Alternative source of stem cells derived from human periodontal ligament: A new treatment for experimental autoimmune encephalomyelitis

Stem Cell Research and Therapy

Volumn 7, Issue 1, 2016, Pages

  Trubiani, Oriana ^a   Giacoppo, Sabrina ^b   Ballerini, Patrizia ^a   Diomede, Francesca ^a   Piattelli, Adriano ^a   Bramanti, Placido ^b   Mazzon, Emanuela ^b  

^a UNIVERSITY OF CHIETI   (Italy)

^b IRCCS CENTRO NEUROLESI BONINO PULEJO   (Italy)

Author keywords

Apoptosis; Multiple sclerosis; Neurotrophic factors; Stem cells derived from human periodontal ligament

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CASPASE 3; CD4 ANTIGEN; GLIAL FIBRILLARY ACIDIC PROTEIN; INTERLEUKIN 10; INTERLEUKIN 1BETA; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; NERVE GROWTH FACTOR; NEUROTROPHIC FACTOR; PROTEIN P21; PROTEIN P53; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR NRF2; TUMOR NECROSIS FACTOR ALPHA; CD8 ANTIGEN; CD8 ANTIGEN, ALPHA CHAIN; GLIAL FIBRILLARY ASTROCYTIC PROTEIN, MOUSE; NFE2L2 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BRAIN TISSUE; CD8+ T LYMPHOCYTE; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE COURSE; EXPERIMENTAL ALLERGIC ENCEPHALITIS; HISTOPATHOLOGY; HUMAN; IMMUNIZATION; IMMUNOHISTOCHEMISTRY; IMMUNOPHENOTYPING; LYMPHOCYTIC INFILTRATION; MALE; MESENCHYMAL STEM CELL; MOUSE; MTT ASSAY; MULTIPLE SCLEROSIS; NEUROPROTECTION; NONHUMAN; PERIODONTAL LIGAMENT; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RNA ISOLATION; SPINAL CORD; TAIL VEIN; WEIGHT REDUCTION; WESTERN BLOTTING; ADULT STEM CELL; ANIMAL; BLOOD BRAIN BARRIER; C57BL MOUSE; CELL DIFFERENTIATION; CYTOLOGY; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; IMMUNOLOGY; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMA CELL; METABOLISM; PATHOLOGY; PHYSIOLOGY; PRIMARY CELL CULTURE; REGULATORY T LYMPHOCYTE; VASCULAR ENDOTHELIUM;

ADULT STEM CELLS; ANIMALS; ANTIGENS, CD4; ANTIGENS, CD8; APOPTOSIS; BLOOD-BRAIN BARRIER; CELL DIFFERENTIATION; CELL PROLIFERATION; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; ENDOTHELIUM, VASCULAR; GLIAL FIBRILLARY ACIDIC PROTEIN; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICE, INBRED C57BL; MULTIPLE SCLEROSIS; NF-E2-RELATED FACTOR 2; PERIODONTAL LIGAMENT; PRIMARY CELL CULTURE; T-LYMPHOCYTES, REGULATORY;

EID: 84954212021     PISSN: None     EISSN: 17576512     Source Type: Journal    
DOI: 10.1186/s13287-015-0253-4     Document Type: Article

References (50)

1. Sospedra M, Martin R. Immunology of multiple sclerosis. Annu Rev Immunol. 2005;23:683-747.
2. Siffrin V, Brandt AU, Herz J, Zipp F. New insights into adaptive immunity in chronic neuroinflammation. Adv Immunol. 2007;96:1-40.
3. Weber MS, Menge T, Lehmann-Horn K, Kronsbein HC, Zettl U, Sellner J, et al. Current treatment strategies for multiple sclerosis - efficacy versus neurological adverse effects. Curr Pharm Des. 2012;18:209-19.
4. Kassis I, Grigoriadis N, Gowda-Kurkalli B, Mizrachi-Kol R, Ben-Hur T, Slavin S, et al. Neuroprotection and immunomodulation with mesenchymal stem cells in chronic experimental autoimmune encephalomyelitis. Arch Neurol. 2008;65:753-61.
5. Bowles AC, Scruggs BA, Bunnell BA. Mesenchymal stem cell-based therapy in a mouse model of experimental autoimmune encephalomyelitis (EAE). Methods Mol Biol. 2014;1213:303-19.
6. Kurte M, Bravo-Alegria J, Torres A, Carrasco V, Ibáñez C, Vega-Letter AM, et al. Intravenous administration of bone marrow-derived mesenchymal stem cells induces a switch from classical to atypical symptoms in experimental autoimmune encephalomyelitis. Stem Cells Int. 2015;2015:140170.
7. El-Akabawy G, Rashed LA. Beneficial effects of bone marrow-derived mesenchymal stem cell transplantation in a non-immune model of demyelination. Ann Anat. 2015;198:11-20.
8. Gold R, Linington C, Lassmann H. Understanding pathogenesis and therapy of multiple sclerosis via animal models: 70 years of merits and culprits in experimental autoimmune encephalomyelitis research. Brain. 2006;129:1953-71.
9. Wagers AJ, Weissman IL. Plasticity of adult stem cells. Cell. 2004;116:639-48.
10. Martino G, Franklin RJ, Baron Van Evercooren A, Kerr DA. Stem Cells in Multiple Sclerosis (STEMS) Consensus Group. Stem cell transplantation in multiple sclerosis: current status and future prospects. Nat Rev Neurol. 2010;6:247-55.
11. Bai L, Lennon DP, Eaton V, Maier K, Caplan AI, Miller SD. Human bone marrow-derived mesenchymal stem cells induce Th2-polarized immune response and promote endogenous repair in animal models of multiple sclerosis. Glia. 2009;57:1192-203.
12. Wilkins A, Kemp K, Ginty M, Hares K, Mallam E, Scolding N. Human bone marrow-derived mesenchymal stem cells secrete brain-derived neurotrophic factor which promotes neuronal survival in vitro. Stem Cell Res. 2009;3:63-70.
13. Kemp K, Hares K, Mallam E, Heesom KJ, Scolding N, Wilkins A. Mesenchymal stem cell-secreted superoxide dismutase promotes cerebellar neuronal survival. J Neurochem. 2010;114:1569-80.
14. Rincon JC, Young WG, Bartold PM. The epithelial cell rests of Malassez - a role in periodontal regeneration? J Periodontal Res. 2006;41:245-52.
15. Diomede F, Caputi S, Merciaro I, Frisone S, D'Arcangelo C, Piattelli A, et al. Pro-inflammatory cytokine release and cell growth inhibition in primary human oral cells after exposure to endodontic sealer. Int Endod J. 2014;47:864-72.
16. Trubiani O, Horenstein AL, Caciagli F, Caputi S, Malavasi F, Ballerini P. Expression of P2X7 ATP receptor mediating the IL8 and CCL20 release in human periodontal ligament stem cells. J Cell Biochem. 2014;115:1138-46.
17. Trubiani O, Piattelli A, Gatta V, Marchisio M, Diomede F, D'Aurora M, et al. Assessment of an efficient xeno-free culture system of human periodontal ligament stem cells. Tissue Eng Part C Meth. 2015;21:52-64.
18. Manescu A, Giuliani A, Mohammadi S, Tromba G, Mazzoni S, Diomede F, et al. Osteogenic potential of dualblocks cultured with human periodontal ligament stem cells: in vitro and synchrotron microtomography study. J Periodontal Res. 2015;11:1-13.
19. Fortino VR, Chen RS, Pelaez D, Cheung HS. Neurogenesis of neural crest-derived periodontal ligament stem cells by EGF and bFGF. J Cell Physiol. 2014;229:479-88.
20. Osathanon T, Manokawinchoke J, Nowwarote N, Aguilar P, Palaga T, Pavasant P. Notch signaling is involved in neurogenic commitment of human periodontal ligament-derived mesenchymal stem cells. Stem Cells Dev. 2013;22:1220-31.
21. Widera D, Grimm WD, Moebius JM, Mikenberg I, Piechaczek C, Gassmann G, et al. Highly efficient neural differentiation of human somatic stem cells, isolated by minimally invasive periodontal surgery. Stem Cells Dev. 2007;16:447-60.
22. Kadar K, Kiraly M, Porcsalmy B, Molnar B, Racz GZ, Blazsek J, et al. Differentiation potential of stem cells from human dental origin - promise for tissue engineering. J Physiol Pharmacol. 2009;7:167-75.
23. Arthur A, Rychkov G, Shi S, Koblar SA, Gronthos S. Adult human dental pulp stem cells differentiate toward functionally active neurons under appropriate environmental cues. Stem Cells. 2008;26:1787-95.
24. Eleuterio E, Trubiani O, Sulpizio M, Di Giuseppe F, Pierdomenico L, Marchisio M, et al. Proteome of human stem cells from periodontal ligament and dental pulp. PLoS One. 2013;8:e71101.
25. Tomar GB, Srivastava RK, Gupta N, Barhanpurkar AP, Pote ST, Jhaveri HM, et al. Human gingiva-derived mesenchymal stem cells are superior to bone marrow-derived mesenchymal stem cells for cell therapy in regenerative medicine. Biochem Biophys Res Commun. 2010;393:377-83.
26. Trubiani O, Isgro A, Zini N, Antonucci I, Aiuti F, Di Primio R, et al. Functional interleukin-7/interleukin-7Ralpha, and SDF-1alpha/CXCR4 are expressed by human periodontal ligament derived mesenchymal stem cells. J Cell Physiol. 2008;214:706-13.
27. Yang H, Gao LN, An Y, Hu CH, Jin F, Zhou J, et al. Comparison of mesenchymal stem cells derived from gingival tissue and periodontal ligament in different incubation conditions. Biomaterials. 2013;34:7033-47.
28. Paschalidis N, Iqbal AJ, Maione F, Wood EG, Perretti M, Flower RJ, et al. Modulation of experimental autoimmune encephalomyelitis by endogenous annexin A1. J Neuroinflammation. 2009;6:33.
29. Rodrigues DH, Vilela MC, Barcelos LS, Pinho V, Teixeira MM, Teixeira AL. Absence of PI3Kgamma leads to increased leukocyte apoptosis and diminished severity of experimental autoimmune encephalomyelitis. J Neuroimmunol. 2010;222:90-4.
30. Trubiani O, Fulle S, Traini T, Paludi M, la Rovere R, Orciani M, et al. Functional assay, expression of growth factors and proteins modulating bone-arrangement in human osteoblasts seeded on an anorganic bovine bone biomaterial. Eur Cell Mater. 2010;20:72-83.
31. Banfi A, Muraglia A, Dozin B, Mastrogiacomo M, Cancedda R, Quarto R. Proliferation kinetics and differentiation potential of ex vivo expanded human bone marrow stromal cells: Implications for their use in cell therapy. Exp Hematol. 2000;28:707-15.
32. Salvadè A, Belotti D, Donzelli E, D'Amico G, Gaipa G, Renoldi G, et al. GMP-grade preparation of biomimetic scaffolds with osteo-differentiated autologous mesenchymal stromal cells for the treatment of alveolar bone resorption in periodontal disease. Cytotherapy. 2007;9:427-38.
33. Li Z, Jiang CM, An S, Cheng Q, Huang YF, Wang YT, et al. Immunomodulatory properties of dental tissue-derived mesenchymal stem cells. Oral Dis. 2014;20:25-34.
34. Peled A, Grabovsky V, Habler L, Sandbank J, Arenzana-Seisdedos F, Petit I, et al. The chemokine SDF-1 stimulates integrin-mediated arrest of CD34(+) cells on vascular endothelium under shear flow. J Clin Invest. 1999;104:1199-211.
35. Zagzag D, Krishnamachary B, Yee H, Okuyama H, Chiriboga L, Ali MA, et al. Stromal cell-derived factor-1alpha and CXCR4 expression in hemangioblastoma and clear cell-renal cell carcinoma: von Hippel-Lindau loss-of-function induces expression of a ligand and its receptor. Cancer Res. 2005;65:6178-88.
36. Ding G, Liu Y, Wang W, Wei F, Liu D, Fan Z, et al. Allogeneic periodontal ligament stem cell therapy for periodontitis in swine. Stem Cells. 2010;28:1829-38.
37. Zappia E, Casazza S, Pedemonte E, Benvenuto F, Bonanni I, Gerdoni E, et al. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood. 2005;106:1755-61.
38. Morando S, Vigo T, Esposito M, Casazza S, Novi G, Principato MC, et al. The therapeutic effect of mesenchymal stem cell transplantation in experimental autoimmune encephalomyelitis is mediated by peripheral and central mechanisms. Stem Cell Res Ther. 2012;3:3.
39. Amor S, Peferoen LA, Vogel DY, Breur M, van der Valk P, Baker D, et al. Inflammation in neurodegenerative diseases - an update. Immunology. 2014;142:151-66.
40. Dittel BN. CD4 T cells: Balancing the coming and going of autoimmune-mediated inflammation in the CNS. Brain Behav Immun. 2008;22:421-30.
41. Marson A, Kretschmer K, Frampton GM, Jacobsen ES, Polansky JK, MacIsaac KD, et al. Foxp3 occupancy and regulation of key target genes during T-cell stimulation. Nature. 2007;445:931-5.
42. Abbott NJ, Patabendige AA, Dolman DE, Yusof SR, Begley DJ. Structure and function of the blood-brain barrier. Neurobiol Dis. 2010;37:13-25.
43. Nitta T, Hata M, Gotoh S, Seo Y, Sasaki H, Hashimoto N, et al. Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice. J Cell Biol. 2003;161:653-60.
44. Abbott NJ, Ronnback L, Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci. 2006;7:41-53.
45. Ji L, Li H, Gao P, Shang G, Zhang DD, Zhang N, et al. Nrf2 pathway regulates multidrug-resistance-associated protein 1 in small cell lung cancer. PLoS One. 2013;8:e63404.
46. Calkins MJ, Johnson DA, Townsend JA, Vargas MR, Dowell JA, Williamson TP, et al. The Nrf2/ARE pathway as a potential therapeutic target in neurodegenerative disease. Antioxid Redox Signal. 2009;11:497-508.
47. Dasgupta A, Zheng J, Perrone-Bizzozero NI, Bizzozero OA. Increased carbonylation, protein aggregation and apoptosis in the spinal cord of mice with experimental autoimmune encephalomyelitis. ASN Neuro. 2013;5:e00111.
48. Lucchinetti C, Brück W, Parisi J, Scheithauer B, Rodriguez M, Lassmann H. Heterogeneity of multiple sclerosis lesions: implications for the pathogenesis of demyelination. Ann Neurol. 2000;47:707-17.
49. Sheikh MS, Fornace Jr AJ. Role of p53 family members in apoptosis. J Cell Physiol. 2000;182:171-81.
50. Binder DK, Scharfman HE. Brain-derived neurotrophic factor. Growth Factors. 2004;22:123-31.