Pulmonary Fibrosis as a Result of Acute Lung Inflammation: Molecular Mechanisms, Relevant In Vivo Models, Prognostic and Therapeutic Approaches
Abstract
:1. Introduction
2. Acute Lung Inflammation as a Precursor of Pulmonary Fibrosis: Etiology, Pathogenesis, Morphological Characteristics, Outcomes
2.1. Acute Lung Injury (ALI) as One of the Etiological Factors of Pulmonary Fibrosis
2.2. Pathogenesis of ALI
2.3. Pathomorphological Changes in the Lungs during ALI Development
2.4. Outcomes of Acute Lung Inflammation
3. Pathomorphological Changes in the Lungs during Fibrosis Development
3.1. Pathogenesis of Pulmonary Fibrosis Development
3.2. Pathomorphological Changes in the Lungs during Fibrosis Development
3.2.1. Histological Classification
3.2.2. Multidisciplinary Classification of American Thoracic Society and European Respiratory Society
4. Molecular Mechanisms of Pulmonary Fibrosis Development
4.1. Main Effector Cells of Pulmonary Fibrosis: Fibroblasts, Myofibroblasts and Fibrocytes
4.1.1. Fibrocytes Characteristics and Their Role in Pulmonary Fibrosis Development
4.1.2. Differentiation of Fibroblasts to Myofibroblasts and Their Role in Pulmonary Fibrosis Development
4.1.3. Lipofibroblasts in Pulmonary Fibrosis Development
4.2. Possible Role of EMT in Pulmonary Fibrosis Development
4.3. Signaling Pathways in Pulmonary Fibrosis Development
4.3.1. TGF-β Signaling Pathway
4.3.2. Wnt/β-Catenin Signaling Pathway
- Wnt/β-catenin signaling induces the anti-apoptotic and pro-fibrotic phenotype in lung fibroblasts, leading to fibroblast proliferation and their differentiation into myofibroblasts, exacerbating lung tissue fibrosis [181];
- Wnt/β-catenin activation of AEC II increases IL-1β production, stimulating inflammatory and pro-fibrotic responses [182];
- Non-canonical activation of Wnt also stimulates fibroblast proliferation and increases the synthesis of ECM components [178].
4.3.3. VEGF Signaling Pathway
4.3.4. Hedgehog Signaling Pathway
4.3.5. Notch Signaling Pathway
4.3.6. Fibroblast Growth Factor Signaling Pathway
4.4. Role of Cytokines in Pulmonary Fibrosis Development
4.5. Role of Immune Cells in Pulmonary Fibrosis Development
4.5.1. T-Lymphocytes
4.5.2. Macrophages
4.5.3. Autoimmunity
4.6. Role of Reactive Oxygen Species in the Development of Pulmonary Fibrosis
5. Relevant Murine Models of Acute Lung Injury and Pulmonary Fibrosis
5.1. Animal Models of Acute Lung Injury
5.1.1. LPS-Induced Acute Lung Injury
5.1.2. Hyperoxia-Induced Acute Lung Injury
5.1.3. Oleic Acid-Induced Acute Lung Injury
5.1.4. Acid Aspiration-Induced Acute Lung Injury
5.1.5. Mechanical Ventilation-Induced Acute Lung Injury
5.2. Animal Models of Pulmonary Fibrosis
5.2.1. Bleomycin-Induced Pulmonary Fibrosis
5.2.2. Radiation-Induced Pulmonary Fibrosis
5.2.3. Silica Particle-Induced Pulmonary Fibrosis
5.2.4. FITC-Induced Pulmonary Fibrosis
6. Prognostic Markers of Acute Lung Injury and Pulmonary Fibrosis
6.1. Biomarkers of Acute Lung Injury
6.1.1. Exudative Phase
6.1.2. Proliferative Phase
6.2. Biomarkers of Pulmonary Fibrosis
7. Therapeutic Approaches to Suppress Transition from Acute Lung Inflammation to Fibrosis
7.1. Approved Fibrosis Therapeutics
7.2. Anti-Fibrotic Therapeutic in Phase II and III Clinical Trials
7.3. Gene Therapy in Pulmonary Fibrosis Treatment
7.3.1. Enhancement of Gene Expression
7.3.2. Suppression of Gene Expression
8. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Model | Histological Characteristics | Modeling Object | Advantages and Disadvantages | References |
---|---|---|---|---|
Lipopolysaccharide (LPS)-induced acute lung injury Inducing agent—LPS | Neutrophil-associated inflammatory infiltration with the admixture of lymphocytes and macrophages, circulatory disruption, microvascular thrombosis, hemorrhages, interstitial and alveolar edemas | Inflammatory response similar to bacterial infection | +Multiplicity of administration routes (intraperitoneal, intranasal, intratracheal) +Reproducibility −Variability of inflammation severity −Dependence on LPS quality/purity/bacteria type | [290,291,292,293,294,295,296] |
Hyperoxia-induced acute lung injury Inducing agent—100% oxygen | Thickening of alveolar walls, alveolar and interstitial edemas, hemorrhages and inflammatory infiltration | Exudative and proliferative phases of ALI/ARDS; lung restoration after injury | +Reproducibility +Clinical relevance regarding ICU patients receiving oxygen support or mechanical ventilation −Relevance regarding healthy lungs | [297,298,299,300] |
Oleic acid-induced acute lung injury Inducing agent—Cis-9-octadecenoic acid | Early necrotic foci and microvascular thrombosis followed by AEC II proliferation and connective tissue growth in sub-pleural areas; polymorphism of damaged sites in the lung tissue | Morphological changes in the lung tissue caused by fat embolism of pulmonary vessels caused by severe trauma or bone fractures | +Reproducibility +Reflection of reversible ALI phases −Dissolution in ethyl alcohol −Few cases of ALI caused by fat embolism in humans | [301,302,303,304] |
Acid aspiration-induced acute lung injury Inducing agent—hydrochloric acid | Neutrophil inflammatory infiltration and alveolar hemorrhages followed by fibroproliferative response; interstitial and alveolar edemas | Morphological changes in the lung tissue caused by gastric contents aspiration; neutrophil migration mechanisms in ALI/ARDS | +Multiple altered parameters in the lungs +Combination with other ALI induction methods −Narrow induction dose of hydrochloric acid −Clinical relevance due to complex mixture of gastric contents in humans | [305,306,307,308,309] |
Mechanical ventilation-induced acute lung injury Inducing agent—mechanical ventilation | Interstitial edema, infiltration of alveolar walls by mononuclear cells, hemorrhages and fibrin deposition | Mechanical ventilation strategies in critical ALI patients support; lung biomechanics during ALI/ARDS development | +Clinical relevance +Combination with other lung damaging factors −Complexity/special equipment | [310,311,312,313,314,315,316] |
Model | Histological Characteristics | Modeling Object | Advantages and Disadvantages | References |
---|---|---|---|---|
Bleomycin-induced pulmonary fibrosis Inducing agent—bleomycin | Mononuclear infiltration of lung tissue, thickening of alveolar walls, congestion of blood vessels, destruction of alveolar epithelium and deposition of newly synthesized collagen fibers in alveolar walls and around blood vessels and bronchi | Mechanisms of pulmonary fibrosis development after inflammation/ARDS; estimation of anti-fibrotic therapy efficacy | +Multiplicity of administration routes (intranasal, intratracheal, intraperitoneal, subcutaneous, intravenous, via inhalations) +Simplicity of induction +Reproducibility/standardization of effects +Clinical relevance regarding ARDS −Self-limiting character of fibrosis −Relevance of induction route regarding human fibrosis | [317,318,319,320,321] |
Radiation-induced pulmonary fibrosis Inducing agent—ionizing radiation | Subpleural fibrotic foci, increased collagen deposition in collapsed alveoli and inflammatory infiltration of surrounding fibrotic tissue | Radiation-triggered pulmonary fibrosis; lung vessels remodeling during pulmonary hypertension | +Clinical relevance −Long duration −High coast (ionizing radiation source, personal protection) | [99,322,323,324,325,326,327] |
Silica particle-induced pulmonary fibrosis Inducing agent—silica particles | Connective tissue growth and formation of fibrotic nodes around silica particles, low inflammation intensity | Silica-associated nodular pulmonary fibrosis, silicosis and silica fibrosis | +Multiplicity of administration routes (aerosol inhalation, intratracheal or oropharyngeal instillation) +Constant fibrotic response +Possibility of long-term investigations −Dependence of fibrosis formation on administration route (intratracheal instillation—two to four weeks, aerosol inhalation—one to three months) −Low reproducibility −Low clinical relevance −Absence of some pulmonary fibrosis characteristics (local heterogeneity, hyperplastic changes in alveolar epithelium) | [328,329,330,331,332] |
Fluorescein isothiocyanate (FITC)-induced lung fibrosis Inducing agent—FITC | Infiltration of lung tissue with mononuclear cells and neutrophils, edema and epithelial cell hyperplasia, culminating in fibrosis development | Fibrosis detection; investigation of anti-fibrotic drugs regarding already formed fibrosis | +Usage of different mouse lines +Constant fibrotic response +Possibility of long-term investigations +Non-self-limiting character −Dependence on FITC quality and size of particles −Narrow difference between effective and toxic doses −Clinical relevance | [332,333,334,335] |
Lung Pathology | Marker | Source | Design of the Study | Proposed Usage in Clinical Setting | References |
---|---|---|---|---|---|
ALI (exudative phase) | IL-6 | Serum, BALF | Murine model; single-center prospective cohort studies | Increased concentration is associated with early exacerbations of pulmonary fibrosis, fatal SARS-CoV-2-induced pneumonia and higher chance of fatal ALI | [345,346,347,348] |
CXCL13 | Serum and plasma | Single center prospective cohort studies | Increased concentration is a prognostic marker of SARS-CoV-2-induced ALI mortality, admission to intensive care unit (ICU) and ICU mortality | [349,350] | |
IL-8 | Plasma, BALF | Single and multiple-center randomized clinical trial | Increased concentration is a marker of severity and increased mortality in ALI patients | [351,352] | |
IL-18 | Peripheral blood, plasma, lung tissue | Murine model; single-center randomized study | Increased concentration indicates morbidity, increased severity and ICU mortality of ALI patients | [353,354] | |
IL-1β | BALF | Single-center observational study | Increased concentration correlates with high ICU mortality | [348] | |
Tumor necrosis factor α | Serum, BALF | Single-center prospective study | Increased concentration indicates high ICU mortality | [348] | |
Surfactant proteins A and D | Serum | Single-center observational study | Increased concentration is a prognostic marker of early severe course of SARS-CoV-2-induced ALI | [355] | |
Krebs von den Lungen-6 | Serum | Literature meta-analysis | Increased concentration predicts severe COVID-19 stratification | [356] | |
Vascular endothelial growth factor | BAL fluid | Single-center observational and retrospective studies | Increased concentration is a prognostic marker of resolving ALI | [357,358] | |
Keratinocyte growth factor | BAL fluid | Single-center prospective study | Increased concentration is a prognostic marker of severity and poor outcome of ALI | [359] | |
Plasminogen activator inhibitor | Plasma | Prospective multi-center observational study | Increased concentration is a predictor of ALI severity | [360] | |
Thrombomodulin | Plasma | Prospective multi-center observational study | Increased concentration predicts increased ALI mortality in first 90 days after invasive mechanical ventilation | [361] | |
ALI (proliferative phase) | Hepatocyte growth factor | BAL fluid | Single-center cohort study | Increased concentration is a prognostic marker of ALI development | [362] |
Pentraxin-3 | Peripheral blood mononuclear cells | Single-center observational study | Increased concentration is a prognostic marker of short term mortality in COVID-19 | [363] | |
Tissue inhibitor of metalloproteinase-1 | Serum | Multi-center observational study | Increased concentration is associated with worse outcome in mechanically ventilated ALI patients | [364] | |
Tenascin-C | BAL fluid | Single-center observational study | Increased concentration is a prognostic marker of severe SARS-CoV-2 induced ALI | [365] | |
Matrix metalloproteinase-8 | BALF | Single-center observational and prospective study | Increased concentration in BALF is a prognostic marker of fatal ALI | [366] | |
Urokinase plasminogen activator | Plasma | Multi-center observational prospective study | Increased concentration in plasma is diagnostic and prognostic marker of mechanically ventilated ALI patients | [367] | |
A disintegrin and metalloproteinase-8 | BAL fluid | Mice model; single-center observational study | Increased concentration is a prognostic marker of ALI onset and severity | [368] | |
Pulmonary fibrosis | Krebs von den Lungen-6 | Serum | Single-center prospective study | Increased concentration is a prognostic factor of acute exacerbation in pulmonary fibrosis | [369] |
Surfactant protein A | Serum | Single-center observational study | Decreased concentration is a prognostic marker of anti-fibrotic therapy effectiveness | [370] | |
Clara cell protein 16 | Serum | Single-center retrospective longitudinal study | Increased concentration is a prognostic marker of active pulmonary fibrosis in systemic sclerosis patients | [371] | |
Matrix metalloproteinase 1 | Peripheral blood, lung tissue | Single-center observational study | Increased peripheral blood concentration is a diagnostic marker of pulmonary fibrosis, differentiating it from other ILDs. | [372] | |
Matrix metalloproteinase 7 | Serum | Multi-center, prospective, randomized, double-blind, placebo-controlled trial | Increased serum concentration is a prognostic marker of high risk of worsening and decline of lung functions | [373] | |
Matrix metalloproteinase-9 | Serum | Multi-center observational study | Increased concentration is a prognostic marker of severe course and worse outcome of pulmonary fibrosis | [374] | |
A disintegrin and metalloproteinase-17 | Peripheral blood mononuclear cells | Single-center observational study | Increased expression is associated with more active disease development and severity | [375] | |
Periostin | Serum | Single-center retrospective study | Increased concentration is a prognostic marker of increased mortality in pulmonary fibrosis patients | [376] | |
Circulating fibrocytes | Serum | Single-center observational study | Increased concentration is a prognostic marker of pulmonary fibrosis activity and increased mortality | [377,378] | |
Osteopontin | Serum | Single-center observational study | Increased concentration is a prognostic marker of exacerbation of pulmonary fibrosis | [379] | |
Lysyl oxidase-like 2 | Serum | Single-center observational study | Increased concentration is a prognostic marker of pulmonary hypertension and worse disease outcome in pulmonary fibrosis | [380] | |
Insulin-like growth factor binding proteins | Serum | Single-center observational studies | Increased concentration is associated with worse disease outcome of systemic sclerosis-associated pulmonary fibrosis | [381,382] |
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Savin, I.A.; Zenkova, M.A.; Sen’kova, A.V. Pulmonary Fibrosis as a Result of Acute Lung Inflammation: Molecular Mechanisms, Relevant In Vivo Models, Prognostic and Therapeutic Approaches. Int. J. Mol. Sci. 2022, 23, 14959. https://doi.org/10.3390/ijms232314959
Savin IA, Zenkova MA, Sen’kova AV. Pulmonary Fibrosis as a Result of Acute Lung Inflammation: Molecular Mechanisms, Relevant In Vivo Models, Prognostic and Therapeutic Approaches. International Journal of Molecular Sciences. 2022; 23(23):14959. https://doi.org/10.3390/ijms232314959
Chicago/Turabian StyleSavin, Innokenty A., Marina A. Zenkova, and Aleksandra V. Sen’kova. 2022. "Pulmonary Fibrosis as a Result of Acute Lung Inflammation: Molecular Mechanisms, Relevant In Vivo Models, Prognostic and Therapeutic Approaches" International Journal of Molecular Sciences 23, no. 23: 14959. https://doi.org/10.3390/ijms232314959