Eyes and Lenses; Crystallins
Prog Retin Eye Res 1998 Oct;17(4):597-636
The eyes of deep-sea fish. I: Lens pigmentation, tapeta and visual pigments.
Douglas RH, Partridge JC, Marshall NJ
Department Optometry and Visual Science, City University, London, U.K.
Deep-sea fish, defined as those living below 200 m, inhabit a most unusual photic environment, being exposed to two sources of visible radiation; very dim downwelling sunlight and bioluminescence, both of which are, in most cases, maximal at wavelengths around 450-500 nm. This paper summarises the reflective properties of the ocular tapeta often found in these animals, the pigmentation of their lenses and the absorption characteristics of their visual pigments. Deep-sea tapeta usually appear blue to the human observer, reflecting mainly shortwave radiation. However, reflection in other parts of the spectrum is not uncommon and uneven tapetal distribution across the retina is widespread. Perhaps surprisingly, given the fact that they live in a photon limited environment, the lenses of some deep-sea teleosts are bright yellow, absorbing much of the shortwave part of the spectrum. Such lenses contain a variety of biochemically distinct pigments which most likely serve to enhance the visibility of bioluminescent signals. Of the 195 different visual pigments characterised by either detergent extract or microspectrophotometry in the retinae of deep-sea fishes, ca. 87% have peak absorbances within the range 468-494 nm. Modelling shows that this is most likely an adaptation for the detection of bioluminescence. Around 13% of deep-sea fish have retinae containing more than one visual pigment. Of these, we highlight three genera of stomiid dragonfishes, which uniquely produce far red bioluminescence from suborbital photophores. Using a combination of longwave-shifted visual pigments and in one species (Malacosteus niger) a chlorophyll-related photosensitizer, these fish have evolved extreme red sensitivity enabling them to see their own bioluminescence and giving them a private spectral waveband invisible to other inhabitants of the deep-ocean.
Prog Retin Eye Res 1998 Oct;17(4):637-85
The eyes of deep-sea fish. II. Functional morphology of the retina.
Wagner HJ, Frohlich E, Negishi K, Collin SP
Anatomisches Institut, Eberhard-Karls-Universitat Tubingen, Germany.
Three different aspects of the morphological organisation of deep-sea fish retinae are reviewed: First, questions of general cell biological relevance are addressed with respect to the development and proliferation patterns of photoreceptors, and problems associated with the growth of multibank retinae, and with outer segment renewal are discussed in situations where there is no direct contact between the retinal pigment epithelium and the tips of rod outer segments. The second part deals with the neural portion of the deep-sea fish retina. Cell densities are greatly reduced, yet neurohistochemistry demonstrates that all major neurotransmitters and neuropeptides found in other vertebrate retinae are also present in deep-sea fish. Quantitatively, convergence rates in unspecialised parts of the retina are similar to those in nocturnal mammals. The differentiation of horizontal cells makes it unlikely that species with more than a single visual pigment are capable of colour vision. In the third part, the diversity of deep-sea fish retinae is highlighted. Based on the topography of ganglion cells, species are identified with areae or foveae located in various parts of the retina, giving them a greatly improved spatial resolving power in specific parts of their visual fields. The highest degree of specialisation is found in tubular eyes. This is demonstrated in a case study of the scopelarchid retina, where as many as seven regions with different degrees of differentiation can be distinguished, ranging from an area giganto cellularis, regions with grouped rods to retinal diverticulum.
Prog Retin Eye Res 1998 Apr;17(2):145-74
Published erratum appears in Prog Retin Eye Res 1999 Jul;18(4):552
Gene sharing in lens and cornea: facts and implications.
Piatigorsky J
Laboratory of Molecular and Developmental Biology, National Eye Institute, National Institutes of Health, Bethesda, MD 20892-2730, USA.
The major water-soluble proteins (crystallins) responsible for the optical properties of the cellular lenses of vertebrates and invertebrates are surprisingly diverse and often differ among species (i.e., are taxon-specific). Many crystallins are encoded by the identical gene specifying a stress protein or a metabolic enzyme which has non-refractive functions in numerous tissues. This double use of a distinct protein has been called gene sharing. Abundant expression of various metabolic enzymes also occurs in a taxon-specific manner in corneal epithelial cells, suggesting that gene sharing extends to this transparent tissue. It has been proposed that one of the most abundant corneal enzymes (aldehyde dehydrogenase class 3) may protect the eye by directly absorbing ultraviolet light, as well as by providing an enzymatic function. It also seems possible that the high expression of corneal enzymes (5-40% of the water-soluble proteins) may reduce scattering in the corneal epithelium by minimizing spatial fluctuations in refractive index as they do in the lens. Thus, gene sharing may be a widespread phenomenon encompassing the lens, cornea and probably other systems. Lens-preferred expression of crystallin genes is integrated in a complex developmental program utilizing in many cases Pax-6. The differential expression of alpha B-crystallin (a small heat shock protein) in different tissues involves the combinatorial use of both shared and lens-specific cis-control elements. Corneal-preferred gene expression appears to depend in part on induction by environmental influences. Among the implications of gene sharing are that gene duplication is not required for the evolution of a new protein phenotype, a change in gene regulation is sufficient, that proteins may be under more than one selective constraint, affecting their evolutionary clock, and that it would be prudent to consider the possibility that any given gene may have important, unrecognized roles when planning to implement gene therapy in the future.
Physiol Rev 1997 Jan;77(1):21-50
Physiological properties of the normal lens.
Mathias RT, Rae JL, Baldo GJ
Department of Physiology and Biophysics, State University of New York, Stony Brook, USA.
The lens is an avascular organ suspended between the aqueous and vitreous humors of the eye. The cellular structure is symmetric about an axis passing through its anterior and posterior poles but asymmetric about a plane passing through its equator. Because of its asymmetric structure, the lens has historically been assumed to perform transport between the aqueous and vitreous humors. Indeed, when anterior and posterior surfaces were isolated in an Ussing chamber, a translens current was measured. However, in the eye, the two surfaces are not isolated. The vibrating probe technique showed the current densities at the surface of a free-standing lens were surprisingly large, about an order of magnitude greater than measured in an Ussing chamber, and were not directed across the lens. Rather, they were inward in the region of either anterior or posterior pole and outward at the equator. This circulating current is the most dramatic physiological property of a normal lens. We believe it is essential to maintain clarity; hence, this review focuses on factors likely to drive and direct it. We review properties and spatial distribution of lens Na+/K+ pumps, ion channels, and gap junctions. Based on these data, we propose a model in which the difference in electromotive potential of surface versus interior cell membranes drives the current, whereas the distribution of gap junctions directs the current in the observed pattern. Although this model is clearly too simple, it appears to quantitatively predict observed currents. However, the model also predicts fluid will move in the same pattern as ionic current. We therefore speculate that the physiological role of the current is to create an internal circulatory system for the avascular lens.
Eur J Biochem 1996 Feb 1;235(3):449-65
Lens crystallins of invertebrates--diversity and recruitment from detoxification enzymes and novel proteins.
Tomarev SI, Piatigorsky J
Laboratory of Molecular and Developmental Biology, National Eye Institute, National Institutes of Health, Bethesda, MD 20892-2730, USA.
The major proteins (crystallins) of the transparent, refractive eye lens of vertebrates are a surprisingly diverse group of multifunctional proteins. A number of lens crystallins display taxon-specificity. In general, vertebrate crystallins have been recruited from stress-protective proteins (i.e. the small heat-shock proteins) and a number of metabolic enzymes by a gene-sharing mechanism. Despite the existence of refractive lenses in the complex and compound eyes of many invertebrates, relatively little is known about their crystallins. Here we review for the first time the state of knowledge of invertebrate crystallins. The major cephalopod (squid, octopus, and cuttlefish) crystallins (S-crystallins) have, like vertebrate crystallins, been recruited from a stress protective metabolic enzyme, glutathione S-transferase. The presence of overlapping AP-1 and antioxidant responsive-like sequences that appear functional in transfected vertebrate cells suggest that the recruitment of glutathione S-transferase to S-crystallins involved response to oxidative stress. Cephalopods also have at least two taxon-specific crystallins: omega-crystallin, related to aldehyde dehydrogenase, and omega-crystallin, related to a superfamily of lipid-binding proteins. L-crystallin (probably identical to O-crystallin) is the major protein of the lens of the squid photophore, a specialized structure for emitting light. The use of L/omega-crystallin in the ectodermal lens of the eye and the mesodermal lens of the photophore of the squid contrasts with the recruitment of different crystallins in the ectodermal lenses of the eye and photophore of fish. S-and omega-crystallins appear to be lens-specific (some S-crystallins are also expressed in cornea) and, except for one S-crystallin polypeptide (SL11/Lops4; possibly a molecular fossil), lack enzymatic activity. The S-crystallins (except SL11/Lops4) contain a variable peptide that has been inserted by exon shuffling. The only other invertebrate crystallins that have been examined are in one marine gastropod (Aplysia, a sea hare), in jellyfish and in the compound eyes of some arthropods; all are different and novel proteins. Drosocrystallin is one of three calcium binding taxon-specific crystallins found selectively in the acellular corneal lens of Drosophila, while antigen 3G6 is a highly conserved protein present in the ommatidial crystallin cone and central nervous system of numerous arthropods. Cubomedusan jellyfish have three novel crystallin families (the J-crystallins); the J1-crystallins are encoded in three very similar intronless genes with markedly different 5' flanking sequences despite their almost identical encoded proteins and high lens expression. The numerous refractive structures that have evolved in the eyes of invertebrates contrast markedly with the limited information on their protein composition, making this field as exciting as it is underdeveloped. The similar requirement of Pax-6 (and possibly other common transcription factors) for eye development as well as the diversity, taxon-specificity and recruitment of stress-protective enzymes as crystallins suggest that borrowing multifunctional proteins for refraction by a gene sharing strategy may have occurred in invertebrates as did in vertebrates.
Eur J Biochem 1994 Oct 1;225(1):1-19
Structure and modifications of the junior chaperone alpha-crystallin. From lens transparency to molecular pathology.
Groenen PJ, Merck KB, de Jong WW, Bloemendal H
Department of Biochemistry, University of Nijmegen, The Netherlands.
alpha-Crystallin is a high-molecular-mass protein that for many decades was thought to be one of the rare real organ-specific proteins. This protein exists as an aggregate of about 800 kDa, but its composition is simple. Only two closely related subunits termed alpha A- and alpha B-crystallin, with molecular masses of approximately 20 kDa, form the building blocks of the aggregate. The idea of organ-specificity had to be abandoned when it was discovered that alpha-crystallin occurs in a great variety of nonlenticular tissues, notably heart, kidney, striated muscle and several tumors. Moreover alpha B-crystallin is a major component of ubiquinated inclusion bodies in human degenerative diseases. An earlier excitement arose when it was found that alpha B-crystallin, due to its very similar structural and functional properties, belongs to the heat-shock protein family. Eventually the chaperone nature of alpha-crystallin could be demonstrated unequivocally. All these unexpected findings make alpha-crystallin a subject of great interest far beyond the lens research field. A survey of structural data about alpha-crystallin is presented here. Since alpha-crystallin has resisted crystallization, only theoretical models of its three-dimensional structure are available. Due to its long life in the eye lens, alpha-crystallin is one of the best studied proteins with respect to post-translational modifications, including age-induced alterations. Because of its similarities with the small heat-shock proteins, the findings about alpha-crystallin are illuminative for the latter proteins as well. This review deals with: structural aspects, post-translational modifications (including deamidation, racemization, phosphorylation, acetylation, glycation, age-dependent truncation), the occurrence outside of the eye lens, the heat-shock relation and the chaperone activity of alpha-crystallin.
Adv Enzymol Relat Areas Mol Biol 1994;69:155-201
Expression of the alpha-crystallin/small heat-shock protein/molecular chaperone genes in the lens and other tissues.
Sax CM, Piatigorsky J
Laboratory of Molecular and Developmental Biology, National Eye Institute, National Institutes of Health, Bethesda, MD.
Biotechnol Genet Eng Rev 1994;12:1-38
Crystallins: the over-expression of functional enzymes and stress proteins in the eye lens.
Wistow G, Richardson J, Jaworski C, Graham C, Sharon-Friling R, Segovia L
Section on Molecular Structure and Function, LMDB, National Eye Institute, National Institutes of Health, Bethesda, MD 20892.
Invest Ophthalmol Vis Sci 1993 Jan;34(1):10-22
Proctor Lecture. The function of alpha-crystallin.
Horwitz J
Jules Stein Eye Institute, UCLA School of Medicine 90024-7008.
Prog Neurobiol 1993 Apr;40(4):413-61
Arthropod eye design and the physical limits to spatial resolving power.
Warrant EJ, McIntyre PD
Department of Zoology, University of Lund, Sweden.
Trends Neurosci 1990 Feb;13(2):55-64
From cornea to retinal image in invertebrate eyes.
Nilsson DE
Department of Zoology, University of Lund, Sweden.
The optical information processing that takes place in an eye involves a large variety of very different optical components that are put together to solve a task which, in its basic nature, does not differ much from one species to another. The principal task of an eye is to sort the incoming photons so that they excite specific sensory neurons depending on angle of incidence, wavelength and plane of polarization. Despite the apparent simplicity of the task, the solutions to it are often complex and the variation between species is enormous. The pinhole camera, the Keplerian and Galilean telescopes, the corner reflector, optical fibres, and interference filters, are all names of optical devices invented by man. It now appears that all of these devices, and many more, exist in various combinations in the optics of invertebrate eyes. The similarity between man's and nature's optical engineering has been useful in many ways. For the study of eyes, it has helped to understand biological design principles in unparalleled detail.