The antidiuretic neurohormone RhoprCAPA-2 downregulates fluid transport across the anterior midgut in the blood-feeding insect Rhodnius prolixus

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 298, Issue 3, 2010, Pages

  Ianowski, Juan P ^a,b   Paluzzi, Jean Paul ^a   Te Brugge, Victoria A ^a   Orchard, Ian ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

cAMP; cGMP; Ion transport; Neuropeptide; Serotonin; Ussing chamber

Indexed keywords

ANTIDIURETIC AGENT; CALCIUM ION; CYCLIC GMP; NEUROHORMONE; RHOPRCAPA 2; SEROTONIN; UNCLASSIFIED DRUG;

ANTIDIURESIS; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFECT; DRUG MECHANISM; FLUID TRANSPORT; HEMOLYMPH; INTRACELLULAR SPACE; MALPIGHIAN TUBULE; MIDGUT; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RHODNIUS PROLIXUS; TRIATOMINAE;

8-BROMO CYCLIC ADENOSINE MONOPHOSPHATE; ANIMALS; BLOOD; CYCLIC GMP; DIURESIS; DOWN-REGULATION; FEMALE; GASTROINTESTINAL TRACT; HEMOLYMPH; INSECT HORMONES; MALE; MALPIGHIAN TUBULES; NEUROPEPTIDES; RHODNIUS; SEROTONIN; VASOPRESSINS; WATER-ELECTROLYTE BALANCE;

EID: 77749306175     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00208.2009     Document Type: Article

References (61)

1. Audsley N, Mclntosh C, Phillips JE. Isolation of a neuropeptide from locust corpus cardiacum which influences ileal transport. J Exp Biol 173: 261-274, 1992.
2. Audsley N, Mclntosh C, Phillips JE, Schooley DA, Coast GM. Neuropeptide regulation of ion and fluid reabsorption in the insect excretory system. In: Perspectives in Comparative Endocrinology, edited by Davey KG, Peter RE, and Tobe SS. Ottawa, Canada: National Research Council of Canada, 1994, p. 74-80.
3. +-ATPase in electrogenesis and epithelial transport in Malpighian tubules. J Exp Biol 203: 1459-1468, 2000.
4. Blumenthal EM. Regulation of chloride permeability by endogenously produced tyramine in Drosophila Malpighian tubule. Am J Physiol Cell Physiol 284: C718-C728, 2003.
5. Broderick KE, MacPherson MR, Regulski M, Tully T, Dow JAT, Davies SA. Interactions between epithelial nitric oxide signaling and phosphodiesterase activity in Drosophila. Am J Physiol Cell Physiol 285: C1207-C1218, 2003.
6. 2+ entry enhances muscarinic receptor-mediated soluble amyloid precursor protein (sAPP) release in SH-SY5Y cells. J Biol Chem 281: 12722-12728, 2006.
7. Coast GM, Holman GM, Nachman RJ. The diuretic activity of a series of cephalomyotropic neuropeptides, the achetakinins, on isolated Malpighian tubules of the house cricket, Acheta domesticus. J Insect Physiol 36: 481-488, 1990.
8. Coast GM, Orchard I, Phillips JE, Schooley DA. Insect diuretic and antidiuretic hormones. Adv Insect Physiol 29: 279-409, 2002.
9. Davies SA, Huesmann GR, Maddrell SHP, O'Donnell MJ, Skaer NJV, Dow JAT, Tublitz NJ. CAP2b, a cardioacceleratory peptide, is present in Drosophila and stimulates tubule fluid secretion via cGMP. Am J Physiol Regul Integr Comp Physiol 269: R1321-R1326, 1995.
10. Douglas SJ, Dawson-Scully K, Sokolowski MB. The neurogonesis and evolution of food-related behaviour. Trends Neurosci 28: 644-652, 2005.
11. Dow JAT. Insect midgut function. Adv Insect Physiol 19: 187-328, 1986.
12. Dow JAT, Maddrell SHP, Davies SA, Skaer NJV, Kaiser K. A novel role for the nitric oxide/cyclic GMP signaling pathway: the control of fluid secretion in Drosophila. Am J Physiol Regul Integr Comp Physiol 266: R1716-R1719, 1994.
13. Dow JAT, Maddrell SHP, Görtz A, Skaer NJV, Brogan S, Kaiser K. The Malpighian tubules of Drosophila melanogaster: a novel phenotype for studies of fluid secretion and its control. J Exp Biol 197: 421-428, 1994.
14. Eigenheer RA, Nicolson SW, Schegg KM, Hull JJ, Schooley DA. Identification of a potent antidiuretic factor acting on beetle Malpighian tubules. Proc Natl Acad Sci USA 99: 84-89, 2002.
15. Farmer J, Maddrell SHP, Spring JH. Absorption of fluid by the midgut of Rhodnius. J Exp Biol 94: 301-316, 1981.
16. 2+ exchange. Am J Physiol Renal Physiol 294: F212-F219, 2008.
17. Furuya K, Milchak RJ, Schegg KM, Zhang J, Tobe SS, Coast GM, Schooley DA. Cockroach diuretic hormones: characterization of a calcitonin-like peptide in insects. Proc Natl Acad Sci USA 97: 6469-6474, 2000.
18. Girardie J, Girardie A, Huet JC, Pernollet JC. Amino acid sequence of locust neuroparsins. FEBS Lett 248: 4-8, 1989.
19. Girardie J, Huet JC, Pernollet JC. The locust neuroparsin-A sequence and similarities with vertebrate and insect polypeptide hormones. Insect Biochem 20: 659-666, 1990.
20. Gringorten JL, Friend WG. Absorption of fluid by the midgut of Rhodnius. J Exp Biol 94: 301-316, 1979.
21. Hayes TK, Pannabecker TL, Hinkley DJ, Hohnan GM, Nachman RJ, Petzel DH, Beyenbach KW. Leucokinins, a new family of ion transport stimulators and inhibitors in insect Malpighian tubules. Life Sci 44: 1259-1266, 1989.
22. Holman GM, Nachman RJ, Schoofs L, Hayes TK, Wright MS, De Koof A. The Leueophaea maderae hindgut preparation a rapid and sensitive bioassay tool for the isolation of insect myotropins of other insect species. Insect Biochem 21: 107-112, 1991.
23. Holman GM, Nachman RJ, Wright MS. Comparative aspects of insect myotropic peptides. In: Progress in Comparative Endocrinology, edited by Epple A, Scanes CG, and Stetson MH. New York: Wiley-Liss, 1990, p. 35-39.
24. + in bumetanide-sensitive transport by Malpighian tubules of Rhodnius prolixus. J Exp Biol 207: 3707-3716, 2004.
25. + across the apical membrane in Malpighian (renal) tubule cells of Rhodnius prolixus. J Exp Biol 209: 1964-1975, 2006.
26. Iversen A, Cazzamali G, Williamson M, Hauser F, Grimmelikhuijzen CJ. Molecular cloning and functional expression of a Drosophila receptor for the neuropeptides capa-1 and -2. Biochem Biophys Res Commun 299: 628-633, 2002.
27. Jeffs LB, Phillips JE. Pharmacological study of the second messengers that control rectal ion and fluid transport in the desert locust (Schistocerca gregaria). Arch Insect Biochem Physiol 31: 169-184, 1996.
28. Karley AJ, Ashford DA, Minto LM, Pritchard J, Douglas AE. The significance of gut sucrase activity for osmoregulation in the pea aphid, Acyrthosiphon pisum. J Insect Physiol 51: 1313-1319, 2005.
29. Kataoka H, Troetschler RG, Li JP, Kramer SJ, Carney RL, Schooley DA. Isolation and identification of a diuretic hormone from the tobacco hornworm, Manduca sexta. Proc Natl Acad Sci USA 86: 2976-2980, 1989.
30. Kean L, Cazenave W, Costes L, Broderick KE, Graham S, Pollock VP, Davies SA, Veenstra JA, Dow JA. Two nitridergic peptides are encoded by the gene capability in Drosophila melanogaster. Am J Physiol Regul Integr Comp Physiol 282: R1297-R1307, 2002.
31. Kim JK, Yoo HY, Kim SJ, Hwang YS, Han J, Kim JA, Kim CS, Cho HS. Effects of sevoflurane on the cAMP-induced short-circuit current in mouse tracheal epithelium and recombinant Cl2 (CFTR) and K1 (KCNQ1) channels. Br J Anaesth 99: 245-251, 2007.
32. Klein U, Koch A, Moffett DF. Ion transport in Lepidoptera. In: Biology of the Insect Midgut, edited by Lehane MH and Billingsley PF. London: Chapman & Hall, 1996, p. 236-264.
33. Kunzelmann K, Sun J, Schreiber R, König J. Effects of dietary lectins on ion transport in epithelia. Br J Pharmacol 142: 1219-1226, 2004.
34. Lange AB. Tyramine: from octopamine precursor to neuroactive chemical in insects. Gen Comp Endocrinol 162: 18-26, 2009.
35. Lee KY, Horodyski FM, Chamberlin ME. Inhibition of midgut ion transport by allatotropin (Mas-AT) and Manduca FLRFamides in the tobacco hornworm Manduca sexta. J Exp Biol 201: 3067-3074, 1998.
36. Li H, Sheppard DN, Hug MJ. Transepithelial electrical measurements with the Ussing chamber. J Cyst Fibro 3: 123-126, 2004.
37. Lincoln TM, Cornwell TL. Intracellular cyclic GMP receptor proteins. FASEB J 7: 328-338, 1993.
38. Loi PK, Tublitz NJ. Sequence and expression of the CAPA/CAP2b gene in the tobacco hawkmoth, Manduca sexta. J Exp Biol 207: 3681-3691, 2004.
39. Maddrell SHP. The fastest fluid-secreting cell known: the upper Malpighian tubule cell of Rhodnius. Bioessays 13: 357-362, 1991.
40. Maddrell SHP, O'Donnell MJ, Caffrey R. The regulation of haemolymph potassium activity during initiation and maintenance of diuresis in fed Rhodnius prolixus. J Exp Biol 177: 273-285, 1993.
41. Massaro RC, Lee LW, Patel AB, Wu DS, Yu MJ, Scott BN, Schooley DA, Schegg KM, Beyenbach KW. The mechanism of action of the antidiuretic peptide Tenmo ADFa in Malpighian tubules of Aedes aegypti. J Exp Biol 207: 2877-2888, 2004.
42. Moffett DF. Bathing solution tonicity and potassium transport by the midgut of the tobacco hornworm Manduca sexta. J Exp Biol 78: 213-223, 1979.
43. Norris MJ. Group effects on feeding in adult males of the desert locust, Schistocerca gregaria (Forsk), in relation to sexual maturation. Bull Entomol Res 51: 731-753, 1961.
44. O'Donnell MJ, Ianowski JP, Linton SM, Rheault MR. Inorganic and organic anion transport by insect renal epithelia. Biochim Biophys Acta 1618: 194-206, 2003.
45. Onken H, Moffett SB, Moffett DF. The anterior stomach of larval mosquitoes (Aedes aegypti): effects of neuropeptides on transepithelial ion transport and muscular motility. J Exp Biol 207: 3731-3739, 2004.
46. Orchard I. Serotonin: a coordinator of feeding-related physiological events in the blood-gorging bug, Rhodnius prolixus. Comp Biochem Physiol A Mol Integr Physiol 144: 316-324, 2006.
47. Paluzzi JP, Orchard I. Distribution, activity and evidence for the release of an anti-diuretic peptide in the kissing bug Rhodnius prolixus. J Exp Biol 209: 907-915, 2006.
48. Paluzzi JP, Russell WK, Nachman RJ, Orchard I. Isolation, cloning and expression mapping of a gene encoding an anti-diuretic hormone and other CAPA-related peptides in the disease vector, Rhodnius prolixus. Endocrinology 149: 4638-4646, 2008.
49. Park Y, Kim YJ, Adams ME. Identification of G protein-coupled receptors for Drosophila PRXamide peptides, CCAP, corazonin, and AKH supports a theory of ligand-receptor coevolution. Proc Natl Acad Sci USA 99: 11423-11428, 2002.
50. Phillips JE. Comparative physiology of insect renal function. Am J Physiol Regul Integr Comp Physiol 241: R241-R257, 1981.
51. Phillips JE, Hanrahan J, Chamberlin M, Thomson B. Mechanisms and control of reabsorption in insect hindgut. Adv Insect Physiol 19: 330-422, 1986.
52. Pollock VP, McGettigan J, Cabrero P, Maudlin IM, Dow JAT, Davies SA. Conservation of capa peptide-induced nitric oxide signaling in Diptera. J Exp Biol 207: 4135-4145, 2004.
53. Quinlan MC, O'Donnell MJ. Anti-diuresis in the blood-feeding insect Rhodnius prolixus Stål: antagonistic actions of cAMP and cGMP and the role of organic acid transport. J Insect Physiol 44: 561-568, 1998.
54. Quinlan MC, Tublitz NJ, O'Donnell MJ. Anti-diuresis in the bloodfeeding insect Rhodnius prolixus Staål: the peptide CAP2b and cyclic GMP inhibit Malpighian tubule fluid secretion. J Exp Biol 200: 2363-2367, 1997.
55. Rosay P, Davies SA, Yu Y, Sozen A, Kaiser K, Dow JA. Cell-type specific calcium signalling in a Drosophila epithelium. J Cell Sci 110: 1683-1692, 1997.
56. 2+ signaling by axonal ryanodine receptors at the hippocampal mossy fiber synapse. Proc Natl Acad Sci USA 105: 11998-12003, 2008.
57. Te Brugge V, Ianowski JP, Orchard I. Biological activity of diuretic factors on the anterior midgut of the blood-feeding bug, Rhodnius prolixus. Gen Comp Endocrinol 162: 105-112, 2009.
58. Terhzaz S, Southall TD, Lilley KS, Kean L, Allan AK, Davies SA, Dow JA. Differential gel electrophoresis and transgenic mitochondrial calcium reporters demonstrate spatiotemporal filtering in calcium control of mitochondria. J Biol Chem 281: 18849-18858, 2006.
59. Van Scott MR, Hester S, Boucher RC. Ion transport by rabbit nonciliated bronchiolar epithelial cells (Clara cells) in culture. Proc Natl Acad Sci USA 84: 5496-5500, 1987.
60. --site-specific agents. J Comp Physiol [B] 162: 331-339, 1992.
61. +-secreting insect midgut epithelium (Manduca sexta). Pflügers Arch 407, 657-663, 1986.