FREE SHIPPING over $40
OVER 10000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Frontiers in veterinary science2022; 9; 890302; doi: 10.3389/fvets.2022.890302

Functional properties of equine adipose-derived mesenchymal stromal cells cultured with equine platelet lysate.

Abstract: Successful translation of multipotent mesenchymal stromal cell (MSC)-based therapies into clinical reality relies on adequate cell production procedures. These should be available not only for human MSC, but also for MSC from animal species relevant to preclinical research and veterinary medicine. The cell culture medium supplementation is one of the critical aspects in MSC production. Therefore, we previously established a scalable protocol for the production of buffy-coat based equine platelet lysate (ePL). This ePL proved to be a suitable alternative to fetal bovine serum (FBS) for equine adipose-derived (AD-) MSC culture so far, as it supported AD-MSC proliferation and basic characteristics. The aim of the current study was to further analyze the functional properties of equine AD-MSC cultured with the same ePL, focusing on cell fitness, genetic stability and pro-angiogenic potency. All experiments were performed with AD-MSC from = 5 horses, which were cultured either in medium supplemented with 10% FBS, 10% ePL or 2.5% ePL. AD-MSC cultured with 2.5% ePL, which previously showed decreased proliferation potential, displayed higher apoptosis but lower senescence levels as compared to 10% ePL medium ( < 0.05). Non-clonal chromosomal aberrations occurred in 8% of equine AD-MSC cultivated with FBS and only in 4.8% of equine AD-MSC cultivated with 10% ePL. Clonal aberrations in the AD-MSC were neither observed in FBS nor in 10% ePL medium. Analysis of AD-MSC and endothelial cells in an indirect co-culture revealed that the ePL supported the pro-angiogenic effects of AD-MSC. In the 10% ePL group, more vascular endothelial growth factor (VEGF-A) was released and highest VEGF-A concentrations were reached in the presence of ePL and co-cultured cells ( < 0.05). Correspondingly, AD-MSC expressed the VEGF receptor-2 at higher levels in the presence of ePL ( < 0.05). Finally, AD-MSC and 10% ePL together promoted the growth of endothelial cells and induced the formation of vessel-like structures in two of the samples. These data further substantiate that buffy-coat-based ePL is a valuable supplement for equine AD-MSC culture media. The ePL does not only support stable equine AD-MSC characteristics as demonstrated before, but it also enhances their functional properties.
Copyright © 2022 Hagen, Niebert, Brandt, Holland, Melzer, Wehrend and Burk.
Get Full Text
Publication Date: 2022-08-09 PubMed ID: 36016806PubMed Central: PMC9395693DOI: 10.3389/fvets.2022.890302Google 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.
LinkedInCopy
  • 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.

This study investigated the use of equine platelet lysate (ePL) in culturing equine adipose-derived mesenchymal stromal cells (AD-MSCs), exploring the effects of ePL on cell behavior, genetic stability, and angiogenic potential. It concludes that ePL not only maintains the stable characteristics of equine AD-MSCs but also enhances their functional properties.

Cell Culturing and Adipose-Derived Mesenchymal Stromal Cells

  • The research highlights the importance of effective cell production procedures in translating the potential of mesenchymal stromal cell (MSC) therapies into clinical reality. Such procedures need to be developed and tailored not just for human MSCs, but also for those from animal species in areas like veterinary medicine and preclinical research.
  • The study focuses on equine adipose-derived mesenchymal stromal cells (AD-MSCs). These are cells isolated from the adipose (fat) tissue of horses, which have certain abilities like differentiation and self-renewal, making them a focus of many therapeutic and scientific research.

Role of Equine Platelet Lysate in Cell Culture

  • Equine platelet lysate (ePL) is an alternative to fetal bovine serum (FBS), a supplement often used in cell culture. The ePL was previously found to support the proliferation and basic characteristics of equine AD-MSCs.
  • In this study, the effects of ePL on the functional properties of AD-MSCs were further analyzed, with a focus on cell fitness, genetic stability, and pro-angiogenic potency – i.e., the capacity to promote new blood vessel formation.

Findings and Conclusions

  • AD-MSCs cultured with 2.5% ePL showed increased rates of apoptosis (programmed cell death) and decreased senescence levels compared to those cultured with 10% ePL.
  • Non-clonal chromosomal aberrations (random changes in chromosome structure or number) occurred less frequently in AD-MSCs cultured with ePL than in those cultured with FBS, suggesting that ePL might promote greater genetic stability.
  • ePL was found to support the pro-angiogenic effects of the AD-MSCs. In the presence of ePL, the cells exhibited increased expression of the vascular endothelial growth factor (VEGF) receptor-2, a key protein involved in angiogenesis. Furthermore, the ePL and the AD-MSCs together promoted the growth of endothelial cells and led to the formation of vessel-like structures in some samples.
  • These findings suggest that ePL is not only a feasible substitute for FBS in equine AD-MSC culture media, but it could actually enhance the functional properties of the cells.

Cite This Article

APA
Hagen A, Niebert S, Brandt VP, Holland H, Melzer M, Wehrend A, Burk J. (2022). Functional properties of equine adipose-derived mesenchymal stromal cells cultured with equine platelet lysate. Front Vet Sci, 9, 890302. https://doi.org/10.3389/fvets.2022.890302

Publication

Frontiers in veterinary science
ISSN: 2297-1769
NlmUniqueID: 101666658
Country: Switzerland
Language: English
Volume: 9
Pages: 890302
PII: 890302

Researcher Affiliations

Hagen, Alina
  • Equine Clinic (Surgery, Orthopedics), Justus-Liebig-University Giessen, Giessen, Germany.
Niebert, Sabine
  • Equine Clinic (Surgery, Orthopedics), Justus-Liebig-University Giessen, Giessen, Germany.
Brandt, Vivian-Pascal
  • Saxon Incubator for Clinical Translation (SIKT), University of Leipzig, Leipzig, Germany.
Holland, Heidrun
  • Saxon Incubator for Clinical Translation (SIKT), University of Leipzig, Leipzig, Germany.
Melzer, Michaela
  • Equine Clinic (Surgery, Orthopedics), Justus-Liebig-University Giessen, Giessen, Germany.
Wehrend, Axel
  • Clinic for Obstetrics, Gynecology and Andrology of Large and Small Animals, Justus-Liebig-University Giessen, Giessen, Germany.
Burk, Janina
  • Equine Clinic (Surgery, Orthopedics), Justus-Liebig-University Giessen, Giessen, Germany.

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 74 references
  1. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. Multilineage potential of adult human mesenchymal stem cells.. Science 1999 Apr 2;284(5411):143-7.
    doi: 10.1126/science.284.5411.143pubmed: 10102814google scholar: lookup
  2. Koch TG, Berg LC, Betts DH. Current and future regenerative medicine - principles, concepts, and therapeutic use of stem cell therapy and tissue engineering in equine medicine.. Can Vet J 2009 Feb;50(2):155-65.
    pmc: PMC2629419pubmed: 19412395
  3. 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.
    doi: 10.1016/j.jcyt.2016.11.011pubmed: 28017599google scholar: lookup
  4. Doucet C, Ernou I, Zhang Y, Llense JR, Begot L, Holy X, Lataillade JJ. Platelet lysates promote mesenchymal stem cell expansion: a safety substitute for animal serum in cell-based therapy applications.. J Cell Physiol 2005 Nov;205(2):228-36.
    doi: 10.1002/jcp.20391pubmed: 15887229google scholar: lookup
  5. Bieback K. Platelet lysate as replacement for fetal bovine serum in mesenchymal stromal cell cultures.. Transfus Med Hemother 2013 Oct;40(5):326-35.
    doi: 10.1159/000354061pmc: PMC3822281pubmed: 24273486google scholar: lookup
  6. van der Valk J, Brunner D, De Smet K, Fex Svenningsen A, Honegger P, Knudsen LE, Lindl T, Noraberg J, Price A, Scarino ML, Gstraunthaler G. Optimization of chemically defined cell culture media--replacing fetal bovine serum in mammalian in vitro methods.. Toxicol In Vitro 2010 Jun;24(4):1053-63.
    doi: 10.1016/j.tiv.2010.03.016pubmed: 20362047google scholar: lookup
  7. Burnouf T, Strunk D, Koh MB, Schallmoser K. Human platelet lysate: Replacing fetal bovine serum as a gold standard for human cell propagation?. Biomaterials 2016 Jan;76:371-87.
    doi: 10.1016/j.biomaterials.2015.10.065pubmed: 26561934google scholar: lookup
  8. European Medicines Agency London Committee for Medicinal Products for Human Use (CHMP). Guideline on the Use of Bovine Serum in the Manufacture of Human Biological Medicinal. 2013.
  9. Trento C, Bernardo ME, Nagler A, Kuçi S, Bornhäuser M, Köhl U, Strunk D, Galleu A, Sanchez-Guijo F, Gaipa G, Introna M, Bukauskas A, Le Blanc K, Apperley J, Roelofs H, Van Campenhout A, Beguin Y, Kuball J, Lazzari L, Avanzini MA, Fibbe W, Chabannon C, Bonini C, Dazzi F. Manufacturing Mesenchymal Stromal Cells for the Treatment of Graft-versus-Host Disease: A Survey among Centers Affiliated with the European Society for Blood and Marrow Transplantation.. Biol Blood Marrow Transplant 2018 Nov;24(11):2365-2370.
    doi: 10.1016/j.bbmt.2018.07.015pmc: PMC6299357pubmed: 30031938google scholar: lookup
  10. Seo JP, Tsuzuki N, Haneda S, Yamada K, Furuoka H, Tabata Y, Sasaki N. Comparison of allogeneic platelet lysate and fetal bovine serum for in vitro expansion of equine bone marrow-derived mesenchymal stem cells.. Res Vet Sci 2013 Oct;95(2):693-8.
    doi: 10.1016/j.rvsc.2013.04.024pubmed: 23683731google scholar: lookup
  11. 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
  12. 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
  13. Hagen A, Lehmann H, Aurich S, Bauer N, Melzer M, Moellerberndt J, Patané V, Schnabel CL, Burk J. Scalable Production of Equine Platelet Lysate for Multipotent Mesenchymal Stromal Cell Culture.. Front Bioeng Biotechnol 2020;8:613621.
    doi: 10.3389/fbioe.2020.613621pmc: PMC7859354pubmed: 33553119google scholar: lookup
  14. Hagen A, Holland H, Brandt VP, Doll CU, Häußler TC, Melzer M, Moellerberndt J, Lehmann H, Burk J. Platelet Lysate for Mesenchymal Stromal Cell Culture in the Canine and Equine Species: Analogous but Not the Same.. Animals (Basel) 2022 Jan 13;12(2).
    doi: 10.3390/ani12020189pmc: PMC8773277pubmed: 35049811google scholar: lookup
  15. 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
  16. Del Bue M, Riccò S, Conti V, Merli E, Ramoni R, Grolli S. Platelet lysate promotes in vitro proliferation of equine mesenchymal stem cells and tenocytes.. Vet Res Commun 2007 Aug;31 Suppl 1:289-92.
    doi: 10.1007/s11259-007-0099-zpubmed: 17682897google scholar: lookup
  17. Caprio CP, Andrews CH. The Effect of Replacing Fetal Bovine Serum with Platelet Releasate on the Characterization of MSCs. Undergraduate Research Scholars Program 2018.
  18. Vallés G, Bensiamar F, Crespo L, Arruebo M, Vilaboa N, Saldaña L. Topographical cues regulate the crosstalk between MSCs and macrophages.. Biomaterials 2015 Jan;37:124-33.
    doi: 10.1016/j.biomaterials.2014.10.028pmc: PMC4245715pubmed: 25453943google scholar: lookup
  19. Luk F, Carreras-Planella L, Korevaar SS, de Witte SFH, Borràs FE, Betjes MGH, Baan CC, Hoogduijn MJ, Franquesa M. Inflammatory Conditions Dictate the Effect of Mesenchymal Stem or Stromal Cells on B Cell Function.. Front Immunol 2017;8:1042.
    doi: 10.3389/fimmu.2017.01042pmc: PMC5581385pubmed: 28894451google scholar: lookup
  20. Herranz N, Gil J. Mechanisms and functions of cellular senescence.. J Clin Invest 2018 Apr 2;128(4):1238-1246.
    doi: 10.1172/JCI95148pmc: PMC5873888pubmed: 29608137google scholar: lookup
  21. D'Arcy MS. Cell death: a review of the major forms of apoptosis, necrosis and autophagy.. Cell Biol Int 2019 Jun;43(6):582-592.
    doi: 10.1002/cbin.11137pubmed: 30958602google scholar: lookup
  22. Alizadeh AH, Briah R, Villagomez DAF, King WA, Koch TG. Cell Identity, Proliferation, and Cytogenetic Assessment of Equine Umbilical Cord Blood Mesenchymal Stromal Cells.. Stem Cells Dev 2018 Dec 15;27(24):1729-1738.
    doi: 10.1089/scd.2018.0105pubmed: 30251918google scholar: lookup
  23. Crespo-Diaz R, Behfar A, Butler GW, Padley DJ, Sarr MG, Bartunek J, Dietz AB, Terzic A. Platelet lysate consisting of a natural repair proteome supports human mesenchymal stem cell proliferation and chromosomal stability.. Cell Transplant 2011;20(6):797-811.
    doi: 10.3727/096368910X543376pubmed: 21092406google scholar: lookup
  24. Trojahn Kølle SF, Oliveri RS, Glovinski PV, Kirchhoff M, Mathiasen AB, Elberg JJ, Andersen PS, Drzewiecki KT, Fischer-Nielsen A. Pooled human platelet lysate versus fetal bovine serum-investigating the proliferation rate, chromosome stability and angiogenic potential of human adipose tissue-derived stem cells intended for clinical use.. Cytotherapy 2013 Sep;15(9):1086-97.
    doi: 10.1016/j.jcyt.2013.01.217pubmed: 23602579google scholar: lookup
  25. Skific M, Golemovic M, Crkvenac-Gornik K, Vrhovac R, Golubic Cepulic B. Comparative Analysis of Biological and Functional Properties of Bone Marrow Mesenchymal Stromal Cells Expanded in Media with Different Platelet Lysate Content.. Cells Tissues Organs 2018;205(4):226-239.
    doi: 10.1159/000492581pubmed: 30223277google scholar: lookup
  26. Martinello T, Bronzini I, Maccatrozzo L, Iacopetti I, Sampaolesi M, Mascarello F, Patruno M. Cryopreservation does not affect the stem characteristics of multipotent cells isolated from equine peripheral blood.. Tissue Eng Part C Methods 2010 Aug;16(4):771-81.
    doi: 10.1089/ten.tec.2009.0512pubmed: 19839741google scholar: lookup
  27. Maia L, Landim-Alvarenga FC, Da Mota LS, De Assis Golim M, Laufer-Amorim R, De Vita B, Barberini DJ, Listoni AJ, De Moraes CN, Heckler MC, Amorim RM. Immunophenotypic, immunocytochemistry, ultrastructural, and cytogenetic characterization of mesenchymal stem cells from equine bone marrow.. Microsc Res Tech 2013 Jun;76(6):618-24.
    doi: 10.1002/jemt.22208pubmed: 23533133google scholar: lookup
  28. Mazurkevych A, Malyuk M, Bezdieniezhnykh N, Starodub L, Kharkevych Y, Brusko E. Immunophenotypic characterisation and cytogenetic analysis of mesenchymal stem cells from equine bone marrow and foal umbilical cords during in vitro culture. J Vet Res 2016 60:339–47.
    doi: 10.1515/jvetres-2016-0051google scholar: lookup
  29. Yong KW, Choi JR, Mohammadi M, Mitha AP, Sanati-Nezhad A, Sen A. Mesenchymal Stem Cell Therapy for Ischemic Tissues.. Stem Cells Int 2018;2018:8179075.
    doi: 10.1155/2018/8179075pmc: PMC6196793pubmed: 30402112google scholar: lookup
  30. Levoux J, Prola A, Lafuste P, Gervais M, Chevallier N, Koumaiha Z, Kefi K, Braud L, Schmitt A, Yacia A, Schirmann A, Hersant B, Sid-Ahmed M, Ben Larbi S, Komrskova K, Rohlena J, Relaix F, Neuzil J, Rodriguez AM. Platelets Facilitate the Wound-Healing Capability of Mesenchymal Stem Cells by Mitochondrial Transfer and Metabolic Reprogramming.. Cell Metab 2021 Feb 2;33(2):283-299.e9.
    doi: 10.1016/j.cmet.2020.12.006pubmed: 33400911google scholar: lookup
  31. Qian Y, Han Q, Chen W, Song J, Zhao X, Ouyang Y, Yuan W, Fan C. Platelet-Rich Plasma Derived Growth Factors Contribute to Stem Cell Differentiation in Musculoskeletal Regeneration.. Front Chem 2017;5:89.
    doi: 10.3389/fchem.2017.00089pmc: PMC5671651pubmed: 29164105google scholar: lookup
  32. Mahmoudian-Sani MR, Rafeei F, Amini R, Saidijam M. The effect of mesenchymal stem cells combined with platelet-rich plasma on skin wound healing.. J Cosmet Dermatol 2018 Oct;17(5):650-659.
    doi: 10.1111/jocd.12512pubmed: 29504236google scholar: lookup
  33. Hersant B, Sid-Ahmed M, Braud L, Jourdan M, Baba-Amer Y, Meningaud JP, Rodriguez AM. Platelet-Rich Plasma Improves the Wound Healing Potential of Mesenchymal Stem Cells through Paracrine and Metabolism Alterations.. Stem Cells Int 2019;2019:1234263.
    doi: 10.1155/2019/1234263pmc: PMC6875194pubmed: 31781232google scholar: lookup
  34. Becherucci V, Piccini L, Casamassima S, Bisin S, Gori V, Gentile F, Ceccantini R, De Rienzo E, Bindi B, Pavan P, Cunial V, Allegro E, Ermini S, Brugnolo F, Astori G, Bambi F. Human platelet lysate in mesenchymal stromal cell expansion according to a GMP grade protocol: a cell factory experience.. Stem Cell Res Ther 2018 May 2;9(1):124.
    doi: 10.1186/s13287-018-0863-8pmc: PMC5930506pubmed: 29720245google scholar: lookup
  35. Viau S, Lagrange A, Chabrand L, Lorant J, Charrier M, Rouger K, Alvarez I, Eap S, Delorme B. A highly standardized and characterized human platelet lysate for efficient and reproducible expansion of human bone marrow mesenchymal stromal cells.. Cytotherapy 2019 Jul;21(7):738-754.
    doi: 10.1016/j.jcyt.2019.04.053pubmed: 31133491google scholar: lookup
  36. Kirsch M, Rach J, Handke W, Seltsam A, Pepelanova I, Strauß S, Vogt P, Scheper T, Lavrentieva A. Comparative Analysis of Mesenchymal Stem Cell Cultivation in Fetal Calf Serum, Human Serum, and Platelet Lysate in 2D and 3D Systems.. Front Bioeng Biotechnol 2020;8:598389.
    doi: 10.3389/fbioe.2020.598389pmc: PMC7844400pubmed: 33520956google scholar: lookup
  37. Palombella S, Perucca Orfei C, Castellini G, Gianola S, Lopa S, Mastrogiacomo M, Moretti M, de Girolamo L. Systematic review and meta-analysis on the use of human platelet lysate for mesenchymal stem cell cultures: comparison with fetal bovine serum and considerations on the production protocol.. Stem Cell Res Ther 2022 Apr 4;13(1):142.
    doi: 10.1186/s13287-022-02815-1pmc: PMC8981660pubmed: 35379348google scholar: lookup
  38. Losi P, Barsotti MC, Foffa I, Buscemi M, De Almeida CV, Fabbri M, Gabbriellini S, Nocchi F, Ursino S, Urciuoli P, Mazzoni A, Soldani G. In vitro human cord blood platelet lysate characterisation with potential application in wound healing.. Int Wound J 2020 Feb;17(1):65-72.
    doi: 10.1111/iwj.13233pmc: PMC7948753pubmed: 31665826google scholar: lookup
  39. Tancharoen W, Aungsuchawan S, Markmee R, Narakornsak S, Pothacharoen P. The effects of human platelet lysate versus commercial endothelial growth medium on the endothelial differentiation potential of human amniotic fluid mesenchymal stem cells.. Heliyon 2020 Sep;6(9):e04873.
    doi: 10.1016/j.heliyon.2020.e04873pmc: PMC7509187pubmed: 32995597google scholar: lookup
  40. Burk J, Ribitsch I, Gittel C, Juelke H, Kasper C, Staszyk C, Brehm W. Growth and differentiation characteristics of equine mesenchymal stromal cells derived from different sources.. Vet J 2013 Jan;195(1):98-106.
    doi: 10.1016/j.tvjl.2012.06.004pubmed: 22841420google scholar: lookup
  41. Raudsepp T. Chromosomal Analysis. Equine Reproductive Procedures 2021 p. 89–95.
    doi: 10.1002/9781119556015.ch22google scholar: lookup
  42. Seabright M. Human chromosome banding.. Lancet 1972 Apr 29;1(7757):967.
    doi: 10.1016/S0140-6736(72)91541-3pubmed: 4112138google scholar: lookup
  43. Seabright M. The use of proteolytic enzymes for the mapping of structural rearrangements in the chromosomes of man.. Chromosoma 1972;36(2):204-10.
    doi: 10.1007/BF00285214pubmed: 5016007google scholar: lookup
  44. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR.. Nucleic Acids Res 2001 May 1;29(9):e45.
    doi: 10.1093/nar/29.9.e45pmc: PMC55695pubmed: 11328886google scholar: lookup
  45. McGowan-Jordan J, Hastings R, Moore S. Re: International System for Human Cytogenetic or Cytogenomic Nomenclature (ISCN): Some Thoughts, by T. Liehr.. Cytogenet Genome Res 2021;161(5):225-226.
    pubmed: 34407535doi: 10.1159/000516655google scholar: lookup
  46. 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.
    doi: 10.1080/14653240600855905pubmed: 16923606google scholar: lookup
  47. Campisi J, d'Adda di Fagagna F. Cellular senescence: when bad things happen to good cells.. Nat Rev Mol Cell Biol 2007 Sep;8(9):729-40.
    doi: 10.1038/nrm2233pubmed: 17667954google scholar: lookup
  48. Childs BG, Baker DJ, Kirkland JL, Campisi J, van Deursen JM. Senescence and apoptosis: dueling or complementary cell fates?. EMBO Rep 2014 Nov;15(11):1139-53.
    doi: 10.15252/embr.201439245pmc: PMC4253488pubmed: 25312810google scholar: lookup
  49. Schallmoser K, Bartmann C, Rohde E, Bork S, Guelly C, Obenauf AC, Reinisch A, Horn P, Ho AD, Strunk D, Wagner W. Replicative senescence-associated gene expression changes in mesenchymal stromal cells are similar under different culture conditions.. Haematologica 2010 Jun;95(6):867-74.
    doi: 10.3324/haematol.2009.011692pmc: PMC2878782pubmed: 20053868google scholar: lookup
  50. Neri S. Genetic Stability of Mesenchymal Stromal Cells for Regenerative Medicine Applications: A Fundamental Biosafety Aspect.. Int J Mol Sci 2019 May 15;20(10).
    doi: 10.3390/ijms20102406pmc: PMC6566307pubmed: 31096604google scholar: lookup
  51. Griffiths S, Baraniak PR, Copland IB, Nerem RM, McDevitt TC. Human platelet lysate stimulates high-passage and senescent human multipotent mesenchymal stromal cell growth and rejuvenation in vitro.. Cytotherapy 2013 Dec;15(12):1469-83.
    doi: 10.1016/j.jcyt.2013.05.020pubmed: 23981539google scholar: lookup
  52. Søndergaard RH, Follin B, Lund LD, Juhl M, Ekblond A, Kastrup J, Haack-Sørensen M. Senescence and quiescence in adipose-derived stromal cells: Effects of human platelet lysate, fetal bovine serum and hypoxia.. Cytotherapy 2017 Jan;19(1):95-106.
    doi: 10.1016/j.jcyt.2016.09.006pubmed: 27771213google scholar: lookup
  53. Refolo MG, D'Alessandro R, Lippolis C, Messa C, Carella N, Cavallini A, Carr BI. Modulation of Doxorubicin mediated growth inhibition of hepatocellular carcinoma cells by platelet lysates.. Anticancer Agents Med Chem 2014;14(8):1154-60.
    doi: 10.2174/1871520614666140604120226pubmed: 24934165google scholar: lookup
  54. Carr BI, Cavallini A, D'Alessandro R, Refolo MG, Lippolis C, Mazzocca A, Messa C. Platelet extracts induce growth, migration and invasion in human hepatocellular carcinoma in vitro.. BMC Cancer 2014 Jan 27;14:43.
    doi: 10.1186/1471-2407-14-43pmc: PMC3974148pubmed: 24468103google scholar: lookup
  55. Roemeling-van Rhijn M, de Klein A, Douben H, Pan Q, van der Laan LJ, Ijzermans JN, Betjes MG, Baan CC, Weimar W, Hoogduijn MJ. Culture expansion induces non-tumorigenic aneuploidy in adipose tissue-derived mesenchymal stromal cells.. Cytotherapy 2013 Nov;15(11):1352-61.
    doi: 10.1016/j.jcyt.2013.07.004pubmed: 24094487google scholar: lookup
  56. Bernardo ME, Zaffaroni N, Novara F, Cometa AM, Avanzini MA, Moretta A, Montagna D, Maccario R, Villa R, Daidone MG, Zuffardi O, Locatelli F. Human bone marrow derived mesenchymal stem cells do not undergo transformation after long-term in vitro culture and do not exhibit telomere maintenance mechanisms.. Cancer Res 2007 Oct 1;67(19):9142-9.
    doi: 10.1158/0008-5472.CAN-06-4690pubmed: 17909019google scholar: lookup
  57. Zaman WS, Makpol S, Sathapan S, Chua KH. Long-term in vitro expansion of human adipose-derived stem cells showed low risk of tumourigenicity.. J Tissue Eng Regen Med 2014 Jan;8(1):67-76.
    doi: 10.1002/term.1501pubmed: 22552847google scholar: lookup
  58. Schallmoser K, Rohde E, Reinisch A, Bartmann C, Thaler D, Drexler C, Obenauf AC, Lanzer G, Linkesch W, Strunk D. Rapid large-scale expansion of functional mesenchymal stem cells from unmanipulated bone marrow without animal serum.. Tissue Eng Part C Methods 2008 Sep;14(3):185-96.
    doi: 10.1089/ten.tec.2008.0060pubmed: 18620484google scholar: lookup
  59. Voga M, Adamic N, Vengust M, Majdic G. Stem Cells in Veterinary Medicine-Current State and Treatment Options.. Front Vet Sci 2020;7:278.
    doi: 10.3389/fvets.2020.00278pmc: PMC7326035pubmed: 32656249google scholar: lookup
  60. Schlosser S, Dennler C, Schweizer R, Eberli D, Stein JV, Enzmann V, Giovanoli P, Erni D, Plock JA. Paracrine effects of mesenchymal stem cells enhance vascular regeneration in ischemic murine skin.. Microvasc Res 2012 May;83(3):267-75.
    doi: 10.1016/j.mvr.2012.02.011pubmed: 22391452google scholar: lookup
  61. Kwon HM, Hur SM, Park KY, Kim CK, Kim YM, Kim HS, Shin HC, Won MH, Ha KS, Kwon YG, Lee DH, Kim YM. Multiple paracrine factors secreted by mesenchymal stem cells contribute to angiogenesis.. Vascul Pharmacol 2014 Oct;63(1):19-28.
    doi: 10.1016/j.vph.2014.06.004pubmed: 24998908google scholar: lookup
  62. Tao H, Han Z, Han ZC, Li Z. Proangiogenic Features of Mesenchymal Stem Cells and Their Therapeutic Applications.. Stem Cells Int 2016;2016:1314709.
    doi: 10.1155/2016/1314709pmc: PMC4736816pubmed: 26880933google scholar: lookup
  63. Gangadaran P, Rajendran RL, Lee HW, Kalimuthu S, Hong CM, Jeong SY, Lee SW, Lee J, Ahn BC. Extracellular vesicles from mesenchymal stem cells activates VEGF receptors and accelerates recovery of hindlimb ischemia.. J Control Release 2017 Oct 28;264:112-126.
    doi: 10.1016/j.jconrel.2017.08.022pubmed: 28837823google scholar: lookup
  64. Goerke SM, Plaha J, Hager S, Strassburg S, Torio-Padron N, Stark GB, Finkenzeller G. Human endothelial progenitor cells induce extracellular signal-regulated kinase-dependent differentiation of mesenchymal stem cells into smooth muscle cells upon cocultivation.. Tissue Eng Part A 2012 Dec;18(23-24):2395-405.
    doi: 10.1089/ten.tea.2012.0147pubmed: 22731749google scholar: lookup
  65. Conze P, van Schie HT, van Weeren R, Staszyk C, Conrad S, Skutella T, Hopster K, Rohn K, Stadler P, Geburek F. Effect of autologous adipose tissue-derived mesenchymal stem cells on neovascularization of artificial equine tendon lesions.. Regen Med 2014;9(6):743-57.
    doi: 10.2217/rme.14.55pubmed: 25431911google scholar: lookup
  66. Oswald J, Boxberger S, Jørgensen B, Feldmann S, Ehninger G, Bornhäuser M, Werner C. Mesenchymal stem cells can be differentiated into endothelial cells in vitro.. Stem Cells 2004;22(3):377-84.
    doi: 10.1634/stemcells.22-3-377pubmed: 15153614google scholar: lookup
  67. Haack-Sorensen M, Friis T, Bindslev L, Mortensen S, Johnsen HE, Kastrup J. Comparison of different culture conditions for human mesenchymal stromal cells for clinical stem cell therapy.. Scand J Clin Lab Invest 2008;68(3):192-203.
    doi: 10.1080/00365510701601681pubmed: 17852829google scholar: lookup
  68. Chiaverina G, di Blasio L, Monica V, Accardo M, Palmiero M, Peracino B, Vara-Messler M, Puliafito A, Primo L. Dynamic Interplay between Pericytes and Endothelial Cells during Sprouting Angiogenesis.. Cells 2019 Sep 19;8(9).
    doi: 10.3390/cells8091109pmc: PMC6770602pubmed: 31546913google scholar: lookup
  69. Maacha S, Sidahmed H, Jacob S, Gentilcore G, Calzone R, Grivel JC, Cugno C. Paracrine Mechanisms of Mesenchymal Stromal Cells in Angiogenesis.. Stem Cells Int 2020;2020:4356359.
    doi: 10.1155/2020/4356359pmc: PMC7085399pubmed: 32215017google scholar: lookup
  70. Carmeliet P, Jain RK. Molecular mechanisms and clinical applications of angiogenesis.. Nature 2011 May 19;473(7347):298-307.
    doi: 10.1038/nature10144pmc: PMC4049445pubmed: 21593862google scholar: lookup
  71. Schallmoser K, Bartmann C, Rohde E, Reinisch A, Kashofer K, Stadelmeyer E, Drexler C, Lanzer G, Linkesch W, Strunk D. Human platelet lysate can replace fetal bovine serum for clinical-scale expansion of functional mesenchymal stromal cells.. Transfusion 2007 Aug;47(8):1436-46.
    doi: 10.1111/j.1537-2995.2007.01220.xpubmed: 17655588google scholar: lookup
  72. Shibuya M. VEGF-VEGFR Signals in Health and Disease.. Biomol Ther (Seoul) 2014 Jan;22(1):1-9.
    doi: 10.4062/biomolther.2013.113pmc: PMC3936422pubmed: 24596615google scholar: lookup
  73. Esteves CL, Sheldrake TA, Dawson L, Menghini T, Rink BE, Amilon K, Khan N, Péault B, Donadeu FX. Equine Mesenchymal Stromal Cells Retain a Pericyte-Like Phenotype.. Stem Cells Dev 2017 Jul 1;26(13):964-972.
    doi: 10.1089/scd.2017.0017pmc: PMC5510672pubmed: 28376684google scholar: lookup
  74. Lozito TP, Kuo CK, Taboas JM, Tuan RS. Human mesenchymal stem cells express vascular cell phenotypes upon interaction with endothelial cell matrix.. J Cell Biochem 2009 Jul 1;107(4):714-22.
    doi: 10.1002/jcb.22167pmc: PMC5543930pubmed: 19415687google scholar: lookup

Citations

This article has been cited 3 times.
  1. Moellerberndt J, Hagen A, Niebert S, Büttner K, Burk J. Cytokines in equine platelet lysate and related blood products. Front Vet Sci 2023;10:1117829.
    doi: 10.3389/fvets.2023.1117829pubmed: 36968472google scholar: lookup
  2. Duysens J, Graide H, Niesten A, Mouithys-Mickalad A, Deby-Dupont G, Franck T, Ceusters J, Serteyn D. Culture and Immunomodulation of Equine Muscle-Derived Mesenchymal Stromal Cells: A Comparative Study of Innovative 2D versus 3D Models Using Equine Platelet Lysate. Cells 2024 Jul 31;13(15).
    doi: 10.3390/cells13151290pubmed: 39120320google scholar: lookup
  3. Moellerberndt J, Niebert S, Fey K, Hagen A, Burk J. Impact of platelet lysate on immunoregulatory characteristics of equine mesenchymal stromal cells. Front Vet Sci 2024;11:1385395.
    doi: 10.3389/fvets.2024.1385395pubmed: 38725585google scholar: lookup
Subscribe to our newsletter
Join 100,129 horse owners like you who receive our email updates on horse health and nutrition.