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Research report:

AG Homberg

Homberg
Prof. Dr. Uwe Homberg

Born January 26th 1953
1978 Diploma University of Berlin
1982 Promotion University of Berlin
1991 Habilitation University of Regensburg
Professor in Marburg since 1997




Research
projects:







Research


Research in our group focusses on the function and development of the insect nervous system. Eight projects are currently under investigation:


Polarization vision in locusts

Behavioral experiments have shown that the polarization pattern of the blue sky serves an important role in insect compass navigation and spatial orientation. We investigate the neural mechanisms underlying skylight navigation in the desert locust Schistocerca gregaria. In S. gregaria, as in other insects, a small dorsal rim

Schistocerca gregaria

Dorsal rim area (arrows) in the compound eyes of the desert locust

area of the compound eye is highly specialized for the detection of polarized light. Polarization-sensitive interneurons were found in the medulla and lobula of the optic lobe, and in the anterior optic tubercle and central complex of the locust midbrain. Polarization-sensitive interneurons in the central complex show polarization opponency, i.e. e-vectors leading to maximal excitation are perpendicular to e-vectors causing maximal inhibition. Current experiments study behavioral responses of tethered flying locusts to polarized light, characterize polarization sensitive neurons at the level of the anterior optic tubercle and central complex and try to identify interneurons which qualify as compass neurons.


Functional role of the central complex in the insect brain


The central complex is a group of interconnected neuropils in the center of the insect brain. It consists of the protocerebral bridge (PB), the upper and lower divisions of the central body (CBU, CBL) and a pair of posterior noduli. The most striking feature of this brain area is a topographically highly ordered arrangement of neural elements, forming a series of layers, subdivided into rows of 16 columns.

Insektengehirn

Wiring diagram showing connections between columns of the protocerebral bridge (PB), columns in the lower division of the central body (CBL) and projections to the lateral triangles (LT).

To understand the functional role of this brain area, we analyze the neuroarchitecture of the locust central complex through computer-assisted 3-dimensional reconstructions of neuropils and neurons from confocal image stacks. Immunocytochemical studies showed that a large variety of neurotransmitters and neuropeptides is present in the central complex. We have provided detailed maps for the distribution of GABA, dopamine, serotonin, and the peptides allatostatin, CCAP, and Lom-tachykinin in distinct populations of central-complex neurons. Single cell recordings suggest that the central complex is involved in flight control. Together with prominent responses of central-complex neurons to polarized light, these data strongly suggest that the central complex serves a role as a navigational center for direction finding and spatial orientation.


The circadian clock in the insect brain


Animals using a sky compass for navigation need to permanently adjust their migratory direction with respect to daytime changes in the position of the sun. This time compensation in sky compass navigation requires an internal circadian clock. We have analyzed the location and internal organization of the circadian clock in a favorable insect, the cockroach Leucophaea maderae. In the cockroach, as in other insects, the internal clock is associated with the accessory medulla in the optic lobe. Current studies focus on the analysis of light entrainment pathways of the clock, and on the morphological and functional characterization of orcokinin-immunoreactive neurons, which might be involved in light entrainment and coupling of the bilaterally symmetric clocks.
nach oben


Neurotransmitters and peptides in the insect brain


The insect brain is supplied with an astounding diversity of signaling molecules including neurotransmitters, neuromodulators, and neuropeptides. In order to understand the chemical compartmentalization of the brain and its constituent neuropils, we mapped the distribution of these substances using immunocytochemical and histochemical staining techniques. So far, these studies revealed novel chemically defined compartments in the antennal lobe, in the mushroom body and in the central complex, and showed reproducible and widespread colocalization of transmitter substances throughout the brain. Transmitter antisera, furthermore, served as valuable tools for developmental studies of the insect brain during metamorphosis. Studies on the functional role of classical transmitters and neuropeptides focus on the accessory medulla and central complex.
nach oben


Regulation and role of nitric oxide (NO) and cGMP during antennal lobe development of the sphinx moth Manduca sexta


The antennal lobe is the first integration center for odor perception in the insect brain. A similar functional organization into so called glomeruli can be found in all first odor integration centers in the animal kingdom, like for example in our olfactory bulb, the vertebrate analogue to the insects antennal lobe. Despite many efforts it is not known how these first odor processing units arise during development. For several reasons the metamorphosing CNS of the moth Manduca sexta is ideally suited to study the mechanisms of antennal lobe development.

 Modell eines Antennallobus

3-D model of an antennal lobe of Manduca sexta. Scale, 100 µm.


We could demonstrate (1) that during formation of the glomeruli the NO/cGMP (cyclic guanosine monophosphate) signaling pathway is used by a defined set of local interneurons of the antennal lobe, (2) that this ability is developmentally regulated by the steroid hormone 20-hydroxyecdysone, and (3), that obviously NO is activity dependent released from olfactory receptor neurons. Furthermore (4), acetylcholine, biogenic amines and copper/zinc superoxide dismutase seem to be involved in the regulation of NO and cGMP concentrations, and (5) pharmacologically interfering with the NO/ cGMP signaling pathway resulted in lower amounts of a ubiquitous synaptic vesicle protein – suggesting a decrease in synaptic density.

In summary our findings support the hypothesis, that the NO/cGMP signaling pathway might be involved in activity dependent synapse formation in the developing glomeruli of the antennal lobe.


Regulation and role of neuropeptides during M. sexta antennal lobe development


Many neuropeptides are expressed in the antennal lobes of insects as well as in the olfactory bulb of vertebrates.

Besides this fact nearly nothing is known about the role of these neuropeptides during signal transmission or during development.

In a first step we examined the expression pattern of various neuropeptide families during antennal lobe development to determine whether the time course of peptide occurrence would allow a role during development.

Neuropeptidfärbung, Antennallobus

Neuropeptide immunostaining in a developing antennal lobe. Scales, 80 µm; inset, 40 µm


Our experiments showed: 1) Persisting larval neurons with neuropeptide immunoreactivity, 2) many local interneurons, presumably newly born during larval life which start to obtain their neuropeptide identities before and during the beginning of glomeruli formation, (3) centrifugal peptidergic neurons, and (4) the regulation of developmental peptide expression pattern via the developmental hormone 20-hydroxyecdysone. (5) Direct mass profiling of defined cell groups of the AL by MALDI-TOF and MALDI-TOF-TOF revealed masses of over 20 presumable neuropeptides. Of the 20 masspeaks we could so far identify 8 masses, which belong to four different families of neuropeptides.

Due to the developmental occurrence of the neuropeptide families examined they might be well suited to influence the formation of the synaptic network in the developing glomeruli. Ongoing studies examine how neuropeptides might be involved in antennal lobe development.


Regulation of peptide release from insect neurohemal organs


of behaviour and physiology. Neurohemal organs are storage and release sites of peptide hormones synthesized within in the central nervous system. The function of many insect peptide hormones is well established. In contrast, only very little is known about the identity of the neurons that provide input to peptidergic secretory cells, and how presynaptic input might trigger the calcium-dependent peptide hormone release.

ahom

Acetylcholine-induced changes in the free intracellular calcium concentration in a peptidergic neuron


Within the Emmy Noether young investigator group that has started in September 2003, we screen for signaling substances (neuro-transmitters, neuropeptides) that are able to induce a calcium increase in peptidergic Drosophila neurons. For that, we use calcium imaging in primary cell cultures and in situ, relying on synthetic and genetically encoded calcium sensors. We are also establishing techniques for i) the optical measurement of peptide release, and ii) the mass spectrometric identification of peptide hormones in the insect hemolymph.


Chemical and morphological characterization of the peptidergic system within the ventral ganglion of the Drosophila-larvae

For several reasons, the fruit fly Drosophila melanogaster is well suited to gain a comprehensive overview of the peptidergic system of an insect: i) all its peptides are predictable due to its sequenced genome, ii) its nervous system and development is well characterized, and iii) peptidergic neurons are easily identifiable without laborious staining methods by the GAL4/UAS-technique. In the larval central nervous systems, an anatomical “reference system” can be established by staining against landmark proteins, which greatly facilitates a precise and comparable morphological description of peptidergic neurons.

Model of CAPA prohormone

Model of the differential processing of the CAPA prohormone


We are establishing an atlas of peptidergic neurons within the ventral ganglion of the Drosophila larva, using immunostainings and confocal 3D reconstructions. To better characterize the peptide inventory of identified peptidergic neurons, we also rely on direct peptide profiling by MALDI-TOF and MALDI-TOF-TOF mass spectrometry. This technique allows in addition the characterization of the often complex post-translational peptide processing.



Publications


Homberg U (2004) In search of the sky compasss in the insect brain. Naturwissenschaften 91:199-208

Homberg U (2004) Multisensory processing in the insect brain. In: TA Christensen (ed) Advances in Insect Sensory Neuroscience. CRC Press, Boca Raton, pp. 3-25

Homberg U, Hofer S, Mappes M, Vitzthum H, Pfeiffer K, Gebhardt S, Müller M, Paech A (2004) Neurobiology of polarization vision in the locust Schistocerca gregaria. Acta Biol Hung 55:81-89

Mappes M, Homberg U (2004) Behavioral analysis of polarization vision in tethered flying locusts. J Comp Physiol A 190:61-68

Schachtner J, Trosowski B, D´Hanis W, Stubner S, Homberg U (2004) Development and steroid regulation of RFamide immunoreactivity in antennal-lobe neurons of the sphinx moth Manduca sexta. J Exp Biol 207:2380-2400

Gebhardt S, Homberg U (2004) Immunocytochemistry of histamine in the brain of the locust Schistocerca gregaria. Cell Tissue Res 317:195-205

Homberg U, Brandl C, Clynen E, Schoofs L, Veenstra JA (2004) Mas-allatotropin/Lom-AG-myotropin I immunostaining in the brain of the locust, Schistocerca gregaria. Cell Tissue Res 318:439-457

Schachtner J, Hütteroth W, Nighorn A, Honegger HW (2004) Cu, Zn-superoxide dismutase (SOD)-like immunoreactivity in the metamorphosing brain of the sphinx moth Manduca sexta. J Comp Neurol 469:141-152

Predel R, Wegener C, Russell WK, Tichy SE, Russell DH, Nachman RJ (2004) Peptidomics of CNS-associated neurohemal systems of Drosophila: a mass spectrometric survey of peptides from individual flies. J Comp Neurol 474:379-392.

Wegener C, Hamasaka Y, Nässel DR (2004) Acetylcholine increases intracellular Ca2+ via nicotinic receptors in cultured PDF-containing clock neurons of Drosophila. J Neurophysiol 91: 912-923.

Huetteroth W, Schachtner J (2005) Standard three-dimensional glomeruli of the Manduca sexta antennal lobe: a tool to study both developmental and adult neuronal plasticity. Cell Tissue Res 319:513-524

Michaelis T, Watanabe T, Natt O, Boretius S, Frahm J, Utz S, Schachtner J (2005) In vivo 3D MRI of insect brain: Cerebral development during metamorphosis of Manduca sexta. Neuroimage 24:596-602

Utz S, Schachtner J (2005) Development of A-type allatostatin immunoreactivity in the antennal lobe of the sphinx moth Manduca sexta. Cell Tissue Res 320:149-162


Kurylas AE, Ott SR, Schachtner J, Elphick MR, Williams L, Homberg U (2005) Localization of nitric oxide synthase in the central complex and surrounding midbrain neuropils of the locust Schistocerca gregaria. J Comp Neurol 484:206-223

Hamasaka Y, Mohrherr C, Predel R, Wegener C (2005): Chronobiological quantification and mass spectrometric characterisation of PDF-immuno-reactive material in the cockroach Leucophaea maderae. J Insect Sci 5:43

Hamasaka Y, Wegener C, Nässel DR (2005): GABA modulates Drosophila circadian clock neurons via GABAB receptors and decreases in calcium. J Neurobiol 65:225-240.

Hofer S, Dircksen H, Tollbäck P, Homberg U (2005) Novel insect orcokinins: characterization and neuronal distribution in the brains of selected dicondylian insects. J Comp Neurol 490:57-71

Pfeiffer K, Kinoshita M, Homberg U (2005) Polarization-sensitive and light-sensitive neurons in two parallel pathways passing through the anterior optic tubercle in the locust brain. J Neurophysiol 94:3903-3915

Schachtner J, Schmidt M, Homberg U (2005) Organization and evolutionary trends of primary olfactory brain centers in Tetraconata (Crustacea + Hexapoda). Arthropod Struct Dev 34:257-299

Hofer S, Homberg U (2006) Orcokinin immunoreactivity in the accessory medulla of the cockroach Leucophaea maderae. Cell Tissue Res, in press.

González-Santos J, Pollák E, Rexer KH, Molnár L, Wegener C: Morphology and metamorphosis of the peptidergic Va neurons and the median nerve system of the fruit fly, Drosophila melanogaster. Submitted.

Vömel M, Wegener C (2006) Acetylcholine and glutamate induce intracellular Ca2+-rises in CCAP-expressing neurons of Drosophila melanogaster. Pesticides, in press.

Wegener C, Reinl T, Jänsch L, Predel R (2006) Direct mass spectrometric profiling and fragmentation in larval peptide hormone release sites of Drosophila melanogaster reveals tagma-specific peptide expression and differential processing. J Neurochem DOI: 10.1111/j.1471-4159.2005.03634.x

Crawford MJ, Thomsen-Zieger N, Ray M, Schachtner J, Roos DS, Seeber F. Toxoplasma gondii is a lipoic acid auxotroph due to secondary loss of its mitochondrial lipoate synthesis machinery. Submitted.


Diploma Theses


Gräbner M (2005) Metamorphose des Antennallobus der Honigbiene Apis mellifera: Entwicklung von A-Typ Allatostatin- und Synapsin-Immunreaktivität und das NO/cGMP-Signalsystem

Heinze S (2005) Charakterisierung von polarisationssensitiven Interneuronen aus dem Zentralkomplex der Wüstenheuschrecke Schistocerca gregaria

Kepura F (2005) In vivo-Imaging am sich entwickelnden Antennallobus des Tabakschwärmers Manduca sexta



Doctoral Theses


Hofer S (2004) Das circadiane System der Schabe Leucophaea maderae: Die Rolle des Neuropeptides Orcokinin und die Synchronisation der Inneren Uhr durch Licht



Grants


DFG HO 950/13-2 „Analyse des Polarisations-Sehsystems der Heuschrecke Schistocerca gregaria“, awarded 29.7.2002 for 2 years

DFG HO 950/14-1 “Topographische Organisation des Zentralkörpers im Gehirn der Heuschrecke Schistocerca gregaria“, awarded 16.4.2002 for 3 years

DFG HO 950/14-2 “Topographische Organisation des Zentralkörpers im Gehirn der Heuschrecke Schistocerca gregaria”, awarded 18.8.2004 for 1 year

DFG HO 950/16-1 „Kartierung und funktionelle Charakterisierung visueller Bahnen zum Zentralkomplex im Gehirn der Heuschrecke Schistocerca gregaria“, awarded 20.10.2004 for 2 years

DFG We 2652/2-1/2 (Emmy Noether-Programm Phase II) „Physiologie und Regulation der Peptidausschüttung aus den Neurohämalorganen des zentralen Nervensystems der Insekten“, awarded 6.3.2003 for 3 years

Fonds der Chemischen Industrie, Financial support for young investigators, awarded 20.11.2003 to Christian Wegener



Editorial Boards


Homberg:

Editorial Board, Zoology, Fischer Verlag

Advisory Board, Arthropod Structure & Development, Elsevier



Members of the Group


Stanley Heinze, PhD student
Karl-Heinz Herklotz, technician
Sabine Hofer, PhD student
Uwe Homberg, professor
Sabine Jesberg, technician
Angela Kurylas, PhD student
Martina Mappes, PhD student
Keram Pfeiffer, PhD student
Ulrike Träger, PhD student

Sandy Fastner, Diploma student
Anton Gorbashov, Diploma student
Jonathan González Santos, PhD student
Matthias Vömel, PhD student
Christian Wegener, junior research group leader

Sandra Utz, PhD student
Wolf Huetteroth, PhD student
Frauke Kepura, PhD student
Karin Müller, technician
Joachim Schachtner, research group leader

Address


Prof. Dr. Uwe Homberg
Fachbereich Biologie
Tierphysiologie
Universität Marburg
D-35032 Marburg
Germany
Tel. +49-6421-28-23402
Fax. +49-6421-28-28941
E-mail: homberg@staff.uni-marburg.de

Zuletzt aktualisiert: 17.05.2006 · dohle

 
 
 
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