Modeling cerebrovascular pathophysiology in amyloid-β metabolism using neural-crest-derived smooth muscle cells

Cell Reports

Volumn 9, Issue 1, 2014, Pages 391-401

  Cheung, Christine ^a,b   Goh, Yeek Teck ^a   Zhang, Jingxian ^a   Wu, Chenghan ^c   Guccione, Ernesto ^a,d  

^a INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^b Dept Medicine Endocrinol Diabet   (Singapore)

^c MONASH UNIVERSITY   (Australia)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; LIPOPROTEIN RECEPTOR; PROTEIN LRP1; UNCLASSIFIED DRUG; GLUCOSE 6 PHOSPHATE ISOMERASE;

ARTICLE; BRAIN BLOOD VESSEL; CELL HYPOXIA; CEREBROVASCULAR DISEASE; CLEARANCE; CONTROLLED STUDY; DEGRADATION KINETICS; HUMAN; HUMAN CELL; LYSOSOME; NEURAL CREST; NUCLEOTIDE SEQUENCE; PATHOPHYSIOLOGY; PHENOTYPE; PLURIPOTENT STEM CELL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN TRANSPORT; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE; ALZHEIMER DISEASE; ANIMAL; HELA CELL LINE; METABOLISM; MOUSE; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; GLUCOSE-6-PHOSPHATE ISOMERASE; HELA CELLS; HUMANS; MICE; MICE, TRANSGENIC; MYOCYTES, SMOOTH MUSCLE; NEURAL CREST;

EID: 84907972747     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.08.065     Document Type: Article

References (59)

1. Alonzo N.C., Hyman B.T., Rebeck G.W., Greenberg S.M. Progression of cerebral amyloid angiopathy: accumulation of amyloid-beta40 in affected vessels. J.Neuropathol. Exp. Neurol. 1998, 57:353-359.
2. Bell R.D., Deane R., Chow N., Long X., Sagare A., Singh I., Streb J.W., Guo H., Rubio A., Van Nostrand W., et al. SRF and myocardin regulate LRP-mediated amyloid-beta clearance in brain vascular cells. Nat. Cell Biol. 2009, 11:143-153.
3. Blaise R., Mateo V., Rouxel C., Zaccarini F., Glorian M., Béréziat G., Golubkov V.S., Limon I. Wild-type amyloid beta 1-40 peptide induces vascular smooth muscle cell death independently from matrix metalloprotease activity. Aging Cell 2012, 11:384-393.
4. Brons I.G., Smithers L.E., Trotter M.W., Rugg-Gunn P., Sun B., Chuva de Sousa Lopes S.M., Howlett S.K., Clarkson A., Ahrlund-Richter L., Pedersen R.A., Vallier L. Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 2007, 448:191-195.
5. Calhoun M.E., Burgermeister P., Phinney A.L., Stalder M., Tolnay M., Wiederhold K.H., Abramowski D., Sturchler-Pierrat C., Sommer B., Staufenbiel M., Jucker M. Neuronal overexpression of mutant amyloid precursor protein results in prominent deposition of cerebrovascular amyloid. Proc. Natl. Acad. Sci. USA 1999, 96:14088-14093.
6. Chambers S.M., Fasano C.A., Papapetrou E.P., Tomishima M., Sadelain M., Studer L. Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat. Biotechnol. 2009, 27:275-280.
7. Cheung C., Sinha S. Human embryonic stem cell-derived vascular smooth muscle cells in therapeutic neovascularisation. J.Mol. Cell. Cardiol. 2011, 51:651-664.
8. Cheung C., Bernardo A.S., Trotter M.W., Pedersen R.A., Sinha S. Generation of human vascular smooth muscle subtypes provides insight into embryological origin-dependent disease susceptibility. Nat. Biotechnol. 2012, 30:165-173.
9. Chi J.T., Rodriguez E.H., Wang Z., Nuyten D.S., Mukherjee S., van de Rijn M., van de Vijver M.J., Hastie T., Brown P.O. Gene expression programs of human smooth muscle cells: tissue-specific differentiation and prognostic significance in breast cancers. PLoS Genet. 2007, 3:1770-1784.
10. Choi Y., Kim H.S., Shin K.Y., Kim E.M., Kim M., Kim H.S., Park C.H., Jeong Y.H., Yoo J., Lee J.P., et al. Minocycline attenuates neuronal cell death and improves cognitive impairment in Alzheimer's disease models. Neuropsychopharmacology 2007, 32:2393-2404.
11. Deane R., Zlokovic B.V. Role of the blood-brain barrier in the pathogenesis of Alzheimer's disease. Curr. Alzheimer Res. 2007, 4:191-197.
12. Deane R., Wu Z., Zlokovic B.V. RAGE (yin) versus LRP (yang) balance regulates alzheimer amyloid beta-peptide clearance through transport across the blood-brain barrier. Stroke 2004, 35(11, Suppl 1):2628-2631.
13. Farkas E., Luiten P.G. Cerebral microvascular pathology in aging and Alzheimer's disease. Prog. Neurobiol. 2001, 64:575-611.
14. Fossati S., Cam J., Meyerson J., Mezhericher E., Romero I.A., Couraud P.O., Weksler B.B., Ghiso J., Rostagno A. Differential activation of mitochondrial apoptotic pathways by vasculotropic amyloid-beta variants in cells composing the cerebral vessel walls. FASEB J. 2010, 24:229-241.
15. Gorelick P.B., Scuteri A., Black S.E., Decarli C., Greenberg S.M., Iadecola C., Launer L.J., Laurent S., Lopez O.L., Nyenhuis D., et al. Vascular contributions to cognitive impairment and dementia: a statement for healthcare professionals from the american heart association/american stroke association. Stroke 2011, 42:2672-2713. American Heart Association Stroke Council, Council on Epidemiology and Prevention, Council on Cardiovascular Nursing, Council on Cardiovascular Radiology and Intervention, and Council on Cardiovascular Surgery and Anesthesia.
16. Guan W., Kozak A., Fagan S.C. Drug repurposing for vascular protection after acute ischemic stroke. Acta Neurochir. Suppl. (Wien) 2011, 111:295-298.
17. Herzig M.C., Winkler D.T., Burgermeister P., Pfeifer M., Kohler E., Schmidt S.D., Danner S., Abramowski D., Stürchler-Pierrat C., Bürki K., et al. Abeta is targeted to the vasculature in a mouse model of hereditary cerebral hemorrhage with amyloidosis. Nat. Neurosci. 2004, 7:954-960.
18. Höing S., Rudhard Y., Reinhardt P., Glatza M., Stehling M., Wu G., Peiker C., Böcker A., Parga J.A., Bunk E., et al. Discovery of inhibitors of microglial neurotoxicity acting through multiple mechanisms using a stem-cell-based phenotypic assay. Cell Stem Cell 2012, 11:620-632.
19. Hu B.Y., Zhang S.C. Differentiation of spinal motor neurons from pluripotent human stem cells. Nat. Protoc. 2009, 4:1295-1304.
20. Jellinger K.A. Prevalence and impact of cerebrovascular lesions in Alzheimer and lewy body diseases. Neurodegener. Dis. 2010, 7:112-115.
21. Kanekiyo T., Liu C.C., Shinohara M., Li J., Bu G. LRP1 in brain vascular smooth muscle cells mediates local clearance of Alzheimer's amyloid-β. J.Neurosci. 2012, 32:16458-16465.
22. Krencik R., Zhang S.C. Directed differentiation of functional astroglial subtypes from human pluripotent stem cells. Nat. Protoc. 2011, 6:1710-1717.
23. Lee G., Ramirez C.N., Kim H., Zeltner N., Liu B., Radu C., Bhinder B., Kim Y.J., Choi I.Y., Mukherjee-Clavin B., et al. Large-scale screening using familial dysautonomia induced pluripotent stem cells identifies compounds that rescue IKBKAP expression. Nat. Biotechnol. 2012, 30:1244-1248.
24. Lefterov I., Fitz N.F., Cronican A.A., Fogg A., Lefterov P., Kodali R., Wetzel R., Koldamova R. Apolipoprotein A-I deficiency increases cerebral amyloid angiopathy and cognitive deficits in APP/PS1DeltaE9 mice. J.Biol. Chem. 2010, 285:36945-36957.
25. Leissring M.A., Turner A.J. Regulation of distinct pools of amyloid β-protein by multiple cellular proteases. Alzheimers Res. Ther. 2013, 5:37.
26. Li N.C., Lee A., Whitmer R.A., Kivipelto M., Lawler E., Kazis L.E., Wolozin B. Use of angiotensin receptor blockers and risk of dementia in a predominantly male population: prospective cohort analysis. BMJ 2010, 340:b5465.
27. Li W., Xiong Y., Shang C., Twu K.Y., Hang C.T., Yang J., Han P., Lin C.Y., Lin C.J., Tsai F.C., et al. Brg1 governs distinct pathways to direct multiple aspects of mammalian neural crest cell development. Proc. Natl. Acad. Sci. USA 2013, 110:1738-1743.
28. Lillis A.P., Van Duyn L.B., Murphy-Ullrich J.E., Strickland D.K. LDL receptor-related protein 1: unique tissue-specific functions revealed by selective gene knockout studies. Physiol. Rev. 2008, 88:887-918.
29. Lippmann E.S., Azarin S.M., Kay J.E., Nessler R.A., Wilson H.K., Al-Ahmad A., Palecek S.P., Shusta E.V. Derivation of blood-brain barrier endothelial cells from human pluripotent stem cells. Nat. Biotechnol. 2012, 30:783-791.
30. Majesky M.W. Developmental basis of vascular smooth muscle diversity. Arterioscler. Thromb. Vasc. Biol. 2007, 27:1248-1258.
31. Majesky M.W., Mummery C.L. Smooth muscle diversity from human pluripotent cells. Nat. Biotechnol. 2012, 30:152-154.
32. Mazur-Kolecka B., Kowal D., Sukontasup T., Dickson D., Frackowiak J. The effect of oxidative stress on accumulation of apolipoprotein E3 and E4 in a cell culture model of beta-amyloid angiopathy (CAA). Brain Res. 2003, 983:48-57.
33. Menendez L., Kulik M.J., Page A.T., Park S.S., Lauderdale J.D., Cunningham M.L., Dalton S. Directed differentiation of human pluripotent cells to neural crest stem cells. Nat. Protoc. 2013, 8:203-212.
34. Miners J.S., Van Helmond Z., Chalmers K., Wilcock G., Love S., Kehoe P.G. Decreased expression and activity of neprilysin in Alzheimer disease are associated with cerebral amyloid angiopathy. J.Neuropathol. Exp. Neurol. 2006, 65:1012-1021.
35. Nedergaard M. Neuroscience. Garbage truck of the brain. Science 2013, 340:1529-1530.
36. Park L., Anrather J., Zhou P., Frys K., Pitstick R., Younkin S., Carlson G.A., Iadecola C. NADPH-oxidase-derived reactive oxygen species mediate the cerebrovascular dysfunction induced by the amyloid beta peptide. J.Neurosci. 2005, 25:1769-1777.
37. Pocathikorn A., Taylor R.R., Mamotte C.D. Atorvastatin increases expression of low-density lipoprotein receptor mRNA in human circulating mononuclear cells. Clin. Exp. Pharmacol. Physiol. 2010, 37:471-476.
38. Qosa H., Abuznait A.H., Hill R.A., Kaddoumi A. Enhanced brain amyloid-β clearance by rifampicin and caffeine as a possible protective mechanism against Alzheimer's disease. J.Alzheimers Dis. 2012, 31:151-165.
39. Rovelet-Lecrux A., Hannequin D., Raux G., Le Meur N., Laquerrière A., Vital A., Dumanchin C., Feuillette S., Brice A., Vercelletto M., et al. APP locus duplication causes autosomal dominant early-onset Alzheimer disease with cerebral amyloid angiopathy. Nat. Genet. 2006, 38:24-26.
40. Ruzali W.A., Kehoe P.G., Love S. Influence of LRP-1 and apolipoprotein E on amyloid-β uptake and toxicity to cerebrovascular smooth muscle cells. J.Alzheimers Dis. 2013, 33:95-110.
41. Schmechel D.E., Saunders A.M., Strittmatter W.J., Crain B.J., Hulette C.M., Joo S.H., Pericak-Vance M.A., Goldgaber D., Roses A.D. Increased amyloid beta-peptide deposition in cerebral cortex as a consequence of apolipoprotein E genotype in late-onset Alzheimer disease. Proc. Natl. Acad. Sci. USA 1993, 90:9649-9653.
42. Shi X., Fu Y., Liao D., Chen Y., Liu J. Alterations of voltage-dependent calcium channel currents in basilar artery smooth muscle cells at early stage of subarachnoid hemorrhage in a rabbit model. PLoS ONE 2014, 9:e84129.
43. Sleegers K., Brouwers N., Gijselinck I., Theuns J., Goossens D., Wauters J., Del-Favero J., Cruts M., van Duijn C.M., Van Broeckhoven C. APP duplication is sufficient to cause early onset Alzheimer's dementia with cerebral amyloid angiopathy. Brain 2006, 129:2977-2983.
44. Soffer D. Cerebral amyloid angiopathy-a disease or age-related condition. Isr. Med. Assoc. J. 2006, 8:803-806.
45. Strittmatter W.J., Saunders A.M., Schmechel D., Pericak-Vance M., Enghild J., Salvesen G.S., Roses A.D. Apolipoprotein E: high-avidity binding to beta-amyloid and increased frequency of type 4 allele in late-onset familial Alzheimer disease. Proc. Natl. Acad. Sci. USA 1993, 90:1977-1981.
46. Urmoneit B., Prikulis I., Wihl G., D'Urso D., Frank R., Heeren J., Beisiegel U., Prior R. Cerebrovascular smooth muscle cells internalize Alzheimer amyloid beta protein via a lipoprotein pathway: implications for cerebral amyloid angiopathy. Lab. Invest. 1997, 77:157-166.
47. Verghese P.B., Castellano J.M., Garai K., Wang Y., Jiang H., Shah A., Bu G., Frieden C., Holtzman D.M. ApoE influences amyloid-β (Aβ) clearance despite minimal apoE/Aβ association in physiological conditions. Proc. Natl. Acad. Sci. USA 2013, 110:E1807-E1816.
48. Viswanathan A., Greenberg S.M. Cerebral amyloid angiopathy in the elderly. Ann. Neurol. 2011, 70:871-880.
49. Wang Z., Yang D., Zhang X., Li T., Li J., Tang Y., Le W. Hypoxia-induced down-regulation of neprilysin by histone modification in mouse primary cortical and hippocampal neurons. PLoS ONE 2011, 6:e19229.
50. Wang A., Tang Z., Li X., Jiang Y., Tsou D.A., Li S. Derivation of smooth muscle cells with neural crest origin from human induced pluripotent stem cells. Cells Tissues Organs (Print) 2012, 195:5-14.
51. Weller R.O., Preston S.D., Subash M., Carare R.O. Cerebral amyloid angiopathy in the aetiology and immunotherapy of Alzheimer disease. Alzheimers Res. Ther. 2009, 1:6.
52. Whitfield J.F. The road to LOAD: late-onset Alzheimer's disease and a possible way to block it. Expert Opin. Ther. Targets 2007, 11:1257-1260.
53. Wilhelmus M.M., Otte-Höller I., van Triel J.J., Veerhuis R., Maat-Schieman M.L., Bu G., de Waal R.M., Verbeek M.M. Lipoprotein receptor-related protein-1 mediates amyloid-beta-mediated cell death of cerebrovascular cells. Am. J. Pathol. 2007, 171:1989-1999.
54. Winkler D.T., Bondolfi L., Herzig M.C., Jann L., Calhoun M.E., Wiederhold K.H., Tolnay M., Staufenbiel M., Jucker M. Spontaneous hemorrhagic stroke in a mouse model of cerebral amyloid angiopathy. J.Neurosci. 2001, 21:1619-1627.
55. Yang Y.M., Gupta S.K., Kim K.J., Powers B.E., Cerqueira A., Wainger B.J., Ngo H.D., Rosowski K.A., Schein P.A., Ackeifi C.A., et al. A small molecule screen in stem-cell-derived motor neurons identifies a kinase inhibitor as a candidate therapeutic for ALS. Cell Stem Cell 2013, 12:713-726.
56. Yao Y., Chen Z.L., Norris E.H., Strickland S. Astrocytic laminin regulates pericyte differentiation and maintains blood brain barrier integrity. Nat. Commun. 2014, 5:3413.
57. Zhang M., Luo G., Zhou Y., Wang S., Zhong Z. Phenotypic screens targeting neurodegenerative diseases. J.Biomol. Screen. 2014, 19:1-16.
58. Zlokovic B.V. Neurovascular pathways to neurodegeneration in Alzheimer's disease and other disorders. Nat. Rev. Neurosci. 2011, 12:723-738.
59. Zuloaga K.L., Gonzales R.J. Dihydrotestosterone attenuates hypoxia inducible factor-1α and cyclooxygenase-2 in cerebral arteries during hypoxia or hypoxia with glucose deprivation. Am. J. Physiol. Heart Circ. Physiol. 2011, 301:H1882-H1890.