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PMID: 18086923 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Myofibroblast contraction activates latent TGF-beta1 from the extracellular matrix.

The Journal of cell biology ·Vol. 179 ·No. 6 ·2007-12-17 ·Pages 1311-23

Wipff PJ, Rifkin DB, Meister JJ, Hinz B

Abstract

The conjunctive presence of mechanical stress and active transforming growth factor beta1 (TGF-beta1) is essential to convert fibroblasts into contractile myofibroblasts, which cause tissue contractures in fibrotic diseases. Using cultured myofibroblasts and conditions that permit tension modulation on the extracellular matrix (ECM), we establish that myofibroblast contraction functions as a mechanism to directly activate TGF-beta1 from self-generated stores in the ECM. Contraction of myofibroblasts and myofibroblast cytoskeletons prepared with Triton X-100 releases active TGF-beta1 from the ECM. This process is inhibited either by antagonizing integrins or reducing ECM compliance and is independent from protease activity. Stretching myofibroblast-derived ECM in the presence of mechanically apposing stress fibers immediately activates latent TGF-beta1. In myofibroblast-populated wounds, activation of the downstream targets of TGF-beta1 signaling Smad2/3 is higher in stressed compared to relaxed tissues despite similar levels of total TGF-beta1 and its receptor. We propose activation of TGF-beta1 via integrin-mediated myofibroblast contraction as a potential checkpoint in the progression of fibrosis, restricting autocrine generation of myofibroblasts to a stiffened ECM.

MeSH Terms
Animals Cells, Cultured Cytoskeleton/physiology Extracellular Matrix/metabolism Fibroblasts/physiology,ultrastructure Integrins/physiology Muscle Contraction/physiology Myoblasts, Smooth Muscle/physiology,ultrastructure Phosphorylation Rats Smad2 Protein/metabolism Smad3 Protein/metabolism Stress, Mechanical Transforming Growth Factor beta1/metabolism Wound Healing/physiology
Chemicals
Integrins Smad2 Protein Smad2 protein, rat Smad3 Protein Smad3 protein, rat Transforming Growth Factor beta1
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Wipff Pierre-Jean
Laboratory of Cell Biophysics, Ecole Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland.
Rifkin Daniel B
Meister Jean-Jacques
Hinz Boris
References (55)
55 references, click to expand
  1. Interactions between growth factors and integrins: latent forms of transforming growth factor-beta are ligands for the integrin alphavbeta1.
    Mol Biol Cell. 1998 Sep;9(9):2627-38 PMID: 9725916
  2. Alpha-smooth muscle actin expression upregulates fibroblast contractile activity.
    Mol Biol Cell. 2001 Sep;12(9):2730-41 PMID: 11553712
  3. A role of the latent TGF-beta 1-binding protein in the assembly and secretion of TGF-beta 1.
    EMBO J. 1991 May;10(5):1091-101 PMID: 2022183
  4. The NH2-terminal peptide of alpha-smooth muscle actin inhibits force generation by the myofibroblast in vitro and in vivo.
    J Cell Biol. 2002 May 13;157(4):657-63 PMID: 11994316
  5. Alpha-smooth muscle actin is crucial for focal adhesion maturation in myofibroblasts.
    Mol Biol Cell. 2003 Jun;14(6):2508-19 PMID: 12808047
  6. Alpha8beta1 integrin is upregulated in myofibroblasts of fibrotic and scarring myocardium.
    J Mol Cell Cardiol. 2004 Mar;36(3):343-53 PMID: 15010273
  7. Mechanical tension controls granulation tissue contractile activity and myofibroblast differentiation.
    Am J Pathol. 2001 Sep;159(3):1009-20 PMID: 11549593
  8. An assay for transforming growth factor-beta using cells transfected with a plasminogen activator inhibitor-1 promoter-luciferase construct.
    Anal Biochem. 1994 Feb 1;216(2):276-84 PMID: 8179182
  9. The integrin alpha v beta 6 binds and activates latent TGF beta 1: a mechanism for regulating pulmonary inflammation and fibrosis.
    Cell. 1999 Feb 5;96(3):319-28 PMID: 10025398
  10. Focal adhesion size controls tension-dependent recruitment of alpha-smooth muscle actin to stress fibers.
    J Cell Biol. 2006 Jan 16;172(2):259-68 PMID: 16401722
  11. Transforming growth factor beta 1 and its latent form binding protein-1 associate with elastic fibres in human dermis: accumulation in actinic damage and absence in anetoderma.
    Br J Dermatol. 1997 Jul;137(1):51-8 PMID: 9274625
  12. Making sense of latent TGFbeta activation.
    J Cell Sci. 2003 Jan 15;116(Pt 2):217-24 PMID: 12482908
  13. Latent TGF-beta binding proteins: extracellular matrix association and roles in TGF-beta activation.
    Crit Rev Clin Lab Sci. 2004;41(3):233-64 PMID: 15307633
  14. Upregulation of TGF-beta1 expression may be necessary but is not sufficient for excessive scarring.
    J Invest Dermatol. 2006 May;126(5):1168-76 PMID: 16498396
  15. Ligation of protease-activated receptor 1 enhances alpha(v)beta6 integrin-dependent TGF-beta activation and promotes acute lung injury.
    J Clin Invest. 2006 Jun;116(6):1606-14 PMID: 16710477
  16. Mechanotransduction involving multimodular proteins: converting force into biochemical signals.
    Annu Rev Biophys Biomol Struct. 2006;35:459-88 PMID: 16689645
  17. Integrin-mediated transforming growth factor-beta activation regulates homeostasis of the pulmonary epithelial-mesenchymal trophic unit.
    Am J Pathol. 2006 Aug;169(2):405-15 PMID: 16877343
  18. The cutaneous microfibrillar apparatus contains latent transforming growth factor-beta binding protein-1 (LTBP-1) and is a repository for latent TGF-beta1.
    J Invest Dermatol. 1998 Oct;111(4):559-64 PMID: 9764833
  19. Contractile activity and smooth muscle alpha-actin organization in thrombin-induced human lung myofibroblasts.
    Am J Physiol Lung Cell Mol Physiol. 2003 Aug;285(2):L334-43 PMID: 12665468
  20. Mechanisms of pulmonary fibrosis.
    Annu Rev Med. 2004;55:395-417 PMID: 14746528
  21. Integrin alphaVbeta6-mediated activation of latent TGF-beta requires the latent TGF-beta binding protein-1.
    J Cell Biol. 2004 Jun 7;165(5):723-34 PMID: 15184403
  22. Substrate rigidity and force define form through tyrosine phosphatase and kinase pathways.
    Trends Cell Biol. 2006 Apr;16(4):213-23 PMID: 16529933
  23. Absence of integrin-mediated TGFbeta1 activation in vivo recapitulates the phenotype of TGFbeta1-null mice.
    J Cell Biol. 2007 Mar 12;176(6):787-93 PMID: 17353357
  24. Increased expression of integrin alphavbeta5 induces the myofibroblastic differentiation of dermal fibroblasts.
    Am J Pathol. 2006 Feb;168(2):499-510 PMID: 16436664
  25. Focal adhesion features during myofibroblastic differentiation are controlled by intracellular and extracellular factors.
    J Cell Sci. 2001 Sep;114(Pt 18):3285-96 PMID: 11591817
  26. The myofibroblast: one function, multiple origins.
    Am J Pathol. 2007 Jun;170(6):1807-16 PMID: 17525249
  27. The compliance of collagen gels regulates transforming growth factor-beta induction of alpha-smooth muscle actin in fibroblasts.
    Am J Pathol. 1999 Mar;154(3):871-82 PMID: 10079265
  28. Release of transforming growth factor-beta 1 from the pericellular matrix of cultured fibroblasts and fibrosarcoma cells by plasmin and thrombin.
    J Biol Chem. 1992 Dec 15;267(35):25378-84 PMID: 1281156
  29. Sequential deposition of latent TGF-beta binding proteins (LTBPs) during formation of the extracellular matrix in human lung fibroblasts.
    Exp Cell Res. 2005 Nov 1;310(2):370-82 PMID: 16157329
  30. Integrin alpha8beta1 mediates adhesion to LAP-TGFbeta1.
    J Cell Sci. 2002 Dec 1;115(Pt 23):4641-8 PMID: 12415008
  31. Active transforming growth factor-beta in wound repair: determination using a new assay.
    Am J Pathol. 1999 Jan;154(1):105-11 PMID: 9916924
  32. Rho-mediated contractility exposes a cryptic site in fibronectin and induces fibronectin matrix assembly.
    J Cell Biol. 1998 Apr 20;141(2):539-51 PMID: 9548730
  33. A monoclonal antibody against alpha-smooth muscle actin: a new probe for smooth muscle differentiation.
    J Cell Biol. 1986 Dec;103(6 Pt 2):2787-96 PMID: 3539945
  34. Stroma-derived three-dimensional matrices are necessary and sufficient to promote desmoplastic differentiation of normal fibroblasts.
    Am J Pathol. 2005 Aug;167(2):475-88 PMID: 16049333
  35. Expression of the integrin alpha8beta1 during pulmonary and hepatic fibrosis.
    Am J Pathol. 2000 Jun;156(6):1927-35 PMID: 10854216
  36. Formation and function of the myofibroblast during tissue repair.
    J Invest Dermatol. 2007 Mar;127(3):526-37 PMID: 17299435
  37. TGF-beta signalling from cell membrane to nucleus through SMAD proteins.
    Nature. 1997 Dec 4;390(6659):465-71 PMID: 9393997
  38. The myofibroblast in pulmonary fibrosis.
    Chest. 2002 Dec;122(6 Suppl):286S-289S PMID: 12475801
  39. The tension mounts: mechanics meets morphogenesis and malignancy.
    J Mammary Gland Biol Neoplasia. 2004 Oct;9(4):325-42 PMID: 15838603
  40. Myofibroblasts and mechano-regulation of connective tissue remodelling.
    Nat Rev Mol Cell Biol. 2002 May;3(5):349-63 PMID: 11988769
  41. TGF-beta activation by traction?
    Trends Cell Biol. 2004 Dec;14(12):657-9 PMID: 15564041
  42. The integrin alpha(v)beta8 mediates epithelial homeostasis through MT1-MMP-dependent activation of TGF-beta1.
    J Cell Biol. 2002 Apr 29;157(3):493-507 PMID: 11970960
  43. The fibronectin domain ED-A is crucial for myofibroblastic phenotype induction by transforming growth factor-beta1.
    J Cell Biol. 1998 Aug 10;142(3):873-81 PMID: 9700173
  44. Quantifying lamella dynamics of cultured cells by SACED, a new computer-assisted motion analysis.
    Exp Cell Res. 1999 Aug 25;251(1):234-43 PMID: 10438589
  45. Alveolar epithelial cell mesenchymal transition develops in vivo during pulmonary fibrosis and is regulated by the extracellular matrix.
    Proc Natl Acad Sci U S A. 2006 Aug 29;103(35):13180-5 PMID: 16924102
  46. BMP1 controls TGFbeta1 activation via cleavage of latent TGFbeta-binding protein.
    J Cell Biol. 2006 Oct 9;175(1):111-20 PMID: 17015622
  47. Latent TGF-beta binding protein LTBP-1 contains three potential extracellular matrix interacting domains.
    J Cell Sci. 2001 Jan;114(Pt 1):187-197 PMID: 11112702
  48. alpha(v)beta(3) Integrin interacts with the transforming growth factor beta (TGFbeta) type II receptor to potentiate the proliferative effects of TGFbeta1 in living human lung fibroblasts.
    J Biol Chem. 2004 Sep 3;279(36):37726-33 PMID: 15187087
  49. The myofibroblast in wound healing and fibrocontractive diseases.
    J Pathol. 2003 Jul;200(4):500-3 PMID: 12845617
  50. TGF-beta 1 binding protein: a component of the large latent complex of TGF-beta 1 with multiple repeat sequences.
    Cell. 1990 Jun 15;61(6):1051-61 PMID: 2350783
  51. Extracellular regulation of TGF-beta activity in wound repair: growth factor latency as a sensor mechanism for injury.
    Thromb Haemost. 2004 Aug;92(2):253-61 PMID: 15269820
  52. The integrin alphavbeta3 is a receptor for the latency-associated peptides of transforming growth factors beta1 and beta3.
    Biochem J. 2003 Jan 15;369(Pt 2):311-8 PMID: 12358597
  53. Latent transforming growth factor-beta binding protein domains involved in activation and transglutaminase-dependent cross-linking of latent transforming growth factor-beta.
    J Cell Biol. 1997 Mar 10;136(5):1151-63 PMID: 9060478
  54. Integrin-mediated activation of latent transforming growth factor beta.
    Cancer Metastasis Rev. 2005 Sep;24(3):395-402 PMID: 16258727
  55. Increased expression of integrin alpha(v)beta3 contributes to the establishment of autocrine TGF-beta signaling in scleroderma fibroblasts.
    J Immunol. 2005 Dec 1;175(11):7708-18 PMID: 16301681
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
1540-8140
Published
2007-12-17
Pages
1311-23
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2140013
Subset
IM
Grants
NIAMS NIH HHS · P01 AR049698 · United States
NCI NIH HHS · R01 CA034282 · United States
NIAMS NIH HHS · AR49698 · United States
NCI NIH HHS · CA34282 · United States
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