Dopamine inhibits pulmonary edema through the VEGF-VEGFR2 axis in a murine model of acute lung injury

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 302, Issue 2, 2012, Pages 185-192

  Vohra, Pawan K ^a   Hoeppner, Luke H ^a   Sagar, Gunisha ^a   Dutta, Shamit K ^a   Misra, Sanjay ^b   Hubmayr, Rolf D ^b   Mukhopadhyay, Debabrata ^a  

^a MAYO GRADUATE SCHOOL   (United States)

^b Mayo Clinic College of Medicine   (United States)

Author keywords

Dopamine receptor D2; Vascular endothelial growth factor

Indexed keywords

DOPAMINE; DOPAMINE 2 RECEPTOR; ENDOTHELIAL NITRIC OXIDE SYNTHASE; MYELOPEROXIDASE; QUINPIROLE; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

ACUTE LUNG INJURY; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL PERMEABILITY; CONTROLLED STUDY; DRUG EFFECT; ENZYME ACTIVITY; LUNG EDEMA; MALE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SURVIVAL RATE;

ACUTE LUNG INJURY; ANIMALS; CAPILLARY PERMEABILITY; DOPAMINE; DOPAMINE ANTAGONISTS; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; NEOVASCULARIZATION, PHYSIOLOGIC; NEUTROPHIL INFILTRATION; NEUTROPHILS; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE III; PEROXIDASE; PHOSPHORYLATION; PULMONARY EDEMA; RECEPTORS, DOPAMINE D2; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84855323185     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00274.2010     Document Type: Article

References (56)

1. Baltalarli A, Goksin I, Sirin H, Ortaç R, Onem G, Baltalarli B, Rendex O, Saçar M. Does anti-inflammatory therapy attenuate the lung injury caused by ischemia/reperfusion of the lower extremities in the rabbit? Int J Thoracic Cardiovasc Surg 3: 22, 2000.
2. Basu S, Nagy JA, Pal S, Vasile E, Eckelhoefer IA, Bliss VS, Manseau EJ, Dasgupta PS, Dvorak HF, Mukhopadhyay D. The neurotransmitter dopamine inhibits angiogenesis induced by vascular permeability factor/ vascular endothelial growth factor. Nat Med 7: 569-574, 2001.
3. Becker PM, Alcasabas A, Yu AY, Semenza GL, Bunton TE. Oxygenindependent upregulation of vascular endothelial growth factor and vascular barrier dysfunction during ventilated pulmonary ischemia in isolated ferret lungs. Am J Respir Cell Mol Biol 22: 272-279, 2000.
4. Berthiaume Y, Matthay MA. Alveolar edema fluid clearance and acute lung injury. Respir Physiol Neurobiol 159: 350-359, 2007.
5. Bertorello AM, Sznajder JI. The dopamine paradox in lung and kidney epithelia: sharing the same target but operating different signaling networks. Am J Respir Cell Mol Biol 33: 432-437, 2005.
6. Bhandari V, Choo-Wing R, Lee CG, Yusuf K, Nedrelow JH, Ambalavanan N, Malkus H, Homer RJ, Elias JA. Developmental regulation of NO-mediated VEGF-induced effects in the lung. Am J Respir Cell Mol Biol 39: 420-430, 2008.
7. Bhattacharya R, Sinha S, Yang SP, Patra C, Dutta S, Wang E, Mukhopadhyay D. The neurotransmitter dopamine modulates vascular permeability in the endothelium. J Mol Signal 3: 14, 2008.
8. Bucci M, Roviezzo F, Posadas I, Yu J, Parente L, Sessa WC, Ignarro LJ, Cirino G. Endothelial nitric oxide synthase activation is critical for vascular leakage during acute inflammation in vivo. Proc Natl Acad Sci USA 102: 904-908, 2005.
9. Chakroborty D, Sarkar C, Mitra RB, Banerjee S, Dasgupta PS, Basu S. Depleted dopamine in gastric cancer tissues: dopamine treatment retards growth of gastric cancer by inhibiting angiogenesis. Clin Cancer Res 10: 4349-4356, 2004.
10. Edirisinghe I, Arunachalam G, Wong C, Yao H, Rahman A, Phipps RP, Jin ZG, Rahman I. Cigarette-smoke-induced oxidative/nitrosative stress impairs VEGF- and fluid-shear-stress-mediated signaling in endothelial cells. Antioxid Redox Signal 12: 1355-1369, 2010.
11. Frey EA, Finlay BB. Lipopolysaccharide induces apoptosis in a bovine endothelial cell line via a soluble CD14 dependent pathway. Microb Pathog 24: 101-109, 1998.
12. Fujita M, Kuwano K, Kunitake R, Hagimoto N, Miyazaki H, Kaneko Y, Kawasaki M, Maeyama T, Hara N. Endothelial cell apoptosis in lipopolysaccharide-induced lung injury in mice. Int Arch Allergy Immunol 117: 202-208, 1998.
13. Fukumura D, Gohongi T, Kadambi A, Izumi Y, Ang J, Yun CO, Buerk DG, Huang PL, Jain RK. Predominant role of endothelial nitric oxide synthase in vascular endothelial growth factor-induced angiogenesis and vascular permeability. Proc Natl Acad Sci USA 98: 2604-2609, 2001.
14. Fulton D, Gratton JP, McCabe TJ, Fontana J, Fujio Y, Walsh K, Franke TF, Papapetropoulos A, Sessa WC. Regulation of endotheliumderived nitric oxide production by the protein kinase Akt. Nature 399: 597-601, 1999.
15. Godzich M, Hodnett M, Frank JA, Su G, Pespeni M, Angel A, Howard MB, Matthay MA, Pittet JF. Activation of the stress protein response prevents the development of pulmonary edema by inhibiting VEGF cell signaling in a model of lung ischemia-reperfusion injury in rats. FASEB J 20: 1519-1521, 2006.
16. Gropper MA, Wiener-Kronish J. The epithelium in acute lung injury/ acute respiratory distress syndrome. Curr Opin Crit Care 14: 11-15, 2008.
17. Guerrero C, Lecuona E, Pesce L, Ridge KM, Sznajder JI. Dopamine regulates Na-K-ATPase in alveolar epithelial cells via MAPK-ERKdependent mechanisms. Am J Physiol Lung Cell Mol Physiol 281: L79-L85, 2001.
18. Gurkan OU, O'Donnell C, Brower R, Ruckdeschel E, Becker PM. Differential effects of mechanical ventilatory strategy on lung injury and systemic organ inflammation in mice. Am J Physiol Lung Cell Mol Physiol 285: L710-L718, 2003.
19. Hatakeyama T, Pappas PJ, Hobson RW 2nd, Boric MP, Sessa WC, Duran WN. Endothelial nitric oxide synthase regulates microvascular hyperpermeability in vivo. J Physiol 574: 275-281, 2006.
20. Hess W, Bruckner JB, von Faber du Faur J, Schmidt D, Tarnow J. The haemodynamic effects of dobutamine and dopamine in patients with coronary artery disease A study performed under general anaesthesia (author's transl). Anaesthesist 28: 316-321, 1979.
21. Hollenberg SM, Guglielmi M, Parrillo JE. Discordance between microvascular permeability and leukocyte dynamics in septic inducible nitric oxide synthase deficient mice. Crit Care 11: R125, 2007.
22. Hotchkiss CE, Hall PD, Cline JM, Willingham MC, Kreitman RJ, Gardin J, Latimer A, Ramage J, Feely T, DeLatte S, Tagge EP, Frankel AE. Toxicology and pharmacokinetics of DTGM, a fusion toxin consisting of a truncated diphtheria toxin (DT388) linked to human granulocyte-macrophage colony-stimulating factor, in cynomolgus monkeys. Toxicol Appl Pharmacol 158: 152-160, 1999.
23. Jacobson JR, Garcia JG. Novel therapies for microvascular permeability in sepsis. Curr Drug Targets 8: 509-514, 2007.
24. Jonkam CC, Bansal K, Traber DL, Hamahata A, Maybauer MO, Maybauer DM, Cox RA, Lange M, Connelly RL, Traber LD, Djukom CD, Salsbury JR, Herndon DN, Enkhbaatar P. Pulmonary vascular permeability changes in an ovine model of methicillin-resistant Staphylococcus aureus sepsis. Crit Care 13: R19, 2009.
25. Kaner RJ, Crystal RG. Pathogenesis of high altitude pulmonary edema: does alveolar epithelial lining fluid vascular endothelial growth factor exacerbate capillary leak? High Alt Med Biol 5: 399-409, 2004.
26. Kaner RJ, Ladetto JV, Singh R, Fukuda N, Matthay MA, Crystal RG. Lung overexpression of the vascular endothelial growth factor gene induces pulmonary edema. Am J Respir Cell Mol Biol 22: 657-664, 2000.
27. Kosmidou I, Karmpaliotis D, Kirtane AJ, Barron HV, Gibson CM. Vascular endothelial growth factors in pulmonary edema: an update. J Thromb Thrombolysis 25: 259-264, 2008.
28. Kroll J, Waltenberger J. VEGF-A induces expression of eNOS and iNOS in endothelial cells via VEGF receptor-2 (KDR). Biochem Biophys Res Commun 252: 743-746, 1998.
29. Leaver SK, Evans TW. Acute respiratory distress syndrome. BMJ 335: 389-394, 2007.
30. Marwick JA, Edirisinghe I, Arunachalam G, Stevenson CS, Macnee W, Kirkham PA, Rahman I. Cigarette smoke regulates VEGFR2- mediated survival signaling in rat lungs. J Inflamm 7: 11, 2010.
31. Matthay MA. Alveolar fluid clearance in patients with ARDS: does it make a difference? Chest 122: 340S-343S, 2002.
32. Matthay MA, Brower RG, Carson S, Douglas IS, Eisner M, Hite D, Holets S, Kallet RH, Liu KD, Macintyre N, Moss M, Schoenfeld D, Steingrub J, Thompson BT. Randomized, placebo-controlled clinical trial of an aerosolized beta-2 agonist for treatment of acute lung injury. Am J Respir Crit Care Med 184: 561-568, 2011.
33. Matthay MA, Calfee CS. Therapeutic value of a lung protective ventilation strategy in acute lung injury. Chest 128: 3089-3091, 2005.
34. Matthay MA, Clerici C, Saumon G. Invited review: Active fluid clearance from the distal air spaces of the lung. J Appl Physiol 93: 1533-1541, 2002.
35. Matthay MA, Robriquet L, Fang X. Alveolar epithelium: role in lung fluid balance and acute lung injury. Proc Am Thorac Soc 2: 206-213, 2005.
36. Matthay MA, Uchida T, Fang X. Clinical acute lung injury and acute respiratory distress syndrome. Curr Treat Options Cardiovasc Med 4: 139-149, 2002.
37. Matthay MA, Zimmerman GA. Acute lung injury and the acute respiratory distress syndrome: four decades of inquiry into pathogenesis and rational management. Am J Respir Cell Mol Biol 33: 319-327, 2005.
38. Medford AR, Douglas SK, Godinho SI, Uppington KM, Armstrong L, Gillespie KM, van Zyl B, Tetley TD, Ibrahim NB, Millar AB. Vascular endothelial growth factor (VEGF) isoform expression and activity in human and murine lung injury. Respir Res 10: 27, 2009.
39. Mullane KM, Kraemer R, Smith B. Myeloperoxidase activity as a quantitative assessment of neutrophil infiltration into ischemic myocardium. J Pharmacol Methods 14: 157-167, 1985.
40. Murohara T, Asahara T, Silver M, Bauters C, Masuda H, Kalka C, Kearney M, Chen D, Symes JF, Fishman MC, Huang PL, Isner JM. Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J Clin Invest 101: 2567-2578, 1998.
41. Patel GP, Grahe JS, Sperry M, Singla S, Elpern E, Lateef O, Balk RA. Efficacy and safety of dopamine versus norepinephrine in the management of septic shock. Shock 33: 375-380, 2010.
42. Perkins GD, McAuley DF, Thickett DR, Gao F. The beta-agonist lung injury trial (BALTI): a randomized placebo-controlled clinical trial. Am J Respir Crit Care Med 173: 281-287, 2006.
43. Pham I, Uchida T, Planes C, Ware LB, Kaner R, Matthay MA, Clerici C. Hypoxia upregulates VEGF expression in alveolar epithelial cells in vitro and in vivo. Am J Physiol Lung Cell Mol Physiol 283: L1133-L1142, 2002.
44. Pyne-Geithman GJ, Caudell DN, Cooper M, Clark JF, Shutter LA. Dopamine D2-receptor-mediated increase in vascular and endothelial NOS activity ameliorates cerebral vasospasm after subarachnoid hemorrhage in vitro. Neurocrit Care 10: 225-231, 2009.
45. Qvist J, Brynjolf I, Munck O. The effects of dopamine and noradrenaline on cardiovascular function in patients with acute respiratory failure. Eur J Anaesthesiol 11: 107-110, 1994.
46. Sarkar C, Chakroborty D, Mitra RB, Banerjee S, Dasgupta PS, Basu S. Dopamine in vivo inhibits VEGF-induced phosphorylation of VEGFR-2, MAPK, and focal adhesion kinase in endothelial cells. Am J Physiol Heart Circ Physiol 287: H1554-H1560, 2004.
47. Sinha S, Vohra PK, Bhattacharya R, Dutta S, Mukhopadhyay D. Dopamine regulates phosphorylation of VEGF receptor 2 by engaging Src-homology-2-domain-containing protein tyrosine phosphatase 2. J Cell Sci 122: 3385-3392, 2009.
48. Tassiopoulos AK, Carlin RE, Gao Y, Pedoto A, Finck CM, Landas SK, Tice DG, Marx W, Hakim TS, McGraw DJ. Role of nitric oxide and tumor necrosis factor on lung injury caused by ischemia/reperfusion of the lower extremities. J Vasc Surg 26: 647-656, 1997.
49. Voelkel NF, Vandivier RW, Tuder RM. Vascular endothelial growth factor in the lung. Am J Physiol Lung Cell Mol Physiol 290: L209-L221, 2006.
50. Ware LB, Kaner RJ, Crystal RG, Schane R, Trivedi NN, McAuley D, Matthay MA. VEGF levels in the alveolar compartment do not distinguish between ARDS and hydrostatic pulmonary oedema. Eur Respir J 26: 101-105, 2005.
51. Ware LB, Matthay MA. The acute respiratory distress syndrome. N Engl J Med 342: 1334-1349, 2000.
52. Ware LB, Matthay MA. Alveolar fluid clearance is impaired in the majority of patients with acute lung injury and the acute respiratory distress syndrome. Am J Respir Crit Care Med 163: 1376-1383, 2001.
53. Wheeler AP, Bernard GR. Acute lung injury and the acute respiratory distress syndrome: a clinical review. Lancet 369: 1553-1564, 2007.
54. Yano K, Liaw PC, Mullington JM, Shih SC, Okada H, Bodyak N, Kang PM, Toltl L, Belikoff B, Buras J, Simms BT, Mizgerd JP, Carmeliet P, Karumanchi SA, Aird WC. Vascular endothelial growth factor is an important determinant of sepsis morbidity and mortality. J Exp Med 203: 1447-1458, 2006.
55. Zhang S, Rahman M, Qi Z, Herwald H, Thorlacius H. Simvastatin regulates CXC chemokine formation in streptococcal M1 protein-induced neutrophil infiltration in the lung. Am J Physiol Lung Cell Mol Physiol 300: L930-L939, 2011.
56. Zheng H, Chen XL, Han ZX, Zhang Z, Wang SY, Xu QL. Ligustrazine attenuates acute lung injury after burn trauma. Burns 31: 453-458, 2005.