The acid test of fluoride: How pH modulates toxicity

PLoS ONE

Volumn 5, Issue 5, 2010, Pages

  Sharma, Ramaswamy ^a   Tsuchiya, Masahiro ^b   Skobe, Ziedonis ^a   Tannous, Bakhos A ^c   Bartlett, John D ^a  

^a FORSYTH INSTITUTE   (United States)

^b TOHOKU UNIVERSITY   (Japan)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMELOBLASTINE; AMELOGENIN; CELL MARKER; DRINKING WATER; ENAMELIN; FLUORIDE; KALLIKREIN; KALLIKREIN 4; LUCIFERASE; MATRIX METALLOPROTEINASE 20; PROTEIN C JUN; PROTEIN PERK; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR ELF 2ALPHA; UNCLASSIFIED DRUG;

ACIDITY; AMELOBLAST; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CELL MATURATION; CELL STRESS; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME RELEASE; GENE EXPRESSION; GENETIC TRANSCRIPTION; MOUSE; NONHUMAN; PH; PROTEIN PHOSPHORYLATION; RAT; REPORTER GENE; TOOTH DEVELOPMENT;

ACIDS; AMELOBLASTS; ANIMALS; FLUORIDES; GENE EXPRESSION REGULATION; HYDROGEN-ION CONCENTRATION; MODELS, BIOLOGICAL; PROTEINS; RATS; STRESS, PHYSIOLOGICAL;

RATTUS;

EID: 77956290742     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0010895     Document Type: Article

References (78)

1. CDC (1995) Engineering and administrative recommendations for water fluoridation, 1995. Centers for Disease Control and Prevention. MMWR Recomm Rep 44: 1-40.
2. WHO (2006) Fzluoride in Drinking Water; Fawell JBK, Chilton J, Dahi E, Fewtrell L, Magara Y, eds. London, UK: IWA Publishing. 144 p.
3. Dean HT, Elvove E (1936) Some Epidemiological Aspects of Chronic Endemic Dental Fluorosis. Am J Public Health Nations Health 26: 567-575
4. Azar HA, Nucho CK, Bayyuk SI, Bayyuk WB (1961) Skeletal sclerosis due to chronic fluoride intoxication. Cases from an endemic area of fluorosis in the region of the Persian Gulf. Ann Intern Med 55: 193-200.
5. Ogilvie AL (1953) Histologic findings in the kidney, liver, pancreas, adrenal, and thyroid glands of the rat following sodium fluoride administration. J Dent Res 32: 386-397.
6. Beltran-Aguilar ED, Barker LK, Canto MT, Dye BA, Gooch BF, et al. (2005) Surveillance for dental caries, dental sealants, tooth retention, edentulism, and enamel fluorosis-United States, 1988-1994 and 1999-2002. MMWR Surveill Summ 54: 1-43.
7. Fejerskov O, Manji F, Baelum V (1990) The nature and mechanisms of dental fluorosis in man. J Dent Res 69 Spec No: 692-700 discussion 721.
8. Smith CE, Issid M, Margolis HC, Moreno EC (1996) Developmental changes in the pH of enamel fluid and its effects on matrix-resident proteinases. Adv Dent Res 10: 159-169.
9. Simmer JP, Fukae M, Tanabe T, Yamakoshi Y, Uchida T, et al. (1998) Purification, characterization, and cloning of enamel matrix serine proteinase 1. J Dent Res 77: 377-386.
10. Smith CE (1998) Cellular and chemical events during enamel maturation. Crit Rev Oral Biol Med 9: 128-161.
11. Simmer JP, Fincham AG (1995) Molecular mechanisms of dental enamel formation. Crit Rev Oral Biol Med 6: 84-108.
12. Smith CE, Chong DL, Bartlett JD, Margolis HC (2005) Mineral acquisition rates in developing enamel on maxillary and mandibular incisors of rats and mice: implications to extracellular acid loading as apatite crystals mature. J Bone Miner Res 20: 240-249.
13. Sharma R, Tsuchiya M, Bartlett JD (2008) Fluoride induces endoplasmic reticulum stress and inhibits protein synthesis and secretion. Environ Health Perspect 116: 1142-1146.
14. Kubota K, Lee DH, Tsuchiya M, Young CS, Everett ET, et al. (2005) Fluoride induces endoplasmic reticulum stress in ameloblasts responsible for dental enamel formation. J Biol Chem 280: 23194-23202.
15. Hammond C, Helenius A (1995) Quality control in the secretory pathway. Curr Opin Cell Biol 7: 523-529.
16. Gow A, Sharma R (2003) The unfolded protein response in protein aggregating diseases. Neuromolecular Med 4: 73-94.
17. Schroder M, Kaufman RJ (2005) The mammalian unfolded protein response. Annu Rev Biochem 74: 739-789.
18. Nishitoh H, Matsuzawa A, Tobiume K, Saegusa K, Takeda K, et al. (2002) ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes Dev 16: 1345-1355.
19. Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, et al. (2000) Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287: 664-666.
20. Zhang C, Kawauchi J, Adachi MT, Hashimoto Y, Oshiro S, et al. (2001) Activation of JNK and transcriptional repressor ATF3/LRF1 through the IRE1/TRAF2 pathway is implicated in human vascular endothelial cell death by homocysteine. Biochem Biophys Res Commun 289: 718-724.
21. Bronckers AL, Lyaruu DM, DenBesten PK (2009) The impact of fluoride on ameloblasts and the mechanisms of enamel fluorosis. J Dent Res 88: 877-893.
22. Angmar-Mansson B, Whitford GM (1984) Enamel fluorosis related to plasma Flevels in the rat. Caries Res 18: 25-32.
23. Garcia-Montalvo EA, Reyes-Perez H, Del Razo LM (2009) Fluoride exposure impairs glucose tolerance via decreased insulin expression and oxidative stress. Toxicology 263: 75-83.
24. Hollien J, Lin JH, Li H, Stevens N, Walter P, et al. (2009) Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J Cell Biol 186: 323-331.
25. Hollien J, Weissman JS (2006) Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313: 104-107.
26. Wright JT, Chen SC, Hall KI, Yamauchi M, Bawden JW (1996) Protein characterization of fluorosed human enamel. J Dent Res 75: 1936-1941.
27. Den Besten PK (1986) Effects of fluoride on protein secretion and removal during enamel development in the rat. J Dent Res 65: 1272-1277.
28. DenBesten PK, Heffernan LM (1989) Enamel proteases in secretory and maturation enamel of rats ingesting 0 and 100 PPM fluoride in drinking water. Adv Dent Res 3: 199-202.
29. Shinoda H, Ogura H (1978) Scanning electron microscopical study on the fluorosis of enamel in rats. Calcif Tissue Res 25: 75-83.
30. Shinoda H (1975) Effect of long-term administration of fluoride on physicochemical properties of the rat incisor enamel. Calcif Tissue Res 18: 91-100.
31. Triller M (1979) Structural and histochemical observations of fluorotic enamel matrix. J Dent Res 58: 1028-1029.
32. Zhou R, Zaki AE, Eisenmann DR (1996) Morphometry and autoradiography of altered rat enamel protein processing due to chronic exposure to fluoride. Arch Oral Biol 41: 739-747.
33. Robinson C, Connell S, Kirkham J, Brookes SJ, Shore RC, et al. (2004) The effect of fluoride on the developing tooth. Caries Res 38: 268-276.
34. Robinson C, Kirkham J (1990) The effect of fluoride on the developing mineralized tissues. J Dent Res 69 Spec No: 685-691; discussion 721.
35. Aoba T, Fejerskov O (2002) Dental fluorosis: chemistry and biology. Crit Rev Oral Biol Med 13: 155-170.
36. Bawden JW, Crenshaw MA, Wright JT, LeGeros RZ (1995) Consideration of possible biologic mechanisms of fluorosis. J Dent Res 74: 1349-1352.
37. Holzer P (2000) Gastroduodenal mucosal defense. Curr Opin Gastroenterol 16: 469-478.
38. Kawase T, Suzuki A (1989) Studies on the transmembrane migration of fluoride and its effects on proliferation of L-929 fibroblasts (L cells) in vitro. Arch Oral Biol 34: 103-107.
39. Hirano S, Ando M (1997) Fluoride mediates apoptosis in osteosarcoma UMR 106 and its cytotoxicity depends on the pH. Arch Toxicol 72: 52-58.
40. Schuster GS, Whitford GM, Lankford MT (1981) Relationship between fluoride resistance of Streptococcus mutans 6715 and medium pH. Caries Res 15: 32-39.
41. Whitford GM, Schuster GS, Pashley DH, Venkateswarlu P (1977) Fluoride uptake by Streptococcus mutans 6715. Infect Immun 18: 680-687.
42. Brussock SM, Kral TA (1987) Effects of pH on expression of sodium fluoride resistance in Streptococcus mutans. J Dent Res 66: 1594-1596.
43. Whitford GM, Pashley DH (1984) Fluoride absorption: the influence of gastric acidity. Calcif Tissue Int 36: 302-307.
44. Whitford GM, Callan RS, Wang HS (1982) Fluoride absorption through the hamster cheek pouch: a pH-dependent event. J Appl Toxicol 2: 303-306.
45. Whitford GM, Pashley DH, Stringer GI (1976) Fluoride renal clearance: a pH-dependent event. Am J Physiol 230: 527-532.
46. Rouch AJ, Whitford GM, Campbell HT (1992) Fluoride flux in the rabbit CCD: a pH-dependent event. Kidney Int 41: 342-349.
47. Whitford GM, Pashley DH (1991) Fluoride reabsorption by nonionic diffusion in the distal nephron of the dog. Proc Soc Exp Biol Med 196: 178-183.
48. Ekstrand J, Ehrnebo M, Whitford GM, Jarnberg PO (1980) Fluoride pharmacokinetics during acid-base balance changes in man. Eur J Clin Pharmacol 18: 189-194.
49. Ekstrand J, Spak CJ, Ehrnebo M (1982) Renal clearance of fluoride in a steady state condition in man: influence of urinary flow and pH changes by diet. Acta Pharmacol Toxicol (Copenh) 50: 321-325.
50. Jarnberg PO, Ekstrand J, Irestedt L (1981) Renal fluoride excretion and plasma fluoride levels during and after enflurane anesthesia are dependent on urinary pH. Anesthesiology 54: 48-52.
51. Whitford GM, Pashley DH, Reynolds KE (1977) Fluoride absorption from the rat urinary bladder: a pH-dependent event. Am J Physiol 232: F10-15.
52. Whitford GM, Angmar-Mansson B (1995) Fluorosis-like effects of acidosis, but not NH+4, on rat incisor enamel. Caries Res 29: 20-25.
53. Whitford GM, Pashley DH, Reynolds KE (1979) Fluoride tissue distribution: short-term kinetics. Am J Physiol 236: F141-148.
54. He H, Ganapathy V, Isales CM, Whitford GM (1998) pH-dependent fluoride transport in intestinal brush border membrane vesicles. Biochim Biophys Acta 1372: 244-254.
55. Kallenbach E (1967) Cell architecture in the papillary layer of rat incisor enamel organ at the stage of enamel maturation. Anat Rec 157: 683-688.
56. Garant PR, Nagy AR, Cho MI (1984) A freeze-fracture study of the papillary layer of the rat incisor enamel organ. Tissue Cell 16: 635-645.
57. Garant PR (1972) The demonstration of complex gap junctions between the cells of the enamel organ with lanthanum nitrate. J Ultrastruct Res 40: 333-348.
58. Toyosawa S, Ogawa Y, Inagaki T, Ijuhin N (1996) Immunohistochemical localization of carbonic anhydrase isozyme II in rat incisor epithelial cells at various stages of amelogenesis. Cell Tissue Res 285: 217-225.
59. Smith CE, Nanci A, Moffatt P (2006) Evidence by signal peptide trap technology for the expression of carbonic anhydrase 6 in rat incisor enamel organs. Eur J Oral Sci 114 Suppl 1: discussion 147-153,164-145, 380-141.
60. Conconi FM, Bank A, Marks PA (1966) Polyribosomes and control of protein synthesis: effects of sodium fluoride and temperature of reticulocytes. J Mol Biol 19: 525-540.
61. DenBesten PK, Thariani H (1992) Biological mechanisms of fluorosis and level and timing of systemic exposure to fluoride with respect to fluorosis. J Dent Res 71: 1238-1243.
62. DenBesten PK, Yan Y, Featherstone JD, Hilton JF, Smith CE, et al. (2002) Effects of fluoride on rat dental enamel matrix proteinases. Arch Oral Biol 47: 763-770.
63. Godchaux W, Atwood KCt (1976) Structure and function of initiation complexes which accumulate during inhibition of protein synthesis by fluoride ion. J Biol Chem 251: 292-301.
64. Helgeland K (1976) Effect of fluoride on protein and collagen biosynthesis in rabbit dental pulp in vitro. Scand J Dent Res 84: 276-285.
65. Holland RI (1979) Fluoride inhibition of protein synthesis. Cell Biol Int Rep 3: 701-705.
66. Holland RI (1979) Fluoride inhibition of protein and DNA synthesis in cells in vitro. Acta Pharmacol Toxicol (Copenh) 45: 96-101.
67. Kruger BJ (1968) Ultrastructural changes in ameloblasts from fluoride treated rats. Arch Oral Biol 13: 969-977.
68. Lin SY, Mosteller RD, Hardesty B (1966) The mechanism of sodium fluoride and cycloheximide inhibition of hemoglobin biosynthesis in the cell-free reticulocyte system. J Mol Biol 21: 51-69.
69. Matsuo S, Inai T, Kurisu K, Kiyomiya K, Kurebe M (1996) Influence of fluoride on secretory pathway of the secretory ameloblast in rat incisor tooth germs exposed to sodium fluoride. Arch Toxicol 70: 420-429.
70. Matsuo S, Nakagawa H, Kiyomiya K, Kurebe M (2000) Fluoride-induced ultrastructural changes in exocrine pancreas cells of rats: fluoride disrupts the export of zymogens from the rough endoplasmic reticulum (rER). Arch Toxicol 73: 611-617.
71. Menoyo I, Rigalli A, Puche RC (2005) Effect of fluoride on the secretion of insulin in the rat. Arzneimittelforschung 55: 455-460.
72. Rigalli A, Ballina JC, Roveri E, Puche RC (1990) Inhibitory effect of fluoride on the secretion of insulin. Calcif Tissue Int 46: 333-338.
73. Vesco C, Colombo B (1970) Effect of sodium fluoride on protein synthesis in HeLa cells: inhibition of ribosome dissociation. J Mol Biol 47: 335-352.
74. Gstraunthaler G, Landauer F, Pfaller W (1992) Ammoniagenesis in LLC-PK1 cultures: role of transamination. Am J Physiol 263: C47-54.
75. Gstraunthaler G, Holcomb T, Feifel E, Liu W, Spitaler N, et al. (2000)Differential expression and acid-base regulation of glutaminase mRNAs in gluconeogenic LLC-PK(1)-FBPase(+) cells. Am J Physiol Renal Physiol 278: F227-F237.
76. Tannous BA, Kim DE, Fernandez JL, Weissleder R, Breakefield XO (2005) Codon-optimized Gaussia luciferase cDNA for mammalian gene expression in culture and in vivo. Mol Ther 11: 435-443.
77. Badr CE, Hewett JW, Breakefield XO, Tannous BA (2007) A highly sensitive assay for monitoring the secretory pathway and ER stress. PLoS One 2: e571.
78. Tsuchiya M, Sharma R, Tye CE, Sugiyama T, Bartlett JD (2009) Transforming growth factor-beta1 expression is up-regulated in maturation-stage enamel organ and may induce ameloblast apoptosis. Eur J Oral Sci 117: 105-112.