FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / Stem Cell Res Ther / Investigation of stemness and multipotency of equine adipose...
Stem cell research & therapy2019; 10(1); 309; doi: 10.1186/s13287-019-1429-0

Investigation of stemness and multipotency of equine adipose-derived mesenchymal stem cells (ASCs) from different fat sources in comparison with lipoma.

Abstract: Adipose tissue-derived mesenchymal stem cells (ASCs) offer a promising cell source for therapeutic applications in musculoskeletal disorders. The appropriate selection of ASCs from various fat depots for cell-based therapy is challenging. The present study aims to compare stemness and multipotency of ASCs derived from retroperitoneal (RP), subcutaneous (SC), and lipoma (LP) fat to assess their usefulness for clinical application. Equine ASCs from the three fat tissue sources were isolated and characterized. The cell viability, proliferation, and self-renewal were evaluated using MTT, sulforhodamine B, and colony forming unit (CFU) assays. Stem cell relative marker CD44, CD90, and CD105 and tumor marker CA9 and osteopontin (OPN) expression were quantified using RT-qPCR. Multipotency of ASCs for adipogenic, osteogenic, and chondrogenic differentiation was examined by quantifying Oil Red O and Alizarin Red S staining, alkaline phosphatase activity (ALP), and expression of differentiation relative markers. All data were statistically analyzed using ANOVA. RP fat-derived ASCs showed a higher cell proliferation rate compared to SC and LP derived cells. In contrast, ASCs from lipoma displayed a lower proliferation rate and impaired CFU capacities. The expression of CD44, CD90, and CD105 was upregulated in RP and SC derived cells but not in LP cells. RP fat-derived cells displayed a higher adipogenic potential compared to SC and LP cells. Although ASCs from all fat sources showed enhanced ALP activity following osteogenic differentiation, SC fat-derived cells revealed upregulated ALP and bone morphogenetic protein-2 expression together with a higher calcium deposition. We found an enhanced chondrogenic potency of RP and SC fat-derived cells as shown by Alcian blue staining and upregulation of aggrecan (Aggre), cartilage oligomeric matrix protein precursor (COMP), and collagen 2a1 (Col2a1) expression compared to LP. The expression of OPN and CA9 was exclusively upregulated in the ASCs of LP. The results provide evidence of variation in ASC performance not only between normal fat depots but also compared to LP cells which suggest a different molecular regulation controlling the cell fate. These data provided are useful when considering a source for cell replacement therapy in equine veterinary medicine.
Get Full Text
Publication Date: 2019-10-22 PubMed ID: 31640774PubMed Central: PMC6805636DOI: 10.1186/s13287-019-1429-0Google 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
  • Comparative Study
  • 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.

The research explores the potential and characteristics of different sources of equine mesenchymal stem cells, specifically those derived from adipose tissue, in order to identify the most suitable type for treating musculoskeletal disorders in horses. It compares the functionality of stem cells from three types of adipose tissue sources, each relating to their origin in different fat deposits.

Research Objectives and Methods

The authors aim to compare the efficiency of stem cells derived from three different fat sources—retroperitoneal (RP), subcutaneous (SC), and lipoma (LP)—in order to determine their applicability in cell-based therapies.

  • The stem cells were isolated from the three different fat tissue sources and their characteristics were evaluated.
  • Various assays, such as MTT, sulforhodamine B, and colony-forming unit (CFU) assays were used to assess the cell viability, proliferation rate, and self-renewal capability of the cells.
  • CD44, CD90, and CD105, are considered stem cell markers, and CA9 and osteopontin (OPN) are considered indicators of tumor cells. The expression of these markers in the stem cells was quantified using RT-qPCR.
  • The multipotency of these stem cells was assessed by analyzing their capability to differentiate into adipogenic, osteogenic, and chondrogenic cells. This was done by staining with Oil Red O and Alizarin Red S, examining the alkaline phosphatase activity (ALP), and analyzing the expression of differentiation markers.
  • Data were processed and statistically analyzed using ANOVA.

Key Findings

The adipose tissue-derived stem cells exhibited different efficiencies based on their source.

  • Stem cells from RP fat demonstrated a higher rate of cellular proliferation when compared to SC and LP derived cells. However, stem cells from lipomas had the lowest proliferation rate and impaired CFU capacities.
  • The expression of specific stem cell markers, namely CD44, CD90, and CD105, was significantly higher in stem cells from RP and SC cells than in those from LP.
  • RP cells exhibited a higher potential for adipogenic differentiation compared to SC and LP cells. On the other hand, SC cells showed enhanced ALP activity, indicating a higher propensity to differentiate into bone cells.
  • An escalated potential for chondrogenic differentiation (development into cartilage cells) was seen in RP and SC cells, as demonstrated by staining and increased expression of specific matrix proteins.
  • The higher expression of CA9 and OPN, which are often linked to cancer, was exclusively seen in LP-derived stem cells.

Implications of the Study

Notably, the research suggests that the origin of the adipose tissue in horses contributes to the functionality and efficiency of the derived stem cells. The varied properties and cellular behavior of stem cells from the LP, SC, and RP fat sources could be indicative of diverse molecular regulations that control stem cell behavior. These findings could be of significant importance when selecting the most suitable adipose tissue source for stem cell therapy in equine veterinary medicine. The high proliferation rate and differentiation potential of RP and SC-derived stem cells suggest these might be better sources, opposed to those from lipomas which showed lower proliferation and higher expression of tumor markers.

Cite This Article

APA
Arnhold S, Elashry MI, Klymiuk MC, Geburek F. (2019). 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, 10(1), 309. https://doi.org/10.1186/s13287-019-1429-0

Publication

Stem cell research & therapy
ISSN: 1757-6512
NlmUniqueID: 101527581
Country: England
Language: English
Volume: 10
Issue: 1
Pages: 309

Researcher Affiliations

Arnhold, Stefan
  • Institute of Veterinary Anatomy, Histology and Embryology, Justus-Liebig-University of Giessen, Frankfurter Str. 98, 35392, Giessen, Germany.
Elashry, Mohamed I
  • Institute of Veterinary Anatomy, Histology and Embryology, Justus-Liebig-University of Giessen, Frankfurter Str. 98, 35392, Giessen, Germany. Mohammed.Elashry@vetmed.uni-giessen.de.
  • Anatomy and Embryology Department, Faculty of Veterinary Medicine, University of Mansoura, Mansoura, 35516, Egypt. Mohammed.Elashry@vetmed.uni-giessen.de.
Klymiuk, Michele C
  • Institute of Veterinary Anatomy, Histology and Embryology, Justus-Liebig-University of Giessen, Frankfurter Str. 98, 35392, Giessen, Germany.
Geburek, Florian
  • Clinic for Horses, University of Veterinary Medicine Hannover, Foundation, Hannover, Germany.

MeSH Terms

  • Adipogenesis
  • Adipose Tissue / cytology
  • Animals
  • Cell Proliferation
  • Cell Shape
  • Cell Survival
  • Chondrogenesis
  • Horses
  • Lipoma / pathology
  • Mesenchymal Stem Cells / cytology
  • Multipotent Stem Cells / cytology
  • Osteogenesis

Conflict of Interest Statement

The authors declare that they have no competing interests.

References

This article includes 57 references
  1. Arnhold S, Wenisch S. Adipose tissue derived mesenchymal stem cells for musculoskeletal repair in veterinary medicine.. Am J Stem Cells 2015;4:1–12.
    pmc: PMC4396154pubmed: 25973326
  2. Ribitsch I, Burk J, Delling U, Geissler C, Gittel C, Juelke H, Brehm W. Basic science and clinical application of stem cells in veterinary medicine.. In: Wolbank S, van Griensven M, Grillari-Voglauer R, Peterbauer-Scherb A, editors. Alternative sources of adult stem cells: human amniotic membrane. 2010. pp. 219–263.
    pubmed: 20309674
  3. Fraser JK, Wulur I, Alfonso Z, Hedrick MH. Fat tissue: an underappreciated source of stem cells for biotechnology.. Trends Biotechnol 2006;24:150–154.
    doi: 10.1016/j.tibtech.2006.01.010pubmed: 16488036google scholar: lookup
  4. Hass R, Kasper C, Böhm S, Jacobs R. Different populations and sources of human mesenchymal stem cells (MSC): a comparison of adult and neonatal tissue-derived MSC.. Cell Commun Signal 2011;9:12.
    doi: 10.1186/1478-811X-9-12pmc: PMC3117820pubmed: 21569606google scholar: lookup
  5. Puissant B, Barreau C, Bourin P, Clavel C, Corre J, Bousquet C. Immunomodulatory effect of human adipose tissue-derived adult stem cells: comparison with bone marrow mesenchymal stem cells.. Br J Haematol 2005;129:118–129.
    doi: 10.1111/j.1365-2141.2005.05409.xpubmed: 15801964google scholar: lookup
  6. Bianco P, Robey PG, Simmons PJ. Mesenchymal stem cells: revisiting history, concepts, and assays.. Cell Stem Cell 2008;2:313–319.
    doi: 10.1016/j.stem.2008.03.002pmc: PMC2613570pubmed: 18397751google scholar: lookup
  7. 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;24:1294–1301.
    doi: 10.1634/stemcells.2005-0342pubmed: 16410387google scholar: lookup
  8. Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ. Multilineage cells from human adipose tissue: implications for cell-based therapies.. Tiss Engin 2001;7:211–228.
    doi: 10.1089/107632701300062859pubmed: 11304456google scholar: lookup
  9. Torres FC, Rodrigues CJ, Stocchero IN, Ferreira MC. Stem cells from the fat tissue of rabbits: an easy-to-find experimental source.. Aesthet Plast Surg 2007;31:574–578.
    doi: 10.1007/s00266-007-0001-ypubmed: 17576503google scholar: lookup
  10. Marycz K, Weiss C, Śmieszek A, Kornicka K. Evaluation of oxidative stress and mitophagy during adipogenic differentiation of adipose-derived stem cells isolated from equine metabolic syndrome (EMS) horses.. Stem Cells Int 2018;2018:5340756.
    doi: 10.1155/2018/5340756pmc: PMC6011082pubmed: 29977307google scholar: lookup
  11. Majors AK, Boehm CA, Nitto H, Midura RJ, Muschler GF. Characterization of human bone marrow stromal cells with respect to osteoblastic differentiation.. J Orthop Res 1997;15:546–557.
    doi: 10.1002/jor.1100150410pubmed: 9379264google scholar: lookup
  12. Gimble JM, Katz AJ, Bunnell BA. Adipose-derived stem cells for regenerative medicine.. Circ Res 2007;100:1249–1260.
    doi: 10.1161/01.RES.0000265074.83288.09pmc: PMC5679280pubmed: 17495232google scholar: lookup
  13. Russo V, Yu C, Belliveau P, Hamilton A, Flynn LE. Comparison of human adipose-derived stem cells isolated from subcutaneous, omental, and intrathoracic adipose tissue depots for regenerative applications.. Stem Cells Transl Med 2014;3:206–217.
    doi: 10.5966/sctm.2013-0125pmc: PMC3925056pubmed: 24361924google scholar: lookup
  14. Van Harmelen V, Röhrig K, Hauner H. Comparison of proliferation and differentiation capacity of human adipocyte precursor cells from the omental and subcutaneous adipose tissue depot of obese subjects.. Metab Clin Exp 2004;53:632–637.
    doi: 10.1016/j.metabol.2003.11.012pubmed: 15131769google scholar: lookup
  15. Tang Y, Pan Z-Y, Zou Y, He Y, Yang P-Y, Tang Q-Q, Yin F. A comparative assessment of adipose-derived stem cells from subcutaneous and visceral fat as a potential cell source for knee osteoarthritis treatment.. J Cell Mol Med 2017;21:2153–2162.
    doi: 10.1111/jcmm.13138pmc: PMC5571554pubmed: 28374574google scholar: lookup
  16. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F.C, Krause D.S, Deans R.J, Keating A, Prockop D.J, Horwitz E.M. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement.. Cytotherapy 2006;8(4):315–317.
    doi: 10.1080/14653240600855905pubmed: 16923606google scholar: lookup
  17. Mosna F, Sensebé L, Krampera M. Human bone marrow and adipose tissue mesenchymal stem cells: a user’s guide.. Stem Cells Dev 2010;19:1449–1470.
    doi: 10.1089/scd.2010.0140pubmed: 20486777google scholar: lookup
  18. Gronthos S, Franklin DM, Leddy HA, Robey PG, Storms RW, Gimble JM. Surface protein characterization of human adipose tissue-derived stromal cells.. J Cell Physiol 2001;189:54–63.
    doi: 10.1002/jcp.1138pubmed: 11573204google scholar: lookup
  19. Festy F, Hoareau L, Bes-Houtmann S, Péquin A-M, Gonthier M-P, Munstun A. Surface protein expression between human adipose tissue-derived stromal cells and mature adipocytes.. Histochem Cell Biol 2005;124:113–121.
    doi: 10.1007/s00418-005-0014-zpubmed: 16032396google scholar: lookup
  20. Qian Y-W, Gao J-H, Lu F, Zheng X-D. The differences between adipose tissue derived stem cells and lipoma mesenchymal stem cells in characteristics.. Zhonghua Zheng Xing Wai Ke Za Zhi 2010;26:125–132.
    pubmed: 20540318
  21. Omonte SV, de Andrade BAB, Leal RM, Capistrano HM, Souza PEA, Horta MCR. Osteolipoma: a rare tumor in the oral cavity.. Oral Surg Oral Med Oral Pathol Oral Radiol 2016;122:e8–e13.
    doi: 10.1016/j.oooo.2015.09.013pubmed: 26652892google scholar: lookup
  22. Chrisinger JSA. Update on Lipomatous tumors with emphasis on emerging entities, unusual anatomic sites, and variant histologic patterns.. Surg Pathol Clin 2019;12:21–33.
    doi: 10.1016/j.path.2018.11.001pubmed: 30709444google scholar: lookup
  23. Mentzel T, Fletcher CD. Lipomatous tumours of soft tissues: an update.. Virchows Arch 1995;427:353–363.
    doi: 10.1007/BF00199383pubmed: 8548119google scholar: lookup
  24. Garcia-Seco E, Wilson DA, Kramer J, Keegan KG, Branson KR, Johnson PJ, Tyler JW. Prevalence and risk factors associated with outcome of surgical removal of pedunculated lipomas in horses: 102 cases (1987-2002). J Am Vet Med Assoc 2005;226:1529–1537.
    doi: 10.2460/javma.2005.226.1529pubmed: 15882006google scholar: lookup
  25. Lin T-M, Chang H-W, Wang K-H, Kao A-P, Chang C-C, Wen C-H. Isolation and identification of mesenchymal stem cells from human lipoma tissue.. Biochem Biophys Res Commun 2007;361:883–889.
    doi: 10.1016/j.bbrc.2007.07.116pubmed: 17679141google scholar: lookup
  26. Suga H, Eto H, Inoue K, Aoi N, Kato H, Araki J. Cellular and molecular features of lipoma tissue: comparison with normal adipose tissue.. Br J Dermatol 2009;161:819–825.
    doi: 10.1111/j.1365-2133.2009.09272.xpubmed: 19558598google scholar: lookup
  27. Raabe O, Shell K, Würtz A, Reich CM, 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-zpubmed: 21614641google scholar: lookup
  28. Vichai V, Kirtikara K. Sulforhodamine B colorimetric assay for cytotoxicity screening.. Nat Protoc 2006;1:1112–1116.
    doi: 10.1038/nprot.2006.179pubmed: 17406391google scholar: lookup
  29. Arnhold SJ, Goletz I, Klein H, Stumpf G, Beluche LA, Rohde C. Isolation and characterization of bone marrow-derived equine mesenchymal stem cells.. Am J Vet Res 2007;68:1095–1105.
    doi: 10.2460/ajvr.68.10.1095pubmed: 17916017google scholar: lookup
  30. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method.. Nat Protoc 2008;3:1101–1108.
    doi: 10.1038/nprot.2008.73pubmed: 18546601google scholar: lookup
  31. Bessey OA, Lowry OH, Brock MJ. A method for the rapid determination of alkaline phosphates with five cubic millimeters of serum.. J Biol Chem 1946;164:321–329.
    pubmed: 20989492
  32. Stojanović Sanja, Najman Stevo, Korać Aleksandra. Stem Cells Derived from Lipoma and Adipose Tissue—Similar Mesenchymal Phenotype but Different Differentiation Capacity Governed by Distinct Molecular Signature.. Cells 2018;7(12):260.
    doi: 10.3390/cells7120260pmc: PMC6316974pubmed: 30544806google scholar: lookup
  33. 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.
    pmc: PMC5052881pubmed: 27733784
  34. Schipper BM, Marra KG, Zhang W, Donnenberg AD, Rubin JP. Regional anatomic and age effects on cell function of human adipose-derived stem cells.. Ann Plast Surg 2008;60:538–544.
    doi: 10.1097/SAP.0b013e3181723bbepmc: PMC4160894pubmed: 18434829google scholar: lookup
  35. Jung S, Kleineidam B, Kleinheinz J. Regenerative potential of human adipose-derived stromal cells of various origins.. J Craniomaxillofac Surg 2015;43:2144–2151.
    doi: 10.1016/j.jcms.2015.10.002pubmed: 26541747google scholar: lookup
  36. Bourin P, Bunnell BA, Casteilla L, Dominici M, Katz AJ, March KL. Stromal cells from the adipose tissue-derived stromal vascular fraction and culture expanded adipose tissue-derived stromal/stem cells: a joint statement of the International Federation for Adipose Therapeutics and Science (IFATS) and the International Society for Cellular Therapy (ISCT). Cytotherapy 2013;15:641–648.
    doi: 10.1016/j.jcyt.2013.02.006pmc: PMC3979435pubmed: 23570660google scholar: lookup
  37. Zavan B, de Francesco F, D’Andrea F, Ferroni L, Gardin C, Salzillo R. Persistence of CD34 stem marker in human lipoma: searching for cancer stem cells.. Int J Biol Sci 2015;11:1127–1139.
    doi: 10.7150/ijbs.11946pmc: PMC4551749pubmed: 26327807google scholar: lookup
  38. Tremp M, Menzi N, Tchang L, Di Summa PG, Schaefer DJ, Kalbermatten DF. Adipose-derived stromal cells from lipomas: isolation, characterisation and review of the literature.. Pathobiology 2016;83:258–266.
    doi: 10.1159/000444501pubmed: 27225269google scholar: lookup
  39. Yaneselli KM, Kuhl CP, Terraciano PB, de Oliveira FS, Pizzato SB, Pazza K. 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.
    doi: 10.4142/jvs.2018.19.1.13pmc: PMC5799390pubmed: 28693305google scholar: lookup
  40. Calle A, Barrajón-Masa C, Gómez-Fidalgo E, Martín-Lluch M, Cruz-Vigo P, Sánchez-Sánchez R, Ramírez MÁ. Iberian pig mesenchymal stem/stromal cells from dermal skin, abdominal and subcutaneous adipose tissues, and peripheral blood: in vitro characterization and migratory properties in inflammation.. Stem Cell Res Ther 2018;9:178.
    doi: 10.1186/s13287-018-0933-ypmc: PMC6032775pubmed: 29973295google scholar: lookup
  41. Peng L, Jia Z, Yin X, Zhang X, Liu Y, Chen P. Comparative analysis of mesenchymal stem cells from bone marrow, cartilage, and adipose tissue.. Stem Cells Dev 2008;17:761–773.
    doi: 10.1089/scd.2007.0217pubmed: 18393634google scholar: lookup
  42. Chi C, Wang F, Xiang B, Deng J, Liu S, Lin H-Y. 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: 10.3727/096368914X685780pubmed: 25562327google scholar: lookup
  43. Locke M, Windsor J, Dunbar PR. Human adipose-derived stem cells: isolation, characterization and applications in surgery.. ANZ J Surg 2009;79:235–244.
    doi: 10.1111/j.1445-2197.2009.04852.xpubmed: 19432707google scholar: lookup
  44. Macotela Y, Emanuelli B, Mori MA, Gesta S, Schulz TJ, Tseng Y-H, Kahn CR. Intrinsic differences in adipocyte precursor cells from different white fat depots.. Diabetes 2012;61:1691–1699.
    doi: 10.2337/db11-1753pmc: PMC3379665pubmed: 22596050google scholar: lookup
  45. Ciuffi S, Zonefrati R, Brandi ML. Adipose stem cells for bone tissue repair.. Clin Cases Miner Bone Metab 2017;14:217–226.
    doi: 10.11138/ccmbm/2017.14.1.217pmc: PMC5726213pubmed: 29263737google scholar: lookup
  46. Inatani H, Yamamoto N, Hayashi K, Kimura H, Takeuchi A, Miwa S. Do mesenchymal stem cells derived from atypical lipomatous tumors have greater differentiation potency than cells from normal adipose tissues?. Clin Orthop Relat Res 2017;475:1693–1701.
    doi: 10.1007/s11999-017-5259-zpmc: PMC5406341pubmed: 28155209google scholar: lookup
  47. Ishijima M, Tsuji K, Rittling SR, Yamashita T, Kurosawa H, Denhardt DT. Osteopontin is required for mechanical stress-dependent signals to bone marrow cells.. J Endocrinol 2007;193:235–243.
    doi: 10.1677/joe.1.06704pubmed: 17470514google scholar: lookup
  48. Giachelli CM, Steitz S. Osteopontin: a versatile regulator of inflammation and biomineralization.. Matrix Biol 2000;19:615–622.
    doi: 10.1016/S0945-053X(00)00108-6pubmed: 11102750google scholar: lookup
  49. Suzuki K, Zhu B, Rittling SR, Denhardt DT, Goldberg HA, McCulloch CAG, Sodek J. Colocalization of intracellular osteopontin with CD44 is associated with migration, cell fusion, and resorption in osteoclasts.. J Bone Miner Res 2002;17:1486–1497.
    doi: 10.1359/jbmr.2002.17.8.1486pubmed: 12162503google scholar: lookup
  50. Chambers AF, Wilson SM, Kerkvliet N, O’Malley FP, Harris JF, Casson AG. Osteopontin expression in lung cancer.. Lung Cancer 1996;15:311–323.
    doi: 10.1016/0169-5002(95)00595-1pubmed: 8959677google scholar: lookup
  51. Denhardt DT, Guo X. Osteopontin: a protein with diverse functions.. FASEB J 1993;7:1475–1482.
    doi: 10.1096/fasebj.7.15.8262332pubmed: 8262332google scholar: lookup
  52. Makiguchi T, Terashi H, Hashikawa K, Yokoo S, Kusaka J. Osteolipoma in the glabella: pathogenesis associated with mesenchymal lipoma-derived stem cells.. J Craniofac Surg 2013;24:1310–1313.
    doi: 10.1097/SCS.0b013e3182953a0bpubmed: 23851795google scholar: lookup
  53. Val-Bernal JF, Val D, Garijo MF, Vega A, González-Vela MC. Subcutaneous ossifying lipoma: case report and review of the literature.. J Cutan Pathol 2007;34:788–792.
    doi: 10.1111/j.1600-0560.2006.00704.xpubmed: 17880585google scholar: lookup
  54. Sunohara M, Ozawa T, Morimoto K, Tateishi C, Ishii M. Lipoma with bone and cartilage components in the left axilla of a middle-aged woman.. Aesthet Plast Surg 2012;36:1164–1167.
    doi: 10.1007/s00266-012-9927-9pubmed: 22660950google scholar: lookup
  55. Yang JS, Kang SH, Cho YJ, Choi HJ. Pure intramuscular osteolipoma.. J Korean Neurosurg Soc 2013;54:518–520.
    doi: 10.3340/jkns.2013.54.6.518pmc: PMC3921282pubmed: 24527197google scholar: lookup
  56. Jang Y, Jung H, Ju JH. Chondrogenic differentiation induction of adipose-derived stem cells by centrifugal gravity.. J Vis Exp 2017.
    pmc: PMC5407704pubmed: 28287507doi: 10.3791/54934google scholar: lookup
  57. Erickson GR, Gimble JM, Franklin DM, Rice HE, Awad H, Guilak F. Chondrogenic potential of adipose tissue-derived stromal cells in vitro and in vivo.. Biochem Biophys Res Commun 2002;290:763–769.
    doi: 10.1006/bbrc.2001.6270pubmed: 11785965google scholar: lookup
Subscribe to our newsletter
Join 99,357 horse owners like you who receive our email updates on horse health and nutrition.