New perspectives on treatment of gastrointestinal diseases: therapeutic potential of mesenchymal stromal cells
DOI:
https://doi.org/10.21638/spbu03.2022.307Abstract
Mesenchymal stromal cells (MSCs) are a promising resource for cell therapy of different organs and systems, including the gastrointestinal tract (GIT). Therapeutic effect of MSC transplantation in GIT diseases may be partly due to their differentiation into various cellular components of the digestive tube. However, more significant is regulatory influence of MSCs on survival, proliferation, and differentiation of the gastric and intestinal epithelial cells, as well as their immunomodulatory, pro-angiogenic and antifibrotic effects. Data from experiments on animals and clinical trials indicate prospect of using MSCs in various diseases affecting any parts of GIT. However, effective and safe clinical use of MSCs requires an in-depth study of the mechanisms of their therapeutic effect, the development of optimal methods of administration, and risk assessment of adverse effects. This review analyzes MSC participation in regeneration of GIT and systematizes data on the potential of using MSCs in the treatment of gastroenterological diseases.
Keywords:
mesenchymal stromal cells, gastrointestinal tract, esophagus, stomach, intestines, regenerative medicine, cell therapy
Downloads
Download data is not yet available.
References
Accarie, A., l'Homme, B., Benadjaoud, M. A., Lim, S. K., Guha, C., Benderitter, M., Tamarat, R., and Sémont, A. 2020. Extracellular vesicles derived from mesenchymal stromal cells mitigate intestinal toxicity in a mouse model of acute radiation syndrome. Stem Cell Research & Therapy 11(1):371. https://doi.org/10.1186/s13287-020-01887-1
Adas, G., Kemik, O., Eryasar, B., Okcu, A., Adas, M., Arikan, S., Erman, G., Kemik, A. S., Kamali, G., Dogan, Y., and Karaoz, E. 2013. Treatment of ischemic colonic anastomoses with systemic transplanted bone marrow derived mesenchymal stem cells. European Review for Medical and Pharmacological Sciences 17(17):2275–2285.
Akduman, H., Dilli, D., Ergün, E., Çakmakçı, E., Çelebi, S. K., Çitli, R., and Zenciroğlu, A. 2021. Successful mesenchymal stem cell application in supraventricular tachycardia-related necrotizing enterocolitis: a case report. Fetal and Pediatric Pathology 40(3):250–255. https://doi.org/10.1080/15513815.2019.1693672
Alazzouni, A. S., Fathalla, A. S., Gabri, M. S., Dkhil, M. A., and Hassan, B. N. 2020. Role of bone marrow derived-mesenchymal stem cells against gastric ulceration: Histological, immunohistochemical and ultrastructural study. Saudi Journal of Biological Sciences 27(12):3456–3464. https://doi.org/10.1016/j.sjbs.2020.09.044
Al-Hakami, A., Alqhatani, S. Q., Shaik, S., Jalfan, S. M., Dhammam, M. S. A., Asiri, W., Alkahtani, A. M., Devaraj, A., and Chandramoorthy, H. C. 2020. Cytokine physiognomies of MSCs from varied sources confirm the regenerative commitment post-coculture with activated neutrophils. Journal of Cellular Physiology 235(11):8691–8701. https://doi.org/10.1002/jcp.29713
An, J. H., Song, W. J., Li, Q., Kim, S. M., Yang, J. I., Ryu, M. O., Nam, A. R., Bhang, D. H., Jung, Y. C., and Youn, H. Y. 2018. Prostaglandin E2 secreted from feline adipose tissue-derived mesenchymal stem cells alleviate DSS-induced colitis by increasing regulatory T cells in mice. BMC Veterinary Research 14(1):354. https://doi.org/10.1186/s12917-018-1684-9
Baberg, F., Geyh, S., Waldera-Lupa, D., Stefanski, A., Zilkens, C., Haas, R., Schroeder, T., and Stühler, K. 2019. Secretome analysis of human bone marrow derived mesenchymal stromal cells. Biochimica et Biophysica Acta — Proteins and Proteomics 1867(4):434–441. https://doi.org/10.1016/j.bbapap.2019.01.013
Banerjee, A., Bizzaro, D., Burra, P., Di Liddo, R., Pathak, S., Arcidiacono, D., Cappon, A., Bo, P., Conconi, M. T., Crescenzi, M., Pinna, C. M., Parnigotto, P. P., Alison, M. R., Sturniolo, G. C., D'Incà, R., and Russo, F. P. 2015. Umbilical cord mesenchymal stem cells modulate dextran sulfate sodium induced acute colitis in immunodeficient mice. Stem Cell Research & Therapy 6(1):79. https://doi.org/10.1186/s13287-015-0073-6
Barnhoorn, M. C., Wasser, M. N. J. M., Roelofs, H., Maljaars, P. W. J., Molendijk, I., Bonsing, B. A., Oosten, L. E. M., Dijkstra, G., van der Woude, C. J., Roelen, D. L., Zwaginga, J. J., Verspaget, H. W., Fibbe, W. E., Hommes, D. W., Peeters, K. C. M. J., and van der Meulen-de Jong, A. E. 2020. Long-term evaluation of allogeneic bone marrow-derived mesenchymal stromal cell therapy for Crohn's disease perianal fistulas. Journal of Crohn's and Colitis 14(1):64–70. https://doi.org/10.1093/ecco-jcc/jjz116
Beeravolu, N., McKee, C., Alamri, A., Mikhael, S., Brown, C., Perez-Cruet, M., and Chaudhry, G. R. 2017. Isolation and characterization of mesenchymal stromal cells from human umbilical cord and fetal placenta. Journal of Visualized Experiments (122):55224. https://doi.org/10.3791/55224
Bie, Q., Zhang, B., Sun, C., Ji, X., Barnie, P.A., Qi, C., Peng, J., Zhang, D., Zheng, D., Su, Z., Wang, S., and Xu, H. 2017. IL-17B activated mesenchymal stem cells enhance proliferation and migration of gastric cancer cells. Oncotarget 8(12):18914–18923. https://doi.org/10.18632/oncotarget.14835
Brügger, M. D., Valenta, T., Fazilaty, H., Hausmann, G., and Basler, K. 2020. Distinct populations of crypt-associated fibroblasts act as signaling hubs to control colon homeostasis. PLOS Biology 18(12):e3001032. https://doi.org/10.1371/journal.pbio.3001032
Caplan, A. I. 1991. Mesenchymal stem cells. Journal of Orthopaedic Research 9(5):641–650. https://doi.org/10.1002/jor.1100090504
Catry, J., Luong-Nguyen, M., Arakelian, L., Poghosyan, T., Bruneval, P., Domet, T., Michaud, L., Sfeir, R., Gottrand, F., Larghero, J., Vanneaux, V., and Cattan, P. 2017. Circumferential esophageal replacement by a tissue-engineered substitute using mesenchymal stem cells: An experimental study in mini pigs. Cell Transplantation 26(12):1831–1839. https://doi.org/10.1177/0963689717741498
Caziuc, A., Calin Dindelegan, G., Pall, E., and Mironiuc, A. 2015. Stem cells improve the quality of colonic anastomoses — A systematic review. Journal of BUON 20(6):1624–1629.
Chang, P., Qu, Y., Liu, Y., Cui, S., Zhu, D., Wang, H., and Jin, X. 2013. Multi-therapeutic effects of human adipose-derived mesenchymal stem cells on radiation-induced intestinal injury. Cell Death & Disease 4(6):e685. https://doi.org/10.1038/cddis.2013.178
Chang, P. Y., Zhang, B. Y., Cui, S., Qu, C., Shao, L. H., Xu, T. K., Qu, Y. Q., Dong, L. H., and Wang, J. 2017. MSC-derived cytokines repair radiation-induced intra-villi microvascular injury. Oncotarget 8(50):87821–87836. https://doi.org/10.18632/oncotarget.21236
Chen, J., Lau, B. T., Andor, N., Grimes, S. M., Handy, C., Wood-Bouwens, C., and Ji, H. P. 2019. Single-cell transcriptome analysis identifies distinct cell types and niche signaling in a primary gastric organoid model. Scientific Reports 9(1):4536. https://doi.org/10.1038/s41598-019-40809-x
Cheng, F., Huang, Z., and Li, Z. 2019. Mesenchymal stem-cell therapy for perianal fistulas in Crohn's disease: a systematic review and meta-analysis. Techniques in Coloproctology 23(7):613–623. https://doi.org/10.1007/s10151-019-02024-8
Dominici, M., Le Blanc, K., Mueller, I., Slaper-Cortenbach, I., Marini, F., Krause, D., Deans, R., Keating, A., Prockop, D., and Horwitz, E. 2006. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8(4):315–317. https://doi.org/10.1080/14653240600855905
Donnelly, J. M., Engevik, A., Feng, R., Xiao, C., Boivin, G. P., Li, J., Houghton, J., and Zavros, Y. 2014. Mesenchymal stem cells induce epithelial proliferation within the inflamed stomach. American Journal of Physiology - Gastrointestinal and Liver Physiology 306(12):G1075–G1088. https://doi.org/10.1152/ajpgi.00489.2012
Gao, J. G., Yu, M. S., Zhang, M. M., Gu, X. W., Ren, Y., Zhou, X. X., Chen, D., Yan, T. L., Li, Y. M., and Jin, X. 2020. Adipose-derived mesenchymal stem cells alleviate TNBS-induced colitis in rats by influencing intestinal epithelial cell regeneration, Wnt signaling, and T cell immunity. World Journal of Gastroenterology 26(26):3750–3766. https://doi.org/10.3748/wjg.v26.i26.3750
Grim, C., Noble, R., Uribe, G., Khanipov, K., Johnson, P., Koltun, W. A., Watts, T., Fofanov, Y., Yochum, G. S., Powell, D. W., Beswick, E. J., and Pinchuk, I. V. 2021. Impairment of tissue resident mesenchymal stem cells in chronic ulcerative colitis and Crohn's disease. Journal of Crohn's and Colitis 15(8):1362–1375. https://doi.org/10.1093/ecco-jcc/jjab001
Han, Y., Li, X., Zhang, Y., Han, Y., Chang, F., and Ding, J. 2019. Mesenchymal stem cells for regenerative medicine. Cells 8(8):886. https://doi.org/10.3390/cells8080886
Han, Y. M., Park, J. M., Choi, Y. S., Jin, H., Lee, Y. S., Han, N. Y., Lee, H., and Hahm, K. B. 2017. The efficacy of human placenta-derived mesenchymal stem cells on radiation enteropathy along with proteomic biomarkers predicting a favorable response. Stem Cell Research & Therapy 8(1):105. https://doi.org/10.1186/s13287-017-0559-5
Hayashi, Y., Tsuji, S., Tsujii, M., Nishida, T., Ishii, S., Iijima, H., Nakamura, T., Eguchi, H., Miyoshi, E., Hayashi, N., and Kawano, S. 2008. Topical transplantation of mesenchymal stem cells accelerates gastric ulcer healing in rats. American Journal of Physiology — Gastrointestinal and Liver Physiology 294(3):G778–G786. https://doi.org/10.1152/ajpgi.00468.2007
He, L., Zhao, F., Zheng, Y., Wan, Y., and Song, J. 2016. Loss of interactions between p53 and survivin gene in mesenchymal stem cells after spontaneous transformation in vitro. The International Journal of Biochemistry & Cell Biology 75:74–84. https://doi.org/10.1016/j.biocel.2016.03.018
He, R., Han, C., Li, Y., Qian, W., and Hou, X. 2021. Cancer-preventive role of bone marrow-derived mesenchymal stem cells on colitis-associated colorectal cancer: roles of gut microbiota involved. Frontiers in Cell and Developmental Biology 9:642948. https://doi.org/10.3389/fcell.2021.642948
He, W., Liang, B., Wang, C., Li, S., Zhao, Y., Huang, Q., Liu, Z., Yao, Z., Wu, Q., Liao, W., Zhang, S., Liu, Y., Xiang, Y., Liu, J., and Shi, M. 2019. MSC-regulated lncRNA MACC1-AS1 promotes stemness and chemoresistance through fatty acid oxidation in gastric cancer. Oncogene 38(23):4637–4654. https://doi.org/10.1038/s41388-019-0747-0
Hegner, B., Schaub, T., Catar, R., Kusch, A., Wagner, P., Essin, K., Lange, C., Riemekasten, G., and Dragun, D. 2016. Intrinsic deregulation of vascular smooth muscle and myofibroblast differentiation in mesenchymal stromal cells from patients with systemic sclerosis. PLoS One 11(4):e0153101. https://doi.org/10.1371/journal.pone.0153101
Horiguchi, H., Endo, M., Kawane, K., Kadomatsu, T., Terada, K., Morinaga, J., Araki, K., Miyata, K., and Oike, Y. 2017. ANGPTL2 expression in the intestinal stem cell niche controls epithelial regeneration and homeostasis. EMBO Journal 36(4):409–424. https://doi.org/10.15252/embj.201695690
Horwitz, E. M., Prockop, D. J., Fitzpatrick, L. A., Koo, W. W., Gordon, P. L., Neel, M., Sussman, M., Orchard, P., Marx, J. C., Pyeritz, R. E., and Brenner, M. K. 1999. Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nature Medicine 5(3):309–313. https://doi.org/10.1038/6529
Hwang, S., Hong, H. N., Kim, H. S., Park, S. R., Won, Y. J., Choi, S. T., Choi, D., and Lee, S. G. 2012. Hepatogenic differentiation of mesenchymal stem cells in a rat model of thioacetamide-induced liver cirrhosis. Cell Biology International 36(3):279–288. https://doi.org/10.1042/CBI20110325
Jensen, A. R., Drucker, N. A., Ferkowicz, M. J., and Markel, T. A. 2018. Umbilical mesenchymal stromal cells provide intestinal protection through nitric oxide dependent pathways. Journal of Surgical Research 224:148–155. https://doi.org/10.1016/j.jss.2017.11.068
Jensen, T., Wanczyk, H., Sharma, I., Mitchell, A., Sayej, W. N., and Finck, C. 2019. Polyurethane scaffolds seeded with autologous cells can regenerate long esophageal gaps: An esophageal atresia treatment model. Journal of Pediatric Surgery 54(9):1744–1754. https://doi.org/10.1016/j.jpedsurg.2018.09.024
Ji, R., Zhang, X., Qian, H., Gu, H., Sun, Z., Mao, F., Yan, Y., Chen, J., Liang, Z., and Xu, W. 2017. miR-374 mediates the malignant transformation of gastric cancer-associated mesenchymal stem cells in an experimental rat model. Oncology Reports 38(3):1473–1481. https://doi.org/10.3892/or.2017.5831
Jiang, H., Qu, L., Dou, R., Lu, L., Bian, S., and Zhu, W. 2013. Potential role of mesenchymal stem cells in alleviating intestinal ischemia/reperfusion impairment. PLoS One 8(9):e74468. https://doi.org/10.1371/journal.pone.0074468
Jiang, T., Shi, M. L., Xia, G., Yang, Y. N., Xu, J. M., Lei, Y. J., Tang, Y. M., and Yang, J. H. 2020. Bone marrow mesenchymal stem cells differentiate into intestinal epithelioid cells through the ERK1/2 pathway. Turkish Journal of Gastroenterology 31(6):459–465. https://doi.org/10.5152/tjg.2020.18644
Jiang, W. and Xu, J. 2020. Immune modulation by mesenchymal stem cells. Cell Proliferation 53(1):e12712. https://doi.org/10.1111/cpr.12712
Juhásová, J., Klíma, J., Martínek, J., Walterová, B., Dolezel, R., Vacková, Z., Kollár, M., and Juhas, S. 2019. Two types of autologous cells in stricture development prevention after complete circular endoscopic dissection in minipig. Rozhledy v chirurgii 98(12):497–508. https://doi.org/10.33699/PIS.2019.98.12.497-508
Kantarcioglu, M., Caliskan, B., Demirci, H., Karacalioglu, O., Kekilli, M., Polat, Z., Gunal, A., Akinci, M., Uysal, C., Eksert, S., Gurel, H., Celebi, G., Avcu, F., Ural, A. U., and Bagci, S. 2014. The efficacy of mesenchymal stem cell transplantation in caustic esophagus injury: an experimental study. Stem Cells International 2014:939674. https://doi.org/10.1155/2014/939674
Kim, I. G., Cho, H., Shin, J., Cho, J. H., Cho, S. W., and Chung, E. J. 2021. Regeneration of irradiation-damaged esophagus by local delivery of mesenchymal stem-cell spheroids encapsulated in a hyaluronic-acid-based hydrogel. Biomaterials Science 9(6):2197–2208. https://doi.org/10.1039/d0bm01655a
Kim, I. G., Wu, Y., Park, S. A., Cho, H., Shin, J. W., and Chung, E. J. 2020a. Tissue-engineered graft for circumferential esophageal reconstruction in rats. Journal of Visualized Experiments (156). https://doi.org/10.3791/60349
Kim, J. E., Fei, L., Yin, W. C., Coquenlorge, S., Rao-Bhatia, A., Zhang, X., Shi, S. S. W., Lee, J. H., Hahn, N. A., Rizvi, W., Kim, K. H., Sung, H. K., Hui, C. C., Guo, G., and Kim, T. H. 2020b. Single cell and genetic analyses reveal conserved populations and signaling mechanisms of gastrointestinal stromal niches. Nature Communications 11(1):334. https://doi.org/10.1038/s41467-019-14058-5
Kim, K., Lee, J., Jang, H., Park, S., Na, J., Myung, J. K., Kim, M. J., Jang, W. S., Lee, S. J., Kim, H., Myung, H., Kang, J., and Shim, S. 2019. Photobiomodulation enhances the angiogenic effect of mesenchymal stem cells to mitigate radiation-induced enteropathy. International Journal of Molecular Sciences 20(5):1131. https://doi.org/10.3390/ijms20051131
Konopljannikov, M. A., Knjazev, O. V., and Baklaushev, V. P. 2021. The use of MSCs for the treatment of inflammatory bowel diseases. Klinicheskaja praktika 12(1):53–65. https://doi.org/10.17816/clinpract64530 (In Russian)
La Francesca, S., Aho, J. M., Barron, M. R., Blanco, E. W., Soliman, S., Kalenjian, L., Hanson, A. D., Todorova, E., Marsh, M., Burnette, K., DerSimonian, H., Odze, R. D., and Wigle, D. A. 2018. Long-term regeneration and remodeling of the pig esophagus after circumferential resection using a retrievable synthetic scaffold carrying autologous cells. Scientific Reports 8(1):4123. https://doi.org/10.1038/s41598-018-22401-x
Lanzoni, G., Alviano, F., Marchionni, C., Bonsi, L., Costa, R., Foroni, L., Roda, G., Belluzzi, A., Caponi, A., Ricci, F., Luigi Tazzari, P., Pagliaro, P., Rizzo, R., Lanza, F., Roberto Baricordi, O., Pasquinelli, G., Roda, E., and Paolo Bagnara, G. 2009. Isolation of stem cell populations with trophic and immunoregulatory functions from human intestinal tissues: potential for cell therapy in inflammatory bowel disease. Cytotherapy 11(8):1020–1031. https://doi.org/10.3109/14653240903253840
Lanzoni, G., Linetsky, E., Correa, D., Messinger Cayetano, S., Alvarez, R. A., Kouroupis, D., Alvarez Gil, A., Poggioli, R., Ruiz, P., Marttos, A. C., Hirani, K., Bell, C. A., Kusack, H., Rafkin, L., Baidal, D., Pastewski, A., Gawri, K., Leñero, C., Mantero, A. M. A., Metalonis, S. W., Wang, X., Roque, L., Masters, B., Kenyon, N. S., Ginzburg, E., Xu, X., Tan, J., Caplan, A. I., Glassberg, M. K., Alejandro, R., and Ricordi, C. 2021. Umbilical cord mesenchymal stem cells for COVID-19 acute respiratory distress syndrome: A double-blind, phase 1/2a, randomized controlled trial. Stem Cells Translational Medicine 10(5):660–673. https://doi.org/10.1002/sctm.20-0472
Lazebnik, L. B., Knjazev, O. V., Konopljanikov, A. G., Parfenov, A. I., Shherbakov, P. L., and Sagynbaeva, V. Je. 2011. Mesenchymal stromal cells in the complex anti-inflammatory therapy of ulcerative colitis. Kletochnaja transplantologija i tkanevaja inzhenerija 6(4):95–103. (In Russian)
Li, W., Zhang, X., Wu, F., Zhou, Y., Bao, Z., Li, H., Zheng, P., and Zhao, S. 2019. Gastric cancer-derived mesenchymal stromal cells trigger M2 macrophage polarization that promotes metastasis and EMT in gastric cancer. Cell Death & Disease 10(12):918. https://doi.org/10.1038/s41419-019-2131-y
Lim, J. Y., Kim, B. S., Ryu, D. B., Kim, T. W., Park, G., and Min, C. K. 2021. The therapeutic efficacy of mesenchymal stromal cells on experimental colitis was improved by the IFN-γ and poly(I:C) priming through promoting the expression of indoleamine 2,3-dioxygenase. Stem Cell Research & Therapy 12(1):37. https://doi.org/10.1186/s13287-020-02087-7
Linard, C., Busson, E., Holler, V., Strup-Perrot, C., Lacave-Lapalun, J. V., Lhomme, B., Prat, M., Devauchelle, P., Sabourin, J. C., Simon, J. M., Bonneau, M., Lataillade, J. J., and Benderitter, M. 2013. Repeated autologous bone marrow-derived mesenchymal stem cell injections improve radiation-induced proctitis in pigs. Stem Cells Translational Medicine 2(11):916–927. https://doi.org/10.5966/sctm.2013-0030
Liu, C. J., Wang, Y. K., Kuo, F. C., Hsu, W. H., Yu, F. J., Hsieh, S., Tai, M. H., Wu, D. C., and Kuo, C. H. 2018. Helicobacter pylori infection-induced hepatoma-derived growth factor regulates the differentiation of human mesenchymal stem cells to myofibroblast-like cells. Cancers 10(12):479. https://doi.org/10.3390/cancers10120479
Liu, L., Chiu, P. W., Lam, P. K., Poon, C. C., Lam, C. C., Ng, E. K., and Lai, P. B. 2015. Effect of local injection of mesenchymal stem cells on healing of sutured gastric perforation in an experimental model. British Journal of Surgery 102(2):e158–e168. https://doi.org/10.1002/bjs.9724
Liu, L., He, Y. R., Liu, S. J., Hu, L., Liang, L. C., Liu, D. L., Liu, L., and Zhu, Z. Q. 2020. Enhanced effect of IL-1β-activated adipose-derived MSCs (ADMSCs) on repair of intestinal ischemia-reperfusion injury via COX-2-PGE2 signaling. Stem Cells International 2020:2803747. https://doi.org/10.1155/2020/2803747
Luo, Y., Wang, B., Liu, J., Ma, F., Luo, D., Zheng, Z., Lu, Q., Zhou, W., Zheng, Y., Zhang, C., Wang, Q., Sha, W., and Chen, H. 2020. Ginsenoside RG1 enhances the paracrine effects of bone marrow-derived mesenchymal stem cells on radiation induced intestinal injury. Aging 13(1):1132–1152. https://doi.org/10.18632/aging.202241
Ma, C., Cong, Y., and Zhang, H. 2020. COVID-19 and the digestive system. American Journal of Gastroenterology 115(7):1003–1006. https://doi.org/10.14309/ajg.0000000000000691
Manieri, N. A., Mack, M. R., Himmelrich, M. D., Worthley, D. L., Hanson, E. M., Eckmann, L., Wang, T. C., and Stappenbeck, T. S. 2015. Mucosally transplanted mesenchymal stem cells stimulate intestinal healing by promoting angiogenesis. Journal of Clinical Investigation 125(9):3606–3618. https://doi.org/10.1172/JCI81423
Markel, T. A., Crafts, T. D., Jensen, A. R., Hunsberger, E. B., and Yoder, M. C. 2015. Human mesenchymal stromal cells decrease mortality after intestinal ischemia and reperfusion injury. Journal of Surgical Research 199(1):56–66. https://doi.org/10.1016/j.jss.2015.06.060
Marzaro, M., Algeri, M., Tomao, L., Tedesco, S., Caldaro, T., Balassone, V., Contini, A. C., Guerra, L., Federici D'Abriola, G., Francalanci, P., Caristo, M. E., Lupoi, L., Boskoski, I., Bozza, A., Astori, G., Pozzato, G., Pozzato, A., Costamagna, G., and Dall'Oglio, L. 2020. Successful muscle regeneration by a homologous microperforated scaffold seeded with autologous mesenchymal stromal cells in a porcine esophageal substitution model. Therapeutic Advances in Gastroenterology 13:1756284820923220. https://doi.org/10.1177/1756284820923220
McCarthy, N., Manieri, E., Storm, E.,E., Saadatpour, A., Luoma, A. M., Kapoor, V. N., Madha, S., Gaynor, L. T., Cox, C., Keerthivasan, S., Wucherpfennig, K., Yuan, G. C., de Sauvage, F. J., Turley, S. J., and Shivdasani, R. A. 2020. Distinct mesenchymal cell populations generate the essential intestinal BMP signaling gradient. Cell Stem Cell 26(3):391–402.e5. https://doi.org/10.1016/j.stem.2020.01.008
McCulloh, C. J., Olson, J. K., Zhou, Y., Wang, Y., and Besner, G. E. 2017. Stem cells and necrotizing enterocolitis: A direct comparison of the efficacy of multiple types of stem cells. Journal of Pediatric Surgery 52(6):999–1005. https://doi.org/10.1016/j.jpedsurg.2017.03.028
Miranda, J. P., Camões, S. P., Gaspar, M. M., Rodrigues, J. S., Carvalheiro, M., Bárcia, R. N., Cruz, P., Cruz, H., Simões, S., and Santos, J. M. 2019. The secretome derived from 3D-cultured umbilical cord tissue MSCs counteracts manifestations typifying rheumatoid arthritis. Frontiers in Immunology 10:18. https://doi.org/10.3389/fimmu.2019.00018
Mizushima, T., Ohnishi, S., Hosono, H., Yamahara, K., Tsuda, M., Shimizu, Y., Kato, M., Asaka, M., and Sakamoto, N. 2017. Oral administration of conditioned medium obtained from mesenchymal stem cell culture prevents subsequent stricture formation after esophageal submucosal dissection in pigs. Gastrointestinal Endoscopy 86(3):542–552.e1. https://doi.org/10.1016/j.gie.2017.01.024
Mona, M., Kobeissy, F., Park, Y. J., Miller, R., Saleh, W., Koh, J., Yoo, M. J., Chen, S., and Cha, S. 2020. Secretome analysis of inductive signals for BM-MSC transdifferentiation into salivary gland progenitors. International Journal of Molecular Sciences 21(23):9055. https://doi.org/10.3390/ijms21239055
Nakatsu, H., Ueno, T., Oga, A., Nakao, M., Nishimura, T., Kobayashi, S., and Oka, M. 2015. Influence of mesenchymal stem cells on stomach tissue engineering using small intestinal submucosa. Journal of Tissue Engineering and Regenerative Medicine 9(3):296–304. https://doi.org/10.1002/term.1794
Ning, X., Zhang, H., Wang, C., and Song, X. 2018. Exosomes released by gastric cancer cells induce transition of pericytes into cancer-associated fibroblasts. Medical Science Monitor 24:2350–2359. https://doi.org/10.12659/msm.906641
Nishikawa, T., Maeda, K., Nakamura, M., Yamamura, T., Sawada, T., Mizutani, Y., Ito, T., Ishikawa, T., Furukawa, K., Ohno, E., Miyahara, R., Kawashima, H., Honda, T., Ishigami, M., Yamamoto, T., Matsumoto, S., Hotta, Y., and Fujishiro, M. 2021. Filtrated adipose tissue-derived mesenchymal stem cell lysate ameliorates experimental acute colitis in mice. Digestive Diseases and Sciences 66(4):1034–1044. https://doi.org/10.1007/s10620-020-06359-3
Numakura, S., Uozaki, H., Kikuchi, Y., Watabe, S., Togashi, A., and Watanabe, M. 2019. Mesenchymal stem cell marker expression in gastric cancer stroma. Anticancer Research 39(1):387–393. https://doi.org/10.21873/anticanres.13124
Okumura, T., Wang, S. S., Takaishi, S., Tu S. P., Ng, V., Ericksen, R. E., Rustgi, A. K., and Wang, T. C. 2009. Identification of a bone marrow-derived mesenchymal progenitor cell subset that can contribute to the gastric epithelium. Laboratory Investigation 89(12):1410–1422. https://doi.org/10.1038/labinvest.2009.88
O'Malley, G., Heijltjes, M., Houston, A. M., Rani, S., Ritter, T., Egan, L. J., and Ryan, A. E. 2016. Mesenchymal stromal cells (MSCs) and colorectal cancer: a troublesome twosome for the anti-tumour immune response? Oncotarget 7(37):60752–60774. https://doi.org/10.18632/oncotarget.11354
Pastuła, A. and Marcinkiewicz, J. 2019. Cellular interactions in the intestinal stem cell niche. Archivum immunologiae et therapiae experimentalis 67(1):19–26. https://doi.org/10.1007/s00005-018-0524-8
Pittenger, M. F., Discher, D. E., Péault, B. M., Phinney, D. G., Hare, J. M., and Caplan, A. I. 2019. Mesenchymal stem cell perspective: cell biology to clinical progress. NPJ Regenerative Medicine 4:22. https://doi.org/10.1038/s41536-019-0083-6
Poggi, A., Varesano, S., and Zocchi, M. R. 2018. How to hit mesenchymal stromal cells and make the tumor microenvironment immunostimulant rather than immunosuppressive. Frontiers in Immunology 9:262. https://doi.org/10.3389/fimmu.2018.00262
Porziella, V., Nachira, D., Boškoski, I., Trivisonno, A., Costamagna, G., and Margaritora, S. 2020. Emulsified stromal vascular fraction tissue grafting: a new frontier in the treatment of esophageal fistulas. Gastrointestinal Endoscopy 92(6):1262–1263. https://doi.org/10.1016/j.gie.2020.06.019
Proskuryakov, S. Y., Konoplyannikov, A. G., Ulyanova, L. P., Logunov, D. Y., Narodicky, B. S., and Gincburg, A. L. 2009. Stem cells of intestinal epithelium. The mechanisms of survival and the role of microbiota. Biochemistry, Supplement Series B: Biomedical Chemistry 3(3):221–236. https://doi.org/10.1134/S1990750809030020
Rager, T. M., Olson, J. K., Zhou, Y., Wang, Y., and Besner, G. E. 2016. Exosomes secreted from bone marrow-derived mesenchymal stem cells protect the intestines from experimental necrotizing enterocolitis. Journal of Pediatric Surgery 51(6):942–947. https://doi.org/10.1016/j.jpedsurg.2016.02.061
Samsonraj, R. M, Raghunath, M., Nurcombe, V., Hui, J. H., van Wijnen, A. J., and Cool, S. M. 2017. Concise review: multifaceted characterization of human mesenchymal stem cells for use in regenerative medicine. Stem Cells Translational Medicine 6(12):2173–2185. https://doi.org/10.1002/sctm.17-0129
Shaker, A., Binkley, J., Darwech, I., Swietlicki, E., McDonald, K., Newberry, R., and Rubin, D. C. 2013. Stromal cells participate in the murine esophageal mucosal injury response. American Journal of Physiology. Gastrointestinal and Liver Physiology 304(7):G662–G672. https://doi.org/10.1152/ajpgi.00225.2012
Shamai, Y., Alperovich, D. C., Yakhini, Z., Skorecki, K., and Tzukerman, M. 2019. Reciprocal reprogramming of cancer cells and associated mesenchymal stem cells in gastric cancer. Stem Cells 37(2):176–189. https://doi.org/10.1002/stem.2942
Shen, Z. Y., Zhang, J., Song, H. L., and Zheng, W. P. 2013. Bone-marrow mesenchymal stem cells reduce rat intestinal ischemia-reperfusion injury, ZO-1 downregulation and tight junction disruption via a TNF-α-regulated mechanism. World Journal of Gastroenterology 19(23):3583–3595. https://doi.org/10.3748/wjg.v19.i23.3583
Shi, X., Chen, Q., and Wang, F. 2019. Mesenchymal stem cells for the treatment of ulcerative colitis: a systematic review and meta-analysis of experimental and clinical studies. Stem Cell Research & Therapy 10(1):266. https://doi.org/10.1186/s13287-019-1336-4
Sigal, M., Reinés, M. D. M., Müllerke, S., Fischer, C., Kapalczynska, M., Berger, H., Bakker, E. R. M., Mollenkopf, H. J., Rothenberg, M. E., Wiedenmann, B., Sauer, S., and Meyer, T. F. 2019. R-spondin-3 induces secretory, antimicrobial Lgr5+ cells in the stomach. Nature Cell Biology 21(7):812–823. https://doi.org/10.1038/s41556-019-0339-9
Signore, M., Cerio, A. M., Boe, A., Pagliuca, A., Zaottini, V., Schiavoni, I., Fedele, G., Petti, S., Navarra, S., Ausiello, C. M., Pelosi, E., Fatica, A., Sorrentino, A., and Valtieri, M. 2012. Identity and ranking of colonic mesenchymal stromal cells. Journal of Cellular Physiology 227(9):3291–3300. https://doi.org/10.1002/jcp.24027
Song, E. M., Jung, S. A., Lee, K. E., Jang, J. Y., Lee, K. H., Tae, C. H., Moon, C. M., Joo, Y. H., Kim, S. E., Jung, H. K., and Shim, K. N. 2017a. The therapeutic efficacy of tonsil-derived mesenchymal stem cells in dextran sulfate sodium-induced acute murine colitis model. Korean Journal of Gastroenterology 69(2):119–128. https://doi.org/10.4166/kjg.2017.69.2.119
Song, W. J., Li, Q., Ryu, M. O., Ahn, J. O., Ha Bhang, D., Chan Jung, Y., and Youn, H. Y. 2017b. TSG-6 secreted by human adipose tissue-derived mesenchymal stem cells ameliorates DSS-induced colitis by inducing M2 macrophage polarization in mice. Scientific Reports 7(1):5187. https://doi.org/10.1038/s41598-017-04766-7
Soontararak, S., Chow, L., Johnson, V., Coy, J., Wheat, W., Regan, D., and Dow, S. 2018. Mesenchymal stem cells (MSC) derived from induced pluripotent stem cells (iPSC) equivalent to adipose-derived MSC in promoting intestinal healing and microbiome normalization in mouse inflammatory bowel disease model. Stem Cells Translational Medicine 7(6):456–467. https://doi.org/10.1002/sctm.17-0305
Sun, L., Huang, C., Zhu, M., Guo, S., Gao, Q., Wang, Q., Chen, B., Li, R., Zhao, Y., Wang, M., Chen, Z., Shen, B., and Zhu, W. 2020. Gastric cancer mesenchymal stem cells regulate PD-L1-CTCF enhancing cancer stem cell-like properties and tumorigenesis. Theranostics 10(26):11950–11962. https://doi.org/10.7150/thno.49717
Takeoka, Y., Matsumoto, K., Taniguchi, D., Tsuchiya, T., Machino, R., Moriyama, M., Oyama, S., Tetsuo, T., Taura, Y., Takagi, K., Yoshida, T., Elgalad, A., Matsuo, N., Kunizaki, M., Tobinaga, S., Nonaka, T., Hidaka, S., Yamasaki, N., Nakayama, K., and Nagayasu, T. 2019. Regeneration of esophagus using a scaffold-free biomimetic structure created with bio-three-dimensional printing. PLoS One 14(3):e0211339. https://doi.org/10.1371/journal.pone.0211339
Tao, Y., Zhu, S., Yang, H., Huang, F., Fu, H., and Tao, X. 2016. Isolation and characterization of putative mesenchymal stem cells from mammalian gut. Cytotechnology 68(6):2753–2759. https://doi.org/10.1007/s10616-016-9992-z
Tayman, C., Uckan, D., Kilic, E., Ulus, A. T., Tonbul, A., Murat Hirfanoglu, I., Helvacioglu, F., Haltas, H., Koseoglu, B., and Tatli, M. M. 2011. Mesenchymal stem cell therapy in necrotizing enterocolitis: a rat study. Pediatric Research 70(5):489–494. https://doi.org/10.1203/PDR.0b013e31822d7ef2
Tolomeo, A. M., Castagliuolo, I., Piccoli, M., Grassi, M., Magarotto, F., De Lazzari, G., Malvicini, R., Caicci, F., Franzin, C., Scarpa, M., Macchi, V., De Caro, R., Angriman, I., Viola, A., Porzionato, A., Pozzobon, M., and Muraca, M. 2021. Extracellular vesicles secreted by mesenchymal stromal cells exert opposite effects to their cells of origin in murine sodium dextran sulfate-induced colitis. Frontiers in Immunology 12:627605. https://doi.org/10.3389/fimmu.2021.627605
Trubicyna, I. E., Onishhenko, N. A., Ljundup, A. V., Knjazev, O. V., Guljaev, A. S., Vasnev, O. S., Abdulatipova, Z. M., Smirnova, A. V., Orlova, Ju. M., and Drozdova, G. A. 2016. Immunomodulatory effect of allogeneic mesenchymal stem cells in rat bone marrow. Jeksperimental'naja i klinicheskaja gastrojenterologija 135(11):59–63. (In Russian)
Tsuda, M., Ohnishi, S., Mizushima, T., Hosono, H., Yamahara, K., Ishikawa, M., Abiko, S., Katsurada, T., Shimizu, Y., and Sakamoto, N. 2018. Preventive effect of mesenchymal stem cell culture supernatant on luminal stricture after endoscopic submucosal dissection in the rectum of pigs. Endoscopy 50(10):1001–1016. https://doi.org/10.1055/a-0584-7262
Usunier, B., Brossard, C., L'Homme, B., Linard, C., Benderitter, M., Milliat, F., and Chapel, A. 2021. HGF and TSG-6 released by mesenchymal stem cells attenuate colon radiation-induced fibrosis. International Journal of Molecular Sciences 22(4):1790. https://doi.org/10.3390/ijms22041790
Van de Putte, D., Demarquay, C., Van Daele, E., Moussa, L., Vanhove, C., Benderitter, M., Ceelen, W., Pattyn, P., and Mathieu, N. 2017. Adipose-derived mesenchymal stromal cells improve the healing of colonic anastomoses following high dose of irradiation through anti-inflammatory and angiogenic processes. Cell Transplantation 26(12):1919–1930. https://doi.org/10.1177/0963689717721515
Wakitani, S., Imoto, K., Yamamoto, T., Saito, M., Murata, N., and Yoneda, M. 2002. Human autologous culture expanded bone marrow mesenchymal cell transplantation for repair of cartilage defects in osteoarthritic knees. Osteoarthritis Cartilage 10(3):199–206. https://doi.org/10.1053/joca.2001.0504
Wang, C., Liu, H., Yang, M., Bai, Y., Ren, H., Zou, Y., Yao, Z., Zhang, B., and Li, Y. 2020a. RNA-Seq based transcriptome analysis of endothelial differentiation of bone marrow mesenchymal stem cells. European Journal of Vascular and Endovascular Surgery 59(5):834–842. https://doi.org/10.1016/j.ejvs.2019.11.003
Wang, F., Maeda, Y., Zachar, V., Ansari, T., and Emmersen, J. 2018a. Regeneration of the oesophageal muscle layer from oesophagus acellular matrix scaffold using adipose-derived stem cells. Biochemical and Biophysical Research Communications 503(1):271–277. https://doi.org/10.1016/j.bbrc.2018.06.014
Wang, H. H., Cui, Y. L., Zaorsky, N. G., Lan, J., Deng, L., Zeng, X. L., Wu, Z. Q., Tao, Z., Guo, W. H., Wang, Q. X., Zhao, L. J., Yuan, Z. Y., Lu, Y., Wang, P., and Meng, M. B. 2016a. Mesenchymal stem cells generate pericytes to promote tumor recurrence via vasculogenesis after stereotactic body radiation therapy. Cancer Letters 375(2):349–359. https://doi.org/10.1016/j.canlet.2016.02.033
Wang, J., Dai, P., Gao, D., Zhang, X., Ruan, C., Li, J., Chen, Y., Zhang, L., and Zhang, Y. 2020b. Genome-wide analysis reveals changes in long noncoding RNAs in the differentiation of canine BMSCs into insulin-producing cells. International Journal of Molecular Sciences 21(15):5549. https://doi.org/10.3390/ijms21155549
Wang, M., Chen, B., Sun, X. X., Zhao, X. D., Zhao, Y. Y., Sun, L., Xu, C. G., Shen, B., Su, Z. L., Xu, W. R., and Zhu, W. 2017. Gastric cancer tissue-derived mesenchymal stem cells impact peripheral blood mononuclear cells via disruption of Treg/Th17 balance to promote gastric cancer progression. Experimental Cell Research 361(1):19–29. https://doi.org/10.1016/j.yexcr.2017.09.036
Wang, M., Liang, C., Hu, H., Zhou, L., Xu, B., Wang, X., Han, Y., Nie, Y., Jia, S., Liang, J., and Wu, K. 2016b. Intraperitoneal injection (IP), Intravenous injection (IV) or anal injection (AI)? Best way for mesenchymal stem cells transplantation for colitis. Scientific Reports 6:30696. https://doi.org/10.1038/srep30696.
Wang, M., Yang, F., Qiu, R., Zhu, M., Zhang, H., Xu, W., Shen, B., and Zhu, W. 2018b. The role of mmu-miR-155-5p-NF-κB signaling in the education of bone marrow-derived mesenchymal stem cells by gastric cancer cells. Cancer Medicine 7(3):856–868. https://doi.org/10.1002/cam4.1355
Wang, S. S., Asfaha, S., Okumura, T., Betz, K. S., Muthupalani, S., Rogers, A. B., Tu, S., Takaishi, S., Jin, G., Yang, X., Wu, D. C., Fox, J. G., and Wang, T. C. 2009. Fibroblastic colony-forming unit bone marrow cells delay progression to gastric dysplasia in a helicobacter model of gastric tumorigenesis. Stem Cells 27(9):2301–2311. https://doi.org/10.1002/stem.165
Wang, S., Miao, Z., Yang, Q., Wang, Y., and Zhang, J. 2018c. The dynamic roles of mesenchymal stem cells in colon cancer. Canadian Journal of Gastroenterology & Hepatology 2018:7628763. https://doi.org/10.1155/2018/7628763
Warnke, P. H., Springer, I. N., Wiltfang, J., Acil, Y., Eufinger, H., Wehmöller, M., Russo, P. A., Bolte, H., Sherry, E., Behrens, E., and Terheyden, H. 2004. Growth and transplantation of a custom vascularised bone graft in a man. Lancet 364(9436):766–770. https://doi.org/10.1016/S0140-6736(04)16935-3
Wu, X., Wu, D., Mu, Y., Zhao, Y., and Ma, Z. 2020. Serum-free medium enhances the therapeutic effects of umbilical cord mesenchymal stromal cells on a murine model for acute colitis. Frontiers in Bioengineering and Biotechnology 8:586. https://doi.org/10.3389/fbioe.2020.00586
Xia, X., Chan, K. F., Wong, G. T. Y., Wang, P., Liu, L., Yeung, B. P. M., Ng, E. K. W., Lau, J. Y. W., and Chiu, P. W. Y. 2019. Mesenchymal stem cells promote healing of nonsteroidal anti-inflammatory drug-related peptic ulcer through paracrine actions in pigs. Science Translational Medicine 11(516):eaat7455. https://doi.org/10.1126/scitranslmed.aat7455
Xia, X., Chiu, P. W. Y., Lam, P. K., Chin, W. C., Ng, E. K. W., and Lau, J. Y. W. 2018. Secretome from hypoxia-conditioned adipose-derived mesenchymal stem cells promotes the healing of gastric mucosal injury in a rodent model. Biochimica et Biophysica Acta — Molecular Basis of Disease 1864(1):178–188. https://doi.org/10.1016/j.bbadis.2017.10.009
Xu, J., Wang, X., Chen, J., Chen, S., Li, Z., Liu, H., Bai, Y., and Zhi, F. 2020. Embryonic stem cell-derived mesenchymal stem cells promote colon epithelial integrity and regeneration by elevating circulating IGF-1 in colitis mice. Theranostics 10(26):12204–12222. https://doi.org/10.7150/thno.47683
Xu, X., Zhang, X., Wang, S., Qian, H., Zhu, W., Cao, H., Wang, M., Chen, Y., and Xu, W. 2011. Isolation and comparison of mesenchymal stem-like cells from human gastric cancer and adjacent non-cancerous tissues. Journal of Cancer Research and Clinical Oncology 137(3):495–504. https://doi.org/10.1007/s00432-010-0908-6
Xue, X., Yan, Y., Ma, Y., Yuan, Y., Li, C., Lang, X., Xu, Z., Chen, H., and Zhang, H. 2019. Stem-cell therapy for esophageal anastomotic leakage by autografting stromal cells in fibrin scaffold. Stem Cells Translational Medicine 8(6):548–556. https://doi.org/10.1002/sctm.18-0137
Yang, L., Liu, Z., Chen, C., Cong, X., Li, Z., Zhao, S., and Ren, M. 2017. Low-dose radiation modulates human mesenchymal stem cell proliferation through regulating CDK and Rb. American Journal of Translational Research 9(4):1914–1921.
Yang, S., Liang, X., Song, J., Li, C., Liu, A., Luo, Y., Ma, H., Tan, Y., and Zhang, X. 2021. A novel therapeutic approach for inflammatory bowel disease by exosomes derived from human umbilical cord mesenchymal stem cells to repair intestinal barrier via TSG-6. Stem Cell Research & Therapy 12(1):315. https://doi.org/10.1186/s13287-021-02404-8
Yang, T., Zhang, X., Wang, M., Zhang, J., Huang, F., Cai, J., Zhang, Q., Mao, F., Zhu, W., Qian, H., and Xu, W. 2014. Activation of mesenchymal stem cells by macrophages prompts human gastric cancer growth through NF-κB pathway. PLoS One 9(5):e97569. https://doi.org/10.1371/journal.pone.0097569
Ye, L., Sun, L. X., Wu, M. H., Wang, J., Ding, X., Shi, H., Lu, S. L., Wu, L., Wei, J., Li, L., and Wang, Y. F. 2018. A simple system for differentiation of functional intestinal stem cell-like cells from bone marrow mesenchymal stem cells. Molecular Therapy — Nucleic Acids 13:110–120. https://doi.org/10.1016/j.omtn.2018.08.017
Yeh, Y. T., Wei, J., Thorossian, S., Nguyen, K., Hoffman, C., Del Álamo, J. C., Serrano, R., Li, Y. J., Wang, K. C., and Chien, S. 2019. MiR-145 mediates cell morphology-regulated mesenchymal stem cell differentiation to smooth muscle cells. Biomaterials 204:59–69. https://doi.org/10.1016/j.biomaterials.2019.03.003
Yilmaz, R., Adas, G., Cukurova, Z., Kart Yasar, K., Isiksacan, N., Oztel, O. N., and Karaoz, E. 2020. Mesenchymal stem cells treatment in COVID-19 patient with multi-organ involvement. Bratislavske Lekarske Listy 121(12):847–852. https://doi.org/10.4149/BLL_2020_139
Yin, L., Zhang, R., Hu, Y., Li, W., Wang, M., Liang, Z., Sun, Z., Ji, R., Xu, W., and Qian, H. 2020. Gastric-cancer-derived mesenchymal stem cells: a promising target for resveratrol in the suppression of gastric cancer metastasis. Human Cell 33(3):652–662. https://doi.org/10.1007/s13577-020-00339-5
Yoshida, S., Tomokiyo, A., Hasegawa, D., Hamano, S., Sugii, H., and Maeda, H. 2020. Insight into the role of dental pulp stem cells in regenerative therapy. Biology 9(7):160. https://doi.org/10.3390/biology9070160
Yu, J., Cao, H., Yang, J., Pan, Q., Ma, J., Li, J., Li, Y., Li, J., Wang, Y., and Li, L. 2012. In vivo hepatic differentiation of mesenchymal stem cells from human umbilical cord blood after transplantation into mice with liver injury. Biochemical and Biophysical Research Communications 422(4):539–545. https://doi.org/10.1016/j.bbrc.2012.04.156
Zhang, J., Lu, S., Liu, X., Song, B., and Shi, L. 2018. Umbilical cord mesenchymal stem cell treatment for Crohn's disease: a randomized controlled clinical trial. Gut Liver 12(1):73–78. https://doi.org/10.5009/gnl17035
Zhang, Y., Babczyk, P., Pansky, A., Kassack, M. U., and Tobiasch, E. 2020. P2 Receptors influence hMSCs differentiation towards endothelial cell and smooth muscle cell lineages. International Journal of Molecular Sciences 21(17):6210. https://doi.org/10.3390/ijms21176210
Zheng, X. B., He, X. W., Zhang, L. J., Qin, H. B., Lin, X. T., Liu, X. H., Zhou, C., Liu, H. S., Hu, T., Cheng, H. C., He, X. S., Wu, X. R., Chen, Y. F., Ke, J., Wu, X. J., and Lan P. 2019. Bone marrow-derived CXCR4-overexpressing MSCs display increased homing to intestine and ameliorate colitis-associated tumorigenesis in mice. Gastroenterology Report 7(2):127–138. https://doi.org/10.1093/gastro/goy017
Zhou, W., Lin, J., Zhao, K., Jin, K., He, Q., Hu, Y., Feng, G., Cai, Y., Xia, C., Liu, H., Shen, W., Hu, X., and Ouyang, H. 2019. Single-cell profiles and clinically useful properties of human mesenchymal stem cells of adipose and bone marrow origin. American Journal of Sports Medicine 47(7):1722–1733. https://doi.org/10.1177/0363546519848678
Downloads
Published
2022-10-10
How to Cite
Payushina, O., Tsomartova, D., Chereshneva, Y., Ivanova, M., Pashina, N., Tsomartova, E., & Kuznetsov, S. (2022). New perspectives on treatment of gastrointestinal diseases: therapeutic potential of mesenchymal stromal cells. Biological Communications, 67(3), 217–230. https://doi.org/10.21638/spbu03.2022.307
License
Articles of Biological Communications are open access distributed under the terms of the License Agreement with Saint Petersburg State University, which permits to the authors unrestricted distribution and self-archiving free of charge.
