Thrown off balance: The effect of antenatal inflammation on the developing lung and immune system

American Journal of Obstetrics and Gynecology

Volumn 208, Issue 6, 2013, Pages 429-437

  Kunzmann, Steffen ^a   Collins, Jennifer J P ^b   Kuypers, Elke ^c   Kramer, Boris W ^c  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^c MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

BPD; chorioamnionitis; immune modulation; RDS; surfactant; TGF

Indexed keywords

INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; TUMOR NECROSIS FACTOR ALPHA;

ANTENATAL INFLAMMATION; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CHORIOAMNIONITIS; CYTOKINE PRODUCTION; FETUS LUNG MATURATION; HUMAN; IMMUNE SYSTEM; INFLAMMATION; LUNG DEVELOPMENT; LUNG DYSPLASIA; NONHUMAN; PREGNANCY OUTCOME; PREMATURITY; PRENATAL EXPOSURE; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CHORIOAMNIONITIS; FEMALE; HUMANS; IMMUNE SYSTEM; IMMUNE TOLERANCE; INFLAMMATION; LUNG; PERIPARTUM PERIOD; PREGNANCY;

EID: 84878390772     PISSN: 00029378     EISSN: 10976868     Source Type: Journal    
DOI: 10.1016/j.ajog.2013.01.008     Document Type: Review

References (141)

1. Internal classification of diseases and related health problems 1992 World Health Organization Geneva
2. R.L. Goldenberg, J.F. Culhane, J.D. Iams, R. Romero Epidemiology and causes of preterm birth Lancet 371 2008 75 84
3. R.L. Goldenberg, J.C. Hauth, W.W. Andrews Intrauterine infection and preterm delivery N Engl J Med 342 2000 1500 1507
4. R. Romero, J. Espinoza, J.P. Kusanovic The preterm parturition syndrome BJOG 113 Suppl 3 2006 17 42
5. R. Romero, J. Espinoza, L.F. Goncalves, J.P. Kusanovic, L. Friel, S. Hassan The role of inflammation and infection in preterm birth Semin Reprod Med 25 2007 21 39
6. R. Romero, C.J. Lockwood Chapter 28: pathogenesis of preterm labor R.K. Creasy, R. Resnik, Maternal-fetal medicine 2009
7. R.W. Redline Placental inflammation Sem Neonatol:SN 9 2004 265 274
8. V.G. Chellam, D.I. Rushton Chorioamnionitis and funiculitis in the placentas of 200 births weighing less than 2.5 kg Br J Obstet Gynaecol 92 1985 808 814
9. M. Gantert, J.V. Been, A.W. Gavilanes, Y. Garnier, L.J. Zimmermann, B.W. Kramer Chorioamnionitis: a multiorgan disease of the fetus? J Perinatol 30 Suppl 2010 S21 S30
10. R.L. Schelonka, K.B. Waites Ureaplasma infection and neonatal lung disease Semin Perinatol 31 2007 2 9
11. B.H. Yoon, J.W. Chang, R. Romero Isolation of Ureaplasma urealyticum from the amniotic cavity and adverse outcome in preterm labor Obstet Gynecol 92 1998 77 82
12. B.W. Kramer Chorioamnionitis - new ideas from experimental models Neonatology 99 2011 320 325
13. D.B. DiGiulio, R. Romero, H.P. Amogan Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: a molecular and culture-based investigation PLoS One 3 2008 e3056
14. S. Gerber, Y. Vial, P. Hohlfeld, S.S. Witkin Detection of Ureaplasma urealyticum in second-trimester amniotic fluid by polymerase chain reaction correlates with subsequent preterm labor and delivery J Infect Dis 187 2003 518 521
15. W.W. Andrews, R.L. Goldenberg, J.C. Hauth, S.P. Cliver, M. Conner, A.R. Goepfert Endometrial microbial colonization and plasma cell endometritis after spontaneous or indicated preterm versus term delivery Am J Obstet Gynecol 193 2005 739 745
16. S.C. Perni, S. Vardhana, I. Korneeva Mycoplasma hominis and Ureaplasma urealyticum in midtrimester amniotic fluid: association with amniotic fluid cytokine levels and pregnancy outcome Am J Obstet Gynecol 191 2004 1382 1386
17. J.H. Steel, S. Malatos, N. Kennea Bacteria and inflammatory cells in fetal membranes do not always cause preterm labor Pediatr Res 57 2005 404 411
18. H. Hagberg, U.B. Wennerholm, K. Savman Sequelae of chorioamnionitis Curr Opin Infect Dis 15 2002 301 306
19. M.J. Kim, R. Romero, M.T. Gervasi Widespread microbial invasion of the chorioamniotic membranes is a consequence and not a cause of intra-amniotic infection Lab Invest 89 2009 924 936
20. C.J. Kim, R. Romero, J.P. Kusanovic The frequency, clinical significance, and pathological features of chronic chorioamnionitis: a lesion associated with spontaneous preterm birth Mod Pathol 23 2010 1000 1011
21. R.W. Redline, O. Faye-Petersen, D. Heller, F. Qureshi, V. Savell, C. Vogler Amniotic infection syndrome: nosology and reproducibility of placental reaction patterns Pediatr Dev Pathol 6 2003 435 448
22. S.M. Jacques, F. Qureshi Chronic chorioamnionitis: a clinicopathologic and immunohistochemical study Hum Pathol 29 1998 1457 1461
23. G. Ogge, R. Romero, D.C. Lee Chronic chorioamnionitis displays distinct alterations of the amniotic fluid proteome J Pathol 223 2011 553 565
24. J. Lee, R. Romero, Z. Dong Unexplained fetal death has a biological signature of maternal anti-fetal rejection: chronic chorioamnionitis and alloimmune anti-human leucocyte antigen antibodies Histopathol 59 2011 928 938
25. J. Lee, R. Romero, Y. Xu Maternal HLA panel-reactive antibodies in early gestation positively correlate with chronic chorioamnionitis: evidence in support of the chronic nature of maternal anti-fetal rejection Am J Reprod Immunol 66 2011 510 526
26. F. Gotsch, R. Romero, J.P. Kusanovic The fetal inflammatory response syndrome Clin Obstet Gynecol 50 2007 652 683
27. R. Romero, R. Gomez, F. Ghezzi A fetal systemic inflammatory response is followed by the spontaneous onset of preterm parturition Am J Obstet Gynecol 179 1998 186 193
28. B.H. Yoon, R. Romero, J.S. Park The relationship among inflammatory lesions of the umbilical cord (funisitis), umbilical cord plasma interleukin 6 concentration, amniotic fluid infection, and neonatal sepsis Am J Obstet Gynecol 183 2000 1124 1129
29. T. Chaiworapongsa, R. Romero, J.C. Kim Evidence for fetal involvement in the pathologic process of clinical chorioamnionitis Am J Obstet Gynecol 186 2002 1178 1182
30. M. Seehase, M. Gantert, A. Ladenburger Myocardial response in preterm fetal sheep exposed to systemic endotoxinaemia Pediatr Res 70 2011 242 246
31. R. Romero, Z.A. Savasan, T. Chaiworapongsa Hematologic profile of the fetus with systemic inflammatory response syndrome J Perinat Med 40 2011 19 32
32. B.G. Sood, A. Madan, S. Saha Perinatal systemic inflammatory response syndrome and retinopathy of prematurity Pediatr Res 67 2010 394 400
33. A.L. Letti Muller, M. Barrios Pde, L.M. Kliemann, E.G. Valerio, R. Gasnier, J.A. Magalhaes Tei index to assess fetal cardiac performance in fetuses at risk for fetal inflammatory response syndrome Ultrasound Obstet Gynecol 36 2010 26 31
34. W. Thomas, C.P. Speer Chorioamnionitis: important risk factor or innocent bystander for neonatal outcome? Neonatol 99 2011 177 187
35. S.K. Ahlfeld, S.J. Conway Aberrant signaling pathways of the lung mesenchyme and their contributions to the pathogenesis of bronchopulmonary dysplasia Birth Defects Res 94 2012 3 15
36. I. Burd, B. Balakrishnan, S. Kannan Models of fetal brain injury, intrauterine inflammation, and preterm birth Am J Reprod Immunol 67 2012 287 294
37. S. Malaeb, O. Dammann Fetal inflammatory response and brain injury in the preterm newborn J Child Neurol 24 2009 1119 1126
38. L.S. Prince, V.O. Okoh, T.O. Moninger, S. Matalon Lipopolysaccharide increases alveolar type II cell number in fetal mouse lungs through Toll-like receptor 4 and NF-kappaB Am J Physiol Lung Cell Mol Physiol 287 2004 L999 L1006
39. T. Ikegami, A. Tsuda, A. Karube, H. Kodama, H. Hirano, T. Tanaka Effects of intrauterine IL-6 and IL-8 on the expression of surfactant apoprotein mRNAs in the fetal rat lung Eur J Obstet Gynecol Reprod Biol 93 2000 97 103
40. C. Gras-Le Guen, C. Denis, M.L. Franco-Montoya Antenatal infection in the rabbit impairs post-natal growth and lung alveolarisation ERJ 32 2008 1520 1528
41. C.F. Uyehara, B.E. Pichoff, H.H. Sim, H.S. Uemura, K.T. Nakamura Hyperoxic exposure enhances airway reactivity of newborn guinea pigs J Appl Physiol 74 1993 2649 2654
42. N.H. Hillman, S.G. Kallapur, J.J. Pillow Airway injury from initiating ventilation in preterm sheep Pediatr Res 67 2010 60 65
43. B.W. Kramer, S. Kramer, M. Ikegami, A.H. Jobe Injury, inflammation, and remodeling in fetal sheep lung after intra-amniotic endotoxin Am J Physiol Lung Cell Mol Physiol 283 2002 L452 L459
44. K.C. Pringle Human fetal lung development and related animal models Clin Obstet Gynecol 29 1986 502 513
45. J.S. Wigglesworth, R. Desai Use of DNA estimation for growth assessment in normal and hypoplastic fetal lungs Arch Dis Child 56 1981 601 605
46. O. Williams, G. Hutchings, C. Hubinont, C. Debauche, A. Greenough Pulmonary effects of prolonged oligohydramnios following mid-trimester rupture of the membranes - antenatal and postnatal management Neonatol 101 2012 83 90
47. K. Bry, A. Hogmalm, E. Backstrom Mechanisms of inflammatory lung injury in the neonate: lessons from a transgenic mouse model of bronchopulmonary dysplasia Sem Perinatol 34 2010 211 221
48. J.T. Benjamin, B.J. Carver, E.J. Plosa NF-kappaB activation limits airway branching through inhibition of Sp1-mediated fibroblast growth factor-10 expression J Immunol 185 2010 4896 4903
49. J.D. Miller, J.T. Benjamin, D.R. Kelly, D.B. Frank, L.S. Prince Chorioamnionitis stimulates angiogenesis in saccular stage fetal lungs via CC chemokines Am J Physiol Lung Cell Mol Physiol 298 2010 L637 L645
50. A.H. Jobe, M. Ikegami Antenatal infection/inflammation and postnatal lung maturation and injury Respir Res 2 2001 27 32
51. W.W. Andrews, R.L. Goldenberg, O. Faye-Petersen, S. Cliver, A.R. Goepfert, J.C. Hauth The Alabama Preterm Birth study: polymorphonuclear and mononuclear cell placental infiltrations, other markers of inflammation, and outcomes in 23- to 32-week preterm newborn infants Am J Obstet Gynecol 195 2006 803 808
52. K.L. Watterberg, L.M. Demers, S.M. Scott, S. Murphy Chorioamnionitis and early lung inflammation in infants in whom bronchopulmonary dysplasia develops Pediatrics 97 1996 210 215
53. C.P. Speer Neonatal respiratory distress syndrome: an inflammatory disease? Neonatology 99 2011 316 319
54. C.P. Speer Chorioamnionitis, postnatal factors and proinflammatory response in the pathogenetic sequence of bronchopulmonary dysplasia Neonatology 95 2009 353 361
55. A.H. Jobe, E. Bancalari Bronchopulmonary dysplasia Am J Respir Crit Care Med 163 2001 1723 1729
56. J.V. Been, L.J. Zimmermann Histological chorioamnionitis and respiratory outcome in preterm infants Arch Dis Child Fetal Neonatal Ed 94 2009 F218 F225
57. L. Hartling, Y. Liang, T. Lacaze-Masmonteil Chorioamnionitis as a risk factor for bronchopulmonary dysplasia: a systematic review and meta-analysis Arch Dis Child Fetal Neonatal Ed 97 2012 F8 F17
58. K.J. Arntzen, A.M. Kjollesdal, J. Halgunset, L. Vatten, R. Austgulen TNF, IL-1, IL-6, IL-8 and soluble TNF receptors in relation to chorioamnionitis and premature labor J Perinat Med 26 1998 17 26
59. A. Witt, A. Berger, C.J. Gruber, L. Petricevic, P. Apfalter, P. Husslein IL-8 concentrations in maternal serum, amniotic fluid and cord blood in relation to different pathogens within the amniotic cavity J Perinat Med 33 2005 22 26
60. K. Bry, U. Lappalainen, M. Hallman Intraamniotic interleukin-1 accelerates surfactant protein synthesis in fetal rabbits and improves lung stability after premature birth J Clin Invest 99 1997 2992 2999
61. V. Glumoff, O. Vayrynen, T. Kangas, M. Hallman Degree of lung maturity determines the direction of the interleukin-1- induced effect on the expression of surfactant proteins Am J Respir Cell Mol Biol 22 2000 280 288
62. G.A. Emerson, K. Bry, M. Hallman Intra-amniotic interleukin-1 alpha treatment alters postnatal adaptation in premature lambs Biol Neonate 72 1997 370 379
63. K.E. Willet, B.W. Kramer, S.G. Kallapur Intra-amniotic injection of IL-1 induces inflammation and maturation in fetal sheep lung Am J Physiol Lung Cell Mol Physiol 282 2002 L411 L420
64. S.G. Kallapur, I. Nitsos, T.J. Moss IL-1 mediates pulmonary and systemic inflammatory responses to chorioamnionitis induced by lipopolysaccharide Am J Respir Crit Care Med 179 2009 955 961
65. A.H. Jobe, J.P. Newnham, K.E. Willet Effects of antenatal endotoxin and glucocorticoids on the lungs of preterm lambs Am J Obstet Gynecol 182 2000 401 408
66. C.J. Bachurski, G.F. Ross, M. Ikegami, B.W. Kramer, A.H. Jobe Intra-amniotic endotoxin increases pulmonary surfactant proteins and induces SP-B processing in fetal sheep Am J Physiol Lung Cell Mol Physiol 280 2001 L279 L285
67. A. Hogmalm, D. Sheppard, U. Lappalainen, K. Bry beta6 Integrin subunit deficiency alleviates lung injury in a mouse model of bronchopulmonary dysplasia Am J Respir Cell Mol Biol 43 2010 88 98
68. K. Bry, J.A. Whitsett, U. Lappalainen IL-1beta disrupts postnatal lung morphogenesis in the mouse Am J Respir Cell Mol Biol 36 2007 32 42
69. U. Lappalainen, J.A. Whitsett, S.E. Wert, J.W. Tichelaar, K. Bry Interleukin-1beta causes pulmonary inflammation, emphysema, and airway remodeling in the adult murine lung Am J Respir Cell Mol Biol 32 2005 311 318
70. B.W. Kramer, A. Ladenburger, S. Kunzmann Intravenous lipopolysaccharide- induced pulmonary maturation and structural changes in fetal sheep Am J Obstet Gynecol 200 2009 195 e1-10
71. G.R. Polglase, R.G. Dalton, I. Nitsos Pulmonary vascular and alveolar development in preterm lambs chronically colonized with Ureaplasma parvum Am J Physiol Lung Cell Mol Physiol 299 2010 L232 L241
72. A.H. Jobe, J.P. Newnham, K.E. Willet Endotoxin-induced lung maturation in preterm lambs is not mediated by cortisol Am J Respir Crit Care Med 162 2000 1656 1661
73. D.G. Sweet, M.T. Huggett, J.A. Warner Maternal betamethasone and chorioamnionitis induce different collagenases during lung maturation in fetal sheep Neonatology 94 2008 79 86
74. E. Kuypers, J.J. Collins, B.W. Kramer Intra-amniotic LPS and antenatal betamethasone: inflammation and maturation in preterm lamb lungs Am J Physiol Lung Cell Mol Physiol 302 2012 L380 L389
75. J.V. Been, I.G. Rours, R.F. Kornelisse Histologic chorioamnionitis, fetal involvement, and antenatal steroids: effects on neonatal outcome in preterm infants Am J Obstet Gynecol 201 2009 587.e1 587.e8
76. W. Thomas, C.P. Speer Chorioamnionitis: important risk factor or innocent bystander for neonatal outcome? Neonatology 99 2010 177 187
77. E.E. Morrisey, B.L. Hogan Preparing for the first breath: genetic and cellular mechanisms in lung development Dev Cell 18 2010 8 23
78. M.F. Beers, E.E. Morrisey The three R's of lung health and disease: repair, remodeling, and regeneration J Clin Invest 121 2011 2065 2073
79. B.W. Kramer, S. Kramer, M. Ikegami, A.H. Jobe Injury, inflammation, and remodeling in fetal sheep lung after intra-amniotic endotoxin Am J Physiol Lung Cell Mol Physiol 283 2002 L452 L459
80. B.W. Kramer, S. Kallapur, J. Newnham, A.H. Jobe Prenatal inflammation and lung development Semin Fetal Neonatal Med 14 2009 2 7
81. K.E. Willet, A.H. Jobe, M. Ikegami, J. Newnham, S. Brennan, P.D. Sly Antenatal endotoxin and glucocorticoid effects on lung morphometry in preterm lambs Pediatr Res 48 2000 782 788
82. S.G. Kallapur, C.J. Bachurski, T.D. Le Cras, S.N. Joshi, M. Ikegami, A.H. Jobe Vascular changes after intra-amniotic endotoxin in preterm lamb lungs Am J Physiol Lung Cell Mol Physiol 287 2004 L1178 L1185
83. S. Kunzmann, C.P. Speer, A.H. Jobe, B.W. Kramer Antenatal inflammation induced TGF-beta1 but suppressed CTGF in preterm lungs Am J Physiol Lung Cell Mol Physiol 292 2007 L223 L231
84. S. Kunzmann, J.J. Collins, Y. Yang Antenatal inflammation reduces expression of caveolin-1 and influences multiple signaling pathways in preterm fetal lungs Am J Respir Cell Mol Biol 45 2011 969 976
85. B.W. Kramer, A. Ladenburger, S. Kunzmann Intravenous lipopolysaccharide- induced pulmonary maturation and structural changes in fetal sheep Am J Obstet Gynecol 200 2009 195.e1 195.e10
86. J.J. Collins, S.G. Kallapur, C.L. Knox Inflammation in fetal sheep from intra-amniotic injection of Ureaplasma parvum Am J Physiol Lung Cell Mol Physiol 299 2010 L852 L860
87. A.K. Perl, E. Gale FGF signaling is required for myofibroblast differentiation during alveolar regeneration Am J Physiol Lung Cell Mol Physiol 297 2009 L299 L308
88. M. Weaver, N.R. Dunn, B.L. Hogan Bmp4 and Fgf10 play opposing roles during lung bud morphogenesis Development 127 2000 2695 2704
89. W. Thomas, S. Seidenspinner, B.W. Kramer Airway concentrations of angiopoietin-1 and endostatin in ventilated extremely premature infants are decreased after funisitis and unbalanced with bronchopulmonary dysplasia/death Pediatr Res 65 2009 468 473
90. W. Thomas, S. Seidenspinner, B.W. Kramer Airway angiopoietin-2 in ventilated very preterm infants: association with prenatal factors and neonatal outcome Pediatr Pulmonol 46 2011 777 784
91. T.D. Le Cras, N.E. Markham, R.M. Tuder, N.F. Voelkel, S.H. Abman Treatment of newborn rats with a VEGF receptor inhibitor causes pulmonary hypertension and abnormal lung structure Am J Physiol Lung Cell Mol Physiol 283 2002 L555 L562
92. M. Jakkula, T.D. Le Cras, S. Gebb Inhibition of angiogenesis decreases alveolarization in the developing rat lung Am J Physiol Lung Cell Mol Physiol 279 2000 L600 L607
93. A.J. Bhatt, G.S. Pryhuber, H. Huyck, R.H. Watkins, L.A. Metlay, W.M. Maniscalco Disrupted pulmonary vasculature and decreased vascular endothelial growth factor, Flt-1, and TIE-2 in human infants dying with bronchopulmonary dysplasia Am J Respir Crit Care Med 164 2001 1971 1980
94. G.R. Polglase, S.B. Hooper, A.W. Gill Intrauterine inflammation causes pulmonary hypertension and cardiovascular sequelae in preterm lambs J Appl Physiol 108 2010 1757 1765
95. D. Alapati, M. Rong, S. Chen Connective tissue growth factor antibody therapy attenuates hyperoxia-induced lung injury in neonatal rats Am J Respir Cell Mol Biol 45 2011 1169 1177
96. S. Chen, M. Rong, A. Platteau CTGF disrupts alveolarization and induces pulmonary hypertension in neonatal mice: implication in the pathogenesis of severe bronchopulmonary dysplasia Am J Physiol Lung Cell Mol Physiol 300 2011 L330 L340
97. S. Wu, A. Platteau, S. Chen, G. McNamara, J. Whitsett, E. Bancalari Conditional overexpression of connective tissue growth factor disrupts postnatal lung development Am J Respir Cell Mol Biol 42 2010 552 563
98. J. Gauldie, T. Galt, P. Bonniaud, C. Robbins, M. Kelly, D. Warburton Transfer of the active form of transforming growth factor-beta 1 gene to newborn rat lung induces changes consistent with bronchopulmonary dysplasia Am J Pathol 163 2003 2575 2584
99. A.G. Vicencio, C.G. Lee, S.J. Cho Conditional overexpression of bioactive transforming growth factor-beta1 in neonatal mouse lung: a new model for bronchopulmonary dysplasia? Am J Respir Cell Mol Biol 31 2004 650 656
100. H. Nakanishi, T. Sugiura, J.B. Streisand, S.M. Lonning, J.D. Roberts Jr TGF-beta-neutralizing antibodies improve pulmonary alveologenesis and vasculogenesis in the injured newborn lung Am J Physiol Lung Cell Mol Physiol 293 2007 L151 L161
101. M. Baguma-Nibasheka, B. Kablar Pulmonary hypoplasia in the connective tissue growth factor (CTGF) null mouse Dev Dyn 237 2008 485 493
102. H. Chen, J. Sun, S. Buckley Abnormal mouse lung alveolarization caused by Smad3 deficiency is a developmental antecedent of centrilobular emphysema Am J Physiol Lung Cell Mol Physiol 288 2005 L683 L691
103. H. Chen, F. Zhuang, Y.H. Liu TGF-beta receptor II in epithelia versus mesenchyme plays distinct roles in the developing lung Eur Respir J 32 2008 285 295
104. U.I. Heine, E.F. Munoz, K.C. Flanders, A.B. Roberts, M.B. Sporn Colocalization of TGF-beta 1 and collagen I and III, fibronectin and glycosaminoglycans during lung branching morphogenesis Development 109 1990 29 36
105. D. Lebeche, S. Malpel, W.V. Cardoso Fibroblast growth factor interactions in the developing lung Mech Dev 86 1999 125 136
106. H.D. Beer, C. Florence, J. Dammeier, L. McGuire, S. Werner, D.R. Duan Mouse fibroblast growth factor 10: cDNA cloning, protein characterization, and regulation of mRNA expression Oncogene 15 1997 2211 2218
107. M. Konigshoff, O. Eickelberg WNT signaling in lung disease: a failure or a regeneration signal? Am J Respir Cell Mol Biol 42 2010 21 31
108. Y. Litingtung, L. Lei, H. Westphal, C. Chiang Sonic hedgehog is essential to foregut development Nat Genet 20 1998 58 61
109. S. Bellusci, Y. Furuta, M.G. Rush, R. Henderson, G. Winnier, B.L. Hogan Involvement of Sonic hedgehog (Shh) in mouse embryonic lung growth and morphogenesis Development 124 1997 53 63
110. J.J. Collins, E. Kuypers, I. Nitsos LPS-induced chorioamnionitis and antenatal corticosteroids modulate Shh signaling in the ovine fetal lung Am J Physiol Lung Cell Mol Physiol 303 2012 L778 L787
111. J. Collins, E. Kuypers, I. Nitsos LPS-induced chorioamnionitis and antenatal corticosteroids modulate Wnt and Shh signaling in the fetal lung American Thoracic Society Meeting. New Orleans 2011
112. J.P. Shenai, F. Chytil, M.T. Stahlman Vitamin A status of neonates with bronchopulmonary dysplasia Pediatr Res 19 1985 185 188
113. B.W. Kramer, K.H. Albertine, T.J. Moss All-trans retinoic acid and intra-amniotic endotoxin-mediated effects on fetal sheep lung Anat Rec (Hoboken) 291 2008 1271 1277
114. A. Akhmetshina, K. Palumbo, C. Dees Activation of canonical Wnt signalling is required for TGF-beta-mediated fibrosis Nat Com 3 2012 735
115. M. Li, C. Li, Y.H. Liu Mesodermal deletion of transforming growth factor-beta receptor II disrupts lung epithelial morphogenesis: cross-talk between TGF-beta and Sonic hedgehog pathways J Biol Chem 283 2008 36257 36264
116. C. Li, L. Hu, J. Xiao Wnt5a regulates Shh and Fgf10 signaling during lung development Dev Biol 287 2005 86 97
117. P. Minoo, C. Li Cross-talk between transforming growth factor-beta and Wingless/Int pathways in lung development and disease Int J Biochem Cell Biol 42 2010 809 812
118. B. Razani, X.L. Zhang, M. Bitzer, G. von Gersdorff, E.P. Bottinger, M.P. Lisanti Caveolin-1 regulates transforming growth factor (TGF)-beta/SMAD signaling through an interaction with the TGF-beta type I receptor J Biol Chem 276 2001 6727 6738
119. B.W. Kramer, S.G. Kallapur, T.J. Moss, I. Nitsos, J.P. Newnham, A.H. Jobe Intra-amniotic LPS modulation of TLR signaling in lung and blood monocytes of fetal sheep Innate Immun 15 2009 101 107
120. B.W. Kramer, M. Ikegami, T.J. Moss, I. Nitsos, J.P. Newnham, A.H. Jobe Endotoxin-induced chorioamnionitis modulates innate immunity of monocytes in preterm sheep Am J Respir Crit Care Med 171 2005 73 77
121. S.G. Kallapur, A.H. Jobe, M.K. Ball Pulmonary and systemic endotoxin tolerance in preterm fetal sheep exposed to chorioamnionitis J Immunol 179 2007 8491 8499
122. B.W. Kramer, S.G. Kallapur, T.J. Moss Modulation of fetal inflammatory response on exposure to lipopolysaccharide by chorioamnion, lung, or gut in sheep Am J Obstet Gynecol 202 2010 77.e1 77.e9
123. S.G. Kallapur, B.W. Kramer, C.L. Knox Chronic fetal exposure to Ureaplasma parvum suppresses innate immune responses in sheep J Immunol 187 2011 2688 2695
124. T.G. Wolfs, R.K. Jellema, G. Turrisi, E. Becucci, G. Buonocore, B.W. Kramer Inflammation-induced immune suppression of the fetus: a potential link between chorioamnionitis and postnatal early onset sepsis J Matern Fetal Neonatal Med 25 Suppl 1 2012 8 11
125. B.W. Kramer, S.N. Joshi, T.J. Moss Endotoxin-induced maturation of monocytes in preterm fetal sheep lung Am J Physiol Lung Cell Mol Physiol 293 2007 L345 L353
126. B.W. Kramer, A.H. Jobe, M. Ikegami Monocyte function in preterm, term, and adult sheep Pediatr Res 54 2003 52 57
127. M. Azizia, J. Lloyd, M. Allen, N. Klein, D. Peebles Immune status in very preterm neonates Pediatrics 129 2012 e967 e974
128. P.C. Greig, W.N. Herbert, B.L. Robinette, L.A. Teot Amniotic fluid interleukin-10 concentrations increase through pregnancy and are elevated in patients with preterm labor associated with intrauterine infection Am J Obstet Gynecol 173 1995 1223 1227
129. J. Wirbelauer, S. Seidenspinner, W. Thomas, S. Kunzmann, C.P. Speer Funisitis is associated with increased interleukin-10 gene expression in cord blood mononuclear cells in preterm infants
130. N.H. Hillman, T.J. Moss, I. Nitsos Toll-like receptors and agonist responses in the developing fetal sheep lung Pediatr Res 63 2008 388 393
131. N. Suzuki, T. Saito IRAK-4 - a shared NF-kappaB activator in innate and acquired immunity Trend Immunol 27 2006 566 572
132. B.W. Kramer, A.H. Jobe The clever fetus: responding to inflammation to minimize lung injury Biol Neonate 88 2005 202 207
133. S.G. Kallapur, I. Nitsos, T.J. Moss Chronic endotoxin exposure does not cause sustained structural abnormalities in the fetal sheep lungs Am J Physiol Lung Cell Mol Physiol 288 2005 L966 L974
134. A. Greenough Long term respiratory outcomes of very premature birth (<32 weeks) Semin Fetal Neonatal Med 17 2012 73 76
135. C. De Felice, P. Toti, R. Santopietro, M. Stumpo, L. Pecciarini, F. Bagnoli Small thymus in very low birth weight infants born to mothers with subclinical chorioamnionitis J Pediatr 135 1999 384 386
136. C. De Felice, G. Latini, A. Del Vecchio, P. Toti, F. Bagnoli, F. Petraglia Small thymus at birth: a predictive radiographic sign of bronchopulmonary dysplasia Pediatrics 110 2002 386 388
137. Y. Yinon, Y. Zalel, B. Weisz Fetal thymus size as a predictor of chorioamnionitis in women with preterm premature rupture of membranes Ultrasound Obstet Gynecol 29 2007 639 643
138. D.L. Jeppesen, H. Hasselbalch, S.D. Nielsen Thymic size in preterm neonates: a sonographic study Acta Paediatr 92 2003 817 822
139. P. Toti, C. De Felice, M. Stumpo Acute thymic involution in fetuses and neonates with chorioamnionitis Hum Pathol 31 2000 1121 1128
140. D. Rosen, J.H. Lee, F. Cuttitta, F. Rafiqi, S. Degan, M.E. Sunday Accelerated thymic maturation and autoreactive T cells in bronchopulmonary dysplasia Am J Respir Crit Care Med 174 2006 75 83
141. S. Kunzmann, K. Glogger, J.V. Been Thymic changes after chorioamnionitis induced by intraamniotic lipopolysaccharide in fetal sheep Am J Obstet Gynecol 202 2010 476.e1 476.e9