Plasma kallikrein-kinin system and diabetic retinopathy

Biological Chemistry

Volumn 394, Issue 3, 2013, Pages 319-328

  Liu, Jia ^a   Feener, Edward P ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

bradykinin receptor; diabetic retinopathy; plasma kallikrein kinin system; retina; vascular permeability

Indexed keywords

1 BENZYL 1H PYRAZOLE 4 CARBOXYLIC ACID 4 CARBAMIMIDOYL BENZYLAMIDE; ASP 440; BLOOD CLOTTING FACTOR 12; BRADYKININ ANTAGONIST; BRADYKININ B1 RECEPTOR; BRADYKININ B2 RECEPTOR; COMPLEMENT COMPONENT C1S INHIBITOR; FOV 2304; KININ; PLASMA KALLIKREIN; R 954; SAFOTIBANT; SERINE PROTEINASE INHIBITOR; UNCLASSIFIED DRUG; VASOACTIVE AGENT;

ANGIOGENESIS; BLOOD VESSEL PERMEABILITY; DIABETIC RETINOPATHY; DISEASE COURSE; ENZYME ACTIVATION; ENZYME BLOOD LEVEL; ENZYME INHIBITION; HUMAN; INFLAMMATION; KALLIKREIN KININ SYSTEM; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; RETINA BLOOD FLOW; REVIEW; UPREGULATION; VASODILATATION;

BLOOD CHEMICAL ANALYSIS; DIABETIC RETINOPATHY; HUMANS; KALLIKREIN-KININ SYSTEM; PLASMA; RETINAL NEOVASCULARIZATION;

ANIMALIA; RATTUS; RODENTIA;

EID: 84876584591     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2012-0316     Document Type: Review

References (77)

1. Abdouh, M., Khanjari, A., Abdelazziz, N., Ongali, B., Couture, R., and Hassessian, H.M. (2003). Early upregulation of kinin B1 receptors in retinal microvessels of the streptozotocin-diabetic rat. Br. J. Pharmacol. 140, 33-40.
2. Abdouh, M., Talbot, S., Couture, R., and Hassessian, H.M. (2008). Retinal plasma extravasation in streptozotocin-diabetic rats mediated by kinin B(1) and B(2) receptors. Br. J. Pharmacol. 154, 136-143.
3. Antonetti, D.A., Klein, R., and Gardner, T.W. (2012). Diabetic retinopathy. N. Engl. J. Med. 366, 1227-1239.
4. Austinat, M., Braeuninger, S., Pesquero, J.B., Brede, M., Bader, M., Stoll, G., Renne, T., and Kleinschnitz, C. (2009). Blockade of bradykinin receptor B1 but not bradykinin receptor B2 provides protection from cerebral infarction and brain edema. Stroke 40, 285-293.
5. Bird, J.E., Smith, P.L., Wang, X., Schumacher, W.A., Barbera, F., Revelli, J.P., and Seiffert, D. (2012). Effects of plasma kallikrein deficiency on haemostasis and thrombosis in mice: Murine ortholog of the Fletcher trait. Thromb. Haemost. 107, 1141-1150.
6. Brovkovych, V., Zhang, Y., Brovkovych, S., Minshall, R.D., and Skidgel, R.A. (2011). A novel pathway for receptor-mediated post-translational activation of inducible nitric oxide synthase. J. Cell. Mol. Med. 15, 258-269.
7. Busse, R. and Fleming, I. (1996). Molecular responses of endothelial tissue to kinins. Diabetes 45 (Suppl 1), S8-13.
8. Catanzaro, O., Labal, E., Andornino, A., Capponi, J.A., Di Martino, I., and Sirois, P (2012). Blockade of early and late retinal biochemical alterations associated with diabetes development by the selective bradykinin B1 receptor antagonist R-954. Peptides 34, 349-352.
9. Cheung, N., Mitchell, P., and Wong, T.Y. (2010). Diabetic retinopathy. Lancet 376, 124-136.
10. Cicardi, M., Banerji, A., Bracho, F., Malbran, A., Rosenkranz, B., Riedl, M., Bork, K., Lumry, W., Aberer, W., Bier, H., et al. (2010a). Icatibant, a new bradykinin-receptor antagonist, in hereditary angioedema. N. Engl. J. Med. 363, 532-541.
11. Cicardi, M., Levy, R.J., McNeil, D.L., Li, H.H., Sheffer, A.L., Campion, M., Horn, P.T., and Pullman, W.E. (2010b). Ecallantide for the treatment of acute attacks in hereditary angioedema. N. Engl. J. Med. 363, 523-531.
12. Clermont, A., Chilcote, T.J., Kita, T., Liu, J., Riva, P., Sinha, S., and Feener, E.P. (2011). Plasma kallikrein mediates retinal vascular dysfunction and induces retinal thickening in diabetic rats. Diabetes 60, 1590-1598.
13. Dalsgaard, T., Kroigaard, C., Misfeldt, M., Bek, T., and Simonsen, U. (2010). Openers of small conductance calcium-activated potassium channels selectively enhance NO-mediated bradykinin vasodilatation in porcine retinal arterioles. Br. J. Pharmacol. 160, 1496-1508.
14. Ehrenfeld, P., Millan, C., Matus, C.E., Figueroa, J.E., Burgos, R.A., Nualart, F., Bhoola, K.D., and Figueroa, C.D. (2006). Activation of kinin B1 receptors induces chemotaxis of human neutrophils. J. Leukoc. Biol. 80, 117-124.
15. Gao, B.B., Clermont, A., Rook, S., Fonda, S.J., Srinivasan, V.J., Wojtkowski, M., Fujimoto, J.G., Avery, R.L., Arrigg, P.G., Bursell, S.E., et al. (2007). Extracellular carbonic anhydrase mediates hemorrhagic retinal and cerebral vascular permeability through prekallikrein activation. Nat. Med. 13, 181-188.
16. Gao, B.B., Chen, X., Timothy, N., Aiello, L.P., and Feener, E.P. (2008). Characterization of the vitreous proteome in diabetes without diabetic retinopathy and diabetes with proliferative diabetic retinopathy. J. Proteome Res. 7, 2516-2525.
17. Giles, T.D., Sander, G.E., Nossaman, B.D., and Kadowitz, P.J. (2012). Impaired vasodilation in the pathogenesis of hypertension: Focus on nitric oxide, endothelial-derived hyperpolarizing factors, and prostaglandins. J. Clin. Hypertens. 14, 198-205.
18. Girolami, A., Scarparo, P., Candeo, N., and Lombardi, A.M. (2010). Congenital prekallikrein deficiency. Exp. Rev. Hematol. 3, 685-695.
19. Guo, Y.L. and Colman, R.W. (2005). Two faces of high-molecularweight kininogen (HK) in angiogenesis: Bradykinin turns it on and cleaved HK (HKa) turns it off. J. Thromb. Haemost. 3, 670-676.
20. Hardy, P., Abran, D., Hou, X., Lahaie, I., Peri, K.G., Asselin, P., Varma, D.R., and Chemtob, S. (1998). A major role for prostacyclin in nitric oxide-induced ocular vasorelaxation in the piglet. Circ. Res. 83, 721-729.
21. Huang, H., Gandhi, J.K., Zhong, X., Wei, Y., Gong, J., Duh, E.J., and Vinores, S.A. (2011). TNFalpha is required for late BRB breakdown in diabetic retinopathy, and its inhibition prevents leukostasis and protects vessels and neurons from apoptosis. Invest. Ophthalmol. Vis. Sci. 52, 1336-1344.
22. Ifuku, M., Farber, K., Okuno, Y., Yamakawa, Y., Miyamoto, T., Nolte, C., Merrino, V.F., Kita, S., Iwamoto, T., Komuro, I., et al. (2007). Bradykinin-induced microglial migration mediated by B1-bradykinin receptors depends on Ca 2 + influx via reverse-mode activity of the Na + /Ca 2 + exchanger. J. Neurosci. 27, 13065-13073.
23. Jacobi, P.C., Osswald, H., and Zrenner, E. (1996). Bradykinin receptor inhibition affects the rod b-wave in the cat electroretinogram. Vision Res. 36, 3843-3849.
24. Jeppesen, P., Aalkjaer, C., and Bek, T. (2002). Bradykinin relaxation in small porcine retinal arterioles. Invest. Ophthalmol. Vis. Sci. 43, 1891-1896.
25. Joseph, K. and Kaplan, A.P. (2005). Formation of bradykinin: A major contributor to the innate inflammatory response. Adv. Immunol. 86, 159-208.
26. Joseph, K., Tholanikunnel, B.G., and Kaplan, A.P. (2002). Heat shock protein 90 catalyzes activation of the prekallikrein-kininogen complex in the absence of factor XII. Proc. Natl. Acad. Sci. USA 99, 896-900.
27. Joussen, A.M., Poulaki, V., Le, M.L., Koizumi, K., Esser, C., Janicki, H., Schraermeyer, U., Kociok, N., Fauser, S., Kirchhof, B., et al. (2004). A central role for inflammation in the pathogenesis of diabetic retinopathy. FASEB J. 18, 1450-1452.
28. Kedzierska, K., Ciechanowski, K., Golembiewska, E., Safranow, K., Ciechanowicz, A., Domanski, L., Myslak, M., and Rozanski, J. (2005). Plasma prekallikrein as a risk factor for diabetic retinopathy. Arch. Med. Res. 36, 539-543.
29. Kim, T., Kim, S.J., Kim, K., Kang, U.B., Lee, C., Park, K.S., Yu, H.G., and Kim, Y. (2007). Profiling of vitreous proteomes from proliferative diabetic retinopathy and nondiabetic patients. Proteomics 7, 4203-4215.
30. Kim, K., Kim, S.J., Yu, H.G., Yu, J., Park, K.S., Jang, I.J., and Kim, Y. (2010). Verification of biomarkers for diabetic retinopathy by multiple reaction monitoring. J. Proteome Res. 9, 689-699.
31. Ko, F., Vitale, S., Chou, C.F., Cotch, M.F., Saaddine, J., and Friedman, D.S. (2012). Prevalence of nonrefractive visual impairment in US adults and associated risk factors, 1999-2002 and 2005-2008. JAMA 308, 2361-2368.
32. Kojima, N., Saito, M., Mori, A., Sakamoto, K., Nakahara, T., and Ishii, K. (2009). Role of cyclooxygenase in vasodilation of retinal blood vessels induced by bradykinin in Brown Norway rats. Vasc. Pharmacol. 51, 119-124.
33. Kolte, D., Osman, N., Yang, J., and Shariat-Madar, Z. (2011). High molecular weight kininogen activates B2 receptor signaling pathway in human vascular endothelial cells. J. Biol. Chem. 286, 24561-24571.
34. Krankel, N., Katare, R.G., Siragusa, M., Barcelos, L.S., Campagnolo, P., Mangialardi, G., Fortunato, O., Spinetti, G., Tran, N., Zacharowski, K., et al. (2008). Role of kinin B2 receptor signaling in the recruitment of circulating progenitor cells with neovascularization potential. Circ. Res. 103, 1335-1343.
35. Kuhr, F., Lowry, J., Zhang, Y., Brovkovych, V., and Skidgel, R.A. (2010). Differential regulation of inducible and endothelial nitric oxide synthase by kinin B1 and B2 receptors. Neuropeptides 44, 145-154.
36. Langhauser, F., Gob, E., Kraft, P., Geis, C., Schmitt, J., Brede, M., Gobel, K., Helluy, X., Pham, M., Bendszus, M., et al. (2012). Kininogen deficiency protects from ischemic neurodegeneration in mice by reducing thrombosis, blood-brain-barrier damage and inflammation. Blood 120, 4082-4092.
37. Lawson, S.R., Gabra, B.H., Guerin, B., Neugebauer, W., Nantel, F., Battistini, B., and Sirois, P. (2005). Enhanced dermal and retinal vascular permeability in streptozotocin-induced type 1 diabetes in Wistar rats: Blockade with a selective bradykinin B1 receptor antagonist. Regul. Pept. 124, 221-224.
38. Lecleire-Collet, A., Audo, I., Aout, M., Girmens, J.F., Sofroni, R., Erginay, A., Le Gargasson, J.F., Mohand-Said, S., Meas, T., Guillausseau, P.J., et al. (2011). Evaluation of retinal function and flicker light-induced retinal vascular response in normotensive patients with diabetes without retinopathy. Invest. Ophthalmol. Vis. Sci. 52, 2861-2867.
39. Lim, S.K., Han, H.J., Kim, K.Y., and Park, S.H. (2009). Both B1R and B2R act as intermediate signaling molecules in high glucoseinduced stimulation of glutamate uptake in ARPE cells. J. Cell. Physiol. 221, 677-687.
40. Lippi, G., Franchini, M., Targher, G., Montagnana, M., Salvagno, G.L., Guidi, G.C., and Favaloro, E.J. (2009). Epidemiological association between fasting plasma glucose and shortened APTT. Clin. Biochem. 42, 118-120.
41. Liu, B., Linley, J.E., Du, X., Zhang, X., Ooi, L., Zhang, H., and Gamper, N. (2010a). The acute nociceptive signals induced by bradykinin in rat sensory neurons are mediated by inhibition of M-type K + channels and activation of Ca 2 + -activated Clchannels. J. Clin. Invest. 120, 1240-1252.
42. Liu, J., Gao, B-B., and Feener, E. (2010b). Proteomic identification of novel plasma kallikrein substrates in the astrocyte secretome. Transl. Stroke Res. 1, 276-286.
43. Liu, J., Gao, B.B., Clermont, A.C., Blair, P., Chilcote, T.J., Sinha, S., Flaumenhaft, R., and Feener, E.P. (2011). Hyperglycemiainduced cerebral hematoma expansion is mediated by plasma kallikrein. Nat. Med. 17, 206-210.
44. Longhurst, H. and Cicardi, M. (2012). Hereditary angio-oedema. Lancet 379, 474-481.
45. Ma, J.X., Song, Q., Hatcher, H.C., Crouch, R.K., Chao, L., and Chao, J. (1996). Expression and cellular localization of the kallikreinkinin system in human ocular tissues. Exp. Eye Res. 63, 19-26.
46. Maas, C., Govers-Riemslag, J.W., Bouma, B., Schiks, B., Hazenberg, B.P., Lokhorst, H.M., Hammarstrom, P., ten Cate, H., de Groot, P.G., Bouma, B.N., et al. (2008). Misfolded proteins activate factor XII in humans, leading to kallikrein formation without initiating coagulation. J. Clin. Invest. 118, 3208-3218.
47. Mizumura, K., Sugiura, T., Katanosaka, K., Banik, R.K., and Kozaki, Y. (2009). Excitation and sensitization of nociceptors by bradykinin: What do we know ? Exp. Brain Res. 196, 53-65.
48. Mohamed, Q., Gillies, M.C., and Wong, T.Y. (2007). Management of diabetic retinopathy: A systematic review. J. Am. Med. Assoc. 298, 902-916.
49. Muller, F., Mutch, N.J., Schenk, W.A., Smith, S.A., Esterl, L., Spronk, H.M., Schmidbauer, S., Gahl, W.A., Morrissey, J.H., and Renne, T. (2009). Platelet polyphosphates are proinflammatory and procoagulant mediators in vivo. Cell 139, 1143-1156.
50. Nakamura, S., Morimoto, N., Tsuruma, K., Izuta, H., Yasuda, Y., Kato, N., Ikeda, T., Shimazawa, M., and Hara, H. (2011). Tissue kallikrein inhibits retinal neovascularization via the cleavage of vascular endothelial growth factor-165. Arterioscler. Thromb. Vasc. Biol. 31, 1041-1048.
51. Orsenigo, F., Giampietro, C., Ferrari, A., Corada, M., Galaup, A., Sigismund, S., Ristagno, G., Maddaluno, L., Young Koh, G., Franco, D., et al. (2012). Phosphorylation of VE-cadherin is modulated by haemodynamic forces and contributes to the regulation of vascular permeability in vivo. Nat. Commun. 3, 1208.
52. Oschatz, C., Maas, C., Lecher, B., Jansen, T., Bjorkqvist, J., Tradler, T., Sedlmeier, R., Burfeind, P., Cichon, S., Hammerschmidt, S., et al. (2011). Mast cells increase vascular permeability by heparin-initiated bradykinin formation in vivo. Immunity 34, 258-268.
53. Parenti, A., Morbidelli, L., Ledda, F., Granger, H.J., and Ziche, M. (2001). The bradykinin/B1 receptor promotes angiogenesis by up-regulation of endogenous FGF-2 in endothelium via the nitric oxide synthase pathway. FASEB J. 15, 1487-1489.
54. Parpura, V., Basarsky, T.A., Liu, F., Jeftinija, K., Jeftinija, S., and Haydon, P.G. (1994). Glutamate-mediated astrocyte-neuron signalling. Nature 369, 744-747.
55. Phipps, J.A., Clermont, A.C., Sinha, S., Chilcote, T.J., Bursell, S.E., and Feener, E.P. (2009). Plasma kallikrein mediates angiotensin II type 1 receptor-stimulated retinal vascular permeability. Hypertension 53, 175-181.
56. Plesnila, N., Schulz, J., Stoffel, M., Eriskat, J., Pruneau, D., and Baethmann, A. (2001). Role of bradykinin B2 receptors in the formation of vasogenic brain edema in rats. J. Neurotrauma 18, 1049-1058.
57. Pouliot, M., Talbot, S., Senecal, J., Dotigny, F., Vaucher, E., and Couture, R. (2012). Ocular application of the kinin B1 receptor antagonist LF22-0542 inhibits retinal inflammation and oxidative stress in streptozotocin-diabetic rats. PLoS One 7, e33864.
58. Prokofyeva, E. and Zrenner, E. (2012). Epidemiology of major eye diseases leading to blindness in Europe: A literature review. Ophthamic Res. 47, 171-188.
59. Pruneau, D., Belichard, P., Sahel, J.A., and Combal, J.P. (2010). Targeting the kallikrein-kinin system as a new therapeutic approach to diabetic retinopathy. Curr. Opin. Invest. Drugs 11, 507-514.
60. Sainz, I.M., Pixley, R.A., and Colman, R.W. (2007). Fifty years of research on the plasma kallikrein-kinin system: From protein structure and function to cell biology and in-vivo pathophysiology. Thromb. Haemost. 98, 77-83.
61. Selvarajan, S., Lund, L.R., Takeuchi, T., Craik, C.S., and Werb, Z. (2001). A plasma kallikrein-dependent plasminogen cascade required for adipocyte differentiation. Nat. Cell Biol. 3, 267-275.
62. Shariat-Madar, Z., Mahdi, F., and Schmaier, A.H. (2002). Identification and characterization of prolylcarboxypeptidase as an endothelial cell prekallikrein activator. J. Biol. Chem. 277, 17962-17969.
63. Sogawa, K., Nagaoka, T., Izumi, N., Nakabayashi, S., and Yoshida, A. (2010). Acute hyperglycemia-induced endothelial dysfunction in retinal arterioles in cats. Invest. Ophthalmol. Vis. Sci. 51, 2648-2655.
64. Storini, C., Bergamaschini, L., Gesuete, R., Rossi, E., Maiocchi, D., and De Simoni, M.G. (2006). Selective inhibition of plasma kallikrein protects brain from reperfusion injury. J. Pharmacol. Exp. Ther. 318, 849-854.
65. Takeda, H., Kimura, Y., Higashida, H., and Yokoyama, S. (1999). Localization of B2 bradykinin receptor mRNA in the rat retina and sclerocornea. Immunopharmacology 45, 51-55.
66. Talahalli, R., Zarini, S., Tang, J., Li, G., Murphy, R., Kern, T.S., and Gubitosi-Klug, R.A. (2012). Leukocytes regulate retinal capillary degeneration in the diabetic mouse via generation of leukotrienes. J. Leukoc. Biol. 93, 135-143.
67. van der Meijden, P.E., Munnix, I.C., Auger, J.M., Govers-Riemslag, J.W., Cosemans, J.M., Kuijpers, M.J., Spronk, H.M., Watson, S.P., Renne, T., and Heemskerk, J.W. (2009). Dual role of collagen in factor XII-dependent thrombus formation. Blood 114, 881-890.
68. van der Meijden, P.E., Van Schilfgaarde, M., Van Oerle, R., Renne, T., ten Cate, H., and Spronk, H.M. (2012). Platelet- and erythrocyte-derived microparticles trigger thrombin generation via factor XIIa. J. Thromb. Haemost. 10, 1355-1362.
69. van Dijk, H.W., Verbraak, F.D., Kok, P.H., Stehouwer, M., Garvin, M.K., Sonka, M., DeVries, J.H., Schlingemann, R.O., and Abramoff, M.D. (2012). Early neurodegeneration in the retina of type 2 diabetic patients. Invest. Ophthalmol. Vis. Sci. 53, 2715-2719.
70. White-Adams, T.C., Berny, M.A., Patel, I.A., Tucker, E.I., Gailani, D., Gruber, A., and McCarty, O.J. (2010). Laminin promotes coagulation and thrombus formation in a factor XII-dependent manner. J. Thromb. Haemost. 8, 1295-1301.
71. Yamauchi, T., Kashii, S., Yasuyoshi, H., Zhang, S., Honda, Y., and Akaike, A. (2003). Mitochondrial ATP-sensitive potassium channel: A novel site for neuroprotection. Invest. Ophthalmol. Vis. Sci. 44, 2750-2756.
72. Yang, Y., Mao, D., Chen, X., Zhao, L., Tian, Q., Liu, C., and Zhou, B.L. (2012). Decrease in retinal neuronal cells in streptozotocininduced diabetic mice. Mol. Vis. 18, 1411-1420.
73. Yasuyoshi, H., Kashii, S., Zhang, S., Nishida, A., Yamauchi, T., Honda, Y., Asano, Y., Sato, S., and Akaike, A. (2000). Protective effect of bradykinin against glutamate neurotoxicity in cultured rat retinal neurons. Invest. Ophthalmol. Vis. Sci. 41, 2273-2278.
74. Yau, J.W., Rogers, S.L., Kawasaki, R., Lamoureux, E.L., Kowalski, J.W., Bek, T., Chen, S.J., Dekker, J.M., Fletcher, A., Grauslund, J., et al. (2012). Global prevalence and major risk factors of diabetic retinopathy. Diabetes Care 35, 556-564.
75. Yayama, K. and Okamoto, H. (2008). Angiotensin II-induced vasodilation via type 2 receptor: Role of bradykinin and nitric oxide. Int. Immunopharmacol. 8, 312-318.
76. Yu, J., Liu, F., Cui, S.J., Liu, Y., Song, Z.Y., Cao, H., Chen, F.E., Wang, W.J., Sun, T., and Wang, F. (2008). Vitreous proteomic analysis of proliferative vitreoretinopathy. Proteomics 8, 3667-3678.
77. Zhao, Y., Zhang, J., Zhang, J., and Wu, J. (2011). Diabetes mellitus is associated with shortened activated partial thromboplastin time and increased fibrinogen values. PLoS One 6, e16470.