Global Feather Orientations Changed by Electric Current

Overview

Journal iScience

Publisher Cell Press

Date 2021 Jun 28

PMID 34179734

Citations 3

Authors

Ting-Xin Jiang

Ang Li

Chih-Min Lin

Cathleen Chiu

Jung-Hwa Cho

Brian Reid

Min Zhao

Robert H Chow

Randall Bruce Widelitz

Cheng-Ming Chuong

Affiliations

Soon will be listed here.

Abstract

During chicken skin development, each feather bud exhibits its own polarity, but a population of buds organizes with a collective global orientation. We used embryonic dorsal skin, with buds aligned parallel to the rostral-caudal body axis, to explore whether exogenous electric fields affect feather polarity. Interestingly, brief exogenous current exposure prior to visible bud formation later altered bud orientations. Applying electric pulses perpendicular to the body rostral-caudal axis realigned bud growth in a collective swirl, resembling an electric field pointing toward the anode. Perturbed buds show normal molecular expression and morphogenesis except for their altered orientation. Epithelial-mesenchymal recombination demonstrates the effects of exogenous electric fields are mediated through the epithelium. Small-molecule channel inhibitor screens show Ca channels and PI3 Kinase are involved in controlling feather bud polarity. This work reveals the importance of bioelectricity in organ development and regeneration and provides an explant culture platform for experimentation.

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References

Chang H, Smallwood P, Williams J, Nathans J . The spatio-temporal domains of Frizzled6 action in planar polarity control of hair follicle orientation. Dev Biol. 2015; 409(1):181-193. PMC: 5125082. DOI: 10.1016/j.ydbio.2015.10.027. View

Ross C . The use of electric, magnetic, and electromagnetic field for directed cell migration and adhesion in regenerative medicine. Biotechnol Prog. 2016; 33(1):5-16. DOI: 10.1002/btpr.2371. View

Yin W, Kim H, Wang S, Gunawan F, Wang L, Kishimoto K . The potassium channel KCNJ13 is essential for smooth muscle cytoskeletal organization during mouse tracheal tubulogenesis. Nat Commun. 2018; 9(1):2815. PMC: 6052067. DOI: 10.1038/s41467-018-05043-5. View

Hanna H, Andre F, Mir L . Electrical control of calcium oscillations in mesenchymal stem cells using microsecond pulsed electric fields. Stem Cell Res Ther. 2017; 8(1):91. PMC: 5397732. DOI: 10.1186/s13287-017-0536-z. View

Chang H, Cahill H, Smallwood P, Wang Y, Nathans J . Identification of Astrotactin2 as a Genetic Modifier That Regulates the Global Orientation of Mammalian Hair Follicles. PLoS Genet. 2015; 11(9):e1005532. PMC: 4587951. DOI: 10.1371/journal.pgen.1005532. View

Jiang T, Chuong C . Mechanism of skin morphogenesis. I. Analyses with antibodies to adhesion molecules tenascin, N-CAM, and integrin. Dev Biol. 1992; 150(1):82-98. DOI: 10.1016/0012-1606(92)90009-6. View

Iwasa S, Popovic M, Morshead C . Skin-derived precursor cells undergo substrate-dependent galvanotaxis that can be modified by neighbouring cells. Stem Cell Res. 2018; 31:95-101. DOI: 10.1016/j.scr.2018.07.019. View

Devenport D, Fuchs E . Planar polarization in embryonic epidermis orchestrates global asymmetric morphogenesis of hair follicles. Nat Cell Biol. 2008; 10(11):1257-68. PMC: 2607065. DOI: 10.1038/ncb1784. View

Guo N, Hawkins C, Nathans J . Frizzled6 controls hair patterning in mice. Proc Natl Acad Sci U S A. 2004; 101(25):9277-81. PMC: 438967. DOI: 10.1073/pnas.0402802101. View

10.

Muncie J, Weaver V . The Physical and Biochemical Properties of the Extracellular Matrix Regulate Cell Fate. Curr Top Dev Biol. 2018; 130:1-37. PMC: 6586474. DOI: 10.1016/bs.ctdb.2018.02.002. View

11.

Cho B, Song S, Axelrod J . Prickle isoforms determine handedness of helical morphogenesis. Elife. 2020; 9. PMC: 7004564. DOI: 10.7554/eLife.51456. View

12.

Hammerick K, Longaker M, Prinz F . In vitro effects of direct current electric fields on adipose-derived stromal cells. Biochem Biophys Res Commun. 2010; 397(1):12-7. PMC: 5718355. DOI: 10.1016/j.bbrc.2010.05.003. View

13.

Silver B, Wolf A, Lee J, Pang M, Nelson C . Epithelial tissue geometry directs emergence of bioelectric field and pattern of proliferation. Mol Biol Cell. 2020; 31(16):1691-1702. PMC: 7521849. DOI: 10.1091/mbc.E19-12-0719. View

14.

Hinkle L, McCaig C, Robinson K . The direction of growth of differentiating neurones and myoblasts from frog embryos in an applied electric field. J Physiol. 1981; 314:121-35. PMC: 1249421. DOI: 10.1113/jphysiol.1981.sp013695. View

15.

Zajdel T, Shim G, Wang L, Rossello-Martinez A, Cohen D . SCHEEPDOG: Programming Electric Cues to Dynamically Herd Large-Scale Cell Migration. Cell Syst. 2020; 10(6):506-514.e3. PMC: 7779114. DOI: 10.1016/j.cels.2020.05.009. View

16.

Wang Y, Badea T, Nathans J . Order from disorder: Self-organization in mammalian hair patterning. Proc Natl Acad Sci U S A. 2006; 103(52):19800-5. PMC: 1750877. DOI: 10.1073/pnas.0609712104. View

17.

Hotary K, Robinson K . Endogenous electrical currents and the resultant voltage gradients in the chick embryo. Dev Biol. 1990; 140(1):149-60. DOI: 10.1016/0012-1606(90)90062-n. View

18.

Jenny A . Planar cell polarity signaling in the Drosophila eye. Curr Top Dev Biol. 2010; 93:189-227. PMC: 5310647. DOI: 10.1016/B978-0-12-385044-7.00007-2. View

19.

Yue Z, Jiang T, Widelitz R, Chuong C . Wnt3a gradient converts radial to bilateral feather symmetry via topological arrangement of epithelia. Proc Natl Acad Sci U S A. 2006; 103(4):951-5. PMC: 1347975. DOI: 10.1073/pnas.0506894103. View

20.

Hamburger V, HAMILTON H . A series of normal stages in the development of the chick embryo. J Morphol. 2014; 88(1):49-92. View