Skip to main content
SpringerLink
Log in

Evidence for a lack of functional receptors for nerve growth factor (NGF) in chick bone cells in vitro

  • Published:
Molecular and Cellular Biochemistry Aims and scope Submit manuscript

Abstract

Nerve growth factor (NGF) is essential for the development and differentiation of sympathetic and sensory neurons. Recently, NGF receptors were demonstrated in non-neural cells, and several mesenchymal cell types including lymphocytes and skeletal myotubes were shown to be stimulated to proliferate by NGF. Our purpose was to examine for the presence of functional NGF receptors in osteoblasts. Bone cells from chick calvaria were used as a model; PC-12 cells derived from rat adrenal pheochromocytoma were used as positive controls. NGF was examined for functions in chick bone cells by studying effects on (1) [3H]-thymidine incorporation; (2) alkaline phosphatase (ALP) activity; and (3) protein tyrosine phosphorylation. Effects of NGF on thymidine incorporation and protein tyrosine phosphorylation by PC-12 cells were also measured. A radioreceptor assay was used to test for the presence of receptors. In chick calvarial cells, NGF had no effect on thymidine incorporation, ALP activity or protein tyrosine phosphorylation. Radioreceptor assay with bone cells showed no evidence of NGF receptors. In contrast, in PC-12 cells, NGF (1) decreased thymidine incorporation; (2) increased protein tyrosine phosphorylation; and (3) showed receptor activity by radioreceptor assay. In conclusion, unlike several other mesenchymal cell types, chick bone cells show no evidence of NGF receptors or functional responses to NGF in vitro.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Calissano P, Cattaneo A, Aloe L, Levi-Montalcini R: The nerve growth factor (NGF). In: HL Choh (ed.) Hormonal Proteins and Peptides, Vol XII. Academic Press, Orlando, 1984, pp. 1–56

    Google Scholar 

  2. Levi-Montalcini R: The nerve growth factor 35 years later. Science 237: 1154–1162, 1987

    CAS  PubMed  Google Scholar 

  3. Schubert D, LaCorbiere M, Whitlock C, Stallcup W: Alterations in the surface properties of cells responsive to nerve growth factor. Nature 273: 718–723, 1978

    Google Scholar 

  4. Whittemore SR, Seiger A: The expression, localization and functional significance of beta-nerve growth factor in the central nervous system. Brain Res 434: 439–464, 1987

    Google Scholar 

  5. Mobley WC, Woo JE, Edwards RH, Riopelle RJ, Longo FM, Weskamp G, Otten U, Valletta JS, Johnston MV: Developmental regulation of nerve growth factor and its receptor in the rat caudate-putamen. Neuron 3: 655–664, 1989

    Google Scholar 

  6. Greene LA, Tischler AS; Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci USA 73: 2424–2428, 1976

    Google Scholar 

  7. Cho K-O, Minsk B, Wagner JA: NICER elements: A family of nerve growth factor-inducible cAMP-extinguishable retrovirus-like elements. Proc Natl Acad Sci USA 87: 3778–3782, 1990

    Google Scholar 

  8. Thomson TM, Rettig WJ, Chesa PG, Green SH, Mena AC, Old LJ: Expression of human nerve growth factor receptor on cells derived from all three germ layers. Exp Cell Res 174: 533–539, 1988

    Google Scholar 

  9. Otten U, Ehrhard P, Peck R: Nerve growth factor induces growth and differentiation of human B lymphocytes. Proc Natl Acad Sci USA 86: 10059–10063, 1989

    Google Scholar 

  10. Brodie C, Sampson SR: Nerve growth factor supports growth of rat skeletal myotubes in culture. Brain Res 435: 393–397, 1987

    Google Scholar 

  11. Ebendal T, Olson L, Seiger Å, Hedlund K-O: Nerve growth factors in the rat iris. Nature 286: 25–28, 1980

    Google Scholar 

  12. Harper GP, Barde YA, Burnstock G, Carstairs JR, Dennison ME, Suda K, Vernon CA: Guinea pig prostate is a rich source of nerve growth factor. Nature 279: 160–162, 1979

    Google Scholar 

  13. Singh IJ, Klein RM, Herskovits M: Autoradiographic assessment of 3H-proline uptake by osteoblasts following guanethidine-induced sympathectomy in the rat. Cell Tissue Res 216: 215–220, 1981

    Google Scholar 

  14. Herskovits MS, Singh IJ: Effect of guanethidine-induced sympathectomy on osteoblastic activity in the rat femur evaluated by 3H-proline autoradiography. Acta Anat 120: 151–155, 1984

    CAS  Google Scholar 

  15. Singh IJ, Herskovits MS, Chiego DJ, Klein RM: Modulation of osteoblastic activity by sensory and autonomic innervation of bone. In: A Dixon, B. Sarnat (eds) Factors and Mechanisms Influencing Bone Growth. Alan R Liss, New York, 1982, pp.535–551.

    Google Scholar 

  16. Sandhu HS, Herskovits MS, Singh IJ: Effect of surgical sympathectomy on bone remodeling at rat incisor and molar root sockets. Anat Rec 219: 32–38, 1987

    Google Scholar 

  17. Frenkel SR, Guerra LA, Mitchell OG, Singh IJ: Nerve growth factor in skeletal tissues of the embryonic chick. Cell Tissue Res 260: 507–511, 1990

    Google Scholar 

  18. Levi-Montalcini R: Effects of mouse tumor transplantation on the nervous system. Ann NY Acad Sci 55: 330–343, 1952

    Google Scholar 

  19. Levi-Montalcini R, Mayer H, Hamburger V: In vitro experiments on the effects of mouse sarcomas 180 and 37 on the spinal and sympathetic ganglia of the chick embryo. Cancer Res 14: 49–57, 1954

    Google Scholar 

  20. Mohan S, Jennings JC, Linkhart TA, Baylink DJ: Primary structure of human skeletal growth factor: homology with human insulin-like growth factor II. Biochim Biophys Acta 966: 44–55, 1988

    Google Scholar 

  21. Drivdahl RH, Puzas JE, Howard GA, Baylink DJ: Regulation of DNA synthesis in chick calvaria cells by factors from bone organ culture. Proc Soc Exp Biol Med 168: 143–150, 1981

    Google Scholar 

  22. Puzas JE, Drivdahl RH, Howard GA, Baylink DJ: Endogenous inhibitor of bone cell proliferation. Proc Soc Exp Biol Med 166: 113–122, 1981

    Google Scholar 

  23. Farley JR, Baylink DJ: Skeletal alkaline phosphatase activity as a bone formation index in vitro. Metabolism 35: 563–571, 1986

    Google Scholar 

  24. Lau K-HW, Jennings JC, Baylink DJ: Bovine skeletal growth factor stimulates protein phosphorylation of chicken bone cells in vitro. Int J Biochem 20: 1443–1450, 1988

    Google Scholar 

  25. Bradford MM: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248–254, 1976

    Article  CAS  PubMed  Google Scholar 

  26. Kasuga M, Zick Y, Blithe DL, Crettaz M, Kahn CR: Insulin stimulates tyrosine phosphorylation of the insulin receptor in a cell free system. Nature 298: 667–669, 1982

    Google Scholar 

  27. Persson H, Lievre CA-L, Söder O, Villar MJ, Metsis M, Olson L, Ritzen M, Hökfelt T: Expression of β-nerve growth factor receptor mRNA in Sertoli cells down-regulated by testosterone. Science 247: 704–707, 1990

    Google Scholar 

  28. Thompson SJ, Schatteman GC, Gown AM, Bothwell M: A monoclonal antibody against nerve growth factor receptor. Immunohistochemical analysis of normal and neoplastic human tissue. Am J Clin Pathol 92: 415–423, 1989

    Google Scholar 

  29. Thorpe LW, Stach RW, Hashim GA, Marchetti D, Perez-Polo JR: Receptors for nerve growth factor on rat spleen mononuclear cells. J Neurosci Res 17: 128–134, 1987

    Google Scholar 

  30. Gee AP, Boyle MDP, Munger KL, Lawman MJP, Young M: Nerve growth factor: Stimulation of polymorphonuclear leukocyte chemotaxis in vitro. Proc Natl Acad Sci USA 80: 7215–7218, 1983

    Google Scholar 

  31. Boyle MDP, Lawman MJP, Gee AP, Young M: Nerve growth factor: a chemotactic factor for polymorphonuclear leukocytes in vivo. J Immunol 134: 564–568, 1985

    Google Scholar 

  32. Thorpe LW, Perez-Polo JR: The influence of nerve growth factor on the in vitro proliferative response of rat spleen lymphocytes. J Neurosci Res 18: 134–139, 1987

    Google Scholar 

  33. Tsuda T, Switzer J, Bienenstock J, Denburg JA: Interactions of hemopoietic cytokines on differentiation of HL-60 cells. Nerve growth factor is a basophilic lineage-specific co-factor. Int Arch Allergy Appl Immunol 91: 15–21, 1990

    Google Scholar 

  34. Linkart TA, Jennings JC, Mohan S, Wakley GK, Baylink DJ: Characterization of mitogenic activities extracted from bovine bone matrix. Bone 7: 479–487, 1986

    Google Scholar 

  35. Mohan S, Linkhart T, Jennings J, Baylink D: Chemical and biological characterization of low-molecular-weight human skeletal growth factor. Biochim Biophys Acta 884: 243–250, 1986

    Google Scholar 

  36. Lau K-HW, Tanimoto H, Baylink DJ: Vanadate stimulates bone cell proliferation and bone collagen synthesis in vitro. Endocrinology 123: 2858–2867, 1988

    Google Scholar 

  37. Farley JR, Wegedal JE, Baylink DJ: Fluoride directly stimulates proliferation and alkaline phosphatase activity of bone-forming cells. Science 222: 330–332, 1983

    CAS  PubMed  Google Scholar 

  38. Maher PA: Nerve growth factor induces protein-tyrosine phosphorylation. Proc Natl Acad Sci USA 85: 6788–6791, 1988

    Google Scholar 

  39. Maher PA: Role of protein tyrosine phosphorylation in the NGF response. J Neurosci Res 24: 29–37, 1989

    Google Scholar 

  40. Miyasaka T, Sternberg DW, Miyasaka J, Sherline P, Saltiel AR: Nerve growth factor stimulates protein tyrosine phosphorylation in PC-12 pheochromocytoma cells. Proc Natl Acad Sci USA 88: 2653–2657, 1991

    Google Scholar 

  41. Dichter MA, Tischler AS, Greene LA: Nerve growth factor-induced increase in electrical excitability and acetylcholine sensitivity in a rat pheochromocytoma cell line. Nature 268: 501–504, 1977

    Google Scholar 

  42. Huff K, End D, Guroff G: Nerve growth factor-induced alteration in the response of PC12 pheochromocytoma cells to epidermal growth factor. J Cell Biol 88: 189–198, 1981

    Google Scholar 

  43. Meier R, Becker-André M, Götz R, Heumann R, Shaw A, Thoenen H: Molecular cloning of bovine and chick nerve growth factor (NGF): delineation of conserved and unconserved do mains and their relationship to the biological activity and antigenicity of NGF. EMBO J 5: 1489–1493, 1986

    Google Scholar 

  44. Selby MJ, Edwards RH, Rutter WJ: Cobra nerve growth factor: structure and evolutionary comparison. J Neurosci Res 18: 293–298, 1987

    Google Scholar 

  45. Maisonpierre PC, Belluscio L, Squinto S, Ip NY, Furth ME, Lindsay RM, Yancopoulos GD: Neurotrophin-3: A neurotrophic factor related to NGF and BDNF. Science 247: 1446–1451, 1990

    CAS  PubMed  Google Scholar 

  46. Wion D, MacGrogan D, Neveu I, Jehan F, Houlgatte R, Brachet P: 1,25-Dihydroxyvitamin D3 is a potent inducer of nerve growth factor synthesis. J Neurosci Res 28: 110–114, 1991

    Google Scholar 

  47. Matsuda H, Kannan Y, Ushio H, Kiso Y, Kanemoto T, Suzuki H, Kitamura Y: Nerve growth factor induces development of connective tissue-type mast cells in vitro from murine bone marrow cells. J Exp Med 174: 7–14, 1991

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Graduate Periodontics, Loma Linda University, Loma Linda, USA

    Richard D. Finkelman

  2. Department of Periodontics, Loma Linda University, Loma Linda, USA

    Richard D. Finkelman

  3. Department of Biochemistry, Loma Linda University, Loma Linda, USA

    Richard D. Finkelman, K. -H. William Lau & David J. Baylink

  4. Department of Pediatrics, Loma Linda University, Loma Linda, USA

    Richard D. Finkelman

  5. Department of Medicine, Loma Linda University, Loma Linda, USA

    K. -H. William Lau & David J. Baylink

  6. Jerry L. Pettis Memorial Veterans Hospital, 11201 Benton Street, 92357, Loma Linda, California, USA

    K. -H. William Lau & David J. Baylink

Authors
  1. Richard D. Finkelman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. -H. William Lau
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Susan M. Abraham
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. David J. Baylink
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Finkelman, R.D., Lau, K.H.W., Abraham, S.M. et al. Evidence for a lack of functional receptors for nerve growth factor (NGF) in chick bone cells in vitro . Mol Cell Biochem 115, 129–136 (1992). https://doi.org/10.1007/BF00230322

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00230322

Key words

Search

Navigation