Journal of Endodontics
Volume 33, Issue 5 , Pages 524-530 , May 2007

Vascular Endothelial Growth Factor and Its Relationship With the Dental Pulp

  • Leticia Grando Mattuella, DDS, MSc

      Affiliations

    • School of Dentistry, Federal University of Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil
    • Corresponding Author InformationAddress requests for reprints to Dr. Letícia Grando Mattuella, Rua Roque Calage, 566/201, 91350-090 Porto Alegre, RS, Brasil.
    • ,
  • Leticia Westphalen Bento, DDS

      Affiliations

    • School of Dentistry, Federal University of Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil
    • ,
  • José Antonio Poli de Figueiredo, DDS, MSc, PhD

      Affiliations

    • Department of Morphological Sciences, Institute of Basic Health Sciences, School of Dentistry, Federal University of Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil
    • Eastman Dental Institute and University College London Hospital, London, United Kingdom
    • ,
  • Jacques Eduardo Nör, DDS, MSc, PhD

      Affiliations

    • Department of Cariology, Restorative Sciences and Endodontics, School of Dentistry, University of Michigan, Ann Arbor, MI.
    • ,
  • Fernando Borba de Araujo, DDS, MSc, PhD

      Affiliations

    • School of Dentistry, Federal University of Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil
    • ,
  • Anna Christina Medeiros Fossati, DDS, MSc, PhD

      Affiliations

    • Department of Morphological Sciences, Institute of Basic Health Sciences, School of Dentistry, Federal University of Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil

References 

  1. Kim S, Liu M, Simchon S, Dorscher-Kim JE. Effects of selected inflammatory mediators on blood flow and vascular permeability in the dental pulp. Proc Finn Dent Soc. 1992;88(Suppl 1):387–392
  2. Chiego Júnior DJ. Histology of pulp. In:  Avery JK editors. Oral development and histology. 2nd ed.. Stuttgart: Thieme; 1994;p. 262–281
  3. Linde A. The extracellular matrix of the dental pulp and dentin. J Dent Res. 1985;64:523–529
  4. Martinez EF, Souza SOM, Corrêa L, Araújo VC. Immunohistochemical localization of tenascin, fibronectin, and type III collagen in human dental pulp. J Endod. 2000;26:708–711
  5. Lukinmaa PL, Waltimo J. Immunohistochemical localization of types I, V and VI collagen in human permanent teeth and periodontal ligament. J Dent Res. 1992;71:391–397
  6. Smith AJ, Murray PE, Lumley PJ. Preserving the vital pulp in operative dentistry: I. A biological approach. Dent Update. 2002;29:64–69
  7. Cooper GM. Cell Signaling. In:  Cooper GM,  Hausman RE editor. The cell: a molecular approach. Washington: Asm Press; 1997;p. 521–560
  8. Lodish H, Berk A, Zipursky L, Matsudaira P, Baltimore D, Darnell J. Cell-to-cell signaling: hormones and receptors. In:  Lodish H,  Darnell J editor. Molecular cell biology. 4th ed.. New York: W. H. Freeman & Co; 2000;p. 848–909
  9. Alberts B, Bray D, Lewis J, Raff M, Roberts K, Watson JD. Cell communication. In:  Alberts B,  Bray D,  Lewis J,  Raff M,  Roberts K,  Watson JD editor. Molecular biology of the cell. 4th ed.. New York: Garland Science; 2002;p. 831–906
  10. Smith AJ. Pulpal responses to caries and dental repair. Caries Res. 2002;36:223–232
  11. Roberts-Clark DJ, Smith AJ. Angiogenic growth factors in human dentine matrix. Arch Oral Biol. 2000;45:1013–1016
  12. Thesleff I, Tummers M. Stem cells and tissue engineering: prospects for regenerating tissues in dental practice. Med Princ Pract. 2003;12(Suppl 1):43–50
  13. Botero TM, Mantellini MG, Song W, Hanks CT, Nör JE. Effect of lipopolysaccharides on vascular endothelial growth factor expression in mouse pulp cells and macrophages. Eur J Oral Sci. 2003;111:228–234
  14. Telles PD, Hanks CT, Machado MAAM, Nör JE. Lipoteichoic acid up-regulates VEGF expression in macrophages and pulp cells. J Dent Res. 2003;82:466–470
  15. Konishi N, Miki C, Yoshida T, Tanaka K, Toiyama Y, Kusunoki M. Interleukin-1 receptor antagonist inhibits the expression of vascular endothelial growth factor in colorectal carcinoma. Oncology. 2005;68:138–145
  16. Akeno N, Robins J, Zhang M, Czyzyk-Krzeska MF, Clemens TL. Induction of vascular endothelial growth factor by IGF-I in osteoblast-like cells is mediated by the PI3K signaling pathway through the hypoxia-inducible factor-2alpha. Endocrinology. 2002;143:420–425
  17. Leung KW, Pon YL, Wong RN, Wong AS. Ginsenoside-Rg1 induces vascular endothelial growth factor expression through the glucocorticoid receptor-related phosphatidylinositol 3-kinase/Akt and beta-catenin/T-cell factor-dependent pathway in human endothelial cells. J Biol Chem. 2006;281:36280–36288
  18. Rishi AK, Parikh R, Wali A, et al. EGF receptor-related protein (ERRP) inhibits invasion of colon cancer cells and tubule formation by endothelial cells in vitro. Anticancer Res. 2006;26:1029–1037
  19. Lee KS, Kim SR, Park SJ, et al. Phosphatase and tensin homolog deleted on chromosome 10 (PTEN) reduces vascular endothelial growth factor expression in allergen-induced airway inflammation. Mol Pharmacol. 2006;69:1829–1839
  20. Narita K, Staub J, Chien J, et al. HSulf-1 inhibits angiogenesis and tumorigenesis in vivo. Cancer Res. 2006;66:6025–6032
  21. Yoshioka M, Yuasa S, Matsumura K, et al. Chondromodulin-I maintains cardiac valvular function by preventing angiogenesis. Nat Med. 2006;12:1151–1159
  22. Folkman J, Klagsbrun M. Angiogenic factors. Science. 1987;235:442–447
  23. Auerbach R, Auerbach W. Vasculogenesis and angiogenesis. In:  Fan TD,  Kohn ED editor. The new angiotherapy. Totowa: Human Press; 2001;p. 1–6.
  24. Folkman J, Shing Y. Angiogenesis. J Biol Chem. 1992;267:10931–10934
  25. Ribatti D. The crucial role of vascular permeability factor/ vascular endothelial growth factor in angiogenesis: a historical review. Br J Haematol. 2004;128:303–309
  26. Ferrara N. VEGF and the quest for tumour angiogenesis factors. Nat Rev Cancer. 2002;2:795–803
  27. Senger DR, Galli SJ, Dvorak AM, Perruzzi CA, Harvey VS, Dvorak HF. Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science. 1983;219:983–985
  28. Ferrara N, Henzel WJ. Pituitary follicular cells secrete a novel heparin-binding growth factor specific for vascular endothelial cells. Biochem Biophys Res Commun. 1989;161:851–858
  29. Keck PJ, Hauser SD, Krivi G, et al. Vascular permeability factor, an endothelial cell mitogen related to PDGF. Science. 1989;246:1309–1312
  30. Leung DW, Cachianes G, Kuang W, Goeddel DV, Ferrara N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science. 1989;246:1306–1309
  31. Keyt BA, Nguyen HV, Berleau LT, et al. Identification of vascular endothelial growth factor determinants for binding KDR and Flt-1 receptors (Generation of receptor-selective VEGF variants by site-directed mutagenesis). J Biol Chem. 1996;271:5638–5646
  32. Park JE, Keller GA, Ferrara N. The vascular endothelial growth factor (VEGF) isoforms: differential deposition into the subepithelial extracellular matrix and bioactivity of extracellular matrix-bound VEGF. Mol Biol Cell. 1993;4:1317–1326
  33. Ferrara N. Vascular endothelial growth factor: basic science and clinical progress. Endocr Rev. 2004;25:581–611
  34. Pimenta FJGS, Sá AR, Gomez RS. Lymphangiogenesis in human dental pulp. Int Endod J. 2003;36:853–856
  35. Ferrara N. Role of vascular endothelial growth factor in regulation of physiological angiogenesis. Am J Physiol Cell Physiol. 2001;280:C1358–C1366
  36. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med. 2003;9:669–676
  37. Waltenberger J, Welsh LC, Siegbahn A, Shibuya M, Heldin CH. Different signal transduction properties of KDR and Flt-1, two receptors for vascular endothelial growth factor. J Biol Chem. 1994;269:26988–26995
  38. Maru Y, Yamagushi S, Shibuya M. Flt-1, a receptor for vascular endothelial growth factor, has transforming and morphogenic potentials. Oncogene. 1998;16:2585–2595
  39. Park JE, Chen HH, Winer J, Houck KA, Ferrara N. Placenta growth factor (potentiation of vascular endothelial growth factor bioactivity in vitro and in vivo and high affinity binding to Flt-1 but not to Flk-1/ KDR). J Biol Chem. 1994;269:25646–25654
  40. Roberts DM, Kearney JB, Johnson JH, Rosenberg MP, Kumar R, Bautch VL. The vascular endothelial growth factor (VEGF) receptor Flt-1 (VEGFR-1) modulates Flk-1 (VEGFR-2) signaling during blood vessel formation. Am J Pathol. 2004;164:1531–1535
  41. Shalaby F, Rossant J, Yamagushi TP, et al. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature. 1995;376:62–66
  42. Niida S, Kaku M, Amano H, et al. Vascular endothelial growth factor can substitute for macrophage colony-stimulating factor in the support of osteoclastic bone resorption. J Exp Med. 1999;190:293–298
  43. Gille H, Kowalski J, Li B, et al. Analysis of biological effects and signaling properties of Flt-1 (VEGFR-1) and KDR (VEGFR-2) (A reassessment using novel receptor-specific vascular endothelial growth factor mutants). J Biol Chem. 2001;276:3222–3230
  44. Matthews B, Andrew D. Microvascular architecture and exchange in teeth. Microcirculation. 1995;2:305–313
  45. Heyeraas KJ, Berggreen E. Interstitial fluid pressure in normal and inflamed pulp. Crit Rev Oral Biol Med. 1999;10:328–336
  46. Seltzer S, Farber PA. Microbiologic factors in endodontology. Oral Surg Oral Med Oral Pathol. 1994;78:634–645
  47. Yang LC, Tsai CH, Huang FM, et al. Induction of vascular endothelial growth factor expression in human pulp fibroblasts stimulated with Black-pigmented Bacteroides. Int Endod J. 2004;37:588–592
  48. Chu SC, Tsai CH, Yang SF, et al. Induction of vascular endothelial growth factor gene expression by proinflammatory cytokines in human pulp and gingival fibroblasts. J Endod. 2004;30:704–707
  49. Rolla G, Oppermann RV, Bowen WH, Ciardi JE, Knox KW. High amounts of lipoteichoic acid in sucrose-induced plaque in vivo. Caries Res. 1980;14:235–238
  50. Ginsburg I. Role of lipoteichoic acid in infection and inflammation. Lancet Infect Dis. 2002;2:171–179
  51. Hoshino E. Predominant obligate anaerobes in human carious dentin. J Dent Res. 1985;64:1195–1198
  52. Love RM, Jenkinson HF. Invasion of dentinal tubules by oral bacteria. Crit Rev Oral Biol Med. 2002;13:171–183
  53. Hahn CL, Falkler WA, Minah GE. Microbiological studies of carious dentine from human teeth with irreversible pulpitis. Arch Oral Biol. 1991;36:147–153
  54. Rietschel ET, Kirikae T, Schade FU, et al. The chemical structure of bacterial endotoxin in relation to bioactivity. Immunobiology. 1993;187:169–190
  55. Matsushita K, Motani R, Sakuta T, et al. Lipopolysaccharide enhances the production of vascular endothelial growth factor by human pulp cells culture. Infect Immun. 1999;67:1633–1639
  56. Matsushita K, Motani R, Sakuta T, et al. 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. J Dent Res. 2000;79:1596–1603
  57. Poltorak A, Smirnova I, Liu MY, et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in TLR4 gene. Science. 1998;282:2085–2088
  58. Hoshino K, Takeuchi O, Kawai T, et al. Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the LPS gene product. J Immunol. 1999;162:3749–3752
  59. Botero TM, Shelburne CE, Holland GR, Hanks CT, Nör JE. TLR4 mediates LPS-induced VEGF expression in odontoblasts. J Endod. 2006;32:951–955
  60. Underhill DM, Ozinsky A, Hajjar AM, et al. The toll-like receptor 2 is recruited to macrophage phagosomes and discriminates between pathogens. Nature. 1999;401:811–815
  61. Mantellini MG, Botero TM, Yaman P, Dennison JB, Hanks CT, Nör JE. Adhesive resin induces apoptosis and cell-cycle arrest of pulp cells. J Dent Res. 2003;82:592–596
  62. Mantellini MG, Botero TM, Yaman P, Dennison JB, Hanks CT, Nör JE. Adhesive resin and the hydrophilic monomer HEMA induce VEGF expression on dental pulp cells and macrophages. Dent Mater. 2006;22:434–440
  63. Artese L, Rubini C, Ferrero G, Fiorini M, Santinelli A, Piattelli A. Vascular endothelial growth factor (VEGF) expression in healthy and inflamed human pulps. J Endod. 2002;28:20–23
  64. Leonardi R, Caltabiano M, Pagano M, Pezzuto V, Loreto C, Palestro G. Detection of vascular endothelial growth factor/ vascular permeability factor in periapical lesions. J Endod. 2003;29:180–183
  65. Derringer KA, Linden RWA. Angiogenic growth factors released in human dental pulp following orthodontic force. Arch Oral Biol. 2003;48:285–291
  66. Derringer KA, Linden RWA. Vascular endothelial growth factor, fibroblast growth factor-2, platelet derived growth factor and transforming growth factor beta released in human dental pulp following orthodontic force. Arch Oral Biol. 2004;49:631–641
  67. Kaku M, Kohno S, Kawata T, et al. Effects of vascular endothelial growth factor on osteoclast induction during tooth movement in mice. J Dent Res. 2001;80:1880–1883
  68. Kohno S, Kaku M, Tsutsui K, et al. Expression of vascular endothelial growth factor and the effects on bone remodeling during experimental tooth movement. J Dent Res. 2003;82:177–182

PII: S0099-2399(07)00007-6

doi: 10.1016/j.joen.2007.01.003

Journal of Endodontics
Volume 33, Issue 5 , Pages 524-530 , May 2007

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