Eur. J. Entomol. 112 (2): 235-244, 2015 | 10.14411/eje.2015.035

Immunochemical detection of the crustacean cardioactive peptide in the cephalic ganglia of cockroaches (Blattodea: Blattidae)

Marcin GLADYSZ1, Joanna GUZIK1, Hana SEHADOVÁ2, Bartosz BARAN1, Jadwiga BEMBENEK1, Bogdan DOLEZYCH1
1 Department of Animal Physiology and Ecotoxicology, Faculty of Biology and Environmental Protection, University of Silesia, Bankowa 9, 40-007 Katowice, Poland; e-mails: marcin.gladyszz@gmail.com, joannaguzik6@wp.pl, bartosz.m.baran@gmail.com; jadwigabembenek@hotmail.com; bogdan.dolezych@us.edu.pl
2 Department of Molecular Biology and Genetics, Institute of Entomology, Biology Centre CAS, 37005 Ceske Budejovice, Czech Republic; e-mail: sehadova@yahoo.com

In insects, the crustacean cardioactive peptide (CCAP) is involved mainly in the regulation of ecdysis and is both a hormone secreted into the haemolymph and a neuromodulator or neurotransmitter in the nervous system. However, this peptide has only been recorded in the brains of a few species of insects. The present study examined the distribution of CCAP in the cephalic ganglia of the cockroach, Periplaneta americana, using two kinds of specific antibodies. The antibody directed against synthetic CCAP detected a large number of CCAP-immunoreactive neurons in the protocerebrum, deutocerebrum, tritocerebrum, suboesophageal ganglion, optic lobes, frontal ganglion and neurohemal organs, while the antibody directed against CCAP precursor (pre-propeptide) stained only a few neurons within the central brain and frontal ganglion. The latter antibody also revealed similar sets of neurons in another species of cockroach, Gromphadorhina portentosa, and identified the CCAP precursor of approximately 15 kDa in size in Western blot analyses.

Keywords: Blattodea, Periplaneta americana, Gromphadorhina portentosa, cockroach, CCAP, neuropeptides

Received: May 12, 2014; Accepted: December 12, 2014; Prepublished online: February 3, 2015; Published: April 2, 2015

Download citation

References

  1. Arakane Y., Li B., Muthukrishnan S., Beeman R.W., Kramer K.J. & Park Y. 2008: Functional analysis of four neuropeptides, EH, ETH, CCAP and bursicon, and their receptors in adult ecdysis behavior of the red flour beetle, Tribolium castaneum. - Mech. Dev. 125: 984-995 Go to original source...
  2. Bradford M.M. 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 Go to original source...
  3. Breidbach O. & Dircksen H. 1991: Crustacean cardioactive peptide-immunoreactive neurons in the ventral nerve cord and the brain of the meal beetle Tenebrio molitor during postembryonic development. - Cell Tissue Res. 265: 129-144 Go to original source...
  4. Cazzamali G., Hauser F., Kobberup S., Williamson M. & Grimmelikhuijzen C.J. 2003: Molecular identification of a Drosophila G protein-coupled receptor specific for crustacean cardioactive peptide. - Biochem. Biophys. Res. Commun. 303: 146-152 Go to original source...
  5. Da Silva S.R., Da Silva R. & Lange A.B. 2011: Effects of crustacean cardioactive peptide on the hearts of two Orthopteran insects, and the demonstration of a Frank-Starling-like effect. - Gen. Comp. Endocrinol. 171: 218-224 Go to original source...
  6. Davis N.T., Homberg U., Dircksen H., Levine R.B. & Hildebrand J.G. 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 Go to original source...
  7. Dircksen H. & Homberg U. 1995: Crustacean cardioactive peptide-immunoreactive neurons innervating brain neuropils, retrocerebral complex and stomatogastric nervous system of the locust, Locusta migratoria. - Cell Tissue Res. 279: 495-515 Go to original source...
  8. Dircksen H., Mueller 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 Go to original source...
  9. Donini A., Agricola H.J. & Lange A.B. 2001: Crustacean cardioactive peptide is a modulator of oviduct contractions in Locusta migratoria. - J. Insect Physiol. 47: 277-285 Go to original source...
  10. Donini A., Ngo C. & Lange A.B. 2002: Evidence for crustacean cardioactive peptide-like innervation of the gut in Locusta migratoria. - Peptides 23: 1915-1923 Go to original source...
  11. Dulcis D., Levine R.B. & Ewer J. 2005: Role of the neuropeptide CCAP in Drosophila cardiac function. - J. Neurobiol. 64: 259-274 Go to original source...
  12. Estevez-Lao T.Y., Boyce D.S., Honegger H.W. & Hillyer J.F. 2013: Cardioacceleratory function of the neurohormone CCAP in the mosquito Anopheles gambiae. - J. Exp. Biol. 216: 601-613 Go to original source...
  13. Furuya K., Liao S., Reynolds S.E., Ota R.B., Hackett M. & Schooley D.A. 1993: Isolation and identification of a cardioactive peptide from Tenebrio molitor and Spodoptera eridania. - Biol. Chem. Hoppe-Seyler 374: 1065-1074 Go to original source...
  14. Gammie S.C. & Truman J.W. 1997: Neuropeptide hierarchies and the activation of sequential motor behaviors in the hawkmoth, Manduca sexta. - J. Neurosci. 17: 4389-4397
  15. Jackson G.E., Mabula A.N., Stone S.R., Gaede G., Koever K.E., Szilagyi L. & Van der Spoel D. 2009: Solution conformations of an insect neuropeptide: Crustacean cardioactive peptide (CCAP). - Peptides 30: 557-564 Go to original source...
  16. Lange A.B. & Patel K. 2005: The presence and distribution of crustacean cardioactive peptide in the central and peripheral nervous system of the stick insect, Baculum extradentatum. - Regul. Pept. 129: 191-201 Go to original source...
  17. Lee D.H., Paluzzi J.P., Orchard I. & Lange A.B. 2011: Isolation, cloning and expression of the crustacean cardioactive peptide gene in the Chagas' disease vector, Rhodnius prolixus. - Peptides 32: 475-482 Go to original source...
  18. Lehman H.K., Murgiuc C.M., Miller T.A., Lee T.D. & Hildebrand J.G. 1993: Crustacean cardioactive peptide in the sphinx moth, Manduca sexta. - Peptides 14: 735-741 Go to original source...
  19. Loi P.K., Emmal S.A., Park Y. & Tublitz N.J. 2001: Identification, sequence and expression of a crustacean cardioactive peptide (CCAP) gene in the moth Manduca sexta. - J. Exp. Biol. 204: 2803-2816
  20. Matsui T., Sakai T., Satake H. & Takeda M. 2013: The pars intercerebralis affects digestive activities of the American cockroach, Periplaneta americana, via crustacean cardioactive peptide and allatostatin-A. - J. Insect Physiol. 59: 33-37 Go to original source...
  21. Park Y., Kim Y.J. & Adams M.E. 2002: 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. U.S.A. 99: 11423-11428 Go to original source...
  22. Phlippen M.K., Webster S.G., Chung J.S. & Dircksen H. 2000: Ecdysis of decapod crustaceans is associated with a dramatic release of crustacean cardioactive peptide into the haemolymph. - J. Exp. Biol. 203: 521-536
  23. Sakai T., Satake H., Minakata H. & Takeda M. 2004: Characterization of crustacean cardioactive peptide as a novel insect midgut factor: isolation, localization, and stimulation of α-amylase activity and gut contraction. - Endocrinology 145: 5671-5678 Go to original source...
  24. Sakai T., Satake H. & Takeda M. 2006: Nutrient-induced alpha-amylase and protease activity is regulated by crustacean cardioactive peptide (CCAP) in the cockroach midgut. - Peptides 27: 2157-2164 Go to original source...
  25. Sehadova H., Shao Q.M., Sehnal F. & Takeda M. 2007: Neurohormones as putative circadian clock output signals in the central nervous system of two cricket species - Cell Tissue Res. 328: 239-255 Go to original source...
  26. Slama K. & Rosinski G. 2005: Delayed pharmacological effects of proctolin and CCAP on heartbeat in pupae of the tobacco hornworm, Manduca sexta. - Physiol. Entomol. 30: 14-28 Go to original source...
  27. Slama K., Sakai T. & Takeda M. 2006: Effect of corazonin and crustacean cardioactive peptide on heartbeat in the adult American cockroach (Periplaneta americana). - Arch. Insect Biochem. Physiol. 62: 91-103 Go to original source...
  28. Stangier J., Hilbich C., Beyreuther K. & Keller R. 1987: Unusual cardioactive peptide (CCAP) from pericardial organs of the shore crab Carcinus maenas. - Proc. Natl. Acad. Sci. U.S.A. 84: 575-579 Go to original source...
  29. Stangier J., Hilbich C., Dircksen H. & Keller R. 1988: Distribution of a novel cardioactive neuropeptide (CCAP) in the nervous system of the shore crab Carcinus maenas. - Peptides 9: 795-800 Go to original source...
  30. Stangier J., Hilbich C. & Keller R. 1989: Occurrence of crustacean cardioactive peptide (CCAP) in the nervous system of an insect, Locusta migratoria. - J. Comp. Physiol. (B) 159: 5-11 Go to original source...
  31. Veelaert D., Passier P., Devreese B., Vanden Broeck J., Van Beeumen J., Vullings H.G.B., Diederen J.H.B., Schoofs L. & De Loof A. 1997: Isolation and characterization of an adipokinetic hormone release-inducing factor in locusts: the crustacean cardioactive peptide. - Endocrinology 138: 138-142 Go to original source...
  32. Vehovszky A., Agricola H.J., Elliott C.J., Ohtani M., Karpati L. & Hernadi L. 2005: Crustacean cardioactive peptide (CCAP)-related molluscan peptide (M-CCAPs) are potential extrinsic modulators of the buccal feeding network in the pond snail Lymnaea stagnalis. - Neurosci. Lett. 373: 200-205 Go to original source...