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Development of the Cholinergic Synapse: Role of Trophic Factors

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Book cover The Cholinergic Synapse

Part of the book series: Handbook of Experimental Pharmacology ((HEP,volume 86))

Abstract

Considerable advances have been made in the last decade in the search for the trophic factors that might be operational during the development of cholinergic systems. The search has been inspired by the discovery of nerve growth factor (NGF), a protein essential for the development and maintenance of both sympathetic and sensory neurons, and various lines of experimental evidence suggesting the necessity of trophic factors for cholinergic neuron development. The use of tissue culture models has provided the technical means of approaching the problem and has now led to the purification of several factors that are putatively involved in various aspects of the development of cholinergic neurons in vivo. This chapter will focus on the work that has been directed to purifying the factors required for the survival and development of the cholinergic motor neurons of the parasympathetic nervous system and the spinal cord in vitro and, in view of its potential role in the expression of the cholinergic phenotype, on the factor purified from heart-cell conditioned medium that induces cholinergic characteristics in sympathetic neurons.

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References

  • Adler R, Varon S (1980) Cholinergic neuronotrophic factors: V. Segregation of survival- and neurite-promoting activities in heart-conditioned media. Brain Res 188:437–448

    Article  PubMed  CAS  Google Scholar 

  • Adler R, Landa KB, Manthorpe M, Varon S (1979) Cholinergic neuronotrophic factors: intraocular distribution of trophic activity for ciliary neurones. Science 204:1434–1436

    Article  PubMed  CAS  Google Scholar 

  • Adler R, Manthorpe M, Skaper SD, Varon S (1981) Polyornithine-attached neurite-promoting factors (PNPFs): culture sources and responsive neurons. Brain Res 206:129–144

    Article  PubMed  CAS  Google Scholar 

  • Barbin G, Manthorpe M, Varon S (1984) Purification of the chick eye ciliary neuronotrophic factor. J Neurochem 43:1468–1478

    Article  PubMed  CAS  Google Scholar 

  • Barde Y-A, Edgar D, Thoenen H (1982) Purification of a new neuronotrophic factor from mammalian brain. EMBO J 1:548–549

    Google Scholar 

  • Bennett MR, White W (1979) The survival and development of cholinergic neurons in potassium-enriched media. Brain Res 173:549–553

    Article  PubMed  CAS  Google Scholar 

  • Bennett MR, Lai K, Nurcombe V (1980) Identification of embryonic motoneurons in vitro: their survival is dependent on skeletal muscle. Brain Res 190:537–542

    Article  PubMed  CAS  Google Scholar 

  • Berg D (1978) Acetylcholine synthesis by chick spinal cord neurons in dissociated cell culture. Dev Biol 66:500–512

    Article  PubMed  CAS  Google Scholar 

  • Bonyhady RE, Hendry IA, Hill CE, McLennan IS (1980) Characterization of a cardiac muscle factor required for the survival of cultured parasympathetic neurones. Neurosci Lett 18:197–201

    Article  PubMed  CAS  Google Scholar 

  • Bonyhady RE, Hendry IA, Hill CE (1982) Reversible dissociation of a bovine cardiac factor that supports survival of avian ciliary ganglionic neurones. J Neurosci Res 7:11–21

    Article  PubMed  CAS  Google Scholar 

  • Brenneman DE, Warren D (1983) Induction of cholinergic expression in developing spinal cord cultures. J Neurochem 41:1349–1356

    Article  PubMed  CAS  Google Scholar 

  • Brookes N, Burt DR, Goldberg AM, Bierkamper GG (1980) The influence of muscle-conditioned medium on cholinergic maturation in spinal cord cell cultures. Brain Res 186:474–479

    Article  PubMed  CAS  Google Scholar 

  • Calof AL, Reichardt LF (1984) Motoneurons purified by cell sorting respond to two distinct activities in myotube-conditioned medium. Dev Biol 106:194–201

    Article  PubMed  CAS  Google Scholar 

  • Chiappinelli V, Giacobini E, Pilar G, Uchimura H (1976) Induction of cholinergic enzymes in chick ciliary ganglion and iris muscle cells during synapse formation. J Physiol (Lond) 257:749–766

    CAS  Google Scholar 

  • Chun LLY, Patterson PH (1977) Role of nerve growth factor in the development of rat sympathetic neurons in vitro. III. Effect on acetycholine production. J Cell Biol 75:712–718

    Article  PubMed  CAS  Google Scholar 

  • Collins F (1978) Induction of neurite outgrowth by a conditioned-medium factor bound to the culture substratum. Proc Natl Acad Sci USA 75:5210–5213

    Article  PubMed  CAS  Google Scholar 

  • Collins F (1985) Electrophoretic similarity of the ciliary ganglion survival factors from different tissues and species. Dev Biol 109:255–258

    Article  PubMed  CAS  Google Scholar 

  • Collins F, Dawson A (1982) Conditioned medium increases the rate of neurite elongation: separation of this activity from the substratum-bound inducer of neurite outgrowth. J Neurosci 2:1005–1010

    PubMed  CAS  Google Scholar 

  • Collins F, Dawson A (1983) An effect of nerve growth factor on parasympathetic neurite outgrowth. Proc Natl Acad Sci USA 80:2091–2094

    Article  PubMed  CAS  Google Scholar 

  • Dohrmann U, Edgar D, Sendtner M, Thoenen H (1986) Muscle-derived factors that support survival and promote fiber outgrowth from embryonic chick spinal motor neurons in culture. Dev Biol 118:209–221

    Article  PubMed  CAS  Google Scholar 

  • Dribin LB (1982) On the species and substrate specificity of conditioned medium enhancement of neuritic outgrowth from spinal cord explants. Dev Brain Res 3:300–304

    Article  Google Scholar 

  • Dribin LB, Barrett JN (1980) Conditioned medium enhances neuritic outgrowth from rat spinal cord explants. Dev Biol 74:184–195

    Article  PubMed  CAS  Google Scholar 

  • Dribin LB, Barrett JN (1982a) Characterization of neuritic outgrowth-promoting activity of conditioned medium on spinal cord explants. Exp Brain Res 4:435–441

    Google Scholar 

  • Dribin LB, Barrett JN (1982b) Two components of conditioned medium increase neuritic outgrowth from rat spinal cord expiants. J Neurosci Res 8:271–280

    Article  PubMed  CAS  Google Scholar 

  • Ebendal T (1979) Stage dependent stimulation of neurite outgrowth exerted by nerve growth factor and chick heart in cultured embryonic ganglia. Dev Biol 72:276–290

    Article  PubMed  CAS  Google Scholar 

  • Ebendal T, Belew M, Jacobson CO, Porath J (1979) Neurite outgrowth elicited by embryonic chick heart: Partial purification of the active factor. Neurosci Lett 14:91–95

    Article  PubMed  CAS  Google Scholar 

  • Edgar D, Barde Y-A, Thoenen H (1981) Subpopulations of cultured chick neurones differ in their requirements for survival factors. Nature 289:294–295

    Article  PubMed  CAS  Google Scholar 

  • Fukada K (1980) Hormonal control of neurotransmitter choice in sympathetic neurone cultures. Nature 287:553–555

    Article  PubMed  CAS  Google Scholar 

  • Fukada K (1985) Purification and partial characterization of a cholinergic neuronal differentiation factor. Proc Natl Acad Sci USA 82:8795–8799

    Article  PubMed  CAS  Google Scholar 

  • Giess MC, Weber MJ (1984) Acetylcholine metabolism in rat spinal cord cultures: regulation by a factor involved in the determination of the neurotransmitter phenotype of sympathetic neurons. J Neurosci 4:1442–1452

    PubMed  CAS  Google Scholar 

  • Giller EL, Schrier BK, Shainberg A, Fisk HR, Nelson PG (1973) Choline acetyltransferase activity is increased in combined cultures of spinal cord and muscle cells from mice. Science 182:588–589

    Article  PubMed  CAS  Google Scholar 

  • Giller EL, Neale JH, Bullock PN, Schrier BK, Nelson PG (1977) Choline acetyltransferase activity of spinal cord cell cultures increased by co-culture with muscle and by muscle- conditioned medium. J Cell Biol 74:16–29

    Article  PubMed  CAS  Google Scholar 

  • Gnahn H, Hefti F, Heumann R, Schwab ME, Thoenen H (1983) NGF-mediated increase of choline acetyltransferase (ChAT) in the neonatal rat forebrain: Evidence for a physiological role of NGF in the brain? Dev Brain Res 9:45–52

    Article  CAS  Google Scholar 

  • Godfrey EW, Schrier BK, Nelson PG (1980) Source and target cell specificities of a conditioned medium factor that increases choline acetyltransferase activity in cultured spinal cord cells. Dev Biol 77:403–418

    Article  PubMed  CAS  Google Scholar 

  • Hamburger V (1934) The effects of limb bud extirpation on the development of the central nervous system in the chick spinal cord. J Exp Zool 68:449–494

    Article  Google Scholar 

  • Hamburger V (1975) Cell death in the development of the lateral motor column of the chick embryo. J Comp Neurol 160:535–546

    Article  PubMed  CAS  Google Scholar 

  • Helfand SL, Smith GA, Wessells NK (1976) Survival and development in culture of dissociated parasympathetic neurons from ciliary ganglia. Dev Biol 50:541–547

    Article  PubMed  CAS  Google Scholar 

  • Helfand SL, Riopelle RJ, Wessells NK (1978) Non-equivalence of conditioned medium and nerve growth factor for sympathetic, parasympathetic, and sensory neurons. Exp Cell Res 113:39–45

    Article  PubMed  CAS  Google Scholar 

  • Henderson CE, Huchet M, Changeux JP (1981) Neurite outgrowth from embryonic chicken spinal neurons is promoted by media conditioned by muscle cells. Proc Natl Acad Sci USA 78:2625–2629

    Article  PubMed  CAS  Google Scholar 

  • Henderson CE, Huchet M, Changeux JP (1983) Denervation increases a neurite-promoting activity in extracts of skeletal muscle. Nature 302:609–611

    Article  PubMed  CAS  Google Scholar 

  • Henderson CE, Huchet M, Changeux JP (1984) Neurite-promoting activities for embryonic spinal neurons and their developmental changes in the chick. Dev Biol 104:336–347

    Article  PubMed  CAS  Google Scholar 

  • Hill CE, Hendry IA, Bonyhady RE (1981) Avian parasympathetic neurotrophic factors: Age-related increases and lack of regional specificity. Dev Biol 85:258–261

    Article  PubMed  CAS  Google Scholar 

  • Hill MA, Bennett MR (1983) Cholinergic growth factor from skeletal muscle elevated following denervation. Neurosci Lett 35:31–35

    Article  PubMed  CAS  Google Scholar 

  • Hollyday M, Hamburger V (1976) Reduction of naturally occurring motorneuron loss by enlargement of the periphery. J Comp Neurol 170:311–320

    Article  PubMed  CAS  Google Scholar 

  • Ishida I, Deguchi T (1983 a) Regulation of acetyltransferase in primary cell cultures of spinal cord by neurotransmitter 1-Norepinephrine. Dev Brain Res 7:13–23

    Article  CAS  Google Scholar 

  • Ishida I, Deguchi T (1983 b) Effect of depolarising agents on choline acetyltransferase and acetylcholinesterase activities in primary cell cultures of spinal cord. J Neurosci 3:1818–1823

    PubMed  CAS  Google Scholar 

  • Johnson M, Ross D, Meyers M, Rees R, Bunge R, Vakshull E, Burton H (1976) Synaptic vesicle cytochemistry changes when cultured sympathetic neurones develop cholinergic interactions. Nature 262:308–310

    Article  PubMed  CAS  Google Scholar 

  • Johnson MI, Ross CD, Meyers M, Spitznagel EL, Bunge RP (1980) Morphological and biochemical studies on the development of cholinergic properties in cultured sympathetic neurons. I. Cholinergic properties. J Cell Biol 84:680–691

    Article  PubMed  CAS  Google Scholar 

  • Kato AC, Ray MJ (1982) Chick ciliary ganglion in dissociated cell culture. I. Cholinergic properties. Dev Biol 94:121–130

    Article  PubMed  CAS  Google Scholar 

  • Kaufman LM, Barrett JN (1983) Serum factor supporting long-term survival of rat central neurons in culture. Science 220:1394–1396

    Article  PubMed  CAS  Google Scholar 

  • Kaufman LM, Barry SR, Barrett JN (1985) Characterization of tissue-derived macromolecules affecting transmitter synthesis in rat spinal cord neurons. J Neurosci 5:160–166

    PubMed  CAS  Google Scholar 

  • Landa KB, Adler R, Manthorpe M, Varon S (1980) Cholinergic neuronotrophic factors. III. Developmental increase of trophic activity for chick embryo ciliary ganglion neurons in their intraocular target tissues. Dev Biol 74:401–408

    Article  PubMed  CAS  Google Scholar 

  • Lander AD, Fujii DK, Reichardt LF (1985) Laminin is associated with the ‘neurite outgrowth-promoting factors’ found in conditioned media. Proc Natl Acad Sci USA 82:2183–2187

    Article  PubMed  CAS  Google Scholar 

  • Landis SC (1976) Rat sympathetic neurons and cardiac myocytes developing in microcultures: correlation of the fine structure of endings with neurotransmitter function in single neurons. Proc Natl Acad Sci USA 73:4220–4224

    Article  PubMed  CAS  Google Scholar 

  • Landis SC, Fredieu JR, Yodlowski M (1985) Neonatal treatment with nerve growth factor antiserum eliminates cholinergic sympathetic innervation of rat sweat glands. Dev Biol 112:222–229

    Article  PubMed  CAS  Google Scholar 

  • Landmesser L, Pilar G (1974 a) Synaptic transmission and cell death during normal ganglion development. J Physiol (Lond) 241:737–749

    CAS  Google Scholar 

  • Landmesser L, Pilar G (1974 b) Synapse formation during embryogenesis on ganglion cells lacking a periphery. J Physiol (Lond) 241:715–736

    CAS  Google Scholar 

  • Lasher J, Zagon R (1972) The effect of potassium on neuronal differentiation in cultures of dissociated newborn rat cerebellum. Brain Res 41:482–488

    Article  PubMed  CAS  Google Scholar 

  • Longo FM, Manthorpe M, Varon S (1982) Spinal cord neuronotrophic factors (SCNTF’s): I. Bioassay of Schwannoma and other conditioned media. Dev Brain Res 3:277–294

    Article  Google Scholar 

  • Mains RE, Patterson PH (1973) Primary cultures of dissociated sympathetic neurons. I. Establishment of long-term growth in culture and studies of differentiated properties. J Cell Biol 59:329–345

    Article  PubMed  CAS  Google Scholar 

  • Manthorpe M, Varon S (1985) Regulation of neuronal survival and neuritic growth in the avian ciliary ganglion by trophic factors. In: Guroff G (ed) Growth and maturation factors, vol III. Wiley, New York, p 77

    Google Scholar 

  • Manthorpe M, Skaper S, Adler R, Landa K, Varon S (1980) Cholinergic neuronotrophic factors: fractionation properties of an extract from selected chick embryonic eye tissues. J Neurochem 24:69–75

    Article  Google Scholar 

  • Manthorpe M, Barbin G, Varon S (1982 a) Isoelectric focusing of the chick eye ciliary neuronotrophic factor. J Neurosci Res 8:233–239

    Article  PubMed  CAS  Google Scholar 

  • Manthorpe M, Longo FM, Varon S (1982 b) Comparative features of spinal neuronotrophic factors in fluids collected in vitro and in vivo. J Neurosci Res 8:241–250

    Article  PubMed  CAS  Google Scholar 

  • Manthorpe M, Engvall E, Ruoslahti E, Longo FM, Davis GE, Varon S (1983 a) Laminin promotes neuritic regeneration from cultured peripheral and central neurons. J Cell Biol 97:1882–1890

    Article  PubMed  CAS  Google Scholar 

  • Manthorpe M, Luyten W, Longo FM, Varon S (1983 b) Endogenous and exogenous factors support neuronal survival and choline acetyltransferase activity in embryonic spinal cord cultures. Brain Res 267:57–66

    Article  PubMed  CAS  Google Scholar 

  • Manthorpe M, Nieto-Sampedro M, Skaper SD, Barbin G, Longo FM, Varon S (1983 c) Neuronotrophic activity in brain wounds in the developing rat: correlation with implant survival in the wound cavity. Brain Res 267:47–56

    Article  PubMed  CAS  Google Scholar 

  • Martinez HJ, Dreyfus CF, Miller Jonakait G, Black IB (1985) Nerve growth factor promotes cholinergic development in brain striatal cultures. Proc Natl Acad Sci USA 82:7777–7781

    Article  PubMed  CAS  Google Scholar 

  • Max SR, Schwab M, Dumas M, Thoenen H (1978) Retrograde transport of nerve growth factor in the ciliary ganglion of the chick and rat. Brain Res 159:411–415

    Article  PubMed  CAS  Google Scholar 

  • McManaman JL, Smith RG, Appel SH (1985) Low-molecular-weight peptide stimulates cholinergic development in ventral spinal cord cultures. Dev Biol 112:248–252

    Article  PubMed  CAS  Google Scholar 

  • Meyer T, Burkart W, Jockusch H (1979) Choline acetyltransferase induction in cultured neurons: Dissociated spinal cord cells are dependent on muscle cells, organotypic expiants are not. Neurosci Lett 11:59–62

    Article  PubMed  CAS  Google Scholar 

  • Mobley WC, Rutkowski JL, Tennekoon GI, Buchanan K, Johnston MV (1985) Choline acetyltransferase activity in striatum of neonatal rats increased by nerve growth factor. Science 229:284–287

    Article  PubMed  CAS  Google Scholar 

  • Narayanan CH, Narayanan Y (1978) Neuronal adjustments in developing nuclear centers of the chick embryo following transplantation of an additional optic primordium. J Embryol Exp Morphol 44:53–70

    PubMed  CAS  Google Scholar 

  • Nieto-Sampedro M, Manthorpe M, Barbin G, Varon S, Cotman CW (1983) Injury-induced neuronotrophic activity in adult rat brain. Correlation with survival of delayed implants in wound cavity. J Neurosci 3:2219–2229

    PubMed  CAS  Google Scholar 

  • Nishi R, Berg DK (1977) Dissociated ciliary ganglion neurons in vitro: survival and synapse formation. Proc Natl Acad Sci USA 74:5171–5175

    Article  PubMed  CAS  Google Scholar 

  • Nishi R, Berg DK (1979) Survival and development of ciliary ganglion neurones grown alone in cell culture. Nature 277:232–234

    Article  PubMed  CAS  Google Scholar 

  • Nishi R, Berg DK (1981 a) Two components from the eye tissue that differentially stimulate the growth and development of ciliary ganglion neurons in cell culture. J Neurosci 1:505–512

    PubMed  CAS  Google Scholar 

  • Nishi R, Berg DK (1981 b) Effects of high K+ concentrations on the growth and development of ciliary ganglion in cell culture. Dev Biol 87:301–307

    Article  PubMed  CAS  Google Scholar 

  • Nurcombe V, Hill MA, Eagleson KL, Bennett MR (1984) Motor neuron survival and neuritic extension from spinal cord explants induced by factors released from denervated muscle. Brain Res 291:19–28

    Article  PubMed  CAS  Google Scholar 

  • Patterson PH, Chun LLY (1974) The influence of non-neuronal cells on catecholamine and acetylcholine synthesis and accumulation in cultures of dissociated sympathetic neurons. Proc Natl Acad Sci USA 71:3607–3610

    Article  PubMed  CAS  Google Scholar 

  • Patterson PH, Chun LLY (1977 a) The induction of acetylcholine synthesis in primary cultures of dissociated rat sympathetic neurons. I. Effects of conditioned medium. Dev Biol 56:263–280

    Article  PubMed  CAS  Google Scholar 

  • Patterson PH, Chun LLY (1977 b) The induction of acetylcholine synthesis in primary cultures of dissociated rat sympathetic neurons. II. Developmental aspects. Dev Biol 60:473–481

    Article  PubMed  CAS  Google Scholar 

  • Patterson PH, Reichardt LF, Chun LLY (1975) Biochemical studies on the development of primary sympathie neurons in culture. Cold Spring Harbor Symp Quant Biol 40:389–397

    Google Scholar 

  • Phillipson OT, Sandler M (1975) The influence of nerve growth factor, potassium depolarisation and dibutyryl (cyclic) adenosine 3´,5´-monophosphate on explant cultures of chick embryo sympathetic ganglia. Brain Res 90:273–281

    Article  PubMed  CAS  Google Scholar 

  • Reichardt LF, Patterson PH (1977) Neurotransmitter synthesis and uptake by isolated sympathetic neurones in microcultures. Nature 270:147–151

    Article  PubMed  CAS  Google Scholar 

  • Richardson GP, Rinschen B, Fox GQ (1985) Torpedo electromotor system development: developmentally regulated neurotrophic activities of electric organ tissue. J Comp Neurol 231:339–352

    Article  PubMed  CAS  Google Scholar 

  • Schmidt-Achert KM, Askanas V, Engel WK (1984) Thyrotropin-releasing hormone enhances choline acetyltransferase and creatine kinase in cultured spinal ventral horn neurons. J Neurochem 43:586–589

    Article  PubMed  CAS  Google Scholar 

  • Schnaar RL, Schaffner AE (1981) Separation of cell types from embryonic chicken and rat spinal cord: characterization of motoneuron-enriched fractions. J Neurosci 1:204–217

    PubMed  CAS  Google Scholar 

  • Scott BS (1977) The effect of elevated potassium on the time course of neuron survival in cultures of dissociated dorsal root ganglia. J Cell Physiol 91:305–316

    Article  PubMed  CAS  Google Scholar 

  • Selak I, Skaper SD, Varon S (1985) Pyruvate participation in the low molecular weight activity for central nervous system neurons in glia-conditioned media. J Neurosci 5:23–28

    PubMed  CAS  Google Scholar 

  • Slack JR, Pockett S (1982) Motor neurotrophic factor in denervated adult skeletal muscle. Brain Res 247:138–140

    Article  PubMed  CAS  Google Scholar 

  • Slack JR, Hopkins WG, Pockett S (1983) Evidence for a motor nerve growth factor. Muscle Nerve 6:243–252

    Article  PubMed  CAS  Google Scholar 

  • Smith RG, Appel SH (1983) Extracts of skeletal muscle increase neurite outgrowth and cholinergic activity of fetal rat spinal motor neurons. Science 291:1079–1081

    Article  Google Scholar 

  • Swerts JP, Thai A Le Van, Vigny A, Weber MJ (1983) Regulation of enzymes responsible for neurotransmitter synthesis and degradation in cultured rat sympathetic neurons. I. Effects of muscle-conditioned medium. Dev Biol 100:1–11

    Article  PubMed  CAS  Google Scholar 

  • Touzeau G, Kato AC (1983) Effects of myotrophic lateral sclerosis sera on cultured cholinergic neurones. Neurology 33:317–322

    PubMed  CAS  Google Scholar 

  • Tuttle JB, Suszkiw JB, Ard M (1980) Long-term survival and development of dissociated parasympathetic neurons in culture. Brain Res 183:161–180

    Article  PubMed  CAS  Google Scholar 

  • Varon S, Manthorpe M, Adler R (1979) Cholinergic neuronotrophic factors: I. Survival, neurite outgrowth and choline acetyltransferase activity in monolayer cultures from chick embryo ciliary ganglia. Brain Res 173:29–45

    Article  PubMed  CAS  Google Scholar 

  • Varon S, Manthorpe M, Selak I, Skaper SD (1983) Humoral agents modulating neuronal survival in vitro. In: Biggio G, Spanno PF, Toffano G, Gessa GL (eds) Symposia in neuroscience, 3rd Capo Boi conference on neuroscience, Sardinia, Italy. Pergamon, Oxford

    Google Scholar 

  • Varon S, Skaper SD, Barbin G, Selak I, Manthorpe M (1984) Low molecular weight agents support survival of cultured neurons from the central nervous system. J Neurosci 4:654–658

    PubMed  CAS  Google Scholar 

  • Wakshull E, Johnson MI, Burton H (1978) Persistance of an amine uptake system in cultured rat sympathetic neurons which use acetylcholine as their transmitter. J Cell Biol 79:121–131

    Article  PubMed  CAS  Google Scholar 

  • Weber M (1981) A diffusible factor responsible for the determination of cholinergic functions in cultured sympathetic neurons. J Biol Chem 256:3447–3453

    PubMed  CAS  Google Scholar 

  • Weber MJ, Raynaud B, Delteil C (1985) Molecular properties of a cholinergic differentiation factor from muscle-conditioned medium. J Neurochem 45:1541–1547

    Article  PubMed  CAS  Google Scholar 

  • Williams LR, Manthorpe M, Barbin G, Nieto-Sampedro M, Cotman CW, Varon S (1984) High ciliary neuronotrophic specific activity in rat peripheral nerve. Int J Dev Neurosci 2:177–180

    Article  Google Scholar 

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Richardson, G.P. (1988). Development of the Cholinergic Synapse: Role of Trophic Factors. In: Whittaker, V.P. (eds) The Cholinergic Synapse. Handbook of Experimental Pharmacology, vol 86. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-73220-1_5

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  • DOI: https://doi.org/10.1007/978-3-642-73220-1_5

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