Ion transport peptide splice forms in central and peripheral neurons throughout postembryogenesis of Drosophila melanogaster

Journal of Comparative Neurology

Volumn 509, Issue 1, 2008, Pages 23-41

  Dircksen, Heinrich ^a   Tesfai, Lily Kahsai ^a   Albus, Christina ^a   Nässel, Dick R ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

Alternative splicing; Antidiuretic hormone; Fruit fly; Hindgut; Insect; Neuropeptide gene; Neurosecretory cells; Peripheral neurons

Indexed keywords

ION TRANSPORT PEPTIDE; MESSENGER RNA; NEUROPEPTIDE;

ALTERNATIVE RNA SPLICING; ANIMAL TISSUE; ARTICLE; DROSOPHILA MELANOGASTER; GENE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; ION TRANSPORT; ITP GENE; LARVA; MASS SPECTROMETER; NERVOUS SYSTEM DEVELOPMENT; NEUROSECRETORY CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CENTRAL NERVOUS SYSTEM; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ION TRANSPORT; METAMORPHOSIS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; NEURONS; PEPTIDES; PERIPHERAL NERVES; PROTEIN ISOFORMS;

EID: 45349092404     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21715     Document Type: Article

References (91)

1. Anderson MS, Halpern ME, Keshishian H. 1988. Identification of the neuropeptide transmitter proctolin in Drosophila larvae: characterization of muscle fiber-specific neuromuscular endings. J Neurosci 8:242-255.
2. Arbeitman MN, Furlong EE, Imam F, Johnson E, Null BH, Baker BS, Krasnow MA, Scott MP, Davis RW, White KP. 2002. Gene expression during the life cycle of Drosophila melanogaster. Science 297:2270-2275.
3. Audsley N, McIntosh C, Phillips JE. 1992. Isolation of a neuropeptide from locust corpus cardiacum which influences ileal transport. J Exp Biol 173:261-274.
4. Audsley N, Meredith J, Phillips JE. 2006. Haemolymph levels of Schistocerca gregaria ion transport peptide and ion transport-like peptide. Physiol Entomol 31:154-163.
5. Bader R, Colomb J, Pankratz B, Schrock A, Stocker RF, Pankratz MJ. 2007. Genetic dissection of neural circuit anatomy underlying feeding behavior in Drosophila: distinct classes of hugin-expressing neurons. J Comp Neurol 502:848-856.
6. Bainbridge SP, Bownes M. 1981. Staging the metamorphosis of Drosophila melanogaster. J Embryol Exp Morphol 66:57-80.
7. Beaudoing E, Gautheret D. 2001. Identification of alternate polyadenylation sites and analysis of their tissue distribution using EST data. Genome Res 11:1520-1526.
8. Bendtsen JD, Nielsen H, von Heijne G, Brunak S. 2004. Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783-795.
9. Böcking D, Dircksen H, Keller R. 2002. The crustacean neuropeptides of the CHH/MIH/GIH family: structures and biological activities. In: Wiese K, editor. The crustacean nervous system. Heidelberg: Springer, p 84-97.
10. Bodmer R, Jan YN. 1987. Morphological differentiation of the embryonic peripheral neurons in Drosophila. Roux Arch Dev Biol 196:69-77.
11. Chan SM, Gu PL, Chu KH, Tobe SS. 2003. Crustacean neuropeptide genes of the CHH/MIH/GIH family: implications from molecular studies. Gen Comp Endocrinol 134:214-219.
12. Chen SH, Lin CY, Kuo CM. 2004. Cloning of two crustacean hyperglycemic hormone isoforms in freshwater giant prawn (Macrobrachium rosenbergii): evidence of alternative splicing. Mar Biotechnol 6:83-94.
13. Chen SH, Lin CY, Kuo CM. 2005. In silico analysis of crustacean hyperglycemic hormone family. Mar Biotechnol 7:193-206.
14. Choi MY, Rafaeli A, Jurenka RA. 2001. Pyrokinin/PBAN-like peptides in the central nervous system of Drosophila melanogaster. Cell Tissue Res 306:459-465.
15. Chung JS, Webster SG. 1996. Does the N-terminal pyroglutamate residue have any physiological significance for crab hyperglycemic neuropeptides? Eur J Biochem 240:358-364.
16. Chung JS, Webster SG. 2004. Expression and release patterns of neuropeptides during embryonic development and hatching of the green shore crab, Carcinus maenas. Development 131:4751-4761.
17. Chung JS, Dircksen H, Webster SG. 1999. A remarkable, precisely timed release of hyperglycemic hormone from endocrine cells in the gut is associated with ecdysis in the crab Carcinus maenas. Proc Natl Acad Sci U S A 96:13103-13107.
18. Coast GM, Orchard I, Phillips JE, Schooley DA. 2002. Insect diuretic and antidiuretic hormones. Adv Insect Physiol 29:279-409.
19. Crossley AC. 1978. The morphology and development of the Drosophila muscular system. In: Asburner M, Wright TRF, editors. The genetics and biology of Drosophila. New York: Academic Press. p 499-560.
20. Dai JD, Gilbert LI. 1991. Metamorphosis of the corpus allatum and degeneration of the prothoracic glands during the larval pupal adult transformation of Drosophila melanogaster - a cytophysiological analysis of the ring gland. Dev Biol 144:309-326.
21. Dai JD, Gilbert LI. 1993. An ultrastructural and developmental analysis of the corpus allatum of juvenile-hormone deficient mutants of Drosophila melanogaster. Roux Arch Devel Biol 202:85-94.
22. Dai L, Zitnan D, Adams ME. 2007. Strategic expression of ion transport peptide gene products in central and peripheral neurons of insects. J Comp Neurol 500:353-367.
23. Davis NT, Homberg U, Dircksen H, Levine RB, Hildebrand JG. 1993. Crustacean cardioactive peptide-immunoreactive neurons in the hawk-moth Manduca sexta and changes in their immunoreactivity during postembryonic development. J Comp Neurol 338:612-627.
24. de Velasco B, Erclik T, Shy D, Sclafani J, Lipshitz H, McInnes R, Hartenstein V. 2007. Specification and development of the pars intercerebralis and pars lateralis, neuroendocrine command centers in the Drosophila brain. Dev Biol 302:309-323.
25. Dircksen H, Heyn U. 1998. Crustacean hyperglycemic hormone-like peptides in crab and locust peripheral intrinsic neurosecretory cells. Ann N Y Acad Sci 839:392-394.
26. Dircksen H, Webster SG, Keller R. 1988. Immunocytochemical demonstration of the neurosecretory systems containing putative moult-inhibiting and hyperglycemic hormone in the eyestalk of brachyuran crustaceans. Cell Tissue Res 251:3-12.
27. Dircksen H, Müller A, Keller R. 1991. Crustacean cardioactive peptide in the nervous system of the locust, Locusta migratoria: an immunocytochemical study on the ventral nerve cord and peripheral innervation. Cell Tissue Res 263:439-457.
28. Dircksen H, Böcking D, Heyn U, Mandel C, Chung JS, Baggerman G, Verhaert P, Daufeldt S, Plösch T, Jaros PP, Waelkens E, Keller R, Webster SG. 2001. Crustacean hyperglycaemic hormone (CHH)-like peptides and CHH-precursor-related peptides from pericardial organ neurosecretory cells in the shore crab, Carcinus maenas, are putatively spliced and modified products of multiple genes. Biochem J 356:159-170.
29. Drexler AL, Harris CC, Dela Pena MG, Asuncion-Uchi M, Chung S, Webster S, Fuse M. 2007. Molecular characterization and cell-specific expression of an ion transport peptide in the tobacco horn worm, Manduca sexta. Cell Tissue Res 329:391-408.
30. Dulcis D, Levine RB. 2003. Innervation of the heart of the adult fruit fly, Drosophila melanogaster. J Comp Neurol 465:560-578.
31. Dulcis D, Levine RB, Ewer J. 2005. Role of the neuropeptide CCAP in Drosophila cardiac function. J Neurobiol 64:259-274.
32. Duve H, Thorpe A. 1994. Distribution and functional significance of Leucallatostatins in the blowfly Calliphora vomitoria. Cell Tissue Res 276:367-379.
33. Eichelberg D, Wessing A, Polenz A. 1973. Structure and function of larval anal organ in Drosophila. Cytobiologie 6:410-426.
34. Endo H, Nagasawa H, Watanabe T. 2000. Isolation of a cDNA encoding a CHH-family peptide from the silkworm Bombyx mori. Insect Biochem Mol Biol 30:355-361.
35. Gloor H, Chen PS. 1950. Über ein Analorgan bei Drosophila- Larven. Rev Suisse Zool 57:570-576.
36. Gorczyca MG, Phillis RW, Budnik V. 1994. The role of tinman, a mesodermal cell fate gene, in axon pathfinding during development of the transverse nerve in Drosophila. Development 120:2143-2152.
37. Han M, Park D, Vanderzalm PJ, Mains RE, Eipper BA, Taghert PH. 2004. Drosophila uses two distinct neuropeptide amidating enzymes, dPAL1 and dPAL2. J Neurochem 90:129-141.
38. Harzsch S. 2002. The phylogenetic significance of crustacean optic neuropils and chiasmata: a re-examination. J Comp Neurol 453:10-21.
39. Harzsch S, Anger K, Dawirs RR. 1997. Immunocytochemical detection of acetylated alpha-tubulin and Drosophila synapsin in the embryonic crustacean nervous system. Int J Dev Biol 41:477-484.
40. Helfrich-Förster C. 1997. Development of pigment-dispersing hormone-immunoreactive neurons in the nervous system of Drosophila melanogaster. J Comp Neurol 380:335-354.
41. Helfrich-Förster C. 2005. Neurobiology of the fruit fly's circadian clock. Genes Brain Behav 4:65-76.
42. Helfrich-Förster C, Shafer OT, Wülbeck C, Grieshaber E, Rieger D, Taghert P. 2007. Development and morphology of the clock-gene-expressing lateral neurons of Drosophila melanogaster. J Comp Neurol 500:47-70.
43. 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.
44. Huberman A, Aguilar MB, Brew K, Shabanowitz J, Hunt DF. 1993. Primary structure of the major isomorph of the crustacean hyperglycemic hormone (CHH-I) from the sinus gland of the Mexican crayfish Procambarus bouvieri (Ortmann): interspecies comparison. Peptides 14:7-16.
45. Huybrechts J, Clynen E, De Loof A, Schoofs L. 2003. Osmotic lysis of corpora cardiaca using distilled water reveals the presence of partially processed peptides and peptide fragments. Physiol Entomol 28:46-53.
46. Jan LY, Jan YN. 1976. Properties of the larval neuromuscular junction in Drosophila melanogaster. J Physiol 262:189-214.
47. Kegel G, Reichwein B, Weese S, Gaus G, Peter-Katalinic J, Keller R. 1989. Amino acid sequence of the crustacean hyperglycemic hormone (CHH) from the shore crab, Carcinus maenas. FEBS Lett 255:10-14.
48. Kegel G, Reichwein B, Tensen CP, Keller R. 1991. Amino acid sequence of crustacean hyperglycemic hormone (CHH) from the crayfish, Orconectes limosus: emergence of a novel neuropeptide family. Peptides 12:909-913.
49. Keller R. 1988. Radioimmunoassays and ELISAs: peptides. In: Gilbert LI, Miller TA, editors. Immunological techniques in insect biology. Heidelberg: Springer. p 253-272.
50. Keller R. 1992. Crustacean neuropeptides: structures, functions and comparative aspects. Experientia 48:439-448.
51. Keller R, Kegel G, Reichwein B, Sedlmeier D, Soyez D. 1999. Biological effects of neurohormones of the CHH/MIH/GIH peptide family in crustaceans. In: Roubos EW, Wendelaar Bonga SE, Vaudry H, De Loof A, editors. Recent developments in comparative endocrinology and neurobiology. Maastricht: Shaker Publishing B.V. p 209-212.
52. Kummer G. 1993. Untersuchungen zur Bindung von hyperglykämischem Neurohormon (CHH) an Membranrezeptoren des Hepatopankreas von Carcinus maenas und Orconectes limosus [PhD thesis]. Bonn, Germany: University of Bonn. 79 p.
53. Kyhse-Andersen J. 1984. Electroblotting of multiple gels: a simple apparatus without buffer tank for rapid transfer of proteins from polyacrylamide to nitrocellulose. J Biochem Biophys Methods 10:203-209.
54. Lacombe C, Greve P, Martin G. 1999. Overview on the sub-grouping of the crustacean hyperglycemic hormone family. Neuropeptides 33:71-80.
55. Landgraf M, Sanchez-Soriano N, Technau GM, Urban J, Prokop A. 2003. Charting the Drosophila neuropile: a strategy for the standardised characterisation of genetically amenable neuntes. Dev Biol 260:207-225.
56. Macins A, Meredith J, Zhao Y, Brock HW, Phillips JE. 1999. Occurrence of ion transport peptide (ITP) and ion transport-like peptide (ITP-L) in orthopteroids. Arch Insect Biochem Physiol 40:107-118.
57. Marco HG, Gäde G. 1999. A comparative immunocytochemical study of the hyperglycaemic, moult-inhibiting and vitellogenesis-inhibiting neurohormone family in three species of decapod Crustacea. Cell Tissue Res 295:171-182.
58. Melcher C, Pankratz MJ. 2005. Candidate gustatory interneurons modulating feeding behavior in the Drosophila brain. PLoS Biol 3:e305.
59. Meredith J, Ring M, Macins A, Marschall J, Cheng NN, Theilmann D, Brock HW, Phillips JE. 1996. Locust ion transport peptide (ITP): primary structure, cDNA and expression in a baculovirus system. J Exp Biol 199:1053-1061.
60. Murakami R, Shigenaga A, Kawano E, Matsumoto A, Yamaoka I, Tanimura T. 1994. Novel tissue units of regional differentiation in the gut epithelium of Drosophila, as revealed by P-element mediated detection of enhancer. Roux Arch Dev Biol 203:243-249.
61. Nässel DR, Shiga S, Mohrherr CJ, Rao KR. 1993. Pigment-dispersing hormone-like peptide in the nervous system of the flies Phormia and Drosophila: immunocytochemistry and partial characterization. J Comp Neurol 331:183-198.
62. Nussbaum T, Dircksen H. 1995. Neuronal pathways of classical crustacean neurohormones in the central-nervous-system of the woodlouse, Oniscus asellus (L.). Philos Trans R Soc London B Biol Sci 347:139-154.
63. O'Donnell MJ, Ianowski JP, Linton SM, Rheault MR. 2003. Inorganic and organic anion transport by insect renal epithelia. BBA 1618:194-206.
64. Orth HP. 1989. In vivo-Untersuchungen zur physiologischen Funktion des hyperglykämischen Neurohormons der Crustaceen (CHH) und Studien zur Charakterisierung des CHH-Prohormons [PhD thesis]. Bonn, Germany: University of Bonn. 86 p.
65. Phillips JE, Meredith J, Wang Y, Zhao Y, Brock H. 2001. Ion transport peptide (ITP): structure, function, evolution. In: Goos HJ, Rastogi RK, Vaudry H, Pierantoni R, editors. Perspectives in comparative endocrinology: unity and diversity. Bologna, Italy: Medimond. p 745-752.
66. Ring M, Meredith J, Wiens C, Macins A, Brock HW, Phillips JE, Theilmann DA. 1998. Expression of Schistocerca gregaria ion transport peptide (ITP) and its homologue (ITP-L) in a baculovirus/insect cell system. Insect Biochem Mol Biol 28:51-58.
67. Rizki TM. 1978. The circulatory system and associated cells and tissues. In: Ashburner M, Wright TRF, editors. The genetics and biology of Drosophila. New York: Academic Press. p 397-452.
68. Sandeman D, Sandeman R, Derby D, Schmidt M. 1992. Morphology of the brain of crayfish, crabs, and spiny lobsters: a common nomenclature for homologous structures. Biol Bull 183:304-326.
69. Santama N, Benjamin PR. 2000. Gene expression and function of FMRFamide-related neuropeptides in the snail Lymnaea. Microsc Res Techniq 49:547-556.
70. Santos JG, Vömel M, Struck R, Homberg U, Nässel DR, Wegener C. 2007. Neuroarchitecture of peptidergic systems in the larval ventral ganglion of Drosophila melanogaster. PLoS ONE 2:e695.
71. Shafer OT, Helfrich-Förster C, Renn SC, Taghert PH. 2006. Reevaluation of Drosophila melanogaster's neuronal circadian pacemakers reveals new neuronal classes. J Comp Neurol 498:180-193.
72. Siegmund T, Korge G. 2001. Innervation of the ring gland of Drosophila melanogaster. J Comp Neurol 431:481-491.
73. Sinakevitch I, Douglass JK, Scholtz G, Loesel R, Strausfeld NJ. 2003. Conserved and convergent organization in the optic lobes of insects and isopods, with reference to other crustacean taxa. J Comp Neurol 467: 150-172.
74. Siviter RJ, Coast GM, Winther AME, Nachman RJ, Taylor CAM, Shirras AD, Coates D, Isaac RE, Nässel DR. 2000. Expression and functional characterization of a Drosophila neuropeptide precursor with homology to mammalian preprotachykinin A. J Biol Chem 275:23273-23280.
75. Soyez D, Laverdure AM, Kallen J, Van Herp F. 1998. Demonstration of a cell-specific isomerization of invertebrate neuropeptides. Neuroscience 82:935-942.
76. Stefanini M, De Martino C, Zamboni L. 1967. Fixation of ejaculated spermatozoa for electron microscopy. Nature 216:173-174.
77. Strausfeld NJ. 1998. Crustacean-insect relationships: the use of brain characters to derive phylogeny amongst segmented invertebrates. Brain Behav Evol 52:186-206.
78. Sullivan W, Ashburner M, Hawley RS. 2000. Drosophila protocols. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
79. Taghert PH, Carr NJ, Wall JB, Copenhaver PF. 1986. Embryonic formation of a simple neurosecretory nerve in the moth Manduca sexta. In: Borkovec AB, Gelman DB, editors. Insect neurochemistry and neurophysiology. Clifton, NJ: Humana Press. p 143-172.
80. Te Velde JH, Molthoff CFM, Scharloo W. 1988. The function of anal papillae in salt adaptation of Drosophila melanogaster larvae. J Evol Biol 1:139-153.
81. Toullec JY, Serrano L, Lopez P, Soyez D, Spanings-Pierrot C. 2006. The crustacean hyperglycemic hormones from an euryhaline crab Pachygrapsus marmoratus and a fresh water crab Potamon ibericum: eyestalk and pericardial isoforms. Peptides 27:1269-1280.
82. Towbin H, Staehlin T, Gordon J. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A 76:4350-4354.
83. Tsarouhas V, Senti KA, Jayaram SA, Tiklova K, Hemphala J, Adler J, Samakovlis C. 2007. Sequential pulses of apical epithelial secretion and endocytosis drive airway maturation in Drosophila. Dev Cell 13: 214-225.
84. Van Herp F, Van Buggenum HJ. 1979. Immunocytochemical localization of hyperglycemic hormone (HGH) in the neurosecretory system of the eyestalk of the crayfish Astacus leptodactylus. Experientia 35:1527-1529.
85. Wen T, Parrish CA, Xu D, Wu Q, Shen P. 2005. Drosophila neuropeptide F and its receptor, NPFR1, define a signaling pathway that acutely modulates alcohol sensitivity. Proc Natl Acad Sci U S A 102:2141-2146.
86. Williams DW, Shepherd D. 1999. Persistent larval sensory neurons in adult Drosophila melanogaster. J Neurobiol 39:275-286.
87. Winther AME, Siviter RJ, Isaac RE, Predel R, Nässel DR. 2003. Neuronal expression of tachykinin-related peptides and gene transcript during postembryonic development of Drosophila. J Comp Neurol 464:180-196.
88. Yasuda A, Yasuda Y, Fujita T, Naya Y. 1994. Characterization of crustacean hyperglycemic hormone from the crayfish (Procambarus clarkii): multiplicity of molecular forms by stereoinversion and diverse functions. Gen Comp Endocrinol 95:387-398.
89. Yoon JG, Stay B. 1995. Immunocytochemical localization of Diploptera punctata allatostatin-like peptide in Drosophila melanogaster. J Comp Neurol 363:475-488.
90. Zitnan D, Sehnal F, Bryant PJ. 1993. Neurons producing specific neuropeptides in the central nervous system of normal and pupariation-delayed Drosophila. Dev Biol 156:117-135.
91. Zubiaga AM, Belasco JG, Greenberg ME. 1995. The nonamer UUAUUUAUU is the key 21 AU-rich sequence motif that mediates mRNA degradation. Mol Cell Biol 15:2219-2230.