Original Article
Molecular Determinants of the Response of Glioblastomas to EGFR Kinase Inhibitors
N Engl J Med 2005; 353:2012-2024November 10, 2005
- Abstract
Background
The epidermal growth factor receptor (EGFR) is frequently amplified, overexpressed, or mutated in glioblastomas, but only 10 to 20 percent of patients have a response to EGFR kinase inhibitors. The mechanism of responsiveness of glioblastomas to these inhibitors is unknown.
Methods
We sequenced kinase domains in the EGFR and human EGFR type 2 (Her2/neu) genes and analyzed the expression of EGFR, EGFR deletion mutant variant III (EGFRvIII), and the tumor-suppressor protein PTEN in recurrent malignant gliomas from patients who had received EGFR kinase inhibitors. We determined the molecular correlates of clinical response, validated them in an independent data set, and identified effects of the molecular abnormalities in vitro.
Results
Of 49 patients with recurrent malignant glioma who were treated with EGFR kinase inhibitors, 9 had tumor shrinkage of at least 25 percent. Pretreatment tissue was available for molecular analysis from 26 patients, 7 of whom had had a response and 19 of whom had rapid progression during therapy. No mutations in EGFR or Her2/neu kinase domains were detected in the tumors. Coexpression of EGFRvIII and PTEN was significantly associated with a clinical response (P<0.001; odds ratio, 51; 95 percent confidence interval, 4 to 669). These findings were validated in 33 patients who received similar treatment for glioblastoma at a different institution (P=0.001; odds ratio, 40; 95 percent confidence interval, 3 to 468). In vitro, coexpression of EGFRvIII and PTEN sensitized glioblastoma cells to erlotinib.
Conclusions
Coexpression of EGFRvIII and PTEN by glioblastoma cells is associated with responsiveness to EGFR kinase inhibitors.
Media in This Article
Figure 1
The PI3K–Akt Signaling Pathway.Figure 2
EGFRvIII and PTEN in Glioblastomas.Article Activity
- Article
Tyrosine kinases are key regulators of intracellular signaling.1,2 Overexpressed or mutated tyrosine kinases occur in many types of cancer and contribute to the development and progression of tumors.3-5 The dependence of tumor cells on persistently activated tyrosine kinases may render tumors susceptible to inhibitors of these kinases.3-7 The epidermal growth factor receptor (EGFR), a receptor tyrosine kinase, is a target for such inhibitors because it is amplified, mutated, or both in a number of neoplasms.8 A small subgroup of patients with lung cancer have a response to EGFR inhibitors,9-11 and mutations in the EGFR kinase domain have been associated with responsiveness.12-14 It is not known, however, whether such mutations affect the responsiveness of other types of cancer to EGFR kinase inhibitors.
Among patients with glioblastoma, the most common primary malignant brain tumor of adults, a small subgroup seems to benefit from the EGFR kinase inhibitors erlotinib and gefitinib.15,16 However, the infrequency of mutations in the EGFR kinase domain in glioblastomas17,18 suggests that such EGFR mutations cannot account for responsiveness to EGFR kinase inhibitors.19 The EGFR gene is commonly amplified in glioblastoma,20 but this abnormality also does not correlate with responsiveness to EGFR kinase inhibitors.16 Glioblastomas often express EGFRvIII, a constitutively active genomic deletion variant of EGFR.21-25 This variant of EGFR strongly and persistently activates the phosphatidylinositol 3' kinase (PI3K) signaling pathway, which provides critical information for cell survival, proliferation, and motility.26-30 Persistent PI3K signaling — as would be instigated by EGFRvIII — is believed to cause “pathway addiction”31; addicted tumor cells die if the pathway is disrupted by tyrosine kinase inhibitors. By promoting chronic dependence on PI3K signaling, EGFRvIII may sensitize glioblastoma cells to EGFR kinase inhibitors.
The PTEN (phosphatase and tensin homologue deleted in chromosome 10) tumor-suppressor protein, an inhibitor of the PI3K signaling pathway, is commonly lost in glioblastoma.20,27,32 This loss may promote cellular resistance to EGFR kinase–inhibitor therapy by dissociating EGFR inhibition from downstream PI3K pathway inhibition (Figure 1Figure 1
The PI3K–Akt Signaling Pathway.).33 We hypothesized that EGFRvIII would sensitize tumors to EGFR kinase inhibitors, whereas PTEN loss would impair the response to such inhibitors.33 To test this hypothesis, we analyzed EGFRvIII and PTEN at the gene and protein levels in glioblastomas from patients before treatment with EGFR kinase inhibitors. We also searched for mutations in EGFR and in its heterodimerization partner Her2/neu, which has been reported to be mutated in glioblastoma and could also affect the response to EGFR kinase inhibitors.34 We found a strong association between the coexpression of EGFRvIII and PTEN in glioblastoma cells and responsiveness to EGFR kinase inhibitors.Methods
Test Set
Since 2001, 49 patients with recurrent glioblastoma have been treated at the University of California, Los Angeles (UCLA) — 37 with gefitinib and 12 with erlotinib — as part of three multi-institutional clinical trials approved by the institutional review board. The clinical studies were performed through the Cancer Therapy Evaluation Program of the National Institutes of Health or Genentech. The correlative study described here was conducted independently and without industry support. Diagnoses were established by two neuropathologists and confirmed by a third pathologist who was unaware of the results of molecular analyses. Tumor specimens were obtained according to a protocol approved by the institutional review board of UCLA. All patients had measurable disease on magnetic resonance imaging (MRI) and had stopped receiving any previous cancer treatment at least four weeks before the start of monotherapy with an EGFR inhibitor.
MRI and clinical assessment were performed at baseline, every two months thereafter, and at the time of progression by a neuroradiologist and a neuro-oncologist who were unaware of the results of the molecular analyses. A response was defined as a decrease of at least 25 percent in the bidirectional area of the contrast-enhancing tumor on MRI in the absence of an increased dose of corticosteroids. Progression was defined as an increase of at least 25 percent in the bidirectional tumor area. Thirty-seven patients, 26 with clear-cut evidence of a response or progression, had sufficient tissue for molecular analysis (Table 1Table 1
Characteristics of the Patients. and Table 2Table 2
EGFR and PTEN Status in Tumor Tissue.). Ten patients fell between these extremes of response to treatment, with tumor growth or shrinkage of 25 percent or less (details are provided in Table 1 of the Supplementary Appendix, available with the full text of this article at www.nejm.org). One patient was excluded because a response occurred coincidently with an increase in the dose of decadron. The statistical methods used are described in the Supplementary Appendix.Validation Set
We obtained paraffin-embedded slides from biopsy specimens of malignant glioma from 33 patients who received erlotinib at the University of California, San Francisco (UCSF). Frozen tissue was not available from these patients. Immunohistochemical evaluation of EGFRvIII and PTEN was scored semiquantitatively by two UCLA pathologists who were unaware of the clinical results.
Molecular Studies
Sequencing of Genomic Tumor DNA
Exons and flanking intronic sequences for EGFR (kinase domain), HER2/neu (kinase domain), and PTEN (all exons) were amplified with the use of specific primers in a 384-well format involving a nested polymerase chain reaction (PCR), as performed by Agencourt Bioscience. Details are provided in the Supplementary Appendix.
Fluorescence in Situ Hybridization
Dual-probe fluorescence in situ hybridization (FISH) was performed on paraffin-embedded sections with locus-specific probes for EGFR and the centromere of chromosome 7 (CEP7) (Vysis). Standard FISH protocols for pretreatment, hybridization, and analyses were followed according to the manufacturer's instructions.20
Reverse Transcriptase–PCR
For the reverse-transcriptase–PCR (RT-PCR) assay, high-quality total RNA was extracted from 13 fresh-frozen tumor samples (4 from patients with a response and 9 from patients without a response). Complementary DNA (cDNA) was synthesized and amplified with the use of primers designed specifically to amplify EGFR (1044-bp product) and EGFRvIII (243-bp product). Details are provided in the Supplementary Appendix.
Real-Time PCR
Genomic DNA was extracted from samples from 15 patients (7 with a response and 8 without a response) and subjected to real-time PCR with the use of the iCycler thermocycler (Bio-Rad Laboratories). All measurements were made in triplicate and confirmed by independent experiments. The Supplementary Appendix lists the primer sequences used and provides complete details.
Immunohistochemistry and Immunoblotting
Paraffin-embedded tissue sections underwent immunohistochemical analysis in which the results were scored independently by two pathologists who were unaware of the findings of the molecular analyses. Scores of 0 and 1 were considered to indicate PTEN loss.27 If staining for PTEN was heterogeneous, tumors with diminished or absent staining in at least 25 percent of the section were considered PTEN-deficient. Tumors demonstrating focal, moderate-to-strong immunostaining for EGFRvIII were considered positive.27 Quantitative image analysis to confirm the pathologists' scoring was also performed with the use of Soft Imaging System software (complete details are provided in the Supplementary Appendix).
Cell-Line Models
U87MG Model
EGFR and EGFRvIII cDNAs were introduced into U87MG cells and U87MG-PTEN cells (which overexpress PTEN) by means of a retroviral vector; 1000 cells per well were seeded into eight sets of 96-well plates. Twenty-four hours later, erlotinib was added at final concentrations ranging from 0 to 10 μM. Plates were incubated for 7 to 10 days, fixed, stained with 0.25 percent crystal violet in methanol, and quantified. The results were confirmed in several independent clones.
Other Cell-Line Models
Mouse-embryonic fibroblasts with deletion of the PTEN locus were kindly provided by Dr. Hong Wu (UCLA). A431 cell lines stably expressing vector RNA interference (RNAi), short hairpin RNA (shRNA) to human PTEN (5'ATAGCTACCTGTTAAAGAA3'), or pWZL-MyrAktΔ4-129 (kindly provided by Dr. Russell Pieper, UCSF) were derived by retroviral infection and selection. PTEN shRNAi and vector shRNA were also stably expressed in amphotropic 293T cells (Orbigen). PKI-166 was provided by Novartis. Cell viability was determined in triplicate by means of trypan blue exclusion, and the results were confirmed in three independent experiments. Cells were plated at a density of 50,000 cells per well in six-well plates, recounted after the cells had adhered to the plate, and then treated with vehicle or an EGFR kinase inhibitor. After four to five days of incubation, the supernatant (containing floating cells) and trypsin-treated adherent cells were pooled, spun at 1500 rpm for 90 seconds, and resuspended in trypan blue for cell counting. The occurrence of apoptosis was confirmed in independent experiments by immunoblotting for caspase-cleaved poly(adenosine diphosphate ribose) polymerase (number 9546, Cell Signaling Technology) and by flow cytometry.
Results
Patients
For the purposes of this study, we selected 7 patients with unequivocal evidence of a response and 19 who had no response (as reflected by evidence of tumor progression on MRI within eight weeks after initiating therapy) (Figures 1A and 1B of the Supplementary Appendix). Median survival after the initiation of treatment with an EGFR kinase inhibitor was significantly longer among patients with a response than among those without a response (21.7 vs. 5.8 months, P=0.01), as was the median time to progression (9.7 vs. 1.7 months, P<0.001) (Table 1, and Figure 1C of the Supplementary Appendix). There were no significant correlations between response and age, sex, the extent of surgical resection, Karnofsky performance status, or the dose of EGFR inhibitor (Table 3Table 3
Biomarkers of a Response to EGFR Kinase Inhibitors.).Mutations in the EGFR Kinase Domain
We sequenced the kinase domain of EGFR in the glioblastomas from the 26 patients. The quality of the DNA was sufficient to allow us to sequence the entire kinase domain of EGFR (exons 18 through 24) in six of seven patients with a response and exon 21 alone in Patient 6. No mutations were detected in the seven patients with a response or in eight of the patients with no response for whom DNA was available for sequencing (Table 2). Thus, mutations in the EGFR kinase domain are unlikely to determine the sensitivity of glioblastomas to EGFR kinase inhibitors. We also sequenced the kinase domain of Her2/neu and found no mutations.
EGFR Gene Amplification
FISH showed — and real-time PCR confirmed — that the EGFR gene was amplified in 12 of 25 glioblastomas (48 percent); 7 of these 12 demonstrated polysomy. No association between amplification of EGFR and a response to EGFR inhibitors was found (Table 3).16
Expression of EGFRvIII and PTEN Protein
We used immunohistochemical analysis to screen for EGFRvIII and validated the results with the use of nucleic acid–based assays (RT-PCR and the ratio of EGFR exon 9 DNA to exon 4 DNA) and immunoblotting in the 15 available samples of frozen tumor (Figure 2AFigure 2
EGFRvIII and PTEN in Glioblastomas. and Figure 2B and Table 2). We found complete agreement between the nucleic acid–based assays and immunohistochemical analysis (κ=1.0, P<0.001) and between immunoblotting and immunohistochemical analysis (κ=1.0, P<0.001) (Figure 3 of the Supplementary Appendix). These results are consistent with recent findings by another group21 and provide support for the use of immunohistochemical analysis to determine the EGFRvIII status in the remaining 11 patients for whom no frozen tissue was available.EGFRvIII was detected in 12 of 26 malignant gliomas (46 percent) (Table 2), similar to the previously reported frequency in glioblastomas.21,27 It was found only in tumors with EGFR amplification or a gain of chromosome 7. Of 12 patients whose tumors expressed EGFRvIII, 6 had a response to EGFR kinase inhibitors, whereas 1 of 14 patients whose tumors did not express EGFRvIII had a response to EGFR kinase inhibitors (P=0.03). These data suggested that the expression of EGFRvIII sensitizes gliomas to EGFR kinase inhibitors. However, the lack of response in 50 percent of patients with EGFRvIII-expressing tumors indicates that other factors influence the outcome of treatment.
Since PTEN may be required for a response to the EGFR family of kinase inhibitors,33 we studied this protein in glioblastomas using immunohistochemical analysis and immunoblotting (Figure 2C). The results of both assays were concordant (κ=0.8, P=0.005). None of 13 patients whose tumors lacked PTEN had a response to EGFR inhibitors, whereas 7 of 13 patients with PTEN-positive tumors had a response (P=0.005) (Table 3). To rule out the possibility that the immunohistochemical assay detected a mutant protein, we sequenced PTEN; no mutations were detected in the responsive tumors. The greatest likelihood of a clinical response to EGFR kinase inhibitors was associated with coexpression of EGFRvIII and PTEN (odds ratio, 51; 95 percent confidence interval, 4 to 669; P<0.001) (Table 3).
Ten patients who had neither tumor regression nor substantial tumor growth while receiving an EGFR kinase inhibitor (Table 1 of the Supplementary Appendix) were excluded from the original analysis because they did not fit the extremes of a clear response or treatment failure. None of these patients, who had a median time to progression of 3.7 months, had tumors that coexpressed EGFRvIII and PTEN (Table 1 of the Supplementary Appendix).
Validation Set
We analyzed the expression of EGFRvIII and PTEN in 33 gliomas from patients who were treated with erlotinib at a different institution, UCSF (Table 2 of the Supplementary Appendix). Of these 33 patients, 8 had a clinical response. A clinical response in this group was also significantly associated with the coexpression of EGFRvIII and PTEN (odds ratio, 40; 95 percent confidence interval, 3 to 468; P=0.001) (Table 3).
In Vitro Studies of the Coexpression of EGFRvIII and PTEN
We induced the expression of relevant combinations of PTEN, EGFR, and EGFRvIII in U87MG glioblastoma cells. U87MG cells are deficient in PTEN,35-38 express low levels of wild-type EGFR, and lack EGFRvIII.39,40 Coexpression of EGFRvIII and PTEN in these glioblastoma cells rendered them highly susceptible to arrest of growth by erlotinib, as compared with control cells and U87MG cells that were transfected with other components of the PTEN–EGFR system (Figure 3AFigure 3
Loss of PTEN and Resistance to EGFR Kinase Inhibitors in EGFR-Sensitized Cells.). In these experiments, erlotinib caused the arrest of growth but not apoptosis in U87MG cells. Because U87MG cells do not depend on EGFR signaling for survival, we examined the effect of a lack of PTEN in three cell lines that undergo apoptosis in the presence of EGFR kinase inhibitors: SF295 human glioblastoma cells, mouse embryonic fibroblasts from mice in which the PTEN gene has been conditionally inactivated,45 and A431 cells with stable PTEN RNAi (Figure 3B). These experiments were performed with two EGFR kinase inhibitors, erlotinib and PKI-166.41 In all three systems, the lack of PTEN abrogated or markedly reduced the extent of apoptosis induced by the two inhibitors of EGFR kinase (Figure 3B).We examined the contribution of Akt to the resistance to EGFR kinase inhibitors conferred by the loss of PTEN, because many of the effects that follow the loss of PTEN occur through the activation of the downstream kinase Akt.46 Erlotinib-induced inhibition of the phosphorylation of Akt correlated with growth inhibition in U87MG cells (Figure 4 of the Supplementary Appendix), but not in all cell lines. For example, in A431 cells expressing PTEN shRNA, phosphorylation of Akt was blocked by EGFR kinase inhibitors (Figure 5 of the Supplementary Appendix, lanes 3 and 4), but the cells remained viable (Figure 3B). Furthermore, overexpression of a membrane-targeted and persistently activated allele of Akt47 (Figure 5 of the Supplementary Appendix, lanes 5 and 6) did not prevent A431 cells from undergoing apoptosis mediated by EGFR kinase inhibitors (Figure 3C). These findings suggest that Akt-independent branches of the PTEN pathway may contribute to the effects of PTEN on the sensitivity of tumors to EGFR kinase inhibitors. We also noted that the levels of EGFR and EGFRvIII phosphorylation were consistently higher in PTEN-deficient cells than in their PTEN-expressing counterparts, suggesting that PTEN affects the receptor protein itself (Figure 6 of the Supplementary Appendix). Taken together, these results suggest the existence of multiple mechanisms by which the loss of PTEN promotes resistance to EGFR kinase inhibitors in glioblastoma cells.
Discussion
In this study of glioblastomas from patients who were treated with gefitinib or erlotinib, we found that responsiveness to EGFR kinase inhibitors was strongly associated with coexpression by the tumor of EGFRvIII and PTEN. EGFRs with mutations in the tyrosine kinase domain selectively activate antiapoptotic signals through the PI3K–Akt signaling pathway (Figure 1).26 Akt, a kinase involved in cellular proliferation and apoptosis, is activated by signals generated by PI3K. Inhibition of this antiapoptotic signal by gefitinib appears to be critical to the efficacy of the drug.26 Like the EGFR kinase domain mutants in lung cancer, EGFRvIII, a constitutively active mutant variant of EGFR, preferentially activates PI3K–Akt signaling and can sensitize glioblastoma cells to EGFR kinase inhibitors.26-30 Loss of PTEN, a tumor-suppressor protein that inhibits the PI3K signaling pathway, may promote resistance to EGFR kinase inhibitors.33 We found that the lack of PTEN in gliomas is associated with resistance to EGFR kinase inhibitors. Moreover, in four isogenic cell lines, loss of PTEN markedly diminished responsiveness to EGFR kinase inhibitors. Our evidence suggests that both Akt-dependent and Akt-independent mechanisms underlie the resistance caused by a loss of PTEN.
These results suggest that screening of tumors for PTEN protein may be warranted in patients with cancers with EGFR kinase mutations that do not respond to gefitinib, erlotinib, or related EGFR kinase inhibitors. Our data also suggest that downstream inhibition of the PI3K pathway, perhaps at the level of the mammalian target of rapamycin (a kinase related to PI3K) (Figure 1), could be combined with EGFR kinase inhibitors in patients with PTEN-deficient tumors to promote responsiveness.48 These studies also raise the possibility that more complete inhibition of EGFR phosphorylation may overcome the resistance to kinase inhibitors caused by a deficiency of PTEN.
In summary, we have implicated EGFRvIII and PTEN as molecular determinants of the sensitivity of glioblastomas to EGFR kinase inhibitors. Prospective validation of EGFRvIII and PTEN as predictors of the clinical response to EGFR kinase inhibitors in independent data sets is warranted.
Supported by grants from the National Institute for Neurological Disorders and Stroke (NS050151 and NS43147, to Dr. Mischel) and the National Cancer Institute (CA95616, to Dr. Cavenee; CA108633, to Dr. Mischel; CA62399, to Dr. Prados; and CA105695, to Dr. Cloughesy); Accelerate Brain Cancer Cure Awards (to Drs. Mischel, Mellinghoff, and Sawyers); the Goldhirsh Foundation (to Dr. Sawyers); a Fellow Award from the National Foundation for Cancer Research (to Dr. Cavenee); a UCSF brain tumor spore grant (CA097257); a Young Investigator Award from the American Society of Clinical Oncology (to Dr. Mellinghoff); a Translational Research Grant from American Brain Tumor Association (to Dr. Wang); the Medical Scientist Training Program at UCLA (to Ms. Huang); a UCLA Tumor Cell Biology Training Grant funded by the National Cancer Institute (5T32CA09056, to Dr. Lu); a Ruth L. Kirschstein National Research Service Award (5F31GM067600, to Dr. Vivanco); the Harry Allgauer Foundation through the Doris R. Ullmann Fund for Brain Tumor Research Technologies; the Henry E. Singleton Brain Tumor Foundation; the Phase One Foundation; a generous donation from the Ziering Family Foundation in memory of Sigi Ziering; and the Art of the Brain and the Roven Family Fund in memory of Dawn Steel.
Dr. Sawyers is an investigator of the Howard Hughes Medical Institute and a Doris Duke Distinguished Clinical Investigator. Drs. Sawyers and Mischel report having received lecture fees from Genentech.
A patent application entitled “Molecular Determinants of EGFR Kinase Inhibitor Response in Glioblastoma” has been filed by the University of California. The patent includes the names of Drs. Mischel, Mellinghoff, Wang, Sawyers, and Cloughesy.
Drs. Mellinghoff, Wang, and Vivanco contributed equally to the article.
We are indebted to Drs. Stanley Nelson, Jonathan Braun, and Harry Vinters at UCLA and Drs. David Eberhard and Barbara Klenke at Genentech for helpful discussions; to Jennifer Cloud and Ralph Debiasi for technical assistance; and to Dr. Darrell Bigner for providing L8A4 antibody.
Source Information
From the Departments of Molecular and Medical Pharmacology and Medicine (I.K.M., C.L.S.), Pathology and Laboratory Medicine (M.Y.W., S.Z., E.Q.D., K.V.L., K.Y., D.J.C., B.L.R., P.N.R., P.S.M.), Human Genetics (J.H.Y.H., S.H.), Biostatistics (S.H.), Neurosurgery (L.M.L.), and Neurology (T.F.C.); the Henry E. Singleton Brain Tumor Program (I.K.M., L.M.L., T.F.C., P.S.M.); the Molecular Biology Institute (I.V., C.L.S.); and the Howard Hughes Medical Institute (C.L.S.) — all at the David Geffen School of Medicine at the University of California, Los Angeles, Los Angeles; the Department of Neurological Surgery, University of California, San Francisco, San Francisco (D.A.H.-K., D.S., M.P.); the Ludwig Institute for Cancer Research at the University of California, San Diego, San Diego (W.K.C.); and the Department of Medical Oncology, Dana–Farber Cancer Institute, the Department of Medicine, Harvard Medical School, and the Broad Institute of Harvard and the Massachusetts Institute of Technology — all in Boston (R.B., T.C.P., J.C.L., W.R.S.).
Address reprint requests to Dr. Mischel at the Department of Pathology and Laboratory Medicine, David Geffen School of Medicine at UCLA, 10833 Le Conte Ave., Center for the Health Sciences, Room 13-321, Los Angeles, CA 90095-1732, or at pmischel@mednet.ucla.edu.
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