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Morphogenetic Implications of Peristalsis-Driven Fluid Flow in the Embryonic Lung.

Bokka KK, Jesudason EC, Lozoya OA, Guilak F, Warburton D, Lubkin SR - PLoS ONE (2015)

Bottom Line: The sensation of internal fluid flows has been shown to have potent morphogenetic effects, as has the transport of morphogens.We hypothesize that these effects play an important role in lung morphogenesis.We analyzed the interaction between the internal flows and diffusion and conclude that AP has a strong effect on flow sensing away from the tip and on transport of morphogens.

View Article: PubMed Central - PubMed

Affiliation: Department of Mechanical Engineering, North Carolina State University, Raleigh, North Carolina, United States of America.

ABSTRACT
Epithelial organs are almost universally secretory. The lung secretes mucus of extremely variable consistency. In the early prenatal period, the secretions are of largely unknown composition, consistency, and flow rates. In addition to net outflow from secretion, the embryonic lung exhibits transient reversing flows from peristalsis. Airway peristalsis (AP) begins as soon as the smooth muscle forms, and persists until birth. Since the prenatal lung is liquid-filled, smooth muscle action can transport fluid far from the immediately adjacent tissues. The sensation of internal fluid flows has been shown to have potent morphogenetic effects, as has the transport of morphogens. We hypothesize that these effects play an important role in lung morphogenesis. To test these hypotheses in a quantitative framework, we analyzed the fluid-structure interactions between embryonic tissues and lumen fluid resulting from peristaltic waves that partially occlude the airway. We found that if the airway is closed, fluid transport is minimal; by contrast, if the trachea is open, shear rates can be very high, particularly at the stenosis. We performed a parametric analysis of flow characteristics' dependence on tissue stiffnesses, smooth muscle force, geometry, and fluid viscosity, and found that most of these relationships are governed by simple ratios. We measured the viscosity of prenatal lung fluid with passive bead microrheology. This paper reports the first measurements of the viscosity of embryonic lung lumen fluid. In the range tested, lumen fluid can be considered Newtonian, with a viscosity of 0.016 ± 0.008 Pa-s. We analyzed the interaction between the internal flows and diffusion and conclude that AP has a strong effect on flow sensing away from the tip and on transport of morphogens. These effects may be the intermediate mechanisms for the enhancement of branching seen in occluded embryonic lungs.

No MeSH data available.


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Viscometry of lumen fluid from prenatal mouse lungs.Ratio of lung fluid viscosity to viscosity of water is 1.1 ± 0.3. Variability between individuals (N = 3) is greater than variability between beads (n = 11–29), locations in lung (m = 3–4), or frequency (0.5–2 Hz).
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pone.0132015.g005: Viscometry of lumen fluid from prenatal mouse lungs.Ratio of lung fluid viscosity to viscosity of water is 1.1 ± 0.3. Variability between individuals (N = 3) is greater than variability between beads (n = 11–29), locations in lung (m = 3–4), or frequency (0.5–2 Hz).

Mentions: Using particle-tracking microrheometry [11] with injected 500 nm beads, we determined the properties of the lumen fluid in 3 prenatal mice from different litters. The slopes of the log-log plots of MSD against time interval (in the range 0.2–30 s-1) did not measurably differ from 1 (R2 > 0.95). Thus, in the prenatal mouse lungs measured, the lumen fluid was Newtonian up to 30 s-1. We found that the viscosity of the lung fluid is an order of magnitude higher than that of water (log10(μ/μw) = 1.1±0.3). Specifically, water has a viscosity of 0.001 Pa-s and we measured embryonic mouse lung lumen viscosity at 0.016 ± 0.008 Pa-s. Variability between individuals was significantly greater than variability within an individual or between frequencies (Fig 5).


Morphogenetic Implications of Peristalsis-Driven Fluid Flow in the Embryonic Lung.

Bokka KK, Jesudason EC, Lozoya OA, Guilak F, Warburton D, Lubkin SR - PLoS ONE (2015)

Viscometry of lumen fluid from prenatal mouse lungs.Ratio of lung fluid viscosity to viscosity of water is 1.1 ± 0.3. Variability between individuals (N = 3) is greater than variability between beads (n = 11–29), locations in lung (m = 3–4), or frequency (0.5–2 Hz).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4493131&req=5

pone.0132015.g005: Viscometry of lumen fluid from prenatal mouse lungs.Ratio of lung fluid viscosity to viscosity of water is 1.1 ± 0.3. Variability between individuals (N = 3) is greater than variability between beads (n = 11–29), locations in lung (m = 3–4), or frequency (0.5–2 Hz).
Mentions: Using particle-tracking microrheometry [11] with injected 500 nm beads, we determined the properties of the lumen fluid in 3 prenatal mice from different litters. The slopes of the log-log plots of MSD against time interval (in the range 0.2–30 s-1) did not measurably differ from 1 (R2 > 0.95). Thus, in the prenatal mouse lungs measured, the lumen fluid was Newtonian up to 30 s-1. We found that the viscosity of the lung fluid is an order of magnitude higher than that of water (log10(μ/μw) = 1.1±0.3). Specifically, water has a viscosity of 0.001 Pa-s and we measured embryonic mouse lung lumen viscosity at 0.016 ± 0.008 Pa-s. Variability between individuals was significantly greater than variability within an individual or between frequencies (Fig 5).

Bottom Line: The sensation of internal fluid flows has been shown to have potent morphogenetic effects, as has the transport of morphogens.We hypothesize that these effects play an important role in lung morphogenesis.We analyzed the interaction between the internal flows and diffusion and conclude that AP has a strong effect on flow sensing away from the tip and on transport of morphogens.

View Article: PubMed Central - PubMed

Affiliation: Department of Mechanical Engineering, North Carolina State University, Raleigh, North Carolina, United States of America.

ABSTRACT
Epithelial organs are almost universally secretory. The lung secretes mucus of extremely variable consistency. In the early prenatal period, the secretions are of largely unknown composition, consistency, and flow rates. In addition to net outflow from secretion, the embryonic lung exhibits transient reversing flows from peristalsis. Airway peristalsis (AP) begins as soon as the smooth muscle forms, and persists until birth. Since the prenatal lung is liquid-filled, smooth muscle action can transport fluid far from the immediately adjacent tissues. The sensation of internal fluid flows has been shown to have potent morphogenetic effects, as has the transport of morphogens. We hypothesize that these effects play an important role in lung morphogenesis. To test these hypotheses in a quantitative framework, we analyzed the fluid-structure interactions between embryonic tissues and lumen fluid resulting from peristaltic waves that partially occlude the airway. We found that if the airway is closed, fluid transport is minimal; by contrast, if the trachea is open, shear rates can be very high, particularly at the stenosis. We performed a parametric analysis of flow characteristics' dependence on tissue stiffnesses, smooth muscle force, geometry, and fluid viscosity, and found that most of these relationships are governed by simple ratios. We measured the viscosity of prenatal lung fluid with passive bead microrheology. This paper reports the first measurements of the viscosity of embryonic lung lumen fluid. In the range tested, lumen fluid can be considered Newtonian, with a viscosity of 0.016 ± 0.008 Pa-s. We analyzed the interaction between the internal flows and diffusion and conclude that AP has a strong effect on flow sensing away from the tip and on transport of morphogens. These effects may be the intermediate mechanisms for the enhancement of branching seen in occluded embryonic lungs.

No MeSH data available.


Related in: MedlinePlus