Abstracts
Mannose binding lectin is a lectin instrumental in the innate immunity. It recognizes carbohydrate patterns found on the surface of a large number of pathogenic micro-organisms, activating the complement system. However, this protein seems to increase the tissue damage after ischemia. In this paper is reviewed some aspects of harmful role of the mannose binding lectin in ischemia/reperfusion injury.
Ischemia; Mannose binding lectin; Complement
Lectina de ligação à manose é uma lectina instrumental na imunidade inata. Ela reconhece padrões de hidratos de carbono encontrados na superfície de um grande número de microrganismos patogênicos, que ativam o sistema complemento. No entanto, esta proteína parece aumentar o dano tecidual após isquemia. Neste trabalho são revisados alguns aspectos do papel nocivo da lectina de ligação à manose na lesão de isquemia/reperfusão.
Isquemia; Lectina de ligação à manose; Complemento
INTRODUCTION
A terosclerosis is one of the leading causes of death in modern society66. Davies MJ, Woolf N, Rowles PM, Pepper J. Morphology of the endothelium over atherosclerotic plaques in human coronary arteries. Br. Heart J. 1988; 60:459-64.. This disease has required a big effort from all medical community not only in preventive measurements but also in the development of new drugs for treatment and procedures of revascularization in order to avoid the ischemic complications.
Aterosclerosis is a disease condition that begins with focal thickening of the intima with accumulation of lipid-laden macrophages (or foam cells). Smooth muscle cells populate the intima and lipids accumulate both intracellularly and extracellularly, producing the fatty streak that is the nidus of an atherosclerotic plaque66. Davies MJ, Woolf N, Rowles PM, Pepper J. Morphology of the endothelium over atherosclerotic plaques in human coronary arteries. Br. Heart J. 1988; 60:459-64.. There is a local chronic inflammatory response promoted by high level of oxidized low-density lipoprotein that attracts a large amount of macrophages and T lymphocytes66. Davies MJ, Woolf N, Rowles PM, Pepper J. Morphology of the endothelium over atherosclerotic plaques in human coronary arteries. Br. Heart J. 1988; 60:459-64.,3636. Williams KJ, Tabas I. The response-to-retention hypothesis of early atherogenesis. Arterioscler Thromb Vasc Biol. 1995; 15:551-61.. Soft plaques may suddenly rupture causing the development of a thrombus and incidentally leading to death of the tissues (infarction)44. Borissoff JI, Heeneman S, Kilinç E, Kassák P, Van Oerle R, Winckers K, et al. Early atherosclerosis exhibits an enhanced procoagulant state. Circulation. 2010 ; 122: 821-30.. As a player in the inflammatory response, the complement system is thought to be involved in this process of inflammation2525. Rugonfalvi-Kiss S, Dósa E, Madsen HO, Endrész V, Prohászka Z, Laki J, et al. High rate of early restenosis after carotid eversion endarterectomy in homozygous carriers of the normal mannose-binding lectin genotype. Stroke. 2005; 36: 944-8.. Indeed, complement activation products have been demonstrated in atherosclerotic plaques2525. Rugonfalvi-Kiss S, Dósa E, Madsen HO, Endrész V, Prohászka Z, Laki J, et al. High rate of early restenosis after carotid eversion endarterectomy in homozygous carriers of the normal mannose-binding lectin genotype. Stroke. 2005; 36: 944-8..
Stents and angioplasties may be used to reduce the incidence of clinical events. Coronary stenting, for example, has become a widely accepted technique2727. Serruys PW, de Jaegere P, Kiemeneij F, Macaya C, Rutsch W, Heyndrickx G, et al. A comparison of balloon-expandable-stent implantation with balloon angioplasty in patients with coronary artery disease. Benestent Study Group. N Engl J Med. 1994; 331: 489-95.. In spite of some relevant strong points favoring its use such as greater success rate and the repeatability of the procedure, several major drawbacks still persist, including restenosis within the treated vessel 11. Akiyama T, Moussa I, Reimers B, Ferraro M, Kobayashi Y, Blengino S,et al. Angiographic and clinical outcome following coronary stenting of small vessels: a comparison with coronary stenting of large vessels. J Am Coll Cardiol. 1998; 32:1610-8.,1010. Elezi S, Kastrati A, Neumann FJ, Hadamitzky M, Dirschinger J, Schömig A.Vessel size and long-term outcome after coronary stent placement. Circulation. 1998; 98: 1875-80.,1919. Kasaoka S, Tobis JM, Akiyama T, Reimers B, Di Mario C, Wong ND, et al. Angiographic and intravascular ultrasound predictors of in-stent restenosis. J Am Coll Cardiol. 1998 15; 32: 1630.,2020. Kastrati A, Schömig A, Elezi S, Schühlen H, Wilhelm M, Dirschinger J. Interlesion dependence of the risk for restenosis in patients with coronary stent placement in in multiple lesions. Circulation. 1998; 97: 2396-401.,2828. Serruys PW, Umans V, Heyndrickx GR, van den Brand M, de Feyter PJ, Wijns W, et al. Elective PTCA of totally occluded coronary arteries not associated with acute myocardial infarction; short-term and long-term results. Eur Heart J. 1985; 6: 2-12.. The restenosis phenomenon is currently the object of intensive research in different areas of biomedical field and therapy. Restenosis means the reoccurrence of stenosis and it can be defined as a reduction in the circumference of the arterial lumen of 50% or more, with the majority of patients needing further angioplasty within six months99. Denes L, Entz L, Jancsik V. Restenosis and therapy. Int J Vasc Med. 2012; 2012:406236.,2828. Serruys PW, Umans V, Heyndrickx GR, van den Brand M, de Feyter PJ, Wijns W, et al. Elective PTCA of totally occluded coronary arteries not associated with acute myocardial infarction; short-term and long-term results. Eur Heart J. 1985; 6: 2-12.. It is due mainly to neointima formation, which is caused primarily by smooth muscular cells proliferation and migration1212. Farb A, Weber DK, Kolodgie FD, Burke AP, Virmani R. Morphological predictors of restenosis after coronary stenting in humans. Circulation. 2002; 105: 2974-80.. The formation of some neointima is necessary for vessel healing after stenting but excessive neointima formation narrows its lumen and has deleterious effect3333. Uchida Y, Uchida Y, Matsuyama A, Koga A, Kanai M, Sakurai T. Formation of web- and membrane-like structures on the edges of bare-metal coronary stents. Circ. J. 2010 ;74:1830-6.. Contributing factors for restenosis are local ischemia/reperfusion, alterations of shear stress of blood stream, levels of C reactive protein and homocysteine, and immune factors, among others99. Denes L, Entz L, Jancsik V. Restenosis and therapy. Int J Vasc Med. 2012; 2012:406236.. It is a destructive event occurring as postoperative complications after angioplasty, bypass operations, or stenting. Despite the fact that restenosis differ in pathogenesis of atherosclerosis, complement system seems, again, to play an active role in the process99. Denes L, Entz L, Jancsik V. Restenosis and therapy. Int J Vasc Med. 2012; 2012:406236..
This review was focused on the role of mannose binding lectin, a component of complement pathway from the immune innate system, in the injury of ischemic/reperfusion syndrome and in restenosis after medical procedures.
MANNOSE BINDING LECTIN: DEFINITION, STRUCTURE AND BIOLOGICAL FUNCTIONS
The human complement system is comprised of three different pathways: the classical, alternative, and the more recently described lectin complement pathway3030. Thiel S, Vorup-Jensen T, Stover CM, Schwaeble W, Laursen SB, Poulsen K, et al. A second serine protease associated with mannan binding lectin that activates complement. Nature. 1997; 386: 506-510.,3131. Turner MW. Mannose-binding lectin: the pluripotent molecule of the innate immune system. Immunol. Today. 1996; 17:532-40.. The lectin complement pathway is an antibody-independent cascade that is normally initiated by binding of mannose-binding lectin (MBL) to cell surface carbohydrates of foreign bacteria, protozoa, or parasites3232. Turner MW. The lectin pathway of complement activation. Res. Immunol. 1996; 147:110-5.. After binding, MBL activates the complement system, via MBL-associated serine proteases (MASPs), initiating the complement activation3131. Turner MW. Mannose-binding lectin: the pluripotent molecule of the innate immune system. Immunol. Today. 1996; 17:532-40.. So, MBL exerts an important role in the innate immune system.
In Figure 1, it is possible to overview the components of complement system and to locate the lectin complement pathway pathway. The activation of final pathway of complement causes the formation of the of membrane attack complex that is responsible for the destructive power of this system. Although it is intend to destroy microorganisms, the membrane attack complex may be deleterious to host cells (Figure 1).
MBL is synthesized in the liver, circulates in the serum and in inflammatory conditions can leave the circulation due to vascular leakage and be detected in the mucosal surface1414. Garred P. Mannose-binding lectin genetics: from A to Z. Biochem Soc Trans. 2008 ;36 (Pt 6):1461-6..
Serum values of MBL may vary broadly from person to person due to the fact that the serum levels are determinate by genetic polymorphisms of the MBL2 gene, on chromosome 10 which has a high prevalence of mutations 99. Denes L, Entz L, Jancsik V. Restenosis and therapy. Int J Vasc Med. 2012; 2012:406236.,1414. Garred P. Mannose-binding lectin genetics: from A to Z. Biochem Soc Trans. 2008 ;36 (Pt 6):1461-6.,3232. Turner MW. The lectin pathway of complement activation. Res. Immunol. 1996; 147:110-5.. High levels of MBL offer defense against invading bacteria but may be deleterious provoking local and systemic inflammation through complement activation, exacerbating inflammatory diseases, and increasing the damage resulting from ischemia and reperfusion1212. Farb A, Weber DK, Kolodgie FD, Burke AP, Virmani R. Morphological predictors of restenosis after coronary stenting in humans. Circulation. 2002; 105: 2974-80.. From the evolutionary point of view, the high prevalence of mutations in the MBL gene suggests that low levels of MBL may be beneficial in some circumstances1212. Farb A, Weber DK, Kolodgie FD, Burke AP, Virmani R. Morphological predictors of restenosis after coronary stenting in humans. Circulation. 2002; 105: 2974-80..
THE ROLE OF MBL IN ISCHEMIA AND ISCHEMIA-REPERFUSION
Several studies have implicated high MBL levels in unsuccessful outcomes in ischemic events and in clinical situations with ischemia reperfusion.
Walsh et al3535. Walsh MC, Bourcier T, Takahashi K, Shi L, Busche MN, Rother RP,et al. Mannose-binding lectin is a regulator of inflammation that accompanies myocardial ischemia and reperfusion injury. J Immunol. 2005; 175: 541-6. have done some experimental studies in mice (both wild type and Knot out for MBL) with cardiac ischemia generated by left anterior descending branch coronary artery ligation, that was loosened after 30 min. They showed that the ejection fraction of left ventricle, measured by echocardiography of wild type mice was significantly decreased. If the animal was genetically modified to be MBL null (MBL KO), the loss of left ventricular function was attenuated. Injecting MBL to MBL KO mice, higher dysfunction was again observed; if the MBL was injected together with antibodies against MBL, the dysfunction tissue injury was diminished. This experiment shows nicely the role of MBL in the ischemic/reperfusion tissue injury in cardiac tissues and raises some therapeutic possibilities.
Gastrointestinal ischemia-reperfusion generally stems from interruption of blood flow within the superior mesenteric artery or vein and leads to small intestinal hypoperfusion and a mortality rate of 70%2929. Tendler D A. Acute intestinal ischemia and infarction. Semin. Gastrointest. Dis. 2003; 14: 66-76.. Clinically, it may be associated with sepsis, hemorrhagic shock, vascular surgery, small bowel transplantation 55. Carden D L, Granger DN. Pathophysiology of ischaemia-reperfusion injury. J. Pathol. 2000; 190: 255-66.,1717. Homer-Vanniasinkam S, Crinnion JN, Gough M J. Post-ischaemic organ dysfunction: a review. Eur. J. Vasc. Endovasc. Surg. 1997; 14: 195-203., and multiple organ failure 1616. Harward TR, Brooks D L, Flynn TC, Seeger JM. Multiple organ dysfunction after mesenteric artery revascularization. J. Vasc. Surg. 1993; 18: 459-67.,2424. Moore EE, Moore FA, Franciose RJ, Kim F, Biffl W, Banerjee A. The postischemic gut serves as a priming bed for circulating neutrophils that provoke multiple organ failure. J. Trauma 1994; 37: 881-7.. Animal studies done by Hart et al1515. Hart ML, Ceonzo KA, Shaffer LA, Takahashi K, Rother RP, Reenstra WR, et al. Gastrointestinal ischemia-reperfusion injury is lectin complement pathway dependent without involving C1q. J Immunol. 2005; 174: 6373-80. using a mice model of intestinal ischemia/reperfusion showed that mice devoid of MBL, yet maintaining intact classical and alternative complement pathways, are protected from intestinal injury, neutrophil infiltration in the intestine, intestinal permeability dysfunction, and secondary liver injury, as measured by transaminases.
In cerebral tissue, researches done with middle cerebral artery occlusion/reperfusion, performed in MBL-deficient and wild-type mice, had shown that infarct volumes studied by magnetic resonance and that clinical neurological deficits were smaller in MBL knockout mice than in wild type77. de la Rosa X, Cervera A, Kristoffersen AK, Valdés CP, Varma HM, Justicia C, et al. Mannose-binding lectin promotes local microvascular thrombosis after transient brain ischemia in mice. Stroke. 2014; 45:1453-9..
Taken together these experimental animal data demonstrate the potential pathophysiologic role of MBL during conditions of ischemia and reperfusion in a variety of vascular beds.
Observational studies in humans reinforce the animal findings. A study with 99 type 1 diabetes patients undergoing simultaneous pancreas-kidney transplantation showed that low pre-transplantation mannose-binding lectin levels predict superior patient and graft survival33. Berger SP, Roos A, Mallat MJ, Schaapherder AF, Doxiadis II, van Kooten C, et al. Low pretransplantation mannose-binding lectin levels predict superior patient and graft survival after simultaneous pancreas-kidney transplantation. J Am Soc Nephrol. 2007; 18: 2416-22.. They have also demonstrated that there is an association of MBL levels >400 ng/ml with poorer graft survival and hypothesized that MBL contributes to the pathogenesis of inflammation-induced vascular damage both in the transplanted organs and in the recipient's native blood vessels33. Berger SP, Roos A, Mallat MJ, Schaapherder AF, Doxiadis II, van Kooten C, et al. Low pretransplantation mannose-binding lectin levels predict superior patient and graft survival after simultaneous pancreas-kidney transplantation. J Am Soc Nephrol. 2007; 18: 2416-22..
In human biopsies, MBL-depositions were observed early after transplantation of ischemically injured kidneys88. de Vries B, Walter SJ, Peutz-Kootstra CJ, Wolfs TG, van Heurn LW, Buurman WA. The mannose-binding lectin-pathway is involved in complement activation in the course of renal ischemia-reperfusion injury. Am J Pathol. 2004; 165: 1677-88.,3434. van der Pol P, Schlagwein N, van Gijlswijk DJ, Berger SP, Roos A, Bajema IM, et al. Mannan-binding lectin mediates renal ischemia/reperfusion injury independent of complement activation. Am J Transplant. 2012; 12: 877-87.. Likewise, Fiane et al 1313. Fiane AE, Videm V, Lingaas PS, Heggelund L, Nielsen EW, Geiran OR, Fung M, Mollnes TE. Mechanism of complement activation and its role in the inflammatory response after thoracoabdominal aortic aneurysm repair. Circulation. 2003; 108:849-56. found considerable MBL dependent complement activation and cytokine production in patients undergoing thoracoabdominal aortic aneurysm repair with thoracoabdominal cross-clamping, a human in vivo model of ischemia-reperfusion.
In restenosis, the role of MBL has been studied by Rugonfalvi-Kiss et al2626. Rugonfalvi-Kiss S, Dósa E, Madsen HO, Endrész V, Prohászka Z, Laki J, et al.. High rate of early restenosis after carotid eversion endarterectomy in homozygous carriers of the normal mannose-binding lectin genotype. Stroke. 2005 ; 36: 944-8. observing 123 patients who underwent carotid endarterectomy and followed-up by carotid duplex scan sonography. They have shown that reoccurrence of stenosis after carotid endarterectomy had a relationship with genetically mediated high MBL serum concentration.
The mechanisms of injury amplification of tissue injury by MBL in this context is not completely understood. Some authors postulate that MBL activation favors local thrombosis77. de la Rosa X, Cervera A, Kristoffersen AK, Valdés CP, Varma HM, Justicia C, et al. Mannose-binding lectin promotes local microvascular thrombosis after transient brain ischemia in mice. Stroke. 2014; 45:1453-9.. The complement and the coagulation systems cross interact at several molecular steps22. Amara U, Rittirsch D, Flierl M, Bruckner U, Klos A, Gebhard F, et al. Interaction between the coagulation and complement system. Adv Exp Med Biol. 2008; 632: 71-79.,2222. Markiewski MM, Nilsson B, Ekdahl KN, Mollnes TE, Lambris JD. Complement and coagulation: strangers or partners in crime? Trends Immunol. 2007;28: 184-192.. Proteins of the lectin pathway can induce thrombus formation through thrombin activation1111. Endo Y, Nakazawa N, Iwaki D, Takahashi M, Matsushita M, Fujita T. Interactions of ficolin and mannose-binding lectin with fibrinogen/fibrin augment the lectin complement pathway. J Innate Immun. 2010;2: 33-42.,2121. La Bonte LR, Pavlov VI, Tan YS, Takahashi K, Takahashi M, Banda NK, et al. Mannose-binding lectin-associated serine protease-1 is a significant contributor to coagulation in a murine model of occlusive thrombosis. J Immunol. 2012; 188: 885-91., thus exacerbating tissue damage after ischemia/reperfusion1818. Jiang H X, Wagner E, Zhang HM, Frank M. Complement 1 inhibitor is a regulator of the alternative complement pathway. J. Exp. Med. 2001; 194: 1609-16.,2323. Matsushita M, Thiel S, Jensenius JC, Terai I, Fujita T. Proteolytic activities of two types of mannose-binding lectin-associated serine protease. J. Immunol. 2000; 165: 2637-42.,3737. Wong N K, Kojima M, Dobo J, Ambrus G, Sim RB. Activities of the MBL-associated serine proteases (MASPs) and their regulation by natural inhibitors. Mol. Immunol. 1999; 36: 853-61..
A direct toxic effect of MBL has also been advocated. Van der Pol et al3434. van der Pol P, Schlagwein N, van Gijlswijk DJ, Berger SP, Roos A, Bajema IM, et al. Mannan-binding lectin mediates renal ischemia/reperfusion injury independent of complement activation. Am J Transplant. 2012; 12: 877-87., using a rat model of renal ischemia, identified that after reperfusion exposure of tubular epithelial cells to circulation-derived MBL occurred internalization of MBL followed by the rapid induction of tubular epithelial cell death. This MBL-mediated tubular injury was completely independent of complement activation since attenuation of complement activation was not protective against renal ischemic reperfusion injury. These observations suggested that MBL may have a direct toxic effect on the cells and that the membrane complex attack resulting from complement activation may not be crucial to this effect.
CONCLUSION
Although the mechanisms by which activation of complement via MBL increase the tissue injury caused by ischemia/reperfusion are not completely understood the deleterious role of this component of innate immune system on this context is clear both in humans and in animals. Specific blockade of MBL or inhibition of the lectin complement pathway may represent a therapeutically relevant strategy for the prevention of ischemic reperfusion associated damage.
REFERENCES
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1Akiyama T, Moussa I, Reimers B, Ferraro M, Kobayashi Y, Blengino S,et al. Angiographic and clinical outcome following coronary stenting of small vessels: a comparison with coronary stenting of large vessels. J Am Coll Cardiol. 1998; 32:1610-8.
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2Amara U, Rittirsch D, Flierl M, Bruckner U, Klos A, Gebhard F, et al. Interaction between the coagulation and complement system. Adv Exp Med Biol. 2008; 632: 71-79.
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3Berger SP, Roos A, Mallat MJ, Schaapherder AF, Doxiadis II, van Kooten C, et al. Low pretransplantation mannose-binding lectin levels predict superior patient and graft survival after simultaneous pancreas-kidney transplantation. J Am Soc Nephrol. 2007; 18: 2416-22.
-
4Borissoff JI, Heeneman S, Kilinç E, Kassák P, Van Oerle R, Winckers K, et al. Early atherosclerosis exhibits an enhanced procoagulant state. Circulation. 2010 ; 122: 821-30.
-
5Carden D L, Granger DN. Pathophysiology of ischaemia-reperfusion injury. J. Pathol. 2000; 190: 255-66.
-
6Davies MJ, Woolf N, Rowles PM, Pepper J. Morphology of the endothelium over atherosclerotic plaques in human coronary arteries. Br. Heart J. 1988; 60:459-64.
-
7de la Rosa X, Cervera A, Kristoffersen AK, Valdés CP, Varma HM, Justicia C, et al. Mannose-binding lectin promotes local microvascular thrombosis after transient brain ischemia in mice. Stroke. 2014; 45:1453-9.
-
8de Vries B, Walter SJ, Peutz-Kootstra CJ, Wolfs TG, van Heurn LW, Buurman WA. The mannose-binding lectin-pathway is involved in complement activation in the course of renal ischemia-reperfusion injury. Am J Pathol. 2004; 165: 1677-88.
-
9Denes L, Entz L, Jancsik V. Restenosis and therapy. Int J Vasc Med. 2012; 2012:406236.
-
10Elezi S, Kastrati A, Neumann FJ, Hadamitzky M, Dirschinger J, Schömig A.Vessel size and long-term outcome after coronary stent placement. Circulation. 1998; 98: 1875-80.
-
11Endo Y, Nakazawa N, Iwaki D, Takahashi M, Matsushita M, Fujita T. Interactions of ficolin and mannose-binding lectin with fibrinogen/fibrin augment the lectin complement pathway. J Innate Immun. 2010;2: 33-42.
-
12Farb A, Weber DK, Kolodgie FD, Burke AP, Virmani R. Morphological predictors of restenosis after coronary stenting in humans. Circulation. 2002; 105: 2974-80.
-
13Fiane AE, Videm V, Lingaas PS, Heggelund L, Nielsen EW, Geiran OR, Fung M, Mollnes TE. Mechanism of complement activation and its role in the inflammatory response after thoracoabdominal aortic aneurysm repair. Circulation. 2003; 108:849-56.
-
14Garred P. Mannose-binding lectin genetics: from A to Z. Biochem Soc Trans. 2008 ;36 (Pt 6):1461-6.
-
15Hart ML, Ceonzo KA, Shaffer LA, Takahashi K, Rother RP, Reenstra WR, et al. Gastrointestinal ischemia-reperfusion injury is lectin complement pathway dependent without involving C1q. J Immunol. 2005; 174: 6373-80.
-
16Harward TR, Brooks D L, Flynn TC, Seeger JM. Multiple organ dysfunction after mesenteric artery revascularization. J. Vasc. Surg. 1993; 18: 459-67.
-
17Homer-Vanniasinkam S, Crinnion JN, Gough M J. Post-ischaemic organ dysfunction: a review. Eur. J. Vasc. Endovasc. Surg. 1997; 14: 195-203.
-
18Jiang H X, Wagner E, Zhang HM, Frank M. Complement 1 inhibitor is a regulator of the alternative complement pathway. J. Exp. Med. 2001; 194: 1609-16.
-
19Kasaoka S, Tobis JM, Akiyama T, Reimers B, Di Mario C, Wong ND, et al. Angiographic and intravascular ultrasound predictors of in-stent restenosis. J Am Coll Cardiol. 1998 15; 32: 1630.
-
20Kastrati A, Schömig A, Elezi S, Schühlen H, Wilhelm M, Dirschinger J. Interlesion dependence of the risk for restenosis in patients with coronary stent placement in in multiple lesions. Circulation. 1998; 97: 2396-401.
-
21La Bonte LR, Pavlov VI, Tan YS, Takahashi K, Takahashi M, Banda NK, et al. Mannose-binding lectin-associated serine protease-1 is a significant contributor to coagulation in a murine model of occlusive thrombosis. J Immunol. 2012; 188: 885-91.
-
22Markiewski MM, Nilsson B, Ekdahl KN, Mollnes TE, Lambris JD. Complement and coagulation: strangers or partners in crime? Trends Immunol. 2007;28: 184-192.
-
23Matsushita M, Thiel S, Jensenius JC, Terai I, Fujita T. Proteolytic activities of two types of mannose-binding lectin-associated serine protease. J. Immunol. 2000; 165: 2637-42.
-
24Moore EE, Moore FA, Franciose RJ, Kim F, Biffl W, Banerjee A. The postischemic gut serves as a priming bed for circulating neutrophils that provoke multiple organ failure. J. Trauma 1994; 37: 881-7.
-
25Rugonfalvi-Kiss S, Dósa E, Madsen HO, Endrész V, Prohászka Z, Laki J, et al. High rate of early restenosis after carotid eversion endarterectomy in homozygous carriers of the normal mannose-binding lectin genotype. Stroke. 2005; 36: 944-8.
-
26Rugonfalvi-Kiss S, Dósa E, Madsen HO, Endrész V, Prohászka Z, Laki J, et al.. High rate of early restenosis after carotid eversion endarterectomy in homozygous carriers of the normal mannose-binding lectin genotype. Stroke. 2005 ; 36: 944-8.
-
27Serruys PW, de Jaegere P, Kiemeneij F, Macaya C, Rutsch W, Heyndrickx G, et al. A comparison of balloon-expandable-stent implantation with balloon angioplasty in patients with coronary artery disease. Benestent Study Group. N Engl J Med. 1994; 331: 489-95.
-
28Serruys PW, Umans V, Heyndrickx GR, van den Brand M, de Feyter PJ, Wijns W, et al. Elective PTCA of totally occluded coronary arteries not associated with acute myocardial infarction; short-term and long-term results. Eur Heart J. 1985; 6: 2-12.
-
29Tendler D A. Acute intestinal ischemia and infarction. Semin. Gastrointest. Dis. 2003; 14: 66-76.
-
30Thiel S, Vorup-Jensen T, Stover CM, Schwaeble W, Laursen SB, Poulsen K, et al. A second serine protease associated with mannan binding lectin that activates complement. Nature. 1997; 386: 506-510.
-
31Turner MW. Mannose-binding lectin: the pluripotent molecule of the innate immune system. Immunol. Today. 1996; 17:532-40.
-
32Turner MW. The lectin pathway of complement activation. Res. Immunol. 1996; 147:110-5.
-
33Uchida Y, Uchida Y, Matsuyama A, Koga A, Kanai M, Sakurai T. Formation of web- and membrane-like structures on the edges of bare-metal coronary stents. Circ. J. 2010 ;74:1830-6.
-
34van der Pol P, Schlagwein N, van Gijlswijk DJ, Berger SP, Roos A, Bajema IM, et al. Mannan-binding lectin mediates renal ischemia/reperfusion injury independent of complement activation. Am J Transplant. 2012; 12: 877-87.
-
35Walsh MC, Bourcier T, Takahashi K, Shi L, Busche MN, Rother RP,et al. Mannose-binding lectin is a regulator of inflammation that accompanies myocardial ischemia and reperfusion injury. J Immunol. 2005; 175: 541-6.
-
36Williams KJ, Tabas I. The response-to-retention hypothesis of early atherogenesis. Arterioscler Thromb Vasc Biol. 1995; 15:551-61.
-
37Wong N K, Kojima M, Dobo J, Ambrus G, Sim RB. Activities of the MBL-associated serine proteases (MASPs) and their regulation by natural inhibitors. Mol. Immunol. 1999; 36: 853-61.
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Financial source: none
Publication Dates
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Publication in this collection
Jan-Mar 2016
History
-
Received
21 May 2015 -
Accepted
03 Sept 2015