|
|
|
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
Development, Vol 122, Issue 4 1207-1214, Copyright © 1996 by Company of Biologists
JOURNAL ARTICLES |
H Yoshida, T Kunisada, M Kusakabe, S Nishikawa and SI Nishikawa
Department of Molecular Genetics, Faculty of Medicine, Kyoto University, Japan.
The injection of an antagonistic anti-murine c-kit monoclonal antibody ACK2 during mouse embryonic development produced three distinctive pigmentation patterns on the coat of the offspring. Pattern 1 consisted of pigmentation in craniofacial and caudal regions and was induced by an ACK2 injection between 9.5 and 11.5 days post coitum (dpc). In pattern 2, the entire coat was unpigmented and was induced by the injection at around 13.0 dpc. Pattern 3 consisted of pigmented patches spreading ventrolaterally from the dorsoanterior trunk regions towards the anterior and posterior directions and it was induced by ACK2 administered at 14.5-15.0 dpc. We investigated the embryological basis of these nonuniform pigmentation patterns to elucidate the process of melanoblast differentiation between lineage commitment and colonization into developing hair follicles. The results showed the following. (1) Melanocyte differentiation at the embryonic stage from 10.5 to 12.5 dpc progresses in a spatially nonuniform fashion, being faster in the craniofacial and caudal regions than in the trunk; pattern 1 reflects this. (2) Melanoblasts are activated to proliferate synchronously upon entering into the epidermis; pattern 2 correlates with this process. (3) c-kit functions as a survival signal for proliferating melanoblasts in the epidermis. (4) The melanoblasts that enter developing hair follicles can survive without a c-kit signal; pattern 3 essentially represents the hair follicles colonized by these cells. Analysis of the melanoblast distribution of ls/ls embryos that bear a loss-of-function mutation in the endothelin 3 gene suggested that endothelin 3 is required for early melanoblast differentiation before entering into the epidermis, whereas proliferation in the epidermis takes place without this molecule. Based on these data, we propose 4 distinct steps of embryonic melanocyte differentiation: (1) migration in the dermis, which requires both c-kit and endothelin 3; (2) a state before epidermal entry that is resistant to anti-c-kit mAb; (3) cell proliferation after entering the epidermal layer, which requires c-kit and endothelin receptor B but not endothelin 3 and (4) integration into developing hair follicles, which renders melanoblasts resistant to anti-c-kit mAb. Thus, melanoblast differentiation proceeds by alternately repeating c-kit -dependent and c-kit-independent stages and c-kit functions as a survival factor for the proliferating melanoblasts.
This article has been cited by other articles:
|
|
 |
|
  T. Inoue-Narita, K. Hamada, T. Sasaki, S. Hatakeyama, S. Fujita, K. Kawahara, M. Sasaki, H. Kishimoto, S. Eguchi, I. Kojima, et al. Pten Deficiency in Melanocytes Results in Resistance to Hair Graying and Susceptibility to Carcinogen-Induced Melanomagenesis Cancer Res., July 15, 2008; 68(14): 5760 - 5768. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. Sato-Jin, E. K. Nishimura, E. Akasaka, W. Huber, H. Nakano, A. Miller, J. Du, M. Wu, K. Hanada, D. Sawamura, et al. Epistatic connections between microphthalmia-associated transcription factor and endothelin signaling in Waardenburg syndrome and other pigmentary disorders FASEB J, April 1, 2008; 22(4): 1155 - 1168. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Y. Shimomura, M. Wajid, L. Shapiro, and A. M. Christiano P-cadherin is a p63 target gene with a crucial role in the developing human limb bud and hair follicle Development, February 15, 2008; 135(4): 743 - 753. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. G. Mills, R. J. Nuckels, and D. M. Parichy Deconstructing evolution of adult phenotypes: genetic analyses of kit reveal homology and evolutionary novelty during adult pigment pattern development of Danio fishes Development, March 15, 2007; 134(6): 1081 - 1090. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Routhouska, A. C. Gilliam, and P. Mirmirani Hair Depigmentation During Chemotherapy With a Class III/V Receptor Tyrosine Kinase Inhibitor. Arch Dermatol, November 1, 2006; 142(11): 1477 - 1479. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Moriyama, M. Osawa, S.-S. Mak, T. Ohtsuka, N. Yamamoto, H. Han, V. Delmas, R. Kageyama, F. Beermann, L. Larue, et al. Notch signaling via Hes1 transcription factor maintains survival of melanoblasts and melanocyte stem cells J. Cell Biol., May 8, 2006; 173(3): 333 - 339. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. Tachibana, N. Jones, D. J. Dumont, M. C. Puri, and A. Bernstein Selective Role of a Distinct Tyrosine Residue on Tie2 in Heart Development and Early Hematopoiesis Mol. Cell. Biol., June 1, 2005; 25(11): 4693 - 4702. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Yamazaki, E. Sakata, T. Yamane, A. Yanagisawa, K. Abe, K.-I. Yamamura, S.-I. Hayashi, and T. Kunisada Presence and distribution of neural crest-derived cells in the murine developing thymus and their potential for differentiation Int. Immunol., May 1, 2005; 17(5): 549 - 558. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. M. Wilson, K. L. Richards, M. L. Ford-Perriss, J.-J. Panthier, and M. Murphy Neural crest cell lineage segregation in the mouse neural tube Development, December 15, 2004; 131(24): 6153 - 6162. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Slominski, D. J. Tobin, S. Shibahara, and J. Wortsman Melanin Pigmentation in Mammalian Skin and Its Hormonal Regulation Physiol Rev, October 1, 2004; 84(4): 1155 - 1228. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 N. Planque, G. Raposo, L. Leconte, O. Anezo, P. Martin, and S. Saule Microphthalmia Transcription Factor Induces Both Retinal Pigmented Epithelium and Neural Crest Melanocytes from Neuroretina Cells J. Biol. Chem., October 1, 2004; 279(40): 41911 - 41917. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. G. Moss, G. C. Toner, J. M. Cherrington, D. B. Mendel, and A. D. Laird Hair Depigmentation Is a Biological Readout for Pharmacological Inhibition of KIT in Mice and Humans J. Pharmacol. Exp. Ther., November 1, 2003; 307(2): 476 - 480. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. R. Fitch, K. A. McGowan, C. D. van Raamsdonk, H. Fuchs, D. Lee, A. Puech, Y. Herault, D. W. Threadgill, M. H. de Angelis, and G. S. Barsh Genetics of dark skin in mice Genes & Dev., January 15, 2003; 17(2): 214 - 228. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Naito, H. Yoshida, E. Nishioka, M. Satoh, S. Azuma, T. Yamamoto, S.-i. Nishikawa, and J.-i. Inoue TRAF6-deficient mice display hypohidrotic ectodermal dysplasia PNAS, June 25, 2002; 99(13): 8766 - 8771. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E. M. J. Peters, D. J. Tobin, N. Botchkareva, M. Maurer, and R. Paus Migration of Melanoblasts into the Developing Murine Hair Follicle Is Accompanied by Transient c-Kit Expression J. Histochem. Cytochem., June 1, 2002; 50(6): 751 - 766. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Hashi, H. Yoshida, K. Honda, S. Fraser, H. Kubo, M. Awane, A. Takabayashi, H. Nakano, Y. Yamaoka, and S.-I. Nishikawa Compartmentalization of Peyer's Patch Anlagen Before Lymphocyte Entry J. Immunol., March 15, 2001; 166(6): 3702 - 3709. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. V. BOTCHKAREVA, M. KHLGATIAN, B. J. LONGLEY, V. A. BOTCHKAREV, and B. A. GILCHREST SCF/c-kit signaling is required for cyclic regeneration of the hair pigmentation unit FASEB J, March 1, 2001; 15(3): 645 - 658. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Kubo, T. Fujiwara, L. Jussila, H. Hashi, M. Ogawa, K. Shimizu, M. Awane, Y. Sakai, A. Takabayashi, K. Alitalo, et al. Involvement of vascular endothelial growth factor receptor-3 in maintenance of integrity of endothelial cell lining during tumor angiogenesis Blood, July 15, 2000; 96(2): 546 - 553. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L Hou, J. Panthier, and H Arnheiter Signaling and transcriptional regulation in the neural crest-derived melanocyte lineage: interactions between KIT and MITF Development, January 12, 2000; 127(24): 5379 - 5389. [Abstract] [PDF]
|
|
|
|
|
|
H. Yoshida, K. Honda, R. Shinkura, S. Adachi, S. Nishikawa, K. Maki, K. Ikuta, and S.-I. Nishikawa IL-7 receptor {alpha}+ CD3– cells in the embryonic intestine induces the organizing center of Peyer's patches Int. Immunol., May 1, 1999; 11(5): 643 - 655. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Parichy, J. Rawls, S. Pratt, T. Whitfield, and S. Johnson Zebrafish sparse corresponds to an orthologue of c-kit and is required for the morphogenesis of a subpopulation of melanocytes, but is not essential for hematopoiesis or primordial germ cell development Development, January 8, 1999; 126(15): 3425 - 3436. [Abstract] [PDF]
|
|
|
|
|
|
Y Saga, S Miyagawa-Tomita, A Takagi, S Kitajima, J. Miyazaki, and T Inoue MesP1 is expressed in the heart precursor cells and required for the formation of a single heart tube Development, January 8, 1999; 126(15): 3437 - 3447. [Abstract] [PDF]
|
|
|
|
 |
|
 T. Kunisada, S.-Z. Lu, H. Yoshida, S. Nishikawa, S.-i. Nishikawa, M. Mizoguchi, S.-i. Hayashi, L. Tyrrell, D. A. Williams, X. Wang, et al. Murine Cutaneous Mastocytosis and Epidermal Melanocytosis Induced by Keratinocyte Expression of Transgenic Stem Cell Factor J. Exp. Med., May 18, 1998; 187(10): 1565 - 1573. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T Kunisada, H Yoshida, H Yamazaki, A Miyamoto, H Hemmi, E Nishimura, L. Shultz, S Nishikawa, and S Hayashi Transgene expression of steel factor in the basal layer of epidermis promotes survival, proliferation, differentiation and migration of melanocyte precursors Development, January 8, 1998; 125(15): 2915 - 2923. [Abstract] [PDF]
|
|
|
|
 |
|
 H. Hibino, Y. Horio, A. Inanobe, K. Doi, M. Ito, M. Yamada, T. Gotow, Y. Uchiyama, M. Kawamura, T. Kubo, et al. An ATP-Dependent Inwardly Rectifying Potassium Channel, KAB-2 (Kir4.1), in Cochlear Stria Vascularis of Inner Ear: Its Specific Subcellular Localization and Correlation with the Formation of Endocochlear Potential J. Neurosci., June 15, 1997; 17(12): 4711 - 4721. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K Opdecamp, A Nakayama, M. Nguyen, C. Hodgkinson, W. Pavan, and H Arnheiter Melanocyte development in vivo and in neural crest cell cultures: crucial dependence on the Mitf basic-helix-loop-helix-zipper transcription factor Development, January 6, 1997; 124(12): 2377 - 2386. [Abstract] [PDF]
|
|
|
|
|
|
M Kluppel, D. Nagle, M Bucan, and A Bernstein Long-range genomic rearrangements upstream of Kit dysregulate the developmental pattern of Kit expression in W57 and Wbanded mice and interfere with distinct steps in melanocyte development Development, January 1, 1997; 124(1): 65 - 77. [Abstract] [PDF]
|
|
|
|
|
|
K Reid, A. Turnley, G. Maxwell, Y Kurihara, H Kurihara, P. Bartlett, and M Murphy Multiple roles for endothelin in melanocyte development: regulation of progenitor number and stimulation of differentiation Development, January 12, 1996; 122(12): 3911 - 3919. [Abstract] [PDF]
|
|
