Reperfusion injury of ischemic skeletal muscle is mediated by natural antibody and complement

doi:10.1084/jem.183.5.2343

This Article

	Full Text (PDF, 2010K)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JEM
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Weiser, M. R.
	Articles by Carroll, M. C.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Weiser, M. R.
	Articles by Carroll, M. C.


Social Bookmarking

	What's this?

ARTICLES

Reperfusion injury of ischemic skeletal muscle is mediated by natural antibody and complement

MR Weiser, JP Williams, FD Moore Jr, L Kobzik, M Ma, HB Hechtman and MC Carroll
Department of Surgery, Harvard Medical School, Boston, Massachusetts 02115, USA.

Reperfusion of ischemic tissue induces an acute inflammatory response that can result in necrosis and irreversible cell injury to both local vascular endothelium and parenchyma. To examine the pathogenesis of ischemia/reperfusion injury, we have used mice deficient in complement components C3, C4, or serum immunoglobulin in a hindlimb model of ischemia. We found that mice homozygous deficient in C3 or C4 were equally protected against reperfusion injury based on a significant reduction in leakage of radiolabeled albumin out of the vasculature. This demonstrates that classical pathway complement is an important factor in the initiation of inflammation following reperfusion. Furthermore, mice deficient in serum immunoglobulin were equally protected and this protection could be reversed by reconstitution with serum from normal mice. Thus, this report describes a novel mechanism for reperfusion injury that involves antibody deposition and activation of complement leading to inflammation permeability.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Dimayuga, P. C., Cesena, F. H. Y., Chyu, K.-Y., Yano, J., Amorn, A., Fishbein, M. C., Shah, P. K., Cercek, B. (2009). Natural antibodies and complement modulate intimal thickening after arterial injury. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297: R1593-R1600 [Abstract] [Full Text]
Busche, M. N., Pavlov, V., Takahashi, K., Stahl, G. L. (2009). Myocardial ischemia and reperfusion injury is dependent on both IgM and mannose-binding lectin. Am. J. Physiol. Heart Circ. Physiol. 297: H1853-H1859 [Abstract] [Full Text]
Frantz, S., Bauersachs, J., Ertl, G. (2009). Post-infarct remodelling: contribution of wound healing and inflammation. Cardiovasc Res 81: 474-481 [Abstract] [Full Text]
Shi, T., Moulton, V. R., Lapchak, P. H., Deng, G.-M., Dalle Lucca, J. J., Tsokos, G. C. (2009). Ischemia-mediated aggregation of the actin cytoskeleton is one of the major initial events resulting in ischemia-reperfusion injury. Am. J. Physiol. Gastrointest. Liver Physiol. 296: G339-G347 [Abstract] [Full Text]
Markiewski, M. M., Lambris, J. D. (2007). The Role of Complement in Inflammatory Diseases From Behind the Scenes into the Spotlight. Am. J. Pathol. 171: 715-727 [Abstract] [Full Text]
Suber, F., Carroll, M. C., Moore, F. D. Jr. (2007). Innate response to self-antigen significantly exacerbates burn wound depth. Proc. Natl. Acad. Sci. USA 104: 3973-3977 [Abstract] [Full Text]
Beenhouwer, D. O., Yoo, E. M., Lai, C.-W., Rocha, M. A., Morrison, S. L. (2007). Human Immunoglobulin G2 (IgG2) and IgG4, but Not IgG1 or IgG3, Protect Mice against Cryptococcus neoformans Infection. Infect. Immun. 75: 1424-1435 [Abstract] [Full Text]
Chan, R. K., Ibrahim, S. I., Takahashi, K., Kwon, E., McCormack, M., Ezekowitz, A., Carroll, M. C., Moore, F. D. Jr., Austen, W. G. Jr. (2006). The Differing Roles of the Classical and Mannose-Binding Lectin Complement Pathways in the Events following Skeletal Muscle Ischemia-Reperfusion. J. Immunol. 177: 8080-8085 [Abstract] [Full Text]
Zhang, M., Takahashi, K., Alicot, E. M., Vorup-Jensen, T., Kessler, B., Thiel, S., Jensenius, J. C., Ezekowitz, R. A. B., Moore, F. D., Carroll, M. C. (2006). Activation of the Lectin Pathway by Natural IgM in a Model of Ischemia/Reperfusion Injury. J. Immunol. 177: 4727-4734 [Abstract] [Full Text]
Dudley, R. W. R., Khairallah, M., Mohammed, S., Lands, L., Des Rosiers, C., Petrof, B. J. (2006). Dynamic responses of the glutathione system to acute oxidative stress in dystrophic mouse (mdx) muscles. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291: R704-R710 [Abstract] [Full Text]
McGrath, F. D. G., Brouwer, M. C., Arlaud, G. J., Daha, M. R., Hack, C. E., Roos, A. (2006). Evidence That Complement Protein C1q Interacts with C-Reactive Protein through Its Globular Head Region.. J. Immunol. 176: 2950-2957 [Abstract] [Full Text]
Day, Y.-J., Huang, L., Ye, H., Li, L., Linden, J., Okusa, M. D. (2006). Renal Ischemia-Reperfusion Injury and Adenosine 2A Receptor-Mediated Tissue Protection: The Role of CD4+ T Cells and IFN-{gamma}.. J. Immunol. 176: 3108-3114 [Abstract] [Full Text]
Zhang, M., Alicot, E. M., Chiu, I., Li, J., Verna, N., Vorup-Jensen, T., Kessler, B., Shimaoka, M., Chan, R., Friend, D., Mahmood, U., Weissleder, R., Moore, F. D., Carroll, M. C. (2006). Identification of the target self-antigens in reperfusion injury. JEM 203: 141-152 [Abstract] [Full Text]
Cramer, D. E., Allendorf, D. J., Baran, J. T., Hansen, R., Marroquin, J., Li, B., Ratajczak, J., Ratajczak, M. Z., Yan, J. (2006). {beta}-Glucan enhances complement-mediated hematopoietic recovery after bone marrow injury. Blood 107: 835-840 [Abstract] [Full Text]
Abonia, J. P., Friend, D. S., Austen, W. G. Jr., Moore, F. D. Jr., Carroll, M. C., Chan, R., Afnan, J., Humbles, A., Gerard, C., Knight, P., Kanaoka, Y., Yasuda, S., Morokawa, N., Austen, K. F., Stevens, R. L., Gurish, M. F. (2005). Mast Cell Protease 5 Mediates Ischemia-Reperfusion Injury of Mouse Skeletal Muscle. J. Immunol. 174: 7285-7291 [Abstract] [Full Text]
Krijnen, P A J, Ciurana, C, Cramer, T, Hazes, T, Meijer, C J L M, Visser, C A, Niessen, H W M, Hack, C E (2005). IgM colocalises with complement and C reactive protein in infarcted human myocardium. J. Clin. Pathol. 58: 382-388 [Abstract] [Full Text]
Casadevall, A., Pirofski, L.-a. (2004). New Concepts in Antibody-Mediated Immunity. Infect. Immun. 72: 6191-6196 [Full Text]
Fleming, S. D., Monestier, M., Tsokos, G. C. (2004). Accelerated Ischemia/Reperfusion-Induced Injury in Autoimmunity-Prone Mice. J. Immunol. 173: 4230-4235 [Abstract] [Full Text]
Zhang, M., Austen, W. G. Jr., Chiu, I., Alicot, E. M., Hung, R., Ma, M., Verna, N., Xu, M., Hechtman, H. B., Moore, F. D. Jr., Carroll, M. C. (2004). Identification of a specific self-reactive IgM antibody that initiates intestinal ischemia/reperfusion injury. Proc. Natl. Acad. Sci. USA 101: 3886-3891 [Abstract] [Full Text]
Yamada, K., Miwa, T., Liu, J., Nangaku, M., Song, W.-C. (2004). Critical Protection from Renal Ischemia Reperfusion Injury by CD55 and CD59. J. Immunol. 172: 3869-3875 [Abstract] [Full Text]
Ratajczak, J., Reca, R., Kucia, M., Majka, M., Allendorf, D. J., Baran, J. T., Janowska-Wieczorek, A., Wetsel, R. A., Ross, G. D., Ratajczak, M. Z. (2004). Mobilization studies in mice deficient in either C3 or C3a receptor (C3aR) reveal a novel role for complement in retention of hematopoietic stem/progenitor cells in bone marrow. Blood 103: 2071-2078 [Abstract] [Full Text]
Saadi, S., Takahashi, T., Holzknecht, R. A., Platt, J. L. (2004). Pathways to Acute Humoral Rejection. Am. J. Pathol. 164: 1073-1080 [Abstract] [Full Text]
Nguyen, H. X, Tidball, J. G (2003). Null mutation of gp91phox reduces muscle membrane lysis during muscle inflammation in mice. J. Physiol. 553: 833-841 [Abstract] [Full Text]
Quigg, R. J. (2003). Complement and the Kidney. J. Immunol. 171: 3319-3324 [Full Text]
Burne-Taney, M. J., Ascon, D. B., Daniels, F., Racusen, L., Baldwin, W., Rabb, H. (2003). B Cell Deficiency Confers Protection from Renal Ischemia Reperfusion Injury. J. Immunol. 171: 3210-3215 [Abstract] [Full Text]
Fiane, A. E., Videm, V., Lingaas, P. S., Heggelund, L., Nielsen, E. W., Geiran, O. R., Fung, M., Mollnes, T. E. (2003). Mechanism of Complement Activation and Its Role in the Inflammatory Response After Thoracoabdominal Aortic Aneurysm Repair. Circulation 108: 849-856 [Abstract] [Full Text]
Riedemann, N. C., Ward, P. A. (2003). Complement in Ischemia Reperfusion Injury. Am. J. Pathol. 162: 363-367 [Full Text]
Stahl, G. L., Xu, Y., Hao, L., Miller, M., Buras, J. A., Fung, M., Zhao, H. (2003). Role for the Alternative Complement Pathway in Ischemia/Reperfusion Injury. Am. J. Pathol. 162: 449-455 [Abstract] [Full Text]
Thurman, J. M., Ljubanovic, D., Edelstein, C. L., Gilkeson, G. S., Holers, V. M. (2003). Lack of a Functional Alternative Complement Pathway Ameliorates Ischemic Acute Renal Failure in Mice. J. Immunol. 170: 1517-1523 [Abstract] [Full Text]
Reid, R. R., Woodcock, S., Shimabukuro-Vornhagen, A., Austen, W. G. Jr., Kobzik, L., Zhang, M., Hechtman, H. B., Moore, F. D. Jr., Carroll, M. C. (2002). Functional Activity of Natural Antibody is Altered in Cr2-Deficient Mice. J. Immunol. 169: 5433-5440 [Abstract] [Full Text]
Fleming, S. D., Shea-Donohue, T., Guthridge, J. M., Kulik, L., Waldschmidt, T. J., Gipson, M. G., Tsokos, G. C., Holers, V. M. (2002). Mice Deficient in Complement Receptors 1 and 2 Lack a Tissue Injury-Inducing Subset of the Natural Antibody Repertoire. J. Immunol. 169: 2126-2133 [Abstract] [Full Text]
SAADI, S., WRENSHALL, L. E., PLATT, J. L. (2002). Regional manifestations and control of the immune system. FASEB J. 16: 849-856 [Abstract] [Full Text]
Dimayuga, P., Cercek, B., Oguchi, S., Fredrikson, G. N., Yano, J., Shah, P. K., Jovinge, S., Nilsson, J. (2002). Inhibitory Effect on Arterial Injury-Induced Neointimal Formation by Adoptive B-Cell Transfer in Rag-1 Knockout Mice. Arterioscler. Thromb. Vasc. Bio. 22: 644-649 [Abstract] [Full Text]
Buerke, M., Schwertz, H., Seitz, W., Meyer, J., Darius, H. (2001). Novel Small Molecule Inhibitor of C1s Exerts Cardioprotective Effects in Ischemia-Reperfusion Injury in Rabbits. J. Immunol. 167: 5375-5380 [Abstract] [Full Text]
Kyriakides, C., Wang, Y., Austen, W. G. Jr., Favuzza, J., Kobzik, L., Moore, F. D. Jr., Hechtman, H. B. (2001). Moderation of skeletal muscle reperfusion injury by a sLex-glycosylated complement inhibitory protein. Am. J. Physiol. Cell Physiol. 281: C224-C230 [Abstract] [Full Text]
PARK, P., HAAS, M., CUNNINGHAM, P. N., ALEXANDER, J. J., BAO, L., GUTHRIDGE, J. M., KRAUS, D. M., HOLERS, V. M., QUIGG, R. J. (2001). Inhibiting the Complement System Does Not Reduce Injury in Renal Ischemia Reperfusion. J. Am. Soc. Nephrol. 12: 1383-1390 [Abstract] [Full Text]
Younger, J. G., Sasaki, N., Waite, M. D., Murray, H. N., Saleh, E. F., Ravage, Z. A., Hirschl, R. B., Ward, P. A., Till, G. O. (2001). Detrimental effects of complement activation in hemorrhagic shock. J. Appl. Physiol. 90: 441-446 [Abstract] [Full Text]
Brock, R. W., Nie, R. G., Harris, K. A., Potter, R. F. (2001). Kupffer cell-initiated remote hepatic injury following bilateral hindlimb ischemia is complement dependent. Am. J. Physiol. Gastrointest. Liver Physiol. 280: G279-G284 [Abstract] [Full Text]
SCHILLER, B., CUNNINGHAM, P. N., ALEXANDER, J. J., BAO, L., HOLERS, V. M., QUIGG, R. J. (2001). Expression of a Soluble Complement Inhibitor Protects Transgenic Mice from Antibody-Induced Acute Renal Failure. J. Am. Soc. Nephrol. 12: 71-79 [Abstract] [Full Text]
Sahu, A., Soulika, A. M., Morikis, D., Spruce, L., Moore, W. T., Lambris, J. D. (2000). Binding Kinetics, Structure-Activity Relationship, and Biotransformation of the Complement Inhibitor Compstatin. J. Immunol. 165: 2491-2499 [Abstract] [Full Text]
Kyriakides, C., Woodcock, S. A., Wang, Y., Favuzza, J., Austen, W. G. Jr., Kobzik, L., Moore, F. D. Jr., Valeri, R. C., Shepro, D., Hechtman, H. B. (2000). Soluble P-selectin moderates complement-dependent reperfusion injury of ischemic skeletal muscle. Am. J. Physiol. Cell Physiol. 279: C520-C528 [Abstract] [Full Text]
Frenette, J., Cai, B., Tidball, J. G. (2000). Complement Activation Promotes Muscle Inflammation during Modified Muscle Use. Am. J. Pathol. 156: 2103-2110 [Abstract] [Full Text]
Collard, C. D., Vakeva, A., Morrissey, M. A., Agah, A., Rollins, S. A., Reenstra, W. R., Buras, J. A., Meri, S., Stahl, G. L. (2000). Complement Activation after Oxidative Stress : Role of the Lectin Complement Pathway. Am. J. Pathol. 156: 1549-1556 [Abstract] [Full Text]
Caliezi, C., Wuillemin, W. A., Zeerleder, S., Redondo, M., Eisele, B., Hack, C. E. (2000). C1-Esterase Inhibitor: An Anti-Inflammatory Agent and Its Potential Use in the Treatment of Diseases Other Than Hereditary Angioedema. Pharmacol. Rev. 52: 91-112 [Abstract] [Full Text]
Kyriakides, C., Austen, W. Jr., Wang, Y., Favuzza, J., Kobzik, L., Moore, F. D. Jr., Hechtman, H. B. (1999). Skeletal muscle reperfusion injury is mediated by neutrophils and the complement membrane attack complex. Am. J. Physiol. Cell Physiol. 277: C1263-C1268 [Abstract] [Full Text]
Prohaszka, Z., Duba, J., Lakos, G., Kiss, E., Varga, L., Janoskuti, L., Csaszar, A., Karadi, I., Nagy, K., Singh, M., Romics, L., Fust, G. (1999). Antibodies against human heat-shock protein (hsp) 60 and mycobacterial hsp65 differ in their antigen specificity and complement-activating ability. Int Immunol 11: 1363-1370 [Abstract] [Full Text]
Heller, T., Hennecke, M., Baumann, U., Gessner, J. E., Meyer zu Vilsendorf, A., Baensch, M., Boulay, F., Kola, A., Klos, A., Bautsch, W., Kohl, J. (1999). Selection of a C5a Receptor Antagonist from Phage Libraries Attenuating the Inflammatory Response in Immune Complex Disease and Ischemia/Reperfusion Injury. J. Immunol. 163: 985-994 [Abstract] [Full Text]
Rittershaus, C. W., Thomas, L. J., Miller, D. P., Picard, M. D., Geoghegan-Barek, K. M., Scesney, S. M., Henry, L. D., Sen, A. C., Bertino, A. M., Hannig, G., Adari, H., Mealey, R. A., Gosselin, M. L., Couto, M., Hayman, E. G., Levin, J. L., Reinhold, V. N., Marsh, H. C. Jr. (1999). Recombinant Glycoproteins That Inhibit Complement Activation and Also Bind the Selectin Adhesion Molecules. J. Biol. Chem. 274: 11237-11244 [Abstract] [Full Text]
Williams, J. P., Pechet, T. T.�V., Weiser, M. R., Reid, R., Kobzik, L., Moore, F. D. Jr., Carroll, M. C., Hechtman, H. B. (1999). Intestinal reperfusion injury is mediated by IgM and complement. J. Appl. Physiol. 86: 938-942 [Abstract] [Full Text]
Collard, C. D., Bukusoglu, C., Agah, A., Colgan, S. P., Reenstra, W. R., Morgan, B. P., Stahl, G. L. (1999). Hypoxia-induced expression of complement receptor type 1�(CR1, CD35) in human vascular endothelial cells. Am. J. Physiol. Cell Physiol. 276: C450-C458 [Abstract] [Full Text]
Schmiedt, W., Kinscherf, R., Deigner, H.-P., Kamencic, H., Nauen, O., Kilo, J., Oelert, H., Metz, J., Bhakdi, S. (1998). Complement C6 Deficiency Protects Against Diet-Induced Atherosclerosis in Rabbits. Arterioscler. Thromb. Vasc. Bio. 18: 1790-1795 [Abstract] [Full Text]
Makrides, S. C. (1998). Therapeutic Inhibition of the Complement System. Pharmacol. Rev. 50: 59-88 [Abstract] [Full Text]
Collard, C. D., Vakeva, A., Bukusoglu, C., Zund, G., Sperati, C. J., Colgan, S. P., Stahl, G. L. (1997). Reoxygenation of Hypoxic Human Umbilical Vein Endothelial Cells Activates the Classic Complement Pathway. Circulation 96: 326-333 [Abstract] [Full Text]
Park, P., Haas, M., Cunningham, P. N., Bao, L., Alexander, J. J., Quigg, R. J. (2002). Injury in renal ischemia-reperfusion is independent from immunoglobulins and T lymphocytes. Am. J. Physiol. Renal Physiol. 282: F352-F357 [Abstract] [Full Text]
Dimayuga, P., Cercek, B., Oguchi, S., Fredrikson, G. N., Yano, J., Shah, P. K., Jovinge, S., Nilsson, J. (2002). Inhibitory Effect on Arterial Injury-Induced Neointimal Formation by Adoptive B-Cell Transfer in Rag-1 Knockout Mice. Arterioscler. Thromb. Vasc. Bio. 22: 644-649 [Abstract] [Full Text]