Comparison between adult and foetal adnexa derived equine post-natal mesenchymal stem cells.
Abstract: Little is known about the differences among adult and foetal equine mesenchymal stem cells (MSCs), and no data exist about their comparative ultrastructural morphology. The aim of this study was to describe and compare characteristics, immune properties, and ultrastructural morphology of equine adult (bone marrow: BM, and adipose tissue: AT) and foetal adnexa derived (umbilical cord blood: UCB, and Wharton's jelly: WJ) MSCs. Results: No differences were observed in proliferation during the first 3 passages. While migration ability was similar among cells, foetal MSCs showed a higher adhesion ability, forming smaller spheroids after hanging drop culture (P < 0.05). All MSCs differentiated toward adipogenic, chondrogenic and osteogenic lineages, only tenogenic differentiation was less evident for WJ-MSCs. Data obtained by PCR confirmed MHC1 expression and lack of MHC2 expression in all four cell types. Foetal adnexa MSCs were positive for genes specific for anti-inflammatory and angiogenic factors (IL6, IL8, ILβ1) and WJ-MSCs were the only positive for OCT4 pluripotency gene. At immunofluorescence all cells expressed typical mesenchymal markers (α-SMA, N-cadherin), except for BM-MSCs, which did not express N-cadherin. By transmission electron microscopy, it was observed that WJ-MSCs had a higher (P < 0.05) number of microvesicles compared to adult MSCs, and UCB-MSCs showed more microvesicles than BM-MSCs (P < 0.05). AT-MSCs had a lower number of mitochondria than WJ-MSCs (P < 0.05), and mitochondrial area was higher for WJ-MSCs compared to UCB and AT-MSCs (P < 0.05). Conclusions: Results demonstrate that MSCs from adult and foetal tissues have different characteristics, and foetal MSCs, particularly WJ derived ones, seem to have some charactestics that warrant further investigation into potential advantages for clinical application.
Publication Date: 2019-08-02 PubMed ID: 31375144PubMed Central: PMC6679462DOI: 10.1186/s12917-019-2023-5Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
- Journal Article
Summary
This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.
This research sought to explore and compare the characteristics, immune properties, and ultrastructural morphology of adult and foetal equine mesenchymal stem cells (MSCs). The outcomes demonstrated that both categories possess distinct attributes, particularly in the foetal MSCs derived from Wharton’s jelly, which might have potential advantages for clinical application.
Objective of the Research
- The primary objective of this study was to investigate and contrast the characteristics, immune properties, and ultrastructural morphology of both adult and foetal mesenchymal stem cells (MSCs) in horses.
- The researchers sought to fill a knowledge gap as prior to this, there was little information available comparing adult and foetal equine MSCs, particularly with regards to their ultrastructural morphology.
Methodology and Findings
The team observed the following:
- There was no noticeable variation in proliferation during the first three cell passages.
- The migration capacity was consistent across the cells, but the foetal MSCs displayed a higher adherence ability.
- All the MSCs showed differentiation potential towards adipogenic, chondrogenic and osteogenic lineages. However, Wharton’s jelly-MSCs (WJ-MSCs) showed less differentiation potential towards tenogenic lineages.
- Immune properties of the cells were also examined; all four cell sources (adult bone marrow and adipose tissue, and foetal umbilical cord blood and Wharton’s jelly) expressed MHC1 but not MHC2.
- Additionally, foetal MSCs were positive for genes specific for anti-inflammatory and angiogenic factors such as IL6, IL8, ILβ1. WJ-MSCs were unique in expressing the pluripotency gene OCT4.
- Regarding ultrastructure, WJ-MSCs had a higher number of microvesicles compared to adult MSCs, and UCB-MSCs showed more microvesicles than BM-MSCs. There were fewer mitochondria in AT-MSCs than WJ-MSCs, and the mitochondrial area was greater for WJ-MSCs compared to UCB and AT-MSCs.
Conclusion and Implications
- The results demonstrated that MSCs from adult and foetal tissues have different characteristics. Particularly, foetal MSCs, especially those derived from Wharton’s jelly, seemed to display some qualities that may present potential advantages for clinical application.
- The implications of this research potentially impact not only equine medicine but may also contribute to the broader field of stem cell research and its application in other animals or humans. It opens up avenues for future comparison studies of stem cells derived from different tissue sources.
Cite This Article
APA
Merlo B, Teti G, Lanci A, Burk J, Mazzotti E, Falconi M, Iacono E.
(2019).
Comparison between adult and foetal adnexa derived equine post-natal mesenchymal stem cells.
BMC Vet Res, 15(1), 277.
https://doi.org/10.1186/s12917-019-2023-5 Publication
Researcher Affiliations
- Department of Veterinary Medical Sciences, University of Bologna, via Tolara di Sopra 50, 40064, Ozzano Emilia, BO, Italy.
- Health Science and Technologies Interdepartmental Center for Industrial Research (HST-ICIR), University of Bologna, Bologna, Italy.
- Department for Biomedical and Neuromotor Sciences, University of Bologna, Bologna, Italy.
- Department of Veterinary Medical Sciences, University of Bologna, via Tolara di Sopra 50, 40064, Ozzano Emilia, BO, Italy.
- Saxon Incubator for Clinical Translation, University of Leipzig, Leipzig, Germany.
- Equine Clinic (Surgery), Justus Liebig University Giessen, Giessen, Germany.
- Department of Comparative Biomedical Sciences, University of Teramo, Teramo, Italy.
- Department for Biomedical and Neuromotor Sciences, University of Bologna, Bologna, Italy.
- Department of Veterinary Medical Sciences, University of Bologna, via Tolara di Sopra 50, 40064, Ozzano Emilia, BO, Italy. eleonora.iacono2@unibo.it.
- Health Science and Technologies Interdepartmental Center for Industrial Research (HST-ICIR), University of Bologna, Bologna, Italy. eleonora.iacono2@unibo.it.
MeSH Terms
- Adult Stem Cells / physiology
- Animals
- Cell Differentiation
- Cell Migration Assays
- Cell Proliferation
- Cellular Senescence
- Fetal Blood / cytology
- Horses
- Mesenchymal Stem Cells
- Wharton Jelly / cytology
Conflict of Interest Statement
The authors declare that they have no competing interests.
References
This article includes 56 references
- Kern S, Eichler H, Stoeve J, Klüter H, Bieback K. Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue.. Stem Cells 2006 May;24(5):1294-301.
- Montesinos JJ, Flores-Figueroa E, Castillo-Medina S, Flores-Guzmán P, Hernández-Estévez E, Fajardo-Orduña G, Orozco S, Mayani H. Human mesenchymal stromal cells from adult and neonatal sources: comparative analysis of their morphology, immunophenotype, differentiation patterns and neural protein expression.. Cytotherapy 2009;11(2):163-76.
- Zhang X, Hirai M, Cantero S, Ciubotariu R, Dobrila L, Hirsh A, Igura K, Satoh H, Yokomi I, Nishimura T, Yamaguchi S, Yoshimura K, Rubinstein P, Takahashi TA. Isolation and characterization of mesenchymal stem cells from human umbilical cord blood: reevaluation of critical factors for successful isolation and high ability to proliferate and differentiate to chondrocytes as compared to mesenchymal stem cells from bone marrow and adipose tissue.. J Cell Biochem 2011 Apr;112(4):1206-18.
- Cavallo C, Cuomo C, Fantini S, Ricci F, Tazzari PL, Lucarelli E, Donati D, Facchini A, Lisignoli G, Fornasari PM, Grigolo B, Moroni L. Comparison of alternative mesenchymal stem cell sources for cell banking and musculoskeletal advanced therapies.. J Cell Biochem 2011 May;112(5):1418-30.
- Christodoulou I, Kolisis FN, Papaevangeliou D, Zoumpourlis V. Comparative Evaluation of Human Mesenchymal Stem Cells of Fetal (Wharton's Jelly) and Adult (Adipose Tissue) Origin during Prolonged In Vitro Expansion: Considerations for Cytotherapy.. Stem Cells Int 2013;2013:246134.
- Toupadakis CA, Wong A, Genetos DC, Cheung WK, Borjesson DL, Ferraro GL, Galuppo LD, Leach JK, Owens SD, Yellowley CE. Comparison of the osteogenic potential of equine mesenchymal stem cells from bone marrow, adipose tissue, umbilical cord blood, and umbilical cord tissue.. Am J Vet Res 2010 Oct;71(10):1237-45.
- 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.
- Lange-Consiglio A, Corradetti B, Meucci A, Perego R, Bizzaro D, Cremonesi F. Characteristics of equine mesenchymal stem cells derived from amnion and bone marrow: in vitro proliferative and multilineage potential assessment.. Equine Vet J 2013 Nov;45(6):737-44.
- 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.
- Burk J, Gittel C, Heller S, Pfeiffer B, Paebst F, Ahrberg AB, Brehm W. Gene expression of tendon markers in mesenchymal stromal cells derived from different sources.. BMC Res Notes 2014 Nov 20;7:826.
- Pratheesh MD, Dubey PK, Gade NE, Nath A, Sivanarayanan TB, Madhu DN, Somal A, Baiju I, Sreekumar TR, Gleeja VL, Bhatt IA, Chandra V, Amarpal, Sharma B, Saikumar G, Taru Sharma G. Comparative study on characterization and wound healing potential of goat (Capra hircus) mesenchymal stem cells derived from fetal origin amniotic fluid and adult bone marrow.. Res Vet Sci 2017 Jun;112:81-88.
- Iacono E, Pascucci L, Rossi B, Bazzucchi C, Lanci A, Ceccoli M, Merlo B. Ultrastructural characteristics and immune profile of equine MSCs from fetal adnexa.. Reproduction 2017 Oct;154(4):509-519.
- Iacono E, Brunori L, Pirrone A, Pagliaro PP, Ricci F, Tazzari PL, Merlo B. Isolation, characterization and differentiation of mesenchymal stem cells from amniotic fluid, umbilical cord blood and Wharton's jelly in the horse.. Reproduction 2012 Apr;143(4):455-68.
- Li G, Zhang XA, Wang H, Wang X, Meng CL, Chan CY, Yew DT, Tsang KS, Li K, Tsai SN, Ngai SM, Han ZC, Lin MC, He ML, Kung HF. Comparative proteomic analysis of mesenchymal stem cells derived from human bone marrow, umbilical cord, and placenta: implication in the migration.. Proteomics 2009 Jan;9(1):20-30.
- Wang W, Itaka K, Ohba S, Nishiyama N, Chung UI, Yamasaki Y, Kataoka K. 3D spheroid culture system on micropatterned substrates for improved differentiation efficiency of multipotent mesenchymal stem cells.. Biomaterials 2009 May;30(14):2705-15.
- Kavanagh DP, Robinson J, Kalia N. Mesenchymal stem cell priming: fine-tuning adhesion and function.. Stem Cell Rev Rep 2014 Aug;10(4):587-99.
- Sart S, Tsai AC, Li Y, Ma T. Three-dimensional aggregates of mesenchymal stem cells: cellular mechanisms, biological properties, and applications.. Tissue Eng Part B Rev 2014 Oct;20(5):365-80.
- Zeisberg M, Neilson EG. Biomarkers for epithelial-mesenchymal transitions.. J Clin Invest 2009 Jun;119(6):1429-37.
- Mazurkevych A, Malyuk M, Bezdieniezhnykh N, Starodub L, Kharkevych Y, Brusko E, Gryzińska M, Andrzej JA. 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;60:339–347.
- 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.
- Lin CS, Ning H, Lin G, Lue TF. Is CD34 truly a negative marker for mesenchymal stromal cells?. Cytotherapy 2012 Nov;14(10):1159-63.
- Ranera B, Lyahyai J, Romero A, Vázquez FJ, Remacha AR, Bernal ML, Zaragoza P, Rodellar C, Martín-Burriel I. Immunophenotype and gene expression profiles of cell surface markers of mesenchymal stem cells derived from equine bone marrow and adipose tissue.. Vet Immunol Immunopathol 2011 Nov 15;144(1-2):147-54.
- Braun J, Hack A, Weis-Klemm M, Conrad S, Treml S, Kohler K, Walliser U, Skutella T, Aicher WK. Evaluation of the osteogenic and chondrogenic differentiation capacities of equine adipose tissue-derived mesenchymal stem cells.. Am J Vet Res 2010 Oct;71(10):1228-36.
- Pascucci L, Curina G, Mercati F, Marini C, Dall'Aglio C, Paternesi B, Ceccarelli P. Flow cytometric characterization of culture expanded multipotent mesenchymal stromal cells (MSCs) from horse adipose tissue: towards the definition of minimal stemness criteria.. Vet Immunol Immunopathol 2011 Dec 15;144(3-4):499-506.
- 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.
- 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.
- De Schauwer C, Goossens K, Piepers S, Hoogewijs MK, Govaere JL, Smits K, Meyer E, Van Soom A, Van de Walle GR. Characterization and profiling of immunomodulatory genes of equine mesenchymal stromal cells from non-invasive sources.. Stem Cell Res Ther 2014 Jan 13;5(1):6.
- Lamalice L, Le Boeuf F, Huot J. Endothelial cell migration during angiogenesis.. Circ Res 2007 Mar 30;100(6):782-94.
- György B, Szabó TG, Pásztói M, Pál Z, Misják P, Aradi B, László V, Pállinger E, Pap E, Kittel A, Nagy G, Falus A, Buzás EI. Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles.. Cell Mol Life Sci 2011 Aug;68(16):2667-88.
- Miki T, Lehmann T, Cai H, Stolz DB, Strom SC. Stem cell characteristics of amniotic epithelial cells.. Stem Cells 2005 Nov-Dec;23(10):1549-59.
- Izumi M, Pazin BJ, Minervini CF, Gerlach J, Ross MA, Stolz DB, Turner ME, Thompson RL, Miki T. Quantitative comparison of stem cell marker-positive cells in fetal and term human amnion.. J Reprod Immunol 2009 Jul;81(1):39-43.
- De Coppi P, Bartsch G Jr, Siddiqui MM, Xu T, Santos CC, Perin L, Mostoslavsky G, Serre AC, Snyder EY, Yoo JJ, Furth ME, Soker S, Atala A. Isolation of amniotic stem cell lines with potential for therapy.. Nat Biotechnol 2007 Jan;25(1):100-6.
- Pirjali T, Azarpira N, Ayatollahi M, Aghdaie MH, Geramizadeh B, Talai T. Isolation and Characterization of Human Mesenchymal Stem Cells Derived from Human Umbilical Cord Wharton's Jelly and Amniotic Membrane.. Int J Organ Transplant Med 2013;4(3):111-6.
- Shaer A, Azarpira N, Aghdaie MH, Esfandiari E. Isolation and characterization of Human Mesenchymal Stromal Cells Derived from Placental Decidua Basalis; Umbilical cord Wharton's Jelly and Amniotic Membrane.. Pak J Med Sci 2014 Sep;30(5):1022-6.
- Iacono E, Rossi B, Merlo B. Stem cells from foetal adnexa and fluid in domestic animals: an update on their features and clinical application.. Reprod Domest Anim 2015 Jun;50(3):353-64.
- Desmarais JA, Demers SP, Suzuki J Jr, Laflamme S, Vincent P, Laverty S, Smith LC. Trophoblast stem cell marker gene expression in inner cell mass-derived cells from parthenogenetic equine embryos.. Reproduction 2011 Mar;141(3):321-32.
- Warthemann R, Eildermann K, Debowski K, Behr R. False-positive antibody signals for the pluripotency factor OCT4A (POU5F1) in testis-derived cells may lead to erroneous data and misinterpretations.. Mol Hum Reprod 2012 Dec;18(12):605-12.
- Guo CL, Liu L, Jia YD, Zhao XY, Zhou Q, Wang L. A novel variant of Oct3/4 gene in mouse embryonic stem cells.. Stem Cell Res 2012 Sep;9(2):69-76.
- Hwang JY, Oh JN, Lee DK, Choi KH, Park CH, Lee CK. Identification and differential expression patterns of porcine OCT4 variants.. Reproduction 2015 Jan;149(1):55-66.
- Liedtke S, Enczmann J, Waclawczyk S, Wernet P, Kögler G. Oct4 and its pseudogenes confuse stem cell research.. Cell Stem Cell 2007 Oct 11;1(4):364-6.
- Teti G, Cavallo C, Grigolo B, Giannini S, Facchini A, Mazzotti A, Falconi M. Ultrastructural analysis of human bone marrow mesenchymal stem cells during in vitro osteogenesis and chondrogenesis.. Microsc Res Tech 2012 May;75(5):596-604.
- Merlo B, Teti G, Mazzotti E, Ingrà L, Salvatore V, Buzzi M, Cerqueni G, Dicarlo M, Lanci A, Castagnetti C, Iacono E. Wharton's Jelly Derived Mesenchymal Stem Cells: Comparing Human and Horse.. Stem Cell Rev Rep 2018 Aug;14(4):574-584.
- García-Prat L, Martínez-Vicente M, Muñoz-Cánoves P. Autophagy: a decisive process for stemness.. Oncotarget 2016 Mar 15;7(11):12286-8.
- Sbrana FV, Cortini M, Avnet S, Perut F, Columbaro M, De Milito A, Baldini N. The Role of Autophagy in the Maintenance of Stemness and Differentiation of Mesenchymal Stem Cells.. Stem Cell Rev Rep 2016 Dec;12(6):621-633.
- Biancone L, Bruno S, Deregibus MC, Tetta C, Camussi G. Therapeutic potential of mesenchymal stem cell-derived microvesicles.. Nephrol Dial Transplant 2012 Aug;27(8):3037-42.
- Suldina LA, Morozova KN, Menzorov AG, Kizilova EA, Kiseleva E. Mitochondria structural reorganization during mouse embryonic stem cell derivation.. Protoplasma 2018 Sep;255(5):1373-1386.
- Sheng ZH. The Interplay of Axonal Energy Homeostasis and Mitochondrial Trafficking and Anchoring.. Trends Cell Biol 2017 Jun;27(6):403-416.
- Devine MJ, Kittler JT. Mitochondria at the neuronal presynapse in health and disease.. Nat Rev Neurosci 2018 Jan 19;19(2):63-80.
- Rainaldi G, Pinto B, Piras A, Vatteroni L, Simi S, Citti L. Reduction of proliferative heterogeneity of CHEF18 Chinese hamster cell line during the progression toward tumorigenicity.. In Vitro Cell Dev Biol 1991 Dec;27A(12):949-52.
- Bellotti C, Duchi S, Bevilacqua A, Lucarelli E, Piccinini F. Long term morphological characterization of mesenchymal stromal cells 3D spheroids built with a rapid method based on entry-level equipment.. Cytotechnology 2016 Dec;68(6):2479-2490.
- Lovati AB, Corradetti B, Cremonesi F, Bizzaro D, Consiglio AL. Tenogenic differentiation of equine mesenchymal progenitor cells under indirect co-culture.. Int J Artif Organs 2012 Nov;35(11):996-1005.
- Mohanty N, Gulati BR, Kumar R, Gera S, Kumar P, Somasundaram RK, Kumar S. Immunophenotypic characterization and tenogenic differentiation of mesenchymal stromal cells isolated from equine umbilical cord blood.. In Vitro Cell Dev Biol Anim 2014 Jun;50(6):538-48.
- Corradetti B, Lange-Consiglio A, Barucca M, Cremonesi F, Bizzaro D. Size-sieved subpopulations of mesenchymal stem cells from intervascular and perivascular equine umbilical cord matrix.. Cell Prolif 2011 Aug;44(4):330-42.
- Jischa S, Walter I, Nowotny N, Palm F, Budik S, Kolodziejek J, Aurich C. Uterine involution and endometrial function in postpartum pony mares.. Am J Vet Res 2008 Nov;69(11):1525-34.
- Castagnetti C, Mariella J, Pirrone A, Cinotti S, Mari G, Peli A. Expression of interleukin-1β, interleukin-8, and interferon-γ in blood samples obtained from healthy and sick neonatal foals.. Am J Vet Res 2012 Sep;73(9):1418-27.
- Visser MB, Pollitt CC. Lamellar leukocyte infiltration and involvement of IL-6 during oligofructose-induced equine laminitis development.. Vet Immunol Immunopathol 2011 Nov 15;144(1-2):120-8.
Citations
This article has been cited 7 times.- Stage HJ, Trappe S, Söllig K, Trachsel DS, Kirsch K, Zieger C, Merle R, Aschenbach JR, Gehlen H. Multilineage Differentiation Potential of Equine Adipose-Derived Stromal/Stem Cells from Different Sources.. Animals (Basel) 2023 Apr 15;13(8).
- Heyman E, Meeremans M, Devriendt B, Olenic M, Chiers K, De Schauwer C. Validation of a color deconvolution method to quantify MSC tri-lineage differentiation across species.. Front Vet Sci 2022;9:987045.
- Iacono E, Merlo B. Stem Cells in Domestic Animals: Applications in Health and Production.. Animals (Basel) 2022 Oct 13;12(20).
- Iacono E, Lanci A, Gugole P, Merlo B. Shipping Temperature, Time and Media Effects on Equine Wharton's Jelly and Adipose Tissue Derived Mesenchymal Stromal Cells Characteristics.. Animals (Basel) 2022 Aug 3;12(15).
- Wang P, Zhang S, Meng Q, Zhu P, Yuan W. Treatment and application of stem cells from different sources for cartilage injury: a literature review.. Ann Transl Med 2022 May;10(10):610.
- Iacono E, Marcoccia R, Merlo B. Current Status on Canine Foetal Fluid and Adnexa Derived Mesenchymal Stem Cells.. Animals (Basel) 2021 Jul 30;11(8).
- Marcoccia R, Nesci S, Merlo B, Ballotta G, Algieri C, Pagliarani A, Iacono E. Biological characteristics and metabolic profile of canine mesenchymal stem cells isolated from adipose tissue and umbilical cord matrix.. PLoS One 2021;16(3):e0247567.
Use Nutrition Calculator
Check if your horse's diet meets their nutrition requirements with our easy-to-use tool Check your horse's diet with our easy-to-use tool
Talk to a Nutritionist
Discuss your horse's feeding plan with our experts over a free phone consultation Discuss your horse's diet over a phone consultation
Submit Diet Evaluation
Get a customized feeding plan for your horse formulated by our equine nutritionists Get a custom feeding plan formulated by our nutritionists