Abstract
We have studied a respiratory distress syndrome (RDS) occurring in newborn calves of the Belgian White and Blue (BWB) breed that represents the large majority of beef cattle in Belgium. Pulmonary surfactant isolated from 14 BWB newborn calves that died from RDS and from 7 healthy controls was analysed for composition and surface activity. An extremely low content or, in some instances, an absence of surfactant protein C (SP-C) was detected in the RDS samples by Western blotting and differential amino acid analysis [0.03+/-0.01% (w/w) relative to total phospholipids, compared with 0.39+/-0.06% for healthy controls (means+/-S.E.M., P < 0.001)]. The contents of surfactant protein B (SP-B) were similar in RDS and control samples. The crude surfactant samples isolated from RDS calves had higher ratios of total protein to total phospholipid, altered phospholipid profiles and lower SP-A contents. Both crude and organic extracts of RDS surfactant samples showed increased dynamic surface tension compared with healthy controls when evaluated with a pulsating-bubble surfactometer. The addition of purified SP-C to organic extracts of RDS surfactant samples lowered surface tension. Strongly decreased levels of mature SP-C associated with fatal RDS and altered surface activity in vitro have, to the best of our knowledge, not been previously reported. The mechanisms underlying RDS and the decrease in SP-C in BWB calves remain to be established.
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- AVERY M. E., MEAD J. Surface properties in relation to atelectasis and hyaline membrane disease. AMA J Dis Child. 1959 May;97(5 Pt 1):517–523. doi: 10.1001/archpedi.1959.02070010519001. [DOI] [PubMed] [Google Scholar]
- Ashbaugh D. G., Bigelow D. B., Petty T. L., Levine B. E. Acute respiratory distress in adults. Lancet. 1967 Aug 12;2(7511):319–323. doi: 10.1016/s0140-6736(67)90168-7. [DOI] [PubMed] [Google Scholar]
- BLIGH E. G., DYER W. J. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959 Aug;37(8):911–917. doi: 10.1139/o59-099. [DOI] [PubMed] [Google Scholar]
- Beers M. F., Atochina E. N., Preston A. M., Beck J. M. Inhibition of lung surfactant protein B expression during Pneumocystis carinii pneumonia in mice. J Lab Clin Med. 1999 May;133(5):423–433. doi: 10.1016/s0022-2143(99)90019-7. [DOI] [PubMed] [Google Scholar]
- Beers M. F., Kim C. Y., Dodia C., Fisher A. B. Localization, synthesis, and processing of surfactant protein SP-C in rat lung analyzed by epitope-specific antipeptide antibodies. J Biol Chem. 1994 Aug 12;269(32):20318–20328. [PubMed] [Google Scholar]
- Clark J. C., Wert S. E., Bachurski C. J., Stahlman M. T., Stripp B. R., Weaver T. E., Whitsett J. A. Targeted disruption of the surfactant protein B gene disrupts surfactant homeostasis, causing respiratory failure in newborn mice. Proc Natl Acad Sci U S A. 1995 Aug 15;92(17):7794–7798. doi: 10.1073/pnas.92.17.7794. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cockshutt A. M., Weitz J., Possmayer F. Pulmonary surfactant-associated protein A enhances the surface activity of lipid extract surfactant and reverses inhibition by blood proteins in vitro. Biochemistry. 1990 Sep 11;29(36):8424–8429. doi: 10.1021/bi00488a032. [DOI] [PubMed] [Google Scholar]
- Crouch E. C. Structure, biologic properties, and expression of surfactant protein D (SP-D). Biochim Biophys Acta. 1998 Nov 19;1408(2-3):278–289. doi: 10.1016/s0925-4439(98)00073-8. [DOI] [PubMed] [Google Scholar]
- Doyle I. R., Davidson K. G., Barr H. A., Nicholas T. E., Payne K., Pfitzner J. Quantity and structure of surfactant proteins vary among patients with alveolar proteinosis. Am J Respir Crit Care Med. 1998 Feb;157(2):658–664. doi: 10.1164/ajrccm.157.2.9701090. [DOI] [PubMed] [Google Scholar]
- Enhorning G. Pulsating bubble technique for evaluating pulmonary surfactant. J Appl Physiol Respir Environ Exerc Physiol. 1977 Aug;43(2):198–203. doi: 10.1152/jappl.1977.43.2.198. [DOI] [PubMed] [Google Scholar]
- Fuchimukai T., Fujiwara T., Takahashi A., Enhorning G. Artificial pulmonary surfactant inhibited by proteins. J Appl Physiol (1985) 1987 Feb;62(2):429–437. doi: 10.1152/jappl.1987.62.2.429. [DOI] [PubMed] [Google Scholar]
- Goerke J. Pulmonary surfactant: functions and molecular composition. Biochim Biophys Acta. 1998 Nov 19;1408(2-3):79–89. doi: 10.1016/s0925-4439(98)00060-x. [DOI] [PubMed] [Google Scholar]
- Gregory T. J., Longmore W. J., Moxley M. A., Whitsett J. A., Reed C. R., Fowler A. A., 3rd, Hudson L. D., Maunder R. J., Crim C., Hyers T. M. Surfactant chemical composition and biophysical activity in acute respiratory distress syndrome. J Clin Invest. 1991 Dec;88(6):1976–1981. doi: 10.1172/JCI115523. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grossmann G., Suzuki Y., Robertson B., Kobayashi T., Berggren P., Li W. Z., Song G. W., Sun B. Pathophysiology of neonatal lung injury induced by monoclonal antibody to surfactant protein B. J Appl Physiol (1985) 1997 Jun;82(6):2003–2010. doi: 10.1152/jappl.1997.82.6.2003. [DOI] [PubMed] [Google Scholar]
- Gustafsson M., Thyberg J., Näslund J., Eliasson E., Johansson J. Amyloid fibril formation by pulmonary surfactant protein C. FEBS Lett. 1999 Dec 31;464(3):138–142. doi: 10.1016/s0014-5793(99)01692-0. [DOI] [PubMed] [Google Scholar]
- Hall S. B., Wang Z., Notter R. H. Separation of subfractions of the hydrophobic components of calf lung surfactant. J Lipid Res. 1994 Aug;35(8):1386–1394. [PubMed] [Google Scholar]
- Hallman M., Spragg R., Harrell J. H., Moser K. M., Gluck L. Evidence of lung surfactant abnormality in respiratory failure. Study of bronchoalveolar lavage phospholipids, surface activity, phospholipase activity, and plasma myoinositol. J Clin Invest. 1982 Sep;70(3):673–683. doi: 10.1172/JCI110662. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hawgood S., Benson B. J., Hamilton R. L., Jr Effects of a surfactant-associated protein and calcium ions on the structure and surface activity of lung surfactant lipids. Biochemistry. 1985 Jan 1;24(1):184–190. doi: 10.1021/bi00322a026. [DOI] [PubMed] [Google Scholar]
- Hawgood S., Benson B. J., Schilling J., Damm D., Clements J. A., White R. T. Nucleotide and amino acid sequences of pulmonary surfactant protein SP 18 and evidence for cooperation between SP 18 and SP 28-36 in surfactant lipid adsorption. Proc Natl Acad Sci U S A. 1987 Jan;84(1):66–70. doi: 10.1073/pnas.84.1.66. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Johansson J., Curstedt T. Molecular structures and interactions of pulmonary surfactant components. Eur J Biochem. 1997 Mar 15;244(3):675–693. doi: 10.1111/j.1432-1033.1997.00675.x. [DOI] [PubMed] [Google Scholar]
- LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
- Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
- Lekeux P., Amory H., Desmecht D., Gustin P., Linden A., Rollin F. Oxygen transport chain in double-muscled blue Belgian cattle. Br Vet J. 1994 Sep-Oct;150(5):463–471. doi: 10.1016/S0007-1935(05)80197-6. [DOI] [PubMed] [Google Scholar]
- Mason R. J., Nellenbogen J., Clements J. A. Isolation of disaturated phosphatidylcholine with osmium tetroxide. J Lipid Res. 1976 May;17(3):281–284. [PubMed] [Google Scholar]
- McCormack F. X. Structure, processing and properties of surfactant protein A. Biochim Biophys Acta. 1998 Nov 19;1408(2-3):109–131. doi: 10.1016/s0925-4439(98)00062-3. [DOI] [PubMed] [Google Scholar]
- Mrsny R. J., Volwerk J. J., Griffith O. H. A simplified procedure for lipid phosphorus analysis shows that digestion rates vary with phospholipid structure. Chem Phys Lipids. 1986 Jan;39(1-2):185–191. doi: 10.1016/0009-3084(86)90111-8. [DOI] [PubMed] [Google Scholar]
- Nogee L. M. Genetics of the hydrophobic surfactant proteins. Biochim Biophys Acta. 1998 Nov 19;1408(2-3):323–333. doi: 10.1016/s0925-4439(98)00078-7. [DOI] [PubMed] [Google Scholar]
- Nogee L. M. Surfactant protein-B deficiency. Chest. 1997 Jun;111(6 Suppl):129S–135S. doi: 10.1378/chest.111.6_supplement.129s-a. [DOI] [PubMed] [Google Scholar]
- Oosterlaken-Dijksterhuis M. A., van Eijk M., van Buel B. L., van Golde L. M., Haagsman H. P. Surfactant protein composition of lamellar bodies isolated from rat lung. Biochem J. 1991 Feb 15;274(Pt 1):115–119. doi: 10.1042/bj2740115. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pison U., Seeger W., Buchhorn R., Joka T., Brand M., Obertacke U., Neuhof H., Schmit-Neuerburg K. P. Surfactant abnormalities in patients with respiratory failure after multiple trauma. Am Rev Respir Dis. 1989 Oct;140(4):1033–1039. doi: 10.1164/ajrccm/140.4.1033. [DOI] [PubMed] [Google Scholar]
- Poorthuis B. J., Yazaki P. J., Hostetler K. Y. An improved two dimensional thin-layer chromatography system for the separation of phosphatidylglycerol and its derivatives. J Lipid Res. 1976 Jul;17(4):433–437. [PubMed] [Google Scholar]
- Putman E., Boere A. J., van Bree L., van Golde L. M., Haagsman H. P. Pulmonary surfactant subtype metabolism is altered after short-term ozone exposure. Toxicol Appl Pharmacol. 1995 Sep;134(1):132–138. doi: 10.1006/taap.1995.1176. [DOI] [PubMed] [Google Scholar]
- Schägger H., von Jagow G. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem. 1987 Nov 1;166(2):368–379. doi: 10.1016/0003-2697(87)90587-2. [DOI] [PubMed] [Google Scholar]
- Smith G. B., Taeusch H. W., Phelps D. S., Keough K. M. Mixtures of low molecular weight surfactant proteins and dipalmitoyl phosphatidylcholine duplicate effects of pulmonary surfactant in vitro and in vivo. Pediatr Res. 1988 May;23(5):484–490. doi: 10.1203/00006450-198805000-00010. [DOI] [PubMed] [Google Scholar]
- Stark M., Wang Y., Danielsson O., Jörnvall H., Johansson J. Determination of proteins, phosphatidylethanolamine, and phosphatidylserine in organic solvent extracts of tissue material by analysis of phenylthiocarbamyl derivatives. Anal Biochem. 1998 Dec 1;265(1):97–102. doi: 10.1006/abio.1998.2856. [DOI] [PubMed] [Google Scholar]
- Strayer D. S., Herting E., Sun B., Robertson B. Antibody to surfactant protein A increases sensitivity of pulmonary surfactant to inactivation by fibrinogen in vivo. Am J Respir Crit Care Med. 1996 Mar;153(3):1116–1122. doi: 10.1164/ajrccm.153.3.8630554. [DOI] [PubMed] [Google Scholar]
- Suzuki Y., Fujita Y., Kogishi K. Reconstitution of tubular myelin from synthetic lipids and proteins associated with pig pulmonary surfactant. Am Rev Respir Dis. 1989 Jul;140(1):75–81. doi: 10.1164/ajrccm/140.1.75. [DOI] [PubMed] [Google Scholar]
- Van Golde L. M., Batenburg J. J., Robertson B. The pulmonary surfactant system: biochemical aspects and functional significance. Physiol Rev. 1988 Apr;68(2):374–455. doi: 10.1152/physrev.1988.68.2.374. [DOI] [PubMed] [Google Scholar]
- Veldhuizen R. A., McCaig L. A., Akino T., Lewis J. F. Pulmonary surfactant subfractions in patients with the acute respiratory distress syndrome. Am J Respir Crit Care Med. 1995 Dec;152(6 Pt 1):1867–1871. doi: 10.1164/ajrccm.152.6.8520748. [DOI] [PubMed] [Google Scholar]
- Yu S., Harding P. G., Smith N., Possmayer F. Bovine pulmonary surfactant: chemical composition and physical properties. Lipids. 1983 Aug;18(8):522–529. doi: 10.1007/BF02535391. [DOI] [PubMed] [Google Scholar]