Abstract: Adipose tissue-derived stromal cells (ADSCs) have generated considerable interest in the field of veterinary medicine, particularly for their potential in therapeutic strategies focused on bone regeneration. These cells possess unique biological characteristics, including their regenerative capacity and their ability to produce bioactive molecules. However, it is crucial to recognize that the characteristics of ADSCs can vary depending on the animal species and the site from which they are derived, such as the subcutaneous and visceral regions (SCAT and VAT, respectively). Thus, the present work aimed to comprehensively review the different traits of ADSCs isolated from diverse anatomical sites in companion animals, i.e., dogs, cats, and horses, in terms of immunophenotype, morphology, proliferation, and osteogenic differentiation potential. The findings indicate that the immunophenotype, proliferation, and osteogenic potential of ADSCs differ according to tissue origin and species. Generally, the proliferation rate is higher in VAT-derived ADSCs in dogs and horses, whereas in cats, the proliferation rate appears to be similar in both cells isolated from SCAT and VAT regions. In terms of osteogenic differentiation potential, VAT-derived ADSCs demonstrate the highest capability in cats, whereas SCAT-derived ADSCs exhibit superior potential in horses. Interestingly, in dogs, VAT-derived cells appear to have greater potential than those isolated from SCAT. Within the VAT, ADSCs derived from the falciform ligament and omentum show increased osteogenic potential, compared to cells isolated from other anatomical locations. Consequently, considering these disparities, optimizing isolation protocols becomes pivotal, tailoring them to the specific target species and therapeutic aims, and judiciously selecting the anatomical site for ADSC isolation. This approach holds promise to enhance the efficacy of ADSCs-based bone regenerative therapies.
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.
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.
Overview
This research investigates how the source location of adipose tissue-derived stromal cells (ADSCs) in companion animals affects their biological characteristics and ability to support bone regeneration.
The study reviews differences in cell properties depending on anatomical site and species—specifically in dogs, cats, and horses—to guide improved therapeutic applications.
Introduction to ADSCs and Their Importance
Adipose tissue-derived stromal cells (ADSCs) are multipotent cells found in fat tissue that have the ability to regenerate tissue and produce bioactive molecules.
These properties make ADSCs valuable for veterinary regenerative medicine, especially for treatments aimed at repairing and regenerating bone.
However, the characteristics of ADSCs vary based on the species of the animal and the anatomical location of the adipose tissue from which they’re isolated.
Two primary fat locations of interest are subcutaneous adipose tissue (SCAT) and visceral adipose tissue (VAT).
Aim of the Study
To comprehensively review and compare ADSCs from different anatomical fat deposits in dogs, cats, and horses.
Focus on evaluating key biological traits: immunophenotype (surface markers), morphology, cell proliferation rates, and the potential for osteogenic (bone-forming) differentiation.
Key Findings on Biological Profiles
Immunophenotype: ADSCs display varying surface markers depending on the tissue origin and species, affecting their identification and functional capacity.
Proliferation:
In dogs and horses, VAT-derived ADSCs proliferate at a higher rate compared to those from SCAT.
In cats, proliferation rates are similar regardless of whether ADSCs are isolated from SCAT or VAT.
Morphology: While details were less emphasized, morphology differences may correlate with the origin site and impact differentiation potential.
Osteogenic Differentiation Potential by Species and Anatomical Site
Cats: ADSCs from VAT have greater bone-forming potential than those from SCAT.
Horses: SCAT-derived ADSCs show superior osteogenic capacity compared to VAT-derived cells.
Dogs: Cells from VAT generally have higher osteogenic potential than those from SCAT.
Within the VAT, cells isolated from specific sites like the falciform ligament and omentum exhibit enhanced osteogenic differentiation capability relative to other VAT locations.
Implications for Veterinary Regenerative Medicine
The findings highlight the importance of carefully selecting the anatomical fat site when isolating ADSCs for therapeutic applications.
Species-specific differences mean that generalized protocols may not be optimal; isolation and culture methods should be customized according to the target animal and the intended regenerative goal.
Optimizing ADSC source selection and preparation can potentially improve the success rates and efficiency of bone regeneration treatments in companion animals.
Understanding these variations in ADSC biological profiles aids in advancing precision medicine approaches within veterinary care.
Conclusion
The anatomical origin of adipose tissue-derived stromal cells strongly influences their biological characteristics and osteogenic potential in dogs, cats, and horses.
Accounting for these differences by tailoring isolation practices according to species and fat depot source is essential to maximize the therapeutic effectiveness of ADSCs-based bone regeneration therapies.
This research provides a foundation for refining regenerative strategies in veterinary medicine, paving the way for improved clinical outcomes in companion animals.
Cite This Article
APA
Ferreira-Baptista C, Ferreira R, Fernandes MH, Gomes PS, Colaço B.
(2023).
Influence of the Anatomical Site on Adipose Tissue-Derived Stromal Cells’ Biological Profile and Osteogenic Potential in Companion Animals.
Vet Sci, 10(12), 673.
https://doi.org/10.3390/vetsci10120673
Centre for the Research and Technology of Agro-Environmental and Biological Sciences (CITAB), University of Trás-os-Montes e Alto Douro (UTAD), 5000-801 Vila Real, Portugal.
BoneLab-Laboratory for Bone Metabolism and Regeneration, Faculty of Dental Medicine, University of Porto, 4200-393 Porto, Portugal.
REQUIMTE/LAQV, University of Porto, 4100-007 Porto, Portugal.
REQUIMTE/LAQV, Department of Chemistry, University of Aveiro, 3810-193 Aveiro, Portugal.
Ferreira, Rita
REQUIMTE/LAQV, Department of Chemistry, University of Aveiro, 3810-193 Aveiro, Portugal.
Fernandes, Maria Helena
BoneLab-Laboratory for Bone Metabolism and Regeneration, Faculty of Dental Medicine, University of Porto, 4200-393 Porto, Portugal.
REQUIMTE/LAQV, University of Porto, 4100-007 Porto, Portugal.
Gomes, Pedro Sousa
BoneLab-Laboratory for Bone Metabolism and Regeneration, Faculty of Dental Medicine, University of Porto, 4200-393 Porto, Portugal.
REQUIMTE/LAQV, University of Porto, 4100-007 Porto, Portugal.
Colaço, Bruno
Centre for the Research and Technology of Agro-Environmental and Biological Sciences (CITAB), University of Trás-os-Montes e Alto Douro (UTAD), 5000-801 Vila Real, Portugal.
REQUIMTE/LAQV, University of Porto, 4100-007 Porto, Portugal.
CECAV-Animal and Veterinary Research Centre UTAD, University of Trás-os-Montes and Alto Douro (UTAD), 5000-801 Vila Real, Portugal.
Associate Laboratory for Animal and Veterinary Sciences (AL4AnimalS), 5000-801 Vila Real, Portugal.
Grant Funding
UIDB/50006/2020 | UIDP/50006/2020, UIDB/04033/2020, UIDB/CVT/00772/2020, LA/P/0059/2020, SFRH/BD/148830/2019 / Fundação para a Ciência e Tecnologia
Conflict of Interest Statement
The authors declare no conflict of interest.
References
This article includes 135 references
Salem H.K., Thiemermann C.. Mesenchymal stromal cells: Current understanding and clinical status.. Stem Cells 2010;28:585–596.
Szydlarska J., Weiss C., Marycz K.. The Effect of Methyl-β-cyclodextrin on Apoptosis, Proliferative Activity, and Oxidative Stress in Adipose-Derived Mesenchymal Stromal Cells of Horses Suffering from Metabolic Syndrome (EMS). Molecules 2018;23:287.
Jiao F., Wang J., Dong Z.-L., Wu M.-J., Zhao T.-B., Li D.-D., Wang X.. Human Mesenchymal Stem Cells Derived From Limb Bud Can Differentiate into All Three Embryonic Germ Layers Lineages.. Cell. Reprogram. 2012;14:324–333.
Kisiel A.H., McDuffee L.A., Masaoud E., Bailey T.R., Gonzalez B.P.E., Nino-Fong R.. Isolation, characterization, and in vitro proliferation of canine mesenchymal stem cells derived from bone marrow, adipose tissue, muscle, and periosteum.. Am. J. Vet. Res. 2012;73:1305–1317.
Arévalo-Turrubiarte M., Olmeo C., Accornero P., Baratta M., Martignani E.. Analysis of mesenchymal cells (MSCs) from bone marrow, synovial fluid and mesenteric, neck and tail adipose tissue sources from equines.. Stem Cell Res. 2019;37:101442.
Kang B.-J., Ryu H.-H., Park S.S., Koyama Y., Kikuchi M., Woo H.-M., Kim W.H., Kweon O.-K.. Comparing the osteogenic potential of canine mesenchymal stem cells derived from adipose tissues, bone marrow, umbilical cord blood, and Wharton’s jelly for treating bone defects.. J. Vet. Sci. 2012;13:299–310.
Martin D.R., Cox N.R., Hathcock T.L., Niemeyer G.P., Baker H.J.. Isolation and characterization of multipotential mesenchymal stem cells from feline bone marrow.. Exp. Hematol. 2002;30:879–886.
Radtke C.L., Nino-Fong R., Gonzalez B.P.E., Stryhn H., McDuffee L.A.. Characterization and osteogenic potential of equine muscle tissue– and periosteal tissue–derived mesenchymal stem cells in comparison with bone marrow– and adipose tissue–derived mesenchymal stem cells.. Am. J. Vet. Res. 2013;74:790–800.
Sasaki A, Mizuno M, Ozeki N, Katano H, Otabe K, Tsuji K, Koga H, Mochizuki M, Sekiya I. Canine mesenchymal stem cells from synovium have a higher chondrogenic potential than those from infrapatellar fat pad, adipose tissue, and bone marrow.. PLoS ONE 2018;13:e0202922.
Webb T.L, Quimby J.M, Dow S.W. In vitro comparison of feline bone marrow-derived and adipose tissue-derived mesenchymal stem cells.. J. Feline Med. Surg. 2011;14:165–168.
Zhang S, Zhao C, Liu S, Wang Y, Zhao Y, Guan W, Zhu Z. Characteristics and multi-lineage differentiation of bone marrow mesenchymal stem cells derived from the Tibetan mastiff.. Mol. Med. Rep. 2018;18:2097–2109.
Lee B-Y, Li Q, Song W-J, Chae H-K, Kweon K, Ahn J-O, Youn H-Y. Altered properties of feline adipose-derived mesenchymal stem cells during continuous in vitro cultivation.. J. Vet. Med. Sci. 2018;80:930–938.
Mensing N, Gasse H, Hambruch N, Haeger J-D, Pfarrer C, Staszyk C. Isolation and characterization of multipotent mesenchymal stromal cells from the gingiva and the periodontal ligament of the horse.. BMC Vet. Res. 2011;7:42.
Presen D.M, Traweger A, Gimona M, Redl H. Mesenchymal Stromal Cell-Based Bone Regeneration Therapies: From Cell Transplantation and Tissue Engineering to Therapeutic Secretomes and Extracellular Vesicles.. Front. Bioeng. Biotechnol. 2019;7:352.
Jin G-Z, Yin X-J, Yu X-F, Cho S-J, Choi E-G, Lee Y-S, Jeon J-T, Yee S-T, Kong I-K. Generation of Neuronal-Like Cells from Umbilical Cord Blood-Derived Mesenchymal Stem Cells of a RFP-Transgenic Cloned Cat.. J. Vet. Med. Sci. 2008;70:723–726.
Sato K, Yamawaki-Ogata A, Kanemoto I, Usui A, Narita Y. Isolation and characterisation of peripheral blood-derived feline mesenchymal stem cells.. Vet. J. 2016;216:183–188.
Zhang B-Y, Wang B-Y, Li S-C, Luo D-Z, Zhan X, Chen S-F, Chen Z-S, Liu C-Y, Ji H-Q, Bai Y-S. Evaluation of the Curative Effect of Umbilical Cord Mesenchymal Stem Cell Therapy for Knee Arthritis in Dogs Using Imaging Technology.. Stem Cells Int. 2018;2018:1983025.
Zuk P.A, Zhu M, Ashjian P, De Ugarte D.A, Huang J.I, Mizuno H, Alfonso Z.C, Fraser J.K, Benhaim P, Hedrick M.H. Human adipose tissue is a source of multipotent stem cells.. Mol. Biol. Cell. 2002;13:4279–4295.
Naem M.A, Bourebaba L, Kucharczyk K, Röcken M, Marycz K. Therapeutic mesenchymal stromal stem cells: Isolation, characterization and role in equine regenerative medicine and metabolic disorders.. Stem Cell Rev. Rep. 2020;16:301–322.
Prządka P, Buczak K, Frejlich E, Gąsior L, Suliga K, Kiełbowicz Z. The Role of Mesenchymal Stem Cells (MSCs) in Veterinary Medicine and Their Use in Musculoskeletal Disorders.. Biomolecules 2021;11:1141.
Harman R, Carlson K, Gaynor J, Gustafson S, Dhupa S, Clement K, Hoelzler M, McCarthy T, Schwartz P, Adams C. A Prospective, Randomized, Masked, and Placebo-Controlled Efficacy Study of Intraarticular Allogeneic Adipose Stem Cells for the Treatment of Osteoarthritis in Dogs. Front. Vet. Sci. 2016;3:81.
Pourebrahim N, Hashemibeni B, Shahnaseri S, Torabinia N, Mousavi B, Adibi S, Heidari F, Alavi MJ. A comparison of tissue-engineered bone from adipose-derived stem cell with autogenous bone repair in maxillary alveolar cleft model in dogs. Int. J. Oral Maxillofac. Surg. 2013;42:562–568.
Wysong A, Ortiz P, Bittel D, Ott L, Karanu F, Filla M, Stehno-Bittel L. Viability, yield and expansion capability of feline MSCs obtained from subcutaneous and reproductive organ adipose depots. BMC Vet. Res. 2021;17:244.
Voga M, Kovač V, Majdic G. Comparison of Canine and Feline Adipose-Derived Mesenchymal Stem Cells/Medicinal Signaling Cells with Regard to Cell Surface Marker Expression, Viability, Proliferation, and Differentiation Potential. Front. Vet. Sci. 2021;7:610240.
Casteilla L, Planat-Benard V, Laharrague P, Cousin B. Adipose-derived stromal cells: Their identity and uses in clinical trials, an update. World J. Stem Cells. 2011;3:25–33.
Trachsel DS, Stage HJ, Rausch S, Trappe S, Söllig K, Sponder G, Merle R, Aschenbach JR, Gehlen H. Comparison of Sources and Methods for the Isolation of Equine Adipose Tissue-Derived Stromal/Stem Cells and Preliminary Results on Their Reaction to Incubation with 5-Azacytidine. Animals 2022;12:2049.
Duan W, Lopez MJ. Effects of Cryopreservation on Canine Multipotent Stromal Cells from Subcutaneous and Infrapatellar Adipose Tissue. Stem Cell Rev. Rep. 2016;12:257–268.
Aziz Aly LA, Menoufy HE, Ragae A, Rashed LA, Sabry D. Adipose stem cells as alternatives for bone marrow mesenchymal stem cells in oral ulcer healing. Int. J. Stem Cells. 2012;5:104–114.
Bahamondes F, Flores E, Cattaneo G, Bruna F, Conget P. Omental adipose tissue is a more suitable source of canine Mesenchymal stem cells. BMC Vet. Res. 2017;13:166.
Chung D-J, Hayashi K, Toupadakis CA, Wong A, Yellowley CE. Osteogenic proliferation and differentiation of canine bone marrow and adipose tissue derived mesenchymal stromal cells and the influence of hypoxia. Res. Vet. Sci. 2012;92:66–75.
Clark KC, Kol A, Shahbenderian S, Granick JL, Walker NJ, Borjesson DL. Canine and Equine Mesenchymal Stem Cells Grown in Serum Free Media Have Altered Immunophenotype. Stem Cell Rev. Rep. 2016;12:245–256.
Dang Le Q, Rodprasert W, Kuncorojakti S, Pavasant P, Osathanon T, Sawangmake C. In vitro generation of transplantable insulin-producing cells from canine adipose-derived mesenchymal stem cells. Sci. Rep. 2022;12:9127.
Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini FC, Krause DS, Deans RJ, Keating A, Prockop DJ, Horwitz EM. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement.. Cytotherapy 2006;8:315–317.
Hendawy H, Uemura A, Ma D, Namiki R, Samir H, Ahmed MF, Elfadadny A, El-Husseiny HM, Chieh-Jen C, Tanaka R. Tissue Harvesting Site Effect on the Canine Adipose Stromal Vascular Fraction Quantity and Quality.. Animals 2021;11:460.
Kim GA, Oh HJ, Lee TH, Lee JH, Oh SH, Lee JH, Kim JW, Kim SW, Lee BC. Effect of culture medium type on canine adipose-derived mesenchymal stem cells and developmental competence of interspecies cloned embryos.. Theriogenology 2014;81:243–249.
Kuk M, Kim Y, Lee SH, Kim WH, Kweon O-K. Osteogenic Ability of Canine Adipose-Derived Mesenchymal Stromal Cell Sheets in Relation to Culture Time.. Cell Transplant 2016;25:1415–1422.
Metcalf GL, McClure SR, Hostetter JM, Martinez RF, Wang C. Evaluation of adipose-derived stromal vascular fraction from the lateral tailhead, inguinal region, and mesentery of horses.. Can. J. Vet. Res. 2016;80:294–301.
Neupane M, Chang C-C, Kiupel M, Yuzbasiyan-Gurkan V. Isolation and Characterization of Canine Adipose–Derived Mesenchymal Stem Cells.. Tissue Eng. Part A 2008;14:1007–1015.
Ock S-A, Maeng G-H, Lee Y-M, Kim T-H, Kumar BM, Lee S-L, Rho G-J. Donor-Matched Functional and Molecular Characterization of Canine Mesenchymal Stem Cells Derived from Different Origins.. Cell Transplant 2013;22:2311–2321.
Oh J, Son YS, Kim WH, Kwon O-K, Kang B-J. Mesenchymal stem cells genetically engineered to express platelet-derived growth factor and heme oxygenase-1 ameliorate osteoarthritis in a canine model.. J. Orthop. Surg. Res. 2021;16:43.
Rashid U, Yousaf A, Yaqoob M, Saba E, Moaeen-ud-Din M, Waseem S, Becker SK, Sponder G, Aschenbach JR, Sandhu MA. Characterization and differentiation potential of mesenchymal stem cells isolated from multiple canine adipose tissue sources.. BMC Vet. Res. 2021;17:388.
Requicha JF, Viegas CA, Albuquerque CM, Azevedo JM, Reis RL, Gomes ME. Effect of Anatomical Origin and Cell Passage Number on the Stemness and Osteogenic Differentiation Potential of Canine Adipose-Derived Stem Cells.. Stem Cell Rev. Rep. 2012;8:1211–1222.
Sanghani-Kerai A, Black C, Cheng SO, Collins L, Schneider N, Blunn G, Watson F, Fitzpatrick N. Clinical outcomes following intra-articular injection of autologous adipose-derived mesenchymal stem cells for the treatment of osteoarthritis in dogs characterized by weight-bearing asymmetry.. Bone Jt. Res. 2021;10:650–658.
Schwarz C, Leicht U, Rothe C, Drosse I, Luibl V, Röcken M, Schieker M. Effects of different media on proliferation and differentiation capacity of canine, equine and porcine adipose derived stem cells.. Res. Vet. Sci. 2012;93:457–462.
Takemitsu H, Zhao D, Yamamoto I, Harada Y, Michishita M, Arai T. Comparison of bone marrow and adipose tissue-derived canine mesenchymal stem cells.. BMC Vet. Res. 2012;8:150.
Teshima T, Matsuoka A, Shiba M, Dairaku K, Matsumoto H, Suzuki R, Koyama H. Comparison of Properties of Stem Cells Isolated from Adipose Tissue and Lipomas in Dogs. Stem Cells Int 2019;2019:1609876.
Wan DC, Shi Y-Y, Nacamuli RP, Quarto N, Lyons KM, Longaker MT. Osteogenic differentiation of mouse adipose-derived adult stromal cells requires retinoic acid and bone morphogenetic protein receptor type IB signaling. Proc Natl Acad Sci USA 2006;103:12335–12340.
Wi H, Lee S, Kim Y, No JG, Lee P, Lee BR, Oh KB, Hur TY, Ock SA. Immunosuppression-enhancing effect of the administration of allogeneic canine adipose-derived mesenchymal stem cells (cA-MSCs) compared with autologous cA-MSCs in vitro. J Vet Sci 2021;22:e63.
Yaneselli KM, Kuhl CP, Terraciano PB, de Oliveira FS, Pizzato SB, Pazza K, Magrisso AB, Torman V, Rial A, Moreno M. Comparison of the characteristics of canine adipose tissue-derived mesenchymal stem cells extracted from different sites and at different passage numbers. J Vet Sci 2018;19:13–20.
Ferreira-Baptista C, Queirós A, Ferreira R, Fernandes MH, Colaço B, Gomes PS. The Osteogenic Potential of Falciform Ligament-Derived Stromal Cells-A Comparative Analysis between Two Osteogenic Induction Programs. Bioengineering 2022;9:810.
Teshima T, Matsumoto H, Michishita M, Matsuoka A, Shiba M, Nagashima T, Koyama H. Allogenic Adipose Tissue-Derived Mesenchymal Stem Cells Ameliorate Acute Hepatic Injury in Dogs. Stem Cells Int 2017;2017:3892514.
Bach FS, Rebelatto CLK, Fracaro L, Senegaglia AC, Fragoso FYI, Daga DR, Brofman PRS, Pimpão CT, Engracia Filho JR, Montiani-Ferreira F. Comparison of the Efficacy of Surgical Decompression Alone and Combined with Canine Adipose Tissue-Derived Stem Cell Transplantation in Dogs with Acute Thoracolumbar Disk Disease and Spinal Cord Injury. Front Vet Sci 2019;6:383.
Krueger E, Magri LMS, Botelho AS, Bach FS, Rebellato CLK, Fracaro L, Fragoso FYI, Villanova JA, Brofman PRS, Popović-Maneski L. Effects of low-intensity electrical stimulation and adipose derived stem cells transplantation on the time-domain analysis-based electromyographic signals in dogs with SCI. Neurosci Lett 2019;696:38–45.
Kono S, Kazama T, Kano K, Harada K, Uechi M, Matsumoto T. Phenotypic and functional properties of feline dedifferentiated fat cells and adipose-derived stem cells. Vet J 2014;199:88–96.
Li D., Luo H., Ruan H., Chen Z., Chen S., Wang B., Xie Y. Isolation and identification of exosomes from feline plasma, urine and adipose-derived mesenchymal stem cells. BMC Vet. Res. 2021;17:272. doi: 10.1186/s12917-021-02960-4.
Parys M., Nelson N., Koehl K., Miller R., Kaneene J.B., Kruger J.M., Yuzbasiyan-Gurkan V. Safety of Intraperitoneal Injection of Adipose Tissue-Derived Autologous Mesenchymal Stem Cells in Cats. J. Vet. Intern. Med. 2016;30:157–163. doi: 10.1111/jvim.13655.
Quimby J.M., Webb T.L., Habenicht L.M., Dow S.W. Safety and efficacy of intravenous infusion of allogeneic cryopreserved mesenchymal stem cells for treatment of chronic kidney disease in cats: Results of three sequential pilot studies. Stem Cell Res. Ther. 2013;4:48. doi: 10.1186/scrt198.
Teshima T., Yasumura Y., Suzuki R., Matsumoto H. Antiviral Effects of Adipose Tissue-Derived Mesenchymal Stem Cells Secretome against Feline Calicivirus and Feline Herpesvirus Type 1. Viruses. 2022;14:1687. doi: 10.3390/v14081687.
Quimby J.M., Webb T.L., Randall E., Marolf A., Valdes-Martinez A., Dow S.W. Assessment of intravenous adipose-derived allogeneic mesenchymal stem cells for the treatment of feline chronic kidney disease: A randomized, placebo-controlled clinical trial in eight cats. J. Feline Med. Surg. 2015;18:165–171. doi: 10.1177/1098612X15576980.
Chae H.-K., Song W.-J., Ahn J.-O., Li Q., Lee B.-Y., Kweon K., Park S.-C., Youn H.-Y. Immunomodulatory effects of soluble factors secreted by feline adipose tissue-derived mesenchymal stem cells. Vet. Immunol. Immunopathol. 2017;191:22–29. doi: 10.1016/j.vetimm.2017.07.013.
Arnhold S., Elashry M.I., Klymiuk M.C., Geburek F. Investigation of stemness and multipotency of equine adipose-derived mesenchymal stem cells (ASCs) from different fat sources in comparison with lipoma. Stem Cell Res. Ther. 2019;10:309. doi: 10.1186/s13287-019-1429-0.
Bagge J., Berg L.C., Janes J., MacLeod J.N. Donor age effects on in vitro chondrogenic and osteogenic differentiation performance of equine bone marrow- and adipose tissue-derived mesenchymal stromal cells. BMC Vet. Res. 2022;18:388. doi: 10.1186/s12917-022-03475-2.
Cacciamali A., Pascucci L., Villa R., Dotti S. Engineered nanoparticles toxicity on adipose tissue derived mesenchymal stem cells: A preliminary investigation. Res. Vet. Sci. 2022;152:134–149. doi: 10.1016/j.rvsc.2022.08.002.
Hillmann A., Ahrberg A.B., Brehm W., Heller S., Josten C., Paebst F., Burk J. Comparative Characterization of Human and Equine Mesenchymal Stromal Cells: A Basis for Translational Studies in the Equine Model. Cell Transpl. 2016;25:109–124. doi: 10.3727/096368915X687822.
Kim H.-R., Lee J., Byeon J.S., Gu N.-Y., Lee J., Cho I.-S., Cha S.-H. Extensive characterization of feline intra-abdominal adipose-derived mesenchymal stem cells. J. Vet. Sci. 2017;18:299–306. doi: 10.4142/jvs.2017.18.3.299.
Lee J., Lee K.S., Kim C.L., Byeon J.S., Gu N.Y., Cho I.S., Cha S.H. Effect of donor age on the proliferation and multipotency of canine adipose-derived mesenchymal stem cells. J. Vet. Sci. 2017;18:141–148. doi: 10.4142/jvs.2017.18.2.141.
Marycz K., Kornicka K., Marędziak M., Golonka P., Nicpoń J. Equine metabolic syndrome impairs adipose stem cells osteogenic differentiation by predominance of autophagy over selective mitophagy. J. Cell. Mol. Med. 2016;20:2384–2404. doi: 10.1111/jcmm.12932.
Maumus M., Roussignol G., Toupet K., Penarier G., Bentz I., Teixeira S., Oustric D., Jung M., Lepage O., Steinberg R., et al. Utility of a Mouse Model of Osteoarthritis to Demonstrate Cartilage Protection by IFNγ-Primed Equine Mesenchymal Stem Cells. Front. Immunol. 2016;7:392. doi: 10.3389/fimmu.2016.00392.
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. Cytom. Part A. 2014;85:678–687. doi: 10.1002/cyto.a.22491.
Radtke C.L., Nino-Fong R., Esparza Gonzalez B.P., McDuffee L.A. Application of a novel sorting system for equine mesenchymal stem cells (MSCs) Can. J. Vet. Res. 2014;78:290–296.
Ranera B., Ordovás L., Lyahyai J., Bernal M.L., Fernandes F., Remacha A.R., Romero A., Vázquez F.J., Osta R., Cons C., et al. Comparative study of equine bone marrow and adipose tissue-derived mesenchymal stromal cells. Equine Vet. J. 2012;44:33–42. doi: 10.1111/j.2042-3306.2010.00353.x.
Stage H.J., Trappe S., Söllig K., Trachsel D.S., Kirsch K., Zieger C., Merle R., Aschenbach J.R., Gehlen H. Multilineage Differentiation Potential of Equine Adipose-Derived Stromal/Stem Cells from Different Sources. Animals. 2023;13:1352. doi: 10.3390/ani13081352.
Ode A., Schoon J., Kurtz A., Gaetjen M., Ode J.E., Geissler S., Duda G.N. CD73/5′-ecto-nucleotidase acts as a regulatory factor in osteo-/chondrogenic differentiation of mechanically stimulated mesenchymal stromal cells. Eur. Cells Mater. 2013;25:37–47. doi: 10.22203/eCM.v025a03.
Anderson P., Carrillo-Gálvez A.B., García-Pérez A., Cobo M., Martín F. CD105 (endoglin)-negative murine mesenchymal stromal cells define a new multipotent subpopulation with distinct differentiation and immunomodulatory capacities. PLoS ONE. 2013;8:e76979. doi: 10.1371/journal.pone.0076979.
Kimura K., Breitbach M., Schildberg F.A., Hesse M., Fleischmann B.K. Bone marrow CD73+ mesenchymal stem cells display increased stemness in vitro and promote fracture healing in vivo. Bone Rep. 2021;15:101133. doi: 10.1016/j.bonr.2021.101133.
Chung M.T., Liu C., Hyun J.S., Lo D.D., Montoro D.T., Hasegawa M., Li S., Sorkin M., Rennert R., Keeney M., et al. CD90 (Thy-1)-positive selection enhances osteogenic capacity of human adipose-derived stromal cells. Tissue Eng. Part A. 2013;19:989–997. doi: 10.1089/ten.tea.2012.0370.
Nakamura H., Yukita A., Ninomiya T., Hosoya A., Hiraga T., Ozawa H. Localization of Thy-1-positive cells in the perichondrium during endochondral ossification. J. Histochem. Cytochem. Off. J. Histochem. Soc. 2010;58:455–462. doi: 10.1369/jhc.2010.955393.
Alves E.G.L., Serakides R., Boeloni J.N., Rosado I.R., Ocarino N.M., Oliveira H.P., Góes A.M., Rezende C.M.F. Comparison of the osteogenic potential of mesenchymal stem cells from the bone marrow and adipose tissue of young dogs. BMC Vet. Res. 2014;10:190. doi: 10.1186/s12917-014-0190-y.
Raabe O., Shell K., Würtz A., Reich C.M., Wenisch S., Arnhold S. Further insights into the characterization of equine adipose tissue-derived mesenchymal stem cells. Vet. Res. Commun. 2011;35:355–365. doi: 10.1007/s11259-011-9480-z.
Bundgaard L., Stensballe A., Elbæk K.J., Berg L.C. Mapping of equine mesenchymal stromal cell surface proteomes for identification of specific markers using proteomics and gene expression analysis: An in vitro cross-sectional study. Stem Cell Res. Ther. 2018;9:288. doi: 10.1186/s13287-018-1041-8.
Levi B., Nelson E.R., Brown K., James A.W., Xu D., Dunlevie R., Wu J.C., Lee M., Wu B., Commons G.W., et al. Differences in Osteogenic Differentiation of Adipose-Derived Stromal Cells from Murine, Canine, and Human Sources In Vitro and In Vivo. Plast. Reconstr. Surg. 2011;128:373–386. doi: 10.1097/PRS.0b013e31821e6e49.
Langenbach F., Handschel J. Effects of dexamethasone, ascorbic acid and β-glycerophosphate on the osteogenic differentiation of stem cells in vitro. Stem Cell Res. Ther. 2013;4:117. doi: 10.1186/scrt328.
Park J.B. Effects of the combination of dexamethasone and fibroblast growth factor-2 on differentiation of osteoprecursor cells. Mol. Med. Rep. 2014;9:659–662. doi: 10.3892/mmr.2013.1811.
Sordi M.B., Curtarelli R.B., da Silva I.T., Fongaro G., Benfatti C.A.M., Magini R.D.S., da Cruz A.C.C. Effect of dexamethasone as osteogenic supplementation in in vitro osteogenic differentiation of stem cells from human exfoliated deciduous teeth. J. Mater. Sci. Mater. Med. 2021;32:1. doi: 10.1007/s10856-020-06475-6.
Wang C., Cao X., Zhang Y. A novel bioactive osteogenesis scaffold delivers ascorbic acid, β-glycerophosphate, and dexamethasone in vivo to promote bone regeneration. Oncotarget. 2017;8:31612–31625. doi: 10.18632/oncotarget.15779.
Cruz A.C.C., Cardozo F.T.G.D.S., Magini R.D.S., Simões C.M.O. Retinoic acid increases the effect of bone morphogenetic protein type 2 on osteogenic differentiation of human adipose-derived stem cells. J. Appl. Oral Sci. 2019;27:e20180317. doi: 10.1590/1678-7757-2018-0317.
Kim Y., Lee S.H., Kang B.J., Kim W.H., Yun H.S., Kweon O.K. Comparison of Osteogenesis between Adipose-Derived Mesenchymal Stem Cells and Their Sheets on Poly-ε-Caprolactone/β-Tricalcium Phosphate Composite Scaffolds in Canine Bone Defects. Stem Cells Int. 2016;2016:8414715. doi: 10.1155/2016/8414715.
Kirkham G.R., Cartmell S.H. Genes and Proteins Involved in the Regulation of Osteogenesis. Top. Tissue Eng. 2007;3:1–22. doi: 10.1016/j.cryobiol.2014.07.005.
Zainal Ariffin S.H., Lim K.W., Megat Abdul Wahab R., Zainal Ariffin Z., Rus Din R.D., Shahidan M.A., Johari A.N., Zainol Abidin I.Z. Gene expression profiles for in vitro human stem cell differentiation into osteoblasts and osteoclasts: A systematic review. PeerJ. 2022;10:e14174. doi: 10.7717/peerj.14174.
Arrigoni E., Lopa S., de Girolamo L., Stanco D., Brini A.T. Isolation, characterization and osteogenic differentiation of adipose-derived stem cells: From small to large animal models. Cell Tissue Res. 2009;338:401–411. doi: 10.1007/s00441-009-0883-x.
de Mattos Carvalho A., Alves A.L.G., Golim M.A., Moroz A., Hussni C.A., de Oliveira P.G.G., Deffune E. Isolation and immunophenotypic characterization of mesenchymal stem cells derived from equine species adipose tissue. Vet. Immunol. Immunopathol. 2009;132:303–306. doi: 10.1016/j.vetimm.2009.06.014.
Chi C., Wang F., Xiang B., Deng J., Liu S., Lin H.-Y., Natarajan K., Li G., Wang J., Lin F., et al. Adipose-Derived Stem Cells From Both Visceral and Subcutaneous Fat Deposits Significantly Improve Contractile Function of Infarcted Rat Hearts. Cell Transplant. 2015;24:2337–2351. doi: 10.3727/096368914X685780.
Panasophonkul S., Samart P., Kongon K., Sathanawongs A. Phenotypic characteristics of feline adipose-derived stem cells affected by cell passage number. Pol. J. Vet. Sci. 2017;20:651–660.
Abo-Soliman A.A.M., Ahmed A.E., Farghali H.A.M.A. Incidence of Appendicular Bone Fracture in Dogs and Cats: Retrospective Study at Veterinary Hospital of Cairo University and some Private Clinics in Egypt. World’s Vet. J. 2020;10:638–652. doi: 10.54203/scil.2020.wvj77.
Keosengthong A., Kampa N., Jitpean S., Seesupa S., Kunkitti P., Hoisang S. Incidence and classification of bone fracture in dogs and cats: A retrospective study at a Veterinary Teaching Hospital, Khon Kaen University, Thailand (2013–2016) Vet. Integr. Sci. 2019;17:127–139.
Gunawardena T.N.A., Rahman M.T., Abdullah B.J.J., Kasim N.H.A. Conditioned media derived from mesenchymal stem cell cultures: The next generation for regenerative medicine. J. Tissue Eng. Regen. Med. 2019;13:569–586. doi: 10.1002/term.2806.
Mahiddine F.Y., Kim J.W., Qamar A.Y., Ra J.C., Kim S.H., Jung E.J., Kim M.J. Conditioned Medium from Canine Amniotic Membrane-Derived Mesenchymal Stem Cells Improved Dog Sperm Post-Thaw Quality-Related Parameters. Animals. 2020;10:1899. doi: 10.3390/ani10101899.
Osugi M., Katagiri W., Yoshimi R., Inukai T., Hibi H., Ueda M. Conditioned Media from Mesenchymal Stem Cells Enhanced Bone Regeneration in Rat Calvarial Bone Defects. Tissue Eng. Part A. 2012;18:1479–1489. doi: 10.1089/ten.tea.2011.0325.
Mocchi M., Dotti S., Del Bue M., Villa R., Bari E., Perteghella S., Torre M.L., Grolli S. Veterinary Regenerative Medicine for Musculoskeletal Disorders: Can Mesenchymal Stem/Stromal Cells and Their Secretome Be the New Frontier? Cells. 2020;9:1453. doi: 10.3390/cells9061453.
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;16:771–781. doi: 10.1089/ten.tec.2009.0512.
Salinas-Varas C, Espinosa G, Muñoz-Caro T, Conejeros I, Gärtner U, Fey K, Arnhold S, Taubert A, Hermosilla C. Equine adipose-derived stem cells modulate in vitro neutrophil extracellular trap release by polymorphonuclear neutrophils.. Front Vet Sci 2025;12:1685757.
Guerra-Gomes M, Ferreira-Baptista C, Barros J, Alves-Pimenta S, Gomes P, Colaço B. Exploring the Potential of Non-Cellular Orthobiologic Products in Regenerative Therapies for Stifle Joint Diseases in Companion Animals.. Animals (Basel) 2025 Feb 18;15(4).
Nan N, Yang N, Liu Y, Hao HQ. Chinese Medicine Combined with Adipose Tissue-Derived Mesenchymal Stem Cells: A New Promising Aspect of Integrative Medicine.. Chin J Integr Med 2025 Jul;31(7):660-672.
Morawska-Kozłowska M, Wilkosz A, Zhalniarovich Y. The Omentum-A Forgotten Structure in Veterinary Surgery in Small Animals' Surgery.. Animals (Basel) 2024 Jun 21;14(13).