Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Subscribe

Logo for

Science 323 (5922): 1722-1725

Copyright © 2009 by the American Association for the Advancement of Science

CD24 and Siglec-10 Selectively Repress Tissue Damage–Induced Immune Responses

Guo-Yun Chen,1 Jie Tang,4 Pan Zheng,1,2* Yang Liu1,3*

Abstract: Patten recognition receptors, which recognize pathogens or components of injured cells (danger), trigger activation of the innate immune system. Whether and how the host distinguishes between danger- versus pathogen-associated molecular patterns remains unresolved. We report that CD24-deficient mice exhibit increased susceptibility to danger- but not pathogen-associated molecular patterns. CD24 associates with high mobility group box 1, heat shock protein 70, and heat shock protein 90; negatively regulates their stimulatory activity; and inhibits nuclear factor {kappa}B (NF-{kappa}B) activation. This occurs at least in part through CD24 association with Siglec-10 in humans or Siglec-G in mice. Our results reveal that the CD24–Siglec G pathway protects the host against a lethal response to pathological cell death and discriminates danger- versus pathogen-associated molecular patterns.

1 Division of Immunotherapy, Department of Surgery, University of Michigan School of Medicine, Ann Arbor, MI 48109, USA.
2 Department of Pathology, University of Michigan School of Medicine, Ann Arbor, MI 48109, USA.
3 Department of Internal Medicine, University of Michigan School of Medicine, Ann Arbor, MI 48109, USA.
4 Institute of Biophysics, Chinese Academy of Science, Beijing, China.

* To whom correspondence should be addressed. E-mail: yangl{at}umich.edu (Y.L.), panz{at}umich.edu (P.Z.)


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
High-mobility group box-1 and its role in angiogenesis.
S. Yang, L. Xu, T. Yang, and F. Wang (2014)
J. Leukoc. Biol. 95, 563-574
   Abstract »    Full Text »    PDF »
Siglec-G Deficiency Leads to More Severe Collagen-Induced Arthritis and Earlier Onset of Lupus-like Symptoms in MRL/lpr Mice.
S. Bokers, A. Urbat, C. Daniel, K. Amann, K. G. C. Smith, M. Espeli, and L. Nitschke (2014)
J. Immunol. 192, 2994-3002
   Abstract »    Full Text »    PDF »
CD24-Triggered Caspase-Dependent Apoptosis via Mitochondrial Membrane Depolarization and Reactive Oxygen Species Production of Human Neutrophils Is Impaired in Sepsis.
M. Parlato, F. Souza-Fonseca-Guimaraes, F. Philippart, B. Misset, Captain Study Group, M. Adib-Conquy, J.-M. Cavaillon, S. Jacqmin, D. Journois, A. Lagrange, et al. (2014)
J. Immunol. 192, 2449-2459
   Abstract »    Full Text »    PDF »
Mast Cell Chymase Degrades the Alarmins Heat Shock Protein 70, Biglycan, HMGB1, and Interleukin-33 (IL-33) and Limits Danger-induced Inflammation.
A. Roy, G. Ganesh, H. Sippola, S. Bolin, O. Sawesi, A. Dagalv, S. M. Schlenner, T. Feyerabend, H.-R. Rodewald, L. Kjellen, et al. (2014)
J. Biol. Chem. 289, 237-250
   Abstract »    Full Text »    PDF »
The role of high mobility group box chromosomal protein 1 in rheumatoid arthritis.
Y. Chen, W. Sun, R. Gao, Y. Su, H. Umehara, L. Dong, and F. Gong (2013)
Rheumatology 52, 1739-1747
   Abstract »    Full Text »    PDF »
Copresentation of Antigen and Ligands of Siglec-G Induces B Cell Tolerance Independent of CD22.
F. Pfrengle, M. S. Macauley, N. Kawasaki, and J. C. Paulson (2013)
J. Immunol. 191, 1724-1731
   Abstract »    Full Text »    PDF »
HMGB1 in Cancer: Good, Bad, or Both?.
R. Kang, Q. Zhang, H. J. Zeh III, M. T. Lotze, and D. Tang (2013)
Clin. Cancer Res. 19, 4046-4057
   Abstract »    Full Text »    PDF »
Cardiovascular Disease and High-Mobility Group Box 1--Is a New Inflammatory Killer in Town?.
P. Cirillo, F. Giallauria, V. D. Palma, F. Maresca, F. Ziviello, M. Bevilacqua, C. Vigorito, and B. Trimarco (2013)
Angiology 64, 343-355
   Abstract »    Full Text »    PDF »
HMGB1 Protein Does Not Mediate the Inflammatory Response in Spontaneous Spinal Cord Regeneration: A HINT FOR CNS REGENERATION.
Y. Dong, Y. Gu, Y. Huan, Y. Wang, Y. Liu, M. Liu, F. Ding, X. Gu, and Y. Wang (2013)
J. Biol. Chem. 288, 18204-18218
   Abstract »    Full Text »    PDF »
The many faces of HMGB1: molecular structure-functional activity in inflammation, apoptosis, and chemotaxis.
H. Yang, D. J. Antoine, U. Andersson, and K. J. Tracey (2013)
J. Leukoc. Biol. 93, 865-873
   Abstract »    Full Text »    PDF »
Messengers without Borders: Mediators of Systemic Inflammatory Response in AKI.
B. B. Ratliff, M. M. Rabadi, R. Vasko, K. Yasuda, and M. S. Goligorsky (2013)
J. Am. Soc. Nephrol. 24, 529-536
   Abstract »    Full Text »    PDF »
HMGB1 in renal ischemic injury.
M. M. Rabadi, T. Ghaly, M. S. Goligorksy, and B. B. Ratliff (2012)
Am J Physiol Renal Physiol 303, F873-F885
   Abstract »    Full Text »    PDF »
Interaction between uric acid and HMGB1 translocation and release from endothelial cells.
M. M. Rabadi, M.-C. Kuo, T. Ghaly, S. M. Rabadi, M. Weber, M. S. Goligorsky, and B. B. Ratliff (2012)
Am J Physiol Renal Physiol 302, F730-F741
   Abstract »    Full Text »    PDF »
High-mobility group nucleosome-binding protein 1 acts as an alarmin and is critical for lipopolysaccharide-induced immune responses.
D. Yang, Y. V. Postnikov, Y. Li, P. Tewary, G. de la Rosa, F. Wei, D. Klinman, T. Gioannini, J. P. Weiss, T. Furusawa, et al. (2012)
J. Exp. Med. 209, 157-171
   Abstract »    Full Text »    PDF »
Immunoprotective Properties of Primary Sertoli Cells in Mice: Potential Functional Pathways that Confer Immune Privilege.
T. J. Doyle, G. Kaur, S. M. Putrevu, E. L. Dyson, M. Dyson, W. T. McCunniff, M. R. Pasham, K. H. Kim, and J. M. Dufour (2012)
Biol Reprod 86, 1-14
   Abstract »    Full Text »    PDF »
Letter to the Glyco-Forum: Since there are PAMPs and DAMPs, there must be SAMPs? Glycan "self-associated molecular patterns" dampen innate immunity, but pathogens can mimic them.
A. Varki (2011)
Glycobiology 21, 1121-1124
   Full Text »    PDF »
PDGFR{alpha}-positive cells in bone marrow are mobilized by high mobility group box 1 (HMGB1) to regenerate injured epithelia.
K. Tamai, T. Yamazaki, T. Chino, M. Ishii, S. Otsuru, Y. Kikuchi, S. Iinuma, K. Saga, K. Nimura, T. Shimbo, et al. (2011)
PNAS 108, 6609-6614
   Abstract »    Full Text »    PDF »
Dangers Within: DAMP Responses to Damage and Cell Death in Kidney Disease.
D. L. Rosin and M. D. Okusa (2011)
J. Am. Soc. Nephrol. 22, 416-425
   Abstract »    Full Text »    PDF »
High-Mobility Group Box Protein 1 Neutralization Reduces Development of Diet-Induced Atherosclerosis in Apolipoprotein E-Deficient Mice.
P. Kanellakis, A. Agrotis, T. S. Kyaw, C. Koulis, I. Ahrens, S. Mori, H. K. Takahashi, K. Liu, K. Peter, M. Nishibori, et al. (2011)
Arterioscler Thromb Vasc Biol 31, 313-319
   Abstract »    Full Text »    PDF »
NFAT5 Regulates T Lymphocyte Homeostasis and CD24-Dependent T Cell Expansion under Pathologic Hypernatremia.
R. Berga-Bolanos, K. Drews-Elger, J. Aramburu, and C. Lopez-Rodriguez (2010)
J. Immunol. 185, 6624-6635
   Abstract »    Full Text »    PDF »
Endogenous IL-10 Attenuates Cisplatin Nephrotoxicity: Role of Dendritic Cells.
R. K. Tadagavadi and W. B. Reeves (2010)
J. Immunol. 185, 4904-4911
   Abstract »    Full Text »    PDF »
Hepatocyte Death: A Clear and Present Danger.
H. Malhi, M. E. Guicciardi, and G. J. Gores (2010)
Physiol Rev 90, 1165-1194
   Abstract »    Full Text »    PDF »
A critical cysteine is required for HMGB1 binding to Toll-like receptor 4 and activation of macrophage cytokine release.
H. Yang, H. S. Hreggvidsdottir, K. Palmblad, H. Wang, M. Ochani, J. Li, B. Lu, S. Chavan, M. Rosas-Ballina, Y. Al-Abed, et al. (2010)
PNAS 107, 11942-11947
   Abstract »    Full Text »    PDF »
In Situ trans Ligands of CD22 Identified by Glycan-Protein Photocross-linking-enabled Proteomics.
T. N. C. Ramya, E. Weerapana, L. Liao, Y. Zeng, H. Tateno, L. Liao, J. R. Yates III, B. F. Cravatt, and J. C. Paulson (2010)
Mol. Cell. Proteomics 9, 1339-1351
   Abstract »    Full Text »    PDF »
Relative Over-Reactivity of Human versus Chimpanzee Lymphocytes: Implications for the Human Diseases Associated with Immune Activation.
P. C. Soto, L. L. Stein, N. Hurtado-Ziola, S. M. Hedrick, and A. Varki (2010)
J. Immunol. 184, 4185-4195
   Abstract »    Full Text »    PDF »
Alleviation of Neurotoxicity by Microglial Human Siglec-11.
Y. Wang and H. Neumann (2010)
J. Neurosci. 30, 3482-3488
   Abstract »    Full Text »    PDF »
Infections and autoimmunity: the multifaceted relationship.
P. Sfriso, A. Ghirardello, C. Botsios, M. Tonon, M. Zen, N. Bassi, F. Bassetto, and A. Doria (2010)
J. Leukoc. Biol. 87, 385-395
   Abstract »    Full Text »    PDF »
Decoration of T-independent antigen with ligands for CD22 and Siglec-G can suppress immunity and induce B cell tolerance in vivo.
B. H. Duong, H. Tian, T. Ota, G. Completo, S. Han, J. L. Vela, M. Ota, M. Kubitz, N. Bovin, J. C. Paulson, et al. (2010)
J. Exp. Med. 207, 173-187
   Abstract »    Full Text »    PDF »
Recognition of Apoptotic Cells by Epithelial Cells: CONSERVED VERSUS TISSUE-SPECIFIC SIGNALING RESPONSES.
V. A. Patel, D. J. Lee, L. Feng, A. Antoni, W. Lieberthal, J. H. Schwartz, J. Rauch, D. S. Ucker, and J. S. Levine (2010)
J. Biol. Chem. 285, 1829-1840
   Abstract »    Full Text »    PDF »
HMGB1 loves company.
M. E. Bianchi (2009)
J. Leukoc. Biol. 86, 573-576
   Abstract »    Full Text »    PDF »
Ethyl pyruvate administration inhibits hepatic tumor growth.
X. Liang, A. Romo de Vivar Chavez, N. E. Schapiro, P. Loughran, S. H. Thorne, A. A. Amoscato, H. J. Zeh, D. Beer-Stolz, M. T. Lotze, and M. E. de Vera (2009)
J. Leukoc. Biol. 86, 599-607
   Abstract »    Full Text »    PDF »
Natural ligands for CD33-related Siglecs?.
A. Varki (2009)
Glycobiology 19, 810-812
   Full Text »    PDF »
IMMUNOLOGY: Dangers In and Out.
M. E. Bianchi and A. A. Manfredi (2009)
Science 323, 1683-1684
   Abstract »    Full Text »    PDF »

To Advertise     Find Products


Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882