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n2:pmcid
PMC0
bibo:doi
10.1038%2Fnm.3667
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introduction
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Genomic alterations in the anaplastic lymphoma kinase (ALK) gene are found in numerous malignancies>>1<<. In a phase I trial, the ALK tyrosine kinase inhibitor (TKI), crizotinib, induced an objective radiographic response (ORR) of 60.8% and a median progression-free survival of 9.7 months2.
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Analysis of ‘exceptional responders’ has revealed important insights into drug sensitivity>>7<<. We describe a patient with ALK+ lung cancer who had an ‘exceptional response’ to an IGF-1R inhibitor prior to ALK TKI therapy.
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results
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Previous studies have reported a 0% response rate for ALK+ lung cancer patients treated with erlotinib alone>>8<<. Thus, we hypothesized that in this patient, either the combination of erlotinib plus the IGF-1R inhibitor was synergistic against ALK+ lung cancer, or the IGF-1R inhibitor alone was somehow responsible for the tumor response.
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The combination of crizotinib plus OSI-906 was confirmed to be synergistic using the Mix-Low method>>9<< (Supplementary Fig.
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OSI-906 has no off-target activity against ALK at the doses used in these experiments>>10<<.
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IRS-1 is a well-known substrate and adaptor protein for IGF-1R>>11<<, and IRS-1 has been demonstrated to be a primary adaptor for PI3K activation in H3122 cells12.
n2:mentions
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_:vb33942546
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IRS-1 is a well-known substrate and adaptor protein for IGF-1R11, and IRS-1 has been demonstrated to be a primary adaptor for PI3K activation in H3122 cells>>12<<. However, the precise mechanism whereby ALK fusion proteins link to effector pathways remains undefined. We observed that IRS-1 levels decreased with crizotinib treatment (Fig. 3b). Using lysates from H3122 cells, we found that ALK and
n2:mentions
n3:21775521
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_:vb33942547
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We also validated that this interaction occurs in vivo using tissue from two different EML4-ALK E13;A20 transgenic mice>>13<< (Fig. 3d).
n2:mentions
n3:20952506
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_:vb33942548
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4b), a more potent and more specific ALK inhibitor>>14<<. Notably, a derivative of X-376 (X-396) is currently in phase I clinical trials (NCT01625234).
n2:mentions
n3:21613408
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_:vb33942549
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4a,b), as previously described>>15<<. These cells did not have any ‘second-site’ ALK kinase domain mutations (data not shown).
n2:mentions
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IGFBP3 is known to block IGF-1 induced activation of IGF-1R>>16<<,17. Overall, these studies show that the IGF-1R signaling pathway is activated by multiple mechanisms in H3122 XR cells.
n2:mentions
n3:18568074
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IGFBP3 is known to block IGF-1 induced activation of IGF-1R16,>>17<<. Overall, these studies show that the IGF-1R signaling pathway is activated by multiple mechanisms in H3122 XR cells.
n2:mentions
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Apoptosis was also enhanced in H3122 XR cells treated with X-376 and the IGF-1R TKI, AEW->>54118<< (Fig. 4f). In accord with these data, combination treatment with ALK and IGF-1R inhibitors in H3122 XR cells inhibited AKT phosphorylation to a greater extent than either inhibitor alone (Fig. 4g). The addition of OSI-906 also partially
n2:mentions
n3:15050915
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Previous studies have suggested that the IGF-1R pathway can drive EGFR inhibitor resistance>>19<<,20. We tested the efficacy of combined EGFR/IGF-1R inhibition in 4 different isogenic pairs of EGFR TKI- sensitive and -resistant cell lines21,22 (Supplementary Table 4).
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Previous studies have suggested that the IGF-1R pathway can drive EGFR inhibitor resistance19,>>20<<. We tested the efficacy of combined EGFR/IGF-1R inhibition in 4 different isogenic pairs of EGFR TKI- sensitive and -resistant cell lines21,22 (Supplementary Table 4).
n2:mentions
n3:23994953
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We tested the efficacy of combined EGFR/IGF-1R inhibition in 4 different isogenic pairs of EGFR TKI- sensitive and -resistant cell lines21,>>22<< (Supplementary Table 4).
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As an orthogonal approach, we performed mRNA expression analysis for IGF-1R and IRS-1 using Nanostring>>23<< on matched patient samples and on isogenic pairs of ALK TKI-sensitive and resistant cell lines.
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The second-generation ALK TKI, LDK-378 (ceritinib), has demonstrated a 56% ORR in patients with ALK+ lung cancer who have progressed on crizotinib>>24<<. Yet, only a minority of patients had ALK alterations, suggesting the possibility of alternative ‘bypass’ mechanisms which are sensitive to LDK-378.
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Interestingly, LDK-378 and the structurally related ALK inhibitor, TAE-684, can inhibit both ALK and IGF-1R in vitro>>25<<. We hypothesized that the efficacy of LDK-378 may be due to this drug's ability to simultaneously block both ALK and IGF-1R. LDK-378 was more potent than crizotinib in H3122 (Fig. 6a), STE-1 (Supplementary Fig. 7a), and H3122 XR cells
n2:mentions
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n6:Section
dc:title
discussion
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Our data may also in part explain the surprising 56% ORR for the ‘second generation’ ALK TKI, LDK-378, in patients with ALK+ lung cancer who had progressed on crizotinib>>24<<. Since responses to LDK-378 were observed in both patients with and without ‘second-site’ ALK mutations, the increased ‘on-target’ potency of LDK-378 towards ALK is alone not enough to explain all of the responses seen to this agent. We
n2:mentions
n3:24670165
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n6:Section
dc:title
online methods
n6:contains
_:vb33942562 _:vb33942563 _:vb33942564 _:vb33942565 _:vb33942566 _:vb33942567 _:vb33942568 _:vb33942569 _:vb33942570 _:vb33942571 _:vb33942572 _:vb33942573
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The human lung adenocarcinoma cell lines H3122 and H2228 have been described previously and were verified to harbor their reported genetic alterations by direct cDNA sequencing>>14<<. Derivation of the human lung adenocarcinoma cell line, STE-1, is described below. The human anaplastic lymphoma cell line, SUDHL-1, has been previously described26. The isogenic pairs of EGFR TKI sensitive and EGFR TKI resistant cell
n2:mentions
n3:21613408
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_:vb33942563
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The human anaplastic lymphoma cell line, SUDHL-1, has been previously described>>26<<. The isogenic pairs of EGFR TKI sensitive and EGFR TKI resistant cell lines used in these studies, including PC-9/PC-9 ERc1, HCC4006/HCC4006 ER, HCC827/HCC827 ER, and HCC2279/HCC2279 ER, have been previously described21,22. The EGFR TKI
n2:mentions
n3:8122112
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The isogenic pairs of EGFR TKI sensitive and EGFR TKI resistant cell lines used in these studies, including PC-9/PC-9 ERc1, HCC4006/HCC4006 ER, HCC827/HCC827 ER, and HCC2279/HCC2279 ER, have been previously described21,>>22<<. The EGFR TKI resistant cells (denoted ‘ER’ for Erlotinib Resistant) were continuously grown in 1 μM erlotinib. All cell lines were maintained in RPMI 1640 medium (Mediatech, Inc., Manassas, VA, USA) supplemented with 10% heat inactivated
n2:mentions
n3:22773810
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The reads were aligned to the Human Genome (UCSC hg19) using BWA>>27<<. The default arguments of BWA were applied to the alignment.
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n3:19451168
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After the alignment, we ran the software SAMtools >>28<< to convert the alignment files to a sorted, indexed binary alignment map (BAM) format.
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n3:19505943
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To obtain the best call set possible, we also used the software GATK>>29<< to do realignment and recalibration.
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n3:20644199
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X-376 was prepared as described previously>>14<<. Crizotinib (ChemieTek, Indianapolis, IN, USA), OSI-906 (Selleck Chemicals, Houston, TX, USA), AEW-541 (Selleck Chemicals, Houston, TX, USA), LDK-378 (Selleck Chemicals, Houston, TX, USA) and Lapatinib (Selleck Chemicals, Houston, TX,
n2:mentions
n3:21613408
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_:vb33942569
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Drug synergism was assessed using the Mix-Low method>>9<<. For soft agar assays, cells were seeded in 96 well plates and treated with drug according to the manufacturer's instructions (Cell Biolabs, Inc., San Diego, CA, USA).
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n3:17768754
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_:vb33942570
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NanoString nCounter analysis of RNA isolated from formalin-fixed and paraffin embedded (FFPE) samples was performed as previously described>>23<<. The raw data were normalized to the nCounter system spike-in positive and negative controls in each sample.
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n3:23052255
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For analysis, the sample probe profile data in the GeneSpring export format was transformed to log-2 scale and normalized using quantile method by applying beadarray package>>31<< in BioConductor 2.11.
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n3:17586828
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Genetically engineered mice harboring the EML4-ALK E13;A20 fusion variant has been previously reported>>13<<. Three month old mice from both genders were used in the described studies. All animal treatment studies were reviewed and approved by the IACUC at the Dana-Farber Cancer Institute.
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For the index patient's tumor, clinical genotyping was performed using the SNaPshot platform as previously described>>32<<.
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