A Requirement for Kit in Embryonic Zebrafish Melanocyte Differentiation is Revealed by Melanoblast Delay

Overview

Journal Dev Genes Evol

Specialty Biology

Date 2004 Aug 10

PMID 15300437

Citations 18

Authors

Eve M Mellgren

Stephen L Johnson

Affiliations

Soon will be listed here.

Abstract

Exploring differences in gene requirements between species can allow us to delineate basic developmental mechanisms, provide insight into patterns of evolution, and explain heterochronic differences in developmental processes. One example of differences in gene requirements between zebrafish and mammals is the requirement of the kit receptor tyrosine kinase in melanocyte development. kit is required for migration, survival and differentiation of all neural crest-derived melanocytes in mammals. In contrast, zebrafish kit is not required for differentiation of embryonic melanocytes during normal development. When melanoblast development in zebrafish embryos is delayed by injecting morpholinos targeted to the mitfa gene, we show that these delayed melanoblasts fail to differentiate in kit mutants. Thus, we show that there is a kit requirement for melanocyte differentiation in zebrafish when melanoblast development is delayed. Furthermore, we show that kit is not involved in maintaining melanocyte precursors through the developmental delay, but instead is required for differentiation of melanocytes after the block on their development is removed. Finally, we suggest there is a heterochronic shift in the onset of melanocyte differentiation between fish and mouse, and developmental delay of melanoblast development in zebrafish removes this heterochronic difference.

Citing Articles

Degradation of endogenous proteins and generation of a null-like phenotype in zebrafish using Trim-Away technology.

Chen X, Liu M, Lou H, Lu Y, Zhou M, Ou R Genome Biol. 2019; 20(1):19.

PMID: 30674345 PMC: 6343325. DOI: 10.1186/s13059-019-1624-4.

Transcriptomics reveals the molecular processes of light-induced rapid darkening of the non-obligate cave dweller Oreolalax rhodostigmatus (Megophryidae, Anura) and their genetic basis of pigmentation strategy.

Zhu W, Liu L, Wang X, Gao X, Jiang J, Wang B BMC Genomics. 2018; 19(1):422.

PMID: 29855256 PMC: 5984452. DOI: 10.1186/s12864-018-4790-y.

Distant Insulin Signaling Regulates Vertebrate Pigmentation through the Sheddase Bace2.

Zhang Y, Zimmer M, Guardia T, Callahan S, Mondal C, Di Martino J Dev Cell. 2018; 45(5):580-594.e7.

PMID: 29804876 PMC: 5991976. DOI: 10.1016/j.devcel.2018.04.025.

Mapping of Variable DNA Methylation Across Multiple Cell Types Defines a Dynamic Regulatory Landscape of the Human Genome.

Gu J, Stevens M, Xing X, Li D, Zhang B, Payton J G3 (Bethesda). 2016; 6(4):973-86.

PMID: 26888867 PMC: 4825665. DOI: 10.1534/g3.115.025437.

Origins of adult pigmentation: diversity in pigment stem cell lineages and implications for pattern evolution.

Parichy D, Spiewak J Pigment Cell Melanoma Res. 2014; 28(1):31-50.

PMID: 25421288 PMC: 4276524. DOI: 10.1111/pcmr.12332.

References

Nakayama A, Nguyen M, Chen C, Opdecamp K, Hodgkinson C, Arnheiter H . Mutations in microphthalmia, the mouse homolog of the human deafness gene MITF, affect neuroepithelial and neural crest-derived melanocytes differently. Mech Dev. 1998; 70(1-2):155-66. DOI: 10.1016/s0925-4773(97)00188-3. View

Rawls J, Mellgren E, Johnson S . How the zebrafish gets its stripes. Dev Biol. 2002; 240(2):301-14. DOI: 10.1006/dbio.2001.0418. View

Quigley I, Parichy D . Pigment pattern formation in zebrafish: a model for developmental genetics and the evolution of form. Microsc Res Tech. 2002; 58(6):442-55. DOI: 10.1002/jemt.10162. View

Hodgkinson C, Moore K, Nakayama A, Steingrimsson E, Copeland N, Jenkins N . Mutations at the mouse microphthalmia locus are associated with defects in a gene encoding a novel basic-helix-loop-helix-zipper protein. Cell. 1993; 74(2):395-404. DOI: 10.1016/0092-8674(93)90429-t. View

Hughes M, Lingrel J, Krakowsky J, Anderson K . A helix-loop-helix transcription factor-like gene is located at the mi locus. J Biol Chem. 1993; 268(28):20687-90. View

Steel K, Davidson D, JACKSON I . TRP-2/DT, a new early melanoblast marker, shows that steel growth factor (c-kit ligand) is a survival factor. Development. 1992; 115(4):1111-9. DOI: 10.1242/dev.115.4.1111. View

Johnson S, Africa D, Walker C, Weston J . Genetic control of adult pigment stripe development in zebrafish. Dev Biol. 1995; 167(1):27-33. DOI: 10.1006/dbio.1995.1004. View

Kimmel C, Ballard W, Kimmel S, Ullmann B, Schilling T . Stages of embryonic development of the zebrafish. Dev Dyn. 1995; 203(3):253-310. DOI: 10.1002/aja.1002030302. View

Takahashi Y . Steel factor and c-kit receptor: from mutants to a growth factor system. Bioessays. 1993; 15(2):77-83. DOI: 10.1002/bies.950150202. View

10.

Hou L, Panthier J, Arnheiter H . Signaling and transcriptional regulation in the neural crest-derived melanocyte lineage: interactions between KIT and MITF. Development. 2000; 127(24):5379-89. DOI: 10.1242/dev.127.24.5379. View

11.

Wehrle-Haller B, Weston J . Soluble and cell-bound forms of steel factor activity play distinct roles in melanocyte precursor dispersal and survival on the lateral neural crest migration pathway. Development. 1995; 121(3):731-42. DOI: 10.1242/dev.121.3.731. View

12.

CAMP E, Lardelli M . Tyrosinase gene expression in zebrafish embryos. Dev Genes Evol. 2001; 211(3):150-3. DOI: 10.1007/s004270000125. View

13.

Jowett T, Yan Y . Double fluorescent in situ hybridization to zebrafish embryos. Trends Genet. 1996; 12(10):387-9. DOI: 10.1016/s0168-9525(96)90091-8. View

14.

Opdecamp K, Nakayama A, Nguyen M, Hodgkinson C, Pavan W, Arnheiter H . Melanocyte development in vivo and in neural crest cell cultures: crucial dependence on the Mitf basic-helix-loop-helix-zipper transcription factor. Development. 1997; 124(12):2377-86. DOI: 10.1242/dev.124.12.2377. View

15.

Kelsh R, Schmid B, Eisen J . Genetic analysis of melanophore development in zebrafish embryos. Dev Biol. 2000; 225(2):277-93. DOI: 10.1006/dbio.2000.9840. View

16.

Postlethwait J, Yan Y, Gates M, Horne S, Amores A, Brownlie A . Vertebrate genome evolution and the zebrafish gene map. Nat Genet. 1998; 18(4):345-9. DOI: 10.1038/ng0498-345. View

17.

Parichy D, Rawls J, Pratt S, Whitfield T, Johnson S . 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. 1999; 126(15):3425-36. DOI: 10.1242/dev.126.15.3425. View

18.

Cable J, JACKSON I, Steel K . Mutations at the W locus affect survival of neural crest-derived melanocytes in the mouse. Mech Dev. 1995; 50(2-3):139-50. DOI: 10.1016/0925-4773(94)00331-g. View

19.

Lister J, Close J, Raible D . Duplicate mitf genes in zebrafish: complementary expression and conservation of melanogenic potential. Dev Biol. 2001; 237(2):333-44. DOI: 10.1006/dbio.2001.0379. View

20.

Rawls J, Johnson S . Requirements for the kit receptor tyrosine kinase during regeneration of zebrafish fin melanocytes. Development. 2001; 128(11):1943-9. DOI: 10.1242/dev.128.11.1943. View