Modeling and rescue of the vascular phenotype of Williams-Beuren syndrome in patient induced pluripotent stem cells

Stem Cells Translational Medicine

Volumn 2, Issue 1, 2013, Pages 2-15

  Kinnear, Caroline ^a   Chang, Wing Y ^b,c   Khattak, Shahryar ^a   Hinek, Aleksander ^a   Thompson, Tadeo ^a   Rodrigues, Deivid de Carvalho ^a   Kennedy, Karen ^a   Mahmut, Naila ^a   Pasceri, Peter ^a   Stanford, William L ^b,c   Ellis, James ^a,d   Mital, Seema ^a  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^c UNIVERSITY OF OTTAWA   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

Cardiac; Pluripotent stem cells; Smooth muscle cells; Vascular development

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CALCIUM ION; ELASTIN; MATRIGEL; MYOSIN; NESTIN; RAPAMYCIN; REX PROTEIN; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX17; TUBULIN; DIFFERENTIATION ANTIGEN; KRUPPEL LIKE FACTOR; KRUPPEL LIKE FACTOR 4; MTOR PROTEIN, HUMAN; MYC PROTEIN; MYC PROTEIN, HUMAN; OCTAMER TRANSCRIPTION FACTOR 4; PEPTIDE FRAGMENT; POU5F1 PROTEIN, HUMAN; RECOMBINANT PROTEIN; SOX2 PROTEIN, HUMAN; TARGET OF RAPAMYCIN KINASE; TRANSCRIPTION FACTOR SOX; TRANSCRIPTOME;

ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DNA FINGERPRINTING; EPIFLUORESCENCE MICROSCOPY; FIBROBLAST; FLOW CYTOMETRY; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION; GENE SEQUENCE; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; MUSCLE CONTRACTILITY; PHENOTYPE; PLURIPOTENT STEM CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SMOOTH MUSCLE FIBER; WILLIAMS BEUREN SYNDROME; BIOSYNTHESIS; CALCIUM SIGNALING; CELL CULTURE; DNA SEQUENCE; DRUG ANTAGONISM; DRUG EFFECT; GENETICS; HEMIZYGOTE; MALE; METABOLISM; MUSCLE CONTRACTION; PATHOLOGY; PHYSIOLOGY; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULAR SMOOTH MUSCLE;

ANTIGENS, DIFFERENTIATION; CALCIUM SIGNALING; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; FIBROBLASTS; HEMIZYGOTE; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MALE; MUSCLE CONTRACTION; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; OCTAMER TRANSCRIPTION FACTOR-3; PEPTIDE FRAGMENTS; PHENOTYPE; PROTO-ONCOGENE PROTEINS C-MYC; RECOMBINANT PROTEINS; SEQUENCE ANALYSIS, DNA; SIROLIMUS; SOXB1 TRANSCRIPTION FACTORS; TOR SERINE-THREONINE KINASES; TRANSCRIPTOME; WILLIAMS SYNDROME;

MLCS; MLOWN;

EID: 84873466364     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.5966/sctm.2012-0054     Document Type: Article

References (60)

1. Pober BR. Williams-Beuren syndrome. N Engl J Med 2010;362:239-252.
2. Wessel A, Gravenhorst V, Buchhorn R et al. Risk of sudden death in the Williams-Beuren syndrome. Am J Med Genet Part A 2004;127A:234-237.
3. Kececioglu D, Kotthoff S, Vogt J. WilliamsBeuren syndrome: A 30-year follow-up of natural and postoperative course. Eur Heart J 1993;14:1458-1464.
4. Metcalfe K, Rucka AK, Smoot L et al. Elastin: Mutational spectrum in supravalvular aortic stenosis. Eur J Hum Genet 2000;8: 955-963.
5. Li DY, Brooke B, Davis EC et al. Elastin is an essential determinant of arterial morphogenesis. Nature 1998;393:276-280.
6. Li DY, Faury G, Taylor DG et al. Novel arterial pathology in mice and humans hemizygous for elastin. J Clin Invest 1998;102: 1783-1787.
7. Akhtar K, Broekelmann TJ, Miao M et al. Oxidative and nitrosative modifications of tropoelastin prevent elastic fiber assembly in vitro. J Biol Chem 2010;285:37396-37404.
8. Kim Y-M, Haghighat L, Spiekerkoetter E et al. Neutrophil elastase is produced by pulmonary artery smooth muscle cells and is linked to neointimal lesions. Am J Pathol 2011;179:1560-1572.
9. Urbán Z, Riazi S, Seidl TL et al. Connection between elastin haploinsufficiency and increased cell proliferation in patients with supravalvular aortic stenosis and Williams-Beuren syndrome. Am J Hum Genet 2002;71:30-44.
10. Arribas SM, Hinek A, González MC. Elastic fibres and vascular structure in hypertension. Pharmacol Ther 2006;111:771-791.
11. Faury G, Ristori MT, Verdetti J et al. Effect of elastin peptides on vascular tone. J Vasc Res 1995;32:112-119.
12. Fülöp T, Jacob MP, Wallach J et al. The elastin-laminin receptor [in French]. J Soc Biol 2001;195:157-164.
13. Mochizuki S, Brassart B, Hinek A. Signaling pathways transduced through the elastin receptor facilitate proliferation of arterial smooth muscle cells. J Biol Chem 2002;277: 44854-44863.
14. Kozel BA, Knutsen RH, Ye L et al. Genetic modifiers of cardiovascular phenotype caused by elastin haploinsufficiency act by extrinsic noncomplementation. J Biol Chem 2011;286: 44926-44936.
15. Hirano E, Knutsen RH, Sugitani H et al. Functional rescue of elastin insufficiency in mice by the human elastin gene. Circ Res 2007; 101:523-531.
16. Li HH, Roy M, Kuscuoglu U et al. Induced chromosome deletions cause hypersociability and other features of WilliamsBeuren syndrome in mice. EMBO Mol Med 2009;1:50-65.
17. Osborne LR. Animal models of Williams syndrome. Am J Med Genet C Semin Med Genet 2010;154C:209-219.
18. Chang WY, Garcha K, Manias JL et al. Deciphering the complexities of human diseases and disorders by coupling induced-pluripotent stem cells and systems genetics. Wiley Interdiscip Rev Syst Biol Med 2012;4:339-350.
19. Carvajal-Vergara X, Sevilla A, D'Souza SL et al. Patient-specific induced pluripotent stem-cell-derived models of LEOPARD syndrome. Nature 2010;465:808-812.
20. Moretti A, Bellin M, Welling A et al. Patient-specific induced pluripotent stem-cell models for long-QT syndrome. N Engl J Med 2010;363:1397-1409.
21. Yazawa M, Hsueh B, Jia X et al. Using induced pluripotent stem cells to investigate cardiac phenotypes in Timothy syndrome. Nature 2011;471:230-234.
22. Zhang J, Lian Q, Zhu G et al. A human iPSC model of Hutchinson Gilford progeria reveals vascular smooth muscle and mesenchymal stem cell defects. Cell Stem Cell 2011;8:31-45.
23. Liu GH, Barkho BZ, Ruiz S et al. Recapitulation of premature ageing with iPSCs from Hutchinson-Gilford progeria syndrome. Nature 2011;472:221-225.
24. Itzhaki I, Maizels L, Huber I et al. Modelling the long QT syndrome with induced pluripotent stem cells. Nature 2011;471: 225-229.
25. Ebert AD, Yu J, Rose FF, Jr., et al. Induced pluripotent stem cells from a spinal muscular atrophy patient. Nature 2009;457: 277-280.
26. Marchetto MC, Carromeu C, Acab A et al. A model for neural development and treatment of Rett syndrome using human induced pluripotent stem cells. Cell 2010;143: 527-539.
27. Lee G, Papapetrou EP, Kim H et al. Modelling pathogenesis and treatment of familial dysautonomia using patient-specific iPSCs. Nature 2009;461:402-406.
28. Hinek A. Nature and multiple functions of the 67 kD elastin/laminin binding protein. Cell Adhes Commun 1994;2:185-193.
29. Poon M, Badimon JJ, Fuster V. Overcoming restenosis with sirolimus: From alphabet soup to clinical reality. Lancet 2002;359:619-622.
30. Poon M, Marx SO, Gallo R et al. Rapamycin inhibits vascular smooth muscle cell migration. J Clin Invest 1996;98:2277-2283.
31. Suzuki T, Kopia G, Hayashi S-i et al. Stentbased delivery of sirolimus reduces neointimal formation in a porcine coronary model. Circulation 2001;104:1188-1193.
32. Hotta A, Cheung AY, Farra N et al. EOS lentiviral vector selection system for human induced pluripotent stem cells. Nat Protoc 2009; 4:1828-1844.
33. Cheung AY, Horvath LM, Grafodatskaya D et al. Isolation of MECP2-null Rett Syndrome patient hiPS cells and isogenic controls through X-chromosome inactivation. Hum Mol Genet 2011;20:2103-2115.
34. Amenduni M, De Filippis R, Cheung AY et al. iPS cells to model CDKL5-related disorders. Eur J Hum Genet 2011;19:1246-1255.
35. Hotta A, Cheung AY, Farra N et al. Isolation of human iPS cells using EOS lentiviral vectors to select for pluripotency. Nat Methods 2009;6:370-376.
36. Xie C-Q, Zhang J, Villacorta L et al. A highly efficient method to differentiate smooth muscle cells from human embryonic stem cells. Arterioscler Thromb Vasc Biol 2007; 27:e311-e312.
37. Hill KL, Obrtlikova P, Alvarez DF et al. Human embryonic stem cell-derived vascular progenitor cells capable of endothelial and smooth muscle cell function. Exp Hematol 2010;38:246-257.e1.
38. Song J, Rolfe BE, Hayward IP et al. Reorganization of structural proteins in vascular smooth muscle cells grown in collagen gel and basement membrane matrices (Matrigel): A comparison with their in situ counterparts. J Struct Biol 2001;133:43-54.
39. Tkachuk N, Tkachuk S, Patecki M et al. The tight junction protein ZO-2 and Janus kinase 1 mediate intercellular communications in vascular smooth muscle cells. Biochem Biophys Res Commun 2011;410: 531-536.
40. Hamed S, Barshack I, Luboshits G et al. Erythropoietin improves myocardial performance in doxorubicin-induced cardiomyopathy. Eur Heart J 2006;27:1876-1883.
41. Chan EM, Ratanasirintrawoot S, Park IH et al. Live cell imaging distinguishes bona fide human iPS cells from partially reprogrammed cells. Nat Biotechnol 2009;27: 1033-1037.
42. Yang L, Soonpaa MH, Adler ED et al. Human cardiovascular progenitor cells develop from a KDR embryonic-stem-cell-derived population. Nature 2008;453:524-528.
43. Cheung C, Bernardo AS, Trotter MWB et al. Generation of human vascular smooth muscle subtypes provides insight into embryological origin-dependent disease susceptibility. Nat Biotechnol 2012;30:165-173.
44. Duca L, Blanchevoye C, Cantarelli BT et al. The elastin receptor complex transduces signals through the catalytic activity of its Neu-1 subunit. J Biol Chem 2007;282:12484-12491.
45. Gerecht-Nir S, Ziskind A, Cohen S et al. Human embryonic stem cells as an in vitro model for human vascular development and the induction of vascular differentiation. Lab Invest 2003;83:1811-1820.
46. Cordes KR, Sheehy NT, White MP et al. miR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature 2009;460:705-710.
47. Xu N, Papagiannakopoulos T, Pan G et al. MicroRNA-145 regulates OCT4, SOX2, and KLF4 and represses pluripotency in human embryonic stem cells. Cell 2009;137:647-658.
48. Kim KY, Hysolli E, Park IH. Neuronal maturation defect in induced pluripotent stem cells from patients with Rett syndrome. Proc Natl Acad Sci USA 2011;108:14169-14174.
49. Majesky MW, Mummery CL. Smooth muscle diversity from human pluripotent cells. Nat Biotechnol 2012;30:152-154.
50. Ge X, Ren Y, Bartulos O et al. Modeling supravalvular aortic stenosis syndrome using human induced pluripotent stem cells. Circulation 2012;126:1695-1704.
51. Majesky MW. Developmental basis of vascular smooth muscle diversity. Arterioscler Thromb Vasc Biol 2007;27:1248-1258.
52. Majesky MW, Dong XR, Regan JN et al. Vascular smooth muscle progenitor cells. Circ Res 2011;108:365-377.
53. Bassareo PP, Mercuro G. Increased arterial stiffness in children with Williams syndrome and normal blood pressure. Blood Press Monit 2010;15:257-261.
54. Sen S, Bunda S, Shi J et al. Retinoblastoma protein modulates the inverse relationship between cellular proliferation and elastogenesis. J Biol Chem 2011;286:36580-36591.
55. Lee K-J, Hinek A, Chaturvedi RR et al. Rapamycin-eluting stents in the arterial duct. Circulation 2009;119:2078-2085.
56. Ruan B, Pong K, Jow F et al. Binding of rapamycin analogs to calcium channels and FKBP52 contributes to their neuroprotective activities. Proc Natl Acad Sci USA 2008;105:33-38.
57. 2+ release by mammalian target of rapamycin (mTOR) in RINm5F cells. J Cell Biochem 2011;112:723-733.
58. Sawyers CL. The cancer biomarker problem. Nature 2008;452:548-552.
59. Kaiser C, Galatius S, Erne P et al. Drugeluting versus bare-metal stents in large coronary arteries. N Engl J Med 2010;363:2310-2319.
60. Kastrati A, Mehilli J, Pache J et al. Analysis of 14 trials comparing sirolimus-eluting stents with bare-metal stents. N Engl J Med 2007;356: 1030-1039.