Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1987 May;84(9):3060–3063. doi: 10.1073/pnas.84.9.3060

Developmentally regulated expression of the nerve growth factor receptor gene in the periphery and brain.

C R Buck, H J Martinez, I B Black, M V Chao
PMCID: PMC304802  PMID: 3033677

Abstract

Nerve growth factor (NGF) regulates development and maintenance of function of peripheral sympathetic and sensory neurons. A potential role for the trophic factor in brain has been detected only recently. The ability of a cell to respond to NGF is due, in part, to expression of specific receptors on the cell surface. To study tissue-specific expression of the NGF receptor gene, we have used sensitive cRNA probes for detection of NGF receptor mRNA. Our studies indicate that the receptor gene is selectively and specifically expressed in sympathetic (superior cervical) and sensory (dorsal root) ganglia in the periphery, and by the septum-basal forebrain centrally, in the neonatal rat in vivo. Moreover, examination of tissues from neonatal and adult rats reveals a marked reduction in steady-state NGF receptor mRNA levels in sensory ganglia. In contrast, a 2- to 4-fold increase was observed in the basal forebrain and in the sympathetic ganglia over the same time period. Our observations suggest that NGF receptor mRNA expression is developmentally regulated in specific areas of the nervous system in a differential fashion.

Full text

PDF
3060

Images in this article

3061Image
on p.3061
3061Image
on p.3061
3061Image
on p.3061
3062Image
on p.3062
3062Image
on p.3062

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aviv H., Leder P. Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc Natl Acad Sci U S A. 1972 Jun;69(6):1408–1412. doi: 10.1073/pnas.69.6.1408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Black I. B. Regulation of autonomic development. Annu Rev Neurosci. 1978;1:183–214. doi: 10.1146/annurev.ne.01.030178.001151. [DOI] [PubMed] [Google Scholar]
  3. Chao M. V., Bothwell M. A., Ross A. H., Koprowski H., Lanahan A. A., Buck C. R., Sehgal A. Gene transfer and molecular cloning of the human NGF receptor. Science. 1986 Apr 25;232(4749):518–521. doi: 10.1126/science.3008331. [DOI] [PubMed] [Google Scholar]
  4. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  5. Cox K. H., DeLeon D. V., Angerer L. M., Angerer R. C. Detection of mrnas in sea urchin embryos by in situ hybridization using asymmetric RNA probes. Dev Biol. 1984 Feb;101(2):485–502. doi: 10.1016/0012-1606(84)90162-3. [DOI] [PubMed] [Google Scholar]
  6. Frazier W. A., Boyd L. F., Szutowicz A., Pulliam M. W., Bradshaw R. A. Specific binding sites for 125I-nerve growth factor in peripheral tissues and brain. Biochem Biophys Res Commun. 1974 Apr 23;57(4):1096–1103. doi: 10.1016/0006-291x(74)90809-2. [DOI] [PubMed] [Google Scholar]
  7. Gnahn H., Hefti F., Heumann R., Schwab M. E., Thoenen H. NGF-mediated increase of choline acetyltransferase (ChAT) in the neonatal rat forebrain: evidence for a physiological role of NGF in the brain? Brain Res. 1983 Jul;285(1):45–52. doi: 10.1016/0165-3806(83)90107-4. [DOI] [PubMed] [Google Scholar]
  8. Green S. H., Greene L. A. A single Mr approximately 103,000 125I-beta-nerve growth factor-affinity-labeled species represents both the low and high affinity forms of the nerve growth factor receptor. J Biol Chem. 1986 Nov 15;261(32):15316–15326. [PubMed] [Google Scholar]
  9. Hefti F., Dravid A., Hartikka J. Chronic intraventricular injections of nerve growth factor elevate hippocampal choline acetyltransferase activity in adult rats with partial septo-hippocampal lesions. Brain Res. 1984 Feb 20;293(2):305–311. doi: 10.1016/0006-8993(84)91237-x. [DOI] [PubMed] [Google Scholar]
  10. Hefti F., Hartikka J., Eckenstein F., Gnahn H., Heumann R., Schwab M. Nerve growth factor increases choline acetyltransferase but not survival or fiber outgrowth of cultured fetal septal cholinergic neurons. Neuroscience. 1985 Jan;14(1):55–68. doi: 10.1016/0306-4522(85)90163-0. [DOI] [PubMed] [Google Scholar]
  11. Herrup K., Shooter E. M. Properties of the beta-nerve growth factor receptor in development. J Cell Biol. 1975 Oct;67(1):118–125. doi: 10.1083/jcb.67.1.118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Honegger P., Lenoir D. Nerve growth factor (NGF) stimulation of cholinergic telencephalic neurons in aggregating cell cultures. Brain Res. 1982 Feb;255(2):229–238. doi: 10.1016/0165-3806(82)90023-2. [DOI] [PubMed] [Google Scholar]
  13. Hosang M., Shooter E. M. Molecular characteristics of nerve growth factor receptors on PC12 cells. J Biol Chem. 1985 Jan 10;260(1):655–662. [PubMed] [Google Scholar]
  14. Huebner K., Isobe M., Chao M., Bothwell M., Ross A. H., Finan J., Hoxie J. A., Sehgal A., Buck C. R., Lanahan A. The nerve growth factor receptor gene is at human chromosome region 17q12-17q22, distal to the chromosome 17 breakpoint in acute leukemias. Proc Natl Acad Sci U S A. 1986 Mar;83(5):1403–1407. doi: 10.1073/pnas.83.5.1403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Johnson D., Lanahan A., Buck C. R., Sehgal A., Morgan C., Mercer E., Bothwell M., Chao M. Expression and structure of the human NGF receptor. Cell. 1986 Nov 21;47(4):545–554. doi: 10.1016/0092-8674(86)90619-7. [DOI] [PubMed] [Google Scholar]
  16. Korsching S., Auburger G., Heumann R., Scott J., Thoenen H. Levels of nerve growth factor and its mRNA in the central nervous system of the rat correlate with cholinergic innervation. EMBO J. 1985 Jun;4(6):1389–1393. doi: 10.1002/j.1460-2075.1985.tb03791.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Landreth G. E., Shooter E. M. Nerve growth factor receptors on PC12 cells: ligand-induced conversion from low- to high-affinity states. Proc Natl Acad Sci U S A. 1980 Aug;77(8):4751–4755. doi: 10.1073/pnas.77.8.4751. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Large T. H., Bodary S. C., Clegg D. O., Weskamp G., Otten U., Reichardt L. F. Nerve growth factor gene expression in the developing rat brain. Science. 1986 Oct 17;234(4774):352–355. doi: 10.1126/science.3764415. [DOI] [PubMed] [Google Scholar]
  19. Marano N., Dietzschold B., Earley J. J., Jr, Schatteman G., Thompson S., Grob P., Ross A. H., Bothwell M., Atkinson B. F., Koprowski H. Purification and amino terminal sequencing of human melanoma nerve growth factor receptor. J Neurochem. 1987 Jan;48(1):225–232. doi: 10.1111/j.1471-4159.1987.tb13151.x. [DOI] [PubMed] [Google Scholar]
  20. Martínez H. J., Dreyfus C. F., Jonakait G. M., Black I. B. Nerve growth factor promotes cholinergic development in brain striatal cultures. Proc Natl Acad Sci U S A. 1985 Nov;82(22):7777–7781. doi: 10.1073/pnas.82.22.7777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Massague J., Guillette B. J., Czech M. P., Morgan C. J., Bradshaw R. A. Identification of a nerve growth factor receptor protein in sympathetic ganglia membranes by affinity labeling. J Biol Chem. 1981 Sep 25;256(18):9419–9424. [PubMed] [Google Scholar]
  22. Melton D. A., Krieg P. A., Rebagliati M. R., Maniatis T., Zinn K., Green M. R. Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Res. 1984 Sep 25;12(18):7035–7056. doi: 10.1093/nar/12.18.7035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mobley W. C., Rutkowski J. L., Tennekoon G. I., Buchanan K., Johnston M. V. Choline acetyltransferase activity in striatum of neonatal rats increased by nerve growth factor. Science. 1985 Jul 19;229(4710):284–287. doi: 10.1126/science.2861660. [DOI] [PubMed] [Google Scholar]
  24. Naujoks K. W., Korsching S., Rohrer H., Thoenen H. Nerve growth factor-mediated induction of tyrosine hydroxylase and of neurite outgrowth in cultures of bovine adrenal chromaffin cells: dependence on developmental stage. Dev Biol. 1982 Aug;92(2):365–379. doi: 10.1016/0012-1606(82)90182-8. [DOI] [PubMed] [Google Scholar]
  25. Puma P., Buxser S. E., Watson L., Kelleher D. J., Johnson G. L. Purification of the receptor for nerve growth factor from A875 melanoma cells by affinity chromatography. J Biol Chem. 1983 Mar 10;258(5):3370–3375. [PubMed] [Google Scholar]
  26. Rohrer H., Barde Y. A. Presence and disappearance of nerve growth factor receptors on sensory neurons in culture. Dev Biol. 1982 Feb;89(2):309–315. doi: 10.1016/0012-1606(82)90320-7. [DOI] [PubMed] [Google Scholar]
  27. Ross A. H., Grob P., Bothwell M., Elder D. E., Ernst C. S., Marano N., Ghrist B. F., Slemp C. C., Herlyn M., Atkinson B. Characterization of nerve growth factor receptor in neural crest tumors using monoclonal antibodies. Proc Natl Acad Sci U S A. 1984 Nov;81(21):6681–6685. doi: 10.1073/pnas.81.21.6681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Schechter A. L., Bothwell M. A. Nerve growth factor receptors on PC12 cells: evidence for two receptor classes with differing cytoskeletal association. Cell. 1981 Jun;24(3):867–874. doi: 10.1016/0092-8674(81)90112-4. [DOI] [PubMed] [Google Scholar]
  29. Seiler M., Schwab M. E. Specific retrograde transport of nerve growth factor (NGF) from neocortex to nucleus basalis in the rat. Brain Res. 1984 May 21;300(1):33–39. doi: 10.1016/0006-8993(84)91338-6. [DOI] [PubMed] [Google Scholar]
  30. Shelton D. L., Reichardt L. F. Expression of the beta-nerve growth factor gene correlates with the density of sympathetic innervation in effector organs. Proc Natl Acad Sci U S A. 1984 Dec;81(24):7951–7955. doi: 10.1073/pnas.81.24.7951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Shelton D. L., Reichardt L. F. Studies on the expression of the beta nerve growth factor (NGF) gene in the central nervous system: level and regional distribution of NGF mRNA suggest that NGF functions as a trophic factor for several distinct populations of neurons. Proc Natl Acad Sci U S A. 1986 Apr;83(8):2714–2718. doi: 10.1073/pnas.83.8.2714. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sutter A., Riopelle R. J., Harris-Warrick R. M., Shooter E. M. Nerve growth factor receptors. Characterization of two distinct classes of binding sites on chick embryo sensory ganglia cells. J Biol Chem. 1979 Jul 10;254(13):5972–5982. [PubMed] [Google Scholar]
  33. Taniuchi M., Schweitzer J. B., Johnson E. M., Jr Nerve growth factor receptor molecules in rat brain. Proc Natl Acad Sci U S A. 1986 Mar;83(6):1950–1954. doi: 10.1073/pnas.83.6.1950. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Thoenen H., Barde Y. A. Physiology of nerve growth factor. Physiol Rev. 1980 Oct;60(4):1284–1335. doi: 10.1152/physrev.1980.60.4.1284. [DOI] [PubMed] [Google Scholar]
  35. Whittemore S. R., Ebendal T., Lärkfors L., Olson L., Seiger A., Strömberg I., Persson H. Development and regional expression of beta nerve growth factor messenger RNA and protein in the rat central nervous system. Proc Natl Acad Sci U S A. 1986 Feb;83(3):817–821. doi: 10.1073/pnas.83.3.817. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Zuker C. S., Cowman A. F., Rubin G. M. Isolation and structure of a rhodopsin gene from D. melanogaster. Cell. 1985 Apr;40(4):851–858. doi: 10.1016/0092-8674(85)90344-7. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES