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Three Streams for the Mechanism of Hair Graying Mechanism of Hair Graying pISSN 1013-9087ㆍeISSN 2005-3894 Ann Dermatol Vol. 30, No. 4, 2018 https://doi.org/10.5021/ad.2018.30.4.397 REVIEW ARTICLE Three Streams for the Mechanism of Hair Graying Seong Kyeong Jo, Ji Yeon Lee, Young Lee1, Chang Deok Kim1, Jeung-Hoon Lee1, Young Ho Lee Departments of Anatomy and 1Dermatology, Chungnam National University College of Medicine, Daejeon, Korea Hair graying is an obvious sign of human aging. Although INTRODUCTION graying has been investigated extensively, the mechanism remains unclear. Here, we reviewed previous studies on the Hair graying is a common process occurring in people as mechanism of graying and seek to offer some new insights. they age. Fifty percent of the population has about 50% The traditional view is that hair graying is caused by ex- gray hair at the age of 50 years, known as the 50-50-50 haustion of the pigmentary potential of the melanocytes of rule1,2. Most non-pigmented hairs are white, attributable to hair bulbs. Melanocyte dysfunction may be attributable to total loss of melanin in the hair bulb. The term ‘gray hair’ the effects of toxic reactive oxygen species on melanocyte refers to an admixture of white non-pigmented hairs and nuclei and mitochondria. A recent study suggests that bulge pigmented hairs. Sometimes a single hair fiber can show a melanocyte stem cells (MSCs) are the key cells in play. progressive dilution of pigment from black, through gray Graying may be caused by defective MSC self-maintenance, to white. Hair graying may be inherited in an autoso- not by any deficiency in bulbar melanocytes. Our previous mal-dominant manner3,4. Hair graying usually develops in- study suggested that graying may be principally attributable itially at the temples, and then spreads to the frontal area, to active hair growth. Active hair growth may produce oxida- the vertex, and the parietal region, affecting the occipital tive or genotoxic stress in hair bulge. These internal stress region last5. If graying occurs prior to the third decade of may cause eventually depletion of MSC in the hair follicles. life, this is generally termed premature graying, although Taken together, hair graying may be caused by MSC deple- the criteria may differ5,6. Hair graying is associated with tion by genotoxic stress in the hair bulge. Hair graying may various autoimmune disorders including vitiligo and sev- also be sometimes caused by dysfunction of the melanocytes eral rare premature aging syndromes including the Hut- by oxidative stress in the hair bulb. In addition, hair graying chinson Gilford and Werner’syndrome7. Hair graying may may be attributable to MSC depletion by active hair growth. also reflect nutritional deficiencies (especially of vitamins) (Ann Dermatol 30(4) 397∼401, 2018) and the use of drugs such as chloroquine8-10. We do not know exactly the cause of hair graying in humans. Some -Keywords- evidences were found in mouse, but still only partial. Hair bulb, Hair bulge, Hair graying, Hair growth, Melanocyte Here, we reviewed previous studies on the mechanism of stem cell, Melanocytes graying in humans and seek to offer some new insights. INVOLVEMENT OF BULBAR Received January 10, 2018, Accepted for publication March 9, 2018 MELANOCYTES IN HAIR GRAYING Corresponding author: Young Ho Lee, Department of Anatomy, Chungnam National University College of Medicine, 266 Moowha-ro, Daejeon 35015, Tobin and Paus5 proposed that graying is caused by the Korea. Tel: 82-42-580-8203, Fax: 82-42-586-4800, E-mail: [email protected] ORCID: https://orcid.org/0000-0001-8238-2345 depletion of hair follicle bulbar melanocytes, due to dysre- This is an Open Access article distributed under the terms of the Creative gulation of antioxidant mechanisms and expression of an- Commons Attribution Non-Commercial License (http://creativecommons. ti-apoptotic factors. Overproduction of copper-zinc super- org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, oxidase induces excessive H2O2 formation and triggers ox- distribution, and reproduction in any medium, provided the original work is properly cited. idative damage. Accumulated reactive oxygen species Copyright © The Korean Dermatological Association and The Korean (ROS) imposes significant oxidative stresses on both bul- Society for Investigative Dermatology bar melanocytes per se and the highly proliferative hair Vol. 30, No. 4, 2018 397 SK Jo, et al bulb epithelium (consisting of keratinocytes)11. Inflammation, amelanogenic melanocytes are also present in the ORSs. ultraviolet light, cigarette smoking, psychoemotional stress, Such melanocytes may be able to migrate and differentiate certain chemicals, and genetic defects may trigger oxida- into melanogenic melanocytes, when certain stimuli are tive stress, inducing graying12-14. It was suggested that applied. Many researchers have sought to identify such graying may be caused by reduced tyrosinase activity in re-activating molecules recently. bulbar melanocytes or an abnormal interaction, melano- somes transfer, between these melanocytes and the cort- INVOLVEMENT OF BULGE MELANOCYTE ical keratinocytes of hair bulbs12,15. Also, graying may re- STEM CELLS IN GRAYING sult from insufficient melanocyte migration from the reser- voir (the hair bulge) of the upper outer root sheath (ORS) Nishimura et al. focused on the role played by melano- to the hair bulb lying closest to the dermal papilla5. The cyte stem cells (MSCs) in the hair bulge, as opposed to fol- levels of both anti-apoptotic factors (including BCL-2) and licular melanocytes, reporting that graying is caused by melanogenic enzymes (TRP-1 and TRP-2) are valuable defective MSC self-maintenance. Such maintenance re- markers of graying. The mitochondrion is the primary tar- quires BCL-2 and the micro-ophthalmia-associated tran- get of oxidative stressors, compromising energy produc- scriptional factor (MITF). Also, transforming growth factor-β tion. Thus, a mitochondrial theory of aging was suggested (TGF-β) and collagen XVII (Col17A1) are involved in reg- to explain hair graying13. ulation of MSC maintenance32-34. Melanin transfer from melanocytes to cortical keratino- Col17A1, a hemidesmosomal transmembrane collagen, is cytes may reduce keratinocyte proliferation and increase highly expressed in follicular stem cells. MSCs of the hair terminal keratinocyte differentiation, probably by modulat- bulge do not express Col17A1, but premature graying and ing intracellular calcium levels16,17. The growth rate of hair loss were evident in mice lacking Col17a1. Expression non-pigmented (white) beard hair is greater than that of of COL17A1 in basal keratinoctyes and follicular stem adjacent pigmented hair18. Melanin granules transferred to cells of COL17a1-deficient mice blocked premature MSC keratinocytes may serve as regulatory packages, control- differentiation and restored TGF-β signaling. Hair fol- ling cell differentiation and metabolic status19,20. Together, licular stem cells in the bulge-sub-bulge area provide a the data suggest that non-pigmented (white) hairs may functional niche for the MSCs35. grow more rapidly and become thicker than pigmented Defective MSC self-maintenance attributable to a Bcl-2 de- hairs, due to an absence of melanin in bulbar kerati- ficiency triggers selective MSC apoptosis, but not apopto- nocytes. Active hair growth of white hairs may be consid- sis of bulbar melanocytes. Aging or injury to MSCs in- ered as a result, not cause, of hair graying. duces ectopic pigmentation and/or differentiation within Insufficient neuroendocrine control of hair follicle melano- the hair bulge niche, accelerated by Mitf, a key transcrip- genesis by locally synthesized factors including adreno- tional regulator of melanogenesis. The roles played by corticotrophic hormone, thyrotrophin-releasing hormone, stem cell apoptosis and ectopic differentiation remain un- thyroid hormone, α-melanocyte stimulating hormone, clear; both may contribute to MSC loss to a similar ex- and β-endorphin, melanocortin has been also suggested tent32. However, the work of Fisher and Nishimura is es- to trigger or progress graying21-28. Clinical interventions sentially mouse-based. Further study should be done in seek to modulate neuroendocrine factor-mediated control humans to unveil hair graying. of melanogenesis and human melanocyte biology, to pre- Graying is associated with age-related defects in MSC vent or reverse graying29. maintenance. Irreversible DNA damage caused by geno- Interestingly, graying is sometimes reversed even in the toxic stressors such as ionizing radiation interrupts MSC elderly. For example, some non-pigmented (white) hairs comeback in mice. MSC depletion via differentiation or begin to produce melanin once more after exposure to ra- apoptosis triggers ‘irreversible’ graying. A defect in the diation or cytokines, becoming proximally pigmented. ataxia-telangiectasia mutated (ATM) gene, a kinase serving One explanation is that melanocytes negative for 3,4-dihy- to transduce the DNA damage response, induces ectopic droxyphenylalanine and most melanocyte-specific makers MSC differentiation. ATM action is important for the main- remain in the ORSs of white hairs and begin to produce tenance of MSC stemness36. pigment after stimulation30,31. Recent work has focused principally on MSCs of the hair Thus, European researchers, including Paus and Tobin, bulge, not on bulbar melanocytes. The B-Raf and C-Raf considered that graying is caused by depletion or dysfunc- kinases that play critical roles in melanoma development
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