Suppression of bactericidal activity of human polymorphonuclear leukocytes by Bacteroides gingivalis

Abstract

The direct effects of the culture supernatant of oral microorganisms on the bactericidal activity of human polymorphonuclear leukocytes (PMNs) were investigated. The bactericidal activity of PMNs, which were preincubated with the supernatant of Bacteroides gingivalis, Bacteroides intermedius, Bacteroides melaninogenicus or phosphate-buffered saline, was examined by counting the surviving bacteria. B. gingivalis-treated PMNs were found to have a diminished ability for killing bacteria in the presence or absence of serum. The chemiluminescence response of PMNs, which were preincubated with the culture supernatant of B. gingivalis, was strikingly reduced compared with that of PMNs preincubated with phosphate-buffered saline or other bacterial culture supernatants. The production of superoxide anion (02-) by PMNs stimulated with either formyl-methionyl-leucyl-phenylalanine or phorbol myristate acetate was reduced in both cases after the PMNs were preincubated with the culture supernatant of B. gingivalis. However, it was observed that there was more reduction in superoxide anion (02) production stimulated with formyl-methionyl-leucyl-phenyalanine compared with that stimulated with phorbol myristate acetate. These results suggest that B. gingivalis releases a factor which interferes with the bactericidal activity of PMNs by modulating the generation of reactive oxygen species. These suppressive effects on bactericidal activity may be important in the pathogenesis of this microorganism. Chronic inflammatory periodontal disease is initiated by bacterial infection. The role of specific gram-negative bacteria in the etiology and pathogenesis of human periodontal disease has been increasingly appreciated in recent years (20, 37). It is generally accepted that Bacteroides gingivalis is closely associated with adult periodontitis (7, 11, 21, 23). Furthermore, the interrelationship between a progression of inflammatory periodontal disease and polymorphonuclear leukocytes (PMNs), which act as one of the host defense systems against bacterial infection, has been widely investigated (2, 4, 9, 15, 27, 44). It has been reported that patients with a diminished function of PMNs often suffered from severe periodontal breakdown (5, 6, 39). Loesche et al. (16) recently reported that gingival crevicular PMNs collected from diseased sites had a diminished ability to form oxidized products after phorbol myristate acetate (PMA) stimulation. This result suggests that the functions of PMNs are affected by the bacteria found in subgingival plaque at the site of periodontal pockets. Van Dyke (43) reported that the soluble products of periodontopathic microorganisms modulated the receptors of the PMNs. It has been also reported that several factors from B. gingivalis affected the function of PMNs (12, 19, 22, 24). We recently reported (18) that the soluble factor from B. gingivalis suppressed the superoxide anion (02-) production of PMNs via the modulation of cell surface receptors and internal cellular events. Because of this result,

Adherence of Porphyromonas gingivalis to matrix proteins via a fimbrial cryptic receptor exposed by its own arginine‐specific protease

“…P. gingivalis protease has been suggested to contribute to the development of periodontal disease in various ways, i.e. degrading the connective tissues (Uitto et al, 1988), binding to fibronectin and laminin (Pike et al, 1996), inactivating immunoglobulins (Grenier et al, 1989;Sato et al, 1987) and the complement systems (Grenier and McBride, 1987), activating the kallikrein cascade (Nilsson et al, 1985), or disrupting the functions of the polymorphonuclear leukocytes (Yoneda et al, 1990). In addition, P. gingivalis protease may act as a processing protease responsible for the maturation of fimbriae (Nakayama et al, 1996).…”

Role of bacterial proteinases in matrix destruction and modulation of host responses

“…Moreover, they indicate that, at the gingival level, there is a very delicate balance between neutrophils and plaque microorganisms that can easily be disturbed by periodontal pathogens. In adult periodontitis there is no clear intrinsic neutrophil disorder but, as several lines of evidence indicate, locally induced phagocyte dysfunction is a result of interactions with factors, released from plaque microorganisms (61,236,317,342,359,375). Among these factors, proteinases seem to play a critical role.…”

Antibody responses to Porphyromonas gingivalis infection in a murine abscess model – involvement of gingipains and responses to re‐infection

“…P. gingivalis possesses many virulence factors, such as fimbriae (3), lipopolysaccharide (4), proteases (5) and so on. We previously reported that P. gingivalis suppresses the functions of polymorphonuclear leukocytes (6), and revealed that the suppression is mainly caused by a cysteine proteinase (7). The cysteine proteinases named gingipains (8) have been well characterized by many groups and reviewed recently (9).…”