Unusual development of light-reflecting pigment cells in intact and regenerating tail in the periodic albino mutant of Xenopus laevis

Abstract

Unusual light-reflecting pigment cells, “white pigment cells”, specifically appear in the periodic albino mutant (ap/ap) of Xenopus laevis and localize in the same place where melanophores normally differentiate in the wild-type. The mechanism responsible for the development of unusual pigment cells is unclear. In this study, white pigment cells in the periodic albino were compared with melanophores in the wild-type, using a cell culture system and a tail-regenerating system. Observations of both intact and cultured cells demonstrate that white pigment cells are unique in (1) showing characteristics of melanophore precursors at various stages of development, (2) accumulating reflecting platelets characteristic of iridophores, and (3) exhibiting pigment dispersion in response to α-melanocyte stimulating hormone (α-MSH) in the same way that melanophores do. When a tadpole tail is amputated, a functionally competent new tail is regenerated. White pigment cells appear in the mutant regenerating tail, whereas melanophores differentiate in the wild-type regenerating tail. White pigment cells in the mutant regenerating tail are essentially similar to melanophores in the wild-type regenerating tail with respect to their localization, number, and response to α-MSH. In addition to white pigment cells, iridophores which are never present in the intact tadpole tail appear specifically in the somites near the amputation level in the mutant regenerating tail. Iridophores are distinct from white pigment cells in size, shape, blue light-induced fluorescence, and response to α-MSH. These findings strongly suggest that white pigment cells in the mutant arise from melanophore precursors and accumulate reflecting platelets characteristic of iridophores.

A wide variety of Mitf transcript variants are expressed in the Xenopus laevis periodic albino mutant

“…These results coincide with previous reports that mitf and dct are expressed in melanin‐producing cells in X. laevis embryos (Kumasaka, Sato, Yajima, & Yamamoto, ; Kumasaka et al., ). It is likely that the expression of both mitf and dct in white pigment cells results in the formation of melanosomes at various stages of development, which has been described previously (Fukuzawa, ). Recently, tfec , another gene in the microphthalmia/transcription factor E (MiT/TFE) family ( mitf , tfe3 , tfeb , and tfec ), has been shown to be expressed in iridophores in zebrafish (Lister, Lane, Nguyen, & Lunney, ).…”

“…The Xenopus tadpole tail is particularly suited to examine gene expression differences between white pigment cells in the mutant and melanophores in the wild type. Only melanophores were present in the posterior region of the wild‐type tail, while in the mutant white pigment cells instead of melanophores were localized in this region (Fukuzawa, , ). Melanophores in the wild‐type tail looked black and did not reflect light; however, white pigment cells in the mutant tail looked brown under transmitted light, but white by reflecting light (Supporting Information Figure S2).…”

“…The periodic albino mutant ( a p / a p ) of X . laevis has been used to study the development and organellogenesis of pigment cells (Fukuzawa, , , ; Fukuzawa & Ide, , ; Hoperskaya, , ; MacMillan, , ). In this mutant, the oocytes do not contain melanin; however, melanin appears in the retinal pigment epithelium (RPE) and in skin melanophores at the larval stages, and then both RPE and melanophores gradually depigment during metamorphosis (Hoperskaya, , ).…”

“…White pigment cells, which show the characteristic features of both melanophores and iridophores, specifically appear in the periodic albino mutant and are localized where melanophores would normally differentiate in the wild type (Fukuzawa, ). White pigment cells are unique due to having (a) features of melanophore precursors at various stages of development and (b) reflecting platelets characteristic of iridophores, and (c) exhibiting pigment dispersion similar to that of melanophores in response to α‐melanocyte stimulating hormone (α‐MSH; Fukuzawa, ). White pigment cells in the mutant have been thought to arise from melanophore precursors, and accumulate reflecting platelets characteristic of iridophores (Fukuzawa, , ).…”

“…White pigment cells are unique due to having (a) features of melanophore precursors at various stages of development and (b) reflecting platelets characteristic of iridophores, and (c) exhibiting pigment dispersion similar to that of melanophores in response to α‐melanocyte stimulating hormone (α‐MSH; Fukuzawa, ). White pigment cells in the mutant have been thought to arise from melanophore precursors, and accumulate reflecting platelets characteristic of iridophores (Fukuzawa, , ). Previous experiments using suppressive subtractive hybridization have revealed that the ferritin H subunit gene is specifically expressed in white pigment cells but not in melanophores in the periodic albino mutant (Fukuzawa, ).…”