Deciphering the transcriptional network of the dendritic cell lineage

Jennifer C. Miller; Brian D. Brown; Tal Shay; Emmanuel L. Gautier; Vladimir Jojic; Ariella Cohain; Gaurav Pandey; Marylene Leboeuf; Kutlu G. Elpek; Julie Helft; Daigo Hashimoto; Andrew Chow; Jeremy Price; Melanie Greter; Milena Bogunovic; Angelique Bellemare-Pelletier; Paul S. Frenette; Gwendalyn J. Randolph; Shannon J. Turley; Miriam Merad; Claudia Jakubzick; Adam J. Best; Jamie Knell; Ananda Goldrath; Daphne Koller; Nadia Cohen; Patrick Brennan; Michael Brenner; Aviv Regev; Anne Fletcher; Deepali Malhotra; 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

doi:10.1038/ni.2370

Deciphering the transcriptional network of the dendritic cell lineage

Jennifer C. Miller, Brian D. Brown, Tal Shay, Emmanuel L. Gautier, Vladimir Jojic, Ariella Cohain, Gaurav Pandey, Marylene Leboeuf, Kutlu G. Elpek, Julie Helft, Daigo Hashimoto, Andrew Chow, Jeremy Price, Melanie Greter, Milena Bogunovic, Angelique Bellemare-Pelletier, Paul S. Frenette, Gwendalyn J. Randolph, Shannon J. Turley, Miriam MeradClaudia Jakubzick, Adam J. Best, Jamie Knell, Ananda Goldrath, Daphne Koller, Nadia Cohen, Patrick Brennan, Michael Brenner, Aviv Regev, Anne Fletcher, Deepali Malhotra, 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

Medicine

Research output: Contribution to journal › Article › peer-review

598 Scopus citations

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.

Original language	English (US)
Pages (from-to)	888-899
Number of pages	12
Journal	Nature Immunology
Volume	13
Issue number	9
DOIs	https://doi.org/10.1038/ni.2370
State	Published - Sep 2012

ASJC Scopus subject areas

Immunology and Allergy
Immunology

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10.1038/ni.2370

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Miller, J. C., Brown, B. D., Shay, T., Gautier, E. L., Jojic, V., Cohain, A., Pandey, G., Leboeuf, M., Elpek, K. G., Helft, J., Hashimoto, D., Chow, A., Price, J., Greter, M., Bogunovic, M., Bellemare-Pelletier, A., Frenette, P. S., Randolph, G. J., Turley, S. J., ... Benoist, C. (2012). Deciphering the transcriptional network of the dendritic cell lineage. Nature Immunology, 13(9), 888-899. https://doi.org/10.1038/ni.2370

Miller, JC, Brown, BD, Shay, T, Gautier, EL, Jojic, V, Cohain, A, Pandey, G, Leboeuf, M, Elpek, KG, Helft, J, Hashimoto, D, Chow, A, Price, J, Greter, M, Bogunovic, M, Bellemare-Pelletier, A, Frenette, PS, Randolph, GJ, Turley, SJ, Merad, M, Jakubzick, C, Best, AJ, Knell, J, Goldrath, A, Koller, D, Cohen, N, Brennan, P, Brenner, M, Regev, A, Fletcher, A, Malhotra, D, Jianu, R, Laidlaw, D, Collins, J, Narayan, K, Sylvia, K, Kang, J, Gazit, R, Rossi, DJ, Kim, F, Rao, TN, Wagers, A, Shinton, SA, Hardy, RR, Monach, P, Bezman, NA, Sun, JC, Kim, CC, Lanier, LL, Heng, T, Kreslavsky, T, Painter, M, Ericson, J, Davis, S, Mathis, D & Benoist, C 2012, 'Deciphering the transcriptional network of the dendritic cell lineage', Nature Immunology, vol. 13, no. 9, pp. 888-899. https://doi.org/10.1038/ni.2370

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title = "Deciphering the transcriptional network of the dendritic cell lineage",

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.",

author = "Miller, {Jennifer C.} and Brown, {Brian D.} and Tal Shay and Gautier, {Emmanuel L.} and Vladimir Jojic and Ariella Cohain and Gaurav Pandey and Marylene Leboeuf and Elpek, {Kutlu G.} and Julie Helft and Daigo Hashimoto and Andrew Chow and Jeremy Price and Melanie Greter and Milena Bogunovic and Angelique Bellemare-Pelletier and Frenette, {Paul S.} and Randolph, {Gwendalyn J.} and Turley, {Shannon J.} and Miriam Merad and Claudia Jakubzick and Best, {Adam J.} and Jamie Knell and Ananda Goldrath and Daphne Koller and Nadia Cohen and Patrick Brennan and Michael Brenner and Aviv Regev and Anne Fletcher and Deepali Malhotra and Radu Jianu and David Laidlaw and Jim Collins and Kavitha Narayan and Katelyn Sylvia and Joonsoo Kang and Roi Gazit and Rossi, {Derrick J.} and Francis Kim and Rao, {Tata Nageswara} and Amy Wagers and Shinton, {Susan A.} and Hardy, {Richard R.} and Paul Monach and Bezman, {Natalie A.} and Sun, {Joseph C.} and Kim, {Charlie C.} and Lanier, {Lewis L.} and Tracy Heng and Taras Kreslavsky and Michio Painter and Jeffrey Ericson and Scott Davis and Diane Mathis and Christophe Benoist",

note = "Funding Information: 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.).",

year = "2012",

month = sep,

doi = "10.1038/ni.2370",

language = "English (US)",

volume = "13",

pages = "888--899",

journal = "Nature Immunology",

issn = "1529-2908",

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number = "9",

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T1 - Deciphering the transcriptional network of the dendritic cell lineage

AU - Miller, Jennifer C.

AU - Brown, Brian D.

AU - Shay, Tal

AU - Gautier, Emmanuel L.

AU - Jojic, Vladimir

AU - Cohain, Ariella

AU - Pandey, Gaurav

AU - Leboeuf, Marylene

AU - Elpek, Kutlu G.

AU - Helft, Julie

AU - Hashimoto, Daigo

AU - Chow, Andrew

AU - Price, Jeremy

AU - Greter, Melanie

AU - Bogunovic, Milena

AU - Bellemare-Pelletier, Angelique

AU - Frenette, Paul S.

AU - Randolph, Gwendalyn J.

AU - Turley, Shannon J.

AU - Merad, Miriam

AU - Jakubzick, Claudia

AU - Best, Adam J.

AU - Knell, Jamie

AU - Goldrath, Ananda

AU - Koller, Daphne

AU - Cohen, Nadia

AU - Brennan, Patrick

AU - Brenner, Michael

AU - Regev, Aviv

AU - Fletcher, Anne

AU - Malhotra, Deepali

AU - Jianu, Radu

AU - Laidlaw, David

AU - Collins, Jim

AU - Narayan, Kavitha

AU - Sylvia, Katelyn

AU - Kang, Joonsoo

AU - Gazit, Roi

AU - Rossi, Derrick J.

AU - Kim, Francis

AU - Rao, Tata Nageswara

AU - Wagers, Amy

AU - Shinton, Susan A.

AU - Hardy, Richard R.

AU - Monach, Paul

AU - Bezman, Natalie A.

AU - Sun, Joseph C.

AU - Kim, Charlie C.

AU - Lanier, Lewis L.

AU - Heng, Tracy

AU - Kreslavsky, Taras

AU - Painter, Michio

AU - Ericson, Jeffrey

AU - Davis, Scott

AU - Mathis, Diane

AU - Benoist, Christophe

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PY - 2012/9

Y1 - 2012/9

N2 - 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.

AB - 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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Deciphering the transcriptional network of the dendritic cell lineage

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