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Deciphering the transcriptional network of the dendritic cell lineage

Nature Immunology volume 13, pages 888–899 (2012)Cite this article

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Abstract

Although much progress has been made in the understanding of the ontogeny and function of dendritic cells (DCs), the transcriptional regulation of the lineage commitment and functional specialization of DCs in vivo remains poorly understood. We made a comprehensive comparative analysis of CD8+, CD103+, CD11b+ and plasmacytoid DC subsets, as well as macrophage DC precursors and common DC precursors, across the entire immune system. Here we characterized candidate transcriptional activators involved in the commitment of myeloid progenitor cells to the DC lineage and predicted regulators of DC functional diversity in tissues. We identified a molecular signature that distinguished tissue DCs from macrophages. We also identified a transcriptional program expressed specifically during the steady-state migration of tissue DCs to the draining lymph nodes that may control tolerance to self tissue antigens.

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Figure 1: Expression of genes encoding transcription factors along the DC lineage.
Figure 2: Identification of genes significantly upregulated in cDCs relative to their expression in macrophages.
Figure 3: Unique gene signatures characterize distinct tissue DC clusters.
Figure 4: Heterogeneity of nonlymphoid-tissue CD11b+ cDCs.
Figure 5: Tissue-migratory cDCs upregulate a unique gene signature regardless of tissue or cellular origin.
Figure 6: Tissue-migratory cDCs express genes encoding immune response–dampening molecules in the steady state.

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Acknowledgements

We thank colleagues of the ImmGen Project, especially the technical team, including M. Painter, J. Ericson and S. Davis, for contributions; C. Benoist for contributions to the design and writing of the manuscript; and eBioscience and Affymetrix for support of the ImmGen Project. Supported by the National Institute of Allergy and Infectious Diseases of the US National Institutes of Health (R24 AI072073 to the ImmGen Project (led by C. Benoist); AI080884 and HL086899 to M.M.; JDRF172010770 and DP2DK083052-01 to B.D.B.; DK074500 and AI045757 to S.J.T.; HL69438, DK056638, HL097819 and HL097700 to P.S.F.; and U54CA149145 to V.J.).

Author information

Author notes

  1. Natalie A Bezman, Joseph C Sun, Charlie C Kim & Lewis L Lanier

    Present address: Department of Microbiology & Immunology, University of California San Francisco, San Francisco, California, USA

  2. Vladimir Jojic

    Present address: Present address: Department of Computer Science, UNC, Chapel Hill, North Carolina, USA.,

Authors and Affiliations

  1. Immunology Institute, Mount Sinai School of Medicine, New York, New York, USA

    Jennifer C Miller, Brian D Brown, Emmanuel L Gautier, Marylene Leboeuf, Julie Helft, Daigo Hashimoto, Andrew Chow, Jeremy Price, Melanie Greter, Milena Bogunovic, Gwendalyn J Randolph & Miriam Merad

  2. Department of Oncological Sciences, Mount Sinai School of Medicine, New York, New York, USA

    Jennifer C Miller, Marylene Leboeuf, Julie Helft, Daigo Hashimoto, Andrew Chow, Jeremy Price, Melanie Greter, Milena Bogunovic & Miriam Merad

  3. Department of Genetics and Genomic Sciences, Institute for Genomics and Multiscale Biology, Mount Sinai School of Medicine, New York, New York, USA

    Brian D Brown, Ariella Cohain & Gaurav Pandey

  4. Broad Institute, Cambridge, Massachusetts, USA

    Tal Shay

  5. Department of Regenerative Biology, Mount Sinai School of Medicine, New York, New York, USA

    Emmanuel L Gautier & Gwendalyn J Randolph

  6. Department of Pathology & Immunology, Washington University in St. Louis, St. Louis, Missouri, USA

    Emmanuel L Gautier & Gwendalyn J Randolph

  7. Computer Science Department, Stanford University, Stanford, California, USA

    Vladimir Jojic & Melanie Greter

  8. Cancer Immunology and AIDS, Dana Farber Cancer Institute, Boston, Massachusetts, USA

    Kutlu G Elpek, Angelique Bellemare-Pelletier & Shannon J Turley

  9. Albert Einstein College of Medicine, Bronx, New York, USA

    Andrew Chow & Paul S Frenette

  10. Mount Sinai Hospital, New York, New York, USA

    Emmanuel L Gautier, Claudia Jakubzick, Gwendalyn J Randolph, Jennifer Miller, Brian Brown & Miriam Merad

  11. Department of Pathology & Immunology, Washington University, St. Louis, Missouri, USA

    Emmanuel L Gautier & Gwendalyn J Randolph

  12. Division of Biological Sciences, University of California San Diego, La Jolla, California, USA

    Adam J Best, Jamie Knell & Ananda Goldrath

  13. Computer Science Department, Stanford University, Stanford, California, USA

    Vladimir Jojic, Daphne Koller & Taras Kreslavsky

  14. Division of Rheumatology, Immunology and Allergy, Brigham and Women's Hospital, Boston, Massachusetts, USA

    Nadia Cohen, Patrick Brennan & Michael Brenner

  15. Broad Institute, Cambridge, Massachusetts, USA

    Tal Shay & Aviv Regev

  16. Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts, USA

    Anne Fletcher, Kutlu Elpek, Angelique Bellemare-Pelletier, Deepali Malhotra & Shannon Turley

  17. Computer Science Department, Brown University, Providence, Rhode Island, USA

    Radu Jianu & David Laidlaw

  18. Department of Biomedical Engineering, Howard Hughes Medical Institute, Boston University, Boston, Massachusetts, USA

    Jim Collins

  19. University of Massachusetts Medical School, Worcester, Massachusetts, USA

    Kavitha Narayan, Katelyn Sylvia & Joonsoo Kang

  20. Department of Stem Cell and Regenerative Biology, Harvard University, and Program in Cellular and Molecular Medicine, Children's Hospital, Boston, Massachusetts, USA

    Roi Gazit & Derrick J Rossi

  21. Joslin Diabetes Center, Boston, Massachusetts, USA

    Francis Kim, Tata Nageswara Rao & Amy Wagers

  22. Fox Chase Cancer Center, Philadelphia, Pennsylvania, USA

    Susan A Shinton & Richard R Hardy

  23. Department of Medicine, Boston University, Boston, Massachusetts, USA

    Paul Monach

  24. Department of Microbiology & Immunobiology, Division of Immunology, Harvard Medical School, Boston, Massachusetts, USA

    Tracy Heng, Michio Painter, Jeffrey Ericson, Scott Davis, Diane Mathis & Christophe Benoist

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the Immunological Genome Consortium

  • Emmanuel L Gautier
  • , Claudia Jakubzick
  • , Gwendalyn J Randolph
  • , Adam J Best
  • , Jamie Knell
  • , Ananda Goldrath
  • , Jennifer Miller
  • , Brian Brown
  • , Miriam Merad
  • , Vladimir Jojic
  • , Daphne Koller
  • , Nadia Cohen
  • , Patrick Brennan
  • , Michael Brenner
  • , Tal Shay
  • , Aviv Regev
  • , Anne Fletcher
  • , Kutlu Elpek
  • , Angelique Bellemare-Pelletier
  • , Deepali Malhotra
  • , Shannon Turley
  • , Radu Jianu
  • , David Laidlaw
  • , Jim Collins
  • , Kavitha Narayan
  • , Katelyn Sylvia
  • , Joonsoo Kang
  • , Roi Gazit
  • , Derrick J Rossi
  • , Francis Kim
  • , Tata Nageswara Rao
  • , Amy Wagers
  • , Susan A Shinton
  • , Richard R Hardy
  • , Paul Monach
  • , Natalie A Bezman
  • , Joseph C Sun
  • , Charlie C Kim
  • , Lewis L Lanier
  • , Tracy Heng
  • , Taras Kreslavsky
  • , Michio Painter
  • , Jeffrey Ericson
  • , Scott Davis
  • , Diane Mathis
  •  & Christophe Benoist

Contributions

J.C.M. did experiments and wrote the paper; M.M. designed experiments and wrote the paper; B.D.B. provided intellectual input, did computational analyses and helped write the paper; T.S. did computation analyses and identified all modules; E.L.G. purified macrophage populations and provided intellectual input; V.J. did computation analyses and, together with T.S., designed Ontogenet; A.C. and G.P. did computation analyses; M.L. did experiments; K.G.E., J.H., D.H., A.C. and J.P. purified DC populations; M.G. purified macrophage populations; M.B. and A.B.-P. purified DC and macrophage populations; P.S.F. provided intellectual input; and G.J.R. and S.J.T. provided intellectual input for experimental design.

Corresponding author

Correspondence to Miriam Merad.

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Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–7 (PDF 1678 kb)

Supplementary Table 1

Comparison of DC subsets transcriptomes (XLSX 192 kb)

Supplementary Table 2

Comparison of the transcriptome of migratory DC and tissue resident DC (XLSX 67 kb)

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Miller, J., Brown, B., Shay, T. et al. Deciphering the transcriptional network of the dendritic cell lineage. Nat Immunol 13, 888–899 (2012). https://doi.org/10.1038/ni.2370

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