Loss of leukemia inhibitory factor receptor β or cardiotrophin-1 causes similar deficits in preganglionic sympathetic neurons and adrenal medulla

Journal of Neuroscience

Volumn 26, Issue 6, 2006, Pages 1823-1832

  Oberle, Stephan ^a   Schober, Andreas ^a   Meyer, Verena ^a   Holtmann, Bettina ^b   Henderson, Christopher ^c   Sendtner, Michael ^b   Unsicker, Klaus ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Adrenal medulla; Cardiotrophin 1; Ciliary neurotrophic factor; Intermediolateral column; LIFR ; Preganglionic sympathetic neurons

Indexed keywords

ADRENALIN; CARDIOTROPHIN 1; CILIARY NEUROTROPHIC FACTOR; LEUKEMIA INHIBITORY FACTOR RECEPTOR; LEUKEMIA INHIBITORY FACTOR RECEPTOR BETA; UNCLASSIFIED DRUG;

ADRENAL GLAND; ADRENAL MEDULLA; ANIMAL TISSUE; ARTICLE; CHROMAFFIN CELL; CONTROLLED STUDY; EMBRYO; GENE DELETION; MOTONEURON; MOUSE; NERVE FIBER; NONHUMAN; PREGANGLIONIC NERVE CELL; PRIORITY JOURNAL; RAT; SPINAL CORD; STATISTICAL SIGNIFICANCE; SYMPATHETIC NERVE CELL;

ACTINS; ADRENAL MEDULLA; ANIMALS; BENZYLAMINES; CYTOKINES; DIZOCILPINE MALEATE; HIPPOCAMPUS; INTERLEUKIN-6; LEUKEMIA INHIBITORY FACTOR; MICE; NERVE FIBERS; NEURONS; OLIGOPEPTIDES; PROTEIN KINASE INHIBITORS; SULFONAMIDES; SYMPATHETIC NERVOUS SYSTEM; SYNAPSES; SYNAPTIC MEMBRANES; SYNAPTOSOMES;

EID: 32544436998     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4127-05.2006     Document Type: Article

References (56)

1. Andrä J, Lojda Z (1986) A histochemical method for the demonstration of acetylcholinesterase activity using semipermeable membranes. Histochemistry 84:575-579.
2. Arakawa Y, Sendtner M, Thoenen H (1990) Survival effect of ciliary neurotrophic factor (CNTF) on chick embryonic motoneurons in culture: comparison with other neurotrophic factors and cytokines. J Neurosci 10:3507-3515.
3. Bazan JF (1991) Neuropoietic cytokines in the hematopoietic fold. Neuron 7:197-208.
4. Blottner D, Baumgarten H-G (1992) Nitric oxides synthas (NOS)-containing sympathoadrenal cholinergic neurons of the rat IML-cell column: evidence from histochemistry, and retrograde labeling. J Comp Neurol 316:45-55.
5. Blottner D, Unsicker K (1990) Maintenance of intermediolateral spinal cord neurons by fibroblast growth factor administered to the medullectomized rat adrenal gland: dependence on intact organ innervation and cellular organization of implants. Eur J Neurosci 2:378-382.
6. Blottner D, Brüggemann W, Unsicker K (1989) Ciliary neurotrophic factor supports target-deprived preganglionic sympathetic spinal cord neurons. Neurosci Lett 105:316-320.
7. Blottner D, Wolf N, Lachmund A, Flanders KC, Unsicker K (1996) TGF-β rescues target deprived preganglionic sympathetic neurons in the spinal cord. Eur J Neurosci 8:202-210.
8. Cheema SS, Richards LJ, Murphy M, Bartlett PF (1994) Leukaemia inhibitory factor rescues motoneurones from axotomy-induced cell death. NeuroReport 5:989-992.
9. Daikoku S, Kinutani M, Sako M (1977) Development of the adrenal medullary cells in rats with reference to synaptogenesis. Cell Tissue Res 179:77-86.
10. Derouet D, Rousseau F, Alfonsi F, Froger J, Hermann J, Barbier F, Perret D, Diveu C, Guillet C, Preisser L, Dumont A, Barbado M, Morel A, deLapeyriere O, Gascan H, Chevalier S (2004) Neuropoietin, a new IL-6-related cytokine signaling through the ciliary neurotrophic factor receptor. Proc Natl Acad Sci USA 101:4827-4832.
11. Ernsberger U, Patzke H, Rohrer H (1997) The developmental expression of choline acetyltransferase (ChAT) and the neuropeptide VIP in chick sympathetic neurons: evidence for different regulatory events in cholinergic differentiation. Mech Dev 68:115-126.
12. Ernsberger U, Reissmann E, Mason I, Rohrer H (2000) The expression of dopamine beta-hydroxylase, tyrosine hydroxylase, and Phox2 transcription factors in sympathetic neurons: evidence for common regulation during noradrenergic induction and diverging regulation later in development. Mech Dev 92:169-177.
13. Forger NG, Prevette D, deLapeyriere O, de Bovis B, Wang S, Bartlett P, Oppenheim RW (2003) Cardiotrophin-like cytokine/cytokine-like factor 1 is an essential trophic factor for lumbar and facial motoneurons in vivo. J Neurosci 23:8854-8858.
14. Gearing DP, Gough NM, King JA, Hilton DJ, Nicola NA, Simpson RJ, Nice EC, Kelso A, Metcalf D (1987) Molecular cloning and expression of cDNA encoding a murine myeloid leukaemia inhibitory factor (LIF). EMBO J 6:3995-4002.
15. Gearing DP, Thut CJ, VandeBos T, Gimpel SD, Delaney PB, King J, Price V, Cosman D, Beckmann MP (1991) Leukemia inhibitory factor receptor is structurally related to the IL-6 signal transducer, gp130. EMBO J 10:2839-2848.
16. Gearing DP, Comeau MR, Friend DJ, Gimpel SD, Thut CJ, McGourty J, Brasher KK, King JA, Gillis S, Mosley B, Zeigler SF, Cosman D (1992) The IL-6 signal transducer, gp130: an oncostatin M receptor and affinity converter for the LIF receptor. Science 255:1434-1437.
17. Gould TW, Oppenheim RW (2004) The function of neurotrophic factor receptors expressed by the developing adductor motor pool in vivo. J Neurosci 12:4668-4682.
18. Heinrich PC, Behrmann I, Haan S, Hermanns HM, Muller-Newen G, Schaper F (2003) Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem J 374:1-20.
19. Holtmann B, Wiese S, Samsam M, Grohmann K, Pennica D, Martini R, Sendtner M (2005) Triple knock-out of CNTF, LIF, and CT-1 defines cooperative and distinct roles of these neurotrophic factors for motoneuron maintenance and function. J Neurosci 25:1778-1787.
20. Huber K, Brühl B, Guillemot F, Olson EN, Ernsberger U, Unsicker K (2002) Development of chromaffin cells depends on MASH1 function. Development 129:4729-4738.
21. Ishii K, Oda Y, Ichikawa T, Deguchi T (1990) Complementary DNAs for choline acetyltransferase from spinal cords of rat and mouse: nucleotide sequences, expression in mammalian cells, and in situ hybridization. Brain Res Mol Brain Res 7:151-159.
22. Lawson SJ, Davies HJ, Bennett JP, Lowrie MB (1997) Evidence that spinal interneurons undergo programmed cell death postnatally in the rat. Eur J Neurosci 9:794-799.
23. Leung DW, Parent AS, Cachianes G, Esch F, Coulombe JN, Nikolics K, Eckenstein FP, Nishi R (1992) Cloning, expression during development, and evidence for release of a trophic factor for ciliary ganglion neurons. Neuron 8:1045-1053.
24. Li M, Sendtner M, Smith A (1995) Essential function of LIF receptor in motor neurons. Nature 378:724-727.
25. Lin LF, Mismer D, Lile JD, Armes LG, Butler ET, Vannice JL, Collins F (1989) Purification, cloning, and expression of ciliary neurotrophic factor (CNTF). Science 246:1023-1025.
26. Markham JA, Vaughn JE (1991) Migration patterns of sympathetic preganglionic neurons in embryonic rat spinal cord. J Neurobiol 22:811-822.
27. Martinou JC, Martinou I, Kato AC (1992) Cholinergic differentiation factor (CDF/LIF) promotes survival of isolated rat embryonic motoneurons in vitro. Neuron 8:737-744.
28. Meyer V, Unsicker K (1994) Cell density and exogenous CNTF affect CNTF mRNA levels in glial cell cultures. NeuroReport 5:1946-1948.
29. Morikawa Y (2005) Oncostatin M in the development of the nervous system. Anat Sci Int 80:53-59.
30. Morita K, Wong DL (1996) Role of Egr-1 in cholinergic stimulation of phenylethanolamine N-methyltransferase promoter. J Neurochem 67:1344-1351.
31. Müller TH, Unsicker K (1981) High-performance liquid chromatography with electrochemical detection as highly efficient tool for studying catecholaminergic systems. I. Quantification of noradrenaline, adrenaline and dopamine in cultured adrenal medullary cells. J Neurosci Methods 4:39-52.
32. Oppenheim RW (1991) Cell death during development of the nervous system. Annu Rev Neurosci 14:453-501.
33. Oppenheim RW, Maderdrut JL, Wells DJ (1982) Cell death of motoneurons in the chick embryo spinal cord. VI. Reduction of naturally occurring cell death in the thoracolumbar column of Terni by nerve growth factor. J Comp Neurol 210:174-189.
34. Oppenheim RW, Wiese S, Prevette D, Armanini M, Wang S, Houenou LJ, Holtmann B, Gotz R, Pennica D, SendtnerM (2001) Cardiotrophin-1, a muscle-derived cytokine, is required for the survival of subpopulations of developing motoneurons. J Neurosci 21:1283-1291.
35. Parker TL, Kesse WK, Tomlinson A, Coupland RE (1988) Ontogenesis of preganglionic sympathetic innervation of rat adrenal chromaffin cells. In: Progress in catecholamine research, part A, basic aspects and peripheral mechanisms (Dahlström A, Belmaker RH, Sandler M, eds), pp 227-232. New York: Alan R. Liss.
36. Pennica D, Shaw KJ, Swanson TA, Moore MW, Shelton DL, Zioncheck KA, Rosenthal A, Taga T, Paoni NF, Wood WI (1995) Cardiotrophin-1. Biological activities and binding to the leukemia inhibitory factor receptor/gp130 signaling complex. J Biol Chem 270:10915-10922.
37. Pennica D, Arce V, Swanson TA, Vejsada R, Pollock RA, Armanini M, Dudley K, Phillips HS, Rosenthal A, Kato AC, Henderson CE (1996) Cardiotrophin-1, a cytokine present in embryonic muscle, supports longterm survival of spinal motoneurons. Neuron 17:63-74.
38. Pyner S, Coote JH (1994) Evidence that sympathetic preganglionic neurones are arranged in target-specific columns in the thoracic spinal cord of the rat. J Comp Neurol 342:15-22.
39. Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208-212.
40. Rind HB, Butowt R, von Bartheld CS (2005) Synaptic targeting of retrogradely transported trophic factors in motoneurons: comparison of glial cell line-derived neurotrophic factor, brain-derived neurotrophic factor, and cardiotrophin-1 with tetanus toxin. J Neurosci 25:539-549.
41. Roosen A, Schober A, Strelau J, Böttner M, Faulhaber J, Bendner G, Seller H, Ehmke H, McIllwarth SL, Lewin GR, Unsicker K (2001) Lack of NT-4 causes selective structural and chemical deficits in sympathetic ganglia and their preganglionic innervation. J Neurosci 21:3073-3084.
42. Schober A, Unsicker K (2001) Growth and neurotrophic factors regulating development and maintenance of sympathetic preganglionic neurons. Int Rev Cytol 205:37-76.
43. Schober A, Minichiello L, Keller M, Huber K, Layer PG, Roig-López JL, García-Arrarás JE, Klein R, Unsicker K (1997) Reduced acetylcholinesterase (AChE) activity in adrenal medulla and loss of sympathetic preganglionic neurons in TrkA-deficient, but not TrkB-deficient, mice. J Neurosci 17:891-903.
44. Schober A, Wolf N, Huber K, Hertel R, Krieglstein K, Minichiello L, Kahane N, Widenfalk J, Kalcheim C, Olson L, Klein R, Lewin GR, Unsicker K (1998) TrkB and neurotrophin-4 are important for development and maintenance of sympathetic preganglionic neurons innervating the adrenal medulla. J Neurosci 18:7272-7284.
45. Schober A, Hertel R, Arumae U, Farkas L, Jaszai J, Krieglstein K, Saarma M, Unsicker K (1999) Glial cell line-derived neurotrophic factor rescues target-deprived sympathetic spinal cord neurons but requires transforming growth factor-β as cofactor in vivo. J Neurosci 19:2008-2015.
46. Seidler FJ, Slotkin TA (1985) Adrenomedullary function in the neonatal rat: response to acute hypoxia. J Physiol (Lond) 358:1-16.
47. Sendtner M, Kreutzberg GW, Thoenen H (1990) Ciliary neurotrophic factor prevents the degeneration of motor neurons after axotomy. Nature 345:440-441.
48. Smeyne RJ, Klein R, Schnapp A, Long LK, Bryant S, Lewin A, Lira SA, Barbacid M (1994) Severe sensory and sympathetic neuropathies in mice carrying a disrupted Trk/NGF receptor gene. Nature 368:193-194.
49. Stöckli KA, Lottspeich F, Sendtner M, Masiakowski P, Carroll P, Gotz R, Lindholm D, Thoenen H (1989) Molecular cloning, expression and regional distribution of rat ciliary neurotrophic factor. Nature 342:920-923.
50. Strack AM, Sawyer WB, Marubio LM, Loewy AD (1988) Spinal origin of sympathetic preganglionic neurons in the rat. Brain Res 455:187-191.
51. Unsicker K, Reichert-Preibsch H, Schmidt R, Pettmann B, Labourdette G, Sensenbrenner M (1987) Astroglial and fibroblast growth factors have neurotrophic functions for cultured peripheral and central nervous system neurons. Proc Natl Acad Sci USA 84:5459-5463.
52. Ware CB, Horowitz MC, Renshaw BR, Hunt JS, Liggitt D, Koblar SA, Gliniak BC, McKenna HJ, Papayannopoulou T, Thoma B, Cheng L, Danovan PJ, Peschon JJ, Bartlett PF, Willis CR, Wright BD, Carpenter MK, Davison BL, Gearing DP (1995) Targeted disruption of the low-affinity leukemia inhibitory factor receptor gene causes placental, skeletal, neural and metabolic defects and results in perinatal death. Development 121:1283-1299.
53. Wetts R, Vaughn JE (1998) Differences in developmental cell death between somatic and autonomic motor neurons of rat spinal cord. J Comp Neurol 396:483-492.
54. Wong V, Arriaga R, Ip NY, Lindsay RM (1993) The neurotrophins BDNF, NT-3 and NT-4/5, but not NGF, up-regulate the cholinergic phenotype of developing motor neurons. Eur J Neurosci 5:466-474.
55. Wurtman RJ, Axelrod J (1965) Adrenaline synthesis: control by the pituitary gland and adrenal glucocorticoids. Science 150:1464-1465.
56. Wurtman RJ, Axelrod J, Vesell ES, Ross GT (1968) Species differences in inducibility of phenylethanolamine-N-methyl transferase. Endocrinology 82:584-590.