A critical role for P2X7 receptor-induced VCAM-1 shedding and neutrophil infiltration during acute lung injury

Journal of Immunology

Volumn 197, Issue 7, 2016, Pages 2828-2837

  Mishra, Amarjit ^a   Guo, Yujie ^a   Zhang, Li ^a   More, Sunil ^a   Weng, Tingting ^a   Chintagari, Narendranath Reddy ^a   Huang, Chaoqun ^a   Liang, Yurong ^a   Pushparaj, Samuel ^a   Gou, Deming ^b   Breshears, Melanie ^a   Liu, Lin ^a  

^a OKLAHOMA STATE UNIVERSITY   (United States)

^b SHENZHEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

PURINERGIC P2X7 RECEPTOR; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME; VASCULAR CELL ADHESION MOLECULE 1;

ACUTE LUNG INJURY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ARTIFICIAL VENTILATION; CONTROLLED STUDY; ENZYME ACTIVATION; EPITHELIUM CELL; HOST RESISTANCE; LIMIT OF QUANTITATION; LUNG ALVEOLUS MACROPHAGE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; DEFICIENCY; DISEASE MODEL; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; NEUTROPHIL; PATHOLOGY;

ACUTE LUNG INJURY; ANIMALS; DISEASE MODELS, ANIMAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUTROPHILS; RECEPTORS, PURINERGIC P2X7; VASCULAR CELL ADHESION MOLECULE-1;

EID: 84989928512     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1501041     Document Type: Article

References (61)

1. Matthay, M. A., and R. L. Zemans. 2011. The acute respiratory distress syndrome: pathogenesis and treatment. Annu. Rev. Pathol. 6: 147-163.
2. Balamayooran, G., S. Batra, M. B. Fessler, K. I. Happel, and S. Jeyaseelan. 2010. Mechanisms of neutrophil accumulation in the lungs against bacteria. Am. J. Respir. Cell Mol. Biol. 43: 5-16.
3. Martin, T. R., B. P. Pistorese, E. Y. Chi, R. B. Goodman, and M. A. Matthay. 1989. Effects of leukotriene B4 in the human lung: recruitment of neutrophils into the alveolar spaces without a change in protein permeability. J. Clin. Invest. 84: 1609-1619.
4. Ong, E. S., X. P. Gao, N. Xu, D. Predescu, A. Rahman, M. T. Broman, D. H. Jho, and A. B. Malik. 2003. E. coli pneumonia induces CD18-independent airway neutrophil migration in the absence of increased lung vascular permeability. Am. J. Physiol. Lung Cell. Mol. Physiol. 285: L879-L888.
5. Tateda, K., T. A. Moore, J. C. Deng, M. W. Newstead, X. Zeng, A. Matsukawa, M. S. Swanson, K. Yamaguchi, and T. J. Standiford. 2001. Early recruitment of neutrophils determines subsequent T1/T2 host responses in a murine model of Legionella pneumophila pneumonia. J. Immunol. 166: 3355-3361.
6. Jeyaseelan, S., S. K. Young, M. Yamamoto, P. G. Arndt, S. Akira, J. K. Kolls, and G. S. Worthen. 2006. Toll/IL-1R domain-containing adaptor protein (TIRAP) is a critical mediator of antibacterial defense in the lung against Klebsiella pneumoniae but not Pseudomonas aeruginosa. J. Immunol. 177: 538- 547.
7. Abraham, E., A. Carmody, R. Shenkar, and J. Arcaroli. 2000. Neutrophils as early immunologic effectors in hemorrhage- or endotoxemia-induced acute lung injury. Am. J. Physiol. Lung Cell. Mol. Physiol. 279: L1137-L1145.
8. Chen, S. C., B. Mehrad, J. C. Deng, G. Vassileva, D. J. Manfra, D. N. Cook, M. T. Wiekowski, A. Zlotnik, T. J. Standiford, and S. A. Lira. 2001. Impaired pulmonary host defense in mice lacking expression of the CXC chemokine lungkine. J. Immunol. 166: 3362-3368.
9. Jeyaseelan, S., R. Manzer, S. K. Young, M. Yamamoto, S. Akira, R. J. Mason, and G. S. Worthen. 2005. Induction of CXCL5 during inflammation in the rodent lung involves activation of alveolar epithelium. Am. J. Respir. Cell Mol. Biol. 32: 531-539.
10. Snelgrove, R. J., P. L. Jackson, M. T. Hardison, B. D. Noerager, A. Kinloch, A. Gaggar, S. Shastry, S. M. Rowe, Y. M. Shim, T. Hussell, and J. E. Blalock. 2010. A critical role for LTA4H in limiting chronic pulmonary neutrophilic inflammation. Science 330: 90-94.
11. Kumasaka, T., N. A. Doyle, W. M. Quinlan, L. Graham, and C. M. Doerschuk. 1996. Role of CD11/CD18 in neutrophil emigration during acute and recurrent Pseudomonas aeruginosa-induced pneumonia in rabbits. Am. J. Pathol. 148: 1297-1305.
12. Bowden, R. A., Z. M. Ding, E. M. Donnachie, T. K. Petersen, L. H. Michael, C. M. Ballantyne, and A. R. Burns. 2002. Role of alpha4 integrin and VCAM-1 in CD18-independent neutrophil migration across mouse cardiac endothelium. Circ. Res. 90: 562-569.
13. Burns, J. A., T. B. Issekutz, H. Yagita, and A. C. Issekutz. 2001. The alpha 4 beta 1 (very late antigen (VLA)-4, CD49d/CD29) and alpha 5 beta 1 (VLA-5, CD49e/CD29) integrins mediate beta 2 (CD11/CD18) integrin-independent neutrophil recruitment to endotoxin-induced lung inflammation. J. Immunol. 166: 4644- 4649.
14. Reinhardt, P. H., J. F. Elliott, and P. Kubes. 1997. Neutrophils can adhere via alpha4beta1-integrin under flow conditions. Blood 89: 3837-3846.
15. Ibbotson, G. C., C. Doig, J. Kaur, V. Gill, L. Ostrovsky, T. Fairhead, and P. Kubes. 2001. Functional alpha4-integrin: A newly identified pathway of neutrophil recruitment in critically ill septic patients. Nat. Med. 7: 465-470.
16. Lucattelli, M., S. Cicko, T. Muller, M. Lommatzsch, G. De Cunto, S. Cardini, W. Sundas, M. Grimm, R. Zeiser, T. Durk, et al. 2011. P2X7 receptor signaling in the pathogenesis of smoke-induced lung inflammation and emphysema. Am. J. Respir. Cell Mol. Biol. 44: 423-429.
17. Muller, T., V. R. Paula, M. Grimm, T. Durk, S. Cicko, R. Zeiser, T. Jakob, S. F. Martin, B. Blumenthal, S. Sorichter, et al. 2010. A potential role for P2X7R in allergic airway inflammation in mice and humans. Am. J. Respir. Cell Mol. Biol. 44: 456-464.
18. Riteau, N., P. Gasse, L. Fauconnier, A. Gombault, M. Couegnat, L. Fick, J. Kanellopoulos, V. F. Quesniaux, S. Marchand-Adam, B. Crestani, et al. 2010. Extracellular ATP is a danger signal activating P2X7 receptor in lung inflammation and fibrosis. Am. J. Respir. Crit. Care Med. 182: 774-783.
19. Denlinger, L. C., L. Shi, A. Guadarrama, K. Schell, D. Green, A. Morrin, K. Hogan, R. L. Sorkness, W. W. Busse, and J. E. Gern. 2009. Attenuated P2X7 pore function as a risk factor for virus-induced loss of asthma control. Am. J. Respir. Crit. Care Med. 179: 265-270.
20. Chen, Z., N. Jin, T. Narasaraju, J. Chen, L. R. McFarland, M. Scott, and L. Liu. 2004. Identification of two novel markers for alveolar epithelial type I and II cells. Biochem. Biophys. Res. Commun. 319: 774-780.
21. Mishra, A., N. R. Chintagari, Y. Guo, T. Weng, L. Su, and L. Liu. 2011. Purinergic P2X7 receptor regulates lung surfactant secretion in a paracrine manner. J. Cell Sci. 124: 657-668.
22. Altemeier, W. A., G. Matute-Bello, S. A. Gharib, R. W. Glenny, T. R. Martin, and W. C. Liles. 2005. Modulation of lipopolysaccharide-induced gene transcription and promotion of lung injury by mechanical ventilation. J. Immunol. 175: 3369-3376.
23. Narasaraju, T. A., N. Jin, C. R. Narendranath, Z. Chen, D. Gou, and L. Liu. 2003. Protein nitration in rat lungs during hyperoxia exposure: A possible role of myeloperoxidase. Am. J. Physiol. Lung Cell. Mol. Physiol. 285: L1037-L1045.
24. Chen, J., Z. Chen, N. R. Chintagari, M. Bhaskaran, N. Jin, T. Narasaraju, and L. Liu. 2006. Alveolar type I cells protect rat lung epithelium from oxidative injury. J. Physiol. 572: 625-638.
25. Corti, M., A. R. Brody, and J. H. Harrison. 1996. Isolation and primary culture of murine alveolar type II cells. Am. J. Respir. Cell Mol. Biol. 14: 309-315.
26. Manzer, R., J. Wang, K. Nishina, G. McConville, and R. J. Mason. 2006. Alveolar epithelial cells secrete chemokines in response to IL-1beta and lipopolysaccharide but not to ozone. Am. J. Respir. Cell Mol. Biol. 34: 158-166.
27. Witherden, I. R., E. J. Vanden Bon, P. Goldstraw, C. Ratcliffe, U. Pastorino, and T. D. Tetley. 2004. Primary human alveolar type II epithelial cell chemokine release: effects of cigarette smoke and neutrophil elastase. Am. J. Respir. Cell Mol. Biol. 30: 500-509.
28. Thorley, A. J., P. A. Ford, M. A. Giembycz, P. Goldstraw, A. Young, and T. D. Tetley. 2007. Differential regulation of cytokine release and leukocyte migration by lipopolysaccharide-stimulated primary human lung alveolar type II epithelial cells and macrophages. J. Immunol. 178: 463-473.
29. Vanderbilt, J. N., E. M. Mager, L. Allen, T. Sawa, J. Wiener-Kronish, R. Gonzalez, and L. G. Dobbs. 2003. CXC chemokines and their receptors are expressed in type II cells and upregulated following lung injury. Am. J. Respir. Cell Mol. Biol. 29: 661-668.
30. Cook-Mills, J. M., M. E. Marchese, and H. Abdala-Valencia. 2011. Vascular cell adhesion molecule-1 expression and signaling during disease: regulation by reactive oxygen species and antioxidants. Antioxid. Redox Signal. 15: 1607- 1638.
31. Gonzalo, J. A., C. M. Lloyd, L. Kremer, E. Finger, C. Martinez-A, M. H. Siegelman, M. Cybulsky, and J. C. Gutierrez-Ramos. 1996. Eosinophil recruitment to the lung in a murine model of allergic inflammation: The role of T cells, chemokines, and adhesion receptors. J. Clin. Invest. 98: 2332-2345.
32. Guo, R. F., N. C. Riedemann, I. J. Laudes, V. J. Sarma, R. G. Kunkel, K. A. Dilley, J. D. Paulauskis, and P. A. Ward. 2002. Altered neutrophil trafficking during sepsis. J. Immunol. 169: 307-314.
33. Ueki, S., J. Kihara, H. Kato, W. Ito, M. Takeda, Y. Kobayashi, H. Kayaba, and J. Chihara. 2009. Soluble vascular cell adhesion molecule-1 induces human eosinophil migration. Allergy 64: 718-724.
34. Kubes, P., X. F. Niu, C. W. Smith, M. E. Kehrli Jr., P. H. Reinhardt, and R. C. Woodman. 1995. A novel beta 1-dependent adhesion pathway on neutrophils: A mechanism invoked by dihydrocytochalasin B or endothelial transmigration. FASEB J. 9: 1103-1111.
35. Petty, J. M., C. C. Lenox, D. J. Weiss, M. E. Poynter, and B. T. Suratt. 2009. Crosstalk between CXCR4/stromal derived factor-1 and VLA-4/VCAM-1 pathways regulates neutrophil retention in the bone marrow. J. Immunol. 182: 604-612.
36. Kitani, A., N. Nakashima, T. Izumihara, M. Inagaki, X. Baoui, S. Yu, T. Matsuda, and T. Matsuyama. 1998. Soluble VCAM-1 induces chemotaxis of Jurkat and synovial fluid T cells bearing high affinity very late antigen-4. J. Immunol. 161: 4931-4938.
37. Bhaskaran, M., N. Kolliputi, Y. Wang, D. Gou, N. R. Chintagari, and L. Liu. 2007. Trans-differentiation of alveolar epithelial type II cells to type I cells involves autocrine signaling by transforming growth factor beta 1 through the Smad pathway. J. Biol. Chem. 282: 3968-3976.
38. Garton, K. J., P. J. Gough, J. Philalay, P. T. Wille, C. P. Blobel, R. H. Whitehead, P. J. Dempsey, and E. W. Raines. 2003. Stimulated shedding of vascular cell adhesion molecule 1 (VCAM-1) is mediated by tumor necrosis factor-Alphaconverting enzyme (ADAM 17). J. Biol. Chem. 278: 37459-37464.
39. Budagian, V., E. Bulanova, L. Brovko, Z. Orinska, R. Fayad, R. Paus, and S. Bulfone-Paus. 2003. Signaling through P2X7 receptor in human T cells involves p56lck, MAP kinases, and transcription factors AP-1 and NF-kappa B. J. Biol. Chem. 278: 1549-1560.
40. Gendron, F. P., J. T. Neary, P. M. Theiss, G. Y. Sun, F. A. Gonzalez, and G. A. Weisman. 2003. Mechanisms of P2X7 receptor-mediated ERK1/2 phosphorylation in human astrocytoma cells. Am. J. Physiol. Cell Physiol. 284: C571-C581.
41. Soond, S. M., B. Everson, D. W. Riches, and G. Murphy. 2005. ERK-mediated phosphorylation of Thr735 in TNFalpha-converting enzyme and its potential role in TACE protein trafficking. J. Cell Sci. 118: 2371-2380.
42. Osborn, L., C. Hession, R. Tizard, C. Vassallo, S. Luhowskyj, G. Chi-Rosso, and R. Lobb. 1989. Direct expression cloning of vascular cell adhesion molecule 1, a cytokine-induced endothelial protein that binds to lymphocytes. Cell 59: 1203- 1211.
43. Rice, G. E., and M. P. Bevilacqua. 1989. An inducible endothelial cell surface glycoprotein mediates melanoma adhesion. Science 246: 1303-1306.
44. Elices, M. J., L. Osborn, Y. Takada, C. Crouse, S. Luhowskyj, M. E. Hemler, and R. R. Lobb. 1990. VCAM-1 on activated endothelium interacts with the leukocyte integrin VLA-4 at a site distinct from the VLA-4/fibronectin binding site. Cell 60: 577-584.
45. Ruegg, C., A. A. Postigo, E. E. Sikorski, E. C. Butcher, R. Pytela, and D. J. Erle. 1992. Role of integrin alpha 4 beta 7/alpha 4 beta P in lymphocyte adherence to fibronectin and VCAM-1 and in homotypic cell clustering. J. Cell Biol. 117: 179-189.
46. Chin, J. E., C. A. Hatfield, G. E. Winterrowd, J. R. Brashler, S. L. Vonderfecht, S. F. Fidler, R. L. Griffin, K. P. Kolbasa, R. F. Krzesicki, L. M. Sly, et al. 1997. Airway recruitment of leukocytes in mice is dependent on alpha4-integrins and vascular cell adhesion molecule-1. Am. J. Physiol. 272: L219-L229.
47. Parmley, L. A., N. D. Elkins, M. A. Fini, Y. E. Liu, J. E. Repine, and R. M. Wright. 2007. Alpha-4/beta-1 and alpha-L/beta-2 integrins mediate cytokine induced lung leukocyte-epithelial adhesion and injury. Br. J. Pharmacol. 152: 915-929.
48. Rose, D. M., P. M. Cardarelli, R. R. Cobb, and M. H. Ginsberg. 2000. Soluble VCAM-1 binding to alpha4 integrins is cell-Type specific and activation dependent and is disrupted during apoptosis in T cells. Blood 95: 602-609.
49. Nakao, S., T. Kuwano, T. Ishibashi, M. Kuwano, and M. Ono. 2003. Synergistic effect of TNF-Alpha in soluble VCAM-1-induced angiogenesis through alpha 4 integrins. J. Immunol. 170: 5704-5711.
50. Wellicome, S. M., P. Kapahi, J. C. Mason, Y. Lebranchu, H. Yarwood, and D. O. Haskard. 1993. Detection of a circulating form of vascular cell adhesion molecule-1: raised levels in rheumatoid arthritis and systemic lupus erythematosus. Clin. Exp. Immunol. 92: 412-418.
51. McDonnell, G. V., S. A. McMillan, J. P. Douglas, A. G. Droogan, and S. A. Hawkins. 1998. Raised CSF levels of soluble adhesion molecules across the clinical spectrum of multiple sclerosis. J. Neuroimmunol. 85: 186-192.
52. Hamzaoui, A., J. Ammar, F. El Mekki, O. Borgi, H. Ghrairi, M. Ben Brahim, and K. Hamzaoui. 2001. Elevation of serum soluble E-selectin and VCAM-1 in severe asthma. Mediators Inflamm. 10: 339-342.
53. Kumasaka, T., W. M. Quinlan, N. A. Doyle, T. P. Condon, J. Sligh, F. Takei, Al. Beaudet, C. F. Bennett, and C. M. Doerschuk. 1996. Role of the intercellular adhesion molecule-1 (ICAM-1) in endotoxin-induced pneumonia evaluated using ICAM-1 antisense oligonucleotides, anti-ICAM-1 monoclonal antibodies, and ICAM-1 mutant mice. J. Clin. Invest. 97: 2362-2369.
54. Folkesson, H. G., and M.A. Matthay. 1997. Inhibition of CD18 or CD11b attenuates acute lung injury after acid instillation in rabbits. J. Appl. Physiol 82: 1743-1750.
55. Gao, X., N. Xu, M. Sekosan, D. Mehta, S. Y. Ma, A. Rahman, and A. B. Malik. 2001. Differential role of CD18 integrins in mediating lung neutrophil sequestration and increased microvascular permeability induced by Escherichia coli in mice. J. Immunol. 167: 2895-2901.
56. Tasaka, S., S. E. Richer, J. P. Mizgerd, and C. M. Doerschuk. 2002. Very late antigen-4 in CD18-independent neutrophil emigration during acute bacterial pneumonia in mice. Am. J. Respir. Crit. Care Med. 166: 53-60.
57. Singh, R. J., J. C. Mason, E. A. Lidington, D. R. Edwards, R. K. Nuttall, R. Khokha, V. Knauper, G. Murphy, and J. Gavrilovic. 2005. Cytokine stimulated vascular cell adhesion molecule-1 (VCAM-1) ectodomain release is regulated by TIMP-3. Cardiovasc. Res. 67: 39-49.
58. Rizzoni, D., M. L. Muiesan, E. Porteri, M. Castellano, M. Salvetti, C. Monteduro, C. De Ciuceis, G. Boari, U. Valentini, A. Cimino, et al. 2003. Circulating adhesion molecules and carotid artery structural changes in patients with noninsulin-dependent diabetes mellitus. J. Hum. Hypertens. 17: 463-470.
59. Atsuta, J., S. A. Sterbinsky, J. Plitt, L. M. Schwiebert, B. S. Bochner, and R. P. Schleimer. 1997. Phenotyping and cytokine regulation of the BEAS-2B human bronchial epithelial cell: demonstration of inducible expression of the adhesion molecules VCAM-1 and ICAM-1. Am. J. Respir. Cell Mol. Biol. 17: 571-582.
60. Vanderstocken, G., B. Bondue, M. Horckmans, L. Di Pietrantonio, B. Robaye, J. M. Boeynaems, and D. Communi. 2010. P2Y2 receptor regulates VCAM-1 membrane and soluble forms and eosinophil accumulation during lung inflammation. J. Immunol. 185: 3702-3707.
61. Lévesque, J. P., Y. Takamatsu, S. K. Nilsson, D. N. Haylock, and P. J. Simmons. 2001. Vascular cell adhesion molecule-1 (CD106) is cleaved by neutrophil proteases in the bone marrow following hematopoietic progenitor cell mobilization by granulocyte colony-stimulating factor. Blood 98: 1289-1297.