J Korean Assoc Oral Maxillofac Surg.  2021 Apr;47(2):65-75. 10.5125/jkaoms.2021.47.2.65.

Mesenchymal stem cells in the treatment of osteonecrosis of the jaw

Affiliations
  • 1Department of Oncology and Hematology, VSHA Fondation , Passy, French.
  • 2Santé Dorée Dental Clinic, Paris, French.
  • 3Smart Dental Clinic, Milan, Italy.

Abstract

Medication-related osteonecrosis of the jaw (MRONJ) has recently associated to the increase in antiresorptive and anti-angiogenic drugs prescriptions in the treatment of oncologic and osteoporotic patients. The physiopathogenesis of MRONJ remains unclear and available treatments are unsatisfactory. Newer pharmacological treatments have shown good results, but are not curative and could have major side effects. At the same time as pharmacological treatments, mesenchymal stem cells (MSCs) have emerged as a promising therapeutic modality for tissue regeneration and repair. MSCs are multipotential non-hematopoietic progenitor cells capable to differentiating into multiple lineages of the mesenchyme. Bone marrow MSCs can differentiate into osteogenic cells and display immunological properties and secrete paracrine anti-inflammatory factors in damaged tissues. The immunomodulatory, reparative, and anti-inflammatory properties of bone marrow MSCs have been tested in a variety of animal models of MRONJ and applied in specific clinical settings. The aim of this review is to discuss critically the immunogenicity and immunomodulatory properties of MSCs, both in vitro and in vivo, the possible underlying mechanisms of their effects, and their potential clinical use as modulators of immune responses in MRONJ, and to identify clinical safety and recommendations for future research.

Keyword

Osteonecrosis; Bone regeneration; Mesenchymal stem cell; Cell therapy

Reference

References

1. Marx RE. 2003; Pamidronate (Aredia) and zoledronate (Zometa) induced avascular necrosis of the jaws: a growing epidemic. J Oral Maxillofac Surg. 61:1115–7. https://doi.org/10.1016/s0278-2391(03)00720-1 . DOI: 10.1016/s0278-2391(03)00720-1. PMID: 12966493.
Article
2. Ruggiero SL, Dodson TB, Fantasia J, Goodday R, Aghaloo T, Mehrotra B, et al. 2014; ; American Association of Oral and Maxillofacial Surgeons. American Association of Oral and Maxillofacial Surgeons position paper on medication-related osteonecrosis of the jaw--2014 update. J Oral Maxillofac Surg. 72:1938–56. https://doi.org/10.1016/j.joms.2014.04.031 . DOI: 10.1016/j.joms.2014.04.031. PMID: 25234529.
Article
3. Rollason V, Laverrière A, MacDonald LC, Walsh T, Tramèr MR, Vogt-Ferrier NB. 2016; Interventions for treating bisphosphonate-related osteonecrosis of the jaw (BRONJ). Cochrane Database Syst Rev. 2:CD008455. https://doi.org/10.1002/14651858.CD008455.pub2c. DOI: 10.1002/14651858.CD008455.pub2. PMID: 26919630. PMCID: PMC7173706.
Article
4. Lombard T, Neirinckx V, Rogister B, Gilon Y, Wislet S. 2016; Medication-related osteonecrosis of the jaw: new insights into molecular mechanisms and cellular therapeutic approaches. Stem Cells Int. 2016:8768162. https://doi.org/10.1155/2016/8768162 . DOI: 10.1155/2016/8768162. PMID: 27721837. PMCID: PMC5046039.
Article
5. Fortunato L, Bennardo F, Buffone C, Giudice A. 2020; Is the application of platelet concentrates effective in the prevention and treatment of medication-related osteonecrosis of the jaw? A systematic review. J Craniomaxillofac Surg. 48:268–85. https://doi.org/10.1016/j.jcms.2020.01.014 . DOI: 10.1016/j.jcms.2020.01.014. PMID: 32063481.
Article
6. Bernardo ME, Locatelli F, Fibbe WE. 2009; Mesenchymal stromal cells. Ann N Y Acad Sci. 1176:101–17. https://doi.org/10.1111/j.1749-6632.2009.04607.x . DOI: 10.1111/nyas.13102. PMID: 27270495.
Article
7. Nauta AJ, Fibbe WE. 2007; Immunomodulatory properties of mesenchymal stromal cells. Blood. 110:3499–506. https://doi.org/10.1182/blood-2007-02-069716 . DOI: 10.2174/1574888X14666181205115452. PMID: 30516112.
Article
8. Gangji V, Hauzeur JP. 2009; Cellular-based therapy for osteonecrosis. Orthop Clin North Am. 40:213–21. https://doi.org/10.1016/j.ocl.2008.10.009 . DOI: 10.1016/j.ocl.2008.10.009. PMID: 19358906.
Article
9. Quarto R, Mastrogiacomo M, Cancedda R, Kutepov SM, Mukhachev V, Lavroukov A, et al. 2001; Repair of large bone defects with the use of autologous bone marrow stromal cells. N Engl J Med. 344:385–6. https://doi.org/10.1056/NEJM200102013440516 . DOI: 10.1056/NEJM200102013440516. PMID: 11195802.
Article
10. Gangji V, Hauzeur JP, Matos C, De Maertelaer V, Toungouz M, Lambermont M. 2004; Treatment of osteonecrosis of the femoral head with implantation of autologous bone-marrow cells. A pilot study. J Bone Joint Surg Am. 86:1153–60. https://doi.org/10.2106/00004623-200406000-00006 . DOI: 10.2106/00004623-200406000-00006. PMID: 15173287.
Article
11. Kikuiri T, Kim I, Yamaza T, Akiyama K, Zhang Q, Li Y, et al. 2010; Cell-based immunotherapy with mesenchymal stem cells cures bisphosphonate-related osteonecrosis of the jaw-like disease in mice. J Bone Miner Res. 25:1668–79. https://doi.org/10.1002/jbmr.37 . DOI: 10.1002/jbmr.37. PMID: 20200952. PMCID: PMC3154005.
Article
12. Li Y, Xu J, Mao L, Liu Y, Gao R, Zheng Z, et al. 2013; Allogeneic mesenchymal stem cell therapy for bisphosphonate-related jaw osteonecrosis in Swine. Stem Cells Dev. 22:2047–56. https://doi.org/10.1089/scd.2012.0615 . DOI: 10.1089/scd.2012.0615. PMID: 23461552. PMCID: PMC3699896.
Article
13. Tatsumi K, Ohashi K, Matsubara Y, Kohori A, Ohno T, Kakidachi H, et al. 2013; Tissue factor triggers procoagulation in transplanted mesenchymal stem cells leading to thromboembolism. Biochem Biophys Res Commun. 431:203–9. https://doi.org/10.1016/j.bbrc.2012.12.134 . DOI: 10.1016/j.bbrc.2012.12.134. PMID: 23313481.
Article
14. Breitbach M, Bostani T, Roell W, Xia Y, Dewald O, Nygren JM, et al. 2007; Potential risks of bone marrow cell transplantation into infarcted hearts. Blood. 110:1362–9. https://doi.org/10.1182/blood-2006-12-063412 . DOI: 10.1182/blood-2006-12-063412. PMID: 17483296.
Article
15. Kaibuchi N, Iwata T, Yamato M, Okano T, Ando T. 2016; Multipotent mesenchymal stromal cell sheet therapy for bisphosphonate-related osteonecrosis of the jaw in a rat model. Acta Biomater. 42:400–10. https://doi.org/10.1016/j.actbio.2016.06.022 . DOI: 10.1016/j.actbio.2016.06.022. PMID: 27326918.
Article
16. Matsuura Y, Atsuta I, Ayukawa Y, Yamaza T, Kondo R, Takahashi A, et al. 2016; Therapeutic interactions between mesenchymal stem cells for healing medication-related osteonecrosis of the jaw. Stem Cell Res Ther. 7:119. https://doi.org/10.1186/s13287-016-0367-3 . DOI: 10.1186/s13287-016-0367-3. PMID: 27530108. PMCID: PMC4988021.
Article
17. Ogata K, Katagiri W, Hibi H. 2017; Secretomes from mesenchymal stem cells participate in the regulation of osteoclastogenesis in vitro. Clin Oral Investig. 21:1979–88. https://doi.org/10.1007/s00784-016-1986-x . DOI: 10.1007/s00784-016-1986-x. PMID: 27796573.
Article
18. Ogata K, Matsumura M, Moriyama M, Katagiri W, Hibi H, Nakamura S. 2017; Cytokine mixtures mimicking secretomes from mesenchymal stem cells improve medication-related osteonecrosis of the jaw in a rat model. JBMR Plus. 2:69–80. https://doi.org/10.1002/jbm4.10013 . DOI: 10.1002/jbm4.10013. PMID: 30283893. PMCID: PMC6124208.
Article
19. Barba-Recreo P, Georgiev-Hristov T, Ruiz Bravo-Burguillos E, Abarrategi A, Burgueño M, et al. Del Castillo Pardo de Vera JL. 2015; Adipose-derived stem cells and platelet-rich plasma for preventive treatment of bisphosphonate-related osteonecrosis of the jaw in a murine model. J Craniomaxillofac Surg. 43:1161–8. https://doi.org/10.1016/j.jcms.2015.04.026 . DOI: 10.1016/j.jcms.2015.04.026. PMID: 26027865.
Article
20. Kuroshima S, Sasaki M, Nakajima K, Tamaki S, Hayano H, Sawase T. 2018; Transplantation of noncultured stromal vascular fraction cells of adipose tissue ameliorates osteonecrosis of the jaw-like lesions in mice. J Bone Miner Res. 33:154–66. https://doi.org/10.1002/jbmr.3292 . DOI: 10.1002/jbmr.3292. PMID: 28902422.
Article
21. Alonso-Rodriguez E, González-Martín-Moro J, Cebrián-Carretero JL, Del Castillo JL, Pozo-Kreilinger JJ, Ruiz-Bravo E, et al. 2019; Bisphosphonate-related osteonecrosis. Application of adipose-derived stem cells in an experimental murine model. Med Oral Patol Oral Cir Bucal. 24:e529–36. https://doi.org/10.4317/medoral.22959 . DOI: 10.4317/medoral.22959. PMID: 31232388. PMCID: PMC6667013.
Article
22. Zang X, He L, Zhao L, He Y, Xiao E, Zhang Y. 2019; Adipose-derived stem cells prevent the onset of bisphosphonate-related osteonecrosis of the jaw through transforming growth factor β-1-mediated gingival wound healing. Stem Cell Res Ther. 10:169. https://doi.org/10.1186/s13287-019-1277-y . DOI: 10.1186/s13287-019-1277-y. PMID: 31196208. PMCID: PMC6567445.
Article
23. Gao SY, Lin RB, Huang SH, Liang YJ, Li X, Zhang SE, et al. 2021; PDGF-BB exhibited therapeutic effects on rat model of bisphosphonate-related osteonecrosis of the jaw by enhancing angiogenesis and osteogenesis. Bone. 144:115117. https://doi.org/10.1016/j.bone.2019.115117 . DOI: 10.1016/j.bone.2019.115117. PMID: 31676407.
Article
24. Watanabe J, Sakai K, Urata Y, Toyama N, Nakamichi E, Hibi H. 2020; Extracellular vesicles of stem cells to prevent BRONJ. J Dent Res. 99:552–60. https://doi.org/10.1177/0022034520906793 . DOI: 10.1177/0022034520906793. PMID: 32119600.
Article
25. Elad S, Czerninski R, Avgil M, Or R. 2005; Hematopoietic stem cells and bisphosphonate-related osteonecrosis of the jaw. Support Care Cancer. 13:455. https://doi.org/10.1111/odi.12056 . DOI: 10.1111/odi.12056,. PMID: 23279619.
Article
26. Matsubara T, Suardita K, Ishii M, Sugiyama M, Igarashi A, Oda R, et al. 2005; Alveolar bone marrow as a cell source for regenerative medicine: differences between alveolar and iliac bone marrow stromal cells. J Bone Miner Res. 20:399–409. https://doi.org/10.1359/JBMR.041117 . DOI: 10.1359/JBMR.041117. PMID: 15746984.
Article
27. Cella L, Oppici A, Arbasi M, Moretto M, Piepoli M, Vallisa D, et al. 2011; Autologous bone marrow stem cell intralesional transplantation repairing bisphosphonate related osteonecrosis of the jaw. Head Face Med. 7:16. https://doi.org/10.1186/1746-160X-7-16 . DOI: 10.1186/1746-160X-7-16. PMID: 21849044. PMCID: PMC3175443.
Article
28. He LH, Xiao E, An JG, He Y, Chen S, Zhao L, et al. 2017; Role of bone marrow stromal cells in impaired bone repair from BRONJ osseous lesions. J Dent Res. 96:539–46. https://doi.org/10.1177/0022034517691507 . DOI: 10.1177/0022034517691507. PMID: 28199140.
Article
29. Voss PJ, Matsumoto A, Alvarado E, Schmelzeisen R, Duttenhöfer F, Poxleitner P. 2017; Treatment of stage II medication-related osteonecrosis of the jaw with necrosectomy and autologous bone marrow mesenchymal stem cells. Odontology. 105:484–93. https://doi.org/10.1007/s10266-017-0295-4 . DOI: 10.1007/s10266-018-00409-z. PMID: 30721386.
Article
30. De Santis GC, de Macedo LD, Orellana MD, Innocentini LMAR, Ferrari TC, Ricz HMA, et al. 2020; Mesenchymal stromal cells administration for osteonecrosis of the jaw caused by bisphosphonate: report of two cases. Acta Oncol. 59:789–92. https://doi.org/10.1080/0284186X.2020.1730004 . DOI: 10.1080/0284186X.2020.1730004. PMID: 32079438.
Article
31. Bouland C, Meuleman N, Widelec J, Keiani-Mothlagh K, Voisin C, Lagneaux L, et al. 2020; Case reports of medication-related osteonecrosis of the jaw (MRONJ) treated with uncultured stromal vascular fraction and L-PRF. J Stomatol Oral Maxillofac Surg. https://doi.org/10.1016/j.jormas.2020.05.024 [Epub ahead of print]. DOI: 10.1016/j.jormas.2020.05.024. PMID: 32540361.
Article
32. Caplan AI, Bruder SP. 2001; Mesenchymal stem cells: building blocks for molecular medicine in the 21st century. Trends Mol Med. 7:259–64. https://doi.org/10.1016/s1471-4914(01)02016-0 . DOI: 10.1016/s1471-4914(01)02016-0. PMID: 11378515.
Article
33. Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, et al. 2001; Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 7:211–28. https://doi.org/10.1089/107632701300062859 . DOI: 10.1089/107632701300062859. PMID: 11304456.
Article
34. Robey PG. 2011; Cell sources for bone regeneration: the good, the bad, and the ugly (but promising). Tissue Eng Part B Rev. 17:423–30. https://doi.org/10.1089/ten.teb.2011.0199 . DOI: 10.1089/ten.teb.2011.0199. PMID: 21797663. PMCID: PMC3223013.
Article
35. Lotfy A, El-Sherbiny YM, Cuthbert R, Jones E, Badawy A. 2019; Comparative study of biological characteristics of mesenchymal stem cells isolated from mouse bone marrow and peripheral blood. Biomed Rep. 11:165–70. https://doi.org/10.3892/br.2019.1236 . DOI: 10.3892/br.2019.1236. PMID: 31565222. PMCID: PMC6760463.
Article
36. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, et al. 2006; Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 8:315–7. https://doi.org/10.1080/14653240600855905 . DOI: 10.1080/14653240600855905. PMID: 16923606.
Article
37. Buhring HJ, Battula VL, Treml S, Kanz L, Vogel W. 2006; Novel markers for the isolation of primary bone marrow derived MSC with multi-lineage differentiation capacity. Blood. 108:2573. https://doi.org/10.1182/blood.V108.11.2573.2573 . DOI: 10.1182/blood.V108.11.2573.2573.
Article
38. Im GI, Shin YW, Lee KB. 2005; Do adipose tissue-derived mesenchymal stem cells have the same osteogenic and chondrogenic potential as bone marrow-derived cells? Osteoarthritis Cartilage. 13:845–53. https://doi.org/10.1016/j.joca.2005.05.005 . DOI: 10.1016/j.joca.2005.05.005. PMID: 16129630.
Article
39. Traktuev DO, Merfeld-Clauss S, Li J, Kolonin M, Arap W, Pasqualini R, et al. 2008; A population of multipotent CD34-positive adipose stromal cells share pericyte and mesenchymal surface markers, reside in a periendothelial location, and stabilize endothelial networks. Circ Res. 102:77–85. https://doi.org/10.1161/CIRCRESAHA.107.159475 . DOI: 10.1161/CIRCRESAHA.107.159475. PMID: 17967785.
Article
40. Yang YK. 2018; Aging of mesenchymal stem cells: implication in regenerative medicine. Regen Ther. 9:120–2. https://doi.org/10.1016/j.reth.2018.09.002 . DOI: 10.1016/j.reth.2018.09.002. PMID: 30525083. PMCID: PMC6222976.
Article
41. Kolf CM, Cho E, Tuan RS. 2007; Mesenchymal stromal cells. Biology of adult mesenchymal stem cells: regulation of niche, self-renewal and differentiation. Arthritis Res Ther. 9:204. https://doi.org/10.1186/ar2116 . DOI: 10.1186/ar2116. PMID: 17316462. PMCID: PMC1860068.
Article
42. Djouad F, Plence P, Bony C, Tropel P, Apparailly F, Sany J, et al. 2003; Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood. 102:3837–44. https://doi.org/10.1182/blood-2003-04-1193 . DOI: 10.1182/blood-2003-04-1193. PMID: 12881305.
Article
43. Le Blanc K. 2003; Immunomodulatory effects of fetal and adult mesenchymal stem cells. Cytotherapy. 5:485–9. https://doi.org/10.1080/14653240310003611 . DOI: 10.1080/14653240310003611. PMID: 14660044.
Article
44. Eliopoulos N, Stagg J, Lejeune L, Pommey S, Galipeau J. 2005; Allogeneic marrow stromal cells are immune rejected by MHC class I- and class II-mismatched recipient mice. Blood. 106:4057–65. https://doi.org/10.1182/blood-2005-03-1004 . DOI: 10.1182/blood-2005-03-1004. PMID: 16118325.
Article
45. Sharaf-Eldin WE, Abu-Shahba N, Mahmoud M, El-Badri N. 2016; The modulatory effects of mesenchymal stem cells on osteoclastogenesis. Stem Cells Int. 2016:1908365. https://doi.org/10.1155/2016/1908365 . DOI: 10.1155/2016/1908365. PMID: 26823668. PMCID: PMC4707367.
Article
46. Oses C, Olivares B, Ezquer M, Acosta C, Bosch P, Donoso M, et al. 2017; Preconditioning of adipose tissue-derived mesenchymal stem cells with deferoxamine increases the production of pro-angiogenic, neuroprotective and anti-inflammatory factors: potential application in the treatment of diabetic neuropathy. PLoS One. 12:e0178011. https://doi.org/10.1371/journal.pone.0178011 . DOI: 10.1371/journal.pone.0178011. PMID: 28542352. PMCID: PMC5438173.
Article
47. Hocevar BA, Brown TL, Howe PH. 1999; TGF-beta induces fibronectin synthesis through a c-Jun N-terminal kinase-dependent, Smad4-independent pathway. EMBO J. 18:1345–56. https://doi.org/10.1093/emboj/18.5.1345 . DOI: 10.1093/emboj/18.5.1345. PMID: 10064600. PMCID: PMC1171224.
Article
48. Tao T, Li Y, Gui C, Ma Y, Ge Y, Dai H, et al. 2018; Fibronectin enhances cartilage repair by activating progenitor cells through integrin α5β1 receptor. Tissue Eng Part A. 24:1112–24. https://doi.org/10.1089/ten.TEA.2017.0322 . DOI: 10.1089/ten.TEA.2017.0322. PMID: 29343182.
Article
49. Clark RA, McCoy GA, Folkvord JM, McPherson JM. 1997; TGF-beta 1 stimulates cultured human fibroblasts to proliferate and produce tissue-like fibroplasia: a fibronectin matrix-dependent event. J Cell Physiol. 170:69–80. https://doi.org/10.1002/(SICI)1097-4652(199701)170:1<69::AID-JCP8>3.0.CO;2-J . DOI: 10.1002/(SICI)1097-4652(199701)170:1<69::AID-JCP8>3.0.CO;2-J. PMID: 9012786.
Article
50. Kaigler D, Krebsbach PH, West ER, Horger K, Huang YC, Mooney DJ. 2005; Endothelial cell modulation of bone marrow stromal cell osteogenic potential. FASEB J. 19:665–7. https://doi.org/10.1096/fj.04-2529fje . DOI: 10.1096/fj.04-2529fje. PMID: 15677693.
Article
51. Liang Y, Wen L, Shang F, Wu J, Sui K, Ding Y. 2016; Endothelial progenitors enhanced the osteogenic capacities of mesenchymal stem cells in vitro and in a rat alveolar bone defect model. Arch Oral Biol. 68:123–30. https://doi.org/10.1016/j.archoralbio.2016.04.007 . DOI: 10.1016/j.archoralbio.2016.04.007. PMID: 27131592.
Article
52. Wen L, Wang Y, Wen N, Yuan G, Wen M, Zhang L, et al. 2016; Role of endothelial progenitor cells in maintaining stemness and enhancing differentiation of mesenchymal stem cells by indirect cell-cell interaction. Stem Cells Dev. 25:123–38. https://doi.org/10.1089/scd.2015.0049 . DOI: 10.1089/scd.2015.0049. PMID: 26528828.
Article
53. Farré-Guasch E, Bravenboer N, Helder MN, Schulten EAJM, Ten Bruggenkate CM, Klein-Nulend J. 2018; Blood vessel formation and bone regeneration potential of the stromal vascular fraction seeded on a calcium phosphate scaffold in the human maxillary sinus floor elevation model. Materials (Basel). 11:161. https://doi.org/10.3390/ma11010161 . DOI: 10.3390/ma11010161. PMID: 29361686. PMCID: PMC5793659.
Article
54. Marolt Presen D, Traweger A, Gimona M, Redl H. 2019; Mesenchymal stromal cell-based bone regeneration therapies: from cell transplantation and tissue engineering to therapeutic secretomes and extracellular vesicles. Front Bioeng Biotechnol. 7:352. https://doi.org/10.3389/fbioe.2019.00352 . DOI: 10.3389/fbioe.2019.00352. PMID: 31828066. PMCID: PMC6890555.
Article
55. Barreca MM, Cancemi P, Geraci F. 2020; Mesenchymal and induced pluripotent stem cells-derived extracellular vesicles: the new frontier for regenerative medicine? Cells. 9:1163. https://doi.org/10.3390/cells9051163 . DOI: 10.3390/cells9051163. PMID: 32397132. PMCID: PMC7290733.
Article
56. Lötvall J, Hill AF, Hochberg F, Buzás EI, Di Vizio D, Gardiner C, et al. 2014; Minimal experimental requirements for definition of extracellular vesicles and their functions: a position statement from the International Society for Extracellular Vesicles. J Extracell Vesicles. 3:26913. https://doi.org/10.3402/jev.v3.26913 . DOI: 10.3402/jev.v3.26913. PMID: 25536934. PMCID: PMC4275645.
Article
57. Rani S, Ryan AE, Griffin MD, Ritter T. 2015; Mesenchymal stem cell-derived extracellular vesicles: toward cell-free therapeutic applications. Mol Ther. 23:812–23. https://doi.org/10.1038/mt.2015.44 . DOI: 10.1038/mt.2015.44. PMID: 25868399. PMCID: PMC4427881.
Article
58. Yáñez-Mó M, Siljander PR, Andreu Z, Zavec AB, Borràs FE, Buzas EI, et al. 2015; Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles. 4:27066. https://doi.org/10.3402/jev.v4.27066 . DOI: 10.3402/jev.v4.27066. PMID: 25979354. PMCID: PMC4433489.
Article
59. Bruno S, Grange C, Deregibus MC, Calogero RA, Saviozzi S, Collino F, et al. 2009; Mesenchymal stem cell-derived microvesicles protect against acute tubular injury. J Am Soc Nephrol. 20:1053–67. https://doi.org/10.1681/ASN.2008070798 . DOI: 10.1681/ASN.2008070798. PMID: 19389847. PMCID: PMC2676194.
Article
60. Spees JL, Olson SD, Whitney MJ, Prockop DJ. 2006; Mitochondrial transfer between cells can rescue aerobic respiration. Proc Natl Acad Sci U S A. 103:1283–8. https://doi.org/10.1073/pnas.0510511103 . DOI: 10.1073/pnas.0510511103. PMID: 16432190. PMCID: PMC1345715.
Article
61. Zhao Q, Ren H, Han Z. 2016; Mesenchymal stem cells: immunomodulatory capability and clinical potential in immune diseases. J Cell Immunother. 2:3–20. https://doi.org/10.1016/j.jocit.2014.12.001 .
Article
62. Beckermann BM, Kallifatidis G, Groth A, Frommhold D, Apel A, Mattern J, et al. 2008; VEGF expression by mesenchymal stem cells contributes to angiogenesis in pancreatic carcinoma. Br J Cancer. 99:622–31. https://doi.org/10.1038/sj.bjc.6604508 . DOI: 10.1038/sj.bjc.6604508. PMID: 18665180. PMCID: PMC2527820.
Article
63. Razban V, Lotfi AS, Soleimani M, Ahmadi H, Massumi M, Khajeh S, et al. 2012; HIF-1α overexpression induces angiogenesis in mesenchymal stem cells. Biores Open Access. 1:174–83. https://doi.org/10.1089/biores.2012.9905 . DOI: 10.1089/biores.2012.9905. PMID: 23514846. PMCID: PMC3559201.
Article
64. Crisan M, Yap S, Casteilla L, Chen CW, Corselli M, Park TS, et al. 2008; A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell. 3:301–13. https://doi.org/10.1016/j.stem.2008.07.003 . DOI: 10.1016/j.stem.2008.07.003. PMID: 18786417.
Article
65. Chow L, Johnson V, Impastato R, Coy J, Strumpf A, Dow S. 2020; Antibacterial activity of human mesenchymal stem cells mediated directly by constitutively secreted factors and indirectly by activation of innate immune effector cells. Stem Cells Transl Med. 9:235–49. https://doi.org/10.1002/sctm.19-0092 . DOI: 10.1002/sctm.19-0092. PMID: 31702119. PMCID: PMC6988770.
Article
66. Krasnodembskaya A, Song Y, Fang X, Gupta N, Serikov V, Lee JW, et al. 2010; Antibacterial effect of human mesenchymal stem cells is mediated in part from secretion of the antimicrobial peptide LL-37. Stem Cells. 28:2229–38. https://doi.org/10.1002/stem.544 . DOI: 10.1002/stem.544. PMID: 20945332. PMCID: PMC3293245.
Article
67. Lichtman MK, Otero-Vinas M, Falanga V. 2016; Transforming growth factor beta (TGF-β) isoforms in wound healing and fibrosis. Wound Repair Regen. 24:215–22. https://doi.org/10.1111/wrr.12398 . DOI: 10.1111/wrr.12398. PMID: 26704519.
Article
68. Le Blanc K, Rasmusson I, Sundberg B, Götherström C, Hassan M, Uzunel M, et al. 2004; Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet. 363:1439–41. https://doi.org/10.1016/S0140-6736(04)16104-7 . DOI: 10.1016/S0140-6736(04)16104-7. PMID: 15121408.
Article
69. Duijvestein M, Vos AC, Roelofs H, Wildenberg ME, Wendrich BB, Verspaget HW, et al. 2010; Autologous bone marrow-derived mesenchymal stromal cell treatment for refractory luminal Crohn's disease: results of a phase I study. Gut. 59:1662–9. https://doi.org/10.1136/gut.2010.215152 . DOI: 10.1136/gut.2010.215152. PMID: 20921206.
Article
70. Liang J, Zhang H, Wang D, Feng X, Wang H, Hua B, et al. 2012; Allogeneic mesenchymal stem cell transplantation in seven patients with refractory inflammatory bowel disease. Gut. 61:468–9. https://doi.org/10.1136/gutjnl-2011-300083 . DOI: 10.1136/gutjnl-2011-300083. PMID: 21617158.
Article
71. Horwitz EM, Prockop DJ, Gordon PL, Koo WW, Fitzpatrick LA, Neel MD, et al. 2001; Clinical responses to bone marrow transplantation in children with severe osteogenesis imperfecta. Blood. 97:1227–31. https://doi.org/10.1182/blood.v97.5.1227 . DOI: 10.1182/blood.v97.5.1227. PMID: 11222364.
Article
72. Sun JM, Kurtzberg J. 2018; Cell therapy for diverse central nervous system disorders: inherited metabolic diseases and autism. Pediatr Res. 83:364–71. https://doi.org/10.1038/pr.2017.254 . DOI: 10.1038/pr.2017.254. PMID: 28985203.
Article
73. Rosset P, Deschaseaux F, Layrolle P. 2014; Cell therapy for bone repair. Orthop Traumatol Surg Res. 100(1 Suppl):S107–12. https://doi.org/10.1016/j.otsr.2013.11.010 . DOI: 10.1016/j.otsr.2013.11.010. PMID: 24411717.
Article
74. Dohan DM, Choukroun J, Diss A, Dohan SL, Dohan AJ, Mouhyi J, et al. 2006; Platelet-rich fibrin (PRF): a second-generation platelet concentrate. Part I: technological concepts and evolution. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 101:e37–44. https://doi.org/10.1016/j.tripleo.2005.07.008 . DOI: 10.1016/j.tripleo.2005.07.008. PMID: 16504849.
Article
75. Dohan Ehrenfest DM, Pinto NR, Pereda A, Jiménez P, Corso MD, Kang BS, et al. 2018; The impact of the centrifuge characteristics and centrifugation protocols on the cells, growth factors, and fibrin architecture of a leukocyte- and platelet-rich fibrin (L-PRF) clot and membrane. Platelets. 29:171–84. https://doi.org/10.1080/09537104.2017.1293812 . DOI: 10.1080/09537104.2017.1293812. PMID: 28437133.
Article
76. Calasans-Maia MD, Del Fabbro M, Le Drapper Vieira F, Capella R, et al. Fernando de Almeida Barros Mourão C. Coutinho de Mello Machado R. 2020; The use of platelet-rich fibrin in the management of medication-related osteonecrosis of the jaw: a case series. J Stomatol Oral Maxillofac Surg. 121:84–9. https://doi.org/10.1016/j.jormas.2019.02.011 . DOI: 10.1016/j.jormas.2019.02.011. PMID: 30794883.
Article
77. Barbanti SH, Santos AR Jr, Zavaglia CA, Duek EA. 2011; Poly(ε-caprolactone) and poly(D,L-lactic acid-co-glycolic acid) scaffolds used in bone tissue engineering prepared by melt compression-particulate leaching method. J Mater Sci Mater Med. 22:2377–85. https://doi.org/10.1007/s10856-011-4398-0 . DOI: 10.1007/s10856-011-4398-0. PMID: 21833608.
Article
78. Zheng P, Yao Q, Mao F, Liu N, Xu Y, Wei B, et al. 2017; Adhesion, proliferation and osteogenic differentiation of mesenchymal stem cells in 3D printed poly-ε-caprolactone/hydroxyapatite scaffolds combined with bone marrow clots. Mol Med Rep. 16:5078–84. https://doi.org/10.3892/mmr.2017.7266 . DOI: 10.3892/mmr.2017.7266. PMID: 28849142. PMCID: PMC5647033.
Article
79. Kuznetsov SA, Mankani MH, Leet AI, Ziran N, Gronthos S, Robey PG. 2007; Circulating connective tissue precursors: extreme rarity in humans and chondrogenic potential in guinea pigs. Stem Cells. 25:1830–9. https://doi.org/10.1634/stemcells.2007-0140 . DOI: 10.1634/stemcells.2007-0140. PMID: 17464083.
Article
80. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, et al. 2007; Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 131:861–72. https://doi.org/10.1016/j.cell.2007.11.019 . DOI: 10.1016/j.cell.2007.11.019. PMID: 18035408.
Article
81. Liao HT, Chen CT. 2014; Osteogenic potential: comparison between bone marrow and adipose-derived mesenchymal stem cells. World J Stem Cells. 6:288–95. https://doi.org/10.4252/wjsc.v6.i3.288 . DOI: 10.4252/wjsc.v6.i3.288. PMID: 25126378. PMCID: PMC4131270.
Article
82. Salgado AJ, Reis RL, Sousa NJ, Gimble JM. 2010; Adipose tissue derived stem cells secretome: soluble factors and their roles in regenerative medicine. Curr Stem Cell Res Ther. 5:103–10. https://doi.org/10.2174/157488810791268564 . DOI: 10.2174/157488810791268564. PMID: 19941460.
Article
83. Xin H, Katakowski M, Wang F, Qian JY, Liu XS, Ali MM, et al. 2017; MicroRNA cluster miR-17-92 cluster in exosomes enhance neuroplasticity and functional recovery after stroke in rats. Stroke. 48:747–53. https://doi.org/10.1161/STROKEAHA.116.015204 . DOI: 10.1161/STROKEAHA.116.015204. PMID: 28232590. PMCID: PMC5330787.
Article
84. Xie H, Wang Z, Zhang L, Lei Q, Zhao A, Wang H, et al. 2017; Extracellular vesicle-functionalized decalcified bone matrix scaffolds with enhanced pro-angiogenic and pro-bone regeneration activities. Sci Rep. 7:45622. https://doi.org/10.1038/srep45622 . DOI: 10.1038/srep45622. PMID: 28367979. PMCID: PMC5377422.
Article
85. Li W, Liu Y, Zhang P, Tang Y, Zhou M, Jiang W, et al. 2018; Tissue-engineered bone immobilized with human adipose stem cells-derived exosomes promotes bone regeneration. ACS Appl Mater Interfaces. 10:5240–54. https://doi.org/10.1021/acsami.7b17620 . DOI: 10.1021/acsami.7b17620. PMID: 29359912.
Article
86. Shi Q, Qian Z, Liu D, Sun J, Wang X, Liu H, et al. 2017; GMSC-derived exosomes combined with a chitosan/silk hydrogel sponge accelerates wound healing in a diabetic rat skin defect model. Front Physiol. 8:904. https://doi.org/10.3389/fphys.2017.00904 . DOI: 10.3389/fphys.2017.00904. PMID: 29163228. PMCID: PMC5681946.
Article
87. Shao L, Zhang Y, Lan B, Wang J, Zhang Z, Zhang L, et al. 2017; MiRNA-sequence indicates that mesenchymal stem cells and exosomes have similar mechanism to enhance cardiac repair. Biomed Res Int. 2017:4150705. https://doi.org/10.1155/2017/4150705 . DOI: 10.1155/2017/4150705. PMID: 28203568. PMCID: PMC5292186.
Article
88. Park SR, Kim JW, Jun HS, Roh JY, Lee HY, Hong IS. 2018; Stem cell secretome and its effect on cellular mechanisms relevant to wound healing. Mol Ther. 26:606–17. https://doi.org/10.1016/j.ymthe.2017.09.023 . DOI: 10.1016/j.ymthe.2017.09.023. PMID: 29066165. PMCID: PMC5835016.
Article
89. Filip S, Mokry J, Horacek J, English D. 2008; Stem cells and the phenomena of plasticity and diversity: a limiting property of carcinogenesis. Stem Cells Dev. 17:1031–8. https://doi.org/10.1089/scd.2007.0234 . DOI: 10.1089/scd.2007.0234. PMID: 19006453.
Article
90. Heslop JA, Hammond TG, Santeramo I, Tort Piella A, Hopp I, Zhou J, et al. 2015; Concise review: workshop review: understanding and assessing the risks of stem cell-based therapies. Stem Cells Transl Med. 4:389–400. https://doi.org/10.5966/sctm.2014-0110 . DOI: 10.5966/sctm.2014-0110. PMID: 25722427. PMCID: PMC4367503.
Article
91. Cyranoski D. 2010; Korean deaths spark inquiry. Nature. 468:485. https://doi.org/10.1038/468485a . DOI: 10.1038/468485a. PMID: 21107396.
Article
92. Jung JW, Kwon M, Choi JC, Shin JW, Park IW, Choi BW, et al. 2013; Familial occurrence of pulmonary embolism after intravenous, adipose tissue-derived stem cell therapy. Yonsei Med J. 54:1293–6. https://doi.org/10.3349/ymj.2013.54.5.1293 . DOI: 10.3349/ymj.2013.54.5.1293. PMID: 23918585. PMCID: PMC3743204.
Article
93. Coppin L, Sokal E, Stéphenne X. 2019; Thrombogenic risk induced by intravascular mesenchymal stem cell therapy: current status and future perspectives. Cells. 8:1160. https://doi.org/10.3390/cells8101160 . DOI: 10.3390/cells8101160. PMID: 31569696. PMCID: PMC6829440.
Article
94. Stultz BG, McGinnis K, Thompson EE, Lo Surdo JL, Bauer SR, Hursh DA. 2016; Chromosomal stability of mesenchymal stromal cells during in vitro culture. Cytotherapy. 18:336–43. https://doi.org/10.1016/j.jcyt.2015.11.017 . DOI: 10.1016/j.jcyt.2015.11.017. PMID: 26780865. PMCID: PMC5516473.
Article
95. André T, Meuleman N, Stamatopoulos B, De Bruyn C, Pieters K, Bron D, et al. 2013; Evidences of early senescence in multiple myeloma bone marrow mesenchymal stromal cells. PLoS One. 8:e59756. https://doi.org/10.1371/journal.pone.0059756 . DOI: 10.1371/journal.pone.0059756. PMID: 23555770. PMCID: PMC3605355.
Article
96. Stagg J, Pommey S, Eliopoulos N, Galipeau J. 2006; Interferon-gamma-stimulated marrow stromal cells: a new type of nonhematopoietic antigen-presenting cell. Blood. 107:2570–7. https://doi.org/10.1182/blood-2005-07-2793 . DOI: 10.1182/blood-2005-07-2793. PMID: 16293599.
Article
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