β2 integrin mediates hantavirus-induced release of neutrophil extracellular traps

Journal of Experimental Medicine

Volumn 211, Issue 7, 2014, Pages 1485-1497

  Raftery, Martin J ^a   Lalwani, Pritesh ^a   Krautkrämer, Ellen ^b   Peters, Thorsten ^c   Scharffetter Kochanek, Karin ^c   Krüger, Renate ^a   Hofmann, Jörg ^a   Seeger, Karl ^a   Krüger, Detlev H ^a   Schönrich, Günther ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c UNIVERSITY HOSPITAL ULM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINO 7 TERT BUTYL 5 (4 CHLOROPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; ANTINUCLEAR ANTIBODY; BETA 2 INTEGRIN RECEPTOR; CD11B ANTIGEN; CD18 ANTIGEN; CELL NUCLEUS ANTIGEN; COMPLEMENT RECEPTOR; COMPLEMENT RECEPTOR 3; COMPLEMENT RECEPTOR 4; GLYCOPROTEIN P 15095; HISTONE; IMMUNOGLOBULIN G ANTIBODY; INTEGRIN RECEPTOR; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; UNCLASSIFIED DRUG;

ADENOVIRUS; ANIMAL EXPERIMENT; ARTICLE; COMPLEMENT ACTIVATION; ENZYME MECHANISM; EPITHELIUM CELL; HANTAVIRUS; HANTAVIRUS INFECTION; HUMAN; IMMUNOPATHOLOGY; IN VITRO STUDY; KIDNEY INJURY; LUNG INJURY; MOUSE; NEUTROPHIL; NEUTROPHIL EXTRACELLULAR TRAP; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYSTEMIC CIRCULATION; VIRUS CELL INTERACTION; VIRUS PARTICLE;

ADENOVIRIDAE; ANIMALS; ANTIGENS, CD18; AUTOANTIBODIES; CHO CELLS; CRICETINAE; CRICETULUS; FEMALE; HANTAVIRUS; HANTAVIRUS INFECTIONS; HUMANS; INTEGRIN ALPHAXBETA2; KIDNEY DISEASES; LUNG DISEASES; MACROPHAGE-1 ANTIGEN; MALE; MICE; MICE, MUTANT STRAINS; NEUTROPHILS;

EID: 84903757114     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20131092     Document Type: Article

References (74)

1. Aga, E., D.M. Katschinski, G. van Zandbergen, H. Laufs, B. Hansen, K. Müller, W. Solbach, and T. Laskay. 2002. Inhibition of the spontaneous apoptosis of neutrophil granulocytes by the intracellular parasite Leishmania major. J. Immunol. 169:898-905. http://dx.doi.org/10.4049/jimmunol.169.2.898
2. Ahrens, I.G., N. Moran, K. Aylward, G. Meade, M. Moser, D. Assefa, D.J. Fitzgerald, C. Bode, and K. Peter. 2006. Evidence for a differential functional regulation of the two β3-integrins άVβ3 and άIIbβ3. Exp. Cell Res. 312:925-937. http://dx.doi.org/10.1016/j.yexcr.2005.11.036
3. Almyroudis, N.G., M.J. Grimm, B.A. Davidson, M. Röhm, C.F. Urban, and B.H. Segal.. 2013. NETosis and NADPH oxidase: at the intersection of host defense, inflammation, and injury. Front Immunol. 4:45 http://dx.doi.org/10.3389/fimmu.2013.00045.
4. Babior, B.M. 1999. NADPH oxidase: an update. Blood. 93:1464-1476.
5. Banchereau, J., and V. Pascual. 2006. Type I interferon in systemic lupus erythematosus and other autoimmune diseases. Immunity. 25:383-392. http://dx.doi.org/10.1016/j.immuni.2006.08.010
6. Borregaard, N. 2010. Neutrophils, from marrow to microbes. Immunity. 33:657-670. http://dx.doi.org/10.1016/j.immuni.2010.11.011
7. Brinkmann, V., U. Reichard, C. Goosmann, B. Fauler, Y. Uhlemann, D.S. Weiss, Y. Weinrauch, and A. Zychlinsky. 2004. Neutrophil extracellular traps kill bacteria. Science. 303:1532-1535. http://dx.doi.org/10.1126/science.1092385
8. Cohen, P.L., and M.A. Maldonado. 2003. Animal models for SLE. Curr. Protoc. Immunol. Chapter 15:Unit 15.20.
9. Darrah, E., and F. Andrade. 2012. NETs: the missing link between cell death and systemic autoimmune diseases? Front Immunol. 3:428.
10. Davis, I.C., A.J. Zajac, K.B. Nolte, J. Botten, B. Hjelle, and S. Matalon. 2002. Elevated generation of reactive oxygen/nitrogen species in hantavirus cardiopulmonary syndrome. J. Virol. 76:8347-8359. http://dx.doi.org/10 .1128/JVI.76.16.8347-8359.2002
11. Diamond, M.S., R. Alon, C.A. Parkos, M.T. Quinn, and T.A. Springer. 1995. Heparin is an adhesive ligand for the leukocyte integrin Mac-1 (CD11b/CD1). J. Cell Biol. 130:1473-1482. http://dx.doi.org/10.1083/jcb.130.6.1473
12. El Kebir, D., and J.G. Filep.. 2013. Modulation of neutrophil apoptosis and the resolution of inflammation through β2 integrins. Front Immunol. 4:60 http://dx.doi.org/10.3389/fimmu.2013.00060.
13. Ermert, D., C.F. Urban, B. Laube, C. Goosmann, A. Zychlinsky, and V. Brinkmann. 2009. Mouse neutrophil extracellular traps in microbial infections. J. Innate Immun. 1:181-193. http://dx.doi.org/10.1159/000205281
14. Fuchs, T.A., U. Abed, C. Goosmann, R. Hurwitz, I. Schulze, V. Wahn, Y. Weinrauch, V. Brinkmann, and A. Zychlinsky. 2007. Novel cell death program leads to neutrophil extracellular traps. J. Cell Biol. 176:231-241. http://dx.doi.org/10.1083/jcb.200606027
15. Garcia-Romo, G.S., S. Caielli, B. Vega, J. Connolly, F. Allantaz, Z. Xu, M. Punaro, J. Baisch, C. Guiducci, R.L. Coffman, et al. 2011. Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Sci. Transl. Med. 3:73ra20.
16. Gavrilovskaya, I.N., M. Shepley, R. Shaw, M.H. Ginsberg, and E.R. Mackow. 1998. β3 Integrins mediate the cellular entry of hantaviruses that cause respiratory failure. Proc. Natl. Acad. Sci. USA. 95:7074-7079. http://dx .doi.org/10.1073/pnas.95.12.7074
17. Gavrilovskaya, I.N., E.J. Brown, M.H. Ginsberg, and E.R. Mackow. 1999. Cellular entry of hantaviruses which cause hemorrhagic fever with renal syndrome is mediated by β3 integrins. J. Virol. 73:3951-3959.
18. Geimonen, E., S. Neff, T. Raymond, S.S. Kocer, I.N. Gavrilovskaya, and E.R. Mackow. 2002. Pathogenic and nonpathogenic hantaviruses differentially regulate endothelial cell responses. Proc. Natl. Acad. Sci. USA. 99:13837-13842. http://dx.doi.org/10.1073/pnas.192298899
19. Gupta, A.K., M.B. Joshi, M. Philippova, P. Erne, P. Hasler, S. Hahn, and T.J. Resink. 2010. Activated endothelial cells induce neutrophil extracellular traps and are susceptible to NETosis-mediated cell death. FEBS Lett. 584:3193-3197. http://dx.doi.org/10.1016/j.febslet.2010.06.006
20. Häcker, H., H. Mischak, T. Miethke, S. Liptay, R. Schmid, T. Sparwasser, K. Heeg, G.B. Lipford, and H. Wagner. 1998. CpG-DNA-specific activation of antigen-presenting cells requires stress kinase activity and is preceded by non-specific endocytosis and endosomal maturation. EMBO J. 17:6230-6240. http://dx.doi.org/10.1093/emboj/17.21.6230
21. Hakkim, A., B.G. Fürnrohr, K. Amann, B. Laube, U.A. Abed, V. Brinkmann, M. Herrmann, R.E. Voll, and A. Zychlinsky. 2010. Impairment of neutrophilextracellular trap degradation is associated with lupus nephritis. Proc. Natl. Acad. Sci. USA. 107:9813-9818. http://dx.doi.org/10.1073/pnas.0909927107
22. Heider, H., B. Ziaja, C. Priemer, A. Lundkvist, J. Neyts, D.H. Krüger, and R. Ulrich. 2001. A chemiluminescence detection method of hantaviral antigens in neutralisation assays and inhibitor studies. J. Virol. Methods. 96:17-23. http://dx.doi.org/10.1016/S0166-0934(01)00314-7
23. Hibbs, M.L., S. Jakes, S.A. Stacker, R.W. Wallace, and T.A. Springer. 1991. The cytoplasmic domain of the integrin lymphocyte function-associated antigen 1 β subunit: sites required for binding to intercellular adhesion molecule 1 and the phorbol ester-stimulated phosphorylation site. J. Exp. Med. 174:1227-1238. http://dx.doi.org/10.1084/jem.174.5.1227
24. Hynes, R.O. 2002. Integrins: bidirectional, allosteric signaling machines. Cell. 110:673-687. http://dx.doi.org/10.1016/S0092-8674(02)00971-6
25. Jenne, C.N., C.H. Wong, F.J. Zemp, B. McDonald, M.M. Rahman, P.A. Forsyth, G. McFadden, and P. Kubes. 2013. Neutrophils recruited to sites of infection protect from virus challenge by releasing neutrophil extracellular traps. Cell Host Microbe. 13:169-180. http://dx.doi.org/10.1016/j.chom.2013.01.005
26. Jonsson, C.B., L.T. Figueiredo, and O. Vapalahti. 2010. A global perspective on hantavirus ecology, epidemiology, and disease. Clin. Microbiol. Rev. 23:412-441. http://dx.doi.org/10.1128/CMR.00062-09
27. Kang, I., T. Quan, H. Nolasco, S.H. Park, M.S. Hong, J. Crouch, E.G. Pamer, J.G. Howe, and J. Craft. 2004. Defective control of latent Epstein-Barr virus infection in systemic lupus erythematosus. J. Immunol. 172:1287-1294. http://dx.doi.org/10.4049/jimmunol.172.2.1287
28. Kessenbrock, K., M. Krumbholz, U. Schönermarck, W. Back, W.L. Gross, Z. Werb, H.J. Gröne, V. Brinkmann, and D.E. Jenne. 2009. Netting neutrophils in autoimmune small-vessel vasculitis. Nat. Med. 15:623-625. http://dx.doi.org/10.1038/nm.1959
29. Khandpur, R., C. Carmona-Rivera, A. Vivekanandan-Giri, A. Gizinski, S. Yalavarthi, J.S. Knight, S. Friday, S. Li, R.M. Patel, V. Subramanian, et al. 2013. NETs are a source of citrullinated autoantigens and stimulate inflammatory responses in rheumatoid arthritis. Sci. Transl. Med. 5:178ra40.
30. Kilpatrick, E.D., M. Terajima, F.T. Koster, M.D. Catalina, J. Cruz, and F.A. Ennis. 2004. Role of specific CD8+ T cells in the severity of a fulminant zoonotic viral hemorrhagic fever, hantavirus pulmonary syndrome. J. Immunol. 172:3297-3304. http://dx.doi.org/10.4049/jimmunol.172.5.3297
31. Krüger, D.H., G. Schönrich, and B. Klempa. 2011. Human pathogenic hantaviruses and prevention of infection. Hum. Vaccin. 7:685-693. http://dx.doi.org/10.4161/hv.7.6.15197
32. Kuijpers, T.W., E. van de Vijver, M.A. Weterman, M. de Boer, A.T. Tool, T.K. van Den Berg, M. Moser, M.E. Jakobs, K. Seeger, O. Sanal, et al. 2009. LAD-1/variant syndrome is caused by mutations in FERMT3. Blood. 113:4740-4746. http://dx.doi.org/10.1182/blood-2008-10-182154
33. Lande, R., D. Ganguly, V. Facchinetti, L. Frasca, C. Conrad, J. Gregorio, S. Meller, G. Chamilos, R. Sebasigari, V. Riccieri, et al.. 2011. Neutrophils activate plasmacytoid dendritic cells by releasing self-DNA-peptide complexes in systemic lupus erythematosus. Sci. Transl. Med. 3:73ra19 http://dx.doi.org/10.1126/scitranslmed.3001180 .
34. Leadbetter, E.A., I.R. Rifkin, A.M. Hohlbaum, B.C. Beaudette, M.J. Shlomchik, and A. Marshak-Rothstein. 2002. Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature. 416:603-607. http://dx.doi.org/10.1038/416603a Lee, M., J.S. Lee, and B.K. Kim. 1983. Disseminated intravascular coagulation in Korean hemorrhagic fever. Bibl. Haematol. (49):181-199.
35. Lee, M., J.S. Lee, and B.K. Kim. 1983. Disseminated intravascular coagulation in Korean hemorrhagic fever. Bibl. Haematol. (49):181-199.
36. Lee, M., B.K. Kim, S. Kim, S. Park, J.S. Han, S.T. Kim, and J.S. Lee.. 1989. Coagulopathy in hemorrhagic fever with renal syndrome (Korean hemorrhagic fever). Rev. Infect. Dis. 11:S877-S883 http://dx.doi.org/10 .1093/clinids/11.Supplement_4.877.
37. Ley, K., C. Laudanna, M.I. Cybulsky, and S. Nourshargh. 2007. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat. Rev. Immunol. 7:678-689. http://dx.doi.org/10.1038/nri2156
38. Lin, A.M., C.J. Rubin, R. Khandpur, J.Y. Wang, M. Riblett, S. Yalavarthi, E.C. Villanueva, P. Shah, M.J. Kaplan, and A.T. Bruce. 2011. Mast cells and neutrophils release IL-17 through extracellular trap formation in psoriasis. J. Immunol. 187:490-500. http://dx.doi.org/10.4049/jimmunol.1100123
39. Linderholm, M., C. Ahlm, B. Settergren, A. Waage, and A. Tärnvik. 1996. Elevated plasma levels of tumor necrosis factor (TNF)-ά, soluble TNF receptors,interleukin (IL)-6, and IL-10 in patients with hemorrhagic fever with renal syndrome. J. Infect. Dis. 173:38-43. http://dx.doi.org/10.1093/infdis/173.1.38
40. Lindgren, T., C. Ahlm, N. Mohamed, M. Evander, H.G. Ljunggren, and N.K. Björkström. 2011. Longitudinal analysis of the human T cell response during acute hantavirus infection. J. Virol. 85:10252-10260. http://dx.doi.org/10.1128/JVI.05548-11
41. Manigold, T., A. Mori, R. Graumann, E. Llop, V. Simon, M. Ferrés, F. Valdivieso, C. Castillo, B. Hjelle, and P. Vial.. 2010. Highly differentiated, resting gnspecific memory CD8+ T cells persist years after infection by andes hantavirus. PLoS Pathog. 6:e1000779 http://dx.doi.org/10.1371/journal. ppat.1000779 .
42. Marsac, D., S. García, A. Fournet, A. Aguirre, K. Pino, M. Ferres, A.M. Kalergis, M. Lopez-Lastra, and F. Veas.. 2011. Infection of human monocyte-derived dendritic cells by ANDES Hantavirus enhances pro-inflammatory state, the secretion of active MMP-9 and indirectly enhances endothelial permeability. Virol. J. 8:223 http://dx.doi.org/10.1186/1743-422X-8-223.
43. Massberg, S., L. Grahl, M.L. von Bruehl, D. Manukyan, S. Pfeiler, C. Goosmann, V. Brinkmann, M. Lorenz, K. Bidzhekov, A.B. Khandagale, et al. 2010. Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases. Nat. Med. 16:887-896. http://dx.doi.org/10 .1038/nm.2184
44. Mayadas, T.N., and X. Cullere. 2005. Neutrophil β2 integrins: moderators of life or death decisions. Trends Immunol. 26:388-395. http://dx.doi.org/10.1016/j.it.2005.05.002
45. Medvedev, A.E., T. Flo, R.R. Ingalls, D.T. Golenbock, G. Teti, S.N. Vogel, and T. Espevik. 1998. Involvement of CD14 and complement receptors CR3 and CR4 in nuclear factor-κB activation and TNF production induced by lipopolysaccharide and group B streptococcal cell walls. J. Immunol. 160:4535-4542.
46. Mustonen, J., H. Helin, K. Pietilä, M. Brummer-Korvenkontio, K. Hedman, A. Vaheri, and A. Pasternack. 1994. Renal biopsy findings and clinicopathologic correlations in nephropathia epidemica. Clin. Nephrol. 41: 121-126.
47. Narasaraju, T., E. Yang, R.P. Samy, H.H. Ng, W.P. Poh, A.A. Liew, M.C. Phoon, N. van Rooijen, and V.T. Chow. 2011. Excessive neutrophils and neutrophil extracellular traps contribute to acute lung injury of influenza pneumonitis. Am. J. Pathol. 179:199-210. http://dx.doi.org/10.1016/j.ajpath.2011.03.013
48. Neeli, I., N. Dwivedi, S. Khan, and M. Radic. 2009. Regulation of extracellular chromatin release from neutrophils. J. Innate Immun. 1:194-201. http://dx.doi.org/10.1159/000206974
49. Outinen, T.K., T. Kuparinen, J. Jylhävä, S. Leppänen, J. Mustonen, S. Mäkelä, I. Pörsti, J. Syrjänen, A. Vaheri, and M. Hurme.. 2012. Plasma cell-free DNA levels are elevated in acute Puumala hantavirus infection. PLoS ONE. 7:e31455 http://dx.doi.org/10.1371/journal.pone.0031455.
50. Paakkala, A., J. Mustonen, M. Viander, H. Huhtala, and A. Pasternack. 2000. Complement activation in nephropathia epidemica caused by Puumala hantavirus. Clin. Nephrol. 53:424-431.
51. Pensiero, M.N., J.B. Sharefkin, C.W. Dieffenbach, and J. Hay. 1992. Hantaan virus infection of human endothelial cells. J. Virol. 66:5929-5936.
52. Raftery, M.J., A.A. Kraus, R. Ulrich, D.H. Krüger, and G. Schönrich. 2002. Hantavirus infection of dendritic cells. J. Virol. 76:10724-10733. http://dx.doi.org/10.1128/JVI.76.21.10724-10733.2002
53. Ramos-Casals, M. 2008. Viruses and lupus: the viral hypothesis. Lupus. 17:163-165. http://dx.doi.org/10.1177/0961203307086268
54. Rasmuson, J., C. Andersson, E. Norrman, M. Haney, M. Evander, and C. Ahlm. 2011. Time to revise the paradigm of hantavirus syndromes? Hantavirus pulmonary syndrome caused by European hantavirus. Eur. J. Clin. Microbiol. Infect. Dis. 30:685-690. http://dx.doi.org/10.1007/s10096-010-1141-6
55. Razanskiene, A., J. Schmidt, A. Geldmacher, A. Ritzi, M. Niedrig, A. Lundkvist, D.H. Krüger, H. Meisel, K. Sasnauskas, and R. Ulrich.. 2004. High yields of stable and highly pure nucleocapsid proteins of different hantaviruses can be generated in the yeast Saccharomyces cerevisiae. J. Biotechnol. 111: 319-333 http://dx.doi.org/10.1016/j.jbiotec.2004.04.010.
56. Rothe, G., and G. Valet. 1990. Flow cytometric analysis of respiratory burst activity in phagocytes with hydroethidine and 2β,7β-dichlorofluorescin. J. Leukoc. Biol. 47:440-448.
57. Saffarzadeh, M., C. Juenemann, M.A. Queisser, G. Lochnit, G. Barreto, S.P. Galuska, J. Lohmeyer, and K.T. Preissner. 2012. Neutrophil extracellulartraps directly induce epithelial and endothelial cell death: a predominant role of histone. PLoS ONE. 7:e32366. http://dx.doi.org/10.1371/journal .pone.0032366 Saitoh, T., J. Komano, Y. Saitoh, T. Misawa, M. Takahama, T. Kozaki, T. Uehata, H. Iwasaki, H. Omori, S. Yamaoka, et al. 2012. Neutrophil extracellular traps mediate a host defense response to human immunodeficiency virus-1. Cell Host Microbe. 12:109-116. http://dx.doi.org/10.1016/j.chom.2012.05.015
58. Saitoh, T., J. Komano, Y. Saitoh, T. Misawa, M. Takahama, T. Kozaki, T. Uehata, H. Iwasaki, H. Omori, S. Yamaoka, et al. 2012. Neutrophil extracellular traps mediate a host defense response to human immunodeficiency virus-1. Cell Host Microbe.7:e32366. http://dx.doi.org/10.1371/journal .pone.0032366
59. Salas, A., M. Sans, A. Soriano, J.C. Reverter, D.C. Anderson, J.M. Piqué, and J. Panés. 2000. Heparin attenuates TNF-ά induced inflammatory response through a CD11b dependent mechanism. Gut. 47:88-96. http://dx.doi.org/10.1136/gut.47.1.88
60. Sangaletti, S., C. Tripodo, C. Chiodoni, C. Guarnotta, B. Cappetti, P. Casalini, S. Piconese, M. Parenza, C. Guiducci, C. Vitali, and M.P. Colombo. 2012. Neutrophil extracellular traps mediate transfer of cytoplasmic neutrophil antigens to myeloid dendritic cells toward ANCA induction and associated autoimmunity. Blood. 120:3007-3018. http://dx.doi.org/10.1182/blood-2012-03-416156
61. Scharffetter-Kochanek, K., H. Lu, K. Norman, N. van Nood, F. Munoz, S. Grabbe, M. McArthur, I. Lorenzo, S. Kaplan, K. Ley, et al. 1998. Spontaneous skin ulceration and defective T cell function in CD18 null mice. J. Exp. Med. 188:119-131. http://dx.doi.org/10.1084/jem.188.1.119
62. Song, J.S., C.H. Min, E. Kang, and S.H. Yu. 1999. Expression of ICAM-1 on the Hantaan virus-infected human umbilical vein endothelial cells. Korean J. Intern. Med. 14:47-54.
63. Stewart, P.L., and G.R. Nemerow. 2007. Cell integrins: commonly used receptors for diverse viral pathogens. Trends Microbiol. 15:500-507. http://dx.doi.org/10.1016/j.tim.2007.10.001
64. Takei, H., A. Araki, H. Watanabe, A. Ichinose, and F. Sendo. 1996. Rapid killing of human neutrophils by the potent activator phorbol 12-myristate 13-acetate (PMA) accompanied by changes different from typical apoptosis or necrosis. J. Leukoc. Biol. 59:229-240.
65. Teichmann, L.L., D. Schenten, R. Medzhitov, M. Kashgarian, and M.J. Shlomchik. 2013. Signals via the adaptor MyD88 in B cells and DCs make distinct and synergistic contributions to immune activation and tissue damage in lupus. Immunity. 38:528-540. http://dx.doi.org/10.1016/j.immuni .2012.11.017
66. Temonen, M., O. Vapalahti, H. Holthöfer, M. Brummer-Korvenkontio, A. Vaheri, and H. Lankinen. 1993. Susceptibility of human cells to Puumala virus infection. J. Gen. Virol. 74:515-518. http://dx.doi.org/10.1099/0022-1317-74-3-515
67. Temonen, M., J. Mustonen, H. Helin, A. Pasternack, A. Vaheri, and H. Holthöfer. 1996. Cytokines, adhesion molecules, and cellular infiltration in nephropathia epidemica kidneys: an immunohistochemical study. Clin. Immunol. Immunopathol. 78:47-55. http://dx.doi.org/10.1006/clin.1996.0007
68. Tillack, K., P. Breiden, R. Martin, and M. Sospedra. 2012. T lymphocyte priming by neutrophil extracellular traps links innate and adaptive immune responses. J. Immunol. 188:3150-3159. http://dx.doi.org/10.4049/jimmunol.1103414
69. Tsokos, G.C. 2011. Systemic lupus erythematosus. N. Engl. J. Med. 365:2110-2121. http://dx.doi.org/10.1056/NEJMra1100359
70. Villanueva, E., S. Yalavarthi, C.C. Berthier, J.B. Hodgin, R. Khandpur, A.M. Lin, C.J. Rubin, W. Zhao, S.H. Olsen, M. Klinker, et al. 2011. Netting neutrophils induce endothelial damage, infiltrate tissues, and expose immunostimulatory molecules in systemic lupus erythematosus. J. Immunol. 187:538-552. http://dx.doi.org/10.4049/jimmunol.1100450
71. Vorup-Jensen, T., C.V. Carman, M. Shimaoka, P. Schuck, J. Svitel, and T.A. Springer. 2005. Exposure of acidic residues as a danger signal for recognition of fibrinogen and other macromolecules by integrin άXβ2. Proc. Natl. Acad. Sci. USA. 102:1614-1619. http://dx.doi.org/10.1073/pnas.0409057102
72. Vorup-Jensen, T., L. Chi, L.C. Gjelstrup, U.B. Jensen, C.A. Jewett, C. Xie, M. Shimaoka, R.J. Linhardt, and T.A. Springer. 2007. Binding between the integrin alphaXbeta2 (CD11c/CD18) and heparin. J. Biol. Chem. 282:30869-30877. http://dx.doi.org/10.1074/jbc.M706114200
73. Wilson, R.W., C.M. Ballantyne, C.W. Smith, C. Montgomery, A. Bradley, W.E. O'Brien, and A.L. Beaudet. 1993. Gene targeting yields a CD18-mutant mouse for study of inflammation. J. Immunol. 151:1571-1578.
74. Yipp, B.G., and P. Kubes. 2013. NETosis: how vital is it? Blood. 122:2784-2794. http://dx.doi.org/10.1182/blood-2013-04-457671