Lupus Nephritis from Pathogenesis to New Therapies: An Update
Abstract
:1. Introduction
2. Epidemiology
3. Pathogenesis of Lupus Nephritis (LN)
3.1. Genetics and Epigenetics
3.2. Environmental Factors
3.3. Immunological Mechanisms
3.3.1. Role of Autoantibodies
3.3.2. The Complex Role of Complement
3.3.3. Vitamin D Deficiency
3.3.4. Role of Infiltrating Immune Cells
Neutrophil
Monocyte/Macrophage
Lymphocyte
Dendritic Cell (DC)
3.4. Role of Kidney Resident Cells
3.4.1. Tubular Epithelial Cells (TEC)
3.4.2. Podocyte
3.4.3. Mesangial Cell (MC)
3.4.4. Glomerular Endothelial Cell (GEC)
4. The Role of Renal Biopsy and of New Biomarkers in the Management of LN
4.1. Renal Biopsy
4.1.1. Renal Biopsy as a Diagnostic Tool
4.1.2. Renal Biopsy as a Prognostic Tool
4.2. Potential Biomarkers
Biomarker | Biological Fluid | Associations | References |
---|---|---|---|
u-Gal-3BP | Urine | Histological disease activity | [152,153,154] |
MCP-1 | Urine | Clinical severity | [155,156] |
TWEAK | Urine | Diagnosis | [157] |
CAM | Urine | Clinical severity | [158,159,160] |
miR146a miR135b | Urine | Histological disease activity; Response to therapy | [161,162,163] |
Axl | Serum | Diagnosis; Clinical severity; Response to therapy; Prognosis | [164,165,166] |
HE4 | Serum | Diagnosis | [167,168] |
IGFBP-2 | Serum | Diagnosis; Clinical severity; Organ damage | [169] |
miR | Serum | Diagnosis | [170,171] |
IL-17 and IL-18 | Serum | Clinical severity and histological activity | [172,173,174] |
sTNFRII | Serum | Clinical severity and histological activity Organ damage | [175,176] |
Adipokines | Serum | Clinical severity; Atherosclerotic organ damage and insulin-resistance | [177,178,179,180] |
BAFF and APRIL | Serum | Clinical severity and histological activity; Response to therapy | [181,182,183,184,185,186,187] |
Syndecan-1 | Serum | Clinical severity and histological (tubulointerstitial) activity | [188] |
4.2.1. Urinary Biomarkers
Urinary Galectin 3 Binding Protein
Monocyte Chemoattractant Protein-1 (MCP-1)
TNF-like Weak Inducer of Apoptosis (TWEAK)
Cell Adhesion Molecules (CAM)
MicroRNA (miRs)
4.2.2. Serum Biomarkers
Axl
Human Epididymis Protein 4 (HE4)
Insulin-like Growth Factor-Binding Protein 2 (IGFBP2)
miR-21
IL-17 and IL 18
Soluble TNF Receptor 2 (sTNFR2)
Adipokines
B Lymphocyte Activating Factor (BAFF) and “a Proliferation-Inducing Ligand” (APRIL)
Syndecan-1 and Other Glycocalyx Components
5. Immunosuppressive (IS) Therapies in LN
5.1. Conventional Is Therapies
5.1.1. Induction Therapy
5.1.2. Maintenance Therapy
5.1.3. The Role of Rituximab (RTX)
5.2. New FDA-Approved Drugs
5.2.1. Belimumab (BEL)
5.2.2. Voclosporin (VOC)
5.3. Drugs in Phase III Clinical Trials
5.3.1. Anifrolumab
5.3.2. Obinutuzumab
5.3.3. Ianalumab
5.3.4. Sodium-Glucose Cotransporter-2 Inhibitors (SGLT2i)
5.4. Other Drugs
5.4.1. Ustekinumab and Secukinumab
5.4.2. Inhibitors of Mammalian Target of Rapamycin (mTOR)
5.4.3. Janus Kinases (JAK) Inhibitors
5.4.4. Daratumumab
6. Adjunctive Therapies beyond Immunosuppression
6.1. Control of Blood Pressure
6.2. Control of Proteinuria
6.3. Control of Dyslipidemia
6.4. Prevention of Thromboembolism
6.5. Prevention of GC-Induced Osteoporosis
6.6. Prevention of Infections
7. The Role of Non-Pharmacological Management
7.1. General Lifestyle Measures
7.2. Dietary and Nutritional Aspects
7.3. Patient Education and Support
8. Current Limitations and New Perspectives
9. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
aCL | anticardiolipin antibody |
ALCAM | activated leukocyte CAM |
APC | antigen presenting cell |
aPL | anti-phospholipid |
APS | anti-phospholipid syndrome |
APRIL | a proliferation-inducing ligand |
BAFF | B cell activating factor for TNF family |
BEL | belimumab |
CAM | cell-adhesion molecule |
circRNA | circular RNA |
CKD | chronic kidney disease |
CYC | cyclophosphamide |
CNI | calcineurin inhibitor |
CR | complete remission |
CRR | complete renal remission |
DC | dendritic cell |
DEG | differentially expressed genes |
ELNT | Euro Lupus Nephritis Trial |
ESRD | end stage renal disease |
EV | extracellular vesicle |
Fn14 | fibroblast growth factor-inducible 14 |
GC | glucocorticoid |
GEC | glomerular endothelial cell |
GN | glomerulonephritis |
HCQ | hydroxychloroquine |
HE4 | human epididymis protein 4 |
IC | immune complex |
IFN | interferon |
IFN-I | type I interferon |
IL | interleukin |
IS | immunosuppressive |
JAK | Janus Kinase |
KIM1 | kidney injury molecule 1 |
LNA | locked nucleic acid |
lncRNA | long non-coding RNA |
MC | mesangial cell |
MCP-1 | monocyte chemoattractant protein1 |
MERTK | MER tyrosine kinase |
MHC | major histocompatibility complex |
miR | microRNA |
MMF | mycophenolate mofetil |
MN | Monocyte neutrophil |
MP | methylprednisolone |
MPA | mycophenolic acid |
mTOR | mammalian target of rapamycin |
ncRNA | non-coding RNA |
NET | neutrophil extracellular trap |
NGAL | neutrophil gelatinase associated lipocalin |
NK | natural killer |
pDC | plasmacytoid dendritic cell |
PDN | prednisone |
PR | partial remission |
RNP | ribonucleoprotein |
RTX | rituximab |
SGLT2i | sodium-glucose cotransporter-2 inhibitor |
SLAMF | signaling lymphocyte activation molecule family |
SLEDAI | systemic lupus erythematosus disease activity index |
Sm | Smith |
SOC | standard of care |
STAT | signal transducer and activation of transcription |
TEC | tubular epithelia cell |
TFH | T follicular helper |
TGFβ | transforming growth factor β |
TMA | thrombotic microangiopathy |
TNF | tumor necrosis factor |
Th | T helper lymphocyte |
Treg | T regulatory lymphocyte |
TWEAK | TNF-like weak inducer of apoptosis |
SAP | SLAM associated protein |
SLAM | costimulatory lymphocyte associated molecule |
SLE | systemic lupus erythematosus |
VCAM-1 | vascular CAM1 |
VOC | voclosporin |
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Country | LN/All Diagnoses | Reference |
---|---|---|
USA | 7% | [20] |
Norway | 4.1% | [21] |
Belgium | 4.1% | [22] |
Germany | 5% | [23] |
Spain | 8.7% | [24] |
China | 7.5% | [25] |
Japan | 6.5% | [26] |
India | 9.4% | [27] |
Colombia | 17.8% | [28] |
Senegal | 13.7% | [29] |
Study (Publication Year) | Drug | Main Results | Other Results and Comments | References |
---|---|---|---|---|
BLISS LN (2020) | BEL | 43% vs. 32% in CRR trial vs. SOC (p < 0.01) | Reduced incidence of renal and extra-renal flares and of renal events or death. It can be used in renal failure and during pregnancy. Impaired response if proteinuria > 3 g/d. It can be associated with either CYC or MMF and GC (triple induction therapy). | [218] |
BEAT LUPUS (2021) | RTX-BEL sequential therapy | Reduced incidence of post-RTX flares | BEL maintenance therapy after RTX may be necessary to prevent flares in SLE refractory to conventional therapy. | [219] |
AURORA 1 (2021) | VOC | 41% vs. 23% in CRR trial vs. SOC (p < 0.01) | Rapid decrease in proteinuria (50% in 1 month). Aggressive GC tapering (PDN 2.5 mg/d by 16 weeks) successful in 80% of patients. It can be associated with MMF and GC as triple induction therapy. | [220] |
AURORA 2 (2022–2023) | VOC | Stable GRF and no evidence of chronic nephrotoxicity at renal biopsy after 3 years. | Less nephrotoxicity than CsA and TAC, but requires GFR > 45 mL/min. | [221] |
TULIP-LN (2022) and extension (2023) | Anifrolumab | 27.3% vs. 17.8% CRR in intensive-regimen Anifrolumab vs. placebo at 2 years. | Improvement of GRF numerically higher in both intensive and basic regimen of Anifrolumab. Higher incidence of Varicella Zoster. | [222] |
NOBILITY (2022) | Obinutuzumab | Primary endpoint not met; however, 38% vs. 16% in CRR trial vs. SOC at 76 week (p < 0.01) with PDN <7.5 mg/d and improved renal responses through week 104. | Superior preservation of renal function and prevention of LN flares at post-hoc analysis. | [223] |
Vaccinations | Indications and Comments |
---|---|
Pneumococcus, meningococcus, haemophilus Influenzae B | Recommended in all SLE patients. |
Tetanus, diphtheria, pertussis | |
Influenza, hepatitis A and B | |
Recombinant herpes zoster | Reactivation of herpes zoster virus is frequent in SLE patients and vaccination can be considered on an individual basis. |
Papillomavirus | Risk factor for cervical cancer in SLE patients. |
COVID-19 | |
Prophylactic treatments | |
Hepatitis B and hepatitis C | Patients with chronic or past infection planned to be treated with lymphocyte depleting agents or intense IS. |
Strongyloides stercoralis | Prophylaxis could be considered in patients planned to be treated with high dose GC pulses to prevent Strongyloides hyperinfection syndrome. |
Pneumocystis jirovecii | Although debated, prophylaxis could be considered in patients planned to be treated with RTX or intense IS; presence of LN and lymphopenia (<500 lymphocytes/mm3) are among risk factors for reactivation. |
Latent tuberculosis | Patients with positive epidemiology and/or positive screening test and/or radiological evidence of previous exposure. |
Measles and chickenpox | Patients exposed to infected people in a contagious phase might be treated with hyperimmune immunoglobulin and varicella zoster immunoglobulin, respectively. |
Type of ncRNA | Mechanism of Action | Comments | Reference |
---|---|---|---|
miR-410 | Inhibition of IL-6 expression | Decreased IL-6, TFG-β1 and collagen I/III production by MC in experimental models. | [303] |
miR-125a-3p | Inhibition of IL-17 and TGF-β1 expression | Suppression of fibrosis in LN mice. | [304] |
miR-127-3p | Inhibition of IFN-I/JACK1 signaling | miR-127b-3p is a negative regulator of STING/IRF3/IFN-I signaling in MC and its expression is reduced in LN; miR-127-3p mimics could correct overactivation of IFN-I/JACK1 signaling in LN. | [305] |
miR-145 | Inhibition of CSF-1 expression | Down-regulation of CSF-1 inhibits JAK/STAT signaling pathway and LN development in vivo. | [306] |
Knockdown of lncRNA RP11-2B6.2 | Inhibition of IFN-I signaling | lncRNA RP11-2B6.2 expression is elevated in renal tissue in LN and correlates with expression of IFN-stimulated genes. | [307] |
Knockdown of circRNA ELK4 | Inhibition of miR-27b-3p | circRNA ELK4 correlates with LN activity. circELK4/ miR-27b-3p/STING/IRF3/IRN-I axis probably crucial in LN. | [305] |
LNA-anti-miR-150 | Inhibition of miR-150 | miR-150 promotes MC aging and expression of pro-fibrotic genes; it is involved in M1 macrophage polarization. | [307] |
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Roveta, A.; Parodi, E.L.; Brezzi, B.; Tunesi, F.; Zanetti, V.; Merlotti, G.; Francese, A.; Maconi, A.G.; Quaglia, M. Lupus Nephritis from Pathogenesis to New Therapies: An Update. Int. J. Mol. Sci. 2024, 25, 8981. https://doi.org/10.3390/ijms25168981
Roveta A, Parodi EL, Brezzi B, Tunesi F, Zanetti V, Merlotti G, Francese A, Maconi AG, Quaglia M. Lupus Nephritis from Pathogenesis to New Therapies: An Update. International Journal of Molecular Sciences. 2024; 25(16):8981. https://doi.org/10.3390/ijms25168981
Chicago/Turabian StyleRoveta, Annalisa, Emanuele Luigi Parodi, Brigida Brezzi, Francesca Tunesi, Valentina Zanetti, Guido Merlotti, Alessia Francese, Antonio G. Maconi, and Marco Quaglia. 2024. "Lupus Nephritis from Pathogenesis to New Therapies: An Update" International Journal of Molecular Sciences 25, no. 16: 8981. https://doi.org/10.3390/ijms25168981