Hypoxia Pretreatment of Bone Marrow Mesenchymal Stem Cells Facilitates Angiogenesis by Improving the Function of Endothelial Cells in Diabetic Rats with Lower Ischemia
Open accessAbstract
Endothelial dysfunction induced by unordered metabolism results in vascular reconstruction challenges in diabetic lower limb ischemia (DLLI). Mesenchymal stem cells (MSCs) are multipotent secretory cells that are suitable for clinical DLLI treatment, but their use has been hampered by poor survival after injection. Hypoxia can significantly enhance the capacity of MSCs to secrete angiogenic factors. We investigated transient hypoxia pretreatment of MSCs to facilitate revascularization in DLLI. Rat bone marrow MSCs (BM-MSCs) were cultured at different oxygen concentrations for varying time periods. The results indicated that transient pretreatment (5% O2, 48 h) not only increased the expression of VEGF-1α, ANG, HIF-1α and MMP-9 in BM-MSCs as assessed by real-time RT-PCR, but also increased the expression of Bcl-2 as determined by western blotting. The transplantation of pretreated BM-MSCs into rats with DLLI demonstrated accelerated vascular reconstruction when assayed by angiography and immunohistochemistry. CM-Dil-labeled tracer experiments indicated that the survival of BM-MSCs was significantly improved, with approximately 5% of the injected cells remaining alive at 14 days. The expression levels of VEGF-1α, MMP-9 and VEGF-R were significantly increased, and the expression of pAKT was up-regulated in ischemic muscle. Double immunofluorescence studies confirmed that the pretreated BM-MSCs promoted the proliferation and inhibited the apoptosis of endothelial cells. In vitro, pretreated BM-MSCs increased the migratory and tube forming capacity of endothelial cells (ECs). Hypoxia pretreatment of BM-MSCs significantly improved angiogenesis in response to tissue ischemia by ameliorating endothelial cell dysfunction and is a promising therapeutic treatment for DLLI.
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.
Integrity signals
Registry
Cites
Statistics
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.
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?
Upregulation of the VEGF gene was evident in all hypoxia cultures.
“Upregulation of the VEGF gene was evident in all hypoxia cultures, which is consistent with other studies [53–56].”
From Short-term physiological hypoxia potentiates the therapeutic function of mesenchymal stem cells (2018) · cites this paper as [56]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Multilineage potential of adult human mesenchymal stem cells
Pittenger, M. F., Mackay, A. M., Beck, S. C., Jaiswal, R. K., Douglas, R., Mosca, J. D., Moorman, M. A., Simonetti, D. W., Craig, S., & Marshak, D. R. (1999) · Science · doi:10.1126/science.284.5411.143 · Cited by 21,052 · see citing works
Wild, S., Roglic, G., Green, A., Sicree, R., & King, H. (2004) · Diabetes Care · doi:10.2337/diacare.27.5.1047 · Cited by 15,297 · see citing works
Angiogenesis in cancer and other diseases
Carmeliet, P., & Jain, R. K. (2000) · Nature · doi:10.1038/35025220 · Cited by 9,070 · see citing works
Nitric Oxide and Peroxynitrite in Health and Disease
Pacher, P., Beckman, J. S., & Liaudet, L. (2007) · Physiological Reviews · doi:10.1152/physrev.00029.2006 · Cited by 6,390 · see citing works
Mechanisms of angiogenesis and arteriogenesis
Carmeliet, P. (2000) · Nature Medicine · doi:10.1038/74651 · Cited by 4,146 · see citing works
Oxidative Stress and Stress-Activated Signaling Pathways: A Unifying Hypothesis of Type 2 Diabetes
Evans, J. L., Goldfine, I. D., Maddux, B. A., & Grodsky, G. M. (2002) · Endocrine Reviews · doi:10.1210/er.2001-0039 · Cited by 2,232 · see citing works
Pathways to Diabetic Limb Amputation: Basis for Prevention
Pecoraro, R. E., Reiber, G. E., & Burgess, E. M. (1990) · Diabetes Care · doi:10.2337/diacare.13.5.513 · Cited by 1,585 · see citing works
Kinnaird, T., Stabile, E., Burnett, M. S., Lee, C. W., Barr, S., Fuchs, S., & Epstein, S. E. (2004) · Circulation Research · doi:10.1161/01.res.0000118601.37875.ac · Cited by 1,415 · see citing works
Lumeij, J. T. (1997) · Elsevier eBooks · doi:10.1016/b978-012396305-5/50031-2 · Cited by 1,185 · see citing works
Central nervous system pericytes in health and disease
Winkler, E. A., Bell, R. D., & Zlokovic, B. V. (2011) · Nature Neuroscience · doi:10.1038/nn.2946 · Cited by 962 · see citing works
Obesity, Insulin Resistance, Diabetes, and Cardiovascular Risk in Children
Steinberger, J., & Daniels, S. R. (2003) · Circulation · doi:10.1161/01.cir.0000060923.07573.f2 · Cited by 812 · see citing works
Rosová, I., Dao, M. A., Capoccia, B. J., Link, D. C., & Nolta, J. A. (2008) · Stem Cells · doi:10.1634/stemcells.2007-1104 · Cited by 690 · see citing works
Hepatic insulin resistance, metabolic syndrome and cardiovascular disease
Meshkani, R., & Adeli, K. (2009) · Clinical Biochemistry · doi:10.1016/j.clinbiochem.2009.05.018 · Cited by 458 · see citing works
Hung, S.-C., Pochampally, R. R., Chen, S.-C., Hsu, S.-C., & Prockop, D. J. (2007) · Stem Cells · doi:10.1634/stemcells.2006-0686 · Cited by 457 · see citing works
Lennon, D. P., Edmison, J. M., & Caplan, A. I. (2001) · Journal of Cellular Physiology · doi:10.1002/jcp.1081 · Cited by 425 · see citing works
Effects of hypoxia on human mesenchymal stem cell expansion and plasticity in 3D constructs
Grayson, W. L., Zhao, F., Izadpanah, R., Bunnell, B. A., & Ma, T. (2005) · Journal of Cellular Physiology · doi:10.1002/jcp.20571 · Cited by 409 · see citing works
Tang, Y., Zhao, Q., Zhang, Y. C., Cheng, L., Liu, M., Shi, J., Yang, Y. Z., Pan, C., Ge, J., & Phillips, M. I. (2003) · Regulatory Peptides · doi:10.1016/j.regpep.2003.09.005 · Cited by 396 · see citing works
Clinical Applications of Blood-Derived and Marrow-Derived Stem Cells for Nonmalignant Diseases
Burt, R. K. (2008) · JAMA · doi:10.1001/jama.299.8.925 · Cited by 353 · see citing works
Role of Blood Flow and Impaired Autoregulation in the Pathogenesis of Diabetic Retinopathy
KOHNER, E. M., Patel, V., & Rassam, S. (1995) · Diabetes · doi:10.2337/diab.44.6.603 · Cited by 325 · see citing works
Hypoxia Promotes Murine Bone‐Marrow‐Derived Stromal Cell Migration and Tube Formation
Annabi, B., Lee, Y., Turcotte, S., Naud, E., Desrosiers, R. R., Champagne, M. A., Eliopoulos, N., Galipeau, J., & Béliveau, R. (2003) · Stem Cells · doi:10.1634/stemcells.21-3-337 · Cited by 302 · see citing works
The role of oxygen in regulating neural stem cells in development and disease
Panchision, D. M. (2009) · Journal of Cellular Physiology · doi:10.1002/jcp.21812 · Cited by 252 · see citing works
Matsumoto, R., Omura, T., Yoshiyama, M., Hayashi, T., Inamoto, S., Koh, K., Ohta, K., Izumi, Y., Nakamura, Y., Akioka, K., et al. (2005) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000165696.25680.ce · Cited by 225 · see citing works
Chang, E. I., Loh, S. A., Ceradini, D. J., Chang, E. I., Lin, S.-E., Bastidas, N., Aarabi, S., Chan, D. A., Freedman, M. L., Giaccia, A. J., et al. (2007) · Circulation · doi:10.1161/circulationaha.107.715847 · Cited by 206 · see citing works
Proliferation and differentiation of bone marrow stromal cells under hypoxic conditions
Ren, H., Cao, Y., Zhao, Q., Li, J., Zhou, C.-X., Liao, L., Jia, M., Zhao, Q., Cai, H., Han, Z., et al. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.05.169 · Cited by 201 · see citing works
Chacko, S. M., Ahmed, S., Selvendiran, K., Kuppusamy, M. L., Khan, M., & Kuppusamy, P. (2010) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00221.2010 · Cited by 200 · see citing works
Potential of mesenchymal stem cells in gene therapy approaches for inherited and acquired diseases
Reiser, J., Zhang, X.-Y., Hemenway, C. S., Mondal, D., Pradhan, L., & Russa, V. F. L. (2005) · Expert Opinion on Biological Therapy · doi:10.1517/14712598.5.12.1571 · Cited by 192 · see citing works
Leroux, L., Descamps, B., Tojais, N. F., Séguy, B., Oses, P., Moreau, C., Daret, D., Ivanović, Z., Boiron, J.-M., Lamazière, J. D., et al. (2010) · Molecular Therapy · doi:10.1038/mt.2010.108 · Cited by 183 · see citing works
Mesenchymal stem cells inhibit both endogenous and exogenous MMPs via secreted TIMPs
Lozito, T. P., & Tuan, R. S. (2011) · Journal of Cellular Physiology · doi:10.1002/jcp.22344 · Cited by 171 · see citing works
Nekanti, U., Dastidar, S., Venugopal, P., Totey, S. M., & Ta, M. (2010) · International Journal of Biological Sciences · doi:10.7150/ijbs.6.499 · Cited by 157 · see citing works
Shen, G. X. (2010) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y10-018 · Cited by 141 · see citing works
Li, H., Isomaa, B., Taskinen, M., Groop, L., & Tuomi, T. (2000) · Diabetes Care · doi:10.2337/diacare.23.5.589 · Cited by 74 · see citing works
Zhang, H., Zhang, N., Li, M., Feng, H., Jin, W., Zhao, H., Chen, X., & Tian, L. (2008) · Annals of Vascular Surgery · doi:10.1016/j.avsg.2007.07.037 · Cited by 44 · see citing works
Kajiya, M., Hirota, M., Inai, Y., Kiyooka, T., Morimoto, T., Iwasaki, T., Endo, K., Mohri, S., Shimizu, J., Yada, T., et al. (2007) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00548.2006 · Cited by 41 · see citing works
Cao, Y., Sagi, S., Häcker, A., Steidler, A., Alken, P. M., & Knoll, T. M. (2006) · Urological Research · doi:10.1007/s00240-006-0055-3 · Cited by 16 · see citing works
Thermodynamic approach to oxygen delivery in vivo by natural and artificial oxygen carriers
Bucci, E. M. (2009) · Biophysical Chemistry · doi:10.1016/j.bpc.2008.12.009 · Cited by 14 · see citing works
Modulation of physical environment makes placental mesenchymal stromal cells suitable for therapy
Mathew, S. A., Rajendran, S., Gupta, P. K., & Bhonde, R. R. (2013) · Cell Biology International · doi:10.1002/cbin.10154 · Cited by 12 · see citing works
Le tissu adipeux : une écologie cellulaire subtile et complexe
Cousin, B., Caspar‐Bauguil, S., Planat‐Benard, V., Laharrague, P. F., Pénicaud, L., & Casteilla, L. (2006) · Journal de la Société de Biologie · doi:10.1051/jbio:2006007 · Cited by 10 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Mesenchymal stromal cell secretome: influencing therapeutic potential by cellular pre-conditioning
Ferreira, J. R., Teixeira, G. Q., Santos, S. G., Barbosa, M. A., Almeida-Porada, G., & Gonçalves, R. M. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02837 · Cited by 572 · see citing works
Macro‐ and microvascular endothelial dysfunction in diabetes
Shi, Y., & Vanhoutte, P. M. (2017) · Journal of Diabetes · doi:10.1111/1753-0407.12521 · Cited by 547 · see citing works
Preconditioning influences mesenchymal stem cell properties in vitro and in vivo
Hu, C., & Li, L. (2018) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.13492 · Cited by 444 · see citing works
The challenges and promises of allogeneic mesenchymal stem cells for use as a cell-based therapy
Zhang, J., Huang, X., Wang, H., Liu, X., Zhang, T., Wang, Y., & Hu, D. (2015) · Stem Cell Research & Therapy · doi:10.1186/s13287-015-0240-9 · Cited by 311 · see citing works
Mesenchymal Stem Cells for Chronic Wound Healing: Current Status of Preclinical and Clinical Studies
Huang, Y., Gou, M., Da, L., Zhang, W., & Xie, H. (2020) · Tissue Engineering Part B Reviews · doi:10.1089/ten.teb.2019.0351 · Cited by 209 · see citing works
Short-term physiological hypoxia potentiates the therapeutic function of mesenchymal stem cells
Antebi, B., Rodriguez, L. A., Walker, K. P., Asher, A. M., Kamucheka, R. M., Alvarado, L., Mohammadipoor, A., & Cancio, L. C. (2018) · Stem Cell Research & Therapy · doi:10.1186/s13287-018-1007-x · Cited by 137 · see citing works
Liu, Y. F., Chen, J., Liang, H., Cai, Y., Li, X., Li, Y., Zhou, L., Shan, L., & Wang, H. (2022) · Stem Cell Research & Therapy · doi:10.1186/s13287-022-02927-8 · Cited by 123 · see citing works
Rivera‐Cruz, C. M., Shearer, J. J., Neto, M. F., & Figueiredo, M. L. (2017) · Stem Cells International · doi:10.1155/2017/4015039 · Cited by 115 · see citing works
Babajani, A., Soltani, P., Jamshidi, E., Farjoo, M. H., & Niknejad, H. (2020) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2020.00748 · Cited by 99 · see citing works
Wang, X., Shen, K., Wang, J., Liu, K., Wu, G., Li, Y., Luo, L., Zheng, Z., & Hu, D. (2020) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2020.07.023 · Cited by 97 · see citing works
Kuss, M. A., Harms, R., Wu, S., Wang, Y., Untrauer, J. B., Carlson, M. A., & Duan, B. (2017) · RSC Advances · doi:10.1039/c7ra04372d · Cited by 81 · see citing works
Zhao, J., Yu, G., Cai, M., Lei, X., Yang, Y., Wang, Q., & Zhai, X. (2018) · Stem Cell Research & Therapy · doi:10.1186/s13287-018-0785-5 · Cited by 80 · see citing works
Potential role of hydrogen sulfide in diabetes-impaired angiogenesis and ischemic tissue repair
Cheng, Z. A., & Kishore, R. (2020) · Redox Biology · doi:10.1016/j.redox.2020.101704 · Cited by 80 · see citing works
Yuan, Y., Shi, M., Li, L., Liu, J., Chen, B., Chen, Y., An, X., Liu, S., Luo, R., Long, D., et al. (2016) · Clinical Science · doi:10.1042/cs20160235 · Cited by 70 · see citing works
Self-citationHan, K. H., Kim, A., Kim, M., Kim, D., Go, H., & Kim, D. (2015) · Cell Biology International · doi:10.1002/cbin.10519 · Cited by 67 · see citing works
Wobma, H., Kanai, M., Ma, S. P., Shih, Y., Li, H. W., Duran‐Struuck, R., WINCHESTER, R. J., Goeta, S., Brown, L. M., & Vunjak‐Novakovic, G. (2018) · Journal of Immunology and Regenerative Medicine · doi:10.1016/j.regen.2018.01.001 · Cited by 66 · see citing works
Zhilai, Z., Biling, M., Sujun, Q., Chao, D., Benchao, S., Huang, S., Shun, Y., & Zhang, H. (2016) · Brain Research · doi:10.1016/j.brainres.2016.04.025 · Cited by 65 · see citing works
Kahrizi, M. S., Mousavi, E., Khosravi, A., Rahnama, S., Salehi, A., Nasrabadi, N., Ebrahimzadeh, F., & Jamali, S. (2023) · Stem Cell Research & Therapy · doi:10.1186/s13287-023-03374-9 · Cited by 61 · see citing works
Jin, C., Yang, Y., Shen, L., Ding, W., Chen, X., Wu, E., Cai, K., & Wang, G. (2016) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-016-0445-1 · Cited by 53 · see citing works
Emerging roles of mesenchymal stem cell therapy in patients with critical limb ischemia
Shirbaghaee, Z., Hassani, M., Keshel, S. H., & Soleimani, M. (2022) · Stem Cell Research & Therapy · doi:10.1186/s13287-022-03148-9 · Cited by 49 · see citing works
CD73 + extracellular vesicles inhibit angiogenesis through adenosine A 2B receptor signalling
Angioni, R., Liboni, C., Herkenne, S., Sánchez‐Rodríguez, R., Borile, G., Marcuzzi, E., Calì, B., Muraca, M., & Viola, A. (2020) · Journal of Extracellular Vesicles · doi:10.1080/20013078.2020.1757900 · Cited by 49 · see citing works
Hao, D., He, C., Ma, B., Lankford, L., Reynaga, L., Farmer, D. L., Guo, F., & Wang, A. (2019) · Stem Cells International · doi:10.1155/2019/9695239 · Cited by 44 · see citing works
Rodriguez, L., Mohammadipoor, A., Alvarado, L., Kamucheka, R. M., Asher, A. M., Cancio, L. C., & Antebi, B. (2019) · Cells · doi:10.3390/cells8050462 · Cited by 42 · see citing works
Calcat-i-Cervera, S., Sanz‐Nogués, C., & O’Brien, T. (2021) · Frontiers in Medicine · doi:10.3389/fmed.2021.728496 · Cited by 42 · see citing works
Rovere, M., Reverberi, D., Arnaldi, P., Palamà, M. E. F., & Gentili, C. (2023) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2023.1297644 · Cited by 37 · see citing works
Chai, Y. C., Mendes, L. F., van Gastel, N., Carmeliet, G., & Luyten, F. P. (2018) · Acta Biomaterialia · doi:10.1016/j.actbio.2018.03.048 · Cited by 37 · see citing works
Xu, T., Lv, Z., Chen, Q., Guo, M., Wang, X., & Huang, F. (2018) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2018.06.129 · Cited by 37 · see citing works
Phelps, J., Hart, D. A., Mitha, A. P., Duncan, N. A., & Sen, A. (2023) · Stem Cell Research & Therapy · doi:10.1186/s13287-023-03439-9 · Cited by 36 · see citing works
Cozens, D., Grahame, E., Sutherland, E., Taylor, G., Berry, C. C., & Davies, R. L. (2018) · Scientific Reports · doi:10.1038/s41598-017-19079-y · Cited by 36 · see citing works
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
Self-citationLee, S., & Joe, Y. A. (2018) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2018.05.086 · Cited by 35 · see citing works
Mesenchymal Stem Cells in Cardiac Repair: Effects on Myocytes, Vasculature, and Fibroblasts
White, S., & Chong, J. J. H. (2020) · Clinical Therapeutics · doi:10.1016/j.clinthera.2020.08.010 · Cited by 35 · see citing works
Rekittke, N. E., Ang, M., Rawat, D., Khatri, R., & Linn, T. (2016) · Stem Cells International · doi:10.1155/2016/3764681 · Cited by 34 · see citing works
Zhu, F., Wei, C., Wu, H., Shuai, B., Yu, T., Gao, F., Yuan, Y., Zuo, D., Liu, X., Zhang, L., et al. (2022) · International Immunopharmacology · doi:10.1016/j.intimp.2022.109426 · Cited by 34 · see citing works
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
Advancements in diabetic foot ulcer research: Focus on mesenchymal stem cells and their exosomes
Wu, S., Zhou, Z., Li, Y., & Jiang, J. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e37031 · Cited by 29 · see citing works
Zhāng, Q., Wan, X.-X., Hu, X., Zhao, W., Ban, X.-X., Huang, Y., Yan, W., & Xiong, K. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.809656 · Cited by 28 · see citing works
Neo, S. H., Her, Z., Othman, R. B., Tee, C. A., Ong, L. C., Wang, Y., Tan, I., Tan, J., Yang, Y., Yang, Z., et al. (2023) · Stem Cell Research & Therapy · doi:10.1186/s13287-023-03481-7 · Cited by 26 · see citing works
Yin, C.-P., Liang, Y., Zhang, J., Ruan, G., Li, Z.-A., Pang, R., & Pan, X. (2016) · Stem Cells International · doi:10.1155/2016/9742034 · Cited by 26 · see citing works
Khasawneh, R. R., Abu‐El‐Rub, E., Serhan, A. O., Serhan, B. O., & Abu-El-Rub, H. (2019) · The Journal of Physiological Sciences · doi:10.1007/s12576-019-00720-6 · Cited by 24 · see citing works
Han, K.-H., Kim, A.-K., Kim, M.-H., Kim, D.-H., Go, H.-N., Kang, D., Chang, J. W., Choi, S. W., Kang, K.-S., & Kim, D.-I. (2017) · Tissue and Cell · doi:10.1016/j.tice.2017.09.006 · Cited by 20 · see citing works
First Clinical Experiences Using Preconditioning Approaches to Improve MSC-Based Therapies
Le, B., Cressman, A., Morales, D. L. S., & Fierro, F. A. (2024) · Current Stem Cell Reports · doi:10.1007/s40778-023-00232-5 · Cited by 20 · see citing works
Han, T. T. Y., & Flynn, L. E. (2020) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1002/term.3133 · Cited by 20 · see citing works
Wei, S., Chen, T., Kao, F., Hsu, Y.-J., & Chen, Y. (2022) · Journal of Tissue Engineering · doi:10.1177/20417314221084096 · Cited by 19 · see citing works
Biological mechanisms and applied prospects of mesenchymal stem cells in premature ovarian failure
Shi, L., Zhang, Z., Deng, M., Zheng, F., Liu, W., & Ye, S. (2022) · Medicine · doi:10.1097/md.0000000000030013 · Cited by 19 · see citing works
Jiang, Q., Yu, T., Huang, K., Lu, J., Zhang, H., & Hu, S. (2016) · PLoS ONE · doi:10.1371/journal.pone.0146074 · Cited by 18 · see citing works
Zhao, Y., Zhang, M., Lu, G., Huang, B., Wang, D., Shao, Y., & Lu, M. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.580131 · Cited by 18 · see citing works
Self-citationCooper, T. T., Sherman, S. E., Bell, G. I., Dayarathna, T. K., McRae, D. M., Ma, J., Lagugné‐Labarthet, F., Pasternak, S., Lajoie, G., & Hess, D. A. (2021) · Stem Cells and Development · doi:10.1089/scd.2020.0206 · Cited by 18 · see citing works
Adipose‐derived stem cells: A candidate for liver regeneration
Yang, D., Wang, Z. Q., Deng, J., Liao, J. Y., Wang, X., Xie, J., Deng, M., & Lü, M. H. (2015) · Journal of Digestive Diseases · doi:10.1111/1751-2980.12268 · Cited by 17 · see citing works
Shen, C., Chen, B., Gu, J., Ning, J., Chen, L., Zeng, J., Yi, B., & Lu, K. (2016) · Experimental Cell Research · doi:10.1016/j.yexcr.2016.04.013 · Cited by 17 · see citing works
Subbarayan, R., Barathidasan, R., Raja, S. T. K., Gnanamani, A., Kuruvilla, S., Shanthi, P., & Rao, S. R. (2019) · Journal of Cellular Biochemistry · doi:10.1002/jcb.29452 · Cited by 17 · see citing works
The Angiogenic Paracrine Potential of Mesenchymal Stem Cells
Rezaie, J., Heidarzadeh, M., Hassanpour, M., Amini, H., Shokrollahi, E., Ahmadi, M., & Rahbarghazi, R. (2019) · IntechOpen eBooks · doi:10.5772/intechopen.84433 · Cited by 17 · see citing works
Peng, X., Liang, B., Wang, H., Hou, J., & Yuan, Q. (2022) · Cell and Tissue Research · doi:10.1007/s00441-021-03562-0 · Cited by 16 · see citing works
Taheri, M., Tehrani, H. A., Dehghani, S., Rajabzadeh, A., Alibolandi, M., Zamani, N., Arefian, E., & Ramezani, M. (2024) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2024.01.004 · Cited by 16 · see citing works
Wang, J., Xiang, B., Deng, J., Lin, H., Freed, D. H., Arora, R. C., & Tian, G. (2017) · Journal of Huazhong University of Science and Technology [Medical Sciences] · doi:10.1007/s11596-017-1766-0 · Cited by 16 · see citing works
Santos, R. D. A., Asensi, K. D., de Barros, J. H. O., de Menezes, R. C. S., Cordeiro, I. R., Brito, J. M., Kasai-Brunswick, T. H., & Goldenberg, R. C. D. S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21249563 · Cited by 15 · see citing works
Subbarayan, R., Girija, D. M., Raja, S. T. K., Krishnamoorthy, A., Srinivasan, D., Shrestha, R., Srivastava, N., & Rao, S. R. (2024) · Molecular Biology Reports · doi:10.1007/s11033-024-09503-8 · Cited by 14 · see citing works
Hirose, S., Tabata, Y., Sone, K., Takahashi, N., Yoshino, D., & Funamoto, K. (2021) · Cell Adhesion & Migration · doi:10.1080/19336918.2021.1978368 · 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
Lee, S. M., Jun, D. W., Kang, H. T., Oh, J., Saeed, W. K., & Ahn, S. B. (2021) · International Journal of Stem Cells · doi:10.15283/ijsc20096 · Cited by 10 · see citing works
Vu, N. B., Phi, L. T., Dao, T. T.-T., Le, H. T.-N., Ta, V. T., & Pham, P. V. (2016) · Biomedical Research and Therapy · doi:10.7603/s40730-016-0046-0 · Cited by 10 · see citing works
Zhao, P., Zhang, Y., Zhang, G., Niu, H., Li, J. J., Hao, R., Xie, M., Chu, S., Li, X., & Li, G. (2025) · Journal of Hypertension · doi:10.1097/hjh.0000000000004022 · Cited by 9 · see citing works
Ciavarella, C., Fittipaldi, S., & Pasquinelli, G. (2016) · Methods in molecular biology · doi:10.1007/7651_2016_350 · Cited by 8 · see citing works
Pham, P. V., Vu, N. B., Dao, T. T.-T., Le, H. T.-N., Phi, L. T., Huynh, O. T., Truong, M. T.-H., Nguyen, O. T.-K., & Phan, N. K. (2017) · Cytotechnology · doi:10.1007/s10616-017-0095-2 · Cited by 6 · see citing works
Weldearegay, Y. B., Brogaard, L., Rautenschlein, S., Meens, J., Valentin‐Weigand, P., & Schaaf, D. (2025) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2025.1565513 · Cited by 5 · see citing works
He, Y. Z., Ma, M., Yan, Y., Chen, C., Luo, H., & Lei, W. (2020) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.15598 · Cited by 5 · see citing works
Fuchs, B., Birt, A., Moellhoff, N., Kuhlmann, C., Giunta, R. E., & Wiggenhauser, P. S. (2023) · Medicina · doi:10.3390/medicina59040706 · Cited by 5 · see citing works
Update on Mesenchymal and Induced Pluripotent Stem Cells
Al‐Anazi, K. A. (2019) · IntechOpen eBooks · doi:10.5772/intechopen.77857 · Cited by 5 · see citing works
Unlocking MSC Potential: Metabolic Reprogramming via Synthetic Biology Approaches
Trufanova, N. A., Trufanov, O., & Petrenko, O. (2025) · SynBio · doi:10.3390/synbio3030013 · Cited by 4 · see citing works
Li, Z., Sun, Y., Wu, J., Zhang, W., Li, T., Tang, S., & Ding, G. (2026) · International Journal of Nanomedicine · doi:10.2147/ijn.s584494 · Cited by 4 · see citing works
Eltrombopag increases the hematopoietic supporting ability of mesenchymal stem/stromal cells
Muntión, S., Preciado, S., Sánchez-Luis, E., Corchete, L. A., Díez‐Campelo, M., Osugui, L., Martí-Chillón, G. J., Vídriales, M., Navarro‐Bailón, A., Rivas, J. D. L., et al. (2022) · Therapeutic Advances in Hematology · doi:10.1177/20406207221142137 · Cited by 4 · see citing works
Metabolic conditioning enhances human bmMSC therapy of doxorubicin-induced heart failure
Jacques, V., Benaouadi, S., Descamps, J.-G., Reina, N., Espagnolle, N., Marsal, D. J., Sainte–Marie, Y., Boudet, A., Carla, P., Farge, T., et al. (2024) · Stem Cells · doi:10.1093/stmcls/sxae050 · Cited by 3 · see citing works
Cell therapy of critical limb ischemia: A review of preclinical and clinical research in China
Liao, L. (2020) · Vascular Investigation and Therapy · doi:10.4103/vit.vit_7_20 · Cited by 3 · see citing works
Boulos, A. N., Elagawany, A. M., Awwad, A., Fouad, G., & El-Rahman, A. A. (2020) · The Egyptian Journal of Histology · doi:10.21608/ejh.2020.24878.1257 · Cited by 3 · see citing works
Orassay, A., Yerzhigit, N., Ganina, A., Chuvakova, E., Lookin, O. N., & Baigenzhin, A. K. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27104323 · Cited by 2 · see citing works
Quantitative Expression of Key Cancer Markers in the AS-30D Hepatocarcinoma Model
Briones-Orta, M. A., Delgado‐Coello, B., Gutiérrez‐Vidal, R., Sosa‐Garrocho, M., Macías‐Silva, M., & Mas‐Oliva, J. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.670292 · Cited by 2 · see citing works
Gofron, M., Mrozikiewicz‐Rakowska, B., Sieńko, D., & Czupryniak, L. (2020) · Clinical Diabetology · doi:10.5603/dk.2020.0065 · Cited by 2 · see citing works
Hypoxia: A Potent Regulator of Angiogenesis Through Extracellular Matrix Remodelling
Karavasili, K., & Koolwijk, P. (2022) · Biology of extracellular matrix · doi:10.1007/978-3-031-19616-4_8 · Cited by 2 · see citing works
Hypoxia Effects in Intervertebral Disc-Derived Stem Cells and Discus Secretomes: An in vitro Study
Romaniyanto, Mahyudin, F., Prakoeswa, C. R. S., Notobroto, H. B., Tinduh, D., Ausrin, R., Rantam, F. A., Suroto, H., Utomo, D. N., & Rhatomy, S. (2022) · Stem Cells and Cloning Advances and Applications · doi:10.2147/sccaa.s363951 · Cited by 2 · see citing works
Karimi, M., Zandsalimi, K., Jafary, H., Akbari, N., & Heidari, B. (2025) · Research Square · doi:10.21203/rs.3.rs-7136519/v1 · Cited by 2 · see citing works
Asadi-Yousefabad, S.-L., Nammian, P., Sheikhha, M. H., Tabei, K., Daneshi, S., Nikukar, H., Lotfi, M., & Razban, V. (2022) · Cell and Tissue Banking · doi:10.1007/s10561-022-10007-7 · Cited by 1 · see citing works
Бобылева, П. И., Rudimova, Y. V., & Buravkova, L. B. (2023) · Bulletin of Experimental Biology and Medicine · doi:10.1007/s10517-023-05870-7 · Cited by 1 · see citing works
The Inflammatory Environment and Its Effects on Mesenchymal Stem/Stromal Cells
Németh, K. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803102-5.00018-5
Yuen, J. S. K., Barrick, B. M., DiCindio, H., Pietropinto, J. A., & Kaplan, D. L. (2023) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.3c00358
Neo, S. H., Her, Z., Othman, R. B., Tee, C. A., Ong, L. C., Wang, Y., Tan, I., Tan, J., Yang, Y., Yang, Z., et al. (2023) · Figshare · doi:10.6084/m9.figshare.24164987
Neo, S. H., Her, Z., Othman, R. B., Tee, C. A., Ong, L. C., Wang, Y., Tan, I., Tan, J., Yang, Y., Yang, Z., et al. (2023) · Figshare · doi:10.6084/m9.figshare.24164990
Neo, S. H., Her, Z., Othman, R. B., Tee, C. A., Ong, L. C., Wang, Y., Tan, I., Tan, J., Yang, Y., Yang, Z., et al. (2023) · Figshare · doi:10.6084/m9.figshare.24164972
Neo, S. H., Her, Z., Othman, R. B., Tee, C. A., Ong, L. C., Wang, Y., Tan, I., Tan, J., Yang, Y., Yang, Z., et al. (2023) · Figshare · doi:10.6084/m9.figshare.24164984
Neo, S. H., Her, Z., Othman, R. B., Tee, C. A., Ong, L. C., Wang, Y., Tan, I., Tan, J., Yang, Y., Yang, Z., et al. (2023) · Figshare · doi:10.6084/m9.figshare.24164975
Phelps, J., Hart, D. A., Mitha, A. P., Duncan, N. A., & Sen, A. (2024) · Figshare · doi:10.6084/m9.figshare.26612204
Phelps, J., Hart, D. A., Mitha, A. P., Duncan, N. A., & Sen, A. (2024) · Figshare · doi:10.6084/m9.figshare.26612195
Neo, S. H., Her, Z., Othman, R. B., Tee, C. A., Ong, L. C., Wang, Y., Tan, I., Tan, J., Yang, Y., Yang, Z., et al. (2023) · Figshare · doi:10.6084/m9.figshare.24164969
Neo, S. H., Her, Z., Othman, R. B., Tee, C. A., Ong, L. C., Wang, Y., Tan, I., Tan, J., Yang, Y., Yang, Z., et al. (2023) · Figshare · doi:10.6084/m9.figshare.24164978
Phelps, J., Hart, D. A., Mitha, A. P., Duncan, N. A., & Sen, A. (2024) · Figshare · doi:10.6084/m9.figshare.26612201
Phelps, J., Hart, D. A., Mitha, A. P., Duncan, N. A., & Sen, A. (2024) · Figshare · doi:10.6084/m9.figshare.26612207
Phelps, J., Hart, D. A., Mitha, A. P., Duncan, N. A., & Sen, A. (2024) · Figshare · doi:10.6084/m9.figshare.26612198
Liu, Y., Chen, J., Liang, H., 蔡月琴, Li, X., Yan, L., Zhou, L., Shan, L., & Wang, H. (2022) · Figshare · doi:10.6084/m9.figshare.20098331
Neo, S. H., Her, Z., Othman, R. B., Tee, C. A., Ong, L. C., Wang, Y., Tan, I., Tan, J., Yang, Y., Yang, Z., et al. (2023) · Figshare · doi:10.6084/m9.figshare.24164966
Phelps, J., Hart, D. A., Mitha, A. P., Duncan, N. A., & Sen, A. (2024) · Figshare · doi:10.6084/m9.figshare.26612192
Basu, R., Madison, M. K., Sualeh, A. H., Clark, T. S., Stashevsky, J., Aridi, H. D., Zhang, N., Anekal, S., Murphy, M. P., Miller, S. J., et al. (2026) · Bioengineering & Translational Medicine · doi:10.1002/btm2.70119
- Authors
- Liu, J., Hao, H., Xia, L., Ti, D., Huang, H., Dong, L., Tong, C., Hou, Q., Zhao, Y., Liu, H., Fu, X., & Han, W.
- Affiliations
- Chinese PLA General Hospital (CN)
- Corresponding author
- Fu, Xiaobing
- Han, Weidong
- ORCID
- Venue
- PLOS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2015-05-21
- Volume
- 10
- Issue
- 5
- Pages
- e0126715
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC4440823
- OpenAlex
- W1506316383
- Cited by
- 101
- References
- 37
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 12 · 2023: 13 · 2022: 11 · 2021: 7 · 2020: 14 · 2019: 6 · 2018: 10 · 2017: 7 · 2016: 10 · 2015: 3
- FWCI
- 5.60
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- National Natural Science Foundation of China (2012CB518105, 81121004, 81230041, 2013AA020105, 2012AA020502, 2012CB518103)
- 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 › Surgery › Tissue Engineering and Regenerative Medicine
- Keywords
- bone marrow mesenchymal stem cells, angiogenesis, endothelial dysfunction, revascularization, HIF-1α, MMP-9, Bcl-2, cell survival after transplantation, Akt signaling, angiogenic factors
- MeSH terms
- Angiography, Animals, Hypoxia, Cell Survival, Cells, Cultured, Diabetes Mellitus, Experimental, Disease Models, Animal, Humans, Ischemia, Male, Neovascularization, Pathologic, Ultrasonography, Signal Transduction, Apoptosis, Lower Extremity, Vascular Endothelial Growth Factors, Endothelial Cells, Angiogenesis Inducing Agents, Mesenchymal Stem Cell Transplantation, Proto-Oncogene Proteins c-akt, Rats, Mesenchymal Stem Cells, Human Umbilical Vein Endothelial Cells
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