Dental enamel is the most highly calcified tissue in mammals, and its formation is an issue of fundamental biomedical importance. The enamel-forming cells must somehow supply calcium in bulk yet avoid the cytotoxic effects of excess calcium. Disrupted calcium transport could contribute to a variety of developmental defects in enamel, and the underlying cellular machinery is a potential target for drugs to improve enamel quality. The mechanisms used to transport calcium remain unclear despite much progress in our understanding of enamel formation. Here, current knowledge of how enamel cells handle calcium is reviewed in the context of findings from other epithelial calcium-transport systems. In the past, most attention has focused on approaches to boost the poor diffusion of calcium in cytosol. Recent biochemical findings led to an alternative proposal that calcium is routed through high-capacity stores associated with the endoplasmic reticulum. Research areas needing further attention and a working model are also discussed. Calcium-handling mechanisms in enamel cells are more generally relevant to the understanding of epithelial calcium transport, biomineralization, and calcium toxicity avoidance.
References
1.
Airaksinen MS, Eilers J., Garaschuk O., Thoenen H., Konnerth A., Meyer M. (1997). Ataxia and altered dendritic calcium signaling in mice carrying a targeted null mutation of the calbindin D28k gene. Proc Natl Acad Sci USA94:1488-1493.
2.
Allbritton NL, Meyer T., Stryer L. (1992). Range of messenger action of calcium ion and inositol 1,4,5-trisphosphate. Science258:1812-1815.
3.
Alonso MT, Barrero MJ, Michelena P., Carnicero E., Cuchillo I., Garcia AG, et al. (1999). Ca2+-induced Ca2+ release in chromaffin cells seen from inside the ER with targeted aequorin. J Cell Biol144:241-254.
4.
Aoba T., Moreno EC (1987). The enamel fluid in the early secretory stage of porcine amelogenesis: chemical composition and saturation with respect to enamel. Calcif Tissue Int41:86-94.
5.
Aoba T., Moreno EC (1992). Changes in the solubility of enamel mineral at various stages of porcine amelogenesis. Calcif Tissue Int50:266-272.
6.
Aoba T., Tanabe T., Moreno EC (1987). Proteins in the enamel fluid of immature porcine teeth. J Dent Res66:1721-1726.
7.
Aoba T., Moreno EC, Shimoda S. (1992). Competitive adsorption of magnesium and calcium ions onto synthetic and biological apatites. Calcif Tissue Int51:143-150.
8.
Balda MS, Matter K. (1998). Tight junctions. J Cell Sci111:541-547.
9.
Banno T., Kohno K. (1996). Conformational changes of smooth endoplasmic reticulum induced by brief anoxia in rat Purkinje cells. J Comp Neurol369:462-471.
10.
Banno T., Kohno K. (1998). Conformational changes of the smooth endoplasmic reticulum are facilitated by L-glutamate and its receptors in rat Purkinje cells. J Comp Neurol402:252-263.
11.
Barritt GJ (1999). Receptor-activated Ca2+ inflow in animal cells. A variety of pathways tailored to meet different intracellular Ca2+ signalling requirements. Biochem J337:153-169.
12.
Bawden JW (1989). Calcium transport during mineralization. Anat Rec224:226-233.
13.
Bawden JW, Crenshaw MA, Takano Y., Hammarstrom L. (1982). Ion transport through the enamel organ. An update. J Dent Res61:1552-1554.
14.
Belan P., Gardner J., Gerasimenko O., Gerasimenko J., Mills CL, Petersen OH, et al. (1998). Isoproterenol evokes extracellular Ca2+ spikes due to secretory events in salivary gland cells. J Biol Chem273:4106-4111.
15.
Benlimame M., Simard D., Nabi IR ( 1995). Autocrine mobility factor receptor is a marker for a distinct membranous tubular organelle. J Cell Biol129:459-471.
16.
Berchtold MW, Celio MR, Heizmann CW (1984). Parvalbumin in non-muscle tissues of the rat. Quantitation and immunohistochemical localization. J Biol Chem259:5189-5196.
17.
Berdal A., Balmain N., Cuisinier-Gleizes P., Mathieu H. (1987). Histology and microradiography of early postnatal molar tooth development in vitamin-D deficient rats. Arch Oral Biol32:493-498.
18.
Berdal A., Balmain N., Brehier A., Hotton D., Cuisinier-Gleizes P., Mathieu H. (1989a). Immunological characterisation, developmental pattern and vitamin D-dependency of calbindin D-28kDa in rat teeth ameloblasts. Differentiation40:27-35.
19.
Berdal A., Balmain N., Thomasset M., Brehier A., Hotton D., Cuisinier-Gleizes P., et al. (1989b). Calbindins D-9kDa and -28kDa and enamel secretion in vitamin D-deficient and control rats. Connect Tissue Res22:165-171.
20.
Berdal A., Hotton D., Kamyab S., Cuisinier-Gleizes P., Mathieu H. (1991a). Subcellular co-localization and co-variations of two vitamin D-dependent proteins in rat ameloblasts. Arch Oral Biol36:715-725.
21.
Berdal A., Nanci A., Smith CE, Ahluwalia JP, Thomasset M., Cuisinier-Gleizes P., et al. (1991b). Differential expression of calbindin-D28kDa in rat incisor ameloblasts throughout enamel development. Anat Rec230:149-163.
22.
Berdal A., Hotton D., Pike JW, Mathieu H., Dupret JM (1993). Cell- and stage-specific expression of vitamin D receptor and calbindin genes in rat incisor. Regulation by 1,25-dihydroxyvitamin D3. Dev Biol155:172-179.
23.
Berdal A., Hotton D., Saffar IL, Thomasset M., Nanci A. (1996). Calbindin-D9k and calbindin-D28k expression in rat mineralized tissues in vivo. J Bone Min Res11:768-779.
24.
Berridge MJ (1993). Inositol trisphosphate and calcium signalling. Nature361:315-325.
25.
Bindels RJM, Timmermans JAH, Hartog A., Coers W., van Os CH (1991). Calbindin-D9k and parvalbumin are exclusively located along basolateral membranes in rat distal nephron. J Am Soc Nephrol2:1122-1129.
26.
Bindels RJM, Koster HPG, van Os CH (1995). Calbindin-D28k facilitates transcellular calcium transport without interfering with calcium signalling (abstract). Nutr125:1980S.
27.
Bonass WA, Kirkham J., Shore RC, Brookes SJ, Godfrey CL, Robinson C. (1998). Identification of rat enamel organ RNA transcripts using differential-display. Connect Tissue Res38:249-256
28.
Borke JL, Zaki AE, Eisenmann DR, Ashrafi SH, Ashrafi SS, Penniston IT (1993). Expression of plasma membrane Ca2+ pump epitopes parallels the progression of enamel and dentin mineralization in rat incisor. J Histochem Cytochem41:175-181.
29.
Borke JL, Zaki AM, Eisenmann DR, Mednieks M.1 (1995). Localization of plasma membrane Ca2+ pump mRNA and protein in human ameloblasts by in situ hybridization and immunohistochemistry. Connect Tissue Res33:139-144.
30.
Boyde A., Reith EJ (1981). Display of maturation cycles in rat incisor enamel with tetracycline labelling. Histochemistry72:551-561.
31.
Bronner F. (1990). Transcellular calcium transport. In: Intracellular calcium regulation. Bronner F, editor. New York: Alan R. Liss, pp. 415-437.
32.
Bronner F. (1991). Calcium transport across epithelia. Int Rev Cytol131:169-212.
33.
Bronner F. (1997). Calcium absorption-a paradigm for mineral absorption. J Nutr128:917-920.
34.
Bronner F., Pansu D. (1999). Nutritional aspects of calcium absorption. J Nutr129:9-12.
35.
Bronner F., Stein WD (1988). CaBPr facilitates intracellular diffusion for Ca pumping in distal convoluted tubule. Am J Physiol255:F558-F562.
36.
Bronner F., Pansu D., Stein WD (1986). An analysis of intestinal calcium transport across the rat intestine. Am J Physiol250:G561-G569.
37.
Carafoli E. (1987). Intracellular calcium homeostasis. Ann Rev Biochem56:395-433.
38.
Carafoli E. (1992). The Ca2+ pump of the plasma membrane. J Biol Chem267:2115-2118.
39.
Celio MR, Norman AW, Heizmann CW (1984). Vitamin-D-dependent calcium-binding protein and parvalbumin occur in bones and teeth. Calcif Tissue Int36:129-130.
40.
Chard PS, Bleakman D., Christakos S., Fullmer CS, Miller RJ (1993). Calcium buffering properties of calbindin D28k and parvalbumin in rat sensory neurones. I Physiol472:341-357.
Clapham DE (1995). Calcium signalling. Cell80:259-268.
43.
Crenshaw MA, Takano Y. (1982). Mechanisms by which the enamel organ controls calcium entry into developing enamel. J Dent Res61:1574-1579.
44.
Davideau JL, Celio MR, Hotton D., Berdal A. (1993). Developmental pattern and subcellular localization of parvalbumin in the rat tooth germ. Arch Oral Biol38:707-715.
45.
DenBesten PK, Thariani H. (1992). Biological mechanisms of fluorosis and level and timing of systemic exposure to fluoride with respect to fluorosis. J Dent Res71:1238-1243.
46.
Deutsch D., Catalano-Sherman ), Dafni L., David S., Palmon A. (1995). Enamel matrix proteins and ameloblast biology. Connect Tissue Res 32197-107.
47.
Dupret JM, L'Horset F., Perret C., Bernaudin JF, Thomaset M. (1992). Calbindin-D9k gene expression in the lung of rat. Absence of regulation by 1,25-dihydroxyvitamin D3 and estrogen. Endocrinology131:2643-2648.
48.
Eckenhoff RG ( 1989). Perinatal changes in lung surfactant calcium measured in situ. J Clin Invest84:1295-1301.
49.
Eisenmann DR, Ashrafi S., Neiman A. (1979). Calcium transport and the secretory ameloblast. Anat Rec193:403-422.
50.
Eisenmann DR, Ashrafi SH, Zaki AE ( 1984). Calcium distribution in freeze-dried enamel organ tissue during normal and altered enamel mineralization. Calcif Tissue Int36:596-603.
51.
Elms TN, Taylor AN (1987). Calbindin-D28k localization in rat molars during odontogenesis. J Dent Res66:1431-1434.
52.
Favus MJ, Tembe V., Ambrosic KA, Nellans HN (1989a). Effects of 1,25(OH)2D3 on enterocyte basolateral membrane Ca transport in rats. Am J Physiol256:G613-G617.
53.
Favus MJ, Tembe V., Tanklefsky MD, Ambrosic KA, Nellans HN (1989b). Effects of quinacrine on calcium active transport by rat intestinal epithelium. Am J Physiol257:G818-G822.
54.
Feher JJ, Fullmer CS, Fritzsch GK (1989). Comparison of the enhanced steady-state diffusion of calcium by calbindin-D9k and calmodulin: possible importance in intestinal calcium absorption. Cell Calcium10:189-203.
55.
Feher JJ, Fullmer CS, Wasserman RH (1992). Role of facilitated diffusion of calcium by calbindin in intestinal calcium absorption. Am J Physiol262:C517-C526.
56.
Fonlupt P., Audebet C., Gire V., Bernier-Valentin F., Rousset B. (1997). Calcium is transported into the lumen of pig thyroid follicles by fluid phase basolateral to apical transcytosis. J Cell Physiol171:43-51.
57.
Freedman RA, Weiser MM, Isselbacher KJ (1977). Calcium translocation by Golgi and lateral-basal membrane vesicles from rat intestine. Decrease in vitamin D-deficient rats. Proc Natl Acad Sci USA74:3612-3616.
58.
Friedman PA (1998). Codependence of renal calcium and sodium transport. Ann Rev Physiol60:179-197.
59.
Friedman PA, Gesek FA (1995). Cellular calcium transport in renal epithelia. Measurement, mechanisms and regulation. Physiol Rev75:429-471.
60.
Fullmer CS (1992). Intestinal calcium absorption. Calcium entry. I Nutr122:644-650.
61.
Garrahan PJ, Rega AF ( 1990). Plasma membrane calcium pump. In: Intracellular calcium regulation. Bronner F, editor. New York: Alan R. Liss, pp. 271-303.
62.
Gerasimenko IV, Tepikin AV, Petersen OH, Gerasimenko OV (1998). Calcium uptake via endocytosis with rapid release from acidifying endosomes. Current Biol8:1335-1338.
63.
Gething MJ, Sambrook I. (1992). Protein folding in the cell. Nature355:33-45.
64.
Gross M., Kumar R. (1990). Physiology and biochemistry of vitamin D-dependent calcium-binding proteins. Am J Physiol259:F195-F209.
65.
Haagsman HP, Hawgood S., Sargeant T., Buckley D., White RT, Drickamer K., et al. (1987). The major lung surfactant protein, SP 28-36, is a calcium-dependent, carbohydrate-binding protein. J Biol Chem262:13877-13880.
66.
Haller T., Dietl P., Deetjen P., Volkl H. (1996). The lysosomal compartment as intracellular calcium store in MDCK cells. A possible involvement in InsP3-mediated Ca2+ release. Cell Calcium19:157-162.
67.
Hanawa M., Takano Y., Wakita M. (1990). An autoradiographic study of calcium movement in the enamel organ of rat molar tooth germs. Arch Oral Biol35:899-906.
68.
Harris-White ME, Zanotti SA, Frautschy SA, Charles AC (1998). Spiral intercellular calcium waves in hippocampal slice cultures. J Neurophysiol79:1045-1052.
69.
Harteneck C., Plant TD, Schultz G. (2000). From worm to man: three subfamilies of TRP channels. Trends Neurosci23: 159-166.
70.
Heizmann CW, Berchtold MW (1987). Expression of parvalbumin and other Ca2+-binding proteins in normal and tumor cells: a topical review. Cell Calcium8:1-41.
71.
Herrington J., Park YB, Babcock DF, Hille B. (1996). Dominant role of mitochondria in clearance of large Ca2+ loads from rat adrenal chromaffin cells. Neuron16:219-228.
72.
Hershberger ME, Tuan RS ( 1998). Placental 57kDa Ca2+binding protein. Regulation of expression and function in trophoblast calcium transport. Dev Biol199:80-92.
73.
Hodgkin AL, Keynes RD (1957). Movements of labelled calcium in squid giant axons. J Physiol138:253-281.
74.
Hoenderop JGJ, van der Kemp AWCM, Hartog A., van de Graf SFJ, van Os CH, Willems PHGM, et al. (1999a). Molecular identification of the apical Ca2+ channel in 1,25-dihydroxyvitamin D3-responsive epithelia. J Biol Chem274: 8375-8378.
75.
Hoenderop JGJ, van der Kemp AWCM, Hartog A., van Os CH, Willems PHGM, Bindels RJM (1999b). The epithelial calcium channel, ECaC, is activated by hyper-polarization and regulated by cytosolic calcium. Biochem Biophys Res Commun261: 488-492.
76.
Hoenderop JGJ, Hartog A., Stuiver M., Doucet A., Willems PHGM, Bindels RJM (2000). Localization of the epithelial Ca2+ channel in rabbit kidney and intestine. I Am Soc Nephrol11: 1171-1178.
77.
Hotton D., Davideau JL, Bernaudin JF, Berdal A. (1995). In situ hybridisation of calbindin-D28k transcripts in undecalcified sections of the rat continuously erupting incisor. Connect Tissue Res32:137-143.
78.
Hubbard MJ (1993). Rapid purification and direct microassay of calbindin9kDa utilizing its solubility in perchloric acid. Biochem J293:223-227.
79.
Hubbard MJ (1995). Calbindin28kDa and calmodulin are hyperabundant in rat dental enamel cells: identification of the protein phosphatase calcineurin as a principal calmodulin target and of a secretion-related role for calbindin28kDa. Eur J Biochem230:68-79.
80.
Hubbard MJ (1996). Abundant calcium homeostasis machinery in rat dental enamel cells. Up-regulation of calcium store proteins during enamel hypermineralization implicates the endoplasmic reticulum in calcium transcytosis. Eur J Biochem239:611-623.
81.
Hubbard MJ (1998a). Enamel cell biology. Towards a comprehensive biochemical understanding. Connect Tissue Res38:17-32.
82.
Hubbard MJ (1998b). Proteomic analysis of enamel cells from developing rat teeth. Big returns from a small tissue. Electrophoresis19:1891-1900.
83.
Hubbard MJ, McHugh NJ (1995). Calbindin28kDa and calbindin30kDa (calretinin) are substantially localised in the particulate fraction of rat brain. FEBS Lett374:333-337.
84.
Hubbard MJ, McHugh NJ (1996). Mitochondrial ATP synthase F1-β-subunit is a calcium-binding protein. FEBS Lett391:323-329.
85.
losephsen K. (1984). Lanthanum tracer study on permeability of ameloblast junctional complexes in maturation zone of rat incisor enamel organ. In: Tooth enamel IV. Fearnhead RW, Suga S, editors. Amsterdam: Elsevier Science, pp. 251-255.
86.
Kallenbach E. (1980). Fate of horseradish peroxidase in the secretion zone of the rat incisor enamel organ. Tissue Cell12:491-501.
87.
Karbach U. (1992). Paracellular calcium transport across the small intestine. J Nutr122:672-677.
88.
Kawamoto T., Shimizu M. (1990). Changes in the mode of calcium and phosphate transport during rat incisal enamel formation. Calcif Tissue Int46:406-414.
89.
Kawamoto T., Shimizu M. (1997). Pathway and speed of calcium movement from blood to mineralizing enamel. J Histochem Cytochem45:213-230.
90.
Kretsinger RH, Mann JE, Simmonds JG (1982). Model of facilitated diffusion of calcium by the intestinal calcium binding protein. In Vitamin D, chemical, biochemical and clinical endocrinology of calcium metabolism. Norman AW, Schaefer K, Herrath DV, Gringoleit HG, editors. New York: Walter de Gruyter, pp. 233-248.
La Bella V., Ho BK, Appel SH, Smith RG (1996). Calbindin-D28k forms a Ca2+-dissociable complex with mellitin in vitro. Biochem Mol Biol Int38:1199-1210.
93.
Leathers VL, Norman AW (1993). Evidence for calcium mediated conformational changes in calbindin-D28k (the vitamin D-induced calcium binding protein) interactions with chick intestinal brush border membrane alkaline phosphatase as studied via photoaffinity labeling techniques. J Cell Biochem52:243-252.
94.
Leese HJ (1988). The formation and function of oviduct fluid. J Reprod Fert82:843-856.
95.
Limeback H. Schlumbohm C., Sen A., Nikiforuk G. (1992). The effects of hypocalcemia/hypophosphatemia on porcine bone and dental hard tissues in an inherited form of type I pseudo-vitamin D deficiency rickets. J Dent Res71:346-352.
96.
Luthra R., Olson MS (1976). Studies of mitochondrial calcium movements using chlortetracycline. Biochim Biophys Acta440:744-758.
97.
Marshak DR, Watterson DM, van Eldik LJ (1981). Calcium-dependent interaction of S100b, troponin C and calmodulin with an immobilised phenothiazine. Proc Natl Acad Sci USA78:6793-6797.
98.
Martone ME Zhang Y. Simpliciano VM, Carragher BO, Ellisman MH (1993). Three-dimensional visualization of the smooth endoplasmic reticulum in Purkinje cell dendrites. J Neurosci13:4636-4646.
99.
Mathieu CL, Burnett SH, Mills SE, Overpeck JG, Bruns DE, Bruns ME (1989a). Gestational changes in calbindin-D9k in rat uterus, yolk sac and placenta. Implications for maternal-fetal calcium transport and uterine muscle function. Proc Natl Acad Sci USA86:3433-3437.
100.
Mathieu CL, Mills SE, Burnett SH, Cloney DL, Bruns DE, Bruns ME (1989b). The presence and estrogen control of immunoreactive calbindin-D9k in the Fallopian tube of the rat. Endocrinology124:2745-2750.
101.
Matsuo S., Yamamoto K., Nishikawa S., Ichikawa H., Wakisaka S., Takano Y., et al. (1986). Influence of colchicine on the distribution of horseradish peroxidase in the secretory ameloblast layer in vitro. Anat Rec216:10-18.
102.
Mayel-Afshar S., Lane SM, Lawson DEM (1988). Relationship between the levels of calbindin synthesis and calbindin mRNA in chick intestine. Quantitation of calbindin mRNA. J Biol Chem263:4355-4361.
103.
McGraw CF, Somlyo AV, Blaustein MP (1980). Localization of calcium in presynaptic nerve terminals. J Cell Biol85:228-241.
104.
McKee MD, Warshawsky H. (1986). Modification of the enamel maturation pattern by vinblastine as revealed by glyoxal bis(2-hydroxyanil) staining as 45calcium radioautography. Histochemistry86:141-145.
105.
McKee MD, Martineau-Doize B., Warshawsky H. (1986). Penetration of various molecular weight proteins into the enamel organ and enamel of the rat incisor. Arch Oral Biol31:287-296.
106.
McKee MD, Nanci A., Smith CE, Warshawsky H. (1989). Cyclical aspects of enamel maturation and the role of ruffle-ended and smooth-ended ameloblasts. In: Tooth enamel V. Fearnhead RW, editor. Yokohama: Florence Publishers, pp. 41-50.
107.
Michalak M., Baksh S., Opas M. ( 1991). Identification and immunolocalization of calreticulin in pancreatic cells: no evidence for 'calciosomes'. Exp Cell Res197:91-99.
108.
Miller A., Bronner F. (1981). Calcium uptake in isolated brush-border vesicles from rat small intestine. Biochem J196:391-401.
109.
Mitic LL, Anderson JM (1998). Molecular architecture of tight junctions. Ann Rev Physiol60:121-142.
110.
Mogami H., Nakano K., Tepikin AV, Petersen OH (1997). Ca2+ flow via tunnels in polarized cells. Recharging of apical Ca2+ stores by focal Ca2+ entry through basal membrane patch. Cell88:49-55.
111.
Mogami H., Tepikin A., Petersen OH (1998). Termination of cytosolic Ca2+ signals. Ca2+ reuptake into intracellular stores is regulated by the free Ca2+ concentration in the store lumen. EMBO J17:435-442.
112.
Mollgard K., Rostgaard J. (1978). Morphological aspects of some sodium transporting epithelia suggesting a transcellular pathway viaelements of the endoplasmic reticulum. J Membr Biol40:71-89.
113.
Mollgard K., Rostgaard J. (1981). Morphological aspects of transepithelial transport with special reference to the endoplasmic reticulum. In: Ion transport by epithelia. Schultz SG, editor. New York: Raven Press, pp. 209-231.
114.
Moran RA, Deaton TG, Bawden JW (1995). Problems associated with estimation of net calcium uptake during enamel formation using 45Ca. J Dent Res74:698-701.
115.
Moreno EC, Aoba T. ( 1987). Calcium binding in enamel fluid and driving force for enamel mineralization in the secretory stage of amelogenesis. Adv Dent Res1:245-251.
116.
Moreno EC, Aoba T. ( 1991). Comparative solubility study of human dental enamel, dentin and hydroxyapatite. Calcil Tissue Int49:6-13.
117.
Nanci A., Warshawsky H. (1984). Characterization of putative secretory sites on ameloblasts of the rat incisor. Am J Anat171:163-189.
118.
Nanci A., Uchida T., Warshawsky H. (1987). The effects of vinblastine on the secretory ameloblasts. An ultrastructural, cytochemical and immunocytochemical study in the rat incisor. Anat Rec219:113-126.
119.
Nanci A., Ahluwalia JP, Pompura JR, Smith CE (1989). Biosynthesis and secretion of enamel proteins in the rat incisor. Anat Rec224:277-291.
120.
Nanci A., Zalzal S., Kan FWK (1993). High-resolution scanning electron microscopy of rat incisor ameloblasts. Scanning Microscopy7:165-175.
121.
Nassar CF, Khairallah EW, Nasser MG, Habbal ZM (1988). Cytoskeletal control of calcium absorption across the rat small intestine. Comp Biochem Physiol89:197-201.
122.
Nellans HN (1990). Intestinal calcium absorption. Interplay of paracellular and cellular pathways. Miner Electrolyte Metab16:101-108.
123.
Nemere I. (1990). Organelles that bind calcium. In: Intracellular calcium regulation. Bronner F, editor. New York: Alan R. Liss, pp. 163-179.
124.
Nemere I. (1992). Vesicular calcium transport in chick intestine. J Nutr122:657-661.
125.
Nemere I., Leathers V., Norman AW (1986). 1,25-dihydroxyvitamin D3-mediated intestinal calcium transport. Biochemical identification of lysosomes containing calcium and calcium-binding protein (calbindin-D28k). J Biol Chem261:16106-16114.
126.
Nemere I., Leathers V., Thompson BS, Luben RA, Norman AW (1991). Redistribution of calbindin-D28k in chick intestine in response to calcium transport. Endocrinology129:2972-2984.
127.
Nemere I., Opperman LA, Ross FP, Norman AW (1992). Noncytoplasmic and filamentous appearance of calbindin-D28k and tubulin in double, indirect immunofluorescent staining of chick embryonic tissue. Mol Cell Endocrinol86:83-91.
128.
Neville MC, Watters CD (1983). Secretion of calcium into milk [review]. J Dairy Sci66:371-380.
129.
Nicaise G., Maggio K., Thirion S., Horoyan M., Keicher E. (1992). The calcium loading of secretory granules. A possible key event in stimulus-secretion coupling. Biol Cell75:89-99.
130.
Ozawa H., Yamada M., Uchida T., Yamamoto T., Takano Y. (1983). Fine structural and cytochemical studies on the Golgi-SER system of ameloblasts with special reference to its resorptive function. In: Mechanisms of tooth enamel formation. Suga S, editor. Tokyo: Quintessence, pp. 17-48.
131.
Parekh AB, Penner R. (1997). Store depletion and calcium influx. Physiol Rev77:901-930.
132.
Peng JB, Chen XZ, Berger UV, Vassilev PM, Tsukaguchi H., Brown EM, et al. (1999). Molecular cloning and characterization of a channel-like transporter mediating intestinal calcium absorption. J Biol Chem274: 22739-22746.
133.
Peng JB, Chen XZ, Berger UV, Vassilev PM, Brown EM, Hediger MA (2000). A rat kidney-specific calcium transporter in the distal nephron. J Biol Chem275: 28186-28194.
134.
Pindborg JJ (1982). Aetiology of developmental enamel defects not related to fluorosis. Int Dent J32:123-134.
135.
Pozzan T., Rizzuto R., Volpe P., Meldolesi J. (1994). Molecular and cellular physiology of intracellular calcium stores. Physiol Rev74:595-636.
136.
Qvortrup K., Rostgaard J. (1990). Three-dimensional organization of a transcellular tubulocisternal endoplasmic reticulum in epithelial cells of Reissner's membrane in the guinea pig. Cell Tissue Res261:287-299.
137.
Reith EJ, Boyde A. (1981). Autoradiographic evidence of cyclical entry of calcium into maturing enamel of the rat incisor tooth. Arch Oral Biol26:983-987.
138.
Reith EJ, Boyde A., Schmid MI (1982). Correlation of rat incisor ameloblasts with maturation cycles as displayed on enamel surface with EDTA. J Dent Res61:1563-1573.
139.
Reith EJ, Schmid MJ, Boyde A. (1984). Rapid uptake of calcium in maturing enamel of the rat incisor. Histochemistry80:409-410.
140.
Renard-Rooney DC, Hajnoczky G., Seitz MB, Schneider TG, Thomas AP (1993). Imaging of inositol 1,4,5-trisphosphate-induced Ca2+ fluxes in single permeabilized hepatocytes. J Biol Chem268:23601-23610.
141.
Risnes S. (1979). A method of calculating the speed of movement of ameloblasts during rat incisor amelogenesis. Arch Oral Biol24:299-306.
142.
Roberts WM (1993). Spatial calcium buffering in saccular hair cells. Nature363:74-76.
143.
Robinson C., Hiller CR, Weatherell JA (1974). Uptake of 32P-labelled phosphate into developing rat incisor enamel. Calcif Tissue Res15:143-152.
144.
Robinson C., Fuchs P., Deutsch D., Weatherell JA (1978). Four chemically distinct stages in developing enamel from bovine incisor teeth. Caries Res12:1-11.
145.
Rubinoff MJ, Nellans HN (1985). Active calcium sequestration by intestinal microsomes. Stimulation by increased calcium load. J Biol Chem260:7824-7828.
146.
Sanderson MJ, Charles AC, Boitano S., Dirksen ER (1994). Mechanisms and function of intercellular calcium signalling. Mol Cell Endocrinol98:173-187.
147.
Sasaki S., Takagi T., Suzuki M. (1991). Cyclical changes in pH in bovine developing enamel as sequential bands. Arch Oral Biol36:227-231.
148.
Sasaki S., Ishibashi I., Marumo F. (1998). Aquaporin-2 and -3. Representatives of two subgroups of the aquaporin family colocalized in the kidney collecting duct. Ann Rev Physiol60:199-220.
149.
Sasaki T., Garant PR (1987). Mitochondrial migration and Ca-ATPase modulation in secretory ameloblasts of fasted and calcium-loaded rats. Am J Anat179:116-130.
150.
Sasaki T., Colflesh DE, Garant PR (1987). Calcium transport by a calmodulin-regulated Ca-ATPase in the enamel organ. Adv Dent Res1:213-226.
151.
Sasaki T., Higashi S., Tachikawa T., Yoshiki S. (1982). Formation of tight junctions in differentiating and secretory ameloblasts of rat molar tooth germs. Arch Oral Biol27:1059-1068.
152.
Sasaki T., Higashi S., Tachikawa T., Yoshiki S. (1983a). Morphology and permeability of junctional complexes in maturing rat ameloblasts of rat incisors. Acta Anat116:74-83.
153.
Sasaki T., Higashi S., Tachikawa T., Yoshiki S. (1983b). Thin-section, tracer and freeze-fracture study of the smooth-ended maturation ameloblasts in rat incisors. Acta Anat117:303-313.
154.
Schroeder B., Dahl MR, Breves G. (1998). Duodenal Ca2+ absorption is not stimulated by calcitriol during early postnatal development of pigs. Am J Physiol275:G305-G313.
155.
Sibley CP (1994). Mechanisms of ion transfer by the rat placenta. A model for human placenta? Placenta15:675-691
156.
Simmer JP, Fincham AG (1995). Molecular mechanisms of dental enamel formation. Crit Rev Oral Biol Med6:84-108.
157.
Smith CE (1984). Stereological analysis of organelle distribution within rat incisor enamel organ at successive stages of amelogenesis. INSERM125:273-282.
158.
Smith CE (1998). Cellular and chemical events during enamel maturation. Crit Rev Oral Biol Med9:128-161.
159.
Smith CE, Nanci A. (1989). A method for sampling the stages of amelogenesis on mandibular rat incisors using the molars as a reference for dissection. Anat Rec225:257-266.
160.
Smith CE, Nanci A. (1995). Overview of morphological changes in enamel organ cells associated with major events in amelogenesis. Int J Dev Biol39:153-161.
161.
Smith CE, Warshawsky H. (1977). Quantitative analysis of cell turnover in the enamel organ of the rat incisor. Acta Anat187:63-98.
162.
Smith CE, McKee MD, Nanci A. (1987). Cyclic induction and rapid movement of sequential waves of new smooth-ended ameloblast modulation bands in rat incisors as visualized by polychrome fluorescent labeling and GBHAstaining of maturing enamel. Adv Dent Res1:162-175.
163.
Smith CE, Dahan S., Fazel A., Lai W., Nanci A. (1992). Correlated biochemical and radioautographic studies of protein turnover in developing rat incisor enamel following pulse-chase labeling with L-[35S]- and L-[methyl-3H]-methionine. Anat Rec232:1-14.
164.
Smith CE, Nanci A., DenBesten PK (1993). Effects of chronic fluoride exposure on morphometric parameters defining the stages of amelogenesis and ameloblast modulation in rat incisors. Anat Rec237:243-258.
165.
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 Res10:159-169.
166.
Speksnijder JE, Miller AL, Weisenseel MH, Chen TH, Jaffe LF (1989). Calcium buffer injections block fucoid egg development by facilitating calcium diffusion. Proc Natl Acad Sci USA86:6607-6611.
167.
Spencer R., Charman M., Wilson P., Lawson E. (1976). Vitamin D-stimulated intestinal calcium absorption may not involve calcium-binding protein directly. Nature263:161-163.
168.
Spencer R., Charman M., Wilson PW, Lawson DEM (1978). The relationship between vitamin D-stimulated calcium transport and intestinal calcium-binding protein in the chicken. Biochem J170:93-101.
169.
Spring KR (1998). Routes and mechanisms of fluid transport by epithelia. Ann Rev Physiol60:105-119
170.
Stein WD (1992). Facilitated diffusion of calcium across the rat intestinal cell. J Nutr122:651-656.
171.
Subramanian K., Meyer T. (1997). Calcium-induced restructuring of nuclear envelope and endoplasmic reticulum calcium stores. Cell89:963-971.
172.
Suga S. ( 1982). Progressive mineralization pattern of developing enamel during the maturation stage. I Dent Res61:1532-1542.
173.
Takano Y. (1994). Histochemical aspects of calcium regulation by the enamel forming cells during matrix formation and maturation. Acta Anat Nippon69:106-122.
174.
Takano Y. (1995). Enamel mineralization and the role of ameloblasts in calcium transport. Connect Tissue Res33:127-137.
175.
Takano Y., Akai M. ( 1988). Histochemical, ultrastructural and x-ray microprobe analytical studies of localization of calcium in the mucous lining of the rat duodenum. Histochemistry89:429-436.
176.
Takano Y., Crenshaw MA (1980). The penetration of intravascularly perfused lanthanum into the ameloblast layer of developing rat molar teeth. Arch Oral Biol25:505-511.
177.
Takano Y., Ozawa H. (1980). Ultrastructural and cytochemical observations on the alternating morphological changes in ameloblasts at the stage of enamel maturation. Arch Histol Jpn43:385-399.
178.
Takano Y., Crenshaw MA, Reith EI (1982). Correlation of 45Ca incorporation with ameloblast morphology in the rat incisor. Calcif Tissue Int34:211-213.
179.
Takano Y., Matsuo S., Wakisaka S., Ichikawa H., Nishikawa S., Akai M. ( 1987). The influence of vanadate on calcium uptake in maturing enamel of the rat incisor. J Dent Res66:1702-1707.
180.
Takano Y., Matsuo S., Wakisaka S., Ichikawa H., Nishikawa S., Akai M. ( 1988). A histochemical demonstration of calcium in the maturation stage enamel organ of rat incisors. Arch Histol Cytol51:241-248.
181.
Takano Y., Matsuo S., Wakisaka S., Ichikawa H., Nishikawa S., Akai M. ( 1989). Histochemical localization of calcium in the enamel organ of rat incisors in early-stage amelogenesis. Acta Anat134:305-311.
182.
Takano Y., Hanawa M., Yamamoto T., Domon T., Fujinami H., Hanaizumi Y., et al. (1990a). Time-related changes in the distribution of 45Ca in the developing enamel of rat incisors as revealed by radioautography. J Biol Buccale18:135-147.
183.
Takano Y., Yamamoto T., Domon T., Wakita M. (1990b). Histochemical, ultrastructural and electron microprobe analytical studies on the localization of calcium in rat incisor ameloblasts at early stage amelogenesis. Anat Rec228:123-131.
184.
Takano Y., Crenshaw MA, Bawden JW (1992). Calcium movement in vivo and in vitro in secretory-stage enamel of rat incisors. Arch Oral Biol37:377-383.
185.
Taylor AN (1984). Tooth formation and the 28,000-dalton vitamin D-dependent calcium-binding protein. J Histochem Cytochem32:159-164.
186.
Taylor AN, Gleason WA, Lankford GL (1984). Rat intestinal vitamin D-dependent calcium-binding protein: immunocytochemical localization in ameloblasts. J Dent Res63:94-97.
187.
Taylor CW, Broad LM (1998). Pharmacological analysis of intracellular Ca2+ signalling. Problems and pitfalls. Trends Pharmacol Sci19:370-375.
188.
Timmermans JAH, Bindels RJM, van Os CH (1995). Stimulation of plasma membrane Ca2+ pump by calbindin-D28k and calmodulin is additive in EGTA-free solutions. J Nutr125:1981S-1986S.
189.
Tribe RM, Borin ML, Blaustein MP (1994). Functionally and spatially distinct Ca2+ stores are revealed in cultured vascular smooth muscle cells. Proc Natl Acad Sci USA91:5908-5912.
190.
Trump BF, Berezesky IK (1995). Calcium-mediated cell injury and cell death. FASEB J9:219-228.
191.
Tuan RS ( 1985). Ca2+-binding protein of the human placenta. Biochem J227:317-326.
192.
Tuan RS, Cavanaugh ST (1986). Identification and characterization of a calcium-binding protein in the mouse chorioallantoic placenta. Biochem J233:41-49.
193.
Tucci J., Hammond V., Senior PV, Gibson A., Beck F. ( 1996). The role of fetal parathyroid hormone-related protein in transplacental calcium transport. J Mol Endocrinol17:159-164.
194.
Uchida T., Warshawsky H. (1992). Zinc iodide-osmium tetroxide impregnation of the tubulo-vesicular system in Tomes' process of the rat incisor ameloblast. Anat Rec232:325-339.
195.
Uchida T., McKee MD, Warshawsky H. (1987). A radioautographic study of the effects of vinblastine on the fate of injected 45calcium and [125I]-insulin in the rat incisor. Arch Oral Biol32:433-437.
196.
van Os CH (1987). Transcellular calcium transport in intestinal and renal epithelial cells. Biochim Biophys Acta905:195-222.
197.
Vicars TM, Stanfield CN, Crenshaw MA, Bawden JW (1983). The effects of ATP depletion and ionophore A23187 on calcium transport in the secretory rat enamel organ. Arch Oral Biol28:513-516.
198.
Warshawsky H. (1978). A freeze-fracture study of the topographic relationship between inner enamel-secretory ameloblasts in the rat incisor. Am J Anat152:153-208.
199.
Warshawsky H. (1988). Formation of enamel and dentin: a critical review. CRC Crit Rev Anat Cell Biol1:425-460.
200.
Wasserman RH, Fullmer CS (1995). Vitamin D and intestinal calcium transport: facts, speculations and hypotheses. J Nutr125:1971S-1979S.
201.
Wasserman RH, Chandler JS, Meyer SA, Smith CA, Brindak ME, Fullmer CS, et al. (1992). Intestinal calcium transport and calcium extrusion processes at the basolateral membrane. Nutr122:662-671.
202.
Wiemann M., Busselberg D., Schirrmacher K., Bingmann D. (1998). A calcium release activated calcium influx in primary cultures of rat osteoblast-like cells. Calcif Tissue Int63:154-159.
203.
Wilkins M., Sneyd J. (1998). Intercellular spiral waves of calcium. J Theoret Biol191:299-308.
204.
Winsky L., Kuznicki J. (1995). Distribution of calretinin, calbindin D28k and parvalbumin in subcellular fractions of rat cerebellum. Effects of calcium. J Neurochem65:381-388.
205.
Zaki AE, Hand AR, Mednieks MI, Eisenmann DR, Borke JL (1996). Quantitative immunocytochemistry of Ca2+-Mg2+ ATPase in ameloblasts associated with enamel secretion and maturation in the rat incisor. Adv Dent Res10:245-251.
206.
Zimmermann B., Lange K., Mertens P., Bernimoulin JP (1994). Inhibition of chondrogenesis and endochondral mineralization in vitro by different calcium channel blockers. Eur J Cell Biol63:114-121.
