CoChat
Sign Up
Cited by 45Mesenchymal stem cell researchCancer Cells and MetastasisImmune cells in cancer

The DOI matches its Crossref record; 7 of the 7 references it cites were found in a registry or an index.

Influence of mesenchymal stem cells on metastasis development in mice in vivo

Open access
Meleshina, Aleksandra V, Cherkasova, Elena I, Shirmanova, Marina V, Klementieva, Natalia V, Kiseleva, Ekaterina V, Snopova, Ludmila В, Prodanets, Natalia N, Zagaynova, Elena V·2015·Stem Cell Research & Therapy
DOI 10.1186/s13287-015-0003-7PMC PMC4415299
Open this paper in CoChat — free accountOpen PDF

Abstract

Introduction: In recent years, mesenchymal stem cells (MSCs) have been demonstrated to play an important role in carcinogenesis. However, the effect of MSCs on tumor and metastasis development and the mechanisms underlying the interaction of cancer and stem cells are not completely understood. This study investigated the effect of MSCs on breast cancer metastasis formation by using the methods of in vivo fluorescence and luminescence imaging. Methods: MSCs were isolated from bone marrow of normal donors, characterized, and genetically labeled with luciferase (luc2). The effects of MSCs on MDA-MB-231 cancer cell proliferation were evaluated in conditioned medium from MSCs. To generate lung metastases, MDA-MB-231 cells stably expressing red fluorescent protein Turbo FP650 were injected intravenously into nude mice. On day 10 after the cancer cell injection, mice were injected via the tail vein with MSCs-luc2 cells (the MET + MSCs group). Animals that received the injection of MDA-MB-231-Turbo FP650 alone (the MET group) and no injections (the intact control group) served as controls. Fluorescence and bioluminescence imaging was performed for monitoring of the metastasis formation and MSC distribution in the recipient’s body. Results: We found that the proliferative activity of the cancer cells in the presence of MSC conditioned medium was lower than that of the cells grown in conventional culture medium. The metastasis formation in the MET + MSCs group was delayed in time as compared with the MET group. Macroscopic and histological examination of isolated lungs 8 weeks after cancer cell injection showed that the total number of metastases in animals of the MET + MSCs group was significantly lower. Using bioluminescence imaging in vivo, we found that MSCs-luc2 cells survived in the host animal for at least 7 weeks and re-migrated to the lung 6 to 7 weeks after injection. Immunohistochemical analysis revealed the presence of MSCs-luc2 in metastases and lung tissue. Conclusions: Long-term in vivo bioluminescence imaging of intravenously injected MSCs-luc2 cells showed distribution of MSCs to the lungs and abdominal organs within the first 2 to 3 weeks and re-migration to the lungs in weeks 6 to 7. It was found that MSCs reduced the proliferative activity of cancer cells in vitro and lung metastasis formation in mice.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1186/s13287-015-0003-7

Cites

7 of 7 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

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

  • Many authors have reported the effect of the secretome of MSCs on tumor cell proliferation and invasion in vitro and in vivo.

    “many authors have been reported the effect of the secretome of MSCs in tumor cell proliferation and invasion in vitro and in vivo [104], [105], [106], [107].”

    From Mesenchymal stem cell secretome for regenerative medicine: Where do we stand? (2025) · cites this paper as [105]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 44

  1. Komarova S, Kawakami Y, Stoff-Khalili MA. Mesenchymal progenitor cells as cellular vehicles for delivery of oncolytic adenoviruses. Mol Cancer Ther. 2006;5:755–66. · DOI · Paper page
  2. Ren C, Kumar S, Chanda D. Therapeutic potential of mesenchymal stem cells producing interferon-alpha in a mouse melanoma lung metastasis model. Stem Cells. 2008;26:2332–8. · DOI
  3. Niess H, Bao Q, Conrad C. Selective targeting of genetically engineered mesenchymal stem cells to tumor stroma microenvironments using tissuespecific suicide gene expression suppresses growth of hepatocellular carcinoma. Ann Surg. 2011;254:767–74. · DOI
  4. Stagg J. Mesenchymal stem cells in cancer. Stem Cell Rev. 2008;4:119–24. · DOI
  5. Roorda BD, TerElst A, Kamps WA, Bont ES. Bone marrow-derived cells and tumor growth:contribution of bone marrow-derived cells to tumor micro-environments with special focus on mesenchymal stem cells. Crit Rev Oncol Hematol. 2009;69:187–98. · DOI
  6. Bhowmick NA, Neilson EG, Moses HL. Stromal fibroblasts in cancer initiation and progression. Nature. 2004;432:332–7. · DOI
  7. Hu M, Polyak K. Molecular characterisation of the tumour microenvironment in breast cancer. Eur J Cancer. 2008;44:2760–5. · DOI
  8. Hugo H, Ackland ML, Blick T. Epithelial-mesenchymal and mesenchymal - epithelial transitions in carcinoma progression. J Cell Physiol. 2007;213:374–83. · DOI
  9. Yang J, Weinberg RA. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev Cell. 2008;14:818–29. · DOI
  10. Karnoub AE, Dash AB, Vo AP, Sullivan A, Brooks MW, Bell GW, et al. Mesenchymal stem cells within tumor stroma promote breast cancer metastasis. Nature. 2007;449:557–63. · DOI · Paper page
  11. Stoff-Khalili MA, Rivera AA, Mathis JM, Banerjee NS, Moon AS, Hess A, et al. Mesenchymal stem cells as a vehicle for targeted delivery of CRAds to lung metastases of breast carcinoma. Breast Cancer Res Treat. 2007;105:157–67. · DOI
  12. Ling X, Marini F, Konopleva M, Schober W, Shi Y, Burks J, et al. Mesenchymal stem cells overexpressing IFN-β inhibit breast cancer growth and metastases through Stat3 signaling in a syngeneic tumor model. Cancer Microenviron. 2010;3:83–95. · DOI
  13. Qiao L, Zhao TJ, Wang FZ, Shan CL, Ye LH, Zhang XD. NF-kappaB downregulation may be involved the depression of tumor cell proliferation mediated by human mesenchymal stem cells. Acta Pharmacol Sin. 2008;29:333–40. · DOI
  14. Loebinger MR, Janes SM. Stem cells as vectors for antitumour therapy. Thorax. 2010;65:362–9. · DOI · Paper page
  15. Wang ML, Pan CM, Chiou SH, Chen WH, Chang HY, Lee OK, et al. Oncostatin m modulates the mesenchymal–epithelial transition of lung adenocarcinoma cells by a mesenchymal stem cell-mediated paracrine effect. Tumor Stem Cell Biol. 2012;72:6051–64.
  16. Liu J, Han G, Liu H, Qin C. Suppression of cholangiocarcinoma cell growth by human umbilical cord mesenchymal stem cells: a possible role of Wnt and Akt signaling. PLoS One. 2013;8:e62844. · DOI
  17. Hou L, Wang X, Zhou Y, Ma H, Wang Z, He J, et al. Inhibitory effect and mechanism of mesenchymal stem cells on liver cancer cells. Tumour Biol. 2014;35:1239–50. · DOI
  18. Zhao C, Tian M, Zhang H. In vivo stem cell imaging. The Open Nucl Med J. 2010;2:171–7. · DOI
  19. Gao Y, Cui Y, Chan JKY, Xu C. Stem cell tracking with optically active nanoparticles. Am J Nucl Med Mol Imaging. 2013;3:232–46.
  20. Zhou Y, Shao G, Liu S. Monitoring breast tumor lung metastasis by U-SPECT-II/CT with an integrinαvβ3-targeted radiotracer 99m Tc-3P-RGD2. Theranostics. 2012;2:577–88. · DOI
  21. Greer LF, Szalay AA. Imaging of light emission from the expression of luciferases in living cells and organisms: a review. Luminescence. 2002;17:43–74. · DOI
  22. Ruan J, Song H, Li C, Bao Ch FH, Wang K, Ni J, et al. DiR-labeled embryonic stem cells for targeted imaging of in vivo gastric cancer cells. Theranostics. 2012;2:618–28. · DOI
  23. Alieva M, Bagó JR, Aguilar E, Soler-Botija C, Vila OF, Molet J, et al. Glioblastoma therapy with cytotoxic mesenchymal stromal cells optimized by bioluminescence imaging of tumor and therapeutic cell response. PLoS One. 2012;7:e35148. doi:10.1371/journal.pone.0035148. · DOI
  24. Shah K. Imaging neural stem cell fate in mouse model of glioma. Curr Protoc Stem Cell Biol. 2009 Mar;Chapter 5:Unit 5A.1. doi:10.1002/9780470151808.sc05a01s8. · DOI
  25. Ke C, Liu R, Suetsugu A, Kimura H, Ho JH, Lee OK, et al. In vivo fluorescence imaging reveals the promotion of mammary tumorigenesis by mesenchymal stromal cells. PLoS One. 2013;8:e69658. · DOI
  26. Wang H, Cao F, De A. Trafficking mesenchymal stem cell engraftment and differentiation in tumor-bearing mice by bioluminescence imaging. Stem Cells. 2009;27:1548–58. · DOI
  27. Wang Y, Li Z. Traceable therapeutic strategy for treatment of breast cancer with mesenchymal stem cells (MSCs). Cancer Cell Microenvironment. 2014;1:e198.
  28. Leng L, Wang Y, He N, Wang D, Zhao Q, Feng G, et al. Molecular imaging for assessment of mesenchymal stem cells mediated breast cancer therapy. Biomaterials. 2014;35:5162–70. · DOI
  29. Mandel K, Yang Y, Schambach A, Glage S, Otte A, Hass R. Mesenchymal stem cells directly interact with breast cancer cells and promote tumor cell growth in vitro and in vivo. Stem Cells Dev. 2013;22:3114–27. · DOI
  30. Cuiffo BG, Karnoub AE. Mesenchymal stem cells in tumor development, Emerging roles and concepts. Cell Adhesion Migration. 2012;6:220–30. · DOI
  31. Albarenque SM, Zwacka RM, Mohr A. Both human and mouse mesenchymal stem cells promote breast cancer metastasis. Stem Cell Res. 2011;7:163–71. · DOI
  32. Ljujic B, Milovanovic M, Volarevic V, Murray B, Bugarski D, Przyborski S, et al. Human mesenchymal stem cells creating an immunosuppressive environment and promote breast cancer in mice. Scientific Reports. 2013;3:1–9. · DOI
  33. Qiao L, Xu Z, Zhao T, Zhao Z, Shi M, Zhao RC, et al. Suppression of tumorigenesis by human mesenchymal stem cells in a hepatoma model. Cell Res. 2008;18:500–7. · DOI
  34. Li Z, Tan F, Liewehr DJ, Steinberg SM, Thiele CJ. In vitro and in vivo inhibition of neuroblastoma tumor cell growth by AKT inhibitor perifosine. J Natl Cancer Inst. 2010;102:758–70. · DOI
  35. Ohlsson LB, Varas L, Kjellman C, Edvardsen K, Lindvall M. Mesenchymal progenitor cell-mediated inhibition of tumor growth in vivo and in vitro in gelatin matrix. Exp Mol Pathol. 2003;75:248–55. · DOI
  36. Kim J, Escalante LE, Dollar BA, Hanson SE, Hematti P. Сomparison of breast and abdominal adipose tissue mesenchymal stromal/stem cells in support of proliferation of breast cancer cells. Cancer Invest. 2013;31:550–4. · DOI
  37. Fierro FA, Sierralta WD, Epunan MJ, Minguell JJ. Marrow-derived mesenchymal stem cells: role in epithelial tumor cell determination metastasis. Clin Exp. 2004;21:313–9. · DOI
  38. Gauthaman K, Yee FC, Cheyyatraivendran S, Biswas A, Choolani M, Bongso A. Human umbilical cord Wharton's jelly stem cell (hWJSC) extracts inhibit cancer cell growth in vitro. J Cell Biochem. 2012;113:2027–39. · DOI
  39. Ono M, Kosaka N, Tominaga N, Yoshioka Y, Takeshita F, Takahashi RU, et al. Exosomes from bone marrow mesenchymal stem cells contain a microRNA that promotes dormancy in metastatic breast cancer cells. Sci Signal. 2014;7:ra63. · DOI
  40. Yang C, Lei D, Ouyang W, Ren J, Li H, Hu J, et al. Conditioned media from human adipose tissue-derived mesenchymal stem cells and umbilical cord-derived mesenchymal stem cells efficiently induced the apoptosis and differentiation in human glioma cell lines in vitro. Biomed Res Int. 2014;2014:109389. doi:10.1155/2014/109389. · DOI
  41. Abd-Allah SH, Shalaby SM, El-Shal AS, Elkader EA, Hussein S, Emam E, et al. Effect of bone marrow-derived mesenchymal stromal cells on hepatoma. Cytotherapy. 2014;16:1197–206. · DOI
  42. Takahara K, Ii M, Inamoto T, Komura K, Ibuki N, Minami K, et al. Adipose-derived stromal cells inhibit prostate cancer cell proliferation inducing apoptosis. Biochem Biophys Res Commun. 2014;446:1102–7. · DOI
  43. Jenkins DE, Hornig YS, Oei Y, Dusich J, Purchio T. Bioluminescent human breast cancer cell lines that permit rapid and sensitive in vivo detection of mammary tumors and multiple metastases in immune deficient mice. Breast Cancer Res. 2005;7:444–54. · DOI
  44. Kidd S, Spaeth E, Dembinski JL. Direct evidence of mesenchymal stem cell tropism for tumor and wounding microenvironments using in vivo bioluminescent imaging. Stem Cells. 2009;27:2614–23. · DOI

Cited by

Sorted by citations

Metadata

Authors
Meleshina, A. V., Cherkasova, E. I., Shirmanova, M. V., Klementieva, N. V., Kiseleva, E. V., Snopova, L. В., Prodanets, N. N., & Zagaynova, E. V.
Affiliations
Koltzov Institute of Developmental Biology (RU)
Corresponding author
Meleshina, Aleksandra V
ORCID
Venue
Stem Cell Research & Therapy
Publisher
Springer Science and Business Media LLC
Published
2015-02-27
Volume
6
Issue
1
Pages
15-15
ISSN
1757-6512 (ISSN-L)
DOI
10.1186/s13287-015-0003-7
PMC
PMC4415299
OpenAlex
W2093172278
Cited by
45
References
7
Citations by year
2025: 2 · 2024: 3 · 2023: 4 · 2022: 4 · 2021: 3 · 2020: 5 · 2019: 6 · 2018: 5 · 2017: 6 · 2016: 4 · 2015: 3
FWCI
3.36
Type
journal article
Language
en
Open access
Licence
Locations
  • Stem Cell Research & Therapy (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
  • Ministry of Education and Science of the Russian Federation (2014/134)
  • Russian Science Foundation (14-15-00536)
  • Medical School, University of Michigan
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Mesenchymal stem cell research
  • Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
  • Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
Keywords
mesenchymal stem cells, breast cancer metastasis, lung metastasis, MDA-MB-231 cells, MSC-conditioned medium, tumor cell proliferation, bioluminescence imaging, fluorescence imaging, bone marrow-derived stem cells
MeSH terms
Animals, Breast Neoplasms, Cell Transformation, Neoplastic, Disease Models, Animal, Female, Lung Neoplasms, Mice, Nude, Neoplasm Transplantation, Culture Media, Conditioned, Mesenchymal Stem Cell Transplantation, Cell Proliferation, Mice, Mesenchymal Stem Cells, Optical Imaging

About these checks

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

Statistics and arithmetic are recomputed, not judged.

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

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

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