Comparison of Silks from Pseudoips prasinana and Bombyx mori Shows Molecular Convergence in Fibroin Heavy Chains but Large Differences in Other Silk Components

. 2021 Jul 31 ; 22 (15) : . [epub] 20210731

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid34361011

Grantová podpora
331 Interreg : European Territorial Co-operation

Many lepidopteran larvae produce silk feeding shelters and cocoons to protect themselves and the developing pupa. As caterpillars evolved, the quality of the silk, shape of the cocoon, and techniques in forming and leaving the cocoon underwent a number of changes. The silk of Pseudoips prasinana has previously been studied using X-ray analysis and classified in the same category as that of Bombyx mori, suggesting that silks of both species have similar properties despite their considerable phylogenetic distance. In the present study, we examined P. prasinana silk using 'omics' technology, including silk gland RNA sequencing (RNA-seq) and a mass spectrometry-based proteomic analysis of cocoon proteins. We found that although the central repetitive amino acid sequences encoding crystalline domains of fibroin heavy chain molecules are almost identical in both species, the resulting fibers exhibit quite different mechanical properties. Our results suggest that these differences are most probably due to the higher content of fibrohexamerin and fibrohexamerin-like molecules in P. prasinana silk. Furthermore, we show that whilst P. prasinana cocoons are predominantly made of silk similar to that of other Lepidoptera, they also contain a second, minor silk type, which is present only at the escape valve.

Zobrazit více v PubMed

Sehnal F., Zurovec M. Construction of silk fiber core in Lepidoptera. Biomacromolecules. 2004;5:666–674. doi: 10.1021/bm0344046. PubMed DOI

Takei F., Kikuchi Y., Kikuchi A., Mizuno S., Shimura K. Further evidence for importance of the subunit combination of silk fibroin in its efficient secretion from the posterior silk gland cells. J. Cell. Biol. 1987;105:175–180. doi: 10.1083/jcb.105.1.175. PubMed DOI PMC

Tanaka K., Inoue S., Mizuno S. Hydrophobic interaction of P25, containing Asn-linked oligosaccharide chains, with the H-L complex of silk fibroin produced by Bombyx mori. Insect. Biochem. Mol. Biol. 1999;29:269–276. doi: 10.1016/S0965-1748(98)00135-0. PubMed DOI

Lucas F., Rudall K.M. Extracellular Fibrous Proteins: The silks. In: Florkin M., Stotz E.H., editors. Comprehensive Biochemistry. Volume 26. Elsevier; Amsterdam, The Netherlands: 1968. pp. 475–558.

Craig C.L. Evolution of arthropod silks. Annu. Rev. Entomol. 1997;42:231–267. doi: 10.1146/annurev.ento.42.1.231. PubMed DOI

Warwicker J.O. Comparative Studies of Fibroins. II. The Crystal Structures of Various Fibroins. J. Mol. Biol. 1960;2:350–362. doi: 10.1016/S0022-2836(60)80046-0. PubMed DOI

Hwang J.S., Lee J.S., Goo T.W., Yun E.Y., Lee K.S., Kim Y.S., Jin B.R., Lee S.M., Kim K.Y., Kang S.W., et al. Cloning of the fibroin gene from the oak silkworm, Antheraea yamamai and its complete sequence. Biotechnol. Lett. 2001;23:1321–1326. doi: 10.1023/A:1010542011150. DOI

Sezutsu H., Yukuhiro K. Dynamic rearrangement within the Antheraea pernyi silk fibroin gene is associated with four types of repetitive units. J. Mol. Evol. 2000;51:329–338. doi: 10.1007/s002390010095. PubMed DOI

Zurovec M., Sehnal F. Unique molecular architecture of silk fibroin in the waxmoth, Galleria mellonella. J. Biol. Chem. 2002;277:22639–22647. doi: 10.1074/jbc.M201622200. PubMed DOI

Tsubota T., Yoshioka T., Jouraku A., Suzuki T.K., Yonemura N., Yukuhiro K., Kameda T., Sezutsu H. Transcriptomic analysis of the bagworm moth silk gland reveals a number of silk genes conserved within Lepidoptera. Insect Sci. 2020;28:885–900. doi: 10.1111/1744-7917.12846. PubMed DOI

Lussi H.G. Chloephorinae, Noctuidae. In: Bartsch D., editor. Die Schmetterlinge Baden-Wurttembergs. Volume 5. Eugen Ulmer Verlag; Stuttgart, Germany: 1997. pp. 523–527.

Fibiger M., Ronkay L., Steiner A., Zilli A. Noctuidae Europaeae. Volume 11. Entomological Press; Soro, Denmark: 2009. Pantheinae—Bryophilinae; pp. 123–124. Apollo Books.

Davey P.A., Power A.M., Santos R., Bertemes P., Ladurner P., Palmowski P., Clarke J., Flammang P., Lengerer B., Hennebert E., et al. Omics-based molecular analyses of adhesion by aquatic invertebrates. Biol. Rev. 2021;96:1051–1075. doi: 10.1111/brv.12691. PubMed DOI

Rouhova L., Kludkiewicz B., Sehadova H., Sery M., Kucerova L., Konik P., Zurovec M. Silk of the common clothes moth, Tineola bisselliella, a cosmopolitan pest belonging to the basal ditrysian moth line. Insect Biochem. Mol. Biol. 2021;130:103527. doi: 10.1016/j.ibmb.2021.103527. PubMed DOI

Sehnal F., Craig C. Silk Production. In: Resh V.H., Cardé R.T., editors. Encyclopedia of Insects. 2nd ed. Academic Press; Burlington, MA, USA: London, UK: 2009. p. 924.

Peng Z., Yang X., Liu C., Dong Z., Wang F., Wang X., Hu W., Zhang X., Zhao P., Xia Q. Structural and mechanical properties of silk from different instars of Bombyx mori. Biomacromolecules. 2019;20:1203–1216. doi: 10.1021/acs.biomac.8b01576. PubMed DOI

Keten S., Xu Z., Ihle B., Buehler M.J. Nanoconfinement controls stiffness, strength and mechanical toughness of beta-sheet crystals in silk. Nat. Mater. 2010;9:359–367. doi: 10.1038/nmat2704. PubMed DOI

Denny M.W. Silks-Their Properties and Functions. In: Vincent J.F.V., Currey J.D., editors. The Mechanical Properties of Biological Materials. Volume 34. Cambridge University Press; Cambridge, UK: 1980. pp. 247–272. PubMed

Numata A., Sato R., Yazawa K., Hikima T., Masunaga H. Crystal structure and physical properties of Antheraea yamamai silk fibers: Long poly(alanine) sequences are partially in the crystalline region. Polymer. 2015;77:87–94. doi: 10.1016/j.polymer.2015.09.025. DOI

Feng Y., Lin J., Niu L., Wang Y., Cheng Z., Sun X., Li M. High molecular weight silk fibroin prepared by papain degumming. Polymers. 2020;12:2105. doi: 10.3390/polym12092105. PubMed DOI PMC

Inoue S., Tanaka K., Arisaka F., Kimura S., Ohtomo K., Mizuno S. Silk fibroin of Bombyx mori is secreted, assembling a high molecular mass elementary unit consisting of H-chain, L-chain, and P25, with a 6:6:1 molar ratio. J. Biol. Chem. 2000;275:40517–40528. doi: 10.1074/jbc.M006897200. PubMed DOI

Inoue S., Tanaka K., Tanaka H., Ohtomo K., Kanda T., Imamura M., Quan G.X., Kojima K., Yamashita T., Nakajima T., et al. Assembly of the silk fibroin elementary unit in endoplasmic reticulum and a role of L-chain for protection of alpha1,2-mannose residues in N-linked oligosaccharide chains of fibrohexamerin/P25. Eur. J. Biochem. 2004;271:356–366. doi: 10.1046/j.1432-1033.2003.03934.x. PubMed DOI PMC

Long D., Lu W., Zhang Y., Guo Q., Xiang Z., Zhao A. New insight into the mechanism underlying fibroin secretion in silkworm, Bombyx mori. FEBS J. 2015;282:89–101. doi: 10.1111/febs.13105. PubMed DOI

Xia Q., Zhou Z., Lu C., Cheng D., Dai F., Li B., Zhao P., Zha X., Cheng T., Chai C., et al. A draft sequence for the genome of the domesticated silkworm (Bombyx mori) Science. 2004;306:1937–1940. PubMed

Sutherland T.D., Young J.H., Weisman S., Hayashi C.Y., Merritt D.J. Insect silk: One name, many materials. Annu. Rev. Entomol. 2010;55:171–188. doi: 10.1146/annurev-ento-112408-085401. PubMed DOI

Kludkiewicz B., Kucerova L., Konikova T., Strnad H., Hradilova M., Zaloudikova A., Sehadova H., Konik P., Sehnal F., Zurovec M. The expansion of genes encoding soluble silk components in the greater wax moth, Galleria mellonella. Insect Biochem. Mol. Biol. 2019;106:28–38. doi: 10.1016/j.ibmb.2018.11.003. PubMed DOI

Tanaka K., Mizuno S. Homologues of fibroin L-chain and P25 of Bombyx mori are present in Dendrolimus spectabilis and Papilio xuthus but not detectable in Antheraea yamamai. Insect Biochem. Mol. Biol. 2001;31:665–677. doi: 10.1016/S0965-1748(00)00173-9. PubMed DOI

Zurovec M., Yonemura N., Kludkiewicz B., Sehnal F., Kodrik D., Vieira L.C., Kucerova L., Strnad H., Konik P., Sehadova H. Sericin composition in the silk of Antheraea yamamai. Biomacromolecules. 2016;17:1776–1787. doi: 10.1021/acs.biomac.6b00189. PubMed DOI

Afgan E., Baker D., Batut B., van den Beek M., Bouvier D., Cech M., Chilton J., Clements D., Coraor N., Gruning B.A., et al. The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update. Nucleic Acids Res. 2018;46:W537–W544. doi: 10.1093/nar/gky379. PubMed DOI PMC

Hall T.A. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids Symp. Ser. 1999;41:95–98.

Hughes C.S., Foehr S., Garfield D.A., Furlong E.E., Steinmetz L.M., Krijgsveld J. Ultrasensitive proteome analysis using paramagnetic bead technology. Mol. Syst. Biol. 2014;10:757. doi: 10.15252/msb.20145625. PubMed DOI PMC

Rappsilber J., Mann M., Ishihama Y. Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat. Protoc. 2007;2:1896–1906. doi: 10.1038/nprot.2007.261. PubMed DOI

Kludkiewicz B., Takasu Y., Fedic R., Tamura T., Sehnal F., Zurovec M. Structure and expression of the silk adhesive protein Ser2 in Bombyx mori. Insect Biochem. Mol. Biol. 2009;39:938–946. doi: 10.1016/j.ibmb.2009.11.005. PubMed DOI

Cox J., Neuhauser N., Michalski A., Scheltema R.A., Olsen J.V., Mann M. Andromeda: A peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 2011;10:1794–1805. doi: 10.1021/pr101065j. PubMed DOI

Tyanova S., Temu T., Sinitcyn P., Carlson A., Hein M.Y., Geiger T., Mann M., Cox J. The Perseus computational platform for comprehensive analysis of (prote)omics data. Nat. Methods. 2016;13:731–740. doi: 10.1038/nmeth.3901. PubMed DOI

Edgar R.C. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–1797. doi: 10.1093/nar/gkh340. PubMed DOI PMC

Lefort V., Longueville J.E., Gascuel O. SMS: Smart model selection in PhyML. Mol. Biol Evol. 2017;34:2422–2424. doi: 10.1093/molbev/msx149. PubMed DOI PMC

Guindon S., Dufayard J.F., Lefort V., Anisimova M., Hordijk W., Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst. Biol. 2010;59:307–321. doi: 10.1093/sysbio/syq010. PubMed DOI

Kumar S., Stecher G., Li M., Knyaz C., Tamura K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 2018;35:1547–1549. doi: 10.1093/molbev/msy096. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...