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Role of Lysocardiolipin Acyltransferase in Cigarette Smoke-Induced Lung Epithelial Cell Mitochondrial ROS, Mitochondrial Dynamics, and Apoptosis

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Abstract

Cigarette smoke is the primary cause of Chronic Obstructive Pulmonary Disorder (COPD). Cigarette smoke extract (CSE)-induced oxidative damage of the lungs results in mitochondrial dysfunction and apoptosis of epithelium. Mitochondrial cardiolipin (CL) present in the inner mitochondrial membrane plays an important role in mitochondrial function, wherein its fatty acid composition is regulated by lysocardiolipin acyltransferase (LYCAT). In this study, we investigated the role of LYCAT expression and activity in mitochondrial oxidative stress, mitochondrial dynamics, and lung epithelial cell apoptosis. LYCAT expression was increased in human lung specimens from smokers, and cigarette smoke-exposed-mouse lung tissues. Cigarette smoke extract (CSE) increased LYCAT mRNA levels and protein expression, modulated cardiolipin fatty acid composition, and enhanced mitochondrial fission in the bronchial epithelial cell line, BEAS-2B in vitro. Inhibition of LYCAT activity with a peptide mimetic, attenuated CSE-mediated mitochondrial (mt) reactive oxygen species (ROS), mitochondrial fragmentation, and apoptosis, while MitoTEMPO attenuated CSE-induced MitoROS, mitochondrial fission and apoptosis of BEAS-2B cells. Collectively, these findings suggest that increased LYCAT expression promotes MitoROS, mitochondrial dynamics and apoptosis of lung epithelial cells. Given the key role of LYCAT in mitochondrial cardiolipin remodeling and function, strategies aimed at inhibiting LYCAT activity and ROS may offer an innovative approach to minimize lung inflammation caused by cigarette smoke.

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All data presented and discussed are contained within the manuscript. All the data and materials are available from V.N.

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Acknowledgements

This work made use of the instrumentation provided by the Core Facility of the University of Illinois at Chicago’s Research Resources Center.

Author contributions

Conceptualization—M.B., V.N., and B.K.; methodology—M.B., V.S., P.F.U., V.N., R.R., L.H., and S.S.; formal analysis—M.B., R.R., S.M., P.V.S., and V.N.; investigation—M.B., V.N., B.K.; resources—V.N., B.K., S.P.R., and S.M.D.; writing—M.B., V.N., and R.R.; writing (review and editing)—B.M., R.R., and V.N.; project administration—V.N.; funding acquisition—V.N.

Funding

This work was supported by National Institutes of Health grants HLBI P01HL126609, P01HL060678, R01HL127342 (to V.N.). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

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Authors and Affiliations

  1. Departments of Bioengineering, University of Illinois at Chicago, Chicago, IL, USA

    Mounica Bandela

  2. Department of Orthopedic Surgery, Rush University Medical Center, Chicago, IL, USA

    Vidyani Suryadevara

  3. Departments of Pharmacology & Regenerative Medicine, University of Illinois at Chicago, Chicago, IL, USA

    Panfeng Fu, Long Shuang Huang, Ramaswamy Ramchandran & Viswanathan Natarajan

  4. The Affiliated Hospital of School of Medicine, Ningbo University, Ningbo, China

    Panfeng Fu

  5. Departments of Pediatrics, University of Illinois at Chicago, Chicago, IL, USA

    Sekhar P. Reddy

  6. Departments of Medicine, University of Illinois at Chicago, Chicago, IL, USA

    Kamesh Bikkavilli, Sugasini Dhavamani, Papasani V. Subbaiah, Sunit Singla, Steven M. Dudek & Viswanathan Natarajan

  7. Division of Allergy, Pulmonary, and Critical Care Medicine, Vanderbilt University School of Medicine, Nashville, TN, USA

    Lorraine B. Ware

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  1. Mounica Bandela
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Bandela, M., Suryadevara, V., Fu, P. et al. Role of Lysocardiolipin Acyltransferase in Cigarette Smoke-Induced Lung Epithelial Cell Mitochondrial ROS, Mitochondrial Dynamics, and Apoptosis. Cell Biochem Biophys 80, 203–216 (2022). https://doi.org/10.1007/s12013-021-01043-3

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