Interactions between immune system and mesenchymal stem cells in dental pulp and periapical tissues

International Endodontic Journal

Volumn 45, Issue 8, 2012, Pages 689-701

  Leprince, J G ^a,b,c   Zeitlin, B D ^a   Tolar, M ^a   Peters, O A ^a  

^a UNIVERSITY OF THE PACIFIC   (United States)

^b UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^c CRIBIO Center for Research and Engineering on Biomaterials   (Belgium)

Author keywords

Cytokines; Growth factors; Immune system; Immunosuppression; Inflammation; Mesenchymal stem cells; Periapical lesion; Pulp capping

Indexed keywords

CYTOKINE;

HUMAN; IMMUNOLOGY; IMMUNOMODULATION; MESENCHYMAL STROMA CELL; PERIODONTIUM; PHYSIOLOGY; REVIEW; TOOTH PULP; WOUND HEALING;

CYTOKINES; DENTAL PULP; HUMANS; IMMUNOMODULATION; MESENCHYMAL STROMAL CELLS; PERIAPICAL TISSUE; WOUND HEALING;

EID: 84863780119     PISSN: 01432885     EISSN: 13652591     Source Type: Journal    
DOI: 10.1111/j.1365-2591.2012.02028.x     Document Type: Review

References (107)

1. About I (2011) Dentin regeneration in vitro: the pivotal role of supportive cells. Advances in Dental Research 23, 320-4.
2. Abukawa H, Kaban LB, Williams WB, Terada S, Vacanti JP, Troulis MJ (2006) Effect of interferon-alpha-2b on porcine mesenchymal stem cells. Journal of Oral and Maxillofacial Surgery 64, 1214-20.
3. Aggarwal S, Pittenger MF (2005) Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105, 1815-22.
4. Aguilar P, Linsuwanont P (2011) Vital pulp therapy in vital permanent teeth with cariously exposed pulp: a systematic review. Journal of Endodontics 37, 581-7.
5. Alm JJ, Koivu HM, Heino TJ, Hentunen TA, Laitinen S, Aro HT (2010) Circulating plastic adherent mesenchymal stem cells in aged hip fracture patients. Journal of Orthopedic Research 28, 1634-42.
6. Alongi DJ, Yamaza T, Song Y et al. (2010) Stem/progenitor cells from inflamed human dental pulp retain tissue regeneration potential. Regenerative Medicine 5, 617-31.
7. Bakopoulou A, Leyhausen G, Volk J et al. (2011) Effects of hema and tedgma on the in vitro odontogenic differentiation potential of human pulp stem/progenitor cells derived from deciduous teeth. Dental Materials 27, 608-17.
8. Bartholomew A, Sturgeon C, Siatskas M et al. (2002) Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Experimental Hematology 30, 42-8.
9. Bjorndal L, Reit C, Bruun G et al. (2010) Treatment of deep caries lesions in adults: randomized clinical trials comparing stepwise vs. Direct complete excavation, and direct pulp capping vs. Partial pulpotomy. European Journal of Oral Sciences 118, 290-7.
10. Brandl A, Meyer M, Bechmann V, Nerlich M, Angele P (2011) Oxidative stress induces senescence in human mesenchymal stem cells. Experimental Cell Research 317, 1541-7.
11. Casagrande L, Demarco FF, Zhang Z, Araujo FB, Shi S, Nor JE (2010) Dentin-derived bmp-2 and odontoblast differentiation. Journal of Dental Research 89, 603-8.
12. Croitoru-Lamoury J, Lamoury FM, Caristo M et al. (2011) Interferon-gamma regulates the proliferation and differentiation of mesenchymal stem cells via activation of indoleamine 2, 3 dioxygenase (ido). PLoS One 6, e14698.
13. D'Alimonte I, Nargi E, Mastrangelo F et al. (2011) Vascular endothelial growth factor enhances in vitro proliferation and osteogenic differentiation of human dental pulp stem cells. Journal of Biological Regulators & Homeostatic Agents 25, 57-69.
14. Deans RJ, Moseley AB (2000) Mesenchymal stem cells: biology and potential clinical uses. Experimental Hematology 28, 875-84.
15. Del Prete G (1998) The concept of type-1 and type-2 helper t cells and their cytokines in humans. International Reviews of Immunology 16, 427-55.
16. Di Nicola M, Carlo-Stella C, Magni M et al. (2002) Human bone marrow stromal cells suppress t-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 99, 3838-43.
17. Diaz-Romero J, Gaillard JP, Grogan SP, Nesic D, Trub T, Mainil-Varlet P (2005) Immunophenotypic analysis of human articular chondrocytes: changes in surface markers associated with cell expansion in monolayer culture. Journal of Cellular Physiology 202, 731-42.
18. Ding G, Liu Y, An Y et al. (2010) Suppression of t cell proliferation by root apical papilla stem cells in vitro. Cells Tissues Organs 191, 357-64.
19. Docheva D, Haasters F, Schieker M (2008) Mesenchymal stem cells and their cell surface receptors. Current Rheumatology Reviews 4, 155-60.
20. Dominici M, Le Blanc K, Mueller I et al. (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The international society for cellular therapy position statement. Cytotherapy 8, 315-7.
21. D'Souza R (2002) Development of the pulpodentin complex. In: Hargreaves K, Goodis H, eds. Seltzer and Bender's Dental Pulp. Carol Stream, IL: Quintessence Publishing Co, Inc, pp. 31-2.
22. Dummer PM, Hicks R, Huws D (1980) Clinical signs and symptoms in pulp disease. International Endodontic Journal 13, 27-35.
23. Fabricius L, Dahlen G, Sundqvist G, Happonen RP, Moller AJ (2006) Influence of residual bacteria on periapical tissue healing after chemomechanical treatment and root filling of experimentally infected monkey teeth. European Journal of Oral Sciences 114, 278-85.
24. Ferracane JL (1994) Elution of leachable components from composites. Journal of Oral Rehabilitation 21, 441-52.
25. Ferracane JL, Cooper PR, Smith AJ (2010) Can interaction of materials with the dentin-pulp complex contribute to dentin regeneration? Odontology 98, 2-14.
26. Fouad A, Huang G (2008) Inflammation and host responses. In: Bakland L, Baumgartner J, eds. Ingle's Endodontics, 7th edn. Hamilton ON, Canada: Beckers, pp. 343-75.
27. Goldberg M, Schmalz G (2011) Toward a strategic plan for pulp healing: from repair to regeneration. Clinical Oral Investigations 15, 1-2.
28. Goldberg M, Farges JC, Lacerda-Pinheiro S et al. (2008) Inflammatory and immunological aspects of dental pulp repair. Pharmacological Research 58, 137-47.
29. Graves DT, Chen CP, Douville C, Jiang YL (2000) Interleukin-1 receptor signaling rather than that of tumor necrosis factor is critical in protecting the host from the severe consequences of a polymicrobe anaerobic infection. Infection and Immunity 68, 4746-51.
30. Graves DT, Oates T, Garlet GP (2011) Review of osteoimmunology and the host response in endodontic and periodontal lesions. Journal of Oral Microbiology 3, 5304. DOI: 10.3402/jom.v3i0.5304.
31. Hahn CL, Liewehr FR (2007a) Update on the adaptive immune responses of the dental pulp. Journal of Endodontics 33, 773-81.
32. Hahn CL, Liewehr FR (2007b) Innate immune responses of the dental pulp to caries. Journal of Endodontics 33, 643-51.
33. Hahn CL, Falkler WA Jr, Siegel MA (1989) A study of t and b cells in pulpal pathosis. Journal of Endodontics 15, 20-6.
34. Harichane Y, Hirata A, Dimitrova-Nakov S et al. (2011) Pulpal progenitors and dentin repair. Advances in Dental Research 23, 307-12.
35. Harrison AJ, Chivatxaranukul P, Parashos P, Messer HH (2010) The effect of ultrasonically activated irrigation on reduction of enterococcus faecalis in experimentally infected root canals. International Endodontic Journal 43, 968-77.
36. He H, Yu J, Liu Y et al. (2008) Effects of fgf2 and tgfbeta1 on the differentiation of human dental pulp stem cells in vitro. Cell Biology International 32, 827-34.
37. Hørsted-Bindslev P, Løvschall H (2002) Treatment outcome of vital pulp treatment. Endodontic Topics 2, 24-34.
38. Howard C, Murray PE, Namerow KN (2010) Dental pulp stem cell migration. Journal of Endodontics 36, 1963-6.
39. Huang GT, Gronthos S, Shi S (2009) Mesenchymal stem cells derived from dental tissues vs. Those from other sources: their biology and role in regenerative medicine. Journal of Dental Research 88, 792-806.
40. Huang CH, Tseng WY, Yao CC, Jeng JH, Young TH, Chen YJ (2010) Glucosamine promotes osteogenic differentiation of dental pulp stem cells through modulating the level of the transforming growth factor-beta type i receptor. Journal of Cellular Physiology 225, 140-51.
41. Huojia M, Muraoka N, Yoshizaki K et al. (2005) Tgf-beta3 induces ectopic mineralization in fetal mouse dental pulp during tooth germ development. Development, Growth & Differentiation 47, 141-52.
42. Iohara K, Nakashima M, Ito M, Ishikawa M, Nakasima A, Akamine A (2004) Dentin regeneration by dental pulp stem cell therapy with recombinant human bone morphogenetic protein 2. Journal of Dental Research 83, 590-5.
43. Jiang L, Zhu YQ, Du R et al. (2008) The expression and role of stromal cell-derived factor-1alpha-cxcr4 axis in human dental pulp. Journal of Endodontics 34, 939-44.
44. Josefowicz SZ, Rudensky A (2009) Control of regulatory t cell lineage commitment and maintenance. Immunity 30, 616-25.
45. Kebriaei P, Robinson S (2011) Treatment of graft-versus-host-disease with mesenchymal stromal cells. Cytotherapy 13, 262-8.
46. Kemoun P, Laurencin-Dalicieux S, Rue J et al. (2007) Human dental follicle cells acquire cementoblast features under stimulation by bmp-2/-7 and enamel matrix derivatives (emd) in vitro. Cell and Tissue Research 329, 283-94.
47. Kikuiri T, Kim I, Yamaza T et al. (2010) Cell-based immunotherapy with mesenchymal stem cells cures bisphosphonate-related osteonecrosis of the jaw-like disease in mice. Journal of Bone and Mineral Research 25, 1668-79.
48. Kim YS, Min KS, Jeong DH, Jang JH, Kim HW, Kim EC (2010) Effects of fibroblast growth factor-2 on the expression and regulation of chemokines in human dental pulp cells. Journal of Endodontics 36, 1824-30.
49. Klyushnenkova E, Mosca JD, Zernetkina V et al. (2005) T cell responses to allogeneic human mesenchymal stem cells: immunogenicity, tolerance, and suppression. Journal of Biomedical Science 12, 47-57.
50. Koh ET, Torabinejad M, Pitt Ford TR, Brady K, McDonald F (1997) Mineral trioxide aggregate stimulates a biological response in human osteoblasts. Journal of Biomedical Materials Research: Part A 37, 432-9.
51. Komabayashi T, Zhu Q (2010) Innovative endodontic therapy for anti-inflammatory direct pulp capping of permanent teeth with a mature apex. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology and Endodontology 109, e75-81.
52. Krifka S, Petzel C, Hiller KA et al. (2010) Resin monomer-induced differential activation of map kinases and apoptosis in mouse macrophages and human pulp cells. Biomaterials 31, 2964-75.
53. Lamblin G, Leprince J, Devaux J, Mestdagh M, Gallez B, Leloup G (2010) Hydroxyl radical release from dental resins: electron paramagnetic resonance evidence. Acta Biomaterialia 6, 3193-8.
54. Le Blanc K (2006) Mesenchymal stromal cells: tissue repair and immune modulation. Cytotherapy 8, 559-61.
55. Le Blanc K, Tammik C, Rosendahl K, Zetterberg E, Ringden O (2003) Hla expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Experimental Hematology 31, 890-6.
56. Leon ER, Iwasaki K, Komaki M, Kojima T, Ishikawa I (2007) Osteogenic effect of interleukin-11 and synergism with ascorbic acid in human periodontal ligament cells. Journal of Periodontal Research 42, 527-35.
57. Leprince JG, Hadis M, Shortall AC et al. (2011) Photoinitiator type and applicability of exposure reciprocity law in filled and unfilled photoactive resins. Dental Materials 27, 157-64.
58. Liao J, Al Shahrani M, Al-Habib M, Tanaka T, Huang GT (2011) Cells isolated from inflamed periapical tissue express mesenchymal stem cell markers and are highly osteogenic. Journal of Endodontics 37, 1217-24.
59. Lima GQ, Oliveira EG, Souza JI, Monteiro Neto V (2005) Comparison of the efficacy of chemomechanical and mechanical methods of caries removal in the reduction of streptococcus mutans and lactobacillus spp in carious dentine of primary teeth. Journal of Applied Oral Science 13, 399-405.
60. Lin LM, Rosenberg PA (2011) Repair and regeneration in endodontics. International Endodontic Journal 44, 889-906.
61. Maddur MS, Othy S, Hegde P et al. (2010) Immunomodulation by intravenous immunoglobulin: role of regulatory t cells. Journal of Clinical Immunology 30(Suppl 1), S4-8.
62. Mathieu S, El-Battari A, Dejou J, About I (2005) Role of injured endothelial cells in the recruitment of human pulp cells. Archives of Oral Biology 50, 109-13.
63. Matsuo T, Nakanishi T, Shimizu H, Ebisu S (1996) A clinical study of direct pulp capping applied to carious-exposed pulps. Journal of Endodontics 22, 551-6.
64. Matsushita K, Motani R, Sakuta T et al. (2000) The role of vascular endothelial growth factor in human dental pulp cells: induction of chemotaxis, proliferation, and differentiation and activation of the ap-1-dependent signaling pathway. Journal of Dental Research 79, 1596-603.
65. McNicholas S, Torabinejad M, Blankenship J, Bakland L (1991) The concentration of prostaglandin e2 in human periradicular lesions. Journal of Endodontics 17, 97-100.
66. Michaelson PL, Holland GR (2002) Is pulpitis painful? International Endodontic Journal 35, 829-32.
67. Miles JP, Gluskin AH, Chambers D, Peters OA (2010) Pulp capping with mineral trioxide aggregate (mta): a retrospective analysis of carious pulp exposures treated by undergraduate dental students. Operative Dentistry 35, 20-8.
68. Miyara M, Sakaguchi S (2007) Natural regulatory t cells: mechanisms of suppression. Trends in Molecular Medicine 13, 108-16.
69. Molander A, Reit C, Dahlen G, Kvist T (1998) Microbiological status of root-filled teeth with apical periodontitis. International Endodontic Journal 31, 1-7.
70. Morsczeck C, Gotz W, Schierholz J et al. (2005) Isolation of precursor cells (pcs) from human dental follicle of wisdom teeth. Matrix Biology 24, 155-65.
71. Murray PE, Garcia-Godoy F, Hargreaves KM (2007) Regenerative endodontics: a review of current status and a call for action. Journal of Endodontics 33, 377-90.
72. Nair PN (2004) Pathogenesis of apical periodontitis and the causes of endodontic failures. Critical Reviews in Oral Biology & Medicine 15, 348-81.
73. Nakashima M (1994) Induction of dentin formation on canine amputated pulp by recombinant human bone morphogenetic proteins (bmp)-2 and -4. Journal of Dental Research 73, 1515-22.
74. Nemeth K, Keane-Myers A, Brown JM et al. (2010) Bone marrow stromal cells use tgf-beta to suppress allergic responses in a mouse model of ragweed-induced asthma. Proceedings of the National Academy of Sciences of the United States of America 107, 5652-7.
75. Ng YL, Mann V, Gulabivala K (2011) A prospective study of the factors affecting outcomes of nonsurgical root canal treatment: part 1: periapical health. International Endodontic Journal 44, 583-609.
76. Pagoria D, Lee A, Geurtsen W (2005) The effect of camphorquinone (cq) and cq-related photosensitizers on the generation of reactive oxygen species and the production of oxidative DNA damage. Biomaterials 26, 4091-9.
77. Paula-Silva FW, Ghosh A, Silva LA, Kapila YL (2009) Tnf-alpha promotes an odontoblastic phenotype in dental pulp cells. Journal of Dental Research 88, 339-44.
78. Peters LB, Wesselink PR (2002) Periapical healing of endodontically treated teeth in one and two visits obturated in the presence or absence of detectable microorganisms. International Endodontic Journal 35, 660-7.
79. Pierdomenico L, Bonsi L, Calvitti M et al. (2005) Multipotent mesenchymal stem cells with immunosuppressive activity can be easily isolated from dental pulp. Transplantation 80, 836-42.
80. Polydorou O, Konig A, Hellwig E, Kummerer K (2009) Long-term release of monomers from modern dental-composite materials. European Journal of Oral Sciences 117, 68-75.
81. Resnick IB, Stepensky P, Shapira MY et al. (2009) Treatment of severe acute graft-versus-host disease with mesenchymal stromal cells. Blood 114, 886-7.
82. Ricketts DN, Kidd EA, Innes N, Clarkson J (2006) Complete or ultraconservative removal of decayed tissue in unfilled teeth. Cochrane Database of Systematic Reviews 3, CD003808.
83. Rodriguez-Lozano FJ, Bueno C, Insausti CL et al. (2011) Mesenchymal stem cells derived from dental tissues. International Endodontic Journal 44, 800-6.
84. Ryan JM, Barry FP, Murphy JM, Mahon BP (2005) Mesenchymal stem cells avoid allogeneic rejection. Journal of Inflammation 2, 8.
85. Sant'Ana AC, Marques MM, Barroso TE, Passanezi E, de Rezende ML (2007) Effects of tgf-beta1, pdgf-bb, and igf-1 on the rate of proliferation and adhesion of a periodontal ligament cell lineage in vitro. Journal of Periodontology 78, 2007-17.
86. Sathorn C, Parashos P, Messer H (2007) Antibacterial efficacy of calcium hydroxide intracanal dressing: a systematic review and meta-analysis. International Endodontic Journal 40, 2-10.
87. Schwab JM, Chiang N, Arita M, Serhan CN (2007) Resolvin e1 and protectin d1 activate inflammation-resolution programmes. Nature 447, 869-74.
88. Shiba H, Nakamura S, Shirakawa M et al. (1995) Effects of basic fibroblast growth factor on proliferation, the expression of osteonectin (sparc) and alkaline phosphatase, and calcification in cultures of human pulp cells. Developmental Biology 170, 457-66.
89. Sloan AJ, Smith AJ (1999) Stimulation of the dentine-pulp complex of rat incisor teeth by transforming growth factor-beta isoforms 1-3 in vitro. Archives of Oral Biology 44, 149-56.
90. Sloan AJ, Rutherford RB, Smith AJ (2000) Stimulation of the rat dentine-pulp complex by bone morphogenetic protein-7 in vitro. Archives of Oral Biology 45, 173-7.
91. Smith AJ, Scheven BA, Takahashi Y, Ferracane JL, Shelton RM, Cooper PR (2011) Dentine as a bioactive extracellular matrix. Archives of Oral Biology 57, 109-21.
92. Sonoyama W, Liu Y, Yamaza T et al. (2008) Characterization of the apical papilla and its residing stem cells from human immature permanent teeth: a pilot study. Journal of Endodontics 34, 166-71.
93. Stashenko P, Wang CY, Tani-Ishii N, Yu SM (1994) Pathogenesis of induced rat periapical lesions. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology and Endodontology 78, 494-502.
94. Stashenko P, Teles R, D'Souza R (1998) Periapical inflammatory responses and their modulation. Critical Reviews in Oral Biology & Medicine 9, 498-521.
95. Suzuki T, Lee CH, Chen M et al. (2011) Induced migration of dental pulp stem cells for in vivo pulp regeneration. Journal of Dental Research 90, 1013-8.
96. Svensäter G, Bergenholtz G (2004) Biofilms in endodontic infections. Endodontic Topics 9, 27-36.
97. Tomic S, Djokic J, Vasilijic S et al. (2011) Immunomodulatory properties of mesenchymal stem cells derived from dental pulp and dental follicle are susceptible to activation by toll-like receptor agonists. Stem Cells and Development 20, 695-708.
98. Tran-Hung L, Laurent P, Camps J, About I (2008) Quantification of angiogenic growth factors released by human dental cells after injury. Archives of Oral Biology 53, 9-13.
99. Trubiani O, Cataldi A, De Angelis F, D'Arcangelo C, Caputi S (2011) Overexpression of interleukin-6 and -8, cell growth inhibition and morphological changes in 2-hydroxyethyl methacrylate-treated human dental pulp mesenchymal stem cells. International Endodontic Journal 45, 19-25.
100. Wada N, Menicanin D, Shi S, Bartold PM, Gronthos S (2009) Immunomodulatory properties of human periodontal ligament stem cells. Journal of Cellular Physiology 219, 667-76.
101. Weinmann W, Thalacker C, Guggenberger R (2005) Siloranes in dental composites. Dental Materials 21, 68-74.
102. Yamaza T, Kentaro A, Chen C et al. (2010) Immunomodulatory properties of stem cells from human exfoliated deciduous teeth. Stem Cell Research & Therapy 1, 5.
103. Yang X, Zhang S, Pang X, Fan M (2011) Proinflammatory cytokines induce odontogenic differentiation of dental pulp derived stem cells. Journal of Cellular Biochemistry 113, 669-77.
104. Zandstra PW, Nagy A (2001) Stem cell bioengineering. Annual Review of Biomedical Engineering 3, 275-305.
105. Zehnder M, Wegehaupt FJ, Attin T (2011) A first study on the usefulness of matrix metalloproteinase 9 from dentinal fluid to indicate pulp inflammation. Journal of Endodontics 37, 17-20.
106. Zhang W, Walboomers XF, Jansen JA (2008) The formation of tertiary dentin after pulp capping with a calcium phosphate cement, loaded with plga microparticles containing tgf-beta1. Journal of Biomedical Materials Research: Part A 85, 439-44.
107. Zhou L, Chong MM, Littman DR (2009) Plasticity of cd4+ t cell lineage differentiation. Immunity 30, 646-55.