A multi-scale model for hair follicles reveals heterogeneous domains driving rapid spatiotemporal hair growth patterning

Qixuan Wang, Ji Won Oh, Hye Lim Lee, Anukriti Dhar, Tao Peng, Raul Ramos, Christian Fernando Guerrero-Juarez, Xiaojie Wang, Ran Zhao, Xiaoling Cao, Jonathan Le, Melisa A. Fuentes, Shelby C. Jocoy, Antoni R. Rossi, Brian Vu, Kim Pham, Xiaoyang Wang, Nanda Maya Mali, Jung Min Park, June Hyug Choi & 12 others Hyunsu Lee, Julien M.D. Legrand, Eve Kandyba, Jung Chul Kim, Moonkyu Kim, John Foley, Zhengquan Yu, Krzysztof Kobielak, Bogi Andersen, Kiarash Khosrotehrani, Qing Nie, Maksim V. Plikus

Research output: Contribution to journalArticle

12 Citations (Scopus)

Abstract

The control principles behind robust cyclic regeneration of hair follicles (HFs) remain unclear. Using multi-scale modeling, we show that coupling inhibitors and activators with physical growth of HFs is sufficient to drive periodicity and excitability of hair regeneration. Model simulations and experimental data reveal that mouse skin behaves as a heterogeneous regenerative field, composed of anatomical domains where HFs have distinct cycling dynamics. Interactions between fast-cycling chin and ventral HFs and slow-cycling dorsal HFs produce bilaterally symmetric patterns. Ear skin behaves as a hyper-refractory domain with HFs in extended rest phase. Such hyper-refractivity relates to high levels of BMP ligands and WNT antagonists, in part expressed by ear-specific cartilage and muscle. Hair growth stops at the boundaries with hyper-refractory ears and anatomically discontinuous eyelids, generating wave-breaking effects. We posit that similar mechanisms for coupled regeneration with dominant activator, hyper-refractory, and wave-breaker regions can operate in other actively renewing organs.

Original languageEnglish (US)
Article numbere22772
JournaleLife
Volume6
DOIs
StatePublished - Jul 11 2017

Fingerprint

Hair Follicle
Refractory materials
Hair
Skin
Growth
Regeneration
Cartilage
Ear
Muscle
Refractive index
Ear Cartilage
Ligands
Chin
Periodicity
Eyelids
Theoretical Models
Muscles

ASJC Scopus subject areas

  • Neuroscience(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Immunology and Microbiology(all)

Cite this

Wang, Q., Oh, J. W., Lee, H. L., Dhar, A., Peng, T., Ramos, R., ... Plikus, M. V. (2017). A multi-scale model for hair follicles reveals heterogeneous domains driving rapid spatiotemporal hair growth patterning. eLife, 6, [e22772]. https://doi.org/10.7554/eLife.22772

A multi-scale model for hair follicles reveals heterogeneous domains driving rapid spatiotemporal hair growth patterning. / Wang, Qixuan; Oh, Ji Won; Lee, Hye Lim; Dhar, Anukriti; Peng, Tao; Ramos, Raul; Guerrero-Juarez, Christian Fernando; Wang, Xiaojie; Zhao, Ran; Cao, Xiaoling; Le, Jonathan; Fuentes, Melisa A.; Jocoy, Shelby C.; Rossi, Antoni R.; Vu, Brian; Pham, Kim; Wang, Xiaoyang; Mali, Nanda Maya; Park, Jung Min; Choi, June Hyug; Lee, Hyunsu; Legrand, Julien M.D.; Kandyba, Eve; Kim, Jung Chul; Kim, Moonkyu; Foley, John; Yu, Zhengquan; Kobielak, Krzysztof; Andersen, Bogi; Khosrotehrani, Kiarash; Nie, Qing; Plikus, Maksim V.

In: eLife, Vol. 6, e22772, 11.07.2017.

Research output: Contribution to journalArticle

Wang, Q, Oh, JW, Lee, HL, Dhar, A, Peng, T, Ramos, R, Guerrero-Juarez, CF, Wang, X, Zhao, R, Cao, X, Le, J, Fuentes, MA, Jocoy, SC, Rossi, AR, Vu, B, Pham, K, Wang, X, Mali, NM, Park, JM, Choi, JH, Lee, H, Legrand, JMD, Kandyba, E, Kim, JC, Kim, M, Foley, J, Yu, Z, Kobielak, K, Andersen, B, Khosrotehrani, K, Nie, Q & Plikus, MV 2017, 'A multi-scale model for hair follicles reveals heterogeneous domains driving rapid spatiotemporal hair growth patterning', eLife, vol. 6, e22772. https://doi.org/10.7554/eLife.22772
Wang, Qixuan ; Oh, Ji Won ; Lee, Hye Lim ; Dhar, Anukriti ; Peng, Tao ; Ramos, Raul ; Guerrero-Juarez, Christian Fernando ; Wang, Xiaojie ; Zhao, Ran ; Cao, Xiaoling ; Le, Jonathan ; Fuentes, Melisa A. ; Jocoy, Shelby C. ; Rossi, Antoni R. ; Vu, Brian ; Pham, Kim ; Wang, Xiaoyang ; Mali, Nanda Maya ; Park, Jung Min ; Choi, June Hyug ; Lee, Hyunsu ; Legrand, Julien M.D. ; Kandyba, Eve ; Kim, Jung Chul ; Kim, Moonkyu ; Foley, John ; Yu, Zhengquan ; Kobielak, Krzysztof ; Andersen, Bogi ; Khosrotehrani, Kiarash ; Nie, Qing ; Plikus, Maksim V. / A multi-scale model for hair follicles reveals heterogeneous domains driving rapid spatiotemporal hair growth patterning. In: eLife. 2017 ; Vol. 6.
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abstract = "The control principles behind robust cyclic regeneration of hair follicles (HFs) remain unclear. Using multi-scale modeling, we show that coupling inhibitors and activators with physical growth of HFs is sufficient to drive periodicity and excitability of hair regeneration. Model simulations and experimental data reveal that mouse skin behaves as a heterogeneous regenerative field, composed of anatomical domains where HFs have distinct cycling dynamics. Interactions between fast-cycling chin and ventral HFs and slow-cycling dorsal HFs produce bilaterally symmetric patterns. Ear skin behaves as a hyper-refractory domain with HFs in extended rest phase. Such hyper-refractivity relates to high levels of BMP ligands and WNT antagonists, in part expressed by ear-specific cartilage and muscle. Hair growth stops at the boundaries with hyper-refractory ears and anatomically discontinuous eyelids, generating wave-breaking effects. We posit that similar mechanisms for coupled regeneration with dominant activator, hyper-refractory, and wave-breaker regions can operate in other actively renewing organs.",
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AU - Lee, Hye Lim

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AU - Peng, Tao

AU - Ramos, Raul

AU - Guerrero-Juarez, Christian Fernando

AU - Wang, Xiaojie

AU - Zhao, Ran

AU - Cao, Xiaoling

AU - Le, Jonathan

AU - Fuentes, Melisa A.

AU - Jocoy, Shelby C.

AU - Rossi, Antoni R.

AU - Vu, Brian

AU - Pham, Kim

AU - Wang, Xiaoyang

AU - Mali, Nanda Maya

AU - Park, Jung Min

AU - Choi, June Hyug

AU - Lee, Hyunsu

AU - Legrand, Julien M.D.

AU - Kandyba, Eve

AU - Kim, Jung Chul

AU - Kim, Moonkyu

AU - Foley, John

AU - Yu, Zhengquan

AU - Kobielak, Krzysztof

AU - Andersen, Bogi

AU - Khosrotehrani, Kiarash

AU - Nie, Qing

AU - Plikus, Maksim V.

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