Table 1. Examples of Bacterial Proteins Interfering with UBI/UBL Conjugation to Host Proteinsa.
UBI/UBL target | Bacteria | Extra/intracellular bacteria | Effector | Enzymatic activity | Effect | Refs |
---|---|---|---|---|---|---|
UBI | Salmonella Typhimurium | Intracellular | SopA | E3 UBI ligase (HECT) | Regulation of host inflammation | [67] |
UBI | EPEC, EHEC | Extracellular | NleL | E3 UBI ligase (HECT) | Regulation of actin pedestal formation | [101] |
UBI | EPEC, EHEC | Extracellular | NleG | E3 UBI ligase (RING) | ND | [102] |
UBI | Pseudomonas syringae | Extracellular | AvrPtoB | E3 UBI ligase (U-box) | Inhibition of plant pattern-triggered immunity | [103,104] |
UBI | Shigella flexneri | Intracellular | OspI | Gln deamidase | Inactivation of UBE2N/UBC13 (E2 UBI enzyme (NF-κB pathway) | [34] |
UBI | Shigella flexneri | Intracellular | IpaH1.4 | E3 UBI ligase (NEL) | Ubiquitination of LUBAC (NF-κB pathway) | [60] |
UBI | Shigella flexneri | Intracellular | IpaH2.5 | E3 UBI ligase (NEL) | Ubiquitination of LUBAC (NF-κB pathway) | [60] |
UBI | Shigella flexneri | Intracellular | IpaH0722 | E3 UBI ligase (NEL) | Ubiquitination of TRAF2 (NF-κB pathway) | [62] |
UBI | Shigella flexneri | Intracellular | IpaH9.8 | E3 UBI ligase (NEL) | Ubiquitination of NEMO (NF-κB pathway) | [61] |
UBI | Salmonella Typhimurium | Intracellular | Ssph1 | E3 UBI ligase (NEL) | Ubiquitination of PKN1 (NF-κB pathway) | [105] |
UBI | Legionella pneumophila | Intracellular | SdeA | Non-eukaryotic UBI ligase | E1/E2-independent ubiquitination of RAB GTPases and RTN4 | [46–48] |
UBI | Shigella flexneri | Intracellular | OspG | Kinase | Inhibition of UBCH5 (E2 UBI enzyme; NF-κB pathway) | [63] |
UBI | EPEC, EHEC | Extracellular | NleB | Glycosyltransferase | Inhibition of TRAF2 ubiquitination (NF-κB pathway) | [106] |
UBI | EPEC | Extracellular | ND | ND | Downregulation of UBE1 and UBA6 (E1 UBI enzymes) | [35] |
UBI | EPEC | Extracellular | NleE | Cys methyltransferase | Inactivation of TAB2 and TAB3 (NF-κB pathway) | [67,107] |
UBI | Legionella pneumophila | Intracellular | SidJ | Deubiquitylase | ND | [50] |
UBI | Shigella flexneri | Intracellular | ShiCE | Deubiquitylase | ND | [54] |
UBI | Chlamydia trachomatis | Intracellular | ChlaDUB1 | Deubiquitylase | Inhibition of NF-κB pathway activation | [108,109] |
UBI | Burkholderia pseudomallei | Extracellular | CHBP | Gln deamidase | Deamidation of UBI | [57] |
SUMO | Listeria monocytogenes | Intracellular | LLO | Pore-forming toxin | Downregulation of UBE2I/UBC9 (E2 SUMO enzyme) | [25] |
SUMO | Clostridium perfringens | Extracellular | PFO | Pore-forming toxin | Downregulation of UBE2I/UBC9 (E2 SUMO enzyme) | [25] |
SUMO | Streptococcus pneumoniae | Extracellular | PLY | Pore-forming toxin | Downregulation of UBE2I/UBC9 (E2 SUMO enzyme) | [25] |
SUMO | Shigella flexneri | Intracellular | ND/Ca2+ influx | ND | Proteolytic cleavage of UBA2/SAE2 (E1 SUMO enzyme) | [39] |
SUMO | Salmonella Typhimurium | Intracellular | ND/miRNAs | ND | Downregulation of UBE2I/UBC9 (E2 SUMO enzyme) | [38] |
SUMO | Xanthomonas euvesicatoria | Extracellular | XopD | DeSUMOylase | DeSUMOylation of SIERF4 (plant immune response) | [51,52] |
NEDD8 | EPEC | Extracellular | CIF | Gln deamidase | Deamidation of NEDD8 | [57,58] |
NEDD8 | Chlamydia trachomatis | Intracellular | ChlaDUB1 | DeNEDDylase | Inhibition of NF-κB pathway activation | [108,109] |
Abbreviations: EPEC, enteropathogenic Escherichia coli; EHEC, enterohemorrhagic Escherichia coli; HECT, homologous to the E6-AP C terminus; ND, not determined; NEL, novel E3 ligase; RING, really interesting new gene.