Follicular dendritic cells emerge from ubiquitous perivascular precursors

Nike Julia Krautler; Veronika Kana; Jan Kranich; Yinghua Tian; Dushan Perera; Doreen Lemm; Petra Schwarz; Annika Armulik; Jeffrey L. Browning; Michelle Tallquist; Thorsten Buch; José B. Oliveira-Martins; Caihong Zhu; Mario Hermann; Ulrich Wagner; Robert Brink; Mathias Heikenwalder; Adriano Aguzzi

doi:10.1016/j.cell.2012.05.032

Follicular dendritic cells emerge from ubiquitous perivascular precursors

Nike Julia Krautler, Veronika Kana, Jan Kranich, Yinghua Tian, Dushan Perera, Doreen Lemm, Petra Schwarz, Annika Armulik, Jeffrey L. Browning, Michelle Tallquist, Thorsten Buch, José B. Oliveira-Martins, Caihong Zhu, Mario Hermann, Ulrich Wagner, Robert Brink, Mathias Heikenwalder, Adriano Aguzzi

Research output: Contribution to journal › Article › peer-review

316 Scopus citations

Abstract

The differentiation of follicular dendritic cells (FDC) is essential to the remarkable microanatomic plasticity of lymphoid follicles. Here we show that FDC arise from ubiquitous perivascular precursors (preFDC) expressing platelet-derived growth factor receptor β (PDGFRβ). PDGFRβ-Cre-driven reporter gene recombination resulted in FDC labeling, whereas conditional ablation of PDGFRβ⁺-derived cells abolished FDC, indicating that FDC originate from PDGFRβ⁺ cells. Lymphotoxin-α-overexpressing prion protein (PrP)⁺ kidneys developed PrP⁺ FDC after transplantation into PrP^- mice, confirming that preFDC exist outside lymphoid organs. Adipose tissue-derived PDGFRβ⁺ stromal-vascular cells responded to FDC maturation factors and, when transplanted into lymphotoxin β receptor (LTβR) ^- kidney capsules, differentiated into Mfge8⁺CD21/35 ⁺FcγRIIβ⁺PrP⁺ FDC capable of trapping immune complexes and recruiting B cells. Spleens of lymphocyte-deficient mice contained perivascular PDGFRβ⁺ FDC precursors whose expansion required both lymphoid tissue inducer (LTi) cells and lymphotoxin. The ubiquity of preFDC and their strategic location at blood vessels may explain the de novo generation of organized lymphoid tissue at sites of lymphocytic inflammation. PaperFlick:

Original language	English
Pages (from-to)	194-206
Number of pages	13
Journal	Cell
Volume	150
Issue number	1
DOIs	https://doi.org/10.1016/j.cell.2012.05.032
State	Published - 6 Jul 2012
Externally published	Yes

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10.1016/j.cell.2012.05.032

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Krautler, N. J., Kana, V., Kranich, J., Tian, Y., Perera, D., Lemm, D., Schwarz, P., Armulik, A., Browning, J. L., Tallquist, M., Buch, T., Oliveira-Martins, J. B., Zhu, C., Hermann, M., Wagner, U., Brink, R., Heikenwalder, M., & Aguzzi, A. (2012). Follicular dendritic cells emerge from ubiquitous perivascular precursors. Cell, 150(1), 194-206. https://doi.org/10.1016/j.cell.2012.05.032

@article{798a5e8c45c94e198a30e85b4d6a8366,

title = "Follicular dendritic cells emerge from ubiquitous perivascular precursors",

abstract = "The differentiation of follicular dendritic cells (FDC) is essential to the remarkable microanatomic plasticity of lymphoid follicles. Here we show that FDC arise from ubiquitous perivascular precursors (preFDC) expressing platelet-derived growth factor receptor β (PDGFRβ). PDGFRβ-Cre-driven reporter gene recombination resulted in FDC labeling, whereas conditional ablation of PDGFRβ+-derived cells abolished FDC, indicating that FDC originate from PDGFRβ+ cells. Lymphotoxin-α-overexpressing prion protein (PrP)+ kidneys developed PrP+ FDC after transplantation into PrP- mice, confirming that preFDC exist outside lymphoid organs. Adipose tissue-derived PDGFRβ+ stromal-vascular cells responded to FDC maturation factors and, when transplanted into lymphotoxin β receptor (LTβR) - kidney capsules, differentiated into Mfge8+CD21/35 +FcγRIIβ+PrP+ FDC capable of trapping immune complexes and recruiting B cells. Spleens of lymphocyte-deficient mice contained perivascular PDGFRβ+ FDC precursors whose expansion required both lymphoid tissue inducer (LTi) cells and lymphotoxin. The ubiquity of preFDC and their strategic location at blood vessels may explain the de novo generation of organized lymphoid tissue at sites of lymphocytic inflammation. PaperFlick:",

author = "Krautler, {Nike Julia} and Veronika Kana and Jan Kranich and Yinghua Tian and Dushan Perera and Doreen Lemm and Petra Schwarz and Annika Armulik and Browning, {Jeffrey L.} and Michelle Tallquist and Thorsten Buch and Oliveira-Martins, {Jos{\'e} B.} and Caihong Zhu and Mario Hermann and Ulrich Wagner and Robert Brink and Mathias Heikenwalder and Adriano Aguzzi",

note = "Funding Information: We thank S. Nagata, M. Kopf, and R. Adams for generously providing Mfge8 −/− , Cd21/35 −/− and Pdgfrb-Cre mice. S. Luther, H. Zeilhofer, S. Uhlig, T. Suter for materials and reagents. D. Junghans, I. Fischer, M. Nuvolone, T. Chtanova, H. Takizawa, T. Phan, and R. Salomon for discussions. R. Moos, M. Delic, A. Wethmar, N. Wey, S. Behnke, A. Fitsche, S. Walters, K. Webster, N. Zammit and J.M. Mateos (Center for Microscopy and Image Analysis, University of Z{\"u}rich) for technical assistance, and R. Kr{\"a}utler for editing. A. Aguzzi is supported by grants of the European Union (PRIORITY and LUPAS), the Swiss National Foundation (SNF) (one individual award and one Sinergia award with T. Buch and P. Pelczar), the Stammbach Foundation, and the Novartis Research Foundation. A. Aguzzi also holds an Advanced Investigator Grant of the European Research Council. N. Krautler and A. Armulik are supported by the SNF. ",

year = "2012",

month = jul,

day = "6",

doi = "10.1016/j.cell.2012.05.032",

language = "English",

volume = "150",

pages = "194--206",

journal = "Cell",

issn = "0092-8674",

publisher = "Elsevier B.V.",

number = "1",

}

Krautler, NJ, Kana, V, Kranich, J, Tian, Y, Perera, D, Lemm, D, Schwarz, P, Armulik, A, Browning, JL, Tallquist, M, Buch, T, Oliveira-Martins, JB, Zhu, C, Hermann, M, Wagner, U, Brink, R, Heikenwalder, M & Aguzzi, A 2012, 'Follicular dendritic cells emerge from ubiquitous perivascular precursors', Cell, vol. 150, no. 1, pp. 194-206. https://doi.org/10.1016/j.cell.2012.05.032

TY - JOUR

T1 - Follicular dendritic cells emerge from ubiquitous perivascular precursors

AU - Krautler, Nike Julia

AU - Kana, Veronika

AU - Kranich, Jan

AU - Tian, Yinghua

AU - Perera, Dushan

AU - Lemm, Doreen

AU - Schwarz, Petra

AU - Armulik, Annika

AU - Browning, Jeffrey L.

AU - Tallquist, Michelle

AU - Buch, Thorsten

AU - Oliveira-Martins, José B.

AU - Zhu, Caihong

AU - Hermann, Mario

AU - Wagner, Ulrich

AU - Brink, Robert

AU - Heikenwalder, Mathias

AU - Aguzzi, Adriano

N1 - Funding Information: We thank S. Nagata, M. Kopf, and R. Adams for generously providing Mfge8 −/− , Cd21/35 −/− and Pdgfrb-Cre mice. S. Luther, H. Zeilhofer, S. Uhlig, T. Suter for materials and reagents. D. Junghans, I. Fischer, M. Nuvolone, T. Chtanova, H. Takizawa, T. Phan, and R. Salomon for discussions. R. Moos, M. Delic, A. Wethmar, N. Wey, S. Behnke, A. Fitsche, S. Walters, K. Webster, N. Zammit and J.M. Mateos (Center for Microscopy and Image Analysis, University of Zürich) for technical assistance, and R. Kräutler for editing. A. Aguzzi is supported by grants of the European Union (PRIORITY and LUPAS), the Swiss National Foundation (SNF) (one individual award and one Sinergia award with T. Buch and P. Pelczar), the Stammbach Foundation, and the Novartis Research Foundation. A. Aguzzi also holds an Advanced Investigator Grant of the European Research Council. N. Krautler and A. Armulik are supported by the SNF.

PY - 2012/7/6

Y1 - 2012/7/6

N2 - The differentiation of follicular dendritic cells (FDC) is essential to the remarkable microanatomic plasticity of lymphoid follicles. Here we show that FDC arise from ubiquitous perivascular precursors (preFDC) expressing platelet-derived growth factor receptor β (PDGFRβ). PDGFRβ-Cre-driven reporter gene recombination resulted in FDC labeling, whereas conditional ablation of PDGFRβ+-derived cells abolished FDC, indicating that FDC originate from PDGFRβ+ cells. Lymphotoxin-α-overexpressing prion protein (PrP)+ kidneys developed PrP+ FDC after transplantation into PrP- mice, confirming that preFDC exist outside lymphoid organs. Adipose tissue-derived PDGFRβ+ stromal-vascular cells responded to FDC maturation factors and, when transplanted into lymphotoxin β receptor (LTβR) - kidney capsules, differentiated into Mfge8+CD21/35 +FcγRIIβ+PrP+ FDC capable of trapping immune complexes and recruiting B cells. Spleens of lymphocyte-deficient mice contained perivascular PDGFRβ+ FDC precursors whose expansion required both lymphoid tissue inducer (LTi) cells and lymphotoxin. The ubiquity of preFDC and their strategic location at blood vessels may explain the de novo generation of organized lymphoid tissue at sites of lymphocytic inflammation. PaperFlick:

AB - The differentiation of follicular dendritic cells (FDC) is essential to the remarkable microanatomic plasticity of lymphoid follicles. Here we show that FDC arise from ubiquitous perivascular precursors (preFDC) expressing platelet-derived growth factor receptor β (PDGFRβ). PDGFRβ-Cre-driven reporter gene recombination resulted in FDC labeling, whereas conditional ablation of PDGFRβ+-derived cells abolished FDC, indicating that FDC originate from PDGFRβ+ cells. Lymphotoxin-α-overexpressing prion protein (PrP)+ kidneys developed PrP+ FDC after transplantation into PrP- mice, confirming that preFDC exist outside lymphoid organs. Adipose tissue-derived PDGFRβ+ stromal-vascular cells responded to FDC maturation factors and, when transplanted into lymphotoxin β receptor (LTβR) - kidney capsules, differentiated into Mfge8+CD21/35 +FcγRIIβ+PrP+ FDC capable of trapping immune complexes and recruiting B cells. Spleens of lymphocyte-deficient mice contained perivascular PDGFRβ+ FDC precursors whose expansion required both lymphoid tissue inducer (LTi) cells and lymphotoxin. The ubiquity of preFDC and their strategic location at blood vessels may explain the de novo generation of organized lymphoid tissue at sites of lymphocytic inflammation. PaperFlick:

UR - http://www.scopus.com/inward/record.url?scp=84863632660&partnerID=8YFLogxK

U2 - 10.1016/j.cell.2012.05.032

DO - 10.1016/j.cell.2012.05.032

M3 - Article

C2 - 22770220

AN - SCOPUS:84863632660

SN - 0092-8674

VL - 150

SP - 194

EP - 206

JO - Cell

JF - Cell

IS - 1

ER -

Follicular dendritic cells emerge from ubiquitous perivascular precursors

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