Cited by 558Autophagy in Disease and TherapyCell death mechanisms and regulationUbiquitin and proteasome pathways

The DOI matches its Crossref record; 52 of the 52 references it cites were found in a registry or an index.

Induction of Autophagy during Extracellular Matrix Detachment Promotes Cell Survival

Open access

Fung, Christopher, Lock, Rebecca, Gao, Sizhen, Salas, Eduardo, Debnath, Jayanta·2008·Molecular Biology of the Cell

DOI 10.1091/mbc.e07-10-1092PMC PMC2262959

Open this paper in CoChat — free account

Abstract

Autophagy has been proposed to promote cell death during lumen formation in three-dimensional mammary epithelial acini because numerous autophagic vacuoles are observed in the dying central cells during morphogenesis. Because these central cells die due to extracellular matrix (ECM) deprivation (anoikis), we have directly interrogated how matrix detachment regulates autophagy. Detachment induces autophagy in both nontumorigenic epithelial lines and in primary epithelial cells. RNA interference-mediated depletion of autophagy regulators (ATGs) inhibits detachment-induced autophagy, enhances apoptosis, and reduces clonogenic recovery after anoikis. Remarkably, matrix-detached cells still exhibit autophagy when apoptosis is blocked by Bcl-2 overexpression, and ATG depletion reduces the clonogenic survival of Bcl-2-expressing cells after detachment. Finally, stable reduction of ATG5 or ATG7 in MCF-10A acini enhances luminal apoptosis during morphogenesis and fails to elicit long-term luminal filling, even when combined with apoptotic inhibition mediated by Bcl-2 overexpression. Thus, autophagy promotes epithelial cell survival during anoikis, including detached cells harboring antiapoptotic lesions.

Integrity signals

Registry

Crossref · 10.1091/mbc.e07-10-1092

Cites

52 of 52 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Repertoires of Autophagy in the Pathogenesis of Ocular Diseases
Li, Y., Jiang, Q. L., Cao, G.-F., Yao, J., & Yan, B. (2015) · Cellular Physiology and Biochemistry · doi:10.1159/000373980 · Cited by 16,351
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
Induction of the Vitamin D Receptor Attenuates Autophagy Dysfunction-Mediated Cell Death Following Traumatic Brain Injury
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
Dissemination and growth of cancer cells in metastatic sites
Chambers, A. F., Groom, A. C., & MacDonald, I. C. (2002) · Nature reviews. Cancer · doi:10.1038/nrc865 · Cited by 4,018
Development by Self-Digestion
Levine, B., & Klionsky, D. J. (2004) · Developmental Cell · doi:10.1016/s1534-5807(04)00099-1 · Cited by 3,728
Bcl-2 Antiapoptotic Proteins Inhibit Beclin 1-Dependent Autophagy
Pattingre, S., Tassa, A., Qu, X., Garuti, R., Liang, X. H., Mizushima, N., Packer, M., Schneider, M. D., & Levine, B. (2005) · Cell · doi:10.1016/j.cell.2005.07.002 · Cited by 3,536
Induction of autophagy and inhibition of tumorigenesis by beclin 1
Liang, X. H., Jackson, S., Seaman, M., Brown, K., Kempkes, B., Hibshoosh, H., & Levine, B. (1999) · Nature · doi:10.1038/45257 · Cited by 3,347
Disruption of epithelial cell-matrix interactions induces apoptosis
Frisch, S., & Francis, H. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.124.4.619 · Cited by 3,276
The role of autophagy during the early neonatal starvation period
Kuma, A., Hatano, M., Matsui, M., Yamamoto, A., Nakaya, H., Yoshimori, T., Ohsumi, Y., Tokuhisa, T., & Mizushima, N. (2004) · Nature · doi:10.1038/nature03029 · Cited by 2,865
Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene
Qu, X., Yu, J., Bhagat, G., Furuya, N., Hibshoosh, H., Troxel, A., Rosen, J., Eskelinen, E.-L., Mizushima, N., Ohsumi, Y., et al. (2003) · Journal of Clinical Investigation · doi:10.1172/jci20039 · Cited by 2,311

Flagged first, then by citations

Show all 52 references

Research works printed but not linked: 2

Frisch S. M., 1999, Methods Mol. Biol, 129, 251
Ogier-Denis E., 2003, Biochim. Biophys. Acta, 1603, 113

Sorted by citations

Items 301–400 of 558

Astrocyte elevated gene 1 (AEG‐1) promotes anoikis resistance and metastasis by inducing autophagy in hepatocellular carcinoma
Zhu, H., Liu, L., Deng, H., Li, Z., Sheng, J., He, X., Tian, D., & Li, P. (2019) · Journal of Cellular Physiology · doi:10.1002/jcp.29377 · Cited by 31
Autophagy protects PC12 cells against deoxynivalenol toxicity via the Class III PI3K/beclin 1/Bcl‐2 pathway
Wang, X., Jiang, Y., Zhu, L., Cao, L., Xu, W., Rahman, S. U., Feng, S., Li, Y., & Wu, J. (2020) · Journal of Cellular Physiology · doi:10.1002/jcp.29433 · Cited by 31
Dormancy in Breast Cancer, the Role of Autophagy, lncRNAs, miRNAs and Exosomes
Jahangiri, L., & Ishola, T. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23095271 · Cited by 31
The Regulators of Peroxisomal Acyl-Carnitine Shuttle CROT and CRAT Promote Metastasis in Melanoma
Lasheras-Otero, I., Feliu, I., Maillo, A., Moreno, H., Redondo-Muñoz, M., Aldaz, P., Bocanegra, A., Olías-Arjona, A., Lecanda, F., Fernández‐Irigoyen, J., et al. (2022) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2022.08.038 · Cited by 32
Cyclosporine A Induces Apoptotic and Autophagic Cell Death in Rat Pituitary GH3 Cells
Kim, H. S., Choi, S., Jeung, E., & Yoo, Y. (2014) · PLoS ONE · doi:10.1371/journal.pone.0108981 · Cited by 30
“Autophagy also protected epithelial cells from apoptotic cell death [31] during metabolic stress [32], drug treatment, and radiation damage for genotoxic ROS [33].”
Background
Olomoucine inhibits cathepsin L nuclear translocation, activates autophagy and attenuates toxicity of 6-hydroxydopamine
Fei, X., Qin, Z., Xiang, B., Li, L., Han, F., Fukunaga, K., & Liang, Z. (2009) · Brain Research · doi:10.1016/j.brainres.2009.01.057 · Cited by 30
Autophagy and thyroid carcinogenesis: genetic and epigenetic links
Morani, F., Titone, R., Pagano, L., Galetto, A., Alabiso, O., Aimaretti, G., & Isidoro, C. (2013) · Endocrine Related Cancer · doi:10.1530/erc-13-0271 · Cited by 30
“…a transient upregulation of autophagy is observed during the epithelial–mesenchymal transition (EMT; Akalay et al. 2013), and this function prevents the cell death by anoikis of cancer cells which have detached from the basement membrane to invade the extracellular matrix (Fung et al. 2008).”
Microenvironment and autophagy cross-talk: Implications in cancer therapy
Gomes, L. R., Vessoni, A. T., & Menck, C. F. M. (2016) · Pharmacological Research · doi:10.1016/j.phrs.2016.03.031 · Cited by 31
TRAIL receptor-induced features of epithelial-to-mesenchymal transition increase tumour phenotypic heterogeneity: potential cell survival mechanisms
Peyre, L., Meyer, M., Hofman, P. M., & Roux, J. (2020) · British Journal of Cancer · doi:10.1038/s41416-020-01177-w · Cited by 31
A functional outside-in signaling network of proteoglycans and matrix molecules regulating autophagy
Neill, T., Kapoor, A., Xie, C., Buraschi, S., & Iozzo, R. V. (2021) · Matrix Biology · doi:10.1016/j.matbio.2021.04.001 · Cited by 29
Autophagy promotes degradation of internalized collagen and regulates distribution of focal adhesions to suppress cell adhesion
Kawano, S., Torisu, T., Esaki, M., Torisu, K., Matsuno, Y., & Kitazono, T. (2017) · Biology Open · doi:10.1242/bio.027458 · Cited by 29
“Cell detachment from the matrix has been demonstrated as a trigger of autophagy, and autophagy protected cells from anoikis (Avivar-Valderas et al., 2011; Fung et al., 2008).”
Background
Autophagy regulates functional differentiation of mammary epithelial cells
Epps, J. L., Pearson, S. J., Payne, H. R., Barhoumi, R., Rijnkels, M., & Porter, W. W. (2020) · Autophagy · doi:10.1080/15548627.2020.1720427 · Cited by 33
“Finally, although other studies have shown that haploinsufficiency or knockdown of Atg7 in MECs results in enhanced cell death [27,28], we did not observe significant cell death or induction of CASP3 activity during peak differentiation time points in shAtg7 cells (data not shown).”
Result
The crucial role of vitamin C and its transporter (SVCT2) in bone marrow stromal cell autophagy and apoptosis
Sangani, R., Periyasamy‐Thandavan, S., Pathania, R., Ahmad, S., Kutiyanawalla, A., Kolhe, R. B., Bhattacharyya, M. H., Chutkan, N. B., Hunter, M., Hill, W., et al. (2015) · Stem Cell Research · doi:10.1016/j.scr.2015.06.002 · Cited by 29
Zidovudine-Mediated Autophagy Inhibition Enhances Mitochondrial Toxicity in Muscle Cells
Lin, H., Stankov, M. V., Hegermann, J., Budida, R., Panayotova‐Dimitrova, D., Schmidt, R. E., & Behrens, G. M. N. (2018) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01443-18 · Cited by 29
“pBABEpuro GFP-LC3 (plasmid 22405), generated by Jayanta Debnath (53), was purchased from Addgene.”
Method
Oxidized Phospholipids in Tumor Microenvironment Stimulate Tumor Metastasis via Regulation of Autophagy
Seok, J. K., Hong, E., Yang, G., Lee, H., Kim, S.-E., Liu, K., Kang, H. C., Cho, Y., Lee, H. S., & Lee, J. Y. (2021) · Cells · doi:10.3390/cells10030558 · Cited by 28
“In addition, autophagy is induced during cancer cell dissociation (anoikis) to promote survival and possibly metastasis [39].”
Background
Epstein-Barr Virus Latent Membrane Protein 2 Induces Autophagy To Promote Abnormal Acinus Formation
Fotheringham, J., & Raab‐Traub, N. (2015) · Journal of Virology · doi:10.1128/jvi.03371-14 · Cited by 31
IRON METABOLISM AND AUTOPHAGY: A POORLY EXPLORED RELATIONSHIP THAT HAS IMPORTANT CONSEQUENCES FOR HEALTH AND DISEASE.
Krishan, S., Jansson, P. J., Gutierrez, E., Lane, D. J. R., Richardson, D. R., & Sahni, S. (2015) · PubMed Central · doi:10.18999/nagjms.77.1-2.1 · Cited by 28
Involvement of HuR in the serum starvation induced autophagy through regulation of Beclin1 in breast cancer cell-line, MCF-7
De, S., Das, S., & Sengupta, S. (2019) · Cellular Signalling · doi:10.1016/j.cellsig.2019.05.008 · Cited by 26
The Hippo network kinase STK38 contributes to protein homeostasis by inhibiting BAG3-mediated autophagy
Klimek, C., Jahnke, R., Wördehoff, J., Kathage, B., Stadel, D., Behrends, C., Hergovich, A., & Höhfeld, J. (2019) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2019.07.007 · Cited by 28
“The autophagic degradation of mechanotransducers and adhesion complexes prevents cell death, when cells are deprived of extra cellular matrix contacts, and mitophagy would limit the production of reactive oxygen species in this situation [46,64 – 66].”
Background
Alphavbeta3 integrin blocking inhibits apoptosis and induces autophagy in murine breast tumor cells
Lino, R. L. B., dos Santos, P. K., Pisani, G. F. D., Altei, W. F., Cominetti, M. R., & Selistre-de-Araújo, H. S. (2019) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2019.118536 · Cited by 28
High expression of the autophagy gene Beclin‐1 is associated with favorable prognosis for salivary gland adenoid cystic carcinoma
Liang, L., Ma, B., Liang, Y., Liu, H., Zheng, G., Zhang, T., Chu, M., Xu, P., Su, Y., & Liao, G. (2012) · Journal of Oral Pathology and Medicine · doi:10.1111/j.1600-0714.2012.01171.x · Cited by 27
Solid-phase inclusion as a mechanism for regulating unfolded proteins in the mitochondrial matrix
Ruan, L., McNamara, J. T., Zhang, X., Chang, A. C.-C., Zhu, J., Dong, Y., Sun, G. L., Peterson, A. F., Na, C. H., & Li, R. (2020) · Science Advances · doi:10.1126/sciadv.abc7288 · Cited by 24
Nanotherapeutics in autophagy: a paradigm shift in cancer treatment
Negi, S., Chaudhuri, A., Kumar, D. N., Dehari, D., Singh, S. K., & Agrawal, A. K. (2022) · Drug Delivery and Translational Research · doi:10.1007/s13346-022-01125-6 · Cited by 27
“It was shown that the knockout of Atg5 and Atg7 genes in the 3D culture model of MCF-10A induced pro-survival autophagy in the epithelial cells promoting cell survival during anoikis [50, 52].”
Background
Autophagy at the gut interface: Mucosal responses to stress and the consequences for inflammatory bowel diseases
Huett, A. S., & Xavier, R. J. (2009) · Inflammatory Bowel Diseases · doi:10.1002/ibd.20991 · Cited by 27
“In addition, models of detachmentinduced cell death have shown induction of autophagy following detachment from the extracellular matrix, inhibition of which resulted in increased levels of apoptotic cell death.(108,109) Therefore, defects in autophagy may alter the state of shed epithelial cells, as well as affect th…”
Background
Androgen receptor-induced integrin α6β1 and Bnip3 promote survival and resistance to PI3K inhibitors in castration-resistant prostate cancer
Nollet, E. A., Cardó‐Vila, M., Ganguly, S. S., Tran, J. D., Schulz, V. V., Cress, A. E., Corey, E., & Miranti, C. K. (2020) · Oncogene · doi:10.1038/s41388-020-1370-9 · Cited by 27
“pBABE-Puro GFP-LC3 (gift from Jayanta Debnath (Addgene plasmid # 22405)) [55] and selected with 2 μg/mL puromycin.”
Method
S100A8 transported by SEC23A inhibits metastatic colonization via autocrine activation of autophagy
Sun, Z., Zeng, B., Liu, D., Zhao, Q., Wang, J., & Xing, H. (2020) · Cell Death and Disease · doi:10.1038/s41419-020-02835-w · Cited by 25
The Role of Autophagy in Breast Cancer Metastasis
Kim, H. M., & Koo, J. S. (2023) · Biomedicines · doi:10.3390/biomedicines11020618 · Cited by 26
Inhibition of JNK-mediated autophagy enhances NSCLC cell sensitivity to mTORC1/2 inhibitors
Jin, H., Hong, S.-E., Park, J.-A., Chang, Y. H., Hong, Y. J., Park, I., & Lee, J. K. (2016) · Scientific Reports · doi:10.1038/srep28945 · Cited by 26
HSV‑TK/GCV can induce cytotoxicity of retinoblastoma cells through autophagy inhibition by activating MAPK/ERK
Yi, Q., Bai, Z.-S., Cai, B., Chen, N., Chen, L., Yuan, T., & Mao, J. (2018) · Oncology Reports · doi:10.3892/or.2018.6454 · Cited by 27
Triazole analog 1-(1-benzyl-5-(4-chlorophenyl)-1H-1,2,3-triazol-4-yl)-2-(4-bromophenylamino)-1-(4-chlorophenyl)ethanol induces reactive oxygen species and autophagy-dependent apoptosis in both in vitro and in vivo breast cancer models
Hamidullah, Saini, K. S., Ajay, A., Devender, N., Bhattacharjee, A., Das, S., Dwivedi, S., Gupt, M. P., Bora, H. K., Mitra, K., et al. (2015) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2015.06.016 · Cited by 26
New iron export pathways acting via holo-ferritin secretion
Yanatori, I., Kishi, F., & Toyokuni, S. (2023) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2023.109737 · Cited by 28
Functional Interactions between 17 β -Estradiol and Progesterone Regulate Autophagy during Acini Formation by Bovine Mammary Epithelial Cells in 3D Cultures
Zielniok, K., Motyl, T., & Gajewska, M. (2014) · BioMed Research International · doi:10.1155/2014/382653 · Cited by 25
“This effect might have resulted from the fact that Western blots were performed on lysates from whole spherical structures, which, as mentioned earlier, are composed of two distinct populations of cells: outer population, which remains in favorable conditions thanks to direct interactions with ECM, and inner populatio…”
BackgroundInfluential
Defective collagen proteostasis and matrix formation in the pathogenesis of lysosomal storage disorders
Settembre, C., Cinque, L., Bartolomeo, R., Malta, C. D., Leonibus, C. D., & Forrester, A. R. (2018) · Matrix Biology · doi:10.1016/j.matbio.2018.06.001 · Cited by 24
Autophagy in the mesh of collagen VI
Castagnaro, S., Gambarotto, L., Cescon, M., & Bonaldo, P. (2020) · Matrix Biology · doi:10.1016/j.matbio.2020.12.004 · Cited by 25
Oncoviruses: Induction of cancer development and metastasis by increasing anoikis resistance
Amjad, Z. S., Shojaeian, A., Nahand, J. S., Bayat, M., Taghizadieh, M., Rostamian, M., Babaei, F., & Moghoofei, M. (2023) · Heliyon · doi:10.1016/j.heliyon.2023.e22598 · Cited by 27
Angiostatic cues from the matrix: Endothelial cell autophagy meets hyaluronan biology
Chen, C. G., & Iozzo, R. V. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.rev120.014391 · Cited by 23
Functional genetic screen identifies ITPR3/calcium/RELB axis as a driver of colorectal cancer metastatic liver colonization
Moy, R. H., Nguyen, A., Loo, J. M., Yamaguchi, N., Kajba, C. M., Santhanam, B., Ostendorf, B. N., Wu, Y. G., Tavazoie, S., & Tavazoie, S. F. (2022) · Developmental Cell · doi:10.1016/j.devcel.2022.04.010 · Cited by 24
Involvement of redox signalling in tumour cell dormancy and metastasis
Puente-Cobacho, B., Varela‐López, A., Quiles, J. L., & Ramírez, L. V. (2023) · Cancer and Metastasis Reviews · doi:10.1007/s10555-022-10077-9 · Cited by 25
Suppression of autophagy by CUB domain‐containing protein 1 signaling is essential for anchorage‐independent survival of lung cancer cells
Uekita, T., Fujii, S., Miyazawa, Y., Hashiguchi, A., Abe, H., Sakamoto, M., & Sakai, R. (2013) · Cancer Science · doi:10.1111/cas.12154 · Cited by 24
Thymidine Analogues Suppress Autophagy and Adipogenesis in Cultured Adipocytes
Stankov, M. V., Panayotova‐Dimitrova, D., Leverkus, M., Schmidt, R. E., & Behrens, G. M. N. (2012) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01560-12 · Cited by 24
Resistance to hormone therapy in breast cancer cells promotes autophagy and EGFR signaling pathway
Siatis, K. E., Giannopoulou, E., Manou, D., Sarantis, P., Karamouzis, M. V., Raftopoulou, S., Fasseas, K., Alzahrani, F. M., Kalofonos, H. P., & Theocharis, A. D. (2023) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00199.2023 · Cited by 23
Autophagy-independent senescence and genome instability driven by targeted telomere dysfunction
Mar, F. A., Debnath, J., & Stohr, B. A. (2015) · Autophagy · doi:10.1080/15548627.2015.1017189 · Cited by 23
“Immunoblotting for LC3-II was performed with a 1:1000 dilution of LC3B antibody that has been previously described and is now commercially available (EMD Millipore, ABC232).(51) Immunoblotting for ATG5 was performed using a 1:500 dilution of ATG5 antibody (Cell Signaling Technology, 2630).”
MethodSelf-citation
Loss of the ubiquitin conjugating enzyme UBE2E3 induces cellular senescence
Plafker, K. S., Zyla, K., Berry, W. L., & Plafker, S. M. (2018) · Redox Biology · doi:10.1016/j.redox.2018.05.008 · Cited by 24
“To assess autophagic flux, we generated an RPE-1 cell line stably expressing GFP-tagged LC3 (GFP-LC3), a reliable proxy for monitoring autophagy [14,40].”
Method
A Key Pathway to Cancer Resilience: The Role of Autophagy in Glioblastomas
Jandrey, E. H. F., Bezerra, M., Inoue, L. T., Furnari, F. B., Camargo, A. A., & Costa, É. T. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.652133 · Cited by 27
Cell adhesion suppresses autophagy via Src/FAK-mediated phosphorylation and inhibition of AMPK
Zhao, M., Finlay, D., Kwong, E. M., Liddington, R., Viollet, B., Sasaoka, N., & Vuori, K. (2021) · Cellular Signalling · doi:10.1016/j.cellsig.2021.110170 · Cited by 23
MicroRNAs in Hepatocellular Carcinoma Pathogenesis: Insights into Mechanisms and Therapeutic Opportunities
Mahboobnia, K., Beveridge, D. J., Yeoh, G. C., Kabir, T. D., & Leedman, P. J. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25179393 · Cited by 23
“ACD suppresses tumor initiation and malignant transformation [87] but also promotes the survival of tumor cells, metastatic progression, and drug resistance by providing substrates for cellular metabolism [88,89].”
Background
Autophagy blockade sensitizes the anticancer activity of CA-4 via JNK-Bcl-2 pathway
Li, Y., Luo, P., Wang, J., Dai, J., Yang, X., Wu, H., Yang, B., & He, Q. (2013) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2013.11.018 · Cited by 23
“The optimal sense sequences of the Atg5, Beclin 1 and JNK-1 siRNA were and 5′-3′ GGAA UAUCCUGCAGAAGAAUU, 5′-3′ CAGTTTGGCACAATCAATA, and 5′-3′ UCACAGUCCUGAAACGAUATT, respectively (Fung et al., 2008; Shen et al., 2008; Zhao et al., 2010).”
Background
Interleukin‐8 enhances myocilin expression, Akt‐FoxO3 signaling and myogenic differentiation in rat skeletal muscle cells
Milewska, M., Domoradzki, T., Majewska, A., Błaszczyk, M., Gajewska, M., Hulanicka, M., Ciecierska, A., & Grzelkowska‐Kowalczyk, K. (2019) · Journal of Cellular Physiology · doi:10.1002/jcp.28568 · Cited by 24
LT-IIc, A Bacterial Type II Heat-Labile Enterotoxin, Induces Specific Lethality in Triple Negative Breast Cancer Cells by Modulation of Autophagy and Induction of Apoptosis and Necroptosis
Masso‐Welch, P. A., Girald-Berlingeri, S. A., King-Lyons, N. D., Mandell, L. M., Hu, J. C., Greene, C., Federowicz, M., Cao, P., Connell, T. D., & Heakal, Y. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms20010085 · Cited by 22
“Activated autophagic flux enables cells to resist detachment-associated cell death (anoikis resistance), which is a critical early step for the development of distal metastases [58].”
Background
Cadmium-induced autophagy promotes survival of rat cerebral cortical neurons by activating class III phosphoinositide 3-kinase/beclin-1/B-cell lymphoma 2 signaling pathways
WANG, Q.-W., WANG, Y., Wang, T., ZHANG, K.-B., JIANG, C.-Y., Hu, F., Yuan, Y., Bian, J., Liu, X., Gu, J., et al. (2015) · Molecular Medicine Reports · doi:10.3892/mmr.2015.3755 · Cited by 22
“The present study further confirmed that disrupting Bcl‑2/beclin-1 interactions may be a mechanism used by cells to promote autophagy and cell survival during conditions of stress (38,39).”
A functional role for NS 5 ATP 9 in the induction of HCV NS 5A‐mediated autophagy
Quan, M., Liu, S., Li, G., Wang, Q., Zhang, J., Zhang, M., Li, M., Gao, P., Feng, S., & Cheng, J. (2013) · Journal of Viral Hepatitis · doi:10.1111/jvh.12155 · Cited by 22
HCaRG/COMMD5 inhibits ErbB receptor-driven renal cell carcinoma
Matsuda, H., Campion, C. G., Fujiwara, K., Ikeda, J., Cossette, S., Verissimo, T., Ogasawara, M., Gaboury, L. A., Saito, K., Yamaguchi, K., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.18012 · Cited by 22
“Autophagy can help cancer cells to survive under hypoxia or insufficient nutritional condition [40].”
Background
Autophagy and Mitochondrial Homeostasis During Infection: A Double-Edged Sword
Wang, S., Zhang, K., Yao, Y., & Li, J. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.738932 · Cited by 24
“Inhibition of expression of ATG5 and ATG7 promotes anoikis of cancer cell via suppression of autophagy (Fung et al., 2008).”
Background
Autophagy in brain tumors: molecular mechanisms, challenges, and therapeutic opportunities
Zhang, J., Jinan, Z., & Chen, Y. (2025) · Journal of Translational Medicine · doi:10.1186/s12967-024-06063-0 · Cited by 24
Decoding the dual role of autophagy in cancer through transcriptional and epigenetic regulation
Yu, Y. S., Kim, I. S., & Baek, S. H. (2025) · FEBS Letters · doi:10.1002/1873-3468.70060 · Cited by 24
“For example, in a 3D culture model of MCF-10A cells, knockdown of ATG5 or ATG7 induced anoikis [32].”
Apoptosis-Like Cell Death Induction and Aberrant Fibroblast Properties in Human Incisional Hernia Fascia
Díaz, R., Quiles, M., Guillem‐Marti, J., Cano, M. L., Huguet, P., y Cajal, S. R., Reventós, J., Armengol, M., & Arbos, M. A. (2011) · American Journal Of Pathology · doi:10.1016/j.ajpath.2011.02.044 · Cited by 24
Recent advancement of autophagy in polyploid giant cancer cells and its interconnection with senescence and stemness for therapeutic opportunities
Patra, S., Naik, P. P., Mahapatra, K. K., Alotaibi, M. R., Patil, S., Patro, B. S., Sethi, G., Efferth, T., & Bhutia, S. K. (2024) · Cancer Letters · doi:10.1016/j.canlet.2024.216843 · Cited by 20
Cell adhesion molecule IGPR-1 activates AMPK connecting cell adhesion to autophagy
Amraei, R., Alwani, T., Ho, R. X.-Y., Aryan, Z., Wang, S., & Rahimi, N. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.ra120.014790 · Cited by 20
Molecular regulation of autophagy in a pro-inflammatory tumour microenvironment: New insight into the role of serum amyloid A
du Plessis, M., Davis, T., Loos, B., Pretorius, E., de Villiers, W. J. S., & Engelbrecht, A. (2021) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2021.01.007 · Cited by 20
Emerging Role of Autophagy in the Development and Progression of Oral Squamous Cell Carcinoma
El-Aziz, Y. S. A., Leck, L. Y. W., Jansson, P. J., & Sahni, S. (2021) · Cancers · doi:10.3390/cancers13246152 · Cited by 22
Role of autophagy in mammary gland development.
Gajewska, M., Sobolewska, A., Kozlowski, M., & Motyl, T. (2008) · PubMed · Cited by 20
The Role of Macroautophagy and Chaperone-Mediated Autophagy in the Pathogenesis and Management of Hepatocellular Carcinoma
Karampa, A. D., GOUSSIA, A. C., Glantzounis, G. K., Mastoridou, E. M., Anastasopoulos, N.-A., & Charchanti, A. V. (2022) · Cancers · doi:10.3390/cancers14030760 · Cited by 20
“Interestingly, autophagy flux is upregulated when the metastatic site is established to promote cancer cell survival in new hostile conditions, such as hypoxia, nutrient deprivation, and detachment from the ECM [84,89].”
Background
Nanomechanical Induction of Autophagy‐Related Fluorescence in Single Cells with Atomic Force Microscopy
Li, B., Wei, Y., Li, Q., Chen, N., Li, J., Liu, L., Zhang, J., Wang, Y., Sun, Y., Shi, J., et al. (2021) · Advanced Science · doi:10.1002/advs.202102989 · Cited by 19
Advancements in precision nanomedicine design targeting the anoikis-platelet interface of circulating tumor cells
Tang, M., Zhang, Z., Wang, P., Zhao, F., Miao, L., Wang, Y., Li, Y., Li, Y., & Gao, Z. (2024) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2024.04.034 · Cited by 19
“It acts as a robust survival pathway during ECM detachment and under hypoxia, enhancing cell resilience until reattachment and signiﬁcantly fortifying resistance to anoikis 90 .”
Background
Gammaherpesvirus 68 Infection of Endothelial Cells Requires both Host Autophagy Genes and Viral Oncogenes for Optimal Survival and Persistence
Suárez, A. L., Kong, R., George, T., He, L., Yue, Z., & van Dyk, L. F. (2011) · Journal of Virology · doi:10.1128/jvi.00001-11 · Cited by 19
“To inhibit autophagy in ECs, we used established siRNA oligonucleotide pools targeting murine ATG7 and ATG12 (14).”
BackgroundMethodInfluential
Cancer stem cells and autophagy: Facts and Perspectives
Hamaï, A., Codogno, P., & Mehrpour, M. (2014) · Journal of Cancer Stem Cell Research · doi:10.14343/jcscr.2014.2e1005 · Cited by 20
“In addition, metastasis induces prosurvival autophagy in epithelial cells to protect them from anoikis, and depletion of ATG protein enhances cell death and reduces clonogenic recovery after anoikis [124, 125].”
Background
Autophagy and radiosensitization in cancer
Sharma, K., Goehe, R. W., Beckta, J. M., Valerie, K. C., & Gewirtz, D. A. (2014) · Europe PMC (PubMed Central) · doi:10.17877/de290r-197 · Cited by 19
“Autophagy can play a critical role in cancer cell survival by allowing cells to survive under conditions of metabolic and genotoxic stress (Wilson et al., 2011; Michallet et al., 2011; Qiang et al., 2013; Fung et al., 2008).”
Background
Loss of TP53I11 Enhances the Extracellular Matrix‐independent Survival by Promoting Activation of AMPK
Xiao, T., Xu, Z., Zhou, Y., Zhang, H., Geng, J., Liang, Y., Qiao, H., & Suo, G. (2018) · IUBMB Life · doi:10.1002/iub.1949 · Cited by 19
Second generation of diazachrysenes: Protection of Ebola virus infected mice and mechanism of action
Selaković, Ž., Tran, J. P., Kota, K. P., Lazić, M., Retterer, C. J., Besch, R., Panchal, R. G., Soloveva, V., Sean, V. A., Jay, W. B., et al. (2018) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2018.10.061 · Cited by 19
Role of Autophagy in Cancer and Tumor Progression
Janji, B., Viry, E., Bagińska, J., Van, K. T., & Berchem, G. (2013) · InTech eBooks · doi:10.5772/55388 · Cited by 19
“have pointed out that autophagy is induced in both non-tumorigenic epithelial cell lines and in primary epithelial cells following the ECM detachment [118].”
Background
Autophagy and cancer metabolism—The two‐way interplay
Yan, R.-L., & Chen, R. (2021) · IUBMB Life · doi:10.1002/iub.2569 · Cited by 20
Dual Implications of Nanosilver-Induced Autophagy: Nanotoxicity and Anti-Cancer Effects
Strużyńska, L. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242015386 · Cited by 24
“Autophagy may also be protective in the progressive phase of the disease by increasing the survival of cancer cells during detachment from tumor, thus facilitating metastasis [42].”
Background
Nano delivery of natural substances as prospective autophagy modulators in glioblastoma
Agarwal, S., & Maekawa, T. (2020) · Nanomedicine Nanotechnology Biology and Medicine · doi:10.1016/j.nano.2020.102270 · Cited by 17
Cooperation of cell adhesion and autophagy in the brain: Functional roles in development and neurodegenerative disease
Hernandez, S. J., Fote, G., Reyes-Ortiz, A. M., Steffan, J. S., & Thompson, L. M. (2021) · Matrix Biology Plus · doi:10.1016/j.mbplus.2021.100089 · Cited by 17
“In mammary epithelial cells, antibody inhibition of integrin b1 in attached cells is sufficient to induce autophagy, while providing suspended cells a laminin-rich ECM suppresses autophagy, suggesting that integrin-mediated adhesion inhibits autophagic function [71].”
Background
PSMD2 contributes to the progression of esophageal squamous cell carcinoma by repressing autophagy
Liu, Y., Wu, M. Y., Xu, S., Niu, X., Liu, W., Miao, C., Lin, A., Xu, Y., & Yu, L. (2023) · Cell & Bioscience · doi:10.1186/s13578-023-01016-4 · Cited by 19
Targeting Degradation of EGFR through the Allosteric Site Leads to Cancer Cell Detachment-Promoted Death
Iradyan, M. A., Iradyan, N., Hulin, P., Hambardzumyan, A. A., Gyulkhandanyan, A., de Sousa, R. A., Hessani, A., Roussakis, C., Bollot, G., Bauvais, C., et al. (2019) · Cancers · doi:10.3390/cancers11081094 · Cited by 17
“EGF binding to EGFR mediates the MAPK/ERK pathway leading to phosphorylation of the Bcl-2 interacting mediator (Bim), the sensor protein, which subsequently binds to microtubules and actin to provide the attachment of α/β-integrins to the ECM and the integrity of cytoskeleton [21].”
BackgroundInfluential
Cellular FLIPL plays a survival role and regulates morphogenesis in breast epithelial cells
Yerbes, R., Palacios, C., Reginato, M. J., & López‐Rivas, A. (2010) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2010.10.003 · Cited by 17
Autophagic and proteolytic processes in the Harderian gland are modulated during the estrous cycle
Macia, M. G., Rubio‐González, A., de Luxán‐Delgado, B., Potes, Y., Rodríguez‐González, S., de Gonzalo‐Calvo, D., Boga, J. A., & Coto‐Montes, A. M. (2013) · Histochemistry and Cell Biology · doi:10.1007/s00418-013-1170-1 · Cited by 17
“Our previous studies showed that Type II cells have an essential role in massive autophagy and in provoking holocrine secretion (Vega-naredo et al. 2009), while Fung and coworkers (Fung et al. 2008) showed that cellular detachment is induced by autophagy.”
BackgroundResult
Autophagy facilitates secretion and protects against degeneration of the Harderian gland
Koenig, U., Fobker, M., Lengauer, B., Brandstetter, M., Resch, G. P., Gröger, M., Plenz, G. A. M., Pammer, J., Barresi, C., Hartmann, C., et al. (2014) · Autophagy · doi:10.4161/15548627.2014.978221 · Cited by 17
“In other glandular epithelial cells, cell detachment induces autophagy as a cytoprotective mechanism and in the Drosophila, the development of the salivary gland is delayed, when autophagy is inhibited.(80,81) Our experiments lead us to propose the following model to explain how autophagy facilitates secretion (see Fi…”
Background
Synergistic Interactions between Heregulin and Peroxisome Proliferator-activated Receptor-γ (PPARγ) Agonist in Breast Cancer Cells
Park, B.-H., Lee, S.-B., Stolz, D. B., Lee, Y. J., & Lee, B.-C. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.191718 · Cited by 16
MiR-181a-5p promotes anoikis by suppressing autophagy during detachment induction in the mammary epithelial cell line MCF10A
Wei, J., Li, Y.-C., Ma, Z., & Jin, Y. (2016) · Protein & Cell · doi:10.1007/s13238-016-0255-8 · Cited by 16
“LETTER MiR-181a-5p promotes anoikis by suppressing autophagy during detachment induction in the mammary epithelial cell line MCF10A”
Influential
Ribosome profiling reveals a functional role for autophagy in mRNA translational control
Goldsmith, J., Marsh, T., Asthana, S., Leidal, A. M., Suresh, D., Olshen, A. B., & Debnath, J. (2020) · Communications Biology · doi:10.1038/s42003-020-1090-2 · Cited by 17
Self-citation
c-Cbl targets active Src for autophagy
Cecconi, F. (2011) · Nature Cell Biology · doi:10.1038/ncb2413 · Cited by 16
Histone deacetylase inhibitors restore toxic BH3 domain protein expression in anoikis-resistant mammary and brain cancer stem cells, thereby enhancing the response to anti-ERBB1/ERBB2 therapy
Cruickshanks, N. A., Hamed, H. A., Booth, L. A., Tavallai, S., Jahangir, S., Sajithlal, G. B., Grant, S., Poklepovic, A. S., & Dent, P. (2013) · Cancer Biology & Therapy · doi:10.4161/cbt.26234 · Cited by 15
“Formation of ducts during development of the mammary gland involves the induction of anoikis in the lumen and anoikis resistance in these luminal cells is believed to be a part of the biology of early stage breast cancers.(2-5) Cancer cells, by their nature, are relatively speaking more able to suppress the induction…”
Background
Differential regulation of autophagy by STAU1 in alveolar rhabdomyosarcoma and non‐transformed skeletal muscle cells
Almasi, S., Parks, T. E. C., Ravel‐Chapuis, A., MacKenzie, A., Côté, J., Cowan, K. N., & Jasmin, B. J. (2021) · Cellular Oncology · doi:10.1007/s13402-021-00607-y · Cited by 14
“A growing body of evidence indicates a crucial role of autophagy in the development of anoikis-resistance in solid tumours [29] and enhancement of their metastasis [30].”
Background
Enhanced Autophagy of Adipose-Derived Stem Cells Grown on Chitosan Substrates
Yang, C.-M., Huang, Y.-J., & Hsu, S. (2015) · BioResearch open access · doi:10.1089/biores.2014.0032 · Cited by 15
Potential Therapeutic Agents Against Par-4 Target for Cancer Treatment: Where Are We Going?
Santos, R. V. C., de Sena, W. L. B., dos Santos, F. A., Filho, A. F. D. S., Pitta, M. G. D. R., Pitta, M. G. D. R., Rego, M. B. D. M., & Pereira, M. C. (2018) · Current Drug Targets · doi:10.2174/1389450120666181126122440 · Cited by 14
The cross-talk of autophagy and apoptosis in breast carcinoma: implications for novel therapies?
Seyrek, K., Wohlfromm, F., Espe, J., & Lavrik, I. N. (2022) · Biochemical Journal · doi:10.1042/bcj20210676 · Cited by 15
The docking protein p130Cas regulates cell sensitivity to proteasome inhibition
Zhao, M., & Vuori, K. (2011) · BMC Biology · doi:10.1186/1741-7007-9-73 · Cited by 14
“Interestingly, cell detachment can also induce autophagy, which offers protection from cell death and limits anoikis [32].”
Background
Autophagy in Tumor Immunity and Viral-Based Immunotherapeutic Approaches in Cancer
Amiri, A. Z., Malone, K., Beug, S. T., Alain, T., & Yeganeh, B. (2021) · Cells · doi:10.3390/cells10102672 · Cited by 14
“After colonization of destination organs, autophagic flux is activated to protect against hypoxia, nutrient deficiencies, and segregation from extracellular matrix [69,70].”
Background
Anopheles aquasalis transcriptome reveals autophagic responses to Plasmodium vivax midgut invasion
Santana, R. A. G., Oliveira, M., Rodriguez, I. C., da Silva, R. C. A., de Sousa, D. R. T., Ferreira, L. D. S., Lacerda, M., Monteiro, W. M., Abrantes, P., Guerra, M. D. G. V. B., et al. (2019) · Parasites & Vectors · doi:10.1186/s13071-019-3506-8 · Cited by 14
Chapter 25 Detachment‐Induced Autophagy In Three‐Dimensional Epithelial Cell Cultures
Debnath, J. (2009) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(08)03625-2 · Cited by 14
Self-citation
Oxidative pentose phosphate pathway inhibition is a key determinant of antimalarial induced cancer cell death
Salas, E., Roy, S., Marsh, T., Rubin, B. P., & Debnath, J. (2015) · Oncogene · doi:10.1038/onc.2015.348 · Cited by 14
Self-citation
Autophagy : Moving Benchside Promises to Patient Bedsides
Belaïd, A., Ndiaye, P. D., Filippakis, H., Roux, J., Röttinger, É., Graba, Y., Brest, P., Hofman, P. M., & Mograbi, B. (2015) · Current Cancer Drug Targets · doi:10.2174/156800961508151001102452 · Cited by 13
Microtubule disrupting agent‐mediated inhibition of cancer cell growth is associated with blockade of autophagic flux and simultaneous induction of apoptosis
Hasanain, M., Sahai, R., Pandey, P. K., Maheshwari, M., Choyal, K., Gandhi, D., Singh, A., Singh, K., Mitra, K., Datta, D. B., et al. (2020) · Cell Proliferation · doi:10.1111/cpr.12749 · Cited by 13
FAK Signaling in Rhabdomyosarcoma
Perrone, C., Pomella, S., Cassandri, M., Braghini, M. R., Pezzella, M., Locatelli, F., & Rota, R. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21228422 · Cited by 11
“Through autophagy, tumor cells can enzymatically degrade and recycle cytosolic components under stressful conditions such as the extracellular matrix (ECM) detachment and starvation [73,74].”
Background
Autophagy and Extracellular Vesicles in Colorectal Cancer: Interactions and Common Actors?
Auger, C., Christou, N., Brunel, A., Perraud, A., & Verdier, M. (2021) · Cancers · doi:10.3390/cancers13051039 · Cited by 14
Britannin, a sesquiterpene lactone induces ROS-dependent apoptosis in NALM-6, REH, and JURKAT cell lines and produces a synergistic effect with vincristine
Mohammadlou, H., Moghadam, M. H., Mohammadi, M. H., Yami, A., & Gharehbaghian, A. (2021) · Molecular Biology Reports · doi:10.1007/s11033-021-06572-x · Cited by 13
“cancer cells, but sometimes this happens in favor of the survival of cancer cells [21, 22].”
Background
ß3-Integrin Inhibits Lipopolysaccharide-Induced Autophagy in Cardiomyocytes via the Akt Signaling Pathway
Zhu, Y., Li, L., Gong, S., Yu, Y., Dai, H., Cai, G., & Yan, J. (2015) · Cardiology · doi:10.1159/000371489 · Cited by 13
Transcription of Autophagy Associated Gene Expression as Possible Predictors of a Colorectal Cancer Prognosis
Bednarczyk, M., Muc‐Wierzgoń, M., Dzięgielewska-Gęsiak, S., Fatyga, E., & Waniczek, D. (2023) · Biomedicines · doi:10.3390/biomedicines11020418 · Cited by 12
“At the same time, it acts as a cellular defense mechanism to prevent cancer cell death after treatment, contributes to cancer recurrence and metastasis, and inhibits anticancer therapy and cancer cell death [9,17,18].”
Background

Authors: Fung, C., Lock, R., Gao, S., Salas, E., & Debnath, J.
Affiliations: University of California, San Francisco (US)
Harvard University (US)
*Department of Pathology and
ORCID: Debnath, Jayanta
Venue: Molecular Biology of the Cell
Publisher: American Society for Cell Biology (ASCB)
Published: 2008-03
Volume: 19
Issue: 3
Pages: 797-806
ISSN: 1059-1524 (ISSN-L)
1939-4586
DOI: 10.1091/mbc.e07-10-1092
PMC: PMC2262959
OpenAlex: W2039403501
Cited by: 558
References: 52
Citations by year: 2026: 10 · 2025: 20 · 2024: 15 · 2023: 26 · 2022: 33 · 2021: 45 · 2020: 41 · 2019: 35 · 2018: 36 · 2017: 23 · 2016: 40 · 2015: 37 · 2014: 44 · 2013: 43 · 2012: 28
FWCI: 9.86
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Molecular Biology of the Cell (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Howard Hughes Medical Institute
American Association for Cancer Research
National Institutes of Health
Genentech
University of California, San Francisco
National Cancer Institute (K08CA098419)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ubiquitin and proteasome pathways
Keywords: autophagy, anoikis, extracellular matrix detachment, lumen formation, epithelial morphogenesis, apoptosis, Bcl-2, ATG5, ATG7, clonogenic survival, autophagy-related genes, mammary tumor cells
MeSH terms: Autophagy-Related Protein 5, Autophagy-Related Protein 7, Animals, Autophagy, Cell Adhesion, Cell Line, Cell Survival, Dogs, Epidermal Growth Factor, Epithelial Cells, Extracellular Matrix, Fibroblasts, Humans, Microtubule-Associated Proteins, Apoptosis, Proto-Oncogene Proteins c-bcl-2, Ubiquitin-Activating Enzymes, Mice, ErbB Receptors

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Induction of Autophagy during Extracellular Matrix Detachment Promotes Cell Survival

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks