137
Views
0
CrossRef citations to date
0
Altmetric
Original Research

Phenotypic and Functional Responses of Human Decidua Basalis Mesenchymal Stem/Stromal Cells to Lipopolysaccharide of Gram-Negative Bacteria

, ORCID Icon, & ORCID Icon
Pages 51-69 | Published online: 02 Nov 2021

References

  • Shin JH, Ryu CM, Yu HY, Shin DM, Choo MS. Current and future directions of stem cell therapy for bladder dysfunction. Stem Cell Rev Rep. 2020;16(1):82–93.
  • Bae SH. Recent achievements in stem cell therapy for pediatric gastrointestinal tract disease. Pediatr Gastroenterol Hepatol Nutr. 2013;16(1):10–16. doi:10.5223/pghn.2013.16.1.10
  • Quante M, Wang TC. Stem cells in gastroenterology and hepatology. Nat Rev Gastroenterol Hepatol. 2009;6(12):724. doi:10.1038/nrgastro.2009.195
  • Van Der Flier LG, Clevers H. Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu Rev Physiol. 2009;71:241–260. doi:10.1146/annurev.physiol.010908.163145
  • Ratajczak M, Suszynskan M, Pedziwiatr D, Mierzejewska K, Greco N. Umbilical cord blood-derived very small embryonic like stem cells (VSELs) as a source of pluripotent stem cells for regenerative medicine. Pediatr Endocrinol Rev. 2012;9(3):639–643.
  • Chu DT, Nguyen TT, Tien NLB, et al. Recent progress of stem cell therapy in cancer treatment: molecular mechanisms and potential applications. Cells. 2020;9(3):563. doi:10.3390/cells9030563
  • Ghafarzadeh M, Namdari P, Tarhani M, Tarhani F. A review of application of stem cell therapy in the management of Congenital Heart Disease. J Matern Fetal Neonatal Med. 2020;33(9):1607–1615.
  • Heo JS, Choi Y, Kim HS, Kim HO. Comparison of molecular profiles of human mesenchymal stem cells derived from bone marrow, umbilical cord blood, placenta and adipose tissue. Int J Mol Med. 2015;37:115–125. doi:10.3892/ijmm.2015.2413
  • Elahi KC, Klein G, Avci-Adali M, Sievert KD, Macneil S, Aicher WK. Human mesenchymal stromal cells from different sources diverge in their expression of cell surface proteins and display distinct differentiation patterns. Stem Cells Int. 2016;2016:1–9. doi:10.1155/2016/5646384
  • Nancarrow-Lei R, Mafi P, Mafi R, Khan W. A systemic review of adult mesenchymal stem cell sources and their multilineage differentiation potential relevant to musculoskeletal tissue repair and regeneration. Curr Stem Cell Res. 2017;12:601–610.
  • Olson TS, Ley K. Chemokines and chemokine receptors in leukocyte trafficking. Am J Physiol Regul Integr Comp Physiol. 2002;283(1):R7–R28. doi:10.1152/ajpregu.00738.2001
  • Gnecchi M, Zhang Z, Ni A, Dzau VJ. Paracrine mechanisms in adult stem cell signaling and therapy. Circ Res. 2008;103(11):1204–1219. doi:10.1161/CIRCRESAHA.108.176826
  • Meirelles LDS, Chagastelles PC, Nardi NB. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J Cell Sci. 2006;119:2204–2213. doi:10.1242/jcs.02932
  • Chen K, Wang D, Du WT, et al. Human umbilical cord mesenchymal stem cells hUC-MSCs exert immunosuppressive activities through a PGE2-dependent mechanism. Clin Immunol. 2010;135:448–458. doi:10.1016/j.clim.2010.01.015
  • Nitzsche F, Müller C, Lukomska B, Jolkkonen J, Deten A, Boltze J. Concise review: MSC adhesion cascade—insights into homing and transendothelial migration. Stem Cells. 2017;35:1446–1460. doi:10.1002/stem.2614
  • Friedenstein AJ, Chailakhjan RK, Lalykina KS. The development of fibroblast colonies in monolayer cultures of Guinea pig bone marrow and spleen cells. Cell Prolif. 1970;3:393–403. doi:10.1111/j.1365-2184.1970.tb00347.x
  • Wagers AJ, Weissman IL. Plasticity of adult stem cells. Cell. 2004;116(5):639–648. doi:10.1016/S0092-8674(04)00208-9
  • Bianco P, Cao X, Frenette PS, et al. The meaning, the sense and the significance: translating the science of mesenchymal stem cells into medicine. Nat Med. 2013;19(1):35–42. doi:10.1038/nm.3028
  • Abomaray FM, Al Jumah MA, Alsaad KO, et al. Phenotypic and functional characterization of mesenchymal stem/multipotent stromal cells from decidua basalis of human term placenta. Stem Cells Int. 2016;2016:1–18. doi:10.1155/2016/5184601
  • Ding DC, Shyu WC, Lin SZ. Mesenchymal stem cells. Cell Transplant. 2011;20(1):5–14. doi:10.3727/096368910X
  • Huang YC, Yang ZM, Chen XH, et al. Isolation of mesenchymal stem cells from human placental decidua basalis and resistance to hypoxia and serum deprivation. Stem Cell Rev. 2009;5:247–255. doi:10.1007/s12015-009-9069-x
  • Kusuma GD, Abumaree MH, Pertile MD, Perkins AV, Brennecke SP, Kalionis B. Mesenchymal stem/stromal cells derived from a reproductive tissue niche under oxidative stress have high aldehyde dehydrogenase activity. Stem Cell Rev Rep. 2016;12(3):285–297. doi:10.1007/s12015-016-9649-5
  • Alshabibi MA, Khatlani T, Abomaray FM, et al. Human decidua basalis mesenchymal stem/stromal cells protect endothelial cell functions from oxidative stress induced by hydrogen peroxide and monocytes. Stem Cell Res Ther. 2018;9(1). doi:10.1186/s13287-018-1021-z
  • Khatlani T, Algudiri D, Alenzi R, et al. Preconditioning by hydrogen peroxide enhances multiple properties of human decidua basalis mesenchymal stem/multipotent stromal cells. Stem Cells Int. 2018;2018:1–13. doi:10.1155/2018/6480793
  • Alshabibi MA, Al Huqail AJ, Khatlani T, et al. Mesenchymal stem/multipotent stromal cells from human decidua basalis reduce endothelial cell activation. Stem Cells Dev. 2017;26:1355–1373. doi:10.1089/scd.2017.0096
  • De Nardin E. The role of inflammatory and immunological mediators in periodontitis and cardiovascular disease. Ann Periodontol. 2001;6:30–40. doi:10.1902/annals.2001.6.1.30
  • Kuramitsu HK, Kang IC, Qi M. Interactions of Porphyromonas gingivalis with host cells: implications for cardiovascular diseases. J Periodontol. 2003;74:85–89. doi:10.1902/jop.2003.74.1.85
  • Li L, Messas E, Batista EL Jr, Levine RA, Amar S. Porphyromonas gingivalis infection accelerates the progression of atherosclerosis in a heterozygous apolipoprotein E-deficient murine model. Circulation. 2002;105:861–867. doi:10.1161/hc0702.104178
  • Horseman MA, Surani S, Bowman JD. Endotoxin, toll-like receptor-4, and atherosclerotic heart disease. Curr Cardiol Rev. 2017;13(2):81–93.
  • Nikaido H. Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev. 2003;67:593–656.
  • Rietschel ET, Kirikae T, Schade FU, et al. Bacterial endotoxin: molecular relationships of structure to activity and function. FASEB J. 1994;8:217–225. doi:10.1096/fasebj.8.2.8119492
  • Raetz CR, Whitfield C. Lipopolysaccharide endotoxins. Annu Rev Biochem. 2002;71:635–700. doi:10.1146/annurev.biochem.71.110601.135414
  • Goto T, Eden S, Nordenstam G, Sundh V, Svanborg-Eden C, Mattsby-Baltzer I. Endotoxin levels in sera of elderly individuals. Clin Diagn Lab Immunol. 1994;1:684–688. doi:10.1128/cdli.1.6.684-688.1994
  • Niebauer J, Volk HD, Kemp M, et al. Endotoxin and immune activation in chronic heart failure: a prospective cohort study. Lancet. 1999;353:1838–1842. doi:10.1016/S0140-6736(98)09286-1
  • Wiedermann CJ, Kiechl S, Dunzendorfer S, et al. Association of endotoxemia with carotid atherosclerosis and cardiovascular disease: prospective results from the Bruneck Study. J Am Coll Cardiol. 1999;34:1975–1981. doi:10.1016/S0735-1097(99)00448-9
  • Kiechl S, Egger G, Mayr M, et al. Chronic infections and the risk of carotid atherosclerosis: prospective results from a large population study. Circulation. 2001;103(8):1064–1070. doi:10.1161/01.CIR.103.8.1064
  • Cani PD, Amar J, Iglesias MA. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes. 2007;56(7):1761–1772. doi:10.2337/db06-1491
  • Applebaum KM, Ray RM, Astrakianakis G. Evidence of a paradoxical relationship between endotoxin and lung cancer after accounting for left truncation in a study of Chinese female textile workers. Occup Environ Med. 2013;70(10):709–715. doi:10.1136/oemed-2012-101240
  • Jeon D, Kim SJ, Kim HS. Anti-inflammatory evaluation of the methanolic extract of Taraxacum officinale in LPS-stimulated human umbilical vein endothelial cells. BMC Complement Altern Med. 2017;17(1). doi:10.1186/s12906-017-2022-7
  • Ross R. Atherosclerosis–an inflammatory disease. N Engl J Med. 1999;340(2):115–126. doi:10.1056/NEJM199901143400207
  • Libby P. Inflammation in atherosclerosis. Arterioscler Thromb Vasc Biol. 2012;32(9):2045–2051. doi:10.1161/ATVBAHA.108.179705
  • Pfeffer R, Ganatos P, Nir A, Weinbaum S. Diffusion of macromolecules across the arterial wall in the presence of multiple endothelial injuries. J Biomech Eng. 1981;103:197–203. doi:10.1115/1.3138278
  • Stoll LL, Denning GM, Weintraub NL. Potential role of endotoxin as a proinflammatory mediator of atherosclerosis. Arterioscler Thromb Vasc Biol. 2004;24:2227–2236. doi:10.1161/01.ATV.0000147534.69062.dc
  • Weinbaum S, Tzeghai G, Ganatos P, Pfeffer R, Chien S. Effect of cell turnover and leaky junctions on arterial macromolecular transport. Am J Physiol. 1985;248:H945–960.
  • Lehr HA, Sagban TA, Ihling C, et al. Immunopathogenesis of atherosclerosis: endotoxin accelerates atherosclerosis in rabbits on hypercholesterolemic diet. Circulation. 2001;104:914–920. doi:10.1161/hc3401.093153
  • Ostos MA, Recalde D, Zakin MM, Scott-Algara D. Implication of natural killer T cells in atherosclerosis development during a LPS-induced chronic inflammation. FEBS Lett. 2002;519:23–29. doi:10.1016/S0014-5793(02)02692-3
  • Rice JB, Stoll LL, Li WG, et al. Low-level endotoxin induces potent inflammatory activation of human blood vessels: inhibition by statins. Arterioscler Thromb Vasc Biol. 2003;23:1576–1582. doi:10.1161/01.ATV.0000081741.38087.F9
  • Ghanim H, Sia CL, Upadhyay M, et al. Orange juice neutralizes the proinflammatory effect of a high-fat, high-carbohydrate meal and prevents endotoxin increase and Toll-like receptor expression. Am J Clin Nutr. 2010;91(4):940–949. doi:10.3945/ajcn.2009.28584
  • Laugerette FC, Vors A, Geloen A. Emulsified lipids increase endotoxemia: possible role in early postprandial low-grade inflammation. J Nutr Biochem. 2011;22(1):53–59. doi:10.1016/j.jnutbio.2009.11.011
  • Abumaree MH, Abomaray FM, Alshabibi MA, AlAskar AS, Kalionis B. Immunomodulatory properties of human placental mesenchymal stem/ stromal cells. Placenta. 2017;59:87–95. doi:10.1016/j.placenta.2017.04.003
  • Abumaree MH, Hakami M, Abomaray FM, et al. Human chorionic villous mesenchymal stem/stromal cells modify the effects of oxidative stress on endothelial cell functions. Placenta. 2017;59:74–86. doi:10.1016/j.placenta.2017.05.001
  • Basmaeil YS, Al Subayyil AM, Khatlani T, et al. Human chorionic villous mesenchymal stem/stromal cells protect endothelial cells from injury induced by high level of glucose. Stem Cell Res Ther. 2018;9:238. doi:10.1186/s13287-018-0984-0
  • Uccelli A, Moretta L, Pistoia V. Mesenchymal stem cells in health and disease. Nat Rev Immunol. 2008;8:726–736. doi:10.1038/nri2395
  • Wei X, Yang X, Han ZP, Qu FF, Shao L, Shi YF. Mesenchymal stem cells: a new trend for cell therapy. Acta Pharmacol Sin. 2013;34:747–754. doi:10.1038/aps.2013.50
  • Squillaro T, Peluso G, Galderisi U. Clinical trials with mesenchymal stem cells: an update. Cell Transplant. 2016;25:829–848. doi:10.3727/096368915X689622
  • Lee KD, Kuo TK, Whang-Peng J, et al. In vitro hepatic differentiation of human mesenchymal stem cells. Hepatology. 2004;40(6):1275–1284. doi:10.1002/hep.20469
  • Paunescu V, Deak E, Herman D, Siska IR, Tanasie G, Bunu C. In vitro differentiation of human mesenchymal stem cells to epithelial lineage. J Cell Mol Med. 2007;11:502–508. doi:10.1111/j.1582-4934.2007.00041.x
  • Quevedo HC, Hatzistergos KE, Oskouei BN, Feigenbaum GS, Rodriguez JE, Valdes D. Allogeneic mesenchymal stem cells restore cardiac function in chronic ischemic cardiomyopathy via trilineage differentiating capacity. Proc Natl Acad Sci. 2009;106:14022–14027. doi:10.1073/pnas.0903201106
  • Friedenstein AJ, Piatetzky-Shapiro II, Petrakova KV. Osteogenesis in transplants of bone marrow cells. J Embryol Exp Morphol. 1966;16:381–390.
  • Ullah I, Subbarao RB, Rho GJ. Human mesenchymal stem cells—current trends and future prospective. Biosci Rep. 2015;28:35.
  • Salgado AJ, Reis RL, Sousa NJ, Gimble JM. Adipose tissue derived stem cells secretome: soluble factors and their roles in regenerative medicine. Curr Stem Cell Res Ther. 2010;5:103–110. doi:10.2174/157488810791268564
  • Jimenez-Puerta GJ, Marchal JA, López-Ruiz E, Gálvez-Martín P. Role of mesenchymal stromal cells as therapeutic agents: potential mechanisms of action and implications in their clinical use. J Clin Med. 2020;9(2):445th ser. doi:10.3390/jcm9020445
  • Kot M, Musiał-Wysocka A, Lasota M, Ulman A, Majka M. Secretion, migration and adhesion as key processes in the therapeutic activity of mesenchymal stem cells. Acta Biochim Pol. 2019;66(4):499–507.
  • Sotiropoulou PA, Perez SA, Salagianni M, Baxevanis CN, Papamichail M. Characterization of the optimal culture conditions for clinical scale production of human mesenchymal stem cells. Stem Cells. 2006;24:462–471. doi:10.1634/stemcells.2004-0331
  • Lee KA, Shim W, Paik MJ, et al. Analysis of changes in the viability and gene expression profiles of human mesenchymal stromal cells over time. Cytotherapy. 2009;11(6):688–697. doi:10.3109/14653240902974032
  • Schoeberlein A, Mueller M, Reinhart U, Sager R, Messerli M, Surbek DV. Homing of placenta-derived mesenchymal stem cells after perinatal intracerebral transplantation in a rat model. Am J Obstet Gynecol. 2011;205(277):e1–e6. doi:10.1016/j.ajog.2011.06.044
  • Fossett E, Khan W. Optimising human mesenchymal stem cell numbers for clinical application: a literature review. Stem Cells Int. 2012;2012:1–5. doi:10.1155/2012/465259
  • Francois S, Mouiseddine M, Allenet-Lepage B. Human mesenchymal stem cells provide protection against radiation-induced liver injury by antioxidative process, vasculature protection, hepatocyte differentiation, and trophic effects. Biomed Res Int. 2013;2013:1–14. doi:10.1155/2013/151679
  • Halabian R, Tehrani HA, Jahanian-Najafabadi A, Roudkenar MH. Lipocalin-2-mediated upregulation of various antioxidants and growth factors protects bone marrow derived mesenchymal stem cells against unfavorable microenvironments. Cell Stress Chaperones. 2013;18:785–800. doi:10.1007/s12192-013-0430-2
  • Han SM, Han SH, Coh YR. Enhanced proliferation and differentiation of Oct4-and Sox2-overexpressing hu man adipose tissue mesenchymal stem cells. Exp Mol Med. 2014;46:e101. doi:10.1038/emm.2014.28
  • Amiri F, Jahanian-Najafabadi A, Roudkenar MH. In vitro augmentation of mesenchymal stem cells viability in stressful microenvironments. Cell Stress Chaperones. 2015;20:237–251. doi:10.1007/s12192-014-0560-1
  • Hagberg H, Mallard C, Ferriero DM. The role of inflammation in perinatal brain injury. Nat Rev Neurol. 2015;11:192. doi:10.1038/nrneurol.2015.13
  • Mueller M, Wolfs TG, Schoeberlein A, Gavilanes AW, Surbek D, Kramer BW. Mesenchymal stem/ stromal cells—a key mediator for regeneration after perinatal morbidity. Mol Cell Pediatr. 2016;3:6. doi:10.1186/s40348-016-0034-x
  • Raijmakers MT, Roes EM, Poston L, Steegers EA, Peters WH. The transient increase of oxidative stress during normal pregnancy is higher and persists after delivery in women with pre-eclampsia. Eur J Obstet Gynecol Reprod Biol. 2008;138(1):39–44. doi:10.1016/j.ejogrb.2007.08.005
  • Ashok A, Nabil A, Botros R. Studies on Women’s Health: Oxidative Stress in Applied Basic Research and Clinical Practice. Agarwal A, Aziz N, Rizk B, editors. New York: Humana Press; 2013.
  • Basmaeil Y, Rashid MA, Khatlani T, et al. Preconditioning of human decidua basalis mesenchymal stem/stromal cells with glucose increased their engraftment and anti-diabetic properties. Tissue Eng Regen Med. 2020;17(2):209.
  • Dominici M, Le Blanc K, Mueller I, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8(4):315–317.
  • Peterson KM, Aly A, Lerman A, Lerman LO, Rodriguez-Porcel M. Improved survival of mesenchymal stromal cell after hypoxia preconditioning: role of oxidative stress. Life Sci. 2011;88(1–2):65–73. doi:10.1016/j.lfs.2010.10.023
  • Lai P, Li T, Yang J, et al. Upregulation of stromal cell-derived factor 1 (SDF-1) expression in microvasculature endothelial cells in retinal ischemia-reperfusion injury. Graefes Arch Clin Exp Ophthalmol. 2008;246(12):1707–1713. doi:10.1007/s00417-008-0907-3
  • Richmond A. Chemokine modulation of the tumor microenvironment. Pigment Cell Melanoma Res. 2010;23(3):312–313. doi:10.1111/j.1755-148X.2010.00714.x
  • Silva LHA, Antunes MA, Dos Santos CC, Weiss DJ, Cruz FF, Rocco PRM. Strategies to improve the therapeutic effects of mesenchymal stromal cells in respiratory diseases. Stem Cell Res Ther. 2018;9(1):45. doi:10.1186/s13287-018-0802-8
  • Zhao L, Hu C, Han F, Cai F, Wang J, Chen J. Preconditioning is an effective strategy for improving the efficiency of mesenchymal stem cells in kidney transplantation. Stem Cell Res Ther. 2020;11(1):197. doi:10.1186/s13287-020-01721-8
  • Kurte M, Vega-Letter AM, Luz-Crawford P, et al. Time-dependent LPS exposure commands MSC immunoplasticity through TLR4 activation leading to opposite therapeutic outcome in EAE. Stem Cell Res Ther. 2020;11(1). doi:10.1186/s13287-020-01840-2
  • Durand N, Russell A, Zubair AC. Effect of comedications and endotoxins on mesenchymal stem cell secretomes, migratory and immunomodulatory capacity. J Clin Med. 2019;8(4):497. doi:10.3390/jcm8040497
  • Goswami R, Kaplan MH. A brief history of IL-9. J Immunol. 2011;186:3283–3288. doi:10.4049/jimmunol.1003049
  • Sun Y, Liu S, Hu R, Zhou Q, Li X. Decreased placental IL9 and IL9R in preeclampsia impair trophoblast cell proliferation, invasion, and angiogenesis. Hypertens Pregnancy. 2020;39(3):228–235.
  • Bigildeev AE, Zezina EA, Shipounova IN, Drize NJ. Interleukin-1 beta enhances human multipotent mesenchymal stromal cell proliferative potential and their ability to maintain hematopoietic precursor cells. Cytokine. 2015;71(2):246–254. doi:10.1016/j.cyto.2014.10.018
  • Matsumura E, Tsuji K, Komori K, Koga H, Sekiya I, Muneta T. Pretreatment with IL-1β enhances proliferation and chondrogenic potential of synovium-derived mesenchymal stem cells. Cytotherapy. 2017;19(2):181–193. doi:10.1016/j.jcyt.2016.11.004
  • Amann EM, Groß A, Rojewski MT, et al. Inflammatory response of mesenchymal stromal cells after in vivo exposure with selected trauma-related factors and polytrauma serum. PLoS One. 2019;14(5):e0216862. doi:10.1371/journal.pone.0216862
  • Cui TX, Brady AE, Fulton CT, et al. CCR2 mediates chronic LPS-induced pulmonary inflammation and hypoalveolarization in a murine model of bronchopulmonary dysplasia. Front Immunol. 2020;11. doi:10.3389/fimmu.2020.579628
  • Wynn RF, Hart CA, Corradi-Perini C, O’Neill L, Evans CA, Wraith JE. A small proportion of mesenchymal stem cells strongly expresses functionally active CXCR4 receptor capable of promoting migration to bone marrow. Blood. 2004;104:2643–2645. doi:10.1182/blood-2004-02-0526
  • Sordi V, Malosio ML, Marchesi F, Mercalli A, Melzi R, Giordano T. Bone marrow mesenchymal stem cells express a restricted set of functionally active chemokine receptors capable of promoting migration to pancreatic islets. Blood. 2005;106:419–427. doi:10.1182/blood-2004-09-3507
  • Honczarenko M, Le Y, Swierkowski M, Ghiran I, Glodek AM, Silberstein LE. Human bone marrow stromal cells express a distinct set of biologically functional chemokine receptors. Stem Cells. 2005;24:1030–1041. doi:10.1634/stemcells.2005-0319
  • Von Luttichau I, Notohamiprodjo M, Wechselberger A, Peters C, Henger A, Seliger C. Human adult CD34- progenitor cells functionally express the chemokine receptors CCR1, CCR4, CCR7, CXCR5, and CCR10 but not CXCR4. Stem Cells Dev. 2005;14:329–336. doi:10.1089/scd.2005.14.329
  • Ringe J, Strassburg S, Neumann K, Endres M, Notter M, Burmester GR. Towards in situ tissue repair: human mesenchymal stem cells express chemokine receptors CXCR1. CXCR2 and CCR2, and migrate upon stimulation with CXCL8 but not CCL2. J Cell Biochem. 2007;101:135–146. doi:10.1002/jcb.21172
  • Ma J, Liu N, Yi B, Zhang X, Gao BB, Zhang Y. Transplanted hUCB-MSCs migrated to the damaged area by SDF-1/CXCR4 signaling to promote functional recovery after traumatic brain injury in rats. Neurol Res. 2015;37:50–56. doi:10.1179/1743132814Y.0000000399
  • Wobus M, List C, Dittrich T, Dhawan A, Duryagina R, Arabanian LS. Breast carcinoma cells modulate the chemoattractive activity of human bone marrow-derived mesenchymal stromal cells by interfering with CXCL12. Int J Cancer. 2014;136:44–54. doi:10.1002/ijc.28960
  • Shen Z, Wang J, Huang Q, et al. Genetic modification to induce CXCR2 overexpression in mesenchymal stem cells enhances treatment benefits in radiation-induced oral mucositis. Cell Death Dis. 2018;9(2). doi:10.1038/s41419-018-0310-x
  • Meirelles LDS, Fontes AM, Covas DT, Caplan AI. Mechanisms involved in the therapeutic properties of mesenchymal stem cells. Cytokine Growth Factor Rev. 2009;20:419–427. doi:10.1016/j.cytogfr.2009.10.002
  • Escacena N, Quesada-Hernandez E, Capilla-Gonzalez V, Soria B, Hmadcha A. Bottlenecks in the efficient use of advanced therapy medicinal products based on mesenchymal stromal cells. Stem Cells Int. 2015;2015:895714.
  • Hmadcha A, Martin-Montalvo A, Gauthier BR, Soria B, Capilla-Gonzalez V. Therapeutic potential of mesenchymal stem cells for cancer therapy. Front Bioeng Biotechnol. 2020;8. doi:10.3389/fbioe.2020.00043
  • Di Nicola M, Carlo-Stella C, Magni M, et al. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood. 2002;99:3838–3843. doi:10.1182/blood.V99.10.3838
  • Nauta AJ, Kruisselbrink AB, Lurvink E, Willemze R, Fibbe WE. Mesenchymal stem cells inhibit generation and function of both CD34+-derived and monocyte-derived dendritic cells. J Immunol. 2006;177:2080–2087. doi:10.4049/jimmunol.177.4.2080
  • Nemeth K, Keane-Myers A, Brown JM, et al. Bone marrow stromal cells use TGF-beta to suppress allergic responses in a mouse model of ragweed-induced asthma. Proc Natl Acad Sci. 2010;107:5652–5657. doi:10.1073/pnas.0910720107
  • Du-Rocher B, Binato R, de-freitas-junior JCM, et al. IL-17 triggers invasive and migratory properties in human MSCs, while IFNγ favors their immunosuppressive capabilities: implications for the “licensing” process. Stem Cell Rev Rep. 2020;16(6):1266–1279. doi:10.1007/s12015-020-10051-4
  • Albanesi C, Cavani A, Girolomoni G. IL-17 is produced by nickel-specific T lymphocytes and regulates ICAM-1 expression and chemokine production in human keratinocytes: synergistic or antagonist effects with IFN-gamma and TNF-alpha. J Immunol. 1999;162(1):494–502.
  • Eid RE, Rao DA, Zhou J, et al. Interleukin-17 and interferon-γ are produced concomitantly by human coronary artery-infiltrating T cells and act synergistically on vascular smooth muscle cells. Circulation. 2009;119(10):1424–1432. doi:10.1161/CIRCULATIONAHA.108.827618
  • Bulek K, Liu C, Swaidani S, et al. The inducible kinase IKKi is required for IL-17-dependent signaling associated with neutrophilia and pulmonary inflammation. Nat Immunol. 2011;12(9):844–852. doi:10.1038/ni.2080
  • Gabr MA, Jing L, Helbling AR, et al. Interleukin-17 synergizes with IFNγ or TNFα to promote inflammatory mediator release and intercellular adhesion molecule-1 (ICAM-1) expression in human intervertebral disc cells. J Orthop Res. 2011;29(1):1–7. doi:10.1002/jor.21206
  • Ekström K, Omar O, Granéli C, Wang X, Vazirisani F, Thomsen P. Monocyte exosomes stimulate the osteogenic gene expression of mesenchymal stem cells. PLoS One. 2013;8(9):e75227. doi:10.1371/journal.pone.0075227
  • Kang Q, Song WX, Luo Q, et al. A comprehensive analysis of the dual roles of BMPs in regulating adipogenic and osteogenic differentiation of mesenchymal progenitor cells. Stem Cells Dev. 2009;18(4):545–559. doi:10.1089/scd.2008.0130
  • Chen G, Deng C, Li YP. TGF-beta and BMP signaling in osteoblast differentiation and bone formation. Int J Biol Sci. 2012;8:272–288. doi:10.7150/ijbs.2929