Skip to main content
Top
Published in: BMC Immunology 1/2014

Open Access 01-12-2014 | Research article

T lymphocytes maintain structure and function of fibroblastic reticular cells via lymphotoxin (LT)-B

Authors: Lintao Zhao, Lina Liu, Jianbao Gao, Yang Yang, Chunyan Hu, Bo Guo, Bo Zhu

Published in: BMC Immunology | Issue 1/2014

Login to get access

Abstract

Background

Although a lot is known about how Fibroblastic Reticular Cells (FRCs) can regulate T lymphocytes (T cells), little is understood about whether or how T cells can regulate FRCs.

Results

This study shows that the absence of T cells inhibited the secretion of ER-TR7 by splenic FRCs, induced the structural disorder of FRCs, down-regulated the expression of the chemokine ligands CCL21 and CCL19, and weakened the homing ability of T cells to the spleen of nude mice. Transfusion of T cells from BALB/c mice restored the structure and functions of FRCs and recovered them. The expression of lymphotoxin (LT)-B was significantly downregulated in the absence of T cells from nude mice and was recovered after the transfusion of T cells. After the occlusion of the LT-B receptor, the FRCs' structure and functions were not restored by transfusion of T cells.

Conclusions

These data reveal that the absence of T cells will subject spleen FRCs to structural and functional abnormality, and weaken the homing ability of T cells to the spleen. These changes are attributed to the T-cell- derived LT-B.
Appendix
Available only for authorised users
Literature
1.
go back to reference Mueller SN, Germain RN: Stromal cell contributions to the homeostasis and functionality of the immune system. Nat Rev Immunol. 2009, 9: 618-629.PubMedPubMedCentral Mueller SN, Germain RN: Stromal cell contributions to the homeostasis and functionality of the immune system. Nat Rev Immunol. 2009, 9: 618-629.PubMedPubMedCentral
2.
go back to reference Turley SJ, Fletcher AL, Elpek KG: The stromal and haematopoietic antigen-presenting cells that reside in secondary lymphoid organs. Nat Rev Immunol. 2010, 10: 813-825. 10.1038/nri2886.PubMedCrossRef Turley SJ, Fletcher AL, Elpek KG: The stromal and haematopoietic antigen-presenting cells that reside in secondary lymphoid organs. Nat Rev Immunol. 2010, 10: 813-825. 10.1038/nri2886.PubMedCrossRef
3.
go back to reference Klaus GG, Humphrey JH, Kunkl A, Dongworth DW: The follicular dendritic cell: its role in antigen presentation in the generation of immunological memory. Immunol Rev. 1980, 53: 3-28. 10.1111/j.1600-065X.1980.tb01038.x.PubMedCrossRef Klaus GG, Humphrey JH, Kunkl A, Dongworth DW: The follicular dendritic cell: its role in antigen presentation in the generation of immunological memory. Immunol Rev. 1980, 53: 3-28. 10.1111/j.1600-065X.1980.tb01038.x.PubMedCrossRef
4.
go back to reference Link A, Vogt TK, Favre S, Britschgi MR, Acha-Orbea H, Hinz B, Cyster JG, Luther SA: Fibroblastic reticular cells in lymph nodes regulate the homeostasis of naive T cells. Nat Immunol. 2007, 8: 1255-1265. 10.1038/ni1513.PubMedCrossRef Link A, Vogt TK, Favre S, Britschgi MR, Acha-Orbea H, Hinz B, Cyster JG, Luther SA: Fibroblastic reticular cells in lymph nodes regulate the homeostasis of naive T cells. Nat Immunol. 2007, 8: 1255-1265. 10.1038/ni1513.PubMedCrossRef
5.
go back to reference Sixt M, Kanazawa N, Seig M, Samson T, Roos G, Reinhardt DP, Pabst R, Lutz MB, Sorokin L: The conduit system transports soluble antigens from the afferent lymph to resident dendritic cells in the T cell area of the lymph node. Immunity. 2005, 22: 19-29. 10.1016/j.immuni.2004.11.013.PubMedCrossRef Sixt M, Kanazawa N, Seig M, Samson T, Roos G, Reinhardt DP, Pabst R, Lutz MB, Sorokin L: The conduit system transports soluble antigens from the afferent lymph to resident dendritic cells in the T cell area of the lymph node. Immunity. 2005, 22: 19-29. 10.1016/j.immuni.2004.11.013.PubMedCrossRef
6.
go back to reference Bajenoff M, Egen JG, Koo LY, Laugier JP, Brau F, Glaichenhaus N, Germain RN: Stromal cell networks regulate lymphocyte entry, migration, and territoriality in lymph nodes. Immunity. 2006, 25: 989-1001. 10.1016/j.immuni.2006.10.011.PubMedPubMedCentralCrossRef Bajenoff M, Egen JG, Koo LY, Laugier JP, Brau F, Glaichenhaus N, Germain RN: Stromal cell networks regulate lymphocyte entry, migration, and territoriality in lymph nodes. Immunity. 2006, 25: 989-1001. 10.1016/j.immuni.2006.10.011.PubMedPubMedCentralCrossRef
7.
go back to reference Mueller SN, Hosiawa-Meagher KA, Konieczny BT, Sullivan BM, Bachmann MF, Locksley RM, Ahmed R, Matloubian M: Regulation of homeostatic chemokine expression and cell trafficking during immune responses. Science. 2007, 317: 670-674. 10.1126/science.1144830.PubMedCrossRef Mueller SN, Hosiawa-Meagher KA, Konieczny BT, Sullivan BM, Bachmann MF, Locksley RM, Ahmed R, Matloubian M: Regulation of homeostatic chemokine expression and cell trafficking during immune responses. Science. 2007, 317: 670-674. 10.1126/science.1144830.PubMedCrossRef
8.
go back to reference Onder L, Narang P, Scandella E, Chai Q, Iolyeva M, Hoorweg K, Halin C, Richie E, Kaye P, Westermann J: IL-7-producing stromal cells are critical for lymph node remodeling. Blood. 2012, 120: 4675-4683. 10.1182/blood-2012-03-416859.PubMedPubMedCentralCrossRef Onder L, Narang P, Scandella E, Chai Q, Iolyeva M, Hoorweg K, Halin C, Richie E, Kaye P, Westermann J: IL-7-producing stromal cells are critical for lymph node remodeling. Blood. 2012, 120: 4675-4683. 10.1182/blood-2012-03-416859.PubMedPubMedCentralCrossRef
9.
go back to reference Fry TJ, Mackall CL: The many faces of IL-7: from lymphopoiesis to peripheral T cell maintenance. J Immunol. 2005, 174: 6571-6576. 10.4049/jimmunol.174.11.6571.PubMedCrossRef Fry TJ, Mackall CL: The many faces of IL-7: from lymphopoiesis to peripheral T cell maintenance. J Immunol. 2005, 174: 6571-6576. 10.4049/jimmunol.174.11.6571.PubMedCrossRef
10.
go back to reference Junt T, Tumanov AV, Harris N, Heikenwalder M, Zeller N, Kuprash DV, Aguzzi A, Ludewig B, Nedospasov SA, Zinkernagel RM: Expression of lymphotoxin beta governs immunity at two distinct levels. Eur J Immunol. 2006, 36: 2061-2075. 10.1002/eji.200626255.PubMedCrossRef Junt T, Tumanov AV, Harris N, Heikenwalder M, Zeller N, Kuprash DV, Aguzzi A, Ludewig B, Nedospasov SA, Zinkernagel RM: Expression of lymphotoxin beta governs immunity at two distinct levels. Eur J Immunol. 2006, 36: 2061-2075. 10.1002/eji.200626255.PubMedCrossRef
11.
go back to reference Tumanov AV, Kuprash DV, Nedospasov SA: The role of lymphotoxin in development and maintenance of secondary lymphoid tissues. Cytokine Growth Factor Rev. 2003, 14: 275-288. 10.1016/S1359-6101(03)00026-1.PubMedCrossRef Tumanov AV, Kuprash DV, Nedospasov SA: The role of lymphotoxin in development and maintenance of secondary lymphoid tissues. Cytokine Growth Factor Rev. 2003, 14: 275-288. 10.1016/S1359-6101(03)00026-1.PubMedCrossRef
12.
go back to reference Zeng M, Paiardini M, Engram JC, Beilman GJ, Chipman JG, Schacker TW, Silvestri G, Haase AT: Critical role of CD4 T cells in maintaining lymphoid tissue structure for immune cell homeostasis and reconstitution. Blood. 2012, 120: 1856-1867. 10.1182/blood-2012-03-418624.PubMedPubMedCentralCrossRef Zeng M, Paiardini M, Engram JC, Beilman GJ, Chipman JG, Schacker TW, Silvestri G, Haase AT: Critical role of CD4 T cells in maintaining lymphoid tissue structure for immune cell homeostasis and reconstitution. Blood. 2012, 120: 1856-1867. 10.1182/blood-2012-03-418624.PubMedPubMedCentralCrossRef
13.
go back to reference Bajenoff M, Glaichenhaus N, Germain RN: Fibroblastic reticular cells guide T lymphocyte entry into and migration within the splenic T cell zone. J Immunol. 2008, 181: 3947-3954. 10.4049/jimmunol.181.6.3947.PubMedPubMedCentralCrossRef Bajenoff M, Glaichenhaus N, Germain RN: Fibroblastic reticular cells guide T lymphocyte entry into and migration within the splenic T cell zone. J Immunol. 2008, 181: 3947-3954. 10.4049/jimmunol.181.6.3947.PubMedPubMedCentralCrossRef
14.
go back to reference Katakai T, Hara T, Sugai M, Gonda H, Shimuzu A: Lymph node fibroblastic reticular cells construct the stromal reticulum via contact with lymphocytes. J Exp Med. 2004, 200: 783-795. 10.1084/jem.20040254.PubMedPubMedCentralCrossRef Katakai T, Hara T, Sugai M, Gonda H, Shimuzu A: Lymph node fibroblastic reticular cells construct the stromal reticulum via contact with lymphocytes. J Exp Med. 2004, 200: 783-795. 10.1084/jem.20040254.PubMedPubMedCentralCrossRef
15.
go back to reference Malhotra D, Fletcher AL, Astarita J, Lukacs-Kornek V, Tayalia P, Gonzalez SF, Elpek KG, Chang SK, Knoblich K, Hemler ME: Transcriptional profiling of stroma from inflamed and resting lymph nodes defines immunological hallmarks. Nat Immunol. 2012, 13: 499-U107. 10.1038/ni.2262.PubMedPubMedCentralCrossRef Malhotra D, Fletcher AL, Astarita J, Lukacs-Kornek V, Tayalia P, Gonzalez SF, Elpek KG, Chang SK, Knoblich K, Hemler ME: Transcriptional profiling of stroma from inflamed and resting lymph nodes defines immunological hallmarks. Nat Immunol. 2012, 13: 499-U107. 10.1038/ni.2262.PubMedPubMedCentralCrossRef
16.
go back to reference Levy Y, Lacabaratz C, Weiss L, Viard JP, Goujard C, Lelievre JD, Rouzioux C, Avettand-Fenoel V: Enhanced T cell recovery in HIV-adults through IL-7 treatment. J Clin Investig. 2009, 119: 997-1007.PubMedPubMedCentral Levy Y, Lacabaratz C, Weiss L, Viard JP, Goujard C, Lelievre JD, Rouzioux C, Avettand-Fenoel V: Enhanced T cell recovery in HIV-adults through IL-7 treatment. J Clin Investig. 2009, 119: 997-1007.PubMedPubMedCentral
17.
go back to reference den Haan JM, Mebius RE, Kraal G: Stromal cells of the mouse spleen. Front Immunol. 2012, 3: 201-201. 10.3389/fimmu.2012.00201.PubMed den Haan JM, Mebius RE, Kraal G: Stromal cells of the mouse spleen. Front Immunol. 2012, 3: 201-201. 10.3389/fimmu.2012.00201.PubMed
18.
19.
go back to reference Malhotra D, Fletcher AL, Turley SJ: Stromal and hematopoietic cells in secondary lymphoid organs: partners in immunity. Immunol Rev. 2013, 251: 160-176. 10.1111/imr.12023.PubMedPubMedCentralCrossRef Malhotra D, Fletcher AL, Turley SJ: Stromal and hematopoietic cells in secondary lymphoid organs: partners in immunity. Immunol Rev. 2013, 251: 160-176. 10.1111/imr.12023.PubMedPubMedCentralCrossRef
20.
go back to reference Siegert S, Luther SA: Positive and negative regulation of T cell responses by fibroblastic reticular cells within paracortical regions of lymph nodes. Front Immunol. 2012, 3: 285-285. 10.3389/fimmu.2012.00285.PubMedPubMedCentralCrossRef Siegert S, Luther SA: Positive and negative regulation of T cell responses by fibroblastic reticular cells within paracortical regions of lymph nodes. Front Immunol. 2012, 3: 285-285. 10.3389/fimmu.2012.00285.PubMedPubMedCentralCrossRef
21.
go back to reference Gretz JE, Kaldjian EP, Anderson AO, Shaw S: Sophisticated strategies for information encounter in the lymph node: the reticular network as a conduit of soluble information and a highway for cell traffic. J Immunol. 1996, 157: 495-499.PubMed Gretz JE, Kaldjian EP, Anderson AO, Shaw S: Sophisticated strategies for information encounter in the lymph node: the reticular network as a conduit of soluble information and a highway for cell traffic. J Immunol. 1996, 157: 495-499.PubMed
22.
go back to reference Luther SA, Bidgol A, Hargreaves DC, Schmidt A, Xu Y, Paniyadi J, Matloubian M, Cyster JG: Differing activities of homeostatic chemokines CCL19, CCL21, and CXCL12 in lymphocyte and dendritic cell recruitment and lymphoid neogenesis. J Immunol. 2002, 169: 424-433. 10.4049/jimmunol.169.1.424.PubMedCrossRef Luther SA, Bidgol A, Hargreaves DC, Schmidt A, Xu Y, Paniyadi J, Matloubian M, Cyster JG: Differing activities of homeostatic chemokines CCL19, CCL21, and CXCL12 in lymphocyte and dendritic cell recruitment and lymphoid neogenesis. J Immunol. 2002, 169: 424-433. 10.4049/jimmunol.169.1.424.PubMedCrossRef
23.
go back to reference Koni PA, Sacca R, Lawton P, Browning JL, Ruddle NH, Flavell RA: Distinct roles in lymphoid organogenesis for lymphotoxins alpha and beta revealed in lymphotoxin beta-deficient mice. Immunity. 1997, 6: 491-500. 10.1016/S1074-7613(00)80292-7.PubMedCrossRef Koni PA, Sacca R, Lawton P, Browning JL, Ruddle NH, Flavell RA: Distinct roles in lymphoid organogenesis for lymphotoxins alpha and beta revealed in lymphotoxin beta-deficient mice. Immunity. 1997, 6: 491-500. 10.1016/S1074-7613(00)80292-7.PubMedCrossRef
24.
go back to reference Korner H, Cook M, Riminton DS, Lemckert FA, Hoek RM, Ledermann B, Kontgen F, Fazekas de St Groth B, Sedgwick JD: Distinct roles for lymphotoxin-alpha and tumor necrosis factor in organogenesis and spatial organization of lymphoid tissue. Eur J Immunol. 1997, 27: 2600-2609. 10.1002/eji.1830271020.PubMedCrossRef Korner H, Cook M, Riminton DS, Lemckert FA, Hoek RM, Ledermann B, Kontgen F, Fazekas de St Groth B, Sedgwick JD: Distinct roles for lymphotoxin-alpha and tumor necrosis factor in organogenesis and spatial organization of lymphoid tissue. Eur J Immunol. 1997, 27: 2600-2609. 10.1002/eji.1830271020.PubMedCrossRef
25.
go back to reference Zeng M, Smith AJ, Wietgrefe SW, Southern PJ, Schacker TW, Reilly CS, Estes JD, Burton GF, Silvestri G, Lifson JD: Cumulative mechanisms of lymphoid tissue fibrosis and T cell depletion in HIV-1 and SIV infections. J Clin Investig. 2011, 121: 998-1008. 10.1172/JCI45157.PubMedPubMedCentralCrossRef Zeng M, Smith AJ, Wietgrefe SW, Southern PJ, Schacker TW, Reilly CS, Estes JD, Burton GF, Silvestri G, Lifson JD: Cumulative mechanisms of lymphoid tissue fibrosis and T cell depletion in HIV-1 and SIV infections. J Clin Investig. 2011, 121: 998-1008. 10.1172/JCI45157.PubMedPubMedCentralCrossRef
26.
go back to reference Yang C-Y, Vogt TK, Favre S, Scarpellino L, Huang H-Y, Tacchini-Cottier F, Luther SA: Trapping of naive lymphocytes triggers rapid growth and remodeling of the fibroblast network in reactive murine lymph nodes. Proc Natl Acad Sci U S A. 2014, 111: E109-E118. 10.1073/pnas.1312585111.PubMedPubMedCentralCrossRef Yang C-Y, Vogt TK, Favre S, Scarpellino L, Huang H-Y, Tacchini-Cottier F, Luther SA: Trapping of naive lymphocytes triggers rapid growth and remodeling of the fibroblast network in reactive murine lymph nodes. Proc Natl Acad Sci U S A. 2014, 111: E109-E118. 10.1073/pnas.1312585111.PubMedPubMedCentralCrossRef
27.
go back to reference Soudja SM, Henri S, Mello M, Chasson L, Mas A, Wehbe M, Auphan-Anezin N, Leserman L, Van den Eynde B, Schmitt-Verhulst A-M: Disrupted lymph node and splenic stroma in mice with induced inflammatory melanomas is associated with impaired recruitment of T and dendritic cells.Plos One 2011, 6., Soudja SM, Henri S, Mello M, Chasson L, Mas A, Wehbe M, Auphan-Anezin N, Leserman L, Van den Eynde B, Schmitt-Verhulst A-M: Disrupted lymph node and splenic stroma in mice with induced inflammatory melanomas is associated with impaired recruitment of T and dendritic cells.Plos One 2011, 6.,
Metadata
Title
T lymphocytes maintain structure and function of fibroblastic reticular cells via lymphotoxin (LT)-B
Authors
Lintao Zhao
Lina Liu
Jianbao Gao
Yang Yang
Chunyan Hu
Bo Guo
Bo Zhu
Publication date
01-12-2014
Publisher
BioMed Central
Published in
BMC Immunology / Issue 1/2014
Electronic ISSN: 1471-2172
DOI
https://doi.org/10.1186/s12865-014-0033-4

Other articles of this Issue 1/2014

BMC Immunology 1/2014 Go to the issue