Tumor-derived factors modulating dendritic cell function

Cancer Immunology, Immunotherapy

Volumn 65, Issue 7, 2016, Pages 821-833

  Zong, Jinbao ^a,b   Keskinov, Anton A ^a   Shurin, Galina V ^a   Shurin, Michael R ^a  

^a UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^b QINGDAO UNIVERSITY   (China)

Author keywords

Cytokines; Dendritic cells; Immunosuppression; Regulatory dendritic cells; Tolerance; Tumor immunoenvironment

Indexed keywords

CHEMOKINE; CHORIONIC GONADOTROPIN; COLONY STIMULATING FACTOR 1; GANGLIOSIDE; INTERLEUKIN 10; INTERLEUKIN 6; LACTIC ACID; MUCIN 1; NEUROPEPTIDE; OSTEOCLAST DIFFERENTIATION FACTOR; POLYAMINE; PROSTANOID; PROSTATE SPECIFIC ANTIGEN; TUMOR ANTIGEN; TUMOR MARKER; VASCULOTROPIN;

CARCINOGENESIS; CELL DIFFERENTIATION; CELL FUNCTION; CELL INTERACTION; CELL MATURATION; DENDRITIC CELL; EFFECTOR CELL; HUMAN; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOLOGICAL TOLERANCE; INNATE IMMUNITY; MEMBRANE MICROPARTICLE; NEOPLASM; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; TUMOR IMMUNITY; ANIMAL; IMMUNOLOGY;

ANIMALS; CELL DIFFERENTIATION; DENDRITIC CELLS; HUMANS; NEOPLASMS;

EID: 84962482523     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-016-1820-y     Document Type: Review

References (117)

1. Zhong H, Shurin MR, Han B (2007) Optimizing dendritic cell-based immunotherapy for cancer. Expert Rev Vaccin 6(3):333–345. doi:10.1586/14760584.6.3.333
2. Ma Y, Shurin GV, Gutkin DW, Shurin MR (2012) Tumor associated regulatory dendritic cells. Semin Cancer Biol 22(4):298–306. doi:10.1016/j.semcancer.2012.02.010
3. Shurin GV, Ma Y, Shurin MR (2013) Immunosuppressive mechanisms of regulatory dendritic cells in cancer. Cancer Microenviron 6(2):159–167. doi:10.1007/s12307-013-0133-3
4. Shurin GV, Ouellette CE, Shurin MR (2012) Regulatory dendritic cells in the tumor immunoenvironment. Cancer Immunol Immunother 61(2):223–230. doi:10.1007/s00262-011-1138-8
5. Ma Y, Shurin GV, Peiyuan Z, Shurin MR (2013) Dendritic cells in the cancer microenvironment. J Cancer 4(1):36–44. doi:10.7150/jca.5046
6. Shurin MR, Naiditch H, Zhong H, Shurin GV (2011) Regulatory dendritic cells: new targets for cancer immunotherapy. Cancer Biol Ther 11(11):988–992
7. Garg AD, Dudek-Peric AM, Romano E, Agostinis P (2015) Immunogenic cell death. Int J Dev Biol 59(1–3):131–140. doi:10.1387/ijdb.150061pa
8. Bianchi ME (2007) DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol 81(1):1–5. doi:10.1189/jlb.0306164
9. Kang R, Chen R, Zhang Q, Hou W, Wu S, Cao L, Huang J, Yu Y, Fan XG, Yan Z, Sun X, Wang H, Wang Q, Tsung A, Billiar TR, Zeh HJ 3rd, Lotze MT, Tang D (2014) HMGB1 in health and disease. Mol Aspects Med 40:1–116. doi:10.1016/j.mam.2014.05.001
10. Sims GP, Rowe DC, Rietdijk ST, Herbst R, Coyle AJ (2010) HMGB1 and RAGE in inflammation and cancer. Annu Rev Immunol 28:367–388. doi:10.1146/annurev.immunol.021908.132603
11. Saenz R, Souza Cda S, Huang CT, Larsson M, Esener S, Messmer D (2010) HMGB1-derived peptide acts as adjuvant inducing immune responses to peptide and protein antigen. Vaccine 28(47):7556–7562. doi:10.1016/j.vaccine.2010.08.054
12. Saenz R, Futalan D, Leutenez L, Eekhout F, Fecteau JF, Sundelius S, Sundqvist S, Larsson M, Hayashi T, Minev B, Carson D, Esener S, Messmer B, Messmer D (2014) TLR4-dependent activation of dendritic cells by an HMGB1-derived peptide adjuvant. J Transl Med 12:211. doi:10.1186/1479-5876-12-211
13. Saenz R, Messmer B, Futalan D, Tor Y, Larsson M, Daniels G, Esener S, Messmer D (2014) Activity of the HMGB1-derived immunostimulatory peptide Hp91 resides in the helical C-terminal portion and is enhanced by dimerization. Mol Immunol 57(2):191–199. doi:10.1016/j.molimm.2013.09.007
14. Demoulin S, Herfs M, Somja J, Roncarati P, Delvenne P, Hubert P (2015) HMGB1 secretion during cervical carcinogenesis promotes the acquisition of a tolerogenic functionality by plasmacytoid dendritic cells. Int J Cancer 137(2):345–358. doi:10.1002/ijc.29389
15. Chen B, Miller AL, Rebelatto M, Brewah Y, Rowe DC, Clarke L, Czapiga M, Rosenthal K, Imamichi T, Chen Y, Chang CS, Chowdhury PS, Naiman B, Wang Y, Yang D, Humbles AA, Herbst R, Sims GP (2015) S100A9 induced inflammatory responses are mediated by distinct damage associated molecular patterns (DAMP) receptors in vitro and in vivo. PLoS ONE 10(2):e0115828. doi:10.1371/journal.pone.0115828
16. Donato R, Cannon BR, Sorci G, Riuzzi F, Hsu K, Weber DJ, Geczy CL (2013) Functions of S100 proteins. Curr Mol Med 13(1):24–57
17. Lee TH, Jang AS, Park JS, Kim TH, Choi YS, Shin HR, Park SW, Uh ST, Choi JS, Kim YH, Kim Y, Kim S, Chung IY, Jeong SH, Park CS (2013) Elevation of S100 calcium binding protein A9 in sputum of neutrophilic inflammation in severe uncontrolled asthma. Ann Allergy Asthma Immunol 111(4):268–275. doi:10.1016/j.anai.2013.06.028
18. Srikrishna G (2012) S100A8 and S100A9: new insights into their roles in malignancy. J Innate Immun 4(1):31–40. doi:10.1159/000330095
19. Engelkamp D, Schafer BW, Mattei MG, Erne P, Heizmann CW (1993) Six S100 genes are clustered on human chromosome 1q21: identification of two genes coding for the two previously unreported calcium-binding proteins S100D and S100E. Proc Natl Acad Sci USA 90(14):6547–6551
20. Zhu L, Kohda F, Nakahara T, Chiba T, Tsuji G, Hachisuka J, Ito T, Tu Y, Moroi Y, Uchi H, Furue M (2013) Aberrant expression of S100A6 and matrix metalloproteinase 9, but not S100A2, S100A4, and S100A7, is associated with epidermal carcinogenesis. J Dermatol Sci 72(3):311–319. doi:10.1016/j.jdermsci.2013.07.005
21. Basso D, Fogar P, Plebani M (2013) The S100A8/A9 complex reduces CTLA4 expression by immature myeloid cells: implications for pancreatic cancer-driven immunosuppression. Oncoimmunology 2(6):e24441. doi:10.4161/onci.24441
22. Harpio R, Einarsson R (2004) S100 proteins as cancer biomarkers with focus on S100B in malignant melanoma. Clin Biochem 37(7):512–518. doi:10.1016/j.clinbiochem.2004.05.012
23. Wang T, Liang Y, Thakur A, Zhang S, Yang T, Chen T, Gao L, Chen M, Ren H (2015) Diagnostic significance of S100A2 and S100A6 levels in sera of patients with non-small cell lung cancer. Tumour Biol. doi:10.1007/s13277-015-4057-z
24. Averill MM, Barnhart S, Becker L, Li X, Heinecke JW, Leboeuf RC, Hamerman JA, Sorg C, Kerkhoff C, Bornfeldt KE (2011) S100A9 differentially modifies phenotypic states of neutrophils, macrophages, and dendritic cells: implications for atherosclerosis and adipose tissue inflammation. Circulation 123(11):1216–1226. doi:10.1161/CIRCULATIONAHA.110.985523
25. Bruhn S, Fang Y, Barrenas F, Gustafsson M, Zhang H, Konstantinell A, Kronke A, Sonnichsen B, Bresnick A, Dulyaninova N, Wang H, Zhao Y, Klingelhofer J, Ambartsumian N, Beck MK, Nestor C, Bona E, Xiang Z, Benson M (2014) A generally applicable translational strategy identifies S100A4 as a candidate gene in allergy. Sci Transl Med 6(218):218ra4. doi:10.1126/scitranslmed.3007410
26. Ampie L, Choy W, Lamano JB, Fakurnejad S, Bloch O, Parsa AT (2015) Heat shock protein vaccines against glioblastoma: from bench to bedside. J Neurooncol 123(3):441–448. doi:10.1007/s11060-015-1837-7
27. Pawaria S, Binder RJ (2011) CD91-dependent programming of T-helper cell responses following heat shock protein immunization. Nat Commun 2:521. doi:10.1038/ncomms1524
28. Kuppner MC, Gastpar R, Gelwer S, Nossner E, Ochmann O, Scharner A, Issels RD (2001) The role of heat shock protein (hsp70) in dendritic cell maturation: hsp70 induces the maturation of immature dendritic cells but reduces DC differentiation from monocyte precursors. Eur J Immunol 31(5):1602–1609. doi:10.1002/1521-4141(200105)31:5<1602:AID-IMMU1602>3.0.CO;2-W
29. Binder RJ, Srivastava PK (2005) Peptides chaperoned by heat-shock proteins are a necessary and sufficient source of antigen in the cross-priming of CD8 + T cells. Nat Immunol 6(6):593–599. doi:10.1038/ni1201
30. Ferrara N, Gerber HP, LeCouter J (2003) The biology of VEGF and its receptors. Nat Med 9(6):669–676. doi:10.1038/nm0603-669
31. Toi M, Matsumoto T, Bando H (2001) Vascular endothelial growth factor: its prognostic, predictive, and therapeutic implications. Lancet Oncol 2(11):667–673. doi:10.1016/S1470-2045(01)00556-3
32. 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(10):1096–1103
33. Gabrilovich D, Ishida T, Oyama T, Ran S, Kravtsov V, Nadaf S, Carbone DP (1998) Vascular endothelial growth factor inhibits the development of dendritic cells and dramatically affects the differentiation of multiple hematopoietic lineages in vivo. Blood 92(11):4150–4166
34. Shi Y, Yu P, Zeng D, Qian F, Lei X, Zhao Y, Tang B, Hao Y, Luo H, Chen J, Tan Y (2014) Suppression of vascular endothelial growth factor abrogates the immunosuppressive capability of murine gastric cancer cells and elicits antitumor immunity. FEBS J 281(17):3882–3893. doi:10.1111/febs.12923
35. 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(2–3):276–284. doi:10.1159/000086784
36. Kim R, Emi M, Tanabe K, Arihiro K (2006) Tumor-driven evolution of immunosuppressive networks during malignant progression. Cancer Res 66(11):5527–5536. doi:10.1158/0008-5472.CAN-05-4128
37. 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(16):4840–4848. doi:10.1158/1078-0432.CCR-07-0409
38. Wang H, Zhang L, Zhang S, Li Y (2015) Inhibition of vascular endothelial growth factor by small interfering RNA upregulates differentiation, maturation and function of dendritic cells. Exper Therap Med 9(1):120–124. doi:10.3892/etm.2014.2059
39. Seeger P, Musso T, Sozzani S (2015) The TGF-beta superfamily in dendritic cell biology. Cytokine Growth Fact Rev 26(6):647–657. doi:10.1016/j.cytogfr.2015.06.002
40. Yasmin N, Konradi S, Eisenwort G, Schichl YM, Seyerl M, Bauer T, Stockl J, Strobl H (2013) Beta-Catenin promotes the differentiation of epidermal Langerhans dendritic cells. J Invest Derm 133(5):1250–1259. doi:10.1038/jid.2012.481
41. Brown RD, Pope B, Murray A, Esdale W, Sze DM, Gibson J, Ho PJ, Hart D, Joshua D (2001) Dendritic cells from patients with myeloma are numerically normal but functionally defective as they fail to up-regulate CD80 (B7-1) expression after huCD40LT stimulation because of inhibition by transforming growth factor-beta1 and interleukin-10. Blood 98(10):2992–2998
42. Kel JM, Girard-Madoux MJ, Reizis B, Clausen BE (2010) TGF-beta is required to maintain the pool of immature Langerhans cells in the epidermis. J Immunol 185(6):3248–3255. doi:10.4049/jimmunol.1000981
43. Lievens D, Habets KL, Robertson AK, Laouar Y, Winkels H, Rademakers T, Beckers L, Wijnands E, Boon L, Mosaheb M, Ait-Oufella H, Mallat Z, Flavell RA, Rudling M, Binder CJ, Gerdes N, Biessen EA, Weber C, Daemen MJ, Kuiper J, Lutgens E (2013) Abrogated transforming growth factor beta receptor II (TGFbetaRII) signalling in dendritic cells promotes immune reactivity of T cells resulting in enhanced atherosclerosis. Eur Heart J 34(48):3717–3727. doi:10.1093/eurheartj/ehs106
44. Ito M, Minamiya Y, Kawai H, Saito S, Saito H, Nakagawa T, Imai K, Hirokawa M, Ogawa J (2006) Tumor-derived TGFbeta-1 induces dendritic cell apoptosis in the sentinel lymph node. J Immun 176(9):5637–5643
45. Song S, Yuan P, Wu H, Chen J, Fu J, Li P, Lu J, Wei W (2014) Dendritic cells with an increased PD-L1 by TGF-beta induce T cell anergy for the cytotoxicity of hepatocellular carcinoma cells. Int Immunopharmacol 20(1):117–123. doi:10.1016/j.intimp.2014.02.027
46. Zhou Z, Li W, Song Y, Wang L, Zhang K, Yang J, Zhang W, Su H, Zhang Y (2013) Growth differentiation factor-15 suppresses maturation and function of dendritic cells and inhibits tumor-specific immune response. PLoS ONE 8(11):e78618. doi:10.1371/journal.pone.0078618
47. Smith DR, Kunkel SL, Burdick MD, Wilke CA, Orringer MB, Whyte RI, Strieter RM (1994) Production of interleukin-10 by human bronchogenic carcinoma. Am J Pathol 145(1):18–25
48. Gu ZJ, Costes V, Lu ZY, Zhang XG, Pitard V, Moreau JF, Bataille R, Wijdenes J, Rossi JF, Klein B (1996) Interleukin-10 is a growth factor for human myeloma cells by induction of an oncostatin M autocrine loop. Blood 88(10):3972–3986
49. Kim KD, Lim HY, Lee HG, Yoon DY, Choe YK, Choi I, Paik SG, Kim YS, Yang Y, Lim JS (2005) Apolipoprotein A-I induces IL-10 and PGE2 production in human monocytes and inhibits dendritic cell differentiation and maturation. Biochem Biophys Res Commun 338(2):1126–1136. doi:10.1016/j.bbrc.2005.10.065
50. Beckebaum S, Zhang X, Chen X, Yu Z, Frilling A, Dworacki G, Grosse-Wilde H, Broelsch CE, Gerken G, Cicinnati VR (2004) Increased levels of interleukin-10 in serum from patients with hepatocellular carcinoma correlate with profound numerical deficiencies and immature phenotype of circulating dendritic cell subsets. Clin Cancer Res 10(21):7260–7269. doi:10.1158/1078-0432.CCR-04-0872
51. Williams LM, Ricchetti G, Sarma U, Smallie T, Foxwell BM (2004) Interleukin-10 suppression of myeloid cell activation: a continuing puzzle. Immunology 113(3):281–292. doi:10.1111/j.1365-2567.2004.01988.x
52. Shurin MR, Yurkovetsky ZR, Tourkova IL, Balkir L, Shurin GV (2002) Inhibition of CD40 expression and CD40-mediated dendritic cell function by tumor-derived IL-10. Int J Cancer 101(1):61–68. doi:10.1002/ijc.10576
53. Shurin MR, Shurin GV, Lokshin A, Yurkovetsky ZR, Gutkin DW, Chatta G, Zhong H, Han B, Ferris RL (2006) Intratumoral cytokines/chemokines/growth factors and tumor infiltrating dendritic cells: friends or enemies? Cancer Metas Rev 25(3):333–356. doi:10.1007/s10555-006-9010-6
54. Oosterhoff D, Lougheed S, van de Ven R, Lindenberg J, van Cruijsen H, Hiddingh L, Kroon J, van den Eertwegh AJ, Hangalapura B, Scheper RJ, de Gruijl TD (2012) Tumor-mediated inhibition of human dendritic cell differentiation and function is consistently counteracted by combined p38 MAPK and STAT3 inhibition. Oncoimmunology 1(5):649–658. doi:10.4161/onci.20365
55. Schwarz AM, Banning-Eichenseer U, Seidel K, Mauz-Korholz C, Korholz D, Staege MS (2013) Impact of interleukin-10 on phenotype and gene expression during early monocyte differentiation into dendritic cells. Anticancer Res 33(11):4791–4798
56. Hirano T (1998) Interleukin 6 and its receptor: 10 years later. Int Rev Immunol 16(3–4):249–284. doi:10.3109/08830189809042997
57. Ratta M, Fagnoni F, Curti A, Vescovini R, Sansoni P, Oliviero B, Fogli M, Ferri E, Della Cuna GR, Tura S, Baccarani M, Lemoli RM (2002) Dendritic cells are functionally defective in multiple myeloma: the role of interleukin-6. Blood 100(1):230–237
58. Nishio H, Yaguchi T, Sugiyama J, Sumimoto H, Umezawa K, Iwata T, Susumu N, Fujii T, Kawamura N, Kobayashi A, Park J, Aoki D, Kawakami Y (2014) Immunosuppression through constitutively activated NF-kappaB signalling in human ovarian cancer and its reversal by an NF-kappaB inhibitor. Br J Cancer 110(12):2965–2974. doi:10.1038/bjc.2014.251
59. Chomarat P, Banchereau J, Davoust J, Palucka AK (2000) IL-6 switches the differentiation of monocytes from dendritic cells to macrophages. Nat Immunol 1(6):510–514. doi:10.1038/82763
60. Alshamsan A (2012) Induction of tolerogenic dendritic cells by IL-6-secreting CT26 colon carcinoma. Immunopharmacol Immunotoxicol 34(3):465–469. doi:10.3109/08923973.2011.625034
61. Yang L, Wu Q, Xu L, Zhang W, Zhu Y, Liu H, Xu J, Gu J (2015) Increased expression of colony stimulating factor-1 is a predictor of poor prognosis in patients with clear-cell renal cell carcinoma. BMC Cancer 15:67. doi:10.1186/s12885-015-1076-5
62. Lin EY, Gouon-Evans V, Nguyen AV, Pollard JW (2002) The macrophage growth factor CSF-1 in mammary gland development and tumor progression. J Mammary Gland Biol Neoplasia 7(2):147–162
63. Menetrier-Caux C, Montmain G, Dieu MC, Bain C, Favrot MC, Caux C, Blay JY (1998) Inhibition of the differentiation of dendritic cells from CD34(+) progenitors by tumor cells: role of interleukin-6 and macrophage colony-stimulating factor. Blood 92(12):4778–4791
64. Lo AS, Gorak-Stolinska P, Bachy V, Ibrahim MA, Kemeny DM, Maher J (2007) Modulation of dendritic cell differentiation by colony-stimulating factor-1: role of phosphatidylinositol 3′-kinase and delayed caspase activation. J Leukoc Biol 82(6):1446–1454. doi:10.1189/jlb.0307142
65. Demoulin SA, Somja J, Duray A, Guenin S, Roncarati P, Delvenne PO, Herfs MF, Hubert PM (2015) Cervical (pre)neoplastic microenvironment promotes the emergence of tolerogenic dendritic cells via RANKL secretion. Oncoimmunology 4(6):e1008334. doi:10.1080/2162402X.2015.1008334
66. Perrot I, Blanchard D, Freymond N, Isaac S, Guibert B, Pacheco Y, Lebecque S (2007) Dendritic cells infiltrating human non-small cell lung cancer are blocked at immature stage. J Immunol 178(5):2763–2769
67. Stoitzner P, Green LK, Jung JY, Price KM, Atarea H, Kivell B, Ronchese F (2008) Inefficient presentation of tumor-derived antigen by tumor-infiltrating dendritic cells. Cancer Immunol Immunother 57(11):1665–1673. doi:10.1007/s00262-008-0487-4
68. Zou W, Machelon V, Coulomb-L’Hermin A, Borvak J, Nome F, Isaeva T, Wei S, Krzysiek R, Durand-Gasselin I, Gordon A, Pustilnik T, Curiel DT, Galanaud P, Capron F, Emilie D, Curiel TJ (2001) Stromal-derived factor-1 in human tumors recruits and alters the function of plasmacytoid precursor dendritic cells. Nat Med 7(12):1339–1346. doi:10.1038/nm1201-1339
69. Teicher BA, Fricker SP (2010) CXCL12 (SDF-1)/CXCR4 pathway in cancer. Clin Cancer Res 16(11):2927–2931. doi:10.1158/1078-0432.CCR-09-2329
70. Hargadon KM, Bishop JD, Brandt JP, Hand ZC, Ararso YT, Forrest OA (2016) Melanoma-derived factors alter the maturation and activation of differentiated tissue-resident dendritic cells. Immunol Cell Biol 94(1):24–38. doi:10.1038/icb.2015.58
71. Aalamian M, Tourkova IL, Chatta GS, Lilja H, Huland E, Huland H, Shurin GV, Shurin MR (2003) Inhibition of dendropoiesis by tumor derived and purified prostate specific antigen. J Urol 170(5):2026–2030. doi:10.1097/01.ju.0000091264.46134.b7
72. Aalamian-Matheis M, Chatta GS, Shurin MR, Huland E, Huland H, Shurin GV (2007) Inhibition of dendritic cell generation and function by serum from prostate cancer patients: correlation with serum-free PSA. Adv Exp Med Biol 601:173–182
73. Pillai K, Pourgholami MH, Chua TC, Morris DL (2015) MUC1 as a potential target in anticancer therapies. Am J Clin Oncol 38(1):108–118. doi:10.1097/COC.0b013e31828f5a07
74. Carlos CA, Dong HF, Howard OM, Oppenheim JJ, Hanisch FG, Finn OJ (2005) Human tumor antigen MUC1 is chemotactic for immature dendritic cells and elicits maturation but does not promote Th1 type immunity. J Immunol 175(3):1628–1635
75. Rughetti A, Pellicciotta I, Biffoni M, Backstrom M, Link T, Bennet EP, Clausen H, Noll T, Hansson GC, Burchell JM, Frati L, Taylor-Papadimitriou J, Nuti M (2005) Recombinant tumor-associated MUC1 glycoprotein impairs the differentiation and function of dendritic cells. J Immunol 174(12):7764–7772
76. Ueno A, Cho S, Cheng L, Wang J, Hou S, Nakano H, Santamaria P, Yang Y (2007) Transient upregulation of indoleamine 2,3-dioxygenase in dendritic cells by human chorionic gonadotropin downregulates autoimmune diabetes. Diabetes 56(6):1686–1693. doi:10.2337/db06-1727
77. Hwu P, Du MX, Lapointe R, Do M, Taylor MW, Young HA (2000) Indoleamine 2,3-dioxygenase production by human dendritic cells results in the inhibition of T cell proliferation. J Immunol 164(7):3596–3599
78. Palmano K, Rowan A, Guillermo R, Guan J, McJarrow P (2015) The role of gangliosides in neurodevelopment. Nutrients 7(5):3891–3913. doi:10.3390/nu7053891
79. Shurin GV, Shurin MR, Bykovskaia S, Shogan J, Lotze MT, Barksdale EM Jr (2001) Neuroblastoma-derived gangliosides inhibit dendritic cell generation and function. Cancer Res 61(1):363–369
80. Peguet-Navarro J, Sportouch M, Popa I, Berthier O, Schmitt D, Portoukalian J (2003) Gangliosides from human melanoma tumors impair dendritic cell differentiation from monocytes and induce their apoptosis. J Immunol 170(7):3488–3494
81. Bennaceur K, Popa I, Chapman JA, Migdal C, Peguet-Navarro J, Touraine JL, Portoukalian J (2009) Different mechanisms are involved in apoptosis induced by melanoma gangliosides on human monocyte-derived dendritic cells. Glycobiology 19(6):576–582. doi:10.1093/glycob/cwp015
82. Pugh S, Thomas GA (1994) Patients with adenomatous polyps and carcinomas have increased colonic mucosal prostaglandin E2. Gut 35(5):675–678
83. Sombroek CC, Stam AG, Masterson AJ, Lougheed SM, Schakel MJ, Meijer CJ, Pinedo HM, van den Eertwegh AJ, Scheper RJ, de Gruijl TD (2002) Prostanoids play a major role in the primary tumor-induced inhibition of dendritic cell differentiation. J Immunol 168(9):4333–4343
84. Trabanelli S, Lecciso M, Salvestrini V, Cavo M, Ocadlikova D, Lemoli RM, Curti A (2015) PGE2-induced IDO1 inhibits the capacity of fully mature DCs to elicit an in vitro antileukemic immune response. J Immunol Res 2015:253191. doi:10.1155/2015/253191
85. Schipper RG, Romijn JC, Cuijpers VM, Verhofstad AA (2003) Polyamines and prostatic cancer. Biochem Soc Trans 31(2):375–380. doi:10.1042/bst0310375
86. Erbas H, Bal O, Cakir E (2015) Effect of rosuvastatin on arginase enzyme activity and polyamine production in experimental breast cancer. Balkan Med J 32(1):89–95. doi:10.5152/balkanmedj.2015.15611
87. Della Bella S, Gennaro M, Vaccari M, Ferraris C, Nicola S, Riva A, Clerici M, Greco M, Villa ML (2003) Altered maturation of peripheral blood dendritic cells in patients with breast cancer. Br J Cancer 89(8):1463–1472. doi:10.1038/sj.bjc.6601243
88. Doherty JR, Cleveland JL (2013) Targeting lactate metabolism for cancer therapeutics. J Clin Invest 123(9):3685–3692. doi:10.1172/JCI69741
89. Gottfried E, Kunz-Schughart LA, Ebner S, Mueller-Klieser W, Hoves S, Andreesen R, Mackensen A, Kreutz M (2006) Tumor-derived lactic acid modulates dendritic cell activation and antigen expression. Blood 107(5):2013–2021. doi:10.1182/blood-2005-05-1795
90. Nasi A, Fekete T, Krishnamurthy A, Snowden S, Rajnavolgyi E, Catrina AI, Wheelock CE, Vivar N, Rethi B (2013) Dendritic cell reprogramming by endogenously produced lactic acid. J Immunol 191(6):3090–3099. doi:10.4049/jimmunol.1300772
91. Vaupel P, Mayer A (2016) Hypoxia-driven adenosine accumulation: a crucial microenvironmental factor promoting tumor progression. Adv Exp Med Biol 876:177–183. doi:10.1007/978-1-4939-3023-4_22
92. Liang D, Zuo A, Shao H, Chen M, Kaplan HJ, Sun D (2015) A2B adenosine receptor activation switches differentiation of bone marrow cells to a CD11c(+)Gr-1(+) dendritic cell subset that promotes the Th17 response. Immun Inflamm Dis 3(4):360–373. doi:10.1002/iid3.74
93. Novitskiy SV, Ryzhov S, Zaynagetdinov R, Goldstein AE, Huang Y, Tikhomirov OY, Blackburn MR, Biaggioni I, Carbone DP, Feoktistov I, Dikov MM (2008) Adenosine receptors in regulation of dendritic cell differentiation and function. Blood 112(5):1822–1831. doi:10.1182/blood-2008-02-136325
94. Ring S, Pushkarevskaya A, Schild H, Probst HC, Jendrossek V, Wirsdorfer F, Ledent C, Robson SC, Enk AH, Mahnke K (2015) Regulatory T cell-derived adenosine induces dendritic cell migration through the Epac-Rap1 pathway. J Immunol 194(8):3735–3744. doi:10.4049/jimmunol.1401434
95. Maroof A, English NR, Bedford PA, Gabrilovich DI, Knight SC (2005) Developing dendritic cells become ‘lacy’ cells packed with fat and glycogen. Immunology 115(4):473–483. doi:10.1111/j.1365-2567.2005.02181.x
96. Dong H, Bullock TN (2014) Metabolic influences that regulate dendritic cell function in tumors. Front Immunol 5:24. doi:10.3389/fimmu.2014.00024
97. Herber DL, Cao W, Nefedova Y, Novitskiy SV, Nagaraj S, Tyurin VA, Corzo A, Cho HI, Celis E, Lennox B, Knight SC, Padhya T, McCaffrey TV, McCaffrey JC, Antonia S, Fishman M, Ferris RL, Kagan VE, Gabrilovich DI (2010) Lipid accumulation and dendritic cell dysfunction in cancer. Nat Med 16(8):880–886. doi:10.1038/nm.2172
98. Tyurin VA, Cao W, Tyurina YY, Gabrilovich DI, Kagan VE (2011) Mass-spectrometric characterization of peroxidized and hydrolyzed lipids in plasma and dendritic cells of tumor-bearing animals. Biochem Biophys Res Com 413(1):149–153. doi:10.1016/j.bbrc.2011.08.074
99. Gardner JK, Mamotte CD, Patel P, Yeoh TL, Jackaman C, Nelson DJ (2015) Mesothelioma tumor cells modulate dendritic cell lipid content, phenotype and function. PLoS ONE 10(4):e0123563. doi:10.1371/journal.pone.0123563
100. Gao F, Liu C, Guo J, Sun W, Xian L, Bai D, Liu H, Cheng Y, Li B, Cui J, Zhang C, Cai J (2015) Radiation-driven lipid accumulation and dendritic cell dysfunction in cancer. Sci Rep 5:9613. doi:10.1038/srep09613
101. Cubillos-Ruiz JR, Silberman PC, Rutkowski MR, Chopra S, Perales-Puchalt A, Song M, Zhang S, Bettigole SE, Gupta D, Holcomb K, Ellenson LH, Caputo T, Lee AH, Conejo-Garcia JR, Glimcher LH (2015) ER stress sensor XBP1 controls anti-tumor immunity by disrupting dendritic cell homeostasis. Cell 161(7):1527–1538. doi:10.1016/j.cell.2015.05.025
102. Wu R, Zhang QH, Lu YJ, Ren K, Yi GH (2015) Involvement of the IRE1alpha-XBP1 pathway and XBP1s-dependent transcriptional reprogramming in metabolic diseases. DNA Cell Biol 34(1):6–18. doi:10.1089/dna.2014.2552
103. Scanlon CS, Banerjee R, Inglehart RC, Liu M, Russo N, Hariharan A, van Tubergen EA, Corson SL, Asangani IA, Mistretta CM, Chinnaiyan AM, D’Silva NJ (2015) Galanin modulates the neural niche to favour perineural invasion in head and neck cancer. Nat Commun 6:6885. doi:10.1038/ncomms7885
104. Covenas R, Munoz M (2014) Cancer progression and substance P. Histol Histopathol 29(7):881–890
105. Voedisch S, Rochlitzer S, Veres TZ, Spies E, Braun A (2012) Neuropeptides control the dynamic behavior of airway mucosal dendritic cells. PLoS ONE 7(9):e45951. doi:10.1371/journal.pone.0045951
106. Toda M, Suzuki T, Hosono K, Hayashi I, Hashiba S, Onuma Y, Amano H, Kurihara Y, Kurihara H, Okamoto H, Hoka S, Majima M (2008) Neuronal system-dependent facilitation of tumor angiogenesis and tumor growth by calcitonin gene-related peptide. Proc Natl Acad Sci USA 105(36):13550–13555. doi:10.1073/pnas.0800767105
107. Gilaberte Y, Roca MJ, Garcia-Prats MD, Coscojuela C, Arbues MD, Vera-Alvarez JJ (2012) Neuropeptide Y expression in cutaneous melanoma. J Am Acad Dermatol 66(6):e201–e208. doi:10.1016/j.jaad.2011.02.015
108. Buttari B, Profumo E, Domenici G, Tagliani A, Ippoliti F, Bonini S, Businaro R, Elenkov I, Rigano R (2014) Neuropeptide Y induces potent migration of human immature dendritic cells and promotes a Th2 polarization. FASEB J 28(7):3038–3049. doi:10.1096/fj.13-243485
109. Makarenkova VP, Shurin GV, Tourkova IL, Balkir L, Pirtskhalaishvili G, Perez L, Gerein V, Siegfried JM, Shurin MR (2003) Lung cancer-derived bombesin-like peptides down-regulate the generation and function of human dendritic cells. J Neuroimmunol 145(1–2):55–67
110. DeRosa DC, Ryan PJ, Okragly A, Witcher DR, Benschop RJ (2008) Tumor-derived death receptor 6 modulates dendritic cell development. Cancer Immunol Immunother 57(6):777–787. doi:10.1007/s00262-007-0413-1
111. D’Souza-Schorey C, Clancy JW (2012) Tumor-derived microvesicles: shedding light on novel microenvironment modulators and prospective cancer biomarkers. Genes Dev 26(12):1287–1299. doi:10.1101/gad.192351.112
112. Valenti R, Huber V, Filipazzi P, Pilla L, Sovena G, Villa A, Corbelli A, Fais S, Parmiani G, Rivoltini L (2006) Human tumor-released microvesicles promote the differentiation of myeloid cells with transforming growth factor-beta-mediated suppressive activity on T lymphocytes. Cancer Res 66(18):9290–9298. doi:10.1158/0008-5472.CAN-06-1819
113. Huang SH, Li Y, Zhang J, Rong J, Ye S (2013) Epidermal growth factor receptor-containing exosomes induce tumor-specific regulatory T cells. Cancer Invest 31(5):330–335. doi:10.3109/07357907.2013.789905
114. Ding G, Zhou L, Qian Y, Fu M, Chen J, Chen J, Xiang J, Wu Z, Jiang G, Cao L (2015) Pancreatic cancer-derived exosomes transfer miRNAs to dendritic cells and inhibit RFXAP expression via miR-212-3p. Oncotarget 6(30):29877–29888. doi:10.18632/oncotarget.4924
115. Feijoo E, Alfaro C, Mazzolini G, Serra P, Penuelas I, Arina A, Huarte E, Tirapu I, Palencia B, Murillo O, Ruiz J, Sangro B, Richter JA, Prieto J, Melero I (2005) Dendritic cells delivered inside human carcinomas are sequestered by interleukin-8. Int J Cancer 116(2):275–281. doi:10.1002/ijc.21046
116. Yang L, Yamagata N, Yadav R, Brandon S, Courtney RL, Morrow JD, Shyr Y, Boothby M, Joyce S, Carbone DP, Breyer RM (2003) Cancer-associated immunodeficiency and dendritic cell abnormalities mediated by the prostaglandin EP2 receptor. J Clin Invest 111(5):727–735. doi:10.1172/JCI16492
117. Ristich V, Liang S, Zhang W, Wu J, Horuzsko A (2005) Tolerization of dendritic cells by HLA-G. Eur J Immunol 35(4):1133–1142. doi:10.1002/eji.200425741