A novel cysteine-rich neurotrophic factor in Aplysia facilitates growth, MAPK activation, and long-term synaptic facilitation

Learning and Memory

Volumn 21, Issue 4, 2014, Pages 215-222

  Pu, Lu ^a,b   Kopec, Ashley M ^a,b,c   Boyle, Heather D ^a,b   Carew, Thomas J ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CYSTEINE; CYSTEINE RICH NEUROTROPHIC FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; NEUROTROPHIC FACTOR; NEUROTROPHIN RECEPTOR P75; UNCLASSIFIED DRUG; CYSTEINE-RICH NEUROTROPHIC FACTOR, LYMNAEA STAGNALIS; NERVE GROWTH FACTOR; NERVE GROWTH FACTOR RECEPTOR; PROTEIN TYROSINE KINASE; TNFRSF16 PROTEIN, RAT;

ADULT; ANIMAL TISSUE; APLYSIA; ARTICLE; BRAIN NERVE CELL; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; ENZYME ACTIVATION; FACILITATION; LONG TERM FACILITATION; LONG TERM MEMORY; MEMORY; MOLECULAR CLONING; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; SEQUENCE ALIGNMENT; SYNAPTIC TRANSMISSION; AMINO ACID SEQUENCE; ANIMAL; CELL CULTURE; CELL ENLARGEMENT; GENETICS; LONG TERM POTENTIATION; LYMNAEA; METABOLISM; MOLECULAR GENETICS; MOTONEURON; NEURITE; PHYSIOLOGY; RAT; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; SYNAPSE;

AMINO ACID SEQUENCE; ANIMALS; APLYSIA; CELL ENLARGEMENT; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; CLONING, MOLECULAR; LONG-TERM POTENTIATION; LYMNAEA; MAP KINASE SIGNALING SYSTEM; MOLECULAR SEQUENCE DATA; MOTOR NEURONS; NERVE GROWTH FACTORS; NEURITES; PROTEIN-TYROSINE KINASES; RATS; RECEPTORS, NERVE GROWTH FACTOR; SENSORY RECEPTOR CELLS; SPECIES SPECIFICITY; SYNAPSES;

EID: 84898957838     PISSN: 10720502     EISSN: 15495485     Source Type: Journal    
DOI: 10.1101/lm.033662.113     Document Type: Article

References (42)

1. Atkins CM, Selcher JC, Petraitis JJ, Trzaskos JM, Sweatt JD. 1998. The MAPK cascade is required for mammalian associative learning. Nat Neurosci 1: 602-609.
2. Bailey CH, Kandel ER. 2008. Synaptic remodeling, synaptic growth and the storage of long-term memory in Aplysia. Prog Brain Res 169: 179-198. (Pubitemid 351451903)
3. Bailey CH, Bartsch D, Kandel ER. 1996. Toward a molecular definition of long-term memory storage. Proc Natl Acad Sci 93: 13445-13452. (Pubitemid 26424140)
4. Beck G, Munno DW, Levy Z, Dissel HM, Van-Minnen J, Syed NI, Fainzilber M. 2004. Neurotrophic activities of trk receptors conserved over 600 million years of evolution. J Neurobiol 60: 12-20. (Pubitemid 38765951)
5. Bibel M, Hoppe E, Barde YA. 1999. Biochemical and functional interactions between the neurotrophin receptors trk and p75NTR. EMBO J 18: 616-622. (Pubitemid 29057246)
6. Carew TJ, Menzel R, Shatz CJ. 1998. Points of contact between development and learning. In Mechanistic relationships between development and learning (ed. Carew TJ, Menzel R, Shatz CJ), pp. 1-14. John Wiley & Sons, Berlin.
7. Chao MV. 2003. Neurotrophins and their receptors: A convergence point for many signalling pathways. Nat Rev Neurosci 4: 299-309. (Pubitemid 37271375)
8. Chin J, Angers A, Cleary LJ, Eskin A, Byrne JH. 2002. Transforming growth factor b1 alters synapsin distribution and modulates synaptic depression in Aplysia. J Neurosci 22: RC220.
9. Cohen-Cory S, Kidane AH, Shirkey NJ, Marshak S. 2010. Brain-derived neurotrophic factor and the development of structural neuronal connectivity. Dev Neurobiol 70: 271-288.
10. Fainzilber M, Smit AB, Syed NI, Wildering WC, Hermann PM, van der Schors RC, Jimenez C, Li KW, van Minnen J, Bulloch AG, et al. 1996. CRNF, a molluscan neurotrophic factor that interacts with the p75 neurotrophin receptor. Science 274: 1540-1543. (Pubitemid 26403932)
11. Gensel JC, Schonberg DL, Alexander JK, McTigue DM, Popovich PG. 2010. Semi-automated Sholl analysis for quantifying changes in growth and differentiation of neurons and glia. J Neurosci Methods 190: 71-79.
12. Hu JY, Glickman L, Wu F, Schacher S. 2004. Serotonin regulates the secretion and autocrine action of a neuropeptide to activate MAPK required for long-term facilitation in Aplysia. Neuron 43: 373-385. (Pubitemid 39061129)
13. Huang EJ, Reichardt LF. 2003. Trk receptors: Roles in neuronal signal transduction. Annu Rev Biochem 72: 609-642. (Pubitemid 36930455)
14. Kassabov SR, Choi YB, Karl KA, Vishwasrao HD, Bailey CH, Kandel ER. 2013. A single aplysia neurotrophin mediates synaptic facilitation via differentially processed isoforms. Cell Rep 3: 1213-1227.
15. Kopec AM, Carew TJ. 2013. Growth factor signaling and memory formation: Temporal and spatial integration of a molecular network. Learn Mem 20: 531-539.
16. Levi-Montalcini R, Angeletti PU. 1968. Nerve growth factor. Physiol Rev 48: 534-569.
17. Lyles V, Zhao Y, Martin KC. 2006. Synapse formation and mRNA localization in cultured Aplysia neurons. Neuron 49: 349-356. (Pubitemid 43152237)
18. Marinesco S, Carew TJ. 2002. Serotonin release evoked by tail nerve stimulation in the CNS of Aplysia: Characterization and relationship to heterosynaptic plasticity. J Neurosci 22: 2299-2312. (Pubitemid 35386529)
19. McIlroy G, Foldi I, Aurikko J, Wentzell JS, Lim MA, Fenton JC, Gay NJ, Hidalgo A. 2013. Toll-6 and Toll-7 function as neurotrophin receptors in the Drosophila melanogaster CNS. Nat Neurosci 16: 1248-1256.
20. McKay SE, Purcell AL, Carew TJ. 1999. Regulation of synaptic function by neurotrophic factors in vertebrates and invertebrates: Implications for development and learning. Learn Mem 6: 193-215. (Pubitemid 29422824)
21. Ormond J, Hislop J, Zhao Y, Webb N, Vaillaincourt F, Dyer JR, Ferraro G, Barker P, Martin KC, Sossin WS. 2004. ApTrkl, a Trk-like receptor, mediates serotonin-dependent ERK activation and long-term facilitation in Aplysia sensory neurons. Neuron 44: 715-728. (Pubitemid 39531234)
22. Philips GT, Tzvetkova EI, Carew TJ. 2007. Transient mitogen-activated protein kinase activation is confined to a narrow temporal window required for the induction of two-trial long-term memory in Aplysia. J Neurosci 27: 13701-13705. (Pubitemid 350278244)
23. Philips GT, Ye X, Kopec AM, Carew TJ. 2013. MAPK establishes a molecular context that defines effective training patterns for long-term memory formation. J Neurosci 33: 7565-7573.
24. Poo MM. 2001. Neurotrophins as synaptic modulators. Nat Rev Neurosci 2: 24-32.
25. Purcell AL, Sharma SK, BagnallMW, Sutton MA, Carew TJ. 2003. Activation of a tyrosine kinase-MAPK cascade enhances the induction of long-term synaptic facilitation and long-term memory in Aplysia. Neuron 37: 473-484. (Pubitemid 36183368)
26. Reissner KJ, Shobe JL, Carew TJ. 2006. Molecular nodes in memory processing: Insights from Aplysia. Cell Mol Life Sci 63: 963-974. (Pubitemid 43800766)
27. Reissner KJ, Boyle HD, Ye X, Carew TJ. 2008. Aplysia synapse associated protein (APSAP): Identification, characterization, and selective interactions with Shaker-type potassium channels. J Neurochem 105: 1006-1018. (Pubitemid 351562738)
28. Reissner KJ, Pu L, Schaffhausen JH, Boyle HD, Smith IF, Parker I, Carew TJ. 2010. A novel postsynaptic mechanism for heterosynaptic sharing of short-term plasticity. J Neurosci 30: 8797-8806.
29. Sharma SK, Sherff CM, Shobe J, Bagnall MW, Sutton MA, Carew TJ. 2003. Differential role of mitogen-activated protein kinase in three distinct phases of memory for sensitization in Aplysia. J Neurosci 23: 3899-3907. (Pubitemid 36958495)
30. Sharma SK, Sherff CM, Stough S, Hsuan V, Carew TJ. 2006. A tropomyosin-related kinase B ligand is required for ERK activation, long-term synaptic facilitation, and long-term memory in Aplysia. Proc Natl Acad Sci 103: 14206-14210. (Pubitemid 44453004)
31. Sherff CM, Carew TJ. 2004. Parallel somatic and synaptic processing in the induction of intermediate-term and long-term synaptic facilitation in Aplysia. Proc Natl Acad Sci 101: 7463-7468. (Pubitemid 38638055)
32. Shi J, Blundell TL, Mizuguchi K. 2001. FUGUE: Sequence-structure homology recognition using environment-specific substitution tables and structure-dependent gap penalties. J Mol Biol 310: 243-257. (Pubitemid 32619966)
33. Shobe JL, Zhao Y, Stough S, Ye X, Hsuan V, Martin KC, Carew TJ. 2009. Temporal phases of activity-dependent plasticity and memory are mediated by compartmentalized routing of MAPK signaling in Aplysia sensory neurons. Neuron 61: 113-125.
34. Sholl DA. 1953. Dendritic organization in the neurons of the visual and motor cortices of the cat. J Anat 87: 387-406.
35. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Soding J, et al. 2011. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7: 539.
36. Sutton MA, Ide J, Masters SE, Carew TJ. 2002. Interaction between amount and pattern of training in the induction of intermediate- and long-term memory for sensitization in Aplysia. Learn Mem 9: 29-40. (Pubitemid 34273349)
37. Vicario-Abejon C, Owens D, McKay R, Segal M. 2002. Role of neurotrophins in central synapse formation and stabilization. Nat Rev Neurosci 3: 965-974. (Pubitemid 135715882)
38. Wiesmann C, de Vos AM. 2001. Nerve growth factor: Structure and function. Cell Mol Life Sci 58: 748-759. (Pubitemid 32553032)
39. Ye X, Shobe JL, Sharma SK, Marina A, Carew TJ. 2008. Small G proteins exhibit pattern sensitivity in MAPK activation during the induction of memory and synaptic facilitation in Aplysia. Proc Natl Acad Sci 105: 20511-20516.
40. Zhang F, Endo S, Cleary LJ, Eskin A, Byrne JH. 1997. Role of transforming growth factor-b in long-term synaptic facilitation in Aplysia. Science 275: 1318-1320. (Pubitemid 27114162)
41. Zhao Y, Wang DO, Martin KC. 2009. Preparation of Aplysia sensory-motor neuronal cell cultures. J Vis Exp 28: e1355.
42. Zhu B, Pennack JA, McQuilton P, Forero MG, Mizuguchi K, Sutcliffe B, Gu CJ, Fenton JC, Hidalgo A. 2008. Drosophila neurotrophins reveal a common mechanism for nervous system formation. PLoS Biol 6: e284.