Case 2 - BBS2042

Case 2 - Cell-derived Molecules as Signalling Mediators

1. Learning Goals

  • Types of Signalling Molecules

    • Peptides

    • Purines

    • Pyrimidines

    • Proteins

    • Lipids

    • Gasses

    • Neurotransmitters: excitatory and inhibitory

  • Types of Vesicles and Formation

  • Signalling Molecule Production

    • Involves proteins and includes simple steps

  • Secretion of Signalling Molecules

    • Primarily proteins

  • Extracellular Vesicle Induced Signalling

    • Mechanism of signalling in target cells

  • Gases as Signalling Molecules

    • Production, secretion, and function in tissues:

    • Nitric oxide (NO): role in the cardiovascular system

    • Carbon monoxide (CO)

    • Hydrogen sulfide (H₂S)

2. What are Signalling Molecules?

  • Definition: Signalling molecules (ligands) are substances released by cells that bind to specific receptors on target cells to trigger a biological response.

  • The Chemical Nature determines:

    • How they are synthesized

    • How they are released

    • Whether they can cross membranes

    • What type of receptor they bind

    • How fast and long-lasting their effects are

2.1 Peptide and Protein Signalling Molecules

  • Description:

    • Peptides: Short chains of amino acids

    • Proteins: Longer, folded chains of amino acids

  • Examples:

    • Peptides: insulin, glucagon, vasopressin, oxytocin

    • Proteins: growth hormone, cytokines (e.g., IL-2, TNF-α), erythropoietin

    • Neuropeptides: substance P, endorphins

  • Transport & Receptors:

    • Hydrophilic → cannot cross lipid bilayers

    • Bind cell-surface receptors such as:

    • GPCRs

    • Ionotropic receptors

    • Receptor tyrosine kinases (RTKs)

    • Cytokine receptors (JAK/STAT)

  • Signalling Characteristics:

    • Fast onset, often short-lived

    • Amplified via second messengers (cAMP, Ca²⁺, IP₃)

  • Typical Roles:

    • Endocrine signalling (hormones)

    • Paracrine/autocrine signalling (growth factors, cytokines)

    • Synaptic neuromodulation

2.2 Purines and Pyrimidines (Nucleotide-based Signalling)

  • Definition: These are nucleotides or nucleosides, not nucleic acids.

  • Main Molecules:

    • Purines: ATP, ADP, adenosine

    • Pyrimidines: UTP, UDP

  • Where They Act:

    • Especially important in:

    • Nervous system

    • Immune system

    • Vascular signalling

  • Receptors:

    • P1 Receptors (Adenosine Receptors)

    • GPCRs (A₁, A₂A, A₂B, A₃)

    • Often inhibitory or modulatory

    • P2 Receptors (Nucleotides)

    • P2X: ligand-gated ion channels (fast response)

    • P2Y: GPCRs (slower, modulatory)

  • Signalling Features:

    • Very rapid signalling (especially P2X)

    • Often short range (paracrine)

    • Quickly degraded by ecto-nucleotidases

  • Typical Functions:

    • Neurotransmission

    • Pain signalling

    • Inflammation

    • Platelet aggregation

    • Vasodilation/constriction

2.3 Lipid-derived Signalling Molecules

  • Definition: Hydrophobic or amphipathic molecules derived from membrane lipids

  • Steroids:

    • Derived from cholesterol

    • Examples:

    • Cortisol

    • Aldosterone

    • Estrogen, testosterone

    • Properties:

    • Cross membranes freely

    • Bind intracellular (nuclear) receptors

    • Act as transcription factors leading to slow onset, long-lasting effects

  • Eicosanoids:

    • Derived from arachidonic acid

    • Examples:

    • Prostaglandins

    • Thromboxanes

    • Leukotrienes

    • Characteristics:

    • Made on demand (not stored)

    • Act locally (paracrine/autocrine)

    • Bind GPCRs

    • Functions:

    • Inflammation

    • Pain

    • Fever

    • Smooth muscle tone

  • Phospholipid Derivatives:

    • Examples:

    • DAG (diacylglycerol)

    • IP₃ (technically water-soluble, but lipid-derived)

    • PIP₃

    • Roles:

    • Serve as second messengers inside cells

    • Control Ca²⁺ release, PKC activation, Akt signalling

  • Endocannabinoids:

    • Examples:

    • Anandamide

    • 2-AG

    • Bind CB₁/CB₂ GPCRs

    • Involved in retrograde signalling in synapses

2.4 Small-molecule Signalling

  • Examples:

    • Gases: NO, CO, H₂S

    • Amino Acids: glutamate, GABA, glycine

    • Biogenic Amines: dopamine, serotonin, histamine

  • Key Properties:

    • Often very fast

    • Short half-life

    • Act via ion channels or GPCRs

2.5 Comparison Overview


  • Classes of Signalling Molecules:

    Class

    Membrane Crossing

    Receptor Type

    Speed

    Duration


    Peptides / proteins

    Cell-surface

    Fast

    Short


    Purines / pyrimidines

    GPCRs / ion channels

    Very fast

    Very short


    Steroid lipids

    Intracellular

    Slow

    Long


    Eicosanoids

    ❌ (mostly)

    GPCRs

    Moderate

    Short


    Gases

    Intracellular

    Very fast

    Very short

    3. What Qualifies as a Neurotransmitter?

    • A molecule is considered a neurotransmitter if it meets all the following criteria:

      1. Is synthesized in the neuron

      2. Is stored in synaptic vesicles (classically; with some exceptions like NO)

      3. Is released upon presynaptic depolarization (Ca²⁺-dependent)

      4. Binds to specific receptors on the postsynaptic cell

      5. Is terminated by reuptake, degradation, or diffusion

    • Excitatory vs. Inhibitory Neurotransmitters:

      • Excitatory: Leads to depolarization (EPSP)

      • Inhibitory: Leads to hyperpolarization or shunting (IPSP) which increases threshold for excitatory neurotransmitters

    3.1 Neurotransmitter Examples

    • Glutamate:

      • Function: Excitatory

      • Accounts for approximately 80% of synaptic transmission in CNS

      • Essential for learning, memory, and plasticity

      • Receptor Type: Ionotropic receptor (fast response)

    • GABA:

      • Function: Inhibitory (in the brain)

      • Synthesized from glutamate via glutamate decarboxylase (GAD)

      • Receptor Types: GABA A, GABA B, GABA C receptors

    • Glycine:

      • Function: Inhibitory (in the spinal cord and brainstem)

      • Major inhibitory transmitter in spinal motor circuits

      • Mechanism: Ligand-gated Cl⁻ channels; blocked by strychnine

    4. What are Vesicles?

    • Definition: Vesicles are small, membrane-bound compartments that transport cargo (proteins, lipids, neurotransmitters) between cellular compartments or to/from the plasma membrane.

    • Their identity is defined by:

      • Coat proteins (how they form)

      • Cargo they carry

      • Direction of transport

    4.1 COPII Vesicles (ER → Golgi)
    • Function: Transport newly synthesized proteins from the rough ER to the Golgi.

    • Formation Steps:

      1. Sar1 Activation:

      • Sar1 (a small GTPase) binds GTP

      • Inserts into ER membrane and initiates curvature

      1. Inner Coat Assembly:

      • Sar1 recruits Sec23/Sec24

      • Sec24 binds cargo or cargo receptors

      1. Outer Coat Assembly:

      • Sec13/Sec31 form a cage around the vesicle

      1. Budding and Scission:

      • The vesicle buds off from ER

      1. Uncoating:

      • GTP hydrolysis → coat disassembles

    • Key Idea: COPII moves proteins forward in the secretory pathway.

    4.2 COPI Vesicles (Golgi → ER, intra-Golgi)
    • Function: Retrograde transport; returns ER-resident proteins and redistributes Golgi enzymes.

    • Formation Steps:

      1. ARF1 Activation:

      • ARF1-GTP inserts into Golgi membrane

      1. Coatomer Recruitment:

      • Multi-subunit COPI coat binds ARF1

      1. Cargo Selection:

      • Recognizes retrieval signals (e.g., KDEL)

      1. Budding and Release:

      • Vesicle forms and detaches

      1. Uncoating:

      • ARF1 hydrolyzes GTP → coat falls off

    • Key Idea: COPI is mainly a recycling vesicle system.

    4.3 Secretory Vesicles
    • Description: These are not coat-defined in the same way as COP or clathrin vesicles.

    • Constitutive Secretory Vesicles:

      • Function: Continuous delivery of:

      • Membrane proteins

      • Lipids

      • Extracellular matrix (ECM) components

      • Characteristics:

      • Default pathway

      • No storage

      • Vesicles fuse with membrane immediately

    • Regulated Secretory Vesicles:

      • Function: Store signalling molecules (e.g., hormones, neuropeptides)

      • Characteristics:

      • Dense-core vesicles

      • Cargo often processed inside vesicle

      • Require Ca²⁺ signal for fusion

    4.4 Multivesicular Bodies (MVBs)
    • Definition: Endosomes containing intraluminal vesicles (ILVs) that sit at a decision point:

      • Fates:

      • Degradation

      • Secretion

    MVB Formation Steps
    1. Early endosome formation

      • From endocytosis

    2. Inward budding

      • Endosomal membrane buds into the lumen forming ILVs

      • Requires ESCRT complexes

    3. Cargo sorting

      • Ubiquitinated proteins preferentially included

      • Removes receptors from plasma membrane

    4.5 ESCRT-Dependent Pathway
    • Definition: The Endosomal Sorting Complex Required for Transport (ESCRT) is the primary machinery used.

    • Process:

      • ESCRT complexes (0, I, II, III) sort cargo, deform the membrane, and abscise (cut) the vesicles.

    4.6 Exosomes (Extracellular)
    • Definition: Small extracellular vesicles (30–150 nm) released when MVBs fuse with the plasma membrane.

    • Formation Steps:

    1. Endocytosis: Inward budding of membranes → forms early endosome

    2. ILVs Formation: Are formed inside multivesicular bodies (MVB)

    3. MVB Fusion: MVB fuses with plasma membrane

    4. Release: ILVs released as exosomes into the extracellular space

    • Exosome Cargo:

      • Proteins

      • Lipids

      • mRNA

      • miRNA

      • Signalling molecules

    • Functions:

      • Intercellular communication

      • Immune modulation

      • Development

      • Cancer signalling

      • Biomarkers (liquid biopsies)

    4.7 Microvesicles (Ectosomes, Extracellular)
    • Definition: Larger extracellular vesicles (100–1000 nm) formed by direct outward budding of the plasma membrane into the extracellular space.

    • Process:

      • Involves blebbing (membrane that draws together) and fission (pinching off the membrane), done by the cytoskeleton

    • Key Features:

      • No MVB involvement

      • Actin-dependent

      • Different composition from exosomes

      • Uses regulatory hormones and neurotransmitters

    5. Production and Secretion of Signalling Molecules

    5.1 Gene Transcription (Nucleus)
    • Process:

      • The gene encoding the signalling protein is transcribed into mRNA.

      • mRNA is processed (capping, splicing, poly-A tail).

      • mRNA exits the nucleus via nuclear pores.

    • Vesicles involved: None

    5.2 Translation and Targeting to the Rough ER
    • Process:

      • Translation begins on a cytosolic ribosome.

      • An N-terminal signal peptide emerges, and the signal recognition particle (SRP) binds the signal peptide.

      • Ribosome is targeted to the rough ER and translation continues with the protein entering the ER lumen.

    • Product: Preproprotein

    • Vesicles involved: None

    5.3 Protein Folding and Early Processing in the ER
    • Process:

      • Signal peptide is cleaved → proprotein

      • Protein folds into its correct conformation.

      • Disulfide bonds form (if required).

      • ER quality control removes misfolded proteins.

    • Vesicles involved: None (still within ER lumen)

    5.4 Export from ER via COPII Vesicles
    • Process:

      • Properly folded proproteins are selected for transport.

      • COPII vesicles bud from the ER membrane.

    • Step-by-step:

      1. ER quality control

      • Only properly folded proteins can exit the ER; misfolded proteins are retained and degraded (ERAD).

      1. Export signals on cargo

      • Many secreted proteins contain ER export motifs:

        • Di-acidic (DXE)

        • Di-hydrophobic

      1. Cargo receptors

      • Soluble proteins cannot directly bind coat proteins.

      • They bind cargo receptors (transmembrane proteins) whose cytosolic tail binds Sec24 (COPII).

      1. COPII coat recruitment

      • Sar1-GTP initiates curvature; Sec23/24 capture cargo; Sec13/31 complete the vesicle.

    • Key Idea: COPII vesicles selectively package proteins that are folded, tagged, and receptor-bound.

    • Function: ER → Golgi transport

    • Vesicle involved: COPII

    5.5 Transport and Processing in the Golgi Apparatus
    • Process:

      • COPII vesicles fuse with the cis-Golgi.

      • Protein moves through the:

      • cis-Golgi

      • medial-Golgi

      • trans-Golgi

    • Processing in Golgi:

      • Glycosylation

      • Sulfation

      • Proteolytic trimming

      • Sorting signals added

    • Vesicles involved:

      • COPI vesicles recycle Golgi enzymes backward

      • COPI vesicles return escaped ER proteins

    • Vesicle involved: COPI (indirectly, recycling)

    5.6 Sorting at the Trans-Golgi Network (TGN)
    • Description: The TGN is the major sorting hub where the protein is sorted into one of two pathways:

      • Constitutive Secretion (Default pathway for most cells)

      • Process:

        • Protein is packaged into constitutive secretory vesicles which bud from the TGN and move directly to the plasma membrane, fusing immediately.

        • Release: Continuous.

      • Examples: ECM proteins, growth factors

      • Vesicle involved: Constitutive secretory vesicle

      • Regulated Secretion (Used by endocrine and neuronal cells)

      • Immature Secretory Granules:

        • Protein is packaged into regulated secretory vesicles, often still in inactive pro-form which bud from the TGN.

      • Step-by-step:

        1. Sorting Signals in Cargo:

        • Specific peptide motifs promote entry into regulated vesicles (aggregation-prone domains, pH–dependent interactions).

        1. Cargo Aggregation:

        • In the TGN (low pH, high Ca²⁺), prohormones aggregate.

        1. Sorting Receptors:

        • Some proteins bind TGN sorting receptors, clustering cargo into dense-core granules.

        1. Proteolytic Processing:

        • Proproteins often enter vesicles inactive; proteases generate the active signalling molecule.

        1. Result:

        • Formation of immature secretory granules, highly enriched in specific cargo.

    • Lysosomal Sorting:

      • Proteins destined for lysosomes carry mannose-6-phosphate (M6P) which binds cargo in TGN and is packaged into clathrin-coated vesicles.

      • This is not used for signalling molecule secretion, but it's an important distinction.

    5.7 Vesicle Maturation
    • Inside regulated secretory vesicles:

      • Proproteins are cleaved into active forms

      • Cargo becomes concentrated

      • Vesicles become dense-core granules

    • Vesicle involved: Regulated secretory vesicle

    5.8 Storage
    • Description: Mature vesicles are stored near the plasma membrane with release waiting for a stimulus.

    5.9 Stimulus-dependent Exocytosis
    • Process:

    • External signal triggers Ca²⁺ influx which activates SNARE proteins to mediate membrane fusion.

    • The vesicle fuses with the plasma membrane and the signalling molecule is released extracellularly.

    Vesicle Targeting and Docking
    1. Rab GTPases:

      • Each vesicle carries specific Rab proteins which interact with:

      • Tethering complexes on target membrane to ensure vesicles dock at the correct membrane.

    2. Tethering:

      • Long tethering proteins capture vesicles and bring them close to the plasma membrane.

    SNARE-mediated Membrane Fusion
    • SNARE Proteins:

      • v-SNAREs (on vesicle)

      • t-SNAREs (on target membrane)

    • Step-by-step Fusion:

      1. SNARE Pairing:

      • v-SNARE and t-SNAREs form a complex that pulls membranes together.

      1. Membrane Destabilization:

      • Lipid bilayers distort and a fusion pore begins to form.

      1. Fusion Pore Opening:

      • Vesicle lumen connects to extracellular space.

    Regulation of Exocytosis
    • Constitutive Exocytosis:

      • SNAREs alone are sufficient, with fusion occurring as soon as the vesicle arrives.

    • Regulated Exocytosis (key for signalling molecules):

      1. Priming:

      • Vesicles are docked but restrained with a partially assembled SNARE complex.

      1. Triggering Signal:

      • Ca²⁺ influx (via voltage-gated channels).

      1. Calcium Sensor:

      • Synaptotagmin binds Ca²⁺, releasing the fusion clamp.

      1. Rapid Fusion:

      • Full SNARE zippering and cargo release occurs in milliseconds–seconds.

    • After fusion:

      • Vesicle membrane becomes part of the plasma membrane.

      • SNAREs are recycled.

      • Membrane excess is removed by endocytosis.

    5.10 Post-secretion Fate
    • Outcomes for the signalling protein:

      • Binds its receptor

      • Degraded extracellularly

      • Or is internalized via clathrin-mediated endocytosis

    6. How Extracellular Vesicles Induce Signalling in Target Cells

    6.1 Release of Extracellular Vesicles from Donor Cell
    • Exosomes:

      • Form inside multivesicular bodies (MVBs) and released when MVBs fuse with the plasma membrane.

    • Microvesicles (Ectosomes):

      • Bud directly outward from the plasma membrane.

    • EV content includes:

      • Membrane proteins (ligands, receptors)

      • Lipids

      • Cytosolic proteins

      • mRNA, miRNA, other ncRNAs

    6.2 EV Transport through the Extracellular Environment
    • EVs can diffuse locally (paracrine) or travel via blood, lymph, interstitial fluid.

    • Protection Advantage:

      • The lipid bilayer protects cargo from:

      • Proteases

      • RNases

      • Harsh extracellular conditions

    6.3 Target Cell Recognition and Binding
    • EVs do not bind randomly; targeting is selective.

    • Mechanisms of Specificity:

      • Surface Ligand–Receptor Interactions:

      • EV membrane proteins bind receptors on target cells such as:

        • Integrins

        • Tetraspanins (CD9, CD63, CD81)

        • Growth factor ligands

      • Lipid-Based Recognition:

      • EVs enriched in phosphatidylserine and sphingolipids are recognised by lipid-binding receptors on target cells

      • Extracellular Matrix Trapping:

      • EVs can bind ECM components, creating local signalling niches

    6.4 Modes of EV-Induced Signalling
    • Core Concept: EVs can signal in multiple fundamentally different ways.

    • Surface Signalling (no uptake required):

      • Receptor activation at the plasma membrane occurs when EV membrane proteins act as ligands, binding to receptors on the target cell and triggering classical signalling cascades.

    • Examples:

      • Growth factor signalling

      • Immune checkpoint signalling

      • Notch-like juxtacrine signalling (EV-bound ligands)

    • EVs function as mobile signalling platforms rather than delivery vehicles.

    • Endocytosis followed by Signalling from Endosomes:

      • EVs are taken up by clathrin-mediated endocytosis, caveolin-mediated endocytosis, macropinocytosis, or phagocytosis (immune cells).

    • Endosomal Signalling:

      • EV membrane proteins remain intact within early or late endosomes, where receptors or ligands signal from endosomal membranes.

    • Importance: Endosomal signalling is prolonged, spatially regulated, and often differs from surface signalling.

    • Cargo Release into the Cytosol:

      • EV membrane fuses with endosomal membrane or becomes leaky, allowing EV contents to enter the cytosol.

    • Functional Cargo Action:

      1. RNA-Mediated Signalling:

      • miRNAs repress target mRNAs, altering gene expression and causing long-term phenotypic changes.

      1. Protein Delivery:

      • EVs may deliver enzymes, transcription factors, and signalling intermediates, constituting horizontal transfer of functional molecules.

    • Lysosomal Processing followed by Signalling:

      • EVs delivered to lysosomes can have their cargo degraded, with breakdown products (e.g., lipids, peptides) potentially activating intracellular sensors or modulating metabolism/inflammation.

    6.5 Downstream Cellular Responses
    • Depending on the signalling mode, EVs can induce:

      • Changes in gene expression

      • Altered proliferation

      • Differentiation

      • Migration

      • Immune activation or suppression

      • Metabolic reprogramming

    • Time Scale:

      • Surface signalling → fast (minutes)

      • Endosomal signalling → intermediate

      • RNA/protein cargo → slow (hours–days)

    6.6 Signal Termination
    • Mechanism:

      • EV–receptor complexes are internalised, cargo is degraded, miRNAs diluted over time, and EV membranes recycled.

    7. General Principles of Gaseous Signalling Molecules

    • Characteristics of Gaseous Signalling Molecules:

      • Are small, diffusible gases

      • Are not stored in vesicles

      • Synthesized on demand

      • Diffuse freely across membranes

      • Act locally (paracrine / autocrine)

      • Have very short half-lives

    • Significance of Diffusion:

      • Freely diffusing gases do not require secretion machinery or classical membrane receptors.

    7.1 General Signalling Logic (All Gasotransmitters)
    • Step-by-step:

      1. Stimulus activates a synthesizing enzyme

      2. Gas is produced in the cytosol

      3. Gas diffuses out of the producing cell

      4. Gas diffuses into neighbouring cells

      5. Gas binds intracellular targets

      6. Gas is rapidly inactivated or degraded

    7.2 Nitric Oxide (NO)
    • Production:

      • Enzyme: Nitric oxide synthase (NOS)

    • Isoforms:

      • nNOS: found in neurons; Ca²⁺-dependent

      • eNOS: found in endothelium; Ca²⁺-dependent

      • iNOS: found in immune cells; Ca²⁺-independent

    • Reaction:
      L-arginine + O₂ + NADPH → NO + L-citrulline

    • Cofactors: BH₄, FAD, FMN

    • Release / Secretion:

      • NO is not secreted but immediately diffuses across membranes acting within ~100–200 µm

    • Target and Signalling Mechanism:

      • Primary target: soluble guanylyl cyclase (sGC)

      1. NO binds heme group on sGC

      2. sGC converts GTP to cGMP

      3. cGMP activates:

        • PKG → intracellular Ca²⁺ decrease → smooth muscle relaxation

        • Ion channels

        • Phosphodiesterases

    • Major Tissue Functions:

      • Vascular System:

      • Acetylcholine activates calcium-calmodulin binding, producing NO leading to vasodilation.

      • Nervous System:

      • Acts as a retrograde neurotransmitter modulating synaptic plasticity (Long-Term Potentiation, LTP).

      • Immune System:

      • iNOS produces large amounts of NO which is cytotoxic to pathogens.

    • Termination:

      • Rapid oxidation to nitrate/nitrite, reaction with hemoglobin, or formation of free radicals may occur.

    7.3 Carbon Monoxide (CO)
    • Production:

      • Enzyme: Heme oxygenase (HO)

    • Reaction:
      Heme → CO + biliverdin + Fe²⁺

    • Release / Secretion:

      • CO diffuses freely from the producing cell and is present in lower concentrations than NO.

    • Target and Signalling Mechanisms:

    • Targets:

      • Soluble guanylyl cyclase (less potent than NO)

      • Ion channels (K⁺, Ca²⁺ channels)

      • Mitochondrial enzymes

    • Major Tissue Functions:

      • Nervous System:

      • Involved in neuromodulation and circadian rhythm regulation.

      • Vascular System:

      • Contributes to vasodilation (weaker than NO).

      • Cytoprotection:

      • Exhibits anti-inflammatory and anti-apoptotic properties.

    • Termination:

      • CO binds to hemoglobin with high affinity and undergoes oxidation in tissues.

    7.4 Hydrogen Sulfide (H₂S)
    • Production:

    • Enzymes: CBS (brain), CSE (cardiovascular), 3-MST (mitochondria) using substrates like cysteine and homocysteine.

    • Release / Secretion:

      • H₂S diffuses freely across membranes and can also be stored in bound sulfane sulfur pools.

    • Target and Signalling Mechanisms:

    • Mechanisms:

      1. Ion Channel Modulation:

      • Opens K_ATP channels and alters Ca²⁺ channels.

      1. Protein Sulfhydration:

      • Modifies cysteine residues and alters enzyme activity.

    • Major Tissue Functions:

      • Cardiovascular System:

      • Promotes vasodilation and offers cardioprotection.

      • Nervous System:

      • Involved in synaptic modulation and neuroprotection.

      • Metabolism:

      • Regulates mitochondrial respiration.

    • Termination:

      • Occurs through mitochondrial oxidation and binding to metalloproteins.

    7.5 Comparison of NO, CO, and H₂S
    • Features:
      | Feature | NO | CO | H₂S |
      |---------------------|-------------|-------------|-------------|
      | Enzyme | NOS | HO | CBS / CSE / 3-MST |
      | Stored? | ❌ | ❌ | Limited |
      | Diffusion | Free | Free | Free |
      | Main Target | sGC | sGC, ion channels | Ion channels, proteins |
      | Speed | Very fast | Fast | Moderate |
      | Half-life | Seconds | Minutes | Minutes |
      | Toxic at high levels | Yes | Yes | Yes |