Transcription Factor Networks Directing the Development, Function, and Evolution of Innate Lymphoid Effectors

Overview

Journal Annu Rev Immunol

Specialty Allergy & Immunology

Date 2015 Feb 5

PMID 25650177

Citations 28

Authors

Joonsoo Kang

Nidhi Malhotra

Affiliations

Soon will be listed here.

Abstract

Mammalian lymphoid immunity is mediated by fast and slow responders to pathogens. Fast innate lymphocytes are active within hours after infections in mucosal tissues. Slow adaptive lymphocytes are conventional T and B cells with clonal antigen receptors that function days after pathogen exposure. A transcription factor (TF) regulatory network guiding early T cell development is at the core of effector function diversification in all innate lymphocytes, and the kinetics of immune responses is set by developmental programming. Operational units within the innate lymphoid system are not classified by the types of pathogen-sensing machineries but rather by discrete effector functions programmed by regulatory TF networks. Based on the evolutionary history of TFs of the regulatory networks, fast effectors likely arose earlier in the evolution of animals to fortify body barriers, and in mammals they often develop in fetal ontogeny prior to the establishment of fully competent adaptive immunity.

Citing Articles

Cholesterol sensing and metabolic adaptation in tissue immunity.

Dang E, Reboldi A Trends Immunol. 2024; 45(11):861-870.

PMID: 39424470 PMC: 11560508. DOI: 10.1016/j.it.2024.09.013.

Single-cell RNA sequencing illuminates the ontogeny, conservation and diversification of cartilaginous and bony fish lymphocytes.

Wang H, Chen J, Li Y, Zhang X, Liu X, Lu Y Nat Commun. 2024; 15(1):7627.

PMID: 39227568 PMC: 11372145. DOI: 10.1038/s41467-024-51761-4.

SOX-5 Transcription Factor: a Novel Psoriatic Autoantigen Preferentially Found in Women.

Orbai A, Fiorentino D, Perin J, Darrah E, Yang Q, Gutierrez-Alamillo L ACR Open Rheumatol. 2024; 6(12):807-819.

PMID: 39218617 PMC: 11638130. DOI: 10.1002/acr2.11740.

Skin γδ T cell inflammatory responses are hardwired in the thymus by oxysterol sensing via GPR183 and calibrated by dietary cholesterol.

Frascoli M, Ferraj E, Miu B, Malin J, Spidale N, Cowan J Immunity. 2023; 56(3):562-575.e6.

PMID: 36842431 PMC: 10306310. DOI: 10.1016/j.immuni.2023.01.025.

Single-Cell Transcriptomics Reveals Longevity Immune Remodeling Features Shared by Centenarians and Their Offspring.

Dong C, Miao Y, Zhao R, Yang M, Guo A, Xue Z Adv Sci (Weinh). 2022; 9(36):e2204849.

PMID: 36354175 PMC: 9799020. DOI: 10.1002/advs.202204849.

References

Sun J, Ugolini S, Vivier E . Immunological memory within the innate immune system. EMBO J. 2014; 33(12):1295-303. PMC: 4194120. DOI: 10.1002/embj.201387651. View

Cohen N, Brennan P, Shay T, Watts G, Brigl M, Kang J . Shared and distinct transcriptional programs underlie the hybrid nature of iNKT cells. Nat Immunol. 2012; 14(1):90-9. PMC: 3764492. DOI: 10.1038/ni.2490. View

Shim S, Kwan K, Li M, Lefebvre V, Sestan N . Cis-regulatory control of corticospinal system development and evolution. Nature. 2012; 486(7401):74-9. PMC: 3375921. DOI: 10.1038/nature11094. View

Sawa S, Cherrier M, Lochner M, Satoh-Takayama N, Fehling H, Langa F . Lineage relationship analysis of RORgammat+ innate lymphoid cells. Science. 2010; 330(6004):665-9. DOI: 10.1126/science.1194597. View

Howard R, Sundaram M . C. elegans EOR-1/PLZF and EOR-2 positively regulate Ras and Wnt signaling and function redundantly with LIN-25 and the SUR-2 Mediator component. Genes Dev. 2002; 16(14):1815-27. PMC: 186391. DOI: 10.1101/gad.998402. View

Egawa T, Eberl G, Taniuchi I, Benlagha K, Geissmann F, Hennighausen L . Genetic evidence supporting selection of the Valpha14i NKT cell lineage from double-positive thymocyte precursors. Immunity. 2005; 22(6):705-16. DOI: 10.1016/j.immuni.2005.03.011. View

Nussbaum J, Van Dyken S, von Moltke J, Cheng L, Mohapatra A, Molofsky A . Type 2 innate lymphoid cells control eosinophil homeostasis. Nature. 2013; 502(7470):245-8. PMC: 3795960. DOI: 10.1038/nature12526. View

Garman R, Doherty P, Raulet D . Diversity, rearrangement, and expression of murine T cell gamma genes. Cell. 1986; 45(5):733-42. DOI: 10.1016/0092-8674(86)90787-7. View

Li L, Zhang J, Dose M, Kueh H, Mosadeghi R, Gounari F . A far downstream enhancer for murine Bcl11b controls its T-cell specific expression. Blood. 2013; 122(6):902-11. PMC: 3739036. DOI: 10.1182/blood-2012-08-447839. View

10.

Klose C, Flach M, Mohle L, Rogell L, Hoyler T, Ebert K . Differentiation of type 1 ILCs from a common progenitor to all helper-like innate lymphoid cell lineages. Cell. 2014; 157(2):340-356. DOI: 10.1016/j.cell.2014.03.030. View

11.

Tsutsui S, Nakamura O, Watanabe T . Lamprey (Lethenteron japonicum) IL-17 upregulated by LPS-stimulation in the skin cells. Immunogenetics. 2007; 59(11):873-82. DOI: 10.1007/s00251-007-0254-2. View

12.

Medvinsky A, Rybtsov S, Taoudi S . Embryonic origin of the adult hematopoietic system: advances and questions. Development. 2011; 138(6):1017-31. DOI: 10.1242/dev.040998. View

13.

Ciofani M, Madar A, Galan C, Sellars M, Mace K, Pauli F . A validated regulatory network for Th17 cell specification. Cell. 2012; 151(2):289-303. PMC: 3503487. DOI: 10.1016/j.cell.2012.09.016. View

14.

Leishman A, Naidenko O, Attinger A, Koning F, Lena C, Xiong Y . T cell responses modulated through interaction between CD8alphaalpha and the nonclassical MHC class I molecule, TL. Science. 2001; 294(5548):1936-9. DOI: 10.1126/science.1063564. View

15.

Neill D, Wong S, Bellosi A, Flynn R, Daly M, Langford T . Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature. 2010; 464(7293):1367-70. PMC: 2862165. DOI: 10.1038/nature08900. View

16.

Solek C, Oliveri P, Loza-Coll M, Schrankel C, Ho E, Wang G . An ancient role for Gata-1/2/3 and Scl transcription factor homologs in the development of immunocytes. Dev Biol. 2013; 382(1):280-92. DOI: 10.1016/j.ydbio.2013.06.019. View

17.

Simionato E, Ledent V, Richards G, Thomas-Chollier M, Kerner P, Coornaert D . Origin and diversification of the basic helix-loop-helix gene family in metazoans: insights from comparative genomics. BMC Evol Biol. 2007; 7:33. PMC: 1828162. DOI: 10.1186/1471-2148-7-33. View

18.

Constantinides M, Bendelac A . Transcriptional regulation of the NKT cell lineage. Curr Opin Immunol. 2013; 25(2):161-7. PMC: 3647452. DOI: 10.1016/j.coi.2013.01.003. View

19.

Zhang B, Lin Y, Dai M, Zhuang Y . Id3 and Id2 act as a dual safety mechanism in regulating the development and population size of innate-like γδ T cells. J Immunol. 2014; 192(3):1055-1063. PMC: 3899720. DOI: 10.4049/jimmunol.1302694. View

20.

Clevers H . Wnt/beta-catenin signaling in development and disease. Cell. 2006; 127(3):469-80. DOI: 10.1016/j.cell.2006.10.018. View