Investigators - Charles E. Smith

Charles E. Smith

My research at the Laboratory for the Study of Calcified Tissues and Biomaterials centers on characterizing and defining three aspects of cellular controls which are involved in natural formation and mineralization of the enamel covering the crowns of teeth. These are: (1) secretory events leading to gradual formation of an organic-rich layer containing specific mixes of matrix proteins, proteinases, and initial mineral deposits, (2) events related to evoking specific changes and then outright proteolysis of the entire extracellular organ matrix as a prelude to secondary and more massive mineral acquisition, and (3) membrane transport systems involved in selective ion movement through the formative epithelial layer.

Experimental techniques being used include electron microscopy, SEM, immunohisto­chemistry, SDS-PAGE and immunoblotting, fluorescence microscopy, and in vitro modeling of mineralization processes.

  • Publications
Tsuchiya, M., Tye, C.E., Sharma, R., Smith, C.E. and Bartlett, J.D. (2008) XBP1 expression may determine the size of the ameloblast ER. J. Dent. Res., in press.

Hermo, L., Schellenberg, M., Lui, L.Y., Dayanandan, B., Zhanga, T., Mandato, C.A. and Smith, C.E. (2008) Membrane domain specificity in the spatial diatribution of aquaporins 5, 7, 9 and 11 in efferent ducts and epididymis of rats. J. Histochem. Cytochem., Sep 15 [Epub ahead of print]

Zalzal, S.F., Smith, C.E. and Nanci, A. (2008) Ameloblastin and amelogenin share a common secretory pathway and are co-secreted during enamel formation. Matrix Biol., 27: 352-359.The epithelially-derived ameloblasts secrete two main categories of extracellular matrix proteins, amelogenins (AMEL) and nonamelogenins. These proteins assume differential distributions in the forming enamel layer and thereby regulate deposition and structuring of the mineral phase. The objective of this study was to elucidate whether their distribution results from distinctive physicochemical behaviors or differences in intracellular routing. Dual-immunogold labeling was used to visualize the presence of AMEL and ameloblastin (AMBN), the major nonamelogenin, and quantify the proportion of secretory granules containing one or both of these proteins in ameloblasts during the phase of appositional growth of the enamel layer in continuously-erupting rat incisors. Some rats were treated with brefeldin A (BFA) to generate a synchronized cohort of newlyformed secretory granules....

Hu, J.C-C., Hu, Y., Smith, C.E., McKee, M.D., Wright, J.T., Yamakoshi, Y., Papagerakis, P., Hunter, G.K., Feng, J.Q., Yamakoshi, F., and Simmer, J.P. (2008) Enamel defects and ameloblast specific expression in Enamelin knockout/Lac Z knockin mice. J. Biol. Chem., 283: 10858-10871.Enamelin is critical for proper dental enamel formation, and defects in the human enamelin gene cause autosomal dominant amelogenesis imperfecta. We used gene targeting to generate a knockin mouse carrying a null allele of enamelin (Enam) that has a lacZ reporter gene replacing the Enam translation initiation site and gene sequences through exon 7. Correct targeting of the transgene was confirmed by Southern blotting and PCR analyses. No enamelin protein could be detected by Western blotting in the Enam-null mice. Histochemical X-gal staining demonstrated ameloblast-specific expression of enamelin. The enamel of the Enam+/- mice was nearly normal in the maxillary incisors but the mandibular incisors were discolored and tended to wear rapidly where they contacted the maxillary incisors...

Moffatt, P., Smith, C.E., St-Arnaud, R. and Nanci, A. (2008) Characterization of Apin, a secreted protein highly expressed in tooth associated epithelia. J. Cell. Biochem., 103: 941-956.We previously reported expression of a protein by enamel organ (EO) cells in rat incisors, originally isolated from the amyloid of Pindborg odontogenic tumors called Apin. The aim of the present study was to further characterize the Apin gene and its protein in various species, assess tissue specificity, and clarify its localization within the EO. Northern blotting and RT-PCR revealed that expression of Apin was highest in the EO and gingiva, moderate in nasal and salivary glands, and lowest in the epididymis. The protein sequences deduced from the cloned cDNA for rat, mouse, pig, and human were aligned together with those obtained from four other mammal genomes. Apin is highly conserved in mammals but is absent in fish, birds, and amphibians. Comparative SDS-PAGE analyses of the protein obtained from bacteria, transfected cells, and extracted from EOs all indicated that Apin is post-translationally modified, a finding consistent with the presence of predicted sites for phosphorylation and O-linked glycosylation. In rodent incisors, Apin was detected only in the ameloblast layer of the EO, starting at post-secretory transition and extending throughout the maturation stage...

Hermo, L., Chung, S., Gregory, M., Smith, C.E., Wang, S.P., El-Alfy, M., Cyr, D.G., Mitchell, G.A., and Trasler, J. (2008) Alterations in the testis of hormone sensitive lipase-deficient mice is associated with decreased sperm counts, sperm motility and fertility. Mol. Reprod. Dev., 75: 565-577.Hormone-sensitive lipase (HSL, Lipe, E.C.3.1.1.3) functions as a triglyceride and cholesteryl esterase, supplying fatty acids, and cholesterol to cells. Gene-targeted HSL-deficient (HSL/) mice reveal abnormal spermatids and are infertile at 24 weeks after birth. The purpose of this study was to follow the evolution of spermatid abnormalities as HSL/ mice age, characterize sperm motility in older HSL/ mice, and determine if mice expressing a human testicular HSL transgene (HSL/ttg) produce normal motile sperm. In situ hybridization indicated that HSL is expressed exclusively in steps 5-16 spermatids, but not in Sertoli cells. In HSL/ mice, abnormalities were evident in step 16 spermatids at 5 weeks after birth, with defects progressively increasing in spermatids with age...

Hermo, L., Korah, N., Gregory, M., Liu, Y.L., Cyr, D.G., d'Azzo, A. and Smith, C.E. (2007) Structural alterations of epididymal epithelial cells in Cathepsin A-deficient mice affect the blood epididymal barrier and lead to altered sperm motility. J. Androl., 28: 784-797.Past studies have shown that the epithelial lining of the epididymis in adult mice deficient in protective protein cathepsin A (PPCA 2/2) becomes swollen and vacuolated as a result of an accumulation of pale lysosomes, some very large, in addition to the presence of an abundance of macrophages infiltrating the intertubular spaces. The purpose of this study was to assess the integrity of the epididymal epithelial-blood barrier in these altered mice by characterizing the distribution of claudins (Cldns) and the leakiness of tight junctions to lanthanum nitrate. A second goal was to characterize sperm motility behavior in PPCA 2/2 mice using computer-assisted sperm analyses (CASA). The results indicated that lanthanum nitrate penetrated apical junctional complexes between adjacent epithelial cells and entered the epididymal lumen in PPCA 2/2 mice but not in control PPCA +/+ mice...

Primiani, N., Gregory, M., Dufresne, J., Smith, C. E., Lui, Y.L., Bartles, J. R., Cyr, D. G. and Hermo, L. (2007) Microvillar size and espin expression in principal cells of the adult rat epididymis are regulated by androgens. J. Androl., 28: 659-669.Principal cells of the epididymis are the most prominent cell type and are noted for an apical cell surface studded with microvilli. The latter contain channel proteins that condition the microenvironment of epididymal lumen and promote sperm maturation; however, the regulation of the structure and integrity of microvilli is not well known. Espins are a family of proteins implicated in microvillar growth. The objectives of this study were to assess the regulation of espin in epididymal principal cells both in vitro and in vivo. Treatment of immortalized rat caput epididymal (RCE) cells with increasing doses of a homogenized testicular extract revealed a dose-dependent increase in the size of microvilli. Reverse transcriptase-polymerase chain reaction (RT-PCR) of adult rat epididymal RNA using espin-specific primers indicated the presence of a band at about 290 base pairs (bp) in all regions...

Wazen, R. M., Tye, C. E., Goldberg, H. A., Hunter, G. K., Smith, C. E. and Nanci, A. (2007) In Vivo Functional Analysis of Polyglutamic Acid Domains in Recombinant Bone Sialoprotein. J. Histochem. Cytochem., 55(1): 35-42.Bone sialoprotein (BSP) is an anionic phosphoprotein expressed in mineralizing connective tissues that binds to hydroxyapatite and nucleates its formation in vitro. Two polyglutamic acid regions (poly [E]) are believed to participate in these activities. The aim of this study was to evaluate the contribution of these acidic regions to the binding of prokaryote recombinant BSP (prBSPE) within an actual in vivo environment. Full-length prBSPE and prBSPE in which the poly [E] domains were replaced by polyalanine (prBSPA) were tagged with dinitrophenol (DNP). The tagged preparations comprised intact molecules and some fragmented forms.....

Khatchadourian, K., Smith, C.E., Metzler, M., Gregory, M., Hayden, M.R., Cyr, D.G. and Hermo, L. (2007) Structural abnormalities in spermatids together with reduced sperm counts and motility underlie the reproductive defect in HIP1 -/- mice. Mol. Reprod. Dev., 74: 341-359.Huntingtin interacting protein 1 (HIP1) is an endocytic adaptor protein with clathrin assembly activity that binds to cytoplasmic proteins, such as F-actin, tubulin, and huntingtin (htt). To gain insight into diverse functions of HIP1, we characterized the male reproductive defect of HIP1/ mice from 7 to 30 weeks of age. High levels of HIP1 protein were expressed in the testis of wild-type mice as seen by Western blots and as a reaction over Sertoli cells and elongating spermatids as visualized by immunocytochemistry. Accordingly, major structural abnormalities were evident in HIP1/ mice with vacuolation of seminiferous tubules caused by an apparent loss of postmeiotic spermatids and a significant reduction in mean profile area...

Moffatt, P., Smith, C.E., Sooknanan, R., St-Arnaud, R. and Nanci, A. (2006) Identification of secreted and membrane proteins in the rat incisor enamel organ using a signal-trap screening approach. Eur J. Oral Sci., 114 (Suppl.1): 139-146.The secretome represents the subset of proteins that are targeted by signal peptides to the endoplasmic reticulum. Among those, secreted proteins play a pivotal role because they regulate determinant cell activities such as differentiation and intercellular communication. In calcified tissues, they also represent key players in extracellular mineralization. This study was carried out to establish a secretome profile of rat enamel organ (EO) cells. A functional genomic technology, based on the signal trap methodology, was applied, starting with a library of 5¢-enriched cDNA fragments prepared from rat incisor EOs. A total of 2,592 clones were analyzed by means of macroarray hybridizations and DNA sequencing. Ninety-four unique clones encoding a signal peptide were retrieved...

Moffatt, P., Smith, C. E., St-Arnaud, R., Simmons, C., Wright, J. T., and Nanci, A. (2006) Cloning of rat amelotin and localization of the protein to the basal lamina of maturation stage ameloblasts and junctional epithelium. Biochem. J., 399: 37-46.Formation of tooth enamel is a very complex process in which a specific set of proteins secreted by ameloblasts play a primordial role. As part of a screening procedure to identify novel proteins secreted by EO (enamel organ) cells of rat incisors, we isolated a partial cDNA fragment (EO-017) that is the homologue of the recently describedmouse Amtn (amelotin) gene [Iwasaki, Bajenova, Somogyi-Ganss, Miller, Nguyen, Nourkeyhani, Gao,Wendel and Ganss (2005) J. Dent. Res. 84, 1127–1132]. Presented herein is the cloning of rat and pig full-length cDNAs with their deduced protein sequences...

Ruz, R., Gregory, M., Smith, C.E., Cyr, D.G., Lubhan, D.B., Hess, R.A. and Hermo, L. (2006) Expression of aquaporins in the efferent ductules, sperm counts, and sperm motility in estrogen receptor-alpha deficient mice fed lab chow versus casein. Mol. Reprod. Dev., 73: 226-237.Estrogens play an important role in the male reproductive tract, and this is especially so for the efferent ductules, where a-estrogen receptors (ERa) have been localized. Mice deficient in ERa (aERKO mice) are infertile, and the effect appears to be due in part to retention of water at the level of the efferent ductules. In the present study, we examined the consequences of ERa deletion on the distribution of certain aquaporins (AQPs), water protein channels, in the efferent ductules and on sperm numbers and motility...

Smith, C.E., Nanci A., and 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): 147-153.During screening of a rat incisor enamel organ cDNA library by signal peptide trap technology, we identified a DNA fragment matching a predicted translation sequence for rat carbonic anhydrase 6 (CA6). This result was unexpected because CA6, to date, has been associated primarily with secretions from glandular tissues. To further characterize this observation, reverse transcription–polymerase chain reaction (RT– PCR) amplifications were carried out on total RNA extracted from freeze-dried secretory and maturation-stage rat incisor enamel organs. A cDNA fragment of the expected size was detected in control samples from rat salivary glands as well as within maturation-stage enamel organ samples. This CA6 RT–PCR fragment was further cloned and sequenced and found to match the nucleotide sequence 770–1079 from clone XM_216584 of GenBank...

Grover, A., Smith, C.E., Gregory, M., Cyr, D.G., Ram Sairam, M. and Hermo, L. (2005) Effects of FSH receptor deletion on epididymal tubules, sperm numbers and sperm mobility. Mol. Reprod. Dev.,72: 135-144.Follicle stimulating hormone (FSH) interacts with its cognate receptor (R) on Sertoli cells within the testis and plays an important role in the maintenance of spermatogenesis. Male FSH-R knock- out (FORKO) mice show fewer Sertoli cells and many that are structurally abnormal and as a consequence fewer germ cells. Lower levels of serum testosterone (T) and androgen binding protein (ABP) also occur, along with reduced fertility. To assess the effects of FSH-R depletion as an outcome of testicular abnorm- alities, sperm from the cauda epididymidis were count- ed and examined ultrastructurally. As reduced fertility may also reflect changes to the epididymis, the sec- ondary responses of the epididymis to lower T and ABP levels were also examined by comparing differences in sizes of epididymal tubules in various regions of FORKO and wild type (WT) mice...

Hermo, L., Lee Chong, D., Moffatt, P., Sly, W., Waheed, A. and Smith, C. E. (2005): Region and cell specific differences in the distribution of carbonic anhydrases II, III, XII, and XIV in the adult rat epididymis. J. Histochem. Cytochem., 53: 699-713.We employed RT-PCR followed by light microscope immunocytochemistry on St. Marie’s- and Bouin’s-fixed tissues to define the distribution of carbonic anhydrase (CA)isoforms in the male reproductive tract. The data revealed that CA II, III, IV, XII, and XIV were expressed in rat epididymis. Whereas CA III was found in principal cells of all epididymalregions, CA II was localized in narrow cells of the initial segment and principal cells of all regions...

Smith, C. E., Lee Chong, D., Bartlett, J.D. and Margolis, H.C. (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.The formation rates of mineral in developing enamel were determined by microweighing of incisors of mice and rats. Computations indicated that a large excess of hydrogen ions would result fromcreating apatite at the calculated rates. Enamel organ cells (ameloblasts), therefore, likely excrete bicarbonate ions to prevent pH in fluid bathing enamel from becoming too acidic.

Bartlett, J.D., Beniash, E., Lee, D.H. and Smith, C. E. (2004) Decreased mineral content in MMP-20 null mouse enamel is prominent during the maturation stage. J. Dent. Res., 83: 909-913.During enamel development, matrix metalloproteinase-20 (MMP-20, enamelysin) is expressed early during the secretory stage as the enamel thickens, and kallikrein-4 (KLK-4, EMSP1) is expressed later during the maturation stage as the enamel hardens. Thus, we investigated whether the physical properties of the secretory/ maturation-stage MMP-20 null enamel were significantly different from those of controls. We demonstrated that although, in relative terms, the weight percent of mature mineral in the MMP-20 null mouse enamel was only 7-16% less than that in controls, overall the enamel mineral was reduced by about 50%, and its hardness was decreased by 37%. Percent mineral content by weight was assessed at 3 different developmental stages. Remarkably, the biggest difference in mineral content between MMP-20 null and controls occurred in the nearly mature enamel, when MMP-20 is normally no longer expressed...

Grover, A., Ram Sairam, M., Smith, C. E. and Hermo, L. (2004) Structural and functional modifications of Sertoli cels in the testis of adult follicle-stimulating hormone receptor knockout mice. Biol. Reprod., 71: 117-129.

Korah, N., Smith, C. E., d’Azzo, A., Mui, J. and Hermo, L. (2003) Characterization of cell- and region-specific abnormalities in the epididymis of cathepsin A deficient mice. Mol. Reprod. Dev., 66: 358-373.

Korah, N., Smith, C. E., d’Azzo, A., El-Alfy, M. and Hermo, L. (2003) An increase in macrophages in the testis of cathepsin A deficient mice suggests an important role for these cells in the interstitial space of this tissue. Mol. Reprod. Dev., 64: 302-320.

DenBesten, P.K., Yan, Y., Featherstone, J.D.B., Hilton, J.F., Smith, C. E. and. Li, W. (2002) Effects of fluoride on enamel matrix proteinases. Archs. Oral Biol., 47: 763-770.

Orsini, G., Lavoie, P., Smith, C.E., and Nanci, A. (2001) Immunochemical characterization of a chicken egg yolk antibody to secretory forms of rat incisor amelogenin. J. Histochem. Cytochem., 49: 285-292.

Chen, W.-Y., Bell, A.W., Simmer, J.P. and Smith, C. E. (2000) Mass spectrometry of native rat amelogenins: primary transcripts, secretory isoforms and C-terminal degradation. J. Dent. Res., 79: 840-849.

Nanci, A. and Smith, C.E. (2000) Matrix-mediated mineralization in enamel and the collagen-based hard tissues. In: Proc. 6th Intl. Con. on Chem. Biol. Min. Tissue (C. Robinson, A. Boskey, M. Goldberg Eds.), Am. Acad. Orthoped. Sug., pp. 217-224.

Josephsen, K., Smith, C.E., and Nanci, A. (1999) Selective but nonspecific immunolabeling of enamel protein-associated compartments by a monoclonal antibody against vimentin. J. Histochem. Cytochem., 47: 1237-1245.

Smith, C. E. and Chen, W.-Y. (1998) Degradative changes in whole enamel homogenates incubated in vitro in the presence of low calcium ion concentrations. Connect. Tissue Res., 39: 379-391.

Smith, C. E. (1998) Cellular and chemical events during enamel maturation. Crit. Rev. Oral Biol. Med., 9: 128-161.

Nanci, A., Zalzal, S., Lavoie, P., Kunikata, M., Chen, W.-Y., Krebsbach, P.H., Yamada, Y., Hammarström, L., Simmer, J.P., Fincham, A.G., Snead, M.L., and Smith, C.E. (1998) Comparative immunochemical analyses of the developmental expression and distribution of ameloblastin and amelogenin in rat incisors. J. Histochem. Cytochem., 46: 911-934.

Hermo, L. and Smith, C. E. (1998) The structure of the Golgi apparatus: a sperm’s eye view in principal epithelial cells of the rat epididymis. Histochem & Cell Biol., 109: 431-447.

Chen, W.-Y., Lu, L., McDonald, K., Osmond, D.G. and Smith, C. E. (1998) Isolation of amelogenin-positive ameloblasts from rat mandibular incisor enamel organs by flow cytometry and fluoresence-activated cell sorting. Connect. Tissue Res., 39: 9-15.

Smith, C.E. and Nanci, A. (1996) The protein dynamics of amelogenesis. Anat. Rec., 245: 186-207.

Smith, C. E., Issid, M., Margolis, H.C. and Moreno, E.C. (1996) Developmental changes in the pH of enamel fluid and its effects on matrix-resident proteinases. Adv. Dent. Res., 10: 159-169.

Lee, E.R., Smith, C. E. and Poole, A.R. (1996) Ultrastructural localization of the C-propeptide released from type II procollagen in fetal-bovine growth plate cartilage. J. Histochem. Cytochem., 44: 433-443.

Nanci, A., Hashimoto, J., Zalzal, S., and Smith, C.E. (1996) Transient accumulation of proteins at interrod and rod enamel growth sites. Adv. Dent. Res., 10: 135-149.

Smith, C.E. and Nanci, A. (1995) Overview of morphological changes in enamel organ cells associated with major events in amelogenesis. Int. J. Dev. Biol., 39: 153-161.

Smith, C. E., Chen, W.-Y, Issid, M. and Fazel, A. (1995) Enamel matrix protein turnover during amelogenesis: basic biochemical properties of short-lived sulfated enamel proteins. Calcif. Tissue Int., 57: 133-144.

Chen, W.-Y., Nanci, A., and Smith, C.E. (1995) Immunoblotting studies on artifactual contamination of enamel homogenates by albumin and other proteins. Calcif. Tissue Int., 57: 145-151.

Smith, C.E., Nanci, A., and DenBesten, P.K. (1993) Effects of chronic fluoride exposure on morphometric parameters defining the stages of amelogenesis and ameloblast modulation in rat incisors. Anat. Rec., 237: 243-258.

Smith, C.E., Dahan, S., Fazel, A., Lai, W., and 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. Rec., 232: 1-14.

Nanci, A. and Smith, C.E. (1992) Development and calcification of enamel. In: Mineralization in Biological Systems. Edited by E. Bonucci, CRC Press, Boca Raton, Chapter 13, pp. 313-343.

Nanci, A., McKee, M.D., and Smith, C.E. (1992) Immunolocalization of enamel proteins during amelogenesis in the cat. Anat. Rec., 233: 335-349.

Berdal, A., Nanci, A., Smith, C.E., Ahluwalia, J.P., Thomasset, M., Cuisinier-Gleizes, P., and Mathieu, H. (1991) Differential expression of calbindin-D 28 kDa in rat incisor ameloblasts throughout enamel development. Anat. Rec., 230: 149-163.

Smith, C. E., Hermo, L., Fazel, A., Lalli, M.F. and Bergeron, J.J.M. (1990) Ultrastructural distribution of NADPase within the Golgi apparatus and lysosomes of mammalian cells. Prog. Histochem. Cytochem., 21(3):1-124.

Nanci, A., Zalzal, S., and Smith, C.E. (1990) Routine use of backscattered electron imaging to visualize cytochemical and autoradiographic reactions in semi-thin plastic sections. J. Histochem. Cytochem., 38: 403-414.

Smith, C.E., Pompura, J.R., Borenstein, S., Fazel, A., and Nanci, A. (1989) Degradation and loss of matrix proteins from developing enamel. Anat. Rec., 224: 292-316.

Smith, C.E. and Nanci, A. (1989) A method for sampling the stages of amelogenesis on mandibular rat incisors using the molars as a reference for dissection. Anat. Rec., 225: 257-266.

Smith, C.E. and Nanci, A. (1989) Secretory activity as a function of the development and maturation of ameloblasts. Connect. Tissue Res., 22: 147-156.

Smith, C.E., Borenstein, S., Fazel, A. and Nanci, A. (1989): In vitro studies of the proteinases which degrade amelogenins in developing rat incisor enamel. In: Tooth Enamel V. Edited by R. W. Fearnhead, Florence Publishers, Yokohama, pp. 286-290.

McKee, M.D., Nanci, A., Smith, C.E. and Warshawsky, H. (1989) Cyclical aspects of enamel maturation and the role of ruffle-ended and smooth-ended ameloblasts. In: Tooth Enamel V. Edited by R. W. Fearnhead, Florence Publishers, Yokohama, pp.41-45.

Nanci, A., Bitton, G.M., Ahluwalia, J.P. and Smith, C.E. (1989): Degradation of newly formed enamel proteins in relation to the secretory activity of ameloblasts. In: Tooth Enamel V. Edited by R. W. Fearnhead, Florence Publishers, Yokohama, pp. 69-73.

Nanci, A., Ahluwalia, J.P., Pompura, J.R., and Smith, C.E. (1989) Biosynthesis and secretion of enamel proteins in the rat incisor. Anat. Rec., 224: 277-291.

Nanci, A., Ahluwalia, J.P., Zalzal, S., and Smith, C.E. (1989) Cytochemical and biochemical characterization of glycoproteins in forming and maturing enamel of the rat incisor. J. Histochem. Cytochem., 37: 1619-1633.

Risnes, S., Smith, C. E. and Warshawsky, H. (1989) An approach to determine if ameloblasts move transversely during rat incisor amelogenesis. In: Tooth Enamel V. Edited by R.W. Fearnhead, Florence Publishers, Yokohama, pp. 196-200.

Bergeron, J.J.M., Kay, D.G., Lai, W.H., Doherty, J.J., Smith, C. E., Khan, M.N. and Posner, B.I. (1988) Functional characteristics of endosomes in rat liver parenchyma. In: Progress in Clinical and Biological Research: Cell Free Analysis of Membrane Traffic, Vol 270. Edited by D.J. Morré, K.E. Howell, G.M.W. Cook, and W.H. Evans, Alan R. Liss Inc., New York, pp. 391-409.

McKee, M.D., Wedlich, L., Pompura, J.R., Nanci, A., Smith, C.E., and Warshawsky, H. (1988) Demonstration by staining and autoradiography of cyclical distributions of protein at the enamel surface in rat incisors. Arch. Oral Biol., 33: 413-423.

Nanci, A. and Smith, C.E. (1988) Les protéines de l'émail dentaire. Etude immunocytochimique de l'amélogenèse. M/S, 4: 42-45.

Smith, C.E., McKee, M.D., and 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 GBHA-staining of maturing enamel. Adv. Dent. Res., 1: 162-175.

Nanci, A., Zalzal, S., and Smith, C.E. (1987) Application of backscattered electron imaging and lectin-gold cytochemistry to visualize the distribution of glycoconjugates in a basal lamina. Scan. Microsc., 1: 1963-1970.

Nanci, A., Slavkin, H.C., and Smith, C.E. (1987) Immunocytochemical and radioautographic evidence for secretion and intracellular degradation of enamel proteins by ameloblasts during the maturation stage of amelogenesis in rat incisors. Anat. Rec., 217: 107-123.

Nanci, A., Slavkin, H.C., and Smith, C.E. (1987) Application of high-resolution immunocytochemistry to the study of the secretory, resorptive, and degradative functions of ameloblasts. Adv. Dent. Res., 1: 148-161.

Paiement, J., Rindress, D., Smith, C. E., Poliquin, L. and Bergeron, J.J.M. (1987) Properties of a GTP sensitive microdomain in rough microsomes. Biochim. Biophys. Acta, 898: 6-22.

Smith, C. E., Paiement, J. and Bergeron, J.J.M. (1986) Subcellular distribution of acid NADPase activity within the parenchymal cells of rat liver. J. Histochem. Cytochem., 34: 649-658.

Bergeron, J.J.M., Paiement, J., Khan, M.N. and Smith, C. E. (1985) Terminal glycosylation in rat hepatic Golgi fractions: heterogeneous locations for sialic acid and galactose acceptors and their transferases. Biochim. Biophys. Acta, 821: 393-403.

Smith, C. E. (1984) Stereological analysis of organelle distribution within rat incisor enamel organ at successive stages of amelogenesis. In: Tooth Morphogenesis and Differentiation. Edited by A.B. Belcourt and J.-V. Ruch, INSERM, Vol. 125, Paris, pp. 273-282.

Parsons, S.M. and Smith, C. E. (1984) Ultrastructural localization of nicotinamide adenine dinucleotide phosphatase (NADPase) activity within columnar, goblet and Paneth cells of rat small intestine. J. Histochem. Cytochem., 32: 989-997.

Smith, C. E. (1981) Ultrastructural localization of coenzyme A phosphatase (CoA-Pase) activity to the GERL system in secretory ameloblasts of the rat incisor. J. Histochem. Cytochem., 29: 1243-1254.

Smith, C. E. (1981) Correlated biochemical and cytochemical studies of nicotinamide adenine dinucleotide phosphatase (NADPase) activity in ameloblasts using structural analogues of NADP. J. Histochem. Cytochem., 29: 822-836.

Smith, C. E. (1980) Effect of glutaraldehyde and decalcifying agents on acid phosphomonoester hydrolase activity in the enamel organ of the rat incisor: a biochemical study comparing enamel organ with liver. J. Histochem. Cytochem., 28: 689-699.

Smith, C. E. (1980) Ultrastructural localization of nicotinamide adenine dinucleotide phosphatase (NADPase) activity to the intermediate saccules of the Golgi apparatus in rat incisor ameloblasts. J. Histochem. Cytochem., 28: 16-26.

Smith, C. E. (1980) Cell turnover in the odontogenic organ of the rat incisor as visualized by graphic reconstruction following a single injection of 3H-thymidine. Am. J. Anat., 158: 321-343.

Smith, C. E. (1979) Ameloblasts: secretory and resorptive functions. J. Dent. Res., 58: 695-706.

Smith, C. E. and Warshawsky, H. (1977) Multinucleate ameloblasts in the rat incisor. Anat. Rec., 188: 407-416.

Smith, C. E. and Warshawsky, H. (1977) Quantitative analysis of cell turnover in the enamel organ of the rat incisor: evidence for ameloblast death immediately after enamel matrix secretion. Anat. Rec., 187: 63-98.

Doty, S., Smith, C. E., Hand, A.R. and Oliver, C. (1977) Inorganic trimetaphosphatase as a histochemical marker for lysosomes in light and electron microscopy. J. Histochem. Cytochem., 25: 1381-1384.

Smith, C. E. and Warshawsky, H. (1976) Movement of entire cell populations during renewal of the rat incisor as shown by radioautography after labeling with 3H-thymidine: the concept of the continuously differentiating cross sectional segment (with an appendix on the development of the periodontal ligament). Am. J. Anat., 145: 225-260.

Smith, C. E. and Warshawsky, H. (1975) Cellular renewal in the enamel organ and the odontoblast layer of the rat incisor as followed by radioautography using 3H-thymidine. Anat. Rec., 183: 523-562.

Smith, C. E. and Warshawsky, H. (1975) Histological and three dimensional organization of the odontogenic organ in the lower incisor of 100 gm rats. Am. J. Anat., 142: 403-430.

Smith, C. E. (1975) Histological and three dimensional organization of the odontogenic organ in the upper incisor of 100 gm rats: comparison to the lower incisor. Am. J. Anat., 142: 431-456.

Warshawsky, H. and Smith C. E. (1974) Morphological classification of rat incisor ameloblasts. Anat. Rec., 179: 423-446.

Smith, C. E. (1974) A method for preparing longitudinal semi-thin Epon sections of entire rat incisors. Arch. Oral Biol., 19: 1045-1048.

Smith, C. E. and Warshawsky, H. (1973) Radiographic determination of the length of maxillary and mandibular incisors in rats. J. Dent. Res., 52: 1234-1237.

Warshawsky, H. and Smith, C. E. (1971) A three dimensional reconstruction of the rods in rat maxillary incisor teeth. Anat. Rec., 169: 585-592.

©2009 Pedro A. Segura