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Current Cancer Drug Targets

Editor-in-Chief

ISSN (Print): 1568-0096
ISSN (Online): 1873-5576

Review Article

Role of Tumor Microenvironment in Cancer Stem Cells Resistance to Radiotherapy

Author(s): Shahram Taeb, Milad Ashrafizadeh, Ali Zarrabi, Saeed Rezapoor, Ahmed Eleojo Musa, Bagher Farhood and Masoud Najafi*

Volume 22, Issue 1, 2022

Published on: 31 January, 2022

Page: [18 - 30] Pages: 13

DOI: 10.2174/1568009622666211224154952

Price: $65

Abstract

Cancer is a chronic disorder that involves several elements of both the tumor and the host stromal cells. At present, the complex relationship between the various factors presents in the tumor microenvironment (TME) and tumor cells, as well as immune cells located within the TME, is still poorly known. Within the TME, the crosstalk of these factors and immune cells essentially determines how a tumor reacts to the treatment and how the tumor can ultimately be destroyed, remain dormant, or develop and metastasize. Also, in TME, reciprocal crosstalk between cancer-associated fibroblasts (CAFs), extracellular matrix (ECM), hypoxia-inducible factor (HIF) intensifies the proliferation capacity of cancer stem cells (CSCs). CSCs are a subpopulation of cells that reside within the tumor bulk and have the capacity to self-renew, differentiate, and repair DNA damage. These characteristics make CSCs develop resistance to a variety of treatments, such as radiotherapy (RT). RT is a frequent and often curative treatment for local cancer which mediates tumor elimination by cytotoxic actions. Also, cytokines and growth factors that are released into TME have been involved in the activation of tumor radioresistance and the induction of different immune cells, altering local immune responses. In this review, we discuss the pivotal role of TME in the resistance of CSCs to RT.

Keywords: Radiotherapy, cancer stem cells, tumor microenvironment, cancer-associated fibroblasts, extracellular matrix, hypoxia- inducible factor.

Graphical Abstract
[1]
Farhood, B.; Khodamoradi, E.; Hoseini-Ghahfarokhi, M.; Motevaseli, E.; Mirtavoos-Mahyari, H.; Eleojo Musa, A.; Najafi, M. TGF-β in radiotherapy: mechanisms of tumor resistance and normal tissues injury. Pharmacol. Res., 2020, 155, 104745.
[http://dx.doi.org/10.1016/j.phrs.2020.104745] [PMID: 32145401]
[2]
Ashrafizadeh, M.; Farhood, B.; Eleojo Musa, A.; Taeb, S.; Rezaeyan, A.; Najafi, M. Abscopal effect in radioimmunotherapy. Int. Immunopharmacol., 2020, 85, 106663.
[http://dx.doi.org/10.1016/j.intimp.2020.106663] [PMID: 32521494]
[3]
Mortezaee, K.; Parwaie, W.; Motevaseli, E.; Mirtavoos-Mahyari, H.; Musa, A.E.; Shabeeb, D.; Esmaely, F.; Najafi, M.; Farhood, B. Targets for improving tumor response to radiotherapy. Int. Immunopharmacol., 2019, 76, 105847.
[http://dx.doi.org/10.1016/j.intimp.2019.105847] [PMID: 31466051]
[4]
Farhood, B.; Ashrafizadeh, M.; Khodamoradi, E.; Hoseini-Ghahfarokhi, M.; Afrashi, S.; Musa, A.E.; Najafi, M. Targeting of cellular redox metabolism for mitigation of radiation injury. Life Sci., 2020, 250, 117570.
[http://dx.doi.org/10.1016/j.lfs.2020.117570] [PMID: 32205088]
[5]
Najafi, M.; Farhood, B.; Mortezaee, K. Extracellular matrix (ECM) stiffness and degradation as cancer drivers. J. Cell. Biochem., 2019, 120(3), 2782-2790.
[http://dx.doi.org/10.1002/jcb.27681] [PMID: 30321449]
[6]
Majidpoor, J.; Mortezaee, K. Steps in metastasis: an updated review. Med. Oncol., 2021, 38(1), 3.
[http://dx.doi.org/10.1007/s12032-020-01447-w] [PMID: 33394200]
[7]
Mortezaee, K. Redox tolerance and metabolic reprogramming in solid tumors. Cell Biol. Int., 2021, 45(2), 273-286.
[http://dx.doi.org/10.1002/cbin.11506] [PMID: 33236822]
[8]
Mortezaee, K. Immune escape: a critical hallmark in solid tumors. Life Sci., 2020, 258, 118110.
[http://dx.doi.org/10.1016/j.lfs.2020.118110] [PMID: 32698074]
[9]
Salvatori, L.; Caporuscio, F.; Verdina, A.; Starace, G.; Crispi, S.; Nicotra, M.R.; Russo, A.; Calogero, R.A.; Morgante, E.; Natali, P.G.; Russo, M.A.; Petrangeli, E. Cell-to-cell signaling influences the fate of prostate cancer stem cells and their potential to generate more aggressive tumors. PLoS One, 2012, 7(2), e31467.
[http://dx.doi.org/10.1371/journal.pone.0031467] [PMID: 22328933]
[10]
Wang, D.; Plukker, J.T.M; Coppes, R. Seminars in cancer biology; Elsevier, 2017, Vol. 44, pp. 60-66.
[11]
Clara, J.A.; Monge, C.; Yang, Y.; Takebe, N. Targeting signalling pathways and the immune microenvironment of cancer stem cells - a clinical update. Nat. Rev. Clin. Oncol., 2020, 17(4), 204-232.
[http://dx.doi.org/10.1038/s41571-019-0293-2] [PMID: 31792354]
[12]
Sung, P-J.; Rama, N.; Imbach, J.; Fiore, S.; Ducarouge, B.; Neves, D.; Chen, H-W.; Bernard, D.; Yang, P-C.; Bernet, A.; Depil, S.; Mehlen, P. Cancer-associated fibroblasts produce netrin-1 to control cancer cell plasticity. Cancer Res., 2019, 79(14), 3651-3661.
[http://dx.doi.org/10.1158/0008-5472.CAN-18-2952] [PMID: 31088838]
[13]
Chopra, S.; Deodhar, K.; Pai, V.; Pant, S.; Rathod, N.; Goda, J.S.; Sudhalkar, N.; Pandey, P.; Waghmare, S.; Engineer, R.; Mahantshetty, U.; Ghosh, J.; Gupta, S.; Shrivastava, S. Cancer stem cells, CD44, and outcomes following chemoradiation in locally advanced cervical cancer: results from a prospective study. Int. J. Radiat. Oncol. Biol. Phys., 2019, 103(1), 161-168.
[http://dx.doi.org/10.1016/j.ijrobp.2018.09.003] [PMID: 30213750]
[14]
Taeb, S.; Mosleh-Shirazi, M.; Ghaderi, A.; Mortazavi, S.; Razmkhah, M. Effects of gamma radiation on adipose-derived mesenchymal stem cells of human breast tissue. Int. J. Radiation. Res., 2021, 19(1), 175-182.
[http://dx.doi.org/10.29252/ijrr.19.1.175]
[15]
aeb, S.; Mosleh-Shiraz, M.; Ghaderi, A.; Mortazavi, S.; Razmkhah, M. Adipose-derived mesenchymal stem cells responses to different doses of gamma radiation. J. Biomed. Phys. Eng., 2020, 2020, 35-42.
[16]
Valkenburg, K.C.; de Groot, A.E.; Pienta, K.J. Targeting the tumour stroma to improve cancer therapy. Nat. Rev. Clin. Oncol., 2018, 15(6), 366-381.
[http://dx.doi.org/10.1038/s41571-018-0007-1] [PMID: 29651130]
[17]
Relation, T.; Dominici, M.; Horwitz, E.M. Concise review: an (im) penetrable shield: how the tumor microenvironment protects cancer stem cells. Stem Cells, 2017, 35(5), 1123-1130.
[http://dx.doi.org/10.1002/stem.2596] [PMID: 28207184]
[18]
Hanahan, D.; Coussens, L.M. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell, 2012, 21(3), 309-322.
[http://dx.doi.org/10.1016/j.ccr.2012.02.022] [PMID: 22439926]
[19]
Henke, E.; Nandigama, R.; Ergün, S. Extracellular matrix in the tumor microenvironment and its impact on cancer therapy. Front. Mol. Biosci., 2020, 6, 160.
[http://dx.doi.org/10.3389/fmolb.2019.00160] [PMID: 32118030]
[20]
Eble, J.A.; Niland, S. The extracellular matrix in tumor progression and metastasis. Clin. Exp. Metastasis, 2019, 36(3), 171-198.
[http://dx.doi.org/10.1007/s10585-019-09966-1] [PMID: 30972526]
[21]
Fournier, C.; Taucher-Scholz, G. Radiation induced cell cycle arrest: an overview of specific effects following high-LET exposure. Radiother. Oncol., 2004, 73(Suppl. 2), S119-S122.
[http://dx.doi.org/10.1016/S0167-8140(04)80031-8] [PMID: 15971325]
[22]
Nasonova, E.; Füssel, K.; Berger, S.; Gudowska-Nowak, E.; Ritter, S. Cell cycle arrest and aberration yield in normal human fibroblasts. I. Effects of X-rays and 195 MeV u(-1) C ions. Int. J. Radiat. Biol., 2004, 80(9), 621-634.
[http://dx.doi.org/10.1080/09553000400001006] [PMID: 15586882]
[23]
Barker, H.E.; Paget, J.T.; Khan, A.A.; Harrington, K.J. The tumour microenvironment after radiotherapy: mechanisms of resistance and recurrence. Nat. Rev. Cancer, 2015, 15(7), 409-425.
[http://dx.doi.org/10.1038/nrc3958] [PMID: 26105538]
[24]
Tsai, K.K.; Chuang, E.Y-Y.; Little, J.B.; Yuan, Z-M. Cellular mechanisms for low-dose ionizing radiation-induced perturbation of the breast tissue microenvironment. Cancer Res., 2005, 65(15), 6734-6744.
[http://dx.doi.org/10.1158/0008-5472.CAN-05-0703] [PMID: 16061655]
[25]
Bahmad, H.F.; Chamaa, F.; Assi, S.; Chalhoub, R.M.; Abou-Antoun, T.; Abou-Kheir, W. Cancer stem cells in neuroblastoma: expanding the therapeutic frontier. Front. Mol. Neurosci., 2019, 12, 131.
[http://dx.doi.org/10.3389/fnmol.2019.00131] [PMID: 31191243]
[26]
Tommelein, J.; De Vlieghere, E.; Verset, L.; Melsens, E.; Leenders, J.; Descamps, B.; Debucquoy, A.; Vanhove, C.; Pauwels, P.; Gespach, C.P.; Vral, A.; De Boeck, A.; Haustermans, K.; de Tullio, P.; Ceelen, W.; Demetter, P.; Boterberg, T.; Bracke, M.; De Wever, O. Radiotherapy-activated cancer-associated fibroblasts promote tumor progression through paracrine IGF1R activation. Cancer Res., 2018, 78(3), 659-670.
[http://dx.doi.org/10.1158/0008-5472.CAN-17-0524] [PMID: 29217764]
[27]
Piper, M.; Mueller, A.C.; Karam, S.D. The interplay between cancer associated fibroblasts and immune cells in the context of radiation therapy. Mol. Carcinog., 2020, 59(7), 754-765.
[http://dx.doi.org/10.1002/mc.23205] [PMID: 32363633]
[28]
Steer, A.; Cordes, N.; Jendrossek, V.; Klein, D. Impact of cancer-associated fibroblast on the radiation-response of solid xenograft tumors. Front. Mol. Biosci., 2019, 6, 70.
[http://dx.doi.org/10.3389/fmolb.2019.00070] [PMID: 31475157]
[29]
Chu, T-Y.; Yang, J-T.; Huang, T-H.; Liu, H-W. Crosstalk with cancer-associated fibroblasts increases the growth and radiation survival of cervical cancer cells. Radiat. Res., 2014, 181(5), 540-547.
[http://dx.doi.org/10.1667/RR13583.1] [PMID: 24785588]
[30]
Zhang, H.; Yue, J.; Jiang, Z.; Zhou, R.; Xie, R.; Xu, Y.; Wu, S. CAF-secreted CXCL1 conferred radioresistance by regulating DNA damage response in a ROS-dependent manner in esophageal squamous cell carcinoma. Cell Death Dis., 2017, 8(5), e2790-e2790.
[http://dx.doi.org/10.1038/cddis.2017.180] [PMID: 28518141]
[31]
Wang, Y.; Gan, G.; Wang, B.; Wu, J.; Cao, Y.; Zhu, D.; Xu, Y.; Wang, X.; Han, H.; Li, X.; Ye, M.; Zhao J.; Mi, J. Cancer-associated fibroblasts promote irradiated cancer cell recovery through autophagy. EBioMedicine, 2017, 17, 45-56.
[32]
Park, C.C.; Zhang, H.J.; Yao, E.S.; Park, C.J.; Bissell, M.J. β1 integrin inhibition dramatically enhances radiotherapy efficacy in human breast cancer xenografts. Cancer Res., 2008, 68(11), 4398-4405.
[http://dx.doi.org/10.1158/0008-5472.CAN-07-6390] [PMID: 18519702]
[33]
Liang, K.; Lu, Y.; Jin, W.; Ang, K.K.; Milas, L.; Fan, Z. Sensitization of breast cancer cells to radiation by trastuzumab. Mol. Cancer Ther., 2003, 2(11), 1113-1120.
[PMID: 14617784]
[34]
Cordes, N.; Beinke, C. Fibronectin alters cell survival and intracellular signaling of confluent A549 cultures after irradiation. Cancer Biol. Ther., 2004, 3(1), 47-53.
[http://dx.doi.org/10.4161/cbt.3.1.570] [PMID: 14726672]
[35]
Gobin, E.; Bagwell, K.; Wagner, J.; Mysona, D.; Sandirasegarane, S.; Smith, N.; Bai, S.; Sharma, A.; Schleifer, R.; She, J-X. A pan- cancer perspective of matrix metalloproteases (MMP) gene expression profile and their diagnostic/prognostic potential. BMC Cancer, 2019, 19(1), 581.
[http://dx.doi.org/10.1186/s12885-019-5768-0] [PMID: 31200666]
[36]
Artacho-Cordón, F.; Ríos-Arrabal, S.; Lara, P.C.; Artacho- Cordón, A.; Calvente, I.; Núñez, M.I. Matrix metalloproteinases: potential therapy to prevent the development of second malignancies after breast radiotherapy. Surg. Oncol., 2012, 21(3), e143-e151.
[http://dx.doi.org/10.1016/j.suronc.2012.06.001] [PMID: 22749313]
[37]
Ager, E.I.; Kozin, S.V.; Kirkpatrick, N.D.; Seano, G.; Kodack, D.P.; Askoxylakis, V.; Huang, Y.; Goel, S.; Snuderl, M.; Muzikansky, A.; Finkelstein, D.M.; Dransfield, D.T.; Devy, L.; Boucher, Y.; Fukumura, D.; Jain, R.K. Blockade of MMP14 activity in murine breast carcinomas: implications for macrophages, vessels, and radiotherapy. J. Natl. Cancer Inst., 2015, 107(4), djv017.
[http://dx.doi.org/10.1093/jnci/djv017] [PMID: 25710962]
[38]
Gu, Q.; He, Y.; Ji, J.; Yao, Y.; Shen, W.; Luo, J.; Zhu, W.; Cao, H.; Geng, Y.; Xu, J.; Zhang, S.; Cao, J.; Ding, W.Q. Hypoxia-inducible factor 1α (HIF-1α) and reactive oxygen species (ROS) mediates radiation-induced invasiveness through the SDF-1α/CXCR4 pathway in non-small cell lung carcinoma cells. Oncotarget, 2015, 6(13), 10893-10907.
[http://dx.doi.org/10.18632/oncotarget.3535] [PMID: 25843954]
[39]
Pozzi, V.; Sartini, D.; Rocchetti, R.; Santarelli, A.; Rubini, C.; Morganti, S.; Giuliante, R.; Calabrese, S.; Di Ruscio, G.; Orlando, F.; Provinciali, M.; Saccucci, F.; Lo Muzio, L.; Emanuelli, M. Identification and characterization of cancer stem cells from head and neck squamous cell carcinoma cell lines. Cell. Physiol. Biochem., 2015, 36(2), 784-798.
[http://dx.doi.org/10.1159/000430138] [PMID: 26021266]
[40]
Zakaria, N.; Yusoff, N.M.; Zakaria, Z.; Lim, M.N.; Baharuddin, P.J.N.; Fakiruddin, K.S.; Yahaya, B. Human non-small cell lung cancer expresses putative cancer stem cell markers and exhibits the transcriptomic profile of multipotent cells. BMC Cancer, 2015, 15(1), 84.
[http://dx.doi.org/10.1186/s12885-015-1086-3] [PMID: 25881239]
[41]
Bahmad, H.F.; Elajami, M.K.; Daouk, R.; Jalloul, H.; Darwish, B.; Chalhoub, R.M.; Assi, S.; Chamaa, F.; Abou-Kheir, W. Stem Cells: in sickness and in health. Curr. Stem Cell Res. Ther., 2021, 16(3), 262-276.
[http://dx.doi.org/10.2174/1574888X15999200831160710] [PMID: 32867660]
[42]
Aponte, P.M.; Caicedo, A. Stemness in cancer: stem cells, cancer stem cells, and their microenvironment. Stem Cells Int., 2017, 2017, 5619472.
[http://dx.doi.org/10.1155/2017/5619472] [PMID: 5619472]
[43]
Mei, W.; Lin, X.; Kapoor, A.; Gu, Y.; Zhao, K.; Tang, D. The contributions of prostate cancer stem cells in prostate cancer initiation and metastasis. Cancers (Basel), 2019, 11(4), 434.
[http://dx.doi.org/10.3390/cancers11040434] [PMID: 30934773]
[44]
Zhou, Y.; Xia, L.; Wang, H.; Oyang, L.; Su, M.; Liu, Q.; Lin, J.; Tan, S.; Tian, Y.; Liao, Q.; Cao, D. Cancer stem cells in progression of colorectal cancer. Oncotarget, 2017, 9(70), 33403-33415.
[http://dx.doi.org/10.18632/oncotarget.23607] [PMID: 30279970]
[45]
Lau, E.Y.-T.; Ho, N.P.-Y.; Lee, T.K.-W. Cancer stem cells and their microenvironment: biology and therapeutic implications. Stem Cells Int., 2017, 2017, 3714190.
[http://dx.doi.org/10.1155/2017/3714190] [PMID: 3714190]
[46]
Ishii, G. Crosstalk between cancer associated fibroblasts and cancer cells in the tumor microenvironment after radiotherapy. EBioMedicine, 2017, 17, 7-8.
[http://dx.doi.org/10.1016/j.ebiom.2017.03.004] [PMID: 28274806]
[47]
Nissen, N.I.; Karsdal, M.; Willumsen, N. Collagens and cancer associated fibroblasts in the reactive stroma and its relation to cancer biology. J. Exp. Clin. Cancer Res., 2019, 38(1), 115.
[http://dx.doi.org/10.1186/s13046-019-1110-6] [PMID: 30841909]
[48]
Gascard, P.; Tlsty, T.D. Carcinoma-associated fibroblasts: orchestrating the composition of malignancy. Genes Dev., 2016, 30(9), 1002-1019.
[http://dx.doi.org/10.1101/gad.279737.116] [PMID: 27151975]
[49]
Shen, H.; Yu, X.; Yang, F.; Zhang, Z.; Shen, J.; Sun, J.; Choksi, S.; Jitkaew, S.; Shu, Y. Reprogramming of normal fibroblasts into cancer-associated fibroblasts by miRNAs-mediated CCL2/VEGFA signaling. PLoS Genet., 2016, 12(8), e1006244.
[http://dx.doi.org/10.1371/journal.pgen.1006244] [PMID: 27541266]
[50]
Tyan, S-W.; Kuo, W-H.; Huang, C-K.; Pan, C-C.; Shew, J-Y.; Chang, K-J.; Lee, E.Y-H.; Lee, W-H. Breast cancer cells induce cancer-associated fibroblasts to secrete hepatocyte growth factor to enhance breast tumorigenesis. PLoS One, 2011, 6(1), e15313.
[http://dx.doi.org/10.1371/journal.pone.0015313] [PMID: 21249190]
[51]
Wu, Z.; Zhang, C.; Najafi, M. Targeting of the tumor immune microenvironment by metformin. J. Cell Commun. Signal., 2021. [Online ahead of print].
[http://dx.doi.org/10.1007/s12079-021-00648-w] [PMID: 34611852]
[52]
Fu, X.; Li, M.; Tang, C.; Huang, Z.; Najafi, M. Targeting of cancer cell death mechanisms by resveratrol: a review. Apoptosis, 2021, 26(11), 561-573.
[53]
Mu, Q.; Najafi, M. Resveratrol for targeting the tumor microenvironment and its interactions with cancer cells. Int. Immunopharmacol., 2021, 98, 107895.
[http://dx.doi.org/10.1016/j.intimp.2021.107895] [PMID: 34171623]
[54]
Yu, C.; Yang, B.; Najafi, M. Targeting of cancer cell death mechanisms by curcumin: Implications to cancer therapy. Basic Clin. Pharmacol. Toxicol., 2021. [Online ahead of print].
[http://dx.doi.org/10.1111/bcpt.13648] [PMID: 34473898]
[55]
Su, S.; Chen, J.; Yao, H.; Liu, J.; Yu, S.; Lao, L.; Wang, M.; Luo, M.; Xing, Y.; Chen, F. CD10+ GPR77+ cancer-associated fibroblasts promote cancer formation and chemoresistance by sustaining cancer stemness. Cell, 2018, 172(4), 841-856. e816.
[56]
Szot, C.; Saha, S.; Zhang, X.M.; Zhu, Z.; Hilton, M.B.; Morris, K.; Seaman, S.; Dunleavey, J.M.; Hsu, K-S.; Yu, G-J.; Morris, H.; Swing, D.A.; Haines, D.C.; Wang, Y.; Hwang, J.; Feng, Y.; Welsch, D.; DeCrescenzo, G.; Chaudhary, A.; Zudaire, E.; Dimitrov, D.S.; St Croix, B. Tumor stroma-targeted antibody-drug conjugate triggers localized anticancer drug release. J. Clin. Invest., 2018, 128(7), 2927-2943.
[http://dx.doi.org/10.1172/JCI120481] [PMID: 29863500]
[57]
Zhen, Z.; Tang, W.; Wang, M.; Zhou, S.; Wang, H.; Wu, Z.; Hao, Z.; Li, Z.; Liu, L.; Xie, J. Protein nanocage mediated fibroblast-activation protein targeted photoimmunotherapy to enhance cytotoxic T cell infiltration and tumor control. Nano Lett., 2017, 17(2), 862-869.
[http://dx.doi.org/10.1021/acs.nanolett.6b04150] [PMID: 28027646]
[58]
Najafi, M.; Farhood, B.; Mortezaee, K. Cancer stem cells (CSCs) in cancer progression and therapy. J. Cell. Physiol., 2019, 234(6), 8381-8395.
[http://dx.doi.org/10.1002/jcp.27740] [PMID: 30417375]
[59]
Pickup, M.W.; Mouw, J.K.; Weaver, V.M. The extracellular matrix modulates the hallmarks of cancer. EMBO Rep., 2014, 15(12), 1243-1253.
[http://dx.doi.org/10.15252/embr.201439246] [PMID: 25381661]
[60]
Martinez-Outschoorn, U.E.; Peiris-Pagés, M.; Pestell, R.G.; Sotgia, F.; Lisanti, M.P. Cancer metabolism: a therapeutic perspective. Nat. Rev. Clin. Oncol., 2017, 14(1), 11-31.
[http://dx.doi.org/10.1038/nrclinonc.2016.60] [PMID: 27141887]
[61]
Sancho, P.; Barneda, D.; Heeschen, C. Hallmarks of cancer stem cell metabolism. Br. J. Cancer, 2016, 114(12), 1305-1312.
[http://dx.doi.org/10.1038/bjc.2016.152] [PMID: 27219018]
[62]
Nazio, F.; Bordi, M.; Cianfanelli, V.; Locatelli, F.; Cecconi, F. Autophagy and cancer stem cells: molecular mechanisms and therapeutic applications. Cell Death Differ., 2019, 26(4), 690-702.
[http://dx.doi.org/10.1038/s41418-019-0292-y] [PMID: 30728463]
[63]
Dituri, F.; Mazzocca, A.; Giannelli, G.; Antonaci, S. PI3K functions in cancer progression, anticancer immunity and immune evasion by tumors. Clinical and Developmental Immunology, 2011, 2011, 947858.
[PMID: 947858]
[64]
Lu, H.; Clauser, K.R.; Tam, W.L.; Fröse, J.; Ye, X.; Eaton, E.N.; Reinhardt, F.; Donnenberg, V.S.; Bhargava, R.; Carr, S.A.; Weinberg, R.A. A breast cancer stem cell niche supported by juxtacrine signalling from monocytes and macrophages. Nat. Cell Biol., 2014, 16(11), 1105-1117.
[http://dx.doi.org/10.1038/ncb3041] [PMID: 25266422]
[65]
Bollyky, P.L.; Wu, R.P.; Falk, B.A.; Lord, J.D.; Long, S.A.; Preisinger, A.; Teng, B.; Holt, G.E.; Standifer, N.E.; Braun, K.R.; Xie, C.F.; Samuels, P.L.; Vernon, R.B.; Gebe, J.A.; Wight, T.N.; Nepom, G.T. ECM components guide IL-10 producing regulatory T-cell (TR1) induction from effector memory T-cell precursors. Proc. Natl. Acad. Sci. USA, 2011, 108(19), 7938-7943.
[http://dx.doi.org/10.1073/pnas.1017360108] [PMID: 21518860]
[66]
Bashour, T.A.; Hancock, W.W.; Lance, C. Substrate rigidity regulates human T cell. J. Immunol., 2012, 189(3), 1330-1339.
[67]
Zhang, H.; Lu, H.; Xiang, L.; Bullen, J.W.; Zhang, C.; Samanta, D.; Gilkes, D.M.; He, J.; Semenza, G.L. HIF-1 regulates CD47 expression in breast cancer cells to promote evasion of phagocytosis and maintenance of cancer stem cells. Proc. Natl. Acad. Sci. USA, 2015, 112(45), E6215-E6223.
[http://dx.doi.org/10.1073/pnas.1520032112] [PMID: 26512116]
[68]
Di Tomaso, T.; Mazzoleni, S.; Wang, E.; Sovena, G.; Clavenna, D.; Franzin, A.; Mortini, P.; Ferrone, S.; Doglioni, C.; Marincola, F.M.; Galli, R.; Parmiani, G.; Maccalli, C. Immunobiological characterization of cancer stem cells isolated from glioblastoma patients. Clin. Cancer Res., 2010, 16(3), 800-813.
[http://dx.doi.org/10.1158/1078-0432.CCR-09-2730] [PMID: 20103663]
[69]
Yakubenko, V.P.; Cui, K.; Ardell, C.L.; Brown, K.E.; West, X.Z.; Gao, D.; Stefl, S.; Salomon, R.G.; Podrez, E.A.; Byzova, T.V. Oxidative modifications of extracellular matrix promote the second wave of inflammation via β2 integrins. Blood, 2018, 132(1), 78-88.
[http://dx.doi.org/10.1182/blood-2017-10-810176] [PMID: 29724896]
[70]
Martinez, F.O.; Gordon, S. The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep., 2014, 6, 13.
[http://dx.doi.org/10.12703/P6-13] [PMID: 24669294]
[71]
Hanahan, D.; Weinberg, R.A. Hallmarks of cancer: the next generation. Cell, 2011, 144(5), 646-674.
[http://dx.doi.org/10.1016/j.cell.2011.02.013] [PMID: 21376230]
[72]
Bates, J.P.; Derakhshandeh, R.; Jones, L.; Webb, T.J. Mechanisms of immune evasion in breast cancer. BMC Cancer, 2018, 18(1), 556.
[http://dx.doi.org/10.1186/s12885-018-4441-3] [PMID: 29751789]
[73]
Mantovani, A.; Sica, A.; Sozzani, S.; Allavena, P.; Vecchi, A.; Locati, M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol., 2004, 25(12), 677-686.
[http://dx.doi.org/10.1016/j.it.2004.09.015] [PMID: 15530839]
[74]
Rodero, M.P.; Khosrotehrani, K. Skin wound healing modulation by macrophages. Int. J. Clin. Exp. Pathol., 2010, 3(7), 643-653.
[PMID: 20830235]
[75]
Raz, Y.; Cohen, N.; Shani, O.; Bell, R.E.; Novitskiy, S.V.; Abramovitz, L.; Levy, C.; Milyavsky, M.; Leider-Trejo, L.; Moses, H.L.; Grisaru, D.; Erez, N. Bone marrow-derived fibroblasts are a functionally distinct stromal cell population in breast cancer. J. Exp. Med., 2018, 215(12), 3075-3093.
[http://dx.doi.org/10.1084/jem.20180818] [PMID: 30470719]
[76]
Li, X.; Shang, B.; Li, Y.N.; Shi, Y.; Shao, C. IFNγ and TNFα synergistically induce apoptosis of mesenchymal stem/stromal cells via the induction of nitric oxide. Stem Cell Res. Ther., 2019, 10(1), 18.
[http://dx.doi.org/10.1186/s13287-018-1102-z] [PMID: 30635041]
[77]
Ren, G.; Su, J.; Zhang, L.; Zhao, X.; Ling, W.; L’huillie, A.; Zhang, J.; Lu, Y.; Roberts, A.I.; Ji, W.; Zhang, H.; Rabson, A.B.; Shi, Y. Species variation in the mechanisms of mesenchymal stem cell-mediated immunosuppression. Stem Cells, 2009, 27(8), 1954-1962.
[http://dx.doi.org/10.1002/stem.118] [PMID: 19544427]
[78]
Zhang, L.; Dang, R-J.; Li, H.; Li, P.; Yang, Y-M.; Guo, X-M.; Wang, X-Y.; Fang, N-Z.; Mao, N.; Wen, N.; Jiang, X.X. SOCS1 regulates the immune modulatory properties of mesenchymal stem cells by inhibiting nitric oxide production. PLoS One, 2014, 9(5), e97256.
[http://dx.doi.org/10.1371/journal.pone.0097256] [PMID: 24826993]
[79]
Hirata, E.; Sahai, E. Tumor microenvironment and differential responses to therapy. Cold Spring Harb. Perspect. Med., 2017, 7(7), a026781.
[http://dx.doi.org/10.1101/cshperspect.a026781] [PMID: 28213438]
[80]
Sahai, E.; Astsaturov, I.; Cukierman, E.; DeNardo, D.G.; Egeblad, M.; Evans, R.M.; Fearon, D.; Greten, F.R.; Hingorani, S.R.; Hunter, T.; Hynes, R.O.; Jain, R.K.; Janowitz, T.; Jorgensen, C.; Kimmelman, A.C.; Kolonin, M.G.; Maki, R.G.; Powers, R.S.; Puré, E.; Ramirez, D.C.; Scherz-Shouval, R.; Sherman, M.H.; Stewart, S.; Tlsty, T.D.; Tuveson, D.A.; Watt, F.M.; Weaver, V.; Weeraratna, A.T.; Werb, Z. A framework for advancing our understanding of cancer-associated fibroblasts. Nat. Rev. Cancer, 2020, 20(3), 174-186.
[http://dx.doi.org/10.1038/s41568-019-0238-1] [PMID: 31980749]
[81]
Chen, C.; Hou, J.; Yu, S.; Li, W.; Wang, X.; Sun, H.; Qin, T.; Claret, F.X.; Guo, H.; Liu, Z. Role of cancer-associated fibroblasts in the resistance to antitumor therapy, and their potential therapeutic mechanisms in non-small cell lung cancer. Oncol. Lett., 2021, 21(5), 413.
[http://dx.doi.org/10.3892/ol.2021.12674] [PMID: 33841574]
[82]
Öhlund, D.; Elyada, E.; Tuveson, D. Fibroblast heterogeneity in the cancer wound. J. Exp. Med., 2014, 211(8), 1503-1523.
[http://dx.doi.org/10.1084/jem.20140692] [PMID: 25071162]
[83]
Meads, M.B.; Gatenby, R.A.; Dalton, W.S. Environment-mediated drug resistance: a major contributor to minimal residual disease. Nat. Rev. Cancer, 2009, 9(9), 665-674.
[http://dx.doi.org/10.1038/nrc2714] [PMID: 19693095]
[84]
Kalluri, R. The biology and function of fibroblasts in cancer. Nat. Rev. Cancer, 2016, 16(9), 582-598.
[http://dx.doi.org/10.1038/nrc.2016.73] [PMID: 27550820]
[85]
Schmidmaier, R.; Baumann, P. Anti-adhesion evolves to a promising therapeutic concept in oncology. Curr. Med. Chem., 2008, 15(10), 978-990.
[http://dx.doi.org/10.2174/092986708784049667] [PMID: 18393855]
[86]
Wu, X.; Tao, P.; Zhou, Q.; Li, J.; Yu, Z.; Wang, X.; Li, J.; Li, C.; Yan, M.; Zhu, Z.; Liu, B.; Su, L. IL-6 secreted by cancer-associated fibroblasts promotes epithelial-mesenchymal transition and metastasis of gastric cancer via JAK2/STAT3 signaling pathway. Oncotarget, 2017, 8(13), 20741-20750.
[http://dx.doi.org/10.18632/oncotarget.15119] [PMID: 28186964]
[87]
Yeung, T-L.; Leung, C.S.; Wong, K-K.; Samimi, G.; Thompson, M.S.; Liu, J.; Zaid, T.M.; Ghosh, S.; Birrer, M.J.; Mok, S.C. TGF-β modulates ovarian cancer invasion by upregulating CAF-derived versican in the tumor microenvironment. Cancer Res., 2013, 73(16), 5016-5028.
[http://dx.doi.org/10.1158/0008-5472.CAN-13-0023] [PMID: 23824740]
[88]
Lwin, T.; Hazlehurst, L.A.; Moscinski, L.C.; Dalton, W.S.; Tao, J. Cell adhesion induces p27kip1-associated cell-cycle arrest through down-regulating scfskp2 ubiquitin ligase pathway in mantle cell and other non-hodgkin’s b-cell lymphomas. Blood, 2006, 108(11), 2048.
[http://dx.doi.org/10.1182/blood.V108.11.2048.2048]
[89]
Liu, L.; Zhang, Z.; Zhou, L.; Hu, L.; Yin, C.; Qing, D.; Huang, S.; Cai, X.; Chen, Y. Cancer associated fibroblasts-derived exosomes contribute to radioresistance through promoting colorectal cancer stem cells phenotype. Exp. Cell Res., 2020, 391(2), 111956.
[http://dx.doi.org/10.1016/j.yexcr.2020.111956] [PMID: 32169425]
[90]
Donnarumma, E.; Fiore, D.; Nappa, M.; Roscigno, G.; Adamo, A.; Iaboni, M.; Russo, V.; Affinito, A.; Puoti, I.; Quintavalle, C.; Rienzo, A.; Piscuoglio, S.; Thomas, R.; Condorelli, G. Cancer-associated fibroblasts release exosomal microRNAs that dictate an aggressive phenotype in breast cancer. Oncotarget, 2017, 8(12), 19592-19608.
[http://dx.doi.org/10.18632/oncotarget.14752] [PMID: 28121625]
[91]
Hu, Y.; Yan, C.; Mu, L.; Huang, K.; Li, X.; Tao, D.; Wu, Y.; Qin, J. Fibroblast-derived exosomes contribute to chemoresistance through priming cancer stem cells in colorectal cancer. PLoS One, 2015, 10(5), e0125625.
[http://dx.doi.org/10.1371/journal.pone.0125625] [PMID: 25938772]
[92]
Bayer, C.; Shi, K.; Astner, S.T.; Maftei, C.-A.; Vaupel, P. Acute versus chronic hypoxia: why a simplified classification is simply not enough. Int. J. Radiation Oncol. Biol. Physics, 2011, 80(4), 965-968.
[93]
Petrova, V.; Annicchiarico-Petruzzelli, M.; Melino, G.; Amelio, I. The hypoxic tumour microenvironment. Oncogenesis, 2018, 7(1), 10.
[http://dx.doi.org/10.1038/s41389-017-0011-9] [PMID: 29362402]
[94]
Fiori, M.E.; Di Franco, S.; Villanova, L.; Bianca, P.; Stassi, G.; De Maria, R. Cancer-associated fibroblasts as abettors of tumor progression at the crossroads of EMT and therapy resistance. Mol. Cancer, 2019, 18(1), 70.
[http://dx.doi.org/10.1186/s12943-019-0994-2] [PMID: 30927908]
[95]
Monteran, L.; Erez, N. The dark side of fibroblasts: cancer-associated fibroblasts as mediators of immunosuppression in the tumor microenvironment. Front. Immunol., 2019, 10, 1835.
[http://dx.doi.org/10.3389/fimmu.2019.01835] [PMID: 31428105]
[96]
Higgins, D.F.; Kimura, K.; Iwano, M.; Haase, V.H. Hypoxia-inducible factor signaling in the development of tissue fibrosis. Cell Cycle, 2008, 7(9), 1128-1132.
[http://dx.doi.org/10.4161/cc.7.9.5804] [PMID: 18418042]
[97]
Andersson-Sjöland, A.; Nihlberg, K.; Eriksson, L.; Bjermer, L.; Westergren-Thorsson, G. Fibrocytes and the tissue niche in lung repair. Respir. Res., 2011, 12(1), 76.
[http://dx.doi.org/10.1186/1465-9921-12-76] [PMID: 21658209]
[98]
Gardner, L.B.; Corn, P.G. Hypoxic regulation of mRNA expression. Cell Cycle, 2008, 7(13), 1916-1924.
[http://dx.doi.org/10.4161/cc.7.13.6203] [PMID: 18604161]
[99]
Kojima, Y.; Acar, A.; Eaton, E.N.; Mellody, K.T.; Scheel, C.; Ben-Porath, I.; Onder, T.T.; Wang, Z.C.; Richardson, A.L.; Weinberg, R.A.; Orimo, A. Autocrine TGF-β and stromal cell-derived factor-1 (SDF-1) signaling drives the evolution of tumor-promoting mammary stromal myofibroblasts. Proc. Natl. Acad. Sci. USA, 2010, 107(46), 20009-20014.
[http://dx.doi.org/10.1073/pnas.1013805107] [PMID: 21041659]
[100]
Curran, C.S.; Keely, P.J. Breast tumor and stromal cell responses to TGF-β and hypoxia in matrix deposition. Matrix Biol., 2013, 32(2), 95-105.
[http://dx.doi.org/10.1016/j.matbio.2012.11.016] [PMID: 23262216]
[101]
Orimo, A.; Gupta, P.B.; Sgroi, D.C.; Arenzana-Seisdedos, F.; Delaunay, T.; Naeem, R.; Carey, V.J.; Richardson, A.L.; Weinberg, R.A. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell, 2005, 121(3), 335-348.
[http://dx.doi.org/10.1016/j.cell.2005.02.034] [PMID: 15882617]
[102]
Giaccia, A.J.; Schipani, E. Diverse effects of hypoxia on tumor progression; Springer, 2010, pp. 31-45.
[http://dx.doi.org/10.1007/82_2010_73]
[103]
Gray, L.H.; Conger, A.D.; Ebert, M.; Hornsey, S.; Scott, O.C. The concentration of oxygen dissolved in tissues at the time of irradiation as a factor in radiotherapy. Br. J. Radiol., 1953, 26(312), 638-648.
[http://dx.doi.org/10.1259/0007-1285-26-312-638] [PMID: 13106296]
[104]
Gray, L.H. Radiobiologic basis of oxygen as a modifying factor in radiation therapy. Am. J. Roentgenol. Radium Ther. Nucl. Med., 1961, 85, 803-815.
[PMID: 13708070]
[105]
Joiner, M.C.; Van der Kogel, A. Basic clinical radiobiology, 4th ed; CRC press, 2009.
[http://dx.doi.org/10.1201/b15450]
[106]
Zhang, K.; Guo, Y.; Wang, X.; Zhao, H.; Ji, Z.; Cheng, C.; Li, L.; Fang, Y.; Xu, D.; Zhu, H.H.; Gao, W.Q. WNT/β-catenin directs self-renewal symmetric cell division of hTERThigh prostate cancer stem cells. Cancer Res., 2017, 77(9), 2534-2547.
[http://dx.doi.org/10.1158/0008-5472.CAN-16-1887] [PMID: 28209613]
[107]
Borah, A.; Raveendran, S.; Rochani, A.; Maekawa, T.; Kumar, D.S. Targeting self-renewal pathways in cancer stem cells: clinical implications for cancer therapy. Oncogenesis, 2015, 4(11), e177-e177.
[http://dx.doi.org/10.1038/oncsis.2015.35] [PMID: 26619402]
[108]
Peitzsch, C.; Perrin, R.; Hill, R.P.; Dubrovska, A.; Kurth, I. Hypoxia as a biomarker for radioresistant cancer stem cells. Int. J. Radiat. Biol., 2014, 90(8), 636-652.
[http://dx.doi.org/10.3109/09553002.2014.916841] [PMID: 24844374]
[109]
Bao, S.; Wu, Q.; McLendon, R.E.; Hao, Y.; Shi, Q.; Hjelmeland, A.B.; Dewhirst, M.W.; Bigner, D.D.; Rich, J.N. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature, 2006, 444(7120), 756-760.
[110]
Hill, R.P.; Marie-Egyptienne, D.T.; Hedley, D.W Seminars in radiation oncology; Elsevier, 2009, Vol. 19, pp. 106-111.
[111]
Kim, H.; Lin, Q.; Glazer, P.M.; Yun, Z. The hypoxic tumor microenvironment in vivo selects the cancer stem cell fate of breast cancer cells. Breast Cancer Res., 2018, 20(1), 16.
[http://dx.doi.org/10.1186/s13058-018-0944-8] [PMID: 29510720]
[112]
van den Beucken, T.; Koch, E.; Chu, K.; Rupaimoole, R.; Prickaerts, P.; Adriaens, M.; Voncken, J.W.; Harris, A.L.; Buffa, F.M.; Haider, S.; Starmans, M.H.W.; Yao, C.Q.; Ivan, M.; Ivan, C.; Pecot, C.V.; Boutros, P.C.; Sood, A.K.; Koritzinsky, M.; Wouters, B.G. Hypoxia promotes stem cell phenotypes and poor prognosis through epigenetic regulation of DICER. Nat. Commun., 2014, 5(1), 5203.
[http://dx.doi.org/10.1038/ncomms6203] [PMID: 25351418]
[113]
Huang, G.; Chen, L. Tumor vasculature and microenvironment normalization: a possible mechanism of antiangiogenesis therapy. Cancer Biother. Radiopharm., 2008, 23(5), 661-667.
[http://dx.doi.org/10.1089/cbr.2008.0492] [PMID: 18986217]
[114]
Comunanza, V.; Bussolino, F. Therapy for cancer: strategy of combining anti-angiogenic and target therapies. Front. Cell Dev. Biol., 2017, 5, 101.
[http://dx.doi.org/10.3389/fcell.2017.00101] [PMID: 29270405]
[115]
Reisfeld, R.A. The tumor microenvironment: a target for combination therapy of breast cancer. Crit. Rev. Oncog., 2013, 18(1-2), 115-133.
[http://dx.doi.org/10.1615/CritRevOncog.v18.i1-2.70] [PMID: 23237555]
[116]
Franco, O.E.; Shaw, A.K.; Strand, D.W.; Hayward, S.W. Cancer associated fibroblasts in cancer pathogenesis. Semin. Cell Dev. Biol., 2010, 21(1), 33-39.
[http://dx.doi.org/10.1016/j.semcdb.2009.10.010] [PMID: 19896548]
[117]
Kopp, H-G.; Ramos, C.A.; Rafii, S. Contribution of endothelial progenitors and proangiogenic hematopoietic cells to vascularization of tumor and ischemic tissue. Curr. Opin. Hematol., 2006, 13(3), 175-181.
[http://dx.doi.org/10.1097/01.moh.0000219664.26528.da] [PMID: 16567962]
[118]
Chang, E.I.; Chang, E.I.; Thangarajah, H.; Hamou, C.; Gurtner, G.C. Hypoxia, hormones, and endothelial progenitor cells in hemangioma. Lymphat. Res. Biol., 2007, 5(4), 237-243.
[http://dx.doi.org/10.1089/lrb.2007.1014] [PMID: 18370914]
[119]
Nakamura, N.; Naruse, K.; Matsuki, T.; Hamada, Y.; Nakashima, E.; Kamiya, H.; Matsubara, T.; Enomoto, A.; Takahashi, M.; Oiso, Y.; Nakamura, J. Adiponectin promotes migration activities of endothelial progenitor cells via Cdc42/Rac1. FEBS Lett., 2009, 583(15), 2457-2463.
[http://dx.doi.org/10.1016/j.febslet.2009.07.011] [PMID: 19596003]
[120]
Muramatsu, T. Midkine and pleiotrophin: two related proteins involved in development, survival, inflammation and tumorigenesis. J. Biochem., 2002, 132(3), 359-371.
[http://dx.doi.org/10.1093/oxfordjournals.jbchem.a003231] [PMID: 12204104]
[121]
Chen, H.; Campbell, R.A.; Chang, Y.; Li, M.; Wang, C.S.; Li, J.; Sanchez, E.; Share, M.; Steinberg, J.; Berenson, A.; Shalitin, D.; Zeng, Z.; Gui, D.; Perez-Pinera, P.; Berenson, R.J.; Said, J.; Bonavida, B.; Deuel, T.F.; Berenson, J.R. Pleiotrophin produced by multiple myeloma induces transdifferentiation of monocytes into vascular endothelial cells: a novel mechanism of tumor-induced vasculogenesis. Blood, 2009, 113(9), 1992-2002.
[http://dx.doi.org/10.1182/blood-2008-02-133751] [PMID: 19060246]
[122]
Kheshtchin, N.; Arab, S.; Ajami, M.; Mirzaei, R.; Ashourpour, M.; Mousavi, N.; Khosravianfar, N.; Jadidi-Niaragh, F.; Namdar, A.; Noorbakhsh, F.; Hadjati, J. Inhibition of HIF-1α enhances anti-tumor effects of dendritic cell-based vaccination in a mouse model of breast cancer. Cancer Immunol. Immunother., 2016, 65(10), 1159-1167.
[http://dx.doi.org/10.1007/s00262-016-1879-5] [PMID: 27497816]
[123]
Zhu, Y.; Zang, Y.; Zhao, F.; Li, Z.; Zhang, J.; Fang, L.; Li, M.; Xing, L.; Xu, Z.; Yu, J. Inhibition of HIF-1α by PX-478 suppresses tumor growth of esophageal squamous cell cancer in vitro and in vivo. Am. J. Cancer Res., 2017, 7(5), 1198-1212.
[PMID: 28560067]
[124]
Majmundar, A.J.; Wong, W.J.; Simon, M.C. Hypoxia-inducible factors and the response to hypoxic stress. Mol. Cell, 2010, 40(2), 294-309.
[http://dx.doi.org/10.1016/j.molcel.2010.09.022] [PMID: 20965423]
[125]
Keith, B.; Simon, M.C. Hypoxia-inducible factors, stem cells, and cancer. Cell, 2007, 129(3), 465-472.
[http://dx.doi.org/10.1016/j.cell.2007.04.019] [PMID: 17482542]
[126]
Zhu, H.; Wang, D.; Liu, Y.; Su, Z.; Zhang, L.; Chen, F.; Zhou, Y.; Wu, Y.; Yu, M.; Zhang, Z.; Shao, G. Role of the hypoxia-inducible factor-1 alpha induced autophagy in the conversion of non- stem pancreatic cancer cells into CD133+ pancreatic cancer stem-like cells. Cancer Cell Int., 2013, 13(1), 119.
[http://dx.doi.org/10.1186/1475-2867-13-119] [PMID: 24305593]
[127]
Harada, H. Hypoxia-inducible factor 1-mediated characteristic features of cancer cells for tumor radioresistance. J. Radiat. Res. (Tokyo), 2016, 57(S1)(Suppl. 1), i99-i105.
[http://dx.doi.org/10.1093/jrr/rrw012] [PMID: 26983985]
[128]
Zhang, H.; Bosch-Marce, M.; Shimoda, L.A.; Tan, Y.S.; Baek, J.H.; Wesley, J.B.; Gonzalez, F.J.; Semenza, G.L. Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J. Biol. Chem., 2008, 283(16), 10892-10903.
[http://dx.doi.org/10.1074/jbc.M800102200] [PMID: 18281291]
[129]
Ke, Q.; Costa, M. Hypoxia-inducible factor-1 (HIF-1). Mol. Pharmacol., 2006, 70(5), 1469-1480.
[http://dx.doi.org/10.1124/mol.106.027029] [PMID: 16887934]
[130]
Poon, E.; Harris, A.L.; Ashcroft, M. Targeting the hypoxia-inducible factor (HIF) pathway in cancer. Expert Rev. Mol. Med., 2009, 11, e26.
[http://dx.doi.org/10.1017/S1462399409001173] [PMID: 19709449]
[131]
Moeller, B.J.; Cao, Y.; Li, C.Y.; Dewhirst, M.W. Radiation activates HIF-1 to regulate vascular radiosensitivity in tumors: role of reoxygenation, free radicals, and stress granules. Cancer Cell, 2004, 5(5), 429-441.
[http://dx.doi.org/10.1016/S1535-6108(04)00115-1] [PMID: 15144951]
[132]
Harada, H.; Kizaka-Kondoh, S.; Li, G.; Itasaka, S.; Shibuya, K.; Inoue, M.; Hiraoka, M. Significance of HIF-1-active cells in angiogenesis and radioresistance. Oncogene, 2007, 26(54), 7508-7516.
[http://dx.doi.org/10.1038/sj.onc.1210556] [PMID: 17563752]
[133]
Harada, H.; Inoue, M.; Itasaka, S.; Hirota, K.; Morinibu, A.; Shinomiya, K.; Zeng, L.; Ou, G.; Zhu, Y.; Yoshimura, M.; McKenna, W.G.; Muschel, R.J.; Hiraoka, M. Cancer cells that survive radiation therapy acquire HIF-1 activity and translocate towards tumour blood vessels. Nat. Commun., 2012, 3(1), 783.
[http://dx.doi.org/10.1038/ncomms1786] [PMID: 22510688]
[134]
Li, N.; Meng, D.; Gao, L.; Xu, Y.; Liu, P.; Tian, Y.; Yi, Z-y.; Zhang, Y.; Tie, X.; Xu, Z. Overexpression of HOTAIR leads to radioresistance of human cervical cancer via promoting HIF-1α expression. Radiat. Oncol., 2018, 13(1), 1-9.
[http://dx.doi.org/10.1186/s13014-018-1153-4] [PMID: 29304828]
[135]
Santoni, G.; Morelli, M.B.; Nabissi, M.; Maggi, F.; Marinelli, O.; Santoni, M.; Amantini, C. Cross-talk between microRNAs, long non-coding RNAs and p21 Cip1 in glioma: diagnostic, prognostic and therapeutic roles. J. Cancer Metastasis Treat., 2020, 6, 22.
[http://dx.doi.org/10.20517/2394-4722.2020.49]
[136]
Huang, X.; Zuo, J. Emerging roles of miR-210 and other non-coding RNAs in the hypoxic response. Acta Biochim. Biophys. Sin. (Shanghai), 2014, 46(3), 220-232.
[http://dx.doi.org/10.1093/abbs/gmt141] [PMID: 24395300]
[137]
Chen, X.; Guo, J.; Xi, R-X.; Chang, Y-W.; Pan, F-Y.; Zhang, X-Z. MiR-210 expression reverses radioresistance of stem-like cells of oesophageal squamous cell carcinoma. World J. Clin. Oncol., 2014, 5(5), 1068-1077.
[http://dx.doi.org/10.5306/wjco.v5.i5.1068] [PMID: 25493243]
[138]
Peng, X.; Gao, H.; Xu, R.; Wang, H.; Mei, J.; Liu, C. The interplay between HIF-1α and noncoding RNAs in cancer. J. Exp. Clin. Cancer Res., 2020, 39(1), 1-19.
[http://dx.doi.org/10.1186/s13046-020-1535-y] [PMID: 31928527]
[139]
Zhou, J.; Xu, D.; Xie, H.; Tang, J.; Liu, R.; Li, J.; Wang, S.; Chen, X.; Su, J.; Zhou, X.; Xia, K.; He, Q.; Chen, J.; Xiong, W.; Cao, P.; Cao, K. miR-33a functions as a tumor suppressor in melanoma by targeting HIF-1α. Cancer Biol. Ther., 2015, 16(6), 846-855.
[http://dx.doi.org/10.1080/15384047.2015.1030545] [PMID: 25891797]
[140]
Tsagakis, I.; Douka, K.; Birds, I.; Aspden, J.L. Long non-coding RNAs in development and disease: conservation to mechanisms. J. Pathol., 2020, 250(5), 480-495.
[http://dx.doi.org/10.1002/path.5405] [PMID: 32100288]
[141]
Ponting, C.P.; Oliver, P.L.; Reik, W. Evolution and functions of long noncoding RNAs. Cell, 2009, 136(4), 629-641.
[http://dx.doi.org/10.1016/j.cell.2009.02.006] [PMID: 19239885]
[142]
Cho, S.W.; Xu, J.; Sun, R.; Mumbach, M.R.; Carter, A.C.; Chen, Y.G.; Yost, K.E.; Kim, J.; He, J.; Nevins, S.A. Promoter of lncRNA gene PVT1 is a tumor-suppressor DNA boundary element. Cell, 2018, 173(6), 1398-1412. e1322.
[http://dx.doi.org/10.1016/j.cell.2018.03.068]
[143]
Wang, C.; Han, C.; Zhang, Y.; Liu, F. LncRNA PVT1 regulate expression of HIF1α via functioning as ceRNA for miR-199a-5p in non-small cell lung cancer under hypoxia. Mol. Med. Rep., 2018, 17(1), 1105-1110.
[PMID: 29115513]
[144]
Huang, T.; Liu, H.W.; Chen, J.Q.; Wang, S.H.; Hao, L.Q.; Liu, M.; Wang, B. The long noncoding RNA PVT1 functions as a competing endogenous RNA by sponging miR-186 in gastric cancer. Biomed. Pharmacother., 2017, 88, 302-308.
[http://dx.doi.org/10.1016/j.biopha.2017.01.049] [PMID: 28122299]
[145]
Wang, Y.; Chen, W.; Lian, J.; Zhang, H.; Yu, B.; Zhang, M.; Wei, F.; Wu, J.; Jiang, J.; Jia, Y.; Mo, F.; Zhang, S.; Liang, X.; Mou, X.; Tang, J. The lncRNA PVT1 regulates nasopharyngeal carcinoma cell proliferation via activating the KAT2A acetyltransferase and stabilizing HIF-1α. Cell Death Differ., 2020, 27(2), 695-710.
[http://dx.doi.org/10.1038/s41418-019-0381-y] [PMID: 31320749]
[146]
Shen, Y.; Liu, Y.; Sun, T.; Yang, W. LincRNA-p21 knockdown enhances radiosensitivity of hypoxic tumor cells by reducing autophagy through HIF-1/Akt/mTOR/P70S6K pathway. Exp. Cell Res., 2017, 358(2), 188-198.
[http://dx.doi.org/10.1016/j.yexcr.2017.06.016] [PMID: 28689810]

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