Wound-induced hair follicle neogenesis: a new perspective on hair follicles regeneration in adult mammals_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

LIU Pengcheng ¹ , TAN Qiuwen ^1,2 , JIANG Yanlin ² ,  LÜ Qing ¹

1. Department of Breast Surgery, Clinical Research Center for Breast Disease, West China Hospital, Sichuan University, Chengdu Sichuan, 610041, P.R.China;
2. Laboratory of Stem Cell and Tissue Engineering, West China Hospital, Sichuan University, Chengdu Sichuan, 610041, P.R.China;

Corresponding author：

LÜ Qing, Email: lvqingwestchina@163.com

Keywords：

Wound-induced hair follicle neogenesis; embryogenic regeneration; skin healing; functional regeneration

DOI：

10.7507/1002-1892.201905102

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To explore the research progress of the cell sources and related signaling pathways of the wound-induced hair follicle neogenesis (WIHN) in recent years.Methods The literature related to WIHN in recent years was reviewed, and the cell sources and molecular mechanism were summarized and discussed.Results Current research shows that WIHN is a rare regeneration phenomenon in the skin of adult mammals, with multiple cell origins, both hair follicle stem cells and epithelial stem cells around the wound. Its molecular mechanism is complicated, which is regulated by many signaling pathways. Besides, the process is closely related to the immune response, the immunocytes and their related cytokines provide suitable conditions for this process.Conclusion There are still many unsolved problems on the cellular origins and molecular mechanisms of the WIHN. Further study on the mechanisms will enhance the understanding of adult mammals’ hair follicle regeneration and may provide new strategy for functional healing of the human skin.

Citation： LIU Pengcheng, TAN Qiuwen, JIANG Yanlin, LÜ Qing. Wound-induced hair follicle neogenesis: a new perspective on hair follicles regeneration in adult mammals. Chinese Journal of Reparative and Reconstructive Surgery, 2020, 34(3): 393-398. doi: 10.7507/1002-1892.201905102 Copy

1.	Myung PS, Takeo M, Ito M, et al. Epithelial Wnt ligand secretion is required for adult hair follicle growth and regeneration. J Invest Dermatol, 2013, 133(1): 31-41.
2.	Clevers H, Loh KM, Nusse R. Stem cell signaling. An integral program for tissue renewal and regeneration: Wnt signaling and stem cell control. Science, 2014, 346(6205): 1248012.
3.	Martínez ML, Escario E, Poblet E, et al. Hair follicle-containing punch grafts accelerate chronic ulcer healing: A randomized controlled trial. J Am Acad Dermatol, 2016, 75(5): 1007-1014.
4.	Seifert AW, Kiama SG, Seifert MG, et al. Skin shedding and tissue regeneration in African spiny mice (Acomys). Nature, 2012, 489(7417): 561-565.
5.	Sun ZY, Diao JS, Guo SZ, et al. A very rare complication: new hair growth around healing wounds. J Int Med Res, 2009, 37(2): 583-586.
6.	Wong TW, Hughes M, Wang SH. Never too old to regenerate? Wound induced hair follicle neogenesis after secondary intention healing in a geriatric patient J Tissue Viability, 2018, 27(2): 114-116.
7.	Ito M, Yang Z, Andl T, et al. Wnt-dependent de novo hair follicle regeneration in adult mouse skin after wounding. Nature, 2007, 447(7142): 316-320.
8.	Chuong CM. Regenerative biology: new hair from healing wounds. Nature, 2007, 447(7142): 265-266.
9.	Fan C, Luedtke MA, Prouty SM, et al. Characterization and quantification of wound-induced hair follicle neogenesis using in vivo confocal scanning laser microscopy. Skin Res Technol, 2011, 17(4): 387-397.
10.	Garza LA, Liu Y, Yang Z, et al. Prostaglandin D2 inhibits hair growth and is elevated in bald scalp of men with androgenetic alopecia. Sci Transl Med, 2012, 4(126): 126ra34.
11.	Slominski A, Wortsman J, Plonka PM, et al. Hair follicle pigmentation. J Invest Dermatol, 2005, 124(1): 13-21.
12.	Lough DM, Wetter N, Madsen C, et al. Transplantation of an LGR6+ epithelial stem cell-enriched scaffold for repair of full-thickness soft-tissue defects: the in vitro development of polarized hair-bearing skin. Plast Reconstr Surg, 2016, 137(2): 495-507.
13.	Yuriguchi M, Aoki H, Taguchi N, et al. Pigmentation of regenerated hairs after wounding. J Dermatol Sci, 2016, 84(1): 80-87.
14.	Kligman AM, Strauss JS. The formation of vellus hair follicles from human adult epidermis. J Invest Dermatol, 1956, 27(1): 19-23.
15.	Driskell RR, Lichtenberger BM, Hoste E, et al. Distinct fibroblast lineages determine dermal architecture in skin development and repair. Nature, 2013, 504(7479): 277-281.
16.	Gay D, Kwon O, Zhang Z, et al. Fgf9 from dermal γδ T cells induces hair follicle neogenesis after wounding. Nat Med, 2013, 19(7): 916-923.
17.	Nelson AM, Katseff AS, Resnik SR, et al. Interleukin-6 null mice paradoxically display increased STAT3 activity and wound-induced hair neogenesis. J Invest Dermatol, 2016, 136(5): 1051-1053.
18.	Nelson AM, Reddy SK, Ratliff TS, et al. dsRNA released by tissue damage activates TLR3 to drive skin regeneration. Cell Stem Cell, 2015, 17(2): 139-151.
19.	Zhou G, Yuan C, He X, et al. Effect of miR-125b on dermal papilla cells of goat secondary hair follicle. Electron J Biotechn, 2017, 25: 64-69.
20.	Gong L, Xu XG, Li YH. Embryonic-like regenerative phenomenon: wound-induced hair follicle neogenesis. Regen Med, 2018, 13(6): 729-739.
21.	Myung P, Ito M. Dissecting the bulge in hair regeneration. J Clin Invest, 2012, 122(2): 448-454.
22.	Fan SM, Tsai CF, Yen CM, et al. Inducing hair follicle neogenesis with secreted proteins enriched in embryonic skin. Biomaterials, 2018, 167: 121-131.
23.	Morris RJ, Liu Y, Marles L, et al. Capturing and profiling adult hair follicle stem cells. Nat Biotechnol, 2004, 22(4): 411-417.
24.	Tumbar T, Guasch G, Greco V, et al. Defining the epithelial stem cell niche in skin. Science, 2004, 303(5656): 359-363.
25.	Gonzales KAU, Fuchs E. Skin and its regenerative powers: an alliance between stem cells and their niche. Dev Cell, 2017, 43(4): 387-401.
26.	Taylor G, Lehrer MS, Jensen PJ, et al. Involvement of follicular stem cells in forming not only the follicle but also the epidermis. Cell, 2000, 102(4): 451-461.
27.	Watt FM. Mammalian skin cell biology: at the interface between laboratory and clinic. Science, 2014, 346(6212): 937-940.
28.	Jensen KB, Collins CA, Nascimento E, et al. Lrig1 expression defines a distinct multipotent stem cell population in mammalian epidermis. Cell Stem Cell, 2009, 4(5): 427-439.
29.	Snippert HJ, Haegebarth A, Kasper M, et al. Lgr6 marks stem cells in the hair follicle that generate all cell lineages of the skin. Science, 2010, 327(5971): 1385-1389.
30.	Wang X, Chen H, Tian R, et al. Macrophages induce AKT/β-catenin-dependent Lgr5 (+) stem cell activation and hair follicle regeneration through TNF. Nat Commun, 2017, 8: 14091.
31.	Li L, Li W. Epithelial-mesenchymal transition in human cancer: comprehensive reprogramming of metabolism, epigenetics, and differentiation. Pharmacol Ther, 2015, 150: 33-46.
32.	Skrypek N, Goossens S, De Smedt E, et al. Epithelial-to-mesenchymal transition: epigenetic reprogramming driving cellular plasticity. Trends Genet, 2017, 33(12): 943-959.
33.	Sayed N, Wong WT, Ospino F, et al. Transdifferentiation of human fibroblasts to endothelial cells: role of innate immunity. Circulation, 2015, 131(3): 300-309.
34.	Shaw T, Martin P. Epigenetic reprogramming during wound healing: loss of polycomb-mediated silencing may enable upregulation of repair genes. EMBO Rep, 2009, 10(8): 881-886.
35.	Telerman SB, Rognoni E, Sequeira I, et al. Dermal Blimp1 acts downstream of epidermal TGFβ and Wnt/β-catenin to regulate hair follicle formation and growth. J Invest Dermatol, 2017, 137(11): 2270-2281.
36.	Clevers H, Nusse R. Wnt/β-catenin signaling and disease. Cell, 2012, 149(6): 1192-1205.
37.	Choi YS, Zhang Y, Xu M, et al. Distinct functions for Wnt/β-catenin in hair follicle stem cell proliferation and survival and interfollicular epidermal homeostasis. Cell Stem Cell, 2013, 13(6): 720-733.
38.	Lien WH, Polak L, Lin M, et al. In vivo transcriptional governance of hair follicle stem cells by canonical Wnt regulators. Nat Cell Biol, 2014, 16(2): 179-190.
39.	Bänziger C, Soldini D, Schütt C, et al. Wntless, a conserved membrane protein dedicated to the secretion of Wnt proteins from signaling cells. Cell, 2006, 125(3): 509-522.
40.	London TB, Lee HJ, Shao Y, et al. Interaction between the internal motif KTXXXI of Idax and mDvl PDZ domain. Biochem Biophys Res Commun, 2004, 322(1): 326-332.
41.	Lee SH, Seo SH, Lee DH, et al. Targeting of CXXC5 by a competing peptide stimulates hair regrowth and wound-induced hair neogenesis. J Invest Dermatol, 2017, 137(11): 2260-2269.
42.	Chen D, Jarrell A, Guo C, et al. Dermal β-catenin activity in response to epidermal Wnt ligands is required for fibroblast proliferation and hair follicle initiation. Development, 2012, 139(8): 1522-1533.
43.	Gurtner GC, Werner S, Barrandon Y, et al. Wound repair and regeneration. Nature, 2008, 453(7193): 314-321.
44.	Chen P, Cescon M, Megighian A, et al. Collagen Ⅵ regulates peripheral nerve myelination and function. FASEB J, 2014, 28(3): 1145-1156.
45.	Kasuya A, Ito T, Tokura Y. M2 macrophages promote wound-induced hair neogenesis. J Dermatol Sci, 2018, 91(3): 250-255.
46.	Osaka N, Takahashi T, Murakami S, et al. ASK1-dependent recruitment and activation of macrophages induce hair growth in skin wounds. J Cell Biol, 2007, 176(7): 903-909.
47.	Cressman DE, Greenbaum LE, DeAngelis RA, et al. Liver failure and defective hepatocyte regeneration in interleukin-6-deficient mice. Science, 1996, 274(5291): 1379-1383.
48.	Hirota H, Kiyama H, Kishimoto T, et al. Accelerated nerve regeneration in mice by upregulated expression of interleukin (IL) 6 and IL-6 receptor after trauma. J Exp Med, 1996, 183(6): 2627-2634.
49.	Jia C. Advances in the regulation of liver regeneration. Expert Rev Gastroenterol Hepatol, 2011, 5(1): 105-121.
50.	Galun E, Rose-John S. The Regenerative Activity of Interleukin-6//Clifton NJ. Methods in molecular biology. Totowa: Humana Press, 2013: 59-77.
51.	Heinrich PC, Behrmann I, Haan S, et al. Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem J, 2003, 374(Pt 1): 1-20.
52.	Lin Q, Wang L, Lin Y, et al. Toll-like receptor 3 ligand polyinosinic: polycytidylic acid promotes wound healing in human and murine skin. J Invest Dermatol, 2012, 132(8): 2085-2092.
53.	Melkamu T, Kita H, O’Grady SM. TLR3 activation evokes IL-6 secretion, autocrine regulation of Stat3 signaling and TLR2 expression in human bronchial epithelial cells. J Cell Commun Signal, 2013, 7(2): 109-118.
54.	Sakakibara S, Nakamura Y, Satoh H, et al. Rna-binding protein Musashi2: developmentally regulated expression in neural precursor cells and subpopulations of neurons in mammalian CNS. J Neurosci, 2001, 21(20): 8091-8107.
55.	Kharas MG, Lengner CJ, Al-Shahrour F, et al. Musashi-2 regulates normal hematopoiesis and promotes aggressive myeloid leukemia. Nat Med, 2010, 16(8): 903-908.
56.	Ito T, Kwon HY, Zimdahl B, et al. Regulation of myeloid leukaemia by the cell-fate determinant Musashi. Nature, 2010, 466(7307): 765-768.
57.	Park SM, Deering RP, Lu Y, et al. Musashi-2 controls cell fate, lineage bias, and TGF-β signaling in HSCs. J Exp Med, 2014, 211(1): 71-87.
58.	Wang S, Li N, Yousefi M, et al. Transformation of the intestinal epithelium by the MSI2 RNA-binding protein. Nat Commun, 2015, 6: 6517.
59.	Rentas S, Holzapfel N, Belew MS, et al. Musashi-2 attenuates AHR signalling to expand human haematopoietic stem cells. Nature, 2016, 532(7600): 508-511.
60.	Sugiyama-Nakagiri Y, Akiyama M, Shibata S, et al. Expression of RNA-binding protein Musashi in hair follicle development and hair cycle progression. Am J Pathol, 2006, 168(1): 80-92.
61.	Ma X, Tian Y, Song Y, et al. Msi2 maintains quiescent state of hair follicle stem cells by directly repressing the Hh signaling pathway. J Invest Dermatol, 2017, 137(5): 1015-1024.
62.	Zhu AS, Li A, Ratliff TS, et al. After skin wounding, noncoding dsRNA coordinates prostaglandins and Wnts to promote regeneration. J Invest Dermatol, 2017, 137(7): 1562-1568.
63.	Hughes MW, Jiang TX, Plikus MV, et al. Msx2 supports epidermal competency during wound-induced hair follicle neogenesis. J Invest Dermatol, 2018, 138(9): 2041-2050.
64.	Kim D, Chen R, Sheu M, et al. Noncoding dsRNA induces retinoic acid synthesis to stimulate hair follicle regeneration via TLR3. Nat Commun, 2019, 10(1): 2811.
65.	Tan QW, Tang SL, Zhang Y, et al. Hydrogel from acellular porcine adipose tissue accelerates wound healing by inducing intradermal adipocyte regeneration. J Invest Dermatol, 2019, 139(2): 455-463.
66.	Gur-Cohen S, Yang H, Baksh SC, et al. Stem cell-driven lymphatic remodeling coordinates tissue regeneration. Science, 2019, 366(6470): 1218-1225.
67.	侯玉森, 段红杰, 刘玲英, 等. MSCs 修复烧伤创面的研究进展. 中国修复重建外科杂志, 2013, 27(5): 571-574.
68.	熊佳超, 宋建星. 脂肪来源干细胞治疗难愈性创面的研究进展. 中国修复重建外科杂志, 2018, 32(4): 457-461.

1. Myung PS, Takeo M, Ito M, et al. Epithelial Wnt ligand secretion is required for adult hair follicle growth and regeneration. J Invest Dermatol, 2013, 133(1): 31-41.
2. Clevers H, Loh KM, Nusse R. Stem cell signaling. An integral program for tissue renewal and regeneration: Wnt signaling and stem cell control. Science, 2014, 346(6205): 1248012.
3. Martínez ML, Escario E, Poblet E, et al. Hair follicle-containing punch grafts accelerate chronic ulcer healing: A randomized controlled trial. J Am Acad Dermatol, 2016, 75(5): 1007-1014.
4. Seifert AW, Kiama SG, Seifert MG, et al. Skin shedding and tissue regeneration in African spiny mice (Acomys). Nature, 2012, 489(7417): 561-565.
5. Sun ZY, Diao JS, Guo SZ, et al. A very rare complication: new hair growth around healing wounds. J Int Med Res, 2009, 37(2): 583-586.
6. Wong TW, Hughes M, Wang SH. Never too old to regenerate? Wound induced hair follicle neogenesis after secondary intention healing in a geriatric patient J Tissue Viability, 2018, 27(2): 114-116.
7. Ito M, Yang Z, Andl T, et al. Wnt-dependent de novo hair follicle regeneration in adult mouse skin after wounding. Nature, 2007, 447(7142): 316-320.
8. Chuong CM. Regenerative biology: new hair from healing wounds. Nature, 2007, 447(7142): 265-266.
9. Fan C, Luedtke MA, Prouty SM, et al. Characterization and quantification of wound-induced hair follicle neogenesis using in vivo confocal scanning laser microscopy. Skin Res Technol, 2011, 17(4): 387-397.
10. Garza LA, Liu Y, Yang Z, et al. Prostaglandin D2 inhibits hair growth and is elevated in bald scalp of men with androgenetic alopecia. Sci Transl Med, 2012, 4(126): 126ra34.
11. Slominski A, Wortsman J, Plonka PM, et al. Hair follicle pigmentation. J Invest Dermatol, 2005, 124(1): 13-21.
12. Lough DM, Wetter N, Madsen C, et al. Transplantation of an LGR6+ epithelial stem cell-enriched scaffold for repair of full-thickness soft-tissue defects: the in vitro development of polarized hair-bearing skin. Plast Reconstr Surg, 2016, 137(2): 495-507.
13. Yuriguchi M, Aoki H, Taguchi N, et al. Pigmentation of regenerated hairs after wounding. J Dermatol Sci, 2016, 84(1): 80-87.
14. Kligman AM, Strauss JS. The formation of vellus hair follicles from human adult epidermis. J Invest Dermatol, 1956, 27(1): 19-23.
15. Driskell RR, Lichtenberger BM, Hoste E, et al. Distinct fibroblast lineages determine dermal architecture in skin development and repair. Nature, 2013, 504(7479): 277-281.
16. Gay D, Kwon O, Zhang Z, et al. Fgf9 from dermal γδ T cells induces hair follicle neogenesis after wounding. Nat Med, 2013, 19(7): 916-923.
17. Nelson AM, Katseff AS, Resnik SR, et al. Interleukin-6 null mice paradoxically display increased STAT3 activity and wound-induced hair neogenesis. J Invest Dermatol, 2016, 136(5): 1051-1053.
18. Nelson AM, Reddy SK, Ratliff TS, et al. dsRNA released by tissue damage activates TLR3 to drive skin regeneration. Cell Stem Cell, 2015, 17(2): 139-151.
19. Zhou G, Yuan C, He X, et al. Effect of miR-125b on dermal papilla cells of goat secondary hair follicle. Electron J Biotechn, 2017, 25: 64-69.
20. Gong L, Xu XG, Li YH. Embryonic-like regenerative phenomenon: wound-induced hair follicle neogenesis. Regen Med, 2018, 13(6): 729-739.
21. Myung P, Ito M. Dissecting the bulge in hair regeneration. J Clin Invest, 2012, 122(2): 448-454.
22. Fan SM, Tsai CF, Yen CM, et al. Inducing hair follicle neogenesis with secreted proteins enriched in embryonic skin. Biomaterials, 2018, 167: 121-131.
23. Morris RJ, Liu Y, Marles L, et al. Capturing and profiling adult hair follicle stem cells. Nat Biotechnol, 2004, 22(4): 411-417.
24. Tumbar T, Guasch G, Greco V, et al. Defining the epithelial stem cell niche in skin. Science, 2004, 303(5656): 359-363.
25. Gonzales KAU, Fuchs E. Skin and its regenerative powers: an alliance between stem cells and their niche. Dev Cell, 2017, 43(4): 387-401.
26. Taylor G, Lehrer MS, Jensen PJ, et al. Involvement of follicular stem cells in forming not only the follicle but also the epidermis. Cell, 2000, 102(4): 451-461.
27. Watt FM. Mammalian skin cell biology: at the interface between laboratory and clinic. Science, 2014, 346(6212): 937-940.
28. Jensen KB, Collins CA, Nascimento E, et al. Lrig1 expression defines a distinct multipotent stem cell population in mammalian epidermis. Cell Stem Cell, 2009, 4(5): 427-439.
29. Snippert HJ, Haegebarth A, Kasper M, et al. Lgr6 marks stem cells in the hair follicle that generate all cell lineages of the skin. Science, 2010, 327(5971): 1385-1389.
30. Wang X, Chen H, Tian R, et al. Macrophages induce AKT/β-catenin-dependent Lgr5 (+) stem cell activation and hair follicle regeneration through TNF. Nat Commun, 2017, 8: 14091.
31. Li L, Li W. Epithelial-mesenchymal transition in human cancer: comprehensive reprogramming of metabolism, epigenetics, and differentiation. Pharmacol Ther, 2015, 150: 33-46.
32. Skrypek N, Goossens S, De Smedt E, et al. Epithelial-to-mesenchymal transition: epigenetic reprogramming driving cellular plasticity. Trends Genet, 2017, 33(12): 943-959.
33. Sayed N, Wong WT, Ospino F, et al. Transdifferentiation of human fibroblasts to endothelial cells: role of innate immunity. Circulation, 2015, 131(3): 300-309.
34. Shaw T, Martin P. Epigenetic reprogramming during wound healing: loss of polycomb-mediated silencing may enable upregulation of repair genes. EMBO Rep, 2009, 10(8): 881-886.
35. Telerman SB, Rognoni E, Sequeira I, et al. Dermal Blimp1 acts downstream of epidermal TGFβ and Wnt/β-catenin to regulate hair follicle formation and growth. J Invest Dermatol, 2017, 137(11): 2270-2281.
36. Clevers H, Nusse R. Wnt/β-catenin signaling and disease. Cell, 2012, 149(6): 1192-1205.
37. Choi YS, Zhang Y, Xu M, et al. Distinct functions for Wnt/β-catenin in hair follicle stem cell proliferation and survival and interfollicular epidermal homeostasis. Cell Stem Cell, 2013, 13(6): 720-733.
38. Lien WH, Polak L, Lin M, et al. In vivo transcriptional governance of hair follicle stem cells by canonical Wnt regulators. Nat Cell Biol, 2014, 16(2): 179-190.
39. Bänziger C, Soldini D, Schütt C, et al. Wntless, a conserved membrane protein dedicated to the secretion of Wnt proteins from signaling cells. Cell, 2006, 125(3): 509-522.
40. London TB, Lee HJ, Shao Y, et al. Interaction between the internal motif KTXXXI of Idax and mDvl PDZ domain. Biochem Biophys Res Commun, 2004, 322(1): 326-332.
41. Lee SH, Seo SH, Lee DH, et al. Targeting of CXXC5 by a competing peptide stimulates hair regrowth and wound-induced hair neogenesis. J Invest Dermatol, 2017, 137(11): 2260-2269.
42. Chen D, Jarrell A, Guo C, et al. Dermal β-catenin activity in response to epidermal Wnt ligands is required for fibroblast proliferation and hair follicle initiation. Development, 2012, 139(8): 1522-1533.
43. Gurtner GC, Werner S, Barrandon Y, et al. Wound repair and regeneration. Nature, 2008, 453(7193): 314-321.
44. Chen P, Cescon M, Megighian A, et al. Collagen Ⅵ regulates peripheral nerve myelination and function. FASEB J, 2014, 28(3): 1145-1156.
45. Kasuya A, Ito T, Tokura Y. M2 macrophages promote wound-induced hair neogenesis. J Dermatol Sci, 2018, 91(3): 250-255.
46. Osaka N, Takahashi T, Murakami S, et al. ASK1-dependent recruitment and activation of macrophages induce hair growth in skin wounds. J Cell Biol, 2007, 176(7): 903-909.
47. Cressman DE, Greenbaum LE, DeAngelis RA, et al. Liver failure and defective hepatocyte regeneration in interleukin-6-deficient mice. Science, 1996, 274(5291): 1379-1383.
48. Hirota H, Kiyama H, Kishimoto T, et al. Accelerated nerve regeneration in mice by upregulated expression of interleukin (IL) 6 and IL-6 receptor after trauma. J Exp Med, 1996, 183(6): 2627-2634.
49. Jia C. Advances in the regulation of liver regeneration. Expert Rev Gastroenterol Hepatol, 2011, 5(1): 105-121.
50. Galun E, Rose-John S. The Regenerative Activity of Interleukin-6//Clifton NJ. Methods in molecular biology. Totowa: Humana Press, 2013: 59-77.
51. Heinrich PC, Behrmann I, Haan S, et al. Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem J, 2003, 374(Pt 1): 1-20.
52. Lin Q, Wang L, Lin Y, et al. Toll-like receptor 3 ligand polyinosinic: polycytidylic acid promotes wound healing in human and murine skin. J Invest Dermatol, 2012, 132(8): 2085-2092.
53. Melkamu T, Kita H, O’Grady SM. TLR3 activation evokes IL-6 secretion, autocrine regulation of Stat3 signaling and TLR2 expression in human bronchial epithelial cells. J Cell Commun Signal, 2013, 7(2): 109-118.
54. Sakakibara S, Nakamura Y, Satoh H, et al. Rna-binding protein Musashi2: developmentally regulated expression in neural precursor cells and subpopulations of neurons in mammalian CNS. J Neurosci, 2001, 21(20): 8091-8107.
55. Kharas MG, Lengner CJ, Al-Shahrour F, et al. Musashi-2 regulates normal hematopoiesis and promotes aggressive myeloid leukemia. Nat Med, 2010, 16(8): 903-908.
56. Ito T, Kwon HY, Zimdahl B, et al. Regulation of myeloid leukaemia by the cell-fate determinant Musashi. Nature, 2010, 466(7307): 765-768.
57. Park SM, Deering RP, Lu Y, et al. Musashi-2 controls cell fate, lineage bias, and TGF-β signaling in HSCs. J Exp Med, 2014, 211(1): 71-87.
58. Wang S, Li N, Yousefi M, et al. Transformation of the intestinal epithelium by the MSI2 RNA-binding protein. Nat Commun, 2015, 6: 6517.
59. Rentas S, Holzapfel N, Belew MS, et al. Musashi-2 attenuates AHR signalling to expand human haematopoietic stem cells. Nature, 2016, 532(7600): 508-511.
60. Sugiyama-Nakagiri Y, Akiyama M, Shibata S, et al. Expression of RNA-binding protein Musashi in hair follicle development and hair cycle progression. Am J Pathol, 2006, 168(1): 80-92.
61. Ma X, Tian Y, Song Y, et al. Msi2 maintains quiescent state of hair follicle stem cells by directly repressing the Hh signaling pathway. J Invest Dermatol, 2017, 137(5): 1015-1024.
62. Zhu AS, Li A, Ratliff TS, et al. After skin wounding, noncoding dsRNA coordinates prostaglandins and Wnts to promote regeneration. J Invest Dermatol, 2017, 137(7): 1562-1568.
63. Hughes MW, Jiang TX, Plikus MV, et al. Msx2 supports epidermal competency during wound-induced hair follicle neogenesis. J Invest Dermatol, 2018, 138(9): 2041-2050.
64. Kim D, Chen R, Sheu M, et al. Noncoding dsRNA induces retinoic acid synthesis to stimulate hair follicle regeneration via TLR3. Nat Commun, 2019, 10(1): 2811.
65. Tan QW, Tang SL, Zhang Y, et al. Hydrogel from acellular porcine adipose tissue accelerates wound healing by inducing intradermal adipocyte regeneration. J Invest Dermatol, 2019, 139(2): 455-463.
66. Gur-Cohen S, Yang H, Baksh SC, et al. Stem cell-driven lymphatic remodeling coordinates tissue regeneration. Science, 2019, 366(6470): 1218-1225.
67. 侯玉森, 段红杰, 刘玲英, 等. MSCs 修复烧伤创面的研究进展. 中国修复重建外科杂志, 2013, 27(5): 571-574.
68. 熊佳超, 宋建星. 脂肪来源干细胞治疗难愈性创面的研究进展. 中国修复重建外科杂志, 2018, 32(4): 457-461.

Chinese Journal of Reparative and Reconstructive Surgery

Wound-induced hair follicle neogenesis: a new perspective on hair follicles regeneration in adult mammals

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