Role of layilin in regulating mitochondria-mediated apoptosis: a study on B cell lymphoma (BCL)-2 family proteins.

Humans Apoptosis / drug effects Mitochondria / metabolism Cell Line, Tumor Proto-Oncogene Proteins c-bcl-2 / metabolism Lectins, C-Type / metabolism Membrane Potential, Mitochondrial / drug effects Membrane Proteins / metabolism bcl-Associated Death Protein / metabolism Staurosporine / pharmacology Caspase 3 / metabolism Mitochondrial Precursor Protein Import Complex Proteins
Apoptosis BAD BCL-2 Layilin

Journal

BMC molecular and cell biology
ISSN: 2661-8850
Titre abrégé: BMC Mol Cell Biol
Pays: England
ID NLM: 101741148

Informations de publication

Date de publication:
25 Oct 2024
Historique:
received: 27 02 2024
accepted: 11 10 2024
medline: 26 10 2024
pubmed: 26 10 2024
entrez: 25 10 2024
Statut: epublish

Résumé

Malignant gliomas exhibit rapid tumor progression and resistance to treatment, leading to high lethality. One of the causes is the reduced progression of apoptosis in glioma cells. Layilin is a type 1 transmembrane protein with a C-type lectin motif in its extracellular domain. We previously reported that layilin is mainly localized to mitochondria or their close proximity and that layilin is essential for maintaining of the fragmented type of mitochondria. This study investigates the effects of layilin on mitochondria-mediated apoptosis, focusing on B cell lymphoma (BCL)-2 family proteins in a glioma cell line of A172 cells. We compared the levels of pro-apoptotic BCL-2 family proteins of BAD, BAK, BAX, and BIM and anti-apoptotic BCL-2 family proteins of BCL-2 and BCL-X This study demonstrates that layilin contributes to ΔΨm reduction to promote apoptosis by up-regulating BAD and down-regulating BCL-2 in glioma cells. Our data elucidates a new function of layilin: regulation of mitochondria-mediated apoptosis.

Sections du résumé

BACKGROUND BACKGROUND
Malignant gliomas exhibit rapid tumor progression and resistance to treatment, leading to high lethality. One of the causes is the reduced progression of apoptosis in glioma cells. Layilin is a type 1 transmembrane protein with a C-type lectin motif in its extracellular domain. We previously reported that layilin is mainly localized to mitochondria or their close proximity and that layilin is essential for maintaining of the fragmented type of mitochondria. This study investigates the effects of layilin on mitochondria-mediated apoptosis, focusing on B cell lymphoma (BCL)-2 family proteins in a glioma cell line of A172 cells.
RESULTS RESULTS
We compared the levels of pro-apoptotic BCL-2 family proteins of BAD, BAK, BAX, and BIM and anti-apoptotic BCL-2 family proteins of BCL-2 and BCL-X
CONCLUSION CONCLUSIONS
This study demonstrates that layilin contributes to ΔΨm reduction to promote apoptosis by up-regulating BAD and down-regulating BCL-2 in glioma cells. Our data elucidates a new function of layilin: regulation of mitochondria-mediated apoptosis.

Identifiants

DOI: 10.1186/s12860-024-00521-9 PMID: 39455917
pubmed: 39455917
doi: 10.1186/s12860-024-00521-9
pii: 10.1186/s12860-024-00521-9
doi:

Substances chimiques

Proto-Oncogene Proteins c-bcl-2 0
Lectins, C-Type 0
Membrane Proteins 0
bcl-Associated Death Protein 0
Staurosporine H88EPA0A3N
Caspase 3 EC 3.4.22.-
TOMM20 protein, human 0
Mitochondrial Precursor Protein Import Complex Proteins 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

24

Subventions

Organisme : St. Marianna University School of Medicine Grant to Promote Diversity in Research
ID : SMUGDIVR20211
Organisme : JSPS KAKENHI
ID : 22K08555

Informations de copyright

© 2024. The Author(s).

Références

Goodenberger ML, Jenkins RB. Genetics of adult glioma. Cancer Genet. 2012;205:613–21. https://doi.org/10.1016/j.cancergen.2012.10.009 .
doi: 10.1016/j.cancergen.2012.10.009 pubmed: 23238284
Louis DN, Ohgaki H, Wiestler OD, et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. 2007;114:97–109. https://doi.org/10.1007/s00401-007-0243-4 .
doi: 10.1007/s00401-007-0243-4 pubmed: 17618441 pmcid: 1929165
Louis DN, Perry A, Reifenberger G, et al. The 2016 world health organization classification of tumors of the central nervous system: a summary. Acta Neuropathol. 2016;131:803–20. https://doi.org/10.1007/s00401-016-1545-1 .
doi: 10.1007/s00401-016-1545-1 pubmed: 27157931
Salvucci M, Zakaria Z, Carberry S, et al. System-based approaches as prognostic tools for glioblastoma. BMC Cancer. 2019;19:1092. https://doi.org/10.1186/s12885-019-6280-2 .
doi: 10.1186/s12885-019-6280-2 pubmed: 31718568 pmcid: 6852738
Borowsky ML, Hynes RO. Layilin, a novel talin-binding transmembrane protein homologous with C-type lectins, is localized in membrane ruffles. J Cell Biol. 1998;143:429–42. https://doi.org/10.1083/jcb.143.2.429 .
doi: 10.1083/jcb.143.2.429 pubmed: 9786953 pmcid: 2132847
Bono P, Rubin K, Higgins JM, et al. Layilin, a novel integral membrane protein, is a hyaluronan receptor. Mol Biol Cell. 2001;12:891–900. https://doi.org/10.1091/mbc.12.4.891 .
doi: 10.1091/mbc.12.4.891 pubmed: 11294894 pmcid: 32274
Bono P, Cordero E, Johnson K, et al. Layilin, a cell surface hyaluronan receptor, interacts with merlin and radixin. Exp Cell Res. 2005;308:177–87. https://doi.org/10.1016/j.yexcr.2005.04.017 .
doi: 10.1016/j.yexcr.2005.04.017 pubmed: 15913605
Zheng C, Zheng L, Yoo JK, et al. Landscape of infiltrating T cells in Liver Cancer revealed by single-cell sequencing. Cell. 2017;169:1342–56. https://doi.org/10.1016/j.cell.2017.05.035 .
doi: 10.1016/j.cell.2017.05.035 pubmed: 28622514
Kaji T, Arito M, Tsutiya A, et al. Layilin enhances the invasive ability of malignant glioma cells via SNAI1 signaling. Brain Res. 2019;1719:140–7. https://doi.org/10.1016/j.brainres.2019.05.034 .
doi: 10.1016/j.brainres.2019.05.034 pubmed: 31145904
Tsutiya A, Arito M, Tagashira T, et al. Layilin promotes mitochondrial fission by cyclin-dependent kinase 1 and dynamin-related protein 1 activation in HEK293T cells. Biochem Biophys Res Commun. 2021;549:143–9. https://doi.org/10.1016/j.bbrc.2021.02.091 .
doi: 10.1016/j.bbrc.2021.02.091 pubmed: 33676182
Hajnóczky G, Davies E, Madesh M, et al. Calcium signaling and apoptosis. Biochem Biophys Res Commun. 2003;304:445–54. https://doi.org/10.1016/S0006-291X(03)00616-8 .
doi: 10.1016/S0006-291X(03)00616-8 pubmed: 12729578
Bauer TM, Murphy E. Role of mitochondrial calcium and the permeability transition pore in regulating cell death. Circul Res. 2020;126:280–93. https://doi.org/10.1161/CIRCRESAHA.119.316306 .
doi: 10.1161/CIRCRESAHA.119.316306
Lemasters JJ, Theruvath TP, Zhong Z, et al. Mitochondrial calcium and the permeability transition in cell death. Biochim Biophys Acta. 2009;1787:1395–401. https://doi.org/10.1016/j.bbabio.2009.06.009 .
doi: 10.1016/j.bbabio.2009.06.009 pubmed: 19576166 pmcid: 2730424
Karbowski M, Youle RJ. Dynamics of mitochondrial morphology in healthy cells and during apoptosis. Cell Death Differ. 2003;10:870–80. https://doi.org/10.1038/sj.cdd.4401260 .
doi: 10.1038/sj.cdd.4401260 pubmed: 12867994
Valdebenito GE, Duchen MR. Monitoring mitochondrial membrane potential in live cells using time-lapse fluorescence imaging. In: Tomar, N, editors Mitochondria. Methods Mol Biol. 2022;2497. https://doi.org/10.1007/978-1-0716-2309-1_22
Gross A, McDonnell JM, Korsmeyer SJ. BCL-2 family members and the mitochondria in apoptosis Genes dev. 1999;13:1899–911. https://doi.org/10.1101/gad.13.15.1899 .
Singh R, Letai A, Sarosiek K. Regulation of apoptosis in health and disease: the balancing act of BCL-2 family proteins. Nat Rev Mol Cell Biol. 2019;20:175–93. https://doi.org/10.1038/s41580-018-0089-8 .
doi: 10.1038/s41580-018-0089-8 pubmed: 30655609 pmcid: 7325303
Mikhailov V, Mikhailova M, Degenhardt K, et al. Association of Bax and bak homo-oligomers in mitochondria. Bax requirement for bak reorganization and cytochrome c release. J Biol Chem. 2003;278:5367–76. https://doi.org/10.1074/jbc.M203392200 .
doi: 10.1074/jbc.M203392200 pubmed: 12454021
Peña-Blanco A, García-Sáez AJ. Bax, Bak and beyond_Mitochondrial performance in apoptosis. FEBS J. 2018;285:416–31. https://doi.org/10.1111/febs.14186 .
doi: 10.1111/febs.14186 pubmed: 28755482
Whelan RS, Konstantinidis K, Wei AC et al. Bax regulates primary necrosis through mitochondrial dynamics. Proc Natl Acad Sci U S A 2012;109:6566–571. https://doi.org/10.1073/pnas.1201608109 .
Hengartner M. The biochemistry of apoptosis. Nature. 2000;407:770–6. https://doi.org/10.1038/35037710 .
doi: 10.1038/35037710 pubmed: 11048727
Slee EA, Harte MT, Kluck RM, et al. Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2, -3, -6, -7, -8, and – 10 in a caspase-9-dependent manner. J Cell Biol. 1999;144:281–92. https://doi.org/10.1083/jcb.144.2.281 .
doi: 10.1083/jcb.144.2.281 pubmed: 9922454 pmcid: 2132895
Tsujimoto Y. Role of Bcl-2 family proteins in apoptosis: apoptosomes or mitochondria? Genes Cells. 1998;3:697–707. https://doi.org/10.1046/j.1365-2443.1998.00223.x .
doi: 10.1046/j.1365-2443.1998.00223.x
Oltvai ZN, Milliman CL, Korsmeyer SJ. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Comp Study Cell. 1993;74:609-19. https://doi.org/10.1016/0092-8674(93)90509-o .
Hirotani M, Zhang Y, Fujita N, et al. NH2-terminal BH4 domain of Bcl-2 is functional for heterodimerization with Bax and inhibition of apoptosis. J Biol Chem. 1999;274:20415–20. https://doi.org/10.1074/jbc.274.29.20415 .
doi: 10.1074/jbc.274.29.20415 pubmed: 10400666
Schindelin J, Arganda-Carreras I, Frise E, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9:676e682. https://doi.org/10.1038/nmeth.2019 .
doi: 10.1038/nmeth.2019
Asano K, Arito M, Kurokawa MS, et al. Secretion of inflammatory factors from chondrocytes by layilin signaling. Biochem Biophys Res Commun. 2014;452:85–90. https://doi.org/10.1016/j.bbrc.2014.08.053 .
doi: 10.1016/j.bbrc.2014.08.053 pubmed: 25150153
Sakai Y, Taguchi M, Morikawa Y, et al. Apoptotic mechanism in human brain microvascular endothelial cells triggered by 40-iodo-α-pyrrolidinononanophenone: contribution of decrease in antioxidant properties. Toxicol Lett. 2022;355:127–40.  https://doi.org/10.1016/j.toxlet.2021.11.018 .
doi: 10.1016/j.toxlet.2021.11.018 pubmed: 34863860
Suyama K, Sakai D, Hayashi S, et al. Bag-1 protects Nucleus Pulposus cells from oxidative stress by interacting with HSP70. Biomedicines. 2023;11:863. https://doi.org/10.3390/biomedicines11030863 .
doi: 10.3390/biomedicines11030863 pubmed: 36979842 pmcid: 10045753
Yang E, Zha J, Jockel J, et al. Bad, a heterodimeric partner for Bcl-XL and Bcl-2, displaces Bax and promotes cell death. Cell. 1995;80:285–91. https://doi.org/10.1016/0092-8674(95)90411-5 .
doi: 10.1016/0092-8674(95)90411-5 pubmed: 7834748
Dispersyn G, Nuydens R, Connors R, et al. Bcl-2 protects against FCCP-induced apoptosis and mitochondrial membrane potential depolarization in PC12 cells. Biochim Biophys Acta. 1999;1428(2–3):357–71. https://doi.org/10.1016/s0304-4165(99)00073-2 .
doi: 10.1016/s0304-4165(99)00073-2 pubmed: 10434055
Prudent J, Zunino R, Sugiura A. MAPL SUMOylation of Drp1 stabilizes an ER/Mitochondrial platform required for cell death. Mol Cell. 2015;59:941–55. https://doi.org/10.1016/j.molcel.2015.08.001 .
doi: 10.1016/j.molcel.2015.08.001 pubmed: 26384664
Hurst S, Hoek J, Sheu SS. Mitochondrial Ca
doi: 10.1007/s10863-016-9672-x pubmed: 27497945 pmcid: 5393273
Neginskaya MA, Morris SE, Pavlov.Both EV. ANT and ATPase are essential for mitochondrial permeability transition but not depolarization. iScience. 2022;25:105447. https://doi.org/10.1016/j.isci.2022.105447 .
doi: 10.1016/j.isci.2022.105447 pubmed: 36388971 pmcid: 9647522
Dong R, Wang Q, He XL, et al. Role of nuclear factor kappa B and reactive oxygen species in the tumor necrosis factor-alpha-induced epithelial-mesenchymal transition of MCF-7 cells. Braz J Med Biol Res. 2007;40:1071–8. https://doi.org/10.1590/s0100-879x2007000800007 .
doi: 10.1590/s0100-879x2007000800007 pubmed: 17665043
Wu Y, Deng J, Rychahou PG, et al. Stabilization of snail by NF-kappaB is required for inflammation-induced cell migration and invasion. Cancer Cell. 2009;15:416–28. https://doi.org/10.1016/j.ccr.2009.03.016 .
doi: 10.1016/j.ccr.2009.03.016 pubmed: 19411070 pmcid: 2881229
Jiang Y, Porter AG. Prevention of tumor necrosis factor (TNF)-mediated induction of p21WAF1/CIP1 sensitizes MCF-7 carcinoma cells to TNF-induced apoptosis. Biochem Biophys Res Commun. 1998;245:691–7. https://doi.org/10.1006/bbrc.1998.8390 .
doi: 10.1006/bbrc.1998.8390 pubmed: 9588176
Rozen F, Zhang J, Pollak M. Antiproliferative action of tumor necrosis factor-alpha on MCF-7 breast cancer cells is associated with increased insulin-like growth factor binding protein-3 accumulation. Int J Oncol. 1998;13:865–9. https://doi.org/10.3892/ijo.13.4.865 .
doi: 10.3892/ijo.13.4.865 pubmed: 9735418
Burow ME, Weldon CB, Melnik LI, et al. PI3-K/AKT regulation of NF-kappaB signaling events in suppression of TNF-induced apoptosis. Biochem Biophys Res Commun. 2000;271:342–5. https://doi.org/10.1006/bbrc.2000.2626 .
doi: 10.1006/bbrc.2000.2626 pubmed: 10799299

Auteurs

Mitsumi Arito (M)

Clinical Proteomics and Molecular Medicine, St. Marianna University Graduate School of Medicine, 2-16-1 Sugao, Miyamae, Kawasaki, Kanagawa, 216-8511, Japan. m-ari@marianna-u.ac.jp.

Atsuhiro Tsutiya (A)

Clinical Proteomics and Molecular Medicine, St. Marianna University Graduate School of Medicine, 2-16-1 Sugao, Miyamae, Kawasaki, Kanagawa, 216-8511, Japan.

Masaaki Sato (M)

Clinical Proteomics and Molecular Medicine, St. Marianna University Graduate School of Medicine, 2-16-1 Sugao, Miyamae, Kawasaki, Kanagawa, 216-8511, Japan.

Kazuki Omoteyama (K)

Clinical Proteomics and Molecular Medicine, St. Marianna University Graduate School of Medicine, 2-16-1 Sugao, Miyamae, Kawasaki, Kanagawa, 216-8511, Japan.

Toshiyuki Sato (T)

Clinical Proteomics and Molecular Medicine, St. Marianna University Graduate School of Medicine, 2-16-1 Sugao, Miyamae, Kawasaki, Kanagawa, 216-8511, Japan.

Yusei Motonaga (Y)

Clinical Proteomics and Molecular Medicine, St. Marianna University Graduate School of Medicine, 2-16-1 Sugao, Miyamae, Kawasaki, Kanagawa, 216-8511, Japan.

Naoya Suematsu (N)

Clinical Proteomics and Molecular Medicine, St. Marianna University Graduate School of Medicine, 2-16-1 Sugao, Miyamae, Kawasaki, Kanagawa, 216-8511, Japan.

Manae S Kurokawa (MS)

Disease Biomarker Analysis and Molecular Regulation, St. Marianna University Graduate School of Medicine, 2-16-1 Sugao, Miyamae, Kawasaki, Kanagawa, 216-8511, Japan.

Tomohiro Kato (T)

Clinical Proteomics and Molecular Medicine, St. Marianna University Graduate School of Medicine, 2-16-1 Sugao, Miyamae, Kawasaki, Kanagawa, 216-8511, Japan.

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Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Role of layilin in regulating...
questionsmedicales.fr › Phénomènes physiologiques cellulaires › Mort cellulaire › Mort cellulaire régulée › Apoptose › Role of layilin in regulating...
questionsmedicales.fr › Cellules › Structures cellulaires › Fractions subcellulaires › Mitochondries › Role of layilin in regulating...
questionsmedicales.fr › Cellules › Cellules cultivées › Cellules cancéreuses en culture › Lignée cellulaire tumorale › Role of layilin in regulating...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines tumorales › Protéines oncogènes › Protéines proto-oncogènes › Protéines proto-oncogènes c-bcl-2 › Role of layilin in regulating...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Lectines › Lectines de type C › Role of layilin in regulating...
questionsmedicales.fr › Phénomènes physiologiques › Phénomènes électrophysiologiques › Potentiel de membrane mitochondriale › Role of layilin in regulating...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines membranaires › Role of layilin in regulating...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Phosphoprotéines › Protéine Bad › Role of layilin in regulating...
questionsmedicales.fr › Composés hétérocycliques › Composés hétérocycliques à cycles fusionnés › Composés hétérocycliques 3 noyaux › Carbazoles › Staurosporine › Role of layilin in regulating...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines et peptides de signalisation intracellulaire › Protéines régulatrices de l'apoptose › Caspases › Caspases effectrices › Caspase-3 › Role of layilin in regulating...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines mitochondriales › Protéines de transport de la membrane mitochondriale › Protéines du complexe d'import des protéines précurseurs mitochondriales › Role of layilin in regulating...