Abstract
The diverse crystallins are water-soluble proteins that are responsible for the optical properties of cellular lenses of animal eyes. While all vertebrate lenses contain physiological stress-related α- and βγ-crystallins, some also contain taxon-specific, often enzyme-related crystallins. To date, the α- and βγ-crystallins have been found only in vertebrate lenses. Here we report lenses from an invertebrate, the pontellid copepod Anomalocera ornata, accumulate βγ-crystallin family members as judged by immunocytochemistry, western immunoblotting and microsequencing. Our data provide the first example of βγ-crystallin members in an invertebrate lens, establishing that the use of this protein family as lens crystallins is not confined to vertebrates.
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References
Bhat SP, Nagineni CN (1989) alphaB subunit of lens-specific protein alpha-crystallin is present in other ocular and non-ocular tissues. Biochem Biophys Res Commun 158:319–325
Blundell T, Lindley P, Miller L, Moss D, Slingsby C, Tickle I, Turnell B, Wistow G (1981) The molecular structure and stability of the eye lens: X-ray analysis of gamma-crystallin II. Nature 289:771–777
Carosa E, Kozmik Z, Rall JE, Piatigorsky J (2002) Structure and expression of the scallop omega-crystallin gene. Evidence for convergent evolution of promoter sequences. J Biol Chem 277:656–664
Colley NJ, Trench RK (1983) Selectivity in phagocytosis and persistence of symbiotic algae in the scyphistoma stage of the jellyfish Cassiopeia xamachana. Proc R Soc Lond 219:61–82
Colley NJ, Tokuyasu KT, Singer SJ (1990) The early expression of myofibrillar proteins in round postmitotic myoblasts of embryonic skeletal muscle. J Cell Sci 95:11–22
Colley NJ, Baker EK, Stamnes MA, Zuker CS (1991) The cyclophilin homolog ninaA is required in the secretory pathway. Cell 67:255–263
Cvekl A, Piatigorsky J (1996) Lens development and crystallin gene expression: many roles for Pax-6. Bioessays 18:621–630
D’Alessio G (2002) The evolution of monomeric and oligomeric betagamma-type crystallins. Facts and hypotheses. Eur J Biochem 269:3122–3130
Di Maro A, Pizzo E, Cubellis MV, D’Alessio G (2002) An intron-less betagamma-crystallin-type gene from the sponge Geodia cydonium. Gene 299:79–82
Driessen HP, Herbrink P, Bloemendal H, de Jong WW (1981) Primary structure of the bovine beta-crystallin Bp chain. Internal duplication and homology with gamma-crystallin. Eur J Biochem 121:83–91
Duncan MK, Cvekl A, Kantorow M, Piatigorsky J (2004) Lens crystallins. In: Robinson ML, Lovicu FJ (eds) Development of the ocular lens. Cambridge University Press, New York
Eldred WD, Zucker C, Karten HJ, Yazulla S (1983) Comparison of fixation and penetration enhancement techniques for use in ultrastructural immunocytochemistry. J Histochem Cytochem 31:285–292
Fleminger A (1956) Taxonomic and distributional studies on the epiplanktonic calanoid copepods (Crustacea) of the Gulf of Mexico. Department of Biology, Harvard University, Boston, p 317
Horwitz J (1992) Alpha-crystallin can function as a molecular chaperone. Proc Natl Acad Sci USA 89:10449–10453
Ingolia TD, Craig EA (1982) Four small Drosophila heat shock proteins are related to each other and to mammalian alpha-crystallin. Proc Natl Acad Sci USA 79:2360–2364
International Human Genome Sequencing Consortium (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921
Jaenicke R, Slingsby C (2001) Lens crystallins and their microbial homologs: structure, stability and function. Crit Rev Biochem Mol Biol 36:435–499
de Jong WW, Hendriks W, Mulders JW, Bloemendal H (1989) Evolution of eye lens crystallins: the stress connection. Trends Biochem Sci 14:365–368
de Jong WW, Leunissen JA, Voorter CE (1993) Evolution of the alpha-crystallin/small heat-shock protein family. Mol Biol Evol 10:103–126
de Jong WW, Lubsen NH, Kraft HJ (1994) Molecular evolution of the eye lens. Prog Retin Eye Res 13:391–442
Kozmik Z, Daube M, Frei E, Norman B, Kos L, Dishaw LJ, Noll M, Piatigorsky J (2003) Role of Pax genes in eye evolution. A cnidarian PaxB gene uniting Pax2 and Pax6 functions. Dev Cell 5:773–785
Krasko A, Muller IM, Muller WE (1997) Evolutionary relationships of the metazoan beta gamma-crystallins, including that from the marine sponge Geodia cydonium. Proc R Soc Lond B Biol Sci 264:1077–1084
Land MF (1984) Crustacea. In: Ali MA (ed) Photoreception and vision in invertebrates, vol 74. Plenum Press, New York, pp 401–438
Lubsen NH, Aarts HJ, Schoenmakers JG (1988) The evolution of lenticular proteins: the beta- and gamma-crystallin super gene family. Prog Biophys Mol Biol 51:47–76
Magabo KS, Horwitz J, Piatigorsky J, Kantorow M (2000) Expression of betaB(2)-crystallin mRNA and protein in retina, brain, and testis. Invest Ophthalmol Vis Sci 41:3056–3060
Moens L, Vanfleteren J, Van de Peer Y, Peeters K, Kapp O, Czeluzniak J, Goodman M, Blaxter M, Vinogradov S (1996) Globins in nonvertebrate species: dispersal by horizontal gene transfer and evolution of the structure-function relationships. Mol Biol Evol 13:324–333
Piatigorsky J (2003) Gene sharing, lens crystallins and speculations on an eye/ear evolutionary relationship. Integr Comp Biol 43:492–499
Piatigorsky J, Wistow GJ (1989) Enzyme/crystallins: gene sharing as an evolutionary strategy. Cell 57:197–199
Piatigorsky J, O’Brien WE, Norman BL, Kalumuck K, Wistow G, Borras T, Nickerson JM, Wawrousek EF (1988) Gene sharing by delta-crystallin and argininosuccinate lyase. Proc Natl Acad Sci USA 85:3479–3483
Piatigorsky J, Horwitz J, Kuwabara T, Cutress CE (1989) The cellular eye lens and crystallins of cubomedusan jellyfish. J Comp Physiol A 164:577–587
Piatigorsky J, Horwitz J, Norman BL (1993) J1-crystallins of the cubomedusan jellyfish lens constitute a novel family encoded in at least three intronless genes. J Biol Chem 268:11894–11901
Piatigorsky J, Kozmik Z, Horwitz J, Ding L, Carosa E, Robison WG, Jr., Steinbach PJ, Tamm ER (2000) Omega-crystallin of the scallop lens. A dimeric aldehyde dehydrogenase class 1/2 enzyme-crystallin. J Biol Chem 275:41064–41073
Piatigorsky J, Norman B, Dishaw LJ, Kos L, Horwitz J, Steinbach PJ, Kozmik Z (2001) J3-crystallin of the jellyfish lens: similarity to saposins. Proc Natl Acad Sci USA 98:12362–12367
Pierce SK, Massey SE, Hanten JJ, Curtis NE (2003) Horizontal transfer of functional nuclear genes between multicellular organisms. Biol Bull 204:237–240
Ray ME, Wistow G, Su YA, Meltzer PS, Trent JM (1997) AIM1, a novel non-lens member of the betagamma-crystallin superfamily, is associated with the control of tumorigenicity in human malignant melanoma. Proc Natl Acad Sci USA 94:3229–3234
Sax CM, Piatigorsky J (1994) Expression of the alpha-crystallin/small heat-shock protein/molecular chaperone genes in the lens and other tissues. Adv Enzymol Relat Areas Mol Biol 69:155–201
Smolich BD, Tarkington SK, Saha MS, Grainger RM (1994) Xenopus gamma-crystallin gene expression: evidence that the gamma-crystallin gene family is transcribed in lens and nonlens tissues. Mol Cell Biol 14:1355–1363
Stanhope MJ, Lupas A, Italia MJ, Koretke KK, Volker C, Brown JR (2001) Phylogenetic analyses do not support horizontal gene transfers from bacteria to vertebrates. Nature 411:940–944
Thyagarajan T, Kulkarni AB (2002) Transforming growth factor-beta1 negatively regulates crystallin expression in teeth. J Bone Miner Res 17:1710–1717
Tomarev SI, Piatigorsky J (1996) Lens crystallins of invertebrates. Diversity and recruitment from detoxification enzymes and novel proteins. Eur J Biochem 235:449–465
Tomarev SI, Zinovieva RD (1988) Squid major lens polypeptides are homologous to glutathione S-transferases subunits. Nature 336:86–88
Tomarev SI, Zinovieva RD, Guo K, Piatigorsky J (1993) Squid glutathione S-transferase. Relationships with other glutathione S-transferases and S-crystallins of cephalopods. J Biol Chem 268:4534–4542
Tomarev SI, Duncan MK, Roth HJ, Cvekl A, Piatigorsky J (1994) Convergent evolution of crystallin gene regulation in squid and chicken: the AP-1/ARE connection. J Mol Evol 39:134–143
Treisman JE (2004) How to make an eye. Development 131:3823–3827
Turner JT, Tester PA, Hettler WF (1985) Zooplankton feeding ecology: a laboratory study of predation on fish eggs and larvae by the copepods Anomalocera ornata and Centropages typicus. Mar Biol 90:1–8
Vaissière R (1961) Morphologie et histologie comparées des yeux des crustacés copépodes. Arch Zool Exp Gén 100:1–125
Wistow G (1990) Evolution of a protein superfamily: relationships between vertebrate lens crystallins and microorganism dormancy proteins. J Mol Evol 30:140–145
Wistow GJ, Piatigorsky J (1988) Lens crystallins: the evolution and expression of proteins for a highly specialized tissue. Annu Rev Biochem 57:479–504
Wistow G, Summers L, Blundell T (1985) Myxococcus xanthus spore coat protein S may have a similar structure to vertebrate lens beta gamma-crystallins. Nature 315:771–773
Wistow G, Jaworski C, Rao PV (1995) A non-lens member of the beta gamma crystallin superfamily in a vertebrate, the amphibian Cynops. Exp Eye Res 61:637–639
Xi J, Farjo R, Yoshida S, Kern TS, Swaroop A, Andley UP (2003) A comprehensive analysis of the expression of crystallins in mouse retina. Mol Vis 9:410–419
Zinovieva RD, Tomarev SI, Piatigorsky J (1993) Aldehyde dehydrogenase-derived omega-crystallins of squid and octopus. Specialization for lens expression. J Biol Chem 268:11449–11455
Acknowledgements
We thank Dr. William S. Lane and other members of the Harvard Microchemistry Facility for their assistance in protein identification. Dr. Nicolette H. Lubsen kindly provided the rat anti-γC antibodies. This work was supported in part by the US National Institutes of Health (EY03897 to Joseph Horwitz and EY08768, EY014378 to Nansi J. Colley), Howard Hughes Medical Institute (Nansi J. Colley), Retinal Research Foundation (Nansi J. Colley), and Research to Prevent Blindness (Nansi J. Colley). Jonathan H. Cohen was supported by a grant from the National Oceanic and Atmospheric Administration ECOHAB program (NA17OP2725) to Dr. Richard B. Forward, Jr.
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Cohen, J.H., Piatigorsky, J., Ding, L. et al. Vertebrate-like βγ-crystallins in the ocular lenses of a copepod. J Comp Physiol A 191, 291–298 (2005). https://doi.org/10.1007/s00359-004-0594-4
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DOI: https://doi.org/10.1007/s00359-004-0594-4