Cited by 57Hair Growth and Disordersdental development and anomaliesSkin and Cellular Biology Research

To grow or not to grow: Hair morphogenesis and human genetic hair disorders

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Duverger, Olivier, Morasso, Maria I.·2014·Seminars in Cell & Developmental Biology

Abstract

Mouse models have greatly helped in elucidating the molecular mechanisms involved in hair formation and regeneration. Recent publications have reviewed the genes involved in mouse hair development based on the phenotype of transgenic, knockout and mutant animal models. While much of this information has been instrumental in determining molecular aspects of human hair development and cycling, mice exhibit a specific pattern of hair morphogenesis and hair distribution throughout the body that cannot be directly correlated to human hair. In this mini-review, we discuss specific aspects of human hair follicle development and present an up-to-date summary of human genetic disorders associated with abnormalities in hair follicle morphogenesis, structure or regeneration.

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  • The in vitro hair follicle developmental timeline corresponds well to that of human fetal hair follicle development in vivo: the hair placode, germ, peg, and follicle differentiation stages occur, mostly, between 80 and 170 days (12-25 gestational weeks), where the full anagen stage hair follicles develop by day 126 (18 gestational weeks).

    “The in vitro hair follicle developmental timeline corresponds well to that of human fetal hair follicle development in vivo: the hair placode, germ, peg, and follicle differentiation stages occur, mostly, between 80 and 170 days (12–25 gestational weeks), where the full anagen stage hair follicles develop by day 126 (18 gestational weeks; Fig. 1)”

    From Generation and characterization of hair-bearing skin organoids from human pluripotent stem cells (2022) · cites this paper as [37]

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  1. [1]Lee J Tumbar T Hairy tale of signaling in hair follicle development and cycling. Semin Cell Dev Biol 2012 23 906 16 22939761 PMC3496046
  2. [2]Sennett R Rendl M Mesenchymal-epithelial interactions during hair follicle morphogenesis and cycling. Semin Cell Dev Biol 2012 23 917 27 22960356 PMC3496047
  3. [3]Ohyama M Vogel JC Amagai M Gene ontology analysis of human hair follicle bulge molecular signature. J Dermatol Sci 2007 45 147 50 17071058
  4. [4]Cotsarelis G Epithelial stem cells: a folliculocentric view. J Invest Dermatol 2006 126 1459 68 16778814
  5. [5]Jaks V Kasper M Toftgard R The hair follicle – a stem cell zoo. Exp Cell Res 2010 316 1422 8 20338163
  6. [6]Langbein L Schweizer J Keratins of the human hair follicle. Int Rev Cytol 2005 243 1 78 15797458
  7. [8]Muller-Rover S Handjiski B van der Veen C Eichmuller S Foitzik K McKay IA A comprehensive guide for the accurate classification of murine hair follicles in distinct hair cycle stages. J Invest Dermatol 2001 117 3 15 11442744
  8. [9]Krause K Foitzik K Biology of the hair follicle: the basics. Semin Cutan Med Surg 2006 25 2 10 16616298
  9. [10]Ahmad W Faiyaz ul Haque M Brancolini V Tsou HC ul Haque S Lam H Alopecia universalis associated with a mutation in the human hairless gene. Science 1998 279 720 4 9445480
  10. [11]Sprecher E Lestringant GG Szargel R Bergman R Labay V Frossard PM Atrichia with papular lesions resulting from a nonsense mutation within the human hairless gene. J Invest Dermatol 1999 113 687 90 10504459
  11. [12]Wen Y Liu Y Xu Y Zhao Y Hua R Wang K Loss-of-function mutations of an inhibitory upstream ORF in the human hairless transcript cause Marie Unna hereditary hypotrichosis. Nat Genet 2009 41 228 33 19122663
  12. [13]Mecklenburg L Nakamura M Sundberg JP Paus R The nude mouse skin pheno-type: the role of Foxn1 in hair follicle development and cycling. Exp Mol Pathol 2001 71 171 8 11599924
  13. [14]Frank J Pignata C Panteleyev AA Prowse DM Baden H Weiner L Exposing the human nude phenotype. Nature 1999 398 473 4 10206641
  14. [15]Clifton-Bligh RJ Wentworth JM Heinz P Crisp MS John R Lazarus JH Mutation of the gene encoding human TTF-2 associated with thyroid agenesis, cleft palate and choanal atresia. Nat Genet 1998 19 399 401 9697705
  15. [16]Kayserili H Uz E Niessen C Vargel I Alanay Y Tuncbilek G ALX4 dys-function disrupts craniofacial and epidermal development. Hum Mol Genet 2009 18 4357 66 19692347
  16. [17]Godwin AR Capecchi MR Hoxc13 mutant mice lack external hair. Genes Dev 1998 12 11 20 9420327 PMC316401
  17. [19]Hughes MR Malloy PJ Kieback DG Kesterson RA Pike JW Feldman D Point mutations in the human vitamin D receptor gene associated with hypocalcemic rickets. Science 1988 242 1702 5 2849209
  18. [20]Oeffner F Fischer G Happle R Konig A Betz RC Bornholdt D IFAP syndrome is caused by deficiency in MBTPS2, an intramembrane zinc metalloprotease essential for cholesterol homeostasis and ER stress response. Am J Hum Genet 2009 84 459 67 19361614 PMC2667992
  19. [21]Aten E Brasz LC Bornholdt D Hooijkaas IB Porteous ME Sybert VP Keratosis Follicularis Spinulosa Decalvans is caused by mutations in MBTPS2. Hum Mutat 2010 31 1125 33 20672378
  20. [22]Irrthum A Devriendt K Chitayat D Matthijs G Glade C Steijlen PM Mutations in the transcription factor gene SOX18 underlie recessive and dominant forms of hypotrichosis-lymphedema-telangiectasia. Am J Hum Genet 2003 72 1470 8 12740761 PMC1180307
  21. [23]Momeni P Glockner G Schmidt O von Holtum D Albrecht B Gillessen-Kaesbach G Mutations in a new gene, encoding a zinc-finger protein, cause tricho-rhino-phalangeal syndrome type I. Nat Genet 2000 24 71 4 10615131
  22. [24]Ludecke HJ Schaper J Meinecke P Momeni P Gross S von Holtum D Genotypic and phenotypic spectrum in tricho-rhino-phalangeal syndrome types I and III. Am J Hum Genet 2001 68 81 91 11112658 PMC1234936
  23. [25]Celli J Duijf P Hamel BC Bamshad M Kramer B Smits AP Heterozygous germline mutations in the p53 homolog p63 are the cause of EEC syndrome. Cell 1999 99 143 53 10535733
  24. [26]McGrath JA Duijf PH Doetsch V Irvine AD de Waal R Vanmolkot KR Hay-Wells syndrome is caused by heterozygous missense mutations in the SAM domain of p63. Hum Mol Genet 2001 10 221 9 11159940
  25. [27]Kantaputra PN Hamada T Kumchai T McGrath JA Heterozygous mutation in the SAM domain of p63 underlies Rapp-Hodgkin ectodermal dysplasia. J Dent Res 2003 82 433 7 12766194
  26. [28]Amiel J Bougeard G Francannet C Raclin V Munnich A Lyonnet S TP63 gene mutation in ADULT syndrome. Eur J Hum Genet 2001 9 642 5 11528512
  27. [30]Monreal AW Ferguson BM Headon DJ Street SL Overbeek PA Zonana J Mutations in the human homologue of mouse dl cause autosomal recessive and dominant hypohidrotic ectodermal dysplasia. Nat Genet 1999 22 366 9 10431241
  28. [33]Zonana J Elder ME Schneider LC Orlow SJ Moss C Golabi M A novel X-linked disorder of immune deficiency and hypohidrotic ectodermal dysplasia is allelic to incontinentia pigmenti and due to mutations in IKK-gamma (NEMO). Am J Hum Genet 2000 67 1555 62 11047757 PMC1287930
  29. [34]Smahi A Courtois G Vabres P Yamaoka S Heuertz S Munnich A Genomic rearrangement in NEMO impairs NF-kappaB activation and is a cause of incontinentia pigmenti. The International Incontinentia Pigmenti (IP) Consortium. Nature 2000 405 466 72 10839543
  30. [35]Adaimy L Chouery E Megarbane H Mroueh S Delague V Nicolas E Mutation in WNT10A is associated with an autosomal recessive ectodermal dysplasia: the odonto-onycho-dermal dysplasia. Am J Hum Genet 2007 81 821 8 17847007 PMC1973944
  31. [37]Shimomura Y Agalliu D Vonica A Luria V Wajid M Baumer A APCDD1 is a novel Wnt inhibitor mutated in hereditary hypotrichosis simplex. Nature 2010 464 1043 7 20393562 PMC3046868
  32. [38]Kljuic A Bazzi H Sundberg JP Martinez-Mir A O'Shaughnessy R Mahoney MG Desmoglein 4 in hair follicle differentiation and epidermal adhesion: evidence from inherited hypotrichosis and acquired pemphigus vulgaris. Cell 2003 113 249 60 12705872
  33. [39]Ayub M Basit S Jelani M Ur Rehman F Iqbal M Yasinzai M A homozygous nonsense mutation in the human desmocollin-3 (DSC3) gene underlies hereditary hypotrichosis and recurrent skin vesicles. Am J Hum Genet 2009 85 515 20 19765682 PMC2756559
  34. [40]McGrath JA McMillan JR Shemanko CS Runswick SK Leigh IM Lane EB Mutations in the plakophilin 1 gene result in ectodermal dysplasia/skin fragility syndrome. Nat Genet 1997 17 240 4 9326952
  35. [41]Levy-Nissenbaum E Betz RC Frydman M Simon M Lahat H Bakhan T Hypotrichosis simplex of the scalp is associated with nonsense mutations in CDSN encoding corneodesmosin. Nat Genet 2003 34 151 3 12754508
  36. [42]Blaydon DC Biancheri P Di WL Plagnol V Cabral RM Brooke MA Inflammatory skin and bowel disease linked to ADAM17 deletion. N Engl J Med 2011 365 1502 8 22010916
  37. [43]Basel-Vanagaite L Attia R Ishida-Yamamoto A Rainshtein L Ben Amitai D Lurie R Autosomal recessive ichthyosis with hypotrichosis caused by a mutation in ST14, encoding type II transmembrane serine protease matriptase. Am J Hum Genet 2007 80 467 77 17273967 PMC1821100
  38. [44]Chavanas S Bodemer C Rochat A Hamel-Teillac D Ali M Irvine AD Mutations in SPINK5, encoding a serine protease inhibitor, cause Netherton syndrome. Nat Genet 2000 25 141 2 10835624
  39. [45]Gu LH Coulombe PA Keratin function in skin epithelia: a broadening palette with surprising shades. Curr Opin Cell Biol 2007 19 13 23 17178453
  40. [46]Wasif N Naqvi SK Basit S Ali N Ansar M Ahmad W Novel mutations in the keratin-74 (KRT74) gene underlie autosomal dominant woolly hair/hypotrichosis in Pakistani families. Hum Genet 2011 129 419 24 21188418
  41. [47]Sprecher E Bergman R Richard G Lurie R Shalev S Petronius D Hypotrichosis with juvenile macular dystrophy is caused by a mutation in CDH3, encoding P-cadherin. Nat Genet 2001 29 134 6 11544476
  42. [48]Kjaer KW Hansen L Schwabe GC Marques-de-Faria AP Eiberg H Mundlos S Distinct CDH3 mutations cause ectodermal dysplasia, ectrodactyly, macular dystrophy (EEM syndrome). J Med Genet 2005 42 292 8 15805154 PMC1736041
  43. [49]Hadj-Rabia S Baala L Vabres P Hamel-Teillac D Jacquemin E Fabre M Claudin-1 gene mutations in neonatal sclerosing cholangitis associated with ichthyosis: a tight junction disease. Gastroenterology 2004 127 1386 90 15521008
  44. [50]Suzuki K Hu D Bustos T Zlotogora J Richieri-Costa A Helms JA Mutations of PVRL1, encoding a cell–cell adhesion molecule/herpesvirus receptor, in cleft lip/palate-ectodermal dysplasia. Nat Genet 2000 25 427 30 10932188
  45. [51]Stranecky V Hoischen A Hartmannova H Zaki MS Chaudhary A Zudaire E Mutations in ANTXR1 cause GAPO syndrome. Am J Hum Genet 2013 92 792 9 23602711 PMC3644626
  46. [52]Lamartine J Munhoz Essenfelder G Kibar Z Lanneluc I Callouet E Laoudj D Mutations in GJB6 cause hidrotic ectodermal dysplasia. Nat Genet 2000 26 142 4 11017065
  47. [53]Kazantseva A Goltsov A Zinchenko R Grigorenko AP Abrukova AV Moliaka YK Human hair growth deficiency is linked to a genetic defect in the phospholipase gene LIPH. Science 2006 314 982 5 17095700
  48. [54]Pasternack SM von Kugelgen I Al Aboud K Lee YA Ruschendorf F Voss K G protein-coupled receptor P2Y5 and its ligand LPA are involved in maintenance of human hair growth. Nat Genet 2008 40 329 34 18297070
  49. [55]Shimomura Y Wajid M Ishii Y Shapiro L Petukhova L Gordon D Disruption of P2RY5, an orphan G protein-coupled receptor, underlies autosomal recessive woolly hair. Nat Genet 2008 40 335 9 18297072
  50. [56]Nousbeck J Spiegel R Ishida-Yamamoto A Indelman M Shani-Adir A Adir N Alopecia, neurological defects, and endocrinopathy syndrome caused by decreased expression of RBM28, a nucleolar protein associated with ribosome biogenesis. Am J Hum Genet 2008 82 1114 21 18439547 PMC2427309
  51. [57]Pasternack SM Refke M Paknia E Hennies HC Franz T Schafer N Mutations in SNRPE, which encodes a core protein of the spliceosome, cause autosomal-dominant hypotrichosis simplex. Am J Hum Genet 2013 92 81 7 23246290 PMC3542472
  52. [58]Alazami AM Al-Saif A Al-Semari A Bohlega S Zlitni S Alzahrani F Mutations in C2orf37, encoding a nucleolar protein, cause hypogonadism, alopecia, diabetes mellitus, mental retardation, and extrapyramidal syndrome. Am J Hum Genet 2008 83 684 91 19026396 PMC2668059
  53. [59]Basel-Vanagaite L Sarig O Hershkovitz D Fuchs-Telem D Rapaport D Gat A RIN2 deficiency results in macrocephaly, alopecia, cutis laxa, and scoliosis: MACS syndrome. Am J Hum Genet 2009 85 254 63 19631308 PMC2725231
  54. [60]Molho-Pessach V Lerer I Abeliovich D Agha Z Abu Libdeh A Broshtilova V The H syndrome is caused by mutations in the nucleoside transporter hENT3. Am J Hum Genet 2008 83 529 34 18940313 PMC2561939
  55. [61]Fantauzzo KA Tadin-Strapps M You Y Mentzer SE Baumeister FA Cianfarani S A position effect on TRPS1 is associated with Ambras syndrome in humans and the Koala phenotype in mice. Hum Mol Genet 2008 17 3539 51 18713754 PMC2572698
  56. [62]Fantauzzo KA Kurban M Levy B Christiano AM Trps1 and its target gene Sox9 regulate epithelial proliferation in the developing hair follicle and are associated with hypertrichosis. PLoS Genet 2012 8 e1003002 23133399 PMC3486859
  57. [63]DeStefano GM Fantauzzo KA Petukhova L Kurban M Tadin-Strapps M Levy B Position effect on FGF13 associated with X-linked congenital generalized hypertrichosis. Proc Natl Acad Sci USA 2013 110 7790 5 23603273 PMC3651487
  58. [64]Fang J Dagenais SL Erickson RP Arlt MF Glynn MW Gorski JL Mutations in FOXC2 (MFH-1), a forkhead family transcription factor, are responsible for the hereditary lymphedema-distichiasis syndrome. Am J Hum Genet 2000 67 1382 8 11078474 PMC1287915
  59. [65]Winter H Rogers MA Langbein L Stevens HP Leigh IM Labreze C Mutations in the hair cortex keratin hHb6 cause the inherited hair disease monilethrix. Nat Genet 1997 16 372 4 9241275
  60. [66]Winter H Labreze C Chapalain V Surleve-Bazeille JE Mercier M Rogers MA A variable monilethrix phenotype associated with a novel mutation, Glu402Lys, in the helix termination motif of the type II hair keratin hHb1. J Invest Dermatol 1998 111 169 72 9665406
  61. [67]van Steensel MA Steijlen PM Bladergroen RS Vermeer M van Geel M A mis-sense mutation in the type II hair keratin hHb3 is associated with monilethrix. J Med Genet 2005 42 e19 15744029 PMC1736019
  62. [68]Zlotogorski A Marek D Horev L Abu A Ben-Amitai D Gerad L An auto-somal recessive form of monilethrix is caused by mutations in DSG4: clinical overlap with localized autosomal recessive hypotrichosis. J Invest Dermatol 2006 126 1292 6 16575393
  63. [69]Naeem M Wajid M Lee K Leal SM Ahmad W A mutation in the hair matrix and cuticle keratin KRTHB5 gene causes ectodermal dysplasia of hair and nail type. J Med Genet 2006 43 274 9 16525032 PMC2563238
  64. [70]Winter H Schissel D Parry DA Smith TA Liovic M Birgitte Lane E An unusual Ala12Thr polymorphism in the 1A alpha-helical segment of the companion layer-specific keratin K6hf: evidence for a risk factor in the etiology of the common hair disorder pseudofolliculitis barbae. J Invest Dermatol 2004 122 652 7 15086549
  65. [71]Norgett EE Hatsell SJ Carvajal-Huerta L Cabezas JC Common J Purkis PE Recessive mutation in desmoplakin disrupts desmoplakin-intermediate filament interactions and causes dilated cardiomyopathy, woolly hair and keratoderma. Hum Mol Genet 2000 9 2761 6 11063735
  66. [72]Whittock NV Wan H Morley SM Garzon MC Kristal L Hyde P Compound heterozygosity for non-sense and mis-sense mutations in desmoplakin underlies skin fragility/woolly hair syndrome. J Invest Dermatol 2002 118 232 8 11841538
  67. [73]McKoy G Protonotarios N Crosby A Tsatsopoulou A Anastasakis A Coonar A Identification of a deletion in plakoglobin in arrhythmogenic right ventricular cardiomyopathy with palmoplantar keratoderma and woolly hair (Naxos disease). Lancet 2000 355 2119 24 10902626
  68. [74]Fujimoto A Farooq M Fujikawa H Inoue A Ohyama M Ehama R A missense mutation within the helix initiation motif of the keratin K71 gene underlies autosomal dominant woolly hair/hypotrichosis. J Invest Dermatol 2012 132 2342 9 22592156
  69. [75]Shimomura Y Wajid M Petukhova L Kurban M Christiano AM Autosomal-dominant woolly hair resulting from disruption of keratin 74 (KRT74), a potential determinant of human hair texture. Am J Hum Genet 2010 86 632 8 20346438 PMC2850421
  70. [76]Price JA Bowden DW Wright JT Pettenati MJ Hart TC Identification of a mutation in DLX3 associated with tricho-dento-osseous (TDO) syndrome. Hum Mol Genet 1998 7 563 9 9467018
  71. [77]Hwang J Mehrani T Millar SE Morasso MI Dlx3 is a crucial regulator of hair follicle differentiation and cycling. Development 2008 135 3149 59 18684741 PMC2707782
  72. [78]Radoja N Guerrini L Lo Iacono N Merlo GR Costanzo A Weinberg WC Homeobox gene Dlx3 is regulated by p63 during ectoderm development: relevance in the pathogenesis of ectodermal dysplasias. Development 2007 134 13 8 17164413
  73. [79]Chelly J Tumer Z Tonnesen T Petterson A Ishikawa-Brush Y Tommerup N Isolation of a candidate gene for Menkes disease that encodes a potential heavy metal binding protein. Nat Genet 1993 3 14 9 8490646
  74. [80]Mercer JF Livingston J Hall B Paynter JA Begy C Chandrasekharappa S Isolation of a partial candidate gene for Menkes disease by positional cloning. Nat Genet 1993 3 20 5 8490647
  75. [81]Vulpe C Levinson B Whitney S Packman S Gitschier J Isolation of a candidate gene for Menkes disease and evidence that it encodes a copper-transporting ATPase. Nat Genet 1993 3 7 13 8490659
  76. [82]Takayama K Salazar EP Broughton BC Lehmann AR Sarasin A Thompson LH Defects in the DNA repair and transcription gene ERCC2(XPD) in trichothiodystrophy. Am J Hum Genet 1996 58 263 70 8571952 PMC1914548
  77. [83]Weeda G Eveno E Donker I Vermeulen W Chevallier-Lagente O Taieb A A mutation in the XPB/ERCC3 DNA repair transcription gene, associated with trichothiodystrophy. Am J Hum Genet 1997 60 320 9 9012405 PMC1712398
  78. [84]Giglia-Mari G Coin F Ranish JA Hoogstraten D Theil A Wijgers N A new, tenth subunit of TFIIH is responsible for the DNA repair syndrome trichothiodystrophy group A. Nat Genet 2004 36 714 9 15220921
  79. [85]Nakabayashi K Amann D Ren Y Saarialho-Kere U Avidan N Gentles S Identification of C7orf11 (TTDN1) gene mutations and genetic heterogeneity in nonphotosensitive trichothiodystrophy. Am J Hum Genet 2005 76 510 6 15645389 PMC1196401

Cited by

Sorted by citations

Authors
Duverger, O., & Morasso, M. I.
Affiliations
National Institutes of Health (US)
Corresponding author
Duverger, Olivier
Venue
Seminars in Cell & Developmental Biology
Publisher
Elsevier BV
Published
2014-01
Volume
25-26
Pages
22-33
ISSN
1084-9521 (ISSN-L)
OpenAlex
W2006376890
Cited by
57
References
6
Citations by year
2025: 1 · 2024: 4 · 2023: 3 · 2022: 6 · 2021: 8 · 2020: 4 · 2019: 8 · 2018: 2 · 2017: 7 · 2016: 7 · 2015: 4 · 2014: 2
FWCI
0.79
Type
journal article
Language
en
Open access
Locations
  • Seminars in Cell and Developmental Biology (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institutes of Health
  • National Institute of Arthritis and Musculoskeletal and Skin Diseases (ZIAAR041171)
Topics
  • Health Sciences › Medicine › Urology › Hair Growth and Disorders
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › dental development and anomalies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Skin and Cellular Biology Research
Keywords
hair morphogenesis, hair follicle development, hair follicle regeneration, mouse model, hair distribution, hair cycle, hair follicle structure
MeSH terms
Alopecia, Animals, Disease Models, Animal, Hair, Hair Diseases, Humans, Morphogenesis, Hair Follicle, Mice

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