HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Figures Only Full Text (PDF) Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Scannapieco, F. A. Search for Related Content PubMed PubMed Citation Articles by Scannapieco, F. A.

Salivary Biochemistry in Buffalo: The Legacy of Michael J. Levine

Department of Oral Biology, 109 Foster Hall, School of Dental Medicine, University at Buffalo, The State University of New York, Buffalo, NY 14214; fas1{at}acsu.buffalo.edu

KEY WORDS: dental plaque • mucins • pellicle • saliva • xerostomia

	INTRODUCTION

TOP INTRODUCTION FOUNDATIONS "TRUCKIN’ BACK TO... SALIVA, PELLICLES, AND DENTAL... AN ENVIRONMENT FOR LEARNING LEVINE’S LEGACY EPILOGUE REFERENCES

 
Occasionally in science, circumstances converge that allow for the gathering of a group of people who together accomplish extraordinary feats. Such were the circumstances between 1975 and 1995 at the University at Buffalo School of Dental Medicine under the guidance of Michael J. Levine (MJL), whose research group helped usher our knowledge of salivary biochemistry from the "pre-technology" era that existed before 1970 into the present post-genomic era.

This article will review MJL’s career in Buffalo and will recount his mentorship of an outstanding cadre of productive and creative scientists, many of whom remain actively involved in oral health research and dental education throughout the United States and the world.

	FOUNDATIONS

TOP INTRODUCTION FOUNDATIONS "TRUCKIN’ BACK TO... SALIVA, PELLICLES, AND DENTAL... AN ENVIRONMENT FOR LEARNING LEVINE’S LEGACY EPILOGUE REFERENCES

 
Following completion of his baccalaureate studies at Cornell University in the early 1960s, and after an abbreviated stint in the US Marine Corps (for which he received an honorable discharge), MJL found his way into the laboratory of Dr. Solon (Art) Ellison as a dishwasher (that is certainly "starting at the bottom"!). This evolved into a position as a laboratory technician. Of interest to Dr. Ellison (then the chair of the recently established Department of Oral Biology) was salivary protein research. Before his tenure at Buffalo, Ellison had worked on the faculty of Columbia University with Dr. Irwin Mandel. Together, they published several classic studies that were among the first to identify immunoglobulins in saliva and several unique salivary proteins and glycoproteins. One of their goals was to correlate the concentration of various constituents of saliva with dental caries experience. MJL began by working to isolate the glycoproteins of parotid saliva, together with J.C. Weill (Levine et al., 1969). It was upon the foundation begun by Art Ellison that MJL grew and prospered.

Before long, MJL decided to enter a formal program of study. Dr. Ellison recounts the story: "One day he (MJL) asked whether he could be a graduate student, since the lab work he was doing could well be the basis for a dissertation. So he began a program. He then decided that as long as he was going to school, he may as well take a DDS also" (Ellison, 1992). Thus, MJL entered the newly founded graduate program in Oral Biology at Buffalo (Emmings, 1999), and then the DDS program. He was one of the first combined dual-degree graduates in the United States, completing first the DDS in 1971 and then the PhD in 1972 (see Fig. 1). His PhD thesis focused on both the immunochemistry and the chemical characterization of glycoprotein components of human parotid saliva, particularly what he later named the "proline-rich glycoproteins".

View larger version (118K): [in this window] [in a new window]   Figure 1. (upper left) MJL graduation portrait from the University at Buffalo Dental School, 1971. (upper right) MJL discussing an "issue" with Bob Cohen, 1987. (lower left) MJL in the lab, ca. 1988. (lower right) Writing a manuscript with N. Ramasubbu, 1990. (Guess what is behind the black box!)

Enthused by the study of glycoproteins, MJL entered the Periodontal Pathobiology Training Program at Harvard University School of Dental Medicine, following his graduation from Buffalo. He combined this with a post-doctoral fellowship in the laboratory of Dr. Robert Spiro, a distinguished glycoprotein biochemist at the Joslin Diabetes Center. Few dentists in those days had the foresight to pursue post-doctoral training in a medical school setting. This was a pivotal experience for MJL. He learned from Dr. Spiro how to organize and run a productive biochemistry laboratory. He was fond of telling stories of the unique strategies Dr. Spiro used to motivate his post-doctoral fellows. One anecdote involved a fellow who was directed to isolate a specific glycoprotein from bovine kidney basement membranes. The kidneys were obtained from a slaughterhouse outside Boston early in the morning and brought to the laboratory on ice, where they then underwent a lengthy process involving multiple steps of column chromatography to isolate the component of interest from the fresh kidney glomeruli. Complex enzyme assays were performed on each column fraction to identify cell organelles (e.g., plasma membrane, golgi, etc. ). This work took many hours and careful attention. After working through the night, the unfortunate fellow found that one of the columns had become contaminated with bacterial growth. Needless to say, the experiment had to be aborted. On learning this, Dr. Spiro simply said, "Well, if you hustle, you should be able to get to the slaughterhouse in the next couple of hours to pick up some more kidneys to start over again." This expectation, that science "is your mistress", left a lasting impression on MJL and set the tone for how he would run his own laboratory in the future.

	"TRUCKIN’ BACK TO BUFFALO..."

TOP INTRODUCTION FOUNDATIONS "TRUCKIN’ BACK TO... SALIVA, PELLICLES, AND DENTAL... AN ENVIRONMENT FOR LEARNING LEVINE’S LEGACY EPILOGUE REFERENCES

 
Following the completion of his training program in Boston, MJL returned to Buffalo in 1975 as an Assistant Professor in the Departments of Oral Biology and Periodontology. He was fortunate to, first, share, and then to inherit, Art Ellison’s well-equipped salivary biochemistry laboratory, a great foundation upon which to build his research effort. While it was well-known by this time that saliva contained several previously described proteins—such as amylase, immunoglobulins, lactoferrin, and lysozyme—it was also clear that there were quite a few components that remained uncharacterized (Ellison, 1966). Thus, he set as his goal to identify and characterize as many of the remaining unknown salivary protein and glycoprotein components as possible. This was a daunting challenge, since, by today’s standards, the available methodologies were quite primitive and labor-intensive, and the number of unique components in saliva appeared to be ever-increasing as more sensitive protein-detection methods were developed. Several of these unknown salivary components were particularly enigmatic. One such component was the basic proline-rich glycoprotein (PRG) of parotid saliva (Levine et al., 1969; Li and Levine, 1980). Other major components that were, until then, quite recalcitrant to study were the high-molecular-weight glycoproteins. These components tend to complex with other salivary proteins that, until then, prevented their isolation to homogeneity. Using the knowledge gained from Spiro, and the efforts of many graduate students and post-doctoral fellows, beginning with Mark Herzberg and a bit later Larry Tabak and Akapron Prakobphol, MJL began the formidable task of isolating and chemically characterizing these components. He also benefited from Art Ellison’s willingness to share his well-equipped laboratory.

Initial studies found at least two high-molecular-weight components in the mucous secretions, both of which were highly glycosylated and resembled mucins: a higher-molecular-weight mucin, named mucin glycoprotein or MG1 (Levine et al., 1978); and a low-molecular-weight mucin or MG2 (Prakobphol et al., 1982). Around this time, Dr. Molakala S. Reddy joined the group and added considerable expertise to the characterization of the carbohydrate moieties of these glycoproteins, utilizing gas chromatography-mass spectroscopy (Reddy et al., 1985). In approximately three weeks, Dr. Reddy disproved the structure proposed by Larry Tabak in his PhD thesis for the major oligosaccharides derived from monkey extraparotid salivary mucins. Fortunately, appropriate corrections were made prior to the submission of the work for publication! Together, they made substantial progress in characterizing this group of molecules (summarized in Tabak et al., 1982; this paper was named a "Citation Classic" by CSI—one of the few oral biology papers to be accorded that distinction). Libuse Bobek eventually accomplished the difficult task of cloning and sequencing of the gene for MG2, now known as MUC7 (Bobek et al., 1993).

During the course of this work, a variety of smaller-molecular-weight phosphoprotein components was identified as contaminants of, and subsequently purified from, the mucins. Among these were the "cysteine-containing phosphoproteins", later recognized as cystatins. These were purified and characterized by John Shomers, who worked as a technician for MJL as he also pursued his MS degree on a part-time basis (Shomers et al., 1982). The gene for cystatin SN was later cloned and sequenced by Ibtisam Al-Hashimi for her PhD thesis work, while the gene for cystatin S was cloned and sequenced by Libuse Bobek (Al-Hashimi et al., 1988; Bobek and Levine, 1992). These proteins have been shown to have cysteine-protease inhibitory activity as well as the ability to influence biomineralization of teeth.

An overriding rationale for the work was, some day, to produce an effective, biologically based artificial saliva for the treatment of xerostomia. The strategy was to simulate the functional characteristics of salivary components by devising synthetic molecules consisting of multiple biologically active or "functional domains". It was imagined that such composite molecules could be "custom-designed" mimics generated from knowledge of the primary sequence and computer-assisted structural predictions of conformation. Promising candidates would then be subjected to in vitro and finally in vivo testing.

It was recognized that an important function of saliva was its lubricity, or ability to lubricate the oral tissues. MJL’s group was one of the first to test purified salivary molecules as lubricants. Michael Hatton, while a dental student, and Alfredo Aguirre, then an MS student, constructed an interesting homemade device based on a previously described device used to evaluate lubricating properties of synovial fluid (Swann et al., 1981). It resembled a record player that used a spinning circular glass plate upon which the substance to be tested was placed. An arm having a sensor was then rested on the spinning plate, and the resistance, assumed to be inversely proportional to the inherent lubricity of the material being tested, was measured (Hatton et al., 1985; Aguirre et al., 1989). It was found that purified glycoproteins such as PRG are lubricative, and that the carbohydrate moieties play a role in this function. It was therefore surprising that later studies found that statherin, a small peptide devoid of carbohydrate thought to contribute to tooth surface mineralization, possesses lubrication properties (Douglas et al., 1991). It appeared that statherin’s amphipathic nature enables it to function as a boundary lubricant on enamel. These findings contradicted the long-held assumption that lubrication of saliva was dependent only on glycosylated salivary components.

	SALIVA, PELLICLES, AND DENTAL PLAQUE

TOP INTRODUCTION FOUNDATIONS "TRUCKIN’ BACK TO... SALIVA, PELLICLES, AND DENTAL... AN ENVIRONMENT FOR LEARNING LEVINE’S LEGACY EPILOGUE REFERENCES

 
Another important function of salivary components is their ability to interact with bacteria. By the mid-1970s, it was recognized that salivary molecules were intimately involved in normal dental plaque formation. Herzberg, Murray Stinson (a member of the microbiology faculty at Buffalo), Tabak, Patricia Murray (as part of her PhD thesis), and Jim Bergey (who later joined MJL as a post-doctoral following training in Stinson’s lab) showed that salivary glycoproteins interacted specifically with oral streptococci. A series of elegant biochemical studies demonstrated that the bacteria possessed surface proteins or lectins which specifically bound to salivary glycoprotein carbohydrate moieties such as sialic acid (Levine et al., 1978; Murray et al., 1982, 1986; Bergey et al., 1986). Again, these were among the first demonstrations of lectin-like proteins on oral bacteria. Other studies focused on specific interactions between oral bacteria and amylase (Scannapieco et al., 1989, 1993; Tseng et al., 1999) and histatins (Raj et al., 1990). For his PhD thesis, Aaron Biesbrock extended such studies to medical pathogens such as Staphylococcus aureus and Pseudomonas aeruginosa and found a salivary mucin-secretory immunoglobulin A (S-IgA) complex to interact with the bacteria (Biesbrock et al., 1991).

Another area of interest was the detailed study of salivary pellicles. Ibtisam AI-Hashimi, in her PhD thesis (Al-Hashimi and Levine, 1989), combined (SDS)-PAGE/Western transfer analyses with specific radiolabeling/SDS-PAGE fluorography to identify salivary proteins in early enamel pellicle. Major components identified in pellicles included amylase, cystatins, salivary mucin, and S-IgA. These studies illustrated the selective nature of salivary protein adsorption to the enamel surface. Similar approaches were later used for PhD studies by Steve Bradway to study mucosal pellicle (Bradway et al., 1992) and Mira Edgerton for denture-pellicle (Edgerton and Levine, 1992). Indeed, the interesting studies of Bradway demonstrated that the enzyme transglutaminase, originating from oral epithelium, could catalyze the covalent attachment of salivary proteins such as the proline-rich proteins within oral pellicles and microbial surfaces (Bradway et al., 1989, 1992; Staab et al., 1999).

	AN ENVIRONMENT FOR LEARNING

TOP INTRODUCTION FOUNDATIONS "TRUCKIN’ BACK TO... SALIVA, PELLICLES, AND DENTAL... AN ENVIRONMENT FOR LEARNING LEVINE’S LEGACY EPILOGUE REFERENCES

 
From its inception in the mid-1970s with six or seven people, MJL’s research group grew exponentially through the 1980s. By the time I arrived as a PhD student in 1985, more than 25 students and post-doctoral fellows were working in the laboratory. It was an exciting time indeed. Spurred on by friendly competition from other salivary biochemistry laboratories, led by Frank Oppenheim at Boston University, Don Hay at Forsyth Dental Center in Boston, and Anders Bennick at the University of Toronto, the laboratory was a beehive of activity. One had the opportunity to learn not only from MJL, but also from many enthusiastic colleagues who, as a group, collectively displayed expertise from classic biochemistry and immunology to molecular and structural biology. The laboratory was also very well-equipped to use "the latest" scientific methods. Through successful grant-writing and the support of Dean William Feagans and Dr. Robert Genco, Chair of Oral Biology, MJL was able to muster considerable resources to equip the laboratory well. One could theoretically select a molecule to be studied, isolate it, determine its amino acid composition and sequence, clone and sequence its gene, express the recombinant protein, study its function, and determine its structural characteristics using a variety of sophisticated spectroscopic methods, all in the same room! While this may seem rather routine today, it was a remarkable range of activities for a single laboratory in the 1980s, especially one in a dental school. MJL believed that it was essential that, if possible, all of the work be done within the confines of the laboratory. This unique facility enabled MJL and colleagues to pursue sophisticated structural biological studies, among the first to be performed for salivary proteins. Researchers such as Ron Loomis, Krishna Bhandary, Antony Raj, and Narayanan Ramasubbu brought structural biology expertise to the laboratory that allowed for the NMR and crystallographic analysis of mucins, amylase, histatins, and cystatins (Loomis et al., 1987; Raj et al., 1990; Bobek et al., 1994; Ramasubbu et al., 1996). For his PhD thesis, Bob Cohen outfitted the laboratory to develop monoclonal antibodies against mucins—again, state-of-the-art technology for the time. He was able to localize the distinct species of mucin to different regions of salivary glands (Cohen et al., 1990, 1991). MJL also embraced the digital age: Every person in the laboratory had access to or owned a personal computer. Soon the laboratory was networked and was one of the first in the University to have Internet access. All of these technological advances allowed the research group to acquire and utilize cutting-edge techniques to advance the science at hand.

While salivary biochemistry was the major focus of MJL’s laboratory, other students in the department were encouraged to utilize its resources, both intellectual and material. So, for example, Tom van Dyke, and later Ernie DeNardin and Drew Dentino, pursued biochemical studies of neutrophil chemotaxis as related to localized juvenile periodontitis (Van Dyke et al., 1983; DeNardin et al., 1990; Dentino et al., 1991). For their PhD theses, Joe Zambon purified and characterized the polysaccharide capsule from Actinobacillus actinomycetemcomitans (Zambon et al., 1984), and Bob Schifferle the capsule from Porphyromonas gingivalis (Schifferle et al., 1989, 1993a,Schifferle et al., b). Ken Miyasaki used high-performance liquid chromatography to purify myeloperoxidase from human neutrophils and study its role in host defense against periodontopathogens (Miyasaki et al., 1987). Many other students, post-doctoral fellows, and faculty took advantage of the unique resources provided by MJL’s laboratory.

	LEVINE’S LEGACY

TOP INTRODUCTION FOUNDATIONS "TRUCKIN’ BACK TO... SALIVA, PELLICLES, AND DENTAL... AN ENVIRONMENT FOR LEARNING LEVINE’S LEGACY EPILOGUE REFERENCES

 
Notwithstanding MJL’s achievements in and providing the materials and technology for research, his most outstanding contribution to oral health science was his mentorship of PhD students (13) and post-doctoral fellows (24). Most of these individuals are presently active in academic or research positions throughout the world. Indeed, many of his students have gone on to train their own cadre of students (see Fig. 2). Through these progeny, it is obvious that MJL’s influence will be felt by the oral health research community for some time to come.

View larger version (17K): [in this window] [in a new window]   Figure 2. Academic progeny of Art Ellison and Michael Levine.

	EPILOGUE

TOP INTRODUCTION FOUNDATIONS "TRUCKIN’ BACK TO... SALIVA, PELLICLES, AND DENTAL... AN ENVIRONMENT FOR LEARNING LEVINE’S LEGACY EPILOGUE REFERENCES

Is it possible that such a research environment could evolve again? The financial limitations of state governments and universities, the vagaries of grant-funding, and the unfortunate lack of interest on the part of contemporary dental student graduates in basic research suggest that the probability of such a group coming together in the future is remote indeed.

MJL’s hard work and extensive accomplishments in research and dental education did not come without a price. After 25 years on the faculty at Buffalo, he retired from full-time research activity in 2000. He continues to spend two days a week teaching periodontics to junior and senior dental students at the University at Buffalo (punctuated by frequent trips to Hawaii). While he was never very active in teaching undergraduate dental students when he was engaged in full-time research, he has embraced clinical teaching and is now a favorite of the dental students. Some things never change: He continues to tease, cajole, entertain, and inspire his students to do more work than they ever wanted to do!

	ACKNOWLEDGMENTS

 
The author thanks Mark Herzberg and Larry Tabak for reading the manuscript and providing important details of the early history of the MJL research group.

Received June 4, 2002; Accepted October 2, 2002

	REFERENCES

TOP INTRODUCTION FOUNDATIONS "TRUCKIN’ BACK TO... SALIVA, PELLICLES, AND DENTAL... AN ENVIRONMENT FOR LEARNING LEVINE’S LEGACY EPILOGUE REFERENCES

 
Aguirre A, Mendoza B, Reddy MS, Scannapieco FA, Levine MJ, Hatton MN (1989). Lubrication of selected salivary molecules and artificial salivas. Dysphagia4:95–100.[Medline]

Al-Hashimi I, Levine MJ (1989). Characterization of in vivo salivary-derived enamel pellicle. Arch Oral Biol 34:289–295.[ISI][Medline]

Al-Hashimi I, Dickinson DP, Levine Ml (1988). Purification, molecular cloning, and sequencing of salivary cystatin SA-1. J Biol Chem 263:9381–9387.[Abstract/Free Full Text]

Bergey EJ, Levine MJ, Reddy MS, Bradway SD, Al-Hashimi I (1986). Use of the photoaffinity cross-linking agent N-hydroxysuccinimidyl-4-azidosalicylic acid to characterize salivary-glycoprotein bacterial interactions. Biochem J 234:43–48.[ISI][Medline]

Biesbrock AR, Reddy MS, Levine MJ (1991). Interaction of a salivary mucin-secretory immunoglobulin A complex with mucosal pathogens. Infect Immun 59:3492–3497.[Abstract/Free Full Text]

Bobek LA, Levine MJ (1992). Cystatins—inhibitors of cysteine proteinases. Crit Rev Oral Biol Med 3:307–332.[Abstract/Free Full Text]

Bobek LA, Tsai H, Biesbrock AR, Levine MJ (1993). Molecular cloning, sequence, and specificity of expression of the gene encoding the low molecular weight human salivary mucin (MUC7). J Biol Chem 268:20563–20569.[Abstract/Free Full Text]

Bobek LA, Ramasubbu N, Wang X, Weaver TR, Levine MJ (1994). Biological activities and secondary structures of variant forms of human salivary cystatin SN produced in Escherichia coli. Gene 15:303–308.

Bradway SD, Bergey EJ, Scannapieco FA, Ramasubbu N, Zawacki S, Levine MJ (1992). Formation of salivary-mucosal pellicle: the role of transglutaminase. Biochem J 284:557–564.

Cohen RE, Aguirre A, Neiders ME, Levine MJ, Jones PC, Reddy MS, et al. (1990). Immunochemistry of high molecular-weight salivary mucin. Arch Oral Biol 35:127–136.[ISI][Medline]

Cohen RE, Aguirre A, Neiders ME, Levine MJ, Jones PC, Reddy MS, et al. (1991). Immunochemistry and immunogenicity of low molecular weight human salivary mucin. Arch Oral Biol 36:347–356.[ISI][Medline]

DeNardin E, DeLuca C, Levine MJ, Genco RJ (1990). Antibodies directed to the chemotactic factor receptor detect differences between chemotactically normal and defective neutrophils from LJP patients. J Periodontol 61:609–617.[ISI][Medline]

Dentino AR, Raj PA, Bhandary KK, Wilson ME, Levine MJ (1991). Role of peptide backbone conformation on biological activity of chemotactic peptides. J Biol Chem 266:18460–18468.[Abstract/Free Full Text]

Douglas WH, Reeh ES, Ramasubbu N, Raj PA, Bhandary KK, Levine MJ (1991). Statherin: a major boundary lubricant of human saliva. Biochem Biophys Res Commun 180:91–97.[ISI][Medline]

Edgerton M, Levine MJ (1992). Characterization of acquired denture pellicle from healthy and stomatitis patients. J Prosthet Dent 68:683–691.[ISI][Medline]

Ellison SA (1966). Salivary antigens. J Dent Res 45:644–654.[Free Full Text]

Ellison SA (1992). Research and research training: the beginnings. In: Roots of renown: history of the School of Dental Medicine, 1882-1992. Powell RA editor. Buffalo: University at Buffalo.

Emmings FG (1999). Oral biology, a dialogue: Solon Arthur Ellison at the State University of New York at Buffalo. J Dent Res 78:725–729.[Free Full Text]

Hatton MN, Loomis RE, Levine MJ, Tabak LA (1985). Masticatory lubrication. The role of carbohydrate in the lubricating property of a salivary glycoprotein-albumin complex. Biochem J 230:817–820.[ISI][Medline]

Levine MJ, Weill JC, Ellison SA (1969). The isolation and analysis of a glycoprotein from parotid saliva. Biochim Biophys Acta 188:165–167.[Medline]

Levine MJ, Herzberg MC, Levine MS, Ellison SA, Stinson MW, Li HC, et al. (1978). Specificity of salivary-bacterial interactions: role of terminal sialic acid residues in the interaction of salivary glycoprotein with Streptococcus sanguis and Streptococcus mutans. Infect Immun 19:107–115.[Abstract/Free Full Text]

Li HC, Levine MJ (1980). Characterization of a glycopeptide from the proline-rich glycoprotein of human parotid saliva. Arch Oral Biol 25:353–355.[ISI][Medline]

Loomis RE, Prakobphol A, Levine MJ, Reddy MS, Jones PC (1987). Biochemical and biophysical comparison of two mucins from human submandibular-sublingual saliva. Arch Biochem Biophys 258:452–464.[ISI][Medline]

Miyasaki KT, Zambon JJ, Jones CA, Wilson ME (1987). Role of high-avidity binding of human neutrophil myeloperoxidase in the killing of Actinobacillus actinomycetemcomitans. Infect Immun 55:1029–1036.[Abstract/Free Full Text]

Murray PA, Levine MJ, Tabak LA, Reddy MS (1982). Specificity of salivary-bacterial interactions: II. Evidence for a lectin on Streptococcus sanguis with specificity for a NeuAcalpha2, 3Galbeta1, 3GalNAc sequence. Biochem Biophys Res Commun 106:390–396.[ISI][Medline]

Murray PA, Levine MJ, Reddy MS, Tabak LA, Bergey EJ (1986). Preparation of a sialic acid-binding protein from Streptococcus mitis KS32AR. Infect Immun 53:359–365.[Abstract/Free Full Text]

Prakobphol A, Levine MJ, Tabak LA, Reddy MS (1982). Purification of a low-molecular-weight, mucin-type glycoprotein from human submandibular-sublingual saliva. Carbohydr Res 108:111–122.[ISI][Medline]

Raj PA, Edgerton M, Levine MJ (1990). Salivary histatin 5: dependence of sequence, chain length, and helical conformation for candidacidal activity. J Biol Chem 265:3898–3905.[Abstract/Free Full Text]

Ramasubbu N, Paloth V, Luo Y, Brayer GD, Levine MJ (1996). The structure of human salivary -amylase at 1.6Å resolution: implications for its role in the oral cavity. J Crystal 52(D):435–446.

Reddy MS, Levine MJ, Prakobphol A (1985). Oligosaccharide structures of the low-molecular-weight salivary mucin from a normal individual and one with cystic fibrosis. J Dent Res 64:33–36.[Abstract/Free Full Text]

Scannapieco FA, Bergey EJ, Reddy MS, Levine MJ (1989). Characterization of salivary -amylase binding to Streptococcus sanguis. Infect Immun 57:2853–2863.[Abstract/Free Full Text]

Scannapieco FA, Torres G, Levine MJ (1993). Salivary -amylase: role in dental plaque and caries formation. Crit Rev Oral Biol Med 4:301–307.[Abstract/Free Full Text]

Schifferle RE, Reddy MS, Zambon JJ, Genco RJ, Levine MJ (1989). Characterization of a polysaccharide antigen from Bacteroides gingivalis. J Immunol 143:3035–3042.[Abstract]

Schifferle RE, Chen PB, Davern LB, Aguirre A, Genco RJ, Levine MJ (1993a). Modification of experimental Porphyromonas gingivalis murine infection by immunization with a polysaccharide-protein conjugate. Oral Microbiol Immunol 8:266–271.[ISI][Medline]

Schifferle RE, Wilson ME, Levine MJ, Genco RJ (1993b). Activation of serum complement by polysaccharide-containing antigens of Porphyromonas gingivalis. J Periodontal Res 28:248–254.[ISI][Medline]

Shomers JP, Tabak LA, Levine MJ, Mandel ID, Hay DI (1982). Properties of cysteine-containing phosphoproteins from human submandibular-sublingual saliva. J Dent Res 61:397–399.[Free Full Text]

Staab JF, Bradway SD, Fidel PL, Sundstrom P (1999). Adhesive and mammalian transglutaminase substrate properties of Candida albicans Hwpl. Science 283:1535–1538.[Abstract/Free Full Text]

Swann DA, Hendren RB, Radin EL, Sotman SL, Duda EA (1981). The lubricating activity of synovial fluid glycoproteins. Arthritis Rheum 24:22–30.[ISI][Medline]

Tabak LA, Levine MJ, Mandel ID, Ellison SA (1982). Role of salivary mucins in the protection of the oral cavity. J Oral Pathol 11:1–17.[ISI][Medline]

Tseng CC, Miyamoto M, Ramalingam K, Hemavathy KC, Levine MJ, Ramasubbu N (1999). The roles of histidine residues at the starch binding site in Streptococcal-binding activities of human salivary -amylase. Arch Oral Biol 44:119–127.[ISI][Medline]

Van Dyke TE, Bartholomew E, Genco RJ, Slots J, Levine MJ (1983). Juvenile periodontitis as a model for neutrophil function: reduced binding of the complement chemotactic fragment C5a. J Periodontol 52:502–508.

Zambon JJ, Slots J, Miyasaki K, Linzer R, Cohen R, Levine M, et al. (1984). Purification and characterization of the serotype c antigen from Actinobacillus actinomycetemcomitans. Infect Immun 44:22–27.[Abstract/Free Full Text]

This Article Figures Only Full Text (PDF) Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Scannapieco, F. A. Search for Related Content PubMed PubMed Citation Articles by Scannapieco, F. A.