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CCAAT/enhancer-binding protein beta (C/EBPβ) knockdown reduces inflammation, ER stress, and apoptosis, and promotes autophagy in oxLDL-treated RAW264.7 macrophage cells

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Abstract

Atherosclerosis is associated with deregulated cholesterol metabolism and formation of macrophage foam cells. CCAAT/enhancer-binding protein beta (C/EBPβ) is a transcription factor, and its inhibition has recently been shown to prevent atherosclerosis development and foam cell formation. However, whether C/EBPβ regulates inflammation, endoplasmic reticulum (ER) stress, and apoptosis, in macrophage foam cells and its underlying molecular mechanism remains unknown. Here, we investigated the effect of C/EBPβ knockdown on proteins and genes implicated in inflammation, ER stress, apoptosis, and autophagy in macrophage foam cells. RAW264.7 macrophage cells were transfected with control and C/EBPβ-siRNA and then treated with nLDL and oxLDL. Key proteins and genes involved in inflammation, ER stress, apoptosis, and autophagy were analyzed by western blot and qPCR. We found that short interfering RNA (siRNA)-mediated knockdown of C/EBPβ attenuated atherogenic lipid-mediated induction of proteins and genes implicated in inflammation (P-NFkB-p65, NFkB-p65, and TNFα), ER stress (ATF4 and ATF6), and apoptosis (CHOP, caspase 1, 3, and 12). Interestingly, C/EBPβ knockdown upregulated the expression of autophagy proteins (LC3A/B-II, ATG5) and genes (LC3B, ATG5) but decreased the mammalian target of rapamycin (mTOR) protein phosphorylation and mTORC1 gene expression in oxLDL-loaded RAW264.7 macrophage cells. More importantly, treatment with rapamycin (inhibitor of mTOR) increased expression of proteins implicated in autophagy and cholesterol efflux in oxLDL-loaded RAW 264.7 macrophage cells. The present results suggest that C/EBPβ inactivation regulates macrophage foam cell formation in atherogenesis by reducing inflammation, ER stress, and apoptosis and by promoting autophagy and inactivating mTOR.

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Abbreviations

C/EBPβ:

CCAAT/enhancer-binding protein beta

ERS:

Endoplasmic reticulum stress

ATG5:

Autophagy gene 5

ATF4:

Activating transcription factor 4

ATF6:

Activating transcription factor 6

LC3-I & II:

Microtubule-associated protein 1 light chain 3-I & II

CHOP:

CCAAT/enhancer-binding protein (C/EBP) homologous protein

mTOR:

Mammalian target of rapamycin

mTORC1:

mTOR complex 1

mTORC2:

mTOR complex 2

ox-LDL:

Oxidized low-density lipoproteins

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Acknowledgements

This research was funded by the American Heart Association (AHA) Beginning Grant In Aid and the Startup Fund (Texas Tech University), USA to SMR.

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Authors and Affiliations

  1. Department of Nutritional Sciences & Obesity Research Institute, Texas Tech University, Lubbock, TX, 79409-1270, USA

    MD Khurshidul Zahid, Michael Rogowski, Naima Moustaid-Moussa & Shaikh M. Rahman

  2. Department of Mathematics, Texas Tech University, Lubbock, TX, 79409-1270, USA

    Christopher Ponce

  3. Department of Pharmaceutical Sciences, Irma Lerma Rangel College of Pharmacy, Texas A&M, Health Sciences Center, College Station, TX, 78363, USA

    Mahua Choudhury

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  1. MD Khurshidul Zahid
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Contributions

SMR designed and supervised the research. MKZ, MR, and CP performed the experiments. MKZ, CP, and SMR analyzed the data. MKZ and SMR wrote the manuscript. MC, NMM, MR and SMR revised the manuscript. All authors read and approved the final manuscript.

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Correspondence to Shaikh M. Rahman.

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Zahid, M.K., Rogowski, M., Ponce, C. et al. CCAAT/enhancer-binding protein beta (C/EBPβ) knockdown reduces inflammation, ER stress, and apoptosis, and promotes autophagy in oxLDL-treated RAW264.7 macrophage cells. Mol Cell Biochem 463, 211–223 (2020). https://doi.org/10.1007/s11010-019-03642-4

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