PMC:7271924 / 13792-25088 JSONTXT

{"target":"https://pubannotation.org/docs/sourcedb/PMC/sourceid/7271924","sourcedb":"PMC","sourceid":"7271924","source_url":"https://www.ncbi.nlm.nih.gov/pmc/7271924","text":"Lactoferrin: an Important Element in Host Defense\n\nNeutrophils and Lactoferrin\nLF plays an important role in host defense, upon its release from the neutrophil (26). LF also enhances natural killer cell activity in immune defense (135) and can restrict the entry of the virus into host cells during infection. As part of the host's inflammatory response, leucocytes, including neutrophils, release LF from their granules, where it is normally stored. Activated neutrophils also release chromatin fibers, known as neutrophil extracellular traps (NETs), which trap and kill, amongst others, bacteria (1, 136). These NETs likewise modulate both acute and chronic inflammation (137, 138). NETs are also found in various autoimmune conditions such as rheumatoid arthritis, systemic lupus erythematosus (139, 140). Interestingly, 106 human neutrophils can release 15 μg of LF (26). In addition to DNA and histones, NET fibers contain extranuclear proteins and proteins such as elastase, myeloperoxidase (MPO), and LF (141). LF may also serve as an intrinsic inhibitor of NETs release into the circulation, and may therefore be central in controlling NETs release (1). See Figure 3.\nFigure 3 Bacterial binding to various receptors, e.g., Toll-like receptors 2 and 4 (TLR2 and 4), as well as complement receptors, leads to protein arginine deiminase 4 (PAD4) activation, followed by chromatin decondensation, hypercitrullination of histones 3 and 4 in the nucleus, and nuclear membrane disruption. Granules also release lactoferrin. Neutrophil Extracellular Traps (NETs) and their protein constituents (including lactoferrin) are released from the neutrophil. Adapted from Jorch and Kubes (142) and Law and Gray (143). Bacteria are expelled and trapped in the NETs. Diagram created with BioRender (https://biorender.com/).\n\nBacteria and Lactoferrin\nOne of the most well-known characteristics of LF is that it is antibacterial (19, 144–148), antiviral (99, 149–151), antifungal (152–154), anti-inflammatory (26), and anti-carcinogenic (155). Its ability to of limit iron availability to microbes is one of its crucial amicrobial properties. Bacteria have, however, developed various ways to sequester iron (156). Figure 4 shows how bacteria acquire iron through receptor-mediated recognition of transferrin, hemopexin, hemoglobin, or hemoglobin-haptoglobin complexes and also LF (30). As well as binding it directly from the environment, bacterial siderophores can obtain iron by removing it from transferrin, lactoferrin, or ferritin (32). These siderophore-iron complexes are then recognized by receptors on the bacterium (30). Host innate immune functions are supported by the circulating protein, siderocalin, also known as Neutrophil gelatinase-associated lipocalin (NGAL), lipocalin2 or Lcn2 as it inhibits siderophore-mediated iron acquisition and release (30).\nFigure 4 Ways by which bacteria acquire iron [adapted from (19, 30)]. Transferrin receptor, lactoferrin receptor, hemophore (Hp), hemophore receptor, and hemopexin. Siderophores remove iron from lactoferrin, ferritin and transferrin, and also from the environment. Stealth siderophores are modified in such a way as to prevent siderocalin binding. A primary bacterial defense against siderocalin involves the production of stealth siderophores. Modified from Rosa et al. and Skaar (19, 30). Diagram created with BioRender (https://biorender.com/). Although LF has various means to counteract bacteria as part of its immune function (131), it is also capable of being hijacked to benefit the activities of bacteria. Thus, bacteria can also exploit LF by removing its bound ferric iron (19, 30). This process involves (1) synthesis of high-affinity ferric ion chelators by bacteria, (2) iron acquisition through LF or transferrin binding, mediated by bacterial-specific surface bacterial receptors, (3) or iron acquisition through bacterial reductases, which are able to reduce ferric to ferrous ions (19, 144–148).\nSeveral Gram-negative pathogens including members of the genera Neisseria and Moraxella have evolved two-component systems that can extract iron from the host LF and transferrin (157). N. meningitidis is a principal cause of bacterial meningitis in children. While the majority of pathogenic bacteria employ siderophores to chelate and scavenge iron (158), Neisseria has evolved a series of protein transporters that directly hijack iron sequestered in host transferrin, lactoferrin, and hemoglobin (159). The system consists of a membrane-bound transporter that extracts and transports iron across the outer membrane (TbpA for transferrin and LbpA for lactoferrin), and a lipoprotein that delivers iron-loaded lactoferrin/transferrin to the transporter (TbpB for transferrin and LbpB for lactoferrin) (157). LbpB binds the N-lobe of lactoferrin, whereas TbpB binds the C-lobe of transferrin (157). However, more than 90% of LF in human milk is in the form of apolactoferrin (160), which competes with siderophilic bacteria for ferric iron, and disrupts the proliferation of these microbial and other pathogens. Similarly LF supplements may play an important role to counteract bacterial processes. LF is consequently a significant element of host defense (19), and its levels may vary in health and during disease. It is hence known to be a modulator of innate and adaptive immune responses (161).\n\nViruses and Lactoferrin\nLF has strong antiviral activity against a broad spectrum of both naked and enveloped DNA and RNA viruses (99, 149–151). LF inhibits the entry of viral particles into host cells, either by direct attachment to the viral particles or by blocking their cellular receptors (discussed in previous paragraphs) (149). Some of the viruses that LF prevents from entering host cells e.g., Herpes simplex virus (162), human papillomavirus (163), human immunodeficiency virus (HIV) (164), and rotavirus (165). These viruses typically utilize common molecules on the cell membrane to facilitate their invasion into cells, including HSPGs (Figure 1). HSPGs provide the first anchoring sites on the host cell surface, and help the virus make primary contact with these cells (99, 162). HSPGs can be either membrane bound, or in secretory vesicles and in the extracellular matrix (86). It has been shown that LF is able to prevent the internalization of some viruses by binding to HSPGs (86).\n\nCOVID-19 and Lactoferrin\nCOVID-19 is caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Many COVID-19 patients develop acute respiratory distress syndrome (ARDS), which leads to pulmonary edema and lung failure, and have liver, heart, and kidney damages. These symptoms are associated with a cytokine storm (166, 167) manifesting elevated serum levels of interleukin (IL) IL-1β, IL-2, IL-7, IL-8, IL-9, IL-10, IL-17, granulocyte colony-stimulating factor (G-CSF), Granulocyte-Macrophage Colony Stimulating Factor (GM-CSF), interferon (IFN)γ, tumor necrosis factor (TNF)α, Interferon gamma-induced protein 10 (IP10), Monocyte Chemoattractant Protein-1 (MCP1), macrophage inflammatory protein 1(MIP1)A and MIP1B (168). IL-22, in collaboration with IL-17 and TNFα, induces antimicrobial peptides in the mucosal organs. IL-22 also upregulates mucins, fibrinogen, anti-apoptotic proteins, serum amyloid A, and LPS binding protein (169); therefore, IL-22 may contribute to the formation of life-threatening oedema with mucins and fibrin (170), seen in SARS-CoV-22 and SARS-CoV patients (168).\nThe 2003 SARS-CoV strain, that also causes severe acute respiratory syndrome, attaches to host cells via host receptor ACE2 (171). This type I integral membrane protein receptor is a well-known receptor for respiratory viruses, and is abundantly expressed in tissues lining the respiratory tract (111). During COVID-19 infection, SARS-CoV-2 also enters host cells via the ACE2 receptor (172). ACE2 is highly expressed on human lung alveolar epithelial cells, enterocytes of the small intestine, and the brush border of the proximal tubular cells of the kidney (99). HSPGs are also one of the preliminary docking sites on the host cell surface and play an important role in the process of SARS-CoV cell entry (99). There is no current confirmed information that SARS-CoV-2 binds to HSPGs, however, LF blocks the infection of SARS-CoV by binding to HSPGs (99). It is not presently known whether LF binds to ACE2, but it does bind to HSPGs (99). Whether SARS-CoV-2 also enters host cells via HPSGs in the same way, as does (the 2003) SARS-CoV clearly warrants further investigation.\nOf particular interest, and in the context of this paper, is the set of interactions between SARS-CoV-2 and host platelets. This is of importance, as COVID-19 infection, can cause hyperinflammation due to a cytokine storm (166). Pathogens like the influenza virus and Francisella tularensis, do trigger life-threatening cytokine storms (173). Such a cytokine storm will significantly affect platelets, as platelets have many receptors where these inflammatory molecules may bind (173) (see Figure 5). Circulating cytokines and inflammagens will hyperactivate platelets, causing low platelet count (thrombocytopenia), and a significant chance of hypercoagulation. Thrombocytopenia is associated with increased risk of severe disease and mortality in patients with COVID-19, and thus serves as clinical indicator of worsening illness during hospitalization (174, 175). Patients with type 2 diabetes are also particularly prone to increased levels of circulating inflammatory cytokines and hypercoagulation (76). COVID-19 patients without other comorbidities but with diabetes are at higher risk of severe pneumonia, excessive uncontrolled inflammatory responses and a hypercoagulable state (176). Guo and co-workers in 2020 also found that serum levels of IL-6, C-reactive protein, serum ferritin, and D-dimer, were significantly higher in diabetic patients compared with those without, suggesting that patients with diabetes are more susceptible to an inflammatory storm eventually leading to rapid deterioration of the patient with COVID-19 (140). Acute pulmonary embolism has also been reported in COVID-19 infection (177). Focal accumulation of activated platelets within the oedematous area ex vivo correlated well with the size of the pulmonary embolism (178). Interestingly, anticoagulant therapy, mainly with (intravenous) heparin (and mainly with low molecular weight heparin, LMWH), appears to be associated with better prognosis in severe COVID-19 patients (179).\nFigure 5 Simplified platelet signaling and receptor activation during disease with main dysregulated molecules thrombin, fibrin(ogen), von Willebrand Factor (vWF) interleukins (IL) like IL-1α, IL-1β, and IL17A and cytokines like TNF-α. Diagram created with BioRender (https://biorender.com/). In COVID-19 infection, LF may have a role to play in not only sequestering iron and inflammatory molecules that are severely increased during the cytokine burst, but also possibly in assisting in occupying receptors and HSPGs to prevent virus binding. Receptor occupancy is an important characteristic of LF, when taken as supplement. Furthermore, it may assist in preventing thrombocytopenia, and hypercoagulation, both prominent features of COVID-19 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