Conservation of CD1 intracellular trafficking patterns between mammalian species

Christopher C. Dascher, Kenji Hiromatsu, Xiaowei Xiong, Masahiko Sugita, Janet E. Buhlmann, Ingrid L. Dodge, Stella Y. Lee, Carme Roura-Mir, Gerald F. Watts, Christopher J. Roy, Samuel M. Behar, Daniel L. Clemens, Steven A. Porcelli, Michael B. Brenner

Research output: Contribution to journalArticle

18 Citations (Scopus)

Abstract

Dendritic cells (DC) are potent APCs that sample Ags from the surrounding environment and present them to naive T cells using cell surface Ag-presenting molecules. The DC in both lymphoid and nonlymphoid tissues express high levels of CD1, a cell surface glycoprotein capable of presenting lipids and glycolipids to T cells. Distinct group 1 CD1 isoforms (CD1a, -b, -c) in man are known to traffic to different parts of the endocytic system where microbial Ags may be sampled. Guinea pigs are the only known rodent species that express the group 1 CD1 proteins. Therefore, we examined the expression and trafficking of guinea pig CD1 (gpCD1) isoforms on isolated DC. Confocal microscopy using mAbs specific for individual gpCD1 isoforms revealed differential trafficking of two distinct CD1b isoforms within DC. Colocalization of MHC class II was observed with the gpCD1b1 isoform, consistent with localization in the late endosomes of DC. In contrast, the gpCD1b3 isoform lacks an endosomal sorting motif and remains on the cell surface. Following incubation with Mycobacterium tuberculosis lipoarabinomannan, colocalization of endocytosed lipoarabinomannan with the gpCD1b1 isoform was observed but not with the gpCD1b3 isoform, which remained primarily on the cell surface. These data demonstrate that guinea pig DC express CD1 isoforms with unique trafficking patterns that recapitulate the patterns seen for human CD1 isoforms. This suggests evolutionary pressure for a conserved mechanism in mammals that allows CD1 to sample lipid Ags from various subcompartments of the endocytic system.

Original languageEnglish (US)
Pages (from-to)6951-6958
Number of pages8
JournalJournal of Immunology
Volume169
Issue number12
StatePublished - Dec 15 2002

Fingerprint

Protein Isoforms
Dendritic Cells
Guinea Pigs
T-Lymphocytes
Lipids
Endosomes
Glycolipids
Membrane Glycoproteins
Lymphoid Tissue
Endocytosis
Mycobacterium tuberculosis
Confocal Microscopy
Mammals
Rodentia
Pressure

ASJC Scopus subject areas

  • Immunology

Cite this

Dascher, C. C., Hiromatsu, K., Xiong, X., Sugita, M., Buhlmann, J. E., Dodge, I. L., ... Brenner, M. B. (2002). Conservation of CD1 intracellular trafficking patterns between mammalian species. Journal of Immunology, 169(12), 6951-6958.

Conservation of CD1 intracellular trafficking patterns between mammalian species. / Dascher, Christopher C.; Hiromatsu, Kenji; Xiong, Xiaowei; Sugita, Masahiko; Buhlmann, Janet E.; Dodge, Ingrid L.; Lee, Stella Y.; Roura-Mir, Carme; Watts, Gerald F.; Roy, Christopher J.; Behar, Samuel M.; Clemens, Daniel L.; Porcelli, Steven A.; Brenner, Michael B.

In: Journal of Immunology, Vol. 169, No. 12, 15.12.2002, p. 6951-6958.

Research output: Contribution to journalArticle

Dascher, CC, Hiromatsu, K, Xiong, X, Sugita, M, Buhlmann, JE, Dodge, IL, Lee, SY, Roura-Mir, C, Watts, GF, Roy, CJ, Behar, SM, Clemens, DL, Porcelli, SA & Brenner, MB 2002, 'Conservation of CD1 intracellular trafficking patterns between mammalian species', Journal of Immunology, vol. 169, no. 12, pp. 6951-6958.
Dascher CC, Hiromatsu K, Xiong X, Sugita M, Buhlmann JE, Dodge IL et al. Conservation of CD1 intracellular trafficking patterns between mammalian species. Journal of Immunology. 2002 Dec 15;169(12):6951-6958.
Dascher, Christopher C. ; Hiromatsu, Kenji ; Xiong, Xiaowei ; Sugita, Masahiko ; Buhlmann, Janet E. ; Dodge, Ingrid L. ; Lee, Stella Y. ; Roura-Mir, Carme ; Watts, Gerald F. ; Roy, Christopher J. ; Behar, Samuel M. ; Clemens, Daniel L. ; Porcelli, Steven A. ; Brenner, Michael B. / Conservation of CD1 intracellular trafficking patterns between mammalian species. In: Journal of Immunology. 2002 ; Vol. 169, No. 12. pp. 6951-6958.
@article{41cc9eafd6284e96b55a23850d73ce5d,
title = "Conservation of CD1 intracellular trafficking patterns between mammalian species",
abstract = "Dendritic cells (DC) are potent APCs that sample Ags from the surrounding environment and present them to naive T cells using cell surface Ag-presenting molecules. The DC in both lymphoid and nonlymphoid tissues express high levels of CD1, a cell surface glycoprotein capable of presenting lipids and glycolipids to T cells. Distinct group 1 CD1 isoforms (CD1a, -b, -c) in man are known to traffic to different parts of the endocytic system where microbial Ags may be sampled. Guinea pigs are the only known rodent species that express the group 1 CD1 proteins. Therefore, we examined the expression and trafficking of guinea pig CD1 (gpCD1) isoforms on isolated DC. Confocal microscopy using mAbs specific for individual gpCD1 isoforms revealed differential trafficking of two distinct CD1b isoforms within DC. Colocalization of MHC class II was observed with the gpCD1b1 isoform, consistent with localization in the late endosomes of DC. In contrast, the gpCD1b3 isoform lacks an endosomal sorting motif and remains on the cell surface. Following incubation with Mycobacterium tuberculosis lipoarabinomannan, colocalization of endocytosed lipoarabinomannan with the gpCD1b1 isoform was observed but not with the gpCD1b3 isoform, which remained primarily on the cell surface. These data demonstrate that guinea pig DC express CD1 isoforms with unique trafficking patterns that recapitulate the patterns seen for human CD1 isoforms. This suggests evolutionary pressure for a conserved mechanism in mammals that allows CD1 to sample lipid Ags from various subcompartments of the endocytic system.",
author = "Dascher, {Christopher C.} and Kenji Hiromatsu and Xiaowei Xiong and Masahiko Sugita and Buhlmann, {Janet E.} and Dodge, {Ingrid L.} and Lee, {Stella Y.} and Carme Roura-Mir and Watts, {Gerald F.} and Roy, {Christopher J.} and Behar, {Samuel M.} and Clemens, {Daniel L.} and Porcelli, {Steven A.} and Brenner, {Michael B.}",
year = "2002",
month = "12",
day = "15",
language = "English (US)",
volume = "169",
pages = "6951--6958",
journal = "Journal of Immunology",
issn = "0022-1767",
publisher = "American Association of Immunologists",
number = "12",

}

TY - JOUR

T1 - Conservation of CD1 intracellular trafficking patterns between mammalian species

AU - Dascher, Christopher C.

AU - Hiromatsu, Kenji

AU - Xiong, Xiaowei

AU - Sugita, Masahiko

AU - Buhlmann, Janet E.

AU - Dodge, Ingrid L.

AU - Lee, Stella Y.

AU - Roura-Mir, Carme

AU - Watts, Gerald F.

AU - Roy, Christopher J.

AU - Behar, Samuel M.

AU - Clemens, Daniel L.

AU - Porcelli, Steven A.

AU - Brenner, Michael B.

PY - 2002/12/15

Y1 - 2002/12/15

N2 - Dendritic cells (DC) are potent APCs that sample Ags from the surrounding environment and present them to naive T cells using cell surface Ag-presenting molecules. The DC in both lymphoid and nonlymphoid tissues express high levels of CD1, a cell surface glycoprotein capable of presenting lipids and glycolipids to T cells. Distinct group 1 CD1 isoforms (CD1a, -b, -c) in man are known to traffic to different parts of the endocytic system where microbial Ags may be sampled. Guinea pigs are the only known rodent species that express the group 1 CD1 proteins. Therefore, we examined the expression and trafficking of guinea pig CD1 (gpCD1) isoforms on isolated DC. Confocal microscopy using mAbs specific for individual gpCD1 isoforms revealed differential trafficking of two distinct CD1b isoforms within DC. Colocalization of MHC class II was observed with the gpCD1b1 isoform, consistent with localization in the late endosomes of DC. In contrast, the gpCD1b3 isoform lacks an endosomal sorting motif and remains on the cell surface. Following incubation with Mycobacterium tuberculosis lipoarabinomannan, colocalization of endocytosed lipoarabinomannan with the gpCD1b1 isoform was observed but not with the gpCD1b3 isoform, which remained primarily on the cell surface. These data demonstrate that guinea pig DC express CD1 isoforms with unique trafficking patterns that recapitulate the patterns seen for human CD1 isoforms. This suggests evolutionary pressure for a conserved mechanism in mammals that allows CD1 to sample lipid Ags from various subcompartments of the endocytic system.

AB - Dendritic cells (DC) are potent APCs that sample Ags from the surrounding environment and present them to naive T cells using cell surface Ag-presenting molecules. The DC in both lymphoid and nonlymphoid tissues express high levels of CD1, a cell surface glycoprotein capable of presenting lipids and glycolipids to T cells. Distinct group 1 CD1 isoforms (CD1a, -b, -c) in man are known to traffic to different parts of the endocytic system where microbial Ags may be sampled. Guinea pigs are the only known rodent species that express the group 1 CD1 proteins. Therefore, we examined the expression and trafficking of guinea pig CD1 (gpCD1) isoforms on isolated DC. Confocal microscopy using mAbs specific for individual gpCD1 isoforms revealed differential trafficking of two distinct CD1b isoforms within DC. Colocalization of MHC class II was observed with the gpCD1b1 isoform, consistent with localization in the late endosomes of DC. In contrast, the gpCD1b3 isoform lacks an endosomal sorting motif and remains on the cell surface. Following incubation with Mycobacterium tuberculosis lipoarabinomannan, colocalization of endocytosed lipoarabinomannan with the gpCD1b1 isoform was observed but not with the gpCD1b3 isoform, which remained primarily on the cell surface. These data demonstrate that guinea pig DC express CD1 isoforms with unique trafficking patterns that recapitulate the patterns seen for human CD1 isoforms. This suggests evolutionary pressure for a conserved mechanism in mammals that allows CD1 to sample lipid Ags from various subcompartments of the endocytic system.

UR - http://www.scopus.com/inward/record.url?scp=0037114128&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0037114128&partnerID=8YFLogxK

M3 - Article

VL - 169

SP - 6951

EP - 6958

JO - Journal of Immunology

JF - Journal of Immunology

SN - 0022-1767

IS - 12

ER -