Ablation of Arg1 in hematopoietic cells improves respiratory function of lung parenchyma, but not that of larger airways or inflammation in asthmatic mice

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 305, Issue 5, 2013, Pages

  Cloots, Roy H E ^a   Sankaranarayanan, Selvakumari ^a   de Theije, Chiel C ^a   Poynter, Matthew E ^c   Terwindt, Els ^a   van Dijk, Paul ^a   Hakvoort, Theodorus B M ^b   Lamers, Wouter H ^a,b   Köhler, S Eleonore ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

Author keywords

Airway hyperresponsiveness; Arginine; Inflammation

Indexed keywords

ARGINASE 1; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 5; MUCIN 5AC; NITRIC OXIDE SYNTHASE; TUMOR NECROSIS FACTOR ALPHA;

ALLERGIC ASTHMA; ALLERGIC REACTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTHMA; CONTROLLED STUDY; CYTOKINE RELEASE; FEMALE; GENE EXPRESSION; HEMATOPOIETIC CELL; HISTOLOGY; IMMUNOHISTOCHEMISTRY; LUNG PARENCHYMA; MALE; MOUSE; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY FUNCTION; RESPIRATORY TRACT ALLERGY;

AIRWAY HYPERRESPONSIVENESS; ARGININE; INFLAMMATION;

AIRWAY RESISTANCE; ANIMALS; ARGINASE; ASTHMA; BLOTTING, WESTERN; BRONCHIAL HYPERREACTIVITY; BRONCHOCONSTRICTOR AGENTS; CHEMOKINES; CYTOKINES; DENDRITIC CELLS; FEMALE; GENE EXPRESSION PROFILING; HYPERSENSITIVITY; IMMUNOENZYME TECHNIQUES; LUNG; MACROPHAGES; MALE; METHACHOLINE CHLORIDE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOID CELLS; OVALBUMIN; PNEUMONIA; REAL-TIME POLYMERASE CHAIN REACTION; RESPIRATORY SYSTEM; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 84883400987     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00341.2012     Document Type: Article

References (60)

1. Bates JH, Rincon M, Irvin CG. Animal models of asthma. Am J Physiol Lung Cell Mol Physiol 297: L401-L410, 2009.
2. Benson RC, Hardy KA, Morris CR. Arginase and arginine dysregulation in asthma. J Allergy (Cairo) 2011: 736319, 2011.
3. Bousquet J, Jeffery PK, Busse WW, Johnson M, Vignola AM. Asthma. From bronchoconstriction to airways inflammation and remodeling. Am J Respir Crit Care Med 161: 1720-1745, 2000.
4. Bratt JM, Franzi LM, Linderholm AL, Last MS, Kenyon NJ, Last JA. Arginase enzymes in isolated airways from normal and nitric oxide synthase 2-knockout mice exposed to ovalbumin. Toxicol Appl Pharmacol 234: 273-280, 2009.
5. Bratt JM, Franzi LM, Linderholm AL, O'Roark EM, Kenyon NJ, Last JA. Arginase inhibition in airways from normal and nitric oxide synthase 2-knockout mice exposed to ovalbumin. Toxicol Appl Pharmacol 242: 1-8, 2010.
6. Busse WW, Lemanske RF Jr. Asthma. N Engl J Med 344: 350-362, 2001.
7. Ckless K, Lampert A, Reiss J, Kasahara D, Poynter ME, Irvin CG, Lundblad LK, Norton R, van der Vliet A, Janssen-Heininger YM. Inhibition of arginase activity enhances inflammation in mice with allergic airway disease, in association with increases in protein S-nitrosylation and tyrosine nitration. J Immunol 181: 4255-4264, 2008.
8. Clark A. Post-transcriptional regulation of pro-inflammatory gene expression. Arthritis Res 2: 172-174, 2000.
9. Clausen BE, Burkhardt C, Reith W, Renkawitz R, Forster I. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res 8: 265-277, 1999.
10. Deshane J, Zmijewski JW, Luther R, Gaggar A, Deshane R, Lai JF, Xu X, Spell M, Estell K, Weaver CT, Abraham E, Schwiebert LM, Chaplin DD. Free radical-producing myeloid-derived regulatory cells: potent activators and suppressors of lung inflammation and airway hyperresponsiveness. Mucosal Immunol 4: 503-518, 2011.
11. Dymecki SM. Flp recombinase promotes site-specific DNA recombination in embryonic stem cells and transgenic mice. Proc Natl Acad Sci USA 93: 6191-6196, 1996.
12. Feletou M, Lonchampt M, Coge F, Galizzi JP, Bassoullet C, Merial C, Robineau P, Boutin JA, Huang PL, Vanhoutte PM, Canet E. Regulation of murine airway responsiveness by endothelial nitric oxide synthase. Am J Physiol Lung Cell Mol Physiol 281: L258-L267, 2001.
13. Fredberg JJ, Stamenovic D. On the imperfect elasticity of lung tissue. J Appl Physiol 67: 2408-2419, 1989.
14. Garcia-Zepeda EA, Rothenberg ME, Ownbey RT, Celestin J, Leder P, Luster AD. Human eotaxin is a specific chemoattractant for eosinophil cells and provides a new mechanism to explain tissue eosinophilia. Nat Med 2: 449-456, 1996.
15. Gordy C, Pua H, Sempowski GD, He YW. Regulation of steady-state neutrophil homeostasis by macrophages. Blood 117: 618-629, 2011.
16. Hamada K, Sasaki T, Koni PA, Natsui M, Kishimoto H, Sasaki J, Yajima N, Horie Y, Hasegawa G, Naito M, Miyazaki J, Suda T, Itoh H, Nakao K, Mak TW, Nakano T, Suzuki A. The PTEN/PI3K pathway governs normal vascular development and tumor angiogenesis. Genes Dev 19: 2054-2065, 2005.
17. Hantos Z, Daroczy B, Suki B, Nagy S. Low-frequency respiratory mechanical impedance in the rat. J Appl Physiol 63: 36-43, 1987.
18. Hasaneen NA, Foda HD, Said SI. Nitric oxide and vasoactive intestinal peptide as co-transmitters of airway smooth-muscle relaxation: analysis in neuronal nitric oxide synthase knockout mice. Chest 124: 1067-1072, 2003.
19. Hjoberg J, Shore S, Kobzik L, Okinaga S, Hallock A, Vallone J, Subramaniam V, De Sanctis GT, Elias JA, Drazen JM, Silverman ES. Expression of nitric oxide synthase-2 in the lungs decreases airway resistance and responsiveness. J Appl Physiol 97: 249-259, 2004.
20. Iijima H, Tulic MK, Duguet A, Shan J, Carbonara P, Hamid Q, Eidelman DH. NOS 1 is required for allergen-induced expression of NOS 2 in mice. Int Arch Allergy Immunol 138: 40-50, 2005.
21. Ilies M, Di Costanzo L, North ML, Scott JA, Christianson DW. 2-Aminoimidazole amino acids as inhibitors of the binuclear manganese metalloenzyme human arginase I. J Med Chem 53: 4266-4276, 2010.
22. Iyer RK, Yoo PK, Kern RM, Rozengurt N, Tsoa R, O'Brien WE, Yu H, Grody WW, Cederbaum SD. Mouse model for human arginase deficiency. Mol Cell Biol 22: 4491-4498, 2002.
23. Jakubzick C, Bogunovic M, Bonito AJ, Kuan EL, Merad M, Randolph GJ. Lymph-migrating, tissue-derived dendritic cells are minor constituents within steady-state lymph nodes. J Exp Med 205: 2839-2850, 2008.
24. Kenyon NJ, Bratt JM, Linderholm AL, Last MS, Last JA. Arginases I and II in lungs of ovalbumin-sensitized mice exposed to ovalbumin: sources and consequences. Toxicol Appl Pharmacol 230: 269-275, 2008.
25. Kisanuki YY, Hammer RE, Miyazaki J, Williams SC, Richardson JA, Yanagisawa M. Tie2-Cre transgenic mice: a new model for endothelial cell-lineage analysis in vivo. Dev Biol 230: 230-242, 2001.
26. Koarai A, Ichinose M, Sugiura H, Yamagata S, Hattori T, Shirato K. Allergic airway hyperresponsiveness and eosinophil infiltration is reduced by a selective iNOS inhibitor, 1400W, in mice. Pulm Pharmacol Ther 13: 267-275, 2000.
27. Koni PA, Joshi SK, Temann UA, Olson D, Burkly L, Flavell RA. Conditional vascular cell adhesion molecule 1 deletion in mice: impaired lymphocyte migration to bone marrow. J Exp Med 193: 741-754, 2001.
28. Kumar RK, Herbert C, Foster PS. The "classical" ovalbumin challenge model of asthma in mice. Curr Drug Targets 9: 485-494, 2008.
29. Lee JJ, McGarry MP, Farmer SC, Denzler KL, Larson KA, Carrigan PE, Brenneise IE, Horton MA, Haczku A, Gelfand EW, Leikauf GD, Lee NA. Interleukin-5 expression in the lung epithelium of transgenic mice leads to pulmonary changes pathognomonic of asthma. J Exp Med 185: 2143-2156, 1997.
30. Li H, Romieu I, Sienra-Monge JJ, Ramirez-Aguilar M, Del Rio-Navarro BE, Kistner EO, Gjessing HK, del Carmen Lara-Sanchez I, Chiu GY, London SJ. Genetic polymorphisms in arginase I and II and childhood asthma and atopy. J Allergy Clin Immunol 117: 119-126, 2006.
31. Long AJ, Sypek JP, Askew R, Fish SC, Mason LE, Williams CM, Goldman SJ. Gob-5 contributes to goblet cell hyperplasia and modulates pulmonary tissue inflammation. Am J Respir Cell Mol Biol 35: 357-365, 2006.
32. Lundblad LK, Rinaldi LM, Poynter ME, Riesenfeld EP, Wu M, Aimi S, Barone LM, Bates JH, Irvin CG. Detrimental effects of albuterol on airway responsiveness requires airway inflammation and is independent of betareceptor affinity in murine models of asthma. Respir Res 12: 27, 2011.
33. Lundblad LK, Thompson-Figueroa J, Allen GB, Rinaldi L, Norton RJ, Irvin CG, Bates JH. Airway hyperresponsiveness in allergically inflamed mice: the role of airway closure. Am J Respir Crit Care Med 175: 768-774, 2007.
34. Maarsingh H, Bossenga BE, Bos IS, Volders HH, Zaagsma J, Meurs H. L-Arginine deficiency causes airway hyperresponsiveness after the late asthmatic reaction. Eur Respir J 34: 191-199, 2009.
35. Maarsingh H, Zaagsma J, Meurs H. Arginase: a key enzyme in the pathophysiology of allergic asthma opening novel therapeutic perspectives. Br J Pharmacol 158: 652-664, 2009.
36. Maarsingh H, Zuidhof AB, Bos IS, van Duin M, Boucher JL, Zaagsma J, Meurs H. Arginase inhibition protects against allergen-induced airway obstruction, hyperresponsiveness, and inflammation. Am J Respir Crit Care Med 178: 565-573, 2008.
37. Mattes J, Yang M, Siqueira A, Clark K, MacKenzie J, McKenzie AN, Webb DC, Matthaei KI, Foster PS. IL-13 induces airways hyperreactivity independently of the IL-4R alpha chain in the allergic lung. J Immunol 167: 1683-1692, 2001.
38. Meurs H, Gosens R, Zaagsma J. Airway hyperresponsiveness in asthma: lessons from in vitro model systems and animal models. Eur Respir J 32: 487-502, 2008.
39. Munder M. Arginase: an emerging key player in the mammalian immune system. Br J Pharmacol 158: 638-651, 2009.
40. Nakanishi A, Morita S, Iwashita H, Sagiya Y, Ashida Y, Shirafuji H, Fujisawa Y, Nishimura O, Fujino M. Role of gob-5 in mucus overproduction and airway hyperresponsiveness in asthma. Proc Natl Acad Sci USA 98: 5175-5180, 2001.
41. Niese KA, Collier AR, Hajek AR, Cederbaum SD, O'Brien WE, Wills-Karp M, Rothenberg ME, Zimmermann N. Bone marrow cell derived arginase I is the major source of allergen-induced lung arginase but is not required for airway hyperresponsiveness, remodeling and lung inflammatory responses in mice. BMC Immunol 10: 33, 2009.
42. North ML, Khanna N, Marsden PA, Grasemann H, Scott JA. Functionally important role for arginase 1 in the airway hyperresponsiveness of asthma. Am J Physiol Lung Cell Mol Physiol 296: L911-L920, 2009.
43. Poynter ME, Cloots R, van Woerkom T, Butnor KJ, Vacek P, Taatjes DJ, Irvin CG, Janssen-Heininger YM. NF-kappa B activation in airways modulates allergic inflammation but not hyperresponsiveness. J Immunol 173: 7003-7009, 2004.
44. Redington AE. Modulation of nitric oxide pathways: therapeutic potential in asthma and chronic obstructive pulmonary disease. Eur J Pharmacol 533: 263-276, 2006.
45. Riesenfeld E, Allen GB, Bates JH, Poynter ME, Wu M, Aimiand S, Lundblad LK. The temporal evolution of airways hyperresponsiveness and inflammation. J Allergy Ther 1: 1-7, 2012.
46. Ruijter JM, Ramakers C, Hoogaars WM, Karlen Y, Bakker O, van den Hoff MJ, Moorman AF. Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res 37: e45, 2009.
47. Sarpong SB, Zhang LY, Kleeberger SR. A novel mouse model of experimental asthma. Int Arch Allergy Immunol 132: 346-354, 2003.
48. Sauer B, Henderson N. Site-specific DNA recombination in mammalian cells by the Cre recombinase of bacteriophage P1. Proc Natl Acad Sci USA 85: 5166-5170, 1988.
49. Schlaeger TM, Mikkola HK, Gekas C, Helgadottir HB, Orkin SH. Tie2Cre-mediated gene ablation defines the stem-cell leukemia gene (SCL/tal1)-dependent window during hematopoietic stem-cell development. Blood 105: 3871-3874, 2005.
50. Schwenk F, Baron U, Rajewsky K. A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells. Nucleic Acids Res 23: 5080-5081, 1995.
51. Shum BO, Rolph MS, Sewell WA. Mechanisms in allergic airway inflammation-lessons from studies in the mouse. Expert Rev Mol Med 10: e15, 2008.
52. Takemoto K, Ogino K, Shibamori M, Gondo T, Hitomi Y, Takigawa T, Wang DH, Takaki J, Ichimura H, Fujikura Y, Ishiyama H. Transiently, paralleled upregulation of arginase and nitric oxide synthase and the effect of both enzymes on the pathology of asthma. Am J Physiol Lung Cell Mol Physiol 293: L1419-L1426, 2007.
53. Ten Broeke R, De Crom R, Van Haperen R, Verweij V, Leusink-Muis T, Van Ark I, De Clerck F, Nijkamp FP, Folkerts G. Overexpression of endothelial nitric oxide synthase suppresses features of allergic asthma in mice. Respir Res 7: 58, 2006.
54. Van den Bossche J, Lamers WH, Koehler ES, Geuns JM, Alhonen L, Uimari A, Pirnes-Karhu S, Van Overmeire E, Morias Y, Brys L, Vereecke L, De Baetselier P, Van Ginderachter JA. Pivotal Advance: Arginase-1-independent polyamine production stimulates the expression of IL-4-induced alternatively activated macrophage markers while inhibiting LPSinduced expression of inflammatory genes. J Leukoc Biol 91: 685-699, 2012.
55. van Eijk HM, Rooyakkers DR, Deutz NE. Rapid routine determination of amino acids in plasma by high-performance liquid chromatography with a 2-3 microns Spherisorb ODS II column. J Chromatogr 620: 143-148, 1993.
56. Wagers S, Lundblad LK, Ekman M, Irvin CG, Bates JH. The allergic mouse model of asthma: normal smooth muscle in an abnormal lung? J Appl Physiol 96: 2019-2027, 2004.
57. Wu G, Morris SM Jr. Arginine metabolism: nitric oxide and beyond. Biochem J 336: 1-17, 1998.
58. Yang M, Rangasamy D, Matthaei KI, Frew AJ, Zimmermann N, Mahalingam S, Webb DC, Tremethick DJ, Thompson PJ, Hogan SP, Rothenberg ME, Cowden WB, Foster PS. Inhibition of arginase I activity by RNA interference attenuates IL-13-induced airways hyperresponsiveness. J Immunol 177: 5595-5603, 2006.
59. Zhang Z, Zhang F, An P, Guo X, Shen Y, Tao Y, Wu Q, Zhang Y, Yu Y, Ning B, Nie G, Knutson MD, Anderson GJ, Wang F. Ferroportin1 deficiency in mouse macrophages impairs iron homeostasis and inflammatory responses. Blood 118: 1912-1922, 2011.
60. Zimmermann N, King NE, Laporte J, Yang M, Mishra A, Pope SM, Muntel EE, Witte DP, Pegg AA, Foster PS, Hamid Q, Rothenberg ME. Dissection of experimental asthma with DNA microarray analysis identifies arginase in asthma pathogenesis. J Clin Invest 111: 1863-1874, 2003.