An O-Methyltransferase Is Required for Infection of Tick Cells by Anaplasma phagocytophilum

Oliva Chávez, Adela S.; Fairman, James W.; Felsheim, Roderick F.; Nelson, Curtis M.; Herron, Michael J.; Higgins, LeeAnn; Burkhardt, Nicole Y.; Oliver, Jonathan D.; Markowski, Todd W.; Kurtti, Timothy J.; Edwards, Thomas E.; Munderloh, Ulrike G.; Skaar, Eric P.

doi:10.1371/journal.ppat.1005248

Title: An O-Methyltransferase Is Required for Infection of Tick Cells by Anaplasma phagocytophilum

Journal Article · Fri Nov 06 00:00:00 EST 2015 · PLoS Pathogens

DOI:https://doi.org/10.1371/journal.ppat.1005248· OSTI ID:1237745

Oliva Chávez, Adela S. ^[1]; Fairman, James W. ^[2]; Felsheim, Roderick F. ^[1]; Nelson, Curtis M. ^[1]; Herron, Michael J. ^[1]; Higgins, LeeAnn ^[3]; Burkhardt, Nicole Y. ^[1]; Oliver, Jonathan D. ^[1]; Markowski, Todd W. ^[3]; Kurtti, Timothy J. ^[1]; Edwards, Thomas E. ^[2]; Munderloh, Ulrike G. ^[1]; Skaar, Eric P. ^[4]

Univ. of Minnesota, Saint Paul, MN (United States)
Emerald Bio, Bainbridge Island, WA (United States); Seattle Structural Genomics Center for Infectious Disease, Seattle, WA (United States)
Univ. of Minnesota, Minneapolis, MN (United States)
Vanderbilt Univ., Nashville, TN (United States)

Anaplasma phagocytophilum, the causative agent of Human Granulocytic Anaplasmosis (HGA), is an obligately intracellular α-proteobacterium that is transmitted by Ixodes spp ticks. However, the pathogen is not transovarially transmitted between tick generations and therefore needs to survive in both a mammalian host and the arthropod vector to complete its life cycle. To adapt to different environments, pathogens rely on differential gene expression as well as the modification of proteins and other molecules. Random transposon mutagenesis of A. phagocytophilum resulted in an insertion within the coding region of an o-methyltransferase (omt) family 3 gene. In wild-type bacteria, expression of omt was up-regulated during binding to tick cells (ISE6) at 2 hr post-inoculation, but nearly absent by 4 hr p.i. Gene disruption reduced bacterial binding to ISE6 cells, and the mutant bacteria that were able to enter the cells were arrested in their replication and development. Analyses of the proteomes of wild-type versus mutant bacteria during binding to ISE6 cells identified Major Surface Protein 4 (Msp4), but also hypothetical protein APH_0406, as the most differentially methylated. Importantly, two glutamic acid residues (the targets of the OMT) were methyl-modified in wild-type Msp4, whereas a single asparagine (not a target of the OMT) was methylated in APH_0406. In vitro methylation assays demonstrated that recombinant OMT specifically methylated Msp4. Towards a greater understanding of the overall structure and catalytic activity of the OMT, we solved the apo (PDB_ID:4OA8), the S-adenosine homocystein-bound (PDB_ID:4OA5), the SAH-Mn²⁺ bound (PDB_ID:4PCA), and SAM- Mn²⁺ bound (PDB_ID:4PCL) X-ray crystal structures of the enzyme. Here, we characterized a mutation in A. phagocytophilum that affected the ability of the bacteria to productively infect cells from its natural vector. Nevertheless, due to the lack of complementation, we cannot rule out secondary mutations.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: National Inst. of Allergy and Infectious Diseases (NIAID); National Inst. of Allergy and Infectious Diseases; National Inst. of Health; Dept. of Health and Human Services; National Science Foundation (NSF)

Grant/Contract Number:: R01-AI042792; HHSN272201200025C; 9871237; NSF-DBI-0215759

OSTI ID:: 1237745

Journal Information:: PLoS Pathogens, Vol. 11, Issue 11; ISSN 1553-7374

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Cited by: 28 works

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Global Transcription Profiles of Anaplasma phagocytophilum at Key Stages of Infection in Tick and Human Cell Lines and Granulocytes Nelson, Curtis M.; Herron, Michael J.; Wang, Xin-Ru Frontiers in Veterinary Science, Vol. 7 https://doi.org/10.3389/fvets.2020.00111	journal	March 2020
Peptide Nucleic Acid Knockdown and Intra-host Cell Complementation of Ehrlichia Type IV Secretion System Effector Sharma, Pratibha; Teymournejad, Omid; Rikihisa, Yasuko Frontiers in Cellular and Infection Microbiology, Vol. 7 https://doi.org/10.3389/fcimb.2017.00228	journal	June 2017
Structural and biochemical characterization of Rv0187, an O-methyltransferase from Mycobacterium tuberculosis Lee, Sanghyun; Kang, Jihoon; Kim, Jungwook Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-44592-7	journal	May 2019
Discovery of in vivo Virulence Genes of Obligatory Intracellular Bacteria by Random Mutagenesis Bekebrede, Hannah; Lin, Mingqun; Teymournejad, Omid Frontiers in Cellular and Infection Microbiology, Vol. 10 https://doi.org/10.3389/fcimb.2020.00002	journal	February 2020
Anaplasma phagocytophilum MSP4 and HSP70 Proteins Are Involved in Interactions with Host Cells during Pathogen Infection Contreras, Marinela; Alberdi, Pilar; Mateos-Hernández, Lourdes Frontiers in Cellular and Infection Microbiology, Vol. 7 https://doi.org/10.3389/fcimb.2017.00307	journal	July 2017
Microbial Invasion vs. Tick Immune Regulation Sonenshine, Daniel E.; Macaluso, Kevin R. Frontiers in Cellular and Infection Microbiology, Vol. 7 https://doi.org/10.3389/fcimb.2017.00390	journal	September 2017

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