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1 Department of Medical Biochemistry, Graduate School of Medicine,
2 Department of Anaesthesiology and Critical Care Medicine, Faculty of Medicine, Tokyo Medical and Dental University, 1-5-45 Yushima, Bunkyo-ku, Tokyo 113-8519, Japan
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Abstract |
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, a well-known ATI marker protein, were targeted to basolateral and apical membranes, respectively, when expressed in polarized Madine Darby canine kidney cells. Moreover, RAGE was expressed in ATI cells after T1in vivo and in ex in vivo organ cultures. In conclusion, RAGE is a marker for basolateral membranes of well-differentiated ATI cells. ATI cells require some signal provided by the in vivo environment to express RAGE. |
Introduction |
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(also called OTS-8) and aquaporin-5 are well known as markers of ATI cells (Nose et al. 1990; Rishi et al. 1995; Gonzalez & Dobbs 1998; Borok et al. 1998; Funaki et al. 1998).
Receptor for advanced glycation end-products (RAGE) is a member of immunoglobulin superfamily of proteins (reviewed in Schmidt et al. 2000). RAGE is a multiligand-binding protein and binds advanced glycation end-products, amyloid ß fibrils, amphoterin, and members of S100/calgranulin family, and is implicated in the pathogenesis of diabetic vascular diseases and Alzheimer's diseases, Cdc42/Rac activation, neurite outgrowth and inflammation. The transcript of RAGE is the most prominent in lung. The study using the in situ hybridization reveals that RAGE mRNA is expressed in ATII cells in lung (Katsuoka et al. 1997). Inconsistent with this, RAGE is detected at the basal face of ATI cells in the immunohistochemistry and the immunoelectron microscopy (Fehrenbach et al. 1998). If RAGE is a marker protein of basolateral membranes of ATI cells, it should be useful for the analysis of differentiation of ATI cells, because both of T1 and aquaporin-5 are localized on apical membranes. In this study, we determined whether the expression of RAGE was parallel to the differentiation of ATI cells and whether RAGE was targeted to the basolateral side of epithelial cells. Moreover, we attempted to differentiate the columnar epithelial cells from rat embryo lung to express RAGE in vitro.
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Results |
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We raised rabbit polyclonal antibodies against recombinant proteins of RAGE and T1, respectively. The anti-RAGE antibody recognized one major protein with 68 kDa and two minor proteins with 61 and 53 kDa in lung (Fig. 1Aa). The major protein had almost the same size as FLAG-RAGE expressed in COS-7 cells. The anti-T1 antibody recognized a single protein with 42 kDa in lung (Fig. 1Ab). Interestingly, the antibody recognized three proteins in COS-7 cells transfected with pFLAG T1. The size of the top fuzzy band was similar to that of the signal recognized in lung. We consider that other two bands may be products of protein degradation or with different post-translation modification. We detected ATII cells by the in situ hybridization for surfactant protein-C (SP-C) and simultaneously immunostained cells by anti-RAGE or anti-T1 antibody (Fig. 1B,C). Both of anti-RAGE and anti-T1 antibodies revealed the signals lining alveoli in lung (Fig. 1Ba,Ca). The cells which were positive for mRNA of SP-C did not express either RAGE or T1 (insets in Fig. 1B,C). In the immunoelectron microscopy, RAGE immunoreactivity decorated basal membranes of ATI cells, while T1 immunoreactivity decorated apical membranes of ATI cells (Fig. 2).
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We next examined whether the localization of RAGE in ATI cells reflects the basolateral targeting of the protein in polarized epithelial cells. For this purpose, we generated stable transformants of MDCK cells expressing FLAG-tagged RAGE and T1. FLAG-RAGE was detected along lateral membranes of MDCK cells and overlapped with ERBIN (Fig. 3Aa). FLAG-T1 was localized on apical membranes (Fig. 3Ab). For the further confirmation, we cultured MDCK cells on Transwell dishes and biotinylated surface proteins from either the apical or the basolateral side. Biotinylated proteins were precipitated by avidin beads and immunoblotted with anti-FLAG antibody. FLAG-RAGE and FLAG-T1 were biotinylated from basolateral and apical sides, respectively (Fig. 3B). We have concluded that RAGE is a marker protein of basolateral membranes of ATI cells.
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in lung development and in primary cultures
We examined the expression of RAGE and T1 in lung development. In Western blottings of rat lung, RAGE started to be detected on embryonal day 20.5 and increased gradually even after birth (Fig. 4Aa). In contrast, T1 was already detected on embryonal day 16.5 (Fig. 4Ab). The amount of T1 reached to the plateau around postnatal day 0. To compare the sensitivities of anti-RAGE and anti-T1 antibody, we expressed FLAG-RAGE and FLAG-T1 in COS-7 cells and prepared the standard samples. We immunoblotted the samples by anti-FLAG antibody and either anti-RAGE or anti-T1 antibody (Fig. 4B). Anti-FLAG antibody barely recognized FLAG-RAGE in the first sample (Fig. 4Ba1, lane 1). However, anti-RAGE antibody detected a signal in the same sample (Fig. 4Ba2, lane 1). This result suggests that anti-RAGE antibody is more sensitive than anti-FLAG antibody. Conversely, the immunoblottings of the standard samples for T1 indicate that the sensitivity of anti-T1 antibody is almost the same or slightly lower than that of anti-FLAG antibody (Fig. 4Bb). Taken together, we conclude that anti-T1 antibody is less sensitive than anti-RAGE antibody and that lung expresses more T1 than RAGE, for instance, on embryonal day 16.5. Moreover, the temporal profiles of expression of each protein also suggest that the expression of T1 precedes that of RAGE. In the immunohistochemistry, RAGE immunoreactivity was lining alveoli on embryonal day 21.5 and postnatal day 0 (Fig. 5A). We did not detect significant signals of RAGE on embryonal day 16.5 and day 18.5. The immunostaining using anti-T1 antibody also revealed linear patterns on embryonal day 21.5 and postnatal day 0 (Fig. 5B). T1 was already expressed in epithelial cells, which still had columnar morphology, on embryonal day 18.5. At this stage, the T1-positive cells were already negative for SP-C (Fig. 5C). We will discuss this observation in Discussion. In the next set of experiments, we cultured ATII cells from adult rat lung and induced the differentiation into ATI-like cells. Consistent with the observation in vivo, RAGE still increased on day 6 in primary cultured cells, while T1 was expressed at the almost maximum level (Fig. 6). In lung development, 68-kDa protein was always predominant among proteins detected by anti-RAGE antibody (Fig. 4A). However, in the cultures of ATII cells, 68 kDa-protein was not the most abundant first, although it became enriched later. The reason for the different expression patterns of RAGE is unclear.
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The data above suggest that RAGE is a maker for well-differentiated ATI cells. We next isolated the columnar epithelial cells from rat embryos on day 18.5 and cultured them in vitro to examine whether these cells could differentiate and express RAGE. Because RAGE is detected on embryonal day 21.5 in vivo, the cells should express RAGE after 3 day cultures. Unexpectedly, we could detect T1 but not RAGE even after 7 day cultures (Fig. 7A and data not shown). We considered the possibility that the formation of lumen might be necessary for the differentiation of ATI cells, and cultured the columnar epithelial cells in matrigels. The cells formed cysts after 1 day. Then, FGF-7 was added to the cultures. Cysts became larger (Fig. 7Ba). On day 7, cells were dissociated from the cysts, plated on cover glasses, and immunostained (Fig. 7Bb). Some cells expressed T1 and others not (arrows and arrow heads). Even so, we could not detect RAGE in any cells (data not shown). Moreover, we prepared lung buds from rat embryos on day 14.5 and cultured them in vitro for 8 days (Fig. 8A). Lung buds expressed T1 but not RAGE (Fig. 8B and data not shown). When we implanted lung buds under the renal capsule in nude mice, they expressed RAGE (Fig. 8C). All these data indicate that ATI cells need some factor provided by the in vivo environment to become well differentiated and express RAGE.
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Discussion |
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The knowledge about the differentiation of ATI cells is currently limited and debatable. Thereby, we set a goal to establish a new method to obtain differentiated ATI cells. Alveolar epithelial cells appear from columnar epithelial cells on canalicular stage around embryonal day 18.5–20 in rat. Thereby, if we differentiate ATI cells from columnar epithelial cells, such cells may be close to physiological ATI cells. To assess whether we obtain ATI cells, we first need markers for ATI cells. T1 is a well-characterized marker for ATI cells. However, embryonic lung epithelium cells widely express T1 (Rishi et al. 1995). A very recent paper using mutant mice uncovered that T1 is essential for the differentiation of ATI cells, suggesting that T1 plays roles before ATI cells are differentiated (Ramirez et al. 2003). Thereby, T1 is a good marker for ATI cells in adult lung, but is not specific for ATI cells during lung development. We need a different marker, which is expressed only in differentiated ATI cells. Aquaporin-5 is also a well-known marker for ATI cells. Its expression increases in accordance with the transition from ATII cells to ATI-like cells in vitro (Borok et al. 1998). However, the expression is not restricted to ATI cells (Krane et al. 2001). HTI56 is an integral membrane protein, which is characterized as a specific marker for human ATI cells, but its molecular identity is still undetermined (Dobbs et al. 1999).
RAGE is a multiligand protein that belongs to the immunoglobulin superfamily. Lung highly expresses RAGE, although the physiological significance of RAGE in lung is currently unknown. The previous immunohistochemical study revealed that RAGE is detected on basal membranes of ATI cells (Fehrenbach et al. 1998). We first tested whether RAGE is expressed only in ATI cells in rat adult lung, because there is a report that mRNA of RAGE is detected selectively in ATII cells (Katsuoka et al. 1997). Our results demonstrated that RAGE is detected only on basal membranes of ATI cells. We performed the in situ hybridization for RAGE, but we could not obtain clear signals (data not shown). Thereby, we could not conclude whether ATII cells have mRNA of RAGE and ATI cells do not, but the protein expression rather suggests that ATI cells have mRNA of RAGE. We next showed that RAGE is targeted to basolateral membranes in polarized epithelial cells in immunofluorescence and biochemical studies. Together with the immunoelectron microscopy, RAGE is considered as a maker for basal membranes of ATI cells.
In immunohistochemistry, RAGE was detected in rat lung after embryonal day 21.5 unlike T1 that was expressed even on embryonal day 16.5. RAGE was also detected after T1 in primary cultures of ATII cells from adult rat lung. The temporal profile supports that the expression of RAGE increases after that of T1 reaches the maximum. Moreover, we calibrated the sensitivities of antibodies and confirmed that the anti-RAGE antibody is more sensitive than the anti-T1 antibody. Thereby, even if we take into consideration the difference between sensitivities of antibodies, we can conclude that RAGE is expressed in more differentiated ATI cells.
The expression pattern of T1 is widespread during lung development (Williams et al. 1996). Consistent with this, we detected T1 in the columnar epithelial cells on embryonal day 16.5. SP-C mRNA was not detected in T1-positive cells, although lungs are still at the pseudoglandular stage, in which epithelial tubes grow into the mesenchyme. This finding implies several scenarios. T1-positive cells may differentiate into SP-C-positive cells at the latter stage and cease to express T1. Subsequently, SP-C-positive cells may further differentiate into ATI cells and express T1 again. The second story is that some of T1-positive cells stop to express T1 and start to express SP-C, but others continue to express T1 and are committed to ATI cells. It may be also possible that SP-C-positive cells are derived from distinct cells from T1-positive cells that may become ATI cells. To test these possibilities, the in vitro system, in which the columnar epithelial cells differentiate into ATI cells, is indispensable.
Using RAGE as a marker, we attempted to establish a method to differentiate columnar epithelial cells into ATI cells. If the columnar epithelial cells retain original properties, they should differentiate into ATI cells in vitro. In betrayal of this expectation, the columnar epithelial cells expressed T1, but not RAGE in vitro. Fibroblasts are known to produce differentiation factors during the canalicular stage (Caniggia et al. 1991). We cocultured the columnar epithelial cells with lung fibroblasts, and also tested the conditional medium from fibroblast cultures. These trials were unsuccessful (data not shown). We also formed cysts from the columnar epithelial cells in matrigels, but the cells did not express RAGE. Lung organ did not express RAGE in vitro, suggesting that some factor outside lung is necessary for the expression of RAGE. Indeed, lung organ expressed RAGE, when it was implanted back underneath the renal capsule. It is necessary to identify such factors to understand the molecular mechanism underlying the differentiation of ATI cells.
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Experimental procedures |
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Various expression vectors were constructed by conventional molecular biology techniques and PCR method. Human RAGE and rat T1 cDNAs were obtained by PCR using human lung and rat lung cDNAs. The following constructs contain the following amino acids; pGex RAGE-2, 27-335 of human RAGE; pLN FLAG RAGE, 23-404; pGex T1-1, 1-166; and pLN FLAG T1, 23-166.
Antibodies and other reagents
Rabbit antibodies were raised against GST-RAGE-2 and GST-T1. The antigens were coupled to HiTrap NHS-activated Sepharose HP (Amersham Pharmacia Biotech) according to the manufacturer's protocol and the antibodies were affinity-purified as previously described (Harlow & Lane 1988). The rabbit anti-ERBIN was described (Ohno et al. 2002). Mouse monoclonal anti-FLAG (M1 and M2) antibody (Sigma-Aldrich), rat monoclonal anti-ZO-1 antibody (Chemicon), Hoechst 33342 (Sigma-Aldrich), recombinant human FGF-7 (Genzyme), collagenase (Worthington), dispase I (Roche Diagnostics Corporation), DNase (Roche Diagnostics Corporation), trypsin (Invitrogen), and G418 (Sigma-Aldrich) were obtained from commercial sources.
Immunohistochemistry
All procedures related to the care and treatment of animals were in accordance with the institutional and National Institutes of Health guidelines. Rat lungs at various developmental stages were fixed in PBS containing 4% (w/v) paraformaldehyde for 6–18 h depending on the size, and immersed with 10, 20 and 30% (w/v) sucrose in PBS, sequentially. Lungs from rats after birth were exposed to negative pressure in PBS to be inflated. Tissue blocks were embedded in Tissue-Tek® O.C.T. compound (Sakura Finetechnical Co., Tokyo, Japan). Sections of 4–6 µm were cut and mounted on aminopropyltriethoxysilane-coated glass slides (Matsunami Glass, Osaka, Japan), and were dried with a stream of cold air. The sections were blocked with PBS containing 5% goat serum and 0.2% (w/v) Triton-X 100 for 1 h at room temperature. They were then incubated with the primary antibody at 4 °C overnight, and visualized with appropriate secondary antibodies. For the immunohistochemistry of in vitro cultured organs and lung transplants, the samples were fixed in 4% (w/v) paraformaldehyde in PBS overnight, were immersed in a graded series of sucrose, and embedded in Tissue-Tek® O.C.T. compound. Sections of 4–6 µm were cut and mounted on MAS-coated glass slides (Matsunami Glass, Osaka, Japan).
Immunoelectron microscopy
Rat lungs were fixed by perfusion and transtracheal infusion of PBS containing 2% (w/v) paraformaldehyde and 0.1% (w/v) glutaraldehyde. Tissues were cut in small pieces and fixed in the same fixative for 3 h on ice, washed with PBS, and dehydrated with a graded series of ethanol. Then, small cubes of lung were embedded in LR white (London resin company, London) and polymerized. Ultrathin sections were transferred to 300-mesh nickel grids and treated with 3% (v/v) H2O2 for 10 min. After blocking with 1% (w/v) BSA in PBS for 30 min, grids were incubated with the affinity-purified rabbit anti-RAGE or anti-T1 antibody and after washed, with 10 nm gold-conjugated goat anti-rabbit IgG (Amersham Pharmacia Biotech) diluted at 1 : 20 for 1 h at room temperature. After rinsed with distilled water, grids were counterstained with 3% uranyl acetate for 20 min. Images were obtained with a Hitachi 7100 electron microscope.
Primary cultures of ATII cells
Primay cultures of ATII cells were performed as previously described (Rannels & Rannels 1994). Briefly, rat lungs were perfused via the pulmonary artery with 0.15 M NaCl, dissected with a heart en bloc, and lavaged. Lungs were treated by intratracheal instillation with porcine pancreas elastase at 37 °C for 30 min, and subsequently with trypsin inhibitor, DNase, and calf serum. Each lobe was separated, minced into small pieces, and filtrated with a nylon mesh. After treated with DNase again, filtrated cells were charged on to a discontinuous Percoll gradient (1.04–1.08 g/mL), and centrifuged at 400 g for 20 min. Cells of the second layer were collected, placed in a tissue culture flask, and incubated at 37 °C for 30–90 min to remove the attached cells. The attached cells were cultured as lung fibroblasts. The unattached cells were plated on tissue-culture grade plastic dishes at a density of 1 x 105 cells/cm2 and cultured in DMEM containing 10% FBS, 100 U/mL of penicillin G, 100 µg/mL of streptomycin, 2.5 µg/mL of amphotericin B, and 50 µg/mL of gentamicin sulphate at 37 °C in a humidified incubator under 5% (v/v) CO2.
Primary cultures of foetal lung epithelial cells
Primary cultures of foetal lung epithelial cells were performed as described (Caniggia et al. 1991; Zimmermann et al. 1994). Foetuses were removed from time-pregnant Wistar rats, gestational age 18.5 day. 8–12 foetal lungs were dissected out, placed in cold Hank's solution without calcium or magnesium (HBSS), cleared of large airways and vessels, and minced. The lungs were washed with HBSS and kept on ice. The supernatant containing red blood cells were removed. This procedure was repeated until the supernatant became clear. Then, lungs were centrifuged at 420 g for 5 min at 4 °C, and incubated in 30 mL of MEM containing 0.125% trypsin and 0.4 mg/mL DNase for 30 min at 37 °C. 30 mL of MEM containing 10% FBS, 50 µg/mL gentamycin, and 0.625 µg/mL amphotericin B (complete MEM) was added to stop trypsinization and the cell suspension was filtered through 100-µm nylon mesh. The filtered cells were pelleted by centrifugation at 420 g for 5 min at 4 °C. The pellet was resuspended in 30 mL of MEM containing 0.1% collagenase. After incubation for 15 min at 37 °C, 20 mL of complete MEM was added and centrifuged at 420 g for 5 min at 4 °C. The pellet was resuspended in 10 mL of complete MEM and transferred to one 75 cm2 tissue culture flask. After 45 min incubation at 37 °C in 5% CO2, the medium was collected and transferred to a new 75 cm2 tissue culture flask. After another 45 min incubation at 37 °C in 5% CO2, the nonadherent cells were collected and cultured in complete MEM.
In situ hybridization
cDNA of mouse SP-C in pBluescript SK(–) was used for the in situ hybridization of rat lung as described (Hashimoto et al. 2000). The plasmid was linearized by appropriate restriction enzymes to achieve transcription of sense and anti-sense templates (EcoRI for sense strand probe, Hindlll for anti-sense strand probe). Digoxigenin (DIG)-labelled cRNA probes were prepared using DIG RNA labelling kit (Roche Diagnostics Corporation) according to the manufacturer's instructions by T7 (for sense strand probe) and T3 (for anti-sense strand probe) RNA polymerases. Tissue sections of lung were prepared as described above for the immunohistochemistry, except that DEPC-treated PBS was used. Sections of 4–6 µm were fixed with 4% (w/v) paraformaldehyde in PBS, washed with PBS, treated with proteinase K (10 µg/mL) for 5–15 min at room temperature, fixed with 4% (w/v) paraformaldehyde in PBS, washed with PBS, treated with 0.1 mM triethanolamine/HCl (TEA) pH 8.0, acetylated with 0.25% acetic acid in 0.1 mM TEA, pH 8.0. Sections were prehybridized with prewarmed hybridization buffer (0.5 mg/mL tRNA, 4 x SSC, 1 x Denhardt's solution, 100 µg/mL Heparin, 5 mM x EDTA, 50% formamide) at 43 °C for 1 h. DIG-labelled cRNA probes were hybridized to sections at 200 ng/mL 43 °C overnight in moisture chamber. Sections were rinsed twice in 5 x SSC, and washed with 50% formamide in 2 x SSC at 50 °C for 30 min, washed with 2 x SSC, treated with RNase A (20 µg/mL) at 37 °C for 30 min, and subsequently washed twice with 2 x SSC and 0.1 x SSC at 50 °C for 15 min. The signal was detected using DIG Nucleic Acid Detection kit (Roche Diagnostics Corporation) according to the manufacturer's instructions. Finally, sections were washed with distilled water, fixed with 4% (w/v) paraformaldehyde in PBS, and used for the immunohistochemistry.
Lung organ cultures and allograft lung transplantation
Lung organ cultures and transplantation were performed as described (Vu et al. 2003). Embryonal day 14.5-lungs were dissected from pregnant Wistar rats, washed with ice cold PBS, and cultured on top of polyethylene terephthalate track-etched membranes of 6.4 mm diameter and 8 µm pore size (Beckton Dickinson Labware). The membrane was floated in BGJb medium containing 10% FBS, 100 U/mL penicillin, and 100 µg/mL streptomycin at 37 °C in a humidified incubator in 5% CO2 atmosphere. For lung transplantation, adult nude mice (BALB/c-nu) were anaesthetized, and the kidney was exposed through a dorsal incision. Renal membranous capsule was incised and detached. Two lungs were placed underneath the capsule per each kidney. The kidney was placed back, and the muscle layer and the skin were closed with nylon sutures.
Stable transformants of MDCK cells and immunocytochemistry
Stable transformants of MDCK cells expressing FLAG-RAGE and FLAG-T1 were prepared as described (Nishimura et al. 2000). Briefly, phoenix ampho cells were transfected with pLN FLAG-RAGE or pLN FLAG-T1 using calcium phosphate precipitation method to generate retrovirus. MDCK cells were infected with the virus and were selected by 1 mg/ml of G418. Immunocytochemistry was performed as previously described (Nishimura et al. 2000).
Surface biotinylation
Cells were cultured to confluency on 24 mm Transwell plates (Corning Inc.), and rinsed with the cold PBS-CM (PBS containing 0.1 mM CaCl2 and 1 mM MgCl2). All procedures for biotinylation were performed at 4 °C. 0.5 mg/mL of sulpho-NHS-SS- biotin (Pierce Chemical Co.) in PBS-CM was added to an upper or a lower chamber. PBS-CM was added to the other chamber. The cells were incubated for 30 min on a shaker. The reaction was stopped by removing the solution and adding 50 mM NH4Cl in PBS-CM. Cells were washed with the cold PBS-CM, collected, and lysed with the lysis buffer (20 mM Tris/HCl at pH 8.0 containing 100 mM NaCl, 1% (w/v) Triton X-100). The lysates were centrifuged at 10 000 g for 15 min and the supernatants were incubated with avidin beads at 4 °C overnight. The proteins attached to beads were analysed with Western blotting.
Other procedures
To prepare the homogenates, COS-7 cells were collected and sonicated in the lysis buffer. Rat lungs were homogenized using a polytron (Kinematica AG) in the lysis buffer. Western blotting was performed using the enhanced chemiluminescence reagent (Amersham Pharmacia Biotech).
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Acknowledgements |
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This study was supported by grants-in-aids for Scientific Research and on Priority Areas, and Special Coordination Funds for Promoting Science and Technology from the Ministry of Education, Culture, Sports, Science, and Technology of Japan.
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Footnotes |
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* Correspondence: E-mail: yuhammch{at}med.tmd.ac.jp
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References |
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Received: 3 November 2003
Accepted: 8 December 2003
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 C S Calfee, L B Ware, M D Eisner, P E Parsons, B T Thompson, N Wickersham, M A Matthay, and the NHLBI ARDS Network Plasma receptor for advanced glycation end products and clinical outcomes in acute lung injury Thorax, December 1, 2008; 63(12): 1083 - 1089. [Abstract] [Full Text] [PDF]
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 S. J. Kemp, A. J. Thorley, J. Gorelik, M. J. Seckl, M. J. O'Hare, A. Arcaro, Y. Korchev, P. Goldstraw, and T. D. Tetley Immortalization of Human Alveolar Epithelial Cells to Investigate Nanoparticle Uptake Am. J. Respir. Cell Mol. Biol., November 1, 2008; 39(5): 591 - 597. [Abstract] [Full Text] [PDF]
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 E. L. Brincks, A. Katewa, T. A. Kucaba, T. S. Griffith, and K. L. Legge CD8 T Cells Utilize TRAIL to Control Influenza Virus Infection J. Immunol., October 1, 2008; 181(7): 4918 - 4925. [Abstract] [Full Text] [PDF]
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S. Hashimoto, F. Amaya, H. Matsuyama, H. Ueno, S. Kikuchi, M. Tanaka, Y. Watanabe, M. Ebina, A. Ishizaka, S. Tsukita, et al. Dysregulation of lung injury and repair in moesin-deficient mice treated with intratracheal bleomycin Am J Physiol Lung Cell Mol Physiol, October 1, 2008; 295(4): L566 - L574. [Abstract] [Full Text] [PDF]
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 J. M. Englert, L. E. Hanford, N. Kaminski, J. M. Tobolewski, R. J. Tan, C. L. Fattman, L. Ramsgaard, T. J. Richards, I. Loutaev, P. P. Nawroth, et al. A Role for the Receptor for Advanced Glycation End Products in Idiopathic Pulmonary Fibrosis Am. J. Pathol., March 1, 2008; 172(3): 583 - 591. [Abstract] [Full Text] [PDF]
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M. He, H. Kubo, K. Ishizawa, A. E. Hegab, Y. Yamamoto, H. Yamamoto, and M. Yamaya The role of the receptor for advanced glycation end-products in lung fibrosis Am J Physiol Lung Cell Mol Physiol, December 1, 2007; 293(6): L1427 - L1436. [Abstract] [Full Text] [PDF]
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J. Wang, K. Edeen, R. Manzer, Y. Chang, S. Wang, X. Chen, C.J. Funk, G. P. Cosgrove, X. Fang, and R. J. Mason Differentiated Human Alveolar Epithelial Cells and Reversibility of their Phenotype In Vitro Am. J. Respir. Cell Mol. Biol., June 1, 2007; 36(6): 661 - 668. [Abstract] [Full Text] [PDF]
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 S. Kobayashi, H. Kubo, T. Suzuki, K. Ishizawa, M. Yamada, M. He, Y. Yamamoto, H. Yamamoto, H. Sasano, H. Sasaki, et al. Endogenous Secretory Receptor for Advanced Glycation End Products in Non-Small Cell Lung Carcinoma Am. J. Respir. Crit. Care Med., January 15, 2007; 175(2): 184 - 189. [Abstract] [Full Text] [PDF]
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 P. J. DeBiase, K. Lane, S. Budinger, K. Ridge, M. Wilson, and J. C.R. Jones Laminin-311 (Laminin-6) Fiber Assembly by Type I-like Alveolar Cells J. Histochem. Cytochem., June 1, 2006; 54(6): 665 - 672. [Abstract] [Full Text] [PDF]
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T. Uchida, M. Shirasawa, L. B. Ware, K. Kojima, Y. Hata, K. Makita, G. Mednick, Z. A. Matthay, and M. A. Matthay Receptor for Advanced Glycation End-Products Is a Marker of Type I Cell Injury in Acute Lung Injury Am. J. Respir. Crit. Care Med., May 1, 2006; 173(9): 1008 - 1015. [Abstract] [Full Text] [PDF]
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 J. Chen, Z. Chen, N. R. Chintagari, M. Bhaskaran, N. Jin, T. Narasaraju, and L. Liu Alveolar type I cells protect rat lung epithelium from oxidative injury J. Physiol., May 1, 2006; 572(3): 625 - 638. [Abstract] [Full Text] [PDF]
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B. Bartling, N. Demling, R.-E. Silber, and A. Simm Proliferative Stimulus of Lung Fibroblasts on Lung Cancer Cells Is Impaired by the Receptor for Advanced Glycation End-Products Am. J. Respir. Cell Mol. Biol., January 1, 2006; 34(1): 83 - 91. [Abstract] [Full Text] [PDF]
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 B. Bartling, H.-S. Hofmann, B. Weigle, R.-E. Silber, and A. Simm Down-regulation of the receptor for advanced glycation end-products (RAGE) supports non-small cell lung carcinoma Carcinogenesis, February 1, 2005; 26(2): 293 - 301. [Abstract] [Full Text] [PDF]
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 M.C. McElroy and M. Kasper The use of alveolar epithelial type I cell-selective markers to investigate lung injury and repair Eur. Respir. J., October 1, 2004; 24(4): 664 - 673. [Abstract] [Full Text] [PDF]
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