Lymphatic function is required prenatally for lung inflation at birth

Journal of Experimental Medicine

Volumn 211, Issue 5, 2014, Pages 815-826

  Jakus, Zoltán ^a   Gleghorn, Jason P ^b   Enis, David R ^a   Sen, Aslihan ^a   Chia, Stephanie ^a   Liu, Xi ^a,c   Rawnsley, David R ^a   Yang, Yiqing ^a   Hess, Paul R ^a   Zou, Zhiying ^a   Yang, Jisheng ^a   Guttentag, Susan H ^d   Nelson, Celeste M ^b   Kahn, Mark L ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b Princeton University   (United States)

^c FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^d CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CCBE 1 PROTEIN; LUNG SURFACTANT; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREATHING; CAUSE OF DEATH; CONTROLLED STUDY; CYANOSIS; EMBRYO; FEMALE; LUNG COMPLIANCE; LUNG DEVELOPMENT; LUNG EDEMA; LUNG INFLATION; LUNG MECHANICS; LYMPH VESSEL; LYMPHANGIECTASIS; MOUSE; NEWBORN; NONHUMAN; PLEURA EFFUSION; PREGNANCY; PREMATURITY; PRIORITY JOURNAL; RESPIRATORY FAILURE;

ANIMALS; ANIMALS, NEWBORN; CALCIUM-BINDING PROTEINS; DNA PRIMERS; ECHOCARDIOGRAPHY; EMBRYO, MAMMALIAN; FETUS; IMMUNOHISTOCHEMISTRY; LUNG; LUNG COMPLIANCE; LYMPHATIC SYSTEM; LYMPHOGRAPHY; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON, TRANSMISSION; PULMONARY EDEMA; REAL-TIME POLYMERASE CHAIN REACTION; TUMOR SUPPRESSOR PROTEINS; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-3;

EID: 84899732109     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20132308     Document Type: Article

References (39)

1. Adams, F.H., T. Fujiwara, G. Emmanouilides, and A. Scudder. 1965. Surface properties and lipids from lungs of infants with hyaline membrane disease. J. Pediatr. 66:357-364. http://dx.doi.org/10.1016/S0022-3476(65)80193-7
2. Alders, M., B.M. Hogan, E. Gjini, F. Salehi, L. Al-Gazali, E.A. Hennekam, E.E. Holmberg, M.M. Mannens, M.F. Mulder, G.J. Offerhaus, et al. 2009. Mutations in CCBE1 cause generalized lymph vessel dysplasia in humans. Nat. Genet. 41:1272-1274. http://dx.doi.org/10.1038/ng.484
3. Atochina-Vasserman, E.N., S.R. Bates, P. Zhang, H. Abramova, Z. Zhang, L. Gonzales, J.Q. Tao, B.R. Gochuico, W. Gahl, C.J. Guo, et al. 2011. Early alveolar epithelial dysfunction promotes lung inflammation in a mouse model of Hermansky-Pudlak syndrome. Am. J. Respir. Crit. Care Med. 184:449-458. http://dx.doi.org/10.1164/rccm.201011-1882OC
4. Avery, M.E., and J. Mead. 1959. Surface properties in relation to atelectasis and hyaline membrane disease. AMA J. Dis. Child. 97:517-523.
5. Bellini, C., M. Mazzella, C. Arioni, C. Campisi, G. Taddei, P. Tomà, F. Boccardo, R.C. Hennekam, and G. Serra. 2003. Hennekam syndrome presenting as nonimmune hydrops fetalis, congenital chylothorax, and congenital pulmonary lymphangiectasia. Am. J. Med. Genet. A. 120A:92-96. http://dx.doi.org/10.1002/ajmg.a.20180
6. Bland, R.D., T.N. Hansen, C.M. Haberkern, M.A. Bressack, T.A. Hazinski, J.U. Raj, and R.B. Goldberg. 1982. Lung fluid balance in lambs before and after birth. J. Appl. Physiol. 53:992-1004.
7. Bourbon, J.R., M. Rieutort, M.J. Engle, and P.M. Farrell. 1982. Utilization of glycogen for phospholipid synthesis in fetal rat lung. Biochim. Biophys. Acta. 712:382-389. http://dx.doi.org/10.1016/0005-2760(82)90356-3
8. Clark, J.C., T.E. Weaver, H.S. Iwamoto, M. Ikegami, A.H. Jobe, W.M. Hull, and J.A. Whitsett. 1997. Decreased lung compliance and air trapping in heterozygous SP-B-deficient mice. Am. J. Respir. Cell Mol. Biol. 16:46-52. http://dx.doi.org/10.1165/ajrcmb.16.1.8998078
9. Compernolle, V., K. Brusselmans, T. Acker, P. Hoet, M. Tjwa, H. Beck, S. Plaisance, Y. Dor, E. Keshet, F. Lupu, et al. 2002. Loss of HIF-2alpha and inhibition of VEGF impair fetal lung maturation, whereas treatment with VEGF prevents fatal respiratory distress in premature mice. Nat. Med. 8:702-710. http://dx.doi.org/10.1038/nm1102-1329b
10. Couser, R.J., T.B. Ferrara, J. Ebert, R.E. Hoekstra, and J.J. Fangman. 1990. Effects of exogenous surfactant therapy on dynamic compliance during mechanical breathing in preterm infants with hyaline membrane disease. J. Pediatr. 116:119-124. http://dx.doi.org/10.1016/S0022-3476(05)81660-9
11. Guyton, A.C., and J.E. Hall. 2000. Textbook of Medical Physiology. W.B. Saunders Company: Philadelphia. 1120 pp.
12. Haddy, T.B., and F.J. Haddy. 1964. The Effect of acute pulmonary edema upon lung compliance. Pediatrics. 33:55-62.
13. Hintz, S.R., W.K. Poole, L.L. Wright, A.A. Fanaroff, D.E. Kendrick, A.R. Laptook, R. Goldberg, S. Duara, B.J. Stoll, and W. Oh. NICHD Neonatal Research Network. 2005. Changes in mortality and morbidities among infants born at less than 25 weeks during the post-surfactant era. Arch. Dis. Child. Fetal Neonatal Ed. 90:F128-F133. http://dx.doi.org/10.1136/adc.2003.046268
14. Hummler, E., P. Barker, J. Gatzy, F. Beermann, C. Verdumo, A. Schmidt, R. Boucher, and B.C. Rossier. 1996. Early death due to defective neonatal lung liquid clearance in αENaC-deficient mice. Nat. Genet. 12: 325-328. http://dx.doi.org/10.1038/ng0396-325
15. Janér, J., P. Lassus, C. Haglund, K. Paavonen, K. Alitalo, and S. Andersson. 2006. Pulmonary vascular endothelial growth factor-C in development and lung injury in preterm infants. Am. J. Respir. Crit. Care Med. 174:326-330. http://dx.doi.org/10.1164/rccm.200508-1291OC
16. Kaipainen, A., J. Korhonen, T. Mustonen, V.W. van Hinsbergh, G.H. Fang, D. Dumont, M. Breitman, and K. Alitalo. 1995. Expression of the fmslike tyrosine kinase 4 gene becomes restricted to lymphatic endothelium during development. Proc. Natl. Acad. Sci. USA. 92:3566-3570. http://dx.doi.org/10.1073/pnas.92.8.3566
17. Karkkainen, M.J., A. Saaristo, L. Jussila, K.A. Karila, E.C. Lawrence, K. Pajusola, H. Bueler, A. Eichmann, R. Kauppinen, M.I. Kettunen, et al. 2001. A model for gene therapy of human hereditary lymphedema. Proc. Natl. Acad. Sci. USA. 98:12677-12682. http://dx.doi.org/10.1073/pnas.221449198
18. Karkkainen, M.J., P. Haiko, K. Sainio, J. Partanen, J. Taipale, T.V. Petrova, M. Jeltsch, D.G. Jackson, M. Talikka, H. Rauvala, et al. 2004. Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat. Immunol. 5:74-80. http://dx.doi.org/10.1038/ni1013
19. Kobayashi, K., R.P. Lemke, and J.J. Greer. 2001. Ultrasound measurements of fetal breathing movements in the rat. J. Appl. Physiol. 91:316-320.
20. Kulkarni, R.M., A. Herman, M. Ikegami, J.M. Greenberg, and A.L. Akeson. 2011. Lymphatic ontogeny and effect of hypoplasia in developing lung. Mech. Dev. 128:29-40. http://dx.doi.org/10.1016/j.mod.2010.09.003
21. Laurence, K.M. 1955. Congenital pulmonary cystic lymphangiectasis. J. Pathol. Bacteriol. 70:325-331. http://dx.doi.org/10.1002/path.1700700208
22. Lee, J.S., Q. Yu, J.T. Shin, E. Sebzda, C. Bertozzi, M. Chen, P. Mericko, M. Stadtfeld, D. Zhou, L. Cheng, et al. 2006. Klf2 is an essential regulator of vascular hemodynamic forces in vivo. Dev. Cell. 11:845-857. http://dx.doi.org/10.1016/j.devcel.2006.09.006
23. Mäkinen, T., T. Veikkola, S. Mustjoki, T. Karpanen, B. Catimel, E.C. Nice, L. Wise, A. Mercer, H. Kowalski, D. Kerjaschki, et al. 2001. Isolated lymphatic endothelial cells transduce growth, survival and migratory signals via the VEGF-C/D receptor VEGFR-3. EMBO J. 20:4762-4773. http://dx.doi.org/10.1093/emboj/20.17.4762
24. Martel, C., W. Li, B. Fulp, A.M. Platt, E.L. Gautier, M. Westerterp, R. Bittman, A.R. Tall, S.H. Chen, M.J. Thomas, et al. 2013. Lymphatic vasculature mediates macrophage reverse cholesterol transport in mice. J. Clin. Invest. 123:1571-1579. http://dx.doi.org/10.1172/JCI63685
25. Milner, A.D., and R.A. Sauders. 1977. Pressure and volume changes during the first breath of human neonates. Arch. Dis. Child. 52:918-924. http://dx.doi.org/10.1136/adc.52.12.918
26. Moessinger, A.C., R. Harding, T.M. Adamson, M. Singh, and G.T. Kiu. 1990. Role of lung fluid volume in growth and maturation of the fetal sheep lung. J. Clin. Invest. 86:1270-1277. http://dx.doi.org/10.1172/JCI114834
27. Morgan, T.E. 1971. Pulmonary surfactant. N. Engl. J. Med. 284:1185-1193. http://dx.doi.org/10.1056/NEJM197105272842105
28. Morikawa, S., P. Baluk, T. Kaidoh, A. Haskell, R.K. Jain, and D.M. McDonald. 2002. Abnormalities in pericytes on blood vessels and endothelial sprouts in tumors. Am. J. Pathol. 160:985-1000. http://dx.doi.org/10.1016/S0002-9440(10)64920-6
29. Nogee, L.M., G. Garnier, H.C. Dietz, L. Singer, A.M. Murphy, D.E. deMello, and H.R. Colten. 1994. A mutation in the surfactant protein B gene responsible for fatal neonatal respiratory disease in multiple kindreds. J. Clin. Invest. 93:1860-1863. http://dx.doi.org/10.1172/JCI117173
30. Noonan, J.A., L.R. Walters, and J.T. Reeves. 1970. Congenital pulmonary lymphangiectasis. Am. J. Dis. Child. 120:314-319.
31. Patrick, J., and J. Challis. 1980. Measurement of human fetal breathing movements in healthy pregnancies using a real-time scanner. Semin. Perinatol. 4:275-286.
32. Schnitzer, J., W.W. Franke, and M. Schachner. 1981. Immunocytochemical demonstration of vimentin in astrocytes and ependymal cells of developing and adult mouse nervous system. J. Cell Biol. 90:435-447. http://dx.doi.org/10.1083/jcb.90.2.435
33. Sharp, J.T., G.T. Griffith, I.L. Bunnell, and D.G. Greene. 1958. Ventilatory mechanics in pulmonary edema in man. J. Clin. Invest. 37:111-117. http://dx.doi.org/10.1172/JCI103577
34. Suresh, G.K., and R.F. Soll. 2005. Overview of surfactant replacement trials. J. Perinatol. 25:S40-S44. http://dx.doi.org/10.1038/sj.jp.7211320
35. Tammela, T., and K. Alitalo. 2010. Lymphangiogenesis: Molecular mechanisms and future promise. Cell. 140:460-476. http://dx.doi.org/10.1016/j.cell.2010.01.045
36. Wang, Y., and G. Oliver. 2010. Current views on the function of the lymphatic vasculature in health and disease. Genes Dev. 24:2115-2126. http://dx.doi.org/10.1101/gad.1955910
37. Wigle, J.T., and G. Oliver. 1999. Prox1 function is required for the development of the murine lymphatic system. Cell. 98:769-778. http://dx.doi.org/10.1016/S0092-8674(00)81511-1
38. Zhang, L., F. Zhou, W. Han, B. Shen, J. Luo, M. Shibuya, and Y. He. 2010. VEGFR-3 ligand-binding and kinase activity are required for lymphangiogenesis but not for angiogenesis. Cell Res. 20:1319-1331. http://dx.doi.org/10.1038/cr.2010.116
39. Zou, Z., D.R. Enis, H. Bui, E. Khandros, V. Kumar, Z. Jakus, C. Thom, Y. Yang, V. Dhillon, M. Chen, et al. 2013. The secreted lymphangiogenic factor CCBE1 is essential for fetal liver erythropoiesis. Blood. 121:3228-3236. http://dx.doi.org/10.1182/blood-2012-10-462689