8Cl-cAMP modifies the balance between PKAR1 and PKAR2 and modulates the cell cycle, growth and apoptosis in human adrenocortical H295R cells

Journal of Molecular Endocrinology

Volumn 44, Issue 6, 2010, Pages 331-347

  Bouizar, Zhor ^a,b   Ragazzon, Bruno ^a,b   Viou, Lucie ^a,b   Hortane, Mariuccia ^a,b   Bertherat, Jerôme ^a,b,c   Rizk Rabin, Marthe ^a,b  

^a INSTITUT COCHIN   (France)

^b INSERM   (France)

^c Groupe Hospitalier Cochin St Vincent de Paul ^*  (France)

Author keywords

[No Author keywords available]

Indexed keywords

8 CHLOROADENOSINE 3',5' PHOSPHATE; CELL NUCLEUS ANTIGEN; CYCLIC AMP DEPENDENT PROTEIN KINASE REGULATORY SUBUNIT IALPHA; CYCLIC AMP DEPENDENT PROTEIN KINASE REGULATORY SUBUNIT IIBETA; CYCLIN A; CYCLIN B; CYCLIN DEPENDENT KINASE 2; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ADRENAL CORTEX CELL; APOPTOSIS; ARTICLE; CELL CYCLE; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE S PHASE; CELL GROWTH; CELL NUCLEUS; CELL PROLIFERATION; CONTROLLED STUDY; DNA SYNTHESIS; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; PRIORITY JOURNAL;

8-BROMO CYCLIC ADENOSINE MONOPHOSPHATE; ADRENAL CORTEX; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLIC AMP-DEPENDENT PROTEIN KINASE RIALPHA SUBUNIT; CYCLIC AMP-DEPENDENT PROTEIN KINASE RIIALPHA SUBUNIT; CYCLIN-DEPENDENT KINASE 2; DNA REPLICATION; HUMANS; PROLIFERATING CELL NUCLEAR ANTIGEN; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 77952775652     PISSN: 09525041     EISSN: 14796813     Source Type: Journal    
DOI: 10.1677/JME-09-0120     Document Type: Article

References (62)

1. Bailly E & Bornens M 1992 Cell biology. Centrosome and cell division. Nature 355 300-301.
2. Beppu T, Ishida Y, Arai H, Wada T, Uesugi N & Sasaki K 1994 Identification of S-phase cells with PC10 antibody to proliferating cell nuclear antigen (PCNA) by flow cytometric analysis. Journal of Histochemistry and Cytochemistry 42 1177-1182. (Pubitemid 24226347)
3. Bertherat J 2001 Protein kinase A in Carney complex: a new example of cAMP pathway alteration in endocrine tumors. European Journal of Endocrinology 144 209-211. (Pubitemid 32266288)
4. Bertherat J, Groussin L, Sandrini F,Matyakhina L, Bei T, Stergiopoulos S, Papageorgiou T, Bourdeau I, Kirschner LS, Vincent-Dejean C et al. 2003 Molecular and functional analysis of PRKAR1A and its locus (17q22-24) in sporadic adrenocortical tumors: 17q losses, somatic mutations, and protein kinase A expression and activity. Cancer Research 63 5308-5319. (Pubitemid 37139845)
5. Bossis I & Stratakis CA 2004 Minireview: PRKAR1A: normal and abnormal functions. Endocrinology 145 5452-5458. (Pubitemid 39564583)
6. Carney JA, Gordon H, Carpenter PC, Shenoy BV & Go VL 1985 The complex of myxomas, spotty pigmentation, and endocrine overactivity. Medicine 64 270-283. (Pubitemid 16247109)
7. Cheadle C, Nesterova M, Watkins T, Barnes KC, Hall JC, Rosen A, Becker KG & Cho-Chung YS 2008 Regulatory subunits of PKA define an axis of cellular proliferation/differentiation in ovarian cancer cells. BMC Medical Genomics 1 43.
8. Cho YS, Kim MK, Tan L, Srivastava R, Agrawal S & Cho-Chung YS 2002 Protein kinase A RIalpha antisense inhibition of PC3M prostate cancer cell growth: Bcl-2 hyperphosphorylation, Bax up-regulation, and Bad- hypophosphorylation. Clinical Cancer Research 8 607-614.
9. Cho-Chung YS 2004 Antisense protein kinase A RI alpha-induced tumor reversion: portrait of a microarray. Biochimica et Biophysica Acta 1697 71-79. (Pubitemid 38326762)
10. Cho-Chung YS & Nesterova MV 2005 Tumor reversion: protein kinase A isozyme switching. Annals of the New York Academy of Sciences 1058 76-86.
11. Ciardiello F, Pepe S, Bianco C, Baldassarre G, Ruggiero A, Bianco C, Selvam MP, Bianco AR & Tortora G 1993 Down-regulation of RI alpha subunit of cAMP-dependent protein kinase induces growth inhibition of human mammary epithelial cells transformed by c-Ha-ras and c-erbB-2 proto-oncogenes. International Journal of Cancer 53 438-443. (Pubitemid 23047892)
12. Dransfield DT, Griner RD, Ray S, Keskintepe M & Bollag WB 2001 8-Cl-adenosine induces growth arrest without differentiation of primary mouse epidermal keratinocytes. Journal of Investigative Dermatology 117 1588-1593. (Pubitemid 34032792)
13. Duckworth BC, Weaver JS & Ruderman JV 2002 G2 arrest in Xenopus oocytes depends on phosphorylation of cdc25 by protein kinase A. PNAS 99 16794-16799. (Pubitemid 36034052)
14. Dyson MT, Kowalewski MP, Manna PR & Stocco DM 2009 The differential regulation of steroidogenic acute regulatory protein-mediated steroidogenesis by type I and type II PKA in MA-10 cells. Molecular and Cellular Endocrinology 300 94-103.
15. Gazdar AF, Oie HK, Shackleton CH, Chen TR, Triche TJ, Myers CE, Chrousos GP, Brennan MF, Stein CA & La Rocca RV 1990 Establishment and characterization of a human adrenocortical carcinoma cell line that expresses multiple pathways of steroid biosynthesis. Cancer Research 50 5488-5496.
16. Griffin KJ, Kirschner LS, Matyakhina L, Stergiopoulos S, Robinson-White A, Lenherr S, Weinberg FD, Claflin E, Meoli E, Cho-Chung YS et al. 2004a Down-regulation of regulatory subunit type 1A of protein kinase A leads to endocrine and other tumors. Cancer Research 64 8811-8815. (Pubitemid 39665482)
17. Griffin KJ, Kirschner LS, Matyakhina L, Stergiopoulos SG, Robinson-White A, Lenherr SM,Weinberg FD, Claflin ES, Batista D, Bourdeau I et al. 2004b A transgenic mouse bearing an antisense construct of regulatory subunit type 1A of protein kinase A develops endocrine and other tumours: comparison with Carney complex and other PRKAR1A induced lesions. Journal of Medical Genetics 41 923-931. (Pubitemid 40007253)
18. Groussin L, Massias JF, Bertagna X & Bertherat J 2000 Loss of expression of the ubiquitous transcription factor cAMP response element-binding protein (CREB) and compensatory overexpression of the activator CREMtau in the human adrenocortical cancer cell line H295R. Journal of Clinical Endocrinology and Metabolism 85 345-354. (Pubitemid 32268836)
19. Groussin L, Kirschner LS, Vincent-Dejean C, Perlemoine K, Jullian E, Delemer B, Zacharieva S, Pignatelli D, Carney JA, Luton JP et al. 2002a 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. American Journal of Human Genetics 71 1433-1442. (Pubitemid 36018745)
20. Groussin L, Jullian E, Perlemoine K, Louvel A, Leheup B, Luton JP, Bertagna X & Bertherat J 2002b Mutations of the PRKAR1A gene in Cushing's syndrome due to sporadic primary pigmented nodular adrenocortical disease. Journal of Clinical Endocrinology and Metabolism 87 4324-4329.
21. Groussin L, Horvath A, Jullian E, Boikos S, Rene-Corail F, Lefebvre H, Cephise-Velayoudom FL, Vantyghem MC, Chanson P, Conte-Devolx B et al. 2006 A PRKAR1A mutation associated with primary pigmented nodular adrenocortical disease in 12 kindreds. Journal of Clinical Endocrinology and Metabolism 91 1943-1949.
22. Horvath A, Boikos S, Giatzakis C, Robinson-White A, Groussin L, Griffin KJ, Stein E, Levine E, Delimpasi G, Hsiao HP et al. 2006 A genome-wide scan identifies mutations in the gene encoding phosphodiesterase 11A4 (PDE11A) in individuals with adrenocortical hyperplasia. Nature Genetics 38 794-800. (Pubitemid 43980600)
23. Horvath A, Giatzakis C, Tsang K, Greene E, Osorio P, Boikos S, Libe R, Patronas Y, Robinson-White A, Remmers E et al. 2008 A cAMP-specific phosphodiesterase (PDE8B) that is mutated in adrenal hyperplasia is expressed widely in human and mouse tissues: a novel PDE8B isoform in human adrenal cortex. European Journal of Human Genetics 16 1245-1253.
24. Jaroenporn S, Furuta C, Nagaoka K, Watanabe G & Taya K 2008 Comparative effects of prolactin versus ACTH, estradiol, progesterone, testosterone, and dihydrotestosterone on cortisol release and proliferation of the adrenocortical carcinoma cell line H295R. Endocrine 33 205-209.
25. Kim SN, Kim SG, Park JH, Lee MA, Park SD, Cho-Chung YS & Hong SH 2000 Dual anticancer activity of 8-Cl-cAMP: inhibition of cell proliferation and induction of apoptotic cell death. Biochemical and Biophysical Research Communications 273 404-410.
26. Kim SN, Ahn YH, Kim SG, Park SD, Cho-Chung YS & Hong SH 2001 8-Cl-cAMP induces cell cycle-specific apoptosis in human cancer cells. International Journal of Cancer 93 33-41. (Pubitemid 32539498)
27. Kirschner LS, Sandrini F, Monbo J, Lin JP, Carney JA & Stratakis CA 2000 Genetic heterogeneity and spectrum of mutations of the PRKAR1A gene in patients with the carney complex. Human Molecular Genetics 9 3037-3046. (Pubitemid 32000777)
28. Knutsen HK, Reinton N, Tasken KA, Hansson V & Eskild W 1996 Regulation of protein kinase A subunits by cyclic adenosine 3′,5′- monophosphate in a mouse Sertoli cell line (MSC-1): induction of RII beta messenger ribonucleic acid is independent of continuous protein synthesis. Biology of Reproduction 55 5-10. (Pubitemid 26293134)
29. Koopman G, Reutelingsperger CP, Kuijten GA, Keehnen RM, Pals ST & van Oers MH 1994 Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood 84 1415-1420. (Pubitemid 24273007)
30. Lange-Carter CA, Vuillequez JJ & Malkinson AM 1993 8-Chloroadenosine mediates 8-chloro-cyclic AMP-induced down-regulation of cyclic AMP-dependent protein kinase in normal and neoplastic mouse lung epithelial cells by a cyclic AMP-independent mechanism. Cancer Research 53 393-400.
31. Lania AG, Mantovani G, Ferrero S, Pellegrini C, Bondioni S, Peverelli E, Braidotti P, Locatelli M, Zavanone ML, Ferrante E et al. 2004 Proliferation of transformed somatotroph cells related to low or absent expression of protein kinase a regulatory subunit 1A protein. Cancer Research 64 9193-9198. (Pubitemid 40003794)
32. Libe R, Fratticci A, Coste J, Tissier F, Horvath A, Ragazzon B, Rene-Corail F, Groussin L, Bertagna X, Raffin-Sanson ML et al. 2008 Phosphodiesterase 11A (PDE11A) and genetic predisposition to adrenocortical tumors. Clinical Cancer Research 14 4016-4024.
33. Liu J, Li XD, Ora A, Heikkila P, Vaheri A & Voutilainen R 2004a cAMP-dependent protein kinase activation inhibits proliferation and enhances apoptotic effect of tumor necrosis factor-alpha in NCI-H295R adrenocortical cells. Journal of Molecular Endocrinology 33 511-522. (Pubitemid 39429573)
34. Liu J, Hu JY, Schacher S & Schwartz JH 2004b The two regulatory subunits of aplysia cAMP-dependent protein kinase mediate distinct functions in producing synaptic plasticity. Journal of Neuroscience 24 2465-2474. (Pubitemid 38327960)
35. Livesey SA, Kemp BE, Re CA, Partridge NC & Martin TJ 1982 Selective hormonal activation of cyclic AMP-dependent protein kinase isoenzymes in normal and malignant osteoblasts. Journal of Biological Chemistry 257 14983-14987.
36. Mantovani G, Lania AG, Bondioni S, Peverelli E, Pedroni C, Ferrero S, Pellegrini C, Vicentini L, Arnaldi G, Bosari S et al. 2008a Different expression of protein kinase A (PKA) regulatory subunits in cortisol-secreting adrenocortical tumors: relationship with cell proliferation. Experimental Cell Research 314 123-130. (Pubitemid 350180780)
37. Mantovani G, Bondioni S, Lania AG, Rodolfo M, Peverelli E, Polentarutti N, Veliz Rodriguez T, Ferrero S, Bosari S, Beck-Peccoz P et al. 2008b High expression of PKA regulatory subunit 1A protein is related to proliferation of human melanoma cells. Oncogene 27 1834-1843. (Pubitemid 351430825)
38. McDaid HM, Cairns MT, Atkinson RJ, McAleer S, Harkin DP, Gilmore P & Johnston PG 1999 Increased expression of the RIalpha subunit of the cAMP-dependent protein kinase A is associated with advanced stage ovarian cancer. British Journal of Cancer 79 933-939. (Pubitemid 29082129)
39. Mikhaylova IV, Kuulasmaa T, Jaaskelainen J & Voutilainen R 2007 Tumor necrosis factor-alpha regulates steroidogenesis, apoptosis, and cell viability in the human adrenocortical cell line NCI-H295R. Endocrinology 148 386-392. (Pubitemid 46021471)
40. Miller WR, Hulme MJ, Cho-Chung YS & Elton RA 1993 Types of cyclic AMP binding proteins in human breast cancers. European Journal of Cancer 29A 989-991.
41. Neary CL, Nesterova M, Cho YS, Cheadle C, Becker KG & Cho-Chung YS 2004 Protein kinase A isozyme switching: eliciting differential cAMP signaling and tumor reversion. Oncogene 23 8847-8856. (Pubitemid 39593299)
42. Nesterova M & Cho-Chung YS 2000 Oligonucleotide sequence-specific inhibition of gene expression, tumor growth inhibition, and modulation of cAMP signaling by an RNA - DNA hybrid antisense targeted to protein kinase A RIalpha subunit. Antisense & Nucleic Acid Drug Development 10 423-433. (Pubitemid 32058031)
43. Nesterova M, Noguchi K, Park YG, Lee YN & Cho-Chung YS 2000 Compensatory stabilization of RIIbeta protein, cell cycle deregulation, and growth arrest in colon and prostate carcinoma cells by antisense-directed down-regulation of protein kinase A RIalpha protein. Clinical Cancer Research 6 3434-3441.
44. Nesterova M, Bossis I, Wen F, Horvath A, Matyakhina L & Stratakis CA 2008 An immortalized human cell line bearing a PRKAR1A-inactivating mutation: effects of overexpression of the wild-type Allele and other protein kinase A subunits. Journal of Clinical Endocrinology and Metabolism 93 565-571. (Pubitemid 351240832)
45. Pepe S, Tortora G, Noguchi PD, Marti GE, Washington GC & Cho-Chung YS 1991 Effects of 8-chloroadenosine 3′,5′-monophosphate and N6-benzyl-cyclic adenosine 5′-monophosphate on cell cycle kinetics of HL-60 leukemia cells. Cancer Research 51 6263-6267.
46. Pines J & Hunter T 1991 Human cyclins A and B1 are differentially located in the cell and undergo cell cycle-dependent nuclear transport. Journal of Cell Biology 115 1-17. (Pubitemid 21909889)
47. Porter DC, Zhang N, Danes C, McGahren MJ, Harwell RM, Faruki S & Keyomarsi K 2001 Tumor-specific proteolytic processing of cyclin E generates hyperactive lower-molecular-weight forms. Molecular and Cellular Biology 21 6254-6269. (Pubitemid 34263525)
48. Ragazzon B, Cazabat L, Rizk-Rabin M, Assie G, Groussin L, Fierrard H, Perlemoine K, Martinez A & Bertherat J 2009 Inactivation of the Carney complex gene 1 (protein kinase A regulatory subunit 1A) inhibits SMAD3 expression and TGF beta-stimulated apoptosis in adrenocortical cells. Cancer Research 69 7278-7284.
49. Rainey WE, Bird IM & Mason I 1994 The NCI-H295 cell line: a pluripotent model for human adrenocortical studies. Molecular and Cellular Endocrinology 100 45-50. (Pubitemid 24109525)
50. Rainey WE, Saner K & Schimmer BP 2004 Adrenocortical cell lines. Molecular and Cellular Endocrinology 228 23-38.
51. Rizk-Rabin M, Assie G, Rene-Corail F, Perlemoine K, Hamzaoui H, Tissier F, Lieberherr M, Bertagna X, Bertherat J & Bouizar Z 2008 Differential expression of parathyroid hormone-related protein in adrenocortical tumors: autocrine/paracrine effects on the growth and signaling pathways in H295R cells. Cancer Epidemiology, Biomarkers & Prevention 17 2275-2285.
52. Robinson-White AJ, Hsiao HP, Leitner WW, Greene E, Bauer A, Krett NL, Nesterova M & Stratakis CA 2008 Protein kinase A-independent inhibition of proliferation and induction of apoptosis in human thyroid cancer cells by 8-Cl-adenosine. Journal of Clinical Endocrinology and Metabolism 93 1020-1029. (Pubitemid 351398588)
53. Rohlff C, Clair T & Cho-Chung YS 1993 8-Cl-cAMP induces truncation and down-regulation of the RI alpha subunit and up-regulation of the RII beta subunit of cAMP-dependent protein kinase leading to type II holoenzyme-dependent growth inhibition and differentiation of HL-60 leukemia cells. Journal of Biological Chemistry 268 5774-5782. (Pubitemid 23090906)
54. Rosenberg D, Groussin L, Bertagna X & Bertherat J 2002 cAMP pathway alterations from the cell surface to the nucleus in adrenocortical tumors. Endocrine Research 28 765-775. (Pubitemid 36050044)
55. Shibuya EK 2003 G2 cell cycle arrest - a direct link between PKA and Cdc25C. Cell Cycle 2 39-41.
56. Stoika RS, Yakymovych IA, Kashchak NI, Boyko MM, Korynevska AV, Klyuchyvska OY, Shafranska GI, Yakymovych MY, Zhylchuk VY, Kudryavets YYet al. 2008 Effect of anticancer drugs on production of transforming growth factor and expression of p53 and Bcl-2 proteins by MCF-7 and T47D cell lines of human breast carcinoma. Experimental Oncology 30 35-41.
57. Stubbs AP, Lalani EN, Stamp GW, Hurst H, Abel P & Waxman J 1996 Second messenger up-regulation of androgen receptor gene transcription is absent in androgen insensitive human prostatic carcinoma cell lines, PC-3 and DU-145. FEBS Letters 383 237-240. (Pubitemid 26104068)
58. Tasken K & Aandahl EM 2004 Localized effects of cAMP mediated by distinct routes of protein kinase A. Physiological Reviews 84 137-167. (Pubitemid 38049878)
59. Uzbekov RE 2004 Analysis of the cell cycle and a method employing synchronized cells for study of protein expression at various stages of the cell cycle. Biochemistry 69 485-496.
60. Veugelers M, Wilkes D, Burton K, McDermott DA, Song Y, Goldstein MM, La Perle K, Vaughan CJ, O'Hagan A, Bennett KR et al. 2004 Comparative PRKAR1A genotype - phenotype analyses in humans with Carney complex and prkar1a haploinsufficient mice. PNAS 101 14222-14227. (Pubitemid 39305057)
61. Vincent-Dejean C, Cazabat L, Groussin L, Perlemoine K, Fumey G, Tissier F, Bertagna X & Bertherat J 2008 Identification of a clinically homogenous subgroup of benign cortisol-secreting adrenocortical tumors characterized by alterations of the protein kinase A (PKA) subunits and high PKA activity. European Journal of Endocrinology 158 829-839. (Pubitemid 351837372)
62. Yamasaki H, Mizusawa N, Nagahiro S, Yamada S, Sano T, Itakura M & Yoshimoto K 2003 GH-secreting pituitary adenomas infrequently contain inactivating mutations of PRKAR1A and LOH of 17q23-24. Clinical Endocrinology 58 464-470. (Pubitemid 36390619)