CoChat
Sign Up
Cited by 70Hair Growth and Disordersdental development and anomaliesSkin and Cellular Biology Research

Bone Morphogenetic Protein Signaling Regulates Postnatal Hair Follicle Differentiation and Cycling

Open access
Guha, Udayan, Mecklenburg, Lars, Cowin, Pamela, Kan, Lixin, O'Guin, W. Michael, D'Vizio, Dolores, Pestell, Richard G., Paus, Ralf +1 more·2004·The American Journal of Pathology
DOI 10.1016/s0002-9440(10)63336-6PMC PMC1618597
Open this paper in CoChat — free account

Abstract

Hair follicle morphogenesis and cycling were examined in transgenic mice that overexpress the bone morphogenetic protein (BMP) inhibitor Noggin under the control of the neuron-specific enolase promoter. The Noggin transgene was misexpressed in the proximal portion of the hair follicle, primarily the matrix cells, apart from the usual expression in neurons. Transgene expression appeared only after induction of both the primary (tylotrich) and secondary (nontylotrich) pelage hair follicles had already occurred, thus allowing examination of the role of BMP signaling in follicles that had been induced normally in the presence of BMPs. The overexpression of Noggin in these animals resulted in a dramatic loss of hair postnatally. There was an apparently normal, but shortened period of postnatal hair follicle morphogenesis, followed by premature initiation of hair follicle cycling via entry into the first catagen transformation. This resulted in a complete loss of hair shafts from the nontylotrich hair follicles in these mice while the tylotrich hair follicles were normal. The onset of anagen of the first postnatal hair follicle cycle was also accelerated in the transgenic mice. Our results show that BMP signaling is specifically required for proper proliferation and differentiation during late morphogenesis of nontylotrich hair follicles and that inhibition of this signaling pathway may be one of the triggers for the onset of catagen when the follicles are in anagen and the onset of anagen when the follicles are in telogen. Ectopic sebocyte differentiation was another hallmark of the phenotype of these transgenic mice suggesting that BMP signaling may be an important determinant of lineage selection by common progenitor cells in the skin. BMPs likely promote a hair follicle-type differentiation pathway of keratinocytes while suppressing the sebaceous differentiation pathway of skin epithelium.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/s0002-9440(10)63336-6

Cites

3 of 3 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 65

  1. Paus R, Peters EM, Eichmuller S, Botchkarev VA. Neural mechanisms of hair growth control. J Invest Dermatol Symp Proc. 1997;2:61–68. doi: 10.1038/jidsymp.1997.13. [DOI] [PubMed] [Google Scholar] · DOI
  2. Botchkarev VA, Eichmuller S, Johansson O, Paus R. Hair cycle-dependent plasticity of skin and hair follicle innervation in normal murine skin. J Comp Neurol. 1997;386:379–395. doi: 10.1002/(sici)1096-9861(19970929)386:3<379::aid-cne4>3.0.co;2-z. [DOI] [PubMed] [Google Scholar] · DOI
  3. Hardy MH. The secret life of the hair follicle. Trends Genet. 1992;8:55–61. doi: 10.1016/0168-9525(92)90350-d. [DOI] [PubMed] [Google Scholar] · DOI
  4. Paus R, Muller-Rover S, Van Der Veen C, Maurer M, Eichmuller S, Ling G, Hofmann U, Foitzik K, Mecklenburg L, Handjiski B. A comprehensive guide for the recognition and classification of distinct stages of hair follicle morphogenesis. J Invest Dermatol. 1999;113:523–532. doi: 10.1046/j.1523-1747.1999.00740.x. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  5. Vielkind U, Hardy MH. Changing patterns of cell adhesion molecules during mouse pelage hair follicle development. 2. Follicle morphogenesis in the hair mutants, Tabby and downy. Acta Anat. 1996;157:183–194. doi: 10.1159/000147880. [DOI] [PubMed] [Google Scholar] · DOI
  6. Philpott MP, PR. Principles of hair follicle morphogenesis. Molecular Basis of Epithelial Appendage Morphogenesis. Chuong CM, editor. Landes Bioscience Publishers,; 1998:pp 75–103. [Google Scholar]
  7. Paus R, Cotsarelis G. The biology of hair follicles. N Engl J Med. 1999;341:491–497. doi: 10.1056/NEJM199908123410706. [DOI] [PubMed] [Google Scholar] · DOI
  8. Weedon D, Strutton G. Apoptosis as the mechanism of the involution of hair follicles in catagen transformation. Acta Derm Venereol. 1981;61:335–339. [PubMed] [Google Scholar]
  9. Lindner G, Botchkarev VA, Botchkareva NV, Ling G, van der Veen C, Paus R. Analysis of apoptosis during hair follicle regression (catagen). Am J Pathol. 1997;151:1601–1617. [PMC free article] [PubMed] [Google Scholar]
  10. Stenn KS, Combates NJ, Eilertsen KJ, Gordon JS, Pardinas JR, Parimoo S, Prouty SM. Hair follicle growth controls. Dermatol Clin. 1996;14:543–558. doi: 10.1016/s0733-8635(05)70383-1. [DOI] [PubMed] [Google Scholar] · DOI
  11. Taylor G, Lehrer MS, Jensen PJ, Sun TT, Lavker RM. Involvement of follicular stem cells in forming not only the follicle but also the epidermis. Cell. 2000;102:451–461. doi: 10.1016/s0092-8674(00)00050-7. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  12. Oshima H, Roshat R, Kedzia C, Kobayashi K, Barrandon Y. Morphogenesis and renewal of hair follicles from adult multipotent stem cells. Cell. 2001;104:233–245. doi: 10.1016/s0092-8674(01)00208-2. [DOI] [PubMed] [Google Scholar] · DOI
  13. Oliver RF. The induction of hair follicle formation in the adult hooded rat by vibrissa dermal papillae. J Embryol Exp Morphol. 1970;23:219–236. [PubMed] [Google Scholar]
  14. Jahoda CA, Horne KA, Oliver RF. Induction of hair growth by implantation of cultured dermal papilla cells. Nature. 1984;311:560–562. doi: 10.1038/311560a0. [DOI] [PubMed] [Google Scholar] · DOI
  15. Stenn KS, Paus R. Controls of hair follicle cycling. Physiol Rev. 2001;81:449–494. doi: 10.1152/physrev.2001.81.1.449. [DOI] [PubMed] [Google Scholar] · DOI
  16. Fuchs E, Merill BJ, Jamora C, DasGupta R. At the roots of a never-ending cycle. Dev Cell. 2001;1:13–25. doi: 10.1016/s1534-5807(01)00022-3. [DOI] [PubMed] [Google Scholar] · DOI
  17. Gat U, DasGupta R, Degenstein L, Fuchs E. De novo hair follicle morphogenesis and hair tumors in mice expressing a truncated beta-catenin in skin. Cell. 1998;95:605–614. doi: 10.1016/s0092-8674(00)81631-1. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  18. Headon DJ, Overbeek PA. Involvement of a novel Tnf receptor homologue in hair follicle induction. Nat Genet. 1999;22:370–374. doi: 10.1038/11943. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  19. Widelitz RB, Jiang TX, Noveen A, Chen CW, Chuong CM. FGF induces new feather buds from developing avian skin. J Invest Dermatol. 1996;107:797–803. doi: 10.1111/1523-1747.ep12330553. [DOI] [PubMed] [Google Scholar] · DOI
  20. St-Jacques B. Sonic hedgehog signaling is essential for hair development. Curr Biol. 1998;8:1058–1068. doi: 10.1016/s0960-9822(98)70443-9. [DOI] [PubMed] [Google Scholar] · DOI
  21. Chiang C, Swan RZ, Grachtchouk M, Bolinger M, Litingtung Y, Robertson EK, Cooper MK, Gaffield W, Westphal H, Beachy PA, Dlugosz AA. Essential role for sonic hedgehog during hair follicle morphogenesis. Dev Biol. 1999;205:1–9. doi: 10.1006/dbio.1998.9103. [DOI] [PubMed] [Google Scholar] · DOI
  22. Oro AE, Higgins KM, Hu Z, Bonifas JM, Epstein EH, Jr, Scott MP. Basal cell carcinomas in mice overexpressing sonic hedgehog. Science. 1997;276:817–821. doi: 10.1126/science.276.5313.817. [DOI] [PubMed] [Google Scholar] · DOI
  23. Finch PW, Rubin JS, Miki T, Ron D, Aaronson SA. Human KGF is FGF-related with properties of a paracrine effector of epithelial cell growth. Science. 1989;245:752–755. doi: 10.1126/science.2475908. [DOI] [PubMed] [Google Scholar] · DOI
  24. Zhou P, Byrne C, Jacobs J, Fuchs E. Lymphoid enhancer factor 1 directs hair follicle patterning and epithelial cell fate. Genes Dev. 1995;9:700–713. doi: 10.1101/gad.9.6.700. [DOI] [PubMed] [Google Scholar] · DOI
  25. DasGupta R, Fuchs E. Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development. 1999;126:4557–4568. doi: 10.1242/dev.126.20.4557. [DOI] [PubMed] [Google Scholar] · DOI
  26. Foitzik K, Paus R, Doetschman T, Dotto GP. The TGF-beta2 isoform is both a required and sufficient inducer of murine hair follicle morphogenesis. Dev Biol. 1999;212:278–289. doi: 10.1006/dbio.1999.9325. [DOI] [PubMed] [Google Scholar] · DOI
  27. Foitzik K, Lindner G, Mueller-Roever S, Maurer M, Botchkareva N, Botchkarev V, Handjiski B, Metz M, Hibino T, Soma T, Dotto GP, Paus R. Control of murine hair follicle regression (catagen) by TGF-beta1 in vivo. EMBO J. 2000;14:752–760. doi: 10.1096/fasebj.14.5.752. [DOI] [PubMed] [Google Scholar] · DOI
  28. Botchkarev VA, Botchkareva NV, Roth W, Nakamura M, Chen LH, Herzog W, Lindner G, McMahon JA, Peters C, Lauster R, McMahon AP, Paus R. Noggin is a mesenchymally derived stimulator of hair-follicle induction. Nat Cell Biol. 1999;1:158–164. doi: 10.1038/11078. [DOI] [PubMed] [Google Scholar] · DOI
  29. Botchkarev VA, Botchkareva NV, Nakamura M, Huber O, Funa K, Lauster R, Paus R, Gilchrest BA. Noggin is required for induction of the hair follicle growth phase in postnatal skin. EMBO J. 2001;15:2205–2214. doi: 10.1096/fj.01-0207com. [DOI] [PubMed] [Google Scholar] · DOI
  30. Botchkarev VA, Botchkareva NV, Sharov AA, Funa K, Huber O, Gilchrest BA. Modulation of BMP signaling by noggin is required for induction of the secondary (nontylotrich) hair follicles. J Invest Dermatol. 2002;118:3–10. doi: 10.1046/j.1523-1747.2002.01645.x. [DOI] [PubMed] [Google Scholar] · DOI
  31. Kulessa H, Turk G, Hogan BL. Inhibition of BMP signaling affects growth and differentiation in the anagen hair follicle. EMBO J. 2000;19:6664–6674. doi: 10.1093/emboj/19.24.6664. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  32. Nakamura M, Matzuk MM, Gerstmayer B, Bosio A, Lauster R, Miyachi Y, Werner S, Paus R. Control of pelage hair follicle development and cycling by complex interactions between follistatin and activin. FASEB J. 2003;17:497–499. doi: 10.1096/fj.02-0247fje. [DOI] [PubMed] [Google Scholar] · DOI
  33. Wilson N, Hynd PI, Powell BC. The role of BMP-2 and BMP-4 in follicle initiation and the murine hair cycle. Exp Dermatol. 1999;8:367–368. [PubMed] [Google Scholar]
  34. Takahashi H, Ikeda T. Transcripts for two members of the transforming growth factor-beta superfamily BMP-3 and BMP-7 are expressed in developing rat embryos. Dev Dyn. 1996;207:439–449. doi: 10.1002/(SICI)1097-0177(199612)207:4<439::AID-AJA8>3.0.CO;2-I. [DOI] [PubMed] [Google Scholar] · DOI
  35. Blessing M, Nanney LB, King LE, Jones CM, Hogan BL. Transgenic mice as a model to study the role of TGF-beta-related molecules in hair follicles. Genes Dev. 1993;7:204–215. doi: 10.1101/gad.7.2.204. [DOI] [PubMed] [Google Scholar] · DOI
  36. Zimmerman LB, DeJesus-Escobar JM, Harland RM. The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell. 1996;86:599–606. doi: 10.1016/s0092-8674(00)80133-6. [DOI] [PubMed] [Google Scholar] · DOI
  37. Forss-Petter S, Danielson PE, Catsicas S, Battenberg E, Price J, Nerenberg M, Sutcliffe JG. Transgenic mice expressing beta-galactosidase in mature neurons under neuron-specific enolase promoter control. Neuron. 1990;5:187–197. doi: 10.1016/0896-6273(90)90308-3. [DOI] [PubMed] [Google Scholar] · DOI
  38. Muller-Rover S, Handjiski B, van der Veen C, Eichmuller S, Foitzik K, McKay IA, Stenn KS, Paus R. A comprehensive guide for the accurate classification of murine hair follicles in distinct hair cycle stages. J Invest Dermatol. 2001;117:3–15. doi: 10.1046/j.0022-202x.2001.01377.x. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  39. O’Guin WM, Sun TT, Manabe M. Interaction of trichohyalin with intermediate filaments: three immunologically defined stages of trichohyalin maturation. J Invest Dermatol. 1992;98:24–32. doi: 10.1111/1523-1747.ep12494172. [DOI] [PubMed] [Google Scholar] · DOI
  40. O’Guin WM, Manabe M. The role of trichohyalin in hair follicle differentiation and its expression in nonfollicular epithelia. Ann NY Acad Sci. 1991;642:51–62. doi: 10.1111/j.1749-6632.1991.tb24380.x. [DOI] [PubMed] [Google Scholar] · DOI
  41. Zhang J, Tan X, Contag CH, Lu Y, Guo D, Harris SE, Feng JQ. Dissection of promoter control modules that direct Bmp4 expression in the epithelium-derived components of hair follicles. Biochem Biophys Res Commun. 2002;293:1412–1419. doi: 10.1016/S0006-291X(02)00416-3. [DOI] [PubMed] [Google Scholar] · DOI
  42. Headon DJ, Overbeek PA. Involvement of a novel Tnf receptor homologue in hair follicle induction. Nat Genet. 1999;22:370–374. doi: 10.1038/11943. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  43. Huelsken J, Vogel R, Erdmann B, Cotsarelis G, Birchmeier W. Beta-catenin controls hair follicle morphogenesis and stem cell differentiation in the skin. Cell. 2001;105:533–545. doi: 10.1016/s0092-8674(01)00336-1. [DOI] [PubMed] [Google Scholar] · DOI
  44. Pikus M, Wong WP, Lin J, Wang X, Jiang TX, Chuong CM. Morpho-regulation of ectodermal organs: integument pathology and phenotypic variations in K14-Noggin engineered mice through modulation of bone morphogenetic protein pathway. Am J Pathol. 2004;164:1099–1114. doi: 10.1016/S0002-9440(10)63197-5. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  45. Sharov A, Weiner L, Sharova R, Siebenhaar F, Brisette J, Botchkarev V. Multiple functions of noggin in cutaneous development: leads and lessons from noggin transgeneic mice. J Invest Dermatol. 2003;121 Abstract 0828. [Google Scholar]
  46. Kobielak K, Pasolli HA, Alonso L, Polak L, Fuchs E. Defining BMP functions in the hair follicle by conditional ablation of BMP receptor IA. J Cell Biol. 2003;163:609–623. doi: 10.1083/jcb.200309042. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  47. Seiberg M, Marthinuss J, Stenn KS. Changes in expression of apoptosis-associated genes in skin mark early catagen. J Invest Dermatol. 1995;104:78–82. doi: 10.1111/1523-1747.ep12613555. [DOI] [PubMed] [Google Scholar] · DOI
  48. Paus R, Foitzik K, Welker P, Bulfone-Paus S, Eichmuller S. Transforming growth factor-beta receptor type I and type II expression during murine hair follicle development and cycling. J Invest Dermatol. 1997;109:518–526. doi: 10.1111/1523-1747.ep12336635. [DOI] [PubMed] [Google Scholar] · DOI
  49. Potter GB, Beaudoin GMR, DeRenzo CL, Zarach JM, Chen SH, Thompson CC. The hairless gene mutated in congenital hair loss disorders encodes a novel nuclear receptor corepressor. Genes Dev. 2001;15:2687–2701. doi: 10.1101/gad.916701. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  50. Panteleyev AA, Botchkareva NV, Sundberg JP, Christiano AM, Paus R. The role of the hairless (hr) gene in the regulation of hair follicle catagen transformation. Am J Pathol. 1999;155:159–171. doi: 10.1016/S0002-9440(10)65110-3. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  51. Botchkarev VA, Welker P, Albers KM, Botchkareva NV, Metz M, Lewin GR, Bulfone-Paus S, Peters EM, Lindner G, Paus R. A new role for neurotrophin-3: involvement in the regulation of hair follicle regression (catagen). Am J Pathol. 1998;153:785–799. doi: 10.1016/S0002-9440(10)65621-0. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  52. Botchkarev VA, Botchkareva NV, Welker P, Metz M, Lewin GR, Subramaniam A, Bulfone-Paus S, Hagen E, Braun A, Lommatzsch M, Renz H, Paus AR. A new role for neurotrophins: involvement of brain-derived neurotrophic factor and neurotrophin-4 in hair cycle control. EMBO J. 1999;13:395–410. doi: 10.1096/fasebj.13.2.395. [DOI] [PubMed] [Google Scholar] · DOI
  53. Botchkarev VA, Botchkareva NV, Albers KM, Chen LH, Welker P, Paus R. A role for p75 neurotrophin receptor in the control of apoptosis-driven hair follicle regression. EMBO J. 2000;14:1931–1942. doi: 10.1096/fj.99-0930com. [DOI] [PubMed] [Google Scholar] · DOI
  54. Tobin DJ, Foitzik K, Reinheckel T, Mecklenburg L, Botchkarev VA, Peters C, Paus R. The lysosomal protease cathepsin L is an important regulator of keratinocyte and melanocyte differentiation during hair follicle morphogenesis and cycling. Am J Pathol. 2002;160:1807–1821. doi: 10.1016/S0002-9440(10)61127-3. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  55. Fuchs E, Merrill BJ, Jamora C, DasGupta R. At the roots of a never-ending cycle. Dev Cell. 2001;1:13–25. doi: 10.1016/s1534-5807(01)00022-3. [DOI] [PubMed] [Google Scholar] · DOI
  56. Alonso L, Fuchs E. Stem cells in the skin: waste not, Wnt not. Genes Dev. 2003;17:1189–1200. doi: 10.1101/gad.1086903. [DOI] [PubMed] [Google Scholar] · DOI
  57. Jamora C, DasGupta R, Kocieniewski P, Fuchs E. Links between signal transduction, transcription and adhesion in epithelial bud development. Nature. 2003;422:317–322. doi: 10.1038/nature01458. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  58. Yuhki M, Yamada M, Kawano M, Iwasato T, Itohara S, Yoshida H, Ogawa M, Mishina Y. BMPR1A signaling is necessary for hair follicle cycling and hair shaft differentiation in mice. Development. 2004;131:1825–1833. doi: 10.1242/dev.01079. [DOI] [PubMed] [Google Scholar] · DOI
  59. Niemann C, Owens DM, Hulsken J, Birchmeier W, Watt FM. Expression of DeltaNLef1 in mouse epidermis results in differentiation of hair follicles into squamous epidermal cysts and formation of skin tumours. Development. 2002;129:95–109. doi: 10.1242/dev.129.1.95. [DOI] [PubMed] [Google Scholar] · DOI
  60. Niemann C, Unden AB, Lyle S, Zouboulis CC, Toftgard R, Watt FM. Indian hedgehog and beta-catenin signaling: role in the sebaceous lineage of normal and neoplastic mammalian epidermis. Proc Natl Acad Sci USA. 2003;100(Suppl 1):S11873–S11880. doi: 10.1073/pnas.1834202100. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  61. Koster MI, Huntzinger KA, Roop DR. Epidermal differentiation: transgenic/knockout mouse models reveal genes involved in stem cell fate decisions and commitment to differentiation. J Invest Dermatol Symp Proc. 2002;7:41–45. doi: 10.1046/j.1523-1747.2002.19639.x. [DOI] [PubMed] [Google Scholar] · DOI
  62. Porter RM, Jahoda CA, Lunny DP, Henderson G, Ross J, McLean IW, Whittock NV, Wilson NJ, Reichelt J, Magin TM, Lane EB. Defolliculated (dfl): a dominant mouse mutation leading to poor sebaceous gland differentiation and total elimination of pelage follicles. J Invest Dermatol. 2002;119:32–37. doi: 10.1046/j.1523-1747.2002.01806.x. [DOI] [PubMed] [Google Scholar] · DOI
  63. Cui CY, Durmowicz M, Ottolenghi C, Hashimoto T, Griggs B, Srivastava AK, Schlessinger D. Inducible mEDA-A1 transgene mediates sebaceous gland hyperplasia and differential formation of two types of mouse hair follicles. Hum Mol Genet. 2003;12:2931–2940. doi: 10.1093/hmg/ddg325. [DOI] [PubMed] [Google Scholar] · DOI
  64. Allen M, Grachtchouk M, Sheng H, Grachtchouk V, Wang A, Wei L, Liu J, Ramirez A, Metzger D, Chambon P, Jorcano J, Dlugosz AA. Hedgehog signaling regulates sebaceous gland development. Am J Pathol. 2003;163:2173–2178. doi: 10.1016/S0002-9440(10)63574-2. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  65. Laurikkala J, Kassai Y, Pakkasjarvi L, Thesleff I, Itoh N. Identification of a secreted BMP antagonist, ectodin, integrating BMP, FGF, and SHH signals from the tooth enamel knot. Dev Biol. 2003;264:91–105. doi: 10.1016/j.ydbio.2003.08.011. [DOI] [PubMed] [Google Scholar] · DOI

Cited by

Sorted by citations

Authors
Guha, U., Mecklenburg, L., Cowin, P., Kan, L., O'Guin, W. M., D'Vizio, D., Pestell, R. G., Paus, R., & Kessler, J. A.
Affiliations
  • Albert Einstein College of Medicine (US)
  • Universität Hamburg (DE)
  • NYU Langone Health (US)
  • Northwestern University (US)
  • Georgetown University Medical Center (US)
Corresponding author
Kessler, John A.
ORCID
Venue
The American Journal of Pathology
Publisher
Elsevier BV
Published
2004-09
Volume
165
Issue
3
Pages
729-740
ISSN
0002-9440 (ISSN-L)
DOI
10.1016/s0002-9440(10)63336-6
PMC
PMC1618597
OpenAlex
W2093308245
Cited by
70
References
3
Citations by year
2026: 3 · 2024: 2 · 2023: 2 · 2022: 5 · 2021: 2 · 2020: 2 · 2019: 5 · 2018: 4 · 2017: 2 · 2016: 1 · 2015: 2 · 2014: 4 · 2012: 3
FWCI
4.31
Type
journal article
Language
en
Open access
Licence
Locations
  • American Journal Of Pathology (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • Bundesministerium für Bildung und Forschung
  • National Institutes of Health (RO1CA75503, NS 20778, NS 34758, R01CA70896)
  • Deutsche Forschungsgemeinschaft (Pa 345/8-3)
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
BMP signaling, hair follicle morphogenesis, hair cycle, noggin, catagen, anagen, telogen, sebocyte differentiation, hair follicle matrix cells, transgenic mice
MeSH terms
Noggin Protein, Animals, Carrier Proteins, Cell Differentiation, Gene Expression Regulation, Mice, Transgenic, Phosphopyruvate Hydratase, Proteins, Sebaceous Glands, Skin, Signal Transduction, Keratinocytes, Apoptosis, Hair Follicle, Bone Morphogenetic Proteins, Mice

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review