The hypoxic environment reprograms the cytokine/chemokine expression profile of human mature dendritic cells

Immunobiology

Volumn 218, Issue 1, 2013, Pages 76-89

  Blengio, Fabiola ^a   Raggi, Federica ^a   Pierobon, Daniele ^b,c   Cappello, Paola ^b,c   Eva, Alessandra ^a   Giovarelli, Mirella ^b,c   Varesio, Luigi ^a   Bosco, Maria Carla ^a  

^a G GASLINI INSTITUTE   (Italy)

^b MOLINETTE HOSPITAL   (Italy)

^c UNIVERSITY OF TURIN   (Italy)

Author keywords

Chemokines cytokines; Dendritic cells; Gene regulation; Hypoxia; Inflammation

Indexed keywords

CCL18 CHEMOKINE; CCL23 CHEMOKINE; CHEMOKINE; CXCL2 CHEMOKINE; CXCL3 CHEMOKINE; CYTOKINE; EPITHELIAL DERIVED NEUTROPHIL ACTIVATING FACTOR 78; GRANULOCYTE CHEMOTACTIC PROTEIN 2; INTERLEUKIN 1BETA; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MESSENGER RNA; OSTEOPONTIN; RANTES; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANGIOGENESIS; ARTICLE; CA2 GENE; CCL18 GENE; CCL20 GENE; CCL23 GENE; CCL3 GENE; CCL5 GENE; CCR6 GENE; CHEMOTAXIS; CONTROLLED STUDY; CXCL2 GENE; CXCL3 GENE; CXCL5 GENE; CXCL6 GENE; CXCL8 GENE; DENDRITIC CELL; ENO2 GENE; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE; GENE CLUSTER; GENE EXPRESSION; HUMAN; HUMAN CELL; HYPOXIA; IL17BR GENE; IL1A GENE; IL1RN GENE; IL23A GENE; INFLAMMATION; MEMORY T LYMPHOCYTE; MIF GENE; MONOCYTE; NEUTROPHIL; NUCLEOTIDE SEQUENCE; OPN GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; RPS19 GENE; THBS1 GENE; UPREGULATION; VEGFA GENE;

CELL DIFFERENTIATION; CELL HYPOXIA; CELL MOVEMENT; CELLS, CULTURED; CELLULAR MICROENVIRONMENT; CHEMOKINES; CYTOKINES; DENDRITIC CELLS; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, CELLULAR; INFLAMMATION MEDIATORS; MONOCYTES; NEOVASCULARIZATION, PATHOLOGIC; OSTEOGENESIS; OSTEOPONTIN; TRANSCRIPTOME; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84870300113     PISSN: 01712985     EISSN: 18783279     Source Type: Journal    
DOI: 10.1016/j.imbio.2012.02.002     Document Type: Article

References (72)

1. Adema G.J., Hartgers F., Verstraten R., de Vries E., Marland G., Menon S., Foster J., Xu Y., Nooyen P., McClanahan T., Bacon K.B., Figdor C.G. A dendritic-cell-derived C-C chemokine that preferentially attracts naive T cells. Nature 1997, 387:713-717.
2. Akhavani M.A., Madden L., Buysschaert I., Sivakumar B., Kang N., Paleolog E.M. Hypoxia upregulates angiogenesis and synovial cell migration in rheumatoid arthritis. Arthritis Res. Ther. 2009, 11:R64.
3. Allavena P., Sica A., Vecchi A., Locati M., Sozzani S., Mantovani A. The chemokine receptor switch paradigm and dendritic cell migration: its significance in tumor tissues. Immunol. Rev. 2000, 177:141-149.
4. Baggiolini M., Loetscher P. Chemokines in inflammation and immunity. Immunol. Today 2000, 21:418-420.
5. Banchereau J., Briere F., Caux C., Davoust J., Lebecque S., Liu Y.J., Pulendran B., Palucka K. Immunobiology of dendritic cells. Annu. Rev. Immunol. 2000, 18:767-811.
6. Battaglia F., Delfino S., Merello E., Puppo M., Piva R., Varesio L., Bosco M.C. Hypoxia transcriptionally induces macrophage-inflammatory protein-3{alpha}/CCL-20 in primary human mononuclear phagocytes through nuclear factor (NF)-{kappa}B. J. Leukoc. Biol. 2008, 83:648-662.
7. Ben Baruch A. Inflammation-associated immune suppression in cancer: the roles played by cytokines, chemokines and additional mediators. Semin. Cancer Biol. 2006, 16:38-52.
8. Beyer C., Schett G., Gay S., Distler O., Distler J.H. Hypoxia. Hypoxia in the pathogenesis of systemic sclerosis. Arthritis Res. Ther. 2009, 11:220.
9. Bizzarri C., Beccari A.R., Bertini R., Cavicchia M.R., Giorgini S., Allegretti M. ELR+ CXC chemokines and their receptors (CXC chemokine receptor 1 and CXC chemokine receptor 2) as new therapeutic targets. Pharmacol. Ther. 2006, 112:139-149.
10. Bjornheden T., Levin M., Evaldsson M., Wiklund O. Evidence of hypoxic areas within the arterial wall in vivo. Arterioscler. Thromb. Vasc. Biol. 1999, 19:870-876.
11. Bosco M.C., Varesio L. Monocytic cell gene regulation by the hypoxic synovial environment in juvenile idiopathic arthritis: implications for disease pathogenesis. J. Clin. Rheumatol. Musculoskeletal Med. 2010, 1:47-55.
12. Bosco M.C., Delfino S., Ferlito F., Battaglia F.P.M., Gregorio A., Gambini C., Gattorno M., Martini A., Varesio L. Hypoxic synovial environment and expression of macrophage inflammatory protein MIP-3α/CCL20 in Juvenile Idiopathic Arthritis. Arthritis Rheum. 2008, 58:1833-1838.
13. Bosco M.C., Pierobon D., Blengio F., Raggi F., Vanni C., Gattorno M., Eva A., Novelli F., Cappello P., Giovarelli M., Varesio L. Hypoxia modulates the gene expression profile of immunoregulatory receptors in human mature dendritic cells: identification of TREM-1 as a novel hypoxic marker in vitro and in vivo. Blood 2011, 117:2625-2639.
14. Bosco M.C., Puppo M., Blengio F., Fraone T., Cappello P., Giovarelli M., Varesio L. Monocytes and dendritic cells in a hypoxic environment: spotlights on chemotaxis and migration. Immunobiology 2008, 213:733-749.
15. Bosco M.C., Puppo M., Pastorino S., Mi Z., Melillo G., Massazza S., Rapisarda A., Varesio L. Hypoxia selectively inhibits monocyte chemoattractant protein-1 production by macrophages. J. Immunol. 2004, 172:1681-1690.
16. Bosco M.C., Puppo M., Santangelo C., Anfosso L., Pfeffer U., Fardin P., Battaglia F., Varesio L. Hypoxia modifies the transcriptome of primary human monocytes: modulation of novel immune-related genes and identification of CC-chemokine ligand 20 as a new hypoxia-inducible gene. J. Immunol. 2006, 177:1941-1955.
17. Bosco M.C., Reffo G., Puppo M., Varesio L. Hypoxia inhibits the expression of the CCR5 chemokine receptor in macrophages. Cell. Immunol. 2004, 228:1-7.
18. Brand S. Crohn's disease: Th1 Th17 or both? The change of a paradigm: new immunological and genetic insights implicate Th17 cells in the pathogenesis of Crohn's disease. Gut 2009, 58:1152-1167.
19. Caldwell C.C., Kojima H., Lukashev D., Armstrong J., Farber M., Apasov S.G., Sitkovsky M.V. Differential effects of physiologically relevant hypoxic conditions on T lymphocyte development and effector functions. J. Immunol. 2001, 167:6140-6149.
20. Cavanagh L.L., Von Andrian U.H. Travellers in many guises: the origins and destinations of dendritic cells. Immunol. Cell Biol. 2002, 80:448-462.
21. Cramer T., Yamanishi Y., Clausen B.E., Förster I., Pawlinski R., Mackman N., Haase V.H., Jaenisch R., Corr M., Nizet V., Firestein G.S., Gerber H.-P., Ferrara N., Johnson R.S. HIF-1α is essential for myeloid cell-mediated inflammation. Cell 2003, 112:645-657.
22. Cummins E.P., Taylor C.T. Hypoxia-responsive transcription factors. Pflugers Arch. 2005, 450:363-371.
23. Di Cesare A., Di Meglio P., Nestle F.O. The IL-23/Th17 axis in the immunopathogenesis of psoriasis. J. Invest. Dermatol. 2009, 129:1339-1350.
24. Dinarello C.A. Interleukin-1 in the pathogenesis and treatment of inflammatory diseases. Blood 2011, 117:3720-3732.
25. Distler J.H., Wenger R.H., Gassmann M., Kurowska M., Hirth A., Gay S., Distler O. Physiologic responses to hypoxia and implications for hypoxia-inducible factors in the pathogenesis of rheumatoid arthritis. Arthritis Rheum. 2004, 50:10-23.
26. Elia A.R., Cappello P., Puppo M., Fraone T., Vanni C., Eva A., Musso T., Novelli F., Varesio L., Giovarelli M. Human dendritic cells differentiated in hypoxia down-modulate antigen uptake and change their chemokine expression profile. J. Leukoc. Biol. 2008, 84:1472-1482.
27. Evans S.M., Hahn S.M., Magarelli D.P., Koch C.J. Hypoxic heterogeneity in human tumors: EF5 binding, vasculature, necrosis, and proliferation. Am. J. Clin. Oncol. 2001, 24:467-472.
28. Fang H.Y., Hughes R., Murdoch C., Coffelt S.B., Biswas S.K., Harris A.L., Johnson R.S., Imityaz H.Z., Simon M.C., Fredlund E., Greten F.R., Rius J., Lewis C.E. Hypoxia-inducible factors 1 and 2 are important transcriptional effectors in primary macrophages experiencing hypoxia. Blood 2009, 114:844-859.
29. Forssmann U., Delgado M.B., Uguccioni M., Loetscher P., Garotta G., Baggiolini M. CKbeta8, a novel CC chemokine that predominantly acts on monocytes. FEBS Lett. 1997, 408:211-216.
30. Gudjonsson J.E., Johnston A., Sigmundsdottir H., Valdimarsson H. Immunopathogenic mechanisms in psoriasis. Clin. Exp. Immunol. 2004, 135:1-8.
31. Jantsch J., Chakravortty D., Turza N., prechtel A.T., Buchholtz B., Gerlach R.G., Volke M., Glasner J., Warnecke C., Wiesener M.S., Eckardt K.U., Steinkasserer A., Hensel M., William C. Hypoxia and hypoxia-inducible factor-1{alpha} modulate lipopolysaccharide-induced dendritic cell activation and function. J. Immunol. 2008, 180:4697-4705.
32. Jögi A., Øra I., Nilsson H., Lindeheim A., Makino Y., Poellinger L., Axelson H., Påhlman S. Hypoxia alters gene expression in human neuroblastoma cells toward an immature and neural crest-like phenotype. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:7021-7026.
33. Koch A.E. Chemokines and their receptors in rheumatoid arthritis: future targets?. Arthritis Rheum. 2005, 52:710-721.
34. Landi A., Babiuk L.A., van Drunen Littel-van den Hurk S. Dendritic cells matured by a prostaglandin E2-containing cocktail can produce high levels of IL-12p70 and are more mature and Th1-biased than dendritic cells treated with TNF-alpha or LPS. Immunobiology 2011, 216:649-662.
35. Lanzavecchia A., Sallusto F. Regulation of T cell immunity by dendritic cells. Cell 2001, 106:263-266.
36. Laoui D., Van Overmeire E., Movahedi K., Van den B.J., Schouppe E., Mommer C., Nikolaou A., Morias Y., De Baetselier P., Van Ginderachter J.A. Mononuclear phagocyte heterogeneity in cancer: different subsets and activation states reaching out at the tumor site. Immunobiology 2011, 216:1192-1202.
37. Lebre M.C., Tak P.P. Dendritic cells in rheumatoid arthritis: which subset should be used as a tool to induce tolerance?. Hum. Immunol. 2009, 70:321-324.
38. Lin A., Schildknecht A., Nguyen L.T., Ohashi P.S. Dendritic cells integrate signals from the tumor microenvironment to modulate immunity and tumor growth. Immunol. Lett. 2010, 127:77-84.
39. Mancino A., Schioppa T., Larghi P., Pasqualini F., Nebuloni M., Chen I.H., Sozzani S., Austyn J.M., Mantovani A., Sica A. Divergent effects of hypoxia on dendritic cell functions. Blood 2008, 112:3723-3734.
40. Mantovani A., Savino B., Locati M., Zammataro L., Allavena P., Bonecchi R. The chemokine system in cancer biology and therapy. Cytokine Growth Factor Rev. 2010, 21:27-39.
41. Melillo G. Hypoxia: jump-starting inflammation. Blood 2011, 117:2561-2562.
42. Mellman I., Steinman R.M. Dendritic cells: specialized and regulated antigen processing machines. Cell 2001, 106:255-258.
43. Moser M., Murphy K.M. Dendritic cell regulation of TH1-TH2 development. Nat. Immunol. 2000, 1:199-205.
44. Murakami M., Iwai S., Hiratsuka S., Yamauchi M., Nakamura K., Iwakura Y., Shibuya M. Signaling of vascular endothelial growth factor receptor-1 tyrosine kinase promotes rheumatoid arthritis through activation of monocytes/macrophages. Blood 2006, 108:1849-1856.
45. Murdoch C., Giannoudis A., Lewis C.E. Mechanisms regulating the recruitment of macrophages into hypoxic areas of tumors and other ischemic tissues. Blood 2004, 104:2224-2234.
46. Muz B., Khan M.N., Kiriakidis S., Paleolog E.M. Hypoxia. The role of hypoxia and HIF-dependent signalling events in rheumatoid arthritis. Arthritis Res. Ther. 2009, 11:201.
47. Nistala K., Moncrieffe H., Newton K.R., Varsani H., Hunter P., Wedderburn L.R. Interleukin-17-producing T cells are enriched in the joints of children with arthritis, but have a reciprocal relationship to regulatory T cell numbers. Arthritis Rheum. 2008, 58:875-887.
48. Nizet V., Johnson R.S. Interdependence of hypoxic and innate immune responses. Nat. Rev. Immunol. 2009, 9:609-617.
49. O'Regan A.W., Nau G.J., Chupp G.L., Berman J.S. Osteopontin (Eta-1) in cell-mediated immunity: teaching an old dog new tricks. Immunol. Today 2000, 21:475-478.
50. Ogino T., Onishi H., Suzuki H., Morisaki T., Tanaka M., Katano M. Inclusive estimation of complex antigen presentation functions of monocyte-derived dendritic cells differentiated under normoxia and hypoxia conditions. Cancer Immunol. Immunother. 2011.
51. Pharoah D.S., Varsani H., Tatham R.W., Newton K.R., de Jager W., Prakken B.J., Klein N., Wedderburn L.R. Expression of the inflammatory chemokines CCL5 CCL3 and CXCL10 in juvenile idiopathic arthritis, and demonstration of CCL5 production by an atypical subset of CD8+ T cells. Arthritis Res. Ther. 2006, 8:R50.
52. Rama I., Brune B., Torras J., Koehl R., Cruzado J.M., Bestard O., Franquesa M., Lloberas N., Weigert A., Herrero-Fresneda I., Gulias O., Grinyo J.M. Hypoxia stimulus: an adaptive immune response during dendritic cell maturation. Kidney Int. 2008, 73:816-825.
53. Ricciardi A., Elia A.R., Cappello P., Puppo M., Vanni C., Fardin P., Eva A., Munroe D., Wu X., Giovarelli M., Varesio L. Transcriptome of hypoxic immature dendritic cells: modulation of chemokine/receptor expression. Mol. Cancer Res. 2008, 6:175-185.
54. Roccaro A.M., Russo F., Cirulli T., Di Pietro G., Vacca A., Dammacco F. Antiangiogenesis for rheumatoid arthritis. Curr. Drug Targets. Inflamm. Allergy 2005, 4:27-30.
55. Rossi M., Young J.W. Human dendritic cells: potent antigen-presenting cells at the crossroads of innate and adaptive immunity. J. Immunol. 2005, 175:1373-1381.
56. Rot A., Von Andrian U.H. Chemokines in innate and adaptive host defense: basic chemokinese grammar for immune cells. Annu. Rev. Immunol. 2004, 22:891-928.
57. Sallusto F., Lanzavecchia A., Mackay C.R. Chemokines and chemokine receptors in T-cell priming and Th1/Th2-mediated responses. Immunol. Today 1998, 19:568-574.
58. Santos L.L., Morand E.F. Macrophage migration inhibitory factor: a key cytokine in RA SLE and atherosclerosis. Clin. Chim. Acta 2009, 399:1-7.
59. Schioppa T., Uranchimeg B., Saccani A., Biswas S.K., Doni A., Rapisarda A., Bernasconi S., Saccani S., Nebuloni M., Vago L., Mantovani A., Melillo G., Sica A. Regulation of the chemokine receptor CXCR4 by hypoxia. J. Exp. Med. 2003, 198:1391-1402.
60. Schutyser E., Struyf S., Van Damme J. The CC chemokine CCL20 and its receptor CCR6. Cytokine Growth Factor Rev. 2003, 14:409-426.
61. Semenza G.L. Oxygen sensing, homeostasis, and disease. N. Engl. J. Med. 2001, 365:537-547.
62. Senger D.R., Ledbetter S.R., Claffey K.P., Papadopoulos-Sergiou A., Peruzzi C.A., Detmar M. Stimulation of endothelial cell migration by vascular permeability factor/vascular endothelial growth factor through cooperative mechanisms involving the alphavbeta3 integrin, osteopontin, and thrombin. Am. J. Pathol. 1996, 149:293-305.
63. Sica A., Melillo G., Varesio L. Hypoxia: a double-edged sword of immunity. J. Mol. Med. (Berl) 2011, 89:657-665.
64. Sitkovsky M., Lukashev D. Regulation of immune cells by local-tissue oxygen tension: HIF1 alpha and adenosine receptors. Nat. Rev. Immunol. 2008, 5:712-721.
65. Staples K.J., Sotoodehnejadnematalahi F., Pearson H., Frankenberger M., Francescut L., Ziegler-Heitbrock L., Burke B. Monocyte-derived macrophages matured under prolonged hypoxia transcriptionally up-regulate HIF-1alpha mRNA. Immunobiology 2011, 216:832-839.
66. 2 tension measurements. Cancer Res. 1991, 51:3316-3322.
67. Vissers J.L., Hartgers F.C., Lindhout E., Teunissen M.B., Figdor C.G., Adema G.J. Quantitative analysis of chemokine expression by dendritic cell subsets in vitro and in vivo. J. Leukoc. Biol. 2001, 69:785-793.
68. Vulcano M., Struyf S., Scapini P., Cassatella M., Bernasconi S., Bonecchi R., Calleri A., Penna G., Adorini L., Luini W., Mantovani A., Van Damme J., Sozzani S. Unique regulation of CCL18 production by maturing dendritic cells. J. Immunol. 2003, 170:3843-3849.
69. Wedderburn L.R., Robinson N., Patel A., Varsani H., Woo P. Selective recruitment of polarized T cells expressing CCR5 and CXCR3 to the inflamed joints of children with juvenile idiopathic arthritis. Arthritis Rheum. 2000, 43:765-774.
70. Xu G., Nie H., Li N., Zheng W., Zhang D., Feng G., Ni L., Xu R., Hong J., Zhang J.Z. Role of osteopontin in amplification and perpetuation of rheumatoid synovitis. J. Clin. Invest. 2005, 115:1060-1067.
71. Yang M., Ma C., Liu S., Sun J., Shao Q., Gao W., Zhang Y., Li Z., Xie Q., Dong Z., Qu X. Hypoxia skews dendritic cells to a T helper type 2-stimulating phenotype and promotes tumour cell migration by dendritic cell-derived osteopontin. Immunology 2009, 128:e237-e249.
72. Zampetaki A., Mitsialis S.A., Pfeilschifter J., Kourembanas S. Hypoxia induces macrophage inflammatory protein-2 (MIP-2) gene expression in murine macrophages via NF-kappaB: the prominent role of p42/p44 and PI3 kinase pathways. FASEB J. 2004, 18:1090-1092.