Human Adipose-derived Stem Cells Upregulate IGF-1 and Alleviate Osteoarthritis in a Two-stage Rabbit Osteoarthritis Model

  • Autores: Wang J.1, Su S.2, Dong C.3, Fan Q.4, Sun J.5, Liang S.6, Qin Z.2, Ma C.7, Jin J.8, Zhu H.9, Jiang T.10, Xu J.11
  • Afiliações:
    1. Key Laboratory of Brain Science Research & Transformation in Tropical Environment of Hainan Province, Hainan Medical University
    2. School of Basic Medicine and Life Sciences, Hainan Medical University
    3. Department of Anatomy, Medical College of Nantong University
    4. Orthopedics Department, Qingdao Jimo District People's Hospital
    5. Neurosurgery Department,, Qingdao Jimo District People's Hospital
    6. , Zhongke Comprehensive Medical Transformation Center Research Institute (Hainan) Co., Ltd
    7. The Second Clinical College,, Hainan Medical University
    8. Department of Biochemistry, School of Basic Medicine and Life Sciences,, Hainan Medical University
    9. Orthopedics Department, Tianjin Hospital
    10. Engineering Research Center for Hainan Bio-Smart Materials and Bio-Medical Devices, Key Laboratory of Emergency and Trauma, Ministry of Education, Key Laboratory of Hainan Functional Materials and Molecular Imaging, College of Emergency and Trauma,, Hainan Medical University
    11. Stem Cell Center, Shanghai East Hospital, School of Medicine, Tongji University
  • Edição: Volume 19, Nº 11 (2024)
  • Páginas: 1472-1483
  • Seção: Medicine
  • URL: https://gynecology.orscience.ru/1574-888X/article/view/645589
  • DOI: https://doi.org/10.2174/011574888X274359231122064109
  • ID: 645589

Citar

Texto integral

Resumo

Objective:In recent times, it has been recognized that mesenchymal stem cells (MSCs) possess the capability to address osteoarthritis (OA). The objective of this research was to examine the impact of injecting human adipose-derived stem cells (hADSCs) into a novel rabbit osteoarthritis model with dual damage.

Methods:The OA model was established surgically first by medial collateral ligament and anterior cruciate ligament transection and medial meniscectomy, then by articular cartilage full-thickness defect. Enhanced Green Fluorescence Protein expressing lentivirus FG12 was used to label hADSCs, which were then injected into the knee joints. Every single rabbit was sacrificed after 4 and 8 weeks following the surgical procedure. Macroscopic examination, immunohistochemistry staining, magnetic resonance imaging, qRT-PCR, and ELISA analysis were utilized for the assessments.

Results:After 4 and 8 weeks, the injection of hADSCs resulted in reduced cartilage loss, minimal fissures and cracks, and a decrease in the volume of joint effusion and cartilage defect as measured by MRI. Moreover, the application of ELISA and qRT-PCR techniques revealed that the administration of hADSCs resulted in an elevation in the IGF-1 concentration.

Conclusions:Based on our findings, it can be inferred that the transplantation of hADSCs facilitates the healing of articular cartilage in the osteoarthritis model of rabbits with double damage. The upregulated IGF-1 may play a crucial part in the process of cartilage repair using hADSCs. The use of hADSC transplantation could potentially be appropriate for clinical implementation in managing osteoarthritis.

Sobre autores

Juan Wang

Key Laboratory of Brain Science Research & Transformation in Tropical Environment of Hainan Province, Hainan Medical University

Autor responsável pela correspondência
Email: info@benthamscience.net

Shibo Su

School of Basic Medicine and Life Sciences, Hainan Medical University

Email: info@benthamscience.net

Chuanming Dong

Department of Anatomy, Medical College of Nantong University

Email: info@benthamscience.net

Qiang Fan

Orthopedics Department, Qingdao Jimo District People's Hospital

Email: info@benthamscience.net

Jishu Sun

Neurosurgery Department,, Qingdao Jimo District People's Hospital

Email: info@benthamscience.net

Siqiang Liang

, Zhongke Comprehensive Medical Transformation Center Research Institute (Hainan) Co., Ltd

Email: info@benthamscience.net

Zuhuo Qin

School of Basic Medicine and Life Sciences, Hainan Medical University

Email: info@benthamscience.net

Chuqing Ma

The Second Clinical College,, Hainan Medical University

Email: info@benthamscience.net

Jianfeng Jin

Department of Biochemistry, School of Basic Medicine and Life Sciences,, Hainan Medical University

Email: info@benthamscience.net

Hongwen Zhu

Orthopedics Department, Tianjin Hospital

Autor responsável pela correspondência
Email: info@benthamscience.net

Tongmeng Jiang

Engineering Research Center for Hainan Bio-Smart Materials and Bio-Medical Devices, Key Laboratory of Emergency and Trauma, Ministry of Education, Key Laboratory of Hainan Functional Materials and Molecular Imaging, College of Emergency and Trauma,, Hainan Medical University

Autor responsável pela correspondência
Email: info@benthamscience.net

Jun Xu

Stem Cell Center, Shanghai East Hospital, School of Medicine, Tongji University

Autor responsável pela correspondência
Email: info@benthamscience.net

Bibliografia

  1. Wakale, S.; Wu, X.; Sonar, Y.; Sun, A.; Fan, X.; Crawford, R.; Prasadam, I. How are aging and osteoarthritis related? Aging Dis., 2023, 14(3), 592-604. doi: 10.14336/AD.2022.0831 PMID: 37191424
  2. Goldring, M.B.; Goldring, S.R. Articular cartilage and subchondral bone in the pathogenesis of osteoarthritis. Ann. N. Y. Acad. Sci., 2010, 1192(1), 230-237. doi: 10.1111/j.1749-6632.2009.05240.x PMID: 20392241
  3. Altman, R.D.; Barthel, H.R. Topical therapies for osteoarthritis. Drugs, 2011, 71(10), 1259-1279. doi: 10.2165/11592550-000000000-00000 PMID: 21770475
  4. Sostres, C.; Gargallo, C.J.; Arroyo, M.T.; Lanas, A. Adverse effects of non-steroidal anti-inflammatory drugs (NSAIDs, aspirin and coxibs) on upper gastrointestinal tract. Best Pract. Res. Clin. Gastroenterol., 2010, 24(2), 121-132. doi: 10.1016/j.bpg.2009.11.005 PMID: 20227026
  5. Liu, G.; Zhou, Y.; Zhang, X.; Guo, S. Advances in hydrogels for stem cell therapy: Regulation mechanisms and tissue engineering applications. J. Mater. Chem. B Mater. Biol. Med., 2022, 10(29), 5520-5536. doi: 10.1039/D2TB01044E PMID: 35819152
  6. Blum, B.; Benvenisty, N. The tumorigenicity of human embryonic stem cells. Adv. Cancer Res., 2008, 100, 133-158. doi: 10.1016/S0065-230X(08)00005-5 PMID: 18620095
  7. Caplan, A.I. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J. Cell. Physiol., 2007, 213(2), 341-347. doi: 10.1002/jcp.21200 PMID: 17620285
  8. Li, Q.; Li, B.; Ye, T.; Xu, W.; Yin, H.; Deng, Z.; Li, H.; Yan, X.; Hao, X.; Li, L.; Tao, Z.; Liu, B.; Chen, Z.; Luo, L.; Qian, H.; Fu, Q.L.; Wang, Q.; Zheng, L.; Wang, Y. Requirements for human mesenchymal stem cell-derived small extracellular vesicles. Interdiscipl Med, 2023, 1(1), e20220015. doi: 10.1002/INMD.20220015
  9. Jiang, T.; Kai, D.; Liu, S.; Huang, X.; Heng, S.; Zhao, J.; Chan, B.Q.Y.; Loh, X.J.; Zhu, Y.; Mao, C.; Zheng, L. Mechanically cartilage-mimicking poly(PCL-PTHF urethane)/collagen nanofibers induce chondrogenesis by blocking NF–kappa B signaling pathway. Biomaterials, 2018, 178, 281-292. doi: 10.1016/j.biomaterials.2018.06.023 PMID: 29945065
  10. Solá, V.M.; Aguilar, J.J.; Farías, A.; Vazquez Mosquera, A.P.; Peralta López, M.E.; Carpentieri, A.R. Melatonin protects gingival mesenchymal stem cells and promotes differentiation into osteoblasts. Cell Biochem. Funct., 2022, 40(6), 636-646. doi: 10.1002/cbf.3733 PMID: 35848411
  11. Jin, P.; Liu, L.; Cheng, L.; Chen, X.; Xi, S.; Jiang, T. Calcium-to-phosphorus releasing ratio affects osteoinductivity and osteoconductivity of calcium phosphate bioceramics in bone tissue engineering. Biomed. Eng. Online, 2023, 22(1), 12. doi: 10.1186/s12938-023-01067-1 PMID: 36759894
  12. Jiang, T.M. Identification of the genetic central dogma in osteogenic differentiation of MSCs by osteoinductive medium from transcriptional data sets. Chronic Dis. Transl. Med., 2022, 8(3), 218-228. doi: 10.1002/cdt3.26 PMID: 36161200
  13. 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(5), 1294-1301. doi: 10.1634/stemcells.2005-0342 PMID: 16410387
  14. Zuk, P.A.; Zhu, M.; Mizuno, H.; Huang, J.; Futrell, J.W.; Katz, A.J.; Benhaim, P.; Lorenz, H.P.; Hedrick, M.H. Multilineage cells from human adipose tissue: Implications for cell-based therapies. Tissue Eng., 2001, 7(2), 211-228. doi: 10.1089/107632701300062859 PMID: 11304456
  15. Qin, Y.; Ge, G.; Yang, P.; Wang, L.; Qiao, Y.; Pan, G.; Yang, H.; Bai, J.; Cui, W.; Geng, D. An update on adipose-derived stem cells for regenerative medicine: Where challenge meets opportunity. Adv. Sci., 2023, 10(20), 2207334. doi: 10.1002/advs.202207334 PMID: 37162248
  16. Rochette, L.; Mazini, L.; Malka, G.; Zeller, M.; Cottin, Y.; Vergely, C. The crosstalk of Adipose-Derived Stem Cells (ADSC), oxidative stress, and inflammation in protective and adaptive responses. Int. J. Mol. Sci., 2020, 21(23), 9262. doi: 10.3390/ijms21239262 PMID: 33291664
  17. Liu, J.P.; Baker, J.; Perkins, A.S.; Robertson, E.J.; Efstratiadis, A. Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r). Cell, 1993, 75(1), 59-72. doi: 10.1016/S0092-8674(05)80084-4 PMID: 8402901
  18. Goodrich, L.R.; Brower-Toland, B.D.; Warnick, L.; Robbins, P.D.; Evans, C.H.; Nixon, A.J. Direct adenovirus-mediated IGF-I gene transduction of synovium induces persisting synovial fluid IGF-I ligand elevations. Gene Ther., 2006, 13(17), 1253-1262. doi: 10.1038/sj.gt.3302757 PMID: 16708081
  19. Katz, A.J.; Tholpady, A.; Tholpady, S.S.; Shang, H.; Ogle, R.C. Cell surface and transcriptional characterization of human adipose-derived adherent stromal (hADAS) cells. Stem Cells, 2005, 23(3), 412-423. doi: 10.1634/stemcells.2004-0021 PMID: 15749936
  20. Gutiérrez-Fernández, M.; Rodríguez-Frutos, B.; Ramos-Cejudo, J.; Teresa Vallejo-Cremades, M.; Fuentes, B.; Cerdán, S.; Díez-Tejedor, E. Effects of intravenous administration of allogenic bone marrow- and adipose tissue-derived mesenchymal stem cells on functional recovery and brain repair markers in experimental ischemic stroke. Stem Cell Res. Ther., 2013, 4(1), 11. doi: 10.1186/scrt159 PMID: 23356495
  21. Mitchell, J.B.; McIntosh, K.; Zvonic, S.; Garrett, S.; Floyd, Z.E.; Kloster, A.; Di Halvorsen, Y.; Storms, R.W.; Goh, B.; Kilroy, G.; Wu, X.; Gimble, J.M. Immunophenotype of human adipose-derived cells: Temporal changes in stromal-associated and stem cell-associated markers. Stem Cells, 2006, 24(2), 376-385. doi: 10.1634/stemcells.2005-0234 PMID: 16322640
  22. Gao, S.; Zhao, P.; Lin, C.; Sun, Y.; Wang, Y.; Zhou, Z.; Yang, D.; Wang, X.; Xu, H.; Zhou, F.; Cao, L.; Zhou, W.; Ning, K.; Chen, X.; Xu, J. Differentiation of human adipose-derived stem cells into neuron-like cells which are compatible with photocurable three-dimensional scaffolds. Tissue Eng. Part A, 2014, 20(7-8), 1271-1284. doi: 10.1089/ten.tea.2012.0773 PMID: 24251600
  23. Martin, J. T.; Collins, C. M.; Ikuta, K.; Mauck, R. L.; Elliott, D. M.; Zhang, Y.; Anderson, D. G.; Vaccaro, A. R.; Albert, T. J.; Arlet, V.; Smith, H. E. Population average T2 MRI maps reveal quantitative regional transformations in the degenerating rabbit intervertebral disc that vary by lumbar level. J Orthop Res, 2015, 33(1), 140-8.
  24. Riester, S.M.; Denbeigh, J.M.; Lin, Y.; Jones, D.L.; de Mooij, T.; Lewallen, E.A.; Nie, H.; Paradise, C.R.; Radel, D.J.; Dudakovic, A.; Camilleri, E.T.; Larson, D.R.; Qu, W.; Krych, A.J.; Frick, M.A. Safety studies for use of adipose tissue-derived mesenchymal stromal/stem cells in a rabbit model for osteoarthritis to support a phase I clinical trial. Stem Cells Trans Med, 2016, 2016, 0097. doi: 10.5966/sctm.2016-0097
  25. Wang, W.; He, N.; Feng, C.; Liu, V.; Zhang, L.; Wang, F.; He, J.; Zhu, T.; Wang, S.; Qiao, W.; Li, S.; Zhou, G.; Zhang, L.; Dai, C.; Cao, W. Human adipose-derived mesenchymal progenitor cells engraft into rabbit articular cartilage. Int. J. Mol. Sci., 2015, 16(12), 12076-12091. doi: 10.3390/ijms160612076 PMID: 26023716
  26. Mwale, F.; Rampersad, S.; Richard, H.; Guoying, Y.; Al Rowas, S.; Madiraju, P.; Antoniou, J.; Laverty, S. The constitutive expression of type x collagen in mesenchymal stem cells from osteoarthritis patients is reproduced in a rabbit model of osteoarthritis. J. Tissue Eng., 2011, 2011, 587547. doi: 10.4061/2011/587547 PMID: 21808721
  27. Desando, G.; Cavallo, C.; Sartoni, F.; Martini, L.; Parrilli, A.; Veronesi, F.; Fini, M.; Giardino, R.; Facchini, A.; Grigolo, B. Intra-articular delivery of adipose derived stromal cells attenuates osteoarthritis progression in an experimental rabbit model. Arthritis Res. Ther., 2013, 15(1), R22. doi: 10.1186/ar4156 PMID: 23360790
  28. Grigolo, B.; Lisignoli, G.; Desando, G.; Cavallo, C.; Marconi, E.; Tschon, M.; Giavaresi, G.; Fini, M.; Giardino, R.; Facchini, A. Osteoarthritis treated with mesenchymal stem cells on hyaluronan-based scaffold in rabbit. Tissue Eng. Part C Methods, 2009, 15(4), 647-658. doi: 10.1089/ten.tec.2008.0569 PMID: 19249964
  29. Mehrabani, D.; Babazadeh, M.; Tanideh, N.; Zare, S.; Hoseinzadeh, S.; Torabinejad, S.; Koohi-Hosseinabadi, O. The healing effect of adipose-derived mesenchymal stem cells in full-thickness femoral articular cartilage defects of rabbit. Int. J. Organ Transplant. Med., 2015, 6(4), 165-175. PMID: 26576262
  30. Toghraie, F.S.; Chenari, N.; Gholipour, M.A.; Faghih, Z.; Torabinejad, S.; Dehghani, S.; Ghaderi, A. Treatment of osteoarthritis with infrapatellar fat pad derived mesenchymal stem cells in Rabbit. Knee, 2011, 18(2), 71-75. doi: 10.1016/j.knee.2010.03.001 PMID: 20591677
  31. Ude CC, Shamsul BS, Ng MH , Chen HC, Ohnmar Htwe, Amaramalar SN, Rizal AR, Johan A, Norhamdan MY, Azizi M, Aminuddin BS, Ruszymah BHI. Long-term evaluation of osteoarthritis sheep knee, treated with TGF-β3 and BMP-6 induced multipotent stem cells. Exp Gerontol 2018; 104: 43-51. doi: 10.1016/j.exger.2018.01.020 PMID: 29421350
  32. Liang, X.; Ding, Y.; Zhang, Y.; Tse, H.F.; Lian, Q. Paracrine mechanisms of mesenchymal stem cell-based therapy: Current status and perspectives. Cell Transplant., 2014, 23(9), 1045-1059. doi: 10.3727/096368913X667709 PMID: 23676629
  33. Peshkova, M.; Korneev, A.; Suleimanov, S.; Vlasova, I.I.; Svistunov, A.; Kosheleva, N.; Timashev, P. MSCs’ conditioned media cytokine and growth factor profiles and their impact on macrophage polarization. Stem Cell Res. Ther., 2023, 14(1), 142. doi: 10.1186/s13287-023-03381-w PMID: 37231519
  34. Wu, H.; Peng, Z.; Xu, Y.; Sheng, Z.; Liu, Y.; Liao, Y.; Wang, Y.; Wen, Y.; Yi, J.; Xie, C.; Chen, X.; Hu, J.; Yan, B.; Wang, H.; Yao, X.; Fu, W.; Ouyang, H. Engineered adipose-derived stem cells with IGF-1-modified mRNA ameliorates osteoarthritis development. Stem Cell Res. Ther., 2022, 13(1), 19. doi: 10.1186/s13287-021-02695-x PMID: 35033199

Arquivos suplementares

Arquivos suplementares
Ação
1. JATS XML

Declaração de direitos autorais © Bentham Science Publishers, 2024