Arginase inhibition prevents bleomycin-induced pulmonary hypertension, vascular remodeling, and collagen deposition in neonatal rat lungs

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 308, Issue 6, 2015, Pages L503-L510

  Grasemann, Hartmut ^a,b   Dhaliwal, Rupinder ^a   Ivanovska, Julijana ^a   Kantores, Crystal ^a   McNamara, Patrick J ^a,b,c   Scott, Jeremy A ^d   Belik, Jaques ^a,b,c   Jankov, Robert P ^a,b,c,e  

^a HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d LAKEHEAD UNIVERSITY   (Canada)

^e UNIVERSITY OF TORONTO   (Canada)

Author keywords

Chronic lung disease; Nitric oxide; Oxidative stress

Indexed keywords

3 NITROTYROSINE; AMINO 2 BORONO 6 HEXANOIC ACID; ARGINASE; ARGINASE 1; ARGINASE 2; ARGININE; BLEOMYCIN; CHEMOKINE; COLLAGEN; CYTOKINE; HEXANOIC ACID; NITRIC OXIDE; UNCLASSIFIED DRUG; 2-AMINO-6-BORONOHEXANOIC ACID; AMINOCAPROIC ACID DERIVATIVE; ANTINEOPLASTIC ANTIBIOTIC; BORON DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOAVAILABILITY; COLLAGEN SYNTHESIS; CONTROLLED STUDY; ENZYME INHIBITION; INFLAMMATION; NITRATIVE STRESS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PULMONARY HYPERTENSION; RAT; VASCULAR REMODELING; ANIMAL; ANTAGONISTS AND INHIBITORS; BRONCHOPULMONARY DYSPLASIA; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; ENZYMOLOGY; HYPERTENSION, PULMONARY; LUNG; LUNG INJURY; METABOLISM; PATHOLOGY; SPRAGUE DAWLEY RAT;

AMINOCAPROATES; ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; ARGINASE; ARGININE; BLEOMYCIN; BORON COMPOUNDS; BRONCHOPULMONARY DYSPLASIA; COLLAGEN; DISEASE MODELS, ANIMAL; HYPERTENSION, PULMONARY; LUNG; LUNG INJURY; NITRIC OXIDE; RATS; RATS, SPRAGUE-DAWLEY; VASCULAR REMODELING;

EID: 84929046403     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00328.2014     Document Type: Article

References (64)

1. Alef MJ, Vallabhaneni R, Carchman E, Morris SM, Shiva S, Wang Y, Kelley EE, Tarpey MM, Gladwin MT, Tzeng E. Nitrite-generated NO circumvents dysregulated arginine/NOS signaling to protect against intimal hyperplasia in Sprague-Dawley rats. J Clin Invest 121: 1646-1656, 2011.
2. Baek KJ, Thiel B, Lucas S, Stuehr D. Macrophage nitric oxide synthase subunits. Purification, characterization, and role of prosthetic groups and substrate in regulating their association into a dimeric enzyme. J Biol Chem 268: 21120-21129, 1993.
3. Blom-Muilwijk M, Vriesendorp R, Veninga T, Hofstra W, Sleyfer D, Wieringa R, Konings A. Pulmonary toxicity after treatment with bleomycin alone or in combination with hyperoxia studies in the rat. Br J Anaesthesia 60: 91-97, 1988.
4. Chen B, Calvert AE, Cui H, Nelin LD. Hypoxia promotes human pulmonary artery smooth muscle cell proliferation through induction of arginase. Am J Physiol Lung Cell Mol Physiol 297: L1151-L1159, 2009.
5. Cho WK, Lee CM, Kang MJ, Huang Y, Giordano FJ, Lee PJ, Trow TK, Homer RJ, Sessa WC, Elias JA. IL-13 receptor α2-arginase 2 pathway mediates IL-13-induced pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 304: L112-L124, 2013.
6. Collaco JM, Romer LH, Stuart BD, Coulson JD, Everett AD, Lawson EE, Brenner JI, Brown AT, Nies MK, Sekar P. Frontiers in pulmonary hypertension in infants and children with bronchopulmonary dysplasia. Pediatr Pulmonol 47: 1042-1053, 2012.
7. Cutroneo KR, White SL, Phan SH, Ehrlich HP. Therapies for bleomycin induced lung fibrosis through regulation of TGF-β1 induced collagen gene expression. J Cell Physiol 211: 585-589, 2007.
8. Dick AS, Ivanovska J, Kantores C, Belcastro R, Keith Tanswell A, Jankov RP. Cyclic stretch stimulates nitric oxide synthase-1-dependent peroxynitrite formation by neonatal rat pulmonary artery smooth muscle. Free Rad Biol Med 61: 310-319, 2013.
9. Durante W. Role of arginase in vessel wall remodeling (Abstract). Front Immunol 4: 11, 2013.
10. Durante W, Johnson FK, Johnson RA. Arginase: critical regulator of nitric oxide synthesis and vascular funcation. Clin Exp Pharmacol Physiol 34: 906-91110.91111, 2007.
11. Durante W, Liao L, Reyna SV, Peyton KJ, Schafer AI. Physiological cyclic stretch directs L-arginine transport and metabolism to collagen synthesis in vascular smooth muscle. FASEB J 14: 1775-1783, 2000.
12. Durante W, Liao L, Reyna SV, Peyton KJ, Schafer AI. Transforming growth factor-β1 stimulates L-arginine transport and metabolism in vascular smooth muscle cells role in polyamine and collagen synthesis. Circulation 103: 1121-1127, 2001.
13. Elms S, Toque H, Rojas M, Xu Z, Caldwell R, Caldwell R. The role of arginase I in diabetes-induced retinal vascular dysfunction in mouse and rat models of diabetes. Diabetologia 56: 654-662, 2013.
14. Endo M, Oyadomari S, Terasaki Y, Takeya M, Suga M, Mori M, Gotoh T. Induction of arginase I and II in bleomycin-induced fibrosis of mouse lung. Am J Physiol Lung Cell Mol Physiol 285: L313-L321, 2003.
15. Förstermann U, Münzel T. Endothelial nitric oxide synthase in vascular disease from marvel to menace. Circulation 113: 1708-1714, 2006.
16. Förstermann U, Sessa WC. Nitric oxide synthases: regulation and function. Eur Heart J 33: 829-837, 2012.
17. Garg UC, Hassid A. Nitric oxide-generating vasodilators and 8-bromocyclic guanosine monophosphate inhibit mitogenesis and proliferation of cultured rat vascular smooth muscle cells (Abstract). J Clin Invest 83: 1774, 1989.
18. Gharaee-Kermani M, McCullumsmith RE, Charo IF, Kunkel SL, Phan SH. CC-chemokine receptor 2 required for bleomycin-induced pulmonary fibrosis. Cytokine 24: 266-276, 2003.
19. Hemmati AA, Rezaie A, Darabpour P. Preventive effects of pomegranate seed extract on bleomycin-induced pulmonary fibrosis in rat (Abstract). Jundishapur J Nat Pharmaceut Prod 8: 76, 2013.
20. Humbert M, Morrell NW, Archer SL, Stenmark KR, MacLean MR, Lang IM, Christman BW, Weir EK, Eickelberg O, Voelkel NF. Cellular and molecular pathobiology of pulmonary arterial hypertension. J Am Coll Cardiol 43: S13-S24, 2004.
21. Jaecklin T, Duerr J, Huang H, Rafii M, Bear CE, Ratjen F, Pencharz PB, Kavanagh BP, Mall MA, Grasemann H. Lung arginase expression and activity is increased in cystic fibrosis mouse models. J Appl Physiol 117: 284-288, 2014.
22. Jankov RP, Kantores C, Belcastro R, Yi S, Ridsdale RA, Post M, Tanswell AK. A role for platelet-derived growth factor b-receptor in a newborn rat model of endothelin-mediated pulmonary vascular remodeling. Am J Physiol Lung Cell Mol Physiol 288: L1162-L1170, 2005.
23. Jankov RP, Luo X, Demin P, Aslam R, Hannam V, Tanswell AK, Pace-Asciak CR. Hepoxilin analogs inhibit bleomycin-induced pulmonary fibrosis in the mouse. J Pharmacol Exp Ther 301: 435-440, 2002.
24. Jenkinson CP, Grody WW, Cederbaum SD. Comparative properties of arginases. Comp Biochem Physiol B Biochem Mol Biol 114: 107-132, 1996.
25. Jin Y, Calvert TJ, Chen B, Chicoine LG, Joshi M, Bauer JA, Liu Y, Nelin LD. Mice deficient in Mkp-1 develop more severe pulmonary hypertension and greater lung protein levels of arginase in response to chronic hypoxia. Am J Physiol Heart Circ Physiol 298: H1518-H1528, 2010.
26. Kantores C, McNamara PJ, Teixeira L, Engelberts D, Murthy P, Kavanagh BP, Jankov RP. Therapeutic hypercapnia prevents chronic hypoxia-induced pulmonary hypertension in the newborn rat. Am J Physiol Lung Cell Mol Physiol 291: L912-L922, 2006.
27. Kelley J, Newman R, Evans J. Bleomycin-induced pulmonary fibrosis in the rat. Prevention with an inhibitor of collagen synthesis. J Lab Clin Med 96: 954-964, 1980.
28. Kim JH, Bugaj LJ, Oh YJ, Bivalacqua TJ, Ryoo S, Soucy KG, Santhanam L, Webb A, Camara A, Sikka G. Arginase inhibition restores NOS coupling and reverses endothelial dysfunction and vascular stiffness in old rats. J Appl Physiol 107: 1249-1257, 2009.
29. Kitowska K, Zakrzewicz D, Königshoff M, Chrobak I, Grimminger F, Seeger W, Bulau P, Eickelberg O. Functional role and species-specific contribution of arginases in pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 294: L34-L45, 2008.
30. Kolpakov V, Gordon D, Kulik TJ. Nitric oxide-generating compounds inhibit total protein and collagen synthesis in cultured vascular smooth muscle cells. Circ Res 76: 305-309, 1995.
31. Lee AH, Dhaliwal R, Kantores C, Ivanovska J, Gosal K, McNamara PJ, Letarte M, Jankov RP. Rho-kinase inhibitor prevents bleomycininduced injury in neonatal rats independent of effects on lung inflammation. Am J Respir Cell Mol Biol 50: 61-73, 2014.
32. Liu H, Drew P, Gaugler AC, Cheng Y, Visner GA. Pirfenidone inhibits lung allograft fibrosis through L-arginineaArginase pathway. Am J Transplan 5: 1256-1263, 2005.
33. Masood A, Yi M, Lau M, Belcastro R, Shek S, Pan J, Kantores C, McNamara PJ, Kavanagh BP, Belik J, Jankov RP, Tanswell AK. Therapeutic effects of hypercapnia on chronic lung injury and vascular remodeling in neonatal rats. Am J Physiol Lung Cell Mol Physiol 297: L920-L930, 2009.
34. McCord J, Fridovich HI. The biology and pathology of oxygen radicals. Ann Intern Med 89: 122-127, 1978.
35. McNamara PJ, Murthy P, Kantores C, Teixeira L, Engelberts D, van Vliet T, Kavanagh BP, Jankov RP. Acute vasodilator effects of Rhokinase inhibitors in neonatal rats with pulmonary hypertension unresponsive to nitric oxide. Am J Physiol Lung Cell Mol Physiol 294: L205-L213, 2008.
36. Mehl A, Ghorbani P, Douda D, Huang H, Palaniyar N, Ratjen F, Grasemann H. Effect of arginase inhibition on pulmonary L-arginine metabolism in murine pseudomonas pneumonia. PLoS One 9: e90232, 2014.
37. Morris CR, Poljakovic M, Lavrisha L, Machado L, Kuypers FA, Morris SM Jr. Decreased arginine bioavailability and increase serum arginase activity in asthma. Am J Respir Crit Care Med 170: 148-153, 2004.
38. Morris JS. Recent advances in arginine metabolism: roles and regulation of the arginases. Biochem Pharmacol 157: 922-930, 2009.
39. Mourani PM, Abman SH. Pulmonary vascular disease in bronchopulmonary dysplasia: pulmonary hypertension and beyond. Curr Opin Pediatrics 25: 329-337, 2013.
40. Naura AS, Zerfaoui M, Kim H, Elmageed ZYA, Rodriguez PC, Hans CP, Ju J, Errami Y, Park J, Ochoa AC. Requirement for inducible nitric oxide synthase in chronic allergen exposure-induced pulmonary fibrosis but not inflammation. J Immunol 185: 3076-3085, 2010.
41. Niese KA, Chiaramonte MG, Ellies LG, Rothenberg ME, Zimmerman N. The cationic amino acid transporter 2 is induced in inflammatory lung models and regulates lung fibrosis (Abstract). Respir Res 11: 87, 2010.
42. Padela S, Cabacungan J, Shek S, Belcastro R, Yi M, Jankov RP, Tanswell AK. Hepatocyte growth factor is required for alveologenesis in the neonatal rat. Am J Respir Crit Care Med 172: 907-914, 2005.
43. Peng G, Ivanovska J, Kantores C, Van Vliet T, Engelberts D, Kavanagh BP, Enomoto M, Belik J, Jain A, McNamara PJ, Jankov RP. Sustained therapeutic hypercapnia attenuates pulmonary arterial Rhokinase activity and ameliorates chronic hypoxic pulmonary hypertension in juvenile rats. Am J Physiol Heart Circ Physiol 302: H2599-H2611, 2012.
44. Pera T, Zuidhof AB, Smit M, Menzen MH, Klein T, Flik G, Zaagsma J, Meurs H, Maarsingh H. Arginase inhibition prevents inflammation and remodeling in a Guinea pig model of chronic obstructive pulmonary disease. J Pharmacol Exp Ther 349: 229-238, 2014.
45. Pullamsetti SS, Savai R, Dumitrascu R, Dahal BK, Wilhelm J, Konigshoff M, Zakrzewicz D, Ghofrani HA, Weissmann N, Eickelberg O, Guenther A, Leiper J, Seeger W, Grimminger F, Schermuly RT. The role of dimethlyarginine dimethylaminohydrolase in idiopathic pulmonary fibrosis. Science Trans Med 15: 53-87, 2011.
46. Racké K, Warnken M. L-Arginine metabolic pathways. Open Nitric Oxide J 2: 9-19, 2010.
47. Santhanam L, Lim HK, Lim HK, Miriel V, Brown T, Patel M, Balanson S, Ryoo S, Anderson M, Irani K. Inducible NO synthasedependent S-nitrosylation and activation of arginase1 contribute to agerelated endothelial dysfunction. Circ Res 101: 692-702, 2007.
48. Sasaki A, Doi S, Mizutani S, Azuma H. Roles of accumulated endogenous nitric oxide synthase inhibitors, enhanced arginase activity, and attenuated nitric oxide synthase activity in endothelial cells for pulmonary hypertension in rats. Am J Physiol Lung Cell Mol Physiol 292: L1480- L1487, 2007.
49. Sato S, Kato S, Arisaka Y, Takahashi H, Takahashi K, Tomoike H. Changes in pulmonary hemodynamics during normoxia and hypoxia in awake rats treated with intratracheal bleomycin. Tohoku J Exp Med 169: 233-244, 1993.
50. Sewing ACP, Kantores C, Ivanovska J, Lee AH, Masood A, Jain A, McNamara PJ, Tanswell AK, Jankov RP. Therapeutic hypercapnia prevents bleomycin-induced pulmonary hypertension in neonatal rats by limiting macrophage-derived tumor necrosis factor-α. Am J Physiol Lung Cell Mol Physiol 303: L75-L87, 2012.
51. Shatanawi ARM, Iddings JA, Chandra S, Umapathy NS, et al. Angiotensin II-induced vascular endothelial dsyfuncation through RhoA/Rho kinase/pg38 mitogen-activated protein kinase/arginase pathway. Am J Physiol Cell Physiol 300: C1181-C1192, 2011.
52. Steppan J, Nyhan D, Berkowitz DE. Development of novel arginase inhibitors for therapy of endothelial dysfunction (Abstract). Front Immunol 4: 278, 2013.
53. Sugiura H, Ichinose M. Nitrative stress in inflammatory lung diseases. Nitric Oxide 25: 138-144, 2011.
54. Tabor CW, Tabor H. Polyamines. Ann Rev Biochem 53: 749-790, 1984.
55. Tomlinson C, Rafii M, Ball RO, Pencharz P. Arginine synthesis from enteral glutamine in healthy adults in the fed state. Am J Physiol Endocrinol Metab 301: E267-E273, 2011.
56. Tourneux P, Markham N, Seedorf G, Balasubramaniam V, Abman SH. Inhaled nitric oxide improves lung structure and pulmonary hypertension in a model of bleomycin-induced bronchopulmonary dysplasia in neonatal rats. Development of novel arginase inhibitors for therapy 297: L1103-L1111, 2009.
57. Tulis DA, Durante W, Peyton KJ, Chapman GB, Evans AJ, Schafer AI. YC-1, a benzyl indazole derivative, stimulates vascular cGMP and inhibits neointima formation. Biochem Biophys Res Commun 279: 646- 652, 2000.
58. Urschel KL, Rafii M, Pencharz PB, Ball RO. A multitracer stable isotope quantification of the effects of arginine intake on whole body arginine metabolism in neonatal piglets. Am J Physiol Endocrinol Metab 293: E811-E818, 2007.
59. Weissler JC. Idiopathic pulmonary fibrosis: cellular and molecular pathogenesis. Am J Med Sc 297: 91-104, 1989.
60. Williams BP JH Jr, Hosseini S, Tran H, Baldwin KM. Haemodynamic sequelae of pulmonary fibrosis following intratracheal belomycin in rats (Abstract). Cardiovasc Res 26: 8, 1992.
61. Wu G, Morris JS. Arginine metabolism: nitric oxide and beyond. Biochem J 336: 1-17, 1998.
62. Xu L, Hilliard B, Carmody RJ, Tsabary G, Shin H, Christianson DW, Chen YH. Arginase and autoimmune inflammation in the central nervous system. Immunology 110: 141-148, 2003.
63. Xu W, Kaneko FT, Zheng S, Comhair SA, Janocha AJ, Goggans T, Thunnissen FB, Farver C, Hazen SL, Jennings C. Increased arginase II and decreased NO synthesis in endothelial cells of patients with pulmonary arterial hypertension. FASEB J 18: 1746-1748, 2004.
64. Yan Zq Yokota T, Zhang W. Expression of inducible nitric oxide synthase inhibits platelet adhesion and restores blood flow in the injured artery. Circ Res 79: 38-44, 1996.