Role of the tumor microenvironment in mediating de novo resistance to drugs and physiological mediators of cell death

Hazlehurst, Lori A; Landowski, Terry H; Dalton, William S

doi:10.1038/sj.onc.1206943

Cited by 203Cancer Cells and MetastasisCell death mechanisms and regulationAcute Myeloid Leukemia Research

Role of the tumor microenvironment in mediating de novo resistance to drugs and physiological mediators of cell death

Hazlehurst, Lori A, Landowski, Terry H, Dalton, William S·2003·Oncogene

DOI 10.1038/sj.onc.1206943

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Abstract

The emergence of clinical drug resistance continues to be an obstacle for the successful treatment of cancer. Our current understanding of mechanisms associated with drug resistance has been ascertained by investigating drug-resistant models created by exposing a parental population to increasing concentrations of a cytotoxic. These unicellular drug-resistant models have been critical in elucidating drug-resistant mechanism and in some cases have aided in the identification of drug targets. However, these models do not address resistance mechanisms that contribute to de novo drug resistance. We propose that specific niches within the tumor microenvironment may provide a sanctuary for subpopulations of tumors cells that affords a survival advantage following initial drug exposure and may facilitate the acquisition of acquired drug resistance. More specifically, we propose that the bone marrow microenvironment is a sanctuary for hema-topoietic cancers. This review will focus on the bone marrow microenvironment and its role in conferring resistance to cytotoxics and physiological mediators of cell death.

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CAFs comprise the majority of cell types within the TME, and their reciprocal interactions with cancer cells are well documented.
“CAFs comprise the majority of cell types within the TME, and their reciprocal interactions with cancer cells have been well documented (Whiteside, 2008; Hazlehurst et al., 2003; Karnoub et al., 2007).”
From Tumor microenvironment derived exosomes pleiotropically modulate cancer cell metabolism (2016) · cites this paper as Hazlehurst et al., 2003

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Background
Desmoplasia and Chemoresistance in Pancreatic Cancer
Schober, M., Jesenofsky, R., Faissner, R., Weidenauer, C., Hagmann, W., Michl, P., Heuchel, R. L., Haas, S., & Löhr, M. J. (2014) · Cancers · doi:10.3390/cancers6042137 · Cited by 183 · see citing works
“Several other groups have shown that a variety of expressed integrins are linked to growth promoting effects via paracrine and autocrine signaling pathways [69–73], and this should be taken into account when attempting to revert a CAM-DR phenotype in vivo [25].”
Background
Interleukin-6 in the bone marrow microenvironment promotes the growth and survival of neuroblastoma cells
Ara, T., Song, L., Shimada, H., Keshelava, N., Russell, H. V., Metelitsa, L. S., Groshen, S. G., Seeger, R. C., & DeClerck, Y. A. (2009) · Cancer Research · doi:10.1158/0008-5472.can-08-0613 · Cited by 175 · see citing works
“It has been previously reported that the bone marrow microenvironment is a known sanctuary for tumor cells and protects them from the cytotoxic effect of chemotherapeutic agents (5).”
Background
Nanoformulations for combination or cascade anticancer therapy
Miao, L., Guo, S., Lin, C. M., Liu, Q., & Huang, L. (2017) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2017.06.003 · Cited by 178 · see citing works
“However, recent studies have demonstrated that specific niches within the TME may provide a sanctuary for subpopulations of tumor cells, leading to a survival advantage following initial drug exposure and facilitating the acquisition of both innate and acquired drug resistance (Figure 6) [16, 18, 166].”
Background
Fibroblast-derived 3D matrix differentially regulates the growth and drug-responsiveness of human cancer cells
Serebriiskii, I. G., Castelló-Cros, R., Lamb, A., Golemis, E. A., & Cukierman, E. (2008) · Matrix Biology · doi:10.1016/j.matbio.2008.02.008 · Cited by 176 · see citing works
“In addition, it has long been known that tumor cells grown in 3D environments differ in their susceptibility to chemotherapeutic agents from cells grown on 2D (Frankel et al., 1997; Hazlehurst et al., 2003; Morin, 2003; Zahir and Weaver, 2004).”
Background
β1 Integrin Targeting Potentiates Antiangiogenic Therapy and Inhibits the Growth of Bevacizumab-Resistant Glioblastoma
Carbonell, W. S., DeLay, M., Jahangiri, A., Park, C. C., & Aghi, M. K. (2013) · Cancer Research · doi:10.1158/0008-5472.can-13-0011 · Cited by 163 · see citing works
Integrin β7-mediated regulation of multiple myeloma cell adhesion, migration, and invasion
Neri, P. E., Ren, L., Azab, A. K., Brentnall, M., Gratton, K., Klimowicz, A. C., Lin, C. P., Duggan, P. R., Tassone, P., Mansoor, A., et al. (2011) · Blood · doi:10.1182/blood-2010-06-292243 · Cited by 162 · see citing works
Extracellular Vesicles from Cancer-Associated Fibroblasts Containing Annexin A6 Induces FAK-YAP Activation by Stabilizing β1 Integrin, Enhancing Drug Resistance
Uchihara, T., Miyake, K., Yonemura, A., Komohara, Y., Itoyama, R., Koiwa, M., Yasuda, T., Arima, K., Harada, K., Eto, K., et al. (2020) · Cancer Research · doi:10.1158/0008-5472.can-19-3803 · Cited by 159 · see citing works
Tumor microenvironment and drug resistance in hematologic malignancies
Li, Z., & Dalton, W. S. (2006) · Blood Reviews · doi:10.1016/j.blre.2005.08.003 · Cited by 156 · see citing works
Self-citation
Epithelial–Mesenchymal Transition Programs and Cancer Stem Cell Phenotypes: Mediators of Breast Cancer Therapy Resistance
Gooding, A. J., & Schiemann, W. P. (2020) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-20-0067 · Cited by 136 · see citing works
A crosstalk between the Wnt and the adhesion-dependent signaling pathways governs the chemosensitivity of acute myeloid leukemia
de Toni, F., Racaud‐Sultan, C., Chicanne, G., Mas, V. M., Cariven, C., Briand‐Mésange, F., Salles, J., Demur, C., Allouche, M., Payrastre, B., et al. (2005) · Oncogene · doi:10.1038/sj.onc.1209346 · Cited by 132 · see citing works
“It has been demonstrated in several hematological malignancies that cell/cell or cell/matrix adhesion processes are involved in chemoresistance (Hazlehurst et al., 2003).”
Background
Targeting autocrine and paracrine VEGF receptor pathways inhibits human lymphoma xenografts in vivo
Wang, E. S., Teruya‐Feldstein, J., Wu, Y. L., Zhu, Z., Hicklin, D. J., & Moore, M. A. S. (2004) · Blood · doi:10.1182/blood-2004-01-0226 · Cited by 128 · see citing works
Deciphering cellular states of innate tumor drug responses
Graudens, E., Boulanger, V., Mollard, C., Mariage, R., Barlet, X., Grémy, G., Couillault, C., Lajémi, M., Piatier‐Tonneau, D., Zaborski, P., et al. (2006) · Genome biology · doi:10.1186/gb-2006-7-3-r19 · Cited by 127 · see citing works
P‐glycoprotein: So Many Ways to Turn It On
Callaghan, R., Crowley, E. H., Biochem, M., Potter, S., & Kerr, I. D. (2007) · The Journal of Clinical Pharmacology · doi:10.1177/0091270007311568 · Cited by 123 · see citing works
Artesunate attenuates the growth of human colorectal carcinoma and inhibits hyperactive Wnt/β‐catenin pathway
Li, L., Zhang, H., Yuan, S., Tian, Z., Wang, L., & Sun, Z. (2007) · International Journal of Cancer · doi:10.1002/ijc.22804 · Cited by 119 · see citing works
“It has been demonstrated that cell/ cell or cell/matrix adhesion progresses are involved in chemoresistance.(31) Recent data indicate that inhibition of Wnt/b-catenin signaling pathway might affect cell adhesive function and chemosensitivity.”
Background
The HMG-CoA reductase inhibitor simvastatin overcomes cell adhesion–mediated drug resistance in multiple myeloma by geranylgeranylation of Rho protein and activation of Rho kinase
Schmidmaier, R., Baumann, P., Şimşek, M., Dayyani, F., Emmerich, B., & Meinhardt, G. (2004) · Blood · doi:10.1182/blood-2003-12-4218 · Cited by 118 · see citing works
Epigenetic and breast cancer therapy: Promising diagnostic and therapeutic applications
Sher, G., Salman, N. A., Khan, A. Q., Prabhu, K. S., Raza, A., Kuliński, M., Dermime, S., Haris, M., Junejo, K., & Shahab Uddin, M. S. (2020) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2020.08.009 · Cited by 110 · see citing works
Regulation of differential pro- and anti-apoptotic signaling by glucocorticoids
Herr, I., Gaßler, N., Friess, H., & Büchler, M. W. (2006) · APOPTOSIS · doi:10.1007/s10495-006-0624-5 · Cited by 105 · see citing works
“General mechanisms of resistance include decreased drug uptake, increased drug efflux, alterations in the drug target, drug metabolism, repair of DNA damage, cell cycle checkpoint mediators, and changes in downstream mediators of the apoptotic pathway [106].”
Background
Activation of fibronectin/PI-3K/Akt2 leads to chemoresistance to docetaxel by regulating survivin protein expression in ovarian and breast cancer cells
Xing, H., Weng, D., Chen, G., Tao, W., Zhu, T., Yang, X., Li, M., Wang, S., Lu, Y., & Ma, D. (2008) · Cancer Letters · doi:10.1016/j.canlet.2007.11.022 · Cited by 104 · see citing works
“ipate in cell survival and resistance to cytotoxic agents [3–5].”
Background
Overview of Oroxylin A: A Promising Flavonoid Compound
Lu, L., Guo, Q., & Zhao, L. (2016) · Phytotherapy Research · doi:10.1002/ptr.5694 · Cited by 103 · see citing works
“Cell adhesion mediated-drug resistance (CAM-DR) belongs to EMDR and induces de novo drug resistance (Hazlehurst et al., 2003).”
Background
Cyclooxygenase‐2 inhibitor celecoxib augments chemotherapeutic drug‐induced apoptosis by enhancing activation of caspase‐3 and ‐9 in prostate cancer cells
Dandekar, D. S., Lopez, M. H., Carey, R. I., & Lokeshwar, B. L. (2005) · International Journal of Cancer · doi:10.1002/ijc.20878 · Cited by 103 · see citing works
“tic response in vivo and reduce cytotoxicity in vitro in a variety of tumors and cell types.(45,46,47) Some reports documented that stromal cells alter expression of cell adhesion molecules, integrins, cytokines, chemokines and also cell cycle-related events.”
Background
Drugs repurposed: An advanced step towards the treatment of breast cancer and associated challenges
Malik, J. A., Ahmed, S., Jan, B., Bender, O., Hagbani, T. A., Alqarni, A., & Anwar, S. (2021) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2021.112375 · Cited by 99 · see citing works
Gelatin Methacrylate Hydrogels as Biomimetic Three-Dimensional Matrixes for Modeling Breast Cancer Invasion and Chemoresponse in Vitro
Arya, A. D., Hallur, P. M., Karkisaval, A. G., Gudipati, A., Rajendiran, S., Dhavale, V., Ramachandran, B., Aravindakshan, J., Gundiah, N., & Chaubey, A. (2016) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.6b06309 · Cited by 98 · see citing works
An open‐label, phase 2 trial of denosumab in the treatment of relapsed or plateau‐phase multiple myeloma
Vij, R., Horvath, N., Spencer, A. G., Taylor, K., Vadhan‐Raj, S., Vescio, R. A., Smith, J. W. G., Qian, Y., Yeh, H., & Jun, S. (2009) · American Journal of Hematology · doi:10.1002/ajh.21509 · Cited by 97 · see citing works
“Moreover, in MM populations that are heavily treated, acquired drug resistance may develop on the survival of myeloma cells during their exposure to antimyeloma therapies and limits detection of treatment effect [22,23].”
Tipifarnib and Bortezomib Are Synergistic and Overcome Cell Adhesion–Mediated Drug Resistance in Multiple Myeloma and Acute Myeloid Leukemia
Yanamandra, N., Colaco, N. M., Parquet, N., Buzzeo, R. W., Boulware, D. C., Wright, G. M., Perez, L. E., Dalton, W. S., & Beaupre, D. M. (2006) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-05-1792 · Cited by 96 · see citing works
Self-citation
Mesenchymal stem cells promote osteosarcoma cell survival and drug resistance through activation of STAT3
Tu, B., Zhu, J., Liu, S., Wang, L., Fan, Q., Hao, Y., Fan, C., & Tang, T.-T. (2016) · Oncotarget · doi:10.18632/oncotarget.10219 · Cited by 95 · see citing works
Cancer Cell-derived Exosomes Induce Mitogen-activated Protein Kinase-dependent Monocyte Survival by Transport of Functional Receptor Tyrosine Kinases*
Song, X., Ding, Y.-P., Liu, G., Yang, X., Zhao, R., Zhang, Y.-L., Zhao, X., Anderson, G., & Nie, G. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.716316 · Cited by 94 · see citing works
“Tumors have been reported to drive an inflammatory microenvironment with a range of pro- and anti-inflammatory factors that are regarded to induce monocyte death (13, 14).”
Background
Understanding Breast cancer: from conventional therapies to repurposed drugs
Costa, B., Amorim, I., Gärtner, F., & Vale, N. (2020) · European Journal of Pharmaceutical Sciences · doi:10.1016/j.ejps.2020.105401 · Cited by 93 · see citing works
Atacicept (TACI-Ig) inhibits growth of TACIhigh primary myeloma cells in SCID-hu mice and in coculture with osteoclasts
Yaccoby, S., Pennisi, A., Li, X., Dillon, S. R., Zhan, F., Barlogie, B., & Shaughnessy, J. D. (2007) · Leukemia · doi:10.1038/sj.leu.2405048 · Cited by 88 · see citing works
Molecular markers associated with outcome and metastasis in human pancreatic cancer
den broeck, A. V., Vankelecom, H. E. J., van Eijsden, R. G. E., Govaere, O., & Topal, B. (2012) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/1756-9966-31-68 · Cited by 83 · see citing works
“Due to the abundance of ECM, the integrin-mediated cell adhesion signalling may play an important role in PDAC tumour growth, migration and even in therapy resistance [25,26].”
Background
Tumour-microenvironmental interactions: paths to progression and targets for treatment
Box, C., Rogers, S. J., Mendiola, M., & Eccles, S. A. (2010) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2010.06.004 · Cited by 83 · see citing works
“[33] Hazlehurst LA, Landowski TH, Dalton WS.”
Background
beta1 integrin as a molecular therapeutic target
Cordes, N., & Park, C. C. (2007) · International Journal of Radiation Biology · doi:10.1080/09553000701639694 · Cited by 73 · see citing works
“In addition, b1 integrin conferred resistance in hepatoma, and lymphoma cells from drug-induced apoptosis via activation of the mitogen activated protein kinase (MAPK) pathway (Zhang et al. 2002), protection from DNA-damage (Hazlehurst et al. 2003), and Akt-dependent inhibition of caspase-8 cleavage (Estrugo et al. 20…”
Background
Associations of chemo- and radio-resistant phenotypes with the gap junction, adhesion and extracellular matrix in a three-dimensional culture model of soft sarcoma
Bai, C., Yang, M., Fan, Z., Li, S., Gao, T., & Fang, Z. (2015) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-015-0175-0 · Cited by 70 · see citing works
“[17].”
Accessory Cells of the Microenvironment Protect Multiple Myeloma from T-Cell Cytotoxicity through Cell Adhesion-Mediated Immune Resistance
de Haart, S. J., van de Donk, N. W. C. J., Minnema, M. C., Huang, J. H. Y., Aarts‐Riemens, T., Bovenschen, N., Yuan, H., Groen, R. W. J., McMillin, D. W., Jakubı́ková, J., et al. (2013) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-12-3676 · Cited by 67 · see citing works
“microenvironment is crucially important in the development of resistance to pharmacologic therapies (3, 35), its contribution to immune resistance, that is, rendering multiple myeloma cells resistant to the cytotoxic effect of CTLs, has received little attention until now.”
Background
Normalizing the bone marrow microenvironment with p38 inhibitor reduces multiple myeloma cell proliferation and adhesion and suppresses osteoclast formation
Nguyen, A. N., Stebbins, E. G., Henson, M., O’Young, G., Choi, S. J., Quon, D. H., Damm, D., Reddy, M., Ma, J. Y., Haghnazari, E., et al. (2006) · Experimental Cell Research · doi:10.1016/j.yexcr.2006.02.026 · Cited by 67 · see citing works
Combination Bcl-2 Antisense and Radiation Therapy for Nasopharyngeal Cancer
Yip, K. W., Mocanu, J. D., Au, P. Y. B., Sleep, G. T., Huang, D. P., Busson, P., Yeh, W., Gilbert, R. W., O’Sullivan, B., Gullane, P. J., et al. (2005) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-05-1266 · Cited by 67 · see citing works
Prediction of individual response to anticancer therapy: historical and future perspectives
Unger, F. T., Witte, I., & David, K. A. (2014) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-014-1772-3 · Cited by 66 · see citing works
“drug sensitivity between cells cultured in monolayers and those grown in 3D cultures [54–56].”
Background
Adhesion-mediated apoptosis resistance in cancer
Westhoff, M., & Fulda, S. (2009) · Drug Resistance Updates · doi:10.1016/j.drup.2009.08.001 · Cited by 64 · see citing works
Molecular Basis of Differential Sensitivity of Myeloma Cells to Clinically Relevant Bolus Treatment with Bortezomib
Shabaneh, T. B., Downey-Kopyscinski, S. L., Goddard, A. L., Screen, M., Lucas, M. M., Eastman, A. R., & Kisselev, A. F. (2013) · PLoS ONE · doi:10.1371/journal.pone.0056132 · Cited by 63 · see citing works
“RPMI8226 derived melphalan-resistant LR5 cells [24] were provided by Dr.”
Background
Integrin-Mediated Adhesion: Tipping the Balance between Chemosensitivity and Chemoresistance
Zutter, M. M. (2007) · Advances in experimental medicine and biology · doi:10.1007/978-0-387-74039-3_6 · Cited by 63 · see citing works
Engineered 3D environments to elucidate the effect of environmental parameters on drug response in cancer
Håkanson, M., Textor, M., & Charnley, M. (2010) · Integrative Biology · doi:10.1039/c0ib00074d · Cited by 62 · see citing works
Cyclooxygenase-2 (COX-2): a molecular target in prostate cancer
Gallego, G. A., Díaz‐Prado, S., Fonseca, P. J., Campelo, R. G., Espinosa, J., & Aparicio, L. M. A. (2007) · Clinical & Translational Oncology · doi:10.1007/s12094-007-0126-0 · Cited by 61 · see citing works
“Stromal cells and factors derived from them have been known to influence therapeutic response in vivo and reduce cytotoxicity in vitro in a variety of tumours and cell types [64].”
Background
Carcinoma-associated fibroblasts affect sensitivity to oxaliplatin and 5FU in colorectal cancer cells
Gonçalves-Ribeiro, S., Díaz-Maroto, N. G., Berdiel‐Acer, M., Soriano, A., Guardiola, J., Martinez–Villacampa, M., Salazar, R., Capellá, G., Villanueva, A., Martinez‐Balibrea, E., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.11121 · Cited by 59 · see citing works
The gene expression signature of relapse in paediatric acute lymphoblastic leukaemia: implications for mechanisms of therapy failure
Beesley, A. H., Cummings, A. J., Freitas, J. R., Hoffmann, K., Firth, M. J., Ford, J., de Klerk, N. H., & Kees, U. R. (2005) · British Journal of Haematology · doi:10.1111/j.1365-2141.2005.05785.x · Cited by 59 · see citing works
“One possibility is that an enhanced ability for leukaemic blasts to invade tissues would enable them to populate so-called sanctuary sites – pockets of disease that can evade chemotherapy or immune surveillance and ultimately result in relapse (Hazlehurst et al, 2003).”
Background
Identification of a novel switch in the dominant forms of cell adhesion-mediated drug resistance in glioblastoma cells
Westhoff, M., Zhou, S., Bachem, M. G., Debatin, K., & Fulda, S. (2008) · Oncogene · doi:10.1038/onc.2008.148 · Cited by 59 · see citing works
“…dependence on adhesion to substrate, often resulting in anoikis upon removal of their microenvironment, in contrast to tumor cells of hemopoietic lineage, which exhibit a more flexible interaction with their microenvironment (Hazlehurst et al., 2003a; Schmidmaier et al., 2004; Krysko et al., 2005).”
Influential
Bone Marrow Stroma Confers Resistance to Apo2 Ligand/TRAIL in Multiple Myeloma in Part by Regulating c-FLIP
Perez, L. E., Parquet, N., Shain, K. H., Nimmanapalli, R., Alsina, M., Anasetti, C., & Dalton, W. S. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.3.1545 · Cited by 57 · see citing works
“There is an increasing body of evidence that hemopoietic stromal elements and soluble factors protect hematological malignancies from chemotherapy (12, 17, 18, 37, 38), the process referred to as EMDR.”
BackgroundSelf-citation
Overcoming multiple drug resistance in cancer using polymeric micelles
Kesharwani, S. S., Kaur, S., Tummala, H., & Sangamwar, A. T. (2018) · Expert Opinion on Drug Delivery · doi:10.1080/17425247.2018.1537261 · Cited by 57 · see citing works
“Multiple growth factors are known to disturb homeostasis leading to disease progression and MDR [61,74].”
Background
Tissue dynamics spectroscopy for phenotypic profiling of drug effects in three-dimensional culture
Nolte, D. D., An, R., Turek, J. J., & Jeong, K. (2012) · Biomedical Optics Express · doi:10.1364/boe.3.002825 · Cited by 52 · see citing works
Development and characterization of a human three-dimensional chondrosarcoma culture for in vitro drug testing
Voissiere, A., Jouberton, E., Maubert, E., Degoul, F., Peyrode, C., Chezal, J.-M., & Miot-Noirault, É. (2017) · PLOS ONE · doi:10.1371/journal.pone.0181340 · Cited by 49 · see citing works
The influence of tumour microenvironmental factors on the efficacy of cisplatin and novel platinum(IV) complexes
Mellor, H. R., Snelling, S. J. B., Hall, M. D., Modok, S., Jaffar, M., Hambley, T. W., & Callaghan, R. (2005) · Biochemical Pharmacology · doi:10.1016/j.bcp.2005.07.016 · Cited by 51 · see citing works
Chemical and Biological Profiles of Novel Copper(II) Complexes Containing S-Donor Ligands for the Treatment of Cancer
Giovagnini, L., Sitran, S., Montopoli, M., Caparrotta, L., Corsini, M., Rosani, C., Zanello, P., Dou, Q. P., & Fregona, D. (2008) · Inorganic Chemistry · doi:10.1021/ic800404e · Cited by 50 · see citing works
Inhibition of integrin β1 decreases the malignancy of ovarian cancer cells and potentiates anticancer therapy via the FAK/STAT1 signaling pathway
Zhang, L., & Zou, W. (2015) · Molecular Medicine Reports · doi:10.3892/mmr.2015.4443 · Cited by 50 · see citing works
“Integrin β 1 (ITGB1), regulates broader functional activities such as cellular proliferation, adhesion, and invasion, and previous studies have suggested its implication in therapeutic resistance in numerous solid cancer models (10-12) and hematopoietic malignancies (13,14).”
Isolation and characterization of squamous carcinoma cells resistant to photodynamic therapy
Sanabria, L. N. M., Cogno, I. S., Rodríguez, M. E., Sanz-Rodrı́guez, F., Zamarrón, A., Gilaberte, Y., Carrasco, E., Rivarola, V. A., & Juarranz, Á. (2011) · Journal of Cellular Biochemistry · doi:10.1002/jcb.23145 · Cited by 50 · see citing works
“In the tumor cells there are numerous mechanisms of resistance [Hazlehurst et al., 2003; Solyanik, 2010].”
Background
Three‐dimensional matrix stiffness and adhesive ligands affect cancer cell response to toxins
Zustiak, S. P., Dadhwal, S., Medina, C., Steczina, S., Chehreghanianzabi, Y., Ashraf, A., & Asuri, P. (2015) · Biotechnology and Bioengineering · doi:10.1002/bit.25709 · Cited by 49 · see citing works
“The role of integrin signaling in cancer cell survival and chemoresistance has also been demonstrated (Hazlehurst et al., 2003), including using 3D glioblastoma in vitro models (Janouskova et al., 2012).”
BackgroundMethod
Humanized chondroitinase ABC sensitizes glioblastoma cells to temozolomide
Jaime‐Ramirez, A. C., Dmitrieva, N., Yoo, J. Y., Banasavadi‐Siddegowda, Y., Zhang, J., Relation, T., Bolyard, C. M., Wojton, J., & Kaur, B. (2017) · The Journal of Gene Medicine · doi:10.1002/jgm.2942 · Cited by 49 · see citing works
“Briefly three different glioma cell lines (Gli36ΔEGFR, U251 and U87ΔEGFR) grown in a three‐dimensional cell culture were incubated with β‐D‐xylopyranoside to reduce CSPG glycosylation.(17,18) Forty‐ eight hours post treatment, a moderate decrease in glioma sphere aggregation was observed in cells treated with β‐D‐xylo…”
A New α5β1 Integrin-Dependent Survival Pathway Through GSK3β Activation in Leukemic Cells
de Toni, F., Despeaux, M., Bertrand, J., Bourogâa, E., Ysebaert, L., Payrastre, B., & Racaud‐Sultan, C. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009807 · Cited by 49 · see citing works
“many tumors [23].”
Osteopontin-mediated enhanced hyaluronan binding induces multidrug resistance in mesothelioma cells
Tajima, K., Ohashi, R., Sekido, Y., Hida, T., Nara, T., Hashimoto, M., Iwakami, S., Minakata, K., Yae, T., Takahashi, F., et al. (2010) · Oncogene · doi:10.1038/onc.2009.478 · Cited by 48 · see citing works
“For instance, it has been reported that small cell lung cancer cells, myeloma cells, glioma cells and colon cancer cells were protected from apoptosis induced by various anticancer agents when the cells were plated on ECM (Damiano et al., 1999; Sethi et al., 1999; Uhm et al., 1999; Kouniavsky et al., 2002).”
Influential
Ultrasound-activated nanomaterials for sonodynamic cancer theranostics
Wu, N., Fan, C.-H., & Yeh, C.-K. (2022) · Drug Discovery Today · doi:10.1016/j.drudis.2022.02.025 · Cited by 49 · see citing works
Overexpression of Cell Surface Cytokeratin 8 in Multidrug-Resistant MCF-7/MX Cells Enhances Cell Adhesion to the Extracellular Matrix
Liu, F., Chen, Z., Wang, J., Shao, X., Cui, Z., Yang, C., Zhu, Z., & Xiong, D. (2008) · Neoplasia · doi:10.1593/neo.08810 · Cited by 47 · see citing works
“Recently, accumulating evidence suggests that the extracellular microenvironment may also influence the drug response and acquisition of drug resistance in cancer cells [5,6].”
Background
Tumor-colonizing bacteria: A potential tumor targeting therapy
Zu, C., & Wang, J. (2013) · Critical Reviews in Microbiology · doi:10.3109/1040841x.2013.776511 · Cited by 46 · see citing works
“Accordingly, multidrug resistance and survival of tumor cells remain challenges in the treatment of various tumors (Groot et al., 2007, Hazlehurst et al., 2003).”
Background
Zinc(II) complexes with dithiocarbamato derivatives: Structural characterisation and biological assays on cancerous cell lines
Nagy, E. M., Sitran, S., Montopoli, M., Favaro, M., Marchiò, L., Caparrotta, L., & Fregona, D. (2012) · Journal of Inorganic Biochemistry · doi:10.1016/j.jinorgbio.2012.09.004 · Cited by 46 · see citing works
STAT3-mediated IGF-2 secretion in the tumour microenvironment elicits innate resistance to anti-IGF-1R antibody
Lee, J. S., Kang, J.-H., Boo, H., Hwang, S.-J., Hong, S., Lee, S.-C., Park, Y.-J., Chung, T.-M., Youn, H., Lee, S. M., et al. (2015) · Nature Communications · doi:10.1038/ncomms9499 · Cited by 46 · see citing works
“The interaction between tumours and stromal cells in the TME is mediated through cell adhesion molecules and/or soluble factors 49 .”
The mesenchymal tumor microenvironment
Cukierman, E., & Bassi, D. (2012) · Cell Adhesion & Migration · doi:10.4161/cam.20210 · Cited by 45 · see citing works
Miniaturized pre-clinical cancer models as research and diagnostic tools
Håkanson, M., Cukierman, E., & Charnley, M. (2013) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2013.11.010 · Cited by 45 · see citing works
The Interplay between Slow-Cycling, Chemoresistant Cancer Cells and Fibroblasts Creates a Proinflammatory Niche for Tumor Progression
Cho, J., Lee, H., Hwang, S. J., Min, H., Kang, H. N., Park, A., Hyun, S. Y., Sim, J. Y., Lee, H. J., Jang, H.-J., et al. (2020) · Cancer Research · doi:10.1158/0008-5472.can-19-0631 · Cited by 44 · see citing works
“Given the ability of CAFs to change the extracellular matrix topology as a main component of tumor progression and anticancer drug resistance (42, 43), it was highly likely that the SCCs recruited fibroblasts in the TME to evade tumor dormancy and promote chemoresistance.”
Background
Resistance to FLT3 inhibition in an in vitro model of primary AML cells with a stem cell phenotype in a defined microenvironment
Mony, U., Jawad, M., Seedhouse, C., Russell, N. H., & Pallis, M. (2008) · Leukemia · doi:10.1038/leu.2008.125 · Cited by 43 · see citing works
Ex vivo cultures and drug testing of primary acute myeloid leukemia samples: Current techniques and implications for experimental design and outcome
Cucchi, D. G. J., Groen, R. W. J., Janssen, J. J. W. M., & Cloos, J. J. (2020) · Drug Resistance Updates · doi:10.1016/j.drup.2020.100730 · Cited by 43 · see citing works
Gain-of-function p53 protein transferred via small extracellular vesicles promotes conversion of fibroblasts to a cancer-associated phenotype
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Authors: Hazlehurst, L. A., Landowski, T. H., & Dalton, W. S.
Affiliations: University of South Florida (US)
Corresponding author: Dalton, William S
ORCID: Hazlehurst, Lori A
Dalton, William S
Venue: Oncogene
Publisher: Springer Science and Business Media LLC
Published: 2003-10-20
Volume: 22
Issue: 47
Pages: 7396-7402
ISSN: 0950-9232 (ISSN-L)
1476-5594
DOI: 10.1038/sj.onc.1206943
OpenAlex: W2041997066
Cited by: 203
References: 61
Citations by year: 2026: 2 · 2024: 2 · 2023: 8 · 2022: 5 · 2021: 6 · 2020: 19 · 2019: 2 · 2018: 3 · 2017: 9 · 2016: 14 · 2015: 9 · 2014: 10 · 2013: 12 · 2012: 18
FWCI: 1.02
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Oncogene (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
Health Sciences › Medicine › Hematology › Acute Myeloid Leukemia Research
Keywords: tumor microenvironment, acquired drug resistance, bone marrow microenvironment, hematopoietic tumors, cytotoxic drugs, cell death, cancer stem cells, hematopoietic stem cells
MeSH terms: Animals, Antineoplastic Agents, Cell Adhesion, DNA Damage, Humans, Neoplasms, Signal Transduction, Integrins, Apoptosis, Drug Resistance, Neoplasm

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Role of the tumor microenvironment in mediating de novo resistance to drugs and physiological mediators of cell death

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