Inhibition of de novo fatty acid synthesis in Mycobacterium tuberculosis.
Emma K Roszkowski, Sarita Charap, Christine R Montague, Paridhi Sukheja, Case W McNamara, Paul S Soma, M Nurul Islam, Barbara Graham, Anna E Grzegorzewicz, Mary Jackson, Baiyuan Yang, Anthony G Hay, David G Russell, John T Belisle, Brian C VanderVen
Abstract
Open AccessDe novo fatty acid synthesis produces the acyl units needed to generate phospholipids, lipoproteins, enzyme prosthetic factors, polyketides, and mycolic acids in mycobacterium tuberculosis (Mtb). Here, we identified sALT629, a butoxyphenyl-tetrazole-acetamide compound that inhibits de novo lipid synthesis in Mtb. This compound disrupts the Mtb lipidome and prevents incorporation of metabolic tracers into acyl chains of Mtb lipids. Unexpectedly, we also found that sALT629 treatment significantly depleted triacylglycerol (TAG) pools as a metabolic compensation mechanism when de novo fatty acid synthesis was inhibited. Resistance to sALT629 was mediated by loss of function mutations in HadC, the non-essential hydroxyacyl- acyl carrier protein -dehydratase subunit involved in the synthesis of long-chain oxygenated mycolic acids. Inactivating HadC rescued sALT629-mediated inhibition by sustaining TAG pools to fulfill Mtb's biosynthetic demand for acyl chains. Lastly, loss of function HadC resistance mutations resulted in cell wall perturbations that confer fitness defects in vitro and in vivo suggesting that this specific resistance mechanism is unlikely to arise in Mtb in a clinical setting. Significance. Having effective antibiotics to treat tuberculosis underpins our ability to control this disease. The spread of antibiotic-resistant tuberculosis has prompted a need to identify new drug candidates with new mechanisms of action. Here we describe an antitubercular that targets de novo fatty acid synthesis in Mtb, a critical process required to generate multiple essential lipid and lipid-based factors in the bacteria. One resistance mechanism to this inhibitor is associated with perturbations to mycolic acid synthesis resulting in Mtb attenuation. These findings demonstrate that de novo fatty acid synthesis in Mtb is an actionable drug target, and uncovered a compensatory metabolic resistance network between TAGs and mycolic acids.