Tropism and pathogenicity of rickettsiae

Tsuneo Uchiyama, Tsuneo Uchiyama

Abstract

Rickettsiae are obligate intracellular parasitic bacteria that cause febrile exanthematous illnesses such as Rocky Mountain spotted fever, Mediterranean spotted fever, epidemic, and murine typhus, etc. Although the vector ranges of each Rickettsia species are rather restricted; i.e., ticks belonging to Arachnida and lice and fleas belonging to Insecta usually act as vectors for spotted fever group (SFG) and typhus group (TG) rickettsiae, respectively, it would be interesting to elucidate the mechanisms controlling the vector tropism of rickettsiae. This review discusses the factors determining the vector tropism of rickettsiae. In brief, the vector tropism of rickettsiae species is basically consistent with their tropism toward cultured tick and insect cells. The mechanisms responsible for rickettsiae pathogenicity are also described. Recently, genomic analyses of rickettsiae have revealed that they possess several genes that are homologous to those affecting the pathogenicity of other bacteria. Analyses comparing the genomes of pathogenic and non-pathogenic strains of rickettsiae have detected many factors that are related to rickettsial pathogenicity. It is also known that a reduction in the rickettsial genome has occurred during the course of its evolution. Interestingly, Rickettsia species with small genomes, such as Rickettsia prowazekii, are more pathogenic to humans than those with larger genomes. This review also examines the growth kinetics of pathogenic and non-pathogenic species of SFG rickettsiae (SFGR) in mammalian cells. The growth of non-pathogenic species is restricted in these cells, which is mediated, at least in part, by autophagy. The superinfection of non-pathogenic rickettsiae-infected cells with pathogenic rickettsiae results in an elevated yield of the non-pathogenic rickettsiae and the growth of the pathogenic rickettsiae. Autophagy is restricted in these cells. These results are discussed in this review.

Keywords: Rickettsia; insect; pathogenicity; spotted fever group; tick; tropism; typhus group; vector.

Figures

Figure 1
Figure 1
Basic tropism of rickettsiae toward cultured cells. The growth of SFGR and TGR was monitored in cells derived from ticks, insects, and mammals. SFGR grew well in tick cells, while TGR grew well in insect cells. However, the growth of SFGR was restricted in insect cells and that of TGR was restricted in tick cells. Both groups of pathogenic rickettsiae grew well in mammalian cells. Both groups of rickettsiae were confirmed to be capable of adhering to all of the tested cells.
Figure 2
Figure 2
Growth kinetics of SFGR and TGR in insect, tick, and mammalian cells. Various cultured cells were infected with SFGR alone or TGR alone, and the yield of rickettsiae was monitored. Some of the infected cultures were superinfected with TG or SFGR, respectively, on day three of infection, and the growth of each Rickettsia species was monitored.
Figure 3
Figure 3
Scanning electron microscopy of cells infected with TGR and SFGR. (A) AeAl2 cells infected with R. typhi at 10 and 60 min after infection. (B) AeAl2 cells infected with R. japonica at 10 and 60 min after infection. Successful adherence to and invasion of AeAl2 insect cells was achieved by both TGR and SFGR soon after their inoculation. The yellow and red arrows indicate adherent and invading rickettsiae, respectively.
Figure 4
Figure 4
Model of the rickettsia-host cell interactions that occur during the course of infection. The first step in SFGR entry into host cells is the adhesion of rickettsiae to cells due to the binding of many rickettsial adhesins to host cell receptors, followed by the activation of intracellular signaling pathways that induce actin polymerization and membrane rearrangement, causing the attached rickettsiae to be engulfed. Just after clathrin and caveolin-2-dependent phagocytosis, rickettsiae escape from the phagosomes that engulfed them by secreting the phospholipases TlyC and Pld. In the case of SFGR, the surface molecules RicA and Sca2 recruit Arp2/3 to polymerize actin, resulting in the formation of an actin tail, which aids the movement of the bacteria. However, in the case of TGR, R. prowazekii does not have an actin tail, while R. typhi has a very short actin tail. SFGR invade the adjacent cells very early in the course of the infection. Rickettsiae grow within cells by binary fission. The VirB-related T4SS is essential for the intracellular survival of rickettsiae as it allows them to secrete effector molecules.
Figure 5
Figure 5
Growth kinetics of non-pathogenic and pathogenic SFGR in mammalian cells. The growth of non-pathogenic and pathogenic rickettsiae was monitored. Some of the cells that had been infected with non-pathogenic R. montanensis were superinfected with pathogenic R. japonica on day three of infection, and the growth of each Rickettsia was monitored. The growth of non-pathogenic SFGR was restricted in mammalian cells. The superinfection of the infected cells with pathogenic SFGR induced an elevated yield of the non-pathogenic SFGR and the growth of the pathogenic species.
Figure 6
Figure 6
Transmission electron microscopy of Vero cells infected with non-pathogenic and pathogenic SFGR. (A) Vero cells infected with R. montanensis alone was observed at 7 days after infection. An arrow marks a degenerating rickettsia in an autophagosome-like vacuole. (B)R. montanensis-infected cells were superinfected with R. japonica on day three of infection and observed at 7 days after the first infection. Many free rickettsiae around 1 μm in length surrounded by halos and those in the course of binary fission were seen in the cytoplasm. Bars, 1 μm.

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