CD93/AA4.1: A novel regulator of inflammation in murine focal cerebral ischemia

Journal of Immunology

Volumn 184, Issue 11, 2010, Pages 6407-6417

  Harhausen, Denise ^a   Prinz, Vincent ^a   Ziegler, Gina ^b   Gertz, Karen ^a   Endres, Matthias ^a   Lehrach, Hans ^b   Gasque, Philippe ^c   Botto, Marina ^d   Stahel, Philip F ^e   Dirnagl, Ulrich ^a   Nietfeld, Wilfried ^b   Trendelenburg, George ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^c UNIVERSITÉ DE LA RÉUNION   (France)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD93 PROTEIN; CELL MARKER; COMPLEMENT COMPONENT C1Q; MESSENGER RNA; SECONDARY LYMPHOID TISSUE CHEMOKINE; UNCLASSIFIED DRUG; COMPLEMENT 1Q RECEPTOR; COMPLEMENT RECEPTOR; MEMBRANE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN; BRAIN DAMAGE; BRAIN EDEMA; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CELL INFILTRATION; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; GENE DELETION; GENETIC TRANSCRIPTION; IMMUNOHISTOCHEMISTRY; IMMUNOREGULATION; LEUKOCYTE; MACROPHAGE; MALE; MICROGLIA; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NEUROPROTECTION; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; REPERFUSION; SIGNAL TRANSDUCTION; UPREGULATION; WILD TYPE; ANIMAL; BIOSYNTHESIS; DNA MICROARRAY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETICS; IMMUNOLOGY; INFLAMMATION; METABOLISM; MOUSE MUTANT; PATHOLOGY; REPERFUSION INJURY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; BRAIN ISCHEMIA; CHEMOKINE CCL21; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RECEPTORS, COMPLEMENT; REPERFUSION INJURY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 77953369343     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0902342     Document Type: Article

References (58)

1. Hossmann, K. A. 2006. Pathophysiology and therapy of experimental stroke. Cell. Mol. Neurobiol. 26: 1055-1081.
2. Dirnagl, U., C. Iadecola, andM. A. Moskowitz. 1999. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci. 22: 391-397.
3. Trendelenburg, G., andU. Dirnagl. 2005. Neuroprotective role of astrocytes in cerebral ischemia: focus on ischemic preconditioning. Glia 50: 307-320.
4. Gasque, P. 2004. Complement: a unique innate immune sensor for danger signals. Mol. Immunol. 41: 1089-1098.
5. de Haas, A. H., H. R. J. van Weering, E. K. de Jong, H. W. G. M. Boddeke, andK. P. H. Biber. 2007. Neuronal chemokines: versatile messengers in central nervous system cell interaction. Mol. Neurobiol. 36: 137-151.
6. Trendelenburg, G. 2008. Acute neurodegeneration and the inflammasome: central processor for danger signals and the inflammatory response? J. Cereb. Blood Flow Metab. 28: 867-881.
7. Biber, K., A. Sauter, N. Brouwer, S. C. Copray, andH. W. Boddeke. 2001. Ischemia-induced neuronal expression of the microglia attracting chemokine Secondary Lymphoid-tissue Chemokine (SLC). Glia 34: 121-133.
8. Lo, J. C., R. K. Chin, Y. Lee, H. S. Kang, Y. Wang, J. V. Weinstock, T. Banks, C. F. Ware, G. Franzoso, andY. X. Fu. 2003. Differential regulation of CCL21 in lymphoid/nonlymphoid tissues for effectively attracting T cells to peripheral tissues. J. Clin. Invest. 112: 1495-1505.
9. Förster, R., A. C. Davalos-Misslitz, andA. Rot. 2008. CCR7 and its ligands: balancing immunity and tolerance. Nat. Rev. Immunol. 8: 362-371.
10. Lu, A., Y. Tang, R. Ran, J. F. Clark, B. J. Aronow, andF. R. Sharp. 2003. Genomics of the periinfarction cortex after focal cerebral ischemia. J. Cereb. Blood Flow Metab. 23: 786-810.
11. MacManus, J. P., T. Graber, C. Luebbert, E. Preston, I. Rasquinha, B. Smith, andJ. Webster. 2004. Translation-state analysis of gene expression in mouse brain after focal ischemia. J. Cereb. Blood Flow Metab. 24: 657-667.
12. Meller, R., S. L. Stevens, M. Minami, J. A. Cameron, S. King, H. Rosenzweig, K. Doyle, N. S. Lessov, R. P. Simon, andM. P. Stenzel-Poore. 2005. Neuroprotection by osteopontin in stroke. J. Cereb. Blood Flow Metab. 25: 217-225.
13. Stenzel-Poore, M. P., S. L. Stevens, Z. Xiong, N. S. Lessov, C. A. Harrington, M. Mori, R. Meller, H. L. Rosenzweig, E. Tobar, T. E. Shaw, et al. 2003. Effect of ischaemic preconditioning on genomic response to cerebral ischaemia: similarity to neuroprotective strategies in hibernation and hypoxia-tolerant states. Lancet 362: 1028-1037.
14. Trendelenburg, G., K. Prass, J. Priller, K. Kapinya, A. Polley, C. Muselmann, K. Ruscher, U. Kannbley, A. O. Schmitt, S. Castell, et al. 2002. Serial analysis of gene expression identifies metallothionein-II as major neuroprotective gene in mouse focal cerebral ischemia. J. Neurosci. 22: 5879-5888.
15. Ziegler, G., D. Harhausen, C. Schepers, O. Hoffmann, C. Röhr, V. Prinz, J. König, H. Lehrach, W. Nietfeld, andG. Trendelenburg. 2007. TLR2 has a detrimental role in mouse transient focal cerebral ischemia. Biochem. Biophys. Res. Commun. 359: 574-579.
16. Kanehisa, M., S. Goto, M. Hattori, K. F. Aoki-Kinoshita, M. Itoh, S. Kawashima, T. Katayama, M. Araki, andM. Hirakawa. 2006. From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res. 34(Database issue): D354-D357.
17. Huang, R., A. Wallqvist, andD. G. Covell. 2006. Comprehensive analysis of pathway or functionally related gene expression in the National Cancer Institute's anticancer screen. Genomics 87: 315-328.
18. Norsworthy, P. J., L. Fossati-Jimack, J. Cortes-Hernandez, P. R. Taylor, A. E. Bygrave, R. D. Thompson, S. Nourshargh, M. J. Walport, andM. Botto. 2004. Murine CD93 (C1qRp) contributes to the removal of apoptotic cells invivo but is not required for C1q-mediated enhancement of phagocytosis. J. Immunol. 172: 3406-3414.
19. Løvik, G., J. T. Vaage, E. Dissen, C. Szpirer, J. C. Ryan, andB. Rolstad. 2000. Characterization and molecular cloning of rat C1qRp, a receptor on NK cells. Eur. J. Immunol. 30: 3355-3362.
20. Nepomuceno, R. R., A. H. Henschen-Edman, W. H. Burgess, andA. J. Tenner. 1997. cDNA cloning and primary structure analysis of C1qR(P), the human C1q/MBL/SPA receptor that mediates enhanced phagocytosis in vitro. Immunity 6: 119-129.
21. Kishore, U., andK. B. M. Reid. 2000. C1q: structure, function, and receptors. Immunopharmacology 49: 159-170.
22. McGreal, E. P., N. Ikewaki, H. Akatsu, B. P. Morgan, andP. Gasque. 2002. Human C1qRp is identical with CD93 and the mNI-11 antigen but does not bind C1q. J. Immunol. 168: 5222-5232.
23. Danet, G. H., J. L. Luongo, G. Butler, M. M. Lu, A. J. Tenner, M. C. Simon, andD. A. Bonnet. 2002. C1qRp defines a new human stem cell population with hematopoietic and hepatic potential. Proc. Natl. Acad. Sci. USA 99: 10441-10445.
24. Goolsby, J., M. C. Marty, D. Heletz, J. Chiappelli, G. Tashko, D. Yarnell, P. S. Fishman, S. Dhib-Jalbut, C. T. Bever, Jr., B. Pessac, andD. Trisler. 2003. Hematopoietic progenitors express neural genes. Proc. Natl. Acad. Sci. USA 100: 14926-14931.
25. Jack, R. M., B. A. Lowenstein, andA. Nicholson-Weller. 1994. Regulation of C1q receptor expression on human polymorphonuclear leukocytes. J. Immunol. 153: 262-269.
26. Bohlson, S. S., R. Silva, M. I. Fonseca, andA. J. Tenner. 2005. CD93 is rapidly shed from the surface of human myeloid cells and the soluble form is detected in human plasma. J. Immunol. 175: 1239-1247.
27. Fonseca, M. I., P. M. Carpenter, M. Park, G. Palmarini, E. L. Nelson, andA. J. Tenner. 2001. C1qR(P), a myeloid cell receptor in blood, is predominantly expressed on endothelial cells in human tissue. J. Leukoc. Biol. 70: 793-800.
28. Nepomuceno, R. R., andA. J. Tenner. 1998. C1qRP, the C1q receptor that enhances phagocytosis, is detected specifically in human cells of myeloid lineage, endothelial cells, and platelets. J. Immunol. 160: 1929-1935.
29. Petrenko, O., A. Beavis, M. Klaine, R. Kittappa, I. Godin, andI. R. Lemischka. 1999. The molecular characterization of the fetal stem cell marker AA4. Immunity 10: 691-700.
30. Jordan, C. T., C. M. Astle, J. Zawadzki, K. Mackarehtschian, I. R. Lemischka, andD. E. Harrison. 1995. Long-term repopulating abilities of enriched fetal liver stem cells measured by competitive repopulation. Exp. Hematol. 23: 1011-1015.
31. Dean, Y. D., E. P. McGreal, andP. Gasque. 2001. Endothelial cells, megakaryoblasts, platelets and alveolar epithelial cells express abundant levels of the mouse AA4 antigen, a C-type lectin-like receptor involved in homing activities and innate immune host defense. Eur. J. Immunol. 31: 1370-1381.
32. Hara, H., P. L. Huang, N. Panahian, M. C. Fishman, andM. A. Moskowitz. 1996. Reduced brain edema and infarction volume in mice lacking the neuronal isoform of nitric oxide synthase after transient MCA occlusion. J. Cereb. Blood Flow Metab. 16: 605-611.
33. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
34. Lin, T. N., Y. Y. He, G. Wu, M. Khan, andC. Y. Hsu. 1993. Effect of brain edema on infarct volume in a focal cerebral ischemia model in rats. Stroke 24: 117-121.
35. Zhang, M., S. S. Bohlson, M. Dy, andA. J. Tenner. 2005. Modulated interaction of the ERM protein, moesin, with CD93. Immunology 115: 63-73.
36. Dean, Y. D., E. P. McGreal, H. Akatsu, andP. Gasque. 2000. Molecular and cellular properties of the rat AA4 antigen, a C-type lectin-like receptor with structural homology to thrombomodulin. J. Biol. Chem. 275: 34382-34392.
37. Katchanov, J., C. Waeber, K. Gertz, A. Gietz, B. Winter, W. Brück, U. Dirnagl, R. W. Veh, andM. Endres. 2003. Selective neuronal vulnerability following mild focal brain ischemia in the mouse. Brain Pathol. 13: 452-464.
38. Endres, M., A. Meisel, D. Biniszkiewicz, S. Namura, K. Prass, K. Ruscher, A. Lipski, R. Jaenisch, M. A. Moskowitz, andU. Dirnagl. 2000. DNA methyltransferase contributes to delayed ischemic brain injury. J. Neurosci. 20: 3175-3181.
39. Bekiaris, V., F. Gaspal, M. Y. Kim, D. R. Withers, F. M. McConnell, G. Anderson, andP. J. Lane. 2009. CD30 is required for CCL21 expression and CD4 T cell recruitment in the absence of lymphotoxin signals. J. Immunol. 182: 4771-4775.
40. van der Net, J. B., D. M. Oosterveer, J. Versmissen, J. C. Defesche, M. Yazdanpanah, B. E. Aouizerat, E. W. Steyerberg, M. J. Malloy, C. R. Pullinger, J. J. Kastelein, et al. 2008. Replication study of 10 genetic polymorphisms associated with coronary heart disease in a specific high-risk population with familial hypercholesterolemia. Eur. Heart J. 29: 2195-2201.
41. Brady, J., J. Neal, N. Sadakar, andP. Gasque. 2004. Human endosialin (tumor endothelial marker 1) is abundantly expressed in highly malignant and invasive brain tumors. J. Neuropathol. Exp. Neurol. 63: 1274-1283.
42. Sumanas, S., T. Jorniak, andS. Lin. 2005. Identification of novel vascular endothelial-specific genes by the microarray analysis of the zebrafish cloche mutants. Blood 106: 534-541.
43. Marchler-Bauer, A., J. B. Anderson, M. K. Derbyshire, C. DeWeese-Scott, N. R. Gonzales, M. Gwadz, L. Hao, S. He, D. I. Hurwitz, J. D. Jackson, et al. 2007. CDD: a conserved domain database for interactive domain family analysis. Nucleic Acids Res. 35(Database issue): D237-D240.
44. Bohlson, S. S., M. Zhang, C. E. Ortiz, andA. J. Tenner. 2005. CD93 interacts with the PDZ domain-containing adaptor protein GIPC: implications in the modulation of phagocytosis. J. Leukoc. Biol. 77: 80-89.
45. Cole, J. W., S. C. Roberts, M. Gallagher, W. H. Giles, B. D. Mitchell, K. K. Steinberg, M. A. Wozniak, R. F. Macko, L. J. Reinhart, andS. J. Kittner; Stroke Prevention in Young Women Study. 2004. Thrombomodulin Ala455Val Polymorphism and the risk of cerebral infarction in a biracial population: the Stroke Prevention in Young Women Study. BMC Neurol. 4: 21.
46. Weiler, H. 2004. Mouse models of thrombosis: thrombomodulin. Thromb. Haemost. 92: 467-477.
47. Park, M., andA. J. Tenner. 2003. Cell surface expression of C1qRP/CD93 is stabilized by O-glycosylation. J. Cell. Physiol. 196: 512-522.
48. Ikewaki, N., J. K. Kulski, andH. Inoko. 2006. Regulation of CD93 cell surface expression by protein kinase C isoenzymes. Microbiol. Immunol. 50: 93-103.
49. Woltman, A. M., N. Schlagwein, S. W. van der Kooij, and C. van Kooten. 2004. The novel cyclophilin-binding drug sanglifehrin A specifically affects antigen uptake receptor expression and endocytic capacity of human dendritic cells. J. Immunol. 172: 6482-6489.
50. Chevrier, S., C. Genton, A. Kallies, A. Karnowski, L. A. Otten, B. Malissen, M. Malissen, M. Botto, L. M. Corcoran, S. L. Nutt, andH. Acha-Orbea. 2009. CD93 is required for maintenance of antibody secretion and persistence of plasma cells in the bone marrow niche. Proc. Natl. Acad. Sci. USA 106: 3895-3900.
51. Babcock, A. A., W. A. Kuziel, S. Rivest, andT. Owens. 2003. Chemokine expression by glial cells directs leukocytes to sites of axonal injury in the CNS. J. Neurosci. 23: 7922-7930.
52. de Jong, E. K., I. M. Dijkstra, M. Hensens, N. Brouwer, M. van Amerongen, R. S. Liem, H. W. Boddeke, andK. Biber. 2005. Vesicle-mediated transport and release of CCL21 in endangered neurons: a possible explanation for microglia activation remote from a primary lesion. J. Neurosci. 25: 7548-7557.
53. Kivisäkk, P., D. J. Mahad, M. K. Callahan, C. Trebst, B. Tucky, T. Wei, L. Wu, E. S. Baekkevold, H. Lassmann, S. M. Staugaitis, et al. 2003. Human cerebrospinal fluid central memory CD4+ T cells: evidence for trafficking through choroid plexus and meninges via P-selectin. Proc. Natl. Acad. Sci. USA 100: 8389-8394.
54. Rappert, A., K. Biber, C. Nolte, M. Lipp, A. Schubel, B. Lu, N. P. Gerard, C. Gerard, H. W. Boddeke, andH. Kettenmann. 2002. Secondary lymphoid tissue chemokine (CCL21) activates CXCR3 to trigger a Cl- current and chemotaxis in murine microglia. J. Immunol. 168: 3221-3226.
55. Chen, S. C., M. W. Leach, Y. Chen, X. Y. Cai, L. Sullivan, M. Wiekowski, B. J. Dovey-Hartman, A. Zlotnik, andS. A. Lira. 2002. Central nervous system inflammation and neurological disease in transgenic mice expressing the CC chemokine CCL21 in oligodendrocytes. J. Immunol. 168: 1009-1017.
56. Utans-Schneitz, U., H. Lorez, W. E. Klinkert, J. da Silva, andW. Lesslauer. 1998. A novel rat CC chemokine, identified by targeted differential display, is upregulated in brain inflammation. J. Neuroimmunol. 92: 179-190.
57. Rappert, A., I. Bechmann, T. Pivneva, J. Mahlo, K. Biber, C. Nolte, A. D. Kovac, C. Gerard, H. W. Boddeke, R. Nitsch, andH. Kettenmann. 2004. CXCR3-dependent microglial recruitment is essential for dendrite loss after brain lesion. J. Neurosci. 24: 8500-8509.
58. Tang, S. C., T. V. Arumugam, X. Xu, A. Cheng, M. R. Mughal, D. G. Jo, J. D. Lathia, D. A. Siler, S. Chigurupati, X. Ouyang, et al. 2007. Pivotal role for neuronal Toll-like receptors in ischemic brain injury and functional deficits. Proc. Natl. Acad. Sci. USA 104: 13798-13803.