CD56 Expression Marks Human Group 2 Innate Lymphoid Cell Divergence from a Shared NK Cell and Group 3 Innate Lymphoid Cell Developmental Pathway

Overview

Journal Immunity

Publisher Cell Press

Specialty Allergy & Immunology

Date 2018 Sep 9

PMID 30193847

Citations 64

Authors

Luxi Chen

Youssef Youssef

Cameron Robinson

Gabrielle F Ernst

Mary Y Carson

Karen A Young

Steven D Scoville

Xiaoli Zhang

Regine Harris

Palak Sekhri

Anthony G Mansour

Wing K Chan

Ansel P Nalin

Hsiaoyin C Mao

Tiffany Hughes

Emily M Mace

Yinghong Pan

Navin Rustagi

Sujash S Chatterjee

Preethi H Gunaratne

Gregory K Behbehani

Bethany L Mundy-Bosse

Michael A Caligiuri

Aharon G Freud

Affiliations

Soon will be listed here.

Abstract

According to the established model of murine innate lymphoid cell (ILC) development, helper ILCs develop separately from natural killer (NK) cells. However, it is unclear how helper ILCs and NK cells develop in humans. Here we elucidated key steps of NK cell, ILC2, and ILC3 development within human tonsils using ex vivo molecular and functional profiling and lineage differentiation assays. We demonstrated that while tonsillar NK cells, ILC2s, and ILC3s originated from a common CD34CD117 ILC precursor pool, final steps of ILC2 development deviated independently and became mutually exclusive from those of NK cells and ILC3s, whose developmental pathways overlapped. Moreover, we identified a CD34CD117 ILC precursor population that expressed CD56 and gave rise to NK cells and ILC3s but not to ILC2s. These data support a model of human ILC development distinct from the mouse, whereby human NK cells and ILC3s share a common developmental pathway separate from ILC2s.

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References

Zook E, Kee B . Development of innate lymphoid cells. Nat Immunol. 2016; 17(7):775-82. DOI: 10.1038/ni.3481. View

Fuchs A, Vermi W, Lee J, Lonardi S, Gilfillan S, Newberry R . Intraepithelial type 1 innate lymphoid cells are a unique subset of IL-12- and IL-15-responsive IFN-γ-producing cells. Immunity. 2013; 38(4):769-81. PMC: 3634355. DOI: 10.1016/j.immuni.2013.02.010. View

Constantinides M, McDonald B, Verhoef P, Bendelac A . A committed precursor to innate lymphoid cells. Nature. 2014; 508(7496):397-401. PMC: 4003507. DOI: 10.1038/nature13047. View

Satoh-Takayama N, Lesjean-Pottier S, Vieira P, Sawa S, Eberl G, Vosshenrich C . IL-7 and IL-15 independently program the differentiation of intestinal CD3-NKp46+ cell subsets from Id2-dependent precursors. J Exp Med. 2010; 207(2):273-80. PMC: 2822619. DOI: 10.1084/jem.20092029. View

Serafini N, Vosshenrich C, Di Santo J . Transcriptional regulation of innate lymphoid cell fate. Nat Rev Immunol. 2015; 15(7):415-28. DOI: 10.1038/nri3855. View

Scoville S, Freud A, Caligiuri M . Modeling Human Natural Killer Cell Development in the Era of Innate Lymphoid Cells. Front Immunol. 2017; 8:360. PMC: 5366880. DOI: 10.3389/fimmu.2017.00360. View

Montaldo E, Teixeira-Alves L, Glatzer T, Durek P, Stervbo U, Hamann W . Human RORγt(+)CD34(+) cells are lineage-specified progenitors of group 3 RORγt(+) innate lymphoid cells. Immunity. 2014; 41(6):988-1000. DOI: 10.1016/j.immuni.2014.11.010. View

Moro K, Kabata H, Tanabe M, Koga S, Takeno N, Mochizuki M . Interferon and IL-27 antagonize the function of group 2 innate lymphoid cells and type 2 innate immune responses. Nat Immunol. 2015; 17(1):76-86. DOI: 10.1038/ni.3309. View

Seehus C, Aliahmad P, Torre B, Iliev I, Spurka L, Funari V . The development of innate lymphoid cells requires TOX-dependent generation of a common innate lymphoid cell progenitor. Nat Immunol. 2015; 16(6):599-608. PMC: 4439271. DOI: 10.1038/ni.3168. View

10.

Huang Y, Guo L, Qiu J, Chen X, Hu-Li J, Siebenlist U . IL-25-responsive, lineage-negative KLRG1(hi) cells are multipotential 'inflammatory' type 2 innate lymphoid cells. Nat Immunol. 2014; 16(2):161-9. PMC: 4297567. DOI: 10.1038/ni.3078. View

11.

Sun J, Lanier L . NK cell development, homeostasis and function: parallels with CD8⁺ T cells. Nat Rev Immunol. 2011; 11(10):645-57. PMC: 4408539. DOI: 10.1038/nri3044. View

12.

Carotta S, Pang S, Nutt S, Belz G . Identification of the earliest NK-cell precursor in the mouse BM. Blood. 2011; 117(20):5449-52. DOI: 10.1182/blood-2010-11-318956. View

13.

Koga S, Hozumi K, Hirano K, Yazawa M, Terooatea T, Minoda A . Peripheral PDGFRαgp38 mesenchymal cells support the differentiation of fetal liver-derived ILC2. J Exp Med. 2018; 215(6):1609-1626. PMC: 5987924. DOI: 10.1084/jem.20172310. View

14.

Cupedo T, Crellin N, Papazian N, Rombouts E, Weijer K, Grogan J . Human fetal lymphoid tissue-inducer cells are interleukin 17-producing precursors to RORC+ CD127+ natural killer-like cells. Nat Immunol. 2008; 10(1):66-74. DOI: 10.1038/ni.1668. View

15.

Dobin A, Davis C, Schlesinger F, Drenkow J, Zaleski C, Jha S . STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2012; 29(1):15-21. PMC: 3530905. DOI: 10.1093/bioinformatics/bts635. View

16.

Finck R, Simonds E, Jager A, Krishnaswamy S, Sachs K, Fantl W . Normalization of mass cytometry data with bead standards. Cytometry A. 2013; 83(5):483-94. PMC: 3688049. DOI: 10.1002/cyto.a.22271. View

17.

Yang Q, Li F, Harly C, Xing S, Ye L, Xia X . TCF-1 upregulation identifies early innate lymphoid progenitors in the bone marrow. Nat Immunol. 2015; 16(10):1044-50. PMC: 4575643. DOI: 10.1038/ni.3248. View

18.

Matos M, Schnier G, Beecher M, Ashman L, William D, Caligiuri M . Expression of a functional c-kit receptor on a subset of natural killer cells. J Exp Med. 1993; 178(3):1079-84. PMC: 2191187. DOI: 10.1084/jem.178.3.1079. View

19.

Horowitz A, Strauss-Albee D, Leipold M, Kubo J, Nemat-Gorgani N, Dogan O . Genetic and environmental determinants of human NK cell diversity revealed by mass cytometry. Sci Transl Med. 2013; 5(208):208ra145. PMC: 3918221. DOI: 10.1126/scitranslmed.3006702. View

20.

Yu J, Freud A, Caligiuri M . Location and cellular stages of natural killer cell development. Trends Immunol. 2013; 34(12):573-82. PMC: 3852183. DOI: 10.1016/j.it.2013.07.005. View