Generic placeholder image

Current HIV Research

Author(s): Sangsang Li, Yanfei Li, Bingpeng Deng, Jie Yan* and Yong Wang*

DOI: 10.2174/1570162X17666190924200354

DownloadDownload PDF Flyer Cite As
Identification of the Differentially Expressed Genes Involved in the Synergistic Neurotoxicity of an HIV Protease Inhibitor and Methamphetamine

Page: [290 - 303] Pages: 14

  • * (Excluding Mailing and Handling)

Explore Articles
About Journal
For Authors
For Editors
For Reviewers

Abstract

Background: The abuse of psychostimulants such as methamphetamine (METH) is common in human immunodeficiency virus (HIV)-infected individuals. Acquired immunodeficiency syndrome (AIDS) patients taking METH and antiretroviral drugs could suffer severe neurologic damage and cognitive impairment.

Objective: To reveal the underlying neuropathologic mechanisms of an HIV protease inhibitor (PI) combined with METH, growth-inhibition tests of dopaminergic cells and RNA sequencing were performed.

Methods: A combination of METH and PI caused more growth inhibition of dopaminergic cells than METH alone or a PI alone. Furthermore, we identified differentially expressed gene (DEG) patterns in the METH vs. untreated cells (1161 genes), PI vs. untreated cells (16 genes), METH-PI vs. PI (3959 genes), and METH-PI vs. METH groups (14 genes).

Results: The DEGs in the METH-PI co-treatment group were verified in the brains of a mouse model using quantitative polymerase chain reaction and were involved mostly in the regulatory functions of cell proliferation and inflammation.

Conclusion: Such identification of key regulatory genes could facilitate the study of their neuroprotective potential in the users of METH and PIs.

Keywords: Methamphetamine, HIV protease inhibitor, synergistic neurotoxicity, RNA-seq, differentially expressed gene, AIDS.

Graphical Abstract

[1]
Sanchez AB, Varano GP, de Rozieres CM, et al. Antiretrovirals, methamphetamine, and HIV-1 envelope protein gp120 compromise neuronal energy homeostasis in association with various degrees of synaptic and neuritic damage. Antimicrob Agents Chemother 2015; 60(1): 168-79.
[http://dx.doi.org/10.1128/AAC.01632-15] [PMID: 26482305]
[2]
Lyons A, Pitts M, Grierson J. Methamphetamine use in a nationwide online sample of older Australian HIV-positive and HIV-negative gay men. Drug Alcohol Rev 2013; 32(6): 603-10.
[http://dx.doi.org/10.1111/dar.12072] [PMID: 24219659]
[3]
Halkitis PN, Levy MD, Solomon TM. Temporal relations between methamphetamine use and HIV seroconversion in gay, bisexual, and other men who have sex with men. J Health Psychol 2016; 21(1): 93-9.
[http://dx.doi.org/10.1177/1359105314522675] [PMID: 24578373]
[4]
Hurt CB, Torrone E, Green K, Foust E, Leone P, Hightow-Weidman L. Methamphetamine use among newly diagnosed HIV-positive young men in North Carolina, United States, from 2000 to 2005. PLoS One 2010; 5(6)e11314
[http://dx.doi.org/10.1371/journal.pone.0011314] [PMID: 20593025]
[5]
Gonzales R, Mooney L, Rawson RA. The methamphetamine problem in the United States. Annu Rev Public Health 2010; 31: 385-98.
[http://dx.doi.org/10.1146/annurev.publhealth.012809.103600] [PMID: 20070191]
[6]
Soontornniyomkij V, Kesby JP, Morgan EE, et al. Translational methamphetamine AIDS research center (TMARC) group. Effects of HIV and methamphetamine on brain and behavior: Evidence from human studies and animal models. J Neuroimmune Pharmacol 2016; 11(3): 495-510.
[http://dx.doi.org/10.1007/s11481-016-9699-0] [PMID: 27484318]
[7]
Vivithanaporn P, Asahchop EL, Acharjee S, Baker GB, Power C. HIV protease inhibitors disrupt astrocytic glutamate transporter function and neurobehavioral performance. AIDS 2016; 30(4): 543-52.
[http://dx.doi.org/10.1097/QAD.0000000000000955] [PMID: 26558720]
[8]
Hoefer MM, Sanchez AB, Maung R, et al. Combination of methamphetamine and HIV-1 gp120 causes distinct long-term alterations of behavior, gene expression, and injury in the central nervous system. Exp Neurol 2015; 263: 221-34.
[http://dx.doi.org/10.1016/j.expneurol.2014.09.010] [PMID: 25246228]
[9]
Silverstein PS, Shah A, Weemhoff J, Kumar S, Singh DP, Kumar A. HIV-1 gp120 and drugs of abuse: interactions in the central nervous system. Curr HIV Res 2012; 10(5): 369-83.
[http://dx.doi.org/10.2174/157016212802138724] [PMID: 22591361]
[10]
Nightingale S, Winston A, Letendre S, et al. Controversies in HIV-associated neurocognitive disorders. Lancet Neurol 2014; 13(11): 1139-51.
[http://dx.doi.org/10.1016/S1474-4422(14)70137-1] [PMID: 25316020]
[11]
Brew BJ, Letendre SL. Biomarkers of HIV related central nervous system disease. Int Rev Psychiatry 2008; 20(1): 73-88.
[http://dx.doi.org/10.1080/09540260701878082] [PMID: 18240064]
[12]
Letendre SL, McCutchan JA, Childers ME, et al. HNRC Group. Enhancing antiretroviral therapy for human immunodeficiency virus cognitive disorders. Ann Neurol 2004; 56(3): 416-23.
[http://dx.doi.org/10.1002/ana.20198] [PMID: 15349869]
[13]
Garvey L, Surendrakumar V, Winston A. Low rates of neurocognitive impairment are observed in neuro-asymptomatic HIV-infected subjects on effective antiretroviral therapy. HIV Clin Trials 2011; 12(6): 333-8.
[http://dx.doi.org/10.1310/hct1206-333] [PMID: 22189152]
[14]
Crum-Cianflone NF, Moore DJ, Letendre S, et al. Low prevalence of neurocognitive impairment in early diagnosed and managed HIV-infected persons. Neurology 2013; 80(4): 371-9.
[http://dx.doi.org/10.1212/WNL.0b013e31827f0776] [PMID: 23303852]
[15]
Tozzi V, Balestra P, Bellagamba R, et al. Persistence of neuropsychologic deficits despite long-term highly active antiretroviral therapy in patients with HIV-related neurocognitive impairment: prevalence and risk factors. J Acquir Immune Defic Syndr 2007; 45(2): 174-82.
[http://dx.doi.org/10.1097/QAI.0b013e318042e1ee] [PMID: 17356465]
[16]
Giancola ML, Lorenzini P, Balestra P, et al. Neuroactive antiretroviral drugs do not influence neurocognitive performance in less advanced HIV-infected patients responding to highly active antiretroviral therapy. J Acquir Immune Defic Syndr 2006; 41(3): 332-7.
[http://dx.doi.org/10.1097/01.qai.0000197077.64021.07] [PMID: 16540934]
[17]
Dougherty RH, Skolasky RL Jr, McArthur JC. Progression of HIV-associated dementia treated with HAART. AIDS Read 2002; 12(2): 69-74.
[PMID: 11905143]
[18]
Rippeth JD, Heaton RK, Carey CL, et al. HNRC Group. Methamphetamine dependence increases risk of neuropsychological impairment in HIV infected persons. J Int Neuropsychol Soc 2004; 10(1): 1-14.
[http://dx.doi.org/10.1017/S1355617704101021] [PMID: 14751002]
[19]
Jernigan TL, Gamst AC, Archibald SL, et al. Effects of methamphetamine dependence and HIV infection on cerebral morphology. Am J Psychiatry 2005; 162(8): 1461-72.
[http://dx.doi.org/10.1176/appi.ajp.162.8.1461] [PMID: 16055767]
[20]
Blackstone K, Iudicello JE, Morgan EE, et al. Translational methamphetamine aids research center group. Human immunodeficiency virus infection heightens concurrent risk of functional dependence in persons with long-term methamphetamine use. J Addict Med 2013; 7(4): 255-63.
[http://dx.doi.org/10.1097/ADM.0b013e318293653d] [PMID: 23648641]
[21]
Kesby JP, Heaton RK, Young JW, et al. Methamphetamine exposure combined with HIV-1 disease or gp120 expression: Comparison of learning and executive functions in humans and mice. Neuropsychopharmacology 2015; 40(8): 1899-909.
[http://dx.doi.org/10.1038/npp.2015.39] [PMID: 25652249]
[22]
Moore DJ, Blackstone K, Woods SP, et al. Hnrc Group And The Tmarc Group. Methamphetamine use and neuropsychiatric factors are associated with antiretroviral non-adherence. AIDS Care 2012; 24(12): 1504-13.
[http://dx.doi.org/10.1080/09540121.2012.672718] [PMID: 22530794]
[23]
UNAIDS. UNAIDS report on the global AIDS epidemic 2013. Geneva, Switzerland: UNAIDS 2013.
[24]
Bhaskaran K, Mussini C, Antinori A, et al. CASCADE Collaboration. Changes in the incidence and predictors of human immunodeficiency virus-associated dementia in the era of highly active antiretroviral therapy. Ann Neurol 2008; 63(2): 213-21.
[http://dx.doi.org/10.1002/ana.21225] [PMID: 17894380]
[25]
Mediouni S, Marcondes MC, Miller C, McLaughlin JP, Valente ST. The cross-talk of HIV-1 Tat and methamphetamine in HIV-associated neurocognitive disorders. Front Microbiol 2015; 6: 1164.
[http://dx.doi.org/10.3389/fmicb.2015.01164] [PMID: 26557111]
[26]
Robertson K, Liner J, Meeker RB. Antiretroviral neurotoxicity. J Neurovirol 2012; 18(5): 388-99.
[http://dx.doi.org/10.1007/s13365-012-0120-3] [PMID: 22811264]
[27]
Robertson KR, Su Z, Margolis DM, et al. A5170 Study Team. Neurocognitive effects of treatment interruption in stable HIV-positive patients in an observational cohort. Neurology 2010; 74(16): 1260-6.
[http://dx.doi.org/10.1212/WNL.0b013e3181d9ed09] [PMID: 20237308]
[28]
Latronico T, Pati I, Ciavarella R, et al. In vitro effect of antiretroviral drugs on cultured primary astrocytes: analysis of neurotoxicity and matrix metalloproteinase inhibition. J Neurochem 2018; 144(3): 271-84.
[http://dx.doi.org/10.1111/jnc.14269] [PMID: 29210076]
[29]
Stern AL, Lee RN, Panvelker N, et al. Differential effects of antiretroviral drugs on neurons In Vitro: Roles for oxidative stress and integrated stress response. J Neuroimmune Pharmacol 2018; 13(1): 64-76.
[http://dx.doi.org/10.1007/s11481-017-9761-6] [PMID: 28861811]
[30]
Abers MS, Shandera WX, Kass JS. Neurological and psychiatric adverse effects of antiretroviral drugs. CNS Drugs 2014; 28(2): 131-45.
[http://dx.doi.org/10.1007/s40263-013-0132-4] [PMID: 24362768]
[31]
Akay C, Cooper M, Odeleye A, et al. Antiretroviral drugs induce oxidative stress and neuronal damage in the central nervous system. J Neurovirol 2014; 20(1): 39-53.
[http://dx.doi.org/10.1007/s13365-013-0227-1] [PMID: 24420448]
[32]
Gannon PJ, Akay-Espinoza C, Yee AC, et al. HIV protease inhibitors alter amyloid precursor protein processing via β-site amyloid precursor protein cleaving enzyme-1 translational up-regulation. Am J Pathol 2017; 187(1): 91-109.
[http://dx.doi.org/10.1016/j.ajpath.2016.09.006] [PMID: 27993242]
[33]
(FDA) FaDA. Updated guidelines for the use of antiretroviral agents in HIV-1-infected adults and adolescents available food and drug administration. FDA 2009.
[34]
van Griensven J, Diro E, Lopez-Velez R, et al. HIV-1 protease inhibitors for treatment of visceral leishmaniasis in HIV-co-infected individuals. Lancet Infect Dis 2013; 13(3): 251-9.
[http://dx.doi.org/10.1016/S1473-3099(12)70348-1] [PMID: 23427890]
[35]
James CW, McNelis KC, Matalia MD, Cohen DM, Szabo S. Central nervous system toxicity and amprenavir oral solution. Ann Pharmacother 2002; 36(1): 174.
[http://dx.doi.org/10.1345/aph.1A251] [PMID: 11816252]
[36]
Pettersen JA, Jones G, Worthington C, et al. Sensory neuropathy in human immunodeficiency virus/acquired immunodeficiency syndrome patients: Protease inhibitor-mediated neurotoxicity. Ann Neurol 2006; 59(5): 816-24.
[http://dx.doi.org/10.1002/ana.20816] [PMID: 16634006]
[37]
Kapadia F, Vlahov D, Donahoe RM, Friedland G. The role of substance abuse in HIV disease progression: Reconciling differences from laboratory and epidemiologic investigations. Clin Infect Dis 2005; 41(7): 1027-34.
[http://dx.doi.org/10.1086/433175] [PMID: 16142670]
[38]
Sanchez AB, Kaul M. Neuronal stress and injury caused by HIV-1, cART and drug abuse: Converging contributions to HAND. Brain Sci 2017; 7(3)E25
[http://dx.doi.org/10.3390/brainsci7030025] [PMID: 28241493]
[39]
Urbina A, Jones K. Crystal methamphetamine, its analogues, and HIV infection: Medical and psychiatric aspects of a new epidemic. Clin Infect Dis 2004; 38(6): 890-4.
[http://dx.doi.org/10.1086/381975] [PMID: 14999636]
[40]
Ellis RJ, Childers ME, Cherner M, Lazzaretto D, Letendre S, Grant I. HIV Neurobehavioral Research Center Group. Increased human immunodeficiency virus loads in active methamphetamine users are explained by reduced effectiveness of antiretroviral therapy. J Infect Dis 2003; 188(12): 1820-6.
[http://dx.doi.org/10.1086/379894] [PMID: 14673760]
[41]
Parameyong A, Charngkaew K, Govitrapong P, Chetsawang B. Melatonin attenuates methamphetamine-induced disturbances in mitochondrial dynamics and degeneration in neuroblastoma SH-SY5Y cells. J Pineal Res 2013; 55(3): 313-23.
[http://dx.doi.org/10.1111/jpi.12078] [PMID: 23889188]
[42]
Chen C, Qincao L, Xu J, et al. Role of PUMA in methamphetamine-induced neuronal apoptosis. Toxicol Lett 2016; 240(1): 149-60.
[http://dx.doi.org/10.1016/j.toxlet.2015.10.020] [PMID: 26524635]
[43]
Floridia M, Masuelli G, Ravizza M, et al. Italian Group on Surveillance of Antiretroviral Treatment in Pregnancy. Atazanavir and darunavir in pregnant women with HIV: Evaluation of laboratory and clinical outcomes from an observational national study. J Antimicrob Chemother 2018; 73(4): 1025-30.
[http://dx.doi.org/10.1093/jac/dkx478] [PMID: 29244115]
[44]
Zha W, Liang G, Xiao J, et al. Berberine inhibits HIV protease inhibitor-induced inflammatory response by modulating ER stress signaling pathways in murine macrophages. PLoS One 2010; 5(2)e9069
[http://dx.doi.org/10.1371/journal.pone.0009069] [PMID: 20161729]
[45]
Yang X, Wang Y, Li Q, et al. The Main Molecular Mechanisms Underlying Methamphetamine- Induced Neurotoxicity and Implications for Pharmacological Treatment. Front Mol Neurosci 2018; 11: 186.
[http://dx.doi.org/10.3389/fnmol.2018.00186] [PMID: 29915529]
[46]
McConnell SE, O’Banion MK, Cory-Slechta DA, Olschowka JA, Opanashuk LA. Characterization of binge-dosed methamphetamine-induced neurotoxicity and neuroinflammation. Neurotoxicology 2015; 50: 131-41.
[http://dx.doi.org/10.1016/j.neuro.2015.08.006] [PMID: 26283213]
[47]
Hruz PW, Yan Q, Struthers H, Jay PY. HIV protease inhibitors that block GLUT4 precipitate acute, decompensated heart failure in a mouse model of dilated cardiomyopathy. FASEB J 2008; 22(7): 2161-7.
[http://dx.doi.org/10.1096/fj.07-102269] [PMID: 18256305]
[48]
Xu D, Liu A, Wang X, et al. Identifying suitable reference genes for developing and injured mouse CNS tissues. Dev Neurobiol 2018; 78(1): 39-50.
[http://dx.doi.org/10.1002/dneu.22558] [PMID: 29134774]
[49]
Best BM, Letendre SL, Brigid E, et al. CHARTER Group. Low atazanavir concentrations in cerebrospinal fluid. AIDS 2009; 23(1): 83-7.
[http://dx.doi.org/10.1097/QAD.0b013e328317a702] [PMID: 19050389]
[50]
Deng X, Cai NS, McCoy MT, Chen W, Trush MA, Cadet JL. Methamphetamine induces apoptosis in an immortalized rat striatal cell line by activating the mitochondrial cell death pathway. Neuropharmacology 2002; 42(6): 837-45.
[http://dx.doi.org/10.1016/S0028-3908(02)00034-5] [PMID: 12015210]
[51]
Jayanthi S, Deng X, Ladenheim B, et al. Calcineurin/NFAT-induced up-regulation of the Fas ligand/Fas death pathway is involved in methamphetamine-induced neuronal apoptosis. Proc Natl Acad Sci USA 2005; 102(3): 868-73.
[http://dx.doi.org/10.1073/pnas.0404990102] [PMID: 15644446]
[52]
Thiriet N, Deng X, Solinas M, et al. Neuropeptide Y protects against methamphetamine-induced neuronal apoptosis in the mouse striatum. J Neurosci 2005; 25(22): 5273-9.
[http://dx.doi.org/10.1523/JNEUROSCI.4893-04.2005] [PMID: 15930374]
[53]
Cadet JL, Jayanthi S, Deng X. Methamphetamine-induced neuronal apoptosis involves the activation of multiple death pathways. Review Neurotox Res 2005; 8(3-4): 199-206.
[http://dx.doi.org/10.1007/BF03033973] [PMID: 16371314]
[54]
Maruoka H, Sasaya H, Shimamura Y, Nakatani Y, Shimoke K, Ikeuchi T. Dibutyryl-cAMP up-regulates nur77 expression via histone modification during neurite outgrowth in PC12 cells. J Biochem 2010; 148(1): 93-101.
[http://dx.doi.org/10.1093/jb/mvq036] [PMID: 20375114]
[55]
Moll UM, Marchenko N, Zhang XK. p53 and Nur77/TR3 - transcription factors that directly target mitochondria for cell death induction. Oncogene 2006; 25(34): 4725-43.
[http://dx.doi.org/10.1038/sj.onc.1209601] [PMID: 16892086]
[56]
Pearen MA, Muscat GE. Minireview: Nuclear hormone receptor 4A signaling: implications for metabolic disease. Mol Endocrinol 2010; 24(10): 1891-903.
[http://dx.doi.org/10.1210/me.2010-0015] [PMID: 20392876]
[57]
Park KC, Song KH, Chung HK, et al. CR6-interacting factor 1 interacts with orphan nuclear receptor Nur77 and inhibits its transactivation. Mol Endocrinol 2005; 19(1): 12-24.
[http://dx.doi.org/10.1210/me.2004-0107] [PMID: 15459248]
[58]
Yang Y, Xie F, Qin D, et al. The orphan nuclear receptor NR4A1 attenuates oxidative stress-induced β cells apoptosis via up-regulation of glutathione peroxidase 1. Life Sci 2018; 203: 225-32.
[http://dx.doi.org/10.1016/j.lfs.2018.04.027] [PMID: 29678743]
[59]
Kuang AA, Cado D, Winoto A. Nur77 transcription activity correlates with its apoptotic function in vivo. Eur J Immunol 1999; 29(11): 3722-8.
[http://dx.doi.org/10.1002/(SICI)1521-4141(199911)29:11<3722:AID-IMMU3722>3.0.CO;2-N] [PMID: 10556828]
[60]
Zhang XK. Targeting Nur77 translocation. Expert Opin Ther Targets 2007; 11(1): 69-79.
[http://dx.doi.org/10.1517/14728222.11.1.69] [PMID: 17150035]
[61]
To SK, Zeng JZ, Wong AS. Nur77: A potential therapeutic target in cancer. Expert Opin Ther Targets 2012; 16(6): 573-85.
[http://dx.doi.org/10.1517/14728222.2012.680958] [PMID: 22537097]
[62]
Lévesque D, Rouillard C. Nur77 and retinoid X receptors: crucial factors in dopamine-related neuroadaptation. Trends Neurosci 2007; 30(1): 22-30.
[http://dx.doi.org/10.1016/j.tins.2006.11.006] [PMID: 17134767]
[63]
Tsai SY, Catts VS, Fullerton JM, Corley SM, Fillman SG, Weickert CS. Nuclear receptors and neuroinflammation in Schizophrenia. Mol Neuropsychiatry 2018; 3(4): 181-91.
[http://dx.doi.org/10.1159/000485565] [PMID: 29888229]
[64]
Bonta PI, van Tiel CM, Vos M, et al. Nuclear receptors Nur77, Nurr1, and NOR-1 expressed in atherosclerotic lesion macrophages reduce lipid loading and inflammatory responses. Arterioscler Thromb Vasc Biol 2006; 26(10): 2288-94.
[http://dx.doi.org/10.1161/01.ATV.0000238346.84458.5d] [PMID: 16873729]
[65]
Li L, Liu Y, Chen HZ, et al. Impeding the interaction between Nur77 and p38 reduces LPS-induced inflammation. Nat Chem Biol 2015; 11(5): 339-46.
[http://dx.doi.org/10.1038/nchembio.1788] [PMID: 25822914]
[66]
Cui P, Wu S, Xu X, et al. Deficiency of the transcription factor NR4A1 enhances bacterial clearance and prevents lung injury during escherichia coli pneumonia. Shock 2019; 51(6): 787-94.
[http://dx.doi.org/10.1097/SHK.0000000000001184] [PMID: 29846361]
[67]
Rouillard C, Baillargeon J, Paquet B, et al. Genetic disruption of the nuclear receptor Nur77 (Nr4a1) in rat reduces dopamine cell loss and l-Dopa-induced dyskinesia in experimental Parkinson’s disease. Exp Neurol 2018; 304: 143-53.
[http://dx.doi.org/10.1016/j.expneurol.2018.03.008] [PMID: 29530712]
[68]
Kim Y, Ryu J, Ryu MS, et al. C-reactive protein induces G2/M phase cell cycle arrest and apoptosis in monocytes through the upregulation of B-cell translocation gene 2 expression. FEBS Lett 2014; 588(4): 625-31.
[http://dx.doi.org/10.1016/j.febslet.2014.01.008] [PMID: 24440351]
[69]
Hwang SL, Kwon O, Lee SJ, Roh SS, Kim YD, Choi JH. B-cell translocation gene-2 increases hepatic gluconeogenesis via induction of CREB. Biochem Biophys Res Commun 2012; 427(4): 801-5.
[http://dx.doi.org/10.1016/j.bbrc.2012.09.146] [PMID: 23058912]
[70]
Lam BY, Zhang W, Ng DC, Maruthappu M, Roderick HL, Chawla S. CREB-dependent Nur77 induction following depolarization in PC12 cells and neurons is modulated by MEF2 transcription factors. J Neurochem 2010; 112(4): 1065-73.
[http://dx.doi.org/10.1111/j.1471-4159.2009.06521.x] [PMID: 19968756]
[71]
Kim YD, Kim SG, Hwang SL, et al. B-cell translocation gene 2 regulates hepatic glucose homeostasis via induction of orphan nuclear receptor Nur77 in diabetic mouse model. Diabetes 2014; 63(6): 1870-80.
[http://dx.doi.org/10.2337/db13-1368] [PMID: 24647738]
[72]
Butcher GQ, Lee B, Obrietan K. Temporal regulation of light-induced extracellular signal-regulated kinase activation in the suprachiasmatic nucleus. J Neurophysiol 2003; 90(6): 3854-63.
[http://dx.doi.org/10.1152/jn.00524.2003] [PMID: 12930817]
[73]
Misra-Press A, Rim CS, Yao H, Roberson MS, Stork PJ. A novel mitogen-activated protein kinase phosphatase. Structure, expression, and regulation. J Biol Chem 1995; 270(24): 14587-96.
[http://dx.doi.org/10.1074/jbc.270.24.14587] [PMID: 7782322]
[74]
Gorostizaga A, Mori Sequeiros García MM, Acquier A, et al. Modulation of albumin-induced endoplasmic reticulum stress in renal proximal tubule cells by upregulation of mapk phosphatase-1. Chem Biol Interact 2013; 206(1): 47-54.
[http://dx.doi.org/10.1016/j.cbi.2013.08.009] [PMID: 23994741]
[75]
Robitaille AC, Caron E, Zucchini N, et al. DUSP1 regulates apoptosis and cell migration, but not the JIP1-protected cytokine response, during respiratory syncytial virus and sendai virus infection. Sci Rep 2017; 7(1): 17388.
[http://dx.doi.org/10.1038/s41598-017-17689-0] [PMID: 29234123]
[76]
Zhang B, Li SL, Xie HL, et al. Effects of silencing the DUSP1 gene using lentiviral vector-mediated siRNA on the release of proinflammatory cytokines through regulation of the MAPK signaling pathway in mice with acute pancreatitis. Int J Mol Med 2018; 41(4): 2213-24.
[http://dx.doi.org/10.3892/ijmm.2018.3429] [PMID: 29393354]
[77]
Adachi K, Goto M, Onoue T, et al. Mitogen-activated protein kinase phosphatase 1 negatively regulates MAPK signaling in mouse hypothalamus. Neurosci Lett 2014; 569: 49-54.
[http://dx.doi.org/10.1016/j.neulet.2014.03.032] [PMID: 24686178]
[78]
Brion L, Maloberti PM, Gomez NV, et al. MAPK phosphatase-1 (MKP-1) expression is up-regulated by hCG/cAMP and modulates steroidogenesis in MA-10 Leydig cells. Endocrinology 2011; 152(7): 2665-77.
[http://dx.doi.org/10.1210/en.2011-0021] [PMID: 21558315]
[79]
Gómez NV, Gorostizaga AB, Mori Sequeiros García MM, et al. MAPK phosphatase-2 (MKP-2) is induced by hCG and plays a role in the regulation of CYP11A1 expression in MA-10 Leydig cells. Endocrinology 2013; 154(4): 1488-500.
[http://dx.doi.org/10.1210/en.2012-2032] [PMID: 23471219]
[80]
Mori Sequeiros Garcia M, Gorostizaga A, Brion L, González-Calvar SI, Paz C. cAMP-activated Nr4a1 expression requires ERK activity and is modulated by MAPK phosphatase-1 in MA-10 Leydig cells. Mol Cell Endocrinol 2015; 408: 45-52.
[http://dx.doi.org/10.1016/j.mce.2015.01.041] [PMID: 25657047]
[81]
Bliss SP, Navratil AM, Xie J, Miller A, Baccarini M, Roberson MS. ERK signaling, but not c-Raf, is required for gonadotropin-releasing hormone (GnRH)-induced regulation of Nur77 in pituitary gonadotropes. Endocrinology 2012; 153(2): 700-11.
[http://dx.doi.org/10.1210/en.2011-0247] [PMID: 22186412]
[82]
Stocco CO, Lau LF, Gibori G. A calcium/calmodulin-dependent activation of ERK1/2 mediates JunD phosphorylation and induction of nur77 and 20alpha-hsd genes by prostaglandin F2alpha in ovarian cells. J Biol Chem 2002; 277(5): 3293-302.
[http://dx.doi.org/10.1074/jbc.M110936200] [PMID: 11719525]
[83]
Martin LJ, Boucher N, El-Asmar B, Tremblay JJ. cAMP-induced expression of the orphan nuclear receptor Nur77 in MA-10 Leydig cells involves a CaMKI pathway. J Androl 2009; 30(2): 134-45.
[http://dx.doi.org/10.2164/jandrol.108.006387] [PMID: 18835829]
[84]
Kovalovsky D, Refojo D, Liberman AC, et al. Activation and induction of NUR77/NURR1 in corticotrophs by CRH/cAMP: involvement of calcium, protein kinase A, and MAPK pathways. Mol Endocrinol 2002; 16(7): 1638-51.
[http://dx.doi.org/10.1210/mend.16.7.0863] [PMID: 12089357]
[85]
Lin YW, Yang JL. Cooperation of ERK and SCFSkp2 for MKP-1 destruction provides a positive feedback regulation of proliferating signaling. J Biol Chem 2006; 281(2): 915-26.
[http://dx.doi.org/10.1074/jbc.M508720200] [PMID: 16286470]
[86]
He J, Mai J, Li Y, et al. miR-597 inhibits breast cancer cell proliferation, migration and invasion through FOSL2. Oncol Rep 2017; 37(5): 2672-8.
[http://dx.doi.org/10.3892/or.2017.5558] [PMID: 28393251]
[87]
Sun X, Dai G, Yu L, Hu Q, Chen J, Guo W. miR-143-3p inhibits the proliferation, migration and invasion in osteosarcoma by targeting FOSL2. Sci Rep 2018; 8(1): 606.
[http://dx.doi.org/10.1038/s41598-017-18739-3] [PMID: 29330462]
[88]
Ling L, Zhang SH, Zhi LD, et al. MicroRNA-30e promotes hepatocyte proliferation and inhibits apoptosis in cecal ligation and puncture-induced sepsis through the JAK/STAT signaling pathway by binding to FOSL2. Biomed Pharmacother 2018; 104: 411-9.
[http://dx.doi.org/10.1016/j.biopha.2018.05.042] [PMID: 29787988]
[89]
Gupta S, Kumar P, Kaur H, et al. Selective participation of c-Jun with Fra-2/c-Fos promotes aggressive tumor phenotypes and poor prognosis in tongue cancer. Sci Rep 2015; 5: 16811.
[http://dx.doi.org/10.1038/srep16811] [PMID: 26581505]
[90]
Beauvais G, Jayanthi S, McCoy MT, Ladenheim B, Cadet JL. Differential effects of methamphetamine and SCH23390 on the expression of members of IEG families of transcription factors in the rat striatum. Brain Res 2010; 1318: 1-10.
[http://dx.doi.org/10.1016/j.brainres.2009.12.083] [PMID: 20059987]
[91]
Liu Y, Matsumoto RR. Alterations in fos-related antigen 2 and sigma1 receptor gene and protein expression are associated with the development of cocaine-induced behavioral sensitization: time course and regional distribution studies. J Pharmacol Exp Ther 2008; 327(1): 187-95.
[http://dx.doi.org/10.1124/jpet.108.141051] [PMID: 18591217]
[92]
Davies JS, Klein DC, Carter DA. Selective genomic targeting by FRA-2/FOSL2 transcription factor: regulation of the Rgs4 gene is mediated by a variant activator protein 1 (AP-1) promoter sequence/CREB-binding protein (CBP) mechanism. J Biol Chem 2011; 286(17): 15227-39.
[http://dx.doi.org/10.1074/jbc.M110.201996] [PMID: 21367864]
[93]
Flammer JR, Popova KN, Pflum MK. Cyclic AMP response element-binding protein (CREB) and CAAT/enhancer-binding protein beta (C/EBPbeta) bind chimeric DNA sites with high affinity. Biochemistry 2006; 45(31): 9615-23.
[http://dx.doi.org/10.1021/bi052521a] [PMID: 16878996]
[94]
Humphries A, Weller J, Klein D, Baler R, Carter DA. NGFI-B (Nurr77/Nr4a1) orphan nuclear receptor in rat pinealocytes: circadian expression involves an adrenergic-cyclic AMP mechanism. J Neurochem 2004; 91(4): 946-55.
[http://dx.doi.org/10.1111/j.1471-4159.2004.02777.x] [PMID: 15525348]