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. 1994 Sep;145(3):631–639.

An immunohistochemical study of the expression of surfactant apoprotein in the hypoplastic lung of rabbit fetuses induced by oligohydramnios.

K Asabe 1, N Toki 1, S Hashimoto 1, S Suita 1, K Sueishi 1
PMCID: PMC1890323  PMID: 8080045

Abstract

We shunted amniotic fluid from alternate gestational sacs into the maternal peritoneal cavity between 23 and 30 days gestation in fetal rabbits (full term, 31 days) to investigate the effect of oligohydramnios on surfactant apoprotein A (SP-A) expression by an immunohistochemical morphometric analysis. The amniotic shunt produced a significant decrease in the amniotic fluid volume (P < 0.02), as well as a reduction in the lung weight (P < 0.005) and lung/body weight ratio (P < 0.001), which indicated lung hypoplasia. These fetuses also showed a statistically significant reduction of SP-A expression, ie, SP-A-positive type II cells per unit area (P < 0.05), SP-A-positive type II cells/total cells ratio (P < 0.001), the percentage of SP-A-positive area per unit area (P < 0.005), and the SP-A-positive area/alveolar epithelium area plus the lung interstitium area ratio (P < 0.005). These results suggest that oligohydramnios significantly retards and modifies the structural growth and functional development of alveolar type II cells in SP-A expression. This animal model of hypoplastic lung in fetuses is thus considered to be useful in helping to further develop the treatment for hypoplastic lung.

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Selected References

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  1. Adzick N. S., Harrison M. R., Glick P. L., Villa R. L., Finkbeiner W. Experimental pulmonary hypoplasia and oligohydramnios: relative contributions of lung fluid and fetal breathing movements. J Pediatr Surg. 1984 Dec;19(6):658–665. doi: 10.1016/s0022-3468(84)80349-8. [DOI] [PubMed] [Google Scholar]
  2. Askenazi S. S., Perlman M. Pulmonary hypoplasia: lung weight and radial alveolar count as criteria of diagnosis. Arch Dis Child. 1979 Aug;54(8):614–618. doi: 10.1136/adc.54.8.614. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Castillo R. A., Devoe L. D., Hadi H. A., Martin S., Geist D. Nonimmune hydrops fetalis: clinical experience and factors related to a poor outcome. Am J Obstet Gynecol. 1986 Oct;155(4):812–816. doi: 10.1016/s0002-9378(86)80026-6. [DOI] [PubMed] [Google Scholar]
  4. Collins M. H., Moessinger A. C., Kleinerman J., James L. S., Blanc W. A. Morphometry of hypoplastic fetal guinea pig lungs following amniotic fluid leak. Pediatr Res. 1986 Oct;20(10):955–960. doi: 10.1203/00006450-198610000-00013. [DOI] [PubMed] [Google Scholar]
  5. Dairaku M., Sueishi K., Tanaka K., Horie A. Immunohistological analysis of surfactant-apoprotein in the bronchiolo-alveolar carcinoma. Virchows Arch A Pathol Anat Histopathol. 1983;400(3):223–234. doi: 10.1007/BF00612184. [DOI] [PubMed] [Google Scholar]
  6. Dempo K., Satoh M., Tsuji S., Mori M., Kuroki Y., Akino T. Immunohistochemical studies on the expression of pulmonary surfactant apoproteins in human lung carcinomas using monoclonal antibodies. Pathol Res Pract. 1987 Oct;182(5):669–675. [PubMed] [Google Scholar]
  7. Dobbs L. G., Wright J. R., Hawgood S., Gonzalez R., Venstrom K., Nellenbogen J. Pulmonary surfactant and its components inhibit secretion of phosphatidylcholine from cultured rat alveolar type II cells. Proc Natl Acad Sci U S A. 1987 Feb;84(4):1010–1014. doi: 10.1073/pnas.84.4.1010. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hallman M., Arjomaa P., Mizumoto M., Akino T. Surfactant proteins in the diagnosis of fetal lung maturity. I. Predictive accuracy of the 35 kD protein, the lecithin/sphingomyelin ratio, and phosphatidylglycerol. Am J Obstet Gynecol. 1988 Mar;158(3 Pt 1):531–535. doi: 10.1016/0002-9378(88)90019-1. [DOI] [PubMed] [Google Scholar]
  9. Harding R., Hooper S. B., Dickson K. A. A mechanism leading to reduced lung expansion and lung hypoplasia in fetal sheep during oligohydramnios. Am J Obstet Gynecol. 1990 Dec;163(6 Pt 1):1904–1913. doi: 10.1016/0002-9378(90)90772-y. [DOI] [PubMed] [Google Scholar]
  10. Hawgood S., Clements J. A. Pulmonary surfactant and its apoproteins. J Clin Invest. 1990 Jul;86(1):1–6. doi: 10.1172/JCI114670. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Higuchi M., Kato T., Yoshino H., Matsuda K., Gotoh K., Hirano H., Koyama K., Maki M. The influence of experimentally produced oligohydramnios on lung growth and pulmonary surfactant content in fetal rabbits. J Dev Physiol. 1991 Oct;16(4):223–227. [PubMed] [Google Scholar]
  12. Hislop A., Fairweather D. V. Amniocentesis and lung growth: an animal experiment with clinical implications. Lancet. 1982 Dec 4;2(8310):1271–1272. doi: 10.1016/s0140-6736(82)90120-9. [DOI] [PubMed] [Google Scholar]
  13. Hislop A., Fairweather D. V., Blackwell R. J., Howard S. The effect of amniocentesis and drainage of amniotic fluid on lung development in Macaca fascicularis. Br J Obstet Gynaecol. 1984 Sep;91(9):835–842. doi: 10.1111/j.1471-0528.1984.tb03693.x. [DOI] [PubMed] [Google Scholar]
  14. Hsu S. M., Raine L., Fanger H. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem. 1981 Apr;29(4):577–580. doi: 10.1177/29.4.6166661. [DOI] [PubMed] [Google Scholar]
  15. Kashiwabara Y., Onoyama Y., Shimokawa H., Hisanaga S., Nakano H. A new method for measurement of surfactant specific apoprotein in amniotic fluid. Int J Gynaecol Obstet. 1989 Jun;29(2):147–152. doi: 10.1016/0020-7292(89)90845-x. [DOI] [PubMed] [Google Scholar]
  16. Katyal S. L., Estes L. W., Lombardi B. Method for the isolation of surfactant from homogenates and lavages of lung of adult, newborn, and fetal rats. Lab Invest. 1977 Jun;36(6):585–592. [PubMed] [Google Scholar]
  17. King J. C., Mitzner W., Butterfield A. B., Queenan J. T. Effect of induced oligohydramnios on fetal lung development. Am J Obstet Gynecol. 1986 Apr;154(4):823–830. doi: 10.1016/0002-9378(86)90465-5. [DOI] [PubMed] [Google Scholar]
  18. King R. J., Klass D. J., Gikas E. G., Clements J. A. Isolation of apoproteins from canine surface active material. Am J Physiol. 1973 Apr;224(4):788–795. doi: 10.1152/ajplegacy.1973.224.4.788. [DOI] [PubMed] [Google Scholar]
  19. King R. J., Ruch J., Gikas E. G., Platzker A. C., Creasy R. K. Appearance of paoproteins of pulmonary surfactant in human amniotic fluid. J Appl Physiol. 1975 Nov;39(5):735–741. doi: 10.1152/jappl.1975.39.5.735. [DOI] [PubMed] [Google Scholar]
  20. King R. J., Simon D., Horowitz P. M. Aspects of secondary and quaternary structure of surfactant protein A from canine lung. Biochim Biophys Acta. 1989 Feb 20;1001(3):294–301. doi: 10.1016/0005-2760(89)90114-8. [DOI] [PubMed] [Google Scholar]
  21. Kuroki Y., Dempo K., Akino T. Immunohistochemical study of human pulmonary surfactant apoproteins with monoclonal antibodies. Pathologic application for hyaline membrane disease. Am J Pathol. 1986 Jul;124(1):25–33. [PMC free article] [PubMed] [Google Scholar]
  22. Kuroki Y., Mason R. J., Voelker D. R. Pulmonary surfactant apoprotein A structure and modulation of surfactant secretion by rat alveolar type II cells. J Biol Chem. 1988 Mar 5;263(7):3388–3394. [PubMed] [Google Scholar]
  23. Maeda H., Shimokawa H., Yamaguchi Y., Sueishi K., Nakano H. The influence of pleural effusion on pulmonary growth in the human fetus. J Perinat Med. 1989;17(3):231–236. doi: 10.1515/jpme.1989.17.3.231. [DOI] [PubMed] [Google Scholar]
  24. Moessinger A. C., Bassi G. A., Ballantyne G., Collins M. H., James L. S., Blanc W. A. Experimental production of pulmonary hypoplasia following amniocentesis and oligohydramnios. Early Hum Dev. 1983 Oct;8(3-4):343–350. doi: 10.1016/0378-3782(83)90017-8. [DOI] [PubMed] [Google Scholar]
  25. Moessinger A. C., Collins M. H., Blanc W. A., Rey H. R., James L. S. Oligohydramnios-induced lung hypoplasia: the influence of timing and duration in gestation. Pediatr Res. 1986 Oct;20(10):951–954. doi: 10.1203/00006450-198610000-00012. [DOI] [PubMed] [Google Scholar]
  26. Nagata N., Dairaku M., Ishida T., Sueishi K., Tanaka K. Sclerosing hemangioma of the lung. Immunohistochemical characterization of its origin as related to surfactant apoprotein. Cancer. 1985 Jan 1;55(1):116–123. doi: 10.1002/1097-0142(19850101)55:1<116::aid-cncr2820550119>3.0.co;2-4. [DOI] [PubMed] [Google Scholar]
  27. Nakamura Y., Funatsu Y., Yamamoto I., Yamana K., Nishimura T., Hosokawa Y., Fukuda S., Nakashima H., Tsunosue M., Hashimoto T. Potter's syndrome associated with renal agenesis or dysplasia. Morphological and biochemical study of the lung. Arch Pathol Lab Med. 1985 May;109(5):441–444. [PubMed] [Google Scholar]
  28. Nakamura Y., Yamamoto I., Funatsu Y., Motomura K., Fukuda S., Hashimoto T., Morimatsu M. Decreased surfactant level in the lung with oligohydramnios: a morphometric and biochemical study. J Pediatr. 1988 Mar;112(3):471–474. doi: 10.1016/s0022-3476(88)80340-8. [DOI] [PubMed] [Google Scholar]
  29. Nakayama D. K., Glick P. L., Harrison M. R., Villa R. L., Noall R. Experimental pulmonary hypoplasia due to oligohydramnios and its reversal by relieving thoracic compression. J Pediatr Surg. 1983 Aug;18(4):347–353. doi: 10.1016/s0022-3468(83)80179-1. [DOI] [PubMed] [Google Scholar]
  30. Nimrod C., Varela-Gittings F., Machin G., Campbell D., Wesenberg R. The effect of very prolonged membrane rupture on fetal development. Am J Obstet Gynecol. 1984 Mar 1;148(5):540–543. doi: 10.1016/0002-9378(84)90743-9. [DOI] [PubMed] [Google Scholar]
  31. Rice W. R., Ross G. F., Singleton F. M., Dingle S., Whitsett J. A. Surfactant-associated protein inhibits phospholipid secretion from type II cells. J Appl Physiol (1985) 1987 Aug;63(2):692–698. doi: 10.1152/jappl.1987.63.2.692. [DOI] [PubMed] [Google Scholar]
  32. Sueishi K., Tanaka K., Oda T. Immunoultrastructural study of surfactant system. Distribution of specific protein of surface active material in rabbit lung. Lab Invest. 1977 Aug;37(2):136–142. [PubMed] [Google Scholar]
  33. Suen H. C., Catlin E. A., Ryan D. P., Wain J. C., Donahoe P. K. Biochemical immaturity of lungs in congenital diaphragmatic hernia. J Pediatr Surg. 1993 Mar;28(3):471–477. doi: 10.1016/0022-3468(93)90250-o. [DOI] [PubMed] [Google Scholar]
  34. Thibeault D. W., Beatty E. C., Jr, Hall R. T., Bowen S. K., O'Neill D. H. Neonatal pulmonary hypoplasia with premature rupture of fetal membranes and oligohydramnios. J Pediatr. 1985 Aug;107(2):273–277. doi: 10.1016/s0022-3476(85)80148-7. [DOI] [PubMed] [Google Scholar]
  35. Walker S. R., Williams M. C., Benson B. Immunocytochemical localization of the major surfactant apoproteins in type II cells, Clara cells, and alveolar macrophages of rat lung. J Histochem Cytochem. 1986 Sep;34(9):1137–1148. doi: 10.1177/34.9.2426341. [DOI] [PubMed] [Google Scholar]
  36. Wigglesworth J. S., Hislop A. A., Desai R. Biochemical and morphometric analyses in hypoplastic lungs. Pediatr Pathol. 1991 Jul-Aug;11(4):537–549. doi: 10.3109/15513819109064789. [DOI] [PubMed] [Google Scholar]
  37. Yoneyama K. Immunohistochemical localization of pulmonary surfactants in fetal rabbit lung. Nihon Sanka Fujinka Gakkai Zasshi. 1988 Nov;40(11):1740–1746. [PubMed] [Google Scholar]

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