Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages

Emmanuel L. Gautiar; Tal Shay; Jennifer Miller; Melanie Greter; Claudia Jakubzick; Stoyan Ivanov; Julie Helft; Andrew Chow; Kutlu G. Elpek; Simon Gordonov; Amin R. Mazloom; Avi Ma'Ayan; Wei Jen Chua; Ted H. Hansen; Shannon J. Turley; Miriam Merad; Gwendalyn J. Randolph; Adam J. Best; Jamie Knell; Ananda Goldrath; Brian Brown; Vladimir Jojic; Daphne Koller; Nadia Cohen; Michael Brenner; Aviv Regev; Anne Fletcher; Angelique Bellemare-Pelletier; Deepali Malhotra; Radu Jianu; David Laidlaw; Jim Collins; Kavitha Narayan; Katelyn Sylvia; Joonsoo Kang; Roi Gazit; Brian S. Garrison; 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.2419

Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages

Emmanuel L. Gautiar, Tal Shay, Jennifer Miller, Melanie Greter, Claudia Jakubzick, Stoyan Ivanov, Julie Helft, Andrew Chow, Kutlu G. Elpek, Simon Gordonov, Amin R. Mazloom, Avi Ma'Ayan, Wei Jen Chua, Ted H. Hansen, Shannon J. Turley, Miriam Merad, Gwendalyn J. Randolph, Adam J. Best, Jamie Knell, Ananda GoldrathBrian Brown, Vladimir Jojic, Daphne Koller, Nadia Cohen, Michael Brenner, Aviv Regev, Anne Fletcher, Angelique Bellemare-Pelletier, Deepali Malhotra, Radu Jianu, David Laidlaw, Jim Collins, Kavitha Narayan, Katelyn Sylvia, Joonsoo Kang, Roi Gazit, Brian S. Garrison, 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

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Abstract

We assessed gene expression in tissue macrophages from various mouse organs. The diversity in gene expression among different populations of macrophages was considerable. Only a few hundred mRNA transcripts were selectively expressed by macrophages rather than dendritic cells, and many of these were not present in all macrophages. Nonetheless, well-characterized surface markers, including MerTK and FcγR1 (CD64), along with a cluster of previously unidentified transcripts, were distinctly and universally associated with mature tissue macrophages. TCEF3, C/EBP-α, Bach1 and CREG-1 were among the transcriptional regulators predicted to regulate these core macrophage-associated genes. The mRNA encoding other transcription factors, such as Gata6, was associated with single macrophage populations. We further identified how these transcripts and the proteins they encode facilitated distinguishing macrophages from dendritic cells.

Original language	English
Pages (from-to)	1118-1128
Number of pages	11
Journal	Nature immunology
Volume	13
Issue number	11
DOIs	https://doi.org/10.1038/ni.2419
State	Published - Nov 2012

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Gautiar, E. L., Shay, T., Miller, J., Greter, M., Jakubzick, C., Ivanov, S., Helft, J., Chow, A., Elpek, K. G., Gordonov, S., Mazloom, A. R., Ma'Ayan, A., Chua, W. J., Hansen, T. H., Turley, S. J., Merad, M., Randolph, G. J., Best, A. J., Knell, J., ... Benoist, C. (2012). Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nature immunology, 13(11), 1118-1128. https://doi.org/10.1038/ni.2419

@article{235f3266ca0846f9823b88888e14fe79,

title = "Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages",

abstract = "We assessed gene expression in tissue macrophages from various mouse organs. The diversity in gene expression among different populations of macrophages was considerable. Only a few hundred mRNA transcripts were selectively expressed by macrophages rather than dendritic cells, and many of these were not present in all macrophages. Nonetheless, well-characterized surface markers, including MerTK and FcγR1 (CD64), along with a cluster of previously unidentified transcripts, were distinctly and universally associated with mature tissue macrophages. TCEF3, C/EBP-α, Bach1 and CREG-1 were among the transcriptional regulators predicted to regulate these core macrophage-associated genes. The mRNA encoding other transcription factors, such as Gata6, was associated with single macrophage populations. We further identified how these transcripts and the proteins they encode facilitated distinguishing macrophages from dendritic cells.",

author = "Gautiar, {Emmanuel L.} and Tal Shay and Jennifer Miller and Melanie Greter and Claudia Jakubzick and Stoyan Ivanov and Julie Helft and Andrew Chow and Elpek, {Kutlu G.} and Simon Gordonov and Mazloom, {Amin R.} and Avi Ma'Ayan and Chua, {Wei Jen} and Hansen, {Ted H.} and Turley, {Shannon J.} and Miriam Merad and Randolph, {Gwendalyn J.} and Best, {Adam J.} and Jamie Knell and Ananda Goldrath and Brian Brown and Vladimir Jojic and Daphne Koller and Nadia Cohen and Michael Brenner and Aviv Regev and Anne Fletcher and Angelique Bellemare-Pelletier 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 Garrison, {Brian S.} 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 our colleagues of the ImmGen Project consortium; V. Jojic, J. Ericson, S. Davis and C. Benoist for contributions; eBioscience and Affymetrix for material support of the ImmGen Project; and M. Colonna (Washington University School of Medicine) for monoclonal antibodies (including anti-Siglec-H) and other reagents. Supported by the National Institute of Allergy and Infectious Diseases of the US National Institutes of Health (R24 AI072073 to fund the ImmGen Project, spearheaded by C. Benoist), the US National Institutes of Health (R01AI049653 and R01AI061741 to G.J.R.; P50GM071558-03 and R01DK08854 to A.M.; and5T32DA007135-27 to A.R.M.) and the American Heart Association (10POST4160140 to E.L.G.).",

year = "2012",

month = nov,

doi = "10.1038/ni.2419",

language = "English",

volume = "13",

pages = "1118--1128",

journal = "Nature immunology",

issn = "1529-2908",

number = "11",

}

Gautiar, EL, Shay, T, Miller, J, Greter, M, Jakubzick, C, Ivanov, S, Helft, J, Chow, A, Elpek, KG, Gordonov, S, Mazloom, AR, Ma'Ayan, A, Chua, WJ, Hansen, TH, Turley, SJ, Merad, M, Randolph, GJ, Best, AJ, Knell, J, Goldrath, A, Brown, B, Jojic, V, Koller, D, Cohen, N, Brenner, M, Regev, A, Fletcher, A, Bellemare-Pelletier, A, Malhotra, D, Jianu, R, Laidlaw, D, Collins, J, Narayan, K, Sylvia, K, Kang, J, Gazit, R, Garrison, BS, 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, 'Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages', Nature immunology, vol. 13, no. 11, pp. 1118-1128. https://doi.org/10.1038/ni.2419

TY - JOUR

T1 - Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages

AU - Gautiar, Emmanuel L.

AU - Shay, Tal

AU - Miller, Jennifer

AU - Greter, Melanie

AU - Jakubzick, Claudia

AU - Ivanov, Stoyan

AU - Helft, Julie

AU - Chow, Andrew

AU - Elpek, Kutlu G.

AU - Gordonov, Simon

AU - Mazloom, Amin R.

AU - Ma'Ayan, Avi

AU - Chua, Wei Jen

AU - Hansen, Ted H.

AU - Turley, Shannon J.

AU - Merad, Miriam

AU - Randolph, Gwendalyn J.

AU - Best, Adam J.

AU - Knell, Jamie

AU - Goldrath, Ananda

AU - Brown, Brian

AU - Jojic, Vladimir

AU - Koller, Daphne

AU - Cohen, Nadia

AU - Brenner, Michael

AU - Regev, Aviv

AU - Fletcher, Anne

AU - Bellemare-Pelletier, Angelique

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 - Garrison, Brian S.

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

N1 - Funding Information: We thank our colleagues of the ImmGen Project consortium; V. Jojic, J. Ericson, S. Davis and C. Benoist for contributions; eBioscience and Affymetrix for material support of the ImmGen Project; and M. Colonna (Washington University School of Medicine) for monoclonal antibodies (including anti-Siglec-H) and other reagents. Supported by the National Institute of Allergy and Infectious Diseases of the US National Institutes of Health (R24 AI072073 to fund the ImmGen Project, spearheaded by C. Benoist), the US National Institutes of Health (R01AI049653 and R01AI061741 to G.J.R.; P50GM071558-03 and R01DK08854 to A.M.; and5T32DA007135-27 to A.R.M.) and the American Heart Association (10POST4160140 to E.L.G.).

PY - 2012/11

Y1 - 2012/11

N2 - We assessed gene expression in tissue macrophages from various mouse organs. The diversity in gene expression among different populations of macrophages was considerable. Only a few hundred mRNA transcripts were selectively expressed by macrophages rather than dendritic cells, and many of these were not present in all macrophages. Nonetheless, well-characterized surface markers, including MerTK and FcγR1 (CD64), along with a cluster of previously unidentified transcripts, were distinctly and universally associated with mature tissue macrophages. TCEF3, C/EBP-α, Bach1 and CREG-1 were among the transcriptional regulators predicted to regulate these core macrophage-associated genes. The mRNA encoding other transcription factors, such as Gata6, was associated with single macrophage populations. We further identified how these transcripts and the proteins they encode facilitated distinguishing macrophages from dendritic cells.

AB - We assessed gene expression in tissue macrophages from various mouse organs. The diversity in gene expression among different populations of macrophages was considerable. Only a few hundred mRNA transcripts were selectively expressed by macrophages rather than dendritic cells, and many of these were not present in all macrophages. Nonetheless, well-characterized surface markers, including MerTK and FcγR1 (CD64), along with a cluster of previously unidentified transcripts, were distinctly and universally associated with mature tissue macrophages. TCEF3, C/EBP-α, Bach1 and CREG-1 were among the transcriptional regulators predicted to regulate these core macrophage-associated genes. The mRNA encoding other transcription factors, such as Gata6, was associated with single macrophage populations. We further identified how these transcripts and the proteins they encode facilitated distinguishing macrophages from dendritic cells.

UR - http://www.scopus.com/inward/record.url?scp=84867740805&partnerID=8YFLogxK

U2 - 10.1038/ni.2419

DO - 10.1038/ni.2419

M3 - Article

C2 - 23023392

AN - SCOPUS:84867740805

SN - 1529-2908

VL - 13

SP - 1118

EP - 1128

JO - Nature immunology

JF - Nature immunology

IS - 11

ER -

Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages

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