Ovine fetal thymus response to lipopolysaccharide-induced chorioamnionitis and antenatal corticosteroids

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Kuypers, Elke ^a   Collins, Jennifer J P ^a   Jellema, Reint K ^a   Wolfs, Tim G A M ^a   Kemp, Matthew W ^b   Nitsos, Ilias ^b,d   Pillow, J Jane ^b   Polglase, Graeme R ^b,d   Newnham, John P ^b   Germeraad, Wilfred T V ^a   Kallapur, Suhas G ^b,c   Jobe, Alan H ^b,c   Kramer, Boris W ^a  

^a MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^c UNIVERSITY OF CINCINNATI   (United States)

^d HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BETAMETHASONE; BONE MORPHOGENETIC PROTEIN 4; CASPASE 3; CD3 ANTIGEN; CELESTON SOLUSPAN; LIPOPOLYSACCHARIDE; SONIC HEDGEHOG PROTEIN; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG; CORTICOSTEROID; FORKHEAD TRANSCRIPTION FACTOR; TOLL LIKE RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; CELL MATURATION; CHORIOAMNIONITIS; CONTROLLED STUDY; FEMALE; FETUS; GENE; GENE EXPRESSION; IMMUNE RESPONSE; INVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRENATAL PERIOD; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; THYMUS; THYMUS FUNCTION; TLR4 GENE; ANIMAL; CELL PROLIFERATION; CHEMICALLY INDUCED DISORDER; CYTOLOGY; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; PREGNANCY; PRENATAL DEVELOPMENT; SHEEP; T LYMPHOCYTE; TIME;

ERINACEIDAE; OVIS;

ADRENAL CORTEX HORMONES; ANIMALS; ANTIGENS, CD3; APOPTOSIS; BONE MORPHOGENETIC PROTEIN 4; CELL PROLIFERATION; CHORIOAMNIONITIS; FEMALE; FETUS; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; HEDGEHOG PROTEINS; LIPOPOLYSACCHARIDES; PREGNANCY; SHEEP; T-LYMPHOCYTES; THYMUS GLAND; TIME FACTORS; TOLL-LIKE RECEPTORS;

EID: 84861691261     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0038257     Document Type: Article

References (51)

1. Goldenberg RL, Culhane JF, Iams JD, Romero R, (2008) Epidemiology and causes of preterm birth. Lancet 371: 75-84.
2. Been JV, Degraeuwe PL, Kramer BW, Zimmermann LJ, (2010) Antenatal steroids and neonatal outcome after chorioamnionitis: a meta-analysis. BJOG 118: 113-122.
3. Goldenberg RL, Hauth JC, Andrews WW, (2000) Intrauterine infection and preterm delivery. N Engl J Med 342: 1500-1507.
4. Hartling L, Liang Y, Lacaze-Masmonteil T, (2012) Chorioamnionitis as a risk factor for bronchopulmonary dysplasia: a systematic review and meta-analysis. Arch Dis Child Fetal Neonatal Ed 97: F8-F17.
5. Shatrov JG, Birch SC, Lam LT, Quinlivan JA, McIntyre S, et al. (2010) Chorioamnionitis and cerebral palsy: a meta-analysis. Obstet Gynecol 116: 387-392.
6. Kallapur SG, Willet KE, Jobe AH, Ikegami M, Bachurski CJ, (2001) Intra-amniotic endotoxin: chorioamnionitis precedes lung maturation in preterm lambs. Am J Physiol Lung Cell Mol Physiol 280: L527-536.
7. Kuypers E, Collins JJ, Kramer BW, Ofman G, Nitsos I, et al. (2012) Intra-amniotic LPS and antenatal betamethasone: inflammation and maturation in preterm lamb lungs. Am J Physiol Lung Cell Mol Physiol 302: L380-389.
8. Wolfs TG, Buurman WA, Zoer B, Moonen RM, Derikx JP, et al. (2009) Endotoxin induced chorioamnionitis prevents intestinal development during gestation in fetal sheep. PLoS One 4: e5837.
9. Kemp MW, Saito M, Nitsos I, Jobe AH, Kallapur SG, et al. (2010) Exposure to in utero lipopolysaccharide induces inflammation in the fetal ovine skin. Reprod Sci 18: 88-98.
10. Gantert M, Been JV, Gavilanes AW, Garnier Y, Zimmermann LJ, et al. (2010) Chorioamnionitis: a multiorgan disease of the fetus? J Perinatol 30 (Suppl): S21-30.
11. Getahun D, Strickland D, Zeiger RS, Fassett MJ, Chen W, et al. (2010) Effect of chorioamnionitis on early childhood asthma. Arch Pediatr Adolesc Med 164: 187-192.
12. Rosen D, Lee JH, Cuttitta F, Rafiqi F, Degan S, et al. (2006) Accelerated thymic maturation and autoreactive T cells in bronchopulmonary dysplasia. Am J Respir Crit Care Med 174: 75-83.
13. Kramer BW, Kallapur SG, Moss TJ, Nitsos I, Newnham JP, et al. (2009) Intra-amniotic LPS modulation of TLR signaling in lung and blood monocytes of fetal sheep. Innate Immun 15: 101-107.
14. Pearse G, (2006) Normal structure, function and histology of the thymus. Toxicol Pathol 34: 504-514.
15. Yinon Y, Zalel Y, Weisz B, Mazaki-Tovi S, Sivan E, et al. (2007) Fetal thymus size as a predictor of chorioamnionitis in women with preterm premature rupture of membranes. Ultrasound Obstet Gynecol 29: 639-643.
16. De Felice C, Toti P, Santopietro R, Stumpo M, Pecciarini L, et al. (1999) Small thymus in very low birth weight infants born to mothers with subclinical chorioamnionitis. J Pediatr 135: 384-386.
17. Kunzmann S, Glogger K, Been JV, Kallapur SG, Nitsos I, et al. (2010) Thymic changes after chorioamnionitis induced by intraamniotic lipopolysaccharide in fetal sheep. Am J Obstet Gynecol 202: 476-485.
18. Kramer BW, Kallapur SG, Moss TJ, Nitsos I, Polglase GP, et al. (2009) Modulation of fetal inflammatory response on exposure to lipopolysaccharide by chorioamnion, lung, or gut in sheep. Am J Obstet Gynecol 202: 77-86.
19. Crompton T, Outram SV, Hager-Theodorides AL, (2007) Sonic hedgehog signalling in T-cell development and activation. Nat Rev Immunol 7: 726-735.
20. Lowrey JA, Stewart GA, Lindey S, Hoyne GF, Dallman MJ, et al. (2002) Sonic hedgehog promotes cell cycle progression in activated peripheral CD4(+) T lymphocytes. J Immunol 169: 1869-1875.
21. Hanson ML, Brundage KM, Schafer R, Tou JC, Barnett JB, (2009) Prenatal cadmium exposure dysregulates sonic hedgehog and Wnt/beta-catenin signaling in the thymus resulting in altered thymocyte development. Toxicol Appl Pharmacol 242: 136-145.
22. Sacedon R, Varas A, Hernandez-Lopez C, Gutierrez-deFrias C, Crompton T, et al. (2003) Expression of hedgehog proteins in the human thymus. J Histochem Cytochem 51: 1557-1566.
23. Hager-Theodorides AL, Outram SV, Shah DK, Sacedon R, Shrimpton RE, et al. (2002) Bone morphogenetic protein 2/4 signaling regulates early thymocyte differentiation. J Immunol 169: 5496-5504.
24. Kramer BW, Moss TJ, Willet KE, Newnham JP, Sly PD, et al. (2001) Dose and time response after intraamniotic endotoxin in preterm lambs. Am J Respir Crit Care Med 164: 982-988.
25. Crowther CA, Harding JE, (2007) Repeat doses of prenatal corticosteroids for women at risk of preterm birth for preventing neonatal respiratory disease. Cochrane Database Syst Rev pp. CD003935.
26. Ballard PL, Ballard RA, (1995) Scientific basis and therapeutic regimens for use of antenatal glucocorticoids. Am J Obstet Gynecol 173: 254-262.
27. Toti P, De Felice C, Stumpo M, Schurfeld K, Di Leo L, et al. (2000) Acute thymic involution in fetuses and neonates with chorioamnionitis. Hum Pathol 31: 1121-1128.
28. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
29. Outram SV, Varas A, Pepicelli CV, Crompton T, (2000) Hedgehog signaling regulates differentiation from double-negative to double-positive thymocyte. Immunity 13: 187-197.
30. Gutierrez-Frias C, Sacedon R, Hernandez-Lopez C, Cejalvo T, Crompton T, et al. (2004) Sonic hedgehog regulates early human thymocyte differentiation by counteracting the IL-7-induced development of CD34+ precursor cells. J Immunol 173: 5046-5053.
31. Cejalvo T, Sacedon R, Hernandez-Lopez C, Diez B, Gutierrez-Frias C, et al. (2007) Bone morphogenetic protein-2/4 signalling pathway components are expressed in the human thymus and inhibit early T-cell development. Immunology 121: 94-104.
32. Graf D, Nethisinghe S, Palmer DB, Fisher AG, Merkenschlager M, (2002) The developmentally regulated expression of Twisted gastrulation reveals a role for bone morphogenetic proteins in the control of T cell development. J Exp Med 196: 163-171.
33. Dave VP, (2009) Hierarchical role of CD3 chains in thymocyte development. Immunol Rev 232: 22-33.
34. Kallapur SG, Kramer BW, Moss TJ, Newnham JP, Jobe AH, et al. (2003) Maternal glucocorticoids increase endotoxin-induced lung inflammation in preterm lambs. Am J Physiol Lung Cell Mol Physiol 284: L633-642.
35. Newnham JP, Kallapur SG, Kramer BW, Moss TJ, Nitsos I, et al. (2003) Betamethasone effects on chorioamnionitis induced by intra-amniotic endotoxin in sheep. Am J Obstet Gynecol 189: 1458-1466.
36. Tonomura N, McLaughlin K, Grimm L, Goldsby RA, Osborne BA, (2003) Glucocorticoid-induced apoptosis of thymocytes: requirement of proteasome-dependent mitochondrial activity. J Immunol 170: 2469-2478.
37. Wang X, Nelin LD, Kuhlman JR, Meng X, Welty SE, et al. (2008) The role of MAP kinase phosphatase-1 in the protective mechanism of dexamethasone against endotoxemia. Life Sci 83: 671-680.
38. Kramer BW, Ikegami M, Moss TJ, Nitsos I, Newnham JP, et al. (2004) Antenatal betamethasone changes cord blood monocyte responses to endotoxin in preterm lambs. Pediatr Res 55: 764-768.
39. Sloboda DM, Newnham JP, Challis JR, (2000) Effects of repeated maternal betamethasone administration on growth and hypothalamic-pituitary-adrenal function of the ovine fetus at term. J Endocrinol 165: 79-91.
40. Bakker JM, Schmidt ED, Kroes H, Kavelaars A, Heijnen CJ, et al. (1995) Effects of short-term dexamethasone treatment during pregnancy on the development of the immune system and the hypothalamo-pituitary adrenal axis in the rat. J Neuroimmunol 63: 183-191.
41. Chabra S, Cottrill C, Rayens MK, Cross R, Lipke D, et al. (1998) Lymphocyte subsets in cord blood of preterm infants: effect of antenatal steroids. Biol Neonate 74: 200-207.
42. Kavelaars A, van der Pompe G, Bakker JM, van Hasselt PM, Cats B, et al. (1999) Altered immune function in human newborns after prenatal administration of betamethasone: enhanced natural killer cell activity and decreased T cell proliferation in cord blood. Pediatr Res 45: 306-312.
43. Wu FF, Momma K, Takao A, (1993) Cardiovascular and pulmonary effects of betamethasone during midtrimester on fetal rats. Fetal Diagn Ther 8: 89-94.
44. Quinlivan JA, Archer MA, Dunlop SA, Evans SF, Beazley LD, et al. (1998) Fetal growth retardation, particularly within lymphoid organs, following repeated maternal injections of betamethasone in sheep. J Obstet Gynaecol Res 24: 173-182.
45. Michie CA, Hasson N, Tulloh R, (1998) The neonatal thymus and antenatal steroids. Arch Dis Child Fetal Neonatal Ed 79: F159.
46. Bakker JM, Schmidt ED, Kroes H, Kavelaars A, Heijnen CJ, et al. (1997) Effects of neonatal dexamethasone treatment on hypothalamo-pituitary adrenal axis and immune system of the rat. J Neuroimmunol 74: 69-76.
47. Bakker JM, Kavelaars A, Kamphuis PJ, Zijlstra J, van Bel F, et al. (2001) Neonatal dexamethasone treatment induces long-lasting changes in T-cell receptor vbeta repertoire in rats. J Neuroimmunol 112: 47-54.
48. Bakker JM, Kavelaars A, Kamphuis PJ, Cobelens PM, van Vugt HH, et al. (2000) Neonatal dexamethasone treatment increases susceptibility to experimental autoimmune disease in adult rats. J Immunol 165: 5932-5937.
49. Smolders-de Haas H, Neuvel J, Schmand B, Treffers PE, Koppe JG, et al. (1990) Physical development and medical history of children who were treated antenatally with corticosteroids to prevent respiratory distress syndrome: a 10- to 12-year follow-up. Pediatrics 86: 65-70.
50. Kramer BW, Ikegami M, Moss TJ, Nitsos I, Newnham JP, et al. (2005) Endotoxin-induced chorioamnionitis modulates innate immunity of monocytes in preterm sheep. Am J Respir Crit Care Med 171: 73-77.
51. Kumar R, Yu Y, Story RE, Pongracic JA, Gupta R, et al. (2008) Prematurity, chorioamnionitis, and the development of recurrent wheezing: a prospective birth cohort study. J Allergy Clin Immunol 121: 878-884 e876.