xu N. Immunohistochemical localization of programmed death-1 ligand-1 (PD-L1) in gastric carcinoma and its clinical significance. Acta Histochem 2006; 108:19-24; PMID:16530813; http://dx. doi. org/10. 1016/j. acthis. 2006. 01. 003
42. Taube JM, Anders RA, Young GD, Xu H, Sharma R, McMiller TL, Chen S, Klein AP, Pardoll DM, Topalian SL, Chen L. Colocalization of inflammatory response with B7-h1 expression in human melanocytic lesions supports an adaptive resistance mechanism of immune escape. Sci Transl Med 2012; 4:127ra37; PMID:22461641; http://dx. doi. org/10. 1126/scitranslmed. 3003689
43. Di Leva G, Garofalo M, Croce CM. MicroRNAs in cancer. Ann Rev Pathol 2014; 9:287-314; PMID:24079833; http://dx. doi. org/10. 1146/ annurev-pathol-012513-104715
44. Gong AY, Zhou R, Hu G, Li X, Splinter PL, O'Hara SP, LaRusso NF, Soukup GA, Dong H, Chen XM. MicroRNA-513 regulates B7-H1 translation and is involved in IFN-gamma-induced B7-H1 expression in cholangiocytes. J Immunol 2009; 182:1325-33; PMID:19155478; http://dx. doi. org/10. 4049/jimmunol. 182. 3. 1325
45. BadoualC, Hans S, Merillon N, Van Ryswick C, Ravel P, BenhamoudaN, Levionnois E, Nizard M, Si-Mohamed A, Besnier N et al. PD-1-expressing tumor-infiltrating T cells are a favorable prognostic biomarker in HPVassociated head and neck cancer. Cancer Res 2013; 73:128-38; PMID:23135914; http://dx. doi. org/10. 1158/0008-5472. CAN-12-2606
46. Keir ME, Butte MJ, Freeman GJ, SharpeAH. PD-1 and its ligands in tolerance and immunity. Annual Rev Immunol 2008; 26:677-704; PMID:18173375; http://dx. doi. org/10. 1146/annurev. immunol. 26. 02-1607. 090331
47. Maude SL, Barrett D, Teachey DT, Grupp SA. Managing cytokine release syndrome associated with novel T cell-engaging therapies. Cancer J 2014; 20:119-22; http://dx. doi. org/10. 1097/PPO. 00000-00000000035
48. Nishio N, Diaconu I, Liu H, Cerullo V, Caruana I, Hoyos V, Bouchier-Hayes L, Savoldo B, Dotti G. Armed oncolytic virus enhances immune functions of chimeric antigen receptor-modified T cells in solid tumors. Cancer Res 2014; 74:5195-205; PMID:25060519; http://dx. doi. org/10. 1158/0008-5472. CAN-14-0697
49. Singh N, Liu X, Hulitt J, Jiang S, June CH, Grupp SA, Barrett DM, Zhao Y. Nature of tumor control by permanently and transiently modified GD2 chimeric antigen receptor T cells in xenograft models of neuroblastoma. Cancer Immunol Res 2014; 2:1059-70; PMID:25104548; http://dx. doi. org/10. 1158/2326-6066. CIR-14-0051
50. Louis CU, Savoldo B, Dotti G, Pule M, Yvon E, Myers GD, Rossig C, Russell HV, Diouf O, Liu E et al. Antitumor activity and long-term fate of chimeric antigen receptor-positive T cells in patients with neuroblastoma. Blood 2011; 118:6050-6; PMID:21984804; http://dx. doi. org/10. 1182/blood-2011-05-354449
51. Balkhi MY, Ma Q, Ahmad S, Junghans RP. T cell exhaustion and Interleukin 2 downregulation. Cytokine 2015; 71:339-47; PMID:25516298; http://dx. doi. org/10. 1016/j. cyto. 2014. 11. 024
52. Taube JM, Klein A, Brahmer JR, Xu H, Pan X, Kim JH, Chen L, Pardoll DM, Topalian SL, Anders RA. Association of PD-1, PD-1 ligands, and other features of the tumor immune microenvironment with response to anti-PD-1 therapy. Clin Cancer Res 2014; 20:5064-74; PMID:24714771; http://dx. doi. org/10. 1158/1078-0432. CCR-13-3271
53. Di Carlo E, Bocca P, Emionite L, Cilli M, Cipollone G, Morandi F, Raffaghello L, Pistoia V, Prigione I. Mechanisms of the antitumor activity of human Vgamma9Vdelta2 T cells in combination with zoledronic acid in a preclinical model of neuroblastoma. Mol Ther 2013; 21:1034-43; PMID:23481325; http://dx. doi. org/10. 1038/mt. 2013. 38
54. Airoldi I, Bertaina A, Prigione I, Zorzoli A, Pagliara D, Cocco C, Meazza R, Loiacono F, Lucarelli B, Bernardo ME, et al. gammadelta T cell reconstitution after HLA-haploidentical hematopoietic transplantation depleted of TCR-alphabeta+/CD19+ lymphocytes. Blood 2015; 125(15):2349-58; PMID:25612623; http://dx. doi. org/10. 1182/ blood-2014-09-599423
55. Corrias MV, Scaruffi P, Occhino M, De Bernardi B, Tonini GP, Pistoia V. Expression of MAGE-1, MAGE-3 and MART-1 genes in neuroblastoma. Int J Cancer 1996; 69:403-7; PMID:8900375; http://dx. doi. org/10. 1002/(SICI)1097-0215(19961021)69:5%3c403::AID-IJC9%3e3. 0. CO;2-9
56. Pastorino F, Loi M, Sapra P, Becherini P, Cilli M, Emionite L, Ribatti D, Greenberger LM, Horak ID, Ponzoni M. Tumor regression and curability of preclinical neuroblastoma models by PEGylated SN38 (EZN-2208), a novel topoisomerase I inhibitor. Clin Cancer Res 2010; 16:4809-21; PMID:20702613; http://dx. doi. org/10. 1158/1078-0432. CCR-10-1354
57. Molenaar JJ, Koster J, Zwijnenburg DA, van Sluis P, Valentijn LJ, van der Ploeg I, Hamdi M, van Nes J, Westerman BA, van Arkel J et al. Sequencing of neuroblastoma identifies chromothripsis and defects in neuritogenesis genes. Nature 2012; 483:589-93; PMID:22367537; http://dx. doi. org/10. 1038/nature10910