β-Catenin-regulated myeloid cell adhesion and migration determine wound healing

Journal of Clinical Investigation

Volumn 124, Issue 6, 2014, Pages 2599-2610

  Amini Nik, Saeid ^a   Cambridge, Elizabeth ^b   Yu, Winston ^a   Guo, Anne ^a   Whetstone, Heather ^a   Nadesan, Puviindran ^a   Poon, Raymond ^a   Hinz, Boris ^b   Alman, Benjamin A ^a,c  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; CELL ADHESION; CELL FUNCTION; CELL LINEAGE; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; DISEASE ASSOCIATION; GENE DELETION; GENE EXPRESSION PROFILING; HUMAN; HUMAN TISSUE; MACROPHAGE MIGRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SCAR FORMATION; SKIN FIBROBLAST; SKIN INJURY; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; WOUND HEALING;

ANIMALS; BETA CATENIN; CELL ADHESION; CELL LINEAGE; CELL MOVEMENT; CICATRIX; CICATRIX, HYPERTROPHIC; HUMANS; MACROPHAGES; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MYELOID CELLS; SKIN; TCF TRANSCRIPTION FACTORS; TRANSCRIPTOME; TRANSFORMING GROWTH FACTOR BETA1; WOUND HEALING;

EID: 84902147928     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI62059     Document Type: Article

References (61)

1. Sen CK, et al. Human skin wounds: a major and snowballing threat to public health and the economy. Wound Repair Regen. 2009;17(6):763-771.
2. Gottrup F. A specialized wound-healing center concept: importance of a multidisciplinary department structure and surgical treatment facilities in the treatment of chronic wounds. Am J Surg. 2004;187(5 A):38S-43S.
3. Gurtner GC, Werner S, Barrandon Y, Longaker MT. Wound repair and regeneration. Nature. 2008;453(7193):314-321.
4. Bielefeld KA, Amini-Nik S, Alman BA. Cutaneous wound healing: recruiting developmental pathways for regeneration. Cell Mol Life Sci. 2013;70(12):2059- 2081.
5. Cheon SS, et al. β-Catenin stabilization dysregulates mesenchymal cell proliferation, motility, and invasiveness and causes aggressive fibromatosis and hyperplastic cutaneous wounds. Proc Natl Acad Sci U S A. 2002;99(10):6973-6978.
6. Amini-Nik S, et al. Ultrafast mid-IR laser scalpel: protein signals of the fundamental limits to minimally invasive surgery. PLoS One. 2010;5(9):e13053.
7. Hinz B, et al. Recent developments in myofibroblast biology: paradigms for connective tissue remodeling. Am J Pathol. 2012;180(4):1340-1355.
8. Radisky DC, Kenny PA, Bissell MJ. Fibrosis and cancer: do myofibroblasts come also from epithelial cells via EMT? J Cell Biochem. 2007;101(4):830-839.
9. Di Pietro LA, Burdick M, Low QE, Kunkel SL, Strieter RM. MIP-1α as a critical macrophage chemoattractant in murine wound repair. J Clin Invest. 1998;101(8):1693-1698.
10. Cheon SS, et al. β-Catenin regulates wound size and mediates the effect of TGF-β in cutaneous healing. FASEB J. 2006;20(6):692-701.
11. Bielefeld KA, et al. Fibronectin and β-catenin act in a regulatory loop in dermal fibroblasts to modulate cutaneous healing. J Biol Chem. 2011;286(31):27687-27697.
12. Harada N, et al. Intestinal polyposis in mice with a dominant stable mutation of the beta-catenin gene. EMBO J. 1999;18(21):5931-5942.
13. van Amerongen R, Nusse R. Towards an integrated view of Wnt signaling in development. Development. 2009;136(19):3205-3214.
14. Geissmann F, Manz MG, Jung S, Sieweke MH, Merad M, Ley K. Development of monocytes, macrophages, and dendritic cells. Science. 2010;327(5966):656-661.
15. Werner S, Grose R. Regulation of wound healing by growth factors and cytokines. Physiol Rev. 2003;83(3):835-870.
16. Goren I, et al. A transgenic mouse model of inducible macrophage depletion: effects of diphtheria toxin-driven lysozyme M-specific cell lineage ablation on wound inflammatory, angiogenic, and contractive processes. Am J Pathol. 2009;175(1):132-147.
17. Mirza R, Di Pietro LA, Koh TJ. Selective and specific macrophage ablation is detrimental to wound healing in mice. Am J Pathol. 2009;175(6):2454-2462.
18. Hopkinson-Woolley J, Hughes D, Gordon S, Martin P. Macrophage recruitment during limb development and wound healing in the embryonic and foetal mouse. J Cell Sci. 1994;107(pt 5):1159-1167.
19. Simpson DM, Ross R. The neutrophilic leukocyte in wound repair a study with antineutrophil serum. J Clin Invest. 1972;51(8):2009-2023.
20. Leibovich SJ, Ross R. The role of the macrophage in wound repair. A study with hydrocortisone and antimacrophage serum. Am J Pathol. 1975;78(1):71-100.
21. Amini-Nik S, Glancy D, Boimer C, Whetstone H, Keller C, Alman BA. Pax7 expressing cells contribute to dermal wound repair, regulating scar size through a β-catenin mediated process. Stem Cells. 2011;29(9):1371-1379.
22. Nolan GP, Fiering S, Nicolas JF, Herzenberg LA. Fluorescence-activated cell analysis and sorting of viable mammalian cells based on β-D-galactosidase activity after transduction of Escherichia coli lacZ. Proc Natl Acad Sci U S A. 1988;85(8):2603-2607.
23. Chari R, et al. A sequence-based approach to identify reference genes for gene expression analysis. BMC Med Genomics. 2010;3:32.
24. Clausen BE, Burkhardt C, Reith W, Renkawitz R, Forster I. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 1999;8(4):265-277.
25. Gu Q, Wang D, Cui C, Gao Y, Xia G, Cui X. Effects of radiation on wound healing. J Environ Pathol Toxicol Oncol. 1998;17(2):117-123.
26. Tsumano T, et al. A new mouse model of impaired wound healing after irradiation. J Plast Surg Hand Surg. 2013;47(2):83-88.
27. Van den Bossche J, et al. Alternatively activated macrophages engage in homotypic and heterotypic interactions through IL-4 and polyamine-induced E-cadherin/catenin complexes. Blood. 2009;114(21):4664-4674.
28. Skokos EA, Charokopos A, Khan K, Wanjala J, Kyriakides TR. Lack of TNF-α-induced MMP-9 production and abnormal E-cadherin redistribution associated with compromised fusion in MCP-1-null macrophages. Am J Pathol. 2011;178(5):2311-2321.
29. Van den Bossche J, Van Ginderachter JA. E-cadherin: from epithelial glue to immunological regulator. Eur J Immunol. 2013;43(1):34-37.
30. Van den Bossche J, Malissen B, Mantovani A, De Baetselier P, Van Ginderachter JA. Regulation and function of the E-cadherin/catenin complex in cells of the monocyte-macrophage lineage and DCs. Blood. 2012;119(7):1623-1633.
31. Allport JR, Muller WA, Luscinskas FW. Monocytes induce reversible focal changes in vascular endo thelial cadherin complex during transendothelial migration under flow. J Cell Biol. 2000;148(1):203-216.
32. Cai J, et al. MicroRNA-374a activates Wnt/β-catenin signaling to promote breast cancer metastasis. J Clin Invest. 2013;123(2):566-579.
33. Hinz B. Formation and function of the myofibroblast during tissue repair. J Invest Dermatol. 2007;127(3):526-537.
34. Wang XJ, Han G, Owens P, Siddiqui Y, Li AG. Role of TGF β-mediated inflammation in cutaneous wound healing. J Investig Dermatol Symp Proc. 2006;11(1):112-117.
35. Poon R, Nik SA, Ahn J, Slade L, Alman BA. β-Catenin and transforming growth factor beta have distinct roles regulating fibroblast cell motility and the induction of collagen lattice contraction. BMC Cell Biol. 2009;10:38.
36. Bertrand S, Godoy M, Semal P, Van Gansen P. Transdifferentiation of macrophages into fibroblasts as a result of Schistosoma mansoni infection. Int J Dev Biol. 1992;36(1):179-184.
37. Bringuier AF, Seebold-Choqueux C, Moricard Y, Simmons DJ, Milhaud G, Labat ML. T-lymphocyte control of HLA-DR blood monocyte differentiation into neo-fibroblasts. Further evidence of pluripotential secreting functions of HLA-DR monocytes, involving not only collagen but also uromodulin, amyloid-β peptide, α-fetoprotein, and carcinoembryonic antigen. Biomed Pharmacother. 1992;46(2-3):91-108.
38. Godoy M, Geuskens M, Van Marck EA, Borojevic R, Van Gansen P. Schistosomiasis and in vitro transdifferentiation of murine peritoneal macrophages into fibroblastic cells. Parasitol Res. 1989;76(2):150-161.
39. Labat ML, et al. Monocytic origin of fibroblasts: spontaneous transformation of blood monocytes into neo-fibroblastic structures in osteomyelosclerosis and Engelmann's disease. Biomed Pharmacother. 1991;45(7):289-299.
40. Lin ML, Li YP, Li ZR, Lin JX, Zhou XL, Liang D. Macrophages acquire fibroblast characteristics in a rat model of proliferative vitreoretinopathy. Ophthalmic Res. 2011;45(4):180-190.
41. Li B, Pozzi A, Young PP. TNFα accelerates monocyte to endothelial transdifferentiation in tumors by the induction of integrin α5 expression and adhesion to fibronectin. Mol Cancer Res. 2011;9(6):702-711.
42. Chaffer CL, Weinberg RA. A perspective on cancer cell metastasis. Science. 2011;331(6024):1559-1564.
43. Rettig WJ, Garin-Chesa P, Beresford HR, Oettgen HF, Melamed MR, Old LJ. Cell-surface glycoproteins of human sarcomas: differential expression in normal and malignant tissues and cultured cells. Proc Natl Acad Sci U S A. 1988;85(9):3110-3114.
44. Jeon ES, et al. Cancer-derived lysophosphatidic acid stimulates differentiation of human mesenchymal stem cells to myofibroblast-like cells. Stem Cells. 2008;26(3):789-797.
45. Karnoub AE, et al. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature. 2007;449(7162):557-563.
46. Cheon S, et al. Prolonged β-catenin stabilization and tcf-dependent transcriptional activation in hyperplastic cutaneous wounds. Lab Invest. 2005;85(3):416-425.
47. Chou WC, et al. Direct migration of follicular melanocyte stem cells to the epidermis after wounding or UVB irradiation is dependent on Mc1r signaling. Nat Med. 2013;19(7):924-929.
48. Peters T, et al. Wound-healing defect of CD18 (-/-) mice due to a decrease in TGF-β1 and myofibroblast differentiation. EMBO J. 2005;24(19):3400-3410.
49. Labus MB, Stirk CM, Thompson WD, Melvin WT. Expression of Wnt genes in early wound healing. Wound Repair Regen. 1998;6(1):58-64.
50. Bielefeld KA, et al. Fibronectin and β-catenin act in a regulatory loop in dermal fibroblasts to modulate cutaneous healing. J Biol Chem. 2011;286(31):27687-27697.
51. Sato M. Upregulation of the Wnt/β-catenin pathway induced by transforming growth factor-beta in hypertrophic scars and keloids. Acta Derm Venereol. 2006;86(4):300-307.
52. Yu H, Bock O, Bayat A, Ferguson MW, Mrowietz U. Decreased expression of inhibitory SMAD6 and SMAD7 in keloid scarring. J Plast Reconstr Aesthet Surg. 2006;59(3):221-229.
53. Carre AL, et al. Interaction of wingless protein (Wnt), transforming growth factor-β1, and hyaluronan production in fetal and postnatal fibroblasts. Plast Reconstr Surg. 2010;125(1):74-88.
54. Srinivas S, et al. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol. 2001;1:4.
55. Brault V, et al. Inactivation of the β-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development. 2001;128(8):1253-1264.
56. Vintersten K, et al. Mouse in red: red fluorescent protein expression in mouse ES cells, embryos, and adult animals. Genesis. 2004;40(4):241-246.
57. Amini-Nik S, et al. Ultrafast mid-IR laser scalpel: protein signals of the fundamental limits to minimally invasive surgery. PLoS One. 2010;5(9):e13053.
58. Weischenfeldt J, Porse B. Bone Marrow-derived Macrophages (BMM): isolation and applications. CSH Protoc. 2008;2008:pdb.prot5080.
59. Amini Nik S, Ebrahim RP, Van Dam K, Cassiman JJ, Tejpar S. TGF-β modulates β-catenin stability and signaling in mesenchymal proliferations. Exp Cell Res. 2007;313(13):2887-2895.
60. Plovins A, Alvarez AM, Ibanez M, Molina M, Nombela C. Use of fluorescein-di-β-D-galactopyranoside (FDG) and C12-FDG as substrates for β-galacto sidase detection by flow cytometry in animal, bacterial, and yeast cells. Appl Environ Microbiol. 1994;60(12):4638-4641.
61. Fearmonti R, Bond J, Erdmann D, Levinson H. A review of scar scales and scar measuring devices. Eplasty. 2010;10:e43.