دورية أكاديمية
أعرض في EDS

The tumour microenvironment shapes dendritic cell plasticity in a human organotypic melanoma culture.

التفاصيل البيبلوغرافية
العنوان: The tumour microenvironment shapes dendritic cell plasticity in a human organotypic melanoma culture.
المؤلفون: Di Blasio S; Department of Tumour Immunology, Radboud Institute for Molecular Life Sciences, Radboud University Medical Center, Nijmegen, The Netherlands.; Tumour-Host Interaction Lab, The Francis Crick Institute, London, UK., van Wigcheren GF; Department of Tumour Immunology, Radboud Institute for Molecular Life Sciences, Radboud University Medical Center, Nijmegen, The Netherlands.; Oncode Institute, Utrecht, The Netherlands., Becker A; Department of Tumour Immunology, Radboud Institute for Molecular Life Sciences, Radboud University Medical Center, Nijmegen, The Netherlands., van Duffelen A; Department of Tumour Immunology, Radboud Institute for Molecular Life Sciences, Radboud University Medical Center, Nijmegen, The Netherlands.; Oncode Institute, Utrecht, The Netherlands., Gorris M; Department of Tumour Immunology, Radboud Institute for Molecular Life Sciences, Radboud University Medical Center, Nijmegen, The Netherlands., Verrijp K; Department of Tumour Immunology, Radboud Institute for Molecular Life Sciences, Radboud University Medical Center, Nijmegen, The Netherlands.; Department of Pathology, Radboud University Medical Center, Nijmegen, The Netherlands., Stefanini I; Division of Biomedical Sciences, The University of Warwick, Coventry, UK.; Department of Life Sciences and Systems Biology, University of Turin, Turin, Italy., Bakker GJ; Department of Cell Biology, Radboud Institute for Molecular Life Sciences, Radboud University Medical Center, Nijmegen, The Netherlands., Bloemendal M; Department of Tumour Immunology, Radboud Institute for Molecular Life Sciences, Radboud University Medical Center, Nijmegen, The Netherlands.; Department of Medical Oncology, Radboud University Medical Center, Nijmegen, The Netherlands., Halilovic A; Department of Tumour Immunology, Radboud Institute for Molecular Life Sciences, Radboud University Medical Center, Nijmegen, The Netherlands.; Department of Pathology, Radboud University Medical Center, Nijmegen, The Netherlands., Vasaturo A; Department of Tumour Immunology, Radboud Institute for Molecular Life Sciences, Radboud University Medical Center, Nijmegen, The Netherlands., Bakdash G; Department of Tumour Immunology, Radboud Institute for Molecular Life Sciences, Radboud University Medical Center, Nijmegen, The Netherlands., Hato SV; Department of Tumour Immunology, Radboud Institute for Molecular Life Sciences, Radboud University Medical Center, Nijmegen, The Netherlands., de Wilt JHW; Department of Surgery, Radboud University Medical Center, Nijmegen, The Netherlands., Schalkwijk J; Department of Dermatology, Radboud University Medical Center, Nijmegen, The Netherlands., de Vries IJM; Department of Tumour Immunology, Radboud Institute for Molecular Life Sciences, Radboud University Medical Center, Nijmegen, The Netherlands., Textor JC; Department of Tumour Immunology, Radboud Institute for Molecular Life Sciences, Radboud University Medical Center, Nijmegen, The Netherlands., van den Bogaard EH; Department of Dermatology, Radboud University Medical Center, Nijmegen, The Netherlands., Tazzari M; Department of Tumour Immunology, Radboud Institute for Molecular Life Sciences, Radboud University Medical Center, Nijmegen, The Netherlands. carl.figdor@radboudumc.nl.; Immunotherapy-Cell Therapy and Biobank Unit, Istituto Scientifico Romagnolo per lo Studio e la Cura dei Tumori (IRST) IRCCS, Meldola, Italy. carl.figdor@radboudumc.nl., Figdor CG; Department of Tumour Immunology, Radboud Institute for Molecular Life Sciences, Radboud University Medical Center, Nijmegen, The Netherlands. marcella.tazzari@irst.emr.it.; Oncode Institute, Utrecht, The Netherlands. marcella.tazzari@irst.emr.it.
المصدر: Nature communications [Nat Commun] 2020 Jun 02; Vol. 11 (1), pp. 2749. Date of Electronic Publication: 2020 Jun 02.
نوع المنشور: Journal Article; Research Support, Non-U.S. Gov't
اللغة: English
بيانات الدورية: Publisher: Nature Pub. Group Country of Publication: England NLM ID: 101528555 Publication Model: Electronic Cited Medium: Internet ISSN: 2041-1723 (Electronic) Linking ISSN: 20411723 NLM ISO Abbreviation: Nat Commun Subsets: MEDLINE
أسماء مطبوعة: Original Publication: [London] : Nature Pub. Group
مواضيع طبية MeSH: Cell Plasticity/*physiology , Dendritic Cells/*metabolism , Melanoma/*metabolism , Tumor Microenvironment/*physiology, Cell Communication ; Cell Survival ; Coculture Techniques ; Fibroblasts/pathology ; Humans ; Keratinocytes/pathology ; Melanoma/immunology ; Melanoma/pathology ; Skin/pathology ; Skin Neoplasms/immunology ; Skin Neoplasms/metabolism ; Skin Neoplasms/pathology ; Tumor Microenvironment/immunology ; Melanoma, Cutaneous Malignant
مستخلص: The tumour microenvironment (TME) forms a major obstacle in effective cancer treatment and for clinical success of immunotherapy. Conventional co-cultures have shed light onto multiple aspects of cancer immunobiology, but they are limited by the lack of physiological complexity. We develop a human organotypic skin melanoma culture (OMC) that allows real-time study of host-malignant cell interactions within a multicellular tissue architecture. By co-culturing decellularized dermis with keratinocytes, fibroblasts and immune cells in the presence of melanoma cells, we generate a reconstructed TME that closely resembles tumour growth as observed in human lesions and supports cell survival and function. We demonstrate that the OMC is suitable and outperforms conventional 2D co-cultures for the study of TME-imprinting mechanisms. Within the OMC, we observe the tumour-driven conversion of cDC2s into CD14 + DCs, characterized by an immunosuppressive phenotype. The OMC provides a valuable approach to study how a TME affects the immune system.
References: Zou, W. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat. Rev. Cancer 5, 263–274 (2005). (PMID: 1577600510.1038/nrc1586)
Pitt, J. M. et al. Targeting the tumor microenvironment: removing obstruction to anticancer immune responses and immunotherapy. Ann. Oncol. 27, 1482–1492 (2016). (PMID: 2706901410.1093/annonc/mdw168)
Klemm, F. & Joyce, J. A. Microenvironmental regulation of therapeutic response in cancer. Trends Cell Biol. 25, 198–213 (2015). (PMID: 2554089410.1016/j.tcb.2014.11.006)
Gajewski, T. F. Failure at the effector phase: immune barriers at the level of the melanoma tumor microenvironment. Clin. Cancer Res. 13, 5256–5261 (2007). (PMID: 1787575310.1158/1078-0432.CCR-07-0892)
Feder-Mengus, C., Ghosh, S., Reschner, A., Martin, I. & Spagnoli, G. C. New dimensions in tumor immunology: what does 3D culture reveal? Trends Mol. Med. 14, 333–340 (2008). (PMID: 1861439910.1016/j.molmed.2008.06.001)
Katt, M. E., Placone, A. L., Wong, A. D., Xu, Z. S. & Searson, P. C. In vitro tumor models: advantages, disadvantages, variables, and selecting the right platform. Front. Bioeng. Biotechnol. 4, 12 (2016). (PMID: 26904541475125610.3389/fbioe.2016.00012)
Hirt, C. et al. “In vitro” 3D models of tumor-immune system interaction. Adv. Drug Deliv. Rev. 79–80, 145–154 (2014). (PMID: 2481921510.1016/j.addr.2014.05.003)
Pauli, C. et al. Personalized in vitro and in vivo cancer models to guide precision medicine. Cancer Disco. 7, 462–477 (2017). (PMID: 10.1158/2159-8290.CD-16-1154)
Choi, Y. et al. Studying cancer immunotherapy using patient-derived xenografts (PDXs) in humanized mice. Exp. Mol. Med. 50, 99 (2018). (PMID: 30089794608285710.1038/s12276-018-0115-0)
Meier, F. et al. Human melanoma progression in skin reconstructs: biological significance of bFGF. Am. J. Pathol. 156, 193–200 (2000). (PMID: 10623667186863910.1016/S0002-9440(10)64719-0)
Li, L., Fukunaga-Kalabis, M. & Herlyn, M. The three-dimensional human skin reconstruct model: a tool to study normal skin and melanoma progression. J. Vis. Exp. 2937, https://doi.org/10.3791/2937 (2011).
Hsu, M.-Y. et al. E-Cadherin expression in melanoma cells restores keratinocyte-mediated growth control and down-regulates expression of invasion-related adhesion receptors. Am. J. Pathol. 156, 1515–1525 (2000). (PMID: 10793063187692310.1016/S0002-9440(10)65023-7)
Syed, D. N. et al. Fisetin inhibits human melanoma cell growth through direct binding to p70S6K and mTOR: findings from 3-D melanoma skin equivalents and computational modeling. Biochem. Pharmacol. 89, 349–360 (2014). (PMID: 24675012411613310.1016/j.bcp.2014.03.007)
Eves, P. et al. Melanoma invasion in reconstructed human skin is influenced by skin cells – investigation of the role of proteolytic enzymes. Clin. Exp. Metastasis 20, 685–700 (2003). (PMID: 1471310310.1023/B:CLIN.0000006824.41376.b0)
Gibot, L., Galbraith, T., Huot, J. & Auger, F. A. Development of a tridimensional microvascularized human skin substitute to study melanoma biology. Clin. Exp. Metastasis 30, 83–90 (2012). (PMID: 2279086610.1007/s10585-012-9511-3)
Van Kilsdonk, J. W. J., Bergers, M., Van Kempen, L. C. L. T., Schalkwijk, J. & Swart, G. W. M. Keratinocytes drive melanoma invasion in a reconstructed skin model. Melanoma Res. 20, 372–380 (2010). (PMID: 20700063)
Ma, Y., Aymeric, L., Locher, C., Kroemer, G. & Zitvogel, L. The dendritic cell–tumor cross-talk in cancer. Curr. Opin. Immunol. 23, 146–152 (2011). (PMID: 2097097310.1016/j.coi.2010.09.008)
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. 127, 77–84 (2010). (PMID: 1977855510.1016/j.imlet.2009.09.003)
Segura, E. & Amigorena, S. Inflammatory dendritic cells in mice and humans. Trends Immunol. 34, 440–445 (2013). (PMID: 2383126710.1016/j.it.2013.06.001)
Veglia, F. & Gabrilovich, D. I. Dendritic cells in cancer: the role revisited. Curr. Opin. Immunol. 45, 43–51 (2017). (PMID: 28192720544925210.1016/j.coi.2017.01.002)
Engblom, C., Pfirschke, C. & Pittet, M. J. The role of myeloid cells in cancer therapies. Nat. Rev. Cancer 16, 447 (2016). (PMID: 2733970810.1038/nrc.2016.54)
Varga, J., De Oliveira, T. & Greten, F. R. The architect who never sleeps: tumor-induced plasticity. FEBS Lett. 588, 2422–2427 (2014). (PMID: 24931375409952310.1016/j.febslet.2014.06.019)
Bakdash, G. et al. Expansion of a BDCA1+CD14+ myeloid cell population in melanoma patients may attenuate the efficacy of dendritic cell vaccines. Cancer Res. 76, 4332 (2016). (PMID: 2732564510.1158/0008-5472.CAN-15-1695)
Michea, P. et al. Adjustment of dendritic cells to the breast-cancer microenvironment is subset specific. Nat. Immunol. 19, 885–897 (2018). (PMID: 3001314710.1038/s41590-018-0145-8)
Segura, E. et al. Human inflammatory dendritic cells induce Th17 cell differentiation. Immunity 38, 336–348 (2013). (PMID: 2335223510.1016/j.immuni.2012.10.018)
Ee, T. J. V. et al. BDCA1+CD14+ immunosuppressive cells in cancer, a potential target? Vaccines 6, 65 (2018). (PMID: 616108610.3390/vaccines6030065)
Bol, K. F., Tel, J., de Vries, I. J. M. & Figdor, C. G. Naturally circulating dendritic cells to vaccinate cancer patients. OncoImmunology 2, e23431 (2013). (PMID: 23802086366117110.4161/onci.23431)
Westdorp, H. et al. Blood-derived dendritic cell vaccinations induce immune responses that correlate with clinical outcome in patients with chemo-naive castration-resistant prostate cancer. J. Immunother. Cancer 7, 302 (2019). (PMID: 31727154685481410.1186/s40425-019-0787-6)
Binnewies, M. et al. Unleashing type-2 dendritic cells to drive protective antitumor CD4(+) T cell immunity. Cell 177, 556–571.E16 (2019). (PMID: 30955881695410810.1016/j.cell.2019.02.005)
Huber, V. et al. Tumor-derived microRNAs induce myeloid suppressor cells and predict immunotherapy resistance in melanoma. J. Clin. Invest. 128, 5505–5516 (2018). (PMID: 30260323626473310.1172/JCI98060)
Mao, Y. et al. Melanoma-educated CD14+ cells acquire a myeloid-derived suppressor cell phenotype through COX-2-dependent mechanisms. Cancer Res. 73, 3877–3887 (2013). (PMID: 2363348610.1158/0008-5472.CAN-12-4115)
Gabrilovich, D. I., Ostrand-Rosenberg, S. & Bronte, V. Coordinated regulation of myeloid cells by tumours. Nat. Rev. Immunol. 12, 253–268 (2012). (PMID: 22437938358714810.1038/nri3175)
Obermajer, N., Muthuswamy, R., Lesnock, J., Edwards, R. P. & Kalinski, P. Positive feedback between PGE2 and COX2 redirects the differentiation of human dendritic cells toward stable myeloid-derived suppressor cells. Blood 118, 5498–5505 (2011). (PMID: 21972293321735210.1182/blood-2011-07-365825)
Zhao, F. et al. S100A9 a new marker for monocytic human myeloid-derived suppressor cells. Immunology 136, 176–183 (2012). (PMID: 22304731340326410.1111/j.1365-2567.2012.03566.x)
von Bergwelt-Baildon, M. S. et al. CD25 and indoleamine 2,3-dioxygenase are up-regulated by prostaglandin E2 and expressed by tumor-associated dendritic cells in vivo: additional mechanisms of T-cell inhibition. Blood 108, 228–237 (2006). (PMID: 10.1182/blood-2005-08-3507)
Weeber, F. et al. Preserved genetic diversity in organoids cultured from biopsies of human colorectal cancer metastases. Proc. Natl Acad. Sci. USA 112, 13308–13311 (2015). (PMID: 2646000910.1073/pnas.1516689112)
van de Wetering, M. et al. Prospective derivation of a living organoid biobank of colorectal cancer patients. Cell 161, 933–945 (2015). (PMID: 6428276642827610.1016/j.cell.2015.03.053)
Clevers, H. Modeling development and disease with organoids. Cell 165, 1586–1597 (2016). (PMID: 2731547610.1016/j.cell.2016.05.082)
Neal, J. T. et al. Organoid modeling of the tumor immune microenvironment. Cell 175, 1972–1988.e1916 (2018). (PMID: 30550791665668710.1016/j.cell.2018.11.021)
Dijkstra, K. K. et al. Generation of tumor-reactive T cells by co-culture of peripheral blood lymphocytes and tumor organoids. Cell 174, 1586–1598.e1512 (2018). (PMID: 30100188655828910.1016/j.cell.2018.07.009)
Hölzel, M., Bovier, A. & Tüting, T. Plasticity of tumour and immune cells: a source of heterogeneity and a cause for therapy resistance? Nat. Rev. Cancer 13, 365–376 (2013). (PMID: 2353584610.1038/nrc3498)
Villani, A.-C. et al. Single-cell RNA-seq reveals new types of human blood dendritic cells, monocytes, and progenitors. Science 356, eaah4573 (2017).
Diao, J. et al. Immunostimulatory conventional dendritic cells evolve into regulatory macrophage-like cells. Blood 119, 4919–4927 (2012). (PMID: 2249068010.1182/blood-2011-11-392894)
Pyfferoen, L. et al. The transcriptome of lung tumor-infiltrating dendritic cells reveals a tumor-supporting phenotype and a microRNA signature with negative impact on clinical outcome. Oncoimmunology 6, e1253655 (2016). (PMID: 28197369528364310.1080/2162402X.2016.1253655)
Gerlini, G. et al. Metastatic melanoma secreted IL-10 down-regulates CD1 molecules on dendritic cells in metastatic tumor lesions. Am. J. Pathol. 165, 1853–1863 (2004). (PMID: 15579430161872610.1016/S0002-9440(10)63238-5)
Lindenberg, J. J. et al. Functional characterization of a STAT3-dependent dendritic cell-derived CD14(+) cell population arising upon IL-10-driven maturation. Oncoimmunology 2, e23837 (2013). (PMID: 23734330365460010.4161/onci.23837)
Martinez, F. O., Gordon, S., Locati, M. & Mantovani, A. Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J. Immunol. 177, 7303–7311 (2006). (PMID: 1708264910.4049/jimmunol.177.10.7303)
Solinas, G. et al. Tumor-conditioned macrophages secrete migration-stimulating factor: a new marker for M2-polarization, influencing tumor cell motility. J. Immunol. 185, 642–652 (2010). (PMID: 2053025910.4049/jimmunol.1000413)
Alvey, C. M. et al. SIRPA-inhibited, marrow-derived macrophages engorge, accumulate, and differentiate in antibody-targeted regression of solid tumors. Curr. Biol. 27, 2065–2077.e6 (2017). (PMID: 28669759584667610.1016/j.cub.2017.06.005)
Prunieras, M., Regnier, M. & Schlotterer, M. New procedure for culturing human epidermal cells on allogenic or xenogenic skin: preparation of recombined grafts. Ann. Chir. Plast. 24, 375–362 (1979).
Rouwkema, J. & Khademhosseini, A. Vascularization and angiogenesis in tissue engineering: beyond creating static networks. Trends Biotechnol. 34, 733–745 (2016). (PMID: 2703273010.1016/j.tibtech.2016.03.002)
Mohammadi, M. H. et al. Skin diseases modeling using combined tissue engineering and microfluidic technologies. Adv. Healthc. Mater. 5, 2459–2480 (2016). (PMID: 2754838810.1002/adhm.201600439)
van den Broek, L. J., Bergers, L. I. J. C., Reijnders, C. M. A. & Gibbs, S. Progress and future prospectives in skin-on-chip development with emphasis on the use of different cell types and technical challenges. Stem Cell Rev. Rep. 13, 418–429 (2017). (PMID: 2853689010.1007/s12015-017-9737-1)
Jenkins, R. W. et al. Ex vivo profiling of PD-1 blockade using organotypic tumor spheroids. Cancer Disco. 8, 196–215 (2017). (PMID: 10.1158/2159-8290.CD-17-0833)
van den Bogaard, E. H. et al. Crosstalk between keratinocytes and T cells in a 3D microenvironment: a model to study inflammatory skin diseases. J. Invest. Dermat. 134, 719–727 (2014). (PMID: 10.1038/jid.2013.417)
Gorris, M. A. J. et al. Eight-color multiplex immunohistochemistry for simultaneous detection of multiple immune checkpoint molecules within the tumor microenvironment. J. Immunol. 200, 347–354 (2017). (PMID: 2914186310.4049/jimmunol.1701262)
Vasaturo, A. et al. T-cell landscape in a primary melanoma predicts the survival of patients with metastatic disease after their treatment with dendritic cell vaccines. Cancer Res. 76, 3496–3506 (2016). (PMID: 2719717910.1158/0008-5472.CAN-15-3211)
Gu, Z., Eils, R. & Schlesner, M. Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics 32, 2847–2849 (2016). (PMID: 2720794310.1093/bioinformatics/btw313)
تواريخ الأحداث: Date Created: 20200604 Date Completed: 20200821 Latest Revision: 20231213
رمز التحديث: 20231215
مُعرف محوري في PubMed: PMC7265463
DOI: 10.1038/s41467-020-16583-0
PMID: 32488012
قاعدة البيانات: MEDLINE
الوصف
تدمد:2041-1723
DOI:10.1038/s41467-020-16583-0