Genetic Heterogeneity among Strains of<i>Treponema phagedenis</i>-Like Spirochetes Isolated from Dairy Cattle with Papillomatous Digital Dermatitis in Japan

Yano, Takahisa; Yamagami, Ryoko; Misumi, Kazuhiro; Kubota, Chikara; Moe, Kyaw Kyaw; Hayashi, Tetsuya; Yoshitani, Kazunori; Ohtake, Osamu; Misawa, Naoaki

doi:10.1128/jcm.01574-08

Cited by 30 publications

(44 citation statements)

References 40 publications

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“…The idea that various species of Treponema are important is not a novel concept (59)(60)(61), but the role that each of these species plays throughout the course of development has been expanded. There is a group of Treponema spp.…”

Section: Discussionmentioning

confidence: 99%

Deep Sequencing Analysis Reveals Temporal Microbiota Changes Associated with Development of Bovine Digital Dermatitis

et al. 2014

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bBovine digital dermatitis (DD) is a leading cause of lameness in dairy cattle throughout the world. Despite 35 years of research, the definitive etiologic agent associated with the disease process is still unknown. Previous studies have demonstrated that multiple bacterial species are associated with lesions, with spirochetes being the most reliably identified organism. This study details the deep sequencing-based metagenomic evaluation of 48 staged DD biopsy specimens collected during a 3-year longitudinal study of disease progression. Over 175 million sequences were evaluated by utilizing both shotgun and 16S metagenomic techniques. Based on the shotgun sequencing results, there was no evidence of a fungal or DNA viral etiology. The bacterial microbiota of biopsy specimens progresses through a systematic series of changes that correlate with the novel morphological lesion scoring system developed as part of this project. This scoring system was validated, as the microbiota of each stage was statistically significantly different from those of other stages (P < 0.001). The microbiota of control biopsy specimens were the most diverse and became less diverse as lesions developed. Although Treponema spp. predominated in the advanced lesions, they were in relatively low abundance in the newly described early lesions that are associated with the initiation of the disease process. The consortium of Treponema spp. identified at the onset of disease changes considerably as the lesions progress through the morphological stages identified. The results of this study support the hypothesis that DD is a polybacterial disease process and provide unique insights into the temporal changes in bacterial populations throughout lesion development.

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Section: Discussionmentioning

confidence: 99%

Deep Sequencing Analysis Reveals Temporal Microbiota Changes Associated with Development of Bovine Digital Dermatitis

et al. 2014

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“…The numbers of both cultivated and uncultivated Treponema phylotypes reported in recent years have rapidly increased, mainly due to the mass of data obtained from efforts to sequence genes encoding 16S rRNA (Choi et al, 1994;Wyss et al, 2004;Demirkan et al, 2006;Molbak et al, 2006;Nordhoff et al, 2008a;Pringle et al, 2008Pringle et al, , 2009Evans et al, 2009;Sayers et al, 2009;Yano et al, 2009). There are currently 49 species of oral Treponema listed on the Human Oral Microbiome Database (Dewhirst et al, 2010), the best-characterized being T. denticola, Treponema amylovorum, T. lecithinolyticum, Treponema maltophilum, Treponema medium, Treponema parvum, …”

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Virulence Factors of the Oral Spirochete Treponema denticola

et al. 2010

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There is compelling evidence that treponemes are involved in the etiology of several chronic diseases, including chronic periodontitis as well as other forms of periodontal disease. There are interesting parallels with other chronic diseases caused by treponemes that may indicate similar virulence characteristics. Chronic periodontitis is a polymicrobial disease, and recent animal studies indicate that co-infection of Treponema denticola with other periodontal pathogens can enhance alveolar bone resorption. The bacterium has a suite of molecular determinants that could enable it to cause tissue damage and subvert the host immune response. In addition to this, it has several non-classic virulence determinants that enable it to interact with other pathogenic bacteria and the host in ways that are likely to promote disease progression. Recent advances, especially in molecular-based methodologies, have greatly improved our knowledge of this bacterium and its role in disease.

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“…To examine the antigens recognized by antibodies in sera of affected cattle, we selected 18 isolates isolated from 12 cattle on 7 farms among the 40 isolates of T. phagedenis-like spirochetes stored in our laboratory (33). As shown in Table 1, the isolates examined included isolates from different cattle on the same or different farms, isolates from different lesions affecting a single cow, and different isolates from the same lesion affecting a single cow.…”

Section: Methodsmentioning

confidence: 99%

“…Interestingly, considerable genetic diversity was detected among the isolates, not only from different cattle but also from the same individuals, using pulsed-field gel electrophoresis and PCRbased random amplified polymorphism DNA methods (33). Such genetic diversity may underlie the antigenic diversity of these spirochetes, and determination of the bacterial antigens recognized by infected cattle would be useful for the development of a suitable vaccine.…”

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“…Recently, for the first time in Japan, we successfully isolated 40 spirochete isolates from dairy cattle with PDD lesions by using a simple two-step culture technique, and these isolates were identified as Treponema phagedenis-like spirochetes on the basis of their biochemical traits and enzyme activities, which were identical to those of T. phagedenis ATCC 27087, and the results of sequencing of the 16S rRNA gene showing that all isolates had Ͼ99% identity to those of the T. phagedenis type strain and T. phagedenis-like spirochetes isolated from PDD lesions in the United States and Europe (33). Interestingly, considerable genetic diversity was detected among the isolates, not only from different cattle but also from the same individuals, using pulsed-field gel electrophoresis and PCRbased random amplified polymorphism DNA methods (33).…”

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Analysis of the IgG Immune Response toTreponema phagedenis-Like Spirochetes in Individual Dairy Cattle with Papillomatous Digital Dermatitis

Moe

Yano

Misumi

et al. 2010

Clin Vaccine Immunol

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Papillomatous digital dermatitis (PDD) is a major infectious disease of the foot skin in dairy cattle.Treponema phagedenis-like spirochetes have been consistently detected in PDD lesions, and antibodies against these organisms have been demonstrated in affected cattle. However, little is known about the dominant antigens recognized by the immune system of affected cattle. Here, we investigated the IgG immune response to T. phagedenis-like isolates by Western blotting with different sera using whole-cell lysates and extracted glycolipid from 18 and 8 isolates, respectively, including those from different cattle on the same or different farms, isolates from different lesions affecting a single cow, and different isolates from the same lesion affecting a single cow. The reactivity of sera in Western blot assays revealed different banding patterns or showed no bands, suggesting that considerable antigenic variations, including glycolipid, may exist among the isolates, even in those from single individuals. With use of a total of 151 serum samples collected from three groups of cattle, i.e., PDD-positive cows on PDD-positive farms (group A), PDD-negative cows on PDD-positive farms (group B), and cows on PDD-free farms (group C), the levels of IgG antibodies against four T. phagedenis-like isolates were measured by enzyme-linked immunosorbent assay (ELISA). The optical density in groups A and B was significantly higher than that in group C, even though the value varied among the antigens used. Therefore, combinations of multiple Treponema species should be used for serological analysis and the development of a suitable vaccine because of antigenic variations.Papillomatous digital dermatitis (PDD) is an important leading cause of severe epidemic lameness in dairy cows (18), with resulting economic losses due to decreases in milk production and reproductive performance and the costs of treatment (10, 15, 27).Interestingly, among bacteria in the lesions, a large number of spirochetes have been consistently detected, and these have been identified as Treponema species which are closely related to Treponema phagedenis, which is an inhabitant of the human genital tract, and human oral treponemes, including T. denticola, T. vincentii, and T. medium (2, 7, 12). Their presence in both superficial lesions and deeper layers of the epidermis implies that they may be one of the most predominant populations in the lesions and play a role in the pathogenesis of PDD (12,17,19). PDD (4,5,6,29,30,31). It has been reported that the levels of antibodies against treponemes in PDD-positive cattle were significantly higher than those in PDD-negative cattle (4, 30, 31). However, little is known about the dominant antigens recognized by the immune system of affected individual cattle. Because no culture methods for isolating treponemes from PDD lesions have been established, there has been a paucity of antigenic and serological analyses using sufficient numbers of isolates. Humoral and cell-mediated immune responses to T. phagedenis-like spir...

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Genetic Heterogeneity among Strains ofTreponema phagedenis-Like Spirochetes Isolated from Dairy Cattle with Papillomatous Digital Dermatitis in Japan

Cited by 30 publications

References 40 publications

Deep Sequencing Analysis Reveals Temporal Microbiota Changes Associated with Development of Bovine Digital Dermatitis

Deep Sequencing Analysis Reveals Temporal Microbiota Changes Associated with Development of Bovine Digital Dermatitis

Virulence Factors of the Oral Spirochete Treponema denticola

Analysis of the IgG Immune Response toTreponema phagedenis-Like Spirochetes in Individual Dairy Cattle with Papillomatous Digital Dermatitis

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