Disruption of aminergic signalling reveals novel compounds with distinct inhibitory effects on mosquito reproduction, locomotor function and survival

Scientific Reports

Volumn 4, Issue , 2014, Pages

  Fuchs, Silke ^a   Rende, Ermelinda ^b   Crisanti, Andrea ^a   Nolan, Tony ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF CALABRIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BIOGENIC AMINE; INSECTICIDE;

ANIMAL; ANOPHELES GAMBIAE; CHEMISTRY; DOSE RESPONSE; DRUG EFFECTS; LOCOMOTION; METABOLISM; PHYSIOLOGY; REPRODUCTION; SEXUAL BEHAVIOR; SURVIVAL RATE; TREATMENT OUTCOME;

ANIMALS; ANOPHELES GAMBIAE; BIOGENIC AMINES; DOSE-RESPONSE RELATIONSHIP, DRUG; INSECTICIDES; LOCOMOTION; REPRODUCTION; SEXUAL BEHAVIOR, ANIMAL; SURVIVAL RATE; TREATMENT OUTCOME;

EID: 84903783214     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep05526     Document Type: Article

References (86)

1. Prapanthadara, L., Hemingway, J. & Ketterman, A. J. Ddt-Resistance in Anopheles-Gambiae (Diptera, Culicidae) from Zanzibar, Tanzania, Based on Increased Ddt-Dehydrochlorinase Activity of Glutathione S-Transferases. Bull Entomol Res 85, 267-274 (1995).
2. Chandre, F. et al. Pyrethroid cross resistance spectrum among populations of Anopheles gambiae s.s. from Cote d'Ivoire. J Am Mosq Control Assoc 15, 53-9 (1999). (Pubitemid 129578050)
3. Corbel, V. et al.Multiple insecticide resistance mechanisms inAnopheles gambiae and Culex quinquefasciatus from Benin, West Africa. Acta Trop 101, 207-16 (2007). (Pubitemid 46533825)
4. Hill, C. A. et al. G protein-coupled receptors in Anopheles gambiae. Science 298, 176-8 (2002).
5. Marinissen, M. J. & Gutkind, J. S. G-protein-coupled receptors and signaling networks: emerging paradigms. Trends Pharmacol Sci 22, 368-76 (2001). (Pubitemid 32592476)
6. Taneja-Bageshwar, S. et al. Biostable agonists that match or exceed activity of native insect kinins on recombinant arthropod GPCRs. Gen Comp Endocrinol 162, 122-8 (2009).
7. Orchard, I. Octopamine in Insects - Neurotransmitter, Neurohormone, and Neuromodulator. Can J Zool 60, 659-669 (1982).
8. Fuchs, S., Behrends, V., Bundy, J. G., Crisanti, A. & Nolan, T. Phenylalanine metabolism regulates reproduction and parasite melanization in the malaria mosquito. PLoS One 9, e84865 (2014).
9. Blenau, W. & Baumann, A. Molecular and pharmacological properties of insect biogenic amine receptors: lessons from Drosophila melanogaster and Apis mellifera. Arch Insect Biochem Physiol 48, 13-38 (2001). (Pubitemid 33609258)
10. Evans, P. D. Biogenic amines in the insect nervous system. Adv. Insect Physiol 15, 317-473 (1980).
11. Usdin, E. & Sandler, M. Trace amines and the brain : proceedings of a study group held at the fourteenth Annual Meeting of the American College of Neuropsychopharmacology, San Juan, Puerto Rico. (Dekker, New York; Basel, 1976).
12. Roeder, T. Tyramine and octopamine: ruling behavior andmetabolism. Annu Rev Entomol 50, 447-77 (2005).
13. Pirri, J. K., McPherson, A. D., Donnelly, J. L., Francis, M. M. & Alkema, M. J. A tyramine-gated chloride channel coordinates distinct motor programs of a Caenorhabditis elegans escape response. Neuron 62, 526-38 (2009).
14. Haigh, A. J. B. & Gichang, M. M. The Activity of Amitraz against Infestations of Rhipicephalus-Appendiculatus. Pestic Sci 11, 674-678 (1980).
15. Elfassy, O. J., Goodman, F. W., Levy, S. A. & Carter, L. L. Efficacy of an amitrazimpregnated collar in preventing transmission of Borrelia burgdorferi by adult Ixodes scapularis to dogs. J Am Vet Med Assoc 219, 185-9 (2001). (Pubitemid 32623302)
16. Pound, J. M., Miller, J. A. & George, J. E. Efficacy of amitraz applied to white-tailed deer by the '4-poster' topical treatment device in controlling free-living lone star ticks (Acari: Ixodidae). J Med Entomol 37, 878-84 (2000).
17. Baxter, J. R. et al. Amitraz or coumaphos efficacy tests in Guatemala for control of Varroa jacobsoni Mesostigmata :Varroidae in honey bees? Southwest Entomol 24, 309-313 (1999). (Pubitemid 30057142)
18. Cossio-Bayugar, R., Miranda-Miranda, E., Padilla, V. N., Olvera-Valencia, F. & Reynaud, E. Perturbation of tyraminergic/octopaminergic function inhibits oviposition in the cattle tick Rhipicephalus (Boophilus) microplus. J Insect Physiol 58, 628-633 (2012).
19. Monastirioti, M., Linn, C. E., Jr. & White, K. Characterization of Drosophila tyramine beta-hydroxylase gene and isolation of mutant flies lacking octopamine. J Neurosci 16, 3900-11 (1996). (Pubitemid 26176054)
20. Saraswati, S., Fox, L. E., Soll, D. R. & Wu, C. F. Tyramine and octopamine have opposite effects on the locomotion of Drosophila larvae. J Neurobiol 58, 425-41 (2004). (Pubitemid 38263943)
21. Fussnecker, B. L., Smith, B. H. & Mustard, J. A. Octopamine and tyramine influence the behavioral profile of locomotor activity in the honey bee (Apis mellifera). J Insect Physiol 52, 1083-92 (2006). (Pubitemid 44634516)
22. Mustard, J. A., Pham, P. M. & Smith, B. H. Modulation of motor behavior by dopamine and the D1-like dopamine receptor AmDOP2 in the honey bee. J Insect Physiol 56, 422-430 (2010).
23. Draper, I., Kurshan, P. T., McBride, E., Jackson, F. R. & Kopin, A. S. Locomotor activity is regulated lay D2-like receptors in Drosophila: An anatomic and functional analysis. Dev Neurobiol 67, 378-393 (2007).
24. Kume, K., Kume, S., Park, S. K., Hirsh, J. & Jackson, F. R. Dopamine is a regulator of arousal in the fruit fly. J Neurosci 25, 7377-7384 (2005). (Pubitemid 41129810)
25. Erber, J., Kloppenburg, P. & Scheidler, A. Neuromodulation by Serotonin and Octopamine in the Honeybee - Behavior, Neuroanatomy and Electrophysiology. Experientia 49, 1073-1083 (1993). (Pubitemid 24011013)
26. Wright, T. R., Bewley, G. C. & Sherald, A. F. The genetics of dopa decarboxylase in Drosophila melanogaster. II. Isolation and characterization of dopadecarboxylase-deficientmutants and their relationship to the alpha-methyl-dopahypersensitive mutants. Genetics 84, 287-310 (1976).
27. Meyer, J. M. et al. A "genome-to-lead" approach for insecticide discovery: pharmacological characterization and screening of Aedes aegypti D(1)-like dopamine receptors. PLoS Negl Trop Dis 6, e1478 (2012).
28. Evans, P. D. & Maqueira, B. Insect octopamine receptors: a new classification scheme based on studies of cloned Drosophila G-protein coupled receptors. Invert Neurosci 5, 111-8 (2005). (Pubitemid 41504353)
29. Bayliss, A., Roselli, G. & Evans, P. D. A comparison of the signalling properties of two tyramine receptors from Drosophila. J Neurochem 125, 37-48 (2013).
30. Wu, S. F. et al. Two splicing variants of a novel family of octopamine receptors with different signaling properties. J Neurochem (2013).
31. Sugamori, K. S., Demchyshyn, L. L., McConkey, F., Forte, M. A. & Niznik, H. B. A primordial dopamine D1-like adenylyl cyclase-linked receptor from Drosophila melanogaster displaying poor affinity for benzazepines. FEBS Lett 362, 131-8 (1995).
32. Blenau, W., Erber, J. & Baumann, A. Characterization of a dopamine D1 receptor from Apis mellifera: Cloning, functional expression, pharmacology, and mRNA localization in the brain. J Neurochem 70, 15-23 (1998). (Pubitemid 28020823)
33. Goltsev, Y. et al. Developmental and evolutionary basis for drought tolerance of the Anopheles gambiae embryo. Dev Biol 330, 462-70 (2009).
34. Wright, T. R. The genetics of biogenic amine metabolism, sclerotization, and melanization in Drosophila melanogaster. Adv Genet 24, 127-222 (1987).
35. Cooper, R. L. & Neckameyer, W. S. Dopaminergic modulation of motor neuron activity and neuromuscular function in Drosophila melanogaster. Comp Biochem Physiol B Biochem Mol Biol 122, 199-210 (1999). (Pubitemid 29127154)
36. Evans, P. Biogenic Amine Receptors and Their Mode of Action in Insects. in Insect Neurochemistry and Neurophysiology? 1986 (eds. Bořkovec, A. & Gelman, D.) 117-141 (Humana Press, 1986).
37. Bendtsen, L., Jensen, R. & Olesen, J. Amitriptyline, a combined serotonin and noradrenaline re-uptake inhibitor, reduces exteroceptive suppression of temporal muscle activity in patients with chronic tension-type headache. Electroencephalogr Clin Neurophysiol 101, 418-22 (1996).
38. Reale, V., Hannan, F., Midgley, J. M. & Evans, P. D. The expression of a cloned Drosophila octopamine/tyramine receptor in Xenopus oocytes. Brain Res 769, 309-320 (1997). (Pubitemid 27461466)
39. Brembs, B., Christiansen, F., Pfluger, H. J. & Duch, C. Flight initiation and maintenance deficits in flies with genetically altered biogenic amine levels. J Neurosci 27, 11122-31 (2007). (Pubitemid 47574165)
40. Rodriguez-Valentin, R. et al.Oviduct contraction in Drosophila is modulated by a neural network that is both, octopaminergic and glutamatergic. J Cell Physiol 209, 183-198 (2006). (Pubitemid 44318679)
41. Orchard, I. & Lange, A. B. Evidence for octopaminergic modulation of an insect visceral muscle. J Neurobiol 16, 171-81 (1985). (Pubitemid 15073402)
42. Monastirioti, M. Distinct octopamine cell population residing in the CNS abdominal ganglion controls ovulation in Drosophila melanogaster. Dev Biol 264, 38-49 (2003). (Pubitemid 37393445)
43. Orchard, I. & Lange, A. B. Neuromuscular transmission in an insect visceral muscle. J Neurobiol 17, 359-72 (1986). (Pubitemid 16013030)
44. Cook, B. J. & Wagner, R. M. Some Pharmacological Properties of the Oviduct Muscularis of the Stable Fly Stomoxys-Calcitrans. Comp Biochem Physiol C Toxicol Pharmacol 102, 273-280 (1992).
45. Saudou, F., Amlaiky, N., Plassat, J. L., Borrelli, E. & Hen, R. Cloning and Characterization of aDrosophila Tyramine Receptor. Embo Journal 9, 3611-3617 (1990).
46. Fernandez, V. M., Giurfa, M., Devaud, J. M. & Farina, W. M. Latent inhibition in an insect: the role of aminergic signaling. Learn Mem 19, 593-7 (2012).
47. Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32, 1792-7 (2004). (Pubitemid 38832724)
48. Li, J. Y. & Christensen, B. M. Involvement of L-Tyrosine and Phenol Oxidase in the Tanning of Aedes-Aegypti Eggs. Insect Biochem and Molec Biol 23, 739-748 (1993).
49. Koller, W. C. & Rueda, M. G. Mechanism of action of dopaminergic agents in Parkinson's disease. Neurology 50, S11-4; discussion S44-8 (1998). (Pubitemid 28270373)
50. Birkmayer, W. & Hornykiewicz, O. [The L-3, 4-dioxyphenylalanine (DOPA)- effect in Parkinson-akinesia]. Wien Klin Wochenschr 73, 787-8 (1961).
51. Ostadali, M. R. et al. The Detection of Dopamine Gene Receptors (DRD1-DRD5) Expression on Human Peripheral Blood Lymphocytes by Real Time PCR. Iran J Allergy Asthma Immunol 3, 169-74 (2004).
52. Garland, E. M., Black, B. K., Harris, P. A. & Robertson, D. Dopamine-betahydroxylase in postural tachycardia syndrome. Am J Physiol Heart Circ Physiol 293, H684-H690 (2007).
53. Vickers, S. et al.Metabolism of carbidopa (1-(-)-alpha-hydrazino-3, 4-dihydroxyalpha-methylhydrocinnamic acid monohydrate), an aromatic amino acid decarboxylase inhibitor, in the rat, rhesus monkey, and man. Drug Metab Dispos 2, 9-22 (1974).
54. Sideri, M., Tsakas, S., Markoutsa, E., Lampropoulou, M. & Marmaras, V. J. Innate immunity in insects: surface-associated dopa decarboxylase- dependent pathways regulate phagocytosis, nodulation and melanization in medfly haemocytes. Immunology 123, 528-37 (2008). (Pubitemid 351280966)
55. Hearn, M. G. et al. A Drosophila dopamine 2-like receptor: Molecular characterization and identification of multiple alternatively spliced variants. Proc Natl Acad Sci U S A 99, 14554-9 (2002). (Pubitemid 35257709)
56. Cazzamali, G., Klaerke, D. A. & Grimmelikhuijzen, C. J. A new family of insect tyramine receptors. Biochem Biophys Res Commun 338, 1189-96 (2005). (Pubitemid 41597763)
57. Kleinau, G. et al. Differential modulation of Beta-adrenergic receptor signaling by trace amine-associated receptor 1 agonists. PLoS One 6, e27073 (2011).
58. Robb, S. et al. Agonist-Specific Coupling of a Cloned Drosophila Octopamine Tyramine Receptor to Multiple 2nd Messenger Systems. Embo Journal 13, 1325-1330 (1994). (Pubitemid 24090213)
59. Carpene, C. et al. Selective activation of beta3-adrenoceptors by octopamine: comparative studies in mammalian fat cells. Naunyn Schmiedebergs Arch Pharmacol 359, 310-21 (1999). (Pubitemid 29210962)
60. Wang, X.M., Zhang, Z. J., Bains, R. & Mokha, S. S. Effect of antisense knock-down of alpha(2a)- and alpha(2c)-adrenoceptors on the antinociceptive action of clonidine on trigeminal nociception in the rat. Pain 98, 27-35 (2002). (Pubitemid 34722466)
61. Hiripi, L., Juhos, S. & Downer, R. G. Characterization of tyramine and octopamine receptors in the insect (Locusta migratoria migratorioides) brain. Brain Res 633, 119-26 (1994).
62. Millan, M. J. et al. Agonist and antagonist actions of yohimbine as compared to fluparoxan at alpha(2)-adrenergic receptors (AR)s, serotonin (5-HT)(1A), 5- HT(1B), 5-HT(1D) and dopamine D(2) and D(3) receptors. Significance for the modulation of frontocortical monoaminergic transmission and depressive states. Synapse 35, 79-95 (2000). (Pubitemid 30036185)
63. Colas, J. F., Launay, J. M., Kellermann, O., Rosay, P. & Maroteaux, L. Drosophila 5- HT2 serotonin receptor: coexpression with fushi-tarazu during segmentation. Proc Natl Acad Sci U S A 92, 5441-5 (1995).
64. Rotte, C. et al. Molecular characterization and localization of the first tyramine receptor of the American cockroach (Periplaneta americana). Neuroscience 162, 1120-33 (2009).
65. Scheer, A., Fanelli, F., Costa, T., De Benedetti, P. G. & Cotecchia, S. The activation process of the alpha1B-adrenergic receptor: potential role of protonation and hydrophobicity of a highly conserved aspartate. Proc Natl Acad Sci U S A 94, 808-13 (1997).
66. Saudou, F., Boschert, U., Amlaiky, N., Plassat, J. L. & Hen, R. A family of Drosophila serotonin receptors with distinct intracellular signalling properties and expression patterns. EMBO J 11, 7-17 (1992).
67. Berthelsen, S. & Pettinger, W. A. A functional basis for classification of alphaadrenergic receptors. Life Sci 21, 595-606 (1977). (Pubitemid 8189368)
68. Evans, P. D. Multiple receptor types for octopamine in the locust. J Physiol 318, 99-122 (1981). (Pubitemid 11059722)
69. Frances, H., Poncelet, M., Danti, S., Goldschmidt, P. & Simon, P. Psychopharmacological Profile of Clenbuterol. Drug Develop Res 3, 349-356 (1983). (Pubitemid 13002243)
70. Williams, R. S. & Bishop, T. Selectivity of dobutamine for adrenergic receptor subtypes: in vitro analysis by radioligand binding. J Clin Invest 67, 1703-11 (1981). (Pubitemid 11127562)
71. Abrahamsson, T. Characterization of the beta 1-adrenoceptor stimulatory effects of the partial beta 1-agonists acebutolol, xamoterol, H142/08 and H201/70. Eur J Pharmacol 164, 121-8 (1989). (Pubitemid 19123488)
72. Juberg, E. N., Minneman, K. P. & Abel, P. W. Beta 1- and beta 2-adrenoceptor binding and functional response in right and left atria of rat heart. Naunyn Schmiedebergs Arch Pharmacol 330, 193-202 (1985). (Pubitemid 15003579)
73. Vaishnavi, S. N. et al.Milnacipran: a comparative analysis of human monoamine uptake and transporter binding affinity. Biol Psychiatry 55, 320-2 (2004). (Pubitemid 38117171)
74. Gould, G. G., Altamirano, A. V., Javors, M. A. & Frazer, A. A comparison of the chronic treatment effects of venlafaxine and other antidepressants on serotonin and norepinephrine transporters. Biol Psychiatry 59, 408-14 (2006). (Pubitemid 43289219)
75. Cusack, B., Nelson, A. & Richelson, E. Binding of antidepressants to human brain receptors: focus on newer generation compounds. Psychopharmacology (Berl) 114, 559-65 (1994). (Pubitemid 24152135)
76. Jang, S. W. et al. Amitriptyline is a TrkA and TrkB receptor agonist that promotes TrkA/TrkB heterodimerization and has potent neurotrophic activity. Chem Biol 16, 644-56 (2009).
77. Tatsumi, M., Groshan, K., Blakely, R. D. & Richelson, E. Pharmacological profile of antidepressants and related compounds at human monoamine transporters. Eur J Pharmacol 340, 249-258 (1997). (Pubitemid 28022649)
78. Chipkin, R. E. et al. Pharmacological Profile of Sch39166 - a Dopamine D1 Selective Benzonaphthazepine with Potential Antipsychotic Activity. J Pharmacol ExpTher 247, 1093-1102 (1988). (Pubitemid 19022121)
79. Setler, P. E., Sarau, H. M., Zirkle, C. L. & Saunders, H. L. The central effects of a novel dopamine agonist. Eur J Pharmacol 50, 419-30 (1978). (Pubitemid 9212897)
80. Freedman, S. B. et al. Expression and pharmacological characterization of the human D3 dopamine receptor. J Pharmacol Exp Ther 268, 417-26 (1994). (Pubitemid 24039117)
81. Heykants, J. et al. On the pharmacokinetics of domperidone in animals and man. IV. The pharmacokinetics of intravenous domperidone and its bioavailability in man following intramuscular, oral and rectal administration. Eur J Drug Metab Pharmacokinet 6, 61-70 (1981). (Pubitemid 11104424)
82. Kvernmo, T., Houben, J. & Sylte, I. Receptor-binding and pharmacokinetic properties of dopaminergic agonists. Curr Top Med Chem 8, 1049-67 (2008).
83. Davis, J. P. & Pitman, R. M. Characterization of receptors mediating the actions of dopamine on an identified inhibitory motoneurone of the cockroach. J Exp Biol 155, 203-17 (1991).
84. Tricklebank, M. D., Forler, C., Middlemiss, D.N. & Fozard, J. R. Subtypes of the 5- HT receptor mediating the behavioural responses to 5-methoxy-N, Ndimethyltryptamine in the rat. Eur J Pharmacol 117, 15-24 (1985). (Pubitemid 16204495)
85. Van Nueten, J. M. et al. Vascular effects of ketanserin (R 41 468), a novel antagonist of 5-HT2 serotonergic receptors. J Pharmacol Exp Ther 218, 217-30 (1981). (Pubitemid 11033743)
86. Chen, F. et al. Characterization of an allosteric citalopram-binding site at the serotonin transporter. J Neurochem 92, 21-8 (2005). (Pubitemid 40193506)