Abstract
Melanin-bearing pigment cells in birds and mammals, much as those in other vertebrates, have at least two developmental origins: the neural crest, giving rise to melanocytes of the integument (skin and its appendages) and of inner organs, and the optic neuroepithelium, giving rise to the retinal pigment epithelium and part of the iris. Both types of cells are derived from precursors that are guided towards their differentiation by complex signaling pathways and transcription factors, some common to both cell types and some unique. Numerous studies show that neural crest-derived melanocytes arise from precursors that emanate from the dorsal neural tube and migrate on a dorso-lateral pathway underneath the surface ectoderm. Others arise from poorly defined precursors that migrate on a ventro-medial pathway and also give rise to Schwann cells. Nevertheless, melanocyte precursors retain developmental plasticity for considerable time, potentially being capable of correcting developmental imbalances in an embryo’s distinct cell populations. Some derivatives even exhibit stem cell features during adulthood, capable of replenishing melanocytes during hair and feather cycles. In fact, the study of the development of melanin-bearing pigment cells provides for fascinating insights into how specific cell types arise and maintain themselves or become abnormal or are lost in pathogenic processes.
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References
Adameyko I, Lallemend F, Aquino JB, Pereira JA, Topilko P, Muller T, Fritz N, Beljajeva A, Mochii M, Liste I et al (2009) Schwann cell precursors from nerve innervation are a cellular origin of melanocytes in skin. Cell 139:366–379
Ambati J, Fowler BJ (2012) Mechanisms of age-related macular degeneration. Neuron 75:26–39
Arnheiter H (1998) Evolutionary biology. Eyes viewed from the skin. Nature 391:632–633
Baggiolini A, Varum S, Mateos JM, Bettosini D, John N, Bonalli M, Ziegler U, Dimou L, Clevers H, Furrer R et al (2015) Premigratory and migratory neural crest cells are multipotent in vivo. Cell Stem Cell 16:314–322
Bharti K, Nguyen MT, Skuntz S, Bertuzzi S, Arnheiter H (2006) The other pigment cell: specification and development of the pigmented epithelium of the vertebrate eye. Pigment Cell Res 19:380–394
Bharti K, Liu W, Csermely T, Bertuzzi S, Arnheiter H (2008) Alternative promoter use in eye development: the complex role and regulation of the transcription factor MITF. Development 135:1169–1178
Bharti K, Gasper M, Ou J, Brucato M, Clore-Gronenborn K, Pickel J, Arnheiter H (2012) A regulatory loop involving PAX6, MITF, and WNT signaling controls retinal pigment epithelium development. PLoS Genet 8:e1002757
Botchkareva NV, Khlgatian M, Longley BJ, Botchkarev VA, Gilchrest BA (2001) SCF/c-kit signaling is required for cyclic regeneration of the hair pigmentation unit. FASEB J 15:645–658
Chen CF, Foley J, Tang PC, Li A, Jiang TX, Wu P, Widelitz RB, Chuong CM (2015) Development, regeneration, and evolution of feathers. Annu Rev Anim Biosci 3:169–195
Chow RL, Altmann CR, Lang RA, Hemmati-Brivanlou A (1999) Pax6 induces ectopic eyes in a vertebrate. Development 126:4213–4222
Dupin E, Le Douarin NM (2014) The neural crest, a multifaceted structure of the vertebrates. Birth Defects Res C Embryo Today 102:187–209
Dupin E, Glavieux C, Vaigot P, Le Douarin NM (2000) Endothelin 3 induces the reversion of melanocytes to glia through a neural crest-derived glial-melanocytic progenitor. Proc Natl Acad Sci U S A 97:7882–7887
Dupin E, Real C, Glavieux-Pardanaud C, Vaigot P, Le Douarin NM (2003) Reversal of developmental restrictions in neural crest lineages: transition from Schwann cells to glial-melanocytic precursors in vitro. Proc Natl Acad Sci U S A 100:5229–5233
Dupin E, Calloni GW, Coelho-Aguiar JM, Le Douarin NM (2018) The issue of the multipotency of the neural crest cells. Dev Biol 444(Suppl 1):S47–S59
Flesher JL, Paterson-Coleman EK, Vasudeva P, Ruiz-Vega R, Marshall M, Pearlman E, Macgregor GR, Neumann J, Ganesan AK (2020) Delineating the role of MITF isoforms in pigmentation and tissue homeostasis. Pigment Cell Melanoma Res 33:279–292
Furlan A, Adameyko I (2018) Schwann cell precursor: a neural crest cell in disguise? Dev Biol 444(Suppl 1):S25–S35
Gacem N, Kavo A, Zerad L, Richard L, Mathis S, Kapur RP, Parisot M, Amiel J, Dufour S, De La Grange P et al (2020) ADAR1 mediated regulation of neural crest derived melanocytes and Schwann cell development. Nat Commun 11:198
Gallagher SJ, Rambow F, Kumasaka M, Champeval D, Bellacosa A, Delmas V, Larue L (2013) Beta-catenin inhibits melanocyte migration but induces melanoma metastasis. Oncogene 32:2230–2238
George A, Zand DJ, Hufnagel RB, Sharma R, Sergeev YV, Legare JM, Rice GM, Scott Schwoerer JA, Rius M, Tetri L et al (2016) Biallelic Mutations in MITF Cause Coloboma, Osteopetrosis, Microphthalmia, Macrocephaly, Albinism, and Deafness. Am J Hum Genet 99:1388–1394
Goding CR, Arnheiter H (2019) MITF-the first 25 years. Genes Dev. https://doi.org/10.1101/gad.324657.119
Halder G, Callaerts P, Gehring WJ (1995) Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 267:1788–1792
Hari L, Miescher I, Shakhova O, Suter U, Chin L, Taketo M, Richardson WD, Kessaris N, Sommer L (2012) Temporal control of neural crest lineage generation by Wnt/beta-catenin signaling. Development 139:2107–2117
Hou L, Panthier JJ, Arnheiter H (2000) Signaling and transcriptional regulation in the neural crest-derived melanocyte lineage: interactions between KIT and MITF. Development 127:5379–5389
Hou L, Pavan WJ, Shin MK, Arnheiter H (2004) Cell-autonomous and cell non-autonomous signaling through endothelin receptor B during melanocyte development. Development 131:3239–3247
Huszar D, Sharpe A, Hashmi S, Bouchard B, Houghton A, Jaenisch R (1991) Generation of pigmented stripes in albino mice by retroviral marking of neural crest melanoblasts. Development 113:653–660
Inaba M, Jiang TX, Liang YC, Tsai S, Lai YC, Widelitz RB, Chuong CM (2019) Instructive role of melanocytes during pigment pattern formation of the avian skin. Proc Natl Acad Sci U S A 116:6884–6890
Jaegle M, Ghazvini M, Mandemakers W, Piirsoo M, Driegen S, Levavasseur F, Raghoenath S, Grosveld F, Meijer D (2003) The POU proteins Brn-2 and Oct-6 share important functions in Schwann cell development. Genes Dev 17:1380–1391
Joshi SS, Tandukar B, Pan L, Huang JM, Livak F, Smith BJ, Hodges T, Mahurkar AA, Hornyak TJ (2019) CD34 defines melanocyte stem cell subpopulations with distinct regenerative properties. PLoS Genet 15:e1008034
Kinsler VA, Larue L (2018) The patterns of birthmarks suggest a novel population of melanocyte precursors arising around the time of gastrulation. Pigment Cell Melanoma Res 31:95–109
Kissel H, Timokhina I, Hardy MP, Rothschild G, Tajima Y, Soares V, Angeles M, Whitlow SR, Manova K, Besmer P (2000) Point mutation in kit receptor tyrosine kinase reveals essential roles for kit signaling in spermatogenesis and oogenesis without affecting other kit responses. EMBO J 19:1312–1326
Kokkinaki M, Abu-Asab M, Gunawardena N, Ahern G, Javidnia M, Young J, Golestaneh N (2013) Klotho regulates retinal pigment epithelial functions and protects against oxidative stress. J Neurosci 33:16346–16359
Krispin S, Nitzan E, Kassem Y, Kalcheim C (2010) Evidence for a dynamic spatiotemporal fate map and early fate restrictions of premigratory avian neural crest. Development 137:585–595
Kumar D, Nitzan E, Kalcheim C (2019) YAP promotes neural crest emigration through interactions with BMP and Wnt activities. Cell Commun Signal 17:69
Le Douarin NM (1974) Cell recognition based on natural morphological nuclear markers. Med Biol 52:281–319
Le Douarin NM, Kalcheim C (1999) The neural crest. Cambridge, Cambridge University Press
Letelier J, Bovolenta P, Martinez-Morales JR (2017) The pigmented epithelium, a bright partner against photoreceptor degeneration. J Neurogenet 31:203–215
Li H, Fan L, Zhu S, Shin MK, Lu F, Qu J, Hou L (2017) Epilation induces hair and skin pigmentation through an EDN3/EDNRB-dependent regenerative response of melanocyte stem cells. Sci Rep 7:7272
Lin SJ, Foley J, Jiang TX, Yeh CY, Wu P, Foley A, Yen CM, Huang YC, Cheng HC, Chen CF et al (2013) Topology of feather melanocyte progenitor niche allows complex pigment patterns to emerge. Science 340:1442–1445
Liu Y, Ye F, Li Q, Tamiya S, Darling DS, Kaplan HJ, Dean DC (2009) Zeb1 represses Mitf and regulates pigment synthesis, cell proliferation, and epithelial morphology. Invest Ophthalmol Vis Sci 50:5080–5088
Lu Z, Xie Y, Huang H, Jiang K, Zhou B, Wang F, Chen T (2020) Hair follicle stem cells regulate retinoid metabolism to maintain the self-renewal niche for melanocyte stem cells. eLife 9:e52712
Ma X, Li H, Chen Y, Yang J, Chen H, Arnheiter H, Hou L (2019) The transcription factor MITF in RPE function and dysfunction. Prog Retin Eye Res 73:100766
Mintz B (1967) Gene control of mammalian pigmentary differentiation. I. Clonal origin of melanocytes. Proc Natl Acad Sci U S A 58:344–351
Moriyama M, Osawa M, Mak SS, Ohtsuka T, Yamamoto N, Han H, Delmas V, Kageyama R, Beermann F, Larue L et al (2006) Notch signaling via Hes1 transcription factor maintains survival of melanoblasts and melanocyte stem cells. J Cell Biol 173:333–339
Ngeow KC, Friedrichsen HJ, Li L, Zeng Z, Andrews S, Volpon L, Brunsdon H, Berridge G, Picaud S, Fischer R et al (2018) BRAF/MAPK and GSK3 signaling converges to control MITF nuclear export. Proc Natl Acad Sci U S A 115:E8668–E8677
Nguyen M, Arnheiter H (2000) Signaling and transcriptional regulation in early mammalian eye development: a link between FGF and MITF. Development 127:3581–3591
Nieto MA (2002) The snail superfamily of zinc-finger transcription factors. Nat Rev Mol Cell Biol 3:155–166
Nishimura EK (2011) Melanocyte stem cells: a melanocyte reservoir in hair follicles for hair and skin pigmentation. Pigment Cell Melanoma Res 24:401–410
Nishimura EK, Jordan SA, Oshima H, Yoshida H, Osawa M, Moriyama M, Jackson IJ, Barrandon Y, Miyachi Y, Nishikawa S (2002) Dominant role of the niche in melanocyte stem-cell fate determination. Nature 416:854–860
Nitzan E, Krispin S, Pfaltzgraff ER, Klar A, Labosky PA, Kalcheim C (2013a) A dynamic code of dorsal neural tube genes regulates the segregation between neurogenic and melanogenic neural crest cells. Development 140:2269–2279
Nitzan E, Pfaltzgraff ER, Labosky PA, Kalcheim C (2013b) Neural crest and Schwann cell progenitor-derived melanocytes are two spatially segregated populations similarly regulated by Foxd3. Proc Natl Acad Sci U S A 110:12709–12714
Opdecamp K, Nakayama A, Nguyen MT, Hodgkinson CA, Pavan WJ, Arnheiter H (1997) Melanocyte development in vivo and in neural crest cell cultures: crucial dependence on the Mitf basic-helix-loop-helix-zipper transcription factor. Development 124:2377–2386
Opdecamp K, Kos L, Arnheiter H, Pavan WJ (1998) Endothelin signalling in the development of neural crest-derived melanocytes. Biochem Cell Biol 76:1093–1099
Parfejevs V, Debbache J, Shakhova O, Schaefer SM, Glausch M, Wegner M, Suter U, Riekstina U, Werner S, Sommer L (2018) Injury-activated glial cells promote wound healing of the adult skin in mice. Nat Commun 9:236
Phelep A, Laouari D, Bharti K, Burtin M, Tammaccaro S, Garbay S, Nguyen C, Vasseur F, Blanc T, Berissi S et al (2017) MITF - A controls branching morphogenesis and nephron endowment. PLoS Genet 13:e1007093
Pla P, Monsoro-Burq AH (2018) The neural border: Induction, specification and maturation of the territory that generates neural crest cells. Dev Biol 444(Suppl 1):S36–S46
Rabbani P, Takeo M, Chou W, Myung P, Bosenberg M, Chin L, Taketo MM, Ito M (2011) Coordinated activation of Wnt in epithelial and melanocyte stem cells initiates pigmented hair regeneration. Cell 145:941–955
Raviv S, Bharti K, Rencus-Lazar S, Cohen-Tayar Y, Schyr R, Evantal N, Meshorer E, Zilberberg A, Idelson M, Reubinoff B et al (2014) PAX6 regulates melanogenesis in the retinal pigmented epithelium through feed-forward regulatory interactions with MITF. PLoS Genet 10:e1004360
Strauss O (2005) The retinal pigment epithelium in visual function. Physiol Rev 85:845–881
Tassabehji M, Newton VE, Read AP (1994) Waardenburg syndrome type 2 caused by mutations in the human microphthalmia (MITF) gene. Nat Genet 8:251–255
Vandamme N, Berx G (2019) From neural crest cells to melanocytes: cellular plasticity during development and beyond. Cell Mol Life Sci 76:1919–1934
Vandewalle C, Van Roy F, Berx G (2009) The role of the ZEB family of transcription factors in development and disease. Cell Mol Life Sci 66:773–787
Weston JA (1991) Sequential segregation and fate of developmentally restricted intermediate cell populations in the neural crest lineage. Curr Top Dev Biol 25:133–153
Wilkie AL, Jordan SA, Jackson IJ (2002) Neural crest progenitors of the melanocyte lineage: coat colour patterns revisited. Development 129:3349–3357
Yun S, Saijoh Y, Hirokawa KE, Kopinke D, Murtaugh LC, Monuki ES, Levine EM (2009) Lhx2 links the intrinsic and extrinsic factors that control optic cup formation. Development 136:3895–3906
Zhang B, Ma S, Rachmin I, He M, Baral P, Choi S, Goncalves WA, Shwartz Y, Fast EM, Su Y et al (2020) Hyperactivation of sympathetic nerves drives depletion of melanocyte stem cells. Nature 577:676–681
Zhou L, Yang K, Carpenter A, Lang RA, Andl T, Zhang Y (2016) CD133-positive dermal papilla-derived Wnt ligands regulate postnatal hair growth. Biochem J 473:3291–3305
Acknowledgments
We thank Drs. Ling Hou, Lionel Larue, and Lukas Sommer for critical suggestions and review of the manuscript. The authors’ own work discussed in this paper was supported in part by NINDS, National Institutes of Health, United States, and the Kanton of Zürich, Switzerland.
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Arnheiter, H., Debbache, J. (2021). Development of Melanin-Bearing Pigment Cells in Birds and Mammals. In: Hashimoto, H., Goda, M., Futahashi, R., Kelsh, R., Akiyama, T. (eds) Pigments, Pigment Cells and Pigment Patterns. Springer, Singapore. https://doi.org/10.1007/978-981-16-1490-3_6
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