Resolution of experimental lung injury by monocyte-derived inducible nitric oxide synthase

Journal of Immunology

Volumn 189, Issue 5, 2012, Pages 2234-2245

  D'Alessio, Franco R ^a   Tsushima, Kenji ^a   Aggarwal, Neil R ^a   Mock, Jason R ^a   Eto, Yoshiki ^a   Garibaldi, Brian T ^a   Files, Daniel C ^a   Avalos, Claudia R ^a   Rodriguez, Jackie V ^a   Waickman, Adam T ^a   Reddy, Sekhar P ^a   Pearse, David B ^a   Sidhaye, Venkataramana K ^a   Hassoun, Paul M ^a   Crow, Michael T ^a   King, Landon S ^a  

^a JOHNS HOPKINS ASTHMA AND ALLERGY CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; CD86 ANTIGEN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; LIPOPOLYSACCHARIDE; MACROPHAGE INFLAMMATORY PROTEIN 2; NITRATE; NITRITE; REACTIVE OXYGEN METABOLITE; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA;

ACUTE LUNG INJURY; ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CELL TRANSFER; CONTROLLED STUDY; CONVALESCENCE; EPITHELIUM CELL; IMMUNOMODULATION; LUNG ALVEOLUS MACROPHAGE; MALE; MONOCYTE; MONOCYTE TRANSFER; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SURVIVAL RATE; TISSUE REPAIR; TREATMENT OUTCOME; UPREGULATION; VIRAL GENE DELIVERY SYSTEM; WILD TYPE;

ACUTE LUNG INJURY; ANIMALS; ANTIGENS, CD86; CELL LINE; CELL LINE, TRANSFORMED; DISEASE MODELS, ANIMAL; INFLAMMATION MEDIATORS; MACROPHAGES, PERITONEAL; MALE; MICE; MICE, CONGENIC; MICE, INBRED C57BL; MICE, KNOCKOUT; MONOCYTES; NITRIC OXIDE SYNTHASE TYPE II;

EID: 84865427563     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1102606     Document Type: Article

References (69)

1. Rubenfeld, G. D., E. Caldwell, E. Peabody, J. Weaver, D. P. Martin, M. Neff, E. J. Stern, and L. D. Hudson. 2005. Incidence and outcomes of acute lung injury. N. Engl. J. Med. 353: 1685-1693.
2. The Acute Respiratory Distress Syndrome Network. 2000. Ventilation with lower tidal volumes as compared with traditional tidal volumes for acute lung injury and the acute respiratory distress syndrome. N. Engl. J. Med. 342: 1301-1308.
3. Ware, L. B., and M. A. Matthay. 2000. The acute respiratory distress syndrome. N. Engl. J. Med. 342: 1334-1349.
4. Bachofen, M., and E. R. Weibel. 1982. Structural alterations of lung parenchyma in the adult respiratory distress syndrome. Clin. Chest Med. 3: 35-56.
5. Anderson, W. R., and K. Thielen. 1992. Correlative study of adult respiratory distress syndrome by light, scanning, and transmission electron microscopy. Ultrastruct. Pathol. 16: 615-628.
6. Meduri, G. U., M. Eltorky, and H. T. Winer-Muram. 1995. The fibroproliferative phase of late adult respiratory distress syndrome. Semin. Respir. Infect. 10: 154-175.
7. Martin, C., L. Papazian, M. J. Payan, P. Saux, and F. Gouin. 1995. Pulmonary fibrosis correlates with outcome in adult respiratory distress syndrome. A study in mechanically ventilated patients. Chest 107: 196-200.
8. Baron, R. M., I. M. Carvajal, X. Liu, R. O. Okabe, L. E. Fredenburgh, A. A. Macias, Y. H. Chen, K. Ejima, M. D. Layne, and M. A. Perrella. 2004. Reduction of nitric oxide synthase 2 expression by distamycin A improves survival from endotoxemia. J. Immunol. 173: 4147-4153.
9. Haddad, I. Y., J. P. Crow, P. Hu, Y. Ye, J. Beckman, and S. Matalon. 1994. Concurrent generation of nitric oxide and superoxide damages surfactant protein A. Am. J. Physiol. 267: L242-L249.
10. Kristof, A. S., P. Goldberg, V. Laubach, and S. N. Hussain. 1998. Role of inducible nitric oxide synthase in endotoxin-induced acute lung injury. Am. J. Respir. Crit. Care Med. 158: 1883-1889.
11. Kooy, N. W., J. A. Royall, Y. Z. Ye, D. R. Kelly, and J. S. Beckman. 1995. Evidence for in vivo peroxynitrite production in human acute lung injury. Am. J. Respir. Crit. Care Med. 151: 1250-1254.
12. Okamoto, T., K. Gohil, E. I. Finkelstein, P. Bove, T. Akaike, and A. van der Vliet. 2004. Multiple contributing roles for NOS2 in LPS-induced acute airway inflammation in mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 286: L198-L209.
13. Farley, K. S., L. F. Wang, H. M. Razavi, C. Law, M. Rohan, D. G. McCormack, and S. Mehta. 2006. Effects of macrophage inducible nitric oxide synthase in murine septic lung injury. Am. J. Physiol. Lung Cell. Mol. Physiol. 290: L1164-L1172.
14. Moncada, S., R. M. Palmer, and E. A. Higgs. 1991. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol. Rev. 43: 109-142.
15. Nathan, C., and Q. W. Xie. 1994. Nitric oxide synthases: roles, tolls, and controls. Cell 78: 915-918.
16. van der Vliet, A., and C. E. Cross. 2000. Oxidants, nitrosants, and the lung. Am. J. Med. 109: 398-421.
17. Kobzik, L., D. S. Bredt, C. J. Lowenstein, J. Drazen, B. Gaston, D. Sugarbaker, and J. S. Stamler. 1993. Nitric oxide synthase in human and rat lung: immunocytochemical and histochemical localization. Am. J. Respir. Cell Mol. Biol. 9: 371-377.
18. Hotchkiss, R. S., and I. E. Karl. 2003. The pathophysiology and treatment of sepsis. N. Engl. J. Med. 348: 138-150.
19. Razavi, H. M., R. Werhun, J. A. Scott, S. Weicker, F. Wang, D. G. McCormack, and S. Mehta. 2002. Effects of inhaled nitric oxide in a mouse model of sepsis-induced acute lung injury. Crit. Care Med. 30: 868-873.
20. Wong, J. M., and T. R. Billiar. 1995. Regulation and function of inducible nitric oxide synthase during sepsis and acute inflammation. Adv. Pharmacol. 34: 155-170.
21. Wei, X. Q., I. G. Charles, A. Smith, J. Ure, G. J. Feng, F. P. Huang, D. Xu, W. Muller, S. Moncada, and F. Y. Liew. 1995. Altered immune responses in mice lacking inducible nitric oxide synthase. Nature 375: 408-411.
22. MacMicking, J. D., C. Nathan, G. Hom, N. Chartrain, D. S. Fletcher, M. Trumbauer, K. Stevens, Q. W. Xie, K. Sokol, N. Hutchinson, et al. 1995. Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase. Cell 81: 641-650.
23. Laubach, V. E., E. G. Shesely, O. Smithies, and P. A. Sherman. 1995. Mice lacking inducible nitric oxide synthase are not resistant to lipopolysaccharide-induced death. Proc. Natl. Acad. Sci. USA 92: 10688-10692.
24. Bogdan, C. 2001. Nitric oxide and the immune response. Nat. Immunol. 2: 907-916.
25. Nathan, C., and M. U. Shiloh. 2000. Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc. Natl. Acad. Sci. USA 97: 8841-8848.
26. Bogdan, C., M. Röllinghoff, and A. Diefenbach. 2000. The role of nitric oxide in innate immunity. Immunol. Rev. 173: 17-26.
27. Bogdan, C., M. Röllinghoff, and A. Diefenbach. 2000. Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity. Curr. Opin. Immunol. 12: 64-76.
28. Diefenbach, A., H. Schindler, N. Donhauser, E. Lorenz, T. Laskay, J. MacMicking, M. Röllinghoff, I. Gresser, and C. Bogdan. 1998. Type 1 interferon (IFNalpha/beta) and type 2 nitric oxide synthase regulate the innate immune response to a protozoan parasite. Immunity 8: 77-87.
29. Spiecker, M., H. Darius, K. Kaboth, F. Hübner, and J. K. Liao. 1998. Differential regulation of endothelial cell adhesion molecule expression by nitric oxide donors and antioxidants. J. Leukoc. Biol. 63: 732-739.
30. Bobé, P., K. Benihoud, D. Grandjon, P. Opolon, L. L. Pritchard, and R. Huchet. 1999. Nitric oxide mediation of active immunosuppression associated with graftversus-host reaction. Blood 94: 1028-1037.
31. Kahn, D. A., D. C. Archer, D. P. Gold, and C. J. Kelly. 2001. Adjuvant immunotherapy is dependent on inducible nitric oxide synthase. J. Exp. Med. 193: 1261-1268.
32. Shi, F. D., M. Flodström, S. H. Kim, S. Pakala, M. Cleary, H. G. Ljunggren, and N. Sarvetnick. 2001. Control of the autoimmune response by type 2 nitric oxide synthase. J. Immunol. 167: 3000-3006.
33. Marshall, H. E., K. Merchant, and J. S. Stamler. 2000. Nitrosation and oxidation in the regulation of gene expression. FASEB J. 14: 1889-1900.
34. Vodovotz, Y., L. Chesler, H. Chong, S. J. Kim, J. T. Simpson, W. DeGraff, G. W. Cox, A. B. Roberts, D. A. Wink, and M. H. Barcellos-Hoff. 1999. Regulation of transforming growth factor beta1 by nitric oxide. Cancer Res. 59: 2142-2149.
35. Obermeier, F., V. Gross, J. Schölmerich, and W. Falk. 1999. Interleukin-1 production by mouse macrophages is regulated in a feedback fashion by nitric oxide. J. Leukoc. Biol. 66: 829-836.
36. Connelly, L., M. Palacios-Callender, C. Ameixa, S. Moncada, and A. J. Hobbs. 2001. Biphasic regulation of NF-kappa B activity underlies the pro- and anti-inflammatory actions of nitric oxide. J. Immunol. 166: 3873-3881.
37. D'Alessio, F. R., K. Tsushima, N. R. Aggarwal, E. E. West, M. H. Willett, M. F. Britos, M. R. Pipeling, R. G. Brower, R. M. Tuder, J. F. McDyer, and L. S. King. 2009. CD4+CD25+Foxp3+ Tregs resolve experimental lung injury in mice and are present in humans with acute lung injury. J. Clin. Invest. 119: 2898-2913.
38. Halbower, A. C., R. J. Mason, S. H. Abman, and R. M. Tuder. 1994. Agarose infiltration improves morphology of cryostat sections of lung. Lab. Invest. 71: 149-153.
39. King, L. S., S. Nielsen, and P. Agre. 1996. Aquaporin-1 water channel protein in lung: ontogeny, steroid-induced expression, and distribution in rat. J. Clin. Invest. 97: 2183-2191.
40. Cuzzocrea, S., E. Mazzon, G. Calabro, L. Dugo, A. De Sarro, F. A. van De LOO, and A. P. Caputi. 2000. Inducible nitric oxide synthase-knockout mice exhibit resistance to pleurisy and lung injury caused by carrageenan. Am. J. Respir. Crit. Care Med. 162: 1859-1866.
41. Peng, X., R. E. Abdulnour, S. Sammani, S. F. Ma, E. J. Han, E. J. Hasan, R. Tuder, J. G. Garcia, and P. M. Hassoun. 2005. Inducible nitric oxide synthase contributes to ventilator-induced lung injury. Am. J. Respir. Crit. Care Med. 172: 470-479.
42. Akaike, T., and H. Maeda. 2000. Nitric oxide and virus infection. Immunology 101: 300-308.
43. Karupiah, G., J. H. Chen, S. Mahalingam, C. F. Nathan, and J. D. MacMicking. 1998. Rapid interferon gamma-dependent clearance of influenza A virus and protection from consolidating pneumonitis in nitric oxide synthase 2-deficient mice. J. Exp. Med. 188: 1541-1546.
44. Shanley, T. P., B. Zhao, D. R. Macariola, A. Denenberg, A. L. Salzman, and P. A. Ward. 2002. Role of nitric oxide in acute lung inflammation: lessons learned from the inducible nitric oxide synthase knockout mouse. Crit. Care Med. 30: 1960-1968.
45. Serhan, C. N., and J. Savill. 2005. Resolution of inflammation: the beginning programs the end. Nat. Immunol. 6: 1191-1197.
46. Nathan, C. 1997. Inducible nitric oxide synthase: what difference does it make? J. Clin. Invest. 100: 2417-2423.
47. Hickey, M. J., K. A. Sharkey, E. G. Sihota, P. H. Reinhardt, J. D. Macmicking, C. Nathan, and P. Kubes. 1997. Inducible nitric oxide synthase-deficient mice have enhanced leukocyte-endothelium interactions in endotoxemia. FASEB J. 11: 955-964.
48. Berg, D. T., A. Gupta, M. A. Richardson, L. A. O'Brien, D. Calnek, and B. W. Grinnell. 2007. Negative regulation of inducible nitric-oxide synthase expression mediated through transforming growth factor-beta-dependent modulation of transcription factor TCF11. J. Biol. Chem. 282: 36837-36844.
49. Jun, C. D., B. M. Choi, S. U. Kim, S. Y. Lee, H. M. Kim, and H. T. Chung. 1995. Down-regulation of transforming growth factor-beta gene expression by antisense oligodeoxynucleotides increases recombinant interferon-gamma-induced nitric oxide synthesis in murine peritoneal macrophages. Immunology 85: 114-119.
50. Pittet, J. F., M. J. Griffiths, T. Geiser, N. Kaminski, S. L. Dalton, X. Huang, L. A. Brown, P. J. Gotwals, V. E. Koteliansky, M. A. Matthay, and D. Sheppard. 2001. TGF-beta is a critical mediator of acute lung injury. J. Clin. Invest. 107: 1537-1544.
51. Letterio, J. J., and A. B. Roberts. 1998. Regulation of immune responses by TGF-beta. Annu. Rev. Immunol. 16: 137-161.
52. Hochberg, D., C. W. Johnson, J. Chen, D. Cohen, J. Stern, E. D. Vaughan, Jr., D. Poppas, and D. Felsen. 2000. Interstitial fibrosis of unilateral ureteral obstruction is exacerbated in kidneys of mice lacking the gene for inducible nitric oxide synthase. Lab. Invest. 80: 1721-1728.
53. Savill, J., I. Dransfield, C. Gregory, and C. Haslett. 2002. A blast from the past: clearance of apoptotic cells regulates immune responses. Nat. Rev. Immunol. 2: 965-975.
54. Fortenberry, J. D., M. L. Owens, M. R. Brown, D. Atkinson, and L. A. Brown. 1998. Exogenous nitric oxide enhances neutrophil cell death and DNA fragmentation. Am. J. Respir. Cell Mol. Biol. 18: 421-428.
55. Ferretti, S., O. Bonneau, G. R. Dubois, C. E. Jones, and A. Trifilieff. 2003. IL-17, produced by lymphocytes and neutrophils, is necessary for lipopolysaccharide-induced airway neutrophilia: IL-15 as a possible trigger. J. Immunol. 170: 2106-2112.
56. Hollingsworth, J. W., B. J. Chen, D. M. Brass, K. Berman, M. D. Gunn, D. N. Cook, and D. A. Schwartz. 2005. The critical role of hematopoietic cells in lipopolysaccharide-induced airway inflammation. Am. J. Respir. Crit. Care Med. 171: 806-813.
57. Koay, M. A., X. Gao, M. K. Washington, K. S. Parman, R. T. Sadikot, T. S. Blackwell, and J. W. Christman. 2002. Macrophages are necessary for maximal nuclear factor-kappa B activation in response to endotoxin. Am. J. Respir. Cell Mol. Biol. 26: 572-578.
58. Croft, M. 2003. Co-stimulatory members of the TNFR family: keys to effective T-cell immunity? Nat. Rev. Immunol. 3: 609-620.
59. Chen, L. 2004. Co-inhibitory molecules of the B7-CD28 family in the control of T-cell immunity. Nat. Rev. Immunol. 4: 336-347.
60. Hashimoto, N., T. Kawabe, K. Imaizumi, T. Hara, M. Okamoto, K. Kojima, K. Shimokata, and Y. Hasegawa. 2004. CD40 plays a crucial role in lipopolysaccharide-induced acute lung injury. Am. J. Respir. Cell Mol. Biol. 30: 808-815.
61. Gold, J. A., M. Parsey, Y. Hoshino, S. Hoshino, A. Nolan, H. Yee, D. B. Tse, and M. D. Weiden. 2003. CD40 contributes to lethality in acute sepsis: in vivo role for CD40 in innate immunity. Infect. Immun. 71: 3521-3528.
62. Nolan, A., M. Weiden, A. Kelly, Y. Hoshino, S. Hoshino, N. Mehta, and J. A. Gold. 2008. CD40 and CD80/86 act synergistically to regulate inflammation and mortality in polymicrobial sepsis. Am. J. Respir. Crit. Care Med. 177: 301-308.
63. Hoyt, J. C., J. Ballering, H. Numanami, J. M. Hayden, and R. A. Robbins. 2006. Doxycycline modulates nitric oxide production in murine lung epithelial cells. J. Immunol. 176: 567-572.
64. Razavi, H. M., F. Wang, S. Weicker, M. Rohan, C. Law, D. G. McCormack, and S. Mehta. 2004. Pulmonary neutrophil infiltration in murine sepsis: role of inducible nitric oxide synthase. Am. J. Respir. Crit. Care Med. 170: 227-233.
65. Wang, F., M. Patel, H. M. Razavi, S. Weicker, M. G. Joseph, D. G. McCormack, and S. Mehta. 2002. Role of inducible nitric oxide synthase in pulmonary microvascular protein leak in murine sepsis. Am. J. Respir. Crit. Care Med. 165: 1634-1639.
66. Taylor, R. W., J. L. Zimmerman, R. P. Dellinger, R. C. Straube, G. J. Criner, K. Davis, Jr., K. M. Kelly, T. C. Smith, and R. J. Small; Inhaled Nitric Oxide in ARDS Study Group. 2004. Low-dose inhaled nitric oxide in patients with acute lung injury: a randomized controlled trial. JAMA 291: 1603-1609.
67. Dellinger, R. P., J. L. Zimmerman, R. W. Taylor, R. C. Straube, D. L. Hauser, G. J. Criner, K. Davis, Jr., T. M. Hyers, and P. Papadakos; Inhaled Nitric Oxide in ARDS Study Group. 1998. Effects of inhaled nitric oxide in patients with acute respiratory distress syndrome: results of a randomized phase II trial. Crit. Care Med. 26: 15-23.
68. Lundin, S., H. Mang, M. Smithies, O. Stenqvist, and C. Frostell; The European Study Group of Inhaled Nitric Oxide. 1999. Inhalation of nitric oxide in acute lung injury: results of a European multicentre study. Intensive Care Med. 25: 911-919.
69. Giordano, D., C. Li, M. S. Suthar, K. E. Draves, D. Y. Ma, M. Gale, Jr., and E. A. Clark. 2011. Nitric oxide controls an inflammatory-like Ly6C(hi)PDCA1+ DC subset that regulates Th1 immune responses. J. Leukoc. Biol. 89: 443-455.