Home LiteratureArticle Details
PMID: 16973908 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Human pulmonary valve progenitor cells exhibit endothelial/mesenchymal plasticity in response to vascular endothelial growth factor-A and transforming growth factor-beta2.

Circulation research ·Vol. 99 ·No. 8 ·2006-10-13 ·Pages 861-9

Paruchuri S, Yang JH, Aikawa E, Melero-Martin JM, Khan ZA, Loukogeorgakis S, Schoen FJ, Bischoff J

Abstract

In situ analysis of fetal semilunar valve leaflets has revealed cells coexpressing endothelial and mesenchymal markers along the endothelium, with diminished frequency seen in adult valves. To determine whether such cells are progenitor cells, we isolated clonal populations from human pulmonary valves. The clones expressed endothelial markers but showed potential to further differentiate into endothelium in response to vascular endothelial growth factor (VEGF)-A. When exposed to transforming growth factor (TGF)-beta2, individual clones adopted a mesenchymal phenotype to varying degrees and expressed markers of endothelial to mesenchymal transformation (EMT). Both VEGF- and TGFbeta2-induced phenotypic changes were partially reversible, indicating the plasticity of these cells. When challenged with VEGF or TGFbeta2, a hierarchy of endothelial/mesenchymal potential could be seen among the clonal populations: cells initially closer to an endothelial phenotype showed a strong response to TGFbeta2 that could be inhibited by VEGF, whereas cells closer to a mesenchymal phenotype responded to TGFbeta2 but were resistant to endothelial-inducing effects of VEGF. These findings suggest the presence of bipotential valve progenitor cells with ability to differentiate into either endothelial or interstitial cells of the valve leaflet. Understanding the differentiation potential and function of these cells may be important for understanding heart valve disease and may also be applied to current paradigms for creating tissue-engineered heart valves.

MeSH Terms
Biomarkers/metabolism Cell Differentiation/drug effects Cell Separation Clone Cells/cytology,physiology Endothelial Cells/cytology,drug effects,metabolism,physiology Female Fetus Heart Valves/embryology Humans Mesoderm/cytology,physiology Middle Aged Muscle, Smooth, Vascular/metabolism Phenotype Pulmonary Valve/cytology Stem Cells/cytology Transcription, Genetic/drug effects Transforming Growth Factor beta/pharmacology Transforming Growth Factor beta2 Up-Regulation Vascular Endothelial Growth Factor A/pharmacology
Chemicals
Biomarkers TGFB2 protein, human Transforming Growth Factor beta Transforming Growth Factor beta2 Vascular Endothelial Growth Factor A
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Paruchuri Sailaja
Department of Surgery, Children's Hospital Boston, 300 Longwood Ave, Boston, MA 02115, USA.
Yang Jeong-Hee
Aikawa Elena
Melero-Martin Juan M
Khan Zia A
Loukogeorgakis Stavros
Schoen Frederick J
Bischoff Joyce
References (32)
32 references, click to expand
  1. Mechanisms involved in valvuloseptal endocardial cushion formation in early cardiogenesis: roles of transforming growth factor (TGF)-beta and bone morphogenetic protein (BMP).
    Anat Rec. 2000 Feb 1;258(2):119-27 PMID: 10645959
  2. Heart valve regeneration.
    Adv Biochem Eng Biotechnol. 2005;94:141-79 PMID: 15915872
  3. Slug is an essential target of TGFbeta2 signaling in the developing chicken heart.
    Dev Biol. 2000 Jul 1;223(1):91-102 PMID: 10864463
  4. Embryonic development is disrupted by modest increases in vascular endothelial growth factor gene expression.
    Development. 2000 Sep;127(18):3941-6 PMID: 10952892
  5. Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors.
    Nature. 2000 Nov 2;408(6808):92-6 PMID: 11081514
  6. Clonality and altered behavior of endothelial cells from hemangiomas.
    J Clin Invest. 2001 Mar;107(6):745-52 PMID: 11254674
  7. A novel role for VEGF in endocardial cushion formation and its potential contribution to congenital heart defects.
    Development. 2001 May;128(9):1531-8 PMID: 11290292
  8. Aortic valve endothelial cells undergo transforming growth factor-beta-mediated and non-transforming growth factor-beta-mediated transdifferentiation in vitro.
    Am J Pathol. 2001 Oct;159(4):1335-43 PMID: 11583961
  9. Mature vascular endothelium can give rise to smooth muscle cells via endothelial-mesenchymal transdifferentiation: in vitro analysis.
    Circ Res. 2002 Jun 14;90(11):1189-96 PMID: 12065322
  10. Temporal and distinct TGFbeta ligand requirements during mouse and avian endocardial cushion morphogenesis.
    Dev Biol. 2002 Aug 1;248(1):170-81 PMID: 12142029
  11. Nf1 has an essential role in endothelial cells.
    Nat Genet. 2003 Jan;33(1):75-9 PMID: 12469121
  12. Human umbilical vein endothelium-derived cells retain potential to differentiate into smooth muscle-like cells.
    J Biol Chem. 2003 Jan 10;278(2):1303-9 PMID: 12417591
  13. NFATc1 mediates vascular endothelial growth factor-induced proliferation of human pulmonary valve endothelial cells.
    J Biol Chem. 2003 Jan 17;278(3):1686-92 PMID: 12427739
  14. A field of myocardial-endocardial NFAT signaling underlies heart valve morphogenesis.
    Cell. 2004 Sep 3;118(5):649-63 PMID: 15339668
  15. Bone marrow-derived myofibroblasts are present in adult human heart valves.
    J Heart Valve Dis. 2005 Sep;14(5):674-8 PMID: 16245507
  16. CD117-positive cells and mast cells in adult human cardiac valves--observations and implications for the creation of bioengineered grafts.
    Cardiovasc Pathol. 2006 Jan-Feb;15(1):36-40 PMID: 16414455
  17. Isolation of "side population" progenitor cells from healthy arteries of adult mice.
    Arterioscler Thromb Vasc Biol. 2006 Feb;26(2):281-6 PMID: 16306431
  18. Human semilunar cardiac valve remodeling by activated cells from fetus to adult: implications for postnatal adaptation, pathology, and tissue engineering.
    Circulation. 2006 Mar 14;113(10):1344-52 PMID: 16534030
  19. An in vivo analysis of hematopoietic stem cell potential: hematopoietic origin of cardiac valve interstitial cells.
    Circ Res. 2006 Mar 17;98(5):690-6 PMID: 16456103
  20. Endothelial progenitor cells from infantile hemangioma and umbilical cord blood display unique cellular responses to endostatin.
    Blood. 2006 Aug 1;108(3):915-21 PMID: 16861344
  21. A null mutation of Hhex results in abnormal cardiac development, defective vasculogenesis and elevated Vegfa levels.
    Development. 2004 Oct;131(20):5197-209 PMID: 15459110
  22. Structural development of endocardial cushions.
    Am J Anat. 1977 Jan;148(1):85-119 PMID: 842477
  23. Migratory behavior of cardiac cushion tissue cells in a collagen-lattice culture system.
    Dev Biol. 1982 Jun;91(2):235-45 PMID: 7095266
  24. Transforming growth factor beta 1 promotes the differentiation of endothelial cells into smooth muscle-like cells in vitro.
    J Cell Sci. 1992 Oct;103 ( Pt 2):521-9 PMID: 1478952
  25. Extracellular fibrillar structure of latent TGF beta binding protein-1: role in TGF beta-dependent endothelial-mesenchymal transformation during endocardial cushion tissue formation in mouse embryonic heart.
    J Cell Biol. 1997 Jan 13;136(1):193-204 PMID: 9008713
  26. Embryonic endothelial cells transdifferentiate into mesenchymal cells expressing smooth muscle actins in vivo and in vitro.
    Circ Res. 1997 Apr;80(4):444-51 PMID: 9118474
  27. Expression of smooth muscle alpha-actin in mesenchymal cells during formation of avian endocardial cushion tissue: a role for transforming growth factor beta3.
    Dev Dyn. 1997 Jul;209(3):296-309 PMID: 9215644
  28. An autocrine function for transforming growth factor beta 3 in the atrioventricular endocardial cushion tissue formation during chick heart development.
    Ann N Y Acad Sci. 1998 Oct 23;857:272-5 PMID: 9917855
  29. Slug is a mediator of epithelial-mesenchymal cell transformation in the developing chicken heart.
    Dev Biol. 1999 Aug 1;212(1):243-54 PMID: 10419699
  30. Multiple developmental roles of VEGF suggested by a LacZ-tagged allele.
    Dev Biol. 1999 Aug 15;212(2):307-22 PMID: 10433823
  31. Cell biology of cardiac cushion development.
    Int Rev Cytol. 2005;243:287-335 PMID: 15797462
  32. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression.
    Nat Cell Biol. 2000 Feb;2(2):76-83 PMID: 10655586
Article Info
Journal
Circulation research
Abbr.
Circ Res
ISSN
1524-4571
Published
2006-10-13
Epub
2006-00-14
Pages
861-9
Language
English
Region
United States
NLM ID
0047103
PMCID
PMC2810464
Subset
IM
Grants
NHLBI NIH HHS · R01 HL060490 · United States
NHLBI NIH HHS · R01 HL060490-10 · United States
NHLBI NIH HHS · R01 HL 06490 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com