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Vol. 83, Issue 6, 1849-1856, December 1997
Department of Anesthesiology and Intensive Care Medicine, School of Medicine, Kanazawa University, Kanazawa 920; and Department of Molecular Pathology, Chest Disease Research Institute, Kyoto University, Kyoto 606, Japan
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Kobayashi, Tsutomu, Katsumi Tashiro, Ken Yamamoto, Shunichi
Nitta, Shigeo Ohmura, and Yasuhiro Suzuki. Effects of surfactant proteins SP-B and SP-C on dynamic and static mechanics of immature lungs. J. Appl. Physiol. 83(6):
1849-1856, 1997.
To investigate the effects of surfactant
proteins B (SP-B) and C (SP-C) on lung mechanics, we compared tidal and
static lung volumes of immature rabbits anesthetized with pentobarbital
sodium and given reconstituted test surfactants (RTS).
With a series of RTS having various SP-B concentrations (0-0.7%)
but a fixed SP-C concentration (1.4%), both the tidal volume with
25-cmH2O insufflation pressure and the static volume deflated to
5-cmH2O airway pressure increased, significantly correlating with the SP-B concentration: the former increased from 6.5 to 26.0 ml/kg (mean), and the latter increased from
6.4 to 31.8 ml/kg. With another series of RTS having a
fixed SP-B concentration (0.7%) but various SP-C concentrations
(0-1.4%), the tidal volume increased from 5.1 to 24.8 ml/kg,
significantly correlating with the SP-C concentration, whereas the
static volume increased from 3.4 to 32.0 ml/kg, the ceiling value, in
the presence of a minimal concentration of SP-C (0.18%). In
conclusion, certain doses of SP-B and SP-C were indispensable for
optimizing dynamic lung mechanics; the static mechanics, however,
required significantly less SP-C.
lung volume; newborn rabbit; surface adsorption; tidal volume; ventilation
INTRODUCTION THE CONTRACTILE FORCE of the alveoli is reduced by
surfactant adsorbed to form a surface film at the air-liquid interface. Static pressure-volume recordings of the lung, especially during deflation from the maximum inflation, reflect the contractile force and
have been used to estimate the activity of pulmonary surfactant (6, 8,
12, 16, 19, 20, 28). The effects of surfactants on lung mechanics,
however, may differ between dynamic and static conditions: the
properties of the surface film during ventilation are changed by the
surface adsorption speed of surfactant molecules (11), and airway
resistance is altered by surfactant activity that also reduces the
contractile force of the bronchioles (5). Changes in the composition or
properties of surfactants, therefore, may separately alter the tidal
and static volumes of the lung.
Surfactant contains several kinds of phospholipids and four protein
families [surfactant protein (SP)], classified into the water-soluble type (SP-A and SP-D) and the hydrophobic type (SP-B and
SP-C). It is generally believed that the phospholipids need the
collaboration of SPs, especially hydrophobic SPs, for the development
of surface activity (for review, see Ref. 9). The precise roles of SP-B
and SP-C, however, are not completely clear. In the present study, we
compared tidal volume seen on mechanical ventilation and the static
volume of the lung in immature newborn rabbits in which alveolar
surfaces had been replaced with several reconstituted test surfactants
having various SP-B and SP-C concentrations and evaluated the roles of
each SP in the dynamic and static mechanics of the lung. For these
purposes, we also examined physical surface properties of the test
surfactants by using a pulsating-bubble technique.
METHODS
We also prepared several reconstituted test surfactants (RTS) in two series, the SP-B series and the SP-C series. For the former series, SP-C was first added to IL, together with the organic solvent used in the column chromatography, with the SP-C concentration at 1.4% adjusted by weight relative to IL. Then, five RTS were made by adding SP-B to the mixture in various concentrations (0-0.7%): 0% (no SP-B), 0.09% (one-eighth of the maximum), 0.18% (one-fourth of the maximum), 0.35% (one-half of the maximum), and 0.7% (the maximum). For the SP-C series, SP-B was first mixed with IL at a concentration of 0.7%. Five RTS were then made by adding SP-C in various concentrations (0-1.4%): 0% (no SP-C), 0.18% (one-eighth of the maximum), 0.35% (one-fourth of the maximum), 0.7% (one-half of the maximum), and 1.4% (the maximum). RTS containing both SP-B and SP-C at their maximum concentrations were combined because they had identical compositions. All RTS and IL were suspended, after evaporation of the organic solvent, in normal saline by repeatedly drawing them into, and expelling them from, a syringe and then by incubation in an ultrasonic bath (Branson 3200, Yamato, Tokyo, Japan) at 45°C for 3 min (19). These suspensions showed pH values below 2.5 by using test paper (Advantec, Toyo Roshi, Tokyo, Japan). We corrected the pH to 5.5-6.5, similar to the values observed in our laboratory in the lung liquid of immature newborn rabbits, by adding 0.1 N sodium hydroxide solution. The final phospholipid concentration of the suspension was adjusted to 50 mg/ml for biological assessment and to 10 mg/ml for evaluation of physical surface properties. CNS and MNS were also suspended in normal saline in the same manner, but the pH (~5.8) was not corrected. These suspensions were frozen and stored at
20°C.
Measurement of tidal volume and survival rate (Fig.
2).
We performed three experiments in which a total of 154 immature newborn
rabbits (from 23 does) were used. The animals were delivered by
hysterotomy at a gestational age of 25 days 18-23 h and were
immediately tracheotomized under anesthesia with intraperitoneal pentobarbital sodium (0.5 mg). In experiment
1, we randomized 34 of them for CNS, MNS, IL, or plain
normal saline. In experiment 2, we
randomized 61 others for IL, MNS, or one of the five RTS of the SP-B
series; and in experiment 3, we
randomized another 59 for IL, MNS, or one of the five RTS of the SP-C
series. They were given, via the tracheal cannula, 100 µl of fluid
containing the corresponding test material before taking their first
breath and were transferred to a system of multiple-body
plethysmographs (13) kept at 37°C. They were then relaxed with
intraperitoneal pancuronium bromide (0.02 mg) and subjected in parallel
to pressure-controlled ventilation. The respirator unit (Servo 900B,
Siemens-Elema, Solna, Sweden) delivered 100% oxygen at a frequency of
40 breaths/min with a 50% inspiration time.
The insufflation pressure was first raised to 35 cmH2O for 1 min to enhance distribution of the administered materials and then was lowered to 25 cmH2O for 15 min and to 20 and 15 cmH2O for 5 min each. Finally, the pressure was again raised to 25 cmH2O for 5 min. No end-expiratory pressure was applied to the common tube of the ventilatory circuit. We continuously monitored the pressure of the circuit with a conventional transducer (model TP-400T, Nihon Kohden, Tokyo, Japan) and confirmed that the above predetermined ventilatory conditions were precisely maintained. Individual tidal volumes were recorded at the end of each 5-min interval by means of a pneumotachograph that consisted of a specially designed flow-resistant tube, a differential pressure transducer (model TP-602T, Nihon Kohden), and an integrator unit (model AR-601G, Nihon Kohden). A volume change of 0.02 ml could be detected by this system. Electrocardiograms were recorded immediately after the period of ventilation, and animals showing QRS complexes at a frequency of over 100 beats/min were considered survivors. Static pressure-volume recordings of the lung-thorax system (Fig. 3). After electrocardiography, another 0.5 mg of pentobarbital sodium was given intraperitoneally for additional anesthesia, and absorption atelectasis was induced by plugging the endotracheal cannula. The abdomen of each animal was opened after death to inspect the diaphragm for evidence of pneumothorax. Thereafter, the plug of the cannula was removed, and animals were left for 1 h at 37°C so as to intensify the atelectasis. Next, animals were connected in parallel to an apparatus for the static pressure-volume recordings of the lung-thorax system (6) with the temperature maintained at 37°C. The airway pressure was raised stepwise from 0 to 30 cmH2O with 1 min of stress relaxation at each 5-cmH2O level and then was lowered in a similar fashion to 0 cmH2O. The volume measurements were corrected for air compression.
Measurement of physical surface property. Suspensions of the test materials were placed in the sample chamber (capacity = 25 µl) of a pulsating-bubble apparatus (Electronetics, Amherst, NY) and were heated to 37°C. A bubble (radius = 0.40 mm) in connection with the ambient air was created in the suspension within 0.2 s while the pressure across the air-liquid interface was continuously monitored for 10 s. The surface tension (
)
of these suspensions was calculated from the pressure and the radius according to the law of Laplace (pressure = 2/radius). We measured the surface adsorption time,
which is the interval between the start of the bubble formation and the
moment when had decreased to 30 mN/m. Then, the bubble was caused
to fluctuate in radius between 0.40 and 0.55 mm at a speed of 40 cycles/min. After 5 min of pulsation, the value of at minimum
bubble size (min) was
recorded.
Statistical analysis.
Values of tidal volume and static lung volume are shown as means ± SD, and the differences were assessed by analysis of variance followed
by Scheffé's method. Linear regression was calculated by the
method of least squares. Differences in survival rate were assessed by
Fisher's exact test. Data of physical surface properties are presented
as median and range, and the differences were examined by the
Kruskal-Wallis test. In all assessments, levels of
P < 0.05 were considered
significant.
RESULTS
|
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), isolated lipids (IL; 
), and plain normal
saline (
). Values are means ± SD;
n = 7-8 animals per each test
material. * P < 0.05 vs.
MNS.
Static pressure-volume recordings of the lung-thorax system during the course of deflation are presented in Fig. 5. In animals given CNS and MNS, mean lung volumes were >63 ml/kg at 30-cmH2O airway pressure, and volumes of >54% (>34 ml/kg) were maintained when the pressure was decreased to 5 cmH2O. No significant difference in lung volume was seen at any airway pressure between animals given CNS and MNS. In animals receiving IL and plain normal saline, the lung volumes were no more than 6 ml/kg at any airway pressure, significantly smaller throughout deflation than in those given CNS and MNS.
), IL
(), and plain normal saline (). Values are means ± SD;
n = 7-8 animals per each test
material. * P < 0.05 vs.
MNS.
Experiment 2: Biological assay for RTS of SP-B series. Six of the sixty-one animals enrolled were excluded because of pneumothorax. From the 55 animals studied, groups of 7-9 were given IL, MNS, or one of the RTS of the SP-B series. The body weight of the animals was 23.5 ± 4.7 g, without significant differences among the test material groups. All animals except those receiving IL survived through the period of ventilation. The survival rate of animals receiving IL was 29% (2 of 7) (P < 0.05 vs. MNS). Tidal volumes seen in experiment 2 are shown in Fig. 6. The volumes measured four times with an insufflation pressure of 25 cmH2O are presented as averages. The findings in animals receiving IL (negative controls) and MNS (positive controls) were almost the same as those seen in experiment 1. At an insufflation pressure of 25 cmH2O, the tidal volume of animals receiving the RTS containing no SP-B (SP-C = 1.4%) was <7 ml/kg (P < 0.05 vs. MNS). The RTS having higher SP-B concentrations caused greater tidal volumes (significant correlation, see Table 2), and animals given the RTS containing the maximum SP-B concentration (SP-B = 0.7%, SP-C = 1.4%) showed the tidal volume similar to that of animals receiving MNS. With insufflation pressures of 20 and 15 cmH2O, however, the tidal volumes of animals given any RTS did not reach the levels of those receiving MNS (P < 0.05 vs. MNS).
),
MNS (), and reconstituted test surfactants of SP-B series (
).
Values are means ± SD; n = 7-9 animals per each test material at 25-, 20-, and
15-cmH2O insufflation pressures.
*P < 0.05 vs. MNS.
|
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), MNS (), and reconstituted test
surfactants of SP-B series (). Values are means ± SD;
n = 7-9 animals per each test
material. *P < 0.05 vs. MNS.
Experiment 3: Biological assay for RTS of SP-C series. Five of the 59 animals enrolled were excluded because of pneumothorax. From the 54 animals studied, groups of 7-9 were given IL, MNS, or one of the RTS of the SP-C series. Their body weight was 24.5 ± 4.1 g, without significant intergroup differences. All animals except those receiving IL survived the period of ventilation. The survival rate of animals receiving IL was 38% (3 of 8; P < 0.05 vs. MNS). Tidal volumes observed in experiment 3 are shown in Fig. 8. The volumes, at an insufflation pressure of 25 cmH2O, are presented as averages of four measurements each. The tidal volumes of animals receiving IL and MNS were similar to those seen in experiments 1 and 2. At an insufflation pressure of 25 cmH2O, the mean tidal volume of animals receiving RTS containing no SP-C (SP-B = 0.7%) was 5.1 ml/kg, which showed no significant difference from that of animals receiving IL. The RTS having higher SP-C concentrations brought about greater tidal volumes (significant correlation, see Table 2), and animals given the RTS of the maximum showed a tidal volume similar to that of animals receiving MNS. With insufflation pressures of 20 and 15 cmH2O, however, the volumes did not reach the levels seen in animals receiving MNS, as in experiment 2 (P < 0.05 vs. MNS).
),
MNS (), and reconstituted test surfactants of SP-C series (
).
Values are means ± SD; n = 7-9 animals per each test material at 25-, 20-, and
15-cmH2O insufflation pressures.
*P < 0.05 vs. MNS.
Figure 9 shows the static lung volumes recorded in experiment 3 at airway pressures of 30 and 5 cmH2O during deflation. These volumes in animals given RTS containing no SP-C were significantly smaller than those in animals that received MNS, but the volumes in animals that were given RTS with the minimum SP-C concentration (0.18%) were similar to those in the newborn rabbits treated with MNS. No greater volumes were found in animals given RTS that had a greater SP-C concentration than the minimum (no correlation, see Table 2).
), MNS (), and reconstituted test
surfactants of SP-C series (). Values are means ± SD;
n = 7-9 animals per each test
material. *P < 0.05 vs. MNS.
Physical surface properties. Table 3 shows the physical surface properties of test materials used in the present study. CNS and MNS exhibited a
min of <3.0 mN/m and a surface adsorption time of <0.18 s (no significant difference between CNS and MNS). In contrast, IL showed a
min of >23 mN/m
(P < 0.05 vs. MNS). The value of
IL did not reach the equilibrium and did not decrease below 30 mN/m
within 10 s after the formation of an air bubble (surface adsorption
time >10 s).
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min were almost the same as
min of MNS until the
concentration of the corresponding proteins decreased to one-fourth of
the maximum. However, even the RTS with the maximum concentrations of
SP-B and SP-C had a significantly longer surface adsorption time than MNS. The RTS with no SP-B and with no SP-C showed nearly the same min values, but the former
exhibited a significantly longer surface adsorption time than did the
latter.
DISCUSSION
Immature newborn rabbits delivered before day 26 of gestation (term = 31 days) are almost devoid of pulmonary surfactant, and the tidal volumes under mechanical ventilation, therefore, provide accurate information on the activity of surfactants administered into the lungs (11, 14). A surfactant preparation with SP-A is reported to improve the dynamic lung compliance of immature rabbits better than such a preparation without it (16, 28). In experiment 1, however, MNS containing no water-soluble SPs (SP-A and SP-D) exhibited almost the same tidal volumes and static pressure-volume recordings as did CNS, which contained all SPs. In addition, administration of IL, which lacked all the proteins, did not result in any meaningful tidal and static lung volumes. No major errors, therefore, are likely if MNS and IL are used as the reference materials for analyzing the mechanics of the lung influenced by hydrophobic SPs (SP-B and SP-C).
In most surfactant preparations, including CNS and MNS, SP-B and SP-C
together represent 1-2% of surfactant components, and the ratio
of the former to the latter is 1 to ~2 by weight (for review, see
Ref. 9). Several reports have shown that phospholipids mixed with SP-C alone or with its analogs alone can reduce the of
the air-liquid interface and can improve dynamic compliance of the lung
at least to some extent (1, 4, 8, 16, 19, 20). We found in
experiment 2, however, that the tidal
volume at an insufflation pressure of 25 cmH2O increased with the SP-B concentration in the presence of SP-C and showed a significant correlation with it. We can conclude, therefore, that SP-B is an
indispensable element in the optimization of dynamic mechanics of the
lung. This conclusion is consistent with the results of several animal
experiments that showed deterioration of the dynamic mechanics of the
lung on administration of antibody to SP-B (12, 22) and may also
coincide with a clinical report that found progressive respiratory
failure in premature infants with an inherent deficiency of SP-B (15).
SP-B has alternating 
-helical and 
-sheet domains and a periodic
distribution of polar and nonpolar residues in the former (26). It is
speculated from these molecular structures that SP-B is an
amphiphilic-surface-seeking substance (23). The precise ways in which
SP-B modulates the mechanics of the lung are unknown, but several
investigators have speculated that SP-B plays a role in accelerating
the surface adsorption of phospholipid molecules (12, 17, 30). To
maintain the alveolar air spaces and the normal dynamic mechanics of
the lung, phospholipid molecules that leave the air-liquid interface
during surface compression (expiration) must be rapidly replenished
from the hypophase by adsorption during surface expansion
(inspiration). Among the RTS of the present study, that with no SP-B
showed the longest surface adsorption time. This suggests that the
roles of SP-B in the improvement of tidal volume are related, at least
in part, to the acceleration of surface adsorption.
Static pressure-volume recordings are thought to be little influenced by surface adsorption rate, because the phospholipid molecules are allowed enough time for the adsorption process at each pressure step. In experiment 2, the tidal and static volumes of the lung improved within the same concentration range of SP-B. We, therefore, find it difficult to explain the improvement of tidal volume on the basis of surface adsorption alone. On the basis of the structure of SP-B or its analogs, some scientists have proposed the hypothesis that SP-B has the function of stabilizing the phospholipid monolayer during surface compression (2, 17, 24, 29). The results of experiment 2 do not contradict the monolayer stabilization hypothesis.
In experiment 3, we gave the animals a series of RTS that had a fixed SP-B concentration (0.7%). Several studies have shown that phospholipids mixed with SP-B or its analogs can improve the dynamic compliance of the lung without the aid of SP-C (2, 3, 16, 19, 21, 29). We found, however, that the tidal volumes of the present animals at an insufflation pressure of 25 cmH2O increased, showing a positive correlation with SP-C concentration. We think, therefore, that SP-C is also an indispensable element in optimizing the dynamic mechanics of the lung, at least within the concentration range existing in natural surfactant.
SP-C has an -helical domain that is extraordinarily hydrophobic, and
this -helical portion may be inserted into lipid bilayers of
surfactant (10). The data of the present study are insufficient for
analyzing the structural and functional implications of SP-C. We found,
however, that even RTS containing SP-C at the minimum concentration
(0.18%) promoted static lung volumes similar to those with MNS, and
the volume did not show any dependency on SP-C above this
concentration. These findings are clearly disparate from those of tidal
volume and may support the assertion that findings obtained in static
measurements do not always show the overall activity of a surfactant
(11). Several investigators have addressed the possible roles of SP-C
in monolayer function (4, 18). In addition, some researchers are
speculating that SP-C accelerates the adsorption of the phospholipid
bilayer to an interfacial monolayer (1, 17, 27, 29). We can deduce from
these considerations that SP-C may play roles in both dynamic and
static mechanics of the lung. In the latter, however, the required dose of SP-C is significantly less than that in the former.
From the findings obtained by the pulsating-bubble technique, we can
deduce, at least within the concentration range of the present study,
that both SP-B and SP-C are indispensable for reducing the
min to below 3 mN/m, the same
level as with MNS. It is believed that materials showing a low
min may also reduce the
alveolar contractile force to a similar extent at the end of
expiration, because this technique compresses and expands the surface
of the sample liquid at a rate similar to the respiratory frequency. The low min, therefore, may be
a necessary factor for normalizing the functional residual capacity and
dynamic mechanics of the lung. In the present study, however, RTS with
min of <3 mN/m did not always
normalize the tidal volume, and so the
min value may be of limited use
for estimating the biological ability of surfactant.
We isolated SP-B and SP-C from MNS by dissolution in a
chloroform-methanol mixture containing hydrochloric acid. Without the addition of an alkaline solution, therefore, all RTS suspended in
normal saline showed a pH of below 2.5 and did not yield a min of <16 mN/m (data not
shown). Although some RTS exhibited a
min of <3 mN/m when the pH
was corrected to 5.5-6.5, the degeneration of some elements due to
the acidity could not be denied. In fact, RTS containing both SP-B and
SP-C at nearly twice the concentration in natural surfactant did not
show a short surface adsorption time similar to that of MNS and did not
normalize the tidal volumes when the insufflation pressure was below 20 cmH2O. As the cause of this
shortcoming, factors other than the degeneration may need examination.
These would include factors such as loss of important elements and
incomplete reconstitution of the lipids and proteins. In addition, it
is necessary to ascertain whether the tidal volume with insufflation
pressures of <20 cmH2O would
increase to the same extent as with MNS, if SP-B and SP-C
concentrations were raised.
Too little is still known to allow analysis of the functional and structural implication of SPs. We deduce, however, that SP-B and SP-C are indispensable elements in the optimization of respiratory function, because they affected the dynamic and static mechanics of the lung. In addition, we conclude that the dose of SP-C required for static mechanics is significantly less than that for dynamic mechanics.
ACKNOWLEDGEMENTS
We thank Drs. Yuko Waseda and Wen-Zhi Li for skillful technical contributions. We are also grateful to C. W. P. Reynolds for correcting the English of the manuscript.
FOOTNOTES
Address for reprint requests: T. Kobayashi, Dept. of Anesthesiology and Intensive Care Medicine, School of Medicine, Kanazawa Univ., 13 Takara-machi, Kanazawa 920, Japan.
Received 10 March 1997; accepted in final form 28 July 1997.
REFERENCES
| 1. | Clercx, A., G. Vandenbussche, T. Curstedt, J. Johansson, H. Jönvall, and J. M. Ruysschaert. Structural and functional importance of the C-terminal part of the pulmonary surfactant polypeptide SP-C. Eur. J. Biochem. 229: 465-472, 1995[Medline]. |
| 2. |
Cochrane, C. G.,
and
S. D. Revak.
Pulmonary surfactant protein B (SP-B): structure-function relationships.
Science
254:
566-568,
1991 |
| 3. | Cochrane, C. G., S. D. Revak, T. A. Merritt, G. P. Heldt, M. Hallman, M. D. Cunningham, D. Easa, A. Pramanik, D. K. Edwards, and M. S. Alberts. The efficacy and safety of KL4-surfactant in preterm infants with respiratory distress syndrome. Am. J. Respir. Crit. Care Med. 153: 404-410, 1996[Abstract]. |
| 4. |
Creuwels, L. A. J. M.,
R. A. Demel,
L. M. G. van Golde,
B. J. Benson,
and
H. P. Haagsman.
Effect of acylation on structure and function of surfactant protein C at the air-liquid interface.
J. Biol. Chem.
268:
26752-26758,
1993 |
| 5. | Enhorning, G., L. C. Duffy, and R. C. Welliver. Pulmonary surfactant maintains patency of conducting airways in the rat. Am. J. Respir. Crit. Care Med. 151: 554-556, 1995[Abstract]. |
| 6. |
Enhöning, G.,
and
B. Robertson.
Lung expansion in the premature rabbit fetus after tracheal deposition of surfactant.
Pediatrics
50:
58-66,
1972 |
| 7. | Frosolono, M. F., B. L. Charms, R. Pawlowski, and S. Slivka. Isolation, characterization, and surface chemistry of a surface-active fraction from dog lung. J. Lipid Res. 11: 439-457, 1970[Abstract]. |
| 8. | Hawgood, S., A. Ogawa, K. Yukitake, M. Schlueter, C. Brown, T. White, D. Buckley, D. Lesikar, and B. Benson. Lung function in premature rabbits treated with recombinant human surfactant protein-C. Am. J. Respir. Crit. Care Med. 154: 484-490, 1996[Abstract]. |
| 9. | Johansson, J., T. Curstedt, and B. Robertson. The proteins of the surfactant system. Eur. Respir. J. 7: 372-391, 1994[Abstract]. |
| 10. |
Johansson, J.,
T. Szyperski,
T. Curstedt,
and
K. Wüthrick.
The NMR structure of the pulmonary surfactant-associated polypeptide SP-C in an apolar solvent contains a valyl-rich -helix.
Biochemistry
33:
6015-6023,
1994[Medline].
|
| 11. |
Kobayashi, T.,
W.-Z. Li,
K. Tashiro,
R. Takahashi,
Y. Waseda,
K. Yamamoto,
and
Y. Suzuki.
Disparity between tidal and static volumes of immature lungs treated with reconstituted surfactants.
J. Appl. Physiol.
80:
62-68,
1996 |
| 12. |
Kobayashi, T.,
K. Nitta,
R. Takahashi,
K. Kurashima,
B. Robertson,
and
Y. Suzuki.
Activity of pulmonary surfactant after blocking the associated proteins SP-A and SP-B.
J. Appl. Physiol.
71:
530-536,
1991 |
| 13. | Lachmann, B., G. Grossmann, J. Freyse, and B. Robertson. Lung-thorax compliance in the artificially ventilated premature rabbit neonate in relation to variations in inspiration: expiration ratio. Pediatr. Res. 15: 833-838, 1981[Medline]. |
| 14. | Nitta, K., and T. Kobayashi. Impairment of surfactant activity and ventilation by proteins in lung edema fluid. Respir. Physiol. 95: 43-51, 1994[Medline]. |
| 15. |
Nogee, L. M.,
D. E. deMello,
L. P. Dehner,
and
H. R. Colten.
Brief report: deficiency of pulmonary surfactant protein B in congenital alveolar proteinosis.
N. Engl. J. Med.
328:
406-410,
1993 |
| 16. |
Ogawa, A.,
C. L. Brown,
M. A. Schlueter,
B. J. Benson,
J. A. Clements,
and
S. Hawgood.
Lung function, surfactant apoprotein content, and level of PEEP in prematurely delivered rabbits.
J. Appl. Physiol.
77:
1840-1849,
1994 |
| 17. | Oosterlaken-Dijksterhuis, M. A., H. P. Haagsman, L. M. G. van Golde, and R. A. Demel. Interaction of lipid vesicles with monomolecular layers containing lung surfactant proteins SP-B or SP-C. Biochemistry 30: 8276-8281, 1991[Medline]. |
| 18. | Post, A., A. V. Nahmen, M. Schmitt, J. Ruths, H. Riegler, M. Sieber, and H.-J. Galla. Pulmonary surfactant protein C containing lipid films at the air-water interface as a model for the surface of lung alveoli. Mol. Membr. Biol. 12: 93-99, 1995[Medline]. |
| 19. | Revak, S. D., T. A. Merritt, M. Hallman, G. Heldt, R. J. La Polla, K. Hoey, R. A. Houghten, and C. G. Cochrane. The use of synthetic peptides in the formation of biophysically and biologically active pulmonary surfactants. Pediatr. Res. 29: 460-465, 1991[Medline]. |
| 20. | Rider, E. D., M. Ikegami, J. A. Whitsett, W. Hull, D. Absolom, and A. H. Jobe. Treatment responses to surfactants containing natural surfactant proteins in preterm rabbits. Am. Rev. Respir. Dis. 147: 669-676, 1993[Medline]. |
| 21. |
Sarin, V. K.,
S. Gupta,
T. K. Leung,
V. E. Taylor,
B. L. Ohning,
J. A. Whitsett,
and
J. L. Fox.
Biophysical and biological activity of a synthetic 8.7-kDa hydrophobic pulmonary surfactant protein SP-B.
Proc. Natl. Acad. Sci. USA
87:
2633-2637,
1990 |
| 22. | Suzuki, Y., B. Robertson, Y. Fujita, and G. Grossmann. Respiratory failure in mice caused by a hybridoma making antibodies to the 15 kDa surfactant apoprotein. Acta Anaesthesiol. Scand. 32: 283-289, 1988[Medline]. |
| 23. | Takahashi, A., A. J. Waring, J. Amirkhanian, B. Fan, and H. W. Taeusch. Structure-function relationship of bovine pulmonary surfactant proteins: SP-B and SP-C. Biochim. Biophys. Acta 1044: 43-49, 1990[Medline]. |
| 24. | Taneva, S. G., and K. M. W. Keough. Dynamic surface properties of pulmonary surfactant proteins SP-B and SP-C and their mixtures with dipalmitoylphosphatidylcholine. Biochemistry 33: 14660-14670, 1994[Medline]. |
| 25. | Thompson, J. F., and G. R. Morrison. Determination of organic nitrogen: control of variables in the use of Nessler's reagent. Anal. Chem. 23: 1153-1157, 1951. |
| 26. | Vandenbussche, G., A. Clercx, M. Clercx, T. Curstedt, J. Johansson, H. Jörnvall, and J.-M. Ruysschaert. Secondary structure and orientation of the surfactant protein SP-B in a lipid environment. A Fourier transform infrared spectroscopy study. Biochemistry 31: 9169-9176, 1992[Medline]. |
| 27. |
Wang, Z.,
O. Gurel,
J. E. Baatz,
and
R. H. Notter.
Acylation of pulmonary surfactant protein-C is required for its optimal surface active interactions with phospholipids.
J. Biol. Chem.
271:
19104-19109,
1996 |
| 28. | Yamada, T., M. Ikegami, B. L. Tabor, and A. H. Jobe. Effects of surfactant protein-A on surfactant function in preterm ventilated rabbits. Am. Rev. Respir. Dis. 142: 754-757, 1990[Medline]. |
| 29. | Yu, S.-H., and F. Possmayer. Role of bovine pulmonary surfactant-associated proteins in the surface-active property of phospholipid mixtures. Biochim. Biophys. Acta 1046: 233-241, 1990[Medline]. |
| 30. | Yu, S.-H., and F. Possmayer. Adsorption, compression and stability of surface films from natural, lipid extract and reconstituted pulmonary surfactants. Biochim. Biophys. Acta 1167: 264-271, 1993[Medline]. |
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