Role of plasma kallikrein in diabetes and metabolism

Thrombosis and Haemostasis

Volumn 110, Issue 3, 2013, Pages 434-441

  Feener, Edward P ^a   Zhou, Qunfang ^a   Fickweiler, Ward ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Contact activation pathway; Diabetes; Klkb1; Plasma kallikrein

Indexed keywords

ADVANCED GLYCATION END PRODUCT; BRADYKININ; GLUCAGON LIKE PEPTIDE 1; GLUCOSE; HEMOGLOBIN A1C; KALLIKREIN;

ADIPOGENESIS; ARTICLE; BLOOD CLOTTING; BLOOD PRESSURE REGULATION; BLOOD VESSEL PERMEABILITY; DIABETES MELLITUS; DIABETIC RETINOPATHY; GENETIC ANALYSIS; GENETIC ASSOCIATION; HEMOSTASIS; HUMAN; HYPERGLYCEMIA; HYPERTENSION; INFLAMMATION; NONHUMAN; PARTIAL THROMBOPLASTIN TIME; PHYSIOLOGY; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; THROMBOCYTE AGGREGATION; THROMBOSIS; VASCULAR ENDOTHELIUM;

ADIPOGENESIS; ANIMALS; BLOOD COAGULATION; BLOOD PRESSURE; BRADYKININ; DIABETES MELLITUS; FACTOR XII; GENE EXPRESSION REGULATION; GENETIC VARIATION; GLUCOSE; HEMOSTASIS; HUMANS; HYPERTENSION; INFLAMMATION; MICE; PLASMA KALLIKREIN; PREKALLIKREIN; THROMBOSIS;

EID: 84883258857     PISSN: 03406245     EISSN: None     Source Type: Journal    
DOI: 10.1160/TH13-02-0179     Document Type: Article

References (90)

1. Sainz IM, Pixley RA, Colman RW. Fifty years of research on the plasma kallikrein-kinin system: from protein structure and function to cell biology and in-vivo pathophysiology. Thromb Haemost 2007; 98: 77-83.
2. Neth P, Arnhold M, Nitschko H, et al. The mRNAs of prekallikrein, factors XI and XII, and kininogen, components of the contact phase cascade are differentially expressed in multiple non-hepatic human tissues. Thromb Haemost 2001; 85: 1043-1047.
3. Fink E, Bhoola KD, Snyman C, et al. Cellular expression of plasma prekallikrein in human tissues. Biol Chem 2007; 388: 957-963.
4. Peek M, Moran P, Mendoza N, et al. Unusual proteolytic activation of pro-hepatocyte growth factor by plasma kallikrein and coagulation factor XIa. J Biol Chem 2002; 277: 47804-4789.
5. Renne T, Dedio J, Meijers JC, et al. Mapping of the discontinuous H-kininogen binding site of plasma prekallikrein. Evidence for a critical role of apple domain-2. J Biol Chem 1999; 274: 25777-25784.
6. Harpel PC. Studies on the interaction between collagen and a plasma kallikreinlike activity. Evidence for a surface-active enzyme system. J Clin Invest 1972; 51: 1813-1822.
7. Liu J, Gao BB, Clermont AC, et al. Hyperglycemia-induced cerebral hematoma expansion is mediated by plasma kallikrein. Nat Med 2011; 206-210.
8. Marceau F, Regoli D. Bradykinin receptor ligands: therapeutic perspectives. Nat Rev Drug Discov 2004; 3: 845-852.
9. Iwaki T, Castellino FJ. Plasma levels of bradykinin are suppressed in factor XIIdeficient mice. Thromb Haemost 2006; 95: 1003-1010.
10. Maas C, Renne T. Regulatory mechanisms of the plasma contact system. Thromb Res 2012; 129 (Suppl 2): S73-S76.
11. White-Adams TC, Berny MA, Patel IA, et al. Laminin promotes coagulation and thrombus formation in a factor XII-dependent manner. J Thromb Haemost 2010; 8: 1295-1301.
12. Van Der Meijden PE, Munnix IC, Auger JM, et al. Dual role of collagen in factor XII-dependent thrombus formation. Blood 2009; 114: 881-890.
13. Oschatz C, Maas C, Lecher B, et al. Mast cells increase vascular permeability by heparin-initiated bradykinin formation in vivo. Immunity 2011; 34: 258-268.
14. Muller F, Mutch NJ, Schenk WA, et al. Platelet polyphosphates are proinflammatory and procoagulant mediators in vivo. Cell 2009; 139: 1143-1156.
15. Cicardi M, Levy RJ, McNeil DL, Li HH, Sheffer AL, Campion M, et al. Ecallantide for the treatment of acute attacks in hereditary angioedema. N Engl J Med 2010; 363: 523-531.
16. Girolami A, Scarparo P, Candeo N, Lombardi AM. Congenital prekallikrein deficiency. Expert Rev Hematol 2010; 3: 685-695.
17. Bird JE, Smith PL, Wang X, et al. Effects of plasma kallikrein deficiency on haemostasis and thrombosis in mice: murine ortholog of the Fletcher trait. Thromb Haemost 2012; 107: 1141-1150.
18. Yu H, Anderson PJ, Freedman BI, et al. Genomic structure of the human plasma prekallikrein gene, identification of allelic variants, and analysis in end-stage renal disease. Genomics 2000; 69: 225-234.
19. Katsuda I, Maruyama F, Ezaki K, et al. A new type of plasma prekallikrein deficiency associated with homozygosity for Gly104Arg and Asn124Ser in apple domain 2 of the heavy-chain region. Eur J Haematol 2007; 79: 59-68.
20. Verweij N, Mahmud H, Mateo L, et al. Genome-wide association study on plasma levels of midregional-proadrenomedullin and C-terminal-pro-endothelin-1. Hypertension 2013; 61: 602-608.
21. Comuzzie AG, Cole SA, Laston SL, et al. Novel genetic loci identified for the pathophysiology of childhood obesity in the Hispanic population. PLoS One 2012; 7: e51954.
22. Suhre K, Shin SY, Petersen AK, et al. Human metabolic individuality in biomedical and pharmaceutical research. Nature 2011; 477: 54-60.
23. Kettunen J, Tukiainen T, Sarin AP, et al. Genome-wide association study identifies multiple loci influencing human serum metabolite levels. Nat Genet 2012; 44: 269-276.
24. Austin H, De Staercke C, Lally C, et al. New gene variants associated with venous thrombosis: a replication study in White and Black Americans. J Thromb Haemost 2011; 9: 489-495.
25. Heit JA, Cunningham JM, Petterson TM, et al. Genetic variation within the anticoagulant, procoagulant, fibrinolytic and innate immunity pathways as risk factors for venous thromboembolism. J Thromb Haemost 2011; 9: 1133-1142.
26. Revenko AS, Gao D, Crosby JR, et al. Selective depletion of plasma prekallikrein or coagulation factor XII inhibits thrombosis in mice without increased risk of bleeding. Blood 2011; 118: 5302-5311.
27. Gaunt TR, Lowe GD, Lawlor DA, et al. A gene-centric analysis of activated partial thromboplastin time and activated protein C resistance using the HumanCVD focused genotyping array. Eur J Hum Genet 2012; Epub ahead of print.
28. Lippi G, Franchini M, Targher G, et al. Epidemiological association between fasting plasma glucose and shortened APTT. Clin Biochem 2009; 42: 118-120.
29. Zhao Y, Zhang J, Zhang J, et al. Diabetes mellitus is associated with shortened activated partial thromboplastin time and increased fibrinogen values. PLoS One 2011; 6: e16470.
30. Patrassi GM, Vettor R, Padovan D, et al. Contact phase of blood coagulation in diabetes mellitus. Eur J Clin Invest 1982; 12: 307-311.
31. Kedzierska K, Ciechanowski K, Golembiewska E, et al. Plasma prekallikrein as a risk factor for diabetic retinopathy. Arch Med Res 2005; 36: 539-543.
32. Federspil G, Vettor R, De Palo E, et al. Plasma kallikrein activity in human diabetes mellitus. Metabolism 1983; 32: 540-542.
33. Clermont A, Chilcote TJ, Kita T, et al. Plasma kallikrein mediates retinal vascular dysfunction and induces retinal thickening in diabetic rats. Diabetes 2011; 60: 1590-1598.
34. Nobukata H, Ishikawa T, Obata M, et al. Long-term administration of highly purified eicosapentaenoic acid ethyl ester prevents diabetes and abnormalities of blood coagulation in male WBN/Kob rats. Metabolism 2000; 49: 912-919.
35. Vazzana N, Ranalli P, Cuccurullo C, et al. Diabetes mellitus and thrombosis. Thromb Res 2012; 129: 371-377.
36. Kimura K, Iguchi Y, Inoue T, et al. Hyperglycemia independently increases the risk of early death in acute spontaneous intracerebral hemorrhage. J Neurol Sci 2007; 255: 90-94.
37. Yau JW, Rogers SL, Kawasaki R, et al. Global prevalence and major risk factors of diabetic retinopathy. Diabetes Care 2012; 35: 556-564.
38. Liu J, Feener EP. Plasma kallikrein-kinin system and diabetic retinopathy. Biol Chem 2013; 394: 319-328.
39. Liu J, Clermont AC, Gao BB, et al. Intraocular Hemorrhage Causes Retinal Vascular Dysfunction via Plasma Kallikrein. Invest Ophthalmol Vis Sci 2013; 54: 1086-1094.
40. Phipps JA, Clermont AC, Sinha S, et al. Plasma kallikrein mediates angiotensin II type 1 receptor-stimulated retinal vascular permeability. Hypertension 2009; 53: 175-181.
41. Joseph K, Kaplan AP. Formation of bradykinin: a major contributor to the innate inflammatory response. Adv Immunol 2005; 86: 159-208.
42. Wende AR, Soto J, Olsen CD, et al. Loss of bradykinin signaling does not accelerate the development of cardiac dysfunction in type 1 diabetic akita mice. Endocrinology 2010; 151: 3536-3542.
43. Kakoki M, Sullivan KA, Backus C, et al. Lack of both bradykinin B1 and B2 receptors enhances nephropathy, neuropathy, and bone mineral loss in Akita diabetic mice. Proc Natl Acad Sci USA 2010; 107: 10190-10195.
44. Barros CC, Haro A, Russo FJ, et al. Altered glucose homeostasis and hepatic function in obese mice deficient for both kinin receptor genes. PLoS One 2012; 7: e40573.
45. Mori MA, Araujo RC, Reis FC, et al. Kinin B1 receptor deficiency leads to leptin hypersensitivity and resistance to obesity. Diabetes 2008; 57: 1491-1500.
46. Fischman AJ, Wildey GM, Matsueda GR, et al. Specificity of serine proteases for cleavage sites on proatrial natriuretic factor. Peptides 1988; 9: 1275-1283.
47. Metters KM, Rossier J, Paquin J, et al. Selective cleavage of proenkephalin-derived peptides (less than 23,300 daltons) by plasma kallikrein. J Biol Chem 1988; 263: 12543-12553.
48. Ichinose A, Fujikawa K, Suyama T. The activation of pro-urokinase by plasma kallikrein and its inactivation by thrombin. J Biol Chem 1986; 261: 3486-3489.
49. Liu J, Gao BB, Feener EP. Proteomic identification of novel plasma kallikrein substrates in the astrocyte secretome. Translational Stroke Res 2010; 1: 276-286.
50. Dong JZ, Shen Y, Zhang J, et al. Discovery and characterization of taspoglutide, a novel analogue of human glucagon-like peptide-1, engineered for sustained therapeutic activity in type 2 diabetes. Diabetes Obes Metab 2011; 13: 19-25.
51. Abid K, Rochat B, Lassahn PG, et al. Kinetic study of neuropeptide Y (NPY) proteolysis in blood and identification of NPY3-35: a new peptide generated by plasma kallikrein. J Biol Chem 2009; 284: 24715-24724.
52. Deacon CF, Johnsen AH, Holst JJ. Degradation of glucagon-like peptide-1 by human plasma in vitro yields an N-terminally truncated peptide that is a major endogenous metabolite in vivo. J Clin Endocrinol Metab 1995; 80: 952-957.
53. Drucker DJ, Nauck MA. The incretin system: glucagon-like peptide-1 receptor agonists and dipeptidyl peptidase-4 inhibitors in type 2 diabetes. Lancet 2006; 368: 1696-1705.
54. Sebokova E, Christ AD, Wang H, et al. Taspoglutide, an analog of human glucagon-like Peptide-1 with enhanced stability and in vivo potency. Endocrinology 2010; 151: 2474-2482.
55. Gefel D, Hendrick GK, Mojsov S, et al. Glucagon-like peptide-I analogs: effects on insulin secretion and adenosine 3',5'-monophosphate formation. Endocrinology 1990; 126: 2164-2168.
56. Rosenstock J, Balas B, Charbonnel B, et al. The Fate of Taspoglutide, a Weekly GLP-1 Receptor Agonist, Versus Twice-Daily Exenatide for Type 2 Diabetes: The T-Emerge 2 Trial. Diabetes Care 2012; Epub ahead of print.
57. Selvarajan S, Lund LR, Takeuchi T, et al. A plasma kallikrein-dependent plasminogen cascade required for adipocyte differentiation. Nat Cell Biol 2001; 3: 267-275.
58. Lilla JN, Joshi RV, Craik CS, et al. Active plasma kallikrein localizes to mast cells and regulates epithelial cell apoptosis, adipocyte differentiation, and stromal remodeling during mammary gland involution. J Biol Chem 2009; 284: 13792-13803.
59. Lund LR, Green KA, Stoop AA, et al. Plasminogen activation independent of uPA and tPA maintains wound healing in gene-deficient mice. EMBO J 2006; 25: 2686-2697.
60. Gao BB, Clermont A, Rook S, et al. Extracellular carbonic anhydrase mediates hemorrhagic retinal and cerebral vascular permeability through prekallikrein activation. Nat Med 2007; 13: 181-188.
61. Maas C, Govers-Riemslag JW, Bouma B, et al. Misfolded proteins activate factor XII in humans, leading to kallikrein formation without initiating coagulation. J Clin Invest 2008; 118: 3208-3218.
62. Gao BB, Chen X, Timothy N, et al. Characterization of the vitreous proteome in diabetes without diabetic retinopathy and diabetes with proliferative diabetic retinopathy. J Proteome Res 2008; 7: 2516-2525.
63. Borissoff JI, Heeneman S, Kilinc E, et al. Early atherosclerosis exhibits an enhanced procoagulant state. Circulation 2010; 122: 821-830.
64. Yan SF, Ramasamy R, Schmidt AM. Mechanisms of disease: advanced glycation end-products and their receptor in inflammation and diabetes complications. Nat Clin Pract Endocrinol Metab 2008; 4: 285-293.
65. Kaji Y, Usui T, Ishida S, et al. Inhibition of diabetic leukostasis and blood-retinal barrier breakdown with a soluble form of a receptor for advanced glycation end products. Invest Ophthalmol Vis Sci 2007; 48: 858-865.
66. Yin W, Ghebrehiwet B, Peerschke EI. Expression of complement components and inhibitors on platelet microparticles. Platelets 2008; 19: 225-233.
67. Van Der Meijden PE, Van Schilfgaarde M, van Oerle R, et al. Platelet-and erythrocyte-derived microparticles trigger thrombin generation via factor XIIa. J Thromb Haemost 2012; 10: 1355-1362.
68. Aleman MM, Gardiner C, Harrison P, et al. Differential contributions of monocyte-and platelet-derived microparticles towards thrombin generation and fibrin formation and stability. J Thromb Haemost 2011; 9: 2251-2261.
69. Nieuwland R, Berckmans RJ, Rotteveel-Eijkman RC, et al. Cell-derived microparticles generated in patients during cardiopulmonary bypass are highly procoagulant. Circulation 1997; 96: 3534-3541.
70. Owens AP, III, Mackman N. Microparticles in hemostasis and thrombosis. Circ Res 2011; 108: 1284-1297.
71. Sabatier F, Darmon P, Hugel B, et al. Type 1 and type 2 diabetic patients display different patterns of cellular microparticles. Diabetes 2002; 51: 2840-2845.
72. Alkhatatbeh MJ, Mhaidat NM, Enjeti AK, et al. The putative diabetic plasma marker, soluble CD36, is non-cleaved, non-soluble and entirely associated with microparticles. J Thromb Haemost 2011; 9: 844-851.
73. Ueba T, Haze T, Sugiyama M, et al. Level, distribution and correlates of plateletderived microparticles in healthy individuals with special reference to the metabolic syndrome. Thromb Haemost 2008; 100: 280-285.
74. Goichot B, Grunebaum L, Desprez D, et al. Circulating procoagulant microparticles in obesity. Diabetes Metab 2006; 32: 82-85.
75. Murakami T, Horigome H, Tanaka K, et al. Impact of weight reduction on production of platelet-derived microparticles and fibrinolytic parameters in obesity. Thromb Res 2007; 119: 45-53.
76. Preston RA, Jy W, Jimenez JJ, et al. Effects of severe hypertension on endothelial and platelet microparticles. Hypertension 2003; 41: 211-217.
77. Nomura S, Inami N, Shouzu A, et al. Correlation and association between plasma platelet-, monocyte-and endothelial cell-derived microparticles in hypertensive patients with type 2 diabetes mellitus. Platelets 2009; 20: 406-414.
78. Ogata N, Imaizumi M, Nomura S, et al. Increased levels of platelet-derived microparticles in patients with diabetic retinopathy. Diabetes Res Clin Pract 2005; 68: 193-201.
79. Chahed S, Leroyer AS, Benzerroug M, et al. Increased vitreous shedding of microparticles in proliferative diabetic retinopathy stimulates endothelial proliferation. Diabetes 2010; 59: 694-701.
80. Tan KT, Tayebjee MH, Lim HS, et al. Clinically apparent atherosclerotic disease in diabetes is associated with an increase in platelet microparticle levels. Diabet Med 2005; 22: 1657-1662.
81. Tsimerman G, Roguin A, Bachar A, et al. Involvement of microparticles in diabetic vascular complications. Thromb Haemost 2011; 106: 310-321.
82. Howard MA, Coghlan M, David R, et al. Coagulation activities of plasma microparticles. Thromb Res 1988; 50: 145-156.
83. Pixley RA, Espinola RG, Ghebrehiwet B, et al. Interaction of high-molecularweight kininogen with endothelial cell binding proteins suPAR, gC1qR and cytokeratin 1 determined by surface plasmon resonance (BiaCore). Thromb Haemost 2011; 105: 1053-1059.
84. Joseph K, Ghebrehiwet B, Kaplan AP. Activation of the kinin-forming cascade on the surface of endothelial cells. Biol Chem 2001; 382: 71-75.
85. 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.
86. Bossi F, Fischetti F, Regoli D, et al. Novel pathogenic mechanism and therapeutic approaches to angioedema associated with C1 inhibitor deficiency. J Allergy Clin Immunol 2009; 124: 1303-1310.
87. Zhu L, Carretero OA, Xu J, et al. Angiotensin II type 2 receptor-stimulated activation of plasma prekallikrein and bradykinin release: role of SHP-1. Am J Physiol Heart Circ Physiol 2012; 302: H2553-H2559.
88. 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.
89. Campbell DJ, Krum H, Esler MD. Losartan increases bradykinin levels in hypertensive humans. Circulation 2005; 111: 315-320.
90. de Maat S, van Dooremalen S, de Groot PG, et al. A nanobody-based method for tracking factor XII activation in plasma. Thromb Haemost 2013; 110: 458-468.