Mas-allatotropin in the developing antennal lobe of the sphinx moth Manduca sexta: Distribution, time course, developmental regulation, and colocalization with other neuropeptides

Developmental Neurobiology

Volumn 68, Issue 1, 2008, Pages 123-142

  Utz, Sandra ^a   Huetteroth, Wolf ^a   Vömel, Matthias ^a   Schachtner, Joachim ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Hormonal regulation; Insect; Metamorphosis; Neuropeptide; Olfactory system

Indexed keywords

ALLATOTROPIN; ECDYSTERONE; MAS ALLATOTROPIN; NEUROPEPTIDE; PHENYLALANYLMETHIONYLARGINYLPHENYLALANINAMIDE; UNCLASSIFIED DRUG;

ANIMAL ANATOMY; ANIMAL TISSUE; ANTENNA; ANTENNAL LOBE; ARTICLE; CELLULAR DISTRIBUTION; HORMONAL REGULATION; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LARVA; MANDUCA SEXTA; METAMORPHOSIS; NONHUMAN; OLFACTORY DISCRIMINATION; OLFACTORY GLOMERULUS; OLFACTORY SYSTEM; PRIORITY JOURNAL; PROTEIN LOCALIZATION; TIME;

AGE FACTORS; ANIMALS; ECDYSTERONE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMAGING, THREE-DIMENSIONAL; INSECT HORMONES; MANDUCA; NERVE NET; NEURONS; NEUROPEPTIDES; SENSE ORGANS;

EID: 38149049789     PISSN: 19328451     EISSN: 1932846X     Source Type: Journal    
DOI: 10.1002/dneu.20579     Document Type: Article

References (100)

1. Abdel-Latief M, Meyering-Vos M, Hoffmann KH. 2003. Molecular characterisation of cDNAs from the fall army-worm Spodoptera frugiperda encoding Manduca sexta allatotropin and allatostatin preprohormone peptides. Insect Biochem Mol Biol 33:467-476.
2. Abdel-Latief M, Meyering-Vos M, Hoffmann KH. 2004. Expression and localization of the Spodoptera frugiperda allatotropin (Spofr-AT) and allatostatin (Spofr-AS) genes. Arch Insect Biochem Physiol 55:188-199.
3. Abercrombie M. 1946. Estimation of nuclear populations from microtome sections. Anat Rec 94:239-247.
4. Amos TM, Gelman DB, Mesce KA. 1996. Steroid hormone fluctuations regulate ganglionic fusion during metamorphosis of the moth Manduca sexta. J Insect Physiol 42:579-591.
5. Bell RA, Joachim FA. 1978. Techniques for rearing laboratory colonies of the tobacco hornworm, Manduca sexta, and pink ballworms. Ann Ent Soc Am 69:365-373.
6. Berg BG, Galizia CG, Brandt R, Mustaparta H. 2002. Digital atlases of the antennal lobe in two species of tobacco budworm moths, the Oriental Helicoverpa assulta (male) and the American Heliothis virescens (male and female). J Comp Neurol 446:123-134.
7. Berg BG, Schachtner J, Utz S, Homberg U. 2007. Distribution of neuropeptides in the primary olfactory center of the heliothine moth Heliothis virescens. Cell Tissue Res 327:385-398.
8. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
9. Caillol M, Aioun J, Baly C, Persuy MA, Salesse R. 2003. Localization of orexins and their receptors in the rat olfactory system: Possible modulation of olfactory perception by a neuropeptide synthetized centrally or locally. Brain Res 960:48-61.
10. Champlin DT, Truman JW. 1998a. Ecdysteroid control of cell proliferation during optic lobe neurogenesis in the moth Manduca sexta. Development 125:269-277.
11. Champlin DT, Truman JW. 1998b. Ecdysteroids govern two phases of eye development during metamorphosis of the moth, Manduca sexta. Development 125:2009-2018.
12. Champlin DT, Truman JW. 2000. Ecdysteroid coordinates optic lobe neurogenesis via a nitric oxide signaling pathway. Development 127:3543-2551.
13. Croll RP. 2000. Insights into early molluscan neuronal development through studies of transmitter phenotypes in embryonic pond snails. Microsc Res Tech 49:570-578.
14. De Felipe C, Pinnock RD, Hunt SP. 1995. Modulation of chemotropism in the developing spinal cord by substance P. Science 267:899-902.
15. Dubuque SH, Schachtner J, Nighorn AJ, Menon KP, Zinn K, Tolbert LP. 2001. Immunolocalization of synaptotagmin for the study of synapses in the developing antennal lobe of Manduca sexta. J Comp Neurol 441:277-287.
16. Eisthen HL. 2002. Why are olfactory systems of different animals so similar? Brain Behav Evol 59:273-293.
17. Elekonich MM, Horodyski FM. 2003. Insect allatotropins belong to a family of structurally-related myoactive peptides present in several invertebrate phyla. Peptides 24:1623-1632.
18. Ephrussi B, Beadle GW. 1936. A technique of transplantation for Drosophila. Nature 70:218-225.
19. Ewer J. 2005. Behavioral actions of neuropeptides in invertebrates: Insights from Drosophila. Horm Behav 48:418-429.
20. Grimaldi D, Engel M. 2005. Evolution of the Insects. Cambridge: Cambridge University Press.
21. Gutierrez-Mecinas M, Crespo C, Blasco-Ibanez JM, Gracia-Llanes FJ, Marques-Mari AI, Martinez-Guijarro FJ. 2005. Characterization of somatostatin- and cholecystokinin-immunoreactive periglomerular cells in the rat olfactory bulb. J Comp Neurol 489:467-479.
22. Hansel DE, Eipper BA, Ronnett GV. 2001a. Regulation of olfactory neurogenesis by amidated neuropeptides. J Neurosci Res 66:1-7.
23. Hansel DE, Eipper BA, Ronnett GV. 2001b. Neuropeptide Y functions as a neuroproliferative factor. Nature 410:940-944.
24. Higgins MR, Gibson NJ, Eckholdt PA, Nighorn A, Copenhaver PF, Nardi J, Tolbert LP. 2002. Different isoforms of fasciclin II are expressed by a subset of developing olfactory receptor neurons and by olfactory-nerve glial cells during formation of glomeruli in the moth Manduca sexta. Dev Biol 244:134-154.
25. Hildebrand JG, Rössler W, Tolbert LP. 1997. Postembryonic development of the olfactory system in the moth Manduca sexta: Primary-afferent control of glomerular development. Semin Cell Dev Biol 8:163-170.
26. Hildebrand JG, Shepherd GM. 1997. Mechanisms of olfactory discrimination: Converging evidence for common principles across phyla. Annu Rev Neurosci 20:595-631.
27. Hökfelt T. 1991. Neuropeptides in perspective: The last ten years. Neuron 7:867-879.
28. Hökfelt T, Broberger C, Xu ZQ, Sergeyev V, Ubink R, Diez M. 2000. Neuropeptides - An overview. Neuropharmacology 39:1337-1356.
29. Homberg U, Brandl C, Clynen E, Schoofs L, Veenstra JA. 2004. Mas-allatotropin/Lom-AG-myotropin-I immunostaining in the brain of the locust, Schistocerca gregaria. Cell Tissue Res 318:439-457.
30. Homberg U, Christensen TA, Hildebrand JG. 1989. Structure and function of the deutocerebrum in insects. Annu Rev Entomol 34:477-501.
31. Homberg U, Hildebrand JG. 1994. Postembryonic development of gamma-aminobutyric acid-like immunoreactivity in the brain of the sphinx moth Manduca sexta. J Comp Neurol 339:132-149.
32. B-, BPP-, and GABA-like immunoreactivity. Cell Tissue Res 259:401-419.
33. Homberg U, Montague RA, Hildebrand JG. 1988. Anatomy of antenno-cerebral pathways in the brain of the sphinx moth Manduca sexta. Cell Tissue Res 254:255-281.
34. Homberg U, Müller U. 1999. Neuroactive substances in the antennal lobe. In: Hansson BS, editor. Insect Olfaction. New York: Springer, pp 181-206.
35. Homberg U, Vitzthum H, Müller M, Binkle U. 1999. Immunocytochemistry of GABA in the central complex of the locust Schistocerca gregaria: Identification of immunoreactive neurons and colocalization with neuropeptides. J Comp Neurol 409:495-507.
36. Horodyski FM, Bhatt SR, Lee KY. 2001. Alternative splicing of transcripts expressed by the Manduca sexta allatotropin (Mas-AT) gene is regulated in a tissue-specific manner. Peptides 22:263-269.
37. Hoskins SG, Homberg U, Kingan TG, Christensen TA, Hildebrand JG. 1986. Immunocytochemistry of GABA in the antennal lobes of the sphinx moth Manduca sexta. Cell Tissue Res 244:243-252.
38. Huetteroth W, Schachtner J. 2005. Standard three-dimensional glomeruli of the Manduca sexta antennal lobe: A tool to study both developmental and adult neuronal plasticity. Cell Tissue Res 319:513-524.
39. Jindra M, Huang JY, Malone F, Asahina M, Riddiford LM. 1997. Identification and mRNA developmental profiles of two ultraspiracle isoforms in the epidermis and wings of Manduca sexta. Insect Mol Biol 6:41-53.
40. Kataoka H, Toschi A, Li JP, Carney L, Schooley DA, Kramer SJ. 1989. Identification of an allatotropin from adult Manduca sexta. Science 243:1481-1483.
41. Kent KS, Hoskins SG, Hildebrand JG. 1987. A novel serotonin- immunoreactive neuron in the antennal lobe of the sphinx moth Manduca sexta persists throughout postembryonic life. J Neurobiol 18:451-465.
42. Kingan TG, Shabanowitz J, Hunt DF, Witten JL. 1996. Characterisation of two myotropic neuropeptides in the FMRFamide family from segmental ganglia of the moth Manduca sexta: Candidate neurohormones and neuromodulators. J Exp Biol 199:1095-1104.
43. Kingan TG, Teplow DB, Phillips JM, Riehm JP, Rao KR, Hildebrand JG, Homberg U, et al. 1990. A new peptide in the FMRFamide family isolated from the CNS of the hawkmoth, Manduca sexta. Peptides 11:849-856.
44. Klagges BRE, Heimbeck G, Godenschwege TA, Hofbauer A, Pflugfelder GO, Reifegerste R, Reisch D, Schaupp M, Buchner S, Buchner E. 1996. Invertebrate Synapsins: A single gene codes for several isoforms in Drosophila. J Neurosci 16:3154-3165.
45. Lee KY, Chamberlin ME, Horodyski FM. 2002. Biological activity of Manduca sexta allatotropin-like peptides, predicted products of tissue-specific and developmentally regulated alternatively spliced mRNAs. Peptides 23:1933-1941.
46. Lehman HK, Klukas KA, Gilchrist LS, Mesce KA. 2000. Steroid regulation of octopamine expression during metamorphic development of the moth Manduca sexta. J Comp Neurol 424:283-296.
47. Levine RB. 1989. Expansion of the central arborizations of persistent sensory neurons during insect metamorphosis: The role of the steroid hormone, 20-hydroxyecdysone. J Neurosci 9:1045-1054.
48. Levine RB, Truman JW, Linn D, Bate CM. 1986. Endocrine regulation of the form and function of axonal arbors during insect metamorphosis. J Neurosci 6:293-299.
49. Lohr C. 2003. Monitoring neuronal calcium signalling using a new method for ratiometric confocal calcium imaging. Cell Calcium 34:295-303.
50. Loi PK, Tublitz NJ. 1993. Hormonal control of transmitter plasticity in insect peptidergic neurons. I. Steroid regulation of the decline in cardioacceleratory peptide 2 (CAP2) expression. J Exp Biol 181:175-194.
51. Malun D, Oland LA, Tolbert LP. 1994. Uniglomerular projection neurons participate in early development of olfactory glomeruli in the moth Manduca sexta. J Comp Neurol 350:1-22.
52. Marder E, Bucher D. 2001. Central pattern generators and the control of rhythmic movements. Curr Biol 11:R986-R996.
53. Marder E, Calabrese RL, Nusbaum MP, Trimmer B. 1987. Distribution and partial characterization of RFamide-like peptides in the stomatogastric nervous system of the rock crab, Cancer borealis, and the spiny lobster Panulirus interruptus. J Comp Neurol 259:150-163.
54. Mercer AR, Hildebrand JG. 2002. Developmental changes in the electrophysiological properties and response characteristics of Manduca antennal-lobe neurons. J Neurophysiol 87:2650-2663.
55. Mesce KA, Fahrbach SE. 2002. Integration of endocrine signals that regulate insect ecdysis. Front Neuroendocrinol 23:179-199.
56. Miao Y, Waters EM, Witten JL. 1998. Developmental and regional-specific expression of FLRFamide peptides in the tobacco hornworm, Manduca sexta, suggests functions at ecdysis. J Neurobiol 37:469-485.
57. Monsma SA, Booker R. 1996a. Genesis of the adult retina and outer optic lobes of the moth, Manduca sexta. I. Patterns of proliferation and cell death. J Comp Neurol 367:10-20.
58. Monsma SA, Booker R. 1996b. Genesis of the adult retina and outer optic lobes of the moth Manduca sexta. II. Effects of deafferentiation and developmental hormone manipulation. J Comp Neurol 367:21-35.
59. Moody TW, Merali Z. 2004. Bombesin-like peptides and associated receptors within the brain: Distribution and behavioral implications. Peptides 25:511-520.
60. Nässel DR. 2002. Neuropeptides in the nervous system of Drosophila and other insects: Multiple roles as neuromodulators and neurohormones. Prog Neurobiol 68:1-84.
61. Nässel DR, Homberg U. 2006. Neuropeptides in interneurons of the insect brain. Cell Tissue Res 326:1-24.
62. Negoescu A, Labat-Moleur F, Lorimier P, Lamarcq L, Guillermet C, Chambaz E, Brambilla E. 1994. F(ab) secondary antibodies: A general method for double immunolabeling with primary antisera from the same species. Efficiency control by chemiluminescence. J Histochem Cytochem 42:433-437.
63. Ng KL, Li JD, Cheng MY, Leslie FM, Lee AG, Zhou QY. 2005. Dependence of olfactory bulb neurogenesis on prokineticin 2 signaling. Science 308:1923-1927.
64. Nusbaum MP, Blitz DM, Swensen AM, Wood D, Marder E. 2001. The roles of co-transmission in neural network modulation. Trends Neurosci 24:146-154.
65. Oland LA, Pott WM, Bukhman G, Sun XJ, Tolbert LP. 1996. Activity blockade does not prevent the construction of olfactory glomeruli in the moth Manduca sexta. Int J Dev Neurosci 14:983-996.
66. Oland LA, Tolbert LP. 1996. Multiple factors shape development of olfactory glomeruli: Insights from an insect model system. J Neurobiol 30:92-109.
67. Petri B, Homberg U, Loesel R, Stengl M. 2002. Evidence for a role of GABA and Mas-allatotropin in photic entrainment of the circadian clock of the cockroach Leucophaea maderae. J Exp Biol 205:1459-1469.
68. Riddiford LM. 1985. Hormone action at the cellular level. In: Kerkut GA, Gilbert LI, editors. Comprehensive Insect Physiology, Biochemistry, and Pharmacology. Oxford: Pergamon, pp 37-84.
69. Schachtner J, Homberg U, Truman JW. 1999. Regulation of cyclic GMP elevation in the developing antennal lobe of the sphinx moth, Manduca sexta. J Neurobiol 41:359-375.
70. Schachtner J, Huetteroth W, Nighorn A, Honegger HW. 2004a. Copper/zinc superoxide dismutase-like immunoreactivity in the metamorphosing brain of the sphinx moth Manduca sexta. J Comp Neurol 469:141-152.
71. Schachtner J, Klaassen L, Truman JW. 1998. Metamorphic control of cyclic guanosine monophosphate expression in the nervous system of the tobacco hornworm, Manduca sexta. J Comp Neurol 396:238-252.
72. Schachtner J, Schmidt M, Homberg U. 2005. Organization and evolutionary trends of primary olfactory brain centers in Tetraconata (Crustacea + Hexapoda). Artropod Struct Dev 34:257-299.
73. Schachtner J, Trosowski B, D'Hanis W, Stubner S, Homber U. 2004b. Development and steroid regulation of RFamide immunoreactivity in antennal lobe neurons of the sphinx moth Manduca sexta. J Exp Biol 207:2389-2400.
74. Schmitt S, Evers JF, Duch C, Scholz M, Obermayer K. 2004. New methods for the computer-assisted 3D reconstruction of neurons from confocal image stacks. Neuroimage 23:1283-1298.
75. Schwartz LM, Truman JW. 1983. Hormonal control of rates of metamorphic development in the tobacco hornworm Manduca sexta. Dev Biol 99:103-114.
76. Sheng Z, Ma L, Cao MX, Li S, Jiang RJ. 2007. Biochemical and molecular characterization of allatotropin and allatostatin from the Eri silkworm, Samia cynthia ricini. Insect Biochem Mol Biol 37:90-96.
77. Smith RL, Baker H, Greer CA. 1993. Immunohistochemical analyses of the human olfactory bulb. J Comp Neurol 333:519-530.
78. Strand FL, Rose KJ, Zuccarelli LA, Kume J, Alves SE, Antonawich FJ, Garrett LY. 1991. Neuropeptide hormones as neurotrophic factors. Physiol Rev 71:1017-1046.
79. Strausfeld NJ, Hildebrand JG. 1999. Olfactory systems: Common design, uncommon origins? Curr Opin Neurobiol 9:634-639.
80. Tolbert LP. 1989. Afferent axons from the antenna influence the number and placement of intrinsic synapses in the antennal lobes of Manduca sexta. Synapse 3:83-95.
81. Tolbert LP, Matsumoto SG, Hildebrand JG. 1983. Development of synapses in the antennal lobes of the moth Manduca sexta during metamorphosis. J Neurosci 3:1158-1175.
82. Tolbert LP, Oland LA, Tucker ES, Gibson NJ, Higgins MR, Lipscomb BW. 2004. Bidirectional influences between neurons and glial cells in the developing olfactory system. Prog Neurobiol 73:73-105.
83. Truman JW. 1996a. Metamorphosis of the insect nervous system. In: Gilbert LI, editor. Metamorphosis: Postembryonic Reprogramming of Gene Expression in Amphibian and Insect Cells. Orlando: Academic Press, pp 283-320.
84. Truman JW. 1996b. Ecdysis control sheds another layer. Science 271:40-41.
85. Truman JW, Reiss SE. 1995. Neuromuscular metamorphosis in the moth Manduca sexta: Hormonal regulation of synapses loss and remodeling. J Neurosci 15:4815-4826.
86. Tublitz NJ, Loi PK. 1993. Hormonal control of transmitter plasticity in insect peptidergic neurons. II. Steroid control of the up-regulation of bursicon expression. J Exp Biol 181:195-212.
87. Utz S, Schachtner J. 2005. Development of A-type allatostatin immunoreactivity in antennal lobe neurons of the sphinx moth Manduca sexta. Cell Tissue Res 320:149-162.
88. Utz S, Huetteroth W, Wegener C, Kahnt J, Predel R, Schachtner J. 2007. Direct peptide profiling of lateral cell groups of the antennal lobes of Manduca sexta reveals specific composition changes in neuropeptide expression during development. Dev Neurobiol 67:764-777.
89. Veenstra JA, Hagedorn HH. 1993. Sensitive enzyme immunoassay for Manduca allatotropin and the existence of an allatrotropin-immunoreactive peptide in Periplaneta americana. Arch Insect Biochem Physiol 23:99-109.
90. Vilim FS, Cropper EC, Price DA, Kupfermann I, Weiss KR. 2000. Peptide cotransmitter release from motorneuron B16 in Aplysia californica: Costorage, corelease, and functional implications. J Neurosci 20:2036-2042.
91. Vitzthum H, Homberg U, Agricola H. 1996. Distribution of dip-allatostatin I-like immunoreactivity in the brain of the locust Schistocerca gregaria with detailed analysis of immunostaining in the central complex. J Comp Neurol 369:419-437.
92. Voronezhskaya EE, Elekes K. 1996. Transient and sustained expression of FMRFamide-like immunoreactivity in the developing nervous system of Lymnaea stagnalis (Mollusca, Pulmonata). Cell Mol Neurobiol 16:661-676.
93. Warren JT, Gilbert LI. 1986. Ecdysone metabolism and distribution during the pupal-adult development of Manduca sexta. Insect Biochem 16:65-82.
94. Weeks JC. 1999. Steroid hormones, dendritic remodeling and neuronal death: Insights from insect metamorphosis. Brain Behav Evol 54:51-60.
95. Weevers RD. 1966. A lepidopteran saline: The effects of inorganic cation concentrations on sensory, reflex and motor responses in a herbivorous insect. J Exp Biol 44:163-176.
96. Winther AM, Acebes A, Ferrus A. 2006. Tachykinin-related peptides modulate odor perception and locomotor activity in Drosophila. Mol Cell Neurosci 31:399-406.
97. Witten JL, Truman JW. 1996. Developmental plasticity of neuropeptide expression in motoneurons of the moth, Manduca sexta: Steroid hormone regulation. J Neurobiol 29:99-114.
98. Wright JW, Copenhaver PF. 2000. Different isoforms of fasciclin II play distinct roles in the guidance of neuronal migration during insect embryogenesis. Dev Biol 225:59-78.
99. Yacubova E, Komuro H. 2002. Stage-specific control of neuronal migration by somatostatin. Nature 415:77-81.
100. Žitňan D, Ross LS, Zitnanova I, Hermesman JL, Gill SS, Adams ME. 1999. Steroid induction of a peptide hormone gene leads to orchestration of a defined behavioral sequence. Neuron 23:523-535.