Human oral mucosa and gingiva: A unique reservoir for mesenchymal stem Cells

Journal of Dental Research

Volumn 91, Issue 11, 2012, Pages 1011-1018

  Zhang, Q Z ^a   Nguyen, A L ^b   Yu, W H ^a   Le, A D ^a,b  

^a UNIVERSITY OF PENNSYLVANIA SCHOOL OF DENTAL MEDICINE   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

gingival derived mesenchymal stem cells; immunomodulation; inflammatory disease; multipotency; oral mucosa; regeneration

Indexed keywords

ANIMAL; ARTICLE; CYTOLOGY; DENDRITIC CELL; FIBROBLAST; GINGIVA; HUMAN; IMMUNOMODULATION; INFLAMMATION; LYMPHOCYTE; MACROPHAGE; MAST CELL; MESENCHYMAL STROMA CELL; MOUTH MUCOSA; PHYSIOLOGY; REGENERATION; SIGNAL TRANSDUCTION;

ANIMALS; DENDRITIC CELLS; FIBROBLASTS; GINGIVA; HUMANS; IMMUNOMODULATION; INFLAMMATION; LYMPHOCYTES; MACROPHAGES; MAST CELLS; MESENCHYMAL STROMAL CELLS; MOUTH MUCOSA; RECEPTOR CROSS-TALK; REGENERATION;

EID: 84867699823     PISSN: 00220345     EISSN: 15440591     Source Type: Journal    
DOI: 10.1177/0022034512461016     Document Type: Article

References (68)

1. Aghajanova L, Horcajadas JA, Esteban FJ, Giudice LC. The bone marrow-derived human mesenchymal stem cell: potential progenitor of the endometrial stromal fibroblast. Biol Reprod. 2010 ; 82: 1076-1087
2. Auletta JJ, Deans RJ, Bartholomew AM. Emerging roles for multipotent, bone marrow-derived stromal cells in host defense. Blood. 2012 ; 119: 1801-1809
3. Bartosh TJ, Ylöstalo JH, Mohammadipoor A, et al. Aggregation of human mesenchymal stromal cells (MSCs) into 3D spheroids enhances their antiinflammatory properties. Proc Natl Acad Sci USA. 2010 ; 107: 13724-13729
4. Bouffi C, Bony C, Jorgensen C, Noël D. Skin fibroblasts are potent suppressors of inflammation in experimental arthritis. Ann Rheum Dis. 2011 ; 70: 1671-1676
5. Brown JB, Cheresh P, Zhang Z, Ryu H, Managlia E, Barrett TA. P-selectin glycoprotein ligand-1 is needed for sequential recruitment of T-helper 1 (Th1) and local generation of Th17 T cells in dextran sodium sulfate (DSS) colitis. Inflamm Bowel Dis. 2012 ; 18: 323-332
6. Brown JM, Nemeth K, Kushnir-Sukhov NM, Metcalfe DD, Mezey E. Bone marrow stromal cells inhibit mast cell function via a COX2-dependent mechanism. Clin Exp Allergy. 2011 ; 41: 526-534
7. Cappellesso-Fleury S, Puissant-Lubrano B, Apoil PA, Titeux M, Winterton P, Casteilla L, et al. Human fibroblasts share immunosuppressive properties with bone marrow mesenchymal stem cells. J Clin Immunol. 2010 ; 30: 607-619
8. Chiesa S, Morbelli S, Morando S, Massollo M, Marini C, Bertoni A, et al. Mesenchymal stem cells impair in vivo T-cell priming by dendritic cells. Proc Natl Acad Sci USA. 2011 ; 108: 17384-17389
9. Choi H, Lee RH, Bazhanov N, Oh JY, Prockop DJ. Anti-inflammatory protein TSG-6 secreted by activated MSCs attenuates zymosan-induced mouse peritonitis by decreasing TLR2/NF-kappaB signaling in resident macrophages. Blood. 2011 ; 118: 330-338
10. Choi YS, Jeong JA, Lim DS. Mesenchymal stem cell-mediated immature dendritic cells induce regulatory T cell-based immunosuppressive effect. Immunol Invest. 2012 ; 41: 214-229
11. Davies LC, Locke M, Webb RD, Roberts JT, Langley M, Thomas DW, et al. A multipotent neural crest-derived progenitor cell population is resident within the oral mucosa lamina propria. Stem Cells Dev. 2010 ; 19: 819-830
12. Davies LC, Lonnies H, Locke M, Sundberg B, Rosendahl K, Gotherstrom C, et al. Oral mucosal progenitor cells are potently immunosuppressive in a dose-independent manner. Stem Cells Dev. 2012 ; 21: 1478-1487
13. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006 ; 8: 315-317
14. English K, Mahon BP. Allogeneic mesenchymal stem cells: agents of immune modulation. J Cell Biochem. 2011 ; 112: 1963-1968
15. Fonacier LS, Dreskin SC, Leung DY. Allergic skin diseases. J Allergy Clin Immunol. 2010 ; 125 (2). S138 - S149
16. Fournier BP, Ferre FC, Couty L, Lataillade JJ, Gourven M, Naveau A, et al. Multipotent progenitor cells in gingival connective tissue. Tissue Eng Part A. 2010 ; 16: 2891-2899
17. Galli SJ, Borregaard N, Wynn TA. Phenotypic and functional plasticity of cells of innate immunity: macrophages, mast cells and neutrophils. Nat Immunol. 2011 ; 12: 1035-1044
18. Garlet GP. Destructive and protective roles of cytokines in periodontitis: a re-appraisal from host defense and tissue destruction viewpoints. J Dent Res. 2010 ; 89: 1349-1363
19. Gronthos S, Mankani M, Brahim J, Robey PG, Shi S. Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc Natl Acad Sci USA. 2000 ; 97: 13625-13630
20. Haniffa MA, Wang XN, Holtick U, Rae M, Isaacs JD, Dickinson AM, et al. Adult human fibroblasts are potent immunoregulatory cells and functionally equivalent to mesenchymal stem cells. J Immunol. 2007 ; 179: 1595-1604
21. Haniffa MA, Collin MP, Buckley CD, Dazzi F. Mesenchymal stem cells: the fibroblasts' new clothes?. Haematologica. 2009 ; 94: 258-263
22. Hermann A, Liebau S, Gastl R, Fickert S, Habisch HJ, Fiedler J, et al. Comparative analysis of neuroectodermal differentiation capacity of human bone marrow stromal cells using various conversion protocols. J Neurosci Res. 2006 ; 83: 1502-1514
23. Hsu SH, Huang GS, Feng F. Isolation of the multipotent MSC subpopulation from human gingival fibroblasts by culturing on chitosan membranes. Biomaterials. 2012a ; 33: 2642-2655
24. Hsu SH, Huang GS, Lin SY, Feng F, Ho TT, Liao YC. Enhanced chondrogenic differentiation potential of human gingival fibroblasts by spheroid formation on chitosan membranes. Tissue Eng Part A. 2012b ; 18: 67-79
25. Kapoor S, Patel SA, Kartan S, Axelrod D, Capitle E, Rameshwar P. Tolerance-like mediated suppression by mesenchymal stem cells in patients with dust mite allergy-induced asthma. J Allergy Clin Immunol. 2012 ; 129: 1094-1101
26. Kim J, Hematti P. Mesenchymal stem cell-educated macrophages: a novel type of alternatively activated macrophages. Exp Hematol. 2009 ; 37: 1445-1453
27. Kobayashi K, Suzuki T, Nomoto Y, Tada Y, Miyake M, Hazama A, et al. Potential of heterotopic fibroblasts as autologous transplanted cells for tracheal epithelial regeneration. Tissue Eng. 2007 ; 13: 2175-2184
28. Kobayashi K, Suzuki T, Nomoto Y, Tada Y, Miyake M, Hazama A, et al. A tissue-engineered trachea derived from a framed collagen scaffold, gingival fibroblasts and adipose-derived stem cells. Biomaterials. 2010 ; 31: 4855-4863
29. Krasnodembskaya A, Samarani G, Song Y, Zhuo H, Su X, Lee JW, et al. Human mesenchymal stem cells reduce mortality and bacteremia in Gram negative sepsis in mice in part by enhancing the phagocytic activity of blood monocytes. Am J Physiol Lung Cell Mol Physiol. 2012 ; 302: L1003 - L1013
30. Kuroda Y, Kitada M, Wakao S, Nishikawa K, Tanimura Y, Makinoshima H, et al. Unique multipotent cells in adult human mesenchymal cell populations. Proc Natl Acad Sci USA. 2010 ; 107: 8639-8643
31. Laskin DL, Sunil VR, Gardner CR, Laskin JD. Macrophages and tissue injury: agents of defense or destruction?. Annu Rev Pharmacol Toxicol. 2011 ; 51: 267-288
32. Lee CH, Shah B, Moioli EK, Mao JJ. CTGF directs fibroblast differentiation from human mesenchymal stem/stromal cells and defines connective tissue healing in a rodent injury model. J Clin Invest. 2010 ; 120: 3340-3349
33. Lee RH, Oh JY, Choi H, Bazhanov N. Therapeutic factors secreted by mesenchymal stromal cells and tissue repair. J Cell Biochem. 2011 ; 112: 3073-3078
34. Lorenz K, Sicker M, Schmelzer E, et al. Multilineage differentiation potential of human dermal skin-derived fibroblasts. Exp Dermatol. 2008 ; 17: 925-932
35. Luria EA, Panasyuk AF, Friedenstein AY. Fibroblast colony formation from monolayer cultures of blood cells. Transfusion. 1971 ; 11: 345-349
36. Lysy PA, Smets F, Sibille C, Najimi M, Sokal EM. Human skin fibroblasts: from mesodermal to hepatocyte-like differentiation. Hepatology. 2007 ; 46: 1574-1585
37. Maggini J, Mirkin G, Bognanni I, Holmberg J, Piazzon IM, Nepomnaschy I, et al. Mouse bone marrow-derived mesenchymal stromal cells turn activated macrophages into a regulatory-like profile. PLoS One. 2010 ; 5: e9252
38. Marynka-Kalmani K, Treves S, Yafee M, Rachima H, Gafni Y, Cohen MA, et al. The lamina propria of adult human oral mucosa harbors a novel stem cell population. Stem Cells. 2010 ; 28: 984-995
39. Mitrano TI, Grob MS, Carrion F, Nova-Lamperti E, Luz PA, Fierro FS, et al. Culture and characterization of mesenchymal stem cells from human gingival tissue. J Periodontol. 2010 ; 81: 917-925
40. Miura M, Gronthos S, Zhao M, Lu B, Fisher LW, Robey PG, et al. SHED: stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci USA. 2003 ; 100: 5807-5812
41. Mostafa NZ, Uluda? H, Varkey M, Dederich DN, Doschak MR, El-Bialy TH. In vitro osteogenic induction of human gingival fibroblasts for bone regeneration. Open Dent J. 2011 ; 5: 139-145
42. Nakajima H, Uchida K, Guerrero AR, Watanabe S, Sugita D, Takeura N, et al. Transplantation of mesenchymal stem cells promotes an alternative pathway of macrophage activation and functional recovery after spinal cord injury. J Neurotrauma. 2012 ; 29: 1614-1625
43. Nakajima K, Abe T, Tanaka M, Hara Y. Periodontal tissue engineering by transplantation of multilayered sheets of phenotypically modified gingival fibroblasts. J Periodontal Res. 2008 ; 43: 681-688
44. Nakasone N, Kubota T, Hoshino C, Nohno K, Itagaki M, Shimizu T, et al. Differential gene and protein expression of tissue inhibitors of metalloproteinases (TIMP)-3 and TIMP-4 in gingival tissues from drug induced gingival overgrowth. Arch Oral Biol. 2009 ; 54: 634-641
45. Nemeth K, Leelahavanichkul A, Yuen PS, Mayer B, Parmelee A, Doi K, et al. Bone marrow stromal cells attenuate sepsis via prostaglandin E(2)-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat Med. 2009 ; 15: 42-49
46. Nishi H, Ohta K, Takechi M, Yoneda S, Hiraoka M, Kamata N. Wound healing effects of gingival fibroblasts cultured in animal-free medium. Oral Dis. 2010 ; 16: 438-444
47. Nombela-Arrieta C, Ritz J, Silberstein LE. The elusive nature and function of mesenchymal stem cells. Nat Rev Mol Cell Biol. 2011 ; 12: 126-131
48. Pinchuk IV, Beswick EJ, Saada JI, Boya G, Schmitt D, Raju GS, et al. Human colonic myofibroblasts promote expansion of CD4(+) CD25(high) Foxp3(+) regulatory T cells. Gastroenterology. 2011 ; 140: 2019-2030
49. Prockop DJ. Repair of tissues by adult stem/progenitor cells (MSCs): controversies, myths, and changing paradigms. Mol Ther. 2009 ; 17: 939-946
50. Prockop DJ, Oh JY. Mesenchymal stem/stromal cells (MSCs): role as guardians of inflammation. Mol Ther. 2012 ; 20: 14-20
51. Roddy GW, Oh JY, Lee RH, Bartosh TJ, Ylostalo J, Coble K, et al. Action at a distance: systemically administered adult stem/progenitor cells (MSCs) reduce inflammatory damage to the cornea without engraftment and primarily by secretion of TNF-alpha stimulated gene/protein 6. Stem Cells. 2011 ; 29: 1572-1579
52. Sahoo S, Toh SL, Goh JC. A bFGF-releasing silk/PLGA-based biohybrid scaffold for ligament/tendon tissue engineering using mesenchymal progenitor cells. Biomaterials. 2010 ; 31: 2990-2998
53. Salem HK, Thiemermann C. Mesenchymal stromal cells: current understanding and clinical status. Stem Cells. 2010 ; 28: 585-596
54. Sayed BA, Christy A, Quirion MR, Brown MA. The master switch: the role of mast cells in autoimmunity and tolerance. Annu Rev Immunol. 2008 ; 26: 705-739
55. Spaggiari GM, Abdelrazik H, Becchetti F, Moretta L. MSCs inhibit monocyte-derived DC maturation and function by selectively interfering with the generation of immature DCs: central role of MSC-derived prostaglandin E2. Blood. 2009 ; 113: 6576-6583
56. Stephens P, Genever P. Non-epithelial oral mucosal progenitor cell populations. Oral Dis. 2007 ; 13: 1-10
57. Su WR, Zhang QZ, Shi SH, Nguyen AL, Le AD. Human gingiva-derived mesenchymal stromal cells attenuate contact hypersensitivity via prostaglandin E(2)-dependent mechanisms. Stem Cells. 2011 ; 29: 1849-1860
58. Sudo K, Kanno M, Miharada K, Ogawa S, Hiroyama T, Saijo K, et al. Mesenchymal progenitors able to differentiate into osteogenic, chondrogenic, and/or adipogenic cells in vitro are present in most primary fibroblast-like cell populations. Stem Cells. 2007 ; 25: 1610-1617
59. Tang L, Li N, Xie H, Jin Y. Characterization of mesenchymal stem cells from human normal and hyperplastic gingiva. J Cell Physiol. 2011 ; 226: 832-842
60. Tasso R, Gaetani M, Molino E, et al. The role of bFGF on the ability of MSC to activate endogenous regenerative mechanisms in an ectopic bone formation model. Biomaterials. 2012 ; 33: 2086-2096
61. 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: 377-383
62. Vocanson M, Hennino A, Rozieres A, Poyet G, Nicolas JF. Effector and regulatory mechanisms in allergic contact dermatitis. Allergy. 2009 ; 64: 1699-1714
63. Wada N, Menicanin D, Shi S, Bartold PM, Gronthos S. Immunomodulatory properties of human periodontal ligament stem cells. J Cell Physiol. 2009 ; 219: 667-676
64. Wada N, Bartold PM, Gronthos S. Human foreskin fibroblasts exert immunomodulatory properties by a different mechanism to bone marrow stromal/stem cells. Stem Cells Dev. 2011 ; 20: 647-659
65. Wang F, Yu M, Yan X, Wen Y, Zeng Q, Yue W, et al. Gingiva-derived mesenchymal stem cell-mediated therapeutic approach for bone tissue regeneration. Stem Cells Dev. 2011 ; 20: 2093-2102
66. Zhang Q, Shi S, Liu Y, Uyanne J, Shi Y, Shi S, et al. Mesenchymal stem cells derived from human gingiva are capable of immunomodulatory functions and ameliorate inflammation-related tissue destruction in experimental colitis. J Immunol. 2009 ; 183: 7787-7798
67. Zhang Q, Su WR, Shi SH, Wilder-Smith P, Xiang AP, Wong A, et al. Human gingiva-derived mesenchymal stem cells elicit polarization of m2 macrophages and enhance cutaneous wound healing. Stem Cells. 2010 ; 28: 1856-1868
68. Zhang Q, Nguyen AL, Shi S, Hill C, Wilder-Smith P, Krasieva TB, et al. Three-dimensional spheroid culture of human gingiva-derived mesenchymal stem cells enhances mitigation of chemotherapy-induced oral mucositis. Stem Cells Dev. 2011 ; 21: 937-947