Lymphocyte subpopulation and dendritic cell phenotyping during antineoplastic therapy in human solid tumors

Clinical and Experimental Medicine

Volumn 11, Issue 4, 2011, Pages 199-210

  Mariucci, Sara ^a   Rovati, Bianca ^a   Manzoni, Mariangela ^b   Della Porta, Matteo Giovanni ^b   Comolli, Giuditta ^a   Delfanti, Sara ^b   Danova, Marco ^b  

^a FONDAZIONE IRCCS POLICLINICO SAN MATTEO   (Italy)

^b UNIVERSITY OF PAVIA   (Italy)

Author keywords

Angiogenesis; Antineoplastic therapy; Dendritic cells; Lymphocyte subsets; Solid tumors

Indexed keywords

AFLIBERCEPT; ANTHRACYCLINE; ANTINEOPLASTIC AGENT; BEVACIZUMAB; CYTOTOXIC AGENT; DENDRITIC CELL VACCINE; ETOPOSIDE; FLUOROURACIL; GAMMA INTERFERON; GRANULOCYTE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 4; INTERLEUKIN 5; PLATINUM DERIVATIVE; SORAFENIB; SUNITINIB; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR FOXP3; TUMOR ANTIGEN; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN;

ADVANCED CANCER; ANTIANGIOGENIC ACTIVITY; ANTIANGIOGENIC THERAPY; ANTIGEN EXPRESSION; B LYMPHOCYTE; BACTERIAL INFECTION; BREAST CANCER; BREAST CARCINOMA; CANCER CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; COLORECTAL CANCER; COLORECTAL CARCINOMA; CYTOKINE PRODUCTION; DENDRITIC CELL; DRUG DOSE ESCALATION; DRUG EFFICACY; ENDOTHELIUM CELL; EPSTEIN BARR VIRUS ASSOCIATED LYMPHOPROLIFERATIVE DISORDER; EPSTEIN BARR VIRUS INFECTION; GASTROINTESTINAL STROMAL TUMOR; HELPER CELL; HUMAN; IMMUNE DEFICIENCY; IMMUNOPHENOTYPING; INFECTION SENSITIVITY; KIDNEY CARCINOMA; LIVER CELL CARCINOMA; LUNG CARCINOMA; LUNG NON SMALL CELL CANCER; LYMPHOCYTE DEPLETION; LYMPHOCYTE SUBPOPULATION; LYMPHOCYTIC INFILTRATION; LYMPHOPROLIFERATIVE DISEASE; METASTASIS; MULTICENTER STUDY (TOPIC); MYCOSIS; NATURAL KILLER CELL; NATURAL KILLER T CELL; NEUTROPENIA; OPPORTUNISTIC INFECTION; OVERALL SURVIVAL; PARASITOSIS; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; REGULATORY T LYMPHOCYTE; REVIEW; SOLID TUMOR; T LYMPHOCYTE; TRANSFUSION ASSOCIATED GRAFT VERSUS HOST DISEASE; TREATMENT OUTCOME; TUMOR ASSOCIATED LEUKOCYTE; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION; VIRUS INFECTION;

ANTINEOPLASTIC AGENTS; DENDRITIC CELLS; DRUG THERAPY, COMBINATION; HUMANS; IMMUNE TOLERANCE; IMMUNOPHENOTYPING; LYMPHOCYTE SUBSETS; NEOPLASMS;

EID: 84855693772     PISSN: 15918890     EISSN: 15919528     Source Type: Journal    
DOI: 10.1007/s10238-010-0120-7     Document Type: Review

References (106)

1. Formenti SC (2010) Immunological aspects of local radiotherapy: Clinical relevance. Discov Med 9:119-124
2. Fens MH, Storm G, Schiffelers RM (2010) Tumor vasculature as target for therapeutic intervention. Expert Opin Investig Drugs. doi:10.1517/13543784.2010. 52
3. Welch S, Spithoff K, Rumble RB, Maroun J (2010) Bevacizumab combined with chemotherapy for patients with advanced colorectal cancer: A systematic review. Ann Oncol 21:1152-1162
4. Winkeljohn DL (2008) Review of panitumumab: A targeted therapy. Clin J Oncol Nurs 12:30-32
5. Catalano MG, Poli R, Pugliese M, Fortunati N, Boccuzzi G (2010) Emerging molecular terapie of advanced thyroid cancer. Mol Aspects Med 31:215-226
6. Lanzavecchia A, Sallusto F (2005) Understanding the generation and function of memory T cells subsets. Curr Opin Immunol 17:326-332 (Pubitemid 40692670)
7. Ruffell B, DeNardo DG, Affara NI, Coussens LM (2010) Lymphocytes in cancer development: Polarization towards protumor immunity. Cytokine Growth Factor Rev 21:3-10
8. Ostrand-Rosenberg S (2008) Immune surveillance: A balance between pro-and anti-tumor immunity. Curr Opin Genet Dev 18:11-18 (Pubitemid 351694442)
9. Lyle S, Salhany KE, Elder DE (2000) TIA-1 positive tumorinfiltrating lymphocytes in nevi and melanomas. Mod Pathol 13:52-55 (Pubitemid 30077904)
10. Elder D (1999) Tumor progression, early diagnosis and prognosis of melanoma. Acta Oncol 38:535-547 (Pubitemid 29333733)
11. Prall F, Dührkop T, Weirich V, Ostwald C, Lenz P, Nizze H, Barten M (2004) Prognostic role of CD8+ tumor-infiltrating lymphocytes in stage III colorectal cancer with and without microsatellite instability. Hum Pathol 35:808-816 (Pubitemid 38903073)
12. Zhang L, Garcia Conejo, Katsaros D, Gimotty PA, Massobrio M, Regnani G, Makrigiannakis A, Gray H, Schlienger K, Liebman MN, Rubin SC, Coukos G (2003) Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N Engl J Med 348:203-213 (Pubitemid 36077915)
13. Uppaluri R, Dunn GP, Lewis JS Jr (2008) Focus on TILs: Prognostic significance of tumor infiltrating lymphocytes in head and neck cancers. Cancer Immun 8:16
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) Science 298:850-854
15. Cesco-Gaspere M, Morris E, Stauss HJ (2009) Immunomodulation in the treatment of haematological malignancies. Clin Exp Med 9:81-92
16. Siu D (2009) Cancer therapy using tumor-associated antigens to reduce side effects. Clin Exp Med 9:181-198
17. de Visser KE, Korets LV, Coussens LM (2005) De novo carcinogenesis promoted by chronic inflammation is B lymphocyte dependent. Cancer Cell 7:411-423 (Pubitemid 40719125)
18. Tan TT, Coussens LM (2007) Humoral immunity, inflammation and cancer. Curr Opin Immunol 19:209-216 (Pubitemid 46356960)
19. Ferlazzo G, Pack M, Thomas D, Paludan C, Schmid D, Strowig T Bougras G, Muller WA, Moretta L, Münz C (2004) Distinct CT roles of IL-12 and IL-15 in human natural killer cell activation by dendritic cells from secondary lymphoid organs. Proc Natl Acad Sci USA 101:16606-16611 (Pubitemid 39557760)
20. Becknell B, Caligiuri MA (2008) Natural killer cells in innate immunity and cancer. J Immunother 31:685-692
21. Trinchieri G (1989) Biology of natural killer cells. Adv Immunol 47:187-376 (Pubitemid 20010960)
22. Giuliani M, Giron-Mechel J, Negrini S, Vacca P, Durali D, Caignard A, Le Bousse-Kerdiles C, Chouaib S, Devocelle A, Bahri R, Durrbach A, Taoufik Y, Ferrini S, Croce M, Mingari MC, Moretta L, Azzarone B (2008) Generation of a novelregulatory NK cell subset from peripheral blood CD34? progenitors promoted by membrane-bound IL-15. PLoS One 3:e2241
23. Smith MJ, Hayakawa Y, Takeda K, Yagita H (2002) New aspects of Natural-Killer-cell surveillance and therapy of cancer. Nat Rev Cancer 2:850-861 (Pubitemid 37328903)
24. Ruggeri L, Capanni M, Urbani E, Perruccio K, Shlomchik WD, Tosti A, Posati S, Rogaia D, Frassoni F, Martelli MF, Velardi A (2002) Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 295:2097-2100 (Pubitemid 34229476)
25. Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S (2008) Functions of natural killer cells. Nat Immunol 9:503-510 (Pubitemid 351560519)
26. Maccalli C, Scaramuzza S, Parmiani G (2009) TNK cells (NKG2D+ CD8+ or CD4+ T lymphocytes) in the control of human tumors. Cancer Immunol Immunother 58:801-807
27. Burke S, Lakshmikanth T, Colucci F, Carbone E (2010) New views on natural killer cell-based immunotherapy for melanoma treatment. Trends Immunol 31:339-345
28. Curiel TJ (2007) Tregs and rethinking cancer immunotherapy. J Clin Invest 117:1167-1174 (Pubitemid 46718401)
29. Quiao M, Thornton AM, Shevach EM (2007) CD4+ CD25+ regulatory T cells render naïve CD4+ CD25-cells anergic and suppressive. Immunology 120:447-455 (Pubitemid 46365018)
30. Ebert LM, Tan BS, Browning J, Svobodovna S, Russel SE, Kirkpatrick N Gedye C, Moss D, Ng SP, MacGregor D, Davis ID, Cebon J, Chen W (2008) The regulatory T cell-associated transcription factor FoxP3 is expressed by tumor cells. Cancer Res 68:3001-3009 (Pubitemid 351556301)
31. Yamamoto M, Kamigaki T, Yamashita K, Hori Y, Hasegawa H, Kuroda D, Moriyama H, Nagata M, Ku Y, Kuroda Y (2009) Enhancement of anti-tumor immunity by high levels of Th1 and Th17 with a combination of dendritic cells fusion hybrids and regulatory T cell depletion in pancreatic cancer. Oncol Rep 22:337-343
32. Zou W, Chen L (2008) Inhibitory B7-family molecules in the tumours microenvironment. Nat Rev Immunol 8:467-477 (Pubitemid 351733418)
33. Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, Liu YJ, Pulendran B, Palucka K (2000) Immunobiology of dendritic cells. Annu Rev Immunol 18:767-811 (Pubitemid 30365397)
34. Steinman RM (2003) Some interface of dendritic cell biology. APMIS 111:675-697 (Pubitemid 37130017)
35. Shortman K, Liu YJ (2002) Mouse and human dendritic cells subtypes. Nat Rev Immunol 2:151-161 (Pubitemid 37336516)
36. Ardavin C, Martinez del Hoyo G, Martin P, Anjuere F, Arias CF, Marin AR, Ruiz S, Parillas H, Hernandez V (2001) Origin and differentiation of dendritic cells. Trends Immunol 22:691-700 (Pubitemid 34008606)
37. Ferrari S, Malugani F, Rovati B, Porta C, Riccardi A, Danova M (2005) Flow cytometric analysis of circulating dendritic cell subsets and intracellular cytokine production in advanced breast cancer patients. Oncol Rep 14:113-120
38. Eksioglu EA, Eisen S, Reddy V (2010) Dendritic cells as therapeutic agents against cancer. Front Biosci 15:321-347
39. Rovati B, Mariucci S, Manzoni M, Bencardino K, Danova M (2008) Flow cytometric detection of circulating dendritic cells in healthy subjects. EJH 52:45-52
40. Gottfried E, Kreutz M, Mackensen A (2007) Tumor-induced modulation of dendritic cell function. Cytokine Growth Factor Rev 19:65-77
41. Ye F, Yu Y, Hu Y, Lu W, Xie X (2010) Alterations of dendritic cells subsets in the peripheral circulation of patients with cervical carcinoma. J Exp Clin Cancer Res 29:78
42. McCoy JL, Rucker R, Petros JA (2000) Cell-mediated immunity to tumor associated antigens is a better predictor of survival in early stage breast cancer than stage, grade or lymph node status. Breast Cancer Res Treat 60:227-234 (Pubitemid 30440538)
43. Mackall CL (2000) T-Cell Immunodeficiency following cytotoxic antineoplastic therapy: A review. Stem Cell 18:10-18 (Pubitemid 30064888)
44. Collova E, Rovati B, Grasso D, Bencardino K, Manzoni M, Danova M (2008) Effect of peg-filgrastim supported dose-dense adjuvant chemotherapy on the peripheral blood leukocyte phenotype in breast cancer patients. Mol Med Rep. doi:10.3892/ mmr-00000000
45. Komada Y, Zhang SL, Zhou YW, Hanada M, Shibata T, Azuma E, Sakurai M (1992) Cellular immunosuppression in children with acute lymphoblastic leukemia: Effect of consolidation chemotherapy. Cancer Immunol Immunother 35:271-276
46. Ageitos AG, Varney ML, Bierman PJ, Vose JM, Warkentin PI, Talmadge JE (1999) Comparison of monocyte-dependent T cell inhibitory activity in GM-CSF vs G-CSF mobilized PSC products. Bone Marrow Transplant 23:63-69 (Pubitemid 29050180)
47. Ino K, Singh RK, Talmadge JE (1997) Monocytes from mobilized stem cells inhibit T cell function. J Leukoc Biol 61:583-591 (Pubitemid 27234455)
48. Citron ML, Berry DA, Cirrincione C, Hudis C, Winer EP, Gradishar WJ, Davidson NE, Martino S, Livingston R, Ingle JN, Perez EA, Carpenter J, Hurd D, Holland JF, Smith BL, Sartor CI, Leung EH, Abrams J, Schilsky RL, Muss HB and Norton L (2003) Randomized trial of dose-dense versus conventionally schedules and sequential versus concurrent combination chemotherapy as post operative adjuvant treatment of node-positive primary breast cancer: First report of Intergroup Trial C9741/cer and Leukemia Group B Trial 9741. J Clin Oncol 21:1431-1439 (Pubitemid 46594092)
49. Tayebi H, Kuttler F, Saas P, Lienard A, Petracca B, Lapierre V, Ferrand C, Fest T, Cahn J, Blaise D, Kuentz M, Hervé P, Tiberghien P, Robinet E (2001) Effect of granulocyte colonystimulating factor mobilization on phenotypical and functional properties of immune cells. Exp Hematol 29:458-470 (Pubitemid 32297670)
50. Valente JF, Alexander JW, Li BG, Noel JG, Custer DA, Ogle JD, Ogle CK (2002) Effect of in vivo infusion of granulocyte colony-stimulating factor on immune function. Shock 17:23-29
51. Rutella S, Pierelli L, Bonanno G, Sica S, Ameglio F, Capoluongo E, Mariotti A, Scambia G, d'Onofrio G, Leone G (2002) Role for granulocyte colony-stimulating factor in the generation of human T regulatory type 1 cells. Blood 100:2562-2571
52. Sewell HF, Halbert CF, Robins RA, Galvin A, Chan S, Blamey RW (1993) Chemotherapy induced differential changes in lymphocyte subsets and natural killer cell function in patients with advanced breast-cancer disease. Int J Cancer 55:735-738 (Pubitemid 23354885)
53. Sara E, Kotsakis A, Souklakos J, Kourousis C, Kakolyris S, Mavromanolakis E, Vlachonicolis J, Georgoulias V (1999) Postchemotherapy lymphopoiesis in patients with solid tumors is characterized by CD4+ cell proliferation. Anticancer Res 19:471-476 (Pubitemid 29168279)
54. Schroeder W, Vering A, Stegmuller M, Strohmeier R (1997) Lymphocytes subsets in patients with ovarian and breast cancer. Eur J Gynaecol Oncol 18:474-479
55. Melichar B, Touskova M, Dvorak J, Jandik P, Kopecky (2001) The peripheral blood leukocyte phenotype in patients with breast cancer: Effect of doxorubicin/paclitaxel combination chemotherapy. Immunopharmacol Immunotoxicol 23:163-173 (Pubitemid 32532044)
56. Ferrari S, Rovati B, Cucca L, Scarabelli C, Presti M, Beccaria C, Collovà E, Porta C, Danova M (2002) Impact of topotecanbased chemotherapy on the immune system of advanced ovarian cancer patients: An immunophenotypic study. Oncol Rep 9:1107-1113
57. Chan OT, Yang KX (2001) The immunological effects of taxanes. Cancer Immunol Immunother 49:181-185 (Pubitemid 30484824)
58. Michael A, Pandha HS (2003) Renal cel carcinoma: Tumour markers, T-cell epitopes, and potential for new therapies. Lancet Oncol 4:215-223 (Pubitemid 36503319)
59. Caignard A, Guillard M, Gaudin C, Escudier B, Dietrich TF (1996) In situ demonstration of renal cell carcinoma-specific T-cell clones. Int J Cancer 66:564-570 (Pubitemid 26176774)
60. Brouwenstijn N, Gaugler B, Kruse KM, van der Spek CW, Mulder A, Osanto S, van den Eynde BJ, Schrier PI (1996) Renal cell carcinoma-specific lysis by cytotoxic T-lymphocyte clones isolated from peripheral blood lymphocytes and tumor-infiltrating lymphocytes. Int J Cancer 68:177-182 (Pubitemid 26380119)
61. Van den Hove LE, Van Gool SW, Van Poppel H, Baert L, Coorevits L, Van Damme B, Ceuppens JL (1997) Phenotype, cytokine production and cytolityc capacity of fresh (uncultured) tumor infiltrating T lymphocytes in human renal cell carcinoma. Clin Exp Immunol 109:501-509 (Pubitemid 27402320)
62. Schwaab T, Schned AR, Heaney JA, Cole BF, Atzpodien J, Wittke F, Ernastoff MS (1999) In vivo description of dendritic cells in human renal cell carcinoma. J Urol 162:291-292
63. Kudo D, Rayman P, Horton C, Cathcart MK, Bukowski RM, Thornton M, Tannenbaum C, Finke JH (2003) Gangliosides expressed by the renal cell carcinoma cell line SK-RC-45 are involved in tumor induced apoptosis of T cells. Cancer Res 63:1676-1683 (Pubitemid 36373661)
64. Rayman P, Uzzo RG, Kolenko V, Bloom T, Cathcart MK, Molto L, Novick AC, Bukowski RM, Hamilton T, Finke JH (2000) Tumor-induced dysfunction in interleukin-2 production and interleukin-2 receptor signaling: A mechanism of immunescape. Cancer J Sci Am 6:S81-S87
65. Finke JH, Rayman P, George R, Tannenbaum CS, Kolenko V, Uzzo R, Novick AC, Bukowski RM (2001) Tumor-induced sensitivity to apoptosis in T cells from patients with renal cell carcinoma: Role of nuclear factor-kappaB. Clin Cancer Res 7:940s-946s (Pubitemid 33600949)
66. Nagler A, Lanier LL, Cwirla S, Phillips JH (1989) Comparative studies of human FcRIII-positive and negative natural killer cells. J Immunol 143:3183-3191 (Pubitemid 20010143)
67. Smyth MJ, Cretney E, Kelly JM, Westwood JA, Street SE, Yagita H, Takeda K, van Dommelen SL, Degli-Esposti MA, Hayakawa Y (2005) Activation of NK cell cytotoxicity. Mol Immunol 42:501-510 (Pubitemid 39655961)
68. Porta C, Bonomi L, Lillaz B, Paglino C, Rovati B, Imarisio I, Morbini P, Villa C, Danova M, Mensi M, Rovereto B (2007) Renal cell carcinoma-induced immunosuppression: An immunophenotypic study of lymphocyte subpopulation and circulating dendritic cells. Anticancer Res 27:165-174 (Pubitemid 46363327)
69. Mackall CL, Fleisher TA, Brown MR, Andrich MP, Chen CC, Feuerstein IM, Magrath IT, Wexler LH, Dimitrov DS, Gress RE (1997) Distinctions between CD8+ and CD4+ T-cell regenerative pathways result in prolonged T cell subset imbalance after intensive chemotherapy. Blood 89:3700-3707 (Pubitemid 27227093)
70. Small TN, Keever CA, Weiner-Fedus S, Heller G, O'Reilly RJ, Flomenberg N (1990) B-cell differentiation following autologous, conventional or T cell depleted bone marrow transplantation: A recapitulation of normal B cell ontogeny. Blood 76:1647-1656 (Pubitemid 20364032)
71. Storek J, Saxon A (1992) Reconstitution of B cell immunity following bone marrow transplantation. Bone Marrow Transplant 9:395-408
72. Sozzani S, Rusnati M, Riboldi E, Mitola S, Presta M (2007) Dendritic cell-endothelial cell cross-talk in angiogenesis. Trends Immunol 28:385-392 (Pubitemid 47385377)
73. Murdoch C, Muthana M, Coffelt SB, Lewis CE (2008) The role of myeloid cells in the promotion of tumour angiogenesis. Nature 8:618-631
74. Della Porta M, Danova M, Rigolin GM, Brugnatelli S, Rovati B, Tronconi C, Fraulini C, Russo Rossi A, Riccardi A, Castoldi G (2005) Dendritic cells and vascular endothelial growth factor in colorectal cancer: Correlations with clinicobiological findings. Oncology 68:276-284 (Pubitemid 41158987)
75. Gottfried E, Kreutz M, Haffner S, Holler E, Iacobelli M, Andreesen R, Eissner G (2007) Differentiation of human tumourassociated dendritic cells into endothelial-like cells: An alternative pathway of tumour angiogenesis. Scand J Immunol 65:329-335 (Pubitemid 46481100)
76. Fernandez Pujol B, Lucibello FC, Zuzarte M, Lütjens P, Müller R, Havemann K (2001) Dendritic cells derived from peripheral monocytes express endothelial markers and in the presence of angiogenic growth factors differentiate into endothelial-like cells. Eur J Cell Biol 80:99-110 (Pubitemid 32098116)
77. Bria E, Di Maio M, Carlini P, Cuppone F, Giannarelli D, Cognetti F, Milella M (2009) Targeting targeted agents: Open issues for clinical trial design. J Exp Clin Cancer Res 28:66-72
78. Folkamn J (1971) Tumor angiogenesis therapeutic implications. N Engl J Med 285:1182-1186
79. Ellis LM, Hicklin DJ (2008) VEGF-targeted therapy: Mechanisms of anti-tumour activity. Nat Rev Cancer 8:579-591
80. Jain RK (2005) Normalization of tumor vasculature: An emerging concept in antiangiogenic therapy. Science 307:58-62 (Pubitemid 40093472)
81. Miller K, Wang M, Gralow J, Dickler M, Cobleigh M, Perez EA, Shenkier T, Cella D, Davidson NE (2007) Paclitaxel plus bevacizumab versus paclitaxel alone for metastatic breast cancer. N Engl J Med 357:2666-2676
82. Sandler A, Gray R, Perry MC, Brahmer J, Schiller JH, Dowlati A, Lilenbaum R, Johnson DH (2006) Paclitaxel-carboplatin alone or with bevacizumab for non-small-cell lung cancer. N Engl J Med 355:2542-2550 (Pubitemid 44917502)
83. Escudier B, Pluzanska A, Koralewski P, Ravaud A, Bracarda S, Szczylik C, Chevreau C, Filipek M, Melichar B, Bajetta E, Gorbunova V, Bay JO, Bodrogi I, Jagiello-Gruszfeld A, Moore N (2007) Bevacizumab plus interferon alfa-2a for treatment of metastatic renal cell carcinoma: A randomised, double-blind phase III trial. Lancet 370:2103-2111 (Pubitemid 350296300)
84. Loupakis F, Bria E, Vaccaro V, Cuppone F, Milella M, Carlini P, Cremolini C, Salvatore L, Falcone A, Muti P, Sperduti I, Giannarelli D, Cognetti F (2010) Magnitude of benefit of the addition of bevacizumab to first-line chemotherapy for metastatic colorectal cancer: Meta-analysis of randomized clinicals trials. J Exp Clin Cancer Res 29:58
85. Kerbel RS (2008) Tumor angiogenesis. N Engl J Med 358:2039-2049 (Pubitemid 351656458)
86. Ebos JM, Lee CR, Cruz-Munoz W, Bjarnason GA, Christensen JG, Kerbel RS (2009) Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 15:232-239
87. Almand B, Resser JR, Lindman B, Nadaf S, Clark JI, Kwon ED, Carbone DP, Gabrilovich DI (2000) Clinical significance of defective dendritic cell differentiation in cancer. Clin Canc Res 6:1755-1766 (Pubitemid 30305068)
88. Ohm JE, Carbone DP (2002) Immune disfunction in cancer patients. Oncology 16:11-18
89. Dikov MM, Ohm JE, Ray N, Tchekneva EE, Burlison J, Moghanaki D, Nadaf S, Carbone DP (2005) Differential roles of vascular endothelial growth factor receptors 1 and 2 in dendritic cell differentiation. J Immunol 174:215-222 (Pubitemid 40007407)
90. Oyama T, Ran S, Ishida T, Nadaf S, Kerr L, Carbone DP, Gabrilovich DI (1998) Vascular endothelial growth factor affects dendritic cell maturation through the inhibition of nuclear factor-kappa B activation in hemopoietic progenitor cells. J Immunol 160:1224-1232 (Pubitemid 28093419)
91. Ohm JE, Shurin MR, Esche C, Lotze MT, Carbone DP, Gabrilovich DI (1999) Effect of vascular endothelial growth factor and FLT3 ligand on dendritic cell generation in vivo. J Immunol 163:3260-3268 (Pubitemid 29431827)
92. Ohm JE, Carbone DP (2001) VEGF as a mediator of tumorassociated immunodeficiency. Immunol Res 23:263-272
93. Laxmanan S, Robertson SW, Wang E, Lau JS, Briscoe DM, Mukhopadhyay D (2005) Vascular endothelial growth factor impairs the functional ability of dendritic cells through Id pathways. Biochem Biophys Res Commun 334:193-198 (Pubitemid 40978525)
94. Mimura K, Kono K, Takahashi A, Kawaguchi Y, Fujii H (2007) Vascular endothelial growth factor inhibits the function of human mature dendritic cell mediated by VEGF receptor 2. Cancer Immunol Immunother 56:761-770 (Pubitemid 46723581)
95. Gabrilovich DI, Chen HL, Girgis KR, Cunningham HT, Meny GM, Nadaf S, Kavanaugh D, Carbone DP (1996) Production of vascular endothelial growth factor by human tumors inhibits the functional maturation of dendritic cells. Nat Med 2:1096-1103 (Pubitemid 26338628)
96. Gabrilovich D (1998) Vascular endothelial growth factors inhibits the development of dendritic cells and dramatically affects the differentiation of multiple hematopoietic lineages in vivo. Blood 92:4150-4166 (Pubitemid 28544331)
97. Saito H, Tsujitani S, Ikeguchi M, Maeta M, Kaibara N (1998) Relationship between the expression of vascular endothelial growth factor and the density of dendritic cells in gastric adenocarcinoma tissue. Br J Cancer 1998(78):1573-1577 (Pubitemid 28550041)
98. Fan XH, Han BH, Dong QG, Sha HF, Bao GL, Liao ML (2003) Vascular endothelial growth factor inhibits dendritic cells from patients with non-small cell lung carcinoma. Zhonghua Jie He He Hu Xi Za Zhi 26:539-543
99. Lissoni P, Malugani F, Bonfanti A, Bucovec R, Secondino S, Brivio F, Ferrari-Bravo A, Ferrante R, Vigoré L, Rovelli F, Mandalà M, Viviani S, Fumagalli L, Gardani GS (2001) Abnormally enhanced blood concentrations of vascular endothelial growth factor (VEGF) in metastatic cancer patients and their relation to circulating dendritic cells, IL-12 and endothelin-1. J Biol Regul Homeostatic Agents 15:140-144 (Pubitemid 32717550)
100. Tsukayama S, Omura K, Yoshida K, Tanaka Y, Watanabe G (2005) Prognostic value of CD83-positive mature dendritic cells and their relation to vascular endothelial growth factor in advanced human gastric cancer. Oncol Rep 14:369-375
101. Fricke I, Mirza N, Dupont J, Lockhart C, Jackson A, Lee JH, Sosman JA, Gabrilovich DI (2007) Vascular endothelial growth factor-trap overcomes defects in dendritic cell differentiation but does not improve antigen-specific immune responses. Clin Cancer Res 13:4840-4848 (Pubitemid 47298146)
102. Osada T, Chong G, Tansik R, Hong T, Spector N, Kumar R, Hurwitz HI, Dev I, Nixon AB, Lyerly HK, Clay T, Morse MA (2008) The effect of anti-VEGF therapy on immature myeloid cell and dendritic cells in cancer patients. Cancer Immunol Immunother 57:1115-1124
103. Manzoni M, Rovati B, Ronzoni M, Loupakis F, Mariucci S, Ricci V, Gattoni E, Salvatore L, Villa E, Tinelli C, Danova M (2010) Imunological effects of bevacizumab-based treatment in metastatic colorectal cancer. Oncology. doi:10.1159/000320609
104. Ohm JE, Gabrilovich DI, Sempowski GD, Kisseleva E, Parman KS, Nadaf S, Carbone DP (2003) VEGF inhibits T-cell development and may contribute to tumor-induced immune suppression. Blood 101:4878-4886 (Pubitemid 36857749)
105. Gottfried E, Kreutz M, Mackensen A (2008) Tumor-induced modulation of dendritic cell function. Cytokine Growth Factor Rev 19:65-77 (Pubitemid 351200062)
106. Gabrilovich DI, Corak J, Ciernik IF, Kavanaugh D, Carbone DP (1997) Decreased antigen presentation by dendritic cells in patients with breast cancer. Clin Cancer Res 3:483-490 (Pubitemid 27158075)