Controversial role of toll-like receptor 4 in adult stem cells

Stem Cell Reviews and Reports

Volumn 11, Issue 4, 2015, Pages 621-634

  Zeuner, Marie ^a   Bieback, Karen ^b   Widera, Darius ^a  

^a UNIVERSITY OF READING   (United Kingdom)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Adult StemCells; DAMPs; Hematopoietic StemCells; IRF3; LPS; Mesenchymal StemCells; Neural Stem Cells; NF kappaB; PAMPs; TLR4

Indexed keywords

BETA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR 4; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; TUMOR NECROSIS FACTOR ALPHA; TLR4 PROTEIN, HUMAN;

ADULT STEM CELL; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; DENTAL PULP STEM CELL; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IMMUNOMODULATION; MESENCHYMAL STEM CELL; MYELOPOIESIS; NEURAL STEM CELL; NONHUMAN; PERIODONTAL STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STELLATE CELL; ADULT; BIOLOGICAL MODEL; CELL MOTION; METABOLISM; PHYSIOLOGY;

ADULT; ADULT STEM CELLS; CELL DIFFERENTIATION; CELL MOVEMENT; CELL PROLIFERATION; HUMANS; LIPOPOLYSACCHARIDES; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4;

EID: 84941924565     PISSN: 15508943     EISSN: 15586804     Source Type: Journal    
DOI: 10.1007/s12015-015-9589-5     Document Type: Article

References (127)

1. Anderson, K. V., Jürgens, G., & Nüsslein-Volhard, C. (1985). Establishment of dorsal-ventral polarity in the Drosophila embryo: Genetic studies on the role of the Toll gene product. Cell, 42, 779-789.
2. Morisato, D., & Anderson, K. V. (1994). The spatzle gene encodes a component of the extracellular signaling pathway establishing the dorsal-ventral pattern of the Drosophila embryo. Cell, 76, 677-688.
3. Lemaitre, B., Nicolas, E., Michaut, L., Reichhart, J. M., & Hoffmann, J. A. (1996). The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell, 86, 973-983.
4. Ozinsky, A., Underhill, D. M., Fontenot, J. D., et al. (2000). The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between Toll-like receptors. Proceedings of the National Academy of Sciences of the United States of America, 97, 13766-13771.
5. Miyake, K. (2007). Innate immune sensing of pathogens and danger signals by cell surface Toll-like receptors. Seminars in Immunology, 19, 3-10.
6. Botos, I., Segal David, M., & Davies David, R. (2011). The structural biology of Toll-like receptors. Structure, 19, 447-459.
7. Chow, J. C., Young, D. W., Golenbock, D. T., Christ, W. J., & Gusovsky, F. (1999). Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction. Journal of Biological Chemistry, 274, 10689-10692.
8. Abreu, M. T., Vora, P., Faure, E., Thomas, L. S., Arnold, E. T., & Arditi, M. (2001). Decreased expression of Toll-like receptor-4 and MD-2 correlates with intestinal epithelial cell protection against dysregulated proinflammatory gene expression in response to bacterial lipopolysaccharide. Journal of Immunology, 167, 1609-1616.
9. Frantz, S., Kobzik, L., Kim, Y. D., et al. (1999). Toll4 (TLR4) expression in cardiac myocytes in normal and failing myocardium. Journal of Clinical Investigation, 104, 271-280.
10. Lehnardt, S., Lachance, C., Patrizi, S., et al. (2002). The Toll-like receptor TLR4 is necessary for lipopolysaccharide-induced oligodendrocyte injury in the CNS. Journal of Neuroscience, 22, 2478-2486.
11. Olson, J. K., & Miller, S. D. (2004). Microglia initiate central nervous system innate and adaptive immune responses through multiple TLRs. Journal of Immunology, 173, 3916-3924.
12. Bowman, C. C., Rasley, A., Tranguch, S. L., & Marriott, I. (2003). Cultured astrocytes express Toll-like receptors for bacterial products. Glia, 43, 281-291.
13. Tang, S. C., Arumugam, T. V., Xu, X., et al. (2007). Pivotal role for neuronal Toll-like receptors in ischemic brain injury and functional deficits. Proceedings of the National Academy of Sciences of the United States of America, 104, 13798-13803.
14. Tang, S. C., Lathia, J. D., Selvaraj, P. K., et al. (2008). Toll-like receptor-4 mediates neuronal apoptosis induced by amyloid betapeptide and the membrane lipid peroxidation product 4-hydroxynonenal. Experimental Neurology, 213, 114-121.
15. Esplin, B. L., Shimazu, T., Welner, R. S., et al. (2011). Chronic exposure to a TLR ligand injures hematopoietic stem cells. Journal of Immunology, 186, 5367-5375.
16. He, J., Xiao, Z., Chen, X., et al. (2010). The expression of functional Toll-like receptor 4 is associated with proliferation and maintenance of stemcell phenotype in endothelial progenitor cells (EPCs). Journal of Cellular Biochemistry, 111, 179-186.
17. Li, C., Li, B., Dong, Z., et al. (2014). Lipopolysaccharide differentially affects the osteogenic differentiation of periodontal ligament stem cells and bone marrow mesenchymal stem cells through Toll-like receptor 4 mediated nuclear factor kappa B pathway. Stem Cell Research & Therapy, 5, 67.
18. Hwang, S. H., Cho, H. K., Park, S. H., et al. (2014). Toll like receptor 3 & 4 responses of human turbinate derived mesenchymal stemcells: stimulation by double stranded RNA and lipopolysaccharide. PloS One, 9, e101558.
19. Raicevic, G., Rouas, R., Najar, M., et al. (2010). Inflammation modifies the pattern and the function of Toll-like receptors expressed by human mesenchymal stromal cells. Human Immunology, 71, 235-244.
20. He, W., Wang, Z., Luo, Z., et al. (2015). LPS promote the odontoblastic differentiation of human dental pulp stem cells via MAPK signaling pathway. Journal of Cellular Physiology, 230, 554-561.
21. Shechter, R., Ronen, A., Rolls, A., et al. (2008). Toll-like receptor 4 restricts retinal progenitor cell proliferation. Journal of Cell Biology, 183, 393-400.
22. Rolls, A., Shechter, R., London, A., et al. (2007). Toll-like receptors modulate adult hippocampal neurogenesis. Nature Cell Biology, 9, 1081-1088.
23. Okun, E., Barak, B., Saada-Madar, R., et al. (2012). Evidence for a developmental role for TLR4 in learning and memory. PloS One, 7, e47522.
24. Pradillo, J. M., Fernandez-Lopez, D., Garcia-Yebenes, I., et al. (2009). Toll-like receptor 4 is involved in neuroprotection afforded by ischemic preconditioning. Journal of Neurochemistry, 109, 287-294.
25. Okun, E., Griffioen, K. J., & Mattson, M. P. (2011). Toll-like receptor signaling in neural plasticity and disease. Trends in Neurosciences, 34, 269-281.
26. Mai, C. W., Kang, Y. B., & Pichika, M. R. (2013). Should a Tolllike receptor 4 (TLR-4) agonist or antagonist be designed to treat cancer? TLR-4: its expression and effects in the ten most common cancers. Onco Targets and therapy, 6, 1573-1587.
27. Watanabe, S., Kumazawa, Y., & Inoue, J. (2013). Liposomal lipopolysaccharide initiates TRIF-dependent signaling pathway independent of CD14. PloS One, 8, e60078.
28. Marsh, B. J., Williams-Karnesky, R. L., & Stenzel-Poore, M. P. (2009). Toll-like receptor signaling in endogenous neuroprotection and stroke. Neuroscience, 158, 1007-1020.
29. Raetz, C. R. H., & Whitfield, C. (2002). Lipopolysaccharide endotoxins. Annual Review of Biochemistry, 71, 635-700.
30. Galanos, C., LÜDeritz, O., Rietschel, E. T., et al. (1985). Synthetic and natural Escherichia coli free lipid A express identical endotoxic activities. European Journal of Biochemistry, 148, 1-5.
31. Si, S. (2004). Akashi S, Yamada T, et al. Lipid A antagonist, lipid IVa, is distinct from lipid A in interaction with Toll-like receptor 4 (TLR4)-MD-2 and ligand-induced TLR4 oligomerization. International Immunology, 16, 961-969.
32. Rietschel, E., Wollenweber, H.-W., Zähringer, U., & Lüderitz, O. (1982). Lipid A, the lipid component of bacterial lipopolysaccharides: Relation of chemical structure to biological activity. Klinische Wochenschrift, 60, 705-709.
33. Gutschow, M. V., Hughey, J. J., Ruggero, N. A., Bajar, B. T., Valle, S. D., & Covert, M. W. (2013). Single-cell and population NF-kappaB dynamic responses depend on lipopolysaccharide preparation. PloS One, 8, e53222.
34. Miller, S. I., Ernst, R. K., & Bader, M.W. (2005). LPS, TLR4 and infectious disease diversity. Nature Reviews Microbiology, 3, 36-46.
35. Sloane, J. A., Blitz, D., Margolin, Z., & Vartanian, T. (2010). A clear and present danger: endogenous ligands of Toll-like receptors. Neuromolecular Medicine, 12, 149-163.
36. Erridge, C. (2010). Endogenous ligands of TLR2 and TLR4: agonists or assistants? Journal of Leukocyte Biology, 87, 989-999.
37. Mendelson, A., & Frenette, P. S. (2014). Hematopoietic stem cell niche maintenance during homeostasis and regeneration. Nature Medicine, 20, 833-846.
38. Boiko, J. R., & Borghesi, L. (2012). Hematopoiesis sculpted by pathogens: Toll-like receptors and inflammatory mediators directly activate stem cells. Cytokine, 57, 1-8.
39. Nagai, Y., Garrett, K. P., Ohta, S., et al. (2006). Toll-like receptors on hematopoietic progenitor cells stimulate innate immune system replenishment. Immunity, 24, 801-812.
40. Ichii, M., Shimazu, T., Welner, R. S., et al. (2010). Functional diversity of stem and progenitor cells with B-lymphopoietic potential. Immunology Reviews, 237, 10-21.
41. Burberry, A., Zeng, M. Y., Ding, L., et al. (2014). Infection mobilizes hematopoietic stem cells through cooperative NOD-like receptor and Toll-like receptor signaling. Cell Host & Microbe, 15, 779-791.
42. Baldridge, M. T., King, K. Y., & Goodell, M. A. (2011). Inflammatory signals regulate hematopoietic stem cells. Trends in Immunology, 32, 57-65.
43. Chambers, S. M., Shaw, C. A., Gatza, C., Fisk, C. J., Donehower, L. A., & Goodell, M. A. (2007). Aging hematopoietic stem cells decline in function and exhibit epigenetic dysregulation. PLoS Biology, 5, e201.
44. Boettcher, S., Ziegler, P., Schmid, M. A., et al. (2012). Cutting edge: LPS-induced emergency myelopoiesis depends on TLR4-expressing nonhematopoietic cells. Journal of Immunology, 188, 5824-5828.
45. Megias, J., Yanez, A., Moriano, S., O'Connor, J. E., Gozalbo, D., & Gil, M. L. (2012). Direct Toll-like receptor-mediated stimulation of hematopoietic stem and progenitor cells occurs in vivo and promotes differentiation toward macrophages. Stem Cells, 30, 1486-1495.
46. Shi, X., Siggins, R.W., Stanford, W. L., Melvan, J. N., Basson, M. D., & Zhang, P. (2013). Toll-like receptor 4/stem cell antigen 1 signaling promotes hematopoietic precursor cell commitment to granulocyte development during the granulopoietic response to Escherichia coli bacteremia. Infection and Immunity, 81, 2197-2205.
47. Pittenger, M. F., Mackay, A. M., Beck, S. C., et al. (1999). Multilineage potential of adult human mesenchymal stem cells. Science, 284, 143-147.
48. Zuk, P. A., Zhu, M., Ashjian, P., et al. (2002). Human adipose tissue is a source of multipotent stem cells. Molecular Biology of the Cell, 13, 4279-4295.
49. Delorme, B., Nivet, E., Gaillard, J., et al. (2010). The human nose harbors a niche of olfactory ectomesenchymal stem cells displaying neurogenic and osteogenic properties. Stem Cells and Development, 19, 853-866.
50. Diaz-Solano, D., Wittig, O., Ayala-Grosso, C., Pieruzzini, R., & Cardier, J. E. (2012). Human olfactory mucosa multipotent mesenchymal stromal cells promote survival, proliferation, and differentiation of human hematopoietic cells. Stem Cells and Development, 21, 3187-3196.
51. Hwang, S. H., Kim, S. Y., Park, S. H., et al. (2012). Human inferior turbinate: an alternative tissue source of multipotent mesenchymal stromal cells. Otolaryngology and Head and Neck Surgery, 147, 568-574.
52. Crisan, M., Yap, S., Casteilla, L., et al. (2008). A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell, 3, 301-313.
53. 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, 315-317.
54. Salem, H. K., & Thiemermann, C. (2010). Mesenchymal stromal cells: current understanding and clinical status. Stem Cells, 28, 585-596.
55. Lalu, M.M., McIntyre, L., Pugliese, C., et al. (2012). Safety of cell therapy with mesenchymal stromal cells (SafeCell): a systematic review and meta-analysis of clinical trials. PloS One, 7, e47559.
56. Kinzebach, S., & Bieback, K. (2013). Expansion of Mesenchymal Stem/Stromal cells under xenogenic-free culture conditions. Advances in Biochemical Engineering/Biotechnology, 129, 33-57.
57. Sharma, R. R., Pollock, K., Hubel, A., & McKenna, D. (2014). Mesenchymal stem or stromal cells: a review of clinical applications and manufacturing practices. Transfusion, 54, 1418-1437.
58. Prockop, D. J. (2007). BStemness^ does not explain the repair of many tissues by mesenchymal stem/multipotent stromal cells (MSCs). Clinical Pharmacology and Therapeutics, 82, 241-243.
59. Bieback, K., Wuchter, P., Besser, D., et al. (2012). Mesenchymal stromal cells (MSCs): science and f (r)iction. Journal of Molecular Medicine (Berl), 90, 773-782.
60. Maumus, M., Jorgensen, C., & Noel, D. (2013). Mesenchymal stem cells in regenerative medicine applied to rheumatic diseases: role of secretome and exosomes. Biochimie, 95, 2229-2234.
61. van den Akker, F., de Jager, S. C., & Sluijter, J. P. (2013). Mesenchymal stem cell therapy for cardiac inflammation: immunomodulatory properties and the influence of Toll-like receptors. Mediators of Inflammation, 2013, 181020.
62. Kyurkchiev, D., Bochev, I., Ivanova-Todorova, E., et al. (2014). Secretion of immunoregulatory cytokines by mesenchymal stem cells. World Journal Stem Cells, 6, 552-570.
63. Liotta, F., Angeli, R., Cosmi, L., et al. (2008). Toll-like receptors 3 and 4 are expressed by human bone marrow-derived mesenchymal stem cells and can inhibit their T-cell modulatory activity by impairing Notch signaling. Stem Cells, 26, 279-289.
64. Shi, L., Wang, J. S., Liu, X. M., Hu, X. Y., & Fang, Q. (2007). Upregulated functional expression of Toll like receptor 4 in mesenchymal stem cells induced by lipopolysaccharide. Chinese Medical Journal, 120, 1685-1688.
65. Pevsner-Fischer, M., Morad, V., Cohen-Sfady, M., e t al. (2007). Toll-like receptors and their ligands control mesenchymal stem cell functions. Blood, 109, 1422-1432.
66. Opitz, C. A., Litzenburger, U.M., Lutz, C., et al. (2009). Toll-like receptor engagement enhances the immunosuppressive properties of human bone marrow-derived mesenchymal stem cells by inducing indoleamine-2,3-dioxygenase-1 via interferon-beta and protein kinase R. Stem Cells, 27, 909-919.
67. Yan, H., Wu, M., Yuan, Y., Wang, Z. Z., Jiang, H., & Chen, T. (2014). Priming of Toll-like receptor 4 pathway in mesenchymal stem cells increases expression of B cell activating factor. Biochemical and Biophysical Research Communications, 448, 212-217.
68. Chen, X., Zhang, Z. Y., Zhou, H., & Zhou, G. W. (2014). Characterization of mesenchymal stem cells under the stimulation of Toll-like receptor agonists. Development, Growth & Differentiation, 56, 233-244.
69. Zhang, L., Liu, D., Pu, D., et al. (2015). The role of Toll-like receptor 3 and 4 in regulating the function of mesenchymal stem cells isolated from umbilical cord. International Journal of Molecular Medicine, 35, 1003-1010.
70. DelaRosa, O., & Lombardo, E. (2010). Modulation of adult mesenchymal stem cells activity by Toll-like receptors: implications on therapeutic potential. Mediators of Inflammation, 2010, 865601.
71. Wang, Z. J., Zhang, F. M., Wang, L. S., Yao, Y. W., Zhao, Q., & Gao, X. (2009). Lipopolysaccharides can protect mesenchymal stem cells (MSCs) from oxidative stress-induced apoptosis and enhance proliferation of MSCs via Toll-like receptor (TLR)-4 and PI3K/Akt. Cell Biology International, 33, 665-674.
72. Giuliani, M., Bennaceur-Griscelli, A., Nanbakhsh, A., et al. (2014). TLR ligands stimulation protects MSC from NK killing. Stem Cells, 32, 290-300.
73. Mei, Y. B., Zhou, W. Q., Zhang, X. Y., Wei, X. J., & Feng, Z. C. (2013). Lipopolysaccharides shapes the human Whartons jellyderived mesenchymal stem cells in vitro. Cellular Physiology and Biochemistry, 32, 390-401.
74. Hwa Cho, H., Bae, Y. C., & Jung, J. S. (2006). Role of Toll-like receptors on human adipose-derived stromal cells. Stem Cells, 24, 2744-2752.
75. Mo, I. F., Yip, K. H., Chan, W. K., Law, H. K., Lau, Y. L., & Chan, G. C. (2008). Prolonged exposure to bacterial toxins downregulated expression of Toll-like receptors in mesenchymal stromal cell-derived osteoprogenitors. BMC Cell Biology, 9, 52.
76. Wang, Y., Abarbanell, A.M., Herrmann, J. L., et al. (2010). TLR4 inhibits mesenchymal stem cell (MSC) STAT3 activation and thereby exerts deleterious effects on MSC-mediated cardioprotection. PloS One, 5, e14206.
77. Raicevic, G., Najar, M., Pieters, K., et al. (2012). Inflammation and Toll-like receptor ligation differentially affect the osteogenic potential of human mesenchymal stromal cells depending on their tissue origin. Tissue Engineering Part A, 18, 1410-1418.
78. Lei, J., Wang, Z., Hui, D., et al. (2011). Ligation of TLR2 and TLR4 on murine bone marrow-derived mesenchymal stem cells triggers differential effects on their immunosuppressive activity. Cellular Immunology, 271, 147-156.
79. Tomchuck, S. L., Zwezdaryk, K. J., Coffelt, S. B., Waterman, R. S., Danka, E. S., & Scandurro, A. B. (2008). Toll-like receptors on human mesenchymal stem cells drive their migration and immunomodulating responses. Stem Cells, 26, 99-107.
80. Lombardo, E., DelaRosa, O., Mancheno-Corvo, P., Menta, R., Ramirez, C., & Buscher, D. (2009). Toll-like receptor-mediated signaling in human adipose-derived stem cells: implications for immunogenicity and immunosuppressive potential. Tissue Engineering Part A, 15, 1579-1589.
81. 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.
82. Covacu, R., Arvidsson, L., Andersson, Å., et al. (2009). TLR Activation Induces TNF-α Production from Adult Neural Stem/Progenitor Cells. The Journal of Immunology, 182, 6889-6895.
83. Schuster, A., Klotz, M., Schwab, T., et al. (2014). Maintenance of the enteric stem cell niche by bacterial lipopolysaccharides? Evidence and perspectives. Journal of Cellular and Molecular Medicine, 18, 1429-1443.
84. Su, Y., Zhang, Z., Trautmann, K., Xu, S., & Schluesener, H. J. (2005). TLR and NOD2 ligands induce cell proliferation in the rat intact spinal cord. Journal of Neuropathology and Experimental Neurology, 64, 991-997.
85. Wu, J. P., Kuo, J. S., Liu, Y. L., & Tzeng, S. F. (2000). Tumor necrosis factor-alpha modulates the proliferation of neural progenitors in the subventricular/ventricular zone of adult rat brain. Neuroscience Letters, 292, 203-206.
86. Wong, G., Goldshmit, Y., & Turnley, A. M. (2004). Interferongamma but not TNF alpha promotes neuronal differentiation and neurite outgrowth of murine adult neural stem cells. Experimental Neurology, 187, 171-177.
87. Widera, D., Mikenberg, I., Elvers, M., Kaltschmidt, C., & Kaltschmidt, B. (2006). Tumor necrosis factor alpha triggers proliferation of adult neural stemcells via IKK/NF-kappaB signaling. BMC Neuroscience, 7, 64.
88. Rubio-Araiz, A., Arevalo-Martin, A., Gomez-Torres, O., et al. (2008). The endocannabinoid system modulates a transient TNF pathway that induces neural stemcell proliferation. Molecular and Cellular Neuroscience, 38, 374-380.
89. Tarassishin, L., Bauman, A., Suh, H. S., & Lee, S. C. (2013). Antiviral and anti-inflammatory mechanisms of the innate immune transcription factor interferon regulatory factor 3: relevance to human CNS diseases. Journal of Neuroimmune Pharmacology, 8, 132-144.
90. Lum, M., Croze, E., Wagner, C., McLenachan, S., Mitrovic, B., & Turnley, A. M. (2009). Inhibition of neurosphere proliferation by IFNgamma but not IFNbeta is coupled to neuronal differentiation. Journal of Neuroimmunology, 206, 32-38.
91. Cacci, E., Claasen, J. H., & Kokaia, Z. (2005). Microglia-derived tumor necrosis factor-alpha exaggerates death of newborn hippocampal progenitor cells in vitro. Journal of Neuroscience Research, 80, 789-797.
92. Koo, J.W., Russo, S. J., Ferguson, D., Nestler, E. J., & Duman, R. S. (2010). Nuclear factor-kappaB is a critical mediator of stressimpaired neurogenesis and depressive behavior. Proceedings of the National Academy of Sciences of the United States of America, 107, 2669-2674.
93. Martino, G., & Pluchino, S. (2007). Neural stem cells: guardians of the brain. Nature Cell Biology, 9, 1031-1034.
94. Wang, P. P., Xie, D. Y., Liang, X. J., et al. (2012). HGF and direct mesenchymal stem cells contact synergize to inhibit hepatic stellate cells activation through TLR4/NF-kB pathway. PloS One, 7, e43408.
95. Edelman, D. A., Jiang, Y., Tyburski, J. G., Wilson, R. F., & Steffes, C. P. (2007). Cytokine production in lipopolysaccharideexposed rat lung pericytes. Journal of Trauma, 62, 89-93.
96. Guijarro-Munoz, I., Compte, M., Alvarez-Cienfuegos, A., Alvarez-Vallina, L., & Sanz, L. (2014). Lipopolysaccharide activates Toll-like receptor 4 (TLR4)-mediated NF-kappaB signaling pathway and proinflammatory response in human pericytes. Journal of Biological Chemistry, 289, 2457-2468.
97. Xiao, Z., Yang, M., Fang, L., et al. (2012). Extracellular nucleotide inhibits cell proliferation and negatively regulates Toll-like receptor 4 signalling in human progenitor endothelial cells. Cell Biology International, 36, 625-633.
98. Yamada, M., Kubo, H., Ishizawa, K., Kobayashi, S., Shinkawa, M., & Sasaki, H. (2005). Increased circulating endothelial progenitor cells in patients with bacterial pneumonia: evidence that bone marrow derived cells contribute to lung repair. Thorax, 60, 410-413.
99. Mao, S. Z., Ye, X., Liu, G., Song, D., & Liu, S. F. (2014). An obligatory role of NF-kappaB in mediating bone marrow derived endothelial progenitor cell recruitment and proliferation following endotoxemic multiple organ injury in mice. PloS One, 9, e111087.
100. Neal, M. D., Sodhi, C. P., Jia, H., et al. (2012). Toll-like receptor 4 is expressed on intestinal stem cells and regulates their proliferation and apoptosis via the p53 up-regulated modulator of apoptosis. Journal of Biological Chemistry, 287, 37296-37308.
101. He, W., Qu, T., Yu, Q., et al. (2013). LPS induces IL-8 expression through TLR4, MyD 88, NF-kappaB and MAPK pathways in human dental pulp stem cells. International Endodontic Journal, 46, 128-136.
102. He, W., Wang, Z., Zhou, Z., et al. (2014). Lipopolysaccharide enhances Wnt5a expression through Toll-like receptor 4, myeloid differentiating factor 88, phosphatidylinositol 3-OH kinase/AKT and nuclear factor kappa B pathways in human dental pulp stem cells. Journal of Endodontia, 40, 69-75.
103. Li, D., Fu, L., Zhang, Y., et al. (2014). The effects of LPS on adhesion and migration of human dental pulp stem cells in vitro. Journal of Dentistry, 42, 1327-1334.
104. Feng, X., Feng, G., Xing, J., et al. (2014). Repeated lipopolysaccharide stimulation promotes cellular senescence in human dental pulp stemcells (DPSCs). Cell and Tissue Research, 356, 369-380.
105. Kim, J. C., Lee, Y. H., Yu, M. K., et al. (2012). Anti-inflammatory mechanismof PPARgamma on LPS-induced pulp cells: role of the ROS removal activity. Archives of Oral Biology, 57, 392-400.
106. Chatzivasileiou, K., Lux, C. A., Steinhoff, G., & Lang, H. (2013). Dental follicle progenitor cells responses to Porphyromonas gingivalis LPS. Journal of Cellular and Molecular Medicine, 17, 766-773.
107. Zhang, J., Zhang, Y., Lv, H., et al. (2013). Human stem cells from the apical papilla response to bacterial lipopolysaccharide exposure and anti-inflammatory effects of nuclear factor I C. Journal of Endodontia, 39, 1416-1422.
108. Chamila Prageeth Pandula, P. K., Samaranayake, L. P., Jin, L. J., & Zhang, C. (2014). Periodontal ligament stem cells: an update and perspectives. Journal of Investigative and Clinical Dentistry, 5, 81-90.
109. Widera, D., Grimm, W. D., Moebius, J. M., et al. (2007). Highly efficient neural differentiation of human somatic stem cells, isolated by minimally invasive periodontal surgery. Stem Cells and Development, 16, 447-460.
110. Osathanon, T., Manokawinchoke, J., Nowwarote, N., Aguilar, P., Palaga, T., & Pavasant, P. (2013). Notch signaling is involved in neurogenic commitment of human periodontal ligament-derived mesenchymal stem cells. Stem Cells and Development, 22, 1220-1231.
111. Huang, L., Liang, J., Geng, Y., et al. (2013).Directing adult human periodontal ligament-derived stem cells to retinal fate. Investigative Ophthalmology & Visual Science, 54, 3965-3974.
112. Lee, J. H., Um, S., Song, I. S., Kim, H. Y., & Seo, B. M. (2014). Neurogenic differentiation of human dental stem cells in vitro. Journal Korean Association Oral Maxillofacial Surgery, 40, 173-180.
113. Kato, H., Taguchi, Y., Tominaga, K., Umeda, M., & Tanaka, A. (2014). Porphyromonas gingivalis LPS inhibits osteoblastic differentiation and promotes pro-inflammatory cytokine production in human periodontal ligament stem cells. Archives of Oral Biology, 59, 167-175.
114. Paik, Y. H., Schwabe, R. F., Bataller, R., Russo, M. P., Jobin, C., & Brenner, D. A. (2003). Toll-like receptor 4 mediates inflammatory signaling by bacterial lipopolysaccharide in human hepatic stellate cells. Hepatology, 37, 1043-1055.
115. Wang, X. B., Chen, X., Song, K. D., et al. (2010). Effects of HMGB1 on human cord blood CD34 (+) hematopoietic stem cells proliferation and differentiation in vitro. Zhonghua Xue Ye Xue Za Zhi, 31, 88-91.
116. Monzen, S., Yoshino, H., Kasai-Eguchi, K., & Kashiwakura, I. (2013). Characteristics of myeloid differentiation and maturation pathway derived from human hematopoietic stem cells exposed to different linear energy transfer radiation types. PloS One, 8, e59385 117.
117. Levin, S., Pevsner-Fischer, M., Kagan, S., et al. (2014). Divergent levels of LBP and TGFbeta1 in murine MSCs lead to heterogenic response to TLR and proinflammatory cytokine activation. Stem Cell Reviews, 10, 376-388.
118. Xu, J., Woods, C. R., Mora, A. L., et al. (2007). Prevention of endotoxin-induced systemic response by bone marrow-derived mesenchymal stem cells in mice. American Journal of Physiology-Lung Cellular and Molecular Physiology, 293, L131-L141.
119. Xu, S., De Becker, A., Van Camp, B., Vanderkerken, K., & Van Riet, I. (2010). An improved harvest and in vitro expansion protocol for murine bone marrow-derived mesenchymal stem cells. Journal of Biomedicine and Biotechnology, 2010, 105940.
120. Huh, J. E., & Lee, S. Y. (1833). IL-6 is produced by adiposederived stromal cells and promotes osteogenesis. Biochimica et Biophysica Acta, 2013, 2608-2616.
121. Secunda, R., Vennila, R., Mohanashankar, A. M., Rajasundari, M., Jeswanth, S., Surendran, R. (2014). Isolation, expansion and characterisation of mesenchymal stem cells from human bone marrow, adipose tissue, umbilical cord blood and matrix: a comparative study. Cytotechnology. doi: 10.1007/s10616-014-9718-z.
122. Al-Nbaheen, M., Vishnubalaji, R., Ali, D., et al. (2013). Human stromal (mesenchymal) stem cells from bone marrow, adipose tissue and skin exhibit differences in molecular phenotype and differentiation potential. Stem Cell Reviews, 9, 32-43.
123. Raicevic, G., Najar, M., Stamatopoulos, B., et al. (2011). The source of human mesenchymal stromal cells influences their TLR profile as well as their functional properties. Cellular Immunology, 270, 207-216.
124. Khoury, J., & Langleben, D. (1998). Effects of endotoxin on lung pericytes in vitro. Microvascular Research, 56, 71-84.
125. Lindemann, D., Werle, S. B., Steffens, D., Garcia-Godoy, F., Pranke, P., & Casagrande, L. (2014). Effects of cryopreservation on the characteristics of dental pulp stem cells of intact deciduous teeth. Archives of Oral Biology, 59, 970-976.
126. Sudchada, S., & Kheolamai, P. (2012). Y UP, et al. CD14−/CD34+ is the founding population of umbilical cord bloodderived endothelial progenitor cells and angiogenin1 is an important factor promoting the colony formation. Annals of Hematology, 91, 321-329.
127. Waterman, R. S., Tomchuck, S. L., Henkle, S. L., & Betancourt, A. M. (2010). A new mesenchymal stem cell (MSC) paradigm: polarization into a pro-inf lammatory MSC1 or an Immunosuppressive MSC2 phenotype. PloS One, 5, e10088