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PLOS ONE  2014 

Molecular Evidence of RNA Editing in Bombyx Chemosensory Protein Family

DOI: 10.1371/journal.pone.0086932

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Abstract:

Chemosensory proteins (CSPs) are small scavenger proteins that are mainly known as transporters of pheromone/odor molecules at the periphery of sensory neurons in the insect antennae and in the producing cells from the moth female pheromone gland. Sequencing cDNAs of RNA encoding CSPs in the antennae, legs, head, pheromone gland and wings from five single individual adult females of the silkworm moth Bombyx mori showed that they differed from genomic sequences by subtle nucleotide replacement (RDD). Both intronless and intronic CSP genes expressed RDDs, although in different rates. Most interestingly, in our study the degree of RDDs in CSP genes were found to be tissue-specific. The proportion of CSP-RDDs was found to be significantly much higher in the pheromone gland. In addition, Western blot analysis of proteins in different tissues showed existence of multiple CSP protein variant chains particularly found in the pheromone gland. Peptide sequencing demonstrated the occurrence of a pleiad of protein variants for most of all BmorCSPs from the pheromone gland. Our findings show that RNA editing is an important feature in the expression of CSPs and that a high variety of RDDs is found to expand drastically thus altering the repertoire of CSP proteins in a tissue-specific manner.

References

[1]  Moore MJ (2005) From birth to death: the complex lives of eukaryotic mRNAs. Science 309: 1514–1518. doi: 10.1126/science.1111443
[2]  Poole AM, Logan DT (2005) Modern mRNA proofreading and repair: clues that the last universal common possessed an RNA genome? Mol Biol Evol 22: 1444–1455. doi: 10.1093/molbev/msi132
[3]  Ju YS, Kim J-II, Kim S, Hong D, Park S, et al. (2011) Extensive genomic and transcriptional diversity identified through massively parallel DNA and RNA sequencing of eighteen Korean individuals. Nat Genet 43: 745–752. doi: 10.1038/ng.872
[4]  Simpson L (1998) RNA editing, pp. 483–496. In: G. Attardi, FAmaldi, eds. Origin and Evolution of Life, Vol I, Mechanisms of Genetical Expression, Section II.
[5]  Gott JM, Emeson RB (2000) Functions and mechanisms of RNA editing. Annu Rev Genet 34: 499–531. doi: 10.1146/annurev.genet.34.1.499
[6]  Nishikura K (2010) Functions and regulation of RNA editing by ADAR deaminases. Annu Rev Biochem 79: 321–349. doi: 10.1146/annurev-biochem-060208-105251
[7]  Song W, Liu Z, Tan J, Nomura Y, Dong K (2004) RNA editing generates tissue-specific sodium channels with distinct gating properties. J Biol Chem 279: 32554–32561. doi: 10.1074/jbc.m402392200
[8]  Tan BZ, Huang H, Lam R, Soong TW (2009) Dynamic regulation of RNA editing of ion channels and receptors in the mammalian nervous system. Mol Brain 2: 13 doi:101186/1756-6606-2-13.
[9]  Keegan LP, McGurk L, Palavicini JP, Brindle J, Paro S, et al. (2011) Functional conservation in human and Drosophila of metazoan ADAR2 involved in RNA editing: loss of ADAR1 in insects. Nucl Acid Res doi: 10.1093/nar/gkr423.
[10]  Chumakov KM, Norwood LP, Parker ML, Dragunski EM, Ran Y, et al. (1992) RNA sequence variants in live poliovirus vaccine and their relation to neurovirulence. J Virol 66: 966–970.
[11]  Picimbon J-F (2003) Biochemistry and evolution of CSP and OBP proteins, pp. 539–566. In: GJBlomquist, RGVogt, eds. Insect Pheromone Biochemistry and Molecular Biology, The Biosynthesis and Detection of Pheromones and Plant Volatiles, Elsevier Academic Press, London, San Diego.
[12]  Pelosi P, Zhou JJ, Ban LP, Calvello M (2006) Soluble proteins in insect chemical communication. Cell Mol Life Sci 63: 1658–1676. doi: 10.1007/s00018-005-5607-0
[13]  Zhou JJ, Kan Y, Antoniw J, Pickett JA, Field LM (2006) Genome and EST analyses and expression of a gene family with putative functions in insect chemoreception. Chem Senses 31: 453–465. doi: 10.1093/chemse/bjj050
[14]  Forêt SK, Wanner W, Maleszka R (2007) Chemosensory proteins in the honeybee: Insights from the annotated genome, comparative analysis and expression profiling. Insect Biochem Mol Biol 37: 19–28. doi: 10.1016/j.ibmb.2006.09.009
[15]  Xu YL, He P, Zhang L, Fang SQ, Dong SL, et al. (2009) Large-scale identification of odorant-binding proteins and chemosensory proteins from expressed sequence tags in insects. BMC Genomics 10: 632–644. doi: 10.1186/1471-2164-10-632
[16]  Picimbon J-F, Dietrich K, Breer H, Krieger J (2000a) Chemosensory proteins of Locusta migratoria (Orthoptera : Acrididae). Insect Biochem Mol Biol 30: 233–241. doi: 10.1016/s0965-1748(99)00121-6
[17]  Picimbon J-F, Dietrich K, Angeli S, Scaloni A, Krieger J, et al. (2000b) Purification and molecular cloning of chemosensory proteins from Bombyx mori. Arch Insect Biochem Physiol 44: 120–129. doi: 10.1002/1520-6327(200007)44:3<120::aid-arch3>3.0.co;2-h
[18]  Angeli S, Ceron F, Scaloni A, Monti M, Monteforti G, et al. (1999) Purification, structural characterization, cloning and immunocytochemical localization of chemoreception proteins from Schistocerca gregaria. Eur J Biochem 262: 745–754. doi: 10.1046/j.1432-1327.1999.00438.x
[19]  Monteforti G, Angeli S, Petacchi R, Minnocci A (2002) Ultrastructural characterization of antennal sensilla and immunocytochemical localization of a chemosensory protein in Carausius morosus Brunner (Phasmida: Phasmatidae). Arthropod Struct Dev 30: 195–205. doi: 10.1016/s1467-8039(01)00036-6
[20]  Ozaki M, Wada-Katsumata A, Fujikawa K, Iwasaki M, Yokohari F, et al. (2005) Ant nestmate and non-nestmate discrimination by a chemosensory sensillum. Science 309: 311–314. doi: 10.1126/science.1105244
[21]  Picimbon J-F, Leal WS (1999) Olfactory soluble proteins of cockroaches. Insect Biochem Mol Biol 30: 973–978. doi: 10.1016/s0965-1748(99)00073-9
[22]  Ishida Y, Chiang V, Leal WS (2002) Protein that makes sense in the argentine ant. Naturwissensch 89: 505–507. doi: 10.1007/s00114-002-0368-1
[23]  Zhang S, Zhang YJ, Su HH, Gao XW, Guo YY (2007) Identification and expression pattern of putative odorant-binding proteins and chemosensory proteins in antennae of the Microplitis mediator (Hymenoptera: braconidae). Chem Senses 34: 503–512. doi: 10.1093/chemse/bjp027
[24]  Gonzales D, Zhao Q, McMahan C, Velasquez D, Haskins WE, et al. (2009) The major antennal chemosensory protein of red imported fire ant workers. Insect Mol Biol 18: 395–404. doi: 10.1111/j.1365-2583.2009.00883.x
[25]  Nomura A, Kawasaki K, Kubo T, Natori S (1992) Purification and localization of p10, a novel protein that increases in nymphal regenerating legs of Periplaneta americana (American cockroach). Int J Dev Biol 36: 391–398.
[26]  Kitabayashi AN, Arai T, Kubo T, Natori S (1998) Molecular cloning of cDNA for p10, a novel protein that increases in the regenerating legs of Periplaneta americana (American cockroach). Insect Biochem Mol Biol 28: 785–790. doi: 10.1016/s0965-1748(98)00058-7
[27]  Picimbon J-F, Dietrich K, Krieger J, Breer H (2001) Identity and expression pattern of chemosensory proteins in Heliothis virescens (Lepidoptera, Noctuidae). Insect Biochem Mol Biol 31: 1173–1181. doi: 10.1016/s0965-1748(01)00063-7
[28]  Wanner KW, Isman MB, Feng Q, Plettner E, Theilmann DA (2005) Developmental expression patterns of four chemosensory protein genes from the Easturn spruce budworm, Choristoneura fumiferana. Insect Mol Biol 14: 289–300. doi: 10.1111/j.1365-2583.2005.00559.x
[29]  Maleszka J, Forêt S, Saint R, Maleszka R (2007) RNAi-induced phenotypes suggest a novel role for a chemosensory protein CSP5 in the development of embryonic integument in the honeybee (Apis mellifera). Dev Genes Evol 217: 189–196. doi: 10.1007/s00427-006-0127-y
[30]  Jacquin-Joly E, Vogt RG, Fran?ois MC, Nagnan-Le Meillour P (2001) Functional and expression pattern analysis of chemosensory proteins expressed in antennae and pheromonal gland of Mamestra brassicae. Chem Senses 26: 833–844. doi: 10.1093/chemse/26.7.833
[31]  Str?ndh M, Johansson T, Ahren D, L?fstedt C (2008) Transcriptional analysis of the pheromone gland of the turnip moth, Agrotis segetum (Noctuidae), reveals candidate genes involved in pheromone production. Insect Mol Biol 17: 73–85. doi: 10.1111/j.1365-2583.2008.00782.x
[32]  Vogel H, Heidel AJ, Heckel DG, Groot AT (2010) Transcriptome analysis of the sex pheromone gland of the noctuid moth Heliothis virescens. BMC Genomics 11: 29. doi: 10.1186/1471-2164-11-29
[33]  Dani FR, Michelucci E, Francese S, Mastrobuoni G, Cappellozza S, et al. (2011) Odorant-binding proteins and chemosensory proteins in pheromone detection and release in the silkworm Bombyx mori. Chem Senses 36: 335–344. doi: 10.1093/chemse/bjq137
[34]  Lartigue A, Campanacci V, Roussel A, Larsson AM, Jones TA, et al. (2002) X-ray structure and ligand binding study of a moth chemosensory protein. J Biol Chem 277: 2094–32098. doi: 10.1074/jbc.m204371200
[35]  Jansen S, Zídek L, L?fstedt C, Picimbon J-F, Sklenar V (2006) 1H, 13C, and 15N resonance assignment of Bombyx mori chemosensory protein 1 (BmorCSP1). J Biomol NMR 36: 47. doi: 10.1007/s10858-006-9019-8
[36]  Jansen S, Chmelik J, Zídek L, Padrta P, Novak P, et al. (2007) Structure of Bombyx mori Chemosensory Protein 1 in solution. Arch Insect Biochem Physiol 66: 135–145. doi: 10.1002/arch.20205
[37]  Tomaselli S, Crescenzi O, Sanfelice D, Ab E, Wechselberger R, et al. (2006) Solution structure of a chemosensory protein from the desert locust Schistocerca gregaria. Biochemistry 45: 1606–1613. doi: 10.1021/bi060998w
[38]  Wanner KW, Willis LG, Theilmann DA, Isman MB, Feng Q, et al. (2004) Analysis of the insect os-d-like gene family. J Chem Ecol 30: 889–911. doi: 10.1023/b:joec.0000028457.51147.d4
[39]  The International Aphid Genomics Consortium (2010) Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biol 8: e1000313 doi:10.1371/journal.pbio.1000313.
[40]  Gong DP, Zhang HJ, Zhao P, Lin Y, Xia QY, et al. (2007) Identification and expression pattern of the Chemosensory Protein gene family in the silkworm, Bombyx mori. Insect Biochem Mol Biol 37: 266–277. doi: 10.1016/j.ibmb.2006.11.012
[41]  Ozaki K, Utoguchi A, Yamada A, Yoshikawa H (2008) Identification and genomic structure of chemosensory proteins (CSP) and odorant binding protein (OBP) genes expressed in foreleg tarsi of the swallowtail butterfly Papilio xuthus. Insect Biochem Mol Biol 38: 969–976. doi: 10.1016/j.ibmb.2008.07.010
[42]  Campanacci V, Lartigue A, H?llberg BM, Jones TA, Giuici-Orticoni MT, et al. (2003) Moth chemosensory protein exhibits drastic conformational changes and cooperativity on ligand binding. Proc Natl Acad Sci USA 100: 5069–5074. doi: 10.1073/pnas.0836654100
[43]  Mosbah A, Campanacci V, Lartigue A, Tegoni M, Cambillau C, et al. (2003) Solution structure of a chemosensory protein from the moth Mamestra brassicae. Biochem J 369: 39–44. doi: 10.1042/bj20021217
[44]  McKenna MP, Hekmat-Scafe DS, Gaines P, Carlson JR (1994) Putative Drosophila pheromone-binding-proteins expressed in a subregion of the olfactory system. J Biol Chem 269: 16340–16347.
[45]  Pikielny CW, Hasan G, Rouyer E, Rosbach M (1994) Members of a family of Drosophila putative odorant-binding proteins are expressed in different subsets of olfactory hairs. Neuron 12: 35–49. doi: 10.1016/0896-6273(94)90150-3
[46]  Robertson HM, Martos R, Sears CR, Todres EZ, Walden KKO, et al. (1999) Diversity of odourant binding proteins revealed by an expressed sequence tag project on male Manduca sexta moth antenna. Insect Mol Biol 8: 501–518. doi: 10.1046/j.1365-2583.1999.00146.x
[47]  Stapleton M, Liao G, Brokstein P, Hong L, Carninci P, et al. (2002) The Drosophila gene collection: identification of putative full-length cDNAs for 70% of D. melanogaster genes. Genome Res 12: 1294–1300. doi: 10.1101/gr.269102
[48]  Ban LP, Scaloni A, Brandazza A, Angeli S, Zhang L, et al. (2003) Chemosensory proteins of Locusta migratoria. Insect Mol Biol 12: 125–134. doi: 10.1046/j.1365-2583.2003.00394.x
[49]  Park Y, Aikins JA, Wang LJ, Beeman RW, Oppert B, et al. (2007) Analysis of transcriptome data in the red flour beetle, Tribolium castaneum. Insect Biochem Mol Biol 38: 380–386. doi: 10.1016/j.ibmb.2007.09.008
[50]  Tweedie S, Ashburner M, Falls K, Leyland P, McQuilton P, et al. (2009) FlyBase: enhancing Drosophila Gene Ontology annotations. Nucl Acids Res 37: D555–D559 doi:10.1093/nar/gkn788.
[51]  Zhou JJ, Vieira FG, He XL, Smadja C, Liu R, et al. (2010) Genome annotation and comparative analyses of the odorant-binding proteins and chemosensory proteins in the pea aphid Acyrthosiphon pisum. Insect Mol Biol 19: 113–122. doi: 10.1111/j.1365-2583.2009.00919.x
[52]  Grosse-Wilde E, Kuebler LS, Bucks S, Vogel H, Wicker D, et al. (2011) Antennal transcriptome of Manduca sexta. Proc Natl Acad Sci USA 108: 7449–7454. doi: 10.1073/pnas.1017963108
[53]  Den Dunnen JT, Antonarakis SE (2000) Mutation nomenclature extensions and suggestions to describe complex mutations: A discussion. The HUGO Mutation Database Initiative: Issues, Databases and Perspectives for the New Millenium 15: 7–12. doi: 10.1002/(sici)1098-1004(200001)15:1<7::aid-humu4>3.0.co;2-n
[54]  Butenandt A, Beckman R, Stamm D, Hecker E (1959) über den Sexuallockstoff des Seidenspinner Bombyx mori, Reidarstellung und Kunstitution. Z Natürforsch 14B: 283–284.
[55]  Kasang G, Kaissling KE, Vostrowsky O, Bestmann HJ (1978) Bombykal, a second pheromone component of the silkworm moth Bombyx mori. L Ang Chem 17: 60. doi: 10.1002/anie.197800601
[56]  Matsumoto S, Moto KI, Wang F (2001) Cellular events and molecular mechanisms underlying sex pheromone production in the silkmoth, Bombyx mori. RIKEN Rev 41: 79–81.
[57]  Schlyter F, Birgesson G (1989) Individual variation in bark beetle and moth pheromones - a comparison and evolutionary background. Holarc Ecol 12: 457–465. doi: 10.1111/j.1600-0587.1989.tb00923.x
[58]  Kim DDY, Kim TTY, Walsh T, Kobayashi Y, Matise TC, et al. (2004) Widespread RNA editing of embedded Alu elements in the human transcriptome. Genome Res 14: 1719–1725. doi: 10.1101/gr.2855504
[59]  Schrider DR, Gout J-F, Hahn MW (2011) Very few RNA and DNA sequence differences in the human transcriptome. PLOS One 6: e25842 doi:10.1371/journal.pone.0025842.
[60]  Li M, Wang IX, Li Y, Bruzel A, Richards AL, et al. (2011) Widespread RNA and DNA sequence differences in the human transcriptome. Science 333: 53–58. doi: 10.1126/science.1207018
[61]  Hayden EC (2012) RNA editing study under intense scrutiny. Nature News & Comments doi:10.1038/nature.2012.10217.
[62]  Piskol R, Peng Z, Wang J, Li JB (2013) Lack of evidence for existence of noncanonical RNA editing. Nature Biotech 31: 19–20. doi: 10.1038/nbt.2472
[63]  Li JB, Levanon EY, Yoon JK, Aach J, Xie B, et al. (2009) Genome-wide identification of human RNA editing sites by parallel DNA capturing and sequencing. Science 324: 1210–1213. doi: 10.1126/science.1170995
[64]  Savva YA, Rieder LE, Reenan RA (2012) The ADAR protein family. Genome Biol 13: 252. doi: 10.1186/gb-2012-13-12-252
[65]  Mita K, Kasahara M, Sasaki S, Nagayasu Y, Yamada T, et al. (2004) The genome sequence of Silkworm, Bombyx mori. DNA Res 11: 27–35. doi: 10.1093/dnares/11.1.27
[66]  Xia Q, Zhou Z, Lu C, Cheng D, Dai F, et al. (2004) A draft sequence for the genome of the domesticated silkworm (Bombyx mori). Science 306: 1937–1940. doi: 10.1126/science.1102210
[67]  Wang J, Xia Q, He X, Dai M, Ruan J, et al. (2005) SilkDB: a knowledgebase for silkworm biology and genomics. Nucl Acids Res 33: 399–402.
[68]  Hogan DJ, Riordan DP, Gerber AP, Herschlag D, Brown PO (2008) Diverse RNA-binding proteins interact with functionally related sets of RNAs, suggesting an extensive regulatory system. PLoS Biol 6: e255 doi:10.1371/journal.pbio.0060255.
[69]  Idler RK, Yan W (2011) Control of messenger RNA fate by RNA binding proteins: an emphasis on mammalian spermatogenesis. J Androl 33: 309–337 doi:10.2164/jandrol.111.014167.
[70]  Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res 32: 1792–1797. doi: 10.1093/nar/gkh340
[71]  Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ (2009) Jalview Version 2 - a multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189–1191. doi: 10.1093/bioinformatics/btp033
[72]  Rappsilber J, Mann M, Ishihama Y (2007) Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nature protocols 2: 1896–1906. doi: 10.1038/nprot.2007.261

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