Doxorubicin attenuates Serotonin-Induced Long-Term synaptic facilitation by phosphorylation of p38 mitogen activated protein kinase

Journal of Neuroscience

Volumn 34, Issue 40, 2014, Pages 13289-13300

  Liu, Rong Yu ^a   Zhang, Yili ^a   Coughlin, Brittany L ^a   Cleary, Leonard J ^a   Byrne, John H ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Aplysia; Chemotherapy; ERK; p38 MAPK; Serotonin; Synaptic plasticity

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; DOXORUBICIN; MITOGEN ACTIVATED PROTEIN KINASE P38; SEROTONIN; GYRASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE;

ANIMAL CELL; APLYSIA; ARTICLE; BRAIN ELECTROPHYSIOLOGY; COGNITIVE DEFECT; CONTROLLED STUDY; EMBRYO; FACILITATION; IMMUNOFLUORESCENCE; IMMUNOREACTIVITY; LONG TERM DEPRESSION; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NONHUMAN; PROTEIN PHOSPHORYLATION; RAT; WESTERN BLOTTING; ANIMAL; BRAIN CORTEX; CELL CULTURE; COCULTURE; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; LONG TERM POTENTIATION; METABOLISM; MOTONEURON; PHOSPHORYLATION; PHYSIOLOGY; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SYNAPSE;

ANIMALS; APLYSIA; CELLS, CULTURED; CEREBRAL CORTEX; COCULTURE TECHNIQUES; DOXORUBICIN; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION, ENZYMOLOGIC; LONG-TERM POTENTIATION; LONG-TERM SYNAPTIC DEPRESSION; MOTOR NEURONS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; RATS; SENSORY RECEPTOR CELLS; SEROTONIN; SIGNAL TRANSDUCTION; SYNAPSES; TOPOISOMERASE II INHIBITORS;

EID: 84907494893     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0538-14.2014     Document Type: Article

References (65)

1. Adams JP, Sweatt JD (2002) Molecular psychology: roles for the ERK MAP kinase cascade in memory. Annu Rev Pharmacol Toxicol 42:135-163. CrossRef Medline
2. Ahles TA, Saykin AJ (2007) Candidate mechanisms for chemotherapyinduced cognitive changes. Nat Rev Cancer 7:192-201. CrossRef Medline
3. Alberini CM, Ghirardi M, Metz R, Kandel ER (1994) C/EBP is an immediate-early gene required for the consolidation of long-term facilitation in Aplysia. Cell 76:1099-1114. CrossRef Medline
4. Bartsch D, Ghirardi M, Skehel PA, Karl KA, Herder SP, Chen M, Bailey CH, Kandel ER (1995) Aplysia CREB2 represses long-term facilitation: relief of repression converts transient facilitation into long-term functional and structural change. Cell 83:979-992. CrossRef Medline
5. Bokemeyer D, Lindemann M, Kramer HJ (1998) Regulation of mitogenactivated protein kinase phosphatase-1 in vascular smooth muscle cells. Hypertension 32:661-667. CrossRef Medline
6. Boland B, Kumar A, Lee S, Platt FM, Wegiel J, Yu WH, Nixon RA (2008) Autophagy induction and autophagosome clearance in neurons: relationship to autophagic pathology in Alzheimer’s disease. J Neurosci 28:6926-6937. CrossRef Medline
7. Bolshakov VY, Carboni L, Cobb MH, Siegelbaum SA, Belardetti F (2000) Dual MAP kinase pathways mediate opposing forms of long-term plasticity at CA3-CA1 synapses. Nat Neurosci 3:1107-1112. CrossRef Medline
8. Chin J, Angers A, Cleary LJ, Eskin A, Byrne JH (1999) TGF-beta1 in Aplysia: role in long-term changes in the excitability of sensory neurons and distribution of TbetaR-II-like immunoreactivity. Learn Mem 6:317-330. Medline
9. Chin J, Liu RY, Cleary LJ, Eskin A, Byrne JH (2006) TGF-beta1-induced long-term changes in neuronal excitability in Aplysia sensory neurons depend on MAPK. J Neurophysiol 95:3286-3290. CrossRef Medline
10. Christie LA, Acharya MM, Parihar VK, Nguyen A, Martirosian V, Limoli CL (2012) Impaired cognitive function and hippocampal neurogenesis following cancer chemotherapy. Clin Cancer Res 18:1954-1965. Cross Ref Medline
11. Cleary LJ, Lee WL, Byrne JH (1998) Cellular correlates of long-term sensitization in Aplysia. J Neurosci 18:5988-5998. Medline
12. Coogan AN, O’Leary DM, O’Connor JJ (1999) P42/44 MAP kinase inhibitor PD98059 attenuates multiple forms of synaptic plasticity in rat dentate gyrus in vitro. J Neurophysiol 81:103-110. Medline
13. Dale N, Kandel ER, Schacher S (1987) Serotonin produces long-term changes in the excitability of Aplysia sensory neurons in culture that depend on new protein synthesis.7:2232-2238J Neurosci. Medline
14. Ehrlich I, Klein M, Rumpel S, Malinow R (2007) PSD-95 is required for activity-driven synapse stabilization. Proc Natl Acad Sci U S A 104:4176-4181. CrossRef Medline
15. Elsea CR, Roberts DA, Druker BJ, Wood LJ (2008) Inhibition of p38 MAPK suppresses inflammatory cytokine induction by etoposide, 5-fluorouracil, and doxorubicin without affecting tumoricidal activity. PLoS One 3:e2355. CrossRef Medline
16. Emptage NJ, Carew TJ (1993) Long-term synaptic facilitation in the absence of short-term facilitation in Aplysia neurons. Science 262:253-256. CrossRef Medline
17. English JD, Sweatt JD (1997) A requirement for the mitogen-activated protein kinase cascade in hippocampal long term potentiation. J Biol Chem 272:19103-19106. CrossRef Medline
18. Fioravante D, Smolen PD, Byrne JH (2006) The 5-HT- and FMRFaactivated signaling pathways interact at the level of the Erk MAPK cascade: potential inhibitory constraints on memory formation. Neurosci Lett 396:235-240. CrossRef Medline
19. Fioravante D, Liu RY, Byrne JH (2008) The ubiquitin-proteasome system is necessary for long-term synaptic depression in Aplysia. J Neurosci 28: 10245-10256. CrossRef Medline
20. Fukushima T, Liu RY, Byrne JH (2007) Transforming growth factor-beta2 modulates synaptic efficacy and plasticity and induces phosphorylation of CREB in hippocampal neurons. Hippocampus 17B:5-9. CrossRef Medline
21. Gewirtz DA (1999) A critical evaluation of the mechanisms of action proposed for the antitumor effects of the anthracycline antibiotics adriamycin and daunorubicin. Biochem Pharmacol 57:727-741. CrossRef Medline
22. Ghirardi M, Montarolo PG, Kandel ER (1995) A novel intermediate stage in the transition between short- and long-term facilitation in the sensory to motor neuron synapse of Aplysia. Neuron 14:413-420. CrossRef Medline
23. Guan Z, Giustetto M, Lomvardas S, Kim JH, Miniaci MC, Schwartz JH, Thanos D, Kandel ER (2002) Integration of long-term-memory-related synaptic plasticity involves bidirectional regulation of gene expression and chromatin structure. Cell 111:483-493. CrossRef Medline
24. Guan Z, Kim JH, Lomvardas S, Holick K, Xu S, Kandel ER, Schwartz JH (2003) p38 MAP kinase mediates both short-term and long-term synaptic depression in Aplysia. J Neurosci 23:7317-7325. Medline
25. Guise S, Braguer D, Carles G, Delacourte A, Briand C (2001) Hyperphosphorylation of tau is mediated by ERK activation during anticancer drug induced apoptosis in neuroblastoma cells. J Neurosci Res 63:257-267. CrossRef Medline
26. Hu JY, Glickman L, Wu F, Schacher S (2004) Serotonin regulates the secretion and autocrine action of a neuropeptide to activate MAPK required for long-term facilitation in Aplysia. Neuron 43:373-385. CrossRef Medline
27. Jansen CE, Cooper BA, Dodd MJ, Miaskowski CA (2011) A prospective longitudinal study of chemotherapy-induced cognitive changes in breast cancer patients. Supportive Care Cancer 19:1647-1656. CrossRef
28. Jansen C, Miaskowski C, Dodd M, Dowling G, Kramer J (2005) Potential mechanisms for chemotherapy-induced impairments in cognitive function. Oncol Nurs Forum 32:1151-1163. CrossRef Medline
29. Jeffrey KL, Camps M, Rommel C, Mackay CR (2007) Targeting dualspecificity phosphatases: manipulating MAP kinase signalling and immune responses. Nat Rev Drug Discov 6:391-403. CrossRef Medline
30. Kang YJ, Zhou ZX, Wang GW, Buridi A, Klein JB (2000) Suppression by metallothionein of doxorubicin-induced cardiomyocyte apoptosis through inhibition of p38 mitogen-activated protein kinases. J Biol Chem 275:13690-13698. CrossRef Medline
31. Kanterewicz BI, Urban NN, McMahon DB, Norman ED, Giffen LJ, Favata MF, Scherle PA, Trzskos JM, Barrionuevo G, Klann E (2000) The extracellular signal-regulated kinase cascade is required for NMDA receptorindependent LTP in area CA1 but not area CA3 of the hippocampus. J Neurosci 20:3057-3066. Medline
32. Liang YC, Huang CC, Hsu KS (2008) A role of p38 mitogen-activated protein kinase in adenosine A(1) receptor-mediated synaptic depotentiation in area CA1 of the rat hippocampus. Mol Brain 1:13. CrossRef Medline
33. Liedke PE, Reolon GK, Kilpp B, Brunetto AL, Roesler R, Schwartsmann G (2009) Systemic administration of doxorubicin impairs aversively motivated memory in rats. Pharmacol Biochem Behav 94:239-243. CrossRef Medline
34. Liu RY, Fioravante D, Shah S, Byrne JH (2008) cAMP response elementbinding protein 1 feedback loop is necessary for consolidation of longterm synaptic facilitation in Aplysia. J Neurosci 28:1970-1976. CrossRef Medline
35. Liu RY, Cleary LJ, Byrne JH (2011) The requirement for enhanced CREB1 expression in consolidation of long-term synaptic facilitation and longterm excitability in sensory neurons of Aplysia. J Neurosci 31:6871-6879. CrossRef Medline
36. Liu RY, Zhang Y, Baxter DA, Smolen P, Cleary LJ, Byrne JH (2013) Deficit in long-term synaptic plasticity is rescued by a computationally predicted stimulus protocol. J Neurosci 33:6944-6949. CrossRef Medline
37. Lopes MA, Meisel A, Dirnagl U, Carvalho FD, Bastos Mde L (2008) Doxorubicin induces biphasic neurotoxicity to rat cortical neurons. Neurotoxicology 29:286-293. CrossRef Medline
38. Martin KC, Michael D, Rose JC, Barad M, Casadio A, Zhu H, Kandel ER (1997) MAP kinase translocates into the nucleus of the presynaptic cell and is required for long-term facilitation in Aplysia. Neuron 18:899-912. CrossRef Medline
39. Michael D, Martin KC, Seger R, Ning MM, Baston R, Kandel ER (1998) Repeated pulses of serotonin required for long-term facilitation activate mitogen-activated protein kinase in sensory neurons of Aplysia. Proc Natl Acad Sci U S A 95:1864-1869. CrossRef Medline
40. Minotti G, Menna P, Salvatorelli E, Cairo G, Gianni L (2004) Anthracyclines: molecular advances and pharmacologic developments in antitumor activity and cardiotoxicity. Pharmacol Rev 56:185-229. CrossRef Medline
41. Mohamed HA, Yao W, Fioravante D, Smolen PD, Byrne JH (2005) cAMPresponse elements in Aplysia creb1, creb2, and Ap-uch promoters: implications for feedback loops modulating long term memory. J Biol Chem 280:27035-27043. CrossRef Medline
42. Mozzachiodi R, Byrne JH (2010) More than synaptic plasticity: role of nonsynaptic plasticity in learning and memory. Trends Neurosci 33:17-26. CrossRef Medline
43. Murray HJ, O’Connor JJ (2003) A role for COX-2 and p38 mitogen activated protein kinase in long-term depression in the rat dentate gyrus in vitro. Neuropharmacology 44:374-380. CrossRef Medline
44. Myers JS (2009) Chemotherapy-related cognitive impairment. Clin J Oncol Nurs 13:413-421. CrossRef Medline
45. Niiya M, Niiya K, Shibakura M, Asaumi N, Yoshida C, Shinagawa K, Teshima T, Ishimaru F, Ikeda K, Tanimoto M (2004) Involvement of ERK1/2 and p38 MAP kinase in doxorubicin-induced uPA expression in human RC-K8 lymphoma and NCI-H69 small cell lung carcinoma cells. Oncology 67:310-319. CrossRef Medline
46. Ormond J, Hislop J, Zhao Y, Webb N, Vaillaincourt F, Dyer JR, Ferraro G, Barker P, Martin KC, Sossin WS (2004) ApTrkl, a Trk-like receptor, mediates serotonin- dependent ERK activation and long-term facilitation in Aplysia sensory neurons. Neuron 44:715-728. CrossRef Medline
47. Philips GT, Ye X, Kopec AM, Carew TJ (2013) MAPK establishes a molecular context that defines effective training patterns for long-term memory formation. J Neurosci 33:7565-7573. CrossRef Medline
48. Poizat C, Puri PL, Bai Y, Kedes L (2005) Phosphorylation-dependent degradation of p300 by doxorubicin-activated p38 mitogen-activated protein kinase in cardiac cells. Mol Cell Biol 25:2673-2687. CrossRef Medline
49. Price DM, Wloka MT, Chik CL, Ho AK (2007) Mitogen-activated protein kinase phosphatase-1 (MKP-1) preferentially dephosphorylates p42/ 44MAPK but not p38MAPK in rat pinealocytes. J Neurochem 101:1685-1693. CrossRef Medline
50. Purcell AL, Sharma SK, Bagnall MW, Sutton MA, Carew TJ (2003) Activation of a tyrosine kinase-MAPK cascade enhances the induction of longterm synaptic facilitation and long-term memory in Aplysia. Neuron 37: 473-484. CrossRef Medline
51. Rojo F, González-Navarrete I, Bragado R, Dalmases A, Menéndez S, Cortes Sempere M, Suárez C, Oliva C, Servitja S, Rodriguez-Fanjul V, SánchezPérez I, Campas C, Corominas JM, Tusquets I, Bellosillo B, Serrano S, Perona R, Rovira A, Albanell J (2009) Mitogen-activated protein kinase phosphatase-1 in human breast cancer independently predicts prognosis and is repressed by doxorubicin. Clin Cancer Res 15:3530-3539. CrossRef Medline
52. Rosenkranz JA, Frick A, Johnston D (2009) Kinase-dependent modification of dendritic excitability after long-term potentiation. J Physiol 587:115-125. CrossRef Medline
53. Sardi I, la Marca G, Cardellicchio S, Giunti L, Malvagia S, Genitori L, Massimino M, de Martino M, Giovannini MG (2013) Pharmacological modulation of blood-brain barrier increases permeability of doxorubicin into the rat brain. Am J Cancer Res 3:424-432. Medline
54. Seigers R, Fardell JE (2011) Neurobiological basis of chemotherapyinduced cognitive impairment: a review of rodent research. Neuroscience and biobehavioral reviews 35:729-741. CrossRef Medline
55. Sharma SK, Carew TJ (2004) The roles of MAPK cascades in synaptic plas ticity and memory in Aplysia: facilitatory effects and inhibitory constraints. Learning and memory 11:373-378. CrossRef Medline
56. Sharma SK, Bagnall MW, Sutton MA, Carew TJ (2003a) Inhibition of calcineurin facilitates the induction of memory for sensitization in Aplysia: requirement of mitogen-activated protein kinase. Proc Natl Acad Sci U S A 100:4861-4866. CrossRef Medline
57. Sharma SK, Sherff CM, Shobe J, Bagnall MW, Sutton MA, Carew TJ (2003b) Differential role of mitogen-activated protein kinase in three distinct phases of memory for sensitization in Aplysia. J Neurosci 23:3899-3907. Medline
58. Small GW, Somasundaram S, Moore DT, Shi YY, Orlowski RZ (2003) Repression of mitogen-activated protein kinase (MAPK) phosphatase-1 by anthracyclines contributes to their antiapoptotic activation of p44/42-MAPK. J Pharmacol Exp Ther 307:861-869. CrossRef Medline
59. Stamboulian S, Choi JS, Ahn HS, Chang YW, Tyrrell L, Black JA, Waxman SG, Dib-Hajj SD (2010) ERK1/2 mitogen-activated protein kinase phosphorylates sodium channel Na(v)1.7 and alters its gating properties. J Neurosci 30:1637-1647. CrossRef Medline
60. Sung YJ, Povelones M, Ambron RT (2001) RISK-1: a novel MAPK homologue in axoplasm that is activated and retrogradely transported after nerve injury. J Neurobiol 47:67-79. CrossRef Medline
61. Tsvetkov AS, Arrasate M, Barmada S, Ando DM, Sharma P, Shaby BA, Finkbeiner S (2013) Proteostasis of polyglutamine varies among neurons and predicts neurodegeneration. Nature chemical biology 9:586-592. CrossRef Medline
62. Weatherill DB, Dyer J, Sossin WS (2010) Ribosomal protein S6 kinase is a critical downstream effector of the target of rapamycin complex 1 for long-term facilitation in Aplysia. J Biol Chem 285:12255-12267. CrossRef Medline
63. Wefel JS, Saleeba AK, Buzdar AU, Meyers CA (2010) Acute and late onset cognitive dysfunction associated with chemotherapy in women with breast cancer. Cancer 116:3348-3356. CrossRef Medline
64. Zhang Y, Liu RY, Heberton GA, Smolen P, Baxter DA, Cleary LJ, Byrne JH (2012) Computational design of enhanced learning protocols. Nat Neurosci 15:294-297. CrossRef Medline
65. Zhong P, Liu W, Gu Z, Yan Z (2008) Serotonin facilitates long-term depression induction in prefrontal cortex via p38 MAPK/Rab5-mediated enhancement of AMPA receptor internalization. J Physiol 586:4465-4479. CrossRef Medline