Fasciclin II: The NCAM Ortholog in Drosophila melanogaster

  • Lars V. Kristiansen
  • Michael HortschEmail author
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 663)


NCAM-type genes form an evolutionary ancient gene family that is expressed in the developing nervous system of a wide variety of different species, including many invertebrates. In the fruit fly Drosophila melanogaster, Fasciclin II represents the structural and functional ortholog of vertebrate NCAM. The genetic and developmental analysis of the fasII gene and its protein product, Fasciclin II, has uncovered many surprising functional similarities to its vertebrate counterparts and indicates a central, conserved role for NCAM-type proteins in many aspects of nervous system formation. The processes that involve Fasciclin II expression in Drosophila include neuronal differentiation, axonal growth and pathfinding, as well as maturation and plasticity of specific synapses. However, these functions do not solely depend on Fasciclin II-mediated homophilic adhesion. In addition, they require interactions with cytoskeletal elements and the activation of several intracellular signaling cascades, specifically those initiated by the Drosophila EGF- and FGF-receptor tyrosine kinases.


Ig-CAMs Synapse Development Receptor tyrosine kinase Adhesion Axon guidance EGFR FGFR 



The authors would like to acknowledge the financial support by a Civitan Emerging Scholar Award to LVK.


  1. 1.
    Chisholm A, Tessier-Lavigne M (1999) Conservation and divergence of axon guidance mechanisms. Curr Opin Neurobiol 9:603-615PubMedCrossRefGoogle Scholar
  2. 2.
    Grenningloh G, Rehm EJ, Goodman CS (1991) Genetic analysis of growth cone guidance in Drosophila: fasciclin II functions as a neuronal recognition molecule. Cell 67:45-57PubMedCrossRefGoogle Scholar
  3. 3.
    Bieber AJ, Snow PM, Hortsch M et al (1989) Drosophila neuroglian: a member of the immunoglobulin superfamily with extensive homology to the vertebrate neural adhesion molecule L1. Cell 59:447-460PubMedCrossRefGoogle Scholar
  4. 4.
    Zhao G, Hortsch M (1998) The analysis of genomic structures in the L1 family of cell adhesion molecules provides no evidence for exon shuffling events after the separation of arthropod and chordate lineages. Gene 215:47-55PubMedCrossRefGoogle Scholar
  5. 5.
    Hortsch M (2000) Structural and functional evolution of the L1 family: are four adhesion molecules better than one? Mol Cell Neurosci 15:1-10PubMedCrossRefGoogle Scholar
  6. 6.
    Pebusque MJ, Coulier F, Birnbaum D et al (1998) Ancient large-scale genome duplications: phylogenetic and linkage analyses shed light on chordate genome evolution. Mol Biol Evol 15:1145-1159PubMedGoogle Scholar
  7. 7.
    Wang DY, Kumar S, Hedges SB (1999) Divergence time estimates for the early history of animal phyla and the origin of plants, animals and fungi. Proc Biol Sci 266:163-171PubMedCrossRefGoogle Scholar
  8. 8.
    Force A, Lynch M, Pickett FB et al (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531-1545PubMedGoogle Scholar
  9. 9.
    Grenningloh G, Bieber AJ, Rehm EJ et al (1990) Molecular genetics of neuronal recognition in Drosophila: evolution and function of immunoglobulin superfamily cell adhesion molecules. Cold Spring Harb Symp Quant Biol 55:327-340PubMedGoogle Scholar
  10. 10.
    Lin DM, Fetter RD, Kopczynski C et al (1994) Genetic analysis of Fasciclin II in Drosophila: defasciculation, refasciculation, and altered fasciculation. Neuron 13:1055-1069PubMedCrossRefGoogle Scholar
  11. 11.
    Rechsteiner M, Rogers SW (1996) PEST sequences and regulation by proteolysis. Trends Biochem Sci 21:267-271PubMedGoogle Scholar
  12. 12.
    Reyes AA, Schulte SV, Small S et al (1993) Distinct NCAM splicing events are differentially regulated during rat brain development. Brain Res Mol Brain Res 17:201-211PubMedCrossRefGoogle Scholar
  13. 13.
    Rutishauser U, Landmesser L (1996) Polysialic acid in the vertebrate nervous system: a promoter of plasticity in cell-cell interactions. Trends Neurosci 19:422-427PubMedGoogle Scholar
  14. 14.
    Roth J, Kempf A, Reuter G et al (1992) Occurrence of sialic acids in Drosophila melanogaster. Science 256:673-675PubMedCrossRefGoogle Scholar
  15. 15.
    Katz F, Moats W, Jan YN (1988) A carbohydrate epitope expressed uniquely on the cell surface of Drosophila neurons is altered in the mutant nac (neurally altered carbohydrate). Embo J 7:3471-3477PubMedGoogle Scholar
  16. 16.
    Snow PM, Patel NH, Harrelson AL et al (1987) Neural-specific carbohydrate moiety shared by many surface glycoproteins in Drosophila and grasshopper embryos. J Neurosci 7:4137-4144PubMedGoogle Scholar
  17. 17.
    Jan LY, Jan YN (1982) Antibodies to horseradish peroxidase as specific neuronal markers in Drosophila and in grasshopper embryos. Proc Natl Acad Sci USA 79:2700-2704PubMedCrossRefGoogle Scholar
  18. 18.
    Bastiani MJ, Harrelson AL, Snow PM et al (1987) Expression of fasciclin I and II glycoproteins on subsets of axon pathways during neuronal development in the grasshopper. Cell 48:745-755PubMedCrossRefGoogle Scholar
  19. 19.
    Brackenbury R (1988) Expression of neural cell adhesion molecules in normal and pathologic tissues. Ann NY Acad Sci 540:39-46PubMedCrossRefGoogle Scholar
  20. 20.
    Walsh FS, Doherty P (1997) Neural cell adhesion molecules of the immunoglobulin superfamily: role in axon growth and guidance. Annu Rev Cell Dev Biol 13:425-456PubMedCrossRefGoogle Scholar
  21. 21.
    Fidzianska A, Kaminska A (1995) Neural cell adhesion molecule (N-CAM) as a marker of muscle tissue alternations. Review of the literature and own observations. Folia Neuropathol 33:125-128PubMedGoogle Scholar
  22. 22.
    Lackie PM, Zuber C, Roth J (1990) Polysialic acid and N-CAM localisation in embryonic rat kidney: mesenchymal and epithelial elements show different patterns of expression. Development 110:933-947PubMedGoogle Scholar
  23. 23.
    Takeda Y, Murakami Y, Asou H et al (2001) The roles of cell adhesion molecules on the formation of peripheral myelin. Keio J Med 50:240-248PubMedCrossRefGoogle Scholar
  24. 24.
    Bonfanti L (2006) PSA-NCAM in mammalian structural plasticity and neurogenesis. Prog Neurobiol 80:129-164PubMedCrossRefGoogle Scholar
  25. 25.
    Bruses JL, Rutishauser U (2001) Roles, regulation, and mechanism of polysialic acid function during neural development. Biochimie 83:635-643PubMedCrossRefGoogle Scholar
  26. 26.
    Seki T, Arai Y (1993) Distribution and possible roles of the highly polysialylated neural cell adhesion molecule (NCAM-H) in the developing and adult central nervous system. Neurosci Res 17:265-290PubMedCrossRefGoogle Scholar
  27. 27.
    Szafranski P, Goode S (2004) A Fasciclin 2 morphogenetic switch organizes epithelial cell cluster polarity and motility. Development 131:2023-2036PubMedCrossRefGoogle Scholar
  28. 28.
    Szafranski P, Goode S (2007) Basolateral junctions are sufficient to suppress epithelial invasion during Drosophila oogenesis. Dev Dyn 236:364-373PubMedCrossRefGoogle Scholar
  29. 29.
    Harrelson AL, Goodman CS (1988) Growth cone guidance in insects: fasciclin II is a member of the immunoglobulin superfamily. Science 242:700-708PubMedCrossRefGoogle Scholar
  30. 30.
    Nassif C, Noveen A, Hartenstein V (2003) Early development of the Drosophila brain: III. The pattern of neuropile founder tracts during the larval period. J Comp Neurol 455:417-434PubMedCrossRefGoogle Scholar
  31. 31.
    Nassif C, Noveen A, Hartenstein V (1998) Embryonic development of the Drosophila brain I. Pattern of pioneer tracts. J Comp Neurol 402:10-31PubMedCrossRefGoogle Scholar
  32. 32.
    Wright JW, Copenhaver PF (2000) Different isoforms of fasciclin II play distinct roles in the guidance of neuronal migration during insect embryogenesis. Dev Biol 225:59-78PubMedCrossRefGoogle Scholar
  33. 33.
    Higgins MR, Gibson NJ, Eckholdt PA et al (2002) Different isoforms of fasciclin II are expressed by a subset of developing olfactory receptor neurons and by olfactory-nerve glial cells during formation of glomeruli in the moth Manduca sexta. Dev Biol 244:134-154PubMedCrossRefGoogle Scholar
  34. 34.
    Wright JW, Snyder MA, Schwinof KM et al (1999) A role for fasciclin II in the guidance of neuronal migration. Development 126:3217-3228PubMedGoogle Scholar
  35. 35.
    Kiselyov VV, Soroka V, Berezin V et al (2005) Structural biology of NCAM homophilic binding and activation of FGFR. J Neurochem 94:1169-1179PubMedCrossRefGoogle Scholar
  36. 36.
    Hortsch M, O’Shea KS, Zhao G et al (1998) A conserved role for L1 as a transmembrane link between neuronal adhesion and membrane cytoskeleton assembly. Cell Adhes Commun 5:61-73PubMedCrossRefGoogle Scholar
  37. 37.
    Urbach R, Technau GM (2003) Molecular markers for identified neuroblasts in the developing brain of Drosophila. Development 130:3621-3637PubMedCrossRefGoogle Scholar
  38. 38.
    Schmucker D, Jackle H, Gaul U (1997) Genetic analysis of the larval optic nerve projection in Drosophila. Development 124:937-948PubMedGoogle Scholar
  39. 39.
    Garcia-Alonso L, VanBerkum MF, Grenningloh G et al (1995) Fasciclin II controls proneural gene expression in Drosophila. Proc Natl Acad Sci USA 92:10501-10505PubMedCrossRefGoogle Scholar
  40. 40.
    Modolell J, Campuzano S (1998) The achaete-scute complex as an integrating device. Int J Dev Biol 42:275-282PubMedGoogle Scholar
  41. 41.
    Whitlock KE (1993) Development of Drosophila wing sensory neurons in mutants with missing or modified cell surface molecules. Development 117:1251-1260PubMedGoogle Scholar
  42. 42.
    Forsthoefel DJ, Liebl EC, Kolodziej PA et al (2005) The Abelson tyrosine kinase, the Trio GEF and Enabled interact with the Netrin receptor frazzled in Drosophila. Development 132:1983-1994PubMedCrossRefGoogle Scholar
  43. 43.
    Liebl EC, Forsthoefel DJ, Franco LS et al (2000) Dosage-sensitive, reciprocal genetic interactions between the Abl tyrosine kinase and the putative GEF trio reveal trio’s role in axon pathfinding. Neuron 26:107-118PubMedCrossRefGoogle Scholar
  44. 44.
    Gertler FB, Bennett RL, Clark MJ et al (1989) Drosophila abl tyrosine kinase in embryonic CNS axons: a role in axonogenesis is revealed through dosage-sensitive interactions with disabled. Cell 58:103-113PubMedCrossRefGoogle Scholar
  45. 45.
    Kurusu M, Awasaki T, Masuda-Nakagawa LM et al (2002) Embryonic and larval development of the Drosophila mushroom bodies: concentric layer subdivisions and the role of fasciclin II. Development 129:409-419PubMedGoogle Scholar
  46. 46.
    Wright JW, Copenhaver PF (2001) Cell type-specific expression of fasciclin II isoforms reveals neuronal-glial interactions during peripheral nerve growth. Dev Biol 234:24-41PubMedCrossRefGoogle Scholar
  47. 47.
    Doherty P, Williams G, Williams EJ (2000) CAMs and axonal growth: a critical evaluation of the role of calcium and the MAPK cascade. Mol Cell Neurosci 16:283-295PubMedCrossRefGoogle Scholar
  48. 48.
    Ming GL, Wong ST, Henley J et al (2002) Adaptation in the chemotactic guidance of nerve growth cones. Nature 417:411-418PubMedCrossRefGoogle Scholar
  49. 49.
    Hoeffer CA, Sanyal S, Ramaswami M (2003) Acute induction of conserved synaptic signaling pathways in Drosophila melanogaster. J Neurosci 23:6362-6372PubMedGoogle Scholar
  50. 50.
    Yu HH, Huang AS, Kolodkin AL (2000) Semaphorin-1a acts in concert with the cell adhesion molecules fasciclin II and connectin to regulate axon fasciculation in Drosophila. Genetics 156:723-731PubMedGoogle Scholar
  51. 51.
    Kiryushko D, Berezin V, Bock E (2004) Regulators of neurite outgrowth: role of cell adhesion molecules. Ann N Y Acad Sci 1014:140-154PubMedCrossRefGoogle Scholar
  52. 52.
    Brittis PA, Lemmon V, Rutishauser U et al (1995) Unique changes of ganglion cell growth cone behavior following cell adhesion molecule perturbations: a time-lapse study of the living retina. Mol Cell Neurosci 6:433-449PubMedCrossRefGoogle Scholar
  53. 53.
    Rutishauser U (1985) Influences of the neural cell adhesion molecule on axon growth and guidance. J Neurosci Res 13:123-131PubMedCrossRefGoogle Scholar
  54. 54.
    Cremer H, Chazal G, Goridis C et al (1997) NCAM is essential for axonal growth and fasciculation in the hippocampus. Mol Cell Neurosci 8:323-335PubMedCrossRefGoogle Scholar
  55. 55.
    Cremer H, Chazal G, Lledo PM et al (2000) PSA-NCAM: an important regulator of hippocampal plasticity. Int J Dev Neurosci 18:213-220PubMedCrossRefGoogle Scholar
  56. 56.
    Cremer H, Chazal G, Carleton A et al (1998) Long-term but not short-term plasticity at mossy fiber synapses is impaired in neural cell adhesion molecule-deficient mice. Proc Natl Acad Sci USA 95:13242-13247PubMedCrossRefGoogle Scholar
  57. 57.
    Panicker AK, Buhusi M, Thelen K et al (2003) Cellular signalling mechanisms of neural cell adhesion molecules. Front Biosci 8:d900-d911PubMedCrossRefGoogle Scholar
  58. 58.
    Brittis PA, Silver J, Walsh FS et al (1996) Fibroblast growth factor receptor function is required for the orderly projection of ganglion cell axons in the developing mammalian retina. Mol Cell Neurosci 8:120-128CrossRefGoogle Scholar
  59. 59.
    Speicher S, Garcia-Alonso L, Carmena A et al (1998) Neurotactin functions in concert with other identified CAMs in growth cone guidance in Drosophila. Neuron 20:221-233PubMedCrossRefGoogle Scholar
  60. 60.
    Garcia-Alonso L, Fetter RD, Goodman CS (1996) Genetic analysis of Laminin A in Drosophila: extracellular matrix containing laminin A is required for ocellar axon pathfinding. Development 122:2611-2621PubMedGoogle Scholar
  61. 61.
    Kristiansen LV, Velasquez E, Romani S et al (2005) Genetic analysis of an overlapping functional requirement for L1- and NCAM-type proteins during sensory axon guidance in Drosophila. Mol Cell Neurosci 28:141-152PubMedCrossRefGoogle Scholar
  62. 62.
    Hortsch M, Bieber AJ, Patel NH et al (1990) Differential splicing generates a nervous system-specific form of Drosophila neuroglian. Neuron 4:697-709PubMedCrossRefGoogle Scholar
  63. 63.
    Hall SG, Bieber AJ (1997) Mutations in the Drosophila neuroglian cell adhesion molecule affect motor neuron pathfinding and peripheral nervous system patterning. J Neurobiol 32:325-340PubMedCrossRefGoogle Scholar
  64. 64.
    Garcia-Alonso L, Romani S, Jimenez F (2000) The EGF and FGF receptors mediate neuroglian function to control growth cone decisions during sensory axon guidance in Drosophila. Neuron 28:741-752PubMedCrossRefGoogle Scholar
  65. 65.
    Forni JJ, Romani S, Doherty P et al (2004) Neuroglian and FasciclinII can promote neurite outgrowth via the FGF receptor Heartless. Mol Cell Neurosci 26:282-291PubMedCrossRefGoogle Scholar
  66. 66.
    Hinsby AM, Berezin V, Bock E (2004) Molecular mechanisms of NCAM function. Front Biosci 9:2227-2244PubMedCrossRefGoogle Scholar
  67. 67.
    Brittis PA, Silver J, Walsh FS et al (1996) Fibroblast growth factor receptor function is required for the orderly projection of ganglion cell axons in the developing mammalian retina. Mol Cell Neurosci 8:120-128CrossRefGoogle Scholar
  68. 68.
    Phelps CB, Brand AH (1998) Ectopic gene expression in Drosophila using GAL4 system. Methods 14:367-379PubMedCrossRefGoogle Scholar
  69. 69.
    Gascon E, Vutskits L, Kiss JZ (2007) Polysialic acid-neural cell adhesion molecule in brain plasticity: from synapses to integration of new neurons. Brain Res Rev 56(1):101-118PubMedCrossRefGoogle Scholar
  70. 70.
    Rønn LC, Berezin V, Bock E (2000) The neural cell adhesion molecule in synaptic plasticity and ageing. Int J Dev Neurosci 18:193-199PubMedCrossRefGoogle Scholar
  71. 71.
    Welzl H, Stork O (2003) Cell adhesion molecules: key players in memory consolidation? News Physiol Sci 18:147-150PubMedGoogle Scholar
  72. 72.
    Mathew D, Popescu A, Budnik V (2003) Drosophila amphiphysin functions during synaptic Fasciclin II membrane cycling. J Neurosci 23:10710-10716PubMedGoogle Scholar
  73. 73.
    Davis GW, Schuster CM, Goodman CS (1996) Genetic dissection of structural and functional components of synaptic plasticity III. CREB is necessary for presynaptic functional plasticity. Neuron 17:669-679PubMedCrossRefGoogle Scholar
  74. 74.
    Gerrow K, El-Husseini A (2006) Cell adhesion molecules at the synapse. Front Biosci 11:2400-2419PubMedCrossRefGoogle Scholar
  75. 75.
    Waites CL, Craig AM, Garner CC (2005) Mechanisms of vertebrate synaptogenesis. Annu Rev Neurosci 28:251-274PubMedCrossRefGoogle Scholar
  76. 76.
    Brunner A, O’Kane CJ (1997) The fascination of the Drosophila NMJ. Trends Genet 13:85-87PubMedCrossRefGoogle Scholar
  77. 77.
    Zito K, Parnas D, Fetter RD et al (1999) Watching a synapse grow: noninvasive confocal imaging of synaptic growth in Drosophila. Neuron 22:719-729PubMedCrossRefGoogle Scholar
  78. 78.
    Rivlin PK, St Clair RM, Vilinsky I et al (2004) Morphology and molecular organization of the adult neuromuscular junction of Drosophila. J Comp Neurol 468:596-613PubMedCrossRefGoogle Scholar
  79. 79.
    Ritzenthaler S, Chiba A (2003) Myopodia (postsynaptic filopodia) participate in synaptic target recognition. J Neurobiol 55:31-40PubMedCrossRefGoogle Scholar
  80. 80.
    Collins CA, DiAntonio A (2007) Synaptic development: insights from Drosophila. Curr Opin Neurobiol 17:35-42PubMedCrossRefGoogle Scholar
  81. 81.
    Zito K, Fetter RD, Goodman CS et al (1997) Synaptic clustering of Fascilin II and Shaker: essential targeting sequences and role of Dlg. Neuron 19:1007-1016PubMedCrossRefGoogle Scholar
  82. 82.
    Schuster CM, Davis GW, Fetter RD et al (1996) Genetic dissection of structural and functional components of synaptic plasticity. I. Fasciclin II controls synaptic stabilization and growth. Neuron 17:641-654PubMedCrossRefGoogle Scholar
  83. 83.
    Hebbar S, Fernandes JJ (2005) A role for Fas II in the stabilization of motor neuron branches during pruning in Drosophila. Dev Biol 285:185-199PubMedCrossRefGoogle Scholar
  84. 84.
    Schuster CM, Davis GW, Fetter RD et al (1996) Genetic dissection of structural and functional components of synaptic plasticity. II. Fasciclin II controls presynaptic structural plasticity. Neuron 17:655-667PubMedCrossRefGoogle Scholar
  85. 85.
    Sigrist SJ, Reiff DF, Thiel PR et al (2003) Experience-dependent strengthening of Drosophila neuromuscular junctions. J Neurosci 23:6546-6556PubMedGoogle Scholar
  86. 86.
    Davis GW, Schuster CM, Goodman CS (1997) Genetic analysis of the mechanisms controlling target selection: target-derived Fasciclin II regulates the pattern of synapse formation. Neuron 19:561-573PubMedCrossRefGoogle Scholar
  87. 87.
    Stewart BA, McLean JR (2004) Population density regulates Drosophila synaptic morphology in a Fasciclin-II-dependent manner. J Neurobiol 61:392-399PubMedCrossRefGoogle Scholar
  88. 88.
    Winberg ML, Mitchell KJ, Goodman CS (1998) Genetic analysis of the mechanisms controlling target selection: complementary and combinatorial functions of netrins, semaphorins, and IgCAMs. Cell 93:581-591PubMedCrossRefGoogle Scholar
  89. 89.
    Rose D, Chiba A (1999) A single growth cone is capable of integrating simultaneously presented and functionally distinct molecular cues during target recognition. J Neurosci 19:4899-4906PubMedGoogle Scholar
  90. 90.
    de Jong S, Cavallo JA, Rios CD et al (2005) Target recognition and synaptogenesis by motor axons: responses to the sidestep protein. Int J Dev Neurosci 23:397-410PubMedCrossRefGoogle Scholar
  91. 91.
    Wan HI, DiAntonio A, Fetter RD et al (2000) Highwire regulates synaptic growth in Drosophila. Neuron 26:313-329PubMedCrossRefGoogle Scholar
  92. 92.
    Aberle H, Haghighi AP, Fetter RD et al (2002) Wishful thinking encodes a BMP type II receptor that regulates synaptic growth in Drosophila. Neuron 33:545-558PubMedCrossRefGoogle Scholar
  93. 93.
    Baines RA, Seugnet L, Thompson A et al (2002) Regulation of synaptic connectivity: levels of Fasciclin II influence synaptic growth in the Drosophila CNS. J Neurosci 22:6587-6595PubMedGoogle Scholar
  94. 94.
    Hebbar S, Hall RE, Demski SA et al (2006) The adult abdominal neuromuscular junction of Drosophila: a model for synaptic plasticity. J Neurobiol 66:1140-1155PubMedCrossRefGoogle Scholar
  95. 95.
    Koh YH, Ruiz-Canada C, Gorczyca M et al (2002) The Ras1-mitogen-activated protein kinase signal transduction pathway regulates synaptic plasticity through fasciclin II-mediated cell adhesion. J Neurosci 22:2496-2504PubMedGoogle Scholar
  96. 96.
    Thomas U, Kim E, Kuhlendahl S et al (1997) Synaptic clustering of the cell adhesion molecule fasciclin II by discs-large and its role in the regulation of presynaptic structure. Neuron 19:787-799PubMedCrossRefGoogle Scholar
  97. 97.
    Beumer K, Matthies HJ, Bradshaw A et al (2002) Integrins regulate DLG/FAS2 via a CaM kinase II-dependent pathway to mediate synapse elaboration and stabilization during postembryonic development. Development 129:3381-3391PubMedGoogle Scholar
  98. 98.
    Ashley J, Packard M, Ataman B et al (2005) Fasciclin II signals new synapse formation through amyloid precursor protein and the scaffolding protein dX11/Mint. J Neurosci 25:5943-5955PubMedCrossRefGoogle Scholar
  99. 99.
    Koh YH, Popova E, Thomas U et al (1999) Regulation of DLG localization at synapses by CaMKII-dependent phosphorylation. Cell 98:353-363PubMedCrossRefGoogle Scholar
  100. 100.
    Packard M, Mathew D, Budnik V (2003) FASt remodeling of synapses in Drosophila. Curr Opin Neurobiol 13:527-534PubMedCrossRefGoogle Scholar
  101. 101.
    Kazama H, Nose A, Morimoto-Tanifuji T (2007) Synaptic components necessary for retrograde signaling triggered by calcium/calmodulin-dependent protein kinase II during synaptogenesis. Neuroscience 145:1007-1015PubMedCrossRefGoogle Scholar
  102. 102.
    Waltereit R, Weller M (2003) Signaling from cAMP/PKA to MAPK and synaptic plasticity. Mol Neurobiol 27:99-106PubMedCrossRefGoogle Scholar
  103. 103.
    Atkins CM, Selcher JC, Petraitis JJ et al (1998) The MAPK cascade is required for mammalian associative learning. Nat Neurosci 1:602-609PubMedCrossRefGoogle Scholar
  104. 104.
    Selcher JC, Weeber EJ, Christian J et al (2003) A role for ERK MAP kinase in physiologic temporal integration in hippocampal area CA1. Learn Mem 10:26-39PubMedCrossRefGoogle Scholar
  105. 105.
    Sweatt JD (2004) Mitogen-activated protein kinases in synaptic plasticity and memory. Curr Opin Neurobiol 14:311-317PubMedCrossRefGoogle Scholar
  106. 106.
    Adams JP, Sweatt JD (2002) Molecular psychology: roles for the ERK MAP kinase cascade in memory. Annu Rev Pharmacol Toxicol 42:135-163PubMedCrossRefGoogle Scholar
  107. 107.
    Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368-376PubMedCrossRefGoogle Scholar
  108. 108.
    Hummel T, Krukkert K, Roos J et al (2000) Drosophila Futsch/22C10 is a MAP1B-like protein required for dendritic and axonal development. Neuron 26:357-370PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  1. 1.Department of Cell and Developmental BiologyUniversity of MichiganAnn ArborUSA
  2. 2.European Science FoundationStrasbourg CedexFrance

Personalised recommendations