Evolution of Protein Physical Structures in Insect Chemosensory Systems

  • Jean-François PicimbonEmail author


Insect chemosensory protein (CSP) structures are built of six-seven α-helices, four cysteines making two adjacent disulfide bridges forming a multifunction prism for transport of lipid chains and small insecticide chemicals. Moth pheromone binding proteins (PBPs) have bowl-like globular structures made of six α-helices; six cysteines forming three interlocked disulfide bridges. Niemann-Pick type C2 proteins mediating chemical communication in ants display β-barrel structures, similar to mammalian lipocalins and odor binding proteins (OBPs). How do all these structures relate to each other from an evolutionary standpoint? What was the folding of the ancestral “chemosensory” molecule? A close overview of “chemosensory” protein structures described in insects suggests that addition of cysteine residues has played a key role in the evolution of function in the vast functional repertoire of binding proteins. In addition, motif insertion, motif inversion, duplication of amino acid pairs and specific residue substitution in typical locations of the protein structure might have been essential to lead to new protein structures and new functions. Importantly, addition of key residues such as glycine near conserved cysteine residues might lead to insertion or deletion of secondary structural elements, depending on the protein family. The chapter presented here describes the multi-level aspects of mutations that govern evolution and function in the vast repertoire of binding protein families. I try to understand evolution of these protein structures and functions using both RNA and peptide mutations recently discovered in the Bombyx system.



Heartfelt thanks to Prof. Em. Anders Liljas (Lund University, Sweden) for inspiration, discussion and most helpful comments on early versions of this manuscript.


  1. Abraham D, Gadenne C, Löfstedt C, Picimbon JF (2005) Molecular characterization and evolution of pheromone binding protein genes in Agrotis moths. Insect Biochem Mol Biol 35:1100–1111PubMedGoogle Scholar
  2. Ahmed T, Zhang T, Wang Z, He K, Bai S (2017) C-terminus methionene specifically involved in binding corn odorants to odor binding protein4 in Macrocentrus cingulum. Front Physiol 8:62PubMedPubMedCentralGoogle Scholar
  3. Aizenberg-Gershtein Y, Izhaki I, Halpem M (2013) Do honeybees shape the bacterial community composition in floral nectar. PLoS One 8:e67556CrossRefPubMedPubMedCentralGoogle Scholar
  4. Alhamidi M, Buvang EK, Fagerheim T, Brox V, Lindal S, Van Ghelue M, Nilssen Ø (2011) Fukutin-related protein resides in the Golgi cisternae of skeletal muscle fibres and form disulfide-linked homodimers via an N-terminal interaction. PLoS One 6:e22968CrossRefPubMedPubMedCentralGoogle Scholar
  5. Altman S (1990) Nobel lecture. Enzymatic cleavage of RNA by RNA. Biosci Rep 10:317–337CrossRefPubMedGoogle Scholar
  6. Åmand HL, Nordén B, Fant K (2012) Functionalization with C-terminal cysteine enhances transfection efficiency of cell-penetrating peptides through dimer formation. Biochem Biophys Res Commun 418:469–474CrossRefPubMedGoogle Scholar
  7. Andras P, Andras C (2005) The origins of life – the ‘protein interaction world’ hypothesis: protein interactions were the first form of self-reproducing life and nucleic acids evolved later as memory molecules. Med Hypotheses 64:678–688CrossRefPubMedGoogle Scholar
  8. Angeli S, Ceron F, Scaloni A, Monti M, Monteforti G, Minnocci A, Petacchi R, Pelosi P (1999) Purification, structural characterization, cloning and immunocytochemical localization of chemoreception proteins from Schistocerca gregaria. Eur J Biochem 262:745–754CrossRefPubMedGoogle Scholar
  9. Arrese EL, Soulages JL (2010) Insect fat body: energy, metabolism, and regulation. Annu Rev Entomol 55:207–225CrossRefPubMedPubMedCentralGoogle Scholar
  10. Atkins JF, Gesterland RF, Cech T (2006) The RNA world: the nature of modern RNA suggests a prebiotic RNA world. Cold Spring Harbor Laboratory Press, Plainview, pp 137–156Google Scholar
  11. Bartkiewicz M, Gold H, Altman S (1989) Identification and characterization of an RNA molecule that copurifies with RNase P activity from HeLa cells. Genes Dev 3:488–499CrossRefPubMedGoogle Scholar
  12. Bashton M, Chothia C (2002) The geometry of domain contribution in proteins. J Mol Biol 315:927–939CrossRefPubMedGoogle Scholar
  13. Baumann K (2017) Stem cells. A key to totipotency. Nat Rev Mol Cell Dev Biol 18:137CrossRefGoogle Scholar
  14. Bell SL, Forstner JF (2001) Role of the cysteine-knot motif at the C-terminus of rat mucin protein Muc2 in dimer formation and secretion. Biochem J 1:203–209CrossRefGoogle Scholar
  15. Bell TJ, Miyashiro KY, Sul JY, Buckley PT, Lee MT, McCullough RM, Jochems J, Kim J, Cantor CR, Parsons TD, Eberwine JH (2010) Intron retention facilitates splice variant diversity in calcium-activated big potassium channel populations. Proc Natl Acad Sci U S A 107:21152–21157CrossRefPubMedPubMedCentralGoogle Scholar
  16. Breaker RR (2012) Riboswitches and the RNA world. Cold Spring Harb Perspect Biol 4:a003566CrossRefPubMedPubMedCentralGoogle Scholar
  17. Bushdid C, Magnasco MO, Vosshall LB, Keller A (2014) Humans can discriminate more than 1 trillion olfactory stimuli. Science 343:1370–1372CrossRefPubMedPubMedCentralGoogle Scholar
  18. Calvo E, Mans BJ, Ribeiro JMC, Andersen JF (2009) Multifunctionality and mechanism of ligand binding in a mosquito antiinflammatory protein. Proc Natl Acad Sci U S A 106:3728–3733CrossRefPubMedPubMedCentralGoogle Scholar
  19. Camoletto P, Colesanti A, Ozon S, Sobel A, Fasolo A (2001) Expression of stathmin and SCG10 proteins in the olfactory neurogenesis during development and after lesion in the adulthood. Brain Res Bull 1:19–28CrossRefGoogle Scholar
  20. Campanacci V, Lartigue A, Hällberg BM, Jones TA, Giuici-Orticoni MT, Tegoni M, Cambillau C (2003) Moth chemosensory protein exhibits drastic conformational changes and cooperativity on ligand binding. Proc Natl Acad Sci U S A 100:5069–5074CrossRefPubMedPubMedCentralGoogle Scholar
  21. Carruthers MD, Nicholson PA, Tracy EN, Munson RS Jr (2013) Acinetobacter baumannii utilizes a type VI secretion system for bacterial competition. PLoS One 8:e59388CrossRefPubMedPubMedCentralGoogle Scholar
  22. Castelvecchi D (2016) Building blocks for “RNA world” made from simple ingredients. Chemical assembly bolsters theory that life might have begun with RNA. Nature
  23. Cech TR (1986) A model for the RNA-catalyzed replication of RNA. Proc Natl Acad Sci U S A 83:4360–4363CrossRefPubMedPubMedCentralGoogle Scholar
  24. Cech TR (1990) Nobel lecture. Self-splicing and enzymatic activity of an intervening sequence RNA from Tetrahymena. Biosci Rep 10:239–261Google Scholar
  25. Cech TR (2012) The RNA worlds in context. Cold Spring Harb Perspect Biol 4:a006742CrossRefPubMedPubMedCentralGoogle Scholar
  26. Chen W et al (2016) The draft genome of whitefly Bemisia tabaci MEAM1, a global crop pest, provides novel insights into virus transmission, host adaptation, and insecticide resistance. BMC Biol 14:110CrossRefPubMedPubMedCentralGoogle Scholar
  27. Claverie JM, Ogata H (2003) Insertion of palindromic repeats in the evolution of proteins. Trends Biochem Sci 28:75–80CrossRefPubMedGoogle Scholar
  28. Condic ML (2014) Totipotency: what it is and what it is not. Stem Cells Dev 23:796–812CrossRefPubMedGoogle Scholar
  29. Crick HH (1968) The origin of the genetic code. J Mol Biol 38:367–379CrossRefPubMedGoogle Scholar
  30. Dawaliby R, Trubbia C, Delporte C, Masureel M, Van Antwerpen P, Kobilka BK, Govaerts C (2016) Allosteric regulation of G-protein coupled receptor activity by phospholipids. Nat Chem Biol 12:35–39CrossRefPubMedGoogle Scholar
  31. Diaz-Latoud C, Buache E, Javouhey E, Arrigo AP (2005) Substitution of the unique cysteine residue of murine Hsp25 interferes with the protective activity of this stress protein through inhibition of dimer formation. Antioxid Redox Signal 7:436–445CrossRefPubMedGoogle Scholar
  32. Douglas AE (2015) Multiorganismal insects: diversity and function of resident microorganisms. Annu Rev Entomol 60:17–34CrossRefPubMedGoogle Scholar
  33. Drurey C, Mathers TC, Prince DC, Wilson C, Caceres-Moreno C, Mugford ST, Hogenhout SA (2017) Chemosensory proteins in the CSP4 clade evolved as plant immunity suppressors before two suborders of plant-feeding hemipteran insects diverged. Cold Spring Harb Lab BioRxiv
  34. Dutton RJ, Boyd D, Berkmen M, Beckwith J (2008) Bacterial species exhibit diversity in their mechanisms and capacity for protein disulfide bond formation. Proc Natl Acad Sci U S A 105:11933–11938CrossRefPubMedPubMedCentralGoogle Scholar
  35. Eckland EH, Szostak JW, Bartel DP (1995) Structurally complex and highly active RNA ligases derived from random RNA sequences. Science 269:364–370CrossRefGoogle Scholar
  36. Feng L, Prestwich GD (1997) Expression and characterization of a lepidopteran general odorant binding protein. Insect Biochem Mol Biol 27:405–412CrossRefPubMedGoogle Scholar
  37. Ferré-D’Amaré AR, Scott WG (2010) Small self-cleaving ribozymes. Cold Spring Harb Prespect Biol 2:a003574Google Scholar
  38. Filloux A (2010) Secretion signal and protein targeting in bacteria: a biological puzzle. J Bacteriol 192:3847–3849CrossRefPubMedPubMedCentralGoogle Scholar
  39. Fujimoto Z, Suzuki R, Shiotsuki T, Tsuchiya W, Tase A, Momma M, Yamazaki T (2013) Crystal structure of silkworm Bombyx mori JHBP in complex with 2-methyl-2,4-pentanediol: plasticity of JH-binding pocket and ligand-induced conformational change of the second cavity in JHBP. PLoS One 8:e56261CrossRefPubMedPubMedCentralGoogle Scholar
  40. Ghai R, Mizuno CM, Picazo A, Camacho A, Rodriguez-Valera F (2013) Metagenomics uncovers a new group of low GC and ultra-small marine Actinobacteria. Sci Rep 3:2471CrossRefPubMedPubMedCentralGoogle Scholar
  41. Gilbert W (1986) The RNA world. Nature 319:618CrossRefGoogle Scholar
  42. Gilbert W (1987) The exon theory of genes. Cold Spring Harb Symp Quant Boil 52:901–905CrossRefGoogle Scholar
  43. Glycos NM, Cesareni G, Kokkindis M (1999) Protein plasticity to the extreme: changing the topology of a 4-alpha-helical bundle with a single amino acid substitution. Structure 7:597–603CrossRefGoogle Scholar
  44. Gong DP, Zhang HJ, Zhao P, Lin Y, Xia QY, Xiang ZH (2007) Identification and expression pattern of the chemosensory protein gene family in the silkworm, Bombyx mori. Insect Biochem Mol Biol 37:266–277CrossRefPubMedGoogle Scholar
  45. Graham LA, Brewer D, Lajoie G, Davies PL (2003) Characterization of a subfamily of beetle odorant-binding proteins found in hemolymph. Mol Cell Proteomics 2:541–549CrossRefPubMedGoogle Scholar
  46. Gräter F, de Groot BL, Jiang H, Grubmüller H (2006a) Ligand release pathways in the pheromone-binding protein of Bombyx mori. Structure 14:1567–1576CrossRefPubMedGoogle Scholar
  47. Gräter F, Xu W, Leal WS, Grubmüller H (2006b) Pheromone discrimination by the pheromone-binding protein of Bombyx mori. Structure 14:1577–1586CrossRefPubMedGoogle Scholar
  48. Greengard P, Valtorta F, Czernik AJ, Benfenati F (1993) Synaptic vesicle phosphoproteins and regulation of synaptic function. Science 5:780–785CrossRefGoogle Scholar
  49. Guerrier-Takada C, Altman S (1984) Catalytic activity of an RNA molecular prepared by transcription in vitro. Science 223:285–286CrossRefPubMedGoogle Scholar
  50. Guerrier-Takada C, Gardiner K, Marsh T, Pace N, Altman S (1983) The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell 35:849–857CrossRefPubMedGoogle Scholar
  51. Hogenhout SA, Oshima K, El Desouky A, Namba S (2008) Phytoplasmas: bacteria that manipulate plants and insects. Mol Plant Pathol 9:403–423CrossRefPubMedGoogle Scholar
  52. Horst R, Damberger F, Luginbühl P, Güntert P, Peng G, Nikonova L, Leal WS, Wüthrich K (2001) NMR structure reveals intramolecular regulation mechanism for pheromone binding and release. Proc Natl Acad Sci U S A 25:14374–14379CrossRefGoogle Scholar
  53. Jaiteh M, Taly A, Hénin J (2016) Evolution of pentameric ligand-gated ion channel: pro-loop receptors. PLoS One 11:e0151934CrossRefPubMedPubMedCentralGoogle Scholar
  54. Jansen S, Zídek L, Löfstedt C, Picimbon JF, Sklenar V (2006) 1H, 13C, and 15N resonance assignment of Bombyx mori chemosensory protein 1 (BmorCSP1). J Biomol NMR 36:47CrossRefPubMedGoogle Scholar
  55. Jansen S, Chmelik J, Zídek L, Padrta P, Novak P, Zdrahal Z, Picimbon JF, Löfstedt C, Sklenar V (2007) Structure of Bombyx mori chemosensory protein 1 in solution. Arch Insect Biochem Physiol 66:135–145CrossRefPubMedGoogle Scholar
  56. Jarvis DL, Summers MD, Bohlmeyer DA (1993) Influence of different signal peptides and prosequences on expression and secretion of human tissue plasminogen activator in the baculovirus system. J Biol Chem 268:16754–16762PubMedGoogle Scholar
  57. Jindra M, Palli SR, Riddiford LM (2013) The juvenile hormone signaling pathway in insect development. Annu Rev Entomol 58:181–204CrossRefPubMedGoogle Scholar
  58. Kaltenpoth M (2009) Actinobacteria as mutualists: general healthcare for insects? Trends Microbiol 17:529–535CrossRefPubMedGoogle Scholar
  59. Kapp K, Schrempf S, Lemberg MK, Dobberstein B (2009) Post-targeting functions of signal peptides. In: Zimmermann R (ed) Protein transport into the endoplasmic reticulum. Landes Bioscience, Austin, 2000–2013Google Scholar
  60. Kay BK, Williamson MP, Sudol M (2000) The importance of being proline: the interaction of proline-rich motifs in signalling proteins with their cognate domains. FASEB J 14:231–241CrossRefPubMedGoogle Scholar
  61. Keeley LL (1981) Neuroendocrine regulation of mitochondrial development and function in the insect fat body. In: Downer RGH (ed) Energy metabolism in insects. Springer, Boston, pp 207–237CrossRefGoogle Scholar
  62. Kim IH, Pham V, Jablonka W, Goodman WG, Ribeiro JMC, Andersen JF (2017) A mosquito hemolymph odorant-binding protein family member specifically binds juvenile hormone. J Biol Chem 292:15329–15339CrossRefPubMedPubMedCentralGoogle Scholar
  63. Knight CA, Molinari NA, Petrov DA (2005) The large genome constraint hypothesis: evolution, ecology and phenotype. Ann Bot 95:177–195CrossRefPubMedPubMedCentralGoogle Scholar
  64. Kolodziejczyk R, Bujacz G, Jakób M, Ożyhar A, Jaskolki M, Kochman M (2008) Insect juvenile hormone binding protein shows ancestral fold present in human lipid-binding proteins. J Mol Biol 377:870–881CrossRefPubMedGoogle Scholar
  65. Krieger F, Möglich A, Kiefhaber T (2005) Effect of proline and glycine residues on dynamics and barriers of loop formation in polypeptide chains. J Am Chem Soc 127:3346–3352CrossRefPubMedGoogle Scholar
  66. Krieger J, Gänßle K, Raming K, Breer H (1993) Odorant binding proteins of Heliothis virescens. Insect Biochem Mol Biol 23:449–456CrossRefPubMedGoogle Scholar
  67. Krieger J, von Nickisch-Roseneck EV, Mameli M, Pelosi P, Breer H (1996) Binding proteins from the antennae of Bombyx mori. Insect Biochem Mol Biol 26:297–307CrossRefPubMedGoogle Scholar
  68. Krishna MMG, Englander SW (2004) The N-terminal to C-terminal motif in protein folding and function. Proc Natl Acad Sci U S A 102:1053–1058CrossRefGoogle Scholar
  69. Kruger K, Grabowski PJ, Zaug AJ, Sands J, Gottschling DE, Cech TR (1982) Self-splicing RNA: autoexcision and autocyclization of the ribosomal RNA intervening sequence of Tetrahymena. Cell 31:147–157CrossRefPubMedGoogle Scholar
  70. Kulmuni J, Wurm Y, Pamilo P (2013) Comparative genomics of chemosensory protein genes reveals rapid evolution and positive selection in ant-specific duplicates. Heredity 110:538–547CrossRefPubMedPubMedCentralGoogle Scholar
  71. Lagarde S, Spinelli S, Qiao H, Tegoni M, Pelosi P, Cambillau C (2011) Crystal structure of a novel type of odorant-binding protein 20 from the malaria mosquito Anopheles gambiae, belonging to the C-plus class. Biochem J 437:423–430CrossRefPubMedGoogle Scholar
  72. Lane JR, Abdul-Ridha A, Canals M (2013) Regulation of G-protein-coupled receptors by allosteric ligands. ACS Chem Neurosci 4:527–534CrossRefPubMedPubMedCentralGoogle Scholar
  73. Lartigue A, Campanacci V, Roussel A, Larsson AM, Jones TA, Tegoni M, Cambillau C (2002) X-ray structure and ligand binding study of a moth chemosensory protein. J Biol Chem 277:32094–32098CrossRefPubMedGoogle Scholar
  74. La Scola B, Raoult D (2004) Acinetobacter baumannii in human body louse. Emerg Infect Dis 10:1671–1673CrossRefPubMedPubMedCentralGoogle Scholar
  75. Leal WS (2000) Duality monomer-dimer of the pheromone-binding protein from Bombyx mori. Biochem Biophys Res Commun 16:521–529CrossRefGoogle Scholar
  76. Leal WS, Nikonova L, Peng G (1999) Disulfide structure of the pheromone binding protein from the silkworm moth, Bombyx mori. FEBS Lett 464:85–90CrossRefPubMedGoogle Scholar
  77. Leshkowitz D, Gazit S, Reuveni E, Ghanim M, Czosnek H, McKenzie C, Shatters RL Jr, Brown JK (2006) Whitefly (Bemisia tabaci) genome project: analysis of sequenced clones from egg, instar and adult (viruliferous and non-viruliferous) cDNA libraries. BMC Genomics 7:79–98CrossRefPubMedPubMedCentralGoogle Scholar
  78. Liljas A, Liljas L, Ash MR, Lindblom G, Nissen P, Kjeldgaard M (2017) Textbook of structural biology, 2nd ed. World Scientific, p 612Google Scholar
  79. Lim S, Smith KR, Lim STS, Tian R, Lu J, Tan M (2016) Regulation of mitochondrial functions by protein phosphorylation and dephosphorylation. Cell Biosci 6:25CrossRefPubMedPubMedCentralGoogle Scholar
  80. Liu GX, Picimbon JF (2017) Bacterial origin of chemosensory odor-binding proteins. Gene Transl Bioinform 3:e1548Google Scholar
  81. Liu GX, Xuan N, Chu D, Xie HY, Fan ZX, Bi YP, Picimbon JF, Qin YC, Zhong ST, Li YF, Gao ZL, Pan WL, Wang GY, Rajashekar B (2014) Biotype expression and insecticide response of Bemisia tabaci chemosensory protein-1. Arch Insect Biochem Physiol 85:137–151CrossRefPubMedGoogle Scholar
  82. Liu GX, Ma HM, Xie YN, Xuan N, Xia G, Fan ZX, Rajashekar B, Arnaud P, Offmann B, Picimbon JF (2016a) Biotype characterization, developmental profiling, insecticide response and binding property of Bemisia tabaci chemosensory proteins: role of CSP in insect defense. PLoS One 11:e0154706CrossRefPubMedPubMedCentralGoogle Scholar
  83. Liu GX, Ma HM, Xie HY, Xuan N, Picimbon JF (2016b) Sequence variation of Bemisia tabaci chemosensory protein 2 in cryptic species B and Q: new DNA markers for whitefly recognition. Gene 576:284–291Google Scholar
  84. Liu GX, Arnaud P, Offmann B, Picimbon JF (2017) Genotyping and bio-sensing chemosensory proteins in insects. Sensors 17:1801CrossRefGoogle Scholar
  85. Liu GX, Yue S, Rajashekar B, Picimbon JF (2019) Expression of chemosensory protein (CSP) structures in Pediculus humanis corporis and Acinetobacter  A. baumannii. SOJ Microbiol Infect Dis in pressGoogle Scholar
  86. Lo N, Tokuda G, Watanabe H, Rose H, Staylor M, Maekawa K, Bandi C, Noda H (2000) Evidence from multiple gene sequences indicates that termites evolved from wood-feeding cockroaches. Curr Biol 10:801–804CrossRefPubMedGoogle Scholar
  87. Lombard J, López-García P, Moreira D (2012) The early evolution of lipid membranes and the three domains of life. Nat Rev Microbiol 10:507–515CrossRefPubMedGoogle Scholar
  88. Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1156CrossRefGoogle Scholar
  89. 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 217:189–196CrossRefPubMedGoogle Scholar
  90. Malhotra J, Dua A, Saxena A, Sangwan N, Mukherjee U, Pandey N, Rajagopal R, Khurana JP, Lal R (2012) Genome sequence of Acinetobacter sp. Strain HA, isolated from the gut of the polyphagous insect pest Helicoverpa armigera. J Bacterial 194:5156CrossRefGoogle Scholar
  91. Manoharan M, Ng Fuk Chong M, Vaïtinadapoulé A, Frumence E, Sowdhamini R, Offmann B (2013) Comparative genomics of odorant binding proteins in Anopheles gambiae, Aedes aegypti, and Culex quinquefasciatus. Genome Biol Evol 5:163–180CrossRefPubMedPubMedCentralGoogle Scholar
  92. 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 269:16340–16347Google Scholar
  93. Merrill CE, Riesgo-Escovar J, Pitts RJ, Kafatos FC, Carlson JR, Zwiebel LJ (2002) Visual arrestins in olfactory pathways of Drosophila and the malaria vector Anopheles gambiae. Proc Natl Acad Sci U S A 99:1633–1638CrossRefPubMedPubMedCentralGoogle Scholar
  94. Micanovic R, Raches DW, Dunbar JD, Driver DA, Bina HA, Dickinson CD, Kharitonenkov A (2009) Different roles of N- and C-termini in the functional activity of FGF21. J Cell Physiol 219:227–234CrossRefPubMedGoogle Scholar
  95. Miller SL (1953) A production of amino acids under possible primitive earth conditions. Science 117:528–529CrossRefGoogle Scholar
  96. Minard G, Mavingui P, Moro CV (2013) Diversity and function of bacterial microbiota in the mosquito holobiont. Parasit Vectors 6:146CrossRefPubMedPubMedCentralGoogle Scholar
  97. Morgan AA, Rubenstein E (2013) Proline: the distribution, frequency, positioning, and common functional roles of proline and polyproline sequences in the human proteome. PLoS One 8:e53785CrossRefPubMedPubMedCentralGoogle Scholar
  98. Nadeau VG, Deber CM (2016) Structure of impact of proline mutations in the loop region of a ancestral membrane protein. Biopolymers 37:37–42CrossRefGoogle Scholar
  99. Nardi JB, Miller LA, Walden KKO, Rovelstad S, Wang L, Frye JC, Ramsdell K, Deem LS, Robertson HM (2003) Expression patterns of odorant binding proteins in antennae of the moth Manduca sexta. Cell Tissue Res 313:321–333Google Scholar
  100. Neurath H (1984) Evolution of proteolytic enzymes. Science 224:350–357CrossRefPubMedPubMedCentralGoogle Scholar
  101. Nishiyama A, Komitova M, Suzuki R, Zhu X (2009) Polydendrocytes (NG2 cells) multifunctional cells with lineage plasticity. Nat Rev Neurosci 10:9–22CrossRefGoogle Scholar
  102. 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 36:391–398PubMedGoogle Scholar
  103. Orgel LE (1968) Evolution of the genetic apparatus. J Mol Biol 38:381–393CrossRefPubMedGoogle Scholar
  104. Ozaki M, Wada-Katsumata A, Fujikawa K, Iwasaki M, Yokohari F, Satoji Y, Nisimura T, Yamaoka R (2005) Ant nestmate and non-nestmate discrimination by a chemosensory sensillum. Science 309:311–314CrossRefPubMedGoogle Scholar
  105. Pancio HA, Vander Heyden N, Ratner L (2000) The C-terminal proline-rich tail of human immunodeficiency virus type 2 Vpx is necessary for nuclear localization of the viral preintgeration complex in nondividing cells. J Virol 74:6162–6167CrossRefPubMedPubMedCentralGoogle Scholar
  106. Payne SH, Bonissone S, Wu S, Brown R, Ivankov DN, Frishman D, Pasa-Tolic L, Smith RD, Pevsner PA (2012) Unexpected diversity of signal peptides in prokaryotes. MBio 3:e00339–e00312CrossRefPubMedPubMedCentralGoogle Scholar
  107. Pesenti ME, Spinelli S, Bezirard V, Briand L, Pernollet JC, Campanacci V, Tegoni M, Cambillau C (2009) Queen bee pheromone binding protein pH-induced domain swapping favors pheromone release. J Mol Biol 390:981–990CrossRefPubMedGoogle Scholar
  108. Picimbon JF (2003) Biochemistry and evolution of CSP and OBP proteins. In: Blomquist GJ, Vogt RG (eds) Insect pheromone biochemistry and molecular biology-the biosynthesis and detection of pheromones and plant volatiles. Elsevier Academic Press, SanDiego/London, pp 539–566Google Scholar
  109. Picimbon JF (2005) Synthesis of odorant reception-suppressing agents, odorant binding proteins (OBPs) and chemosensory proteins (CSPs): molecular target for pest management. In: Regnault-Roger C, BJR P, Vincent C (eds) Biopesticides of plant origin. Lavoiser Publishing Inc., Intercept Ltd, Hampshire/Paris/Secaucus, pp 245–266Google Scholar
  110. Picimbon JF (2014a) RNA mutations: source of life. Gene Technol 3:112–122Google Scholar
  111. Picimbon JF (2014b) RNA mutations in the moth pheromone gland. RNA Dis 1:e240Google Scholar
  112. Picimbon JF (2014c) Renaming Bombyx mori chemosensory proteins. Int J Bioorganic Chem Mol Biol 2:201–204Google Scholar
  113. Picimbon JF (2016) Mutations in the insect transcriptome. J Clin Exp Pathol 6:3Google Scholar
  114. Picimbon JF (2017) A new view of genetic mutations. Australas Med J 10:701–715CrossRefGoogle Scholar
  115. Picimbon JF (2018) Molecular mechanism of insect chemosensory systems and human totipotent stem cells: RNA and protein editing. Scene 205: cell fate determinants and stem cell biology. BIT’s 9th Annual World DNA and Genome Day (WDD-2018), DalianGoogle Scholar
  116. Picimbon JF, Leal WS (1999) Olfactory soluble proteins of cockroaches. Insect Biochem Mol Biol 29:973–978CrossRefGoogle Scholar
  117. Picimbon JF, Gadenne G (2002) Evolution in noctuid pheromone binding proteins: identification of PBP in the black cutworm moth, Agrotis ipsilon. Insect Biochem Mol Biol 32:839–846PubMedGoogle Scholar
  118. Picimbon JF, Regnault-Roger C (2008) Composés semiochimiques volatils, phytoprotection et olfaction: cibles moleculaires pour la lutte intégrée. In: Regnault-Roger C, Philogѐne BJR, Vincent C (eds) Biopesticides d’Origine Végétale, 2nd edn. Lavoisier, Paris, pp 383–415Google Scholar
  119. Picimbon JF, Dietrich K, Breer H, Krieger J (2000a) Chemosensory proteins of Locusta migratoria (Orthoptera: Acrididae). Insect Biochem Mol Biol 30:233–241CrossRefPubMedGoogle Scholar
  120. Picimbon JF, Dietrich K, Angeli S, Scaloni A, Krieger J, Breer H, Pelosi P (2000b) Purification and molecular cloning of chemosensory proteins from Bombyx mori. Arch Insect Biochem Physiol 44:120–129CrossRefPubMedGoogle Scholar
  121. Picimbon JF, Dietrich K, Krieger J, Breer H (2001) Identity and expression pattern of chemosensory proteins in Heliothis virescens (Lepidoptera, Noctuidae). Insect Biochem Mol Biol 31:1173–1181CrossRefPubMedGoogle Scholar
  122. Pikielny CW, Hasan G, Rouyer F, Rosbach M (1994) Members of a family of Drosophila putative odorant-binding proteins are expressed in different subsets of olfactory hairs. Neuron 12:35–49Google Scholar
  123. Poole AM, Phillips MJ, Penny D (2003) Prokaryote and eukaryote evolvability. Biosystems 69:163–185CrossRefPubMedGoogle Scholar
  124. Rahme LG, Ausubel FM, Cao H, Drenkard E, Goumnerov BC, Lau GW, Mahajan-Miklos S, Plotnikova J, Tan MW, Tsongalis J, Walendziewicz CL, Tompkins RG (2000) Plants and animals share functionally common bacterial virulence factors. Proc Natl Acad Sci U S A 97:8815–8821CrossRefPubMedPubMedCentralGoogle Scholar
  125. Reanney DC (1982) The evolution of RNA viruses. Annu Rev Microbiol 36:47–73CrossRefPubMedGoogle Scholar
  126. Ringstad N, Nemoto Y, De Camilli P (1997) The SH3p4/Sh3p8/SH3p13 protein family: binding partners for synaptojanin and dynamin via a Grb2-like Src homology 3 domain. Proc Natl Acad Sci U S A 5:8569–8574CrossRefGoogle Scholar
  127. Rothemund S, Liou YC, Davies PL, Sönnichsen FD (1997) Backbone structure and dynamics of a hemolymph protein from the mealworm beetle Tenebrio molitor. Biochemistry 36:13791–13801CrossRefPubMedGoogle Scholar
  128. Rothemund S, Liou YC, Davies PL, Krause E, Sönnichsen FD (1999) A new class of hexahelical insect proteins revealed as putative carriers of small hydrophobic ligands. Structure 7:1325–1332CrossRefPubMedGoogle Scholar
  129. Sabatier L, Jouanguy E, Dostert C, Zachary D, Dimarcq JL, Bulet P, Imler JL (2003) Pherokine-2 and -3: two Drosophila molecules related to pheromone/odor-binding proteins induced by viral and bacterial infections. Eur J Biol 270:3398–3407CrossRefGoogle Scholar
  130. Salem H, Kreutzer E, Sudakaran S, Kaltenpoth M (2013) Actinobacteria as essential symbionts in firebugs and cotton stainers (Hemiptera, Pyrrhocoridae). Environ Microbiol 15:1956–1968CrossRefPubMedGoogle Scholar
  131. Sandler BH, Nikonova L, Leal WS, Clardy J (2000) Sexual attraction in the silkworm moth: structure of the pheromone-binding-protein-bombykol complex. Chem Biol 7:143–151CrossRefPubMedGoogle Scholar
  132. Scaloni A, Monti M, Angeli S, Pelosi P (1999) Structural analysis and disulfide bridge pairing of two odorant binding proteins from Bombyx mori. Biochem Biophys Res Commun 266:386–391CrossRefPubMedGoogle Scholar
  133. Schymkovitz JW, Rousseau F, Wilkinson HR, Friedler A, Itzakhi LS (2001) Observation of signal transduction in three-dimensional domain swapping. Nat Struct Biol 8:888–892CrossRefGoogle Scholar
  134. Seipke RF, Kaltenpoth M, Hutchings MI (2012) Streptomyces as symbionts: an emerging and widespread theme? FEMS Microbiol Rev 36:862–875CrossRefPubMedGoogle Scholar
  135. Sheperd GM (2004) The human sense of smell: are we better than we think? PLoS Biol 2:e146CrossRefGoogle Scholar
  136. Skieterska K, Rondou P, Van Craenenbroeck K (2017) Regulation of G protein-coupled receptors by ubiquitination. Int J Mol Sci 18:923CrossRefPubMedCentralGoogle Scholar
  137. Steinbrecht RA, Laue M, Ziegelberger G (1995) Immunolocalization of pheromone-binding protein and general odorant binding protein in olfactory sensilla of the silk moths Antheraea and Bombyx. Cell Tissue Res 282:287–302CrossRefGoogle Scholar
  138. Suzuki R, Fujimoto Z, Shiotsuki T, Tsuchiya W, Momma M, Tase A, Miyazawa M, Yamazaki T (2011) Structural mechanism of JH delivery in hemolymph by JHBP of silkworm Bombyx mori. Sci Rep 1:133CrossRefPubMedPubMedCentralGoogle Scholar
  139. Tamura T, Asakura T, Uemura T, Ueda T, Terauchi K, Misaka T, Abe K (2008) Signal peptide peptidase and its homologs in Arabidopsis thaliana-plant tissue-specific expression and distinct subcellular localization. FEBS J 275:34–43CrossRefPubMedGoogle Scholar
  140. Tomaselli S, Crescenzi O, Sanfelice D, Ab E, Wechselberger R, Angeli S, Scaloni A, Boelens R, Tancredi T, Pelosi P, Picone D (2006) Solution structure of a chemosensory protein from the desert locust Schistocerca gregaria. Biochemistry 45:1606–1613CrossRefGoogle Scholar
  141. Tsitanou KE, Drakou CE, Thireou T, Gruber AV, Kythreoti G, Azem A, Fessas D, Eliopoulos E, Iatrou K, Zographos SE (2013) Crystal and solution studies of the “Plus-C” odorant-binding protein 48 from Anopheles gambiae – control of binding specificity through three-dimensional domain swapping. J Biol Chem 288:33427–33438CrossRefGoogle Scholar
  142. Vibranovski MD, Sakabe NJ, Suza SJD (2006) A possible role of exon-shuffling in the evolution of signal peptides of human proteins. FEBS Lett 580:1621–1624CrossRefPubMedGoogle Scholar
  143. Vieira FG, Sánchez-Gracia A, Rozas J (2007) Comparative genomic analysis of the odorant-binding protein family in 12 Drosophila genomes: purifying selection and birth-and-death evolution. Genome Biol 8:R235CrossRefPubMedPubMedCentralGoogle Scholar
  144. Vogel C, Bashton M, Kerrison ND, Chotia C, Teichmann SA (2004) Structure, function and evolution of multidomain proteins. Curr Opin Struct Biol 14:208–216CrossRefPubMedGoogle Scholar
  145. Vogt RG (2003) Biochemical diversity of odor detection: OBPs, ODEs and SNMPs. In: Blomquist GJ, Vogt RG (eds) Insect pheromone biochemistry and molecular biology-the biosynthesis and detection of pheromones and plant volatiles. Elsevier Academic Press, SanDiego/London, pp 391–446Google Scholar
  146. Vogt RG (2005) Molecular basis of pheromone detection in insects. In: Gilbert LI, Iatrou K, Gill S (eds) Comprehensive insect physiology, biochemistry, pharmacology and molecular biology, vol. 3. Endocrinology. Elsevier, London, pp 753–804Google Scholar
  147. Vogt RG, Riddiford LM (1981) Pheromone binding and inactivation by moth antennae. Nature 293:161–163CrossRefGoogle Scholar
  148. Vogt RG, Köhne AC, Dubnau JT, Prestwich GD (1989) Expression of pheromone binding proteins during antennal development in the gypsy moth Lymantria dispar. J Neurosci 9:332–3346CrossRefGoogle Scholar
  149. Vogt RG, Rybczynski R, Lerner MR (1991) Molecular cloning and sequencing of general odorant-binding proteins GOBP1 and GOBP2 from the tobacco hawk moth Manduca sexta: comparisons with other insect OBPs and their signal peptides. J Neurosci 11:2972–2984CrossRefPubMedGoogle Scholar
  150. Vogt RG, Rogers ME, Franco MD, Sun M (2002) A comparative study of odorant binding protein genes: differential expression of the PBP1-GOBP2 gene cluster in Manduca sexta (Lepidoptera) and the organization of OBP genes in Drosophila melanogaster (Diptera). J Exp Biol 205:719–744PubMedGoogle Scholar
  151. Wada-Katsumata A, Zurek L, Nalyanya G, Roelofs WL, Zhang A, Schal C (2015) Gut bacteria mediate aggregation in the German cockroach. Proc Natl Acad Sci U S A 112:15678–15683PubMedPubMedCentralGoogle Scholar
  152. Walter NG, Engelke DR (2002) Ribozymes: catalytic RNAs that cut things, make things, and do odd and useful jobs. Biologist (London) 49:199–203Google Scholar
  153. Wang W, Barger SW (2011) Roles of quaternary structure and cysteine residues in the activity of human serine racemase. BMC Biochem 12:1–11CrossRefGoogle Scholar
  154. Wanner KW, Isman MB, Feng Q, Plettner E, Theilmann DA (2005) Developmental expression patterns of four chemosensory protein genes from the Eastern spruce budworm, Choristoneura fumiferana. Insect Mol Biol 14:289–300CrossRefPubMedGoogle Scholar
  155. Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G, Gummienny R, Heer FT, De Beer TAP, Rempfer C, Bordoli L, Lepore R, Schwede T (2018) SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res 46:W296-W303Google Scholar
  156. Watson JD (1993) Prologue: early speculations and facts about RNA templates. In: Gesteland RF, Atkins JF (eds) The RNA world. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp xv–xxiiiGoogle Scholar
  157. Woese CR (1967) The genetic code: the molecular basis for genetic expression. Harper & Row, New York, p 186Google Scholar
  158. Wojtasek H, Leal WS (1999) Conformational change in the pheromone-binding protein from Bombyx mori induced by pH and by interaction with membranes. J Biol Chem 274:30950–30956CrossRefPubMedGoogle Scholar
  159. Wong JWH, Ho SYW, Hogg PJ (2011) Disulfide bond acquisition through eukaryotic protein evolution. Mol Biol Evol 28:327–334CrossRefPubMedGoogle Scholar
  160. Wooldridge L, Ekeruche-Makinde J, van den Berg HA, Skowera A, Miles JJ, Tan MP, Dolton G, Clement M, Liewellyn-Lacey S, Price DA, Pealman M, Sewell AK (2012) A single autoimmune T cell receptor recognizes more than a million different peptides. J Biol Chem 287:1168–1177CrossRefPubMedGoogle Scholar
  161. Xu XM, Turanov AA, Carlson BA, Yoo MH, Everley RA, Nandakumar R, Sorokina I, Gygi SP, Gladyshev VN, Hatfield DL (2010) Targeted insertion of cysteine by decoding UGA codons with mammalian selenocysteine machinery. Proc Natl Acad Sci U S A 14:21430–21434CrossRefGoogle Scholar
  162. Xuan N, Bu X, Liu YY, Yang X, Liu GX, Fan ZX, Bi YP, Yang LQ, Lou QN, Rajashekar B, Leppik G, Kasvandik S, Picimbon JF (2014) Molecular evidence of RNA editing in Bombyx chemosensory protein family. PLoS One 9:e86932CrossRefPubMedPubMedCentralGoogle Scholar
  163. Xuan N, Guo X, Xie HY, Lou QN, Bo LX, Liu GX, Picimbon JF (2015) Increased expression of CSP and CYP genes in adult silkworm females exposed to avermectins. Insect Sci 22:203–219 (INSECT SCIENCE AWARD 2017)Google Scholar
  164. Xuan N, Rajashekar B, Kasvandik S, Picimbon JF (2016) Structural components of chemosensory protein mutations in the silkworm moth, Bombyx mori. Agri Gene 2:53–58CrossRefGoogle Scholar
  165. Xuan N, Rajashekar B, Picimbon JF (2019) DNA and RNA-dependent polymerization in editing of Bombyx chemosensory protein (CSP) gene family. Agri Gene in pressGoogle Scholar
  166. Zalewska M, Kochman A, Estève JP, Lopez F, Chaoui K, Susini C, Ożyhar A, Kochman M (2009) Juvenile hormone binding protein traffic – interaction with ATP synthase and lipid transfer proteins. Biochim Biophys Acta Biomembr 1788:1695–1705CrossRefGoogle Scholar
  167. Zhou JJ, Roberson G, He X, Dufour S, Hooper AM, Pickett JA, Keep NH, Field LM (2009) Characterisation of Bombyx mori odorant-binding-proteins reveals that a general odorant-binding-protein discriminates between sex pheromone components. J Mol Biol 389:529–545CrossRefPubMedGoogle Scholar
  168. Zhu J, Ban L, Son LM, Liu Y, Pelosi P, Wang G (2016) General odorant-binding proteins and sex pheromone guide larvae of Plutella xylostella to better food. Insect Biochem Mol Biol 72:10–19CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.School of BioengineeringQILU University of TechnologyJinanPeople’s Republic of China

Personalised recommendations