Developmental changes in the transmitter properties of sympathetic neurons that innervate the periosteum

Journal of Neuroscience

Volumn 20, Issue 4, 2000, Pages 1495-1504

  Asmus, Stephen E ^a,b   Parsons, Sarah ^a   Landis, Story C ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b CENTRE COLLEGE   (United States)

Author keywords

Autonomic neurons; Cholinergic differentiation factor; Neural crest; Neuropoietic cytokines; Sweat glands; Synapse formation; Transmitter plasticity

Indexed keywords

CYTOKINE; NEUROPEPTIDE; OXIDOPAMINE; VASOACTIVE INTESTINAL POLYPEPTIDE;

ANIMAL TISSUE; ARTICLE; IMMUNOCYTOCHEMISTRY; NERVE FIBER GROWTH; NEURAL CREST; NEUROTRANSMISSION; NEWBORN; NONHUMAN; PERIOSTEUM; PRIORITY JOURNAL; RAT; STERNUM; SWEAT GLAND; SYMPATHETIC NERVE CELL;

EID: 0034652131     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-04-01495.2000     Document Type: Article

References (64)

1. Alfonso A, Grundahl K, McManus JR, Ashury JM, Rand JB (1994) Alternative splicing leads to two cholinergic proteins in Caenorhabditis elegans. J Mol Biol 241:627-630.
2. Bazan JF (1991) Neuropoietic cytokines in the hematopoetic fold. Neuron 7:197-208.
3. Bejanin S, Cervini R, Mallet J, Berrard S (1994) A unique gene organization for two cholinergic markers, choline acetyltransferase and a putative vesicular transporter of acetylcholine. J Biol Chem 269:21944-21947.
4. Berrard S, Varoqui H, Cervini R, Israel M, Mallet J, Diebler M-F (1995) Coregulation of two embedded gene products, choline acetyltransferase and the vesicular acetylcholine transporter. J Neurochem 65:939-942.
5. Berse B, Blusztajn JK (1995) Coordinated up-regulation of choline acetyltransferase and vesicular acetylcholine transporter gene expression by the retinoic acid receptor alpha, cAMP, and leukemia inhibitory factor/ciliary neurotrophic factor signaling pathways in a murine septal cell line. J Biol Chem 270:22101-22104.
6. Bjurholm A, Kreicbergs A, Terenius L, Goldstein M, Schultzberg M (1988) Neuropeptide Y, tyrosine hydroxylase- and vasoactive intestinal polypeptide-immunoreactive nerves in bone and surrounding tissues. J Auton Nerv Syst 25:119-125.
7. Bjurholm A, Kreicbergs A, Dahlberg L, Schultzherg M (1990) The occurrence of neuropeptides at different stages of DBM-induced heterotopic bone formation. Bone Miner 10:95-107.
8. Burman MS, Umansky M (1930) An experimental study of free periosteal transplants wrapped around tendon. J Bone Joint Surg Am 12:579-594.
9. Cochard PM, Goldstein M, Black IB (1979) Initial development of the noradrenergic phenotype in autonomic neuroblasts of the rat embryo in vivo. Dev Biol 71:100-114.
10. Coulombe JN, Nishi R (1991) Stimulation of somatostatin expression in developing ciliary ganglion neurons by cells of the choroid layer. J Neurosci 11:553-562.
11. Dale HH, Feldberg W (1934) The chemical transmission of secretory impulses to the sweat glands of the cat. J Physiol (Lond) 82:121-123.
12. Darland DC, Nishi R (1998) Activin A and follistatin influence expression of somatostatin in the ciliary ganglion in vivo. Dev Biol 202:292-303.
13. de la Torre JC (1980) An improved approach to histofluorescence using the SPG method for tissue monoamines. J Neurosci Methods 3:1-5.
14. Erickson JD, Varoqui H, Schaffer MK-H, Modi W, Diebler M-F, Weihe E, Rand J, Eiden LE, Bonner TI, Usdin TB (1994) Functional identification of a vesicular acetylcholine transporter and its expression from a "cholinergic" gene locus. J Biol Chem 269:21929-21932.
15. Finch L, Haeusler G, Thoenen H (1973) A comparison of the effects of chemical sympathectomy by 6-hydroxydopamine in newborn and adult rats. Br J Pharmacol 47:249-260.
16. Francis NJ, Asmus SE, Landis SC (1997) CNTF and LIF are not required for the target-directed acquisition of cholinergic and peptidergic properties by sympathetic neurons in vivo. Dev Biol 182:76-87.
17. Fukada K (1985) Purification and partial characterization of a cholinergic differentiation factor. Proc Natl Acad Sci USA 82:8795-8799.
18. Grant MP, Francis NJ, Landis S (1995) The role of acetylcholine in regulating secretory responsiveness in rat sweat glands. Mol Cell Neurosci 6:32-42.
19. Guidry G, Landis S (1998a) Developmental regulation of neurotransmitters in sympathetic neurons. Adv Pharmacol 42:895-898.
20. Guidry G, Landis SC (1998b) Target-dependent development of the vesicular acetylcholine transporter in rodent sweat gland innervation. Dev Biol 199:175-184.
21. Habecker BA, Pennica D, Landis SC (1995) Cardiotrophin-1 is not the sweat gland derived factor. NeuroReport 7:41-44.
22. Habecker BA, Symes AJ, Stahl N, Francis NJ, Economides A, Fink J, Yancopoulos GD, Landis S (1997) A sweat gland-derived differentiation activity acts through known cytokine signaling pathways. J Biol Chem 272:30421-30428.
23. Hall AK, MacPhedran SE (1995) Multiple mechanisms regulate sympathetic neuronal phenotype. Development 121:2361-2371.
24. Hall BK (1970) Cellular differentiation in skeletal tissues. Biol Rev 45:455-484.
25. Hill EL, Elde R (1991) Distribution of cGRP-, VIP-, SP-, and NPY- immunoreactive nerves in the periosteum of the rat. Cell Tissue Res 264:469-480.
26. Hill EL, Turner R, Eide R (1991) Effects of neonatal sympathectomy and capsaicin treatment on bone remodeling in rats. Neuroscience 44:747-755.
27. Hohmann EL, Tashjian AH (1984) Functional receptors for vasoactive intestinal peptide on human osteosarcoma cells. Endocrinology 114:1321-1327.
28. Hohmann EL, Levine L, Tashjian AH (1983) Vasoactive intestinal peptide stimulates bone resporption via a cyclic adenosine 3,5′-monophosphate-dependent mechanism. Endocrinology 112:1233-1239.
29. Hohmann EL, Elde RP, Rysavy JA, Einzig S, Gehhard RL (1986) Innervation of periosteum and bone by sympathetic vasoactive intestinal peptide-containing nerve fibers. Science 232:868-871.
30. Horgan K, van der Kooy D (1992) Visceral targets specify calcitonin gene-related peptide and substance P enrichment in trigeminal afferent projections. J Neurosci 12:1135-1143.
31. Hyatt-Sachs H, Schreiber R, Bennett T, Zigmond R (1993) Phenotypic plasticity in adult sympathetic ganglia in vivo: effects of deafferentation and axotomy on the expression of vasoactive intestinal peptide. J Neurosci 13:1642-1653.
32. Kummer W, Heym C (1988) Neuropeptide distribution in the cervicothoracic paravertebral ganglia of the cat with particular reference to calcitonin gene-related peptide immunoreactivity. Cell Tissue Res 252:463-471.
33. Landis SC, Keefe D (1983) Evidence for neurotransmitter plasticity in vivo: developmental changes in the properties of cholinergic sympathetic neurons. Dev Biol 98:349-372.
34. Landis SC, Schwab M, Siegel RE (1988) Evidence for neurotransmitter plasticity in vivo. II. Immunocytochemical studies of rat sweat gland innervation during development. Dev Biol 126:129-138.
35. Langley JN (1891) On the course and connections of the secretory fibers supplying the sweat glands of the feet of the cat. J Physiol (Lond) 12:347-369.
36. Leblanc G, Landis SC (1986) Development of choline acetyltransferase activity in the cholinergic sympathetic innervation of sweat glands. J Neurosci 6:260-265.
37. Lindh B, Lundberg J, Hokfelt T (1989) NPY-, galanin-, VIP/PHI-, CGRP- and substance P-immunoreactive neuronal subpopulations in cat autonomic and sensory ganglia and their projections. Cell Tissue Res 256:259-273.
38. Lundberg JM, Hokfelt T, Schultzberg M, Uvnas-Wallensten K, Kohler C, Said SI (1979) Occurrence of vasoactive intestinal polypeptide(VIP)-like immunoreactivity in certain cholinergic neurons of the cat: evidence from combined immunohistochemistry and acetylcholinesterase staining. Neuroscience 4:1539-1559.
39. Mclaughlin BJ, Wood JG, Saito K, Roberts E, Wu JY (1975) The fine structural localization of glutamate decarhoxylase in developing axonal processes and presynaptic terminals of rodent cerebellum. Brain Res 85:355-371.
40. Misawa H, Takahashi R, Deguchi T (1995) Coordinate expression of vesicular acetylcholine transporter and choline acetyltransferase in sympathetic superior cervical neurones. NeuroReport 6:965-968.
41. Morales MA, Holmberg K, Xu Z, Cozzari C, Hartman B, Emson P, Goldstein M, Elfvin L, Hokfelt T (1995) Localization of choline acetyltransferase in rat peripheral sympathetic neurons and its coexistence with nitric oxide synthase and neuropeptides. Proc Natl Acad Sci USA 92:11819-11823.
42. Patterson P (1992) The emerging neuropoietic cytokine family: first CDF/LIF, CNTF and IL-6; next ONC, MGF GCSF? Curr Opin Neurobiol 2:94-97.
43. Pennica D, Shaw KJ, Swanson TA, Moore MW, Shelton DL, Zioncheck KA, Rosenthal A, Taga T, Paoni NF, Wood WW (1995) Cardiotrophin-1: biological activities and binding to the leukemia inhibitory factor receptor/gp130 signalling complex. J Biol Chem 270:10915-10922.
44. Rao M, Landis S (1990) Characterization of a target-derived neuronal cholinergic differentiation factor. Neuron 5:899-910.
45. Rao MS, Patterson PH, Landis SC (1992) Multiple cholinergic differentiation factors are present in footpad extracts: comparison with known cholinergic factors. Development 116:731-744.
46. Rao MS, Escary J, Sun Y, Perreau J, Patterson PH, Zigmond RE, Brulet P, Landis SC (1993) Leukemia inhibitory factor mediates an injury response hut not a target-mediated developmental transmitter switch in sympathetic neurons. Neuron 11:1175-1185.
47. Roghani A, Shirzadi A, Butcher LL, Edwards RH (1998) Distribution of the vesicular transporter for acetylcholine in the rat central nervous system. Neuroscience 82:1195-1212.
48. Romano SJ, Corriveau RA, Schwarz RI, Berg DK (1997) Expression of the nicotinic receptor alpha 7 gene in tendon and periosteum during early development. J Neurochem 68:640-648.
49. Saadat S, Sendtner M, Rohrer H (1989) Ciliary neurotrophic factor induces cholinergic differentiation of rat sympathetic neurons in culture. J Cell Biol 108:1807-1816.
50. Sandhu HS, Herskovits MS, Singh IJ (1987) Effect of surgical sympathectomy on bone remodeling at rat incisor and molar root sockets. Anat Rec 219:32-38.
51. Sandhu HS, Kwong-Hing A, Herskovits MS, Singh IJ (1990) The effects of surgical sympathectomy on bone resorption in the rat incisor socket. Arch Oral Biol 35:1003-1007.
52. Schafer MK, Eiden LE, Weihe E (1998) Cholinergic neurons and terminal fields revealed by immunohistochemistry for the vesicular acetylcholine transporter. II. The peripheral nervous system. Neuroscience 84:361-376.
53. Schotzinger R, Landis SC (1988) Cholinergic phenotype developed by noradrenergic sympathetic neurons after innervation of a novel cholinergic target in vivo. Nature 335:637-639.
54. Schotzinger RJ, Landis SC (1990) Postnatal development of autonomic and sensory innervation of thoracic hairy skin in the rat. Cell Tissue Res 260:575-587.
55. Schotzinger RJ, Yin X, Landis SC (1994) Target determination of neurotransmitter phenotype in sympathetic neurons. J Neurobiol 25:620-639.
56. Singh IJ, Herskovits MS, Chiego DJ, Klein RM (1982) Modulation of osteoblastic activity by sensory and autonomic innervation of bone. In: Factors and mechanisms influencing bone growth (Dixon J, Sarnat M, eds), pp 535-551. New York: Liss.
57. Sjoqvist F (1963) The correlation between the occurrence and localization of acetylcholinesterase-rich cell bodies in the stellate ganglion and the outflow of cholinergic sweat secretory fibers to the fore paw of the cat. Acta Physiol Scand 57:339-351.
58. Specht LA, Pickel VM, Joh TH, Reis DJ (1981) Light-microscopic immunocytochemical localization of tyrosine hydroxylase in prenatal rat brain. I. Early ontogeny. J Comp Neurol 199:233-253.
59. Stevens LM, Landis SC (1987) Development and properties of the secretory response in rat sweat glands: relationship to the induction of cholinergic function in sweat gland innervation. Dev. Biol. 123:179-190.
60. Teitelman G, Baker H, Joh TH, Reis DJ (1979) Appearance of catecholamine synthesizing enzymes during development of the rat nervous system: possible role of tissue environment. Proc Natl Acad Sci USA 76:509-513.
61. Tyrrell S, Landis SC (1994) NPY and VIP expression in sympathetic neuroblasts and subsequent regulation of neuropeptide expression. J Neurosci 14:4529-4547.
62. Yamagata M, Sanes JR (1995) Target-independent diversification and target-specific projection of chemically defined retinal ganglion cell subsets. Development 121:3763-3776.
63. Yamamori T, Fukada K, Aebersold R, Korsching S, Fann MJ, Patterson PH (1989) The cholinergic neuronal differentiation factor from heart cells is identical to leukemia inhibitory factor. Science 246:1412-1416.
64. Yodlowski ML, Fredieu JR, Landis SC (1984) Neonatal 6-hydroxy-dopamine treatment eliminates cholinergic sympathetic innervation and induces sensory sprouting in rat sweat glands. J Neurosci 4:1535-1548.