Transcriptome analysis for Notch3 target genes identifies Grip2 as a novel regulator of myogenic response in the cerebrovasculature

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 33, Issue 1, 2013, Pages 76-86

  Fouillade, Charles ^a,b   Baron Menguy, Céline ^a,b   Domenga Denier, Valérie ^a,b   Thibault, Christelle ^c   Takamiya, Kogo ^d   Huganir, Richard ^e   Joutel, Anne ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^d UNIVERSITY OF MIYAZAKI   (Japan)

^e JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

cerebrovasculature; myogenic response; Notch3; smooth muscle cell; transcriptome

Indexed keywords

GLUTAMATE RECEPTOR INTERACTING PROTEIN 2; IMMUNOGLOBULIN J RECOMBINATION SIGNAL SEQUENCE BINDING PROTEIN; NOTCH3 RECEPTOR; POTASSIUM CHANNEL KV1.5; TRANSCRIPTOME; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ARTERY; BRAIN BLOOD VESSEL; CONTROLLED STUDY; GENE CONTROL; GENE DELETION; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENE LOSS; GENE TARGETING; MALE; MOLECULAR DYNAMICS; MOUSE; MUSCLE CONTRACTION; MUSCLE DEVELOPMENT; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; RNA ANALYSIS; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER;

ALANINE; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; AZEPINES; CARRIER PROTEINS; CEREBRAL ARTERIES; ENZYME INHIBITORS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; IMMUNOGLOBULIN J RECOMBINATION SIGNAL SEQUENCE-BINDING PROTEIN; KV1.5 POTASSIUM CHANNEL; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NERVE TISSUE PROTEINS; RECEPTORS, NOTCH; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; VASOCONSTRICTION; VASOCONSTRICTOR AGENTS; VASODILATION; VASODILATOR AGENTS;

EID: 84871757594     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.112.251736     Document Type: Article

References (52)

1. Hill MA, Meininger GA, Davis MJ, Laher I. Therapeutic potential of pharmacologically targeting arteriolar myogenic tone. Trends Pharmacol Sci. 2009;30:363-374.
2. Iadecola C, Davisson RL. Hypertension and cerebrovascular dysfunction. Cell Metab. 2008;7:476-484.
3. Pantoni L. Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol. 2010;9:689-701.
4. Hofmann JJ, Iruela-Arispe ML. Notch signaling in blood vessels: who is talking to whom about what? Circ Res. 2007;100:1556-1568.
5. Phng LK, Gerhardt H. Angiogenesis: a team effort coordinated by notch. Dev Cell. 2009;16:196-208.
6. Fouillade C, Monet-Leprêtre M, Baron-Menguy C, Joutel A. Notch signalling in smooth muscle cells during development and disease. Cardiovasc Res. 2012;95:138-146.
7. Domenga V, Fardoux P, Lacombe P, Monet M, Maciazek J, Krebs LT, Klonjkowski B, Berrou E, Mericskay M, Li Z, Tournier-Lasserve E, Gridley T, Joutel A. Notch3 is required for arterial identity and maturation of vascular smooth muscle cells. Genes Dev. 2004;18:2730-2735.
8. Proweller A, Wright AC, Horng D, Cheng L, Lu MM, Lepore JJ, Pear WS, Parmacek MS. Notch signaling in vascular smooth muscle cells is required to pattern the cerebral vasculature. Proc Natl Acad Sci USA. 2007;104:16275-16280.
9. Joutel A. Pathogenesis of CADASIL: transgenic and knock-out mice to probe function and dysfunction of the mutated gene, Notch3, in the cerebrovasculature. Bioessays. 2011;33:73-80.
10. Belin de Chantemele EJ, Retailleau K, Pinaud F, Vessieres E, Bocquet A, Guihot AL, Lemaire B, Domenga V, Baufreton C, Loufrani L, Joutel A, Henrion D. Notch3 is a major regulator of vascular tone in cerebral and tail resistance arteries. Arterioscler Thromb Vasc Biol. 2008;28: 2216-2224.
11. Arboleda-Velasquez JF, Zhou Z, Shin HK, Louvi A, Kim HH, Savitz SI, Liao JK, Salomone S, Ayata C, Moskowitz MA, Artavanis-Tsakonas S. Linking Notch signaling to ischemic stroke. Proc Natl Acad Sci USA. 2008;105:4856-4861.
12. Joutel A, Corpechot C, Ducros A, et al. Notch3 mutations in CADASIL, a hereditary adult-onset condition causing stroke and dementia. Nature. 1996;383:707-710.
13. Kopan R, Ilagan MX. The canonical Notch signaling pathway: unfolding the activation mechanism. Cell. 2009;137:216-233.
14. Sanalkumar R, Dhanesh SB, James J. Non-canonical activation of Notch signaling/target genes in vertebrates. Cell Mol Life Sci. 2010;67:2957-2968.
15. Heitzler P. Biodiversity and noncanonical Notch signaling. Curr Top Dev Biol. 2010;92:457-481.
16. Andersson ER, Sandberg R, Lendahl U. Notch signaling: simplicity in design, versatility in function. Development. 2011;138:3593-3612.
17. Bray S, Bernard F. Notch targets and their regulation. Curr Top Dev Biol. 2010;92:253-275.
18. Monet M, Domenga V, Lemaire B, Souilhol C, Langa F, Babinet C, Gridley T, Tournier-Lasserve E, Cohen-Tannoudji M, Joutel A. The archetypal R90C CADASIL-NOTCH3 mutation retains NOTCH3 function in vivo. Hum Mol Genet. 2007;16:982-992.
19. Jin S, Hansson EM, Tikka S, Lanner F, Sahlgren C, Farnebo F, Baumann M, Kalimo H, Lendahl U. Notch signaling regulates platelet-derived growth factor receptor-beta expression in vascular smooth muscle cells. Circ Res. 2008;102:1483-1491.
20. Scheppke L, Murphy EA, Zarpellon A, Hofmann JJ, Merkulova A, Shields DJ, Weis SM, Byzova TV, Ruggeri ZM, Iruela-Arispe ML, Cheresh DA. Notch promotes vascular maturation by inducing integrin-mediated smooth muscle cell adhesion to the endothelial basement membrane. Blood. 2012;119:2149-2158.
21. Han H, Tanigaki K, Yamamoto N, Kuroda K, Yoshimoto M, Nakahata T, Ikuta K, Honjo T. Inducible gene knockout of transcription factor recombination signal binding protein-J reveals its essential role in T versus B lineage decision. Int Immunol. 2002;14:637-645.
22. Wirth A, Benyó Z, Lukasova M, Leutgeb B, Wettschureck N, Gorbey S, Orsy P, Horváth B, Maser-Gluth C, Greiner E, Lemmer B, Schütz G, Gutkind JS, Offermanns S. G12-G13-LARG-mediated signaling in vascular smooth muscle is required for salt-induced hypertension. Nat Med. 2008;14:64-68.
23. Souilhol C, Cormier S, Monet M, Vandormael-Pournin S, Joutel A, Babinet C, Cohen-Tannoudji M. Nas transgenic mouse line allows visualization of Notch pathway activity in vivo. Genesis. 2006;44:277-286.
24. Takamiya K, Kostourou V, Adams S, Jadeja S, Chalepakis G, Scambler PJ, Huganir RL, Adams RH. A direct functional link between the multi-PDZ domain protein GRIP1 and the Fraser syndrome protein Fras1. Nat Genet. 2004;36:172-177.
25. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet. 1999;21:70-71.
26. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003;4:249-264.
27. Dong H, Zhang P, Song I, Petralia RS, Liao D, Huganir RL. Characterization of the glutamate receptor-interacting proteins GRIP1 and GRIP2. J Neurosci. 1999;19:6930-6941.
28. Joutel A, Monet-Leprêtre M, Gosele C, Baron-Menguy C, Hammes A, Schmidt S, Lemaire-Carrette B, Domenga V, Schedl A, Lacombe P, Hubner N. Cerebrovascular dysfunction and microcirculation rarefaction precede white matter lesions in a mouse genetic model of cerebral ischemic small vessel disease. J Clin Invest. 2010;120:433-445.
29. Oloizia B, Paul RJ. Ca2+ clearance and contractility in vascular smooth muscle: evidence from gene-altered murine models. J Mol Cell Cardiol. 2008;45:347-362.
30. Salomone S, Potts EM, Tyndall S, Ip PC, Chun J, Brinkmann V, Waeber C. Analysis of sphingosine 1-phosphate receptors involved in constriction of isolated cerebral arteries with receptor null mice and pharmacological tools. Br J Pharmacol. 2008;153:140-147.
31. Plane F, Johnson R, Kerr P, Wiehler W, Thorneloe K, Ishii K, Chen T, Cole W. Heteromultimeric Kv1 channels contribute to myogenic control of arterial diameter. Circ Res. 2005;96:216-224.
32. Krishna K, Redies C. Expression of cadherin superfamily genes in brain vascular development. J Cereb Blood Flow Metab. 2009;29: 224-229.
33. Guo K, Li J, Wang H, Osato M, Tang JP, Quah SY, Gan BQ, Zeng Q. PRL-3 initiates tumor angiogenesis by recruiting endothelial cells in vitro and in vivo. Cancer Res. 2006;66:9625-9635.
34. Liu H, Kennard S, Lilly B. NOTCH3 expression is induced in mural cells through an autoregulatory loop that requires endothelial-expressed JAGGED1. Circ Res. 2009;104:466-475.
35. Mao L, Takamiya K, Thomas G, Lin DT, Huganir RL. GRIP1 and 2 regulate activity-dependent AMPA receptor recycling via exocyst complex interactions. Proc Natl Acad Sci USA. 2010;107:19038-19043.
36. Dong H, O'Brien RJ, Fung ET, Lanahan AA, Worley PF, Huganir RL. GRIP: a synaptic PDZ domain-containing protein that interacts with AMPA receptors. Nature. 1997;386:279-284.
37. DeSouza S, Fu J, States BA, Ziff EB. Differential palmitoylation directs the AMPA receptor-binding protein ABP to spines or to intracellular clusters. J Neurosci. 2002;22:3493-3503.
38. Cipolla MJ, Smith J, Kohlmeyer MM, Godfrey JA. SKCa and IKCa channels, myogenic tone, and vasodilator responses in middle cerebral arteries and parenchymal arterioles: effect of ischemia and reperfusion. Stroke. 2009;40:1451-1457.
39. Brückner K, Pablo Labrador J, Scheiffele P, Herb A, Seeburg PH, Klein R. EphrinB ligands recruit GRIP family PDZ adaptor proteins into raft membrane microdomains. Neuron. 1999;22:511-524.
40. Stegmüller J, Werner H, Nave KA, Trotter J. The proteoglycan NG2 is complexed with alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors by the PDZ glutamate receptor interaction protein (GRIP) in glial progenitor cells. Implications for glial-neuronal signaling. J Biol Chem. 2003;278:3590-3598.
41. Wyszynski M, Kim E, Dunah AW, Passafaro M, Valtschanoff JG, Serra-Pagès C, Streuli M, Weinberg RJ, Sheng M. Interaction between GRIP and liprin-alpha/SYD2 is required for AMPA receptor targeting. Neuron. 2002;34:39-52.
42. Monea S, Jordan BA, Srivastava S, DeSouza S, Ziff EB. Membrane localization of membrane type 5 matrix metalloproteinase by AMPA receptor binding protein and cleavage of cadherins. J Neurosci. 2006;26:2300-2312.
43. Foo SS, Turner CJ, Adams S, Compagni A, Aubyn D, Kogata N, Lindblom P, Shani M, Zicha D, Adams RH. Ephrin-B2 controls cell motility and adhesion during blood-vessel-wall assembly. Cell. 2006;124:161-173.
44. Otten J, van der Ven PF, Vakeel P, Eulitz S, Kirfel G, Brandau O, Boesl M, Schrickel JW, Linhart M, Hayess K, Naya FJ, Milting H, Meyer R, Fürst DO. Complete loss of murine Xin results in a mild cardiac phenotype with altered distribution of intercalated discs. Cardiovasc Res. 2010;85:739-750.
45. Vicent S, Luis-Ravelo D, Antón I, García-Tuñón I, Borrás-Cuesta F, Dotor J, De Las Rivas J, Lecanda F. A novel lung cancer signature mediates metastatic bone colonization by a dual mechanism. Cancer Res. 2008;68:2275-2285.
46. Greiner EF, Kirfel J, Greschik H, Huang D, Becker P, Kapfhammer JP, Schüle R. Differential ligand-dependent protein-protein interactions between nuclear receptors and a neuronal-specific cofactor. Proc Natl Acad Sci USA. 2000;97:7160-7165.
47. Zhang J, Yu L, Fu Q, Gao J, Xie Y, Chen J, Zhang P, Liu Q, Zhao S. Mouse phosphoglycerate mutase M and B isozymes: cDNA cloning, enzyme activity assay and mapping. Gene. 2001;264:273-279.
48. Chen TT, Luykenaar KD, Walsh EJ, Walsh MP, Cole WC. Key role of Kv1 channels in vasoregulation. Circ Res. 2006;99:53-60.
49. Murakami A, Takasugi H, Ohnuma S, et al. Sphingosine 1-phosphate (S1P) regulates vascular contraction via S1P3 receptor: investigation based on a new S1P3 receptor antagonist. Mol Pharmacol. 2010;77:704-713.
50. Wellman GC, Santana LF, Bonev AD, Nelson MT. Role of phospholamban in the modulation of arterial Ca(2+) sparks and Ca(2+)-activated K(+) channels by cAMP. Am J Physiol Cell Physiol. 2001;281:C1029-C1037.
51. Ledoux J, Werner ME, Brayden JE, Nelson MT. Calcium-activated potassium channels and the regulation of vascular tone. Physiology. 2006;21:69-78.
52. Manderfield LJ, High FA, Engleka KA, Liu F, Li L, Rentschler S, Epstein JA. Notch activation of Jagged1 contributes to the assembly of the arterial wall. Circulation. 2012;125:314-323.