Characteristics and Immunological Roles of Surface Layer Proteins in Clostridium difficile

다국어 초록 (Multilingual Abstract)

Clostridium difficile is a major causative agent of antibiotic-associated diarrhea and has become the most common pathogen of healthcare-associated infection worldwide. The pathogenesis of C. difficile infection (CDI) is mediated by many factors such as colonization involving attachment to host intestinal epithelial cells, sporulation, germination, and toxin production. Bacterial cell surface components are crucial for the interaction between the bacterium and host cells. C. difficile has two distinct surface layer proteins (SLPs): a conserved high-molecular-weight SLP and a highly variable low-molecular-weight SLP. Recent studies have shown that C. difficile SLPs play roles not only in growth and survival, but also in adhesion to host epithelial cells and induction of cytokine production. Sequence typing of the variable region of the slpA gene, which encodes SLPs, is one of the methods currently used for typing C. difficile. SLPs have received much attention in recent years as vaccine candidates and new therapeutic agents in the treatment of C. difficile-associated diseases. Gaining mechanistic insights into the molecular functions of C. difficile SLPs will help advance our understanding of CDI pathogenesis and the development of vaccines and new therapeutic approaches. In this review, we summarize the characteristics and immunological roles of SLPs in C. difficile.

참고문헌 (Reference)

• 1 Kato H, "Typing of Clostridium difficile isolates endemic in Japan by sequencing of slpA and its application to direct typing" 59 : 556-562, 2010
• 2 Kato H, "Typing by sequencing the slpA gene of Clostridium difficile strains causing multiple outbreaks in Japan" 54 : 167-171, 2005
• 3 Tagashira Y, "Two cases of fulminant colitis due to binary toxin-positive Clostridium difficile that are not PCR ribotype 027 or type 078" 62 : 1486-1489, 2013
• 4 Collins MD, "The phylogeny of the genus Clostridium: proposal of five new genera and eleven new species combinations" 44 : 812-826, 1994
• 5 Freeman J, "The changing epidemiology of Clostridium difficile infections" 23 : 529-549, 2010
• 6 Kandalaft H, "Targeting surface-layer proteins with single-domain antibodies: a potential therapeutic approach against Clostridium difficile-associated disease" 99 : 8549-8562, 2015
• 7 Sanchez-Hurtado K, "Systemic antibody response to Clostridium difficile in colonized patients with and without symptoms and matched controls" 57 : 717-724, 2008
• 8 Merrigan MM, "Surface-layer protein A (SlpA) is a major contributor to host-cell adherence of Clostridium difficile" 8 : e78404-, 2013
• 9 Spigaglia P, "Surface-layer (S-layer) of human and animal Clostridium difficile strains and their behaviour in adherence to epithelial cells and intestinal colonization" 62 : 1386-1393, 2013
• 10 Collins LE, "Surface layer proteins isolated from Clostridium difficile induce clearance responses in macrophages" 16 : 391-400, 2014
• 11 Lynch M, "Surface layer proteins from virulent Clostridium difficile ribotypes exhibit signatures of positive selection with consequences for innate immune response" 17 : 135-, 2017
• 12 Fagan RP, "Structural insights into the molecular organization of the S-layer from Clostridium difficile" 71 : 1308-1322, 2009
• 13 Eidhin DN, "Sequence and phylogenetic analysis of the gene for surface layer protein, slpA, from 14 PCR ribotypes of Clostridium difficile" 55 : 69-83, 2006
• 14 Sara M, "S-layer proteins" 182 : 859-868, 2000
• 15 de la Riva L, "Roles of cysteine proteases Cwp84 and Cwp13 in biogenesis of the cell wall of Clostridium difficile" 193 : 3276-3285, 2011
• 16 Tasteyre A, "Role of FliC and FliD flagellar proteins of Clostridium difficile in adherence and gut colonization" 69 : 7937-7940, 2001
• 17 Bloomfield MG, "Risk factors for mortality in Clostridium difficile infection in the general hospital population: a systematic review" 82 : 1-12, 2012
• 18 Dingle KE, "Recombinational switching of the Clostridium difficile S-layer and a novel glycosylation gene cluster revealed by large-scale whole-genome sequencing" 207 : 675-686, 2013
• 19 Lawson PA, "Reclassification of Clostridium difficile as Clostridioides difficile (Hall and O'Toole 1935) Prevot 1938" 40 : 95-99, 2016
• 20 Peniche AG, "Recent insights into Clostridium difficile pathogenesis" 26 : 447-451, 2013
• 21 Kato H, "Rapid analysis of Clostridium difficile strains recovered from hospitalized patients by using the slpA sequence typing system" 15 : 199-202, 2009
• 22 Takeoka A, "Purification and characterization of S layer proteins from Clostridium difficile GAI 0714" 137 : 261-267, 1991
• 23 Niwa H, "Postoperative Clostridium difficile infection with PCR ribotype 078 strain identified at necropsy in five Thoroughbred racehorses" 173 : 6077-, 2013
• 24 O'Brien JB, "Passive immunization of hamsters against Clostridium difficile infection using antibodies to surface layer proteins" 246 : 199-205, 2005
• 25 Virdi V, "Orally fed seeds producing designer IgAs protect weaned piglets against enterotoxigenic Escherichia coli infection" 110 : 11809-11814, 2013
• 26 Siontorou CG, "Nanobodies as novel agents for disease diagnosis and therapy" 8 : 4215-4227, 2013
• 27 Xiao K, "Multiplex PCR targeting slpA: a rapid screening method to predict common Clostridium difficile ribotypes among fluoroquinolone resistant clinical strains" 45 : 595-599, 2013
• 28 Takahashi M, "Multi-institution case-control and cohort study of risk factors for the development and mortality of Clostridium difficile infections in Japan" 4 : e005665-, 2014
• 29 Miller-Roll T, "Molecular types and antimicrobial susceptibility patterns of Clostridium difficile isolates in different epidemiological settings in a tertiary care center in Israel" 86 : 450-454, 2016
• 30 Cheng JW, "Molecular epidemiology and antimicrobial susceptibility of Clostridium difficile isolates from a university teaching hospital in China" 7 : 1621-, 2016
• 31 Calabi E, "Molecular characterization of the surface layer proteins from Clostridium difficile" 40 : 1187-1199, 2001
• 32 Poilane I, "Molecular characterization of Clostridium difficile clinical isolates in a geriatric hospital" 56 : 386-390, 2007
• 33 Sarker MR, "Molecular basis of early stages of Clostridium difficile infection: germination and colonization" 7 : 933-943, 2012
• 34 Karjalainen T, "Molecular and genomic analysis of genes encoding surface-anchored proteins from Clostridium difficile" 69 : 3442-3446, 2001
• 35 Qazi O, "Mass spectrometric analysis of the S-layer proteins from Clostridium difficile demonstrates the absence of glycosylation" 44 : 368-374, 2009
• 36 Oren A, "List of new names and new combinations previously effectively, but not validly, published" 65 : 3763-3767, 2015
• 37 Shirvan AN, "Isolation of recombinant antibodies directed against surface proteins of Clostridium difficile" 47 : 394-402, 2016
• 38 Honda H, "Incidence and mortality associated with Clostridium difficile infection at a Japanese tertiary care center" 25 : 5-10, 2014
• 39 Bianco M, "Immunomodulatory activities of surface-layer proteins obtained from epidemic and hypervirulent Clostridium difficile strains" 60 : 1162-1167, 2011
• 40 Bruxelle JF, "Immunogenic properties of the surface layer precursor of Clostridium difficile and vaccination assays in animal models" 37 : 78-84, 2016
• 41 Madan R, "Immune responses to Clostridium difficile infection" 18 : 658-666, 2012
• 42 Janoir C, "Identification and characterization of a fibronectin-binding protein from Clostridium difficile" 149 : 2779-2787, 2003
• 43 Drudy D, "Human antibody response to surface layer proteins in Clostridium difficile infection" 41 : 237-242, 2004
• 44 Collins DA, "Epidemiology of Clostridium difficile infection in Asia" 2 : 21-, 2013
• 45 von Muller L, "Epidemiology of Clostridium difficile in Germany based on a single center long-term surveillance and German-wide genotyping of recent isolates provided to the advisory laboratory for diagnostic reasons" 305 : 807-813, 2015
• 46 Goorhuis A, "Emergence of Clostridium difficile infection due to a new hypervirulent strain, polymerase chain reaction ribotype 078" 47 : 1162-1170, 2008
• 47 Knight DR, "Diversity and evolution in the genome of Clostridium difficile" 28 : 721-741, 2015
• 48 Stahlmann J, "Detection of nosocomial Clostridium difficile infections with toxigenic strains despite negative toxin A and B testing on stool samples" 20 : 590-592, 2014
• 49 Killgore G, "Comparison of seven techniques for typing international epidemic strains of Clostridium difficile: restriction endonuclease analysis, pulsed-field gel electrophoresis, PCR-ribotyping, multilocus sequence typing, multilocus variable-number tandem-repeat analysis, amplified fragment length polymorphism, and surface layer protein A gene sequence typing" 46 : 431-437, 2008
• 50 Ternan NG, "Comparative transcriptional analysis of clinically relevant heat stress response in Clostridium difficile strain 630" 7 : e42410-, 2012
• 51 Walk ST, "Clostridium difficile ribotype does not predict severe infection" 55 : 1661-1668, 2012
• 52 McCoubrey J, "Clostridium difficile in a geriatric unit: a prospective epidemiological study employing a novel S-layer typing method" 52 : 573-578, 2003
• 53 Fagan RP, "Clostridium difficile has two parallel and essential Sec secretion systems" 286 : 27483-27493, 2011
• 54 Karjalainen T, "Clostridium difficile genotyping based on slpA variable region in S-layer gene sequence: an alternative to serotyping" 40 : 2452-2458, 2002
• 55 Gerding DN, "Clostridium difficile binary toxin CDT" 5 : 15-27, 2014
• 56 Mori N, "Clinical characteristics and risk factors for community-acquired Clostridium difficile infection: a retrospective, case-control study in a tertiary care hospital in Japan" 21 : 864-867, 2015
• 57 Cerquetti M, "Characterization of surface layer proteins from different Clostridium difficile clinical isolates" 28 : 363-372, 2000
• 58 Waligora AJ, "Characterization of a cell surface protein of Clostridium difficile with adhesive properties" 69 : 2144-2153, 2001
• 59 Joost I, "Characterization of Clostridium difficile isolates by slpA and tcdC gene sequencing" 33 (33): S13-S18, 2009
• 60 Masuda K, "Characterization and reassembly of a regular array in the cell wall of Clostridium difficile GAI 4131" 33 : 287-298, 1989
• 61 Kirk JA, "Characteristics of the Clostridium difficile cell envelope and its importance in therapeutics" 10 : 76-90, 2017
• 62 Huber CA, "Challenges for standardization of Clostridium difficile typing methods" 51 : 2810-2814, 2013
• 63 Lessa FC, "Burden of Clostridium difficile infection in the United States" 372 : 825-834, 2015
• 64 Fagan RP, "Biogenesis and functions of bacterial Slayers" 12 : 211-222, 2014
• 65 Calabi E, "Binding of Clostridium difficile surface layer proteins to gastrointestinal tissues" 70 : 5770-5778, 2002
• 66 Marsh JW, "Association of relapse of Clostridium difficile disease with BI/NAP1/027" 50 : 4078-4082, 2012
• 67 Hensgens MPM, "All-cause and disease-specific mortality in hospitalized patients with Clostridium difficile infection: a multicenter cohort study" 56 : 1108-1116, 2013
• 68 Ni Eidhin DB, "Active immunization of hamsters against Clostridium difficile infection using surface-layer protein" 52 : 207-218, 2008
• 69 Ryan A, "A role for TLR4 in Clostridium difficile infection and the recognition of surface layer proteins" 7 : e1002076-, 2011
• 70 Fagan RP, "A proposed nomenclature for cell wall proteins of Clostridium difficile" 60 : 1225-1228, 2011
• 71 Yutin N, "A genomic update on clostridial phylogeny: Gram-negative spore formers and other misplaced clostridia" 15 : 2631-2641, 2013