Membrane attack complex contributes to destruction of vascular integrity in acute lung allograft rejection

Journal of Immunology

Volumn 169, Issue 8, 2002, Pages 4620-4627

  Nakashima, Shinji ^a   Qian, Zhiping ^a   Rahimi, Salma ^a   Wasowska, Barbara A ^a   Baldwin III, William M ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C3D; COMPLEMENT COMPONENT C5; COMPLEMENT COMPONENT C5A; COMPLEMENT COMPONENT C5B; COMPLEMENT COMPONENT C6; COMPLEMENT COMPONENT C7; COMPLEMENT COMPONENT C8; COMPLEMENT COMPONENT C9; COMPLEMENT MEMBRANE ATTACK COMPLEX; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MESSENGER RNA; PROTEIN; VON WILLEBRAND FACTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; GRAFT REJECTION; HUMORAL IMMUNITY; LUNG EDEMA; LUNG HEMORRHAGE; LUNG TRANSPLANTATION; LYMPHOCYTIC INFILTRATION; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; RESPIRATORY DISTRESS SYNDROME;

EID: 0037108593     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.169.8.4620     Document Type: Article

References (65)

1. Baldwin, W. M., III, S. K. Pruitt, R. B. Brauer, M. R. Daha, and F. Sanfilippo. 1995. Complement in organ transplantation: contribution to inflammation, injury and rejection. Transplantation 59:797.
2. Baldwin, W. M., III, M. Samaniego-Picota, E. K. Kasper, A. Clark, M. Czader, C. Rohde, A. A. Zachary, F. Sanfilippo, and H. Hruban. 1999. Complement deposition in early cardiac transplant biopsies is associated with ischemic injury and subsequent rejection episodes. Transplantation 68:894.
3. Baldwin, W. M., III, Z. Qian, H. Ota, M. Samaniego, B. Wasowska, F. Sanfilippo, and R. H. Hruban. 2000. Complement as a mediator of vascular inflammation and activation in allografts. J. Heart Lung Transplant. 19:723.
4. Baldwin, W. M., III, C. P. Larsen, and R. L. Fairchild. 2001. Innate immune responses to transplants: a significant variable with cadaver donors. Immunity 14:369.
5. Brauer, R. B., W. M. Baldwin III, S. Ibrahim, and F. Sanfilippo. 1995. The contribution of terminal complement components to acute and hyperacute allograft rejection in the rat. Transplantation 59:288.
6. Qian, Z., F. M. Jakobs, T. Pfaff-Amesse, F. Sanfilippo, and W. M. Baldwin III. 1998. Complement contributes to the rejection of complete and class I MHC incompatible cardiac allografts. J. Heart Lung Transplant. 17:470.
7. Qian, Z., B. A. Wasowska, E. Behrens, J. R. Brody, S. S. Kadkol, D. L. Cangello, L. Horwitz, J. Liu, C. Lowenstein, A. D. Hess, et al. 1999. C6 produced by macrophages contributes to cardiac allograft rejection. Am. J. Pathol. 155:1293.
8. Feucht, H. E., E. Felber, M. J. Gokel, G. Hillebrand, U. Nattermann, C. Brockmeyer, E. Held, G. Riethmuller, W. Land, and E. Albert. 1991. Vascular deposition of complement-split products in kidney allografts with cell-mediated rejection. Clin. Exp. Immunol. 86:464.
9. Feucht, H. E., H. Schneeberger, G. Hillebrand, K. Burkhardt, M. Weiss, G. Riethmuller, W. Land, and E. Albert. 1993. Capillary deposition of C4d complement fragment and early renal graft loss. Kidney Int. 43:1333.
10. Bechtel, U., R. Scheuer, R. Landgraf, A. Konig, and H. E. Feucht. 1994. Assessment of soluble adhesion molecules (sICAM-1, sVCAM-1, sELAM-1) and complement cleavage products (sC4d, sC5b-9) in urine. Transplantation 58:905.
11. Feucht, H. E., and G. Opelz. 1996. The humoral immune response towards HLA class II determinants in renal transplantation. Kidney Int. 50:1464.
12. Lederer, S. R., H. Schneeberger, E. Albert, J. P. Johnson, R. Gruber, W. Land, K. Burkhardt, G. Hillebrand, and H. E. Feucht. 1996. Early renal graft dysfunction: the role of preformed antibodies to DR-typed lymphoblastoid cell lines. Transplantation 61:313.
13. Behr, T. M., H. E. Feucht, K. Richter, C. Reiter, C. H. Spes, D. Pongratz, P. Uberfuhr, B. Meiser, K. Theisen, and C. E. Angermann. 1999. Detection of humoral rejection in human cardiac allografts by assessing the capillary deposition of complement fragment C4d in endomyocardial biopsies. J. Heart Lung Transplant. 18:904.
14. Collins, A. B., E. E. Schneeberger, M. A. Pascual, S. L. Saidman, W. W. Williams, N. Tolkoff-Rubin, A. B. Cosimi, and R. B. Colvin. 1999. Complement activation in acute humoral renal allograft rejection: diagnostic significance of C4d deposits in peritubular capillaries. J. Am. Soc. Nephrol. 10:2208.
15. Montgomery, R. A., A. A. Zachary, L. C. Racusen, M. S. Leffell, K. E. King, J. F. Burdick, W. R. Maley, and L. E. Ratner. 2000. Plasmapheresis and intravenous immune globulin provides effective rescue therapy for refractory humoral rejection and allows kidneys to be successfully transplanted into cross-match-positive recipients. Transplantation 70:887.
16. Crespo, M., M. Pascual, N. Tolkoff-Rubin, S. Mauiyyedi, A. B. Collins, D. Fitzpatrick, M. L. Farrell, W. W. Williams, F. L. Delmonico, A. B. Cosimi, et al. 2001. Acute humoral rejection in renal allograft recipients. I. Incidence, serology and clinical characteristics. Transplantation 71:652.
17. Herzenberg, A. M., J. S. Gill, O. Djurdjev, and A. B. Magil. 2002. C4d deposition in acute rejection: an independent long-term prognostic factor. J. Am. Soc. Nephrol. 13:234.
18. Lederer, S. R., B. Kluth-Pepper, H. Schneeberger, E. Albert, W. Land, and H. E. Feucht. 2001. Impact of humoral alloreactivity early after transplantation on the long-term survival of renal allografts. Kidney Int. 59:334.
19. Mauiyyedi, S., P. D. Pelle, S. Saidman, A. B. Collins, M. Pascual, N. E. Tolkoff-Rubin, W. W. Williams, A. A. Cosimi, E. E. Schneeberger, and R. B. Colvin. 2001. Chronic humoral rejection: identification of antibody-mediated chronic renal allograft rejection by C4d deposits in peritubular capillaries. J. Am. Soc. Nephrol. 12:574.
20. Qian, Z., W. Hu, J. Liu, F. Sanfilippo, R. H. Hruban, and W. M. Baldwin III. 2001. Accelerated graft arteriosclerosis in cardiac transplants: complement activation promotes progression of lesions from medium to large arteries. Transplantation 72:900.
21. Theruvath, T. P., S. L. Saidman, S. Mauiyyedi, F. L. Delmonico, W. W. Williams, N. Tolkoff-Rubin, A. B. Collins, R. B. Colvin, A. B. Cosimi, and M. Pascual. 2001. Control of antidonor antibody production with tacrolimus and mycophenolate mofetil in renal allograft recipients with chronic rejection. Transplantation 72:77.
22. Baldwin, W. M., III, N. A. Flavahan, and R. L. Fairchild. 2002. Integration of complement and leukocytes in response to allotransplantation. Curr. Opin. Transplant. 7:92.
23. Mulligan, M. S., E. Schmid, B. Beck-Schimmer, G. O. Till, H. P. Friedl, R. B. Brauer, T. E. Hugli, M. Miyasaka, R. L. Warner, K. J. Johnson, et al. 1996. Requirement and role of C5a in acute lung inflammatory injury in rats. J. Clin. Invest. 98:503.
24. Mulligan, M. S., E. Schmid, G. O. Till, T. E. Hugli, H. P. Friedl, R. A. Roth, and P. A. Ward. 1997. C5a-dependent up-regulation in vivo of lung vascular P-selectin. J. Immunol. 158:1857.
25. Czermak, B. J., A. B. Lentsch, N. M. Bless, H. Schmal, H. P. Friedl, and P. A. Ward. 1999. Synergistic enhancement of chemokine generation and lung injury by C5a or the membrane attack complex of complement. Am. J. Pathol. 154:1513.
26. Riedemann, N. C., R. F. Guo, V. J. Sarma, I. J. Laudes, M. Huber-Lang, R. L. Warner, E. A. Albrecht, C. L. Speyer, and P. A. Ward. 2002. Expression and function of the C5a receptor in rat alveolar epithelial cells. J. Immunol. 168:1919.
27. Czermak, B. J., V. Sarma, N. M. Bless, H. Schmal, H. P. Friedl, and P. A. Ward. 1999. In vitro and in vivo dependency of chemokine generation on C5a and TNF-α. J. Immunol. 162:2321.
28. Foreman, K. E., A. A. Vaporciyan, B. K. Bonish, M. L. Jones, K. J. Johnson, M. M. Glovsky, S. M. Eddy, and P. A. Ward. 1994. C5a-induced expression of P-selectin in endothelial cells. J. Clin. Invest. 94:1147.
29. Hattori, R., K. K. Hamilton, R. P. McEver, and P. J. Sims. 1989. Complement proteins C5b-C9 induce secretion of high molecular weight multimers of endothelial von Willebrand factor and translocation of granule membrane protein GMP-140 to the cell surface. J. Biol. Chem. 264:9053.
30. Kilgore, K. S., J. P. Shen, B. F. Miller, P. A. Ward, and J. S. Warren. 1995. Enhancement by the complement membrane attack complex of tumor necrosis factor-α-induced endothelial cell expression of E-selectin and ICAM-1. J. Immunol. 155:1434.
31. Tedesco, F., M. Pausa, E. Nardon, M. Introna, A. Mantovani, and A. Dobrina. 1997. The cytolytically inactive terminal complement complex activates endothelial cells to express adhesion molecules and tissue factor procoagulant activity. J. Exp. Med. 185:1619.
32. Merten, S., J. C. Chen, H. Ha, K. Plain, R. A. Boyd, M. J. Penny, P. Leenaerts, and B. M. Hall. 1998. The cellular basis of cardiac allograft rejection. VIII. Mechanisms underlying delayed allograft rejection in PVG C6-deficient rats. Transplantation 65:1152.
33. Sundaresan, S., T. Mohanakumar, M. A. Smith, E. P. Trulock, J. Lynch, D. Phelan, J. D. Cooper, and G. A. Patterson. 1998. HLA-A locus mismatches and development of antibodies to HLA after lung transplantation correlate with the development of bronchiolitis obliterans syndrome. Transplantation 65:648.
34. Jaramillo, A., M. A. Smith, D. Phelan, S. Sundaresan, E. P. Trulock, J. P. Lynch, J. D. Cooper, G. A. Patterson, and T. Mohanakumar. 1999. Development of ELISA-detected anti-HLA antibodies precedes the development of bronchiolitis obliterans syndrome and correlates with progressive decline in pulmonary function after lung transplantation. Transplantation 67:1155.
35. Prop, J., P. Nieuwenhuis, and C. R. Wildevuur. 1985. Lung allograft rejection in the rat. I. Accelerated rejection caused by graft lymphocytes. Transplantation 40:25.
36. Prop, J., C. R. Wildevuur, and P. Nieuwenhuis. 1985. Lung allograft rejection in the rat. II. Specific immunological properties of lung grafts. Transplantation 40:126.
37. Prop, J., C. R. Wildevuur, and P. Nieuwenhuis. 1985. Lung allograft rejection in the rat. III. Corresponding morphological rejection phases in various rat strain combinations. Transplantation 40:132.
38. Brauer, R. B., W. M. Baldwin III, D. Wang, L. R. Horwitz, A. D. Hess, A. S. Klein, and F. Sanfilippo. 1994. Hepatic and extrahepatic biosynthesis of complement factor C6 in the rat. J. Immunol. 153:3168.
39. Marck, K. W., J. Prop, C. R. Wildevuur, and P. Nieuwenhuis. 1985. Lung transplantation in the rat: histopathology of left lung iso- and allografts. J. Heart Transplant. 4:263.
40. Reis, A., A. Giaid, C. Serrick, and H. Shennib. 1995. Improved outcome of rat lung transplantation with modification of the nonsuture external cuff technique. J. Heart Lung Transplant. 14:274.
41. Yousem, S. A., G. J. Berry, P. T. Cagle, D. Chamberlain, A. N. Husain, R. H. Hruban, A. Marchevsky, N. P. Ohori, J. Ritter, S. Stewart, et al. 1996. Revision of the 1990 working formulation for the classification of pulmonary allograft rejection: Lung Rejection Study Group. J. Heart Lung Transplant. 15:1.
42. Damoiseaux, J. G., E. A. Dopp, W. Calame, D. Chao, G. G. MacPherson, and C. D. Dijkstra. 1994. Rat macrophage lysosomal membrane antigen recognized by monoclonal antibody ED1. Immunology. 83:140.
43. Wray, D. W., W. M. Baldwin III, and F. Sanfilippo. 1992. IgM and IgG alloantibody responses to MHC class I and II following rat renal allograft rejection: effects of transplantectomy and posttransplantation blood transfusions. Transplantation 53:167.
44. Wray, D. W., W. M. Baldwin III, and F. Sanfilippo. 1993. Different patterns of sensitization following renal allograft rejection in an inbred rat strain combination. Transplantation 55:1132.
45. Strunk, R. C., D. M. Eidlen, and R. J. Mason. 1988. Pulmonary alveolar type II epithelial cells synthesize and secrete proteins of the classical and alternative complement pathways. J. Clin. Invest. 81:1419.
46. Rothman, B. L., A. W. Despins, and D. L. Kreutzer. 1990. Cytokine regulation of C3 and C5 production by the human type II pneumocyte cell line, A549. J. Immunol. 145:592.
47. Varsano, S., M. Kaminsky, M. Kaiser, and L. Rashkovsky. 2000. Generation of complement C3 and expression of cell membrane complement inhibitory proteins by human bronchial epithelium cell line. Thorax 55:364.
48. Brooimans, R. A., A. P. Stegmann, W. T. van Dorp, A. A. van der Ark, F. J. van der Woude, L. van Es, and M. R. Daha. 1991. Interleukin 2 mediates stimulation of complement C3 biosynthesis in human proximal tubular epithelial cells. J. Clin. Invest. 88:379.
49. Takada, M., K. C. Nadeau, G. D. Shaw, K. A. Marquette, and N. L. Tilney. 1997. The cytokine-adhesion molecule cascade in ischemia/reperfusion injury of the rat kidney: inhibition by a soluble P-selectin ligand. J. Clin. Invest. 99:2682.
50. Pratt, J. R., K. Abe, M. Miyazaki, W. Zhou, and S. H. Sacks. 2000. In situ localization of C3 synthesis in experimental acute renal allograft rejection. Am. J. Pathol. 157:825.
51. Yasojima, K., C. Schwab, E. G. McGeer, and P. L. McGeer. 2001. Generation of C-reactive protein and complement components in atherosclerotic plaques. Am. J. Pathol. 158:1039.
52. Brauer, R. B., W. M. Baldwin III, M. R. Daha, S. K. Pruitt, and F. Sanfilippo. 1993. The use of C6-deficient rats to evaluate the mechanism of hyperacute rejection of discordant cardiac xenografts. J. Immunol. 151:7240.
53. Mead, R. J., S. K. Singhrao, J. W. Neal, H. Lassmann, and B. P. Morgan. 2002. The membrane attack complex of complement causes severe demyelination associated with acute axonal injury. J. Immunol. 168:458.
54. Brauer, R. B., W. M. Baldwin III, D. Wang, S. K. Pruitt, A. S. Klein, and F. Sanfilippo. 1996. Functional activity of anti-C6 antibodies elicited in C6 deficient rats reconstituted by liver allografts: ability to inhibit hyperacute rejection of discordant cardiac xenografts. Transplantation 61:588.
55. Leenaerts, P. L., R. K. Stad, B. M. Hall, B. J. Van Damme, Y. Vanrenterghem, and M. R. Daha. 1994. Hereditary C6 deficiency in a strain of PVG/c rats. Clin. Exp. Immunol. 97:478.
56. Fitch, J. C., S. Rollins, L. Matis, B. Alford, S. Aranki, C. D. Collard, M. Dewar, J. Elefteriades, R. Hines, G. Kopf, et al. 1999. Pharmacology and biological efficacy of a recombinant, humanized, single-chain antibody C5 complement inhibitor in patients undergoing coronary artery bypass graft surgery with cardiopulmonary bypass. Circulation 100:2499.
57. Haviland, D. L., R. L. McCoy, W. T. Whitehead, H. Akama, E. P. Molmenti, A. Brown, J. C. Haviland, W. C. Parks, D. H. Perlmutter, and R. A. Wetsel. 1995. Cellular expression of the C5a anaphylatoxin receptor (C5aR): demonstration of C5aR on nonmyeloid cells of the liver and lung. J. Immunol. 154:1861.
58. Drouin, S. M., J. Kildsgaard, J. Haviland, J. Zabner, H. P. Jia, P. B. McCray, Jr., B. F. Tack, and R. A. Wetsel. 2001. Expression of the complement anaphylatoxin C3a and C5a receptors on bronchial epithelial and smooth muscle cells in models of sepsis and asthma. J. Immunol. 166:2025.
59. Hopken, U. E., B. Lu, N. P. Gerard, and C. Gerard. 1997. Impaired inflammatory responses in the reverse arthus reaction through genetic deletion of the C5a receptor. J. Exp. Med. 186:749.
60. Ruggeri, Z. M. 1997. von Willebrand factor. J. Clin. Invest. 99:559.
61. Couser, W. G., J. W. Pippin, and S. J. Shankland. 2001. Complement (C5b-9) induces DNA synthesis in rat mesangial cells in vitro. Kidney Int. 59:905.
62. Niculescu, F., T. Badea, and H. Rus. 1999. Sublytic C5b-9 induces proliferation of human aortic smooth muscle cells: role of mitogen activated protein kinase and phosphatidylinositol 3-kinase. Atherosclerosis 142:47.
63. Niculescu, F., and H. Rus. 2001. Mechanisms of signal transduction activated by sublytic assembly of terminal complement complexes on nucleated cells. Immunol. Res. 24:191.
64. Pratt, J. R., S. A. Basheer, and S. H. Sacks. 2002. Local synthesis of complement component C3 regulates acute renal transplant rejection. Nat. Med. 8:582.
65. Berry, G. J., E. M. Brunt, D. Chamberlain, R. H. Hruban, R. K. Sibley, S. Stewart, and H. D. Tazelaar. 1990. A working formulation for the standardization of nomenclature in the diagnosis of heart and lung rejection: Lung Rejection Study Group: The International Society for Heart Transplantation. J. Heart Transplant. 9:593.