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Current Psychopharmacology

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ISSN (Print): 2211-5560
ISSN (Online): 2211-5579

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Research Article

Cocaine Administration Protects Gut Mucosa Barrier and Reduces Plasma Level of TNF-α

Author(s): Xiaoyu Fu, Chuanxiu Bian, Anna Kruyer, Zejun Zhou, Zhenwu Luo, Azizul Haque, Amanda Wagner, Sylvia Fitting, Catrina Robinson, Aimee McRae-Clark, Davide Amato*, Wei Jiang* and Ren Lang

Volume 11, Issue 2, 2022

Published on: 12 September, 2022

Article ID: e180822207620 Pages: 8

DOI: 10.2174/2211556011666220818091709

Price: $65

Abstract

Background: Cocaine affects not only the central nervous system but also systemic immunity. The role of cocaine in gut mucosal integrity is not fully understood.

Methods: Here we evaluated the effect of cocaine use on gut endothelial permeability and system inflammation in rats that self-administered cocaine or saline and humans using immunohistochemistry, qPCR, ELISA, and Transepithelial/transendothelial electrical resistance (TEER).

Results: Cocaine administration maintained intact and undisturbed intestinal mucosal structures, increased tight junction claudin 1 and 2 mRNA expression, and decreased plasma TNF-α levels, compared to the control group, at the end of the study in rats. Further, cocaine treatment decreased gut endothelial permeability in a dose-dependent manner in human epithelial Caco-2 cells in vitro. Consistently, chronic cocaine users exhibited decreased plasma levels of TNF-α compared with non-drug users in vivo. However, plasma IL-6 levels were similar between cocaine use and control groups both in humans and rats in vivo.

Conclusion: Our results from both human and rat studies in vivo and in vitro suggest that cocaine use may exert a protective effect on the integrity of gut mucosa and suppresses plasma TNF-α levels. This study may provide information on some beneficial effects of cocaine use on gut endothelial cells integrity and systemic inflammation.

Keywords: Cocaine, gut, permeability, systemic, inflammation, tight junction.

[1]
Yamada T, Yamanaka I. Microglial localization of alpha interferon receptor in human brain tissues. Neurosci Lett 1995; 189(2): 73-6.
[http://dx.doi.org/10.1016/0304-3940(95)11452-3] [PMID: 7609922]
[2]
Shimizu F, Nishihara H, Sano Y, et al. Markedly increased IP-10 production by blood brain barrier in neuromyelitis optica. PLoS One 2015; 10(3): e0122000.
[http://dx.doi.org/10.1371/journal.pone.0122000] [PMID: 25811465]
[3]
Zimmermann J, Emrich M, Krauthausen M, et al. IL-17A Promotes granulocyte infiltration, myelin loss, microglia activation, and behavioral deficits during cuprizone induced demyelination. Mol Neurobiol 2018; 55(2): 946-57.
[http://dx.doi.org/10.1007/s12035-016-0368-3] [PMID: 28084589]
[4]
Ahmed SH, Lutjens R, Stap LD, et al. Gene expression evidence for remodeling of lateral hypothalamic circuitry in cocaine addiction. Proc Natl Acad Sci USA 2005; 102(32): 11533-8.
[http://dx.doi.org/10.1073/pnas.0504438102] [PMID: 16076954]
[5]
Piechota M, Korostynski M, Solecki W, et al. The dissection of transcriptional modules regulated by various drugs of abuse in the mouse striatum. Genome Biol 2010; 11(5): R48.
[http://dx.doi.org/10.1186/gb-2010-11-5-r48] [PMID: 20459597]
[6]
Poon HF, Abdullah L, Mullan MA, Mullan MJ, Crawford FC. Cocaine induced oxidative stress precedes cell death in human neuronal progenitor cells. Neurochem Int 2007; 50(1): 69-73.
[http://dx.doi.org/10.1016/j.neuint.2006.06.012] [PMID: 16956698]
[7]
Dalvi P, Wang K, Mermis J, et al. HIV-1/cocaine induced oxidative stress disrupts tight junction protein-1 in human pulmonary microvascular endothelial cells: Role of Ras/ERK1/2 pathway. PLoS One 2014; 9(1): e85246.
[http://dx.doi.org/10.1371/journal.pone.0085246] [PMID: 24409324]
[8]
Chivero ET, Ahmad R, Thangaraj A, et al. Cocaine induces inflammatory gut milieu by compromising the mucosal barrier integrity and altering the gut microbiota colonization. Sci Rep 2019; 9(1): 12187.
[http://dx.doi.org/10.1038/s41598-019-48428-2] [PMID: 31434922]
[9]
Meng J, Sindberg GM, Roy S. Disruption of gut homeostasis by opioids accelerates HIV disease progression. Front Microbiol 2015; 6: 643.
[http://dx.doi.org/10.3389/fmicb.2015.00643] [PMID: 26167159]
[10]
Sindberg GM, Sharma U, Banerjee S, et al. An infectious murine model for studying the systemic effects of opioids on early HIV pathogenesis in the gut. J Neuroimmune Pharmacol 2015; 10(1): 74-87.
[http://dx.doi.org/10.1007/s11481-014-9574-9] [PMID: 25502600]
[11]
Banerjee S, Sindberg G, Wang F, et al. Opioid induced gut microbial disruption and bile dysregulation leads to gut barrier compromise and sustained systemic inflammation. Mucosal Immunol 2016; 9(6): 1418-28.
[http://dx.doi.org/10.1038/mi.2016.9] [PMID: 26906406]
[12]
Liao K, Guo M, Niu F, Yang L, Callen SE, Buch S. Cocaine mediated induction of microglial activation involves the ER stress-TLR2 axis. J Neuroinflammation 2016; 13: 33.
[http://dx.doi.org/10.1186/s12974-016-0501-2] [PMID: 26860188]
[13]
Fonseca AC, Matias D, Garcia C, et al. The impact of microglial activation on blood brain barrier in brain diseases. Front Cell Neurosci 2014; 8: 362.
[http://dx.doi.org/10.3389/fncel.2014.00362] [PMID: 25404894]
[14]
Hong S, Banks WA. Role of the immune system in HIV associated neuroinflammation and neurocognitive implications. Brain Behav Immun 2015; 45: 1-12.
[http://dx.doi.org/10.1016/j.bbi.2014.10.008] [PMID: 25449672]
[15]
Halpern JH, Sholar MB, Glowacki J, Mello NK, Mendelson JH, Siegel AJ. Diminished interleukin-6 response to proinflammatory challenge in men and women after intravenous cocaine administration. J Clin Endocrinol Metab 2003; 88(3): 1188-93.
[http://dx.doi.org/10.1210/jc.2002-020804] [PMID: 12629105]
[16]
Kubera M, Filip M, Basta Kaim A, et al. The effect of cocaine sensitization on mouse immunoreactivity. Eur J Pharmacol 2004; 483(2-3): 309-15.
[http://dx.doi.org/10.1016/j.ejphar.2003.10.021] [PMID: 14729122]
[17]
Yao H, Duan M, Buch S. Cocaine mediated induction of platelet-derived growth factor: Implication for increased vascular permeability. Blood 2011; 117(8): 2538-47.
[http://dx.doi.org/10.1182/blood-2010-10-313593] [PMID: 21148086]
[18]
Zihni C, Mills C, Matter K, Balda MS. Tight junctions: From simple barriers to multifunctional molecular gates. Nat Rev Mol Cell Biol 2016; 17(9): 564-80.
[http://dx.doi.org/10.1038/nrm.2016.80] [PMID: 27353478]
[19]
Scorza C, Piccini C, Martínez BM, Abin JA, Zunino P. Alterations in the gut microbiota of rats chronically exposed to volatilized cocaine and its active adulterants caffeine and phenacetin. Neurotox Res 2019; 35(1): 111-21.
[http://dx.doi.org/10.1007/s12640-018-9936-9] [PMID: 30066173]
[20]
Volpe GE, Ward H, Mwamburi M, et al. Associations of cocaine use and HIV infection with the intestinal microbiota, microbial translocation, and inflammation. J Stud Alcohol Drugs 2014; 75(2): 347-57.
[http://dx.doi.org/10.15288/jsad.2014.75.347] [PMID: 24650829]
[21]
Chabot S, Wagner JS, Farrant S, Neutra MR. TLRs regulate the gatekeeping functions of the intestinal follicle associated epithelium. J Immunol 2006; 176(7): 4275-83.
[http://dx.doi.org/10.4049/jimmunol.176.7.4275] [PMID: 16547265]
[22]
Kruyer A, Ball LE, Townsend DM, Kalivas PW, Uys JD. Post translational S-glutathionylation of cofilin increases actin cycling during cocaine seeking. PLoS One 2019; 14(9): e0223037.
[http://dx.doi.org/10.1371/journal.pone.0223037] [PMID: 31550273]
[23]
Knackstedt LA, Melendez RI, Kalivas PW. Ceftriaxone restores glutamate homeostasis and prevents relapse to cocaine seeking. Biol Psychiatry 2010; 67(1): 81-4.
[http://dx.doi.org/10.1016/j.biopsych.2009.07.018] [PMID: 19717140]
[24]
Fu X, Cheng D, Luo Z, et al. Oral enrichment of streptococcus and its role in systemic inflammation related to monocyte activation in humans with cocaine use disorder. J Neuroimmune Pharmacol 2022; 17(1-2): 305-17.
[http://dx.doi.org/10.1007/s11481-021-10007-6] [PMID: 34448131]
[25]
Luo Z, Fitting S, Robinson C, et al. Chronic cannabis smoking-enriched oral pathobiont drives behavioral changes, macrophage infiltration, and increases β-amyloid protein production in the brain. EBioMedicine 2021; 74: 103701.
[http://dx.doi.org/10.1016/j.ebiom.2021.103701] [PMID: 34826801]
[26]
Robinson SM, Sobell LC, Sobell MB, Leo GI. Reliability of the timeline followback for cocaine, cannabis, and cigarette use. Psychol Addict Behav 2014; 28(1): 154-62.
[http://dx.doi.org/10.1037/a0030992] [PMID: 23276315]
[27]
Zhou Z, Bian C, Luo Z, et al. Progesterone decreases gut permeability through upregulating occludin expression in primary human gut tissues and Caco-2 cells. Sci Rep 2019; 9(1): 8367.
[http://dx.doi.org/10.1038/s41598-019-44448-0] [PMID: 31182728]
[28]
Lee K, Vuong HE, Nusbaum DJ, Hsiao EY, Evans CJ, Taylor AMW. The gut microbiota mediates reward and sensory responses associated with regimen-selective morphine dependence. Neuropsychopharmacology 2018; 43(13): 2606-14.
[http://dx.doi.org/10.1038/s41386-018-0211-9] [PMID: 30258112]
[29]
Kang M, Mischel RA, Bhave S, et al. The effect of gut microbiome on tolerance to morphine mediated antinociception in mice. Sci Rep 2017; 7: 42658.
[http://dx.doi.org/10.1038/srep42658] [PMID: 28211545]
[30]
Bauman BD, Meng J, Zhang L, et al. Enteric glial mediated enhancement of intestinal barrier integrity is compromised by morphine. J Surg Res 2017; 219: 214-21.
[http://dx.doi.org/10.1016/j.jss.2017.05.099] [PMID: 29078884]
[31]
Barlass U, Dutta R, Cheema H, et al. Morphine worsens the severity and prevents pancreatic regeneration in mouse models of acute pancreatitis. Gut 2018; 67(4): 600-2.
[PMID: 28642332]
[32]
Kiraly DD, Walker DM, Calipari ES, et al. Alterations of the host microbiome affect behavioral responses to cocaine. Sci Rep 2016; 6: 35455.
[http://dx.doi.org/10.1038/srep35455] [PMID: 27752130]
[33]
Anda T, Yamashita H, Khalid H, et al. Effect of tumor necrosis factor-alpha on the permeability of bovine brain microvessel endothelial cell monolayers. Neurol Res 1997; 19(4): 369-76.
[http://dx.doi.org/10.1080/01616412.1997.11758599] [PMID: 9263215]
[34]
Al-Sadi R, Guo S, Ye D, Rawat M, Ma TY. TNF-α Modulation of intestinal tight junction permeability is mediated by NIK/IKK-α axis activation of the canonical NF-κB pathway. Am J Pathol 2016; 186(5): 1151-65.
[http://dx.doi.org/10.1016/j.ajpath.2015.12.016] [PMID: 26948423]
[35]
Marchiando AM, Shen L, Graham WV, et al. Caveolin-1-dependent occludin endocytosis is required for TNF induced tight junction regulation in vivo. J Cell Biol 2010; 189(1): 111-26.
[http://dx.doi.org/10.1083/jcb.200902153] [PMID: 20351069]
[36]
Pastorelli L, De Salvo C, Mercado JR, Vecchi M, Pizarro TT. Central role of the gut epithelial barrier in the pathogenesis of chronic intestinal inflammation: Lessons learned from animal models and human genetics. Front Immunol 2013; 4: 280.
[http://dx.doi.org/10.3389/fimmu.2013.00280] [PMID: 24062746]
[37]
Schulzke JD, Ploeger S, Amasheh M, et al. Epithelial tight junctions in intestinal inflammation. Ann N Y Acad Sci 2009; 1165: 294-300.
[http://dx.doi.org/10.1111/j.1749-6632.2009.04062.x] [PMID: 19538319]
[38]
Yao H, Yang Y, Kim KJ, et al. Molecular mechanisms involving sigma receptor-mediated induction of MCP-1: Implication for increased monocyte transmigration. Blood 2010; 115(23): 4951-62.
[http://dx.doi.org/10.1182/blood-2010-01-266221] [PMID: 20354174]
[39]
Davidson TL, Hargrave SL, Kearns DN, et al. Cocaine impairs serial-feature negative learning and blood brain barrier integrity. Pharmacol Biochem Behav 2018; 170: 56-63.
[http://dx.doi.org/10.1016/j.pbb.2018.05.005] [PMID: 29753886]
[40]
Meckel KR, Kiraly DD. A potential role for the gut microbiome in substance use disorders. Psychopharmacology 2019; 236(5): 1513-30.
[http://dx.doi.org/10.1007/s00213-019-05232-0] [PMID: 30982128]
[41]
Braniste V, Asmakh M, Kowal C, et al. The gut microbiota influences blood brain barrier permeability in mice. Sci Transl Med 2014; 6(263): 263ra158.
[http://dx.doi.org/10.1126/scitranslmed.3009759] [PMID: 25411471]

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