Abstract
Immediately following the discovery of tryptophan hydroxylase in Drosophila, we demonstrated the presence of tryptophan hydroxylase in the brain of the beetle Harmonia axyridis (Coleoptera: Coccinellidae). However, whether tryptophan hydroxylase is present in the brains of other insects is still a matter of discussion. In the current study, sheep anti-tryptophan hydroxylase polyclonal antibody has been applied to test for tryptophan hydroxylase immunoreactivity in a broader taxonomic range of insect brains, including holometabolous and hemimetabolous insects: one species each of Coleoptera, Hymenoptera, Diptera, and Blattaria, and two species of Lepidoptera. All species show consistent tryptophan hydroxylase immunoreactivity with distribution patterns matching that of serotonin. The immuno-positive results of such an antibody in brains from diverse orders of insects suggest that specific tryptophan hydroxylase responsible for central serotonin synthesis is probably present in the brains of all insects.
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References
Alcaňiz S, Silva FJ (1997) Phenylalanine hydroxylase participation in the synthesis of serotonin and pteridines in Drosophila melanogaster. Comp Biochem Physiol [C] 116:205–212
Bao XX, Zheng YP, Zhang HS, Xia YZ, Song CT (1999) CP embedding agent and its application to the serial section of the body wall tissue of insects. Chinese Sci Bull 44:1021–1024
Bao XX, Tian XX, Hu XH, Zhao ZF, Qu YT, Song CT (2006) Discovery of specific tryptophan hydroxylase in the brain of the beetle Harmonia axyridis. Brain Res 1073–1074:202–208
Bender DA, Joseph MH, Kochen W, Steinhart H (1987) Progress in tryptophan and serotonin research II. Proceedings of ISTRY-86, the 5th meeting of the International Study Group for Tryptophan Research. Walter de Gruyter, Berlin
Boularand S, Biguet NF, Vidal B, Veron M, Mallet J, Vincent J, Dufour S, Vernier P (1998) Tyrosine hydroxylase in the European eel (Anguilla anguilla): cDNA cloning, brain distribution, and phylogenetic analysis. J Neurochem 71:460–470
Claassen DE, Kammer AE (1986) Effects of octopamine, dopamine and serotonin on production of flight motor output by thoracic ganglia of Manduca sexta. J Neurobiol 17:1–14
Coleman CM, Neckameyer WS (2004) Substrate regulation of serotonin and dopamine synthesis in Drosophila. Invert Neurosci 5:85–96
Coleman CM, Neckameyer WS (2005) Serotonin synthesis by two distinct enzymes in Drosophila melanogaster. Arch Insect Biochem Phys 59:12–31
Gatellier L, Nagao T, Kanzaki R (2004) Serotonin modifies the sensitivity of the male silkmoth to pheromone. J Exp Biol 207:2487–2496
Grenett HE, Ledley FD, Reed L, Woo SLC (1987) Full-length cDNA for rabbit tryptophan hydroxylase: functional domains and evolution of aromatic amino acid hydroxylases. Proc Natl Acad Sci USA 84:5530–5534
Grosmaitre X, Marion-Poll F, Renou M (2001) Biogenic amines modulate olfactory receptor neurons firing activity in Mamestra brassicae. Chem Senses 26:653–661
Hill ES, Okada K, Kanzaki R (2003) Visualization of modulatory effects of serotonin in the silkmoth antennal lobe. J Exp Biol 206:345–352
Homberg U (1994) Distribution of neurotransmitters in the insect brain. Prog Zool 40:301–306
Homberg U, Hildebrand JG (1989) Serotonin-immunoreactive neurons in the median protocerebrum and suboesophageal ganglion of the sphinx moth Manduca sexta. Cell Tissue Res 258:1–24
Kravitz EA, Edwards DH (1997) Serotonin, social status and aggression. Curr Opin Neurosci 7:812–819
Ledley FD, Grenett HE, Bartos DP, Tuinen P, Ledbetter DH, Woo SLC (1987) Assignment of human tryptophan hydroxylase locus to chromosome 11: gene duplication and translocation in evolution of aromatic amino acid hydroxylases. Somat Cell Mol Genet 13:575–580
Manastirioti M (1999) Biogenic amine systems in Drosophila melanogaster. Microsc Res Tech 45:106–121
Menzel R, Heyne A, Kinzel C, Gerber B, Fiala A (1999) Pharmacological dissociation between the reinforcing, sensitizing, and response-releasing functions of reward in honeybee classical conditioning. Behav Neurosci 113:744–754
Nässel DR (1988) Serotonin and serotonin-immunoreactive neurons in the nervous system of insects. Prog Neurobiol 30:1–85
Neckameyer WS, White K (1992) A single locus encodes both phenylalanine hydroxylase and tryptophan hydroxylase activities in Drosophila. J Biol Chem 267:4199–4206
Neckameyer WS, Coleman CM, Eadie S, Goodwin SF (2007) Compartmentalization of neuronal and peripheral serotonin synthesis in Drosophila melanogaster. Genes Brain Behav 6:1–14
Patton SJ, Luke GN, Holland PWH (1998) Complex history of a chromosomal paralogy region: insights from amphioxus aromatic amino acid hydroxylase genes and insulin-related genes. Mol Biol Evol 15:1373–1380
Saifullah ASM, Tomoika K (2002) Serotonin sets the day state in the neurons that control coupling between the optic lobe circadian pacemakers in the cricket Gryllus bimaculatus. J Exp Biol 205:1305–1314
Stevenson PA, Hofmann HA, Schoch K, Schildberger K (2000) The fight or flight responses of crickets depleted of biogenic amines. J Neurobiol 43:107–120
Stevenson PA, Dyakonova V, Rillich J, Schildberger K (2005) Octopamine and experience-dependent modulation of aggression in crickets. J Neurosci 25:1431–1441
The C. elegans Sequencing Consortium (1998) Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282:2012–2018
Walther DJ, Bader M (2003) A unique central tryptophan hydroxylase isoform. Biochem Pharmacol 66:1673–1680
Walther DJ, Peter JU, Bashammakh S, Hortnagl H, Voits M, Fink H, Bader M (2003) Synthesis of serotonin by a second tryptophan hydroxylase isoform. Science 299:76
Yuan Q, Lin F, Zheng X, Sehgal A (2005) Serotonin modulates circadian entrainment in Drosophila. Neuron 47:115–127
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We thank Samuel Beshers for assistance with editing and English.
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This work was supported by grants from the National Natural Science Foundation of China (grant no. 30470546) and the Natural Science Foundation of Jilin Province (grant no. 20030550–7).
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Bao, X., Tian, X., Zhao, Z. et al. Immunohistochemical evidence for the presence of tryptophan hydroxylase in the brains of insects as revealed by sheep anti-tryptophan hydroxylase polyclonal antibody. Cell Tissue Res 332, 555–563 (2008). https://doi.org/10.1007/s00441-008-0596-6
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DOI: https://doi.org/10.1007/s00441-008-0596-6