Restoration of Mal overcomes the defects of apoptosis in lung cancer cells


Autoři: Li-Tao Yang aff001;  Fei Ma aff001;  Hao-Tao Zeng aff001;  Miao Zhao aff001;  Xian-Hai Zeng aff001;  Zhi-Qiang Liu aff001;  Ping-Chang Yang aff001
Působiště autorů: ENT Institute, Research Center of Allergy & Immunology, Shenzhen University School of Medicine, Shenzhen, China aff001;  Guangdong Provincial Key Laboratory of Regional Immunity and Diseases, Shenzhen, China aff002
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: 10.1371/journal.pone.0227634

Souhrn

Background and aims

Cancer is one of the life-threatening diseases of human beings; the pathogenesis of cancer remains to be further investigated. Toll like receptor (TLR) activities are involved in the apoptosis regulation. This study aims to elucidate the role of Mal (MyD88-adapter-like) molecule in the apoptosis regulation of lung cancer (LC) cells.

Methods

The LC tissues were collected from LC patients. LC cells and normal control (NC) cells were isolated from the tissues and analyzed by pertinent biochemical and immunological approaches.

Results

We found that fewer apoptotic LC cells were induced by cisplatin in the culture as compared to NC cells. The expression of Fas ligand (FasL) was lower in LC cells than that in NC cells. FasL mRNA levels declined spontaneously in LC cells. A complex of FasL/TDP-43 was detected in LC cells. LC cells expressed less Mal than NC cells. Activation of Mal by lipopolysaccharide (LPS) increased TDP-43 expression in LC cells. TDP-43 formed a complex with FasL mRNA to prevent FasL mRNA from decay. Reconstitution of Mal or TDP-43 restored the sensitiveness of LC cells to apoptotic inducers.

Conclusions

LC cells express low Mal levels that contributes to FasL mRNA decay through impairing TDP-43 expression. Reconstitution of Mal restores sensitiveness of LC cells to apoptosis inducers that may be a novel therapeutic approach for LC treatment.

Klíčová slova:

Apoptosis – Cancer treatment – Gene expression – Lung and intrathoracic tumors – Pathogenesis – RNA interference – RNA-binding proteins – Toll-like receptors


Zdroje

1. Nanavaty P, Alvarez MS, Alberts WM. Lung cancer screening: advantages, controversies, and applications. Cancer Control. 2014;21(1):9–14. Epub 2013/12/21. doi: 10.1177/107327481402100102 24357736.

2. Kadara H, Scheet P, Wistuba II, Spira AE. Early Events in the Molecular Pathogenesis of Lung Cancer. Cancer Prev Res (Phila). 2016;9(7):518–27. Epub 2016/03/24. doi: 10.1158/1940-6207.Capr-15-0400 27006378.

3. Hirsch FR, Scagliotti GV, Mulshine JL, Kwon R, Curran WJ Jr., Wu YL, et al. Lung cancer: current therapies and new targeted treatments. Lancet. 2017;389(10066):299–311. Epub 2016/08/31. doi: 10.1016/S0140-6736(16)30958-8 27574741.

4. Zhang L, Yu J. Role of apoptosis in colon cancer biology, therapy, and prevention. Curr Colorectal Cancer Rep. 2013;9(4). Epub 2013/11/26. doi: 10.1007/s11888-013-0188-z 24273467; PubMed Central PMCID: PMC3836193.

5. Pore MM, Hiltermann TJ, Kruyt FA. Targeting apoptosis pathways in lung cancer. Cancer Lett. 2013;332(2):359–68. Epub 2010/10/27. doi: 10.1016/j.canlet.2010.09.012 20974517.

6. Suvarna V, Singh V, Murahari M. Current overview on the clinical update of Bcl-2 anti-apoptotic inhibitors for cancer therapy. European journal of pharmacology. 2019;862:172655. doi: 10.1016/j.ejphar.2019.172655 31494078.

7. Zanoaga O, Braicu C, Jurj A, Rusu A, Buiga R, Berindan-Neagoe I. Progress in Research on the Role of Flavonoids in Lung Cancer. International journal of molecular sciences [Internet]. 2019 2019/09//; 20(17). Available from: http://europepmc.org/abstract/MED/31480720 http://europepmc.org/articles/PMC6747533?pdf=render http://europepmc.org/articles/PMC6747533 https://doi.org/10.3390/ijms20174291.

8. Yu LC, Flynn AN, Turner JR, Buret AG. SGLT-1-mediated glucose uptake protects intestinal epithelial cells against LPS-induced apoptosis and barrier defects: a novel cellular rescue mechanism? Faseb j. 2005;19(13):1822–35. Epub 2005/11/02. doi: 10.1096/fj.05-4226com 16260652.

9. Mikulandra M, Pavelic J, Glavan TM. Recent Findings on the Application of Toll-like Receptors Agonists in Cancer Therapy. Curr Med Chem. 2017;24(19):2011–32. Epub 2017/03/23. doi: 10.2174/0929867324666170320114359 28322156.

10. Mimori K, Shiraishi T, Mashino K, Sonoda H, Yamashita K, Yoshinaga K, et al. MAL gene expression in esophageal cancer suppresses motility, invasion and tumorigenicity and enhances apoptosis through the Fas pathway. Oncogene. 2003;22(22):3463–71. Epub 2003/05/31. doi: 10.1038/sj.onc.1206378 12776198.

11. Popp MW, Maquat LE. Nonsense-mediated mRNA Decay and Cancer. Curr Opin Genet Dev. 2018;48:44–50. Epub 2017/11/10. doi: 10.1016/j.gde.2017.10.007 29121514; PubMed Central PMCID: PMC5869107.

12. Labno A, Tomecki R, Dziembowski A. Cytoplasmic RNA decay pathways—Enzymes and mechanisms. Biochim Biophys Acta. 2016;1863(12):3125–47. Epub 2016/11/05. doi: 10.1016/j.bbamcr.2016.09.023 27713097.

13. Gerstberger S, Hafner M, Tuschl T. A census of human RNA-binding proteins. Nat Rev Genet. 2014;15(12):829–45. Epub 2014/11/05. doi: 10.1038/nrg3813 25365966.

14. Warraich ST, Yang S, Nicholson GA, Blair IP. TDP-43: a DNA and RNA binding protein with roles in neurodegenerative diseases. The international journal of biochemistry & cell biology. 2010;42(10):1606–9. doi: 10.1016/j.biocel.2010.06.016 20601083.

15. Dewey CM, Cenik B, Sephton CF, Johnson BA, Herz J, Yu G. TDP-43 aggregation in neurodegeneration: are stress granules the key? Brain Res. 2012;1462:16–25. Epub 2012/03/13. doi: 10.1016/j.brainres.2012.02.032 22405725; PubMed Central PMCID: PMC3372581.

16. Guo F, Jiao F, Song Z, Li S, Liu B, Yang H, et al. Regulation of MALAT1 expression by TDP43 controls the migration and invasion of non-small cell lung cancer cells in vitro. Biochem Biophys Res Commun. 2015;465(2):293–8. Epub 2015/08/13. doi: 10.1016/j.bbrc.2015.08.027 26265046.

17. Wang M, Su P. The role of the Fas/FasL signaling pathway in environmental toxicant-induced testicular cell apoptosis: An update. Syst Biol Reprod Med. 2018;64(2):93–102. Epub 2018/01/05. doi: 10.1080/19396368.2017.1422046 29299971.

18. Sui Y, Yang Y, Wang J, Li Y, Ma H, Cai H, et al. Lysophosphatidic Acid Inhibits Apoptosis Induced by Cisplatin in Cervical Cancer Cells. Biomed Res Int. 2015;2015:598386. Epub 2015/09/15. doi: 10.1155/2015/598386 26366416; PubMed Central PMCID: PMC4558435.

19. Lee S, Park B. InSAC: A novel sub-nuclear body essential for Interleukin-6 and -10 RNA processing and stability. BMB Rep. 2015;48(5):239–40. Epub 2015/04/08. doi: 10.5483/BMBRep.2015.48.5.060 25845943; PubMed Central PMCID: PMC4578560.

20. Mashima T, Tsuruo T. Defects of the apoptotic pathway as therapeutic target against cancer. Drug Resist Updat. 2005;8(6):339–43. Epub 2005/12/13. doi: 10.1016/j.drup.2005.11.001 16338161.

21. Rathore R, McCallum JE, Varghese E, Florea AM, Busselberg D. Overcoming chemotherapy drug resistance by targeting inhibitors of apoptosis proteins (IAPs). Apoptosis. 2017;22(7):898–919. Epub 2017/04/21. doi: 10.1007/s10495-017-1375-1 28424988; PubMed Central PMCID: PMC5486846.

22. Tian Y, Wang J, Wang W, Ding Y, Sun Z, Zhang Q, et al. Mesenchymal stem cells improve mouse non-heart-beating liver graft survival by inhibiting Kupffer cell apoptosis via TLR4-ERK1/2-Fas/FasL-caspase3 pathway regulation. Stem Cell Res Ther. 2016;7(1):157. Epub 2016/10/30. doi: 10.1186/s13287-016-0416-y 27788674; PubMed Central PMCID: PMC5084468.

23. Bonham KS, Orzalli MH, Hayashi K, Wolf AI, Glanemann C, Weninger W, et al. A promiscuous lipid-binding protein diversifies the subcellular sites of toll-like receptor signal transduction. Cell. 2014;156(4):705–16. Epub 2014/02/18. doi: 10.1016/j.cell.2014.01.019 24529375; PubMed Central PMCID: PMC3951743.

24. Yang C, Liu HZ, Fu ZX. PEG-liposomal oxaliplatin induces apoptosis in human colorectal cancer cells via Fas/FasL and caspase-8. Cell Biol Int. 2012;36(3):289–96. Epub 2011/09/06. doi: 10.1042/CBI20100825 21888623.

25. An YF, Geng XR, Mo LH, Liu JQ, Yang LT, Zhang XW, et al. The 3-methyl-4-nitrophenol (PNMC) compromises airway epithelial barrier function. Toxicology. 2018;395:9–14. Epub 2018/01/09. doi: 10.1016/j.tox.2018.01.001 29307546.

26. He W, Yang C, Xia L, Zhao MZ, Ge RT, Huang H, et al. CD4(+) T cells from food allergy model are resistant to TCR-dependent apoptotic induction. Cytokine. 2014;68(1):32–9. Epub 2014/05/03. doi: 10.1016/j.cyto.2014.03.010 24787054.

27. Zhang P, Ma Y, Lv C, Huang M, Li M, Dong B, et al. Upregulation of programmed cell death ligand 1 promotes resistance response in non-small-cell lung cancer patients treated with neo-adjuvant chemotherapy. Cancer Sci. 2016;107(11):1563–71. Epub 2016/09/02. doi: 10.1111/cas.13072 27581532; PubMed Central PMCID: PMC5132280.

28. Parrish AB, Freel CD, Kornbluth S. Cellular mechanisms controlling caspase activation and function. Cold Spring Harb Perspect Biol. 2013;5(6). Epub 2013/06/05. doi: 10.1101/cshperspect.a008672 23732469; PubMed Central PMCID: PMC3660825.

29. Figgett WA, Fairfax K, Vincent FB, Le Page MA, Katik I, Deliyanti D, et al. The TACI receptor regulates T-cell-independent marginal zone B cell responses through innate activation-induced cell death. Immunity. 2013;39(3):573–83. Epub 2013/09/10. doi: 10.1016/j.immuni.2013.05.019 24012421.


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