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http://dx.doi.org/10.4142/jvs.2021.22.e74

Comparative characteristic study from bone marrow-derived mesenchymal stem cells  

Purwaningrum, Medania (Veterinary Stem Cell and Bioengineering Innovation Center (VSCBIC), Veterinary Pharmacology and Stem Cell Research Laboratory, Faculty of Veterinary Science, Chulalongkorn University)
Jamilah, Nabila Syarifah (Veterinary Stem Cell and Bioengineering Innovation Center (VSCBIC), Veterinary Pharmacology and Stem Cell Research Laboratory, Faculty of Veterinary Science, Chulalongkorn University)
Purbantoro, Steven Dwi (Veterinary Stem Cell and Bioengineering Innovation Center (VSCBIC), Veterinary Pharmacology and Stem Cell Research Laboratory, Faculty of Veterinary Science, Chulalongkorn University)
Sawangmake, Chenphop (Veterinary Stem Cell and Bioengineering Innovation Center (VSCBIC), Veterinary Pharmacology and Stem Cell Research Laboratory, Faculty of Veterinary Science, Chulalongkorn University)
Nantavisai, Sirirat (Veterinary Stem Cell and Bioengineering Innovation Center (VSCBIC), Veterinary Pharmacology and Stem Cell Research Laboratory, Faculty of Veterinary Science, Chulalongkorn University)
Publication Information
Journal of Veterinary Science / v.22, no.6, 2021 , pp. 74.1-74.13 More about this Journal
Abstract
Tissue engineering has been extensively investigated and proffered to be a potential platform for novel tissue regeneration. The utilization of mesenchymal stem cells (MSCs) from various sources has been widely explored and compared. In this regard, MSCs derived from bone marrow have been proposed and described as a promising cell resource due to their high yield of isolated cells with colony-forming potential, self-renewal capacity, MSC surface marker expression, and multi-lineage differentiation capacities in vitro. However, there is evidence for bone marrow MSCs (BM-MSCs) both in vitro and in vivo from different species presenting identical and distinct potential stemness characteristics. In this review, the fundamental knowledge of the growth kinetics and stemness properties of BM-MSCs in different animal species and humans are compared and summarized. Finally, to provide a full perspective, this review will procure results of current information studies focusing on the use of BM-MSCs in clinical practice.
Keywords
Tissue engineering; mesenchymal stem cells; bone marrow mesenchymal stem cells; stemness characteristics;
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1 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(1):150.   DOI
2 Shang Q, Wang Z, Liu W, Shi Y, Cui L, Cao Y. Tissue-engineered bone repair of sheep cranial defects with autologous bone marrow stromal cells. J Craniofac Surg. 2001;12(6):586-593.   DOI
3 McDaniel JS, Antebi B, Pilia M, Hurtgen BJ, Belenkiy S, Necsoiu C, et al. Quantitative assessment of optimal bone marrow site for the isolation of porcine mesenchymal stem cells. Stem Cells Int. 2017;2017:1836960.
4 Vidal MA, Walker NJ, Napoli E, Borjesson DL. Evaluation of senescence in mesenchymal stem cells isolated from equine bone marrow, adipose tissue, and umbilical cord tissue. Stem Cells Dev. 2012;21(2):273-283.   DOI
5 Lee SH. The advantages and limitations of mesenchymal stem cells in clinical application for treating human diseases. Osteoporos Sarcopenia. 2018;4:150.   DOI
6 Suto EG, Mabuchi Y, Suzuki N, Suzuki K, Ogata Y, Taguchi M, et al. Prospectively isolated mesenchymal stem/stromal cells are enriched in the CD73+ population and exhibit efficacy after transplantation. Sci Rep. 2017;7(1):4838.   DOI
7 Wu Y, Zhao RC, Tredget EE. Concise review: bone marrow-derived stem/progenitor cells in cutaneous repair and regeneration. Stem Cells 2010;28(5):905-915.   DOI
8 Quimby JM, Borjesson DL. Mesenchymal stem cell therapy in cats: current knowledge and future potential. J Feline Med Surg. 2018;20(3):208-216.   DOI
9 Bianco P, Robey PG, Simmons PJ. Mesenchymal stem cells: revisiting history, concepts, and assays. Cell Stem Cell. 2008;2(4):313-319.   DOI
10 Dias LD, Casali KR, Ghem C, da Silva MK, Sausen G, Palma PB, et al. Mesenchymal stem cells from sternum: the type of heart disease, ischemic or valvular, does not influence the cell culture establishment and growth kinetics. J Transl Med. 2017;15(1):161.   DOI
11 Chaudhary JK, Rath P. A simple method for isolation, propagation, characterization, and differentiation of adult mouse bone marrow-derived multipotent mesenchymal stem cells. J Cell Sci Ther. 2017;8:261.
12 Friedenstein AJ, Chailakhyan RK, Gerasimov UV. Bone marrow osteogenic stem cells: in vitro cultivation and transplantation in diffusion chambers. Cell Tissue Kinet. 1987;20(3):263-272.
13 Liu R, Chang W, Wei H, Zhang K. Comparison of the biological characteristics of mesenchymal stem cells derived from bone marrow and skin. Stem Cells Int. 2016;2016:3658798.
14 de Paula DR, Capuano V, Filho DM, Carneiro AC, de Oliveira Crema V, de Oliveira LF, et al. Biological properties of cardiac mesenchymal stem cells in rats with diabetic cardiomyopathy. Life Sci. 2017;188:45-52.   DOI
15 Sangeetha P, Maiti S, Divya M, Shivaraju S, Raguvaran R, Rafee MA, et al. Mesenchymal stem cells derived from rat bone marrow (rBM MSC): techniques for isolation, expansion and differentiation. J Stem Cell Res Ther. 2017;3(3):272-277.
16 Webb TL, Quimby JM, Dow SW. In vitro comparison of feline bone marrow-derived and adipose tissue-derived mesenchymal stem cells. J Feline Med Surg. 2012;14(2):165-168.   DOI
17 Bellotti C, Capanni C, Lattanzi G, Donati D, Lucarelli E, Duchi S. Detection of mesenchymal stem cells senescence by prelamin A accumulation at the nuclear level. Springerplus. 2016;5(1):1427.   DOI
18 Kazemi S, Parivar K, Roudbari NH, Yaghmaei P, Sadeghi B. Growth kinetic comparison of human mesenchymal stem cells from bone marrow, adipose tissue and decidua. Med Sci. 2020;24:223-234.
19 Bertolo A, Steffen F, Malonzo-Marty C, Stoyanov J. Canine mesenchymal stem cell potential and the importance of dog breed: implication for cell-based therapies. Cell Transplant. 2015;24(10):1969-1980.   DOI
20 Maciel BB, Rebelatto CLK, Brofman PRS, Brito HFV, Patricio LFL, Cruz MA, et al. Morphology and morphometry of feline bone marrow-derived mesenchymal stem cells in culture. Pesq Vet Bras. 2014;34(11):1127-1134.   DOI
21 Hu Y, Lou B, Wu X, Wu R, Wang H, Gao L, et al. Comparative study on in vitro culture of mouse bone marrow mesenchymal stem cells. Stem Cells Int. 2018;2018:6704583.   DOI
22 Caroti CM, Ahn H, Salazar HF, Joseph G, Sankar SB, Willett NJ, et al. A novel technique for accelerated culture of murine mesenchymal stem cells that allows for sustained multipotency. Sci Rep. 2017;7(1):13334.   DOI
23 Ikegame Y, Yamashita K, Hayashi S, Mizuno H, Tawada M, You F, et al. Comparison of mesenchymal stem cells from adipose tissue and bone marrow for ischemic stroke therapy. Cytotherapy. 2011;13(6):675-685.   DOI
24 Ridzuan N, Al Abbar A, Yip WK, Maqbool M, Ramasamy R. Characterization and expression of senescence marker in prolonged passages of rat bone marrow-derived mesenchymal stem cells. Stem Cells Int. 2016;2016:8487264.
25 Bearden RN, Huggins SS, Cummings KJ, Smith R, Gregory CA, Saunders WB. In-vitro characterization of canine multipotent stromal cells isolated from synovium, bone marrow, and adipose tissue: a donor-matched comparative study. Stem Cell Res Ther. 2017;8(1):218.   DOI
26 Schultz MB, Sinclair DA. When stem cells grow old: phenotypes and mechanisms of stem cell aging. Development. 2016;143(1):3-14.   DOI
27 Wu J, Niu J, Li X, Wang X, Guo Z, Zhang F. TGF-β1 induces senescence of bone marrow mesenchymal stem cells via increase of mitochondrial ROS production. BMC Dev Biol. 2014;14(1):21.   DOI
28 Zhang K, Huang L, Sun H, Zhu Y, Xiao Y, Huang M, et al. Role of Notch expression in premature senescence of murine bone marrow stromal cells. Prog Nat Sci. 2009;19(5):557-562.   DOI
29 Russell KA, Chow NH, Dukoff D, Gibson TW, LaMarre J, Betts DH, et al. Characterization and immunomodulatory effects of canine adipose tissue- and bone marrow-derived mesenchymal stromal cells. PLoS One. 2016;11(12):e0167442.   DOI
30 Hu Y, Lou B, Wu X, Wu R, Wang H, Gao L, et al. Immunophenotype and differentiation capacity of bone marrow-derived mesenchymal stem cells from CBA/Ca, ICR and Balb/c mice. World J Stem Cells. 2013;5(1):34-42.   DOI
31 Tan SL, Ahmad TS, Selvaratnam L, Kamarul T. Isolation, characterization and the multi-lineage differentiation potential of rabbit bone marrow-derived mesenchymal stem cells. J Anat. 2013;222(4):437-450.   DOI
32 Khatri M, O'Brien TD, Sharma JM. Isolation and differentiation of chicken mesenchymal stem cells from bone marrow. Stem Cells Dev. 2009;18(10):1485-1492.   DOI
33 Jiang Y, Vaessen B, Lenvik T, Blackstad M, Reyes M, Verfaillie CM. Multipotent progenitor cells can be isolated from postnatal murine bone marrow, muscle, and brain. Exp Hematol. 2002;30(8):896-904.   DOI
34 Kumar K, Das K, Madhusoodan AP, Kumar A, Singh P, Mondal T, et al. Rat bone marrow derived mesenchymal stem cells differentiate to germ cell like cells. bioRxiv 2018. Epub ahead of print. doi:10.1101/418962.   DOI
35 Kamishina H, Farese JP, Storm JA, Cheeseman JA, Clemmons RM. The frequency, growth kinetics, and osteogenic/adipogenic differentiation properties of canine bone marrow stromal cells. In Vitro Cell Dev Biol Anim. 2008;44(10):472-479.   DOI
36 Nadri S, Soleimani M, Hosseni RH, Massumi M, Atashi A, Izadpanah R. An efficient method for isolation of murine bone marrow mesenchymal stem cells. Int J Dev Biol. 2007;51(8):723-729.   DOI
37 Truong NH, Nguyen NH, Le TV, Vu NB, Huynh N, Nguyen TV, et al. Comparison of the treatment efficiency of bone marrow-derived mesenchymal stem cell transplantation via tail and portal veins in CCl4-induced mouse liver fibrosis. Stem Cells Int. 2016;2016:5720413.
38 Sung JH, Yang HM, Park JB, Choi GS, Joh JW, Kwon CH, et al. Isolation and characterization of mouse mesenchymal stem cells. Transplant Proc. 2008;40(8):2649-2654.   DOI
39 Fafian-Labora J, Fernandez-Pernas P, Fuentes I, De Toro J, Oreiro N, Sangiao-Alvarellos S, et al. Influence of age on rat bone-marrow mesenchymal stem cells potential. Sci Rep. 2015;5(1):16765.   DOI
40 Franken NA, Rodermond HM, Stap J, Haveman J, van Bree C. Clonogenic assay of cells in vitro. Nat Protoc. 2006;1(5):2315-2319.   DOI
41 Meirelles Lda S, Nardi NB. Murine marrow-derived mesenchymal stem cell: isolation, in vitro expansion, and characterization. Br J Haematol. 2003;123:702-711.   DOI
42 Karaoz E, Aksoy A, Ayhan S, Sariboyaci AE, Kaymaz F, Kasap M. Characterization of mesenchymal stem cells from rat bone marrow: ultrastructural properties, differentiation potential and immunophenotypic markers. Histochem Cell Biol. 2009;132(5):533-546.   DOI
43 Blasco MA. Telomere length, stem cells and aging. Nat Chem Biol. 2007;3(10):640-649.   DOI
44 Shiota Y, Nagai A, Sheikh AM, Mitaki S, Mishima S, Yano S, et al. Transplantation of a bone marrow mesenchymal stem cell line increases neuronal progenitor cell migration in a cerebral ischemia animal model. Sci Rep. 2018;8(1):14951.   DOI
45 de Isla N, Huseltein C, Jessel N, Pinzano A, Decot V, Magdalou J, et al. Introduction to tissue engineering and application for cartilage engineering. Biomed Mater Eng. 2010;20(3):127-133.
46 Gholami A, Dadkhah K, Anijdan SHM. Nanofiber and stem cell to bone, cartilage and muscle tissue engineering. Scholars Acad J Biosci. 2015;3(7):624-626.
47 Hesse E, Kluge G, Atfi A, Correa D, Haasper C, Berding G, et al. Repair of a segmental long bone defect in human by implantation of a novel multiple disc graft. Bone. 2010;46(5):1457-1463.   DOI
48 Fragkakis EM, El-Jawhari JJ, Dunsmuir RA, Millner PA, Rao AS, Henshaw KT, et al. Vertebral body versus iliac crest bone marrow as a source of multipotential stromal cells: Comparison of processing techniques, tri-lineage differentiation and application on a scaffold for spine fusion. PLoS One. 2018;13(5):e0197969.   DOI
49 Matic I, Antunovic M, Brkic S, Josipovic P, Mihalic KC, Karlak I, et al. Expression of OCT-4 and SOX-2 in bone marrow-derived human mesenchymal stem cells during osteogenic differentiation. Open Access Maced J Med Sci. 2016;4(1):9-16.   DOI
50 Yusop N, Battersby P, Alraies A, Sloan AJ, Moseley R, Waddington RJ. Isolation and characterisation of mesenchymal stem cells from rat bone marrow and the endosteal niche: a comparative study. Stem Cells Int. 2018;2018:6869128.
51 Yuan J, Cui L, Zhang WJ, Liu W, Cao Y. Repair of canine mandibular bone defects with bone marrow stromal cells and porous β-tricalcium phosphate. Biomaterials. 2007;28(6):1005-1013.   DOI
52 Rodprasert W, Nantavisai S, Pathanachai K, Pavasant P, Osathanon T, Sawangmake C. Tailored generation of insulin producing cells from canine mesenchymal stem cells derived from bone marrow and adipose tissue. Sci Rep. 2021;11(1):12409.   DOI
53 Voga M, Adamic N, Vengust M, Majdic G. Stem Cells in Veterinary Medicine-Current State and Treatment Options. Front Vet Sci. 2020;7:278.   DOI
54 Mocchi M, Dotti S, Bue MD, Villa R, Bari E, Perteghella S, et al. Veterinary regenerative medicine for musculoskeletal disorders: can mesenchymal stem/stromal cells and their secretome be the new frontier? Cells. 2020;9(6):1453.   DOI
55 Yamzon JL, Kokorowski P, Koh CJ. Stem cells and tissue engineering applications of the genitourinary tract. Pediatr Res. 2008;63(5):472-477.   DOI
56 Caddeo S, Boffito M, Sartori S. Tissue engineering approaches in the design of healthy and pathological in vitro tissue models. Front Bioeng Biotechnol. 2017;5:40.   DOI
57 Rici RE, Alcantara D, Fratini P, Wenceslau CV, Ambrosio CE, Miglino MA, et al. Mesenchymal stem cells with rhBMP-2 inhibits the growth of canine osteosarcoma cells. BMC Vet Res. 2012;8(1):17.   DOI
58 Deng Y, Zhou H, Yan C, Wang Y, Xiao C, Gu P, et al. In vitro osteogenic induction of bone marrow stromal cells with encapsulated gene-modified bone marrow stromal cells and in vivo implantation for orbital bone repair. Tissue Eng Part A. 2014;20(13-14):2019-2029.   DOI
59 Yuan J, Zhang WJ, Liu G, Wei M, Qi ZL, Liu W, et al. Repair of canine mandibular bone defects with bone marrow stromal cells and coral. Tissue Eng Part A. 2010;16(4):1385-1394.   DOI
60 Ghasemzadeh-Hasankolaei M, Batavani R, Eslaminejad MB, Sayahpour F. Transplantation of autologous bone marrow mesenchymal stem cells into the testes of infertile male rats and new germ cell formation. Int J Stem Cells. 2016;9(2):250-263.   DOI
61 Nantavisai S, Egusa H, Osathanon T, Sawangmake C. Mesenchymal stem cell-based bone tissue engineering for veterinary practice. Heliyon (Lond). 2019;5(11):e02808.   DOI
62 Arnhold S, Elashry MI, Klymiuk MC, Wenisch S. Biological macromolecules and mesenchymal stem cells: Basic research for regenerative therapies in veterinary medicine. Int J Biol Macromol. 2019;123:889-899.   DOI
63 Baddoo M, Hill K, Wilkinson R, Gaupp D, Hughes C, Kopen GC, et al. Characterization of mesenchymal stem cells isolated from murine bone marrow by negative selection. J Cell Biochem. 2003;89(6):1235-1249.   DOI
64 Berthiaume F, Maguire TJ, Yarmush ML. Tissue engineering and regenerative medicine: history, progress, and challenges. Annu Rev Chem Biomol Eng. 2011;2(1):403-430.   DOI
65 Levenberg S, Langer R. Advances in tissue engineering. Curr Top Dev Biol. 2004;61:113-134.   DOI
66 Wang W, Yuan C, Liu Z, Geng T, Li X, Wei L, et al. Characteristic comparison between canine and human dental mesenchymal stem cells for periodontal regeneration research in preclinical animal studies. Tissue Cell. 2020;67:101405.   DOI
67 Joannides A, Gaughwin P, Schwiening C, Majed H, Sterling J, Compston A, et al. Efficient generation of neural precursors from adult human skin: astrocytes promote neurogenesis from skin-derived stem cells. Lancet. 2004;364(9429):172-178.   DOI
68 El-Kehdy H, Pourcher G, Zhang W, Hamidouche Z, Goulinet-Mainot S, Sokal E, et al. Hepatocytic differentiation potential of human fetal liver mesenchymal stem cells: in vitro and in vivo evaluation. Stem Cells Int. 2016;2016:6323486.   DOI
69 Petrenko Y, Vackova I, Kekulova K, Chudickova M, Koci Z, Turnovcova K, et al. A comparative analysis of multipotent mesenchymal stromal cells derived from different sources, with a focus on neuroregenerative potential. Sci Rep. 2020;10(1):4290.   DOI
70 Peister A, Mellad JA, Larson BL, Hall BM, Gibson LF, Prockop DJ. Adult stem cells from bone marrow (MSCs) isolated from different strains of inbred mice vary in surface epitopes, rates of proliferation, and differentiation potential. Blood. 2004;103(5):1662-1668.   DOI
71 Zhu Y, Zhang K, Zhao R, Ye X, Chen X, Xiao Z, et al. Bone regeneration with micro/nano hybrid-structured biphasic calcium phosphate bioceramics at segmental bone defect and the induced immunoregulation of MSCs. Biomaterials. 2017;147:133-144.   DOI
72 Kim JW, Lee JH, Lyoo YS, Jung DI, Park HM. The effects of topical mesenchymal stem cell transplantation in canine experimental cutaneous wounds. Vet Dermatol. 2013;24(2):242-e53.   DOI
73 Tang W, Lin D, Yu Y, Niu H, Guo H, Yuan Y, et al. Bioinspired trimodal macro/micro/nano-porous scaffolds loading rhBMP-2 for complete regeneration of critical size bone defect. Acta Biomater. 2016;32:309-323.   DOI
74 Wang Y, Bi X, Zhou H, Deng Y, Sun J, Xiao C, et al. Repair of orbital bone defects in canines using grafts of enriched autologous bone marrow stromal cells. J Transl Med. 2014;12(1):123.   DOI
75 Kadiyala S, Jaiswal N, Bruder SP. Culture-expanded, bone marrow-derived mesenchymal stem cells can regenerate a critical-sized segmental bone defect. Tissue Eng. 1997;3(2):173-185.   DOI
76 Bruder SP, Kurth AA, Shea M, Hayes WC, Jaiswal N, Kadiyala S. Bone regeneration by implantation of purified, culture-expanded human mesenchymal stem cells. J Orthop Res. 1998;16(2):155-162.   DOI
77 Leuning DG, Reinders ME, Li J, Peired AJ, Lievers E, de Boer HC, et al. Clinical-grade isolated human kidney perivascular stromal cells as an organotypic cell source for kidney regenerative medicine. Stem Cells Transl Med. 2017;6(2):405-418.   DOI
78 Woodbury D, Schwarz EJ, Prockop DJ, Black IB. Adult rat and human bone marrow stromal cells differentiate into neurons. J Neurosci Res. 2000;61(4):364-370.   DOI
79 Pittenger MF, Discher DE, Peault BM, Phinney DG, Hare JM, Caplan AI. Mesenchymal stem cell perspective: cell biology to clinical progress. NPJ Regen Med. 2019;4:22.   DOI
80 Egusa H, Sonoyama W, Nishimura M, Atsuta I, Akiyama K. Stem cells in dentistry--Part II: Clinical applications. J Prosthodont Res. 2012;56(4):229-248.   DOI
81 Kulus M, Kulus J, Jankowski M, Borowiec B, Jeseta M, Bukowska D, et al. The use of mesenchymal stem cells in veterinary medicine. Med J Cell Biol. 2018;6(3):101-107.   DOI
82 Quimby JM, Webb TL, Gibbons DS, Dow SW. Evaluation of intrarenal mesenchymal stem cell injection for treatment of chronic kidney disease in cats: a pilot study. J Feline Med Surg. 2011;13(6):418-426.   DOI
83 Crisan M, Yap S, Casteilla L, Chen CW, Corselli M, Park TS, et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell. 2008;3(3):301-313.   DOI
84 Sharma AK, Bury MI, Marks AJ, Fuller NJ, Meisner JW, Tapaskar N, et al. A nonhuman primate model for urinary bladder regeneration using autologous sources of bone marrow-derived mesenchymal stem cells. Stem Cells. 2011;29(2):241-250.   DOI
85 Tropel P, Noel D, Platet N, Legrand P, Benabid AL, Berger F. Isolation and characterisation of mesenchymal stem cells from adult mouse bone marrow. Exp Cell Res. 2004;295(2):395-406.   DOI
86 Martin DR, Cox NR, Hathcock TL, Niemeyer GP, Baker HJ. Isolation and characterization of multipotential mesenchymal stem cells from feline bone marrow. Exp Hematol. 2002;30(8):879-886.   DOI
87 Bosnakovski D, Mizuno M, Kim G, Takagi S, Okumura M, Fujinaga T. Isolation and multilineage differentiation of bovine bone marrow mesenchymal stem cells. Cell Tissue Res. 2005;319(2):243-253.   DOI
88 Gomes IS, de Oliveira VC, Pinheiro AO, Roballo KCS, de Araujo GSM, Veronezi JC, et al. Bone marrow stem cell applied in the canine veterinary clinics. Pesqui Vet Bras. 2017;37:1139-1145.   DOI
89 Caplan AI. Mesenchymal stem cells. J Orthop Res. 1991;9(5):641-650.   DOI
90 Grellier M, Granja PL, Fricain JC, Bidarra SJ, Renard M, Bareille R, et al. The effect of the co-immobilization of human osteoprogenitors and endothelial cells within alginate microspheres on mineralization in a bone defect. Biomaterials. 2009;30(19):3271-3278.   DOI
91 Horwitz EM, Prockop DJ, Fitzpatrick LA, Koo WW, Gordon PL, Neel M, et al. Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat Med. 1999;5(3):309-313.   DOI
92 Tharasanit T, Phutikanit N, Wangdee C, Soontornvipart K, Tantrajak S, Kaewamatawong T, et al. Differentiation potentials of canine bone marrow mesenchymal stem cells. Wetchasan Sattawaphaet. 2011;41:79.
93 Townsend FI 3rd. Bone marrow aspiration in dogs and cats. Lab Anim (NY). 2008;37(11):497-498.   DOI
94 Zhang E, Yang Y, Zhang J, Ding G, Chen S, Peng C, et al. Efficacy of bone marrow mesenchymal stem cell transplantation in animal models of pulmonary fibrosis after exposure to bleomycin: A meta-analysis. Exp Ther Med. 2019;17(3):2247-2255.
95 Drela K, Stanaszek L, Snioch K, Kuczynska Z, Wrobel M, Sarzynska S, et al. Bone marrow-derived from the human femoral shaft as a new source of mesenchymal stem/stromal cells: an alternative cell material for banking and clinical transplantation. Stem Cell Res Ther. 2020;11(1):262.   DOI
96 Chang YP, Hong HP, Lee YH, Liu IH. The canine epiphyseal-derived mesenchymal stem cells are comparable to bone marrow derived-mesenchymal stem cells. J Vet Med Sci. 2015;77(3):273-280.   DOI
97 Soleimani M, Nadri S. A protocol for isolation and culture of mesenchymal stem cells from mouse bone marrow. Nat Protoc. 2009;4(1):102-106.   DOI
98 Sawangmake C, Nantavisai S, Osathanon T, Pavasant P. Osteogenic differentiation potential of canine bone marrow-derived mesenchymal stem cells under different β-glycerophosphate concentrations in vitro. Wetchasan Sattawaphaet. 2016;46:617-625.
99 Lotfy A, El-Sherbiny YM, Cuthbert R, Jones E, Badawy A. Comparative study of biological characteristics of mesenchymal stem cells isolated from mouse bone marrow and peripheral blood. Biomed Rep. 2019;11(4):165-170.
100 Li Y, Chen SK, Li L, Qin L, Wang XL, Lai YX. Bone defect animal models for testing efficacy of bone substitute biomaterials. J Orthop Translat. 2015;3:95-104.   DOI
101 Kim HJ, Park JS. Usage of human mesenchymal stem cells in cell-based therapy: advantages and disadvantages. Dev Reprod. 2017;21:1-10.   DOI
102 Sun Q, Zhang Z, Sun Z. The potential and challenges of using stem cells for cardiovascular repair and regeneration. Genes Dis. 2014;1(1):113-119.   DOI
103 Smajilagic A, Aljicevic M, Redzic A, Filipovic S, Lagumdzija A. Rat bone marrow stem cells isolation and culture as a bone formative experimental system. Bosn J Basic Med Sci. 2013;13(1):27-30.   DOI
104 Aponte PM, Caicedo A. Stemness in cancer: stem cells, cancer stem cells, and their microenvironment. Stem Cells Int. 2017;2017:5619472.   DOI
105 Wang X, Li C, Gong H. Morphological and functional changes in bone marrow mesenchymal stem cells in rats with heart failure. Exp Ther Med. 2017;13(6):2888-2892.   DOI
106 Mushtaq M, Kovalevska L, Darekar S, Abramsson A, Zetterberg H, Kashuba V, et al. Cell stemness is maintained upon concurrent expression of RB and the mitochondrial ribosomal protein S18-2. Proc Natl Acad Sci U S A. 2020;117(27):15673-15683.   DOI
107 Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8(4):315-317.   DOI
108 Humenik F, Cizkova D, Cikos S, Luptakova L, Madari A, Mudronova D, et al. Canine bone marrow-derived mesenchymal stem cells: genomics, proteomics and functional analyses of paracrine factors. Mol Cell Proteomics. 2019;18(9):1824-1835.   DOI
109 Chambers I, Tomlinson SR. The transcriptional foundation of pluripotency. Development. 2009;136(14):2311-2322.   DOI
110 Bhandari DR, Seo KW, Roh KH, Jung JW, Kang SK, Kang KS. REX-1 expression and p38 MAPK activation status can determine proliferation/differentiation fates in human mesenchymal stem cells. PLoS One. 2010;5(5):e10493.   DOI
111 Shahsavari A, Weeratunga P, Ovchinnikov DA, Whitworth DJ. Pluripotency and immunomodulatory signatures of canine induced pluripotent stem cell-derived mesenchymal stromal cells are similar to harvested mesenchymal stromal cells. Sci Rep. 2021;11(1):3486.   DOI
112 Nantavisai S, Pisitkun T, Osathanon T, Pavasant P, Kalpravidh C, Dhitavat S, et al. Systems biology analysis of osteogenic differentiation behavior by canine mesenchymal stem cells derived from bone marrow and dental pulp. Sci Rep. 2020;10(1):20703.   DOI
113 Pierantozzi E, Gava B, Manini I, Roviello F, Marotta G, Chiavarelli M, et al. Pluripotency regulators in human mesenchymal stem cells: expression of NANOG but not of OCT-4 and SOX-2. Stem Cells Dev. 2011;20(5):915-923.   DOI