A receptor-specific function for Notch2 in mediating vascular smooth muscle cell growth arrest through cyclin-dependent kinase inhibitor 1B

Circulation Research

Volumn 113, Issue 8, 2013, Pages 975-985

  Boucher, Joshua M ^a   Harrington, Anne ^a   Rostama, Bahman ^a   Lindner, Volkhard ^a   Liaw, Lucy ^a  

^a Maine Medical Center Research Institute   (United States)

Author keywords

Carotid intima media thickness; Cell proliferation; Receptors, Notch; Smooth muscle; Vascular intima

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1B; CYCLINE; F BOX PROTEIN; JAGGED1; NOTCH2 RECEPTOR; NOTCH3 RECEPTOR; PROTEIN P27; S PHASE KINASE ASSOCIATED PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CAROTID ARTERY; CELL CYCLE; CELL GROWTH; CONTROLLED STUDY; HALF LIFE TIME; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; UBIQUITINATION; VASCULAR DISEASE; VASCULAR SMOOTH MUSCLE;

CAROTID INTIMA-MEDIA THICKNESS; CELL PROLIFERATION; RECEPTORS, NOTCH; SMOOTH MUSCLE; VASCULAR INTIMA;

ANIMALS; CALCIUM-BINDING PROTEINS; CAROTID ARTERIES; CAROTID ARTERY INJURIES; CELL CYCLE; CELL PROLIFERATION; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE INHIBITOR P27; DISEASE MODELS, ANIMAL; HUMANS; HYPERPLASIA; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MEMBRANE PROTEINS; MICE; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PHENOTYPE; PROLIFERATING CELL NUCLEAR ANTIGEN; RECEPTOR, NOTCH2; RNA INTERFERENCE; S-PHASE KINASE-ASSOCIATED PROTEINS; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION;

EID: 84885307987     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.113.301272     Document Type: Article

References (37)

1. Alexander MR, Owens GK. Epigenetic control of smooth muscle cell differentiation and phenotypic switching in vascular development and disease. Annu Rev Physiol. 2012;74:13-40
2. 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
3. Boucher J, Gridley T, Liaw L. Molecular pathways of notch signaling in vascular smooth muscle cells. Front Physiol. 2012;3:81
4. 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
5. Joutel A, Vahedi K, Corpechot C, Troesch A, Chabriat H, Vayssière C, Cruaud C, Maciazek J, Weissenbach J, Bousser MG, Bach JF, Tournier- Lasserve E. Strong clustering and stereotyped nature of Notch3 mutations in CADASIL patients. Lancet. 1997;350:1511-1515
6. McCright B, Gao X, Shen L, Lozier J, Lan Y, Maguire M, Herzlinger D, Weinmaster G, Jiang R, Gridley T. Defects in development of the kidney, heart and eye vasculature in mice homozygous for a hypomorphic Notch2 mutation. Development. 2001;128:491-502
7. Varadkar P, Kraman M, Despres D, Ma G, Lozier J, McCright B. Notch2 is required for the proliferation of cardiac neural crest-derived smooth muscle cells. Dev Dyn. 2008;237:1144-1152
8. Wang Q, Zhao N, Kennard S, Lilly B. Notch2 and Notch3 function together to regulate vascular smooth muscle development. PLoS One. 2012;7:e37365
9. Wu X, Zou Y, Zhou Q, Huang L, Gong H, Sun A, Tateno K, Katsube K, Radtke F, Ge J, Minamino T, Komuro I. Role of Jagged1 in arterial lesions after vascular injury. Arterioscler Thromb Vasc Biol. 2011;31:2000-2006
10. Kumar A, Hoover JL, Simmons CA, Lindner V, Shebuski RJ. Remodeling and neointimal formation in the carotid artery of normal and P-selectindeficient mice. Circulation. 1997;96:4333-4342
11. Tang Y, Urs S, Boucher J, Bernaiche T, Venkatesh D, Spicer DB, Vary CP, Liaw L. Notch and transforming growth factor-beta (TGFbeta) signaling pathways cooperatively regulate vascular smooth muscle cell differentiation. J Biol Chem. 2010;285:17556-17563
12. Boucher JM, Peterson SM, Urs S, Zhang C, Liaw L. The miR-143/145 cluster is a novel transcriptional target of Jagged-1/Notch signaling in vascular smooth muscle cells. J Biol Chem. 2011;286:28312-28321
13. Li Y, Takeshita K, Liu PY, Satoh M, Oyama N, Mukai Y, Chin MT, Krebs L, Kotlikoff MI, Radtke F, Gridley T, Liao JK. Smooth muscle Notch1 mediates neointimal formation after vascular injury. Circulation. 2009;119:2686-2692
14. 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
15. Wessely R. New drug-eluting stent concepts. Nat Rev Cardiol. 2010;7:194-203
16. Hirota T, Lipp JJ, Toh BH, Peters JM. Histone H3 serine 10 phosphorylation by Aurora B causes HP1 dissociation from heterochromatin. Nature. 2005;438:1176-1180
17. Chen M, Huang J, Yang X, Liu B, Zhang W, Huang L, Deng F, Ma J, Bai Y, Lu R, Huang B, Gao Q, Zhuo Y, Ge J. Serum starvation induced cell cycle synchronization facilitates human somatic cells reprogramming. PLoS One. 2012;7:e28203
18. Tanner FC, Boehm M, Akyürek LM, San H, Yang ZY, Tashiro J, Nabel GJ, Nabel EG. Differential effects of the cyclin-dependent kinase inhibitors p27(Kip1), p21(Cip1), and p16(Ink4) on vascular smooth muscle cell proliferation. Circulation. 2000;101:2022-2025
19. Tanner FC, Greutert H, Barandier C, Frischknecht K, Lüscher TF. Different cell cycle regulation of vascular smooth muscle in genetic hypertension. Hypertension. 2003;42:184-188
20. Lacy ER, Filippov I, Lewis WS, Otieno S, Xiao L, Weiss S, Hengst L, Kriwacki RW. p27 binds cyclin-CDK complexes through a sequential mechanism involving binding-induced protein folding. Nat Struct Mol Biol. 2004;11:358-364
21. Ishida N, Kitagawa M, Hatakeyama S, Nakayama K. Phosphorylation at serine 10, a major phosphorylation site of p27(Kip1), increases its protein stability. J Biol Chem. 2000;275:25146-25154
22. Kotake Y, Nakayama K, Ishida N, Nakayama KI. Role of serine 10 phosphorylation in p27 stabilization revealed by analysis of p27 knock-in mice harboring a serine 10 mutation. J Biol Chem. 2005;280:1095-1102
23. Carrano AC, Eytan E, Hershko A, Pagano M. SKP2 is required for ubiquitin-mediated degradation of the CDK inhibitor p27. Nat Cell Biol. 1999;1:193-199
24. Shirane M, Harumiya Y, Ishida N, Hirai A, Miyamoto C, Hatakeyama S, Nakayama K, Kitagawa M. Down-regulation of p27(Kip1) by two mechanisms, ubiquitin-mediated degradation and proteolytic processing. J Biol Chem. 1999;274:13886-13893
25. Dohda T, Maljukova A, Liu L, Heyman M, Grandér D, Brodin D, Sangfelt O, Lendahl U. Notch signaling induces SKP2 expression and promotes reduction of p27Kip1 in T-cell acute lymphoblastic leukemia cell lines. Exp Cell Res. 2007;313:3141-3152
26. Sarmento LM, Huang H, Limon A, Gordon W, Fernandes J, Tavares MJ, Miele L, Cardoso AA, Classon M, Carlesso N. Notch1 modulates timing of G1-S progression by inducing SKP2 transcription and p27 Kip1 degradation. J Exp Med. 2005;202:157-168
27. Wu YJ, Sala-Newby GB, Shu KT, Yeh HI, Nakayama KI, Nakayama K, Newby AC, Bond M. S-phase kinase-associated protein-2 (Skp2) promotes vascular smooth muscle cell proliferation and neointima formation in vivo. J Vasc Surg. 2009;50:1135-1142
28. Wu YJ, Bond M, Sala-Newby GB, Newby AC. Altered S-phase kinaseassociated protein-2 levels are a major mediator of cyclic nucleotide-induced inhibition of vascular smooth muscle cell proliferation. Circ Res. 2006;98:1141-1150
29. Majesky MW. Developmental basis of vascular smooth muscle diversity. Arterioscler Thromb Vasc Biol. 2007;27:1248-1258
30. Gizard F, Zhao Y, Findeisen HM, Qing H, Cohn D, Heywood EB, Jones KL, Nomiyama T, Bruemmer D. Transcriptional regulation of S phase kinase-associated protein 2 by NR4A orphan nuclear receptor NOR1 in vascular smooth muscle cells. J Biol Chem. 2011;286:35485-35493
31. Caolo V, Schulten HM, Zhuang ZW, Murakami M, Wagenaar A, Verbruggen S, Molin DG, Post MJ. Soluble Jagged-1 inhibits neointima formation by attenuating Notch-Herp2 signaling. Arterioscler Thromb Vasc Biol. 2011;31:1059-1065
32. Pan D, Yang J, Lu F, Xu D, Zhou L, Shi A, Cao K. Platelet-derived growth factor BB modulates PCNA protein synthesis partially through the transforming growth factor beta signalling pathway in vascular smooth muscle cells. Biochem Cell Biol. 2007;85:606-615
33. Redmond EM, Guha S, Walls D, Cahill PA. Investigational Notch and Hedgehog inhibitors-therapies for cardiovascular disease. Expert Opin Investig Drugs. 2011;20:1649-1664
34. Haapasalo A, Kovacs DM. The many substrates of presenilin/gammasecretase. J Alzheimers Dis. 2011;25:3-28
35. Wu Y, Cain-Hom C, Choy L, et al. Therapeutic antibody targeting of individual Notch receptors. Nature. 2010;464:1052-1057
36. Thyberg J. Phenotypic modulation of smooth muscle cells during formation of neointimal thickenings following vascular injury. Histol Histopathol. 1998;13:871-891
37. McDaniell R, Warthen DM, Sanchez-Lara PA, Pai A, Krantz ID, Piccoli DA, Spinner NB. NOTCH2 mutations cause Alagille syndrome, a heterogeneous disorder of the notch signaling pathway. Am J Hum Genet. 2006;79:169-173