Elevated plasma levels of vascular permeability factors in C1 inhibitor-deficient hereditary angioedema

Allergy: European Journal of Allergy and Clinical Immunology

Volumn 71, Issue 7, 2016, Pages 989-996

  Loffredo, S ^a   Bova, M ^a   Suffritti, C ^b   Borriello, F ^a   Zanichelli, A ^b   Petraroli, A ^a   Varricchi, G ^a   Triggiani, M ^c   Cicardi, M ^b   Marone, Gianni ^a,d  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF SALERNO   (Italy)

^d CNR   (Italy)

Author keywords

Angiopoietins; bradykinin; endothelial nitric oxide synthase; hereditary angioedema with C1 inhibitor deficiency; kininogen; vascular endothelial growth factor; vascular permeability

Indexed keywords

ANGIOPOIETIN 1; ANGIOPOIETIN 2; COMPLEMENT COMPONENT C1S INHIBITOR; VASCULOTROPIN A; VASCULOTROPIN C; BIOLOGICAL MARKER;

ADULT; ANGIONEUROTIC EDEMA; ARTICLE; CLINICAL ASSESSMENT; CLINICAL EVALUATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME IMMUNOASSAY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HEREDITARY ANGIOEDEMA WITH C1 INHIBITOR DEFICIENCY; HUMAN; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; REMISSION; ADOLESCENT; BLOOD; CASE CONTROL STUDY; CHILD; DISEASE EXACERBATION; MIDDLE AGED; PRESCHOOL CHILD; SEVERITY OF ILLNESS INDEX; YOUNG ADULT;

ADOLESCENT; ADULT; ANGIOPOIETIN-1; ANGIOPOIETIN-2; BIOMARKERS; CASE-CONTROL STUDIES; CHILD; CHILD, PRESCHOOL; DISEASE PROGRESSION; FEMALE; HEREDITARY ANGIOEDEMA TYPES I AND II; HUMANS; MALE; MIDDLE AGED; SEVERITY OF ILLNESS INDEX; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR C; YOUNG ADULT;

EID: 84960867357     PISSN: 01054538     EISSN: 13989995     Source Type: Journal    
DOI: 10.1111/all.12862     Document Type: Article

References (45)

1. Cicardi M, Aberer W, Banerji A, Bas M, Bernstein JA, Bork K, et al., Classification, diagnosis, and approach to treatment for angioedema: consensus report from the Hereditary Angioedema International Working Group. Allergy 2014; 69: 602-616.
2. Agostoni A, Aygoren-Pursun E, Binkley KE, Blanch A, Bork K, Bouillet L, et al., Hereditary and acquired angioedema: problems and progress: proceedings of the third C1 esterase inhibitor deficiency workshop and beyond. J Allergy Clin Immunol 2004; 114 (Suppl): S51-S131.
3. Rosen FS, Pensky J, Donaldson V, Charache P,. Hereditary Angioneurotic Edema: Two Genetic Variants. Science 1965; 148: 957-958.
4. Zanichelli A, Arcoleo F, Barca MP, Borrelli P, Bova M, Cancian M, et al., A nationwide survey of hereditary angioedema due to C1 inhibitor deficiency in Italy. Orphanet J Rare Dis 2015; 10: 11.
5. Caccia S, Castelli R, Maiocchi D, Bergamaschini L, Cugno M,. Interaction of C1 inhibitor with thrombin on the endothelial surface. Blood Coagul Fibrinolysis 2011; 22: 571-575.
6. Silverman GA, Bird PI, Carrell RW, Church FC, Coughlin PB, Gettins PG, et al., The serpins are an expanding superfamily of structurally similar but functionally diverse proteins. Evolution, mechanism of inhibition, novel functions, and a revised nomenclature. J Biol Chem 2001; 276: 33293-33296.
7. Nussberger J, Cugno M, Amstutz C, Cicardi M, Pellacani A, Agostoni A,. Plasma bradykinin in angio-oedema. Lancet 1998; 351: 1693-1697.
8. Shoemaker LR, Schurman SJ, Donaldson VH, Davis AE 3rd,. Hereditary angioneurotic oedema: characterization of plasma kinin and vascular permeability-enhancing activities. Clin Exp Immunol 1994; 95: 22-28.
9. Suffritti C, Zanichelli A, Maggioni L, Bonanni E, Cugno M, Cicardi M,. High-molecular-weight kininogen cleavage correlates with disease states in the bradykinin-mediated angioedema due to hereditary C1-inhibitor deficiency. Clin Exp Allergy 2014; 44: 1503-1514.
10. Kuhr F, Lowry J, Zhang Y, Brovkovych V, Skidgel RA,. Differential regulation of inducible and endothelial nitric oxide synthase by kinin B1 and B2 receptors. Neuropeptides 2010; 44: 145-154.
11. Demirturk M, Gelincik A, Cinar S, Kilercik M, Onay-Ucar E, Colakoglu B, et al., Increased eNOS levels in hereditary angioedema. Int Immunopharmacol 2014; 20: 264-268.
12. Ferrara N, Gerber HP, LeCouter J,. The biology of VEGF and its receptors. Nat Med 2003; 9: 669-676.
13. Marone G, Varricchi G, Loffredo S, Granata F,. Mast cells and basophils in inflammatory and tumor angiogenesis and lymphangiogenesis. Eur J Pharmacol 2016; 778: 146-151.
14. Stacker SA, Williams SP, Karnezis T, Shayan R, Fox SB, Achen MG,. Lymphangiogenesis and lymphatic vessel remodelling in cancer. Nat Rev Cancer 2014; 14: 159-172.
15. Kumar P, Shen Q, Pivetti CD, Lee ES, Wu MH, Yuan SY,. Molecular mechanisms of endothelial hyperpermeability: implications in inflammation. Expert Rev Mol Med 2009; 11:e19.
16. Carmeliet P,. Angiogenesis in health and disease. Nat Med 2003; 9: 653-660.
17. Senger DR, Galli SJ, Dvorak AM, Perruzzi CA, Harvey VS, Dvorak HF,. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 1983; 219: 983-985.
18. Hood JD, Meininger CJ, Ziche M, Granger HJ,. VEGF upregulates ecNOS message, protein, and NO production in human endothelial cells. Am J Physiol 1998; 274: H1054-H1058.
19. Grover TR, Zenge JP, Parker TA, Abman SH,. Vascular endothelial growth factor causes pulmonary vasodilation through activation of the phosphatidylinositol-3-kinase-nitric oxide pathway in the late-gestation ovine fetus. Pediatr Res 2002; 52: 907-912.
20. Davis S, Aldrich TH, Jones PF, Acheson A, Compton DL, Jain V, et al., Isolation of angiopoietin-1, a ligand for the TIE2 receptor, by secretion-trap expression cloning. Cell 1996; 87: 1161-1169.
21. Maisonpierre PC, Suri C, Jones PF, Bartunkova S, Wiegand SJ, Radziejewski C, et al., Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science 1997; 277: 55-60.
22. Moss A,. The angiopoietin: tie 2 interaction: a potential target for future therapies in human vascular disease. Cytokine Growth Factor Rev 2013; 24: 579-592.
23. Fiedler U, Scharpfenecker M, Koidl S, Hegen A, Grunow V, Schmidt JM, et al., The Tie-2 ligand angiopoietin-2 is stored in and rapidly released upon stimulation from endothelial cell Weibel-Palade bodies. Blood 2004; 103: 4150-4156.
24. Zhang L, Yang N, Park JW, Katsaros D, Fracchioli S, Cao G, et al., Tumor-derived vascular endothelial growth factor up-regulates angiopoietin-2 in host endothelium and destabilizes host vasculature, supporting angiogenesis in ovarian cancer. Cancer Res 2003; 63: 3403-3412.
25. Nag S, Papneja T, Venugopalan R, Stewart DJ,. Increased angiopoietin2 expression is associated with endothelial apoptosis and blood-brain barrier breakdown. Lab Invest 2005; 85: 1189-1198.
26. Xie Z, Ghosh CC, Patel R, Iwaki S, Gaskins D, Nelson C, et al., Vascular endothelial hyperpermeability induces the clinical symptoms of Clarkson disease (the systemic capillary leak syndrome). Blood 2012; 119: 4321-4332.
27. van der Flier M, van Leeuwen HJ, van Kessel KP, Kimpen JL, Hoepelman AI, Geelen SP,. Plasma vascular endothelial growth factor in severe sepsis. Shock 2005; 23: 35-38.
28. Parikh SM, Mammoto T, Schultz A, Yuan HT, Christiani D, Karumanchi SA, et al., Excess circulating angiopoietin-2 may contribute to pulmonary vascular leak in sepsis in humans. PLoS Med 2006; 3:e46.
29. Gompels MM, Lock RJ,. C1 inhibitor deficiency: diagnosis. Clin Exp Dermatol 2005; 30: 460-462.
30. Berrettini M, Lammle B, White T, Heeb MJ, Schwarz HP, Zuraw B, et al., Detection of in vitro and in vivo cleavage of high molecular weight kininogen in human plasma by immunoblotting with monoclonal antibodies. Blood 1986; 68: 455-462.
31. Harper SJ, Bates DO,. VEGF-A splicing: the key to anti-angiogenic therapeutics? Nat Rev Cancer 2008; 8: 880-887.
32. Bates DO, Cui TG, Doughty JM, Winkler M, Sugiono M, Shields JD, et al., VEGF165b, an inhibitory splice variant of vascular endothelial growth factor, is down-regulated in renal cell carcinoma. Cancer Res 2002; 62: 4123-4131.
33. Qiu Y, Ferguson J, Oltean S, Neal CR, Kaura A, Bevan H, et al., Overexpression of VEGF165b in podocytes reduces glomerular permeability. J Am Soc Nephrol 2010; 21: 1498-1509.
34. Gompels MM, Lock RJ, Morgan JE, Osborne J, Brown A, Virgo PF,. A multicentre evaluation of the diagnostic efficiency of serological investigations for C1 inhibitor deficiency. J Clin Pathol 2002; 55: 145-147.
35. Cicardi M, Igarashi T, Rosen FS, Davis AE 3rd,. Molecular basis for the deficiency of complement 1 inhibitor in type I hereditary angioneurotic edema. J Clin Invest 1987; 79: 698-702.
36. Bafunno V, Bova M, Loffredo S, Divella C, Petraroli A, Marone G, et al., Mutational spectrum of the c1 inhibitor gene in a cohort of Italian patients with hereditary angioedema: description of nine novel mutations. Ann Hum Genet 2014; 78: 73-82.
37. Hansen CB, Csuka D, Munthe-Fog L, Varga L, Farkas H, Hansen KM, et al., The levels of the lectin pathway serine protease MASP-1 and its complex formation with C1 inhibitor are linked to the severity of hereditary angioedema. J Immunol 2015; 195: 3596-3604.
38. Kaplan AP, Joseph K,. Pathogenic mechanisms of bradykinin mediated diseases: dysregulation of an innate inflammatory pathway. Adv Immunol 2014; 121: 41-89.
39. Yano K, Liaw PC, Mullington JM, Shih SC, Okada H, Bodyak N, et al., Vascular endothelial growth factor is an important determinant of sepsis morbidity and mortality. J Exp Med 2006; 203: 1447-1458.
40. Han ED, MacFarlane RC, Mulligan AN, Scafidi J, Davis AE 3rd,. Increased vascular permeability in C1 inhibitor-deficient mice mediated by the bradykinin type 2 receptor. J Clin Invest 2002; 109: 1057-1063.
41. Craig TJ, Levy RJ, Wasserman RL, Bewtra AK, Hurewitz D, Obtulowicz K, et al., Efficacy of human C1 esterase inhibitor concentrate compared with placebo in acute hereditary angioedema attacks. J Allergy Clin Immunol 2009; 124: 801-808.
42. Cicardi M, Banerji A, Bracho F, Malbran A, Rosenkranz B, Riedl M, et al., Icatibant, a new bradykinin-receptor antagonist, in hereditary angioedema. N Engl J Med 2010; 363: 532-541.
43. 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.
44. Granata F, Frattini A, Loffredo S, Staiano RI, Petraroli A, Ribatti D, et al., Production of vascular endothelial growth factors from human lung macrophages induced by group IIA and group X secreted phospholipases A2. J Immunol 2010; 184: 5232-5241.
45. Loffredo S, Staiano RI, Granata F, Genovese A, Marone G,. Immune cells as a source and target of angiogenic and lymphangiogenic factors. Chem Immunol Allergy 2014; 99: 15-36.