Selective V1a agonism attenuates vascular dysfunction and fluid accumulation in ovine severe sepsis

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 303, Issue 10, 2012, Pages

  Rehberg, Sebastian ^a,b   Yamamoto, Yusuke ^a   Sousse, Linda ^a   Bartha, Eva ^a   Jonkam, Collette ^a   Hasselbach, Anthony K ^a   Traber, Lillian D ^a   Cox, Robert A ^a,c   Westphal, Martin ^b   Enkhbaatar, Perenlei ^a,c   Traber, Daniel L ^a,c  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^c SHRINERS HOSPITALS FOR CHILDREN   (United States)

Author keywords

Angiopoietin 2; Arginine vasopressin; Vascular endothelial growth factor; Vascular leakage

Indexed keywords

ANGIOPOIETIN 2; ARGIPRESSIN; UNCLASSIFIED DRUG; VASCULOTROPIN; VASOPRESSIN DERIVATIVE; VASOPRESSIN V1A RECEPTOR; VASOPRESSIN V1A RECEPTOR AGONIST; VASOPRESSIN V2 RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ARTIFICIAL VENTILATION; BACTERIAL PNEUMONIA; CONTROLLED STUDY; DISEASE SEVERITY; HYPOTENSION; IMMUNOHISTOCHEMISTRY; LUNG BURN; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; NONHUMAN; PRIORITY JOURNAL; SEPSIS; SEPTIC SHOCK; SHEEP; VASCULAR ENDOTHELIUM;

ANGIOPOIETIN-2; ANIMALS; ARGININE VASOPRESSIN; ARTERIAL PRESSURE; BLOOD VESSELS; CAPILLARY PERMEABILITY; DISEASE MODELS, ANIMAL; FEMALE; HEMODYNAMICS; INFUSIONS, INTRAVENOUS; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; NEUTROPHIL INFILTRATION; NITRIC OXIDE; PNEUMONIA, STAPHYLOCOCCAL; RECEPTORS, VASOPRESSIN; SEPSIS; SHEEP; SMOKE INHALATION INJURY; TIME FACTORS; TYROSINE; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASOCONSTRICTION; VASOCONSTRICTOR AGENTS; VASOTOCIN; VENTRICULAR FUNCTION, LEFT;

EID: 84869159866     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00390.2012     Document Type: Article

References (55)

1. Barrett LK, Singer M, Clapp LH. Vasopressin: mechanisms of action on the vasculature in health and in septic shock. Crit Care Med 35: 33-40, 2007
2. Berde B, Boissonnas RA, Huguenin RL, Sturmer E. Vasopressin analogues with selective pressor activity. Experientia 20: 42-43, 1964.
3. Bernard GR, Artigas A, Brigham KL, Carlet J, Falke K, Hudson L, Lamy M, Legall JR, Morris A, Spragg R. The American-European Consensus Conference on ARDS. Definitions, mechanisms, relevant outcomes, and clinical trial coordination. Am J Respir Crit Care Med 149: 818-824, 1994.
4. Boyd JH, Forbes J, Nakada TA, Walley KR, Russell JA. Fluid resuscitation in septic shock: a positive fluid balance and elevated central venous pressure are associated with increased mortality. Crit Care Med 39: 259-265, 2011.
5. Burkhoff D, Mirsky I, Suga H. Assessment of systolic and diastolic ventricular properties via pressure-volume analysis: a guide for clinical, translational, and basic researchers. Am J Physiol Heart Circ Physiol 289: H501-H512, 2005.
6. Chappell D, Westphal M, Jacob M. The impact of the glycocalyx on microcirculatory oxygen distribution in critical illness. Curr Opin Anaesthesiol 22: 155-162, 2009.
7. Cox RA, Burke AS, Soejima K, Murakami K, Katahira J, Traber LD, Herndon DN, Schmalstieg FC, Traber DL, Hawkins HK. Airway obstruction in sheep with burn and smoke inhalation injuries. Am J Respir Cell Mol Biol 29: 295-302, 2003.
8. 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 36: 296-327, 2008.
9. Dunser MW, Mayr AJ, Ulmer H, Knotzer H, Sumann G, Pajk W, Friesenecker B, Hasibeder WR. Arginine vasopressin in advanced vasodilatory shock: a prospective, randomized, controlled study. Circulation 107: 2313-2319, 2003.
10. Enkhbaatar P, Connelly R, Wang J, Nakano Y, Lange M, Hamahata A, Horvath E, Szabo C, Jaroch S, Holscher P, Hillmann M, Traber LD, Schmalstieg FC, Herndon DN, Traber DL. Inhibition of neuronal nitric oxide synthase in ovine model of acute lung injury. Crit Care Med 37: 208-214, 2009.
11. Enkhbaatar P, Joncam C, Traber L, Nakano Y, Wang J, Lange M, Connelly R, Kulp G, Saunders F, Huda R, Cox R, Schmalstieg F, Herndon D, Traber D. Novel ovine model of methicillin-resistant Staphylococcus aureus-induced pneumonia and sepsis. Shock 29: 642-649, 2008
12. Fiedler U, Scharpfenecker M, Koidl S, Hegen A, Grunow V, Schmidt JM, Kriz W, Thurston G, Augustin HG. The Tie-2 ligand angiopoietin-2 is stored in and rapidly released upon stimulation from endothelial cell Weibel-Palade bodies. Blood 103: 4150-4156, 2004.
13. Ganter MT, Cohen MJ, Brohi K, Chesebro BB, Staudenmayer KL, Rahn P, Christiaans SC, Bir ND, Pittet JF. Angiopoietin-2, marker and mediator of endothelial activation with prognostic significance early after trauma? Ann Surg 247: 320-326, 2008.
14. Gillett AM, Wallace MJ, Gillespie MT, Hooper SB. Increased expansion of the lung stimulates calmodulin 2 expression in fetal sheep. Am J Physiol Lung Cell Mol Physiol 282: L440-L447, 2002.
15. Jonkam CC, Lange M, Traber DL, Maybauer DM, Maybauer MO, Bansal K, Hamahata A, Zhu Y, Esechie A, Traber LD, Sousse L, Rehberg S, Herndon DN, Enkhbaatar P. Cardiovascular collapse and vascular permeability changes in an ovine model of methicillin-resistant staphylococcus aureus sepsis. Shock 32: 621-625, 2009.
16. Kanwar S, Woodman RC, Poon MC, Murohara T, Lefer AM, Davenpeck KL, Kubes P. Desmopressin induces endothelial P-selectin expression and leukocyte rolling in postcapillary venules. Blood 86: 2760-2766, 1995.
17. 2 receptor-and cAMPmediated signaling. J Thromb Haemost 1: 821-828, 2003.
18. Kaufmann JE, Vischer UM. Cellular mechanisms of the hemostatic effects of desmopressin (DDAVP). J Thromb Haemost 1: 682-689, 2003.
19. Kim I, Kim HG, So JN, Kim JH, Kwak HJ, Koh GY. Angiopoietin-1 regulates endothelial cell survival through the phosphatidylinositol 3'-kinase/Akt signal transduction pathway. Circ Res 86: 24-29, 2000.
20. Kumar P, Shen Q, Pivetti CD, Lee ES, Wu MH, Yuan SY. Molecular mechanisms of endothelial hyperpermeability: implications in inflammation. Expert Rev Mol Med 11: e19, 2009.
21. Kumpers P, Lukasz A, David S, Horn R, Hafer C, Faulhaber-Walter R, Fliser D, Haller H, Kielstein JT. Excess circulating angiopoietin-2 is a strong predictor of mortality in critically ill medical patients. Crit Care 12: R147, 2008.
22. Lange M, Connelly R, Traber DL, Hamahata A, Nakano Y, Esechie A, Jonkam C, von Borzyskowski S, Traber LD, Schmalstieg FC, Herndon DN, Enkhbaatar P. Time course of nitric oxide synthases, nitrosative stress, and poly(ADP ribosylation) in an ovine sepsis model. Crit Care 14: R129, 2010.
23. Lange M, Traber DL, Enkhbaatar P. The authors reply. Crit Care Med 40: 356-357, 2011.
24. 1a receptor agonist FE 202158 reverses platelet activating factor (PAF)-induced hypotension, vascular leak, impaired tissue perfusion, and mortality in rats (Abstract). Shock 1, Suppl 2: P21, 2008.
25. Lee WL, Liles WC. Endothelial activation, dysfunction and permeability during severe infections. Curr Opin Hematol 18: 191-196, 2011.
26. Luckner G, Dunser MW, Jochberger S, Mayr VD, Wenzel V, Ulmer H, Schmid S, Knotzer H, Pajk W, Hasibeder W, Mayr AJ, Friesenecker B. Arginine vasopressin in 316 patients with advanced vasodilatory shock. Crit Care Med 33: 2659-2666, 2005.
27. Maisonpierre PC, Suri C, Jones PF, Bartunkova S, Wiegand SJ, Radziejewski C, Compton D, McClain J, Aldrich TH, Papadopoulos N, Daly TJ, Davis S, Sato TN, Yancopoulos GD. Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science 277: 55-60, 1997.
28. 2+ concentration in cultured rat hippocampal neurons. Brain Res Bull 49: 343-347, 1999.
29. Morelli A, Ertmer C, Rehberg S, Lange M, Orecchioni A, Cecchini V, Bachetoni A, D'Alessandro M, Van Aken H, Pietropaoli P, Westphal M. Continuous terlipressin versus vasopressin infusion in septic shock (TERLIVAP): a randomized, controlled pilot study. Crit Care 13: R130, 2009
30. Orfanos SE, Kotanidou A, Glynos C, Athanasiou C, Tsigkos S, Dimopoulou I, Sotiropoulou C, Zakynthinos S, Armaganidis A, Papapetropoulos A, Roussos C. Angiopoietin-2 is increased in severe sepsis: correlation with inflammatory mediators. Crit Care Med 35: 199-206, 2007.
31. Patel BM, Chittock DR, Russell JA, Walley KR. Beneficial effects of short-term vasopressin infusion during severe septic shock. Anesthesiology 96: 576-582, 2002.
32. Paulus P, Jennewein C, Zacharowski K. Biomarkers of endothelial dysfunction: can they help us deciphering systemic inflammation and sepsis? Biomarkers 16, Suppl 1: S11-S21, 2011.
33. Pearce ML, Yamashita J, Beazell J. Measurement of Pulmonary Edema. Circ Res 16: 482-488, 1965.
34. 2 receptors in animal models relevant to human disease. Basic Clin Pharmacol Toxicol 99: 96-103, 2006.
35. Pickkers P, Sprong T, Eijk L, Hoeven H, Smits P, Deuren M. Vascular endothelial growth factor is increased during the first 48 hours of human septic shock and correlates with vascular permeability. Shock 24: 508-512, 2005.
36. Polito A, Parisini E, Ricci Z, Picardo S, Annane D. Vasopressin for treatment of vasodilatory shock: an ESICM systematic review and metaanalysis. Intensive Care Med 38: 9-19, 2011.
37. Rehberg S, Enkhbaatar P, Rehberg J, La E, Ferdyan N, Qi S, Wisniewski K, Traber LD, Schteingart C, Rivière P, Laporte R, Traber DL. Unlike arginine vasopressin, the selective V1a receptor agonist FE 202158 does not cause procoagulant effects by releasing von Willebrand factor. Crit Care Med 40: 1957-1960, 2012.
38. Rehberg S, Ertmer C, Kohler G, Spiegel HU, Morelli A, Lange M, Moll K, Schlack K, Van Aken H, Su F, Vincent JL, Westphal M. Role of arginine vasopressin and terlipressin as first-line vasopressor agents in fulminant ovine septic shock. Intensive Care Med 35: 1286-1296, 2009.
39. 2-receptor antagonism in septic shock: a randomized, controlled, experimental study. Crit Care 14: R200, 2010.
40. 1a receptor agonism in ovine septic shock. Crit Care Med 39: 119-125, 2011.
41. Russell J, Walley K, Singer J, Gordon A, Hébert P, Cooper D, Holmes C, Mehta S, Granton J, Storms M, Cook D, Presneill J, Ayers D. Vasopressin versus norepinephrine infusion in patients with septic shock. N Engl J Med 358: 877-887, 2008.
42. Russell JA. Management of sepsis. N Engl J Med 355: 1699-1713, 2006.
43. Simon F, Giudici R, Scheuerle A, Groger M, Asfar P, Vogt JA, Wachter U, Ploner F, Georgieff M, Moller P, Laporte R, Radermacher P, Calzia E, Hauser B. Comparison of cardiac, hepatic, and renal effects of arginine vasopressin and noradrenaline during porcine fecal peritonitis: a randomized controlled trial. Crit Care 13: R113, 2009.
44. Soriano FG, Nogueira AC, Caldini EG, Lins MH, Teixeira AC, Cappi SB, Lotufo PA, Bernik MM, Zsengeller Z, Chen M, Szabo C. Potential role of poly(adenosine 5'-diphosphate-ribose) polymerase activation in the pathogenesis of myocardial contractile dysfunction associated with human septic shock. Crit Care Med 34: 1073-1079, 2006.
45. Sun Q, Dimopoulos G, Nguyen DN, Tu Z, Nagy N, Hoang AD, Rogiers P, De Backer D, Vincent JL. Low-dose vasopressin in the treatment of septic shock in sheep. Am J Respir Crit Care Med 168: 481-486, 2003.
46. Thurston G, Rudge JS, Ioffe E, Zhou H, Ross L, Croll SD, Glazer N, Holash J, McDonald DM, Yancopoulos GD. Angiopoietin-1 protects the adult vasculature against plasma leakage. Nat Med 6: 460-463, 2000.
47. Torgersen C, Dunser MW, Wenzel V, Jochberger S, Mayr V, Schmittinger CA, Lorenz I, Schmid S, Westphal M, Grander W, Luckner G. Comparing two different arginine vasopressin doses in advanced vasodilatory shock: a randomized, controlled, open-label trial. Intensive Care Med 36: 57-65, 2010.
48. 1a receptor agonists in experimental septic shock (Abstract). Crit Care 11: P51, 2007.
49. van der Heijden M, van Nieuw Amerongen GP, Koolwijk P, van Hinsbergh VW, Groeneveld AB. Angiopoietin-2, permeability oedema, occurrence and severity of ALI/ARDS in septic and non-septic critically ill patients. Thorax 63: 903-909, 2008.
50. Vincent JL. Vasopressin: useful or not? Curr Infect Dis Rep 10: 351-352, 2008
51. Vincent JL, De Backer D. Microvascular dysfunction as a cause of organ dysfunction in severe sepsis. Crit Care 9, Suppl 4: S9-S12, 2005.
52. Westphal M, Enkhbaatar P, Schmalstieg FC, Kulp GA, Traber LD, Morita N, Cox RA, Hawkins HK, Westphal-Varghese BB, Rudloff HE, Maybauer DM, Maybauer MO, Burke AS, Murakami K, Saunders F, Horvath EM, Szabo C, Traber DL. Neuronal nitric oxide synthase inhibition attenuates cardiopulmonary dysfunctions after combined burn and smoke inhalation injury in sheep. Crit Care Med 36: 1196-1204, 2008.
53. Westphal M, Sielenkamper AW, Van Aken H, Stubbe HD, Daudel F, Schepers R, Schulte S, Bone HG. Dopexamine reverses the vasopressinassociated impairment in tissue oxygen supply but decreases systemic blood pressure in ovine endotoxemia. Anesth Analg 99: 878-885, 2004.
54. 1a receptor agonists. J Med Chem 54: 4388-4398, 2011.
55. Yano K, Liaw PC, Mullington JM, Shih SC, Okada H, Bodyak N, Kang PM, Toltl L, Belikoff B, Buras J, Simms BT, Mizgerd JP, Carmeliet P, Karumanchi SA, Aird WC. Vascular endothelial growth factor is an important determinant of sepsis morbidity and mortality. J Exp Med 203: 1447-1458, 2006.