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Vertebrate-like βγ-crystallins in the ocular lenses of a copepod

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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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Colley NJ, Baker EK, Stamnes MA, Zuker CS (1991) The cyclophilin homolog ninaA is required in the secretory pathway. Cell 67:255–263

    Article  Google Scholar 

  • Cvekl A, Piatigorsky J (1996) Lens development and crystallin gene expression: many roles for Pax-6. Bioessays 18:621–630

    Google Scholar 

  • D’Alessio G (2002) The evolution of monomeric and oligomeric betagamma-type crystallins. Facts and hypotheses. Eur J Biochem 269:3122–3130

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • International Human Genome Sequencing Consortium (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921

    Google Scholar 

  • Jaenicke R, Slingsby C (2001) Lens crystallins and their microbial homologs: structure, stability and function. Crit Rev Biochem Mol Biol 36:435–499

    Google Scholar 

  • de Jong WW, Hendriks W, Mulders JW, Bloemendal H (1989) Evolution of eye lens crystallins: the stress connection. Trends Biochem Sci 14:365–368

    Article  Google Scholar 

  • de Jong WW, Leunissen JA, Voorter CE (1993) Evolution of the alpha-crystallin/small heat-shock protein family. Mol Biol Evol 10:103–126

    PubMed  Google Scholar 

  • de Jong WW, Lubsen NH, Kraft HJ (1994) Molecular evolution of the eye lens. Prog Retin Eye Res 13:391–442

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Piatigorsky J (2003) Gene sharing, lens crystallins and speculations on an eye/ear evolutionary relationship. Integr Comp Biol 43:492–499

    Google Scholar 

  • Piatigorsky J, Wistow GJ (1989) Enzyme/crystallins: gene sharing as an evolutionary strategy. Cell 57:197–199

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Pierce SK, Massey SE, Hanten JJ, Curtis NE (2003) Horizontal transfer of functional nuclear genes between multicellular organisms. Biol Bull 204:237–240

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Thyagarajan T, Kulkarni AB (2002) Transforming growth factor-beta1 negatively regulates crystallin expression in teeth. J Bone Miner Res 17:1710–1717

    Google Scholar 

  • Tomarev SI, Piatigorsky J (1996) Lens crystallins of invertebrates. Diversity and recruitment from detoxification enzymes and novel proteins. Eur J Biochem 235:449–465

    Article  Google Scholar 

  • Tomarev SI, Zinovieva RD (1988) Squid major lens polypeptides are homologous to glutathione S-transferases subunits. Nature 336:86–88

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Treisman JE (2004) How to make an eye. Development 131:3823–3827

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Vaissière R (1961) Morphologie et histologie comparées des yeux des crustacés copépodes. Arch Zool Exp Gén 100:1–125

    Google Scholar 

  • Wistow G (1990) Evolution of a protein superfamily: relationships between vertebrate lens crystallins and microorganism dormancy proteins. J Mol Evol 30:140–145

    Google Scholar 

  • Wistow GJ, Piatigorsky J (1988) Lens crystallins: the evolution and expression of proteins for a highly specialized tissue. Annu Rev Biochem 57:479–504

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

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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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Correspondence to Jonathan H. Cohen.

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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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