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Salivary Amylase Induction by Tannin-Enriched Diets as a Possible Countermeasure Against Tannins

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Abstract

Tannins are characterized by protein-binding affinity. They have astringent/bitter properties that act as deterrents, affecting diet selection. Two groups of salivary proteins, proline-rich proteins and histatins, are effective precipitators of tannin, decreasing levels of available tannins. The possibility of other salivary proteins having a co-adjuvant role on host defense mechanisms against tannins is unknown. In this work, we characterized and compared the protein profile of mice whole saliva from animals fed on three experimental diets: tannin-free diet, diet with the incorporation of 5% hydrolyzable tannins (tannic acid), or diet with 5% condensed tannins (quebracho). Protein analysis was performed by one-dimensional gel electrophoresis combined with Matrix-Assisted Laser Desorption Ionization-Time of Flight mass spectrometry to allow the dynamic study of interactions between diet and saliva. Since abundant salivary proteins obscure the purification and identification of medium and low expressed salivary proteins, we used centrifugation to obtain saliva samples free from proteins that precipitate after tannin binding. Data from Peptide Mass Fingerprinting allowed us to identify ten different proteins, some of them showing more than one isoform. Tannin-enriched diets were observed to change the salivary protein profile. One isoform of α-amylase was overexpressed with both types of tannins. Aldehyde reductase was only identified in saliva of the quebracho group. Additionally, a hypertrophy of parotid salivary gland acini was observed by histology, along with a decrease in body mass in the first 4 days of the experimental period.

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References

  • Ahmed, N. K., Felsted, R. L., Bachur, and N. R. 1978. Heterogeneity of anthracycline antibiotic carbonyl reductases in mammalian livers. Biochem. Pharmacol. 27:2713–2719.

    Article  PubMed  CAS  Google Scholar 

  • Ahmed, A. E., Smithard, R., and Ellis, M. 1991. Activities of enzymes of the pancreas, and the lumen and mucosa of the small intestine in growing broiler cockerels fed on tannin-containing diets. Br. J. Nutr. 65:189–197.

    Article  PubMed  CAS  Google Scholar 

  • Ann, D. K., Clements, S., Johnstone, E. M., and Carlson, D. M. 1987. Induction of tissue-specific proline-rich protein multigene families in rat and mouse parotid glands by isoproterenol. Unusual strain differences of proline-rich protein mRNAs. J. Biol. Chem. 262:899–904.

    PubMed  CAS  Google Scholar 

  • Ann, D. K., Lin, H. H., and Kousvelari, E. 1997. Regulation of salivary gland specific gene expression. Crit. Rev. Oral Biol. Med. 8:244–252.

    PubMed  CAS  Google Scholar 

  • Bank, R. A., Hettema, H. E., Arwert, F., Amerongen, A. V., and Pronk, J. C. 1991. Electrophoretic characterization of post-translational modifications of human parotid salivary alpha-amylase. Electrophoresis 12:1032–1041.

    Article  Google Scholar 

  • Bedi, G. S. 1993. The effect of adrenergic agonists and antagonists on the expression of proteins in rat submandibular and parotid glands. Crit. Rev. Oral Biol. Med. 4:565–571.

    PubMed  CAS  Google Scholar 

  • Beeley, J. A., Sweeney, D., Lindsay, J. C., Buchanan, M. L., Sarna, L., and Khoo, K. S. 1991. Sodium dodecyl sulphate-polyacrylamide gel electrophoresis of human parotid salivary proteins. Electrophoresis 12:1032–1041.

    Article  PubMed  CAS  Google Scholar 

  • Bennick, A. 2002. Interaction of plant polyphenols with salivary proteins. Crit. Rev. Oral Biol. Med. 13:184–196.

    PubMed  Google Scholar 

  • Breslin, P. S. A., Gilmore, M. M., Beauchamp, G. K., and Green, B. G. 1993. Psychophysical evidence that oral astringency is a tactil sensation. Chem. Senses. 18:405–415.

    Article  CAS  Google Scholar 

  • Chatterton Jr, R. T., Vogelsong, K. M., Lu, Y. C., Ellman, A. B., and Hudgensg, A. 1996. Salivary alpha-amylase as a measure of endogenous adrenergic activity. Clin. Physiol. 16:433–448.

    PubMed  CAS  Google Scholar 

  • De Freitas, V., and Mateus, N. 2001. Structural features of procyanidin interactions with salivary proteins. J. Agric. Food Chem. 49:940–945.

    Article  PubMed  CAS  Google Scholar 

  • Denny, P. C., Mirels, L., and Denny, P. A. 1996. Mouse submandibular gland salivary apomucin contains repeated N-glycosylation sites. Glycobiology 6:43–50.

    Article  PubMed  CAS  Google Scholar 

  • Dlouhy, S. R., Taylor, B. A., and Karn, R. C. 1987. The genes for mouse salivary androgen-binding protein (ABP) subunits alpha and gamma are located on chromosome 7. Genetics 115:535–543.

    PubMed  CAS  Google Scholar 

  • Engelen, L., Van Den Keybus, P. A., De Wijk, R. A., Veerman, E. C., Amerongen, A. V., Bosman, F., Prinz, J. F., and Van Der Bilt, A. 2007. The effect of saliva composition on texture perception of semi-solids. Arch. Oral Biol. 52:518–525.

    Article  PubMed  CAS  Google Scholar 

  • Gallacher, D. V., and Petersen, O. H. 1983. Stimulus-secretion coupling in mammalian salivary glands. Int. Rev. Physiol. 28:1–52.

    PubMed  CAS  Google Scholar 

  • Gho, F., Pena-neira, A., and Lopez-solis, R. O. 2007. Induction of salivary polypeptides associated with parotid hypertrophy by gallotannins administered topically into the mouse mouth. J. Cell Biochem. 100:487–498.

    Article  PubMed  CAS  Google Scholar 

  • Gjorstrup, P. 1980. Taste and chewing as stimuli for the secretion of amylase from the parotid gland of the rabbit. Acta Physiol. Scand. 110:295–301.

    Article  PubMed  CAS  Google Scholar 

  • Glendinning, J. I. 1994. Is the bitter rejection response always adaptive? Physiol. Behav. 56:1217–1227.

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez, M. J., Peña, Y., Lillo, S., Alliende, C., and Lopez-solis, R. O. 2000. Cell-enlargement-related polypeptides are induced via beta(1)-adrenoceptors in mouse parotids. Exp. Mol. Pathol. 69:91–101.

    Article  PubMed  CAS  Google Scholar 

  • Gorr, S.-U., Venkatesh, S. G., and Darling, D. S. 2005. Parotid secretory granules: crossroads of secretory pathways and protein storage. J. Dent. Res. 84:500–509.

    PubMed  CAS  Google Scholar 

  • Granger, D. A., Kivlighan, K. T., El-Sheikh, M., Godis, E. B., and Stroud, L. R. 2007. Salivary alpha-amylase in biobehavioral research: recent developments and applications. Ann. N Y Acad. Sci. 1098:122–144.

    Article  PubMed  CAS  Google Scholar 

  • Hagerman, A. E., ice, M. E., and itchard, N. T. 1998. Mechanisms of protein precipitation for two tannins, pentagalloyl glucose and epicatechin (4-8) catechin (procyanidin). J. Agric. Food Chem. 46:2590–2595.

    Article  CAS  Google Scholar 

  • Hagenbüchle, O., Bovey, R., and Young, R. A. 1980. Tissue-specific expression of mouse α-amylase genes: Nucleotide sequence isoenzyme mRNAs from pancreas and salivary gland. Cell 21:179–187.

    Article  PubMed  Google Scholar 

  • Hardt, M., Witkowska, H. E., Webb, S., Thomas, L. R., Dixon, S. E., Hall, S. C., and Fisher, S. J. 2005a. Assessing the effects of diurnal variation in the composition of human parotid saliva: quantitative analysis of native peptides using iTRAQ reagents. Anal Chem. 77:4947–4954.

    Article  PubMed  CAS  Google Scholar 

  • Hardt, M., Thomas, L. R., Dixon, S. E., Newport, G., Agabian, N., Prakobphol, A., Hall, S. C., Witkowska, H. E., and Fisher, S. J. 2005b. Toward defining the human parotid gland salivary proteome and peptidome: identification and characterization using 2D SDS-PAGE, ultrafiltration, HPLC, and mass spectrometry. Biochemistry 44:2885–2899.

    Article  PubMed  CAS  Google Scholar 

  • Haslam, E. 1998. Practical Polyphenols: From Structure to Molecular Recognition and Physiological Action. Cambridge University Press, Cambridge.

    Google Scholar 

  • Henriksson, R. 1982. Beta 1- and beta 2-adrenoceptor agonists have different effects on rat parotid acinar cells. Am. J. Physiol. 242:G481–G482.

    PubMed  CAS  Google Scholar 

  • Hirtz, C., Chevalier, F., Centeno, D., ofidal, V., Egea, J. C., ossignol, M., Sommerer, N., and Periere, D. D. 2005a. MS characterization of multiple forms of alpha-amylase in human saliva. Proteomics 5:4597–4607.

    Article  PubMed  CAS  Google Scholar 

  • Hirtz, C., Chevalier, F., Centeno, D., Egea, J. C., ossignol, M., Sommerer, N., and Périère, D. D. 2005b. Complexity of the human whole saliva proteome. J. Physiol. Biochem. 61:469–80.

    Article  PubMed  CAS  Google Scholar 

  • Hoffmann, F., and Maser, E. 2007. Carbonyl reductases and pluripotent hydroxysteroid dehydrogenases of the short-chain dehydrogenase/reductase superfamily. Drug Metab. Rev. 39:87–144.

    Article  PubMed  CAS  Google Scholar 

  • Huang, C. M. 2004. Comparative proteomic analysis of human whole saliva. Arch. Oral Biol. 49:951–962.

    Article  PubMed  CAS  Google Scholar 

  • Humphrey, S. P., and Williamson, R. T. 2001. A review of saliva normal composition, flow and function. J. Prosthet. Dent. 85:162–169.

    Article  PubMed  CAS  Google Scholar 

  • Iwata, N., Inazu, N., and Satoh, T. 1990. Immunological and enzymological localization of carbonyl reductase in ovary and liver of various species. J. Biochem. (Tokyo) 107:209–212.

    CAS  Google Scholar 

  • Jansman, A. J., Frohlich, A. A., and Marquardt, R. R. 1994. Production of proline-rich proteins by the parotid glands of rats is enhanced by feeding diets containing tannins from faba beans (Vicia faba L.). J. Nutr. 124:249–258.

    PubMed  CAS  Google Scholar 

  • Kandra, L., Gyémánt, G., Zajacz, A., and Batta, G. 2004. Inhibitory effects of tannin on human salivary alpha amylase. Biochem. Biophy. Res. Comm. 319:1265–1271.

    Article  CAS  Google Scholar 

  • Karn, R. C., and Laukaitis, C. M. 2003. Characterization of two forms of mouse salivary androgen-binding protein (ABP): Implications for evolutionary relationships and ligand-binding function. Biochemistry 42:7162–7170.

    Article  PubMed  CAS  Google Scholar 

  • Katsukawa, H., and Ninomiya, Y. 1999. Capsaicin induces S-like substances in submandibular saliva of the rat. J. Dent. Res. 78:1609–1616.

    PubMed  CAS  Google Scholar 

  • Kim, W. S., Nakayama, K., Nakagawa, T., Kawamura, Y., Haraguchi, K., and Murakami, K. 1991. Mouse submandibular gland prorenin-converting enzyme is a member of glandular kallikrein family. J. Biol. Chem. 266:19283–19287.

    PubMed  CAS  Google Scholar 

  • Le Magnen, J. 1986. Hunger. Problems in the Behavioural Sciences. Cambridge University Press, Cambridge.

    Google Scholar 

  • Lesschaeve, I., and Noble, A. C. 2005. Polyphenols: factors influencing their sensory properties and their effects on food and beverage preferences. Am. J. Clin. Nutr. 81:330S–335S.

    PubMed  CAS  Google Scholar 

  • Lin, H. H., and Ann, D. K. 1991. Molecular characterization of rat multigene family encoding proline-rich proteins. Genomics 10:102–113.

    Article  PubMed  CAS  Google Scholar 

  • Lopez-solis, R. O., and Kemmerling, U. 2005. Codominant expression of genes coding for different sets of inducible salivary polypeptides associated with parotid hypertrophy in two inbred mouse strains. J. Cell Biochem. 95:99–107.

    Article  PubMed  CAS  Google Scholar 

  • Lu, Y., and Bennick, A. 1998. Interaction of tannin with human salivary proline-rich proteins. Arch. Oral Biol. 43:717–728.

    Article  PubMed  CAS  Google Scholar 

  • Madsen, H. O., and Hjorth, J. P. 1985. Molecular cloning of mouse PSP mRNA. Nuc. Acids Res. 13:1–13.

    Article  CAS  Google Scholar 

  • Mahmood, S., and Smithard, R. 1993. A comparison of effects of body weight and feed intake on digestion in broiler cockrels with effects of tannins. Br. J. Nutr. 70:701–709.

    Article  PubMed  CAS  Google Scholar 

  • Mcdougall, G. J., Shpiro, F., Dobson, P., Smith, P., Blake, A., and Stewart, D. 2005. Different polyphenolic components of soft fruits inhibit alpha-amylase and alpha-glucosidase. J. Agric. Food Chem. 53:2760–2766.

    Article  PubMed  CAS  Google Scholar 

  • Mehansho, H., Hagerman, A. E., Clements, S., Butler, L. G., ogler, J., and Carlson, D. M. 1983. Modulation of proline-rich protein biosynthesis in rat parotid glands by sorghum with high tannin levels. Proc. Natl. Acad. Sci. USA. 80:3948–3952.

    Article  PubMed  CAS  Google Scholar 

  • Mehansho, H., Hagerman, A. E., Cements, S., Butler, L., ogler, J., and Carlson, D. M. 1985. Indution of proline rich glycoproteins synthesis in mouse salivary glands by isopretrenol and by tannins. J. Biol. Chem. 260:4418–4423.

    PubMed  CAS  Google Scholar 

  • Mehansho, H., ogler, J., and Carlson, D. M. 1987. Dietary tannins and salivary proline rich peroteins: interation, inductions and defense mechanisms. Annu. Rev. Nutr. 7:423–440.

    Article  PubMed  CAS  Google Scholar 

  • Muenzer, J., Bildstein, C., Gleason, M., and Carlson, D. M. 1979. Purification of proline-rich proteins from parotid glands of isoproterenol-treated rats. J Biol. Chem. 254:5623–5628.

    PubMed  CAS  Google Scholar 

  • Myal, Y., Iwasiow, B., Cosby, H., Yarmill, A., Blanchard, A., Tsuyuki, D., Fresnoza, A., Duckworth, M. L., and Shiu, R. P. C. 1998. Analysis of tissue- and hormone-specific regulation of the human prolactin-induceble protein/gross cystic disease fluid proein-15 gene in transgenic mice. J. Mol. Endocrinol. 21:217–223.

    Article  PubMed  CAS  Google Scholar 

  • Nakayama, T., Yashiro, K., Inoue, Y., Matsuura, K., Ichikawa, H., Hara, A., and Sawada, H. 1986. Characterization of pulmonary carbonyl reductase of mouse and guinea pig. Biochim. Biophys. Acta 882:220–227.

    PubMed  CAS  Google Scholar 

  • Neuhoff, V., Arold, N., Taube, D., and Ehrhardt, W. 1988. Improved staining of proteins in polyacrilamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brillant Blue G-250 and R-250. Electrophoresis 9:255–262.

    Article  PubMed  CAS  Google Scholar 

  • Neyraud, E., Sayd, T., Morzel, M., and Dransfield, E. 2006. Proteomic analysis of human whole and parotid salivas following stimulation by different tastes. J. Proteome Res. 5:2474–2480.

    Article  PubMed  CAS  Google Scholar 

  • Oppenheim, F. G., Salih, E., Siqueira, W. L., Zhang, W., and Helmerhorst, E. J. 2007. Salivary proteome and its genetic polymorphisms. Ann N Y Acad. Sci. 1098:22–50.

    Article  PubMed  CAS  Google Scholar 

  • Pandey, A., Andersen, J. S., and Mann, M. 2000. Use of mass spectrometry to study signaling pathways. Sci STKE 37:PL1.

    Google Scholar 

  • Perkins, D. N., Pappin, D. J., Creasy, D. M., and Cottrell, J. S. 1999. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20:3551–3567.

    Article  PubMed  CAS  Google Scholar 

  • Prinz, J. F., and Lucas, P. W. 2000. Saliva tannin interactions. J. Oral Rehabil. 27:991–994.

    Article  PubMed  CAS  Google Scholar 

  • Proctor, G. B., and Carpenter, G. H. 2007. Regulation of salivary gland function by autonomic nerves. Auton. Neurosci. 133:3–18.

    Article  PubMed  CAS  Google Scholar 

  • Roxo-Rosa, M., Da Costa, G., Luider, T. M., Scholte, B. J., Coelho, A. V., Amaral, D. M., and Penque, D. 2006. Proteomic analysis of nasal cells from cystic fibrosis (CF) patients and non-CF control individuals: search for novel biomarkers of CF lung disease. Proteomics 6:2314–25.

    Article  PubMed  CAS  Google Scholar 

  • Shaw, P. A., and Yu, W. A. 2000. Autonomic regulation of cystatin S gene expression in rat submandibular glands. Auton. Neurosci. 83:49–57.

    Article  PubMed  CAS  Google Scholar 

  • Shimada, T., Saitoh, T., and Matsui, T. 2004. Does acclimation reduce the negative effects of acorn tannins in the wood mouse Apodemus speciosus?. Acta Theriol. 49:203–214.

    Google Scholar 

  • Shimada, T., Saitoh, T., Sasaki, E., Nishitani, Y., and Osawa, R. 2006. Role of tannin-binding salivary proteins and tannase-producing bacteria in the acclimation of the Japanese wood mouse to acorn tannins. J. Chem Ecol. 32:1165–1180.

    Article  PubMed  CAS  Google Scholar 

  • Shori, D. K., and Asking, B. 2001. Dynamics of protein and fluid secretion from the major salivary glands of rat: relevance of research findings to clinically observed defective secretion in cystic fibrosis. Pflugers Arch. 443:Suppl 1535–543.

    Google Scholar 

  • Skopec, M. M., Hagerman, A. E., and Karasov, W. H. 2004. Do salivary proline-rich proteins counteract dietary hyrdolyzable tannin in laboratory rats. J. Chem. Ecol. 30:1679–1692.

    Article  PubMed  CAS  Google Scholar 

  • Sladeck, N. 2003. Human aldehyde dehydrogenase: Potential pathological, pharmacological and toxicological impact. J. Biochem. Mol. Toxicol. 17:7–23.

    Article  CAS  Google Scholar 

  • STJEIN, V., AMEROGEN, A.V., Veerman, E.C.I., Kasanmoentalib, S., and OVerduk, B., 1999. Chitinase in whole human saliva and in whole saliva of patients with periodontal inflammation. Eur. J. Oral Sci. 107:328–337.

    Article  Google Scholar 

  • Vitorino, R., Lobo, M. J., Ferrer-correira, A. J., Dubin, J. R., Tomer, K. B., Domingues, P. M., and Amado, F. M. 2004. Identification of human whole saliva protein components using proteomics. Proteomics 4:951–962.

    Article  CAS  Google Scholar 

  • Waters, C. A., Morand, J. N., Schatzman, R. C., and Carlson, D. M. 1998. Induction of p34cdc2 in mouse parotid glands upon activation of beta 1-adrenergic receptors. Cell Mol. Biol. (Noisy-le-grand) 44:333–342.

    CAS  Google Scholar 

  • Williams, K. M., Ekstrom, J., and Marshal, T. 1999. High resolution electrophoretic analysis of rat parotid salivary proteins. Electrophoresis 20:1373–1381.

    Article  PubMed  CAS  Google Scholar 

  • Yao, Y., Berg, E., Costello, C. E., Troxler, R. F., and Oppenheim, F. G. 2003. Identification of proteins components in human acquired enamel pellicle and whole saliva using novel proteomics approaches. J. Biol. Chem. 278:5300–5308.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We acknowledge the generous offer of Tupafin Ato from the Silva Chimica Company (Italy) to Dr André M. Almeida to review this manuscript and Prof. Alfredo Pereira for support with the statistical analysis. This work was supported by POCTI FCT-CVT/33039/99-00 scientific project. Gonçalo da Costa and Elsa Lamy acknowledge a PhD grant from 3° Quadro Comunitário de Apoio of FCT—Fundação para a Ciência e a Tecnologia of the Ministério da Ciência Tecnologia e Ensino Superior.

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Authors and Affiliations

  1. ITQB-Instituto de Tecnologia Química e Biológica, Oeiras, Portugal

    G. da Costa & A. V. Coelho

  2. ICAM-Instituto de Ciências Agrárias Mediterrânicas, Universidade de Évora, Évora, Portugal

    E. Lamy & E. Sales Baptista

  3. Departamento de Zootecnia, Universidade de Évora, Évora, Portugal

    E. Lamy & E. Sales Baptista

  4. Departamento de Biologia, Universidade de Évora, Évora, Portugal

    F. Capela e Silva

  5. Centro de Investigação em Ciências e Tecnologias da Saúde, Universidade de Évora, Évora, Portugal

    F. Capela e Silva

  6. Department of Biochemistry and Molecular Biology, University of Southern Denmark, Odense, Denmark

    J. Andersen

  7. Departamernto de Química Universidade de Évora, Évora, Portugal

    A. V. Coelho

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  1. G. da Costa
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  2. E. Lamy
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  3. F. Capela e Silva
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  6. A. V. Coelho
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Correspondence to A. V. Coelho.

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G. da Costa and E. Lamy have contributed equally to this work.

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da Costa, G., Lamy, E., Capela e Silva, F. et al. Salivary Amylase Induction by Tannin-Enriched Diets as a Possible Countermeasure Against Tannins. J Chem Ecol 34, 376–387 (2008). https://doi.org/10.1007/s10886-007-9413-z

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