Home LiteratureArticle Details
PMID: 12657682 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Adenylate cyclase 1 as a key actor in the refinement of retinal projection maps.

The Journal of neuroscience : the official journal of the Society for Neuroscience ·Vol. 23 ·No. 6 ·2003-03-15 ·Pages 2228-38

Ravary A, Muzerelle A, Hervé D, Pascoli V, Ba-Charvet KN, Girault JA, Welker E, Gaspar P

Abstract

cAMP occupies a strategic position to control neuronal responses to a large variety of developmental cues. We have analyzed the role of calcium-stimulated adenylate cyclase 1 (AC1) in the development of retinal topographic maps. AC1 is expressed in retinal ganglion cells (RGCs) from embryonic day 15 to adulthood with a peak during the first postnatal week. At that time, the other calcium-stimulated AC, AC8, is expressed in the superior colliculus (SC) but not in the RGCs. In mice of the barrelless strain, which carry an inactivating mutation of the AC1 gene, calcium-stimulated AC activity is reduced by 40-60% in the SC and retina. RGC projection maps were analyzed with a variety of anterograde and retrograde tracers. After an initially normal development until postnatal day 3, retinal fibers from the ipsilateral and contralateral eye fail to segregate into eye-specific domains in the lateral geniculate nucleus and the SC. Topographic defects in the fine tuning of the retinotectal and retinogeniculate maps are also observed with abnormalities in the confinement of the retinal axon arbors in the anteroposterior and mediolateral dimensions. This is attributable to the lack of elimination of misplaced axon collaterals and to the maintenance of a transient ipsilateral projection. These results establish an essential role of AC1 in the fine patterning of the retinal map. Calcium-modulated cAMP production in the RGCs could constitute an important link between activity-dependent changes and the anatomical restructuring of the retinal terminal arbors within central targets.

MeSH Terms
Adenylyl Cyclases/genetics,physiology Animals Axons/enzymology,physiology Cell Count Geniculate Bodies/cytology,embryology,enzymology,growth & development In Situ Hybridization Isoenzymes/genetics,physiology Mice Mice, Neurologic Mutants RNA, Messenger/analysis,biosynthesis Retina/cytology,enzymology Retinal Ganglion Cells/cytology,enzymology Superior Colliculi/cytology,embryology,enzymology,growth & development Visual Pathways/cytology,embryology,enzymology,growth & development
Chemicals
Isoenzymes RNA, Messenger Adenylyl Cyclases adenylyl cyclase 1
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Ravary Anne
Institut National de la Santé et de la Recherche Médicale Unite 106, Hôpital Pitié-Salpêtrière, 75651 Paris, France.
Muzerelle Aude
Hervé Denis
Pascoli Vincent
Ba-Charvet Kim Nguyen
Girault Jean-Antoine
Welker Egbert
Gaspar Patricia
References (56)
56 references, click to expand
  1. Genetic control of retinal ganglion cell projections.
    J Comp Neurol. 1978 Dec 1;182(3):399-421 PMID: 102659
  2. Excess of serotonin (5-HT) alters the segregation of ispilateral and contralateral retinal projections in monoamine oxidase A knock-out mice: possible role of 5-HT uptake in retinal ganglion cells during development.
    J Neurosci. 1999 Aug 15;19(16):7007-24 PMID: 10436056
  3. Calcium-stimulated adenylyl cyclase activity is critical for hippocampus-dependent long-term memory and late phase LTP.
    Neuron. 1999 Aug;23(4):787-98 PMID: 10482244
  4. Dynamics of retinal waves are controlled by cyclic AMP.
    Neuron. 1999 Nov;24(3):673-85 PMID: 10595518
  5. Genetic analysis of ephrin-A2 and ephrin-A5 shows their requirement in multiple aspects of retinocollicular mapping.
    Neuron. 2000 Mar;25(3):563-74 PMID: 10774725
  6. Altered stress-induced anxiety in adenylyl cyclase type VIII-deficient mice.
    J Neurosci. 2000 Jul 1;20(13):4809-20 PMID: 10864938
  7. The multiple decisions made by growth cones of RGCs as they navigate from the retina to the tectum in Xenopus embryos.
    J Neurobiol. 2000 Aug;44(2):246-59 PMID: 10934326
  8. Growth cone form, behavior, and interactions in vivo: retinal axon pathfinding as a model.
    J Neurobiol. 2000 Aug;44(2):260-70 PMID: 10934327
  9. Excessive activation of serotonin (5-HT) 1B receptors disrupts the formation of sensory maps in monoamine oxidase a and 5-ht transporter knock-out mice.
    J Neurosci. 2001 Feb 1;21(3):884-96 PMID: 11157075
  10. Multiple roles of EPH receptors and ephrins in neural development.
    Nat Rev Neurosci. 2001 Mar;2(3):155-64 PMID: 11256076
  11. Requirement of the nicotinic acetylcholine receptor beta 2 subunit for the anatomical and functional development of the visual system.
    Proc Natl Acad Sci U S A. 2001 May 22;98(11):6453-8 PMID: 11344259
  12. Neuronal cyclic AMP controls the developmental loss in ability of axons to regenerate.
    J Neurosci. 2001 Jul 1;21(13):4731-9 PMID: 11425900
  13. The CRE/CREB pathway is transiently expressed in thalamic circuit development and contributes to refinement of retinogeniculate axons.
    Neuron. 2001 Aug 16;31(3):409-20 PMID: 11516398
  14. An instructive role for retinal waves in the development of retinogeniculate connectivity.
    Neuron. 2002 Jan 31;33(3):357-67 PMID: 11832224
  15. Lack of 5-HT(1B) receptor and of serotonin transporter have different effects on the segregation of retinal axons in the lateral geniculate nucleus compared to the superior colliculus.
    Neuroscience. 2002;111(3):597-610 PMID: 12031347
  16. Retinogeniculate axons undergo eye-specific segregation in the absence of eye-specific layers.
    J Neurosci. 2002 Jul 1;22(13):5259-64 PMID: 12097474
  17. EphB forward signaling controls directional branch extension and arborization required for dorsal-ventral retinotopic mapping.
    Neuron. 2002 Aug 1;35(3):475-87 PMID: 12165470
  18. Refinement of thalamocortical arbors and emergence of barrel domains in the primary somatosensory cortex: a study of normal and monoamine oxidase a knock-out mice.
    J Neurosci. 2002 Oct 1;22(19):8541-52 PMID: 12351728
  19. Development of topographic order in the mammalian retinocollicular projection.
    J Neurosci. 1992 Apr;12(4):1212-32 PMID: 1313491
  20. Bound and determined: a computer program for making buffers of defined ion concentrations.
    Anal Biochem. 1992 Feb 14;201(1):119-26 PMID: 1621949
  21. Biochemical studies of stimulus convergence during classical conditioning in Aplysia: dual regulation of adenylate cyclase by Ca2+/calmodulin and transmitter.
    J Neurosci. 1991 Sep;11(9):2655-65 PMID: 1679120
  22. Distribution of mRNA for the calmodulin-sensitive adenylate cyclase in rat brain: expression in areas associated with learning and memory.
    Neuron. 1991 Mar;6(3):431-43 PMID: 2001286
  23. Postnatal changes in arborization patterns of murine retinocollicular axons.
    J Comp Neurol. 1986 Apr 15;246(3):395-408 PMID: 3700722
  24. Selective breeding for variations in patterns of mystacial vibrissae of mice. Bilaterally symmetrical strains derived from ICR stock.
    J Hered. 1986 Mar-Apr;77(2):66-82 PMID: 3711643
  25. Topographic targeting errors in the retinocollicular projection and their elimination by selective ganglion cell death.
    J Neurosci. 1986 Dec;6(12):3692-705 PMID: 3794796
  26. Fate of uncrossed retinal projections following early or late prenatal monocular enucleation in the mouse.
    J Comp Neurol. 1987 Jan 1;255(1):97-109 PMID: 3819012
  27. A highly sensitive adenylate cyclase assay.
    Anal Biochem. 1974 Apr;58(2):541-8 PMID: 4827395
  28. An electrophysiological study of the visual projection to the superior colliculus of the rat.
    J Comp Neurol. 1966 Aug;127(4):435-44 PMID: 5968989
  29. Cell death during differentiation of the retina in the mouse.
    J Comp Neurol. 1984 Nov 1;229(3):362-73 PMID: 6501608
  30. Prenatal and postnatal development of retinogeniculate and retinocollicular projections in the mouse.
    J Comp Neurol. 1984 Dec 20;230(4):552-75 PMID: 6520251
  31. Ganglion cell death during development of ipsilateral retino-collicular projection in golden hamster.
    Nature. 1984 Mar 22-28;308(5957):362-5 PMID: 6709042
  32. Origins of crossed and uncrossed retinal projections in pigmented and albino mice.
    J Comp Neurol. 1980 Jun;191(3):383-412 PMID: 7410600
  33. Characterization of the signaling interactions that promote the survival and growth of developing retinal ganglion cells in culture.
    Neuron. 1995 Oct;15(4):805-19 PMID: 7576630
  34. Adenylyl cyclases and the interaction between calcium and cAMP signalling.
    Nature. 1995 Mar 30;374(6521):421-4 PMID: 7700350
  35. Mediation of hippocampal mossy fiber long-term potentiation by cyclic AMP.
    Science. 1994 Sep 23;265(5180):1878-82 PMID: 7916482
  36. cAMP contributes to mossy fiber LTP by initiating both a covalently mediated early phase and macromolecular synthesis-dependent late phase.
    Cell. 1994 Oct 7;79(1):69-79 PMID: 7923379
  37. Type VIII adenylyl cyclase. A Ca2+/calmodulin-stimulated enzyme expressed in discrete regions of rat brain.
    J Biol Chem. 1994 Apr 22;269(16):12190-5 PMID: 8163524
  38. Signal recognition and integration by Gs-stimulated adenylyl cyclases.
    Curr Opin Neurobiol. 1993 Jun;3(3):345-51 PMID: 8369627
  39. Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons.
    Science. 1993 Jun 11;260(5114):1661-4 PMID: 8389057
  40. Altered sensory processing in the somatosensory cortex of the mouse mutant barrelless.
    Science. 1996 Mar 29;271(5257):1864-7 PMID: 8596955
  41. Contrasting effects of protein synthesis inhibition and of cyclic AMP on apoptosis in the developing retina.
    Development. 1996 May;122(5):1439-48 PMID: 8625832
  42. Adenylate cyclases: critical foci in neuronal signaling.
    Trends Neurosci. 1995 Dec;18(12):536-42 PMID: 8638294
  43. Differential expression of type I, II, and V adenylyl cyclase gene in the postnatal developing rat brain.
    J Neurochem. 1997 Feb;68(2):498-506 PMID: 9003034
  44. The Eph family in retinal axon guidance.
    Curr Opin Neurobiol. 1997 Feb;7(1):75-80 PMID: 9039788
  45. Emergence of order in visual system development.
    J Physiol Paris. 1996;90(3-4):141-50 PMID: 9116657
  46. cAMP-induced switching in turning direction of nerve growth cones.
    Nature. 1997 Jul 17;388(6639):275-9 PMID: 9230436
  47. Competition in retinogeniculate patterning driven by spontaneous activity.
    Science. 1998 Mar 27;279(5359):2108-12 PMID: 9516112
  48. The ephrins and Eph receptors in neural development.
    Annu Rev Neurosci. 1998;21:309-45 PMID: 9530499
  49. Type I adenylyl cyclase mutant mice have impaired mossy fiber long-term potentiation.
    J Neurosci. 1998 May 1;18(9):3186-94 PMID: 9547227
  50. LTP and activity-dependent synaptogenesis: the more alike they are, the more different they become.
    Curr Opin Neurobiol. 1998 Feb;8(1):139-48 PMID: 9568401
  51. Impaired cerebellar long-term potentiation in type I adenylyl cyclase mutant mice.
    Neuron. 1998 Jun;20(6):1199-210 PMID: 9655507
  52. Loss of adenylyl cyclase I activity disrupts patterning of mouse somatosensory cortex.
    Nat Genet. 1998 Jul;19(3):289-91 PMID: 9662407
  53. Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides.
    Science. 1998 Sep 4;281(5382):1515-8 PMID: 9727979
  54. Depolarization and cAMP elevation rapidly recruit TrkB to the plasma membrane of CNS neurons.
    Neuron. 1998 Oct;21(4):681-93 PMID: 9808456
  55. Cell production and cell death in the generation of variation in neuron number.
    J Neurosci. 1998 Dec 1;18(23):9948-53 PMID: 9822750
  56. Transient developmental expression of monoamine transporters in the rodent forebrain.
    J Comp Neurol. 1998 Nov 30;401(4):506-24 PMID: 9826275
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2003-03-15
Pages
2228-38
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6742000
Subset
IM
External Links
PubMed source PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2