Zebrafish Melanophilin Facilitates Melanosome Dispersion by Regulating Dynein

Sheets, Lavinia; Ransom, David G.; Mellgren, Eve M.; Johnson, Stephen L.; Schnapp, Bruce J.

doi:10.1016/j.cub.2007.09.028

Cited by 75 publications

(73 citation statements)

References 37 publications

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“…8 were generated with a Tol2 transposon bearing the Xenopus EF1a promoter (Johnson and Krieg, 1995) driving GFP expression (EF1a >GFP, T. Chen and S.L.J., unpublished). We injected 25 pg EF1a >GFP transposon plasmid and 20 pg capped transposase mRNA into one-or two-cell mlpha/mlpha (Sheets et al, 2007) embryos, sorted for GFP + embryos at 24 hours, and reared these to adult stages before scoring for melanocyte, xanthophore or iridophore clones.…”

Section: Generation Of Mosaic Animalsmentioning

confidence: 99%

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Clonal analyses reveal roles of organ founding stem cells, melanocyte stem cells and melanoblasts in establishment, growth and regeneration of the adult zebrafish fin

Johnson

2010

Development

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this marker express GFP weakly in somatic muscle (which is absent in the fin), and strongly in all differentiated melanocytes, making it appropriate for fin melanocyte lineage analysis. In addition, the Xenopus EF1a promoter drives GFP (EF1a>GFP) (Johnson and Krieg, 1995) with ubiquitous expression, making it suitable to compare lineage relationship of melanocytes with other cell types in the fin.Here, we use clonal and lineage analyses to study the contribution of melanocyte lineages to the adult fin. Clones generated by the fTyrp>GFP transposon reveal the number of melanocyte-producing FSCs (mFSCs) that contribute to the anal and caudal fins, melanin-less differentiation in PTU shows where new melanocytes develop, X-irradiation induced clones uncover the role of individual stem cells in the growing fin, and labeling with the EF1a>GFP transposon shows the relationship of melanocytes to other pigmented cells. We also show that ontogenetic and regeneration melanocytes of the adult fin are derived from the same mFSCs, and that kit-dependent and kitindependent regeneration melanocytes (Rawls and Johnson, 2000) Development 137, 3931-3939 (2010) SUMMARYIn vertebrates, the adult form emerges from the embryo by mobilization of precursors or adult stem cells. What different cell types these precursors give rise to, how many precursors establish the tissue or organ, and how they divide to establish and maintain the adult form remain largely unknown. We use the pigment pattern of the adult zebrafish fin, with a variety of clonal and lineage analyses, to address these issues. Early embryonic labeling with lineage-marker-bearing transposons shows that all classes of fin melanocytes (ontogenetic, regeneration and kit-independent melanocytes) and xanthophores arise from the same melanocyte-producing founding stem cells (mFSCs), whereas iridophores arise from distinct precursors. Additionally, these experiments show that, on average, six and nine mFSCs colonize the caudal and anal fin primordia, and daughters of different mFSCs always intercalate to form the adult pattern. Labeled clones are arrayed along the proximal-distal axis of the fin, and melanocyte time-of-differentiation lineage assays show that although most of the pigment pattern growth is at the distal edge of the fin, significant growth also occurs proximally. This suggests that leading edge melanocyte stem cells (MSCs) divide both asymmetrically to generate new melanocytes, and symmetrically to expand the MSCs and leave quiescent MSCs in their wake. Clonal labeling in adult stages confirms this and reveals different contributions of MSCs and transient melanoblasts during growth. These analyses build a comprehensive picture for how MSCs are established and grow to form the pigment stripes of the adult zebrafish fins.

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Section: Generation Of Mosaic Animalsmentioning

confidence: 99%

“…8A) and screened 845 fish that survived to adulthood for labeled melanocyte clones. Failure of melanosome dispersion in mlpha mutants (Sheets et al, 2007) allows for easier identification of GFP + melanocytes. We identified 22 fish with EF1a>GFP labeled melanocytes in their fins.…”

Section: Melanocytes and Xanthophores Arise From The Same Fin Progenimentioning

confidence: 99%

Clonal analyses reveal roles of organ founding stem cells, melanocyte stem cells and melanoblasts in establishment, growth and regeneration of the adult zebrafish fin

Johnson

2010

Development

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Section: Introductionmentioning

confidence: 99%

“…Rab27a, through geranylgeranylation, attaches to the melanosome membrane, and melanophilin connects myosin-Va and Rab27a. Myosin-V-based intracellular movement has been analyzed in many other eukaryotes, including frogs, fish, mammals, and plants; plant myosin-XI is the functional homologue of yeast and vertebrate myosin-V ( Kinkema and Schiefelbein, 1994;Provance and Mercer, 1999;Tuma and Gelfand, 1999;Desnos et al, 2007;Li and Nebenfuhr, 2007;Sheets et al, 2007;Shimmen, 2007).Genetic screens have identified several molecules that play a role in organelle inheritance. For example, vacuole inheritance utilizes the actin cytoskeleton and the class-V myosin complex, composed of Myo2p, Vac17p, and Vac8p (Hill et al, 1996;Wang et al, 1998;Ishikawa et al, 2003;Tang et al, 2003).…”

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confidence: 99%

PTC1Is Required for Vacuole Inheritance and Promotes the Association of the Myosin-V Vacuole-specific Receptor Complex

Jin

Eves

Tang

et al. 2009

MBoC

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Organelle inheritance occurs during cell division. In Saccharomyces cerevisiae, inheritance of the vacuole, and the distribution of mitochondria and cortical endoplasmic reticulum are regulated by Ptc1p, a type 2C protein phosphatase. Here we show that PTC1/VAC10 controls the distribution of additional cargoes moved by a myosin-V motor. These include peroxisomes, secretory vesicles, cargoes of Myo2p, and ASH1 mRNA, a cargo of Myo4p. We find that Ptc1p is required for the proper distribution of both Myo2p and Myo4p. Surprisingly, PTC1 is also required to maintain the steady-state levels of organelle-specific receptors, including Vac17p, Inp2p, and Mmr1p, which attach Myo2p to the vacuole, peroxisomes, and mitochondria, respectively. Furthermore, Vac17p fused to the cargo-binding domain of Myo2p suppressed the vacuole inheritance defect in ptc1⌬ cells. These findings suggest that PTC1 promotes the association of myosin-V with its organelle-specific adaptor proteins. Moreover, these observations suggest that despite the existence of organelle-specific receptors, there is a higher order regulation that coordinates the movement of diverse cellular components. INTRODUCTIONDuring each cell cycle, cytoplasmic organelles are actively distributed between dividing cells to maintain organelle copy number and volume. The yeast Saccharomyces cerevisiae is an excellent model system for studying the spatial and temporal control of organelle inheritance. In yeast, several organelles are transmitted from mother to daughter cells. These include the vacuole, mitochondria, the endoplasmic reticulum (ER), late-Golgi elements and peroxisomes (reviewed in Weisman, 2006).Early in the cell cycle, a portion of each organelle is transported into the emerging bud. The polarized transport of most organelles from the mother to the bud is an active process that requires the actin cytoskeleton, myosin-V motors, and receptor proteins, which physically connect the motor to organelle cargoes (Beach et al., 2000;Yin et al., 2000;Boldogh et al., 2001;Barr, 2002;Bretscher, 2003;Du et al., 2004;Fagarasanu et al., 2006bFagarasanu et al., , 2007Weisman, 2006). Thus, formation of a complex between the motor and receptor protein is important for polarized organelle transport.Similar to yeast, in vertebrates, myosin-V motors move cargoes along the actin cytoskeleton. The best studied cargo of vertebrate myosin-V are melanosomes, which are moved in melanocytes by myosin-Va. Melanosomes attach to myosin-Va through Rab27a and melanophilin (Fukuda and Kuroda, 2002;Wu et al., 2002). Rab27a, through geranylgeranylation, attaches to the melanosome membrane, and melanophilin connects myosin-Va and Rab27a. Myosin-V-based intracellular movement has been analyzed in many other eukaryotes, including frogs, fish, mammals, and plants; plant myosin-XI is the functional homologue of yeast and vertebrate myosin-V ( Kinkema and Schiefelbein, 1994;Provance and Mercer, 1999;Tuma and Gelfand, 1999;Desnos et al., 2007;Li and Nebenfuhr, 2007;Sheets et al., 2007;Shimmen, 2007).Ge...

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“…WT fish were either the inbred SJA line or melanophilina (mlpha) (Sheets et al, 2007) mutants. mlpha mutants contain contracted melanosomes, facilitating quantitative analysis, but have no other melanocyte defects (Sheets et al, 2007;Hultman et al, 2009). All clonal analysis was performed in mlpha or mlpha; kita null/+ embryos.…”

Section: Fish Stocks and Husbandrymentioning

confidence: 99%

Kit signaling is involved in melanocyte stem cell fate decisions in zebrafish embryos

O'Reilly-Pol

Johnson

2013

Development

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SUMMARYAdult stem cells are crucial for growth, homeostasis and repair of adult animals. The melanocyte stem cell (MSC) and melanocyte regeneration is an attractive model for studying regulation of adult stem cells. The process of melanocyte regeneration can be divided into establishment of the MSC, recruitment of the MSC to produce committed daughter cells, and the proliferation, differentiation and survival of these daughter cells. Reduction of Kit signaling results in dose-dependent reduction of melanocytes during larval regeneration. Here, we use clonal analysis techniques to develop assays to distinguish roles for these processes during zebrafish larval melanocyte regeneration. We use these clonal assays to investigate which processes are affected by the reduction in Kit signaling. We show that the regeneration defect in kita mutants is not due to defects in MSC recruitment or in the proliferation, differentiation or survival of the daughter cells, but is instead due to a defect in stem cell establishment. Our analysis suggests that the kit MSC establishment defect results from inappropriate differentiation of the MSC lineage.

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Zebrafish Melanophilin Facilitates Melanosome Dispersion by Regulating Dynein

Abstract: We propose that cAMP-induced melanosome dispersion depends on the actin-independent suppression of dynein by Mlpha and that Mlpha coordinates the early outward movement of melanosomes along microtubules and their later transfer to actin filaments.

Cited by 75 publications

References 37 publications

Clonal analyses reveal roles of organ founding stem cells, melanocyte stem cells and melanoblasts in establishment, growth and regeneration of the adult zebrafish fin

Clonal analyses reveal roles of organ founding stem cells, melanocyte stem cells and melanoblasts in establishment, growth and regeneration of the adult zebrafish fin

PTC1Is Required for Vacuole Inheritance and Promotes the Association of the Myosin-V Vacuole-specific Receptor Complex

Kit signaling is involved in melanocyte stem cell fate decisions in zebrafish embryos

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