Dissection of experimental asthma with DNA microarray analysis identifies arginase in asthma pathogenesis

Journal of Clinical Investigation

Volumn 111, Issue 12, 2003, Pages 1863-1874

  Zimmermann, Nives ^a   King, Nina E ^a   Laporte, Johanne ^b   Yang, Ming ^c   Mishra, Anil ^a   Pope, Sam M ^a   Muntel, Emily E ^a   Witte, David P ^a   Pegg, Anthony A ^d   Foster, Paul S ^c   Hamid, Qutayba ^b   Rothenberg, Marc E ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b MCGILL UNIVERSITY   (Canada)

^c Biology and Environment   (Australia)

^d PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; AMINO ACID TRANSPORTER; ARGINASE; ARGINASE I; ARGINASE II; COLLAGEN; INTERLEUKIN 13; INTERLEUKIN 4; MESSENGER RNA; NITRIC OXIDE; POLYAMINE; PUTRESCINE; UNCLASSIFIED DRUG; ARGININE; CYTOKINE; ISOENZYME; STAT6 PROTEIN; STAT6 PROTEIN, HUMAN; STAT6 PROTEIN, MOUSE; TRANSACTIVATOR PROTEIN;

ADULT; ALLERGIC ASTHMA; ALLERGY; AMINO ACID METABOLISM; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTHMA; CONTROLLED STUDY; DNA MICROARRAY; DRUG TARGETING; ENZYME ACTIVITY; EXPERIMENTAL ASTHMA; FEMALE; GENE EXPRESSION PROFILING; GENE INDUCTION; GENETIC TRANSCRIPTION; HUMAN; HUMAN TISSUE; IN SITU HYBRIDIZATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROVOCATION TEST; RESPIRATORY TRACT INFLAMMATION; RESPIRATORY TRACT MUCOSA; ANIMAL; BAGG ALBINO MOUSE; DISEASE MODEL; ENZYMOLOGY; GENETIC MARKER; GENETICS; IMMUNOLOGY; LUNG; METABOLISM; MOUSE MUTANT; PHYSIOLOGY; TH2 CELL;

ANIMALS; ARGINASE; ARGININE; ASTHMA; CYTOKINES; DISEASE MODELS, ANIMAL; GENE EXPRESSION PROFILING; GENETIC MARKERS; HUMANS; ISOENZYMES; LUNG; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; NITRIC OXIDE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RNA, MESSENGER; STAT6 TRANSCRIPTION FACTOR; TH2 CELLS; TRANS-ACTIVATORS;

EID: 0042243556     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI200317912     Document Type: Article

References (58)

1. Holgate, S.T. 1999. The epidemic of allergy and asthma. Nature. 402:B2-B4.
2. Umetsu, D.T., McIntire, J.J., Akbari, O., Macaubas, C., and DeKruyff, R.H. 2002. Asthma: an epidemic of dysregulated immunity. Nat. Immunol. 3:715-720.
3. Broide, D.H. 2001. Molecular and cellular mechanisms of allergic disease. J. Allergy Clin. Immunol. 108:S65-S71.
4. Busse, W.W., and Lemanske, R.F., Jr. 2001. Asthma. Engl. J. Med. 344:350-362.
5. Lee, N.A., Gelfand, E.W., and Lee, J.J. 2001. Pulmonary T cells and eosinophils: coconspirators or independent triggers of allergic respiratory pathology? J. Allergy Clin. Immunol. 107:945-957.
6. Robinson, D.S., et al. 1992. Predominant TH2-like bronchoalveolar T-lymphocyte population in atopic asthma. N. Engl. J. Med. 326:298-304.
7. Drazen, J.M., Arm, J.P., and Austen, K.F. 1996. Sorting out the cytokines of asthma. J. Exp. Med. 183:1-5.
8. Ray, A., and Cohn, L. 1999. Th2 cells and GATA-3 in asthma: new insights into the regulation of airway inflammation. J. Clin. Invest. 104:985-993.
9. Bochner, B.S., Undem, B.J., and Lichtenstein, L.M. 1994. Immunological aspects of allergic asthma. Annu. Rev. Immunol. 12:295-335.
10. Wills-Karp, M. 2001. IL-12/IL-13 axis in allergic asthma. J. Allergy Clin. Immunol. 107:9-18.
11. Barnes, P.J. 2000. New directions in allergic diseases: mechanism-based anti-inflammatory therapies. J. Allergy Clin. Immunol. 106:5-16.
12. Morris, S.M., Jr. 2002. Regulation of enzymes of the urea cycle and arginine metabolism. Annu. Rev. Nutr. 22:87-105.
13. Mills, C.D. 2001. Macrophage arginine metabolism to ornithine/urea or nitric oxide/citrulline: a life or death issue. Crit. Rev. Immunol. 21:399-425.
14. Mishra, A., Weaver, T.E., Beck, D.C., and Rothenberg, M.E. 2001. Interleukin-5-mediated allergic airway inflammation inhibits the human surfactant protein C promoter in transgenic mice. J. Biol. Chem. 276:8453-8459.
15. Mehlhop, P.D., et al. 1997. Allergen-induced bronchial hyperreactivity and eosinophilic inflammation occur in the absence of IgE in a mouse model of asthma. Proc. Natl. Acad. Sci. U. S. A. 94:1344-1349.
16. Kurup, V.P., Seymour, B.W., Choi, H., and Coffman, R.L. 1994. Particulate Aspergillus fumigatus antigens elicit a TH2 response in BALB/c mice. J. Allergy Clin. Immunol. 93:1013-1020.
17. Zimmermann, N., et al. 2000. Murine eotaxin-2: a constitutive eosinophil chemokine induced by allergen challenge and IL-4 overexpression. J. Immunol. 165:5839-5846.
18. Rankin, J.A., et al. 1996. Phenotypic and physiologic characterization of transgenic mice expressing interleukin 4 in the lung: lymphocytic and eosinophilic inflammation without airway hyperreactivity. Proc. Natl. Acad. Sci. U. S. A. 93:7821-7825.
19. Shimoda, K., et al. 1996 Lack of IL-4-induced Th2 response and IgE class switching in mice with disrupted Stat6 gene. Nature. 380:630-633.
20. Pope, S.M., et al. 2001. IL-13 induces eosinophil recruitment into the lung by an IL-5- and eotaxin-dependent mechanism. J. Allergy Clin. Immunol. 108:594-601.
21. Yang, M., et al. 2001. Interleukin-13 mediates airways hyperreactivity through the IL-4 receptor-alpha chain and STAT-6 independently of IL-5 and eotaxin. Am. J. Respir. Cell Mol. Biol. 25:522-530.
22. Marthews, A.N., et al. 1998. Eotaxin is required for the baseline level of tissue eosinophils. Proc. Natl. Acad. Sci. U. S. A. 95:6273-6278.
23. Wei, L.H., Jacobs, A.T., Morris, S.M., Jr., and Ignatto, L.J. 2000. IL-4 and IL-13 upregulate arginase I expression by cAMP and JAK/STAT6 pathways in vascular smooth muscle cells. Am. J. Physiol. Cell Physiol. 279:C248-C256.
24. Wei, L.H., Wu, G., Morris, S.M., Jr., and Ignatto, L.J. 2001. Elevated arginase I expression in rat aortic smooth muscle cells increases cell proliferation. Proc. Natl. Acad. Sci. U. S. A. 98:9260-9264.
25. Li, H., et al. 2002. Activities of arginase I and II are limiting for endothelial cell proliferation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 282:R64-R69.
26. Lopatin, A.N., Shantz, L.M., Mackintosh, C.A., Nichols, C.G., and Pegg, A.E. 2000. Modulation of potassium channels in the hearts of transgenic and mutant mice with altered polyamine biosynthesis. J. Mol. Cell Cardiol. 32:2007-2024.
27. American Thoracic Society. 1987. Standards for the diagnosis and care of patients with chronic obstructive pulmonary disease (COPD) and asthma. Am. Rev. Respir. Dis. 136:225-244.
28. Olivenstein, R., Taha, R., Minshall, E-M., and Hamid, Q.A. 1999. IL-4 and IL-5 mRNA expression in induced sputum of asthmatic subjects: comparison with bronchial wash. J. Allergy Clin. Immunol. 103:238-245.
29. Hamid, Q. 1997. Immunohistochemistry. In Allergy and allergic disease. A.B. Kay, editor. Blackwell Science Ltd. London, United Kingdom. 775-778.
30. Rothenberg, M.E., MacLean, J.A., Pearlman, E., Luster, A.D., and Leder, P. 1997. Targeted disruption of the chemokine eotaxin partially reduces antigen-induced tissue eosinophilia. J. Exp. Med. 185:785-790.
31. Kurup, V.P., Mauze, S., Choi, H., Seymour, B.W., and Coffman, R.L. 1992. A murine model of allergic bronchopulmonary aspergillosis with elevated eosinophils and IgE. J. Immunol. 148:3783-3788.
32. Iyer, R., et al. 1998 The human arginases and arginase deficiency. J. Inherit. Metab. Dis. 21:86-100.
33. Elias, J.A., Zhu, Z., Chupp, G., and Homer, R.J. 1999. Airway remodeling in asthma. J. Clin. Invest. 104:1001-1006.
34. Eisenbarth, S.C., et al. 2002. Lipopolysaccharide-enhanced, toll-like receptor 4-dependent T helper cell type 2 responses to inhaled antigen. J. Exp. Med. 196:1640-1651.
35. Esch, F., et al. 1998. Purification of a multipotent antideath activity from bovine liver and its identification as arginase: nitric oxide-independent inhibition of neuronal apoptosis. J. Neurosci. 18:4083-4095.
36. Hoet, P.H., and Nemery, B. 2000. Polyamines in the lung: polyamine uptake and polyamine-linked pathological or toxicological conditions. Am. J. Physiol. Lung Cell Mol. Physiol. 278:L417-L433.
37. Kharitonov, S.A., and Barnes, P.J. 2000. Clinical aspects of exhaled nitric oxide. Eur. Respir. J. 16:781-792.
38. Hunt, J., and Gaston, B. 2000. Airway nitrogen oxide measurements in asthma and other pediatric respiratory diseases. J. Pediatr. 137:14-20.
39. Munder, M., et al. 1999. Th1/Th2-regulated expression of arginase isoforms in murine macrophages and dendritic cells. J. Immunol. 163:3771-3777.
40. Ihle, J.N. 2001. The Stat family in cytokine signaling. Curr. Opin. Cell Biol. 13:211-217.
41. Rutschman, R., et al. 2001. Cutting edge: Star6-dependent substrate depletion regulates nitric oxide production. J. Immunol. 166:2173-2177.
42. Grunig, G., et al. 1998. Requirement for IL-13 independently of IL-4 in experimental asthma. Science. 282:2261-2263.
43. Hesse, M., et al. 2001. Differential regulation of nitric oxide synthase-2 and arginase-1 by type 1/type 2 cytokines in vivo: granulomatous pathology is shaped by the pattern of L-arginine metabolism. J. Immunol. 167:6533-6544.
44. Guo, F.H., et al. 2000. Molecular mechanisms of increased nitric oxide (NO) in asthma: evidence for transcriptional and post-translational regulation of NO synthesis. J. Immunol. 164:5970-5980.
45. MacPherson, J.C., et al. 2001. Eosinophils are a major source of nitric oxide-derived oxidants in severe asthma: characterization of pathways available to eosinophils for generating reactive nitrogen species. J. Immunol. 166:5763-5772.
46. Nijkamp, F.P., van der Linde, H.J., and Folkerts, G. 1993. Nitric oxide synthesis inhibitors induce airway hyperresponsiveness in the guinea pig in vivo and in vitro. Role of the epithelium. Am. Rev. Respir. Dis. 148:727-734.
47. De Boer, J., et al. 1996. Deficiency of nitric oxide in allergen-induced airway hyperreactivity to contractile agonists after the early asthmatic reaction: an ex vivo study. Br. J. Pharmacol. 119:1109-1116.
48. Schuiling, M., et al. 1998. Role of nitric oxide in the development and partial reversal of allergen-induced airway hyperreactivity in conscious, unrestrained guinea-pigs. Br. J. Pharmacol. 123:1450-1456.
49. Taylor, D.A., McGrath, J.L., Orr, L.M., Barnes, P.J., and O'Connor, B.J. 1998. Effect of endogenous nitric oxide inhibition on airway responsiveness to histamine and adenosine-5′-monophosphate in asthma. Thorax. 53:483-489.
50. Schuiling, M., Meurs, H., Zuidhof, A.B., Venema, N., and Zaagsma, J. 1998. Dual action of iNOS-derived nitric oxide in allergen-induced airway hyperreactivicy in conscious, unrestrained guinea pigs. Am. J. Respir. Crit. Care Med. 158:1442-1449.
51. Hammermann, R., et al. 1999. Cationic proteins inhibit L-arginine uptake in rat alveolar macrophages and tracheal epithelial cells. Implications for nitric oxide synthesis. Am. J. Respir. Cell Mol. Biol. 21:155-162.
52. Kurosawa, M., Shimizu, Y., Tsukagoshi, H., and Ueki, M. 1992. Elevated levels of peripheral-blood, naturally occurring aliphatic polyamines in bronchial asthmatic patients with active symptoms. Allergy. 47:638-643.
53. Nilsson, B.O., and Hellstrand, P. 1993. Effects of polyamines on intracellular calcium and mechanical activity in smooth muscle of guinea-pig taenia coli. Acta. Physiol. Scand. 148:37-43.
54. Sward, K., Pato, M.D., Nilsson, B.O., Nordstrom, I., and Hellstrand, P. 1995. Polyamines inhibit myosin phosphatase and increase LC20 phosphorylation and force in smooth muscle. Am. J. Physiol. 269:C563-C571.
55. Thomas, T., and Thomas T.J. 2001. Polyamines in cell growth and cell death: molecular mechanisms and therapeutic applications. Cell Mol. Life Sci. 58:244-258.
56. Ma, L., Wang, W.P., Chow, J.Y., Lam, S.K., and Cho, C.H. 2000. The role of polyamines in gastric mucus synthesis inhibited by cigarette smoke or its extract. Gut. 47:170-177.
57. Albina, J.E., Abate, J.A., and Mastrofrancesco, B. 1993. Role of ornithine as a proline precursor in healing wounds. J. Surg. Res. 55:97-102.
58. Kershenobich, D., Fierro, F.J., and Rojkind, M. 1970. The relationship between the free pool of proline and collagen content in human liver cirrhosis. J. Clin. Invest. 49:2246-2249.