Hypoxia-Inducible Factor 1a Signaling Promotes Repair of the Alveolar Epithelium after Acute Lung Injury

From the Division of Pulmonary, Critical Care, and Sleep Medicine,* Department of Medicine, and the Program in Cell Biology,y Department of Pediatrics, National Jewish Health, Denver, Colorado; the Division of Pulmonary Sciences and Critical Care Medicine,z Mucosal Inflammation Program,{ Integrated Department of Immunology,k and Program in Translational Lung Research,zz Division of Pulmonary Sciences and Critical Care Medicine, University of Colorado Denver, Aurora, Colorado; the Department of Research,x Denver Veterans Affairs Medical Center, Denver, Colorado; the Department of Anesthesiology and Perioperative Medicine,** University of Alabama at Birmingham, Birmingham, Alabama; and the Division of Pulmonary and Critical Care Medicine,yy University of California San Francisco, San Francisco, California

[1]  M. Balaan,et al.  Acute Respiratory Distress Syndrome , 2016, Critical care nursing quarterly.

[2]  Thibault Lagache,et al.  Statistical analysis of molecule colocalization in bioimaging , 2015, Cytometry. Part A : the journal of the International Society for Analytical Cytology.

[3]  C. Ackerley,et al.  Hypoxia-inducible factor-1 stimulates postnatal lung development but does not prevent O2-induced alveolar injury. , 2015, American journal of respiratory cell and molecular biology.

[4]  S. Rafii,et al.  Platelet-derived SDF-1 primes the pulmonary capillary vascular niche to drive lung alveolar regeneration , 2015, Nature Cell Biology.

[5]  M. Loebe,et al.  Hypoxia-induced deoxycytidine kinase contributes to epithelial proliferation in pulmonary fibrosis. , 2014, American journal of respiratory and critical care medicine.

[6]  M. Krasnow,et al.  Alveolar progenitor and stem cells in lung development, renewal and cancer , 2014, Nature.

[7]  D. McDonald,et al.  Identification of pY654-β-catenin as a critical co-factor in hypoxia-inducible factor-1α signaling and tumor responses to hypoxia , 2013, Oncogene.

[8]  Christoph H. Borchers,et al.  HIF1A Reduces Acute Lung Injury by Optimizing Carbohydrate Metabolism in the Alveolar Epithelium , 2013, PLoS biology.

[9]  Michael J. Cronce,et al.  Type 2 alveolar cells are stem cells in adult lung. , 2013, The Journal of clinical investigation.

[10]  M. Kahn,et al.  Role of β-catenin-regulated CCN matricellular proteins in epithelial repair after inflammatory lung injury. , 2013, American journal of physiology. Lung cellular and molecular physiology.

[11]  R. Mason,et al.  Efficient and rapid isolation and purification of mouse alveolar type II epithelial cells , 2012, Experimental lung research.

[12]  Arthur S Slutsky,et al.  Acute Respiratory Distress Syndrome The Berlin Definition , 2012 .

[13]  C. Waters,et al.  CXCR4 regulates migration of lung alveolar epithelial cells through activation of Rac1 and matrix metalloproteinase-2. , 2012, American journal of physiology. Lung cellular and molecular physiology.

[14]  M. Kahn,et al.  Neutrophil transmigration triggers repair of the lung epithelium via β-catenin signaling , 2011, Proceedings of the National Academy of Sciences.

[15]  N. Heintz,et al.  Activation of hypoxia-inducible factor-1 protects airway epithelium against oxidant-induced barrier dysfunction. , 2011, American journal of physiology. Lung cellular and molecular physiology.

[16]  G. Adami,et al.  FoxM1 mediates the progenitor function of type II epithelial cells in repairing alveolar injury induced by Pseudomonas aeruginosa , 2011, The Journal of experimental medicine.

[17]  P. Fagenholz,et al.  Hypoxia and inflammation. , 2011, The New England journal of medicine.

[18]  Nupura S. Bhise,et al.  Synergistic effect of HIF-1α gene therapy and HIF-1-activated bone marrow-derived angiogenic cells in a mouse model of limb ischemia , 2009, Proceedings of the National Academy of Sciences.

[19]  W. Seeger,et al.  Macrophage tumor necrosis factor-alpha induces epithelial expression of granulocyte-macrophage colony-stimulating factor: impact on alveolar epithelial repair. , 2009, American journal of respiratory and critical care medicine.

[20]  J. Harkema,et al.  HIF1α Is Essential for Normal Intrauterine Differentiation of Alveolar Epithelium and Surfactant Production in the Newborn Lung of Mice* , 2008, Journal of Biological Chemistry.

[21]  C. Waters,et al.  Mechanical stretch decreases migration of alveolar epithelial cells through mechanisms involving Rac1 and Tiam1. , 2008, American journal of physiology. Lung cellular and molecular physiology.

[22]  R. Buscà,et al.  HIF1 transcription factor regulates laminin-332 expression and keratinocyte migration , 2008, Journal of Cell Science.

[23]  R. Lehmann,et al.  Hypoxia-Inducible Factor-1 Is Central to Cardioprotection: A New Paradigm for Ischemic Preconditioning , 2008, Circulation.

[24]  M. López-Lázaro,et al.  The warburg effect: why and how do cancer cells activate glycolysis in the presence of oxygen? , 2008, Anti-cancer agents in medicinal chemistry.

[25]  K. Brown,et al.  Pulmonary Stromal-Derived Factor-1 Expression and Effect on Neutrophil Recruitment during Acute Lung Injury1 , 2007, The Journal of Immunology.

[26]  Wei Li,et al.  Extracellular heat shock protein‐90α: linking hypoxia to skin cell motility and wound healing , 2007, The EMBO journal.

[27]  A. C. Williams,et al.  Interaction between beta-catenin and HIF-1 promotes cellular adaptation to hypoxia. , 2007, Nature cell biology.

[28]  R. DePinho,et al.  Mouse model for noninvasive imaging of HIF prolyl hydroxylase activity: assessment of an oral agent that stimulates erythropoietin production. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[29]  G. Camenisch,et al.  Integration of Oxygen Signaling at the Consensus HRE , 2005, Science's STKE.

[30]  Michael K. Wendt,et al.  CXCL12 activation of CXCR4 regulates mucosal host defense through stimulation of epithelial cell migration and promotion of intestinal barrier integrity. , 2005, American journal of physiology. Gastrointestinal and liver physiology.

[31]  W. Seeger,et al.  Role of hypoxia-inducible factor-1alpha in hypoxia-induced apoptosis of primary alveolar epithelial type II cells. , 2005, American journal of respiratory cell and molecular biology.

[32]  J. Sznajder,et al.  Effects of hypoxia on the alveolar epithelium. , 2005, Proceedings of the American Thoracic Society.

[33]  M. Burdick,et al.  Circulating fibrocytes traffic to the lungs in response to CXCL12 and mediate fibrosis. , 2004, The Journal of clinical investigation.

[34]  Geoffrey C Gurtner,et al.  Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1 , 2004, Nature Medicine.

[35]  Caroline C. Blouin,et al.  Hypoxic gene activation by lipopolysaccharide in macrophages: implication of hypoxia-inducible factor 1alpha. , 2004, Blood.

[36]  S. Saccani,et al.  Regulation of the Chemokine Receptor CXCR4 by Hypoxia , 2003, The Journal of experimental medicine.

[37]  G. Semenza Targeting HIF-1 for cancer therapy , 2003, Nature Reviews Cancer.

[38]  K. Iwabuchi,et al.  VEGF regulates the proliferation of acid-exposed alveolar lining epithelial cells , 2003, Thorax.

[39]  Brian Keith,et al.  Differential roles of hypoxia-inducible factor 1alpha (HIF-1alpha) and HIF-2alpha in hypoxic gene regulation. , 2003, Molecular and cellular biology.

[40]  R. Groves,et al.  Increased migration of murine keratinocytes under hypoxia is mediated by induction of urokinase plasminogen activator. , 2002, The Journal of investigative dermatology.

[41]  Miguel Vicente-Manzanares,et al.  Cutting Edge: Association of the Motor Protein Nonmuscle Myosin Heavy Chain-IIA with the C Terminus of the Chemokine Receptor CXCR4 in T Lymphocytes1 , 2002, The Journal of Immunology.

[42]  S. Colgan,et al.  Ecto-5'-nucleotidase (CD73) regulation by hypoxia-inducible factor-1 mediates permeability changes in intestinal epithelia. , 2002, The Journal of clinical investigation.

[43]  T. Geiser,et al.  Keratinocyte growth factor can enhance alveolar epithelial repair by nonmitogenic mechanisms. , 2002, American journal of physiology. Lung cellular and molecular physiology.

[44]  N. Chandel,et al.  Anoxia-induced apoptosis occurs through a mitochondria-dependent pathway in lung epithelial cells. , 2002, American journal of physiology. Lung cellular and molecular physiology.

[45]  M. Nishita,et al.  Stromal Cell-Derived Factor 1α Activates LIM Kinase 1 and Induces Cofilin Phosphorylation for T-Cell Chemotaxis , 2002, Molecular and Cellular Biology.

[46]  P. Carmeliet,et al.  Loss of HIF-2α and inhibition of VEGF impair fetal lung maturation, whereas treatment with VEGF prevents fatal respiratory distress in premature mice , 2002, Nature Medicine.

[47]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[48]  D. Theodorescu,et al.  Cell density mediated pericellular hypoxia leads to induction of HIF-1α via nitric oxide and Ras/MAP kinase mediated signaling pathways , 2001, Oncogene.

[49]  R. Hershberg,et al.  Hypoxia-Inducible Factor 1–Dependent Induction of Intestinal Trefoil Factor Protects Barrier Function during Hypoxia , 2001, The Journal of experimental medicine.

[50]  M. Matthay,et al.  Alveolar fluid clearance is impaired in the majority of patients with acute lung injury and the acute respiratory distress syndrome. , 2001, American journal of respiratory and critical care medicine.

[51]  T. Mcclanahan,et al.  Involvement of chemokine receptors in breast cancer metastasis , 2001, Nature.

[52]  L. D. Nielsen,et al.  KGF regulates pulmonary epithelial proliferation and surfactant protein gene expression in adult rat lung. , 2000, American journal of physiology. Lung cellular and molecular physiology.

[53]  J. M. Arbeit,et al.  Coordinate up-regulation of hypoxia inducible factor (HIF)-1alpha and HIF-1 target genes during multi-stage epidermal carcinogenesis and wound healing. , 2000, Cancer research.

[54]  T. Geiser,et al.  Interleukin-1beta augments in vitro alveolar epithelial repair. , 2000, American journal of physiology. Lung cellular and molecular physiology.

[55]  M. Müller,et al.  Keratinocyte growth factor-induced hyperplasia of rat alveolar type II cells in vivo is resolved by differentiation into type I cells and by apoptosis. , 1999, The European respiratory journal.

[56]  N. Chandel,et al.  Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[57]  P. Carmeliet,et al.  Role of HIF-1α in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis , 1998, Nature.

[58]  J. Pittet,et al.  Biochemical detection of type I cell damage after nitrogen dioxide-induced lung injury in rats. , 1997, American journal of physiology. Lung cellular and molecular physiology.

[59]  T. Springer,et al.  The Chemokine SDF-1 Is a Chemoattractant for Human CD34+ Hematopoietic Progenitor Cells and Provides a New Mechanism to Explain the Mobilization of CD34+ Progenitors to Peripheral Blood , 1997, The Journal of experimental medicine.

[60]  T. Springer,et al.  A highly efficacious lymphocyte chemoattractant, stromal cell-derived factor 1 (SDF-1) , 1996, The Journal of experimental medicine.

[61]  Lieve Moons,et al.  Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele , 1996, Nature.

[62]  H. Folkesson,et al.  Transforming growth factor-alpha enhances alveolar epithelial cell repair in a new in vitro model. , 1994, The American journal of physiology.

[63]  C. Leslie,et al.  Hepatocyte growth factor is a growth factor for rat alveolar type II cells. , 1994, American journal of respiratory cell and molecular biology.

[64]  J. Whitsett,et al.  Production of immortalized distal respiratory epithelial cell lines from surfactant protein C/simian virus 40 large tumor antigen transgenic mice. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[65]  M. Matthay,et al.  Differential responses of the endothelial and epithelial barriers of the lung in sheep to Escherichia coli endotoxin. , 1991, The Journal of clinical investigation.

[66]  P. Rogol Intact epithelial barrier function is critical for resolution of alveolar edema in humans. , 1991, The American review of respiratory disease.

[67]  J. Hogg,et al.  Alveolar epithelial damage. A critical difference between high pressure and oleic acid-induced low pressure pulmonary edema. , 1986, The Journal of clinical investigation.

[68]  R. Mason,et al.  Pulmonary alveolar type II cells isolated from rats. Release of phosphatidylcholine in response to beta-adrenergic stimulation. , 1979, The Journal of clinical investigation.

[69]  D H Bowden,et al.  The type 2 cell as progenitor of alveolar epithelial regeneration. A cytodynamic study in mice after exposure to oxygen. , 1974, Laboratory investigation; a journal of technical methods and pathology.

[70]  R. J. Stephens,et al.  Renewal of alveolar epithelium in the rat following exposure to NO2. , 1973, The American journal of pathology.

[71]  J. Reif,et al.  Insensitivity of the alveolar septum to local hypoxia. , 1972, The American journal of physiology.

[72]  G. Winter,et al.  Effect of Air Exposure and Occlusion on Experimental Human Skin Wounds , 1963, Nature.

[73]  M. Haneklaus,et al.  Succinate is an inflammatory signal that induces IL-1 beta through HIF-1 alpha , 2017 .