Abstract
We have shown that plasma membranes from lymphoid cells have inhibitory activity for the growth of normal lymphocytes and lymphoid tumor cells (Stallcup, K. C., A. Dawson, and M. F. Mescher, J. Cell Biol. 99:1221- 1226). This growth-inhibitory activity has been found to co-purify with major histocompatibility complex class I antigens (H-2K and D) when these cell surface glycoproteins are isolated from detergent lysates of cells by affinity chromatography on monoclonal antibody columns. When incorporated into liposomes, the affinity-purified H-2 antigens inhibited the growth of both normal lymphocytes and tumor cells at concentrations of 1-3 micrograms/ml. Inhibition was readily reversed upon removal of the liposomes from the cell cultures, even after several days of exposure of cells to the inhibitor. Inhibitory activity was insensitive to protease digestion or heat treatment, indicating that it was not due to the H-2 glycoproteins. This was confirmed by the demonstration that inhibitory activity could be separated from the H-2 protein by gel filtration in the presence of deoxycholate and could be extracted from membranes or H-2 antigen preparations with organic solvents. The results demonstrate that the growth-inhibitory component(s) of the plasma membrane is a minor lipid or lipid-like molecule which retains activity in the absence of other membrane components. The findings reported here and in the preceding article suggest that this novel membrane component may have a role in control of lymphoid cell growth, possibly mediated by cell contacts.
Full Text
The Full Text of this article is available as a PDF (1.2 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- AMES B. N., DUBIN D. T. The role of polyamines in the neutralization of bacteriophage deoxyribonucleic acid. J Biol Chem. 1960 Mar;235:769–775. [PubMed] [Google Scholar]
- Frazier W., Glaser L. Surface components and cell recognition. Annu Rev Biochem. 1979;48:491–523. doi: 10.1146/annurev.bi.48.070179.002423. [DOI] [PubMed] [Google Scholar]
- Germain R. N., Mayer S. V., Mescher M. F. Role of I-region gene products in T cell activation. I. Stimulation of T lymphocyte proliferative responses by subcellular membrane preparations containing Ia alloantigens. J Immunol. 1982 Jan;128(1):506–511. [PubMed] [Google Scholar]
- Hakomori S. Glycosphingolipids in cellular interaction, differentiation, and oncogenesis. Annu Rev Biochem. 1981;50:733–764. doi: 10.1146/annurev.bi.50.070181.003505. [DOI] [PubMed] [Google Scholar]
- Harel L., Jullien M., de Monti M. Diffusible factor(s) controlling density inhibition of 3T3 cell growth: a new approach. J Cell Physiol. 1978 Sep;96(3):327–332. doi: 10.1002/jcp.1040960308. [DOI] [PubMed] [Google Scholar]
- Henning R., Milner R. J., Reske K., Cunningham B. A., Edelman G. M. Subunit structure, cell surface orientation, and partial amino-acid sequences of murine histocompatibility antigens. Proc Natl Acad Sci U S A. 1976 Jan;73(1):118–122. doi: 10.1073/pnas.73.1.118. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Herrmann S. H., Chow C. M., Mescher M. F. Proteolytic modifications of the carboxyl-terminal region of H-2Kk. J Biol Chem. 1982 Dec 10;257(23):14181–14186. [PubMed] [Google Scholar]
- Herrmann S. H., Mescher M. F. Purification of the H-2Kk molecule of the murine major histocompatibility complex. J Biol Chem. 1979 Sep 25;254(18):8713–8716. [PubMed] [Google Scholar]
- Herrmann S. H., Mescher M. F. Secondary cytolytic T lymphocyte stimulation by purified H-2Kk in liposomes. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2488–2492. doi: 10.1073/pnas.78.4.2488. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Herrmann S. H., Weinberger O., Burakoff S. J., Mescher M. F. Analysis of the two-signal requirement for precursor cytolytic T lymphocyte activation using H-2Kk in liposomes. J Immunol. 1982 May;128(5):1968–1974. [PubMed] [Google Scholar]
- Holley R. W., Kiernan J. A. "Contact inhibition" of cell division in 3T3 cells. Proc Natl Acad Sci U S A. 1968 May;60(1):300–304. doi: 10.1073/pnas.60.1.300. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hyman R., Trowbridge I. Analysis of lymphocyte surface antigen expression by the use of variant cell lines. Cold Spring Harb Symp Quant Biol. 1977;41(Pt 1):407–415. doi: 10.1101/sqb.1977.041.01.049. [DOI] [PubMed] [Google Scholar]
- LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
- Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
- Lemonnier F., Mescher T. M., sherman L., Burakoff S. The induction of cytolytic T lymphocytes with purified plasma membranes. J Immunol. 1978 Apr;120(4):1114–1120. [PubMed] [Google Scholar]
- Lerner R. A., Hodge L. D. Gene expression in synchronized lymphocytes: studies on the control of synthesis of immunoglobulin polypeptides. J Cell Physiol. 1971 Apr;77(2):265–276. doi: 10.1002/jcp.1040770215. [DOI] [PubMed] [Google Scholar]
- Mescher M. F., Balk S. P., Burakoff S. J., Herrmann S. H. Cytolytic T lymphocyte recognition of subcellular antigen. Adv Exp Med Biol. 1982;146:41–55. doi: 10.1007/978-1-4684-8959-0_3. [DOI] [PubMed] [Google Scholar]
- Mescher M. F., Jose M. J., Balk S. P. Actin-containing matrix associated with the plasma membrane of murine tumour and lymphoid cells. Nature. 1981 Jan 15;289(5794):139–144. doi: 10.1038/289139a0. [DOI] [PubMed] [Google Scholar]
- Mescher M. F., Stallcup K. C., Sullivan C. P., Turkewitz A. P., Herrmann S. H. Purification of murine MHC antigens by monoclonal antibody affinity chromatography. Methods Enzymol. 1983;92:86–109. doi: 10.1016/0076-6879(83)92011-6. [DOI] [PubMed] [Google Scholar]
- Oi V. T., Jones P. P., Goding J. W., Herzenberg L. A., Herzenberg L. A. Properties of monoclonal antibodies to mouse Ig allotypes, H-2, and Ia antigens. Curr Top Microbiol Immunol. 1978;81:115–120. doi: 10.1007/978-3-642-67448-8_18. [DOI] [PubMed] [Google Scholar]
- Peterson S. W., Lerch V. Inhibition of DNA synthesis in SV3T3 cultures by isolated 3T3 plasma membranes. J Cell Biol. 1983 Jul;97(1):276–279. doi: 10.1083/jcb.97.1.276. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Peterson S. W., Lerch V., Moynahan M. E., Carson M. P., Vale R. Partial characterization of a growth-inhibiting protein in 3T3 cell plasma membranes. Exp Cell Res. 1982 Dec;142(2):447–451. doi: 10.1016/0014-4827(82)90386-x. [DOI] [PubMed] [Google Scholar]
- Raben D., Lieberman M. A., Glaser L. Growth inhibitory protein(s) in the 3T3 cell plasma membrane. Partial purification and dissociation of growth inhibitory events from inhibition of amino acid transport. J Cell Physiol. 1981 Jul;108(1):35–45. doi: 10.1002/jcp.1041080106. [DOI] [PubMed] [Google Scholar]
- Stallcup K. C., Dawson A., Mescher M. F. Growth-inhibitory activity of lymphoid cell plasma membranes. I. Inhibition of lymphocyte and lymphoid tumor cell growth. J Cell Biol. 1984 Oct;99(4 Pt 1):1221–1226. doi: 10.1083/jcb.99.4.1221. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stallcup K. C., Springer T. A., Mescher M. F. Characterization of an anti-H-2 monoclonal antibody and its use in large-scale antigen purification. J Immunol. 1981 Sep;127(3):923–930. [PubMed] [Google Scholar]
- Steck P. A., Blenis J., Voss P. G., Wang J. L. Growth control in cultured 3T3 fibroblasts II. Molecular properties of a fraction enriched in growth inhibitory activity. J Cell Biol. 1982 Feb;92(2):523–530. doi: 10.1083/jcb.92.2.523. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Steck P. A., Voss P. G., Wang J. L. Growth control in cultured 3T3 fibroblasts. Assays of cell proliferation and demonstration of a growth inhibitory activity. J Cell Biol. 1979 Dec;83(3):562–575. doi: 10.1083/jcb.83.3.562. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stoker M. G. Role of diffusion boundary layer in contact inhibition of growth. Nature. 1973 Nov 23;246(5430):200–203. doi: 10.1038/246200a0. [DOI] [PubMed] [Google Scholar]
- TODARO G. J., GREEN H., GOLDBERG B. D. TRANSFORMATION OF PROPERTIES OF AN ESTABLISHED CELL LINE BY SV40 AND POLYOMA VIRUS. Proc Natl Acad Sci U S A. 1964 Jan;51:66–73. doi: 10.1073/pnas.51.1.66. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Todaro G. J., Lazar G. K., Green H. The initiation of cell division in a contact-inhibited mammalian cell line. J Cell Physiol. 1965 Dec;66(3):325–333. doi: 10.1002/jcp.1030660310. [DOI] [PubMed] [Google Scholar]
- Whittenberger B., Glaser L. Inhibition of DNA synthesis in cultures of 3T3 cells by isolated surface membranes. Proc Natl Acad Sci U S A. 1977 Jun;74(6):2251–2255. doi: 10.1073/pnas.74.6.2251. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Whittenberger B., Raben D., Lieberman M. A., Glaser L. Inhibition of growth of 3T3 cells by extract of surface membranes. Proc Natl Acad Sci U S A. 1978 Nov;75(11):5457–5461. doi: 10.1073/pnas.75.11.5457. [DOI] [PMC free article] [PubMed] [Google Scholar]