title: Lens crystallins of invertebrates--diversity and recruitment from detoxification enzymes and novel proteins.
abstract: 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.
authors.affiliation: Laboratory of Molecular and Developmental Biology, National Eye Institute, National Institutes of Health, Bethesda, MD 20892-2730, USA.
authors.forename: S I
authors.initials: SI
authors.lastname: Tomarev
authors.forename: J
authors.initials: J
authors.lastname: Piatigorsky
mesh_terms: D000595:Amino Acid Sequence; D000818:Animals; D003459:Crystallins / Q000235:genetics* / Q000378:metabolism*; D005786:Gene Expression Regulation; D005982:Glutathione Transferase / Q000378:metabolism*; D007448:Invertebrates; D007908:Lens, Crystalline / Q000201:enzymology / Q000378:metabolism*; D008969:Molecular Sequence Data
chemical_list: D003459:Crystallins; D005982:Glutathione Transferase