Microenvironmental reprogramming by threedimensional culture enables dermal papilla cells to induce de novo human hair-follicle growth

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 49, 2013, Pages 19679-19688

  Higgins, Claire A ^a   Chen, James C ^b,c   Cerise, Jane E ^a   Jahoda, Colin A B ^d   Christiano, Angela M ^a,b  

^a Departments of Dermatology   (United States)

^b Departments of Genetics and Development   (United States)

^c Och Spine at New York Presbyterian Hospitals   (United States)

^d DURHAM UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTOME;

ARTICLE; CELL REGENERATION; GENE EXPRESSION; HAIR FOLLICLE; HAIR GROWTH; HUMAN; HUMAN CELL; MICROENVIRONMENT; PRIORITY JOURNAL; SKIN CELL; TUMOR SPHEROID; BIOLOGY; CULTURE TECHNIQUE; CYTOLOGY; DERMIS; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION PROFILING; MICROARRAY ANALYSIS; MULTICELLULAR SPHEROID; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REGENERATION; SYSTEMS BIOLOGY; TUMOR MICROENVIRONMENT;

CELL CULTURE TECHNIQUES; CELLULAR MICROENVIRONMENT; COMPUTATIONAL BIOLOGY; DERMIS; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION PROFILING; HAIR FOLLICLE; HUMANS; MICROARRAY ANALYSIS; REAL-TIME POLYMERASE CHAIN REACTION; REGENERATION; SPHEROIDS, CELLULAR; SYSTEMS BIOLOGY;

EID: 84889688816     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1309970110     Document Type: Article

References (62)

1. Pinkus H (1958) The Biology of Hair Growth, eds Montagna W, Ellis RA (Academic, New York), pp 1-32.
2. Jacobson CM (1966) A comparative study of the mechanisms by which X-irradiation and genetic mutation cause loss of vibrissae in embryo mice. J Embryol Exp Morphol 16(2):369-379.
3. Kollar EJ (1970) The induction of hair follicles by embryonic dermal papillae. J Invest Dermatol 55(6):374-378.
4. Dhouailly D (1973) Dermo-epidermal interactions between birds and mammals: Differentiation of cutaneous appendages. J Embryol Exp Morphol 30(3):587-603.
5. Millar SE (2002) Molecular mechanisms regulating hair follicle development. J InvestDermatol 118(2):216-225.
6. Ito M, et al. (2007) Wnt-dependent de novo hair follicle regeneration in adult mouse skin after wounding. Nature 447(7142):316-320.
7. Cohen J (1961) The transplantation of individual rat and guineapig whisker papillae. J Embryol Exp Morphol 9:117-127.
8. Oliver RF (1970) The induction of hair follicle formation in the adult hooded rat by vibrissa dermal papillae. J Embryol Exp Morphol 23(1):219-236.
9. Jahoda CA, Horne KA, Oliver RF (1984) Induction of hair growth by implantation of cultured dermal papilla cells. Nature 311(5986):560-562.
10. Kishimoto J, Burgeson RE, Morgan BA (2000) Wnt signaling maintains the hairinducing activity of the dermal papilla. Genes Dev 14(10):1181-1185.
11. Rendl M, Polak L, Fuchs E (2008) BMP signaling in dermal papilla cells is required for their hair follicle-inductive properties. Genes Dev 22(4):543-557.
12. Cooley J (2004) Follicular cell implantation: An update on "hair follicle cloning" Facial Plast Surg Clin North Am 12(2):219-224.
13. Teumer J, Cooley J (2005) Follicular cell implantation: An emerging cell therapy for hair loss. Semin Plast Surg 19(2):194-200.
14. Reynolds AJ, Lawrence C, Cserhalmi-Friedman PB, Christiano AM, Jahoda CA (1999) Trans-gender induction of hair follicles. Nature 402(6757):33-34.
15. Jahoda CA, et al. (2001) Trans-species hair growth induction by human hair follicle dermal papillae. Exp Dermatol 10(4):229-237.
16. Reynolds AJ, Jahoda CA (1996) Hair matrix germinative epidermal cells confer follicleinducing capabilities on dermal sheath and high passage papilla cells. Development 122(10):3085-3094.
17. Ouji Y, Nakamura-Uchiyama F, Yoshikawa M (2013) Canonical Wnts, specifically Wnt- 10b, show ability to maintain dermal papilla cells. Biochem Biophys Res Commun 438(3):493-499.
18. Ohyama M, Kobayashi T, Sasaki T, Shimizu A, Amagai M (2012) Restoration of the intrinsic properties of human dermal papilla in vitro. J Cell Sci 125(Pt 17):4114-4125.
19. Qiao J, et al. (2009) Hair follicle neogenesis induced by cultured human scalp dermal papilla cells. Regen Med 4(5):667-676.
20. Jahoda CA, Oliver RF (1984) Vibrissa dermal papilla cell aggregative behaviour in vivo and in vitro. J Embryol Exp Morphol 79:211-224.
21. Birgersdotter A, Sandberg R, Ernberg I (2005) Gene expression perturbation in vitro - a growing case for three-dimensional (3D) culture systems. Semin Cancer Biol 15(5): 405-412.
22. Higgins CA, Richardson GD, Ferdinando D, Westgate GE, Jahoda CA (2010) Modelling the hair follicle dermal papilla using spheroid cell cultures. Exp Dermatol 19(6): 546-548.
23. Trapp BD, Honegger P, Richelson E, Webster HD (1979) Morphological differentiation of mechanically dissociated fetal rat brain in aggregating cell cultures. Brain Res 160(1):117-130.
24. Shimomura Y, et al. (2010) APCDD1 is a novel Wnt inhibitor mutated in hereditary hypotrichosis simplex. Nature 464(7291):1043-1047.
25. Kratochwil K, Dull M, Farinas I, Galceran J, Grosschedl R (1996) Lef1 expression is activated by BMP-4 and regulates inductive tissue interactions in tooth and hair development. Genes Dev 10(11):1382-1394.
26. Goodarzi H, Elemento O, Tavazoie S (2009) Revealing global regulatory perturbationsacross human cancers. Mol Cell 36(5):900-911.
27. Andl T, Reddy ST, Gaddapara T, Millar SE (2002) WNT signals are required for the initiation of hair follicle development. Dev Cell 2(5):643-653.
28. Schmeichel KL, Bissell MJ (2003) Modeling tissue-specific signaling and organ function in three dimensions. J Cell Sci 116(Pt 12):2377-2388.
29. Eichler GS, Huang S, Ingber DE (2003) Gene Expression Dynamics Inspector (GEDI): For integrative analysis of expression profiles. Bioinformatics 19(17):2321-2322.
30. Greco V, et al. (2009) A two-step mechanism for stem cell activation during hair regeneration.Cell Stem Cell 4(2):155-169.
31. Rendl M, Lewis L, Fuchs E (2005) Molecular dissection of mesenchymal-epithelial interactions in the hair follicle. PLoS Biol 3(11):e331.
32. Ito Y, et al. (2007) Isolation of murine hair-inducing cells using the cell surface marker prominin-1/CD133. J Invest Dermatol 127(5):1052-1060.
33. Närhi K, et al. (2012) Sostdc1 defines the size and number of skin appendage placodes. Dev Biol 364(2):149-161.
34. van Genderen C, et al. (1994) Development of several organs that require inductive epithelial-mesenchymal interactions is impaired in LEF-1-deficient mice. Genes Dev 8(22):2691-2703.
35. Clavel C, et al. (2012) Sox2 in the dermal papilla niche controls hair growth by finetuning BMP signaling in differentiating hair shaft progenitors. Dev Cell 23(5): 981-994.
36. Kulessa H, Turk G, Hogan BL (2000) Inhibition of Bmp signaling affects growth and differentiation in the anagen hair follicle. EMBO J 19(24):6664-6674.
37. Plikus MV, et al. (2008) Cyclic dermal BMP signalling regulates stem cell activation during hair regeneration. Nature 451(7176):340-344.
38. Thomas PD, et al. (2003) PANTHER: A browsable database of gene products organized by biological function, using curated protein family and subfamily classification. Nucleic Acids Res 31(1):334-341.
39. Margolin AA, et al. (2006) ARACNE: An algorithm for the reconstruction of gene regulatory networks in a mammalian cellular context. BMC Bioinformatics 7(Suppl 1):S7.
40. Lefebvre C, et al. (2010) A human B-cell interactome identifies MYB and FOXM1 as master regulators of proliferation in germinal centers. Mol Syst Biol 6:377.
41. Asano Y, et al. (2009) Transcription factor Fli1 regulates collagen fibrillogenesis in mouse skin. Mol Cell Biol 29(2):425-434.
42. Skokowa J, et al. (2012) Interactions among HCLS1, HAX1 and LEF-1 proteins are essential for G-CSF-triggered granulopoiesis. Nat Med 18(10):1550-1559.
43. Chen D, Jarrell A, Guo C, Lang R, Atit R (2012) Dermal ß-catenin activity in response to epidermal Wnt ligands is required for fibroblast proliferation and hair follicle initiation. Development 139(8):1522-1533.
44. Myung PS, Takeo M, Ito M, Atit RP (2013) Epithelial Wnt ligand secretion is required for adult hair follicle growth and regeneration. J Invest Dermatol 133(1):31-41.
45. Barna M, Pandolfi PP, Niswander L (2005) Gli3 and Plzf cooperate in proximal limb patterning at early stages of limb development. Nature 436(7048):277-281.
46. Toyoshima KE, et al. (2012) Fully functional hair follicle regeneration through the rearrangement of stem cells and their niches. Nat Commun 3:784.
47. Kang BM, Kwack MH, Kim MK, Kim JC, Sung YK (2012) Sphere formation increases the ability of cultured human dermal papilla cells to induce hair follicles from mouse epidermal cells in a reconstitution assay. J Invest Dermatol 132(1):237-239.
48. Messenger AG, Senior HJ, Bleehen SS (1986) The in vitro properties of dermal papilla cell lines established from human hair follicles. Br J Dermatol 114(4):425-430.
49. Jahoda CA (1998) Cellular and developmental aspects of androgenetic alopecia. Exp Dermatol 7(5):235-248.
50. Huang YC, et al. (2013) Scalable production of controllable dermal papilla spheroids on PVA surfaces and the effects of spheroid size on hair follicle regeneration. Biomaterials 34(2):442-451.
51. Tung YC, et al. (2011) High-throughput 3D spheroid culture and drug testing using a 384 hanging drop array. Analyst (Lond) 136(3):473-478.
52. Messenger AG, Rundegren J (2004) Minoxidil: Mechanisms of action on hair growth. Br J Dermatol 150(2):186-194.
53. Nelson CM, Bissell MJ (2005) Modeling dynamic reciprocity: Engineering threedimensional culture models of breast architecture, function, and neoplastic transformation. Semin Cancer Biol 15(5):342-352.
54. Lee GY, Kenny PA, Lee EH, Bissell MJ (2007) Three-dimensional culture models of normal and malignant breast epithelial cells. Nat Methods 4(4):359-365.
55. Spencer VA, Xu R, Bissell MJ (2010) Gene expression in the third dimension: The ECMnucleus connection. J Mammary Gland Biol Neoplasia 15(1):65-71.
56. Gurdon JB (1988) A community effect in animal development. Nature 336(6201): 772-774.
57. Saka Y, Lhoussaine C, Kuttler C, Ullner E, Thiel M (2011) Theoretical basis of the community effect in development. BMC Syst Biol 5:54.
58. Zimber MP, et al. (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(11):1308-1312.
59. Jahoda CA, Christiano AM (2011) Niche crosstalk: Intercellular signals at the hair follicle. Cell 146(5):678-681.
60. Carro MS, et al. (2010) The transcriptional network for mesenchymal transformation of brain tumours. Nature 463(7279):318-325.
61. Basso K, et al. (2005) Reverse engineering of regulatory networks in human B cells. Nat Genet 37(4):382-390.
62. Mani KM, et al. (2008) A systems biology approach to prediction of oncogenes and molecular perturbation targets in B-cell lymphomas. Mol Syst Biol 4:169.