{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,11]],"date-time":"2026-03-11T06:43:28Z","timestamp":1773211408193,"version":"3.50.1"},"reference-count":42,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2026,2,28]],"date-time":"2026-02-28T00:00:00Z","timestamp":1772236800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Taishan Industry Leading Talents Project of Shandong Province","award":["tscx202312104"],"award-info":[{"award-number":["tscx202312104"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pharmaceuticals"],"abstract":"<jats:p>Aim: This study investigated the synergistic therapeutic effects and underlying mechanisms of tetrahydroberberine (THB) combined with protopanaxadiol (PPD) on p-chlorophenylalanine (PCPA)-induced insomnia in rats. Methods: Rats were randomly divided into normal, model, diazepam, THB monotherapy, PPD monotherapy, and THB + PPD combination groups. Evaluations included the pentobarbital sleep test, HE staining, ELISA, 16S rRNA sequencing, metabolomics, and Western blot. Results: Results demonstrated that the THB + PPD combination exhibited significant synergistic effects compared with monotherapies: the combination shortened sleep latency by 56.2% (vs. 44.2% for THB alone and 20.7% for PPD alone) and prolonged sleep duration by 112.8% (vs. 70.2% for THB and 59.6% for PPD) relative to the model group, while effectively restoring body weight gain. Histologically, combined treatment significantly alleviated hippocampal neuronal damage and increased the number of intact neurons in the dentate gyrus. Molecularly, it upregulated brain-derived neurotrophic factor (BDNF) and glial cell line-derived neurotrophic factor (GDNF) levels, restored neurotransmitter balance (serotonin, dopamine, and glutamate), suppressed overactivation of the hypothalamic\u2013pituitary\u2013adrenal (HPA) axis (reducing corticotropin-releasing hormone and corticosterone), and decreased pro-inflammatory cytokine expression. Gut microbiota analysis revealed that the combination restored microbial homeostasis (increasing beneficial bacteria such as *Lactobacillus*) and modulated the glycine\u2013serine\u2013threonine metabolic pathway. Mechanistically, THB + PPD synergistically activated the PI3K\/AKT neurotrophic pathway (p-PI3K and p-AKT expression increased by 1.9-fold and 2.5-fold, respectively, vs. model), inhibited the AGE\/RAGE pro-inflammatory axis (RAGE expression decreased by 31.8%), and enhanced blood\u2013brain barrier integrity by upregulating tight junction proteins (ZO-1, Occludin). Conclusions: THB combined with PPD exerts synergistic anti-insomnia effects through multi-level regulation of the microbiota\u2013gut\u2013brain axis, neurochemical balance, and key signaling pathways, providing a promising foundation for developing safe natural product-based combination therapies.<\/jats:p>","DOI":"10.3390\/ph19030390","type":"journal-article","created":{"date-parts":[[2026,3,2]],"date-time":"2026-03-02T16:06:59Z","timestamp":1772467619000},"page":"390","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Synergistic Therapeutic Effects of Tetrahydroberberine Combined with Protopanaxadiol on PCPA-Induced Insomnia in Rats: Involvement of the Microbiota\u2013Gut\u2013Brain Axis and Regulation of PI3K\/AKT\/AGE-RAGE Pathways"],"prefix":"10.3390","volume":"19","author":[{"given":"Meijia","family":"Li","sequence":"first","affiliation":[{"name":"College of Chinese Pharmacy, Tianjin University of Traditional Chinese Medicine, Tianjin 301600, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0009-0008-5915-2806","authenticated-orcid":false,"given":"Ying","family":"Wang","sequence":"additional","affiliation":[{"name":"School of Medicine and Pharmacy, Ocean University of China, Qingdao 266003, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0009-0005-1142-4647","authenticated-orcid":false,"given":"Zixia","family":"Liang","sequence":"additional","affiliation":[{"name":"Chinese Pharmacy, Guangdong Pharmaceutical University, Guangzhou 510006, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Honghua","family":"Li","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Integration and Innovation of Classic Formula and Modern Chinese Medicine, Lunan Pharmaceutical Group Co., Ltd., No. 209 Hongqi Road, Linyi 276000, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yun","family":"Zhao","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Integration and Innovation of Classic Formula and Modern Chinese Medicine, Lunan Pharmaceutical Group Co., Ltd., No. 209 Hongqi Road, Linyi 276000, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ling","family":"Kong","sequence":"additional","affiliation":[{"name":"School of Pharmacy, Heilongjiang University of Chinese Medicine, Harbin 154600, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Na","family":"Guo","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Integration and Innovation of Classic Formula and Modern Chinese Medicine, Lunan Pharmaceutical Group Co., Ltd., No. 209 Hongqi Road, Linyi 276000, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Guoxin","family":"Dai","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Integration and Innovation of Classic Formula and Modern Chinese Medicine, Lunan Pharmaceutical Group Co., Ltd., No. 209 Hongqi Road, Linyi 276000, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Guimin","family":"Zhang","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Integration and Innovation of Classic Formula and Modern Chinese Medicine, Lunan Pharmaceutical Group Co., Ltd., No. 209 Hongqi Road, Linyi 276000, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xiaoyan","family":"Lu","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Integration and Innovation of Classic Formula and Modern Chinese Medicine, Lunan Pharmaceutical Group Co., Ltd., No. 209 Hongqi Road, Linyi 276000, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9697-4931","authenticated-orcid":false,"given":"Jingchun","family":"Yao","sequence":"additional","affiliation":[{"name":"College of Chinese Pharmacy, Tianjin University of Traditional Chinese Medicine, Tianjin 301600, China"},{"name":"State Key Laboratory of Integration and Innovation of Classic Formula and Modern Chinese Medicine, Lunan Pharmaceutical Group Co., Ltd., No. 209 Hongqi Road, Linyi 276000, China"},{"name":"Lunan Better Pharmaceutical Co., Ltd., No. 209 Hongqi Road, Linyi 276000, China"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2026,2,28]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"767","DOI":"10.1016\/j.neurol.2023.08.008","article-title":"Insomnia in neurological disorders: Prevalence, mechanisms, impact and treatment approaches","volume":"179","author":"Geoffroy","year":"2023","journal-title":"Rev. Neurol."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Tom\u00e1s, C.C., Oliveira, E., Sousa, D., Uba-Chupel, M., Furtado, G., Rocha, C., Teixeira, A., Ferreira, P., Alves, C., and Gisin, S. (2016). Proceedings of the 3rd IPLeiria\u2019s International Health Congress. BMC Health Serv. Res., 16.","DOI":"10.1186\/s12913-016-1423-5"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1016\/j.pcad.2023.02.005","article-title":"Sleep physiology, pathophysiology, and sleep hygiene","volume":"77","author":"Baranwal","year":"2023","journal-title":"Prog. Cardiovasc. Dis."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1016\/j.smrv.2009.04.002","article-title":"The hyperarousal model of insomnia: A review of the concept and its evidence","volume":"14","author":"Riemann","year":"2010","journal-title":"Sleep Med. Rev."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"394","DOI":"10.1038\/s41588-018-0333-3","article-title":"Genome-wide analysis of insomnia in 1,331,010 individuals identifies new risk loci and functional pathways","volume":"51","author":"Jansen","year":"2019","journal-title":"Nat. Genet."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1016\/j.jsmc.2023.02.003","article-title":"Sleep and Inflammation: Bidirectional Relationship","volume":"18","author":"Veler","year":"2023","journal-title":"Sleep Med. Clin."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Zielinski, M.R., and Gibbons, A.J. (2022). Neuroinflammation, Sleep, and Circadian Rhythms. Front. Cell. Infect. Microbiol., 12.","DOI":"10.3389\/fcimb.2022.853096"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"105758","DOI":"10.1016\/j.nbd.2022.105758","article-title":"Targeting the MGBA with -biotics in epilepsy: New insights from preclinical and clinical studies","volume":"170","author":"Riva","year":"2022","journal-title":"Neurobiol. Dis."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.sleep.2021.08.003","article-title":"Relationship between sleep disorders and gut dysbiosis: What affects what?","volume":"87","author":"Neroni","year":"2021","journal-title":"Sleep Med."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"10813","DOI":"10.1007\/s12035-025-04846-0","article-title":"Microbiome Gut-Brain-Axis: Impact on Brain Development and Mental Health","volume":"62","author":"Ramadan","year":"2025","journal-title":"Mol. Neurobiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"101646","DOI":"10.1016\/j.smrv.2022.101646","article-title":"Effects of cognitive behavioral therapy for insomnia (CBT-I) on quality of life: A systematic review and meta-analysis","volume":"64","author":"Alimoradi","year":"2022","journal-title":"Sleep Med. Rev."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"191","DOI":"10.7326\/M14-2841","article-title":"Cognitive Behavioral Therapy for Chronic Insomnia: A Systematic Review and Meta-analysis","volume":"163","author":"Trauer","year":"2015","journal-title":"Ann. Intern. Med."},{"key":"ref_13","first-page":"575","article-title":"Insomnia Study Group of the Spanish Sleep Society (SES). Melatonin in sleep disorders","volume":"37","author":"Poza","year":"2022","journal-title":"Neurologia (Engl. Ed.)"},{"key":"ref_14","first-page":"154","article-title":"Treatment of Chronic Insomnia in Adults","volume":"109","author":"Matheson","year":"2024","journal-title":"Am. Fam. Physician."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Monmai, C., Kim, J.S., and Baek, S.H. (2023). Effect of Ginseng Sapogenin Protopanaxadiol-Enriched Rice (DJ-PPD) on Immunomodulation. Plants, 12.","DOI":"10.3390\/plants12040767"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"156186","DOI":"10.1016\/j.phymed.2024.156186","article-title":"Ginsenoside Rg1 enriches gut microbial indole-3-acetic acid to alleviate depression-like behavior in mice via oxytocin signaling","volume":"135","author":"Yu","year":"2024","journal-title":"Phytomedicine"},{"key":"ref_17","first-page":"301","article-title":"Antifibrillatory effect of tetrahydroberberine","volume":"14","author":"Sun","year":"1993","journal-title":"Zhongguo Yao Li Xue Bao (Chin. J. Pharmacol. Toxicol.)"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"112141","DOI":"10.1016\/j.biopha.2021.112141","article-title":"Soporific effect of modified Suanzaoren Decoction on mice models of insomnia by regulating Orexin-A and HPA axis homeostasis","volume":"143","author":"Dong","year":"2021","journal-title":"Biomed. Pharmacother."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1186\/s12966-019-0791-8","article-title":"Depression, emotional eating and long-term weight changes: A population-based prospective study","volume":"16","author":"Konttinen","year":"2019","journal-title":"Int. J. Behav. Nutr. Phys. Act."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"118401","DOI":"10.1016\/j.jep.2024.118401","article-title":"A comprehensive study on the regulation of Compound Zaoren Granules on cAMP\/CREB signaling pathway and metabolic disorder in CUMS-PCPA induced insomnia rats","volume":"332","author":"Wang","year":"2024","journal-title":"J. Ethnopharmacol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"15450","DOI":"10.1007\/s12035-025-05210-y","article-title":"Neurochemical Insights into the Role of Tryptophan Metabolites and Kynurenine Pathway in Insomnia and its Psychological and Neurological Comorbidities","volume":"62","author":"Sarawi","year":"2025","journal-title":"Mol. Neurobiol."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Gabryelska, A., Turkiewicz, S., Ditmer, M., Gajewski, A., Strzelecki, D., Bia\u0142asiewicz, P., Cha\u0142ubi\u0144ski, M., and Sochal, M. (2024). The Complex Relationship between Neuromodulators, Circadian Rhythms, and Insomnia in Patients with Obstructive Sleep Apnea. Int. J. Mol. Sci., 25.","DOI":"10.3390\/ijms25158469"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"e13902","DOI":"10.1111\/jsr.13902","article-title":"The orexin story and orexin receptor antagonists for the treatment of insomnia","volume":"32","author":"Muehlan","year":"2023","journal-title":"J. Sleep Res."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"101588","DOI":"10.1016\/j.smrv.2022.101588","article-title":"HPA axis activity in patients with chronic insomnia: A systematic review and meta-analysis of case-control studies","volume":"62","author":"Dressle","year":"2022","journal-title":"Sleep Med. Rev."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"859","DOI":"10.1001\/jamapsychiatry.2025.1327","article-title":"Inflammatory Exposure and Depression in Older Adults With Insomnia: A Randomized Clinical Trial","volume":"82","author":"Irwin","year":"2025","journal-title":"JAMA Psychiatry"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/j.jad.2023.01.086","article-title":"Effects of exercise training on inflammatory, neurotrophic and immunological markers and neurotransmitters in people with depression: A systematic review and meta-analysis","volume":"326","author":"Feter","year":"2023","journal-title":"J. Affect. Disord."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"118036","DOI":"10.1016\/j.lfs.2020.118036","article-title":"DHA reduces hypothalamic inflammation and improves central leptin signaling in mice","volume":"257","author":"Cheng","year":"2020","journal-title":"Life Sci."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"175171","DOI":"10.1016\/j.ejphar.2022.175171","article-title":"Remodeling of microbiota gut-brain axis using psychobiotics in depression","volume":"931","author":"Palepu","year":"2022","journal-title":"Eur. J. Pharmacol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"114344","DOI":"10.1016\/j.biopha.2023.114344","article-title":"Gut microbiota: A new target of traditional Chinese medicine for insomnia","volume":"160","author":"Feng","year":"2023","journal-title":"Biomed. Pharmacother."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1709","DOI":"10.2147\/NSS.S526037","article-title":"Gut Microbiome Composition Changes During Insomnia Treatment with Lemborexant","volume":"17","author":"Miyata","year":"2025","journal-title":"Nat. Sci. Sleep"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"10603","DOI":"10.1080\/21655979.2021.2000242","article-title":"Impacts of changes in intestinal flora on the metabolism of Sprague-Dawley rats","volume":"12","author":"Wang","year":"2021","journal-title":"Bioengineered"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1716701","DOI":"10.1155\/2017\/1716701","article-title":"Multifarious Beneficial Effect of Nonessential Amino Acid, Glycine: A Review","volume":"2017","author":"Razak","year":"2017","journal-title":"Oxid. Med. Cell. Longev."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"iyad136","DOI":"10.1093\/genetics\/iyad136","article-title":"Sleep need, the key regulator of sleep homeostasis, is indicated and controlled by phosphorylation of threonine 221 in salt-inducible kinase 3","volume":"225","author":"Li","year":"2023","journal-title":"Genetics"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"102028","DOI":"10.1016\/j.xcrm.2025.102028","article-title":"Microbiota-produced immune regulatory bile acid metabolites control central nervous system autoimmunity","volume":"6","author":"Montini","year":"2025","journal-title":"Cell Rep. Med."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"116012","DOI":"10.1016\/j.biopha.2023.116012","article-title":"Berberine exerts antidepressant effects in vivo and in vitro through the PI3K\/AKT\/CREB\/BDNF signaling pathway","volume":"170","author":"Tang","year":"2024","journal-title":"Biomed. Pharmacother."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Vianello, E., Beltrami, A.P., Aleksova, A., Janjusevic, M., Fluca, A.L., Romanelli, M.M.C., La Sala, L., and Dozio, E. (2025). The Advanced Glycation End-Products (AGE)-Receptor for AGE System (RAGE): An Inflammatory Pathway Linking Obesity and Cardiovascular Diseases. Int. J. Mol. Sci., 26.","DOI":"10.3390\/ijms26083707"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s12272-020-01287-2","article-title":"Pathological angiogenesis and inflammation in tissues","volume":"44","author":"Jeong","year":"2021","journal-title":"Arch. Pharm. Res."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"e0046824","DOI":"10.1128\/iai.00468-24","article-title":"Rickettsia disrupts and reduces endothelial tight junction protein zonula occludens-1 in association with inflammasome activation","volume":"93","author":"Velatooru","year":"2025","journal-title":"Infect. Immun."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Wu, N., Li, X., Ma, H., Zhang, X., Liu, B., Wang, Y., Zheng, Q., and Fan, X. (2023). The role of the gut microbiota and fecal microbiota transplantation in neuroimmune diseases. Front. Neurol., 14.","DOI":"10.3389\/fneur.2023.1108738"},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Wang, L., Qi, X., Wang, S., Tian, C., Zou, T., Liu, Z., Chen, Q., Chen, Y., Zhao, Y., and Li, S. (2024). Banxia-Yiyiren alleviates insomnia and anxiety by regulating the gut microbiota and metabolites of PCPA-induced insomnia model rats. Front. Microbiol., 15.","DOI":"10.3389\/fmicb.2024.1405566"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1016\/j.jep.2009.01.012","article-title":"Methanol extract of Longanae Arillus augments pentobarbital-induced sleep behaviors through the modification of GABAergic systems","volume":"122","author":"Ma","year":"2009","journal-title":"J. Ethnopharmacol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"e114852","DOI":"10.1016\/j.intimp.2025.114852","article-title":"Promotion of sleep by cinnamic acid in parachlorophenylalanine-induced insomnia in rats","volume":"158","author":"Ye","year":"2025","journal-title":"Int. Immunopharmacol."}],"container-title":["Pharmaceuticals"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1424-8247\/19\/3\/390\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,3,10]],"date-time":"2026-03-10T08:59:12Z","timestamp":1773133152000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1424-8247\/19\/3\/390"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,2,28]]},"references-count":42,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2026,3]]}},"alternative-id":["ph19030390"],"URL":"https:\/\/doi.org\/10.3390\/ph19030390","relation":{},"ISSN":["1424-8247"],"issn-type":[{"value":"1424-8247","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,2,28]]}}}