Autophagy in cancer associated fibroblasts promotes tumor cell survival Role of hypoxia, HIF1 induction and NFκB activation in the tumor stromal microenvironment
Recently, using a co-culture system, we demonstrated that MCF7 epithelial cancer cells induce oxidative stress in adjacent cancer-associated fibroblasts, resulting in the autophagic/lysosomal degradation of stromal caveolin-1 (Cav-1). However, the detailed signaling mechanism(s) underlying this proc...
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| Published in: | Cell cycle (Georgetown, Tex.) Vol. 9; no. 17; pp. 3515 - 3533 |
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| Main Authors: | , , , , , , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
| Published: |
United States
Taylor & Francis
01.09.2010
Landes Bioscience |
| Subjects: | |
| ISSN: | 1538-4101, 1551-4005, 1551-4005 |
| Online Access: | Get full text |
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| Abstract | Recently, using a co-culture system, we demonstrated that MCF7 epithelial cancer cells induce oxidative stress in adjacent cancer-associated fibroblasts, resulting in the autophagic/lysosomal degradation of stromal caveolin-1 (Cav-1). However, the detailed signaling mechanism(s) underlying this process remain largely unknown. Here, we show that hypoxia is sufficient to induce the autophagic degradation of Cav-1 in stromal fibroblasts, which is blocked by the lysosomal inhibitor chloroquine. Concomitant with the hypoxia-induced degradation of Cav-1, we see the upregulation of a number of well-established autophagy/mitophagy markers, namely LC3, ATG16L, BNIP3, BNIP3L, HIF-1α and NFκB. In addition, pharmacological activation of HIF-1α drives Cav-1 degradation, while pharmacological inactivation of HIF-1 prevents the downregulation of Cav-1. Similarly, pharmacological inactivation of NFκB-another inducer of autophagy-prevents Cav-1 degradation. Moreover, treatment with an inhibitor of glutathione synthase, namely BSO, which induces oxidative stress via depletion of the reduced glutathione pool, is sufficient to induce the autophagic degradation of Cav-1. Thus, it appears that oxidative stress mediated induction of HIF1- and NFκB-activation in fibroblasts drives the autophagic degradation of Cav-1. In direct support of this hypothesis, we show that MCF7 cancer cells activate HIF-1α- and NFκB-driven luciferase reporters in adjacent cancer-associated fibroblasts, via a paracrine mechanism. Consistent with these findings, acute knock-down of Cav-1 in stromal fibroblasts, using an siRNA approach, is indeed sufficient to induce autophagy, with the upregulation of both lysosomal and mitophagy markers. How does the loss of stromal Cav-1 and the induction of stromal autophagy affect cancer cell survival? Interestingly, we show that a loss of Cav-1 in stromal fibroblasts protects adjacent cancer cells against apoptotic cell death. Thus, autophagic cancer-associated fibroblasts, in addition to providing recycled nutrients for cancer cell metabolism, also play a protective role in preventing the death of adjacent epithelial cancer cells. We demonstrate that cancer-associated fibroblasts upregulate the expression of TIGAR in adjacent epithelial cancer cells, thereby conferring resistance to apoptosis and autophagy. Finally, the mammary fat pads derived from Cav-1 (-/-) null mice show a hypoxia-like response in vivo, with the upregulation of autophagy markers, such as LC3 and BNIP3L. Taken together, our results provide direct support for the "Autophagic Tumor Stroma Model of Cancer Metabolism," and explain the exceptional prognostic value of a loss of stromal Cav-1 in cancer patients. Thus, a loss of stromal fibroblast Cav-1 is a biomarker for chronic hypoxia, oxidative stress and autophagy in the tumor microenvironment, consistent with its ability to predict early tumor recurrence, lymph node metastasis and tamoxifen-resistance in human breast cancers. Our results imply that cancer patients lacking stromal Cav-1 should benefit from HIF-inhibitors, NFκB-inhibitors, anti-oxidant therapies, as well as autophagy/lysosomal inhibitors. These complementary targeted therapies could be administered either individually or in combination, to prevent the onset of autophagy in the tumor stromal compartment, which results in a "lethal" tumor microenvironment. |
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| AbstractList | Recently, using a co-culture system, we demonstrated that MCF7 epithelial cancer cells induce oxidative stress in adjacent cancer-associated fibroblasts, resulting in the autophagic/lysosomal degradation of stromal caveolin-1 (Cav-1). However, the detailed signaling mechanism(s) underlying this process remain largely unknown. Here, we show that hypoxia is sufficient to induce the autophagic degradation of Cav-1 in stromal fibroblasts, which is blocked by the lysosomal inhibitor chloroquine. Concomitant with the hypoxia-induced degradation of Cav-1, we see the upregulation of a number of well-established autophagy/mitophagy markers, namely LC3, ATG16L, BNIP3, BNIP3L, HIF-1α and NFκB. In addition, pharmacological activation of HIF-1α drives Cav-1 degradation, while pharmacological inactivation of HIF-1 prevents the downregulation of Cav-1. Similarly, pharmacological inactivation of NFκB—another inducer of autophagy—prevents Cav-1 degradation. Moreover, treatment with an inhibitor of glutathione synthase, namely BSO, which induces oxidative stress via depletion of the reduced glutathione pool, is sufficient to induce the autophagic degradation of Cav-1. Thus, it appears that oxidative stress mediated induction of HIF1- and NFκB-activation in fibroblasts drives the autophagic degradation of Cav-1. In direct support of this hypothesis, we show that MCF7 cancer cells activate HIF-1α- and NFκB-driven luciferase reporters in adjacent cancer-associated fibroblasts, via a paracrine mechanism. Consistent with these findings, acute knockdown of Cav-1 in stromal fibroblasts, using an siRNA approach, is indeed sufficient to induce autophagy, with the upregulation of both lysosomal and mitophagy markers. How does the loss of stromal Cav-1 and the induction of stromal autophagy affect cancer cell survival? Interestingly, we show that a loss of Cav-1 in stromal fibroblasts protects adjacent cancer cells against apoptotic cell death. Thus, autophagic cancer-associated fibroblasts, in addition to providing recycled nutrients for cancer cell metabolism, also play a protective role in preventing the death of adjacent epithelial cancer cells. We demonstrate that cancer-associated fibroblasts upregulate the expression of TIGAR in adjacent epithelial cancer cells, thereby conferring resistance to apoptosis and autophagy. Finally, the mammary fat pads derived from Cav-1 (−/−) null mice show a hypoxia-like response in vivo, with the upregulation of autophagy markers, such as LC3 and BNIP3L. Taken together, our results provide direct support for the “autophagic tumor stroma model of cancer metabolism”, and explain the exceptional prognostic value of a loss of stromal Cav-1 in cancer patients. Thus, a loss of stromal fibroblast Cav-1 is a biomarker for chronic hypoxia, oxidative stress and autophagy in the tumor microenvironment, consistent with its ability to predict early tumor recurrence, lymph node metastasis and tamoxifen-resistance in human breast cancers. Our results imply that cancer patients lacking stromal Cav-1 should benefit from HIF-inhibitors, NFκB-inhibitors, anti-oxidant therapies, as well as autophagy/lysosomal inhibitors. These complementary targeted therapies could be administered either individually or in combination, to prevent the onset of autophagy in the tumor stromal compartment, which results in a “lethal” tumor microenvironment. Recently, using a co-culture system, we demonstrated that MCF7 epithelial cancer cells induce oxidative stress in adjacent cancer-associated fibroblasts, resulting in the autophagic/lysosomal degradation of stromal caveolin-1 (Cav-1). However, the detailed signaling mechanism(s) underlying this process remain largely unknown. Here, we show that hypoxia is sufficient to induce the autophagic degradation of Cav-1 in stromal fibroblasts, which is blocked by the lysosomal inhibitor chloroquine. Concomitant with the hypoxia-induced degradation of Cav-1, we see the upregulation of a number of well-established autophagy/mitophagy markers, namely LC3, ATG16L, BNIP3, BNIP3L, HIF-1α and NFκB. In addition, pharmacological activation of HIF-1α drives Cav-1 degradation, while pharmacological inactivation of HIF-1 prevents the downregulation of Cav-1. Similarly, pharmacological inactivation of NFκB--another inducer of autophagy-prevents Cav-1 degradation. Moreover, treatment with an inhibitor of glutathione synthase, namely BSO, which induces oxidative stress via depletion of the reduced glutathione pool, is sufficient to induce the autophagic degradation of Cav-1. Thus, it appears that oxidative stress mediated induction of HIF1- and NFκB-activation in fibroblasts drives the autophagic degradation of Cav-1. In direct support of this hypothesis, we show that MCF7 cancer cells activate HIF-1α- and NFκB-driven luciferase reporters in adjacent cancer-associated fibroblasts, via a paracrine mechanism. Consistent with these findings, acute knock-down of Cav-1 in stromal fibroblasts, using an siRNA approach, is indeed sufficient to induce autophagy, with the upregulation of both lysosomal and mitophagy markers. How does the loss of stromal Cav-1 and the induction of stromal autophagy affect cancer cell survival? Interestingly, we show that a loss of Cav-1 in stromal fibroblasts protects adjacent cancer cells against apoptotic cell death. Thus, autophagic cancer-associated fibroblasts, in addition to providing recycled nutrients for cancer cell metabolism, also play a protective role in preventing the death of adjacent epithelial cancer cells. We demonstrate that cancer-associated fibroblasts upregulate the expression of TIGAR in adjacent epithelial cancer cells, thereby conferring resistance to apoptosis and autophagy. Finally, the mammary fat pads derived from Cav-1 (-/-) null mice show a hypoxia-like response in vivo, with the upregulation of autophagy markers, such as LC3 and BNIP3L. Taken together, our results provide direct support for the "Autophagic Tumor Stroma Model of Cancer Metabolism", and explain the exceptional prognostic value of a loss of stromal Cav-1 in cancer patients. Thus, a loss of stromal fibroblast Cav-1 is a biomarker for chronic hypoxia, oxidative stress and autophagy in the tumor microenvironment, consistent with its ability to predict early tumor recurrence, lymph node metastasis and tamoxifen-resistance in human breast cancers. Our results imply that cancer patients lacking stromal Cav-1 should benefit from HIF-inhibitors, NFκB-inhibitors, anti-oxidant therapies, as well as autophagy/lysosomal inhibitors. These complementary targeted therapies could be administered either individually or in combination, to prevent the onset of autophagy in the tumor stromal compartment, which results in a "lethal" tumor microenvironment.Recently, using a co-culture system, we demonstrated that MCF7 epithelial cancer cells induce oxidative stress in adjacent cancer-associated fibroblasts, resulting in the autophagic/lysosomal degradation of stromal caveolin-1 (Cav-1). However, the detailed signaling mechanism(s) underlying this process remain largely unknown. Here, we show that hypoxia is sufficient to induce the autophagic degradation of Cav-1 in stromal fibroblasts, which is blocked by the lysosomal inhibitor chloroquine. Concomitant with the hypoxia-induced degradation of Cav-1, we see the upregulation of a number of well-established autophagy/mitophagy markers, namely LC3, ATG16L, BNIP3, BNIP3L, HIF-1α and NFκB. In addition, pharmacological activation of HIF-1α drives Cav-1 degradation, while pharmacological inactivation of HIF-1 prevents the downregulation of Cav-1. Similarly, pharmacological inactivation of NFκB--another inducer of autophagy-prevents Cav-1 degradation. Moreover, treatment with an inhibitor of glutathione synthase, namely BSO, which induces oxidative stress via depletion of the reduced glutathione pool, is sufficient to induce the autophagic degradation of Cav-1. Thus, it appears that oxidative stress mediated induction of HIF1- and NFκB-activation in fibroblasts drives the autophagic degradation of Cav-1. In direct support of this hypothesis, we show that MCF7 cancer cells activate HIF-1α- and NFκB-driven luciferase reporters in adjacent cancer-associated fibroblasts, via a paracrine mechanism. Consistent with these findings, acute knock-down of Cav-1 in stromal fibroblasts, using an siRNA approach, is indeed sufficient to induce autophagy, with the upregulation of both lysosomal and mitophagy markers. How does the loss of stromal Cav-1 and the induction of stromal autophagy affect cancer cell survival? Interestingly, we show that a loss of Cav-1 in stromal fibroblasts protects adjacent cancer cells against apoptotic cell death. Thus, autophagic cancer-associated fibroblasts, in addition to providing recycled nutrients for cancer cell metabolism, also play a protective role in preventing the death of adjacent epithelial cancer cells. We demonstrate that cancer-associated fibroblasts upregulate the expression of TIGAR in adjacent epithelial cancer cells, thereby conferring resistance to apoptosis and autophagy. Finally, the mammary fat pads derived from Cav-1 (-/-) null mice show a hypoxia-like response in vivo, with the upregulation of autophagy markers, such as LC3 and BNIP3L. Taken together, our results provide direct support for the "Autophagic Tumor Stroma Model of Cancer Metabolism", and explain the exceptional prognostic value of a loss of stromal Cav-1 in cancer patients. Thus, a loss of stromal fibroblast Cav-1 is a biomarker for chronic hypoxia, oxidative stress and autophagy in the tumor microenvironment, consistent with its ability to predict early tumor recurrence, lymph node metastasis and tamoxifen-resistance in human breast cancers. Our results imply that cancer patients lacking stromal Cav-1 should benefit from HIF-inhibitors, NFκB-inhibitors, anti-oxidant therapies, as well as autophagy/lysosomal inhibitors. These complementary targeted therapies could be administered either individually or in combination, to prevent the onset of autophagy in the tumor stromal compartment, which results in a "lethal" tumor microenvironment. Recently, using a co-culture system, we demonstrated that MCF7 epithelial cancer cells induce oxidative stress in adjacent cancer-associated fibroblasts, resulting in the autophagic/lysosomal degradation of stromal caveolin-1 (Cav-1). However, the detailed signaling mechanism(s) underlying this process remain largely unknown. Here, we show that hypoxia is sufficient to induce the autophagic degradation of Cav-1 in stromal fibroblasts, which is blocked by the lysosomal inhibitor chloroquine. Concomitant with the hypoxia-induced degradation of Cav-1, we see the upregulation of a number of well-established autophagy/mitophagy markers, namely LC3, ATG16L, BNIP3, BNIP3L, HIF-1α and NFκB. In addition, pharmacological activation of HIF-1α drives Cav-1 degradation, while pharmacological inactivation of HIF-1 prevents the downregulation of Cav-1. Similarly, pharmacological inactivation of NFκB--another inducer of autophagy-prevents Cav-1 degradation. Moreover, treatment with an inhibitor of glutathione synthase, namely BSO, which induces oxidative stress via depletion of the reduced glutathione pool, is sufficient to induce the autophagic degradation of Cav-1. Thus, it appears that oxidative stress mediated induction of HIF1- and NFκB-activation in fibroblasts drives the autophagic degradation of Cav-1. In direct support of this hypothesis, we show that MCF7 cancer cells activate HIF-1α- and NFκB-driven luciferase reporters in adjacent cancer-associated fibroblasts, via a paracrine mechanism. Consistent with these findings, acute knock-down of Cav-1 in stromal fibroblasts, using an siRNA approach, is indeed sufficient to induce autophagy, with the upregulation of both lysosomal and mitophagy markers. How does the loss of stromal Cav-1 and the induction of stromal autophagy affect cancer cell survival? Interestingly, we show that a loss of Cav-1 in stromal fibroblasts protects adjacent cancer cells against apoptotic cell death. Thus, autophagic cancer-associated fibroblasts, in addition to providing recycled nutrients for cancer cell metabolism, also play a protective role in preventing the death of adjacent epithelial cancer cells. We demonstrate that cancer-associated fibroblasts upregulate the expression of TIGAR in adjacent epithelial cancer cells, thereby conferring resistance to apoptosis and autophagy. Finally, the mammary fat pads derived from Cav-1 (-/-) null mice show a hypoxia-like response in vivo, with the upregulation of autophagy markers, such as LC3 and BNIP3L. Taken together, our results provide direct support for the "Autophagic Tumor Stroma Model of Cancer Metabolism", and explain the exceptional prognostic value of a loss of stromal Cav-1 in cancer patients. Thus, a loss of stromal fibroblast Cav-1 is a biomarker for chronic hypoxia, oxidative stress and autophagy in the tumor microenvironment, consistent with its ability to predict early tumor recurrence, lymph node metastasis and tamoxifen-resistance in human breast cancers. Our results imply that cancer patients lacking stromal Cav-1 should benefit from HIF-inhibitors, NFκB-inhibitors, anti-oxidant therapies, as well as autophagy/lysosomal inhibitors. These complementary targeted therapies could be administered either individually or in combination, to prevent the onset of autophagy in the tumor stromal compartment, which results in a "lethal" tumor microenvironment. |
| Author | Capozza, Franco Zhou, Jie Pavlides, Stephanos Caro, Jaime Martinez-Cantarin, Maria P. Martinez-Outschoorn, Ubaldo E. Wang, Chenguang Howell, Anthony Lisanti, Michael P. Trimmer, Casey Whitaker-Menezes, Diana Witkiewicz, Agnieszka K. Sotgia, Federica Pestell, Richard G. Lin, Zhao Chiavarina, Barbara Flomenberg, Neal |
| AuthorAffiliation | 2 The Jefferson Stem Cell Biology and Regenerative Medicine Center; Thomas Jefferson University; Philadelphia, PA USA 5 Department of Pathology; Jefferson Center for Pancreatic, Biliary and Related Cancers; Thomas Jefferson University; Philadelphia, PA USA 6 Manchester Breast Centre & Breakthrough Breast Cancer Research Unit; Paterson Institute for Cancer Research; School of Cancer; Enabling Sciences and Technology; Manchester Academic Health Science Centre; University of Manchester; Manchester, UK 1 Department of Medical Oncology; Thomas Jefferson University; Philadelphia, PA USA 7 Division of Hematology; Department of Medicine; Cardeza Foundation; Thomas Jefferson University; Philadelphia, PA USA 4 Division of Nephrology; Department of Medicine; Thomas Jefferson University; Philadelphia, PA USA 3 Departments of Stem Cell Biology & Regenerative Medicine and Cancer Biology; Kimmel Cancer Center; Thomas Jefferson University; Philadelphia, PA USA |
| AuthorAffiliation_xml | – name: 5 Department of Pathology; Jefferson Center for Pancreatic, Biliary and Related Cancers; Thomas Jefferson University; Philadelphia, PA USA – name: 7 Division of Hematology; Department of Medicine; Cardeza Foundation; Thomas Jefferson University; Philadelphia, PA USA – name: 6 Manchester Breast Centre & Breakthrough Breast Cancer Research Unit; Paterson Institute for Cancer Research; School of Cancer; Enabling Sciences and Technology; Manchester Academic Health Science Centre; University of Manchester; Manchester, UK – name: 2 The Jefferson Stem Cell Biology and Regenerative Medicine Center; Thomas Jefferson University; Philadelphia, PA USA – name: 1 Department of Medical Oncology; Thomas Jefferson University; Philadelphia, PA USA – name: 4 Division of Nephrology; Department of Medicine; Thomas Jefferson University; Philadelphia, PA USA – name: 3 Departments of Stem Cell Biology & Regenerative Medicine and Cancer Biology; Kimmel Cancer Center; Thomas Jefferson University; Philadelphia, PA USA |
| Author_xml | – sequence: 1 givenname: Ubaldo E. surname: Martinez-Outschoorn fullname: Martinez-Outschoorn, Ubaldo E. – sequence: 2 givenname: Casey surname: Trimmer fullname: Trimmer, Casey – sequence: 3 givenname: Zhao surname: Lin fullname: Lin, Zhao – sequence: 4 givenname: Diana surname: Whitaker-Menezes fullname: Whitaker-Menezes, Diana – sequence: 5 givenname: Barbara surname: Chiavarina fullname: Chiavarina, Barbara – sequence: 6 givenname: Jie surname: Zhou fullname: Zhou, Jie – sequence: 7 givenname: Chenguang surname: Wang fullname: Wang, Chenguang – sequence: 8 givenname: Stephanos surname: Pavlides fullname: Pavlides, Stephanos – sequence: 9 givenname: Maria P. surname: Martinez-Cantarin fullname: Martinez-Cantarin, Maria P. – sequence: 10 givenname: Franco surname: Capozza fullname: Capozza, Franco – sequence: 11 givenname: Agnieszka K. surname: Witkiewicz fullname: Witkiewicz, Agnieszka K. – sequence: 12 givenname: Neal surname: Flomenberg fullname: Flomenberg, Neal – sequence: 13 givenname: Anthony surname: Howell fullname: Howell, Anthony – sequence: 14 givenname: Richard G. surname: Pestell fullname: Pestell, Richard G. – sequence: 15 givenname: Jaime surname: Caro fullname: Caro, Jaime – sequence: 16 givenname: Michael P. surname: Lisanti fullname: Lisanti, Michael P. email: federica.sotgia@jefferson.edu – sequence: 17 givenname: Federica surname: Sotgia fullname: Sotgia, Federica email: federica.sotgia@jefferson.edu |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/20855962$$D View this record in MEDLINE/PubMed |
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| Cites_doi | 10.1073/pnas.92.5.1381 10.4161/auto.6.6.12574 10.1016/j.cell.2007.12.018 10.1074/jbc.M112274200 10.1073/pnas.0602235103 10.1016/j.cmet.2006.01.012 10.4161/cc.9.11.11848 10.1074/jbc.M001914200 10.1128/MCB.00166-09 10.1038/sj.cdd.4401838 10.4161/cbt.7.8.6220 10.4161/cc.8.23.10238 10.4161/cbt.8.11.8874 10.4161/auto.8822 10.2353/ajpath.2009.080658 10.1038/45257 10.4161/cbt.10.2.11983 10.1016/j.cmet.2006.02.002 10.1002/pros.20946 10.1016/j.cell.2006.05.036 10.2353/ajpath.2007.060661 10.1016/j.humpath.2008.06.018 10.1158/0008-5472.CAN-05-1235 10.1074/jbc.M205948200 10.4161/cc.9.16.12553 10.2353/ajpath.2009.080653 10.1002/emmm.201000073 10.1016/S0046-8177(96)90214-2 10.1128/MCB.25.17.7546-7556.2005 10.1002/hep.22753 10.1152/jn.1972.35.4.405 10.1073/pnas.95.20.11715 10.1016/j.cbi.2005.12.009 10.4161/cc.8.11.8544 10.2353/ajpath.2009.080873 10.1074/jbc.272.36.22642 10.4161/cc.9.12.12048 10.1074/jbc.M008340200 10.1038/nature06905 10.1158/1541-7786.MCR-07-0309 10.1074/jbc.M110970200 10.1016/j.ccr.2009.12.041 10.1016/j.cmet.2005.05.001 10.1093/emboj/17.22.6633 10.1113/jphysiol.2003.058131 10.1038/nrc1877 10.1158/0008-5472.CAN-07-5127 10.4161/cc.9.17.12721 10.2353/ajpath.2009.080924 10.1097/01.ju.0000138082.68045.48 10.4161/auto.8788 10.1074/jbc.M800102200 10.1038/emboj.2009.242 10.1016/j.bbrc.2005.08.111 10.1042/bj20021279 10.1038/emboj.2009.364 10.1111/j.1582-4934.2008.00615.x 10.1016/S0891-5849(00)00364-6 10.1038/nrc2618 10.1128/MCB.01396-08 10.1016/j.molcel.2004.08.025 10.1158/0008-5472.CAN-09-2211 10.1158/1078-0432.CCR-08-0732 10.1038/sj.onc.1209937 10.1074/jbc.272.26.16374 10.1038/sj.onc.1201661 |
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| References_xml | – ident: R28 doi: 10.1073/pnas.92.5.1381 – ident: R54 doi: 10.4161/auto.6.6.12574 – ident: R26 doi: 10.1016/j.cell.2007.12.018 – volume: 277 start-page: 16464 year: 2002 ident: R67 publication-title: J Biol Chem doi: 10.1074/jbc.M112274200 – ident: R14 doi: 10.1073/pnas.0602235103 – ident: R1 doi: 10.1016/j.cmet.2006.01.012 – ident: R44 doi: 10.4161/cc.9.11.11848 – ident: R11 doi: 10.1074/jbc.M001914200 – ident: R24 doi: 10.1128/MCB.00166-09 – ident: R12 doi: 10.1038/sj.cdd.4401838 – ident: R32 doi: 10.4161/cbt.7.8.6220 – ident: R63 doi: 10.4161/cc.8.23.10238 – ident: R36 doi: 10.4161/cbt.8.11.8874 – ident: R22 doi: 10.4161/auto.8822 – ident: R64 doi: 10.2353/ajpath.2009.080658 – ident: R25 doi: 10.1038/45257 – ident: R35 doi: 10.4161/cbt.10.2.11983 – ident: R2 doi: 10.1016/j.cmet.2006.02.002 – volume: 69 start-page: 991 year: 2009 ident: R60 publication-title: Prostate doi: 10.1002/pros.20946 – ident: R43 doi: 10.1016/j.cell.2006.05.036 – volume: 171 start-page: 1608 year: 2007 ident: R51 publication-title: Am J Pathol doi: 10.2353/ajpath.2007.060661 – ident: R55 doi: 10.1016/j.humpath.2008.06.018 – volume: 65 start-page: 9047 year: 2005 ident: R41 publication-title: Cancer Res doi: 10.1158/0008-5472.CAN-05-1235 – volume: 277 start-page: 40091 year: 2002 ident: R66 publication-title: J Biol Chem doi: 10.1074/jbc.M205948200 – ident: R39 doi: 10.4161/cc.9.16.12553 – ident: R68 doi: 10.2353/ajpath.2009.080653 – ident: R48 doi: 10.1002/emmm.201000073 – volume: 17 start-page: 158 year: 1968 ident: R65 publication-title: J Electron Microsc (Tokyo) – ident: R57 doi: 10.1016/S0046-8177(96)90214-2 – volume: 25 start-page: 7546 year: 2005 ident: R18 publication-title: Mol Cell Biol doi: 10.1128/MCB.25.17.7546-7556.2005 – volume: 49 start-page: 1297 year: 2009 ident: R59 publication-title: Hepatology doi: 10.1002/hep.22753 – volume: 35 start-page: 405 year: 1972 ident: R8 publication-title: J Neurophysiol doi: 10.1152/jn.1972.35.4.405 – ident: R10 doi: 10.1073/pnas.95.20.11715 – ident: R6 doi: 10.1016/j.cbi.2005.12.009 – ident: R37 doi: 10.4161/cc.8.11.8544 – ident: R33 doi: 10.2353/ajpath.2009.080873 – ident: R3 doi: 10.1074/jbc.272.36.22642 – ident: R40 doi: 10.4161/cc.9.12.12048 – ident: R62 doi: 10.1074/jbc.M008340200 – ident: R16 doi: 10.1038/nature06905 – volume: 6 start-page: 364 year: 2008 ident: R49 publication-title: Mol Cancer Res doi: 10.1158/1541-7786.MCR-07-0309 – volume: 277 start-page: 8635 year: 2002 ident: R45 publication-title: J Biol Chem doi: 10.1074/jbc.M110970200 – ident: R52 doi: 10.1016/j.ccr.2009.12.041 – ident: R4 doi: 10.1016/j.cmet.2005.05.001 – ident: R31 doi: 10.1093/emboj/17.22.6633 – volume: 556 start-page: 175 year: 2004 ident: R9 publication-title: J Physiol doi: 10.1113/jphysiol.2003.058131 – ident: R38 doi: 10.4161/cc.8.23.10238 – ident: R27 doi: 10.1038/nrc1877 – ident: R58 doi: 10.1158/0008-5472.CAN-07-5127 – ident: R46 doi: 10.4161/cc.9.17.12721 – ident: R34 doi: 10.2353/ajpath.2009.080924 – volume: 172 start-page: 2421 year: 2004 ident: R61 publication-title: J Urol doi: 10.1097/01.ju.0000138082.68045.48 – ident: R23 doi: 10.4161/auto.8788 – ident: R19 doi: 10.1074/jbc.M800102200 – ident: R42 doi: 10.1038/emboj.2009.242 – volume: 338 start-page: 617 year: 2005 ident: R5 publication-title: Biochem Biophys Res Commun doi: 10.1016/j.bbrc.2005.08.111 – volume: 370 start-page: 1011 year: 2003 ident: R15 publication-title: Biochem J doi: 10.1042/bj20021279 – ident: R20 doi: 10.1038/emboj.2009.364 – volume: 13 start-page: 202 year: 2009 ident: R53 publication-title: J Cell Mol Med doi: 10.1111/j.1582-4934.2008.00615.x – ident: R47 doi: 10.1016/S0891-5849(00)00364-6 – ident: R50 doi: 10.1038/nrc2618 – ident: R21 doi: 10.1128/MCB.01396-08 – ident: R7 doi: 10.1016/j.molcel.2004.08.025 – ident: R17 doi: 10.1158/0008-5472.CAN-09-2211 – ident: R56 doi: 10.1158/1078-0432.CCR-08-0732 – volume: 25 start-page: 6717 year: 2006 ident: R13 publication-title: Oncogene doi: 10.1038/sj.onc.1209937 – ident: R29 doi: 10.1074/jbc.272.26.16374 – ident: R30 doi: 10.1038/sj.onc.1201661 |
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| Snippet | Recently, using a co-culture system, we demonstrated that MCF7 epithelial cancer cells induce oxidative stress in adjacent cancer-associated fibroblasts,... |
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| StartPage | 3515 |
| SubjectTerms | Animals Antirheumatic Agents - pharmacology Apoptosis Regulatory Proteins Autophagy Binding Biology Bioscience Breast Neoplasms - metabolism Breast Neoplasms - pathology Calcium Cancer Caveolin 1 - genetics Caveolin 1 - metabolism Cell Cell Hypoxia Cell Line, Tumor Cell Survival Chloroquine - pharmacology Coculture Techniques Cycle Female Fibroblasts - metabolism Glutathione Synthase - antagonists & inhibitors Glutathione Synthase - metabolism Humans Hypoxia-Inducible Factor 1, alpha Subunit - metabolism Intracellular Signaling Peptides and Proteins - metabolism Landes Membrane Proteins - metabolism Mice Mice, Knockout Microtubule-Associated Proteins - metabolism NF-kappa B - metabolism Organogenesis Oxidative Stress Paracrine Communication Proteins Proto-Oncogene Proteins - metabolism RNA Interference RNA, Small Interfering - metabolism Stromal Cells - metabolism Tumor Microenvironment Tumor Suppressor Proteins - metabolism Up-Regulation |
| Subtitle | Role of hypoxia, HIF1 induction and NFκB activation in the tumor stromal microenvironment |
| Title | Autophagy in cancer associated fibroblasts promotes tumor cell survival |
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| Volume | 9 |
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