Innate immune collectin surfactant protein D enhances the clearance of DNA by macrophages and minimizes anti-DNA antibody generation

Journal of Immunology

Volumn 174, Issue 11, 2005, Pages 7352-7358

  Palaniyar, Nades ^a,b   Clark, Howard ^a   Nadesalingam, Jeya ^a   Shih, Michael J ^a   Hawgood, Samuel ^c   Reid, Kenneth B M ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIGEN; COLLECTIN; DNA; DNA ANTIBODY; MANNOSE BINDING LECTIN; SURFACTANT PROTEIN A; SURFACTANT PROTEIN D;

ANIMAL CELL; ARTICLE; CELL DEATH; COMPLEMENT ACTIVATION; DNA DETERMINATION; EPITHELIUM CELL; EXTRACELLULAR MATRIX; FLUORESCENCE ACTIVATED CELL SORTING; INNATE IMMUNITY; LUNG ALVEOLUS MACROPHAGE; LUNG LAVAGE; MACROPHAGE ACTIVATION; MONOCYTE; MOUSE; NONHUMAN; PATTERN RECOGNITION; PHAGOCYTOSIS; PINOCYTOSIS; PRIORITY JOURNAL; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION;

EID: 18944389560     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.174.11.7352     Document Type: Article

References (43)

1. Sparwasser, T., T. Miethke, G. Lipford, K. Borschert, H. Hacker, K. Heeg, and H. Wagner. 1997. Bacterial DNA causes septic shock. Nature 386: 336-337.
2. Krieg, A. M., A. K. Yi, S. Matson, T. J. Waldschmidt, G. A. Bishop, R. Teasdale, G. A. Koretzky, and D. M. Klinman. 1995. CpG motifs in bacterial DNA trigger direct B-cell activation. Nature 374: 546-549.
3. Whitchurch, C. B., T. Tolker-Nielsen, P. C. Ragas, and J. S. Mattick. 2002. Extracellular DNA required for bacterial biofilm formation. Science 295: 1487.
4. Savill, J., I. Dransfield, C. Gregory, and C. Haslett. 2002. A blast from the past clearance of apoptotic cells regulates immune responses. Nat. Rev. Immunol. 2: 965-975.
5. Palaniyar, N., J. Nadesalingam, and K. B. Reid. 2002. Pulmonary innate immune proteins and receptors that interact with gram-positive bacterial ligands. Immunobiology 205: 575-594.
6. Hawgood, S., and F. R. Poulain. 2001. The pulmonary collectins and surfactant metabolism. Annu. Rev. Physiol. 63: 495-519.
7. McCormack, F. X., and J. A. Whitsett. 2002. The pulmonary collectins, SP-A and SP-D, orchestrate innate immunity in the lung. J. Clin. Invest. 109: 707-712.
8. Botas, C., F. Poulain, J. Akiyama, C. Brown, L. Allen, J. Goerke, J. Clements, E. Carlson, A. M. Gillespie, C. Epstein, and S. Hawgood. 1998. Altered surfactant homeostasis and alveolar type II cell morphology in mice lacking surfactant protein D. Proc. Natl. Acad. Sci. USA 95: 11869-11874.
9. Korfhagen, T. R., V. Sheftelyevich, M. S. Burhans, M. D. Bruno, G. F. Ross, S. E. Wert, M. T. Stahlman, A. H. Jobe, M. Ikegami, J. A. Whitsett, and J. H. Fisher. 1998. Surfactant protein-D regulates surfactant phospholipid homeostasis in vivo. J. Biol. Chem. 273: 28438-28443.
10. Gardai, S. J., Y. Q. Xiao, M. Dickinson, J. A. Nick, D. R. Voelker, K. E. Greene, and P. M. Henson. 2003. By binding SIRPα or calreticulin/CD91, lung collectins act as dual function surveillance molecules to suppress or enhance inflammation. Cell 115: 13-23.
11. Clark, H., N. Palaniyar, P. Strong, J. Edmondson, S. Hawgood, and K. B. Reid. 2002. Surfactant protein D reduces alveolar macrophage apoptosis in vivo. J. Immunol. 169: 2892-2899.
12. Vandivier, R. W., C. A. Ogden, V. A. Fadok, P. R. Hoffmann, K. K. Brown, M. Botto, M. J. Walport, J. H. Fisher, P. M. Henson, and K. E. Greene. 2002. Role of surfactant proteins A, D, and C1q in the clearance of apoptotic cells in vivo and in vitro: calreticulin and CD91 as a common collectin receptor complex. J. Immunol. 169: 3978-3986.
13. Brown, S., I. Heinisch, E. Ross, K. Shaw, C. D. Buckley, and J. Savill. 2002. Apoptosis disables CD31-mediated cell detachment from phagocytes promoting binding and engulfment. Nature 418: 200-203.
14. Anderson, H. A., C. A. Maylock, J. A. Williams, C. P. Paweletz, H. Shu, and E. Shacter. 2003. Serum-derived protein S binds to phosphatidylserine and stimulates the phagocytosis of apoptotic cells. Nat. Immunol. 4: 87-91.
15. Hanayama, R., M. Tanaka, K. Miwa, A. Shinohara, A. Iwamatsu, and S. Nagata. 2002. Identification of a factor that links apoptotic cells to phagocytes. Nature 417: 182-187.
16. Ezekowitz, R. A. 2002. Local opsonization for apoptosis? Nat. -Immunol. 3: 510-512.
17. Madsen, J., A. Kliem, I. Tornoe, K. Skjodt, C. Koch, and U. Holmskov. 2000. Localization of lung surfactant protein D on mucosal surfaces in human tissues. J. Immunol. 164: 5866-5870.
18. Holmskov, U., S. Thiel, and J. C. Jensenius. 2003. Collectins and ficolins: humoral lectins of the innate immune defense. Annu. Rev. Immunol. 21: 547-578.
19. Hakansson, K., N. K. Lim, H. J. Hoppe, and K. B. Reid. 1999. Crystal structure of the trimeric α-helical coiled-coil and the three lectin domains of human lung surfactant protein D. Structure Fold Des. 7: 255-264.
20. Persson, A., D. Chang, and E. Crouch. 1990. Surfactant protein D is a divalent cation-dependent carbohydrate-binding protein. J. Biol. Chem. 265: 5755-5760.
21. Crouch, E., D. Chang, K. Rust, A. Persson, and J. Heuser. 1994. Recombinant pulmonary surfactant protein D. Post-translational modification and molecular assembly. J. Biol. Chem. 269: 15808-15813.
22. Lu, J., H. Wiedemann, R. Timpl, and K. B. Reid. 1993. Similarity in structure between C1q and the collectins as judged by electron microscopy. Behring. Inst. Mitt. 93: 6-16.
23. Palaniyar, N., R. A. Ridsdale, C. E. Holterman, K. Inchley, F. Possmayer, and G. Harauz. 1998. Structural changes of surfactant protein A induced by cations reorient the protein on lipid bilayers. J. Struct. Biol. 122: 297-310.
24. Palaniyar, N., M. Ikegami, T. Korfhagen, J. Whitsett, and F. X. McCormack. 2001. Domains of surfactant protein A that affect protein oligomerization, lipid structure and surface tension. Comp Biochem. Physiol. A. Mol. Integr. Physiol. 129: 109-127.
25. Nadesalingam, J., A. L. Bernal, A. W. Dodds, A. C. Willis, D. J. Mahoney, A. J. Day, K. B. Reid, and N. Palaniyar. 2003. Identification and characterization of a novel interaction between pulmonary surfactant protein D and decorin. J. Biol. Chem. 278: 25678-25687.
26. Palaniyar, N., J. Nadesalingam, and K. B. Reid. 2003. Innate immune collectins bind nucleic acids and enhance DNA clearance in vitro. Ann. NY Acad. Sci. 1010: 467-470.
27. Palaniyar, N., H. Clark, J. Nadesalingam, S. Hawgood, and K. B. Reid. 2003. Surfactant protein D binds genomic DNA and apoptotic cells, and enhances their clearance, in vivo. Ann. NY Acad. Sci. 1010: 471-475.
28. Palaniyar, N., J. Nadesalingam, H. Clark, M. J. Shih, A. W. Dodds, and K. B. Reid. 2004. Nucleic acid is a novel ligand for innate, immune pattern recognition collectins surfactant proteins A and D and mannose-binding lectin. J. Biol. Chem. 279: 32728-32736.
29. Li, G., J. Siddiqui, M. Hendry, J. Akiyama, J. Edmondson, C. Brown, L. Allen, S. Levitt, F. Poulain, and S. Hawgood. 2002. Surfactant protein-A-deficient mice display an exaggerated early inflammatory response to a β-resistant strain of influenza A virus. Am. J. Respir. Cell Mol. Biol. 26: 277-282.
30. Caponi, L., D. Chimenti, F. Pratesi, and P. Migliorini. 2002. Anti-ribosomal antibodies from lupus patients bind DNA. Clin. Exp. Immunol. 130: 541-547.
31. Gross, J. A., J. Johnston, S. Mudri, R. Enselman, S. R. Dillon, K. Madden, W. Xu, J. Parrish-Novak, D. Foster, C. Lofton-Day, et al. 2000. TACI and BCMA are receptors for a TNF homologue implicated in B-cell autoimmune disease. Nature 404: 995-999.
32. Schagat, T. L., J. A. Wofford, and J. R. Wright. 2001. Surfactant protein A enhances alveolar macrophage phagocytosis of apoptotic neutrophils. J. Immunol. 166: 2727-2733.
33. Ogden, C. A., A. deCathelineau, P. R. Hoffmann, D. Bratton, B. Ghebrehiwet, V. A. Fadok, and P. M. Henson. 2001. C1q and mannose binding lectin engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J. Exp. Med. 194: 781-795.
34. Jiang, H., B. Cooper, F. A. Robey, and H. Gewurz. 1992. DNA binds and activates complement via residues 14-26 of the human C1q A chain. J. Biol. Chem. 267: 25597-25601.
35. Botto, M., C. Dell'Agnola, A. E. Bygrave, E. M. Thompson, H. T. Cook, F. Petry, M. Loos, P. P. Pandolfi, and M. J. Walport. 1998. Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat. Genet. 19: 56-59.
36. Kawane, K., H. Fukuyama, H. Yoshida, H. Nagase, Y. Ohsawa, Y. Uchiyama, K. Okada, T. Iida, and S. Nagata. 2003. Impaired thymic development in mouse embryos deficient in apoptotic DNA degradation. Nat. Immunol. 4: 138-144.
37. Bickerstaff, M. C., M. Botto, W. L. Hutchinson, J. Herbert, G. A. Tennent, A. Bybee, D. A. Mitchell, H. T. Cook, P. J. Butler, M. J. Walport, and M. B. Pepys. 1999. Serum amyloid P component controls chromatin degradation and prevents antinuclear autoimmunity. Nat. Med. 5: 694-697.
38. Peiser, L., S. Mukhopadhyay, and S. Gordon. 2002. Scavenger receptors in innate immunity. Curr. Opin. Immunol. 14: 123-128.
39. Platt, N., H. Suzuki, T. Kodama, and S. Gordon. 2000. Apoptotic thymocyte clearance in scavenger receptor class A-deficient mice is apparently normal. J. Immunol. 164: 4861-4867.
40. Fine, A., Y. Janssen-Heininger, R. P. Soultanakis, S. G. Swisher, and B. D. Uhal. 2000. Apoptosis in lung pathophysiology. Am. J. Physiol. Lung Cell Mol. Physiol. 279: L423-L427.
41. Liacos, C., S. Katsaragakis, M. M. Konstadoulakis, E. G. Messaris, M. Papanicolaou, G. G. Georgiadis, E. Menenakos, A. Vasiliadi-Chioti, and G. Androulakis. 2001. Apoptosis in cells of bronchoalveolar lavage: a cellular reaction in patients who die with sepsis and respiratory failure. Crit. Care Med. 29: 2310-2317.
42. Vignola, A. M., G. Chiappara, R. Gagliardo, M. Gjomarkaj, A. Merendino, L. Siena, J. Bousquet, and G. Bonsignore. 2000. Apoptosis and airway inflammation in asthma. Apoptosis 5: 473-485.
43. Postle, A. D., A. Mander, K. B. Reid, J. Y. Wang, S. M. Wright, M. Moustaki, and J. O. Warner. 1999. Deficient hydrophilic lung surfactant proteins A and D with normal surfactant phospholipid molecular species in cystic fibrosis. Am. J. Respir. Cell Mol. Biol. 20: 90-98.