Regulation of transforming growth factor β-induced responses by protein kinase A in pancreatic acinar cells

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 295, Issue 1, 2008, Pages

  Yang, Huibin ^a   Lee, Cheong J ^a   Zhang, Lizhi ^a   Sans, Maria Dolors ^a   Simeone, Diane M ^a,b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

Sample keywords

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; NUCLEAR PROTEIN; PROTEIN P21; PROTEIN SNON; SMAD3 PROTEIN; SMAD4 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; CREB1 PROTEIN, MOUSE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; ONCOPROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; SKIL PROTEIN, MOUSE;

ACINAR CELL; ANIMAL CELL; ARTICLE; CELL FUNCTION; CELL GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME REGULATION; GROWTH INHIBITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; ANIMAL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; PANCREAS; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CELLS, CULTURED; CYCLIC AMP; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; GENE EXPRESSION REGULATION; MALE; MICE; MICE, INBRED C57BL; PANCREAS, EXOCRINE; PROTO-ONCOGENE PROTEINS; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 51149095049     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00492.2007     Document Type: Article

References (58)

1. Bakin AV, Tomlinson AK, Bhowmick NA, Moses HL, Arteaga CL. Phosphatidylinositol 3-kinase function is required for transforming growth factor beta-mediated epithelial to mesenchymal transition and cell migration. J Biol Chem 275: 36803-36810, 2000.
2. Bhattacharyya E, Panchal A, Wilkins TJ, de Ondarza J, Hootman SR. Insulin, transforming growth factors, and substrates modulate growth of guinea pig pancreatic duct cells in vitro. Gastroenterology 109: 944-952, 1995.
3. Bhowmick NA, Zent R, Ghiassi M, McDonnell M, Moses HL. Integrin beta 1 signaling is necessary for transforming growth factor-beta activation of p38MAPK and epithelial plasticity. J Biol Chem 276: 46707-46713, 2001.
4. Bottinger EP, Jakubczak JL, Roberts IS, Mumy M, Hemmati P, Bagnall K, Merlino G, Wakefield LM. Expression of a dominant-negative mutant TGF-beta type II receptor in transgenic mice reveals essential roles for TGF-beta in regulation of growth and differentiation in the exocrine pancreas. EMBO J 16: 2621-2633, 1997.
5. Boyton AL, Whitfield JF. The role of cAMP in cell proliferation: a critical assessment of the evidence. In: Advances in Cyclic Nucleotide Research (vol. 15), edited by Greengard P and Robison GA. New York: Raven, 1983, p. 193-294.
6. Cho YS, Cho-Chung YS. Antisense protein kinase A RIalpha synergistically with hydroxycamptothecin to inhibit growth and induce apoptosis in human cancer cells: molecular basis for combinatorial therapy. Clin Cancer Res 9: 1171-1178, 2003.
7. Clegg CH, Cadd GG, McKnight GS. Genetic characterization of a brain-specific form of the type I regulatory subunit of cAMP-dependent protein kinase. Proc Natl Acad Sci USA 85: 3703-3707, 1988.
8. Colwell AS, Krummel TM, Longaker MT, Lorenz HP. Wnt-4 expression is increased in fibroblasts after TGF-beta1 stimulation and during fetal and postnatal wound repair. Plast Reconstr Surg 117: 2297-2301, 2006.
9. Cvijic ME, Yang WL, Chin KV. Cisplatin resistance in cyclic AMP-dependent protein kinase mutants. Pharmacol Ther 78: 115-128, 1998.
10. DiMagno MJ, Williams JA, Hao Y, Ernst SA, Owyang C. Endothelial nitric oxide synthase is protective in the initiation of caerulein-induced acute pancreatitis in mice. Am J Physiol Gastrointest Liver Physiol 287: G80-G87, 2004.
11. Edwards AS, Scott JD. A-kinase anchoring proteins: protein kinase A and beyond. Curr Opin Cell Biol 12: 217-221, 2000.
12. Engel ME, McDonnell MA, Law BK, Moses HL. Interdependent SMAD and JNK signaling in transforming growth factor-beta-mediated transcription. J Biol Chem 274: 37413-37420, 1999.
13. Giannouli CC, Kletsas D. TGF-β regulates differentially the proliferation of fetal and adult human skin fibroblasts via the activation of PKA and the autocrine action of FGF-2. Cell Signal 18: 1417-1429, 2006.
14. Ginty DD, Kornhauser JM, Thompson MA, Bading H, Mayo KE, Takahashi JS, Greenberg ME. Regulation of CREB phosphorylation in the suprachiasmatic nucleus by light and a circadian clock. Science 260: 238-241, 1993.
15. Gittes GK, Galante PE, Hanahan D, Rutter WJ, Debas HT. Lineage-specific morphogenesis in the developing pancreas: role of mesenchymal factors. Development 122: 439-447, 1996.
16. Glass DB, Cheng HC, Kemp BE, Walsh DA. Differential and common recognition of the catalytic sites of the cGMP-dependent and cAMP-dependent protein kinases by inhibitory peptides derived from the heat stable inhibitor protein. J Biol Chem 261: 12166-12171, 1986.
17. Hahn SA, Schutte M, Hoque AT, Moskaluk CA, da Costa LT, Rozenblum E, Weinstein CL, Fischer A, Yeo CJ, Hruban RH, Kern SE. DPC4, a candidate tumor suppressor gene at human chromosome 18q21.1. Science 271: 350-353, 1996.
18. Hartsough MT, Mulder KM. Transforming growth factor beta activation of p44mapk in proliferating cultures of epithelial cells. J Biol Chem 270: 7117-7124, 1995.
19. Ishida A, Fujita N, Kitazawa R, Tsuruo T. Transforming growth factor-beta induces expression of receptor activator of NF-kappa B ligand in vascular endothelial cells derived from bone. J Biol Chem 277: 26217-26224, 2002.
20. Jahnsen T, Hedin L, Kidd VJ, Beattie WG, Lohmann SM, Walter U, Durica J, Schultz TZ, Schiltz E, Browner M, Lawrence CB, Goldman D, Ratoosh SL, Richards JS. Molecular cloning, cDNA structure, and regulation of the regulatory subunit of type II cAMP-dependent protein kinase from rat ovarian granulosa cells. J Biol Chem 261: 12352-12361, 1986.
21. Kirschner LS, Carney JA, Pack SD, Taymans SE, Giatzakis C, Cho YS, Cho-Chung YS, Stratakis CA. Mutations of the gene encoding the protein kinase A type Ia regulatory subunit in patients with Carney complex. Nat Genet 26: 89-92, 2000.
22. Kunzmann S, Mantel PY, Wohlfahrt JG, Akdis M, Blaser K, Schmidt-Weber CB. Histamine enhances TGF-beta1-mediated suppression of Th2 responses. FASEB J 17: 1089-1095, 2003.
23. Laiho M, DeCaprio JA, Ludlow JW, Livingston DM, Massague J. Growth inhibition by TGF-beta linked to suppression of retinoblastoma protein phosphorylation. Cell 62: 175-185, 1990.
24. Letamendia A, Labbe E, Attisano L. Transcriptional regulation by Smads: crosstalk between the TGF-beta and Wnt pathways. J Bone Joint Surg Am 83-A, Suppl 1: S31-S39, 2001.
25. Logsdon CD, Keyes L, Beauchamp RD. Transforming growth factor-β (TGF-β1) inhibits pancreatic acinar cell growth. Am J Physiol Gastrointest Liver Physiol 262: G364-G368, 1992.
26. Lu Z, Kolodecik TR, Karne S, Nyce M, Gorelick F. Effect of ligands that increase cAMP on caerulein-induced zymogen activation in pancreatic acini. Am J Physiol Gastrointest Liver Physiol 285: G822-G828, 2003.
27. Luo K. Ski and SnoN: negative regulators of TGF-β signaling. Curr Opin Genet Dev 14: 65-70, 2004.
28. Marino CR, Leach SD, Schaefer JF, Miller LJ, Gorelick FS. Characterization of cAMP-dependent protein kinase activation by CCK in the rat pancreas. FEBS Lett 316: 48-52, 1993.
29. Massague J. TGF-beta signal transduction. Annu Rev Biochem 67: 753-791, 1998.
30. Massague J, Blain SW, Lo RS. TGFbeta signaling in growth control, cancer, and heritable disorders. Cell 103: 295-309, 2000.
31. - channels in bile duct epithelial cells through a cAMP-dependent mechanism. Am J Physiol Gastrointest Liver Physiol 266: G731-G736, 1994.
32. Millar SE. Smad7: licensed to kill beta-catenin. Dev Cell 11: 274-276, 2006.
33. Normura N, Saamoto S, Ishii S, Date T, Matsui M, Ishizaki R. Isolation of human cDNA clones of ski and the ski-related gene, sno. Nucleic Acids Res 17: 5489-5500, 1989.
34. Patterson GI, Padgett RW. TGF beta-related pathways. Role of Caenorhabditis elegans development. Trends Genet 16: 27-33, 2000.
35. Pearson-White S, Crittenden R. Proto-oncogene Sno expression, alternative isoforms and immediate early serum response. Nucleic Acids Res 25: 2930-2937, 1997.
36. Rousse S, Lallemand F, Montarras D, Pinset C, Mazars A, Prunier C, Atfi A, Dubois C. Transforming growth factor-beta inhibition of insulin-like growth factor-binding protein-5 synthesis in skeletal muscle cells involves a c-Jun N-terminal kinase-dependent pathway. J Biol Chem 276: 46961-46967, 2001.
37. Sanvito F, Herrera PL, Montesano R, Orci L, Vassalli JD. TGF-β1 influences the relative development of the exocrine and endocrine pancreas in vitro. Development 120: 3451-3462, 1994.
38. Scott JD, Glaccum MB, Zoller MJ, Uhler MD, Helfman DM, McKnight GS, Krebs EG. The molecular cloning of a type II regulatory subunit of the cAMP-dependent protein kinase from rat skeletal muscle and mouse brain. Proc Natl Acad Sci USA 84: 5192-5196, 1987.
39. Sharma K, Wang L, Zhu Y, Bokkala S, Joseph SK. Transforming growth factor-beta1 inhibits type I inositol 1,4,5-triphosphate receptor expression and enhances its phosphorylation in mesangial cells. J Biol Chem 272: 14617-14623, 1997.
40. Shaywitz AJ, Greenberg ME. CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu Rev Biochem 68: 821-861, 1999.
41. Shi Y, Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113: 685-700, 2003.
42. Simeone DM, Pham T, Logsdon CD. Disruption of TGF-β signaling pathways in human pancreatic cancer cells. Ann Surg 232: 73- 80, 2000.
43. Simeone DM, Zhang L, Graziano K, Nicke B, Pham T, Schaefer C, Logsdon CD. Smad4 mediates activation of mitogen-activated protein kinases by TGF-beta in pancreatic acinar cells. Am J Physiol Cell Physiol 281: C311-C319, 2001.
44. Singh LP, Green K, Alexander M, Bassly S, Crook ED. Hexosamines and TGF-β1 use similar signaling pathways to mediate matrix protein synthesis in mesangial cells. Am J Physiol Renal Physiol 286: F409-F416, 2004.
45. Srivastava RK, Srivastava AR, Seth P, Agrwawal S, Cho-Chung YS. Growth arrest and induction of apoptosis in breast cancer cells by anti-sense depletion of protein kinase A-RI alpha subunit: p53-independent mechanism of action. Mol Cell Biochem 195: 25-36, 1999.
46. Stroschein SL, Wang W, Zhou S, Zhou Q, Luo K. Negative feedback regulation of TGF-beta signaling by the SnoN oncoprotein. Science 286: 771-774, 1999.
47. Ten Dijke PT, Goumans MJ, Itoh F, Itoh S. Regulation of cell proliferation by Smad proteins. J Cell Physiol 191: 1-16, 2002.
48. Tesmer JJ, Sprang SR. The structure, catalytic mechanism and regulation of adenylyl cyclase. Curr Opin Struct Biol 8: 713-719, 1998.
49. Tobimatsu T, Kaji H, Sowa H, Naito J, Canaff L, Hendy GN, Sugimoto T, Chihara K. Parathyroid hormone increases β-catenin levels through Smad3 in mouse osteoblastic cells. Endocrinology 147: 2583-2590, 2006.
50. Tortora G, Cho-Chung YS. Type II regulatory subunit of protein kinase restores cAMP-dependent transcription in a cAMP-unresponsive cell line. J Biol Chem 265: 18067-18070, 1990.
51. Uhler MD, Chrivia JC, McKnight GS. Evidence for a second isoform of the catalytic subunit of cAMP-dependent protein kinase. J Biol Chem 261: 15360-15363, 1986.
52. Ventra C, Porcellini A, Feliciello A, Gallo A, Paolillo M, Mele E, Avvedimento VE, Schettini G. The differential response of protein kinase A to cAMP in discrete brain areas correlates with the abundance of regulatory subunit II. J Neurochem 66: 1752-1761, 1996.
53. Walsh DA, Van Patten SM. Multiple pathway signal transduction by the cAMP-dependent protein kinase. FASEB J 8: 1227-1236, 1994.
54. Wang FM, Hu T, Tan H, Zhou XD. p38 mitogen-activated protein kinase affects transforming growth factor-β/Smad signaling in human dental pulp cells. Mol Cell Biochem 291: 49-54, 2006.
55. Wang L, Zhu Y, Sharma K. Transforming growth factor-beta1 stimulates protein kinase A in mesangial cells. J Biol Chem 273: 8522-8527, 1998.
56. Zavadil J, Bitzer M, Liang D, Yang YC, Massimi A, Kneitz S, Piek E, Bottinger EP. Genetic programs of epithelial cell plasticity directed by transforming growth factor-beta. Proc Natl Acad Sci USA 98: 6686-6691, 2001.
57. Zhang L, Duan C, Binkley C, Li G, Uhler M, Logsdon C, Simeone D. A TGF-beta induced Smad3/Smad4 complex directly activates protein kinase A. Mol Cell Biol 24: 2169-2180, 2004.
58. Zhang L, Graziano K, Pham T, Logsdon CD, Simeone DM. Adenovirus-mediated gene transfer of dominant-negative Smad4 blocks TGF-beta signaling in pancreatic acinar cells. Am J Physiol Gastrointest Liver Physiol 280: G1247-G1253, 2001.