Modulation of innate immune-related pathways in nicotine-treated SH-SY5Y cells

Amino Acids

Volumn 43, Issue 3, 2012, Pages 1157-1169

  Cui, Wen Yan ^a,b   Wang, Ju ^b   Wei, Jinxue ^b   Cao, Junran ^b   Chang, Sulie L ^c   Gu, Jun ^a   Li, Ming D ^b  

^a PEKING UNIVERSITY   (China)

^b UNIVERSITY OF VIRGINIA   (United States)

^c SETON HALL UNIVERSITY   (United States)

Author keywords

Immune system; Nicotine; SH SY5Y; Signaling

Indexed keywords

DEATH RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; NICOTINE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; TOLL LIKE RECEPTOR;

ARTICLE; BCL 2 GENE; CONTROLLED STUDY; FLIP GENE; GENE; GENE EXPRESSION; GENE IDENTIFICATION; HUMAN; HUMAN CELL; IMMUNOMODULATION; IN VITRO STUDY; INNATE IMMUNITY; MICROARRAY ANALYSIS; NEUROBLASTOMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING;

APOPTOSIS; CELL LINE; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, INNATE; IMMUNOLOGIC FACTORS; MAP KINASE SIGNALING SYSTEM; NEURONS; NF-KAPPA B; NICOTINE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RECEPTORS, DEATH DOMAIN; TOLL-LIKE RECEPTORS; TRANSCRIPTOME;

EID: 84867035327     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-011-1171-0     Document Type: Article

References (76)

1. Allan LA, Morrice N, Brady S, Magee G, Pathak S, Clarke PR (2003) Inhibition of caspase-9 through phosphorylation at Thr 125 by ERK MAPK. Nat Cell Biol 5:647-654 (Pubitemid 36818087)
2. Ashkenazi A, Dixit VM (1998) Death receptors: signaling and modulation. Science 281:1305-1308 (Pubitemid 28406815)
3. Barr J, Sharma CS, Sarkar S, Wise K, Dong L, Periyakaruppan A, Ramesh GT (2007) Nicotine induces oxidative stress and activates nuclear transcription factor kappa B in rat mesencephalic cells. Mol Cell Biochem 297:93-99 (Pubitemid 46443533)
4. Belluardo N, Mudo G, Blum M, Itoh N, Agnati L, Fuxe K (2004) Nicotine-induced FGF-2 mRNA in rat brain is preserved during aging. Neurobiol Aging 25:1333-1342 (Pubitemid 39299171)
5. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289-300
6. Blalock EM, Geddes JW, Chen KC, Porter NM, Markesbery WR, Landfield PW (2004) Incipient Alzheimer's disease: microarray correlation analyses reveal major transcriptional and tumor suppressor responses. Proc Natl Acad Sci USA 101:2173-2178 (Pubitemid 38229034)
7. Blalock EM, Chen KC, Stromberg AJ, Norris CM, Kadish I, Kraner SD, Porter NM, Landfield PW (2005) Harnessing the power of gene microarrays for the study of brain aging and Alzheimer's disease: statistical reliability and functional correlation. Ageing Res Rev 4:481-512 (Pubitemid 43293164)
8. Brunzell DH, Russell DS, Picciotto MR (2003) In vivo nicotine treatment regulates mesocorticolimbic CREB and ERK signaling in C57Bl/6J mice. J Neurochem 84:1431-1441 (Pubitemid 36343609)
9. Cantarella G, Uberti D, Carsana T, Lombardo G, Bernardini R, Memo M (2003) Neutralization of TRAIL death pathway protects human neuronal cell line from beta-amyloid toxicity. Cell Death Differ 10:134-141 (Pubitemid 36511839)
10. Cao J, Dwyer JB, Mangold JE, Wang J, Wei J, Leslie FM, Li MD (2011) Modulation of cell adhesion systems by prenatal nicotine exposure in limbic brain regions of adolescent female rats. Int J Neuropsychopharmacol 14:157-174
11. Casciano I, Banelli B, Croce M, De Ambrosis A, di Vinci A, Gelvi I, Pagnan G, Brignole C, Allemanni G, Ferrini S, Ponzoni M, Romani M (2004) Caspase-8 gene expression in neuroblastoma. Ann N Y Acad Sci 1028:157-167 (Pubitemid 40361820)
12. Chen NJ, Chio II, Lin WJ, Duncan G, Chau H, Katz D, Huang HL, Pike KA, Hao Z, Su YW, Yamamoto K, de Pooter RF, Zuniga- Pflucker JC, Wakeham A, Yeh WC, Mak TW (2008) Beyond tumor necrosis factor receptor: TRADD signaling in toll-like receptors. Proc Natl Acad Sci USA 105:12429-12434
13. Chu ZL, McKinsey TA, Liu L, Gentry JJ, Malim MH, Ballard DW (1997) Suppression of tumor necrosis factor-induced cell death by inhibitor of apoptosis c-IAP2 is under NF-kappaB control. Proc Natl Acad Sci USA 94:10057-10062 (Pubitemid 27406993)
14. Colquhoun D (1987) Molecular neurobiology. A new type of ionchannel block. Nature 329:204-205
15. Dajas-Bailador FA, Soliakov L, Wonnacott S (2002) Nicotine activates the extracellular signal-regulated kinase 1/2 via the alpha7 nicotinic acetylcholine receptor and protein kinase A, in SHSY5Y cells and hippocampal neurones. J Neurochem 80:520-530 (Pubitemid 36383035)
16. Dajas-Bailador FA, Heimala K, Wonnacott S (2003) The allosteric potentiation of nicotinic acetylcholine receptors by galantamine is transduced into cellular responses in neurons: Ca2+ signals and neurotransmitter release. Mol Pharmacol 64:1217-1226 (Pubitemid 37314007)
17. Damaj MI (2000) The involvement of spinal Ca(2+)/calmodulinprotein kinase II in nicotine-induced antinociception in mice. Eur J Pharmacol 404:103-110
18. DC C (2008) Smoking-attributable mortality, years of potential life lost, and productivity losses-United States, 2000-2004. MMWR Morb Mortal Wkly Rep 57:1226-1228
19. del Peso L, Gonzalez-Garcia M, Page C, Herrera R, Nunez G (1997) Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science 278:687-689 (Pubitemid 27464966)
20. Derkach VA, Selyanko AA, Skok VI (1983) Acetylcholine-induced current fluctuations and fast excitatory post-synaptic currents in rabbit sympathetic neurones. J Physiol 336:511-526 (Pubitemid 13153429)
21. Dougherty JD, Garcia AD, Nakano I, Livingstone M, Norris B, Polakiewicz R, Wexler EM, Sofroniew MV, Kornblum HI, Geschwind DH (2005) PBK/TOPK, a proliferating neural progenitor-specific mitogen-activated protein kinase kinase. J Neurosci 25:10773-10785 (Pubitemid 41681926)
22. Dudek H, Datta SR, Franke TF, Birnbaum MJ, Yao R, Cooper GM, Segal RA, Kaplan DR, Greenberg ME (1997) Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science 275:661-665 (Pubitemid 27061332)
23. Dunckley T, Lukas RJ (2003) Nicotine modulates the expression of a diverse set of genes in the neuronal SH-SY5Y cell line. J Biol Chem 278:15633-15640 (Pubitemid 36799673)
24. Ermolaeva MA, Michallet MC, Papadopoulou N, Utermohlen O, Kranidioti K, Kollias G, Tschopp J, Pasparakis M (2008) Function of TRADD in tumor necrosis factor receptor 1 signaling and in TRIF-dependent inflammatory responses. Nat Immunol 9:1037-1046
25. Fenster CP, Beckman ML, Parker JC, Sheffield EB, Whitworth TL, Quick MW, Lester RA (1999) Regulation of alpha4beta2 nicotinic receptor desensitization by calcium and protein kinase C. Mol Pharmacol 55:432-443 (Pubitemid 29128099)
26. Fratiglioni L, Wang HX (2000) Smoking and Parkinson's and Alzheimer's disease: review of the epidemiological studies. Behav Brain Res 113:117-120 (Pubitemid 30645549)
27. Garrido R, Mattson MP, Hennig B, Toborek M (2001) Nicotine protects against arachidonic-acid-induced caspase activation, cytochrome c release and apoptosis of cultured spinal cord neurons. J Neurochem 76:1395-1403 (Pubitemid 32198244)
28. Guan ZZ, Yu WF, Nordberg A (2003) Dual effects of nicotine on oxidative stress and neuroprotection in PC12 cells. Neurochem Int 43:243-249 (Pubitemid 36419525)
29. Hejmadi MV, Dajas-Bailador F, Barns SM, Jones B, Wonnacott S (2003) Neuroprotection by nicotine against hypoxia-induced apoptosis in cortical cultures involves activation of multiple nicotinic acetylcholine receptor subtypes. Mol Cell Neurosci 24:779-786 (Pubitemid 37506019)
30. Hetman M, Gozdz A (2004) Role of extracellular signal regulated kinases 1 and 2 in neuronal survival. Eur J Biochem 271:2050-2055 (Pubitemid 38747973)
31. Imtiyaz HZ, Rosenberg S, Zhang Y, Rahman ZS, Hou YJ, Manser T, Zhang J (2006) The Fas-associated death domain protein is required in apoptosis and TLR-induced proliferative responses in B cells. J Immunol 176:6852-6861 (Pubitemid 43787866)
32. Karin M, Lin A (2002) NF-kappaB at the crossroads of life and death. Nat Immunol 3:221-227
33. Kihara T, Shimohama S, Sawada H, Honda K, Nakamizo T, Shibasaki H, Kume T, Akaike A (2001) Alpha 7 nicotinic receptor transduces signals to phosphatidylinositol 3-kinase to block A beta-amyloid-induced neurotoxicity. J Biol Chem 276:13541-13546
34. Konu O, Xu X, Ma JZ, Kane J, Wang J, Shi SJ, Li MD (2004) Application of a customized pathway-focused microarray for gene expression profiling of cellular homeostasis upon exposure to nicotine in PC12 cells. Brain Res Mol Brain Res 121:102-113 (Pubitemid 38224174)
35. Li MD, Kane JK, Wang J, Ma JZ (2004) Time-dependent changes in transcriptional profiles within five rat brain regions in response to nicotine treatment. Brain Res Mol Brain Res 132:168-180 (Pubitemid 39586759)
36. Lin CH, Yeh SH, Lu KT, Leu TH, Chang WC, Gean PW (2001) A role for the PI-3 kinase signaling pathway in fear conditioning and synaptic plasticity in the amygdala. Neuron 31:841-851
37. Liu ZG, Hsu H, Goeddel DV, Karin M (1996) Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-kappaB activation prevents cell death. Cell 87:565-576 (Pubitemid 26374329)
38. Ma Y, Liu H, Tu-Rapp H, Thiesen HJ, Ibrahim SM, Cole SM, Pope RM (2004) Fas ligation on macrophages enhances IL-1R1-Tolllike receptor 4 signaling and promotes chronic inflammation. Nat Immunol 5:380-387 (Pubitemid 38500086)
39. Ma Y, Li J, Chiu I, Wang Y, Sloane JA, Lu J, Kosaras B, Sidman RL, Volpe JJ, Vartanian T (2006) Toll-like receptor 8 functions as a negative regulator of neurite outgrowth and inducer of neuronal apoptosis. J Cell Biol 175:209-215 (Pubitemid 44631415)
40. Mattson MP, Camandola S (2001) NF-kappaB in neuronal plasticity and neurodegenerative disorders. J Clin Invest 107:247-254 (Pubitemid 32162153)
41. Meffert MK, Baltimore D (2005) Physiological functions for brain NF-kappaB. Trends Neurosci 28:37-43
42. Meffert MK, Chang JM, Wiltgen BJ, Fanselow MS, Baltimore D (2003) NF-kappa B functions in synaptic signaling and behavior. Nat Neurosci 6:1072-1078 (Pubitemid 37186199)
43. Messing RO, Stevens AM, Kiyasu E, Sneade AB (1989) Nicotinic and muscarinic agonists stimulate rapid protein kinase C translocation in PC12 cells. J Neurosci 9:507-512 (Pubitemid 19069495)
44. Mihailescu S, Drucker-Colin R (2000) Nicotine, brain nicotinic receptors, and neuropsychiatric disorders. Arch Med Res 31:131-144 (Pubitemid 30392348)
45. Mokdad AH, Marks JS, Stroup DF, Gerberding JL (2004) Actual causes of death in the United States, 2000. JAMA 291:1238-1245 (Pubitemid 38541668)
46. Monaghan TK, Pou C, MacKenzie CJ, Plevin R, Lutz EM (2008) Neurotrophic actions of PACAP-38 and LIF on human neuroblastoma SH-SY5Y cells. J Mol Neurosci 36:45-56
47. Morens DM, Grandinetti A, Reed D, White LR (1994) Smokingassociated protection from Alzheimer's and Parkinson's disease. Lancet 343:356-357 (Pubitemid 24043194)
48. Nakayama H, Numakawa T, Ikeuchi T, Hatanaka H (2001) Nicotineinduced phosphorylation of extracellular signal-regulated protein kinase and CREB in PC12h cells. J Neurochem 79:489-498 (Pubitemid 33029922)
49. Okuda S, Saito H, Katsuki H (1994) Arachidonic acid: toxic and trophic effects on cultured hippocampal neurons. Neuroscience 63:691-699 (Pubitemid 24360223)
50. Parrish WR, Rosas-Ballina M, Gallowitsch-Puerta M, Ochani M, Ochani K, Yang LH, Hudson L, Lin X, Patel N, Johnson SM, Chavan S, Goldstein RS, Czura CJ, Miller EJ, Al-Abed Y, Tracey KJ, Pavlov VA (2008) Modulation of TNF release by choline requires alpha7 subunit nicotinic acetylcholine receptormediated signaling. Mol Med 14:567-574
51. Picciotto MR, Zoli M (2008) Neuroprotection via nAChRs: the role of nAChRs in neurodegenerative disorders such as Alzheimer's and Parkinson's disease. Front Biosci 13:492-504 (Pubitemid 351599760)
52. Pobezinskaya YL, Kim YS, Choksi S, Morgan MJ, Li T, Liu C, Liu Z (2008) The function of TRADD in signaling through tumor necrosis factor receptor 1 and TRIF-dependent Toll-like receptors. Nat Immunol 9:1047-1054
53. Prehaud C, Megret F, Lafage M, Lafon M (2005) Virus infection switches TLR-3-positive human neurons to become strong producers of beta interferon. J Virol 79:12893-12904 (Pubitemid 41433208)
54. Rezvani AH, Levin ED (2001) Cognitive effects of nicotine. Biol Psychiatry 49:258-267 (Pubitemid 32178435)
55. Ribas J, Gomez-Arbones X, Boix J (2005) Caspase 8/10 are not mediating apoptosis in neuroblastoma cells treated with CDK inhibitory drugs. Eur J Pharmacol 524:49-52 (Pubitemid 41606812)
56. Sanz V, Arozarena I, Crespo P (2000) Distinct carboxy-termini confer divergent characteristics to the mitogen-activated protein kinase p38alpha and its splice isoform Mxi2. FEBS Lett 474:169-174 (Pubitemid 30330828)
57. Serova L, Sabban EL (2002) Involvement of alpha 7 nicotinic acetylcholine receptors in gene expression of dopamine biosynthetic enzymes in rat brain. J Pharmacol Exp Ther 303:896-903 (Pubitemid 35424369)
58. Smith MA (1998) Alzheimer disease. Int Rev Neurobiol 42:1-54
59. Steiner RC, Heath CJ, Picciotto MR (2007) Nicotine-induced phosphorylation of ERK in mouse primary cortical neurons: evidence for involvement of glutamatergic signaling and CaMKII. J Neurochem 103:666-678 (Pubitemid 47498033)
60. Sweatt JD (2004) Mitogen-activated protein kinases in synaptic plasticity and memory. Curr Opin Neurobiol 14:311-317 (Pubitemid 38759861)
61. Tamura K, Sudo T, Senftleben U, Dadak AM, Johnson R, Karin M (2000) Requirement for p38alpha in erythropoietin expression: a role for stress kinases in erythropoiesis. Cell 102:221-231
62. Tang SC, Arumugam TV, Xu X, Cheng A, Mughal MR, Jo DG, Lathia JD, Siler DA, Chigurupati S, Ouyang X, Magnus T, Camandola S, Mattson MP (2007) Pivotal role for neuronal Tolllike receptors in ischemic brain injury and functional deficits. Proc Natl Acad Sci USA 104:13798-13803 (Pubitemid 350003400)
63. Tong HX, Lu CW, Zhang JH, Ma L (2007) Combination of gammainterferon with TRAIL and cisplatin or etoposide induces apoptosis in human neuroblastoma cell line SH-SY5Y. Chin Med Sci J 22:38-43
64. Ulloa L (2005) The vagus nerve and the nicotinic anti-inflammatory pathway. Nat Rev Drug Discov 4:673-684 (Pubitemid 41149761)
65. Van Antwerp DJ, Martin SJ, Kafri T, Green DR, Verma IM (1996) Suppression of TNF-alpha-induced apoptosis by NF-kappaB. Science 274:787-789
66. Wang CY, Mayo MW, Baldwin AS Jr (1996) TNF- and cancer therapy-induced apoptosis: potentiation by inhibition of NFkappaB. Science 274:784-787 (Pubitemid 26398259)
67. Wang CY, Mayo MW, Korneluk RG, Goeddel DV, Baldwin AS Jr (1998) NF-kappaB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science 281:1680-1683
68. Wang H, Yu M, Ochani M, Amella CA, Tanovic M, Susarla S, Li JH, Yang H, Ulloa L, Al-Abed Y, Czura CJ, Tracey KJ (2003) Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 421:384-388 (Pubitemid 36157937)
69. Wang H, Liao H, Ochani M, Justiniani M, Lin X, Yang L, Al-Abed Y, Metz C, Miller EJ, Tracey KJ, Ulloa L (2004) Cholinergic agonists inhibit HMGB1 release and improve survival in experimental sepsis. Nat Med 10:1216-1221 (Pubitemid 39540438)
70. Wang J, Gutala R, Sun D, Ma JZ, Sheela RC, Ticku MK, Li MD (2007) Regulation of platelet-derived growth factor signaling pathway by ethanol, nicotine, or both in mouse cortical neurons. Alcohol Clin Exp Res 31:357-375 (Pubitemid 46239267)
71. Wei J, Wang J, Dwyer JB, Mangold J, Cao J, Leslie FM, Li MD (2011) Gestational nicotine treatment modulates cell death/ survival-related pathways in the brains of adolescent female rats. Int J Neuropsychopharmacol 14:91-106
72. Wilson NS, Dixit V, Ashkenazi A (2009) Death receptor signal transducers: nodes of coordination in immune signaling networks. Nat Immunol 10:348-355
73. Xia Z, Dickens M, Raingeaud J, Davis RJ, Greenberg ME (1995) Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270:1326-1331
74. Yang YH, Dudoit S, Luu P, Lin DM, Peng V, Ngai J, Speed TP (2002) Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res 30:e15
75. Zeidler R, Albermann K, Lang S (2007) Nicotine and apoptosis. Apoptosis 12:1927-1943 (Pubitemid 47498221)
76. Zhou L, Wang X, Wang YJ, Zhou Y, Hu S, Ye L, Hou W, Li H, Ho WZ (2009) Activation of toll-like receptor-3 induces interferonlambda expression in human neuronal cells. Neuroscience 159:629-637