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Review Article

Vascular adhesion protein-1: Role in human pathology and application as a biomarker

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Pages 284-300 | Received 27 Jan 2015, Accepted 10 May 2015, Published online: 18 Aug 2015

References

  • Salmi M, Jalkanen S. A 90-kilodalton endothelial cell molecule mediating lymphocyte binding in humans. Science 1992;257:1407–9
  • Noonan T, Lukas S, Peet GW, et al. The oxidase activity of vascular adhesion protein-1 (VAP-1) is essential for function. Am J Clin Exp Immunol 2013;2:172–85
  • Kaitaniemi S, Grön K, Elovaara H, et al. Functional modulation of vascular adhesion protein-1 by a novel splice variant. PLoS One 2013;8:e54151
  • Amine oxidase, copper-containing, 3; AOC3. *603735. Available at http://www.omim.org/entry/603735
  • Bligt-Lindén E, Arunachalam R, Parkash V, Salminen TA. Structural comparison of the active site channels in rodent and primate vascular adhesion protein-1. J Neural Transm 2013;120:947–50
  • Airenne TT, Nymalm Y, Kidron H, et al. Crystal structure of the human vascular adhesion protein-1: unique structural features with functional implications. Protein Sci 2005;14:1964–74
  • Jakobsson E, Nilsson J, Ogg D, Kleywegt GJ. Structure of human semicarbazide-sensitive amine oxidase/vascular adhesion protein-1. Acta Crystallogr D Biol Crystallogr 2005;61:1550–62
  • Kurkijärvi R, Yegutkin GG, Gunson BK, et al. Circulating soluble vascular adhesion protein 1 accounts for the increased serum monoamine oxidase activity in chronic liver disease. Gastroenterology 2000;119:1096–103
  • Wang YC, Li HY, Wei JN, et al. Serum vascular adhesion protein-1 level is higher in smokers than non-smokers. Ann Hum Biol 2013;40:413–8
  • Aalto K, Maksimow M, Juonala M, et al. Soluble vascular adhesion protein-1 correlates with cardiovascular risk factors and early atherosclerotic manifestations. Arterioscler Thromb Vasc Biol 2012;32:523–32
  • Boomsma F, Bhaggoe UM, van der Houwen AM, van den Meiracker AH. Plasma semicarbazide-sensitive amine oxidase in human (patho)physiology. Biochim Biophys Acta 2003;1647:48–54
  • McEwen CM Jr, Castell DO. Abnormalities of serum monoamine oxidase in chronic liver disease. J Lab Clin Med 1967;70:36–47
  • Tufvesson G. Determination of monoamine oxidase activity in human blood serum with 14C-benzylamine and 14C-tyramine as substrates. Scand J Clin Lab Invest 1969;23:71–7
  • van Dijk J, Boomsma F, Alberts G, et al. Determination of semicarbazide-sensitive amine oxidase activity in human plasma by high-performance liquid chromatography with fluorimetric detection. J Chromatogr B Biomed Appl 1995;663:43–50
  • Holt A, Palcic MM. A peroxidase-coupled continuous absorbance platereader assay for flavin monoamine oxidases, copper-containing amine oxidases and related enzymes. Nat Protoc 2006;1:2498–505
  • Lin MS, Li HY, Wei JN, et al. Serum vascular adhesion protein-1 is higher in subjects with early stages of chronic kidney disease. Clin Biochem 2008;41:1362–7
  • Kurkijärvi R, Adams DH, Leino R, et al. Circulating form of human vascular adhesion protein-1 (VAP-1): increased serum levels in inflammatory liver diseases. J Immunol 1998;161:1549–57
  • Dugué B, Leppänen E, Gräsbeck R. Preanalytical factors (biological variation) and the measurement of serum soluble intercellular adhesion molecule-1 in humans: influence of the time of day, food intake, and physical and psychological stress. Clin Chem 1999;45:1543–7
  • Hartweg J, Gunter M, Perera R, et al. Stability of soluble adhesion molecules, selectins, and C-reactive protein at various temperatures: implications for epidemiological and large-scale clinical studies. Clin Chem 2007;53:1858–60
  • Salmi M, Kalimo K, Jalkanen S. Induction and function of vascular adhesion protein-1 at sites of inflammation. J Exp Med 1993;178:2255–60
  • Weston CJ, Shepherd EL, Adams DH. Cellular localization and trafficking of vascular adhesion protein-1 as revealed by an N-terminal GFP fusion protein. J Neural Transm 2013;120:951–61
  • Solé M, Unzeta M. Vascular cell lines expressing SSAO/VAP-1: a new experimental tool to study its involvement in vascular diseases. Biol Cell 2011;103:543–57
  • Salmi M, Jalkanen S. Developmental regulation of the adhesive and enzymatic activity of vascular adhesion protein-1 (VAP-1) in humans. Blood 2006;108:1555–61
  • Smith DJ, Vainio PJ. Targeting vascular adhesion protein-1 to treat autoimmune and inflammatory diseases. Ann NY Acad Sci 2007;1110:382–8
  • Jaakkola K, Kaunismäki K, Tohka S, et al. Human vascular adhesion protein-1 in smooth muscle cells. Am J Pathol 1999;155:1953–65
  • Koskinen K, Vainio PJ, Smith DJ, et al. Granulocyte transmigration through endothelium is regulated by the oxidase activity of vascular adhesion protein-1 (VAP-1). Blood 2004;103:3388–95
  • Salmi M, Jalkanen S. Cell-surface enzymes in control of leukocyte trafficking. Nat Rev Immunol 2005;5:760–71
  • Mercier N, Moldes M, El Hadri K, Feve B. Semicarbazide-sensitive amine oxidase activation promotes adipose conversion of 3T3-L1 cells. Biochem J 2001;358:335–42
  • Zorzano A, Abella A, Marti L, et al. Semicarbazide-sensitive amine oxidase activity exerts insulin-like effects on glucose metabolism and insulin-signaling pathways in adipose cells. Biochim Biophys Acta 2003;1647:3–9
  • Gokturk C, Nilsson J, Nordquist J, et al. Overexpression of semicarbazide-sensitive amine oxidase in smooth muscle cells leads to an abnormal structure of the aortic elastic laminas. Am J Pathol 2003;163:1921–8
  • Salmi M, Tohka S, Berg EL, et al. Vascular adhesion protein 1 (VAP-1) mediates lymphocyte subtype-specific, selectin-independent recognition of vascular endothelium in human lymph nodes. J Exp Med 1997;186:589–600
  • Tohka S, Laukkanen ML, Jalkanen S, Salmi M. Vascular adhesion protein 1 (VAP-1) functions as a molecular brake during granulocyte rolling and mediates their recruitment in vivo. FASEB J 2001;15:373–82
  • Stolen CM, Marttila-Ichihara F, Koskinen K, et al. Absence of the endothelial oxidase AOC3 leads to abnormal leukocyte traffic in vivo. Immunity 2005;22:105–15
  • Jaakkola K, Nikula T, Holopainen R, et al. In vivo detection of vascular adhesion protein-1 in experimental inflammation. Am J Pathol 2000;157:463–71
  • Salmi M, Jalkanen S. Human vascular adhesion protein-1 (VAP-1) is a unique sialoglycoprotein that mediates carbohydrate-dependent binding of lymphocytes to endothelial cells. J Exp Med 1996;183:569–79
  • Salmi M, Yegutkin G, Lehvonen R, et al. A cell surface amine oxidase directly controls lymphocyte migration. Immunity 2001;14:265–76
  • Smith DJ, Salmi M, Bono P, et al. Cloning of vascular adhesion protein 1 reveals a novel multifunctional adhesion molecule. J Exp Med 1998;188:17–27
  • Yu PH, Davis BA, Deng Y. 2-Bromoethylamine as a potent selective suicide inhibitor for semicarbazide-sensitive amine oxidase. Biochem Pharmacol 2001;61:741–8
  • Salter-Cid LM, Wang E, O'Rourke AM, et al. Anti-inflammatory effects of inhibiting the amine oxidase activity of semicarbazide-sensitive amine oxidase. J Pharmacol Exp Ther 2005;315:553–62
  • Inoue T, Morita M, Tojo T, et al. Novel 1H-imidazol-2-amine derivatives as potent and orally active vascular adhesion protein-1 (VAP-1) inhibitors for diabetic macular edema treatment. Bioorg Med Chem 2013;21:3873–81
  • Esteban G, Bolea I, Sun P, et al. A therapeutic approach to cerebrovascular diseases based on indole substituted hydrazides and hydrazines able to interact with human vascular adhesion protein-1, monoamine oxidases (A and B), AChE and BuChE. J Neural Transm 2013;120:911–18
  • Xu HL, Salter-Cid L, Linnik MD, et al. Vascular adhesion protein-1 plays an important role in postis chemic inflammation and neuropathology in diabetic, estrogen-treated ovariectomized female rats subjected to transient forebrain ischemia. J Pharmacol Exp Ther 2006;317:19–29
  • Wang EY, Gao H, Salter-Cid L, et al. Design, synthesis, and biological evaluation of semicarbazide-sensitive amine oxidase (SSAO) inhibitors with anti-inflammatory activity. J Med Chem 2006;49:2166–73
  • O'Rourke AM, Wang EY, Miller A, et al. Anti-inflammatory effects of LJP 1586 [Z-3-fluoro-2-(4-methoxybenzyl)allylamine hydrochloride], an amine-based inhibitor of semicarbazide-sensitive amine oxidase activity. J Pharmacol Exp Ther 2008;324:867–75
  • Inoue T, Morita M, Tojo T, et al. Synthesis and SAR study of new thiazole derivatives as vascular adhesion protein-1 (VAP-1) inhibitors for the treatment of diabetic macular edema: part 2. Bioorg Med Chem 2013;21:2478–94
  • Inoue T, Morita M, Tojo T, et al. Synthesis and SAR study of new thiazole derivatives as vascular adhesion protein-1 (VAP-1) inhibitors for the treatment of diabetic macular edema. Bioorg Med Chem 2013;21:1219–33
  • Foot JS, Yow TT, Schilter H, et al. PXS-4681A, a potent and selective mechanism-based inhibitor of SSAO/VAP-1 with anti-inflammatory effects in vivo. J Pharmacol Exp Ther 2013;347:365–74
  • Enzsöly A, Dunkel P, Récsán Z, et al. Preliminary studies of the effects of vascular adhesion protein-1 inhibitors on experimental corneal neovascularization. J Neural Transm 2011;118:1065–9
  • Marttila-Ichihara F, Auvinen K, Elima K, et al. Vascular adhesion protein-1 enhances tumor growth by supporting recruitment of Gr-1+CD11b + myeloid cells into tumors. Cancer Res 2009;69:7875–83
  • Marttila-Ichihara F, Castermans K, Auvinen K, et al. Small-molecule inhibitors of vascular adhesion protein-1 reduce the accumulation of myeloid cells into tumors and attenuate tumor growth in mice. J Immunol 2010;184:3164–73
  • Kirton CM, Laukkanen ML, Nieminen A, et al. Function-blocking antibodies to human vascular adhesion protein-1: a potential anti-inflammatory therapy. Eur J Immunol 2005;35:3119–30
  • Vainio PJ, Kortekangas-Savolainen O, Mikkola JH, et al. Safety of blocking vascular adhesion protein-1 in patients with contact dermatitis. Basic Clin Pharmacol Toxicol 2005;96:429–35
  • Bligt-Lindén E, Pihlavisto M, Szatmári I, et al. Novel pyridazinone inhibitors for vascular adhesion protein-1 (VAP-1): old target-new inhibition mode. J Med Chem 2013;56:9837–48
  • Li HY, Lin MS, Wei JN, et al. Change of serum vascular adhesion protein-1 after glucose loading correlates to carotid intima-medial thickness in non-diabetic subjects. Clin Chim Acta 2009;403:97–101
  • Boomsma F, de Kam PJ, Tjeerdsma G, et al. Plasma semicarbazide-sensitive amine oxidase (SSAO) is an independent prognostic marker for mortality in chronic heart failure. Eur Heart J 2000;21:1859–63
  • Aalto K, Havulinna AS, Jalkanen S, et al. Soluble vascular adhesion protein-1 predicts incident major adverse cardiovascular events and improves reclassification in a Finnish prospective cohort study. Circ Cardiovasc Genet 2014;7:529–35
  • Bour S, Caspar-Bauguil S, Iffiú-Soltész Z, et al. Semicarbazide-sensitive amine oxidase/vascular adhesion protein-1 deficiency reduces leukocyte infiltration into adipose tissue and favors fat deposition. Am J Pathol 2009;174:1075–83
  • Raimondi L, Pirisino R, Banchelli G, et al. Cultured preadipocytes produce a semicarbazide-sensitive amine oxidase (SSAO) activity. J Neural Transm Suppl 1990;32:331–6
  • Moldes M, Fève B, Pairault J. Molecular cloning of a major mRNA species in murine 3T3 adipocyte lineage differentiation-dependent expression, regulation, and identification as semicarbazide-sensitive amine oxidase. J Biol Chem 1999;274:9515–23
  • Bour S, Daviaud D, Gres S, et al. Adipogenesis-related increase of semicarbazide-sensitive amine oxidase and monoamine oxidase in human adipocytes. Biochimie 2007;89:916–25
  • Weiss HG, Klocker J, Labeck B, et al. Plasma amine oxidase: a postulated cardiovascular risk factor in nondiabetic obese patients. Metabolism 2003;52:688–92
  • Iffiú-Soltész Z, Mercader J, Daviaud D, et al. Increased primary amine oxidase expression and activity in white adipose tissue of obese and diabetic db−/− mice. J Neural Transm 2011;118:1071–7
  • Carpéné C, Abello V, Iffiú-Soltész Z, et al. Limitation of adipose tissue enlargement in rats chronically treated with semicarbazide-sensitive amine oxidase and monoamine oxidase inhibitors. Pharmacol Res 2008;57:426–34
  • Carpéné C, Iffiú-Soltesz Z, Bour S, et al. Reduction of fat deposition by combined inhibition of monoamine oxidases and semicarbazide-sensitive amine oxidases in obese Zucker rats. Pharmacol Res 2007;56:522–30
  • Enrique-Tarancon G, Mart L, Lizcano JM, et al. Role of semicarbazide-sensitive amine oxidase on glucose transport and GLUT4 recruitment to the cell surface in adipose cell. J Biol Chem 1998;273:8025–32
  • Boomsma F, van den Meiracker AH, Winke S, et al. Circulating semicarbazide-sensitive amine oxidase is raised both in type I (insulin-dependent), in type II (non-insulin-dependent) diabetes mellitus and even in childhood type I diabetes at first clinical diagnosis. Diabetologia 1999;42:233–7
  • Li HY, Jiang YD, Chang TJ, et al. Serum vascular adhesion protein-1 predicts 10-year cardiovascular and cancer mortality in individuals with type 2 diabetes. Diabetes 2011;60:993–9
  • Li HY, Wei JN, Lin MS, et al. Serum vascular adhesion protein-1 is increased in acute and chronic hyperglycemia. Clin Chim Acta 2009;404:149–53
  • Somfai GM, Knippel B, Ruzicska E, et al. Soluble semicarbazide-sensitive amine oxidase (SSAO) activity is related to oxidative stress and subchronic inflammation in streptozotocin-induced diabetic rats. Neurochem Int 2006;48:746–52
  • Boomsma F, Pedersen-Bjergaard U, Agerholm-Larsen B, et al. Association between plasma activities of semicarbazide-sensitive amine oxidase and angiotensin-converting enzyme in patients with type 1 diabetes mellitus. Diabetologia 2005;48:1002–7
  • Boomsma F, Derkx FHM, van den Meiracker AH, et al. Plasma semicarbazide-sensitive amine oxidase activity is elevated in diabetes mellitus and correlates with glycosylated haemoglobin. Clin Sci (Lond) 1995;88:675–9
  • Abella A, Garcia-Vicente S, Viguerie N, et al. Adipocytes release a soluble form of VAP-1/SSAO by a metalloprotease-dependent process and in a regulated manner. Diabetologia 2004;47:429–38
  • Salmi M, Stolen C, Jousilahti P, et al. Insulin-regulated increase of soluble vascular adhesion protein-1 in diabetes. Am J Pathol 2002;161:2255–62
  • Stolen CM, Madanat R, Marti L, et al. Semicarbazide sensitive amine oxidase overexpression has dual consequences: insulin mimicry and diabetes-like complications. FASEB J 2004;18:702–4
  • Karim S, Liaskou E, Fear J, et al. Dysregulated hepatic expression of glucose transporters in chronic disease: contribution of semicarbazide-sensitive amine oxidase to hepatic glucose uptake. Am J Physiol Gastrointest Liver Physiol 2014;307:G1180–90
  • Marti L, Abella A, Carpéné C, et al. Combined treatment with benzylamine and low dosages of vanadate enhances glucose tolerance and reduces hyperglycemia in streptozotocin-induced diabetic rats. Diabetes 2001;50:2061–8
  • Deng Y, Yu PH. Simultaneous determination of formaldehyde and methylglyoxal in urine: involvement of semicarbazide-sensitive amine oxidase-mediated deamination in diabetic complications. J Chromatogr Sci 1999;37:317–22
  • Gubisne-Haberle D, Hill W, Kazachkov M, et al. Protein cross-linkage induced by formaldehyde derived from semicarbazide-sensitive amine oxidase-mediated deamination of methylamine. J Pharmacol Exp Ther 2004;310:1125–32
  • Yu PH, Zuo DM. Oxidative deamination of methylamine by semicarbazide-sensitive amine oxidase leads to cytotoxic damage in endothelial cells: possible consequences for diabetes. Diabetes 1993;42:594–603
  • Nunes SF, Figueiredo IV, Pereira JS, et al. Monoamine oxidase and semicarbazide-sensitive amine oxidase kinetic analysis in mesenteric arteries of patients with type 2 diabetes. Physiol Res 2011;60:309–15
  • Sun P, Solé M, Unzeta M. Involvement of SSAO/VAP-1 in oxygen-glucose deprivation-mediated damage using the endothelial hSSAO/VAP-1-expressing cells as experimental model of cerebral ischemia. Cerebrovasc Dis 2014;37:171–80
  • Hernandez-Guillamon M, Garcia-Bonilla L, Solé M, et al. Plasma VAP-1/SSAO activity predicts intracranial hemorrhages and adverse neurological outcome after tissue plasminogen activator treatment in stroke. Stroke 2010;41:1528–35
  • Ma Q, Manaenko A, Khatibi NH, et al. Vascular adhesion protein-1 inhibition provides antiinflammatory protection after an intracerebral hemorrhagic stroke in mice. J Cereb Blood Flow Metab 2011;31:881–93
  • Garpenstrand H, Ekblom J, Bäcklund LB, et al. Elevated plasma semicarbazide-sensitive amine oxidase (SSAO) activity in Type 2 diabetes mellitus complicated by retinopathy. Diab Med 1999;16:514–21
  • Grönvall-Nordquist JL, Backlund LB, Garpenstrand H, et al. Follow-up of plasma semicarbazide-sensitive amine oxidase activity and retinopathy in Type 2 diabetes mellitus. J Diab Complications 2001;15:250–6
  • Murata M, Noda K, Fukuhara J, et al. Soluble vascular adhesion protein-1 accumulates in proliferative diabetic retinopathy. Invest Ophthalmol Vis Sci 2012;53:4055–62
  • Almulki L, Noda K, Nakao S, et al. Localization of vascular adhesion protein-1 (VAP-1) in the human eye. Exp Eye Res 2010;90:26–32
  • Merinen M, Irjala H, Salmi M, et al. Vascular adhesion protein-1 is involved in both acute and chronic inflammation in the mouse. Am J Pathol 2005;166:793–800
  • Noda K, Nakao S, Zandi S, et al. Vascular adhesion protein-1 regulates leukocyte transmigration rate in the retina during diabetes. Exp Eye Res 2009;89:774–81
  • Yoshikawa N, Noda K, Shinoda H, et al. Serum vascular adhesion protein-1 correlates with vascular endothelial growth factor in patients with type II diabetes. J Diabetes Complications 2013;27:162–6
  • Nakao S, Noda K, Zandi S, et al. VAP-1-mediated M2 macrophage infiltration underlies IL-1β- but not VEGF-A-induced lymph- and angiogenesis. Am J Pathol 2011;178:1913–21
  • Luo W, Xie F, Zhang Z, Sun D. Vascular adhesion protein 1 in the eye. J Ophthalmol 2013;2013:925267
  • Yoshikawa N, Noda K, Ozawa Y, et al. Blockade for vascular adhesion protein-1 suppresses pathological neovascularization in oxygen-induced retinopathy. Acta Ophthalmol 2013;91:e409–10
  • Noda K, Miyahara S, Nakazawa T, et al. Inhibition of vascular adhesion protein-1 suppresses endotoxin-induced uveitis. FASEB J 2008;22:1094–103
  • Noda K, She H, Nakazawa T, et al. Vascular adhesion protein-1 blockade suppresses choroidal neovascularization. FASEB J 2008;22:2928–35
  • Fukuhara J, Kase S, Noda K, et al. Immunolocalization of vascular adhesion protein-1 in human conjunctival tumors. Ophthalmic Res 2012;48:33–7
  • Weston CJ, Adams DH. Hepatic consequences of vascular adhesion protein-1 expression. J Neural Transm 2011;118:1055–64
  • McNab G, Reeves JL, Salmi M, et al. Vascular adhesion protein 1 mediates binding of T cells to human hepatic endothelium. Gastroenterology 1996;110:522–8
  • Bonder CS, Norman MU, Swain MG, et al. Rules of recruitment for Th1 and Th2 lymphocytes in inflamed liver: a role for alpha-4 integrin and vascular adhesion protein-1. Immunity 2005;23:153–63
  • Lalor PF, Edwards S, McNab G, et al. Vascular adhesion protein-1 mediates adhesion and transmigration of lymphocytes on human hepatic endothelial cells. J Immunol 2002;169:983–92
  • Lalor PF, Sun PJ, Weston CJ, et al. Activation of vascular adhesion protein-1 on liver endothelium results in an NF-kappaB-dependent increase in lymphocyte adhesion. Hepatology 2007;45:465–74
  • Aspinall AI, Curbishley SM, Lalor PF, et al. CX(3)CR1 and vascular adhesion protein-1-dependent recruitment of CD16(+)monocytes across human liver sinusoidal endothelium. Hepatology 2010;51:2030–9
  • Oo YH, Banz V, Kavanagh D, et al. CXCR3-dependent recruitment and CCR6-mediated positioning of Th-17 cells in the inflamed liver. J Hepatol 2012;57:1044–51
  • Liaskou E, Karikoski M, Reynolds GM, et al. Regulation of mucosal addressin cell adhesion molecule 1 expression in human and mice by vascular adhesion protein 1 amine oxidase activity. Hepatology 2011;53:661–72
  • Weston CJ, Shepherd EL, Claridge LC, et al. Vascular adhesion protein-1 promotes liver inflammation and drives hepatic fibrosis. J Clin Invest 2015;125:501–20
  • Martelius T, Salaspuro V, Salmi M, et al. Blockade of vascular adhesion protein-1 inhibits lymphocyte infiltration in rat liver allograft rejection. Am J Pathol 2004;165:1993–2001
  • Lee WY, Salmi M, Kelly MM, et al. Therapeutic advantage of anti-VAP-1 over anti-α4 integrin antibody in concanavalin a-induced hepatitis. Hepatology 2013;58:1413–23
  • Koutroubakis IE, Petinaki E, Vardas E, et al. Circulating soluble vascular adhesion protein 1 in patients with inflammatory bowel disease. Eur J Gastroenterol Hepatol 2002;14:405–8
  • Koc-Zorawska E, Malyszko J, Zbroch E, et al. Vascular adhesion protein-1 and renalase in regard to diabetes in hemodialysis patients. Arch Med Sci 2012;8:1048–52
  • Koc-Zorawska E, Malyszko J, Zbroch E, et al. VAP-1 in peritoneally dialyzed patients. Postepy Hig Med Dosw (Online) 2013;67:1340–4
  • Nemcsik J, Szökö E, Soltész Z, et al. Alteration of serum semicarbazide-sensitive amine oxidase activity in chronic renal failure. J Neural Transm 2007;114:841–3
  • Koc-Zorawska E, Malyszko J, Malyszko JS, Mysliwiec M. VAP-1, a novel molecule linked to endothelial damage and kidney function in kidney allograft recipients. Kidney Blood Press Res 2012;36:242–7
  • Koc-Zorawska E, Przybylowski P, Malyszko JS, et al. Vascular adhesion protein-1, a novel molecule, in kidney and heart allograft recipients. Transplant Proc 2013;45:2009–12
  • Wong MY, Saad S, Pollock C, Wong MG. Semicarbazide-sensitive amine oxidase and kidney disease. Am J Physiol Renal Physiol 2013;305:F1637–44
  • Bolt H. Experimental toxicology of formaldehyde. J Cancer Res Clin Oncol 1987;13:305–9
  • Heck H, Casanova M, Starr T. Formaldehyde toxicity-new understanding. Crit Rev Toxicol 1990;20:397–426
  • Yu P, Wright S, Fan E, et al. Physiological and pathological implications of semicarbazide-sensitive amine-oxidase. Biochem Biophys Acta 2003;1647:193–9
  • Singh B, Shinagawa K, Taube C, et al. Strain-specific differences in perivascular inflammation in lungs in two murine models of allergic airway inflammation. Clin Exp Immunol 2005;141:223–9
  • Yu PH, Lu LX, Fan H, et al. Involvement of semicarbazide-sensitive amine oxidase-mediated deamination in lipopolysaccharide-induced pulmonary inflammation. Am J Pathol 2006;168:718–26
  • Dunkel J, Aguilar-Pimentel JA, Ollert M, et al. Endothelial amine oxidase AOC3 transiently contributes to adaptive immune responses in the airways. Eur J Immunol 2014;44:3232–9
  • Sallisalmi M, Tenhunen J, Yang R, et al. Vascular adhesion protein-1 and syndecan-1 in septic shock. Acta Anaesthesiol Scand 2012;56:316–22
  • Marttila-Ichihara F, Smith DJ, Stolen C, et al. Vascular amine oxidases are needed for leukocyte extravasation into inflamed joints in vivo. Arthritis Rheum 2006;54:2852–62
  • Jalkanen S, Salmi M. Cell surface monoamine oxidases: enzymes in search of a function. EMBO J 2001;20:3893–901
  • Nurminen EM, Pihlavisto M, Lázár L, et al. Novel hydrazine molecules as tools to understand the flexibility of vascular adhesion protein-1 ligand-binding site. J Med Chem 2011;54:2143–54
  • Fett N. Scleroderma: nomenclature, etiology, pathogenesis, prognosis, and treatments: facts and controversies. Clin Dermatol 2013;31:432–7
  • Yanaba K, Yoshizaki A, Muroi E, et al. Increased circulating soluble vascular adhesion protein-1 levels in systemic sclerosis: association with lower frequency and severity of interstitial lung disease. Int J Rheum Dis 2013;16:442–7
  • Madej A, Reich A, Orda A, Szepietowski JC. Vascular adhesion protein-1 (VAP-1) is overexpressed in psoriatic patients. J Eur Acad Dermatol Venereol 2007;21:72–8
  • Nemati H, Khodarahmi R, Rahmani A, et al. Serum lipid profile in psoriatic patients: correlation between vascular adhesion protein 1 and lipoprotein (a). Cell Biochem Funct 2013;31:36–40
  • Asefi M, Vaisi-Raygani A, Khodarahmi R, et al. Methylentetrahydrofolatereductase (rs1801133) polymorphism and psoriasis: contribution to oxidative stress, lipid peroxidation and correlation with vascular adhesion protein 1, preliminary report. J Eur Acad Dermatol Venereol 2014;28:1192–8
  • Arvilommi AM, Salmi M, Kalimo K, Jalkanen S. Lymphocyte binding to vascular endothelium in inflamed skin revisited: a central role for vascular adhesion protein-1 (VAP-1). Eur J Immunol 1996;26:825–33
  • Arvilommi AM, Salmi M, Jalkanen S. Organ-selective regulation of vascular adhesion protein-1 expression in man. Eur J Immunol 1997;27:1794–800
  • Unzeta M, Solé M, Boada M, Hernández M. Semicarbazide-sensitive amine oxidase (SSAO) and its possible contribution to vascular damage in Alzheimer's disease. J Neural Transm 2007;114:857–62
  • del Mar Hernandez M, Esteban M, Szabo P, et al. Human plasma semicarbazide sensitive amine oxidase (SSAO), beta-amyloid protein and aging. Neurosci Lett 2005;384:183–7
  • Yu PH. Involvement of cerebrovascular semicarbazide-sensitive amine oxidase in the pathogenesis of Alzheimer's disease and vascular dementia. Med Hypotheses 2001;57:175–9
  • Ferrer I, Lizcano JM, Hernández M, Unzeta M. Overexpression of semicarbazide sensitive amine oxidase in the cerebral blood vessels in patients with Alzheimer's disease and cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy. Neurosci Lett 2002;321:21–4
  • Castillo V, Lizcano JM, Visa J, Unzeta M. Semicarbazide-sensitive amine oxidase (SSAO) from human and bovine cerebrovascular tissues: biochemical and immunohistological characterization. Neurochem Int 1998;33:415–23
  • Ekblom J, Grönvall JL, Garpenstrand H, et al. Is semicarbazide-sensitive amine oxidase in blood plasma partly derived from the skeleton? Neurobiology (Bp) 2000;8:129–35
  • Valente T, Gella A, Solé M, et al. Immunohistochemical study of semicarbazide-sensitive amine oxidase/vascular adhesion protein-1 in the hippocampal vasculature: pathological synergy of Alzheimer's disease and diabetes mellitus. J Neurosci Res 2012;90:1989–96
  • Airas L, Mikkola J, Vainio JM, et al. Elevated serum soluble vascular adhesion protein-1 (VAP-1) in patients with active relapsing remitting multiple sclerosis. J Neuroimmunol 2006;177:132–5
  • O'Rourke AM, Wang EY, Salter-Cid L, et al. Benefit of inhibiting SSAO in relapsing experimental autoimmune encephalomyelitis. J Neural Transm 2007;114:845–9
  • Ramsay RR. Inhibitor design for monoamine oxidases. Curr Pharm Des 2013;19:2529–39
  • Roessner V, Weber A, Becker A, et al. Decreased serum semicarbazide sensitive aminooxidase (SSAO) activity in patients with major depression. Prog Neuropsychopharmacol Biol Psychiatry 2006;30:906–9
  • Toiyama Y, Miki C, Inoue Y, et al. Circulating form of human vascular adhesion protein-1 (VAP-1): decreased serum levels in progression of colorectal cancer and predictive marker of lymphatic and hepatic metastasis. J Surg Oncol 2009;99:368–72
  • Yasuda H, Toiyama Y, Ohi M, et al. Serum soluble vascular adhesion protein-1 is a valuable prognostic marker in gastric cancer. J Surg Oncol 2011;103:695–9
  • Kemik O, Sümer A, Kemik AS, et al. Human vascular adhesion proteın-1 (VAP-1): serum levels for hepatocellular carcinoma in non-alcoholic and alcoholic fatty liver disease. World J Surg Oncol 2010;8:83
  • Yu TY, Li HY, Jiang YD, et al. Serum vascular adhesion protein-1 level predicts risk of incident cancers in subjects with type II diabetes. Cancer Epidemiol Biomarkers Prev 2014;23:1366–73
  • Li YI, Hung JS, Yu TY, et al. Serum vascular adhesion protein-1 predicts all-cause mortality and cancer-related mortality in subjects with colorectal cancer. Clin Chim Acta 2014;428:51–6
  • Kaplan MA, Kucukoner M, Inal A, et al. Relationship between serum soluble vascular adhesion protein-1 level and gastric cancer prognosis. Oncol Res Treat 2014;37:340–4
  • Ferjančič Š, Gil-Bernabé AM, Hill SA, et al. VCAM-1 and VAP-1 recruit myeloid cells that promote pulmonary metastasis in mice. Blood 2013;121:3289–97
  • Li R, Li H, Luo HJ, et al. SSAO inhibitors suppress hepatocellular tumor growth in mice. Cell Immunol 2013;283:61–9
  • Chen J, Xi J, Tian Y, et al. Identification, prioritization, and evaluation of glycoproteins for aggressive prostate cancer using quantitative glycoproteomics and antibody-based assays on tissue specimens. Proteomics 2013;13:2268–77
  • Irjala H, Salmi M, Alanen K, et al. Vascular adhesion protein 1 mediates binding of immunotherapeutic effector cells to tumor endothelium. J Immunol 2001;166:6937–43
  • Yoong KF, McNab G, Hübscher SG, Adams DH. Vascular adhesion protein-1 and ICAM-1 support the adhesion of tumor-infiltrating lymphocytes to tumor endothelium in human hepatocellular carcinoma. J Immunol 1998;160:3978–88

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