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Transcription induced by EGFR activation often involves the coordinated expression of genes that positively and negatively regulate the original signaling pathway; therefore, altera-tion

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associated with MIG6 expression

Takeshi Nagashima1, Ryoko Ushikoshi-Nakayama1, Atsushi Suenaga2, Kaori Ide1, Noriko Yumoto1, Yoshimi Naruo3, Kaoru Takahashi1, Yuko Saeki1, Makoto Taiji2, Hiroshi Tanaka3, Shih-Feng Tsai4 and Mariko Hatakeyama1

1 Cellular Systems Modeling Team, Computational Systems Biology Research Group, Advanced Computational Sciences Department, RIKEN Advanced Science Institute, Yokohama, Kanagawa, Japan

2 High-Performance Molecular Simulation Team, Computational Systems Biology Research Group, Advanced Computational Sciences Department, RIKEN Advanced Science Institute, Yokohama, Kanagawa, Japan

3 School of Biomedical Science, Tokyo Medical and Dental University, Tokyo, Japan

4 Division of Molecular and Genomic Medicine, National Health Research Institutes, Zhunan, Miaoli, Taiwan

Keywords

EGFR; gene expression; MIG6; mutation;

signal transduction

Correspondence

M Hatakeyama, Cellular Systems Modeling

Team, Computational Systems Biology

Research Group, Advanced Computational

Sciences Department, RIKEN Advanced

Science Institute, 1-7-22 Suehiro-cho,

Tsurumi-ku, Yokohama, Kanagawa

230-0045, Japan

Fax: +81 45 509 9613

Tel: +81 45 509 9302

E-mail: marikoh@gsc.riken.jp

Database

Microarray data used in the present

study have been deposited in the Gene

Expression Omnibus database (http://www.

ncbi.nlm.nih.gov/geo/) with accession

number GSE11729

(Received 10 May 2009, revised 14 July

2009, accepted 16 July 2009)

doi:10.1111/j.1742-4658.2009.07220.x

Controlled activation of epidermal growth factor receptor (EGFR) is sys-tematically guaranteed at the molecular level; however, aberrant activation

of EGFR is frequently found in cancer Transcription induced by EGFR activation often involves the coordinated expression of genes that positively and negatively regulate the original signaling pathway; therefore, altera-tions in EGFR kinase activity may reflect changes in gene expression asso-ciated with the pathway In the present study, we investigated transcriptional changes after EGF stimulation with or without the EGFR kinase inhibitor Iressa in H1299 human non-small-cell lung cancer cells [parental H1299, H1299 cells that overexpress wild-type EGFR (EGFR-WT) and mutant H1299 cells that overexpress EGFR where Leu858 is substituted with Arg (L858R)] The results obtained clearly demonstrate differences in transcriptional activity in the absence or presence of EGFR kinase activity, with genes sharing the same molecular functions showing distinct expression dynamics The results show the particular enrichment of EGFR⁄ ErbB signaling-related genes in a differentially expressed gene set, and significant protein expression of MIG6⁄ RALT(ERRFI1), an EGFR negative regulator, was confirmed in L858R High MIG6 protein expres-sion was correlated with basal EGFR phosphorylation and inversely corre-lated with EGF-induced extracellular signal-regucorre-lated protein kinase phosphorylation levels Investigation of the NCI-60 cell lines showed that ERRFI1expression was correlated with EGFR expression, regardless of tis-sue type These results suggest that cells accumulate MIG6 as an inherent negative regulator to suppress excess EGFR activity when basal EGFR kinase activity is considerably high Taking all the above together, an EGFR mutation can cause transcriptional changes to accommodate the activation potency of the original signaling pathway at the cellular level

Abbreviations

AU, approximate unbiased; EGFR, epidermal growth factor receptor; ERK, extracellular signal-regulated protein kinase; GEO, gene

expression omnibus; GO, gene ontology; KEGG, Kyoto Encyclopedia of Genes and Genomes; MAPK, mitogen-activated protein kinase; MEK, mitogen-activated protein kinase kinase; NSCLC, human non-small-cell lung cancer; SHC, Src homology 2 domain containing.

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Epidermal growth factor receptor (EGFR) is a

mem-brane tyrosine kinase that is involved in the regulation

of a wide variety of biological processes [1] Controlled

activation of EGFR is systemically and evolutionarily

guaranteed by the presence of a variety of ligands, or

by dimerization and trans-activation with other family

member receptors of ErbB [2,3] Additionally, the

potency and dynamics of EGFR signaling are

adap-tively tuned via biochemical parameters such as affinity

constants, catalytic activities, the concentration of the

signaling mediators and plastic pathway architectures

[4–6], thereby ensuring that cells can produce the

desired outputs in response to various cellular

condi-tions Transcription induced shortly after ligand

stimu-lation is quantitatively regulated by upstream signaling

dynamics, which concomitantly regulate the dynamics

of the original pathway Kinases and effector proteins

in the EGFR-mitogen-activated protein kinase

(MAPK) cascade are particular major targets [7–10]

Therefore, quantitative transcriptional outcomes, in

addition to qualitative ones, may be altered if EGFR

kinase activity is modified by mutation,

overexpres-sion, or suppressed by inhibitors such as Iressa

(Gefiti-nib, AstraZeneca, London, UK) or Tarceva (Erloti(Gefiti-nib,

Roche, Basel, Switzerland)

In the present study, time-course genome-wide gene

expression was investigated, aiming to delineate the

transcriptional outcomes induced by EGFR activation

under various conditions In brief, the human

non-small-cell lung cancer (NSCLC) cell line H1299 with

EGFR overexpression (wild-type: EGFR-WT) and

with or without the mutation in which Leu858 is

substituted with Arg (mutant: L858R), in addition to

the parental cell line, was used Various point

muta-tions at L858R, L861, S768, E709 and G719 in the

EGFR kinase domain, insertions in exon 20 and

dele-tion mutadele-tions in exon 19 of the gene for EGFR are

often found in NSCLC patients Among these, the

L858R mutation has been known to be a good

predic-tive marker of Iressa (Gefitinib) responsiveness [11–13]

Therefore, delineating the transcriptional regulation of

this mutant is of clinical importance in terms of

con-tributing towards our understanding of patient

sensi-tivity to Iressa, as well as side effects and drug

resistance The results obtained demonstrate

differ-ences in EGF-stimulated transcription in the absence

or presence of Iressa in all cell lines tested, and show

that the expression dynamics of the affected genes with

overlapping molecular functions are distinct in each

cell group Particular enrichment of cell-specific genes

involved in the cell cycle and MAPK signaling

path-way was found and, of these, we confirmed significant protein expression of the EGFR negative regulator MIG6⁄ RALT only in L858R cells

MIG6⁄ RALT is known to be a transcriptional feed-back regulator of the ErbB-MAPK signaling pathway [14,15] and its loss is associated with ErbB2⁄ HER-2 oncogenic potency leading to Herceptin resistance [16] Furthermore, its overexpression is associated with down-regulation of phosphorylated-ErbB2 [17] in breast cancer The present study, using lung cancer cell lines with various EGFR mutants, suggested that endogenous MIG6 may be directly associated with basal EGFR kinase activity Cells might accumulate MIG6 to suppress excess EGFR activity; therefore, MIG6 may be regarded as a molecular marker for indicating the intrinsic kinase activity of EGFR, regardless of tissue type

Results

Ligand-induced transcriptional signatures of EGFR-WT and L858R in the absence or presence

of EGFR kinase activity The transcriptional activity that follows EGFR activa-tion often involves the expression of genes that nega-tively and positively adjust the magnitude and duration of the original EGFR-MAPK signaling path-ways [7–10,18] Therefore, quantitative transcriptional outcomes, in addition to qualitative ones, may be altered if EGFR kinase activity is modified by muta-tion and overexpression, or suppressed by kinase inhibitors such as Iressa Accordingly, time-course microarray analysis was performed to identify genes that functionally modulate the EGFR signaling path-way For this purpose, three derivatives of human NSCLC cell lines, comprising parental H1299,

EGFR-WT and L858R, were employed as cellular systems The overall transcriptional signatures after EGF administration in the absence or presence of the EGFR kinase inhibitor Iressa were investigated using Affymetrix GeneChip (U133Plus 2.0; Affymetrix, Santa Clara, CA, USA) The workflow of gene expres-sion data analysis is shown in Fig 1

Cell-specific differentially expressed genes and effect of EGFR kinase inhibitor on gene expression

First, the overall gene expression profiles in the EGF- and Iressa-stimulated three cell lines were

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examined A hierarchical clustering together with

assessment of cluster uncertainty was carried out

according to the expression levels of all probe sets on

the array for each cell stimulated with EGF in the

absence or presence of Iressa Cluster analysis clearly

showed distinct transcriptional outcomes in the three

cell lines Interestingly, the cellular response of L858R

was similar to that of EGFR-WT in terms of the EGF

response, and similar to the parental cell line in the

presence of Iressa (Fig 2A)

Cell-specific gene expression associated with EGFR

activity was determined using two criteria: (a) where

the expression level shifted relative to nonstimulated

cells after stimulation by EGF or EGF + Iressa

(ligand responsive genes) and (b) where the expression

level was altered in the absence or presence of Iressa

(kinase responsive genes) As a result, 746, 1034 and

1444 genes were identified for H1299, EGFR-WT and

L858R, respectively (2234 genes in total) (Fig 2B)

The list of induced genes obtained included DUSP6 (a

MAPK phosphatase), ERBB2 and ERBB3, which

modulate EGFR signaling

Cluster analysis of selected genes clearly showed a

discrepancy in the expression dynamics of each cell

type (Fig 2C) Although H1299 only had two major

clusters (simple ascending and descending), EGFR-WT

and L858R cells showed multiple clusters for EGF or

EGF + Iressa stimulation Additionally, comparison

of EGF- and EGF + Iressa-induced time courses

highlighted differences in the effect of Iressa on gene expression dynamics in the three cell lines (Fig 3) Consistent with the clustering results, Iressa induced only minor changes in gene expression of the parental cell line (Fig 3A) On the other hand, EGFR-WT exhibited larger changes in gene expression levels in response to Iressa compared to L858R, whereas a lar-ger change in the expression time course was observed for L858R (Fig 3B) Furthermore, our analysis revealed a distinct time-dependent effect of Iressa among the cell lines examined (Fig 3C) In

EGFR-WT, the effect of Iressa on gene expression was rather temporal (4–6 h), whereas its effect was more persis-tent in L858R (> 10 h)

Different transcriptional regulation of biological pathways induced by ligand and EGFR kinase inhibitor

In an effort to assess the biological functions of the differentially expressed genes described above, func-tional enrichment analysis was performed using the Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway [19] and Gene Ontology (GO) [20] databases The results showed that EGF and Iressa altered the expression levels of genes involved in specific biological processes, such as the cell cycle, circadian rhythm, MAPK signaling pathway, small cell lung cancer and p53 signaling pathway (Table 1) Furthermore, GO term analysis for individual clusters highlighted the commonality and discrepancy of cellular responses to ligand stimulation in the absence or presence of EGFR kinase activity (Table S1) For example, genes involved

in transcriptional regulation and protein binding were found to be enriched in the early response gene cluster

of the three cell lines (clusters presented within a red bar in Fig 2C) Genes associated with cell cycle func-tions were also significantly selected for all cell lines; however, the time-course expression patterns differed for each Different expression time courses for the same molecular function were also observed, such as genes related to signal transduction via receptor bind-ing and receptor activity Thus, a difference in EGFR activity can result in the distinct transcriptional regula-tion of important biological processes that may con-tribute to the sensitivity of the cells to Iressa or ligand

Identification of direct EGFR regulators through functional annotation of Iressa-induced

differentially expressed genes

As described above, EGF and Iressa-induced overall expression dynamics differed between cell lines, and

Fig 1 Workflow of gene expression data analysis The workflow

of microarray data analysis applied in the present study is shown.

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these differences were observed even in those genes

associated with same molecular functions In an effort

to further examine how a single amino acid mutation

in the EGFR kinase domain affects downstream gene

expression, those genes likely to be under the

regula-tion of activated EGFR were examined Genes

show-ing distinct time-course patterns in the absence or

presence of Iressa were extracted (a correlation

coeffi-cient of <)0.5 between EGF and EGF + Iressa) As

a result, 405 genes were selected (12, 117 and 299 genes for H1299, EGFR-WT and L858R, respectively) Of these, KEGG pathway analysis revealed that the ErbB signaling pathway is enriched in L858R (P = 0.02057; Bonferonni corrected) Furthermore, functional annotation using public databases identified 52 out

of 405 genes (12.8%) as comprising regulators of EGFR⁄ ErbB and MAPK signaling pathways (Fig 4A)

A

B

C

Fig 2 Gene expression profiles in H1299, EGFR-WT and L858R after EGF or Iressa stimulation (A) Overall similarity of gene expression profiles in EGF- and Iressa-stimulated cells Clusters with high AU values (> 95) are highlighted by red rectangles (B) The number of differ-entially expressed genes in each cell line The Venn diagram represents the number of differdiffer-entially expressed genes obtained using two selection criteria (see Experimental procedures) in H1299, EGFR-WT and L858R cell lines Numbers in round and square brackets represent the number of probe sets and the number of probe sets without gene IDs, respectively Other numbers refer to the number of genes (C) Clustering of expression profiles of differentially expressed genes Representative genes were shown by number: 1, ERRFI1; 2, DUSP6; 3, SPRY4; 4, ERBB3; 5, ERBB2 Ctrl, control (no stimulation); I, Iressa; E, EGF; E+I, EGF and Iressa.

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Among these, we noted cell-specific differential

expression of two direct EGFR regulators: SPRY4

(Sprouty-4) and ERRFI1 (MIG6)

Sprouty family member proteins are known to be

negative and positive regulators of fibroblast growth

factor and EGFRs, respectively [10,21–23] In our

analysis, SPRY4 expression was stimulated by EGF and reduced by the addition of Iressa in EGFR-WT How-ever, the induction of Sprouty-4 remained unchanged at the protein level in both cell types (data not shown) MIG6 (RALT or ERRFI1) is a cytoplasmic adapter protein that can inhibit EGFR kinase activity through

B

Fig 3 Iressa-induced differences in gene expression Iressa-induced differences in gene expression amplitude (A) and time course (B) Dif-ferences in Iressa-induced gene expression were calculated using two indexes: (a) the Icvalue that reflects differences in the expression level and (b) the correlation coefficient which represents differences in the expression pattern Two time-course profiles (EGF and EGF + Iressa) of selected genes were used for the analysis The distribution of I c and correlation coefficient in three cell lines are shown in (A) and (B), respectively Larger (Ic> 10) and smaller (Ic< )10) I c values were rounded to 10 and )10, respectively (C) The number of probe sets where the expression level was altered by Iressa at individual time points in H1299, EGFR-WT and L858R.

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direct binding to the kinase domain [15,24–26]

ERR-FI1expression was significantly induced in EGFR-WT

and L858R cells Although ERRFI1 was reduced in

response to EGF stimulation in H1299 cells, it was

transiently expressed in EGFR-WT cells and

constitu-tively expressed in L858R cells Western blot analysis

identified higher basal levels of MIG6 protein in

L858R compared to parental H1299 and EGFR-WT

cells, and little change was observed in response to

EGF stimulation (Fig 4B)

The evolutionarily conserved ErbB-binding region

(EBR) of MIG6 is known to bind the RYLVIQ

sequence of EGFR (amino acids 953–958), which

par-ticipates in the allosteric control of EGFR activity

[26] Therefore, high expression of MIG6 may be able

to suppress the effect of EGF for EGFR

phosphoryla-tion in EGFR-WT Indeed, our validaphosphoryla-tion experiment

confirmed that overexpression of MIG6 decreased the

phosphorylation of EGFR in the presence of a high

concentration of EGF in EGFR-WT cells (data not

shown), as previously reported for breast [17] and

other cell lines [24]

Accordingly, the expression level of MIG6 should be

associated with high EGFR expression levels because

the overexpression of EGFR has often been linked to

high EGFR kinase activity Therefore, ERRFI1

expres-sion in various cancer cell lines was investigated using

the publicly available NCI-60 dataset The dataset was

downloaded from the Gene Expression Omnibus (GEO)

database (http://www.ncbi.nlm.nih.gov/geo/; accession

number = GSE5720) The results of the analysis

sur-prisingly showed that ERRFI1 expression levels varied

among all cell lines and no tissue-specific trend was

observed (Fig 5A), although a previous study reported

tissue-specific expression of ERRFI1 in some cancers

[24] ERRFI1 expression was most correlated with

EGFR expression, regardless of cancer cell type, and

was not correlated with other ERBB gene expression

(Fig 5B) The results indicate that MIG6 could be uti-lized as a molecular marker for indicating the func-tional activity of EGFR in tissues, regardless of cancer type Indeed, our transcriptional analysis indicated that Iressa totally abolished the expression of ERRFI1 in EGFR-WT and L858R cells (Fig 2C) Accordingly, ERRFI1may operate as a molecular sensor to monitor EGFR kinase activity

Relationship between MIG6 expression and EGFR mutation

Although a functional role of MIG6 in relation to EGFR kinase regulation has been reported, as described above, and was confirmed in the present study, its relationship to Iressa sensitivity, EGFR mutation and the MAPK signaling pathway has not been reported

Earlier studies found that clinical responsiveness to Iressa was closely associated with EGFR mutations such as L858R and delL747-P753insS in the kinase domain, which also enhance EGF-dependent EGFR activation [11,12] Huang et al [13] performed muta-tional analysis of the EGFR gene from exons 18–21 in

a series of surgically resected NSCLCs and found a high mutation rate for EGFR in Taiwanese patients

In addition to major mutation types such as the L858R mutation and deletions in exon 19, various point mutations at residues L861, S768, E709, G719 and H835 and insertions in exon 20 of the EGFR gene have been observed [13]

Accordingly, other H1299 derivatives that overex-press different types of EGFR mutants, including EGFR-Del (deletion of the kinase domain), S768I, L861Q, E709G and G719S [27], in addition to parental H1299, EGFR-WT and L858R, were assessed by quan-titative western blot analysis in an effort to delineate the relationship between EGFR mutation, Iressa sensitivity

Table 1 Enriched KEGG pathways in differentially expressed genes.

KEGG pathway

*P < 0.01, **P < 0.05.

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and MIG6 expression Surprisingly, MIG6 expression

was significantly high in L861Q and G719S cells

Accordingly, no clear correlation was observed between

MIG6 expression and Iressa sensitivity in the eight cell

lines tested (Figs 6A and S1A) However, MIG6

expres-sion levels were uniquely correlated or anti-correlated

with the phosphorylation state of EGFR, Src homology

2 domain containing (SHC), mitogen-activated protein

kinase kinase (MEK) and extracellular signal-regulated

protein kinase (ERK) in the absence or presence of

EGF (Figs 6B and S1B) Interestingly, MIG6 expression

showed good correlation with basal phosphorylation

levels of EGFR (correlation coefficient = 0.61) and

with its direct effector protein SHC (correlation

coefficient = 0.75) in the absence of stimuli, and strong

anti-correlation (correlation coefficient =)0.83) with

ERK phosphorylation in the presence of stimuli These

results imply that increased MIG6 expression effectively

inhibits signal transduction to the downstream pathway

when EGFR is irregularly activated

Discussion

In the present study, we investigated the property of biological networks under various conditions related to EGFR kinase activity, which was altered by single amino acid mutation, activation by EGF and suppres-sion by Iressa Time-course microarray analysis enabled us to identify differentially expressed genes and obtain insight into the dynamic behavior of coor-dinated transcription associated with their upstream signaling pathways and functions

The L858R mutation of EGFR has been shown to

be a good predictive marker in terms of Iressa treat-ment [11,12] The data obtained in the present study showed that Iressa effectively suppressed EGF-induced expression of DUSP6 and ERRFI1 and, at the same time, increased the expression of ERBB2 and ERBB3 (i.e dimerization partners of EGFR) in L858R cells The regulatory pattern of these four genes suggests that the activation of EGFR or ErbB2-3 pathways is an

Fig 4 Direct EGFR regulator ERRFI1

(MIG6) is included in the Iressa responsive

MAPK and ErbB signaling-related gene list,

its protein expression (A) 52 MAPK and

ErbB signaling-related genes in 405 Iressa

responsive genes are shown Genes

involved in the EGFR ⁄ ErbB signaling

path-way are highlighted in blue Genes included

in the 405 gene group, which were

differen-tially expressed and where the expression

pattern was reversed by Iressa, are shown

in red Genes included in 2234 gene group,

but not in the 405 gene group, are depicted

in orange PG, PubMed and GeneRIF.

(B) MIG6 protein expression in EGF (10 n M )

or EGF + Iressa (10 l M ) stimulated H1299,

EGFR-WT and L858R as determined by

western blot analysis The experiment was

performed twice independently.

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immediate transcriptional effect of Iressa Given that

L858R cells are more sensitive to Iressa [27], inhibition

of EGFR kinase activity may lead to the activation of

alternative pathways that compensate for the loss of

EGFR pathway activity in L858R cells Indeed,

ERR-FI1demonstrated an anti-correlated expression pattern

with ERBB2 and ERBB3 in various tumors and cancer

cell lines [15,16], and higher expression levels of

recep-tor tyrosine kinase genes were observed in other

NSCLC cell lines showing high Iressa sensitivity (data

not shown) Thus, the inherited molecular fragility of

L858R in terms of Iressa sensitivity appeared to be

neutralized by transcriptional feedback

Although we initially speculated that MIG6

expres-sion was EGF-inducible, as was observed for ERRFI1

expression, this was not the case Rather, we found that

MIG6 expression was static and correlated with basal

phosphorylation levels of EGFR and SHC, and was

negatively correlated with EGF-stimulated

phosphory-lated ERK levels in H1299 cell lines The presence of

high levels of MIG6 expression might ensure, in the eight cell lines examined in the present study, that sig-nal transduction downstream of EGFR is disturbed However, further investigations are required to eluci-date the regulatory mechanism of MIG6 in relation to the EGFR mutation

The present study is the first to show the association

of MIG6 expression with the EGFR mutation in cancer MIG6⁄ RALT is known to be a transcriptional negative regulator of EGFR signaling [14] Ferby et al [24] also showed: (a) reduced expression of ERRFI1 in skin, breast, pancreatic and ovarian cancers, as well as psoriasis; (b) an inverse relationship between MIG6 expression and phosphorylated EGFR; and (c) an inverse correlation between ERRFI1 and ERBB3 mRNA levels in human melanoma cell lines Their results suggest that down-regulation of MIG6 in tumors and cancer cell lines leads to activation of ErbB signaling [24] Although the results obtained in the present study partially support those reported in

A

Fig 5 ERRFI1 and ErbB receptor family member expression in NCI-60 (A) ERRFI1 gene expression level in various cancer cell lines The dataset comprises nine different types of cancer, presented in different colors Vertical and horizontal axes represent cell line names and the gene expression level, respectively (B) Cluster analysis of ERRFI1 and ERBB expression in the NCI-60 dataset Prior to cluster analysis, the expression level of a gene was normalized so that the mean = 0 and SD = 1 Red and blue represent high and low normalized expression levels, respectively Color bars at the top of the heatmap represent the cancer type, with the same colors being used in the upper panel.

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earlier studies [24], our data clearly showed that MIG6

expression is correlated with the phosphorylated active

state of EGFR and that ERRFI1 expression is

associ-ated with basal EGFR kinase activity in the absence

of ligand Furthermore, MIG6 expression may be

indi-rectly (i.e not diindi-rectly) associated with EGFR or other

ERBB mRNA levels Among the ErbB receptor

fam-ily, the ErbB2 receptor is the most preferred binding

partner that leads to activation of EGFR kinase

[28,29] Thus, cells with distinct EGFR mutations have

their total signaling activity modulated at the

molecu-lar (kinase activity) and transcriptional levels, and

these modulations might compensate each other to

control the final cellular output at the systems level

Experimental procedures

Cell culture and RNA isolation

EGFR-mutated H1299 human lung cancer derivatives

were established as described previously [27] Cells were

maintained in RPMI medium supplemented with 10%

fetal bovine serum and 1 mm sodium pyruvate Prior to growth hormone treatment, cells were serum-starved for 16–24 h For EGFR kinase inhibition, Iressa (a generous gift from Astra Zeneca, London, UK) was added 20 min prior to growth hormone administration For the tran-scriptional analysis, cells were incubated with 10 nm EGF for 0.5, 1, 2, 4, 6 or 10 h and then washed twice with NaCl⁄ Pi Cells not treated with growth hormone were used as the control Cells were scraped using ice-cold NaCl⁄ Pi containing 10 lgÆmL)1 cycloheximide Total RNA was isolated using TRIzol reagent (Life Technolo-gies Corporation, Carlsbad, CA, USA) and then purified using the QIAGEN RNeasy Mini kit RNA quality was assessed using a Bioanalyzer (Agilent Technologies Inc., Santa Clara, CA, USA)

Western blot analysis Cells were treated with EGF in the absence or presence of Iressa for the indicated time period, washed three times with NaCl⁄ Pi, and then lysed using Bio-Plex lysis buffer (Bio-Rad laboratories, Hercules, CA, USA) The cell

B

Fig 5 Continued.

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A B

Fig 6 Comparison of MIG6 expression and phosphorylation of signaling molecules (A) MIG6 expression levels in eight H1299 derivative cell lines was compared with the Iressa sensitivity reported in a previous study [22] IC50values were extracted from fig 2b,c of the same study [22] and values < 0.02 were rounded to 0 (B) Basal MIG6 protein expression levels were compared with phosphorylation levels of EGFR, SHC, MEK and ERK in eight H1299 derivative cell lines in the absence (left) or presence (right) of EGF stimulation (5 min, 10 n M ) Protein expression and phosphorylation were measured by western blot analysis Western blot images are shown in Fig S1 Horizontal and vertical axes represent quantified signal intensities for MIG6 and signaling molecules (EGFR, SHC, MEK and ERK), respectively.

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