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Androgen modulation of Wnt/β-catenin signaling in androgenetic alopecia

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Abstract

Androgenetic alopecia (AGA) is a dermatological disorder of scalp hair loss characterized by a progressive miniaturization of hair follicles with shortened anagen phase leading to a decreased number of hairs on the scalp. It is a complex polygenic trait prevailing around two-thirds of the male population. Elevated expressions of 5α-dihydrotestosterone and androgen receptor are the causal factors for AGA. This review describes recent studies on the role of androgens and androgen receptor (AR) transactivation activity in modulating the Wnt/β-catenin signaling in the dermal papilla cells of the balding scalp in androgenetic alopecia. Here, we analyse the androgen-induced dermal papilla secreted factors on stimulating catagen entry in hair follicles and the molecular cross-talk between AR and Wnt/β-catenin signaling with a brief mention on alternative treatment strategy targeting Wnt/β-catenin signaling for promoting hair growth.

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References

  1. Alonso L, Fuchs E (2006) The hair cycle. J Cell Sci 119:391–393. https://doi.org/10.1242/jcs.02793

    Article  PubMed  CAS  Google Scholar 

  2. Bai X, Lei M, Shi J, Yu Y, Qiu W, Lai X, Liu Y, Yang T, Yang L, Widelitz RB, Chuong C-M, Lian X (2015) Roles of gasdermina3 in catagen–telogen transition during hair cycling. J Investig Dermatol 135:2162–2172. https://doi.org/10.1038/jid.2015.147

    Article  PubMed  CAS  Google Scholar 

  3. Bhargava S (2014) Increased DHT levels in androgenic alopecia have been selected for to protect men from prostate cancer. Med Hypotheses 82:428–432. https://doi.org/10.1016/j.mehy.2014.01.016

    Article  PubMed  CAS  Google Scholar 

  4. Breitkopf T, Leung G, Yu M, Wang E, McElwee KJ (2013) The basic science of hair biology: what are the causal mechanisms for the disordered hair follicle? Dermatol Clin 31:1–19. https://doi.org/10.1016/j.det.2012.08.006

    Article  PubMed  CAS  Google Scholar 

  5. Chamberlain NL, Driver ED, Miesfeld RL (1994) The length and location of CAG trinucleotide repeats in the androgen receptor N-terminal domain affect transactivation function. Nucleic Acids Res 22:3181–3186

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Clevers H, Nusse R (2012) Wnt/β-catenin signaling and disease. Cell 149:1192–1205. https://doi.org/10.1016/j.cell.2012.05.012

    Article  PubMed  CAS  Google Scholar 

  7. Cranwell W, Sinclair R (2016) Male androgenetic alopecia. Endotext. MDText.com, Inc, South Dartmouth

    Google Scholar 

  8. Culig Z (2016) Androgen receptor coactivators in regulation of growth and differentiation in prostate cancer. J Cell Physiol 231:270–274. https://doi.org/10.1002/jcp.25099

    Article  PubMed  CAS  Google Scholar 

  9. Ding D, Xu L, Menon M, Reddy GP, Barrack ER (2005) Effect of GGC (glycine) repeat length polymorphism in the human androgen receptor on androgen action. Prostate 62:133–139. https://doi.org/10.1002/pros.20128

    Article  PubMed  CAS  Google Scholar 

  10. Dinh QQ, Sinclair R (2007) Female pattern hair loss: current treatment concepts. Clin Interv Aging 2:189–199

    PubMed  PubMed Central  Google Scholar 

  11. Ellis JA, Sinclair R, Harrap SB (2002) Androgenetic alopecia: pathogenesis and potential for therapy. Expert Rev Mol Med 4:1–11. https://doi.org/10.1017/S1462399402005112 doi

    Article  PubMed  Google Scholar 

  12. Ellis JA, Stebbing M, Harrap SB (2001) Polymorphism of the androgen receptor gene is associated with male pattern baldness. J Investig Dermatol 116:452–455. https://doi.org/10.1046/j.1523-1747.2001.01261.x

    Article  PubMed  CAS  Google Scholar 

  13. Faydaci G, Bilal E, Necmettin P, Fatih T, Asuman O, Ugur K (2008) Baldness, benign prostate hyperplasia, prostate cancer and androgen levels. Aging Male 11:189–192. https://doi.org/10.1080/13685530802400995

    Article  PubMed  CAS  Google Scholar 

  14. Fong P, Tong HH, Ng KH, Lao CK, Chong CI, Chao CM (2015) In silico prediction of prostaglandin D2 synthase inhibitors from herbal constituents for the treatment of hair loss. J Ethnopharmacol 175:470–480. https://doi.org/10.1016/j.jep.2015.10.005

    Article  PubMed  CAS  Google Scholar 

  15. Garza LA, Liu Y, Yang Z, Alagesan B, Lawson JA, Norberg SM, Loy DE, Zhao T, Blatt HB, Stanton DC, Carrasco L, Ahluwalia G, Fischer SM, FitzGerald GA, Cotsarelis G (2012) Prostaglandin D2 inhibits hair growth and is elevated in bald scalp of men with androgenetic alopecia. Sci Transl Med 4:126ra134. https://doi.org/10.1126/scitranslmed.3003122

    Article  Google Scholar 

  16. Garza LA, Yang CC, Zhao T, Blatt HB, Lee M, He H, Stanton DC, Carrasco L, Spiegel JH, Tobias JW, Cotsarelis G (2011) Bald scalp in men with androgenetic alopecia retains hair follicle stem cells but lacks CD200-rich and CD34-positive hair follicle progenitor cells. J Clin Invest 121:613–622. https://doi.org/10.1172/JCI44478

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Hamilton JB (1942) Male hormone stimulation is prerequisite and an incitant in common baldness. Am J Anat 71:451–480. https://doi.org/10.1002/aja.1000710306

    Article  Google Scholar 

  18. Hamilton JB (1951) Patterned loss of hair in man; types and incidence. Ann N Y Acad Sci 53:708–728

    Article  PubMed  CAS  Google Scholar 

  19. Hamilton JB (1958) Chapter 16—age, sex, and genetic factors in the regulation of hair growth in man: a comparison of Caucasian and Japanese populations 1. The biology of hair growth. Academic Press, ‎Cambridge, pp 399–433. https://doi.org/10.1016/B978-1-4832-3287-4.50022-2

    Book  Google Scholar 

  20. Heilmann-Heimbach S, Hochfeld LM, Paus R, Nothen MM (2016) Hunting the genes in male-pattern alopecia: how important are they, how close are we and what will they tell us? Exp Dermatol 25:251–257. https://doi.org/10.1111/exd.12965

    Article  PubMed  Google Scholar 

  21. Herman A, Herman AP (2016) Mechanism of action of herbs and their active constituents used in hair loss treatment. Fitoterapia 114:18–25. https://doi.org/10.1016/j.fitote.2016.08.008

    Article  PubMed  CAS  Google Scholar 

  22. Hibberts NA, Howell AE, Randall VA (1998) Balding hair follicle dermal papilla cells contain higher levels of androgen receptors than those from non-balding scalp. J Endocrinol 156:59–65

    Article  PubMed  CAS  Google Scholar 

  23. Hillmer AM, Hanneken S, Ritzmann S, Becker T, Freudenberg J, Brockschmidt FF, Flaquer A, Freudenberg-Hua Y, Jamra RA, Metzen C, Heyn U, Schweiger N, Betz RC, Blaumeiser B, Hampe J, Schreiber S, Schulze TG, Hennies HC, Schumacher J, Propping P, Ruzicka T, Cichon S, Wienker TF, Kruse R, Nothen MM (2005) Genetic variation in the human androgen receptor gene is the major determinant of common early-onset androgenetic alopecia. Am J Hum Genet 77:140–148. https://doi.org/10.1086/431425

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Inui S, Fukuzato Y, Nakajima T, Kurata S, Itami S (2007) Androgen receptor co-activator Hic-5/ARA55 as a molecular regulator of androgen sensitivity in dermal papilla cells of human hair follicles. J Investig Dermatol 127:2302–2306. https://doi.org/10.1038/sj.jid.5700883

    Article  PubMed  CAS  Google Scholar 

  25. Inui S, Fukuzato Y, Nakajima T, Yoshikawa K, Itami S (2002) Androgen-inducible TGF-beta1 from balding dermal papilla cells inhibits epithelial cell growth: a clue to understand paradoxical effects of androgen on human hair growth. FASEB J 16:1967–1969. https://doi.org/10.1096/fj.02-0043fje

    Article  PubMed  CAS  Google Scholar 

  26. Inui S, Fukuzato Y, Nakajima T, Yoshikawa K, Itami S (2003) Identification of androgen-inducible TGF-beta1 derived from dermal papilla cells as a key mediator in androgenetic alopecia. J Investig Dermatol Symp Proc 8:69–71. https://doi.org/10.1046/j.1523-1747.2003.12174.x

    Article  Google Scholar 

  27. Inui S, Itami S (2011) Molecular basis of androgenetic alopecia: from androgen to paracrine mediators through dermal papilla. J Dermatol Sci 61:1–6. https://doi.org/10.1016/j.jdermsci.2010.10.015

    Article  CAS  Google Scholar 

  28. Itami S, Kurata S, Sonoda T, Takayasu S (1995) Interaction between dermal papilla cells and follicular epithelial cells in vitro: effect of androgen. Br J Dermatol 132:527–532

    PubMed  CAS  Google Scholar 

  29. Jain R, De-Eknamkul W (2014) Potential targets in the discovery of new hair growth promoters for androgenic alopecia. Expert Opin Ther Targets 18:787–806. https://doi.org/10.1517/14728222.2014.922956

    Article  PubMed  CAS  Google Scholar 

  30. Jo SJ, Shin H, Park YW, Paik SH, Park WS, Jeong YS, Shin HJ, Kwon O (2014) Topical valproic acid increases the hair count in male patients with androgenetic alopecia: a randomized, comparative, clinical feasibility study using phototrichogram analysis. J Dermatol 41:285–291. https://doi.org/10.1111/1346-8138.12422

    Article  PubMed  CAS  Google Scholar 

  31. Kazemi-Esfarjani P, Trifiro MA, Pinsky L (1995) Evidence for a repressive function of the long polyglutamine tract in the human androgen receptor: possible pathogenetic relevance for the (CAG)n-expanded neuronopathies. Hum Mol Genet 4:523–527

    Article  PubMed  CAS  Google Scholar 

  32. Kelly Y, Blanco A, Tosti A (2016) Androgenetic alopecia: an update of treatment options. Drugs 76:1349–1364. https://doi.org/10.1007/s40265-016-0629-5

    Article  PubMed  CAS  Google Scholar 

  33. Kim D, Garza LA (2017) The negative regulator CXXC5: making WNT look a little less dishevelled. J Investig Dermatol 137:2248–2250. https://doi.org/10.1016/j.jid.2017.07.826

    Article  PubMed  CAS  Google Scholar 

  34. Kimura-Ueki M, Oda Y, Oki J, Komi-Kuramochi A, Honda E, Asada M, Suzuki M, Imamura T (2012) Hair cycle resting phase is regulated by cyclic epithelial FGF18 signaling. J Investig Dermatol 132:1338–1345. https://doi.org/10.1038/jid.2011.490

    Article  PubMed  CAS  Google Scholar 

  35. Kishimoto J, Burgeson RE, Morgan BA (2000) Wnt signaling maintains the hair-inducing activity of the dermal papilla. Genes Dev 14:1181–1185

    PubMed  PubMed Central  CAS  Google Scholar 

  36. Kitagawa T, Matsuda K, Inui S, Takenaka H, Katoh N, Itami S, Kishimoto S, Kawata M (2009) Keratinocyte growth inhibition through the modification of Wnt signaling by androgen in balding dermal papilla cells. J Clin Endocrinol Metab 94:1288–1294. https://doi.org/10.1210/jc.2008-1053

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Klokk TI, Kurys P, Elbi C, Nagaich AK, Hendarwanto A, Slagsvold T, Chang C-Y, Hager GL, Saatcioglu F (2007) Ligand-specific dynamics of the androgen receptor at its response element in living cells. Mol Cell Biol 27:1823–1843. https://doi.org/10.1128/MCB.01297-06

    Article  PubMed  CAS  Google Scholar 

  38. Krieger K, Millar SE, Mikuda N, Krahn I, Kloepper JE, Bertolini M, Scheidereit C, Paus R, Schmidt-Ullrich R (2017) NF-κB participates in mouse hair cycle control and plays distinct roles in the various pelage hair follicle types. J Investig Dermatol. https://doi.org/10.1016/j.jid.2017.08.042

    Article  PubMed  Google Scholar 

  39. Kucerova R, Bienova M, Kral M, Bouchal J, Trtkova KS, Burdova A, Student V, Kolar Z (2015) Androgenetic alopecia and polymorphism of the androgen receptor gene (SNP rs6152) in patients with benign prostate hyperplasia or prostate cancer. J Eur Acad Dermatol Venereol 29:91–96. https://doi.org/10.1111/jdv.12468

    Article  PubMed  CAS  Google Scholar 

  40. Kwack MH, Ahn JS, Kim MK, Kim JC, Sung YK (2012) Dihydrotestosterone-inducible IL-6 inhibits elongation of human hair shafts by suppressing matrix cell proliferation and promotes regression of hair follicles in mice. J Investig Dermatol 132:43–49. https://doi.org/10.1038/jid.2011.274

    Article  PubMed  CAS  Google Scholar 

  41. Kwack MH, Kim MK, Kim JC, Sung YK (2012) Dickkopf 1 promotes regression of hair follicles. J Investig Dermatol 132:1554–1560. https://doi.org/10.1038/jid.2012.24

    Article  PubMed  CAS  Google Scholar 

  42. Kwack MH, Sung YK, Chung EJ, Im SU, Ahn JS, Kim MK, Kim JC (2008) Dihydrotestosterone-inducible dickkopf 1 from balding dermal papilla cells causes apoptosis in follicular keratinocytes. J Investig Dermatol 128:262–269. https://doi.org/10.1038/sj.jid.5700999

    Article  PubMed  CAS  Google Scholar 

  43. Lai J-J, Chang P, Lai K-P, Chen L, Chang C (2012) The role of androgen and androgen receptor in the skin-related disorders. Arch Dermatol Res 304:499–510. https://doi.org/10.1007/s00403-012-1265-x

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  44. Lee P, Zhu C-C, Sadick NS, Diwan AH, Zhang PS, Liu JS, Prieto VG (2005) Expression of androgen receptor coactivator ARA70/ELE1 in androgenic alopecia. J Cutan Pathol 32:567–571. https://doi.org/10.1111/j.0303-6987.2005.00397.x

    Article  PubMed  Google Scholar 

  45. Lee S-H, Seo SH, Lee D-H, Pi L-Q, Lee W-S, Choi K-Y (2017) Targeting of CXXC5 by a competing peptide stimulates hair regrowth and wound-induced hair neogenesis. J Investig Dermatol 137:2260–2269. https://doi.org/10.1016/j.jid.2017.04.038

    Article  PubMed  CAS  Google Scholar 

  46. Lee S-H, Yoon J, Shin SH, Zahoor M, Kim HJ, Park PJ, Park W-S, Min DS, Kim H-Y, Choi K-Y (2012) Valproic acid induces hair regeneration in murine model and activates alkaline phosphatase activity in human dermal papilla cells. PLOS One 7:e34152. https://doi.org/10.1371/journal.pone.0034152

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Lei M-X, Chuong C-M, Widelitz RB (2013) Tuning Wnt signals for more or fewer hairs. J Investig Dermatol 133:7–9. https://doi.org/10.1038/jid.2012.446

    Article  PubMed  Google Scholar 

  48. Lei M, Yang L, Chuong C-M (2017) Getting to the core of the dermal papilla. J Investig Dermatol 137:2250–2253. https://doi.org/10.1016/j.jid.2017.07.824

    Article  PubMed  CAS  Google Scholar 

  49. Leiros GJ, Attorresi AI, Balana ME (2012) Hair follicle stem cell differentiation is inhibited through cross-talk between Wnt/beta-catenin and androgen signalling in dermal papilla cells from patients with androgenetic alopecia. Br J Dermatol 166:1035–1042. https://doi.org/10.1111/j.1365-2133.2012.10856.x

    Article  PubMed  CAS  Google Scholar 

  50. Leirós GJ, Ceruti JM, Castellanos ML, Kusinsky AG, Balañá ME (2017) Androgens modify Wnt agonists/antagonists expression balance in dermal papilla cells preventing hair follicle stem cell differentiation in androgenetic alopecia. Mol Cell Endocrinol 439:26–34. https://doi.org/10.1016/j.mce.2016.10.018

    Article  PubMed  CAS  Google Scholar 

  51. Li Vivian SW, Ng Ser S, Boersema Paul J, Low Teck Y, Karthaus Wouter R, Gerlach Jan P, Mohammed S, Heck Albert JR, Maurice Madelon M, Mahmoudi T, Clevers H (2012) Wnt signaling through inhibition of β-catenin degradation in an intact axin1 complex. Cell 149:1245–1256. https://doi.org/10.1016/j.cell.2012.05.002

    Article  PubMed  CAS  Google Scholar 

  52. Li Y-H, Zhang K, Yang K, Ye J-X, Xing Y-Z, Guo H-Y, Deng F, Lian X-H, Yang T (2013) Adenovirus-mediated Wnt10b overexpression induces hair follicle regeneration. J Investig Dermatol 133:42–48. https://doi.org/10.1038/jid.2012.235

    Article  PubMed  CAS  Google Scholar 

  53. Masumi Inaba YI (1996) Androgenetic alopecia. In: Androgenetic alopecia: modern concepts of pathogenesis and treatment. Springer, Tokyo, pp 161–168. https://doi.org/10.1007/978-4-431-67038-4_17

    Chapter  Google Scholar 

  54. Meidan VM, Touitou E (2001) Treatments for androgenetic alopecia and alopecia areata: current options and future prospects. Drugs. https://doi.org/10.2165/00003495-200161010-00006

    Article  PubMed  Google Scholar 

  55. Nelson AM, Garza LA (2015) Bad hair day: testosterone and Wnts. J Investig Dermatol 135:2567–2569. https://doi.org/10.1038/jid.2015.304

    Article  PubMed  CAS  Google Scholar 

  56. Nelson AM, Loy DE, Lawson JA, Katseff AS, Fitzgerald GA, Garza LA (2013) Prostaglandin D2 inhibits wound-induced hair follicle neogenesis through the receptor, Gpr44. J Invest Dermatol 133:881–889. https://doi.org/10.1038/jid.2012.398

    Article  PubMed  CAS  Google Scholar 

  57. Nusse R, Clevers H (2017) Wnt/β-catenin signaling, disease, and emerging therapeutic modalities. Cell 169:985–999. https://doi.org/10.1016/j.cell.2017.05.016

    Article  PubMed  CAS  Google Scholar 

  58. Nuwaihyd R, Redler S, Heilmann S, Drichel D, Wolf S, Birch P, Dobson K, Lutz G, Giehl KA, Kruse R, Tazi-Ahnini R, Hanneken S, Böhm M, Miesel A, Fischer T, Wolff H, Becker T, Garcia-Bartels N, Blume-Peytavi U, Nöthen MM, Messenger AG, Betz RC (2014) Investigation of four novel male androgenetic alopecia susceptibility loci: no association with female pattern hair loss. Arch Dermatol Res 306:413–418. https://doi.org/10.1007/s00403-013-1436-4

    Article  PubMed  CAS  Google Scholar 

  59. Olsen EA, Hordinsky M, Whiting D, Stough D, Hobbs S, Ellis ML, Wilson T, Rittmaster RS (2006) The importance of dual 5α-reductase inhibition in the treatment of male pattern hair loss: results of a randomized placebo-controlled study of dutasteride versus finasteride. J Am Acad Dermatol 55:1014–1023. https://doi.org/10.1016/j.jaad.2006.05.007

    Article  PubMed  Google Scholar 

  60. Park P-J, Moon B-S, Lee S-H, Kim S-N, Kim A-R, Kim H-J, Park W-S, Choi K-Y, Cho E-G, Lee TR (2012) Hair growth-promoting effect of Aconiti Ciliare Tuber extract mediated by the activation of Wnt/β-catenin signaling. Life Sci 91:935–943. https://doi.org/10.1016/j.lfs.2012.09.008

    Article  PubMed  CAS  Google Scholar 

  61. Rabbani P, Takeo M, Chou W, Myung P, Bosenberg M, Chin L, Taketo MM, Ito M (2011) Coordinated activation of Wnt in epithelial and melanocyte stem cells initiates pigmented hair regeneration. Cell 145:941–955. https://doi.org/10.1016/j.cell.2011.05.004

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Randall VA (2008) Androgens and hair growth. Dermatol Ther 21:314–328. https://doi.org/10.1111/j.1529-8019.2008.00214.x

    Article  PubMed  Google Scholar 

  63. Randall VA (2010) Molecular basis of androgenetic alopecia. In: Trüeb RM, Tobin DJ (eds) Aging hair. Springer, Berlin, pp 9–24. https://doi.org/10.1007/978-3-642-02636-2_2

    Chapter  Google Scholar 

  64. Randall VA, Hibberts NA, Thornton MJ, Hamada K, Merrick AE, Kato S, Jenner TJ, De Oliveira I, Messenger AG (2000) The hair follicle: a paradoxical androgen target organ. Hormone Res 54:243–250

    Article  PubMed  CAS  Google Scholar 

  65. Rishikaysh P, Dev K, Diaz D, Qureshi WMS, Filip S, Mokry J (2014) Signaling involved in hair follicle morphogenesis and development. Int J Mol Sci 15:1647–1670. https://doi.org/10.3390/ijms15011647

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Sanke S, Chander R, Jain A, Garg T, Yadav P (2016) A comparison of the hormonal profile of early androgenetic alopecia in men with the phenotypic equivalent of polycystic ovarian syndrome in women. JAMA Dermatol 152:986–991. https://doi.org/10.1001/jamadermatol.2016.1776

    Article  PubMed  Google Scholar 

  67. Sasaki M, Karube A, Karube Y, Watari M, Sakuragi N, Fujimoto S, Dahiya R (2005) GGC and StuI polymorphism on the androgen receptor gene in endometrial cancer patients. Biochem Biophys Res Commun 329:100–104. https://doi.org/10.1016/j.bbrc.2005.01.104

    Article  PubMed  CAS  Google Scholar 

  68. Sawaya ME, Shalita AR (1998) Androgen receptor polymorphisms (CAG repeat lengths) in androgenetic alopecia, hirsutism, and acne. J Cutan Med Surg 3:9–15. https://doi.org/10.1177/120347549800300103

    Article  PubMed  CAS  Google Scholar 

  69. Schweiger ES, Boychenko O, Bernstein RM (2010) Update on the pathogenesis, genetics and medical treatment of patterned hair loss. JDD 9:1412–1419

    PubMed  Google Scholar 

  70. Sinclair R (1998) Male pattern androgenetic alopecia. BMJ 317:865–869

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  71. Sinclair R, Greenland KJ, Egmond S, Hoedemaker C, Chapman A, Zajac JD (2007) Men with Kennedy disease have a reduced risk of androgenetic alopecia. Br J Dermatol 157:290–294. https://doi.org/10.1111/j.1365-2133.2007.08026.x

    Article  PubMed  CAS  Google Scholar 

  72. Smith AA, Li J, Liu B, Hunter D, Pyles M, Gillette M, Dhamdhere GR, Abo A, Oro A, Helms JA (2016) Activating hair follicle stem cells via R-spondin2 to stimulate hair growth. J Investig Dermatol 136:1549–1558. https://doi.org/10.1016/j.jid.2016.01.041

    Article  PubMed  CAS  Google Scholar 

  73. Tobin DJ (2005) Biology of hair. The biogenesis and growth of human hair. In: Tobin DJ (ed) Hair in toxicology: an important bio-monitor. The Royal Society of Chemistry, London, pp 1–33. https://doi.org/10.1039/9781847552518-00001

    Chapter  Google Scholar 

  74. Tobin DJ (2010) Gerontobiology of the hair follicle. In: Trüeb RM, Tobin DJ (eds) Aging hair. Springer, Berlin, pp 1–8. https://doi.org/10.1007/978-3-642-02636-2_1

    Chapter  Google Scholar 

  75. Vano-Galvan S, Camacho F (2017) New treatments for hair loss. Actas Dermo Sifiliogr 108:221–228. https://doi.org/10.1016/j.ad.2016.11.010

    Article  CAS  Google Scholar 

  76. Wilma F, Bergfeld, Mulinari-Brenner F (2009) Hair disorders. http://www.clevelandclinicmeded.com/medicalpubs/diseasemanagement/dermatology/hair-disorders/. Accessed 8 Feb 2018

  77. Wu M, Yu Q, Li Q (2016) Differences in reproductive toxicology between alopecia drugs: an analysis on adverse events among female and male cases. Oncotarget 7:82074–82084. https://doi.org/10.18632/oncotarget.12617

    Article  PubMed  PubMed Central  Google Scholar 

  78. Yamauchi K, Kurosaka A (2009) Inhibition of glycogen synthase kinase-3 enhances the expression of alkaline phosphatase and insulin-like growth factor-1 in human primary dermal papilla cell culture and maintains mouse hair bulbs in organ culture. Arch Dermatol Res 301:357–365. https://doi.org/10.1007/s00403-009-0929-7

    Article  PubMed  CAS  Google Scholar 

  79. Zhu H, Ma H, Ni H, Ma X-H, Mills N, Yang Z-M (2004) Expression and regulation of lipocalin-type prostaglandin D synthase in rat testis and epididymis1. Biol Reprod 70:1088–1095. https://doi.org/10.1095/biolreprod.103.022079

    Article  PubMed  CAS  Google Scholar 

  80. Zhuo FL, Xu W, Wang L, Wu Y, Xu ZL, Zhao JY (2012) Androgen receptor gene polymorphisms and risk for androgenetic alopecia: a meta-analysis. Clin Exp Dermatol 37:104–111. https://doi.org/10.1111/j.1365-2230.2011.04186.x

    Article  PubMed  CAS  Google Scholar 

  81. Zimber MP, Ziering C, Zeigler F, Hubka M, Mansbridge JN, Baumgartner M, Hubka K, Kellar R, Perez-Meza D, Sadick N, Naughton GK (2011) Hair regrowth following a wnt- and follistatin-containing treatment: safety and efficacy in a first-in-man phase 1 clinical trial. J Drugs Dermatol 10:1308–1312

    PubMed  CAS  Google Scholar 

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Acknowledgements

The authors acknowledge Vellore Institute of Technology, Vellore, India for providing the computational facilities. Mr. A. Premanand is a Ph.D. Scholar at Vellore Institute of Technology and is supported by Junior Research Fellowship provided by the Council of Scientific and Industrial Research, New Delhi, India (Award No: 09/844(0045)/2017-EMR-1).

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  1. Department of Integrative Biology, School of Bio Sciences and Technology, Vellore Institute of Technology, Vellore, 632014, Tamil Nadu, India

    A. Premanand & B. Reena Rajkumari

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Premanand, A., Reena Rajkumari, B. Androgen modulation of Wnt/β-catenin signaling in androgenetic alopecia. Arch Dermatol Res 310, 391–399 (2018). https://doi.org/10.1007/s00403-018-1826-8

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  • DOI: https://doi.org/10.1007/s00403-018-1826-8

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