Gut–Brain–Skin Axis in Psoriasis: A Review

Guang Chen1,2, Chen Zai-ming1, Xiaoyan Fan2, Yinlong Jin2, Xin Li3,2, Shi-Ren Wu1, Weiwei Ge1, Chen Lv1, Yao-Kun Wang3, Jinguang Chen2
1Department of Dermatology, Taizhou Second People’s Hospital, Taizhou, China
2Department of Basic Medical Sciences, Taizhou University Hospital, Taizhou University, Taizhou, China
3Department of Medicine, Jiamusi University, Jiamusi, China

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WHO 2016. Global report on psoriasis. 1–44. https://www.who.int/about/licensing/%0A(www.who.int/about/licensing/%0Acopyright_form/en/index.html)%00. Accessed 16 Feb 2016.

Cannavò SP, Riso G, Casciaro M, et al. Oxidative stress involvement in psoriasis: a systematic review. Free Radic Res. 2019;53(8):829–40.

Helmick CG, Lee-Han H, Hirsch SC, et al. Prevalence of psoriasis among adults in the US: 2003–2006 and 2009–2010 National Health and Nutrition Examination Surveys. Am J Prev Med. 2014;47(1):37–45.

Boehncke WH, Schön MP. Psoriasis. Lancet. 2015;386:983–94.

Schön MP, Boehncke WH. Psoriasis. N Engl J Med. 2005;352:1899–912.

Nestle FO, Kaplan DH, Barker J. Psoriasis. N Engl J Med. 2009;361:496–509.

Harden JL, Krueger JG, Bowcock AM. The immunogenetics of psoriasis: a comprehensive review. J Autoimmun. 2015;64:66–73.

Schön MP, Erpenbeck L. The interleukin-23/interleukin-17 axis links adaptive and innate immunity in psoriasis. Front Immunol. 2018;9:1323.

Prinz JC. Human leukocyte antigen-class I alleles and the autoreactive T cell response in psoriasis pathogenesis. Front Immunol. 2018;9:954.

Ogawa E, Sato Y, Minagawa A, et al. Pathogenesis of psoriasis and development of treatment. J Dermatol. 2018;45(3):264–72.

Duan Y, Dong Y, Hu H, et al. IL-33 contributes to disease severity in psoriasis-like models of mouse. Cytokine. 2019;119:159–67.

Gangemi S, Merendino RA, Guarneri F, et al. Serum levels of interleukin-18 and s-ICAM-1 in patients affected by psoriasis: preliminary considerations. J Eur Acad Dermatol Venereol. 2003;17(1):42–6.

Karbach S, Croxford AL, Oelze M, et al. Interleukin 17drives vascular inflammation, endothelial dysfunction, and arterial hypertension in psoriasis-like skin disease. Arterioscler Thromb Vasc Biol. 2014;34(12):2658–68.

Limanaqi F, Biagioni F, Gaglione A, et al. A sentinel in the crosstalk between the nervous and immune system: the (immuno)-proteasome. Front Immunol. 2019;10:628.

Skaper SD. Nerve growth factor: a neuroimmune crosstalk mediator for all seasons. Immunology. 2017;151(1):1–15.

Pinho-Ribeiro FA, Verri WA Jr, Chiu IM. Nociceptor sensory neuron-immune interactions in pain and inflammation. Trends Immunol. 2017;38(1):5–19.

Marietta E, Horwath I, Taneja V. Microbiome, immunomodulation, and the neuronal system. Neurotherapeutics. 2018;15(1):23–30.

Dantzer R. Neuroimmune interactions: from the brain to the immune system and vice versa. Physiol Rev. 2018;98(1):477–504.

Strandwitz P. Neurotransmitter modulation by the gut microbiota. Brain Res. 2018;1693(Pt B):128–33.

Codoñer FM, Ramírez-Bosca A, Climent E, et al. Gut microbial composition in patients with psoriasis. Sci Rep. 2018;8(1):3812.

Tan L, Zhao S, Zhu W, et al. The Akkermansia muciniphila is a gut microbiota signature in psoriasis. Exp Dermatol. 2018;27(2):144–9.

Cani PD, de Vos WM. Next-generation beneficial microbes: the case of Akkermansia muciniphila. Front Microbiol. 2017;8:1765.

Shapiro J, Cohen NA, Shalev V, et al. Psoriatic patients have a distinct structural and functional fecal microbiota compared with controls. J Dermatol. 2019;46(7):595–603.

Huang L, Gao R, Yu N, et al. Dysbiosis of gut microbiota was closely associated with psoriasis. Sci China Life Sci. 2019;62(6):807–15.

Hidalgo-Cantabrana C, Gómez J, Delgado S, et al. Gut microbiota dysbiosis in a cohort of patients with psoriasis. Br J Dermatol. 2019;181(6):1287–95.

Ellis SR, Nguyen M, Vaughn AR, et al. The skin and gut microbiome and its role in common dermatologic conditions. Microorganisms. 2019;7(11):E550.

Li J, Lin S, Vanhoutte PM, et al. Akkermansia Muciniphila protects against atherosclerosis by preventing metabolic endotoxemia-induced inflammation in Apoe−/− mice. Circulation. 2016;133:2434–46.

Schneeberger M, Everard A, Gomez-Valades AG, et al. Akkermansia muciniphila inversely correlates with the onset of inflammation, altered adipose tissue metabolism and metabolic disorders during obesity in mice. Sci Rep. 2015;5:16643.

Png CW, Lindén SK, Gilshenan KS, et al. Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria. Am J Gastroenterol. 2010;105:2420–8.

Reunanen J, Kainulainen V, Huuskonen L, et al. Akkermansia muciniphila adheres to enterocytes and strengthens the integrity of the epithelial cell layer. Appl Environ Microbiol. 2015;81:3655–62.

Scher JU, Ubeda C, Artacho A, et al. Decreased bacterial diversity characterizes the altered gut microbiota in patients with psoriatic arthritis, resembling dysbiosis in inflammatory bowel disease. Arthritis Rheumatol. 2015;67(1):128–39.

Fry L, Baker BS. Triggering psoriasis: the role of infections and medications. Clin Dermatol. 2007;25(6):606–15.

O’Neill CA, Monteleone G, McLaughlin JT, et al. The gut–skin axis in health and disease: a paradigm with therapeutic implications. Bioessays. 2016;38:1167–76.

Levkovich T, Poutahidis T, Smillie C, et al. Probiotic bacteria induce a ‘glow of health’. PLoS One. 2013;8:e53867.

Kim HJ, Lee SH, Hong SJ. Antibiotics-induced dysbiosis of intestinal microbiota aggravates atopic dermatitis in mice by altered short-chain fatty acids. Allergy Asthma Immunol Res. 2020;12(1):137–48.

Polkowska-Pruszyńska B, Gerkowicz A, Krasowska D. The gut microbiome alterations in allergic and inflammatory skin diseases—an update. J Eur Acad Dermatol Venereol. 2020;34(3):455–64.

Samuelson DR, Welsh DA, Shellito JE. Regulation of lung immunity and host defense by the intestinal microbiota. Front Microbiol. 2015;6:1085.

Dawson LF, Donahue EH, Cartman ST, et al. The analysis of paracresol production and tolerance in Clostridium difficile 027 and 012 strains. BMC Microbiol. 2011;11:86.

Miyazaki K, Masuoka N, Kano M, et al. Bifidobacterium fermented milk and galacto-oligosaccharides lead to improved skin health by decreasing phenols production by gut microbiota. Benef Microbes. 2014;5:121–8.

Shen T-CD. Diet and gut microbiota in health and disease. Nestle Nutr Inst Workshop Ser. 2017;88:117–26.

Forbes JD, Van Domselaar G, Bernstein CN. The gut microbiota in immune-mediated inflammatory diseases. Front Microbiol. 2016;7:1081.

Kosiewicz MM, Dryden GW, Chhabra A, et al. Relationship between gut microbiota and development of T cell associated disease. FEBS Lett. 2014;588:4195–206.

Szántó M, Dózsa A, Antal D, et al. Targeting the gut–skin axis—probiotics as new tools for skin disorder management? Exp Dermatol. 2019;28(11):1210–8.

Bravo JA, Forsythe P, Chew MV, et al. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci USA. 2011;108:16050–5.

Tolhurst G, Heffron H, Lam YS, et al. Short-chain fatty acids stimulate glucagon like peptide-1 secretion via the G-protein-coupled receptor FFAR2. Diabetes. 2012;61:364–71.

Wang Y, Telesford KM, Ochoa-Reparaz J, et al. An intestinal commensal symbiosis factor controls neuroinflammation via TLR2-mediated CD39 signaling. Nat Commun. 2014;5:4432.

Singh V, Roth S, Llovera G, et al. Microbiota dysbiosis controls the neuroinflammatory response after stroke. J Neurosci. 2016;36:7428–40.

Yano JM, Yu K, Donaldson GP, et al. Indigenous bacteria from the gut microbiota regulate host serotonin biosynthesis. Cell. 2015;161:264–76.

Wikoff WR, Anfora AT, Liu J, et al. Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc Natl Acad Sci USA. 2009;106:3698–703.

Barrett E, Ross RP, O’Toole PW, et al. Gamma-aminobutyric acid production by culturable bacteria from the human intestine. J Appl Microbiol. 2012;113:411–7.

Minuk GY. Gamma-aminobutyric-acid (GABA) production by eight common bacterial pathogens. Scand J Infect Dis. 1986;18:465–7.

Kuley E, Ozogul F, Ozogul Y, et al. The function of lactic acid bacteria and brine solutions on biogenic amine formation by food borne pathogens in trout fillets. Food Chem. 2011;129(3):1211–6.

Shishov VA, Kirovskaya TA, Kudrin VS, et al. Amine neuromediators, their precursors, and oxidation products in the culture of Escherichia coli K-12. Appl Biochem Micro. 2009;45:494–7.

Asano Y, Hiramoto T, Nishino R, et al. Critical role of gut microbiota in the production of biologically active, free catecholamines in the gut lumen of mice. Am J Physiol Gastrointest Liver Physiol. 2012;303:G1288–95.

Bowe W, Patel NB, Logan AC. Acne vulgaris, probiotics and the gut–brain–skin axis: from anecdote to translational medicine. Benef Microbes. 2014;5(2):185–99.

Bowe WP, Logan AC. Acne vulgaris, probiotics and the gut–brain–skin axis—back to the future? Gut Pathog. 2011;3(1):1.

Loney T, Standage M, Lewis S. Not just ‘skin deep’: psychosocial effects of dermatological-related social anxiety in a sample of acne patients. J Health Psychol. 2008;13:47–54.

Dreno B, Bagatin E, Blume-Peytavi U, et al. Female type of adult acne: physiological and psychological considerations and management. J Dtsch Dermatol Ges. 2018;16(10):1185–94.

Mallon E, Newton JN, Klassen A, et al. The quality of life in acne: a comparison with general medical conditions using generic questionnaires. Br J Dermatol. 1999;140:672–6.

Uhlenhake E, Yentzer BA, Feldman SR. Acne vulgaris and depression: a retrospective examination. J Cosmet Dermatol. 2010;9:59–63.

Quatrini L, Vivier E, Ugolini S. Neuroendocrine regulation of innate lymphoid cells. Immunol Rev. 2018;286(1):120–36.

Valles-Colomer M, Falony G, Darzi Y, et al. The neuroactive potential of the human gut microbiota in quality of life and depression. Nat Microbiol. 2019;4(4):623–32.

Eskeland S, Halvorsen JA, Tanum L. Antidepressants have anti-inflammatory effects that may be relevant to dermatology: a systematic review. Acta Derm Venereol. 2017;97(8):897–905.

Baharav E, Bar M, Taler M, et al. Immunomodulatory effect of sertraline in a rat model of rheumatoid arthritis. Neuroimmunomodulation. 2012;19:309–18.

Kubera M, Curzytek K, Majewska-Szczepanik M, et al. Inhibitory effect of antidepressant drugs on contact hypersensitivity reaction. Pharmacol Rep. 2012;64:714–22.

Mandrioli R, Protti M, Mercolini L. New-generation, non-SSRI antidepressants: therapeutic drug monitoring and pharmacological interactions. Part 1: SNRIs, SMSs, SARIs. Curr Med Chem. 2018;25(7):772–92.

Klein MO, Battagello DS, Cardoso AR, et al. Dopamine: functions, signaling, and association with neurological diseases. Cell Mol Neurobiol. 2019;39(1):31–59.

Freestone PP, Williams PH, Haigh RD, et al. Growth stimulation of intestinal commensal Escherichia coli by catecholamines: a possible contributory factor in trauma-induced sepsis. Shock. 2002;18:465–70.

Bansal T, Englert D, Lee J, et al. Differential effects of epinephrine, norepinephrine, and indole on Escherichia coli O157:H7 chemotaxis, colonization, and gene expression. Infect Immun. 2007;75:4597–607.

O’Donnell PM, Aviles H, Lyte M, et al. Enhancement of in vitro growth of pathogenic bacteria by norepinephrine: importance of inoculum density and role of transferrin. Appl Environ Microbiol. 2006;72:5097–9.

Bain KA, Milling S. T cell addiction: can pathogenic T cells be controlled using dopamine receptors? Immunology. 2019;158(3):151–2.

Rousset L, Halioua B. Stress and psoriasis. Int J Dermatol. 2018;57(10):1165–72.

Mori T, Kabashima K, Fukamachi S, et al. D1-like dopamine receptors antagonist inhibits cutaneous immune reaction mediated by Th2 and mast cells. J Dermatol Sci. 2013;71:37–44.

Keren A, Gilhar A, Ullmann Y, et al. Instantaneous depolarization of T cells via dopamine receptors, and inhibition of activated T cells of psoriasis patients and inflamed human skin, by D1-like receptor agonist: fenoldopam. Immunology. 2019;158:171–92.

Parrado AC, Canellada A, Gentile T, et al. Dopamine agonists upregulate IL-6 and IL-8 production in human keratinocytes. Neuroimmunomodulation. 2012;19:359–66.

Wardhana M, Windari M, Puspasari N, et al. Role of serotonin and dopamine in psoriasis: a case-control study. Open Access Maced J Med Sci. 2019;7:1138–42.

Idzko M, Panther E, Stratz C, et al. The serotoninergic receptors of human dendritic cells: identification and coupling to cytokine release. J Immunol. 2004;172(10):6011–9.

Sikander A, Rana SV, Prasad KK. Role of serotonin in gastrointestinal motility and irritable bowel syndrome. Clin Chim Acta. 2009;403(1–2):47–55.

Murphy DL, Andrews AM, Wichems CH, et al. Brain serotonin neurotransmission: an overview and update with an emphasis on serotonin subsystem heterogeneity, multiple receptors, interactions with other neurotransmitter systems, and consequent implications for understanding the actions of serotonergic drugs. J Clin Psychiatry. 1998;59(15):4–12.

Gershon MD, Tack J. The serotonin signaling system: from basic understanding to drug development for functional GI disorders. Gastroenterology. 2007;132:397–414.

Cloëz-Tayarani I, Petit-Bertron A-F, Venters HD, et al. Differential effect of serotonin on cytokine production in lipopolysaccharide-stimulated human peripheral blood mononuclear cells: involvement of 5-hydroxytryptamine 2A receptors. Int Immunol. 2003;15(2):233–40.

Arreola R, Becerril-Villanueva E, Cruz-Fuentes C, et al. Immunomodulatory effects mediated by serotonin. J Immunol Res. 2015;2015:354957.

Ngo DH, Vo TS. An updated review on pharmaceutical properties of gamma-aminobutyric acid. Molecules. 2019;24(15):E2678.

Stagg CJ, Bachtiar V, Johansen-Berg H. The role of GABA in human motor learning. Curr Biol. 2011;21:480–4.

Nuss P. Anxiety disorders and GABA neurotransmission: a disturbance of modulation. Neuropsychiatr Dis Treat. 2015;11:165–75.

Wagner S, Castel M, Gainer H, et al. GABA in the mammalian suprachiasmatic nucleus and its role in diurnal rhythmicity. Nature. 1997;387:598–603.

Gottesmann C. GABA mechanisms and sleep. Neuroscience. 2002;111:231–9.

Plante DT, Jensen JE, Schoerning L, et al. Reduced-aminobutyric acid in occipital and anterior cingulate cortices in primary insomnia: a link to major depressive disorder? Neuropsychopharmacology. 2012;37:1548–57.

Rashmi D, Zanan R, John S, et al. γ-Aminobutyric acid (GABA): biosynthesis, role, commercial production, and application. In: Rahman A, editor., et al., Study in natural products chemistry, vol. 57. 1st ed. Amsterdam: Elsevier; 2018. p. 413–52.

Strandwitz P, Kim KH, Terekhova D, et al. GABA-modulating bacteria of the human gut microbiota. Nat Microbiol. 2019;4(3):396–403.

Kootte RS, Levin E, Salojärvi J, et al. Improvement of insulin sensitivity after lean donor feces in metabolic syndrome is driven by baseline intestinal microbiota composition. Cell Metab. 2017;26:611 e616-619 e616.

Lee NK, Paik HD. Bioconversion using lactic acid bacteria: ginsenosides, GABA, and phenolic compounds. J Microbiol Biotechnol. 2017;27(5):869–77.

Han D, Kim H-Y, Lee H-J, et al. Wound healing activity of gamma-aminobutyric acid (GABA) in rats. J Microbiol Biotechnol. 2007;17:1661–9.

Bajić SS, Đokić J, Dinić M, et al. GABA potentiate the immunoregulatory effects of Lactobacillus brevis BGZLS10-17 via ATG5-dependent autophagy in vitro. Sci Rep. 2020;10(1):1347.

Nigam R, El-Nour H, Amatya B, et al. GABA and GABA(A) receptor expression on immune cells in psoriasis: a pathophysiological role. Arch Dermatol Res. 2010;302(7):507–15.

Di Meglio P, Villanova F, Nestle FO. Psoriasis. Cold Spring Harb Perspect Med. 2014;4(8):a015354.

Wang JW, Kuo CH, Kuo FC, et al. Fecal microbiota transplantation: review and update. J Formos Med Assoc. 2019;118(Suppl 1):S23–31.

Kragsnaes MS, Kjeldsen J, Horn HC, et al. Efficacy and safety of faecal microbiota transplantation in patients with psoriatic arthritis: protocol for a 6-month, double-blind, randomised, placebo-controlled trial. BMJ Open. 2018;8(4):e019231.

Yin G, Li JF, Sun YF, et al. Fecal microbiota transplantation as a novel therapy for severe psoriasis. Zhonghua Nei Ke Za Zhi. 2019;58(10):782–5.