Treatment of experimental asthma using a single small molecule with anti-inflammatory and BK channelactivating properties

FASEB Journal

Volumn 27, Issue 12, 2013, Pages 4975-4986

  Goldklang, Monica P ^a,b   Perez Zoghbi, Jose F ^e   Trischler, Jordis ^a   Nkyimbeng, Takwi ^a   Zakharov, Sergey I ^c,d   Shiomi, Takayuki ^a   Zelonina, Tina ^a   Marks, Andrew R ^a   D'Armiento, Jeanine M ^a,b   Marx, Steven O ^c,d  

^a Department of Anesthesiology ^*  (United States)

^b Division of Pulmonary   (United States)

^c Division of Cardiology   (United States)

^d Department of Physiology and Cellular Biophysics ^*  (United States)

^e TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

Author keywords

Airway contractility; Airway smooth muscle; ERK; MAP kinases

Indexed keywords

LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; ROTTLERIN;

AIRWAY RESISTANCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; ASTHMA; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CELL MEMBRANE; CONTROLLED STUDY; DERMATOPHAGOIDES; EX VIVO STUDY; FEMALE; HUMAN; HUMAN CELL; INFLAMMATORY CELL; LUNG LAVAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY TRACT ALLERGY; TH2 CELL;

AIRWAY CONTRACTILITY; AIRWAY SMOOTH MUSCLE; ERK; MAP KINASES;

ACETOPHENONES; ACTION POTENTIALS; ANIMALS; ANTI-INFLAMMATORY AGENTS; ANTIGENS, DERMATOPHAGOIDES; ASTHMA; BENZOPYRANS; CALCIUM SIGNALING; CELLS, CULTURED; FEMALE; HUMANS; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; MICE; MICE, INBRED C57BL; MYOCYTES, SMOOTH MUSCLE; OVALBUMIN; TRACHEA;

EID: 84890474284     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-235176     Document Type: Article

References (55)

1. Fanta, C. H. (2009) Asthma. N. Engl. J. Med. 360, 1002-1014
2. Janssen, L. J., and Killian, K. (2006) Airway smooth muscle as a target of asthma therapy: history and new directions. Respir. Res. 7, 123
3. Liu, Q. H., Zheng, Y. M., Korde, A. S., Yadav, V. R., Rathore, R., Wess, J., and Wang, Y. X. (2009) Membrane depolarization causes a direct activation of G protein-coupled receptors leading to local Ca2+ release in smooth muscle. Proc. Natl. Acad. Sci. U. S. A. 106, 11418-11423
4. Perez, J. F., and Sanderson, M. J. (2005) The frequency of calcium oscillations induced by 5-HT, ACH, and KCl determine the contraction of smooth muscle cells of intrapulmonary bronchioles. J. Gen. Physiol. 125, 535-553
5. Ben-Chaim, Y., Tour, O., Dascal, N., Parnas, I., and Parnas, H. (2003) The M2 muscarinic G-protein-coupled receptor is voltage-sensitive. J. Biol. Chem. 278, 22482-22491
6. Janssen, L. J., Tazzeo, T., Zuo, J., Pertens, E., and Keshavjee, S. (2004) KCl evokes contraction of airway smooth muscle via activation of RhoA and Rho-kinase. Am. J. Physiol. Lung Cell. Mol. Physiol. 287, L852-L858
7. Liu, C., Zuo, J., Pertens, E., Helli, P. B., and Janssen, L. J. (2005) Regulation of Rho/ROCK signaling in airway smooth muscle by membrane potential and [Ca2+]i. Am. J. Physiol. Lung Cell. Mol. Physiol. 289, L574-L582
8. Kotlikoff, M. I., and Kamm, K. E. (1996) Molecular mechanisms of beta-adrenergic relaxation of airway smooth muscle. Annu. Rev. Physiol. 58, 115-141
9. Butler, A., Tsunoda, S., McCobb, D. P., Wei, A., and Salkoff, L. (1993) mSlo, a complex mouse gene encoding "maxi" calciumactivated potassium channels. Science 261, 221-224
10. Knaus, H. G., Garcia-Calvo, M., Kaczorowski, G. J., and Garcia, M. L. (1994) Subunit composition of the high conductance calcium-activated potassium channel from smooth muscle, a representative of the mSlo and slowpoke family of potassium channels. J. Biol. Chem. 269, 3921-3924
11. Semenov, I., Wang, B., Herlihy, J. T., and Brenner, R. (2006) BK channel beta1-subunit regulation of calcium handling and constriction in tracheal smooth muscle. Am. J. Physiol. Lung Cell. Mol. Physiol. 291, L802-L810
12. Seibold, M. A., Wang, B., Eng, C., Kumar, G., Beckman, K. B., Sen, S., Choudhry, S., Meade, K., Lenoir, M., Watson, H. G., Thyne, S., Williams, L. K., Kumar, R., Weiss, K. B., Grammer, L. C., Avila, P. C., Schleimer, R. P., Burchard, E. G., and Brenner, R. (2008) An african-specific functional polymorphism in KCNMB1 shows sex-specific association with asthma severity. Hum. Mol. Genet. 17, 2681-2690
13. Zakharov, S. I., Morrow, J. P., Liu, G., Yang, L., and Marx, S. O. (2005) Activation of the BK (SLO1) potassium channel by mallotoxin. J. Biol. Chem. 280, 30882-30887
14. Springael, C., Thomas, S., Rahmouni, S., Vandamme, A., Goldman, M., Willems, F., and Vosters, O. (2007) Rottlerin inhibits human T cell responses. Biochem. Pharmacol. 73, 515-525
15. Townsend, E. A., Thompson, M. A., Pabelick, C. M., and Prakash, Y. S. (2010) Rapid effects of estrogen on intracellular Ca2+ regulation in human airway smooth muscle. Am. J. Physiol. Lung Cell. Mol. Physiol. 298, L521-L530
16. Johnson, J. R., Wiley, R. E., Fattouh, R., Swirski, F. K., Gajewska, B. U., Coyle, A. J., Gutierrez-Ramos, J. C., Ellis, R., Inman, M. D., and Jordana, M. (2004) Continuous exposure to house dust mite elicits chronic airway inflammation and structural remodeling. Am. J. Respir. Crit. Care Med. 169, 378-385
17. Henderson, W. R., Jr., Tang, L. O., Chu, S. J., Tsao, S. M., Chiang, G. K., Jones, F., Jonas, M., Pae, C., Wang, H., and Chi, E. Y. (2002) A role for cysteinyl leukotrienes in airway remodeling in a mouse asthma model. Am. J. Respir. Crit. Care Med. 165, 108-116
18. Perez-Zoghbi, J. F., Bai, Y., and Sanderson, M. J. (2010) Nitric oxide induces airway smooth muscle cell relaxation by decreasing the frequency of agonist-induced Ca2+ oscillations. J. Gen. Physiol. 135, 247-259
19. Sanderson, M. J., and Parker, I. (2003) Video-rate confocal microscopy. Methods Enzymol. 360, 447-481
20. Wang, J., Homer, R. J., Chen, Q., and Elias, J. A. (2000) Endogenous and exogenous IL-6 inhibit aeroallergen-induced Th2 inflammation. J. Immunol. 165, 4051-4061
21. Neuhaus-Steinmetz, U., Glaab, T., Daser, A., Braun, A., Lommatzsch, M., Herz, U., Kips, J., Alarie, Y., and Renz, H. (2000) Sequential development of airway hyperresponsiveness and acute airway obstruction in a mouse model of allergic inflammation. Int. Arch. Allergy Immunol. 121, 57-67
22. Mehra, D., Sternberg, D. I., Jia, Y., Canfield, S., Lemaitre, V., Nkyimbeng, T., Wilder, J., Sonett, J., and D'Armiento, J. (2010) Altered lymphocyte trafficking and diminished airway reactivity in transgenic mice expressing human MMP-9 in a mouse model of asthma. Am. J. Physiol. Lung Cell. Mol. Physiol. 298, L189-L196
23. Cho, S. H., Woo, C. H., Yoon, S. B., and Kim, J. H. (2004) Protein kinase Cdelta functions downstream of Ca2+ mobilization in FcepsilonRI signaling to degranulation in mast cells. J. Allergy Clin. Immunol. 114, 1085-1092
24. Blacquiere, M. J., Hylkema, M. N., Postma, D. S., Geerlings, M., Timens, W., and Melgert, B. N. (2010) Airway inflammation and remodeling in two mouse models of asthma: comparison of males and females. Int. Arch. Allergy Immunol. 153, 173-181
25. Taylor, A., Verhagen, J., Blaser, K., Akdis, M., and Akdis, C. A. (2006) Mechanisms of immune suppression by interleukin-10 and transforming growth factor-beta: the role of T regulatory cells. Immunology 117, 433-442
26. Jaffar, Z., Sivakuru, T., and Roberts, K. (2004) CD4+CD25+ T cells regulate airway eosinophilic inflammation by modulating the Th2 cell phenotype. J. Immunol. 172, 3842-3849
27. Fattouh, R., Al-Garawi, A., Fattouh, M., Arias, K., Walker, T. D., Goncharova, S., Coyle, A. J., Humbles, A. A., and Jordana, M. (2011) Eosinophils are dispensable for allergic remodeling and immunity in a model of house dust mite-induced airway disease. Am. J. Respir. Crit. Care Med. 183, 179-188
28. Naureckas, E. T., Ndukwu, I. M., Halayko, A. J., Maxwell, C., Hershenson, M. B., and Solway, J. (1999) Bronchoalveolar lavage fluid from asthmatic subjects is mitogenic for human airway smooth muscle. Am. J. Respir. Crit. Care Med. 160, 2062-2066
29. Lee, J. H., Johnson, P. R., Roth, M., Hunt, N. H., and Black, J. L. (2001) ERK activation and mitogenesis in human airway smooth muscle cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 280, L1019-L1029
30. Eynott, P. R., Nath, P., Leung, S. Y., Adcock, I. M., Bennett, B. L., and Chung, K. F. (2003) Allergen-induced inflammation and airway epithelial and smooth muscle cell proliferation: role of Jun N-terminal kinase. Brit. J. Pharmacol. 140, 1373-1380
31. Zhou, X. B., Wulfsen, I., Lutz, S., Utku, E., Sausbier, U., Ruth, P., Wieland, T., and Korth, M. (2008) M2 muscarinic receptors induce airway smooth muscle activation via a dual, Gbetagamma-mediated inhibition of large conductance Ca2-activated K-channel activity. J. Biol. Chem. 283, 21036-21044
32. Kume, H., Mikawa, K., Takagi, K., and Kotlikoff, M. I. (1995) Role of G proteins and KCa channels in the muscarinic and beta-adrenergic regulation of airway smooth muscle. Am. J. Physiol. Lung Cell. Mol. Physiol. 268, L221-L229
33. Semenov, I., Wang, B., Herlihy, J. T., and Brenner, R. (2011) BK channel beta1 subunits regulate airway contraction secondary to M2 muscarinic acetylcholine receptor mediated depolarization. J. Physiol. 589, 1803-1817
34. Barnes, P. J. (1985) Clinical studies with calcium antagonists in asthma. Br. J. Clin. Pharmacol. 20(Suppl. 2), 289S-298S 35. Janssen, L. J. (1997) T-type and L-type Ca2+ currents in canine bronchial smooth muscle: characterization and physiological roles. Am. J. Physiol. Cell Physiol. 272, C1757-C1765
35. Gschwendt, M., Muller, H. J., Kielbassa, K., Zang, R., Kittstein, W., Rincke, G., and Marks, F. (1994) Rottlerin, a novel protein kinase inhibitor. Biochem. Biophys. Res. Commun. 199, 93-98
36. Soltoff, S. P. (2007) Rottlerin: an inappropriate and ineffective inhibitor of PKCdelta. Trends Pharmacol. Sci. 28, 453-458
37. Davies, S. P., Reddy, H., Caivano, M., and Cohen, P. (2000) Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351, 95-105
38. Soltoff, S. P. (2001) Rottlerin is a mitochondrial uncoupler that decreases cellular ATP levels and indirectly blocks protein kinase Cdelta tyrosine phosphorylation. J. Biol. Chem. 276, 37986-37992
39. Langlois, A., Chouinard, F., Flamand, N., Ferland, C., Rola-Pleszczynski, M., and Laviolette, M. (2009) Crucial implication of protein kinase C (PKC)-delta, PKC-zeta, ERK-1/2, and p38 MAPK in migration of human asthmatic eosinophils. J. Leukoc. Biol. 85, 656-663
40. Schubl, S., Tsai, S., Ryer, E. J., Wang, C., Hu, J., Kent, K. C., and Liu, B. (2009) Upregulation of protein kinase cdelta in vascular smooth muscle cells promotes inflammation in abdominal aortic aneurysm. J. Surg. Res. 153, 181-187
41. Roose, J. P., Mollenauer, M., Gupta, V. A., Stone, J., and Weiss, A. (2005) A diacylglycerol-protein kinase C-RasGRP1 pathway directs Ras activation upon antigen receptor stimulation of T cells. Mol. Cell. Biol. 25, 4426-4441
42. Lee, J. S., Kim, I. S., Ryu, J. S., and Yun, C. Y. (2008) House dust mite, Dermatophagoides pteronissinus increases expression of MCP-1, IL-6, and IL-8 in human monocytic THP-1 cells. Cytokine 42, 365-371
43. Liu, W., Liang, Q., Balzar, S., Wenzel, S., Gorska, M., and Alam, R. (2008) Cell-specific activation profile of extracellular signalregulated kinase 1/2, Jun N-terminal kinase, and p38 mitogenactivated protein kinases in asthmatic airways. J. Allergy Clin. Immunol. 121, 893-902 e892
44. Grunstein, M. M., Veler, H., Shan, X., Larson, J., Grunstein, J. S., and Chuang, S. (2005) Proasthmatic effects and mechanisms of action of the dust mite allergen, Der p 1, in airway smooth muscle. J. Allergy Clin. Immunol. 116, 94-101
45. Miura, K., Schroeder, J. T., Hubbard, W. C., and MacGlashan, D. W., Jr. (1999) Extracellular signal-regulated kinases regulate leukotriene C4 generation, but not histamine release or IL-4 production from human basophils. J. Immunol. 162, 4198-4206
46. Bates, M. E., Green, V. L., and Bertics, P. J. (2000) ERK1 and ERK2 activation by chemotactic factors in human eosinophils is interleukin 5-dependent and contributes to leukotriene C(4) biosynthesis. J. Biol. Chem. 275, 10968-10975
47. Moore, P. E., Church, T. L., Chism, D. D., Panettieri, R. A., Jr. and Shore, S. A. (2002) IL-13 and IL-4 cause eotaxin release in human airway smooth muscle cells: a role for ERK. Am. J. Physiol. Lung Cell. Mol. Physiol. 282, L847-L853
48. Kampen, G. T., Stafford, S., Adachi, T., Jinquan, T., Quan, S., Grant, J. A., Skov, P. S., Poulsen, L. K., and Alam, R. (2000) Eotaxin induces degranulation and chemotaxis of eosinophils through the activation of ERK2 and p38 mitogen-activated protein kinases. Blood 95, 1911-1917
49. Hallsworth, M. P., Moir, L. M., Lai, D., and Hirst, S. J. (2001) Inhibitors of mitogen-activated protein kinases differentially regulate eosinophil-activating cytokine release from human airway smooth muscle. Am. J. Respir. Crit. Care Med. 164, 688-697
50. Duan, W., Chan, J. H., Wong, C. H., Leung, B. P., and Wong, W. S. (2004) Anti-inflammatory effects of mitogen-activated protein kinase kinase inhibitor U0126 in an asthma mouse model. J. Immunol. 172, 7053-7059
51. Goplen, N., Karim, Z., Guo, L., Zhuang, Y., Huang, H., Gorska, M. M., Gelfand, E., Pages, G., Pouyssegur, J., and Alam, R. (2012) ERK1 is important for Th2 differentiation and development of experimental asthma. FASEB J. 26, 1934-1945
52. Alrashdan, Y. A., Alkhouri, H., Chen, E., Lalor, D. J., Poniris, M., Henness, S., Brightling, C. E., Burgess, J. K., Armour, C. L., Ammit, A. J., and Hughes, J. M. (2012) Asthmatic airway smooth muscle CXCL10 production: mitogen-activated protein kinase JNK involvement. Am. J. Physiol. Lung Cell. Mol. Physiol. 302, L1118-L1127
53. Tan, X., Alrashdan, Y. A., Alkhouri, H., Oliver, B. G., Armour, C. L., and Hughes, J. M. (2013) Airway smooth muscle CXCR3 ligand production: regulation by JAK-STAT1 and intracellular calcium. Am. J. Physiol. Lung Cell. Mol. Physiol. 304, L790-L802
54. Gujral, M. L., Varma, D. R., Sareen, K. N., and Roy, A. K. (1960) Oral contraceptives. Part II. Antifertility effect of Mallotus philippinensis Mueller-Argoviensis. Indian J. Med. Res. 48, 52-58
55. Zhang, D., Anantharam, V., Kanthasamy, A., and Kanthasamy, A. G. (2007) Neuroprotective effect of protein kinase C delta inhibitor rottlerin in cell culture and animal models of Parkinson's disease. J. Pharmacol. Exp. Ther. 322, 913-922