Molecular definition of the identity and activation of natural killer cells

Natalie A. Bezman; Charles C. Kim; Joseph C. Sun; Gundula Min-Oo; Deborah W. Hendricks; Yosuke Kamimura; J. Adam Best; Ananda W. Goldrath; Lewis L. Lanier; Emmanuel L. Gautier; Claudia Jakubzick; Gwendalyn J. Randolph; Adam J. Best; Jamie Knell; 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 J. 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; Charlie C. Kim; Tracy Heng; Taras Kreslavsky; Michio Painter; Jeffrey Ericson; Scott Davis; Diane Mathis; Christophe Benoist

doi:10.1038/ni.2395

Molecular definition of the identity and activation of natural killer cells

Natalie A. Bezman, Charles C. Kim, Joseph C. Sun, Gundula Min-Oo, Deborah W. Hendricks, Yosuke Kamimura, J. Adam Best, Ananda W. Goldrath, Lewis L. Lanier, Emmanuel L. Gautier, Claudia Jakubzick, Gwendalyn J. Randolph, Adam J. Best, Jamie Knell, Jennifer Miller, Brian Brown, Miriam Merad, Vladimir Jojic, Daphne Koller, Nadia CohenPatrick Brennan, Michael Brenner, Tal Shay, Aviv Regev, Anne Fletcher, Kutlu Elpek, Angelique Bellemare-Pelletier, Deepali Malhotra, Shannon Turley, Radu Jianu, David Laidlaw, Jim J. 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, Charlie C. Kim, Tracy Heng, Taras Kreslavsky, Michio Painter, Jeffrey Ericson, Scott Davis, Diane Mathis, Christophe Benoist

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Abstract

Using whole-genome microarray data sets of the Immunological Genome Project, we demonstrate a closer transcriptional relationship between NK cells and T cells than between any other leukocytes, distinguished by their shared expression of genes encoding molecules with similar signaling functions. Whereas resting NK cells are known to share expression of a few genes with cytotoxic CD8 + T cells, our transcriptome-wide analysis demonstrates that the commonalities extend to hundreds of genes, many encoding molecules with unknown functions. Resting NK cells demonstrate a 'preprimed' state compared with naive T cells, which allows NK cells to respond more rapidly to viral infection. Collectively, our data provide a global context for known and previously unknown molecular aspects of NK cell identity and function by delineating the genome-wide repertoire of gene expression of NK cells in various states.

Original language	English
Pages (from-to)	1000-1008
Number of pages	9
Journal	Nature immunology
Volume	13
Issue number	10
DOIs	https://doi.org/10.1038/ni.2395
State	Published - Oct 2012

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Bezman, N. A., Kim, C. C., Sun, J. C., Min-Oo, G., Hendricks, D. W., Kamimura, Y., Best, J. A., Goldrath, A. W., Lanier, L. L., Gautier, E. L., Jakubzick, C., Randolph, G. J., Best, A. J., Knell, J., Miller, J., Brown, B., Merad, M., Jojic, V., Koller, D., ... Benoist, C. (2012). Molecular definition of the identity and activation of natural killer cells. Nature immunology, 13(10), 1000-1008. https://doi.org/10.1038/ni.2395

@article{d284100c75a84d5c8125152f3e38046e,

title = "Molecular definition of the identity and activation of natural killer cells",

abstract = "Using whole-genome microarray data sets of the Immunological Genome Project, we demonstrate a closer transcriptional relationship between NK cells and T cells than between any other leukocytes, distinguished by their shared expression of genes encoding molecules with similar signaling functions. Whereas resting NK cells are known to share expression of a few genes with cytotoxic CD8 + T cells, our transcriptome-wide analysis demonstrates that the commonalities extend to hundreds of genes, many encoding molecules with unknown functions. Resting NK cells demonstrate a 'preprimed' state compared with naive T cells, which allows NK cells to respond more rapidly to viral infection. Collectively, our data provide a global context for known and previously unknown molecular aspects of NK cell identity and function by delineating the genome-wide repertoire of gene expression of NK cells in various states.",

author = "Bezman, {Natalie A.} and Kim, {Charles C.} and Sun, {Joseph C.} and Gundula Min-Oo and Hendricks, {Deborah W.} and Yosuke Kamimura and Best, {J. Adam} and Goldrath, {Ananda W.} and Lanier, {Lewis L.} and Gautier, {Emmanuel L.} and Claudia Jakubzick and Randolph, {Gwendalyn J.} and Best, {Adam J.} and Jamie Knell and Jennifer Miller and Brian Brown and Miriam Merad and Vladimir Jojic and Daphne Koller and Nadia Cohen and Patrick Brennan and Michael Brenner and Tal Shay and Aviv Regev and Anne Fletcher and Kutlu Elpek and Angelique Bellemare-Pelletier and Deepali Malhotra and Shannon Turley and Radu Jianu and David Laidlaw and Collins, {Jim J.} 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 Kim, {Charlie C.} 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 A. Weiss (University of California, San Francisco) for antibody to Syk; the members of the ImmGen Consortium and M. Dozmorov for discussions; the ImmGen core team (M. Painter, J. Ericson and S. Davis) for data generation and processing; J. Jarjoura and J. Arakawa-Hoyt for assistance in cell sorting; A. Beaulieu, J. Karo and S. Madera for data from MCMV infection experiments; and eBioscience, Affymetrix and Expression Analysis 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 and R01 AI068129; T32AI060537 to D.W.H.; T32AI060536 to J.A.B.; and AI072117 to A.W.G.), the American Cancer Society (L.L.L. and N.A.B.), the Canadian Institutes of Health Research (G.M.-O.) and the Searle Scholars Program (J.C.S.).",

year = "2012",

month = oct,

doi = "10.1038/ni.2395",

language = "English",

volume = "13",

pages = "1000--1008",

journal = "Nature immunology",

issn = "1529-2908",

number = "10",

}

Bezman, NA, Kim, CC, Sun, JC, Min-Oo, G, Hendricks, DW, Kamimura, Y, Best, JA, Goldrath, AW, Lanier, LL, Gautier, EL, Jakubzick, C, Randolph, GJ, Best, AJ, Knell, J, Miller, J, Brown, B, Merad, M, Jojic, V, Koller, D, Cohen, N, Brennan, P, Brenner, M, Shay, T, Regev, A, Fletcher, A, Elpek, K, Bellemare-Pelletier, A, Malhotra, D, Turley, S, Jianu, R, Laidlaw, D, Collins, JJ, Narayan, K, Sylvia, K, Kang, J, Gazit, R, Rossi, DJ, Kim, F, Rao, TN, Wagers, A, Shinton, SA, Hardy, RR, Monach, P, Kim, CC, Heng, T, Kreslavsky, T, Painter, M, Ericson, J, Davis, S, Mathis, D & Benoist, C 2012, 'Molecular definition of the identity and activation of natural killer cells', Nature immunology, vol. 13, no. 10, pp. 1000-1008. https://doi.org/10.1038/ni.2395

TY - JOUR

T1 - Molecular definition of the identity and activation of natural killer cells

AU - Bezman, Natalie A.

AU - Kim, Charles C.

AU - Sun, Joseph C.

AU - Min-Oo, Gundula

AU - Hendricks, Deborah W.

AU - Kamimura, Yosuke

AU - Best, J. Adam

AU - Goldrath, Ananda W.

AU - Lanier, Lewis L.

AU - Gautier, Emmanuel L.

AU - Jakubzick, Claudia

AU - Randolph, Gwendalyn J.

AU - Best, Adam J.

AU - Knell, Jamie

AU - Miller, Jennifer

AU - Brown, Brian

AU - Merad, Miriam

AU - Jojic, Vladimir

AU - Koller, Daphne

AU - Cohen, Nadia

AU - Brennan, Patrick

AU - Brenner, Michael

AU - Shay, Tal

AU - Regev, Aviv

AU - Fletcher, Anne

AU - Elpek, Kutlu

AU - Bellemare-Pelletier, Angelique

AU - Malhotra, Deepali

AU - Turley, Shannon

AU - Jianu, Radu

AU - Laidlaw, David

AU - Collins, Jim J.

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 - Kim, Charlie C.

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 A. Weiss (University of California, San Francisco) for antibody to Syk; the members of the ImmGen Consortium and M. Dozmorov for discussions; the ImmGen core team (M. Painter, J. Ericson and S. Davis) for data generation and processing; J. Jarjoura and J. Arakawa-Hoyt for assistance in cell sorting; A. Beaulieu, J. Karo and S. Madera for data from MCMV infection experiments; and eBioscience, Affymetrix and Expression Analysis 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 and R01 AI068129; T32AI060537 to D.W.H.; T32AI060536 to J.A.B.; and AI072117 to A.W.G.), the American Cancer Society (L.L.L. and N.A.B.), the Canadian Institutes of Health Research (G.M.-O.) and the Searle Scholars Program (J.C.S.).

PY - 2012/10

Y1 - 2012/10

N2 - Using whole-genome microarray data sets of the Immunological Genome Project, we demonstrate a closer transcriptional relationship between NK cells and T cells than between any other leukocytes, distinguished by their shared expression of genes encoding molecules with similar signaling functions. Whereas resting NK cells are known to share expression of a few genes with cytotoxic CD8 + T cells, our transcriptome-wide analysis demonstrates that the commonalities extend to hundreds of genes, many encoding molecules with unknown functions. Resting NK cells demonstrate a 'preprimed' state compared with naive T cells, which allows NK cells to respond more rapidly to viral infection. Collectively, our data provide a global context for known and previously unknown molecular aspects of NK cell identity and function by delineating the genome-wide repertoire of gene expression of NK cells in various states.

AB - Using whole-genome microarray data sets of the Immunological Genome Project, we demonstrate a closer transcriptional relationship between NK cells and T cells than between any other leukocytes, distinguished by their shared expression of genes encoding molecules with similar signaling functions. Whereas resting NK cells are known to share expression of a few genes with cytotoxic CD8 + T cells, our transcriptome-wide analysis demonstrates that the commonalities extend to hundreds of genes, many encoding molecules with unknown functions. Resting NK cells demonstrate a 'preprimed' state compared with naive T cells, which allows NK cells to respond more rapidly to viral infection. Collectively, our data provide a global context for known and previously unknown molecular aspects of NK cell identity and function by delineating the genome-wide repertoire of gene expression of NK cells in various states.

UR - http://www.scopus.com/inward/record.url?scp=84866537220&partnerID=8YFLogxK

U2 - 10.1038/ni.2395

DO - 10.1038/ni.2395

M3 - Article

C2 - 22902830

AN - SCOPUS:84866537220

SN - 1529-2908

VL - 13

SP - 1000

EP - 1008

JO - Nature immunology

JF - Nature immunology

IS - 10

ER -

Molecular definition of the identity and activation of natural killer cells

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