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Home / Equine Research Bank / Front Vet Sci / Interactions Between Allogeneic Mesenchymal Stromal Cells an...
Frontiers in veterinary science2021; 7; 617647; doi: 10.3389/fvets.2020.617647

Interactions Between Allogeneic Mesenchymal Stromal Cells and the Recipient Immune System: A Comparative Review With Relevance to Equine Outcomes.

Abstract: Despite significant immunosuppressive activity, allogeneic mesenchymal stromal cells (MSCs) carry an inherent risk of immune rejection when transferred into a recipient. In naïve recipients, this immune response is initially driven by the innate immune system, an immediate reaction to the foreign cells, and later, the adaptive immune system, a delayed response that causes cell death due to recognition of specific alloantigens by host cells and antibodies. This review describes the actions of MSCs to both suppress and activate the different arms of the immune system. We then review the survival and effectiveness of the currently used allogeneic MSC treatments.
Copyright © 2021 Kamm, Riley, Parlane, Gee and McIlwraith.
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Publication Date: 2021-01-13 PubMed ID: 33521090PubMed Central: PMC7838369DOI: 10.3389/fvets.2020.617647Google 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 paper reviews the interactions of mesenchymal stromal cells (MSCs) when transferred into a different organism, primarily focusing on the immune responses they induce and the implications this has for the use of allogeneic MSC treatments.

Interactions of Allogenic Mesenchymal Stromal Cells

  • This study looks into the complex interactions that occur when MSCs from one organism are transplanted into a different organism (allogenic transplantation). These are most commonly used in regenerative medicine due to their potential to differentiate into a variety of cell types.
  • Despite their potential benefits, allogenic MSCs face the inherent risk of being rejected by the recipient’s immune system, affecting cell survival and the efficacy of the treatment.

Immune Response to MSCs

  • In naive recipients(i.e. ones that have not been previously exposed to the transplanted cells), the immune response follows a twofold pattern.
  • Initially, the innate immune system triggers an immediate response to the foreign cells, leading to inflammation and destruction of the transplanted cells.
  • Subsequently, the adaptive immune system ensues a more specific and prolonged response that results in cell death due to alloantigens being recognized by host cells and antibodies. This can compromise the longevity and effectiveness of the MSC transplant.

MSCs’ Interaction with the Immune System

  • Mesenchymal stromal cells have a dual role in interacting with the immune system. On one hand, they exert a significant immunosuppressive activity, reducing the inflammation and immune response triggered by innate immunity, and promoting cell survival. This is critical for the survival of the transplants.
  • On the other hand, MSCs can also activate the immune system, potentially causing an adaptive immune response and leading to transplant rejection.

Survival and Effectiveness of Allogeneic MSC treatments

  • This paper further reviews the current state of allogeneic MSC treatments, focusing on their survival rates and their effectiveness in a clinical setting.
  • This includes discussing factors such as immunosuppressive conditioning of patients, the source of MSCs, the method of administration, and the extent of HLA mismatch, which can potentially affect the outcome of an allogeneic MSC transplant.

Cite This Article

APA
Kamm JL, Riley CB, Parlane N, Gee EK, McIlwraith CW. (2021). Interactions Between Allogeneic Mesenchymal Stromal Cells and the Recipient Immune System: A Comparative Review With Relevance to Equine Outcomes. Front Vet Sci, 7, 617647. https://doi.org/10.3389/fvets.2020.617647

Publication

Frontiers in veterinary science
ISSN: 2297-1769
NlmUniqueID: 101666658
Country: Switzerland
Language: English
Volume: 7
Pages: 617647
PII: 617647

Researcher Affiliations

Kamm, J Lacy
  • School of Veterinary Science, Massey University, Palmerston North, New Zealand.
Riley, Christopher B
  • School of Veterinary Science, Massey University, Palmerston North, New Zealand.
Parlane, Natalie
  • Hopkirk Laboratory, AgResearch, Palmerston North, New Zealand.
Gee, Erica K
  • School of Veterinary Science, Massey University, Palmerston North, New Zealand.
McIlwraith, C Wayne
  • Orthopaedic Research Center, C. Wayne McIlwraith Translational Medical Institute, Colorado State University, Fort Collins, CO, United States.

Conflict of Interest Statement

JLK and CWM are partners in Advanced Regenerative Therapies New Zealand. The remaining 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 103 references
  1. Squillaro T, Peluso G, Galderisi U. Clinical Trials With Mesenchymal Stem Cells: An Update.. Cell Transplant 2016;25(5):829-48.
    doi: 10.3727/096368915X689622pubmed: 26423725google scholar: lookup
  2. Chahal J, Gómez-Aristizábal A, Shestopaloff K, Bhatt S, Chaboureau A, Fazio A, Chisholm J, Weston A, Chiovitti J, Keating A, Kapoor M, Ogilvie-Harris DJ, Syed KA, Gandhi R, Mahomed NN, Marshall KW, Sussman MS, Naraghi AM, Viswanathan S. Bone Marrow Mesenchymal Stromal Cell Treatment in Patients with Osteoarthritis Results in Overall Improvement in Pain and Symptoms and Reduces Synovial Inflammation.. Stem Cells Transl Med 2019 Aug;8(8):746-757.
    doi: 10.1002/sctm.18-0183pmc: PMC6646697pubmed: 30964245google scholar: lookup
  3. Wilson A, Hodgson-Garms M, Frith JE, Genever P. Multiplicity of Mesenchymal Stromal Cells: Finding the Right Route to Therapy.. Front Immunol 2019;10:1112.
    doi: 10.3389/fimmu.2019.01112pmc: PMC6535495pubmed: 31164890google scholar: lookup
  4. Frisbie DD, Smith RK. Clinical update on the use of mesenchymal stem cells in equine orthopaedics.. Equine Vet J 2010 Jan;42(1):86-9.
    doi: 10.2746/042516409X477263pubmed: 20121921google scholar: lookup
  5. Peeters CM, Leijs MJ, Reijman M, van Osch GJ, Bos PK. Safety of intra-articular cell-therapy with culture-expanded stem cells in humans: a systematic literature review.. Osteoarthritis Cartilage 2013 Oct;21(10):1465-73.
    doi: 10.1016/j.joca.2013.06.025pubmed: 23831631google scholar: lookup
  6. Huang XP, Ludke A, Dhingra S, Guo J, Sun Z, Zhang L, Weisel RD, Li RK. Class II transactivator knockdown limits major histocompatibility complex II expression, diminishes immune rejection, and improves survival of allogeneic bone marrow stem cells in the infarcted heart.. FASEB J 2016 Sep;30(9):3069-82.
    doi: 10.1096/fj.201600331Rpubmed: 27221978google scholar: lookup
  7. Brohlin M, Kingham PJ, Novikova LN, Novikov LN, Wiberg M. Aging effect on neurotrophic activity of human mesenchymal stem cells.. PLoS One 2012;7(9):e45052.
    doi: 10.1371/journal.pone.0045052pmc: PMC3444498pubmed: 23028757google scholar: lookup
  8. Ardanaz N, Vázquez FJ, Romero A, Remacha AR, Barrachina L, Sanz A, Ranera B, Vitoria A, Albareda J, Prades M, Zaragoza P, Martín-Burriel I, Rodellar C. Inflammatory response to the administration of mesenchymal stem cells in an equine experimental model: effect of autologous, and single and repeat doses of pooled allogeneic cells in healthy joints.. BMC Vet Res 2016 Mar 31;12:65.
    doi: 10.1186/s12917-016-0692-xpmc: PMC4815220pubmed: 27029614google scholar: lookup
  9. Selmani Z, Naji A, Zidi I, Favier B, Gaiffe E, Obert L, Borg C, Saas P, Tiberghien P, Rouas-Freiss N, Carosella ED, Deschaseaux F. Human leukocyte antigen-G5 secretion by human mesenchymal stem cells is required to suppress T lymphocyte and natural killer function and to induce CD4+CD25highFOXP3+ regulatory T cells.. Stem Cells 2008 Jan;26(1):212-22.
    doi: 10.1634/stemcells.2007-0554pubmed: 17932417google scholar: lookup
  10. Remacha AR, Barrachina L, Álvarez-Arguedas S, Ranera B, Romero A, Vázquez FJ, Zaragoza P, Yañez R, Martín-Burriel I, Rodellar C. Expression of genes involved in immune response and in vitro immunosuppressive effect of equine MSCs.. Vet Immunol Immunopathol 2015 Jun 15;165(3-4):107-18.
    doi: 10.1016/j.vetimm.2015.04.004pubmed: 25977164google scholar: lookup
  11. Colbath AC, Dow SW, Phillips JN, McIlwraith CW, Goodrich LR. Autologous and Allogeneic Equine Mesenchymal Stem Cells Exhibit Equivalent Immunomodulatory Properties In Vitro.. Stem Cells Dev 2017 Apr 1;26(7):503-511.
    doi: 10.1089/scd.2016.0266pubmed: 27958776google scholar: lookup
  12. Ge W, Jiang J, Arp J, Liu W, Garcia B, Wang H. Regulatory T-cell generation and kidney allograft tolerance induced by mesenchymal stem cells associated with indoleamine 2,3-dioxygenase expression.. Transplantation 2010 Dec 27;90(12):1312-20.
    doi: 10.1097/TP.0b013e3181fed001pubmed: 21042238google scholar: lookup
  13. Ranera B, Antczak D, Miller D, Doroshenkova T, Ryan A, McIlwraith CW, Barry F. Donor-derived equine mesenchymal stem cells suppress proliferation of mismatched lymphocytes.. Equine Vet J 2016 Mar;48(2):253-60.
    doi: 10.1111/evj.12414pubmed: 25582202google scholar: lookup
  14. Consentius C, Reinke P, Volk HD. Immunogenicity of allogeneic mesenchymal stromal cells: what has been seen in vitro and in vivo?. Regen Med 2015;10(3):305-15.
    doi: 10.2217/rme.15.14pubmed: 25933239google scholar: lookup
  15. Moravej A, Karimi MH, Geramizadeh B, Hossein Aghdaie M, Kohi-Hoseinabadi O, Ebrahimnezhad S. Effect of Mesenchymal Stem Cells on ILT3 Expression in the Splenocytes of Skin Graft Recipient Mice.. Iran J Immunol 2016 Dec;13(4):274-288.
    pubmed: 27999239
  16. Khosravi M, Karimi MH, Hossein Aghdaie M, Kalani M, Naserian S, Bidmeshkipour A. Mesenchymal stem cells can induce regulatory T cells via modulating miR-126a but not miR-10a.. Gene 2017 Sep 5;627:327-336.
    doi: 10.1016/j.gene.2017.06.012pubmed: 28600182google scholar: lookup
  17. Girdlestone J. Mesenchymal stromal cells with enhanced therapeutic properties.. Immunotherapy 2016 Dec;8(12):1405-1416.
    doi: 10.2217/imt-2016-0098pubmed: 28000538google scholar: lookup
  18. Clinicaltrials.gov, terms MSC, auto-immune, graft vs host, transplant, (2020).
  19. Dunavin N, Dias A, Li M, McGuirk J. Mesenchymal Stromal Cells: What Is the Mechanism in Acute Graft-Versus-Host Disease?. Biomedicines 2017 Jul 1;5(3).
    doi: 10.3390/biomedicines5030039pmc: PMC5618297pubmed: 28671556google scholar: lookup
  20. Murphy KA. Basic concepts in immunology. Janeways Immunobiology 8th ed, New York, NY: Garland Science; (2012). p. 1–36.
  21. Murphy KA. The complement system and innate immunity. Janeways Immunobiology 8th ed New York, NY: Garland Science; (2012) p. 48–65.
  22. Gavin C, Meinke S, Heldring N, Heck KA, Achour A, Iacobaeus E, Höglund P, Le Blanc K, Kadri N. The Complement System Is Essential for the Phagocytosis of Mesenchymal Stromal Cells by Monocytes.. Front Immunol 2019;10:2249.
    doi: 10.3389/fimmu.2019.02249pmc: PMC6763726pubmed: 31616424google scholar: lookup
  23. Li Y, Lin F. Mesenchymal stem cells are injured by complement after their contact with serum.. Blood 2012 Oct 25;120(17):3436-43.
    doi: 10.1182/blood-2012-03-420612pmc: PMC3482856pubmed: 22966167google scholar: lookup
  24. Li Y, Fung J, Lin F. Local Inhibition of Complement Improves Mesenchymal Stem Cell Viability and Function After Administration.. Mol Ther 2016 Sep;24(9):1665-74.
    doi: 10.1038/mt.2016.142pmc: PMC5113108pubmed: 27377042google scholar: lookup
  25. Li Y, Qiu W, Zhang L, Fung J, Lin F. Painting factor H onto mesenchymal stem cells protects the cells from complement- and neutrophil-mediated damage.. Biomaterials 2016 Sep;102:209-19.
    doi: 10.1016/j.biomaterials.2016.05.055pmc: PMC5290709pubmed: 27343468google scholar: lookup
  26. Scozzi D, Ibrahim M, Menna C, Krupnick AS, Kreisel D, Gelman AE. The Role of Neutrophils in Transplanted Organs.. Am J Transplant 2017 Feb;17(2):328-335.
    doi: 10.1111/ajt.13940pmc: PMC5183560pubmed: 27344051google scholar: lookup
  27. Mardpour S, Hamidieh AA, Taleahmad S, Sharifzad F, Taghikhani A, Baharvand H. Interaction between mesenchymal stromal cell-derived extracellular vesicles and immune cells by distinct protein content.. J Cell Physiol 2019 Jun;234(6):8249-8258.
    doi: 10.1002/jcp.27669pubmed: 30378105google scholar: lookup
  28. Mumaw JL, Schmiedt CW, Breidling S, Sigmund A, Norton NA, Thoreson M, Peroni JF, Hurley DJ. Feline mesenchymal stem cells and supernatant inhibit reactive oxygen species production in cultured feline neutrophils.. Res Vet Sci 2015 Dec;103:60-9.
    doi: 10.1016/j.rvsc.2015.09.010pubmed: 26679797google scholar: lookup
  29. Mittal SK, Mashaghi A, Amouzegar A, Li M, Foulsham W, Sahu SK, Chauhan SK. Mesenchymal Stromal Cells Inhibit Neutrophil Effector Functions in a Murine Model of Ocular Inflammation.. Invest Ophthalmol Vis Sci 2018 Mar 1;59(3):1191-1198.
    doi: 10.1167/iovs.17-23067pmc: PMC5837663pubmed: 29625439google scholar: lookup
  30. Salami F, Tavassoli A, Mehrzad J, Parham A. Immunomodulatory effects of mesenchymal stem cells on leukocytes with emphasis on neutrophils.. Immunobiology 2018 Dec;223(12):786-791.
    doi: 10.1016/j.imbio.2018.08.002pubmed: 30119931google scholar: lookup
  31. Jiang D, Muschhammer J, Qi Y, Kügler A, de Vries JC, Saffarzadeh M, Sindrilaru A, Beken SV, Wlaschek M, Kluth MA, Ganss C, Frank NY, Frank MH, Preissner KT, Scharffetter-Kochanek K. Suppression of Neutrophil-Mediated Tissue Damage-A Novel Skill of Mesenchymal Stem Cells.. Stem Cells 2016 Sep;34(9):2393-406.
    doi: 10.1002/stem.2417pmc: PMC5572139pubmed: 27299700google scholar: lookup
  32. 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
  33. Barrachina L, Remacha AR, Romero A, Vitoria A, Albareda J, Prades M, Roca M, Zaragoza P, Vázquez FJ, Rodellar C. Assessment of effectiveness and safety of repeat administration of proinflammatory primed allogeneic mesenchymal stem cells in an equine model of chemically induced osteoarthritis.. BMC Vet Res 2018 Aug 17;14(1):241.
    doi: 10.1186/s12917-018-1556-3pmc: PMC6098603pubmed: 30119668google scholar: lookup
  34. Colbath AC, Dow SW, Hopkins LS, Phillips JN, McIlwraith CW, Goodrich LR. Allogeneic vs. autologous intra-articular mesenchymal stem cell injection within normal horses: Clinical and cytological comparisons suggest safety.. Equine Vet J 2020 Jan;52(1):144-151.
    doi: 10.1111/evj.13136pubmed: 31120574google scholar: lookup
  35. Chatzistamatiou TK, Papassavas AC, Michalopoulos E, Gamaloutsos C, Mallis P, Gontika I, Panagouli E, Koussoulakos SL, Stavropoulos-Giokas C. Optimizing isolation culture and freezing methods to preserve Wharton's jelly's mesenchymal stem cell (MSC) properties: an MSC banking protocol validation for the Hellenic Cord Blood Bank.. Transfusion 2014 Dec;54(12):3108-20.
    doi: 10.1111/trf.12743pubmed: 24894363google scholar: lookup
  36. Esmann L, Idel C, Sarkar A, Hellberg L, Behnen M, Möller S, van Zandbergen G, Klinger M, Köhl J, Bussmeyer U, Solbach W, Laskay T. Phagocytosis of apoptotic cells by neutrophil granulocytes: diminished proinflammatory neutrophil functions in the presence of apoptotic cells.. J Immunol 2010 Jan 1;184(1):391-400.
    doi: 10.4049/jimmunol.0900564pubmed: 19949068google scholar: lookup
  37. Williams LB, Koenig JB, Black B, Gibson TW, Sharif S, Koch TG. Equine allogeneic umbilical cord blood derived mesenchymal stromal cells reduce synovial fluid nucleated cell count and induce mild self-limiting inflammation when evaluated in an lipopolysaccharide induced synovitis model.. Equine Vet J 2016 Sep;48(5):619-25.
    doi: 10.1111/evj.12477pubmed: 26114736google scholar: lookup
  38. Broeckx S, Suls M, Beerts C, Vandenberghe A, Seys B, Wuertz-Kozak K, Duchateau L, Spaas JH. Allogenic mesenchymal stem cells as a treatment for equine degenerative joint disease: a pilot study.. Curr Stem Cell Res Ther 2014;9(6):497-503.
    doi: 10.2174/1574888X09666140826110601pubmed: 25175766google scholar: lookup
  39. 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.
    doi: 10.1111/j.1532-950X.2014.12100.xpubmed: 24433318google scholar: lookup
  40. Vega A, Martín-Ferrero MA, Del Canto F, Alberca M, García V, Munar A, Orozco L, Soler R, Fuertes JJ, Huguet M, Sánchez A, García-Sancho J. Treatment of Knee Osteoarthritis With Allogeneic Bone Marrow Mesenchymal Stem Cells: A Randomized Controlled Trial.. Transplantation 2015 Aug;99(8):1681-90.
    doi: 10.1097/TP.0000000000000678pubmed: 25822648google scholar: lookup
  41. Gupta PK, Chullikana A, Rengasamy M, Shetty N, Pandey V, Agarwal V, Wagh SY, Vellotare PK, Damodaran D, Viswanathan P, Thej C, Balasubramanian S, Majumdar AS. Efficacy and safety of adult human bone marrow-derived, cultured, pooled, allogeneic mesenchymal stromal cells (Stempeucel®): preclinical and clinical trial in osteoarthritis of the knee joint.. Arthritis Res Ther 2016 Dec 20;18(1):301.
    doi: 10.1186/s13075-016-1195-7pmc: PMC5168586pubmed: 27993154google scholar: lookup
  42. Lamo-Espinosa JM, Mora G, Blanco JF, Granero-Moltó F, Nuñez-Córdoba JM, Sánchez-Echenique C, Bondía JM, Aquerreta JD, Andreu EJ, Ornilla E, Villarón EM, Valentí-Azcárate A, Sánchez-Guijo F, Del Cañizo MC, Valentí-Nin JR, Prósper F. Intra-articular injection of two different doses of autologous bone marrow mesenchymal stem cells versus hyaluronic acid in the treatment of knee osteoarthritis: multicenter randomized controlled clinical trial (phase I/II).. J Transl Med 2016 Aug 26;14(1):246.
    doi: 10.1186/s12967-016-0998-2pmc: PMC5002157pubmed: 27565858google scholar: lookup
  43. Murray PJ, Wynn TA. Protective and pathogenic functions of macrophage subsets.. Nat Rev Immunol 2011 Oct 14;11(11):723-37.
    doi: 10.1038/nri3073pmc: PMC3422549pubmed: 21997792google scholar: lookup
  44. Chiossone L, Conte R, Spaggiari GM, Serra M, Romei C, Bellora F, Becchetti F, Andaloro A, Moretta L, Bottino C. Mesenchymal Stromal Cells Induce Peculiar Alternatively Activated Macrophages Capable of Dampening Both Innate and Adaptive Immune Responses.. Stem Cells 2016 Jul;34(7):1909-21.
    doi: 10.1002/stem.2369pubmed: 27015881google scholar: lookup
  45. 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
  46. Cassano JM, Schnabel LV, Goodale MB, Fortier LA. The immunomodulatory function of equine MSCs is enhanced by priming through an inflammatory microenvironment or TLR3 ligand.. Vet Immunol Immunopathol 2018 Jan;195:33-39.
    doi: 10.1016/j.vetimm.2017.10.003pubmed: 29249315google scholar: lookup
  47. Murphy KA. The induced responses of innate immunity. Janeways Immunobiology 8th ed, New York, NY: Garland Science; (2012). p. 75–98.
  48. Berglund AK, Fisher MB, Cameron KA, Poole EJ, Schnabel LV. Transforming Growth Factor-β2 Downregulates Major Histocompatibility Complex (MHC) I and MHC II Surface Expression on Equine Bone Marrow-Derived Mesenchymal Stem Cells Without Altering Other Phenotypic Cell Surface Markers.. Front Vet Sci 2017;4:84.
    doi: 10.3389/fvets.2017.00084pmc: PMC5466990pubmed: 28660198google scholar: lookup
  49. Kamm JL, Parlane NA, Riley CB, Gee EK, Dittmer KE, McIlwraith CW. Blood type and breed-associated differences in cell marker expression on equine bone marrow-derived mesenchymal stem cells including major histocompatibility complex class II antigen expression.. PLoS One 2019;14(11):e0225161.
    doi: 10.1371/journal.pone.0225161pmc: PMC6867698pubmed: 31747418google scholar: lookup
  50. Milosavljevic N, Gazdic M, Simovic Markovic B, Arsenijevic A, Nurkovic J, Dolicanin Z, Djonov V, Lukic ML, Volarevic V. Mesenchymal stem cells attenuate acute liver injury by altering ratio between interleukin 17 producing and regulatory natural killer T cells.. Liver Transpl 2017 Aug;23(8):1040-1050.
    doi: 10.1002/lt.24784pubmed: 28481005google scholar: lookup
  51. Li Y, Qu YH, Wu YF, Liu L, Lin XH, Huang K, Wei J. Bone marrow mesenchymal stem cells suppressing activation of allogeneic cytokine-induced killer/natural killer cells either by direct or indirect interaction.. Cell Biol Int 2015 Apr;39(4):435-45.
    doi: 10.1002/cbin.10404pubmed: 25492047google scholar: lookup
  52. Eisenbarth SC. Dendritic cell subsets in T cell programming: location dictates function.. Nat Rev Immunol 2019 Feb;19(2):89-103.
    doi: 10.1038/s41577-018-0088-1pmc: PMC7755085pubmed: 30464294google scholar: lookup
  53. Zhang Y, Ge XH, Guo XJ, Guan SB, Li XM, Gu W, Xu WG. Bone Marrow Mesenchymal Stem Cells Inhibit the Function of Dendritic Cells by Secreting Galectin-1.. Biomed Res Int 2017;2017:3248605.
    doi: 10.1155/2017/3248605pmc: PMC5497648pubmed: 28713822google scholar: lookup
  54. Haabeth OA, Tveita AA, Fauskanger M, Schjesvold F, Lorvik KB, Hofgaard PO, Omholt H, Munthe LA, Dembic Z, Corthay A, Bogen B. How Do CD4(+) T Cells Detect and Eliminate Tumor Cells That Either Lack or Express MHC Class II Molecules?. Front Immunol 2014;5:174.
    doi: 10.3389/fimmu.2014.00174pmc: PMC3995058pubmed: 24782871google scholar: lookup
  55. Hickey MJ, Valenzuela NM, Reed EF. Alloantibody Generation and Effector Function Following Sensitization to Human Leukocyte Antigen.. Front Immunol 2016;7:30.
    doi: 10.3389/fimmu.2016.00030pmc: PMC4740371pubmed: 26870045google scholar: lookup
  56. Pei J, Collisson EW. Specific antibody secreting cells from chickens can be detected by three days and memory B cells by three weeks post-infection with the avian respiratory coronavirus.. Dev Comp Immunol 2005;29(2):153-60.
    doi: 10.1016/j.dci.2004.06.009pmc: PMC7103210pubmed: 15450755google scholar: lookup
  57. Wood BA, Carver S, Troyer RM, Elder JH, VandeWoude S. Domestic cat microsphere immunoassays: detection of antibodies during feline immunodeficiency virus infection.. J Immunol Methods 2013 Oct 31;396(1-2):74-86.
    doi: 10.1016/j.jim.2013.08.001pmc: PMC3823060pubmed: 23954271google scholar: lookup
  58. Akondy RS, Fitch M, Edupuganti S, Yang S, Kissick HT, Li KW, Youngblood BA, Abdelsamed HA, McGuire DJ, Cohen KW, Alexe G, Nagar S, McCausland MM, Gupta S, Tata P, Haining WN, McElrath MJ, Zhang D, Hu B, Greenleaf WJ, Goronzy JJ, Mulligan MJ, Hellerstein M, Ahmed R. Origin and differentiation of human memory CD8 T cells after vaccination.. Nature 2017 Dec 21;552(7685):362-367.
    doi: 10.1038/nature24633pmc: PMC6037316pubmed: 29236685google scholar: lookup
  59. 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
  60. Hill JA, Cassano JM, Goodale MB, Fortier LA. Antigenicity of mesenchymal stem cells in an inflamed joint environment.. Am J Vet Res 2017 Jul;78(7):867-875.
    doi: 10.2460/ajvr.78.7.867pubmed: 28650243google scholar: lookup
  61. Barrachina L, Remacha AR, Romero A, Zaragoza P, Vázquez FJ, Rodellar C. Differentiation of equine bone marrow derived mesenchymal stem cells increases the expression of immunogenic genes.. Vet Immunol Immunopathol 2018 Jun;200:1-6.
    doi: 10.1016/j.vetimm.2018.04.004pubmed: 29776607google scholar: lookup
  62. 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
  63. Miller D, Tallmadge RL, Binns M, Zhu B, Mohamoud YA, Ahmed A, Brooks SA, Antczak DF. Polymorphism at expressed DQ and DR loci in five common equine MHC haplotypes.. Immunogenetics 2017 Mar;69(3):145-156.
    doi: 10.1007/s00251-016-0964-4pmc: PMC5316504pubmed: 27889800google scholar: lookup
  64. Berglund AK, Schnabel LV. Allogeneic major histocompatibility complex-mismatched equine bone marrow-derived mesenchymal stem cells are targeted for death by cytotoxic anti-major histocompatibility complex antibodies.. Equine Vet J 2017 Jul;49(4):539-544.
    doi: 10.1111/evj.12647pmc: PMC5425313pubmed: 27862236google scholar: lookup
  65. Bloom DD, Centanni JM, Bhatia N, Emler CA, Drier D, Leverson GE, McKenna DH Jr, Gee AP, Lindblad R, Hei DJ, Hematti P. A reproducible immunopotency assay to measure mesenchymal stromal cell-mediated T-cell suppression.. Cytotherapy 2015 Feb;17(2):140-51.
    doi: 10.1016/j.jcyt.2014.10.002pmc: PMC4297551pubmed: 25455739google scholar: lookup
  66. Wang Y, Zhang A, Ye Z, Xie H, Zheng S. Bone marrow-derived mesenchymal stem cells inhibit acute rejection of rat liver allografts in association with regulatory T-cell expansion.. Transplant Proc 2009 Dec;41(10):4352-6.
    doi: 10.1016/j.transproceed.2009.08.072pubmed: 20005397google scholar: lookup
  67. Prasanna SJ, Gopalakrishnan D, Shankar SR, Vasandan AB. Pro-inflammatory cytokines, IFNgamma and TNFalpha, influence immune properties of human bone marrow and Wharton jelly mesenchymal stem cells differentially.. PLoS One 2010 Feb 2;5(2):e9016.
    doi: 10.1371/journal.pone.0009016pmc: PMC2814860pubmed: 20126406google scholar: lookup
  68. Klinker MW, Marklein RA, Lo Surdo JL, Wei CH, Bauer SR. Morphological features of IFN-γ-stimulated mesenchymal stromal cells predict overall immunosuppressive capacity.. Proc Natl Acad Sci U S A 2017 Mar 28;114(13):E2598-E2607.
    doi: 10.1073/pnas.1617933114pmc: PMC5380055pubmed: 28283659google scholar: lookup
  69. Liu F, Qiu H, Xue M, Zhang S, Zhang X, Xu J, Chen J, Yang Y, Xie J. MSC-secreted TGF-β regulates lipopolysaccharide-stimulated macrophage M2-like polarization via the Akt/FoxO1 pathway.. Stem Cell Res Ther 2019 Nov 26;10(1):345.
    doi: 10.1186/s13287-019-1447-ypmc: PMC6878630pubmed: 31771622google scholar: lookup
  70. Darlan DM, Munir D, Putra A, Jusuf NK. MSCs-released TGFβ1 generate CD4(+)CD25(+)Foxp3(+) in T-reg cells of human SLE PBMC.. J Formos Med Assoc 2021 Jan;120(1 Pt 3):602-608.
    doi: 10.1016/j.jfma.2020.06.028pubmed: 32718891google scholar: lookup
  71. Pezzanite LM, Fortier LA, Antczak DF, Cassano JM, Brosnahan MM, Miller D, Schnabel LV. Equine allogeneic bone marrow-derived mesenchymal stromal cells elicit antibody responses in vivo.. Stem Cell Res Ther 2015 Apr 12;6(1):54.
    doi: 10.1186/s13287-015-0053-xpmc: PMC4414005pubmed: 25889095google scholar: lookup
  72. Montespan F, Deschaseaux F, Sensébé L, Carosella ED, Rouas-Freiss N. Osteodifferentiated mesenchymal stem cells from bone marrow and adipose tissue express HLA-G and display immunomodulatory properties in HLA-mismatched settings: implications in bone repair therapy.. J Immunol Res 2014;2014:230346.
    doi: 10.1155/2014/230346pmc: PMC4022112pubmed: 24877156google scholar: lookup
  73. Nasef A, Mathieu N, Chapel A, Frick J, François S, Mazurier C, Boutarfa A, Bouchet S, Gorin NC, Thierry D, Fouillard L. Immunosuppressive effects of mesenchymal stem cells: involvement of HLA-G.. Transplantation 2007 Jul 27;84(2):231-7.
    doi: 10.1097/01.tp.0000267918.07906.08pubmed: 17667815google scholar: lookup
  74. Pigott JH, Ishihara A, Wellman ML, Russell DS, Bertone AL. Investigation of the immune response to autologous, allogeneic, and xenogeneic mesenchymal stem cells after intra-articular injection in horses.. Vet Immunol Immunopathol 2013 Nov 15;156(1-2):99-106.
    doi: 10.1016/j.vetimm.2013.09.003pubmed: 24094688google scholar: lookup
  75. Kol A, Wood JA, Carrade Holt DD, Gillette JA, Bohannon-Worsley LK, Puchalski SM, Walker NJ, Clark KC, Watson JL, Borjesson DL. Multiple intravenous injections of allogeneic equine mesenchymal stem cells do not induce a systemic inflammatory response but do alter lymphocyte subsets in healthy horses.. Stem Cell Res Ther 2015 Apr 15;6(1):73.
    doi: 10.1186/s13287-015-0050-0pmc: PMC4446064pubmed: 25888916google scholar: lookup
  76. Gu LH, Zhang TT, Li Y, Yan HJ, Qi H, Li FR. Immunogenicity of allogeneic mesenchymal stem cells transplanted via different routes in diabetic rats.. Cell Mol Immunol 2015 Jul;12(4):444-55.
    doi: 10.1038/cmi.2014.70pmc: PMC4496541pubmed: 25242276google scholar: lookup
  77. Owens SD, Kol A, Walker NJ, Borjesson DL. Allogeneic Mesenchymal Stem Cell Treatment Induces Specific Alloantibodies in Horses.. Stem Cells Int 2016;2016:5830103.
    doi: 10.1155/2016/5830103pmc: PMC5018342pubmed: 27648075google scholar: lookup
  78. Sernee MF, Ploegh HL, Schust DJ. Why certain antibodies cross-react with HLA-A and HLA-G: epitope mapping of two common MHC class I reagents.. Mol Immunol 1998 Feb;35(3):177-88.
    doi: 10.1016/S0161-5890(98)00026-1pubmed: 9694518google scholar: lookup
  79. Gao B, Rong C, Porcheray F, Moore C, Girouard TC, Saidman SL, Wong W, Fu Y, Zorn E. Evidence to Support a Contribution of Polyreactive Antibodies to HLA Serum Reactivity.. Transplantation 2016 Jan;100(1):217-26.
    doi: 10.1097/TP.0000000000000840pmc: PMC5384715pubmed: 26285015google scholar: lookup
  80. Soland MA, Bego MG, Colletti E, Porada CD, Zanjani ED, St Jeor S, Almeida-Porada G. Modulation of human mesenchymal stem cell immunogenicity through forced expression of human cytomegalovirus us proteins.. PLoS One 2012;7(5):e36163.
    doi: 10.1371/journal.pone.0036163pmc: PMC3364258pubmed: 22666319google scholar: lookup
  81. Broeckx SY, Seys B, Suls M, Vandenberghe A, Mariën T, Adriaensen E, Declercq J, Van Hecke L, Braun G, Hellmann K, Spaas JH. Equine Allogeneic Chondrogenic Induced Mesenchymal Stem Cells Are an Effective Treatment for Degenerative Joint Disease in Horses.. Stem Cells Dev 2019 Mar 15;28(6):410-422.
    doi: 10.1089/scd.2018.0061pmc: PMC6441287pubmed: 30623737google scholar: lookup
  82. Magri C, Schramme M, Febre M, Cauvin E, Labadie F, Saulnier N, François I, Lechartier A, Aebischer D, Moncelet AS, Maddens S. Comparison of efficacy and safety of single versus repeated intra-articular injection of allogeneic neonatal mesenchymal stem cells for treatment of osteoarthritis of the metacarpophalangeal/metatarsophalangeal joint in horses: A clinical pilot study.. PLoS One 2019;14(8):e0221317.
    doi: 10.1371/journal.pone.0221317pmc: PMC6715221pubmed: 31465445google scholar: lookup
  83. Delco ML, Goodale M, Talts JF, Pownder SL, Koff MF, Miller AD, Nixon B, Bonassar LJ, Lundgren-Åkerlund E, Fortier LA. Integrin α10β1-Selected Mesenchymal Stem Cells Mitigate the Progression of Osteoarthritis in an Equine Talar Impact Model.. Am J Sports Med 2020 Mar;48(3):612-623.
    doi: 10.1177/0363546519899087pubmed: 32004077google scholar: lookup
  84. Van Loon VJ, Scheffer CJ, Genn HJ, Hoogendoorn AC, Greve JW. Clinical follow-up of horses treated with allogeneic equine mesenchymal stem cells derived from umbilical cord blood for different tendon and ligament disorders.. Vet Q 2014;34(2):92-7.
    doi: 10.1080/01652176.2014.949390pubmed: 25072527google scholar: lookup
  85. Lange-Consiglio A, Tassan S, Corradetti B, Meucci A, Perego R, Bizzaro D, Cremonesi F. Investigating the efficacy of amnion-derived compared with bone marrow-derived mesenchymal stromal cells in equine tendon and ligament injuries.. Cytotherapy 2013 Aug;15(8):1011-20.
    doi: 10.1016/j.jcyt.2013.03.002pubmed: 23602577google scholar: lookup
  86. Beerts C, Suls M, Broeckx SY, Seys B, Vandenberghe A, Declercq J, Duchateau L, Vidal MA, Spaas JH. Tenogenically Induced Allogeneic Peripheral Blood Mesenchymal Stem Cells in Allogeneic Platelet-Rich Plasma: 2-Year Follow-up after Tendon or Ligament Treatment in Horses.. Front Vet Sci 2017;4:158.
    doi: 10.3389/fvets.2017.00158pmc: PMC5622984pubmed: 29018808google scholar: lookup
  87. Vagnozzi RJ, Maillet M, Sargent MA, Khalil H, Johansen AKZ, Schwanekamp JA, York AJ, Huang V, Nahrendorf M, Sadayappan S, Molkentin JD. An acute immune response underlies the benefit of cardiac stem cell therapy.. Nature 2020 Jan;577(7790):405-409.
    doi: 10.1038/s41586-019-1802-2pmc: PMC6962570pubmed: 31775156google scholar: lookup
  88. Xia C, Cao J. Imaging the survival and utility of pre-differentiated allogeneic MSC in ischemic heart.. Biochem Biophys Res Commun 2013 Aug 23;438(2):382-7.
    doi: 10.1016/j.bbrc.2013.07.084pubmed: 23899528google scholar: lookup
  89. Tasso R, Ilengo C, Quarto R, Cancedda R, Caspi RR, Pennesi G. Mesenchymal stem cells induce functionally active T-regulatory lymphocytes in a paracrine fashion and ameliorate experimental autoimmune uveitis.. Invest Ophthalmol Vis Sci 2012 Feb;53(2):786-93.
    doi: 10.1167/iovs.11-8211pmc: PMC3317420pubmed: 22232435google scholar: lookup
  90. Guest DJ, Smith MR, Allen WR. Monitoring the fate of autologous and allogeneic mesenchymal progenitor cells injected into the superficial digital flexor tendon of horses: preliminary study.. Equine Vet J 2008 Mar;40(2):178-81.
    doi: 10.2746/042516408X276942pubmed: 18267891google scholar: lookup
  91. Guest DJ, Smith MR, Allen WR. Equine embryonic stem-like cells and mesenchymal stromal cells have different survival rates and migration patterns following their injection into damaged superficial digital flexor tendon.. Equine Vet J 2010 Oct;42(7):636-42.
    doi: 10.1111/j.2042-3306.2010.00112.xpubmed: 20840579google scholar: lookup
  92. Lacitignola L, Staffieri F, Rossi G, Francioso E, Crovace A. Survival of bone marrow mesenchymal stem cells labelled with red fluorescent protein in an ovine model of collagenase-induced tendinitis.. Vet Comp Orthop Traumatol 2014;27(3):204-9.
    doi: 10.3415/VCOT-13-09-0113pubmed: 24764044google scholar: lookup
  93. Braid LR, Wood CA, Wiese DM, Ford BN. Intramuscular administration potentiates extended dwell time of mesenchymal stromal cells compared to other routes.. Cytotherapy 2018 Feb;20(2):232-244.
    doi: 10.1016/j.jcyt.2017.09.013pubmed: 29167063google scholar: lookup
  94. Li M, Luo X, Lv X, Liu V, Zhao G, Zhang X, Cao W, Wang R, Wang W. In vivo human adipose-derived mesenchymal stem cell tracking after intra-articular delivery in a rat osteoarthritis model.. Stem Cell Res Ther 2016 Nov 10;7(1):160.
    doi: 10.1186/s13287-016-0420-2pmc: PMC5103374pubmed: 27832815google scholar: lookup
  95. Feng C, Luo X, He N, Xia H, Lv X, Zhang X, Li D, Wang F, He J, Zhang L, Lin X, Lin L, Yin H, He J, Wang J, Cao W, Wang R, Zhou G, Wang W. Efficacy and Persistence of Allogeneic Adipose-Derived Mesenchymal Stem Cells Combined with Hyaluronic Acid in Osteoarthritis After Intra-articular Injection in a Sheep Model.. Tissue Eng Part A 2018 Feb;24(3-4):219-233.
    doi: 10.1089/ten.tea.2017.0039pubmed: 28486025google scholar: lookup
  96. Wang AT, Feng Y, Jia HH, Zhao M, Yu H. Application of mesenchymal stem cell therapy for the treatment of osteoarthritis of the knee: A concise review.. World J Stem Cells 2019 Apr 26;11(4):222-235.
    doi: 10.4252/wjsc.v11.i4.222pmc: PMC6503460pubmed: 31110603google scholar: lookup
  97. Colbath AC, Dow SW, Hopkins LS, Phillips JN, McIlwraith CW, Goodrich LR. Single and repeated intra-articular injections in the tarsocrural joint with allogeneic and autologous equine bone marrow-derived mesenchymal stem cells are safe, but did not reduce acute inflammation in an experimental interleukin-1β model of synovitis.. Equine Vet J 2020 Jul;52(4):601-612.
    doi: 10.1111/evj.13222pmc: PMC7283005pubmed: 31821594google scholar: lookup
  98. Mahmoud EE, Adachi N, Mawas AS, Deie M, Ochi M. Multiple intra-articular injections of allogeneic bone marrow-derived stem cells potentially improve knee lesions resulting from surgically induced osteoarthritis: an animal study.. Bone Joint J 2019 Jul;101-B(7):824-831.
    doi: 10.1302/0301-620X.101B7.BJJ-2018-1532.R1pubmed: 31256666google scholar: lookup
  99. Dyson SJ. Medical management of superficial digital flexor tendonitis: a comparative study in 219 horses (1992-2000).. Equine Vet J 2004 Jul;36(5):415-9.
    doi: 10.2746/0425164044868422pubmed: 15253082google scholar: lookup
  100. Yuksel S, Guleç MA, Gultekin MZ, Adanır O, Caglar A, Beytemur O, Onur Küçükyıldırım B, Avcı A, Subaşı C, İnci Ç, Karaoz E. Comparison of the early period effects of bone marrow-derived mesenchymal stem cells and platelet-rich plasma on the Achilles tendon ruptures in rats.. Connect Tissue Res 2016 Sep;57(5):360-73.
    doi: 10.1080/03008207.2016.1189909pubmed: 27191749google scholar: lookup
  101. Khan MR, Dudhia J, David FH, De Godoy R, Mehra V, Hughes G, Dakin SG, Carr AJ, Goodship AE, Smith RKW. Bone marrow mesenchymal stem cells do not enhance intra-synovial tendon healing despite engraftment and homing to niches within the synovium.. Stem Cell Res Ther 2018 Jun 19;9(1):169.
    doi: 10.1186/s13287-018-0900-7pmc: PMC6009051pubmed: 29921317google scholar: lookup
  102. Lee SY, Kwon B, Lee K, Son YH, Chung SG. Therapeutic Mechanisms of Human Adipose-Derived Mesenchymal Stem Cells in a Rat Tendon Injury Model.. Am J Sports Med 2017 May;45(6):1429-1439.
    doi: 10.1177/0363546517689874pubmed: 28291954google scholar: lookup
  103. Giri J, Galipeau J. Mesenchymal stromal cell therapeutic potency is dependent upon viability, route of delivery, and immune match.. Blood Adv 2020 May 12;4(9):1987-1997.
    doi: 10.1182/bloodadvances.2020001711pmc: PMC7218435pubmed: 32384543google scholar: lookup

Citations

This article has been cited 6 times.
  1. Lopez-Yus M, García-Sobreviela MP, Del Moral-Bergos R, Arbones-Mainar JM. Gene Therapy Based on Mesenchymal Stem Cells Derived from Adipose Tissue for the Treatment of Obesity and Its Metabolic Complications.. Int J Mol Sci 2023 Apr 18;24(8).
    doi: 10.3390/ijms24087468pubmed: 37108631google scholar: lookup
  2. Leal Reis I, Lopes B, Sousa P, Sousa AC, Branquinho M, Caseiro AR, Pedrosa SS, Rêma A, Oliveira C, Porto B, Atayde L, Amorim I, Alvites R, Santos JM, Maurício AC. Allogenic Synovia-Derived Mesenchymal Stem Cells for Treatment of Equine Tendinopathies and Desmopathies-Proof of Concept.. Animals (Basel) 2023 Apr 11;13(8).
    doi: 10.3390/ani13081312pubmed: 37106875google scholar: lookup
  3. Cequier A, Vázquez FJ, Romero A, Vitoria A, Bernad E, García-Martínez M, Gascón I, Barrachina L, Rodellar C. The immunomodulation-immunogenicity balance of equine Mesenchymal Stem Cells (MSCs) is differentially affected by the immune cell response depending on inflammatory licensing and major histocompatibility complex (MHC) compatibility.. Front Vet Sci 2022;9:957153.
    doi: 10.3389/fvets.2022.957153pubmed: 36337202google scholar: lookup
  4. Watson-Levings RS, Palmer GD, Levings PP, Dacanay EA, Evans CH, Ghivizzani SC. Gene Therapy in Orthopaedics: Progress and Challenges in Pre-Clinical Development and Translation.. Front Bioeng Biotechnol 2022;10:901317.
    doi: 10.3389/fbioe.2022.901317pubmed: 35837555google scholar: lookup
  5. Cequier A, Romero A, Vázquez FJ, Vitoria A, Bernad E, Fuente S, Zaragoza P, Rodellar C, Barrachina L. Equine Mesenchymal Stem Cells Influence the Proliferative Response of Lymphocytes: Effect of Inflammation, Differentiation and MHC-Compatibility.. Animals (Basel) 2022 Apr 11;12(8).
    doi: 10.3390/ani12080984pubmed: 35454231google scholar: lookup
  6. Depuydt E, Broeckx SY, Chiers K, Patruno M, Da Dalt L, Duchateau L, Saunders J, Pille F, Martens A, Van Hecke L, Spaas JH. Cellular and Humoral Immunogenicity Investigation of Single and Repeated Allogeneic Tenogenic Primed Mesenchymal Stem Cell Treatments in Horses Suffering From Tendon Injuries.. Front Vet Sci 2021;8:789293.
    doi: 10.3389/fvets.2021.789293pubmed: 35281431google scholar: lookup
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