Mice deficient in surfactant protein A (SP-A) and SP-D or in TLR2 manifest delayed parturition and decreased expression of inflammatory and contractile genes

Endocrinology

Volumn 154, Issue 1, 2013, Pages 483-498

  Montalbano, Alina P ^a   Hawgood, Samuel ^b   Mendelson, Carole R ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MARKER; CONNEXIN 43; INTERLEUKIN 1BETA; INTERLEUKIN 6; MYOMETRIAL CONTRACTION ASSOCIATED PROTEIN; OXYTOCIN RECEPTOR; PROTEIN; SURFACTANT PROTEIN A; SURFACTANT PROTEIN D; TOLL LIKE RECEPTOR 2; UNCLASSIFIED DRUG;

AMNION FLUID; ANIMAL EXPERIMENT; ARTICLE; BIRTH; COITUS; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HOMOZYGOTE; LABOR; MACROPHAGE; MOUSE; MYOMETRIUM; NONHUMAN; PREGNANCY; PRIORITY JOURNAL;

AMNIOTIC FLUID; ANIMALS; CELLS, CULTURED; FEMALE; FLOW CYTOMETRY; LUNG; MICE; MICE, KNOCKOUT; MYOMETRIUM; PARTURITION; PREGNANCY; PULMONARY SURFACTANT-ASSOCIATED PROTEIN A; PULMONARY SURFACTANT-ASSOCIATED PROTEIN D; REAL-TIME POLYMERASE CHAIN REACTION; TOLL-LIKE RECEPTOR 2;

EID: 84871683969     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-1797     Document Type: Article

References (84)

1. Blencowe H, Cousens S, Oestergaard MZ, Chou D, Moller AB, Narwal R, Adler A, Vera Garcia C, Rohde S, Say L, Lawn JE 2012 National, regional, and worldwide estimates of preterm birth rates in the year 2010 with time trends since 1990 for selected countries: a systematic analysis and implications. Lancet 379:2162-2172
2. Romero R, Mazor M, Wu YK, Sirtori M, Oyarzun E, Mitchell MD, Hobbins JC 1988 Infection in the pathogenesis of preterm labor. Semin Perinatol 12:262-279
3. Green NS, Damus K, Simpson JL, Iams J, Reece EA, Hobel CJ, Merkatz IR, Greene MF, Schwarz RH 2005 Research agenda for preterm birth: recommendations from the March of Dimes. Am J Obstet Gynecol 193:626-635 (Pubitemid 41261455)
4. Goldenberg RL, Culhane JF, Iams JD, Romero R 2008 Epidemiology and causes of preterm birth. Lancet 371:75-84
5. Hirsch E, Wang H 2005 The molecular pathophysiology of bacterially induced preterm labor: insights from the murine model. J Soc Gynecol Investig 12:145-155 (Pubitemid 40387807)
6. Elovitz MA, Mrinalini C 2004 Animal models of preterm birth. Trends Endocrinol Metab 15:479-487 (Pubitemid 39488151)
7. Challis JR, Lockwood CJ, Myatt L, Norman JE, Strauss 3rd JF, Petraglia F 2009 Inflammation and pregnancy. Reprod Sci 16:206-215
8. Mendelson CR 2009 Minireview: fetal-maternal hormonal signaling in pregnancy and labor. Mol Endocrinol 23:947-954
9. Cox SM, Casey ML, MacDonald PC 1997 Accumulation of interleukin- 1β and interleukin-6 in amniotic fluid: a sequela of labour at term and preterm. Hum Reprod Update 3:517-527 (Pubitemid 28069955)
10. Thomson AJ, Telfer JF, Young A, Campbell S, Stewart CJ, Cameron IT, Greer IA, Norman JE 1999 Leukocytes infiltrate the myometrium during human parturition: further evidence that labour is an inflammatory process. Hum Reprod 14:229-236 (Pubitemid 29046344)
11. Osman I, Young A, Ledingham MA, Thomson AJ, Jordan F, Greer IA, Norman JE 2003 Leukocyte density and pro-inflammatory cytokine expression in human fetal membranes, decidua, cervix and myometrium before and during labour at term. Mol Hum Reprod 9:41-45 (Pubitemid 36285142)
12. Shynlova O, Tsui P, Jaffer S, Lye SJ 2009 Integration of endocrine and mechanical signals in the regulation of myometrial functions during pregnancy and labour. Eur J Obstet Gynecol Reprod Biol 144(Suppl 1):S2-S10
13. Romero R, Espinoza J, Gonçalves LF, Kusanovic JP, Friel L, Hassan S 2007 The role of inflammation and infection in preterm birth. Semin Reprod Med 25:21-39 (Pubitemid 46147842)
14. Condon JC, Jeyasuria P, Faust JM, Mendelson CR 2004 Surfactant protein secreted by the maturing mouse fetal lung acts as a hormone that signals the initiation of parturition. Proc Natl Acad Sci USA 101:4978-4983 (Pubitemid 38469188)
15. López Bernal A, Newman GE, Phizackerley PJ, Turnbull AC 1988 Surfactant stimulates prostaglandin E production in human amnion. Br J Obstet Gynaecol 95:1013-1017
16. Mendelson CR, Boggaram V 1990 Hormonal and developmental regulation of pulmonary surfactant synthesis in fetal lung. Baillieres Clin Endocrinol Metab 4:351-378 (Pubitemid 20282608)
17. Whitsett JA, Weaver TE 2002 Hydrophobic surfactant proteins in lung function and disease. N Engl J Med 347:2141-2148 (Pubitemid 36015127)
18. Hawgood S, Shiffer K 1991 Structures and properties of the surfactant- associated proteins. Annu Rev Physiol 53:375-394
19. Hawgood S, Poulain FR 2001 The pulmonary collectins and surfactant metabolism. Annu Rev Physiol 63:495-519 (Pubitemid 32304327)
20. Snyder JM, Kwun JE, O'Brien JA, Rosenfeld CR, Odom MJ 1988 The concentration of the 35-kDa surfactant apoprotein in amniotic fluid from normal and diabetic pregnancies. Pediatr Res 24:728-734 (Pubitemid 19013155)
21. Mendelson CR, Condon JC 2005 New insights into the molecular endocrinology of parturition. J Steroid Biochem Mol Biol 93:113-119 (Pubitemid 40602483)
22. Drickamer K 1999 C-type lectin-like domains. Curr Opin Struct Biol 9:585-590 (Pubitemid 29460584)
23. Seaton BA, Crouch EC, McCormack FX, Head JF, Hartshorn KL, Mendelsohn R 2010 Review: structural determinants of pattern recognition by lung collectins. Innate Immun 16:143-150
24. Kuroki Y, Takahashi M, Nishitani C 2007 Pulmonary collectins in innate immunity of the lung. Cell Microbiol 9:1871-1879 (Pubitemid 47087079)
25. Crouch E, Wright JR 2001 Surfactant proteins A and D and pulmonary host defense. Annu Rev Physiol 63:521-554 (Pubitemid 32304328)
26. Kingma PS, Whitsett JA 2006 In defense of the lung: surfactant protein A and surfactant protein D. Curr Opin Pharmacol 6:277-283 (Pubitemid 43670905)
27. Wright JR 2005 Immunoregulatory functions of surfactant proteins. Nat Rev Immunol 5:58-68 (Pubitemid 40070331)
28. Guillot L, Balloy V, McCormack FX, Golenbock DT, Chignard M, Si-Tahar M 2002 Cutting edge: the immunostimulatory activity of the lung surfactant protein-A involves Toll-like receptor 4. J Immunol 168:5989-5992 (Pubitemid 34620010)
29. Murakami S, Iwaki D, Mitsuzawa H, Sano H, Takahashi H, Voelker DR, Akino T, Kuroki Y 2002 Surfactant protein A inhibits peptidoglycan- induced tumor necrosis factor-α secretion in U937 cells and alveolar macrophages by direct interaction with toll-like receptor 2. J Biol Chem 277:6830-6837 (Pubitemid 34953065)
30. Gardai SJ, Xiao YQ, Dickinson M, Nick JA, Voelker DR, Greene KE, Henson PM 2003 By binding SIRPα or calreticulin/CD91, lung collectins act as dual function surveillance molecules to suppress or enhance inflammation. Cell 115:13-23 (Pubitemid 37255314)
31. Sano H, Kuroki Y 2005 The lung collectins, SP-A and SP-D, modulate pulmonary innate immunity. Mol Immunol 42:279-287 (Pubitemid 39626759)
32. Mukherjee S, Giamberardino C, Thomas J, Evans K, Goto H, Ledford JG, Hsia B, Pastva AM, Wright JR 2012 Surfactant protein A integrates activation signal strength to differentially modulate T cell proliferation. J Immunol 188:957-967
33. Sato M, Sano H, Iwaki D, Kudo K, Konishi M, Takahashi H, Takahashi T, Imaizumi H, Asai Y, Kuroki Y 2003 Direct binding of Toll-like receptor 2 to zymosan, and zymosan-induced NF-κB activation and TNF-α secretion are down-regulated by lung collectin surfactant protein A. J Immunol 171:417-425 (Pubitemid 36745315)
34. Ohya M, Nishitani C, Sano H, Yamada C, Mitsuzawa H, Shimizu T, Saito T, Smith K, Crouch E, Kuroki Y 2006 Human pulmonary surfactant protein D binds the extracellular domains of Toll-like receptors 2 and 4 through the carbohydrate recognition domain by a mechanism different from its binding to phosphatidylinositol and lipopolysaccharide. Biochemistry 45:8657-8664 (Pubitemid 44078886)
35. Tsan MF, Gao B 2004 Endogenous ligands of Toll-like receptors. J Leukoc Biol 76:514-519 (Pubitemid 39129081)
36. Yamada C, Sano H, Shimizu T, Mitsuzawa H, Nishitani C, Himi T, Kuroki Y 2006 Surfactant protein A directly interacts with TLR4 and MD-2 and regulates inflammatory cellular response. Importance of supratrimeric oligomerization. J Biol Chem 281:21771-21780 (Pubitemid 44181881)
37. Janeway Jr CA, Medzhitov R 2002 Innate immune recognition. Annu Rev Immunol 20:197-216 (Pubitemid 34293424)
38. Medzhitov R 2001 Toll-like receptors and innate immunity. Nat Rev Immunol 1:135-145 (Pubitemid 33741967)
39. Li G, Siddiqui J, Hendry M, Akiyama J, Edmondson J, Brown C, Allen L, Levitt S, Poulain F, Hawgood S 2002 Surfactant protein A-deficient mice display an exaggerated early inflammatory response to a β-resistant strain of influenza A virus. Am J Respir Cell Mol Biol 26:277-282 (Pubitemid 34170054)
40. Botas C, Poulain F, Akiyama J, Brown C, Allen L, Goerke J, Clements J, Carlson E, Gillespie AM, Epstein C, Hawgood S 1998 Altered surfactant homeostasis and alveolar type II cell morphology in mice lacking surfactant protein D. Proc Natl Acad Sci USA 95: 11869-11874 (Pubitemid 28460506)
41. Hawgood S, Ochs M, Jung A, Akiyama J, Allen L, Brown C, Edmondson J, Levitt S, Carlson E, Gillespie AM, Villar A, Epstein CJ, Poulain FR 2002 Sequential targeted deficiency of SP-A and -D leads to progressive alveolar lipoproteinosis and emphysema. Am J Physiol Lung Cell Mol Physiol 283:L1002-L1010 (Pubitemid 35204892)
42. Chomczynski P, Sacchi N 1987 Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159 (Pubitemid 17064313)
43. Livak KJ, Schmittgen TD 2001 Analysis of relative gene expression data using real-time quantitative PCR and the 2[-ΔΔC(T)] method. Methods 25:402-408 (Pubitemid 34164012)
44. Murray SA, Morgan JL, Kane C, Sharma Y, Heffner CS, Lake J, Donahue LR 2010 Mouse gestation length is genetically determined. PLoS One 5:e12418
45. Yan X, Sun M, Gibb W 2002 Localization of nuclear factor-κB (NF-κB) and inhibitory factor-κB (IκB) in human fetal membranes and decidua at term and preterm delivery. Placenta 23:288-293 (Pubitemid 41348521)
46. Chow L, Lye SJ 1994 Expression of the gap junction protein connexin- 43 is increased in the human myometrium toward term and with the onset of labor. Am J Obstet Gynecol 170:788-795 (Pubitemid 24224700)
47. Ou CW, Chen ZQ, Qi S, Lye SJ 1998 Increased expression of the rat myometrial oxytocin receptor messenger ribonucleic acid during labor requires both mechanical and hormonal signals. Biol Reprod 59:1055-1061 (Pubitemid 28498914)
48. Renthal NE, Chen CC, Williams KC, Gerard RD, Prange-Kiel J, Mendelson CR 2010 miR-200 family and targets, ZEB1 and ZEB2, modulate uterine quiescence and contractility during pregnancy and labor. Proc Natl Acad Sci U S A 107:20828-20833
49. Takeuchi O, Hoshino K, Kawai T, Sanjo H, Takada H, Ogawa T, Takeda K, Akira S 1999 Differential roles of TLR2 and TLR4 in recognition of gram-negative and Gram-positive bacterial cell wall components. Immunity 11:443-451 (Pubitemid 29504199)
50. Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, Birdwell D, Alejos E, Silva M, Galanos C, Freudenberg M, Ricciardi- Castagnoli P, Layton B, Beutler B 1998 Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282:2085-2088
51. Canavan TP, Simhan HN 2007 Innate immune function of the human decidual cell at the maternal-fetal interface. J Reprod Immunol 74:46-52 (Pubitemid 46679062)
52. Youssef RE, Ledingham MA, Bollapragada SS, O'Gorman N, Jordan F, Young A, Norman JE 2009 The role of toll-like receptors (TLR-2 and -4) and triggering receptor expressed on myeloid cells 1 (TREM-1) in human term and preterm labor. Reprod Sci 16:843-856
53. O'Brien M, Morrison JJ, Smith TJ 2008 Upregulation of PSCDBP, TLR2, TWIST1, FLJ35382, EDNRB, and RGS 12 gene expression in human myometrium at labor. Reprod Sci 15:382-393 (Pubitemid 351697337)
54. Henning LN, Azad AK, Parsa KV, Crowther JE, Tridandapani S, Schlesinger LS 2008 Pulmonary surfactant protein A regulates TLR expression and activity in human macrophages. J Immunol 180: 7847-7858
55. Luther SA, Bidgol A, Hargreaves DC, Schmidt A, Xu Y, Paniyadi J, Matloubian M, Cyster JG 2002 Differing activities of homeostatic chemokines CCL19, CCL21, and CXCL12 in lymphocyte and dendritic cell recruitment and lymphoid neogenesis. J Immunol 169: 424-433 (Pubitemid 34686164)
56. Hershey GK 2003 IL-13 receptors and signaling pathways: an evolving web. J Allergy Clin Immunol 111:677-690; quiz 691
57. Locksley RM, Killeen N, Lenardo MJ 2001 The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 104: 487-501 (Pubitemid 32201945)
58. Homey B, Alenius H, Müller A, Soto H, Bowman EP, Yuan W, McEvoy L, Lauerma AI, Assmann T, Bünemann E, Lehto M, Wolff H, Yen D, Marxhausen H, To W, Sedgwick J, Ruzicka T, Lehmann P, Zlotnik A 2002 CCL27-CCR10 interactions regulate T cell-mediated skin inflammation. Nat Med 8:157-165 (Pubitemid 34155127)
59. Karjalainen MK, Huusko JM, Tuohimaa A, Luukkonen A, Haataja R, Hallman M 2012 A study of collectin genes in spontaneous preterm birth reveals an association with a common surfactant protein D gene polymorphism. Pediatr Res 71:93-99
60. Shynlova O, Tsui P, Dorogin A, Lye SJ 2008 Monocyte chemoattractant protein-1 (CCL-2) integrates mechanical and endocrine signals that mediate term and preterm labor. J Immunol 181:1470-1479
61. Sooranna SR, Lee Y, Kim LU, Mohan AR, Bennett PR, Johnson MR 2004 Mechanical stretch activates type 2 cyclooxygenase via activator protein-1 transcription factor in human myometrial cells. Mol Hum Reprod 10:109-113 (Pubitemid 38196512)
62. Wu X, Morgan KG, Jones CJ, Tribe RM, Taggart MJ 2008 Myometrial mechanoadaptation during pregnancy: implications for smooth muscle plasticity and remodelling. J Cell Mol Med 12:1360-1373
63. Keelan JA, Blumenstein M, Helliwell RJ, Sato TA, Marvin KW, Mitchell MD 2003 Cytokines, prostaglandins and parturition-a review. Placenta 24(Suppl A):S33-S46
64. Hardy DB, Janowski BA, Corey DR, Mendelson CR 2006 Progesterone receptor (PR) plays a major anti-inflammatory role in human myometrial cells by antagonism of NF-κB activation of cyclooxygenase 2 (COX-2) expression. Mol Endocrinol 20:2724-2733 (Pubitemid 44834326)
65. Dong YL, Gangula PR, Fang L, Yallampalli C 1996 Differential expression of cyclooxygenase-1 and -2 proteins in rat uterus and cervix during the estrous cycle, pregnancy, labor and in myometrial cells. Prostaglandins 52:13-34 (Pubitemid 26299822)
66. Allport VC, Pieber D, Slater DM, Newton R, White JO, Bennett PR 2001 Human labour is associated with nuclear factor-κB activity which mediates cyclo-oxygenase-2 expression and is involved with the 'functional progesterone withdrawal.' Mol Hum Reprod 7:581-586 (Pubitemid 32536878)
67. Dudley DJ, Collmer D, Mitchell MD, Trautman MS 1996 Inflammatory cytokine mRNA in human gestational tissues: implications for term and preterm labor. J Soc Gynecol Investig 3:328-335 (Pubitemid 26374248)
68. Romero R, Parvizi ST, Oyarzun E, Mazor M, Wu YK, Avila C, Athanassiadis AP, Mitchell MD 1990 Amniotic fluid interleukin-1 in spontaneous labor at term. J Reprod Med 35:235-238 (Pubitemid 20137791)
69. Abbondanzo SJ, Cullinan EB, McIntyre K, Labow MA, Stewart CL 1996 Reproduction in mice lacking a functional type 1 IL-1 receptor. Endocrinology 137:3598-3601 (Pubitemid 26250218)
70. Sadowsky DW, Adams KM, Gravett MG, Witkin SS, Novy MJ 2006 Preterm labor is induced by intraamniotic infusions of interleukin- 1β and tumor necrosis factor-α but not by interleukin-6 or interleukin- 8 in a nonhuman primate model. Am J Obstet Gynecol 195:1578-1589 (Pubitemid 44792645)
71. Romero R, Mazor M, Tartakovsky B 1991 Systemic administration of interleukin-1 induces preterm parturition in mice. Am J Obstet Gynecol 165:969-971
72. Yoshimura K, Hirsch E 2003 Interleukin-6 is neither necessary nor sufficient for preterm labor in a murine infection model. J Soc Gynecol Investig 10:423-427 (Pubitemid 37159229)
73. Robertson SA, Christiaens I, Dorian CL, Zaragoza DB, Care AS, Banks AM, Olson DM 2010 Interleukin-6 is an essential determinant of on-time parturition in the mouse. Endocrinology 151:3996-4006
74. Nayak A, Dodagatta-Marri E, Tsolaki AG, Kishore U 2012 An insight into the diverse roles of surfactant proteins, SP-A and SP-D in innate and adaptive immunity. Front Immunol 3:131
75. Harju K, Glumoff V, Hallman M 2001 Ontogeny of Toll-like receptors Tlr2 and Tlr4 in mice. Pediatr Res 49:81-83 (Pubitemid 32015004)
76. Bry K, Lappalainen U 2001 Intra-amniotic endotoxin accelerates lung maturation in fetal rabbits. Acta Paediatr 90:74-80 (Pubitemid 32147231)
77. Bry K, Lappalainen U, Hallman M 1997 Intraamniotic interleukin- 1 accelerates surfactant protein synthesis in fetal rabbits and improves lung stability after premature birth. J Clin Invest 99:2992-2999 (Pubitemid 27278676)
78. Jobe AH, Newnham JP, Willet KE, Sly P, Ervin MG, Bachurski C, Possmayer F, Hallman M, Ikegami M 2000 Effects of antenatal endotoxin and glucocorticoids on the lungs of preterm lambs. Am J Obstet Gynecol 182:401-408 (Pubitemid 30127355)
79. Tsuda H, Takahashi Y, Iwagaki S, Kawabata I, Hayakawa H, Kotani T, Shibata K, Kikkawa F 2010 Intra-amniotic infection increases amniotic lamellar body count before 34 weeks of gestation. J Matern Fetal Neonatal Med 23:1230-1236
80. Chuang CY, Chen TG, Tai YT, Chen TL, Lin YH, Tsai CH, Chen RM 2011 Toll-like receptor 2-mediated sequential activation of MyD88 and MAPKs contributes to lipopolysaccharide-induced SP-A gene expression in human alveolar epithelial cells. Immunobiology 216:707-714
81. Döring B, Shynlova O, Tsui P, Eckardt D, Janssen-Bienhold U, Hofmann F, Feil S, Feil R, Lye SJ, Willecke K 2006 Ablation of connexin43 in uterine smooth muscle cells of the mouse causes delayed parturition. J Cell Sci 119:1715-1722 (Pubitemid 43810998)
82. Martin FJ, Prince AS 2008 TLR2 regulates gap junction intercellular communication in airway cells. J Immunol 180:4986-4993
83. Ey B, Eyking A, Gerken G, Podolsky DK, Cario E 2009 TLR2 mediates gap junctional intercellular communication through connexin- 43 in intestinal epithelial barrier injury. J Biol Chem 284: 22332-22343
84. Foley JP, Lam D, Jiang H, Liao J, Cheong N, McDevitt TM, Zaman A, Wright JR, Savani RC 2012 TLR2, TGFβ, hyaluronan and RHAMM are required for surfactant protein A-stimulated macrophage chemotaxis. J Biol Chem 287:37406-37419