cAMP and protein kinase A in endocrine (and other) tumors

Expert Review of Endocrinology and Metabolism

Volumn 2, Issue 5, 2007, Pages 667-676

  Nesterova, Maria ^a   Stratakis, Constantine A ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Adrenal tumor; cAMP; Cushing syndrome; Multiple endocrine neoplasia; Protein kinase A; Tumor suppressor gene

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GROWTH HORMONE; HYDROCORTISONE; ISOENZYME; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHODIESTERASE; PROLACTIN; PROTEIN KINASE; REPLICATION FACTOR C;

ADRENAL CORTEX TUMOR; APOPTOSIS; AUTOPHAGY; CARCINOGENESIS; CARNEY COMPLEX; CELL CYCLE; CELL DIFFERENTIATION; CELL GROWTH; CELL MEMBRANE; CELL PROLIFERATION; CELL STRUCTURE; CELL TRANSFORMATION; CELL TYPE; CELLULAR DISTRIBUTION; CUSHING SYNDROME; ENDOCRINE TUMOR; ENZYME ACTIVITY; ENZYME STRUCTURE; GENE MUTATION; GOLGI COMPLEX; HUMAN; MEDICAL RESEARCH; MITOCHONDRION; NONHUMAN; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; STOP CODON; TUMOR GROWTH;

EID: 34648833460     PISSN: 17446651     EISSN: None     Source Type: Journal    
DOI: 10.1586/17446651.2.5.667     Document Type: Review

References (90)

1. Robison GA. The biological role of cyclic AMP: an update review. In: Prostaglandins and Cyclic AMP: Biological Actions and Clinical Applications. Kahn RH, Lands WEM (Eds). Academic Press, NY, USA 229-247 (1973).
2. Mayr B, Montminy M. Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat. Rev. Mol. Cell Biol. 2, 599-609 (2001).
3. Conkright MD, Guzman E, Flechner L, Su AI, Hogenesch JB, Montminy M. Genome-wide analysis of CREB target genes reveals a core promoter requirement for cAMP responsiveness. Mol. Cell 11, 1101-1108 (2003).
4. Zhang X, Odom DT, Koo SH et al. Genome-wide analysis of cAMP-response element binding protein occupancy, phosphorylation, and target gene activation in human tissues. Proc. Natl Acad. Sci. USA 102, 4459-4464 (2005).
5. Dodge-Kafka KL, Soughayer J, Pare GC et al. The protein kinase A anchoring protein mAKAP coordinates two integrated cAMP effector pathways. Nature 437, 574-578 (2005).
6. Kopperud R, Krakstad C, Selheim F, Døskeland SO. cAMP effector mechanisms. Novel twists for an 'old' signaling system. FEBS Lett. 546, 121-126 (2003).
7. Gross-Langenhoff M, Hofbauer K, Weber J, Schultz A, Schultz JE. cAMP is a ligand for the tandem GAF domain of human phosphodiesterase 10 and cGMP for the tandem GAF domain of phosphodiesterase 11. J. Biol. Chem. 281, 2841-2846 (2006).
8. Kuo JF, Greengard P. Cyclic nucleotide-dependent kinases. IV. Widespread occurrence of adenosine 3′:5′-monophosphate-dependent protein kinase in various tissues and phyla of the animal kingdom. Proc. Natl Acad. Sci. USA 64, 1349-1355 (1969).
9. Beebe SJ, Corbin JD. Cyclic nucleotide-dependent protein kinases. In: The Enzymes: Control by Phospharylation, Part A. Boyer PD, Krebs EG (Eds). Academic Press, NY, USA 17, 43-111 (1986).
10. Corbin JD, Keely SL, Park CR. The distribution and dissociation of cyclic adenosine 3′:5′-monophosphate dependent protein kinases in adipose, cardiac, and other tissues. J. Biol. Chem. 250, 218-225 (1975).
11. Kurten RC, Levy LO, Shey J Durica JM, Richards JS. Identification and characterization of the GC-rich and cyclic adenosine 3′,5′-monophosphate (cAMP)-inducible promoter of the type II β cAMP dependent protein kinase regulatory subunit gene. Mol. Endocrinol. 6, 536-550 (1992).
12. Nowak I, Seipel K, Schwartz M, Jans DA, Hemmings BA. Isolation of cDNA and characterization of the 5′ flanking region of the gene encoding the type I regulatory subunit of the cAMP-dependent protein kinase. Eur. J. Blochem. 167, 27-33 (1987).
13. Dostmann WR, Taylor SS, Genieser HG, Jastorff B, Døskeland SO, Ogreid D. Probing the cyclic nucleotide binding sites of cAMP-dependent protein kinases I and II with analogs of adenosine 3′,5′-cyclic phosphorothioates. J. Biol. Chem. 265, 10484-10491 (1990).
14. Hofmann F. Apparent constants for the interaction of regulatory and catalytic subunit of cAMP-dependent protein kinase I and II. J. Biol. Chem. 255, 1559-1564 (1980).
15. Vigil D, Blumenthal DK, Brown S et al. Differential effects of substrate on type I and type II PKA holoenzyme dissociation. Biochemistry 43, 5629-5636 (2004).
16. Kim C, Xuong NH, Taylor SS. Crystal structure of a complex between the catalytic and regulatory (RIα) subunits of PKA. Science 307, 690-696 (2005).
17. Scott JD, McCartney S. Localization of A-kinase through anchoring proteins. Mol. Endocrinol. 8, 5-11 (1994).
18. Kondrashin AA, Nesterova MV, Cho-Chung YS. Subcellular distribution of the R-subunits of cAMP-dependent protein kinase in LS-174T human colon carcinoma cells. Biochem. Mol. Biol. Intern. 45, 237-244 (1998).
19. Imazumi-Scherrer T, Faust DM, Barradeau S, Hellio R, Weiss MC. Type I protein kinase A is localized to interphase microtubules and strongly associated with the mitotic spindle. Exp. Cell Res. 264, 250-265 (2001).
20. Carlson CR, Witczak O, Vossebein L et al. CDK1-mediated phosphorylation of the RIIα regulatory subunit of PKA works as a molecular switch that promotes dissociation of RIIα from centrosomes at mitosis. J. Cell. Sci. 114, 3243-3254 (2001).
21. Riabowol KT, Fink JS, Oilman MZ, Walsh DA, Goodman RH, Feramisco JR. The catalytic subunit of cAMP-dependent protein kinase induces expression of genes containing cAMP-responsive enhancer elements. Nature 336, 83-86 (1988).
22. Solberg R, Tasken K, Wen W et al. Human regulatory subunit RIβ of cAMP-dependent protein kinases: expression, holoenzyme formation and microinjection into living cells. Exp. Cell Res. 214, 595-605 (1994).
23. Neary CL, Cho-Chung YS. Nuclear translocation of the catalytic subunit of protein kinase A induced by an antisense oligonucleotide directed against the RIα regulatory subunit. Oncogene 20, 8019-8024 (2001).
24. Constantinescu A, Wu M, Asher O, Diamond I. cAMP-dependent protein kinase type I regulates ethanol-induced cAMP response element-mediated gene expression via activation of CREB-binding protein and inhibition of MAPK. J. Biol. Chem. 279, 43321-43329 (2004).
25. Feliciello A, Giuliano P, Porcellini A et al. The v-Ki-Ras oncogene alters cAMP nuclear signaling by regulating the location and the expression of cAMP-dependent protein kinase IIβ. J. Biol. Chem. 271, 25350-25359 (1996).
26. Hofmann F, Bechtel PJ, Krebs EG. Concentrations of cyclic AMP-dependent protein kinase subunits in various tissues. J. Biol. Chem. 252, 1441-1447 (1977).
27. Uhler MD, McKnight GS. Expression of cDNAs for two isoforms of the catalytic subunit of cAMP-dependent protein kinase. J. Biol. Chem. 262, 15202-15207 (1987).
28. Cummings DE, Brandon EF, Planas JV, Motamed K, Idzerda RL, McKnight GS. Genetically lean mice result from targeted disruption of the RII β subunit of protein kinase A. Nature 382, 622-626 (1996).
29. Schreyer SA, Cummings DE, McKnight GS, LeBoeuf RC. Mutation of the RII β subunit of protein kinase A prevents diet-induced insulin resistance and dyslipidemia in mice. Diabetes 50, 2555-2562 (2001).
30. Planas JV, Cummings DE, Idzerda RL, McKnight GS. Mutation of the RII β subunit of protein kinase A differentially affects lipolysis but not gene induction in white adipose tissue. J. Biol. Chem. 274, 36281-36287 (1999).
31. Brandon EP, Logue SF, Adams MR et al. Defective motor behavior and neural gene expression in RIIβ-protein kinase A mutant mice. J. Neurosci. 18, 3639-3649 (1998).
32. Adams MR, Brandon EP, Chartoff E, Idzerda RL, Dorsa DM, McKnight GS. Loss of haloperidol induced gene expression and catalepsy in protein kinase A-deficient mice. Proc. Natl Acad. Sci. USA 94, 12157-12161 (1997).
33. Amieux PS, Cummings DE, Motamed K et al. Compensatory regulation of RI α protein levels in protein kinase A mutant mice. J. Biol. Chem. 272, 3993-3998 (1997).
34. 2+ channel activity by cAMP-dependent protein kinase. Proc. Natl Acad. Sci. USA 94, 11067-11072 (1997).
35. Burton KA, Treash-Osio B, Muller CH et al. Deletion of type II α regulatory subunit delocalizes protein kinase A in mouse sperm without affecting motility or fertilization. J. Biol. Chem. 274, 24131-24136 (1999).
36. Skalhegg BS, Johansen AK, Levy FO et al. Isozymes of cyclic AMP-dependent protein kinases (PKA) in human lymphoid cell lines. Levels of endogenous cAMP influence levels of PKA subunits and growth in lymphoid cell lines. J. Cell Physiol. 177, 85-93 (1998).
37. Schuller HM. Neurotransmitter receptor-mediated signaling pathways as modulators of carcinogenesis. Prog. Exp. Tumor Res. 39, 45-63 (2007).
38. Cho-Chung YS. Role of cyclic AMP receptor proteins in growth, differentiation, and suppression of malignancy: new approaches to therapy. Cancer Res. 50, 7093-7100 (1990).
39. Boynton AL, Whietfield JF. The role of cyclic AMP in cell proliferation: a critical assessment of the evidence. In: Advances in Cyclic Nucleotide Research. Greengard P, Robinson GA (Eds). Raven Press, NY, USA 15, 193-294 (1983).
40. Russell DH. Type I cyclic AMP-dependent protein kinase as a positive effector of growth. In: Advances in Cyclic Nucleotide Research. Greengard P, Robinson GA (Eds). Raven Press, NY, USA 9, 493-506 (1978).
41. Cho-Chung YS, Nesterova MV, Pepe S et al. Antisense DNA-targeting protein kinase A-RIa subunit: a novel approach to cancer treatment. Front. Biosci. 4, D898-D907 (1990).
42. Amieux PS, McKnight GS. The Essential Role of RIα in the maintenance of regulated PKA activity. Ann. NY Acad. Sci. 968, 75-95 (2002).
43. Fossberg TM, Doskeland SO, Ueland PM. Protein kinases in human renal cell carcinoma and renal cortex. A comparison of isozyme distribution and of responsiveness to adenosine 3′,5′-cyclic monophosphate. Arch. Biochem. Biophys. 189, 372-381 (1978).
44. Handshin JC, Handloser K Takahashi A, Eppenberger U. Cyclic adenosine 3′,5′-monophosphate receptor proteins in dysplastic and neoplastic human breast tissue cytosol and their inverse relationship with estrogen receptors. Cancer Res. 43, 2947-2954 (1983).
45. Miller WR. Regulatory subunits of PKA and breast cancer. Ann. NY Acad. Sci. 968, 37-48 (2002).
46. Neary CL, Nesterova M, Cho YS, Cheadle C, Becker KG, Cho-Chung YS. Protein kinase A isozyme switching-eliciting differential cAMP signaling and tumor reversion. Oncogene 23, 8847-8856 (2004).
47. Cho YS, Kim M-K, Cheadle C, Neary C, Becker KG, Cho-Chung YS. Antisense DNAs as multisite genomic modulators identified by DNA microarray. Proc. Natl Acad. Sci. USA 98, 9819-9823 (2001).
48. Cho-Chung YS, Nesterova M, Park YG, Lee YN. Protein kinase A-RIα antisense: antitumor machanism of action. Antisense Nucleic Acid Drug Dev. 9, 383-388 (1999).
49. Alper O, Hacker NF, Cho-Chung YS. Protein kinase A-Iα subunit-directed antisense inhibition of ovarian cancer cell growth: crosstalk with tyrosine kinase signaling pathway. Oncogene 18, 4999-5004 (1999).
50. Srivastava RK, Srivastava AR, Korsmeyer SJ, Nesterova M, Cho-Chung YS, Longo DL. Involvement of microtubules in the regulation of Bcl2 phosphorylation and apoptosis through cyclic AMP-dependent protein kinase. Mol. Cell. Biol. 18, 3509-3517 (1998).
51. Cho YS, Kim MK, Tan L et al. Protein kinase A RIα antisense inhibition of PC3M prostate cancer cell growth: bcl-2 hyperphosphorylation, Bax up-regulation, and Bad hypophosphorylation. Clin. Cancer Res. 8, 607-614 (2002).
52. Kirschner LS, Sandrini F, Monbo J, Lin JP, Carney JA, Stratakis CA. Genetic heterogeneity and spectrum of mutations of the PRKAR1A gene in patients with Carney complex. Hum. Mol. Genet. 9, 3037-3046 (2000).
53. Kirschner LS, Carney JA, Pack SD et al. Mutations of the gene encoding the protein kinase A type I-α regulatory subunit in patients with the Carney complex. Nat. Genet. 26, 89-92 (2000).
54. Stratakis CA, Kirshner LS, Carney JA. Clinical and molecular features of the Carney complex: diagnostic criteria and recommendations for patient evaluation. J. Clin. Endocrinol. Metab. 86, 4041-4046 (2001).
55. Stratakis CA. Genetics of Carney complex and related familial lentiginoses, and other multiple tumor syndromes. Front. Biosci. 5, 353-366 (2000).
56. Groussin L, Kirschner LS, Vincent-Dejean C et al. Molecular analysis of the cyclic AMP-dependent protein kinase A (PKA) regulatory subunit 1A (PRKAR1A) gene in patients with Carney complex and primary pigmented nodular adrenocortical disease (PPNAD) reveals novel mutations and clues for pathophysiology: augmented PKA signaling is associated with adrenal tumorigenesis in PPNAD. Am. J. Hum. Genet. 71, 1433-42 (2002).
57. Robinson-White A, Stratakis CA. Protein kinase A signaling: "cross-talk" with other pathways in endocrine cells. Ann. NY Acad Sci. 968, 256-270 (2002).
58. Robinson-White A, Hundley TR, Shiferaw M et al. Protein kinase-A activity in PRKAR1A-mutant cells, and regulation of mitogen-activated protein kinases ERK1/2. Hum. Mol. Genet. 12, 1475-1484 (2003).
59. Robinson-White A, Meoli E, Stergiopoulos S et al. PRKAR1A mutations and protein kinase A interactions with other signaling pathways in the adrenal cortex. J. Clin. Endocrinol. Metab. 91, 2380-2388 (2006).
60. Robinson-White AJ, Leitner WW, Aleem E, Kaldis P, Bossis I, Stratakis CA. PRKAR1A inactivation leads to increased proliferation and decreased apoptosis in human B lymphocytes. Cancer Res. 66, 10603-10612 (2006).
61. 1 switching. Cell Signal. 16, 1397-1403 (2004).
62. EL, MM, MC, TM, TT, HMS: NNK activates ERK1/2 and CREB/ATF-1 via β-1-AR and EGFR signaling in human lung adenocarcinoma and small airway epithelial cells. Int. J. Cancer. 119, 1547-1552 (2006).
63. Horvath A, Boikos S, Giatzakis C et al. A genome-wide scan identifies mutations in the gene encoding phosphodiesterase 11A4 ( PDE11A) in individuals with adrenocortical hyperplasia. Nat. Genet. 38, 794-800 (2006).
64. Horvath A, Giatzakis C, Robinson-White A et al. Adrenal hyperplasia and adenomas are associated with inhibition of phosphodiesterase 11A in carriers of PDE11A sequence variants that are frequent in the population. Cancer Res. 15, 66, 11571-11575 (2006).
65. Matyakhina L, Pack S, Kirshner LS et al. Chromosome 2 (2p16) abnormalities in Carney complex tumors. J. Med. Genet. 40, 268-277 (2003).
66. Imaizumi-Scherrer T, Faust DM, Barradeau S, Hellio R, Weiss MC. Type I protein kinase A is localized to interphase microtubules and strongly associated with the mitotic spindle. Exp. Cell Res. 264, 250-265 (2001).
67. Gupte RS, Weng Y, Liu L, Lee MY. The second subunit of the replication factor C complex (RFC40) and the regulatory subunit (RIα) of protein kinase A form a protein complex promoting cell survival. Cell Cycle 4, 323-329 (2005).
68. Gupte RS, Traganos F, Darzynkiewicz Z, Lee MY. Phosphorylation of RIα by cyclin-dependent kinase CDK 2/cyclin E modulates the dissociation of the RIα-RFC40 complex. Cell Cycle 5, 653-660 (2006).
69. Gupte RS, Sampson V, Traganos F, Darzynkiewicz Z, Lee MY. Cyclic AMP regulates the expression and nuclear translocation of RFC40 in MCF7 cells. Exp. Cell Res. 312, 796-806 (2006).
70. Yang WL, Iacono L, Tang WM, Chin KV. A novel mechanism of cAMP signaling through the interaction of the regulatory subunit of protein kinase A with cytochrome c oxidase subunit Vb. Biochemistry 37, 14175-14180 (1998).
71. Liu J, Rone MB, Papadopoulos V. Protein-protein interactions mediate mitochondrial cholesterol transport and steroid biosynthesis. J. Biol. Chem. 281, 38879-38893 (2006).
72. Ciardiello F, Tortora G. Interactions between the epidermal growth factor receptor and type I protein kinase A: biological significance and therapeutic implications. Clin. Cancer Res. 4, 821-828 (1998).
73. Liguori L, de Lamirande E, Minelli A, Gagnon C. Various protein kinases regulate human sperm acrosome reaction and the associated phosphorylation of Tyr residues and of the Thr-Glu-Tyr motif. Mol. Hum. Reprod. 11, 211-221 (2005).
74. Chaturverdi D, Poppleton HM, Stringfield T, Barbier A, Patel TB. Subcellular localization and biological actions of activated RSK1 are determined by its interactions with subunits of cyclic AMP-dependent protein kinase. Mol. Cell. Biol. 26, 4586-4600 (2006).
75. Noda T, Ohsumi Y. TOR, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J. Biol. Chem. 273, 3963-3966 (1998).
76. Kim J, Huang WP, Stromhaug PE, Klionsky DJ. Convergence of multiple autophagy and cytoplasm to vacuole targeting components to a perivacuolar membrane compartment prior to de novo vesicle formation. J. Biol. Chem. 277, 763-773 (2002).
77. Suzuki K, Kirisako T, Kamada Y, Mizushima N, Noda T, Ohsumi Y. The pre-autophagosomal structure organized by concerted functions of APG genes is essential for autophagosome formation. EMBO J. 20, 5971-5981 (2001).
78. Wullschleger S, Loewith R, Hall MN. TOR signaling in growth and metabolism. Cell. 124, 471-484 (2006).
79. Mavrakis M, Lippincott-Schwartz J, Stratakis CA, Bossis I. Depletion of type IA regulatory subunit (RIα) of protein kinase A (PKA) in mammalian cells and tissues activates mTOR and causes autophagic deficiency. Hum. Mol. Genet. 15, 2962-2971 (2006).
80. Haddox MK, Roeske WR, Russell DH. Independent expression of cardiac type I and II cyclic AMP-dependent protein kinase during murine embryogenesis and postnatal development. Biochim. Biophys. Acta 585, 527-534 (1979).
81. Malkinson AM, Hogy L, Gharrett AJ, Gunderson TJ. Ontogenic studies of cyclic AMP-dependent protein kinase enzymes from mouse heart and other tissues. J. Exp. Zool. 205, 423-432 (1978).
82. Skalhegg BS, Landmark BF, Døskeland SO, Hansson V, Lea T, Jahnsen T. Cyclic AMP-dependent protein kinase type I mediates the inhibitory effect of 3′,5′-cyclic adenosine monophosphate on cell replication in human T lymphocytes. J. Biol. Chem. 267, 15707-15714 (1992).
83. Tasken K, Hansson V, Aukrust P et al. PKAI as a potential target for therapeutic intervention. Drug News Perspect. 13, 12-18 (2000).
84. Laxminarayana D, Kammer GM. mRNA mutations of type I protein kinase A regulatory subunit α in T lymphocytes as a subject with systemic lupus erythematosus. Int. Immunol. 12, 1521-1529 (2000)
85. Khan IU, Laxminarayana D, Kammer GM. Protein kinase A RI β subunit deficiency in lupus T lymphocytes: bypassing a block in RI β translation reconstitutes protein kinase A activity and augments IL-2 production. J. Immunol. 166, 7600-7605 (2001).
86. Lania A, Mantovani G, Ferrero S et al. Proliferation of transformed somatotroph cells related to low or absent expression of PKA regulatory subunit 1A protein. Cancer Res. 64, 9193-9198 (2004).
87. Griffin KJ, Kirschner LS, Matyakhina L et al. Down-regulation of regulatory subunit type 1A of protein kinase A leads to endocrine and other tumors. Cancer Res. 64, 8811-8815 (2004).
88. Deppert W. Mutant p53: from guardian to fallen angel? Oncogene 26, 2142-2144 (2007).
89. Cho-Chung YS, Nesterova MV. Tumor reversion: protein kinase A isozyme switching. Ann. NY Acad. Sci. 1058, 76-86 (2005).
90. Tortora G, Ciardiello F. Antisense targeting protein kinase A Type I as a drug for integrated strategies of cancer therapy. Ann. NY Acad. Sci. 1002, 236-243 (2003).