Phosphodiesterase-4D knock-out and RNA interference-mediated knock-down enhance memory and increase hippocampal neurogenesis via increased cAMP signaling

Journal of Neuroscience

Volumn 31, Issue 1, 2011, Pages 172-183

  Li, Yun Feng ^a,d   Cheng, Yu Fang ^a,e   Huang, Ying ^a   Conti, Marco ^b   Wilson, Steven P ^c   O'Donnell, James M ^a   Zhang, Han Ting ^a  

^a WEST VIRGINIA UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d BEIJING INSTITUTE OF PHARMACOLOGY AND TOXICOLOGY   (China)

^e SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ADRENERGIC RECEPTOR; CYCLIC AMP; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; LENTIVIRUS VECTOR; MICRORNA; PHOSPHODIESTERASE IV; PHOSPHODIESTERASE IV INHIBITOR; ROLIPRAM;

ANESTHESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; DOWN REGULATION; HIPPOCAMPUS; INTRACELLULAR SIGNALING; MALE; MEMORY; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE; VOMITING; WILD TYPE;

ANALYSIS OF VARIANCE; ANIMALS; AVOIDANCE LEARNING; BROMODEOXYURIDINE; CREB-BINDING PROTEIN; CYCLIC AMP; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 4; EXPLORATORY BEHAVIOR; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; MALE; MAZE LEARNING; MEMORY; MICE; MICE, INBRED C57BL; MICE, INBRED ICR; MICE, KNOCKOUT; MICRORNAS; NERVE TISSUE PROTEINS; NEUROGENESIS; NEUROPSYCHOLOGICAL TESTS; PHOSPHODIESTERASE 4 INHIBITORS; RECOGNITION (PSYCHOLOGY); RNA INTERFERENCE; ROLIPRAM; SIGNAL TRANSDUCTION; SOXB1 TRANSCRIPTION FACTORS; TIME FACTORS;

EID: 78650891913     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5236-10.2011     Document Type: Article

References (87)

1. Abel T, Kandel E (1998) Positive and negative regulatory mechanisms that mediate long-term memory storage. Brain Res Brain Res Rev 26:360-378.
2. Baillie GS, MacKenzie SJ, McPhee I, Houslay MD (2000) Sub-family selective actions in the ability of Erk2 MAP kinase to phosphorylate and regulate the activity of PDE4 cyclic AMP-specific phosphodiesterases. Br J Pharmacol 131:811-819.
3. Barad M, Bourtchouladze R, Winder DG, Golan H, Kandel E (1998) Rolipram, a type IV-specific phosphodiesterase inhibitor, facilitates the establishment of long-lasting long-term potentiation and improves memory. Proc Natl Acad Sci U S A 95:15020-15025.
4. Barco A, Pittenger C, Kandel ER (2003) CREB, memory enhancement and the treatment of memory disorders: promises, pitfalls and prospects. Expert Opin Ther Targets 7:101-114.
5. Bolger GB, McPhee I, Houslay MD (1996) Alternative splicing of cAMP-specific phosphodiesterase mRNA transcripts: characterization of a novel tissue-specific isoform, RNPDE4A8. J Biol Chem 271:1065-1071.
6. Bolger GB, Erdogan S, Jones RE, Loughney K, Scotland G, Hoffmann R, Wilkinson I, Farrell C, Houslay MD (1997) Characterization of five different proteins produced by alternatively spliced mRNAs from the human cAMP-specific phosphodiesterase PDE4D gene. Biochem J 328:539-548.
7. Bourtchouladze R, Lidge R, Catapano R, Stanley J, Gossweiler S, Romashko D, Scott R, Tully T (2003) A mouse model of Rubinstein-Taybi syndrome: defective long-term memory is ameliorated by inhibitors of phosphodiesterase 4. Proc Natl Acad Sci U S A 100:10518-10522.
8. Boyes BE, Kim SU, Lee V, Sung SC (1986) Immunohistochemical colocalization of S-100β and the glial fibrillary acidic protein in rat brain. Neuroscience 17:857-865.
9. Bruel-Jungerman E, Laroche S, Rampon C (2005) New neurons in the dentate gyrus are involved in the expression of enhanced long-term memory following environmental enrichment. Eur J Neurosci 21:513-521.
10. Burgin AB, Magnusson OT, Singh J, Witte P, Staker BL, Bjornsson JM, Thorsteinsdottir M, Hrafnsdottir S, Hagen T, Kiselyov AS, Stewart LJ, Gurney ME (2010) Design of phosphodiesterase 4D (PDE4D) allosteric modulators for enhancing cognition with improved safety. Nat Biotechnol 28:63-70.
11. Chandrasekaran A, Toh KY, Low SH, Tay SK, Brenner S, Goh DL (2008) Identification and characterization of novel mouse PDE4D isoforms: molecular cloning, subcellular distribution and detection of isoform-specific intracellular localization signals. Cell Signal 20:139-153.
12. Cherry JA, Davis RL (1999) Cyclic AMP phosphodiesterases are localized in regions of the mouse brain associated with reinforcement, movement, and affect. J Comp Neurol 407:287-301.
13. Cheung YF, Kan Z, Garrett-Engele P, Gall I, Murdoch H, Baillie GS, Camargo LM, Johnson JM, Houslay MD, Castle JC (2007) PDE4B5, a novel, super-short, brain-specific cAMP phosphodiesterase-4 variant whose isoform-specifying N-terminal region is identical to that of cAMP phosphodiesterase-4D6 (PDE4D6). J Pharmacol Exp Ther 322:600-609.
14. Conti M, Richter W, Mehats C, Livera G, Park JY, Jin C (2003) Cyclic AMP-specific PDE4 phosphodiesterases as critical components of cyclic AMP signaling. J Biol Chem 278:5493-5496.
15. Cullen BR (2005) RNAi the natural way. Nat Genet 37:1163-1165.
16. de Lima MN, Laranja DC, Bromberg E, Roesler R, Schröder N (2005) Preor post-training administration of the NMDA receptor blocker MK-801 impairs object recognition memory in rats. Behav Brain Res 156:139-143.
17. Dlaboga D, Hajjhussein H, O'Donnell JM (2006) Regulation of phosphodiesterase-4 (PDE4) expression in mouse brain by repeated antidepressant treatment: comparison with rolipram. Brain Res 1096:104-112.
18. D'Sa C, Eisch AJ, Bolger GB, Duman RS (2005) Differential expression and regulation of the cAMP-selective phosphodiesterase type 4A splice variants in rat brain by chronic antidepressant administration. Eur J Neurosci 22:1463-1475.
19. Dull T, Zufferey R, Kelly M, Mandel RJ, Nguyen M, Trono D, Naldini L (1998) A third-generation lentivirus vector with a conditional packaging system. J Virol 72:8463-8471.
20. Duman RS, Malberg J, Nakagawa S (2001) Regulation of adult neurogenesis by psychotropic drugs and stress. J Pharmacol Exp Ther 299:401-407. (Pubitemid 32979649)
21. Dyke HJ, Montana JG (2002) Update on the therapeutic potential of PDE4 inhibitors. Expert Opin Investig Drugs 11:1-13.
22. Egawa T, Mishima K, Matsumoto Y, Iwasaki K, Iwasaki K, Fujiwara M (1997) Rolipram and its optical isomers, phosphodiesterase 4 inhibitors, attenuated the scopolamine-induced impairments of learning and memory in rats. Jpn J Pharmacol 75:275-281.
23. Encinas JM, Vaahtokari A, Enikolopov G (2006) Fluoxetine targets early progenitor cells in the adult brain. Proc Natl Acad Sci U S A 103:8233-8238.
24. Episkopou V (2005) SOX2 functions in adult neural stem cells. Trends Neurosci 28:219-221.
25. Epp JR, Spritzer MD, Galea LA (2007) Hippocampus-dependent learning promotes survival of new neurons in the dentate gyrus at a specific time during cell maturation. Neuroscience 149:273-285.
26. Fujioka T, Fujioka A, Duman RS (2004) Activation of cAMP signaling facilitates the morphological maturation of newborn neurons in adult hippocampus. J Neurosci 24:319-328.
27. Giorgi M, Modica A, Pompili A, Pacitti C, Gasbarri A (2004) The induction of cyclic nucleotide phosphodiesterase 4 gene (PDE4D) impairs memory in a water maze task. Behav Brain Res 154:99-106.
28. Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ (1999) Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 2:260-265. (Pubitemid 30491297)
29. Graham V, Khudyakov J, Ellis P, Pevny L (2003) SOX2 functions to maintain neural progenitor identity. Neuron 39:749-765.
30. Grillo CA, Tamashiro KL, Piroli GG, Melhorn S, Gass JT, Newsom RJ, Reznikov LR, Smith A, Wilson SP, Sakai RR, Reagan LP (2007) Lentivirus-mediated downregulation of hypothalamic insulin receptor expression. Physiol Behav 92:691-701.
31. Hansen G, Jin S, Umetsu DT, Conti M (2000) Absence of muscarinic cholinergic airway responses in mice deficient in the cyclic nucleotide phosphodiesterase PDE4D. Proc Natl Acad Sci U S A 97:6751-6756.
32. Houslay MD (2001) PDE4 cAMP-specific phosphodiesterases. Prog Nucleic Acid Res Mol Biol 69:249-315.
33. Houslay MD (2010) Underpinning compartmentalised cAMP signalling through targeted cAMP breakdown. Trends Biochem Sci 35:91-100.
34. Houslay MD, Baillie GS, Maurice DH (2007) cAMP-Specific phosphodiesterase-4 enzymes in the cardiovascular system: a molecular toolbox for generating compartmentalized cAMP signaling. Circ Res 100:950-966.
35. Huston E, Lumb S, Russell A, Catterall C, Ross AH, Steele MR, Bolger GB, Perry MJ, Owens RJ, Houslay MD (1997) Molecular cloning and transient expression in COS7 cells of a novel human PDE4B cAMP-specific phosphodiesterase, HSPDE4B3. Biochem J 328:549-558.
36. Imanishi T, Sawa A, Ichimaru Y, Miyashiro M, Kato S, Yamamoto T, Ueki S (1997) Ameliorating effects of rolipram on experimentally induced impairments of learning and memory in rodents. Eur J Pharmacol 321:273-278.
37. Jin SL, Richard FJ, Kuo WP, D'Ercole AJ, Conti M (1999) Impaired growth and fertility of cAMP-specific phosphodiesterase PDE4D-deficient mice. Proc Natl Acad Sci U S A 96:11998-12003.
38. Johnston LA, Erdogan S, Cheung YF, Sullivan M, Barber R, Lynch MJ, Baillie GS, Van Heeke G, Adams DR, Huston E, Houslay MD (2004) Expression, intracellular distribution and basis for lack of catalytic activity of the PDE4A7 isoform encoded by the human PDE4A cAMP-specific phosphodiesterase gene. Biochem J 380:371-384.
39. Kempermann G, Gast D, Kronenberg G, Yamaguchi M, Gage FH (2003) Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 130:391-399.
40. Kolosionek E, Savai R, Ghofrani HA, Weissmann N, Guenther A, Grimminger F, Seeger W, Banat GA, Schermuly RT, Pullamsetti SS (2009) Expression and activity of phosphodiesterase isoforms during epithelial mesenchymal transition: the role of phosphodiesterase 4. Mol Biol Cell 20:4751-4765.
41. Li X, Huston E, Lynch MJ, Houslay MD, Baillie GS (2006) Phosphodiesterase-4 influences the PKA phosphorylation status and membrane translocation of G-protein receptor kinase 2 (GRK2) in HEK-293beta2 cells and cardiac myocytes. Biochem J 394:427-435.
42. Li YF, Huang Y, Amsdell SL, Xiao L, O'Donnell JM, Zhang HT (2009) Antidepressant- and anxiolytic-like effects of the phosphodiesterase-4 (PDE4) inhibitor rolipram on behavior depend on cyclic AMP-response element binding protein (CREB)-mediated neurogenesis in the hippocampus. Neuropsychopharmacology 34:2404-2419.
43. Lynch MJ, Baillie GS, Mohamed A, Li X, Maisonneuve C, Klussmann E, van Heeke G, Houslay MD (2005) RNA silencing identifies PDE4D5 as the functionally relevant cAMP phosphodiesterase interacting with beta arrestin to control the protein kinase A/AKAP79-mediated switching of the beta2-adrenergic receptor to activation of ERK in HEK293B2 cells. J Biol Chem 280:33178-33189.
44. Lynex CN, Li Z, Chen ML, Toh KY, Low RW, Goh DL, Tay SK (2008) Identification and molecular characterization of a novel PDE4D11 cAMP-specific phosphodiesterase isoform. Cell Signal 20:2247-2255.
45. MacKenzie SJ, Houslay MD (2000) Action of rolipram on specific PDE4 cAMP phosphodiesterase isoforms and on the phosphorylation of cAMP-response-element- binding protein (CREB) and p38 mitogen-activated protein (MAP) kinase in U937 monocytic cells. Biochem J 347:571-578.
46. Malberg JE, Eisch AJ, Nestler EJ, Duman RS (2000) Chronic antidepressant treatment increases neurogenesis in adult hippocampus. J Neurosci 20:9104-9110.
47. Maurice T, Privat A (1997) SA4503, a novel cognitive enhancer with σ1 receptor agonist properties, facilitates NMDA receptor-dependent learning in mice. Eur J Pharmacol 328:9-18.
48. McPhee I, Cochran S, Houslay MD (2001) The novel long PDE4A10 cyclic AMP phosphodiesterase shows a pattern of expression within brain that is distinct from the long PDE4A5 and short PDE4A1 isoforms. Cell Signal 13:911-918.
49. Millar JK, Pickard BS, Mackie S, James R, Christie S, Buchanan SR, Malloy MP, Chubb JE, Huston E, Baillie GS, Thomson PA, Hill EV, Brandon NJ, Rain JC, Camargo LM, Whiting PJ, Houslay MD, Blackwood DH, Muir WJ, Porteous DJ (2005) DISC1 and PDE4B are interacting genetic factors in schizophrenia that regulate cAMP signaling. Science 310:1187-1191.
50. Miró X, Pérez-Torres S, Puigdomènech P, Palacios JM, Mengod G (2002) Differential distribution of PDE4D splice variant mRNAs in rat brain suggests association with specific pathways and presynaptical localization. Synapse 45:259-269.
51. Monti B, Berteotti C, Contestabile A (2006) Subchronic rolipram delivery activates hippocampal CREB and Arc, enhances retention and slows down extinction of conditioned fear. Neuropsychopharmacology 31:278-286.
52. Morris RG, Garrud P, Rawlins JN, O'Keefe J (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297:681-683.
53. Mullen R, Buck CR, Smith AM (1992) NeuN, a neuronal specific nuclear protein in vertebrates. Development 116:201-211.
54. Nakagawa S, Kim JE, Lee R, Malberg JE, Chen J, Steffen C, Zhang YJ, Nestler EJ, Duman RS (2002a) Regulation of neurogenesis in adult mouse hippocampus by cAMP and the cAMP response element-binding protein. J Neurosci 22:3673-3682. (Pubitemid 37465772)
55. Nakagawa S, Kim JE, Lee R, Chen J, Fujioka T, Malberg J, Tsuji S, Duman RS (2002b) Localization of phosphorylated cAMP response element binding protein in immature neurons of adult hippocampus. J Neurosci 22:9868-9876.
56. Némoz G, Zhang R, Sette C, Conti M (1996) Identification of cyclic AMP-phosphodiesterase variants from the PDE4D gene expressed in human peripheral mononuclear cells. FEBS Lett 384:97-102.
57. O'Donnell JM, Zhang HT (2004) Antidepressant effects of inhibitors of cAMP phosphodiesterase (PDE4). Trends Pharmacol Sci 25:158-163.
58. Otmakhov N, Khibnik L, Otmakhova N, Carpenter S, Riahi S, Asrican B, Lisman J (2004) Forskolin-induced LTP in the CA1 hippocampal region is NMDA receptor dependent. J Neurophysiol 91:1955-1962.
59. Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates. Ed 2. San Diego: Academic.
60. 3H]rolipram binding autoradiography: comparison with monkey and rat brain. J Chem Neuroanat 20:349-374.
61. Remondes M, Schuman EM (2004) Role for a cortical input to hippocampal area CA1 in the consolidation of a long-term memory. Nature 431:699-703.
62. Richter W, Jin SL, Conti M (2005) Splice variants of the cyclic nucleotide phosphodiesterase PDE4D are differentially expressed and regulated in rat tissue. Biochem J 388:803-811.
63. Robichaud A, Savoie C, Stamatiou PB, Tattersall FD, Chan CC (2001) PDE4 inhibitors induce emesis in ferrets via a noradrenergic pathway. Neuropharmacology 40:262-269.
64. Robichaud A, Savoie C, Stamatiou PB, Lachance N, Jolicoeur P, Rasori R, Chan CC (2002a) Assessing the emetic potential of PDE4 inhibitors in rats. Br J Pharmacol 135:113-118.
65. Robichaud A, Stamatiou PB, Jin SL, Lachance N, MacDonald D, Laliberté F, Liu S, Huang Z, Conti M, Chan CC (2002b) Deletion of phosphodiesterase 4D in mice shortens alpha(2)-adrenoceptor-mediated anesthesia, a behavioral correlate of emesis. J Clin Invest 110:1045-1052.
66. Romano A, Delorenzi A, Pedreira ME, Tomsic D, Maldonado H (1996) Acute administration of a permeant analog of cAMP and a phosphodiesterase inhibitor improve long-term habituation in the crab Chasmagnathus. Behav Brain Res 75:119-125.
67. Rutten K, Misner DL, Works M, Blokland A, Novak TJ, Santarelli L, Wallace TL (2008) Enhanced long-term potentiation and impaired learning in phosphodiesterase 4D-knockout (PDE4D) mice. Eur J Neurosci 28:625-632.
68. Sasaki T, Kitagawa K, Omura-Matsuoka E, Todo K, Terasaki Y, Sugiura S, Hatazawa J, Yagita Y, Hori M (2007) The phosphodiesterase inhibitor rolipram promotes survival of newborn hippocampal neurons after ischemia. Stroke 38:1597-1605.
69. Schmidt HD, Duman RS (2007) The role of neurotrophic factors in adult hippocampal neurogenesis, antidepressant treatments and animal models of depressive-like behavior. Behav Pharmacol 18:391-418.
70. Schneider HH (1984) Brain cAMP response to phosphodiesterase inhibitors in rats killed by microwave irradiation or decapitation. Biochem Pharmacol 33:1690-1693.
71. Schratt GM, Tuebing F, Nigh EA, Kane CG, Sabatini ME, Kiebler M, Greenberg ME (2006) A brain-specific microRNA regulates dendritic spine development. Nature 439:283-289.
72. Shors TJ, Miesegaes G, Beylin A, Zhao M, Rydel T, Gould E (2001) Neurogenesis in the adult is involved in the formation of trace memories. Nature 410:372-376.
73. Siuciak JA, McCarthy SA, Chapin DS, Martin AN (2008) Behavioral and neurochemical characterization of mice deficient in the phosphodiesterase-4B (PDE4B) enzyme. Psychopharmacology 197:115-126.
74. Stegmeier F, Hu G, Rickles RJ, Hannon GJ, Elledge SJ (2005) A lentiviral microRNA-based system for single-copy polymerase II-regulated RNA interference in mammalian cells. Proc Natl Acad Sci U S A 102:13212-13217.
75. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH (2002) Functional neurogenesis in the adult hippocampus. Nature 415:1030-1034.
76. Villiger JW, Dunn AJ (1981) Phosphodiesterase inhibitors facilitate memory for passive avoidance conditioning. Behav Neural Biol 31:354-359.
77. Zala D, Bensadoun JC, Pereira de Almeida L, Leavitt BR, Gutekunst CA, Aebischer P, Hayden MR, Déglon N (2004) Long-term lentiviral-mediated expression of ciliary neurotrophic factor in the striatum of Huntington's disease transgenic mice. Exp Neurol 185:26-35.
78. Zentilin L, Giacca M (2004) In vivo transfer and expression of genes coding for short interfering RNAs. Curr Pharm Biotechnol 5:341-347.
79. Zeringue HC, Constantine-Paton M (2004) Post-transcriptional gene silencing in neurons. Curr Opin Neurobiol 14:654-659.
80. Zhang HT (2009) Cyclic AMP-specific phosphodiesterase-4 as a target for the development of antidepressant drugs. Curr Pharm Des 15:1688-1698.
81. Zhang HT, O'Donnell JM (2000) Effects of rolipram on scopolamine-induced impairment of working and reference memory in the radial-arm maze tests in rats. Psychopharmacology 150:311-316.
82. Zhang HT, Crissman AM, Dorairaj NR, Chandler LJ, O'Donnell JM (2000) Inhibition of cyclic AMP phosphodiesterase (PDE4) reverses memory deficits associated with NMDA receptor antagonism. Neuropsychopharmacology 23:198-204.
83. Zhang HT, Huang Y, Jin SL, Frith SA, Suvarna N, Conti M, O'Donnell JM (2002) Antidepressant-like Profile and Reduced Sensitivity to Rolipram in Mice Deficient in the PDE4D Phosphodiesterase Enzyme. Neuropsychopharmacology 27:587-595.
84. Zhang HT, Zhao Y, Huang Y, Dorairaj NR, Chandler LJ, O'Donnell JM (2004) Inhibition of the phosphodiesterase 4 (PDE4) enzyme reverses memory deficits produced by infusion of the MEK inhibitor U0126 into the CA1 subregion of the rat hippocampus. Neuropsychopharmacology 29:1432-1439.
85. Zhang HT, Huang Y, Suvarna NU, Deng C, Crissman AM, Hopper AT, De Vivo M, Rose GM, O'Donnell JM (2005) Effects of the novel PDE4 inhibitors MEM1018 and MEM1091 on memory in the radial-arm maze and inhibitory avoidance tests in rats. Psychopharmacology 179:613-619.
86. Zhang HT, Huang Y, Masood A, Stolinski LR, Li Y, Zhang L, Dlaboga D, Jin SL, Conti M, O'Donnell JM (2008) Anxiogenic-like behavioral phenotype of mice deficient in phosphodiesterase 4B (PDE4B). Neuropsychopharmacology 33:1611-1623.
87. Zufferey R, Dull T, Mandel RJ, Bukovsky A, Quiroz D, Naldini L, Trono D (1998) Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J Virol 72:9873-9880.