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Molecular & Cellular Proteomics 7:911-926, 2008.
© 2008 by The American Society for Biochemistry and Molecular Biology, Inc.

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Research

Trafficking and Postsecretory Events Responsible for the Formation of Secreted Human Salivary Peptides

A Proteomics Approach^*

Irene Messana^,, Tiziana Cabras^,, Elisabetta Pisano, Maria Teresa Sanna, Alessandra Olianas, Barbara Manconi, Mariagiuseppina Pellegrini, Gaetano Paludetti^¶, Emanuele Scarano^¶, Antonella Fiorita^¶, Stefania Agostino^¶, Alessia M. Contucci^¶, Lea Calò^¶, Pasqualina M. Picciotti^¶, Armando Manni^||, Anders Bennick^**, Alberto Vitali, Chiara Fanali^,, Rosanna Inzitari^, and Massimo Castagnola^,,¶¶,||||

From the Dipartimento di Scienze Applicate ai Biosistemi, Università di Cagliari, I-09042 Cagliari, Italy, Istituto di ^¶ Clinica Otorinolaringoiatrica and ^|| Clinica Odontoiatrica, Università Cattolica, I-00168 Roma, Italy, ^** Department of Biochemistry, University of Toronto, Toronto M5S 1A8, Canada, and Istituto di Biochimica e di Biochimica Clinica, Università Cattolica and Istituto per la Chimica del Riconoscimento Molecolare, Consiglio Nazionale delle Ricerche (CNR),^¶¶ Istituto Scientifico Internazionale (ISI) Paolo VI, I-00168 Roma, Italy

To elucidate the localization of post-translational modifications of different classes of human salivary proteins and peptides (acidic and basic proline-rich proteins (PRPs), Histatins, Statherin, P-B peptide, and "S type" Cystatins) a comparative reversed phase HPLC-ESI-MS analysis on intact proteins of enriched granule preparations from parotid and submandibular glands as well as parotid, submandibular/sublingual (Sm/Sl), and whole saliva was performed. The main results of this study indicate the following. (i) Phosphorylation of all salivary peptides, sulfation of Histatin 1, proteolytic cleavages of acidic and precursor basic PRPs occur before granule storage. (ii) In agreement with previous studies, basic PRPs are secreted by the parotid gland only, whereas all isoforms of acidic PRPs (aPRPs) are secreted by both parotid and Sm/Sl glands. (iii) Phosphorylation levels of aPRPs, Histatin 1, and Statherin are higher in the parotid gland, whereas the extent of cleavage of aPRP is higher in Sm/Sl glands. (iv) O-Sulfation of tyrosines of Histatin 1 is a post-translational modification specific for the submandibular gland. (v) The concentration of Histatin 3, Histatin 5, and Histatin 6, but not Histatin 1, is higher in parotid saliva. (vi) Histatin 3 is submitted to the first proteolytic cleavage (generating Histatins 6 and 5) during granule maturation, and it occurs to the same relative extent in both glands. (vii) The proteolytic cleavages of Histatin 5 and 6, generating a cascade of Histatin 3 fragments, take place after granule secretion and are more extensive in parotid secretion. (viii) Basic PRPs are cleaved in the oral cavity by unknown peptidases, generating various small proline-rich peptides. (ix) C-terminal removal from Statherin is more extensive in parotid saliva. (x) P-B peptide is secreted by both glands, and its relative quantity is higher in submandibular/sublingual secretion. (xi) In agreement with previous studies, S type Cystatins are mainly the product of Sm/Sl glands.

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