Intraocular hemorrhage causes retinal vascular dysfunction via plasma kallikrein

Investigative Ophthalmology and Visual Science

Volumn 54, Issue 2, 2013, Pages 1086-1094

  Liu, Jia ^a   Clermont, Allen C ^a   Gao, Ben Bo ^a   Feener, Edward P ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACRIDINE ORANGE; BRADYKININ; COLLAGEN; COLLAGENASE; PLASMA KALLIKREIN; PROTEOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD AUTOTRANSFUSION; BLOOD VESSEL PERMEABILITY; CONTROLLED STUDY; COW; FLUOROPHOTOMETRY; INTRAOCULAR HEMORRHAGE; LEUKOSTASIS; LIQUID CHROMATOGRAPHY; MALE; MASS SPECTROMETRY; NONHUMAN; PERICYTE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; RAT; RETINA BLOOD VESSEL; SCANNING LASER OPHTHALMOSCOPE; TANDEM MASS SPECTROMETRY;

ANIMALS; BLOOD; BLOOD-RETINAL BARRIER; BRADYKININ; CAPILLARY PERMEABILITY; CATTLE; CELLS, CULTURED; COLLAGENASES; CONCANAVALIN A; EVANS BLUE; FLUORESCEIN-5-ISOTHIOCYANATE; FLUOROPHOTOMETRY; INTRAVITREAL INJECTIONS; LEUKOSTASIS; MALE; PERICYTES; PLASMA KALLIKREIN; RATS; RATS, LONG-EVANS; RATS, SPRAGUE-DAWLEY; RETINAL DISEASES; RETINAL HEMORRHAGE; RETINAL VESSELS; TANDEM MASS SPECTROMETRY; VITREOUS BODY;

EID: 84874957469     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.12-10537     Document Type: Article

References (48)

1. Levin AV. Retinal hemorrhages: advances in understanding. Pediatr Clin North Am. 2009;56:333-344.
2. Levin AV. Retinal hemorrhage in abusive head trauma. Pediatrics. 2010;126:961-970.
3. Barthelmes D, Bosch MM, Merz TM, et al. Delayed appearance of high altitude retinal hemorrhages. PLoS One. 2011;6: e11532.
4. 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.
5. Frank RN. Diabetic retinopathy. N Engl J Med. 2004;350:48-58.
6. Schmaier AH, McCrae KR. The plasma kallikrein-kinin system: its evolution from contact activation. J Thromb Haemost. 2007;5:2323-2329.
7. Muller F, Mutch NJ, Schenk WA, et al. Platelet polyphosphates are proinflammatory and procoagulant mediators in vivo. Cell. 2009;139:1143-1156.
8. 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.
9. 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.
10. 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.
11. Abdouh M, Talbot S, Couture R, Hassessian HM. Retinal plasma extravasation in streptozotocin-diabetic rats mediated by kinin B(1) and B(2) receptors. Br J Pharmacol. 2008;154:136-143.
12. Phipps JA, Clermont AC, Sinha S, Chilcote TJ, Bursell SE, Feener EP. Plasma kallikrein mediates angiotensin II type 1 receptor-stimulated retinal vascular permeability. Hypertension. 2009;53:175-181.
13. 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.
14. 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.
15. 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.
16. Acar K, Yagci M, Sucak GT, Haznedar R. Isolated prolonged activated partial thromboplastin time in an asymptomatic patient: Fletcher factor deficiency. Thromb Res. 2006;118: 765-766.
17. Liu J, Gao BB, Clermont AC, et al. Hyperglycemia-induced cerebral hematoma expansion is mediated by plasma kallikrein. Nat Med. 2011;17:206-210.
18. Horio N, Clermont AC, Abiko A, et al. Angiotensin AT(1) receptor antagonism normalizes retinal blood flow and acetylcholine-induced vasodilatation in normotensive diabetic rats. Diabetologia. 2004;47:113-123.
19. Pouliot M, Talbot S, Sénécal J, Dotigny F, Vaucher E, Couture R. Ocular application of the kinin B(1) receptor antagonist LF22-0542 inhibits retinal inflammation and oxidative stress in streptozotocin-diabetic rats. PLoS One. 2012;7:e33864.
20. Nayak RC, Berman AB, George KL, Eisenbarth GS, King GL. A monoclonal antibody (3G5)-defined ganglioside antigen is expressed on the cell surface of microvascular pericytes. J Exp Med. 1988;167:1003-1015.
21. Gao BB, Stuart L, Feener EP. Label-free quantitative analysis of one-dimensional PAGE LC/MS/MS proteome: application on angiotensin II-stimulated smooth muscle cells secretome. Mol Cell Proteomics. 2008;7:2399-2409.
22. Liu J, Gao BB, Feener EP. Proteomic identification of novel plasma kallikrein substrates in the astrocyte secretome. Transl Stroke Res. 2010;1:276-286.
23. Patton N, Aslam T, Macgillivray T, Pattie A, Deary IJ, Dhillon B. Retinal vascular image analysis as a potential screening tool for cerebrovascular disease: a rationale based on homology between cerebral and retinal microvasculatures. J Anat. 2005;206:319-348.
24. Wang J, Doré S. Inflammation after intracerebral hemorrhage. J Cereb Blood Flow Metab. 2007;27:894-908.
25. Balami JS, Buchan AM. Complications of intracerebral haemorrhage. Lancet Neurol. 2012;11:101-118.
26. Qureshi AI, Tuhrim S, Broderick JP, Batjer HH, Hondo H, Hanley DF. Spontaneous intracerebral hemorrhage. N Engl J Med. 2001;344:1450-1460.
27. Keep RF, Xiang J, Ennis SR, et al. Blood-brain barrier function in intracerebral hemorrhage. Acta Neurochir Suppl. 2008;105: 73-77.
28. Wadas TM. Emerging inflammatory biomarkers with acute stroke. Crit Care Nurs Clin North Am. 2009;21:493-505.
29. Noda K, Nakao S, Zandi S, Engelsẗadter V, Mashima Y, Hafezi-Moghadam A. Vascular adhesion protein-1 regulates leukocyte transmigration rate in the retina during diabetes. Exp Eye Res. 2009;89:774-781.
30. Miyahara S, Kiryu J, Yamashiro K, et al. Simvastatin inhibits leukocyte accumulation and vascular permeability in the retinas of rats with streptozotocin-induced diabetes. Am J Pathol. 2004;164:1697-1706.
31. Penn JS, McCollum GW, Barnett JM, Werdich XQ, Koepke KA, Rajaratnam VS. Angiostatic effect of penetrating ocular injury: role of pigment epithelium-derived factor. Invest Ophthalmol Vis Sci. 2006;47:405-414.
32. Selvarajan S, Lund LR, Takeuchi T, Craik CS, Werb Z. A plasma kallikrein-dependent plasminogen cascade required for adipocyte differentiation. Nat Cell Biol. 2001;3:267-275.
33. Lund LR, Green KA, Stoop AA, et al. Plasminogen activation independent of uPA and tPA maintains wound healing in genedeficient mice. EMBO J. 2006;25:2686-2697.
34. Saunders WB, Bayless KJ, Davis GE. MMP-1 activation by serine proteases and MMP-10 induces human capillary tubular network collapse and regression in 3D collagen matrices. J Cell Sci. 2005;118:2325-2340.
35. MacLellan CL, Silasi G, Auriat AM, Colbourne F. Rodent models of intracerebral hemorrhage. Stroke. 2010;41:S95-S98.
36. Kaur C, Foulds WS, Ling EA. Blood-retinal barrier in hypoxic ischaemic conditions: basic concepts, clinical features and management. Prog Retin Eye Res. 2008;27:622-647.
37. Daneman R, Zhou L, Kebede AA, Barres BA. Pericytes are required for blood-brain barrier integrity during embryogenesis. Nature. 2010;468:562-566.
38. Armulik A, Genové G, M̈ae M, et al. Pericytes regulate the blood-brain barrier. Nature. 2010;468:557-561.
39. Fisher M. Pericyte signaling in the neurovascular unit. Stroke. 2009;40(suppl 3):S13-S15.
40. Kose N, Asashima T, Muta M, et al. Altered expression of basement membrane-related molecules in rat brain pericyte, endothelial, and astrocyte cell lines after transforming growth factor-beta1 treatment. Drug Metab Pharmacokinet. 2007;22: 255-266.
41. Bou-Gharios G, Ponticos M, Rajkumar V, Abraham D. Extracellular matrix in vascular networks. Cell Prolif. 2004;37:207-220.
42. Kalluri R. Basement membranes: structure, assembly and role in tumour angiogenesis. Nat Rev Cancer. 2003;3:422-433.
43. Rosell A, Cuadrado E, Ortega-Aznar A, Hernández-Guillamon M, Lo EH, Montaner J. MMP-9-positive neutrophil infiltration is associated to blood-brain barrier breakdown and basal lamina type IV collagen degradation during hemorrhagic transformation after human ischemic stroke. Stroke. 2008;39:1121-1126.
44. Scholler K, Trinkl A, Klopotowski M, et al. Characterization of microvascular basal lamina damage and blood-brain barrier dysfunction following subarachnoid hemorrhage in rats. Brain Res. 2007;1142:237-246.
45. Gould DB, Phalan FC, Breedveld GJ, et al. Mutations in Col4a1 cause perinatal cerebral hemorrhage and porencephaly. Science. 2005;308:1167-1171.
46. Gould DB, Phalan FC, van Mil SE, et al. Role of COL4A1 in small-vessel disease and hemorrhagic stroke. N Engl J Med. 2006;354:1489-1496.
47. Vahed K, Kubis N, Boukobza M, et al. COL4A1 mutation in a patient with sporadic, recurrent intracerebral hemorrhage. Stroke. 2007;38:1461-1464.
48. Rosenberg GA. Matrix metalloproteinases in neuroinflammation. Glia. 2002;39:279-291.