Cited by 410Mesenchymal stem cell researchPeriodontal Regeneration and TreatmentsPluripotent Stem Cells Research

Comparative analysis of human mesenchymal stem cells from bone marrow and adipose tissue under xeno-free conditions for cell therapy

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Li, Chun-yu, Wu, Xiao-yun, Tong, Jia-bei, Yang, Xin-xin, Zhao, Jing-li, Zheng, Quan-fu, Zhao, Guo-bin, Ma, Zhi-jie·2015·Stem Cell Research & Therapy

Abstract

INTRODUCTION: Mesenchymal stem cells (MSCs) are promising candidates for cell-based therapies. Human platelet lysate represents an efficient alternative to fetal bovine serum for clinical-scale expansion of MSCs. Different media used in culture processes should maintain the biological characteristics of MSCs during multiple passages. However, bone marrow-derived MSCs and adipose tissue-derived MSCs have not yet been directly compared with each other under human platelet lysate conditions. This study aims to conduct a direct head-to-head comparison of the biological characteristics of the two types of MSCs under human platelet lysate-supplemented culture conditions for their ability to be used in regenerative medicine applications. METHODS: The bone marrow- and adipose tissue-derived MSCs were cultured under human platelet lysate conditions and their biological characteristics evaluated for cell therapy (morphology, immunophenotype, colony-forming unit-fibroblast efficiency, proliferation capacity, potential for mesodermal differentiation, secreted proteins, and immunomodulatory effects). RESULTS: Under human platelet lysate-supplemented culture conditions, bone marrow- and adipose tissue-derived MSCs exhibited similar fibroblast-like morphology and expression patterns of surface markers. Adipose tissue-derived MSCs had greater proliferative potential than bone marrow-derived MSCs, while no significantly difference in colony efficiency were observed between the two types of cells. However, bone marrow-derived MSCs possessed higher capacity toward osteogenic and chondrogenic differentiation compared with adipose tissue-derived MSCs, while similar adipogenic differentiation potential wase observed between the two types of cells. There were some differences between bone marrow- and adipose tissue-derived MSCs for several secreted proteins, such as cytokine (interferon-γ), growth factors (basic fibroblast growth factor, hepatocyte growth factor, and insulin-like growth factor-1), and chemokine (stem cell-derived factor-1). Adipose tissue-derived MSCs had more potent immunomodulatory effects than bone marrow-derived MSCs. CONCLUSIONS: Adipose tissue-derived MSCs have biological advantages in the proliferative capacity, secreted proteins (basic fibroblast growth factor, interferon-γ, and insulin-like growth factor-1), and immunomodulatory effects, but bone marrow-derived MSCs have advantages in osteogenic and chondrogenic differentiation potential and secreted proteins (stem cell-derived factor-1 and hepatocyte growth factor); these biological advantages should be considered systematically when choosing the MSC source for specific clinical application.

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  1. [1]Zou JP Huang S Peng Y Liu HW Cheng B Fu XB Mesenchymal stem cells/multipotent mesenchymal stromal cells (MSCs): potential role in healing cutaneous chronic wounds Int J Low Extrem Wounds 2012 11 244 53 23222159
  2. [2]da Silva ML Chagastelles PC Nardi NB Mesenchymal stem cells reside in virtually all post-natal organs and tissues J Cell Sci 2006 119 2204 13 10.1242/jcs.02932 16684817 · DOI
  3. [3]Hoogduijn MJ Dor FJ Mesenchymal stem cells: are we ready for clinical application in transplantation and tissue regeneration? Front Immunol 2013 4 144 10.3389/fimmu.2013.00144 23781219 PMC3678105 · DOI
  4. [4]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 29 10.1111/j.1365-2141.2005.05409.x 15801964 · DOI
  5. [5]Chung CS Fujita N Kawahara N Yui S Nam E Nishimura R A comparison of neurosphere differentiation potential of canine bone marrow-derived mesenchymal stem cells and adipose-derived mesenchymal stem cells J Vet Med Sci 2013 75 879 86 10.1292/jvms.12-0470 23419261 · DOI
  6. [6]Cooper GM Durham EL Cray JJ Jr Bykowski MR DeCesare GE Smalley MA Direct comparison of progenitor cells derived from adipose, muscle, and bone marrow from wild-type or craniosynostotic rabbits Plast Reconstr Surg 2011 127 88 97 10.1097/PRS.0b013e3181fad311 20871482 PMC3015002 · DOI
  7. [7]Danisovic L Varga I Polak S Ulicna M Hlavackova L Bohmer D Comparison of in vitro chondrogenic potential of human mesenchymal stem cells derived from bone marrow and adipose tissue Gen Physiol Biophys 2009 28 56 62 10.4149/gpb_2009_01_56 19390137 · DOI
  8. [8]De Ugarte DA Morizono K Elbarbary A Alfonso Z Zuk PA Zhu M Comparison of multi-lineage cells from human adipose tissue and bone marrow Cells Tissues Organs 2003 174 101 9 10.1159/000071150 12835573 · DOI · Paper page
  9. [9]Vishnubalaji R Al-Nbaheen M Kadalmani B Aldahmash A Ramesh T Comparative investigation of the differentiation capability of bone-marrow- and adipose-derived mesenchymal stem cells by qualitative and quantitative analysis Cell Tissue Res 2012 347 419 27 10.1007/s00441-011-1306-3 22287041 · DOI
  10. [10]Elman JS Li M Wang F Gimble JM Parekkadan B A comparison of adipose and bone marrow-derived mesenchymal stromal cell secreted factors in the treatment of systemic inflammation J Inflamm 2014 11 1 10.1186/1476-9255-11-1 PMC3895743 24397734 · DOI
  11. [11]Ertas G Ural E Ural D Aksoy A Kozdag G Gacar G Comparative analysis of apoptotic resistance of mesenchymal stem cells isolated from human bone marrow and adipose tissue ScientificWorldJournal 2012 2012 105698 10.1100/2012/105698 22619573 PMC3349309 · DOI
  12. [12]Rasmussen JG Frobert O Holst-Hansen C Kastrup J Baandrup U Zachar V Comparison of human adipose-derived stem cells and bone marrow-derived stem cells in a myocardial infarction model Cell Transplant 2014 23 195 206 10.3727/096368912X659871 23211469 · DOI
  13. [13]Huang JI Kazmi N Durbhakula MM Hering TM Yoo JU Johnstone B Chondrogenic potential of progenitor cells derived from human bone marrow and adipose tissue: a patient-matched comparison J Orthop Res 2005 23 1383 9 10.1016/j.orthres.2005.03.008.1100230621 15936917 · DOI
  14. [15]Ahmadian Kia N Bahrami AR Ebrahimi M Matin MM Neshati Z Almohaddesin MR Comparative analysis of chemokine receptor's expression in mesenchymal stem cells derived from human bone marrow and adipose tissue J Mol Neurosci 2011 44 178 85 10.1007/s12031-010-9446-6 20938756 · DOI
  15. [16]Muller I Kordowich S Holzwarth C Spano C Isensee G Staiber A Animal serum-free culture conditions for isolation and expansion of multipotent mesenchymal stromal cells from human BM Cytotherapy 2006 8 437 44 10.1080/14653240600920782 17050248 · DOI
  16. [17]van der Valk J Brunner D De Smet K Fex Svenningsen A Honegger P Knudsen LE Optimization of chemically defined cell culture media–replacing fetal bovine serum in mammalian in vitro methods Toxicol In Vitro 2010 24 1053 63 10.1016/j.tiv.2010.03.016 20362047 · DOI
  17. [18]Spees JL Gregory CA Singh H Tucker HA Peister A Lynch PJ Internalized antigens must be removed to prepare hypoimmunogenic mesenchymal stem cells for cell and gene therapy Mol Ther 2004 9 747 56 10.1016/j.ymthe.2004.02.012 15120336 · DOI
  18. [19]Lange C Cakiroglu F Spiess AN Cappallo-Obermann H Dierlamm J Zander AR Accelerated and safe expansion of human mesenchymal stromal cells in animal serum-free medium for transplantation and regenerative medicine J Cell Physiol 2007 213 18 26 10.1002/jcp.21081 17458897 · DOI
  19. [20]Capelli C Domenghini M Borleri G Bellavita P Poma R Carobbio A Human platelet lysate allows expansion and clinical grade production of mesenchymal stromal cells from small samples of bone marrow aspirates or marrow filter washouts Bone Marrow Transplant 2007 40 785 91 10.1038/sj.bmt.1705798 17680021 · DOI
  20. [22]Naaijkens BA Niessen HW Prins HJ Krijnen PA Kokhuis TJ de Jong N Human platelet lysate as a fetal bovine serum substitute improves human adipose-derived stromal cell culture for future cardiac repair applications Cell Tissue Res 2012 348 119 30 10.1007/s00441-012-1360-5 22395775 PMC3316780 · DOI
  21. [23]Schallmoser K Bartmann C Rohde E Reinisch A Kashofer K Stadelmeyer E Human platelet lysate can replace fetal bovine serum for clinical-scale expansion of functional mesenchymal stromal cells Transfusion 2007 47 1436 46 10.1111/j.1537-2995.2007.01220.x 17655588 · DOI
  22. [24]Walenda G Hemeda H Schneider RK Merkel R Hoffmann B Wagner W Human platelet lysate gel provides a novel three dimensional-matrix for enhanced culture expansion of mesenchymal stromal cells Tissue Eng Part C Methods 2012 18 924 34 10.1089/ten.tec.2011.0541 22670863 · DOI
  23. [25]Gottipamula S Sharma A Krishnamurthy S Majumdar AS Seetharam RN Human platelet lysate is an alternative to fetal bovine serum for large-scale expansion of bone marrow-derived mesenchymal stromal cells Biotechnol Lett 2012 34 1367 74 10.1007/s10529-012-0893-8 22476583 · DOI
  24. [26]Xia W Li H Wang Z Xu R Fu Y Zhang X Human platelet lysate supports ex vivo expansion and enhances osteogenic differentiation of human bone marrow-derived mesenchymal stem cells Cell Biol Int 2011 35 639 43 10.1042/CBI20100361 21235529 · DOI
  25. [27]Abdelrazik H Spaggiari GM Chiossone L Moretta L Mesenchymal stem cells expanded in human platelet lysate display a decreased inhibitory capacity on T- and NK-cell proliferation and function Eur J Immunol 2011 41 3281 90 10.1002/eji.201141542 21874650 · DOI
  26. [28]Sensebe L Bourin P Tarte K Good manufacturing practices production of mesenchymal stem/stromal cells Hum Gene Ther 2011 22 19 26 10.1089/hum.2010.197 21028982 · DOI
  27. [29]Meirelles Lda S Fontes AM Covas DT Caplan AI Mechanisms involved in the therapeutic properties of mesenchymal stem cells Cytokine Growth Factor Rev 2009 20 419 27 10.1016/j.cytogfr.2009.10.002 19926330 · DOI · Paper page
  28. [30]Mok PL Leong CF Cheong SK Cellular mechanisms of emerging applications of mesenchymal stem cells Malays J Pathol 2013 35 17 32 23817392
  29. [31]Ozaki K Sato K Oh I Meguro A Tatara R Muroi K Mechanisms of immunomodulation by mesenchymal stem cells Int J Hematol 2007 86 5 7 10.1532/IJH97.07003 17675259 · DOI
  30. [32]Schallmoser K Rohde E Reinisch A Bartmann C Thaler D Drexler C Rapid large-scale expansion of functional mesenchymal stem cells from unmanipulated bone marrow without animal serum Tissue Eng Part C Methods 2008 14 185 96 10.1089/ten.tec.2008.0060 18620484 · DOI
  31. [33]Parker AM Shang H Khurgel M Katz AJ Low serum and serum-free culture of multipotential human adipose stem cells Cytotherapy 2007 9 637 46 10.1080/14653240701508452 17917877 · DOI
  32. [34]Yoshimura H Muneta T Nimura A Yokoyama A Koga H Sekiya I Comparison of rat mesenchymal stem cells derived from bone marrow, synovium, periosteum, adipose tissue, and muscle Cell Tissue Res 2007 327 449 62 10.1007/s00441-006-0308-z 17053900 · DOI
  33. [35]Zimmermann JA McDevitt TC Pre-conditioning mesenchymal stromal cell spheroids for immunomodulatory paracrine factor secretion Cytotherapy 2014 16 331 45 10.1016/j.jcyt.2013.09.004 24219905 · DOI
  34. [36]Abdelkhalek NK Komiya A Kato-Unoki Y Somamoto T Nakao M Molecular evidence for the existence of two distinct IL-8 lineages of teleost CXC-chemokines Fish Shellfish Immunol 2009 27 763 7 10.1016/j.fsi.2009.08.004 19699802 · DOI
  35. [37]Zhou Y, Guan X, Yu M, Wang X, Zhu W, Wang C, et al. Angiogenic/osteogenic response of BMMSCs on bone-derived scaffold: effect of hypoxia and role of PI3K/Akt-mediated VEGF-VEGFR pathway. Biotechnol J. 2014. 24421279
  36. [39]Mosna F Sensebe L Krampera M Human bone marrow and adipose tissue mesenchymal stem cells: a user's guide Stem Cells Dev 2010 19 1449 70 10.1089/scd.2010.0140 20486777 · DOI
  37. [40]Secunda R, Vennila R, Mohanashankar AM, Rajasundari M, Jeswanth S, Surendran R. Isolation, expansion and characterisation of mesenchymal stem cells from human bone marrow, adipose tissue, umbilical cord blood and matrix: a comparative study. Cytotechnology. 2014. [Epub ahead of print]. PMC4545441 24798808
  38. [41]Jin HJ Bae YK Kim M Kwon SJ Jeon HB Choi SJ Comparative analysis of human mesenchymal stem cells from bone marrow, adipose tissue, and umbilical cord blood as sources of cell therapy Int J Mol Sci 2013 14 17986 8001 10.3390/ijms140917986 24005862 PMC3794764 · DOI
  39. [42]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 73 10.1089/scd.2007.0217 18393634 · DOI · Paper page
  40. [43]Nakanishi C Nagaya N Ohnishi S Yamahara K Takabatake S Konno T Gene and protein expression analysis of mesenchymal stem cells derived from rat adipose tissue and bone marrow Circ J 2011 75 2260 8 10.1253/circj.CJ-11-0246 21747191 · DOI
  41. [44]Khubutiya MS Vagabov AV Temnov AA Sklifas AN Paracrine mechanisms of proliferative, anti-apoptotic and anti-inflammatory effects of mesenchymal stromal cells in models of acute organ injury Cytotherapy 2014 16 579 85 10.1016/j.jcyt.2013.07.017 24113425 · DOI
  42. [45]Xagorari A Siotou E Yiangou M Tsolaki E Bougiouklis D Sakkas L Protective effect of mesenchymal stem cell-conditioned medium on hepatic cell apoptosis after acute liver injury Int J Clin Exp Pathol 2013 6 831 40 23638214 PMC3638093
  43. [46]Liang X Ding Y Zhang Y Tse HF Lian Q Paracrine mechanisms of mesenchymal stem cell-based therapy: current status and perspectives Cell Transplant 2014 23 1045 59 10.3727/096368913X667709 23676629 · DOI · Paper page
  44. [47]Elmadbouh I Haider H Jiang S Idris NM Lu G Ashraf M Ex vivo delivered stromal cell-derived factor-1alpha promotes stem cell homing and induces angiomyogenesis in the infarcted myocardium J Mol Cell Cardiol 2007 42 792 803 10.1016/j.yjmcc.2007.02.001 17350033 PMC2753220 · DOI
  45. [48]Lee JM Jung J Lee HJ Jeong SJ Cho KJ Hwang SG Comparison of immunomodulatory effects of placenta mesenchymal stem cells with bone marrow and adipose mesenchymal stem cells Int Immunopharmacol 2012 13 219 24 10.1016/j.intimp.2012.03.024 22487126 · DOI

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Authors
Li, C.-Y., Wu, X.-Y., Tong, J.-B., Yang, X.-X., Zhao, J.-L., Zheng, Q.-F., Zhao, G.-B., & Ma, Z.-J.
Affiliations
  • Shandong First Medical University (CN)
  • Changchun University of Chinese Medicine (CN)
  • Jilin Vocational College of Industry and Technology (CN)
  • 302 Military Hospital of China (CN)
  • Hebei North University (CN)
  • Capital Medical University (CN)
Corresponding author
Ma, Zhi-jie
Venue
Stem Cell Research & Therapy
Published
2015-04-13
Volume
6
Issue
1
Pages
55-55
ISSN
1757-6512 (ISSN-L)
OpenAlex
W1976604464
Cited by
410
References
3
Citations by year
2026: 21 · 2025: 13 · 2024: 43 · 2023: 39 · 2022: 42 · 2021: 27 · 2020: 60 · 2019: 40 · 2018: 39 · 2017: 45 · 2016: 33 · 2015: 7
FWCI
23.14
Type
journal article
Language
en
Open access
Locations
  • Stem Cell Research & Therapy (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
National Natural Science Foundation of China
Topics
  • Health Sciences › Medicine › Genetics › Mesenchymal stem cell research
  • Health Sciences › Medicine › Urology › Periodontal Regeneration and Treatments
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
Keywords
mesenchymal stem cells, bone marrow-derived mesenchymal stem cells, adipose-derived stem cells, human platelet lysate, xeno-free culture, cell therapy, osteogenic differentiation, chondrogenic differentiation, adipogenesis, immunomodulation, secreted proteins, interferon-gamma, basic fibroblast growth factor, hepatocyte growth factor, insulin-like growth factor I, cell proliferation, immunophenotype
MeSH terms
Adipose Tissue, Blood Platelets, Bone Marrow Cells, Cell Differentiation, Cells, Cultured, Enzyme-Linked Immunosorbent Assay, Humans, Insulin-Like Growth Factor I, Mesoderm, Antigens, CD, Immunophenotyping, Cytokines, Fibroblast Growth Factor 2, Hepatocyte Growth Factor, Cell Proliferation, Chemokine CXCL12, Mesenchymal Stem Cells, Cell- and Tissue-Based Therapy

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