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Infection and Immunity, October 1999, p. 5069-5075, Vol. 67, No. 10
Kuzell Institute for Arthritis and Infectious
Diseases, California Pacific Medical Center Research Institute, San
Francisco, California 94115
Received 3 May 1999/Returned for modification 14 June 1999/Accepted 14 July 1999
Mycobacterium avium is an opportunistic pathogen in
AIDS patients, who acquire the infection mainly through the
gastrointestinal tract. Previous studies in vitro have shown that
M. avium invades epithelial cells of both intestinal and
laryngeal origin. In addition, M. avium enters the
intestinal mucosa of healthy mice. Because M. avium
invasion of the intestinal mucosa in vivo initially is not accompanied
by significant influx of inflammatory cells, we sought to determine
whether M. avium would trigger chemokine release upon entry
into epithelial cells by using HT-29 intestinal and HEp-2 laryngeal
epithelial cell lines. Chemokine synthesis was measured both by the
presence of specific mRNA and protein secretion in the cell culture
supernatant as determined by enzyme-linked immunosorbent assay.
Infection of HT-29 intestinal cells with M. avium did not
induce the release of interleukin-8 (IL-8) or RANTES for up to 7 days
postinfection. However, infection of HEp-2 cells resulted in the
release of IL-8 and RANTES at 72 h. Similar findings were observed
with other AIDS M. avium isolates belonging to different
serovars. Secretion of IL-8 by HEp-2 cells was dependent upon bacterial
uptake. In addition, prior infection with M. avium suppressed IL-8 production by HT-29 cells infected with
Salmonella typhimurium. Our results suggest that M. avium infection of epithelial cells is associated with a delay in
IL-8 and RANTES production which, in the case of HT-29, is prolonged up
to 1 week. These findings may explain the weak inflammatory response
after intestinal mucosa invasion in mice and are probably related with
the ability of the bacterium to evade the host's immune response.
Infections caused by organisms of
the Mycobacterium avium complex are the most common
bacterial infection in patients with AIDS (11, 14). In AIDS
patients, in contrast to individuals without AIDS, where the pulmonary
infection is more frequent, the gastrointestinal (GI) tract appears to
be the primary route of M. avium infection (7, 15,
22). Colonization of the intestine is usually observed months
prior to the diagnosis of disseminated infection (7, 22,
26), and it is assumed to be a risk factor for the disseminated disease.
We have shown that M. avium is able to bind to and invade
intestinal and laryngeal epithelial cells in vitro (3, 4). In addition, when given orally to mice, M. avium enters the
intact intestinal mucosa and subsequently disseminates (2).
Epithelial cells of the intestinal mucosal surface form a major
mechanical barrier that separates the host's internal milieu from the
external environment. Mucosal surfaces have a highly specialized immune
system, and mucosal epithelial cells produce an array of cytokines and
chemokines in response to different stimuli. The existence of mucosal
cytokine response to infection was first shown to occur in mice as well
as in patients after urinary tract colonization by Escherichia
coli (10). In addition, secretion of interleukin-6
(IL-6), IL-1 In mice, infection of the intestinal mucosa by M. avium is
followed by little inflammatory response, with neutrophil infiltration of the Peyer's patches being observed approximately 1 week after infection and migration of mononuclear cells to the site of infection thereafter (17). Because the release of chemokines, such as IL-8 (a potent T-cell and neutrophil recruitment factor) has been reported in a number of inflammatory conditions of the mucosal layer,
we investigated, using two different cell lines, whether M. avium infection of epithelial cells results in the induction of
chemokine secretion.
Bacteria.
M. avium strains 101 (serovar 1), 104 (serovar 1), and 100 (serovar 8) were isolated from the blood of AIDS
patients. Mycobacterium smegmatis 11727 and Salmonella
typhimurium 15277 were purchased from The American Type Culture
Collection (ATCC), Rockville, Md. E. coli DH5
0019-9567/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Mycobacterium avium Infection of Epithelial Cells
Results in Inhibition or Delay in the Release of Interleukin-8
and RANTES
ABSTRACT
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
INTRODUCTION
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
, and IL-8 have been demonstrated in a number of studies
in vitro and in vivo after infection of mucosal epithelial cells with
E. coli (9), Helicobacter pylori (6, 13, 24), Salmonella spp. (16, 27),
and Shigella spp. (16), as well as other
microorganisms (23).
MATERIALS AND METHODS
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
was a gift
from Raul Barletta (University of Nebraska, Lincoln, Nebr.).
Cell cultures. The human intestinal epithelial cell line HT-29 was obtained from the ATCC. Cells were grown in a medium consisting of modified McCoy-5A medium (Difco) with 10% of galactose (Sigma Chemicals, St. Louis, Mo.) and 10% fetal bovine serum (Sigma). The HEp-2 laryngeal cell line was also obtained from the ATCC, and it was maintained in RPMI 1640 supplemented with 5% fetal bovine serum as described previously (4).
Cell lines were used between passages 15 and 20. HT-29 and HEp-2 cells were seeded in 24-well or 12-well tissue culture plates (Costar, Cambridge, Mass.) at 1 × 105 or 2 × 105 cells per well, respectively, in a volume of 1 ml, and then cultured to 90 to 100% confluence. HT-29 cells were also seeded on transwell membrane (3-µm pore size) and allowed to achieve confluence (ca. 1 week). The integrity of the polarized monolayers on transwell was determined by measuring the transmembrane resistance. Monolayers were used when the resistance reached approximately 400
/cm2.
Monolayers were infected with bacteria by removing the medium and
replacing it with 1 ml of medium containing 106 organisms
to each well in the 24-well tissue culture plate and transwell
monolayers or 2 × 106 in each well in the 12-well plates.
Invasion assay and intracellular growth. The invasion assay was performed as previously described (3, 4), with the modification that bacteria were allowed to invade for 1 h at 37°C instead of 2 h as originally described (4). After 1 h, cells were washed to remove unattached bacteria and incubated with 200 µg of amikacin per ml for 2 h (4). Then, cells were lysed by adding 1% Triton X-100 (Sigma), and the lysate was subsequently diluted and plated onto 7H10 agar to quantitate the viable intracellular bacteria. Results were reported as a percentage of the initial inoculum that entered both HT-29 and HEp-2 cells. The viability of the infected monolayers versus uninfected control was monitored during the experiments by trypan blue exclusion and did not show any differential cytotoxic effect related to the presence of the bacteria.
Infected transwell monolayers were maintained for up to 1 week, and the integrity of the monolayer was verified daily by measuring the resistance between both membranes.Coinfection experiments. To determine whether M. avium infection of HT-29 cells would suppress IL-8 production by the cells after uptake of S. typhimurium, we infected a 100% confluent HT-29 cell monolayer with 107 or 108 M. avium 101 for 1 h; this was then washed and treated with amikacin for 2 h as described above. After 18 h the monolayers were infected with S. typhimurium (105 cells) for 2 h and then treated with gentamicin (20 µg/ml) for 1 h. Monolayers were then washed, and 24 h later the supernatants were obtained to measure IL-8 concentration. Controls of cells without infection, infected with M. avium or Salmonella were run in parallel.
To determine whether M. avium and Salmonella were coinfecting the same cells, we performed similar assays in LabTek chamber slides as reported (1, 4). After M. avium and/or Salmonella infection and treatment with antibiotics, the monolayers were fixed with 2% paraformaldehyde for 30 min at room temperature. After being washed with Hank's balanced salt solution (HBSS), monolayers were incubated with Triton X-100 (Sigma) for 10 min and then washed three more times with HBSS. Rabbit anti-M. avium antibody (1:40) and fluorescein isothiocyanate (FITC)-labelled anti-rabbit antibody (1:400), as well as mouse anti-S. typhimurium (1:30) antibody and Texas Red anti-mouse antibody (1:800), were used to identify the bacteria. After a washing, the slides were mounted and observed by using a light microscope (Nikkon). Intracellular bacteria in 100 cells per field in 10 fields were numbered by using a source of UV light and specific filters for FITC and Texas Red.Assays for chemokine release.
Monolayers were infected with
bacteria or incubated with lipopolysaccharide (LPS). Infection was
allowed to occur for 1 h at 37°C, and then the wells were washed
with HBSS to remove noninternalized bacteria. Fresh medium was then
added, and at 4, 24, 48, and 72 h after infection, supernatants
were obtained, filtered through a 0.22-pore-size-µm filter to remove
residual bacteria and cell debris, and frozen at 
20°C.
, IL-1,
transforming growth factor (TGF-), and IL-6 were measured in the
supernatant by enzyme-linked immunosorbent assay (ELISA) by using kits
purchased from R & D Systems, Minneapolis, Minn., and BioSource,
Camarillo, Calif. The assays were carried out according to directions
provided by the manufacturers.
RNA preparation and RT-PCR analysis. To determine the relative level of IL-8 mRNA transcription, total RNA was obtained with the RNeasy Mini Kit (QIAGEN, Santa Clarita, CA), following the supplier's instructions, from 12-well infected monolayers. It was then retrotranscribed with the Ready-To-Go T-Primed First-Strand Kit (Pharmacia, Piscataway, NJ), and quantitated by reverse transcriptase PCR (RT-PCR) with previously described primers (ATG ACT TCC AAG CTG GCC GTG GCT and TCT CAG CCC TCT TCA AAA ACT TCT C) for IL-8 and GADPH (glyceraldehyde-3-phosphate dehydrogenase) as a control (TGA AGG TCG GAG TCA ACG GAT TTG CT and CAT GTG GGC CAT GAG GTC CAC CAC) (16).
The samples were heated at 94°C for 4 min and then subjected to 30 cycles of denaturation at 94°C for 45 s, annealing at 60°C for 30 s, and extension at 72°C for 45 s in a GeneAmp PCR System 2400 (Perkin-Elmer, Foster City, Calif.). Then, 10 µl of the PCR products was separated on 1.5% agarose gels and visualized by staining with ethidium bromide.Statistical analysis. Each experiment was repeated at least three times, and the results were expressed as the mean ± the standard deviation. The significance of the differences between experimental groups was analyzed by the Student's t test. A P value of <0.05 was considered significant.
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RESULTS |
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Chemokine and cytokine production by uninfected cells.
HT-29
intestinal cells do not produce IL-1, IL-1, IL-6, or RANTES
constitutively. However, IL-8 and TGF- (ca. 800 and 700 pg,
respectively) were observed in uninfected HT-29, confirming results
shown by Eckmann and colleagues (8). Uninfected HEp-2 produced approximately 1,600 pg of IL-8 and 1,400 pg of RANTES per ml.
Chemokine and cytokine production after infection in vitro.
After infection with M. avium at a ratio of 10:1, HT-29
cells secreted IL-8 at similar levels of noninfected monolayer at 24, 48, 72, 96, and 168 h (Fig. 1). In
addition, no production of other inflammatory cytokines (IL-1,
IL-1, and IL-6) was observed (data not shown). In contrast, HT-29
cells infected with a 10:1 ratio of S. typhimurium produced
6,400 ± 150 pg of IL-8 by 24 h.
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, a noninvasive
strain of E. coli, infection of HEp-2 cells with S. typhimurium triggered a significant release of IL-8 after
24 h.
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was 0.0018%, and that for S. typhimurium was approximately 26% of the inoculum (Table
1). Because Salmonella invades
HEp-2 cells more efficiently than M. avium, we repeated the
assay with a 100:1 ratio of M. avium and a 10:1 ratio
Salmonella per cell. After 2 h of uptake, the number of
intracellular bacteria was determined and shown to be similar. We then
measured IL-8 production by the monolayers after 24 h. As shown in
Fig. 4, Salmonella still induced significantly more IL-8 production, while M. avium
uptake did not induce IL-8 at 24 h, which can be explained by
the shorter replication time of Salmonella compared with
M. avium.
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mRNA. As shown in Fig. 5A and B, RT-PCR with total RNA extracted from HT-29 and HEp-2 cells confirmed the results shown by ELISA that M. avium does not trigger IL-8 production by epithelial cells.
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Uptake is necessary to induce IL-8 production.
Previous
studies have determined that M. avium entry into both HEp-2
and HT-29 cells was accompanied by cytoskeleton rearrangement and
incubation of epithelial cells with cytochalasin prior to the exposure
to the bacterium would block uptake (4). Cytochalasin D (5 µM, a concentration that blocks 90 ± 4% of M. avium
uptake) was then used to examine whether bacterium uptake was necessary to induce IL-8 production by HEp-2 cells. Cytochalasin was added for 30 min and then removed, and then M. avium 101 was used to infect HEp-2 monolayers (at a multiplicity of infection [MOI] of 10).
After 2 h, extracellular bacteria was removed by washing, and
amikacin (200 µg/ml) was used for an additional 2 h to kill extracellular bacteria. As shown in Fig.
6, IL-8 production after 72 h of
incubation did not occur if uptake was inhibited. Cytochalasin D,
however, when added alone or 1 h after M. avium
infection, did not have influence on chemokine production by HEp-2
cells. In addition, cytochalasin D does not block IL-8 production by HEp-2 cells stimulated with IL-1 (data not shown).
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M. avium blocks IL-8 production in response to Salmonella invasion. HT-29 monolayers were infected with either 107 or 108 (to maximize the number of infected cells) M. avium 101 and 18 h later infected with S. typhimurium (105/well) for 1 h. Preinfection with M. avium resulted in complete blockage of IL-8 release by 24 h after S. typhimurium infection (Fig. 7). To determine the percentage of cells that had the two bacteria, we stained intracellular bacteria with different colors and scored them. We found that 78 ± 4% of the cells had at least one M. avium bacillus, while 81 ± 6% of the cells had at least one Salmonella organism and that 72 ± 5% of the cells in the monolayer were coinfected with M. avium and Salmonella.
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DISCUSSION |
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Several studies have demonstrated that M. avium
infection in AIDS patients is acquired primarily through the GI tract
(7, 15, 22). When M. avium is given orally to
healthy C57BL/6 mice, the bacterium invades the intact mucosa of the
intestinal tract and secondarily causes disseminated infection
(2). Epithelial cells are the first cell type to encounter
bacteria at mucosal sites. It was proposed that epithelial cell
cytokine-chemokine production could function as an "early warning
system" of mucosal infection. In fact, a number of microorganisms
have been shown to induce cytokine-chemokine synthesis upon contact
with epithelial cells such as IL-8, MCP-1, granulocyte-macrophage
colony-stimulating factor, tumor necrosis factor alpha, IL-6, and
IL-1 (6, 8, 16, 20).
In this study we show that M. avium uptake by both HT-29 intestinal and HEp-2 laryngeal cell lines does not result in the release of chemokines for several days. We found that the ability to delay IL-8 and RANTES production was shared among the three strains of M. avium (representing the three most common serovars isolated from AIDS patients). It is interesting that previous studies by Yuanguang et al. (28) and Rhoades et al. (21) had shown that Mycobacterium tuberculosis infection of the A549 lung epithelial cell line and macrophages, respectively, trigger the release of great amounts of chemokines, including IL-8. In fact, Yuanguang et al. also showed that M. avium infection of A549 cells did not induce the synthesis of IL-8 and MCP-1. Although these authors argued that M. avium's failure to induce chemokine production was due to the inability to grow intracellularly, this is not the case with both HT-29 and HEp-2 cells, in which M. avium grows intracellularly (4). These findings suggest that the initial mechanisms of pathogenesis (i.e., contact with the epithelial layer) differ significantly between M. avium and M. tuberculosis. It is certainly plausible to hypothesize that, because of the decreased intrinsic virulence compared with M. tuberculosis, M. avium is required to prevent immune response early in the infection to survive. M. avium infection of the intestinal mucosa ultimately causes segmental necrosis of the intestinal villi followed by the influx of inflammatory cells (17). However, this is not observed until several weeks after infection, which suggests that M. avium infection of intestinal epithelial cells is a quiet process in its beginning.
While bacteria such as Salmonella trigger chemokine production soon after entering intestinal cells (27), it has been shown that organisms such as Chlamydia sp. also delay inflammation for several hours (20). Therefore, it may be important to some bacteria to maintain the immune system of the host "in check" while the infection is being established. Several of the cytokines and chemokines are potent chemoattractants and activators for neutrophils, monocytes, and T lymphocytes (8, 25). The fact that intestinal epithelial cells can participate in the network of cytokine-chemokine response and the observation that these cells can express human lymphocyte antigen class II molecules suggests a role for them in the mucosal defense against M. avium infection. Cytokines and chemokines in the intestinal mucosa provide bidirectional communication between inflammatory cells such as tissue macrophages, monocytes, T cells, and epithelial cells. Inhibition of chemokines production appears to be secondary to active interaction of the bacterium and epithelial cells. Although M. avium infection cannot inhibit RANTES and IL-8 production after LPS stimulation (data not shown), it significantly inhibits IL-8 production after stimulation with Salmonella, suggesting that the mechanisms of chemokine stimulation is probably different for LPS and Salmonella. This also implies that M. avium infection actively blocks some step the signal transduction pathway triggered by Salmonella and does not simply remain quiet in the host cell, thus resembling the case of Yersinia, which is able to interrupt host cell pathways through the secretion of Yop proteins (19).
The findings that M. avium triggers different responses in HT-29 intestinal and HEp-2 laryngeal cells could be relevant for the pathogenesis of the infection and is currently being investigated. However, it also suggests either that the signal transduction pathways for chemokine synthesis differ between the cells or that the mechanism of M. avium invasion of HT-29 cells is probably different from the mechanism of invasion of HEp-2 cells.
It is interesting to speculate that in human immunodeficiency virus type 1 (HIV-1)-infected individuals, infection of the intestinal mucosa with HIV-1 prior to M. avium may be associated with production of chemokines (18), although HIV-1 has been shown to enter the intestinal mucosa through M cells (5), whereas M. avium invades the intestinal mucosa primarily through enterocytes (12).
Our findings offer another perspective on M. avium infection of the host, with little initial inflammatory response followed, depending on the cell infected, by the release of inflammatory cytokines (17). However, it seems important for M. avium to be able to prevent cytokines and chemokine synthesis by infected cells, potentially creating a protective shield against the host immune response.
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ACKNOWLEDGMENTS |
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We thank Karen Allen for preparing the manuscript.
This work was supported by contract N01-AI-25140 of the National Institute of Allergy and Infectious Diseases. F.J.S. was supported by a fellowship of the North Atlantic Treaty Organization.
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FOOTNOTES |
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* Corresponding author. Mailing address: Kuzell Institute, 2200 Webster St., Ste. 305, San Francisco, CA 94115. Phone: (415) 561-1734. Fax: (415) 441-8548. E-mail: luizb{at}cooper.cpmc.org.
Editor: S. H. E. Kaufmann
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Introduction
Materials and Methods
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Discussion
References
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Infection and Immunity, October 1999, p. 5069-5075, Vol. 67, No. 10
0019-9567/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
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