Tumor necrosis factor-α-activated mesenchymal stem cells promote endothelial progenitor cell homing and angiogenesis

Kwon, Yang Woo; Heo, Soon Chul; Jeong, Geun Ok; Yoon, Jung Won; Mo, Won Min; Lee, Mi Jeong; Jang, Il-Ho; Kwon, Sang Mo; Lee, Jung Sub; Kim, Jae Ho

doi:10.1016/j.bbadis.2013.08.002

Cited by 137Mesenchymal stem cell researchAngiogenesis and VEGF in CancerWound Healing and Treatments

Tumor necrosis factor-α-activated mesenchymal stem cells promote endothelial progenitor cell homing and angiogenesis

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Kwon, Yang Woo, Heo, Soon Chul, Jeong, Geun Ok, Yoon, Jung Won, Mo, Won Min, Lee, Mi Jeong, Jang, Il-Ho, Kwon, Sang Mo +2 more·2013·Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease

DOI 10.1016/j.bbadis.2013.08.002

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Abstract

Mesenchymal stem cells (MSCs) accelerate regeneration of ischemic or injured tissues by stimulation of angiogenesis through a paracrine mechanism. Tumor necrosis factor-α (TNF-α)-activated MSCs secrete pro-angiogenic cytokines, including IL-6 and IL-8. In the present study, using an ischemic hindlimb animal model, we explored the role of IL-6 and IL-8 in the paracrine stimulation of angiogenesis and tissue regeneration by TNF-α-activated MSCs. Intramuscular injection of conditioned medium derived from TNF-α-treated MSCs (TNF-α CM) into the ischemic hindlimb resulted in attenuated severe limb loss and stimulated blood perfusion and angiogenesis in the ischemic limb. Immunodepletion of IL-6 and IL-8 resulted in attenuated TNF-α CM-stimulated tissue repair, blood perfusion, and angiogenesis. In addition, TNF-α CM induced migration of human cord blood-derived endothelial progenitor cells (EPCs) through IL-6- and IL-8-dependent mechanisms in vitro. Intramuscular injection of TNF-α CM into the ischemic limb led to augmented homing of tail vein-injected EPCs into the ischemic limb in vivo and immunodepletion of IL-6 or IL-8 from TNF-α CM attenuated TNF-α CM-stimulated homing of EPCs. In addition, intramuscular injection of recombinant IL-6 and IL-8 proteins resulted in increased homing of intravenously transplanted EPCs into the ischemic limb and improved blood perfusion in vivo. These results suggest that TNF-α CM stimulates angiogenesis and tissue repair through an increase in homing of EPCs through paracrine mechanisms involving IL-6 and IL-8.

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Several cytokines produced by inflammatory cells, including TNF, IL-6, and IL-8, have angiogenic effects.
“Additionally, several cytokines produced by inflammatory cells have angiogenic effects, including TNF, IL-6, and IL-8 (57, 58).”
From The ominous triad of adipose tissue dysfunction: inflammation, fibrosis, and impaired angiogenesis. (2017) · cites this paper as [57]

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A Comparison of Phenotypic and Functional Properties of Mesenchymal Stromal Cells and Multipotent Adult Progenitor Cells
Khan, R. S., & Newsome, P. N. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01952 · Cited by 55 · see citing works
Persistent Inflammatory Stimulation Drives the Conversion of MSCs to Inflammatory CAFs That Promote Pro-Metastatic Characteristics in Breast Cancer Cells
Rubinstein-Achiasaf, L., Morein, D., Ben-Yaakov, H., Liubomirski, Y., Meshel, T., Elbaz, E., Dorot, O., Pichinuk, E., Gershovits, M., Weil, M., et al. (2021) · Cancers · doi:10.3390/cancers13061472 · Cited by 53 · see citing works
Human Umbilical Cord-Derived Mesenchymal Stem Cells Improve Learning and Memory Function in Hypoxic-Ischemic Brain-Damaged Rats via an IL-8-Mediated Secretion Mechanism Rather than Differentiation Pattern Induction
Zhou, X., Gu, J., Gu, Y., He, M., Bi, Y., Chen, J., & Li, T. (2015) · Cellular Physiology and Biochemistry · doi:10.1159/000374040 · Cited by 52 · see citing works
TNF ‐α promotes survival and migration of MSC s under oxidative stress via NF ‐κB pathway to attenuate intimal hyperplasia in vein grafts
Bai, X., Xi, J., Bi, Y., Zhao, X., Bing, W., Meng, X., Liu, Y., Zhu, Z., & Song, G. (2017) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.13131 · Cited by 50 · see citing works
“promote homing of endothelial progenitor cells and angiogenesis [45].”
Background
Disease-specific primed human adult stem cells effectively ameliorate experimental atopic dermatitis in mice
Lee, B., Kim, J.-J., Lee, J. Y., Kang, I., Shin, N., Lee, S., Choi, S. W., Cho, J., Kim, H., & Kang, K. (2019) · Theranostics · doi:10.7150/thno.32945 · Cited by 50 · see citing works
“Recent studies have suggested various enhancement strategies for stem cell therapy, including preconditioning with disease-related factors, such as TNF-α and IFN-γ [7, 22-24].”
Background
Mesenchymal stem cells for critical limb ischemia: their function, mechanism, and therapeutic potential
Navarro, L., Chen, X., Viviescas, L. T. G., Ardila-Roa, A. K., Luna-González, M., Sossa, C., & Arango-Rodríguez, M. L. (2022) · Stem Cell Research & Therapy · doi:10.1186/s13287-022-03043-3 · Cited by 49 · see citing works
Endothelial progenitor cells and revascularization following stroke
Ma, F., Morancho, A., Montaner, J., & Rosell, A. (2015) · Brain Research · doi:10.1016/j.brainres.2015.02.010 · Cited by 49 · see citing works
Encapsulated human mesenchymal stem cells (eMSCs) as a novel anti-cancer agent targeting breast cancer stem cells: Development of 3D primed therapeutic MSCs
Mandal, S., Arfuso, F., Sethi, G., Dharmarajan, A., & Warrier, S. R. (2019) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2019.02.001 · Cited by 49 · see citing works
Transcriptome sequencing wide functional analysis of human mesenchymal stem cells in response to TLR4 ligand
Kim, S. H., Das, A., Chai, J. C., Binas, B., Choi, M., Park, K. S., Lee, Y. S., Jung, K. H., & Chai, Y. G. (2016) · Scientific Reports · doi:10.1038/srep30311 · Cited by 48 · see citing works
Periostin Accelerates Bone Healing Mediated by Human Mesenchymal Stem Cell-Embedded Hydroxyapatite/Tricalcium Phosphate Scaffold
Heo, S. C., Shin, W. C., Lee, M. J., Kim, B. R., Jang, I. H., Choi, E., Lee, J. S., & Kim, J. H. (2015) · PLoS ONE · doi:10.1371/journal.pone.0116698 · Cited by 44 · see citing works
“hASCs have been reported to promote tissue repair by stimulating angiogenesis through a paracrine mechanism [42, 43].”
Background
Synergistic protein secretion by mesenchymal stromal cells seeded in 3D scaffolds and circulating leukocytes in physiological flow
Ballotta, V., Smits, A. I. P. M., Driessen‐Mol, A., Bouten, C. V. C., & Baaijens, F. F. (2014) · Biomaterials · doi:10.1016/j.biomaterials.2014.07.042 · Cited by 43 · see citing works
“Substantial production of IL-6 and IL-8 was suggested to induce BMSC, previously exposed to TNFa, to stimulate angiogenesis and tissue repair through increased homing of endothelial progenitor cells [37].”
Background
Bone Marrow-Derived Mesenchymal Stem Cells Drive Lymphangiogenesis
Maertens, L., Erpicum, C., Detry, B., Blacher, S., Lenoir, B., Carnet, O., Péqueux, C., Cataldo, D. D., Lecomte, J., Paupert, J., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0106976 · Cited by 41 · see citing works
Isolation, Characterization, Differentiation and Immunomodulatory Capacity of Mesenchymal Stromal/Stem Cells from Human Perirenal Adipose Tissue
Baer, P. C., Koch, B., Hickmann, E., Schubert, R., Cinatl, J. J., Hauser, I. A., & Geiger, H. (2019) · Cells · doi:10.3390/cells8111346 · Cited by 41 · see citing works
“The ASCs incubated with TNFα increased the secretion of IL-6 and IL-8, resulting in promoting endothelial progenitor cell homing and stimulating angiogenesis in an ischemic hindlimb model [40].”
Background
Pretreatment of Mesenchymal Stem Cells Manipulates Their Vasculoprotective Potential While Not Altering Their Homing Within the Injured Gut
Kavanagh, D. P. J., Suresh, S., Newsome, P. N., Frampton, J., & Kalia, N. (2015) · Stem Cells · doi:10.1002/stem.2061 · Cited by 40 · see citing works
Improving the therapeutic efficacy of mesenchymal stromal cells to restore perfusion in critical limb ischemia through pulsed focused ultrasound
Tebebi, P. A., Kim, S. J., Williams, R. A., Milo, B., Frenkel, V., Burks, S. R., & Frank, J. A. (2017) · Scientific Reports · doi:10.1038/srep41550 · Cited by 39 · see citing works
Human mesenchymal stromal cells and derived extracellular vesicles: Translational strategies to increase their proangiogenic potential for the treatment of cardiovascular disease
Nazari‐Shafti, T. Z., Neuber, S., Duran, A. G., Xu, Z.-Y., Beltsios, E. T., Seifert, M., Falk, V., & Stamm, C. (2020) · Stem Cells Translational Medicine · doi:10.1002/sctm.19-0432 · Cited by 39 · see citing works
“in inducing angiogenesis and improving oxygen supply to ischemic tissues.(58,59) In addition, it has been shown that MSCs, when cultured on”
Background
Enhancement of the efficacy of mesenchymal stem cells in the treatment of ischemic diseases
Luo, R., Lu, Y., Liu, J., Cheng, J., & Chen, Y. (2018) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2018.11.068 · Cited by 36 · see citing works
Biomaterials-Based Strategies to Enhance Angiogenesis in Diabetic Wound Healing
Pal, D., Das, P., Mukherjee, P., Roy, S., Chaudhuri, S., Kesh, S. S., Ghosh, D., & Nandi, S. K. (2024) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.4c00216 · Cited by 37 · see citing works
Can Mesenchymal Stem Cells Act Multipotential in Traumatic Brain Injury?
Dehghanian, F., Soltani, Z., & Khaksari, M. (2020) · Journal of Molecular Neuroscience · doi:10.1007/s12031-019-01475-w · Cited by 37 · see citing works
“2013) are main reasons for using SCs in TBI treatment trials (Kwon et al. 2013).”
Background
Single-cell transcriptomic profiling and characterization of endothelial progenitor cells: new approach for finding novel markers
Abdelgawad, M. E., Desterke, C., Uzan, G., & Naserian, S. (2021) · Stem Cell Research & Therapy · doi:10.1186/s13287-021-02185-0 · Cited by 34 · see citing works
Equilibrium among Inflammatory Factors Determines Human MSC-Mediated Immunosuppressive Effect
Suzdaltseva, Y. G., Goryunov, K. V., Silina, E. V., Manturova, N., Stupin, V. A., & Киселев, С. Л. (2022) · Cells · doi:10.3390/cells11071210 · Cited by 35 · see citing works
Nanospheres Loaded with Curcumin Improve the Bioactivity of Umbilical Cord Blood-Mesenchymal Stem Cells via c-Src Activation during the Skin Wound Healing Process
Kim, D. W., Choi, C., Park, J. P., & Lee, S. (2020) · Cells · doi:10.3390/cells9061467 · Cited by 33 · see citing works
“These results are consistent with the notion that MSCs treated with TNF-α stimulate the tissue regeneration process through paracrine mechanisms [66].”
Human Bone Marrow-Derived Mesenchymal Stem Cells Home via the PI3K-Akt, MAPK, and Jak/Stat Signaling Pathways in Response to Platelet-Derived Growth Factor
Popielarczyk, T. L., Huckle, W. R., & Barrett, J. G. (2019) · Stem Cells and Development · doi:10.1089/scd.2019.0003 · Cited by 32 · see citing works
Mapping the Secretome of Dental Pulp Stem Cells Under Variable Microenvironmental Conditions
Bousnaki, M., Bakopoulou, A., Pich, A., Papachristou, E., Κritis, A., & Koidis, P. T. (2021) · Stem Cell Reviews and Reports · doi:10.1007/s12015-021-10255-2 · Cited by 32 · see citing works
“DPSCs were analyzed by flow cytometry for mesenchymal (CD90/Thy-1, CD146, STRO-1, CD73), endothelial (CD105/endoglin), embryonic (SSEA-4) and hematopoietic (CD34, CD45) stem cell (SC) markers, as previously described [27].”
BackgroundMethodResultInfluential
Extracellular Vesicles and Alveolar Epithelial-Capillary Barrier Disruption in Acute Respiratory Distress Syndrome: Pathophysiological Role and Therapeutic Potential
Esquivel‐Ruiz, S., González‐Rodríguez, P., Lorente, J. A., Pérez‐Vizcaíno, F., Herrero, R., & Moreno, L. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.752287 · Cited by 32 · see citing works
Coadministration of endothelial and smooth muscle cells derived from human induced pluripotent stem cells as a therapy for critical limb ischemia
Park, J. J., Kwon, Y. W., Kim, J. W., Park, G. T., Yoon, J. W., Kim, Y. S., Kim, D. S., Kwon, S., Bae, S. S., Ko, K., et al. (2020) · Stem Cells Translational Medicine · doi:10.1002/sctm.20-0132 · Cited by 31 · see citing works
“function through angiogenesis, neovascularization, and vascular repair, leading to the formation of new blood vessels and increased branching of existing blood vessels after vascular disease.(5,6) In addi-”
Background
The JNK-EGR1 signaling axis promotes TNF-α-induced endothelial differentiation of human mesenchymal stem cells via VEGFR2 expression
Jung, E., Ou, S., Ahn, S. S., Yeo, H., Lee, Y. H., & Shin, S. Y. (2022) · Cell Death and Differentiation · doi:10.1038/s41418-022-01088-8 · Cited by 29 · see citing works
“TNF-α, a pro-inflammatory cytokine in the TME, stimulates MSCs to aid tumor angiogenesis [20].”
Background
Adipose Tissue Plasticity: A Comprehensive Definition and Multidimensional Insight
Mo, Y.-Y., Han, Y., Xu, S., Jiang, H., Wu, H., Cai, J., Li, L., Bu, Y., Xiao, F., Liang, H., et al. (2024) · Biomolecules · doi:10.3390/biom14101223 · Cited by 28 · see citing works
Donor variability among anti-inflammatory pre-activated mesenchymal stromal cells
Gray, A., Schloss, R. S., & Yarmush, M. L. (2016) · TECHNOLOGY · doi:10.1142/s2339547816500084 · Cited by 24 · see citing works
Human Umbilical Cord Mesenchymal Stem Cells Encapsulated with Pluronic F-127 Enhance the Regeneration and Angiogenesis of Thin Endometrium in Rat via Local IL-1β Stimulation
Zhou, S., Yu, L., Wang, P., Chen, J., Zeng, L., Qu, T., Maldonado, M., Huang, J., Han, T., Wen, Z., et al. (2022) · Stem Cells International · doi:10.1155/2022/7819234 · Cited by 28 · see citing works
“Incubation of MSCs with tumor necrosis factor-alpha (TNF-α) would promote the secretion of proangiogenic cytokines, which induce angiogenesis and tissue repair [24].”
Background
Small extracellular vesicles of hypoxic endothelial cells regulate the therapeutic potential of adipose-derived mesenchymal stem cells via miR-486-5p/PTEN in a limb ischemia model
Shen, Z., Wang, W., Chen, J., Chen, B., Tang, Y., Hou, J., Li, J., Liu, S., Mei, Y., Zhang, L., et al. (2022) · Journal of Nanobiotechnology · doi:10.1186/s12951-022-01632-1 · Cited by 21 · see citing works
“Inflammatory cytokines, such as interferon gamma (IFN-γ) [17, 18] and tumor necrosis factor alpha (TNF-α) [19, 20], have been considered able to mimic the inflammatory environment after transplantation and to boost the immunomodulatory effects of ADSCs.”
Background
Variability in Endogenous Perfusion Recovery of Immunocompromised Mouse Models of Limb Ischemia
Thomas, D., Thirumaran, A., Mallard, B. L., Chen, X., Browne, S., Wheatley, A. M., O’Brien, T., & Pandit, A. S. (2016) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2015.0441 · Cited by 21 · see citing works
Netrin-1-Induced Stem Cell Bioactivity Contributes to the Regeneration of Injured Tissues via the Lipid Raft-Dependent Integrin α6β4 Signaling Pathway
Lee, S. S., Lee, S., Lee, S. H., Ryu, J. M., Lim, H. S., Kim, J. S., Song, E. J., Jung, Y. H., Lee, H. J., Kim, C. H., et al. (2016) · Scientific Reports · doi:10.1038/srep37526 · Cited by 21 · see citing works
“Our results are consistent with the notion that MSCs treated with TNF-α stimulate the tissue regeneration process through paracrine mechanisms 53 .”
Role of Endothelial Progenitor Cell Transplantation in Rats With Sepsis
Xu, X., Yang, J. O., Li, N., Wu, R.-N., Tian, H., Song, H., & Wang, H. (2015) · Transplantation Proceedings · doi:10.1016/j.transproceed.2015.10.024 · Cited by 21 · see citing works
Role of Mesenchymal Stem/Stromal Cells in Head and Neck Cancer—Regulatory Mechanisms of Tumorigenic and Immune Activity, Chemotherapy Resistance, and Therapeutic Benefits of Stromal Cell-Based Pharmacological Strategies
Starska, K. (2024) · Cells · doi:10.3390/cells13151270 · Cited by 20 · see citing works
“D culture system [119–122].”
Effect of Tumor Necrosis Factor Alpha Dose and Exposure Time on Tumor Necrosis Factor-Induced Gene-6 Activation by Neonatal and Adult Mesenchymal Stromal Cells
Jahromi, S. H., Li, Y.-Q., & Davies, J. E. (2017) · Stem Cells and Development · doi:10.1089/scd.2017.0179 · Cited by 19 · see citing works
Role of secretomes in cell-free therapeutic strategies in regenerative medicine
Karimian, A., Khoshnazar, S. M., Kazemi, T., Asadi, A., & Abdolmaleki, A. (2023) · Cell and Tissue Banking · doi:10.1007/s10561-023-10073-5 · Cited by 18 · see citing works
“TNF-α has also been proven in the lab and in animals with limb ischemia to make MSCs more angiogenic (Kwon et al. 2013).”
Towards standardization of human adipose-derived stromal cells secretomes
Pinheiro-Machado, E., Getova, V. E., Harmsen, M. C., Burgess, J. K., & Smink, A. M. (2023) · Stem Cell Reviews and Reports · doi:10.1007/s12015-023-10567-5 · Cited by 17 · see citing works
“They do this by stimulating processes of angiogenesis [3], mitogenesis [4], cellular migration [5], and suppressing apoptosis [6].”
Background
Multiomics analyses of cytokines, genes, miRNA, and regulatory networks in human mesenchymal stem cells expanded in stirred microcarrier-spinner cultures
Lam, A. T., Lee, A., Jayaraman, P., Tan, K. Y., Raghothaman, D., Lim, H. L., He, C., Zhou, L., Tan, A. H., Reuveny, S., et al. (2021) · Stem Cell Research · doi:10.1016/j.scr.2021.102272 · Cited by 17 · see citing works
Preconditioning Human Adipose-Derived Stromal Cells on Decellularized Adipose Tissue Scaffolds Within a Perfusion Bioreactor Modulates Cell Phenotype and Promotes a Pro-regenerative Host Response
Han, T. T. Y., Walker, J. T., Grant, A. L., Dekaban, G. A., & Flynn, L. E. (2021) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2021.642465 · Cited by 17 · see citing works
“, 2004), it is becoming increasingly recognized that inflammation plays an important role in stimulating angiogenesis and tissue regeneration (Sainson et al., 2008; Kwon et al., 2013).”
Significant curative functions of the mesenchymal stem cells on methotrexate‐induced kidney and liver injuries in rats
Gad, A. M., Hassan, W. A., & Fikry, E. M. (2017) · Journal of Biochemical and Molecular Toxicology · doi:10.1002/jbt.21919 · Cited by 17 · see citing works
New Perspectives to Improve Mesenchymal Stem Cell Therapies for Drug-Induced Liver Injury
Ezquer, F. E., Huang, Y.-L., & Ezquer, M. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23052669 · Cited by 17 · see citing works
“The exposure of MSCs to INFγ stimulates IDO [70]; the pretreatment of MSCs with TNF-α increases migration, proliferation and angiogenic activity [71], whereas cytokine priming of MSCs with the combination of both TNF-α and INFγ can induce the secretion of cytokines such as IL-6, IL-5, IL-13, and increase the expressio…”
Background
Inflammatory response associated with choke vessel remodeling in the extended perforator flap model
Qing, L., Lei, P., Tang, J., Wu, P., Wang, L., Xie, J., & Hu, Y. (2017) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2017.4205 · Cited by 16 · see citing works
Relevance of angiogenesis in autoimmune testis inflammation
Gualdoni, G. S., Jacobo, P. V., Sobarzo, C., Pérez, C. V., Durand, L. A. H., Theas, M. S., Lustig, L., & Guazzone, V. A. (2020) · Molecular Human Reproduction · doi:10.1093/molehr/gaaa073 · Cited by 15 · see citing works
Three-Dimensional Culture of Equine Bone Marrow–Derived Mesenchymal Stem Cells Enhances Anti-Inflammatory Properties in a Donor-Dependent Manner
Bogers, S. H., & Barrett, J. G. (2022) · Stem Cells and Development · doi:10.1089/scd.2022.0074 · Cited by 14 · see citing works
“Pretreatment conditioning by exposure to exogenous cytokines [4–10], hypoxia [11–13], or through three-dimensional (3D) spheroid culture [14–16] enhances the anti-inﬂammatory phenotype of MSCs. Three-dimensional culture of human MSCs upregulates caspase-dependent IL-1 signaling during…”
Evaluation of secretomes derived from human dermal and adipose tissue mesenchymal stem/stromal cells for skin wound healing: not as effective as cells
Zomer, H. D., Lima, V. J. D. S., Bion, M. C., Brito, K. N. L., Rode, M. P., Stimamiglio, M. A., Jeremias, T. D. S., & Trentin, A. G. (2024) · Stem Cell Research & Therapy · doi:10.1186/s13287-023-03630-y · Cited by 14 · see citing works
Impaired angiogenesis in diabetic critical limb ischemia is mediated by a miR-130b/INHBA signaling axis
Cheng, H. S., Pérez‐Cremades, D., Zhuang, R., Jamaiyar, A., Wu, W. W., Chen, J., Tzani, A. I., Stone, L., Plutzky, J., RYAN, T. E., et al. (2023) · JCI Insight · doi:10.1172/jci.insight.163041 · Cited by 13 · see citing works
“Intramuscular injection of IL-8 increased neovascularization after hindlimb ischemia in mice by improving homing of tail vein-injected endothelial progenitor cells (46).”
Background
What Is the Impact of Depletion of Immunoregulatory Genes on Wound Healing? A Systematic Review of Preclinical Evidence
Nogueira, B. C. F., Campos, A. K., Alves, R. S., Sarandy, M. M., Novaes, R. D., Esposito, D., & Gonçalves, R. V. (2020) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2020/8862953 · Cited by 13 · see citing works
“In the proliferative phase, TNF-α controls the angiogenesis and formation of the tissue granulation; this is composed of cells and a network of blood vessels responsible for reestablishing regional circulation [17, 18].”
Background
An Outstanding Role of Adipose Tissue in Canine Stem Cell Therapy
Prišlin, M., Vlahović, D., Kostešić, P., Ljolje, I., Brnić, D., Turk, N., Lojkić, I., Kunić, V., Karadjole, T., & Krešić, N. (2022) · Animals · doi:10.3390/ani12091088 · Cited by 13 · see citing works
“In the liver, the mRNA expression levels of pro-inflammatory cytokines, such as IL-1, IL-6, IL-8, and IFNγ decreased significantly, but anti-inflammatory cytokines such as IL-4 and IL-10, HGF and VEGFA, were significantly increased after the first ASCs injection.”
Background
Bone marrow-derived mesenchymal stromal cell: what next?
Borges, F. T., Convento, M. B., & Schor, N. (2018) · Stem Cells and Cloning Advances and Applications · doi:10.2147/sccaa.s147804 · Cited by 12 · see citing works
“Conditioning of MSC with tumor necrosis factor α (TNF-α), an inflammatory cytokine produced by macrophages, stimulated an MSC angiogenic effect through VEGF production, proliferation, and differentiation into osteocytes.(58,59) Proteins can also be carried by EVs released by MSC, which keep them protected from microen…”
Background
Therapeutic potential of ixmyelocel-T, an expanded autologous multicellular therapy for treatment of ischemic cardiovascular diseases
Ledford, K. J., Murphy, N., Zeigler, F., Bartel, R. L., & Tubo, R. A. (2015) · Stem Cell Research & Therapy · doi:10.1186/s13287-015-0007-3 · Cited by 12 · see citing works
“Additionally, IL-6 and IL-8 are reported to increase endothelial progenitor cell homing to areas of ischemia [21].”
Background
Preconditioning of Human Dental Pulp Stem Cells with Leukocyte- and Platelet-Rich Fibrin-Derived Factors Does Not Enhance Their Neuroregenerative Effect
Gervois, P., Ratajczak, J., Wolfs, E., Vangansewinkel, T., Dillen, Y., Merckx, G., Bronckaers, A., & Lambrichts, I. (2019) · Stem Cells International · doi:10.1155/2019/8589149 · Cited by 12 · see citing works
“enhance MSC-mediated angiogenesis [27, 41, 50] whereas IL-10, IFN-γ, IL-α, and IL-1β were shown to stimulate the immunomodulatory properties of MSCs [28, 30, 31].”
Background
Time-dependently Appeared Microenvironmental Changes and Mechanism after Cartilage or Joint Damage and the Influences on Cartilage Regeneration
Yue, D., Du, L., Zhang, B., Wu, H. C., Yang, Q., Wang, M., & Pan, J. P. (2021) · Organogenesis · doi:10.1080/15476278.2021.1991199 · Cited by 11 · see citing works
“TNF-α activated MSCs promote endothelial progenitor cell homing and angiogenesis.(78) Inflammation affects immunomodulation and inflammation modulation of MSCs.”
Background
Revolutionizing orofacial pain management: the promising potential of stem cell therapy
Ren, K., Vickers, R., Murillo, J., & Ruparel, N. B. (2023) · Frontiers in Pain Research · doi:10.3389/fpain.2023.1239633 · Cited by 12 · see citing works
Hypoxia in Mesenchymal Stem Cell
Widowati, W., Rihibiha, D. D., Khiong, K., Widodo, M. A., Sumitro, S. B., & Bachtiar, I. (2017) · InTech eBooks · doi:10.5772/65510 · Cited by 11 · see citing works
“Pretreatment of TNF-α in MSCs provided superior angiogenic activity in vitro, as indicated by expression of VEGF, as well as in vivo in an animal model of critical limb ischemia, as compared to untreated MSCs [89].”
Current status of myocardial restoration via the paracrine function of mesenchymal stromal cells
Nguyen‐Truong, M., Hematti, P., & Wang, Z. (2021) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00217.2021 · Cited by 11 · see citing works
Transplantation of adipose tissue-derived microvascular fragments promotes therapy of critical limb ischemia
Park, G. T., Lim, J. K., Choi, E.-B., Lim, M.-J., Yun, B.-Y., Kim, D. K., Yoon, J. W., Hong, Y. G., Chang, J. H., Bae, S. H., et al. (2023) · Biomaterials Research · doi:10.1186/s40824-023-00395-6 · Cited by 10 · see citing works
Low Levels of Endothelial Progenitor Cells and Their Association with Systemic Inflammation and Monocyte Activation in Older HIV-Infected Men
Seang, S., Kelesidis, T., Huynh, D., Park, S., Moe, A. A., Currier, J. S., & Lake, J. E. (2017) · AIDS Research and Human Retroviruses · doi:10.1089/aid.2017.0057 · Cited by 10 · see citing works
Hypoxia and interleukin-1-primed mesenchymal stem/stromal cells as novel therapy for stroke
Salaudeen, M. A., Allan, S. M., & Pinteaux, E. (2023) · Human Cell · doi:10.1007/s13577-023-00997-1 · Cited by 9 · see citing works
“This cytokine also enhanced homing following intramuscular administration of the activated MSC and promoted tissue repair through the release of pro-angiogenic cytokines [113].”
Background
A Supportive Role of Mesenchymal Stem Cells on Insulin-Producing Langerhans Islets with a Specific Emphasis on The Secretome
Sionov, R. V., & Ahdut-HaCohen, R. (2023) · Biomedicines · doi:10.3390/biomedicines11092558 · Cited by 12 · see citing works
Therapeutic angiogenesis using tumor cell‐conditioned medium
Jang, H., Kim, B., Han, J., Yoon, J., Lee, J., Jeong, G., & Shin, J. (2016) · Biotechnology Progress · doi:10.1002/btpr.2226 · Cited by 9 · see citing works
Effects of Copper Reduction on Angiogenesis-Related Factors in Recurrent Glioblastoma Cases
Jazayeri, S., Feli, A., Bitaraf, M. A., Dodaran, M. S., Alikhani, M., & Hosseinzadeh‐Attar, M. J. (2016) · Europe PMC (PubMed Central) · doi:10.22034/apjcp.2016.17.10.4609 · Cited by 9 · see citing works
“Effects of TNF-α on angiogenesis and vasculogenesis already have shown in experimental models (Kwon et al., 2013).”
BackgroundMethodInfluential
Human umbilical cord blood-mesenchymal stem cell-derived secretome in combination with atorvastatin enhances endothelial progenitor cells proliferation and migration
Oktaviono, Y. H., Hutomo, S. A., Farabi, M. J. A., Chouw, A., & Sandra, F. (2020) · F1000Research · doi:10.12688/f1000research.23547.2 · Cited by 9 · see citing works
Specific Features of the Functional Activity of Human Adipose Stromal Cells in the Structure of a Partial Skin-Equivalent
Aleynik, D. Y., Charykova, I. N., Rubtsova, Y. P., Linkova, D. D., Александровна, Ф. Е., & Николаевна, Е. М. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25126290 · Cited by 8 · see citing works
“For example, in studies on ischemia models [82] and on skin wound healing [83] by depleting IL-6 and IL-8 from the ASC’s secretome, a signiﬁcant decrease in regenerative activity was demonstrated.”
Background
Mesenchymal Stem Cells
Patel, A. N., Bartlett, C. E., & Ichim, T. E. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-801888-0.00011-4 · Cited by 8 · see citing works
The effects of culture conditions on the functionality of efficiently obtained mesenchymal stromal cells from human cord blood
Laitinen, A., Lampinen, M., Liedtke, S., Kilpinen, L., Kerkelä, E., Sarkanen, J., Heinonen, T., Kögler, G., & Laitinen, S. (2016) · Cytotherapy · doi:10.1016/j.jcyt.2015.11.014 · Cited by 8 · see citing works
Tumor necrosis factor-α-activated mesenchymal stem cells accelerate wound healing through vascular endothelial growth factor regulation in rats
Nugraha, A., & Putra, A. B. (2018) · Universa Medicina · doi:10.18051/univmed.2018.v37.135-142 · Cited by 26 · see citing works
Mesenchymal stromal cell therapy in intestinal diseases
Ciccocioppo, R., Fioravante, M., & Frulloni, L. (2018) · Current Opinion in Organ Transplantation · doi:10.1097/mot.0000000000000586 · Cited by 7 · see citing works
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Authors: Kwon, Y. W., Heo, S. C., Jeong, G. O., Yoon, J. W., Mo, W. M., Lee, M. J., Jang, I.-H., Kwon, S. M., Lee, J. S., & Kim, J. H.
Affiliations: Pusan National University (KR)
Pusan National University Yangsan Hospital (KR)
Corresponding author: Kim, Jae Ho
ORCID: Heo, Soon Chul
Yoon, Jung Won
Jang, Il-Ho
Kwon, Sang Mo
Lee, Jung Sub
Kim, Jae Ho
Venue: Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease
Publisher: Elsevier BV
Published: 2013-12
Volume: 1832
Issue: 12
Pages: 2136-2144
ISSN: 0925-4439 (ISSN-L)
DOI: 10.1016/j.bbadis.2013.08.002
OpenAlex: W1968254493
Cited by: 137
References: 42
Citations by year: 2026: 5 · 2025: 3 · 2024: 11 · 2023: 12 · 2022: 13 · 2021: 13 · 2020: 17 · 2019: 11 · 2018: 11 · 2017: 11 · 2016: 16 · 2015: 11 · 2014: 3
FWCI: 4.92
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 365 d)
Locations: Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease (publishedVersion)
PubMed (publishedVersion)
Funders: National Research Foundation of Korea
Ministry of Education, Science and Technology (2010-0020274, 2012M3A9C7050093, 2012M3A9C7050184)
Topics: Health Sciences › Medicine › Genetics › Mesenchymal stem cell research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
Health Sciences › Medicine › Rehabilitation › Wound Healing and Treatments
Keywords: mesenchymal stem cells, TNF-α, endothelial progenitor cells, angiogenesis, EPC homing, interleukin-6, interleukin-8, paracrine signaling, hindlimb ischemia, tissue regeneration, blood perfusion, conditioned medium, immunodepletion
MeSH terms: Animals, Cell Movement, Cells, Cultured, Fluorescent Antibody Technique, Hindlimb, Humans, Ischemia, Mice, Nude, Necrosis, Stem Cells, Tumor Necrosis Factor-alpha, Wound Healing, Blotting, Western, Interleukin-6, Interleukin-8, Culture Media, Conditioned, Adipocytes, Neovascularization, Physiologic, Cell Proliferation, Mice, Mesenchymal Stem Cells, Human Umbilical Vein Endothelial Cells

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Tumor necrosis factor-α-activated mesenchymal stem cells promote endothelial progenitor cell homing and angiogenesis

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