Inhibition of human malignant pleural mesothelioma growth by mesenchymal stromal cells

V. Coccè; S. La Monica; M. Bonelli; G. Alessandri; R. Alfieri; C.A. Lagrasta; D. Madeddu; C. Frati; L. Flammini; D. Lisini; A. Marcianti; E. Parati; F. Paino; A. Giannì; G. Farronato; A. Falco; L. Spaggiari; F. Petrella; A. Pessina

doi:10.3390/cells10061427

Inhibition of human malignant pleural mesothelioma growth by mesenchymal stromal cells

V. Coccè, S. La Monica, M. Bonelli, G. Alessandri, R. Alfieri, C.A. Lagrasta, D. Madeddu, C. Frati, L. Flammini, D. Lisini, A. Marcianti, E. Parati, F. Paino, A. Giannì, G. Farronato, A. Falco, L. Spaggiari, F. Petrella, A. Pessina

Research output: Contribution to journal › Article › peer-review

Abstract

Background: Malignant Pleural Mesothelioma (MPM) is an aggressive tumor that has a significant incidence related to asbestos exposure with no effective therapy and poor prognosis. The role of mesenchymal stromal cells (MSCs) in cancer is controversial due to their opposite effects on tumor growth and in particular, only a few data are reported on MSCs and MPM. Methods: We investigated the in vitro efficacy of adipose tissue-derived MSCs, their lysates and secretome against different MPM cell lines. After large-scale production of MSCs in a bioreactor, their efficacy was also evaluated on a human MPM xenograft in mice. Results: MSCs, their lysate and secretome inhibited MPM cell proliferation in vitro with S or G0/G1 arrest of the cell cycle, respectively. MSC lysate induced cell death by apoptosis. The efficacy of MSC was confirmed in vivo by a significant inhibition of tumor growth, similar to that produced by systemic administration of paclitaxel. Interestingly, no tumor progression was observed after the last MSC treatment, while tumors started to grow again after stopping chemotherapeutic treatment. Conclusions: These data demonstrated for the first time that MSCs, both through paracrine and cell-to-cell interaction mechanisms, induced a significant inhibition of human mesothelioma growth. Since the prognosis for MPM patients is poor and the options of care are limited to chemotherapy, MSCs could provide a potential new therapeutic approach for this malignancy. © 2021 by the authors. Licensee MDPI, Basel, Switzerland.

Original language	English
Journal	Cells
Volume	10
Issue number	6
DOIs	https://doi.org/10.3390/cells10061427
Publication status	Published - 2021

Keywords

Cell therapy
Malignant pleural mesothelioma (MPM)
Mesenchymal stromal cells
Mesothelioma
caspase 3
caspase 9
CD146 antigen
CD34 antigen
doxorubicin
fibroblast growth factor
fibronectin
fluorouracil
gamma interferon
gemcitabine
hydrogel
interleukin 10
interleukin 1beta
interleukin 6
oxaliplatin
paclitaxel
phosphatidylserine
platelet endothelial cell adhesion molecule 1
protein Bax
Thy 1 membrane glycoprotein
tubulin
tumor necrosis factor
vasculotropin
adipose tissue
ADSC cell line
animal cell
animal experiment
animal model
antineoplastic activity
antiproliferative activity
apoptosis
Article
cancer chemotherapy
cancer growth
cancer inhibition
cancer prognosis
cancer therapy
cell cycle arrest
cell death
cell lysate
cell proliferation
cell viability
clinical article
controlled study
cytokine production
dendritic cell
female
flow cytometry
fluorescence microscopy
histology
human
human cell
immunofluorescence
immunohistochemistry
in vitro study
in vivo study
mesenchymal stroma cell
mesothelioma cell line
mouse
MTT assay
nonhuman
pleura mesothelioma
secretomics
T lymphocyte
transwell assay
tumor growth
tumor microenvironment
tumor xenograft

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10.3390/cells10061427

https://www.scopus.com/inward/record.uri?eid=2-s2.0-85110337877&doi=10.3390%2fcells10061427&partnerID=40&md5=928aa20d15bd411cd79b7725eae7f8a9

Cite this

Coccè, V., La Monica, S., Bonelli, M., Alessandri, G., Alfieri, R., Lagrasta, C. A., Madeddu, D., Frati, C., Flammini, L., Lisini, D., Marcianti, A., Parati, E., Paino, F., Giannì, A., Farronato, G., Falco, A., Spaggiari, L., Petrella, F., & Pessina, A. (2021). Inhibition of human malignant pleural mesothelioma growth by mesenchymal stromal cells. Cells, 10(6). https://doi.org/10.3390/cells10061427

Coccè, V, La Monica, S, Bonelli, M, Alessandri, G, Alfieri, R, Lagrasta, CA, Madeddu, D, Frati, C, Flammini, L, Lisini, D, Marcianti, A, Parati, E, Paino, F, Giannì, A, Farronato, G, Falco, A, Spaggiari, L , Petrella, F & Pessina, A 2021, 'Inhibition of human malignant pleural mesothelioma growth by mesenchymal stromal cells', Cells, vol. 10, no. 6. https://doi.org/10.3390/cells10061427

@article{864df95680d2407b8a0e39688c00cab7,

title = "Inhibition of human malignant pleural mesothelioma growth by mesenchymal stromal cells",

abstract = "Background: Malignant Pleural Mesothelioma (MPM) is an aggressive tumor that has a significant incidence related to asbestos exposure with no effective therapy and poor prognosis. The role of mesenchymal stromal cells (MSCs) in cancer is controversial due to their opposite effects on tumor growth and in particular, only a few data are reported on MSCs and MPM. Methods: We investigated the in vitro efficacy of adipose tissue-derived MSCs, their lysates and secretome against different MPM cell lines. After large-scale production of MSCs in a bioreactor, their efficacy was also evaluated on a human MPM xenograft in mice. Results: MSCs, their lysate and secretome inhibited MPM cell proliferation in vitro with S or G0/G1 arrest of the cell cycle, respectively. MSC lysate induced cell death by apoptosis. The efficacy of MSC was confirmed in vivo by a significant inhibition of tumor growth, similar to that produced by systemic administration of paclitaxel. Interestingly, no tumor progression was observed after the last MSC treatment, while tumors started to grow again after stopping chemotherapeutic treatment. Conclusions: These data demonstrated for the first time that MSCs, both through paracrine and cell-to-cell interaction mechanisms, induced a significant inhibition of human mesothelioma growth. Since the prognosis for MPM patients is poor and the options of care are limited to chemotherapy, MSCs could provide a potential new therapeutic approach for this malignancy. {\textcopyright} 2021 by the authors. Licensee MDPI, Basel, Switzerland.",

keywords = "Cell therapy, Malignant pleural mesothelioma (MPM), Mesenchymal stromal cells, Mesothelioma, caspase 3, caspase 9, CD146 antigen, CD34 antigen, doxorubicin, fibroblast growth factor, fibronectin, fluorouracil, gamma interferon, gemcitabine, hydrogel, interleukin 10, interleukin 1beta, interleukin 6, oxaliplatin, paclitaxel, phosphatidylserine, platelet endothelial cell adhesion molecule 1, protein Bax, Thy 1 membrane glycoprotein, tubulin, tumor necrosis factor, vasculotropin, adipose tissue, ADSC cell line, animal cell, animal experiment, animal model, antineoplastic activity, antiproliferative activity, apoptosis, Article, cancer chemotherapy, cancer growth, cancer inhibition, cancer prognosis, cancer therapy, cell cycle arrest, cell death, cell lysate, cell proliferation, cell viability, clinical article, controlled study, cytokine production, dendritic cell, female, flow cytometry, fluorescence microscopy, histology, human, human cell, immunofluorescence, immunohistochemistry, in vitro study, in vivo study, mesenchymal stroma cell, mesothelioma cell line, mouse, MTT assay, nonhuman, pleura mesothelioma, secretomics, T lymphocyte, transwell assay, tumor growth, tumor microenvironment, tumor xenograft",

author = "V. Cocc{\`e} and {La Monica}, S. and M. Bonelli and G. Alessandri and R. Alfieri and C.A. Lagrasta and D. Madeddu and C. Frati and L. Flammini and D. Lisini and A. Marcianti and E. Parati and F. Paino and A. Giann{\`i} and G. Farronato and A. Falco and L. Spaggiari and F. Petrella and A. Pessina",

note = "Cited By :1 Export Date: 15 October 2021 Correspondence Address: La Monica, S.; Department of Medicine and Surgery, Italy; email: silvia.lamonica@unipr.it Chemicals/CAS: caspase 3, 169592-56-7; caspase 9, 180189-96-2; doxorubicin, 23214-92-8, 25316-40-9; fibroblast growth factor, 62031-54-3; fibronectin, 86088-83-7; fluorouracil, 51-21-8; gamma interferon, 82115-62-6; gemcitabine, 103882-84-4; oxaliplatin, 61825-94-3; paclitaxel, 33069-62-4; vasculotropin, 127464-60-2 Manufacturers: Labsonic UBraun, Germany; Euroclone, Italy; Becton Dickinson, United States; Dow, United StatesSarstedt, Germany; Abcam, United Kingdom; Biorad, United States; Terumo BCT, United States References: Carbone, M., Ly, B.H., Dodson, R.F., Pagano, I., Morris, P.T., Dogan, U.A., Gazdar, A.F., Yang, H., Malignant mesothelioma: Facts, myths, and hypotheses (2012) J. Cell Physiol, 227, pp. 44-58. , [CrossRef] [PubMed]; Peto, J., Decarli, A., La Vecchia, C., Levi, F., Negri, E., The European mesothelioma epidemic (1999) Br. J. Cancer, 79, pp. 666-672. , [CrossRef] [PubMed]; Fennell, D.A., Gaudino, G., O{\textquoteright}Byrne, K.J., Mutti, L., van Meerbeeck, J., Advances in the systemic therapy of malignant pleural mesothelioma (2008) Nat. Clin. Pract. Oncol, 5, pp. 136-147. , [CrossRef]; Krug, L.M., Pass, H.I., Rusch, V.W., Kindler, H.L., Sugarbaker, D.J., Rosenzweig, K.E., Flores, R., Monberg, M., Multicenter phase II trial of neoadjuvant pemetrexed plus cisplatin followed by extrapleural pneumonectomy and radiation for malignant pleural mesothelioma (2009) J. Clin. Oncol, 27, pp. 3007-3013. , [CrossRef]; Mutti, L., Peikert, T., Robinson, B.W.S., Scherpereel, A., Tsao, A.S., de Perrot, M., Woodard, G.A., Hirsch, F.R., Scientific Advances and New Frontiers in Mesothelioma Therapeutics (2018) J. Thorac. Oncol, 13, pp. 1269-1283. , [CrossRef] [PubMed]; Li, W., Zhou, Y., Yang, J., Zhang, X., Zhang, H., Zhang, T., Zhao, S., Wu, H., Gastric cancer-derived mesenchymal stem cells prompt gastric cancer progression through secretion of interleukin-8 (2015) J. Exp. Clin. Cancer Res, 34, p. 52. , [CrossRef]; Li, G.C., Zhang, H.W., Zhao, Q.C., Sun, L.I., Yang, J.J., Hong, L., Feng, F., Cai, L., Mesenchymal stem cells promote tumor angiogenesis via the action of transforming growth factor β1 (2016) Oncol. Lett, 11, pp. 1089-1094. , [CrossRef] [PubMed]; Houthuijzen, J.M., Daenen, L.G., Roodhart, J.M., Voest, E.E., The role of mesenchymal stem cells in anti-cancer drug resistance and tumour progression (2012) Br. J. Cancer, 106, pp. 1901-1906. , [CrossRef]; Ramasamy, R., Lam, E.W., Soeiro, I., Tisato, V., Bonnet, D., Dazzi, F., Mesenchymal stem cells inhibit proliferation and apoptosis of tumor cells: Impact on in vivo tumor growth (2007) Leukemia, 21, pp. 304-310. , [CrossRef]; Chanda, D., Isayeva, T., Kumar, S., Hensel, J.A., Sawant, A., Ramaswamy, G., Siegal, G.P., Ponnazhagan, S., Therapeutic potential of adult bone marrow-derived mesenchymal stem cells in prostate cancer bone metastasis (2009) Clin. Cancer Res, 15, pp. 7175-7185. , [CrossRef]; Ohlsson, L.B., Varas, L., Kjellman, C., Edvardsen, K., Lindvall, M., Mesenchymal progenitor cell-mediated inhibition of tumor growth in vivo and in vitro in gelatin matrix (2003) Exp. Mol. Pathol, 75, pp. 248-255. , [CrossRef]; Ayuzawa, R., Doi, C., Rachakatla, R.S., Pyle, M.M., Maurya, D.K., Troyer, D., Tamura, M., Na{\"i}ve human umbilical cord matrix derived stem cells significantly attenuate growth of human breast cancer cells in vitro and in vivo (2009) Cancer Lett, 280, pp. 31-37. , [CrossRef]; Yuan, Z., Kolluri, K.K., Gowers, K.H., Janes, S.M., TRAIL delivery by MSC-derived extracellular vesicles is an effective anticancer therapy (2017) J. Extracell. Vesicles, 6, p. 1265291. , [CrossRef]; Li, L., Tian, H., Chen, Z., Yue, W., Li, S., Li, W., Inhibition of lung cancer cell proliferation mediated by human mesenchymal stem cells (2011) Acta Biochim. Biophys. Sin. (Shanghai), 43, pp. 143-148. , [CrossRef] [PubMed]; Ramdasi, S., Sarang, S., Viswanathan, C., Potential of Mesenchymal Stem Cell based application in Cancer (2015) Int. J. Hematol. Oncol. Stem Cell Res, 9, pp. 95-103; Galland, S., Stamenkovic, I., Mesenchymal stromal cells in cancer: A review of their immunomodulatory functions and dual effects on tumor progression (2020) J. Pathol, 250, pp. 555-572. , [CrossRef]; Hmadcha, A., Martin-Montalvo, A., Gauthier, B.R., Soria, B., Capilla-Gonzalez, V., Therapeutic Potential of Mesenchymal Stem Cells for Cancer Therapy (2020) Front. Bioeng. Biotechnol, 8, p. 43. , [CrossRef] [PubMed]; Nwabo Kamdje, A.H., Kamga, P.T., Simo, R.T., Vecchio, L., Seke Etet, P.F., Muller, J.M., Bassi, G., Amvene, J.M., Mesenchymal stromal cells{\textquoteright} role in tumor microenvironment: Involvement of signaling pathways (2017) Cancer Biol. Med, 14, pp. 129-141. , [CrossRef]; Cortes-Dericks, L., Froment, L., Kocher, G., Schmid, R.A., Human lung-derived mesenchymal stem cell-conditioned medium exerts in vitro antitumor effects in malignant pleural mesothelioma cell lines (2016) Stem Cell Res. 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year = "2021",

doi = "10.3390/cells10061427",

language = "English",

volume = "10",

journal = "Cells",

issn = "2073-4409",

publisher = "MDPI AG",

number = "6",

}

TY - JOUR

T1 - Inhibition of human malignant pleural mesothelioma growth by mesenchymal stromal cells

AU - Coccè, V.

AU - La Monica, S.

AU - Bonelli, M.

AU - Alessandri, G.

AU - Alfieri, R.

AU - Lagrasta, C.A.

AU - Madeddu, D.

AU - Frati, C.

AU - Flammini, L.

AU - Lisini, D.

AU - Marcianti, A.

AU - Parati, E.

AU - Paino, F.

AU - Giannì, A.

AU - Farronato, G.

AU - Falco, A.

AU - Spaggiari, L.

AU - Petrella, F.

AU - Pessina, A.

N1 - Cited By :1 Export Date: 15 October 2021 Correspondence Address: La Monica, S.; Department of Medicine and Surgery, Italy; email: silvia.lamonica@unipr.it Chemicals/CAS: caspase 3, 169592-56-7; caspase 9, 180189-96-2; doxorubicin, 23214-92-8, 25316-40-9; fibroblast growth factor, 62031-54-3; fibronectin, 86088-83-7; fluorouracil, 51-21-8; gamma interferon, 82115-62-6; gemcitabine, 103882-84-4; oxaliplatin, 61825-94-3; paclitaxel, 33069-62-4; vasculotropin, 127464-60-2 Manufacturers: Labsonic UBraun, Germany; Euroclone, Italy; Becton Dickinson, United States; Dow, United StatesSarstedt, Germany; Abcam, United Kingdom; Biorad, United States; Terumo BCT, United States References: Carbone, M., Ly, B.H., Dodson, R.F., Pagano, I., Morris, P.T., Dogan, U.A., Gazdar, A.F., Yang, H., Malignant mesothelioma: Facts, myths, and hypotheses (2012) J. Cell Physiol, 227, pp. 44-58. , [CrossRef] [PubMed]; Peto, J., Decarli, A., La Vecchia, C., Levi, F., Negri, E., The European mesothelioma epidemic (1999) Br. J. Cancer, 79, pp. 666-672. , [CrossRef] [PubMed]; Fennell, D.A., Gaudino, G., O’Byrne, K.J., Mutti, L., van Meerbeeck, J., Advances in the systemic therapy of malignant pleural mesothelioma (2008) Nat. Clin. Pract. Oncol, 5, pp. 136-147. , [CrossRef]; Krug, L.M., Pass, H.I., Rusch, V.W., Kindler, H.L., Sugarbaker, D.J., Rosenzweig, K.E., Flores, R., Monberg, M., Multicenter phase II trial of neoadjuvant pemetrexed plus cisplatin followed by extrapleural pneumonectomy and radiation for malignant pleural mesothelioma (2009) J. Clin. Oncol, 27, pp. 3007-3013. , [CrossRef]; Mutti, L., Peikert, T., Robinson, B.W.S., Scherpereel, A., Tsao, A.S., de Perrot, M., Woodard, G.A., Hirsch, F.R., Scientific Advances and New Frontiers in Mesothelioma Therapeutics (2018) J. Thorac. Oncol, 13, pp. 1269-1283. , [CrossRef] [PubMed]; Li, W., Zhou, Y., Yang, J., Zhang, X., Zhang, H., Zhang, T., Zhao, S., Wu, H., Gastric cancer-derived mesenchymal stem cells prompt gastric cancer progression through secretion of interleukin-8 (2015) J. Exp. Clin. Cancer Res, 34, p. 52. , [CrossRef]; Li, G.C., Zhang, H.W., Zhao, Q.C., Sun, L.I., Yang, J.J., Hong, L., Feng, F., Cai, L., Mesenchymal stem cells promote tumor angiogenesis via the action of transforming growth factor β1 (2016) Oncol. Lett, 11, pp. 1089-1094. , [CrossRef] [PubMed]; Houthuijzen, J.M., Daenen, L.G., Roodhart, J.M., Voest, E.E., The role of mesenchymal stem cells in anti-cancer drug resistance and tumour progression (2012) Br. J. Cancer, 106, pp. 1901-1906. , [CrossRef]; Ramasamy, R., Lam, E.W., Soeiro, I., Tisato, V., Bonnet, D., Dazzi, F., Mesenchymal stem cells inhibit proliferation and apoptosis of tumor cells: Impact on in vivo tumor growth (2007) Leukemia, 21, pp. 304-310. , [CrossRef]; Chanda, D., Isayeva, T., Kumar, S., Hensel, J.A., Sawant, A., Ramaswamy, G., Siegal, G.P., Ponnazhagan, S., Therapeutic potential of adult bone marrow-derived mesenchymal stem cells in prostate cancer bone metastasis (2009) Clin. Cancer Res, 15, pp. 7175-7185. , [CrossRef]; Ohlsson, L.B., Varas, L., Kjellman, C., Edvardsen, K., Lindvall, M., Mesenchymal progenitor cell-mediated inhibition of tumor growth in vivo and in vitro in gelatin matrix (2003) Exp. Mol. Pathol, 75, pp. 248-255. , [CrossRef]; Ayuzawa, R., Doi, C., Rachakatla, R.S., Pyle, M.M., Maurya, D.K., Troyer, D., Tamura, M., Naïve human umbilical cord matrix derived stem cells significantly attenuate growth of human breast cancer cells in vitro and in vivo (2009) Cancer Lett, 280, pp. 31-37. , [CrossRef]; Yuan, Z., Kolluri, K.K., Gowers, K.H., Janes, S.M., TRAIL delivery by MSC-derived extracellular vesicles is an effective anticancer therapy (2017) J. Extracell. Vesicles, 6, p. 1265291. , [CrossRef]; Li, L., Tian, H., Chen, Z., Yue, W., Li, S., Li, W., Inhibition of lung cancer cell proliferation mediated by human mesenchymal stem cells (2011) Acta Biochim. Biophys. Sin. (Shanghai), 43, pp. 143-148. , [CrossRef] [PubMed]; Ramdasi, S., Sarang, S., Viswanathan, C., Potential of Mesenchymal Stem Cell based application in Cancer (2015) Int. J. Hematol. Oncol. Stem Cell Res, 9, pp. 95-103; Galland, S., Stamenkovic, I., Mesenchymal stromal cells in cancer: A review of their immunomodulatory functions and dual effects on tumor progression (2020) J. Pathol, 250, pp. 555-572. , [CrossRef]; Hmadcha, A., Martin-Montalvo, A., Gauthier, B.R., Soria, B., Capilla-Gonzalez, V., Therapeutic Potential of Mesenchymal Stem Cells for Cancer Therapy (2020) Front. Bioeng. Biotechnol, 8, p. 43. , [CrossRef] [PubMed]; Nwabo Kamdje, A.H., Kamga, P.T., Simo, R.T., Vecchio, L., Seke Etet, P.F., Muller, J.M., Bassi, G., Amvene, J.M., Mesenchymal stromal cells’ role in tumor microenvironment: Involvement of signaling pathways (2017) Cancer Biol. Med, 14, pp. 129-141. , [CrossRef]; Cortes-Dericks, L., Froment, L., Kocher, G., Schmid, R.A., Human lung-derived mesenchymal stem cell-conditioned medium exerts in vitro antitumor effects in malignant pleural mesothelioma cell lines (2016) Stem Cell Res. 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PY - 2021

Y1 - 2021

N2 - Background: Malignant Pleural Mesothelioma (MPM) is an aggressive tumor that has a significant incidence related to asbestos exposure with no effective therapy and poor prognosis. The role of mesenchymal stromal cells (MSCs) in cancer is controversial due to their opposite effects on tumor growth and in particular, only a few data are reported on MSCs and MPM. Methods: We investigated the in vitro efficacy of adipose tissue-derived MSCs, their lysates and secretome against different MPM cell lines. After large-scale production of MSCs in a bioreactor, their efficacy was also evaluated on a human MPM xenograft in mice. Results: MSCs, their lysate and secretome inhibited MPM cell proliferation in vitro with S or G0/G1 arrest of the cell cycle, respectively. MSC lysate induced cell death by apoptosis. The efficacy of MSC was confirmed in vivo by a significant inhibition of tumor growth, similar to that produced by systemic administration of paclitaxel. Interestingly, no tumor progression was observed after the last MSC treatment, while tumors started to grow again after stopping chemotherapeutic treatment. Conclusions: These data demonstrated for the first time that MSCs, both through paracrine and cell-to-cell interaction mechanisms, induced a significant inhibition of human mesothelioma growth. Since the prognosis for MPM patients is poor and the options of care are limited to chemotherapy, MSCs could provide a potential new therapeutic approach for this malignancy. © 2021 by the authors. Licensee MDPI, Basel, Switzerland.

AB - Background: Malignant Pleural Mesothelioma (MPM) is an aggressive tumor that has a significant incidence related to asbestos exposure with no effective therapy and poor prognosis. The role of mesenchymal stromal cells (MSCs) in cancer is controversial due to their opposite effects on tumor growth and in particular, only a few data are reported on MSCs and MPM. Methods: We investigated the in vitro efficacy of adipose tissue-derived MSCs, their lysates and secretome against different MPM cell lines. After large-scale production of MSCs in a bioreactor, their efficacy was also evaluated on a human MPM xenograft in mice. Results: MSCs, their lysate and secretome inhibited MPM cell proliferation in vitro with S or G0/G1 arrest of the cell cycle, respectively. MSC lysate induced cell death by apoptosis. The efficacy of MSC was confirmed in vivo by a significant inhibition of tumor growth, similar to that produced by systemic administration of paclitaxel. Interestingly, no tumor progression was observed after the last MSC treatment, while tumors started to grow again after stopping chemotherapeutic treatment. Conclusions: These data demonstrated for the first time that MSCs, both through paracrine and cell-to-cell interaction mechanisms, induced a significant inhibition of human mesothelioma growth. Since the prognosis for MPM patients is poor and the options of care are limited to chemotherapy, MSCs could provide a potential new therapeutic approach for this malignancy. © 2021 by the authors. Licensee MDPI, Basel, Switzerland.

KW - Cell therapy

KW - Malignant pleural mesothelioma (MPM)

KW - Mesenchymal stromal cells

KW - Mesothelioma

KW - caspase 3

KW - caspase 9

KW - CD146 antigen

KW - CD34 antigen

KW - doxorubicin

KW - fibroblast growth factor

KW - fibronectin

KW - fluorouracil

KW - gamma interferon

KW - gemcitabine

KW - hydrogel

KW - interleukin 10

KW - interleukin 1beta

KW - interleukin 6

KW - oxaliplatin

KW - paclitaxel

KW - phosphatidylserine

KW - platelet endothelial cell adhesion molecule 1

KW - protein Bax

KW - Thy 1 membrane glycoprotein

KW - tubulin

KW - tumor necrosis factor

KW - vasculotropin

KW - adipose tissue

KW - ADSC cell line

KW - animal cell

KW - animal experiment

KW - animal model

KW - antineoplastic activity

KW - antiproliferative activity

KW - apoptosis

KW - Article

KW - cancer chemotherapy

KW - cancer growth

KW - cancer inhibition

KW - cancer prognosis

KW - cancer therapy

KW - cell cycle arrest

KW - cell death

KW - cell lysate

KW - cell proliferation

KW - cell viability

KW - clinical article

KW - controlled study

KW - cytokine production

KW - dendritic cell

KW - female

KW - flow cytometry

KW - fluorescence microscopy

KW - histology

KW - human

KW - human cell

KW - immunofluorescence

KW - immunohistochemistry

KW - in vitro study

KW - in vivo study

KW - mesenchymal stroma cell

KW - mesothelioma cell line

KW - mouse

KW - MTT assay

KW - nonhuman

KW - pleura mesothelioma

KW - secretomics

KW - T lymphocyte

KW - transwell assay

KW - tumor growth

KW - tumor microenvironment

KW - tumor xenograft

U2 - 10.3390/cells10061427

DO - 10.3390/cells10061427

M3 - Article

SN - 2073-4409

VL - 10

JO - Cells

JF - Cells

IS - 6

ER -

Inhibition of human malignant pleural mesothelioma growth by mesenchymal stromal cells

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