Trapping of naive lymphocytes triggers rapid growth and remodeling of the fibroblast network in reactive murine lymph nodes

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 1, 2014, Pages

  Yang, Chen Ying ^a   Vogt, Tobias K ^a   Favre, Stéphanie ^a   Scarpellino, Leonardo ^a   Huang, Hsin Ying ^a   Tacchini Cottier, Fabienne ^a   Luther, Sanjiv A ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Fibroblasts; Lymph node swelling; Lymphotoxin; MyD88; Stromal cells

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; GLYCOPROTEIN; GLYCOPROTEIN GP 38; INTERLEUKIN 17; LYMPHOTOXIN ALPHA BETA; LYMPHOTOXIN BETA RECEPTOR; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; MONTANIDE ISA 51; MYELOID DIFFERENTIATION FACTOR 88; OVALBUMIN; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; SECONDARY LYMPHOID TISSUE CHEMOKINE; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; CELL AGGREGATION; CELL COUNT; CELL EXPANSION; CELL GROWTH; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DENDRITIC CELL; ENDOTHELIUM CELL; FIBROBLAST; FIBROBLASTIC RETICULAR CELL; IMMUNIZATION; INFLAMMATION; INNATE IMMUNITY; LYMPH NODE; LYMPH NODE HYPERPLASIA; LYMPHOCYTE MIGRATION; LYMPHOCYTE TRAPPING; LYMPHOID ORGAN; MEDULLARY CORD; MOUSE; NONHUMAN; PHENOTYPE; PLASTICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETICULUM CELL; STROMA CELL; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; T ZONE; TISSUE STRUCTURE;

FIBROBLASTS; LYMPH NODE SWELLING; LYMPHOTOXIN; MYD88; STROMAL CELLS;

ADAPTIVE IMMUNITY; ANIMALS; CELL MOVEMENT; CELL PROLIFERATION; DENDRITIC CELLS; FIBROBLASTS; HOMEOSTASIS; INFLAMMATION; LYMPH NODES; LYMPHOCYTE ACTIVATION; LYMPHOCYTES; LYMPHOTOXIN-ALPHA; MICE; MICE, INBRED C57BL; MICROSCOPY, FLUORESCENCE; MYELOID DIFFERENTIATION FACTOR 88; STROMAL CELLS; T-LYMPHOCYTES;

EID: 84891940082     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1312585111     Document Type: Article

References (56)

1. Mueller SN, Germain RN (2009) Stromal cell contributions to the homeostasis and functionality of the immune system. Nat Rev Immunol 9(9): 618-629.
2. Turley SJ, Fletcher AL, Elpek KG (2010) The stromal and haematopoietic antigenpresenting cells that reside in secondary lymphoid organs. Nat Rev Immunol 10(12): 813-825.
3. Link A, et al. (2007) Fibroblastic reticular cells in lymph nodes regulate the homeostasis of naive T cells. Nat Immunol 8(11): 1255-1265.
4. Angeli V, et al. (2006) B cell-driven lymphangiogenesis in inflamed lymph nodes enhances dendritic cell mobilization. Immunity 24(2): 203-215.
5. Mohr E, et al. (2009) Dendritic cells and monocyte/macrophages that create the IL-6/ APRIL-rich lymph node microenvironments where plasmablasts mature. J Immunol 182(4): 2113-2123.
6. Abe J, et al. (2012) B cells regulate antibody responses through the medullary remodeling of inflamed lymph nodes. Int Immunol 24(1): 17-27.
7. Bajénoff M, et al. (2006) Stromal cell networks regulate lymphocyte entry, migration, and territoriality in lymph nodes. Immunity 25(6): 989-1001.
8. Siegert S, Luther SA (2012) Positive and negative regulation of T cell responses by fibroblastic reticular cells within paracortical regions of lymph nodes. Front Immunol 3:285.
9. Chyou S, et al. (2008) Fibroblast-type reticular stromal cells regulate the lymph node vasculature. J Immunol 181(6): 3887-3896.
10. Katakai T, et al. (2008) Organizer-like reticular stromal cell layer common to adult secondary lymphoid organs. J Immunol 181(9): 6189-6200.
11. Cyster JG, Schwab SR (2012) Sphingosine-1-phosphate and lymphocyte egress from lymphoid organs. Annu Rev Immunol 30: 69-94.
12. Zhu MZ, Fu YX (2011) The role of core TNF/LIGHT family members in lymph node homeostasis and remodeling. Immunol Rev 244(1): 75-84.
13. Tan KW, et al. (2012) Expansion of cortical and medullary sinuses restrains lymph node hypertrophy during prolonged inflammation. J Immunol 188(8): 4065-4080.
14. Webster B, et al. (2006) Regulation of lymph node vascular growth by dendritic cells. J Exp Med 203(8): 1903-1913.
15. Girard JP, Moussion C, Förster R (2012) HEVs, lymphatics and homeostatic immune cell trafficking in lymph nodes. Nat Rev Immunol 12(11): 762-773.
16. Katakai T, Hara T, Sugai M, Gonda H, Shimizu A (2004) Lymph node fibroblastic reticular cells construct the stromal reticulum via contact with lymphocytes. J Exp Med 200(6): 783-795.
17. Chyou S, et al. (2011) Coordinated regulation of lymph node vascular-stromal growth first by CD11c+ cells and then by T and B cells. J Immunol 187(11): 5558-5567.
18. Hess E, et al. (2012) RANKL induces organized lymph node growth by stromal cell proliferation. J Immunol 188(3): 1245-1254.
19. Tzeng TC, et al. (2010) CD11c(hi) dendritic cells regulate the re-establishment of vascular quiescence and stabilization after immune stimulation of lymph nodes. J Immunol 184(8): 4247-4257.
20. Mueller SN, et al. (2007) Regulation of homeostatic chemokine expression and cell trafficking during immune responses. Science 317(5838): 670-674.
21. Scandella E, et al. (2008) Restoration of lymphoid organ integrity through the interaction of lymphoid tissue-inducer cells with stroma of the T cell zone. Nat Immunol 9(6): 667-675.
22. Vega F, et al. (2006) Tissue-specific function of lymph node fibroblastic reticulum cells. Pathobiology 73(2): 71-81.
23. Benedict CA, et al. (2006) Specific remodeling of splenic architecture by cytomegalovirus. PLoS Pathog 2(3):e16.
24. Bekiaris V, et al. (2008) Ly49H+ NK cells migrate to and protect splenic white pulp stroma from murine cytomegalovirus infection. J Immunol 180(10): 6768-6776.
25. Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C, Brown RA (2002) Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol 3(5): 349-363.
26. Martin-Fontecha A, et al. (2003) Regulation of dendritic cell migration to the draining lymph node: Impact on T lymphocyte traffic and priming. J Exp Med 198(4): 615-621.
27. Boyman O, Ramsey C, Kim DM, Sprent J, Surh CD (2008) IL-7/anti-IL-7 mAb complexes restore T cell development and induce homeostatic T cell expansion without lymphopenia. J Immunol 180(11): 7265-7275.
28. Noss EH, Brenner MB (2008) The role and therapeutic implications of fibroblast-like synoviocytes in inflammation and cartilage erosion in rheumatoid arthritis. Immunol Rev 223: 252-270.
29. Schneider K, Potter KG, Ware CF (2004) Lymphotoxin and LIGHT signaling pathways and target genes. Immunol Rev 202: 49-66.
30. Moussion C, Girard JP (2011) Dendritic cells control lymphocyte entry to lymph nodes through high endothelial venules. Nature 479(7374): 542-546.
31. Prlic M, Hernandez-Hoyos G, Bevan MJ (2006) Duration of the initial TCR stimulus controls the magnitude but not functionality of the CD8+ T cell response. J Exp Med 203(9): 2135-2143.
32. Bénézech C, et al. (2012) Lymphotoxin-β receptor signaling through NF-κB2-RelB pathway reprograms adipocyte precursors as lymph node stromal cells. Immunity 37(4): 721-734.
33. Reilkoff RA, Bucala R, Herzog EL (2011) Fibrocytes: Emerging effector cells in chronic inflammation. Nat Rev Immunol 11(6): 427-435.
34. Gretz JE, Norbury CC, Anderson AO, Proudfoot AEI, Shaw S (2000) Lymph-borne chemokines and other low molecular weight molecules reach high endothelial venules via specialized conduits while a functional barrier limits access to the lymphocyte microenvironments in lymph node cortex. J Exp Med 192(10): 1425-1440.
35. Liao S, Ruddle NH (2006) Synchrony of high endothelial venules and lymphatic vessels revealed by immunization. J Immunol 177(5): 3369-3379.
36. Probst HC, et al. (2005) Histological analysis of CD11c-DTR/GFP mice after in vivo depletion of dendritic cells. Clin Exp Immunol 141(3): 398-404.
37. Malhotra D, et al.; Immunological Genome Project Consortium (2012) Transcriptional profiling of stroma from inflamed and resting lymph nodes defines immunological hallmarks. Nat Immunol 13(5): 499-510.
38. Ware CF (2008) Targeting lymphocyte activation through the lymphotoxin and LIGHT pathways. Immunol Rev 223: 186-201.
39. Ngo VN, Cornall RJ, Cyster JG (2001) Splenic T zone development is B cell dependent. J Exp Med 194(11): 1649-1660.
40. Wendland M, et al. (2011) Lymph node T cell homeostasis relies on steady-state homing of dendritic cells. Immunity 35(6): 945-957.
41. Ngo VN, et al. (1999) Lymphotoxin alpha/beta and tumor necrosis factor are required for stromal cell expression of homing chemokines in B and T cell areas of the spleen. J Exp Med 189(2): 403-412.
42. Kumar V, et al. (2010) Global lymphoid tissue remodeling during a viral infection is orchestrated by a B cell-lymphotoxin-dependent pathway. Blood 115(23): 4725-4733.
43. Roozendaal R, Mebius RE, Kraal G (2008) The conduit system of the lymph node. Int Immunol 20(12): 1483-1487.
44. Tomei AA, Siegert S, Britschgi MR, Luther SA, Swartz MA (2009) Fluid flow regulates stromal cell organization and CCL21 expression in a tissue-engineered lymph node microenvironment. J Immunol 183(7): 4273-4283.
45. Siegert S, et al. (2011) Fibroblastic reticular cells from lymph nodes attenuate T cell expansion by producing nitric oxide. PLoS ONE 6(11):e27618.
46. Adachi O, et al. (1998) Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 9(1): 143-150.
47. Yamamoto M, et al. (2003) Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science 301(5633): 640-643.
48. Takeuchi O, et al. (1999) Differential roles of TLR2 and TLR4 in recognition of gramnegative and gram-positive bacterial cell wall components. Immunity 11(4): 443-451.
49. Hoshino K, et al. (1999) Cutting edge. Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: Evidence for TLR4 as the Lps gene product. J Immunol 162(7): 3749-3752.
50. Senn KA, et al. (2000) T1-deficient and T1-Fc-transgenic mice develop a normal protective Th2-type immune response following infection with Nippostrongylus brasiliensis. Eur J Immunol 30(7): 1929-1938.
51. Sun Z, et al. (2000) Requirement for RORgamma in thymocyte survival and lymphoid organ development. Science 288(5475): 2369-2373.
52. Koni PA, et al. (1997) Distinct roles in lymphoid organogenesis for lymphotoxins alpha and beta revealed in lymphotoxin beta-deficient mice. Immunity 6(4): 491-500.
53. Müller U, et al. (1994) Functional role of type I and type II interferons in antiviral defense. Science 264(5167): 1918-1921.
54. Vogt TK, Link A, Perrin J, Finke D, Luther SA (2009) Novel function for interleukin-7 in dendritic cell development. Blood 113(17): 3961-3968.
55. Manley PW, et al. (2010) Structural resemblances and comparisons of the relative pharmacological properties of imatinib and nilotinib. Bioorg Med Chem 18(19): 6977-6986.
56. Manley PW, et al. (2002) Anthranilic acid amides: A novel class of antiangiogenic VEGF receptor kinase inhibitors. J Med Chem 45(26): 5687-5693.