Antenatal inflammation reduces expression of caveolin-1 and influences multiple signaling pathways in preterm fetal lungs

American Journal of Respiratory Cell and Molecular Biology

Volumn 45, Issue 5, 2011, Pages 969-976

  Kunzmann, Steffen ^a   Collins, Jennifer J P ^b   Yang, Yang ^c   Uhlig, Stefan ^c   Kallapur, Suhar G ^d,e   Speer, Christian P ^a   Jobe, Alan H ^d,e   Kramer, Boris W ^b  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c RWTH AACHEN UNIVERSITY   (Germany)

^d CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^e UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

a SMase; Bronchopulmonary dysplasia; Ceramide; Chorioamnionitis; TGF

Indexed keywords

CAVEOLIN 1; CERAMIDE; ENDOTOXIN; HEME OXYGENASE 1; LIPOPOLYSACCHARIDE; SMAD1 PROTEIN; SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD5 PROTEIN; SODIUM CHLORIDE; SPHINGOMYELIN PHOSPHODIESTERASE; STAT1 PROTEIN; STAT3 PROTEIN;

ANIMAL TISSUE; ARTICLE; CHORIOAMNIONITIS; CONTROLLED STUDY; FETUS; IMMUNOHISTOCHEMISTRY; NONHUMAN; PNEUMONIA; PREMATURITY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SHEEP; SIGNAL TRANSDUCTION;

ANIMALS; ANIMALS, NEWBORN; CAVEOLIN 1; CERAMIDES; CHORIOAMNIONITIS; ENDOTOXINS; FEMALE; FETUS; HEME OXYGENASE-1; LUNG; PHOSPHORYLATION; PNEUMONIA; PREGNANCY; PREMATURE BIRTH; SHEEP; SIGNAL TRANSDUCTION; SPHINGOMYELIN PHOSPHODIESTERASE; TRANSCRIPTION FACTORS;

OVIS ARIES;

EID: 80555156705     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2010-0519OC     Document Type: Article

References (56)

1. Thomas W, Speer CP. Chorioamnionitis: important risk factor or innocent bystander for neonatal outcome? Neonatology 2010;99:177-187.
2. Kramer BW, Kallapur S, Newnham J, Jobe AH. Prenatal inflammation and lung development. Semin Fetal Neonatal Med 2009;14:2-7.
3. Lahra MM, Jeffery HE. A fetal response to chorioamnionitis is associated with early survival after preterm birth. Am J Obstet Gynecol 2004;190:147-151. (Pubitemid 38156339)
4. Yoon BH, Jun JK, Romero R, Park KH, Gomez R, Choi JH, Kim IO. Amniotic fluid inflammatory cytokines (interleukin-6, interleukin-1beta, and tumor necrosis factor - alpha), neonatal brain white matter lesions, and cerebral palsy. Am J Obstet Gynecol 1997;177:19-26. (Pubitemid 27327305)
5. Gantert M, Been JV, Gavilanes AW, Garnier Y, Zimmermann LJ, Kramer BW. Chorioamnionitis: a multiorgan disease of the fetus? J Perinatol 2010;30:S21-S30.
6. Jobe AJ. The new BPD: an arrest of lung development. Pediatr Res 1999;46:641-643.
7. Razani B, Engelman JA, Wang XB, Schubert W, Zhang XL, Marks CB, Macaluso F, Russell RG, Li M, Pestell RG, et al. Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities. J Biol Chem 2001;276:38121-38138.
8. Jin Y, Lee SJ, Minshall RD, Choi AM. Caveolin-1: a critical regulator of lung injury. Am J Physiol Lung Cell Mol Physiol 2011;300:L151-L160.
9. Williams TM, Lisanti MP. The caveolin genes: from cell biology to medicine. Ann Med 2004;36:584-595. (Pubitemid 40051435)
10. Gosens R, Mutawe M, Martin S, Basu S, Bos ST, Tran T, Halayko AJ. Caveolae and caveolins in the respiratory system. Curr Mol Med 2008;8:741-753.
11. Razani B, Zhang XL, Bitzer M, von Gersdorff G, Bottinger EP, Lisanti MP. Caveolin-1 regulates transforming growth factor (TGF)eta/SMAD signaling through an interaction with the TGF-beta Type I receptor. J Biol Chem 2001;276:6727-6738.
12. Santibanez JF, Blanco FJ, Garrido-Martin EM, Sanz-Rodriguez F, del Pozo MA, Bernabeu C. Caveolin-1 interacts and cooperates with the transforming growth factor - beta Type I receptor ALK1 in endothelial caveolae. Cardiovasc Res 2008;77:791-799. (Pubitemid 351301871)
13. Bennett D, Alphey L. PP1 binds Sara and negatively regulates Dpp signaling in Drosophila melanogaster. Nat Genet 2002;31:419-423. (Pubitemid 35154454)
14. Jasmin JF, Mercier I, Hnasko R, Cheung MW, Tanowitz HB, Dupuis J, Lisanti MP. Lung remodeling and pulmonary hypertension after myocardial infarction: pathogenic role of reduced caveolin expression. Cardiovasc Res 2004;63:747-755. (Pubitemid 39078689)
15. Sehgal PB, Guo GG, Shah M, Kumar V, Patel K. Cytokine signaling: STATS in plasma membrane rafts. J Biol Chem 2002;277:12067-12074. (Pubitemid 34952770)
16. Veldman RJ, Maestre N, Aduib OM, Medin JA, Salvayre R, Levade T. A neutral sphingomyelinase resides in sphingolipid-enriched microdomains and is inhibited by the caveolin-scaffolding domain: potential implications in tumour necrosis factor signalling. Biochem J 2001;355:859-868. (Pubitemid 32434106)
17. Yang Y, Yin J, Baumgartner W, Samapati R, Solymosi EA, Reppien E, Kuebler WM, Uhlig S. Platelet-activating factor reduces endothelial nitric oxide production: role of acid sphingomyelinase. Eur Respir J 2010;36:417-427.
18. Gao H, Ward PA. STAT3 and suppressor of cytokine signaling 3: potential targets in lung inflammatory responses. Expert Opin Ther Targets 2007;11:869-880. (Pubitemid 47061314)
19. Severgnini M, Takahashi S, Rozo LM, Homer RJ, Kuhn C, Jhung JW, Perides G, Steer M, Hassoun PM, Fanburg BL, et al. Activation of the STAT pathway in acute lung injury. Am J Physiol Lung Cell Mol Physiol 2004;286:L1282-L1292. (Pubitemid 38656666)
20. Severgnini M, Takahashi S, Tu P, Perides G, Homer RJ, Jhung JW, Bhavsar D, Cochran BH, Simon AR. Inhibition of the Src and Jak kinases protects against lipopolysaccharide-induced acute lung injury. Am J Respir Crit Care Med 2005;171:858-867. (Pubitemid 40562716)
21. Uhlig S, Gulbins E. Sphingolipids in the lungs. Am J Respir Crit Care Med 2008;178:1100-1114.
22. von Bismarck P, Wistadt CF, Klemm K, Winoto-Morbach S, Uhlig U, Schutze S, Adam D, Lachmann B, Uhlig S, Krause MF. Improved pulmonary function by acid sphingomyelinase inhibition in a newborn piglet lavage model. Am J Respir Crit Care Med 2008;177:1233-1241.
23. Jin Y, Kim HP, Chi M, Ifedigbo E, Ryter SW, Choi AM. Deletion of caveolin-1 protects against oxidative lung injury via up-regulation of heme oxygenase - 1. Am J Respir Cell Mol Biol 2008;39:171-179.
24. Fredenburgh LE, Perrella MA, Mitsialis SA. The role of heme oxygenase - 1 in pulmonary disease. Am J Respir Cell Mol Biol 2007;36:158-165. (Pubitemid 46233468)
25. Kunzmann S, Speer CP, Jobe AH, Kramer BW. Antenatal inflammation induced TGF-beta1 but suppressed CTGF in preterm lungs. Am J Physiol Lung Cell Mol Physiol 2007;292:L223-L231. (Pubitemid 46103447)
26. Ding H, Zhou FQ, Cai HR, Zhou YH, Meng FQ. Expression of caveolin-1 and extracellular matrix induced by transforming growth factor beta1 in human fetal lung fibroblasts [in Chinese]. Zhonghua Jie He He Hu Xi Za Zhi 2010;33:280-283.
27. Igarashi J, Shoji K, Hashimoto T, Moriue T, Yoneda K, Takamura T, Yamashita T, Kubota Y, Kosaka H. Transforming growth factor - beta1 downregulates caveolin-1 expression and enhances sphingosine 1-phosphate signaling in cultured vascular endothelial cells. Am J Physiol Cell Physiol 2009;297:C1263-C1274.
28. Wang XM, Zhang Y, Kim HP, Zhou Z, Feghali-Bostwick CA, Liu F, Ifedigbo E, Xu X, Oury TD, Kaminski N, et al. Caveolin-1: a critical regulator of lung fibrosis in idiopathic pulmonary fibrosis. J Exp Med 2006;203:2895-2906. (Pubitemid 46026167)
29. Kramer BW, Moss TJ, Willet KE, Newnham JP, Sly PD, Kallapur SG, Ikegami M, Jobe AH. Dose and time response after intraamniotic endotoxin in preterm lambs. Am J Respir Crit Care Med 2001;164:982-988. (Pubitemid 32971645)
30. Kramer BW, Kallapur SG, Moss TJ, Nitsos I, Newnham JP, Jobe AH. Intra-amniotic LPS modulation of TLR signaling in lung and blood monocytes of fetal sheep. Innate Immun 2009;15:101-107.
31. Kramer BW, Kramer S, Ikegami M, Jobe AH. Injury, inflammation, and remodeling in fetal sheep lung after intra-amniotic endotoxin. Am J Physiol Lung Cell Mol Physiol 2002;283:L452-L459. (Pubitemid 34804003)
32. Wiegmann K, Schutze S, Machleidt T, Witte D, Kronke M. Functional dichotomy of neutral and acidic sphingomyelinases in tumor necrosis factor signaling. Cell 1994;78:1005-1015. (Pubitemid 24292328)
33. Jensen JM, Schutze S, Forl M, Kronke M, Proksch E. Roles for tumor necrosis factor receptor p55 and sphingomyelinase in repairing the cutaneous permeability barrier. J Clin Invest 1999;104:1761-1770. (Pubitemid 30053193)
34. Benjamin JT, Carver BJ, Plosa EJ, Yamamoto Y, Miller JD, Liu JH, van der Meer R, Blackwell TS, Prince LS. NF-kappaB activation limits airway branching through inhibition of Sp1-mediated fibroblast growth factor - 10 expression. J Immunol 2010;185:4896-4903.
35. Benjamin JT, Gaston DC, Halloran BA, Schnapp LM, Zent R, Prince LS. The role of integrin alpha8beta1 in fetal lung morphogenesis and injury. Dev Biol 2009;335:407-417.
36. Kunzmann S, Glogger K, Been JV, Kallapur SG, Nitsos I, Moss TJ, Speer CP, Newnham JP, Jobe AH, Kramer BW. Thymic changes after chorioamnionitis induced by intraamniotic lipopolysaccharide in fetal sheep. Am J Obstet Gynecol 2010;202:e471-e479.
37. Moss TJ, Newnham JP, Willett KE, Kramer BW, Jobe AH, Ikegami M. Early gestational intra-amniotic endotoxin: lung function, surfactant, and morphometry. Am J Respir Crit Care Med 2002;165:805-811. (Pubitemid 34229651)
38. Wolfs TG, Buurman WA, Zoer B, Moonen RM, Derikx JP, Thuijls G, Villamor E, Gantert M, Garnier Y, Zimmermann LJ, et al. Endotoxin induced chorioamnionitis prevents intestinal development during gestation in fetal sheep. PLoS ONE 2009;4:e5837.
39. Jobe AH, Newnham JP, Willet KE, Moss TJ, Gore Ervin M, Padbury JF, Sly P, Ikegami M. Endotoxin-induced lung maturation in preterm lambs is not mediated by cortisol. Am J Respir Crit Care Med 2000;162:1656-1661.
40. Kallapur SG, Moss TJ, Auten RL Jr, Nitsos I, Pillow JJ, Kramer BW, Maeda DY, Newnham JP, Ikegami M, Jobe AH. IL-8 signaling does not mediate intra-amniotic LPS-induced inflammation and maturation in preterm fetal lamb lung. Am J Physiol Lung Cell Mol Physiol 2009;297:L512-L519.
41. Kallapur SG, Nitsos I,Moss TJ, Polglase GR, Pillow JJ, Cheah FC, Kramer BW, Newnham JP, Ikegami M, Jobe AH. IL-1 mediates pulmonary and systemic inflammatory responses to chorioamnionitis induced by lipopolysaccharide. Am J Respir Crit Care Med 2009;179:955-961.
42. DiGiulio DB, Romero R, Amogan HP, Kusanovic JP, Bik EM, Gotsch F, Kim CJ, Erez O, Edwin S, Relman DA. Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: a molecular and culture-based investigation. PLoS ONE 2008;3:e3056.
43. Kotecha S, Wangoo A, Silverman M, Shaw RJ. Increase in the concentration of transforming growth factor beta-1 in bronchoalveolar lavage fluid before development of chronic lung disease of prematurity. J Pediatr 1996;128:464-469. (Pubitemid 26114082)
44. Lecart C, Cayabyab R, Buckley S, Morrison J, Kwong KY, Warburton D, Ramanathan R, Jones CA, Minoo P. Bioactive transforming growth factor - beta in the lungs of extremely low birthweight neonates predicts the need for home oxygen supplementation. Biol Neonate 2000;77:217-223. (Pubitemid 30307309)
45. Del Galdo F, Lisanti MP, Jimenez SA. Caveolin-1, transforming growth factor - beta receptor internalization, and the pathogenesis of systemic sclerosis. Curr Opin Rheumatol 2008;20:713-719.
46. Di Guglielmo GM, Le Roy C, Goodfellow AF, Wrana JL. Distinct endocytic pathways regulate TGF-beta receptor signalling and turnover. Nat Cell Biol 2003;5:410-421. (Pubitemid 36592263)
47. Le Saux O, Teeters K, Miyasato S, Choi J, Nakamatsu G, Richardson JA, Starcher B, Davis EC, Tam EK, Jourdan-Le Saux C. The role of caveolin-1 in pulmonary matrix remodeling and mechanical properties. Am J Physiol Lung Cell Mol Physiol 2008;295:L1007-L1017.
48. Le Saux CJ, Teeters K, Miyasato SK, Hoffmann PR, Bollt O, Douet V, Shohet RV, Broide DH, Tam EK. Down-regulation of caveolin-1, an inhibitor of transforming growth factoreta signaling, in acute allergen-induced airway remodeling. J Biol Chem 2008;283:5760-5768.
49. Darnell JE Jr. STATs and gene regulation. Science 1997;277:1630-1635.
50. Park DS, Lee H, Frank PG, Razani B, Nguyen AV, Parlow AF, Russell RG, Hulit J, Pestell RG, Lisanti MP. Caveolin-1 - deficient mice show accelerated mammary gland development during pregnancy, premature lactation, and hyperactivation of the Jak-2/STAT5a signaling cascade. Mol Biol Cell 2002;13:3416-3430. (Pubitemid 35191364)
51. Marchesini N, Hannun YA. Acid and neutral sphingomyelinases: roles and mechanisms of regulation. Biochem Cell Biol 2004;82:27-44. (Pubitemid 38580872)
52. Kim HP, Wang X, Galbiati F, Ryter SW, Choi AM. Caveolae compartmentalization of heme oxygenase-1 in endothelial cells. FASEB J 2004;18:1080-1089. (Pubitemid 38859216)
53. Farkas I, Maroti Z, Katona M, Endreffy E, Monostori P, Mader K, Turi S. Increased heme oxygenase-1 expression in premature infants with respiratory distress syndrome. Eur J Pediatr 2008;167:1379-1383.
54. Maroti Z, Katona M, Orvos H, Nemeth I, Farkas I, Turi S. Heme oxygenase - 1 expression in premature and mature neonates during the first week of life. Eur J Pediatr 2007;166:1033-1038. (Pubitemid 47313067)
55. Razani B, Lisanti MP. Caveolin-deficient mice: insights into caveolar function human disease. J Clin Invest 2001;108:1553-1561. (Pubitemid 33144862)
56. Tourkina E, Richard M, Gooz P, Bonner M, Pannu J, Harley R, Bernatchez PN, Sessa WC, Silver RM, Hoffman S. Antifibrotic properties of caveolin-1 scaffolding domain in vitro and in vivo. Am J Physiol Lung Cell Mol Physiol 2008;294:L843-L861.