top of page

 

Unravel the mechanisms linking alteration of the heme-oxidative stress pathway to lung tumor development and progression

 

In cancers, heme signaling can be deregulated through alteration of the oxidative stress homeostasis. Oxidative stress is induced by elevated intracellular levels of reactive oxygen species (ROS). ROS play pleiotropic roles in tumorigenesis; while ROS are pro-tumorigenic, high ROS levels are cytotoxic. Cancer cells exhibit aberrant redox homeostasis that allows them to thrive under conditions of high oxidative burden. Specifically, hyperproliferation of tumor cells is accompanied by high ROS production, however, cancer cells accommodate high ROS levels by increasing their antioxidant status to optimize ROS-driven proliferation, while at the same time avoiding ROS thresholds that would trigger senescence and apoptosis.

To maintain oxidative homeostasis and sustain tumor growth, ~30% of non-small cell lung cancers (NSCLCs) increase the transcription of antioxidant genes by acquiring either stabilizing mutations in the transcription factor NRF2 (the NFE2L2 gene product) or by selecting for Loss-of-Function (LOF) mutations in its negative regulator, KEAP1. NRF2 increases the cells antioxidant defense by upregulating, among the others, genes involved in glutathione and NADPH metabolism as well as genes involved in the maintenance of signaling heme homeostasis. Excess of signaling heme is cytotoxic since it catalyzes the formation of ROS through Fenton reaction, resulting in oxidative stress. In turn, oxidative stress elicits heme release from heme-binding proteins, thus amplifying heme toxicity. NRF2 avoids the self-amplifying, pro-oxidant effects of signaling heme by inducing the transcription of genes regulating heme homeostasis, among which heme-oxygenase-1 (HO-1), the enzyme degrading signaling heme.

 

Using CRISPR/Cas9 in KP (KRASG12D; p53-/-) GEMM (i.e., genetically engineered mouse model), we recently discovered that LOF mutations of KEAP1 in NSCLC promote tumor progression via alteration of the heme signaling. Our findings contributed to identify novel vulnerabilities in lung cancer patients harboring alteration of the KEAP1/NRF2 pathway, and demonstrated that drugs targeting the heme pathway can be effectively used as therapeutics to inhibit the progression of these cancers. However, given that the heme signaling potentially targets multiple cellular pathways, effectors and substrates, the role of heme pathway in these cancers remains to be defined.

Today, our laboratory aims to achieve a deep understanding of the mechanisms linking alterations of the heme signaling to cancer development, and, in particular, to KEAP1/NRF2 mutant lung tumors pathogenesis. Our ultimate goal is to identify genotype-specific cancer vulnerabilities which may pave the road for the design of new personalized genotype-based therapies.

To pursue our goals, we focus on:

 

1. Understanding how KEAP1/NRF2 mutations in lung cancer impact on the heme-UPS regulated protein degradation. For our analyses, we use orthogonal approaches combining biochemistry, proteomics and mouse genetics to identify the heme-UPS substrates which are deregulated in cancer and to determine their role in the mechanisms of tumorigenesis. 

 

2.  Investigating how alteration of heme-BACH1 impacts on the biology of KEAP1/NRF2 mutant lung cancer models harboring mutations in additional signaling pathways that frequently co-occur in patients. To replicate these specific lung cancer patient genotypes, we use CRISPR/Cas9. Currently, we are generating lung cancer models harboring mutations in the oncogene KRAS and on the tumor suppressor LKB1; these two genes are mutated in ~30% (for KRAS) and ~45% (for LKB1) of the lung cancer patients with KEAP1 lesions, respectively. We use genomic approaches to identify the targets of the heme-BACH1 pathway in these tumor models, and molecular biology together with mouse genetics to understand how alteration of these targets influence tumor evolution.

 

bottom of page