The ovarian cancer Chemokine landscape is conducive to homing of vaccine-primed and CD3/CD28-Costimulated T cells prepared for adoptive therapy

Clinical Cancer Research

Volumn 21, Issue 12, 2015, Pages 2840-2850

  Zsiros, Emese ^a,b   Duttagupta, Priyanka ^a   Dangaj, Denarda ^a,c   Li, Hongzhe ^a   Frank, Renee ^a   Garrabrant, Thomas ^a   Hagemann, Ian S ^a   Levine, Bruce L ^a   June, Carl H ^a   Zhang, Lin ^a   Wang, Ena ^d,e   Marincola, Francesco M ^d,e   Bedognetti, Davide ^d,e   Powell, Daniel J ^a   Tanyi, Janos ^a   Feldman, Michael D ^a   Kandalaft, Lana E ^a,c,f   Coukos, George ^a,c,f  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b ROSWELL PARK CANCER INSTITUTE   (United States)

^c LUDWIG INSTITUTE FOR CANCER RESEARCH   (Switzerland)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

^e SIDRA MEDICAL AND RESEARCH CENTER   (Qatar)

^f LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CD28 ANTIGEN; CD3 ANTIGEN; CHEMOKINE; CHEMOKINE RECEPTOR; CHEMOKINE RECEPTOR CXCR3; CHEMOKINE RECEPTOR CXCR4; CXCL16 CHEMOKINE; DENDRITIC CELL VACCINE; EPIDERMAL GROWTH FACTOR RECEPTOR 2; GAMMA INTERFERON INDUCIBLE PROTEIN 10; HLA A2 ANTIGEN; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; STROMAL CELL DERIVED FACTOR 1; BIOLOGICAL MARKER; CANCER VACCINE; T LYMPHOCYTE RECEPTOR;

ADOPTIVE IMMUNOTHERAPY; ADULT; ADVANCED CANCER; ARTICLE; CELL EXPANSION; EX VIVO STUDY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; LYMPHOCYTE HOMING; LYMPHOCYTE MIGRATION; MAJOR CLINICAL STUDY; OVARY CANCER; PHASE 1 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; T LYMPHOCYTE; TISSUE MICROARRAY; TUMOR ASSOCIATED LEUKOCYTE; CANCER GRADING; CANCER STAGING; CLUSTER ANALYSIS; DENDRITIC CELL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; METABOLISM; NEUTROPHIL CHEMOTAXIS; OVARIAN NEOPLASMS; T LYMPHOCYTE SUBPOPULATION;

ANTIGENS, CD28; ANTIGENS, CD3; BIOMARKERS; CANCER VACCINES; CHEMOKINES; CHEMOTAXIS, LEUKOCYTE; CLUSTER ANALYSIS; DENDRITIC CELLS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOHISTOCHEMISTRY; IMMUNOTHERAPY, ADOPTIVE; NEOPLASM GRADING; NEOPLASM STAGING; OVARIAN NEOPLASMS; T-CELL ANTIGEN RECEPTOR SPECIFICITY; T-LYMPHOCYTE SUBSETS;

EID: 84936890861     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-14-2777     Document Type: Article

References (50)

1. Zhang L, Conejo-Garcia JR, Katsaros D, Gimotty PA, Massobrio M, Regnani G, et al. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N Engl J Med 2003;348:203-13.
2. Curiel TJ, Coukos G, Zou L, Alvarez X, Cheng P, Mottram P, et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 2004;10:942-9.
3. Kryczek I, Wei S, Zhu G, Myers L, Mottram P, Cheng P, et al. Relationship between B7-H4, regulatory T cells, and patient outcome in human ovarian carcinoma. Cancer Res 2007;67:8900-5.
4. Kandalaft LE, Powell DJ Jr, Chiang CL, Tanyi J, Kim S, Bosch M, et al. Autologous lysate-pulsed dendritic cell vaccination followed by adoptive transfer of vaccine-primed ex vivo co-stimulated T cells in recurrent ovarian cancer. Oncoimmunology 2013;2:e22664.
5. Chiang CL, Hagemann AR, Leskowitz R, Mick R, Garrabrant T, Czerniecki BJ, et al. Day-4 myeloid dendritic cells pulsed with whole tumor lysate are highly immunogenic and elicit potent anti-Tumor responses. PLoS ONE 2011;6:e28732.
6. Kandalaft LE, Chiang CL, Tanyi J, Motz G, Balint K, Mick R, et al. A phase I vaccine trial using dendritic cells pulsed with autologous oxidized lysate for recurrent ovarian cancer. J Transl Med 2013;11:149.
7. Chiang CL, Kandalaft LE, Tanyi J, Hagemann AR, Motz GT, Svoronos N, et al. A dendritic cell vaccine pulsed with autologous hypochlorous acidoxidized ovarian cancer lysate primes effective broad antitumor immunity: from bench to bedside. Clin Cancer Res 2013;19:4801-15.
8. Springer TA. Traffic signals for lymphocyte recirculation and leukocyte emigration: The multistep paradigm. Cell 1994;76:301-14.
9. Mukai S, Kjaergaard J, Shu S, Plautz GE. Infiltration of tumors by systemically transferred tumor-reactive T lymphocytes is required for antitumor efficacy. Cancer Res 1999;59:5245-9.
10. Zlotnik A, YoshieO.Chemokines: A new classification system and their role in immunity. Immunity 2000;12:121-7.
11. Baggiolini M, Dewald B, Moser B. Human chemokines: An update. Annu Rev Immunol 1997;15:675-705.
12. Luster AD. Chemokines-chemotactic cytokines that mediate inflammation. N Engl J Med 1998;338:436-45.
13. Kulbe H, Chakravarty P, Leinster DA, Charles KA, Kwong J, Thompson RG, et al. A dynamic inflammatory cytokine network in the human ovarian cancer microenvironment. Cancer Res 2012;72:66-75.
14. Vandercappellen J, Van Damme J, Struyf S. The role of CXC chemokines and their receptors in cancer. Cancer Lett 2008;267:226-44.
15. Wang JM, Deng X, Gong W, Su S. Chemokines and their role in tumor growth and metastasis. J Immunol Methods 1998;220:1-17.
16. Zlotnik A, Yoshie O. The chemokine superfamily revisited. Immunity 2012;36:705-16.
17. Balkwill FR. The chemokine system and cancer. J Pathol 2012;226:148-57.
18. Owen JL, Criscitiello MF, Libreros S, Garcia-Areas R, Guthrie K, Torroella-Kouri M, et al. Expression of the inflammatory chemokines CCL2, CCL5 and CXCL2 and the receptors CCR1-3 and CXCR2 in T lymphocytes from mammary tumor-bearing mice. Cell Immunol 2011;270:172-82.
19. Hwang TL, Lee LY, Wang CC, Liang Y, Huang SF, WuCM. CCL7 and CCL21 overexpression in gastric cancer is associated with lymph node metastasis and poor prognosis. World J Gastroenterol 2012;18:1249-56.
20. Vinader V, Afarinkia K. The emerging role of CXC chemokines and their receptors in cancer. Future Med Chem 2012;4:853-67.
21. Oh SM, Oh K, Lee DS. Intratumoral administration of secondary lymphoid chemokine and unmethylated cytosine-phosphorothioate-guanine oligodeoxynucleotide synergistically inhibits tumor growth in vivo. J Korean Med Sci 2011;26:1270-6.
22. Liu Q, Tomei S, Ascierto ML, De Giorgi V, Bedognetti D, Dai C, et al. Melanoma NOS1 expression promotes dysfunctional IFN signaling. J Clin Invest 2014;124:2147-59.
23. Tothill RW, Tinker AV, George J, Brown R, Fox SB, Lade S, et al. Novel molecular subtypes of serous and endometrioid ovarian cancer linked to clinical outcome. Clin Cancer Res 2008;14:5198-208.
24. Bertozzi CC, Chang CY, Jairaj S, Shan X, Huang J, Weber BL, et al. Multiple initial culture conditions enhance the establishment of cell lines from primary ovarian cancer specimens. In Vitro Cell Dev Biol Anim 2006;42:58-62.
25. Lanitis E, Dangaj D, Hagemann IS, Song DG, Best A, Sandaltzopoulos R, et al. Primary human ovarian epithelial cancer cells broadly express HER2 at immunologically-detectable levels. PLoS ONE 2012;7: e49829.
26. Hagemann AR, Hagemann IS, Cadungog M, Hwang WT, Patel P, Lal P, et al. Tissue-based immune monitoring II: multiple tumor sites reveal immunologic homogeneity in serous ovarian carcinoma. Cancer Biol Ther 2011;12:367-77.
27. Facciabene A, Peng X, Hagemann IS, Balint K, Barchetti A, Wang LP, et al. Tumour hypoxia promotes tolerance and angiogenesis via CCL28 and T (reg) cells. Nature 2011;475:226-30.
28. Facciabene A, Santoro S, Coukos G. Know thy enemy: why are tumorinfiltrating regulatory T cells so deleterious? Oncoimmunology 2012;1: 575-7.
29. Kiefer F, Siekmann AF. The role of chemokines and their receptors in angiogenesis. Cell Mol Life Sci 2011;68:2811-30.
30. Dunussi-Joannopoulos K, Zuberek K, Runyon K, Hawley RG, Wong A, Erickson J, et al. Efficacious immunomodulatory activity of the chemokine stromal cell-derived factor 1 (SDF-1): local secretion of SDF-1 at the tumor site serves as T-cell chemoattractant and mediates T-cell-dependent antitumor responses. Blood 2002;100:1551-8.
31. Franciszkiewicz K, Boutet M, Gauthier L, Vergnon I, Peeters K, Duc O, et al. Synaptic release of CCL5 storage vesicles triggers CXCR4 surface expression promoting CTL migration in response to CXCL12. J Immunol 2014;193: 4952-61.
32. Guo L, Cui ZM, Zhang J, Huang Y. Chemokine axes CXCL12/CXCR4 and CXCL16/CXCR6 correlate with lymph node metastasis in epithelial ovarian carcinoma. Chinese J Cancer 2011;30:336-43.
33. Son DS, Parl AK, Rice VM, Khabele D. Keratinocyte chemoattractant (KC)/human growth-regulated oncogene (GRO) chemokines and pro-inflammatory chemokine networks in mouse and human ovarian epithelial cancer cells. Cancer Biol Ther 2007;6:1302-12.
34. Phillips RJ, Burdick MD, Lutz M, Belperio JA, Keane MP, Strieter RM. The stromal derived factor-1/CXCL12-CXC chemokine receptor 4 biological axis in non-small cell lung cancer metastases. Am J Respir Crit Care Med 2003;167:1676-86.
35. Zeelenberg IS, Ruuls-Van Stalle L, Roos E. The chemokine receptor CXCR4 is required for outgrowth of colon carcinoma micrometastases. Cancer Res 2003;63:3833-9.
36. Jiang YP, WuXH, Shi B, WuWX, Yin GR. Expression of chemokine CXCL12 and its receptor CXCR4 in human epithelial ovarian cancer: An independent prognostic factor for tumor progression. Gynecol Oncol 2006;103: 226-33.
37. Machelon V, Gaudin F, Camilleri-Broet S, Nasreddine S, Bouchet-Delbos L, Pujade-Lauraine E, et al. CXCL12 expression by healthy and malignant ovarian epithelial cells. BMC Cancer 2011;11:97.
38. Hershberger PM, Peddibhotla S, Sugarman E, Maloney P, Key D, Suyama E, et al. Probing the CXCR6/CXCL16 axis: Targeting prevention of prostate cancer metastasis. Probe Reports from the NIH Molecular Libraries Program. Bethesda (MD); 2010.
39. Matsushita K, Toiyama Y, Tanaka K, Saigusa S, Hiro J, Uchida K, et al. Soluble CXCL16 in preoperative serum is a novel prognostic marker and predicts recurrence of liver metastases in colorectal cancer patients. Ann Surg Oncol 2012;19:S518-27.
40. Deng L, Chen N, Li Y, Zheng H, Lei Q. CXCR6/CXCL16 functions as a regulator in metastasis and progression of cancer. Biochim Biophys Acta 2010;1806:42-9.
41. Huang J, Zhang L, Greshock J, Colligon TA, Wang Y, Ward R, et al. Frequent genetic abnormalities of the PI3K/AKT pathway in primary ovarian cancer predict patient outcome. Genes Chromosomes Cancer 2011;50:606-18.
42. Rainczuk A, Rao JR, Gathercole JL, Fairweather NJ, Chu S, Masadah R, et al. Evidence for the antagonistic form of CXC-motif chemokine CXCL10 in serous epithelial ovarian tumours. Int J Cancer 2013;134:530-41.
43. Feig C, Jones JO, Kraman M, Wells RJ, Deonarine A, Chan DS, et al. Targeting CXCL12 from FAP-expressing carcinoma-Associated fibroblasts synergizes with anti-PD-L1 immunotherapy in pancreatic cancer. Proc Natl Acad Sci U S A 2013;110:20212-7.
44. Zou W, Machelon V, Coulomb-L'Hermin A, Borvak J, NomeF, Isaeva T, et al. Stromal-derived factor-1 in humantumors recruits and alters the function of plasmacytoid precursor dendritic cells. Nat Med 2001;7:1339-46.
45. Wang Z, Zhang L, Qiao A, Watson K, Zhang J, Fan GH. Activation of CXCR4 triggers ubiquitination and down-regulation of major histocompatibility complex class I (MHC-I) on epithelioid carcinoma HeLa cells. J Biol Chem 2008;283:3951-9.
46. Han LY, Fletcher MS, Urbauer DL, Mueller P, Landen CN, Kamat AA, et al. HLA class I antigen processing machinery component expression and intratumoral T-Cell infiltrate as independent prognostic markers in ovarian carcinoma. Clin Cancer Res 2008;14:3372-9.
47. Buckanovich RJ, Facciabene A, Kim S, Benencia F, Sasaroli D, Balint K, et al. Endothelin B receptormediates the endothelial barrier to T cell homing to tumors and disables immune therapy. Nat Med 2008;14:28-36.
48. Motz GT, Santoro SP, Wang LP, Garrabrant T, Lastra RR, Hagemann IS, et al. Tumor endothelium FasL establishes a selective immune barrier promoting tolerance in tumors. Nat Med 2014;20:607-15.
49. Motz GT, Coukos G. Deciphering and reversing tumor immune suppression. Immunity 2013;39:61-73.
50. Gaber T, Strehl C, Sawitzki B, Hoff P, Buttgereit F. Cellular Energy Metabolism in T-Lymphocytes. Int Rev Immunol 2015;34:34-49.