Abstract
The dioptric visual system relies on precisely focusing lenses that project light onto a neural retina. While the proteins that constitute the lenses of many vertebrates are relatively well characterized, less is known about the proteins that constitute invertebrate lenses, especially the lens facets in insect compound eyes. To address this question, we used mass spectrophotometry to define the major proteins that comprise the corneal lenses from the adult Drosophila melanogaster compound eye. This led to the identification of four cuticular proteins: two previously identified lens proteins, drosocrystallin and retinin, and two newly identified proteins, Cpr66D and Cpr72Ec. To determine which ommatidial cells contribute each of these proteins to the lens, we conducted in situ hybridization at 50% pupal development, a key age for lens secretion. Our results confirm previous reports that drosocrystallin and retinin are expressed in the two primary corneagenous cells—cone cells and primary pigment cells. Cpr72Ec and Cpr66D, on the other hand, are more highly expressed in higher order interommatidial pigment cells. These data suggest that the complementary expression of cuticular proteins give rise to the center vs periphery of the corneal lens facet, possibly facilitating a refractive gradient that is known to reduce spherical aberration. Moreover, these studies provide a framework for future studies aimed at understanding the cuticular basis of corneal lens function in holometabolous insect eyes.
References
Blanco J, Girard F, Kamachi Y, Kondoh H, Gehring WJ (2005) Functional analysis of the chicken delta 1-crystallin enhancer activity in Drosophila reveals remarkable evolutionary conservation between chicken and fly. Development 132:1895–1905. doi:10.1242/dev.01738
Blest AD, Land MF (1977) Physiological optics of Dinopis subrufus L Koch—fish-lens in a spider. Proc R Soc Ser B-Bio 196:197–222. doi:10.1098/rspb.1977.0037
Bloemendal H, de Jong W, Jaenicke R, Lubsen NH, Slingsby C, Tardieu A (2004) Ageing and vision: structure, stability and function of lens crystallins. Prog Biophys Mol Bio 86:407–485. doi:10.1016/j.pbiomolbio.2003.11.012
Cagan RL, Ready DF (1989) The emergence of order in the Drosophila pupal retina. Dev Biol 136:346–362. doi:10.1016/0012-1606(89)90261-3
Castellano S et al (2005) Diversity and functional plasticity of eukaryotic selenoproteins: identification and characterization of the SelJ family. Proc Natl Acad Sci U S A 102:16188–16193. doi:10.1073/pnas.0505146102
Chandran RR, Iordanou E, Ajja C, Wille M, Jiang L (2014) Gene expression profiling of Drosophila tracheal fusion cells. GEP 15:112–123. doi:10.1016/j.gep.2014.05.004
Charlton-Perkins M, Brown NL, Cook TA (2011) The lens in focus: a comparison of lens development in Drosophila and vertebrates. MGG 286:189–213. doi:10.1007/s00438-011-0643-y
Chiou SH (1984) Physicochemical characterization of a Crystallin from the squid lens and its comparison with vertebrate lens crystallins. J Biol Chem 95:75–82
Cornman RS, Togawa T, Dunn WA, He N, Emmons AC, Willis JH (2008) Annotation and analysis of a large cuticular protein family with the R&R consensus in Anopheles gambiae. BMC Genomics 9:22. doi:10.1186/1471-2164-9-22
Cornman RS, Willis JH (2009) Annotation and analysis of low-complexity protein families of Anopheles gambiae that are associated with cuticle. Insect Mol Biol 18:607–622. doi:10.1111/j.1365-2583.2009.00902.x
de Jong WW, Hendriks W, Mulders JWM, Bloemendal H (1989) Evolution of eye lens crystallins: the stress connection. Trends Biochem Sci 14:365–368. doi:10.1016/0968-0004(89)90009-1
de Jong WW, Leunissen JA, Leenen PJ, Zweers A, Versteeg M (1988) Dogfish alpha-crystallin sequences. Comparison with small heat shock proteins and Schistosoma egg antigen. J Biol Chem 263:5141–5149
Dziedzic K, Heaphy J, Prescott H, Kavaler J (2009) The transcription factor D-Pax2 regulates crystallin production during eye development in Drosophila melanogaster. Dev Dyn 238:2530–2539. doi:10.1002/dvdy.22082
Franceschini N (1972) Pupil and pseudopupil in the compound eye of Drosophila. In., vol Chapter 10. Springer Berlin Heidelberg, Berlin, Heidelberg, pp 75–82. doi:10.1007/978-3-642-65477-0_10
Haussmann IU, White K, Soller M (2008) Erect wing regulates synaptic growth in Drosophila by integration of multiple signaling pathways. Genome Biol 9. doi: ARTN R73. 10.1186/gb-2008-9-4-r73
Horwitz J (1992) Alpha-crystallin can function as a molecular chaperone. Proc Natl Acad Sci U S A 89:10449–10453
Hyde DR, Mecklenburg KL, Pollock JA, Vihtelic TS, Benzer S (1990) Twenty Drosophila visual system cDNA clones: one is a homolog of human arrestin. Proc Natl Acad Sci U S A 87:1008–1012. doi:10.1073/pnas.87.3.1008
Ioannidou ZS, Theodoropoulou MC, Papandreou NC, Willis JH, Hamodrakas SJ (2014) CutProtFam-Pred: detection and classification of putative structural cuticular proteins from sequence alone, based on profile hidden Markov models. Insect Biochem Mol Biol 52:51–59. doi:10.1016/j.ibmb.2014.06.004
Janssens H, Gehring WJ (1999) Isolation and characterization of drosocrystallin, a lens crystallin gene of Drosophila melanogaster. Dev Biol 207:204–214. doi:10.1006/dbio.1998.9170
Jia L-P, Liang A-P (2017) An apposition compound eye adapted for nocturnal vision in the moth midge Clogmia albipunctata (Williston)(Diptera: Psychodidae). J Insect Physiol 98:188–198
Kang L, Aggarwal DD, Rashkovetsky E, Korol AB, Michalak P (2016) Rapid genomic changes in Drosophila melanogaster adapting to desiccation stress in an experimental evolution system. BMC Genomics 17:233. doi:10.1186/s12864-016-2556-y
Karouzou MV, Spyropoulos Y, Iconomidou VA, Cornman RS, Hamodrakas SJ, Willis JH (2007) Drosophila cuticular proteins with the R&R consensus: annotation and classification with a new tool for discriminating RR-1 and RR-2 sequences. Insect Biochem Mol Biol 37:754–760. doi:10.1016/j.ibmb.2007.03.007
Kim E, Choi Y, Lee S, Seo Y, Yoon J, Baek K (2008) Characterization of the Drosophila melanogaster retinin gene encoding a cornea-specific protein. Insect Mol Biol 17:537–543. doi:10.1111/j.1365-2583.2008.00822.x
Komori N, Usukura J, Matsumoto H (1992) Drosocrystallin, a major 52 kDa glycoprotein of the Drosophila melanogaster corneal lens. Purification, biochemical characterization, and subcellular localization. J Cell Sci 102(Pt 2):191–201
Kozmik Z, Swamynathan SK, Ruzickova J, Jonasova K, Paces V, Vlcek C, Piatigorsky J (2008) Cubozoan crystallins: evidence for convergent evolution of pax regulatory sequences. Evol Dev 10:52–61. doi:10.1111/j.1525-142X.2007.00213.x
Land MF, Nilsson D-E (2012) Animal eyes. Oxford University Press. doi:10.1093/acprof:oso/9780199581139.001.0001
Montgomery MK, McFall-Ngai MJ (1992) The muscle-derived lens of a squid bioluminescent organ is biochemically convergent with the ocular lens. Evidence for recruitment of aldehyde dehydrogenase as a predominant structural protein. J Biol Chem 267:20999–21003
Napoletano F et al (2011) Polyglutamine atrophin provokes neurodegeneration in Drosophila by repressing fat. EMBO J 30:945–958. doi:10.1038/emboj.2011.1
Perry MM (1968) Further studies on the development of the eye of Drosophila melanogaster. II. The interommatidial bristles. J Morphol 124:249–261. doi:10.1002/jmor.1051240209
Piatigorsky J (1998) Multifunctional lens crystallins and corneal enzymes: more than meets the eye. Ann N Y Acad Sci 842:7–15. doi:10.1111/j.1749-6632.1998.tb09626.x
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, 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 U S A 98:12362–12367. doi:10.1073/pnas.231310698
Pumphrey RJ (1961) Pumphrey: concerning vision. In: The cell and the organism. Ramsay, JA & Wigglesworth VB (eds). Cambridge University Press pp193–208. doi:10.1007/BF01802978
Rebers JE, Riddiford LM (1988) Structure and expression of a Manduca sexta larval cuticle gene homologous to Drosophila cuticle genes. J Mol Biol 203:411–423
Ren N, Zhu CM, Lee H, Adler PN (2005) Gene expression during Drosophila wing morphogenesis and differentiation. Genetics 171:625–638. doi:10.1534/genetics.105.043687
Robinson RAS, Kellie JF, Kaufman TC, Clemmer DE (2010) Insights into aging through measurements of the Drosophila proteome as a function of temperature. Mech Ageing Dev 131:584–590. doi:10.1016/j.mad.2010.08.004
Sakamoto K, Hisatomi O, Tokunaga F, Eguchi E (1996) Two opsins from the compound eye of the crab Hemigrapsus sanguineus. JEB 199:441–450
Slingsby C, Wistow GJ (2014) Functions of crystallins in and out of lens: roles in elongated and post-mitotic cells. Prog Biophys Mol Bio 115:52–67. doi:10.1016/j.pbiomolbio.2014.02.006
Sweeney AM, Des Marais DL, Ban YEA, Johnsen S (2007) Evolution of graded refractive index in squid lenses. J R Soc Interface 4:685–698. doi:10.1098/rsif.2006.0210
Tomarev SI, Piatigorsky J (1996) Lens crystallins of invertebrates—diversity and recruitment from detoxification enzymes and novel proteins. European J Biol Chem / FEBS 235:449–465
Tomarev SI, Zinovieva RD (1988) Squid major lens polypeptides are homologous to glutathione S-transferases subunits. Nature 336:86–88. doi:10.1038/336086a0
Vannini L, Augustine Dunn W, Reed TW, Willis JH (2014) Changes in transcript abundance for cuticular proteins and other genes three hours after a blood meal in Anopheles gambiae. Insect Biochem Mol Biol 44:33–43. doi:10.1016/j.ibmb.2013.11.002
Vopalensky P, Kozmik Z (2009) Eye evolution: common use and independent recruitment of genetic components. Philos T R Soc B 364:2819–2832. doi:10.1098/rstb.2009.0079
Waddington CH, Perry MM (1960) The ultra-structure of the developing eye of Drosophila. Proc R Soc London, Ser B: Biological Sciences 153:155–178. doi:10.1098/rspb.1960.0094
Xu H et al (2004) A lysosomal tetraspanin associated with retinal degeneration identified via a genome-wide screen. EMBO J 23:811–822. doi:10.1038/sj.emboj.7600112
Xun ZY, Sowell RA, Kaufman TC, Clemmer DE (2008) Quantitative proteomics of a presymptomatic A53T alpha-synuclein Drosophila model of Parkinson disease. MCP 7:1191–1203. doi:10.1074/mcp.M700467-MCP200
Zhou Y, Badgett MJ, Bowen JH, Vannini L, Orlando R, Willis JH (2016) Distribution of cuticular proteins in different structures of adult Anopheles gambiae. Insect Biochem Mol Biol 75:45–57. doi:10.1016/j.ibmb.2016.05.001
Zhu KY, Merzendorfer H, Zhang WQ, Zhang JZ, Muthukrishnan S (2016) Biosynthesis, turnover, and functions of chitin in insects. Annu Rev Entomol 61:177–196. doi:10.1146/annurev-ento-010715-023933
Zinovieva RD, Piatigorsky J, Tomarev SI (1999) O-Crystallin, arginine kinase and ferritin from the octopus lens. BBA – Protein Struct M 1431:512–517. doi:10.1016/S0167-4838(99)00066-7
Acknowledgements
We would like to thank David Terrell and Angela St. John for assistance with the lens protein isolations, the University of Cincinnati Proteomics Core for the mass spectrophotometry analysis, and the Cincinnati Children’s Hospital Medical Center Confocal Imagine Core for microscopy needs. We are grateful to the rest of Buschbeck lab for analysis input. The research was supported by NIH-R01-EY017907 and NIH-R21-EY024405 (to TC) and NSF-IOS1456757 (to EKB, TC).
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Stahl, A.L., Charlton-Perkins, M., Buschbeck, E.K. et al. The cuticular nature of corneal lenses in Drosophila melanogaster . Dev Genes Evol 227, 271–278 (2017). https://doi.org/10.1007/s00427-017-0582-7
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DOI: https://doi.org/10.1007/s00427-017-0582-7