Critical Transition in Tissue Homeostasis Accompanies Murine Lung Senescence
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{"title"=>"Critical transition in tissue homeostasis accompanies murine lung senescence", "type"=>"journal", "authors"=>[{"first_name"=>"Carla L.", "last_name"=>"Calvi", "scopus_author_id"=>"36894823100"}, {"first_name"=>"Megan", "last_name"=>"Podowski", "scopus_author_id"=>"9639245900"}, {"first_name"=>"Franco R.", "last_name"=>"D'Alessio", "scopus_author_id"=>"12792796100"}, {"first_name"=>"Shana L.", "last_name"=>"Metzger", "scopus_author_id"=>"54410870600"}, {"first_name"=>"Kaori", "last_name"=>"Misono", "scopus_author_id"=>"54411121800"}, {"first_name"=>"Hataya", "last_name"=>"Poonyagariyagorn", "scopus_author_id"=>"7801450945"}, {"first_name"=>"Armando", "last_name"=>"Lopez-Mercado", "scopus_author_id"=>"54411019100"}, {"first_name"=>"Therese", "last_name"=>"Ku", "scopus_author_id"=>"54410844900"}, {"first_name"=>"Thomas", "last_name"=>"Lauer", "scopus_author_id"=>"56437935500"}, {"first_name"=>"Christopher", "last_name"=>"Cheadle", "scopus_author_id"=>"6603422519"}, {"first_name"=>"C. Conover", "last_name"=>"Talbot", "scopus_author_id"=>"7102656875"}, {"first_name"=>"Chunfa", "last_name"=>"Jie", "scopus_author_id"=>"7006488232"}, {"first_name"=>"Sharon", "last_name"=>"McGrath-Morrow", "scopus_author_id"=>"6603231818"}, {"first_name"=>"Landon S.", "last_name"=>"King", "scopus_author_id"=>"7403028552"}, {"first_name"=>"Jeremy", "last_name"=>"Walston", "scopus_author_id"=>"7003712269"}, {"first_name"=>"Enid R.", "last_name"=>"Neptune", "scopus_author_id"=>"6603348087"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "sgr"=>"79959368002", "pui"=>"361981250", "scopus"=>"2-s2.0-79959368002", "issn"=>"19326203", "pmid"=>"21713037", "doi"=>"10.1371/journal.pone.0020712"}, "id"=>"559cf55f-e54a-3a61-af38-88a59f4d802a", "abstract"=>"BACKGROUND: Respiratory dysfunction is a major contributor to morbidity and mortality in aged populations. The susceptibility to pulmonary insults is attributed to \"low pulmonary reserve\", ostensibly reflecting a combination of age-related musculoskeletal, immunologic and intrinsic pulmonary dysfunction.\\n\\nMETHODS/PRINCIPAL FINDINGS: Using a murine model of the aging lung, senescent DBA/2 mice, we correlated a longitudinal survey of airspace size and injury measures with a transcriptome from the aging lung at 2, 4, 8, 12, 16 and 20 months of age. Morphometric analysis demonstrated a nonlinear pattern of airspace caliber enlargement with a critical transition occurring between 8 and 12 months of age marked by an initial increase in oxidative stress, cell death and elastase activation which is soon followed by inflammatory cell infiltration, immune complex deposition and the onset of airspace enlargement. The temporally correlative transcriptome showed exuberant induction of immunoglobulin genes coincident with airspace enlargement. Immunohistochemistry, ELISA analysis and flow cytometry demonstrated increased immunoglobulin deposition in the lung associated with a contemporaneous increase in activated B-cells expressing high levels of TLR4 (toll receptor 4) and CD86 and macrophages during midlife. These midlife changes culminate in progressive airspace enlargement during late life stages.\\n\\nCONCLUSION/SIGNIFICANCE: Our findings establish that a tissue-specific aging program is evident during a presenescent interval which involves early oxidative stress, cell death and elastase activation, followed by B lymphocyte and macrophage expansion/activation. This sequence heralds the progression to overt airspace enlargement in the aged lung. These signature events, during middle age, indicate that early stages of the aging immune system may have important correlates in the maintenance of tissue morphology. We further show that time-course analyses of aging models, when informed by structural surveys, can reveal nonintuitive signatures of organ-specific aging pathology.", "link"=>"http://www.mendeley.com/research/critical-transition-tissue-homeostasis-accompanies-murine-lung-senescence", "reader_count"=>17, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Researcher"=>6, "Student > Ph. D. Student"=>4, "Student > Postgraduate"=>1, "Other"=>1, "Student > Master"=>3}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Researcher"=>6, "Student > Ph. D. Student"=>4, "Student > Postgraduate"=>1, "Other"=>1, "Student > Master"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>2, "Agricultural and Biological Sciences"=>7, "Medicine and Dentistry"=>4, "Business, Management and Accounting"=>1, "Chemistry"=>1, "Social Sciences"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>4}, "Chemistry"=>{"Chemistry"=>1}, "Social Sciences"=>{"Social Sciences"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>7}, "Business, Management and Accounting"=>{"Business, Management and Accounting"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Unspecified"=>{"Unspecified"=>1}}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/763353"], "description"=>"<p>A. Representative immunohistochemical staining for nitrotyrosine in mice at 2 months, 8 months, 12 months and 20 months of age. Robust staining is evident by 8 months of age. Site of staining is in alveolar epithelial cells (arrowheads). N = 4–6 mice per group. Original magnification, 20×. B. Quantitative immunohistochemistry of nitrotyrosine staining shows enhanced staining in the 8 month old lung which progresses through later time points. N = 6 mice per group. C. Quantitative immunohistochemistry of TUNEL staining of lungs from aging mice shows increased cell death at 8 months of age which persists through later time points. N = 6 mice per group. Reported data are mean values +/− SEM from at least five mice for each group. *p<0.05, **p<0.01.</p>", "links"=>[], "tags"=>["oxidative", "murine"], "article_id"=>433708, "categories"=>["Physiology", "Immunology"], "users"=>["Carla L. Calvi", "Megan Podowski", "Franco R. D'Alessio", "Shana L. Metzger", "Kaori Misono", "Hataya Poonyagariyagorn", "Armando Lopez-Mercado", "Therese Ku", "Thomas Lauer", "Christopher Cheadle", "C. Conover Talbot Jr", "Chunfa Jie", "Sharon McGrath-Morrow", "Landon S. King", "Jeremy Walston", "Enid R. Neptune"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020712.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Increased_oxidative_stress_and_cell_death_evident_in_murine_mid_life_/433708", "title"=>"Increased oxidative stress and cell death evident in murine mid-life.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-21 01:01:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/764054"], "description"=>"<p>Schematic depiction of the ontogeny of injury events associated with airspace enlargement in the aging murine lung.</p>", "links"=>[], "tags"=>["depiction", "ontogeny", "events", "airspace", "enlargement", "aging", "murine"], "article_id"=>434407, "categories"=>["Physiology", "Immunology"], "users"=>["Carla L. Calvi", "Megan Podowski", "Franco R. D'Alessio", "Shana L. Metzger", "Kaori Misono", "Hataya Poonyagariyagorn", "Armando Lopez-Mercado", "Therese Ku", "Thomas Lauer", "Christopher Cheadle", "C. Conover Talbot Jr", "Chunfa Jie", "Sharon McGrath-Morrow", "Landon S. King", "Jeremy Walston", "Enid R. Neptune"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020712.g007", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Schematic_depiction_of_the_ontogeny_of_injury_events_associated_with_airspace_enlargement_in_the_aging_murine_lung_/434407", "title"=>"Schematic depiction of the ontogeny of injury events associated with airspace enlargement in the aging murine lung.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-21 01:13:27"}
  • {"files"=>["https://ndownloader.figshare.com/files/763887"], "description"=>"<p>A. Movat's staining of lungs from mice at designated ages. Left panel shows representative high power (40×) images of lung parenchyma. Right panel shows low power (10×) images of bronchioles. Arrowheads denote sites of elastin deposition (blue-black). Line demarcation indicates areas of enhanced collagen content (yellow). Elastin deposition in the alveolar walls is modestly reduced at 12 months but shows recovered abundance at 20 months. Peribronchiolar collagen deposition is increased in the 12 month and 20 month old lungs. N = 4–6 mice per time point. B. Zymographic analysis of lungs from mice at the designated ages. Top arrow denotes MMP9 band. Bottom arrow denotes MMP2 band. N = 4–6 mice per time point. C. Quantitation of alveolar attachments in the lungs of mice at the designated ages show a progressive reduction in attachments with increasing age. N = 4–6 mice per time point. *p<0.05 compared with 2 months.</p>", "links"=>[], "tags"=>["localization", "aging"], "article_id"=>434248, "categories"=>["Physiology", "Immunology"], "users"=>["Carla L. Calvi", "Megan Podowski", "Franco R. D'Alessio", "Shana L. Metzger", "Kaori Misono", "Hataya Poonyagariyagorn", "Armando Lopez-Mercado", "Therese Ku", "Thomas Lauer", "Christopher Cheadle", "C. Conover Talbot Jr", "Chunfa Jie", "Sharon McGrath-Morrow", "Landon S. King", "Jeremy Walston", "Enid R. Neptune"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020712.g006", "stats"=>{"downloads"=>4, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Matrix_localization_in_aging_lung_/434248", "title"=>"Matrix localization in aging lung.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-21 01:10:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/764221"], "description"=>"<p>Overrepresented pathways within airspace peak.</p>", "links"=>[], "tags"=>["pathways", "airspace"], "article_id"=>434581, "categories"=>["Physiology", "Immunology"], "users"=>["Carla L. Calvi", "Megan Podowski", "Franco R. D'Alessio", "Shana L. Metzger", "Kaori Misono", "Hataya Poonyagariyagorn", "Armando Lopez-Mercado", "Therese Ku", "Thomas Lauer", "Christopher Cheadle", "C. Conover Talbot Jr", "Chunfa Jie", "Sharon McGrath-Morrow", "Landon S. King", "Jeremy Walston", "Enid R. Neptune"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020712.t001", "stats"=>{"downloads"=>2, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Overrepresented_pathways_within_airspace_peak_/434581", "title"=>"Overrepresented pathways within airspace peak.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-06-21 01:16:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/763761"], "description"=>"<p>A. Representative histograms depicting lymphocyte subsets identified in lungs of mice at indicated ages. An increase in CD19+ cells occurs at 12 months of age compared with earlier time points (2 and 8 months). N = 4–6 mice per time point. B. Relative proportion of lymphocyte subsets quantified by flow cytometry in lung mononuclear cells isolated from mice at designated ages. N = 4–6 mice per time point. C. Quantitative immunohistochemistry of macrophage abundance in lungs of aging mice. An increase in macrophage infiltration occurs at 12 months of age compared with 8 months. Data are mean +/− SEM. N = 3–6 mice per time point. D. IL12/23 and IL17 ELISA analyses of lung lysates from mice at designated ages. A reduction of IL17 levels is evident in the lungs of mice 8 months of age and older compared with 2 month old mice.</p>", "links"=>[], "tags"=>["compartments", "aging"], "article_id"=>434118, "categories"=>["Physiology", "Immunology"], "users"=>["Carla L. Calvi", "Megan Podowski", "Franco R. D'Alessio", "Shana L. Metzger", "Kaori Misono", "Hataya Poonyagariyagorn", "Armando Lopez-Mercado", "Therese Ku", "Thomas Lauer", "Christopher Cheadle", "C. Conover Talbot Jr", "Chunfa Jie", "Sharon McGrath-Morrow", "Landon S. King", "Jeremy Walston", "Enid R. Neptune"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020712.g005", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Alterations_in_immune_cell_compartments_in_the_aging_lung_/434118", "title"=>"Alterations in immune cell compartments in the aging lung.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-21 01:08:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/764278"], "description"=>"<p>*<b>p<0.05.</b></p>", "links"=>[], "tags"=>["cytometric", "mononculear", "subsets", "aging"], "article_id"=>434631, "categories"=>["Physiology", "Immunology"], "users"=>["Carla L. Calvi", "Megan Podowski", "Franco R. D'Alessio", "Shana L. Metzger", "Kaori Misono", "Hataya Poonyagariyagorn", "Armando Lopez-Mercado", "Therese Ku", "Thomas Lauer", "Christopher Cheadle", "C. Conover Talbot Jr", "Chunfa Jie", "Sharon McGrath-Morrow", "Landon S. King", "Jeremy Walston", "Enid R. Neptune"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020712.t002", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Flow_cytometric_analysis_of_mononculear_cell_subsets_in_aging_lungs_/434631", "title"=>"Flow cytometric analysis of mononculear cell subsets in aging lungs.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-06-21 01:17:11"}
  • {"files"=>["https://ndownloader.figshare.com/files/763619"], "description"=>"<p>A. ELISA analysis of IgG containing complexes in serum from mice at designated ages. A trend towards a significant increase is apparent between 8 and 12 months of age. N = 6 mice per group. B. ELISA analysis of lung lysates from mice at different ages. Data are mean +/− SEM. A significant increase in immunoglobulin deposition in the lung occurs between 8 and 12 months of age. N = 4–6 mice per time point. C. Densitometric analysis of immunoglobulin expression in lung lysates from mice at the denoted ages show that IgM (top panel) and IgG (bottom panel) are induced in the 8 and 12 month old lung, respectively. D. Immunohistochemical staining for IgG in lungs of representative mice at designated ages. Arrows denote immunoglobulin deposition in airspace wall. Arrowheads denote cell-associated deposition. N = 6–8 mice per group. A generalized increase in deposition in the airspace compartment occurs in the 12 month old lung. All images are 20×, except for insets on right, which are 40×. E. Coimmunofluorescent staining for IgG (red) and C3 complement (green) with phase overlay (L) shows evidence of granular colocalization (white arrowheads) in alveolar epithelial cells along with sites of predominant IgG deposition (black arrow) and C3 deposition (white arrow). Coimmunofluroescent staining for IgG and C3 complement in 12 month old lung shows strong colocalization in the perivascular region. V-vessel lumen. 40× magnification.</p>", "links"=>[], "tags"=>["deposition", "lungs", "aging"], "article_id"=>433972, "categories"=>["Physiology", "Immunology"], "users"=>["Carla L. Calvi", "Megan Podowski", "Franco R. D'Alessio", "Shana L. Metzger", "Kaori Misono", "Hataya Poonyagariyagorn", "Armando Lopez-Mercado", "Therese Ku", "Thomas Lauer", "Christopher Cheadle", "C. Conover Talbot Jr", "Chunfa Jie", "Sharon McGrath-Morrow", "Landon S. King", "Jeremy Walston", "Enid R. Neptune"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020712.g004", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Immunoglobulin_deposition_in_lungs_of_aging_mice_/433972", "title"=>"Immunoglobulin deposition in lungs of aging mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-21 01:06:12"}
  • {"files"=>["https://ndownloader.figshare.com/files/763182"], "description"=>"<p>A. Schematic diagram of the lung harvest time points and the corresponding phases of human aging. B. Representative lung histology from hematoxylin and eosin stains of 2 month, 12 month and 20 month old mice depict a progressive increase in airspace size with age. Photomicrographs are representative of N = 4–6 mice per group. Original magnification 20×. C. Morphometric analysis of airspace caliber denotes transition point to progressive airspace enlargement between 8 and 12 months of age. N = 6 mice per group. D. Body weight measurement establishes trend to weight loss initiated between 8 and 12 months of age. N = 6 mice per group. MLI-Mean linear intercept (mm). BW-Body weight. The pale versus dark shades show different phases in the evolution of the noted parameter.</p>", "links"=>[], "tags"=>["aging"], "article_id"=>433538, "categories"=>["Physiology", "Immunology"], "users"=>["Carla L. Calvi", "Megan Podowski", "Franco R. D'Alessio", "Shana L. Metzger", "Kaori Misono", "Hataya Poonyagariyagorn", "Armando Lopez-Mercado", "Therese Ku", "Thomas Lauer", "Christopher Cheadle", "C. Conover Talbot Jr", "Chunfa Jie", "Sharon McGrath-Morrow", "Landon S. King", "Jeremy Walston", "Enid R. Neptune"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020712.g001", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Time_course_analysis_of_aging_lung_phenotype_/433538", "title"=>"Time course analysis of aging lung phenotype.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-21 00:58:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/383813", "https://ndownloader.figshare.com/files/383829", "https://ndownloader.figshare.com/files/383849", "https://ndownloader.figshare.com/files/383864", "https://ndownloader.figshare.com/files/383895", "https://ndownloader.figshare.com/files/383906", "https://ndownloader.figshare.com/files/383916"], "description"=>"<div><h3>Background</h3><p>Respiratory dysfunction is a major contributor to morbidity and mortality in aged populations. The susceptibility to pulmonary insults is attributed to “low pulmonary reserve”, ostensibly reflecting a combination of age-related musculoskeletal, immunologic and intrinsic pulmonary dysfunction.</p> <h3>Methods/Principal Findings</h3><p>Using a murine model of the aging lung, senescent DBA/2 mice, we correlated a longitudinal survey of airspace size and injury measures with a transcriptome from the aging lung at 2, 4, 8, 12, 16 and 20 months of age. Morphometric analysis demonstrated a nonlinear pattern of airspace caliber enlargement with a critical transition occurring between 8 and 12 months of age marked by an initial increase in oxidative stress, cell death and elastase activation which is soon followed by inflammatory cell infiltration, immune complex deposition and the onset of airspace enlargement. The temporally correlative transcriptome showed exuberant induction of immunoglobulin genes coincident with airspace enlargement. Immunohistochemistry, ELISA analysis and flow cytometry demonstrated increased immunoglobulin deposition in the lung associated with a contemporaneous increase in activated B-cells expressing high levels of TLR4 (toll receptor 4) and CD86 and macrophages during midlife. These midlife changes culminate in progressive airspace enlargement during late life stages.</p> <h3>Conclusion/Significance</h3><p>Our findings establish that a tissue-specific aging program is evident during a presenescent interval which involves early oxidative stress, cell death and elastase activation, followed by B lymphocyte and macrophage expansion/activation. This sequence heralds the progression to overt airspace enlargement in the aged lung. These signature events, during middle age, indicate that early stages of the aging immune system may have important correlates in the maintenance of tissue morphology. We further show that time-course analyses of aging models, when informed by structural surveys, can reveal nonintuitive signatures of organ-specific aging pathology.</p> </div>", "links"=>[], "tags"=>["homeostasis", "accompanies", "murine", "senescence"], "article_id"=>135791, "categories"=>["Physiology", "Immunology"], "users"=>["Carla L. Calvi", "Megan Podowski", "Franco R. D'Alessio", "Shana L. Metzger", "Kaori Misono", "Hataya Poonyagariyagorn", "Armando Lopez-Mercado", "Therese Ku", "Thomas Lauer", "Christopher Cheadle", "C. Conover Talbot Jr", "Chunfa Jie", "Sharon McGrath-Morrow", "Landon S. King", "Jeremy Walston", "Enid R. Neptune"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0020712.s001", "https://dx.doi.org/10.1371/journal.pone.0020712.s002", "https://dx.doi.org/10.1371/journal.pone.0020712.s003", "https://dx.doi.org/10.1371/journal.pone.0020712.s004", "https://dx.doi.org/10.1371/journal.pone.0020712.s005", "https://dx.doi.org/10.1371/journal.pone.0020712.s006", "https://dx.doi.org/10.1371/journal.pone.0020712.s007"], "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Critical_Transition_in_Tissue_Homeostasis_Accompanies_Murine_Lung_Senescence/135791", "title"=>"Critical Transition in Tissue Homeostasis Accompanies Murine Lung Senescence", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-06-21 01:36:31"}
  • {"files"=>["https://ndownloader.figshare.com/files/763495"], "description"=>"<p>Nine profiles generated by random selection for difference from evenly spaced profiles are depicted. The profile whose peak corresponded to the onset of airspace enlargement is enlarged on the left. Red shows the top 200 genes. Blue shows the remainder of genes within the cluster.</p>", "links"=>[], "tags"=>["k-means", "temporally", "approximates", "airspace"], "article_id"=>433847, "categories"=>["Physiology", "Immunology"], "users"=>["Carla L. Calvi", "Megan Podowski", "Franco R. D'Alessio", "Shana L. Metzger", "Kaori Misono", "Hataya Poonyagariyagorn", "Armando Lopez-Mercado", "Therese Ku", "Thomas Lauer", "Christopher Cheadle", "C. Conover Talbot Jr", "Chunfa Jie", "Sharon McGrath-Morrow", "Landon S. King", "Jeremy Walston", "Enid R. Neptune"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020712.g003", "stats"=>{"downloads"=>1, "page_views"=>26, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Schematic_of_selection_of_K_means_cluster_profile_that_temporally_approximates_airspace_enlargement_/433847", "title"=>"Schematic of selection of K-means cluster profile that temporally approximates airspace enlargement.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-21 01:04:07"}

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