Autophagosome proteins LC3A, LC3B and LC3C have distinct subcellular distribution kinetics and expression in cancer cell lines.
Open accessAbstract
LC3s (MAP1-LC3A, B and C) are structural proteins of autophagosomal membranes, widely used as biomarkers of autophagy. Whether these three LC3 proteins have a similar biological role in autophagy remains obscure. We examine in parallel the subcellular expression patterns of the three LC3 proteins in a panel of human cancer cell lines, as well as in normal MRC5 fibroblasts and HUVEC, using confocal microscopy and western blot analysis of cell fractions. In the cytoplasm, there was a minimal co-localization between LC3A, B and C staining, suggesting that the relevant autophagosomes are formed by only one out of the three LC3 proteins. LC3A showed a perinuclear and nuclear localization, while LC3B was equally distributed throughout the cytoplasm and localized in the nucleolar regions. LC3C was located in the cytoplasm and strongly in the nuclei (excluding nucleoli), where it extensively co-localized with the LC3A and the Beclin-1 autophagy initiating protein. Beclin 1 is known to contain a nuclear trafficking signal. Blocking nuclear export function by Leptomycin B resulted in nuclear accumulation of all LC3 and Beclin-1 proteins, while Ivermectin that blocks nuclear import showed reduction of accumulation, but not in all cell lines. Since endogenous LC3 proteins are used as major markers of autophagy in clinical studies and cell lines, it is essential to check the specificity of the antibodies used, as the kinetics of these molecules are not identical and may have distinct biological roles. The distinct subcellular expression patterns of LC3s provide a basis for further studies.
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Some studies suggest isoform specificity in selective autophagy.
“some studies suggest isoform specificity in selective autophagy (Shpilka et al., 2011; Maruyama et al., 2014; Koukourakis et al., 2015).”
From Microtubule-associated protein 1 light chain 3B, (LC3B) is necessary to maintain lipid-mediated homeostasis in the retinal pigment epithelium (2018) · cites this paper as Koukourakis et al., 2015
Specifying individual LC3 isoform is necessary because the isoforms have different expression patterns and biology.
“Specifying individual LC3 isoform is necessary as the isoforms have different expression patterns and biology (Cann et al., 2008; Koukourakis et al., 2015).”
From Microtubule-associated protein 1 light chain 3B, (LC3B) is necessary to maintain lipid-mediated homeostasis in the retinal pigment epithelium (2018) · cites this paper as Koukourakis et al., 2015
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LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing.
Kabeya, Y., Mizushima, N., Ueno, T., Yamamoto, A., Kirisako, T., Noda, T., Kominami, E., Ohsumi, Y., & Yoshimori, T. (2000) · The EMBO Journal · doi:10.1093/emboj/19.21.5720 · Cited by 6,605 · see citing works
Cui, C., Cui, J., Jin, F., Cui, Y., Li, R., Jiang, X., Tian, Y., Wang, R. C., Jiang, P., & Gao, J. (2017) · Cellular Physiology and Biochemistry · doi:10.1159/000479571 · Cited by 5,214 · see citing works
Tissue fractionation studies. 6. Intracellular distribution patterns of enzymes in rat-liver tissue
Duve, C. D., Pressman, B. C., Gianetto, R., Wattiaux, R., & Appelmans, F. (1955) · Biochemical Journal · doi:10.1042/bj0600604 · Cited by 4,176 · see citing works
Autophagy as a regulated pathway of cellular degradation.
Klionsky, D., & Emr, S. (2000) · Science · doi:10.1126/science.290.5497.1717 · Cited by 3,794 · see citing works
Antimicrobial Autophagy: A Conserved Innate Immune Response in Drosophila
Moy, R. H., & Cherry, S. R. (2013) · Journal of Innate Immunity · doi:10.1159/000350326 · Cited by 3,549 · see citing works
A ubiquitin-like system mediates protein lipidation
Ichimura, Y., Kirisako, T., Takao, T., Satomi, Y., Shimonishi, Y., Ishihara, N., Mizushima, N., Tanida, I., Kominami, E., Ohsumi, M., et al. (2000) · Nature · doi:10.1038/35044114 · Cited by 2,064 · see citing works
Exportin 1 (Crm1p) Is an Essential Nuclear Export Factor
Stade, K., Ford, C. S., Guthrie, C., & Weis, K. (1997) · Cell · doi:10.1016/s0092-8674(00)80370-0 · Cited by 1,145 · see citing works
Kudo, N. R., Matsumori, N., Taoka, H., Fujiwara, D., Schreiner, E. P., Wolff, B., Yoshida, M., & Horinouchi, S. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.16.9112 · Cited by 1,033 · see citing works
Autophagy: assays and artifacts
Barth, S., Glick, D. R., & Macleod, K. F. (2010) · The Journal of Pathology · doi:10.1002/path.2694 · Cited by 794 · see citing works
Wagstaff, K. M., Sivakumaran, H., Heaton, S. M., Harrich, D., & Jans, D. A. (2012) · Biochemical Journal · doi:10.1042/bj20120150 · Cited by 682 · see citing works
He, H., Dang, Y., Dai, F., Guo, Z., Wu, J., She, X., Pei, Y., Chen, Y., Ling, W., Wu, C., et al. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m303800200 · Cited by 273 · see citing works
Liang, X., Yu, J., Brown, K., & Levine, B. (2001) · PubMed · Cited by 269 · see citing works
Tanida, I., Ueno, T., & Kominami, E. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m407016200 · Cited by 244 · see citing works
Defective autophagy in neurons and astrocytes from mice deficient in PI(3,5)P2
Ferguson, C. J., Lenk, G. M., & Meisler, M. H. (2009) · Human Molecular Genetics · doi:10.1093/hmg/ddp460 · Cited by 202 · see citing works
Molecular cloning and characterization of rat LC3A and LC3B—Two novel markers of autophagosome
Wu, J., Dang, Y., Su, W., Liu, C., Ma, H., Shan, Y., Pei, Y., Wan, B., Guo, J., & Yu, L. (2005) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2005.10.211 · Cited by 174 · see citing works
Aoki, H., Kondo, Y., Aldape, K., Yamamoto, A., Iwado, E., Yokoyama, T., Hollingsworth, E., Kobayashi, R., Hess, K. R., Shinojima, N., et al. (2008) · Autophagy · doi:10.4161/auto.5668 · Cited by 126 · see citing works
Karim, M. R., Kanazawa, T., Daigaku, Y., Fujimura, S., Miotto, G., & Kadowaki, M. (2007) · Autophagy · doi:10.4161/auto.4615 · Cited by 120 · see citing works
Nucleocytoplasmic Distribution and Dynamics of the Autophagosome Marker EGFP-LC3
Drake, K. R., Kang, M., & Kenworthy, A. K. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009806 · Cited by 97 · see citing works
Bai, H., Inoue, J., Kawano, T., & Inazawa, J. (2012) · Oncogene · doi:10.1038/onc.2011.613 · Cited by 88 · see citing works
"Autophagic flux" in normal mouse tissues: Focus on endogenous LC3A processing
Zois, C. E., Giatromanolaki, A. N., Sivridis, E., Papaiakovou, M., Kainulainen, H., & Koukourakis, M. I. (2011) · Autophagy · doi:10.4161/auto.7.11.16664 · Cited by 62 · see citing works
He, W., Hu, C. X., Hou, J., Fan, L., Xu, Y., Liu, M.-H., Yan, S. Y., Chen, G. Q., & Huang, Y. (2014) · PLoS ONE · doi:10.1371/journal.pone.0113089 · Cited by 14 · see citing works
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Klionsky, D. J., Abdel-Aziz, A. K., Abdelfatah, S., Abdellatif, M., Abdoli, A., Abel, S., Abeliovich, H., Abildgaard, M. H., Abudu, Y. P., Acevedo-Arozena, A., et al. (2021) · Autophagy · doi:10.1080/15548627.2020.1797280 · Cited by 2,622 · see citing works
Self-citationKandemır, F. M., Küçükler, S., Çağlayan, C., Gür, C., Batil, A. A., & Gülçın, İ. (2017) · Journal of Food Biochemistry · doi:10.1111/jfbc.12398 · Cited by 142 · see citing works
Kandemır, F. M., Küçükler, S., Eldutar, E., Çağlayan, C., & Gülçın, İ. (2017) · Scientia Pharmaceutica · doi:10.3390/scipharm85010004 · Cited by 132 · see citing works
Maiti, P., Scott, J., Sengupta, D., Gharaibeh, A., & Dunbar, G. L. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20020399 · Cited by 115 · see citing works
Ji, Y., Li, L., Ma, Y., Li, W., Li, L., Zhu, H., Wu, M., & Zhou, J. (2019) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2019.03.018 · Cited by 105 · see citing works
Jiang, L., Zheng, H., Lyu, Q., Hayashi, S., Sato, K., Sekido, Y., Nakamura, K., Tanaka, H., Ishikawa, K., Kajiyama, H., et al. (2021) · Redox Biology · doi:10.1016/j.redox.2021.101989 · Cited by 101 · see citing works
Zhu, J., Gao, M., Zhang, R., Sun, Z., Wang, C., Yang, F., Huang, T., Qu, S., Zhao, L. M., Li, Y., et al. (2017) · Microbial Cell Factories · doi:10.1186/s12934-017-0809-3 · Cited by 99 · see citing works
Gür, C., Kandemır, F. M., Çağlayan, C., & Satıcı, E. (2022) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2022.110073 · Cited by 98 · see citing works
Buckingham, E. M., Jarosinski, K. W., Jackson, W., Carpenter, J. E., & Grose, C. F. (2016) · Journal of Virology · doi:10.1128/jvi.00915-16 · Cited by 96 · see citing works
Sirtuin 6 overexpression relieves sepsis-induced acute kidney injury by promoting autophagy
Zhang, Y., Wang, L., Meng, L., Cao, G., & Wu, Y. (2019) · Cell Cycle · doi:10.1080/15384101.2019.1568746 · Cited by 90 · see citing works
Conformational flexibility of BECN1: Essential to its key role in autophagy and beyond
Yang, M., Glover, K., Su, M., & Sinha, S. C. (2016) · Protein Science · doi:10.1002/pro.2984 · Cited by 88 · see citing works
Jatana, N., Ascher, D. B., Pires, D. E. V., Gokhale, R. S., & Thukral, L. (2019) · Autophagy · doi:10.1080/15548627.2019.1606636 · Cited by 84 · see citing works
D’Adamo, S., Cetrullo, S., Guidotti, S., Silvestri, Y., Minguzzi, M., Santi, S., Cattini, L., Filardo, G., Flamigni, F., & Borzı̀, R. M. (2020) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2020.03.029 · Cited by 81 · see citing works
Yardım, A., Kandemır, F. M., Çomaklı, S., Özdemir, S., Çağlayan, C., Küçükler, S., & Çelik, H. (2020) · Neurochemical Research · doi:10.1007/s11064-020-03174-0 · Cited by 77 · see citing works
Koukourakis, M. I., Mitrakas, A. G., & Giatromanolaki, A. N. (2016) · British Journal of Cancer · doi:10.1038/bjc.2016.19 · Cited by 76 · see citing works
Shim, M. S., Nettesheim, A., Hirt, J., & Liton, P. B. (2019) · Autophagy · doi:10.1080/15548627.2019.1662584 · Cited by 75 · see citing works
PINK1-dependent mitophagy is driven by the UPS and can occur independently of LC3 conversion
Rakovic, A., Ziegler, J., Mårtensson, C. U., Prasuhn, J., Shurkewitsch, K., König, P., Paulson, H. L., & Klein, C. (2019) · Cell Death & Differentiation · doi:10.1038/s41418-018-0219-z · Cited by 69 · see citing works
Baeken, M. W., Weckmann, K., Diefenthäler, P., Schulte, J., Yusifli, K., Moosmann, B., Behl, C., & Hajieva, P. (2020) · Cells · doi:10.3390/cells9102315 · Cited by 62 · see citing works
Petibone, D. M., Majeed, W., & Casciano, D. A. (2016) · Journal of Applied Toxicology · doi:10.1002/jat.3393 · Cited by 61 · see citing works
Zhang, L., Xia, Q., Zhou, Y., & Li, J. (2019) · Toxicology Letters · doi:10.1016/j.toxlet.2019.05.001 · Cited by 60 · see citing works
LC3A-mediated autophagy regulates lung cancer cell plasticity
Miao, C., Hwang, W., Chu, L.-Y., Yang, L., Ha, C.-T., Chen, P., Kuo, M.-H., Lin, S., Yang, Y., Chuang, S., et al. (2021) · Autophagy · doi:10.1080/15548627.2021.1964224 · Cited by 60 · see citing works
Delaney, J. R., Patel, C. B., Bapat, J., Jones, C. M., Zapatero, M. R., Ortell, K. K., Tanios, R., Haghighiabyaneh, M., Axelrod, J. L., DeStefano, J., et al. (2020) · PLoS Genetics · doi:10.1371/journal.pgen.1008558 · Cited by 55 · see citing works
Mitochondria in Aging and Alzheimer’s Disease: Focus on Mitophagy
Pradeepkiran, J. A., Baig, J., Seman, A., & Reddy, P. H. (2023) · The Neuroscientist · doi:10.1177/10738584221139761 · Cited by 50 · see citing works
El-Gazar, A. A., Soubh, A. A., Mohamed, E. A., Awad, A. S., & El-Abhar, H. S. (2019) · Brain Research · doi:10.1016/j.brainres.2019.04.003 · Cited by 49 · see citing works
Kızıl, H. E., Gür, C., Ayna, A., Darendelioğlu, E., Küçükler, S., & Sağ, S. (2023) · Chemistry & Biodiversity · doi:10.1002/cbdv.202200982 · Cited by 47 · see citing works
Cheng, C.-Y., Kao, S.-T., & Lee, Y.-C. (2019) · The American Journal of Chinese Medicine · doi:10.1142/s0192415x19500034 · Cited by 47 · see citing works
The regulatory role of autophagy-related miRNAs in lung cancer drug resistance
Shahverdi, M., Hajiasgharzadeh, K., Sorkhabi, A. D., Jafarlou, M., Shojaee, M., Tabrizi, N. J., Alizadeh, N., Santarpía, M., Brunetti, O., Safarpour, H., et al. (2022) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2022.112735 · Cited by 46 · see citing works
Fluorescence‐based ATG8 sensors monitor localization and function of LC3/GABARAP proteins
Stolz, A., Putyrski, M., Kutle, I., Huber, J., Wang, C., Major, V., Sidhu, S. S., Youle, R. J., Rogov, V. V., Dötsch, V., et al. (2016) · The EMBO Journal · doi:10.15252/embj.201695063 · Cited by 44 · see citing works
Role of autophagy in tumor response to radiation: Implications for improving radiotherapy
Roy, A., Bera, S., Saso, L., & Dwarakanath, B. S. R. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.957373 · Cited by 43 · see citing works
The Autophagoproteasome a Novel Cell Clearing Organelle in Baseline and Stimulated Conditions
Lenzi, P., Lazzeri, G., Biagioni, F., Busceti, C. L., Gambardella, S., Salvetti, A., & Fornai, F. (2016) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2016.00078 · Cited by 44 · see citing works
Varışlı, B., Darendelioğlu, E., Çağlayan, C., Kandemır, F. M., Ayna, A., Genç, A., & Kandemir, Ö. (2022) · Cardiovascular Toxicology · doi:10.1007/s12012-022-09751-9 · Cited by 43 · see citing works
Nuclear LC3 Associates with Slowly Diffusing Complexes that Survey the Nucleolus
Kraft, L. J., Manral, P., Dowler, J., & Kenworthy, A. K. (2016) · Traffic · doi:10.1111/tra.12372 · Cited by 43 · see citing works
Dhingra, A., Bell, B. A., Peachey, N. S., Daniele, L. L., Reyes-Reveles, J., Sharp, R. C., Jun, B., Bazan, N. G., Sparrow, J. R., Kim, H. J., et al. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00351 · Cited by 41 · see citing works
LC3B: A microtubule-associated protein influences disease progression and prognosis
Chen, Y., Yi, H., Liao, S., He, J., Zhou, Y., & Lei, Y. (2024) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2024.11.006 · Cited by 40 · see citing works
Wu, C., Chen, C. C., Hwang, C., Chen, S., Hwang, W., & Yang, D. (2016) · Journal of Neurochemistry · doi:10.1111/jnc.13937 · Cited by 38 · see citing works
Nguyen, T., Guo, R., Chai, J., Wu, J., Liu, J., Chen, X., Abdel-Rahman, M. A., Xia, H., & Xu, X. (2022) · Toxins · doi:10.3390/toxins14100717 · Cited by 35 · see citing works
LC3A, LC3B and Beclin-1 Expression in Gastric Cancer
Giatromanolaki, A. N., Koukourakis, M. I., Georgiou, I. A., Kouroupi, M., & Sivridis, E. (2018) · Anticancer Research · doi:10.21873/anticanres.13056 · Cited by 34 · see citing works
Besnoitia besnoitibradyzoite stages induce suicidal- and rapid vital-NETosis
Zhou, E., Silva, L. M. R., Conejeros, I., Velásquez, Z. D., Hirz, M., Gärtner, U., Jacquiet, P., Taubert, A., & Hermosilla, C. R. (2019) · Parasitology · doi:10.1017/s0031182019001707 · Cited by 34 · see citing works
Jiang, H., Yang, L., Guo, L., Cui, N., Zhang, G., Liu, C., Xing, L., Shao, Z., & Wang, H. (2018) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2018/6328051 · Cited by 33 · see citing works
Kopiasz, Ł., Dziendzikowska, K., Gajewska, M., Oczkowski, M., Majchrzak, K., Królikowski, T., & Gromadzka-Ostrowska, J. (2021) · Nutrients · doi:10.3390/nu13020321 · Cited by 32 · see citing works
Sharma, S. K., Ghufran, S. M., Ghose, S., & Biswas, S. (2021) · Scientific Reports · doi:10.1038/s41598-021-82381-3 · Cited by 30 · see citing works
Ragusa, M. A., Naselli, F., Cruciata, I., Volpes, S., Schimmenti, C., Serio, G., Mauro, M., Librizzi, M., Luparello, C., Chiarelli, R., et al. (2023) · Nutrients · doi:10.3390/nu15153495 · Cited by 30 · see citing works
Yan, S., Liu, L., Ren, F., Gao, Q., Xu, S., Hou, B., Wang, Y., Jiang, X., & Che, Y. (2017) · Cell Death and Disease · doi:10.1038/cddis.2017.387 · Cited by 30 · see citing works
Hersi, F., Omar, H. A., Al‐Qawasmeh, R. A., Ahmad, Z., Jaber, A. M., Zaher, D. M., & Al‐Tel, T. H. (2020) · Scientific Reports · doi:10.1038/s41598-020-59685-x · Cited by 29 · see citing works
López-Pérez, Ó., Otero, A., Filali, H., Sánz-Rubio, D., Toivonen, J. M., Zaragoza, P., Badiola, J. J., Bolea, R., & Martín‐Burriel, I. (2019) · Scientific Reports · doi:10.1038/s41598-019-38500-2 · Cited by 27 · see citing works
Therapeutic Potential for Targeting Autophagy in ER+ Breast Cancer
Finnegan, R., Elshazly, A. M., Schoenlein, P. V., & Gewirtz, D. A. (2022) · Cancers · doi:10.3390/cancers14174289 · Cited by 27 · see citing works
Costa, J. R., Prak, K., Aldous, S. G., Gewinner, C. A., & Ketteler, R. (2016) · Oncotarget · doi:10.18632/oncotarget.9754 · Cited by 25 · see citing works
Yang, M., Hao, Y., Gao, J., Zhang, Y., Xu, W., & Tao, L. (2017) · Comparative Biochemistry and Physiology Part C Toxicology & Pharmacology · doi:10.1016/j.cbpc.2017.02.008 · Cited by 24 · see citing works
LC3A Silencing Hinders Aggresome Vimentin Cage Clearance in Primary Choroid Plexus Carcinoma
Nassar, M., Samaha, H., Ghabriel, M., Yehia, M., Taha, H., Salem, S., Shaaban, K., Omar, M., Ahmed, N. M., & El‐Naggar, S. (2017) · Scientific Reports · doi:10.1038/s41598-017-07403-5 · Cited by 23 · see citing works
Colafrancesco, S., Vomero, M., Iannizzotto, V., Minniti, A., Barbati, C., Arienzo, F., Mastromanno, L., Colasanti, T., Izzo, R., Nayar, S., et al. (2020) · Arthritis Research & Therapy · doi:10.1186/s13075-020-02317-6 · Cited by 23 · see citing works
Wu, P.-S., Yen, J.-H., Wang, C., Chen, P., Hung, J., & Wu, M. (2020) · Biomedicines · doi:10.3390/biomedicines8110506 · Cited by 23 · see citing works
Mechanism of Pterostilbene-Induced Cell Death in HT-29 Colon Cancer Cells
Wawszczyk, J., Jesse, K., Smolik, S., & Kapral, M. (2022) · Molecules · doi:10.3390/molecules27020369 · Cited by 24 · see citing works
Cerrito, M. G., Giorgi, M. D., Pelizzoni, D., Bonomo, S., Digiacomo, N., Scagliotti, A., Bugarin, C., Gaipa, G., Grassilli, E., Lavitrano, M., et al. (2018) · Oncotarget · doi:10.18632/oncotarget.25422 · Cited by 23 · see citing works
Yang, M., Ramanathan, A., Glover, K., Stanley, C. B., Sanishvili, R., Chakravarthy, S., Yang, Z., Colbert, C. L., & Sinha, S. C. (2016) · Biochemistry · doi:10.1021/acs.biochem.5b01264 · Cited by 21 · see citing works
Kim, J., Kang, H., Yu, S., Song, J., Kim, C., Kim, B., Park, B.-S., Shin, S., & Kim, I. (2018) · Journal of Cellular Biochemistry · doi:10.1002/jcb.26728 · Cited by 22 · see citing works
Giatromanolaki, A. N., Kouroupi, M., Balaska, K., & Koukourakis, M. I. (2020) · In Vivo · doi:10.21873/invivo.12154 · Cited by 22 · see citing works
Pang, Z., Xu, Y. J., & Zhu, Q. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.773665 · Cited by 21 · see citing works
Manfredi, L. H., Ang, J., Peker, N., Dagda, R. K., & McFarlane, C. (2019) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00516.2018 · Cited by 21 · see citing works
Yan, H., Li, C., Zou, C., Xin, X. L., Li, X., Li, H., Li, Y., Li, Z., Wang, Y., Chen, H., et al. (2021) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2021.115440 · Cited by 21 · see citing works
Gioti, K., Papachristodoulou, A., Benaki, D. C., Beloukas, A. I., Vontzalidou, A., Aligiannis, N., Skaltsounis, A., Mikros, E., & Τέντα, Ρ. (2019) · Nutrition and Cancer · doi:10.1080/01635581.2019.1632357 · Cited by 20 · see citing works
Gioti, K., Papachristodoulou, A., Benaki, D. C., Havaki, S., Beloukas, A. I., Vontzalidou, A., Aligiannis, N., Skaltsounis, A., Mikros, E., & Τέντα, Ρ. (2019) · Planta Medica · doi:10.1055/a-0954-6704 · Cited by 20 · see citing works
Yang, P. C., Qin, Y., Zhu, Y. X., Li, F., Xia, S., Zhou, B., Wang, Q., Lu, J. L., Li, L., & Huang, H. (2020) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2020.112990 · Cited by 20 · see citing works
Katsaros, I., Sotiropoulou, M. G., Vailas, M. G., Papachristou, F., Papakyriakopoulou, P., Grigoriou, M. E., Kostomitsopoulos, N. G., Giatromanolaki, A. N., Valsami, G. N., Tsaroucha, A. K., et al. (2024) · Nutrients · doi:10.3390/nu16244282 · Cited by 19 · see citing works
Lin, H., Chang, Y., Chen, R.-Y., Hung, L., Chen, P. C.-H., Chen, Y., Medeiros, L. J., Chiang, P., & Chang, K. (2021) · Cancer Science · doi:10.1111/cas.14833 · Cited by 18 · see citing works
Racetin, A., Filipović, N., Lozić, M., Ogata, M., Ensor, L. G., Kelam, N., Kovačević, P., Watanabe, K., Katsuyama, Y., Saraga‐Babić, M., et al. (2021) · Biomolecules · doi:10.3390/biom11040609 · Cited by 17 · see citing works
Prabhakar, N., Merisaari, J., Joncour, V. L., Peurla, M., Karaman, D. Ş., Casals, E., Laakkonen, P. M., Westermarck, J. K., & Rosenholm, J. M. (2021) · Cancers · doi:10.3390/cancers13112631 · Cited by 17 · see citing works
Squiavinato, A. C. M. S., Ramos, D. A. A., Wagner, M. S., Tessmann, J. W., de‐Freitas‐Junior, J. C. M., & Morgado‐Díaz, J. A. (2022) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2022.175253 · Cited by 17 · see citing works
Berberine Inhibits MDA-MB-231 Cells as an Agonist of G Protein-Coupled Estrogen Receptor 1
Qi, M., Liu, X., Zhou, Y. F., Wang, H., Zhao, Y., Ren, J., & Xiang, J. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222111466 · Cited by 17 · see citing works
Li, A., Zhang, H., Han, H., Zhang, W., Yang, S., Huang, Z., Tan, J., & Yi, B. (2019) · Metabolism · doi:10.1016/j.metabol.2019.06.008 · Cited by 16 · see citing works
Kan, L. L., Liu, D., Chan, B. C.-L., Tsang, M. S., Hou, T., Leung, P., Lam, C. W.-K., & Wong, C. K. (2020) · Journal of Leukocyte Biology · doi:10.1002/jlb.3ma0720-682rr · Cited by 16 · see citing works
Alterations in antioxidant system, mitochondrial biogenesis and autophagy in preeclamptic myometrium
Vishnyakova, P., Volodina, M. A., Tarasova, N. V., Marey, M. V., Кан, Н. Е., Сагдуллаевна, Х. З., Vysokikh, M. Y., & Sukhikh, G. T. (2017) · BBA Clinical · doi:10.1016/j.bbacli.2017.06.002 · Cited by 16 · see citing works
Uzel, G., Oylumlu, E., Durmus, L., & Çıracı, C. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241713446 · Cited by 15 · see citing works
Moura-Martiniano, N. O., Machado-Ferreira, E., Gazêta, G. S., & Soares, C. A. G. (2017) · Experimental and Applied Acarology · doi:10.1007/s10493-017-0193-z · Cited by 15 · see citing works
Koukourakis, M. I., Giatromanolaki, A. N., Fylaktakidou, K. C., Sivridis, E., Zois, C. E., Kalamida, D., Mitrakas, A. G., Pouliliou, S., Karagounis, I. V., Simopoulos, K., et al. (2018) · Investigational New Drugs · doi:10.1007/s10637-018-0566-0 · Cited by 15 · see citing works
Polyamine supplementation reduces DNA damage in adipose stem cells cultured in 3-D
Minguzzi, M., Guidotti, S., Platano, D., D’Adamo, S., Cetrullo, S., Assirelli, E., Santi, S., Mariani, E., Trisolino, G., Filardo, G., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-50543-z · Cited by 15 · see citing works
The Clinical Influence of Autophagy-Associated Proteins on Human Lung Cancer
Chen, Y., Schnitzler, K. L., Ma, Y., Nenkov, M., Theis, B., & Petersen, I. (2018) · Disease Markers · doi:10.1155/2018/8314963 · Cited by 15 · see citing works
Normal-Tension Glaucoma and Potential Clinical Links to Alzheimer’s Disease
Ho, K., Bodi, N. E., & Sharma, T. P. (2024) · Journal of Clinical Medicine · doi:10.3390/jcm13071948 · Cited by 14 · see citing works
Monteiro, M. B., Pelaes, T. S., Santos‐Bezerra, D. P., Thieme, K., Lerário, A. M., Oba‐Shinjo, S. M., Machado, U. F., Passarelli, M., Marie, S. K. N., & Corrêa‐Giannella, M. L. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.00238 · Cited by 13 · see citing works
Chen, S.-L., Chou, H., Lin, K.-C., Yang, J., Xie, R., Chen, C., Liu, X.-Y., Chung, J. H.-Y., & Chen, G. (2021) · Materials Today Bio · doi:10.1016/j.mtbio.2021.100182 · Cited by 13 · see citing works
Kopiasz, Ł., Dziendzikowska, K., Oczkowski, M., Harasym, J., & Gromadzka-Ostrowska, J. (2023) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2023.127832 · Cited by 13 · see citing works
Havaki, S., Vlachou, V., Zampetidis, C., Selemenakis, P., Kotsinas, A., Mavrogonatou, E., Rizou, S. V., Kyrodimos, E., Evangelou, K., Kletsas, D., et al. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18091920 · Cited by 13 · see citing works
Wu, Q., Wang, B., Zhou, C., Lin, P., Qin, S., Gao, P., Wang, Z., Xia, Z., & Wu, M. (2019) · Immunology · doi:10.1111/imm.13108 · Cited by 13 · see citing works
Wu, Y., Boulogne, C., Carle, S., Podinovskaia, M., Barth, H., Spang, A., Cintrat, J., Gillet, D., & Barbier, J. (2020) · FEBS Journal · doi:10.1111/febs.15201 · Cited by 12 · see citing works
Transcranial Photosensitizer-Free Laser Treatment of Glioblastoma in Rat Brain
Semyachkina-Glushkovskaya, O. V., Sokolovski, S. G., Fedosov, I. V., Shirokov, A. A., Наволокин, Н. А., Bucharskaya, A. B., Андреевна, Б. И., Terskov, A. V., Dubrovsky, A. I., Telnova, V., et al. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241813696 · Cited by 11 · see citing works
Uppar, P. M., Kim, N. Y., Harish, K. K., Beeraka, N. M., Gaonkar, S. L., Mahendra, M., Sethi, G., Rangappa, K. S., Nikolenko, V. N., Chinnathambi, A., et al. (2025) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2025.111528 · Cited by 12 · see citing works
Panda, S. P., & Singh, V. (2023) · Molecular Neurobiology · doi:10.1007/s12035-023-03402-y · Cited by 11 · see citing works
Autophagy Modulation and Its Implications on Glioblastoma Treatment
Chen, J., Salinas, A., Morales, M. A., & Fang, X. (2023) · Current Issues in Molecular Biology · doi:10.3390/cimb45110546 · Cited by 11 · see citing works
García‐González, V., & Mas‐Oliva, J. (2017) · Scientific Reports · doi:10.1038/s41598-017-13880-5 · Cited by 11 · see citing works
Combining ADCs with Immuno-Oncology Agents
Müller, P., Rios‐Doria, J., Harper, J. W., & Cao, A. (2018) · Cancer drug discovery and develogment/Cancer drug discovery and development · doi:10.1007/978-3-319-78154-9_2 · Cited by 11 · see citing works
Lijie, G., Yueyue, Z., Zhu, N., Ling, W., Xuan, W., & Weijie, Y. (2019) · Cell Biology International · doi:10.1002/cbin.11097 · Cited by 12 · see citing works
Yoon, K., Kim, N., Park, Y., Kim, B. K., Park, J. H., Shin, C. M., Lee, D. H., & Surh, Y. (2019) · PLoS ONE · doi:10.1371/journal.pone.0211736 · Cited by 11 · see citing works
Yi, Y., Han, J., Zhao, L., Wang, C., Fang, Y., Wei, Q., Hu, L., Liu, J., Zhang, Y., & Wang, L. (2015) · Europe PMC (PubMed Central) · doi:10.3978/j.issn.1000-9604.2015.12.07 · Cited by 11 · see citing works
Simons, I. M., Mohrlüder, J., Feederle, R., Kremmer, E., Zobel, T., Dobner, J., Bleffert, N., Hoffmann, S., & Willbold, D. (2019) · Scientific Reports · doi:10.1038/s41598-018-36717-1 · Cited by 10 · see citing works
Jiang, Z., Lau, Y. K., Wu, M., Casal, M. L., & Smith, L. J. (2020) · Journal of Anatomy · doi:10.1111/joa.13305 · Cited by 10 · see citing works
Astaxanthin Protects Against Heat-induced Mitochondrial Alterations in Mouse Hypothalamus
Chen, Y., Yu, T., & Deuster, P. A. (2021) · Neuroscience · doi:10.1016/j.neuroscience.2021.09.010 · Cited by 10 · see citing works
Amer, N., Hesham, D., Al‐Shehaby, N., Elshoky, H. A., Amer, M., Magdeldin, S., Mansour, M., Abou‐Aisha, K., & El‐Naggar, S. (2024) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2024.107398 · Cited by 9 · see citing works
Sun, Y., Zhu, D., Kong, L., Du, W., Qu, L., Yang, Y., Rao, G.-X., Huang, F., & Tong, X. (2024) · International Immunopharmacology · doi:10.1016/j.intimp.2024.112996 · Cited by 9 · see citing works
Neri, S., Guidotti, S., Panichi, V., Minguzzi, M., Cattini, L., Platano, D., Ursini, F., Arciola, C. R., & Borzı̀, R. M. (2024) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2024.10.299 · Cited by 9 · see citing works
Suman, I., Jezidžić, A., Dobrić, D., Domitrović, R., & Domitrović, R. (2025) · Biology · doi:10.3390/biology14050527 · Cited by 9 · see citing works
The multifaceted roles of nucleophagy in cancer development and therapy
Zhao, L., Li, W., Luo, X., & Sheng, S. (2020) · Cell Biology International · doi:10.1002/cbin.11504 · Cited by 9 · see citing works
- Authors
- Koukourakis, M. I., Kalamida, D., Giatromanolaki, A., Zois, C. E., Sivridis, E., Pouliliou, S., Mitrakas, A., Gatter, K. C., & Harris, A. L.
- Affiliations
- Democritus University of Thrace (GR)
- John Radcliffe Hospital (GB)
- University of Oxford (GB)
- Corresponding author
- Koukourakis, Michael I.
- ORCID
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2015-09-17
- Volume
- 10
- Issue
- 9
- Pages
- e0137675
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC4574774
- OpenAlex
- W2300762239
- Cited by
- 183
- References
- 21
- Citations by year
- 2026: 13 · 2025: 12 · 2024: 27 · 2023: 16 · 2022: 16 · 2021: 17 · 2020: 19 · 2019: 24 · 2018: 13 · 2017: 14 · 2016: 11 · 2015: 1
- FWCI
- 10.15
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- Cancer Research UK (11359, 16466)
- National Institute for Health and Care Research (NF-SI-0611-10163)
- Topics
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ubiquitin and proteasome pathways
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Keywords
- LC3A, LC3B, LC3C, autophagosomes, autophagy, subcellular localization, nuclear localization, Beclin-1, nuclear export, nuclear import, leptomycin B, ivermectin, antibody specificity, cancer cell lines
- MeSH terms
- Beclin-1, Antibodies, Autophagy, Fatty Acids, Unsaturated, Gene Expression Regulation, Humans, Ivermectin, Membrane Proteins, Microtubule-Associated Proteins, Neoplasms, Macrolides, Active Transport, Cell Nucleus, RNA Interference, RNA, Small Interfering, Cell Line, Tumor, Apoptosis Regulatory Proteins, Human Umbilical Vein Endothelial Cells
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