Applications of hair follicle stem cells

doi:10.3877/cma.j.issn.2095-1221.2020.06.007

Abstract

Abstract:

Hair follicle stem cells are a kind of adult stem cells which exist in the protuberance of root sheath outside hair follicles, which characterize in rich sources and easy access. Like other adult stem cells in hair follicles, hair follicle stem cells have many advantages, such as self-renewal, high proliferation ability and multi-differentiation potential, etc., resulting in that hair follicle stem cells become a very good source of isolated stem cells and a tissue source for tissue engineering and regenerative medicine applications. The researches on hair follicle stem cells in epidermis and skin tissue engineering are booming, calling for a comprehensive review. This paper mainly reviews the advances in the application of hair follicle stem cells, including the induction of hair regeneration by stem cells, the repair of damaged skin, the promotion of nerve and spinal cord repair and the differentiation of cardiac-like cells.

Key words: Hair follicle stem cells, Nerve repair, Wound healing, Spinal cord injury, Cardiac-like cells

Jingyue Wu, Min Li, Gang Wang, Bo Diao. Applications of hair follicle stem cells[J]. Chinese Journal of Cell and Stem Cell(Electronic Edition), 2020, 10(06): 359-363.

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References 76

1	Cotsarelis G. Epithelial stem cells: a folliculocentric view[J]. J Invest Dermatol, 2006, 126(7): 1459-1468.
2	Li B, Hu W, Ma K, et al. Are hair follicle stem cells promising candidates for wound healing?[J]. Expert Opin Biol Ther, 2019, 19(2): 119-128.
3	Blanpain C, Fuchs E. Epidermal stem cells of the skin[J]. Annu Rev Cell Dev Biol, 2006, 22:339-373.
4	Oshima H, Rochat A, Kedzia C, et al. Morphogenesis and renewal of hair follicles from adult multipotent stem cells[J]. Cell, 2001, 104(2): 233-245.
5	Cotsarelis G. Epithelial stem cells: a folliculocentric view[J]. J Invest Dermatol, 2006, 126(7): 1459-1468.
6	Turksen K. Preface. Stem cell renewal and cell-cell communication [J]. Methods Mol Biol, 2015, 1212:v. doi: 10.1007/978-1-4939-2590-2.
7	Najafzadeh N, Nobakht M, Pourheydar B, et al. Rat hair follicle stem cells differentiate and promote recovery following spinal cord injury[J]. Neural Regen Res, 2013, 8(36): 3365-3372.
8	Najafzadeh N, Esmaeilzade B, Dastan Imcheh M. Hair follicle stem cells: In vitro and in vivo neural differentiation[J]. World J Stem Cells, 2015, 7(5): 866-872.
9	Liu F, Uchugonova A, Kimura H, et al. The bulge area is the major hair follicle source of nestin-expressing pluripotent stem cells which can repair the spinal cord compared to the dermal papilla[J]. Cell Cycle, 2011, 10(5):830-839.
10	Najafzadeh N, Sagha M, Heydari Tajaddod S, et al. In vitro neural differentiation of CD34 (+) stem cell populations in hair follicles by three different neural induction protocols[J]. In Vitro Cell Dev Biol Anim, 2015, 51(2): 192-203.
11	Aoki H, Hara A, Motohashi T, et al. Keratinocyte stem cells but not melanocyte stem cells are the primary target for radiation-induced hair graying[J]. J Invest Dermatol, 2013, 133(9): 2143-2151.
12	Babakhani A, Hashemi P, Mohajer Ansari J, et al. In vitro Differentiation of Hair Follicle Stem Cell into Keratinocyte by Simvastatin[J]. Iran Biomed J, 2019, 23(6): 404-411.
13	Xu ZC, Zhang Q, Li H. Human hair follicle stem cell differentiation into contractile smooth muscle cells is induced by transforming growth factor-β1 and platelet-derived growth factor BB[J]. Mol Med Rep, 2013, 8(6): 1715-1721.
14	Xu ZC, Zhang Q, Li H. Differentiation of human hair follicle stem cells into endothelial cells induced by vascular endothelial and basic fibroblast growth factors[J]. Mol Med Rep, 2014, 9(1): 204-210.
15	Ma D, Lee ST, Chua AWC. Isolation and culture of hair follicle dermal sheath mesenchymal stromal cells[J]. Methods Mol Biol, 2019, 1993:61-70.
16	Yashiro M, Mii S, Aki R, et al. From hair to heart: nestin-expressing hair-follicle-associated pluripotent (HAP) stem cells differentiate to beating cardiac muscle cells[J]. Cell Cycle, 2015, 14(14): 2362-2366.
17	Yamazaki A, Yashiro M, Mii S, et al. Isoproterenol directs hair follicle-associated pluripotent (HAP) stem cells to differentiate in vitro to cardiac muscle cells which can be induced to form beating heart-muscle tissue sheets[J]. Cell Cycle, 2016, 15(5): 760-765.
18	Pasolli HA. The hair follicle bulge: a niche for adult stem cells[J]. Microsc Microanal, 2011, 17(4): 513-519.
19	Cotsarelis G, Sun TT, Lavker RM. Label-retaining cells reside in the bulge area of pilosebaceous unit: implications for follicular stem cells, hair cycle, and skin carcinogenesis[J]. Cell, 1990, 61(7): 1329-1337.
20	Paus R, Cotsarelis G. The biology of hair follicles[J]. N Engl J Med, 1999, 341(7): 491-497.
21	Stenn KS, Paus R. Controls of hair follicle cycling[J]. Physiol Rev, 2001, 81(1): 449-494.
22	Fuchs E. Cell biology: More than skin deep[J]. J Cell Biol, 2015, 209(5): 629-631.
23	Zhang H, Zhang S, Zhao H, et al. Ovine hair follicle stem cells derived from single vibrissae reconstitute haired skin[J]. Int J Mol Sci, 2015, 16(8): 17779-17797.
24	Su YS, Miao Y, Jiang JD, et al. A simple and rapid model for hair-follicle regeneration in the nude mouse[J]. Clin Exp Dermatol, 2015, 40(6): 653-658.
25	孙锡金, 胡志奇, 苗勇. 小鼠毛囊细胞注射移植实验研究[J]. 中华整形外科杂志, 2012, (01): 44-49.
26	Li G, Tang X, Zhang S, et al. SIRT7 activates quiescent hair follicle stem cells to ensure hair growth in mice[J]. EMBO J, 2020, 39(18):e104365.
27	Gentile P. Autologous cellular method using micrografts of human adipose tissue derived follicle stem cells in androgenic alopecia[J]. Int J Mol Sci, 2019, 20(14):3446.
28	Elmaadawi IH, Mohamed BM, Ibrahim ZAS, et al. Stem cell therapy as a novel therapeutic intervention for resistant cases of alopecia areata and androgenetic alopecia[J]. J Dermatolog Treat, 2018, 29(5): 431-440.
29	Gonzales KAU, Fuchs E. Skin and its regenerative powers: An alliance between stem cells and their niche[J]. Dev Cell, 2017, 43(4): 387-401.
30	Ansell DM, Kloepper JE, Thomason HA, et al. Exploring the "hair growth-wound healing connection" : anagen phase promotes wound re-epithelialization[J]. J Invest Dermatol, 2011, 131(2): 518-528.
31	Vagnozzi AN, Reiter JF, Wong SY. Hair follicle and interfollicular epidermal stem cells make varying contributions to wound regeneration[J]. Cell Cycle, 2015, 14(21): 3408-3417.
32	Brownell I, Guevara E, Bai CB, et al. Nerve-derived sonic hedgehog defines a niche for hair follicle stem cells capable of becoming epidermal stem cells[J]. Cell Stem Cell, 2011, 8(5): 552-565.
33	Cheng C, Guo GF, Martinez JA, et al. Dynamic plasticity of axons within a cutaneous milieu[J]. J Neurosci, 2010, 30(44): 14735-14744.
34	Langton AK, Herrick SE, Headon DJ. An extended epidermal response heals cutaneous wounds in the absence of a hair follicle stem cell contribution[J]. J Invest Dermatol, 2008, 128(5): 1311-1318.
35	Nakrieko KA, Rudkouskaya A, Irvine TS, et al. Targeted inactivation of integrin-linked kinase in hair follicle stem cells reveals an important modulatory role in skin repair after injury[J]. Mol Biol Cell, 2011, 22(14): 2532-2540.
36	Ito M, Cotsarelis G. Is the hair follicle necessary for normal wound healing?[J]. J Invest Dermatol, 2008, 128(5): 1059-1061.
37	Heidari F, Yari A, Rasoolijazi H, et al. Bulge hair follicle stem cells accelerate cutaneous wound healing in rats[J]. Wounds, 2016, 28(4): 132-141.
38	Claudinot S, Nicolas M, Oshima H, et al. Long-term renewal of hair follicles from clonogenic multipotent stem cells[J]. Proc Natl Acad Sci U S A, 2005, 102(41): 14677-14682.
39	Ito M, Liu Y, Yang Z, et al. Stem cells in the hair follicle bulge contribute to wound repair but not to homeostasis of the epidermis[J]. Nat Med, 2005, 11(12): 1351-1354.
40	Morris RJ, Liu Y, Marles L, et al. Capturing and profiling adult hair follicle stem cells[J]. Nat Biotechnol, 2004, 22(4): 411-417.
41	Blanpain C, Lowry WE, Geoghegan A, et al. Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche[J]. Cell, 2004, 118(5): 635-648.
42	Morris RJ, Potten CS. Highly persistent label-retaining cells in the hair follicles of mice and their fate following induction of anagen[J]. J Invest Dermatol, 1999, 112(4): 470-475.
43	Chovatiya GL, Sarate RM, Sunkara RR, et al. Secretory phospholipase A-IIA overexpressing mice exhibit cyclic alopecia mediated through aberrant hair shaft differentiation and impaired wound healing response[J]. Sci Rep, 2017, 7(1): 11619.
44	Heidari F, Yari A, Rasoolijazi H, et al. Bulge hair follicle stem cells accelerate cutaneous wound healing in rats[J]. Wounds, 2016, 28(4): 132-141.
45	Li Y, Xia WD, Van der Merwe L, et al. Efficacy of stem cell therapy for burn wounds: a systematic review and meta-analysis of preclinical studies[J]. Stem Cell Res Ther, 2020, 11(1): 322.
46	Quan R, Du W, Zheng X, et al. VEGF165 induces differentiation of hair follicle stem cells into endothelial cells and plays a role in in vivo angiogenesis[J]. J Cell Mol Med, 2017, 21(8): 1593-1604.
47	史明艳, 高雪, 杨学义, 等. 构建具有毛囊结构的组织工程皮肤及移植研究[J]. 畜牧兽医学报, 2019, 50(10): 2097-2104.
48	Liu F, Zhou H, Du W, et al. Hair follicle stem cells combined with human allogeneic acellular amniotic membrane for repair of full thickness skin defects in nude mice.[J]. J Tissue Eng Regen Med, 2020, 14(5): 723-735.
49	Jiménez F, Garde C, Poblet E, et al. A pilot clinical study of hair grafting in chronic leg ulcers[J]. Wound Repair Regen, 2012, 20(6): 806-814.
50	Liu JQ, Zhao KB, Feng ZH, et al. Hair follicle units promote re-epithelialization in chronic cutaneous wounds: A clinical case series study.[J]. Exp Ther Med, 2015, 10(1): 25-30.
51	Martínez-Martínez ML, Escario Travesedo E, Jiménez Acosta F. Hair-follicle transplant into chronic ulcers: A new graft concept[J]. Actas Dermosifiliogr, 2017, 108(6): 524-531.
52	Martínez ML, Escario E, Poblet E, et al. Hair follicle-containing punch grafts accelerate chronic ulcer healing: A randomized controlled trial[J]. J Am Acad Dermatol, 2016, 75(5): 1007-1014.
53	Garcin CL, Ansell DM. The battle of the bulge: re-evaluating hair follicle stem cells in wound repair[J]. Exp Dermatol, 2017, 26(2): 101-104.
54	Amoh Y, Kanoh M, Niiyama S, et al. Human and mouse hair follicles contain both multipotent and monopotent stem cells[J]. Cell Cycle, 2009, 8(1): 176-177.
55	Mii S, Duong J, Tome Y, et al. Nestin-expressing hair-follicle-associated pluripotent (HAP) stem cells promote whisker sensory-nerve growth in long-term 3D-Gelfoam^® histoculture[J]. Methods Mol Biol, 2016, 145339-145347.
56	Amoh Y, Kanoh M, Niiyama S, et al. Human hair follicle pluripotent stem (hfPS) cells promote regeneration of peripheral-nerve injury: an advantageous alternative to ES and iPS cells[J]. J Cell Biochem, 2009, 107(5): 1016-1020.
57	Hoffman RM, Amoh Y. Hair follicle-associated pluripotent(HAP) stem cells[J]. Prog Mol Biol Transl Sci, 2018, 160:23-28.
58	Hoffman RM, Mii S, Duong J, et al. Nerve growth and interaction in gelfoam histoculture: a nervous system organoid[J]. Methods Mol Biol, 2018, 1760:163-186.
59	Obara K, Tohgi N, Shirai K, et al. Hair-follicle-associated pluripotent (HAP) stem cells encapsulated on polyvinylidene fluoride membranes (PFM) promote functional recovery from spinal cord injury[J]. Stem Cell Rev Rep, 2019, 15(1): 59-66.
60	Amoh Y, Li L, Campillo R, et al. Implanted hair follicle stem cells form Schwann cells that support repair of severed peripheral nerves[J]. Proc Natl Acad Sci U S A, 2005, 102(49): 17734-17738.
61	Hoffman RM. Nestin-expressing hair follicle-accessible pluripotent stem cells for nerve and spinal cord repair[J]. Cells Tissues Organs, 2014, 200(1): 42-47.
62	Liu F, Hoffman RM. Hair follicle-associated pluripotent (HAP) stem cells in gelfoam histoculture for use in spinal cord repair[J]. Methods Mol Biol, 2018, 1760:145-162.
63	Yamazaki A, Obara K, Tohgi N, et al. Implanted hair-follicle-associated pluripotent (HAP) stem cells encapsulated in polyvinylidene fluoride membrane cylinders promote effective recovery of peripheral nerve injury.[J]. Cell Cycle, 2017, 16(20): 1927-1932.
64	Okano H, Nakamura M, Yoshida K, et al. Steps toward safe cell therapy using induced pluripotent stem cells.[J]. Circ Res, 2013, 112(3): 523-533.
65	Nori S, Okada Y, Yasuda A, et al. Grafted human-induced pluripotent stem-cell-derived neurospheres promote motor functional recovery after spinal cord injury in mice.[J]. Proc Natl Acad Sci U S A, 2011, 108(40): 16825-16830.
66	Amoh Y, Katsuoka K, Hoffman RM. Peripheral-Nerve and Spinal-Cord regeneration in mice using hair-follicle-associated pluripotent (HAP) stem cells.[J]. Methods Mol Biol, 2016, 1453:21-32.
67	席海燕, 丁海麦, 李晓晶, 等. 小鼠毛囊干细胞向心肌细胞的诱导分化及其鉴定[J]. 重庆医学, 2020, 49(18): 534-537.
68	Kim YH, Kim BJ, Kim SM, et al. Induction of cardiomyocytelike cells from hair follicle cells in mice.[J]. Int J Mol Med, 2019, 43(5): 2230-2240.
69	Hoffman RM. Human hair follicle associated-pluripotent (hHAP) stem cells differentiate to cardiac muscle cells[J]. Methods Mol Biol, 2019, 1879:385-392.
70	Tohgi N, Obara K, Yashiro M, et al. Human hair-follicle associated pluripotent (hHAP) stem cells differentiate to cardiac-muscle cells.[J]. Cell Cycle, 2017, 16(1): 95-99.
71	Yashiro M, Mii S, Aki R, et al. Protocols for efficient differentiation of hair follicle-associated pluripotent (HAP) stem cells to beating cardiac muscle cells[J]. Methods Mol Biol, 2016, 1453:151-159.
72	Shirai K, Hamada Y, Arakawa N, et al. Hypoxia enhances differentiation of hair follicle-associated-pluripotent (HAP) stem cells to cardiac-muscle cells[J]. J Cell Biochem, 2017, 118(3):554-558.
73	Ferrari S, Pellegrini G, Matsui T, et al. Gene therapy in combination with tissue engineering to treat epidermolysis bullosa.[J]. Expert Opin Biol Ther, 2006, 6(4): 367-378.
74	Mavilio F, Pellegrini G, Ferrari S, et al. Correction of junctional epidermolysis bullosa by transplantation of genetically modified epidermal stem cells.[J]. Nat Med, 2006, 12(12): 1397-1402.
75	Tiede S, Kloepper JE, Bodò E, et al. Hair follicle stem cells: walking the maze.[J]. Eur J Cell Biol, 2007, 86(7): 355-376.
76	李承新. 激光脱毛疗效回顾及进展[J]. 中国激光医学杂志, 2014, 23(5): 271.

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