Advertisement

Archives of Dermatological Research

, Volume 310, Issue 5, pp 391–399 | Cite as

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

Review

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.

Keywords

Androgenetic alopecia Androgen Androgen receptor Dihydrotestosterone Dermal papilla Wnt β-catenin 

Notes

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).

Funding

Nil.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

No original data are collected for this review, and hence, this study did not meet the criteria for ethical approval and formal consent is not required.

References

  1. 1.
    Alonso L, Fuchs E (2006) The hair cycle. J Cell Sci 119:391–393.  https://doi.org/10.1242/jcs.02793 CrossRefPubMedGoogle Scholar
  2. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 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 CrossRefPubMedGoogle Scholar
  4. 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 CrossRefPubMedGoogle Scholar
  5. 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 22:3181–3186CrossRefPubMedPubMedCentralGoogle Scholar
  6. 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 CrossRefPubMedGoogle Scholar
  7. 7.
    Cranwell W, Sinclair R (2016) Male androgenetic alopecia. Endotext. MDText.com, Inc, South DartmouthGoogle Scholar
  8. 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 CrossRefPubMedGoogle Scholar
  9. 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 CrossRefPubMedGoogle Scholar
  10. 10.
    Dinh QQ, Sinclair R (2007) Female pattern hair loss: current treatment concepts. Clin Interv Aging 2:189–199PubMedPubMedCentralGoogle Scholar
  11. 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 doiCrossRefGoogle Scholar
  12. 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 CrossRefPubMedGoogle Scholar
  13. 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 CrossRefPubMedGoogle Scholar
  14. 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 CrossRefPubMedGoogle Scholar
  15. 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 CrossRefGoogle Scholar
  16. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  17. 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 CrossRefGoogle Scholar
  18. 18.
    Hamilton JB (1951) Patterned loss of hair in man; types and incidence. Ann N Y Acad Sci 53:708–728CrossRefPubMedGoogle Scholar
  19. 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 Google Scholar
  20. 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 CrossRefPubMedGoogle Scholar
  21. 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 CrossRefPubMedGoogle Scholar
  22. 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 156:59–65CrossRefPubMedGoogle Scholar
  23. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 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 CrossRefPubMedGoogle Scholar
  25. 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 CrossRefPubMedGoogle Scholar
  26. 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 CrossRefGoogle Scholar
  27. 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 CrossRefGoogle Scholar
  28. 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 132:527–532PubMedGoogle Scholar
  29. 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 CrossRefPubMedGoogle Scholar
  30. 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 CrossRefPubMedGoogle Scholar
  31. 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 4:523–527CrossRefPubMedGoogle Scholar
  32. 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 CrossRefPubMedGoogle Scholar
  33. 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 CrossRefPubMedGoogle Scholar
  34. 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 CrossRefPubMedGoogle Scholar
  35. 35.
    Kishimoto J, Burgeson RE, Morgan BA (2000) Wnt signaling maintains the hair-inducing activity of the dermal papilla. Genes Dev 14:1181–1185PubMedPubMedCentralGoogle Scholar
  36. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 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 CrossRefPubMedGoogle Scholar
  38. 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 Google Scholar
  39. 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 CrossRefPubMedGoogle Scholar
  40. 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 CrossRefPubMedGoogle Scholar
  41. 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 CrossRefPubMedGoogle Scholar
  42. 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 CrossRefPubMedGoogle Scholar
  43. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  44. 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 CrossRefPubMedGoogle Scholar
  45. 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 CrossRefPubMedGoogle Scholar
  46. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  47. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  48. 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 CrossRefPubMedGoogle Scholar
  49. 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 CrossRefPubMedGoogle Scholar
  50. 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 CrossRefPubMedGoogle Scholar
  51. 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 CrossRefPubMedGoogle Scholar
  52. 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 CrossRefPubMedGoogle Scholar
  53. 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 CrossRefGoogle Scholar
  54. 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 PubMedGoogle Scholar
  55. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  56. 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 CrossRefPubMedGoogle Scholar
  57. 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 CrossRefPubMedGoogle Scholar
  58. 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 CrossRefPubMedGoogle Scholar
  59. 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 CrossRefPubMedGoogle Scholar
  60. 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 CrossRefPubMedGoogle Scholar
  61. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Randall VA (2008) Androgens and hair growth. Dermatol Ther 21:314–328.  https://doi.org/10.1111/j.1529-8019.2008.00214.x CrossRefPubMedGoogle Scholar
  63. 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 CrossRefGoogle Scholar
  64. 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 54:243–250CrossRefPubMedGoogle Scholar
  65. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  66. 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 CrossRefPubMedGoogle Scholar
  67. 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 CrossRefPubMedGoogle Scholar
  68. 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 CrossRefPubMedGoogle Scholar
  69. 69.
    Schweiger ES, Boychenko O, Bernstein RM (2010) Update on the pathogenesis, genetics and medical treatment of patterned hair loss. JDD 9:1412–1419PubMedGoogle Scholar
  70. 70.
    Sinclair R (1998) Male pattern androgenetic alopecia. BMJ 317:865–869CrossRefPubMedPubMedCentralGoogle Scholar
  71. 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 CrossRefPubMedGoogle Scholar
  72. 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 CrossRefPubMedGoogle Scholar
  73. 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 CrossRefGoogle Scholar
  74. 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 Google Scholar
  75. 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 CrossRefGoogle Scholar
  76. 76.
    Wilma F, Bergfeld, Mulinari-Brenner F (2009) Hair disorders. http://www.clevelandclinicmeded.com/medicalpubs/diseasemanagement/dermatology/hair-disorders/. Accessed 8 Feb 2018
  77. 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 PubMedPubMedCentralGoogle Scholar
  78. 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 CrossRefPubMedGoogle Scholar
  79. 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 CrossRefPubMedGoogle Scholar
  80. 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 CrossRefPubMedGoogle Scholar
  81. 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 10:1308–1312PubMedGoogle Scholar

Related articles recently published in Archives of Dermatological Research (selected by the journal’s editorial staff):

  1. 82.
    Ardigo M, Agozzino M, Franceschini C, Donadio C, Abraham LS, Barbieri L, Sperduti I, Berardesca E, Gonzalez S (2016) Reflectance confocal microscopy for scarring and non-scarring alopecia real-time assessment. Arch Dermatol Res 308:309–318CrossRefPubMedGoogle Scholar
  2. 83.
    Fortes C, Mastroeni S, Mannooranparampil T, Abeni D, Panebianco A (2018) Mediterranean diet: fresh herbs and fresh vegetables decrease the risk of androgenetic alopecia in males. Arch Dermatol Res 310:71–76CrossRefPubMedGoogle Scholar
  3. 84.
    Woo H, Lee S, Kim S, Park D, Jung E (2017) Effect of sinapic acid on hair growth promoting in human hair follicle dermal papilla cells via Akt activation. Arch Dermatol Res 309:381–388CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Integrative Biology, School of Bio Sciences and TechnologyVellore Institute of TechnologyVelloreIndia

Personalised recommendations