Compositional Alteration of Gut Microbiota in Psoriasis Treated with IL-23 and IL-17 Inhibitors
Abstract
:1. Introduction
2. Results
2.1. Patient Demographic and Characteristics
2.2. Gut Microbial Diversity in Psoriasis after the Treatment with Il-23 and IL-17 Inhibitors
2.3. Altered Composition of Gut Microbiota in Psoriatic Patients after Treatment with IL-23 and IL-17 Inhibitors
2.4. Changes in Relative Abundance of Gut Bacteria between Responders and Non-Responders
2.5. Functional Prediction of Gut Microbiome after Treatment with IL-23 and IL-17 Inhibitors
3. Discussion
4. Material and Methods
4.1. Study Design and Patients
4.2. DNA Isolation and 16S rRNA Gene Sequencing
4.3. Sequencing Data Processing and Species Annotation
4.4. Microbial Gene Function Prediction
4.5. Statistical Analysis
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Griffiths, C.E.M.; Armstrong, A.W.; Gudjonsson, J.E.; Barker, J. Psoriasis. Lancet 2021, 397, 1301–1315. [Google Scholar] [CrossRef] [PubMed]
- Eder, L.; Widdifield, J.; Rosen, C.F.; Cook, R.; Lee, K.A.; Alhusayen, R.; Paterson, M.J.; Cheng, S.Y.; Jabbari, S.; Campbell, W.; et al. Trends in the prevalence and incidence of psoriasis and psoriatic arthritis in Ontario, Canada: A population-based study. Arthritis Care Res. 2019, 71, 1084–1091. [Google Scholar] [CrossRef] [PubMed]
- Parisi, R.; Iskandar, I.Y.K.; Kontopantelis, E.; Augustin, M.; Griffiths, C.E.M.; Ashcroft, D.M.; Global Psoriasis, A. National, regional, and worldwide epidemiology of psoriasis: Systematic analysis and modelling study. BMJ 2020, 369, m1590. [Google Scholar] [CrossRef]
- Capon, F. The genetic basis of psoriasis. Int. J. Mol. Sci. 2017, 18, 2526. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Horton, D.B.; Scott, F.I.; Haynes, K.; Putt, M.E.; Rose, C.D.; Lewis, J.D.; Strom, B.L. Antibiotic exposure, infection, and the development of pediatric psoriasis: A nested case-control study. JAMA Dermatol. 2016, 152, 191–199. [Google Scholar] [CrossRef] [Green Version]
- Chen, Y.J.; Ho, H.J.; Wu, C.Y.; Juan, C.K.; Wu, C.Y. Infantile infection and antibiotic exposure in association with pediatric psoriasis development: A nationwide nested case-control study. J. Am. Acad. Dermatol. 2021, 85, 626–635. [Google Scholar] [CrossRef]
- Alekseyenko, A.V.; Perez-Perez, G.I.; De Souza, A.; Strober, B.; Gao, Z.; Bihan, M.; Li, K.; Methe, B.A.; Blaser, M.J. Community differentiation of the cutaneous microbiota in psoriasis. Microbiome 2013, 1, 31. [Google Scholar] [CrossRef] [Green Version]
- Fahlen, A.; Engstrand, L.; Baker, B.S.; Powles, A.; Fry, L. Comparison of bacterial microbiota in skin biopsies from normal and psoriatic skin. Arch. Dermatol. Res. 2012, 304, 15–22. [Google Scholar] [CrossRef] [PubMed]
- Sikora, M.; Stec, A.; Chrabaszcz, M.; Knot, A.; Waskiel-Burnat, A.; Rakowska, A.; Olszewska, M.; Rudnicka, L. Gut microbiome in psoriasis: An updated review. Pathogens 2020, 9, 463. [Google Scholar] [CrossRef] [PubMed]
- Marietta, E.; Mangalam, A.K.; Taneja, V.; Murray, J.A. Intestinal dysbiosis in, and enteral bacterial therapies for, systemic autoimmune Diseases. Front. Immunol. 2020, 11, 573079. [Google Scholar] [CrossRef]
- Kinashi, Y.; Hase, K. Partners in leaky gut syndrome: Intestinal dysbiosis and autoimmunity. Front. Immunol. 2021, 12, 673708. [Google Scholar] [CrossRef]
- Hidalgo-Cantabrana, C.; Gómez, J.; Delgado, S.; Requena-López, S.; Queiro-Silva, R.; Margolles, A.; Coto, E.; Sánchez, B.; Coto-Segura, P. Gut microbiota dysbiosis in a cohort of patients with psoriasis. Br. J. Dermatol. 2019, 181, 1287–1295. [Google Scholar] [CrossRef]
- Shapiro, J.; Cohen, N.A.; Shalev, V.; Uzan, A.; Koren, O.; Maharshak, N. Psoriatic patients have a distinct structural and functional fecal microbiota compared with controls. J. Dermatol. 2019, 46, 595–603. [Google Scholar] [CrossRef] [PubMed]
- Chen, Y.J.; Ho, H.J.; Tseng, C.H.; Lai, Z.L.; Shieh, J.J.; Wu, C.Y. Intestinal microbiota profiling and predicted metabolic dysregulation in psoriasis patients. Exp. Dermatol. 2018, 27, 1336–1343. [Google Scholar] [CrossRef] [PubMed]
- Huang, L.; Gao, R.; Yu, N.; Zhu, Y.; Ding, Y.; Qin, H. Dysbiosis of gut microbiota was closely associated with psoriasis. Sci. China Life Sci. 2019, 62, 807–815. [Google Scholar] [CrossRef]
- Zanvit, P.; Konkel, J.E.; Jiao, X.; Kasagi, S.; Zhang, D.; Wu, R.; Chia, C.; Ajami, N.J.; Smith, D.P.; Petrosino, J.F.; et al. Antibiotics in neonatal life increase murine susceptibility to experimental psoriasis. Nat. Commun. 2015, 6, 8424. [Google Scholar] [CrossRef] [PubMed]
- Drago, F.; Ciccarese, G.; Indemini, E.; Savarino, V.; Parodi, A. Psoriasis and small intestine bacterial overgrowth. Int. J. Dermatol. 2018, 57, 112–113. [Google Scholar] [CrossRef] [PubMed]
- Martin, R.; Henley, J.B.; Sarrazin, P.; Seite, S. Skin microbiome in patients with psoriasis before and after balneotherapy at the thermal care center of La Roche-Posay. J. Drugs Dermatol. 2015, 14, 1400–1405. [Google Scholar]
- Assarsson, M.; Duvetorp, A.; Dienus, O.; Söderman, J.; Seifert, O. Significant changes in the skin microbiome in patients with chronic plaque psoriasis after treatment with narrowband ultraviolet B. Acta Derm. Venereol. 2018, 98, 428–436. [Google Scholar] [CrossRef] [Green Version]
- Liu, S.H.; Yu, H.Y.; Chang, Y.C.; Hui, C.Y.R.; Huang, Y.C.; Huang, Y.H. Host characteristics and dynamics of Staphylococcus aureus colonization in patients with moderate-to-severe psoriasis before and after treatment: A prospective cohort study. J. Am. Acad. Dermatol. 2019, 81, 605–607. [Google Scholar] [CrossRef] [Green Version]
- Yeh, N.L.; Hsu, C.Y.; Tsai, T.F.; Chiu, H.Y. Gut Microbiome in psoriasis is perturbed differently during secukinumab and ustekinumab therapy and associated with response to treatment. Clin. Drug Investig. 2019, 39, 1195–1203. [Google Scholar] [CrossRef]
- Rendon, A.; Schakel, K. Psoriasis Pathogenesis and Treatment. Int. J. Mol. Sci. 2019, 20, 1475. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yang, C.C. The other side of biologics for psoriasis. Dermatol. Sin. 2022, 40, 65–66. [Google Scholar] [CrossRef]
- Nermes, M.; Kantele, J.M.; Atosuo, T.J.; Salminen, S.; Isolauri, E. Interaction of orally administered Lactobacillus rhamnosus GG with skin and gut microbiota and humoral immunity in infants with atopic dermatitis. Clin. Exp. Allergy 2011, 41, 370–377. [Google Scholar] [CrossRef]
- Targan, S.R.; Feagan, B.; Vermeire, S.; Panaccione, R.; Melmed, G.Y.; Landers, C.; Li, D.; Russell, C.; Newmark, R.; Zhang, N.; et al. A randomized, double-blind, placebo-controlled Phase 2 study of brodalumab in patients with moderate-to-severe Crohn’s disease. Am. J. Gastroenterol. 2016, 111, 1599–1607. [Google Scholar] [CrossRef] [PubMed]
- Hueber, W.; Sands, B.E.; Lewitzky, S.; Vandemeulebroecke, M.; Reinisch, W.; Higgins, P.D.; Wehkamp, J.; Feagan, B.G.; Yao, M.D.; Karczewski, M.; et al. Secukinumab, a human anti-IL-17A monoclonal antibody, for moderate to severe Crohn’s disease: Unexpected results of a randomised, double-blind placebo-controlled trial. Gut 2012, 61, 1693–1700. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Colombel, J.F.; Sendid, B.; Jouault, T.; Poulain, D. Secukinumab failure in Crohn’s disease: The yeast connection? Gut 2013, 62, 800–801. [Google Scholar] [CrossRef]
- Wang, J.; Bhatia, A.; Krugliak Cleveland, N.; Gupta, N.; Dalal, S.; Rubin, D.T.; Sakuraba, A. Rapid Onset of Inflammatory Bowel Disease after receiving secukinumab infusion. ACG Case Rep. J. 2018, 5, e56. [Google Scholar] [CrossRef]
- Sandborn, W.J.; D’Haens, G.R.; Reinisch, W.; Panés, J.; Chan, D.; Gonzalez, S.; Weisel, K.; Germinaro, M.; Frustaci, M.E.; Yang, Z.; et al. Guselkumab for the treatment of Crohn’s Disease: Induction results from the Phase 2 GALAXI-1 study. Gastroenterology 2022, 162, 1650–1664.e8. [Google Scholar] [CrossRef] [PubMed]
- Franzin, M.; Stefančič, K.; Lucafò, M.; Decorti, G.; Stocco, G. Microbiota and drug response in Inflammatory Bowel Disease. Pathogens 2021, 10, 211. [Google Scholar] [CrossRef]
- Seong, G.; Kim, N.; Joung, J.G.; Kim, E.R.; Chang, D.K.; Chun, J.; Hong, S.N.; Kim, Y.H. Changes in the intestinal microbiota of patients with Inflammatory Bowel Disease with clinical remission during an 8-Week infliximab infusion cycle. Microorganisms 2020, 8, 874. [Google Scholar] [CrossRef] [PubMed]
- Doherty Matthew, K.; Ding, T.; Koumpouras, C.; Telesco Shannon, E.; Monast, C.; Das, A.; Brodmerkel, C.; Schloss Patrick, D. Fecal microbiota signatures are associated with response to Ustekinumab therapy among Crohn’s Disease patients. mBio 2018, 9, e02120-17. [Google Scholar] [CrossRef] [Green Version]
- Ratajczak, W.; Rył, A.; Mizerski, A.; Walczakiewicz, K.; Sipak, O.; Laszczyńska, M. Immunomodulatory potential of gut microbiome-derived short-chain fatty acids (SCFAs). Acta Biochim. Pol. 2019, 66, 1–12. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yao, Y.; Cai, X.; Fei, W.; Ye, Y.; Zhao, M.; Zheng, C. The role of short-chain fatty acids in immunity, inflammation and metabolism. Crit. Rev. Food Sci. Nutr. 2022, 62, 1–12. [Google Scholar] [CrossRef] [PubMed]
- Sears, C.L. A dynamic partnership: Celebrating our gut flora. Anaerobe 2005, 11, 247–251. [Google Scholar] [CrossRef]
- Liu, L.; Xu, M.; Lan, R.; Hu, D.; Li, X.; Qiao, L.; Zhang, S.; Lin, X.; Yang, J.; Ren, Z.; et al. Bacteroides vulgatus attenuates experimental mice colitis through modulating gut microbiota and immune responses. Front. Immunol. 2022, 13, 1036196. [Google Scholar] [CrossRef]
- Wexler, A.G.; Goodman, A.L. An insider’s perspective: Bacteroides as a window into the microbiome. Nat. Microbiol. 2017, 2, 17026. [Google Scholar] [CrossRef] [Green Version]
- Yoshida, N.; Emoto, T.; Yamashita, T.; Watanabe, H.; Hayashi, T.; Tabata, T.; Hoshi, N.; Hatano, N.; Ozawa, G.; Sasaki, N.; et al. Bacteroides vulgatus and Bacteroides dorei Reduce Gut Microbial Lipopolysaccharide Production and Inhibit Atherosclerosis. Circulation 2018, 138, 2486–2498. [Google Scholar] [CrossRef]
- Ahluwalia, B.; Magnusson, M.K.; Ohman, L. Mucosal immune system of the gastrointestinal tract: Maintaining balance between the good and the bad. Scand. J. Gastroenterol. 2017, 52, 1185–1193. [Google Scholar] [CrossRef]
- Blum, H.E. The human microbiome. Adv. Med. Sci. 2017, 62, 414–420. [Google Scholar] [CrossRef]
- Egeberg, A.; Mallbris, L.; Warren, R.B.; Bachelez, H.; Gislason, G.H.; Hansen, P.R.; Skov, L. Association between psoriasis and inflammatory bowel disease: A Danish nationwide cohort study. Br. J. Dermatol. 2016, 175, 487–492. [Google Scholar] [CrossRef] [PubMed]
- Zakostelska, Z.; Malkova, J.; Klimesova, K.; Rossmann, P.; Hornova, M.; Novosadova, I.; Stehlikova, Z.; Kostovcik, M.; Hudcovic, T.; Stepankova, R.; et al. Intestinal Microbiota Promotes Psoriasis-Like Skin inflammation by enhancing Th17 response. PLoS ONE 2016, 11, e0159539. [Google Scholar] [CrossRef] [Green Version]
- Pinget, G.V.; Tan, J.K.; Ni, D.; Taitz, J.; Daien, C.I.; Mielle, J.; Moore, R.J.; Stanley, D.; Simpson, S.; King, N.J.C.; et al. Dysbiosis in imiquimod-induced psoriasis alters gut immunity and exacerbates colitis development. Cell Rep. 2022, 40, 111191. [Google Scholar] [CrossRef]
- Li, M.; Dai, B.; Tang, Y.; Lei, L.; Li, N.; Liu, C.; Ge, T.; Zhang, L.; Xu, Y.; Hu, Y.; et al. Altered Bacterial-Fungal interkingdom networks in the guts of Ankylosing Spondylitis patients. mSystems 2019, 4, e00176-18. [Google Scholar] [CrossRef] [Green Version]
- Chen, Y.J.; Wu, H.; Wu, S.D.; Lu, N.; Wang, Y.T.; Liu, H.N.; Dong, L.; Liu, T.T.; Shen, X.Z. Parasutterella, in association with irritable bowel syndrome and intestinal chronic inflammation. J. Gastroenterol. Hepatol. 2018, 33, 1844–1852. [Google Scholar] [CrossRef] [PubMed]
- Liu, L.; Chen, Y.; Wu, Q.; Shu, A.; Sun, J. Sodium butyrate attenuated diabetes-induced intestinal inflammation by modulating gut microbiota. Evid.-Based Complement. Alternat. Med. 2022, 2022, 4646245. [Google Scholar] [CrossRef] [PubMed]
- Zeng, C.; Wen, B.; Hou, G.; Lei, L.; Mei, Z.; Jia, X.; Chen, X.; Zhu, W.; Li, J.; Kuang, Y.; et al. Lipidomics profiling reveals the role of glycerophospholipid metabolism in psoriasis. Gigascience 2017, 6, 1–11. [Google Scholar] [CrossRef] [Green Version]
- Zhu, J.; Thompson, C.B. Metabolic regulation of cell growth and proliferation. Nat. Rev. Mol. Cell Biol. 2019, 20, 436–450. [Google Scholar] [CrossRef] [PubMed]
- Luo, Y.; Hara, T.; Kawashima, A.; Ishido, Y.; Suzuki, S.; Ishii, N.; Kambara, T.; Suzuki, K. Pathological role of excessive DNA as a trigger of keratinocyte proliferation in psoriasis. Clin. Exp. Immunol. 2020, 202, 1–10. [Google Scholar] [CrossRef] [PubMed]
- Pohla, L.; Ottas, A.; Kaldvee, B.; Abram, K.; Soomets, U.; Zilmer, M.; Reemann, P.; Jaks, V.; Kingo, K. Hyperproliferation is the main driver of metabolomic changes in psoriasis lesional skin. Sci. Rep. 2020, 10, 3081. [Google Scholar] [CrossRef] [Green Version]
- Jami, M.; Ghanbari, M.; Kneifel, W.; Domig, K.J. Phylogenetic diversity and biological activity of culturable Actinobacteria isolated from freshwater fish gut microbiota. Microbiol. Res. 2015, 175, 6–15. [Google Scholar] [CrossRef]
- Chang, C.J.; Zhang, J.; Tsai, Y.L.; Chen, C.B.; Lu, C.W.; Huo, Y.P.; Liou, H.M.; Ji, C.; Chung, W.H. Compositional features of distinct microbiota base on serum extracellular vesicle metagenomics analysis in moderate to severe psoriasis patients. Cells 2021, 10, 2349. [Google Scholar] [CrossRef]
- Marcinkiewicz, J.; Kontny, E. Taurine and inflammatory diseases. Amino Acids 2014, 46, 7–20. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hillmann, B.; Al-Ghalith, G.A.; Shields-Cutler, R.R.; Zhu, Q.; Gohl, D.M.; Beckman, K.B.; Knight, R.; Knights, D. Evaluating the Information Content of Shallow Shotgun Metagenomics. mSystems 2018, 3, e00069-18. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Huang, Y.C.; Lee, M.S.; Pan, W.H.; Wahlqvist, M.L. Validation of a simplified food frequency questionnaire as used in the Nutrition and Health Survey in Taiwan (NAHSIT) for the elderly. Asia Pac. J. Clin. Nutr. 2011, 20, 134–140. [Google Scholar]
- Lee, C.C.; Feng, Y.; Yeh, Y.M.; Lien, R.; Chen, C.L.; Zhou, Y.L.; Chiu, C.H. Gut dysbiosis, bacterial colonization and translocation, and neonatal sepsis in very-low-birth-weight preterm infants. Front. Microbiol. 2021, 12, 746111. [Google Scholar] [CrossRef]
- Caporaso, J.G.; Lauber, C.L.; Walters, W.A.; Berg-Lyons, D.; Lozupone, C.A.; Turnbaugh, P.J.; Fierer, N.; Knight, R. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl. Acad. Sci. USA 2011, 108 (Suppl. S1), 4516–4522. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Callahan, B.J.; McMurdie, P.J.; Rosen, M.J.; Han, A.W.; Johnson, A.J.; Holmes, S.P. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods 2016, 13, 581–583. [Google Scholar] [CrossRef] [Green Version]
- Pedregosa, F.; Varoquaux, G.; Gramfort, A.; Michel, V.; Thirion, B.; Grisel, O.; Blondel, M.; Prettenhofer, P.; Weiss, R.; Dubourg, V.; et al. Scikit-learn: Machine learning in python. J. Mach. Learn. Res. 2011, 12, 2825–2830. [Google Scholar]
- Quast, C.; Pruesse, E.; Yilmaz, P.; Gerken, J.; Schweer, T.; Yarza, P.; Peplies, J.; Glockner, F.O. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 2013, 41, D590–D596. [Google Scholar] [CrossRef]
- Caporaso, J.G.; Bittinger, K.; Bushman, F.D.; DeSantis, T.Z.; Andersen, G.L.; Knight, R. PyNAST: A flexible tool for aligning sequences to a template alignment. Bioinformatics 2010, 26, 266–267. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Price, M.N.; Dehal, P.S.; Arkin, A.P. FastTree: Computing large minimum evolution trees with profiles instead of a distance matrix. Mol. Biol. Evol. 2009, 26, 1641–1650. [Google Scholar] [CrossRef] [PubMed]
- Aßhauer, K.P.; Wemheuer, B.; Daniel, R.; Meinicke, P. Tax4Fun: Predicting functional profiles from metagenomic 16S rRNA data. Bioinformatics 2015, 31, 2882–2884. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Variables | All (n = 48) | IL-23 Inhibitor (Guselkumab) (n = 30) | IL-17 Inhibitor (Secukinumab and Ixekizumab (n = 18) | p-Value a |
---|---|---|---|---|
Ages (years), mean ± SD | 48.1 ± 11.9 | 45.2 ± 11.6 | 52.8 ± 12.6 | 0.045 * |
Gender/male, n (%) | 41 (85.4%) | 25 (83.3%) | 16 (88.9%) | 0.696 |
Weight (kg), mean ± SD | 75.2 ± 11.6 | 74.7 ± 12.5 | 76.1 ± 10.2 | 0.675 |
Psoriatic arthritis, n (%) | 15 (31.3%) | 8 (26.7%) | 7 (38.9%) | 0.522 |
PASI score, mean ± SD | 16.0 ± 6.6 | 15.2 ± 6.5 | 17.4 ± 6.7 | 0.273 |
PASI-90 at wk24, n (%) | 31 (64.6%) | 17 (57.0%) | 14 (77.0%) | 0.214 |
CRP (mg/L), mean ± SD | 3.3 ± 2.8 | 2.7 ± 2.3 | 4.4 ± 3.6 | 0.084 |
Treatment | KEGG Pathway | Week 0 | Week 24 | p-Value |
---|---|---|---|---|
IL-23 inhibitor | Lipid metabolism | |||
Fatty acid biosynthesis [PATH:ko00061] | 0.00864 | 0.008873 | 0.002367 | |
00071 Fatty acid degradation [PATH:ko00071] | 0.004989 | 0.005184 | 0.04726 | |
00565 Ether lipid metabolism [PATH:ko00565] | 0.000109 | 0.000132 | 0.03842 | |
00592 alpha-linolenic acid metabolism [PATH:ko00592] | 5.31 × 10−5 | 6.27 × 10−5 | 0.04265 | |
Energy metabolism | ||||
00195 Photosynthesis [PATH:ko00195] | 0.005238 | 0.005149 | 0.02341 | |
00680 Methane metabolism [PATH:ko00680] | 0.01616 | 0.01592 | 0.007612 | |
00710 Carbon fixation in photosynthetic organisms [PATH:ko00710] | 0.01162 | 0.01144 | 0.002367 | |
Amino acid metabolism | ||||
00220 Arginine biosynthesis [PATH:ko00220] | 0.01214 | 0.01188 | 0.01205 | |
00270 Cysteine and methionine metabolism [PATH:ko00270] | 0.02268 | 0.0225 | 0.04049 | |
00480 Glutathione metabolism [PATH:ko00480] | 0.003758 | 0.003977 | 0.0221 | |
Carbohydrate metabolism | ||||
00051 Fructose and mannose metabolism [PATH:ko00051] | 0.01362 | 0.01336 | 0.0106 | |
00562 Inositol phosphate metabolism [PATH:ko00562] | 0.001421 | 0.001496 | 0.03272 | |
00332 Carbapenem biosynthesis [PATH:ko00332] | 0.001633 | 0.001594 | 0.04971 | |
IL-17 inhibitor | 00300 Lysine biosynthesis [PATH:ko00300] | 0.01177 | 0.01159 | 0.03423 |
00901 Indole alkaloid biosynthesis [PATH:ko00901] | 1.91 × 10−6 | 2.50 × 10−6 | 0.03036 |
Treatment | KEGG Pathway | Responder | Non-Responder | p-Value |
---|---|---|---|---|
IL-23 inhibitor | Taurine and hypotaurine metabolism [PATH:ko00430] | 0.0001581 | −7.16 × 10−5 | 0.04808 |
IL-17 inhibitor | Amino acid metabolism | |||
Glycine, serine, and threonine metabolism [PATH:ko00260] | 0.0002248 | −0.0007905 | 0.02484 | |
Valine, leucine, and isoleucine biosynthesis [PATH:ko00290] | 9.18 × 10−5 | −0.0009196 | 0.04641 | |
Phenylalanine, tyrosine, and tryptophan biosynthesis [PATH:ko00400] | 3.27 × 10−5 | −0.001027 | 0.04641 | |
Cysteine and methionine metabolism [PATH:ko00270] | −7.21 × 10−5 | −0.0007994 | 0.03464 | |
Lysine biosynthesis [PATH:ko00300] | −7.21 × 10−5 | −0.0007994 | 0.03464 | |
Biosynthesis of other secondary metabolite | ||||
Novobiocin biosynthesis [PATH:ko00401] | 3.53 × 10−5 | −0.0001187 | 0.03464 | |
Acarbose and validamycin biosynthesis [PATH:ko00525] | 8.18 × 10−5 | −0.0001209 | 0.01765 | |
Carbohydrate metabolism | ||||
Citrate cycle (TCA cycle) [PATH:ko00020] | 0.0004246 | −0.001106 | 0.04641 | |
C5-Branched dibasic acid metabolism [PATH:ko00660] | 9.64 × 10−5 | −0.000547 | 0.04641 | |
One carbon pool by folate [PATH:ko00670] | 0.0001271 | −0.000506 | 0.01765 | |
Glucosinolate biosynthesis [PATH:ko00966] | 1.24 × 10−5 | −0.0001168 | 0.02484 | |
Synthesis and degradation of ketone bodies [PATH:ko00072] | −4.68 × 10−6 | 0.0002448 | 0.02484 | |
Biosynthesis of vancomycin group antibiotics [PATH:ko01055] | 5.35 × 10−5 | −9.27 × 10−5 | 0.02484 | |
Sphingolipid metabolism [PATH:ko00600] | 0.0003941 | −0.0008993 | 0.03464 | |
Glycosphingolipid biosynthesis—globo and isoglobo series [PATH:ko00603] | 0.0002465 | −0.000696 | 0.03464 | |
Aminobenzoate degradation [PATH:ko00627] | 3.99 × 10−5 | 0.0002052 | 0.04641 |
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Huang, Y.-H.; Chang, L.-C.; Chang, Y.-C.; Chung, W.-H.; Yang, S.-F.; Su, S.-C. Compositional Alteration of Gut Microbiota in Psoriasis Treated with IL-23 and IL-17 Inhibitors. Int. J. Mol. Sci. 2023, 24, 4568. https://doi.org/10.3390/ijms24054568
Huang Y-H, Chang L-C, Chang Y-C, Chung W-H, Yang S-F, Su S-C. Compositional Alteration of Gut Microbiota in Psoriasis Treated with IL-23 and IL-17 Inhibitors. International Journal of Molecular Sciences. 2023; 24(5):4568. https://doi.org/10.3390/ijms24054568
Chicago/Turabian StyleHuang, Yu-Huei, Lun-Ching Chang, Ya-Ching Chang, Wen-Hung Chung, Shun-Fa Yang, and Shih-Chi Su. 2023. "Compositional Alteration of Gut Microbiota in Psoriasis Treated with IL-23 and IL-17 Inhibitors" International Journal of Molecular Sciences 24, no. 5: 4568. https://doi.org/10.3390/ijms24054568