Different Sources of Bone Marrow Mesenchymal Stem Cells: A Comparison of Subchondral, Mandibular, and Tibia Bone-derived Mesenchymal Stem Cells
- Authors: Wang Y.1, Li H.1, Guan S.2, Yu S.1, Zhou Y.1, Zheng L.1, Zhang J.3
-
Affiliations:
- State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Sichuan University
- Department of Stomatology, Medical College, Dalian University, Dalian, Liaoning, Dalian University
- Yunnan Key Laboratory of Stomatology, Kunming Medical University School and Hospital of Stomatology, Kunming Medical University
- Issue: Vol 19, No 7 (2024)
- Pages: 1029-1041
- Section: Medicine
- URL: https://rjpbr.com/1574-888X/article/view/645891
- DOI: https://doi.org/10.2174/011574888X260686231023091127
- ID: 645891
Cite item
Full Text
Abstract
Background::Stem cell properties vary considerably based on the source and tissue site of mesenchymal stem cells (MSCs). The mandibular condyle is a unique kind of craniofacial bone with a special structure and a relatively high remodeling rate. MSCs here may also be unique to address specific physical needs.
Objective::The aim of this study was to compare the proliferation and multidirectional differentiation potential among MSCs derived from the tibia (TMSCs), mandibular ramus marrow (MMSCs), and condylar subchondral bone (SMSCs) of rats in vitro.
Methods::Cell proliferation and migration were assessed by CCK-8, laser confocal, and cell scratch assays. Histochemical staining and real-time PCR were used to evaluate the multidirectional differentiation potential and DNA methylation and histone deacetylation levels.
Results::The proliferation rate and self-renewal capacity of SMSCs were significantly higher than those of MMSCs and TMSCs. Moreover, SMSCs possessed significantly higher mineralization and osteogenic differentiation potential. Dnmt2, Dnmt3b, Hdac6, Hdac7, Hdac9, and Hdac10 may be instrumental in the osteogenesis of SMSCs. In addition, SMSCs are distinct from MMSCs and TMSCs with lower adipogenic differentiation and chondrogenic differentiation potential. The multidirectional differentiation capacities of TMSCs were exactly the opposite of those of SMSCs, and the results of MMSCs were intermediate.
Conclusion::This research offers a new paradigm in which SMSCs could be a useful source of stem cells for further application in stem cell-based medical therapies due to their strong cell renewal and osteogenic capacity.
About the authors
Yu Wang
State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Sichuan University
Email: info@benthamscience.net
Hong-Yu Li
State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Sichuan University
Email: info@benthamscience.net
Shu-Yuan Guan
Department of Stomatology, Medical College, Dalian University, Dalian, Liaoning, Dalian University
Email: info@benthamscience.net
Si-Han Yu
State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Sichuan University
Email: info@benthamscience.net
Ya-Chuan Zhou
State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Sichuan University
Email: info@benthamscience.net
Li-Wei Zheng
State Key Laboratory of Oral Diseases, National Clinical Research Center for Oral Diseases, West China Hospital of Stomatology, Sichuan University, Sichuan University
Author for correspondence.
Email: info@benthamscience.net
Jun Zhang
Yunnan Key Laboratory of Stomatology, Kunming Medical University School and Hospital of Stomatology, Kunming Medical University
Author for correspondence.
Email: info@benthamscience.net
References
- Brown C, McKee C, Bakshi S, et al. Mesenchymal stem cells: Cell therapy and regeneration potential. J Tissue Eng Regen Med 2019; 13(9): 1738-55. doi: 10.1002/term.2914 PMID: 31216380
- Galipeau J, Sensébé L. Mesenchymal stromal cells: Clinical challenges and therapeutic opportunities. Cell Stem Cell 2018; 22(6): 824-33. doi: 10.1016/j.stem.2018.05.004 PMID: 29859173
- Ding L, Zhou B, Hou Y, Xu L. Stem cells in tendon regeneration and factors governing tenogenesis. Curr Stem Cell Res Ther 2022; 17(6): 503-12. doi: 10.2174/1574888X17666220127111135 PMID: 35086458
- Rady D, Abbass MMS, El-Rashidy AA, et al. Mesenchymal stem/progenitor cells: The prospect of human clinical translation. Stem Cells Int 2020: 8837654.2020; doi: 10.1155/2020/8837654
- Adams MK, Goodrich LR, Rao S, et al. Equine bone marrow-derived mesenchymal stromal cells (BMDMSCs) from the ilium and sternum: Are there differences? Equine Vet J 2013; 45(3): 372-5. doi: 10.1111/j.2042-3306.2012.00646.x PMID: 23009322
- Anggita M, Nugroho WS, Fibrianto YH, Budhi S, Budipitojo T. Callus formation in fractured femur of rats treated with injection of human umbilical cord mesenchymal stem cell-conditioned medium. Vet Med Int 2021; 2021: 8410175. doi: 10.1155/2021/8410175
- Zhou W, Lin J, Zhao K, et al. Single-cell profiles and clinically useful properties of human mesenchymal stem cells of adipose and bone marrow origin. Am J Sports Med 2019; 47(7): 1722-33. doi: 10.1177/0363546519848678 PMID: 31100005
- Egusa H, Sonoyama W, Nishimura M, Atsuta I, Akiyama K. Stem cells in dentistry - Part I: Stem cell sources. J Prosthodont Res 2012; 56(3): 151-65. doi: 10.1016/j.jpor.2012.06.001 PMID: 22796367
- Bar JK, Lis-Nawara A, Grelewski PG. Dental pulp stem cell-derived secretome and its regenerative potential. Int J Mol Sci 2021; 22(21): 12018. doi: 10.3390/ijms222112018
- Ching H, Luddin N, Rahman I, Ponnuraj K. Expression of odontogenic and osteogenic markers in DPSCs and SHED: A review. Curr Stem Cell Res Ther 2016; 12(1): 71-9. doi: 10.2174/1574888X11666160815095733 PMID: 27527527
- Herrmann M, Hildebrand M, Menzel U, et al. Phenotypic characterization of bone marrow mononuclear cells and derived stromal cell populations from human iliac crest, vertebral body and femoral head. Int J Mol Sci 2019; 20(14): 3454. doi: 10.3390/ijms20143454
- Kadkhoda Z, Motie P, Rad MR, Mohaghegh S, Kouhestani F, Motamedian SR. Comparison of periodontal ligament stem cells with mesenchymal stem cells from other sources: A scoping systematic review of in-vitro and in-vivo studies. Curr Stem Cell Res Ther 2022; 17: 1574888X17666220429123319. doi: 10.2174/1574888X17666220429123319 PMID: 36397622
- Zhou Y, Hu X, Zheng X, et al. Differentiation potential of mesenchymal stem cells derived from adipose tissue vs bone marrow toward annulus fibrosus cells in vitro. Curr Stem Cell Res Ther 2017; 12(5): 432-9. doi: 10.2174/1574888X12666170214093955 PMID: 28201959
- Xu L, Liu Y, Sun Y, et al. Tissue source determines the differentiation potentials of mesenchymal stem cells: A comparative study of human mesenchymal stem cells from bone marrow and adipose tissue. Stem Cell Res Ther 2017; 8(1): 275. doi: 10.1186/s13287-017-0716-x
- Jain M, Minocha E, Tripathy NK, Singh N, Chaturvedi CP, Nityanand S. Comparison of the cardiomyogenic potency of human amniotic fluid and bone marrow mesenchymal stem cells. Int J Stem Cells 2019; 12(3): 449-56. doi: 10.15283/ijsc18087 PMID: 31658508
- Deluiz D, Delcroix GJ, D'Ippolito G, et al. Human bone marrow-derived mesenchymal stromal cell-seeded bone biomaterial directs fast and superior mandibular bone augmentation in rats. Sci Rep 2019; 9(1): 11806. doi: 10.1038/s41598-019-48236-8
- Yamaza T, Ren G, Akiyama K, Chen C, Shi Y, Shi S. Mouse mandible contains distinctive mesenchymal stem cells. J Dent Res 2011; 90(3): 317-24. doi: 10.1177/0022034510387796 PMID: 21076121
- Simon M, Major B, Vácz G, et al. The effects of hyperacute serum on the elements of the human subchondral bone marrow niche. Stem Cells Int 2018; 20108: 4854619. doi: 10.1155/2018/4854619
- Zhang H, Li ZL, Su XZ, Ding L, Li J, Zhu H. Subchondral bone derived mesenchymal stem cells display enhanced osteo-chondrogenic differentiation, self-renewal and proliferation potentials. Exp Animal 2018; 67(3): 349-59. doi: 10.1538/expanim.17-0137 PMID: 29515059
- Liao J, Huang Y, Wang Q, et al. Gene regulatory network from cranial neural crest cells to osteoblast differentiation and calvarial bone development. Cell Mol Life Sci 2022; 79(3): 158. doi: 10.1007/s00018-022-04208-2
- Berendsen AD, Olsen BR. Bone development. Bone 2015; 80: 14-8. doi: 10.1016/j.bone.2015.04.035 PMID: 26453494
- Li C, Wang F, Zhang R, Qiao P, Liu H. Comparison of proliferation and osteogenic differentiation potential of rat mandibular and femoral bone marrow mesenchymal stem cells in vitro. Stem Cells Dev 2020; 29(11): 728-36. doi: 10.1089/scd.2019.0256 PMID: 32122257
- Mao JJ, Giannobile WV, Helms JA, et al. Craniofacial tissue engineering by stem cells. J Dent Res 2006; 85(11): 966-79. doi: 10.1177/154405910608501101 PMID: 17062735
- Gomez M, Wittig O, Diaz-Solano D, Cardier JE. Mesenchymal stromal cell transplantation induces regeneration of large and full-thickness cartilage defect of the temporomandibular joint. Cartilage 2021; 13(1_suppl): 1814S-21S. doi: 10.1177/1947603520926711 PMID: 32493042
- Cardoneanu A, Macovei LA, Burlui AM, et al. Temporomandibular joint osteoarthritis: Pathogenic mechanisms involving the cartilage and subchondral bone, and potential therapeutic strategies for joint regeneration. Int J Mol Sci 2022; 24(1): 171. doi: 10.3390/ijms24010171
- Li B, Guan G, Mei L, Jiao K, Li H. Pathological mechanism of chondrocytes and the surrounding environment during osteoarthritis of temporomandibular joint. J Cell Mol Med 2021; 25(11): 4902-11. doi: 10.1111/jcmm.16514 PMID: 33949768
- Zhu S, Zhu J, Zhen G, et al. Subchondral bone osteoclasts induce sensory innervation and osteoarthritis pain. J Clin Invest 2019; 129(3): 1076-93. doi: 10.1172/JCI121561 PMID: 30530994
- Lin C, Liu L, Zeng C, et al. Activation of mTORC1 in subchondral bone preosteoblasts promotes osteoarthritis by stimulating bone sclerosis and secretion of CXCL12. Bone Res 2019; 7: 5. doi: 10.1038/s41413-018-0041-8
- Zhen G, Wen C, Jia X, et al. Inhibition of TGF-β signaling in mesenchymal stem cells of subchondral bone attenuates osteoarthritis. Nat Med 2013; 19(6): 704-12. doi: 10.1038/nm.3143 PMID: 23685840
- Crane JL, Cao X. Bone marrow mesenchymal stem cells and TGF-β signaling in bone remodeling. J Clin Invest 2014; 124(2): 466-72. doi: 10.1172/JCI70050 PMID: 24487640
- Zhao W, Wang T, Luo Q, et al. Cartilage degeneration and excessive subchondral bone formation in spontaneous osteoarthritis involves altered TGF-β signaling. J Orthop Res 2016; 34(5): 763-70. doi: 10.1002/jor.23079 PMID: 26496668
- Ganguly P, El-Jawhari JJ, Burska AN, Ponchel F, Giannoudis PV, Jones EA. The analysis of in vivo aging in human bone marrow mesenchymal stromal cells using colony-forming unit-fibroblast assay and the CD45lowCD271+ phenotype. Stem Cells Int 2019; 2019: 5197983. doi: 10.1155/2019/5197983
- Pajarinen J, Lin T, Gibon E, et al. Mesenchymal stem cell-macrophage crosstalk and bone healing. Biomaterials 2019; 196: 80-9. doi: 10.1016/j.biomaterials.2017.12.025 PMID: 29329642
- Mesure B, Menu P, Venkatesan JK, Cucchiarini M, Velot É. Biomaterials and gene therapy: A smart combination for MSC musculoskeletal engineering. Curr Stem Cell Res Ther 2019; 14(4): 337-43. doi: 10.2174/1574888X14666181205121658 PMID: 30516113
- Casado-Díaz A, Quesada-Gómez JM, Dorado G. Extracellular vesicles derived from mesenchymal stem cells (MSC) in regenerative medicine: Applications in skin wound healing. Front Bioeng Biotechnol 2020; 8: 146. doi: 10.3389/fbioe.2020.00146
- Leucht P, Kim JB, Amasha R, James AW, Girod S, Helms JA. Embryonic origin and Hox status determine progenitor cell fate during adult bone regeneration. Development 2008; 135(17): 2845-54. doi: 10.1242/dev.023788 PMID: 18653558
- Mauney JR, Volloch V, Kaplan DL. Role of adult mesenchymal stem cells in bone tissue engineering applications: Current status and future prospects. Tissue Eng 2005; 11(5-6): 787-802. doi: 10.1089/ten.2005.11.787 PMID: 15998219
- Parada C, Chai Y. Mandible and tongue development. Curr Top Dev Biol 2015; 115: 31-58. doi: 10.1016/bs.ctdb.2015.07.023 PMID: 26589920
- Isern J, García-García A, Martín AM, et al. The neural crest is a source of mesenchymal stem cells with specialized hematopoietic stem cell niche function. Elife 2014; 4: 03696. doi: 10.7554/eLife.03696
- Oh IH, Kwon KR. Concise review: Multiple niches for hematopoietic stem cell regulations. Stem Cells 2010; 28(7): 1243-9. doi: 10.1002/stem.453 PMID: 20517982
- Burja B, Barlič A, Erman A, et al. Human mesenchymal stromal cells from different tissues exhibit unique responses to different inflammatory stimuli. Curr Res Transl Med 2020; 68(4): 217-24. doi: 10.1016/j.retram.2020.05.006 PMID: 32843323
- Lee YH, Park HK, Auh QS, et al. Emerging potential of exosomes in regenerative medicine for temporomandibular joint osteoarthritis. Int J Mol Sci 2020; 21(4): 1541. doi: 10.3390/ijms21041541 PMID: 32102392
- Minervini G, Del Mondo D, Russo D, Cervino G, DAmico C, Fiorillo L. Stem cells in temporomandibular joint engineering: state of art and future persectives. J Craniofac Surg 2022; 33(7): 2181-7. doi: 10.1097/SCS.0000000000008771 PMID: 36201705
- Zhang S, Teo KYW, Chuah SJ, Lai RC, Lim SK, Toh WS. MSC exosomes alleviate temporomandibular joint osteoarthritis by attenuating inflammation and restoring matrix homeostasis. Biomaterials 2019; 200: 35-47. doi: 10.1016/j.biomaterials.2019.02.006 PMID: 30771585
- Tian Y, Chen J, Yan X, et al. Overloaded orthopedic force induces condylar subchondral bone absorption by stimulating rat mesenchymal stem cells differentiating into osteoclasts via mTOR-Regulated RANKL/OPG secretion in osteoblasts. Stem Cells Dev 2021; 30(1): 29-38. doi: 10.1089/scd.2020.0163 PMID: 33176606
- Uder C, Brückner S, Winkler S, Tautenhahn HM, Christ B. Mammalian MSC from selected species: Features and applications. Cytometry A 2018; 93(1): 32-49. doi: 10.1002/cyto.a.23239 PMID: 28906582
- Guo Y, Chi X, Wang Y, et al. Mitochondria transfer enhances proliferation, migration, and osteogenic differentiation of bone marrow mesenchymal stem cell and promotes bone defect healing. Stem Cell Res Ther 2020; 11(1): 245. doi: 10.1186/s13287-020-01704-9
- Patel DM, Shah J, Srivastava AS. Therapeutic potential of mesenchymal stem cells in regenerative medicine. Stem Cells Int 2013; 2013: 1-15. doi: 10.1155/2013/496218 PMID: 23577036
- Fitzsimmons REB, Mazurek MS, Soos A, Simmons CA. Mesenchymal stromal/stem cells in regenerative medicine and tissue engineering. Stem Cells Int 2018; 2018: 8031718. doi: 10.1155/2018/8031718
- Parekkadan B, Milwid JM. Mesenchymal stem cells as therapeutics. Annu Rev Biomed Eng 2010; 12(1): 87-117. doi: 10.1146/annurev-bioeng-070909-105309 PMID: 20415588
- Martinotti S, Ranzato E. Scratch wound healing assay. Methods Mol Biol 2019; 2109: 225-9. doi: 10.1007/7651_2019_259 PMID: 31414347
- Ullah M, Liu DD, Thakor AS. Mesenchymal stromal cell homing: Mechanisms and strategies for improvement. iScience 2019; 15: 421-38. doi: 10.1016/j.isci.2019.05.004 PMID: 31121468
- Li X, He L, Yue Q, et al. MiR-9-5p promotes MSC migration by activating β-catenin signaling pathway. Am J Physiol Cell Physiol 2017; 313(1): C80-93. doi: 10.1152/ajpcell.00232.2016 PMID: 28424168
- Lefebvre V, Angelozzi M, Haseeb A. SOX9 in cartilage development and disease. Curr Opin Cell Biol 2019; 61: 39-47. doi: 10.1016/j.ceb.2019.07.008 PMID: 31382142
- Nguyen JKB, Eames BF. Evolutionary repression of chondrogenic genes in the vertebrate osteoblast. FEBS J 2020; 287(20): 4354-61. doi: 10.1111/febs.15228 PMID: 31994313
- Ba R, Kong L, Wu G, et al. Increased expression of Sox9 during Balance of BMSCs/Chondrocyte Bricks in platelet-rich plasma promotes construction of a Stable 3-D chondrogenesis microenvironment for BMSCs. Stem Cells Int 2020; 2020: 5492059. doi: 10.1155/2020/5492059
- Wu X, Chen C, Han T, et al. Stat5a promotes Col10a1 gene expression during chondrocyte hypertrophic differentiation. Am J Transl Res 2023; 15(6): 4006-19.
- Fang H, Judd RL. Adiponectin regulation and function. Compr Physiol 2018; 8(3): 1031-63. doi: 10.1002/cphy.c170046
- Aprile M, Ambrosio MR, DEsposito V, et al. PPARG in human adipogenesis: Differential contribution of canonical transcripts and dominant negative isoforms. PPAR Res 2014; 2014: 1-11. doi: 10.1155/2014/537865 PMID: 24790595
- Chen Q, Shou P, Zheng C, et al. Fate decision of mesenchymal stem cells: Adipocytes or osteoblasts? Cell Death Differ 2016; 23(7): 1128-39. doi: 10.1038/cdd.2015.168 PMID: 26868907
- Almalki SG, Agrawal DK. Key transcription factors in the differentiation of mesenchymal stem cells. Differentiation 2016; 92(1-2): 41-51. doi: 10.1016/j.diff.2016.02.005 PMID: 27012163
- Willems NMBK, Langenbach GEJ, Everts V, Zentner A. The microstructural and biomechanical development of the condylar bone: A review. Eur J Orthod 2014; 36(4): 479-85. doi: 10.1093/ejo/cjt093 PMID: 24375755
- Zhao C, Gu Y, Wang Y, et al. miR-129-5p promotes osteogenic differentiation of BMSCs and bone regeneration via repressing Dkk3. Stem Cells Int 2021; 2021: 7435605. doi: 10.1155/2021/7435605
- Wang R, Wang Y, Zhu L, Liu Y, Li W. Epigenetic regulation in mesenchymal stem cell aging and differentiation and osteoporosis. Stem Cells Int 2020; 2020: 8836258. doi: 10.1155/2020/8836258
- Laker RC, Ryall JG. DNA methylation in skeletal muscle stem cell specification, proliferation, and differentiation. Stem Cells Int 2016; 2016: 1-9. doi: 10.1155/2016/5725927 PMID: 26880971
- Sun J, Yang J, Miao X, Loh HH, Pei D, Zheng H. Proteins in DNA methylation and their role in neural stem cell proliferation and differentiation. Cell Regen 2021; 10(1): 7. doi: 10.1186/s13619-020-00070-4
- Tuorto F, Herbst F, Alerasool N, et al. The TRNA methyltransferase Dnmt2 is required for accurate polypeptide synthesis during haematopoiesis. EMBO J 2015; 34(18): 2350-62. doi: 10.15252/embj.201591382 PMID: 26271101
- Ying J, Xu T, Wang C, et al. Dnmt3b ablation impairs fracture repair through upregulation of Notch pathway. JCI Insight 2020; 5(3): e131816. doi: 10.1172/jci.insight.131816
- Zhu XW, Zuo JL, Liu YH, et al. Osteogenesis of umbilical mesenchymal stem cells is enhanced in absence of DNA methyltransferase 3B (DNMT3B) through upregulating Runx2 expression. Eur Rev Med Pharmacol Sci 2014; 18(20): 3004-9. PMID: 25392095
- Ma C, Gao J, Liang J, et al. HDAC6 inactivates Runx2 promoter to block osteogenesis of bone marrow stromal cells in age-related bone loss of mice. Stem Cell Res Ther 2021; 12(1): 484. doi: 10.1186/s13287-021-02545-w
- Wang B, Gong S, Han L, et al. Knockdown of HDAC9 inhibits osteogenic differentiation of human bone marrow mesenchymal stem cells partially by suppressing the MAPK signaling pathway. Clin Interv Aging 2022; 17: 777-87. doi: 10.2147/CIA.S361008
- Lopa S, Colombini A, Moretti M, de Girolamo L. Injective mesenchymal stem cell-based treatments for knee osteoarthritis: From mechanisms of action to current clinical evidences. Knee Surg Sports Traumatol Arthrosc 2019; 27(6): 2003-20. doi: 10.1007/s00167-018-5118-9 PMID: 30159741
- Dupuis V, Oltra E. Methods to produce induced pluripotent stem cell-derived mesenchymal stem cells: Mesenchymal stem cells from induced pluripotent stem cells. World J Stem Cells 2021; 13(8): 1094-111. doi: 10.4252/wjsc.v13.i8.1094 PMID: 34567428
Supplementary files
