Efficacy of leukadherin-1 in the prevention of hyperoxia-induced lung injury in neonatal rats

American Journal of Respiratory Cell and Molecular Biology

Volumn 53, Issue 6, 2015, Pages 793-801

  Jagarapu, Jawahar ^a   Kelchtermans, Jelte ^a   Rong, Min ^a   Chen, Shaoyi ^a   Hehre, Dorothy ^a   Hummler, Stefanie ^a   Faridi, Mohd Hafeez ^b   Gupta, Vineet ^b   Wu, Shu ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b RUSH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

BPD; Hyperoxia; Inflammation; Integrin; LA1

Indexed keywords

INTEGRIN; LEUKADHERIN 1; MONOCYTE CHEMOTACTIC PROTEIN 1; PLACEBO; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VASCULOTROPIN; VON WILLEBRAND FACTOR; ANTIINFLAMMATORY AGENT; BENZOIC ACID DERIVATIVE; LEUKADHERIN-1; THIOHYDANTOIN DERIVATIVE;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; HEART RIGHT VENTRICLE HYPERTROPHY; HYPEROXIA; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; LEUKOCYTE COUNT; LUNG ALVEOLUS; LUNG DYSPLASIA; LUNG INJURY; MACROPHAGE; NEUTROPHIL; NEWBORN; NONHUMAN; PROTEIN EXPRESSION; PULMONARY HYPERTENSION; RAT; WESTERN BLOTTING; ANIMAL; BRONCHOPULMONARY DYSPLASIA; COMPLICATION; DRUG EFFECTS; HYPERTENSION, PULMONARY; IMMUNOLOGY; LUNG; NEUTROPHIL CHEMOTAXIS; PRECLINICAL STUDY; SPRAGUE DAWLEY RAT; TREATMENT OUTCOME; VASCULAR REMODELING; VASCULARIZATION;

ANIMALS; ANIMALS, NEWBORN; ANTI-INFLAMMATORY AGENTS; BENZOATES; BRONCHOPULMONARY DYSPLASIA; DRUG EVALUATION, PRECLINICAL; HYPEROXIA; HYPERTENSION, PULMONARY; LUNG; NEUTROPHIL INFILTRATION; RATS, SPRAGUE-DAWLEY; THIOHYDANTOINS; TREATMENT OUTCOME; VASCULAR REMODELING;

EID: 84963838149     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2014-0422OC     Document Type: Article

References (55)

1. Jobe AH, Bancalari E. Bronchopulmonary dysplasia. Am J Respir Crit Care Med 2001;163:1723-1729.
2. Bhandari A, Bhandari V. Pitfalls, problems, and progress in bronchopulmonary dysplasia. Pediatrics 2009;123:1562-1573.
3. Thebaud B, Abmen SH. Bronchpulmonary dysplasia: Where have all the vessels gone? Roles of angiogenic growth factors in chronic lung disease. Am J Respir Crit Care Med 2007;175:978-985.
4. Stenmark KR, Abman SH. Lung vascular development: implications for pathogenesis of bronchopulmonary dysplasia. Annu Rev Physiol 2005;67:623-661.
5. Speer CP. Inflammation and bronchopulmonary dysplasia: A continuing story. Semin Fetal Neonatal Med 2006;11:354-362.
6. Bose CL, Dammann CE, Laughon MM. BPD and inflammatory biomarkers in the premature neonate. Arch Dis Child Fetal Neonatal Ed 2008;93:F455-F461.
7. Wright CJ, Kirpalani H. Targeting inflammation to prevent bronchopulmonary dysplasia: can new insights be translated into therapies. Pediatrics 2011;128:111-126.
8. Ambalavanan N, Schelonka RL, Dimmitt RA, Carlo WA, Munoz- Hernandez B, Das A, McDonald SA, Thorsen P, Skogstrand K, Hougaard DM, et al.; Eunice Kennedy Shriver National Institute of Child Health and Human development Neonatal Research Network. Cytokines associated with bronchopulmonary dysplasia or death in extremely low birth weight infants. Pediatrics 2009;123:1132-1141.
9. Jónsson B, Tullus K, Brauner A, Lu Y, Noack G. Early increase of TNF alpha and IL-6 in tracheobronchial aspirate fluid indicator of subsequent chronic lung disease in preterm infants. Arch Dis Child Fetal Neonatal Ed 1997;77:F198-F201.
10. Bland RD, Mokres LM, Ertsey R, Jacobson BE, Jiang S, Rabinovitch M, Xu L, Shinwell ES, Zhang F, Beasley MA. Mechanical ventilation with 40% oxygen reduces pulmonary expression of genes that regulate lung development and impairs alveolar septation in newborn mice. Am J Physiol Lung Cell Mol Physiol 2007;293:L1099-L1110.
11. Hilgendorff A, Parai K, Ertsey R, Juliana Rey-Parra G, Thébaud B, Tamosiuniene R, Jain N, Navarro EF, Starcher BC, Nicolls MR, et al. Neonatal mice genetically modified to express the elastase inhibitor elafin are protected against the adverse effects of mechanical ventilation on lung growth. Am J Physiol Lung Cell Mol Physiol 2012; 303:L215-L227.
12. Ogden BE, Murphy SA, Saunders GC, Pathak D, Johnson JD. Neonatal lung neutrophils and elastase/proteinase inhibitor imbalance. Am Rev Respir Dis 1984;130:817-821.
13. LeFlore JL, Salhab WA, Broyles RS, Engle WD. Association of antenatal and postnatal dexamethasone exposure with outcome in extremely low bith weight neoanates. Pediatrics 2002;110:275-279.
14. Halliday H, Ehrenkranz R, Doyle L. Early (, 8d) postnatal corticosteroids for preventing BPD in preterm infants. Cochrane Database Syst Rev 2009; (1):CD001146.
15. Wilson-Costello D, Walsh MC, Langer JC, Guillet R, Laptook AR, Stoll BJ, Shankaran S, Finer NN, Van Meurs KP, Engle WA, Das A; Eunice Kennedy Shriver National Institute of Child Health and Human Development Neonatal Research Network. Impact of postnatal corticosteroid use on neurodevelopment at 18 to 22 months' adjusted age: Effects of dose, timing, and risk of bronchopulmonary dysplasia in extremely low birth weight infants. Pediatrics 2009;123: E430-E437.
16. Arnaout MA. Structure and function of the leukocyte adhesion molecules CD11/CD18. Blood 1990;75:1037-1050.
17. Li R, Arnaout MA. Functional analysis of the beta 2 integrins. Methods Mol Biol 1999;129:105-124.
18. Mayadas TN, Cullere X. Neutrophil beta2 integrins: moderators of life or death decisions. Trends Immunol 2005;26:388-395.
19. Simon DI, Dhen Z, Seifert P, Edelman ER, Ballantyne CM, Rogers C. Decreased neointimal formation in Mac-1(2/2) mice reveals a role for inflammation in vascular repair after angioplasty. J Clin Invest 2000;105:293-300.
20. Faridi MH, Maiguel D, Barth CJ, Stoub D, Day R, Schürer S, Gupta V. Identification of novel agonists of the integrin CD11b/CD18. Bioorg Med Chem Lett 2009;19:6902-6906.
21. Maiguel D, Faridi MH, Wei C, Kuwano Y, Balla KM, Hernandez D, Barth CJ, Lugo G, Donnelly M, Nayer A, et al. Small molecule-mediated activation of the integrin CD11b/CD18 reduces inflammatory disease. Sci Signal 2011;4:ra57.
22. Faridi MH, Altintas MM, Gomez C, Duque JC, Vazquez-Padron RI, Gupta V. Small molecule agonists of integrin CD11b/CD18 do not induce global conformational changes and are significantly better than activating antibodies in reducing vascular injury. Biochim Biophys Acta 2013;1830:3696-3710.
23. Bhandari V. Molecular mechanisms of hyperoxia-induced acute lung injury. Front Biosci 2008;13:6653-6661.
24. Bonikos DS, Bensch KG, Ludwin SK, Northway WH. Oxygen toxicity in the newborn: The effect of prolonged 100 per cent O2 exposure on the lungs of newborn mice. Lab Invest 1975;32:619-635.
25. Buczynski B, Maduekwe ET, O'Reilly MA. The role of hyperoxia in the pathogenesis of experimental BPD. Semin Perinatol 2013;37:69-78.
26. Alapati D, Rong M, Chen S, Hehre D, Rodriguez MM, Lipson KE, Wu S. Connective tissue growth factor antibody therapy attenuates hyperoxia-induced lung injury in neonatal rats. Am J Respir Cell Mol Biol 2011;45:1169-1177.
27. Hummler SC, Rong M, Chen S, Hehre D, Alapati D, Wu S. Targeting GSK-3b to prevent hyperoxia-induced lung injury in neonatal rats. Am J Respir Cell Mol Biol 2013;48:578-588.
28. Alapati D, Rong M, Chen S, Hehre D, Hummler SC, Wu S. Inhibition of b-catenin signaling improves alveolarization and reduces pulmonary hypertension in experimental BPD. Am J Respir Cell Mol Biol 2014;51:104-113.
29. Chen S, Rong M, Platteau A, Hehre D, Ruiz P, Whitsett J, Bancalari B, Wu S. CTGF disrupts alveolarization and induces pulmonary hypertension in neonatal mice: implication in the pathogenesis of severe bronchopulmonary dysplasia. Am J Physiol Lung Cell Mol Physiol 2011;300:L330-L340.
30. Husain AN, Siddiqui NH, Stocker JT. Pathology of arrested acinar development in postsurfactant bronchopulmonary dysplasia. Hum Pathol 1998;29:710-717.
31. Jobe AL. The new BPD: An arrest of lung development. Pediatr Res 1999;46:641-643.
32. Coalson JJ. Pathology of new bronchopulmonary dysplasia. Semin Neonatol 2003;8:73-81.
33. Ryan RM, Ahmed Q, Lakshminrusimha S. Inflammatory mediators in the immunobiology of bronchopulmonary dysplasia. Clin Rev Allergy Immunol 2008;34:174-190.
34. Hilgendroff A, Reiss I, Ehrardt H, Eickelberg O, Alvira CM. Chronic lung disease in the preterm infant: lessons learned from animal models. Am J Respir Cell Mol Biol 2014;50:233-245.
35. Groneck P, Gotze-Speer B, Oppermann M, Eiffert H, Speer CP. Association of pulmonary inflammation and increased microvascular permeability during the development of bronchopulmonary dysplasia: A sequential analysis of inflammatory mediators in respiratory fluids of high-risk preterm infants. Pediatrics 1994;93:712-718.
36. Kim BI, Lee HE, Choi CW, Jo HS, Choi EH, Koh YY, Choi JH. Increased in cord blood soluble E-selectin and tracheal aspirate neutropils at birth and the development of new bronchopulmonary dysplasia. J Perinat Med 2004;3293:282-287.
37. Kotecha S, Silverman M, Shaw RJ, Klein N. Soluble L-selectin concentration in bronchoalveolar lavage fluid obtained from infants who develop chronic lung disease of prematurity. Arch Dis Child Fetal Neonatal Ed 1998;78:F143-F147.
38. Nold MF, Mangan NM, Rudloff I, Cho SX, Shariatian N, Samarasinghe TD, Skuza EM, Pedersen J, Veldman A, Berger PJ, et al. Interleukin-1 receptor antagonist prevents murine bronchopulmonary dysplasia induced by perinatal inflammation and hyperoxia. Proc Natl Acad Sci USA 2013;110:14384-14389.
39. Auten RL, Mason SN, Tanaka DT, Welty-Wolf K, Whorton MH. Anti-neutropil chemokine preserves alveolar development in hyperoxia-exposed newborn rats. Am J Physiol Lung Cell Mol Physiol 2001;281:L336-L344.
40. Deng H, Mason SN, Auton RL. Lung inflammation in hyperoxia can be prevented by antichemokine treatment in newborn rats. Am J Respir Crit Care Med 2000;162:2316-2323.
41. Vozzelli MA, Mason SN, Whorton MH, Auton RL. Antimacrophage chemokine treatment prevents neutropil and macrophage influx in hyperoxia-exposed newborn rats. Am J Physiol Lung Cell Mol Physiol 2004;286:L488-L493.
42. van Haaften T, Byrne R, Bonnet S, Rochefort GY, Akabutu J, Bouchentouf M, Rey-Parra GJ, Galipeau J, Haromy A, Eaton F, et al. Airway delivery of mesenchymal stem cells prevents arrested alveolar growth in neonatal lung injury in rats. Am J Respir Crit Care Med 2009;180:1131-1142.
43. Aslam M, Baveja R, Liang OD, Fernandez-Gonzalez A, Lee C, Mitsialis SA, Kourembanas S. Bone marrow stromal cells attenuate lung injury in a murine model of neonatal chronic lung disease. Am J Respir Crit Care Med 2009;180:1122-1130.
44. Sutsko RP, Young KC, Ribeiro A, Torres E, Rodriguez M, Hehre D, Devia C, McNiece I, Suguihara C. Long-term reparative effects of mesenchymal stem cell therapy following neonatal hyperoxiainduced lung injury. Pediatr Res 2013;73:46-53.
45. Voelkel NF, Vandivier RW, Tuder RM. Vascular endothelial growth factor in the lung. Am J Physiol Lung Cell Mol Physiol 2006;290: L209-L221.
46. McGrath-Morrow SA, Cho C, Cho C, Zhen L, Hicklin DJ, Tuder RM. Vascular endothelial growth factor receptor 2 blockade disrupts postnatal lung development. Am J Respir Cell Mol Biol 2005;32: 420-427.
47. Maniscalco WM, Watkins RH, D'Angio CT, Ryan RM. Hyperoxic injury decreases alveolar epithelial cell expression of vascular endothelial growth factor (VEGF) in neonatal rabbit lung. Am J Respir Cell Mol Biol 1997;16:557-567.
48. Kunig AM, Balasubramaniam V, Markham NE, Seedorf G, Gien J, Abman SH. Recombinant human VEGF treatment transiently increases lung edema but enhances lung structure after neonatal hyperoxia. Am J Physiol Lung Cell Mol Physiol 2006;291: L1068-L1078.
49. Thébaud B, Ladha F, Michelakis ED, Sawicka M, Thurston G, Eaton F, Hashimoto K, Harry G, Haromy A, Korbutt G, et al. Vascular endothelial growth factor gene therapy increases survival, promotes lung angiogenesis, and prevents alveolar damage in hyperoxia- induced lung injury: Evidence that angiogenesis participates alveolarization. Circulation 2005;112: 2477-2486.
50. Dasgupta C, Sakurai R, Wang Y, Guo P, Ambalavanan N, Torday JS, Rahan VK. Hyperoxia-induced neonatal rat lung injury involves activation of TGF-(beta) and Wnt signaling and is protected by rosiglitazone. Am J Physiol Lung Cell Mol Physiol 2009;296: L1031-L1041.
51. Popova AP, Bentley JK, Anyanwu AC, Richardson MN, Linn MJ, Lei J, Wong EJ, Goldsmith AM, Pryhuber GS, Hershenson MB. Glycogen synthase kinase-3b/b-catenin signaling regulates neonatal lung mesenchymal stromal cell myofibroblastic differentiation. Am J Physiol Lung Cell Mol Physiol 2012;303: L439-L448.
52. Heise RL, Stober V, Chelucaraju C, Hollingsworth JW, Garrantziotis S. Mechanical stretch induces epithelial-mesenchymal transition in alveolar epithelia via hyaluronan activation of innate immunity. J Biol Chem 2011;286:17435-17444.
53. Li HH, Li Q, Liu P, Liu Y, Wasserloos K, Chao W, You M, Oury TD, Chhinder S, Hackam DJ, et al. WNT1-inducible signaling pathway protein 1 contributes to ventilator-induced lung injury. Am J Respir Cell Mol Biol 2012;47:528-535.
54. Konigshoff M, Kramer M, Balsara N, Wilhelm J, Amarie OV, Jahn A, Rose F, Fink L, Seegar W, Schaefer L, et al. WNT1-inducible signaling protein-1 mediates pulmonary fibrosis in mice and is upregulated in humans with idiopathic pulmonary fibrosis. J Clin Invest 2009;119:772-787.
55. Alapathi D, Rong M, Chen S, Lin C, Li Y, Wu S. Inhibition of LRP5/6- mediated Wnt/b-catenin signaling by Mesd attenuates hyperoxiainduced pulmonary hypertension in neonatal rats. Pediatr Res 2013; 73:719-725.