human gene to a unique human chromosome. In screening a number of mouse permanent cell lines we have
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1 Proc. Nati. Acad. Sci. USA Vol. 77, No. 7, pp , July 198 Genetics Genetic analysis of epidermal growth factor action: Assignment of human epidermal growth factor receptor gene to chromosome 7 (binding assay/cell hybrids/chromosome analysis) ROBIN L. DAVIES, VIRGINIA A. GROSSE, RAjU KUCHERLAPATI, AND MARK BOTHWELL* Department of Biochemical Sciences, Princeton University, Princeton, New Jersey 8544 Communicated by Howard K. Schachman, April 4,198 ABSRA4C Purified murine epidermal growth factor (EGF) binds to mouse and human cells. Two mouse transformed cell lines of different origins, PG19 and B82, were found to lack EGF receptors (EGFR). The defect in each of these two cell lines seems to be identical because they fail to complement each other. Somatic cell hybrids between these EGFR-deficient mouse cells and human cells expressing EGFR were produced. Several of these hybrids bound labeled EGF. Detailed cytogenetic analysis of these cell hybrids followed by correlation of EGFR expression with human chromosomes revealed that EGFR presence correlated with human chromosome 7. The results suggest that the structural gene or a gene necessary for expression of the human EGF receptor is located on human chromosome 7. For the great majority of hormones, growth factors, and neurotransmitters in animal cells, biological function is mediated by specific receptor proteins localized on the plasma membrane. One of the consequences of cellular differentiation is that each differentiated cell type expresses only certain characteristic receptors and hence responds to a limited number of hormones. In recent years, considerable effort has been made to characterize various receptor proteins biochemically. As a result, the molecular properties of several receptors, including those of acetylcholine (1) and insulin (2), are known in some detail. The critical role played by plasma membrane receptors is illustrated by the involvement of insulin receptor deficiencies in some forms of diabetes (3) and of low density lipoprotein receptors in hypercholesterolemia (4). The biological activity of the mitogenic peptide epidermal growth factor (EGF) is mediated by a plasma membrane receptor (5). The mouse EGF receptor (EGFR) has been characterized by covalent attachment of a photoactivated derivative of 125I-labeled EGF (125I-EGF) and shown to be a 19,- dalton protein (6). Specific EGFRs are found on a wide variety of mammalian cells derived from different tissue and cell types (see ref. 7 for a review). Human diploid fibroblasts bind both mouse and human 125I-EGF with an apparent equilibrium constant of about 3 X 1-1 M (8, 9). Genetic approaches to probing the mechanism of action and functional role of receptor proteins should be extremely valuable but have not yet been much utilized. An important initial step in the application of a genetic approach is the determination of the chromosomal location of the structural gene for the receptor. We have used somatic cell genetic techniques to approach this problem. Fusion of mouse and human cells results in the formation of hybrids that usually retain all of the mouse complement of chromosomes and a small, random subset of human chromosomes (1). Because both the murine and human genes are usually functional (1), one can assay each hybrid The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U. S. C solely to indicate this fact. clone for the presence of a given gene product. Identification of the human chromosomes present in each hybrid clone and consideration of this information in concert with the results of the differential gene product assay allow the mapping of the human gene to a unique human chromosome. In screening a number of mouse permanent cell lines we have observed that two of them do not bind EGF. We have obtained somatic cell hybrids between these cells and human cells that do bind EGF. Analysis of the hybrids allowed us to identify a genetic element located on human chromosome 7 which plays a role in EGFR expression. MATERIALS AND METHODS Cells and Hybrids. The murine parental lines were B82 (thymidine kinase-deficient L cells) and PG19 (hypoxanthine phosphoribosyltransferase-deficient cells derived from a melanoma). Human parental lines were HT18 (derived from a fibrosarcoma) and BP (normal diploid fibroblasts). The sources and characteristics of these cell lines have been described (11). Cells were maintained in Dulbecco's modified Eagle's medium (GIBCO) supplemented with 1% fetal bovine serum (Flow, McLean, VA), penicillin and streptomycin (GIBCO), and glutamine (GIBCO). BCH hybrids resulted from the fusion of B82 and HT18 cells, and PEP hybrids resulted from the fusion of PG19 and BP- cells. The cell fusion procedure was as described (11). Briefly, a mixture of the two parental cells was treated with 5% polyethylene glycol 1 (J. T. Baker) for 1 min and washed with fresh medium. After 24 hr the cells were trypsinized, replated, and subjected to selection conditions. The selective medium contained hypoxanthine (15,g/ml)/aminopterin (1,gg/ml)/thymidine (5,qg/ml) and 1,gM ouabain. Resistant colonies appeared in 2-3 weeks. Well-separated colonies were isolated and expanded for analysis. The hybrids were maintained in the above selective medium without ouabain. PGB hybrids resulted from the fusion of PG19 and B82 cells and were prepared by R. Te-pper by the same method. Chromosome Analysis. Metaphase chromosome spreads were prepared by conventional methods and karyotyping was performed as reported (11). Purification of EGF. EGF was purified from epinephrine-elicited saliva from mature male Swiss-Webster mice. Saliva was collected and a partially purified preparation of high molecular weight EGF was prepared by a modification of the method of Burton et al. (12). Pooled saliva from 8 mice (1 ml) was centrifuged 3 min at 2, X g at 4C. The supernatant was chromatographed on a column (2.5 X 95 cm) of Sepharore S-2 (Pharmacia) equilibrated with 1 mm sodium phosphate (ph 6.8) at 4C. Abbreviations: EGF, epidermal growth factor; EGFR, epidermal growth factor receptor. * To whom reprint requests should be addressed. 4188
2 Genetics: Davies et al. Four major peaks of protein were eluted; the third consisted primarily of high molecular weight EGF, idetitifiect by- iielectric focusing on polyacrylamide gels according to the method of Server and Shooter (13). The EGF-containing peak was pooled, dialyzed for 3 hr against 5 mm sodium phosphate (ph 7.5), and iyophilized. The material was dissolved in.1 M HC (2 ml) and centrifuged (2 min, 15, X g, 4C). The supernatant was chromatographed on a column (2 X 5 cm) of Sephadex G-75 (superfine; Pharmacia) equilibrated with 5 mm HCI/5 mm NaCI at 4C. The last of three peaks of protein eluted consisted of homogeneous low molecular weight EGF (6.5 mg). lodination. Todination of EGF with Na 125I (Amersham) was performed by using the chloramine-t method as described by Carpenter and Cohen (9). 125I-EGF Binding Assay. Measurement of binding of 125I-EGF was performed by using a modification of the method of Carpenter and Cohen (9). Cells to be assayed were plated in 35-mm culture dishes and were used at confluence. The culture medium was removed from five plates of each cell type and the plates were incubated for 4 min with.6 ml of one of three buffered solutions as follows: one plate received bovine serum albumin (1 mg/ml) in Dulbecco's phosphate-buffered saline with calcium and magnesium (binding buffer); two plates received l25-ilabeled EGF (5 ng/ml) in binding buffer; and two plates received 125I-EGF (5 ng/ml) in binding buffer supplemented with unlabeled EGF (1 Ag/ml). After incubation, 6,ul aliquots of the supernatant buffer were collected for measurement of radioactivity. The cells were then washed four times with 1-ml aliquots of bovine serum albumin (.5 mg/ml) in phosphate-buffered saline. The unlabeled plate (binding buffer alone) then received.6 ml of pancreatin (GIBCO) to remove the cells for counting in a hemocytometer. The four labeled plates received.5 ml of 1 M NaOH and the cell layers were collected on cotton swabs which were then placed into tubes for measurement of radioactivity. Supernatant and cell samples were assayed in an Intertechnique (CG 4) gamma counter. RESULTS EGF Receptors in Mouse and Human Cells. An important prerequisite for gene mapping by using somatic cell hybrids is to distinguish between species-specific phenotypes. This was not possible for EGFRs because purified mouse EGF binds with equal affinity to both mouse and human cells. It was known that some mouse cell lines do not bind EGF. Because the lack of a phenotype in mouse cells can be used for gene mapping purposes, we tested a number of cell lines of murine and human origin for EGFRs. Both secondary and permanent cell lines of human origin bind EGF. In our screen we found that two independently derived mouse cell lines failed to bind EGF. These cell lines were B82, a mouse fibroblast line, and PG19, a line derived from a mouse melanoma. Assay of EGF Binding to Parental Cells. Unambiguous detection of EGFR binding requires demonstration of saturability of the receptors at appropriately low EGF concentrations. Accordingly, we presented increasing amounts of labeled EGF to a constant number of cells. Under these circumstances, specific binding will be reflected by a plateau in the amount of label bound to cells, whereas nonspecific binding will increase with increasing concentration of labeled probe. EGFRs of normal human fibroblasts are known to achieve 5% of saturation at approximately 2 ng of EGF per ml (9). Human diploid fibroblasts and HT18, a human fibrosarcoma cell line, were tested for EGFR binding at various concentrations of EGF. Representative results from this assay (Fig. 1) indicate that the D 6( G 4( ~ 2 '-4 x S 1 Q8 6. Pk 4 2 D F Proc. Natl. Acad. Sci. USA 77 (198) 4189 * A EGF, ng/ml FIG. 1. EGF binding to human and hybrid cells. Two plates each of the different cell lines were incubated with increasing concentrations of 125I-EGF. Excess (1 jg/ml) unlabeled EGF was added to one plate to determine nonspecific binding; cpm due to nonspecific binding were subtracted from the total binding (from plates incubated with labeled EGF alone). This corrected value was then converted to cpm/16 cells. A, HT18;, BCH2; *, BCH16. binding of EGF that was detected in these cell lines is due to the presence of the appropriate receptors. These results confirm those reported for HT18 by Todaro et al. (14). To determine the sensitivity of the assay, we mixed HT18 cells and mouse B82 cells in various proportions and assayed them for EGF binding. When the mixture contained as few as 5% HT18 cells we were able to detect their presence. These results indicated that, in the cell hybrids, a population containing 1% or more cells carrying the gene(s) responsible for EGFRs can be detected, because the hybrids usually carry a single copy of any given human chromosome per cell. As such, hybrid cell lines exhibiting EGF binding at a level greater than 1% of that of HT18 were considered to be positive for EGFRs. Nature of Defect in B82 and PG19. B82 and PG19 were tested for EGF binding under conditions identical to those used for the assay of HT18. Both of the cell lines failed to bind EGF. It is possible that the two cell lines share the same defect. Alternatively, if multiple genes are responsible for EGFRs, different elements might be altered in these two cell lines. To address this question we obtained hybrids between these two cells. The hybrid nature of the cells was established by isozyme and chromosome analysis. The hybrid cells were tested for EGFRs. The PGB series hybrids did not bind EGF. Because intraspecific hybrids do not lose chromosomes, we conclude that each of these cells probably has the same deficiency. Assignment of a Gene Involved in EGFR Expression. We attempted to determine if a human genetic component from HT18 or diploid fibroblasts would complement the deficiency in the mouse cells. A total of 13 hybrid cell lines were assayed; 8 of these were derived from fusion of HT18 and B82 and the rest were obtained by fusing PG19 and BP. The results of EGF binding assays of mouse-human hybrids are shown in Fig. 2. To ascertain that we were detecting EGFR
3 419 Genetics: Davies et al. Proc. Nati. Acad. Sci. USA 77 (198) loor * HT * BCH 6 PL. w IPo r. :5 A 7F F 21 * PEP 3d * BCH 7 * PEP 12a * BCH 5 BCH2 PEP 13a * BCH 16 BH 1 fb 82 BH1 PEP6a BCH15 O BCH 11 PEP 9c FIG. 2. Levels of EGF binding to parental and hybrid cells. EGF binding was measured at 5 ng of 125I-EGF per ml. Values are means from multiple assays and are expressed as percentage of 125I-EGF bound to HT18. PG19 exhibited %/ binding. activity, we examined three different cell lines extensively. Results of these studies (Figs. 1 and 3) indicate that the binding in these lines is saturable and, as such, specific. Mouse cell line lor Ca) in -4 x 1-, 6 x8. 4 I EGF, ng/ml FIG. 3. Saturability of EGFR in BCH2. Total b measured by adding increasing amounts of 125I-EGF t( of cells. Nonspecific binding (-) was determined by acdding increasing amounts of 1251-EGF to cells in the presence of unlal beled EGF at 1,ug/ml. FIG. 4. Metaphase chromosomes from hybrid cell line BCH5. Chromosomes were stained with quinicrine dihydrochloride. This cell contains two copies of human chromosome 7 (indicated by arrows). PG19 did not bind EGF. The low level of binding exhibited by B82 (Fig. 2) was nonsaturable and, as such, nonspecific. In contrast, binding by BCH 16 (which bound EGF at a level 24% that of HT18) was saturable and was considered to be specific (Fig. 1). For reasons described above, we considered any hybrid cell line that bound EGF to an extent less than 1% that of HT18 to be EGFR-negative. On this basis, the hybrids could be easily classified into two categories: one that bound EGF and one that did not. The hybrids that bound EGF did not show uniform binding values. We conclude that the human EGFRs are either expressed in a mouse genetic background or that the human genome can complement the mouse cell deficiency. The variation in the level of EGF binding most probably is due to variation in the frequency of individual human chromosome(s) present in these hybrids. Assignment of EGFR Gene. Detailed chromosome analysis was conducted on all of the 13 hybrid cell lines used in the study. PEP hybrids involved human fibroblasts that had a normal karyotype. The other human cell line used in these studies, HT18, contained all normal chromosomes except two, which were modified chromosomes 5 and 11 (15). All of these chromosomes could be identified unambiguously. At least 2 cells were examined from each cell line. The metaphase chromosomes from a representative hybrid cell are shown in Fig. 4. The results of the chromosome analysis are presented in Table 1. A detailed concordance and discordance analysis of EGF expression and various human chromosomes (Table 2) revealed that, in these hybrids, EGFR expression correlated best with the presence of human chromosome 7. On the basis of these results we conclude that a genetic element(s) located on human chromosome 7 participates in EGFR expression. DISCUSSION Examination of cell surface components, such as receptors for 2 24 specific molecules, by binding assay is dependent upon the )inding () was equal numbers ability to distinguish between nonspecific and specific binding. An important way to distinguish between these two types of binding is to determine if the binding is saturable at appropriate levels of the specific effector molecule. The saturation assays we performed on parental and hybrid cells clearly indicate that we observed specific binding (Figs. 1 and 3).
4 Genetics: Davies et al. Proc. Natl. Acad. Sci. USA 77 (198) 4191 Table 1. EGFR expression and chromosomal composition of hybrids Human EGFR-positive ceillines EGFR-negative cell lines chromosome BCH2 BCH3 BCH5 BCH6 BCH7 BCH16 PEP3d PEP12a PEP13a BCH11 BCH15 PEP6a PEP9c _ + _ _ _ _ + _ + _ _ + _ x Both of the mouse cell lines we used in these studies were found to be deficient in EGF binding. Because the nature and complexity of the EGFR is not known, it is possible that the deficiencies resulting in lack of EGF binding in PG19 and B82 are different. If so, it might be expected that the two cell types would complement each other's deficiencies. Results of the analysis of cell hybrids between the two cell lines indicate that the lesions in both PG19 and B82 are similar if not identical. It is also possible that one of the two cell lines carries a dominant mutation which prevents EGFR expression, especially since De Larco and Todaro (16) have reported the production by sar- Table 2. Correlation of EGFR expression with presence of individual human chromosomes Human Number of hybrid lines chromosome Concordant Discordant X 6 7 coma virus-transformed cells of a factor that competes with EGF for its receptor sites. This results in decreased EGF binding and would be a dominant phenotype. Results from our interspecific hybrids rule out this possibility because many hybrids were clearly capable of binding EGF. The lack of complementation between B82 and PG19 provided the rationale for grouping the two series of interspecies hybrids for gene mapping purposes. The reasons for the lack of EGFR in B82 and PG19 are not known. The normal counterparts of these cells are fibroblasts and melanocytes. Fibroblasts of different origins have EGFR (5, 8, 17, 18). Rodent or human melanocytes have not been tested but cell lines derived from melanomas were found not to contain EGFR (18). Results from the experiments presented here and those of others (14, 16-18) indicate that there is no apparent correlation between transformed and malignant phenotypes and EGFR expression. The interspecific cell hybrids can be readily classified into two categories based on their ability to bind EGF-those that are positive and those that are negative. Both sets of hybrids behaved similarly. All of the interspecific hybrids retained a full complement of the mouse chromosomes. Because several of these hybrids were also EGFR positive, it is highly unlikely that the defect in the mouse cells is of a dominant regulatory type. The lesion in the murine cells is probably due to a structural gene alteration. Based on the detailed chromosome analysis, the expression of EGFR and the presence of chromosome 7 were found to be concordant in all cases tested. The next best correlation of EGFR presence was with chromosomes 1 and 3: 2 of the 13 lines tested were discordant for these chromosomes. Both of these lines contained these chromosomes at high frequency (11). This observation validates the elimination of these two chromosomes as candidates for carrying the gene for EGFR expression. Based upon these analyses we conclude that human chromosome 7 carries a gene responsible for EGFR expression. The gene on this chromosome could code for human EGFR or complement the deficiency in PG19 and B82. If these two elements are different, EGFR expression in the cell hybrids might correlate
5 4192 Genetics: Davies et al. with one of two or more chromosomes. The fact that we observed positive correlation of EGFR and chromosome 7 and negative correlation with all other chromosomes indicates that the gene we have mapped is most probably the structural gene for EGFR. The unambiguous determination of the nature of this gene awaits detailed biochemical characterization of the receptor molecule. Several genes coding for cell surface antigens have been mapped to the human genome, including two to chromosome 7 (19, 2). The identification of these antigens was based on immunological assays. it is possible that the EGFRs that we have mapped to chromosome 7 are the same as those that were mapped by either Cicurel and Croce (19) or Knowles et al. (2).- Note Added in Proof. Similar results have been reported in abstract form (21). The idea for this study arose during discussions with Dr. Stanley Cohen. We thank Mrs. Noel Mann for manuscript preparation. This work was supported by grants from the American Cancer Society, National Science Foundation, March of Dimes-Birth Defects Foundation, National Institutes of Health, and a center grant to Princeton University from the National Cancer Institute. R.L.D. is a recipient of a National Science Foundation fellowship. 1. Heidmann, T. & Changeux, J. P. (1978) Annu. Rev. Biochem. 47, Cuatrecasas, P. (1974) Annu. Rev. Biochem. 43, Flier, J. S., Kahn, C. R., Roth, J. & Bar, R. S. (1975) Science 19, Brown, M. S. & Goldstein, J. L. (1976) Science 191, Proc. Natl. Acad. Sci. USA 77 (198) 5. Hollenberg, M. D. & Cuatrecasas, P. (1973) Proc. Natl. Acad. Sci. USA 7, Das, M., Miyakawa, T., Fox, C. F., Pruss, R. M., Aharonov, A. & Herschman, H. R. (1977) Proc. Natl. Acad. Sci. USA 74, Carpenter, G. & Cohen, S. (1979) Annu. Rev. Biochem. 48, Carpenter, G., Lembach, K. J., Morrison, M. & Cohen, S. (1975) J. Biol. Chem. 25, Carpenter, G. & Cohen, S. (1976) J. Cell Biol. 71, Weiss, M. C. & Green, H. (1967) Proc. Natl. Acad. Sci. USA 58, Kucherlapati, R., Tepper, R., Granelli-Piperno, A. & Reich, E. (1978) Cell 15, Burton, L. E., Wilson, W. H. & Shooter, E. M. (1978) J. Biol. Chem. 253, Server, A. C. & Shooter, E. M. (1976) J. Biol. Chem. 251, Todaro, G. J., De Larco, J. E., Nissley, S. P. & Rechler, M. M. (1977) Nature (London) 267, Rasheed, S., Nelson-Rees, W. A., Toth, E. M., Arnstein, P. & Gardner, M. B. (1974) Cancer 33, De Larco, J. E. & Todaro, G. J. (1978) Proc. Natl. Acad. Sci. USA 75, Todaro, G. J., De Larco, J. E. & Cohen, S. (1976) Nature (London) 264, Fabricant, R. N., De Larco, J. E. & Todaro, G. J. (1977) Proc. Natl. Acad. Sci. USA 74, Circurel, L. & Croce, C. M. (1977) J. Immunol. 118, Knowles, B. B., Solter, D., Trinchieri, G., Maloney, K. M., Ford, S. R. & Aden, D. P. (1977) J. Exp. Med. 145, Shimizu, N., Miskimins, K. & Shimizu, Y. (1979) Cytogenet. Cell Genet. 25,22.
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