Sp1-mediated nonmuscle myosin light chain kinase expression and enhanced activity in vascular endothelial growth factor–induced vascular permeability

Pulmonary Circulation

Volumn 5, Issue 4, 2015, Pages 707-715

  Shimizua, Yuka ^a   Campa, Sara M ^a   Sun, Xiaoguang ^a   Zhou, Tong ^a   Wang, Ting ^a   Garcia, Joe G N ^a  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

ARDS; Endothelial; MYLK; Myosin light chain kinase (MLCK); Permeability; Promoter; Sp1; Transcription factor; Vascular endothelial growth factor (VEGF)

Indexed keywords

EID: 85026335799     PISSN: 20458932     EISSN: 20458940     Source Type: Journal    
DOI: 10.1086/684124     Document Type: Article

References (59)

1. MacCallum NS, Evans TW. Epidemiology of acute lung injury. Curr Opin Crit Care 2005;11(1):43–49.
2. Ware LB, Matthay MA. The acute respiratory distress syndrome. N Engl J Med 2000;342(18):1334–1349.
3. Brown LM, Kallet RH, Matthay MA, Dicker RA. The influence of race on the development of acute lung injury in trauma patients. Am J Surg 2011;201(4):486–491.
4. Moss M, Mannino DM. Race and gender differences in acute respiratory distress syndrome deaths in the United States: an analysis of multiplecause mortality data (1979–1996). Crit Care Med 2002;30(8):1679–1685.
5. Christie JD, Ma SF, Aplenc R, Li M, Lanken PN, Shah CV, Fuchs B, Albelda SM, Flores C, Garcia JG. Variation in the myosin light chain kinase gene is associated with development of acute lung injury after major trauma. Crit Care Med 2008;36(10):2794–2800.
6. Flores C, Ma SF, Maresso K, Wade MS, Villar J, Garcia JG. IL6 genewide haplotype is associated with susceptibility to acute lung injury. Transl Res 2008;152(1):11–17.
7. Gao L, Grant A, Halder I, Brower R, Sevransky J, Maloney JP, Moss M, et al. Novel polymorphisms in the myosin light chain kinase gene confer risk for acute lung injury. Am J Respir Cell Mol Biol 2006;34(4):487–495.
8. Ma SF, Flores C, Wade MS, Dudek SM, Nicolae DL, Ober C, Garcia JG. A common cortactin gene variation confers differential susceptibility to severe asthma. Genet Epidemiol 2008;32(8):757–766.
9. Ma SF, Xie L, Pino-Yanes M, Sammani S, Wade MS, Letsiou E, Siegler J, et al. Type 2 deiodinase and host responses of sepsis and acute lung injury. Am J Respir Cell Mol Biol 2011;45(6):1203–1211.
10. Mitra S, Wade MS, Sun X, Moldobaeva N, Flores C, Ma SF, Zhang W, Garcia JG, Jacobson JR. GADD45a promoter regulation by a functional genetic variant associated with acute lung injury. PloS ONE 2014;9(6): e100169.
11. Sun X, Elangovan VR, Mapes B, Camp SM, Sammani S, Saadat L, Ceco E, et al. The NAMPT promoter is regulated by mechanical stress, signal transducer and activator of transcription 5, and acute respiratory distress syndrome–associated genetic variants. Am J Respir Cell Mol Biol 2014;51 (5):660–667.
12. Sun X, Ma SF, Wade MS, Acosta-Herrera M, Villar J, Pino-Yanes M, Zhou T, et al. Functional promoter variants in sphingosine 1-phosphate receptor 3 associate with susceptibility to sepsis-associated acute respiratorydistress syndrome. Am J Physiol Lung Cell Mol Physiol 2013;305 (7):L467–L477.
13. Garcia JG, Davis HW, Patterson CE. Regulation of endothelial cell gap formation and barrier dysfunction: role of myosin light chain phosphorylation. J Cell Physiol 1995;163(3):510–522.
14. Flores C, Ma SF, Maresso K, Ober C, Garcia JG. A variant of the myosin light chain kinase gene is associated with severe asthma in African Americans. Genet Epidemiol 2007;31(4):296–305.
15. Gao L, Grant AV, Rafaels N, Stockton-Porter M, Watkins T, Gao P, Chi P, et al. Polymorphisms in the myosin light chain kinase gene that confer risk of severe sepsis are associated with a lower risk of asthma. J Allergy Clin Immunol 2007;119(5):1111–1118.
16. Rossi JL, Velentza AV, Steinhorn DM, Watterson DM, Wainwright MS. MLCK210 gene knockout or kinase inhibition preserves lung function following endotoxin-induced lung injury in mice. Am J Physiol Lung Cell Mol Physiol 2007;292(6):L1327–L1334.
17. Mirzapoiazova T, Moitra J, Moreno-Vinasco L, Sammani S, Turner JR, Chiang ET, Evenoski C, et al. Non-muscle myosin light chain kinase isoform is a viable molecular target in acute inflammatory lung injury. Am J Respir Cell Mol Biol 2011;44(1):40–52.
18. Moitra J, Evenoski C, Sammani S, Wadgaonkar R, Turner JR, Ma SF, Garcia JG. A transgenic mouse with vascular endothelial over-expression of the non-muscle myosin light chain kinase–2 isoform is susceptible to inflammatory lung injury: role of sexual dimorphism and age. Transl Res 2008;151(3):141–153.
19. Wang T, Moreno-Vinasco L, Ma SF, Zhou T, Shimizu Y, Sammani S, Epshtein Y, Watterson DM, Dudek SM, Garcia JG. Nonmuscle myosin light chain kinase regulates murine asthmatic inflammation. Am J Respir Cell Mol Biol 2014;50(6):1129–1135.
20. Ferrara N. Vascular endothelial growth factor: basic science and clinical progress. Endocr Rev 2004;25(4):581–611.
21. Harper SJ, Bates DO. VEGF-A splicing: the key to anti-angiogenic therapeutics? Nat Rev Cancer 2008;8(11):880–887.
22. McDonald DM. Angiogenesis and remodeling of airway vasculature in chronic inflammation. Am J Respir Crit Care Med 2001;164(10 pt 2): S39–S45.
23. Weis SM, Cheresh DA. Pathophysiological consequences of VEGFinduced vascular permeability. Nature 2005;437(7058):497–504.
24. Dvorak HF, Brown LF, Detmar M, Dvorak AM. Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am J Pathol 1995;146(5):1029–1039.
25. Dvorak HF, Dvorak AM, Manseau EJ, Wiberg L, Churchill WH. Fibrin gel investment associated with line 1 and line 10 solid tumor growth, angiogenesis, and fibroplasia in guinea pigs: role of cellular immunity, myofibroblasts, microvascular damage, and infarction in line 1 tumor regression. J Natl Cancer Inst 1979;62(6):1459–1472.
26. Dvorak HF, Orenstein NS, Carvalho AC, Churchill WH, Dvorak AM, Galli SJ, Feder J, Bitzer AM, Rypysc J, Giovinco P. Induction of a fibringel investment: an early event in line 10 hepatocarcinoma growth mediated by tumor-secreted products. J Immunol 1979;122(1):166–174.
27. Becker PM, Verin AD, Booth MA, Liu F, Birukova A, Garcia JG. Differential regulation of diverse physiological responses to VEG F inpulmonary endothelial cells. Am J Physiol Lung Cell Mol Physiol 2001;281(6):L1500–L1511.
28. Barratt S, Medford AR, Millar AB. Vascular endothelial growth factor in acute lung injury and acute respiratory distress syndrome. Respiration 2014;87(4):329–342.
29. Feltis BN, Wignarajah D, Zheng L, Ward C, Reid D, Harding R, Walters EH. Increased vascular endothelial growth factor and receptors: relationship to angiogenesis in asthma. Am J Respir Crit Care Med 2006;173(11):1201–1207.
30. Kanazawa H, Hirata K, Yoshikawa J. Involvement of vascular endothelial growth factor in exercise induced bronchoconstriction in asthmatic patients. Thorax 2002;57(10):885–888.
31. Medford AR, Millar AB. Vascular endothelial growth factor (VEGF) in acute lung injury (ALI) and acute respiratory distress syndrome (ARDS): paradox or paradigm? Thorax 2006;61(7):621–626.
32. Thickett DR, Armstrong L, Christie SJ, Millar AB. Vascular endothelial growth factor may contribute to increased vascular permeability in acute respiratory distress syndrome. Am J Respir Crit Care Med 2001;164 (9):1601–1605.
33. Carmeliet P, Ferreira V, Breier G, Pollefeyt S, Kieckens L, Gertsenstein M, Fahrig M, et al. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 1996;380(6573):435–439.
34. Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, O’Shea KS, Powell-Braxton L, Hillan KJ, Moore MW. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 1996;380(6573):439–442.
35. Berse B, Brown LF, Van de Water L, Dvorak HF, Senger DR. Vascular permeability factor (vascular endothelial growth factor) gene is expressed differentially in normal tissues, macrophages, and tumors. Mol Biol Cell 1992;3(2):211–220.
36. Monacci WT, Merrill MJ, Oldfield EH. Expression of vascular permeability factor/vascular endothelial growth factor in normal rat tissues. Am J Physiol 1993;264(4 pt 1):C995–C1002.
37. Mirzapoiazova T, Kolosova I, Usatyuk PV, Natarajan V, Verin AD. Diverse effects of vascular endothelial growth factor on human pulmonary endothelial barrier and migration. Am J Physiol Lung Cell Mol Physiol 2006;291(4):L718–L724.
38. Azamfirei L, Gurzu S, Solomon R, Copotoiu R, Copotoiu S, Jung I, Tilinca M, et al. Vascular endothelial growth factor: a possible mediator of endothelial activation in acute respiratory distress syndrome. Minerva Anestesiol 2010;76(8):609–616.
39. Zhai R, Gong MN, Zhou W, Thompson TB, Kraft P, Su L, Christiani DC. Genotypes and haplotypes of the VEGF gene are associated with higher mortality and lower VEGF plasma levels in patients with ARDS. Thorax 2007;62(8):718–722.
40. Dudek SM, Jacobson JR, Chiang ET, Birukov KG, Wang P, Zhan X, Garcia JG. Pulmonary endothelial cell barrier enhancement by sphingosine 1-phosphate: roles for cortactin and myosin light chain kinase. J Biol Chem 2004;279(23):24692–24700.
41. Brown M, Adyshev D, Bindokas V, Moitra J, Garcia JG, Dudek SM. Quantitative distribution and colocalization of non-muscle myosin light chain kinase isoforms and cortactin in human lung endothelium. Microvasc Res 2010;80(1):75–88.
42. Wang T, Zhou T, Saadat L, Garcia JG. A MYLK variant regulates asthmatic inflammation via alterations in mRNA secondary structure. Eur J Hum Genet 2015;23(6):874–876.
43. Garcia JG, Liu F, Verin AD, Birukova A, Dechert MA, Gerthoffer WT, Bamberg JR, English D. Sphingosine 1-phosphate promotes endothelial cell barrier integrity by Edg-dependent cytoskeletal rearrangement. J Clin Invest 2001;108(5):689–701.
44. Camp SM, Bittman R, Chiang ET, Moreno-Vinasco L, Mirzapoiazova T, Sammani S, Lu X, et al. Synthetic analogs of FTY720 [2-amino-2-(2-[4-octylphenyl]ethyl)-1,3-propanediol] differentially regulate pulmonary vascular permeability in vivo and in vitro. J Pharmacol Exp Ther 2009;331 (1):54–64.
45. Frech K, Danescu-Mayer J, Werner T. A novel method to develop highly specific models for regulatory units detects a new LTR in GenBank which contains a functional promoter. J Mol Biol 1997;270(5):674–687.
46. Klingenhoff A, Frech K, Quandt K, Werner T. Functional promoter modules can be detected by formal models independent of overall nucleotide sequence similarity. Bioinformatics 1999;15(3):180–186.
47. Wierstra I. Sp1: emerging roles—beyond constitutive activation of TATAless housekeeping genes. Biochem Biophys Res Commun 2008;372(1):1–13.
48. Dudek SM, Garcia JG. Cytoskeletal regulation of pulmonary vascular permeability. J Appl Physiol 2001;91(4):1487–1500.
49. Komarova Y, Malik AB. Regulation of endothelial permeability via paracellular and transcellular transport pathways. Annu Rev Physiol 2010;72:463–493.
50. Grigoryev DN, Finigan JH, Hassoun P, Garcia JG. Science review: searching for gene candidates in acute lung injury. Crit Care 2004;8(6):440–447.
51. Grigoryev DN, Ma SF, Irizarry RA, Ye SQ, Quackenbush J, Garcia JG. Orthologous gene-expression profiling in multi-species models: search for candidate genes. Genome Biol 2004;5(5):R34.
52. Simon BA, Easley RB, Grigoryev DN, Ma SF, Ye SQ, Lavoie T, Tuder RM, Garcia JG. Microarray analysis of regional cellular responses to local mechanical stress in acute lung injury. Am J Physiol Lung Cell Mol Physiol 2006;291(5):L851–L861.
53. Jacobson JR, Dudek SM, Singleton PA, Kolosova IA, Verin AD, Garcia JG. Endothelial cell barrier enhancement by ATP is mediated by the small GTPase Rac and cortactin. Am J Physiol Lung Cell Mol Physiol 2006;291(2):L289–L295.
54. Goldblum SE, Hennig B, Jay M, Yoneda K, McClain CJ. Tumor necrosis factor α–induced pulmonary vascular endothelial injury. Infect Immun 1989;57(4):1218–1226.
55. Hirano S, Rees RS, Yancy SL, Welsh MJ, Remick DG, Yamada T, Hata J, Gilmont RR. Endothelial barrier dysfunction caused by LPS correlates with phosphorylation of HSP27 in vivo. Cell Biol Toxicol 2004;20(1):1–14.
56. Penn MS, Chisolm GM. Relation between lipopolysaccharide-induced endothelial cell injury and entry of macromolecules into the rat aorta in vivo. Circ Res 1991;68(5):1259–1269.
57. Garcia JG, Schaphorst KL. Regulation of endothelial cell gap formation and paracellular permeability. J Investig Med 1995;43(2):117–126.
58. Petrache I, Birukov K, Zaiman AL, Crow MT, Deng H, Wadgaonkar R, Romer LH, Garcia JG. Caspase-dependent cleavage of myosin light chain kinase (MLCK) is involved in TNF-α-mediated bovine pulmonary endothelial cell apoptosis. FASEB J 2003;17(3):407–416.
59. Wadgaonkar R, Linz-McGillem L, Zaiman AL, Garcia JG. Endothelial cell myosin light chain kinase (MLCK) regulates TNFα-induced NFκB activity. J Cell Biochem 2005;94(2):351–364.