Skip to main content
SpringerLink
Log in

Mas-allatotropin/Lom-AG-myotropin I immunostaining in the brain of the locust, Schistocerca gregaria

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

Mas-allatotropin (Mas-AT) and Lom-accessory gland-myotropin I (Lom-AG-MTI) are two members of a conserved family of insect neuropeptides, collectively termed allatotropins, which have diverse functions, ranging from stimulation of juvenile hormone secretion to myotropic effects on heart and hindgut. In addition, allatotropins appear to be abundant within the nervous system, suggesting neuroactive roles. To identify neurons in the insect brain suitable for a neurophysiological analysis of the roles of allatotropins, we used antisera against Mas-AT and Lom-AG-MTI to map allatotropin-immunoreactive neurons in the brain of a suitable insect, the locust Schistocerca gregaria. Both antisera revealed basically identical staining patterns throughout the locust brain with more than 12,500 immunostained interneurons per brain hemisphere. Neurosecretory cells were not labeled, and the retrocerebral complex was devoid of immunostaining. Prominent immunoreactive cell types include about 9,600 lamina monopolar neurons, medulla to lobula interneurons, local neurons of the antennal lobe, a giant interneuron of the mushroom body, projection neurons of the glomerular lobe to the mushroom body, and three systems of tangential neurons of the central complex. Several groups of neurons showed colocalization of Mas-AT- and γ-aminobutyric acid immunostaining. Mass spectrometric analysis identified a peptide with a molecular mass identical to Lom-AG-MTI in all major parts of the locust brain but not in the retrocerebral complex. This study strongly suggests that Lom-AG-MTI is highly abundant in the locust brain, and is likely to play a neuroactive role in many brain circuits including all stages of sensory processing, learning and memory, and higher levels of motor control.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  • Abercrombie M (1946) Estimation of nuclear population from microtome sections. Anat Rec 94:239–247

    Google Scholar 

  • Anton S, Hansson B (1996) Antennal lobe interneurons in the desert locust Schistocerca gregaria (Forskal): processing of aggregation pheromones in adult males and females. J Comp Neurol 370:85–96

    Article  CAS  PubMed  Google Scholar 

  • Anton S, Homberg U (1999) Antennal lobe structure. In: Hansson BS (ed) Insect olfaction. Springer, Berlin Heidelberg New York, pp 97–124

  • Bernard F (1937) Recherches sur la morphogénèse des yeux composés d’arthropodes. Bull Biol Fr Belg Suppl 23:1–162

    Google Scholar 

  • Blaney WM (1974) Electrophysiological responses of the terminal sensilla on the maxillary palps of Locusta migratoria (L.) to some electrolytes and non-electrolytes. J Exp Biol 60:275–293

    CAS  PubMed  Google Scholar 

  • Bogus MI, Scheller K (1994) Identification of allatotropin-secreting cells in the brain of an insect larva. Naturwissenschaften 81:87–89

    Article  CAS  Google Scholar 

  • Duve H, Thorpe A (2003) Neuropeptide co-localization in the lepidopteran frontal ganglion studied by confocal laser scanning microscopy. Cell Tissue Res 311:79–89

    Article  CAS  PubMed  Google Scholar 

  • Duve H, East PD, Thorpe A (1999) Regulation of lepidopteran foregut movement by allatostatins and allatotropin from the frontal ganglion. J Comp Neurol 413:405–416

    Article  CAS  PubMed  Google Scholar 

  • Duve H, Audsley N, Weaver RJ, Thorpe A (2000) Triple co-localization of two types of allatostatin and an allatotropin in the frontal ganglion of the lepidopteran Lacanobia oleracea (Noctuidae): innervation and action on the foregut. Cell Tissue Res 300:153–163

    CAS  PubMed  Google Scholar 

  • Ehmer B, Gronenberg W (2002) Segregation of visual input to the mushroom bodies in the honeybee (Apis mellifera). J Comp Neurol 451:362–373

    Article  PubMed  Google Scholar 

  • Elekonich MM, Horodyski FM (2003) Insect allatotropins belong to a family of structurally-related myoactive peptides present in several invertebrate phyla. Peptides 24:1623–1632

    Article  CAS  PubMed  Google Scholar 

  • Elphick MR, Williams L, O’Shea M (1996) New features of the locust optic lobe: evidence of a role for nitric oxide in insect vision. J Exp Biol 199:2395–2407

    CAS  PubMed  Google Scholar 

  • Ernst KD, Boeckh J, Boeckh V (1977) A neuroanatomical study on the organization of the central antennal pathways in insects. Cell Tissue Res 176:285–308

    CAS  PubMed  Google Scholar 

  • Frambach I, Schürmann F-W (2004) Separate distribution of deutocerebral projection neurones in the mushroom bodies of the cricket brain. Acta Biol Hung 55:21–29

    Google Scholar 

  • Gronenberg W (2001) Subdivisions of hymenopteran mushroom body calyces by their afferent supply. J Comp Neurol 463:474–489

    Article  Google Scholar 

  • Hanström B (1928) Vergleichende Anatomie des Nervensystems der wirbellosen Tiere unter Berücksichtigung seiner Funktion. Springer, Berlin Heidelberg New York

  • Helfrich-Förster C, Stengl M, Homberg U (1998) Organization of the circadian system in insects. Chronobiol Int 15:567–594

    PubMed  Google Scholar 

  • Hoffmann KH, Meyering-Vos M, Lorenz MW (1999). Allatostatins and allatotropins: is the regulation of corpora allata activity their primary function? Eur J Entomol 96:256–266

    Google Scholar 

  • Homberg U (1994) Distribution of neurotransmitters in the insect brain. Progress in zoology, vol 40. Fischer, Stuttgart

  • Homberg U (2002) Neurotransmitters and neuropeptides in the brain of the locust. Microsc Res Tech 56:189–209

    Article  CAS  PubMed  Google Scholar 

  • Homberg U, Paech A (2002) Ultrastructure and orientation of ommatidia in the dorsal rim area of the locust compound eye. Arthropod Struct Dev 30:271–280

    Article  Google Scholar 

  • Homberg U, Montague RA, Hildebrand JG (1988) Anatomy of antenno-cerebral pathways in the brain of the sphinx moth Manduca sexta. Cell Tissue Res 254:255–281

    CAS  PubMed  Google Scholar 

  • Homberg U, Kingan TG, Hildebrand JG (1990) Distribution of FMRFamide-like immunoreactivity in the brain and suboesophageal ganglion of the sphinx moth Manduca sexta and colocalization with SCPB-, BPP-, and GABA-like immunoreactivity. Cell Tissue Res 259:401–419

    CAS  PubMed  Google Scholar 

  • Homberg U, Vitzthum H, Müller M, Binkle U (1999) Immunocytochemistry of GABA in the central complex of the locust Schistocerca gregaria: identification of immunoreactive neurons and colocalization with neuropeptides. J Comp Neurol 409:495–507

    Article  CAS  PubMed  Google Scholar 

  • Homberg U, Reischig T, Stengl M (2003) Neural organization of the circadian system of the cockroach Leucophaea maderae. Chronobiol Int 20:577–591

    Article  CAS  PubMed  Google Scholar 

  • Horodyski FM, Bhatt SR, Lee K-Y (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

    Article  CAS  PubMed  Google Scholar 

  • Ignell R (2001) Monoamines and neuropeptides in antennal lobe interneurons of the desert locust, Schistocerca gregaria: an immunocytochemical study. Cell Tissue Res 306:143–156

    Article  CAS  PubMed  Google Scholar 

  • Ignell R, Anton S, Hansson BS (1998) Central nervous processing of behaviourally relevant odours in solitary and gregarious fifth instar locusts, Schistocerca gregaria. J Comp Physiol A 183:453–465

    Article  CAS  Google Scholar 

  • Ignell R, Anton S, Hansson BS (1999) Integration of behaviourally relevant odours at the central nervous level in solitary and gregarious third instar locusts, Schistocerca gregaria. J Insect Physiol 45:993–1000

    Article  CAS  PubMed  Google Scholar 

  • Ignell R, Anton S, Hansson BS (2000) The maxillary palp sensory pathway of Orthoptera. Arthropod Struct Dev 29:295–305

    Article  Google Scholar 

  • Ignell R, Anton S, Hansson BS (2001) The antennal lobe of Orthoptera—anatomy and evolution. Brain Behav Evol 57:1–17

    Article  CAS  PubMed  Google Scholar 

  • Jawłowski, H (1954) Über die Struktur des Gehirnes bei Saltatoria. Ann Univ Mariae Curie-Skłodowska C8:403–434

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Koladich PM, Tobe SS, McNeil JN (2002a) Enhanced haemolymph circulation by insect ventral nerve cord: hormonal control by Pseudaletia unipuncta allatotropin and serotonin. J Exp Biol 205:3123–3131

    CAS  PubMed  Google Scholar 

  • Koladich PM, Cusson M, Bendena WG, Tobe SS, McNeil JN (2002b) Cardioacceleratory effects of Manduca sexta allatotropin in the true armyworm moth, Pseudaletia unipuncta. Peptides 23:645–651

    Article  CAS  PubMed  Google Scholar 

  • Laurent G (2002) Olfactory network dynamics and the coding of multidimensional signals. Nat Rev Neurosci 3:884–895

    Article  CAS  PubMed  Google Scholar 

  • Laurent G, Wehr M, Davidowitz H (1996) Temporal representations of odors in an olfactory network. J Neurosci 16:3837–3847

    CAS  PubMed  Google Scholar 

  • Lee K-Y, Horodyski FM, Chamberlin ME (1998) Inhibition of midgut ion transport by allatotropin (Mas-AT) and Manduca FLRFamide peptides in the tobacco hornworm, Manduca sexta. J Exp Biol 201:3067–3074

    CAS  PubMed  Google Scholar 

  • Lee K-Y, Chamberlin ME, Horodyski FM (2002) Biological activity of Manduca sexta allatotropin-like peptides, predicted products of tissue-specific and developmentally regulated alternatively spliced mRNAs. Peptides 23:1933–1941

    Article  CAS  PubMed  Google Scholar 

  • Leitch B, Laurent G (1996) GABAergic synapses in the antennal lobe and mushroom body of the locust olfactory system. J Comp Neurol 372:487–514

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Unnithan GC, Veenstra JA, Feyereisen R, Noriega FG (2003) Stimulation of JH biosynthesis by the corpora allata of adult female Aedes aegypti in vitro: effect of farnesoic acid and Aedes allatotropin. J Exp Biol 206:1825–1832

    Article  CAS  PubMed  Google Scholar 

  • MacLeod K, Laurent G (1996) Distinct mechanisms of synchronization and temporal patterning of odor-encoding neural assemblies. Science 274:976–979

    Article  CAS  PubMed  Google Scholar 

  • Meeusen T, Mertens I, De Loof A, Schoofs L (2003) G protein-coupled receptors in invertebrates: a state of the art. Int Rev Cytol 230:189–261

    Article  CAS  PubMed  Google Scholar 

  • Mobbs PG (1982) The brain of the honeybee Apis mellifera. I. The connections and spatial organization of the mushroom bodies. Philos Trans R Soc Lond B 298:309–354

    Google Scholar 

  • Nässel DR (1987) Neuroactive substances in the insect CNS. In: Ali MA (ed) Nervous system in invertebrates. Plenum, New York, pp 171–212

  • Nässel DR (2000) Functional roles of neuropeptides in the insect central nervous system. Naturwissenschaften 87:439–449

    Article  PubMed  Google Scholar 

  • Nowel MS, Shelton PMJ (1981) A Golgi-electron-microscopical study of the structure and development of the lamina ganglionaris of the locust optic lobe. Cell Tissue Res 216:377–401

    CAS  PubMed  Google Scholar 

  • Nusbaum MP, Blitz DM, Swensen AM, Wood D, Marder E (2001) The roles of co-transmission in neural network modulation. Trends Neurosci 24:146–154

    Article  CAS  PubMed  Google Scholar 

  • Oeh U, Lorenz MW, Dyker H, Lösel P, Hoffmann KP (2000) Interaction between Manduca sexta allatotropin and Manduca sexta allatostatin in the fall armyworm Spodoptera frugiperda. Insect Biochem Mol Biol 30:719–727

    Article  CAS  PubMed  Google Scholar 

  • Paemen L, Tips A, Schoofs L, Proost P, Van Damme J, De Loof A (1991) Lom-AG-myotropin: a novel myotropic peptide from the male accessory glands of Locusta migratoria. Peptides 12:7–10

    Article  CAS  PubMed  Google Scholar 

  • Paemen L, Schoofs L, De Loof A (1992) Localization of Lom-AG-myotropin I-like substances in the male reproductive and nervous tissue of the locust, Locusta migratoria. Cell Tissue Res 268:91–97

    CAS  PubMed  Google Scholar 

  • Park C, Jeon SK, Kim M-Y, Han SS, Yu CH, Lee BH (2001) Postembryonic localization of allatotropin- and allatostatin-producing cells in central nervous system of the silk moth Bombyx mori. Zool Sci 18:367–379

    Google Scholar 

  • Park C, Hwang JS, Kang SW, Lee BH (2002) Molecular characterization of a cDNA from the silk moth Bombyx mori encoding Manduca sexta allatotropin peptide. Zool Sci 19:287–292

    CAS  PubMed  Google Scholar 

  • Persson MGS, Nässel DR (1999) Neuropeptides in insect sensory neurons: tachykinin, FMRFamide- and allatotropin-related peptides in terminals of locust thoracic sensory afferents. Brain Res 816:131–141

    Article  CAS  PubMed  Google Scholar 

  • Petri B, Stengl M, Würden S, Homberg U (1995) Immunocytochemical characterization of the accessory medulla in Leucophaea maderae. Cell Tissue Res 282:3–19

    Article  CAS  PubMed  Google Scholar 

  • Petri B, Homberg U, Loesel R, Stengl M (2002) Evidence for a role of GABA and Mas-allatotropin in photic entrainment of the circadian clock of the cockroach Leucophaea maderae. J Exp Biol 205:1459–1469

    CAS  PubMed  Google Scholar 

  • Rachinsky A, Feldlaufer MF (2000) Responsiveness of honey bee (Apis mellifera L.) corpora allata to allatoregulatory peptides from four insect species. J Insect Physiol 46:41–46

    Article  CAS  PubMed  Google Scholar 

  • Rachinsky A, Srinivasan A, Ramaswamy SB (2003) Regulation of juvenile hormone biosynthesis in Heliothis virescens by Manduca sexta allatotropin. Arch Insect Biochem Physiol 54:121–133

    Article  CAS  PubMed  Google Scholar 

  • Riehle MA, Garczynski SF, Crim JW, Hill CA, Brown MR (2002) Neuropeptides and peptide hormones in Anopheles gambiae. Science 298:172–175

    Article  CAS  PubMed  Google Scholar 

  • Rudwall AJ, Sliwowska J, Nässel DR (2000) Allatotropin-like neuropeptide in the cockroach abdominal nervous system: myotropic actions, sexually dimorphic distribution and colocalization with serotonin. J Comp Neurol 428:159–173

    Article  CAS  PubMed  Google Scholar 

  • Satija RC (1958) A histological and experimental study of nervous pathways in the brain and thoracic nerve cord of Locusta migratoria migratoriodes (R & F). Res Bull Panjab Univ 9:13–32

    Google Scholar 

  • Sattelle DB (1990) GABA receptors of insects. Adv Insect Physiol 22:1–113

    Google Scholar 

  • Spittaels K, Vankeerberghen A, Schoofs L, Proost P, Van Damme J, De Loof A (1996) Isolation and characterization of Locusta migratoria accessory gland myotropin I (Lom-AG-MT-I) from the brain of the Colorado potato beetle, Leptinotarsa decemlineata. Arch Insect Biochem Physiol 31:149–155

    Article  CAS  PubMed  Google Scholar 

  • Sternberger LA (1979) Immunocytochemistry. Wiley, New York

  • Stopfer M, Bhagvan S, Smith BH, Laurent G (1997) Impaired odour discrimination of odour-encoding neural assemblies. Nature 390:70–74

    Article  CAS  PubMed  Google Scholar 

  • Strausfeld NJ, Hansen L, Li Y, Gomez RS, Ito K (1998) Evolution, discovery, and interpretations of arthropod mushroom bodies. Learn Mem 5:11–37

    CAS  PubMed  Google Scholar 

  • Taylor PA III, Bhatt TR, Horodyski FM (1996) Molecular characterization and expression analysis of Manduca sexta allatotropin. Eur J Biochem 239:588–596

    CAS  PubMed  Google Scholar 

  • Truesdell PF, Koladich PM, Kataoka H, Kojima K, Suzuki A, McNeil J, Mizoguchi A, Tobe SS, Bendena WG (2000) Molecular characterization of a cDNA from the true armyworm Pseudaletia unipuncta encoding Manduca sexta allatotropin peptide. Insect Biochem Mol Biol 30:691–702

    Article  CAS  PubMed  Google Scholar 

  • Tu MT, Kou R, Wang Z-S, Stoffolano JG Jr, Yin C-M (2001) Immunolocalization and possible effect of a moth allatotropin-like substance in a fly, Phormia regina (Diptera: Calliphoridae). J Insect Physiol 47:233–244

    Article  CAS  PubMed  Google Scholar 

  • Veelaert D, Schoofs L, De Loof A (1998) Peptidergic control of the corpus cardiacum-corpora allata complex of locusts. Int Rev Cytol 182:249–302

    CAS  PubMed  Google Scholar 

  • Veenstra JA, Costes L (1999) Isolation and identification of a peptide and its cDNA from the mosquito Aedes aegypti related to Manduca sexta allatotropin. Peptides 20:1145–1151

    Article  CAS  PubMed  Google Scholar 

  • Veenstra JA, Hagedorn HH (1993) Sensitive enzyme immunoassay for Manduca allatotropin and the existence of an allatotropin-immunoreactive peptide in Periplaneta americana. Arch Insect Biochem Physiol 23:99–109

    CAS  Google Scholar 

  • Veenstra JA, Lehman HK, Davis NT (1994) Allatotropin is a cardioacceleratory peptide in Manduca sexta. J Exp Biol 188:347–354

    CAS  PubMed  Google Scholar 

  • Vitzthum H, Homberg U (1998) Immunocytochemical demonstration of locustatachykinin-related peptides in the central complex of the locust brain. J Comp Neurol 390:455–469

    Article  CAS  PubMed  Google Scholar 

  • Vitzthum H, Müller M, Homberg U (2002) Neurons of the central complex of the locust Schistocerca gregaria are sensitive to polarized light. J Neurosci 22:1114–1125

    CAS  PubMed  Google Scholar 

  • Wilson RI, Turner GC, Laurent G (2004) Transformation of olfactory representations in the Drosophila antennal lobe. Science 303:366–370

    Article  CAS  PubMed  Google Scholar 

  • Würden S, Homberg U (1995) Immunocytochemical mapping of serotonin and neuropeptides in the accessory medulla of the locust, Schistocerca gregaria. J Comp Neurol 362:305–319

    PubMed  Google Scholar 

  • Zars T (2000) Behavioral functions of the insect mushroom bodies. Curr Opin Neurobiol 10:790–795

    Article  CAS  PubMed  Google Scholar 

  • Žitňan 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

    Google Scholar 

  • Žitňan D, Kingan TG, Kramer SJ, Beckage NE (1995) Accumulation of neuropeptides in the cerebral neuroseretory system of Manduca sexta larvae parasitized by the braconid wasp Cotesia congregata. J Comp Neurol 356:83–100

    Google Scholar 

Download references

Acknowledgements

We are grateful to Dr. Timothy Kingan for the donation of anti-GABA antiserum. We thank Dr. Lez Williams for advice regarding nomenclature and are grateful to Ulrike Binkle and Jutta Seyfarth for expert technical assistance. E. Clynen is a post-doc of the FWO Flanders.

Author information

Authors and Affiliations

  1. Fachbereich Biologie/Tierphysiologie, Universität Marburg, 35032, Marburg, Germany

    Uwe Homberg

  2. Institut für Zoologie, Universität Regensburg, 93053, Regensburg, Germany

    Christian Brandl

  3. Zoological Institute, K.U. Leuven, Naamsestraat 59, 3000, Leuven, Belgium

    Elke Clynen & Liliane Schoofs

  4. Neuroendocrinol Lab, University of Bordeaux 1, 33405, Talence, France

    Jan A. Veenstra

Authors
  1. Uwe Homberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christian Brandl
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Elke Clynen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Liliane Schoofs
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jan A. Veenstra
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Uwe Homberg.

Additional information

This work was supported by DFG grant HO 950/14 to U.H.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Homberg, U., Brandl, C., Clynen, E. et al. Mas-allatotropin/Lom-AG-myotropin I immunostaining in the brain of the locust, Schistocerca gregaria. Cell Tissue Res 318, 439–457 (2004). https://doi.org/10.1007/s00441-004-0913-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-004-0913-7

Keywords

Search

Navigation