Form and Function of the Vertebrate and Invertebrate Blood-Brain Barriers
Abstract
:1. Introduction
1.1. Goals of This Review
1.2. The Historical and Current Focus on BBB of Humans
1.3. Evolution of Blood-Brain Barriers
2. The Blood-Brain Barrier of Mammals
2.1. Form and Function of the Mammalian Blood-Brain Barrier
2.1.1. Form
2.1.2. Function
2.2. Factors Altering BBB Function
2.2.1. Development
2.2.2. Nutrition
2.2.3. Hypoxia
2.2.4. Ambient Temperature
2.2.5. Psycho-Social Stress
2.2.6. BBB and Developmental Malleability
2.2.7. Environmental Toxicants and Pollutants
2.3. Special Considerations
2.4. Knowledge Gaps/Limitations
- What are the unique characteristics of BBBs of mammals that inhabit different environments (e.g., aquatic versus terrestrial, high-altitude versus sea level, cold versus hot)?
- How does the form and function of the BBB of wild mammals differ from that of laboratory mammals?
- What are the implications of the behavior on BBB function in mammals, especially characteristics associated with social versus non-social animals?
- What is the impact of parental strategies and maternal care on mammalian BBB (humans versus marsupials versus rodents)?
- What is the impact of environmental contaminants on the BBB of mammals that inhabit polluted areas?
- What are the factors that influence the development of the mammalian BBB across species?
3. The Blood-Brain Barrier of Birds
3.1. Form and Function of the Avian Blood-Brain Barrier
3.2. Unique Features of the Avian Blood-Brain Barrier
3.3. Factors Altering the Avian Blood-Brain Barrier
3.3.1. Nutrition
3.3.2. Temperature
3.3.3. Special Considerations: Migration, Navigation, Altitude, and Attitude (Mating Behavior)
3.4. Knowledge Gaps/Limitations
- Beyond early embryonic and fetal stages of life, how does the BBB of birds differ from mammalian BBB?
- What role does the BBB play in navigation during migration in birds?
- What is the function of the blood barrier that surrounds the glycogen body of birds?
- Does thiamine deficiency, and nutritional deficiency in general, cause behavioral derangement in birds through disruption of the BBB?
- Does the BBB play a significant role in the mating behavior and mating success of birds?
- Can maternally-derived egg yolk factors and eggshell characteristics of oviparous bird species alter the trajectory of BBB development?
4. The Blood-Brain Barrier of Reptiles
4.1. Form of the Reptilian Blood-Brain Barrier
4.2. Factors Altering Reptilian Blood-Brain Barrier Function
4.3. Other Characteristics of the Reptile Blood-Brain Barrier
4.3.1. Regeneration
4.3.2. Protein Synthesis
4.3.3. Ion Transport and Enzyme Activity
4.4. Knowledge Gap/Limitations
- What are the similarities and differences between reptiles and other vertebrates, perhaps especially focusing on the similarities of birds as their closest relatives?
- Do those reptiles that generally show systemic regenerative properties also have blood-brain barriers that have high self-repair capabilities?
- What are the functional capacities of the reptile BBB with respect to transport of ions, glucose, and other key materials?
- Given how little is known about tight junctions in the reptilian BBB, how representative are the few data available?
- Given how little is known about ion transport in the reptilian BBB, how representative are the few data available?
- Can the ‘ancient’ extant reptiles—i.e., the crocodilians—tell us about the evolutionary history of the reptilian BBB?
5. The Blood-Brain Barrier of Amphibians
5.1. Form of the Amphibian Blood-Brain Barrier
5.2. Function of the Amphibian Blood-Brain Barrier
5.3. Factors Altering Amphibian Blood-Brain Barrier Function
5.3.1. Hypoxia and Hypothermia
5.3.2. Hypertonicity
5.3.3. Hydrostatic Pressure
5.3.4. Biologically Active Compounds
5.3.5. Viral Infection
5.3.6. The Blood-Brain Barrier and Nerve Regeneration
5.4. Other Characteristics of the Amphibian Blood-Brain Barrier
5.4.1. Protein Synthesis
5.4.2. Ion Transport and Enzyme Activity
5.5. Knowledge Gap/Limitations
- How does the process of metamorphosis, and the associated apoptosis of the PNS in the trunk, as well as the growth of innervation into the growing limbs, alter the integrity of the neurovascular boundaries?
- What effects do potentially large changes in temperature, salinity, and oxygen have on the effectiveness of the amphibian BBB barrier?
- Does the degree of terrestriality affect neural function and especially the integrity of the amphibian BBB?
- Does the considerable regenerative ability of amphibians translate into greater repair capabilities of an injured BBB?
- What differences, if any, exist between the blood-brain barrier of Anura (frogs and toads), Urodela (salamanders and newts), and Apoda (caecilians)?
- Given how little is known about ion and nutrient transport in the reptilian BBB, how representative are the few data available?
6. The Blood-Brain Barrier of Fish
6.1. Form of the Piscine Blood-Brain Barrier
6.1.1. Mature Fish
6.1.2. Developing Fish
6.2. Function of the Piscine Blood-Brain Barrier
6.2.1. Protective Barrier
6.2.2. Ion Transport and Enzyme Activity
6.3. Factors Altering Piscine BBB Function
6.3.1. Environmental Contaminants
6.3.2. Microbial Infection
6.3.3. Nitric Oxide
6.3.4. Hyperosmotic Stress
6.4. Knowledge Gaps/Limitations
- Does the increased neurogenesis found in fish impact the BBB?
- What undiscovered factors alter the BBB, and how do they alter function as well as form? Many studies thus far have focused mainly on how form is altered, but little is known about functional characteristics that may also be impacted.
- How does the life history of different fishes impact their BBB structure?
- Why do elasmobranchs and sturgeons have a glial BBB—what adaptive value does this provide?
- What are the mechanisms linking disruption of the BBB and behavior?
- How does the glial barrier seen in sturgeons and elasmobranchs develop compared to the endothelial barrier seen in other fish?
7. Blood-Brain Barriers of Non-Vertebrate Chordates—Cephalochordata and Tunicata
8. The Blood-Brain Barrier of Non-Chordate Deuterostome Invertebrates
9. The Blood-Brain Barrier of Protostome Invertebrates
9.1. Arthropods
9.1.1. Form
9.1.2. Function
9.1.3. Factors Altering Structure and Function
9.2. Molluscs
9.2.1. Form
9.2.2. Function
9.3. Knowledge Gaps/Limitations for Invertebrate Blood-Brain Barriers
- Are there differences in BBB function between arthropod taxa with tight junctions in their (sub)perineurium (e.g., the emerging spider model Parasteatoda tepidariorum) and those without (e.g., Drosophila)?
- What is the influence of terrestriality on presence and tightness of the BBB in invertebrates (e.g., aquatic vs. terrestrial snails; marine vs. freshwater vs. terrestrial decapods; aquatic insect larvae vs. terrestrial adults)?
- Can differences in salinity and thus hemolymph osmolarity be correlated with differences in BBB tightness in closely related species (e.g., lobsters vs. crayfish), thus pointing towards evolutionary causes?
- What is the influence of higher sensory input on presence and tightness of the BBB (e.g., comparison within insects, crustaceans, or cephalopods)?
- Are there trends towards convergent evolution of BBB function in different groups of eusocial insects?
- Does toxicological alteration of BBB permeability affect complex behavioral patterns in invertebrates (e.g., courtship behavior in scorpions or the cephalopod Sepia officinalis)?
10. Conclusions and Future Directions
10.1. The Plurality of Blood-Brain Barriers
10.2. Areas for Future Research
10.2.1. Environment and the Evolution of the Blood-Brain Barrier
10.2.2. Plasticity of the Blood-Brain Barrier
10.2.3. The Blood-Brain Barrier and Behavior
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
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Group | Main Barrier Location | Endothelial Cells | Glial Cells | Pericytes | Basal Lamina | Other Notes | References |
---|---|---|---|---|---|---|---|
Teleosts | Endothelium | Present | Present, Radial glia | Present | Present | Jurisch-Yaksi et al., 2020; Jeong et al., 2008; Fleming et al., 2013; O’Brown et al., 2018 | |
Sturgeons | Glia | Present, overlapping with tight junctions, leaky due to caveolae and vesicles | Present, not joined by tight junctions, possibly gap junctions/interdigitating glial lamellae | None | Present | Endothelium not as leaky as in elasmobranchs | Bundgaard and Abbott, 2008 |
Lungfish | Endothelium | Present, joined by tight junctions | Present, discontinuous | Undetermined/“Perivascular cells” rather than glial cells | Reduced, not present on brain side | Discontinuous glia allow neurons to interact with pericytes, basal lamina, endothelium | Bundgaard and Abbott, 2008 |
Bichirs | Endothelium | Present, continuous tight junctions | Present, discontinuous | Undetermined | Reduced | Bundgaard and Abbott, 2008 | |
Lamprey and Hagfish | Endothelium | Present, joined by tight junctions, overlapping | Present, continuous sheath | None | Present | Endothelial cells have many abluminal vesicles and tubules | Bundgaard, 1982; Bundgaard et al., 1979 |
Chimaera | Endothelium | Present, described as “thick” | Present, discontinuous | None | Present, possibly covering glial processes as well | Bundgaard, 1982 | |
Elasmobranchs | Glia | Present, leaky, and not joined by tight junctions | Present, radial glia, continuous, joined by tight junctions | Present | Present | Bundgaard and Cserr, 1981; Balmaceda-Aguilera et al., 2012; O’Brown et al., 2018 |
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Dunton, A.D.; Göpel, T.; Ho, D.H.; Burggren, W. Form and Function of the Vertebrate and Invertebrate Blood-Brain Barriers. Int. J. Mol. Sci. 2021, 22, 12111. https://doi.org/10.3390/ijms222212111
Dunton AD, Göpel T, Ho DH, Burggren W. Form and Function of the Vertebrate and Invertebrate Blood-Brain Barriers. International Journal of Molecular Sciences. 2021; 22(22):12111. https://doi.org/10.3390/ijms222212111
Chicago/Turabian StyleDunton, Alicia D., Torben Göpel, Dao H. Ho, and Warren Burggren. 2021. "Form and Function of the Vertebrate and Invertebrate Blood-Brain Barriers" International Journal of Molecular Sciences 22, no. 22: 12111. https://doi.org/10.3390/ijms222212111