Angiopoietin-1 variant reduces LPS-induced microvascular dysfunction in a murine model of sepsis

Critical Care

Volumn 16, Issue 5, 2012, Pages

  Alfieri, Alessio ^a   Watson, Jay J ^a   Kammerer, Richard A ^b   Tasab, Mohammed ^c   Progias, Pavlos ^c   Reeves, Kimberly ^a   Brown, Nicola J ^a   Brookes, Zoe L ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b PAUL SCHERRER INSTITUTE   (Switzerland)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENIC FACTOR; ANGIOPOIETIN 1; CADHERIN; CYTOKINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; MATRILIN 1 ANGIOPOIETIN 1; PROTEIN KINASE B; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN; ANGPT1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DOPPLER FLOWMETRY; ENDOTOXEMIA; FLUID TRANSPORT; IMMUNOMODULATION; MALE; MICROANGIOPATHY; MICROCIRCULATION; MICROSCOPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEPSIS; TISSUE PERFUSION; ANIMAL; C3H MOUSE; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; GENETIC VARIABILITY; GENETICS; HUMAN; PHYSIOLOGY; RANDOMIZATION;

ANGIOPOIETIN-1; ANIMALS; DISEASE MODELS, ANIMAL; GENETIC VARIATION; HUMANS; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED C3H; MICROCIRCULATION; RANDOM ALLOCATION; SEPSIS;

EID: 84866928765     PISSN: 13648535     EISSN: 1466609X     Source Type: Journal    
DOI: 10.1186/cc11666     Document Type: Article

References (50)

1. Hawiger J, Musser JM. How to approach gene wars in sepsis?. Crit Care 2011, 15:1007. 10.1186/cc10482, 22136332.
2. Spronk PE, Zandstra DF, Ince C. Bench-to-bedside review: sepsis is a disease of the microcirculation. Crit Care 2004, 8:462-468. 10.1186/cc2894, 1065042, 15566617.
3. Ince C. The microcirculation is the motor of sepsis. Crit Care 2005, 9(Suppl 4):S13-S19. 10.1186/cc3753, 3226164, 16168069.
4. Jones AE, Puskarich MA. Sepsis-induced tissue hypoperfusion. Crit Care Clin 2009, 25:769-779, ix. 10.1016/j.ccc.2009.06.003, 19892252.
5. Angus DC, Linde-Zwirble WT, Lidicker J, Clermont G, Carcillo J, Pinsky MR. Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit Care Med 2001, 29:1303-1310. 10.1097/00003246-200107000-00002, 11445675.
6. Dellinger RP, Levy MM, Carlet JM, Bion J, Parker MM, Jaeschke R, Reinhart K, Angus DC, Brun-Buisson C, Beale R, Calandra T, Dhainaut JF, Gerlach H, Harvey M, Marini JJ, Marshall J, Ranieri M, Ramsay G, Sevransky J, Thompson BT, Townsend S, Vender JS, Zimmerman JL, Vincent JL. Surviving Sepsis Campaign: international guidelines for management of severe sepsis and septic shock: 2008. Crit Care Med 2008, 36:296-327. 10.1097/01.CCM.0000298158.12101.41, 18158437.
7. Brindle NP, Saharinen P, Alitalo K. Signaling and functions of angiopoietin-1 in vascular protection. Circ Res 2006, 98:1014-1023. 10.1161/01.RES.0000218275.54089.12, 2270395, 16645151.
8. Augustin HG, Koh GY, Thurston G, Alitalo K. Control of vascular morphogenesis and homeostasis through the angiopoietin-Tie system. Nat Rev Mol Cell Biol 2009, 10:165-177. 10.1038/nrm2639, 19234476.
9. Partovian C, Zhuang Z, Moodie K, Lin M, Ouchi N, Sessa WC, Walsh K, Simons M. PKCα activates eNOS and increases arterial blood flow in vivo. Circ Res 2005, 97:482-487. 10.1161/01.RES.0000179775.04114.45, 16081872.
10. Witzenbichler B, Westermann D, Knueppel S, Schultheiss HP, Tschope C. Protective role of angiopoietin-1 in endotoxic shock. Circulation 2005, 111:97-105. 10.1161/01.CIR.0000151287.08202.8E, 15611372.
11. Mammoto T, Parikh SM, Mammoto A, Gallagher D, Chan B, Mostoslavsky G, Ingber DE, Sukhatme VP. Angiopoietin-1 requires p190 RhoGAP to protect against vascular leakage in vivo. J Biol Chem 2007, 282:23910-23918. 10.1074/jbc.M702169200, 17562701.
12. Zhu YG, Qu JM, Zhang J, Jiang HN, Xu JF. Novel interventional approaches for ALI/ARDS: cell-based gene therapy. Mediators Inflamm 2011, 2011:560194. 3139183, 21785528.
13. Cho CH, Kammerer RA, Lee HJ, Steinmetz MO, Ryu YS, Lee SH, Yasunaga K, Kim KT, Kim I, Choi HH, Kim W, Kim SH, Park SK, Lee GM, Koh GY. COMP-Ang1: a designed angiopoietin-1 variant with nonleaky angiogenic activity. Proc Natl Acad Sci USA 2004, 101:5547-5552. 10.1073/pnas.0307574101, 397420, 15060279.
14. Macdonald PR, Progias P, Ciani B, Patel S, Mayer U, Steinmetz MO, Kammerer RA. Structure of the extracellular domain of Tie receptor tyrosine kinases and localization of the angiopoietin-binding epitope. J Biol Chem 2006, 281:28408-28414. 10.1074/jbc.M605219200, 16849318.
15. Poschl E, Fox JW, Block D, Mayer U, Timpl R. Two non-contiguous regions contribute to nidogen binding to a single EGF-like motif of the laminin gamma 1 chain. EMBO J 1994, 13:3741-3747. 395285, 8070402.
16. Bingle L, Lewis CE, Corke KP, Reed MW, Brown NJ. Macrophages promote angiogenesis in human breast tumour spheroids in vivo. Br J Cancer 2006, 94:101-107. 10.1038/sj.bjc.6602901, 2361081, 16404363.
17. Brookes ZL, Stedman EN, Guerrini R, Lawton BK, Calo G, Lambert DG. Proinflammatory and vasodilator effects of nociceptin/orphanin FQ in the rat mesenteric microcirculation are mediated by histamine. Am J Physiol Heart Circ Physiol 2007, 293:H2977-H2985. 10.1152/ajpheart.00448.2007, 17766480.
18. Cho CH, Kammerer RA, Lee HJ, Yasunaga K, Kim KT, Choi HH, Kim W, Kim SH, Park SK, Lee GM, Koh GY. Designed angiopoietin-1 variant, COMP-Ang1, protects against radiation-induced endothelial cell apoptosis. Proc Natl Acad Sci USA 2004, 101:5553-5558. 10.1073/pnas.0307575101, 397421, 15060280.
19. Allcock GH, Allegra M, Flower RJ, Perretti M. Neutrophil accumulation induced by bacterial lipopolysaccharide: effects of dexamethasone and annexin 1. Clin Exp Immunol 2001, 123:62-67. 10.1046/j.1365-2249.2001.01370.x, 1905950, 11167999.
20. McGown CC, Brown NJ, Hellewell PG, Reilly CS, Brookes ZL. Beneficial microvascular and anti-inflammatory effects of pravastatin during sepsis involve nitric oxide synthase III. Br J Anaesth 2010, 104:183-190. 10.1093/bja/aep361, 20086063.
21. Matsuda N, Hattori Y. Vascular biology in sepsis: pathophysiological and therapeutic significance of vascular dysfunction. J Smooth Muscle Res 2007, 43:117-137. 10.1540/jsmr.43.117, 17928746.
22. Lee WL, Liles WC. Endothelial activation, dysfunction and permeability during severe infections. Curr Opin Hematol 2011, 18:191-196. 10.1097/MOH.0b013e328345a3d1, 21423012.
23. Aird WC. The role of the endothelium in severe sepsis and multiple organ dysfunction syndrome. Blood 2003, 101:3765-3777. 10.1182/blood-2002-06-1887, 12543869.
24. Pettipher ER, Higgs GA, Henderson B. Interleukin 1 induces leukocyte infiltration and cartilage proteoglycan degradation in the synovial joint. Proc Natl Acad Sci USA 1986, 83:8749-8753. 10.1073/pnas.83.22.8749, 387009, 3490671.
25. Rampart M, Williams TJ. Evidence that neutrophil accumulation induced by interleukin-1 requires both local protein biosynthesis and neutrophil CD18 antigen expression in vivo. Br J Pharmacol 1988, 94:1143-1148. 10.1111/j.1476-5381.1988.tb11632.x, 1854081, 2850056.
26. Bateman RM, Sharpe MD, Ellis CG. Bench-to-bedside review: microvascular dysfunction in sepsis - hemodynamics, oxygen transport, and nitric oxide. Crit Care 2003, 7:359-373. 10.1186/cc2353, 270719, 12974969.
27. Damas P, Canivet JL, de GD, Vrindts Y, Albert A, Franchimont P, Lamy M. Sepsis and serum cytokine concentrations. Crit Care Med 1997, 25:405-412. 10.1097/00003246-199703000-00006, 9118654.
28. Pinsky MR, Vincent JL, Deviere J, Alegre M, Kahn RJ, Dupont E. Serum cytokine levels in human septic shock. Relation to multiple-system organ failure and mortality. Chest 1993, 103:565-575. 10.1378/chest.103.2.565, 8432155.
29. Murata A. Granulocyte colony-stimulating factor as the expecting sword for the treatment of severe sepsis. Curr Pharm Des 2003, 9:1115-1120. 10.2174/1381612033454982, 12769751.
30. Pugin J. Immunostimulation is a rational therapeutic strategy in sepsis. Novartis Found Symp 2007, 280:21-27.
31. Bossink AW, Paemen L, Jansen PM, Hack CE, Thijs LG, Van DJ. Plasma levels of the chemokines monocyte chemotactic proteins-1 and -2 are elevated in human sepsis. Blood 1995, 86:3841-3847.
32. Zisman DA, Kunkel SL, Strieter RM, Tsai WC, Bucknell K, Wilkowski J, Standiford TJ. MCP-1 protects mice in lethal endotoxemia. J Clin Invest 1997, 99:2832-2836. 10.1172/JCI119475, 508132, 9185504.
33. Al SH. Therapeutic angiogenesis in cardiovascular disease. J Cardiothorac Surg 2007, 2:49. 10.1186/1749-8090-2-49, 2169246, 18021404.
34. Mankhambo LA, Banda DL, Jeffers G, White SA, Balmer P, Nkhoma S, Phiri H, Molyneux EM, Hart CA, Molyneux ME, Heyderman RS, Carrol ED. The role of angiogenic factors in predicting clinical outcome in severe bacterial infection in Malawian children. Crit Care 2010, 14:R91. 10.1186/cc9025, 2911728, 20492647.
35. Mofarrahi M, Nouh T, Qureshi S, Guillot L, Mayaki D, Hussain SN. Regulation of angiopoietin expression by bacterial lipopolysaccharide. Am J Physiol Lung Cell Mol Physiol 2008, 294:L955-L963. 10.1152/ajplung.00449.2007, 18310225.
36. Potter MD, Barbero S, Cheresh DA. Tyrosine phosphorylation of VE-cadherin prevents binding of p120- and beta-catenin and maintains the cellular mesenchymal state. J Biol Chem 2005, 280:31906-31912. 10.1074/jbc.M505568200, 16027153.
37. Orrington-Myers J, Gao X, Kouklis P, Broman M, Rahman A, Vogel SM, Malik AB. Regulation of lung neutrophil recruitment by VE-cadherin. Am J Physiol Lung Cell Mol Physiol 2006, 291:L764-L771. 10.1152/ajplung.00502.2005, 16782751.
38. Cunha FQ, Assreuy J, Moss DW, Rees D, Leal LM, Moncada S, Carrier M, O'Donnell CA, Liew FY. Differential induction of nitric oxide synthase in various organs of the mouse during endotoxaemia: role of TNF-alpha and IL-1-beta. Immunology 1994, 81:211-215. 1422329, 7512527.
39. Hollenberg SM, Cinel I. Bench-to-bedside review: nitric oxide in critical illness - update 2008. Crit Care 2009, 13:218. 10.1186/cc7706, 2750127, 19664175.
40. Buwalda M, Ince C. Opening the microcirculation: can vasodilators be useful in sepsis?. Intensive Care Med 2002, 28:1208-1217. 10.1007/s00134-002-1407-2, 12209267.
41. Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev 2007, 87:315-424. 10.1152/physrev.00029.2006, 2248324, 17237348.
42. Hwang JA, Lee EH, Lee SD, Park JB, Jeon BH, Cho CH. COMP-Ang1 ameliorates leukocyte adhesion and reinforces endothelial tight junctions during endotoxemia. Biochem Biophys Res Commun 2009, 381:592-596. 10.1016/j.bbrc.2009.02.096, 19245790.
43. Kim DH, Jung YJ, Lee AS, Lee S, Kang KP, Lee TH, Lee SY, Jang KY, Moon WS, Choi KS, Yoon KH, Sung MJ, Park SK, Kim W. COMP-angiopoietin-1 decreases lipopolysaccharide-induced acute kidney injury. Kidney Int 2009, 76:1180-1191. 10.1038/ki.2009.387, 19812542.
44. Eklund L, Olsen BR. Tie receptors and their angiopoietin ligands are context-dependent regulators of vascular remodeling. Exp Cell Res 2006, 312:630-641. 10.1016/j.yexcr.2005.09.002, 16225862.
45. David S, Park JK, Meurs M, Zijlstra JG, Koenecke C, Schrimpf C, Shushakova N, Gueler F, Haller H, Kumpers P. Acute administration of recombinant angiopoietin-1 ameliorates multiple-organ dysfunction syndrome and improves survival in murine sepsis. Cytokine 2011, 55:251-259. 10.1016/j.cyto.2011.04.005, 21531574.
46. Kumpers P, Gueler F, David S, Van SP, Dumont DJ, Park JK, Bockmeyer CL, Parikh SM, Pavenstadt H, Haller H, Shushakova N. The synthetic Tie2 agonist peptide vasculotide protects against vascular leakage and reduces mortality in murine abdominal sepsis. Crit Care 2011, 15:R261. 10.1186/cc10523, 3334812, 22040774.
47. Thomas M, Augustin HG. The role of the Angiopoietins in vascular morphogenesis. Angiogenesis 2009, 12:125-137. 10.1007/s10456-009-9147-3, 19449109.
48. Vestweber D. VE-cadherin: the major endothelial adhesion molecule controlling cellular junctions and blood vessel formation. Arterioscler Thromb Vasc Biol 2008, 28:223-232.
49. Findley CM, Cudmore MJ, Ahmed A, Kontos CD. VEGF induces Tie2 shedding via a phosphoinositide 3-kinase/Akt dependent pathway to modulate Tie2 signaling. Arterioscler Thromb Vasc Biol 2007, 27:2619-2626. 10.1161/ATVBAHA.107.150482, 17901375.
50. Novotny NM, Lahm T, Markel TA, Crisostomo PR, Wang M, Wang Y, Tan J, Meldrum DR. Angiopoietin-1 in the treatment of ischemia and sepsis. Shock 2009, 31:335-341. 10.1097/SHK.0b013e3181862c63, 18791498.