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PMID: 17070513 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Periostin promotes atrioventricular mesenchyme matrix invasion and remodeling mediated by integrin signaling through Rho/PI 3-kinase.

Developmental biology ·Vol. 302 ·No. 1 ·2007-02-01 ·Pages 256-66

Butcher JT, Norris RA, Hoffman S, Mjaatvedt CH, Markwald RR

Abstract

Recent evidence suggests that extracellular matrix components may play a signaling role in embryonic valve development. We have previously identified the spatiotemporal expression patterns of periostin in developing valves, but its function during this process is largely unknown. To evaluate the functional role periostin plays during valvulogenesis, two separate three-dimensional culture assay systems, which model chick atrioventricular cushion development, were employed. These assays demonstrated that cushion mesenchymal cells adhered and spread on purified periostin in a dose-responsive manner, similar to collagen I and fibronectin via alpha(v)beta(3) and beta(1) integrin pairs. Periostin overexpression resulted in enhanced mesenchyme invasion through 3D collagen gels and increased matrix compaction. This invasion was dependent on alpha(v)beta(3) more than beta(1) integrin signaling, and was mediated differentially by Rho kinase and PI 3-kinase. Both matrix invasion and compaction were associated with a colocalization of periostin and beta(1) integrin expression to migratory cell phenotype in both surface and deep cells. The Rho/PI 3-kinase pathway also differentially mediated matrix compaction. Both Rho and PI 3-kinase were involved in normal cushion mesenchyme matrix compaction, but only PI 3-kinase was required for the enhanced matrix compaction due to periostin. Taken together, these results highlight periostin as a mediator of matrix remodeling by cushion mesenchyme towards a mature valve structure.

MeSH Terms
Adenoviridae/genetics Animals Cell Adhesion Cell Adhesion Molecules/genetics,metabolism,physiology Cell Line Chick Embryo Collagen/metabolism Extracellular Matrix/metabolism Heart Valves/embryology Humans In Vitro Techniques Integrins/metabolism Intracellular Signaling Peptides and Proteins/metabolism Mesoderm/cytology,metabolism Mice Phosphatidylinositol 3-Kinases/metabolism Protein Serine-Threonine Kinases/metabolism rho-Associated Kinases
Chemicals
Cell Adhesion Molecules Integrins Intracellular Signaling Peptides and Proteins Postn protein, mouse Collagen Protein Serine-Threonine Kinases rho-Associated Kinases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Butcher Jonathan T
Cardiovascular Developmental Biology Center, Chair of Cell Biology and Anatomy, Medical University of South Carolina, Charleston, SC 29425, USA.
Norris Russell A
Hoffman Stanley
Mjaatvedt Corey H
Markwald Roger R
References (57)
57 references, click to expand
  1. Identification and characterization of a novel protein, periostin, with restricted expression to periosteum and periodontal ligament and increased expression by transforming growth factor beta.
    J Bone Miner Res. 1999 Jul;14(7):1239-49 PMID: 10404027
  2. Acquired expression of periostin by human breast cancers promotes tumor angiogenesis through up-regulation of vascular endothelial growth factor receptor 2 expression.
    Mol Cell Biol. 2004 May;24(9):3992-4003 PMID: 15082792
  3. Vascular injury induces expression of periostin: implications for vascular cell differentiation and migration.
    Arterioscler Thromb Vasc Biol. 2005 Jan;25(1):77-83 PMID: 15514205
  4. Cell biology of cardiac cushion development.
    Int Rev Cytol. 2005;243:287-335 PMID: 15797462
  5. Immunolocalization of chick periostin protein in the developing heart.
    Anat Rec A Discov Mol Cell Evol Biol. 2005 May;284(1):415-23 PMID: 15803479
  6. Comparison of the four mouse fasciclin-containing genes expression patterns during valvuloseptal morphogenesis.
    Gene Expr Patterns. 2005 Jun;5(5):593-600 PMID: 15907457
  7. periostin null mice exhibit dwarfism, incisor enamel defects, and an early-onset periodontal disease-like phenotype.
    Mol Cell Biol. 2005 Dec;25(24):11131-44 PMID: 16314533
  8. Periostin family of proteins: therapeutic targets for heart disease.
    Anat Rec A Discov Mol Cell Evol Biol. 2005 Dec;287(2):1205-12 PMID: 16240445
  9. Vascular endothelial growth factor receptor signaling is required for cardiac valve formation in zebrafish.
    Dev Dyn. 2006 Jan;235(1):29-37 PMID: 16170785
  10. Periostin is an extracellular matrix protein required for eruption of incisors in mice.
    Biochem Biophys Res Commun. 2006 Apr 14;342(3):766-72 PMID: 16497272
  11. BMP and FGF regulatory pathways control cell lineage diversification of heart valve precursor cells.
    Dev Biol. 2006 Apr 15;292(2):292-302 PMID: 16680829
  12. Hearts and bones: shared regulatory mechanisms in heart valve, cartilage, tendon, and bone development.
    Dev Biol. 2006 Jun 15;294(2):292-302 PMID: 16643886
  13. Transduction of a mesenchyme-specific gene periostin into 293T cells induces cell invasive activity through epithelial-mesenchymal transformation.
    J Biol Chem. 2006 Jul 14;281(28):19700-8 PMID: 16702213
  14. Phosphatidylinositol-3-kinase signaling mediates vascular smooth muscle cell expression of periostin in vivo and in vitro.
    Atherosclerosis. 2006 Oct;188(2):292-300 PMID: 16325820
  15. Permissive effect of fibronectin on collagen gel contraction mediated by bovine trabecular meshwork cells.
    Invest Ophthalmol Vis Sci. 2003 Oct;44(10):4331-6 PMID: 14507877
  16. Vitronectin or fibronectin is required for corneal fibroblast-seeded collagen gel contraction.
    Invest Ophthalmol Vis Sci. 2000 Jan;41(1):103-9 PMID: 10634608
  17. Motility and invasion are differentially modulated by Rho family GTPases.
    Oncogene. 2000 Jan 27;19(4):580-91 PMID: 10698528
  18. Disruption of hyaluronan synthase-2 abrogates normal cardiac morphogenesis and hyaluronan-mediated transformation of epithelium to mesenchyme.
    J Clin Invest. 2000 Aug;106(3):349-60 PMID: 10930438
  19. Periostin (an osteoblast-specific factor) is expressed within the embryonic mouse heart during valve formation.
    Mech Dev. 2001 May;103(1-2):183-8 PMID: 11335131
  20. Effects of pdgf-bb on rat dermal fibroblast behavior in mechanically stressed and unstressed collagen and fibrin gels.
    Exp Cell Res. 2001 May 15;266(1):155-66 PMID: 11339834
  21. UDP-glucose dehydrogenase required for cardiac valve formation in zebrafish.
    Science. 2001 Aug 31;293(5535):1670-3 PMID: 11533493
  22. Regulation of human lung fibroblast phenotype and function by vitronectin and vitronectin integrins.
    J Cell Sci. 2001 Oct;114(Pt 19):3507-16 PMID: 11682610
  23. Transforming growth factor beta stimulates fibroblast-collagen matrix contraction by different mechanisms in mechanically loaded and unloaded matrices.
    Exp Cell Res. 2002 Feb 15;273(2):248-55 PMID: 11822880
  24. Bone morphogenetic protein-2 can mediate myocardial regulation of atrioventricular cushion mesenchymal cell formation in mice.
    Dev Biol. 2004 May 15;269(2):505-18 PMID: 15110716
  25. Exposure of cardiac fibroblasts to the herbicide nitrofen causes altered interactions with the extracellular matrix.
    Cell Biol Toxicol. 2004 Feb;20(1):15-24 PMID: 15119844
  26. Development of heart valve leaflets and supporting apparatus in chicken and mouse embryos.
    Dev Dyn. 2004 Jun;230(2):239-50 PMID: 15162503
  27. Expression and function of periostin-isoforms in bone.
    J Cell Biochem. 2004 Aug 1;92(5):1044-61 PMID: 15258926
  28. Unique morphology and focal adhesion development of valvular endothelial cells in static and fluid flow environments.
    Arterioscler Thromb Vasc Biol. 2004 Aug;24(8):1429-34 PMID: 15117733
  29. A field of myocardial-endocardial NFAT signaling underlies heart valve morphogenesis.
    Cell. 2004 Sep 3;118(5):649-63 PMID: 15339668
  30. Lineage and morphogenetic analysis of the cardiac valves.
    Circ Res. 2004 Sep 17;95(6):645-54 PMID: 15297379
  31. Periostin as a novel factor responsible for ventricular dilation.
    Circulation. 2004 Sep 28;110(13):1806-13 PMID: 15381649
  32. Glycosaminoglycan synthesis by the early embryonic chick heart.
    Dev Biol. 1973 Dec;35(2):332-48 PMID: 4274694
  33. Protein extracts from early embryonic hearts initiate cardiac endothelial cytodifferentiation.
    Dev Biol. 1985 Dec;112(2):414-26 PMID: 3935503
  34. Conditioning of native substrates by chondroitin sulfate proteoglycans during cardiac mesenchymal cell migration.
    J Cell Biol. 1986 Dec;103(6 Pt 1):2475-87 PMID: 3782305
  35. Histochemical and ultrastructural changes in the extracellular matrix of the developing chick semilunar heart valves.
    Acta Anat (Basel). 1991;142(1):87-96 PMID: 1781247
  36. A series of normal stages in the development of the chick embryo. 1951.
    Dev Dyn. 1992 Dec;195(4):231-72 PMID: 1304821
  37. Hyaluronate degradation affects ventricular function of the early postlooped embryonic rat heart in situ.
    Circ Res. 1994 Feb;74(2):244-52 PMID: 8293563
  38. Elastic extracellular matrix of the embryonic chick heart: an immunohistological study using laser confocal microscopy.
    Dev Dyn. 1994 Aug;200(4):321-32 PMID: 7994079
  39. TGFbeta2 knockout mice have multiple developmental defects that are non-overlapping with other TGFbeta knockout phenotypes.
    Development. 1997 Jul;124(13):2659-70 PMID: 9217007
  40. Development of the papillary muscles of the mitral valve: morphogenetic background of parachute-like asymmetric mitral valves and other mitral valve anomalies.
    J Thorac Cardiovasc Surg. 1998 Jul;116(1):36-46 PMID: 9671895
  41. The Cspg2 gene, disrupted in the hdf mutant, is required for right cardiac chamber and endocardial cushion formation.
    Dev Biol. 1998 Oct 1;202(1):56-66 PMID: 9758703
  42. Development of the atrioventricular valve tension apparatus in the human heart.
    Anat Embryol (Berl). 1998 Oct;198(4):317-29 PMID: 9764545
  43. Bone morphogenetic protein-2 acts synergistically with transforming growth factor-beta3 during endothelial-mesenchymal transformation in the developing chick heart.
    J Cell Physiol. 1999 Jul;180(1):35-45 PMID: 10362015
  44. Heart-valve mesenchyme formation is dependent on hyaluronan-augmented activation of ErbB2-ErbB3 receptors.
    Nat Med. 2002 Aug;8(8):850-5 PMID: 12134143
  45. Matricellular proteins: extracellular modulators of cell function.
    Curr Opin Cell Biol. 2002 Oct;14(5):608-16 PMID: 12231357
  46. Periostin secreted by epithelial ovarian carcinoma is a ligand for alpha(V)beta(3) and alpha(V)beta(5) integrins and promotes cell motility.
    Cancer Res. 2002 Sep 15;62(18):5358-64 PMID: 12235007
  47. Identification of motifs in the fasciclin domains of the transforming growth factor-beta-induced matrix protein betaig-h3 that interact with the alphavbeta5 integrin.
    J Biol Chem. 2002 Nov 29;277(48):46159-65 PMID: 12270930
  48. VEGF modulates early heart valve formation.
    Anat Rec A Discov Mol Cell Evol Biol. 2003 Mar;271(1):202-8 PMID: 12552636
  49. Fibroblast biology in three-dimensional collagen matrices.
    Trends Cell Biol. 2003 May;13(5):264-9 PMID: 12742170
  50. Defective valvulogenesis in HB-EGF and TACE-null mice is associated with aberrant BMP signaling.
    EMBO J. 2003 Jun 2;22(11):2704-16 PMID: 12773386
  51. Identification of the alphavbeta3 integrin-interacting motif of betaig-h3 and its anti-angiogenic effect.
    J Biol Chem. 2003 Jul 11;278(28):25902-9 PMID: 12704192
  52. Form and function of developing heart valves: coordination by extracellular matrix and growth factor signaling.
    J Mol Med (Berl). 2003 Jul;81(7):392-403 PMID: 12827270
  53. Signal transduction in matrix contraction and the migration of vascular smooth muscle cells in three-dimensional matrix.
    J Vasc Res. 2003 Jul-Aug;40(4):378-88 PMID: 12891007
  54. Insulin-like growth factor I induces migration and invasion of human multiple myeloma cells.
    Blood. 2004 Jan 1;103(1):301-8 PMID: 14504085
  55. Periostin is expressed within the developing teeth at the sites of epithelial-mesenchymal interaction.
    Dev Dyn. 2004 Apr;229(4):857-68 PMID: 15042709
  56. Conformational resemblance between the structures of integrin-activating pentapetides derived from betaig-h3 and RGD peptide analogues in a membrane environment.
    Peptides. 2004 Feb;25(2):199-205 PMID: 15063001
  57. Identification and detection of the periostin gene in cardiac development.
    Anat Rec A Discov Mol Cell Evol Biol. 2004 Dec;281(2):1227-33 PMID: 15532025
Article Info
Journal
Developmental biology
Abbr.
Dev Biol
ISSN
0012-1606
DOI
10.1016/j.ydbio.2006.09.048
Published
2007-02-01
Epub
2006-00-04
Pages
256-66
Language
English
Region
United States
NLM ID
0372762
PMCID
PMC1913192
Subset
IM
Grants
NHLBI NIH HHS · HL52813 · United States
NHLBI NIH HHS · R01 HL066231 · United States
NHLBI NIH HHS · P01 HL052813 · United States
NHLBI NIH HHS · R01 HL033756 · United States
NHLBI NIH HHS · T32 HL007710 · United States
NHLBI NIH HHS · HL133756 · United States
NHLBI NIH HHS · HL66231 · United States
External Links
PubMed source DOI: 10.1016/j.ydbio.2006.09.048 PMC Full Text View journal details
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