Tumor induced inactivation of natural killer cell cytotoxic function; implication in growth, expansion and differentiation of cancer stem cells

Journal of Cancer

Volumn 2, Issue 1, 2011, Pages 443-457

  Jewett, Anahid ^a   Tseng, Han Ching ^a  

^a UCLA SCHOOL OF DENTISTRY   (United States)

Author keywords

Apoptosis; Cancer stem cells; Differentiation; NF B; Nk

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN;

CANCER STEM CELL; CELL DIFFERENTIATION; EMBRYO; EMBRYONIC STEM CELL; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; MICROENVIRONMENT; MONOCYTE; MOUTH CARCINOMA; NATURAL KILLER CELL; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; PLURIPOTENT STEM CELL; REVIEW; SQUAMOUS CELL CARCINOMA; TISSUE REGENERATION; TISSUE REPAIR; TUMOR GROWTH; TUMOR RESISTANCE;

EID: 84868332376     PISSN: None     EISSN: 18379664     Source Type: Journal    
DOI: 10.7150/jca.2.443     Document Type: Review

References (126)

1. Hernandez G, et al. Rapid progression from oral leukoplakia to carcinoma in an immunosuppressed liver transplant recipient. Oral Oncol, 2003. 39(1): 87-90.
2. Bilinska-Pietraszek E, et al. [A case of tongue neoplasm in a 15-year old patient treated with immunosuppressants for renal insufficiency]. Otolaryngol Pol, 2001. 55(1): 95-7.
3. de Visscher JG, et al. Squamous cell carcinoma of the lower lip in renal-transplant recipients. Report of six cases. Int J Oral Maxillofac Surg, 1997. 26(2): 120-3.
4. King GN, et al. Increased prevalence of dysplastic and malignant lip lesions in renal-transplant recipients. N Engl Med J, 1995. 332(16): 1052-7.
5. van Zuuren E.J, et al. Carcinoma of the lip in kidney transplant recipients. J Am Acad Dermatol, 1998. 38(3): 497-9.
6. Bhatia S, et al. Solid cancers after bone marrow transplantation. J Clin Oncol, 2001. 19(2): 464-71.
7. Kolenko V, et al. Tumor-induced suppression of T lymphocyte proliferation coincides with inhibition of Jak3 expression and IL-2 receptor signaling: role of soluble products from human renal cell carcinomas. Immunol J, 1997. 159(6): 3057-67.
8. Mulder W.M, et al. cell receptor-zeta T and granzyme B expression in mononuclear cell infiltrates in normal colon mucosa and colon carcinoma. Gut, 1997. 40(1): 113-9.
9. Camp B.J, et al. In situ cytokine production by breast cancer tumor-infiltrating lymphocytes. Ann Surg Oncol, 1996. 3(2): 176-84.
10. Gimmi C.D, et al. Breast cancer-associated antigen, DF3/MUC1, induces apoptosis of activated human T cells. Nat Med, 1996. 2(12): 1367-70.
11. Bennett M.W, et al. The Fas counterattack in vivo: apoptotic depletion of tumor-infiltrating lymphocytes associated with Fas ligand expression by human esophageal carcinoma. Immunol J, 1998. 160(11): 5669-75.
12. Jewett A, Head C, and Cacalano N.A. Emerging mechanisms of immunosuppression in oral cancers. J Dent Res, 2006. 85(12): 1061-73.
13. Tanaka H, et al. Nonsteroidal anti-inflammatory drugs differentially regulate cytokine production in human lymphocytes: up-regulation of TNF, IFN-gamma and IL-2, in contrast to down-regulation of IL-6 production. Cytokine, 1995. 7(4): 372-9.
14. Miescher S, et al. Preferential clonogenic deficit of CD8-positive T-lymphocytes infiltrating human solid tumors. Cancer Res, 1988. 48(24 Pt 1): 6992-8.
15. Qin J, Han B, and Pang J. [The relationship between TIL from human primary hepatic carcinoma and prognosis]. Zhonghua Yi Xue Za Zhi, 1997. 77(3): 167-70.
16. Han X, et al. Tumor lymphocytes in patients with advanced ovarian cancer: changes during in vitro culture and implications for immunotherapy. Gynecol Oncol, 1997. 65(3): 391-8.
17. Aggarwal S and Pittenger M.F. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood, 2005. 105(4): 1815-22.
18. Selmani Z, et al. Human leukocyte antigen-G5 secretion by human mesenchymal stem cells is required to suppress lymphocyte T and natural killer function and to induce CD4+CD25highFOXP3+ regulatory T cells. Stem Cells, 2008. 26(1): 212-22.
19. Spaggiari G.M, et al. Mesenchymal stem cells inhibit natural killer-cell proliferation, cytotoxicity, and cytokine production: role of indoleamine 2,3-dioxygenase and prostaglandin E2. Blood, 2008. 111(3): 1327-33.
20. Jewett A and Bonavida B. Target-induced inactivation and cell death by apoptosis in a subset of human NK cells. Immunol J, 1996. 156(3): 907-15.
21. Jewett A and Bonavida B. Target-induced anergy of natural killer cytotoxic function is restricted to the NK-target conjugate subset. Cell Immunol, 1995. 160(1): 91-7.
22. Nakagomi H, et al. Decreased expression of the signal-transducing zeta chains in tumor-infiltrating T-cells and NK cells of patients with colorectal carcinoma. Cancer Res, 1993. 53(23): 5610-2.
23. Rayet B and Gelinas C. Aberrant rel/nfkb genes and activity in human cancer. Oncogene, 1999. 18(49): 6938-47.
24. Teruel A, et al. Potential contribution of naive immune effectors to oral tumor resistance: role in synergistic induction of VEGF, IL-6, and IL-8 secretion. Cancer Immunol Immunother, 2008 Mar;57(3):359-66.
25. Tseng H.C, et al. Increased lysis of stem cells but not their differentiated cells by natural killer cells; de-differentiation or reprogramming activates NK cells. PLoS One. 2010;5(7): e11590.
26. Rioux S, et al. Isolation and characterization of LPS mutants of Actinobacillus pleuropneumoniae serotype 1. Curr Microbiol, 1997. 35(3): 139-44.
27. Opitz O.G, et al. A mouse model of human oral-esophageal cancer. J Clin Invest, 2002. 110(6): 761-9.
28. Jewett A, et al. Inhibition of nuclear factor kappa B (NFkappaB) activity in oral tumor cells prevents depletion of cells NK and increases their functional activation. Cancer Immunol Immunother, 2006. 55(9): 1052-63.
29. Jewett A, et al. Cytokine dependent inverse regulation of CD54 (ICAM1) and major histocompatibility complex class I antigens by nuclear factor kappaB in HEp2 tumor cell line: effect on the function of natural killer cells. Hum Immunol, 2003. 64(5): 505-20.
30. Karin M, et al. NF-kappaB in cancer: from innocent bystander to major culprit. Nat Rev Cancer, 2002. 2(4): 301-10.
31. Burnet F.M. The concept of immunological surveillance. Prog Exp Tumor Res, 1970. 13: 1-27.
32. Burnet F.M. Immunological surveillance in neoplasia. Transplant Rev, 1971. 7: 3-25.
33. Burnet F.M. Implications of immunological surveillance for cancer therapy. Isr J Med Sci, 1971. 7(1): 9-16.
34. Dunn G.P, et al. Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol, 2002. 3(11): 991-8.
35. Dunn G.P, Old L.J, and Schreiber R.D. The immunobiology of cancer immunosurveillance and immunoediting. Immunity, 2004. 21(2): 137-48.
36. Whiteside T.L, et al. Evidence for local and systemic activation of immune cells by peritumoral injections of interleukin 2 in patients with advanced squamous cell carcinoma of the head and neck. Cancer Res, 1993. 53(23): 5654-62.
37. Rivoltini L, et al. In vivo interleukin 2-induced activation of lymphokine-activated killer cells and tumor cytotoxic T-cells in cervical lymph nodes of patients with head and neck tumors. Cancer Res, 1990. 50(17): 5551-7.
38. Cortesina G, et al. Treatment of recurrent squamous cell carcinoma of the head and neck with low doses of interleukin-2 injected perilymphatically. Cancer, 1988. 62(12): 2482-5.
39. Whiteside T.L, et al. Antitumor effects of cytolytic T lymphocytes (CTL) and natural killer (NK) cells in head and neck cancer. Anticancer Res, 1996. 16(4C): 2357-64.
40. Zoller M, Goodman M.L, and Cummings C.W. Guidelines for prognosis in head and neck cancer with nodal metastasis. Laryngoscope, 1978. 88(1 Pt 1): 135-40.
41. Hayry P and Totterman T.H. Cytological and functional analysis of inflammatory infiltrates in human malignant tumors. I. Composition of the inflammatory infiltrates. Eur Immunol J, 1978. 8(12): 866-71.
42. Itoh K, Tilden A.B, and Balch C.M. Interleukin 2 activation of cytotoxic T-lymphocytes infiltrating into human metastatic melanomas. Cancer Res, 1986. 46(6): 3011-7.
43. Marrogi A.J, et al. Study of tumor infiltrating lymphocytes and transforming growth factor-beta as prognostic factors in breast carcinoma. Int Cancer J, 1997. 74(5): 492-501.
44. Hartveit F, Breast cancer: poor short-term prognosis in cases with moderate lymphocyte infiltration at the tumour edge: a preliminary report. Oncol Rep, 1998. 5(2): 423-6.
45. Wada Y, et al. Clinicopathological study on hepatocellular carcinoma with lymphocytic infiltration. Hepatology, 1998. 27(2): 407-14.
46. Clemente C.G, et al. Prognostic value of tumor infiltrating lymphocytes in the vertical growth phase of primary cutaneous melanoma. Cancer, 1996. 77(7): 1303-10.
47. Bethwaite P.B, et al. Infiltration by immunocompetent cells in early stage invasive carcinoma of the uterine cervix: a prognostic study. Pathology, 1996. 28(4): 321-7.
48. Coca S, et al. The prognostic significance of intratumoral natural killer cells in patients with colorectal carcinoma. Cancer, 1997. 79(12): 2320-8.
49. Thomas D.W, et al. Inflammatory cell infiltrate associated with primary and transplanted tumours in an inbred model of oral carcinogenesis. J Oral Pathol Med, 1995. 24(1): 23-31.
50. Schantz S.P, et al. Natural killer cell activity and head and neck cancer: a clinical assessment. J Natl Cancer Inst, 1986. 77(4): 869-75.
51. Hoffmann T.K, et al. Frequencies of tetramer+ T cells specific for the wild-type sequence p53(264-272) peptide in the circulation of patients with head and neck cancer. Cancer Res, 2002. 62(12): 3521-9.
52. Reichert T.E, et al. Signaling abnormalities, apoptosis, and reduced proliferation of circulating and tumor-infiltrating lymphocytes in patients with oral carcinoma. Clin Cancer Res, 2002. 8(10): 3137-45.
53. Jewett A, et al. Rapid and potent induction of cell death and loss of NK cell cytotoxicity against oral tumors by F(ab')2 fragment of anti-CD16 antibody. Cancer Immunol Immunother, 2008. 57(7): 1053-66.
54. Romero-Reyes M, et al. Potent induction of TNF-alpha during interaction of immune effectors with oral tumors as a potential mechanism for the loss of cell viability NK and function. Apoptosis, 2007 Nov;12(11):2063-75.
55. Parham P, et al. Primate-specific regulation of natural killer cells. J Med Primatol. 2010;39(4): 194-212.
56. Jewett A, Cavalcanti M, and Bonavida B. Pivotal role of endogenous TNF-alpha in the induction of functional inactivation and apoptosis in NK cells. Immunol J, 1997. 159(10): 4815-22.
57. Kojima M, et al. Follicular lymphoma of the salivary gland: a clinicopathological and molecular study of six cases. Int J Surg Pathol, 2001. 9(4): 287-93.
58. Yang F.C, et al. CD27/CD70 interaction directly induces natural killer cell killing activity. Immunology, 1996. 88(2): 289-93.
59. Yang L, et al. Cancer-associated immunodeficiency and dendritic cell abnormalities mediated by the prostaglandin EP2 receptor. J Clin Invest, 2003. 111(5): 727-35.
60. Thomas G.R, et al. Cytokines IL-1 alpha, IL-6, and GM-CSF constitutively secreted by oral squamous carcinoma induce down-regulation of CD80 costimulatory molecule expression: restoration by interferon gamma. Cancer Immunol Immunother, 2004. 53(1): 33-40.
61. Rhodus N.L, et al. NF-kappaB dependent cytokine levels in saliva of patients with oral preneoplastic lesions and oral squamous cell carcinoma. Cancer Detect Prev, 2005. 29(1): 42-5.
62. Diehl S and Rincon M. The two faces of IL-6 on Th1/Th2 differentiation. Mol Immunol, 2002. 39(9): 531-6.
63. Menetrier-Caux C, et al. Inhibition of the differentiation of dendritic cells from CD34(+) progenitors by tumor cells: role of interleukin-6 and macrophage colony-stimulating factor. Blood, 1998. 92(12): 4778-91.
64. Gabrilovich D, et al. Vascular endothelial growth factor inhibits the development of dendritic cells and dramatically affects the differentiation of multiple hematopoietic lineages in vivo. Blood, 1998. 92(11): 4150-66.
65. Chang C.C, et al. Tolerization of dendritic cells by T(S) cells: the crucial role of inhibitory receptors ILT3 and ILT4. Nat Immunol, 2002. 3(3): 237-43.
66. Vuk-Pavlovic S. Rebuilding immunity in cancer patients. Blood Cells Mol Dis, 2008. 40(1): 94-100.
67. Greten T.F, Manns M.P, and Korangy F. Myeloid derived suppressor cells in human diseases. Int Immunopharmacol. 2011;11(7): 802-6.
68. Coffelt S.B, Hughes R, and Lewis C.E. Tumor-associated macrophages: effectors of angiogenesis and tumor progression. Biochim Biophys Acta, 2009. 1796(1): 11-8.
69. Mantovani A and Sica A. Macrophages, innate immunity and cancer: balance, tolerance, and diversity. Curr Opin Immunol. 2010; 22(2): 231-7.
70. Yaguchi T, et al. The mechanisms of cancer immunoescape and development of overcoming strategies. Int J Hematol. 2011;93(3): 294-300.
71. Jewett A, et al. Strategies to rescue mesenchymal stem cells (MSCs) and dental pulp stem cells (DPSCs) from NK cell mediated cytotoxicity. PLoS One. 2010;5(3): e9874.
72. Wang T, et al. Regulation of the innate and adaptive immune responses by Stat-3 signaling in tumor cells. Nat Med, 2004. 10(1): 48-54.
73. Murakami J, et al. Effects of histone deacetylase inhibitor FR901228 on the expression level of telomerase reverse transcriptase in oral cancer. Cancer Chemother Pharmacol, 2005. 56(1): 22-8.
74. Murakami J, et al. Influence of CpG island methylation status in O6-methylguanine-DNA methyltransferase expression of oral cancer cell lines. Oncol Rep, 2004. 12(2): 339-45.
75. Abdulkarim B, et al. Antiviral agent Cidofovir restores p53 function and enhances the radiosensitivity in HPV-associated cancers. Oncogene, 2002. 21(15): 2334-46.
76. Pasparakis M, et al. TNF-mediated inflammatory skin disease in mice with epidermis-specific deletion of IKK2. Nature, 2002. 417(6891): 861-6.
77. Berlin A.L, Paller A.S, and Chan L.S. Incontinentia pigmenti: a review and update on the molecular basis of pathophysiology. J Am Acad Dermatol, 2002. 47(2): 169-87.
78. Greten F.R, et al. IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell, 2004. 118(3): 285-96.
79. Greten F.R and Karin M. The IKK/NF-kappaB activation pathway-a target for prevention and treatment of cancer. Cancer Lett, 2004. 206(2): 193-9.
80. Seitz C.S, et al. Alterations in NF-kappaB function in transgenic epithelial tissue demonstrate a growth inhibitory role for NF-kappaB. Proc Natl Acad Sci U S A, 1998. 95(5): 2307-12.
81. van Hogerlinden M, et al. Squamous cell carcinomas and increased apoptosis in skin with inhibited Rel/nuclear factor-kappaB signaling. Cancer Res, 1999. 59(14): 3299-303.
82. van Hogerlinden M, et al. Characterization of the progressive skin disease and inflammatory cell infiltrate in mice with inhibited NF-kappaB signaling. J Invest Dermatol, 2004. 123(1): 101-8.
83. Oka N, et al. VEGF promotes tumorigenesis and angiogenesis of human glioblastoma stem cells. Biochem Biophys Res Commun, 2007. 360(3): 553-9.
84. Inagaki A, et al. Long-term maintenance of brain tumor stem cell properties under at non-adherent and adherent culture conditions. Biochem Biophys Res Commun, 2007. 361(3): 586-92.
85. Soeda A, et al. Epidermal growth factor plays a crucial role in mitogenic regulation of human brain tumor stem cells. J Biol Chem, 2008. 283(16): 10958-66.
86. Rahaman S.O, et al. Inhibition of constitutively active Stat3 suppresses proliferation and induces apoptosis in glioblastoma multiforme cells. Oncogene, 2002. 21(55): 8404-13.
87. Hu P.F, et al. Natural killer cell immunodeficiency in HIV disease is manifest by profoundly decreased numbers of CD16+CD56+ cells and expansion of a population of CD16dimCD56-cells with low lytic activity. J Acquir Immune Defic Syndr Hum Retrovirol, 1995. 10(3): 331-40.
88. Lai P, et al. Alterations in expression and function of signal-transducing proteins in tumor-associated T and natural killer cells in patients with ovarian carcinoma. Clin Cancer Res, 1996. 2(1): 161-73.
89. Kuss I, et al. Clinical significance of decreased zeta chain expression in peripheral blood lymphocytes of patients with head and neck cancer. Clin Cancer Res, 1999. 5(2): 329-34.
90. Patankar M.S, et al. Potent suppression of natural killer cell response mediated by the ovarian tumor marker CA125. Gynecol Oncol, 2005 Dec;99(3):704-13.
91. Mandelboim O, et al. Human CD16 as a lysis receptor mediating direct natural killer cell cytotoxicity. Proc Natl Acad Sci U S A, 1999. 96(10): 5640-4.
92. Jewett A, et al. Differential secretion of TNF-alpha and IFN-gamma by human peripheral blood-derived subsets NK and association with functional maturation. J Clin Immunol, 1996. 16(1): 46-54.
93. Ortaldo J.R, Mason A.T, and O'Shea J.J. Receptor-induced death in human natural killer cells: involvement of CD16. J Exp Med, 1995. 181(1): 339-44.
94. Azzoni L, et al. Ligand binding to Fc gamma R induces c-myc-dependent apoptosis in IL-2-stimulated NK cells. Immunol J, 1995. 154(2): 491-9.
95. Jewett A, et al. Coengagement of CD16 and CD94 receptors mediates secretion of chemokines and induces apoptotic death of naive natural killer cells. Clin Cancer Res, 2006. 12(7 Pt 1): 1994-2003.
96. Bonavida B, Lebow L.T, and Jewett A. Natural killer cell sub-sets: maturation, differentiation and regulation. Nat Immun, 1993. 12(4-5): 194-208.
97. Bonavida B, et al. Qualitative and quantitative analysis of sub-populations of cytotoxic effector cells by flow cytometry. J Lipid Mediat Cell Signal, 1994. 9(1): 19-25.
98. Jewett A and Bonavida B. Activation of the human immature natural killer cell subset by IL-12 and its regulation by endogenous TNF-alpha and IFN-gamma secretion. Cell Immunol, 1994. 154(1): 273-86.
99. Jewett A and Bonavida B. Interferon-alpha activates cytotoxic function but inhibits interleukin-2-mediated proliferation and tumor necrosis factor-alpha secretion by immature human natural killer cells. J Clin Immunol, 1995. 15(1): 35-44.
100. Jewett A and Bonavida B. MHC-Class I antigens regulate both the function and the survival of human peripheral blood NK cells: role of endogenously secreted TNF-alpha. Clin Immunol, 2000. 96(1): 19-28.
101. Cooper M.A, Fehniger T.A, and Caligiuri M.A. The biology of human natural killer-cell subsets. Trends Immunol, 2001. 22(11): 633-40.
102. Nemeth E, Baird A.W, and O'Farrelly C. Microanatomy of the liver immune system. Semin Immunopathol, 2009. 31(3): 333-43.
103. Bubenik J, MHC class I down-regulation: tumour escape from immune surveillance? (review). Int Oncol J, 2004. 25(2): 487-91.
104. Curiel T.J, et al. Blockade of B7-H1 improves myeloid dendritic cell-mediated antitumor immunity. Nat Med, 2003. 9(5): 562-7.
105. Jewett A, et al. Inhibition of nuclear factor kappa B (NFkappaB) activity in oral tumor cells prevents depletion of cells NK and increases their functional activation. Cancer Immunol Immunother, 2005;: 1-12.
106. Lutz C.T and Kurago Z.B. Human leukocyte antigen class I expression on squamous cell carcinoma cells regulates natural killer cell activity. Cancer Res, 1999. 59(22): 5793-9.
107. Chen Z, et al. Expression of proinflammatory and proangiogenic cytokines in patients with head and neck cancer. Clin Cancer Res, 1999. 5(6): 1369-79.
108. Okada K, et al. Interactions between autologous CD4+ and CD8+ lymphocytes T and human squamous cell carcinoma of the head and neck. Cell Immunol, 1997. 177(1): 35-48.
109. Romano M, et al. Role of IL-6 and its soluble receptor in induction of chemokines and leukocyte recruitment. Immunity, 1997. 6(3): 315-25.
110. Woods K.V, et al. Interleukin-1 regulates interleukin-6 secretion in human oral squamous cell carcinoma in vitro: possible influence of p53 but not human papillomavirus E6/E7. Cancer Res, 1998. 58(14): 3142-9.
111. Bromberg J.F, et al. Stat3 as an oncogene. Cell, 1999. 98(3): 295-303.
112. Calo V, et al. STAT proteins: from normal control of cellular events to tumorigenesis. J Cell Physiol, 2003. 197(2): 157-68.
113. Grandis J.R, et al. Constitutive activation of Stat3 signaling abrogates apoptosis in squamous cell carcinogenesis in vivo. Proc Natl Acad Sci U S A, 2000. 97(8): 4227-32.
114. Hirano T, Ishihara K, and Hibi M. Roles of STAT3 in mediating the cell growth, differentiation and survival signals relayed through the IL-6 family of cytokine receptors. Oncogene, 2000. 19(21): 2548-56.
115. Kijima T, et al. STAT3 activation abrogates growth factor dependence and contributes to head and neck squamous cell carcinoma tumor growth in vivo. Cell Growth Differ, 2002. 13(8): 355-62.
116. Sriuranpong V, et al. Epidermal growth factor receptor-independent constitutive activation of STAT3 in head and neck squamous cell carcinoma is mediated by the autocrine/paracrine stimulation of the interleukin 6/gp130 cytokine system. Cancer Res, 2003. 63(11): 2948-56.
117. Gastman B.R, et al. Fas ligand is expressed on human squamous cell carcinomas of the head and neck, and it promotes apoptosis of T lymphocytes. Cancer Res, 1999. 59(20): 5356-64.
118. Kim J.W, et al. Fas ligand-positive membranous vesicles isolated from sera of patients with oral cancer induce apoptosis of activated T lymphocytes. Clin Cancer Res, 2005. 11(3): 1010-20.
119. Biswas P, et al. Interleukin-6 induces monocyte chemotactic protein-1 in peripheral blood mononuclear cells and in the U937 cell line. Blood, 1998. 91(1): 258-65.
120. Gabrilovich D. Mechanisms and functional significance of tumour-induced dendritic-cell defects. Nat Rev Immunol, 2004. 4(12): 941-52.
121. Gabrilovich D.I, et al. Production of vascular endothelial growth factor by human tumors inhibits the functional maturation of dendritic cells. Nat Med, 1996. 2(10): 1096-103.
122. Laxmanan S, et al. Vascular endothelial growth factor impairs the functional ability of dendritic cells through Id pathways. Biochem Biophys Res Commun, 2005. 334(1): 193-8.
123. Nefedova Y, et al. Activation of dendritic cells via inhibition of Jak2/STAT3 signaling. Immunol J, 2005. 175(7): 4338-46.
124. Nefedova Y, et al. Hyperactivation of STAT3 is involved in abnormal differentiation of dendritic cells in cancer. Immunol J, 2004. 172(1): 464-74.
125. Oyama T, et al. Vascular endothelial growth factor affects dendritic cell maturation through the inhibition of nuclear factor-kappa B activation in hemopoietic progenitor cells. Immunol J, 1998. 160(3): 1224-32.
126. Park S.J, et al. IL-6 regulates in vivo dendritic cell differentiation through STAT3 activation. Immunol J, 2004. 173(6): 3844-54.