Interaction between the membrane protein of a pathogen and insect microfilament complex determines insect-vector specificity

• Published in: Proceedings of the National Academy of Sciences - PNAS 2006-03, Vol.103 (11), p.4252-4257
• Main Authors: Suzuki, S, Oshima, K, Kakizawa, S, Arashida, R, Jung, H.Y, Yamaji, Y, Nishigawa, H, Ugaki, M, Namba, S
• Format: Article
• Language: English
• Subjects: actin; Actin Cytoskeleton - metabolism; Actin Cytoskeleton - microbiology; Actins; Actins - metabolism; Animals; antigenic membrane protein; Bacteria; bacterial proteins; Bacterial Proteins - metabolism; Base Sequence; Biological Sciences; Candidatus Phytoplasma asteris; Cloning, Molecular; Disease transmission; disease vectors; DNA, Complementary - genetics; Gels; Genes, Insect; Hemiptera - metabolism; Hemiptera - microbiology; Host parasite relationships; host specificity; insect pests; Insect proteins; Insect Proteins - genetics; Insect Proteins - metabolism; Insect vectors; Insect Vectors - metabolism; Insect Vectors - microbiology; Insects; Macrosteles; Macrosteles striifrons; Membrane proteins; Membrane Proteins - metabolism; Microbiology; Microfilaments; Molecular biology; Multiprotein Complexes; myosin heavy chains; myosin light chains; Myosins - metabolism; Parasite hosts; Pathogens; Phytoplasma; Phytoplasma - metabolism; Phytoplasma - pathogenicity; Plant Diseases - microbiology; plant pathogenic bacteria; protein-protein interactions; Species Specificity; Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.0508668103

Many insect-transmissible pathogens are transmitted by specific insect species and not by others, even if they are closely related. The molecular mechanisms underlying such strict pathogen-insect specificity are poorly understood. Candidatus Phytoplasma asteris, OY strain, line W (OY), is a phytopathogenic bacterium transmitted from plant to plant by sap-feeding insect vectors (leafhoppers). Our study focused on an abundant cell-surface membrane protein of the phytoplasma named antigenic membrane protein (Amp), which is not homologous with any reported functional protein. Immunofluorescence microscopy of the phytoplasma-infected insect showed that OY phytoplasma was localized to the microfilaments of the visceral smooth muscle surrounding the insect's intestinal tract. The affinity column assay showed that Amp forms a complex with three insect proteins: actin, myosin heavy chain, and myosin light chain. Amp-microfilament complexes were detected in all OY-transmitting leafhopper species, but not in the non-OY-transmitting leafhoppers, suggesting that the formation of the Amp-microfilament complex is correlated with the phytoplasma-transmitting capability of leafhoppers. Although several studies have reported interactions between pathogens and mammalian microfilaments, this is an example of host-specific interactions between a bacterial surface protein and a host microfilament in insect cells. Our data also suggest that the utilization of a host microfilament may be a universal system for pathogenic bacteria infecting mammals or insects.