Gradients of the signaling lipid S1P in lymph nodes position natural killer cells and regulate their interferon-γ 3 response

Nature Immunology

Volumn 18, Issue 1, 2017, Pages 15-25

  Fang, Victoria ^a   Chaluvadi, V Sai ^a   Ramos Perez, Willy D ^a,d   Mendoza, Alejandra ^a   Baeyens, Audrey ^a   Rivera, Richard ^b   Chun, Jerold ^b   Cammer, Michael ^c   Schwab, Susan R ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^d UNIVERSITY OF PUERTO RICO SCHOOL OF MEDICINE   (Puerto Rico)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; GAMMA INTERFERON; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE 1 PHOSPHATE RECEPTOR; ANION TRANSPORT PROTEIN; CXCR4 PROTEIN, MOUSE; LYSOPHOSPHOLIPID; SPHINGOSINE; SPHINGOSINE 1-PHOSPHATE; SPNS2 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOTHELIUM CELL; LYMPH NODE; LYMPH VESSEL; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T LYMPHOCYTE; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL DIFFERENTIATION; CELL MOTION; CHEMISTRY; CHEMOTAXIS; GENETICS; HELPER CELL; HOMEOSTASIS; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; METABOLISM; PHYSIOLOGY;

ANIMALS; ANION TRANSPORT PROTEINS; CELL DIFFERENTIATION; CELL MOVEMENT; CELLS, CULTURED; CHEMOTAXIS; ENDOTHELIAL CELLS; HOMEOSTASIS; INTERFERON-GAMMA; KILLER CELLS, NATURAL; LYMPH NODES; LYMPHOCYTE ACTIVATION; LYSOPHOSPHOLIPIDS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, CXCR4; RECEPTORS, LYSOSPHINGOLIPID; SIGNAL TRANSDUCTION; SPHINGOSINE; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 84995470409     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.3619     Document Type: Article

References (50)

1. Phan, T. G., Grigorova, I., Okada, T. & Cyster, J. G. Subcapsular encounter and complement-dependent transport of immune complexes by lymph node B cells. Nat. Immunol. 8, 992-1000 (2007).
2. Phan, T. G., Green, J. A., Gray, E. E., Xu, Y. & Cyster, J. G. Immune complex relay by subcapsular sinus macrophages and noncognate B cells drives antibody affinity maturation. Nat. Immunol. 10, 786-793 (2009).
3. Junt, T. et al. Subcapsular sinus macrophages in lymph nodes clear lymph-borne viruses and present them to antiviral B cells. Nature 450, 110-114 (2007).
4. Iannacone, M. et al. Subcapsular sinus macrophages prevent CNS invasion on peripheral infection with a neurotropic virus. Nature 465, 1079-1083 (2010).
5. Kastenmüller, W., Torabi-Parizi, P., Subramanian, N., Lämmermann, T. & Germain, R. N. A spatially-organized multicellular innate immune response in lymph nodes limits systemic pathogen spread. Cell 150, 1235-1248 (2012).
6. Carrasco, Y. R. & Batista, F. D. B cells acquire particulate antigen in a macrophage-rich area at the boundary between the follicle and the subcapsular sinus of the lymph node. Immunity 27, 160-171 (2007).
7. Gonzalez, S. F. et al. Capture of influenza by medullary dendritic cells via SIGN-R1 is essential for humoral immunity in draining lymph nodes. Nat. Immunol. 11, 427-434 (2010).
8. Gerner, M. Y., Torabi-Parizi, P. & Germain, R. N. Strategically localized dendritic cells promote rapid T cell responses to lymph-borne particulate antigens. Immunity 42, 172-185 (2015).
9. Suan, D. et al. T follicular helper cells have distinct modes of migration and molecular signatures in naive and memory immune responses. Immunity 42, 704-718 (2015).
10. Kastenmüller, W. et al. Peripheral prepositioning and local CXCL9 chemokine-mediated guidance orchestrate rapid memory CD8+ T cell responses in the lymph node. Immunity 38, 502-513 (2013).
11. Groom, J. R. et al. CXCR3 chemokine receptor-ligand interactions in the lymph node optimize CD4+ T helper 1 cell differentiation. Immunity 37, 1091-1103 (2012).
12. Hickman, H. D. et al. Direct priming of antiviral CD8+ T cells in the peripheral interfollicular region of lymph nodes. Nat. Immunol. 9, 155-165 (2008).
13. Sung, J. H. et al. Chemokine guidance of central memory T cells is critical for antiviral recall responses in lymph nodes. Cell 150, 1249-1263 (2012).
14. Chtanova, T. et al. Dynamics of T cell, antigen-presenting cell, and pathogen interactions during recall responses in the lymph node. Immunity 31, 342-355 (2009).
15. León, B. et al. Regulation of TH2 development by CXCR5+ dendritic cells and lymphotoxin-expressing B cells. Nat. Immunol. 13, 681-690 (2012).
16. Woodruff, M. C. et al. Trans-nodal migration of resident dendritic cells into medullary interfollicular regions initiates immunity to influenza vaccine. J. Exp. Med. 211, 1611-1621 (2014).
17. Barral, P. et al. CD169+ macrophages present lipid antigens to mediate early activation of iNKT cells in lymph nodes. Nat. Immunol. 11, 303-312 (2010).
18. Dokun, A. O., Chu, D. T., Yang, L., Bendelac, A. S. & Yokoyama, W. M. Analysis of in situ NK cell responses during viral infection. J. Immunol. 167, 5286-5293 (2001).
19. Coombes, J. L., Han, S. J., van Rooijen, N., Raulet, D. H. & Robey, E. A. Infection-induced regulation of natural killer cells by macrophages and collagen at the lymph node subcapsular sinus. Cell Rep. 2, 124-135 (2012).
20. Garcia, Z. et al. Subcapsular sinus macrophages promote NK cell accumulation and activation in response to lymph-borne viral particles. Blood 120, 4744-4750 (2012).
21. Beuneu, H. et al. Dynamic behavior of NK cells during activation in lymph nodes. Blood 114, 3227-3234 (2009).
22. Bajénoff, M. et al. Natural killer cell behavior in lymph nodes revealed by static and real-time imaging. J. Exp. Med. 203, 619-631 (2006).
23. Walzer, T. et al. Natural killer cell trafficking in vivo requires a dedicated sphingosine 1-phosphate receptor. Nat. Immunol. 8, 1337-1344 (2007).
24. Garrod, K. R., Wei, S. H., Parker, I. & Cahalan, M. D. Natural killer cells actively patrol peripheral lymph nodes forming stable conjugates to eliminate MHC-mismatched targets. Proc. Natl. Acad. Sci. USA 104, 12081-12086 (2007).
25. Decker, T., Stockinger, S., Karaghiosoff, M., Müller, M. & Kovarik, P. IFNs and STATs in innate immunity to microorganisms. J. Clin. Invest. 109, 1271-1277 (2002).
26. Mendoza, A. et al. The transporter Spns2 is required for secretion of lymph but not plasma sphingosine-1-phosphate. Cell Rep. 2, 1104-1110 (2012).
27. Cyster, J. G. & Schwab, S. R. Sphingosine-1-phosphate and lymphocyte egress from lymphoid organs. Annu. Rev. Immunol. 30, 69-94 (2012).
28. Ramos-Perez, W. D., Fang, V., Escalante-Alcalde, D., Cammer, M. & Schwab, S. R. A map of the distribution of sphingosine 1-phosphate in the spleen. Nat. Immunol. 16, 1245-1252 (2015).
29. Liu, C. H. et al. Ligand-induced trafficking of the sphingosine-1-phosphate receptor EDG-1. Mol. Biol. Cell 10, 1179-1190 (1999).
30. Kühn, R., Schwenk, F., Aguet, M. & Rajewsky, K. Inducible gene targeting in mice. Science 269, 1427-1429 (1995).
31. Ruzankina, Y. et al. Deletion of the developmentally essential gene ATR in adult mice leads to age-related phenotypes and stem cell loss. Cell Stem Cell 1, 113-126 (2007).
32. Gray, E. E. & Cyster, J. G. Lymph node macrophages. J. Innate Immun. 4, 424-436 (2012).
33. Pham, T. H. et al. Lymphatic endothelial cell sphingosine kinase activity is required for lymphocyte egress and lymphatic patterning. J. Exp. Med. 207, 17-27 (2010).
34. Braun, A. et al. Afferent lymph-derived T cells and DCs use different chemokine receptor CCR7-dependent routes for entry into the lymph node and intranodal migration. Nat. Immunol. 12, 879-887 (2011).
35. Grigorova, I. L., Panteleev, M. & Cyster, J. G. Lymph node cortical sinus organization and relationship to lymphocyte egress dynamics and antigen exposure. Proc. Natl. Acad. Sci. USA 107, 20447-20452 (2010).
36. Quancard, J. et al. A potent and selective S1P1 antagonist with efficacy in experimental autoimmune encephalomyelitis. Chem. Biol. 19, 1142-1151 (2012).
37. Jenne, C. N. et al. T-bet-dependent S1P5 expression in NK cells promotes egress from lymph nodes and bone marrow. J. Exp. Med. 206, 2469-2481 (2009).
38. Cyster, J. G. Homing of antibody secreting cells. Immunol. Rev. 194, 48-60 (2003).
39. Schmidt, T. H., Bannard, O., Gray, E. E. & Cyster, J. G. CXCR4 promotes B cell egress from Peyer's patches. J. Exp. Med. 210, 1099-1107 (2013).
40. Mayol, K., Biajoux, V., Marvel, J., Balabanian, K. & Walzer, T. Sequential desensitization of CXCR4 and S1P5 controls natural killer cell trafficking. Blood 118, 4863-4871 (2011).
41. Schols, D., Esté, J. A., Henson, G. & De Clercq, E. Bicyclams, a class of potent anti-HIV agents, are targeted at the HIV coreceptor fusin/CXCR-4. Antiviral Res. 35, 147-156 (1997).
42. Uy, G. L. et al. A phase 1/2 study of chemosensitization with the CXCR4 antagonist plerixafor in relapsed or refractory acute myeloid leukemia. Blood 119, 3917-3924 (2012).
43. Nie, Y. et al. The role of CXCR4 in maintaining peripheral B cell compartments and humoral immunity. J. Exp. Med. 200, 1145-1156 (2004).
44. Nagahashi, M. et al. Spns2, a transporter of phosphorylated sphingoid bases, regulates their blood and lymph levels, and the lymphatic network. FASEB J. 27, 1001-1011 (2013).
45. Wei, S. H. et al. Sphingosine 1-phosphate type 1 receptor agonism inhibits transendothelial migration of medullary T cells to lymphatic sinuses. Nat. Immunol. 6, 1228-1235 (2005).
46. Green, J. A. et al. The sphingosine 1-phosphate receptor S1P maintains the homeostasis of germinal center B cells and promotes niche confinement. Nat. Immunol. 12, 672-680 (2011).
47. Moriyama, S. et al. Sphingosine-1-phosphate receptor 2 is critical for follicular helper T cell retention in germinal centers. J. Exp. Med. 211, 1297-1305 (2014).
48. Zhang, Y. et al. Migratory and adhesive cues controlling innate-like lymphocyte surveillance of the pathogen-exposed surface of the lymph node. eLife 5, e18156 (2016).
49. Murata, K. et al. CD69-null mice protected from arthritis induced with anti-type II collagen antibodies. Int. Immunol. 15, 987-992 (2003).
50. Schaefer, B. C., Schaefer, M. L., Kappler, J. W., Marrack, P. & Kedl, R. M. Observation of antigen-dependent CD8+ T-cell/ dendritic cell interactions in vivo. Cell. Immunol. 214, 110-122 (2001).