Transcriptional profiles during the differentiation and maturation of monocyte-derived dendritic cells, analyzed using focused microarrays

• Autorzy: Zhong W , Fei M. , Zhu Y. , Zhang X.
• Języki publikacji: EN

Abstrakty

EN

Dendritic cells (DC) are professional antigen-presenting cells capable of initiating primary immune responses. They have been intensively studied and are used in both basic immunology research and clinical immunotherapy. However, the genetic pathways leading to DC differentiation and maturation remain poorly understood. Using focused microarrays with oligonucletotide probes for 120 genes encoding co-stimulatory molecules, chemokines, chemokine receptors, cytokines, cytokine receptors, TLRs, and several other related molecules, we analyzed the kinetics of gene expression for the overall differentiation process of monocytes into mature DC. In parallel, we compared the transcriptional profiles in DC maturation in the presence of LPS, TNF-α or trimeric CD40L. We found similar transcriptional profiles for early immature DC and immature DC, respectively generated by culturing monocytes with GM-CSF and IL-4 for three or six days. We identified sets of common and stimuli-specific genes, the expression of which changed following stimulation with LPS, TNF-α or CD40L. A dynamic analysis of the entire DC differentiation and maturation process showed that some important inflammatory and constitutive chemokines are transcribed in both immature and mature DC. The correlative expression kinetics of the gene pairs IL1R1/IL1R2, IL15/IL15RA, DC-SIGN/ICAM-2 and DC-SIGN/ICAM-3 imply that they all play crucial roles in mediating DC functions. Thus, our analysis with focused microarrays shed light on the transcriptional kinetics of DC differentiation and maturation, and this method may also prove useful for identifying novel marker genes involved in DC functions.

Słowa kluczowe

EN

transcriptional profile; differentiation; maturation; monocyte-derived dendritic cell; microarray; dendritic cell; antigen; immune response; immunotherapy

• Wydawca: -
• Czasopismo: Cellular and Molecular Biology Letters
• Rocznik: 2009
• Tom: 14
• Numer: 4
• Opis fizyczny: p.587-608,fig.,ref.

Twórcy

autor

Zhong W

• Soochow University, Suzhou, P.R.China

autor

Fei M.

autor

Zhu Y.

autor

Zhang X.

Bibliografia

• 1. Banchereau, J. and Steinman, R. M. Dendritic cells and the control of immunity. Nature 392 (1998) 245-251. DOI: 10.1038/32588.
• 2. Caux, C., Dezutter-Dambuyant, C., Schmitt, D. and Banchereau, J. GM-CSF and TNF-alpha cooperate in the generation of dendritic Langerhans cells. Nature 360 (1992) 258-261. DOI: 10.1038/360258a0.
• 3. Reid, C., Stackpoole, A., Meager, A. and Tikerpae, J. Interactions of tumor necrosis factor with granulocyte-macrophage colony-stimulating factor and other cytokines in the regulation of dendritic cell growth in vitro from early bipotent CD34 progenitors in human bone marrow. J. Immunol. 149 (1992) 2681-2688.
• 4. Avigan, D. Dendritic cells: development, function and potential use for cancer immunotherapy. Blood Rev. 13 (1999) 51-64. DOI: 10.1016/S0268- 960X(99)90023-1.
• 5. Felzmann, T., Witt, V., Wimmer, D., Ressmann, G., Wagner, D., Paul, P., Huttner, K. and Fritsch, G. Monocyte enrichment from leukapharesis products for the generation of DCs by plastic adherence, or by positive or negative selection. Cytotherapy 5 (2003) 391-398. DOI: 10.1080/ 14653240310003053.
• 6. Sallusto, F., Cella, M., Danieli, C. and Lanzavecchia, A. Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products. J. Exp. Med. 182 (1995) 389-400.
• 7. Cella, M., Scheidegger, D., Palmer-Lehmann, K., Lane, P., Lanzavecchia, A. and Alber, G. Ligation of CD40 on dendritic cells triggers production of high levels of interleukin-12 and enhances T cell stimulatory capacity: T-T help via APC activation. J. Exp. Med. 184 (1996) 747-752.
• 8. de Jong, E.C., Vieira, P.L., Kalinski, P., Schuitemaker, J.H., Tanaka, Y., Wierenga, E.A., Yazdanbakhsh, M. and Kapsenberg, M.L. Microbial compounds selectively induce Th1 cell-promoting or Th2 cell-promoting dendritic cells in vitro with diverse th cell-polarizing signals. J. Immunol. 168 (2002) 1704-1709.
• 9. Vieira, P.L., de Jong, E.C., Wierenga, E.A., Kapsenberg, M.L. and Kaliński, P. Development of Th1-inducing capacity in myeloid dendritic cells requires environmental instruction. J. Immunol. 164 (2000) 4507-4512.
• 10. Le Naour, F., Hohenkirk, L., Grolleau, A., Misek, D.E., Lescure, P., Geiger, J.D., Hanash, S. and Beretta, L. Profiling changes in gene expression during differentiation and maturation of monocyte-derived dendritic cells using both oligonucleotide microarrays and proteomics. J. Biol. Chem. 276 (2001) 17920-17931. DOI: 10.1074/jbc.M100156200.
• 11. Türeci, O., Bian, H., Nestle, F.O., Raddrizzani, L., Rosinski, J.A., Tassis, A., Hilton, H., Walstead, M., Sahin, U. and Hammer, J. Cascades of transcriptional induction during dendritic cell maturation revealed by genome-wide expression analysis. FASEB J. 17 (2003) 836-847.
• 12. Moschella, F., Maffei, A., Catanzaro, R.P., Papadopoulos, K.P., Skerrett, D., Hesdorffer, C.S. and Harris, P.E. Transcript profiling of human dendritic cells maturation-induced under defined culture conditions: comparison of the effects of tumour necrosis factor alpha, soluble CD40 ligand trimer and interferon gamma. Br. J. Haematol. 114 (2001) 444-457. DOI: 10.1046/j.1365-2141.2001.02953.x.
• 13. Messmer, D., Messmer, B. and Chiorazzi, N. The global transcriptional maturation program and stimuli-specific gene expression profiles of human myeloid dendritic cells. Int. Immunol. 15 (2003) 491-503.
• 14. Lapteva, N., Ando, Y., Nieda, M., Hohjoh, H., Okai, M., Kikuchi, A., Dymshits, G., Ishikawa, Y., Juji, T. and Tokunaga, K. Profiling of genes expressed in human monocytes and monocyte-derived dendritic cells using cDNA expression array. Br. J. Haematol. 114 (2001) 191-197. DOI: 10.1046/j.1365-2141.2001.02910.x.
• 15. Shin, J.W., Jin, P., Fan, Y., Slezak, S., David-Ocampo, V., Khuu, H.M., Read, E.J., Wang, E., Marincola, F.M. and Stroncek, D.F. Evaluation of gene expression profiles of immature dendritic cells prepared from peripheral blood mononuclear cells. Transfusion 48 (2008) 647-657. DOI: 10.1111/j.1537-2995.2007.01615.x.
• 16. Lipscomb, M.F. and Masten, B.J. Dendritic cells: immune regulators in health and disease. Physiol. Rev. 82 (2002) 97-130. DOI: 10.1152/physrev.00023.2001.
• 17. Banchereau, J., Briere, F., Caux, C., Davoust, J., Lebecque, S., Liu, Y.J., Pulendran, B. and Palucka, K. Immunobiology of dendritic cells. Annu. Rev. Immunol. 18 (2000) 767-811. DOI: 10.1146/annurev.immunol. 18.1.767.
• 18. Jirmanova, L., Jankovic, D., Fornace, A.J. Jr. and Ashwell, J.D. Gadd45alpha regulates p38-dependent dendritic cell cytokine production and Th1 differentiation. J. Immunol. 178 (2007) 4153-4158.
• 19. Eisen, M.B., Spellman, P.T., Brown, P.O. and Botstein, D. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. USA 95 (1998) 14863-14868.
• 20. Soukas, A., Cohen, P., Socci, N.D. and Friedman, J.M. Leptin-specific patterns of gene expression in white adipose tissue. Genes Dev. 14 (2000) 963-980.
• 21. Granucci, F., Vizzardelli, C., Virzi, E., Rescigno, M. and RicciardiCastagnoli, P. Transcriptional reprogramming of dendritic cells by differentiation stimuli. Eur. J. Immunol. 31 (2001) 2539-2546. DOI: 10.1002/1521-4141(200109)31:9<2539::AID-IMMU2539> 3.0.CO;2-9.
• 22. Skelton, L., Cooper, M., Murphy, M. and Platt, A. Human immature monocyte-derived dendritic cells express the G protein-coupled receptor GPR105 (KIAA001, P2Y14) and increase intracellular calcium in response to its agonist uridine diphosphoglucose. J. Immunol. 171 (2003) 1941-1949.
• 23. Tang, Z. and Saltzman, A. Understanding human dendritic cell biology through gene profiling. Inflamm. Res. 53 (2004) 424-441. DOI: 10.1007/s00011-004-1283-z.
• 24. Lindstedt, M., Johansson-Lindbom, B. and Borrebaeck, C.A. Global reprogramming of dendritic cells in response to a concerted action of inflammatory mediators. Int. Immunol. 14 (2002) 1203-1213.
• 25. Kanazawa, N., Nakamura, T., Tashiro, K., Muramatsu, M., Morita, K., Yoneda, K., Inaba, K., Imamura, S. and Honjo, T. Fractalkine and macrophage-derived chemokine: T cell-attracting chemokines expressed in T cell area dendritic cells. Eur. J. Immunol. 29 (1999) 1925-1932. DOI: 10.1002/(SICI)1521-4141(199906)29:06<1925::AID-IMMU1925>3.0.CO;2-U.
• 26. Papadopoulos, E.J., Sassetti, C., Saeki, H., Yamada, N., Kawamura, T., Fitzhugh, D.J., Saraf, M.A., Schall, T., Blauvelt, A., Rosen, S.D. and Hwang, S.T. Fractalkine, a CX3C chemokine, is expressed by dendritic cells and is up-regulated upon dendritic cell maturation. Eur. J. Immunol. 29 (1999) 2551-2559. DOI: 10.1002/(SICI)1521-4141(199908)29:08<2551:: AID-IMMU2551>3.0.CO;2-T.
• 27. Sallusto, F., Palermo, B., Lenig, D., Miettinen, M., Matikainen, S., Julkunen, I., Forster, R., Burgstahler, R., Lipp, M. and Lanzavecchia, A. Distinct patterns and kinetics of chemokine production regulate dendritic cell function. Eur. J. Immunol. 29 (1999) 1617-1625. DOI: 10.1002/(SICI)1521- 4141(199905)29:05<1617::AID-IMMU1617>3.0.CO;2-3.
• 28. Alderson, M.R., Armitage, R.J., Tough, T.W., Strockbine, L., Fanslow, W.C. and Spriggs, M.K. CD40 expression by human monocytes: regulation by cytokines and activation of monocytes by the ligand for CD40. J. Exp. Med. 178 (1993) 669-674.
• 29. Relloso, M., Puig-Kröger, A., Pello, O.M., Rodríguez-Fernández, J.L., de la Rosa, G., Longo, N., Navarro, J., Muñoz-Fernández, M.A., Sánchez-Mateos, P. and Corbí, A.L. DC-SIGN (CD209) expression is IL-4 dependent and is negatively regulated by IFN, TGF-β, and anti-inflammatory agents. J. Immunol. 168 (2002) 2634-2643.
• 30. Dietz, A.B., Bulur, P.A., Knutson, G.J., Matasić, R. and Vuk-Pavlović, S. Maturation of human monocyte-derived dendritic cells studied by microarray hybridization. Biochem. Biophys. Res. Commun. 275 (2000) 731-738. DOI: s10.1006/bbrc.2000.3372.
• 31. Hieshima, K., Imai, T., Opdenakker, G., Van Damme, J., Kusuda, J., Tei, H., Sakaki, Y., Takatsuki, K., Miura, R., Yoshie, O. and Nomiyama, H. Molecular cloning of a novel human CC chemokine liver and activationregulated chemokine (LARC) expressed in liver. Chemotactic activity for lymphocytes and gene localization on chromosome 2. J. Biol. Chem. 272 (1997) 5846-5853.
• 32. Homey, B., Dieu-Nosjean, M.C., Wiesenborn, A., Massacrier, C., Pin, J.J., Oldham, E., Catron, D., Buchanan, M.E., Müller, A., deWaal Malefyt, R., Deng, G., Orozco, R., Ruzicka, T., Lehmann, P., Lebecque, S., Caux, C. and Zlotnik, A. Up-regulation of macrophage inflammatory protein-3 alpha/CCL20 and CC chemokine receptor 6 in psoriasis. J. Immunol. 164 (2000) 6621-6632.
• 33. Dauer, M., Obermaier, B., Herten, J., Haerle, C., Pohl, K., Rothenfusser, S., Schnurr, M., Endres, S. and Eigler, A. Mature dendritic cells derived from human monocytes within 48 hours: a novel strategy for dendritic cell differentiation from blood precursors, J. Immunol. 170 (2003) 4069-4076.
• 34. Olas, K., Butterweck, H., Teschner, W., Schwarz, H.P. and Reipert, B. Immunomodulatory properties of human serum immunoglobulin A: antiinflammatory and pro-inflammatory activities in human monocytes and peripheral blood mononuclear cells. Clin. Exp. Immunol. 140 (2005) 478-490. DOI: 10.1111/j.1365-2249.2005.02779.x.
• 35. Lu, Y., Liu, Y., Fukuda, K., Nakamura, Y., Kumagai, N. and Nishida, T. Inhibition by triptolide of chemokine, proinflammatory cytokine, and adhesion molecule expression induced by lipopolysaccharide in corneal fibroblasts. Invest. Ophthalmol. Vis. Sci. 47 (2006) 3796-3800. DOI: 10.1167/iovs.06-0319.
• 36. Blanco, P., Palucka, A.K., Pascual, V. and Banchereau, J. Dendritic cells and cytokines in human inflammatory and autoimmune diseases. Cytokine Growth Factor Rev. 19 (2008) 41-52. DOI: 10.1016/j.cytogfr.2007.10.004.
• 37. Nolte, M.A., Leibundgut-Landmann, S., Joffre, O. and Reis e Sousa, C. Dendritic cell quiescence during systemic inflammation driven by LPS stimulation of radioresistant cells in vivo. J. Exp. Med. 204 (2007) 1487-1501. DOI: 10.1084/jem.20070325.
• 38. Anisowicz, A., Messineo, M., Lee, S.W. and Sager, R. An NF-kappa B-like transcription factor mediates IL-1/TNF-alpha induction of gro in human fibroblasts. J. Immunol. 147 (1991) 520-527.
• 39. Bunting, K., Rao, S., Hardy, K., Woltring, D., Denyer, G.S., Wang, J., Gerondakis, S. and Shannon, M.F. Genome-wide analysis of gene expression in T cells to identify targets of the NF-kappa B transcription factor c-Rel. J. Immunol. 178 (2007) 7097-7109.
• 40. Zhan, Q., Lord, K.A., Alamo, I. Jr., Hollander, M.C., Carrier, F., Ron, D., Kohn, K.W., Hoffman, B., Liebermann, D.A. and Fornace, A.J. Jr. The gadd and MyD genes define a novel set of mammalian genes encoding acidic proteins that synergistically suppress cell growth. Mol. Cell. Biol. 14 (1994) 2361-2371.
• 41. Smith, M.L., Ford, J.M., Hollander, M.C., Bortnick, R.A., Amundson, S.A., Seo, Y.R., Deng, C.X., Hanawalt, P.C. and Fornace, A.J. Jr. p53-mediated DNA repair responses to UV radiation: studies of mouse cells lacking p53, p21, and/or gadd45 genes. Mol. Cell. Biol. 20 (2000) 3705-3714.
• 42. Wang, X.W., Zhan, Q., Coursen, J.D., Khan, M.A., Kontny, H.U., Yu, L., Hollander, M.C., O'Connor, P.M., Fornace, A.J. Jr. and Harris, C.C. GADD45 induction of a G2/M cell cycle checkpoint. Proc. Nat. Acad. Sci. USA 96 (1999) 3706-3711.
• 43. Takekawa, M. and Saito, H. A family of stress-inducible GADD45-like proteins mediate activation of the stress-responsive MTK1/MEKK4 MAPKKK. Cell 95 (1998) 521-530. DOI: 10.1016/S0092-8674(00)81619-0.
• 44. Frasca, L., Fedele, G., Deaglio, S., Capuano, C., Palazzo, R., Vaisitti, T., Malavasi, F. and Ausiello, C.M. CD38 orchestrates migration, survival, and Th1 immune response of human mature dendritic cells. Blood 107 (2006) 2392-2399. DOI: 10.1182/blood-2005-07-2913.
• 45. Kaliński, P., Schuitemaker, J.H., Hilkens, C.M., Wierenga, E.A. and Kapsenberg, M.L. Final maturation of dendritic cells is associated with impaired responsiveness to IFN-gamma and to bacterial IL-12 inducers: decreased ability of mature dendritic cells to produce IL-12 during the interaction with Th cells. J. Immunol. 162 (1999) 3231-3236.
• 46. De Smaele, E., Zazzeroni, F., Papa, S., Nguyen, D.U., Jin, R., Jones, J., Cong, R. and Franzoso, G. Induction of gadd45beta by NF-kappaB downregulates pro-apoptotic JNK signalling. Nature 414 (2001) 308-313. DOI: 10.1038/35104560.
• 47. Zazzeroni, F., Papa, S., Algeciras-Schimnich, A., Alvarez, K., Melis, T., Bubici, C., Majewski, N., Hay, N., De Smaele, E., Peter, M.E. and Franzoso, G. Gadd45 beta mediates the protective effects of CD40 costimulation against Fas-induced apoptosis. Blood 102 (2003) 3270-3279. DOI: 10.1182/blood-2003-03-0689.
• 48. Josien, R., Li, H.L., Ingulli, E., Sarma, S., Wong, B.R., Vologodskaia, M., Steinman, R.M. and Choi, Y. TRANCE, a tumor necrosis factor family member, enhances the longevity and adjuvant properties of dendritic cells in vivo. J. Exp. Med. 191 (2000) 495-502.
• 49. Wong, B.R., Josien, R., Lee, S.Y., Sauter, B., Li, H.L., Steinman, R.M. and Choi, Y. TRANCE (tumor necrosis factor [TNF]-related activation-induced cytokine), a new TNF family member predominantly expressed in T cells, is a dendritic cell-specific survival factor. J. Exp. Med. 186 (1997) 2075-2080.
• 50. Dinarello, C.A. Biologic basis for interleukin-1 in disease. Blood 87 (1996) 2095-2147.
• 51. Neumann, D., Kollewe, C., Martin, M.U. and Boraschi, D. The membrane form of the type II IL-1 receptor accounts for inhibitory function. J. Immunol. 165 (2000) 3350-3357.
• 52. Orlando, S., Polentarutti, N. and Mantovani, A. Selectivity release of the type II decoy IL-1 receptor. Cytokine 12 (2000) 1001-1006. DOI: 10.1006/cyto.1999.0601.
• 53. Lang, D., Knop, J., Wesche, H., Raffetseder, U., Kurrle, R., Boraschi, D. and Martin, M.U. The type II IL-1 receptor interacts with the IL-1 receptor accessory protein: a novel mechanism of regulation of IL-1 responsiveness. J. Immunol. 161 (1998) 6871-6877.
• 54. O'Neill, L. IL-1 versus TNF in arthritis? Trends Immunol. 22 (2001) 353-354. DOI: 10.1016/S1471-4906(01)01992-5.
• 55. Eriksson, U., Kurrer, M.O., Sonderegger, I., Iezzi, G., Tafuri, A., Hunziker, L., Suzuki, S., Bachmaier, K., Bingisser, R.M., Penninger, J.M. and Kopf, M. Activation of dendritic cells through the interleukin 1 receptor 1 is critical for the induction of autoimmune myocarditis. J. Exp. Med. 197 (2003) 323-331.
• 56. Ferlazzo, G., Pack, M., Thomas, D., Paludan, C., Schmid, D., Strowig, T., Bougras, G., Muller, W.A., Moretta, L. and Münz, C. Distinct 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 (2004) 16606- 16611. DOI: 10.1073/pnas.0407522101.
• 57. Mortier, E., Woo, T., Advincula, R., Gozalo, S. and Ma, A. IL-15R chaperones IL-15 to stable dendritic cell membrane complexes that activate NK cells via trans presentation. J. Exp. Med. 205 (2008) 1213-1225.
• 58. Mattei, F., Schiavoni, G., Belardelli, F. and Tough, D.F. IL-15 is expressed by dendritic cells in response to type I IFN, double-stranded RNA, or lipopolysaccharide and promotes dendritic cell activation. J. Immunol. 167 (2001) 1179-1187.
• 59. Dubois, S.P., Waldmann, T.A. and Müller, J.R. Survival adjustment of mature dendritic cells by IL-15. Proc. Natl. Acad. Sci. USA 102 (2005) 8662-8667. DOI: 10.1073/ pnas.0503360102.
• 60. Geijtenbeek, T.B., Krooshoop, D.J., Bleijs, D.A., van Vliet, S.J., van Duijnhoven, G.C., Grabovsky, V., Alon, R., Figdor, C.G. and van Kooyk, Y. DC-SIGN-ICAM-2 interaction mediates dendritic cell trafficking. Nat. Immunol. 1 (2000) 353-357. DOI: 10.1038/79815.
• 61. Geijtenbeek, T.B., Torensma, R., van Vliet, S.J., van Duijnhoven, G.C., Adema, G.J., van Kooyk, Y. and Figdor, C.G. Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell 100 (2000) 575-585. DOI: 10.1016/S0092- 8674(00)80693-5.