Cytokine-induced iNOS and ERK1/2 inhibit adenylyl cyclase type 5/6 activity and stimulate phosphodiesterase 4D5 activity in intestinal longitudinal smooth muscle

American Journal of Physiology - Cell Physiology

Volumn 307, Issue 4, 2014, Pages

  Mahavadi, Sunila ^a   Nalli, Ancy D ^a   Kumar, Divya P ^a   Hu, Wenhui ^b   Kuemmerle, John F ^a   Grider, John R ^a   Murthy, Karnam S ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Inflammation; Muscle relaxation; Phosphodiesterases; Protein kinase A; S nitrosylation

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; ADENYLATE CYCLASE; ADENYLATE CYCLASE 5; ADENYLATE CYCLASE 6; CYCLIC AMP; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; LYASE; MITOGEN ACTIVATED PROTEIN KINASE 1; N [3 (AMINOMETHYL)BENZYL]ACETAMIDINE; PHOSPHODIESTERASE; PHOSPHODIESTERASE 4D5; PHOSPHODIESTERASE IV; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; COLITIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; IN VITRO STUDY; INTESTINAL DYSMOTILITY; INTESTINE MUSCLE; MOUSE; NITROSYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMOOTH MUSCLE FIBER; SMOOTH MUSCLE RELAXATION;

INFLAMMATION; MUSCLE RELAXATION; PHOSPHODIESTERASES; PROTEIN KINASE A; S-NITROSYLATION;

ADENYLATE CYCLASE; ANIMALS; COLITIS; COLON; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 4; CYTOKINES; DISEASE MODELS, ANIMAL; DOWN-REGULATION; ENZYME ACTIVATION; ENZYME INHIBITORS; GASTROINTESTINAL MOTILITY; INFLAMMATION MEDIATORS; INTERLEUKIN-1BETA; MALE; MICE; MICE, INBRED C57BL; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MUSCLE RELAXATION; MUSCLE, SMOOTH; NITRIC OXIDE SYNTHASE TYPE II; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRINITROBENZENESULFONIC ACID; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

EID: 84907646162     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00123.2014     Document Type: Article

References (50)

1. Al-Shboul O, Nalli AD, Kumar DP, Mahavadi S, Kuemmerle JF, Grider JR, Murthy KS. Jun kinase-induced overexpression of leukemiaassociated RhoGEF (LARG) mediates sustained hypercontraction of longitudinal smooth muscle in inflammation. Am J Physiol Cell Physiol 306: C1129-C1141, 2014.
2. Baillie GS, MacKenzie SJ, Houslay MD. Phorbol 12-myristate 13-acetate triggers the protein kinase A-mediated phosphorylation and activation of the PDE4D5 cAMP phosphodiesterase in human aortic smooth muscle cells through a route involving extracellular signal regulated kinase (ERK). Mol Pharmacol 60: 1100-1111, 2001.
3. Baillie GS, MacKenzie SJ, McPhee I, Houslay MD. Sub-family selective actions in the ability of Erk2 MAP kinase to phosphorylate and regulate the activity of PDE4 cyclic AMP-specific phosphodiesterases. Br J Pharmacol 131: 811-819, 2000.
4. Cao W, Vrees MD, Potenti FM, Harnett KM, Fiocchi C, Pricolo VE. Interleukin 1β-induced production of H2O2 contributes to reduced sigmoid colonic circular smooth muscle contractility in ulcerative colitis. J Pharmacol Exp Ther 311: 60-70, 2004.
5. Conti M, Jin SL. The molecular biology of cyclic nucleotide phosphodiesterases. Prog Nucleic Acid Res Mol Biol 63: 1-38, 1999.
6. Cooper DM. Regulation and organization of adenylyl cyclases and cAMP. Biochem J 375: 517-529, 2003.
7. de Godoy MA, Rattan S. Role of rho kinase in the functional and dysfunctional tonic smooth muscles. Trends Pharmacol Sci 32: 384-393, 2011.
8. Ekholm D, Belfrage P, Manganiello V, Degerman E. Protein kinase A-dependent activation of PDE4 (cAMP-specific cyclic nucleotide phosphodiesterase) in cultured bovine vascular smooth muscle cells. Biochim Biophys Acta 1356: 64-70, 1997.
9. Francis SH, Turko IV, Corbin JD. Cyclic nucleotide phosphodiesterases: relating structure and function. Prog Nucleic Acid Res Mol Biol 65: 1-52, 2000.
10. Grider JR, Makhlouf GM. Contraction mediated by Ca2+ release in circular and Ca2+ influx in longitudinal intestinal muscle cells. J Pharmacol Exp Ther 244: 432-437, 1988.
11. Hacker BM, Tomlison JE, Wayman GA, Sultana R, Villacres E, Disteche C, Storm DR. Cloning, chromosomal mapping and regulatory properties of human type 9 adenylyl cyclase (ADCY9). Genomics 50: 97-104, 1998.
12. Hazelgrove KB, Flynn RS, Qiao LY, Grider JR, Kuemmerle JF. Endogenous IGF-I and αvβ3 integrin ligands regulate increased smooth muscle growth in TNBS-induced colitis. Am J Physiol Gastrointest Liver Physiol 296: G1230-G1237, 2009.
13. Hill EV, Houslay MD, Baillie GS. Investigation of extracellular signalregulated kinase 2 mitogen-activated protein kinase phosphorylation and regulation of activity of PDE4 cyclic adenosine monophosphate-specific phosphodiesterases. Methods Mol Biol 307: 225-237, 2005.
14. Hill EV, Sheppard CL, Cheung YF, Gall I, Krause E, Houslay MD. Oxidative stress employs phosphatidyl inositol 3-kinase and ERK signalling pathways to activate cAMP phosphodiesterase-4D3 (PDE4D3) through multisite phosphorylation at Ser239 and Ser579. Cell Signal 18: 2056-2069, 2006.
15. Hoffmann R, Baillie GS, MacKenzie SJ, Yarwood SJ, Houslay MD. The MAP kinase ERK2 inhibits the cyclic AMP-specific phosphodiesterase HSPDE4D3 by phosphorylating it at Ser579. EMBO J 18: 893-903, 1999.
16. Houslay MD, Adams DR. PDE4 cAMP phosphodiesterases: modular enzymes that orchestrate signalling cross-talk, desensitization and compartmentalization. Biochem J 370: 1-18, 2003.
17. Houslay MD, Baillie GS. The role of ERK2 docking and phosphorylation of PDE4 cAMP phosphodiesterase isoforms in mediating cross-talk between the cAMP and ERK signalling pathways. Biochem Soc Trans 31: 1186-1190, 2003.
18. Houslay MD, Kolch W. Cell-type specific integration of cross-talk between extracellular signal-regulated kinase and cAMP signaling. Mol Pharmacol 58: 659-668, 2000.
19. Hu W, Li F, Mahavadi S, Murthy KS. Upregulation of RGS4 and downregulation of CPI-17 mediate inhibition of colonic smooth muscle contraction by interleukin-1β. Am J Physiol Cell Physiol 293: C1991-C2000, 2007.
20. Hu W, Li F, Mahavadi S, Murthy KS. Interleukin-1β up-regulates RGS4 through the canonical IKK2/IκBα/NF-κB pathway in rabbit colonic smooth muscle. Biochem J 412: 35-43, 2008.
21. Hu W, Li F, Mahavadi S, Murthy KS. Upregulation of RGS4 expression by IL-1β in colonic smooth muscle is enhanced by ERK1/2 and p38 MAPK and inhibited by the PI3K/Akt/GSK3β pathway. Am J Physiol Cell Physiol 296: C1310-C1320, 2009.
22. Iwami G, Kawabe J, Ebina T, Cannon PJ, Homcy CJ, Ishikawa Y. Regulation of adenylyl cyclase by protein kinase A. J Biol Chem 270: 12481-12484, 1995.
23. Khan WI, Collins SM. Gut motor function: immunological control in enteric infection and inflammation. Clin Exp Immunol 143: 389-397, 2006.
24. Kuemmerle JF, Makhlouf GM. Agonist-stimulated cyclic ADP ribose: endogenous modulator of Ca2+-induced Ca2+-release in intestinal longitudinal muscle. J Biol Chem 270: 25488-25494, 1995.
25. Kuemmerle JF, Murthy KS, Makhlouf GM. Longitudinal smooth muscle of the mammalian intestine: a model for Ca2+ signaling by cADPR. Cell Biochem Biophys 28: 31-44, 1998.
26. Lim J, Pahlke G, Conti M. Activation of the cAMP-specific phosphodiesterase PDE4D3 by phosphorylation. Identification and function of an inhibitory domain. J Biol Chem 274: 19677-19685, 1999.
27. Liu H, Maurice DH. Phosphorylation-mediated activation and translocation of the cyclic AMP-specific phosphodiesterase PDE4D3 by cyclic AMP-dependent protein kinase and mitogen-activated protein kinases. A potential mechanism allowing for the coordinated regulation of PDE4D activity and targeting. J Biol Chem 274: 10557-10565, 1999.
28. Liu H, Palmer D, Jimmo SL, Tilley DG, Dunkerley HA, Pang SC, Maurice DH. Expression of phosphodiesterase 4D (PDE4D) is regulated by both the cyclic AMP-dependent protein kinase and mitogen-activated protein kinase signaling pathways. A potential mechanism allowing for the coordinated regulation of PDE4D activity and expression in cells. J Biol Chem 275: 26615-26624, 2000.
29. MacKenzie SJ, Baillie GS, McPhee I, Bolger GB, Houslay MD. ERK2 mitogen-activated protein kinase binding, phosphorylation, and regulation of the PDE4D cAMP-specific phosphodiesterases. The involvement of COOH-terminal docking sites and NH2-terminal UCR regions. J Biol Chem 275: 16609-16617, 2000.
30. MacKenzie SJ, Baillie GS, McPhee I, MacKenzie C, Seamons R, McSorley T, Millen J, Beard MB, van Heeke G, Houslay MD. Long PDE4 cAMP specific phosphodiesterases are activated by protein kinase A-mediated phosphorylation of a single serine residue in upstream conserved region 1 (UCR1). Br J Pharmacol 136: 421-433, 2002.
31. Murthy KS. Signaling for contraction and relaxation in smooth muscle of the gut. Annu Rev Physiol 68: 345-374, 2006.
32. Murthy KS, Grider JR, Makhlouf GM. InsP3-dependent Ca2+ mobilization in circular but not longitudinal muscle cells of intestine. Am J Physiol Gastrointest Liver Physiol 261: G937-G944, 1991.
33. Murthy KS, Kuemmerle JF, Makhlouf GM. Release of arachidonic acid by agonist-mediated activation of PLA2 initiates Ca2+ mobilization in intestinal smooth muscle. Am J Physiol Gastrointest Liver Physiol 269: G93-G102, 1995.
34. Murthy KS, Makhlouf GM. Regulation of adenylyl cylase type V/VI in smooth muscle: interplay of inhibitory G protein and Ca2+ influx. Mol Pharmacol 54: 122-128, 1998.
35. Murthy KS, Makhlouf GM. Differential coupling of muscarinic m2 and m3 receptors to adenylyl cyclases V/VI in smooth muscle. Concurrent M2-mediated inhibition via Gαi3 and m3-mediated stimulation via Gβ. J Biol Chem 272: 21317-21324, 1997.
36. Murthy KS, Zhou H, Grider JR, Brautigan DL, Eto M, Makhlouf GM. Differential signaling by m3 and m2 receptors in smooth muscle: m2-mediated inactivation of MLCK via Gi3, Cdc42/Rac1, and PAK1, and m3-mediated MLC20 phosphorylation via Rho kinase/MYPT1 and PKC/ CPI-17 pathways. Biochem J 374: 145-155, 2003.
37. Murthy KS, Zhou H, Makhlouf GM. PKA-dependent inactivation of PDE3A and PDE4 and inhibition of adenylyl cyclase V/VI in smooth muscle. Am J Physiol Cell Physiol 282: C508-C517, 2002.
38. Murthy KS, Sriwai W. Stimulatory phosphorylation of cAMP-specific PDE4D5 by contractile agonists is mediated by PKC-dependent inactivation of protein phosphatase 2A. Am J Physiol Gastrointest Liver Physiol 294: G327-G335, 2008.
39. Nalli AD, Kumar DP, Mahavadi S, Alshboul O, Alkhatani R, Kuemmerle JF, Grider JR, Murthy KS. Hypercontractility of intestinal longitudinal smooth muscle induced by cytokines is mediated by NFκB/ AMP-kinase/MLC kinase pathway. J Pharmacol Exp Therap 350: 89-98, 2014.
40. Ohama T, Hori M, Sato K, Ozaki H, Karaki H. Chronic treatment with interleukin-1β attenuates contractions by decreasing the activities of CPI-17 and MYPT-1 in intestinal smooth muscle. J Biol Chem 278: 48794-48804, 2003.
41. Ohama T, Hori M, Ozaki H. Mechanism of abnormal intestinal motility in inflammatory bowel disease: how smooth muscle contraction is reduced. J Smooth Muscle Res 43: 43-54, 2007.
42. Sette C, Conti M. Phosphorylation and activation of a cAMP-specific phosphodiesterase by the cAMP-dependent protein kinase. Involvement of serine 54 in the enzyme activation. J Biol Chem 271: 16526-16534, 1996.
43. Shea-Donohue T, Notari L, Sun R, Zhao A. Mechanisms of smooth muscle responses to inflammation. Neurogastroenterol Motil 24: 802-811, 2012.
44. Shi XZ, Lindholm PF, Sarna SK. NF-kappa B activation by oxidative stress and inflammation suppresses contractility in colonic circular smooth muscle cells. Gastroenterology 124: 1369-1380, 2003.
45. Shi XZ, Sarna SK. Transcriptional regulation of inflammatory mediators secreted by human colonic circular smooth muscle cells. Am J Physiol Gastrointest Liver Physiol 289: G274-G284, 2005.
46. Soderling SH, Beavo JA. Regulation of cAMP and cGMP signaling: new phosphodiesterases and new functions. Curr Opin Cell Biol 12: 174-179, 2000.
47. Sunahara RK, Dessauer CW, Gliman AG. Complexity and diversity of mammalian adenylyl cylcases. Annu Rev Pharmacol Toxicol 36: 461-480, 1996.
48. Taussig R, Gliman AG. Mammalian membrane-bound adenylyl cyclases. J Biol Chem 270: 1-4, 1995.
49. Xie F, Garcia MA, Carlson AE, Schuh SM, Babcock DF, Jaiswal BS, Gossen JA, Esposito G, van Dulin M, Conti M. Soluble adenylyl cyclase (sAC) is indispensable for sperm function and fertilization. Dev Biol 296: 33-362, 2006.
50. Yang Z, Sun R, Grinchuk V, Fernandez-Blanco JA, Notari L, Bohl JA, McLean LP, Ramalingam TR, Wynn TA, Urban JF Jr, Vogel SN, Shea-Donohue T, Zhao A. IL-33-induced alterations in murine intestinal function and cytokine responses are MyD88, STAT6, and IL-13 dependent. Am J Physiol Gastrointest Liver Physiol 304: G381-G389, 2013.