Notes on Innate Immunity: PRRs, Inflammation, Neutrophils, Macrophages, ILCs, and NK Cells

Pattern Recognition Receptors (PRRs) and initial sensing

  • Microbes release PAMPs (pathogen-associated molecular patterns) such as sugars, proteins, and lipids on their surfaces.

  • Damaged host cells release DAMPs (damage-associated molecular patterns), e.g., ATP or misplaced organelle components.

  • PRRs detect PAMPs and DAMPs to recognize infection or tissue damage. A classic example is TLR4 (TLR 4) signaling in response to bacterial components.

  • Upon PRR recognition of PAMPs/DAMPs, two main signaling pathways are engaged:

    • MyD88-dependent pathway: activates nuclear factor kappa B (NF-κB) → transcription of pro-inflammatory cytokines.

    • MyD88-independent pathway (often referred to as TRIF-dependent): activates IRF (Interferon Regulatory Factor) axis → production of interferons (antiviral components).

  • Downstream, recognition leads to inflammasome activation, linking sensing to inflammatory effector functions.

Inflammasomes and cytokine maturation

  • Inflammasomes are multi-protein complexes whose structure can vary depending on the signal (PAMP or DAMP) detected.

  • Primary purpose: activate caspase-1 from its inactive zymogen procaspase-1.

  • Caspase-1 then cleaves inactive cytokine precursors to active cytokines:

    • extprocIL1β<br>ightarrowextIL1βext{proc-IL-1β} <br>ightarrow ext{IL-1β}

    • extprocIL18<br>ightarrowextIL18ext{proc-IL-18} <br>ightarrow ext{IL-18}

  • IL-1β and IL-18 are pro-inflammatory cytokines that initiate and amplify the inflammatory response.

  • Caspase-1 activation can also induce a form of programmed cell death known as pyroptosis, a lytic, inflammatory cell death that helps contain infection.

  • The inflammasome can be activated via signals from PRRs (including the NF-κB-driven production of pro-IL-1β/IL-18) and also directly by DAMPs.

Key cytokinic players and their roles

  • IL-1β and IL-18: pro-inflammatory cytokines central to initiating and propagating inflammation.

  • Interferons (IFNs): antiviral components produced via the IRF pathway; help limit viral replication and modulate immune responses.

  • NF-κB: transcription factor activated via MyD88-dependent signaling; upregulates many inflammatory genes.

  • Pro-inflammatory context: Activation of inflammasomes and cytokines leads to recruitment and activation of additional immune cells.

Big picture: why inflammation matters

  • Presence of microbes in tissue triggers inflammatory signals to recruit leukocytes to the site of infection.

  • Inflammation involves both immune cell recruitment and vascular changes to allow cells and mediators to reach the tissue.

  • While necessary to control infection, excessive or prolonged inflammation can cause tissue damage; therapeutic blockade of PRRs or inflammasome components can reduce inflammation but increases infection risk.

  • In veterinary contexts (e.g., horses), pharmacologic blockade of these pathways has been used to control inflammation, with caveats about infection susceptibility when inflammation is suppressed.


The “dance” of inflammation: from recognition to recruitment

  • Recognized microbes or damaged cells release signals that initiate the inflammatory cascade.

  • Pattern Recognition Receptors (PRRs) are the primary sensors on immune cells.

  • Upon recognition, the NF-κB and IRF pathways are activated via the two main routes (MyD88-dependent and independent).

  • Activation leads to inflammasome formation and production of pro-inflammatory cytokines, particularly IL-1β and IL-18, which set the stage for inflammation.

  • Inflammation involves signaling to nearby blood vessels to become more permeable and to express adhesion molecules that facilitate leukocyte recruitment.

Recruitment of neutrophils: the first responders

  • The first immune cells to arrive at the site of infection are neutrophils (the “lawyers” of the immune system in this analogy).

  • Recruitment steps (extravasation) in order:

    1. Tethering: neutrophils loosely attach to the endothelium.

    2. Rolling: rolling along the vascular surface mediated by selectin–glycoprotein interactions.

    3. Activation and stable adhesion: endothelial receptors (addressins) signal neutrophils; adhesion strengthened by integrins (e.g., LFA-1 which is composed of CD11 and CD18 subunits) binding to ICAM-1.

    4. Arrest and transmigration (diapedesis): neutrophils squeeze through the endothelial barrier into tissue.

    5. Chemotaxis: neutrophils migrate toward the infection using chemokine cues, chiefly IL-8 (CXCL8) and macrophage inflammatory protein-1α (MIP-1α).

  • Addresses on endothelium: endothelial cells express adhesion molecules that act as “addresses” to tell neutrophils where inflammation should occur.

  • CD18 (part of LFA-1) is critical for firm adhesion and stopping the neutrophil at the correct site; deficiency of CD18 can cause leukocyte adhesion deficiency in animals (e.g., cattle and dogs), reducing effective inflammatory responses.

  • The tethering–rolling–adhesion–transmigration sequence ensures that neutrophils exit the bloodstream specifically at sites of infection and inflammation.

Neutrophil functions in the tissue: phagocytosis and extracellular defenses

  • After transmigration, neutrophils recognize microbes via opsonization and surface receptors (e.g., Fc receptors for IgG, complement receptors) that bind tagged pathogens.

  • Cytoplasmic extensions (pseudopods) attach to and engulf microbes, forming a phagosome (an intracellular vesicle).

  • Inside the phagosome, several antimicrobial mechanisms are deployed:

    • Respiratory burst: generation of reactive oxygen species (ROS) via NADPH oxidase, converting oxygen to superoxide and downstream ROS.

    • Approximate reactions:

      • extNADPH+2O<em>2ightarrowextNADP++2O</em>2+H+ext{NADPH} + 2 \, O<em>2 ightarrow ext{NADP}^+ + 2 \, O</em>2^{\cdot-} + H^+

      • O<em>2+2  H+H</em>2O2+OO<em>2^{\cdot-} + 2 \; H^+ \rightarrow H</em>2O_2 + O

    • Oxygen scavenging and reactive species destruction: hydrogen peroxide (H₂O₂) and other ROS damage microbial components.

    • Antimicrobial peptides (e.g., defensins) and digestive enzymes delivered by lysosomes fuse with the phagosome (phagolysosome) to digest microbes.

    • Lactoferrin in phagosomes chelates free iron (Fe³⁺), depriving microbes of iron needed for growth:

    • extFe3++extlactoferrin<br>ightarrowextFelactoferrincomplexext{Fe}^{3+} + ext{lactoferrin} <br>ightarrow ext{Fe-lactoferrin complex}

    • Phagosomal acidification: proton pumps acidify the phagosome, activating hydrolases and optimally functioning antimicrobial enzymes.

    • Lysosomal enzymes: proteases, nucleases, and other hydrolases digest microbial components.

    • The oxidative burst and enzymes together effectively kill most engulfed microbes within the phagosome.

  • PT: Hydrogen peroxide is also used externally in wound care and is generated internally via ROS production to kill microbes inside phagosomes.

  • It is critical that microbes are destroyed within phagosomes; excessive leakage of digestive contents can damage host tissue.

  • NETs (neutrophil extracellular traps): neutrophils can also deploy extracellular traps composed of DNA strands with histones and antimicrobial proteins (e.g., lactoferrin, defensins) to trap and kill microbes outside the cell.

  • Lifespan and limitations:

    • Neutrophils are rapidly mobilized and have a relatively short lifespan; they have limited capacity for repeated phagocytosis.

Monocytes/macrophages: longer-lived defenders and tissue remodelers

  • Circulating monocytes infiltrate tissues and differentiate into macrophages.

  • Macrophages provide a second wave of defense and are more potent than neutrophils, with longer life and the ability to perform repeated phagocytosis.

  • Macrophages can recruit other lymphocytes (T cells and B cells) and help initiate adaptive immune responses by presenting antigens and promoting antibody production.

  • Macrophage polarization:

    • M1 (classically activated, pro-inflammatory):

    • Generate nitric oxide (NO) via nitric oxide synthase (NOS) from arginine; NO contributes to vasodilation and antimicrobial activity.

    • Pro-inflammatory cytokine production helps sustain inflammation.

    • M2 (alternatively activated, anti-inflammatory/healing):

    • Express arginase, converting arginine to ornithine, reducing NO production and promoting tissue repair.

  • Nitric oxide production in macrophages:

    • extArginine<br>ightarrowextNO+extCitrulline ext(viaNOS,especiallyiNOSinactivatedmacrophages)ext{Arginine} <br>ightarrow ext{NO} + ext{Citrulline} \ ext{(via NOS, especially iNOS in activated macrophages)}

  • NO effects: vasodilation, increased blood flow to the site, and antimicrobial activity; NO and reactive nitrogen species contribute to pathogen killing.

  • Macrophage roles beyond killing microbes:

    • Phagocytose dead neutrophils and debris to prevent collateral tissue damage.

    • Remodel connective tissue and aid in tissue repair after infection.

    • Shift from M1 to M2 phenotype over the course of inflammation to promote resolution and healing.

Innate lymphoid cells (ILCs) and natural killer (NK) cells: first responders beyond classic adaptive immunity

  • Innate lymphoid cells (ILCs): lymphocytes that reside in non-lymphoid tissues (e.g., subcutaneous tissues) and lack antigen-specific receptors. They respond to cytokine environments produced by infected or damaged tissues and influence other immune cells.

    • ILC1: secrete interferon-gamma (IFN-γ) and contribute to type 1 responses.

    • ILC2: secrete IL-5 and IL-13, promoting type 2 immunity and tissue repair processes.

    • ILC3: secrete IL-17 and IL-22, contributing to barrier defense and antimicrobial responses.

  • NK cells: specialized innate lymphocytes that kill infected or transformed cells, not by recognizing specific antigens, but by sensing stressed cells.

    • NK cells determine whether a cell is infected by detecting stress signals and/or reduced MHC class I expression on target cells.

    • Mechanism: degranulation releasing perforin and granzymes to induce apoptosis in the infected cell, thereby preventing replication and spread of pathogen.

    • NK cells can also secrete cytokines (e.g., IFN-γ) to further modulate the immune response.

  • MHC dependence and horse-specific notes:

    • NK recognition often involves interactions with MHC class I on target cells; healthy cells expressing normal MHC I inhibit NK activation via inhibitory receptors.

    • Infected or stressed cells often downregulate MHC I, removing inhibitory signals and allowing NK cell-mediated killing.

    • Horses differ in inhibitory receptors: they possess the LY-49 receptor (an NK-inhibitory receptor) and may lack certain other receptor types found in some other species; some farm animals have both, but horses rely on LY-49 for this inhibitory function.

  • Innate cytokine signaling by ILCs: three major ILC types secrete characteristic cytokines (as listed above), enabling rapid, antigen-independent regulation of inflammation and tissue homeostasis.

Putting it all together: the sequence of innate immune responses to infection

  • Step 1: Recognition

    • PRRs detect PAMPs and DAMPs (e.g., TLR4 detects LPS; other PRRs detect various microbial components and damaged self-signals).

    • Activation of MyD88-dependent and MyD88-independent pathways leads to NF-κB–driven cytokine transcription and IRF-driven interferon production, respectively.

    • Inflammasomes are activated, caspase-1 is activated, and IL-1β/IL-18 are produced (and can induce pyroptosis in infected cells).

    • This recognition represents the initial “alarm signal” that infection is present and needs to be contained.

  • Step 2: Inflammation and vascular changes

    • Inflammation is initiated; cytokines promote vasodilation and increased vascular permeability, allowing fluid and leukocytes to exit the bloodstream and enter tissue.

    • Endothelial cells express “addresses” (adhesion molecules) that guide neutrophil extravasation to the site of infection.

    • NO production by macrophages and other cells contributes to vasodilation and further enhances tissue perfusion.

  • Step 3: Recruitment of neutrophils and macrophages

    • Neutrophils arrive first and perform rapid phagocytosis and extracellular defense (NETs).

    • Monocytes follow and differentiate into macrophages (M1 then M2 shift as inflammation resolves).

  • Step 4: Effector antimicrobial actions

    • Neutrophils: phagocytose microbes into phagosomes; kill via ROS (NADPH oxidase) and antimicrobial enzymes; acidify phagosomes to optimize enzyme activity; release lactoferrin to sequester iron; can deploy NETs for extracellular killing.

    • Macrophages: continue phagocytosis, generate NO (via iNOS) to kill microbes and promote vasodilation; M2 macrophages promote tissue repair and anti-inflammatory functions; recruit lymphocytes and coordinate adaptive responses.

  • Step 5: Bridging to adaptive immunity

    • Macrophages present antigens and recruit T and B cells; this supports antibody production and a targeted adaptive response.

    • NK cells monitor for infected cells; they kill stressed cells and secrete cytokines to shape subsequent immune responses.

  • Step 6: Resolution and repair

    • M2 macrophages promote tissue repair, remodeling, and suppression of excessive inflammation.

    • Inflammation declines as pathogens are cleared and tissue integrity is restored; excessive persistence of inflammatory signals can cause collateral tissue damage.


Practical implications and examples

  • Therapeutic modulation: Drugs that block PRRs or inflammasome components can reduce inflammation (e.g., in horses), but at the cost of increased susceptibility to infections.

  • Balance of inflammation: Early neutrophil responses are essential for containment, but prolonged neutrophil activity and cytokine production can cause tissue damage if not resolved.

  • Relevance to clinical disease: Dysregulation of these pathways can contribute to inflammatory diseases, sepsis, and chronic inflammatory conditions; understanding the sequence helps tailor interventions (e.g., timing of anti-inflammatory therapy).

  • Species differences: Receptor repertoires vary among species (e.g., the LY-49 NK receptor in horses vs other mammals); these differences influence how innate immunity operates in different animals.


Key takeaways (big picture)

  • PRRs detect PAMPs and DAMPs and initiate two main signaling axes: MyD88-dependent NF-κB activation for cytokines and MyD88-independent IRF activation for interferons.

  • Inflammasomes activate caspase-1, which matures IL-1β and IL-18, driving inflammation and potentially pyroptotic cell death.

  • Inflammation proceeds through neutrophil recruitment (tethering, rolling, adhesion via CD18/LFA-1, transmigration, chemotaxis) and phagocytosis, with phagosomal killing via ROS, proteases, lactoferrin, and acidification.

  • NETs provide extracellular antimicrobial defense when neutrophils cannot contain infection intracellularly.

  • Monocytes/macrophages follow neutrophils, differentiating into M1 (pro-inflammatory, NO production) and M2 (anti-inflammatory, tissue repair) phenotypes, and bridging innate and adaptive immunity by recruiting T and B cells.

  • Innate lymphoid cells (ILCs) and NK cells furnish rapid, non-antigen-specific responses; NK cells kill infected cells via granule release and can be regulated by MHC I interactions and stress signals.

  • No single component works alone; the coordinated interplay among PRR signaling, inflammasomes, cytokines, phagocytes, macrophages, and NK/ILCs constitutes the core of the innate immune response and its transition to adaptive immunity.

Note: The content above reflects the lecture’s emphasis on pathways, cell types, and their interactions, including the practical implications of anti-inflammatory therapies and species-specific differences in innate immunity.