CD13 restricts TLR4 endocytic signal transduction in inflammation

Journal of Immunology

Volumn 194, Issue 9, 2015, Pages 4466-4476

  Ghosh, Mallika ^a   Subramani, Jaganathan ^a,b   Rahman, M Mamunur ^a,c   Shapiro, Linda H ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

^c SCIVAX Life Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; CD14 ANTIGEN; DYNAMIN; HIGH MOBILITY GROUP B1 PROTEIN; INTERFERON REGULATORY FACTOR 3; JANUS KINASE; LIPOPOLYSACCHARIDE; MICROSOMAL AMINOPEPTIDASE; NITRIC OXIDE SYNTHASE; RAB PROTEIN; RAB5 PROTEIN; STAT PROTEIN; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG; MYELOID DIFFERENTIATION FACTOR 88; NITRITE; PROTEIN BINDING;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; BIOACCUMULATION; BONE MARROW CELL; CONTROLLED STUDY; DENDRITIC CELL; ENDOCYTOSIS; ENDOSOME; GENE TARGETING; GENETIC TRANSCRIPTION; IMMUNOMODULATION; IMMUNOREGULATION; IN VIVO STUDY; INFLAMMATION; INNATE IMMUNITY; INTERNALIZATION; ISCHEMIA; MACROPHAGE ACTIVATION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; TISSUE INJURY; UPREGULATION; ANIMAL; CELL MEMBRANE; DRUG EFFECTS; GENE EXPRESSION; GENETICS; IMMUNOLOGY; MACROPHAGE; METABOLISM; SPLEEN;

ANIMALS; ANTIGENS, CD13; CELL MEMBRANE; DENDRITIC CELLS; ENDOCYTOSIS; ENDOSOMES; GENE EXPRESSION; INFLAMMATION; INTERFERON REGULATORY FACTOR-3; ISCHEMIA; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; MYELOID DIFFERENTIATION FACTOR 88; NITRITES; PROTEIN BINDING; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; SPLEEN; TOLL-LIKE RECEPTOR 4;

EID: 84928501302     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1403133     Document Type: Article

References (41)

1. Frantz, S., K. Hu, A. Adamek, J. Wolf, A. Sallam, S. K. Maier, S. Lonning, H. Ling, G. Ertl, and J. Bauersachs. 2008. Transforming growth factor β inhibition increases mortality and left ventricular dilatation after myocardial infarction. Basic Res. Cardiol. 103: 485-492.
2. Caso, J. R., J. M. Pradillo, O. Hurtado, P. Lorenzo, M. A. Moro, and I. Lizasoain. 2007. Toll-like receptor 4 is involved in brain damage and inflammation after experimental stroke. Circulation 115: 1599-1608.
3. Sachdev, U., X. Cui, and E. Tzeng. 2013. HMGB1 and TLR4 mediate skeletal muscle recovery in a murine model of hindlimb ischemia. J. Vasc. Surg. 58: 460-469.
4. Kagan, J. C., T. Su, T. Horng, A. Chow, S. Akira, and R. Medzhitov. 2008. TRAM couples endocytosis of Toll-like receptor 4 to the induction of interferon-β. Nat. Immunol. 9: 361-368.
5. Watts, C. 2008. Location, location, location: identifying the neighborhoods of LPS signaling. Nat. Immunol. 9: 343-345.
6. Zanoni, I., R. Ostuni, L. R. Marek, S. Barresi, R. Barbalat, G. M. Barton, F. Granucci, and J. C. Kagan. 2011. CD14 controls the LPS-induced endocytosis of Toll-like receptor 4. Cell 147: 868-880.
7. Salcedo, R., A. Worschech, M. Cardone, Y. Jones, Z. Gyulai, R. M. Dai, E. Wang, W. Ma, D. Haines, C. O'hUigin, et al. 2010. MyD88-mediated signaling prevents development of adenocarcinomas of the colon: role of interleukin 18. J. Exp. Med. 207: 1625-1636.
8. Reder, A. T., and X. Feng. 2013. Aberrant type I interferon regulation in autoimmunity: opposite directions in MS and SLE, shaped by evolution and body ecology. Front. Immunol. 4: 281.
9. Ghosh, M., B. McAuliffe, J. Subramani, S. Basu, and L. H. Shapiro. 2012. CD13 regulates dendritic cell cross-presentation and T cell responses by inhibiting receptor-mediated antigen uptake. J. Immunol. 188: 5489-5499.
10. Mina-Osorio, P., B. Winnicka, C. O'Conor, C. L. Grant, L. K. Vogel, D. Rodriguez-Pinto, K. V. Holmes, E. Ortega, and L. H. Shapiro. 2008. CD13 is a novel mediator of monocytic/endothelial cell adhesion. J. Leukoc. Biol. 84: 448-459.
11. Winnicka, B., C. O'Conor, W. Schacke, K. Vernier, C. L. Grant, F. H. Fenteany, F. E. Pereira, B. Liang, A. Kaur, R. Zhao, et al. 2010. CD13 is dispensable for normal hematopoiesis and myeloid cell functions in the mouse. J. Leukoc. Biol. 88: 347-359.
12. Pereira, F. E., C. Cronin, M. Ghosh, S. Y. Zhou, M. Agosto, J. Subramani, R. Wang, J. B. Shen, W. Schacke, B. Liang, et al. 2013. CD13 is essential for inflammatory trafficking and infarct healing following permanent coronary artery occlusion in mice. Cardiovasc. Res. 100: 74-83.
13. Rahman, M. M., M. Ghosh, J. Subramani, G. H. Fong, M. E. Carlson, and L. H. Shapiro. 2014. CD13 regulates anchorage and differentiation of the skeletal muscle satellite stem cell population in ischemic injury. Stem Cells 32: 1564-1577.
14. Subramani, J., M. Ghosh, M. M. Rahman, L. A. Caromile, C. Gerber, K. Rezaul, D. K. Han, and L. H. Shapiro. 2013. Tyrosine phosphorylation of CD13 regulates inflammatory cell-cell adhesion and monocyte trafficking. J. Immunol. 191: 3905-3912.
15. Sigismund, S., S. Confalonieri, A. Ciliberto, S. Polo, G. Scita, and P. P. Di Fiore. 2012. Endocytosis and signaling: cell logistics shape the eukaryotic cell plan. Physiol. Rev. 92: 273-366.
16. Husebye, H., Ø. Halaas, H. Stenmark, G. Tunheim, Ø. Sandanger, B. Bogen, A. Brech, E. Latz, and T. Espevik. 2006. Endocytic pathways regulate Toll-like receptor 4 signaling and link innate and adaptive immunity. EMBO J. 25: 683-692.
17. Macia, E., M. Ehrlich, R. Massol, E. Boucrot, C. Brunner, and T. Kirchhausen. 2006. Dynasore, a cell-permeable inhibitor of dynamin. Dev. Cell 10: 839-850.
18. Sadik, C. D., M. Bachmann, J. Pfeilschifter, and H. Mühl. 2009. Activation of interferon regulatory factor-3 via Toll-like receptor 3 and immunomodulatory functions detected in A549 lung epithelial cells exposed to misplaced U1-snRNA. Nucleic Acids Res. 37: 5041-5056.
19. Servant, M. J., N. Grandvaux, and J. Hiscott. 2002. Multiple signaling pathways leading to the activation of interferon regulatory factor 3. Biochem. Pharmacol. 64: 985-992.
20. Scaffidi, P., T. Misteli, and M. E. Bianchi. 2002. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418: 191-195.
21. Ghosh, M., C. Gerber, M. M. Rahman, K. M. Vernier, F. E. Pereira, J. Subramani, L. A. Caromile, and L. H. Shapiro. 2014. Molecular mechanisms regulating CD13-mediated adhesion. Immunology 142: 636-647.
22. Rahman, M. M., J. Subramani, M. Ghosh, J. K. Denninger, K. Takeda, G. H. Fong, M. E. Carlson, and L. H. Shapiro. 2014. CD13 promotes mesenchymal stem cell-mediated regeneration of ischemic muscle. Front. Physiol. 4: 402.
23. Jacobs, A. T., and L. J. Ignarro. 2001. Lipopolysaccharide-induced expression of interferon-β mediates the timing of inducible nitric-oxide synthase induction in RAW 264.7 macrophages. J. Biol. Chem. 276: 47950-47957.
24. Gutierrez, H. H., B. R. Pitt, M. Schwarz, S. C. Watkins, C. Lowenstein, I. Caniggia, P. Chumley, and B. A. Freeman. 1995. Pulmonary alveolar epithelial inducible NO synthase gene expression: regulation by inflammatory mediators. Am. J. Physiol. 268: L501-L508.
25. Burgdorf, S., V. Lukacs-Kornek, and C. Kurts. 2006. The mannose receptor mediates uptake of soluble but not of cell-associated antigen for cross-presentation. J. Immunol. 176: 6770-6776.
26. Kim, H. J., K. Tsoyi, J. M. Heo, Y. J. Kang, M. K. Park, Y. S. Lee, J. H. Lee, H. G. Seo, H. S. Yun-Choi, and K. C. Chang. 2007. Regulation of lipopolysaccharide-induced inducible nitric-oxide synthase expression through the nuclear factor-κB pathway and interferon-β/tyrosine kinase 2/Janus tyrosine kinase 2-signal transducer and activator of transcription-1 signaling cascades by 2-naphthylethyl-6,7-dihydroxy-1,2,3,4-tetrahydroisoquinoline (THI 53), a new synthetic isoquinoline alkaloid. J. Pharmacol. Exp. Ther. 320: 782-789.
27. Huschak, G., K. Zur Nieden, R. Stuttmann, and D. Riemann. 2003. Changes in monocytic expression of aminopeptidase N/CD13 after major trauma. Clin. Exp. Immunol. 134: 491-496.
28. Brieger, A., L. Rink, and H. Haase. 2013. Differential regulation of TLR-dependent MyD88 and TRIF signaling pathways by free zinc ions. J. Immunol. 191: 1808-1817.
29. Kenny, E. F., and L. A. O'Neill. 2008. Signalling adaptors used by Toll-like receptors: an update. Cytokine 43: 342-349.
30. Ishida, A., K. Akita, Y. Mori, S. Tanida, M. Toda, M. Inoue, and H. Nakada. 2014. Negative regulation of Toll-like receptor-4 signaling through the binding of glycosylphosphatidylinositol-anchored glycoprotein, CD14, with the sialic acid-binding lectin, CD33. J. Biol. Chem. 289: 25341-25350.
31. Chaudhary, A., T. M. Fresquez, and M. J. Naranjo. 2007. Tyrosine kinase Syk associates with Toll-like receptor 4 and regulates signaling in human monocytic cells. Immunol. Cell Biol. 85: 249-256.
32. Kagan, J. C., and R. Medzhitov. 2006. Phosphoinositide-mediated adaptor recruitment controls Toll-like receptor signaling. Cell 125: 943-955.
33. Ling, G. S., J. Bennett, K. J. Woollard, M. Szajna, L. Fossati-Jimack, P. R. Taylor, D. Scott, G. Franzoso, H. T. Cook, and M. Botto. 2014. Integrin CD11b positively regulates TLR4-induced signalling pathways in dendritic cells but not in macrophages. Nat. Commun. 5: 3039.
34. Triantafilou, M., and K. Triantafilou. 2002. Lipopolysaccharide recognition: CD14, TLRs and the LPS-activation cluster. Trends Immunol. 23: 301-304.
35. McMahon, H. T., and E. Boucrot. 2011. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 12: 517-533.
36. Petrovic, N., W. Schacke, J. R. Gahagan, C. A. O'Conor, B. Winnicka, R. E. Conway, P. Mina-Osorio, and L. H. Shapiro. 2007. CD13/APN regulates endothelial invasion and filopodia formation. Blood 110: 142-150.
37. Sarnataro, D., A. Caputo, P. Casanova, C. Puri, S. Paladino, S. S. Tivodar, V. Campana, C. Tacchetti, and C. Zurzolo. 2009. Lipid rafts and clathrin cooperate in the internalization of PrP in epithelial FRT cells. PLoS One 4: e5829.
38. Ares, G. R., and P. A. Ortiz. 2012. Dynamin2, clathrin, and lipid rafts mediate endocytosis of the apical Na/K/2Cl cotransporter NKCC2 in thick ascending limbs. J. Biol. Chem. 287: 37824-37834.
39. Navarrete Santos, A., J. Roentsch, E. M. Danielsen, J. Langner, and D. Riemann. 2000. Aminopeptidase N/CD13 is associated with raft membrane microdomains in monocytes. Biochem. Biophys. Res. Commun. 269: 143-148.
40. Traub, L. M., and J. S. Bonifacino. 2013. Cargo recognition in clathrin-mediated endocytosis. Cold Spring Harb. Perspect. Biol. 5: a016790.
41. Kim, S., S. Y. Kim, J. P. Pribis, M. Lotze, K. P. Mollen, R. Shapiro, P. Loughran, M. J. Scott, and T. R. Billiar. 2013. Signaling of high mobility group box 1 (HMGB1) through Toll-like receptor 4 in macrophages requires CD14. Mol. Med. 19: 88-98.