Impact of Three Different Serum Sources on Functional Properties of Equine Mesenchymal Stromal Cells.
Abstract: Culture and expansion of equine mesenchymal stromal cells (MSCs) are routinely performed using fetal bovine serum (FBS) as a source of growth factors, nutrients, and extracellular matrix proteins. However, the desire to minimize introduction of xenogeneic bovine proteins or pathogens and to standardize cellular products intended for clinical application has driven evaluation of alternatives to FBS. Replacement of FBS in culture for several days before administration has been proposed to reduce antigenicity and potentially prolong survival after injection. However, the functional consequences of MSC culture in different serum types have not been fully evaluated. The objective of this study was to compare the immunomodulatory and antibacterial properties of MSCs cultured in three serum sources: FBS or autologous or allogeneic equine serum. We hypothesized that continuous culture in FBS would generate MSCs with improved functionality compared to equine serum and that there would not be important differences between MSCs cultured in autologous vs. allogeneic equine serum. To address these questions, MSCs from three healthy donor horses were expanded in medium with FBS and then switched to culture in FBS or autologous or allogeneic equine serum for 72 h. The impact of this 72-h culture period in different sera on cell viability, cell doubling time, cell morphology, bactericidal capability, chondrogenic differentiation, and production of cytokines and antimicrobial peptides was assessed. Altering serum source did not affect cell viability or morphology. However, cells cultured in FBS had shorter cell doubling times and secreted more interleukin 4 (IL-4), IL-5, IL-17, RANTES, granulocyte-macrophage colony-stimulating factor, fibroblast growth factor 2, eotaxin, and antimicrobial peptide cathelicidin/LL-37 than cells cultured in either source of equine serum. Cells cultured in FBS also exhibited greater spontaneous bactericidal activity. Notably, significant differences in any of these parameters were not observed when autologous vs. allogeneic equine serum was used for cell culture. Chondrogenic differentiation was not different between different serum sources. These results indicate that MSC culture in FBS will generate more functional cells based on a number of parameters and that the theoretical risks of FBS use in MSC culture should be weighed against the loss of MSC function likely to be incurred from culture in equine serum.
Copyright © 2021 Pezzanite, Chow, Griffenhagen, Dow and Goodrich.
Publication Date: 2021-04-30 PubMed ID: 33996964PubMed Central: PMC8119767DOI: 10.3389/fvets.2021.634064Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
- Journal Article
Summary
This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.
The research article studies the impact of different serum sources on the functional properties of equine mesenchymal stromal cells (MSCs). The researchers tested the effect of fetal bovine serum (FBS), autologous equine serum, and allogeneic equine serum on cell viability, cell doubling times, cytokine production, and antibacterial activity among other parameters.
Objectives and Hypothesis
- The main objective was to assess the effects of three different types of serum: FBS, autologous equine serum, and allogeneic equine serum on the functionalities of MSCs. The study hypothesized that continuous culture in FBS would produce more functional cells compared to those cultured in equine serums. Also, it anticipated no significant differences between MSCs cultured in autologous or allogeneic equine serum.
Methodology
- The study used MSCs from three healthy donor horses which were first expanded in medium with FBS, then switched to culture in either FBS, autologous equine serum, or allogeneic equine serum for 72 hours.
- The impact of the 72-hour culture period in different serums on various properties of the cells was evaluated. These included: cell viability, cell doubling time, cell morphology, bactericidal capability, chondrogenic differentiation, and production of cytokines and antimicrobial peptides.
Results
- The change in serum sources did not affect the cells’ viability or morphology. However, cells cultured in FBS had shorter doubling times and secreted more of several cytokines, including IL-4, IL-5, IL-17, and others, plus the antimicrobial peptide cathelicidin/LL-37.
- The FBS-cultured cells also showed greater spontaneous bactericidal activity. There were no significant differences noted in parameters when cultures used autologous versus allogeneic equine serum.
- Chondrogenic differentiation remained the same across different serum sources.
Conclusion
- The results suggested that MSC cultures in FBS will produce more functional cells based on several parameters. The researchers advise that the potential risks of using FBS in MSC culture should be weighed against the potential loss of MSC function that might occur if equine serum is used instead.
Cite This Article
APA
Pezzanite L, Chow L, Griffenhagen G, Dow S, Goodrich L.
(2021).
Impact of Three Different Serum Sources on Functional Properties of Equine Mesenchymal Stromal Cells.
Front Vet Sci, 8, 634064.
https://doi.org/10.3389/fvets.2021.634064 Publication
Researcher Affiliations
- Department of Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO, United States.
- Department of Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO, United States.
- Department of Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO, United States.
- Department of Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO, United States.
- Department of Microbiology, Immunology and Pathology, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO, United States.
- Department of Clinical Sciences, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO, United States.
Conflict of Interest Statement
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
References
This article includes 85 references
- Smith RK, Korda M, Blunn GW, Goodship AE. Isolation and implantation of autologous equine mesenchymal stem cells from bone marrow into the superficial digital flexor tendon as a potential novel treatment.. Equine Vet J 2003 Jan;35(1):99-102.
- Smith RK. Mesenchymal stem cell therapy for equine tendinopathy.. Disabil Rehabil 2008;30(20-22):1752-8.
- Cortés-Araya Y, Amilon K, Rink BE, Black G, Lisowski Z, Donadeu FX, Esteves CL. Comparison of Antibacterial and Immunological Properties of Mesenchymal Stem/Stromal Cells from Equine Bone Marrow, Endometrium, and Adipose Tissue.. Stem Cells Dev 2018 Nov 1;27(21):1518-1525.
- Harman RM, Yang S, He MK, Van de Walle GR. Antimicrobial peptides secreted by equine mesenchymal stromal cells inhibit the growth of bacteria commonly found in skin wounds.. Stem Cell Res Ther 2017 Jul 4;8(1):157.
- Bussche L, Harman RM, Syracuse BA, Plante EL, Lu YC, Curtis TM, Ma M, Van de Walle GR. Microencapsulated equine mesenchymal stromal cells promote cutaneous wound healing in vitro.. Stem Cell Res Ther 2015 Apr 11;6(1):66.
- MacDonald ES, Barrett JG. The Potential of Mesenchymal Stem Cells to Treat Systemic Inflammation in Horses.. Front Vet Sci 2019;6:507.
- Arnhold SJ, Goletz I, Klein H, Stumpf G, Beluche LA, Rohde C, Addicks K, Litzke LF. Isolation and characterization of bone marrow-derived equine mesenchymal stem cells.. Am J Vet Res 2007 Oct;68(10):1095-105.
- Sherman AB, Gilger BC, Berglund AK, Schnabel LV. Effect of bone marrow-derived mesenchymal stem cells and stem cell supernatant on equine corneal wound healing in vitro.. Stem Cell Res Ther 2017 May 25;8(1):120.
- Davis AB, Schnabel LV, Gilger BC. Subconjunctival bone marrow-derived mesenchymal stem cell therapy as a novel treatment alternative for equine immune-mediated keratitis: A case series.. Vet Ophthalmol 2019 Sep;22(5):674-682.
- Ferris DJ, Frisbie DD, Kisiday JD, McIlwraith CW, Hague BA, Major MD, Schneider RK, Zubrod CJ, Kawcak CE, Goodrich LR. Clinical outcome after intra-articular administration of bone marrow derived mesenchymal stem cells in 33 horses with stifle injury.. Vet Surg 2014 Mar;43(3):255-65.
- Godwin EE, Young NJ, Dudhia J, Beamish IC, Smith RK. Implantation of bone marrow-derived mesenchymal stem cells demonstrates improved outcome in horses with overstrain injury of the superficial digital flexor tendon.. Equine Vet J 2012 Jan;44(1):25-32.
- Berner D, Brehm W, Gerlach K, Gittel C, Offhaus J, Paebst F, Scharner D, Burk J. Longitudinal Cell Tracking and Simultaneous Monitoring of Tissue Regeneration after Cell Treatment of Natural Tendon Disease by Low-Field Magnetic Resonance Imaging.. Stem Cells Int 2016;2016:1207190.
- Schubert S, Brehm W, Hillmann A, Burk J. Serum-free human MSC medium supports consistency in human but not in equine adipose-derived multipotent mesenchymal stromal cell culture.. Cytometry A 2018 Jan;93(1):60-72.
- Drach G, Maret A, Richard MF, Barbu E. [Transfer and induction of delayed hypersensitivity to methylated bovine serum albumin in the absence of adjuvant].. C R Acad Hebd Seances Acad Sci D 1977 Jun 20;284(23):2435-7.
- . Medicinal and other products and human and animal transmissible spongiform encephalopathies: memorandum from a WHO meeting.. Bull World Health Organ 1997;75(6):505-13.
- Karnieli O, Friedner OM, Allickson JG, Zhang N, Jung S, Fiorentini D, Abraham E, Eaker SS, Yong TK, Chan A, Griffiths S, Wehn AK, Oh S, Karnieli O. A consensus introduction to serum replacements and serum-free media for cellular therapies.. Cytotherapy 2017 Feb;19(2):155-169.
- European Commission. Note for Guidance on Minimizing the Risk of Transmitting Animal Spongiform Enceaphlopathy Agents via Human and Veterinary Medicinal Products (EMA/410/01 rev.3). Official Journal of the European Union Brussels; (2011).
- European Medicines Agency. Guideline on Human Cell-Based Medicinal Products. European Medicines Agency London; (2008).
- European Medicines Agency. Guideline on the Use of Bovine Serum in the Manufacture of Human Biological Medicinal Products 2013. European Medicines Agency London; (2013).
- Mendicino M, Bailey AM, Wonnacott K, Puri RK, Bauer SR. MSC-based product characterization for clinical trials: an FDA perspective.. Cell Stem Cell 2014 Feb 6;14(2):141-5.
- Müller I, Kordowich S, Holzwarth C, Spano C, Isensee G, Staiber A, Viebahn S, Gieseke F, Langer H, Gawaz MP, Horwitz EM, Conte P, Handgretinger R, Dominici M. Animal serum-free culture conditions for isolation and expansion of multipotent mesenchymal stromal cells from human BM.. Cytotherapy 2006;8(5):437-44.
- Lange C, Cakiroglu F, Spiess AN, Cappallo-Obermann H, Dierlamm J, Zander AR. Accelerated and safe expansion of human mesenchymal stromal cells in animal serum-free medium for transplantation and regenerative medicine.. J Cell Physiol 2007 Oct;213(1):18-26.
- Blande IS, Bassaneze V, Lavini-Ramos C, Fae KC, Kalil J, Miyakawa AA, Schettert IT, Krieger JE. Adipose tissue mesenchymal stem cell expansion in animal serum-free medium supplemented with autologous human platelet lysate.. Transfusion 2009 Dec;49(12):2680-5.
- Laitinen A, Oja S, Kilpinen L, Kaartinen T, Möller J, Laitinen S, Korhonen M, Nystedt J. A robust and reproducible animal serum-free culture method for clinical-grade bone marrow-derived mesenchymal stromal cells.. Cytotechnology 2016 Aug;68(4):891-906.
- Gottipamula S, Muttigi MS, Chaansa S, Ashwin KM, Priya N, Kolkundkar U, SundarRaj S, Majumdar AS, Seetharam RN. Large-scale expansion of pre-isolated bone marrow mesenchymal stromal cells in serum-free conditions.. J Tissue Eng Regen Med 2016 Feb;10(2):108-19.
- Chase LG, Lakshmipathy U, Solchaga LA, Rao MS, Vemuri MC. A novel serum-free medium for the expansion of human mesenchymal stem cells.. Stem Cell Res Ther 2010 Apr 2;1(1):8.
- Swamynathan P, Venugopal P, Kannan S, Thej C, Kolkundar U, Bhagwat S, Ta M, Majumdar AS, Balasubramanian S. Are serum-free and xeno-free culture conditions ideal for large scale clinical grade expansion of Wharton's jelly derived mesenchymal stem cells? A comparative study.. Stem Cell Res Ther 2014 Jul 28;5(4):88.
- Oikonomopoulos A, van Deen WK, Manansala AR, Lacey PN, Tomakili TA, Ziman A, Hommes DW. Optimization of human mesenchymal stem cell manufacturing: the effects of animal/xeno-free media.. Sci Rep 2015 Nov 13;5:16570.
- Clark KC, Kol A, Shahbenderian S, Granick JL, Walker NJ, Borjesson DL. Canine and Equine Mesenchymal Stem Cells Grown in Serum Free Media Have Altered Immunophenotype.. Stem Cell Rev Rep 2016 Apr;12(2):245-56.
- Ho ST, Tanavde VM, Hui JH, Lee EH. Upregulation of Adipogenesis and Chondrogenesis in MSC Serum-Free Culture.. Cell Med 2011;2(1):27-41.
- Rakian R, Block TJ, Johnson SM, Marinkovic M, Wu J, Dai Q, Dean DD, Chen XD. Native extracellular matrix preserves mesenchymal stem cell "stemness" and differentiation potential under serum-free culture conditions.. Stem Cell Res Ther 2015 Dec 1;6:235.
- Heathman TR, Stolzing A, Fabian C, Rafiq QA, Coopman K, Nienow AW, Kara B, Hewitt CJ. Serum-free process development: improving the yield and consistency of human mesenchymal stromal cell production.. Cytotherapy 2015 Nov;17(11):1524-35.
- Miwa H, Hashimoto Y, Tensho K, Wakitani S, Takagi M. Xeno-free proliferation of human bone marrow mesenchymal stem cells.. Cytotechnology 2012 May;64(3):301-8.
- Meuleman N, Tondreau T, Delforge A, Dejeneffe M, Massy M, Libertalis M, Bron D, Lagneaux L. Human marrow mesenchymal stem cell culture: serum-free medium allows better expansion than classical alpha-MEM medium.. Eur J Haematol 2006 Apr;76(4):309-16.
- Agata H, Watanabe N, Ishii Y, Kubo N, Ohshima S, Yamazaki M, Tojo A, Kagami H. Feasibility and efficacy of bone tissue engineering using human bone marrow stromal cells cultivated in serum-free conditions.. Biochem Biophys Res Commun 2009 May 1;382(2):353-8.
- Lindroos B, Boucher S, Chase L, Kuokkanen H, Huhtala H, Haataja R, Vemuri M, Suuronen R, Miettinen S. Serum-free, xeno-free culture media maintain the proliferation rate and multipotentiality of adipose stem cells in vitro.. Cytotherapy 2009;11(7):958-72.
- Wu X, Kang H, Liu X, Gao J, Zhao K, Ma Z. Serum and xeno-free, chemically defined, no-plate-coating-based culture system for mesenchymal stromal cells from the umbilical cord.. Cell Prolif 2016 Oct;49(5):579-88.
- Aldahmash A, Haack-Sørensen M, Al-Nbaheen M, Harkness L, Abdallah BM, Kassem M. Human serum is as efficient as fetal bovine serum in supporting proliferation and differentiation of human multipotent stromal (mesenchymal) stem cells in vitro and in vivo.. Stem Cell Rev Rep 2011 Nov;7(4):860-8.
- Kuznetsov SA, Mankani MH, Robey PG. Effect of serum on human bone marrow stromal cells: ex vivo expansion and in vivo bone formation.. Transplantation 2000 Dec 27;70(12):1780-7.
- Popov A, Scotchford C, Grant D, Sottile V. Impact of Serum Source on Human Mesenchymal Stem Cell Osteogenic Differentiation in Culture.. Int J Mol Sci 2019 Oct 11;20(20).
- Escobedo-Lucea C, Bellver C, Gandia C, Sanz-Garcia A, Esteban FJ, Mirabet V, Forte G, Moreno I, Lezameta M, Ayuso-Sacido A, Garcia-Verdugo JM. A xenogeneic-free protocol for isolation and expansion of human adipose stem cells for clinical uses.. PLoS One 2013;8(7):e67870.
- Cardoso TC, Ferrari HF, Garcia AF, Novais JB, Silva-Frade C, Ferrarezi MC, Andrade AL, Gameiro R. Isolation and characterization of Wharton's jelly-derived multipotent mesenchymal stromal cells obtained from bovine umbilical cord and maintained in a defined serum-free three-dimensional system.. BMC Biotechnol 2012 May 4;12:18.
- Pérez-Ilzarbe M, Díez-Campelo M, Aranda P, Tabera S, Lopez T, del Cañizo C, Merino J, Moreno C, Andreu EJ, Prósper F, Pérez-Simón JA. Comparison of ex vivo expansion culture conditions of mesenchymal stem cells for human cell therapy.. Transfusion 2009 Sep;49(9):1901-10.
- Rowland AL, Burns ME, Levine GJ, Watts AE. Xenogen-free stem cell preparation enhances safety and efficacy. Proceedings, NAVRMA Conference Niagara on the Lake, ON (2019).
- Esteves CL, Sheldrake TA, Mesquita SP, Pesántez JJ, Menghini T, Dawson L, Péault B, Donadeu FX. Isolation and characterization of equine native MSC populations.. Stem Cell Res Ther 2017 Apr 18;8(1):80.
- Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop Dj, Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement.. Cytotherapy 2006;8(4):315-7.
- Greenwood SK, Hill RB, Sun JT, Armstrong MJ, Johnson TE, Gara JP, Galloway SM. Population doubling: a simple and more accurate estimation of cell growth suppression in the in vitro assay for chromosomal aberrations that reduces irrelevant positive results.. Environ Mol Mutagen 2004;43(1):36-44.
- Chow L, Johnson V, Impastato R, Coy J, Strumpf A, Dow S. Antibacterial activity of human mesenchymal stem cells mediated directly by constitutively secreted factors and indirectly by activation of innate immune effector cells.. Stem Cells Transl Med 2020 Feb;9(2):235-249.
- Bates D, Maechler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. J Statis Software (2015) 67:1–48.
- Kuznetsova A, Brockhoff PB, Christensen RHB. lmerTest package: tests in linear mixed effects models. J Statis Software (2017) 82:1–26.
- Lenth R. emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.5.5-1 (2021).
- R Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing Vienna; (2020).
- Steen-Louws C, Popov-Celeketic J, Mastbergen SC, Coeleveld K, Hack CE, Eijkelkamp N, Tryfonidou M, Spruijt S, van Roon JAG, Lafeber FPJG. IL4-10 fusion protein has chondroprotective, anti-inflammatory and potentially analgesic effects in the treatment of osteoarthritis.. Osteoarthritis Cartilage 2018 Aug;26(8):1127-1135.
- Demazière A, Leek R, Athanasou NA. Histological distribution of the interleukin-4 receptor (IL4R) within the normal and pathological synovium.. Rev Rhum Mal Osteoartic 1992 Mar;59(3):219-24.
- van Meegeren ME, Roosendaal G, Jansen NW, Wenting MJ, van Wesel AC, van Roon JA, Lafeber FP. IL-4 alone and in combination with IL-10 protects against blood-induced cartilage damage.. Osteoarthritis Cartilage 2012 Jul;20(7):764-72.
- Millward-Sadler SJ, Khan NS, Bracher MG, Wright MO, Salter DM. Roles for the interleukin-4 receptor and associated JAK/STAT proteins in human articular chondrocyte mechanotransduction.. Osteoarthritis Cartilage 2006 Oct;14(10):991-1001.
- Forster T, Chapman K, Loughlin J. Common variants within the interleukin 4 receptor alpha gene (IL4R) are associated with susceptibility to osteoarthritis.. Hum Genet 2004 Mar;114(4):391-5.
- Salter DM, Nuki G, Wright MO. IL-4 inhibition of cartilage breakdown in bovine articular explants.. J Rheumatol 1996 Jul;23(7):1314-5.
- Alaaeddine N, Di Battista JA, Pelletier JP, Kiansa K, Cloutier JM, Martel-Pelletier J. Inhibition of tumor necrosis factor alpha-induced prostaglandin E2 production by the antiinflammatory cytokines interleukin-4, interleukin-10, and interleukin-13 in osteoarthritic synovial fibroblasts: distinct targeting in the signaling pathways.. Arthritis Rheum 1999 Apr;42(4):710-8.
- Jenkins JK, Arend WP. Interleukin 1 receptor antagonist production in human monocytes is induced by IL-1 alpha, IL-3, IL-4 and GM-CSF.. Cytokine 1993 Sep;5(5):407-15.
- Vangsness CT Jr, Burke WS, Narvy SJ, MacPhee RD, Fedenko AN. Human knee synovial fluid cytokines correlated with grade of knee osteoarthritis--a pilot study.. Bull NYU Hosp Jt Dis 2011;69(2):122-7.
- Cuéllar VG, Cuéllar JM, Kirsch T, Strauss EJ. Correlation of Synovial Fluid Biomarkers With Cartilage Pathology and Associated Outcomes in Knee Arthroscopy.. Arthroscopy 2016 Mar;32(3):475-85.
- Conti P, DiGioacchino M. MCP-1 and RANTES are mediators of acute and chronic inflammation.. Allergy Asthma Proc 2001 May-Jun;22(3):133-7.
- Shahrara S, Pickens SR, Dorfleutner A, Pope RM. IL-17 induces monocyte migration in rheumatoid arthritis.. J Immunol 2009 Mar 15;182(6):3884-91.
- Gaffen SL. The role of interleukin-17 in the pathogenesis of rheumatoid arthritis.. Curr Rheumatol Rep 2009 Oct;11(5):365-70.
- Chia SL, Sawaji Y, Burleigh A, McLean C, Inglis J, Saklatvala J, Vincent T. Fibroblast growth factor 2 is an intrinsic chondroprotective agent that suppresses ADAMTS-5 and delays cartilage degradation in murine osteoarthritis.. Arthritis Rheum 2009 Jul;60(7):2019-27.
- Ellman MB, An HS, Muddasani P, Im HJ. Biological impact of the fibroblast growth factor family on articular cartilage and intervertebral disc homeostasis.. Gene 2008 Aug 15;420(1):82-9.
- Yan D, Chen D, Cool SM, van Wijnen AJ, Mikecz K, Murphy G, Im HJ. Fibroblast growth factor receptor 1 is principally responsible for fibroblast growth factor 2-induced catabolic activities in human articular chondrocytes.. Arthritis Res Ther 2011 Aug 11;13(4):R130.
- Li X, Ellman MB, Kroin JS, Chen D, Yan D, Mikecz K, Ranjan KC, Xiao G, Stein GS, Kim SG, Cole B, van Wijnen AJ, Im HJ. Species-specific biological effects of FGF-2 in articular cartilage: implication for distinct roles within the FGF receptor family.. J Cell Biochem 2012 Jul;113(7):2532-42.
- Hsu YH, Hsieh MS, Liang YC, Li CY, Sheu MT, Chou DT, Chen TF, Chen CH. Production of the chemokine eotaxin-1 in osteoarthritis and its role in cartilage degradation.. J Cell Biochem 2004 Nov 15;93(5):929-39.
- Li B, Zhang YL, Yu SY. Synovial Fluid Eotaxin-1 Levels May Reflect Disease Progression in Primary Knee Osteoarthritis Among Elderly Han Chinese: A Cross-Sectional Study.. Cartilage 2019 Oct;10(4):408-416.
- Syversen SW, Goll GL, Haavardsholm EA, Bøyesen P, Lea T, Kvien TK. A high serum level of eotaxin (CCL 11) is associated with less radiographic progression in early rheumatoid arthritis patients.. Arthritis Res Ther 2008;10(2):R28.
- Lotfi N, Thome R, Rezaei N, Zhang GX, Rezaei A, Rostami A, Esmaeil N. Roles of GM-CSF in the Pathogenesis of Autoimmune Diseases: An Update.. Front Immunol 2019;10:1265.
- Krasnodembskaya A, Song Y, Fang X, Gupta N, Serikov V, Lee JW, Matthay MA. Antibacterial effect of human mesenchymal stem cells is mediated in part from secretion of the antimicrobial peptide LL-37.. Stem Cells 2010 Dec;28(12):2229-38.
- Krasnodembskaya A, Samarani G, Song Y, Zhuo H, Su X, Lee JW, Gupta N, Petrini M, Matthay MA. Human mesenchymal stem cells reduce mortality and bacteremia in gram-negative sepsis in mice in part by enhancing the phagocytic activity of blood monocytes.. Am J Physiol Lung Cell Mol Physiol 2012 May 15;302(10):L1003-13.
- Le Blanc K, Mougiakakos D. Multipotent mesenchymal stromal cells and the innate immune system.. Nat Rev Immunol 2012 Apr 25;12(5):383-96.
- Mei SH, Haitsma JJ, Dos Santos CC, Deng Y, Lai PF, Slutsky AS, Liles WC, Stewart DJ. Mesenchymal stem cells reduce inflammation while enhancing bacterial clearance and improving survival in sepsis.. Am J Respir Crit Care Med 2010 Oct 15;182(8):1047-57.
- Mezey É, Nemeth K. Mesenchymal stem cells and infectious diseases: Smarter than drugs.. Immunol Lett 2015 Dec;168(2):208-14.
- Monneret G. Mesenchymal stem cells: another anti-inflammatory treatment for sepsis?. Nat Med 2009 Jun;15(6):601-2; author reply 602.
- Németh K, Leelahavanichkul A, Yuen PS, Mayer B, Parmelee A, Doi K, Robey PG, Leelahavanichkul K, Koller BH, Brown JM, Hu X, Jelinek I, Star RA, Mezey E. Bone marrow stromal cells attenuate sepsis via prostaglandin E(2)-dependent reprogramming of host macrophages to increase their interleukin-10 production.. Nat Med 2009 Jan;15(1):42-9.
- Kim J, Hematti P. Mesenchymal stem cell-educated macrophages: a novel type of alternatively activated macrophages.. Exp Hematol 2009 Dec;37(12):1445-53.
- Lee JW, Gupta N, Serikov V, Matthay MA. Potential application of mesenchymal stem cells in acute lung injury.. Expert Opin Biol Ther 2009 Oct;9(10):1259-70.
- Cruz FF, Weiss DJ, Rocco PR. Prospects and progress in cell therapy for acute respiratory distress syndrome.. Expert Opin Biol Ther 2016 Nov;16(11):1353-1360.
- Gebler A, Zabel O, Seliger B. The immunomodulatory capacity of mesenchymal stem cells.. Trends Mol Med 2012 Feb;18(2):128-34.
- de Witte SFH, Luk F, Sierra Parraga JM, Gargesha M, Merino A, Korevaar SS, Shankar AS, O'Flynn L, Elliman SJ, Roy D, Betjes MGH, Newsome PN, Baan CC, Hoogduijn MJ. Immunomodulation By Therapeutic Mesenchymal Stromal Cells (MSC) Is Triggered Through Phagocytosis of MSC By Monocytic Cells.. Stem Cells 2018 Apr;36(4):602-615.
Citations
This article has been cited 6 times.- Petrova V, Vachkova E. Outlook of Adipose-Derived Stem Cells: Challenges to Their Clinical Application in Horses.. Vet Sci 2023 May 12;10(5).
- Jammes M, Contentin R, Cassé F, Galéra P. Equine osteoarthritis: Strategies to enhance mesenchymal stromal cell-based acellular therapies.. Front Vet Sci 2023;10:1115774.
- Kamperman T, Willemen NGA, Kelder C, Koerselman M, Becker M, Lins L, Johnbosco C, Karperien M, Leijten J. Steering Stem Cell Fate within 3D Living Composite Tissues Using Stimuli-Responsive Cell-Adhesive Micromaterials.. Adv Sci (Weinh) 2023 Apr;10(10):e2205487.
- Pezzanite LM, Chow L, Strumpf A, Johnson V, Dow SW. Immune Activated Cellular Therapy for Drug Resistant Infections: Rationale, Mechanisms, and Implications for Veterinary Medicine.. Vet Sci 2022 Nov 4;9(11).
- Pilgrim CR, McCahill KA, Rops JG, Dufour JM, Russell KA, Koch TG. A Review of Fetal Bovine Serum in the Culture of Mesenchymal Stromal Cells and Potential Alternatives for Veterinary Medicine.. Front Vet Sci 2022;9:859025.
- Rampin A, Skoufos I, Raghunath M, Tzora A, Diakakis N, Prassinos N, Zeugolis DI. Allogeneic Serum and Macromolecular Crowding Maintain Native Equine Tenocyte Function in Culture.. Cells 2022 May 5;11(9).
Use Nutrition Calculator
Check if your horse's diet meets their nutrition requirements with our easy-to-use tool Check your horse's diet with our easy-to-use tool
Talk to a Nutritionist
Discuss your horse's feeding plan with our experts over a free phone consultation Discuss your horse's diet over a phone consultation
Submit Diet Evaluation
Get a customized feeding plan for your horse formulated by our equine nutritionists Get a custom feeding plan formulated by our nutritionists