Expression of the Manduca sexta allatotropin gene in cells of the central and enteric nervous systems

Journal of Comparative Neurology

Volumn 403, Issue 3, 1999, Pages 407-420

  Bhatt, Tejal R ^a,c   Horodyski, Frank M ^b,d  

^a UNIVERSITY OF NEVADA   (United States)

^b OHIO UNIVERSITY   (United States)

^c CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^d OHIO UNIVERSITY   (United States)

Author keywords

Frontal ganglion; In situ hybridization; Juvenile hormone; Metamorphosis; Neuropeptide

Indexed keywords

ALLATOTROPHIN; JUVENILE HORMONE; NEUROPEPTIDE; UNCLASSIFIED DRUG;

ARTICLE; GENE EXPRESSION REGULATION; GROWTH REGULATION; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; METAMORPHOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN SYNTHESIS REGULATION; TISSUE DISTRIBUTION;

ANIMALS; BRAIN; DIGESTIVE SYSTEM; GANGLIA, INVERTEBRATE; IN SITU HYBRIDIZATION, FLUORESCENCE; INSECT HORMONES; MANDUCA; NERVOUS SYSTEM; NEURONS; NEUROPEPTIDES; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

EID: 0033579964     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19990118)403:3<407::AID-CNE9>3.0.CO;2-Y     Document Type: Article

References (88)

1. Amara SG, Jonas V, Rosenfeld MG, Ong ES, Evans RM. 1982. Alternative RNA processing in calcitonin gene expression generates mRNAs encoding different polypeptide products. Nature 298:240-244.
2. Amos TM, Mesce KA. 1994. Reorganization of the ventral nerve cord in the moth Manduca sexta (L.) (Lepidoptera: Sphingidae). Int J Insect Morphol Embryol 23:21-37.
3. Bell RA, Joachim FA. 1976. Techniques for rearing laboratory colonies of tobacco hornworms and pink bollworms. Ann Entomol Soc Am 69: 365-373.
4. Bellés X, Maestro JL, Piulachs MD, Johnson AH, Duve H, Thorpe A. 1994. Allatostatic neuropeptides from the cockroach Blattella germanica (L.) (Dictyoptera, Blattellidae). Identification, immunolocalization and activity. Regul Pept 53:237-247.
5. 32P labeled and unlabeled nucleic acids. Methods Enzymol 152:49-54.
6. Bhaskaran G, Jones G. 1980. Neuroendocrine regulation of corpus allatum activity in Manduca sexta: the endocrine basis for starvation-induced supernumerary larval moult. J Insect Physiol 26:431-440.
7. Bhaskaran G, Dahm KH., Barrera P, Pacheco JL, Peck KE, Muszynska-Pytel M. 1990. Allatinhibin, a neurohormonal inhibitor of juvenile hormone biosynthesis in Manduca sexta. Gen Comp Endocrinol 78: 123-136.
8. Bhatt TR, Taylor PA III, Horodyski FM. 1997. Combined fluorescence in situ hybridization and immunocytochemistry double labeling in whole-mount Manduca sexta tissue. BioTechniques 23:1000-1006.
9. Bogus MI, Cymborowski B. 1984. Induction of supernumerary moults in Galleria mellonella: evidence for an allatotropic function of the brain. J Insect Physiol 30:557-561.
10. Bogus MI, Scheller K. 1994. Identification of allatotropin-secreting cells in the brain of an insect larva. Naturwissenschaften 81:87-89.
11. Bogus M, Scheller K. 1996. Allatotropin released by the brain controls larval molting in Galleria mellonella by affecting juvenile hormone synthesis. Int J Dev Biol 40:205-210.
12. Chen Y, Veenstra J, Hagedorn H, Davis NT. 1994. Leukokinin and diuretic hormone immunoreactivity of neurons in the tobacco hornworm, Manduca sexta, and co-localization of this immunoreactivity in lateral neurosecretory cells of abdominal ganglia. Cell Tissue Res 278:493-507.
13. Copenhaver PF, Truman JW. 1986. Metamorphosis of the cerebral neuroendocrine system in the moth Manduca sexta. J Comp Neurol 249: 186-204.
14. Copenhaver PF, Taghert PH. 1989. Development of the enteric nervous system in the moth: I. Diversity of cell types and the embryonic expression of FMRFamide-related neuropeptides. Dev Biol 131:70-84.
15. Copenhaver PF, Taghert PH. 1991. Origins of the insect enteric nervous system: differentiation of the enteric ganglia from a neurogenic epithelium. Development 113:1115-1132.
16. Couillaud F, Girardie A. 1990. Disconnected corpora allata provide a novel assay for allatostimulating factors. J Exp Zool 253:330-333.
17. Davis NT, Homberg U, Dircksen H, Levine RB, Hildebrand JG. 1993. Crustacean cardioactive peptide-immunoreactive neurons in the hawkmoth Manduca sexta and changes in their immunoreactivity during postembryonic development. J Comp Neurol 338:612-627.
18. Davis NT, Veenstra J, Feyereisen R, Hildebrand JG. 1997. Allatostatin-like-immunoreactive neurons of the tobacco hornworm, Manduca sexta, and isolation and identification of a new neuropeptide related to cockroach allatostatins. J Comp Neurol 385:265-284.
19. Ding Q, Donly BC, Bendena WG. 1995. Comparison of the allatostatin neuropeptide precursors in the distantly related cockroaches Periplaneta americana and Diploptera punctata. Eur J Biochem 234:737-746.
20. Donly BC, Ding Q, Tobe S, Bendena WG. 1993. Molecular cloning of the gene for the allatostatin family of neuropeptides from the cockroach Diploptera punctata. Proc Natl Acad Sci USA 90:8807-8811.
21. Duve H, Johnsen AH, Scott AG, Yu CG, Yagi KJ, Tobe SS, Thorpe A. 1993. Callatostatins: neuropeptides from the blowfly Calliphora vomitoria with sequence homology to cockroach allatostatins. Proc Natl Acad Sci USA 90:2456-2460.
22. 3]Metcallatostatin: identification and biological properties of a novel neuropeptide from the blowfly Calliphora vomitoria. J Biol Chem 269:21059-21066.
23. East P, Tregenza K, Duve H, Thorpe A. 1996. Identification of the dipteran Leu-callatostatin peptide family: characterization of the prohormone gene from Calliphora vomitoria and Lucilia cuprina. Regul Pept 67:1-9.
24. Eipper BA, Mains RE. 1978. Analysis of the common precursor to corticotropin and endorphin. J Biol Chem 253:5732-5744.
25. Ferenz H-J, Diehl I. 1983. Stimulation of juvenile hormone biosynthesis in vitro by locust allatotropin. Z Naturforsch 38c:856-858.
26. Feyereisen R. 1985. Regulation of juvenile hormone titer: synthesis. In: Kerkut GA, Gilbert LI, editors. Comprehensive insect physiology, biochemistry and pharmacology. Vol. 7. Oxford: Pergamon Press. p 391-429.
27. Feyereisen R, Tobe SS. 1981. A rapid partition assay for routine analysis of juvenile hormone release by insect corpora allata. Anal Biochem 111:372-375.
28. Fisher JM, Sossin W, Newcomb R, Scheller RH. 1988. Multiple neuropeptides derived from a common precursor are differentially packaged and transported. Cell 54:813-822.
29. Fischer-Lougheed J, O'Shea M, Cornish I, Losberger C, Roulet E, Schulz-Aellen M-F. 1993. AKH biosynthesis: transcriptional and translational control of two co-localized prohormones. J Exp Biol 177:223-241.
30. Gadot M, Applebaum SW. 1985. Rapid in vitro activation of corpora allata by extracted locust brain allatotropic factor. Arch Insect Biochem Physiol 2:117-129.
31. Gadot M, Rafaeli A, Applebaum SW. 1987. Partial purification and characterization of locust allatotropin I. Arch Insect Biochem Physiol 4: 213-223.
32. Granger NA, Sehnal F. 1974. Regulation of corpora allata in Galleria mellonella. Nature 251:415-417.
33. Griss C, Simpson SJ, Rohrbacher J, Rowell CHF. 1991. Localization in the central nervous system of larval Manduca sexta (Lepidoptera: Sphingidae) of areas responsible for aspects of feeding behavior. J Insect Physiol 37:477-482.
34. Hammock BD. 1985. Regulation of juvenile hormone titer: degradation. In: Kerkut GA, Gilbert LI, editors. Comprehensive insect physiology, biochemistry and pharmacology. Vol. 7. Oxford: Pergamon Press. p 431-472.
35. Hebda C, Yu J-H, Bhaskaran G, Dahm KH. 1994. Reactivation of corpora allata in pharate adult Manduca sexta. J Insect Physiol 40:849-858.
36. Homberg U, Davis NT, Hildebrand JG. 1991. Peptide-immunocytochemistry of neurosecretory cells in the brain and retrocerebral complex of the sphinx moth Manduca sexta. J Comp Neurol 303:35-52.
37. Horodyski FM, Riddiford LM, Truman JW. 1989. Isolation and expression of the eclosion hormone gene from the tobacco hornworm, Manduca sexta. Proc Natl Acad Sci USA 86:8123-8127.
38. Höltke H-J, Kessler C. 1990. Non-radioactive labeling of RNA transcripts in vitro with the hapten digoxigenin (DIG): hybridization and ELISA-based detection. Nucleic Acids Res 18:5843-5851.
39. Jansons IS, Cusson M, McNeil JN, Tobe SS, Bendena WG. 1996. Molecular characterization of a cDNA from Pseudaletia unipuncta encoding the Manduca sexta allatostatin peptide (Mas-AST). Insect Biochem Mol Biol 26:767-773.
40. Kataoka H, Toschi A, Li JP, Carney RL, Schooley DA, Kramer SJ. 1989. Identification of an allatotropin from adult Manduca sexta. Science 243:1481-1483.
41. Kingan TG, Shabanowitz J, Hunt DF, Witten JL. 1996. Characterization 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.
42. Kingan TG, Žitňan D, Jaffe H, Beckage NE. 1997. Identification of neuropeptides in the midgut of parasitized insects: FLRFamides as candidate paracrines. Mol Cell Endocrinol 133:19-32.
43. Kramer SJ, Toschi A, Miller CA, Kataoka H, Quistad GB, Li JP, Carney RL, Schooley DA. 1991. Identification of an allatostatin from the tobacco hornworm Manduca sexta. Proc Natl Acad Sci USA 88:9458-9462.
44. Lange AB, Chan KK, Stay B. 1993. Effect of allatostatin and proctolin on antennal pulsatile organ muscle in the cockroach, Diploptera punctata. Arch Insect Biochem Physiol 24:79-92.
45. Lee K, Horodyski FM, Chamberlin ME. 1998. Inhibition of midgut ion transport by allatotropin (mas-AT) and Manduca FRLFamides in the tobacco hornworm, Manduca sexta. J Exp Biol (In press).
46. Lehmberg E, Ferenz H-J, Applebaum SW. 1992. Maturation and responsiveness to extracts of corpora allata from male Locusta migratoria containing allatotropic factors. Z Naturforsch 47c:449-452.
47. Mesce KA., Klukas KA, Brelje TC. 1993. Improvements for the anatomical characterization of insect neurons in whole mount: the use of cyanine-derived fluorophores and laser scanning confocal microscopy. Cell Tissue Res 271:381-397.
48. Mészáros M, Morton DB. 1996. Expression of a developmentally regulated gene, Mng10, in identified neurosecretory cells in the CNS of Manduca sexta. J Neurobiol 30:349-358.
49. Miles CI, Booker R. 1994. The role of the frontal ganglion in foregut movements of the moth, Manduca sexta. J Comp Physiol (A) 174: 755-767.
50. Moulins M, Girardie A, Girardie J. 1974. Manipulation of sexual physiology by brain stimulation in insects. Nature 250:339-340.
51. Muszynska-Pytel M. 1987. Allatotropic activity of the median neurosecretory cells of Galleria mellonella (Lepidoptera) larval brain. Experientia 43:908-909.
52. Nishiitsutsuji-Uwo J, Endo Y. 1981. Gut endocrine cells in insects: the ultrastructure of the endocrine cells in the cockroach midgut. Biomed Res 2:30-44.
53. Pratt GE, Tobe SS. 1974. Juvenile hormones radiobiosynthesized by corpora allata of adult female locusts in vitro. Life Sci 14:575-586.
54. Pratt GE, Farnsworth DE, Siegel NR, Fok KF, Feyereisen R. 1989. Identification of an allatostatin from adult Diploptera punctata. Biochem Biophys Res Commun 163:1243-1247.
55. Pratt GE, Farnsworth DE, Fok KF, Siegel NR, McCormack AL, Shabanowitz J, Hunt DF, Feyereisen R. 1991. Identity of a second type of allatostatin from cockroach brains: an octadecapeptide amide with a tyrosine-rich address sequence. Proc Natl Acad Sci USA 88:2412-2416.
56. Reichwald K, Unnithan GC, Davis NT, Agricola H, Feyereisen R. 1994. Expression of the allatostatin gene in endocrine cells of the cockroach midgut. Proc Natl Acad Sci USA 91:11894-11898.
57. Rembold H, Schlagintweit B, Ulrich GM. 1986. Activation of juvenile hormone synthesis in vitro by a corpus cardiacum factor from Locusta migratoria. J Insect Physiol 32:91-94.
58. Riddiford LM. 1994. Cellular and molecular actions of juvenile hormone: I. General considerations and premetamorphic actions. Adv Insect Physiol 24:213-274.
59. Riddiford LM, Curtis AT, Kiguchi K. 1979. Culture of the epidermis of the tobacco hornworm, Manduca sexta. Tissue Cult Assoc Man 5:975-985.
60. Riddiford LM, Hewes RS, Truman JW. 1994. Dynamics and metamorphosis of an identifiable peptidergic neuron in an insect. J Neurobiol 25: 819-830.
61. Scheller RH, Jackson JF, McAllister LB, Rothman BS, Mayeri E, Axel R. 1983. A single gene encodes multiple neuropeptides mediating a stereotyped behavior. Cell 32:7-22.
62. Sehnal F, Rembold H. 1985. Brain stimulation of juvenile hormone production in insect larvae. Experientia 41:684-685.
63. Stay B, Woodhead AP. 1993. Neuropeptide regulators of the corpora allata. Am Zool 33:357-364.
64. Stay B, Chan KK, Woodhead AP. 1992. Allatostatin-immunopositive neurons projecting to the corpora allata of adult Diploptera punctata. Cell Tissue Res 270:15-23.
65. Stay B, Tobe SS, Bendena WG. 1994. Allatostatins: identification, primary structures, functions and distribution. Adv Insect Physiol 25:267-337.
66. Taghert PH, Truman JW. 1982. Identification of the bursicon-containing neurones in abdominal ganglia of the tobacco hornworm, Manduca sexta. J Exp Biol 98:385-401.
67. Taylor PA III, Bhatt TR, Horodyski FM. 1996. Molecular characterization and expression analysis of Manduca sexta allatotropin. Eur J Biochem 239:588-596.
68. Thorn RS, Truman JW. 1994. Sexual differentiation in the CNS of the moth, Manduca sexta: I. Sex and segment-specificity in production, differentiation, and survival of the imaginal midline neurons. J Neurobiol 25:1039-1053.
69. Tobe SS, Pratt GE. 1974. The influence of substrate concentrations on the rate of juvenile hormone biosynthesis by corpora allata of the desert locust in vitro. Biochem J 144:107-113.
70. Tobe SS, Girardie J, Girardie A. 1982. Enhancement of juvenile hormone biosynthesis in locusts following electrostimulation of cerebral neurosecretory cells. J Insect Physiol 28:867-871.
71. Truman JW, Copenhaver PF. 1989. The larval eclosion hormone neurones in Manduca sexta: identification of the brain-proctodeal neurosecretory system. J Exp Biol 147:457-470.
72. Tublitz NJ, Sylwester AW. 1990. Postembryonic alteration of transmitter phenotype in individually identified peptidergic neurons. J Neurosci 10:161-168.
73. Tublitz NJ, Truman JW. 1985a. Identification of neurones containing cardioacceleratory peptides (CAPs) in the ventral nerve cord of the tobacco hawkmoth, Manduca sexta. J Exp Biol 116:395-410.
74. Tublitz NJ, Truman JW. 1985b. Insect cardioactive peptides: I. Distribution and molecular characteristics of two cardioacceleratory peptides in the tobacco hawkmoth, Manduca sexta. J Exp Biol 114:365-379.
75. 2) during wandering behavior in Manduca sexta larvae. J Exp Biol 165:241-264.
76. Unni BG, Bhaskaran G, Dahm KH, Hayes TK. 1991. Stimulation of juvenile hormone biosynthesis by analogues of a Manduca sexta allatotropin: in vitro studies. Arch Insect Biochem Physiol 17:129-142.
77. Vanden Broeck J, Veelaert D, Bendena WG, Tobe SS, De Loof A. 1996. Molecular cloning of the precursor cDNA for schistostatins, locust allatostatin-like peptides with myoinhibiting properties. Mol Cell Endocrinol 122:191-198.
78. Veelaert D, Devreese B, Schoofs L, Van Beeumen J, Vanden Broeck J, Tobe SS, De Loof A. 1996. Isolation and characterization of eight myoinhibiting peptides from the desert locust, Schistocerca gregaria: new members of the cockroach allatostatin family. Mol Cell Endocrinol 122: 183-190.
79. Veenstra JA, Lehman HK, Davis NT. 1994. Allatotropin is a cardioacceleratory peptide in Manduca sexta. J Exp Biol 188:347-354.
80. Weaver RJ, Freeman ZA, Pickering MG, Edwards JP. 1994. Identification of two allatostatins from the CNS of the cockroach Periplaneta americana: novel members of a family of neuropeptide inhibitors of insect juvenile hormone biosynthesis. Comp Biochem Physiol 107C:119-127.
81. Westbrook AL, Regan SA, Bollenbacher WE. 1993. Developmental expression of the prothoracicotropic hormone in the CNS of the tobacco hornworm. J Comp Neurol 327:1-16.
82. Woodhead AP, Stay B, Seidel SL, Khan MA, Tobe SS. 1989. Primary structure of four allatostatins: neuropeptide inhibitors of juvenile hormone synthesis. Proc Natl Acad Sci USA 86:5997-6001.
83. Woodhead AP, Asano WY, Stay B. 1993. Allatostatins in the haemolymph of Diploptera punctata and their effect in vivo. J Insect Physiol 39: 1001-1005.
84. Wyatt GR, Davey KG. 1996. Cell and molecular actions of juvenile hormone: II. Roles of juvenile hormone in adult insects. Adv Insect Physiol 26:1-155.
85. Yu CG, Stay B, Joshi S, Tobe SS. 1993. Allatostatin content of brain, corpora allata and haemolymph at different developmental stages of the cockroach, Diploptera punctata: quantitation by ELISA and bioassay. J Insect Physiol 39:111-122.
86. Yu CG, Stay B, Ding Q, Bendena WG, Tobe SS. 1995. Immunochemical identification and expression of allatostatins in the gut of Diploptera punctata. J Insect Physiol 41:1035-1043.
87. Žitňan D, Sauman I, Sehnal F. 1993. Peptidergic innervation and endocrine cells of insect midgut. Arch Insect Biochem Physiol 22:113-132.
88. Žitňan D, Kingan TG, Kramer SJ, Beckage NE. 1995. Accumulation of neuropeptides in the cerebral neurosecretory system of Manduca sexta larvae parasitized by the braconid wasp Cotesia congregata. J Comp Neurol 356:83-100.