Pharmacological approaches to nitric oxide signalling during neural development of locusts and other model insects

Archives of Insect Biochemistry and Physiology

Volumn 64, Issue 1, 2007, Pages 43-58

  Bicker, Gerd ^a  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

Author keywords

Cell migration; Cell proliferation; cGMP; Growth cone; Pest insects; Pioneer neuron

Indexed keywords

CYCLIC GMP; NITRIC OXIDE;

ANIMAL; CELL MOTION; CELL PROLIFERATION; CYTOSKELETON; GRASSHOPPER; GROWTH CONE; INTESTINE INNERVATION; METABOLISM; NERVE CELL PLASTICITY; PHOTORECEPTOR; PHYSIOLOGY; PRENATAL DEVELOPMENT; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CELL MOVEMENT; CELL PROLIFERATION; CYCLIC GMP; CYTOSKELETON; ENTERIC NERVOUS SYSTEM; GRASSHOPPERS; GROWTH CONES; NEURONAL PLASTICITY; NITRIC OXIDE; PHOTORECEPTORS, INVERTEBRATE; SIGNAL TRANSDUCTION;

ACHETA; HEXAPODA; LEPIDOPTERA; LOCUSTA; MAMMALIA; MANDUCA; ORTHOPTERA; SCHISTOCERCA; VERTEBRATA;

EID: 33846546130     PISSN: 07394462     EISSN: 15206327     Source Type: Journal    
DOI: 10.1002/arch.20161     Document Type: Review

References (97)

1. Ayali A. 2004. The insect frontal ganglion and stomatogastric pattern generator networks. Neurosignals 13:20-36.
2. Ball EE, Truman JW. 1998. Developing grasshopper neurons show variable levels of guanylyl cyclase activity on arrival of their targets. J Comp Neurol 394:1-13.
3. Bate CM. 1976. Pioneer neurones in an insect embryo. Nature 260:54-56.
4. Bellamy TC, Garthwaite J. 2002. Pharmacology of the nitric oxide receptor, soluble guanylyl cyclase, in cerebellar cells. Br J Pharmacol 136:95-103.
5. Bentley D, O'Connor TP. 1992. Guidance and steering of peripheral pioneer growth cones in grasshopper embryos. In: Letourneau C, Kater SB, Macagno, ER, editors. The nerve growth cone. New York: Raven Press Ltd. p 265-282.
6. Berlot K, Goodman CS. 1984. Guidance of peripheral pioneer neurons in the grasshopper: adhesive hierarchy of epithelial and neuronal surfaces. Science 223:493-496.
7. Bicker G. 1999. Histochemistry of classical neurotransmitters in antennal lobes and mushroom bodies of the honeybee. Microsc Res Tech 45:174-183.
8. Bicker G. 2001. Nitric oxide: an unconventional messenger in the nervous system of an orthopteroid insect. Arch Insect Biochem Physiol 48:100-110.
9. Bicker G, Schmachtenberg O. 1997. Cytochemical evidence for nitric oxide/cyclic GMP signal transmission in the visual system of the locust. Eur J Neurosci 9:189-193.
10. Bicker G, Schmachtenberg O, De Vente J. 1996. The nitric oxide/cyclic GMP messenger system in olfactory pathways of the locust brain. Eur J Neurosci 8:2635-2643.
11. Bicker G, Schmachtenberg O, De Vente J. 1997. Geometric considerations of nitric oxide-cyclic GMP signalling in the glomerular neuropil of the locust antennal lobe. Proc R Soc Lond B 264:1177-1181.
12. Bicker G, Naujock M, Haase A. 2004. Cellular expression patterns of acetylcholinesterase activity during grasshopper development. Cell Tissue Res 317:207-220.
13. Boehning D, Snyder SH. 2003. Novel neural modulators. Annu Rev Neurosci 26:105-131.
14. Boyan GS, Williams JLD. 2004. Embryonic development of the sensory innervation of the antenna of the grasshopper Schistocerca gregaria. Arthropod Struct Dev 33:381-397.
15. Boyan G, Therianos S, Williams JL, Reichert H. 1995. Axogenesis in the embryonic brain of the grasshopper Schistocerca gregaria: an identified cell analysis of early brain development. Development 121:75-86.
16. Bredt DS, Snyder SH. 1992. Nitric oxide, a novel neuronal messenger. Neuron 8:3-11.
17. Brown C, Pan X, Hassid A. 1999. Nitric oxide and C-type atrial natriuretic peptide stimulate primary aortic smooth muscle cell migration via a cGMP-dependent mechanism: relationship to microfilament dissociation and altered cell morphology. Circ Res 84:655-667.
18. Bullerjahn A, Pflüger HJ. 2003. The distribution of putative nitric oxide releasing neurones in the locust abdominal nervous system: a comparison of NADPHd histochemistry and NOS-immunocytochemistry. Zoology 106:3-17.
19. Burrows M. 1996. The neurobiology of an insect brain. New York: Oxford University Press.
20. Cayre M, Strambi C, Strambi A. 1994. Neurogenesis in adult insect brain and its hormonal control. Nature 368:57-59
21. Cayre M, Malaterre J, Scotto-Lomassese S, Holstein GR, Martinelli GP, ForniC, Nicolas S, Aouane A, Strambi C, Strambi A. 2005. A role for nitric oxide in sensory-induced neurogenesis in an adult insect brain. Eur J Neurosci 21:2893-2902.
22. Champlin DT, Truman JW. 2000. Ecdysteroid coordinates optic lobe neurogenesis via a nitric oxide signaling pathway. Development 127:3543-3551.
23. Chilton JK. 2006. Molecular mechanisms of axon guidance. Dev Biol 292:13-24.
24. Christie AE, Edwards JM, Cherny E, Clason TA, Graubard K. 2003. Immunocytochemical evidence for nitric oxide- and carbon monoxide- producingneurons in the stomatogastric nervous system of the crayfish Cherax quadricarinatus. J Comp Neurol 467:293-306.
25. Copenhaver PF, Taghert PH. 1989. Development of the enteric nervous system in the moth. I. Diversity of celltypes and the embryonic expression of FMRFamide-related neuropeptides. Dev Biol 131:70-84.
26. Copenhaver PF, Horgan AM, Combes S. 1996. An identified set of visceral muscle bands is essential for the guidance of migratory neurons in the enteric nervous system of Manduca sexta. Dev Biol 179:412-426.
27. Currie DA, de Vente J, Moody WJ. 2006. Developmental appearance of cyclic guanosine monophosphate (cGMP) production and nitric oxide responsiveness in embryonic mouse cortex and striatum. Dev Dyn 235:1668-1677.
28. Demyanenko GP, Halberstadt AI, Pryzwansky KB, Werner C, Hofmann F, Maness PF. 2005. Abnormal neocortical development in mice lacking cGMP-dependent protein kinase I. Brain Res Dev Brain Res 160:1-8.
29. De Vente J, Steinbusch HWM, Schipper J. 1987. A new approach to immunocytochemistiy of 3′,5′-cyclic guanosine monophosphate: preparation, specificity, and initial application of a new antiserum against formaldehyde-fixed 3′,5′-cyclic guanosine monophosphate. Neuroscience 22:361-373.
30. Dickson B J. 2002. Molecular mechanisms of axon guidance. Science 298:959-964.
31. Ding JD, Burette A, Weinberg RJ. 2005. Expression of soluble guanylyl cyclase in rat cerebral cortex during postnatal development. J Comp Neurol 485:255-265.
32. Elphick MR, Rayne RC, Riveros-Moreno V, Moncada S, O'Shea M, 1995. Nitric oxide synthesis in locust olfactory interneurones. J Exp Biol 198:821-829.
33. Enikolopov G, Banerji J, Kuzin B. 1999. Nitric oxide and Drosophila development. Cell Death Differ 6:956-963.
34. Fahrbach SE. 2006. Structure of the mushroom bodies of the insect brain. Annu Rev Entomol 51:209-232.
35. Ganfornina MD, Sanchez D, Bastiani MJ. 1996. Embryonic development of the enteric nervous system of the grasshopper Schistocerca americana. J Comp Neurol 372:581-596.
36. Garthwaite J, Boulton CL. 1995. Nitric oxide signalling in the central nervous system. Annu Rev Physiol 57:683-706.
37. Gibbs SM, Truman WT. 1998. Nitric oxide and cyclic GMP regulate retinal patterning in the optic lobe of Drosophila. Neuron 20:83-93.
38. Gibbs SM, Becker A, Hardy RW, Truman JW. 2001. Soluble guanylate cyclase is required during development for visual system function in Drosophila. J Neurosci 21:7705-7714.
39. Gibson NJ, Nighorn A. 2000. Expression of nitric oxide synthase and soluble guanylyl cyclase in the developing olfactory system of Manduca sexta. J Comp Neurol 422:191-205.
40. Gibson NJ, Rössler W, Nighorn AJ, Oland LA, Hildebrand JG, Tolbert LP. 2001. Neuron-glia communication via nitric oxide is essential in establishing antennal-lobe structure in Manduca sexta. Dev Biol 240:326-339.
41. Godfrey EW, Schwarte RC. 2003. The role of nitric oxide signaling in the formation of the neuromuscularjunction. J Neurocytol 32:591-602.
42. Goodman CS, Bate CM. 1981. Neuronal development in the grasshopper. Trends Neurosci 4:163-169.
43. Grueber WB, Truman JW. 1999. Development and organization of a nitric-oxide-sensitive peripheral neuralplexus in larvae of the moth, Manduca sexta. J Comp Neurol 404:127-141.
44. Haase A, Bicker G. 2003. Nitric oxide and cyclic nucleotides are regulators of neuronal migration in an insect embryo. Development 130:3977-3987.
45. Hartenstein V. 1997. Development of the insect stomatogastric nervous system. Trends Neurosci 20:421-427.
46. Hawkins RD, Son H, Arancio O. 1998. Nitric oxide as a retrograde messenger during long-term potentiation in hippocampus. Prog Brain Res 118:155-172.
47. Heisenberg M. 2003. Mushroom body memoir: from maps to models. Nat Rev Neurosci 4:266-275.
48. Ho RK, Goodman CS. 1982. Peripheral pathways are pioneered by an array of central and peripheral neurones in grasshopper embryos. Nature 297:404-406.
49. Isbister CM, Tsai A, Wong ST, Kolodkin AL, O'Connor TP. 1999. Discrete roles for secreted and transmembrane semaphorins in neuronal growth cone guidance in vivo. Development 126:2007-2019.
50. Keilhoff G, Fansa H, Wolf G. 2002. Differences in peripheral nerve degeneration/regeneration between wild-type and neuronal nitric oxide synthase knockout mice. J Neurosci Res 68:432-441.
51. Keynes RG, Garthwaite J. 2004. Nitric oxide and its role in ischaemic brain injury. Curr Mol Med 4:179-191.
52. Knipp S, Bicker G. 2006. The gaseous messenger molecules CO and NO regulate neuronal cell migration in an insect embryo. FENS Forum Abstracts A122.14.
53. Krumenacker JS, Murad F. 2006. NO-cGMP signaling in development and stem cells. Mol Genet Metab 87:311-214.
54. Kuzin B, Roberts I, Peunova N, Enikolopov G. 1996. Nitric oxide regulates cell proliferation during Drosophila development. Cell 87:639-649.
55. Kuzin B, Regulski M, Stasiv Y, Scheinker V, Tully T, Enikolopov G. 2000. Nitric oxide interacts with the retinoblastoma pathway to control eyedevelopment in Drosophila. Curr Biol 10:459-462.
56. Lauffenburger DA, Horwitz AF. 1996. Cell migration: a physically integrated molecular process. Cell 84:359-369.
57. Legg AT, O'Connor TP. 2003. Gradients and growth cone guidance of grasshopper neurons. J Histochem Cytochem 51:445-454.
58. Lucas KA, Pitari GM, Kazerounian S, Ruiz-Stewart I, Park J, Schulz S,Chepenik KP, Waldman SA. 2000. Guanylyl cyclases and signaling by cyclic GMP. Pharmacol Rev 52:375-414.
59. Martinez-Guijarro FJ, Gutierrez-Mecinas M, Gracia-Llanes FJ, Marques-Mari AI, Varea E, Nachev J, Blasco-Ibáñez JM, Crespo C. 2006. Migrating neuroblasts of the rostral migratory stream are putative targets for the action of nitric oxide. FENS Forum Abstracts A122.16.
60. Matsumoto T, Nakane M, Pollock JS, Kuk JE, Förstermann U. 1993. A correlation between soluble brain nitric oxide synthase and NADPH-diaphorase activity is only seen after exposure of the tissue to fixative. Neurosci Lett 155:61-64.
61. Moreno-Lopez B, Romero-Grimaldi C, Noval JA, Murillo-Carretero M, Matarredona ER, Estrada C. 2004. Nitric oxide is a physiological inhibitor of neurogenesis in the adult mouse subventricular zone and olfactory bulb. J Neurosci 24:85-95.
62. Moroz LL. 2001. Gaseous transmission across time and species. Amer Zool 41:304-320.
63. Morton DB. 2004. Atypical soluble guanylyl cyclases in Drosophila can function as molecular oxygen sensors. J Biol Chem 279:50651-50653.
64. Müller U, Bicker G. 1994. Calcium activated release of nitric oxide and cellular distribution of nitric oxide synthesizing neurons in the nervous system of the locust. J Neurosci 14:7521-7528.
65. Okamoto K, Nagai T, Miyawaki A, Hayashi Y. 2004. Rapid and persistent modulation of actin dynamics regulates postsynapticreorganization underlying bidirectional plasticity. Nat Neurosci 7:1104-1112.
66. Ott SR, Burrows M. 1999. NADPH diaphorase histochemistry in the thoracic ganglia of locusts, crickets, and cockroaches: species differences and the impact of fixation. J Comp Neurol 410:387-397.
67. Ott SR, Delago A, Elphick MR. 2004. An evolutionarily conserved mechanism for sensitization of soluble guanylylcyclase reveals extensive nitric oxide-mediated upregulation of cyclic GMP in insect brain. Eur J Neurosci 20:1231-1244.
68. Packer MA, Stasiv Y, Benraiss A, Chmielnicki E, Grinberg A, Westphal H, Goldman SA, Enikolopov G. 2003. Nitric oxide negatively regulates mammalian adult neurogenesis. Proc Natl Acad Sci USA 100:9566-9571.
69. Pätschke A, Bicker G. 2006. Influence of NO/cGMP on the growth of peripheral pioneer neurons in the grasshopper. Berlin, Germany: Neuro-DoWo Abstracts.
70. Pätschke A, Bicker G, Stern M. 2004. Axonal regeneration of proctolinergic neurons in the central nervous system of the locust. Brain Res Dev Brain Res 150:73-76.
71. Polleux F, Morrow T, Ghosh A. 2000. Semaphorin 3A is a chemoattractant for cortical apical dendrites. Nature 404:557-573.
72. 2+/calmodulin dependent nitric oxide synthase. Proc Natl Acad Sci USA 92:9072-9076.
73. Regulski M, Stasiv Y, Tully T, Enikolopov G. 2004. Essential function of nitric oxide synthase in Drosophila. Curr Biol. 14:881-882.
74. Santacana M, Uttenthal LO, Bentura ML, Fernandez AP, Serrano J, Martinez deVelasco J, Alonso D, Martinez-Murillo R, Rodrigo J. 1998. Expression of neuronal nitric oxide synthase during embryonic development of the rat cerebral cortex. Brain Res Dev Brain Res 111:205-222.
75. th German Neurosci Soc Conf Stuttgart. New York: Thieme Verlag. 1999 p.
76. Schachtner J, Klaassen L, Truman JW. 1998. Metamorphic control of cyclic guanosine monophosphate expression in the nervous system of the tobacco hornworm, Manduca sexta. J Comp Neurol 396:238-252.
77. Schachtner J, Homberg U, Truman JW. 1999. Regulation of cyclic GMP elevation in the developing lobe of the sphinx moth, Manduca sexta. J Neurobiol 41:359-375.
78. Seidel C, Bicker G. 2000. Nitric oxide and cyclic GMP influence axonogenesis of antennal pioneer neurons. Development 127:4541-4549.
79. Seidel C, Bicker G. 2002. Developmental expression of nitric oxide/cyclic GMP signaling pathways in the brain of the embryonic grasshopper. Brain Res Dev Brain Res 138:71-79.
80. Song H, Poo MM. 2001. The cell biology of neuronal navigation. Nat Cell Biol 3:81-88.
81. Stamler JS, Toone EJ, Lipton SA, Sucher NJ. 1997. (S)NO Signals: translocation, regulation, and a consensus motif. Neuron 18:691-696.
82. th DZG Meeting, Münster, Germany.
83. Stern M, Knipp S, Bicker G. 2006. Embryonic differentiation of serotonin-containing neurons in the enteric nervous system of the locust (Locusta migratoria) J Comp Neurol (in press)
84. Strausfeld NJ, Hansen L, Li Y, Gomez RS, Ito K. 1998. Evolution, discovery, and interpretations of arthropod mushroom bodies. Learn Mem 5:11-37.
85. Tanaka M, Yoshida S, Yano M, Hanaoka F. 1994. Roles of endogenous nitric oxide in cerebellar cortical evelopment in slice cultures. Neuroreport 5:2049-2052.
86. Tolbert LP, Oland LA, Christensen TC, Goriely AR. 2003. Neuronal and glial morphology in olfactory systems: significance for information-processing and underlying developmental mechanisms. Brain Mind 4:27-49.
87. Trimm KR, Rehder V. 2004. Nitric oxide acts as a slow-down and search signal in developing neurites. Eur J Neurosci 19:809-818.
88. Truman JW, De Vente J, Ball EE. 1996. Nitric oxide-sensitive guanylate cyclase activity is associated with the maturational phase of neuronal development of insects. Development 122:3949-3958.
89. Van Wagenen S, Rehder V. 1999. Regulation of neuronal growth cone filopodia by nitric oxide. J Neurobiol 39:168-185.
90. Van Wagenen S, Rehder V. 2001. Regulation of neuronal growth cone filopodia by nitric oxide depends on soluble guanylyl cyclase. J Neurobiol 46:206-219.
91. Wang HG, Lu FM, Jin I, Udo H, Kandel ER, de Vente J, Walter U, Lohmann SM,Hawkins RD, Antonova I. 2005. Presynaptic and postsynaptic roles of NO, cGK, and RhoA in long-lasting potentiation and aggregation of synaptic proteins. Neuron 45:389-403.
92. 2+ release. Eur J Neurosci 22:3006-3016.
93. Wildemann B, Bicker G. 1999a. Developmental expression of nitric oxide / cyclic GMP synthesizing cells in the nervous system of Drosophila melanogaster. J Neurobiol 38:1-15.
94. Wildemann B, Bicker G. 1999b. Nitric oxide and cyclic GMP induce vesicle release at Drosophila neuromuscular junction. J Neurobiol 39:337-346.
95. Wright JW, Copenhaver PF. 2000. Different isoforms of fasciclin II play distinct roles in the guidance of neuronal migration during insect embryogenesis. Dev Biol 225:59-78.
96. Wright JW, Schwinof KM, Snyder MA, Copenhaver F. 1998. A delayed role for nitric oxide-sensitive guanylate cyclases in a migratory population of embryonic neurons. Dev Biol 204:15-33.
97. Yamamoto T, Yao Y, Harumi T, Suzuki N. 2003. Localization of the nitric oxide/cGMP signaling pathway-related genes and influences of morpholino knock-down of soluble guanylyl cyclase on medaka fish embryogenesis. Zool Sci 20:181-191.