Review: The plasma kallikrein/kinin and renin angiotensin systems in blood pressure regulation in sepsis

Abstract

The hemodynamics of septic shock after endotoxinemiais influenced by the plasma kallikrein/kinin and the renin angiotensin systems. In recent years, new information has improved understanding of the protein/biologically active peptide interactions between these two systems. The plasma kallikrein/kinin system, more commonly known as the contact system, has undergone a re-evaluation as to how it assembles on cell membranes for physiological and pathophysiological activation and as to its role in Gram-negative sepsis. It has been proposed that it counterbalances the plasma renin angiotensin system. Furthermore, more knowledge about the renin angiotensin system has become available on how it either opposes the actions of the kallikrein/kinin system or, in some cases, summates with it. Understanding the interactions between these two systems may lead to development of better pharmacological treatments for endotoxin-induced shock.

Keywords

Kallikrein/kinin renin angiotensin hemodynamics sepsis blood pressure

References

O'Donnell TF , Clowes GH , Talamo RC , Colman RW Kinin activation in the blood of patients with sepsis. Surg Gynecol Obstet 1976; 143: 539-545.

Mason JW , Colman RW The role of Hageman factor in disseminated intravascular coagulationinduced by septicemia, neoplasia, or liver disease. Thromb Diath Haemorrh 1971; 26: 325-331.

Wiggins RC , Cochran CC The autoactivation of rabbit Hageman factor. J Exp Med 1979; 150: 1122-1133.

Miller G. , Silverberg M. , Kaplan AP Autoactivability of human Hageman factor. Biochem Biophys Res Commun 1980; 92: 803-810.

Wachtfogel YT , Harpel PC , Edmunds Jr LH , Colman RW Formation of C1s-C1-inhibitor, kallikrein-C1-inhibitor, and plasmin alpha-2-plasmin inhibitor complexes during cardiopulmonary bypass. Blood 1989; 73: 468-471.

Matsumoto K. , Yamamoto T. , Kamata R. , Maeda H. Pathogenesis of serratial infection: activation of the Hageman factor-prekallikrein cascade by serratial protease. J Biochem 1984 ; 96: 739-749.

Herwald H. , Collie M. , Muller-Esterl W. , Bjorck L. Streptococcal cysteine proteinase release kinins. A novel virulence mechanism . J Exp Med 1996; 184: 665-673.

Greengard JS , Griffin JH Receptors for high molecular weight kininogen on stimulated washed human platelets . Biochemistry 1984; 23: 6863-6869.

Gustafson EJ , Schutsky D. , Knight LC , Schmaier AH High molecular weight kininogen binds to unstimulated platelets. J Clin Invest 1986; 78: 310-318.

10.

Gustafson EJ , Schmaier AH , Wachtfogel YT , Kaufman N. , Kucich U. , Colman RW Human neutrophils contain and bind high molecular weight kininogen. J Clin Invest 1989; 84: 28-35.

11.

Schmaier AH , Kuo A. , Lundberg D. , Murray S. , Cines DB Expression of high molecular weight kininogen on human umbilical vein endothelial cells. J Biol Chem 1988; 263: 16327-16333.

12.

Herwald H. , Dedio J. , Kellner R. , Loos M. , Muller-Esterl W. Isolation and characterization of the kininogen binding protein p33 from endothelial cells. J Biol Chem 1996; 271: 13040-13047.

13.

Joseph K. , Ghebrehiwet B. , Peerschke Eib , Reid Kbn , Kaplan AP Identification of the zinc-dependent endothelial cell binding protein for high molecular weight kininogen and factor XII: identity with the receptor that binds to the globular “heads” of C1q (gC1q-R). Proc Natl Acad Sci USA 1996; 93: 8552-8557.

14.

Colman RW , Pixley RA , Najamunnisa S. , McCrae KR. Binding of high molecular weight kininogen to human endothelial cells is mediated via a site within domains 2 and 3 of the urokinase receptor . J Clin Invest 1997; 100: 1481-1487.

15.

Hasan Aak , Zisman T. , Schmaier AH Identification of cytokeratin 1 as a binding protein and presentation receptor for kininogens on endothelial cells. Proc Natl Acad Sci USA 1998: 95: 3615-3620.

16.

Shariat-Madar Z. , Mahdi F. , Schmaier AH Mapping binding domains of kininogens on endothelial cell cytokeratin 1. J Biol Chem 1999; 274: 7137-7145.

17.

Zhang JC , Donate F. , Qi X. et al. The antiangiogenic activity of cleaved high molecular weight kininogen is mediated through binding to endothelial cell tropomyosin. Proc Natl Acad Sci USA 2002; 99: 12224-12229.

18.

Motta G. , Rojkjaer R. , Hasan Aak , Cines DB , Schmaier AH High molecular weight kininogen regulates prekallikrein assembly and activation on endothelial cells: a novel mechanism for contact activation. Blood 1998; 91: 516-528.

19.

Shariat-Madar Z. , Mahdi F. , Schmaier AH Factor XI assembly and activation on human umbilical vein endothelial cells in culture. Thromb Haemost 2001; 85: 544-551.

20.

Zhao Y. , Qiu Q. , Mahdi F. , Shariat-Madar Z. , Rojkjaer R. , Schmaier AH Assembly and activation of the HK-PK complex on endothelial cells results in bradykininliberation and NO formation. Am J Physiol 2001; 280: H1821-H1829.

21.

Mahdi F. , Shariat-Madar Z. , Figueroa C. , Schmaier AH Factor XII interacts with the multiprotein assembly of urokinase plasminogen activator receptor, gC1qR, and cytokeratin 1 on endothelial cell membranes . Blood 2002; 99: 3585-3596.

22.

Joseph K. , Shibayama Y. , Ghebrehiwet B. , Kaplan AP Factor XIIdependent contact activation on endothelial cells and binding proteins gC1qR and cytokeratin 1. Thromb Haemost 2001 ; 85: 119-124.

23.

Rojkjaer R. , Hasan Aak , Motta G. , Schousboe I. , Schmaier AH Factor XII does not initiate prekallikrein activation on endothelial cells. Thromb Haemost 1998; 80: 74-81.

24.

Motta G. , Shariat-Madar Z. , Mahdi F. , Sampaio Cam , Schmaier AH Assembly and activation of high molecular weight kininogen and prekallikrein on cell matrix. Thromb Haemost 2001; 86: 840-847.

25.

Shariat-Madar Z. , Mahdi F. , Schmaier AH Identification and characterization of prolylcarboxypeptidase as an endothelial cell prekallikrein activator. J Biol Chem 2002; 277: 17962-17969.

26.

Moreira CR , Schmaier AH , Mahdi F. , da Motta G. , Nader HB , Shariat-Madar Z. Identification of prolylcarboxypeptidase as the cell matrix-associated prekallikrein activator. FEBS Lett 2002; 523: 167-170.

27.

Han ED , MacFarlane RC, Mulligan AN , Scafidi J. , Davis AE III. Increased vascular permeability in C1 inhibitor-deficient mice mediated by the bradykinin type 2 receptor. J Clin Invest 2002; 109: 1057-1063.

28.

Erdös EG , Yang Hyt. An enzyme in microsomal fraction of kidney that inactivates bradykinin. Life Sci 1967; 6: 569-574.

29.

Odya CE , MarinkovicDV, Hammon KJ, Stewart TA, Erdös EG. Purification and properties of prolylcarboxypeptidase (angiotensinase C) from human kidney. J Biol Chem 1978; 253: 5927-5931.

30.

Vickers C. , Hales P. , Kaushik V. et al. Hydrolysis of biologic peptides by human angiotensin-converting enzyme-related carboxypeptidase. J Biol Chem 2002; 277: 14838-14843.

31.

Yang Hyt , Erdös EG , Levin Y. A dipeptide carboxypeptidase that converts angiotensin I and inactivates bradykinin . Biochim Biophys Acta 1970; 214: 374-376.

32.

Yang Hyt , Erdös EG , Levin Y. Characterization of a dipeptide hydrolase (kininase II, angiotensin I converting enzyme). J Pharmacol Exp Ther 1971; 177: 291-300.

33.

Hasan Aak , Amenta S. , Schmaier AH Bradykinin and its metabolite, ARG-PRO-PRO-GLY-PHE, are selective inhibitors of a-thrombin-induced platelet activation. Circulation 1996; 94: 517-528.

34.

Hasan Aak , Warnock M. , Nieman M. et al. The mechanisms of Arg-Pro-Pro-Gly-Phe inhibition of thrombin . Am J Physiol 2003; 285: H183-H193.

35.

Bernstein KE Two ACEs and a heart. Nature 2002; 417: 799-802.

36.

Tipnis SR , Hooper NM , Hyde R. , Karran E. , Christie G. , Turner AJ A human homolog of angiotensin-converting enzyme. J Biol Chem 2000; 275: 33238-33243.

37.

Santos Ras , Simoes e Silva A. , Maric C. et al. Angiotensin-(1-7) is an endogenousligand for the G protein-coupled receptor MAS. Proc Natl Acad Sci USA 2003; 100: 8258-8263.

38.

Santos Ras , Passaglio KT , Pesquero JB , Bader M. , Simoes e Silva AC Interactions between angiotensin-(1-7), kinins, and angiotensin II in kidney and blood vessels. Hypertension 2001; 38: 660-664.

39.

Tsutsumi Y. , Matsubara H. , Masaki H. et al. Angiotensin II type 2 receptor overexpression activates the vascular kinin system and causes vasodilation. J Clin Invest 1999; 104: 925-935.

40.

Sealey JE , Atlas SA , Laragh JH Linking the kallikrein and renin systems via activation of inactive renin . New data and a hypothesis. Am J Med 1978 ; 65: 994-1000.

41.

Derkx Fhm , Schalekamp Mpa , Bouma B. , Kluft C, Schalekamp MADH. Plasma kallikrein-mediated activation of the renin-angiotensin system does not require prior acidification of prorenin. J Clin Endocrinol Metab 1982; 54: 343-348.

42.

Siragy HM , Jaffa AA , Margolius HS , Carey RM Renin-angiotensin system modulates renal bradykinin production. Am J Physiol 1996; 271: R1090-R1095.

43.

Siragy HM , Carey RM Protective role of angiotensin AT2 receptor in a renal wrap hypertension model . Hypertension 1999; 33: 1237-1242.

44.

Gohlke P. , Pees C. , Unger T. AT2 receptor stimulation increases aortic cyclic GMP in SHRSP by kinin-dependent mechanisms. Hypertension 1998; 31: 349-355.

45.

Katada J. , Majima M. AT2 receptor-dependent vasodilation is mediated by activation of vascular kinin generation under flow conditions. Br J Pharmacol 2002; 136: 484-491.

46.

AbdAlla S. , Lother H. , El Massiery A. , Quitterer U. Increased AT1 receptor heterodimers in preeclampsia mediate enhanced angiotensin II responsiveness. Nat Med 2001; 7: 1003-1009.

47.

AbdAlla S. , Lother H. , Quitterer U. AT1-receptor heterodimers show enhanced G-protein activation and altered receptor sequestration. Nature 2002; 407: 94-97.

48.

Schmaier AH The kallikrein/kinin and the renin angiotensin systems have a multi-layered interaction. Am J Physiol 2003; 285: R1-R13.

49.

Aird WC The role of the endothelium in severe sepsis and multiple organ dysfunction syndrome. Blood 2003; 101: 3765-3777.

50.

Gailani D. , Broze Jr GJ. Factor XI activation in a revised model of blood coagulation . Science 1991; 253: 909-912.

51.

Colman RW , Mason JW , Sherry S. The kallikreinogen-kallikrein enzyme system of human plasma. Ann Intern Med 1969; 71: 763-773.

52.

Mason JW , Kleeberg U. , Dolan P. , Colman RW Plasma kallikrein and Hageman factor in Gram-negative bacteremia. Ann Intern Med 1970; 73: 545-551.

53.

O'Donnell TF , Clowes Gha , Talamo RC , Colman RW Kinin activation in the blood of patients with sepsis. Surg Gynecol Obstet 1976; 143: 539-545.

54.

Wing DA , Yamada T. , Hayley HB , Pettit GW Model for disseminated intravascular coagulation: bacterial sepsis in rhesus monkeys. J Lab Clin Med 1978; 92: 239-251.

55.

Colman RW , Edelman R. , Scott CF , Cilman RH Plasma kallikrein activation and inhibition during typhoid fever. J Clin Invest 1978; 61: 287-296.

56.

Gallimore MJ , Aasen AO , Lyngaas Khn , Larsbraaten M. , Amundsen E. Falls in plasma levels of prekallikrein, high molecular weight kininogen, and kallikrein inhibitors during lethal endotoxin shock in dogs. Thromb Res 1978; 12: 307-318.

57.

Smith-Erichsen N. , Aasen AO , Gallimore MJ , Amundsen E. Studies of components of the coagulation system in normal individuals and septic shock patients. Circ Shock 1982; 9: 491-497.

58.

Roeise O. , Bouma BN , Stadaas JO , Aasen AO Dose dependence of endotoxin-induced activation of the plasma contact system: an in vitro study. Circ Shock 1988; 26: 419-430.

59.

Schmaier AH , Farber A. , Schein R. , Sprung C. Structural changes of plasma high molecular weight kininogen after in vitro activation and in sepsis. J Lab Clin Med 1988; 112: 182-192.

60.

Nuijens JH , Huijbregts CC , Eerenberg-Belmer Ajm et al. Quantification of plasma factor XIIa-C1 inhibitor and kallikrein-C1 inhibitor complexes in sepsis. Blood 1988; 72: 1841-1848.

61.

Kaufman N. , Page JD , Pixley RA , Schein R. , Schmaier AH , Colman RW α2-Macroglobulin-kallikrein complexes detect contact system activation in hereditary angioedema and human sepsis. Blood 1991; 77: 2660-2667.

62.

Matsumoto K. , Yamamoto T. , Kamata R. , Maeda H. Pathogenesis of serratial infection: activation of the Hageman factor-prekallikrein cascade by serratial protease. J Biochem 1984; 96: 739-749.

63.

Mattsson E. , Herwald H. , Cramer H. , Persson K. , Sjobring U. , Bjorck L. Staphylococcus aureus induces release of bradykinin in human plasma. Infect Immun 2001; 69: 3877-3882.

64.

Sriskandan S. , Kemball-Cook G. , Moyes D. , Canvin J. , Tuddenham E. , Cohen J. Contact activation in shock caused by invasive group A Streptococcus pyogenes. Crit Care Med 2000; 28: 3684-3691.

65.

Fein AM , Bernard GR , Criner GJ et al. Treatment of severe systemic inflammatory response syndrome and sepsis with a novel bradykinin antagonist, deltibant (CP-0127). Results of a randomized, double-blind, placebo-controlled trial. CP-0127 SIRS and Sepsis Study Group. JAMA 1997; 277: 482-487.

66.

Herwald H. , Morgelin M. , Olsen A. et al. Activation of the contact-phase system on bacterial surfaces a clue to serious complications in infectious diseases. Nat Med 1998; 4: 298-302.

67.

Persson K. , Russell W. , Morgelin M. , Herwald H. The conversion of fibrinogen to fibrin at the surface of curliated E. coli bacteria leads to the generation of proinflammatory fibrinopeptides. J Biol Chem 2003; 278: 31884-31890.

68.

Bian Z. , Yan Z-Q. , Hansson GK , Thoren P. , Normark S. Activation of inducible nitric oxide synthase/nitric oxide by curli fibers leads to a fall in blood pressure during systemic Escherichia coli infection in mice. J Infect Dis 2001; 183: 612-619.

69.

Ben Nasr AB , Olsen A. , Sjobring U. , Muller-Esterl W. , Bjorck L. Assembly of human contact phase factors and release of bradykinin at the surface of curli-expressing Escherichia coli . Mol Microbiol 1996; 20: 927-935.

70.

Maeda H. , Wu J. , Okamoto T. , Maruo K. , Akaike T. Kallikreinkinin in infection and cancer. Immunopharmacology 1999; 43: 115-128.

71.

DeLa Cadena R. , Sufffredini AF , Page JD et al. Activation of the kallikrein-kinin system after endotoxin administration to normal human volunteers. Blood 1993; 81: 3313-3317.

72.

Hack CE , Wagstaff J. , Strack van Schijndel M. et al. Studies on the contact system of coagulation during therapy with high doses of recombinant IL-2: implications for septic shock. Thromb Haemost 1991; 65: 497-503.

73.

Oleksowicz L. , Strack M. , Dutcher JP et al. A distinct coagulopathy associated with interleukin-2 therapy. Br J Haematol 1994; 88: 892-894.

74.

Carvalho AC , DeMarinis S. , Scott CF , Silver LD , Schmaier AH , Colman RW Activation of the contact system of plasma proteolysis in the adult respiratory distress syndrome. J Lab Clin Med 1988; 112: 270-277.

75.

Van Der Poll T. , Buller HR , Ten Cate H. et al. Activation of coagulation after administration of tumor necrosis factor to normal subjects. N Engl J Med 1990; 322: 1622-1627.

76.

Pixley RA , DeLa Cadena RA , Page JD et al. Activation of the contact system in lethal hypotensivebacteremia in a baboon model. Am J Pathol 1992; 140: 897-906.

77.

Pixley RA , DeLa Cadena RA , Page JD et al. The contact system contributed to hypotension but not disseminated intravascular coagulation in lethal bacteremia. J Clin Invest 1993; 91: 61-68.

78.

Taylor Jr FB , Chang A. , Ruf W. et al. Lethal E. coli septic shock is prevented by blocking tissue factor with monoclonal antibody. Circ Shock 1991; 33: 127-134.

79.

Hughes B. , Parratt JR The effects of the protease inhibitor, aprotinin, on the course of shock induced by endotoxin in cats. Br J Pharmacol 1985; 86: 399-403.

80.

Svartholm E. , Haglund U. , Ljungberg J. , Hedner U. Influence of aprotinin, a protease inhibitor, on porcine E. coli shock. Studies on coagulation, fibrinolytic and hemodynamic response. Acta Chir Scand 1989; 155: 7-13.

81.

Erdos EG , Massion WH , Downs DR , Gecse A. Effect of the inhibition of angiotensin I converting enzyme in endotoxin and hemorrhagic shock. Proc Soc Exp Biol Med 1974 ; 145: 948-951.

82.

Manson NH , Hess ML Role of angiotensin I and glucagon in canine endotoxin shock: effect of converting enzyme inhibitor and prior immunization. Circ Shock 1984; 12: 177-189.

83.

Gennari R. , Alexander JW , Boyce ST , Lilly N. , Babcock GF , Cornaggia M. Effects of the angiotensin converting enzyme inhibitor enalapril on bacterial translocation after thermal injury and bacterial challenge. Shock 1996; 6: 95-100.

84.

Aneman A. , Pettersson A. , Eisenhofer G. et al. Sympathetic and renin-angiotensin activation during graded hypovolemiain pigs: impact on mesenteric perfusion and duodenal mucosal function. Shock 1997; 8: 378-384.

85.

Yilmaz EN , Vahl AC , van Rij GL et al. The renin-angiotensin system in swine during hypovolaemic shock combined with low-flow ischemia of the sigmoid colon. Cardiovasc Surg 1999; 7: 539-544.

86.

Boldt J. , Papsdorf M. , Kumle B. , Piper S. , Hempelmann G. Influence of angiotensin-converting enzyme inhibitor enalaprilate on endothelial-revived substances in the critically ill. Crit Care Med 1998; 26: 1663-1670.

87.

Hilgenfeldt U. , Kienapfel G. , Kellerman W. , Schott R. , Schmidt M. Renin-angiotensin in sepsis. Clin Exp Theory Practice 1987; A9: 1493-1504.

88.

Schaller MD , Waeber B. , Nussberger J. , Brunner HR Angiotensin II, vasopressin, and sympathetic activity in conscious rats with endotoxemia. Am J Physiol 1985; 249: H1086-H1092.

89.

Baker CH , Sutton ET , Dietz JR Endotoxin alteration of muscle microvascular renin-angiotensin responses. Circ Shock 1992; 36: 224-230.

90.

Dunn CW , Horton JW Role of angiotensin II in neonatal sepsis. Circ Shock 1993; 40: 144-150.

91.

Deitz DM , Swartz KR , Wright M. , Murphy E. , Connell RS , Harrison MW Effects of E. coli endotoxin on rat plasma angiotensin converting enzyme activity in vitro and in vivo. Circ Shock 1987; 21: 23-29.

92.

Wray GM , Coakley JH Severe septic shock unresponsive to noradrenaline. Lancet 1995; 346: 1604.

93.

Yunge M. , Petros A. Angiotensin for septic shock unresponsive to noradrenaline. Arch Dis Child 2000; 82: 388-389.

94.

Tadros T. , Traber DL , Herndon DN Trauma- and sepsis-induced hepatic ischemia and reperfusion injury. Role of angiotensin II. Arch Surg 2000; 135: 766-772.

95.

Nishimura H. , Tsuji H. , Masuda H. et al. Angiotensin II increases plasminogen activator inhibitor-1 and tissue factor mRNA expression without changing that of tissue type plasminogen activator or tissue factor pathway inhibitor in cultured rat aortic endothelial cells. Thromb Haemost 1997; 77: 1189-1195.

96.

Vaughan DE , Lazos SA , Tong K. Angiotensin II regulates the expression of plasminogen activator inhibitor-1 in cultured endothelial cells. J Clin Invest 1995; 96: 2515-2520.

97.

Schmaier AH , Srikanth S. , Elghetany MT et al. Hemostatic/ fibrinolytic protein changes in C3H/HeN mice infected with Rickettsia conorii. Thromb Haemost 2001; 86: 871-879.

98.

Hermans Pwm , Hibberd ML , Booy R. et al. and the Meningococcal Research Group. 4G/5G promoter polymorphism in the plasminogen-activator-inhibitor-1 gene and outcome of meningococcal disease. Lancet 1999; 354: 556-560.

99.

Westendrop Rgj , Hottenga J-J. , Slagboom PE Variation in plasminogen-activator-inhibitor-1 gene and risk of meningococcal septic shock. Lancet 1999; 354: 561-563.

100.

Yasuda S. , Lew Wyw. Angiotensin II exacerbates lipopolysaccharide-induced contractile depression in rabbit cardiac myocytes. Am J Physiol 1999 ; 276: H1442-H1449.

101.

Bucher M. , Hobbhahn J. , Kurtz A. Nitric oxide-dependent downregulation of angiotensin II type 2 receptors during experimental sepsis. Crit Care Med 2001; 29: 1750-1755.

102.

Bucher M. , Ittner K-P. , Hobbhahn J. , Taeger K. , Kurtz A. Downregulation of angiotensin II Type 1 receptors during sepsis. Hypertension 2001; 38: 177-182.

103.

Chan Jyh , Wang L-L. , Ou C-C. , Chan Shh. Downregulation of angiotensin subtype 1 receptor in rostral ventrolateral medulla during endotoxemia. Hypertension 2003 ; 42: 103-109.

104.

Yekebas E. , Treede H. , Jochum M. et al. Bradykinin B2-receptor antagonism attenuates fatal cardiocirculatory breakdown induced by severe experimental pancreatitis . Crit Care Med 2000; 28: 1119-1127.

105.

Janssen HF , Pugh JL , Lange DL Bradykinin does not contribute to hypotension in early canine endotoxemia . Circ Shock 1987; 23: 197-204.

106.

Hallemeesch MM , Cobben Dcp , Soeters PB , Deutz Nep. Differential effects of selective and non-selective NOS inhibition on renal arginine and protein metabolism during endotoxemia in rats. Clin Nutr 2002; 21: 111-117.

107.

Metcalf K. , Jungersten L. , Lisander B. Effective inhibition of nitric oxide production by aminoguanidine does not reverse hypotension in endotoxaemic rats. Acta Anaesth Scand 2002; 46: 17-23.

108.

Suzuki S. , Togari H. , Yamaguchi N. , Mullins K. Nitric oxide inhalation and nitric oxide synthase inhibitor supplement for endotoxin-induced hypotension. Pediatr Int 2001; 43: 343-349.

109.

Minneci P. , Deans K. , Natanson C. , Eichacker PQ Increasing the efficacy of anti-inflammatory agents used in the treatment of sepsis. Eur J Clin Microbiol Infect Dis 2003; 22: 1-9.