Home IgG4-related disease complicated by PLA2R-associated membranous nephropathy: A case report
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IgG4-related disease complicated by PLA2R-associated membranous nephropathy: A case report

  • Meichun Huang EMAIL logo , Jun Liu and Xiuxiu Li
Published/Copyright: July 25, 2024
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Open Life Sciences
From the journal Open Life Sciences Volume 19 Issue 1

Abstract

IgG4-related tubulointerstitial nephritis (IgG4-related TIN) is the prevalent clinical manifestation of IgG4-related diseases (IgG4-RD). However, there are limited cases of IgG4-RD occurring with membranous nephropathy (MN) in the absence of phospholipase A2 receptor (PLA2R). There have been no indications of treatment using Tripterygium wilfordii. This study reported a rare case of IgG4-RD with PLA2R-associated MN without any of the distinct IgG4-related TIN. The patient was treated effectively with T. wilfordii. A 71-year-old patient was admitted to the medical facility after presenting with a 1 month history of edema and 8 months of albuminuria. The renal biopsy tissue examination confirmed the presence of MN (phase II) in the absence of pathological manifestations of IgG4-related TIN. Immunohistochemistry identified PLA2R++ (granular capillaries). The serum PLA2R antibody titer was 1:180 (1:20). The patient met the diagnosis with IgG4-RD. Over 8 years of follow-up, the patient was effectively treated with low-dose hormones and T. wilfordii, without any adverse effects. This MN is considered a unique form of IgG4-RD, regardless of whether PLA2R antibodies are present or not. Research suggests that T. wilfordii could be a promising option for elderly people with IgG4-related MN, as it has been found to have fewer adverse effects.

Keywords: IgG4-related disease; IgG4-related kidney disease; membranous nephropathy; phospholipase A2 receptor; Tripterygium wilfordii

1 Introduction

IgG4-related diseases (IgG4-RD) are systemic disorders that can impact a wide range of organs. The diagnostic criteria for IgG4-RD were initially suggested in 2011, and then, an IgG4-RD classification system was introduced in 2019 [1,2]. IgG4-related tubulointerstitial nephritis (IgG4-related TIN) is the most common manifestation of kidney injury, characterized by dense lymphoplasmacytic infiltration (≥10 IgG4+ plasma cells/HP) and/or an IgG4+/IgG+ plasma cell ratio of ≥40%. There is limited evidence of IgG4-RD presenting with membranous nephropathy (MN), which is frequently accompanied by IgG4-TIN and is characterized without phospholipase A2 receptor (PLA2R) expression [1,2].

The understanding of IgG4-RD is constantly expanding, accompanied by investigations into their diagnosis and treatment. The link between these diseases and renal damage is complex. Multifactorial factors frequently contribute to the increasing prevalence of MN, which is recognized as an immune-related disease. In this report, a highly rare case of an IgG4-RD with PLA2R-associated MN was presented, which lacks the typical IgG4-related TIN. During the 8-year follow-up period, the patient experienced no recurrence or adverse effects after being treated with low-dose hormones in combination with Tripterygium wilfordii. The diagnosis of IgG4-RD in this patient was challenging and two diagnostic criteria were used. IgG4-RD was predicated upon the first criterion, whereas the diagnosis met the requirements of the second criterion. The diagnosis of IgG4-RD, the relationship between IgG4-RD and MN, and the role of PLA2R antibodies are also reviewed. More specifically among elderly patients, T. wilfordii is found to have therapeutic effects.

2 Case report

A 71-year old male was admitted to the Nephrology Department on March 4, 2015, due to albuminuria persisting for 8 months and edema for 1 month, along with symptoms of fatigue, dry mouth, and polydipsia. Urine analysis showed red blood cells 1–3/HP, protein+++, and proteinuria 3500.00 mg/day. Serum analysis revealed albumin 24.4 g/L, creatinine 79 μmol/L (40–83 μmol/L), IgA: 1.74 g/L, IgM: 1.21 g/L, IgG: 20.68 g/L (7–16.00), IgG4: 9.95 g/L (0.03–2.01), IgG4/IgG: 48.11%, C3: 0.38 g/L (0.79–1.52), and C4: 0.04 g/L (0.16–0.38). The PLA2R antibody titer in serum was 1:180 (1:20). Changes in bilateral parotid echo were detected via ultrasound, whereas abdominal CT and enhanced MRI revealed that both the body and tail of the pancreas were enlarged. Blood eosinophils and IgE, thyroid function, tumor markers, antinuclear antibodies, and routine bone marrow tests were normal. The immunofluorescence for renal biopathology was examined on March 25, 2015. The main findings were as follows: 3 glomeruli, IgG+ (capillaries), C3++ (capillaries), IgM++ (capillaries), C1q++ (capillaries), IgA−, Fg−, and C4−. The light microscopy analysis revealed 29 glomeruli, of which 5 showed glomerulosclerosis and the remaining 29 displayed mild hyperplasia of the mesangial tissue, basement membrane thickening, double tracks, nail processes, renal tubule atrophy, rare interstitial fibrous tissue hyperplasia, and inflammatory cell infiltration (≤5%) (Figure 1). Diffuse fusion of foot processes, basement membrane hypertrophy, mesangial matrix enlargement, and accumulation of electron-dense matter beneath the epithelium, within the basement membrane, and in the mesangial region were all observed via electron microscopy. Immunohistochemistry showed HBsAg (−), HBcAg (−), K (−), L (−), focal distribution of CD138-positive plasma cells in the renal interstitium with an average of 18/Hp, IgG4-positive plasma cells < 10/Hp (Figure 2), and PLA2R++ (capillaries, granular) (Figure 3). The pathological symptoms of IgG4-related TIN were not indicated by the diagnosis of MN (phase II).

Figure 1 Histopathological examination of the kidney reveals MN via periodic acid Schiff-methenamine staining (400×).
Figure 1

Histopathological examination of the kidney reveals MN via periodic acid Schiff-methenamine staining (400×).

Figure 2 Immunohistochemical analysis of IgG4+ plasma cells < 10/high power field (Hp) (400×).
Figure 2

Immunohistochemical analysis of IgG4+ plasma cells < 10/high power field (Hp) (400×).

Figure 3 Immunohistochemical analysis of the kidney reveals PLA2R++ (400×).
Figure 3

Immunohistochemical analysis of the kidney reveals PLA2R++ (400×).

Based on the patient’s clinical symptoms (dry mouth and excessive drinking, bilateral abnormalities in the parotid glands, significant enlargement of the pancreas, increased serum IgG4 level, and hypocomplementemia), the patient met all inclusion and exclusion criteria and obtained a total score of 26 points (≥20 points) on the IgG4-RD classification standard. Thus, a clinical diagnosis of IgG4-RD was determined by the classification criteria of the European League Against Rheumatology and the American College of Rheumatology. This led to the diagnosis of IgG4-RD in combination with MN for the patient. The patient received prednisone (20 mg/day) treatment on March 5, 2015. IgG4 levels had decreased to 4.77 g/L, while serum IgG and parotid gland levels had returned to normal after 3 months. However, the nephrotic syndrome remained unresolved. After this, the patient was prescribed a daily dose of prednisone (20 mg) along with T. wilfordii (30 mg). After 2 months, the urine protein test was negative, which led to a gradual decrease in dosage. Finally, a daily dose of prednisone (5 mg) and T. wilfordii (10 mg) was given and continued, until it was stopped 1 year ago (Figure 4). The serum anti-PlA2R became negative. All clinical indicators remained within normal ranges in the 8-year follow-up period.

Figure 4 Disease progression is monitored by quantifying serum proteinuria, serum albumin, serum IgG4 level, serum IgG level, and serum C3 level. T. wilfordii were administered after the initiation of prednisolone therapy. W = week.
Figure 4

Disease progression is monitored by quantifying serum proteinuria, serum albumin, serum IgG4 level, serum IgG level, and serum C3 level. T. wilfordii were administered after the initiation of prednisolone therapy. W = week.

  1. Informed consent: Informed consent has been obtained from all individuals included in this study.

  2. Ethical approval: The research related to human use has been complied with all the relevant national regulations, institutional policies and in accordance with the tenets of the Helsinki Declaration, and has been approved by the authors’ institutional review board or equivalent committee.

3 Discussion

Based on the diagnostic criteria from 2011, the patient was identified as having suspected IgG4-RD during his 2015 visit. However, the diagnosis of IgG4-RD remained possible following 8 years of follow-up observation and the use of the 2019 revised classification criteria. However, the patient also developed nephrotic syndrome, which was characterized by the pathological presentation of MN but lacked evidence of IgG4-TIN. There was a positive finding of PLA2R in both the serum and renal tissue, while electron microscopy revealed the presence of electron-dense deposition commonly observed in atypical MN.

Currently, there is a gradual increase in the incidence rate of MN in glomerular diseases. Despite secondary MN is frequently observed as a pathological symptom, its underlying cause is often unclear. Based on the results, the serum anti-PLA2R antibody level showed remarkable sensitivity (68%) and specificity (97%) in differentiating primary and secondary MN. The PLA2R antibody level is a characteristic indicator of primary MN with low positivity in secondary MN [3–5]. Recently, there have been a few reports of IgG4-RD associated with MN, which may be IgG4-related MN. Most of these cases are negative for PLA2R antibodies, and IgG4-TIN often occurs simultaneously or progressively. Peking University Hospital reported 42 patients with IgG4-related kidney disease (IgG4-RKD), with an average age of 58.5 ± 8.7 years (male to female ratio = 5:1). Among them, 66.7% showed acute kidney injury. IgG4-related TIN was identified in 40 patients, of which 19 (47.5%) had concurrent glomerular pathologies. The patients with MN received prednisone (0.5–1.0 mg/kg/day) and or combined with Cyclophosphamide or Cyclosporine. In another study, IgG4-related TIN and MN were observed in 27.4% of the patients. IgG4-related MN can have rare manifestations associated with tumors, monoclonal globulinemia, systemic lupus erythematosus, and secondary infection with the EB virus. The etiology of IgG4-related MN remains largely unknown [6,7].

Most patients with IgG4-related MN are negative for anti-PLA2R, with rare reports of anti-PLA2R-positivity. A patient who had previously experienced pancreatitis associated with IgG4 was admitted to the hospital with nephrotic syndrome; upon pathological examination, positive serum anti-PLA2R antibody levels indicated MN without interstitial nephritis. The patient was treated with hormones combined with Cyclophosphamide. A case of pancreatic and liver damage with typical IgG4-RD was reported. MN developed nephrotic syndrome during the active phase of the disease 5 months later. Serum and renal tissue were both positive for anti-PLA2R via immunofluorescent analysis. MN experienced relief after Rituximab treatment. A 55-year-old woman was reported to have been diagnosed with MN in combination with IgG4-RD in the absence of interstitial nephritis in 2022. The renal tissue was positive for anti-PLA2R. Despite a reduction in IgG4 levels after hormone therapy, the nephrotic syndrome persisted and was effectively treated with Obinutuzumab [8,9].

These patients were diagnosed with IgG4-RD concurrent with PLA2R-related MN, without interstitial nephritis. It is evident from these patients that PLA2R-associated MN may occur either after IgG4-RD or at the same time, without interstitial nephritis generally. The efficacy of hormone therapy alone is not satisfactory. However, after immunosuppression or combined treatment with biological agents, the prognosis may be good.

Currently, it is challenging to determine if the associated MN indicates idiopathic PLA2R-related MN or IgG4-related MN.

What is the mechanism between PLA2R-related MN and IgG4-RD? There is a genetic predisposition to the primary MN, with a genetic interaction of a locus in or near an enhancer region of the PLA2R1 gene itself and the larger class II major histocompatibility complex locus. PLA2R was expressed by normal human podocytes. In disease, PLA2R binds to their in situ or circulating immune complexes on the podocyte, leading to the accumulation of immune complexes, which cause gradual accumulation of the deposits beneath the podocyte (in a subepithelial position). It is not clear why this occurs in discrete areas, leading to more complexes in some locations but not others. The clinical utility of the identification of PLA2R is not only a specific way to diagnose PLA2R-related MN [4,5] but also the prediction of the subsequent clinical course. The formation of immune complexes with IgG4 seems likely to be described in rheumatoid arthritis, IgG4-RD, and MN. The pathogenesis of IgG4-RD assumes the increased activity of T regulatory cells with overexpression of IL-10, production of transforming growth factor-β, and upregulation of Th2 response, in which interleukins 4, 5, and 13 play predominant roles. These cytokines translate into specific pathophysiological phenomena such as the activation of B cells and plasma cells to IgG4 production. So, B- and T-cells are vital to disease pathogenesis [1,5]. The mechanism is unclear in which PLA2R-immune complexes are activated in the pathological process of IgG4-related MN.

We present a rare case of PLA2R-associated MN concomitant with IgG4-RD. However, electron-dense subepithelial, endosubcutaneous, and mesangial deposits suggested a secondary etiology for MN.

During the 8 years follow-up, the patient did not develop any membranous kidney-related tumors, poisoning, thyroid diseases, or infections. With the remission of IgG4-RD disease, nephrotic syndrome did not recur and the PLA2R titer did not increase again. Previous studies showed the presence of deposits in the subendothelial or mesangial regions, or both, in people with IgG4-related MN. Therefore, although the present case was PLA2R-positive, it is believed that the MN may be a secondary IgG4-RD. In IgG4-RD, serum IgG4 levels decline after B cell depletion but do not normalize, probably because of the long-lived plasma cells that continue to produce it, which results in persistently elevated immunoglobulin. Therefore, the patient’s treatment with only hormone therapy is ineffective. However, a significant improvement resulting in complete remission without recurrence, was noted after T. wilfordii treatment.

Polyglycosides from T. wilfordii are extracted from the root core, which has been widely used for the treatment of IgA nephropathy, MN, and diabetic nephropathy, as well as rheumatoid arthritis, systemic lupus erythematosus, and other immune diseases [10–12]. The therapeutic activity of T. wilfordii triptolide is mediated by the PI3K/AKT/mTOR pathway to alleviate membranous nephropathy [13]. Molecular biological research on the treatment of MN with Tripterygium glycosides, according to the principles of traditional Chinese medicine, the effects of treatment with Tripterygium glycosides mainly involves the AGE-RAGE signaling pathway, lipids and atherosclerosis, the IL-17 signaling pathway, fluid shear stress, atherosclerosis, and the NF-κB signaling pathway to regulate the release of inflammatory factors and T cell proliferation [13–15]. Tipterygium glycosides can also suppress the Toll-like receptor 4 pathway, while triptolide can inhibit both cell proliferation and inflammatory cytokine expression in IL-6/sIL-6R-stimulated fibroblast-like synoviocytes by suppressing JAK2/STAT3 signaling and reduce the levels of TNF-α, IL-8, CXCL2, and VEGF [12,15,16]. After treatment of patients with chronic nephritis with T. wilfordii polyglycoside tablets, both the CD4+ and CD4+/CD8+ ratios increased, while that of CD8+ decreased [17]. Triptolide reduced podocyte injury via microRNA-155-5p/brain-derived neurotrophic factor [11]. T. wilfordii was effective in preventing T cell proliferation and regulated the balance of Tfr/Tfh through inhibiting proliferating B cells [18]. Tripterygium glycosides can improve abnormal lipid deposition in nephrotic syndrome, and decrease renal oxidative damage and apoptosis [19]. So, T. wilfordii has a potential multi-component, multi-target, and multi-pathway molecular mechanism of action for the treatment of MN [20]. According to a study on the efficacy and safety of T. wilfordii multiglycosides in idiopathic membranous nephropathy, the reported incidence of reproductive toxicity and hepatotoxicity among users of T. wilfordii multiglycoside tablets (1–1.5 mg/kg body weight/day, orally, divided to three doses) was less [21,22]. Even the adverse effects were mild and reversible. The use of excessive doses is the main cause of adverse effects. We selected a 30 mg/day low-dose treatment, which has no adverse effects and has good clinical efficacy.

4 Conclusion

This study concluded that MN is a unique form of IgG4-RD, irrespective of whether PLA2R antibodies are present or not. Studies suggest that T. wilfordii could offer potential benefits for elderly people with IgG4-MN, due to its therapeutic impact and reduced risk of side effects.

Acknowledgements

The authors thank the patient for consenting us to publish his case data to write this article. They also acknowledge the contributions of the colleagues in the renal department of Tongde Hospital of Zhejiang Province that aided the efforts of the authors. The authors specially acknowledge the director of the renal department, Ying Lu, for her help.

  1. Funding information: Authors state no funding involved.

  2. Author contributions: M.H. contributed to the conception of the study and wrote, reviewed, and revised the manuscript; J.L. was responsible for analysis and interpretation of kidney pathology and preparation of pathological data; and X.L. contributed significantly to the analysis and preparation of clinical data.

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

  4. Data availability statement: The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Received: 2024-02-24
Revised: 2024-06-04
Accepted: 2024-06-17
Published Online: 2024-07-25

© 2024 the author(s), published by De Gruyter

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

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  105. The expression and clinical significance of syncytin-1 in serum exosomes of hepatocellular carcinoma patients
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  111. Heterogeneous nuclear ribonucleoprotein K is a potential target for enhancing the chemosensitivity of nasopharyngeal carcinoma
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  113. Anti-γ-aminobutyric acid-B receptor autoimmune encephalitis with syncope as the initial symptom: Case report and literature review
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  115. Human umbilical cord mesenchymal stem cells regulate glutathione metabolism depending on the ERK–Nrf2–HO-1 signal pathway to repair phosphoramide mustard-induced ovarian cancer cells
  116. Electroacupuncture on GB acupoints improves osteoporosis via the estradiol–PI3K–Akt signaling pathway
  117. Renalase protects against podocyte injury by inhibiting oxidative stress and apoptosis in diabetic nephropathy
  118. Review: Dicranostigma leptopodum: A peculiar plant of Papaveraceae
  119. Combination effect of flavonoids attenuates lung cancer cell proliferation by inhibiting the STAT3 and FAK signaling pathway
  120. Renal microangiopathy and immune complex glomerulonephritis induced by anti-tumour agents: A case report
  121. Correlation analysis of AVPR1a and AVPR2 with abnormal water and sodium and potassium metabolism in rats
  122. Gastrointestinal health anti-diarrheal mixture relieves spleen deficiency-induced diarrhea through regulating gut microbiota
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  124. Exploring the effects of culture conditions on Yapsin (YPS) gene expression in Nakaseomyces glabratus
  125. Screening of prognostic core genes based on cell–cell interaction in the peripheral blood of patients with sepsis
  126. Coagulation factor II thrombin receptor as a promising biomarker in breast cancer management
  127. Ileocecal mucinous carcinoma misdiagnosed as incarcerated hernia: A case report
  128. Methyltransferase like 13 promotes malignant behaviors of bladder cancer cells through targeting PI3K/ATK signaling pathway
  129. The debate between electricity and heat, efficacy and safety of irreversible electroporation and radiofrequency ablation in the treatment of liver cancer: A meta-analysis
  130. ZAG promotes colorectal cancer cell proliferation and epithelial–mesenchymal transition by promoting lipid synthesis
  131. Baicalein inhibits NLRP3 inflammasome activation and mitigates placental inflammation and oxidative stress in gestational diabetes mellitus
  132. Impact of SWCNT-conjugated senna leaf extract on breast cancer cells: A potential apoptotic therapeutic strategy
  133. MFAP5 inhibits the malignant progression of endometrial cancer cells in vitro
  134. Major ozonated autohemotherapy promoted functional recovery following spinal cord injury in adult rats via the inhibition of oxidative stress and inflammation
  135. Axodendritic targeting of TAU and MAP2 and microtubule polarization in iPSC-derived versus SH-SY5Y-derived human neurons
  136. Differential expression of phosphoinositide 3-kinase/protein kinase B and Toll-like receptor/nuclear factor kappa B signaling pathways in experimental obesity Wistar rat model
  137. The therapeutic potential of targeting Oncostatin M and the interleukin-6 family in retinal diseases: A comprehensive review
  138. BA inhibits LPS-stimulated inflammatory response and apoptosis in human middle ear epithelial cells by regulating the Nf-Kb/Iκbα axis
  139. Role of circRMRP and circRPL27 in chronic obstructive pulmonary disease
  140. Investigating the role of hyperexpressed HCN1 in inducing myocardial infarction through activation of the NF-κB signaling pathway
  141. Characterization of phenolic compounds and evaluation of anti-diabetic potential in Cannabis sativa L. seeds: In vivo, in vitro, and in silico studies
  142. Quantitative immunohistochemistry analysis of breast Ki67 based on artificial intelligence
  143. Ecology and Environmental Science
  144. Screening of different growth conditions of Bacillus subtilis isolated from membrane-less microbial fuel cell toward antimicrobial activity profiling
  145. Degradation of a mixture of 13 polycyclic aromatic hydrocarbons by commercial effective microorganisms
  146. Evaluation of the impact of two citrus plants on the variation of Panonychus citri (Acari: Tetranychidae) and beneficial phytoseiid mites
  147. Prediction of present and future distribution areas of Juniperus drupacea Labill and determination of ethnobotany properties in Antalya Province, Türkiye
  148. Population genetics of Todarodes pacificus (Cephalopoda: Ommastrephidae) in the northwest Pacific Ocean via GBS sequencing
  149. A comparative analysis of dendrometric, macromorphological, and micromorphological characteristics of Pistacia atlantica subsp. atlantica and Pistacia terebinthus in the middle Atlas region of Morocco
  150. Macrofungal sporocarp community in the lichen Scots pine forests
  151. Assessing the proximate compositions of indigenous forage species in Yemen’s pastoral rangelands
  152. Food Science
  153. Gut microbiota changes associated with low-carbohydrate diet intervention for obesity
  154. Reexamination of Aspergillus cristatus phylogeny in dark tea: Characteristics of the mitochondrial genome
  155. Differences in the flavonoid composition of the leaves, fruits, and branches of mulberry are distinguished based on a plant metabolomics approach
  156. Investigating the impact of wet rendering (solventless method) on PUFA-rich oil from catfish (Clarias magur) viscera
  157. Non-linear associations between cardiovascular metabolic indices and metabolic-associated fatty liver disease: A cross-sectional study in the US population (2017–2020)
  158. Knockdown of USP7 alleviates atherosclerosis in ApoE-deficient mice by regulating EZH2 expression
  159. Utility of dairy microbiome as a tool for authentication and traceability
  160. Agriculture
  161. Enhancing faba bean (Vicia faba L.) productivity through establishing the area-specific fertilizer rate recommendation in southwest Ethiopia
  162. Impact of novel herbicide based on synthetic auxins and ALS inhibitor on weed control
  163. Perspectives of pteridophytes microbiome for bioremediation in agricultural applications
  164. Fertilizer application parameters for drip-irrigated peanut based on the fertilizer effect function established from a “3414” field trial
  165. Improving the productivity and profitability of maize (Zea mays L.) using optimum blended inorganic fertilization
  166. Application of leaf multispectral analyzer in comparison to hyperspectral device to assess the diversity of spectral reflectance indices in wheat genotypes
  167. Animal Sciences
  168. Knockdown of ANP32E inhibits colorectal cancer cell growth and glycolysis by regulating the AKT/mTOR pathway
  169. Development of a detection chip for major pathogenic drug-resistant genes and drug targets in bovine respiratory system diseases
  170. Exploration of the genetic influence of MYOT and MB genes on the plumage coloration of Muscovy ducks
  171. Transcriptome analysis of adipose tissue in grazing cattle: Identifying key regulators of fat metabolism
  172. Comparison of nutritional value of the wild and cultivated spiny loaches at three growth stages
  173. Transcriptomic analysis of liver immune response in Chinese spiny frog (Quasipaa spinosa) infected with Proteus mirabilis
  174. Disruption of BCAA degradation is a critical characteristic of diabetic cardiomyopathy revealed by integrated transcriptome and metabolome analysis
  175. Plant Sciences
  176. Effect of long-term in-row branch covering on soil microorganisms in pear orchards
  177. Photosynthetic physiological characteristics, growth performance, and element concentrations reveal the calcicole–calcifuge behaviors of three Camellia species
  178. Transcriptome analysis reveals the mechanism of NaHCO3 promoting tobacco leaf maturation
  179. Bioinformatics, expression analysis, and functional verification of allene oxide synthase gene HvnAOS1 and HvnAOS2 in qingke
  180. Water, nitrogen, and phosphorus coupling improves gray jujube fruit quality and yield
  181. Improving grape fruit quality through soil conditioner: Insights from RNA-seq analysis of Cabernet Sauvignon roots
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  183. Revealing the effects of amino acid, organic acid, and phytohormones on the germination of tomato seeds under salinity stress
  184. Combined effects of nitrogen fertilizer and biochar on the growth, yield, and quality of pepper
  185. Comprehensive phytochemical and toxicological analysis of Chenopodium ambrosioides (L.) fractions
  186. Impact of “3414” fertilization on the yield and quality of greenhouse tomatoes
  187. Exploring the coupling mode of water and fertilizer for improving growth, fruit quality, and yield of the pear in the arid region
  188. Metagenomic analysis of endophytic bacteria in seed potato (Solanum tuberosum)
  189. Antibacterial, antifungal, and phytochemical properties of Salsola kali ethanolic extract
  190. Exploring the hepatoprotective properties of citronellol: In vitro and in silico studies on ethanol-induced damage in HepG2 cells
  191. Enhanced osmotic dehydration of watermelon rind using honey–sucrose solutions: A study on pre-treatment efficacy and mass transfer kinetics
  192. Effects of exogenous 2,4-epibrassinolide on photosynthetic traits of 53 cowpea varieties under NaCl stress
  193. Comparative transcriptome analysis of maize (Zea mays L.) seedlings in response to copper stress
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  196. Antioxidant and antimicrobial activities of Salsola imbricata methanolic extract and its phytochemical characterization
  197. Bioengineering and Biotechnology
  198. Absorbable calcium and phosphorus bioactive membranes promote bone marrow mesenchymal stem cells osteogenic differentiation for bone regeneration
  199. New advances in protein engineering for industrial applications: Key takeaways
  200. An overview of the production and use of Bacillus thuringiensis toxin
  201. Research progress of nanoparticles in diagnosis and treatment of hepatocellular carcinoma
  202. Bioelectrochemical biosensors for water quality assessment and wastewater monitoring
  203. PEI/MMNs@LNA-542 nanoparticles alleviate ICU-acquired weakness through targeted autophagy inhibition and mitochondrial protection
  204. Unleashing of cytotoxic effects of thymoquinone-bovine serum albumin nanoparticles on A549 lung cancer cells
  205. Erratum
  206. Erratum to “Investigating the association between dietary patterns and glycemic control among children and adolescents with T1DM”
  207. Erratum to “Activation of hypermethylated P2RY1 mitigates gastric cancer by promoting apoptosis and inhibiting proliferation”
  208. Retraction
  209. Retraction to “MiR-223-3p regulates cell viability, migration, invasion, and apoptosis of non-small cell lung cancer cells by targeting RHOB”
  210. Retraction to “A data mining technique for detecting malignant mesothelioma cancer using multiple regression analysis”
  211. Special Issue on Advances in Neurodegenerative Disease Research and Treatment
  212. Transplantation of human neural stem cell prevents symptomatic motor behavior disability in a rat model of Parkinson’s disease
  213. Special Issue on Multi-omics
  214. Inflammasome complex genes with clinical relevance suggest potential as therapeutic targets for anti-tumor drugs in clear cell renal cell carcinoma
  215. Gastroesophageal varices in primary biliary cholangitis with anti-centromere antibody positivity: Early onset?
https://doi.org/10.1515/biol-2022-0921
Keywords for this article
IgG4-related disease; IgG4-related kidney disease; membranous nephropathy; phospholipase A2 receptor; Tripterygium wilfordii
Creative Commons
BY 4.0

Articles in the same Issue

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  85. Analysis of the microecological mechanism of diabetic kidney disease based on the theory of “gut–kidney axis”: A systematic review
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  89. Association of low attenuation area scores with pulmonary function and clinical prognosis in patients with chronic obstructive pulmonary disease
  90. Long non-coding RNAs in bone formation: Key regulators and therapeutic prospects
  91. The deubiquitinating enzyme USP35 regulates the stability of NRF2 protein
  92. Neutrophil-to-lymphocyte ratio and platelet-to-lymphocyte ratio as potential diagnostic markers for rebleeding in patients with esophagogastric variceal bleeding
  93. G protein-coupled receptor 1 participating in the mechanism of mediating gestational diabetes mellitus by phosphorylating the AKT pathway
  94. LL37-mtDNA regulates viability, apoptosis, inflammation, and autophagy in lipopolysaccharide-treated RLE-6TN cells by targeting Hsp90aa1
  95. The analgesic effect of paeoniflorin: A focused review
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  97. Knockdown of HCK promotes HREC cell viability and inner blood–retinal barrier integrity by regulating the AMPK signaling pathway
  98. The role of rapamycin in the PINK1/Parkin signaling pathway in mitophagy in podocytes
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  100. Clinical value of macrogenome next-generation sequencing on infections
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  102. TAK-242 alleviates diabetic cardiomyopathy via inhibiting pyroptosis and TLR4/CaMKII/NLRP3 pathway
  103. Hypomethylation in promoters of PGC-1α involved in exercise-driven skeletal muscular alterations in old age
  104. Profile and antimicrobial susceptibility patterns of bacteria isolated from effluents of Kolladiba and Debark hospitals
  105. The expression and clinical significance of syncytin-1 in serum exosomes of hepatocellular carcinoma patients
  106. A histomorphometric study to evaluate the therapeutic effects of biosynthesized silver nanoparticles on the kidneys infected with Plasmodium chabaudi
  107. PGRMC1 and PAQR4 are promising molecular targets for a rare subtype of ovarian cancer
  108. Analysis of MDA, SOD, TAOC, MNCV, SNCV, and TSS scores in patients with diabetes peripheral neuropathy
  109. SLIT3 deficiency promotes non-small cell lung cancer progression by modulating UBE2C/WNT signaling
  110. The relationship between TMCO1 and CALR in the pathological characteristics of prostate cancer and its effect on the metastasis of prostate cancer cells
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  112. PHB2 alleviates retinal pigment epithelium cell fibrosis by suppressing the AGE–RAGE pathway
  113. Anti-γ-aminobutyric acid-B receptor autoimmune encephalitis with syncope as the initial symptom: Case report and literature review
  114. Comparative analysis of chloroplast genome of Lonicera japonica cv. Damaohua
  115. Human umbilical cord mesenchymal stem cells regulate glutathione metabolism depending on the ERK–Nrf2–HO-1 signal pathway to repair phosphoramide mustard-induced ovarian cancer cells
  116. Electroacupuncture on GB acupoints improves osteoporosis via the estradiol–PI3K–Akt signaling pathway
  117. Renalase protects against podocyte injury by inhibiting oxidative stress and apoptosis in diabetic nephropathy
  118. Review: Dicranostigma leptopodum: A peculiar plant of Papaveraceae
  119. Combination effect of flavonoids attenuates lung cancer cell proliferation by inhibiting the STAT3 and FAK signaling pathway
  120. Renal microangiopathy and immune complex glomerulonephritis induced by anti-tumour agents: A case report
  121. Correlation analysis of AVPR1a and AVPR2 with abnormal water and sodium and potassium metabolism in rats
  122. Gastrointestinal health anti-diarrheal mixture relieves spleen deficiency-induced diarrhea through regulating gut microbiota
  123. Myriad factors and pathways influencing tumor radiotherapy resistance
  124. Exploring the effects of culture conditions on Yapsin (YPS) gene expression in Nakaseomyces glabratus
  125. Screening of prognostic core genes based on cell–cell interaction in the peripheral blood of patients with sepsis
  126. Coagulation factor II thrombin receptor as a promising biomarker in breast cancer management
  127. Ileocecal mucinous carcinoma misdiagnosed as incarcerated hernia: A case report
  128. Methyltransferase like 13 promotes malignant behaviors of bladder cancer cells through targeting PI3K/ATK signaling pathway
  129. The debate between electricity and heat, efficacy and safety of irreversible electroporation and radiofrequency ablation in the treatment of liver cancer: A meta-analysis
  130. ZAG promotes colorectal cancer cell proliferation and epithelial–mesenchymal transition by promoting lipid synthesis
  131. Baicalein inhibits NLRP3 inflammasome activation and mitigates placental inflammation and oxidative stress in gestational diabetes mellitus
  132. Impact of SWCNT-conjugated senna leaf extract on breast cancer cells: A potential apoptotic therapeutic strategy
  133. MFAP5 inhibits the malignant progression of endometrial cancer cells in vitro
  134. Major ozonated autohemotherapy promoted functional recovery following spinal cord injury in adult rats via the inhibition of oxidative stress and inflammation
  135. Axodendritic targeting of TAU and MAP2 and microtubule polarization in iPSC-derived versus SH-SY5Y-derived human neurons
  136. Differential expression of phosphoinositide 3-kinase/protein kinase B and Toll-like receptor/nuclear factor kappa B signaling pathways in experimental obesity Wistar rat model
  137. The therapeutic potential of targeting Oncostatin M and the interleukin-6 family in retinal diseases: A comprehensive review
  138. BA inhibits LPS-stimulated inflammatory response and apoptosis in human middle ear epithelial cells by regulating the Nf-Kb/Iκbα axis
  139. Role of circRMRP and circRPL27 in chronic obstructive pulmonary disease
  140. Investigating the role of hyperexpressed HCN1 in inducing myocardial infarction through activation of the NF-κB signaling pathway
  141. Characterization of phenolic compounds and evaluation of anti-diabetic potential in Cannabis sativa L. seeds: In vivo, in vitro, and in silico studies
  142. Quantitative immunohistochemistry analysis of breast Ki67 based on artificial intelligence
  143. Ecology and Environmental Science
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  145. Degradation of a mixture of 13 polycyclic aromatic hydrocarbons by commercial effective microorganisms
  146. Evaluation of the impact of two citrus plants on the variation of Panonychus citri (Acari: Tetranychidae) and beneficial phytoseiid mites
  147. Prediction of present and future distribution areas of Juniperus drupacea Labill and determination of ethnobotany properties in Antalya Province, Türkiye
  148. Population genetics of Todarodes pacificus (Cephalopoda: Ommastrephidae) in the northwest Pacific Ocean via GBS sequencing
  149. A comparative analysis of dendrometric, macromorphological, and micromorphological characteristics of Pistacia atlantica subsp. atlantica and Pistacia terebinthus in the middle Atlas region of Morocco
  150. Macrofungal sporocarp community in the lichen Scots pine forests
  151. Assessing the proximate compositions of indigenous forage species in Yemen’s pastoral rangelands
  152. Food Science
  153. Gut microbiota changes associated with low-carbohydrate diet intervention for obesity
  154. Reexamination of Aspergillus cristatus phylogeny in dark tea: Characteristics of the mitochondrial genome
  155. Differences in the flavonoid composition of the leaves, fruits, and branches of mulberry are distinguished based on a plant metabolomics approach
  156. Investigating the impact of wet rendering (solventless method) on PUFA-rich oil from catfish (Clarias magur) viscera
  157. Non-linear associations between cardiovascular metabolic indices and metabolic-associated fatty liver disease: A cross-sectional study in the US population (2017–2020)
  158. Knockdown of USP7 alleviates atherosclerosis in ApoE-deficient mice by regulating EZH2 expression
  159. Utility of dairy microbiome as a tool for authentication and traceability
  160. Agriculture
  161. Enhancing faba bean (Vicia faba L.) productivity through establishing the area-specific fertilizer rate recommendation in southwest Ethiopia
  162. Impact of novel herbicide based on synthetic auxins and ALS inhibitor on weed control
  163. Perspectives of pteridophytes microbiome for bioremediation in agricultural applications
  164. Fertilizer application parameters for drip-irrigated peanut based on the fertilizer effect function established from a “3414” field trial
  165. Improving the productivity and profitability of maize (Zea mays L.) using optimum blended inorganic fertilization
  166. Application of leaf multispectral analyzer in comparison to hyperspectral device to assess the diversity of spectral reflectance indices in wheat genotypes
  167. Animal Sciences
  168. Knockdown of ANP32E inhibits colorectal cancer cell growth and glycolysis by regulating the AKT/mTOR pathway
  169. Development of a detection chip for major pathogenic drug-resistant genes and drug targets in bovine respiratory system diseases
  170. Exploration of the genetic influence of MYOT and MB genes on the plumage coloration of Muscovy ducks
  171. Transcriptome analysis of adipose tissue in grazing cattle: Identifying key regulators of fat metabolism
  172. Comparison of nutritional value of the wild and cultivated spiny loaches at three growth stages
  173. Transcriptomic analysis of liver immune response in Chinese spiny frog (Quasipaa spinosa) infected with Proteus mirabilis
  174. Disruption of BCAA degradation is a critical characteristic of diabetic cardiomyopathy revealed by integrated transcriptome and metabolome analysis
  175. Plant Sciences
  176. Effect of long-term in-row branch covering on soil microorganisms in pear orchards
  177. Photosynthetic physiological characteristics, growth performance, and element concentrations reveal the calcicole–calcifuge behaviors of three Camellia species
  178. Transcriptome analysis reveals the mechanism of NaHCO3 promoting tobacco leaf maturation
  179. Bioinformatics, expression analysis, and functional verification of allene oxide synthase gene HvnAOS1 and HvnAOS2 in qingke
  180. Water, nitrogen, and phosphorus coupling improves gray jujube fruit quality and yield
  181. Improving grape fruit quality through soil conditioner: Insights from RNA-seq analysis of Cabernet Sauvignon roots
  182. Role of Embinin in the reabsorption of nucleus pulposus in lumbar disc herniation: Promotion of nucleus pulposus neovascularization and apoptosis of nucleus pulposus cells
  183. Revealing the effects of amino acid, organic acid, and phytohormones on the germination of tomato seeds under salinity stress
  184. Combined effects of nitrogen fertilizer and biochar on the growth, yield, and quality of pepper
  185. Comprehensive phytochemical and toxicological analysis of Chenopodium ambrosioides (L.) fractions
  186. Impact of “3414” fertilization on the yield and quality of greenhouse tomatoes
  187. Exploring the coupling mode of water and fertilizer for improving growth, fruit quality, and yield of the pear in the arid region
  188. Metagenomic analysis of endophytic bacteria in seed potato (Solanum tuberosum)
  189. Antibacterial, antifungal, and phytochemical properties of Salsola kali ethanolic extract
  190. Exploring the hepatoprotective properties of citronellol: In vitro and in silico studies on ethanol-induced damage in HepG2 cells
  191. Enhanced osmotic dehydration of watermelon rind using honey–sucrose solutions: A study on pre-treatment efficacy and mass transfer kinetics
  192. Effects of exogenous 2,4-epibrassinolide on photosynthetic traits of 53 cowpea varieties under NaCl stress
  193. Comparative transcriptome analysis of maize (Zea mays L.) seedlings in response to copper stress
  194. An optimization method for measuring the stomata in cassava (Manihot esculenta Crantz) under multiple abiotic stresses
  195. Fosinopril inhibits Ang II-induced VSMC proliferation, phenotype transformation, migration, and oxidative stress through the TGF-β1/Smad signaling pathway
  196. Antioxidant and antimicrobial activities of Salsola imbricata methanolic extract and its phytochemical characterization
  197. Bioengineering and Biotechnology
  198. Absorbable calcium and phosphorus bioactive membranes promote bone marrow mesenchymal stem cells osteogenic differentiation for bone regeneration
  199. New advances in protein engineering for industrial applications: Key takeaways
  200. An overview of the production and use of Bacillus thuringiensis toxin
  201. Research progress of nanoparticles in diagnosis and treatment of hepatocellular carcinoma
  202. Bioelectrochemical biosensors for water quality assessment and wastewater monitoring
  203. PEI/MMNs@LNA-542 nanoparticles alleviate ICU-acquired weakness through targeted autophagy inhibition and mitochondrial protection
  204. Unleashing of cytotoxic effects of thymoquinone-bovine serum albumin nanoparticles on A549 lung cancer cells
  205. Erratum
  206. Erratum to “Investigating the association between dietary patterns and glycemic control among children and adolescents with T1DM”
  207. Erratum to “Activation of hypermethylated P2RY1 mitigates gastric cancer by promoting apoptosis and inhibiting proliferation”
  208. Retraction
  209. Retraction to “MiR-223-3p regulates cell viability, migration, invasion, and apoptosis of non-small cell lung cancer cells by targeting RHOB”
  210. Retraction to “A data mining technique for detecting malignant mesothelioma cancer using multiple regression analysis”
  211. Special Issue on Advances in Neurodegenerative Disease Research and Treatment
  212. Transplantation of human neural stem cell prevents symptomatic motor behavior disability in a rat model of Parkinson’s disease
  213. Special Issue on Multi-omics
  214. Inflammasome complex genes with clinical relevance suggest potential as therapeutic targets for anti-tumor drugs in clear cell renal cell carcinoma
  215. Gastroesophageal varices in primary biliary cholangitis with anti-centromere antibody positivity: Early onset?
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