Staphylococcus aureus lipoproteins in infectious diseases

Infections with the Gram-positive bacterial pathogen Staphylococcus aureus remain a major challenge for the healthcare system and demand new treatment options. The increasing antibiotic resistance of S. aureus poses additional challenges, consequently inflicting a huge strain in the society due to enormous healthcare costs. S. aureus expresses multiple molecules, including bacterial lipoproteins (Lpps), which play a role not only in immune response but also in disease pathogenesis. S. aureus Lpps, the predominant ligands of TLR2, are important for bacterial survival as they maintain the metabolic activity of the bacteria. Moreover, Lpps possess many diverse properties that are of vital importance for the bacteria. They also contribute to host cell invasion but so far their role in different staphylococcal infections has not been fully defined. In this review, we summarize the current knowledge about S. aureus Lpps and their distinct roles in various infectious disease animal models, such as septic arthritis, sepsis, and skin and soft tissue infections. The molecular and cellular response of the host to S. aureus Lpp exposure is also a primary focus.

[1]  Abukar Ali,et al.  Commensal Bacteria Augment Staphylococcus aureus septic Arthritis in a Dose-Dependent Manner , 2022, Frontiers in Cellular and Infection Microbiology.

[2]  H. Hayen,et al.  Lipoproteins Cause Bone Resorption in a Mouse Model of Staphylococcus aureus Septic Arthritis , 2022, Frontiers in Microbiology.

[3]  S. Feng,et al.  Staphylococcus aureus lipoproteins play crucial roles in inducing inflammatory responses and bacterial internalization into bovine mammary epithelial cells. , 2021, Microbial pathogenesis.

[4]  H. Valadi,et al.  Lipoproteins Are Responsible for the Pro-Inflammatory Property of Staphylococcus aureus Extracellular Vesicles , 2021, International journal of molecular sciences.

[5]  A. Karlsson,et al.  Staphylococcus aureus lipoproteins promote abscess formation in mice, shielding bacteria from immune killing , 2021, Communications biology.

[6]  R. Pullerits,et al.  Bacteria and Host Interplay in Staphylococcus aureus Septic Arthritis and Sepsis , 2021, Pathogens.

[7]  Gordon Y C Cheung,et al.  Pathogenicity and virulence of Staphylococcus aureus , 2021, Virulence.

[8]  D. Missiakas,et al.  The Expression of von Willebrand Factor-Binding Protein Determines Joint-Invading Capacity of Staphylococcus aureus, a Core Mechanism of Septic Arthritis , 2020, mBio.

[9]  S. Han,et al.  Bacterial Lipoproteins Induce BAFF Production via TLR2/MyD88/JNK Signaling Pathways in Dendritic Cells , 2020, Frontiers in Immunology.

[10]  F. Götz,et al.  Lipoproteins in Gram-Positive Bacteria: Abundance, Function, Fitness , 2020, Frontiers in Microbiology.

[11]  Majd Mohammad,et al.  Lipoproteins in Staphylococcus aureus infections , 2020 .

[12]  Timothy C. Meredith,et al.  Lipoprotein N-Acylation in Staphylococcus aureus Is Catalyzed by a Two-Component Acyl Transferase System , 2020, mBio.

[13]  Abukar Ali,et al.  Tofacitinib treatment aggravates Staphylococcus aureus septic arthritis, but attenuates sepsis and enterotoxin induced shock in mice , 2020, Scientific Reports.

[14]  A. Karlsson,et al.  The role of Staphylococcus aureus lipoproteins in hematogenous septic arthritis , 2020, Scientific Reports.

[15]  B. Maček,et al.  Staphylococcus aureus Lpl protein triggers human host cell invasion via activation of Hsp90 receptor , 2020, Cellular microbiology.

[16]  Yifan Rao,et al.  β-Lactam Antibiotics Enhance the Pathogenicity of Methicillin-Resistant Staphylococcus aureus via SarA-Controlled Lipoprotein-Like Cluster Expression , 2019, mBio.

[17]  A. Karlsson,et al.  The YIN and YANG of lipoproteins in developing and preventing infectious arthritis by Staphylococcus aureus , 2019, PLoS pathogens.

[18]  Timothy C. Meredith,et al.  Copper-Induced Expression of a Transmissible Lipoprotein Intramolecular Transacylase Alters Lipoprotein Acylation and the Toll-Like Receptor 2 Response to Listeria monocytogenes , 2019, Journal of bacteriology.

[19]  N. D. de Jong,et al.  Immune Evasion by Staphylococcus aureus , 2019, Microbiology spectrum.

[20]  Suguru Saito,et al.  Staphylococcus aureus Lipoprotein Induces Skin Inflammation, Accompanied with IFN-γ-Producing T Cell Accumulation through Dermal Dendritic Cells , 2018, Pathogens.

[21]  F. Götz,et al.  Toll-Like Receptor 2 and Lipoprotein-Like Lipoproteins Enhance Staphylococcus aureus Invasion in Epithelial Cells , 2018, Infection and Immunity.

[22]  Toshiyuki Shimizu,et al.  Mechanisms controlling nucleic acid-sensing Toll-like receptors , 2018, International immunology.

[23]  O. Tichá,et al.  Lipid moieties on lipoproteins of commensal and non-commensal staphylococci induce differential immune responses , 2017, Nature Communications.

[24]  P. Zhu,et al.  Pretreatment of Pam3CSK4 attenuates inflammatory responses caused by systemic infection of methicillin-resistant Staphylococcus aureus in mice. , 2017, Biomedicine & pharmacotherapy = Biomedecine & pharmacotherapie.

[25]  F. Götz,et al.  Impact of cell wall peptidoglycan O-acetylation on the pathogenesis of Staphylococcus aureus in septic arthritis. , 2017, International journal of medical microbiology : IJMM.

[26]  F. Götz,et al.  Aspartate tightens the anchoring of staphylococcal lipoproteins to the cytoplasmic membrane , 2017, MicrobiologyOpen.

[27]  H. Valadi,et al.  Radiological features of experimental staphylococcal septic arthritis by micro computed tomography scan , 2017, PloS one.

[28]  Y. Le Loir,et al.  Staphylococcus aureus Lpl Lipoproteins Delay G2/M Phase Transition in HeLa Cells , 2016, Front. Cell. Infect. Microbiol..

[29]  R. Pullerits,et al.  RAGE Deficiency Impairs Bacterial Clearance in Murine Staphylococcal Sepsis, but Has No Significant Impact on Staphylococcal Septic Arthritis , 2016, PloS one.

[30]  F. Götz,et al.  Evaluation of Staphylococcus aureus Lipoproteins: Role in Nutritional Acquisition and Pathogenicity , 2016, Front. Microbiol..

[31]  F. Götz,et al.  Lipoproteins of Gram-Positive Bacteria: Key Players in the Immune Response and Virulence , 2016, Microbiology and Molecular Reviews.

[32]  M. Pekna,et al.  Deficiency of the Complement Component 3 but Not Factor B Aggravates Staphylococcus aureus Septic Arthritis in Mice , 2016, Infection and Immunity.

[33]  E. Huizinga,et al.  Structural basis for inhibition of TLR2 by staphylococcal superantigen-like protein 3 (SSL3) , 2015, Proceedings of the National Academy of Sciences.

[34]  E. Josefsson,et al.  IL-1 Receptor Antagonist Treatment Aggravates Staphylococcal Septic Arthritis and Sepsis in Mice , 2015, PloS one.

[35]  K. Ohlsen,et al.  The νSaα Specific Lipoprotein Like Cluster (lpl) of S. aureus USA300 Contributes to Immune Stimulation and Invasion in Human Cells , 2015, PLoS pathogens.

[36]  Vance G. Fowler,et al.  Staphylococcus aureus Infections: Epidemiology, Pathophysiology, Clinical Manifestations, and Management , 2015, Clinical Microbiology Reviews.

[37]  B. Finlay,et al.  Lipoprotein in the cell wall of Staphylococcus aureus is a major inducer of nitric oxide production in murine macrophages. , 2015, Molecular immunology.

[38]  E. Josefsson,et al.  CTLA4 Immunoglobulin but Not Anti-Tumor Necrosis Factor Therapy Promotes Staphylococcal Septic Arthritis in Mice. , 2015, The Journal of infectious diseases.

[39]  N. Buddelmeijer The molecular mechanism of bacterial lipoprotein modification--how, when and why? , 2015, FEMS microbiology reviews.

[40]  Xiaoyang Wang,et al.  Antibiotic‐Killed Staphylococcus aureus Induces Destructive Arthritis in Mice , 2015, Arthritis & rheumatology.

[41]  H. Rammensee,et al.  Cutaneous innate immune sensing of Toll-like receptor 2-6 ligands suppresses T cell immunity by inducing myeloid-derived suppressor cells. , 2014, Immunity.

[42]  I. Autenrieth,et al.  NOD2 Stimulation by Staphylococcus aureus-Derived Peptidoglycan Is Boosted by Toll-Like Receptor 2 Costimulation with Lipoproteins in Dendritic Cells , 2014, Infection and Immunity.

[43]  Eric P. Skaar,et al.  IsdB-dependent hemoglobin binding is required for acquisition of heme by Staphylococcus aureus. , 2014, The Journal of infectious diseases.

[44]  C. Wolz,et al.  Heterogeneity of Host TLR2 Stimulation by Staphylocoocus aureus Isolates , 2014, PloS one.

[45]  A. Chong,et al.  Protective Immunity against Recurrent Staphylococcus aureus Skin Infection Requires Antibody and Interleukin-17A , 2014, Infection and Immunity.

[46]  Timothy J. Foster,et al.  Adhesion, invasion and evasion: the many functions of the surface proteins of Staphylococcus aureus , 2013, Nature Reviews Microbiology.

[47]  Hong-Hee Kim,et al.  Lipoproteins are an important bacterial component responsible for bone destruction through the induction of osteoclast differentiation and activation , 2013, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[48]  Y. Le Loir,et al.  Staphylococcus aureus-Induced G2/M Phase Transition Delay in Host Epithelial Cells Increases Bacterial Infective Efficiency , 2013, PloS one.

[49]  Eric P. Skaar,et al.  Iron in infection and immunity. , 2013, Cell host & microbe.

[50]  Friedrich Götz,et al.  What distinguishes highly pathogenic staphylococci from medium- and non-pathogenic? , 2013, Current topics in microbiology and immunology.

[51]  H. Nakayama,et al.  Lipoproteins in bacteria: structures and biosynthetic pathways , 2012, The FEBS journal.

[52]  J. McCormick,et al.  Staphylococcal superantigens in colonization and disease , 2012, Front. Cell. Inf. Microbio..

[53]  H. Nakayama,et al.  Environment-Mediated Accumulation of Diacyl Lipoproteins over Their Triacyl Counterparts in Staphylococcus aureus , 2012, Journal of bacteriology.

[54]  Eric P. Skaar,et al.  A battle for iron: host sequestration and Staphylococcus aureus acquisition. , 2012, Microbes and infection.

[55]  D. Heinrichs,et al.  The iron-regulated staphylococcal lipoproteins , 2012, Front. Cell. Inf. Microbio..

[56]  L. Miller,et al.  Innate and adaptive immune responses against Staphylococcus aureus skin infections , 2012, Seminars in Immunopathology.

[57]  Eric P Skaar,et al.  Molecular mechanisms of Staphylococcus aureus iron acquisition. , 2011, Annual review of microbiology.

[58]  E. Josefsson,et al.  The combination of a tumor necrosis factor inhibitor and antibiotic alleviates staphylococcal arthritis and sepsis in mice. , 2011, The Journal of infectious diseases.

[59]  A. Edwards,et al.  How does Staphylococcus aureus escape the bloodstream? , 2011, Trends in microbiology.

[60]  F. Taieb,et al.  Cycle Inhibiting Factors (Cifs): Cyclomodulins That Usurp the Ubiquitin-Dependent Degradation Pathway of Host Cells , 2011, Toxins.

[61]  K. Kurokawa,et al.  The role of phagocytosis in IL-8 production by human monocytes in response to lipoproteins on Staphylococcus aureus. , 2011, Biochemical and biophysical research communications.

[62]  R. Titball,et al.  Lipoproteins of Bacterial Pathogens , 2010, Infection and Immunity.

[63]  S. Kaesler,et al.  Staphylococcal Peptidoglycan Co-Localizes with Nod2 and TLR2 and Activates Innate Immune Response via Both Receptors in Primary Murine Keratinocytes , 2010, PloS one.

[64]  S. Kaesler,et al.  Natural Staphylococcus aureus‐derived peptidoglycan fragments activate NOD2 and act as potent costimulators of the innate immune system exclusively in the presence of TLR signals , 2010, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[65]  S. Kaesler,et al.  The Staphylococcus aureus Lipoprotein SitC Colocalizes with Toll-Like Receptor 2 (TLR2) in Murine Keratinocytes and Elicits Intracellular TLR2 Accumulation , 2010, Infection and Immunity.

[66]  R. Landmann,et al.  Staphylococcal lipoproteins and their role in bacterial survival in mice. , 2010, International journal of medical microbiology : IJMM.

[67]  T. Kohler,et al.  The wall teichoic acid and lipoteichoic acid polymers of Staphylococcus aureus. , 2010, International journal of medical microbiology : IJMM.

[68]  J. Belisle,et al.  TLR2 looks at lipoproteins. , 2009, Immunity.

[69]  T. Lamkemeyer,et al.  Role of the Twin-Arginine Translocation Pathway in Staphylococcus , 2009, Journal of bacteriology.

[70]  R. Landmann,et al.  Lipoproteins in Staphylococcus aureus Mediate Inflammation by TLR2 and Iron-Dependent Growth In Vivo1 , 2009, The Journal of Immunology.

[71]  M. Hashimoto,et al.  Characterization of N-terminal Structure of TLR2-activating Lipoprotein in Staphylococcus aureus* , 2009, Journal of Biological Chemistry.

[72]  S. Akira,et al.  The Triacylated ATP Binding Cluster Transporter Substrate-binding Lipoprotein of Staphylococcus aureus Functions as a Native Ligand for Toll-like Receptor 2* , 2009, Journal of Biological Chemistry.

[73]  H. Heine,et al.  TLR2 - promiscuous or specific? A critical re-evaluation of a receptor expressing apparent broad specificity. , 2008, Immunobiology.

[74]  O. Schneewind,et al.  Genome Sequence of Staphylococcus aureus Strain Newman and Comparative Analysis of Staphylococcal Genomes: Polymorphism and Evolution of Two Major Pathogenicity Islands , 2007, Journal of bacteriology.

[75]  S. Akira,et al.  Both TLR2 and TLR4 are required for the effective immune response in Staphylococcus aureus-induced experimental murine brain abscess. , 2008, The American journal of pathology.

[76]  D. Heinrichs,et al.  Heme Coordination by Staphylococcus aureus IsdE* , 2007, Journal of Biological Chemistry.

[77]  Eric P. Skaar,et al.  Staphylococcus aureus IsdB Is a Hemoglobin Receptor Required for Heme Iron Utilization , 2006, Journal of bacteriology.

[78]  D. Missiakas,et al.  Host defenses against Staphylococcus aureus infection require recognition of bacterial lipoproteins , 2006, Proceedings of the National Academy of Sciences.

[79]  M. Hashimoto,et al.  Not Lipoteichoic Acid but Lipoproteins Appear to Be the Dominant Immunobiologically Active Compounds in Staphylococcus aureus1 , 2006, The Journal of Immunology.

[80]  E. Pearlman,et al.  Staphylococcus aureus-Induced Corneal Inflammation Is Dependent on Toll-Like Receptor 2 and Myeloid Differentiation Factor 88 , 2006, Infection and Immunity.

[81]  G. Sensabaugh,et al.  Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus , 2006, The Lancet.

[82]  M. Hashimoto,et al.  Lipoprotein is a predominant Toll-like receptor 2 ligand in Staphylococcus aureus cell wall components. , 2006, International immunology.

[83]  Ryan M. O’Connell,et al.  MyD88 mediates neutrophil recruitment initiated by IL-1R but not TLR2 activation in immunity against Staphylococcus aureus. , 2006, Immunity.

[84]  Alex van Belkum,et al.  The role of nasal carriage in Staphylococcus aureus infections. , 2005, The Lancet. Infectious diseases.

[85]  D. Philpott,et al.  Recognition of Staphylococcus aureus by the Innate Immune System , 2005, Clinical Microbiology Reviews.

[86]  J. Dengjel,et al.  Staphylococcus aureus Deficient in Lipidation of Prelipoproteins Is Attenuated in Growth and Immune Activation , 2005, Infection and Immunity.

[87]  D. Heinrichs,et al.  FhuD1, a Ferric Hydroxamate-binding Lipoprotein in Staphylococcus aureus , 2004, Journal of Biological Chemistry.

[88]  D. Heinrichs,et al.  Involvement of SirABC in Iron-Siderophore Import in Staphylococcus aureus , 2004, Journal of bacteriology.

[89]  Eric P. Skaar,et al.  Iron-Source Preference of Staphylococcus aureus Infections , 2004, Science.

[90]  Katherine O'Riordan,et al.  Staphylococcus aureus Capsular Polysaccharides , 2004, Clinical Microbiology Reviews.

[91]  S. Mazmanian,et al.  An iron-regulated sortase anchors a class of surface protein during Staphylococcus aureus pathogenesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[92]  D. Heinrichs,et al.  Identification and Characterization offhuD1 and fhuD2, Two Genes Involved in Iron-Hydroxamate Uptake in Staphylococcus aureus , 2001, Journal of bacteriology.

[93]  M. Kanehisa,et al.  Whole genome sequencing of meticillin-resistant Staphylococcus aureus , 2001, The Lancet.

[94]  S. Akira,et al.  Cutting Edge: TLR2-Deficient and MyD88-Deficient Mice Are Highly Susceptible to Staphylococcus aureus Infection1 , 2000, The Journal of Immunology.

[95]  Philip J. Hill,et al.  Molecular Cloning and Analysis of a Putative Siderophore ABC Transporter from Staphylococcus aureus , 2000, Infection and Immunity.

[96]  D. Heinrichs,et al.  Identification and Characterization of a Membrane Permease Involved in Iron-Hydroxamate Transport inStaphylococcus aureus , 2000, Journal of bacteriology.

[97]  D. Heinrichs,et al.  Identification and Characterization of a Membrane Permease Involved in Iron-Hydroxamate Transport in Staphylococcus aureus , 2000 .

[98]  P. Godowski,et al.  Cell activation and apoptosis by bacterial lipoproteins through toll-like receptor-2. , 1999, Science.

[99]  B. Bloom,et al.  Host defense mechanisms triggered by microbial lipoproteins through toll-like receptors. , 1999, Science.

[100]  Andrej Tarkowski,et al.  Intra-articularly localized bacterial DNA containing CpG motifs induces arthritis , 1999, Nature Medicine.

[101]  M. Hanson,et al.  Identification and Characterization of SirA, an Iron-Regulated Protein from Staphylococcus aureus , 1999, Journal of bacteriology.

[102]  F. Lowy Staphylococcus aureus infections. , 2009, The New England journal of medicine.

[103]  D. Goldenberg,et al.  Septic arthritis , 1998, The Lancet.

[104]  W. Bessler,et al.  A comparative analysis of cytokine production and tolerance induction by bacterial lipopeptides, lipopolysaccharides and Staphyloccocus aureus in human monocytes , 1997, Immunology.

[105]  W. Bessler,et al.  Stimulation of human and murine adherent cells by bacterial lipoprotein and synthetic lipopeptide analogues. , 1988, Immunobiology.

[106]  K. Pavelić,et al.  Stimulation of humoral immunity by peptidoglycan monomer from Brevibacterium divaricatum. , 1979, Zeitschrift für Immunitätsforschung Immunobiology.

[107]  R. Krause Immunological activity of the peptidoglycan. , 1975, Zeitschrift fur Immunitatsforschung, experimentelle und klinische Immunologie.

[108]  V. Braun,et al.  Chemical characterization, spatial distribution and function of a lipoprotein (murein-lipoprotein) of the E. coli cell wall. The specific effect of trypsin on the membrane structure. , 1969, European journal of biochemistry.

[109]  H. Morton,et al.  Staphylococcus aureus , 1948, Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine.