Chronic stress targets posttranscriptional mechanisms to rapidly upregulate α1C-subunit of Cav1.2b calcium channels in colonic smooth muscle cells

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 300, Issue 1, 2011, Pages

  Li, Qingjie ^a   Sarna, Sushil K ^a,b  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

GSK 3; Irritable bowel syndrome; Posttranslational regulation; Wnt signaling

Indexed keywords

CALCIUM CHANNEL; CYANOPINDOLOL; GLYCOGEN SYNTHASE KINASE 3BETA; LITHIUM CHLORIDE; MESSENGER RNA; NORADRENALIN; PHENTOLAMINE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOPROTEIN; PRAZOSIN; PROPRANOLOL; PROTEASOME; PROTEIN KINASE B;

ANIMAL TISSUE; ARTICLE; CHRONIC STRESS; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; INTESTINE MUSCLE; NONHUMAN; NORADRENALIN RELEASE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; RNA TRANSLATION; SMOOTH MUSCLE; SMOOTH MUSCLE FIBER; TRANSCRIPTION REGULATION; UBIQUITINATION; UPREGULATION;

ANIMALS; CALCIUM CHANNELS, L-TYPE; COLON; EUKARYOTIC INITIATION FACTOR-2; GLYCOGEN SYNTHASE KINASE 3; LITHIUM CHLORIDE; MYOCYTES, SMOOTH MUSCLE; NOREPINEPHRINE; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTEIN SUBUNITS; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ADRENERGIC, ALPHA; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, MESSENGER; SIGNAL TRANSDUCTION; STRESS, PSYCHOLOGICAL; UBIQUITINATION; UP-REGULATION;

EID: 78650782122     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00393.2010     Document Type: Article

References (41)

1. Aberle H, Bauer A, Stappert J, Kispert A, Kemler R. β-Catenin is a target for the ubiquitin-proteasome pathway. EMBO J 16: 3797-3804, 1997.
2. Barry SP, Davidson SM, Townsend PA. Molecular regulation of cardiac hypertrophy. Int J Biochem Cell Biol 40: 2023-2039, 2008.
3. Bennett EJ, Tennant CC, Piesse C, Badcock CA, Kellow JE. Level of chronic life stress predicts clinical outcome in irritable bowel syndrome. Gut 43: 256-261, 1998. (Pubitemid 28348331)
4. Cadigan KM, Nusse R. Wnt signaling: a common theme in animal development. Genes Dev 11: 3286-3305, 1997. (Pubitemid 28023954)
5. Carrasco GA, Van de Kar LD. Neuroendocrine pharmacology of stress. Eur J Pharmacol 463: 235-272, 2003.
6. Castagliuolo I, Lamont JT, Qiu B, Fleming SM, Bhaskar KR, Nikulasson ST, Kornetsky C, Pothoulakis C. Acute stress causes mucin release from rat colon: role of corticotropin releasing factor and mast cells. Am J Physiol Gastrointest Liver Physiol 271: G884-G892, 1996. (Pubitemid 26404739)
7. Choudhury BK, Shi XZ, Sarna SK. Gene plasticity in colonic circular smooth muscle cells underlies motility dysfunction in a model of postinfective IBS. Am J Physiol Gastrointest Liver Physiol 296: G632-G642, 2009.
8. Choudhury BK, Shi XZ, Sarna SK. Norepinephrine mediates the transcriptional effects of heterotypic chronic stress on colonic motor function. Am J Physiol Gastrointest Liver Physiol 296: G1238-G1247, 2009.
9. Cross DA, Alessi DR, Cohen P, Andjelkovich M, Hemmings BA. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378: 785-789, 1995. (Pubitemid 26004411)
10. Dale TC. Signal transduction by the Wnt family of ligands. Biochem J 329: 209-223, 1998.
11. De Haro C, Mendez R, Santoyo J. The eIF-2alpha kinases and the control of protein synthesis. FASEB J 10: 1378-1387, 1996. (Pubitemid 26347872)
12. Dever TE. Gene-specific regulation by general translation factors. Cell 108: 545-556, 2002. (Pubitemid 34260879)
13. Ding VW, Chen RH, McCormick F. Differential regulation of glycogen synthase kinase 3beta by insulin and Wnt signaling. J Biol Chem 275: 32475-32481, 2000.
14. Dolmetsch RE, Pajvani U, Fife K, Spotts JM, Greenberg ME. Signaling to the nucleus by an L-type calcium channel-calmodulin complex through the MAP kinase pathway. Science 294: 333-339, 2001.
15. Embi N, Rylatt DB, Cohen P. Glycogen synthase kinase-3 from rabbit skeletal muscle. Separation from cyclic-AMP-dependent protein kinase and phosphorylase kinase. Eur J Biochem 107: 519-527, 1980.
16. Frost RA, Lang CH, Gelato MC. Transient exposure of human myoblasts to tumor necrosis factor-alpha inhibits serum and insulin-like growth factor-I stimulated protein synthesis. Endocrinology 138: 4153-4159, 1997.
17. 2+ channels requires membrane targeting of PKA and phosphorylation of channel subunits. Neuron 19: 185-196, 1997.
18. Ghosh A, Greenberg ME. Calcium signaling in neurons: molecular mechanisms and cellular consequences. Science 268: 239-247, 1995.
19. Hall DD, Feekes JA, Arachchige Don AS, Shi M, Hamid J, Chen L, Strack S, Zamponi GW, Horne MC, Hell JW. Binding of protein phosphatase 2A to the L-type calcium channel Cav1.2 next to Ser1928, its main PKA site, is critical for Ser1928 dephosphorylation. Biochemistry 45: 3448-3459, 2006.
20. Hardt SE, Sadoshima J. Glycogen synthase kinase-3beta: a novel regulator of cardiac hypertrophy and development. Circ Res 90: 1055-1063, 2002.
21. Hart A, Kamm MA. Review article: mechanisms of initiation and perpetuation of gut inflammation by stress. Aliment Pharmacol Ther 16: 2017-2028, 2002.
22. Harwood AJ. Regulation of GSK-3: a cellular multiprocessor. Cell 105: 821-824, 2001.
23. Heineke J, Molkentin JD. Regulation of cardiac hypertrophy by intracellular signalling pathways. Nat Rev Mol Cell Biol 7: 589-600, 2006.
24. Hell JW, Westenbroek RE, Warner C, Ahlijanian MK, Prystay W, Gilbert MM, Snutch TP, Catterall WA. Identification and differential subcellular localization of the neuronal class C and class D L-type calcium channel alpha 1 subunits. J Cell Biol 123: 949-962, 1993.
25. Hulme JT, Westenbroek RE, Scheuer T, Catterall WA. Phosphorylation of serine 1928 in the distal C-terminal domain of cardiac CaV1.2 channels during beta1-adrenergic regulation. Proc Natl Acad Sci USA 103: 16574-16579, 2006.
26. Lee TS, Karl R, Moosmang S, Lenhardt P, Klugbauer N, Hofmann F, Kleppisch T, Welling A. Calmodulin kinase II is involved in voltage-dependent facilitation of the L-type Cav1.2 calcium channel: identification of the phosphorylation sites. J Biol Chem 281: 25560-25567, 2006.
27. Li Q, Sarna SK. Nuclear myosin II regulates the assembly of preinitiation complex for ICAM-1 gene transcription. Gastroenterology 137: 1051-1060, 2009.
28. a.Linding R, Jensen LJ, Ostheimer GJ, van Vugt MA, Jorgensen C, Miron IM, Diella F, Colwill K, Taylor L, Elder K, Metalnikov P, Nguyen V, Pasculescu A, Jin J, Park JG, Samson LD, Woodgett JR, Russell RB, Bork P, Yaffe MB, Pawson T. Systematic discovery of in vivo phosphorylation networks. Cell 129: 1415-1426, 2007.
29. Liu X, Rusch NJ, Striessnig J, Sarna SK. Down-regulation of L-type calcium channels in inflamed circular smooth muscle cells of the canine colon. Gastroenterology 120: 480-489, 2001.
30. Miller DB, O'Callaghan JP. Neuroendocrine aspects of the response to stress. Metabolism 51: 5-10, 2002.
31. Miller JR, Hocking AM, Brown JD, Moon RT. Mechanism and function of signal transduction by the Wnt/beta-catenin and Wnt/Ca2+ pathways. Oncogene 18: 7860-7872, 1999. (Pubitemid 30066232)
32. Pause A, Belsham GJ, Gingras AC, Donze O, Lin TA, Lawrence JC Jr, Sonenberg N. Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5′-cap function. Nature 371: 762-767, 1994. (Pubitemid 124000078)
33. 2+ channels by cyclic nucleotide cross activation of opposing protein kinases in rabbit portal vein. Circ Res 82: 557-565, 1998.
34. Shi XZ, Choudhury BK, Pasricha PJ, Sarna SK. A novel role of VIP in colonic motility function: induction of excitation-transcription coupling in smooth muscle cells. Gastroenterology 132: 1388-1400, 2007.
35. Sobell HM. Actinomycin and DNA transcription. Proc Natl Acad Sci USA 82: 5328-5331, 1985.
36. 2+ channel. Circ Res 105: 51-60, 2009.
37. Tsigos C, Chrousos GP. Hypothalamic-pituitary-adrenal axis, neuroendocrine factors and stress. J Psychosom Res 53: 865-871, 2002. (Pubitemid 35282615)
38. Vale W, Spiess J, Rivier C, Rivier J. Characterization of a 41-residue ovine hypothalamic peptide that stimulates secretion of corticotropin and beta-endorphin. Science 213: 1394-1397, 1981. (Pubitemid 12243637)
39. Whitehead WE, Crowell MD, Robinson JC, Heller BR, Schuster MM. Effects of stressful life events on bowel symptoms: subjects with irritable bowel syndrome compared with subjects without bowel dysfunction. Gut 33: 825-830, 1992.
40. Xu C, Kim NG, Gumbiner BM. Regulation of protein stability by GSK3 mediated phosphorylation. Cell Cycle 8: 4032-4039, 2009.
41. Yang L, Doshi D, Morrow J, Katchman A, Chen X, Marx SO. Protein kinase C isoforms differentially phosphorylate Ca(v)1.2 alpha(1c). Biochemistry 48: 6674-6683, 2009.