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Frontiers in veterinary science2022; 9; 958724; doi: 10.3389/fvets.2022.958724

Comparing the immunomodulatory properties of equine BM-MSCs culture expanded in autologous platelet lysate, pooled platelet lysate, equine serum and fetal bovine serum supplemented culture media.

Abstract: Joint injury often leads to cartilage damage and posttraumatic inflammation, which drives continued extracellular matrix degradation culminating in osteoarthritis. Mesenchymal stem cells (MSCs) have been proposed as a biotherapeutic to modulate inflammation within the joint. However, concerns have been raised regarding the immunogenicity of MSCs cultured in traditional fetal bovine serum (FBS) containing media, and the potential of xenogenic antigens to activate the immune system causing rejection and destruction of the MSCs. Xenogen-free alternatives to FBS have been proposed to decrease MSC immunogenicity, including platelet lysate (PL) and equine serum. The objective of this study was to compare the immunomodulatory properties of BM-MSCs culture-expanded in media supplemented with autologous PL (APL), pooled PL (PPL), equine serum (ES) or FBS. We hypothesized that BM-MSCs culture expanded in media with xenogen-free supplements would exhibit superior immunomodulatory properties to those cultured in FBS containing media. Bone marrow-derived MSCs (BM-MSCs) were isolated from six horses and culture expanded in each media type. Blood was collected from each horse to isolate platelet lysate. The immunomodulatory function of the BM-MSCs was assessed a T cell proliferation assay and through multiplex immunoassay quantification of cytokines, including IL-1β, IL-6, IL-8, IL-10, and TNFα, following preconditioning of BM-MSCs with IL-1β. The concentration of platelet-derived growth factor BB (PDGF-BB), IL-10, and transforming growth factor-β (TGF-β) in each media was measured immunoassay. BM-MSCs cultured in ES resulted in significant suppression of T cell proliferation ( = 0.02). Cell culture supernatant from preconditioned BM-MSCs cultured in ES had significantly higher levels of IL-6. PDGF-BB was significantly higher in APL media compared to FBS media ( = 0.016), while IL-10 was significantly higher in PPL media than ES and FBS ( = 0.04). TGF-β was highest in APL media, with a significant difference in comparison to ES media ( = 0.03). In conclusion, expansion of equine BM-MSCs in ES may enhance their immunomodulatory abilities, while PL containing media may have some inherent therapeutic potential associated with higher concentrations of growth factors. Further studies are needed to elucidate which xenogen-free supplement optimizes BM-MSC performance.
Copyright © 2022 Even, Gaesser, Ciamillo, Linardi and Ortved.
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Publication Date: 2022-08-25 PubMed ID: 36090170PubMed Central: PMC9453159DOI: 10.3389/fvets.2022.958724Google Scholar: Lookup
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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.

This research article investigates the immunomodulatory properties of horse bone marrow-derived mesenchymal stem cells (BM-MSCs) when culture expanded in different types of media. Specifically, the study compares media supplemented with autologous platelet lysate (APL), pooled platelet lysate (PPL), equine serum (ES), or fetal bovine serum (FBS). The primary finding is that BM-MSCs cultured in ES appear to have superior immunomodulatory abilities, while media containing PL may contain growth factors beneficial to therapeutic applications.

Article’s Detailed Explanation

This study aimed to contribute to improving our understanding of the most optimal methods of effectively culturing equine bone marrow mesenchymal stem cells (BM-MSCs) for therapeutic purposes in treating inflammation caused by joint injury.

  • The researchers elaborated on the problem with traditional culture mediums. The traditionally used fetal bovine serum (FBS) may invoke an immune response rejecting the cultured stem cells due to the presence of xenogenic (foreign) antigens.
  • They proposed testing four different culture mediums: autologous platelet lysate (APL), pooled platelet lysate (PPL), equine serum (ES), and the traditionally used fetal bovine serum (FBS). The platelet lysate and equine serum are xenogen-free and hypothesized to reduce the chances of an immune reaction.
  • A panel of tests was conducted to assess the immunomodulatory properties of the cultured BM-MSCs. These included a T cell proliferation assay and quantitative multi-immunoassays for cytokines like IL-1β, IL-6, IL-8, IL-10, and TNFα. The concentration of platelet-derived growth factor BB (PDGF-BB), IL-10, and transforming growth factor-β (TGF-β) in each medium were also measured.
  • The results indicated that BM-MSCs cultured in equine serum showed significantly enhanced capability to suppress T cell proliferation. Furthermore, the supernatant from BM-MSCs cultured in ES had significantly higher levels of IL-6, revealing that ES may enhance the immunomodulatory abilities of MSCs.
  • APL media showed significantly higher levels of PDGF-BB compared to FBS media. IL-10 was significantly higher in PPL media over ES and FBS. TGF-β was the highest in APL media, displaying a significant difference in comparison to ES media.
  • These results suggest that while equine serum may be more effective at inducing immunomodulatory properties, platelet lysate growth factors potentially lead to improved therapeutic performance.

Conclusions

The research indicates that equine serum may be a more effective medium for enhancing the immunomodulatory properties of bone marrow-derived mesenchamal stem cells. However, the study also reveals that platelet lysate media have higher concentrations of beneficial growth factors, hinting at additional therapeutic potential. Ultimately, the authors argue, further studies are required to determine the optimal xenogen-free supplement for maximizing the performance of BM-MSCs in therapy.

Cite This Article

APA
Even KM, Gaesser AM, Ciamillo SA, Linardi RL, Ortved KF. (2022). Comparing the immunomodulatory properties of equine BM-MSCs culture expanded in autologous platelet lysate, pooled platelet lysate, equine serum and fetal bovine serum supplemented culture media. Front Vet Sci, 9, 958724. https://doi.org/10.3389/fvets.2022.958724

Publication

Frontiers in veterinary science
ISSN: 2297-1769
NlmUniqueID: 101666658
Country: Switzerland
Language: English
Volume: 9
Pages: 958724
PII: 958724

Researcher Affiliations

Even, Kayla M
  • Department of Clinical Studies, New Bolton Center, School of Veterinary Medicine, University of Pennsylvania, Kennett Square, PA, United States.
Gaesser, Angela M
  • Department of Clinical Studies, New Bolton Center, School of Veterinary Medicine, University of Pennsylvania, Kennett Square, PA, United States.
Ciamillo, Sarah A
  • Department of Clinical Studies, New Bolton Center, School of Veterinary Medicine, University of Pennsylvania, Kennett Square, PA, United States.
Linardi, Renata L
  • Department of Clinical Studies, New Bolton Center, School of Veterinary Medicine, University of Pennsylvania, Kennett Square, PA, United States.
Ortved, Kyla F
  • Department of Clinical Studies, New Bolton Center, School of Veterinary Medicine, University of Pennsylvania, Kennett Square, PA, United States.

Grant Funding

  • U01 TR002953 / NCATS NIH HHS

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 60 references
  1. Clegg P, Booth T. Drugs used to treat osteoarthritis in the horse. In Practice (2000) 22:594–603.
    doi: 10.1136/inpract.22.10.594google scholar: lookup
  2. Mankin HJ. The response of articular cartilage to mechanical injury.. J Bone Joint Surg Am 1982 Mar;64(3):460-6.
    doi: 10.2106/00004623-198264030-00022pubmed: 6174527google scholar: lookup
  3. Lieberthal J, Sambamurthy N, Scanzello CR. Inflammation in joint injury and post-traumatic osteoarthritis.. Osteoarthritis Cartilage 2015 Nov;23(11):1825-34.
    doi: 10.1016/j.joca.2015.08.015pmc: PMC4630675pubmed: 26521728google scholar: lookup
  4. MacDonald ES, Barrett JG. The Potential of Mesenchymal Stem Cells to Treat Systemic Inflammation in Horses.. Front Vet Sci 2019;6:507.
    doi: 10.3389/fvets.2019.00507pmc: PMC6985200pubmed: 32039250google scholar: lookup
  5. Castro-Manrreza ME, Montesinos JJ. Immunoregulation by mesenchymal stem cells: biological aspects and clinical applications.. J Immunol Res 2015;2015:394917.
    doi: 10.1155/2015/394917pmc: PMC4417567pubmed: 25961059google scholar: lookup
  6. Yang SH, Park MJ, Yoon IH, Kim SY, Hong SH, Shin JY, Nam HY, Kim YH, Kim B, Park CG. Soluble mediators from mesenchymal stem cells suppress T cell proliferation by inducing IL-10.. Exp Mol Med 2009 May 31;41(5):315-24.
    doi: 10.3858/emm.2009.41.5.035pmc: PMC2701980pubmed: 19307751google scholar: lookup
  7. van Buul GM, Villafuertes E, Bos PK, Waarsing JH, Kops N, Narcisi R, Weinans H, Verhaar JA, Bernsen MR, van Osch GJ. Mesenchymal stem cells secrete factors that inhibit inflammatory processes in short-term osteoarthritic synovium and cartilage explant culture.. Osteoarthritis Cartilage 2012 Oct;20(10):1186-96.
    doi: 10.1016/j.joca.2012.06.003pubmed: 22771777google scholar: lookup
  8. Pittenger MF, Martin BJ. Mesenchymal stem cells and their potential as cardiac therapeutics.. Circ Res 2004 Jul 9;95(1):9-20.
    doi: 10.1161/01.RES.0000135902.99383.6fpubmed: 15242981google scholar: lookup
  9. Murphy JM, Fink DJ, Hunziker EB, Barry FP. Stem cell therapy in a caprine model of osteoarthritis.. Arthritis Rheum 2003 Dec;48(12):3464-74.
    doi: 10.1002/art.11365pubmed: 14673997google scholar: lookup
  10. van Velthoven CT, Sheldon RA, Kavelaars A, Derugin N, Vexler ZS, Willemen HL, Maas M, Heijnen CJ, Ferriero DM. Mesenchymal stem cell transplantation attenuates brain injury after neonatal stroke.. Stroke 2013 May;44(5):1426-32.
    doi: 10.1161/STROKEAHA.111.000326pmc: PMC3694433pubmed: 23539530google scholar: lookup
  11. Naskou MC, Norton NA, Copland IB, Galipeau J, Peroni JF. Innate immune responses of equine monocytes cultured in equine platelet lysate.. Vet Immunol Immunopathol 2018 Jan;195:65-71.
    doi: 10.1016/j.vetimm.2017.11.005pubmed: 29249319google scholar: lookup
  12. Naskou MC, Sumner SM, Chocallo A, Kemelmakher H, Thoresen M, Copland I, Galipeau J, Peroni JF. Platelet lysate as a novel serum-free media supplement for the culture of equine bone marrow-derived mesenchymal stem cells.. Stem Cell Res Ther 2018 Mar 22;9(1):75.
    doi: 10.1186/s13287-018-0823-3pmc: PMC5863827pubmed: 29566772google scholar: lookup
  13. Rowland AL, Burns ME, Levine GJ, Watts AE. Preparation Technique Affects Recipient Immune Targeting of Autologous Mesenchymal Stem Cells.. Front Vet Sci 2021;8:724041.
    doi: 10.3389/fvets.2021.724041pmc: PMC8478329pubmed: 34595230google scholar: lookup
  14. Sundin M, Ringdén O, Sundberg B, Nava S, Götherström C, Le Blanc K. No alloantibodies against mesenchymal stromal cells, but presence of anti-fetal calf serum antibodies, after transplantation in allogeneic hematopoietic stem cell recipients.. Haematologica 2007 Sep;92(9):1208-15.
    doi: 10.3324/haematol.11446pubmed: 17666368google scholar: lookup
  15. Spees JL, Gregory CA, Singh H, Tucker HA, Peister A, Lynch PJ, Hsu SC, Smith J, Prockop DJ. Internalized antigens must be removed to prepare hypoimmunogenic mesenchymal stem cells for cell and gene therapy.. Mol Ther 2004 May;9(5):747-56.
    doi: 10.1016/j.ymthe.2004.02.012pubmed: 15120336google scholar: lookup
  16. 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.
    doi: 10.3389/fvets.2022.859025pmc: PMC9111178pubmed: 35591873google scholar: lookup
  17. Joswig AJ, Mitchell A, Cummings KJ, Levine GJ, Gregory CA, Smith R 3rd, Watts AE. Repeated intra-articular injection of allogeneic mesenchymal stem cells causes an adverse response compared to autologous cells in the equine model.. Stem Cell Res Ther 2017 Feb 28;8(1):42.
    doi: 10.1186/s13287-017-0503-8pmc: PMC5329965pubmed: 28241885google scholar: lookup
  18. 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.
    doi: 10.1007/s12015-015-9638-0pmc: PMC4841858pubmed: 26638159google scholar: lookup
  19. 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.
    doi: 10.1002/cyto.a.23240pubmed: 28926198google scholar: lookup
  20. Gilbertie JM, Long JM, Schubert AG, Berglund AK, Schaer TP, Schnabel LV. Pooled Platelet-Rich Plasma Lysate Therapy Increases Synoviocyte Proliferation and Hyaluronic Acid Production While Protecting Chondrocytes From Synoviocyte-Derived Inflammatory Mediators.. Front Vet Sci 2018;5:150.
    doi: 10.3389/fvets.2018.00150pmc: PMC6039577pubmed: 30023361google scholar: lookup
  21. Yaneselli K, Barrachina L, Remacha AR, Algorta A, Vitoria A, Cequier A, Romero A, Vázquez FJ, Maisonnave J, Rodellar C. Effect of allogeneic platelet lysate on equine bone marrow derived mesenchymal stem cell characteristics, including immunogenic and immunomodulatory gene expression profile.. Vet Immunol Immunopathol 2019 Nov;217:109944.
    doi: 10.1016/j.vetimm.2019.109944pubmed: 31563725google scholar: lookup
  22. Boswell SG, Cole BJ, Sundman EA, Karas V, Fortier LA. Platelet-rich plasma: a milieu of bioactive factors.. Arthroscopy 2012 Mar;28(3):429-39.
    doi: 10.1016/j.arthro.2011.10.018pubmed: 22284405google scholar: lookup
  23. Russell KA, Koch TG. Equine platelet lysate as an alternative to fetal bovine serum in equine mesenchymal stromal cell culture - too much of a good thing?. Equine Vet J 2016 Mar;48(2):261-4.
    doi: 10.1111/evj.12440pubmed: 25772755google scholar: lookup
  24. Chapman HS, Gale AL, Dodson ME, Linardi RL, Ortved KF. Autologous Platelet Lysate Does Not Enhance Chondrogenic Differentiation of Equine Bone Marrow-Derived Mesenchymal Stromal Cells Despite Increased TGF-β1 Concentration.. Stem Cells Dev 2020 Feb 1;29(3):144-155.
    doi: 10.1089/scd.2019.0239pubmed: 31802705google scholar: lookup
  25. Gale AL, Linardi RL, McClung G, Mammone RM, Ortved KF. Comparison of the Chondrogenic Differentiation Potential of Equine Synovial Membrane-Derived and Bone Marrow-Derived Mesenchymal Stem Cells.. Front Vet Sci 2019;6:178.
    doi: 10.3389/fvets.2019.00178pmc: PMC6562279pubmed: 31245393google scholar: lookup
  26. Laval K, Favoreel HW, Poelaert KC, Van Cleemput J, Nauwynck HJ. Equine Herpesvirus Type 1 Enhances Viral Replication in CD172a+ Monocytic Cells upon Adhesion to Endothelial Cells.. J Virol 2015 Nov;89(21):10912-23.
    doi: 10.1128/JVI.01589-15pmc: PMC4621108pubmed: 26292328google scholar: lookup
  27. Paebst F, Piehler D, Brehm W, Heller S, Schroeck C, Tárnok A, Burk J. Comparative immunophenotyping of equine multipotent mesenchymal stromal cells: an approach toward a standardized definition.. Cytometry A 2014 Aug;85(8):678-87.
    doi: 10.1002/cyto.a.22491pubmed: 24894974google scholar: lookup
  28. De Schauwer C, Piepers S, Van de Walle GR, Demeyere K, Hoogewijs MK, Govaere JL, Braeckmans K, Van Soom A, Meyer E. In search for cross-reactivity to immunophenotype equine mesenchymal stromal cells by multicolor flow cytometry.. Cytometry A 2012 Apr;81(4):312-23.
    doi: 10.1002/cyto.a.22026pubmed: 22411893google scholar: lookup
  29. Connard SS, Linardi RL, Even KM, Berglund AK, Schnabel LV, Ortved KF. Effects of continuous passage on the immunomodulatory properties of equine bone marrow-derived mesenchymal stem cells in vitro.. Vet Immunol Immunopathol 2021 Apr;234:110203.
    doi: 10.1016/j.vetimm.2021.110203pubmed: 33636546google scholar: lookup
  30. Schnabel LV, Pezzanite LM, Antczak DF, Felippe MJ, Fortier LA. Equine bone marrow-derived mesenchymal stromal cells are heterogeneous in MHC class II expression and capable of inciting an immune response in vitro.. Stem Cell Res Ther 2014 Jan 24;5(1):13.
    doi: 10.1186/scrt402pmc: PMC4055004pubmed: 24461709google scholar: lookup
  31. Barrachina L, Cequier A, Romero A, Vitoria A, Zaragoza P, Vázquez FJ, Rodellar C. Allo-antibody production after intraarticular administration of mesenchymal stem cells (MSCs) in an equine osteoarthritis model: effect of repeated administration, MSC inflammatory stimulation, and equine leukocyte antigen (ELA) compatibility.. Stem Cell Res Ther 2020 Feb 7;11(1):52.
    doi: 10.1186/s13287-020-1571-8pmc: PMC7006079pubmed: 32028995google scholar: lookup
  32. Cassano JM, Schnabel LV, Goodale MB, Fortier LA. Inflammatory licensed equine MSCs are chondroprotective and exhibit enhanced immunomodulation in an inflammatory environment.. Stem Cell Res Ther 2018 Apr 3;9(1):82.
    doi: 10.1186/s13287-018-0840-2pmc: PMC5883371pubmed: 29615127google scholar: lookup
  33. Daynes RA, Dowell T, Araneo BA. Platelet-derived growth factor is a potent biologic response modifier of T cells.. J Exp Med 1991 Dec 1;174(6):1323-33.
    doi: 10.1084/jem.174.6.1323pmc: PMC2119044pubmed: 1660523google scholar: lookup
  34. Seidel SRT, Vendruscolo CP, Moreira JJ, Fülber J, Ottaiano TF, Oliva MLV, Michelacci YM, Baccarin RYA. Does Double Centrifugation Lead to Premature Platelet Aggregation and Decreased TGF-β1 Concentrations in Equine Platelet-Rich Plasma?. Vet Sci 2019 Aug 21;6(3).
    doi: 10.3390/vetsci6030068pmc: PMC6789863pubmed: 31438534google scholar: lookup
  35. Arora S, Doda V, Kotwal U, Dogra M. Quantification of platelets and platelet derived growth factors from platelet-rich-plasma (PRP) prepared at different centrifugal force (g) and time.. Transfus Apher Sci 2016 Feb;54(1):103-10.
    doi: 10.1016/j.transci.2016.01.028pubmed: 26883885google scholar: lookup
  36. Argüelles D, Carmona JU, Pastor J, Iborra A, Viñals L, Martínez P, Bach E, Prades M. Evaluation of single and double centrifugation tube methods for concentrating equine platelets.. Res Vet Sci 2006 Oct;81(2):237-45.
    doi: 10.1016/j.rvsc.2005.12.008pubmed: 16969921google scholar: lookup
  37. Hemeda H, Kalz J, Walenda G, Lohmann M, Wagner W. Heparin concentration is critical for cell culture with human platelet lysate.. Cytotherapy 2013 Sep;15(9):1174-81.
    doi: 10.1016/j.jcyt.2013.05.006pubmed: 23845186google scholar: lookup
  38. Laner-Plamberger S, Oeller M, Poupardin R, Krisch L, Hochmann S, Kalathur R, Pachler K, Kreutzer C, Erdmann G, Rohde E, Strunk D, Schallmoser K. Heparin Differentially Impacts Gene Expression of Stromal Cells from Various Tissues.. Sci Rep 2019 May 10;9(1):7258.
    doi: 10.1038/s41598-019-43700-xpmc: PMC6510770pubmed: 31076619google scholar: lookup
  39. Barrachina L, Remacha AR, Romero A, Vázquez FJ, Albareda J, Prades M, Gosálvez J, Roy R, Zaragoza P, Martín-Burriel I, Rodellar C. Priming Equine Bone Marrow-Derived Mesenchymal Stem Cells with Proinflammatory Cytokines: Implications in Immunomodulation-Immunogenicity Balance, Cell Viability, and Differentiation Potential.. Stem Cells Dev 2017 Jan 1;26(1):15-24.
    doi: 10.1089/scd.2016.0209pubmed: 27712399google scholar: lookup
  40. Barrachina L, Remacha AR, Romero A, Vázquez FJ, Albareda J, Prades M, Ranera B, Zaragoza P, Martín-Burriel I, Rodellar C. Effect of inflammatory environment on equine bone marrow derived mesenchymal stem cells immunogenicity and immunomodulatory properties.. Vet Immunol Immunopathol 2016 Mar;171:57-65.
    doi: 10.1016/j.vetimm.2016.02.007pubmed: 26964718google scholar: lookup
  41. Krampera M. Mesenchymal stromal cell 'licensing': a multistep process.. Leukemia 2011 Sep;25(9):1408-14.
    doi: 10.1038/leu.2011.108pubmed: 21617697google scholar: lookup
  42. Szabó E, Fajka-Boja R, Kriston-Pál É, Hornung Á, Makra I, Kudlik G, Uher F, Katona RL, Monostori É, Czibula Á. Licensing by Inflammatory Cytokines Abolishes Heterogeneity of Immunosuppressive Function of Mesenchymal Stem Cell Population.. Stem Cells Dev 2015 Sep 15;24(18):2171-80.
    doi: 10.1089/scd.2014.0581pubmed: 26153898google scholar: lookup
  43. Ferreira JR, Teixeira GQ, Neto E, Ribeiro-Machado C, Silva AM, Caldeira J, Leite Pereira C, Bidarra S, Maia AF, Lamghari M, Barbosa MA, Gonçalves RM. IL-1β-pre-conditioned mesenchymal stem/stromal cells' secretome modulates the inflammatory response and aggrecan deposition in intervertebral disc.. Eur Cell Mater 2021 Apr 20;41:431-453.
    doi: 10.22203/eCM.v041a28pubmed: 33877647google scholar: lookup
  44. Kapoor M, Martel-Pelletier J, Lajeunesse D, Pelletier JP, Fahmi H. Role of proinflammatory cytokines in the pathophysiology of osteoarthritis.. Nat Rev Rheumatol 2011 Jan;7(1):33-42.
    doi: 10.1038/nrrheum.2010.196pubmed: 21119608google scholar: lookup
  45. Hackel A, Aksamit A, Bruderek K, Lang S, Brandau S. TNF-α and IL-1β sensitize human MSC for IFN-γ signaling and enhance neutrophil recruitment.. Eur J Immunol 2021 Feb;51(2):319-330.
    pubmed: 32845509doi: 10.1002/eji.201948336google scholar: lookup
  46. Petri RM, Hackel A, Hahnel K, Dumitru CA, Bruderek K, Flohe SB, Paschen A, Lang S, Brandau S. Activated Tissue-Resident Mesenchymal Stromal Cells Regulate Natural Killer Cell Immune and Tissue-Regenerative Function.. Stem Cell Reports 2017 Sep 12;9(3):985-998.
    doi: 10.1016/j.stemcr.2017.06.020pmc: PMC5599186pubmed: 28781075google scholar: lookup
  47. Brandau S, Jakob M, Hemeda H, Bruderek K, Janeschik S, Bootz F, Lang S. Tissue-resident mesenchymal stem cells attract peripheral blood neutrophils and enhance their inflammatory activity in response to microbial challenge.. J Leukoc Biol 2010 Nov;88(5):1005-15.
    doi: 10.1189/jlb.0410207pubmed: 20682625google scholar: lookup
  48. Brandau S, Jakob M, Bruderek K, Bootz F, Giebel B, Radtke S, Mauel K, Jäger M, Flohé SB, Lang S. Mesenchymal stem cells augment the anti-bacterial activity of neutrophil granulocytes.. PLoS One 2014;9(9):e106903.
    doi: 10.1371/journal.pone.0106903pmc: PMC4169522pubmed: 25238158google scholar: lookup
  49. Gesser B, Lund M, Lohse N, Vestergaad C, Matsushima K, Sindet-Pedersen S, Jensen SL, Thestrup-Pedersen K, Larsen CG. IL-8 induces T cell chemotaxis, suppresses IL-4, and up-regulates IL-8 production by CD4+ T cells.. J Leukoc Biol 1996 Mar;59(3):407-11.
    doi: 10.1002/jlb.59.3.407pubmed: 8604020google scholar: lookup
  50. Dorronsoro A, Lang V, Ferrin I, Fernández-Rueda J, Zabaleta L, Pérez-Ruiz E, Sepúlveda P, Trigueros C. Intracellular role of IL-6 in mesenchymal stromal cell immunosuppression and proliferation.. Sci Rep 2020 Dec 14;10(1):21853.
    doi: 10.1038/s41598-020-78864-4pmc: PMC7736882pubmed: 33318571google scholar: lookup
  51. Dienz O, Rincon M. The effects of IL-6 on CD4 T cell responses.. Clin Immunol 2009 Jan;130(1):27-33.
    doi: 10.1016/j.clim.2008.08.018pmc: PMC2660866pubmed: 18845487google scholar: lookup
  52. Philipp D, Suhr L, Wahlers T, Choi YH, Paunel-Görgülü A. Preconditioning of bone marrow-derived mesenchymal stem cells highly strengthens their potential to promote IL-6-dependent M2b polarization.. Stem Cell Res Ther 2018 Oct 25;9(1):286.
    doi: 10.1186/s13287-018-1039-2pmc: PMC6202843pubmed: 30359316google scholar: lookup
  53. Endo K, Horiuchi K, Katano H, Ozeki N, Sakamaki Y, Koga H, Sekiya I. Intra-articular Injection of PDGF-BB Explored in a Novel in Vitro Model Mobilizes Mesenchymal Stem Cells From the Synovium Into Synovial Fluid in Rats.. Stem Cell Rev Rep 2021 Oct;17(5):1768-1779.
    doi: 10.1007/s12015-021-10156-4pubmed: 33772387google scholar: lookup
  54. Fierro FA, Kalomoiris S, Sondergaard CS, Nolta JA. Effects on proliferation and differentiation of multipotent bone marrow stromal cells engineered to express growth factors for combined cell and gene therapy.. Stem Cells 2011 Nov;29(11):1727-37.
    doi: 10.1002/stem.720pmc: PMC3784258pubmed: 21898687google scholar: lookup
  55. Chen MJ, Whiteley JP, Please CP, Schwab A, Ehlicke F, Waters SL, Byrne HM. Inducing chondrogenesis in MSC/chondrocyte co-cultures using exogenous TGF-β: a mathematical model.. J Theor Biol 2018 Feb 14;439:1-13.
    doi: 10.1016/j.jtbi.2017.11.024pubmed: 29203122google scholar: lookup
  56. Dahlin RL, Ni M, Meretoja VV, Kasper FK, Mikos AG. TGF-β3-induced chondrogenesis in co-cultures of chondrocytes and mesenchymal stem cells on biodegradable scaffolds.. Biomaterials 2014 Jan;35(1):123-32.
    doi: 10.1016/j.biomaterials.2013.09.086pmc: PMC3844679pubmed: 24125773google scholar: lookup
  57. de Araújo Farias V, Carrillo-Gálvez AB, Martín F, Anderson P. TGF-β and mesenchymal stromal cells in regenerative medicine, autoimmunity and cancer.. Cytokine Growth Factor Rev 2018 Oct;43:25-37.
    doi: 10.1016/j.cytogfr.2018.06.002pubmed: 29954665google scholar: lookup
  58. Esebanmen GE, Langridge WHR. The role of TGF-beta signaling in dendritic cell tolerance.. Immunol Res 2017 Oct;65(5):987-994.
    doi: 10.1007/s12026-017-8944-9pubmed: 28845509google scholar: lookup
  59. Li X, Dong Y, Yin H, Qi Z, Wang D, Ren S. Mesenchymal stem cells induced regulatory dendritic cells from hemopoietic progenitor cells through Notch pathway and TGF-β synergistically.. Immunol Lett 2020 Jun;222:49-57.
    doi: 10.1016/j.imlet.2020.03.005pubmed: 32199868google scholar: lookup
  60. Liu KS, Fan XQ, Zhang L, Wen QN, Feng JH, Chen FC, Luo JM, Sun WB. Effects of recombinant human interleukin-10 on Treg cells, IL-10 and TGF-β in transplantation of rabbit skin.. Mol Med Rep 2014 Feb;9(2):639-44.
    doi: 10.3892/mmr.2013.1817pmc: PMC3896515pubmed: 24270972google scholar: lookup

Citations

This article has been cited 5 times.
  1. Rashid U, Saba E, Yousaf A, Tareen WA, Sarfraz A, Rhee MH, Sandhu MA. Autologous Platelet Lysate Is an Alternative to Fetal Bovine Serum for Canine Adipose-Derived Mesenchymal Stem Cell Culture and Differentiation. Animals (Basel) 2023 Aug 17;13(16).
    doi: 10.3390/ani13162655pubmed: 37627446google scholar: lookup
  2. Gaesser AM, Cianci JM, Even K, Linardi RL, Ruthel G, Barot D, Elkhenany H, Engiles JB, Ortved KF. Equine Bone Marrow-Derived MSCs and Their EVs Exhibit Different Immunomodulatory Effects on Cartilage Explants in an In Vitro Osteoarthritis Model. Cartilage 2025 Sep 25;:19476035251378693.
    doi: 10.1177/19476035251378693pubmed: 40995888google scholar: lookup
  3. Yaneselli K, Ávila G, Rossi A, Rial A, Castro S, Estradé MJ, Suárez G, Algorta A. Impact of different formulations of platelet lysate on proliferative and immune profile of equine mesenchymal stromal cells. Front Vet Sci 2024;11:1410855.
    doi: 10.3389/fvets.2024.1410855pubmed: 39161460google scholar: lookup
  4. Jammes M, Contentin R, Audigié F, Cassé F, Galéra P. Effect of pro-inflammatory cytokine priming and storage temperature of the mesenchymal stromal cell (MSC) secretome on equine articular chondrocytes. Front Bioeng Biotechnol 2023;11:1204737.
    doi: 10.3389/fbioe.2023.1204737pubmed: 37720315google scholar: lookup
  5. Li L, Hua S, You L, Zhong T. Secretome Derived from Mesenchymal Stem/Stromal Cells: A Promising Strategy for Diabetes and its Complications. Curr Stem Cell Res Ther 2024;19(10):1328-1350.
    doi: 10.2174/1574888X19666230913154544pubmed: 37711134google scholar: lookup
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