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The cellular eye lens and crystallins of cubomedusan jellyfish

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Summary

The ultrastructure and major soluble proteins of the transparent eye lens of two cubomedusan jellyfish,Tripedalia cystophora andCarybdea marsupialis, have been examined. Each species has two complex eyes (one large and one small) on four sensory structures called rhopalia. The lenses consist of closely spaced cells with few organelles. The lens is situated next to the retina, with only an acellular layer separating it from the photoreceptors. SDS-PAGE showed that the large lens ofC. marsupialis has only two crystallin polypeptide bands (with molecular masses of approximately 20000 and 35000 daltons), while that ofT. cystophora has three bands (two with a molecular mass near 20000 daltons and one with a molecular mass near 35000 daltons). Interestingly, the small lens ofT. cystophora appears to be markedly deficient in or lack the lower molecular weight proteins. The crystallins behaved as monomeric proteins by FPLC and showed no immunological reaction with antisera of the major squid crystallin, chickenδ-crystallin or mouseγ-crystallin in western immunoblots. Very weak reactions were found with antimouseα- andβ-crystallin sera. The 35000 dalton crystallin ofT. cystophora was purified and called J1-crystallin. It contained relatively high leucine (13%) and tyrosine (9%) and low methionine (2%). Several tryptic peptides were sequenced. Weak sequence similarities were found withα- andβ-crystallins, which may account for some of the apparent weak immunological crossreactivity with these vertebrate crystallins. A polyclonal antiserum made in rabbits from a synthetic peptide of J1-crystallin reacted strongly with J1-crystallin ofT. cystophora andC. marsupialis in immunoblots; by contrast, no reaction was obtained with the lower molecular weight crystallins from these jellyfish, with the squid crystallin, or with any crystallins from the frog or human lens. Thus, despite the structural similarities between the cubomedusan, squid and vertebrate lenses, their crystallins appear very different.

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Abbreviations

SDS-PAGE :

sodium dodecylsulfate-polyacrylamide gel electrophoresis

bp :

base pairs

PTC :

phenylisothiocyanate

FPLC :

fast phase liquid chromatography

NBRF :

National Biomedical Research Foundation

References

  • Ali MA (ed) (1982) Photoreception and vision in invertebrates. Nato ASI Ser A, vol 74. Plenum Press, New York, pp 1–858

    Google Scholar 

  • Anderson PAV, Mackie GO (1977) Electrically coupled, photosensitivie neurons control swimming in a jellyfish. Science 197:186–188

    Google Scholar 

  • Arkett SA, Spencer AN (1986) Neuronal mechanisms of a hydromedusan shadow reflex. I. Identified reflex components and sequence of events. J Comp Physiol A 159:201–213

    Google Scholar 

  • Arneson AC, Cutress CE (1976) Life history ofCarybdea alata Reymond, 1830 (Cubomedusae). In: Mackie GO (ed) Coelenterate ecology of behavior. Plenum Press, New York, pp 227–236

    Google Scholar 

  • Berger EW (1898) The histological structure of the eyes of cubomedusae. J Comp Neurol 8:223–230

    Google Scholar 

  • Berger EW (1900) Physiology and histology of the Cubomedusae, including Dr. F.S. Conant's notes on the physiology. Mem Biol Lab Johns Hopkins Univ 4:1–84

    Google Scholar 

  • Bloemendal H (1982) Lens proteins. CRC Critical Rev Biochem 12:1–38

    Google Scholar 

  • Burr AH (1984) Evolution of eyes and photoreceptor organelles in the lower phyla. In: Ali MA (ed) Photoreception and vision in invertebrates. Plenum, New York, pp 131–178

    Google Scholar 

  • Carper D, Nishimura C, Shinohara T, Dietzchold B, Wistow G, Craft C, Kador P, Kinoshita JH (1987) Aldose reductase andρ-crystallin belong to the same protein superfamily as aldehyde reductase. FEBS Lett 220:209–213

    Google Scholar 

  • Chapman DM (1985) X-ray microanalysis of selected coelenterate statoliths. J Mar Biol Ass UK 65:617–627

    Google Scholar 

  • Chiou S-H (1984) Physiochemical characterization of a crystallin from the squid lens and its comparison with vertebrate lens crystallins. J Biochem 95:75–82

    Google Scholar 

  • Chiou S-H (1986) Phylogenetic comparison of lens crystallins from the vertebrate and invertebrate-convergent or divergent evolution? FEBS Lett 201:69–73

    Google Scholar 

  • Chiou S-H, Chang T, Changa W-C, Kuo J, Lo T-B (1986) Characterization of lens crystallins and their mRNA from the carp lenses. Biochim Biophys Acta 871:324–328

    Google Scholar 

  • Clayton RM (1974) Comparative aspects of lens proteins. In: Davson H, Graham LT (eds) The eye, vol. 5. Academic Press, San Francisco, pp 399–494

    Google Scholar 

  • Clayton RM, Jeanny J-C, Bower DJ, Errington LH (1986) The presence of extralenticular crystallins and its relationship with transdifferentiation to lens. Curr Topics Develop Biol 20:137–151

    Google Scholar 

  • Conant FS (1897) Notes on the Cubomedusae. Johns Hopkins Univ Circ No 132:8–10

    Google Scholar 

  • Conant FS (1898) The Cubomedusae. Mem Biol Lab Johns Hopkins Univ 4(1):1–61

    Google Scholar 

  • Cronin TW (1986) Photoreception in marine invertebrates. Am Zool 26:403–415

    Google Scholar 

  • Cutress CE, Studebaker JP (1973) Development of the Cubomedusa,Carybdea marsupialis. Proc AIMLC 9:25

    Google Scholar 

  • de Jong WW (1981) Evolution of lens and crystallins. In: Bloemendal H (ed) Molecular and cellular biology of the eye lens. Wiley, New York, pp 221–278

    Google Scholar 

  • de Jong WW, Stapel SO, Zweers A (1981) A comparison of avian and reptilianδ-crystallin. Comp Biochem Physiol 69B:593–598

    Google Scholar 

  • Eakin RM (1972) Structure of invertebrate photoreceptors. In: Dartnall HJA (ed) Photochemistry of vision (Handbook of sensory physiology, vol. VII/1) Springer, Berlin Heidelberg New York, pp 625–684

    Google Scholar 

  • Eakin RM (1979) Evolutionary significance of photoreceptors: in retrospect. Am Zool 19:647–653

    Google Scholar 

  • Eakin RM, Westfall JA (1962) Fine structure of photoreceptors in the hydromedusan,Polyorchis penicillatus. Proc Natl Acad Sci USA 48:826–833

    Google Scholar 

  • Ebert RF (1986) Amino acid analysis by HPLC: optimized conditions for chromatography of phenylthiocarbamyl derivatives. Anal Biochem 154:431–435

    Google Scholar 

  • Field KG, Olsen GJ, Lane DJ, Giovannoni SJ, Ghiselin MT, Raff EC, Pace NR, Raff RA (1988) Molecular phylogeny of the animal kingdom. Science 239:748–753

    Google Scholar 

  • Gause GG Jr, Tomarev SI, Zonovieva RD, Arutyunyan KG, Dolgilevich SM (1986) Crystallin gene sequences of the frogRana temporaria. In: Duncan G (ed) The lens: transparency and cataract. Proceedings of the Eurage/BBS Symposium, pp 171–179

  • Huang Q-L, Russell P, Stone SH, Zigler JS, Jr (1987) Zetacrystallin, a novel lens protein from the guinea pig. Curr Eye Res 6:725–732

    Google Scholar 

  • Hyman LH (1940) The invertebrates: Protozoa through ctenophora, vol 1. McGraw Hill, New York, pp 1–726

    Google Scholar 

  • Ingolia TD, Craig EA (1982) Four smallDrosophila heat shock proteins are related to each other and to mammalianα-crystallin. Proc Natl Acad Sci USA 79:2360–2364

    Google Scholar 

  • Kent S, Clark-Lewis I (1985) Modern methods for the chemical synthesis of biologically active peptides. In: Alitalo K, Partanen P, Vaheri A (eds) Synthetic peptides in biology and medicine. Elsevier, Amsterdam, pp 29–57

    Google Scholar 

  • Kuwabara T (1968) Microtubules in the lens. Arch Ophthalmol 79:189–195

    Google Scholar 

  • Kuwabara T (1975) The maturation of the lens cell: a morphologic study. Exp Eye Res 20:427–443

    Google Scholar 

  • Laska VG, Hundgen M (1982) Morphologie und Ultrastruktur der Lichtsinnesorgane vonTripedalia cystophora Conant (Cnidaria, Cubozoa). Zool Jb Anat 108:107–123

    Google Scholar 

  • Manski W, Halbert SP (1965) Immunochemical investigation on the phylogeny of lens proteins. In: Peeters H (ed) Protides of the biological fluids. Proceedings of the Twelfth Colloquium, Bruges, 1964. Elsevier, Amsterdam, pp 117–134

    Google Scholar 

  • McDermott MJ, Gawinowicz-Kolks MA, Chiesa R, Spector A (1988) The disulfide content of calfγ-crystallin. Arch Biochem Biphys 262:609–619

    Google Scholar 

  • Milstone LM, Piatigorsky J (1975) Rates of protein synthesis in explanted embryonic chick lens epithelia: differential stimulation ofδ-crystallin synthesis. Dev Biol 43:91–100

    Google Scholar 

  • Nene V, Dunne DW, Johnson KS, Taylor DW, Cordingley JS (1986) Sequence and expression of a major egg antigen fromSchistosoma mansoni. Mol Biochem Parasitol 21:179–189

    Google Scholar 

  • Oakley BR, Kirsch RD, Morris NR (1980) A simplified ultrasensitive silver stain for detecting proteins in polyacrylamide gels. Anal Biochem 105:361–363

    Google Scholar 

  • Ostrer H, Beebe DC, Piatigorsky J (1981)β-Crystallin mRNAs: Differential distribution in the developing chicken lens. Dev Biol 86:403–408

    Google Scholar 

  • Packard A (1972) Cephalopods and fish: the limits of convergence. Biol Rev 47:241–307

    Google Scholar 

  • Pearse JS, Pearse VB (1978) Vision in cubomedusan jellyfishes. Science 199:458

    Google Scholar 

  • Peterson CA, Piatigorsky J (1986) Preferential conservation of the globular domains of theβA3/A1-crystallin polypeptide of the chicken eye lens. Gene 45:139–147

    Google Scholar 

  • Piatigorsky J (1984) Delta crystallins and their nucleic acids. Mol Cell Biochem 59:33–56

    Google Scholar 

  • Piatigorsky J, Webster H de F, Craig SP (1972) Protein systhesis and ultrastructure during the formation of embryonic chick lens fibers in vivo and in vitro. Dev Biol 27:176–189

    Google Scholar 

  • Piatigorsky J, O'Brien WE, Norman BL, Kalumuck K, Wistow GJ, Borras T, Nickerson JM, Wawrousek EF (1988) Gene sharing byδ-crystallin and argininosuccinate lyase. Proc Natl Acad Sci USA 85:3479–3483

    Google Scholar 

  • Robson EA (1985) Speculations on coelenterates. In: Morris SC, George JD, Gibson R, Platt HM (eds) The systematics association, Special Vol 28. The origins and relationships of lower invertebrates. Clarendon Press, Oxford, pp 60–77

    Google Scholar 

  • Salvini-Plawen L von, Mayr E (1977) On the evolution of photoreceptors and eyes. Evol Biol 10:207–263

    Google Scholar 

  • Satterlie RA (1979) Central control of swimming in the cubomedusan jellyfishCarybdea rastonii. J Comp Physiol 133:357–367

    Google Scholar 

  • Siezen RJ, Shaw DC (1982) Physicochemical characterization of lens proteins of the squidNototodarus gouldi and comparison with vertebrate crystallins. Biochim Biophys Acta 704:304–320

    Google Scholar 

  • Singla CL (1974) Ocelli of hydromedusae. Cell Tissue Res 149:413–429

    Google Scholar 

  • Singla CL, Weber C (1982) Fine structure studies of the ocelli ofPolyorchis penicillatus (Hydrozoa, Anthomedusae) and their connection with the nerve ring. Zoomorphology 99:117–129

    Google Scholar 

  • Singla CL, Weber C (1982) Fine structure of the ocellus ofSarsia tubulosa (Hydrozoa, Anthomedusae). Zoomorphology 100:11–22

    Google Scholar 

  • Sivak JG (1976) Optics of the eye of the ‘four-eyed fish’ (Anableps anableps). Vision Res 16:531–534

    Google Scholar 

  • Spencer AN, Arkett SA (1984) Radial symmetry and the organization of central neurones in a hydrozoan jellyfish. J Exp Biol 110:69–90

    Google Scholar 

  • Stapel SO, de Jong WW (1983) Lamprey 48-kDa lens protein represents a novel class of crystallins. FEBS Lett 162:305–309

    Google Scholar 

  • Stapel SO, Zweers A, Dodemont HJ, Kan JH, de Jong WW (1985)ε-Crystallin, a novel avian and reptilian eye lens protein. Eur J Biochem 147:129–136

    Google Scholar 

  • Takemoto L, Hansen J, Horwitz J (1985) Antisera to synthetic peptides of lens MIP26K (major intrinsic polypeptide): characterization and use as site-specific probes of membrane changes in the aging human lens. Exp Eye Res 41:415–422

    Google Scholar 

  • Tomarev SI, Zinovieva RD, Dolgilevich SM, Luchin SV, Krayev AS, Skryabin KG, Gause GG Jr (1984) A novel type of crystallin in the frog eye lens. 35-kDa polypeptide is not homologous to any of the major classes of lens crystallins. FEBS Lett 171:297–302

    Google Scholar 

  • Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76:4350–4354

    Google Scholar 

  • Watanabe K, Fujii Y, Nakayama K, Ohkubo H, Kuramitsu S, Kagamiyama H, Nakanishi S, Hayaishi O (1988) Structural similarity of bovine lung prostaglandin F synthase to lensε-crystallin of the European common frog. Proc Natl Acad Sci USA 85:11–15

    Google Scholar 

  • Weber C (1981) Lens of the hydromedusanCladonema studied by SDS gel electrophoresis and immunofluorescent technique. J Exp Zool 217:15–21

    Google Scholar 

  • Weber C (1981) Structure, histochemistry, ontogenetic development, and regeneration of the ocellus ofCladonema radiatum Dujardin (Cnidaria, Hydrozoa, Anthomedusae). J Morphol 167:313–331

    Google Scholar 

  • Weber C (1982a) Electrical activities of a type of electroretinogram recorded from the ocellus of a jellyfish,Polyorchis penicillatus (Hydromedusae). J Exp Zool 223:231–243

    Google Scholar 

  • Weber C (1982b) Electrical activity in response to light of the ocellus of the hydromedusan,Sarsia tubulosa. Biol Bull 162:413–422

    Google Scholar 

  • Werner B, Chapman DM, Cutress CE (1976) Muscular and nervous systems of the cubopolyp (Cnidaria). Experientia 32:1047–1048

    Google Scholar 

  • Werner B, Cutress CE, Studebaker JP (1971) Life cycle ofTripedalia cystophora Conant (Cubomedusae). Nature 232:582–583

    Google Scholar 

  • Willekens B, Vrensen G, Jacob T, Duncan G (1984) The ultrastructure of the lens of the cephalopodSepiola: a scanning electron microscopic study. Tissue Cell 16:941–950

    Google Scholar 

  • Williams LA, Ding L, Horwitz J, Piatigorsky J (1985)τ-Crystallin from the turtle lens: purification and partial characterization. Exp Eye Res 40:741–749

    Google Scholar 

  • Williams LA, Piatigorsky J, Horwitz J (1982) Structural features ofδ-crystallin of turtle lens. Biochim Biophys Acta 708:49–56

    Google Scholar 

  • Wistow GJ, Mulders JWM, de Jong WW (1987) The enzyme lactate dehydrogenase as a structural protein in avian and crocodilian lenses. Nature 326:622–624

    Google Scholar 

  • Wistow G, Piatigorsky J (1987) Recruitment of enzymes and lens structural proteins. Science 236:1554–1556

    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

    Google Scholar 

  • Wistow G, Slingsby C, Blundell T, Driessen H, de Jong W, Bloemendal H (1981) Eye-lens proteins: the three-dimensional structure of β-crystallin predicted from monomericγ-crystallin. FEBS Lett 133:9–16

    Google Scholar 

  • Wistow G, Summers L, Blundell T (1985)Myxococcus xanthus spore coat protein S may have a similar structure to vertebrate lensβγ-crystallins. Nature 315:771–773

    Google Scholar 

  • Wistow G, Turnell B, Summers L, Slingsby C, Moss D, Miller L, Lindley P, Blundell T (1983) X-ray analysis of the eye lens proteinγ-II crystallin at 1.9 Å resolution. J Mol Biol 170:175–202

    Google Scholar 

  • Yamasu T, Yoshida M (1976) Fine structure of complex ocelli of a cubomedusan,Tamoya bursaria Haeckel. Cell Tissue Res 170:325–339

    Google Scholar 

  • Yeh L-SL, Elzanowski A, Hunt LT, Barker WC (1988) Homology of delta crystallin and argininosuccinate lyase. Comp Biochem Physiol 89B: 433–437

    Google Scholar 

  • Zigler JS Jr, Sidbury JB Jr (1976) A comparative study of theβ-crystallins of four sub-mammalian species. Comp Biochem Physiol 55B: 19–24

    Google Scholar 

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Piatigorsky, J., Horwitz, J., Kuwabara, T. et al. The cellular eye lens and crystallins of cubomedusan jellyfish. J. Comp. Physiol. 164, 577–587 (1989). https://doi.org/10.1007/BF00614500

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