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Chromatophore

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Chromatophore is the collective term for pigment containing and light reflecting cells found in amphibians, fish, reptiles, crustaceans and cephalopods. Derived from the neural crest, chromatophores are largely responsible for generating skin and eye colour in poikilothermic animals. These cells are subclassed as xanthophores, erythrophores, iridophores, leucophores, melanophores and cyanophores according to their hue under white light. The translocation of pigment and reorientation of reflective plates within the cells are the mechanisms through which some species, notably chameleons and octopus, can rapidly change colour. Mammals and birds have just one class of chromatophore-like cell type, the melanocyte.

zebrafish chromatophores mediate background adaptation on exposure to dark (top) and light environments (bottom).

Classification

Chromforo was first used to describe invertebrate pigment bearing cells in 1819 and the term chromatophore (Greek: khrōma = "colour", phoros = "bearing") later adopted as a name for the neural crest derived pigment bearing cells of cold blooded vertebrates and cephalopods (in contrast to the chromato-cytes found in mammals and birds). By the 1960s, sufficient understanding of the structure and colour of chromatophores was available to sub-classify them according to appearance and, despite subsequent studies revealing the biochemical nature of the pigments within chromatophore types, this classification system persists.[1] While all chromatophores contain pigments or structural elements capable of reflecting light (except in mutant animals like albinos), not all pigment containing cells are chromatophores. Haem, for example, is a biopigment responsible for the red appearance of blood. It is primarily found in erythrocytes, which are generated in bone marrow and therefore not considered chromatophores.

Xanthophores and erythrophores

Originally termed lipophores due to their fat-soluble content, chromatophores that contain large amounts of yellow pteridine pigments were renamed xanthophores and those with an excess of red/orange carotinoids termed erythrophores. [1] Soon after, it was discovered that pterinosome and carotinoid vesicles are found within the same cell, and that the manifest colour depends on the ratio of red and yellow pigments. [2] Thus the distinction between these chromatophore types is essentially arbitrary. The capacity to biosynthesise pteridines from guanosine triphosphate de novo is a feature common to most chromatophores, but xanthophores appear to have supplemental biochemical pathways that result in an excess accumulation of yellow pigment. In contrast, carotinoids are metabolised from the diet and transported to erythrophores. Thus normally green frogs reared on a diet of carotene-restricted crickets display an erythrophore specific defect, resulting in a blue appearance.

 
A veiled chameleon, Chamaeleo calyptratus. Structural green and blue colours are generated by overlaying chromatophore types to reflect filtered light. A process known as Rayleigh scattering.

Iridophores and leucophores

Biochromes, such as pteridines and carotinoids, selectively absorb a part of the visual spectrum that makes up white incident light, while they let the other wavelengths pass and reach the eye of the observer. Not all colours are generated in this manner, however. Some, most notably blues and greens, are generated by the scattering, interference and diffusion of light by colourless crystalline structures called schemochromes.

Iridophores are lower vertebrate pigment cells that reflect light using plates of crystalline guanine schemochromes.[3] When illuminated they generate iridescent colours due to the diffraction of light within the stacked plates. Orientation of the schemochrome determines the nature of the structural colour observed.[4] By using biochromes as filters, iridophores mediate an optical effect known as Tyndall or Rayleigh scattering, producing bright blue or green colours that are not modified by the angle of vision.[5] A related type of chromatophore, the leucophore, is found in some fish species. Like iridophores, they utilize crystalline purines to reflect light, providing the bright white colour seen in some fish. As with xanthophores and erythrophores, the distinction between iridophores and leucophores in fish is not always obvious, but generally iridophores are considered to generate iridescent or metallic colours while leucophores produce structural white hues.[5]

Melanophores

The most widely studied chromatophore, due both to its extensive taxonomic distribution and apparent colour, is the melanophore. Eumelanin, the biochrome found in melanophores, is generated from tyrosine in a series of catalysed chemical reactions. The end product is a complex biopolymer containing units of dihydroxyindole and dihydroxyindole-2-carboxylic acid with some pyrrole rings.[6] This type of melanin, when packaged in vesicles called melanosomes and distributed throughout the cell, appears black or dark brown due to its light absorbing qualities. The key enzyme in melanogenesis is tyrosinase. When this protein is defective, no melanin can be generated resulting in albinism.

In some amphibian species there are other pigments packaged alongside eumelanin. For example, a novel deep red coloured pigment called was identified in the melanophores of phyllomedusine frogs.[7] This was subsequently identified as pterorhodin, a pterodine dimer that accumulates around eumelanin. While it is likely that other species have complex melanophore pigments, it is nevertheless true that the majority of melanophores studied to date contain eumelanin exclusively.

 
Dendrobates pumilio, a poison dart frog. Some brightly coloured species have unusual chromatophores of unknown pigment composition.

Cyanophores

In 1995 it was demonstrated that the vibrant blue colours of mandarin fish are not structural in nature. Instead, a cyan biochrome of unknown chemical nature is responsible.[5] This pigment, found within fibrous vesicles in at least two species callionymid fish, is highly unusual in the animal kingdom, as all other blue colourings thus far investigated are schemochromatic. Therefore a novel chromatophore type, the cyanophore, was proposed. Although cyanophores are unusual in their taxonomic restriction, there may be other unusual chromatophore types in lesser-studied fish and amphibians. Indeed, bright coloured chromatophores with undefined pigments have been observed in both poison dart frogs and glass frogs.[8]

Pigment translocation

Many species have the ability to translocate the pigment inside chromatophores, resulting in an apparent change in colour. This process, known as physiological colour change, is most widely studied in melanophores, as melanin is the darkest and most visible pigment. In most species with a relatively thin dermis, the dermal melanophores tend to be flat and cover a large surface area. However, in animals with thick dermal layers, such as adult reptiles, dermal melanophores often form three-dimensional units with other chromatophores. These dermal chromatophore units (DCU) consist of an uppermost xanthophore or erythrophore layer, then an iridophore layer, and finally a basket-like melanophore layer with processes covering the iridophores.[9]

Both types of dermal melanophores are extremely important in physiological colour change. Flat dermal melanophores will often overlay other chromatophores so when the pigment is dispersed throughout the cell the skin appears dark. When the pigment is aggregated towards the centre of the cell, the pigments in other chromatophores are exposed to light and thus the skin takes on their hue. Similarly, after melanin aggregation in DCUs, the skin appears green through xanthophore (yellow) filtering of scattered (blue) light from the iridophore layer. On the dispersion of melanin, the light is no longer scattered and the skin appears dark. As the other biochromatic chomatophores are also capable of pigment translocation, by making good use of the divisional effect animals with multiple chromatophore types can generate a spectacular array of skin colours.[10],[11]

 
A single zebrafish melanophore imaged by time lapse during pigment aggregation after treatment with melanin concentrating hormone.

The control and mechanics of rapid pigment translocation has been well studied in a multitude of species, particularly amphibians and teleost fish. [12],[5] It has been demonstrated that the process can be under hormonal, neuronal control or both. Neurochemicals that are known to translocate pigment include noradrenaline, via its α2-adrenoceptor on the surface on melanophores.[13] The primary hormones involved in regulating translocation appear to be the melanocortins, melatonin and melanin concentrating hormone (MCH), that are produced mainly in the pituitary, pineal gland and hypothalamus respectively, though may also be generated in a paracrine fashion by peripheral tissues. At the surface of the melanophore these peptides have been shown to activate specific G protein coupled receptors that, in turn, transduce the signal into the cell. Melanocortins result in the dispersion of pigment, while melatonin and MCH results in aggregation.[14]

Numerous melanocortin, MCH and melatonin receptors have been identified in fish [15] and frogs,[16] including the orthologue of MC1R,[17] a melanocortin receptor known to regulate skin and hair colour in humans.[18] Inside the cell, cyclic adenosine monophosphate (cAMP) has been shown to be an important second messenger of pigment translocation. Through a mechanism not yet fully understood, cAMP influences other proteins to drive molecular motors carrying melanosomes along both microtubules and microfilaments.[19],[20],[21]


Background adaptation

Most fish, reptiles and amphibians animals undergo physiological colour change in response to a change in environment. Known as background adaptation, this most commonly manifests as a slight darkening or lightening of skin tone to approximately mimic the hue of the immediate environment, a type of camouflage. It has been demonstrated that the process is vision dependent (the animal needs to be able to see the environment to adapt to it),[22] and that melanin translocation in melanophores is the primary mechanism for colour change.[14] Some animals, such as chameleons and anoles, have a highly evolved background adaptation response capable of generating different colours very rapidly. They have adapted this capability to change colour in response to temperature, mood, stress levels and social cues, rather than to simply mimic their environment.

 
Transverse section of a developing vertebrate trunk showing the dosolateral (red) and ventromedial (blue) routes of chromatoblast migration.

Development

During vertebrate embryonic development, chromatophores are one of a number of cell types generated in the neural crest, a paired strip of cells arising at the margins of the neural tube. These cells have the ability to migrate long distances, allowing chromatophores to populate many organs of the body, including the skin, eye, ear and brain. Leaving the neural crest in waves, chromatophores take either a dorsolateral route through the dermis, entering the ectoderm through small holes in the basal lamina, or a ventromedial route between the somites and the neural tube. The exception to this are the melanophores of the retinal pigmented epithelium of the eye, these are not derived from the neural crest, instead an outpouching of the neural tube generates the optic cup which, in turn, forms the retina.

When and how multipotent chromatophore precursor cells (called chromatoblasts) develop into their daughter subtypes is an area of ongoing research. It is known in zebrafish embryos, for example, that by 3 days after fertilization each of the cell classes found in the adult fish - melanophores, xanthophores and iridophores - are already present. Studies using mutant fish have demonstrated that transcription factors such as, kit, sox10 and mitf are important in controlling chromatophore differentiation.[23]

Practical applications

In addition to basic research into better understanding of chromatophores themselves, the cells are used for applied research purposes. For example, zebrafish larvae are used to study how chromatophores undergo controlled proliferation and migration during embryogenesis to accurately generate the regular horizontal striped pattern in seen in adult fish.[24] This is seen as a useful model system for understanding patterning in the evolutionary developmental biology field. Chromatophore biology has also been used to model human condition or disease, mainly melanoma. Recently the gene responsible for the melanophore-specific golden phenotype in zebrafish, Slc24a5, was shown to have a human equivalent that strongly corrolates with skin colour.[25]

Chromatophores are also used as a biomarker of blindness in poikilotherms, as animals with certain visual defects fail to background adapt to light environments. [22] Human homologues of receptors that mediate pigment translocation in melanophores are thought to involved in processes such as appetite suppression and tanning, making them attractive targets for drugs.[17] Therefore pharmaceutical companies have developed a biological assay for rapidly identifying potential active compounds using melanophores from the African clawed frog.[26] Other scientists have developed techniques for using melanophores as biosensors,[27] and for rapid disease detection (based on the discovery that pertussis toxin blocks pigment aggregation in fish melanophores).[28] Potential military applications of chromatophore mediated colour changes have been proposed, mainly as a type of adaptive camouflage.[29] However, currently this does not appear to have been realised.


 
An adult Euprymna scolopes, a species of sepiolid squid, displaying large melanophores, erthrophores and xanthophores.

Cephalopod chromatophores

Most notable in brightly coloured squid, cuttlefish and octopuses, cephalopods have complex multicellular 'organs' which they use to change colour rapidly. Each chromotophore unit is composed of a single chromatophore cell and numerous muscle, nerve, glial and sheath cells.[30] Inside the chromatophore cell, pigment granules are inclosed in an elastic sac, called the cytoelastic sacculus. To change colour the animal distorts the sacculus form or size by muscular contraction, thus changing its translucency, reflectivity or opacity. This differs from the mechanism used in fish, amphibians and reptiles, in that the shape of the sacculus is being changed rather than a translocation of pigment vesicles within the cell. Octopuses operate chromatophores in complex, multi-cellular chromatic displays, resulting in a spectacular variety of colour schemes. Often repetitive waves of colour changes are observed as over 1 million neurons controlling the muscular contractions are patterned in the basal and peduncle lobes of the brain.[31] Like chameleons, cephalopods use physiological colour change for social interaction. They are also among the most skilled at background adaptation, having the ability to match both the colour and the texture of their local environment with remarkable accuracy.

Notes

  1. ^ a b Bagnara JT. Cytology and cytophysiology of non-melanophore pigment cells. Int Rev Cytol. 1966; 20:173-205. Cite error: The named reference "Cytology" was defined multiple times with different content (see the help page).
  2. ^ Matsumoto J. Studies on fine structure and cytochemical properties of erythrophores in swordtail, Xiphophorus helleri. J Cell Biol. 1965; 27:493-504.
  3. ^ Taylor JD. The effects of intermedin on the ultrastructure of amphibian iridophores. Gen Comp Endocrinol. 1969; 12:405-16.
  4. ^ Morrison RL. A transmission electron microscopic (TEM) method for determining structural colors reflected by lizard iridophores. Pigment Cell Res. 1995; 8:28-36.
  5. ^ a b c d Fujii R. The regulation of motile activity in fish chromatophores. Pigment Cell Res. 2000; 13:300-19. Cite error: The named reference "fish" was defined multiple times with different content (see the help page).
  6. ^ Ito S & Wakamatsu K. Quantitative analysis of eumelanin and pheomelanin in humans, mice, and other animals: a comparative review. Pigment Cell Res. 2003; 16:523-31.
  7. ^ Bagnara JT et al. Color changes, unusual melanosomes, and a new pigment from leaf frogs. Science. 1973; 182:1034-5.
  8. ^ Schwalm PA et al. Infrared reflectance in leaf-sitting neotropical frogs. Science. 1977; 196:1225-7.
  9. ^ Bagnara JT et al. The dermal chromatophore unit. J Cell Biol. 1968; 38:67-79.
  10. ^ Palazzo RE et al. Rearrangements of pterinosomes and cytoskeleton accompanying pigment dispersion in goldfish xanthophores. Cell Motil Cytoskeleton. 1989; 13:9-20.
  11. ^ Porras MG et al. Corazonin promotes tegumentary pigment migration in the crayfish Procambarus clarkii. Peptides. 2003; 24:1581-9.
  12. ^ Deacon SW et al. Dynactin is required for bidirectional organelle transport. J Cell Biol. 2003; 160:297-301.
  13. ^ Aspengren S et al. Noradrenaline- and melatonin-mediated regulation of pigment aggregation in fish melanophores. Pigment Cell Res. 2003; 16:59-64.
  14. ^ a b Logan DW et al. Regulation of pigmentation in zebrafish melanophores. Pigment Cell Res. 2006; 19:206-13.
  15. ^ Logan DW et al. Sequence characterization of teleost fish melanocortin receptors. Ann N Y Acad Sci. 2003; 994:319-30.
  16. ^ Sugden D et al. Melatonin, melatonin receptors and melanophores: a moving story. Pigment Cell Res. 2004; 17:454-60.
  17. ^ a b Logan DW et al. The structure and evolution of the melanocortin and MCH receptors in fish and mammals. Genomics. 2003; 81:184-91.
  18. ^ Valverde P et al. Variants of the melanocyte-stimulating hormone receptor gene are associated with red hair and fair skin in humans. Nat Genet. 1995; 11:328-30.
  19. ^ Snider J et al. Intracellular actin-based transport: how far you go depends on how often you switch. Proc Natl Acad Sci USA. 2004; 101:13204-9.
  20. ^ Rodionov VI et al. Functional coordination of microtubule-based and actin-based motility in melanophores. Curr Biol. 1998; 8:165-8.
  21. ^ Rodionov VI et al. Switching between microtubule- and actin-based transport systems in melanophores is controlled by cAMP levels. Curr Biol. 2003; 13:1837-47.
  22. ^ a b Neuhauss SC. Behavioral genetic approaches to visual system development and function in zebrafish. J Neurobiol. 2003; 54:148-60.
  23. ^ Kelsh RN et al. Genetic analysis of melanophore development in zebrafish embryos. Dev Biol. 2000; 225:277-93.
  24. ^ Kelsh RN. Genetics and evolution of pigment patterns in fish. Pigment Cell Res. 2004; 17:326-36.
  25. ^ Lamason RL et al. SLC24A5, a putative cation exchanger, affects pigmentation in zebrafish and humans. Science. 2005; 310:1782-6.
  26. ^ Jayawickreme CK et al. Use of a cell-based, lawn format assay to rapidly screen a 442,368 bead-based peptide library. J Pharmacol Toxicol Methods. 1999; 42:189-97.
  27. ^ Andersson TP et al. Frog melanophores cultured on fluorescent microbeads: biomimic-based biosensing. Biosens Bioelectron. 2005; 21:111-20.
  28. ^ Karlsson JO et al. The melanophore aggregating response of isolated fish scales: a very rapid and sensitive diagnosis of whooping cough. FEMS Microbiol Lett. 1991; 66:169-75
  29. ^ Lee I. Nanotubes for noisy signal processing: Adaptive Camouflage PhD Thesis. 2005; University of Southern California
  30. ^ Cloney RA. & Florey E. Ultrastructure of cephalopod chromatophore organs. Zeits. für Zellforsch. 1968; 89:250-280.
  31. ^ Demski LS. Chromatophore systems in teleosts and cephalopods: a levels oriented analysis of convergent systems. Brain Behav Evol. 1992; 40:141-56.

See also

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