Neuropoietic cytokines and activin A differentially regulate the phenotype of cultured sympathetic neurons (original) (raw)

Abstract

A number of cytokines sharing limited sequence homology have been grouped as a family because of partially overlapping biological activities, receptor subunit promiscuity, and the prediction of a shared secondary structure. Since several of these cytokines regulate gene expression and cell number in the nervous and hematopoietic systems, this specific group is termed the neuropoietic cytokine family. Using a reverse transcription-polymerase chain reaction-based assay system for monitoring the expression of multiple phenotypic markers in cultured sympathetic neurons, we present further evidence that, in addition to cholinergic differentiation factor/leukemia inhibitory factor and ciliary neurotrophic factor, oncostatin M, growth promoting activity, interleukin 6, and interleukin 11 belong in this family. In addition, one member of the transforming growth factor beta superfamily, activin A, shares a selective overlap with the neuropoietic family in the spectrum of neuropeptides that it induces in sympathetic neurons. The particular neuropeptides induced by activin A, however, demonstrate that the activity of this cytokine is distinct from that of the neuropoietic family. Twenty-six other cytokines and growth factors were without detectable activity in this assay.

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  1. Adler R., Landa K. B., Manthorpe M., Varon S. Cholinergic neuronotrophic factors: intraocular distribution of trophic activity for ciliary neurons. Science. 1979 Jun 29;204(4400):1434–1436. doi: 10.1126/science.451576. [DOI] [PubMed] [Google Scholar]
  2. Bazan J. F. Neuropoietic cytokines in the hematopoietic fold. Neuron. 1991 Aug;7(2):197–208. doi: 10.1016/0896-6273(91)90258-2. [DOI] [PubMed] [Google Scholar]
  3. Bruce A. G., Hoggatt I. H., Rose T. M. Oncostatin M is a differentiation factor for myeloid leukemia cells. J Immunol. 1992 Aug 15;149(4):1271–1275. [PubMed] [Google Scholar]
  4. Coulombe J. N., Schwall R., Parent A. S., Eckenstein F. P., Nishi R. Induction of somatostatin immunoreactivity in cultured ciliary ganglion neurons by activin in choroid cell-conditioned medium. Neuron. 1993 May;10(5):899–906. doi: 10.1016/0896-6273(93)90205-6. [DOI] [PubMed] [Google Scholar]
  5. Davis S., Aldrich T. H., Valenzuela D. M., Wong V. V., Furth M. E., Squinto S. P., Yancopoulos G. D. The receptor for ciliary neurotrophic factor. Science. 1991 Jul 5;253(5015):59–63. doi: 10.1126/science.1648265. [DOI] [PubMed] [Google Scholar]
  6. Fann M. J., Patterson P. H. A novel approach to screen for cytokine effects on neuronal gene expression. J Neurochem. 1993 Oct;61(4):1349–1355. doi: 10.1111/j.1471-4159.1993.tb13628.x. [DOI] [PubMed] [Google Scholar]
  7. Fukada K. Purification and partial characterization of a cholinergic neuronal differentiation factor. Proc Natl Acad Sci U S A. 1985 Dec;82(24):8795–8799. doi: 10.1073/pnas.82.24.8795. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gadient R. A., Cron K. C., Otten U. Interleukin-1 beta and tumor necrosis factor-alpha synergistically stimulate nerve growth factor (NGF) release from cultured rat astrocytes. Neurosci Lett. 1990 Sep 18;117(3):335–340. doi: 10.1016/0304-3940(90)90687-5. [DOI] [PubMed] [Google Scholar]
  9. Gearing D. P., Bruce A. G. Oncostatin M binds the high-affinity leukemia inhibitory factor receptor. New Biol. 1992 Jan;4(1):61–65. [PubMed] [Google Scholar]
  10. Gearing D. P., Gough N. M., King J. A., Hilton D. J., Nicola N. A., Simpson R. J., Nice E. C., Kelso A., Metcalf D. Molecular cloning and expression of cDNA encoding a murine myeloid leukaemia inhibitory factor (LIF). EMBO J. 1987 Dec 20;6(13):3995–4002. doi: 10.1002/j.1460-2075.1987.tb02742.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gearing D. P., Thut C. J., VandeBos T., Gimpel S. D., Delaney P. B., King J., Price V., Cosman D., Beckmann M. P. Leukemia inhibitory factor receptor is structurally related to the IL-6 signal transducer, gp130. EMBO J. 1991 Oct;10(10):2839–2848. doi: 10.1002/j.1460-2075.1991.tb07833.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hawrot E., Patterson P. H. Long-term culture of dissociated sympathetic neurons. Methods Enzymol. 1979;58:574–584. doi: 10.1016/s0076-6879(79)58174-9. [DOI] [PubMed] [Google Scholar]
  13. Ip N. Y., Nye S. H., Boulton T. G., Davis S., Taga T., Li Y., Birren S. J., Yasukawa K., Kishimoto T., Anderson D. J. CNTF and LIF act on neuronal cells via shared signaling pathways that involve the IL-6 signal transducing receptor component gp130. Cell. 1992 Jun 26;69(7):1121–1132. doi: 10.1016/0092-8674(92)90634-o. [DOI] [PubMed] [Google Scholar]
  14. Jessell T. M., Melton D. A. Diffusible factors in vertebrate embryonic induction. Cell. 1992 Jan 24;68(2):257–270. doi: 10.1016/0092-8674(92)90469-s. [DOI] [PubMed] [Google Scholar]
  15. Kamegai M., Niijima K., Kunishita T., Nishizawa M., Ogawa M., Araki M., Ueki A., Konishi Y., Tabira T. Interleukin 3 as a trophic factor for central cholinergic neurons in vitro and in vivo. Neuron. 1990 Mar;4(3):429–436. doi: 10.1016/0896-6273(90)90055-k. [DOI] [PubMed] [Google Scholar]
  16. Kishimoto T., Akira S., Taga T. Interleukin-6 and its receptor: a paradigm for cytokines. Science. 1992 Oct 23;258(5082):593–597. doi: 10.1126/science.1411569. [DOI] [PubMed] [Google Scholar]
  17. Landis S. C. Target regulation of neurotransmitter phenotype. Trends Neurosci. 1990 Aug;13(8):344–350. doi: 10.1016/0166-2236(90)90147-3. [DOI] [PubMed] [Google Scholar]
  18. Leung D. W., Parent A. S., Cachianes G., Esch F., Coulombe J. N., Nikolics K., Eckenstein F. P., Nishi R. Cloning, expression during development, and evidence for release of a trophic factor for ciliary ganglion neurons. Neuron. 1992 Jun;8(6):1045–1053. doi: 10.1016/0896-6273(92)90126-x. [DOI] [PubMed] [Google Scholar]
  19. Lin L. F., Mismer D., Lile J. D., Armes L. G., Butler E. T., 3rd, Vannice J. L., Collins F. Purification, cloning, and expression of ciliary neurotrophic factor (CNTF). Science. 1989 Nov 24;246(4933):1023–1025. doi: 10.1126/science.2587985. [DOI] [PubMed] [Google Scholar]
  20. Lord K. A., Abdollahi A., Thomas S. M., DeMarco M., Brugge J. S., Hoffman-Liebermann B., Liebermann D. A. Leukemia inhibitory factor and interleukin-6 trigger the same immediate early response, including tyrosine phosphorylation, upon induction of myeloid leukemia differentiation. Mol Cell Biol. 1991 Sep;11(9):4371–4379. doi: 10.1128/mcb.11.9.4371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Martinou J. C., Martinou I., Kato A. C. Cholinergic differentiation factor (CDF/LIF) promotes survival of isolated rat embryonic motoneurons in vitro. Neuron. 1992 Apr;8(4):737–744. doi: 10.1016/0896-6273(92)90094-t. [DOI] [PubMed] [Google Scholar]
  22. Massagué J. The transforming growth factor-beta family. Annu Rev Cell Biol. 1990;6:597–641. doi: 10.1146/annurev.cb.06.110190.003121. [DOI] [PubMed] [Google Scholar]
  23. Mehler M. F., Rozental R., Dougherty M., Spray D. C., Kessler J. A. Cytokine regulation of neuronal differentiation of hippocampal progenitor cells. Nature. 1993 Mar 4;362(6415):62–65. doi: 10.1038/362062a0. [DOI] [PubMed] [Google Scholar]
  24. Nawa H., Yamamori T., Le T., Patterson P. H. Generation of neuronal diversity: analogies and homologies with hematopoiesis. Cold Spring Harb Symp Quant Biol. 1990;55:247–253. doi: 10.1101/sqb.1990.055.01.027. [DOI] [PubMed] [Google Scholar]
  25. Oppenheim R. W., Prevette D., Yin Q. W., Collins F., MacDonald J. Control of embryonic motoneuron survival in vivo by ciliary neurotrophic factor. Science. 1991 Mar 29;251(5001):1616–1618. doi: 10.1126/science.2011743. [DOI] [PubMed] [Google Scholar]
  26. Patterson P. H., Chun L. L. The induction of acetylcholine synthesis in primary cultures of dissociated rat sympathetic neurons. I. Effects of conditioned medium. Dev Biol. 1977 Apr;56(2):263–280. doi: 10.1016/0012-1606(77)90269-x. [DOI] [PubMed] [Google Scholar]
  27. Patterson P. H. The emerging neuropoietic cytokine family: first CDF/LIF, CNTF and IL-6; next ONC, MGF, GCSF? Curr Opin Neurobiol. 1992 Feb;2(1):94–97. doi: 10.1016/0959-4388(92)90169-l. [DOI] [PubMed] [Google Scholar]
  28. Rao M. S., Patterson P. H., Landis S. C. Multiple cholinergic differentiation factors are present in footpad extracts: comparison with known cholinergic factors. Development. 1992 Nov;116(3):731–744. doi: 10.1242/dev.116.3.731. [DOI] [PubMed] [Google Scholar]
  29. Rao M. S., Symes A., Malik N., Shoyab M., Fink J. S., Landis S. C. Oncostatin M regulates VIP expression in a human neuroblastoma cell line. Neuroreport. 1992 Oct;3(10):865–868. doi: 10.1097/00001756-199210000-00011. [DOI] [PubMed] [Google Scholar]
  30. Rao M. S., Tyrrell S., Landis S. C., Patterson P. H. Effects of ciliary neurotrophic factor (CNTF) and depolarization on neuropeptide expression in cultured sympathetic neurons. Dev Biol. 1992 Apr;150(2):281–293. doi: 10.1016/0012-1606(92)90242-9. [DOI] [PubMed] [Google Scholar]
  31. Richards C. D., Brown T. J., Shoyab M., Baumann H., Gauldie J. Recombinant oncostatin M stimulates the production of acute phase proteins in HepG2 cells and rat primary hepatocytes in vitro. J Immunol. 1992 Mar 15;148(6):1731–1736. [PubMed] [Google Scholar]
  32. Rohrer H. Cholinergic neuronal differentiation factors: evidence for the presence of both CNTF-like and non-CNTF-like factors in developing rat footpad. Development. 1992 Mar;114(3):689–698. doi: 10.1242/dev.114.3.689. [DOI] [PubMed] [Google Scholar]
  33. Rose T. M., Bruce A. G. Oncostatin M is a member of a cytokine family that includes leukemia-inhibitory factor, granulocyte colony-stimulating factor, and interleukin 6. Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8641–8645. doi: 10.1073/pnas.88.19.8641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Saadat S., Sendtner M., Rohrer H. Ciliary neurotrophic factor induces cholinergic differentiation of rat sympathetic neurons in culture. J Cell Biol. 1989 May;108(5):1807–1816. doi: 10.1083/jcb.108.5.1807. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Sendtner M., Stöckli K. A., Thoenen H. Synthesis and localization of ciliary neurotrophic factor in the sciatic nerve of the adult rat after lesion and during regeneration. J Cell Biol. 1992 Jul;118(1):139–148. doi: 10.1083/jcb.118.1.139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Shadiack A. M., Hart R. P., Carlson C. D., Jonakait G. M. Interleukin-1 induces substance P in sympathetic ganglia through the induction of leukemia inhibitory factor (LIF). J Neurosci. 1993 Jun;13(6):2601–2609. doi: 10.1523/JNEUROSCI.13-06-02601.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Smith J., Vyas S., Garcia-Arraras J. E. Selective modulation of cholinergic properties in cultures of avian embryonic sympathetic ganglia. J Neurosci Res. 1993 Feb 15;34(3):346–356. doi: 10.1002/jnr.490340312. [DOI] [PubMed] [Google Scholar]
  38. Stöckli K. A., Lottspeich F., Sendtner M., Masiakowski P., Carroll P., Götz R., Lindholm D., Thoenen H. Molecular cloning, expression and regional distribution of rat ciliary neurotrophic factor. Nature. 1989 Dec 21;342(6252):920–923. doi: 10.1038/342920a0. [DOI] [PubMed] [Google Scholar]
  39. Wetzler M., Talpaz M., Lowe D. G., Baiocchi G., Gutterman J. U., Kurzrock R. Constitutive expression of leukemia inhibitory factor RNA by human bone marrow stromal cells and modulation by IL-1, TNF-alpha, and TGF-beta. Exp Hematol. 1991 Jun;19(5):347–351. [PubMed] [Google Scholar]
  40. Wolinsky E. J., Landis S. C., Patterson P. H. Expression of noradrenergic and cholinergic traits by sympathetic neurons cultured without serum. J Neurosci. 1985 Jun;5(6):1497–1508. doi: 10.1523/JNEUROSCI.05-06-01497.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Yamamori T., Fukada K., Aebersold R., Korsching S., Fann M. J., Patterson P. H. The cholinergic neuronal differentiation factor from heart cells is identical to leukemia inhibitory factor. Science. 1989 Dec 15;246(4936):1412–1416. doi: 10.1126/science.2512641. [DOI] [PubMed] [Google Scholar]
  42. Yang Y. C., Yin T. Interleukin-11 and its receptor. Biofactors. 1992 Dec;4(1):15–21. [PubMed] [Google Scholar]
  43. Zurn A. Fibroblast growth factor differentially modulates the neurotransmitter phenotype of cultured sympathetic neurons. J Neurosci. 1992 Nov;12(11):4195–4201. doi: 10.1523/JNEUROSCI.12-11-04195.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]