L-type calcium channel blockers and substance P induce angiogenesis of cortical vessels associated with beta-amyloid plaques in an Alzheimer mouse model

Neurobiology of Aging

Volumn 36, Issue 3, 2015, Pages 1333-1341

  Daschil, Nina ^a   Kniewallner, Kathrin M ^a   Obermair, Gerald J ^a   Hutter Paier, Birgit ^b   Windisch, Manfred ^c   Marksteiner, Josef ^d   Humpel, Christian ^a  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b QPS Austria GmbH   (Austria)

^c NeuroScios GmbH   (Austria)

^d Tirol Kliniken   (Austria)

Author keywords

Alzheimer; Angiogenesis; Beta amyloid plaque; L type calcium channel; Reactive astrocytes; Substance P; Vessels

Indexed keywords

AMYLOID PRECURSOR PROTEIN; CALCIUM CHANNEL BLOCKING AGENT; CALCIUM CHANNEL L TYPE; COLLAGEN TYPE 4; MESSENGER RNA; OLIGONUCLEOTIDE; PREPROTACHYKININ; SUBSTANCE P; AMYLOID BETA PROTEIN;

ADULT; ALZHEIMER DISEASE; AMYLOID PLAQUE; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BETA AMYLOID PLAQUE; BRAIN BLOOD VESSEL; BRAIN CORTEX; CONFOCAL MICROSCOPY; CONTROLLED STUDY; HIPPOCAMPUS; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; MALE; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TISSUE CULTURE; ANIMAL; DISEASE MODEL; GENETICS; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE; VASCULARIZATION;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; ASTROCYTES; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS, L-TYPE; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; MICE, TRANSGENIC; NEOVASCULARIZATION, PATHOLOGIC; PLAQUE, AMYLOID; RNA, MESSENGER; SUBSTANCE P;

EID: 84923610115     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2014.12.027     Document Type: Article

References (49)

1. Abd El-Rahman R.R., Harraz O.F., Brett S.E., Anfinogenova Y., Mufti R.E., Goldman D., Welsh D.G. Identification of L- and T-type Ca2+ channels in rat cerebral arteries: role in myogenic tone development. Am. J. Physiol. Heart Circ. Physiol. 2013, 304:H58-H71.
2. Alborch E., Salom J.B., Torregrosa G. Calcium channels in cerebral arteries. Pharmacol. Ther. 1995, 68:1-34.
3. Albrecht-Schgoer K., Schgoer W., Holfeld J., Theurl M., Wiedemann D., Steger C., Gupta R., Semsroth S., Fischer Colbrie R., Beer A.G., Stanzl U., Huber E., Misener S., Dejaco D., Kishore R., Pachinger O., Grimm M., Bonaros N., Kirchmair R. The angiogenic factor secretoneurin induces coronary angiogenesis in a model of myocardial infarction by stimulation of vascular endothelial growth factor signaling in endothelial cells. Circulation 2012, 126:2491-2501.
4. Arikkath J., Campbell K.P. Auxiliary subunits: essential components of the voltage-gated calcium channel complex. Curr. Opin. Neurobiol. 2003, 13:298-307. Review.
5. Armstrong R.A. Classic beta-amyloid deposits cluster around large diameter blood vessels rather than capillaries in sporadic Alzheimer's disease. Curr. Neurovasc Res. 2006, 3:289-294.
6. Beckmann N., Schuler A., Mueggler T., Meyer E.P., Wiederhold K.H., Staufenbiel M., Krucker T. Age-dependent cerebrovascular abnormalities and blood flow disturbances in APP23 mice modeling Alzheimer's disease. J.Neurosci. 2003, 23:8453-8459.
7. Borysova L., Wray S., Eisner D.A., Burdyga T. How calcium signals in myocytes and pericytes are integrated across in situ microvascular networks and control microvascular tone. Cell Calcium 2013, 54:163-174.
8. Catterall W.A. Structure and regulation of voltage-gated Ca2+ channels. Annu. Rev. Cell. Dev. Biol. 2000, 16:521-555.
9. Cole R.L., Lechner S.M., Williams M.E., Prodanovich P., Bleicher L., Varney M.A., Gu G. Differential distribution of voltage-gated calcium channel alpha-2 delta (alpha2delta) subunit mRNA-containing cells in the rat central nervous system and the dorsal root ganglia. J.Comp. Neurol. 2005, 491:246-269.
10. Crews L., Rockenstein E., Masliah E. APP transgenic modeling of Alzheimer's disease: mechanisms of neurodegeneration and aberrant neurogenesis. Brain Struct. Funct. 2010, 214:111-126.
11. Daschil N., Geisler S., Obermair G.J., Humpel C. Short- and long-term treatment of mouse cortical primary astrocytes with β-amyloid differentially regulates the mRNA expression of L-type calcium channels. Pharmacology 2014, 93:24-31.
12. Daschil N., Obermair G.J., Flucher B.E., Stefanova N., Hutter-Paier B., Windisch M., Humpel C., Marksteiner J. CaV1.2 calcium channel expression in reactive astrocytes is associated with the formation of amyloid-β plaques in an Alzheimer's disease mouse model. J.Alzheimers Dis. 2013, 37:439-451.
13. Davis J., Xu F., Deane R., Romanov G., Previti M.L., Zeigler K., Zlokovic B.V., Van Nostrand W.E. Early-onset and robust cerebral microvascular accumulation of amyloid beta-protein in transgenic mice expressing low levels of a vasculotropic Dutch/Iowa mutant form of amyloid beta-protein precursor. J.Biol. Chem. 2004, 279:20296-20306.
14. de la Torre J.C. Alzheimer's disease as a vascular disorder: nosological evidence. Stroke 2002, 33:1152-1162.
15. Green K.N., Smith I.F., LaFerla F.M. Role of calcium in the pathogenesis of Alzheimer's disease and transgenic models. Subcell Biochem. 2007, 45:507-521.
16. Groth R.D., Tirko N.N., Tsien R.W. Cav1.2 calcium channels: just cut out to be regulated?. Neuron 2014, 82:939-940. Previews.
17. Havas D., Hutter-Paier B., Ubhi K., Rockenstein E., Crailsheim K., Masliah E., Windisch M. Alongitudinal study of behavioral deficits in an AβPP transgenic mouse model of Alzheimer's disease. J.Alzheimers Dis. 2011, 25:231-243.
18. Humpel C. Chronic mild cerebrovascular dysfunction as a cause for Alzheimer's disease?. Exp. Gerontol. 2011, 46:225-232. Review.
19. Humpel C., Wetmore C., Olson L. Regulation of brain-derived neurotrophic factor messenger RNA and protein at the cellular level in pentylenetetrazol-induced epileptic seizures. Neuroscience 1993, 53:909-918.
20. Hutter-Paier B., Huttunen J.J., Puglielli L., Eckman C.B., Kim D.Y., Hofmeister A., Moir R.D., Domnitz S.B., Frosch M.P., Windisch M., Kovacs D.M. The ACAT inhibitor CP-113,818 markedly reduces amyloid pathology in a mouse model of Alzheimer's disease. Neuron 2004, 44:227-238.
21. Iadecola C. Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat. Rev. Neurosci. 2004, 5:347-360.
22. Kamouchi M., Kitazono T., Ago T., Wakisaka M., Ooboshi H., Ibayashi S., Iida M. Calcium influx pathways in rat CNS pericytes. Brain Res. Mol. Brain Res. 2004, 126:114-120.
23. Kawai M., Kalaria R.N., Harik S.I., Perry G. The relationship of amyloid plaques to cerebral capillaries in Alzheimer's disease. Am. J. Pathol. 1990, 137:1435-1446.
24. Kohara H., Tajima S., Yamamoto M., Tabata Y. Angiogenesis induced by controlled release of neuropeptide substance P. Biomaterials 2010, 31:8617-8625.
25. Kumar-Singh S., Pirici D., McGowan E., Serneels S., Ceuterick C., Hardy J., Duff K., Dickinson D., Van Broeckhoven C. Dense-core plaques in Tg2576 and PSAPP mouse models of Alzheimer's disease are centered on vessel walls. Am. J. Pathol. 2005, 167:527-543.
26. Ludwig A., Flockerzi V., Hofmann F. Regional expression and cellular localization of the alpha1 and beta subunit of high voltage-activated calcium channels in rat brain. J.Neurosci. 1997, 17:1339-1349.
27. Maghni K., Michoud M.C., Alles M., Rubin A., Govindaraju V., Meloche C., Martin J.G. Airway smooth muscle cells express functional neurokinin-1 receptors and the nerve-derived preprotachykinin-a gene: regulation by passive sensitization. Am. J. Respir. Cell. Mol. Biol. 2003, 28:103-110.
28. Meyer E.P., Ulmann-Schuler A., Staufenbiel M., Krucker T. Altered morphology and 3D architecture of brain vasculature in a mouse model for Alzheimer's disease. PNAS 2008, 105:3587-3592.
29. Milner P., Bodin P., Guiducci S., Del Rosso A., Kahaleh M.B., Matucci-Cerinic M., Burnstock G. Regulation of substance P mRNA expression in human dermal microvascular endothelial cells. Clin. Exp. Rheumatol. 2004, 22(3 Suppl 33):24-27. Review.
30. Moser K.V., Schmidt-Kastner R., Hinterhuber H., Humpel C. Brain capillaries and cholinergic neurons persist in organotypic brain slices in the absence of blood flow. Eur. J. Neurosci. 2003, 18:85-94.
31. Obermair G.J., Flucher B.E. Neuronal functions of auxiliary calcium channel subunits. Modulation of Presynaptic Calcium Channels, Springer Science+ Business Media Dordrecht 2013, 29-60. G. Stephens, S. Mochida (Eds.).
32. Pelletier L., Angonin R., Regnard J., Fellmann D., Charbord P. Human bone marrow angiogenesis: invitro modulation by substance P and neurokinin A. Br. J. Haematol. 2002, 119:1083-1089.
33. Reimer D., Huber I.G., Garcia M.L., Haase H., Striessnig J. Beta subunit heterogeneity of L-type Ca(2+) channels in smooth muscle tissues. FEBS Lett. 2000, 467:65-69.
34. Rockenstein E., Crews L., Masliah E. Transgenic animal models of neurodegenerative diseases and their application to treatment development. Adv. Drug Deliv. Rev. 2007, 59:1093-1102.
35. Santos S.F., Pierrot N., Octave J.N. Network excitability dysfunction in Alzheimer's disease: insights from invitro and invivo models. Rev. Neurosci. 2010, 21:153-171.
36. Schlick B., Flucher B., Obermair G.J. Voltage-activated calcium channel expression profiles in mouse brain and cultured hippocampal neurons. Neuroscience 2010, 167:786-798.
37. Seegers H.C., Hood V.C., Kidd B.L., Cruwys S.C., Walsh D.A. Enhancement of angiogenesis by endogenous substance P release and neurokinin-1 receptors during neurogenic inflammation. J.Pharmacol. Exp. Ther. 2003, 306:8-12.
38. Serrano-Pozo A., Muzikansky A., Gómez-Isla T., Growdon J.H., Betensky R.A., Frosch M.P., Hyman B.T. Differential relationships of reactive astrocytes and microglia to fibrillar amyloid deposits in Alzheimer disease. J.Neuropathol. Exp. Neurol. 2013, 72:462-471.
39. Stones R.W., Loesch A., Beard R.W., Burnstock G. Substance P: endothelial localization and pharmacology in the human ovarian vein. Obstet. Gynecol. 1995, 85:273-278.
40. Striessnig J., Koschak A., Sinnegger-Brauns M.J., Hetzenauer A., Nguyen N.K., Busquet P., Pelster G., Singewald N. Role of voltage-gated L-type Ca2+ channel isoforms for brain function. Biochem. Soc. Trans. 2006, 34(Pt 5):903-909.
41. Thibault O., Gant J.C., Landfield P.W. Expansion of the calcium hypothesis of brain aging and Alzheimer's disease: minding the store. Aging Cell 2007, 6:307-317.
42. Ullrich C., Daschil N., Humpel C. Organotypic vibrosections: novel whole sagittal brain cultures. J.Neurosci. Methods 2011, 201:131-141.
43. Wiedermann C.J., Auer B., Sitte B., Reinisch N., Schratzberger P., Kähler C.M. Induction of endothelial cell differentiation into capillary-like structures by substance P. Eur. J. Pharmacol. 1996, 298:335-338.
44. Willis M., Hutter-Paier B., Wietzorrek G., Windisch M., Humpel C., Knaus H.G., Marksteiner J. Localization and expression of substance P in transgenic mice overexpressing human APP751 with the London (V717I) and Swedish (K670M/N671L) mutations. Brain Res. 2007, 1143:199-207.
45. Willis M., Kaufmann W.A., Wietzorrek G., Hutter-Paier B., Moosmang S., Humpel C., Hofmann F., Windisch M., Knaus H.G., Marksteiner J. L-type calcium channel CaV 1.2 in transgenic mice overexpressing human AbetaPP751 with the London (V717I) and Swedish (K670M/N671L) mutations. J.Alzheimers Dis. 2010, 20:1167-1180.
46. Willis M., Prokesch M., Hutter-Paier B., Windisch M., Stridsberg M., Mahata S.K., Kirchmair R., Wietzorrek G., Knaus H.G., Jellinger K., Humpel C., Marksteiner J. Chromogranin B and secretogranin II in transgenic mice overexpressing human APP751 with the London (V717I) and Swedish (K670M/N671L) mutations and in Alzheimer patients. J.Alzheimers Dis. 2008, 13:123-135.
47. Xie H., Guan J., Borrelli L.A., Xu J., Serrano-Pozo A., Bacskai B.J. Mitochondrial alterations near amyloid plaques in an Alzheimer's disease mouse model. J.Neurosci. 2013, 33:17042-17051.
48. Zhang Z., Lin H., Cao C., Khurana S., Pallone T.L. Voltage-gated divalent currents in descending vasa recta pericytes. Am. J. Physiol. Renal Physiol. 2010, 299:F862-F871.
49. Ziche M., Morbidelli L., Masini E., Amerini S., Granger H.J., Maggi C.A., Geppetti P., Ledda F. Nitric oxide mediates angiogenesis invivo and endothelial cell growth and migration invitro promoted by substance P. J.Clin. Invest. 1994, 94:2036-2044.