TGF-β3 modulates the inflammatory environment and reduces scar formation following vocal fold mucosal injury in rats

DMM Disease Models and Mechanisms

Volumn 7, Issue 1, 2014, Pages 83-91

  Chang, Zhen ^a   Kishimoto, Yo ^a   Hasan, Ayesha ^a   Welham, Nathan V ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

Fibrosis; Larynx; Tissue repair; Wound healing

Indexed keywords

PLACEBO; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; TRANSFORMING GROWTH FACTOR BETA3;

ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL SUBPOPULATION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FIBROBLAST; GENETIC TRANSCRIPTION; IMMUNOHISTOCHEMISTRY; IMMUNOLOCALIZATION; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; LARYNX INJURY; MOUTH MUCOSA; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SCAR FORMATION; THERAPY EFFECT; TREATMENT RESPONSE; VOCAL FOLD MUCOSAL INJURY; WOUND HEALING;

FIBROSIS; LARYNX; TISSUE REPAIR; WOUND HEALING;

ANIMALS; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; CELLS, CULTURED; CICATRIX; EPITHELIAL CELLS; EXTRACELLULAR MATRIX; FIBROBLASTS; FLOW CYTOMETRY; HUMANS; INFLAMMATION; MALE; MOUTH MUCOSA; RATS; RATS, INBRED F344; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA3; VOCAL CORDS; WOUND HEALING;

EID: 84892406239     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.013326     Document Type: Article

References (61)

1. Bandyopadhyay, B., Fan, J., Guan, S., Li, Y., Chen, M., Woodley, D. T. and Li, W. (2006). A "traffic control" role for TGF-β3: orchestrating dermal and epidermal cell motility during wound healing. J. Cell Biol. 172, 1093-1105.
2. Blakytny, R., Ludlow, A., Martin, G. E. M., Ireland, G., Lund, L. R., Ferguson, M. W. J. and Brunner, G. (2004). Latent TGF-β1 activation by platelets. J. Cell. Physiol. 199, 67-76.
3. Branski, R. C., Verdolini, K., Sandulache, V., Rosen, C. A. and Hebda, P. A. (2006). Vocal fold wound healing: a review for clinicians. J. Voice 20, 432-442.
4. Catten, M., Gray, S. D., Hammond, T. H., Zhou, R. and Hammond, E. (1998). Analysis of cellular location and concentration in vocal fold lamina propria. Otolaryngol. Head Neck Surg. 118, 663-667.
5. Chang, Z., Ling, C., Yamashita, M. and Welham, N. V. (2010). Microarray-driven validation of reference genes for quantitative real-time polymerase chain reaction in a rat vocal fold model of mucosal injury. Anal. Biochem. 406, 214-221.
6. Chen, X. and Thibeault, S. L. (2009). Novel isolation and biochemical characterization of immortalized fibroblasts for tissue engineering vocal fold lamina propria. Tissue Eng. Part C Methods 15, 201-212.
7. Clark, R. A. F. (1990). Fibronectin matrix deposition and fibronectin receptor expression in healing and normal skin. J. Invest. Dermatol. 94 Suppl., 128S-134S.
8. Coolen, N. A., Schouten, K. C. W. M., Middelkoop, E. and Ulrich, M. M. W. (2010). Comparison between human fetal and adult skin. Arch. Dermatol. Res. 302, 47-55.
9. Cowin, A. J., Brosnan, M. P., Holmes, T. M. and Ferguson, M. W. J. (1998). Endogenous inflammatory response to dermal wound healing in the fetal and adult mouse. Dev. Dyn. 212, 385-393.
10. Cowin, A. J., Holmes, T. M., Brosnan, P. and Ferguson, M. W. J. (2001). Expression of TGF-β and its receptors in murine fetal and adult dermal wounds. Eur. J. Dermatol. 11, 424-431.
11. Damoiseaux, J. G., Döpp, E. A., Calame, W., Chao, D., MacPherson, G. G. and Dijkstra, C. D. (1994). Rat macrophage lysosomal membrane antigen recognized by monoclonal antibody ED1. Immunology 83, 140-147.
12. Derynck, R. and Zhang, Y. E. (2003). Smad-dependent and Smad-independent pathways in TGF-β family signalling. Nature 425, 577-584.
13. Ferguson, M. W. J. and O'Kane, S. (2004). Scar-free healing: from embryonic mechanisms to adult therapeutic intervention. Philos. Trans. R. Soc. B 359, 839-850.
14. Ferguson, M. W. J., Duncan, J. A. L., Bond, J. S., Bush, J. A., Durani, P., So, K., Taylor, L., Chantrey, J., Mason, T., James, G. et al. (2009). Prophylactic administration of avotermin for improvement of skin scarring: three double-blind, placebo-controlled, phase I/II studies. Lancet 373, 1264-1274.
15. Flanders, K. C., Thompson, N. L., Cissel, D. S., Van Obberghen-Schilling, E., Baker, C. C., Kass, M. E., Ellingsworth, L. R., Roberts, A. B. and Sporn, M. B. (1989). Transforming growth factor-β1: histochemical localization with antibodies to different epitopes. J. Cell Biol. 108, 653-660.
16. Flanders, K. C., Lüdecke, G., Engels, S., Cissel, D. S., Roberts, A. B., Kondaiah, P., Lafyatis, R., Sporn, M. B. and Unsicker, K. (1991). Localization and actions of transforming growth factor-βs in the embryonic nervous system. Development 113, 183-191.
17. Gurtner, G. C., Werner, S., Barrandon, Y. and Longaker, M. T. (2008). Wound repair and regeneration. Nature 453, 314-321.
18. Hamann, J. (2004). The EGF-TM7 family of the rat. Immunogenetics 56, 679-681.
19. Hirschi, S. D., Gray, S. D. and Thibeault, S. L. (2002). Fibronectin: an interesting vocal fold protein. J. Voice 16, 310-316.
20. Hosokawa, R., Nonaka, K., Morifuji, M., Shum, L. and Ohishi, M. (2003). TGF-β3 decreases type I collagen and scarring after labioplasty. J. Dent. Res. 82, 558-564.
21. Kurita, S., Nagata, K. and Hirano, M. (1983). A comparative study of the layer structure of the vocal fold. In Vocal Fold Physiology: Contemporary Research and Clinical Issues (ed. D. M. Bless and J. H. Abbs), pp. 3-21. San Diego, CA: College- Hill Press.
22. Leask, A. (2008). Targeting the TGF-β, endothelin-1 and CCN2 axis to combat fibrosis in scleroderma. Cell. Signal. 20, 1409-1414.
23. Leask, A., Parapuram, S. K., Shi-Wen, X. and Abraham, D. J. (2009). Connective tissue growth factor (CTGF, CCN2) gene regulation: a potent clinical bio-marker of fibroproliferative disease? J. Cell Commun. Signal. 3, 89-94.
24. Lim, X., Tateya, I., Tateya, T., Muñoz-Del-Río, A. and Bless, D. M. (2006). Immediate inflammatory response and scar formation in wounded vocal folds. Ann. Otol. Rhinol. Laryngol. 115, 921-929.
25. Ling, C., Yamashita, M., Waselchuk, E. A., Raasch, J. L., Bless, D. M. and Welham, N. V. (2010). Alteration in cellular morphology, density and distribution in rat vocal fold mucosa following injury. Wound Repair Regen. 18, 89-97.
26. Livak, K. J. and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25, 402-408.
27. Lyons, R. M., Miller, D. A., Graycar, J. L., Moses, H. L. and Derynck, R. (1991). Differential binding of transforming growth factor-β1, -β2, and -β3 by fibroblasts and epithelial cells measured by affinity cross-linking of cell surface receptors. Mol. Endocrinol. 5, 1887-1896.
28. Manning, C. N., Kim, H. M., Sakiyama-Elbert, S., Galatz, L. M., Havlioglu, N. and Thomopoulos, S. (2011). Sustained delivery of transforming growth factor-β3 enhances tendon-to-bone healing in a rat model. J. Orthop. Res. 29, 1099-1105.
29. Martin, P. (1997). Wound healing-aiming for perfect skin regeneration. Science 276, 75-81.
30. Martin, P. and Leibovich, S. J. (2005). Inflammatory cells during wound repair: the good, the bad and the ugly. Trends Cell Biol. 15, 599-607.
31. Martin, P., D'Souza, D., Martin, J., Grose, R., Cooper, L., Maki, R. and McKercher, S. R. (2003). Wound healing in the PU.1 null mouse-tissue repair is not dependent on inflammatory cells. Curr. Biol. 13, 1122-1128.
32. Mast, B. A., Flood, L. C., Haynes, J. H., DePalma, R. L., Cohen, I. K., Diegelmann, R. F. and Krummel, T. M. (1991). Hyaluronic acid is a major component of the matrix of fetal rabbit skin and wounds: implications for healing by regeneration. Matrix 11, 63-68.
33. McCollum, P. T., Bush, J. A., James, G., Mason, T., O'Kane, S., McCollum, C., Krievins, D., Shiralkar, S. and Ferguson, M. W. J. (2011). Randomized phase II clinical trial of avotermin versus placebo for scar improvement. Br. J. Surg. 98, 925-934.
34. McKnight, A. J., Macfarlane, A. J., Dri, P., Turley, L., Willis, A. C. and Gordon, S. (1996). Molecular cloning of F4/80, a murine macrophage- restricted cell surface glycoprotein with homology to the G-protein-linked transmembrane 7 hormone receptor family. J. Biol. Chem. 271, 486-489.
35. Murata, H., Zhou, L., Ochoa, S., Hasan, A., Badiavas, E. and Falanga, V. (1997). TGF-β3 stimulates and regulates collagen synthesis through TGF-β1-dependent and independent mechanisms. J. Invest. Dermatol. 108, 258-262.
36. O'Kane, S. and Ferguson, M. W. J. (1997). Transforming growth factor-βs and wound healing. Int. J. Biochem. Cell Biol. 29, 63-78.
37. Occleston, N. L., Laverty, H. G., O'Kane, S. and Ferguson, M. W. J. (2008a). Prevention and reduction of scarring in the skin by Transforming Growth Factor-β3 (TGF-β3): from laboratory discovery to clinical pharmaceutical. J. Biomater. Sci. Polym. Ed. 19, 1047-1063.
38. Occleston, N. L., O'Kane, S., Goldspink, N. and Ferguson, M. W. J. (2008b). New therapeutics for the prevention and reduction of scarring. Drug Discov. Today 13, 973-981.
39. Occleston, N. L., Fairlamb, D., Hutchison, J., O'Kane, S. and Ferguson, M. W. J. (2009). Avotermin for the improvement of scar appearance: a new pharmaceutical in a new therapeutic area. Expert Opin. Investig. Drugs 18, 1231-1239.
40. Occleston, N. L., O'Kane, S., Laverty, H. G., Cooper, M., Fairlamb, D., Mason, T., Bush, J. A. and Ferguson, M. W. J. (2011). Discovery and development of avotermin (recombinant human transforming growth factor-β3): a new class of prophylactic therapeutic for the improvement of scarring. Wound Repair Regen. 19 Suppl., s38-s48.
41. Ohno, T., Hirano, S. and Rousseau, B. (2009). Gene expression of transforming growth factor-β1 and hepatocyte growth factor during wound healing of injured rat vocal fold. Laryngoscope 119, 806-810.
42. Ohno, S., Hirano, S., Kanemaru, S.-I., Tateya, I., Kitani, Y., Kojima, T., Nakamura, T. and Ito, J. (2011). Prevention of buccal mucosa scarring with transforming growth factor-β3. Laryngoscope 121, 1404-1409.
43. Ohno, S., Hirano, S., Kanemaru, S.-I., Kitani, Y., Kojima, T., Ishikawa, S., Mizuta, M., Tateya, I., Nakamura, T. and Ito, J. (2012). Transforming growth factor-β3 for the prevention of vocal fold scarring. Laryngoscope 122, 583-589.
44. Riede, T. (2011). Subglottal pressure, tracheal airflow, and intrinsic laryngeal muscle activity during rat ultrasound vocalization. J. Neurophysiol. 106, 2580-2592.
45. Riede, T., York, A., Furst, S., Müller, R. and Seelecke, S. (2011). Elasticity and stress relaxation of a very small vocal fold. J. Biomech. 44, 1936-1940.
46. Schrementi, M. E., Ferreira, A. M., Zender, C. and DiPietro, L. A. (2008). Sitespecific production of TGF-β in oral mucosal and cutaneous wounds. Wound Repair Regen. 16, 80-86.
47. Serini, G. and Gabbiana, G. (1996). Modulation of alpha-smooth muscle actin expression in fibroblasts by transforming growth factor-β isoforms: an in vivo and in vitro study. Wound Repair Regen. 4, 278-287.
48. Shah, M., Foreman, D. M. and Ferguson, M. W. J. (1995). Neutralisation of TGF-β1 and TGF-β2 or exogenous addition of TGF-β3 to cutaneous rat wounds reduces scarring. J. Cell Sci. 108, 985-1002.
49. So, K., McGrouther, D. A., Bush, J. A., Durani, P., Taylor, L., Skotny, G., Mason, T., Metcalfe, A. D., O'Kane, S. and Ferguson, M. W. J. (2011). Avotermin for scar improvement following scar revision surgery: a randomized, double-blind, withinpatient, placebo-controlled, phase II clinical trial. Plast. Reconstr. Surg. 128, 163-172.
50. Stramer, B. M., Mori, R. and Martin, P. (2007). The inflammation-fibrosis link? A Jekyll and Hyde role for blood cells during wound repair. J. Invest. Dermatol. 127, 1009-1017.
51. Tateya, T., Tateya, I., Sohn, J. H. and Bless, D. M. (2005). Histologic characterization of rat vocal fold scarring. Ann. Otol. Rhinol. Laryngol. 114, 183-191.
52. Tateya, T., Tateya, I. and Bless, D. M. (2006a). Collagen subtypes in human vocal folds. Ann. Otol. Rhinol. Laryngol. 115, 469-476.
53. Tateya, T., Tateya, I., Sohn, J. H. and Bless, D. M. (2006b). Histological study of acute vocal fold injury in a rat model. Ann. Otol. Rhinol. Laryngol. 115, 285-292.
54. Vyas, B., Ishikawa, K., Duflo, S. M., Chen, X. and Thibeault, S. L. (2010). Inhibitory effects of hepatocyte growth factor and interleukin-6 on transforming growth factor- β1 mediated vocal fold fibroblast-myofibroblast differentiation. Ann. Otol. Rhinol. Laryngol. 119, 350-357.
55. Waddington, S. N., Crossley, R., Sheard, V., Howe, S. J., Buckley, S. M. K., Coughlan, L., Gilham, D. E., Hawkins, R. E. and McKay, T. R. (2010). Gene delivery of a mutant TGF-β3 reduces markers of scar tissue formation after cutaneous wounding. Mol. Ther. 18, 2104-2111.
56. Wakefield, L. M., Winokur, T. S., Hollands, R. S., Christopherson, K., Levinson, A. D. and Sporn, M. B. (1990). Recombinant latent transforming growth factor-β1 has a longer plasma half-life in rats than active transforming growth factor-β1, and a different tissue distribution. J. Clin. Invest. 86, 1976-1984.
57. Welham, N. V., Marriott, G., Tateya, I. and Bless, D. M. (2008). Proteomic changes in rat thyroarytenoid muscle induced by botulinum neurotoxin injection. Proteomics 8, 1933-1944.
58. Welham, N. V., Choi, S. H., Dailey, S. H., Ford, C. N., Jiang, J. J. and Bless, D. M. (2011). Prospective multi-arm evaluation of surgical treatments for vocal fold scar and pathologic sulcus vocalis. Laryngoscope 121, 1252-1260.
59. Whitby, D. J. and Ferguson, M. W. J. (1991). Immunohistochemical localization of growth factors in fetal wound healing. Dev. Biol. 147, 207-215.
60. Yamashita, M., Bless, D. M. and Welham, N. V. (2010). Morphological and extracellular matrix changes following vocal fold injury in mice. Cells Tissues Organs 192, 262-271.
61. Zhang, Y. E. (2009). Non-Smad pathways in TGF-β signaling. Cell Res. 19, 128-139.