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

Seminars in Cell and Developmental Biology

Volumn 25-26, Issue , 2014, Pages 22-33

  Duverger, Olivier ^a   Morasso, Maria I ^a  

^a NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

Author keywords

Alopecia; Genetic disorders; Hair follicle; Morphogenesis; Shaft differentiation

Indexed keywords

TRANSCRIPTION FACTOR;

ANALYTICAL PARAMETERS; BRITTLENESS; CHEMICAL COMPOSITION; DISEASE ASSOCIATION; GENE MUTATION; GENETIC DISORDER; HAIR; HAIR DISEASE; HAIR FOLLICLE; HAIR GROWTH; HUMAN; HYPERTRICHOSIS; HYPOTRICHOSIS; MORPHOGENESIS; NONHUMAN; REVIEW; SCANTY HAIR; TRANSCRIPTION REGULATION; ALOPECIA; ANIMAL; CONGENITAL MALFORMATION; DISEASE MODEL; GENETICS; GROWTH, DEVELOPMENT AND AGING; MOUSE; PATHOLOGY;

ANIMALIA; MUS;

ALOPECIA; ANIMALS; DISEASE MODELS, ANIMAL; HAIR; HAIR DISEASES; HAIR FOLLICLE; HUMANS; MICE; MORPHOGENESIS;

EID: 84898485814     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2013.12.006     Document Type: Review

References (85)

1. Lee J., Tumbar T. Hairy tale of signaling in hair follicle development and cycling. Semin Cell Dev Biol 2012, 23:906-916.
2. Sennett R., Rendl M. Mesenchymal-epithelial interactions during hair follicle morphogenesis and cycling. Semin Cell Dev Biol 2012, 23:917-927.
3. Ohyama M., Vogel J.C., Amagai M. Gene ontology analysis of human hair follicle bulge molecular signature. J Dermatol Sci 2007, 45:147-150.
4. Cotsarelis G. Epithelial stem cells: a folliculocentric view. J Invest Dermatol 2006, 126:1459-1468.
5. Jaks V., Kasper M., Toftgard R. The hair follicle - a stem cell zoo. Exp Cell Res 2010, 316:1422-1428.
6. Langbein L., Schweizer J. Keratins of the human hair follicle. Int Rev Cytol 2005, 243:1-78.
7. Duverger O., Morasso M.I. Epidermal patterning and induction of different hair types during mouse embryonic development. Birth Defects Res C Embryo Today 2009, 87:263-272.
8. Muller-Rover S., Handjiski B., van der Veen C., Eichmuller S., Foitzik K., McKay I.A., et al. A comprehensive guide for the accurate classification of murine hair follicles in distinct hair cycle stages. J Invest Dermatol 2001, 117:3-15.
9. Krause K., Foitzik K. Biology of the hair follicle: the basics. Semin Cutan Med Surg 2006, 25:2-10.
10. Ahmad W., Faiyaz ul Haque M., Brancolini V., Tsou H.C., ul Haque S., Lam H., et al. Alopecia universalis associated with a mutation in the human hairless gene. Science 1998, 279:720-724.
11. Sprecher E., Lestringant G.G., Szargel R., Bergman R., Labay V., Frossard P.M., et al. Atrichia with papular lesions resulting from a nonsense mutation within the human hairless gene. J Invest Dermatol 1999, 113:687-690.
12. Wen Y., Liu Y., Xu Y., Zhao Y., Hua R., Wang K., et al. Loss-of-function mutations of an inhibitory upstream ORF in the human hairless transcript cause Marie Unna hereditary hypotrichosis. Nat Genet 2009, 41:228-233.
13. Mecklenburg L., Nakamura M., Sundberg J.P., Paus R. The nude mouse skin phenotype: the role of Foxn1 in hair follicle development and cycling. Exp Mol Pathol 2001, 71:171-178.
14. Frank J., Pignata C., Panteleyev A.A., Prowse D.M., Baden H., Weiner L., et al. Exposing the human nude phenotype. Nature 1999, 398:473-474.
15. Clifton-Bligh R.J., Wentworth J.M., Heinz P., Crisp M.S., John R., Lazarus J.H., et al. Mutation of the gene encoding human TTF-2 associated with thyroid agenesis, cleft palate and choanal atresia. Nat Genet 1998, 19:399-401.
16. Kayserili H., Uz E., Niessen C., Vargel I., Alanay Y., Tuncbilek G., et al. ALX4 dysfunction disrupts craniofacial and epidermal development. Hum Mol Genet 2009, 18:4357-4366.
17. Godwin A.R., Capecchi M.R. Hoxc13 mutant mice lack external hair. Genes Dev 1998, 12:11-20.
18. Lin Z., Chen Q., Shi L., Lee M., Giehl K.A., Tang Z., et al. Loss-of-function mutations in HOXC13 cause pure hair and nail ectodermal dysplasia. Am J Hum Genet 2012, 91:906-911.
19. Hughes M.R., Malloy P.J., Kieback D.G., Kesterson R.A., Pike J.W., Feldman D., et al. Point mutations in the human vitamin D receptor gene associated with hypocalcemic rickets. Science 1988, 242:1702-1705.
20. Oeffner F., Fischer G., Happle R., Konig A., Betz R.C., Bornholdt D., et al. 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, 84:459-467.
21. Aten E., Brasz L.C., Bornholdt D., Hooijkaas I.B., Porteous M.E., Sybert V.P., et al. Keratosis Follicularis Spinulosa Decalvans is caused by mutations in MBTPS2. Hum Mutat 2010, 31:1125-1133.
22. Irrthum A., Devriendt K., Chitayat D., Matthijs G., Glade C., Steijlen P.M., et al. Mutations in the transcription factor gene SOX18 underlie recessive and dominant forms of hypotrichosis-lymphedema-telangiectasia. Am J Hum Genet 2003, 72:1470-1478.
23. Momeni P., Glockner G., Schmidt O., von Holtum D., Albrecht B., Gillessen-Kaesbach G., et al. Mutations in a new gene, encoding a zinc-finger protein, cause tricho-rhino-phalangeal syndrome type I. Nat Genet 2000, 24:71-74.
24. Ludecke H.J., Schaper J., Meinecke P., Momeni P., Gross S., von Holtum D., et al. Genotypic and phenotypic spectrum in tricho-rhino-phalangeal syndrome types I and III. Am J Hum Genet 2001, 68:81-91.
25. Celli J., Duijf P., Hamel B.C., Bamshad M., Kramer B., Smits A.P., et al. Heterozygous germline mutations in the p53 homolog p63 are the cause of EEC syndrome. Cell 1999, 99:143-153.
26. McGrath J.A., Duijf P.H., Doetsch V., Irvine A.D., de Waal R., Vanmolkot K.R., et al. Hay-Wells syndrome is caused by heterozygous missense mutations in the SAM domain of p63. Hum Mol Genet 2001, 10:221-229.
27. Kantaputra P.N., Hamada T., Kumchai T., McGrath J.A. Heterozygous mutation in the SAM domain of p63 underlies Rapp-Hodgkin ectodermal dysplasia. J Dent Res 2003, 82:433-437.
28. Amiel J., Bougeard G., Francannet C., Raclin V., Munnich A., Lyonnet S., et al. TP63 gene mutation in ADULT syndrome. Eur J Hum Genet 2001, 9:642-645.
29. Kere J., Srivastava A.K., Montonen O., Zonana J., Thomas N., Ferguson B., et al. X-linked anhidrotic (hypohidrotic) ectodermal dysplasia is caused by mutation in a novel transmembrane protein. Nat Genet 1996, 13:409-416.
30. Monreal A.W., Ferguson B.M., Headon D.J., Street S.L., Overbeek P.A., Zonana J. Mutations in the human homologue of mouse dl cause autosomal recessive and dominant hypohidrotic ectodermal dysplasia. Nat Genet 1999, 22:366-369.
31. Headon D.J., Emmal S.A., Ferguson B.M., Tucker A.S., Justice M.J., Sharpe P.T., et al. Gene defect in ectodermal dysplasia implicates a death domain adapter in development. Nature 2001, 414:913-916.
32. Bal E., Baala L., Cluzeau C., El Kerch F., Ouldim K., Hadj-Rabia S., et al. Autosomal dominant anhidrotic ectodermal dysplasias at the EDARADD locus. Hum Mutat 2007, 28:703-709.
33. Zonana J., Elder M.E., Schneider L.C., Orlow S.J., Moss C., Golabi M., et al. 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, 67:1555-1562.
34. Smahi A., Courtois G., Vabres P., Yamaoka S., Heuertz S., Munnich A., et al. Genomic rearrangement in NEMO impairs NF-kappaB activation and is a cause of incontinentia pigmenti. The International Incontinentia Pigmenti (IP) Consortium. Nature 2000, 405:466-472.
35. Adaimy L., Chouery E., Megarbane H., Mroueh S., Delague V., Nicolas E., et al. Mutation in WNT10A is associated with an autosomal recessive ectodermal dysplasia: the odonto-onycho-dermal dysplasia. Am J Hum Genet 2007, 81:821-828.
36. Bohring A., Stamm T., Spaich C., Haase C., Spree K., Hehr U., et al. WNT10A mutations are a frequent cause of a broad spectrum of ectodermal dysplasias with sex-biased manifestation pattern in heterozygotes. Am J Hum Genet 2009, 85:97-105.
37. Shimomura Y., Agalliu D., Vonica A., Luria V., Wajid M., Baumer A., et al. APCDD1 is a novel Wnt inhibitor mutated in hereditary hypotrichosis simplex. Nature 2010, 464:1043-1047.
38. Kljuic A., Bazzi H., Sundberg J.P., Martinez-Mir A., O'Shaughnessy R., Mahoney M.G., et al. Desmoglein 4 in hair follicle differentiation and epidermal adhesion: evidence from inherited hypotrichosis and acquired pemphigus vulgaris. Cell 2003, 113:249-260.
39. Ayub M., Basit S., Jelani M., Ur Rehman F., Iqbal M., Yasinzai M., et al. A homozygous nonsense mutation in the human desmocollin-3 (DSC3) gene underlies hereditary hypotrichosis and recurrent skin vesicles. Am J Hum Genet 2009, 85:515-520.
40. McGrath J.A., McMillan J.R., Shemanko C.S., Runswick S.K., Leigh I.M., Lane E.B., et al. Mutations in the plakophilin 1 gene result in ectodermal dysplasia/skin fragility syndrome. Nat Genet 1997, 17:240-244.
41. Levy-Nissenbaum E., Betz R.C., Frydman M., Simon M., Lahat H., Bakhan T., et al. Hypotrichosis simplex of the scalp is associated with nonsense mutations in CDSN encoding corneodesmosin. Nat Genet 2003, 34:151-153.
42. Blaydon D.C., Biancheri P., Di W.L., Plagnol V., Cabral R.M., Brooke M.A., et al. Inflammatory skin and bowel disease linked to ADAM17 deletion. N Engl J Med 2011, 365:1502-1508.
43. Basel-Vanagaite L., Attia R., Ishida-Yamamoto A., Rainshtein L., Ben Amitai D., Lurie R., et al. Autosomal recessive ichthyosis with hypotrichosis caused by a mutation in ST14, encoding type II transmembrane serine protease matriptase. Am J Hum Genet 2007, 80:467-477.
44. Chavanas S., Bodemer C., Rochat A., Hamel-Teillac D., Ali M., Irvine A.D., et al. Mutations in SPINK5, encoding a serine protease inhibitor, cause Netherton syndrome. Nat Genet 2000, 25:141-142.
45. Gu L.H., Coulombe P.A. Keratin function in skin epithelia: a broadening palette with surprising shades. Curr Opin Cell Biol 2007, 19:13-23.
46. Wasif N., Naqvi S.K., 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, 129:419-424.
47. Sprecher E., Bergman R., Richard G., Lurie R., Shalev S., Petronius D., et al. Hypotrichosis with juvenile macular dystrophy is caused by a mutation in CDH3, encoding P-cadherin. Nat Genet 2001, 29:134-136.
48. Kjaer K.W., Hansen L., Schwabe G.C., Marques-de-Faria A.P., Eiberg H., Mundlos S., et al. Distinct CDH3 mutations cause ectodermal dysplasia, ectrodactyly, macular dystrophy (EEM syndrome). J Med Genet 2005, 42:292-298.
49. Hadj-Rabia S., Baala L., Vabres P., Hamel-Teillac D., Jacquemin E., Fabre M., et al. Claudin-1 gene mutations in neonatal sclerosing cholangitis associated with ichthyosis: a tight junction disease. Gastroenterology 2004, 127:1386-1390.
50. Suzuki K., Hu D., Bustos T., Zlotogora J., Richieri-Costa A., Helms J.A., et al. Mutations of PVRL1, encoding a cell-cell adhesion molecule/herpesvirus receptor, in cleft lip/palate-ectodermal dysplasia. Nat Genet 2000, 25:427-430.
51. Stranecky V., Hoischen A., Hartmannova H., Zaki M.S., Chaudhary A., Zudaire E., et al. Mutations in ANTXR1 cause GAPO syndrome. Am J Hum Genet 2013, 92:792-799.
52. Lamartine J., Munhoz Essenfelder G., Kibar Z., Lanneluc I., Callouet E., Laoudj D., et al. Mutations in GJB6 cause hidrotic ectodermal dysplasia. Nat Genet 2000, 26:142-144.
53. Kazantseva A., Goltsov A., Zinchenko R., Grigorenko A.P., Abrukova A.V., Moliaka Y.K., et al. Human hair growth deficiency is linked to a genetic defect in the phospholipase gene LIPH. Science 2006, 314:982-985.
54. Pasternack S.M., von Kugelgen I., Al Aboud K., Lee Y.A., Ruschendorf F., Voss K., et al. G protein-coupled receptor P2Y5 and its ligand LPA are involved in maintenance of human hair growth. Nat Genet 2008, 40:329-334.
55. Shimomura Y., Wajid M., Ishii Y., Shapiro L., Petukhova L., Gordon D., et al. Disruption of P2RY5, an orphan G protein-coupled receptor, underlies autosomal recessive woolly hair. Nat Genet 2008, 40:335-339.
56. Nousbeck J., Spiegel R., Ishida-Yamamoto A., Indelman M., Shani-Adir A., Adir N., et al. Alopecia, neurological defects, and endocrinopathy syndrome caused by decreased expression of RBM28, a nucleolar protein associated with ribosome biogenesis. Am J Hum Genet 2008, 82:1114-1121.
57. Pasternack S.M., Refke M., Paknia E., Hennies H.C., Franz T., Schafer N., et al. Mutations in SNRPE, which encodes a core protein of the spliceosome, cause autosomal-dominant hypotrichosis simplex. Am J Hum Genet 2013, 92:81-87.
58. Alazami A.M., Al-Saif A., Al-Semari A., Bohlega S., Zlitni S., Alzahrani F., et al. Mutations in C2orf37, encoding a nucleolar protein, cause hypogonadism, alopecia, diabetes mellitus, mental retardation, and extrapyramidal syndrome. Am J Hum Genet 2008, 83:684-691.
59. Basel-Vanagaite L., Sarig O., Hershkovitz D., Fuchs-Telem D., Rapaport D., Gat A., et al. RIN2 deficiency results in macrocephaly, alopecia, cutis laxa, and scoliosis: MACS syndrome. Am J Hum Genet 2009, 85:254-263.
60. Molho-Pessach V., Lerer I., Abeliovich D., Agha Z., Abu Libdeh A., Broshtilova V., et al. The H syndrome is caused by mutations in the nucleoside transporter hENT3. Am J Hum Genet 2008, 83:529-534.
61. Fantauzzo K.A., Tadin-Strapps M., You Y., Mentzer S.E., Baumeister F.A., Cianfarani S., et al. A position effect on TRPS1 is associated with Ambras syndrome in humans and the Koala phenotype in mice. Hum Mol Genet 2008, 17:3539-3551.
62. Fantauzzo K.A., Kurban M., Levy B., Christiano A.M. Trps1 and its target gene Sox9 regulate epithelial proliferation in the developing hair follicle and are associated with hypertrichosis. PLoS Genet 2012, 8:e1003002.
63. DeStefano G.M., Fantauzzo K.A., Petukhova L., Kurban M., Tadin-Strapps M., Levy B., et al. Position effect on FGF13 associated with X-linked congenital generalized hypertrichosis. Proc Natl Acad Sci USA 2013, 110:7790-7795.
64. Fang J., Dagenais S.L., Erickson R.P., Arlt M.F., Glynn M.W., Gorski J.L., et al. Mutations in FOXC2 (MFH-1), a forkhead family transcription factor, are responsible for the hereditary lymphedema-distichiasis syndrome. Am J Hum Genet 2000, 67:1382-1388.
65. Winter H., Rogers M.A., Langbein L., Stevens H.P., Leigh I.M., Labreze C., et al. Mutations in the hair cortex keratin hHb6 cause the inherited hair disease monilethrix. Nat Genet 1997, 16:372-374.
66. Winter H., Labreze C., Chapalain V., Surleve-Bazeille J.E., Mercier M., Rogers M.A., et al. 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, 111:169-172.
67. van Steensel M.A., Steijlen P.M., Bladergroen R.S., Vermeer M., van Geel M. A missense mutation in the type II hair keratin hHb3 is associated with monilethrix. J Med Genet 2005, 42:e19.
68. Zlotogorski A., Marek D., Horev L., Abu A., Ben-Amitai D., Gerad L., et al. An autosomal recessive form of monilethrix is caused by mutations in DSG4: clinical overlap with localized autosomal recessive hypotrichosis. J Invest Dermatol 2006, 126:1292-1296.
69. Naeem M., Wajid M., Lee K., Leal S.M., 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, 43:274-279.
70. Winter H., Schissel D., Parry D.A., Smith T.A., Liovic M., Birgitte Lane E., et al. 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, 122:652-657.
71. Norgett E.E., Hatsell S.J., Carvajal-Huerta L., Cabezas J.C., Common J., Purkis P.E., et al. Recessive mutation in desmoplakin disrupts desmoplakin-intermediate filament interactions and causes dilated cardiomyopathy, woolly hair and keratoderma. Hum Mol Genet 2000, 9:2761-2766.
72. Whittock N.V., Wan H., Morley S.M., Garzon M.C., Kristal L., Hyde P., et al. Compound heterozygosity for non-sense and mis-sense mutations in desmoplakin underlies skin fragility/woolly hair syndrome. J Invest Dermatol 2002, 118:232-238.
73. McKoy G., Protonotarios N., Crosby A., Tsatsopoulou A., Anastasakis A., Coonar A., et al. Identification of a deletion in plakoglobin in arrhythmogenic right ventricular cardiomyopathy with palmoplantar keratoderma and woolly hair (Naxos disease). Lancet 2000, 355:2119-2124.
74. Fujimoto A., Farooq M., Fujikawa H., Inoue A., Ohyama M., Ehama R., et al. A missense mutation within the helix initiation motif of the keratin K71 gene underlies autosomal dominant woolly hair/hypotrichosis. J Invest Dermatol 2012, 132:2342-2349.
75. Shimomura Y., Wajid M., Petukhova L., Kurban M., Christiano A.M. Autosomal-dominant woolly hair resulting from disruption of keratin 74 (KRT74), a potential determinant of human hair texture. Am J Hum Genet 2010, 86:632-638.
76. Price J.A., Bowden D.W., Wright J.T., Pettenati M.J., Hart T.C. Identification of a mutation in DLX3 associated with tricho-dento-osseous (TDO) syndrome. Hum Mol Genet 1998, 7:563-569.
77. Hwang J., Mehrani T., Millar S.E., Morasso M.I. Dlx3 is a crucial regulator of hair follicle differentiation and cycling. Development 2008, 135:3149-3159.
78. Radoja N., Guerrini L., Lo Iacono N., Merlo G.R., Costanzo A., Weinberg W.C., et al. Homeobox gene Dlx3 is regulated by p63 during ectoderm development: relevance in the pathogenesis of ectodermal dysplasias. Development 2007, 134:13-18.
79. Chelly J., Tumer Z., Tonnesen T., Petterson A., Ishikawa-Brush Y., Tommerup N., et al. Isolation of a candidate gene for Menkes disease that encodes a potential heavy metal binding protein. Nat Genet 1993, 3:14-19.
80. Mercer J.F., Livingston J., Hall B., Paynter J.A., Begy C., Chandrasekharappa S., et al. Isolation of a partial candidate gene for Menkes disease by positional cloning. Nat Genet 1993, 3:20-25.
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.
82. Takayama K., Salazar E.P., Broughton B.C., Lehmann A.R., Sarasin A., Thompson L.H., et al. Defects in the DNA repair and transcription gene ERCC2(XPD) in trichothiodystrophy. Am J Hum Genet 1996, 58:263-270.
83. Weeda G., Eveno E., Donker I., Vermeulen W., Chevallier-Lagente O., Taieb A., et al. A mutation in the XPB/ERCC3 DNA repair transcription gene, associated with trichothiodystrophy. Am J Hum Genet 1997, 60:320-329.
84. Giglia-Mari G., Coin F., Ranish J.A., Hoogstraten D., Theil A., Wijgers N., et al. A new, tenth subunit of TFIIH is responsible for the DNA repair syndrome trichothiodystrophy group A. Nat Genet 2004, 36:714-719.
85. Nakabayashi K., Amann D., Ren Y., Saarialho-Kere U., Avidan N., Gentles S., et al. Identification of C7orf11 (TTDN1) gene mutations and genetic heterogeneity in nonphotosensitive trichothiodystrophy. Am J Hum Genet 2005, 76:510-516.