Hyperpigmentation Results in Aberrant Immune Development in Silky Fowl (Gallus gallus domesticus Brisson).

Deping Han,Shuxiang Wang,Junying Li,Xuemei Deng,Jiankui Wang,Zu Yang,Yuanyuan Zhang,Xianggui Dong,Yanxin Hu,Andrzej T Slominski

doi:10.1371/journal.pone.0125686

Abstract

The Silky Fowl (SF) is known for its special phenotypes and atypical distribution of melanocytes among internal organs. Although the genes associated with melanocyte migration have been investigated substantially, there is little information on the postnatal distribution of melanocytes in inner organs and the effect of hyperpigmentation on the development of SF. Here, we analyzed melanocyte distribution in 26 tissues or organs on postnatal day 1 and weeks 2, 3, 4, 6, 10, and 23. Except for the liver, pancreas, pituitary gland, and adrenal gland, melanocytes were distributed throughout the body, primarily around blood vessels. Interaction between melanocytes and the tissue cells was observed, and melanin was transported by filopodia delivery through engulfed and internalized membrane-encapsulated melanosomes. SFs less than 10 weeks old have lower indices of spleen, thymus, and bursa of Fabricius than White Leghorns (WLs). The expression levels of interferon-γ and interlukin-4 genes in the spleen, and serum antibody levels against H5N1 and infectious bursal disease virus were lower in SF than in WL. We also found immune organ developmental difference between Black-boned and non-Black- boned chickens from SFs and WLs hybrid F2 population. However, degeneration of the thymus and bursa of Fabricius occurred later in SF than in WL after sexual maturity. Analysis of apoptotic cells and apoptosis-associated Bax and Bcl-2 proteins indicated that apoptosis is involved in degeneration of the thymus and bursa of Fabricius. Therefore, these results suggest that hyperpigmentation in SF may have a close relationship with immune development in SF, which can provide an important animal model to investigate the roles of melanocyte.

Highlights

The Silky Fowl (SF) is a natural mutant breed in China with unique morphological features such as fluffy head feathers, rose comb, blue earlobes, silky feathers, black skin, hair-like leg feathers, and five toes
After dissection and comparison with White Leghorns (WLs), significant distribution of melanin was visible in multiple SF tissues by anatomy, including the skin, connective tissues, skeletal muscle, respiratory tract, immune organs, intestines, and reproductive organs
Melanoblasts originate from neural crest cells, migrate through the mesenchyme of the developed embryo, and give rise to melanocytes [22]

Summary

Introduction

The Silky Fowl (SF) is a natural mutant breed in China with unique morphological features such as fluffy head feathers, rose comb, blue earlobes, silky feathers, black skin, hair-like leg feathers, and five toes. Comprehensive understanding of the mechanism of benign hyperpigmentation may facilitate investigations of the functions of melanocytes during the development of SF and may help understand the pathogenesis of melanoma in mammals. A few studies have analyzed the effects of hyperpigmentation in inner organs that affect the development of SF. We found that genes involved in the innate and adoptive immune responses are up and down regulated, respectively, during embryonic development on days 3, 3.5, 4, and 4.5 [19]. We determined the histological distribution of melanocytes and analyzed the populations of immune cells and cytokine gene expression in immune organs during development in SF, White Leghorn (WL), and the hybrid F2 generation birds

Materials and Methods

Results

Discussion