ROCK suppression promotes differentiation and expansion of endothelial cells from embryonic stem cell-derived Flk1+ mesodermal precursor cells

Blood

Volumn 120, Issue 13, 2012, Pages 2733-2744

  Joo, Hyung Joon ^a,b   Choi, Dong Kyu ^a   Lim, Joon Seo ^a   Park, Jin Sung ^a   Lee, Seung Hun ^a   Song, Sukhyun ^a   Shin, Jennifer H ^a   Lim, Do Sun ^b   Kim, Injune ^a   Hwang, Ki Chul ^c   Koh, Gou Young ^a  

^a Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^b Korea University College of Medicine   (South Korea)

^c Yonsei University College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

12 (2 CYANOETHYL) 6,7,12,13 TETRAHYDRO 13 METHYL 5 OXOINDOLO[2,3 A]PYRROLO[3,4 C]CARBAZOLE; 2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; 4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; 4 [4 (1,3 BENZODIOXOL 5 YL) 5 (2 PYRIDINYL) 1H IMIDAZOL 2 YL]BENZAMIDE; KT 5720; KT 5823; MATRIGEL; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RAPAMYCIN; RHO KINASE; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL EXPANSION; COMPARATIVE STUDY; CONTROLLED STUDY; EMBRYONIC STEM CELL; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MESODERM; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

EID: 84866865798     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2012-04-421610     Document Type: Article

References (45)

1. Yamashita JK. ES and iPS cell research for cardiovascular regeneration. Exp Cell Res. 2010;316(16):2555-2559.
2. Nishikawa SI, Nishikawa S, Hirashima M, Matsuyoshi N, Kodama H. Progressive lineage analysis by cell sorting and culture identifies FLK1+VE-cadherin+ cells at a diverging point of endothelial and hemopoietic lineages. Development. 1998;125(9):1747-1757. (Pubitemid 28256742)
3. Hirashima M, Kataoka H, Nishikawa S, Matsuyoshi N, Nishikawa S. Maturation of embryonic stem cells into endothelial cells in an in vitro model of vasculogenesis. Blood. 1999;93(4):1253-1263. (Pubitemid 29076140)
4. Yamashita J, Itoh H, Hirashima M, et al. Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors. Nature. 2000;408(6808):92-96.
5. Yamashita JK. Differentiation of arterial, venous, and lymphatic endothelial cells from vascular progenitors. Trends Cardiovasc Med. 2007;17(2):59-63. (Pubitemid 46205329)
6. Narazaki G, Uosaki H, Teranishi M, et al. Directed and systematic differentiation of cardiovascular cells from mouse induced pluripotent stem cells. Circulation. 2008;118(5):498-506.
7. Yurugi-Kobayashi T, Itoh H, Schroeder T, et al. Adrenomedullin/cyclic AMP pathway induces Notch activation and differentiation of arterial endothelial cells from vascular progenitors. Arterioscler Thromb Vasc Biol. 2006;26(9):1977-1984. (Pubitemid 44253777)
8. Yamamizu K, Kawasaki K, Katayama S, Watabe T, Yamashita JK. Enhancement of vascular progenitor potential by protein kinase A through dual induction of Flk-1 and Neuropilin-1. Blood. 2009;114(17):3707-3716.
9. Yamamizu K, Furuta S, Katayama S, et al. The kappa opioid system regulates endothelial cell differentiation and pathfinding in vascular development. Blood. 2011;118(3):775-785.
10. Kawasaki K, Watabe T, Sase H, et al. Ras signaling directs endothelial specification of VEGFR2+ vascular progenitor cells. J Cell Biol. 2008;181(1):131-141. (Pubitemid 351519770)
11. Bekhite MM, Finkensieper A, Binas S, et al. VEGF-mediated PI3K class IA and PKC signaling in cardiomyogenesis and vasculogenesis of mouse embryonic stem cells. J Cell Sci. 2011;124(11):1819-1830.
12. Joo HJ, Kim H, Park SW, et al. Angiopoietin-1 promotes endothelial differentiation from embryonic stem cells and induced pluripotent stem cells. Blood. 2011;118(8):2094-2104.
13. Watabe T, Nishihara A, Mishima K, et al. TGF-beta receptor kinase inhibitor enhances growth and integrity of embryonic stem cell-derived endothelial cells. J Cell Biol. 2003;163(6):1303-1311. (Pubitemid 38032091)
14. James D, Nam HS, Seandel M, et al. Expansion and maintenance of human embryonic stem cell-derived endothelial cells by TGFbeta inhibition is Id1 dependent. Nat Biotechnol. 2010;28(2):161-166.
15. Noghero A, Bussolino F, Gualandris A. Role of the microenvironment in the specification of endothelial progenitors derived from embryonic stem cells. Microvasc Res. 2010;79(3):178-183.
16. Wang ZZ, Au P, Chen T, et al. Endothelial cells derived from human embryonic stem cells form durable blood vessels in vivo. Nat Biotechnol. 2007;25(3):317-318. (Pubitemid 46398769)
17. Coultas L, Chawengsaksophak K, Rossant J. Endothelial cells and VEGF in vascular development. Nature. 2005;438(7070):937-945. (Pubitemid 43093959)
18. Lohela M, Bry M, Tammela T, Alitalo K. VEGFs and receptors involved in angiogenesis versus lymphangiogenesis. Curr Opin Cell Biol. 2009;21(2):154-165.
19. Riento K, Ridley AJ. Rocks: multifunctional kinases in cell behaviour. Nat Rev Mol Cell Biol. 2003;4(6):446-456. (Pubitemid 36648590)
20. McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell. 2004;6(4):483-495. (Pubitemid 38456178)
21. Jaffe AB, Hall A. Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol. 2005;21:247-269. (Pubitemid 41740635)
22. Zhao ZS, Manser E. PAK and other Rho-associated kinases-effectors with surprisingly diverse mechanisms of regulation. Biochem J. 2005;386(2):201-214. (Pubitemid 40343777)
23. Charrasse S, Comunale F, Fortier M, Portales-Casamar E, Debant A, Gauthier-Rouviere C. M-cadherin activates Rac1 GTPase through the Rho-GEF trio during myoblast fusion. Mol Biol Cell. 2007;18(5):1734-1743. (Pubitemid 46717555)
24. Castellani L, Salvati E, Alema S, Falcone G. Fine regulation of RhoA and Rock is required for skeletal muscle differentiation. J Biol Chem. 2006;281(22):15249-15257. (Pubitemid 43855114)
25. Pagiatakis C, Gordon JW, Ehyai S, McDermott JC. A novel RhoA/ROCK-CPI-17-MEF2C signaling pathway regulates vascular smooth muscle cell gene expression. J Biol Chem. 2012;287(11):8361-8370.
26. Watanabe K, Ueno M, Kamiya D, et al. A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat Biotechnol. 2007;25(6):681-686. (Pubitemid 46897207)
27. Ohgushi M, Matsumura M, Eiraku M, et al. Molecular pathway and cell state responsible for dissociation-induced apoptosis in human pluripotent stem cells. Cell Stem Cell. 2010;7(2):225-239.
28. Chen G, Hou Z, Gulbranson DR, Thomson JA. Actin-myosin contractility is responsible for the reduced viability of dissociated human embryonic stem cells. Cell Stem Cell. 2010;7(2):240-248.
29. Cho HJ, Lee CS, Kwon YW, et al. Induction of pluripotent stem cells from adult somatic cells by protein-based reprogramming without genetic manipulation. Blood. 2010;116(3):386-395.
30. Koh YJ, Kim HZ, Hwang SI, et al. Double antiangiogenic protein, DAAP, targeting VEGF-A and angiopoietins in tumor angiogenesis, metastasis, and vascular leakage. Cancer Cell. 2010;18(2):171-184.
31. Jeong GS, Han S, Shin Y, et al. Sprouting angiogenesis under a chemical gradient regulated by interactions with an endothelial monolayer in a microfluidic platform. Anal Chem. 2011;83(22):8454-8459.
32. Chung S, Sudo R, Mack PJ, Wan CR, Vickerman V, Kamm RD. Cell migration into scaffolds under co-culture conditions in a microfluidic platform. Lab Chip. 2009;9(2):269-275.
33. Li Z, Dong X, Wang Z, et al. Regulation of PTEN by Rho small GTPases. Nat Cell Biol. 2005;7(4):399-404. (Pubitemid 40533130)
34. Fehrenbach ML, Cao G, Williams JT, Finklestein JM, Delisser HM. Isolation of murine lung endothelial cells. Am J Physiol Lung Cell Mol Physiol. 2009;296(6):L1096-L1103.
35. Koh YJ, Koh BI, Kim H, et al. Stromal vascular fraction from adipose tissue forms profound vascular network through the dynamic reassembly of blood endothelial cells. Arterioscler Thromb Vasc Biol. 2011;31(5):1141-1150.
36. Losordo DW, Dimmeler S. Therapeutic angiogenesis and vasculogenesis for ischemic disease: II. Cell-based therapies. Circulation. 2004;109(22):2692-2697. (Pubitemid 38737912)
37. Dimmeler S, Zeiher AM. Endothelial cell apoptosis in angiogenesis and vessel regression. Circ Res. 2000;87(6):434-439.
38. Kim I, Ryu YS, Kwak HJ, et al. EphB ligand, ephrinB2, suppresses the VEGF- and angiopoietin 1-induced Ras/mitogen-activated protein kinase pathway in venous endothelial cells. FASEB J. 2002;16(9):1126-1128.
39. Aitsebaomo J, Portbury AL, Schisler JC, Patterson C. Brothers and sisters: molecular insights into arterial-venous heterogeneity. Circ Res. 2008;103(9):929-939.
40. Atkins GB, Jain MK, Hamik A. Endothelial differentiation: molecular mechanisms of specification and heterogeneity. Arterioscler Thromb Vasc Biol. 2011;31(7):1476-1484.
41. Kroll J, Epting D, Kern K, et al. Inhibition of Rho-dependent kinases ROCK I/II activates VEGF-driven retinal neovascularization and sprouting angiogenesis. Am J Physiol Heart Circ Physiol. 2009;296(3):H893-H899.
42. Hoang MV, Whelan MC, Senger DR. Rho activity critically and selectively regulates endothelial cell organization during angiogenesis. Proc Natl Acad Sci U S A. 2004;101(7):1874-1879. (Pubitemid 38228984)
43. Bryan BA, Dennstedt E, Mitchell DC, et al. RhoA/ROCK signaling is essential for multiple aspects of VEGF-mediated angiogenesis. FASEB J. 2010;24(9):3186-3195.
44. van Nieuw Amerongen GP, Koolwijk P, Versteilen A, van Hinsbergh VW. Involvement of RhoA/Rho kinase signaling in VEGF-induced endothelial cell migration and angiogenesis in vitro. Arterioscler Thromb Vasc Biol. 2003;23(2):211-217. (Pubitemid 36231930)
45. McCloskey KE, Smith DA, Jo H, Nerem RM. Embryonic stem cell-derived endothelial cells may lack complete functional maturation in vitro. J Vasc Res. 2006;43(5):411-421.