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IN MEMORIAM |
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The primary focus of his research throughout his career was directed at biological and clinical aspects of several macromolecules present in oral tissues and fluids, termed "anionic glycoconjugates". The work was fundamental to the progress of 25 post-graduate PhD students, mainly funded on MRC training awards, as well as numerous post-doctoral fellows. His work provided the basis for an in-depth understanding of the biology of these molecules in the oral environment and as biomarkers of periodontal disease, the interface between connective tissues and biomaterials, and the formation of oral biofilms. His work was recognized by the award of the Colgate prize of the IADR British Division, a Distinguished Scientist Award in Oral Biology of the IADR in 1997, and a DSc award (Doctorate of Science) by the University of Wales in 1993.
His huge contribution covered 35 years. He was the first to show a distinction between mucins present in oral salivary secretions and proteoglycans present in oral connective tissues, the first to characterize the glycosaminoglycan, chondroitin sulphate, in dentin (Embery, 1974), and among the first to recognize its conjugation to a protein in forming a proteoglycan (termed "acid mucopolysaccharide" at that time). This early work also indicated, for the first time, the dynamic equilibrium of the dentinal matrix and the absence of these molecules from enamel.
His early studies laid the foundation for the investigation of the hitherto poorly defined chemistry of these tissue proteins. This led to the first paper defining the presence of proteoglycans in dentin and the influence of high-fluoride regimes in reducing the hydrodynamic size of these macromolecules in vitro (Smalley and Embery, 1980). This work had implications for skeletal fluorosis in general and offered a biological explanation for the skeletal changes evident in many regions of the world, such as India and Africa, where fluorosis was endemic. The influence of fluoride on proteoglycan structure was pursued with a series of papers in the 1990s, with co-worker Rachel Waddington, demonstrating that fluoride influences the post-translational synthesis of the glycosaminoglycan chain within the proteoglycan molecules. Later work also demonstrated that fluoride exerts similar post-translational changes to phosphoproteins present in dentin and the enzymes involved in this process (e.g., Milan et al., 1999; Waddington et al., 2003). Together with the embracement of recombinant technology in generating chimeric forms of proteoglycans (Sugars et al., 2003), these studies reinforced Graham’s visionary ideas and hypotheses that these macromolecules play a variety of roles in matrix formation and mineralization during dentinogenesis (Embery et al., 2001).
His work also identified glycosaminoglycans and proteoglycans in a range of other dental tissues such as alveolar bone and gingiva. Glycosaminoglycans in human gingival crevicular fluid were studied as indicators of active periodontal disease (Last et al., 1985). This work indicated that bone proteoglycans were liberated into gingival sulcus fluid in a variety of clinical conditions and could be used to indicate active disease. The advent of specific monoclonal antibodies toward proteoglycans allowed for further characterization of these molecules (e.g., Waddington et al.., 1998) and led to a greater understanding of the key events in alveolar bone resorption. The mechanisms were studied in a series of papers (e.g., Moseley et al., 1998) that examined the involvement of polymorphonuclear leukocytes as an inflammatory factor and revealed a non-enzyme cell system in the destruction of the matrix components of the periodontium and the role of oxygen free radicals in the pathogenesis of periodontal disease.
His analyses of proteoglycans were not restricted to contemporary tissues, but included investigations on the chemical compositions of teeth from Lindow man (who had been preserved for 2000 years in a bog found near Wilmslow Cheshire, UK) and the detection of non-collagenous proteins from the compact bone of the dinosaur Iguanodon. The latter revealed the presence of anionic molecules and glycosaminoglycans in dinosaurs and represented the first clear indication of non-collagenous material entrapped within fossilized bone.
Parallel to these studies, Graham also fostered a research interest on the anionic glycoconjugates in saliva and the formation of oral biofilms. His paper on the sulphated glycoproteins in rat whole saliva (Embery and Whitehead, 1975) was instrumental in characterizing sulphated glycoproteins as being distinct from the sulphated acid-mucopolysaccharides present in the oral connective tissues of dentin, alveolar bone, and gingiva. This paper was widely quoted and contributed to many years spent developing and refining separative and analytical methodology for understanding these molecules. Of note were the adherent properties of salivary glycoproteins, identifying specific domains involved in their attachment to hydroxyapatite and to Streptococcus sanguis and S. salivarius (Wassall et al., 1995), thereby furthering our understanding of the mechanisms involved in the formation of acquired dental pellicle and its initial colonization. His interest extended to the role of agents in dentifrices in controlling plaque formation, and he was co-editor and contributor of the collected publications "Tooth Surface Interactions and Preventative Dentistry".
Graham Embery’s contribution to dental research is undeniable. He led by example and stimulated a team approach. He cared deeply about his co-research workers and has left behind dedicated and enthusiastic researchers who will continue his work in this field at Cardiff and Liverpool. Moreover, he was a very well-respected member of the oral and dental research community. He served on many national and international committees, including those of the Medical Research Council. Prior to his election as IADR President, he had been President of the British Society of Dental Research and had served on the management committee for more than 15 years. Important in understanding his approach to his work and his success was his love of sport (rugby and golf), his love of music (he was an accomplished piano, violin, and banjo player), and his love of the fellowship of the International Dental Research community. Most of all, he was hugely supported by his wife Vivienne and his children in his life’s work, including the IADR, and was immensely proud of them.
— Stephen Challacombe and Rachel Waddington
September, 2003
FOOTNOTES
The references in this tribute can be found at http://www.dentalresearch.org.
REFERENCES
Embery G (1974). The isolation of chondroitin 4-35S-sulphate from the molar teeth of young rats receiving sodium 35S-sulphate. Calcif Tissue Res 14:59–65.[ISI][Medline]
Embery G, Whitehead E (1975). Sulphated glycoproteins in rat saliva. Arch Oral Biol 20:843–847.[ISI][Medline]
Embery G, Hall R, Waddington R, Septier D, Goldberg M (2001). Proteoglycans in dentinogenesis. Crit Rev Oral Biol Med 12:331–349.[Abstract]
Last KS, Stanbury JB, Embery G (1985). Glycosaminoglycans in human gingival crevicular fluid as indicators of active periodontal disease. Arch Oral Biol 30:275–281.[ISI][Medline]
Milan AM, Waddington RJ, Embery G (1999). Altered phosphorylation of rat dentine phosphoproteins by fluoride in vivo. (1999) Calcif Tissue Int 64:234–238.[ISI][Medline]
Moseley R, Waddington RJ, Embery G, Rees SG (1998). The modification of alveolar bone proteoglycans by reactive oxygen species in vitro. Connect Tissue Res 37:13–28.[ISI][Medline]
Smalley JW, Embery G (1980). The influence of fluoride administration on the structure of proteoglycans in the developing rat incisor. Biochem J 190:263–272.[ISI][Medline]
Sugars RV, Milan AM, Brown JO, Waddington RJ, Embery G (2003). Molecular interaction of recombinant decorin and biglycan with type I collagen influences crystal growth. Connect Tissue Res 44:189–195.
Waddington RJ, Embery G, Hall RC (1993). The influence of fluoride on proteoglycan structure using a rat odontoblast in vitro system. Calcif Tissue Int 52:392–398.[ISI][Medline]
Waddington RJ, Embery G, Smith AJ (1998). Immunochemical detection of the proteoglycans decorin and biglycan in human gingival crevicular fluid from sites of advanced periodontitis. Arch Oral Biol 43:287–295.[ISI][Medline]
Waddington RJ, Hall RC, Embery G, Lloyd DM (2003). Changing profiles of proteoglycans in the transition of predentine to dentine. Matrix Biol 22:153–161.[ISI][Medline]
Wassall MA, Embery G, Bagg J (1995). The role of hydrophobicity in Streptococcus sanguis and Streptococcus salivarius adhesion to salivary fraction coated hydroxyapatite. Colloids Surf B 5:143–152.
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