Abstract
The formation of neuronal sprouts, either from synaptic terminals or nearby nodes of Ranvier, is a widely known form of plasticity of motoneurons. Sprouts form in response to several stimuli, but most notably in partially denervated or paralyzed muscle. In search of the cellular or molecular basis of this phenomenon, several largely parallel lines of investigation have been pursued. Strong evidence is presented that at least four cytokines or growth factors may be involved in motoneuron sprouting, each of which uses a distinctive signaling pathway. Three of the different proposed sprouting molecules: neuroleukin, insulin-like growth factor, and neural cell adhesion molecules can be viewed as muscle-derived retrograde signaling molecules of roughly equal potency to induce motoneurons to sprout. A fourth molecule, ciliary neurotrophic factor (CNTF) is likely to form an essential anterograde signal, from Schwann cells to muscle fibers, that ultimately produces sprouting. Other cytokines and growth factors such a neurotrophins or GDNF family members are discussed, but their role in motoneuron sprouting is less clear. These cytokines and growth factors could represent redundant mechanisms for self-repair of the neuromuscular junction or they could interact at different levels of their cellular pathways.
Similar content being viewed by others
References
ABE, K., NAMIKAWA, K., HONMA, M., IWATA, T., MATSUOKA, I., WATABE, K. & KIYAMA, H. (2001) Inhibition of Ras extracellular-signal-regulated kinase (ERK) mediated signaling promotes ciliary neurotrophic factor (CNTF) expression in Schwann cells. J. Neurochem. 77, 70–703.
AIGNER, L., ARBER, S., KAPFHAMMER, J. P., LAUX, T., SCHNEIDER, C., BOTTERI, F., BRENNER, H. R. & CARONI, P. (1995) Overexpression of the neural growth-associated protein GAP-43 induces nerve sprouting in the adult nervous system of transgenic mice. Cell 83, 26–278.
AIRAKSINEN, M. S. & SAARMA, M. (2002) The GDNF family: Signalling, biological functions and therapeutic value. Nature Rev. 3, 38–394.
ANGAUT-PETIT, D., MOLGO, J., COMELLA, J. X., FAILLE, L. & TABTI, N. (1990) Terminal sprouting in mouse neuromuscular junctions poisoned with botulinum type A toxin: Morphological and electrophysiological features. Neurosci. 37, 79–808.
BALICE-GORDON, R. J. & LICHTMAN, J. W. (1990) In vivo visualization of the growth of pre-and postsynaptic elements of neuromuscular junctions in the mouse. J. Neurosci. 10, 89–908.
BARBACID, M. (1995) Structural and functional properties of the TRK family of neurotrophin receptors. Ann. NY Acad. Sci. 766, 44–458.
BARDE, Y.-A., EDGAR, D. & THOENEN, H. (1982) Purification of a new neurotrophic factor from mammalian brain. EMBO J. 1, 54–553.
BATCHELOR, P. E., LIBERATORE, G. T., PORRITT, M. J., DONNAN, G. A. & HOWELLS, D. W. (2000) Inhibition of brain-derived neurotrophic factor and glial cell line-derived neurotrophic factor expression reduces dopaminergic sprouting in the injured striatum. Eur. J. Neurosci. 12, 346–3468.
BAXTER, G. T., RADEKE, M. J., KUO, R. C., MAKRIDES, V., HINKLE, B., HOANG, R., MEDINA-SELBY, A., COIT, D., VALENZUELA, P. & FEINSTEIN, S. C. (1997) Signal transduction mediated by the truncated trkB receptor isoforms, trkB.T1 and trkB.T2. J. Neurosci. 17, 268–2690.
BETZ, W. J., CALDWELL, J. H. & RIBCHESTER, R. R. (1980) Sprouting of active nerve terminals in partially inactive muscles of the rat. J. Physiol. (Lond.) 303, 28–297.
BONNEH-BARKAY, D., SHLISSEL, M., BERMAN, B., SHAOUL, E., ADMON, A., VLODAVSKY, I., CAREY, D. J., ASUNDI, V. K., REICH-SLOTKY, R. & RON, D. (1997) Identification of glypican as a dual modulator of the biological activity of fibroblast growth factors. J. Biol. Chem. 272, 1241–12421.
BOOTH, C. M., KEMPLAY, S. K. & BROWN, M. C. (1990) An antibody to neural cell adhesion molecule impairs motor nerve terminal sprouting in a mouse muscle locally paralysed with botulinum toxin. Neurosci. 35, 8– 91.
BOYD, J. G. & GORDON, T. (2002) A dose-dependent facilitation and inhibition of peripheral nerve regeneration by brain-derived neurotrophic factor. Eur. J. Neurosci. 15, 61–626.
BROWN, M. & IRONTON, R. (1977) Motor neurone sprouting induced by prolonged tetrodotoxin block of nerve action potentials. Nature 265, 45–461.
BROWN, M. C., GOODWIN, G. M. & IRONTON, R. (1977) Prevention of motor nerve sprouting in botulinum toxin poisoned mouse soleus muscles by direct stimulation of the muscle. J. Physiol. (Lond.) 267, 42P-43P.
BROWN, M. C., HOLLAND, R. E., HOPKINS, W. G. & KEYNES, R. J. (1980a) Anassessment of the spread of the signal for terminal sprouting within and between muscles. Brain Res. 210, 14–151.
BROWN, M. C., HOLLAND, R. L. & IRONTON, R. (1980b) Nodal and terminal sprouting frommotor nerves in fast and slow muscles of the mouse. J. Physiol. (Lond.) 306, 49–510.
BROWN, M. C. & IRONTON, R. (1978) Sprouting and regression of neuromuscular synapses in partially denervated mammalian muscles. J. Physiol. (Lond.) 278, 32–348.
CAMU, W. & HENDERSON, C. E. (1992) Purification of embryonic rat motoneurons by panning on a monoclonal antibody to the low-affinity NGF receptor J. Neurosci. Meth. 44, 5–70.
CARONI, P. & GRANDES, P. (1990) Nerve sprouting in innervated adult skeletal muscle induced by exposure to elevated levels of insulin-like growth factors. J. Cell Biol. 110, 130–1317.
CARONI, P., SCHNEIDER, C., KIEFER, M. C. & ZAPF, J. (1994) Role of muscle insulin-like growth factors in nerve sprouting: Suppression of terminal sprouting in paralyzed muscle by IGF-binding protein 4. J. Cell Biol. 125, 89–902.
CHAPUT, M., CLAES, V., PORTETELLE, D., CLUDTS, I., CRAVADOR, A., BURNY, A., GRAS, H. & TARTAR, A. (1988) The neurotrophic factor neuroleukin is 90% homologous with phosphohexose isomerase. Nature 332, 45–455.
CHUANG, T. Y., HUANG, M. C., CHEN, K. C., CHANG, Y. C., YEN, Y. S., LEE, L. S. & CHENG, H. (2002) Forelimb muscle activity following nerve graft repair of ventral roots in the rat cervical spinal cord. Life Sci. 71, 48–496.
CIFUENTES-DIAZ, C., VELASCO, E., MEUNIER, F. A., GOUDOU, D., BELKADI, L., FAILLE, L., MURAWSKY, M., ANGAUT-PETIT, D., MOLGO, J., SCHACHNER, M., SAGA, Y., AIZAWA, S. & RIEGER, F. (1998) The peripheral nerve and the neuromuscular junction are affected in the tenascin-C-deficient mouse. Cell Mol. Biol. 44, 35–379.
COVAULT, J. & SANES, J. R. (1985) Neural cell adhesion molecule (N-CAM) accumulates in denervated and paralyzed skeletal muscles. Proc. Natl. Acad. Sci. USA 82, 454–4548.
DAVIS, S., ALDRICH, T. H., VALENZUELA, D. M., WONG, V. V., FURTH, M. E., SQUINTO, S. P. & YANCOPOULOS, G. D. (1991) The receptor for ciliary neurotrophic factor. Science 253, 5–63.
DE PABLO, F., PEREZ-VILLAMIL, B., SERNA, J., GONZALEZ-GUERRERO, P. R., LOPEZCARRANZA, A., DE LA ROSA, E. J., ALEMANY, J. & CALDES, T. (1993) IGF-I and the IGF-I receptor in development of nonmammalian vertebrates. Mol. Reprod. Dev. 35, 42–432.
DE PAIVA, A., MEUNIER, F. A., MOLGO, J., AOKI, K. R. & DOLLY, J. O. (1999) Functional repair of motor endplates after botulinum neurotoxin A posioning: Biphasic switch of synaptic activity between nerve sprouts and their parent terminals. Proc. Natl. Acad. Sci. USA 96, 320–3205.
DIAZ, J. & PECOT-DECHAVASSINE, M. (1990) Nerve sprouting induced by a piece of peripheral nerve placed over a normally innervated frog muscle. J. Physiol. (Lond.) 421, 12–133.
DOHERTY, P., FRUNS, M., SEATON, P., DICKSON, G., BARTON, C. H., SEARS, T. A. & WALSH, F. S. (1990) A threshold effect of the major isoforms of NCAM on neurite outgrowth. Nature 343, 46–466.
DUCHEN, J. W. & STRICH, S. (1968) The effects of botulinum toxin on the pattern of innervation of skeletal muscle in the mouse. Quart. J. Exp. Physiol. 53, 8–89.
DUCHEN, L. W. (1970) Effects of botulinum toxin on the distribution of succinate dehydrogenase and phosphorylase in fast and slow skeletal muscles of the mouse. J. Neurol. Neurosurg. Psychiat. 33, 58–585.
DUCHEN, L. W. (1971) Changes in the electron microscopic structure of slow and fast skeletal muscle fibres of the mouse after the local injection of botulinum toxin. J. Neurol. Sci. 14, 6–74.
ENGLISH, A. W. & LETBETTER, W. D. (1982) Anatomy and innervation patterns of cat lateral gastrocnemius and plantaris muscles. Am. J. Anat. 164, 6–77.
ENGLISH, A. W. & SCHWARTZ, G. (1995) Both basic fibroblast growth factor and ciliary neurotrophic factor promote the retention of polyneuronal innervation of developing skeletal muscle fibers. Dev. Biol. 169, 5–64.
FAIK, P., WALKER, J. I., REDMILL, A. A. & MORGAN, M. J. (1988) Mouse glucose-6-phosphate isomerase and neuroleukin have identical 3? sequences. Nature 332, 45–457.
FLORKIEWICZ, R. Z., MAJACK, R. A., BUECHLER, R. D. & FLORKIEWICZ, E. (1995) Quantitative export of FGF-2 occurs through an alternative, energy-dependent, non-ER/Golgi pathway. J. Cell Physiol. 162, 38– 399.
FLORKIEWICZ, R. Z. & SOMMER, A. (1989) Human basic fibroblast growth factor gene encodes four polypeptides: Three initiate translation from non-AUG codons. Proc. Natl. Acad. Sci. USA 86, 397–3981.
FREY, D., SCHNEIDER, C., XU, L., BORG, J., SPOOREN, W. & CARONI, P. (2000) Early and selective loss of neuromuscular synapse subtypes with low sprouting competence in motoneuron diseases. J. Neurosci. 20, 253–2542.
FRIEDMAN, B., SCHERER, S. S., RUDGE, J. S., HELGREN, M., MORRISEY, D., MCCLAIN, J., WANG, D. Y., WIEGAND, S. J., FURTH, M. E., LINDSAY, R. M. & IP, N. Y. (1992) Regulation of ciliary neurotrophic factor expression in myelin related Schwann cells in vivo. Neuron 9, 29–305.
FRISEN, J., VERGE, V. M., FRIED, K., RISLING, M., PERSSON, H., TROTTER, J., HOKFLET, T. & LINDHOLM, D. (1993) Characterization of glial trkB receptors: Differential response to injury in the central and peripheral nervous systems. Proc. Natl. Acad. Sci. USA 90, 497–4975.
FUJIMOTO, I., BRUSES, J. L. & RUTISHAUSER, U. (2001) Regulation of cell adhesion by polysialic acid. Effects on cadherin, immunoglobulin cell adhesion molecule, and integrin function and independence from neural cell adhesion molecule binding or signaling activity. J. Biol. Chem. 276, 3174–31751.
FUNAKOSHI, H., BELLUARDO, N., ARENAS, E., YAMAMOTO, Y., CASABONA, A., PERSSON, H. & IBANEZ, C. F. (1995) Muscle-derived neurotrophin-4 as an activity-dependent trophic signal for adult motor neurons. Science 268, 149–1499.
FUNAKOSHI, H., FRISEN, J., BARBANY, G., TIMMUSK, T., ZACHRISSON, O., VERGE, V. M. & PERSSON, H. (1993) Differential expression of mRNAs for neurotrophins and their receptors after axotomy of the sciatic nerve. J. Cell Biol. 123, 45–465.
GATESY, S. M. & ENGLISH, A. W. (1993) Evidence for compartmental identity in the development of the rat lateral gastrocnemius muscle. Dev. Dyn. 196, 17–182.
GEARING, D. P. (1993) The leukemia inhibitory factor and its receptor Adv. Immunol. 53, 3–58.
GEARING, D. P., THUT, C. J., VANDEBOS, T., GIMPEL, S. D., DELANEY, P. B., KING, J., PRICE, V., COSMAN, D. & BECKMANN, M. P. (1991) Leukemia inhibitory factor receptor is structurally related to the IL-6 signal transducer, gp130. EMBO J. 10, 283–2848.
GLAZNER, G. W. & ISHII, D. N. (1995) Insulin like growth factor gene expression in rat muscle during reinnervation. Muscle Nerve. 18, 143–1442.
GONZALEZ, M., RUGGIERO, F. P., CHANG, Q., SHI, Y. J., RICH, M. M., KRANER, S. & BALICE-GORDON, R. J. (1999) Disruption of Trkb-mediated signaling induces disassembly of postsynaptic receptor clusters at neuromuscular junctions. Neuron 24, 56–583.
GRIESBECK, O., PARSADANIAN, A. S., SENDTNER, M. & THOENEN, H. (1995) Expression of neurotrophins in skeletal muscle: Quantitative comparison and significance for motoneuron survival and maintenance of function. J. Neurosci. Res. 42, 2–33.
GURNEY, M. E. (1984) Suppression of sprouting at the neuromuscular junction by immune sera. Nature 307, 54–548.
GURNEY, M. E. (1987) Neuroleukin: Basic biology and functional interaction with human immunodeficiency virus. Immunol. Rev. 100, 20–223.
GURNEY, M. E., APATOFF, B. R. & HEINRICH, S. P. (1986a) Suppression of terminal axonal sprouting at the neuromuscular junction by monoclonal antibodies against a muscle-derived antigen of 56,000 daltons. J. Cell Biol. 102, 226–2272.
GURNEY, M. E., APATOFF, B. R. & HEINRICH, S. P. (1987) Purification of a survival factor for spinal neurons from mouse salivary gland. Adv. Exp. Med. Biol. 209, 5–58.
GURNEY, M. E., APATOFF, B. R., SPEAR, G. T., BAUMEL, M. J., ANTEL, J. P., BANIA, M. B. & REDER, A. T. (1986b) Neuroleukin:Alymphokine product of lectin-stimulated T cells. Science 234, 57–581.
GURNEY, M. E., BELTON, A. C., CASHMAN, N. & ANTEL, J. P. (1984) Inhibition of terminal axonal sprouting by serumfrompatients with amyotrophic lateral sclerosis. N. Engl. J. Med. 311, 93–939.
GURNEY, M. E., HEINRICH, S. P., LEE, M. R. & YIN, H. S. (1986c) Molecular cloning and expression of neuroleukin, a neurotrophic factor for spinal and sensory neurons. Science 234, 56–574.
GURNEY, M. E., YAMAMOTO, H. & KWON, Y. (1992) Induction of motor neuron sprouting in vivo by ciliary neurotrophic factor and basic fibroblast growth factor. J. Neurosci. 12, 324–3247.
HAGA, A., NIINAKA, Y. & RAZ, A. (2000) Phosphohexose isomerase/autocrine motility factor/neuroleukin/ maturation factor is a multifunctional phosphoprotein. Biochim. Biophys. Acta. 1480, 23–244.
HALLAK, H., SEILER, A. E., GREEN, J. S., ROSS, B. N. & RUBIN, R. (2000) Association of heterotrimeric G(i) with the insulin-like growth factor-I receptor. Release of G (beta gamma) subunits upon receptor activation. J. Biol. Chem. 275, 225–2258.
HANSSON, H. A., DAHLIN, L. B., DANIELSEN, N., FRYKLUND, L., NACHEMSON, A. K., POLLERYD, P., ROZELL, B., SKOTTNER, A., STEMME, S. & LUNDBORG, G. (1986) Evidence indicating trophic importance of IGF-I in regenerating peripheral nerves. Acta Physiol. Scand. 126, 60–614.
HASSAN, S. M., JENNEKENS, F. G., VELDMAN, H. & OESTREICHER, B. A. (1994) GAP-43 and p75NGFR immunoreactivity in presynaptic cells following neuromuscular blockade by botulinum toxin in rat. J. Neurocytol. 23, 35–363.
HELLER, S., FINN, T. P., HUBER, J., NISHI, R., GEISSEN, M., PUSCHEL, A. W. & ROHRER, H. (1995) Analysis of function and expression of the chick GPA receptor (GPAR alpha) suggests multiple roles in neuronal development. Development 121, 268–2693.
HOFFMAN, H. (1950) Local reinnervation in partially denervated muscle: A histophysiological study. Aust. J. Exp. Biol. Med. Sci. 28, 38–397.
HOLLAND, R. & BROWN, M. (1980) Postsynaptic transmission block can cause terminal sprouting of a motor nerve. Science 207, 64–651.
HUBER, K., MEISINGER, C. & GROTHE, C. (1997) Expression of fibroblast growth factor-2 in hypoglossal motoneurons is stimulated by peripheral nerve injury. J. Comp. Neurol. 382, 18–198.
HUGHES, R. A., SENDTNER, M. & THOENEN, H. (1993) Members of several gene families influence survival of rat motoneurons in vitro and in vivo. J. Neurosci. Res. 36, 66–671.
IP, N. Y., MCCLAIN, J., BARREZUETA, N. X., ALDRICH, T. H., PAN, L., LI, Y., WIEGAND, S. J., FRIEDMAN, B., DAVIS, S. & YANCOPOULOS, G. D. (1993) The alpha component of the CNTF receptor is required for signaling and defines potential CNTF targets in the adult and during development. Neuron 10, 8–102.
IRONTON, R., BROWN, M. C. & HOLLAND, R. L. (1978) Stimuli to intramuscular nerve growth. Brain Res. 156, 35–354.
ISHII, D. N. (1989) Relationship of insulin-like growth factor II gene expression in muscle to synaptogenesis. Proc. Natl. Acad. Sci. USA 86, 289–2902.
ISHII, D. N., GLAZNER, G. W. & PU, S. F. (1994) Role of insulin-like growth factors in peripheral nerve regeneration. Pharmacol. Therapeut. 62, 12–144.
JOHNSON, H., HOKFELT, T. & ULFHAKE, B. (1996) Decreased expression of TrkB and TrkC mRNAs in spinal motoneurons of aged rats. Eur. J. Neurosci. 8, 49–499.
JUZANS, P., COMELLA, J. X., MOLGO, J., FAILLE, L. & ANGAUT-PETIT, D. (1996) Nerve terminal sprouting in botulinum type-A treated mouse levator auris longus muscle. Neuromus. Disord. 6, 17–185.
KELLER-PECK, C. R., FENG, G., SANES, J. R., YAN, Q., L ICHTMAN, J. W. & SNIDER, W. D. (2001) Glial cell line-derived neurotrophic factor administration in postnatal life results in motor unit enlargement and continuous synaptic remodeling at the neuromuscular junction. J. Neurosci. 21, 613–6146.
KEMPLAY, S. (1981) Terminal sprouting in the sternocostalis muscle of the rat. Effects of increasing extent of partial denervation. Cell Tiss. Res. 218, 42–425.
KIRSCH, M., SCHNEIDER, T., LEE, M. Y. & HOFMANN, H. D. (1998) Lesion-induced changes in the expression of ciliary neurotrophic factor and its receptor in rat optic nerve. Glia. 23, 23–248.
KLEIN, R., CONWAY, D., PARADA, L. F. & BARBACID, M. (1990) The trkB tyrosine protein kinase gene codes for a second neurogenic receptor that lacks the catalytic kinase domain. Cell 61, 64–656.
KOLIATSOS, V. E., CLATTERBUCK, R. E., WINSLOW, J. W., CAYOUETTE, M. H. & PRICE, D. L. (1993) Evidence that brain derived neurotrophic factor is a trophic factor for motoneurons in vivo. Neuron 10, 35–367.
KUST, B. M., COPRAY, J. C., BROUWER, N., TROOST, D. & BODDEKE, H. W. (2002) Elevated levels of neurotrophins inhumanbiceps brachii tissue of amyotrophic lateral sclerosis. Exp. Neurol. 177, 41–427.
LANGENFELD-OSTER, B., FAISSNER, A., IRINTCHEV, A. & WERNIG, A. (1994) Polyclonal antibodies against NCAM and tenascin delay endplate reinnervation. J. Neurocytol. 23, 59–604.
LECLERC, N., VALLEE, A. & NABI, I. R. (2000) Expression of the AMF/neuroleukin receptor in developing 958 ENGLISH and adult brain cerebellum. J. Neurosci. Res. 60, 60– 612.
LELIEVRE, E., PLUN-FAVREAU, H., CHEVALIER, S., FROGER, J., GUILLET, C., ELSON, G. C., GAUCHAT, J. F. & GASCAN, H. (2001) Signaling pathways recruited by the cardiotrophin-like cytokine/cytokine-like factor-1 composite cytokine: Specific requirement of the membrane-bound form of ciliary neurotrophic factor receptor alpha component. J. Biol. Chem. 276, 2247–22484.
LEWIS, M. E., NEFF, N. T., CONTRERAS, P. C., STONG, D. B., OPPENHEIM, R. W., GREBOW, P. E. & VAUGHT, J. L. (1993) Insulin-like growth factor-I: Potential for treatment of motor neuronal disorders. Exp. Neurol. 124, 7–88.
LICHTMAN, J. W., MAGRASSI, L. & PURVES, D. (1987) Visualization of neuromuscular junctions over periods of several months in living mice. J. Neurosci. 7, 121–1222.
LIEBROCK, J., LOTSPEICH, F., HOHN, A., HOFER, M., HENGERER, B., MASIAKOWSKI, P., THOENEN, H. & BARDE, Y.-A. (1989) Molecular cloning and expression of brain-derived neurotrophic factor. Nature 341, 14–152.
LIEM, R. S., BROUWER, N. & COPRAY, J. C. (2001) Ultrastructural localisation of intramuscular expression of BDNF mRNA by silver-gold intensified non-radioactive in situ hybridisation Histochem. Cell Biol. 116, 54–551.
LOMEN-HOERTH, C. & SHOOTER, E. M. (1995) Widespread neurotrophin receptor expression in the immune system and other nonneuronal rat tissues J. Neurochem. 64, 178–1789.
LOVE, F. M. & THOMPSON, W. J. (1999) Glial cells promote muscle reinnervation by responding to activity-dependent postsynaptic signals. J. Neurosci. 19, 1039–10396.
LUO, Y., LONG, J. M., LU, C., CHAN, S. L., SPANGLER, E. L., MASCARUCCI, P., RAZ, A., LONGO, D. L., MATTSON, M. P., INGRAM, D. K. & WENG, N. P. (2002) A link between maze learning and hippocampal expression of neuroleukin and its receptor, gp78. J. Neurochem. 80, 35–361.
LUTTRELL, L. M., VAN BIESEN, T., HAWES, B. E., KOCH, W. J., TOUHARA, K. & LEFKOWITZ, R. J. (1995) G beta gamma subunits mediate mitogenactivated protein kinase activation by the tyrosine kinase insulin-like growth factor 1 receptor. J. Biol. Chem. 270, 1649–16498.
MARCH, C. J., BOSLEY, B., LARSEN, A., CERRETTI, D. P., BRAEDT, G. & PRICE, V. (1985) Cloning, sequence and expression of two distinct human interleukin-1 complementary DNAs. Nature 315, 641.
MASON, I. J. (1994) Do adhesion molecules signal via FGF receptors? Current Biol. 4, 115–1161.
MIDDLEMAS, D. S., LINDBERG, R. A. & HUNTER, T. (1991) trkB, a neural receptor protein-tyrosine kinase: Evidence for a full-length and two truncated receptors. Mol. Cell. Biol. 11, 14–153.
MILLECAMPS, S., NICOLLE, D., CEBALLOS-PICOT, I., MALLET, J. & BARKATS, M. (2001) Synaptic sprouting increases the uptake capacities of motoneurons in amyotrophic lateral sclerosis mice. Proc. Natl. Acad. Sci. USA 98, 758–7587.
MIZRACHI, Y. (1989) Neurotrophic activity of monomeric glucophosphoisomerase was blocked by human immunodeficiency virus (HIV-1) and peptides from HIV-1 envelope glycoprotein. J. Neurosci. Res. 23, 21–224.
MOSCOSO, L. M., CREMER, H. & SANES, J. R. (1998) Organization and reorganization of neuromuscular junctions in mice lacking neural cell adhesion molecule, tenascin-C, or fibroblast growth factor-5. J. Neurosci. 18, 146–1477.
MURPHY, M., DUTTON, R., KOBLAR, S., CHEEMA, S. S. & BARTLETT, P. (1997) Cytokines which signal through the LIF receptor and their actions in the nervous system. Progr. Neurobiol. 52, 35–378.
NABI, I. R., WATANABE, H. & RAZ, A. (1992) Autocrine motility factor and its receptor: Role in cell locomotion and metastasis. Cancer Metast. Rev. 11, –20.
NEVE, R. L., COOPERSMITH, R., MCPHIE, D. L., SANTEUFEMIO, C., PRATT, K. G., MURPHY, C. J. & LYNN, S. D. (1998) The neuronal growth-associated protein GAP-43 interacts with rabaptin-5 and participates in endocytosis. J. Neurosci. 18, 775–7767.
NGUYEN, Q. T., PARSADANIAN, A. S., SNIDER, W. D. & LICHTMAN, J. W. (1998) Hyperinnervation of neuromuscular junctions caused by GDNF overexpression in muscle. Science 279, 172–1729.
NICOLA, N. A. & HILTON, D. J. (1996) Leukemia inhibitory factor and its receptor. In Growth Factors and Cytokines in Health and Disease (edited by LE ROITH, D. & BANDY, C.). Greenwich: JAI Press, Inc.
NIETHAMMER, P., DELLING, M., SYTNYK, V., DITYATEV, A., FUKAMI, K. & SCHACHNER, M. (2002) Cosignaling of NCAM via lipid rafts and the FGF receptor is required for neuritogenesis. J. Cell Biol. 157, 52–532.
ORNITZ, D. M. & ITOH, N. (2001) Fibroblast growth factors. Genome Biology. 2, 3005.
PESTRONK, A. & DRACHMAN, D. B. (1978) Motor nerve sprouting and acetylcholine receptors. Science 199, 122–1225.
PLUN-FAVREAU, H., ELSON, G., CHABBERT, M., FROGER, J., DELAPEYRIERE, O., LELIEVRE, E., GUILLET, C., HERMANN, J., GAUCHAT, J. F., GASCAN, H. & CHEVALIER, S. (2001) The ciliary neurotrophic factor receptor alpha component induces the secretion of and is required for functional responses to cardiotrophin-like cytokine. EMBO J. 20, 169–1703.
POWERS, C. J., MCLESKEY, S. W. & WELLSTEIN, A. (2000) Fibroblast growth factors, their receptors and signaling. Endocrine-Related Cancer. 7, 16–197.
PU, S. F., ZHUANG, H. X., MARSH, D. J. & ISHII, D. N. (1999a) Insulin-like growth factor-II increases and IGF is required for postnatal rat spinal motoneuron survival following sciatic nerve axotomy. J. Neurosci. Res. 55, –16.
PU, S. F., ZHUANG, H. X., MARSH, D. J. & ISHII, D. N. (1999b) Time-dependent alteration of insulin-like growth factor gene expression during nerve regeneration in regions of muscle enriched with neuromuscular junctions. Brain Res. Mol. Brain Res. 63, 20–216.
RAMER, M. S., THOMPSON, S. W. & MCMAHON, S. B. (1999) Causes and consequences of sympathetic basket formation in dorsal root ganglia. Pain Suppl, S11– S120.
RAMIREZ, J. J., FINKLESTEIN, S. P., KELLER, J., ABRAMS, W., GEORGE, M. N. & PARAKH, T. (1999) Basic fibroblast growth factor enhances sprouting after cortical injury in rats. NeuroReport. 10, 120–1024.
RENDE, M., GIAMBANCO, I., BURATTA, M. & TONALI, P. (1995) Axotomy induces a different modulation of both low-affinity nerve growth factor receptor and choline acetyltransferase between adult rat spinal and brainstem motoneurons. J. Comp. Neurol. 363, 24–263.
RENDE, M., PROVENZANO, C. & TONALI, P. (1993) Modulation of low-affinity nerve growth factor receptor in injured adult rat spinal cord motoneurons. J. Comp. Neurol. 338, 56–574.
REYNOLDS, M. L. & WOOLF, C. J. (1992) Terminal Schwann cells elaborate extensive processes following denervation of the motor endplate. J. Neurocytol. 21, 5–66.
ROMERO, M. I., RANGAPPA, N., LI, L., LIGHTFOOT, E., GARRY, M. G. & SMITH, G. M. (2000) Extensive sprouting of sensory afferents and hyperalgesia induced by conditional expression of nerve growth factor in the adult spinal cord. J. Neurosci. 20, 443–4445.
SALA, C., ANDREOSE, J. S., FUMAGALLI, G. & LOMO, T. (1995) Calcitonin gene-related peptide: Possible role in formation and maintenance of neuromsucular junctions. J. Neurosci. 15, 52–528.
SANES, J. R. & LICHTMAN, J. W. (1999) Development of the vertebrate neuromuscular junction. Ann. Rev. Neurosci. 22, 38–442.
SANTAFE, M., URBANO, F. J., LANUZA, M. A. & UCHITEL, O. D. (2000) Multiple types of calcium channels mediate transmitter release during functional recovery of botulinum toxin type A-poisoned mouse motor nerve terminals. Neurosci. 95, 22–234.
SCHLESSINGER, J. & ULLRICH, A. (1992) Growth factor signaling by receptor tyrosine kinases. Neuron 9, 38– 391.
SIDDLE, K., SOOS, M. A., FIELD, C. E. & NAVE, B. T. (1994) Hybrid and atypical insulin/insulin-like growth factor I receptors. Hormone Res. 41, 5–64.
SIDDLE, K., URSO, B., NIESLER, C. A., COPE, D. L., MOLINA, L., SURINYA, K. H. & SOOS, M. A. (2001) Specificity in ligand binding and intracellular signalling by insulin and insulin-like growth factor receptors. Biochem. Soc. Trans. 29, 51–525.
SIEGEL, S. G., PATTON, B. & ENGLISH, A. W. (2000) Ciliary neurotrophic factor is required for motoneuron sprouting. Exp. Neurol. 166, 20–212.
SILLETTI, S. & RAZ, A. (1993) Autocrine motility factor is a growth factor. Biochem. Biophys. Res. Com. 194, 44– 457.
SILLETTI, S. & RAZ, A. (1996) Regulation of autocrine motility factor receptor expression in tumor cell locomotion and metastasis. Curr. Top. Microbiol. Immunol. 213, 13–169.
SKENE, J. H. (1989) Axonal growth-associated proteins. Ann. Rev. Neurosci. 12, 12–156.
SLEEMAN, M. W., ANDERSON, K. D., LAMBERT, P. D., YANCOPOULOS, G. D. & WIEGAND, S. J. (2000) The ciliary neurotrophic factor and its receptor, CNTFR alpha. Pharmaceut. Acta Helvet. 74, 26–272.
SON, Y.-J. & THOMPSON, W. J. (1995) Nerve sprouting in muscle is induced and guided by processes extended by Schwann cells. Neuron 14, 13–141.
SOOS, M. A., FIELD, C. E. & SIDDLE, K. (1993) Purified hybrid insulin/insulin-like growth factor-I receptors bind insulin-like growth factor-I, but not insulin, with high affinity. Biochem. J. 290, 41–426.
STAHL, N. & YANCOPOULOS, G. D. (1994) The tripartite CNTF receptor complex: Activation and signaling involves components shared with other cytokines. J. Neurobiol. 25, 145–1466.
STOCKLI, K. A., LILLIEN, L. E., NAHER-NOE, M., BREITFELD, G., HUGHES, R. A., RAFF, M. C., THOENEN, H. & SENDTNER, M. (1991) Regional distribution, developmental changes, and cellular localization of CNTF-mRNA and protein in the rat brain. J. Cell Biol. 115, 44–459.
STOOP, R. & POO, M. M. (1996) Synaptic modulation by neurotrophic factors. Progr. Brain Res. 109, 35–364.
STRACKE, M. L., GUIRGUIS, R., LIOTTA, L. A. & SCHIFFMANN, E. (1987) Pertussis toxin inhibits stimulated motility independently of the adenylate cyclase pathway inhumanmelanoma cells. Biochem. Biophys. Res. Com. 146, 33–345.
TAKAHASHI, M. (2001) THe GDNF/Ret signaling pathway and human diseases. Cytokine Growth Factor Rev. 12, 36–373.
TARABAL, O., CALDERO, J. & ESQUERDA, J. E. (1996) Intramuscular nerve sprouting induced by CNTF is associated with increases in CGRP content in mouse motor nerve terminals. Neurosci. Lett. 219, 6–64.
THOMPSON, S. W. & MAJITHIA, A. A. (1998) Leukemia inhibitory factor induces sympathetic sprouting in intact dorsal root ganglia in the adult rat in vivo. J. Physiol. (Lond.) 506, 80–816.
TORIGOE, K. (1985) Distribution of motor nerve sprouting in the mouse gastrocnemius muscle after partial denervation. Brain Res. 330, 27–282.
TRUPP, M., SCOTT, R. W., WHITEMORE, S. R. & IBANEZ, C. F. (1999) Ret-dependent and-independent mechanisms of glial cell line-derived neurotrophic factor signaling in neuronal cells. J. Biol. Chem. 274, 2088–20894.
TSOULFAS, P., SOPPET, D., ESCANDON, E., TESSAROLLO, L., MENDOZA-RAMIREZ, J. L., ROSENTHAL, A., NIKOLICS, K. & PARADA, L. F. (1993) The rat trkC locus encodes multiple neurogenic receptors that exhibit differential response to neurotrophin-3 in PC12 cells. Neuron 10, 97–990.
TSUI-PIERCHALA, B. A., ENCINAS, M., MILBRANDT, J. & JOHNSON, E. M., JR. (2002) Lipid rafts in neuronal signaling and function. Trends Neurosci. 25, 41–417.
VALENZUELA, D. M., MAISONPIERRE, P. C., GLASS, D. J., ROJAS, E., NUNEZ, L., KONG, Y., GIES, D. R., STITT, T. N., IP, N. Y. & YANCOPOULOS, G. D. (1993) Alternative forms of rat TrkC with different functional capabilities. Neuron 10, 96–974.
VLODAVSKY, I., MIAO, H. Q., MEDALION, B., DANAGHER, P. & RON, D. (1996) Involvement of heparan sulfate and related molecules in sequestration and growth promoting activity of fibroblast growth factor. Cancer Metast. Rev. 15, 17–186.
WALSH, F. S. & DOHERTY, P. (1991) Glycosylphosphatidylinositol anchored recognition molecules that function in axonal fasciculation, growth and guidance in the nervous system. Cell Biol. Internatl. Rep. 15, 115– 1166.
WALSH, F. S. & DOHERTY, P. (1997) Neural cell adhesion molecules of the immunoglobulin superfamily: Role in axon growth and guidance Ann. Rev. Cell Dev. Biol. 13, 42–456.
WALSH, F. S., HOBBS, C., WELLS, D. J., SLATER, C. R. & FAZELI, S. (2000) Ectopic expression of NCAM in skeletal muscle of transgenic mice results in terminal sprouting at the neuromuscular junction and altered structure but not function. Mol. Cell. Neurosci. 15, 24–261.
WALSH, F. S., MEIRI, K. & DOHERTY, P. (1997) Cell signalling and CAM-mediated neurite outgrowth. Soc. Gen. Physiol. Ser. 52, 22–226.
WATANABE, H., TAKEHANA, K., DATE, M., SHINOZAKI, T. & RAZ, A. (1996) Tumor cell autocrine motility factor is the neuroleukin/phosphohexose isomerase polypeptide. Cancer Res. 56, 296– 2963.
WEIS, J., LIE, D. C., RAGOSS, U., ZUCHNER, S. L., SCHRODER, J. M., KARPATI, G., FARRUGGELLA, T., STAHL, N., YANCOPOULOS, G. D. & DISTEFANO, P. S. (1998) Increased expression of CNTF receptor alpha in denervated human skeletal muscle. J. Neuropath. Exp. Neurol. 57, 85– 857.
WELLS, D. G., MCKECHNIE, B. A., KELKAR, S. & FALLON, J. R. (1999) Neurotrophins regulate agrininduced postsynaptic differentiation. Proc. Natl. Acad. Sci. USA 96, 111–1117.
WIGSTON, D. J. (1990) Repeated in vivo visualization of neuromuscular junctions in adult mouse lateral gastrocnemius. J. Neurosci. 10, 175–1761.
WINES, M. M. & HALL-CRAGGS, E. C. (1986) Neuromuscular relationships in a muscle having segregated motor endplate zones. II. The response to partial denervation. J. Comp. Neurol. 249, 15–156.
XU, W., SEITER, K., FELDMAN, E., AHMED, T. & CHIAO, J. W. (1996) The differentiation and maturation mediator for human myeloid leukemia cells shares homology with neuroleukin or phosphoglucose isomerase. Blood. 87, 450–4506.
YAMADA, S., BUFFINGER, N., DIMARIO, J. & STROHMAN, R. C. (1989) Fibroblast growth factor is stored in fiber extracellular matrix and plays a role in regulating muscle hypertrophy. Med. Sci. Sports Exer. 21, S17–180.
YOSHINOUCHI, M., MIURA, M., GAOZZA, E., LI, S. W. & BASERGA, R. (1993) Basic fibroblast growth factor stimulates DNA synthesis in cells overexpressing the insulin-like growth factor-I receptor. Mol. Endocrinol. 7, 116–1168.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
English, A.W. Cytokines, growth factors and sprouting at the neuromuscular junction. J Neurocytol 32, 943–960 (2003). https://doi.org/10.1023/B:NEUR.0000020634.59639.cf
Issue Date:
DOI: https://doi.org/10.1023/B:NEUR.0000020634.59639.cf