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A model for carrier-mediated biological signal transduction based on equilibrium ligand binding theory. (English) Zbl 1348.92060

Summary: Different variants of a mathematical model for carrier-mediated signal transduction are introduced with focus on the odor dose-electrophysiological response curve of insect olfaction. The latter offers a unique opportunity to observe experimentally the effect of an alteration in the carrier molecule composition on the signal molecule-dependent response curve. Our work highlights the role of involved carrier molecules, which have largely been ignored in mathematical models for response curves in the past. The resulting model explains how the involvement of more than one carrier molecule in signal molecule transport can cause dose-response curves as observed in experiments, without the need of more than one receptor per neuron. In particular, the model has the following features: (1) An extended sensitivity range of neuronal response is implemented by a system consisting of only one receptor but several carrier molecules with different affinities for the signal molecule. (2) Given that the sensitivity range is extended by the involvement of different carrier molecules, the model implies that a strong difference in the expression levels of the carrier molecules is absolutely essential for wide range responses. (3) Complex changes in dose-response curves which can be observed when the expression levels of carrier molecules are altered experimentally can be explained by interactions between different carrier molecules. The principles we demonstrate here for electrophysiological responses can also be applied to any other carrier-mediated biological signal transduction process. The presented concept provides a framework for modeling and statistical analysis of signal transduction processes if sufficient information on the underlying biology is available.

MSC:

92C40 Biochemistry, molecular biology
92C42 Systems biology, networks
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[1] Akera T, Cheng VJK (1977) A simple method for the determination of affinity and binding site activity in receptor binding studies. Biochim Biophys Acta-Biomembr 470(3):412-423 · doi:10.1016/0005-2736(77)90132-8
[2] Balakrishnan K, Dippel S, Wimmer E, Schütz S (2015) Odor binding proteins in the olfaction of the flour beetle Tribolium castaneum. Mitt. Dtsch.Ges.allg.angew.Ent. 20 (in press)
[3] Ben-Naim A (2001) Cooperativity and regulation in biochemical processes. Springer, Berlin · doi:10.1007/978-1-4757-3302-0
[4] Benton R, Sachse S, Michnick SW, Vosshall LB (2006) Atypical membrane topology and heteromeric function of Drosophila odorant receptors in vivo. PLoS Biol 4(2):e20 · doi:10.1371/journal.pbio.0040020
[5] Benton R, Vornice KS, Vosshall LB (2007) An essential role for a CD-36 related receptor in pheromone detection in Drosophila. Nature 450:289-293 · doi:10.1038/nature06328
[6] Biessmann H, Andronopoulou E, Biessmann MR, Douris V, Dimitratos SD, Eliopoulos E, Guerin PM, Iatrou K, Justice RW, Kröber T, Marinotti O, Tsitoura P, Woods DF, Walter MF (2010) The Anopheles gambiae odorant binding protein 1 (AgamOBP1) mediates indole recognition in the antennae of female mosquitoes. PLoS One 5(3):e9471 · doi:10.1371/journal.pone.0009471
[7] Buck L, Axel R (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65(1):175-187 · doi:10.1016/0092-8674(91)90418-X
[8] Byers JA (2013) Modeling and regression analysis of semiochemical dose-response curves of insect antennal reception and behavior. J Chem Ecol 39(8):1081-1089 · doi:10.1007/s10886-013-0328-6
[9] Byers JA (2014) Response to Martini and Habeck: Semiochemical dose-response curves fit by kinetic formation functions. J Chem Ecol 40(11-12):1165-1166 · doi:10.1007/s10886-014-0527-9
[10] Cantor CR, Schimmel PR (1980) Biophysical chemistry. Part III. The behavior of biological macromolecules, W. H, Freeman, New York
[11] Clyne PJ, Warr CG, Freeman MR, Lessing D, Kim J, Carlson JR (1999) A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22(2):327-338 · doi:10.1016/S0896-6273(00)81093-4
[12] De Bruyne M, Baker TC (2008) Odor detection in insects: volatile codes. J Chem Ecol 34(7):882-897 · doi:10.1007/s10886-008-9485-4
[13] Dippel S, Oberhofer G, Kahnt J, Gerischer L, Opitz L, Schachtner J, Stanke M, Schütz S, Wimmer E, Angeli S (2014) Tissue-specific transcriptomics, chromosomal localization, and phylogeny of chemosensory and odorant binding proteins from the red flour beetle Tribolium castaneum reveal subgroup specificities for olfaction or more general functions. BMC Genomics 15(1):1141 · doi:10.1186/1471-2164-15-1141
[14] Engsontia P, Sanderson AP, Cobb M, Walden KKO, Robertson HM, Brown S (2008) The red flour beetle’s large nose: an expanded odorant receptor gene family in Tribolium castaneum. Insect Biochem Mol Biol 38(4):387-397 · doi:10.1016/j.ibmb.2007.10.005
[15] Forstner M, Breer H, Krieger J (2009) A receptor and binding protein interplay in the detection of a distinct pheromone component in the silkmoth Antheraea polyphemus. Int J Biol Sci 5(7):745-757 · doi:10.7150/ijbs.5.745
[16] Getz WM, Lánsky P (2001) Receptor dissociation constants and the information entropy of membranes coding ligand concentration. Chem Senses 26(2):95-104 · doi:10.1093/chemse/26.2.95
[17] Hallem EA, Ho MG, Carlson JR (2004) The molecular basis of odor coding in the Drosophila antenna. Cell 117(7):965-979 · doi:10.1016/j.cell.2004.05.012
[18] Harada E, Nakagawa J, Asano T, Taoka M, Sorimachi H, Ito Y, Aigaki T, Matsuo T (2012) Functional evolution of duplicated odorant-binding protein genes, Obp57d and Obp57e Drosophila. PloS One 7(1):e29710 · doi:10.1371/journal.pone.0029710
[19] Hasselbalch K (1916) Die Berechnung der Wasserstoffzahl des Blutes aus der freien und gebundenen Kohlensäure desselben, und die Sauerstoffbindung des Blutes als Funktion der Wasserstoffzahl. Julius Springer, Berlin
[20] He P, Zhang J, Liu N, Zhang Y, Yang K, Dong S (2011) Distinct expression profiles and different functions of odorant binding proteins in Nilaparvata lugens Stål. PloS One 6(12):e28921 · doi:10.1371/journal.pone.0028921
[21] Henderson LJ (1913) The fitness of the environment. Macmillan, New York
[22] Hill TL (1985) Cooperativity theory in biochemistry: steady-state and equilibrium systems. Springer, New York
[23] Ignatious Raja JS, Katanayeva N, Katanaev VL, Galizia CG (2014) Role of Go/i subgroup of G proteins in olfactory signaling of Drosophila melanogaster. Eur J Neurosci 39(8):1245-1255 · doi:10.1111/ejn.12481
[24] Jin X, Ha TS, Smith DP (2008) SNMP is a signaling component required for pheromone sensitivity in Drosophila. PNAS 105:10996-11004 · doi:10.1073/pnas.0803309105
[25] Kaissling KE (2009) Olfactory perireceptor and receptor events in moths: a kinetic model revised. J Comp Physiol A 195(10):895-922 · doi:10.1007/s00359-009-0461-4
[26] Krauss G (2006) Biochemistry of signal transduction and regulation. Wiley, New York
[27] Krieger MJB, Ross KG (2005) Molecular evolutionary analyses of the odorant-binding protein gene Gp-9 in fire ants and other Solenopsis species. Mol Biol Evol 22(10):2090-2103 · doi:10.1093/molbev/msi203
[28] Lambert DG (2004) Drugs and receptors. Contin Educ Anaesth Crit Pain 4(6):181-184 · doi:10.1093/bjaceaccp/mkh049
[29] Leal WS (2013) Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. Annu Rev Entomol 58:373-391 · doi:10.1146/annurev-ento-120811-153635
[30] Li J, Lehmann S, Weißbecker B, Naharros IO, Schütz S, Joop G, Wimmer EA (2013) Odoriferous defensive stink gland transcriptome to identify novel genes necessary for quinone synthesis in the red flour beetle Tribolium castaneum. PloS Genet 9(7):e1003596 · doi:10.1371/journal.pgen.1003596
[31] Lummis SCR, McGonigle I, Ashby JA, Dougherty DA (2011) Two amino acid residues contribute to a cation-\[ \pi\] π binding interaction in the binding site of an insect GABA receptor. J Neurosci 31(34):12371-12376 · doi:10.1523/JNEUROSCI.1610-11.2011
[32] Lánskỳ P, Getz WM (2001) Receptor heterogeneity and its effect on sensitivity and coding range in olfactory sensory neurons. Bull Math Biol 63(5):885-908 · Zbl 1323.92047 · doi:10.1006/bulm.2001.0249
[33] Martini JWR, Habeck M (2014) Kinetics or equilibrium? A commentary on a recent simulation study of semiochemical dose-response curves of insect olfactory sensing. J Chem Ecol 40(11-12):1163-1164 · doi:10.1007/s10886-014-0526-x
[34] Martini JWR, Habeck M (2015) Comparison of the kinetics of different Markov models for ligand binding under varying conditions. J Chem Phys 142(9):094104 · doi:10.1063/1.4908531
[35] Martini JWR, Habeck M, Schlather M (2014) A derivation of the Grand Canonical Partition Function for systems with a finite number of binding sites using a Markov chain model for the dynamics of single molecules. J Math Chem 52(3):665-674 · Zbl 1311.92218 · doi:10.1007/s10910-013-0287-8
[36] Martini JWR, Schlather M, Ullmann GM (2013) On the interaction of two different types of ligands binding to the same molecule. Part I: basics and the transfer of the decoupled sites representation to systems with n and one binding sites. J Math Chem 51(2):672-695 · Zbl 1327.92077 · doi:10.1007/s10910-012-0107-6
[37] Martini JWR, Schlather M, Ullmann GM (2013) On the interaction of different types of ligands binding to the same molecule. Part II: systems with n to 2 and n to 3 binding sites. J Math Chem 51(2):696-714 · Zbl 1267.92040 · doi:10.1007/s10910-012-0108-5
[38] Martini JWR, Schlather M, Ullmann GM (2013) The meaning of the decoupled sites representation in terms of statistical mechanics and stochastics MATCH. Commun Math Comput Chem 70(3):829-850 · Zbl 1299.92022
[39] Martini JWR, Ullmann GM (2013) A mathematical view on the decoupled sites representation. J Math Biol 66(3):477-503 · Zbl 1316.92029 · doi:10.1007/s00285-012-0517-x
[40] Martini JWR, Luis D, Michael H (2015) Cooerative binding: a multiple personality. J Math Biol 72(7):1747-1774 · Zbl 1347.82009 · doi:10.1007/s00285-015-0922-z
[41] Pelletier J, Guidolin A, Syed Z, Cornel AJ, Leal WS (2010) Knockdown of a mosquito odorant-binding protein involved in the sensitive detection of oviposition attractants. J Chem Ecol 36(3):245-248 · doi:10.1007/s10886-010-9762-x
[42] Pliska V (1999) Partial agonism: mechanisms based on ligand-receptor interactions and on stimulus-response coupling. J Recept Signal Transduct 19:597-629 · doi:10.3109/10799899909036675
[43] Qiao H, He X, Schymura D, Ban L, Field L, Dani FR, Michelucci E, Caputo B, Della Torre A, Iatrou K, Zhou JJ, Krieger J, Pelosi P (2011) Cooperative interactions between odorant-binding proteins of Anopheles gambiae. Cell Mol Life Sci 68(10):1799-1813 · doi:10.1007/s00018-010-0539-8
[44] Ritz C (2010) Toward a unified approach to dose-response modeling in ecotoxicology. Environ Toxicol Chem 29(1):220-229 · doi:10.1002/etc.7
[45] Ruiz-Herrero T, Estrada J, Guantes R, Miguez DG (2013) A tunable coarse-grained model for ligand-receptor interaction. PloS Comput Biol 9(11):e1003274 · doi:10.1371/journal.pcbi.1003274
[46] Rützler M, Zwiebel LJ (2005) Molecular biology of insect olfaction: recent progress and conceptual models. J Comp Physiol A 191(9):777-790 · doi:10.1007/s00359-005-0044-y
[47] Sachse, S.; Krieger, J., No article title, Olfaction in insects. e-Neuroforum, 2, 49-60 (2011) · doi:10.1007/s13295-011-0020-7
[48] Schellman JA (1975) Macromolecular binding. Biopolymers 14:999-1018 · doi:10.1002/bip.1975.360140509
[49] Schultze A, Pregitzer P, Walter MF, Woods DF, Marinotti O, Breer H, Krieger J (2013) 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 · doi:10.1371/journal.pone.0069412
[50] Schütz S (2001) Der Einfluß verletzungsinduzierter Emissionen der Kartoffelpflanze S. tuberosum auf die geruchliche Wirtspflanzenfindung und-auswahl durch den Kartoffelkäfer L. decemlineata: Ein Biosensor für die Diagnose von Pflanzenschäden. Wissenschaftlicher Fachverlag Dr. Fleck, Wetzlar
[51] Vogt RG, Riddiford LM (1981) Pheromone binding and inactivation by moth antennae. Nature 293:161-163 · doi:10.1038/293161a0
[52] von Fragstein M, Holighaus G, Schütz S, Tscharntke T (2013) Weak defence in a tritrophic system: olfactory response to salicylaldehyde reflects prey specialization of potter wasps. Chemoecology 23(3):181-190 · doi:10.1007/s00049-013-0133-2
[53] Vosshall LB, Amrein H, Morozov PS, Rzhetsky A, Axel R (1999) A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96(5):725-736 · doi:10.1016/S0092-8674(00)80582-6
[54] Wicher D, Schäfer R, Bauernfeind R, Stensmyr MC, Heller R, Heinemann SH, Hansson BS (2008) Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels. Nature 452(7190):1007-1011 · doi:10.1038/nature06861
[55] Wyman J, Gill SJ (1990) Binding and linkage: functional chemistry of biological macromolecules. University Science Books, Mill Valley
[56] Xu P, Atkinson R, Jones DNM, Smith DP (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
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