Upregulation of Vascular Endothelial Growth Factor Receptor-3 in the Spinal Cord of Lewis Rats with Experimental Autoimmune Encephalomyelitis

Journal of Histochemistry and Cytochemistry

Volumn 61, Issue 1, 2013, Pages 31-44

  Park, Jang Mi ^a   Shin, Yoo Jin ^a   Cho, Jeong Min ^a   Choi, Jae Youn ^a   Jeun, Sin Soo ^a   Cha, Jung Ho ^a   Lee, Mun Yong ^a  

^a The Catholic University of Korea   (South Korea)

Author keywords

experimental autoimmune encephalomyelitis; macrophage; microglia; reactive astrocyte; VEGFR 3

Indexed keywords

VASCULOTROPIN RECEPTOR 3; MESSENGER RNA; VASCULOTROPIN C;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; GRAY MATTER; LEWIS RAT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL CORD; WHITE MATTER; ACUTE DISEASE; ANIMAL; BIOSYNTHESIS; GENETICS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MACROPHAGE; METABOLISM; MICROGLIA; NERVE CELL; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION;

ANIMALIA; RATTUS;

ACUTE DISEASE; ANIMALS; ASTROCYTES; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MACROPHAGES; MICROGLIA; NEURONS; RATS; RATS, INBRED LEW; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; SPINAL CORD; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR C; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-3;

EID: 84874512668     PISSN: 00221554     EISSN: None     Source Type: Journal    
DOI: 10.1369/0022155412462975     Document Type: Article

References (60)

1. Ajami B,Bennett JL,Krieger C,McNagny KM,Rossi FM.Infiltrating monocytes trigger EAE progression, but do not contribute to the resident microglia pool.Nat Neurosci. 2011;14:1142-1149.
2. Almolda B,Costa M,Montoya M,González B,Castellano BJ.CD4 microglial expression correlates with spontaneous clinical improvement in the acute Lewis rat EAE model.J Neuroimmunol. 2009;209:65-80.
3. Almolda B,Gonzalez B,Castellano B.Antigen presentation in EAE: role of microglia, macrophages and dendritic cells.Front Biosci. 2011;16:1157-1171.
4. Aquino DA,Chiu FC,Brosnan CF,Norton WT.Glial fibrillary acidic protein increases in the spinal cord of Lewis rats with acute experimental autoimmune encephalomyelitis.J Neurochem. 1988;51:1085-1096.
5. Bauer J,Huitinga I,Zhao W,Lassmann H,Hickey WF,Dijkstra CD.The role of macrophages, perivascular cells, and microglial cells in the pathogenesis of experimental autoimmune encephalomyelitis.Glia. 1995;15:437-446.
6. Benveniste EN.Role of macrophages/microglia in multiple sclerosis and experimental allergic encephalomyelitis.J Mol Med. 1997;75:165-173.
7. Bø L,Vedeler CA,Nyland H,Trapp BD,Mørk SJ.Intracortical multiple sclerosis lesions are not associated with increased lymphocyte infiltration.Mult Scler. 2003;9:323-331.
8. Brosnan CF,Bornstein MB,Bloom BR.The effects of macrophage depletion on the clinical and pathologic expression of experimental allergic encephalomyelitis.J Immunol. 1981;126:614-620.
9. Calvo CF,Fontaine RH,Soueid J,Tammela T,Makinen T,Alfaro-Cervello C,Bonnaud F,Miguez A,Benhaim L,Xu Y, et al.Vascular endothelial growth factor receptor 3 directly regulates murine neurogenesis.Genes Dev. 2011;25:831-844.
10. Cassan C,Liblau RS.Immune tolerance and control of CNS autoimmunity: from animal models to MS patients.J Neurochem. 2007;100:883-892.
11. Centonze D,Muzio L,Rossi S,Furlan R,Bernardi G,Martino G.The link between inflammation, synaptic transmission and neurodegeneration in multiple sclerosis.Cell Death Differ. 2010;17:1083-1091.
12. Chastain EM,Duncan DS,Rodgers JM,Miller SD.The role of antigen presenting cells in multiple sclerosis.Biochim Biophys Acta. 2011;1812:265-274.
13. Chen L,Hamrah P,Cursiefen C,Zhang Q,Pytowski B,Streilein JW,Dana MR.Vascular endothelial growth factor receptor-3 mediates induction of corneal alloimmunity.Ocul Immunol Inflamm. 2007;15:275-278.
14. Compston A,Coles A.Multiple sclerosis.Lancet. 2008;372:1502-1517.
15. del Valle J,Camins A,Pallàs M,Vilaplana J,Pelegrí C.A new method for determining blood-brain barrier integrity based on intracardiac perfusion of an Evans Blue-Hoechst cocktail.J Neurosci Methods. 2008;174:42-49.
16. Frohman EM,Racke MK,Raine CS.Multiple sclerosis-the plaque and its pathogenesis.N Engl J Med. 2006;354:942-955.
17. Gandhi R,Laroni A,Weiner HL.Role of the innate immune system in the pathogenesis of multiple sclerosis.J Neuroimmunol. 2010;221:7-14.
18. Gao H,Gao Y,Li X,Shen A,Yan M.Spatiotemporal patterns of dexamethasone-induced Ras protein 1 expression in the central nervous system of rats with experimental autoimmune encephalomyelitis.J Mol Neurosci. 2010;41:198-209.
19. Gentleman SM,Nash MJ,Sweeting CJ,Graham DI,Roberts GW.Beta-amyloid precursor protein (beta APP) as a marker for axonal injury after head injury.Neurosci Lett. 1993;160:139-144.
20. Graeber MB,Streit WJ.Microglia: biology and pathology.Acta Neuropathol. 2010;119:89-105.
21. Guillemin GJ,Brew BJ.Microglia, macrophages, perivascular macrophages, and pericytes: a review of function and identification.J Leukoc Biol. 2004;75:388-397.
22. Hamrah P,Chen L,Cursiefen C,Zhang Q,Joyce NC,Dana MR.Expression of vascular endothelial growth factor receptor-3 (VEGFR-3) on monocytic bone marrow-derived cells in the conjunctiva.Exp Eye Res. 2004;79:553-561.
23. Hamrah P,Chen L,Zhang Q,Dana MR.Novel expression of vascular endothelial growth factor receptor (VEGFR)-3 and VEGF-C on corneal dendritic cells.Am J Pathol. 2003;163:57-68.
24. Heppner FL,Greter M,Marino D,Falsig J,Raivich G,Hövelmeyer N,Waisman A,Rülicke T,Prinz M,Priller J, et al.Experimental autoimmune encephalomyelitis repressed by microglial paralysis.Nat Med. 2005;11:146-152.
25. Huitinga I,van Rooijen N,de Groot CJ,Uitdehaag BM,Dijkstra CD.Suppression of experimental allergic encephalomyelitis in Lewis rats after elimination of macrophages.J Exp Med. 1990;172:1025-1033.
26. Itoyama Y,Webster HD.Immunocytochemical study of myelin-associated glycoprotein (MAG) and basic protein (BP) in acute experimental allergic encephalomyelitis (EAE).J Neuroimmunol. 1982;3:351-364.
27. Kirk SL,Karlik SJ.VEGF and vascular changes in chronic neuroinflammation.J Autoimmun. 2003;21:353-363.
28. Kofler J,Wiley CA.Microglia: key innate immune cells of the brain. Toxicol Pathol. 2010;39:103-114.
29. Ladeby R,Wirenfeldt M,Garcia-Ovejero D,Fenger C,Dissing-Olesen L,Dalmau I,Finsen B.Microglial cell population dynamics in the injured adult central nervous system.Brain Res Brain Res Rev. 2005;48:196-206.
30. Lassmann H,Wisniewski HM.Chronic relapsing experimental allergic encephalomyelitis: morphological sequence of myelin degradation.Brain Res. 1979;169:357-368.
31. Le Bras B,Barallobre MJ,Homman-Ludiye J,Ny A,Wyns S,Tammela T,Haiko P,Karkkainen MJ,Yuan L,Muriel MP, et al.VEGF-C is a trophic factor for neural progenitors in the vertebrate embryonic brain.Nat Neurosci. 2006;9:340-348.
32. Lee J,Gray A,Yuan J,Luoh SM,Avraham H,Wood WI.Vascular endothelial growth factor-related protein: a ligand and specific activator of the tyrosine kinase receptor Flt4.Proc Natl Acad Sci U S A. 1996;93:1988-1992.
33. Li L,Liu F,Welser-Alves JV,McCullough LD,Milner R.Upregulation of fibronectin and the α5β1 and αvβ3 integrins on blood vessels within the cerebral ischemic penumbra.Exp Neurol. 2012;233:283-291.
34. Liedtke W,Edelmann W,Chiu FC,Kucherlapati R,Raine CS.Experimental autoimmune encephalomyelitis in mice lacking glial fibrillary acidic protein is characterized by a more severe clinical course and an infiltrative central nervous system lesion.Am J Pathol. 1998;152:251-259.
35. Matsumoto Y,Ohmori K,Fujiwara M.Microglial and astroglial reactions to inflammatory lesions of experimental autoimmune encephalomyelitis in the rat central nervous system.J Neuroimmunol. 1992;37:23-33.
36. Matsuo A,Lee GC,Terai K,Takami K,Hickey WF,McGeer EG,McGeer PL.Unmasking of an unusual myelin basic protein epitope during the process of myelin degeneration in humans: a potential mechanism for the generation of autoantigens.Am J Pathol. 1997;150:1253-1266.
37. Milner R,Hung S,Erokwu B,Dore-Duffy P,LaManna JC,del Zoppo GJ.Increased expression of fibronectin and the alpha 5 beta 1 integrin in angiogenic cerebral blood vessels of mice subject to hypobaric hypoxia.Mol Cell Neurosci. 2008;38:43-52.
38. Moore GR.Current concepts in the neuropathology and pathogenesis of multiple sclerosis.Can J Neurol Sci. 2010;37:S5-15.
39. Morita S,Miyata S.Different vascular permeability between the sensory and secretory circumventricular organs of adult mouse brain.Cell Tissue Res. 2012;349:589-603.
40. Moxon-Emre I,Schlichter LC.Evolution of inflammation and white matter injury in a model of transient focal ischemia.J Neuropathol Exp Neurol. 2010;69:1-15.
41. Penninger JM,Irie-Sasaki J,Sasaki T,Oliveira-dos-Santos AJ.CD45: new jobs for an old acquaintance.Nat Immunol. 2001;2:389-396.
42. Petrova TV,Bono P,Holnthoner W,Chesnes J,Pytowski B,Sihto H,Laakkonen P,Heikkilä P,Joensuu H,Alitalo K.VEGFR-3 expression is restricted to blood and lymphatic vessels in solid tumors.Cancer Cell. 2008;13:554-556.
43. Polfliet MM,van de,Veerdonk F,Döpp EA,van Kesteren-Hendrikx EM,van Rooijen N,Dijkstra CD,van den Berg TK.The role of perivascular and meningeal macrophages in experimental allergic encephalomyelitis.J Neuroimmunol. 2002;122:1-8.
44. Proescholdt MA,Jacobson S,Tresser N,Oldfield EH,Merrill MJ.Vascular endothelial growth factor is expressed in multiple sclerosis plaques and can induce inflammatory lesions in experimental allergic encephalomyelitis rats.J Neuropathol Exp Neurol. 2002;61:914-925.
45. Raivich G,Banati R.Brain microglia and blood-derived macrophages: molecular profiles and functional roles in multiple sclerosis and animal models of autoimmune demyelinating disease.Brain Res Brain Res Rev. 2004;46:261-281.
46. Saria A,Lundberg JM.Evans blue fluorescence: quantitative and morphological evaluation of vascular permeability in animal tissues.J Neurosci Methods. 1983;8:41-49.
47. Sasaki M,Lankford KL,Brown RJ,Ruddle NH,Kocsis JD.Focal experimental autoimmune encephalomyelitis in the Lewis rat induced by immunization with myelin oligodendrocyte glycoprotein and intraspinal injection of vascular endothelial growth factor.Glia. 2010;58:1523-1531.
48. Seabrook TJ,Littlewood-Evans A,Brinkmann V,Pöllinger B,Schnell C,Hiestand PC.Angiogenesis is present in experimental autoimmune encephalomyelitis and pro-angiogenic factors are increased in multiple sclerosis lesions.J Neuroinflammation. 2010;22:7-95.
49. Shin YJ,Choi JS,Choi JY,Hou Y,Cha JH,Chun MH,Lee MY.Induction of vascular endothelial growth factor receptor-3 mRNA in glial cells following focal cerebral ischemia in rats.J Neuroimmunol. 2010;229:81-90.
50. Shin YJ,Choi JS,Lee JY,Choi JY,Cha JH,Chun MH,Lee MY.Differential regulation of vascular endothelial growth factor-C and its receptor in the rat hippocampus following transient forebrain ischemia.Acta Neuropathol. 2008;116:517-527.
51. Skobe M,Hamberg LM,Hawighorst T,Schirner M,Wolf GL,Alitalo K,Detmar M.Concurrent induction of lymphangiogenesis, angiogenesis, and macrophage recruitment by vascular endothelial growth factor-C in melanoma.Am J Pathol. 2001;159:893-903.
52. Slavin A,Kelly-Modis L,Labadia M,Ryan K,Brown ML.Pathogenic mechanisms and experimental models of multiple sclerosis.Autoimmunity. 2010;43:504-513.
53. Stepanova OI,Krylov AV,Lioudyno VI,Kisseleva EP.Gene expression for VEGF-A, VEGF-C, and their receptors in murine lymphocytes and macrophages.Biochemistry. 2007;72:1194-1198.
54. Strbian D,Durukan A,Pitkonen M,Marinkovic I,Tatlisumak E,Pedrono E,Abo-Ramadan U,Tatlisumak T.The blood-brain barrier is continuously open for several weeks following transient focal cerebral ischemia.Neuroscience. 2008;153:175-181.
55. Su JJ,Osoegawa M,Matsuoka T,Minohara M,Tanaka M,Ishizu T,Mihara F,Taniwaki T,Kira J.Upregulation of vascular growth factors in multiple sclerosis: correlation with MRI findings.J Neurol Sci. 2006;243:21-30.
56. Tham E,Gielen AW,Khademi M,Martin C,Piehl F.Decreased expression of VEGF-A in rat experimental autoimmune encephalomyelitis and in cerebrospinal fluid mononuclear cells from patients with multiple sclerosis.Scand J Immunol. 2006;64:609-622.
57. Toft-Hansen H,Füchtbauer L,Owens T.Inhibition of reactive astrocytosis in established experimental autoimmune encephalomyelitis favors infiltration by myeloid cells over T cells and enhances severity of disease.Glia. 2011;59:166-176.
58. Voskuhl RR,Peterson RS,Song B,Ao Y,Morales LB,Tiwari-Woodruff S,Sofroniew MV.Reactive astrocytes form scar-like perivascular barriers to leukocytes during adaptive immune inflammation of the CNS.J Neurosci. 2009;29:11511-11522.
59. Wu J,Ohlsson M,Warner EA,Loo KK,Hoang TX,Voskuhl RR,Havton LA.Glial reactions and degeneration of myelinated processes in spinal cord gray matter in chronic experimental autoimmune encephalomyelitis.Neuroscience. 2008;156:586-596.
60. Zhu CS,Hu XQ,Xiong ZJ,Lu ZQ,Zhou GY,Wang DJ.Adenoviral delivery of soluble VEGF receptor 1 (sFlt-1) inhibits experimental autoimmune encephalomyelitis in dark Agouti (DA) rats.Life Sci. 2008;83:404-412.