Abnormal recruitment of extracellular matrix proteins by excess Notch3 ECD: A new pathomechanism in CADASIL

Brain

Volumn 136, Issue 6, 2013, Pages 1830-1845

  Monet Leprêtre, Marie ^a,b   Haddad, Iman ^c   Baron Menguy, Céline ^a,b   Fouillot Panchal, Maï ^a,b   Riani, Meriem ^a,b   Domenga Denier, Valérie ^a,b   Dussaule, Claire ^a,b   Cognat, Emmanuel ^a,b   Vinh, Joelle ^c   Joutel, Anne ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c ESPCI ParisTech   (France)

Author keywords

CADASIL; cerebrovasculature; extracellular matrix proteins; Notch3; protein aggregation

Indexed keywords

CYSTEINE; NOTCH3 RECEPTOR; SCLEROPROTEIN; TISSUE INHIBITOR OF METALLOPROTEINASE 3; VITRONECTIN;

ADULT; AGED; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN BLOOD VESSEL; BRAIN TISSUE; CADASIL; COMPLEX FORMATION; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; FRACTIONATION; GENE MUTATION; HUMAN; HUMAN CELL CULTURE; HUMAN TISSUE; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; IN SITU HYBRIDIZATION; IN VIVO STUDY; LIQUID CHROMATOGRAPHY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEOMICS; TANDEM MASS SPECTROMETRY; WESTERN BLOTTING; ZYMOGRAPHY;

EID: 84878874902     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awt092     Document Type: Article

References (40)

1. Arboleda-Velasquez JF, Manent J, Lee JH, Tikka S, Ospina C, Vanderburg CR, et al. Hypomorphic Notch 3 alleles link Notch signaling to ischemic cerebral small-vessel disease. Proc Natl Acad Sci USA 2011; 108: E128-35.
2. Chabriat H, Joutel A, Dichgans M, Tournier-Lasserve E, Bousser MG. Cadasil. Lancet Neurol 2009; 8: 643-53.
3. Dichgans M. Genetics of ischaemic stroke. Lancet Neurol 2007; 6: 149-61.
4. Domenga V, Fardoux P, Lacombe P, Monet M, Maciazek J, Krebs LT, et al. Notch3 is required for arterial identity and maturation of vascular smooth muscle cells. Genes Dev 2004; 18: 2730-5.
5. Dong H, Blaivas M, Wang MM. Bidirectional encroachment of collagen into the tunica media in cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy. Brain Res 2012; 1456: 64-71.
6. Duering M, Karpinska A, Rosner S, Hopfner F, Zechmeister M, Peters N, et al. Co-aggregate formation of CADASIL-mutant NOTCH3: a singleparticle analysis. Hum Mol Genet 2011; 20: 3256-65.
7. Ebrahem Q, Qi JH, Sugimoto M, Ali M, Sears JE, Cutler A, et al. Increased neovascularization in mice lacking tissue inhibitor of metalloproteinases-3. Invest Ophthalmol Vis Sci 2011; 52: 6117-23.
8. Fariss RN, Apte SS, Luthert PJ, Bird AC, Milam AH. Accumulation of tissue inhibitor of metalloproteinases-3 in human eyes with Sorsby's fundus dystrophy or retinitis pigmentosa. Br J Ophthalmol 1998; 82: 1329-34.
9. Fouillade C, Monet-Lepretre M, Baron-Menguy C, Joutel A. Notch signalling in smooth muscle cells during development and disease. Cardiovasc Res 2012; 95: 138-46.
10. Ishiko A, Shimizu A, Nagata E, Takahashi K, Tabira T, Suzuki N. Notch3 ectodomain is a major component of granular osmiophilic material (GOM) in CADASIL. Acta Neuropathol 2006; 112: 333-9.
11. Joutel A, Andreux F, Gaulis S, Domenga V, Cecillon M, Battail N, et al. The ectodomain of the Notch3 receptor accumulates within the cerebrovasculature of CADASIL patients. J Clin Invest 2000; 105: 597-605.
12. Joutel A, Corpechot C, Ducros A, Vahedi K, Chabriat H, Mouton P, et al. Notch3 mutations in CADASIL, a hereditary adult-onset condition causing stroke and dementia. Nature 1996; 383: 707-10.
13. Joutel A, Favrole P, Labauge P, Chabriat H, Lescoat C, Andreux F, et al. Skin biopsy immunostaining with a Notch3 monoclonal antibody for CADASIL diagnosis. Lancet 2001; 358: 2049-51.
14. Joutel A, Monet M, Domenga V, Riant F, Tournier-Lasserve E. Pathogenic mutations associated with cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy differently affect Jagged1 binding and Notch3 activity via the RBP/JK signaling pathway. Am J Hum Genet 2004; 74: 338-47.
15. Joutel A, Monet-Lepretre M, Gosele C, Baron-Menguy C, Hammes A, Schmidt S, et al. Cerebrovascular dysfunction and microcirculation rarefaction precede white matter lesions in a mouse genetic model of cerebral ischemic small vessel disease. J Clin Invest 2010; 120: 433-45.
16. Joutel A, Vahedi K, Corpechot C, Troesch A, Chabriat H, Vayssiere C, et al. Strong clustering and stereotyped nature of Notch3 mutations in CADASIL patients. Lancet 1997; 350: 1511-5.
17. Kopan R, Ilagan MX. The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 2009; 137: 216-33.
18. Lee MH, Atkinson S, Murphy G. Identification of the extracellular matrix (ECM) binding motifs of tissue inhibitor of metalloproteinases (TIMP)-3 and effective transfer to TIMP-1. J Biol Chem 2007; 282: 6887-98.
19. Lesnik Oberstein SA, van Duinen SG, van den Boom R, Maat-Schieman ML, van Buchem MA, van Houwelingen HC, et al. Evaluation of diagnostic NOTCH3 immunostaining in CADASIL. Acta Neuropathol (Berl) 2003; 106: 107-11.
20. Liu H, Sadygov RG, Yates JR III. A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal Chem 2004; 76: 4193-201.
21. Liu H, Zhang W, Kennard S, Caldwell RB, Lilly B. Notch3 is critical for proper angiogenesis and mural cell investment. Circ Res 2010; 107: 860-70.
22. Monet M, Domenga V, Lemaire B, Souilhol C, Langa F, Babinet C, et al. The archetypal R90C CADASIL-NOTCH3 mutation retains NOTCH3 function in vivo. Hum Mol Genet 2007; 16: 982-92.
23. Monet-Lepretre M, Bardot B, Lemaire B, Domenga V, Godin O, Dichgans M, et al. Distinct phenotypic and functional features of CADASIL mutations in the Notch3 ligand binding domain. Brain 2009; 132: 1601-12.
24. Nagase H, Visse R, Murphy G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res 2006; 69: 562-73.
25. Olzscha H, Schermann SM, Woerner AC, Pinkert S, Hecht MH, Tartaglia GG, et al. Amyloid-like aggregates sequester numerous metastable proteins with essential cellular functions. Cell 2011; 144: 67-78.
26. Opherk C, Duering M, Peters N, Karpinska A, Rosner S, Schneider E, et al. CADASIL mutations enhance spontaneous multimerization of NOTCH3. Hum Mol Genet 2009; 18: 2761-7.
27. Pantoni L. Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol 2010; 9: 689-701.
28. Peters N, Opherk C, Bergmann T, Castro M, Herzog J, Dichgans M. Spectrum of mutations in biopsy-proven CADASIL: implications for diagnostic strategies. Arch Neurol 2005; 62: 1091-4.
29. Peters N, Opherk C, Zacherle S, Capell A, Gempel P, Dichgans M. CADASIL-associated Notch3 mutations have differential effects both on ligand binding and ligand-induced Notch3 receptor signaling through RBP-Jk. Exp Cell Res 2004; 299: 454-64.
30. Preissner KT, Reuning U. Vitronectin in vascular context: facets of a multitalented matricellular protein. Semin Thromb Hemost 2011; 37: 408-24.
31. Qi JH, Ebrahem Q, Moore N, Murphy G, Claesson-Welsh L, Bond M, et al. A novel function for tissue inhibitor of metalloproteinases-3 (TIMP3): inhibition of angiogenesis by blockage of VEGF binding to VEGF receptor-2. Nat Med 2003; 9: 407-15.
32. Ruchoux MM, Domenga V, Brulin P, Maciazek J, Limol S, Tournier-Lasserve E, et al. Transgenic mice expressing mutant Notch3 develop vascular alterations characteristic of cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy. Am J Pathol 2003; 162: 329-42.
33. Ruchoux MM, Guerouaou D, Vandenhaute B, Pruvo JP, Vermersch P, Leys D. Systemic vascular smooth muscle cell impairment in cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy. Acta Neuropathol (Berl) 1995; 89: 500-12.
34. Shevchenko A. Evaluation of the efficiency of in-gel digestion of proteins by peptide isotopic labeling and MALDI mass spectrometry. Anal Biochem 2001; 296: 279-83.
35. Stetler-Stevenson WG. Tissue inhibitors of metalloproteinases in cell signaling: metalloproteinase-independent biological activities. Sci Signal 2008; 1: re6.
36. Stratman AN, Schwindt AE, Malotte KM, Davis GE. Endothelial-derived PDGF-BB and HB-EGF coordinately regulate pericyte recruitment during vasculogenic tube assembly and stabilization. Blood 2010; 116: 4720-30.
37. Tikka S, Mykkanen K, Ruchoux MM, Bergholm R, Junna M, Poyhonen M, et al. Congruence between NOTCH3 mutations and GOM in 131 CADASIL patients. Brain 2009; 132: 933-39.
38. Weber BH, Vogt G, Pruett RC, Stohr H, Felbor U. Mutations in the tissue inhibitor of metalloproteinases-3 (TIMP3) in patients with Sorsby's fundus dystrophy. Nat Genet 1994; 8: 352-6.
39. Wolfe KJ, Cyr DM. Amyloid in neurodegenerative diseases: friend or foe Semin Cell Dev Biol 2011; 22: 476-81.
40. Yousif S, Marie-Claire C, Roux F, Scherrmann JM, Decleves X. Expression of drug transporters at the blood-brain barrier using an optimized isolated rat brain microvessel strategy. Brain Res 2007; 1134: 1-11.