Molecular Definition of Group 1 Innate Lymphoid Cells in the Mouse Uterus

Overview

Journal Nat Commun

Specialty Biology

Date 2018 Oct 31

PMID 30374017

Citations 43

Authors

Iva Filipovic

Laura Chiossone

Paola Vacca

Russell S Hamilton

Tiziano Ingegnere

Jean-Marc Doisne

Delia A Hawkes

Maria Cristina Mingari

Andrew M Sharkey

Lorenzo Moretta

Francesco Colucci

Affiliations

Soon will be listed here.

Abstract

Determining the function of uterine lymphocytes is challenging because of the dynamic changes in response to sex hormones and, during pregnancy, to the invading foetal trophoblast cells. Here we provide a genome-wide transcriptome atlas of mouse uterine group 1 innate lymphoid cells (ILCs) at mid-gestation. Tissue-resident EomesCD49a NK cells (trNK), which resemble human uterine NK cells, are most abundant during early pregnancy, and have gene signatures associated with TGF-β responses and interactions with trophoblast, epithelial, endothelial, smooth muscle cells, leucocytes and extracellular matrix. Conventional NK cells expand late in gestation and may engage in crosstalk with trNK cells involving IL-18 and IFN-γ. EomesCD49a ILC1s dominate before puberty, and specifically expand in second pregnancies when the expression of the memory cell marker CXCR6 is upregulated. These results identify trNK cells as the cellular hub of uterine group 1 ILCs, and mark CXCR6 ILC1s as potential memory cells of pregnancy.

Citing Articles

Treg cells promote decidual vascular remodeling and modulate uterine NK cells in pregnant mice.

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References

Moffett A, Shreeve N . First do no harm: uterine natural killer (NK) cells in assisted reproduction. Hum Reprod. 2015; 30(7):1519-25. PMC: 4472320. DOI: 10.1093/humrep/dev098. View

Kieckbusch J, Gaynor L, Moffett A, Colucci F . MHC-dependent inhibition of uterine NK cells impedes fetal growth and decidual vascular remodelling. Nat Commun. 2014; 5:3359. PMC: 3948146. DOI: 10.1038/ncomms4359. View

Siewiera J, El Costa H, Tabiasco J, Berrebi A, Cartron G, Le Bouteiller P . Human cytomegalovirus infection elicits new decidual natural killer cell effector functions. PLoS Pathog. 2013; 9(4):e1003257. PMC: 3617138. DOI: 10.1371/journal.ppat.1003257. View

Crespo A, Strominger J, Tilburgs T . Expression of KIR2DS1 by decidual natural killer cells increases their ability to control placental HCMV infection. Proc Natl Acad Sci U S A. 2016; 113(52):15072-15077. PMC: 5206558. DOI: 10.1073/pnas.1617927114. View

Hiby S, Walker J, OShaughnessy K, Redman C, Carrington M, Trowsdale J . Combinations of maternal KIR and fetal HLA-C genes influence the risk of preeclampsia and reproductive success. J Exp Med. 2004; 200(8):957-65. PMC: 2211839. DOI: 10.1084/jem.20041214. View

Chen Z, Huang A, Sun J, Jiang T, Qin F, Wu A . Inference of immune cell composition on the expression profiles of mouse tissue. Sci Rep. 2017; 7:40508. PMC: 5233994. DOI: 10.1038/srep40508. View

Peng H, Jiang X, Chen Y, Sojka D, Wei H, Gao X . Liver-resident NK cells confer adaptive immunity in skin-contact inflammation. J Clin Invest. 2013; 123(4):1444-56. PMC: 3613925. DOI: 10.1172/JCI66381. View

Tse S, Radtke A, Espinosa D, Cockburn I, Zavala F . The chemokine receptor CXCR6 is required for the maintenance of liver memory CD8⁺ T cells specific for infectious pathogens. J Infect Dis. 2014; 210(9):1508-16. PMC: 4207865. DOI: 10.1093/infdis/jiu281. View

Pope G, Roberts E, Lolait S, OCarroll A . Central and peripheral apelin receptor distribution in the mouse: species differences with rat. Peptides. 2011; 33(1):139-48. PMC: 3314948. DOI: 10.1016/j.peptides.2011.12.005. View

10.

Bartemes K, Chen C, Iijima K, Drake L, Kita H . IL-33-Responsive Group 2 Innate Lymphoid Cells Are Regulated by Female Sex Hormones in the Uterus. J Immunol. 2017; 200(1):229-236. PMC: 5736420. DOI: 10.4049/jimmunol.1602085. View

11.

Allen M, Nilsen-Hamilton M . Granzymes D, E, F, and G are regulated through pregnancy and by IL-2 and IL-15 in granulated metrial gland cells. J Immunol. 1998; 161(6):2772-9. View

12.

Bernink J, Peters C, Munneke M, Te Velde A, Meijer S, Weijer K . Human type 1 innate lymphoid cells accumulate in inflamed mucosal tissues. Nat Immunol. 2013; 14(3):221-9. DOI: 10.1038/ni.2534. View

13.

Hernandez-Diaz S, Toh S, Cnattingius S . Risk of pre-eclampsia in first and subsequent pregnancies: prospective cohort study. BMJ. 2009; 338:b2255. PMC: 3269902. DOI: 10.1136/bmj.b2255. View

14.

Chen Z, Zhang J, Hatta K, Lima P, Yadi H, Colucci F . DBA-lectin reactivity defines mouse uterine natural killer cell subsets with biased gene expression. Biol Reprod. 2012; 87(4):81. PMC: 3467293. DOI: 10.1095/biolreprod.112.102293. View

15.

Zuo R, Gu X, Qi Q, Wang T, Zhao X, Liu J . Warburg-like Glycolysis and Lactate Shuttle in Mouse Decidua during Early Pregnancy. J Biol Chem. 2015; 290(35):21280-91. PMC: 4571859. DOI: 10.1074/jbc.M115.656629. View

16.

Manickam C, Nwanze C, Ram D, Shah S, Smith S, Jones R . Progressive lentivirus infection induces natural killer cell receptor-expressing B cells in the gastrointestinal tract. AIDS. 2018; 32(12):1571-1578. PMC: 6043388. DOI: 10.1097/QAD.0000000000001855. View

17.

Gardiner C, Finlay D . What Fuels Natural Killers? Metabolism and NK Cell Responses. Front Immunol. 2017; 8:367. PMC: 5376555. DOI: 10.3389/fimmu.2017.00367. View

18.

Berod L, Friedrich C, Nandan A, Freitag J, Hagemann S, Harmrolfs K . De novo fatty acid synthesis controls the fate between regulatory T and T helper 17 cells. Nat Med. 2014; 20(11):1327-33. DOI: 10.1038/nm.3704. View

19.

Wilkens J, Male V, Ghazal P, Forster T, Gibson D, Williams A . Uterine NK cells regulate endometrial bleeding in women and are suppressed by the progesterone receptor modulator asoprisnil. J Immunol. 2013; 191(5):2226-35. PMC: 3843142. DOI: 10.4049/jimmunol.1300958. View

20.

Velasquez S, Killian D, Schulte J, Sticht C, Thiel M, Lindner H . Short Term Hypoxia Synergizes with Interleukin 15 Priming in Driving Glycolytic Gene Transcription and Supports Human Natural Killer Cell Activities. J Biol Chem. 2016; 291(25):12960-77. PMC: 4933215. DOI: 10.1074/jbc.M116.721753. View