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Identification of Mycobacterium Avium Pathogenicity Island Important For MICROBIOLOGY. For the article ‘‘Identification of Mycobacterium avium pathogenicity island important for macrophage and amoeba infection,’’ by Lia Danelishvili, Martin Wu, Bernadette Stang, Melanie Harriff, Stuart Cirillo, Jeffrey Cirillo, Robert Bildfell, Brian Arbogast, and Luiz E. Bermudez, which appeared in issue 26, June 26, 2007, of Proc Natl Acad Sci USA (104:11038– 11043; first published June 19, 2007; 10.1073͞pnas.0610746104), the author name Stuart Cirillo should have appeared as Suat L. G. Cirillo, and the author name Jeffrey Cirillo should have appeared as Jeffrey D. Cirillo. The online version has been corrected. The corrected author line appears below. Addition- ally, the present address for both these authors should be: Department of Microbial and Molecular Pathogenesis, Texas A&M University College of Medicine, College Station, TX 77843-1114. The authors also note that Fig. 1 did not print at high resolution. The corrected figure and its legend appear below. Lia Danelishvili, Martin Wu, Bernadette Stang, Melanie Harriff, Suat L. G. Cirillo, Jeffrey D. Cirillo, Robert Bildfell, Brian Arbogast, and Luiz E. Bermudez Fig. 1. Chromosome regions. (A) Organization of the chromosome region inactivated in the 8H8 clone of M. avium involved in the glycosylation of the lipopeptide core. (B) Organization of the chromosome region inactivated in the M. avium 9B9 clone. The M. avium gene names correspond to MAP numbers from the M. avium subsp. paratuberculosis genome sequence. (C) Genetic organization of M. avium 104 PI associated with low invasion of macrophages and virulence in mice. The M. avium 104 (b) sequence and gene organization of this region are presented in comparison with M. tuberculosis H37Rv (a) and M. avium subsp. paratuberculosis (c) similar loci. Numbers in parentheses indicate the approximate size of the different regions in the abovementioned mycobacterial species. The gene name or corresponding Rv or MAP number from the M. tuberculosis H37Rv and M. avium subsp. paratu- berculosis genome sequences is shown above the construct. Unknown M. avium genes are presented as ORFs 1–8. The arrows on the genes indicate the location of genes disrupted by the insertion of transposon Tn5367. www.pnas.org͞cgi͞doi͞10.1073͞pnas.0706836104 20636 ͉ www.pnas.org Downloaded by guest on September 25, 2021 Identification of Mycobacterium avium pathogenicity island important for macrophage and amoeba infection Lia Danelishvili*, Martin Wu*, Bernadette Stang*, Melanie Harriff*, Stuart Cirillo†‡, Jeffrey Cirillo†‡, Robert Bildfell*, Brian Arbogast§, and Luiz E. Bermudez*¶ʈ Departments of *Biomedical Sciences, College of Veterinary Medicine, and ¶Microbiology, College of Science, and §Environmental Health Sciences Center, Oregon State University, Corvallis, OR 97331; and ‡Department of Veterinary and Biomedical Sciences, University of Nebraska, Lincoln, NE 68583-0905 Edited by E. Peter Greenberg, University of Washington School of Medicine, Seattle, WA, and approved May 17, 2007 (received for review December 4, 2006) The ability to infect macrophages is a common characteristic shared phagocytic cells, although they can enter and replicate in other host among many mycobacterial species. Mycobacterium avium, Myco- cells (2). The reason some pathogens adapted to the intracellular bacterium tuberculosis, and Mycobacterium kansasii enter macro- environment in the first place is unknown, but presumably it is phages, using the complement receptors CR1, CR3, CR4, and the related to the availability of specific nutrients and because of the mannose receptor. To identify M. avium genes and host cell protection that the intracellular environment provides against host pathways involved in the bacterial uptake by macrophages, we defense mechanisms. It seems to be clear that both M. avium and screened a M. avium transposon mutant library for the inability to M. tuberculosis can alter their environment in the macrophage, very enter macrophages. Uptake-impaired clones were selected. Se- likely creating the right condition for gene expression associated quence of six M. avium clones identified one gene involved in with the natural progression of the disease (12). glycopeptidolipid biosynthesis, one gene encoding the conserved It is possible that M. avium and M. tuberculosis differ regarding membrane protein homologue to the M. avium subsp. paratuber- the primary pathways by which they enter or are ingested by culosis MAP2446c gene and four others belonging to the same macrophages. Although both bacteria have a common ancestor region of the chromosome. Analysis of the chromosome region source, they evolved in a diverse manner, allowing for important revealed a pathogenicity island inserted between two tRNA se- differences to take place in their genome. To obtain new insight into quences with 58% of G؉C content versus 69% in the M. avium the mechanism by which M. avium is ingested by macrophages, it genome. The region is unique for M. avium and is not present in M. was decided to screen a transposon mutant bank for phagocytosis tuberculosis or M. paratuberculosis. Although the mutants did not in vitro. differ from the WT bacterium regarding the binding to macro- phage cell membrane, analysis of macrophage proteins after 1 h Results infection revealed a deficiency in the mutant to phosphorylate Identification of M. avium Mutants Associated With Low Invasion of certain proteins on uptake. To understand M. avium interaction Macrophages. A transposon library was partially screened for inva- with two evolutionarily distinct hosts, the mutants were evaluated sion of human monocyte cell line and the phenotype of the selected for Acanthamoeba castellanii invasion. The defect in the ability of clones was confirmed by using human monocyte-derived macro- the mutants to invade both cells was highly similar, suggesting phages. Three groups of mutants were identified: (i) six clones with that M. avium might have evolved mechanisms that are used to uptake of Ͻ5% in 1 h, compared with 14 Ϯ 0.5% of the WT enter amoebas and human macrophages. bacterium; (ii) 17 clones with uptake between 5% and 8%; and (iii) 39 mutants between 8.1% and 12%. We decided to concentrate uptake initially on the group with Ͻ5% uptake. As shown in Table 1, six clones were identified. Among them, the 8H8 clone had an inac- ycobacterium avium complex is an intracellular pathogen tivated gene belonging to the glycopeptolipid synthesis pathway Mthat can infect a variety of host cells (1–4). M. avium, like (Fig. 1A); the 9B9 clone had a conserved membrane protein the majority of pathogenic mycobacteria, infects and replicates inactivated (Fig. 1B); and the other four clones (9C3, 9E6, 10A11, within macrophages (5, 6), which are the phagocytic cells where and 10B9) had genes in a unique region of the M. avium chromo- M. avium establishes a long-term infection (7). some (Fig. 1C). Among the mutants identified, 9C3, 9E6, and 10B9 A number of studies in vitro have determined that M. avium,in had mutation in the different locations of ORF7 of this region (Fig. a manner similar to Mycobacterium tuberculosis, is taken up by 1C). Although complemented 9C3 strain restored the same phe- macrophages using the complement receptors CR3, CR4, and CR1 notype of the WT bacterium, this was not observed to comple- (8–10), and/or the mannose receptor (8, 11). M. tuberculosis has been found to bind to the CD11b chain of the ␤-integrin of the CR3 Author contributions: L.D. and L.E.B. designed research; L.D., M.W., B.S., S.C., R.B., B.A., and and CR4 receptors, which happened without participation of the L.E.B. performed research; M.H. contributed new reagents/analytic tools; L.D., M.W., B.S., serum complement proteins (10). Other studies demonstrated that M.H., J.C., and L.E.B. analyzed data; and L.D. and L.E.B. wrote the paper. the mannose capped lipoarabinomannan antigen of virulent M. The authors declare no conflict of interest. tuberculosis cell wall is capable to recognize and bind to the This article is a PNAS Direct Submission. mannose receptors on the macrophage membrane (11). Abbreviation: PI, pathogenicity island. It has been hypothesized that virulent mycobacteria bind to many †Present address: Department of Microbiology and Molecular Pathogenesis, TexasA&M receptors because pathogenic mycobacteria would use several University, College of Medicine, College Station, TX 77843–1114. different receptors on the macrophage membrane to be internal- ʈTo whom correspondence should be addressed. Department of Biomedical Sciences Col- ized, as a strategy to guarantee phagocytosis, even when a site- lege of Veterinary Medicine, Oregon State University, Corvallis, OR 97331-8797. E-mail: specific macrophage would not contain one or more membrane [email protected]. receptors. In addition, this property would address the possibility This article contains supporting information online at www.pnas.org/cgi/content/full/ that mycobacteria may not express all of the ligands during all 0610746104/DC1. phases of infection. Most mycobacteria evolved to survive inside © 2007 by The National Academy of Sciences of the USA 11038–11043 ͉ PNAS ͉ June 26, 2007 ͉ vol. 104 ͉ no. 26 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0610746104 Table 1. Percent of uptake and intracellular growth of M. avium Table 2. Invasion of Acanthamoeba castellanii by M. avium 109 and clones in U937 and monocyte-derived macrophages Invasion Uptake Uptake Bacteria strain at1h,% U937 hM0 Growth in Mo WT 28.6 Ϯ 6 Clone (1 h), % (1 h), % U937 (4-day) 8H8 24.7 Ϯ 4 Ϯ WT bacterium 14 Ϯ 0.4 16 Ϯ 0.8 log 1.8 9C3 3.3 1* Ϯ 8H8 2 Ϯ 0.1 2.2 Ϯ 0.1 log 0.1 9E6 3.1 2* Ϯ 9B9 2 Ϯ 0.3 2.1 Ϯ 0.4 log 2.7 9B9 2.7 0.5* Ϯ 9C3 1 Ϯ 0.2 1.0 Ϯ 0.3 log 2.8 Complemented 9C3 27.6 4.2 9E6 3 Ϯ 0.6 2.8 Ϯ 0.2 log 2.5 *, P Ͻ 0.05 compared with the WT bacterium.
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