Expression of vascular endothelial growth factor (VEGF) mRNA, VEGF receptor 2 (Flk-1) mRNA, and of VEGF co-receptor neuropilin (Nrp)-1 mRNA in brain tissue of aging Tg2576 mice by in situ hybridization

International Journal of Developmental Neuroscience

Volumn 43, Issue , 2015, Pages 25-34

  Muche, Abebe ^a,b   Bigl, Marina ^b   Arendt, Thomas ^b   Schliebs, Reinhard ^b  

^a UNIVERSITY OF GONDAR   (Ethiopia)

^b UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

Beta amyloid plaques; Flk 1 mRNA; Nrp 1 mRNA; Transgenic mouse brain; VEGF mRNA

Indexed keywords

AMYLOID BETA PROTEIN; MESSENGER RNA; NEUROPILIN 1; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2; AMYLOID PRECURSOR PROTEIN; PRION; VASCULOTROPIN A;

ADULT; AGING; AMYLOID PLAQUE; ANIMAL TISSUE; ARTICLE; BRAIN; CONTROLLED STUDY; ENTORHINAL CORTEX; FLK 1 GENE; FRONTAL CORTEX; GENE EXPRESSION; GENE LOCATION; HIPPOCAMPUS; IN SITU HYBRIDIZATION; MALE; MOUSE; NONHUMAN; NRP 1 GENE; PRIORITY JOURNAL; PYRIFORM CORTEX; RNA TRANSCRIPTION; UPREGULATION; VEGF GENE; WILD TYPE; ANIMAL; C57BL MOUSE; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HAMSTER; HUMAN; METABOLISM; MUTATION; PRION; TRANSGENIC MOUSE;

MUS; MUS MUSCULUS;

AGING; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BRAIN; CRICETINAE; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUTATION; NEUROPILIN-1; PRIONS; RNA, MESSENGER; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84927749804     PISSN: 07365748     EISSN: 1873474X     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2015.03.003     Document Type: Article

References (61)

1. Apelt J., Bigl M., Wunderlich P., Schliebs R. Aging-related increase in oxidative stress correlates with developmental pattern of beta-secretase activity and beta-amyloid plaque formation in transgenic Tg2576 mice with Alzheimer-like pathology. Int. J. Dev. Neurosci. 2004, 22:475-484.
2. Bao X., Feng M., Wei J., Han Q., Zhao H., Li G., Zhu Z., Xing H., An Y., Qin C., et al. Transplantation of Flk-1+ human bone marrow-derived mesenchymal stem cells promotes angiogenesis and neurogenesis after cerebral ischemia in rats. Eur. J. Neurosci. 2011, 34:87-98.
3. Bates D.O., Harper S.J. Regulation of vascular permeability by vascular endothelial growth factors. Vasc. Pharmacol. 2002, 39:225-237.
4. Berchtold N.C., Cribbs D.H., Coleman P.D., Rogers J., Head E., Kim R., Beach T., Miller C., Troncoso J., Trojanowski J.Q., et al. Gene expression changes in the course of normal brain aging are sexually dimorphic. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:15605-15610.
5. Buga A.M., Margaritescu C., Scholz C.J., Radu E., Zelenak C., Popa-Wagner A. Transcriptomics of post-stroke angiogenesis in the aged brain. Front. Aging Neurosci. 2014, 6:44.
6. Buga A.-M., Sascau M., Pisoschi C., Herndon J.G., Kessler C., Popa-Wagner A. The genomic response of the ipsilateral and contralateral cortex to stroke in aged rats. J. Cell. Mol. Med. 2008, 12:2731-2753.
7. Bürger S., Noack M., Kirazov L.P., Kirazov E.P., Naydenov C.L., Kouznetsova E., Yafai Y., Schliebs R. Vascular endothelial growth factor (VEGF) affects processing of amyloid precursor protein and beta-amyloidogenesis in brain slice cultures derived from transgenic Tg2576 mouse brain. Int. J. Dev. Neurosci. 2009, 27:517-523.
8. Bürger S., Yafai Y., Bigl M., Wiedemann P., Schliebs R. Effect of VEGF and its receptor antagonist SU-5416 an inhibitor of angiogenesis, on processing of the β-amyloid precursor protein in primary neuronal cells derived from brain tissue of Tg2576 mice. Int. J. Dev. Neurosci. 2010, 28:597-604.
9. Cao Y. Positive and negative modulation of angiogenesis by VEGFR1 ligands. Sci. Signal. 2009, 2. re1.
10. Chapuis J., Tian J., Shi J., Bensemain F., Cottel D., Lendon C., Amouyel P., Mann D., Lambert J.-C. Association study of the vascular endothelial growth factor gene with the risk of developing Alzheimer's disease. Neurobiol. Aging 2006, 27:1212-1215.
11. Chiarini A., Whitfield J., Bonafini C., Chakravarthy B., Armato U., Dal Prà I. Amyloid-β(25-35), an amyloid-β(1-42) surrogate, and proinflammatory cytokines stimulate VEGF-A secretion by cultured, early passage, normoxic adult human cerebral astrocytes. J. Alzheimers Dis. 2010, 21:915-926.
12. Choi J.-S., Shin Y.-J., Lee J.-Y., Yun H., Cha J.-H., Choi J.-Y., Chun M.-H., Lee M.-Y. Expression of vascular endothelial growth factor receptor-3 mRNA in the rat developing forebrain and retina. J. Comp. Neurol. 2010, 518:1064-1081.
13. Corsi M.M., Licastro F., Porcellini E., Dogliotti G., Galliera E., Lamont J.L., Innocenzi P.J., Fitzgerald S.P. Reduced plasma levels of P-selectin and L-selectin in a pilot study from Alzheimer disease: relationship with neuro-degeneration. Biogerontology 2011, 12:451-454.
14. Darrington E., Zhong M., Vo B.-H., Khan S.A. Vascular endothelial growth factor A secreted in response to transforming growth factor-β1 under hypoxic conditions, induces autocrine effects on migration of prostate cancer cells. Asian J. Androl. 2012, 14:745-751.
15. De la Torre J.C., Mussivand T. Can disturbed brain microcirculation cause Alzheimer's disease?. Neurol. Res. 1993, 15:146-153.
16. Desai B.S., Schneider J.A., Li J.-L., Carvey P.M., Hendey B. Evidence of angiogenic vessels in Alzheimer's disease. J. Neural Transm. 2009, 116:587-597.
17. Ferrara N., Houck K., Jakeman L., Leung D.W. Molecular and biological properties of the vascular endothelial growth factor family of proteins. Endocr. Rev. 1992, 13:18-32.
18. Gage F.H., Kempermann G., Palmer T.D., Peterson D.A., Ray J. Multipotent progenitor cells in the adult dentate gyrus. J. Neurobiol. 1998, 36:249-266.
19. Ge S., Song L., Pachter J.S. Where is the blood-brain barrier . really?. J. Neurosci. Res. 2005, 79:421-427.
20. Hardy J.A., Higgins G.A. Alzheimer's disease: the amyloid cascade hypothesis. Science 1992, 256:184-185.
21. Hou S.T., Keklikian A., Slinn J., O'Hare M., Jiang S.X., Aylsworth A. Sustained up-regulation of semaphorin 3A neuropilin1, and doublecortin expression in ischemic mouse brain during long-term recovery. Biochem. Biophys. Res. Commun. 2008, 367:109-115.
22. Hou Y., Shin Y.-J., Han E.J., Choi J.-S., Park J.-M., Cha J.-H., Choi J.-Y., Lee M.-Y. Distribution of vascular endothelial growth factor receptor-3/Flt4 mRNA in adult rat central nervous system. J. Chem. Neuroanat. 2011, 42:56-64.
23. Hsiao K., Chapman P., Nilsen S., Eckman C., Harigaya Y., Younkin S., Yang F., Cole G. Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 1996, 274:99-102.
24. Huang L., Jia J., Liu R. Decreased serum levels of the angiogenic factors VEGF and TGF-β1 in Alzheimer's disease and amnestic mild cognitive impairment. Neurosci. Lett. 2013, 550:60-63.
25. Iida K., Kawakami Y., Sone H., Suzuki H., Yatoh S., Isobe K., Takekoshi K., Yamada N. Vascular endothelial growth factor gene expression in a retinal pigmented cell is up-regulated by glucose deprivation through 3' UTR. Life Sci. 2002, 71:1607-1614.
26. Isingrini E., Desmidt T., Belzung C., Camus V. Endothelial dysfunction: a potential therapeutic target for geriatric depression and brain amyloid deposition in Alzheimer's disease?. Curr. Opin. Invest. Drugs Lond. Engl. 2009, 2000(10):46-55.
27. Jain R.K. Molecular regulation of vessel maturation. Nat. Med. 2003, 9:685-693.
28. Kara F., van Dongen E.S., Schliebs R., van Buchem M.A., de Groot H.J.M., Alia A. Monitoring blood flow alterations in the Tg2576 mouse model of Alzheimer's disease by in vivo magnetic resonance angiography at 17.6T. Neuroimage 2012, 60:958-966.
29. Khaibullina A.A., Rosenstein J.M., Krum J.M. Vascular endothelial growth factor promotes neurite maturation in primary CNS neuronal cultures. Brain Res. Dev. Brain Res. 2004, 148:59-68.
30. Koch S., Tugues S., Li X., Gualandi L., Claesson-Welsh L. Signal transduction by vascular endothelial growth factor receptors. Biochem. J. 2011, 437:169-183.
31. Koike M.A., Lin A.J., Pham J., Nguyen E., Yeh J.J., Rahimian R., Tromberg B.J., Choi B., Green K.N., LaFerla F.M. APP knockout mice experience acute mortality as the result of ischemia. PLoS ONE 2012, 7:e42665.
32. Kouznetsova E., Klingner M., Sorger D., Sabri O., Grossmann U., Steinbach J., Scheunemann M., Schliebs R. Developmental and amyloid plaque-related changes in cerebral cortical capillaries in transgenic Tg2576 Alzheimer mice. Int. J. Dev. Neurosci. 2006, 24:187-193.
33. Kuznetsova E., Schliebs R. β-Amyloid cholinergic transmission, and cerebrovascular system - a developmental study in a mouse model of Alzheimer's disease. Curr. Pharm. Des. 2013, 19:6749-6765.
34. Lagercrantz J., Farnebo F., Larsson C., Tvrdik T., Weber G., Piehl F. A comparative study of the expression patterns for vegf, vegf-b/vrf and vegf-c in the developing and adult mouse. Biochim. Biophys. Acta 1998, 1398:157-163.
35. Li Y.-N., Pan R., Qin X.-J., Yang W.-L., Qi Z., Liu W., Liu K.J. Ischemic neurons activate astrocytes to disrupt endothelial barrier via increasing VEGF expression. J. Neurochem. 2014, 129:120-129.
36. Liu H., Xing A., Wang X., Liu G., Li L. Regulation of β-amyloid level in the brain of rats with cerebrovascular hypoperfusion. Neurobiol. Aging 2012, 33:826e31-826e42.
37. Mateo I., Llorca J., Infante J., Rodríguez-Rodríguez E., Fernández-Viadero C., Peña N., Berciano J., Combarros O. Low serum VEGF levels are associated with Alzheimer's disease. Acta Neurol. Scand. 2007, 116:56-58.
38. Mito T., Konomi H., Houdou S., Takashima S. Immunohistochemical study of the vasculature in the developing brain. Pediatr. Neurol. 1991, 7:18-22.
39. Muche A., Bürger S., Arendt T., Schliebs R. Hypoxic stress, brain vascular system, and β-amyloid: a primary cell culture study. Nutr. Neurosci. 2013.
40. Murugesan N., Demarest T.G., Madri J.A., Pachter J.S. Brain regional angiogenic potential at the neurovascular unit during normal aging. Neurobiol. Aging 2012, 33:1004e1-1004e16.
41. Narasimhan P., Liu J., Song Y.S., Massengale J.L., Chan P.H. VEGF Stimulates the ERK 1/2 signaling pathway and apoptosis in cerebral endothelial cells after ischemic conditions. Stroke J. Cereb. Circ. 2009, 40:1467-1473.
42. Nicolakakis N., Hamel E. Neurovascular function in Alzheimer's disease patients and experimental models. J. Cereb. Blood Flow Metab. 2011, 31:1354-1370.
43. Nitzan A., Kermer P., Shirvan A., Bähr M., Barzilai A., Solomon A.S. Examination of cellular and molecular events associated with optic nerve axotomy. Glia 2006, 54:545-556.
44. Paris D., Patel N., DelleDonne A., Quadros A., Smeed R., Mullan M. Impaired angiogenesis in a transgenic mouse model of cerebral amyloidosis. Neurosci. Lett. 2004, 366:80-85.
45. Paris D., Townsend K., Quadros A., Humphrey J., Sun J., Brem S., Wotoczek-Obadia M., DelleDonne A., Patel N., Obregon D.F., et al. Inhibition of angiogenesis by Abeta peptides. Angiogenesis 2004, 7:75-85.
46. Paris D., Ait-Ghezala G., Mathura V.S., Patel N., Quadros A., Laporte V., Mullan M. Anti-angiogenic activity of the mutant Dutch A(beta) peptide on human brain microvascular endothelial cells. Brain Res. Mol. Brain Res. 2005, 136:212-230.
47. Pitzer M.R., Sortwell C.E., Daley B.F., McGuire S.O., Marchionini D., Fleming M., Collier T.J. Angiogenic and neurotrophic effects of vascular endothelial growth factor (VEGF165): studies of grafted and cultured embryonic ventral mesencephalic cells. Exp. Neurol. 2003, 182:435-445.
48. Rosenstein J.M., Krum J.M. New roles for VEGF in nervous tissue - beyond blood vessels. Exp. Neurol. 2004, 187:246-253.
49. Rosenstein J.M., Mani N., Khaibullina A., Krum J.M. Neurotrophic effects of vascular endothelial growth factor on organotypic cortical explants and primary cortical neurons. J. Neurosci. 2003, 23:11036-11044.
50. Roskoski R. VEGF receptor protein-tyrosine kinases: structure and regulation. Biochem. Biophys. Res. Commun. 2008, 375:287-291.
51. Schliebs R. Alzheimer's disease. In Handbook of Neuroinformatics. L 2013, 889-910. Springer, Frankfurt. N. Kasabov (Ed.).
52. Schliebs R., Arendt T. The cholinergic system in aging and neuronal degeneration. Behav. Brain Res. 2011, 221:555-563.
53. Shin Y.-J., Choi J.-S., Lee J.-Y., Choi J.-Y., Cha J.-H., Chun M.-H., Lee M.-Y. Differential regulation of vascular endothelial growth factor-C and its receptor in the rat hippocampus following transient forebrain ischemia. Acta Neuropathol. (Berl.) 2008, 116:517-527.
54. Sköld M.K., von Gertten C., Sandberg-Nordqvist A.-C., Mathiesen T., Holmin S. VEGF and VEGF receptor expression after experimental brain contusion in rat. J. Neurotrauma 2005, 22:353-367.
55. Smith C.P., Steinle J.J. Changes in growth factor expression in normal aging of the rat retina. Exp. Eye Res. 2007, 85:817-824.
56. Tang H., Mao X., Xie L., Greenberg D.A., Jin K. Expression level of vascular endothelial growth factor in hippocampus is associated with cognitive impairment in patients with Alzheimer's disease. Neurobiol. Aging 2013, 34:1412-1415.
57. Tarkowski E., Issa R., Sjögren M., Wallin A., Blennow K., Tarkowski A., Kumar P. Increased intrathecal levels of the angiogenic factors VEGF and TGF-beta in Alzheimer's disease and vascular dementia. Neurobiol. Aging 2002, 23:237-243.
58. Wang W.Y., Dong J.H., Liu X., Wang Y., Ying G.X., Ni Z.M., Zhou C.F. Vascular endothelial growth factor and its receptor Flk-1 are expressed in the hippocampus following entorhinal deafferentation. Neuroscience 2005, 134:1167-1178.
59. Whitehead S.N., Gangaraju S., Slinn J., Hou S.T. Transient and bilateral increase in neuropilin-1: fer kinase and collapsin response mediator proteins within membrane rafts following unilateral occlusion of the middle cerebral artery in mouse. Brain Res. 2010, 1344:209-216.
60. Ye Y., Huang C., Jiang L., Shen X., Zhu S., Rao Y., Wang J., Zhang Q. Huanglian-Jie-Du-Tang extract protects against chronic brain injury after focal cerebral ischemia via hypoxia-inducible-factor-1α-regulated vascular endothelial growth factor signaling in mice. Biol. Pharm. Bull. 2012, 35:355-361.
61. Zhang Z.G., Tsang W., Zhang L., Powers C., Chopp M. Up-regulation of neuropilin-1 in neovasculature after focal cerebral ischemia in the adult rat. J. Cereb. Blood Flow Metab. 2001, 21:541-549.