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PMID: 17911384 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

ALK5- and TGFBR2-independent role of ALK1 in the pathogenesis of hereditary hemorrhagic telangiectasia type 2.

Blood ·Vol. 111 ·No. 2 ·2008-01-15 ·Pages 633-42

Park SO, Lee YJ, Seki T, Hong KH, Fliess N, Jiang Z, Park A, Wu X, Kaartinen V, Roman BL, Oh SP

Abstract

ALK1 belongs to the type I receptor family for transforming growth factor-beta family ligands. Heterozygous ALK1 mutations cause hereditary hemorrhagic telangiectasia type 2 (HHT2), a multisystemic vascular disorder. Based largely on in vitro studies, TGF-beta1 has been considered as the most likely ALK1 ligand related to HHT, yet the identity of the physiologic ALK1 ligand remains controversial. In cultured endothelial cells, ALK1 and another TGF-beta type I receptor, ALK5, regulate angiogenesis by controlling TGF-beta signal transduction, and ALK5 is required for ALK1 signaling. However, the extent to which such interactions between these 2 receptors play a role in pathogenesis of HHT is unknown. We directly addressed these issues in vivo by comparing the phenotypes of mice in which the Alk1, Alk5, or Tgfbr2 gene was conditionally deleted in restricted vascular endothelia using a novel endothelial Cre transgenic line. Alk1-conditional deletion resulted in severe vascular malformations mimicking all pathologic features of HHT. Yet Alk5- or Tgfbr2-conditional deletion in mice, or Alk5 inhibition in zebrafish, did not affect vessel morphogenesis. These data indicate that neither ALK5 nor TGFBR2 is required for ALK1 signaling pertinent to the pathogenesis of HHT and suggest that HHT might not be a TGF-beta subfamily disease.

MeSH Terms
Activin Receptors, Type I/genetics,metabolism Activin Receptors, Type II Animals Cell Line Endothelium, Vascular/metabolism,pathology Ligands Mice Mice, Knockout Neovascularization, Pathologic/genetics,metabolism,pathology Protein Serine-Threonine Kinases/genetics,metabolism Receptor, Transforming Growth Factor-beta Type I Receptor, Transforming Growth Factor-beta Type II Receptors, Transforming Growth Factor beta/genetics,metabolism Signal Transduction/genetics Telangiectasia, Hereditary Hemorrhagic/genetics,metabolism,pathology Transforming Growth Factor beta1/genetics,metabolism Zebrafish/genetics,metabolism Zebrafish Proteins
Chemicals
Ligands Receptors, Transforming Growth Factor beta Transforming Growth Factor beta1 Zebrafish Proteins Protein Serine-Threonine Kinases Activin Receptors, Type I Activin Receptors, Type II Acvrl1 protein, mouse Receptor, Transforming Growth Factor-beta Type I Receptor, Transforming Growth Factor-beta Type II Tgfbr1 protein, mouse
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Park Sung O
Department of Physiology and Functional Genomics, University of Florida College of Medicine, Shands Cancer Center, Gainesville 32610, USA.
Lee Young Jae
Seki Tsugio
Hong Kwon-Ho
Fliess Naime
Jiang Zhigang
Park Alice
Wu Xiaofang
Kaartinen Vesa
Roman Beth L
Oh S Paul
References (54)
54 references, click to expand
  1. Conditional inactivation of the TGF-beta type II receptor using Cre:Lox.
    Genesis. 2002 Feb;32(2):73-5 PMID: 11857781
  2. GS domain mutations that constitutively activate T beta R-I, the downstream signaling component in the TGF-beta receptor complex.
    EMBO J. 1995 May 15;14(10):2199-208 PMID: 7774578
  3. Analysis of ALK-1 and endoglin in newborns from families with hereditary hemorrhagic telangiectasia type 2.
    Hum Mol Genet. 2000 May 1;9(8):1227-37 PMID: 10767348
  4. VE-Cadherin-Cre-recombinase transgenic mouse: a tool for lineage analysis and gene deletion in endothelial cells.
    Dev Dyn. 2006 Mar;235(3):759-67 PMID: 16450386
  5. A combined syndrome of juvenile polyposis and hereditary haemorrhagic telangiectasia associated with mutations in MADH4 (SMAD4).
    Lancet. 2004 Mar 13;363(9412):852-9 PMID: 15031030
  6. Nonoverlapping expression patterns of ALK1 and ALK5 reveal distinct roles of each receptor in vascular development.
    Lab Invest. 2006 Feb;86(2):116-29 PMID: 16344855
  7. Endoglin expression is reduced in normal vessels but still detectable in arteriovenous malformations of patients with hereditary hemorrhagic telangiectasia type 1.
    Am J Pathol. 2000 Mar;156(3):911-23 PMID: 10702408
  8. The zebrafish gene map defines ancestral vertebrate chromosomes.
    Genome Res. 2005 Sep;15(9):1307-14 PMID: 16109975
  9. Evidence for novel fate of Flk1+ progenitor: contribution to muscle lineage.
    Genesis. 2003 Mar;35(3):153-9 PMID: 12640619
  10. Arterial endothelium-specific activin receptor-like kinase 1 expression suggests its role in arterialization and vascular remodeling.
    Circ Res. 2003 Oct 3;93(7):682-9 PMID: 12970115
  11. Endoglin null endothelial cells proliferate faster and are more responsive to transforming growth factor beta1 with higher affinity receptors and an activated Alk1 pathway.
    J Biol Chem. 2005 Jul 29;280(30):27800-8 PMID: 15923183
  12. Diagnostic criteria for hereditary hemorrhagic telangiectasia (Rendu-Osler-Weber syndrome).
    Am J Med Genet. 2000 Mar 6;91(1):66-7 PMID: 10751092
  13. Positive-negative selection gene targeting with the diphtheria toxin A-chain gene in mouse embryonic stem cells.
    Transgenic Res. 1993 Jul;2(4):183-90 PMID: 8364601
  14. Abnormal angiogenesis but intact hematopoietic potential in TGF-beta type I receptor-deficient mice.
    EMBO J. 2001 Apr 2;20(7):1663-73 PMID: 11285230
  15. Mouse model for hereditary hemorrhagic telangiectasia has a generalized vascular abnormality.
    Circulation. 2003 Apr 1;107(12):1653-7 PMID: 12668501
  16. p53 activation by knockdown technologies.
    PLoS Genet. 2007 May 25;3(5):e78 PMID: 17530925
  17. Defective paracrine signalling by TGFbeta in yolk sac vasculature of endoglin mutant mice: a paradigm for hereditary haemorrhagic telangiectasia.
    Development. 2004 Dec;131(24):6237-47 PMID: 15548578
  18. A murine model of hereditary hemorrhagic telangiectasia.
    J Clin Invest. 1999 Nov;104(10):1343-51 PMID: 10562296
  19. Endoglin, a TGF-beta binding protein of endothelial cells, is the gene for hereditary haemorrhagic telangiectasia type 1.
    Nat Genet. 1994 Dec;8(4):345-51 PMID: 7894484
  20. Tie2-Cre transgenic mice: a new model for endothelial cell-lineage analysis in vivo.
    Dev Biol. 2001 Feb 15;230(2):230-42 PMID: 11161575
  21. Essential functions of Alk3 during AV cushion morphogenesis in mouse embryonic hearts.
    Dev Biol. 2007 Jan 1;301(1):276-86 PMID: 16959237
  22. A mouse model for hereditary hemorrhagic telangiectasia (HHT) type 2.
    Hum Mol Genet. 2003 Mar 1;12(5):473-82 PMID: 12588795
  23. Genetic analysis of the mammalian transforming growth factor-beta superfamily.
    Endocr Rev. 2002 Dec;23(6):787-823 PMID: 12466190
  24. Molecular and functional analysis identifies ALK-1 as the predominant cause of pulmonary hypertension related to hereditary haemorrhagic telangiectasia.
    J Med Genet. 2003 Dec;40(12):865-71 PMID: 14684682
  25. Mutations in the activin receptor-like kinase 1 gene in hereditary haemorrhagic telangiectasia type 2.
    Nat Genet. 1996 Jun;13(2):189-95 PMID: 8640225
  26. Ultrastructure and three-dimensional organization of the telangiectases of hereditary hemorrhagic telangiectasia.
    J Invest Dermatol. 1990 Oct;95(4):422-7 PMID: 2212727
  27. Stages of embryonic development of the zebrafish.
    Dev Dyn. 1995 Jul;203(3):253-310 PMID: 8589427
  28. Balancing the activation state of the endothelium via two distinct TGF-beta type I receptors.
    EMBO J. 2002 Apr 2;21(7):1743-53 PMID: 11927558
  29. Identification of BMP9 and BMP10 as functional activators of the orphan activin receptor-like kinase 1 (ALK1) in endothelial cells.
    Blood. 2007 Mar 1;109(5):1953-61 PMID: 17068149
  30. Assignment of transforming growth factor beta1 and beta3 and a third new ligand to the type I receptor ALK-1.
    J Biol Chem. 1999 Apr 9;274(15):9984-92 PMID: 10187774
  31. Isolation of a regulatory region of activin receptor-like kinase 1 gene sufficient for arterial endothelium-specific expression.
    Circ Res. 2004 Apr 30;94(8):e72-7 PMID: 15059937
  32. Two-color whole-mount in situ hybridization to vertebrate and Drosophila embryos.
    Trends Genet. 1994 Aug;10(8):266 PMID: 7940754
  33. Radiation hybrid mapping of the zebrafish genome.
    Proc Natl Acad Sci U S A. 1999 Aug 17;96(17):9745-50 PMID: 10449765
  34. Dosage-dependent requirement of BMP type II receptor for maintenance of vascular integrity.
    Blood. 2007 Sep 1;110(5):1502-10 PMID: 17496203
  35. Activation and roles of ALK4/ALK7-mediated maternal TGFbeta signals in zebrafish embryo.
    Biochem Biophys Res Commun. 2006 Jun 30;345(2):694-703 PMID: 16696945
  36. Disruption of acvrl1 increases endothelial cell number in zebrafish cranial vessels.
    Development. 2002 Jun;129(12):3009-19 PMID: 12050147
  37. Clinical manifestations in a large hereditary hemorrhagic telangiectasia (HHT) type 2 kindred.
    Am J Med Genet. 2000 Aug 14;93(4):320-7 PMID: 10946360
  38. Hereditary haemorrhagic telangiectasia: current views on genetics and mechanisms of disease.
    J Med Genet. 2006 Feb;43(2):97-110 PMID: 15879500
  39. Arteriovenous malformations in mice lacking activin receptor-like kinase-1.
    Nat Genet. 2000 Nov;26(3):328-31 PMID: 11062473
  40. Smad1 recognition and activation by the ALK1 group of transforming growth factor-beta family receptors.
    J Biol Chem. 1999 Feb 5;274(6):3672-7 PMID: 9920917
  41. Generalized lacZ expression with the ROSA26 Cre reporter strain.
    Nat Genet. 1999 Jan;21(1):70-1 PMID: 9916792
  42. SB-431542 is a potent and specific inhibitor of transforming growth factor-beta superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7.
    Mol Pharmacol. 2002 Jul;62(1):65-74 PMID: 12065756
  43. Activin receptor-like kinase 1 is implicated in the maturation phase of angiogenesis.
    Blood. 2002 Dec 15;100(13):4495-501 PMID: 12453878
  44. Endoglin expression in early development is associated with vasculogenesis and angiogenesis.
    Mech Dev. 2002 Jan;110(1-2):193-6 PMID: 11744382
  45. Mesendoderm and left-right brain, heart and gut development are differentially regulated by pitx2 isoforms.
    Development. 2000 Mar;127(5):1081-93 PMID: 10662647
  46. Tie-1-directed expression of Cre recombinase in endothelial cells of embryoid bodies and transgenic mice.
    J Cell Sci. 2001 Feb;114(Pt 4):671-6 PMID: 11171372
  47. TGF-beta signal transduction.
    Annu Rev Biochem. 1998;67:753-91 PMID: 9759503
  48. Activin receptor-like kinase 1 modulates transforming growth factor-beta 1 signaling in the regulation of angiogenesis.
    Proc Natl Acad Sci U S A. 2000 Mar 14;97(6):2626-31 PMID: 10716993
  49. Activin receptor-like kinase (ALK)1 is an antagonistic mediator of lateral TGFbeta/ALK5 signaling.
    Mol Cell. 2003 Oct;12(4):817-28 PMID: 14580334
  50. BMP-9 signals via ALK1 and inhibits bFGF-induced endothelial cell proliferation and VEGF-stimulated angiogenesis.
    J Cell Sci. 2007 Mar 15;120(Pt 6):964-72 PMID: 17311849
  51. Bone morphogenetic protein receptor 1A signaling is dispensable for hematopoietic development but essential for vessel and atrioventricular endocardial cushion formation.
    Development. 2006 Sep;133(17):3473-84 PMID: 16887829
  52. Endoglin promotes endothelial cell proliferation and TGF-beta/ALK1 signal transduction.
    EMBO J. 2004 Oct 13;23(20):4018-28 PMID: 15385967
  53. Endoglin is an accessory protein that interacts with the signaling receptor complex of multiple members of the transforming growth factor-beta superfamily.
    J Biol Chem. 1999 Jan 8;274(2):584-94 PMID: 9872992
  54. Efficient in vivo manipulation of mouse genomic sequences at the zygote stage.
    Proc Natl Acad Sci U S A. 1996 Jun 11;93(12):5860-5 PMID: 8650183
Article Info
Journal
Blood
Abbr.
Blood
ISSN
0006-4971
Published
2008-01-15
Epub
2007-00-02
Pages
633-42
Language
English
Region
United States
NLM ID
7603509
PMCID
PMC2200847
Subset
IM
Grants
NHLBI NIH HHS · R01 HL064024 · United States
NHLBI NIH HHS · R01 HL079108 · United States
NHLBI NIH HHS · HL079108 · United States
NHLBI NIH HHS · HL64024 · United States
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