Journal of Neural Transmission

, Volume 118, Issue 7, pp 1055–1064 | Cite as

Hepatic consequences of vascular adhesion protein-1 expression

Basic Neurosciences, Genetics and Immunology - Review Article


The liver is constantly exposed to antigens present in the blood and to particulate antigens delivered from the gut. To maintain effective levels of immune surveillance and yet tolerate food antigens, the hepatic environment has become highly specialised. A low flow environment exists within the hepatic sinusoids that not only facilitates the exchange of toxins and nutrients within the liver parenchyma, but also provides an ideal niche for the recruitment of leukocytes. One such adhesion molecule involved in this process, the vascular adhesion protein-1 (VAP-1), is unusual in the context of the leukocyte adhesion cascade in that it is both an adhesion molecule and a primary amine oxidase. In this review, we examine the biological functions of VAP-1 and examine what role this molecule might play in the establishment and progression of chronic liver disease.


Vascular adhesion protein-1 SSAO Liver Hepatic Leukocyte recruitment Primary amine oxidase 



Hepatocellular carcinoma


Hepatitis C virus


High endothelial venule


Liver sinusoidal endothelial cells


Lysyl oxidase


Mucosal addressin cell adhesion molecule-1


Monoamine oxidase


Non-alcoholic fatty liver disease


Non-alcoholic steatohepatitis


Primary biliary cirrhosis


Primary sclerosing cholangitis


Semicarbazide sensitive amine oxidase


Vascular adhesion protein-1


  1. Abella A, Garcia-Vicente S, Viguerie N, Ros-Baro A, Camps M, Palacin M, Zorzano A, Marti L (2004) Adipocytes release a soluble form of VAP-1/SSAO by a metalloprotease-dependent process and in a regulated manner. Diabetologia 47:429–438PubMedGoogle Scholar
  2. Airenne TT, Nymalm Y, Kidron H, Smith DJ, Pihlavisto M, Salmi M, Jalkanen S, Johnson MS, Salminen TA (2005) Crystal structure of the human vascular adhesion protein-1: unique structural features with functional implications. Protein Sci 14:1964–1974PubMedGoogle Scholar
  3. Altamirano J, Bataller R (2010) Cigarette smoking and chronic liver diseases. Gut 59:1159–1162PubMedGoogle Scholar
  4. Asatoor AM, Kerr DN (1961) Amines in blood and urine in relation to liver disease. Clin Chim Acta 6:149–156Google Scholar
  5. Aspinall AI, Curbishley SM, Lalor PF, Weston CJ, Liaskou E, Adams RM, Holt AP, Adams DH (2010) CX(3)CR1 and vascular adhesion protein-1-dependent recruitment of CD16(+) monocytes across human liver sinusoidal endothelium. Hepatology 51:2030–2039PubMedGoogle Scholar
  6. Baba S, Watanabe Y, Gejyo F, Arakawa M (1984) High-performance liquid chromatographic determination of serum aliphatic amines in chronic renal failure. Clin Chim Acta 136:49–56PubMedGoogle Scholar
  7. Barry-Hamilton V, Spangler R, Marshall D, McCauley S, Rodriguez HM, Oyasu M, Mikels A, Vaysberg M, Ghermazien H, Wai C, Garcia CA, Velayo AC, Jorgensen B, Biermann D, Tsai D, Green J, Zaffryar-Eilot S, Holzer A, Ogg S, Thai D, Neufeld G, Van VP, Smith V (2010) Allosteric inhibition of lysyl oxidase-like-2 impedes the development of a pathologic microenvironment. Nat Med 16:1009–1017PubMedGoogle Scholar
  8. Bertoletti A, D’Elios MM, Boni C, De Carli M, Zignego AL, Durazzo M, Missale G, Penna A, Fiaccadori F, Del Prete G, Ferrari C (1997) Different cytokine profiles of intraphepatic T cells in chronic hepatitis B and hepatitis C virus infections. Gastroenterology 112:193–199PubMedGoogle Scholar
  9. Blau K (1961) Chromatographic methods for the study of amines from biological material. Biochem J 80:193–200PubMedGoogle Scholar
  10. Bolt HM (1987) Experimental toxicology of formaldehyde. J Cancer Res Clin Oncol 113:305–309PubMedGoogle Scholar
  11. Bonder CS, Norman MU, Swain MG, Zbytnuik LD, Yamanouchi J, Santamaria P, Ajuebor M, Salmi M, Jalkanen S, Kubes P (2005) Rules of recruitment for Th1 and th2 lymphocytes in inflamed liver: a role for alpha-4 integrin and vascular adhesion protein-1. Immunity 23:153–163PubMedGoogle Scholar
  12. Bono P, Salmi M, Smith DJ, Jalkanen S (1998) Cloning and characterization of mouse vascular adhesion protein-1 reveals a novel molecule with enzymatic activity. J Immunol 160:5563–5571PubMedGoogle Scholar
  13. Bono P, Jalkanen S, Salmi M (1999) Mouse vascular adhesion protein 1 is a sialoglycoprotein with enzymatic activity and is induced in diabetic insulitis. Am J Pathol 155:1613–1624PubMedGoogle Scholar
  14. Boomsma F, van Veldhuisen DJ, de Kam PJ, Man-in ’t-Veld AJ, Mosterd A, Lie KI, Schalekamp MA (1997) Plasma semicarbazide-sensitive amine oxidase is elevated in patients with congestive heart failure. Cardiovasc Res 33:387–391Google Scholar
  15. Boor PJ, Trent MB, Lyles GA, Tao M, Ansari GA (1992) Methylamine metabolism to formaldehyde by vascular semicarbazide-sensitive amine oxidase. Toxicology 73:251–258PubMedGoogle Scholar
  16. Borchers AT, Shimoda S, Bowlus C, Keen CL, Gershwin ME (2009) Lymphocyte recruitment and homing to the liver in primary biliary cirrhosis and primary sclerosing cholangitis. Semin Immunopathol 31:309–322PubMedGoogle Scholar
  17. Crispe IN (2003) Hepatic T cells and liver tolerance. Nat Rev Immunol 3:51–62PubMedGoogle Scholar
  18. D’Souza SE, Ginsberg MH, Plow EF (1991) Arginyl-glycyl-aspartic acid (RGD): a cell adhesion motif. Trends Biochem Sci 16:246–250PubMedGoogle Scholar
  19. Day CP (2002) Pathogenesis of steatohepatitis. Best Pract Res Clin Gastroenterol 16:663–678PubMedGoogle Scholar
  20. Dunkel P, Gelain A, Barlocco D, Haider N, Gyires K, Sperlagh B, Magyar K, Maccioni E, Fadda A, Matyus P (2008) Semicarbazide-sensitive amine oxidase/vascular adhesion protein 1: recent developments concerning substrates and inhibitors of a promising therapeutic target. Curr Med Chem 15:1827–1839PubMedGoogle Scholar
  21. Elvevold K, Smedsrod B, Martinez I (2008) The liver sinusoidal endothelial cell: a cell type of controversial and confusing identity. Am J Physiol Gastrointest Liver Physiol 294:G391–G400PubMedGoogle Scholar
  22. Enrique-Tarancon G, Marti L, Morin N, Lizcano JM, Unzeta M, Sevilla L, Camps M, Palacin M, Testar X, Carpene C, Zorzano A (1998) Role of semicarbazide-sensitive amine oxidase on glucose transport and GLUT4 recruitment to the cell surface in adipose cells. J Biol Chem 273:8025–8032PubMedGoogle Scholar
  23. Enrique-Tarancon G, Castan I, Morin N, Marti L, Abella A, Camps M, Casamitjana R, Palacin M, Testar X, Degerman E, Carpene C, Zorzano A (2000) Substrates of semicarbazide-sensitive amine oxidase co-operate with vanadate to stimulate tyrosine phosphorylation of insulin-receptor- substrate proteins, phosphoinositide 3-kinase activity and GLUT4 translocation in adipose cells. Biochem J 350(Pt1):171–180Google Scholar
  24. Erler JT, Giaccia AJ (2006) Lysyl oxidase mediates hypoxic control of metastasis. Cancer Res 66:10238–10241PubMedGoogle Scholar
  25. Erler JT, Bennewith KL, Nicolau M, Dornhofer N, Kong C, Le QT, Chi JT, Jeffrey SS, Giaccia AJ (2006) Lysyl oxidase is essential for hypoxia-induced metastasis. Nature 440:1222–1226PubMedGoogle Scholar
  26. Erler JT, Bennewith KL, Cox TR, Lang G, Bird D, Koong A, Le QT, Giaccia AJ (2009) Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche. Cancer Cell 15:35–44PubMedGoogle Scholar
  27. Fleming TH, Humpert PM, Nawroth PP, Bierhaus A (2010) Reactive metabolites and AGE/RAGE-mediated cellular dysfunction affect the aging process—a mini-review. Gerontology. doi:10.1159/000322087
  28. Fontana E, Boucher J, Marti L, Lizcano JM, Testar X, Zorzano A, Carpene C (2001) Amine oxidase substrates mimic several of the insulin effects on adipocyte differentiation in 3T3 F442A cells. Biochem J 356:769–777PubMedGoogle Scholar
  29. Forster-Horvath C, Dome B, Paku S, Ladanyi A, Somlai B, Jalkanen S, Timar J (2004) Loss of vascular adhesion protein-1 expression in intratumoral microvessels of human skin melanoma. Melanoma Res 14:135–140PubMedGoogle Scholar
  30. Garcia-Monzon C, Sanchez-Madrid F, Garcia-Buey L, Garcia-Arroyo A, Garcia-Sanchez A, Moreno-Otero R (1995) Vascular adhesion molecule expression in viral chronic hepatitis: evidence of neoangiogenesis in portal tracts. Gastroenterology 108:231–241PubMedGoogle Scholar
  31. Garcia-Vicente S, Abella A, Viguerie N, Ros-Baro A, Camps M, Testar X, Palacin M, Zorzano A, Marti L (2005) The release of soluble VAP-1/SSAO by 3T3–L1 adipocytes is stimulated by isoproterenol and low concentrations of TNFalpha. J Physiol Biochem 61:395–401PubMedGoogle Scholar
  32. Grant AJ, Lalor PF, Hubscher SG, Briskin M, Adams DH (2001) MAdCAM-1 expressed in chronic inflammatory liver disease supports mucosal lymphocyte adhesion to hepatic endothelium (MAdCAM-1 in chronic inflammatory liver disease). Hepatology 33:1065–1072PubMedGoogle Scholar
  33. Gubisne-Haberle D, Hill W, Kazachkov M, Richardson JS, Yu PH (2004) Protein cross-linkage induced by formaldehyde derived from semicarbazide-sensitive amine oxidase-mediated deamination of methylamine. J Pharmacol Exp Ther 310:1125–1132PubMedGoogle Scholar
  34. Guimaraes EL, Empsen C, Geerts A, van Grunsven LA (2010) Advanced glycation end products induce production of reactive oxygen species via the activation of NADPH oxidase in murine hepatic stellate cells. J Hepatol 52:389–397PubMedGoogle Scholar
  35. Henderson NC, Iredale JP (2007) Liver fibrosis: cellular mechanisms of progression and resolution. Clin Sci (Lond) 112:265–280Google Scholar
  36. Humphrey W, Dalke A, Schulten K (1996) VMD—Visual molecular dynamics. J Molec Graphics 14:33–38Google Scholar
  37. Hyogo H, Yamagishi S (2008) Advanced glycation end products (AGEs) and their involvement in liver disease. Curr Pharm Des 14:969–972PubMedGoogle Scholar
  38. Iffiu-Soltesz Z, Wanecq E, Lomba A, Portillo MP, Pellati F, Szoko E, Bour S, Woodley J, Milagro FI, Alfredo MJ, Valet P, Carpene C (2010) Chronic benzylamine administration in the drinking water improves glucose tolerance, reduces body weight gain and circulating cholesterol in high-fat diet-fed mice. Pharmacol Res 61:355–363PubMedGoogle Scholar
  39. Irjala H, Salmi M, Alanen K, Grenman R, Jalkanen S (2001) Vascular adhesion protein 1 mediates binding of immunotherapeutic effector cells to tumor endothelium. J Immunol 166:6937–6943PubMedGoogle Scholar
  40. Jaakkola K, Jokimaa V, Kallajoki M, Jalkanen S, Ekholm E (2000) Pre-eclampsia does not change the adhesion molecule status in the placental bed. Placenta 21:133–141PubMedGoogle Scholar
  41. Jakobsson E, Nilsson J, Ogg D, Kleywegt GJ (2005) Structure of human semicarbazide-sensitive amine oxidase/vascular adhesion protein-1. Acta Crystallogr D Biol Crystallogr 61:1550–1562PubMedGoogle Scholar
  42. Jalkanen S, Salmi M (2001) Cell surface monoamine oxidases: enzymes in search of a function. EMBO J 20:3893–3901PubMedGoogle Scholar
  43. Jalkanen S, Karikoski M, Mercier N, Koskinen K, Henttinen T, Elima K, Salmivirta K, Salmi M (2007) The oxidase activity of vascular adhesion protein-1 (VAP-1) induces endothelial E- and P-selectins and leukocyte binding. Blood 110:1864–1870PubMedGoogle Scholar
  44. Kakumu S, Yoshioka K, Wakita T, Ishikawa T, Murase K, Kusakabe A, Kurokawa S (1990) Comparisons of peripheral blood and hepatic lymphocyte subpopulations and interferon production in chronic viral hepatitis. J Clin Lab Immunol 33:1–6PubMedGoogle Scholar
  45. Karadi I, Meszaros Z, Csanyi A, Szombathy T, Hosszufalusi N, Romics L, Magyar K (2002) Serum semicarbazide-sensitive amine oxidase (SSAO) activity is an independent marker of carotid atherosclerosis. Clin Chim Acta 323:139–146PubMedGoogle Scholar
  46. Karikoski M, Irjala H, Maksimow M, Miiluniemi M, Granfors K, Hernesniemi S, Elima K, Moldenhauer G, Schledzewski K, Kzhyshkowska J, Goerdt S, Salmi M, Jalkanen S (2009) Clever-1/Stabilin-1 regulates lymphocyte migration within lymphatics and leukocyte entrance to sites of inflammation. Eur J Immunol 39:3477–3487PubMedGoogle Scholar
  47. Karlmark KR, Weiskirchen R, Zimmermann HW, Gassler N, Ginhoux F, Weber C, Merad M, Luedde T, Trautwein C, Tacke F (2009) Hepatic recruitment of the inflammatory Gr1+ monocyte subset upon liver injury promotes hepatic fibrosis. Hepatology 50:261–274PubMedGoogle Scholar
  48. Kirton CM, Laukkanen ML, Nieminen A, Merinen M, Stolen CM, Armour K, Smith DJ, Salmi M, Jalkanen S, Clark MR (2005) Function-blocking antibodies to human vascular adhesion protein-1: a potential anti-inflammatory therapy. Eur J Immunol 35:3119–3130PubMedGoogle Scholar
  49. Kivi E, Elima K, Aalto K, Nymalm Y, Auvinen K, Koivunen E, Otto DM, Crocker PR, Salminen TA, Salmi M, Jalkanen S (2009) Human Siglec-10 can bind to vascular adhesion protein-1 and serves as its substrate. Blood 114:5385–5392PubMedGoogle Scholar
  50. Koskinen K, Vainio PJ, Smith DJ, Pihlavisto M, Yla-Herttuala S, Jalkanen S, Salmi M (2004) Granulocyte transmigration through endothelium is regulated by the oxidase activity of vascular adhesion protein-1 (VAP-1). Blood 103:3388–3395PubMedGoogle Scholar
  51. Kurkijarvi R, Adams DH, Leino R, Mottonen T, Jalkanen S, Salmi M (1998) Circulating form of human vascular adhesion protein-1 (VAP-1): increased serum levels in inflammatory liver diseases. J Immunol 161:1549–1557PubMedGoogle Scholar
  52. Kurkijarvi R, Yegutkin GG, Gunson BK, Jalkanen S, Salmi M, Adams DH (2000) Circulating soluble vascular adhesion protein 1 accounts for the increased serum monoamine oxidase activity in chronic liver disease. Gastroenterology 119:1096–1103PubMedGoogle Scholar
  53. Kurkijarvi R, Jalkanen S, Isoniemi H, Salmi M (2001) Vascular adhesion protein-1 (VAP-1) mediates lymphocyte–endothelial interactions in chronic kidney rejection. Eur J Immunol 31:2876–2884PubMedGoogle Scholar
  54. Lalor PF, Edwards S, McNab G, Salmi M, Jalkanen S, Adams DH (2002a) Vascular adhesion protein-1 mediates adhesion and transmigration of lymphocytes on human hepatic endothelial cells. J Immunol 169:983–992PubMedGoogle Scholar
  55. Lalor PF, Shields P, Grant A, Adams DH (2002b) Recruitment of lymphocytes to the human liver. Immunol Cell Biol 80:52–64PubMedGoogle Scholar
  56. Lalor PF, Lai WK, Curbishley SM, Shetty S, Adams DH (2006) Human hepatic sinusoidal endothelial cells can be distinguished by expression of phenotypic markers related to their specialised functions in vivo. World J Gastroenterol 12:5429–5439PubMedGoogle Scholar
  57. Lalor PF, Sun PJ, Weston CJ, Martin-Santos A, Wakelam MJ, Adams DH (2007) Activation of vascular adhesion protein-1 on liver endothelium results in an NF-kappaB-dependent increase in lymphocyte adhesion. Hepatology 45:465–474PubMedGoogle Scholar
  58. Levental KR, Yu H, Kass L, Lakins JN, Egeblad M, Erler JT, Fong SF, Csiszar K, Giaccia A, Weninger W, Yamauchi M, Gasser DL, Weaver VM (2009) Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139:891–906PubMedGoogle Scholar
  59. Lewinsohn R (1977) Human serum amine oxidase enzyme activity in severely burnt patients and in patients with cancer. Clin Chim Acta 81:247–256PubMedGoogle Scholar
  60. Lewinsohn R (1978) Benzylamine oxidase. Lancet 311:483Google Scholar
  61. Lewinsohn R (1984) Mammalian monoamine-oxidizing enzymes, with special reference to benzylamine oxidase in human tissues. Brazilian J Med Biol Res 17:233–256Google Scholar
  62. Liaskou E, Karikoski M, Reynolds GM, Lalor PF, Weston CJ, Pullen N, Salmi M, Jalkanen S, Adams DH (2011) Regulation of mucosal addressin cell adhesion molecule 1 expression in human and mice by vascular adhesion protein 1 amine oxidase activity. Hepatology 53:661–672PubMedGoogle Scholar
  63. Lohwasser C, Neureiter D, Popov Y, Bauer M, Schuppan D (2009) Role of the receptor for advanced glycation end products in hepatic fibrosis. World J Gastroenterol 15:5789–5798PubMedGoogle Scholar
  64. Lyles GA (1995) Substrate-specificity of mammalian tissue-bound semicarbazide-sensitive amine oxidase. Prog Brain Res 106:293–303PubMedGoogle Scholar
  65. Lyles GA (1996) Mammalian plasma and tissue-bound semicarbazide-sensitive amine oxidases: biochemical, pharmacological and toxicological aspects. Int J Biochem Cell Biol 28:259–274PubMedGoogle Scholar
  66. Lyles GA, Chalmers J (1992) The metabolism of aminoacetone to methylglyoxal by semicarbazide-sensitive amine oxidase in human umbilical artery. Biochem Pharmacol 43:1409–1414PubMedGoogle Scholar
  67. Lyles GA, McDougall SA (1989) The enhanced daily excretion of urinary methylamine in rats treated with semicarbazide or hydralazine may be related to the inhibition of semicarbazide-sensitive amine oxidase activities. J Pharm Pharmacol 41:97–100PubMedGoogle Scholar
  68. Martelius T, Salaspuro V, Salmi M, Krogerus L, Hockerstedt K, Jalkanen S, Lautenschlager I (2004) Blockade of vascular adhesion protein-1 inhibits lymphocyte infiltration in rat liver allograft rejection. Am J Pathol 165:1993–2001PubMedGoogle Scholar
  69. Marttila-Ichihara F, Auvinen K, Elima K, Jalkanen S, Salmi M (2009) Vascular adhesion protein-1 enhances tumor growth by supporting recruitment of Gr-1+CD11b+ myeloid cells into tumors. Cancer Res 69:7875–7883PubMedGoogle Scholar
  70. Marttila-Ichihara F, Castermans K, Auvinen K, Oude Egbrink MG, Jalkanen S, Griffioen AW, Salmi M (2010) Small-molecule inhibitors of vascular adhesion protein-1 reduce the accumulation of myeloid cells into tumors and attenuate tumor growth in mice. J Immunol 184:3164–3173PubMedGoogle Scholar
  71. Maula SM, Salminen T, Kaitaniemi S, Nymalm Y, Smith DJ, Jalkanen S (2005) Carbohydrates located on the top of the “cap” contribute to the adhesive and enzymatic functions of vascular adhesion protein-1. Eur J Immunol 35:2718–2727PubMedGoogle Scholar
  72. McNab G, Reeves JL, Salmi M, Hubscher S, Jalkanen S, Adams DH (1996) Vascular adhesion protein 1 mediates binding of T cells to human hepatic endothelium. Gastroenterology 110:522–528PubMedGoogle Scholar
  73. Mercier N, Kakou A, Challande P, Lacolley P, Osborne-Pellegrin M (2009) Comparison of the effects of semicarbazide and beta-aminopropionitrile on the arterial extracellular matrix in the Brown Norway rat. Toxicol Appl Pharmacol 239:258–267PubMedGoogle Scholar
  74. Merinen M, Irjala H, Salmi M, Jaakkola I, Hanninen A, Jalkanen S (2005) Vascular adhesion protein-1 is involved in both acute and chronic inflammation in the mouse. Am J Pathol 166:793–800PubMedGoogle Scholar
  75. Mestas J, Hughes CC (2004) Of mice and not men: differences between mouse and human immunology. J Immunol 172:2731–2738PubMedGoogle Scholar
  76. Meszaros Z, Szombathy T, Raimondi L, Karadi I, Romics L, Magyar K (1999) Elevated serum semicarbazide-sensitive amine oxidase activity in non-insulin-dependent diabetes mellitus: correlation with body mass index and serum triglyceride. Metabolism 48:113–117PubMedGoogle Scholar
  77. Morin N, Lizcano JM, Fontana E, Marti L, Smih F, Rouet P, Prevot D, Zorzano A, Unzeta M, Carpene C (2001) Semicarbazide-sensitive amine oxidase substrates stimulate glucose transport and inhibit lipolysis in human adipocytes. J Pharmacol Exp Ther 297:563–572PubMedGoogle Scholar
  78. Morsy MA, Norman PJ, Mitry R, Rela M, Heaton ND, Vaughan RW (2005) Isolation, purification and flow cytometric analysis of human intrahepatic lymphocytes using an improved technique. Lab Invest 85:285–296PubMedGoogle Scholar
  79. Murakami J, Shimizu Y, Kashii Y, Kato T, Minemura M, Okada K, Nambu S, Takahara T, Higuchi K, Maeda Y, Kumada T, Watanabe A (1999) Functional B-cell response in intrahepatic lymphoid follicles in chronic hepatitis C. Hepatology 30:143–150PubMedGoogle Scholar
  80. Napoli J, Bishop GA, McGuinness PH, Painter DM, McCaughan GW (1996) Progressive liver injury in chronic hepatitis C infection correlates with increased intrahepatic expression of Th1-associated cytokines. Hepatology 24:759–765PubMedGoogle Scholar
  81. Niethammer P, Grabher C, Look AT, Mitchison TJ (2009) A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature 459:996–999PubMedGoogle Scholar
  82. Nixon R (1972) Volatile amines in mouse brain: a radioassay with picogram sensitivity. Anal Biochem 48:460–470PubMedGoogle Scholar
  83. O’Rourke AM, Wang EY, Miller A, Podar EM, Scheyhing K, Huang L, Kessler C, Gao H, Ton-Nu HT, Macdonald MT, Jones DS, Linnik MD (2008) 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 324:867–875PubMedGoogle Scholar
  84. Palfreyman MG, McDonald IA, Bey P, Danzin C, Zreika M, Cremer G (1994). Haloallylamine inhibitors of MAO and SSAO and their therapeutic potential. J Neural Transm Suppl 41:407–414Google Scholar
  85. Papaharalambus CA, Griendling KK (2007) Basic mechanisms of oxidative stress and reactive oxygen species in cardiovascular injury. Trends Cardiovasc Med 17:48–54PubMedGoogle Scholar
  86. Pfundstein B, Tricker AR, Preussmann R (1991) Determination of primary and secondary amines in foodstuffs using gas chromatography and chemiluminescence detection with a modified thermal energy analyser. J Chromatogr 539:141–148PubMedGoogle Scholar
  87. Precious E, Gunn CE, Lyles GA (1988) Deamination of methylamine by semicarbazide-sensitive amine oxidase in human umbilical artery and rat aorta. Biochem Pharmacol 37:707–713PubMedGoogle Scholar
  88. Ramaiah SK, Jaeschke H (2007) Role of neutrophils in the pathogenesis of acute inflammatory liver injury. Toxicol Pathol 35:757–766PubMedGoogle Scholar
  89. Rodriguez C, Martinez-Gonzalez J, Raposo B, Alcudia JF, Guadall A, Badimon L (2008) Regulation of lysyl oxidase in vascular cells: lysyl oxidase as a new player in cardiovascular diseases. Cardiovasc Res 79:7–13PubMedGoogle Scholar
  90. Salmi M, Jalkanen S (1992) A 90-kilodalton endothelial cell molecule mediating lymphocyte binding in humans. Science 257:1407–1409PubMedGoogle Scholar
  91. Salmi M, Jalkanen S (1996) Human vascular adhesion protein-1 (vap-1) is a unique sialoglycoprotein that mediates carbohydrate-dependent binding of lymphocytes to endothelial-cells. J Exp Med 183:569–579PubMedGoogle Scholar
  92. Salmi M, Jalkanen S (2005) Cell-surface enzymes in control of leukocyte trafficking. Nat Rev Immunol 5:760–771PubMedGoogle Scholar
  93. Salmi M, Jalkanen S (2006) Developmental regulation of the adhesive and enzymatic activity of vascular adhesion protein-1 (VAP-1) in humans. Blood 108:1555–1561PubMedGoogle Scholar
  94. Salmi M, Kalimo K, Jalkanen S (1993) Induction and function of vascular adhesion protein-1 at sites of inflammation. J Exp Med 178:2255–2260PubMedGoogle Scholar
  95. Salmi M, Tohka S, Berg EL, Butcher EC, Jalkanen S (1997) Vascular adhesion protein 1 (VAP-1) mediates lymphocyte subtype-specific, selectin-independent recognition of vascular endothelium in human lymph nodes. J Exp Med 186:589–600PubMedGoogle Scholar
  96. Salmi M, Hellman J, Jalkanen S (1998) The role of two distinct endothelial molecules, vascular adhesion protein-1 and peripheral lymph node addressin, in the binding of lymphocyte subsets to human lymph nodes. J Immunol 160:5629–5636PubMedGoogle Scholar
  97. Salmi M, Tohka S, Jalkanen S (2000) Human vascular adhesion protein-1 (VAP-1) plays a critical role in lymphocyte–endothelial cell adhesion cascade under shear. Circ Res 86:1245–1251 (see comments)PubMedGoogle Scholar
  98. Salmi M, Stolen C, Jousilahti P, Yegutkin GG, Tapanainen P, Janatuinen T, Knip M, Jalkanen S, Salomaa V (2002) Insulin-regulated increase of soluble vascular adhesion protein-1 in diabetes. Am J Pathol 161:2255–2262PubMedGoogle Scholar
  99. Salmi M, Koskinen K, Henttinen T, Elima K, Jalkanen S (2004) CLEVER-1 mediates lymphocyte transmigration through vascular and lymphatic endothelium. Blood 104:3849–3857PubMedGoogle Scholar
  100. Schmeltz I, Hoffmann D (1977) Nitrogen-containing compounds in tobacco and tobacco smoke. Chem Rev 77:295–311Google Scholar
  101. Schwelberger HG (2007) The origin of mammalian plasma amine oxidases. J Neural Transm 114:757–762PubMedGoogle Scholar
  102. Schwelberger HG (2010) Structural organization of mammalian copper-containing amine oxidase genes. Inflamm Res 59 Suppl 2:S223–S225Google Scholar
  103. Sebela M, Sayre LM (2009) Inhibitors of copper amine oxidases: past, present, and future. In: Floris G, Mondovi B, (eds) Copper amine oxidases: structures, catalytic mechanisms, and role in pathophysiology. CRC Press, USA, pp 219–237Google Scholar
  104. Seiler N (2002) Ammonia and Alzheimer’s disease. Neurochem Int 41:189–207PubMedGoogle Scholar
  105. Shields PL, Morland CM, Salmon M, Qin S, Hubscher SG, Adams DH (1999) Chemokine and chemokine receptor interactions provide a mechanism for selective T cell recruitment to specific liver compartments within hepatitis C-infected liver. J Immunol 163:6236–6243PubMedGoogle Scholar
  106. Smith DJ, Salmi M, Bono P, Hellman J, Leu T, Jalkanen S (1998) Cloning of vascular adhesion protein 1 reveals a novel multifunctional adhesion molecule. J Exp Med 188:17–27PubMedGoogle Scholar
  107. Sole M, Hernandez-Guillamon M, Boada M, Unzeta M (2008) p53 phosphorylation is involved in vascular cell death induced by the catalytic activity of membrane-bound SSAO/VAP-1. Biochim Biophys Acta 1783:1085–1094PubMedGoogle Scholar
  108. Stedman RL (1968) The chemical composition of tobacco and tobacco smoke. Chem Rev 68:153–207PubMedGoogle Scholar
  109. Stolen CM, Madanat R, Marti L, Kari S, Yegutkin GG, Sariola H, Zorzano A, Jalkanen S (2004a) Semicarbazide sensitive amine oxidase overexpression has dual consequences: insulin mimicry and diabetes-like complications. FASEB J 18:702–704PubMedGoogle Scholar
  110. Stolen CM, Yegutkin GG, Kurkijarvi R, Bono P, Alitalo K, Jalkanen S (2004b) Origins of serum semicarbazide-sensitive amine oxidase. Circ Res 95:50–57PubMedGoogle Scholar
  111. Stolen CM, Marttila-Ichihara F, Koskinen K, Yegutkin GG, Turja R, Bono P, Skurnik M, Hanninen A, Jalkanen S, Salmi M (2005) Absence of the endothelial oxidase AOC3 leads to abnormal leukocyte traffic in vivo. Immunity 22:105–115PubMedGoogle Scholar
  112. Strauss-Ayali D, Conrad SM, Mosser DM (2007) Monocyte subpopulations and their differentiation patterns during infection. J Leukoc Biol 82:244–252PubMedGoogle Scholar
  113. Taniyama Y, Griendling KK (2003) Reactive oxygen species in the vasculature: molecular and cellular mechanisms. Hypertension 42:1075–1081PubMedGoogle Scholar
  114. Tjandra K, Sharkey KA, Swain MG (2000) Progressive development of a Th1-type hepatic cytokine profile in rats with experimental cholangitis. Hepatology 31:280–290PubMedGoogle Scholar
  115. Tohka S, Laukkanen M, Jalkanen S, Salmi M (2001) Vascular adhesion protein 1 (VAP-1) functions as a molecular brake during granulocyte rolling and mediates recruitment in vivo. FASEB J 15:373–382PubMedGoogle Scholar
  116. Toiyama Y, Miki C, Inoue Y, Kawamoto A, Kusunoki M (2009) 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 99:368–372PubMedGoogle Scholar
  117. Vainio PJ, Kortekangas-Savolainen O, Mikkola JH, Jaakkola K, Kalimo K, Jalkanen S, Veromaa T (2005) Safety of blocking vascular adhesion protein-1 in patients with contact dermatitis. Basic Clin Pharmacol Toxicol 96:429–435PubMedGoogle Scholar
  118. Wong J, Johnston B, Lee SS, Bullard DC, Smith CW, Beaudet AL, Kubes P (1997) A minimal role for selectins in the recruitment of leukocytes into the inflamed liver microvasculature. J Clin Invest 99:2782–2790PubMedGoogle Scholar
  119. Xiao S, Yu PH (2009) A fluorometric high-performance liquid chromatography procedure for simultaneous determination of methylamine and aminoacetone in blood and tissues. Anal Biochem 384:20–26PubMedGoogle Scholar
  120. Yang M, Butler M (2002) Effects of ammonia and glucosamine on the heterogeneity of erythropoietin glycoforms. Biotechnol Prog 18:129–138PubMedGoogle Scholar
  121. Yoong KF, McNab G, Hubscher SG, Adams DH (1998) Vascular adhesion protein-1 and ICAM-1 support the adhesion of tumor-infiltrating lymphocytes to tumor endothelium in human hepatocellular carcinoma. J Immunol 160:3978–3988PubMedGoogle Scholar
  122. Yraola F, Albericio F, Royo M (2007) Inhibition of VAP1: quickly gaining ground as an anti-inflammatory therapy. Chem Med Chem 2:173–174PubMedGoogle Scholar
  123. Yu PH, Dyck RF (1998) Impairment of methylamine clearance in uremic patients and its nephropathological implications. Clin Nephrol 49:299–302PubMedGoogle Scholar
  124. Yu PH, Wright S, Fan EH, Lun ZR, Gubisne-Harberle D (2003) Physiological and pathological implications of semicarbazide-sensitive amine oxidase. Biochim Biophys Acta 1647:193–199PubMedGoogle Scholar
  125. Ziegler-Heitbrock HW, Fingerle G, Strobel M, Schraut W, Stelter F, Schutt C, Passlick B, Pforte A (1993) The novel subset of CD14+/CD16+ blood monocytes exhibits features of tissue macrophages. Eur J Immunol 23:2053–2058PubMedGoogle Scholar

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© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Centre for Liver Research and NIHR Biomedical Research Unit, 5th Floor, Institute of Biomedical Research, MRC Centre for Immune Regulation, College of Medicine and DentistryUniversity of BirminghamBirminghamUK

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