Display options
Share it on

Adv Sci (Weinh). 2019 Mar 14;6(9):1801780. doi: 10.1002/advs.201801780. eCollection 2019 May 03.

Collagen Fibrils Mechanically Contribute to Tissue Contraction in an In Vitro Wound Healing Scenario.

Advanced science (Weinheim, Baden-Wurttemberg, Germany)

Erik Brauer, Evi Lippens, Oliver Klein, Grit Nebrich, Sophie Schreivogel, Gabriela Korus, Georg N Duda, Ansgar Petersen

Affiliations

  1. Julius Wolff Institute Charité-Universitätsmedizin Berlin 13353 Berlin Germany.
  2. Berlin-Brandenburg School for Regenerative Therapies Charité-Universitätsmedizin Berlin 13353 Berlin Germany.
  3. Berlin-Brandenburg Center for Regenerative Therapies Charité-Universitätsmedizin Berlin 13353 Berlin Germany.
  4. Center for Musculo-Skeletal Surgery Charité-Universitätsmedizin Berlin 13353 Berlin Germany.

PMID: 31065517 PMCID: PMC6498124 DOI: 10.1002/advs.201801780

Abstract

Wound contraction is an ancient survival mechanism of vertebrates that results from tensile forces supporting wound closure. So far, tissue tension was attributed to cellular forces produced by tissue-resident (myo-)fibroblasts alone. However, difficulties in explaining pathological deviations from a successful healing path motivate the exploration of additional modulatory factors. Here, it is shown in a biomaterial-based in vitro wound healing model that the storage of tensile forces in the extracellular matrix has a significant, so-far neglected contribution to macroscopic tissue tension. In situ monitoring of tissue forces together with second harmonic imaging reveal that the appearance of collagen fibrils correlates with tissue contraction, indicating a mechanical contribution of tensioned collagen fibrils in the contraction process. As the re-establishment of tissue tension is key to successful wound healing, the findings are expected to advance the understanding of tissue healing but also underlying principles of misregulation and impaired functionality in scars and tissue contractures.

Keywords: cell force; collagen; extracellular matrix; second harmonic imaging; tension; tissue regeneration; traction force microscopy; wound contraction

Conflict of interest statement

The authors declare no conflict of interest.

References

  1. Am J Pathol. 1999 Mar;154(3):871-82 - PubMed
  2. J Biomed Mater Res. 2001;58(4):352-7 - PubMed
  3. Mol Biol Cell. 2001 Sep;12(9):2730-41 - PubMed
  4. Nat Rev Mol Cell Biol. 2002 May;3(5):349-63 - PubMed
  5. Breast Cancer Res. 2003;5(5):R129-35 - PubMed
  6. Int J Biochem Cell Biol. 2004 Jun;36(6):1031-7 - PubMed
  7. J Mater Sci Mater Med. 2004 Aug;15(8):925-32 - PubMed
  8. J Clin Invest. 2005 Feb;115(2):209-18 - PubMed
  9. Exp Cell Res. 2006 Feb 15;312(4):423-33 - PubMed
  10. J Invest Dermatol. 2007 Mar;127(3):526-37 - PubMed
  11. J Pathol. 2008 Jan;214(2):199-210 - PubMed
  12. J R Soc Interface. 2008 Oct 6;5(27):1173-80 - PubMed
  13. Tissue Eng Part A. 2009 Jan;15(1):45-54 - PubMed
  14. Proc Natl Acad Sci U S A. 2009 Jun 23;106(25):10097-102 - PubMed
  15. J Biomech. 2010 Jan 5;43(1):146-55 - PubMed
  16. Dev Biol. 2010 May 1;341(1):126-40 - PubMed
  17. Dev Biol. 2010 Aug 1;344(1):259-71 - PubMed
  18. Bone. 2010 Dec;47(6):1076-9 - PubMed
  19. Am J Pathol. 2011 Mar;178(3):1221-32 - PubMed
  20. Biomech Model Mechanobiol. 2012 Mar;11(3-4):461-73 - PubMed
  21. Lab Invest. 1990 Jul;63(1):21-9 - PubMed
  22. Proc Natl Acad Sci U S A. 2012 Jan 31;109(5):1506-11 - PubMed
  23. Tissue Eng Part A. 2012 Sep;18(17-18):1804-17 - PubMed
  24. Am J Physiol Lung Cell Mol Physiol. 2012 Aug 1;303(3):L169-80 - PubMed
  25. J Cell Sci. 2012 Jul 1;125(Pt 13):3015-24 - PubMed
  26. Wound Repair Regen. 2012 Sep-Oct;20(5):658-66 - PubMed
  27. Ann Biomed Eng. 2013 May;41(5):917-30 - PubMed
  28. Dev Biol. 2013 Oct 15;382(2):457-69 - PubMed
  29. PLoS One. 2013 Sep 05;8(9):e73545 - PubMed
  30. Nat Protoc. 2014 Feb;9(2):457-63 - PubMed
  31. Adv Wound Care (New Rochelle). 2013 Mar;2(2):37-43 - PubMed
  32. J Mech Behav Biomed Mater. 2014 Sep;37:186-95 - PubMed
  33. Methods Cell Biol. 2014;123:367-94 - PubMed
  34. Methods Cell Biol. 2015;125:269-87 - PubMed
  35. N Engl J Med. 2015 Mar 19;372(12):1138-49 - PubMed
  36. J Mech Behav Biomed Mater. 2015 Dec;52:14-21 - PubMed
  37. Organogenesis. 2015;11(1):1-15 - PubMed
  38. Integr Biol (Camb). 2015 Oct;7(10):1120-34 - PubMed
  39. Nano Lett. 2015 Jun 10;15(6):3729-34 - PubMed
  40. Nat Commun. 2015 Aug 14;6:8026 - PubMed
  41. Sci Transl Med. 2015 Aug 19;7(301):301ra130 - PubMed
  42. PLoS One. 2016 Jan 06;11(1):e0146588 - PubMed
  43. Nat Commun. 2016 Mar 16;7:11036 - PubMed
  44. Oncogene. 2016 Oct 6;35(40):5263-5271 - PubMed
  45. Matrix. 1989 Jan;9(1):34-9 - PubMed
  46. J R Soc Interface. 2016 May;13(118): - PubMed
  47. J Mater Sci Mater Med. 2016 Jul;27(7):120 - PubMed
  48. Sci Adv. 2018 Jan 17;4(1):eaao4881 - PubMed
  49. Nat Commun. 2018 Oct 25;9(1):4430 - PubMed
  50. World J Surg. 1980 May;4(3):279-87 - PubMed
  51. Am J Pathol. 1994 Jul;145(1):114-25 - PubMed
  52. J Cell Biol. 1994 Feb;124(4):401-4 - PubMed
  53. Invest Ophthalmol Vis Sci. 1994 May;35(6):2804-8 - PubMed
  54. J Cell Physiol. 1998 Jun;175(3):323-32 - PubMed
  55. Plast Reconstr Surg. 1998 Jul;102(1):124-31; discussion 132-4 - PubMed

Publication Types