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Biofouling
The Journal of Bioadhesion and Biofilm Research
Volume 32, 2016 - Issue 9
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Articles

Profiling of adhesive-related genes in the freshwater cnidarian Hydra magnipapillata by transcriptomics and proteomics

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Pages 1115-1129 | Received 09 Jun 2016, Accepted 01 Sep 2016, Published online: 23 Sep 2016

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol. 215:403–410. doi:10.1016/S0022-2836(05)80360-2
  • Amano H, Koizumi O, Kobayakawa Y. 1997. Morphogenesis of the atrichous isorhiza, a type of nematocyst, in Hydra observed with a monoclonal antibody. Dev Genes Evol. 207:413–416. doi:10.1007/s004270050131
  • Arbore R, Sekii K, Beisel C, Ladurner P, Berezikov E, Schärer L. 2015. Positional RNA-Seq identifies candidate genes for phenotypic engineering of sexual traits. Front Zool. 12.
  • Ashton NN, Roe DR, Weiss RB, Cheatham TE, Stewart RJ. 2013. Self-tensioning aquatic caddisfly silk: Ca2+-dependent structure, strength, and load cycle hysteresis. Biomacromolecules. 14:3668–3681.10.1021/bm401036z
  • Bacchetti De Gregoris T, Borra M, Biffali E, Bekel T, Burgess JG, Kirby RR, Clare AS. 2009. Construction of an adult barnacle (Balanus amphitrite) cDNA library and selection of reference genes for quantitative RT-PCR studies. BMC Mol Biol. 10:62. doi:10.1186/1471-2199-10-62
  • Balasubramanian PG, Beckmann A, Warnken U, Schnolzer M, Schuler A, Bornberg-Bauer E, Holstein TW, Ozbek S. 2012. Proteome of Hydra nematocyst. J Biol Chem. 287:9672–9681. doi:10.1074/jbc.M111.328203
  • Blankenberg D, Taylor J, Schenck I, He J, Zhang Y, Ghent M, Veeraraghavan N, Albert I, Miller W, Makova KD, et al. 2007. A framework for collaborative analysis of ENCODE data: making large-scale analyses biologist-friendly. Genome Res. 17:960–964. doi:10.1101/gr.5578007
  • Bridge DM, Stover NA, Steele RE. 2000. Expression of a novel receptor tyrosine kinase gene and a paired-like homeobox gene provides evidence of differences in patterning at the oral and aboral ends of Hydra. Dev Biol. 220:253–262. doi:10.1006/dbio.2000.9653
  • Chaet AB. 1965. Invertebrate adhering surfaces: secretions of the starfish, Asterias forbesi, and the coelenterate, Hydra pirardi. Ann NY Acad Sci. 118:921–929.
  • Chapman JA, Kirkness EF, Simakov O, Hampson SE, Mitros T, Weinmaier T, Rattei T, Balasubramanian PG, Borman J, Busam D, et al. 2010. The dynamic genome of Hydra. Nature. 464:592–596. doi:10.1038/nature08830
  • Choresh O, Bayarmagnai B, Lewis RV. 2009. Spider web glue: two proteins expressed from opposite strands of the same DNA sequence. Biomacromolecules. 10:2852–2856. doi:10.1021/bm900681w
  • Davis LE. 1973. Histological and ultrastructural studies of the basal disk of Hydra. Z Für Zellforsch Mikrosk Anat. 139:1–27. doi:10.1007/BF00307458
  • Dübel S, Hoffmeister SA, Schaller HC. 1987. Differentiation pathways of ectodermal epithelial cells in Hydra. Differ Res Biol Divers. 35:181–189. doi:10.1111/j.1432-0436.1987.tb00167.x
  • Eddy SR. 2011. Accelerated profile HMM searches. PLoS Comput Biol. 7:e1002195. doi:10.1371/journal.pcbi.1002195
  • Eisenberg D, Gill HS, Pfluegl GM, Rotstein SH. 2000. Structure–function relationships of glutamine synthetases. Biochim Biophys Acta. 1477:122–145. doi:10.1016/S0167-4838(99)00270-8
  • Endrizzi BJ, Stewart RJ. 2009. Glueomics: an expression survey of the adhesive gland of the sandcastle worm. J Adhes. 85:546–559. doi:10.1080/00218460902996457
  • Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, Potter SC, Punta M, Qureshi M, Sangrador-Vegas A, et al. 2016. The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res. 44:D279–D285. doi:10.1093/nar/gkv1344
  • Flammang P, Lambert A, Bailly P, Hennebert E. 2009. Polyphosphoprotein-containing marine adhesives. J Adhes. 85:447–464. doi:10.1080/00218460902996358
  • Flammang P, Michel A, Cauwenberge A, Alexandre H, Jangoux M. 1998. A study of the temporary adhesion of the podia in the sea star Asterias rubens (Echinodermata, Asteroidea) through their footprints. J Exp Biol. 201:2383–2395.
  • Fleming RI, Mackenzie CD, Cooper A, Kennedy MW. 2009. Foam nest components of the tungara frog: a cocktail of proteins conferring physical and biological resilience. Proc R Soc B Biol Sci. 276:1787–1795. doi:10.1098/rspb.2008.1939
  • Foerder CA, Shapiro BM. 1977. Release of ovoperoxidase from sea urchin eggs hardens the fertilization membrane with tyrosine crosslinks. Proc Natl Acad Sci. 74:4214–4218. doi:10.1073/pnas.74.10.4214
  • Gorb SN. 2008. Biological attachment devices: exploring nature’s diversity for biomimetics. Philos Trans A Math Phys Eng Sci. 366:1557–1574. doi:10.1098/rsta.2007.2172
  • Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, et al. 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 29:644–652. doi:10.1038/nbt.1883
  • Graham LD, Glattauer V, Li D, Tyler MJ, Ramshaw JAM. 2013. The adhesive skin exudate of Notaden bennetti frogs (Anura: Limnodynastidae) has similarities to the prey capture glue of Euperipatoides sp. velvet worms (Onychophora: Peripatopsidae). Comp Biochem Physiol B Biochem Mol Biol. 165:250–259. doi:10.1016/j.cbpb.2013.04.008
  • Grens A, Gee L, Fisher DA, Bode HR. 1996. CnNK-2, an NK-2 homeobox gene, has a role in patterning the basal end of the axis in Hydra. Dev Biol. 180:473–488. doi:10.1006/dbio.1996.0321
  • Guerette PA, Hoon S, Seow Y, Raida M, Masic A, Wong FT, Ho VHB, Kong KW, Demirel MC, Pena-Francesch A, et al. 2013. Accelerating the design of biomimetic materials by integrating RNA-seq with proteomics and materials science. Nat Biotechnol. 31:908–915. doi:10.1038/nbt.2671
  • Habetha M, Bosch TCG. 2005. Symbiotic Hydra express a plant-like peroxidase gene during oogenesis. J Exp Biol. 208:2157–2165. doi:10.1242/jeb.01571
  • Hawkes EW, Eason EV, Christensen DL, Cutkosky MR. 2014. Human climbing with efficiently scaled gecko-inspired dry adhesives. J R Soc Interface. 12:20140675–20140675. doi:10.1098/rsif.2014.0675
  • Hennebert E, Leroy B, Wattiez R, Ladurner P. 2015. An integrated transcriptomic and proteomic analysis of sea star epidermal secretions identifies proteins involved in defense and adhesion. J Proteomics. 128:83–91. doi:10.1016/j.jprot.2015.07.002
  • Hennebert E, Wattiez R, Demeuldre M, Ladurner P, Hwang DS, Waite JH, Flammang P. 2014. Sea star tenacity mediated by a protein that fragments, then aggregates. Proc Natl Acad Sci. 111:6317–6322. doi:10.1073/pnas.1400089111
  • Hennebert E, Wattiez R, Flammang P. 2010. Characterisation of the carbohydrate fraction of the temporary adhesive secreted by the tube feet of the sea star Asterias rubens. Mar Biotechnol. 13:484–495.
  • Hobmayer B, Holstein TW, David CN. 1997. Stimulation of tentacle and bud formation by the neuropeptide head activator in Hydra magnipapillata. Dev Biol. 183:1–8. doi:10.1006/dbio.1996.8491
  • Hobmayer B, Jenewein M, Eder D, Eder M-K, Glasauer S, Gufler S, Hartl M, Salvenmoser W. 2012. Stemness in Hydra – a current perspective. Int J Dev Biol. 56:509–517. doi:10.1387/ijdb.113426bh
  • Hoffmeister-Ullerich SAH, Herrmann D, Kielholz J, Schweizer M, Schaller HC. 2002. Isolation of a putative peroxidase, a target for factors controlling foot-formation in the coelenterate Hydra. Eur J Biochem. 269:4597–4606. doi:10.1046/j.1432-1033.2002.03159.x
  • Jonker J-L, Abram F, Pires E, Varela Coelho A, Grunwald I, Power AM. 2014. Adhesive proteins of stalked and acorn barnacles display homology with low sequence similarities. PLoS ONE. 9:e108902. doi:10.1371/journal.pone.0108902
  • Juliano CE, Reich A, Liu N, Gotzfried J, Zhong M, Uman S, Reenan RA, Wessel GM, Steele RE, Lin H. 2014. PIWI proteins and PIWI-interacting RNAs function in Hydra somatic stem cells. Proc Natl Acad Sci. 111:337–342. doi:10.1073/pnas.1320965111
  • Kamino K, Nakano M, Kanai S. 2012. Significance of the conformation of building blocks in curing of barnacle underwater adhesive. FEBS J. 279:1750–1760.10.1111/j.1742-4658.2012.08552.x
  • Khanlari S, Dubé MA. 2013. Bioadhesives: a Review. Macromol React Eng. 7:573–587. doi:10.1002/mren.v7.11
  • Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10:R25. doi:10.1186/gb-2009-10-3-r25
  • Lebesgue N, da Costa G, Ribeiro RM, Ribeiro-Silva C, Martins GG, Matranga V, Scholten A, Cordeiro C, Heck AJR, Santos R. 2016. Deciphering the molecular mechanisms underlying sea urchin reversible adhesion: a quantitative proteomics approach. J Proteomics. 138:61–71. doi:10.1016/j.jprot.2016.02.026
  • Lee H, Dellatore SM, Miller WM, Messersmith PB. 2007. Mussel-inspired surface chemistry for multifunctional coatings. Science. 318:426–430. doi:10.1126/science.1147241
  • Leng N, Dawson JA, Thomson JA, Ruotti V, Rissman AI, Smits BMG, Haag JD, Gould MN, Stewart RM, Kendziorski C. 2013. EBSeq: an empirical Bayes hierarchical model for inference in RNA-seq experiments. Bioinformatics. 29:1035–1043. doi:10.1093/bioinformatics/btt087
  • Lengerer B, Hennebert E, Flammang P, Salvenmoser W, Ladurner P 2016. Adhesive organ regeneration in Macrostomum lignano. BMC Dev Biol. 16.
  • Lengerer B, Pjeta R, Wunderer J, Rodrigues M, Arbore R, Schärer L, Berezikov E, Hess MW, Pfaller K, Egger B, et al. 2014. Biological adhesion of the flatworm Macrostomum lignano relies on a duo-gland system and is mediated by a cell type-specific intermediate filament protein. Front Zool. 11:12. doi:10.1186/1742-9994-11-12
  • Li B, Dewey CN. 2011. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinf. 12:1.
  • Li W, Godzik A. 2006. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics. 22:1658–1659. doi:10.1093/bioinformatics/btl158
  • Lin H-C, Wong YH, Tsang LM, Chu KH, Qian P-Y, Chan BKK. 2014. First study on gene expression of cement proteins and potential adhesion-related genes of a membranous-based barnacle as revealed from next-generation sequencing technology. Biofouling. 30:169–181. doi:10.1080/08927014.2013.853051
  • Merker RI, Smit J. 1988. Characterization of the adhesive holdfast of marine and freshwater caulobacters. Appl Environ Microbiol. 54:2078–2085.
  • Miao Y, Zhang L, Sun Y, Jiao W, Li Y, Sun J, Wang Y, Wang S, Bao Z, Liu W. 2015. Integration of transcriptomic and proteomic approaches provides a core set of genes for understanding of scallop attachment. Mar Biotechnol. 17:523–532. doi:10.1007/s10126-015-9635-y
  • Ohkawa K, Nishida A, Yamamoto H, Waite JH. 2004. A glycosylated byssal precursor protein from the green mussel Perna viridis with modified dopa side-chains. Biofouling. 20:101–115. doi:10.1080/08927010410001681246
  • Pawlicki JM, Pease LB, Pierce CM, Startz TP, Zhang Y, Smith AM. 2004. The effect of molluscan glue proteins on gel mechanics. J Exp Biol. 207:1127–1135. doi:10.1242/jeb.00859
  • Peng Y, Leung HCM, Yiu S-M, Lv M-J, Zhu X-G, Chin FYL. 2013. IDBA-tran: a more robust de novo de Bruijn graph assembler for transcriptomes with uneven expression levels. Bioinformatics. 29:i326–i334. doi:10.1093/bioinformatics/btt219
  • Petersen HO, Höger SK, Looso M, Lengfeld T, Kuhn A, Warnken U, Nishimiya-Fujisawa C, Schnölzer M, Krüger M, Özbek S, et al. 2015. A comprehensive transcriptomic and proteomic analysis of Hydra head regeneration. Mol Biol Evol. 32:1928–1947.
  • Pfister D, De Mulder K, Philipp I, Kuales G, Hrouda M, Eichberger P, Borgonie G, Hartenstein V, Ladurner P. 2007. The exceptional stem cell system of Macrostomum lignano: screening for gene expression and studying cell proliferation by hydroxyurea treatment and irradiation. Front Zool. 4:9. doi:10.1186/1742-9994-4-9
  • Philpott DE, Chaet AB, Burnett AL. 1966. A study of the secretory granules of the basal disk of Hydra. J Ultrastruct Res. 14:74–84. doi:10.1016/S0022-5320(66)80036-9
  • Rodrigues M, Leclère P, Flammang P, Hess MW, Salvenmoser W, Hobmayer B, Ladurner P. 2016. The cellular basis of bioadhesion of the freshwater polyp Hydra. BMC Zool. 1:297. doi:10.1186/s40850-016-0005-7
  • Rodrigues M, Lengerer B, Ostermann T, Ladurner P. 2014. Molecular biology approaches in bioadhesion research. Beilstein J Nanotechnol. 5:983–993. doi:10.3762/bjnano.5.112
  • Rzepecki LM, Waite JH. 1993. The byssus of the zebra mussel, Dreissena polymorpha. II: structure and polymorphism of byssal polyphenolic protein families. Mol Mar Biol Biotechnol. 2:267–279.
  • Sagert J, Sun C, Waite JH. 2006. Chemical subtleties of mussel and polychaete holdfasts. In: Smith AM, Callow JA, editors. Biological Adhesives. Berlin: Springer; p. 125–143. doi:10.1007/978-3-540-31049-5
  • Shirokova VN, Begas OS, Knyazev NA, Samoilovich MP. 2009. Antigenic marker of differentiated cells of a Hydra basal disc. Cell Tissue Biol. 3:84–92. doi:10.1134/S1990519X0901012X
  • Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. 2015. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 31:3210–3212. doi:10.1093/bioinformatics/btv351
  • Smith AM, Callow JA, editors. 2006. Biological adhesives. Berlin: Springer.
  • Steele RE. 2002. Developmental signaling in Hydra: what does it take to build a “simple” animal? Dev Biol. 248:199–219. doi:10.1006/dbio.2002.0744
  • Stewart RJ, Ransom TC, Hlady V. 2011. Natural underwater adhesives. J Polym Sci Part B Polym Phys. 49:757–771. doi:10.1002/polb.22256
  • Stewart RJ, Wang CS. 2010. Adaptation of caddisfly larval silks to aquatic habitats by phosphorylation of H-fibroin serines. Biomacromolecules. 11:969–974. doi:10.1021/bm901426d
  • Suzek BE, Huang H, McGarvey P, Mazumder R, Wu CH. 2007. UniRef: comprehensive and non-redundant UniProt reference clusters. Bioinformatics. 23:1282–1288. doi:10.1093/bioinformatics/btm098
  • Tan Y, Hoon S, Guerette PA, Wei W, Ghadban A, Hao C, Miserez A, Waite JH. 2015. Infiltration of chitin by protein coacervates defines the squid beak mechanical gradient. Nat Chem Biol. 11:488–495. doi:10.1038/nchembio.1833
  • Technau U, Miller MA, Bridge D, Steele RE. 2003. Arrested apoptosis of nurse cells during Hydra oogenesis and embryogenesis. Dev Biol. 260:191–206. doi:10.1016/S0012-1606(03)00241-0
  • Thomsen S, Bosch TCG. 2006. Foot differentiation and genomic plasticity in Hydra: lessons from the PPOD gene family. Dev Genes Evol. 216:57–68. doi:10.1007/s00427-005-0032-9
  • Thongda W, Li C, Luo Y, Beck BH, Peatman E. 2014. l-Rhamnose-binding lectins (RBLs) in channel catfish, Ictalurus punctatus: characterization and expression profiling in mucosal tissues. Dev Comp Immunol. 44:320–331. doi:10.1016/j.dci.2014.01.018
  • Toubarro D, Gouveia A, Ribeiro RM, Simões N, da Costa G, Cordeiro C, Santos R. 2016. Cloning, characterization, and expression levels of the nectin gene from the tube feet of the sea urchin Paracentrotus Lividus. Mar Biotechnol. 18:372–383. doi:10.1007/s10126-016-9698-4
  • Treangen TJ, Sommer DD, Angly FE, Koren S, Pop M. 2011. Next generation sequence assembly with AMOS. In: Baxevanis AD, Petsko GA, Stein LD, Stormo GD, editors. Curr Protoc Bioinforma. Hoboken (NJ): John Wiley; p. 11.8.1–11.8.18.
  • Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG. 2012. Primer3–new capabilities and interfaces. Nucleic Acids Res. 40:e115–e115. doi:10.1093/nar/gks596
  • Vizcaíno JA, Csordas A, del-Toro N, Dianes JA, Griss J, Lavidas I, Mayer G, Perez-Riverol Y, Reisinger F, Ternent T, et al. 2016. 2016 update of the PRIDE database and related tools. Nucleic Acids Res. 44:D447–D456. doi:10.1093/nar/gkv1145
  • von Byern J, Grunwald I, editors. 2010. Biological adhesive systems. Vienna: Springer.
  • Wang C-S, Ashton NN, Weiss RB, Stewart RJ. 2014. Peroxinectin catalyzed dityrosine crosslinking in the adhesive underwater silk of a casemaker caddisfly larvae, Hysperophylax occidentalis. Insect Biochem Mol Biol. 54:69–79. doi:10.1016/j.ibmb.2014.08.009
  • Wang Z, Leary DH, Liu J, Settlage RE, Fears KP, North SH, Mostaghim A, Essock-Burns T, Haynes SE, Wahl KJ, Spillmann CM. 2015. Molt-dependent transcriptomic analysis of cement proteins in the barnacle Amphibalanus amphitrite. BMC Genomics. 16:859. doi:10.1186/s12864-015-2076-1
  • Warner SC, Waite JH. 1999. Expression of multiple forms of an adhesive plaque protein in an individual mussel, Mytilus edulis. Mar Biol. 134:729–734. doi:10.1007/s002270050589
  • Wenger Y, Galliot B. 2013. RNAseq versus genome-predicted transcriptomes: a large population of novel transcripts identified in an Illumina-454 Hydra transcriptome. BMC Genomics. 14:204. doi:10.1186/1471-2164-14-204
  • Westwood G, Horton TN, Wilker JJ. 2007. Simplified polymer mimics of cross-linking adhesive proteins. Macromolecules. 40:3960–3964. doi:10.1021/ma0703002
  • Yan X-C, Chen Z-F, Sun J, Matsumura K, Wu RSS, Qian P-Y. 2012. Transcriptomic analysis of neuropeptides and peptide hormones in the barnacle Balanus amphitrite: evidence of roles in larval settlement. PLoS ONE. 7:e46513. doi:10.1371/journal.pone.0046513
  • Zhao H, Sagert J, Hwang DS, Waite JH. 2009. Glycosylated hydroxytryptophan in a mussel adhesive protein from Perna viridis. J Biol Chem. 284:23344–23352. doi:10.1074/jbc.M109.022517