Infection, Immunity, and Allergy Caused by Propionibacterium acnes

A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Medical Microbiology".

Deadline for manuscript submissions: closed (25 June 2022) | Viewed by 17194

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Guest Editor
Department of Human Pathology, Graduate School and Faculty of Medicine, Tokyo Medical and Dental University, 1-5-45 Yushima, Bunkyo-ku, Tokyo 113-8519, Japan
Interests: P. acnes; sarcoidosis; granuloma; prostatitis; prostate cancer; H. pylori; gastritis; gastric cancer; inflammatory bowel diseases; immunohistochemistry
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Special Issue Information

Dear Colleagues,

Propionibacterium acnes, formerly known as Corynebacterium parvum and currently referred to as Cutibacterium acnes, is a gram-positive anaerobic bacterium that is part of the normal microbiota of the skin, oral cavity and gastrointestinal and genitourinary tracts. P. acnes survives intracellularly and persists in macrophages without intracellular replication. An overload of P. acnes in macrophages induces autophagy and some P. acnes remain persistent within these cells. Intracellular P. acnes has been identified in alveolar and sinus macrophages in the lungs and lymph nodes, respectively, and colonies of P. acnes have been isolated from peripheral lungs and mediastinal lymph nodes, even in the absence of inflammation. The bacterium can also invade epithelial cells and has been found to persist intracellularly in prostate glands, where it may lead to the development of disease. The mechanisms that allow us to tolerate the presence of P. acnes in our body without eliciting destructive inflammation are unknown. Alternatively, inflammatory conditions potentially caused by this commensal bacterium have been reported in some patients with diseases of unknown causes. The aim of this Special Issue is to report an overview of the latest research on the complexed interaction between infection, immunity, and hypersensitivity caused by P. acnes and/or other commensal microorganisms that are thought to be normally symbiotic in the human body.

Dr. Yoshinobu Eishi
Guest Editor

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Keywords

  • latent infection
  • persistent infection
  • intracellular bacteria
  • symbiotic bacteria
  • commensal bacteria
  • dormant bacteria
  • cell-wall-deficient bacteria
  • L-form
  • endogenous reactivation
  • allergic endogenous infection
  • autoinflammatory disease
  • innate immunity
  • hypersensitivity
  • immune tolerance
  • Treg
  • Th1/Th17

Published Papers (6 papers)

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Research

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10 pages, 1564 KiB  
Article
Propionibacterium acnes-Derived Circulating Immune Complexes in Sarcoidosis Patients
by Keisuke Uchida, Asuka Furukawa, Akiko Yoneyama, Haruhiko Furusawa, Daisuke Kobayashi, Takashi Ito, Kurara Yamamoto, Masaki Sekine, Keiko Miura, Takumi Akashi, Yoshinobu Eishi and Kenichi Ohashi
Microorganisms 2021, 9(11), 2194; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9112194 - 21 Oct 2021
Cited by 6 | Viewed by 1463
Abstract
Propionibacterium acnes is a potential etiologic agent of sarcoidosis and a dysregulated immune response to the commensal bacterium is suspected to cause granuloma formation. P. acnes-derived insoluble immune complexes were recently demonstrated in sinus macrophages of sarcoidosis lymph nodes, suggesting local proliferation [...] Read more.
Propionibacterium acnes is a potential etiologic agent of sarcoidosis and a dysregulated immune response to the commensal bacterium is suspected to cause granuloma formation. P. acnes-derived insoluble immune complexes were recently demonstrated in sinus macrophages of sarcoidosis lymph nodes, suggesting local proliferation of the bacterium in affected organs. In the present study, we developed a method for detecting P. acnes-derived immune complexes in human blood by measuring the concentration of P. acnes-specific lipoteichoic acid (PLTA) detectable after an antigen retrieval pretreatment of plasma samples. Before pretreatment, anti-PLTA antibody was detected and PLTA could not be detected, in all plasma samples from 51 sarcoidosis patients and 35 healthy volunteers. After pretreatment, however, a significant level of PLTA (>105 ng/mL) was detected in 33 (65%) sarcoidosis patients and 5 (14%) control subjects, with 86% specificity and 65% sensitivity for sarcoidosis. In both groups, plasma anti-PLTA antibody titers did not differ between samples with and without detection of PLTA. PLTA levels were abnormally increased (>202 ng/mL) in 21 (41%) sarcoidosis patients. These findings suggest that P. acnes-derived circulating immune complexes present in human blood are abnormally increased in many sarcoidosis patients, presumably due to local proliferation of the bacterium in the affected organs. Full article
(This article belongs to the Special Issue Infection, Immunity, and Allergy Caused by Propionibacterium acnes)
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14 pages, 2479 KiB  
Article
Immunohistochemical Detection of Propionibacterium acnes in Granulomas for Differentiating Sarcoidosis from Other Granulomatous Diseases Utilizing an Automated System with a Commercially Available PAB Antibody
by Takuma Isshiki, Sakae Homma, Yoshinobu Eishi, Matsuko Yabe, Kazuya Koyama, Yasuhiko Nishioka, Tetsuo Yamaguchi, Keisuke Uchida, Kurara Yamamoto, Kenichi Ohashi, Atsushi Arakawa, Kazutoshi Shibuya, Susumu Sakamoto and Kazuma Kishi
Microorganisms 2021, 9(8), 1668; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9081668 - 04 Aug 2021
Cited by 9 | Viewed by 2216
Abstract
Propionibacterium acnes is implicated in the pathogenesis of sarcoidosis. We investigated the usefulness of immunohistochemistry (IHC) with a commercially available P. acnes-specific monoclonal antibody (PAB antibody) for differentiating sarcoidosis from other granulomatous diseases. Formalin-fixed paraffin-embedded tissue samples from 94 sarcoidosis patients and [...] Read more.
Propionibacterium acnes is implicated in the pathogenesis of sarcoidosis. We investigated the usefulness of immunohistochemistry (IHC) with a commercially available P. acnes-specific monoclonal antibody (PAB antibody) for differentiating sarcoidosis from other granulomatous diseases. Formalin-fixed paraffin-embedded tissue samples from 94 sarcoidosis patients and 30 control patients with other granulomatous diseases were examined by the original manual IHC method. We also compared the detection frequency of P. acnes in sarcoid granulomas between manual and automated IHC methods. P. acnes was detected in sarcoid granulomas of samples obtained by transbronchial lung biopsy (64%), video-associated thoracic surgery (67%), endobronchial-ultrasound-guided transbronchial-needle aspiration (32%), lymph node biopsy (80%), and skin biopsy (80%) from sarcoidosis patients, but not in any non-sarcoid granulomas of the samples obtained from control patients. P. acnes outside granulomas, however, was frequently detected in both groups. The detection status of P. acnes in granulomas did not correlate with the clinical characteristics of sarcoidosis patients. The automated Leica system exhibited the best detection sensitivity (72%) and almost an identical localization for P. acnes in sarcoid granulomas compared with the manual method. IHC with a PAB antibody is useful for differentiating sarcoidosis from other granulomatous diseases by detecting P. acnes in granulomas. An automated method by the Leica system can be used in pathology laboratories for differential diagnosis of granulomas by IHC with the PAB antibody. Full article
(This article belongs to the Special Issue Infection, Immunity, and Allergy Caused by Propionibacterium acnes)
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10 pages, 1447 KiB  
Article
Genomic Analysis of Cutibacterium acnes Strains Isolated from Prosthetic Joint Infections
by Llanos Salar-Vidal, Yvonne Achermann, John-Jairo Aguilera-Correa, Anja Poehlein, Jaime Esteban, Holger Brüggemann and on behalf of the ESCMID Study Group for Implant-Associated Infections (ESGIAI)
Microorganisms 2021, 9(7), 1500; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9071500 - 14 Jul 2021
Cited by 6 | Viewed by 3451
Abstract
Cutibacterium acnes is a common cause of prosthetic joint infections (PJIs). The C. acnes population can be divided into six main phylotypes (IA1, IA2, IB, IC, II and III) that are associated with different clinical conditions and normal skin. [...] Read more.
Cutibacterium acnes is a common cause of prosthetic joint infections (PJIs). The C. acnes population can be divided into six main phylotypes (IA1, IA2, IB, IC, II and III) that are associated with different clinical conditions and normal skin. A single-locus sequence typing (SLST) scheme can distinguish ten main SLST types: A-E (all IA1), F (IA2), G (IC), H (IB), K (II), L (III). We genome-sequenced and compared 16 strains of C. acnes isolated from healthy skin (n = 4) and PJIs (n = 12), including six PJI cases with a good outcome (four shoulder PJIs, one hip PJI, one knee PJI) and six with infection relapse (three shoulder PJIs, three hip PJIs). The sequenced strains belonged to four different phylotypes (IA1, IA2, IB and II) and seven different SLST types. All five type IB strains (all SLST type H1) were PJI isolates (three hip PJIs, two shoulder PJIs), and four of these caused infection relapse (three hip PJIs, one shoulder PJI). Isolates from PJI cases with a good outcome belonged to three different phylotypes (IA, IB, II). Interestingly, four strains (three strains from PJI cases with good outcome and one strain from healthy skin) contained a linear plasmid; these strains belonged to different SLST types (A1, C1, F4, H1) and were isolated in three different hospitals. This study suggests that type IB strains have the potential to cause infection relapse, in particular regarding hip PJIs. Moreover, our study revealed that strains belonging to the same SLST type can differ in their accessory genome in different geographic locations, indicative of microevolution. Full article
(This article belongs to the Special Issue Infection, Immunity, and Allergy Caused by Propionibacterium acnes)
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Review

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14 pages, 2435 KiB  
Review
Potential Association of Cutibacterium acnes with Sarcoidosis as an Endogenous Hypersensitivity Infection
by Yoshinobu Eishi
Microorganisms 2023, 11(2), 289; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms11020289 - 22 Jan 2023
Cited by 5 | Viewed by 2010
Abstract
The immunohistochemical detection of Cutibacterium acnes in sarcoid granulomas suggests its potential role in granuloma formation. C. acnes is the sole microorganism ever isolated from sarcoid lesions. Histopathologic analysis of some sarcoid lymph nodes reveals latent infection and intracellular proliferation of cell-wall-deficient C. [...] Read more.
The immunohistochemical detection of Cutibacterium acnes in sarcoid granulomas suggests its potential role in granuloma formation. C. acnes is the sole microorganism ever isolated from sarcoid lesions. Histopathologic analysis of some sarcoid lymph nodes reveals latent infection and intracellular proliferation of cell-wall-deficient C. acnes followed by insoluble immune-complex formation. Activation of T helper type 1 (Th1) immune responses by C. acnes is generally higher in sarcoidosis patients than in healthy individuals. Pulmonary granulomatosis caused by an experimental adjuvant-induced allergic immune response to C. acnes is preventable by antimicrobials, suggesting that the allergic reaction targets C. acnes commensal in the lungs. C. acnes is the most common bacterium detected intracellularly in human peripheral lungs and mediastinal lymph nodes. Some sarcoidosis patients have increased amounts of C. acnes-derived circulating immune complexes, which suggests the proliferation of C. acnes in affected organs. In predisposed individuals with hypersensitive Th1 immune responses to C. acnes, granulomas may form to confine the intracellular proliferation of latent C. acnes triggered by certain host-related or drug-induced conditions. Current clinical trials in patients with cardiac sarcoidosis are evaluating combined treatment with steroids and antimicrobials during active disease with continued antimicrobial therapy while tapering off steroids after the disease subsides. Full article
(This article belongs to the Special Issue Infection, Immunity, and Allergy Caused by Propionibacterium acnes)
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14 pages, 1876 KiB  
Review
The Role of Cutibacterium acnes in Sarcoidosis: From Antigen to Treatable Trait?
by Raisa Kraaijvanger and Marcel Veltkamp
Microorganisms 2022, 10(8), 1649; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10081649 - 15 Aug 2022
Cited by 6 | Viewed by 4351
Abstract
Cutibacterium acnes (C. acnes, formerly Propionibacterium acnes) is considered to be a non-pathogenic resident of the human skin, as well as mucosal surfaces. However, it also has been demonstrated that C. acnes plays a pathogenic role in diseases such as [...] Read more.
Cutibacterium acnes (C. acnes, formerly Propionibacterium acnes) is considered to be a non-pathogenic resident of the human skin, as well as mucosal surfaces. However, it also has been demonstrated that C. acnes plays a pathogenic role in diseases such as acne vulgaris or implant infections after orthopedic surgery. Besides a role in infectious disease, this bacterium also seems to harbor immunomodulatory effects demonstrated by studies using C. acnes to enhance anti-tumor activity in various cancers or vaccination response. Sarcoidosis is a systemic inflammatory disorder of unknown causes. Cultures of C. acnes in biopsy samples of sarcoidosis patients, its presence in BAL fluid, tissue samples as well as antibodies against this bacterium found in serum of patients with sarcoidosis suggest an etiological role in this disease. In this review we address the antigenic as well as immunomodulatory potential of C. acnes with a focus on sarcoidosis. Furthermore, a potential role for antibiotic treatment in patients with sarcoidosis will be explored. Full article
(This article belongs to the Special Issue Infection, Immunity, and Allergy Caused by Propionibacterium acnes)
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Other

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8 pages, 2724 KiB  
Brief Report
A Potential Predictive Role of the Scalp Microbiome Profiling in Patients with Alopecia Areata: Staphylococcus caprae, Corynebacterium, and Cutibacterium Species
by Eun Jeong Won, Hyun Hee Jang, Hansoo Park and Seong Jin Kim
Microorganisms 2022, 10(5), 864; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10050864 - 21 Apr 2022
Cited by 7 | Viewed by 2287
Abstract
Little is known about the scalp bacterial composition of alopecia areata (AA) patients. The aim of this study was to investigate the differences in the scalp microbiome of AA patients according to their prognosis, in addition to healthy controls. A total of 33 [...] Read more.
Little is known about the scalp bacterial composition of alopecia areata (AA) patients. The aim of this study was to investigate the differences in the scalp microbiome of AA patients according to their prognosis, in addition to healthy controls. A total of 33 AA patients and 12 healthy controls (HC) were included in this study. The microbiomes were characterized by sequencing 16S rRNA genes on the Illumina MiSeq platform. The scalp microbiome was more diverse in AA patients compared to HC, but not significantly different according to the severity of AA. Nevertheless, the higher proportion of Corynebacterium species and the lower proportion of Staphylococcus caprae among the Staphylococcus species were noticed in severe AA patients compared to HC or mild AA. The higher ratio of Cutibacterium species to S. caprae was noticed in severe AA. We highlight the potential predictive role of scalp microbiome profiling to a worse prognosis of patients with alopecia areata. Full article
(This article belongs to the Special Issue Infection, Immunity, and Allergy Caused by Propionibacterium acnes)
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