Impairment of adenylyl cyclase 2 function and expression in hypoxanthine phosphoribosyltransferase-deficient rat B103 neuroblastoma cells as model for Lesch-Nyhan disease: BODIPY-forskolin as pharmacological tool

Naunyn-Schmiedeberg's Archives of Pharmacology

Volumn 385, Issue 7, 2012, Pages 671-683

  Kinast, Liz ^a   Von Der Ohe, Juliane ^a   Burhenne, Heike ^a   Seifert, Roland ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Adenylyl cyclase; B103 rat neuroblastoma cells; BODIPY forskolin; Hypoxanthine phosphoribosyltransferase; Lesch Nyhan syndrome

Indexed keywords

2' (3') O (N METHYLANTHRANILOYL)GUANOSINE 5' (GAMMA THIO)TRIPHOSPHATE; 2' (3') O (N METHYLANTHRANILOYL)NUCLEOSIDE 5' (GAMMA THIO)TRIPHOSPHATE DERIVATIVE; 4,4 DIFLUORO 4 BORA 3A,4A DIAZA S INDACENE FORSKOLIN; ADENYLATE CYCLASE; ADENYLATE CYCLASE 1; ADENYLATE CYCLASE 2; ADENYLATE CYCLASE 5; CYCLIC AMP; FORSKOLIN DERIVATIVE; GUANOSINE TRIPHOSPHATE; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; LESCH NYHAN SYNDROME; NEUROBLASTOMA CELL; NONHUMAN; PATHOPHYSIOLOGY; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION;

ADENYLATE CYCLASE; ANIMALS; BORON COMPOUNDS; CELL LINE, TUMOR; ENZYME INHIBITORS; FLUORESCENT DYES; FORSKOLIN; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; ISOENZYMES; LESCH-NYHAN SYNDROME; NEUROBLASTOMA; RATS;

EID: 84862903683     PISSN: 00281298     EISSN: 14321912     Source Type: Journal    
DOI: 10.1007/s00210-012-0759-6     Document Type: Article

References (78)

1. Bogard AS, Xu C, Ostrom RS (2011) Human bronchial smooth muscle cells express adenylyl cyclase isoforms 2, 4, and 6 in distinct microdomains. J Pharmacol Exp Ther 337:209-217
2. Braumann T, Jastorff B, Richter-Landsberg C (1986) Fate of cyclic nucleotides in PC12 cell culture: uptake, metabolism, and effects of metabolites on nerve growth factor-induced neurite outgrowth. J Neurochem 47:912-919 (Pubitemid 16029576)
3. Cabral GA, McNerney PJ, Mishkin EM (1987) Interaction of delta-9tetrahydrocannabinol with rat B103 neuroblastoma cells. Arch Toxicol 60:438-449 (Pubitemid 17137307)
4. Calebiro D, Nikolaev VO, Gagliani MC, de Filippis T, Dees C, Tachetti C, Persani L, Lohse MJ (2009) Persistent cAMP-signals triggered by internalized G-protein-coupled receptors. PLoS Biol 7:e1000172
5. Chang CY, Ma KH, Wang JK, Tung YL, Chueh SH (2011) Inhibition of protein kinase C promotes differentiation of neuroblastoma× glioma NG108-15 hybrid cells. Eur J Neurosci 34:1074-1084
6. Connolly GP (2001) Hypoxanthine-guanine phosphoribosyltransferasedeficiency produces abberant neurite outgrowth of rodent neuroblastoma used to model the neurological disorder Lesch-Nyhan syndrome. Neurosci Lett 314:61-64 (Pubitemid 33043805)
7. Conti M, Beavo J (2007) Biochemistry and physiology of cyclic nucleotide phosphodiesterases: essential components in cyclic nucleotide signaling. Annu Rev Biochem 76:481-511
8. Copsel S, Garcia C, Diez F, Vermeulem M, Baldi A, Bianciotti LG, Russel FG, Shayo C, Davio C (2011) Multidrug resistance protein 4 (MRP4/ABCC4) regulates cAMP cellular levels and controls human leukemia cell proliferation and differentiation. J Biol Chem 286:6979-6988
9. Crespo-López ME, De Sá Lima A, Herculano AM, Rodríguez Burbano R, Martins do Nascimento JL (2007) Methylmercury genotoxicity: a novel effect in human cell lines of the central nervous system. Environ Int 33:141-146 (Pubitemid 44960458)
10. Defer N, Best-Belpomme M, Hanoune J (2000) Tissue specificity and physiological relevance of various isoforms of adenylyl cyclase. Am J Physiol Renal Physiol 279:F400-F416
11. Duley JA, Christodoulou J, de Brouwer AP (2011) The PRPP synthetase spectrum: what does it demonstrate about nucleotide syndromes? Nucleosides Nucleotides Nucleic Acids 30:1129-1139
12. Erdorf M, Seifert R (2011) Pharmacological characterization of adenylyl cyclase isoforms in rabbit kidney membranes. NaunynSchmiedeberg's Arch Pharmacol 383:357-372
13. 2Y receptor-mediated signaling in HPRT-deficient B103 neuroblastoma cells. Neurosci Lett 504:311-315
14. Erdorf M, Mou TC, Seifert R (2011b) Impact of divalent metal ions on regulation of adenylyl cyclase isoforms by forskolin analogs. Biochem Pharmacol 82:1673-1681
15. s-proteins. Naunyn-Schmiedeberg's Arch Pharmacol 368:210-215 (Pubitemid 37255482)
16. Gille A, Wenzel-Seifert K, Doughty MB, Seifert R (2003) GDP affinity and order state of the catalytic site are critical for function of xanthine nucleotide-selective Gαs proteins. J Biol Chem 278:7822-7828 (Pubitemid 36800515)
17. Gille A, Lushington GH, Mou TC, Doughty MB, Johnson RA, Seifert R (2004) Differential inhibition of adenylyl cyclase isoforms and soluble guanylyl cyclase by purine and pyrimidine nucleotides. J Biol Chem 279:19955-19969 (Pubitemid 38623438)
18. Gille A, Guo J, Mou TC, Doughty MB, Lushington GH, Seifert R (2005) Differential interactions of G-proteins and adenylyl cyclase with nucleoside 5'-triphosphates, nucleoside 5'-[γ-thio]triphosphates and nucleoside 5'-[β,γ-imido]triphosphates. Biochem Pharmacol 71:89-97 (Pubitemid 41713530)
19. Gilman AG (1987) G proteins: transducers of receptor-generated signals. Annu Rev Biochem 56:615-649
20. Göttle M, Geduhn J, König B, Gille A, Höcherl K, Seifert R (2009) Characterization of mouse heart adenylyl cyclase. J Pharmacol Exp Ther 329:1156-1165
21. Guibinga GH, Hsu S, Friedmann T (2010) Deficiency of the housekeeping gene hypoxanthine-guanine phosphoribosyltransferase (HPRT) dysregulates neurogenesis. Mol Ther 18:54-62
22. Guibinga GH, Hrustanovic G, Bouic K, Jinnah HA, Friedmann T (2012) MicroRNA-mediated dysregulation of neuronal development genes in HPRT deficiency: clues for Lesch-Nyhan disease? Hum Mol Genet 21:609-622
23. Hacke K, Szakmary A, Cuddihy AR, Rozengurt N, Lemp NA, Aubrecht J, Lawson GW, Rao NP, Crooks GM, Schiestl RH, Kasahara N (2012) Combined preconditioning and in vivo chemoselection with 6-thioguanine alone achieves highly efficient reconstitution of normal hematopoiesis with HPRT-deficient bone marrow. Exp Hematol 40:3-13.e3
24. Han JZ, Lin W, Lou SJ, Qiu J, Chen YZ (2002) A rapid, nongenomic action of glucocorticoids in rat B103 neuroblastoma cells. Biochim Biophys Acta 1591:21-27 (Pubitemid 35232064)
25. Han HE, Sellamuthu S, Shin BH, Lee YJ, Song S, Seo JS, Baek IS, Bae J, Kim H, Yoo YJ, Jung YK, Song WK, Han PL, Park WJ (2010) The nuclear inclusion a (NIa) protease of turnip mosaic virus (TuMV) cleaves amyloid-β. PLoS One 5:e15645
26. Harris JC (2010) Advances in understanding behavioral phenotypes in neurogenetic syndromes. Am J Med Genet 154C:389-399
27. s. J Biol Chem 272:19017-19021
28. Hirose M, Ishizaki T, Watanabe N, Uehata M, Kranenburg O, Moolenaar WH, Matsumura F, Maekawa M, Bito H, Narumiya S (1998) Molecular dissection of the rho-associated protein kinase (p160ROCK)-regulated neurite remodeling in neuroblastoma N1E-115 cells. J Cell Biol 141:1625-1636 (Pubitemid 28309176)
29. Ishii I, Chun J (2002) Anandamide-induced neuroblastoma cellrounding via the CB1 cannabinoid, receptors. NeuroReport 13:593-596 (Pubitemid 34293473)
30. Ishii K, Adachi Y, Hatanaka M, Sakamoto H, Furuyama JI (1990) Spontaneous and cAMP-dependent induction of a resting phase and neurite formation in cell hybrids between human neuroblastoma cells and thymidine auxotrophs of rat nerve-like cells. J Cell Physiol 143:569-576
31. Iwamoto T, Okumura S, Iwatsubo K, Kawabe J, Ohtsu K, Sakai I, Hashimoto Y, Izumitani A, Sango K, Ajiki K, Toya Y, Umemura S, Goshima Y, Arai N, Vatner SF, Ishikawa Y (2003) Motor dysfunction in type 5 adenylyl cyclase-null mice. J Biol Chem 278:16936-16940 (Pubitemid 36799567)
32. Iwasa H, Kikuchi S, Mine S, Miyagishima H, Sugita K, Sato T, Hasegawa S (2000) Up-regulation of type II adenylyl cyclase mRNA in kindling model of epilepsy in rats. Neurosci Lett 282:173-176 (Pubitemid 30136455)
33. Jalink K, Moolenaar WH (1992) Thrombin receptor activation causes rapid neural cell rounding and neurite retraction independent of classic second messengers. J Cell Biol 118:411-419
34. Jinnah HA (2009) Lesch-Nyhan disease: from mechanism to model and back again. Dis Model Mech 2:116-121
35. Jinnah HA, Friedmann T (2000) Lesch-Nyhan disease and its variants. In: Scriver C, Beaudet A, Sly W, Valle D, Kinzler KW, Vogelstein B (eds) The metabolic basis of inherited disease, vol Chapter 107, 8th edn. McGraw-Hill, New York
36. Jinnah HA, Langlais PJ, Friedmann T (1992) Functional analysis of brain dopamine systems in a genetic mouse model of Lesch-Nyhan syndrome. J Pharmacol Exp Ther 263:596-607
37. Kang TH, Guibinga GH, Jinnah HA, Friedmann T (2011) HPRT deficiency coordinately dysregulates canonical Wnt and presenilin-1 signaling: a neuro-developmental regulatory role for a housekeeping gene? PLoS One 6:e16572
38. Kato K, Fukui R, Okabe K, Tanabe E, Kitayoshi M, Fukushima N, Tsujiuchi T (2012) Constitutively active lysophosphatidic acid receptor-1 enhances the induction of matrix metalloproteinase-2. Biochem Biophys Res Commun 417:790-793
39. 2+ influx on endothelin-1-induced mitogenesis. Eur J Pharmacol 425:173-179 (Pubitemid 32770064)
40. Kim KS, Han PL (2009) Mice lacking adenylyl cyclase-5 cope badly with repeated restraint stress. J Neurosci Res 87:2983-2993
41. Kim KS, Kim H, Baek IS, Lee KW, Han PL (2011) Mice lacking adenylyl cyclase type 5 (AC5) show increased ethanol consumption and reduced ethanol sensitivity. Psychopharmacology (Berl) 215:391-398
42. A receptors. Biosci Rep 19:535-546 (Pubitemid 30351185)
43. Laurenza A, Khandelwal Y, de Souza NJ, Rupp RH, Metzger H, Seamon KB (1987) Stimulation of adenylate cyclase by watersoluble analogues of forskolin. Mol Pharmacol 32:133-139 (Pubitemid 17112325)
44. Laurenza A, Sutkowski EM, Seamon KB (1989) Forskolin: a specific stimulator of adenylyl cyclase or a diterpene with multiple sites of action? Trends Pharmacol Sci 10:442-447 (Pubitemid 19264294)
45. Lecoeur H (2002) Nuclear apoptosis detection by flow cytometry: influence of endogenous endonucleases. Exp Cell Res 277:1-14 (Pubitemid 34948336)
46. Lee KW, Hong JH, Choi IY, Che Y, Lee JK, Yang SD, Song CW, Kang HS, Lee JH, Noh JS, Han PL (2002) Impaired D2 dopamine receptor function in mice lacking type 5 adenylyl cyclase. J Neurosci 22:7931-7940 (Pubitemid 35379098)
47. Liu CY, Zhang H, Christofi FL (1998) Adenylyl cyclase co-distribution with the CaBPs, calbindin-D28 and calretinin with cell type. Assessment with the fluorescent dye, BODIPY forskolin, in enteric ganglia. Cell Tissue Res 293:57-73 (Pubitemid 28331975)
48. Lorenz V, Pinto CS, Seifert R (2007) Complex changes in ectonucleoside 5'-triphosphate diphosphohydrolase expression in hypoxanthine phosphoribosyl transferase deficiency. Neurosci Lett 420:6-11 (Pubitemid 46777102)
49. Ma MH, Stacey NC, Connolly GP (2001) Hypoxanthine impairs morphogenesis and enhances proliferation of a neuroblastoma model of Lesch Nyhan syndrome. J Neurosci Res 63:500-508 (Pubitemid 32193707)
50. Mastrangelo L, Kim JE, Miyanohara A, Kang TH, Friedmann T (2012) Purinergic signaling in human pluripotent stem cells is regulated by the housekeeping gene encoding hypoxanthine guanine phosphoribosyltransferase. Proc Natl Acad Sci USA 109:3377-3382
51. Matsuoka I, Suzuki Y, Defer N, Nakanishi H, Hanoune J (1997) Differential expression of type I, II, and V adenylyl cyclase gene in the postnatal developing rat brain. J Neurochem 68:498-506 (Pubitemid 27044708)
52. sα. Biochemistry 33:12852-12859 (Pubitemid 24352876)
53. Monaghan TK, MacKenzie CJ, Plevin R, Lutz EM (2008) PACAP-38 induces neuronal differentiation of human SH-SY5Y neuroblastoma cells via cAMP-mediated activation of ERK and p38 MAP kinases. J Neurochem 104:74-88 (Pubitemid 350265065)
54. Mons N, Segu L, Nogues X, Buhot MC (2004) Effects of age and spatial learning on adenylyl cyclase mRNA expression in mouse hippocampus. Neurobiol Aging 25:1095-1106 (Pubitemid 38798071)
55. o proteins in modulation of adenylyl cyclase type-2 activity. J Neurochem 83:1252-1261 (Pubitemid 35477465)
56. Nguyen CH, Watts VJ (2006) Dexamethasone-induced ras protein 1 negatively regulates protein kinase C 6: implications for adenylyl cyclase 2 signaling. Mol Pharmacol 69:1763-1771
57. 2-Adrenergic receptor distribution in heart failure changes cAMP compartmentation. Science 327:1653-1657
58. Nyhan WL (1997) The recognition of Lesch-Nyhan syndrome as an inborn error of purine metabolism. J Inherit Metab Dis 20:171178
59. Ostrom RS, Bogard AS, Gros R, Feldman RD (2012) Choreographing the adenylyl cyclase signalosome: sorting out the partners and the steps. Naunyn-Schmiedeberg's Arch Pharmacol 385:5-12
60. Pieroni JP, Chen HA, Jacobowitz O, Magnusson RP, Iyengar R (1995) Distinct characteristics of the basal activities of adenylyl cyclases 2 and 6. J Biol Chem 270:21368-21373
61. Pierre S, Eschenhagen T, Geisslinger G, Scholich K (2009) Capturing adenylyl cyclases as potential drug targets. Nat Rev Drug Discov 8:321-335
62. Pinto CS, Seifert R (2006) Decreased GTP-stimulated adenylyl cyclase activity in HPRT-deficient human and mouse fibroblast and rat B103 neuroblastoma cell membranes. J Neurochem 96:454-459
63. Pinto CS, Jinnah HA, Shirley TL, Nyhan WL, Seifert R (2005) Altered membrane NTPase activity in Lesch-Nyhan disease fibroblasts: Comparison with HPRT knock-out mice and HPRT-deficient cell lines. J Neurochem 93:1579-1586 (Pubitemid 40853281)
64. Pinto C, Papa D, Hübner M, Mou TC, Lushington GH, Seifert R (2008) Activation and inhibition of adenylyl cyclase isoforms by forskolin analogs. J Pharmacol Exp Ther 325:27-36 (Pubitemid 351439155)
65. Sadana R, Dessauer CW (2009) Physiological roles for G proteinregulated adenylyl cyclase isoforms: insights from knockout and overexpression studies. Neurosignals 17:5-22
66. Schallmach E, Steiner D, Vogel Z (2006) Inhibition of AC-II activity following chronic agonist exposure is modulated by phosphorylation. J Mol Neurosci 29:115-122 (Pubitemid 44352535)
67. Schubert D, Heinemann S, Carlisle W, Tarikas H, Kimes B, Patrick J, Steinbach JH (1974) Clonal cell lines from the rat central nervous system. Nature 249:224-227
68. Seamon KB, Padgett W, Daly JW (1981) Forskolin: unique diterpene activator of adenylate cyclase in membranes and intact cells. Proc Natl Acad Sci USA 78:3363-3367 (Pubitemid 11059290)
69. Seifert R, Wenzel-Seifert K (2002) Constitutive activity of G-proteincoupled receptors: cause of disease and common property of wildtype receptors. Naunyn-Schmiedeberg's Arch Pharmacol 366:381-416 (Pubitemid 35251788)
70. Seifert R, Lushington GH, Mou TC, Gille A, Sprang SR (2012) Inhibitors of membranous adenylyl cyclases. Trends Pharmacol Sci 33:64-78
71. Shirley TL, Lewers JC, Egami K, Majumdar A, Kelly M, CeballosPicot I, Seidman MM, Jinnah HA (2007) A human neuronal tissue culture model for Lesch-Nyhan disease. J Neurochem 101:841-853 (Pubitemid 46633331)
72. Song S, Friedmann T (2007) Tissue-specific aberrations of gene expression in HPRT-deficient mice: functional complexity in a monogenic disease? Mol Ther 15:1432-1443 (Pubitemid 47099300)
73. Sunahara R, Taussig R (2002) Isoforms of mammalian adenylyl cyclase: multiplicities of signaling. Mol Interv 2:168-184
74. Tanura H, Fukada M, Fujikawa A, Noda M (2006) Protein tyrosine phosphatase receptor type Z is involved in hippocampusdependent memory formation through dephosphorylation at Y1105 on p190 RhoGAP. Neurosci Lett 399:33-38
75. Torres RJ, Puig JG, Jinnah HA (2012) Update on the phenotypic spectrum of Lesch-Nyhan disease and its attenuated variants. Curr Rheumatol Rep 14:189-194
76. Wang T, Brown MJ (2004) Differential expression of adenylyl cyclase subtypes in human cardiovascular system. Mol Cell Endocrinol 223:55-62 (Pubitemid 38992910)
77. Wolter S, Doerrie A, Weber A, Schneider H, Hoffmann E, von der Ohe J, Bakiri L, Wagner EF, Resch K, Kracht M (2008) c-Jun controls NF-κB recruitment, and polymerase II function to activate ccl2 gene. Mol Cell Biol 28:4407-4423 (Pubitemid 351904962)
78. Zoref-Shani E, Bromberg Y, Brosh S, Sidi Y, Sperling O (1993) Characterization of the alterations in purine nucleotide metabolism in hypoxanthine-guanine phosphoribosyltransferasedeficient rat neuroma cell line. J Neurochem 61:457-463 (Pubitemid 23215787)