Combining Antiangiogenic Therapy with Adoptive Cell Immunotherapy Exerts Better Antitumor Effects in Non-Small Cell Lung Cancer Models

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Shi, Shujing ^a   Wang, Rui ^a   Chen, Yitian ^a   Song, Haizhu ^a   Chen, Longbang ^a   Huang, Guichun ^a  

^a MEDICAL SCHOOL OF NANJING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GADOLINIUM PENTETATE; RECOMBINANT ENDOSTATIN;

ADOPTIVE IMMUNOTHERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC THERAPY; ARTICLE; CANCER INHIBITION; CD3+ T LYMPHOCYTE; CELL MEDIATED CYTOTOXICITY; CONTRAST ENHANCEMENT; CONTROLLED STUDY; CYTOKINE INDUCED KILLER CELL; FLOW CYTOMETRY; HYPOXIA; IMMUNOHISTOCHEMISTRY; LUNG NON SMALL CELL CANCER; LYMPHOCYTE HOMING; LYMPHOCYTE MIGRATION; LYMPHOCYTE PROLIFERATION; LYMPHOCYTIC INFILTRATION; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; TUMOR ASSOCIATED LEUKOCYTE; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION;

ANGIOGENESIS INHIBITORS; ANIMALS; CARCINOMA, NON-SMALL-CELL LUNG; CELL HYPOXIA; CELL LINE, TUMOR; CELL MOVEMENT; CELL SHAPE; COMBINED MODALITY THERAPY; CYTOKINE-INDUCED KILLER CELLS; ENDOSTATINS; HUMANS; IMMUNOTHERAPY, ADOPTIVE; LUNG NEOPLASMS; LYMPHOCYTES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, NUDE; MICROVESSELS; MYELOID CELLS; SPLEEN; TUMOR BURDEN; TUMOR MICROENVIRONMENT; XENOGRAFT MODEL ANTITUMOR ASSAYS;

MURINAE;

EID: 84879058083     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065757     Document Type: Article

References (53)

1. Siegel R, Naishadham D, Jemal A, (2010) Cancer statistics. CA Cancer J Clin 62: 10-29.
2. Rettinger E, Kuçi S, Naumann I, Becker P, Kreyenberg H, et al. (2012) The cytotoxic potential of interleukin-15-stimulated cytokine-induced killer cells against leukemia cells. Cytotherapy 14: 91-103.
3. Yu J, Ren X, Li H, Cao S, Han Y, et al. (2011) Synergistic effect of CH-296 and interferon gamma on cytokine-induced killer cells expansion for patients with advanced-stage malignant solid tumors. Cancer Biother Radiopharm 26: 485-494.
4. Chen J, Huang X, Huang G, Chen Y, Chen L, et al. (2012) Preconditioning chemotherapy with cisplatin enhances the antitumor activity of cytokine-induced killer cells in a murine melanoma model. Cancer Biother Radiopharm 27: 210-220.
5. Draghiciu O, Nijman HW and Daemen T (2011) From tumor immunosuppression to radication: targeting homing and activity of immune effector cells to tumors. Clin Dev Immunol 2011. Available: http://www.hindawi.com/journals/cdi/2011/439053/. Accepted 6 September 2011.
6. Rosenberg SA, (2008) Overcoming obstacles to the effective immunotherapy of human cancer. Proc Natl Acad Sci USA 105: 12643-12644.
7. Griffioen AW, (2008) Anti-angiogenesis: making the tumor vulnerable to the immune system. Cancer Immunol Immunother 57: 1553-1558.
8. Jiang XD, Dai P, Wu J, Song DA, Yu JM, (2011) Inhibitory effect of radiotherapy combined with weekly recombinant human endostatin on the human pulmonary adenocarcinoma A549 xenografts in nude mice. Lung Cancer 72: 165-171.
9. Sharma R, (2011) Nitroimidazole radiopharmaceuticals in hypoxia: part II cytotoxicity and radiosensitization applications. Curr Radiopharm 4: 379-393.
10. Sophie D, Dimas CB, Manuela P, Laura A, Chiara R, et al. (2012) HIF-1 activation induces doxorubicin resistance in MCF7 3-D spheroids via P-glycoprotein expression: a potential model of the chemo-resistance of invasive micropapillary carcinoma of the breast. BMC Cancer 12: 4. Available: http://www.biomedcentral.com/1471-2407/12/4. Accessed 4 January 2012.
11. Jain RK, (2005) Antiangiogenic Therapy Normalization of Tumor Vasculature: An Emerging Concept in Antiangiogenic therapy. Science 307: 58-62.
12. Huang Y, Yuan J, Righi E, Kamoun WS, Ancukiewicz M, et al. (2012) Vascular normalizing doses of antiangiogenic treatment reprogram the immunosuppressive tumor microenvironment and enhance immunotherapy. Proc Natl Acad Sci U S A 109: 17561-17566.
13. Cerniglia GJ, Pore N, Tsai JH, Schultz S, Mick R, et al. (2009) Epidermal Growth Factor Receptor Inhibition Modulates the Microenvironment by Vascular Normalization to Improve Chemotherapy and Radiotherapy Efficacy. PLoS ONE 4(8): e6539. Available: http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0006539. Accessed 6 August 2009.
14. Myers AL, Williams RF, Ng CY, Hartwich JE, Davidoff AM, (2012) Bevacizumab-induced tumor vessel remodeling in rhabdomyosarcoma xenografts increases the effectiveness of adjuvant ionizing radiation. J Pediatr Surg 45: 1080-1085.
15. Huang KW, Wu HL, Lin HL, Liang PC, Chen PJ, et al. (2010) Combining antiangiogenic therapy with immunotherapy exerts better therapeutical effects on large tumors in a woodchuck hepatoma model. Proc Natl Acad Sci U S A 107: 14769-14774.
16. Shrimali RK, Yu Z, Theoret MR, Chinnasamy D, Restifo NP, et al. (2010) Antiangiogenic agents can increase lymphocyte infiltration into tumor and enhance the effectiveness of adoptive immunotherapy of cancer. Cancer Res 70: 6171-6180.
17. Sakurai T, Kudo M, (2011) Signaling pathways governing tumor angiogenesis. Oncology 81: 24-29.
18. Zhang HY, Han QW, Xu YF, Fan YR, Dai QM, et al. (2005) The methods for determining the purity and in vitro or in vivo activity of recombinant human endostatin. Cancer Biol Ther 4: 207-212.
19. Huang G, Chen LB, (2010) Recombinant human endostatin improves anti-tumor efficacy of paclitaxel by normalizing tumor vasculature in Lewis lung carcinoma. J Cancer Res Clin Oncol 136: 1201-1211.
20. Wen QL, Meng MB, Yang B, Tu LL, Jia L, et al. (2009) Endostar, a recombined humanized endostatin, enhances the radioresponse for human nasopharyngeal carcinoma and human lung adenocarcinoma xenografts in mice. Cancer Sci 100: 1510-1519.
21. Feng B, Wang R, Song HZ, Chen LB, (2012) MicroRNA-200b reverses chemoresistance of docetaxel-resistant human lung adenocarcinoma cells by targeting E2F3. Cancer 118: 3365-3376.
22. George AL, Rajoria S, Suriano R, Mittleman A, Tiwari RK, (2012) Hypoxia and estrogen are functionally equivalent in breast cancer-endothelial cell interdependence. Mol Cancer 22 11: 80.
23. Hongeng S, Petvises S, Worapongpaiboon S, Rerkamnuaychoke B, Pakakasama S, et al. (2003) Generation of CD3+ CD56+ cytokine-induced killer cells and their in vitro cytotoxicity against pediatric cancer cells. Int J Hematol 77: 175-179.
24. Jin ZJ, (1980) Liner transformation of Michaelis-Menton equation by Lineweaver-Burk's method. Acta Pharm Sinica 1: 3-7.
25. Shi H, Yang W, Cui ZH, Lu CW, Li XH, et al. (2011) Tracking of CFSE-labeled endothelial progenitor cells in laser-injured mouse retina. Chin Med J (Engl) 124: 751-757.
26. Zhou QY, Guo P, Gallo JM, (2008) Impact of angiogenesis inhibition by sunitinib on tumor distribution of temozolomide. Clin Cancer Res 14: 1540-1549.
27. Tofts PS, Brix G, Buckley DL, Evelhoch JL, Henderson E, et al. (1999) Estimating kinetic parameters from dynamic contrast-enhanced T(1)-weighted MRI of a diffusable tracer: standardized quantities and symbols. J Magn Reson Imaging 10: 223-232.
28. Rettinger E, Kuçi S, Naumann I, Becker P, Kreyenberg H, et al. (2012) The cytotoxic potential of interleukin-15-stimulated cytokine-induced killer cells against leukemia cells. Cytotherapy 14: 91-103.
29. Yu J, Ren X, Li H, Cao S, Han Y, et al. (2011) Synergistic effect of CH-296 and interferon gamma on cytokine-induced killer cells expansion for patients with advanced-stage malignant solid tumors. Cancer Biother Radiopharm 26: 485-494.
30. Sangiolo D, (2011) Cytokine induced killer cells as promising immunotherapy for solid tumors. J Cancer 2: 363-368.
31. Chinnasamy D, Yu Z, Theoret MR, Zhao Y, Shrimali RK, et al. (2010) Gene therapy using genetically modified lymphocytes targeting VEGFR-2 inhibits the growth of vascularized syngenic tumors in mice. J Clin Invest 120: 3953-3968.
32. Fukumura D, Jain RK, (2007) Tumor microvasculature and microenvironment: targets for anti-angiogenesis and normalization. Microvasc Res 74: 72-84.
33. Hamzah J, Jugold M, Kiessling F, Rigby P, Manzur M, et al. (2008) Vascular normalization in Rgs5-deficient tumours promotes immune destruction. Nature 453: 410-414.
34. Javaherian K, Lee TY, Tjin Tham Sjin RM, Parris GE, Hlatky L, (2011) Two endogenous antiangiogenic inhibitors, endostatin and angiostatin, demonstrate biphasic curves in their antitumor profiles. Dose-Response 9: 369-376.
35. Lee CT, Mace T, Repasky EA, (2010) Hypoxia-driven immunosuppression: a new reason to use thermal therapy in the treatment of cancer? Int J Hyperthermi 26: 232-246.
36. Wei J, Wu A, Kong LY, Wang Y, Fuller G, et al. (2011) Hypoxia potentiates glioma-mediated immunosuppression. PLoS ONE 6: e16195. Available: http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0016195. Accessed 20 January, 2011.
37. Relf M, LeJeune S, Scott PA, Fox S, Smith K, et al. (1997) Expression of the angiogenic factors vascular endothelial cell growth factor, acidic and basic fibroblast growth factor, tumor growth factor beta-1, platelet-derived endothelial cell growth factor, placenta growth factor, and pleiotrophin in human primary breast cancer and its relation to angiogenesis. Cancer Res 57: 963-969.
38. Nagy JA, Benjamin L, Zeng HY, Dvorak AM, Dvorak HF, (2008) Vascular permeability, vascular hyperpermeability and angiogenesis. Angiogenesis 11: 109-119.
39. Øvrebø KM, Ellingsen C, Hompland T, Rofstad EK (2012) Dynamic contrast-enhanced magnetic resonance imaging of the metastatic potential of tumors: A preclinical study of cervical carcinoma and melanoma xenografts. Acta Oncol 2012. Available: http://informahealthcare.com/doi/abs/10.3109/0284186X.2012.689851. Accessed 6 November, 2012.
40. Hompland T, Gulliksrud K, Ellingsen C, Rofstad EK (2012) Assessment of the interstitial fluid pressure of tumors by dynamic contrast-enhanced magnetic resonance imaging with contrast agents of different molecular weights. Acta Oncol. Available: http://informahealthcare.com/doi/abs/10.3109/0284186X.2012.737931. Accepted 28 September 2012.
41. Barsoum IB, Hamilton TK, Li X, Cotechini T, Miles EA, et al. (2011) Hypoxia induces escape from innate immunity in cancer cells via increased expression of ADAM10: role of nitric oxide. Cancer Res 71: 7433-7441.
42. Noman MZ, Messai Y, Carré T, Akalay I, Méron M, et al. (2011) Microenvironmental hypoxia orchestrating the cell stroma cross talk, tumor progression and antitumor response. Crit Rev Immunol 31: 357-377.
43. Ogino T, Onishi H, Suzuki H, Morisaki T, Tanaka M, et al. (2012) Inclusive estimation of complex antigen presentation functions of monocyte-derived dendritic cells differentiated under normoxia and hypoxia conditions. Cancer Immunol Immunother 61: 409-424.
44. Hasmim M, Noman MZ, Lauriol J, Benlalam H, Mallavialle A, et al. (2011) Hypoxia-dependent inhibition of tumor cell susceptibility to CTL-mediated lysis involves NANOG induction in target cells. J Immunol 187: 4031-4039.
45. Naruse T, Kawasaki G, Yanamoto S, Mizuno A, Umeda M, (2011) Immunohistochemical study of VEGF expression in oral squamous cell carcinomas: correlation with the mTOR-HIF-1α pathway. Anticancer Res 31: 4429-4437.
46. Dirkx AE, oude Egbrink MG, Castermans K, van der Schaft DW, Thijssen VL, et al. (2006) Anti-angiogenesis therapy can overcome endothelial cell anergy and promote leukocyte-endothelium interactions and infiltration in tumors. FASEB J 20: 621-630.
47. Dirkx AE, Oude Egbrink MG, Kuijpers MJ, van der Niet ST, Heijnen VV, et al. (2003) Tumor angiogenesis modulates leukocyte-vessel wall interactions in vivo by reducing endothelial adhesion molecule expression. Cancer Res 63: 2322-2329.
48. Diaz-Montero CM, Salem ML, Nishimura MI, Garrett-Mayer E, Cole DJ, et al. (2009) Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin-cyclophosphamide chemotherapy. Cancer Immunol Immunother 58: 49-59.
49. Ostrand-Rosenberg S, Sinha P, (2009) Myeloid-derived suppressor cells: linking inflammation and cancer. J Immunol 182: 4499-4506.
50. Lu T, Ramakrishnan R, Altiok S, Youn JI, Cheng P, et al. (2011) Tumor-infiltrating myeloid cells induce tumor cell resistance to cytotoxic T cells in mice. J Clin Invest 121: 4015-4029.
51. Martinez FO, Helming L, Gordon S, (2009) Alternative activation of macrophages: an immunologic functional perspective. Annu Rev Immuno 27: 451-483.
52. Sica A, Schioppa T, Mantovani A, Allavena P, (2006) Tumour-associated macrophages are a distinct M2 polarised population promoting tumour progression: Potential targets of anti-cancer therapy. Eur J Cancer 42: 717-727.
53. Cortez-Retamozo V, Etzrodt M, Newton A, Rauch PJ, Chudnovskiy A, et al. (2012) Origins of tumor-associated macrophages and neutrophils. Proc Natl Acad Sci USA 109: 2491-2496.