Abstract
The developmental regulation of neuronal survival by vasoactive intestinal peptide (VIP) was investigated in dissociated spinal cord- dorsal root ganglion (SC-DRG) cultures. Previous studies demonstrated that VIP increased neuronal survival in SC-DRG cultures when synaptic transmission was blocked with tetrodotoxin (TTX). This effect was further investigated to determine if VIP acted directly on neurons or via nonneuronal cells. For these studies, SC-DRG cells were cultured under conditions designed to provide preparations enriched for a particular cell type: astrocyte-enriched background cell (BG) cultures, meningeal fibroblast cultures, standard mixed neuron-nonneuron (STD) cultures, and neuron-enriched (N) cultures. Addition of 0.1 nM VIP to TTX-treated STD cultures for 5 d prevented the TTX-mediated death and the death that occurred naturally during development in culture, whereas the same treatment on N cultures did not prevent neuronal cell death. Conditioned medium from VIP-stimulated BG cultures prevented neuronal cell death when added to the medium (10% of total volume) of N cultures treated with TTX. The same amount of conditioned medium from BG cultures that were not treated with VIP had no protective action on N cultures. Conditioned medium from N or meningeal fibroblast cultures, either with or without VIP treatment, did not prevent TTX-mediated cell death in N test cultures. These data indicate that VIP increases the availability of neurotrophic survival-promoting substances derived from nonneuronal cultures, the most likely source being astroglial cells. This study suggests that VIP has a role in mediating a neuron-glia- neuron interaction that influences the trophic regulation of neuronal survival.
Full Text
The Full Text of this article is available as a PDF (2.8 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Banker G. A. Trophic interactions between astroglial cells and hippocampal neurons in culture. Science. 1980 Aug 15;209(4458):809–810. doi: 10.1126/science.7403847. [DOI] [PubMed] [Google Scholar]
- Bergey G. K., Fitzgerald S. C., Schrier B. K., Nelson P. G. Neuronal maturation in mammalian cell culture is dependent on spontaneous electrical activity. Brain Res. 1981 Feb 23;207(1):49–58. doi: 10.1016/0006-8993(81)90678-8. [DOI] [PubMed] [Google Scholar]
- Brenneman D. E., Eiden L. E., Siegel R. E. Neurotrophic action of VIP on spinal cord cultures. Peptides. 1985;6 (Suppl 2):35–39. doi: 10.1016/0196-9781(85)90132-9. [DOI] [PubMed] [Google Scholar]
- Brenneman D. E., Eiden L. E. Vasoactive intestinal peptide and electrical activity influence neuronal survival. Proc Natl Acad Sci U S A. 1986 Feb;83(4):1159–1162. doi: 10.1073/pnas.83.4.1159. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brenneman D. E., Fitzgerald S., Litzinger M. J. Neuronal survival during electrical blockade is increased by 8-bromo cyclic adenosine 3',5' monophosphate. J Pharmacol Exp Ther. 1985 May;233(2):402–408. [PubMed] [Google Scholar]
- Brenneman D. E., Fitzgerald S., Nelson P. G. Interaction between trophic action and electrical activity in spinal cord cultures. Brain Res. 1984 Aug;317(2):211–217. doi: 10.1016/0165-3806(84)90098-1. [DOI] [PubMed] [Google Scholar]
- Brenneman D. E., Neale E. A., Habig W. H., Bowers L. M., Nelson P. G. Developmental and neurochemical specificity of neuronal deficits produced by electrical impulse blockade in dissociated spinal cord cultures. Brain Res. 1983 Jul;285(1):13–27. doi: 10.1016/0165-3806(83)90104-9. [DOI] [PubMed] [Google Scholar]
- Creazzo T. L., Sohal G. S. Effects of chronic injections of alpha-bungarotoxin on embryonic cell death. Exp Neurol. 1979 Oct;66(1):135–145. doi: 10.1016/0014-4886(79)90069-4. [DOI] [PubMed] [Google Scholar]
- Dahl D., Bignami A. Immunogenic properties of the glial fibrillary acidic protein. Brain Res. 1976 Oct 29;116(1):150–157. doi: 10.1016/0006-8993(76)90257-2. [DOI] [PubMed] [Google Scholar]
- Dahl D., Bignami A. Preparation of antisera to neurofilament protein from chicken brain and human sciatic nerve. J Comp Neurol. 1977 Dec 15;176(4):645–657. doi: 10.1002/cne.901760412. [DOI] [PubMed] [Google Scholar]
- Eagleson K. L., Raju T. R., Bennett M. R. Motoneurone survival is induced by immature astrocytes from developing avian spinal cord. Brain Res. 1985 Jan;349(1-2):95–104. doi: 10.1016/0165-3806(85)90135-x. [DOI] [PubMed] [Google Scholar]
- Epelbaum J., Tapia-Arancibia L., Besson J., Rotsztejn W. H., Kordon C. Vasoactive intestinal peptide inhibits release of somatostatin from hypothalamus in vitro. Eur J Pharmacol. 1979 Oct 15;58(4):493–495. doi: 10.1016/0014-2999(79)90323-6. [DOI] [PubMed] [Google Scholar]
- Evans T., McCarthy K. D., Harden T. K. Regulation of cyclic AMP accumulation by peptide hormone receptors in immunocytochemically defined astroglial cells. J Neurochem. 1984 Jul;43(1):131–138. doi: 10.1111/j.1471-4159.1984.tb06688.x. [DOI] [PubMed] [Google Scholar]
- Guillemin R., Brazeau P., Böhlen P., Esch F., Ling N., Wehrenberg W. B. Growth hormone-releasing factor from a human pancreatic tumor that caused acromegaly. Science. 1982 Nov 5;218(4572):585–587. doi: 10.1126/science.6812220. [DOI] [PubMed] [Google Scholar]
- Hsu S. M., Raine L., Fanger H. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem. 1981 Apr;29(4):577–580. doi: 10.1177/29.4.6166661. [DOI] [PubMed] [Google Scholar]
- Magistretti P. J., Manthorpe M., Bloom F. E., Varon S. Functional receptors for vasoactive intestinal polypeptide in cultured astroglia from neonatal rat brain. Regul Pept. 1983 Apr;6(1):71–80. doi: 10.1016/0167-0115(83)90136-2. [DOI] [PubMed] [Google Scholar]
- McCarthy K. D., Partlow L. M. Preparation of pure neuronal and non-neuronal cultures from embryonic chick sympathetic ganglia: a new method based on both differential cell adhesiveness and the formation of homotypic neuronal aggregates. Brain Res. 1976 Sep 24;114(3):391–414. doi: 10.1016/0006-8993(76)90962-8. [DOI] [PubMed] [Google Scholar]
- Müller H. W., Beckh S., Seifert W. Neurotrophic factor for central neurons. Proc Natl Acad Sci U S A. 1984 Feb;81(4):1248–1252. doi: 10.1073/pnas.81.4.1248. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Noble M., Fok-Seang J., Cohen J. Glia are a unique substrate for the in vitro growth of central nervous system neurons. J Neurosci. 1984 Jul;4(7):1892–1903. doi: 10.1523/JNEUROSCI.04-07-01892.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pittman R. H., Oppenheim R. W. Neuromuscular blockade increases motoneurone survival during normal cell death in the chick embryo. Nature. 1978 Jan 26;271(5643):364–366. doi: 10.1038/271364a0. [DOI] [PubMed] [Google Scholar]
- Ransom B. R., Neale E., Henkart M., Bullock P. N., Nelson P. G. Mouse spinal cord in cell culture. I. Morphology and intrinsic neuronal electrophysiologic properties. J Neurophysiol. 1977 Sep;40(5):1132–1150. doi: 10.1152/jn.1977.40.5.1132. [DOI] [PubMed] [Google Scholar]
- Ruberg M., Rotsztejn W. H., Arancibia S., Besson J., Enjalbert A. Stimulation of prolactin release by vasoactive intestinal peptide (VIP). Eur J Pharmacol. 1978 Oct 1;51(3):319–320. doi: 10.1016/0014-2999(78)90421-1. [DOI] [PubMed] [Google Scholar]
- Samson W. K., Burton K. P., Reeves J. P., McCann S. M. Vasoactive intestinal peptide stimulates luteinizing hormone-releasing hormone release from median eminence synaptosomes. Regul Pept. 1981 Aug;2(4):253–264. doi: 10.1016/0167-0115(81)90029-x. [DOI] [PubMed] [Google Scholar]
- Schmechel D., Marangos P. J., Zis A. P., Brightman M., Goodwin F. K. Brain endolases as specific markers of neuronal and glial cells. Science. 1978 Jan 20;199(4326):313–315. doi: 10.1126/science.339349. [DOI] [PubMed] [Google Scholar]
- Silver J., Lorenz S. E., Wahlsten D., Coughlin J. Axonal guidance during development of the great cerebral commissures: descriptive and experimental studies, in vivo, on the role of preformed glial pathways. J Comp Neurol. 1982 Sep 1;210(1):10–29. doi: 10.1002/cne.902100103. [DOI] [PubMed] [Google Scholar]
- Vijayan E., Samson W. K., Said S. I., McCann S. M. Vasoactive intestinal peptide: evidence for a hypothalamic site of action to release growth hormone, luteinizing hormone, and prolactin in conscious ovariectomized rats. Endocrinology. 1979 Jan;104(1):53–57. doi: 10.1210/endo-104-1-53. [DOI] [PubMed] [Google Scholar]
- Wessells N. K., Letourneau P. C., Nuttall R. P., Ludueña-Anderson M., Geiduschek J. M. Responses to cell contacts between growth cones, neurites and ganglionic non-neuronal cells. J Neurocytol. 1980 Oct;9(5):647–664. doi: 10.1007/BF01205031. [DOI] [PubMed] [Google Scholar]