An RGS4-mediated phenotypic switch of bronchial smooth muscle cells promotes fixed airway obstruction in asthma

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Damera, Gautam ^a   Druey, Kirk M ^b   Cooper, Philip R ^a   Krymskaya, Vera P ^a   Soberman, Roy J ^c   Amrani, Yassine ^d   Hoshi, Toshinori ^e   Brightling, Christopher E ^d   Panettieri, Reynold A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF LEICESTER   (United Kingdom)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN COUPLED RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; RGS4 PROTEIN; CARBACHOL; MITOGENIC AGENT; PLATELET DERIVED GROWTH FACTOR; PROTEIN KINASE B; RGS PROTEIN;

ADULT; AIRWAY OBSTRUCTION; ARTICLE; ASTHMA; BRONCHOSPASM; BRONCHUS BIOPSY; BRONCHUS MUSCLE; CALCIUM MOBILIZATION; CELL COUNT; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; EXCITATION CONTRACTION COUPLING; FEMALE; FORCED EXPIRATORY VOLUME; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; LUNG FUNCTION; MALE; PHENOTYPIC PLASTICITY; PROTEIN EXPRESSION; PROTEIN FUNCTION; SMOOTH MUSCLE CONTRACTION; BIOLOGICAL MODEL; BRONCHUS; DRUG EFFECT; ENZYMOLOGY; METABOLISM; MIDDLE AGED; PATHOLOGY; PATHOPHYSIOLOGY; PHENOTYPE; SMOOTH MUSCLE FIBER; SPUTUM;

AIRWAY OBSTRUCTION; ASTHMA; BRONCHI; BRONCHOCONSTRICTION; CARBACHOL; CELL PROLIFERATION; EXCITATION CONTRACTION COUPLING; FEMALE; HUMANS; MALE; MIDDLE AGED; MITOGENS; MODELS, BIOLOGICAL; MYOCYTES, SMOOTH MUSCLE; PHENOTYPE; PHOSPHATIDYLINOSITOL 3-KINASES; PLATELET-DERIVED GROWTH FACTOR; PROTO-ONCOGENE PROTEINS C-AKT; RGS PROTEINS; SPUTUM;

EID: 84855791275     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0028504     Document Type: Article

References (41)

1. Tliba O, Panettieri RA Jr, (2009) Noncontractile functions of airway smooth muscle cells in asthma. Annu Rev Physiol 71: 509-535.
2. Panettieri RA Jr, Covar R, Grant E, Hillyer EV, Bacharier L, (2008) Natural history of asthma: persistence versus progression-does the beginning predict the end? J Allergy Clin Immunol 121: 607-613.
3. Chamley-Campbell J, Campbell GR, Ross R, (1979) The smooth muscle cell in culture. Physiol Rev 59: 1-61.
4. Owens GK, (1995) Regulation of differentiation of vascular smooth muscle cells. Physiol Rev 75: 487-517.
5. Gabella G, (1976) Quantitative morphological study of smooth muscle cells of the guinea-pig taenia coli. Cell Tissue Res 170: 161-186.
6. Gabella G, (1989) Development of smooth muscle: ultrastructural study of the chick embryo gizzard. Anat Embryol (Berl) 180: 213-226.
7. Thyberg J, Roy J, Tran PK, Blomgren K, Dumitrescu A, et al. (1997) Expression of caveolae on the surface of rat arterial smooth muscle cells is dependent on the phenotypic state of the cells. Lab Invest 77: 93-101.
8. Willars GB, (2006) Mammalian RGS proteins: multifunctional regulators of cellular signalling. Semin Cell Dev Biol 17: 363-376.
9. Bansal G, Xie Z, Rao S, Nocka KH, Druey KM, (2008) Suppression of immunoglobulin E-mediated allergic responses by regulator of G protein signaling 13. Nat Immunol 9: 73-80.
10. Vanhaesebroeck B, Guillermet-Guibert J, Graupera M, Bilanges B, (2010) The emerging mechanisms of isoform-specific PI3K signalling. Nat Rev Mol Cell Biol 11: 329-341.
11. Engelman JA, Luo J, Cantley LC, (2006) The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat Rev Genet 7: 606-619.
12. Liang G, Bansal G, Xie Z, Druey KM, (2009) RGS16 inhibits breast cancer cell growth by mitigating phosphatidylinositol 3-kinase signaling. J Biol Chem 284: 21719-21727.
13. Brightling CE, Bradding P, Symon FA, Holgate ST, Wardlaw AJ, et al. (2002) Mast-cell infiltration of airway smooth muscle in asthma. N Engl J Med 346: 1699-1705.
14. Bansal G, Druey KM, Xie Z, (2007) R4 RGS proteins: regulation of G-protein signaling and beyond. Pharmacol Ther 116: 473-495.
15. Cooper PR, Panettieri RA Jr, (2008) Steroids completely reverse albuterol-induced beta2-adrenergic receptor tolerance in human small airways. J Allergy Clin Immunol 122: 734-740.
16. Bernstein LS, Grillo AA, Loranger SS, Linder ME, (2000) RGS4 binds to membranes through an amphipathic alpha helix. J Biol Chem 275: 18520-18526.
17. Krymskaya VP, Orsini MJ, Eszterhas AJ, Brodbeck KC, Benovic JL, et al. (2000) Mechanisms of proliferation synergy by receptor tyrosine kinase and G protein-coupled receptor activation in human airway smooth muscle. Am J Respir Cell Mol Biol 23: 546-554.
18. Krymskaya VP, Goncharova EA, Ammit AJ, Lim PN, Goncharov DA, et al. (2005) Src is necessary and sufficient for human airway smooth muscle cell proliferation and migration. FASEB J 19: 428-430.
19. Chiou YL, Shieh JJ, Lin CY, (2006) Blocking of Akt/NF-kappaB signaling by pentoxifylline inhibits platelet-derived growth factor-stimulated proliferation in Brown Norway rat airway smooth muscle cells. Pediatr Res 60: 657-662.
20. Hirst SJ, Martin JG, Bonacci JV, Chan V, Fixman ED, et al. (2004) Proliferative aspects of airway smooth muscle. J Allergy Clin Immunol 114: S2-S17.
21. Takuwa N, Fukui Y, Takuwa Y, (1999) Cyclin D1 expression mediated by phosphatidylinositol 3-kinase through mTOR-p70(S6K)-independent signaling in growth factor-stimulated NIH 3T3 fibroblasts. Mol Cell Biol 19: 1346-1358.
22. Owen VJ, Burton PB, Mullen AJ, Birks EJ, Barton P, et al. (2001) Expression of RGS3, RGS4 and Gi alpha 2 in acutely failing donor hearts and end-stage heart failure. Eur Heart J 22: 1015-1020.
23. Rogers JH, Tamirisa P, Kovacs A, Weinheimer C, Courtois M, et al. (1999) RGS4 causes increased mortality and reduced cardiac hypertrophy in response to pressure overload. J Clin Invest 104: 567-576.
24. Moore WC, Peters SP, (2006) Severe asthma: an overview. J Allergy Clin Immunol 117: 487-494.
25. Brasier AR, Victor S, Boetticher G, Ju H, Lee C, et al. (2008) Molecular phenotyping of severe asthma using pattern recognition of bronchoalveolar lavage-derived cytokines. J Allergy Clin Immunol 121: 30-37.
26. Wenzel SE, Schwartz LB, Langmack EL, Halliday JL, Trudeau JB, et al. (1999) Evidence that severe asthma can be divided pathologically into two inflammatory subtypes with distinct physiologic and clinical characteristics. Am J Respir Crit Care Med 160: 1001-1008.
27. Chanez P, Wenzel SE, Anderson GP, Anto JM, Bel EH, et al. (2007) Severe asthma in adults: what are the important questions? J Allergy Clin Immunol 119: 1337-1348.
28. Sorkness RL, Bleecker ER, Busse WW, Calhoun WJ, Castro M, et al. (2008) Lung function in adults with stable but severe asthma: air trapping and incomplete reversal of obstruction with bronchodilation. J Appl Physiol 104: 394-403.
29. Hollinger S, Hepler JR, (2002) Cellular regulation of RGS proteins: modulators and integrators of G protein signaling. Pharmacol Rev 54: 527-559.
30. Cho H, Harrison K, Schwartz O, Kehrl JH, (2003) The aorta and heart differentially express RGS (regulators of G-protein signalling) proteins that selectively regulate sphingosine 1-phosphate, angiotensin II and endothelin-1 signalling. Biochem J 371: 973-980.
31. Cho H, Kozasa T, Bondjers C, Betsholtz C, Kehrl JH, (2003) Pericyte-specific expression of RGS5: implications for PDGF and EDG receptor signaling during vascular maturation. FASEB J 17: 440-442.
32. Derrien A, Zheng B, Osterhout JL, Ma YC, Milligan G, et al. (2003) Src-mediated RGS16 tyrosine phosphorylation promotes RGS16 stability. J Biol Chem 278: 16107-16116.
33. Sambi BS, Hains MD, Waters CM, Connell MC, Willard FS, et al. (2006) The effect of RGS12 on PDGFbeta receptor signalling to p42/p44 mitogen activated protein kinase in mammalian cells. Cell Signal 18: 971-981.
34. Hurst JH, Mendpara N, Hooks SB, (2009) Regulator of G-protein signalling expression and function in ovarian cancer cell lines. Cell Mol Biol Lett 14: 153-174.
35. Harris DM, Cohn HI, Pesant S, Eckhart AD, (2008) GPCR signalling in hypertension: role of GRKs. Clin Sci (Lond) 115: 79-89.
36. Heximer SP, Knutsen RH, Sun X, Kaltenbronn KM, Rhee MH, et al. (2003) Hypertension and prolonged vasoconstrictor signaling in RGS2-deficient mice. J Clin Invest 111: 1259.
37. Castro M, Rubin AS, Laviolette M, Fiterman J, De Andrade Lima M, et al. (2010) Effectiveness and safety of bronchial thermoplasty in the treatment of severe asthma: a multicenter, randomized, double-blind, sham-controlled clinical trial. Am J Respir Crit Care Med 181: 116-124.
38. Cox G, Thomson NC, Rubin AS, Niven RM, Corris PA, et al. (2007) Asthma control during the year after bronchial thermoplasty. N Engl J Med 356: 1327-1337.
39. Neubig RR, (2008) And the winner is: RGS4! Circ Res 103: 444-446.
40. O'Brien M, Morrison JJ, Smith TJ, (2008) Upregulation of PSCDBP, TLR2, TWIST1, FLJ35382, EDNRB, and RGS12 gene expression in human myometrium at labor. Reprod Sci 15: 382-393.
41. Salomonis N, Cotte N, Zambon AC, Pollard KS, Vranizan K, et al. (2005) Identifying genetic networks underlying myometrial transition to labor. Genome Biol 6: R12.