Receptor Guanylyl Cyclases in Inka Cells Targeted by Eclosion Hormone

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2009 Aug 12

PMID 19666575

Citations 21

Authors

Jer-Cherng Chang

Ruey-Bing Yang

Michael E Adams

Kuang-Hui Lu

Affiliations

Soon will be listed here.

Abstract

A signature of eclosion hormone (EH) action in insect ecdysis is elevation of cGMP in Inka cells, leading to massive release of ecdysis triggering hormone (ETH) and ecdysis initiation. Although this aspect of EH-induced signal transduction is well known, the receptor mediating this process has not been identified. Here, we describe a receptor guanylyl cyclase BdmGC-1 and its isoform BdmGC-1B in the Oriental fruit fly Bactrocera dorsalis that are activated by EH. The B form exhibits the conserved domains and putative N-glycosylation sites found in BdmGC-1, but possesses an additional 46-amino acid insertion in the extracellular domain and lacks the C-terminal tail of BdmGC-1. Combined immunolabeling and in situ hybridization reveal that BdmGC-1 is expressed in Inka cells. Heterologous expression of BdmGC-1 in HEK cells leads to robust increases in cGMP following exposure to low picomolar concentrations of EH. The B-isoform responds only to higher EH concentrations, suggesting different physiological roles of these cyclases. We propose that BdmGC-1 and BdmGC-1B are high- and low-affinity EH receptors, respectively.

Citing Articles

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References

Marti T, Takio K, Walsh K, Terzi G, Truman J . Microanalysis of the amino acid sequence of the eclosion hormone from the tobacco hornworm Manduca sexta. FEBS Lett. 1987; 219(2):415-8. DOI: 10.1016/0014-5793(87)80263-6. View

Clark A, Del Campo M, Ewer J . Neuroendocrine control of larval ecdysis behavior in Drosophila: complex regulation by partially redundant neuropeptides. J Neurosci. 2004; 24(17):4283-92. PMC: 6729283. DOI: 10.1523/JNEUROSCI.4938-03.2004. View

Shyjan A, de Sauvage F, Gillett N, Goeddel D, Lowe D . Molecular cloning of a retina-specific membrane guanylyl cyclase. Neuron. 1992; 9(4):727-37. DOI: 10.1016/0896-6273(92)90035-c. View

Kataoka H, Troetschler R, Kramer S, Cesarin B, Schooley D . Isolation and primary structure of the eclosion hormone of the tobacco hornworm, Manduca sexta. Biochem Biophys Res Commun. 1987; 146(2):746-50. DOI: 10.1016/0006-291x(87)90592-4. View

Morton D, Simpson P . Cellular signaling in eclosion hormone action. J Insect Physiol. 2003; 48(1):1-13. DOI: 10.1016/s0022-1910(01)00157-3. View

Park Y, Filippov V, Gill S, Adams M . Deletion of the ecdysis-triggering hormone gene leads to lethal ecdysis deficiency. Development. 2002; 129(2):493-503. DOI: 10.1242/dev.129.2.493. View

Klein C, Kallenborn H, Radlicki C . The 'Inka cell' and its associated cells: ultrastructure of the epitracheal glands in the gypsy moth, Lymantria dispar. J Insect Physiol. 2003; 45(1):65-73. DOI: 10.1016/s0022-1910(98)00085-7. View

Zitnan D, Kim Y, Zitnanova I, Roller L, Adams M . Complex steroid-peptide-receptor cascade controls insect ecdysis. Gen Comp Endocrinol. 2007; 153(1-3):88-96. PMC: 4955941. DOI: 10.1016/j.ygcen.2007.04.002. View

Lucas K, Pitari G, Kazerounian S, Ruiz-Stewart I, Park J, Schulz S . Guanylyl cyclases and signaling by cyclic GMP. Pharmacol Rev. 2000; 52(3):375-414. View

10.

Dizhoor A, Lowe D, Olshevskaya E, Laura R, Hurley J . The human photoreceptor membrane guanylyl cyclase, RetGC, is present in outer segments and is regulated by calcium and a soluble activator. Neuron. 1994; 12(6):1345-52. DOI: 10.1016/0896-6273(94)90449-9. View

11.

Schrem A, Lange C, Beyermann M, Koch K . Identification of a domain in guanylyl cyclase-activating protein 1 that interacts with a complex of guanylyl cyclase and tubulin in photoreceptors. J Biol Chem. 1999; 274(10):6244-9. DOI: 10.1074/jbc.274.10.6244. View

12.

Scott R, Thelin W, Milgram S . A novel PDZ protein regulates the activity of guanylyl cyclase C, the heat-stable enterotoxin receptor. J Biol Chem. 2002; 277(25):22934-41. DOI: 10.1074/jbc.M202434200. View

13.

Dizhoor A, Olshevskaya E, Henzel W, Wong S, Stults J, Ankoudinova I . Cloning, sequencing, and expression of a 24-kDa Ca(2+)-binding protein activating photoreceptor guanylyl cyclase. J Biol Chem. 1995; 270(42):25200-6. DOI: 10.1074/jbc.270.42.25200. View

14.

Horodyski F, Ewer J, Riddiford L, Truman J . Isolation, characterization and expression of the eclosion hormone gene of Drosophila melanogaster. Eur J Biochem. 1993; 215(2):221-8. DOI: 10.1111/j.1432-1033.1993.tb18026.x. View

15.

Zitnan D, Zitnanova I, Spalovska I, Takac P, Park Y, Adams M . Conservation of ecdysis-triggering hormone signalling in insects. J Exp Biol. 2003; 206(Pt 8):1275-89. DOI: 10.1242/jeb.00261. View

16.

Kingan T, Cardullo R, Adams M . Signal transduction in eclosion hormone-induced secretion of ecdysis-triggering hormone. J Biol Chem. 2001; 276(27):25136-42. DOI: 10.1074/jbc.M102421200. View

17.

Lowe D, Dizhoor A, Liu K, Gu Q, Spencer M, Laura R . Cloning and expression of a second photoreceptor-specific membrane retina guanylyl cyclase (RetGC), RetGC-2. Proc Natl Acad Sci U S A. 1995; 92(12):5535-9. PMC: 41730. DOI: 10.1073/pnas.92.12.5535. View

18.

De Lean A, McNicoll N, Labrecque J . Natriuretic peptide receptor A activation stabilizes a membrane-distal dimer interface. J Biol Chem. 2003; 278(13):11159-66. DOI: 10.1074/jbc.M212862200. View

19.

Zitnan D, Ross L, Zitnanova I, Hermesman J, Gill S, Adams M . Steroid induction of a peptide hormone gene leads to orchestration of a defined behavioral sequence. Neuron. 1999; 23(3):523-35. DOI: 10.1016/s0896-6273(00)80805-3. View

20.

Ewer J, Gammie S, Truman J . Control of insect ecdysis by a positive-feedback endocrine system: roles of eclosion hormone and ecdysis triggering hormone. J Exp Biol. 1997; 200(Pt 5):869-81. DOI: 10.1242/jeb.200.5.869. View