Odorant-binding protein

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Odorant-binding proteins (OBPs) are small (10 to 30 kDa) soluble proteins secreted by auxiliary cells surrounding olfactory receptor neurons, including the nasal mucus of many vertebrate species and in the sensillar lymph of chemosensory sensilla of insects. OBPs are characterized by a specific protein domain that comprises six α-helices joined by three disulfide bonds. Although the function of the OBPs as a whole is not well established, it is believed that they act as odorant transporters, delivering the odorant molecules to olfactory receptors in the cell membrane of sensory neurons.

Contents

The olfactory receptors of terrestrial animals exist in an aqueous environment, yet detect odorants that are primarily hydrophobic. [1] The aqueous solubility of hydrophobic odorants is greatly enhanced via odorant-binding proteins, which exist in the extracellular fluid surrounding the odorant receptors. [1] This family is composed of pheromone binding proteins (PBP), which are male-specific and associate with pheromone-sensitive neurons and general-odorant-binding proteins (GOBP).

These proteins were initially identified on the basis of their ability to bind with moderate-affinity radioactively labeled odorants. [2] [3]

Structure

OBPs are small proteins on the order of 14 kDa in size. All odorant binding proteins are believed to have a common structure despite their genetic diversity and highly variable primary structures. [4] In vertebrates, OBPs are a part of the lipocalin family. They are structurally characterized by a β-barrel motif composed of antiparallel β-sheets. Insect OBPs share very little amino acid sequence similarity to vertebrate OBPs as they mainly contain α-helical domains. [5] [6] [7] OBPs are divergent across and within species. The percentage of conserved residues between species has been shown to be as low as 8%. [7] OBPs' have a characteristic signature that is recognized by a conserved pattern of six cysteines that are connected in the protein by three disulfide bridges. [8] Their structures have been investigated to explore new bio-inspired repellents against mosquitoes, with potentially improved OBP binding affinity, selectivity, and reduced volatility. [9] [10]

Function

The functions of odorant binding proteins as a whole is not well understood. They are generally believed to increase the solubility of hydrophobic odorants by binding them and transporting them across the aqueous sensillum lymph to receptors in the dendrites, [11] [5] [12] [13] [14] [15] and several studies support a role for OBPs in olfactory perception in vivo. [16] [17] [18] Some odorant binding proteins are hypothesized to hasten odor response termination by extracting odorant molecules from the sensillar lymph or from receptors themselves. [19] [20] Presently, just one OBP, Obp76a, has been thoroughly investigated in the olfactory system of Drosophila and has a known physiological role. [11] [14] [21] Obp76a, better known as LUSH, is located trichoid sensilla and is necessary for normal response of the odor receptor Or67d to its pheromone ligand cis-vaccenyl acetate (cVA), although responses of Or67d to cVA have been detected in the absence of Obp76a [11] [22] [23] [24] LUSH has also been found to bind cVA in vitro [21] [25] and is known to bind other insect pheromones, [26] short-chain alcohols, [27] [28] and phthalates. [29]

In 2016, Larter et al. found that the deletion of the sole abundant OBP, Obp28a, in ab8 sensilla of Drosophila does not reduce the magnitude of their olfactory responses, suggesting that Obp28a is not required for odorant transport and that ab8 sensilla do not require an abundant OBP. Their results further suggest Obp28a may be buffering changes in the odor environment, possibly as molecular gain control, which has not been previously reported for OBPs. [30]

OBPs are thought to have multiple roles besides olfaction, including reproduction, egg laying and antiinflammatory responses. [31]

Expression

OBPs are numerous and diverse. In Drosophila, they are encoded by 52 genes of the same family yet only share 20% amino acid similarity between themselves. Some are encoded by the most abundant mRNAs of the antennae. [32] [33] Within and between species, OBPs are expressed in several different tissues, including the antennal sensilla, [34] [35] [36] the taste system, and chemosensory organs. [37] [38] [35] [39] [40] They are also known to be ectopically expressed in tissues such as the gut. [15]

Genomic analysis of Drosophila and other insect species ( Anopheles gambiae , Apis mellifera, Bombyx mori , and Triboliumcastaneum ) has revealed that the OBP genes significantly differ between species. The OBP family contains 21 (in A. mellifera) to 66 genes (in A. gambiae), whereas it ranges from 52 members in Drosophila to 20 in T. castaneum. [41] [42] [43] Generally these genes are irregularly scattered across the genome. Most (69% of the OBP genes in Drosophila) are arranged in small clusters from 2 to 6 OBP genes. [43] The Drosophila OBP gene family has been classified into several subfamilies based on structural features, functional information, and phylogenetic relationships: the Classic, Minus-C, Plus-C, Dimer, PBP/GOBP, ABPI and ABPII, CRLBP, and D7 subfamilies. [43] These subfamilies are unequally distributed across arthropods, even among the dipterans and are totally absent in some species. [15]

See also

References

  1. 1 2 Vogt, R. G.; Prestwich, G. D.; Lerner, M. R. (January 1991). "Odorant-binding-protein subfamilies associate with distinct classes of olfactory receptor neurons in insects". Journal of Neurobiology. 22 (1): 74–84. doi:10.1002/neu.480220108. ISSN   0022-3034. PMID   2010751.
  2. ↑ Pelosi, P.; Baldaccini, N. E.; Pisanelli, A. M. (1982-01-01). "Identification of a specific olfactory receptor for 2-isobutyl-3-methoxypyrazine". The Biochemical Journal. 201 (1): 245–248. doi:10.1042/bj2010245. ISSN   0264-6021. PMC   1163633 . PMID   7082286.
  3. ↑ Shi, W.; Ostrov, D.A.; Gerchman, S.E.; Graziano, V.; Kycia, H.; Studier, B.; Almo, S.C.; Burley, S.K. (1999-08-25). "PNP Oxidase from Saccharomyces Cerevisiae". doi:10.2210/pdb1ci0/pdb.{{cite journal}}: Cite journal requires |journal= (help)
  4. ↑ Graham, Laurie A; Davies, Peter L (June 2002). "The odorant-binding proteins of Drosophila melanogaster : annotation and characterization of a divergent gene family". Gene. 292 (1–2): 43–55. doi: 10.1016/s0378-1119(02)00672-8 . ISSN   0378-1119. PMID   12119098.
  5. 1 2 Sandler, Benjamin H; Nikonova, Larisa; Leal, Walter S; Clardy, Jon (February 2000). "Sexual attraction in the silkworm moth: structure of the pheromone-binding-protein–bombykol complex". Chemistry & Biology. 7 (2): 143–151. doi: 10.1016/s1074-5521(00)00078-8 . ISSN   1074-5521. PMID   10662696.
  6. ↑ Lartigue, Audrey; Campanacci, Valérie; Roussel, Alain; Larsson, Anna M.; Jones, T. Alwyn; Tegoni, Mariella; Cambillau, Christian (2002-08-30). "X-ray Structure and Ligand Binding Study of a Moth Chemosensory Protein". Journal of Biological Chemistry. 277 (35): 32094–32098. doi: 10.1074/jbc.M204371200 . ISSN   0021-9258. PMID   12068017.
  7. 1 2 Tegoni, Mariella; Campanacci, Valérie; Cambillau, Christian (May 2004). "Structural aspects of sexual attraction and chemical communication in insects". Trends in Biochemical Sciences. 29 (5): 257–264. doi:10.1016/j.tibs.2004.03.003. ISSN   0968-0004. PMID   15130562.
  8. ↑ Pelosi, P. (2005-01-01). "Diversity of Odorant-binding Proteins and Chemosensory Proteins in Insects". Chemical Senses. 30 (Supplement 1): i291 –i292. doi: 10.1093/chemse/bjh229 . ISSN   0379-864X. PMID   15738163.
  9. ↑ da Costa, Kauȇ Santana; Galúcio, João Marcos; da Costa, Clauber Henrique Souza; Santana, Amanda Ruslana; dos Santos Carvalho, Vitor; do Nascimento, Lidiane Diniz; Lima e Lima, Anderson Henrique; Neves Cruz, Jorddy; Alves, Claudio Nahum; Lameira, Jerônimo (2019-12-31). "Exploring the Potentiality of Natural Products from Essential Oils as Inhibitors of Odorant-Binding Proteins: A Structure- and Ligand-Based Virtual Screening Approach To Find Novel Mosquito Repellents". ACS Omega. 4 (27): 22475–22486. doi:10.1021/acsomega.9b03157. ISSN   2470-1343. PMC   6941369 . PMID   31909330.
  10. ↑ Thireou, Trias; Kythreoti, Georgia; Tsitsanou, Katerina E.; Koussis, Konstantinos; Drakou, Christina E.; Kinnersley, Julie; Kröber, Thomas; Guerin, Patrick M.; Zhou, Jing-Jiang; Iatrou, Kostas; Eliopoulos, Elias (July 2018). "Identification of novel bioinspired synthetic mosquito repellents by combined ligand-based screening and OBP-structure-based molecular docking" . Insect Biochemistry and Molecular Biology. 98: 48–61. doi:10.1016/j.ibmb.2018.05.001. PMID   29751047. S2CID   21670580.
  11. 1 2 3 Gomez-Diaz, Carolina; Reina, Jaime H.; Cambillau, Christian; Benton, Richard (2013-04-30). "Ligands for Pheromone-Sensing Neurons Are Not Conformationally Activated Odorant Binding Proteins". PLOS Biology. 11 (4): e1001546. doi: 10.1371/journal.pbio.1001546 . ISSN   1545-7885. PMC   3640100 . PMID   23637570.
  12. ↑ Vogt, R. G.; Riddiford, L. M.; Prestwich, G. D. (1985-12-01). "Kinetic properties of a sex pheromone-degrading enzyme: the sensillar esterase of Antheraea polyphemus". Proceedings of the National Academy of Sciences. 82 (24): 8827–8831. Bibcode:1985PNAS...82.8827V. doi: 10.1073/pnas.82.24.8827 . ISSN   0027-8424. PMC   391531 . PMID   3001718.
  13. ↑ Wojtasek, Hubert; Leal, Walter S. (1999-10-22). "Conformational Change in the Pheromone-binding Protein fromBombyx mori Induced by pH and by Interaction with Membranes". Journal of Biological Chemistry. 274 (43): 30950–30956. doi: 10.1074/jbc.274.43.30950 . ISSN   0021-9258. PMID   10521490.
  14. 1 2 Xu, PingXi; Atkinson, Rachel; Jones, David N.M.; Smith, Dean P. (January 2005). "Drosophila OBP LUSH Is Required for Activity of Pheromone-Sensitive Neurons". Neuron. 45 (2): 193–200. doi: 10.1016/j.neuron.2004.12.031 . ISSN   0896-6273. PMID   15664171.
  15. 1 2 3 Vieira, Filipe G.; Rozas, Julio (2011-01-01). "Comparative Genomics of the Odorant-Binding and Chemosensory Protein Gene Families across the Arthropoda: Origin and Evolutionary History of the Chemosensory System". Genome Biology and Evolution. 3: 476–490. doi:10.1093/gbe/evr033. PMC   3134979 . PMID   21527792.
  16. ↑ Biessmann, Harald; Andronopoulou, Evi; Biessmann, Max R.; Douris, Vassilis; Dimitratos, Spiros D.; Eliopoulos, Elias; Guerin, Patrick M.; Iatrou, Kostas; Justice, Robin W. (2010-03-01). "The Anopheles gambiae Odorant Binding Protein 1 (AgamOBP1) Mediates Indole Recognition in the Antennae of Female Mosquitoes". PLOS ONE. 5 (3): e9471. Bibcode:2010PLoSO...5.9471B. doi: 10.1371/journal.pone.0009471 . ISSN   1932-6203. PMC   2830424 . PMID   20208991.
  17. ↑ Pelletier, Julien; Guidolin, Aline; Syed, Zainulabeuddin; Cornel, Anthony J.; Leal, Walter S. (2010-02-27). "Knockdown of a Mosquito Odorant-binding Protein Involved in the Sensitive Detection of Oviposition Attractants". Journal of Chemical Ecology. 36 (3): 245–248. doi:10.1007/s10886-010-9762-x. ISSN   0098-0331. PMC   2837830 . PMID   20191395.
  18. ↑ Swarup, S.; Williams, T. I.; Anholt, R. R. H. (2011-06-14). "Functional dissection of Odorant binding protein genes in Drosophila melanogaster". Genes, Brain and Behavior. 10 (6): 648–657. doi:10.1111/j.1601-183x.2011.00704.x. ISSN   1601-1848. PMC   3150612 . PMID   21605338.
  19. ↑ Vogt, Richard G.; Riddiford, Lynn M. (September 1981). "Pheromone binding and inactivation by moth antennae". Nature. 293 (5828): 161–163. Bibcode:1981Natur.293..161V. doi:10.1038/293161a0. ISSN   0028-0836. PMID   18074618. S2CID   4361816.
  20. ↑ Ziegelberger, Gunde (September 1995). "Redox-Shift of the Pheromone-Binding Protein in the Silkmoth Antheraea Polyphemus". European Journal of Biochemistry. 232 (3): 706–711. doi:10.1111/j.1432-1033.1995.tb20864.x. ISSN   0014-2956. PMID   7588707.
  21. 1 2 Laughlin, John D.; Ha, Tal Soo; Jones, David N.M.; Smith, Dean P. (June 2008). "Activation of Pheromone-Sensitive Neurons Is Mediated by Conformational Activation of Pheromone-Binding Protein". Cell. 133 (7): 1255–1265. doi:10.1016/j.cell.2008.04.046. ISSN   0092-8674. PMC   4397981 . PMID   18585358.
  22. ↑ Benton, Richard; Vannice, Kirsten S.; Vosshall, Leslie B. (2007-10-17). "An essential role for a CD36-related receptor in pheromone detection in Drosophila". Nature. 450 (7167): 289–293. Bibcode:2007Natur.450..289B. doi:10.1038/nature06328. ISSN   0028-0836. PMID   17943085. S2CID   4402715.
  23. ↑ Li, Zhengzheng; Ni, Jinfei D.; Huang, Jia; Montell, Craig (2014-09-25). "Requirement for Drosophila SNMP1 for Rapid Activation and Termination of Pheromone-Induced Activity". PLOS Genetics. 10 (9): e1004600. doi: 10.1371/journal.pgen.1004600 . ISSN   1553-7404. PMC   4177743 . PMID   25255106.
  24. ↑ van der Goes van Naters, Wynand; Carlson, John R. (April 2007). "Receptors and Neurons for Fly Odors in Drosophila". Current Biology. 17 (7): 606–612. doi:10.1016/j.cub.2007.02.043. ISSN   0960-9822. PMC   1876700 . PMID   17363256.
  25. ↑ Kruse, Schoen W; Zhao, Rui; Smith, Dean P; Jones, David N M (2003-07-27). "Structure of a specific alcohol-binding site defined by the odorant binding protein LUSH from Drosophila melanogaster". Nature Structural & Molecular Biology. 10 (9): 694–700. doi:10.1038/nsb960. ISSN   1545-9993. PMC   4397894 . PMID   12881720.
  26. ↑ Katti, S.; Lokhande, N.; González, D.; Cassill, A.; Renthal, R. (2012-11-01). "Quantitative analysis of pheromone-binding protein specificity". Insect Molecular Biology. 22 (1): 31–40. doi:10.1111/j.1365-2583.2012.01167.x. ISSN   0962-1075. PMC   3552018 . PMID   23121132.
  27. ↑ Bucci, Brigid K.; Kruse, Schoen W.; Thode, Anna B.; Alvarado, Sylvia M.; Jones, David N. M. (February 2006). "Effect ofn-Alcohols on the Structure and Stability of theDrosophilaOdorant Binding Protein LUSH†". Biochemistry. 45 (6): 1693–1701. doi:10.1021/bi0516576. ISSN   0006-2960. PMID   16460016.
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  29. ↑ Zhou, Jing-Jiang; Zhang, Guo-An; Huang, Wensheng; Birkett, Michael A; Field, Linda M; Pickett, John A; Pelosi, Paolo (2004-01-07). "Revisiting the odorant-binding protein LUSH ofDrosophila melanogaster: evidence for odour recognition and discrimination". FEBS Letters. 558 (1–3): 23–26. doi: 10.1016/s0014-5793(03)01521-7 . ISSN   0014-5793. PMID   14759510.
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  32. ↑ Hekmat-Scafe, Daria S.; Scafe, Charles R.; McKinney, Aimee J.; Tanouye, Mark A. (2002-09-01). "Genome-Wide Analysis of the Odorant-Binding Protein Gene Family in Drosophila melanogaster". Genome Research. 12 (9): 1357–1369. doi:10.1101/gr.239402. ISSN   1088-9051. PMC   186648 . PMID   12213773.
  33. ↑ Menuz, Karen; Larter, Nikki K.; Park, Joori; Carlson, John R. (2014-11-20). "An RNA-Seq Screen of the Drosophila Antenna Identifies a Transporter Necessary for Ammonia Detection". PLOS Genetics. 10 (11): e1004810. doi: 10.1371/journal.pgen.1004810 . ISSN   1553-7404. PMC   4238959 . PMID   25412082.
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  35. 1 2 Pikielny, C.W.; Hasan, G.; Rouyer, F.; Rosbash, M. (January 1994). "Members of a family of drosophila putative odorant-binding proteins are expressed in different subsets of olfactory hairs". Neuron. 12 (1): 35–49. doi:10.1016/0896-6273(94)90150-3. ISSN   0896-6273. PMID   7545907. S2CID   15776205.
  36. ↑ Schultze, Anna; Pregitzer, Pablo; Walter, Marika F.; Woods, Daniel F.; Marinotti, Osvaldo; Breer, Heinz; Krieger, Jürgen (2013-07-05). "The Co-Expression Pattern of Odorant Binding Proteins and Olfactory Receptors Identify Distinct Trichoid Sensilla on the Antenna of the Malaria Mosquito Anopheles gambiae". PLOS ONE. 8 (7): e69412. Bibcode:2013PLoSO...869412S. doi: 10.1371/journal.pone.0069412 . ISSN   1932-6203. PMC   3702612 . PMID   23861970.
  37. ↑ Galindo, K.; Smith, D. P. (November 2001). "A large family of divergent Drosophila odorant-binding proteins expressed in gustatory and olfactory sensilla". Genetics. 159 (3): 1059–1072. doi:10.1093/genetics/159.3.1059. ISSN   0016-6731. PMC   1461854 . PMID   11729153.
  38. ↑ Jeong, Yong Taek; Shim, Jaewon; Oh, So Ra; Yoon, Hong In; Kim, Chul Hoon; Moon, Seok Jun; Montell, Craig (August 2013). "An Odorant-Binding Protein Required for Suppression of Sweet Taste by Bitter Chemicals". Neuron. 79 (4): 725–737. doi:10.1016/j.neuron.2013.06.025. ISSN   0896-6273. PMC   3753695 . PMID   23972598.
  39. ↑ S., Shanbhag; S.-K., Park; C., Pikielny; R., Steinbrecht (2001-05-28). "Gustatory organs of Drosophila melanogaster : fine structure and expression of the putative odorant-binding protein PBPRP2". Cell and Tissue Research. 304 (3): 423–437. doi:10.1007/s004410100388. ISSN   0302-766X. PMID   11456419. S2CID   23354983.
  40. ↑ Park, S.-K.; Shanbhag, S. R.; Wang, Q.; Hasan, G.; Steinbrecht, R. A.; Pikielny, C. W. (2000-03-30). "Expression patterns of two putative odorant-binding proteins in the olfactory organs of Drosophila melanogaster have different implications for their functions". Cell and Tissue Research. 300 (1): 181–192. doi:10.1007/s004410050059 (inactive 1 November 2024). ISSN   0302-766X. PMID   10805087.{{cite journal}}: CS1 maint: DOI inactive as of November 2024 (link)
  41. ↑ Forêt, Sylvain; Maleszka, Ryszard (November 2006). "Function and evolution of a gene family encoding odorant binding-like proteins in a social insect, the honey bee (Apis mellifera)". Genome Research. 16 (11): 1404–1413. doi:10.1101/gr.5075706. ISSN   1088-9051. PMC   1626642 . PMID   17065610.
  42. ↑ Forêt, Sylvain; Wanner, Kevin W.; Maleszka, Ryszard (January 2007). "Chemosensory proteins in the honey bee: Insights from the annotated genome, comparative analyses and expressional profiling". Insect Biochemistry and Molecular Biology. 37 (1): 19–28. doi:10.1016/j.ibmb.2006.09.009. ISSN   0965-1748. PMID   17175443.
  43. 1 2 3 Vieira, Filipe G.; Sánchez-Gracia, Alejandro; Rozas, Julio (2007). "Comparative genomic analysis of the odorant-binding protein family in 12 Drosophila genomes: purifying selection and birth-and-death evolution". Genome Biology. 8 (11): R235. doi: 10.1186/gb-2007-8-11-r235 . ISSN   1474-760X. PMC   2258175 . PMID   18039354.
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