Neuropilin-1 Is Expressed on Lymphoid Tissue Residing LTi-like Group 3 Innate Lymphoid Cells and Associated with Ectopic Lymphoid Aggregates

Cell Reports

Volumn 18, Issue 7, 2017, Pages 1761-1773

  Shikhagaie, Medya Mara ^a   Björklund, Åsa K ^b   Mjösberg, Jenny ^b   Erjefält, Jonas S ^c   Cornelissen, Anne S ^a   Ros, Xavier Romero ^a   Bal, Suzanne M ^a   Koning, Jasper J ^d   Mebius, Reina E ^d   Mori, Michiko ^c   Bruchard, Melanie ^a   Blom, Bianca ^a   Spits, Hergen ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b KAROLINSKA INSTITUTE   (Sweden)

^c LUND UNIVERSITY   (Sweden)

^d VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

chemotaxis; HEVs; high endothelial venues; human innate lymphoid cells 3; ILC3; LA; LTi; lymphoid tissue inducer cells; neuropilin 1; NRP1; smoke induced pulmonary lymphoid aggregates; vascular endothelial growth factor A; VEGF A

Indexed keywords

CD45RA ANTIGEN; CD45RO ANTIGEN; CELL MARKER; CHEMOTACTIC FACTOR; NEUROPILIN 1; VASCULOTROPIN A; CYTOKINE; RECEPTOR TYPE TYROSINE PROTEIN PHOSPHATASE C;

ADULT; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD; CELL AGGREGATION; CELL SURFACE; CELLULAR DISTRIBUTION; CHRONIC OBSTRUCTIVE LUNG DISEASE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENDOTHELIUM; FETUS; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LUNG PARENCHYMA; LYMPHOCYTE MIGRATION; LYMPHOID CELL; LYMPHOID TISSUE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SKIN; SMOKING; VENULE; ANIMAL; CELL CULTURE; CELL MOTION; LYMPHOCYTE; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); PHYSIOLOGY;

ANIMALS; CELL MOVEMENT; CELLS, CULTURED; CYTOKINES; HUMANS; LEUKOCYTE COMMON ANTIGENS; LYMPHOCYTES; LYMPHOID TISSUE; MICE; NEOVASCULARIZATION, PATHOLOGIC; NEUROPILIN-1; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 85013188332     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2017.01.063     Document Type: Article

References (49)

1. Artis, D., Spits, H., The biology of innate lymphoid cells. Nature 517 (2015), 293–301.
2. Bal, S.M., Bernink, J.H., Nagasawa, M., Groot, J., Shikhagaie, M.M., Golebski, K., van Drunen, C.M., Lutter, R., Jonkers, R.E., Hombrink, P., et al. IL-1β, IL-4 and IL-12 control the fate of group 2 innate lymphoid cells in human airway inflammation in the lungs. Nat Immunol. 17 (2016), 636–645.
3. Barone, F., Nayar, S., Campos, J., Cloake, T., Withers, D.R., Toellner, K.M., Zhang, Y., Fouser, L., Fisher, B., Bowman, S., et al. IL-22 regulates lymphoid chemokine production and assembly of tertiary lymphoid organs. Proc. Natl. Acad. Sci. USA 112 (2015), 11024–11029.
4. Bernink, J.H., Krabbendam, L., Germar, K., de Jong, E., Gronke, K., Kofoed-Nielsen, M., Munneke, J.M., Hazenberg, M.D., Villaudy, J., Buskens, C.J., et al. Interleukin-12 and -23 control plasticity of CD127+ group 1 and group 3 innate lymphoid cells in the intestinal lamina propria. Immunity 43 (2015), 146–160.
5. Björklund, Å.K., Forkel, M., Picelli, S., Konya, V., Theorell, J., Friberg, D., Sandberg, R., Mjösberg, J., The heterogeneity of human CD127 innate lymphoid cells revealed by single-cell RNA sequencing. Nat. Immunol. 17 (2016), 451–460.
6. Bracke, K.R., Verhamme, F.M., Seys, L.J., Bantsimba-Malanda, C., Cunoosamy, D.M., Herbst, R., Hammad, H., Lambrecht, B.N., Joos, G.F., Brusselle, G.G., Role of CXCL13 in cigarette smoke-induced lymphoid follicle formation and chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 188 (2013), 343–355.
7. Brusselle, G.G., Demoor, T., Bracke, K.R., Brandsma, C.A., Timens, W., Lymphoid follicles in (very) severe COPD: beneficial or harmful?. Eur. Respir. J. 34 (2009), 219–230.
8. Carragher, D.M., Rangel-Moreno, J., Randall, T.D., Ectopic lymphoid tissues and local immunity. Semin. Immunol. 20 (2008), 26–42.
9. Carrasco, Y.R., Fleire, S.J., Cameron, T., Dustin, M.L., Batista, F.D., LFA-1/ICAM-1 interaction lowers the threshold of B cell activation by facilitating B cell adhesion and synapse formation. Immunity 20 (2004), 589–599.
10. Carrega, P., Loiacono, F., Di Carlo, E., Scaramuccia, A., Mora, M., Conte, R., Benelli, R., Spaggiari, G.M., Cantoni, C., Campana, S., et al. NCR(+)ILC3 concentrate in human lung cancer and associate with intratumoral lymphoid structures. Nat. Commun., 6, 2015, 8280.
11. Chung, K.F., Adcock, I.M., Multifaceted mechanisms in COPD: inflammation, immunity, and tissue repair and destruction. Eur. Respir. J. 31 (2008), 1334–1356.
12. Constantinides, M.G., McDonald, B.D., Verhoef, P.A., Bendelac, A., A committed precursor to innate lymphoid cells. Nature 508 (2014), 397–401.
13. Cupedo, T., Crellin, N.K., Papazian, N., Rombouts, E.J., Weijer, K., Grogan, J.L., Fibbe, W.E., Cornelissen, J.J., Spits, H., Human fetal lymphoid tissue-inducer cells are interleukin 17-producing precursors to RORC+ CD127+ natural killer-like cells. Nat. Immunol. 10 (2009), 66–74.
14. De Grove, K.C., Provoost, S., Verhamme, F.M., Bracke, K.R., Joos, G.F., Maes, T., Brusselle, G.G., Characterization and quantification of innate lymphoid cell subsets in human lung. PLoS ONE, 11, 2016, e0145961.
15. Drayton, D.L., Liao, S., Mounzer, R.H., Ruddle, N.H., Lymphoid organ development: from ontogeny to neogenesis. Nat. Immunol. 7 (2006), 344–353.
16. E, X.Q., Meng, H.X., Cao, Y., Zhang, S.Q., Bi, Z.G., Yamakawa, M., Distribution of regulatory T cells and interaction with dendritic cells in the synovium of rheumatoid arthritis. Scand. J. Rheumatol. 41 (2012), 413–420.
17. Edelbauer, M., Datta, D., Vos, I.H., Basu, A., Stack, M.P., Reinders, M.E., Sho, M., Calzadilla, K., Ganz, P., Briscoe, D.M., Effect of vascular endothelial growth factor and its receptor KDR on the transendothelial migration and local trafficking of human T cells in vitro and in vivo. Blood 116 (2010), 1980–1989.
18. Elliot, J.G., Jensen, C.M., Mutavdzic, S., Lamb, J.P., Carroll, N.G., James, A.L., Aggregations of lymphoid cells in the airways of nonsmokers, smokers, and subjects with asthma. Am. J. Respir. Crit. Care Med. 169 (2004), 712–718.
19. Evans, R., Patzak, I., Svensson, L., De Filippo, K., Jones, K., McDowall, A., Hogg, N., Integrins in immunity. J. Cell Sci. 122 (2009), 215–225.
20. Folkman, J., Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat. Med. 1 (1995), 27–31.
21. Garay, E., Patiño-López, G., Islas, S., Alarcón, L., Canche-Pool, E., Valle-Rios, R., Medina-Contreras, O., Granados, G., Chávez-Munguía, B., Juaristi, E., et al. CRTAM: a molecule involved in epithelial cell adhesion. J. Cell. Biochem. 111 (2010), 111–122.
22. Hogg, J., Peripheral lung remodelling in asthma and chronic obstructive pulmonary disease. Eur. Respir. J. 24 (2004), 893–894.
23. Ishizuka, I.E., Chea, S., Gudjonson, H., Constantinides, M.G., Dinner, A.R., Bendelac, A., Golub, R., Single-cell analysis defines the divergence between the innate lymphoid cell lineage and lymphoid tissue-inducer cell lineage. Nat. Immunol. 17 (2016), 269–276.
24. Killig, M., Glatzer, T., Romagnani, C., Recognition strategies of group 3 innate lymphoid cells. Front. Immunol., 5, 2014, 142.
25. Kuschner, W.G., D'Alessandro, A., Wong, H., Blanc, P.D., Dose-dependent cigarette smoking-related inflammatory responses in healthy adults. Eur. Respir. J. 9 (1996), 1989–1994.
26. Lamalice, L., Le Boeuf, F., Huot, J., Endothelial cell migration during angiogenesis. Circ. Res. 100 (2007), 782–794.
27. Lee, C.G., Ma, B., Takyar, S., Ahangari, F., Delacruz, C., He, C.H., Elias, J.A., Studies of vascular endothelial growth factor in asthma and chronic obstructive pulmonary disease. Proc. Am. Thorac. Soc. 8 (2011), 512–515.
28. Litsiou, E., Semitekolou, M., Galani, I., Morianos, I., Tsoutsa, A., Kara, P., Rontogianni, D., Bellenis, I., Konstantinou, M., Potaris, K., et al. Reply: CXCL13 in tertiary lymphoid tissues: sites of production are different from sites of functional localization. Am. J. Respir. Crit. Care Med. 189 (2014), 370–371.
29. Maijenburg, M.W., Kleijer, M., Vermeul, K., Mul, E.P., van Alphen, F.P., van der Schoot, C.E., Voermans, C., The composition of the mesenchymal stromal cell compartment in human bone marrow changes during development and aging. Haematologica 97 (2012), 179–183.
30. Marwick, J.A., Stevenson, C.S., Giddings, J., MacNee, W., Butler, K., Rahman, I., Kirkham, P.A., Cigarette smoke disrupts VEGF165-VEGFR-2 receptor signaling complex in rat lungs and patients with COPD: morphological impact of VEGFR-2 inhibition. Am. J. Physiol. Lung Cell. Mol. Physiol. 290 (2006), L897–L908.
31. Milpied, P., Massot, B., Renand, A., Diem, S., Herbelin, A., Leite-de-Moraes, M., Rubio, M.T., Hermine, O., IL-17-producing invariant NKT cells in lymphoid organs are recent thymic emigrants identified by neuropilin-1 expression. Blood 118 (2011), 2993–3002.
32. Mjösberg, J., Spits, H., Human innate lymphoid cells. J. Allergy Clin. Immunol. 138 (2016), 1265–1276.
33. Mori, M., Andersson, C.K., Svedberg, K.A., Glader, P., Bergqvist, A., Shikhagaie, M., Löfdahl, C.G., Erjefält, J.S., Appearance of remodelled and dendritic cell-rich alveolar-lymphoid interfaces provides a structural basis for increased alveolar antigen uptake in chronic obstructive pulmonary disease. Thorax 68 (2013), 521–531.
34. Pitzalis, C., Jones, G.W., Bombardieri, M., Jones, S.A., Ectopic lymphoid-like structures in infection, cancer and autoimmunity. Nat. Rev. Immunol. 14 (2014), 447–462.
35. Rabe, K.F., Hurd, S., Anzueto, A., Barnes, P.J., Buist, S.A., Calverley, P., Fukuchi, Y., Jenkins, C., Rodriguez-Roisin, R., van Weel, C., Zielinski, J., Global Initiative for Chronic Obstructive Lung Disease. Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: GOLD executive summary. Am. J. Respir. Crit. Care Med. 176 (2007), 532–555.
36. Reference Genome Group of the Gene Ontology Consortium. The Gene Ontology's Reference Genome Project: a unified framework for functional annotation across species. PLoS Comput. Biol., 5, 2009, e1000431.
37. Roan, F., Stoklasek, T.A., Whalen, E., Molitor, J.A., Bluestone, J.A., Buckner, J.H., Ziegler, S.F., CD4+ group 1 innate lymphoid cells (ILC) form a functionally distinct ILC subset that is increased in systemic sclerosis. J. Immunol. 196 (2016), 2051–2062.
38. Robinette, M.L., Fuchs, A., Cortez, V.S., Lee, J.S., Wang, Y., Durum, S.K., Gilfillan, S., Colonna, M., Immunological Genome Consortium. Transcriptional programs define molecular characteristics of innate lymphoid cell classes and subsets. Nat. Immunol. 16 (2015), 306–317.
39. Roos, A.B., Sandén, C., Mori, M., Bjermer, L., Stampfli, M.R., Erjefält, J.S., IL-17A is elevated in end-stage chronic obstructive pulmonary disease and contributes to cigarette smoke-induced lymphoid neogenesis. Am. J. Respir. Crit. Care Med. 191 (2015), 1232–1241.
40. Scoville, S.D., Mundy-Bosse, B.L., Zhang, M.H., Chen, L., Zhang, X., Keller, K.A., Hughes, T., Chen, L., Cheng, S., Bergin, S.M., et al. A progenitor cell expressing transcription factor RORγt generates all human innate lymphoid cell subsets. Immunity 44 (2016), 1140–1150.
41. Silver, J.S., Kearley, J., Copenhaver, A.M., Sanden, C., Mori, M., Yu, L., Pritchard, G.H., Berlin, A.A., Hunter, C.A., Bowler, R., et al. Inflammatory triggers associated with exacerbations of COPD orchestrate plasticity of group 2 innate lymphoid cells in the lungs. Nat. Immunol. 17 (2016), 626–635.
42. Subramanian, A., Tamayo, P., Mootha, V.K., Mukherjee, S., Ebert, B.L., Gillette, M.A., Paulovich, A., Pomeroy, S.L., Golub, T.R., Lander, E.S., Mesirov, J.P., Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 102 (2005), 15545–15550.
43. Suzuki, T., Hirakawa, S., Shimauchi, T., Ito, T., Sakabe, J., Detmar, M., Tokura, Y., VEGF-A promotes IL-17A-producing γδ T cell accumulation in mouse skin and serves as a chemotactic factor for plasmacytoid dendritic cells. J. Dermatol. Sci. 74 (2014), 116–124.
44. Thorley, A.J., Tetley, T.D., Pulmonary epithelium, cigarette smoke, and chronic obstructive pulmonary disease. Int. J. Chron. Obstruct. Pulmon. Dis. 2 (2007), 409–428.
45. Tschernig, T., Pabst, R., Bronchus-associated lymphoid tissue (BALT) is not present in the normal adult lung but in different diseases. Pathobiology 68 (2000), 1–8.
46. Vacca, P., Montaldo, E., Croxatto, D., Loiacono, F., Canegallo, F., Venturini, P.L., Moretta, L., Mingari, M.C., Identification of diverse innate lymphoid cells in human decidua. Mucosal Immunol. 8 (2015), 254–264.
47. Van Pottelberge, G.R., Bracke, K.R., Van den Broeck, S., Reinartz, S.M., van Drunen, C.M., Wouters, E.F., Verleden, G.M., Vermassen, F.E., Joos, G.F., Brusselle, G.G., Plasmacytoid dendritic cells in pulmonary lymphoid follicles of patients with COPD. Eur. Respir. J. 36 (2010), 781–791.
48. Yadav, M., Louvet, C., Davini, D., Gardner, J.M., Martinez-Llordella, M., Bailey-Bucktrout, S., Anthony, B.A., Sverdrup, F.M., Head, R., Kuster, D.J., et al. Neuropilin-1 distinguishes natural and inducible regulatory T cells among regulatory T cell subsets in vivo. J. Exp. Med. 209 (2012), 1713–1722 S1–S19.
49. Yang, Y.C., Zhang, N., Van Crombruggen, K., Hu, G.H., Hong, S.L., Bachert, C., Transforming growth factor-beta1 in inflammatory airway disease: a key for understanding inflammation and remodeling. Allergy 67 (2012), 1193–1202.