CoChat
Sign Up
Cited by 155Hair Growth and DisordersDevelopmental Biology and Gene Regulationdental development and anomalies

Hierarchical patterning modes orchestrate hair follicle morphogenesis

Open access
Glover, James D., Wells, Kirsty L., Matthäus, Franziska, Painter, Kevin J., Ho, William, Riddell, Jon, Johansson, Jeanette A., Ford, Matthew J. +4 more·2017·PLOS Biology
DOI 10.1371/journal.pbio.2002117PMC PMC5507405
Open this paper in CoChat — free accountOpen PDF

Abstract

Two theories address the origin of repeating patterns, such as hair follicles, limb digits, and intestinal villi, during development. The Turing reaction-diffusion system posits that interacting diffusible signals produced by static cells first define a prepattern that then induces cell rearrangements to produce an anatomical structure. The second theory, that of mesenchymal self-organisation, proposes that mobile cells can form periodic patterns of cell aggregates directly, without reference to any prepattern. Early hair follicle development is characterised by the rapid appearance of periodic arrangements of altered gene expression in the epidermis and prominent clustering of the adjacent dermal mesenchymal cells. We assess the contributions and interplay between reaction-diffusion and mesenchymal self-organisation processes in hair follicle patterning, identifying a network of fibroblast growth factor (FGF), wingless-related integration site (WNT), and bone morphogenetic protein (BMP) signalling interactions capable of spontaneously producing a periodic pattern. Using time-lapse imaging, we find that mesenchymal cell condensation at hair follicles is locally directed by an epidermal prepattern. However, imposing this prepattern's condition of high FGF and low BMP activity across the entire skin reveals a latent dermal capacity to undergo spatially patterned self-organisation in the absence of epithelial direction. This mesenchymal self-organisation relies on restricted transforming growth factor (TGF) β signalling, which serves to drive chemotactic mesenchymal patterning when reaction-diffusion patterning is suppressed, but, in normal conditions, facilitates cell movement to locally prepatterned sources of FGF. This work illustrates a hierarchy of periodic patterning modes operating in organogenesis.

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 · 10.1371/journal.pbio.2002117

Cites

5 of 5 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?

  • T-SKOs resembled the natural process of HF development in vivo.

    “resembled the natural process of HF development in vivo [23, 24].”

    From The empowering influence of air-liquid interface culture on skin organoid hair follicle development (2025) · cites this paper as [23]

    The Introduction describes hair follicle development in mouse embryos, including epidermal placodes and dermal condensates. The Materials and methods describe cultured embryonic skin explants, but our copy does not discuss T-SKOs or compare them with in vivo development (searched: T-SKO, skin organoid, and resemblance to in vivo development). (LLM, conf=0.73)

    Experimental — accuracy not yet measured

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: 78

  1. [1]Held LI. Models for embryonic periodicity. New York: Karger; 1992. 1501607
  2. [2]Turing AM. The Chemical Basis of Morphogenesis. Philos Trans R Soc Lond B Biol Sci. 1952; 237(641): 37– 72. PMC4360114 25750229
  3. [3]Gierer A, Meinhardt H. A theory of biological pattern formation. Biol Cybern. 1972; 12(1): 30– 9. 4663624
  4. [4]Painter KJ, Hunt GS, Wells KL, Johansson JA, Headon DJ. Towards an integrated experimental-theoretical approach for assessing the mechanistic basis of hair and feather morphogenesis. Interface Focus. 2012; 2(4): 433– 50. doi: 10.1098/rsfs.2011.0122 23919127 PMC3363042 · DOI
  5. [5]Klika V, Baker RE, Headon D, Gaffney EA. The influence of receptor-mediated interactions on reaction-diffusion mechanisms of cellular self-organisation. Bull Math Biol. 2012; 74(4): 935– 57. doi: 10.1007/s11538-011-9699-4 22072186 · DOI
  6. [6]Korvasova K, Gaffney EA, Maini PK, Ferreira MA, Klika V. Investigating the Turing conditions for diffusion-driven instability in the presence of a binding immobile substrate. J Theor Biol. 2015; 367: 286– 95. doi: 10.1016/j.jtbi.2014.11.024 25484005 · DOI
  7. [7]Marcon L, Diego X, Sharpe J, Muller P. High-throughput mathematical analysis identifies Turing networks for patterning with equally diffusing signals. Elife. 2016; 5: e14022 doi: 10.7554/eLife.14022 27058171 PMC4922859 · DOI
  8. [8]Harris AK, Stopak D, Warner P. Generation of spatially periodic patterns by a mechanical instability: a mechanical alternative to the Turing model. J Embryol Exp Morphol. 1984; 80: 1– 20. 6747520
  9. [9]Oster GF, Murray JD, Harris AK. Mechanical aspects of mesenchymal morphogenesis. J Embryol Exp Morphol. 1983; 78: 83– 125. 6663234
  10. [10]Vaughan BL, Baker RE, Kay D, Maini PK. A Modified Oster-Murray-Harris Mechanical Model of Morphogenesis. Siam Journal on Applied Mathematics. 2013; 73(6): 2124– 42.
  11. [11]Oster GF, Murray JD. Pattern formation models and developmental constraints. J Exp Zool. 1989; 251(2): 186– 202. doi: 10.1002/jez.1402510207 2671251 · DOI
  12. [12]Maini PK, Myerscough MR, Winters KH, Murray JD. Bifurcating Spatially Heterogeneous Solutions in a Chemotaxis Model for Biological Pattern Generation. Bull Math Biol. 1991; 53(5): 701– 19. 1933036
  13. [13]Keller EF, Segel LA. Initiation of slime mold aggregation viewed as an instability. J Theor Biol. 1970; 26(3): 399– 415. 5462335
  14. [14]Miura T, Shiota K. Extracellular matrix environment influences chondrogenic pattern formation in limb bud micromass culture: experimental verification of theoretical models. Anat Rec. 2000; 258(1): 100– 7. 10603453
  15. [15]Watanabe M, Kondo S. Is pigment patterning in fish skin determined by the Turing mechanism? Trends Genet. 2015; 31(2): 88– 96. doi: 10.1016/j.tig.2014.11.005 25544713 · DOI
  16. [16]Hiscock TW, Megason SG. Mathematically guided approaches to distinguish models of periodic patterning. Development. 2015; 142(3): 409– 19. doi: 10.1242/dev.107441 25605777 PMC4302999 · DOI
  17. [17]Meinhardt H, Gierer A. Pattern formation by local self-activation and lateral inhibition. Bioessays. 2000; 22(8): 753– 60. doi: 10.1002/1521-1878(200008)22:8<753::AID-BIES9>3.0.CO;2-Z 10918306 · DOI
  18. [18]Schmidt-Ullrich R, Paus R. Molecular principles of hair follicle induction and morphogenesis. Bioessays. 2005; 27(3): 247– 61. doi: 10.1002/bies.20184 15714560 · DOI
  19. [19]Biggs LC, Mikkola ML. Early inductive events in ectodermal appendage morphogenesis. Semin Cell Dev Biol. 2014; 25–26: 11– 21. doi: 10.1016/j.semcdb.2014.01.007 24487243 · DOI
  20. [20]Ahtiainen L, Lefebvre S, Lindfors PH, Renvoise E, Shirokova V, Vartiainen MK, et al Directional cell migration, but not proliferation, drives hair placode morphogenesis. Dev Cell. 2014; 28(5): 588– 602. doi: 10.1016/j.devcel.2014.02.003 24636260 · DOI
  21. [21]Cheng CW, Niu B, Warren M, Pevny LH, Lovell-Badge R, Hwa T, et al Predicting the spatiotemporal dynamics of hair follicle patterns in the developing mouse. Proc Natl Acad Sci U S A. 2014; 111(7): 2596– 601. doi: 10.1073/pnas.1313083111 24550288 PMC3932898 · DOI
  22. [22]Mou C, Jackson B, Schneider P, Overbeek PA, Headon DJ. Generation of the primary hair follicle pattern. Proc Natl Acad Sci U S A. 2006; 103(24): 9075– 80. doi: 10.1073/pnas.0600825103 16769906 PMC1482568 · DOI · Paper page
  23. [23]Morgan BA. The dermal papilla: an instructive niche for epithelial stem and progenitor cells in development and regeneration of the hair follicle. Cold Spring Harb Perspect Med. 2014; 4(7): a015180 doi: 10.1101/cshperspect.a015180 24985131 PMC4066645 · DOI
  24. [24]Hardy MH. The secret life of the hair follicle. Trends Genet. 1992; 8(2): 55– 61. 1566372
  25. [25]Zhang Y, Tomann P, Andl T, Gallant NM, Huelsken J, Jerchow B, et al Reciprocal requirements for EDA/EDAR/NF-kappaB and Wnt/beta-catenin signaling pathways in hair follicle induction. Dev Cell. 2009; 17(1): 49– 61. doi: 10.1016/j.devcel.2009.05.011 19619491 PMC2859042 · DOI
  26. [27]Huh SH, Narhi K, Lindfors PH, Haara O, Yang L, Ornitz DM, et al Fgf20 governs formation of primary and secondary dermal condensations in developing hair follicles. Genes Dev. 2013; 27(4): 450– 8. doi: 10.1101/gad.198945.112 23431057 PMC3589561 · DOI
  27. [28]Botchkarev VA, Botchkareva NV, Roth W, Nakamura M, Chen LH, Herzog W, et al Noggin is a mesenchymally derived stimulator of hair-follicle induction. Nat Cell Biol. 1999; 1(3): 158– 64. doi: 10.1038/11078 10559902 · DOI
  28. [29]Pummila M, Fliniaux I, Jaatinen R, James MJ, Laurikkala J, Schneider P, et al Ectodysplasin has a dual role in ectodermal organogenesis: inhibition of Bmp activity and induction of Shh expression. Development. 2007; 134(1): 117– 25. doi: 10.1242/dev.02708 17164417 · DOI
  29. [31]Narhi K, Jarvinen E, Birchmeier W, Taketo MM, Mikkola ML, Thesleff I. Sustained epithelial beta-catenin activity induces precocious hair development but disrupts hair follicle down-growth and hair shaft formation. Development. 2008; 135(6): 1019– 28. doi: 10.1242/dev.016550 18256193 · DOI
  30. [32]Zhang Y, Andl T, Yang SH, Teta M, Liu F, Seykora JT, et al Activation of beta-catenin signaling programs embryonic epidermis to hair follicle fate. Development. 2008; 135(12): 2161– 72. doi: 10.1242/dev.017459 18480165 PMC2516408 · DOI
  31. [33]Petiot A, Conti FJ, Grose R, Revest JM, Hodivala-Dilke KM, Dickson C. A crucial role for Fgfr2-IIIb signalling in epidermal development and hair follicle patterning. Development. 2003; 130(22): 5493– 501. doi: 10.1242/dev.00788 14530295 · DOI
  32. [35]Andl T, Ahn K, Kairo A, Chu EY, Wine-Lee L, Reddy ST, et al Epithelial Bmpr1a regulates differentiation and proliferation in postnatal hair follicles and is essential for tooth development. Development. 2004; 131(10): 2257– 68. doi: 10.1242/dev.01125 15102710 · DOI
  33. [36]Jiang TX, Jung HS, Widelitz RB, Chuong CM. Self-organization of periodic patterns by dissociated feather mesenchymal cells and the regulation of size, number and spacing of primordia. Development. 1999; 126(22): 4997– 5009. 10529418
  34. [37]Levy V, Lindon C, Harfe BD, Morgan BA. Distinct stem cell populations regenerate the follicle and interfollicular epidermis. Dev Cell. 2005; 9(6): 855– 61. doi: 10.1016/j.devcel.2005.11.003 16326396 · DOI
  35. [38]St-Jacques B, Dassule HR, Karavanova I, Botchkarev VA, Li J, Danielian PS, et al Sonic hedgehog signaling is essential for hair development. Curr Biol. 1998; 8(19): 1058– 68. 9768360
  36. [39]Sick S, Reinker S, Timmer J, Schlake T. WNT and DKK determine hair follicle spacing through a reaction-diffusion mechanism. Science. 2006; 314(5804): 1447– 50. doi: 10.1126/science.1130088 17082421 · DOI · Paper page
  37. [40]Schmidt-Ullrich R, Tobin DJ, Lenhard D, Schneider P, Paus R, Scheidereit C. NF-kappaB transmits Eda A1/EdaR signalling to activate Shh and cyclin D1 expression, and controls post-initiation hair placode down growth. Development. 2006; 133(6): 1045– 57. doi: 10.1242/dev.02278 16481354 · DOI · Paper page
  38. [41]Fliniaux I, Mikkola ML, Lefebvre S, Thesleff I. Identification of dkk4 as a target of Eda-A1/Edar pathway reveals an unexpected role of ectodysplasin as inhibitor of Wnt signalling in ectodermal placodes. Dev Biol. 2008; 320(1): 60– 71. doi: 10.1016/j.ydbio.2008.04.023 18508042 · DOI
  39. [42]Bazzi H, Fantauzzo KA, Richardson GD, Jahoda CA, Christiano AM. The Wnt inhibitor, Dickkopf 4, is induced by canonical Wnt signaling during ectodermal appendage morphogenesis. Dev Biol. 2007; 305(2): 498– 507. doi: 10.1016/j.ydbio.2007.02.035 17397822 · DOI
  40. [43]Ferrer-Vaquer A, Piliszek A, Tian G, Aho RJ, Dufort D, Hadjantonakis AK. A sensitive and bright single-cell resolution live imaging reporter of Wnt/ss-catenin signaling in the mouse. BMC Dev Biol. 2010; 10: 121 doi: 10.1186/1471-213X-10-121 21176145 PMC3017038 · DOI
  41. [44]Gay D, Kwon O, Zhang Z, Spata M, Plikus MV, Holler PD, et al Fgf9 from dermal gammadelta T cells induces hair follicle neogenesis after wounding. Nat Med. 2013; 19(7): 916– 23. doi: 10.1038/nm.3181 23727932 PMC4054871 · DOI
  42. [45]Kurics T, Menshykau D, Iber D. Feedback, receptor clustering, and receptor restriction to single cells yield large Turing spaces for ligand-receptor-based Turing models. Phys Rev E Stat Nonlin Soft Matter Phys. 2014; 90(2): 022716 doi: 10.1103/PhysRevE.90.022716 25215767 · DOI
  43. [46]Plikus M, Wang WP, Liu 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 morphogenic protein pathway. Am J Pathol. 2004; 164(3): 1099– 114. doi: 10.1016/S0002-9440(10)63197-5 14982863 PMC1614723 · DOI
  44. [47]Cui CY, Kunisada M, Piao Y, Childress V, Ko MS, Schlessinger D. Dkk4 and Eda regulate distinctive developmental mechanisms for subtypes of mouse hair. PLoS One. 2010; 5(4): e10009 doi: 10.1371/journal.pone.0010009 20386733 PMC2850388 · DOI
  45. [48]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(2): 278– 89. doi: 10.1006/dbio.1999.9325 10433821 · DOI
  46. [49]Gazzerro E, Gangji V, Canalis E. Bone morphogenetic proteins induce the expression of noggin, which limits their activity in cultured rat osteoblasts. J Clin Invest. 1998; 102(12): 2106– 14. doi: 10.1172/JCI3459 9854046 PMC509165 · DOI
  47. [50]Grotewold L, Plum M, Dildrop R, Peters T, Ruther U. Bambi is coexpressed with Bmp-4 during mouse embryogenesis. Mech Dev. 2001; 100(2): 327– 30. 11165491
  48. [51]Song HK, Lee SH, Goetinck PF. FGF-2 signaling is sufficient to induce dermal condensations during feather development. Dev Dyn. 2004; 231(4): 741– 9. doi: 10.1002/dvdy.20243 15532057 · DOI
  49. [52]Lin CM, Jiang TX, Baker RE, Maini PK, Widelitz RB, Chuong CM. Spots and stripes: pleomorphic patterning of stem cells via p-ERK-dependent cell chemotaxis shown by feather morphogenesis and mathematical simulation. Dev Biol. 2009; 334(2): 369– 82. doi: 10.1016/j.ydbio.2009.07.036 19647731 PMC2811698 · DOI
  50. [53]Tsai SY, Sennett R, Rezza A, Clavel C, Grisanti L, Zemla R, et al Wnt/beta-catenin signaling in dermal condensates is required for hair follicle formation. Dev Biol. 2014; 385(2): 179– 88. doi: 10.1016/j.ydbio.2013.11.023 24309208 PMC3933391 · DOI
  51. [54]Sennett R, Wang Z, Rezza A, Grisanti L, Roitershtein N, Sicchio C, et al An Integrated Transcriptome Atlas of Embryonic Hair Follicle Progenitors, Their Niche, and the Developing Skin. Dev Cell. 2015; 34(5): 577– 91. doi: 10.1016/j.devcel.2015.06.023 26256211 PMC4573840 · DOI · Paper page
  52. [56]Economou AD, Ohazama A, Porntaveetus T, Sharpe PT, Kondo S, Basson MA, et al Periodic stripe formation by a Turing mechanism operating at growth zones in the mammalian palate. Nat Genet. 2012; 44(3): 348– 51. doi: 10.1038/ng.1090 22344222 PMC3303118 · DOI
  53. [57]Yamaguchi M, Yoshimoto E, Kondo S. Pattern regulation in the stripe of zebrafish suggests an underlying dynamic and autonomous mechanism. Proc Natl Acad Sci U S A. 2007; 104(12): 4790– 3. doi: 10.1073/pnas.0607790104 17360399 PMC1820822 · DOI
  54. [58]Pelton RW, Nomura S, Moses HL, Hogan BL. Expression of transforming growth factor beta 2 RNA during murine embryogenesis. Development. 1989; 106(4): 759– 67. 2485246
  55. [59]Tomann P, Paus R, Millar SE, Scheidereit C, Schmidt-Ullrich R. Lhx2 is a direct NF-kappaB target gene that promotes primary hair follicle placode down-growth. Development. 2016; 143(9): 1512– 22. doi: 10.1242/dev.130898 26952977 PMC6514410 · DOI
  56. [60]Ting-Berreth SA, Chuong CM. Local delivery of TGF beta2 can substitute for placode epithelium to induce mesenchymal condensation during skin appendage morphogenesis. Dev Biol. 1996; 179(2): 347– 59. doi: 10.1006/dbio.1996.0266 8903351 · DOI
  57. [61]Postlethwaite AE, Keski-Oja J, Moses HL, Kang AH. Stimulation of the chemotactic migration of human fibroblasts by transforming growth factor beta. J Exp Med. 1987; 165(1): 251– 6. 3491869 PMC2188256
  58. [62]Verrecchia F, Mauviel A. Transforming growth factor-beta signaling through the Smad pathway: role in extracellular matrix gene expression and regulation. J Invest Dermatol. 2002; 118(2): 211– 5. doi: 10.1046/j.1523-1747.2002.01641.x 11841535 · DOI
  59. [63]Wang H, Radjendirane V, Wary KK, Chakrabarty S. Transforming growth factor beta regulates cell-cell adhesion through extracellular matrix remodeling and activation of focal adhesion kinase in human colon carcinoma Moser cells. Oncogene. 2004; 23(32): 5558– 61. doi: 10.1038/sj.onc.1207701 15133493 · DOI
  60. [64]Havis E, Bonnin MA, Olivera-Martinez I, Nazaret N, Ruggiu M, Weibel J, et al Transcriptomic analysis of mouse limb tendon cells during development. Development. 2014; 141(19): 3683– 96. doi: 10.1242/dev.108654 25249460 · DOI
  61. [65]Ferguson JW, Mikesh MF, Wheeler EF, LeBaron RG. Developmental expression patterns of Beta-ig (betaIG-H3) and its function as a cell adhesion protein. Mech Dev. 2003; 120(8): 851– 64. 12963107
  62. [66]Adams JC, Lawler J. The thrombospondins. Cold Spring Harb Perspect Biol. 2011; 3(10): a009712 doi: 10.1101/cshperspect.a009712 21875984 PMC3179333 · DOI
  63. [67]Lu P, Takai K, Weaver VM, Werb Z. Extracellular matrix degradation and remodeling in development and disease. Cold Spring Harb Perspect Biol. 2011; 3(12): a005058 doi: 10.1101/cshperspect.a005058 21917992 PMC3225943 · DOI · Paper page
  64. [68]Hynes RO. The extracellular matrix: not just pretty fibrils. Science. 2009; 326(5957): 1216– 9. doi: 10.1126/science.1176009 19965464 PMC3536535 · DOI · Paper page
  65. [70]Raspopovic J, Marcon L, Russo L, Sharpe J. Modeling digits. Digit patterning is controlled by a Bmp-Sox9-Wnt Turing network modulated by morphogen gradients. Science. 2014; 345(6196): 566– 70. doi: 10.1126/science.1252960 25082703 · DOI
  66. [71]Moore GP, Jackson N, Isaacs K, Brown G. Pattern and morphogenesis in skin. J Theor Biol. 1998; 191(1): 87– 94. doi: 10.1006/jtbi.1997.0567 9593659 · DOI
  67. [72]Driskell RR, Lichtenberger BM, Hoste E, Kretzschmar K, Simons BD, Charalambous M, et al Distinct fibroblast lineages determine dermal architecture in skin development and repair. Nature. 2013; 504(7479): 277– 81. doi: 10.1038/nature12783 24336287 PMC3868929 · DOI · Paper page
  68. [73]Bard JB. Traction and the formation of mesenchymal condensations in vivo. Bioessays. 1990; 12(8): 389– 95. doi: 10.1002/bies.950120809 2241937 · DOI
  69. [74]Jahoda CA, Oliver RF. Vibrissa dermal papilla cell aggregative behaviour in vivo and in vitro. J Embryol Exp Morphol. 1984; 79: 211– 24. 6716045
  70. [75]Takebe T, Enomura M, Yoshizawa E, Kimura M, Koike H, Ueno Y, et al Vascularized and Complex Organ Buds from Diverse Tissues via Mesenchymal Cell-Driven Condensation. Cell Stem Cell. 2015; 16(5): 556– 65. doi: 10.1016/j.stem.2015.03.004 25891906 · DOI
  71. [76]Miura T, Komori M, Shiota K. A novel method for analysis of the periodicity of chondrogenic patterns in limb bud cell culture: correlation of in vitro pattern formation with theoretical models. Anat Embryol (Berl). 2000; 201(5): 419– 28. 10839636
  72. [77]Zeng W, Thomas GL, Glazier JA. Non-Turing stripes and spots: a novel mechanism for biological cell clustering. Physica a-Statistical Mechanics and Its Applications. 2004; 341: 482– 94.
  73. [78]Salazar-Ciudad I, Garcia-Fernandez J, Sole RV. Gene networks capable of pattern formation: from induction to reaction-diffusion. J Theor Biol. 2000; 205(4): 587– 603. doi: 10.1006/jtbi.2000.2092 10931754 · DOI
  74. [79]Salazar-Ciudad I, Sole RV, Newman SA. Phenotypic and dynamical transitions in model genetic networks. II. Application to the evolution of segmentation mechanisms. Evol Dev. 2001; 3(2): 95– 103. 11341678
  75. [80]Salazar-Ciudad I, Jernvall J, Newman SA. Mechanisms of pattern formation in development and evolution. Development. 2003; 130(10): 2027– 37. 12668618
  76. [81]Mort RL, Keighren M, Hay L, Jackson IJ. Ex vivo culture of mouse embryonic skin and live-imaging of melanoblast migration. J Vis Exp. 2014(87): doi: 10.3791/51352 24894489 PMC4193345 · DOI
  77. [82]Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012; 9(7): 676– 82. doi: 10.1038/nmeth.2019 22743772 PMC3855844 · DOI · Paper page
  78. [83]Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012; 9(7): 671– 5. 22930834 PMC5554542

Cited by

Sorted by citations

Authors
Glover, J. D., Wells, K. L., Matthäus, F., Painter, K. J., Ho, W., Riddell, J., Johansson, J. A., Ford, M. J., Jahoda, C. A. B., Klika, V., Mort, R. L., & Headon, D. J.
Affiliations
  • Roslin Institute (GB)
  • Goethe University Frankfurt (DE)
  • Heriot-Watt University (GB)
  • Western General Hospital (GB)
  • Durham University (GB)
  • Lancaster University (GB)
Corresponding author
Headon, Denis J.
ORCID
Venue
PLOS Biology
Publisher
Public Library of Science (PLoS)
Published
2017-07-11
Volume
15
Issue
7
Pages
e2002117
ISSN
  • 1544-9173 (ISSN-L)
  • 1545-7885
DOI
10.1371/journal.pbio.2002117
PMC
PMC5507405
OpenAlex
W2735125533
Cited by
155
References
5
Citations by year
2026: 17 · 2025: 12 · 2024: 25 · 2023: 12 · 2022: 14 · 2021: 18 · 2020: 17 · 2019: 22 · 2018: 13 · 2017: 5
FWCI
21.82
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS Biology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Durham Research Online (Durham University) (acceptedVersion, other-oa)
  • PORTO@Iris (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Lancaster EPrints (Lancaster University) (submittedVersion)
  • Figshare (submittedVersion, cc-by)
  • Durham Research Online (Durham University) (submittedVersion, cc-by)
  • Publication Server of Goethe University Frankfurt am Main (Goethe University Frankfurt) (submittedVersion, cc-by)
  • Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, cc-by)
Funders
Biotechnology and Biological Sciences Research Council (BBS/E/D/10002071, BB/J017183/1, BB/J004316/1, BB/P013732/1, BB/N008545/1, 1076855, BBS/E/D/20221657)
Topics
  • Health Sciences › Medicine › Urology › Hair Growth and Disorders
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › dental development and anomalies
Keywords
hair follicle morphogenesis, reaction-diffusion, epithelial-mesenchymal interactions, FGF signaling, Wnt signaling, BMP signaling, TGF-beta signaling, prepattern, organogenesis, epidermis
MeSH terms
Animals, Cell Differentiation, Female, Male, Mice, Inbred Strains, Skin, Signal Transduction, Transforming Growth Factor beta, Hair Follicle, Body Patterning, Gene Expression Profiling, 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