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Circadian cycle and neuroinflammation

  • Xinzi Xu , Junli Wang und Guohua Chen EMAIL logo
Veröffentlicht/Copyright: 17. Oktober 2023
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Open Life Sciences
Aus der Zeitschrift Open Life Sciences Band 18 Heft 1

Abstract

Circadian cycle is a fundamental characteristic of life formed in the long-term evolution of organisms and plays an important role in maintaining the proliferation, migration, and activation of immune cells. Studies have shown that circadian rhythm disorders affect the occurrence and development of neuroinflammation by inducing glial cell activation and peripheral immune responses. In this article, we briefly described the research progress of neuroinflammation and circadian rhythm in recent years and explored the effects and possible mechanism of circadian rhythmicity on microglia, astrocytes, and peripheral immune function.

Keywords: circadian rhythm; neuroinflammation; microglia; astrocyte

1 Introduction

Neuroinflammation refers to a wide range of inflammatory responses that occur in the central nervous system (CNS), characterized by glial cell activation, production, and release of inflammatory mediators, and recruitment of peripheral immune cells [1]. Neuroinflammation is an important physiological response of the brain to defend against infections and injuries, promote tissue repair, and clear cellular debris and pathogens [2]. However, a large number of pro-inflammatory mediators could be released under excessive inflammatory stimulation, which leads to blood-brain barrier (BBB) leakage and neurotoxic damage, thus participating in the pathological processes of various neurological and psychiatric disorders [3].

The circadian cycle is the regular biological activity variation with the day-night cycle as its period that organisms have developed through long-term evolution. Studies have found that the disruption of the circadian cycle is closely related to the immune function and inflammatory response of the body [4]. Almost all immune cells in humans and animals (such as microglia, neutrophils, monocytes, and lymphocytes) could express clock genes [5,6] and are involved in regulating the maturation and activation of immune cells [7,8]. Therefore, the disruption of the circadian cycle may be an important cause of mediating central and peripheral inflammatory responses. We will review the research progress in recent years on the disruption of the circadian cycle and its regulation of microglia, astrocytes, and peripheral immune cells involved in neuroinflammation.

2 Circadian cycle and clock genes

The circadian cycle is a characteristic biological process observed in organisms at both physiological and behavioral levels. For example, animal feeding, activity, sleep-wake cycles [9], as well as fluctuations in heart rate, blood pressure, body temperature, and some hormone levels all exhibit rhythmicity with a period of approximately 24 h [10]. The circadian cycle system consists of three parts: input, central oscillator, and output. The input pathway primarily refers to the components, like the retina, which can perceive changes in external environmental signals such as natural light, temperature, and feeding. These components transmit the changes in signals to the biological clock. The output pathway refers to the various biological rhythms regulated by the biological clock, oscillating near a 24 h cycle and involving various crucial physiological and biochemical processes in the human body. In humans and mammals, the central oscillator is mainly located in the suprachiasmatic nucleus (SCN) of the hypothalamus. As the pacemaker of the circadian cycle (also known as the central clock), it can sense external environmental information conveyed by entrainment factors (such as the light–dark signal projection received by the retinohypothalamic nerve tracts), and then transmit the signal to peripheral clocks through changes in autonomic nervous excitability and neuroendocrine activity, adjusting its own phase to adapt the body to the external environment.

At the molecular level, the circadian cycle is mainly controlled by the transcription-translation negative feedback loop composed of core components of the biological clock. The positive elements mainly include the Clock and Bmal1 genes. As transcription factors, Clock and Bmal1 form a heterodimer through the PAS (PER–ARNT–SIM) domain. This heterodimer binds to the E-box (CACGTC) sequence in the promoter region of downstream genes, driving the transcription of target genes such as Per and Cry. When the expression of Per and Cry increases, they can translocate to the cell nucleus as negative elements and feedback inhibit the activity of Clock–Bmal1. Also, the Clock–Bmal1 heterodimer can activate clock-controlled genes Rev-erb and ROR transcription, which competitively bind to the RORE site on the Bmal1 promoter, thereby influencing the expression of Bmal1 [11]. In addition, genes such as E4BP4, DBP, and NFIL3 can also assist in regulating the expression of the negative feedback loop, jointly maintaining the approximate 24 h periodic oscillation of the biological clock.

Natural light is the most important zeitgeber that acts on organisms, promoting the synchronization of their circadian cycle with periodic environmental changes. Studies have shown that factors such as urban light pollution, nocturne jobs, and jet lag, which cause light signals to be out of sync with the natural light cycle, can suppress melatonin secretion and lead to a disrupted circadian cycle, with reduced amplitude and/or delayed phase. In addition, daily activities such as eating, socializing, and exercise can also affect the dynamic changes of the circadian cycle by influencing the neuroendocrine system, including the secretion of glucocorticoids to achieve synchronization of peripheral clocks [12,13].

3 Circadian cycle disturbance and neuroinflammation

In 1960, Halberg et al. first discovered that the mortality rate of mice induced by lipopolysaccharide changed in a time-dependent manner. A dose of endotoxin which is compatible with the survival of most animals when given during the middle of the daily dark period is highly lethal when it is given 8–12 h earlier or later, suggesting that the immune system may have a circadian cycle [14]. Subsequent studies confirmed that the number of circulating white blood cells in the human and animal body shows regular fluctuations within 24 h. For nocturnal mice, the peak occurs mostly around dusk, while for humans it is mostly around 8 am [15]. Further research found that the proliferation, migration, and activation of immune cells are also influenced by the circadian cycle and the expression of clock genes [16], indicating a close association between the circadian cycle and immune inflammation.

3.1 Circadian cycle and neuroinflammatory factors

In recent years, studies have suggested that the inflammatory response in the CNS is also regulated by the circadian cycle. Animal models exposed to night-shift work or night light showed significantly increased levels of activated microglia and proinflammatory cytokines in brain tissue, affecting the recovery of neural function in a focal brain ischemia model and inducing anxiety and depressive behavior in mice [17,18]. Sleep deprivation can activate NF-κB and increase the release of inflammatory factors such as IL-1β and TNF-α in the hippocampus, leading to neuronal damage [19]. IL-1β and TNF-α, as important cell factors that mediate inflammatory damage, are believed to be closely related to the regulation of the sleep–wake cycle and sleep phase in the body. Studies have shown that IL-1β and TNF-α mRNA levels in the brain tissue of experimental animals exhibit significant circadian rhythm changes that are consistent with changes in the sleep–wake cycle. Inhibiting the expression of IL-1β and TNF-α can reduce the spontaneous non-rapid eye movement sleep in experimental animals [20,21,22], confirming that pro-inflammatory cytokines may be important factors in mediating the interaction between circadian cycle and neuroimmune function.

3.2 Circadian cycle and microglia

Microglia are the most common resident immune cells in the CNS. Lineage tracing studies have shown that microglia originate from precursor cells in the yolk sac erythromyeloid lineage and migrate to the neural tube during early embryonic development. They then settle in the brain parenchyma and maintain their numbers through continuous self-renewal [23]. Microglia exhibit high plasticity and heterogeneity. In the adult brain, microglia in a steady state exhibit a small, highly branched morphology (M0 phenotype) and dynamically sense changes in the microenvironment. They interact extensively with neurons, astrocytes, and oligodendrocytes, among others, to perform important physiological functions such as immune surveillance, synaptic remodeling, and clearance of cellular debris [24,25,26]. Once exposed to abnormal conditions, microglia can be rapidly activated into an amoeboid shape and transform into multiple functional phenotypes in response to various stimuli, thereby enhancing phagocytic activity and regulating inflammatory responses [27]. Receptors associated with phagocytic function include chemokine CX3C receptor 1, triggering receptor expressed on myeloid cells 2, purinergic receptor P2Y12, complement component receptors, and integrin αM subunits, among others [28]. In the classical activation pathway, microglia can be activated to the M1 proinflammatory phenotype by stimuli such as damage or pathogens such as lipopolysaccharide, interferon-γ, and β-amyloid protein. This leads to the release of large amounts of proinflammatory factors such as TNF-α, IL-18, IL-1β, and nitrogen-containing substances and reactive oxygen species, triggering antigen presentation-mediated adaptive immunity [29]. Microglia also exhibit an alternative activation M2 phenotype, which mainly expresses anti-inflammatory cytokines and growth factors such as IL-4, IL-10, and TGF-β. This plays an important role in suppressing inflammatory responses, protecting and repairing neurons, among other functions [30].

In recent years, transcriptomic analysis has revealed functional heterogeneity among subpopulations of microglia [31]. Besides external environmental stimuli, the phenotype of microglia is tightly regulated to some extent by their intrinsic characteristics [32]. It is believed that the endogenous circadian system is one of the important factors influencing microglial activation and phenotype transformation [8]. In 2011, Nakazato et al. first demonstrated the expression of clock genes, such as Per1 and Per2, in primary cultured microglia and BV2 cells [33]. Subsequent studies also confirmed the periodic oscillation of endogenous clock genes in microglia at the level of in vitro and ex vivo isolation and purification. Among them, the secretion peak of Per1 and Per2 occurs at Zeitgeber time (ZT) 14, which is 2 h into the dark phase, while the peak of Rev-erb appears at ZT18 [5]. It is worth noting that different clock gene expressions can mediate structural and functional changes in microglia, leading them to follow the circadian cycle consistent with the central clock. Studies have shown that compared to the sleep phase (i.e., light phase), microglial processes in the wakefulness phase of the mouse cortex are longer and the number of branches increases [34]. P2Y12 receptor, as a microglial surface-specific protein, is an important signaling molecule that drives its directional movement and cell tropism [35]. During wakefulness, the secretion of cathepsin S by microglia can mediate changes in cell morphology and increase process length by activating its own P2Y12 receptor [34]. On the other hand, the circadian cycle is also closely related to the phagocytic function and immune activity of microglia. Research shows that under conditions of light exposure, the inflammatory activity of rat microglia is enhanced, with a significant increase in the production and release of pro-inflammatory cytokines TNF-α, IL-1β, and IL-6. At this time, the phagocytic function of microglia is weakened, and the expression of surface activation marker protein CD11b, complement pathway, and milk fat globule epidermal growth factor 8 (MFG-E8) are inhibited [36]. MFG-E8 acts as a soluble bridging molecule, which binds to microglia integrin subunit αγβ3 or αγβ5 to induce its phagocytic function. Bmal1, as one of the core clock genes, is believed to be associated with rhythmic changes in microglial function. Wang et al. [37] found that when Bmal1 gene was knocked down in mice and BV2 cell models exposed to LPS, it could lead to downregulation of pro-inflammatory cytokine expression, upregulation of antioxidant and anti-inflammatory gene expression, and the mechanism of which requires further investigation. Clock-controlled gene Rev-erb also plays an important role in the molecular clock and neuroinflammatory regulation of microglia. Wolff et al. observed that after intervening with the primary microglia cells using the Rev-erb gene activator SR9011, SR9011 interferes with the rhythmic secretion of cells, participates in inhibiting their inflammatory activity and phagocytic function, and downregulates the mitochondrial respiration and ATP production of microglial cells [38]. In addition, research shows that the negative feedback transcription factor E4bp4 can also downregulate the activation of microglia by directly binding to the D-box element in the promoter region to inhibit the MAPK/ERK signaling pathway [39].

3.3 Circadian cycle and astrocytes

Astrocytes are the largest type of glial cells in the CNS, with multiple elongated branches that fill the CNS. They form extensive connections with neurons, oligodendrocytes, and microglia, and participate in important processes such as synapse formation, regulation of neuronal activity, and maintenance of the integrity of the BBB in physiological conditions [40]. However, in pathological situations such as trauma, infection, and ischemia, astrocytes rapidly respond by forming reactive astrocytes (RAS) characterized by hypertrophy, proliferation, and molecular remodeling [41]. Currently, it is generally believed that RAS induced by inflammatory and ischemic stimuli have significant differences in gene expression and are respectively named classical astrocytes (A1 type) and selective astrocytes (A2 type) [42]. A1-type astrocytes are the main source of the synaptic destructive classical complement cascade components (C3 and C4B), and can release neurotoxins such as long-chain saturated lipids, causing neuronal and oligodendrocyte death. A2-type astrocytes can release various neurotrophic factors such as vascular endothelial growth factor and have neuroprotective effects [43]. Therefore, astrocytes also play an important role in neuroinflammatory reactions.

Traditional views hold that the circadian cycle is controlled by the electrical activity coupling of different neuron subgroups within the SCN. However, recent studies have found that astrocytes are also an indispensable part of the regulation of the SCN circadian cycle [44]. On the one hand, astrocytes can influence neuronal activity by regulating extracellular levels of gamma-aminobutyric acid (GABA) and glutamate, thereby mediating the regulation of the SCN circadian cycle [45,46]. When glutamate release from astrocytes is inhibited, neuronal Ca2+ rhythmic oscillations are impaired, and the SCN loses synchronized rhythms [46]. Specific loss of the Bmal1 gene can delay the phase of autonomous movement in mice by affecting the expression of neuronal clock proteins through the GABA signal [45]. On the other hand, astrocytes can autonomously initiate and maintain the oscillation of SCN clock genes and rhythmic behavioral expression in adult animals and cells. Research has found that transfection of SCN astrocytes with a lentiviral vector overexpressing the Cry gene can restore the daily circadian rhythms and behavior of Cry knockout mice [47]. In addition, disruption of the circadian clock genes also affects the biological functions of astrocytes. Abnormal activation and increased release of pro-inflammatory cytokines can be observed in astrocytes with Bmal1 gene knockout, possibly due to inhibition of the glutathione-S-transferase signaling pathway [48]. The low-affinity nerve growth factor receptor p75NTR is also a circadian clock gene that contains evolutionarily conserved E-box enhancers and can be directly regulated by Clock–Bmal1 heterodimers [49]. It has been found that rhythmic expression of p75NTR can mediate the daily metabolic balance of glucose or glycogen in astrocytes, and lactate generated by glycolysis can be transferred from astrocytes to neurons to meet their energy demands [50].

3.4 Circadian cycle and peripheral immune system

In the past, due to the belief that the brain has special anatomical and physiological features, such as the lack of a lymphatic drainage system and specific antigen-presenting cells, as well as the presence of the BBB that restricts the entry of pathogens and immune cells, it has been considered as one of the body’s immune privileged sites. However, current research has shown that there exists a complex lymphatic drainage network in the brain, composed of perivascular spaces (VRS), glial lymphatic system, and meningeal lymphatic vessels, which allows peripheral immune cells to enter the cerebrospinal fluid and VRS under physiological conditions, playing an immunosurveillance role [51,52]. Under pathological stimulation, most cells in the CNS, such as microglia, astrocytes, and neurons, can express the major histocompatibility complex (MHC), playing an antigen-presenting role [53,54]. In addition, sustained activation of microglia and astrocytes can cause BBB leakage, leading to the infiltration, adhesion, and migration of a large number of neutrophils and lymphocytes into the CNS, further mediating neuroinflammatory responses [55]. However, some studies have also shown that in the neuroinflammatory response induced by autoimmune encephalomyelitis models, microglia may not primarily function as antigen-presenting cells, but rather through infiltrated dendritic cells expressing MHC class II molecules to mediate T-cell immune responses [56]. Therefore, there exist complex interactions between the peripheral immune system and the CNS, involving multiple pathological processes in the neuroimmune response.

The circadian cycle plays an important role in the regulation of the peripheral immune system. Most peripheral immune cells, including innate and adaptive immune cells, have their own molecular clock and exhibit significant rhythmic differences during recruitment and activation processes [15,57,58]. Studies have found that the bone marrow chemokine CXCL12 is regulated by the hypothalamic sympathetic–parasympathetic nervous system in a circadian manner, leading to periodic fluctuations in CXCL12 levels and activation of the CXCR4 receptor to maintain the daily rhythmic changes in the number of neutrophils in the blood reserve in the bone marrow [59]. In addition, Bmal1 can regulate neutrophil transcription and migration by controlling the CXCR2 and CXCR4 signaling pathways, respectively, and exert pro-/anti-aging effects on neutrophils [7]. In macrophages, the circadian cycle affects the signaling pathways of macrophage pattern recognition receptors, inflammatory mediators, and phagocytic activity [60]. Krüppel-like factor 4 (KLF4) expression is thought to be a time-specific molecule, and its periodic secretion is involved in the regulation of macrophage phenotype and the rhythmic expression of inflammatory factors. KLF4 expression is downregulated in aging macrophages, and disrupting the circadian rhythms of macrophages after inhibiting KLF4 gene expression further confirms the close relationship between circadian rhythms expression and disruption of the innate immune state [61]. Studies have suggested that the clock gene REV-ERBα mediates the expression of the PI3K/Akt signaling pathway and is involved in regulating the diurnal rhythm of macrophage polarization [62], indicating that REV-ERBα could also be a potential drug intervention target for regulating the circadian rhythms and inflammatory response. Similarly, adaptive immune responses also exhibit rhythmicity. Studies have shown that the strength of the immune response induced by antigen immunization at different times of the day varies significantly. Compared to nighttime, more CD8+ T cells are produced in response to antigen immunization at noon, and the rhythmic response disappears after knocking out the Bmal1 gene in T cells, further confirming the importance of circadian rhythms in regulating adaptive immune responses [63].

4 Conclusion

As an important characteristic of adaptive evolution in organisms, the circadian cycle is involved in various life processes at multiple levels, including the organism, organ, and cellular levels. Disruptions in the circadian cycle are closely related to neuroinflammation, where the disruption of the rhythmicity of microglia, astrocytes, and peripheral immune function mediate abnormal phenotypic transformation and secretion activity of inflammatory cells, promoting the development of neuroinflammation. However the mechanisms by which disruptions in the circadian cycle regulate neuroinflammation are not fully understood, and some of which involve the modulation of sleep and the expression of NLRP3 inflammasomes [64,65]. Therefore, further exploration of the molecular patterns of circadian rhythms regulation and the specific mechanisms of its interaction with neuroinflammation may be an important research direction in the future.

# Co-first author. These authors contributed equally to this work.

  1. Funding information: The youth project of Wuhan Municipality’s Health and Family Planning Commission (No. WZ21Q08) and Wuhan Application Foundation Frontier Project (No. 2020020601012302) funded this work.

  2. Conflict of interest: Authors state no conflict of interest.

  3. Data availability statement: Data sharing is not applicable to this article as no datasets were generated or analyzed during the current study.

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Received: 2023-04-20
Revised: 2023-07-05
Accepted: 2023-08-06
Published Online: 2023-10-17

© 2023 the author(s), published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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  265. An advanced approach for fig leaf disease detection and classification: Leveraging image processing and enhanced support vector machine methodology
  266. Erratum
  267. Erratum to “Protein Z modulates the metastasis of lung adenocarcinoma cells”
  268. Erratum to “BRCA1 subcellular localization regulated by PI3K signaling pathway in triple-negative breast cancer MDA-MB-231 cells and hormone-sensitive T47D cells”
  269. Retraction
  270. Retraction to “Protocatechuic acid attenuates cerebral aneurysm formation and progression by inhibiting TNF-alpha/Nrf-2/NF-kB-mediated inflammatory mechanisms in experimental rats”
https://doi.org/10.1515/biol-2022-0712
Schlagwörter für diesen Artikel
circadian rhythm; neuroinflammation; microglia; astrocyte
Creative Commons
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Artikel in diesem Heft

  1. Biomedical Sciences
  2. Systemic investigation of inetetamab in combination with small molecules to treat HER2-overexpressing breast and gastric cancers
  3. Immunosuppressive treatment for idiopathic membranous nephropathy: An updated network meta-analysis
  4. Identifying two pathogenic variants in a patient with pigmented paravenous retinochoroidal atrophy
  5. Effects of phytoestrogens combined with cold stress on sperm parameters and testicular proteomics in rats
  6. A case of pulmonary embolism with bad warfarin anticoagulant effects caused by E. coli infection
  7. Neutrophilia with subclinical Cushing’s disease: A case report and literature review
  8. Isoimperatorin alleviates lipopolysaccharide-induced periodontitis by downregulating ERK1/2 and NF-κB pathways
  9. Immunoregulation of synovial macrophages for the treatment of osteoarthritis
  10. Novel CPLANE1 c.8948dupT (p.P2984Tfs*7) variant in a child patient with Joubert syndrome
  11. Antiphospholipid antibodies and the risk of thrombosis in myeloproliferative neoplasms
  12. Immunological responses of septic rats to combination therapy with thymosin α1 and vitamin C
  13. High glucose and high lipid induced mitochondrial dysfunction in JEG-3 cells through oxidative stress
  14. Pharmacological inhibition of the ubiquitin-specific protease 8 effectively suppresses glioblastoma cell growth
  15. Levocarnitine regulates the growth of angiotensin II-induced myocardial fibrosis cells via TIMP-1
  16. Age-related changes in peripheral T-cell subpopulations in elderly individuals: An observational study
  17. Single-cell transcription analysis reveals the tumor origin and heterogeneity of human bilateral renal clear cell carcinoma
  18. Identification of iron metabolism-related genes as diagnostic signatures in sepsis by blood transcriptomic analysis
  19. Long noncoding RNA ACART knockdown decreases 3T3-L1 preadipocyte proliferation and differentiation
  20. Surgery, adjuvant immunotherapy plus chemotherapy and radiotherapy for primary malignant melanoma of the parotid gland (PGMM): A case report
  21. Dosimetry comparison with helical tomotherapy, volumetric modulated arc therapy, and intensity-modulated radiotherapy for grade II gliomas: A single‑institution case series
  22. Soy isoflavone reduces LPS-induced acute lung injury via increasing aquaporin 1 and aquaporin 5 in rats
  23. Refractory hypokalemia with sexual dysplasia and infertility caused by 17α-hydroxylase deficiency and triple X syndrome: A case report
  24. Meta-analysis of cancer risk among end stage renal disease undergoing maintenance dialysis
  25. 6-Phosphogluconate dehydrogenase inhibition arrests growth and induces apoptosis in gastric cancer via AMPK activation and oxidative stress
  26. Experimental study on the optimization of ANM33 release in foam cells
  27. Primary retroperitoneal angiosarcoma: A case report
  28. Metabolomic analysis-identified 2-hydroxybutyric acid might be a key metabolite of severe preeclampsia
  29. Malignant pleural effusion diagnosis and therapy
  30. Effect of spaceflight on the phenotype and proteome of Escherichia coli
  31. Comparison of immunotherapy combined with stereotactic radiotherapy and targeted therapy for patients with brain metastases: A systemic review and meta-analysis
  32. Activation of hypermethylated P2RY1 mitigates gastric cancer by promoting apoptosis and inhibiting proliferation
  33. Association between the VEGFR-2 -604T/C polymorphism (rs2071559) and type 2 diabetic retinopathy
  34. The role of IL-31 and IL-34 in the diagnosis and treatment of chronic periodontitis
  35. Triple-negative mouse breast cancer initiating cells show high expression of beta1 integrin and increased malignant features
  36. mNGS facilitates the accurate diagnosis and antibiotic treatment of suspicious critical CNS infection in real practice: A retrospective study
  37. The apatinib and pemetrexed combination has antitumor and antiangiogenic effects against NSCLC
  38. Radiotherapy for primary thyroid adenoid cystic carcinoma
  39. Design and functional preliminary investigation of recombinant antigen EgG1Y162–EgG1Y162 against Echinococcus granulosus
  40. Effects of losartan in patients with NAFLD: A meta-analysis of randomized controlled trial
  41. Bibliometric analysis of METTL3: Current perspectives, highlights, and trending topics
  42. Performance comparison of three scaling algorithms in NMR-based metabolomics analysis
  43. PI3K/AKT/mTOR pathway and its related molecules participate in PROK1 silence-induced anti-tumor effects on pancreatic cancer
  44. The altered expression of cytoskeletal and synaptic remodeling proteins during epilepsy
  45. Effects of pegylated recombinant human granulocyte colony-stimulating factor on lymphocytes and white blood cells of patients with malignant tumor
  46. Prostatitis as initial manifestation of Chlamydia psittaci pneumonia diagnosed by metagenome next-generation sequencing: A case report
  47. NUDT21 relieves sevoflurane-induced neurological damage in rats by down-regulating LIMK2
  48. Association of interleukin-10 rs1800896, rs1800872, and interleukin-6 rs1800795 polymorphisms with squamous cell carcinoma risk: A meta-analysis
  49. Exosomal HBV-DNA for diagnosis and treatment monitoring of chronic hepatitis B
  50. Shear stress leads to the dysfunction of endothelial cells through the Cav-1-mediated KLF2/eNOS/ERK signaling pathway under physiological conditions
  51. Interaction between the PI3K/AKT pathway and mitochondrial autophagy in macrophages and the leukocyte count in rats with LPS-induced pulmonary infection
  52. Meta-analysis of the rs231775 locus polymorphism in the CTLA-4 gene and the susceptibility to Graves’ disease in children
  53. Cloning, subcellular localization and expression of phosphate transporter gene HvPT6 of hulless barley
  54. Coptisine mitigates diabetic nephropathy via repressing the NRLP3 inflammasome
  55. Significant elevated CXCL14 and decreased IL-39 levels in patients with tuberculosis
  56. Whole-exome sequencing applications in prenatal diagnosis of fetal bowel dilatation
  57. Gemella morbillorum infective endocarditis: A case report and literature review
  58. An unusual ectopic thymoma clonal evolution analysis: A case report
  59. Severe cumulative skin toxicity during toripalimab combined with vemurafenib following toripalimab alone
  60. Detection of V. vulnificus septic shock with ARDS using mNGS
  61. Novel rare genetic variants of familial and sporadic pulmonary atresia identified by whole-exome sequencing
  62. The influence and mechanistic action of sperm DNA fragmentation index on the outcomes of assisted reproduction technology
  63. Novel compound heterozygous mutations in TELO2 in an infant with You-Hoover-Fong syndrome: A case report and literature review
  64. ctDNA as a prognostic biomarker in resectable CLM: Systematic review and meta-analysis
  65. Diagnosis of primary amoebic meningoencephalitis by metagenomic next-generation sequencing: A case report
  66. Phylogenetic analysis of promoter regions of human Dolichol kinase (DOLK) and orthologous genes using bioinformatics tools
  67. Collagen changes in rabbit conjunctiva after conjunctival crosslinking
  68. Effects of NM23 transfection of human gastric carcinoma cells in mice
  69. Oral nifedipine and phytosterol, intravenous nicardipine, and oral nifedipine only: Three-arm, retrospective, cohort study for management of severe preeclampsia
  70. Case report of hepatic retiform hemangioendothelioma: A rare tumor treated with ultrasound-guided microwave ablation
  71. Curcumin induces apoptosis in human hepatocellular carcinoma cells by decreasing the expression of STAT3/VEGF/HIF-1α signaling
  72. Rare presentation of double-clonal Waldenström macroglobulinemia with pulmonary embolism: A case report
  73. Giant duplication of the transverse colon in an adult: A case report and literature review
  74. Ectopic thyroid tissue in the breast: A case report
  75. SDR16C5 promotes proliferation and migration and inhibits apoptosis in pancreatic cancer
  76. Vaginal metastasis from breast cancer: A case report
  77. Screening of the best time window for MSC transplantation to treat acute myocardial infarction with SDF-1α antibody-loaded targeted ultrasonic microbubbles: An in vivo study in miniswine
  78. Inhibition of TAZ impairs the migration ability of melanoma cells
  79. Molecular complexity analysis of the diagnosis of Gitelman syndrome in China
  80. Effects of maternal calcium and protein intake on the development and bone metabolism of offspring mice
  81. Identification of winter wheat pests and diseases based on improved convolutional neural network
  82. Ultra-multiplex PCR technique to guide treatment of Aspergillus-infected aortic valve prostheses
  83. Virtual high-throughput screening: Potential inhibitors targeting aminopeptidase N (CD13) and PIKfyve for SARS-CoV-2
  84. Immune checkpoint inhibitors in cancer patients with COVID-19
  85. Utility of methylene blue mixed with autologous blood in preoperative localization of pulmonary nodules and masses
  86. Integrated analysis of the microbiome and transcriptome in stomach adenocarcinoma
  87. Berberine suppressed sarcopenia insulin resistance through SIRT1-mediated mitophagy
  88. DUSP2 inhibits the progression of lupus nephritis in mice by regulating the STAT3 pathway
  89. Lung abscess by Fusobacterium nucleatum and Streptococcus spp. co-infection by mNGS: A case series
  90. Genetic alterations of KRAS and TP53 in intrahepatic cholangiocarcinoma associated with poor prognosis
  91. Granulomatous polyangiitis involving the fourth ventricle: Report of a rare case and a literature review
  92. Studying infant mortality: A demographic analysis based on data mining models
  93. Metaplastic breast carcinoma with osseous differentiation: A report of a rare case and literature review
  94. Protein Z modulates the metastasis of lung adenocarcinoma cells
  95. Inhibition of pyroptosis and apoptosis by capsaicin protects against LPS-induced acute kidney injury through TRPV1/UCP2 axis in vitro
  96. TAK-242, a toll-like receptor 4 antagonist, against brain injury by alleviates autophagy and inflammation in rats
  97. Primary mediastinum Ewing’s sarcoma with pleural effusion: A case report and literature review
  98. Association of ADRB2 gene polymorphisms and intestinal microbiota in Chinese Han adolescents
  99. Tanshinone IIA alleviates chondrocyte apoptosis and extracellular matrix degeneration by inhibiting ferroptosis
  100. Study on the cytokines related to SARS-Cov-2 in testicular cells and the interaction network between cells based on scRNA-seq data
  101. Effect of periostin on bone metabolic and autophagy factors during tooth eruption in mice
  102. HP1 induces ferroptosis of renal tubular epithelial cells through NRF2 pathway in diabetic nephropathy
  103. Intravaginal estrogen management in postmenopausal patients with vaginal squamous intraepithelial lesions along with CO2 laser ablation: A retrospective study
  104. Hepatocellular carcinoma cell differentiation trajectory predicts immunotherapy, potential therapeutic drugs, and prognosis of patients
  105. Effects of physical exercise on biomarkers of oxidative stress in healthy subjects: A meta-analysis of randomized controlled trials
  106. Identification of lysosome-related genes in connection with prognosis and immune cell infiltration for drug candidates in head and neck cancer
  107. Development of an instrument-free and low-cost ELISA dot-blot test to detect antibodies against SARS-CoV-2
  108. Research progress on gas signal molecular therapy for Parkinson’s disease
  109. Adiponectin inhibits TGF-β1-induced skin fibroblast proliferation and phenotype transformation via the p38 MAPK signaling pathway
  110. The G protein-coupled receptor-related gene signatures for predicting prognosis and immunotherapy response in bladder urothelial carcinoma
  111. α-Fetoprotein contributes to the malignant biological properties of AFP-producing gastric cancer
  112. CXCL12/CXCR4/CXCR7 axis in placenta tissues of patients with placenta previa
  113. Association between thyroid stimulating hormone levels and papillary thyroid cancer risk: A meta-analysis
  114. Significance of sTREM-1 and sST2 combined diagnosis for sepsis detection and prognosis prediction
  115. Diagnostic value of serum neuroactive substances in the acute exacerbation of chronic obstructive pulmonary disease complicated with depression
  116. Research progress of AMP-activated protein kinase and cardiac aging
  117. TRIM29 knockdown prevented the colon cancer progression through decreasing the ubiquitination levels of KRT5
  118. Cross-talk between gut microbiota and liver steatosis: Complications and therapeutic target
  119. Metastasis from small cell lung cancer to ovary: A case report
  120. The early diagnosis and pathogenic mechanisms of sepsis-related acute kidney injury
  121. The effect of NK cell therapy on sepsis secondary to lung cancer: A case report
  122. Erianin alleviates collagen-induced arthritis in mice by inhibiting Th17 cell differentiation
  123. Loss of ACOX1 in clear cell renal cell carcinoma and its correlation with clinical features
  124. Signalling pathways in the osteogenic differentiation of periodontal ligament stem cells
  125. Crosstalk between lactic acid and immune regulation and its value in the diagnosis and treatment of liver failure
  126. Clinicopathological features and differential diagnosis of gastric pleomorphic giant cell carcinoma
  127. Traumatic brain injury and rTMS-ERPs: Case report and literature review
  128. Extracellular fibrin promotes non-small cell lung cancer progression through integrin β1/PTEN/AKT signaling
  129. Knockdown of DLK4 inhibits non-small cell lung cancer tumor growth by downregulating CKS2
  130. The co-expression pattern of VEGFR-2 with indicators related to proliferation, apoptosis, and differentiation of anagen hair follicles
  131. Inflammation-related signaling pathways in tendinopathy
  132. CD4+ T cell count in HIV/TB co-infection and co-occurrence with HL: Case report and literature review
  133. Clinical analysis of severe Chlamydia psittaci pneumonia: Case series study
  134. Bioinformatics analysis to identify potential biomarkers for the pulmonary artery hypertension associated with the basement membrane
  135. Influence of MTHFR polymorphism, alone or in combination with smoking and alcohol consumption, on cancer susceptibility
  136. Catharanthus roseus (L.) G. Don counteracts the ampicillin resistance in multiple antibiotic-resistant Staphylococcus aureus by downregulation of PBP2a synthesis
  137. Combination of a bronchogenic cyst in the thoracic spinal canal with chronic myelocytic leukemia
  138. Bacterial lipoprotein plays an important role in the macrophage autophagy and apoptosis induced by Salmonella typhimurium and Staphylococcus aureus
  139. TCL1A+ B cells predict prognosis in triple-negative breast cancer through integrative analysis of single-cell and bulk transcriptomic data
  140. Ezrin promotes esophageal squamous cell carcinoma progression via the Hippo signaling pathway
  141. Ferroptosis: A potential target of macrophages in plaque vulnerability
  142. Predicting pediatric Crohn's disease based on six mRNA-constructed risk signature using comprehensive bioinformatic approaches
  143. Applications of genetic code expansion and photosensitive UAAs in studying membrane proteins
  144. HK2 contributes to the proliferation, migration, and invasion of diffuse large B-cell lymphoma cells by enhancing the ERK1/2 signaling pathway
  145. IL-17 in osteoarthritis: A narrative review
  146. Circadian cycle and neuroinflammation
  147. Probiotic management and inflammatory factors as a novel treatment in cirrhosis: A systematic review and meta-analysis
  148. Hemorrhagic meningioma with pulmonary metastasis: Case report and literature review
  149. SPOP regulates the expression profiles and alternative splicing events in human hepatocytes
  150. Knockdown of SETD5 inhibited glycolysis and tumor growth in gastric cancer cells by down-regulating Akt signaling pathway
  151. PTX3 promotes IVIG resistance-induced endothelial injury in Kawasaki disease by regulating the NF-κB pathway
  152. Pancreatic ectopic thyroid tissue: A case report and analysis of literature
  153. The prognostic impact of body mass index on female breast cancer patients in underdeveloped regions of northern China differs by menopause status and tumor molecular subtype
  154. Report on a case of liver-originating malignant melanoma of unknown primary
  155. Case report: Herbal treatment of neutropenic enterocolitis after chemotherapy for breast cancer
  156. The fibroblast growth factor–Klotho axis at molecular level
  157. Characterization of amiodarone action on currents in hERG-T618 gain-of-function mutations
  158. A case report of diagnosis and dynamic monitoring of Listeria monocytogenes meningitis with NGS
  159. Effect of autologous platelet-rich plasma on new bone formation and viability of a Marburg bone graft
  160. Small breast epithelial mucin as a useful prognostic marker for breast cancer patients
  161. Continuous non-adherent culture promotes transdifferentiation of human adipose-derived stem cells into retinal lineage
  162. Nrf3 alleviates oxidative stress and promotes the survival of colon cancer cells by activating AKT/BCL-2 signal pathway
  163. Favorable response to surufatinib in a patient with necrolytic migratory erythema: A case report
  164. Case report of atypical undernutrition of hypoproteinemia type
  165. Down-regulation of COL1A1 inhibits tumor-associated fibroblast activation and mediates matrix remodeling in the tumor microenvironment of breast cancer
  166. Sarcoma protein kinase inhibition alleviates liver fibrosis by promoting hepatic stellate cells ferroptosis
  167. Research progress of serum eosinophil in chronic obstructive pulmonary disease and asthma
  168. Clinicopathological characteristics of co-existing or mixed colorectal cancer and neuroendocrine tumor: Report of five cases
  169. Role of menopausal hormone therapy in the prevention of postmenopausal osteoporosis
  170. Precisional detection of lymph node metastasis using tFCM in colorectal cancer
  171. Advances in diagnosis and treatment of perimenopausal syndrome
  172. A study of forensic genetics: ITO index distribution and kinship judgment between two individuals
  173. Acute lupus pneumonitis resembling miliary tuberculosis: A case-based review
  174. Plasma levels of CD36 and glutathione as biomarkers for ruptured intracranial aneurysm
  175. Fractalkine modulates pulmonary angiogenesis and tube formation by modulating CX3CR1 and growth factors in PVECs
  176. Novel risk prediction models for deep vein thrombosis after thoracotomy and thoracoscopic lung cancer resections, involving coagulation and immune function
  177. Exploring the diagnostic markers of essential tremor: A study based on machine learning algorithms
  178. Evaluation of effects of small-incision approach treatment on proximal tibia fracture by deep learning algorithm-based magnetic resonance imaging
  179. An online diagnosis method for cancer lesions based on intelligent imaging analysis
  180. Medical imaging in rheumatoid arthritis: A review on deep learning approach
  181. Predictive analytics in smart healthcare for child mortality prediction using a machine learning approach
  182. Utility of neutrophil–lymphocyte ratio and platelet–lymphocyte ratio in predicting acute-on-chronic liver failure survival
  183. A biomedical decision support system for meta-analysis of bilateral upper-limb training in stroke patients with hemiplegia
  184. TNF-α and IL-8 levels are positively correlated with hypobaric hypoxic pulmonary hypertension and pulmonary vascular remodeling in rats
  185. Stochastic gradient descent optimisation for convolutional neural network for medical image segmentation
  186. Comparison of the prognostic value of four different critical illness scores in patients with sepsis-induced coagulopathy
  187. Application and teaching of computer molecular simulation embedded technology and artificial intelligence in drug research and development
  188. Hepatobiliary surgery based on intelligent image segmentation technology
  189. Value of brain injury-related indicators based on neural network in the diagnosis of neonatal hypoxic-ischemic encephalopathy
  190. Analysis of early diagnosis methods for asymmetric dementia in brain MR images based on genetic medical technology
  191. Early diagnosis for the onset of peri-implantitis based on artificial neural network
  192. Clinical significance of the detection of serum IgG4 and IgG4/IgG ratio in patients with thyroid-associated ophthalmopathy
  193. Forecast of pain degree of lumbar disc herniation based on back propagation neural network
  194. SPA-UNet: A liver tumor segmentation network based on fused multi-scale features
  195. Systematic evaluation of clinical efficacy of CYP1B1 gene polymorphism in EGFR mutant non-small cell lung cancer observed by medical image
  196. Rehabilitation effect of intelligent rehabilitation training system on hemiplegic limb spasms after stroke
  197. A novel approach for minimising anti-aliasing effects in EEG data acquisition
  198. ErbB4 promotes M2 activation of macrophages in idiopathic pulmonary fibrosis
  199. Clinical role of CYP1B1 gene polymorphism in prediction of postoperative chemotherapy efficacy in NSCLC based on individualized health model
  200. Lung nodule segmentation via semi-residual multi-resolution neural networks
  201. Evaluation of brain nerve function in ICU patients with Delirium by deep learning algorithm-based resting state MRI
  202. A data mining technique for detecting malignant mesothelioma cancer using multiple regression analysis
  203. Markov model combined with MR diffusion tensor imaging for predicting the onset of Alzheimer’s disease
  204. Effectiveness of the treatment of depression associated with cancer and neuroimaging changes in depression-related brain regions in patients treated with the mediator-deuterium acupuncture method
  205. Molecular mechanism of colorectal cancer and screening of molecular markers based on bioinformatics analysis
  206. Monitoring and evaluation of anesthesia depth status data based on neuroscience
  207. Exploring the conformational dynamics and thermodynamics of EGFR S768I and G719X + S768I mutations in non-small cell lung cancer: An in silico approaches
  208. Optimised feature selection-driven convolutional neural network using gray level co-occurrence matrix for detection of cervical cancer
  209. Incidence of different pressure patterns of spinal cerebellar ataxia and analysis of imaging and genetic diagnosis
  210. Pathogenic bacteria and treatment resistance in older cardiovascular disease patients with lung infection and risk prediction model
  211. Adoption value of support vector machine algorithm-based computed tomography imaging in the diagnosis of secondary pulmonary fungal infections in patients with malignant hematological disorders
  212. From slides to insights: Harnessing deep learning for prognostic survival prediction in human colorectal cancer histology
  213. Ecology and Environmental Science
  214. Monitoring of hourly carbon dioxide concentration under different land use types in arid ecosystem
  215. Comparing the differences of prokaryotic microbial community between pit walls and bottom from Chinese liquor revealed by 16S rRNA gene sequencing
  216. Effects of cadmium stress on fruits germination and growth of two herbage species
  217. Bamboo charcoal affects soil properties and bacterial community in tea plantations
  218. Optimization of biogas potential using kinetic models, response surface methodology, and instrumental evidence for biodegradation of tannery fleshings during anaerobic digestion
  219. Understory vegetation diversity patterns of Platycladus orientalis and Pinus elliottii communities in Central and Southern China
  220. Studies on macrofungi diversity and discovery of new species of Abortiporus from Baotianman World Biosphere Reserve
  221. Food Science
  222. Effect of berrycactus fruit (Myrtillocactus geometrizans) on glutamate, glutamine, and GABA levels in the frontal cortex of rats fed with a high-fat diet
  223. Guesstimate of thymoquinone diversity in Nigella sativa L. genotypes and elite varieties collected from Indian states using HPTLC technique
  224. Analysis of bacterial community structure of Fuzhuan tea with different processing techniques
  225. Untargeted metabolomics reveals sour jujube kernel benefiting the nutritional value and flavor of Morchella esculenta
  226. Mycobiota in Slovak wine grapes: A case study from the small Carpathians wine region
  227. Elemental analysis of Fadogia ancylantha leaves used as a nutraceutical in Mashonaland West Province, Zimbabwe
  228. Microbiological transglutaminase: Biotechnological application in the food industry
  229. Influence of solvent-free extraction of fish oil from catfish (Clarias magur) heads using a Taguchi orthogonal array design: A qualitative and quantitative approach
  230. Chromatographic analysis of the chemical composition and anticancer activities of Curcuma longa extract cultivated in Palestine
  231. The potential for the use of leghemoglobin and plant ferritin as sources of iron
  232. Investigating the association between dietary patterns and glycemic control among children and adolescents with T1DM
  233. Bioengineering and Biotechnology
  234. Biocompatibility and osteointegration capability of β-TCP manufactured by stereolithography 3D printing: In vitro study
  235. Clinical characteristics and the prognosis of diabetic foot in Tibet: A single center, retrospective study
  236. Agriculture
  237. Biofertilizer and NPSB fertilizer application effects on nodulation and productivity of common bean (Phaseolus vulgaris L.) at Sodo Zuria, Southern Ethiopia
  238. On correlation between canopy vegetation and growth indexes of maize varieties with different nitrogen efficiencies
  239. Exopolysaccharides from Pseudomonas tolaasii inhibit the growth of Pleurotus ostreatus mycelia
  240. A transcriptomic evaluation of the mechanism of programmed cell death of the replaceable bud in Chinese chestnut
  241. Melatonin enhances salt tolerance in sorghum by modulating photosynthetic performance, osmoregulation, antioxidant defense, and ion homeostasis
  242. Effects of plant density on alfalfa (Medicago sativa L.) seed yield in western Heilongjiang areas
  243. Identification of rice leaf diseases and deficiency disorders using a novel DeepBatch technique
  244. Artificial intelligence and internet of things oriented sustainable precision farming: Towards modern agriculture
  245. Animal Sciences
  246. Effect of ketogenic diet on exercise tolerance and transcriptome of gastrocnemius in mice
  247. Combined analysis of mRNA–miRNA from testis tissue in Tibetan sheep with different FecB genotypes
  248. Isolation, identification, and drug resistance of a partially isolated bacterium from the gill of Siniperca chuatsi
  249. Tracking behavioral changes of confined sows from the first mating to the third parity
  250. The sequencing of the key genes and end products in the TLR4 signaling pathway from the kidney of Rana dybowskii exposed to Aeromonas hydrophila
  251. Development of a new candidate vaccine against piglet diarrhea caused by Escherichia coli
  252. Plant Sciences
  253. Crown and diameter structure of pure Pinus massoniana Lamb. forest in Hunan province, China
  254. Genetic evaluation and germplasm identification analysis on ITS2, trnL-F, and psbA-trnH of alfalfa varieties germplasm resources
  255. Tissue culture and rapid propagation technology for Gentiana rhodantha
  256. Effects of cadmium on the synthesis of active ingredients in Salvia miltiorrhiza
  257. Cloning and expression analysis of VrNAC13 gene in mung bean
  258. Chlorate-induced molecular floral transition revealed by transcriptomes
  259. Effects of warming and drought on growth and development of soybean in Hailun region
  260. Effects of different light conditions on transient expression and biomass in Nicotiana benthamiana leaves
  261. Comparative analysis of the rhizosphere microbiome and medicinally active ingredients of Atractylodes lancea from different geographical origins
  262. Distinguish Dianthus species or varieties based on chloroplast genomes
  263. Comparative transcriptomes reveal molecular mechanisms of apple blossoms of different tolerance genotypes to chilling injury
  264. Study on fresh processing key technology and quality influence of Cut Ophiopogonis Radix based on multi-index evaluation
  265. An advanced approach for fig leaf disease detection and classification: Leveraging image processing and enhanced support vector machine methodology
  266. Erratum
  267. Erratum to “Protein Z modulates the metastasis of lung adenocarcinoma cells”
  268. Erratum to “BRCA1 subcellular localization regulated by PI3K signaling pathway in triple-negative breast cancer MDA-MB-231 cells and hormone-sensitive T47D cells”
  269. Retraction
  270. Retraction to “Protocatechuic acid attenuates cerebral aneurysm formation and progression by inhibiting TNF-alpha/Nrf-2/NF-kB-mediated inflammatory mechanisms in experimental rats”
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Heruntergeladen am 6.9.2025 von https://www.degruyterbrill.com/document/doi/10.1515/biol-2022-0712/html?lang=de
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