Many types of cancer now have 'targeted treatments', which specifically home in on genes cancer cells rely on for survival. But there are very few of these treatments available for the most common type of mouth cancer, oral squamous cell carcinoma, which around 350,000 people are diagnosed with each year.

Designing targeted treatments relies on detailed knowledge of the genetic makeup of the cancer cells. But, little is known about which genes drive oral squamous cell carcinoma, especially among patients living in Asia, which is where over half of yearly cases are diagnosed. One way to resolve this is to use gene editing technology to find the genes that the cancer cells need to survive.

Now, Chai et al. have used a gene editing tool known as CRISPR to examine 21 cell lines from patients diagnosed with oral squamous cell carcinoma. Most of these lines were from Asian patients, some of whom had a history of chewing betel quid which increases the risk of mouth cancer. By individually inactivating genes in these cell lines one by one, Chai et al. were able to identify 918 genes linked to the survival of the cancer cells. Some of these genes have already been associated with the spread of other types of cancer, whereas others are completely unique to oral squamous cell carcinoma. The screen also discovered that some cell lines could not survive without genes involved in a signalling pathway called Hippo, which is known to contribute to the progression of many other types of cancer.

Uncovering the genes associated with oral squamous cell carcinoma opens the way for the development of new targeted treatments. Targeted therapies already exist for some of the genes identified in this study, and it may be possible to repurpose them as a treatment for this widespread mouth cancer. But, given that different cell lines relied on different genes to survive, the next step will be to identify which genes to inactivate in each patient.

Head and neck squamous cell carcinoma (HNSCC) is a heterogeneous tumor arising from the mucosal surfaces lining the upper aerodigestive tract. The commonest subtype, oral squamous cell carcinoma (OSCC) is especially prevalent among Asian countries (Bray et al., 2018). OSCC has been associated with distinct risk habits such as betel quid chewing, tobacco smoking and alcohol consumption (Shield et al., 2017). The 5-year survival rate for OSCC is about 50% (Kumar et al., 2016) and surgery remains the mainstay of treatment. Cetuximab, an inhibitor of the epidermal growth factor receptor (EGFR), is used in combination with platinum-based chemotherapy for the treatment of advanced OSCC (Vermorken et al., 2008). However, the improvement in survival remains marginal (Vermorken et al., 2008). More recently, immune checkpoint inhibitors have been approved for the treatment of advanced and metastatic OSCC (Cohen et al., 2019). Although an improvement in patients’ outcome is anticipated with the advancement of immunotherapy, clinical trial outcomes showed an average objective response rate of only 13–36% (Bauml et al., 2017; Burtness et al., 2019; Ferris et al., 2016), and the factors determining response towards checkpoint inhibitors are still largely unknown. This underscores the need to identify further therapeutic targets for OSCC.

Genomic sequencing technology has enabled the delineation of the comprehensive mutational and transcriptomic landscape of cancers, including OSCC (The Cancer Genome Atlas Network, 2015; Pickering et al., 2013). However, the functional significance of most of these genetic alterations remains unclear and little is known about their value as therapeutic targets for OSCC. Identifying the genetic dependencies of OSCC will, therefore, be critical for the development of novel therapies. Genome-scale functional genetic screens allow the high-throughput identification of genes that govern cell survival (Gerhards and Rottenberg, 2018). Previously, such genes were identified using RNA interference (RNAi) technology (McDonald et al., 2017; Tsherniak et al., 2017). More recently, essential genes have been identified through the use of CRISPR-Cas9 technology due to its high specificity and efficiency compared to RNAi (Gerhards and Rottenberg, 2018). Several studies using genome-wide CRISPR-Cas9 screen have already shown promising outcome in identifying novel cancer-specific vulnerabilities that are useful drug targets (Steinhart et al., 2017; Wang et al., 2017), as well as improving the understanding of drug mechanism of action (Barazas et al., 2018; Hou et al., 2017).

The Cancer Dependency Map project (a consortium effort by the Wellcome Sanger Institute and the Broad Institute) have conducted CRISPR-Cas9 screen on a large number of cell lines including some OSCC models (Behan et al., 2019; Meyers et al., 2017). However, there is a lack of representation of Asians OSCC, such as those associated with betel quid chewing habit, one of the major risk factors of OSCC in many Asian countries (Shield et al., 2017). Further, the comparison of genomics data across different populations has revealed distinctive features in the different populations (Chai et al., 2020).

To identify genetic vulnerabilities in OSCC, we performed genome-wide CRISPR-Cas9 screens on 21 highly annotated OSCC cell lines, most of which are unique models derived from Asian patients (Fadlullah et al., 2016). Our study contributes to approximately one-third of the OSCC functional genetic screens currently available globally, expanding the representation of this heterogeneous disease (Behan et al., 2019; Meyers et al., 2017). In addition to finding known genetic vulnerabilities, we also uncover novel candidate genes essential for OSCC survival that can facilitate the development of new targeted therapies for OSCC. We validated the essentiality of Yes-associated protein 1 (YAP1) and WW domain-containing transcription regulator protein 1 (WWTR1) and revealed mutually exclusive dependency and compensable functions of these paralogs in different subsets of OSCC models. We identified OSCC tumors with a gene expression signature similar to cell lines with validated dependencies. Among which, OSCC resembling the WWTR1-dependent cell lines showed significant enrichment of immune-related pathways and are associated with biomarkers of response towards checkpoint inhibitors. In summary, our study demonstrated the robustness of genome-wide CRISPR-Cas9 screen in identifying genetic vulnerabilities in diverse OSCC models, offering new molecular insights into this disease.

New therapeutic targets are urgently needed for the development of OSCC treatment. However, genomics studies have shown that oncogenic mutations in OSCC are largely limited to PIK3CA and HRAS and even in these, mutations are only found in a small subset of patients. Therefore, determining the oncogenic pathways and specific therapeutic targets have not been straight forward for this disease. We performed genome-wide CRISPR-Cas9 screens in a unique collection of OSCC cell lines derived from patients with diverse risk habits to identify genetic vulnerabilities that can serve as a basis for further therapeutic development for OSCC. Adding to existing genomics datasets in OSCC, this approach identifies fitness genes required for the survival of cancer cells where targeting these will result in the killing of these cells. The majority of the cell lines used in this study were from Asian patients where OSCC is more prevalent, and where causative factors include betel quid chewing in addition to smoking that is more often found in Caucasian patients (Cheong et al., 2017; Kumar et al., 2016). The molecular drivers of these patients are under-characterized as genomics data on Asian patients remain limited (India Project Team of the International Cancer Genome Consortium, 2013; Su et al., 2017).

Here, we identified 918 fitness genes in OSCC. Pathway enrichment analysis revealed that these genes were highly associated with diverse cancers pathways, confirming the robustness of our screen and pipeline in identifying targetable genetic dependencies. These included known candidate genes that are already being investigated in clinical trials for OSCC or other cancers such as CDK6, PIK3CA, and FGFR1, as well as novel genes that are yet to be explored as therapeutic targets, including those within the oxidative stress pathway (KEAP1, NFE2L2). Notably, we showed that about 5% (45/918) of these genes are highly tractable with approved drugs, or have drugs that are in late-stage of clinical testing, demonstrating that these screens could help to prioritize drugs that could be repurposed for OSCC treatment. We compared our screens with previous genome-wide RNAi screens and found that candidate genes such as those relating to the cell cycle (CKAP5, KPNB1, RAN, TPX2, and KIF11) were also identified in our dataset (Martens-de Kemp et al., 2013). However, due to stringent filtering of core-fitness genes (Behan et al., 2019; Hart et al., 2014; Hart et al., 2017; Meyers et al., 2017), these were no longer within the list of OSCC non-core fitness genes.

Notably, the unique inclusion of several Asian OSCC models known to be associated with betel-quid chewing in our screen enabled us to identify that the NF-kB signaling pathway is among one of the most significantly enriched dependencies among betel-quid associated OSCC compared to cancers not associated with this risk habit. This finding is in line with the past studies reporting direct activation of the NF-kB signaling, upon treatment of OSCC cell lines with the extract of areca nut which is the main component in the betel quid (Chiang et al., 2008; Lin et al., 2005). By contrast, members of this signaling pathway (TRIM25, NFKB2, TNFAIP3) did not seem to be fitness genes in the other cell lines not associated with betel quid chewing, nor those from the Project Score or DepMap (Behan et al., 2019; Meyers et al., 2017). Members of the NF-kB signaling pathways have been proposed as therapeutic targets for inflammatory diseases and cancers, with various types of inhibitors being developed. In the event of the development of NF-kB inhibitosr with promising clinical utililty in the future, it would be of interest to investigate if increase efficacy of this inhibitor would be seen among the betel-quid-associated OSCC. Appreciating this differences in dependencies in Asian OSCC that remains undiscovered in existing large genetic screens could have significant implications, especially when employing precision medicine in the different populations. We acknowledge, however, that further in-depth investigations including a larger sample size and further representative models, are needed in order to confirm our findings and to inform the basis of developing potential targeted therapy against the unique vulnerabilities among the Asian OSCC.

Driver mutations are often expected to be robust biomarkers in precision medicine. However, upon analysing the dependency profiles on cancer genes that are commonly mutated in HNSCC and those with driver mutations among our 21 OSCC cell lines, we show that with the exception of some genes with driver mutations leading to oncogene addiction (PIK3CA, HRAS and NFE2L2), most other driver mutations did not confer preferential gene dependency and their value as a drug target remains unclear.

Given the propensity of copy number alterations in driving OSCC, a ‘C’ class tumor (The Cancer Genome Atlas Network, 2015; Ciriello et al., 2013), we investigated the commonly amplified genomic regions to look for functionally important candidate genes. One of the pathways that was significantly enriched was the Hippo pathway. Within this pathway, we focused our analyses on YAP1 and WWTR1, two paralogs that show differential dependency pattern in our 21 OSCC cell lines. Copy number amplifications of 11q22 and 3q25 (where YAP1 and WWTR1 are located, respectively) are common events reported in OSCC, often in mutual exclusive manner (Campbell et al., 2018; Wang et al., 2018). These two genes are the major effectors negatively regulated by the Hippo pathway that is increasingly reported to play multiple roles in carcinogenesis, as reviewed comprehensively in recent years (Dey et al., 2020; Santos-de-Frutos et al., 2019). However, the majority of the studies focused on either one of the paralogs or had assumed similar functions between paralogs (Santos-de-Frutos et al., 2019; Zanconato et al., 2016). Emerging evidence demonstrate that YAP1 and WWTR1 have distinct roles where they partner with different transcription factors, drive different downstream effectors and also modulate the tumor microenvironment distinctively (Callus et al., 2019; Janse van Rensburg et al., 2018; Kaan et al., 2017; Plouffe et al., 2018). Our study revealed the intricate dominance of dependency on either one of the paralogs, despite the other not being deleted or loss. More intriguingly, the subset of lines thought not to be dependent on either YAP1 or WWTR1, were actually lines where the remaining paralog is able to compensate for the lost paralog, therefore, enabling the cells to continue surviving.

In the context of OSCC/HNSCC, studies demonstrating the distinct roles and regulatory mechanism of YAP1 and WWTR1 are emerging. Analysis of genome-wide transcriptional changes upon knockdown of YAP1 or WWTR1 in OSCC showed that YAP1 had a more prominent role in transcriptional regulation (Hiemer et al., 2015). Using a tongue orthotopic mouse model with the deletion of MOB1A/B, Omori et al., 2020 provided strong evidence that YAP1 acted as a strong driver in OSCC tumor initiation and progression, whereby WWTR1 did not seems to play an equivalent role (Omori et al., 2020). The differences between YAP1 and WWTR1 can also be further exemplified in terms of their interaction with upstream/downstream pathways, that would involve other frequently co-amplified genes such as PIK3CA, TP63, and SOX2. The co-occurrence of amplifications in these genes that are part of the extended signaling network of the Hippo pathway underscores the critical role of the Hippo pathway in driving the OSCC tumorigenesis. Overexpression of PIK3CA was shown to be correlated with YAP1 activation and associated with poor clinical outcome (García-Escudero et al., 2018). Further, the activation of the PI3K through mitogenic signaling inhibits the Hippo pathway leading to YAP1 activation and cell growth (Fan et al., 2013). On the other hand, WWTR1 was shown to act upstream of SOX2, facilitating stemnesses in HNSCC (Li et al., 2019). Intriguingly, while WWTR1 knockdown led to reduction of SOX2 mRNA and protein expression, this was not seen when YAP1 was knockdown in the HNSCC cells (Cal27 and Fadu) (Li et al., 2019; Huang et al., 2017). In support of that, an inverse relationship between the expression levels of YAP1 and ΔNp63 were reported in lung SCC tumor samples (Huang et al., 2017). However, this was not seen in HNSCC tumor samples and cell lines (Ge et al., 2011), suggesting a cancer/context-specific regulatory mechanism might be in place. Consistent with the oncogenic roles of YAP1 reported in OSCC (Hiemer et al., 2015; Omori et al., 2020), another study showed that p63, together with the co-expressing chromotin remodeling factor, ACTL6A, can drive YAP1 activation, suppressing differentiation and promoting cell proliferation in HNSCC (Saladi et al., 2017). Similar observations between WWTR1 and TP63 have not been reported thus far. Hence, understanding the context in which the OSCC lines can be either YAP1-dependent/WWTR1-dependent or having compensable YAP1/WWTR1 is important, as YAP1 and WWTR1-dependency appear to be associated with the enrichment of distinct pathways. Current inhibitors of YAP1 such as verteporfin and CA3 that blocks its interactions with the TEAD transcription factors also targets WWTR1 (Song et al., 2018; Zhang et al., 2015); therefore, this data underscores the need to develop more specific inhibitors to prevent the targeting of many different downstream pathways. Intriguingly, we also observed enrichment of PIK3CA mutant (p=0.0003) among OSCC lines that are compensable for YAP1 or WWTR1. As recent studies have provided evidence that YAP1 and WWTR1 could mediate mutant PIK3CA-induced tumorigenesis (Zhao et al., 2018) andother studies also suggested crosstalk between these Hippo pathway effectors with the PI3K-Akt pathway (García-Escudero et al., 2018), confirmatory and mechanistic studies will be needed to delineate why YAP1 and WWTR1 function can be compensated in these PIK3CA-mutated cell lines, while distinct dependencies on either paralog are observed in PIK3CA wild-type lines. The functional loss of mutated FAT1 has also been reported to be associated with YAP1 activation in head and neck cancer (Martin et al., 2018), however, no enrichment of FAT1 mutation was seen among the YAP1-dependent nor WWTR1-dependent models in this study.

We also provided tissue-relevant insights of our findings by including analysis of the OSCC tumors from TCGA. Since YAP1 and WWTR1 are transcription co-factors that could regulate a plethora of gene transcriptions, we devised an analysis workflow utilizing the DEGs among the three subsets of OSCC models. We have identified 105 OSCC tumors that show highly similar gene expression signature as the cell lines, which are predicted to share the same dependency pattern. Similarly, comparison of the OSCC tumors based on their gene signatures revealed significant differences in terms of their enriched gene sets and immune signatures. As checkpoint blockade is approved for the treatment of recurrent and metastatic OSCC, understanding how YAP1 and WWTR1 influence the immune microenvironment could provide clues on the combination therapies that could increase the subset of patients responding checkpoint inhibitors. In particular, OSCC with high WWTR1 dependency signature score are significantly associated with various biomarkers that were predicted to show good response toward checkpoint inhibitors. This finding is consistent with the recent discovery that constitutively active WWTR1 induces PD-L1 expression, to a greater extent than YAP1 (Janse van Rensburg et al., 2018), and that tumors with YAP1 amplifications have low T-cell infiltration (Saloura et al., 2019). These observations have clinical implication as anti-PD1 is an approved therapy for HNSCC and therefore, further investigation and validation will be needed to confirm this observation and its clinical impact. While many companies are developing novel inhibitors targeting YAP1-TEAD transcriptional activity, which should be effective against all other OSCC, combination with checkpoint inhibitor could be considered for those OSCC with WWTR1 dependency signatures. We acknowledge, however, that whilst the dependency observed in cell lines could be recapitulated in OSCC, OSCC tissues would be much more heterogenous and could harbor specific genetic abrogations that could be the dominant driver of tumorigenesis. Therefore, further validation of the association between WWTR1-dependency signature and response to checkpoint inhibitors should be validated particularly in the context of clinical trials involving checkpoint inhibitors.

The roles of the Hippo signaling pathway and its effectors YAP1 and WWTR1 in cancer immunity remains unclear. The inactivation of the Hippo pathway through the loss of LATS1/2 was reported to cause the induction of anti-tumor immune response and inhibition of HNSCC tumor growth, via the hyperactivation of YAP1/WWTR1 (Barth et al., 2013; Moroishi et al., 2016). This demonstrates that components of the Hippo signaling pathway could also modulate the host tumor microenvironment in addition to what we have demonstrsated in cancer cells. The design and models used in our study have not been set up to examine this where the inherent limitation of using cell lines do not consider the components of the tumor microenvironment in the in vitro screening. Nonetheless, our findings provided a novel insight linking the intricate dependency on YAP1 and WWTR1 with differential state of the immune microenvironment in OSCC which warrants further investigation with the use of immune-competent mouse models, before further clinical evaluation can be made.

In summary, our study is the first large-scale CRISPR-Cas9 screen and focused analysis conducted on large panels of Asian derived OSCC cell lines and provided a cancer-specific overview of the fitness genes landscape, affording opportunities for further therapeutic targets development. The ability to scrutinize the functional genomics of these fitness genes/pathways to a greater detail was also exemplified in this study.

All main data generated or analysed during this study are included in the manuscript and supplementary files. Source data files for each figures and supplements have also been provided. The larger datasets of CRISPR screens, WES and RNA-sequencing output are available from Figshare (https://doi.org/10.6084/m9.figshare.11919753).

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