Cited by 268Mesenchymal stem cell researchBacterial Cancer TherapyAngiogenesis and VEGF in Cancer

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Mesenchymal Stem Cell Targeting of Microscopic Tumors and Tumor Stroma Development Monitored by Noninvasive In vivo Positron Emission Tomography Imaging

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Hung, Shih-Chieh, Deng, Win-Ping, Yang, Wen K., Liu, Ren-Shyan, Lee, Chien-Chih, Su, Tzu-Chi, Lin, Rue-Jen, Yang, Den-Mei, Chang, Chi-Wei, Chen, Wei-Hong, Wei, Hon-Jian, Gelovani, Juri G.·2005·Clinical Cancer Research

DOI 10.1158/1078-0432.ccr-05-0876

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Abstract

The aim of this study was to assess the efficacy human mesenchymal stem cells (hMSC) for targeting microscopic tumors and suicide gene or cytokine gene therapy. Immunodeficient mice were transplanted s.c. with human colon cancer cells of HT-29 Inv2 or CCS line, and 3 to 4 days later, i.v. with “tracer” hMSCs expressing herpes simplex virus type 1 thymidine kinase (HSV1-TK) and enhanced green fluorescent protein (EGFP) reporter genes. Subsequently, these tumors were examined for specificity and magnitude of HSV1-TK+, EGFP+ stem cell engraftment and proliferation in tumor stroma by in vivo positron emission tomography (PET) with 18F-labeled 9-(4-fluoro-3-hydroxymethylbutyl)-guanine ([18F]-FHBG). In vivo PET images of tumors growing for 4 weeks showed the presence of HSV1-TK+ tumor stroma with an average of 0.36 ± 0.24% ID/g [18F]-FHBG accumulation. In vivo imaging results were validated by in situ correlative histochemical, immunofluorescent, and cytometric analyses, which revealed EGFP expression in vWF+ and CD31+ endothelial cells of capillaries and larger blood vessels, in germinal layer of dermis and hair follicles proximal to the s.c. tumor site. These differentiated HSV1-TK+, GFP+ endothelial cells had limited proliferative capacity and a short life span of <2 weeks in tumor fragments transplanted into secondary hosts. We conclude that hMSCs can target microscopic tumors, subsequently proliferate and differentiate, and contribute to formation of a significant portion of tumor stroma. PET imaging should facilitate clinical translation of stem cell–based anticancer gene therapeutic approaches by providing the means for in vivo noninvasive whole-body monitoring of trafficking, tumor targeting, and proliferation of HSV1-tk-expressing “tracer” hMSCs in tumor stroma.

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Show all 46 references

Sorted by citations

Items 101–200 of 268

Immune properties of mesenchymal stem cells
Sotiropoulou, P. A., & Papamichail, M. (2007) · Methods in Molecular Biology · doi:10.1007/978-1-59745-536-7_16 · Cited by 57
“The targeting of microscopic tumors by MSCs and their proliferation and contribution to the tumor stroma was confirmed by in vivo imaging (75), whereas enrichment of angiogenesis of the developed tumors and elevated capability of proliferation and highly metastatic ability of the cancer cells within were also evidence…”
Background
The dual effect of mesenchymal stem cells on tumour growth and tumour angiogenesis
Kéramidas, M., de Fraipont, F., Karageorgis, A., Moisan, A., Persoons, V., Richard, M., Coll, J., & Rome, C. (2013) · Stem Cell Research & Therapy · doi:10.1186/scrt195 · Cited by 53
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Background
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Background
Multimodal Imaging of Neural Progenitor Cell Fate in Rodents
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Safe and Effective Delivery of Antitumor Drug Using Mesenchymal Stem Cells Impregnated with Submicron Carriers
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Differential Mechanical Response of Mesenchymal Stem Cells and Fibroblasts to Tumor-Secreted Soluble Factors
McGrail, D. J., Ghosh, D., Quach, N. D., & Dawson, M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033248 · Cited by 52
“use of systemically infused MSCs to tumors has been investigated in breast [13], colon [14], ovarian carcinomas [15], gliomas [16], and Kaposi’s sarcomas [17].”
Background
Concise Review: Genetically Engineered Stem Cell Therapy Targeting Angiogenesis and Tumor Stroma in Gastrointestinal Malignancy
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Generation of Osteosarcomas from a Combination of Rb Silencing and c-Myc Overexpression in Human Mesenchymal Stem Cells
Wang, J., Wu, P., Chen, P. C.-H., Lee, C.-W., Chen, W., & Hung, S. (2016) · Stem Cells Translational Medicine · doi:10.5966/sctm.2015-0226 · Cited by 53
Self-citation
Molecular imaging and cancer gene therapy
Saadatpour, Z., Bjørklund, G., Chirumbolo, S., Alimohammadi, M., Ehsani, H., Ebrahiminejad, H., Pourghadamyari, H., Baghaei, B., Mirzaei, H., Sahebkar, A., et al. (2016) · Cancer Gene Therapy · doi:10.1038/cgt.2016.62 · Cited by 49
CRISPR-enhanced engineering of therapy-sensitive cancer cells for self-targeting of primary and metastatic tumors
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The extracellular matrix proteins type I collagen, type III collagen, fibronectin, and laminin 421 stimulate migration of cancer cells
Graf, F., Horn, P., Ho, A. D., Boutros, M., & Maercker, C. (2021) · The FASEB Journal · doi:10.1096/fj.202002558rr · Cited by 52
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Background
The Cancer Stem Cell–Vascular Niche Complex in Brain Tumor Formation
Veeravagu, A., Bababeygy, S. R., Kalani, M. Y. S., Hou, L. C., & Tse, V. (2008) · Stem Cells and Development · doi:10.1089/scd.2008.0047 · Cited by 45
“In addition to their contribution to neovasculature, MSCs may also engraft into ischemic lesions, differentiate into von Willabrand Factor (vWF) and CD31 + endothelial-like cells, and incorporate into the tumor stroma [46].”
Structure-guided Engineering of Human Thymidine Kinase 2 as a Positron Emission Tomography Reporter Gene for Enhanced Phosphorylation of Non-natural Thymidine Analog Reporter Probe
Campbell, D. O., Yaghoubi, S. S., Su, Y., Lee, J. T., Auerbach, M. S., Herschman, H. R., Satyamurthy, N., Czernin, J. G., Lavie, A., & Radu, C. G. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.314666 · Cited by 46
Cytosine deaminase‐producing human mesenchymal stem cells mediate an antitumor effect in a mouse xenograft model
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Hyperthermia‐treated mesenchymal stem cells exert antitumor effects on human carcinoma cell line
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“During tumor progression, stromagenesis occurs in parallel with tumorigenesis, and predisposes to the development of tumor metastasis by generating new vessels.(11,12) A recent study demonstrated that MSCs, within the tumor stroma, promoted tumor invasion and metastasis,(13) clearly suggesting an interaction between M…”
Background
Human adipose tissue-derived mesenchymal stromal cells as vehicles for tumor bystander effect: a model based on bioluminescence imaging
Vilalta, M., Degano, I. R., Bagó, J. R., Aguilar, E., Gambhir, S. S., Rubio, N., & Blanco, J. (2008) · Gene Therapy · doi:10.1038/gt.2008.176 · Cited by 42
Comparison Between Adenoviral and Retroviral Vectors for the Transduction of the Thymidine Kinase PET Reporter Gene in Rat Mesenchymal Stem Cells
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S100A4 and Uric Acid Promote Mesenchymal Stromal Cell Induction of IL-10+/IDO+ Lymphocytes
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“Systemically transferred MSCs, for example, can also migrate into colon carcinomas (13).”
Background
Imaging techniques: new avenues in cancer gene and cell therapy
Saadatpour, Z., Rezaei, A., Ebrahimnejad, H., Baghaei, B., Bjørklund, G., Chartrand, M. S., Sahebkar, A., Morovati, H., Mirzaei, H. R., & Mirzaei, H. (2016) · Cancer Gene Therapy · doi:10.1038/cgt.2016.61 · Cited by 42
Until Death Do Us Part: Necrosis and Oxidation Promote the Tumor Microenvironment
Lotfi, R., Kaltenmeier, C., Lotze, M. T., & Bergmann, C. (2016) · Transfusion Medicine and Hemotherapy · doi:10.1159/000444941 · Cited by 42
Imaging Stem Cell Implant for Cellular-Based Therapies
Lee, Z., Dennis, J. E., & Gerson, S. L. (2008) · Experimental Biology and Medicine · doi:10.3181/0709-mr-234 · Cited by 40
“In particular, the differences between this and the other published MSC tracking study (27) are: 1) this study is a general purpose investigation on imaging-based MSC tracking technique while the other study focused on tumor metastasis tracking; 2) primary human MSCs were used here instead of immortalized MSCs; 3) thi…”
Result
Targeted destruction of the orchestration of the pancreatic stroma and tumor cells in pancreatic cancer cases: Molecular basis for therapeutic implications
Kong, X., Li, L., Li, Z., & Xie, K. (2012) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2012.06.006 · Cited by 40
In vivo Neural Stem Cell Imaging: Current Modalities and Future Directions
Gera, A., Steinberg, G. K., & Guzman, R. G. (2009) · Regenerative Medicine · doi:10.2217/rme.09.79 · Cited by 40
MR Tracking of Magnetically Labeled Mesenchymal Stem Cells in Rat Kidneys with Acute Renal Failure
Sun, J., Teng, G., Ju, S., Ma, Z., Mai, X., & Ma, M. (2008) · Cell Transplantation · doi:10.3727/096368908784153878 · Cited by 39
Antitumoral Activity and Osteogenic Potential of Mesenchymal Stem Cells Expressing the Urokinase-Type Plasminogen Antagonist Amino-Terminal Fragment in a Murine Model of Osteolytic Tumor
Fritz, V., Noël, D., Bouquet, C., Opolon, P., Voide, R., Apparailly, F., Louis‐Plence, P., Bouffi, C., Drissi, H., Xie, C. L., et al. (2008) · Stem Cells · doi:10.1634/stemcells.2008-0139 · Cited by 38
In Vivo Differentiation of Magnetically Labeled Mesenchymal Stem Cells Into Hepatocytes for Cell Therapy to Repair Damaged Liver
Ju, S., Teng, G., Lu, H., Jin, J., Zhang, Y., Zhang, A., & Ni, Y. (2010) · Investigative Radiology · doi:10.1097/rli.0b013e3181ed55f4 · Cited by 36
Pitfalls on the roadmap to γδ T cell-based cancer immunotherapies
Martinet, L., Poupot, R., & Fournié, J. (2009) · Immunology Letters · doi:10.1016/j.imlet.2009.03.011 · Cited by 38
In vivo MR imaging of magnetically labeled mesenchymal stem cells transplanted into rat liver through hepatic arterial injection
Cai, J., Zhang, X., Wang, X., Li, C., & Liu, G. (2008) · Contrast Media & Molecular Imaging · doi:10.1002/cmmi.231 · Cited by 36
Cytosine deaminase-expressing human neural stem cells inhibit tumor growth in prostate cancer-bearing mice
Lee, H. J., Doo, S. W., Kim, D. H., Cha, Y. J., Kim, J. H., Song, Y. S., & Kim, S. U. (2013) · Cancer Letters · doi:10.1016/j.canlet.2013.01.048 · Cited by 36
“Since stem cells selectively migrate towards tumors of various types [3–8], stem cells encoding therapeutic gene such as CD may serve as a more general application of gene-directed enzyme prodrug therapy of cancer [3,11–13].”
Background
Novel aspects of parenchymal–mesenchymal interactions: from cell types to molecules and beyond
Blüguermann, C., Wu, L., Petrigliano, F. A., McAllister, D. R., Miriuka, S., & Evseenko, D. A. (2013) · Cell Biochemistry and Function · doi:10.1002/cbf.2950 · Cited by 35
Pericytes Promote Malignant Ovarian Cancer Progression in Mice and Predict Poor Prognosis in Serous Ovarian Cancer Patients
Sinha, D., Chong, L., George, J., Schlüter, H., Mönchgesang, S., Mills, S. J., Li, J., Parish, C. R., Bowtell, D. D. L., & Kaur, P. (2015) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-15-1931 · Cited by 36
Stem Cell Monitoring with a Direct or Indirect Labeling Method
Kim, M. H., Lee, Y. J., & Kang, J. H. (2015) · Nuclear Medicine and Molecular Imaging · doi:10.1007/s13139-015-0380-y · Cited by 34
Lost signature: progress and failures in in vivo tracking of implanted stem cells
von der Haar, K., Lavrentieva, A. V., Stahl, F., Scheper, T. H., & Blume, C. A. (2015) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-015-6965-7 · Cited by 34
“…SPIONs (Ludtke-Buzug et al. 2010) PET In vivo Indirect MSC Human Rat 18FDG-D2R (Schonitzer et al. 2014) PET In vivo Indirect MSC Human Mouse 18FFHBG-HSV1-TK (Hung et al. 2005) PET In vivo Indirect GSC Mouse Mouse 64Cu-NOTA-AC133 (Gaedicke et al. 2014) PET In vivo Direct MSC Rat Mouse 124I-HIB…”
Background
Activation and Differentiation of Mesenchymal Stem Cells
Mishra, P. J., & Banerjee, D. (2011) · Methods in molecular biology · doi:10.1007/978-1-61779-024-9_14 · Cited by 32
A Specific Subpopulation of Mesenchymal Stromal Cell Carriers Overrides Melanoma Resistance to an Oncolytic Adenovirus
Bolontrade, M. F., Sganga, L., Piaggio, E., Viale, D. L., Sorrentino, M., Robinson, A., Sevlever, G. E., García, M. G., Mazzolini, G. D., & Podhajcer, O. L. (2012) · Stem Cells and Development · doi:10.1089/scd.2011.0643 · Cited by 32
“However, a major drawback in terms of their potential use in the clinics is the rather low amount of exonously administered MSCs able to reach the tumor mass [22,26–28].”
Pre-clinical models for studying the interaction between mesenchymal stromal cells and cancer cells and the induction of stemness
Avnet, S., Lemma, S., Cortini, M., Di Pompo, G., Perut, F., & Baldini, N. (2019) · Frontiers in Oncology · doi:10.3389/fonc.2019.00305 · Cited by 29
“colon carcinoma (62, 64, 65, 74–77) (52, 62, 64, 65)”
Method
Molecular imaging of cell-based cancer immunotherapy
Liu, G., Swierczewska, M., Niu, G., Zhang, X. M., & Chen, X. S. (2011) · Molecular BioSystems · doi:10.1039/c0mb00198h · Cited by 30
PET Imaging of β-Glucuronidase Activity by an Activity-Based 124I-Trapping Probe for the Personalized Glucuronide Prodrug Targeted Therapy
Su, Y.-C., Cheng, T.-C., Leu, Y.-L., Roffler, S. R., Wang, J., Chuang, C., Kao, C.-H., Chen, K., Wang, H.-E., & Cheng, T. (2014) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-14-0212 · Cited by 30
Activation and Differentiation of Mesenchymal Stem Cells
Mishra, P. J., & Banerjee, D. (2017) · Methods in molecular biology · doi:10.1007/978-1-4939-6759-9_13 · Cited by 30
Amniotic fluid-derived mesenchymal stem cells: characteristics and therapeutic applications
Zhou, J., Wang, D., Liang, T., Guo, Q., & Zhang, G. (2014) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-014-3231-7 · Cited by 30
“The tropism of MSCs has been demonstrated in various experimental tumor models, including malignant melanoma, Kaposi’s sarcoma, colon cancer, ovarian cancer, ewing sarcoma, fibrosarcoma, breast cancer and renal cell carcinoma [4, 50, 52, 54, 55].”
Background
Nuclear Imaging of Cancer Cell Therapies
Ponomarev, V. (2009) · Journal of Nuclear Medicine · doi:10.2967/jnumed.109.064055 · Cited by 29
“A similar approach has been used for the monitoring of mesenchymal stem cell targeting of microscopic tumors and tumor stroma development (21).”
Method
Human menstrual blood-derived mesenchymal stem cells as a cellular vehicle for malignant glioma gene therapy
Wang, X., Xiang, B., Ding, Y., Chen, L., Zou, H., Mou, X., & Xiang, C. C. (2017) · Oncotarget · doi:10.18632/oncotarget.17621 · Cited by 29
“Several studies have confirmed that MSCs migrate toward human gliomas in vivo, [5, 24] and transduced MSCs retain a migratory ability that is similar to the pattern observed in untransduced MSCs [25].”
Result
Imaging of human mesenchymal stromal cells: homing to human brain tumors
Menon, L. G., Pratt, J. S., Yang, H. W., Black, P. M., Sorensen, A. G., & Carroll, R. S. (2011) · Journal of Neuro-Oncology · doi:10.1007/s11060-011-0754-7 · Cited by 29
Construction of Mutant TKGFP for Real-Time Imaging of Temporal Dynamics of HIF-1 Signal Transduction Activity Mediated by Hypoxia and Reoxygenation in Tumors in Living Mice
Hsieh, C., Kuo, J.-W., Lee, Y., Chang, C., Gelovani, J. G., & Liu, R.-S. (2009) · Journal of Nuclear Medicine · doi:10.2967/jnumed.108.061234 · Cited by 30
Self-citation
Human Bone Marrow-Derived Mesenchymal Stem Cells
Nasef, A., Fouillard, L., Taguri, A. E., & Lopez, M. (2007) · Libyan Journal of Medicine · doi:10.3402/ljm.v2i4.4729 · Cited by 29
Mesenchymal Stem Cell-Derived Extracellular Vesicles: Pleiotropic Impacts on Breast Cancer Occurrence, Development, and Therapy
Guo, Y., Zhai, Y., Wu, L., Wang, Y., Wu, P., & Xiong, L. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23062927 · Cited by 28
Therapeutic potential of transgenic mesenchymal stem cells engineered to mediate anti–high mobility group box 1 activity: targeting of colon cancer
Kikuchi, H., Yagi, H., Hasegawa, H., Ishii, Y., Okabayashi, K., Tsuruta, M., Hoshino, G., Takayanagi, A., & Kitagawa, Y. (2014) · Journal of Surgical Research · doi:10.1016/j.jss.2014.02.047 · Cited by 28
“Among these studies, a recent report documented that colon cancer can also recruit MSCs by secreting bioactive molecules [37,38].”
Background
Tracking Inflammation-Induced Mobilization of Mesenchymal Stem Cells
Spaeth, E. L., Kidd, S. M., & Marini, F. C. (2012) · Methods in molecular biology · doi:10.1007/978-1-61779-943-3_15 · Cited by 28
The Development of a Novel Cancer Immunotherapeutic Platform Using Tumor-targeting Mesenchymal Stem Cells and a Protein Vaccine
Wei, H.-J., Wu, A. T. H., Hsu, C.-H., Lin, Y.-P., Cheng, W., Su, C., Chiu, W., Whang‐Peng, J., Douglas, F. L., & Deng, W. (2011) · Molecular Therapy · doi:10.1038/mt.2011.152 · Cited by 28
Self-citation
Serial in vivo imaging of the lung metastases model and gene therapy using HSV1-tk and ganciclovir.
Deng, W. P., Wu, C., Lee, C.-C., Yang, W.-K., Wang, H.-E., Liu, R. S., Wei, H.-J., Gelovani, J. G., Hwang, J., Yang, D. M., et al. (2006) · PubMed · Cited by 28
Self-citation
Tumor microenvironment and the role of mesenchymal stromal cells
KUCEROVA, L., & SKOLEKOVA, S. (2012) · Neoplasma · doi:10.4149/neo_2013_001 · Cited by 27
Genotoxic damage of human adipose-tissue derived mesenchymal stem cells triggers their terminal differentiation
Altanerová, V., Horváthová, E., Matúšková, M., Kučerová, L., & Altaner, Č. (2009) · Neoplasma · doi:10.4149/neo_2009_06_542 · Cited by 28
“Increasing number of reports indicated that MSCs are recruited in large numbers to the stroma of developing tumors [21, 24], or they could act by enhancing the motility, invasion and metastasis ability of adjacent cancer cells [25].”
Background
The Impact of Mesenchymal Stem Cell Source on Proliferation, Differentiation, Immunomodulation and Therapeutic Efficacy
Cheng, H. Y. (2014) · Journal of Stem Cell Research & Therapy · doi:10.4172/2157-7633.1000237 · Cited by 27
Transcriptional profiling of interleukin-2-primed human adipose derived mesenchymal stem cells revealed dramatic changes in stem cells response imposed by replicative senescence
Niu, P., Smagul, A., Wang, L., Sadvakas, A., Sha, Y., Pérez, L. M., Nussupbekova, A., Amirbekov, A., Akanov, A. A., Gálvez, B. G., et al. (2015) · Oncotarget · doi:10.18632/oncotarget.4852 · Cited by 26
Proliferating fibroblasts and HeLa cells co-cultured in vitro reciprocally influence growth patterns, protein expression, chromatin features and cell survival.
Delinassios, J. G., Angeli, F., Koumakis, G., Kumar, S., Kang, W.-H., Sica, G., Iacopino, F., Lama, G., Lamprecht, S. A., Sigal-Batikoff, I., et al. (2015) · PubMed · Cited by 24
Stem Cell Based Gene Therapy in Prostate Cancer
Kim, J. H., Lee, H. J., & Song, Y. S. (2014) · BioMed Research International · doi:10.1155/2014/549136 · Cited by 26
“This is probably due to less number of therapeutic cells reaching the tumor with this delivery route [25] and to the fact that therapeutic cells are administered at a later timepoint.”
Background
Molecular imaging of stem cells
Gambhir (2009) · StemBook · doi:10.3824/stembook.1.49.1 · Cited by 26
The therapeutic potential of bone marrow‐derived mesenchymal stromal cells on hepatocellular carcinoma
Bayo, J., Marrodán, M., Aquino, J. B., Silva, M., García, M. G., & Mazzolini, G. D. (2013) · Liver International · doi:10.1111/liv.12338 · Cited by 24
“Homing of MSCs towards experimental tumours has been reported in several animal models including glioma (89, 90), melanoma (32), breast (33), colon (91), HCC (92–94) and liver metastasis of colon cancer (95).”
Background
Multipotent mesenchymal stromal cells promote tumor growth in distinct colorectal cancer cells by a β1‐integrin‐dependent mechanism
Widder, M., Lützkendorf, J., Caysa, H., Unverzagt, S., Wickenhauser, C., Benndorf, R. A., Schmoll, H., Müller‐Tidow, C., Müller, T. H., & Müller, L. P. (2015) · International Journal of Cancer · doi:10.1002/ijc.29844 · Cited by 24
“J. Cancer: 138, 964–975 (2016) VC 2015 UICC International Journal of Cancer IJC cytokines, carcinoma associated fibroblasts (CAF) and an increased production of extracellular matrix (ECM).6–8 Several studies suggest that CAF can be derived from multipotent mesenchymal stromal cells (MSC).9 MSC represent a distinct pop…”
BackgroundInfluential
In Vivo Mesenchymal Stem Cell Tracking with PET Using the Dopamine Type 2 Receptor and 18F-Fallypride
Schönitzer, V., Haasters, F., Käsbauer, S., Ulrich, V., Mille, E., Gildehaus, F. J., Carlsen, J., Pape, M., Beck, R., Delker, A., et al. (2014) · Journal of Nuclear Medicine · doi:10.2967/jnumed.113.134775 · Cited by 23
“There is unfortunately no advantage here over, for example, the use of hMSCs expressing HSV1-Tk, which shows even a more intense bowel uptake (35).”
Background
Adipose-Derived Stem Cells Enhance Cancer Stem Cell Property and Tumor Formation Capacity in Lewis Lung Carcinoma Cells Through an Interleukin-6 Paracrine Circuit
Lu, J.-H., Wei, H.-J., Peng, B., Chou, H.-H., Chen, W.-H., Liu, H., & Deng, W. (2016) · Stem Cells and Development · doi:10.1089/scd.2016.0163 · Cited by 23
Self-citation
Anti-tumor effects of engineered mesenchymal stem cells in colon cancer model
Yang, J., Lv, K., Sun, J., & Guan, J. (2019) · Cancer Management and Research · doi:10.2147/cmar.s209880 · Cited by 23
Exosomes Derived from Breast Cancer Cells, Small Trojan Horses?
Villagrasa, A., Alvarez, P. J., Osuna, A., Garrido, J. M., Aránega, A., & Rodríguez‐Serrano, F. (2014) · Journal of Mammary Gland Biology and Neoplasia · doi:10.1007/s10911-015-9332-5 · Cited by 24
“Mesenchymal stem cells (MSCs) have the capacity to differentiate into a large number of cell types [63] but they can also act as precursors of tumor stroma, in part through the generation of myofibroblasts that provide a favorable environment for tumor progression [64, 65].”
Background
Heterotypic signaling of cancer-associated fibroblasts in shaping the cancer cell drug resistance
Butti, R., Khaladkar, A., Bhardwaj, P., & Prakasam, G. (2023) · Cancer Drug Resistance · doi:10.20517/cdr.2022.72 · Cited by 23
Gene, Stem Cell, and Future Therapies for Orphan Diseases
Phillips, M. I. (2012) · Clinical Pharmacology & Therapeutics · doi:10.1038/clpt.2012.82 · Cited by 20
Translational aspects in targeting the stromal tumour microenvironment: From bench to bedside
Bhome, R., AlSaihati, H., Goh, R. W., Bullock, M. D., Primrose, J. M., Thomas, G. J., Sayan, E., & Mirnezami, A. H. (2016) · European Journal of Molecular & Clinical Medicine · doi:10.1016/j.nhtm.2016.03.001 · Cited by 22
“The mesenchymal stroma and ECM are equally important in cancer progression but therapies specifically targeting CAFs, MSCs and ECM proteins are fewer and in comparatively earlier stages of development.”
BackgroundInfluential
Increased proliferation and chemosensitivity of human mesenchymal stromal cells expressing fusion yeast cytosine deaminase
Kučerová, L., Poturnajova, M., Tyčiaková, S., & Matúšková, M. (2011) · Stem Cell Research · doi:10.1016/j.scr.2011.11.006 · Cited by 21
“Hung et al. (2005) detected radiolabelled substrate retention indicative of HSV-TK-MSCs' participation in tumor stroma via micro-PET imaging.”
Background
How tumors might withstand γδ T-cell attack
Capietto, A.-H., Martinet, L., & Fournié, J. (2011) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-011-0705-7 · Cited by 24
“MSCs are present in melanoma [51], glioma [52], carcinoma of the colon [53], ovaries [54], breast [55] and in the microenvironment of gastric carcinoma [56].”
Background
Titration of Variant HSV1-tk Gene Expression to Determine the Sensitivity of 18F-FHBG PET Imaging in a Prostate Tumor
Johnson, M., Karanikolas, B. D. W., Priceman, S. J., Powell, R., Black, M. E., Wu, H.-M., Czernin, J. G., Huang, S., & Wu, L. (2009) · Journal of Nuclear Medicine · doi:10.2967/jnumed.108.058438 · Cited by 20
“This noninvasive and highly sensitive approach can be used to monitor the biodistribution (2,3), magnitude (4,5), and persistence of the therapeutic gene expression over time (6,7).”
The myofibroblast in connective tissue repair and regeneration
Hinz, B. (2010) · Elsevier eBooks · doi:10.1533/9781845697792.39 · Cited by 20
Migratory Properties of Mesenchymal Stem Cells
Dittmar, T., & Entschladen, F. (2012) · Advances in biochemical engineering, biotechnology · doi:10.1007/10_2012_144 · Cited by 20
Tumor-Targeted Immunotherapy by Using Primary Adipose-Derived Stem Cells and an Antigen-Specific Protein Vaccine
Lu, J.-H., Peng, B., Chang, C., Dubey, N. K., Lo, W., Cheng, H.-C., Wang, J., Wei, H.-J., & Deng, W. (2018) · Cancers · doi:10.3390/cancers10110446 · Cited by 20
Self-citation
Combination of Mesenchymal Stem Cell-Delivered Oncolytic Virus with Prodrug Activation Increases Efficacy and Safety of Colorectal Cancer Therapy
Ho, C.-T., Wu, M.-H., Chen, M., Lin, S., Yen, Y., & Hung, S. (2021) · Biomedicines · doi:10.3390/biomedicines9050548 · Cited by 20
“The bio‐ distribution and cell‐fate tracking of human MSCs following IV infusion into mice bearing human tumor xenografts have been well studied before [13].”
BackgroundSelf-citation
Combination of Single-Photon Emission Computed Tomography and Magnetic Resonance Imaging to Track 111 In-Oxine–Labeled Human Mesenchymal Stem Cells in Neuroblastoma-Bearing Mice
Cussó, L., Mirones, I., Peña-Zalbidea, S., García‐Vázquez, V., Garcı́a-Castro, J., & Desco, M. (2014) · Molecular Imaging · doi:10.2310/7290.2014.00033 · Cited by 19
“, infarcted myocardium) in animals and patients.(3,4) hMSCs are also capable of homing to several types of tumors, including glioma, carcinoma (breast, colon, and lung), leukemia, and many types of metastatic tumors.”
Background
Current status and challenges of stem cell-based therapy for the treating of glioblastoma multiforme Stem cell-based therapy treating glioblastoma multiforme
Abadi, B., Ahmadi‐Zeidabadi, M., Dini, L., & Vergallo, C. (2020) · Hematology/Oncology and Stem Cell Therapy · doi:10.1016/j.hemonc.2020.08.001 · Cited by 22
“Positron emission tomography is another imaging detection method of therapeutic SCs highly sensitive [139].”
Effect of bone marrow mesenchymal stem cells on hepatocellular carcinoma in microcirculation
Gong, P., Wang, Y., Wang, Y., Jin, S., Luo, H., Zhang, J., Bao, H., & Wang, Z. (2013) · Tumor Biology · doi:10.1007/s13277-013-0749-4 · Cited by 18
Safety and Efficacy Endpoints for Mesenchymal Stromal Cell Therapy in Renal Transplant Recipients
Bank, J. R., Rabelink, T. J., de Fijter, J. W., & Reinders, M. E. J. (2015) · Journal of Immunology Research · doi:10.1155/2015/391797 · Cited by 17
“In vitro and in vivo studies have shown that MSCs have a potential for mal differentiation into neoplastic cells as well as the possibility to promote growth of the tumor cells [54, 55].”
Background
Regulated Mesenchymal Stem Cells Mediated Colon Cancer Therapy Assessed by Reporter Gene Based Optical Imaging
Kalimuthu, S., Zhu, L., Oh, J. H., Lee, H., Gangadaran, P., Rajendran, R. L., Baek, S. H., Jeon, Y., Jeong, S., Lee, S., et al. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19041002 · Cited by 18
“The FACS-sorted immortalized MSCs expressing HSV1-sr39TK exhibited in vitro susceptibility to GCV [19].”
Pancreatic cancer growth promoted by bone marrow mesenchymal stromal cell–derived IL-6 is reversed predominantly by IL-6 blockade
Antoon, R., Wang, X., Saleh, A. H., Warrington, J., Hedley, D. W., & Keating, A. (2022) · Cytotherapy · doi:10.1016/j.jcyt.2021.12.005 · Cited by 17
In vitro labeling of endothelial progenitor cells isolated from peripheral blood with superparamagnetic iron oxide nanoparticles
Sun, J., Zhang, Y., Nie, C., QIAN, S.-P., Yu, X., Xie, H., Zhou, L., & Zheng, S. (2012) · Molecular Medicine Reports · doi:10.3892/mmr.2012.912 · Cited by 17
“In order to monitor the transplanted cells, several non-invasive in vivo tracking imaging techniques, such as MRI, nuclear medicine and optical imaging, have been investigated (23-25).”
IFNα-Expressing Amniotic Fluid-Derived Mesenchymal Stem Cells Migrate to and Suppress HeLa Cell-Derived Tumors in a Mouse Model
Zhou, J., Liang, T., Wang, D., Li, L., Cheng, Y., Guo, Q., & Zhang, G. (2018) · Stem Cells International · doi:10.1155/2018/1241323 · Cited by 17
“They are not only of low immunogenicity and oncogenicity, but they can also selectively migrate to tumor sites [2, 3, 9, 10].”
Background
Hyperthermia on mesenchymal stem cells (MSCs) can sensitize tumor cells to undergo cell death†
Park, H., Cho, J.-A., Kim, S., Kim, J., & Lee, S. (2008) · International Journal of Hyperthermia · doi:10.1080/02656730802253117 · Cited by 17
“During tumor progression, stromagenesis occurs in parallel with tumorigenesis and predisposes to the development of tumor metastasis by generating new vessels [15, 17, 18].”
Background
Human mesenchymal stem cells preferentially migrate toward highly oncogenic human hepatocellular carcinoma cells with activated EpCAM signaling
Endaya, B., Guan, S. P., Newman, J. P. A., Huynh, H. T., Sia, K. C., Chong, S. T., Kok, C. Y. L., Chung, A. Y. F., Liu, B. B., Hui, K. M., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.17633 · Cited by 16
“The findings that MSC could target microscopic tumors when administered systemically [3] bear important www.”
Background
ATP promotes immunosuppressive capacities of mesenchymal stromal cells by enhancing the expression of indoleamine dioxygenase
Lotfi, R., Steppe, L., Hang, R., Rojewski, M., Massold, M., Jahrsdörfer, B., & Schrezenmeier, H. (2018) · Immunity Inflammation and Disease · doi:10.1002/iid3.236 · Cited by 16
“Systemically transferred MSCs, for example, can also migrate into tumor tissue such as colon carcinomas or glioblastoma.(13,14) MSCs can act as immunoregulatory cells, releasing IL-10 and prostaglandin E2, or by expressing the enzyme indoleamine 2,3-dioxygenase (IDO).”
Background
De novo formed satellite DNA-based mammalian artificial chromosomes and their possible applications
Katona, R. (2015) · Chromosome Research · doi:10.1007/s10577-014-9458-0 · Cited by 14
“…possibly supporting tumor growth and inducing resistance to chemotherapy (Aboody et al. 2006a; Aboody et al. 2006b; Danks et al. 2007; Houthuijzen et al. 2012; Hung et al. 2005; Karnoub et al. 2007; Koh and Kang 2012; Orimo et al. 2005; Roodhart et al. 2011; Studeny et al. 2004; Zhu et al. 2006).”
Background
A Novel Cell-Based Therapy for Contusion Spinal Cord Injury Using GDNF-Delivering NIH3T3 Cells with Dual Reporter Genes Monitored by Molecular Imaging
Lo, W., Hsu, C.-H., Wu, A. T. H., Yang, L., Chen, W.-H., Chiu, W., Lai, W., Wu, C., Gelovani, J. G., & Deng, W. (2008) · Journal of Nuclear Medicine · doi:10.2967/jnumed.108.051896 · Cited by 15
“To develop a novel therapy consisting of GDNF-secreting cells for the amelioration of SCI using a rat model, we used gene-modified NIH3T3 cells (NIH3T3-TG), which contain dual reporters, namely herpes simplex virus type I thymidine kinase (HSV1-TK; T) and Aequorea victoria–enhanced green fluorescent protein (eGFP; G),…”
BackgroundMethodSelf-citation
Pericytes in Metastasis
Pieterse, Z., Sinha, D., & Kaur, P. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-16908-4_5 · Cited by 14
Noninvasive in vivo cell tracking using molecular imaging: A useful tool for developing mesenchymal stem cell-based cancer treatment
Rajendran, R. L., Jogalekar, M. P., Gangadaran, P., & Ahn, B. (2020) · World Journal of Stem Cells · doi:10.4252/wjsc.v12.i12.1492 · Cited by 14
Dissecting Mesenchymal Stem Cell Movement: Migration Assays for Tracing and Deducing Cell Migration
Spaeth, E. L., & Marini, F. C. (2011) · Methods in molecular biology · doi:10.1007/978-1-61779-145-1_17 · Cited by 14
Genetically Modified Murine Adipose-Derived Mesenchymal Stem Cells Producing Interleukin-2 Favor B16F10 Melanoma Cell Proliferation
Bahrambeigi, V., Ahmadi, N., Salehi, R., & Javanmard, S. H. (2015) · Immunological Investigations · doi:10.3109/08820139.2014.988719 · Cited by 14
“…response suppression (Djouad et al., 2003), inhibition of tumor apoptosis (Ramasamy et al., 2007), stimulation of an epithelial-to-mesenchymal transition (Martin et al., 2010), angiogenesis (Hung et al., 2005), cancer stem cell populations (Liu et al., 2011), and metastasis (Karnoub et al., 2007).”
Background
Targeted antitumor therapy mediated by prodrug-activating mesenchymal stromal cells
Kučerová, L., Durinikova, E., Toro, L., Cihova, M., Miklikova, S., Poturnajova, M., Kozovská, Z., & Matúšková, M. (2017) · Cancer Letters · doi:10.1016/j.canlet.2017.08.016 · Cited by 13
Mesenchymal Stem Cells as Regulators of Carcinogenesis
Hayal, T. B., Kıratlı, B., Şişli, H. B., Şahin, F., & Doğan, A. (2018) · Advances in experimental medicine and biology · doi:10.1007/5584_2018_311 · Cited by 13
Genetically Engineered Multilineage-Differentiating Stress-Enduring Cells as Cellular Vehicles against Malignant Gliomas
Yamasaki, T., Wakao, S., Kawaji, H., Koizumi, S., Sameshima, T., Dezawa, M., & Namba, H. (2017) · Molecular Therapy — Oncolytics · doi:10.1016/j.omto.2017.06.001 · Cited by 13
“A highly promising noninvasive method to visualize the presence of HSVtk gene-expressing cells in the brain is positron emission tomographic scans using radioactive nucleic acid analogs, such as 9-(4-(18)F-fluoro-3-[hydroxymethyl]butyl)guanine, as the reporter.(38,39) In clinical trials, these strategies could be used…”
Method
In Vivo Stem Cell Imaging
Zhao, C., Tian, M., & Zhang, H. (2010) · The Open Nuclear Medicine Journal · doi:10.2174/1876388x01002010171 · Cited by 12
“Techniques available for in vivo molecular imaging so far include MR imaging [17], fluorescence and bioluminescence imaging [18, 19], SPECT and PET [20-22] based on their different principle (Table 1).”
BackgroundInfluential
Imaging Mesenchymal Stem Cell Migration and the Implications for Stem Cell-Based Cancer Therapies
Wang, H., & Chen, X. S. (2008) · Future Oncology · doi:10.2217/14796694.4.5.623 · Cited by 12
Biological characteristics of adipose tissue‐derived stem cells labeled with amine‐surface‐modified superparamagnetic iron oxide nanoparticles
Wang, N., Zhao, J., Guan, X., Dong, Y., Liu, Y., Zhou, X., Wu, R., Du, Y., Zhao, L., Zou, W., et al. (2015) · Cell Biology International · doi:10.1002/cbin.10457 · Cited by 11
“These techniques include nuclear medicine, optical imaging, and MRI (Weissleder, 1999; Shichinohe et al., 2004; Hung et al., 2005).”
Method
The use of hypoxic cultured mesenchymal stem cell for oncolytic virus therapy
Yf, H., Chen, M.-J., Wu, M., & Hung, S.-C. (2013) · Cancer Gene Therapy · doi:10.1038/cgt.2013.22 · Cited by 11
Self-citation
Reconstitution of Schwannian Stroma in Neuroblastomas Using Human Bone Marrow Stromal Cells
Du, W., Hozumi, N., Sakamoto, M., Hata, J.-I., & Yamada, T. (2008) · American Journal Of Pathology · doi:10.2353/ajpath.2008.070309 · Cited by 11

Authors: Hung, S.-C., Deng, W.-P., Yang, W. K., Liu, R.-S., Lee, C.-C., Su, T.-C., Lin, R.-J., Yang, D.-M., Chang, C.-W., Chen, W.-H., Wei, H.-J., & Gelovani, J. G.
Affiliations: Institute of Biomedical Sciences, Academia Sinica (TW)
Taipei Medical University (TW)
Taipei Veterans General Hospital (TW)
2Institute of Biomedical Materials, Taipei Medical University; Departments of
The University of Texas MD Anderson Cancer Center (US)
ORCID: Hung, Shih-Chieh
Deng, Win-Ping
Yang, Wen K.
Chang, Chi-Wei
Gelovani, Juri G.
Venue: Clinical Cancer Research
Publisher: American Association for Cancer Research (AACR)
Published: 2005-11-01
Volume: 11
Issue: 21
Pages: 7749-7756
ISSN: 1078-0432 (ISSN-L)
1557-3265
DOI: 10.1158/1078-0432.ccr-05-0876
OpenAlex: W2149287721
Cited by: 268
References: 46
Citations by year: 2026: 1 · 2025: 1 · 2024: 2 · 2023: 4 · 2022: 5 · 2021: 8 · 2020: 4 · 2019: 7 · 2018: 10 · 2017: 12 · 2016: 19 · 2015: 17 · 2014: 15 · 2013: 29 · 2012: 19
FWCI: 7.14
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Clinical Cancer Research (publishedVersion)
PubMed (publishedVersion)
Funders: University of California, Los Angeles
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Mesenchymal stem cell research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Bacterial Cancer Therapy
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
Keywords: mesenchymal stem cells, tumor targeting, tumor stroma, HSV-1 thymidine kinase, suicide gene therapy, cytokine gene therapy, 18F-FHBG, stem cell differentiation, endothelial cells, colon cancer, HT-29 cells, non-invasive imaging, stem cell trafficking
MeSH terms: Animals, Cell Membrane, Flow Cytometry, Genetic Vectors, Humans, Immunohistochemistry, Mesoderm, Neoplasm Transplantation, Neoplasms, Stem Cells, Time Factors, Protein Biosynthesis, Genetic Therapy, Lentivirus, Polymerase Chain Reaction, Cytokines, Genes, Reporter, Platelet Endothelial Cell Adhesion Molecule-1, Cell Line, Tumor, Cell Proliferation, Positron-Emission Tomography, Green Fluorescent Proteins, Mice

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Mesenchymal Stem Cell Targeting of Microscopic Tumors and Tumor Stroma Development Monitored by Noninvasive In vivo Positron Emission Tomography Imaging

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