Resilin matrix distribution, variability and function in Drosophila.
Cuticle
Drosophila
Extracellular matrix
Flight
Resilin
Journal
BMC biology
ISSN: 1741-7007
Titre abrégé: BMC Biol
Pays: England
ID NLM: 101190720
Informations de publication
Date de publication:
14 12 2020
14 12 2020
Historique:
received:
22
02
2020
accepted:
19
10
2020
entrez:
15
12
2020
pubmed:
16
12
2020
medline:
3
7
2021
Statut:
epublish
Résumé
Elasticity prevents fatigue of tissues that are extensively and repeatedly deformed. Resilin is a resilient and elastic extracellular protein matrix in joints and hinges of insects. For its mechanical properties, Resilin is extensively analysed and applied in biomaterial and biomedical sciences. However, there is only indirect evidence for Resilin distribution and function in an insect. Commonly, the presence of dityrosines that covalently link Resilin protein monomers (Pro-Resilin), which are responsible for its mechanical properties and fluoresce upon UV excitation, has been considered to reflect Resilin incidence. Using a GFP-tagged Resilin version, we directly identify Resilin in pliable regions of the Drosophila body, some of which were not described before. Interestingly, the amounts of dityrosines are not proportional to the amounts of Resilin in different areas of the fly body, arguing that the mechanical properties of Resilin matrices vary according to their need. For a functional analysis of Resilin matrices, applying the RNA interference and Crispr/Cas9 techniques, we generated flies with reduced or eliminated Resilin function, respectively. We find that these flies are flightless but capable of locomotion and viable suggesting that other proteins may partially compensate for Resilin function. Indeed, localizations of the potentially elastic protein Cpr56F and Resilin occasionally coincide. Thus, Resilin-matrices are composite in the way that varying amounts of different elastic proteins and dityrosinylation define material properties. Understanding the biology of Resilin will have an impact on Resilin-based biomaterial and biomedical sciences.
Sections du résumé
BACKGROUND
Elasticity prevents fatigue of tissues that are extensively and repeatedly deformed. Resilin is a resilient and elastic extracellular protein matrix in joints and hinges of insects. For its mechanical properties, Resilin is extensively analysed and applied in biomaterial and biomedical sciences. However, there is only indirect evidence for Resilin distribution and function in an insect. Commonly, the presence of dityrosines that covalently link Resilin protein monomers (Pro-Resilin), which are responsible for its mechanical properties and fluoresce upon UV excitation, has been considered to reflect Resilin incidence.
RESULTS
Using a GFP-tagged Resilin version, we directly identify Resilin in pliable regions of the Drosophila body, some of which were not described before. Interestingly, the amounts of dityrosines are not proportional to the amounts of Resilin in different areas of the fly body, arguing that the mechanical properties of Resilin matrices vary according to their need. For a functional analysis of Resilin matrices, applying the RNA interference and Crispr/Cas9 techniques, we generated flies with reduced or eliminated Resilin function, respectively. We find that these flies are flightless but capable of locomotion and viable suggesting that other proteins may partially compensate for Resilin function. Indeed, localizations of the potentially elastic protein Cpr56F and Resilin occasionally coincide.
CONCLUSIONS
Thus, Resilin-matrices are composite in the way that varying amounts of different elastic proteins and dityrosinylation define material properties. Understanding the biology of Resilin will have an impact on Resilin-based biomaterial and biomedical sciences.
Identifiants
pubmed: 33317537
doi: 10.1186/s12915-020-00902-4
pii: 10.1186/s12915-020-00902-4
pmc: PMC7737337
doi:
Substances chimiques
Insect Proteins
0
resilin
61790-52-1
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
195Subventions
Organisme : Deutsche Forschungsgemeinschaft
ID : MO1714/8
Pays : International
Commentaires et corrections
Type : ErratumIn
Références
Kozel BA, Mecham RP. Elastic fiber ultrastructure and assembly. Matrix Biol. 2019;84:31–40.
pubmed: 31669522
pmcid: 31669522
Mecham RP. Elastin in lung development and disease pathogenesis. Matrix Biol. 2018;73:6–20.
pubmed: 29331337
pmcid: 29331337
Weis-Fogh T. A rubber-like protein in insect cuticle. J Exp Biol. 1960;37(4):889–907.
Weis-Fogh T. Molecular interpretation of the elasticity of Resilin, a rubber-like protein. J Mol Biol. 1961;3:648–67.
Burrows M, Sutton GP. Locusts use a composite of resilin and hard cuticle as an energy store for jumping and kicking. J Exp Biol. 2012;215(Pt 19):3501–12.
Hatch G. Structure and mechanics of the dragonfly pterothorax. Ann Entomol Soc Am. 1966;59:702–14.
Michels J, Gorb SN. Detailed three-dimensional visualization of resilin in the exoskeleton of arthropods using confocal laser scanning microscopy. J Microsc. 2012;245(1):1–16.
Andersen SO. The cross-links in resilin identified as dityrosine and trityrosine. Biochim Biophys Acta. 1964;93:213–5.
Andersen SO. Covalent cross-links in a structural protein, resilin. Acta Physiol Scand Suppl. 1966;263:1–81.
Elvin CM, Carr AG, Huson MG, Maxwell JM, Pearson RD, Vuocolo T, Liyou NE, Wong DC, Merritt DJ, Dixon NE. Synthesis and properties of crosslinked recombinant pro-resilin. Nature. 2005;437(7061):999–1002.
Michels J, Appel E, Gorb SN. Functional diversity of resilin in Arthropoda. Beilstein J Nanotechnol. 2016;7:1241–59.
pubmed: 5082342
pmcid: 5082342
Goodwyn PP, Peressadko A, Schwarz H, Kastner V, Gorb S. Material structure, stiffness, and adhesion: why attachment pads of the grasshopper (Tettigonia viridissima) adhere more strongly than those of the locust (Locusta migratoria) (Insecta : Orthoptera). J Comp Physiol A. 2006;192(11):1233–43.
Ardell DH, Andersen SO. Tentative identification of a resilin gene in Drosophila melanogaster. Insect Biochem Mol Biol. 2001;31(10):965–70.
Andersen SO. Studies on resilin-like gene products in insects. Insect Biochem Mol Biol. 2010;40(7):541–51.
Cornman RS, Togawa T, Dunn WA, He N, Emmons AC, Willis JH. Annotation and analysis of a large cuticular protein family with the R&R consensus in Anopheles gambiae. BMC Genomics. 2008;9:22.
pubmed: 2259329
pmcid: 2259329
Qin G, Hu X, Cebe P, Kaplan DL. Mechanism of resilin elasticity. Nat Commun. 2012;3:1003.
Qin G, Lapidot S, Numata K, Hu X, Meirovitch S, Dekel M, Podoler I, Shoseyov O, Kaplan DL. Expression, cross-linking, and characterization of recombinant chitin binding resilin. Biomacromolecules. 2009;10(12):3227–34.
Qin G, Rivkin A, Lapidot S, Hu X, Preis I, Arinus SB, Dgany O, Shoseyov O, Kaplan DL. Recombinant exon-encoded resilins for elastomeric biomaterials. Biomaterials. 2011;32(35):9231–43.
pubmed: 3190647
pmcid: 3190647
Neff D, Frazier SF, Quimby L, Wang RT, Zill S. Identification of resilin in the leg of cockroach, Periplaneta americana: confirmation by a simple method using pH dependence of UV fluorescence. Arthropod Struct Dev. 2000;29(1):75–83.
Wong DC, Pearson RD, Elvin CM, Merritt DJ. Expression of the rubber-like protein, resilin, in developing and functional insect cuticle determined using a Drosophila anti-rec 1 resilin antibody. Dev Dyn. 2012;241(2):333–9.
Clements AN, Potter SA. The fine structure of the spermathecae and their ducts in the mosquito Aedes aegypti. J Insect Physiol. 1967;13(12):1825–36.
Hepburn HR. Proboscis extension and recoil in Lepidoptera. J Insect Physiol. 1971;17:637–56.
Rice MJ. Function of resilin in tsetse fly feeding mechanism. Nature. 1970;228(5278):1337–8.
Andersen SO. Characterization of a new type of cross-linkage in resilin, a rubber-like protein. Biochim Biophys Acta. 1963;69:249–62.
Andersen SO. Regional differences in degree of resilin cross-linking in the desert locust, Schistocerca gregaria. Insect Biochem Mol Biol. 2004;34(5):459–66.
Zuber R, Shaik KS, Meyer F, Ho HN, Speidel A, Gehring N, Bartoszewski S, Schwarz H, Moussian B. The putative C-type lectin Schlaff ensures epidermal barrier compactness in Drosophila. Sci Rep. 2019;9(1):5374.
pubmed: 6440989
pmcid: 6440989
Wang Y, Carballo RG, Moussian B. Double cuticle barrier in two global pests, the whitefly Trialeurodes vaporariorum and the bedbug Cimex lectularius. J Exp Biol. 2017;220(Pt 8):1396–9.
Wang Y, Yu Z, Zhang J, Moussian B. Regionalization of surface lipids in insects. Proc Biol Sci. 2016;283(1830):1-8.
Ja WW, Carvalho GB, Mak EM, de la Rosa NN, Fang AY, Liong JC, Brummel T, Benzer S. Prandiology of Drosophila and the CAFE assay. Proc Natl Acad Sci U S A. 2007;104(20):8253–6.
pubmed: 1899109
pmcid: 1899109
Karouzou MV, Spyropoulos Y, Iconomidou VA, Cornman RS, Hamodrakas SJ, Willis JH. 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. 2007;37(8):754–60.
pubmed: 17628275
pmcid: 17628275
Lehmann FO, Gorb S, Nasir N, Schutzner P. Elastic deformation and energy loss of flapping fly wings. J Exp Biol. 2011;214(Pt 17):2949–61.
pubmed: 21832138
pmcid: 21832138
Consortium m, Roy S, Ernst J, Kharchenko PV, Kheradpour P, Negre N, Eaton ML, Landolin JM, Bristow CA, Ma L, et al. Identification of functional elements and regulatory circuits by Drosophila modENCODE. Science. 2010;330(6012):1787–97.
Burrows M, Borycz JA, Shaw SR, Elvin CM, Meinertzhagen IA. Antibody labelling of resilin in energy stores for jumping in plant sucking insects. Plos One. 2011;6(12):e28456.
pubmed: 22163306
pmcid: 22163306
Deora T, Gundiah N, Sane SP. Mechanics of the thorax in flies. J Exp Biol. 2017;220(Pt 8):1382–95.
pubmed: 28424311
pmcid: 28424311
Appel E, Gorb SN. Resilin-bearing wing vein joints in the dragonfly Epiophlebia superstes. Bioinspir Biomim. 2011;6(4):046006.
pubmed: 21993162
pmcid: 21993162
Ma Y, Ning JG, Ren HL, Zhang PF, Zhao HY. The function of resilin in honeybee wings. J Exp Biol. 2015;218(Pt 13):2136–42.
Mamat N, Yazawa K, Numata K, Norma-Rashid Y. Morphological and mechanical properties of flexible resilin joints on damselfly wings (Rhinocypha spp.). Plos One. 2018;13(3):e0193147.
Burrows M, Shaw SR, Sutton GP. Resilin and chitinous cuticle form a composite structure for energy storage in jumping by froghopper insects. BMC Biol. 2008;6:41.
pubmed: 18826572
pmcid: 18826572
Wang Y, Berger J, Moussian B. Trynity models a tube valve in the Drosophila larval airway system. Dev Biol. 2018;437(2):75–83.
pubmed: 29518377
pmcid: 29518377
Manzo A, Silies M, Gohl DM, Scott K. Motor neurons controlling fluid ingestion in Drosophila. Proc Natl Acad Sci U S A. 2012;109(16):6307–12.
pubmed: 3341050
pmcid: 3341050
Kristensen BI. Time course of incorporation of tyrosine into rubber-like cuticle of locusts. J Insect Physiol. 1968;14:1135–40.
Neville AC. Growth and deposition od resilin and chitin in locust rubber-like cuticle. J Insect Physiol. 1963;9:265–78.
Aghaei-Ghareh-Bolagh B, Mithieux SM, Weiss AS. Elastic proteins and elastomeric protein alloys. Curr Opin Biotechnol. 2016;39:56–60.
pubmed: 4899202
pmcid: 4899202
Schrader CU, Heinz A, Majovsky P, Karaman Mayack B, Brinckmann J, Sippl W, Schmelzer CEH. Elastin is heterogeneously cross-linked. J Biol Chem. 2018;293(39):15107–19.
pubmed: 6166741
pmcid: 6166741
Hirano E, Knutsen RH, Sugitani H, Ciliberto CH, Mecham RP. Functional rescue of elastin insufficiency in mice by the human elastin gene: implications for mouse models of human disease. Circ Res. 2007;101(5):523–31.
Benoit JB, Adelman ZN, Reinhardt K, Dolan A, Poelchau M, Jennings EC, Szuter EM, Hagan RW, Gujar H, Shukla JN, et al. Unique features of a global human ectoparasite identified through sequencing of the bed bug genome. Nat Commun. 2016;7:10165.
pubmed: 4740739
pmcid: 4740739
Desai MS, Lee SW. Protein-based functional nanomaterial design for bioengineering applications. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2015;7(1):69–97.
Mintchev S, Shintake J, Floreano D. Bioinspired dual-stiffness origami. Sci Robot. 2018;3(20):1–7.
Renner JN, Cherry KM, Su RS, Liu JC. Characterization of resilin-based materials for tissue engineering applications. Biomacromolecules. 2012;13(11):3678–85.
Zuber R, Norum M, Wang Y, Oehl K, Gehring N, Accardi D, Bartozsewski S, Berger J, Flotenmeyer M, Moussian B. The ABC transporter Snu and the extracellular protein Snsl cooperate in the formation of the lipid-based inward and outward barrier in the skin of Drosophila. Eur J Cell Biol. 2018;97(2):90–101.
Siwanowicz I, Burrows M. Three dimensional reconstruction of energy stores for jumping in planthoppers and froghoppers from confocal laser scanning microscopy. eLife. 2017;6:1–25.
Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, et al. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem. 2009;55(4):611–22.
pubmed: 19246619
pmcid: 19246619