DOI: 10.4049/jimmunol.0903867. Surfactant Protein-A as an Anti-Inflammatory Component in the Amnion: Implications for Human Pregnancy

Surfactant Protein-A as an Anti-Inflammatory Component in the Amnion: Implications for Human Pregnancy

10.4049/jimmunol.0903867

Crossref journal-article

Oxford University Press (OUP)

The Journal of Immunology (286)

Abstract

AbstractThe mechanism of mouse parturition is thought to involve myometrial infiltration by amniotic fluid (AF) macrophages, activated by surfactant protein-A (SP-A). In humans, the concentration of AF SP-A decreases during labor, and no fetal macrophages are found in the myometrium after labor. Therefore, it appears that the mechanisms of labor in mice and humans are different. We investigated a potential role for SP-A in human pregnancy and parturition by examining SP-A expression patterns in AF and amnion. High molecular mass (&gt;250 kDa) oligomeric SP-A was increased in AF with advancing gestation. Interestingly, these oligomers were more abundant in placental amnion before labor at term, while they increased primarily in reflected amnion during labor (p &lt; 0.05). Immunoblotting showed a binding of high molecular mass SP-A in AF to amnion. In C57BL/6 mice, oligomeric SP-A was also readily detected in AF from E15 onwards, but not in amnion. Macrophage density in mice myometrium did not change with advancing gestational age. Microarray analysis of human amnion explants incubated with SP-A revealed a molecular signature of inhibited cytokine–cytokine receptor interaction with downregulation of IL-1β, CXCL2, and CXCL5 mRNA expression. The findings in this study strongly suggest that SP-A signals amniotic anti-inflammatory response via AF during pregnancy. We propose that an SP-A interaction among AF, placental amnion, and reflected amnion is a unique mechanism for immunoregulation in human pregnancy akin to that established in lung biology. However, AF SP-A and fetal macrophages by themselves do not seem to be exclusive effectors of parturition in humans.

Bibliography

Lee, D.-C., Romero, R., Kim, C. J., Chaiworapongsa, T., Tarca, A. L., Lee, J., Suh, Y.-L., Mazaki-Tovi, S., Vaisbuch, E., Mittal, P., Draghici, S., Erez, O., Kusanovic, J. P., Hassan, S. S., & Kim, J.-S. (2010). Surfactant Protein-A as an Anti-Inflammatory Component in the Amnion: Implications for Human Pregnancy. The Journal of Immunology, 184(11), 6479â6491.

Authors 15

Deug-Chan Lee (first)
Roberto Romero (additional)
Chong Jai Kim (additional)
Tinnakorn Chaiworapongsa (additional)
Adi L. Tarca (additional)
JoonHo Lee (additional)
Yeon-Lim Suh (additional)
Shali Mazaki-Tovi (additional)
Edi Vaisbuch (additional)
Pooja Mittal (additional)
Sorin Draghici (additional)
Offer Erez (additional)
Juan Pedro Kusanovic (additional)
Sonia S. Hassan (additional)
Jung-Sun Kim (additional)

References 54 Referenced 32

10.1016/j.ajog.2005.08.057 / Am. J. Obstet. Gynecol. / Human spontaneous labor without histologic chorioamnionitis is characterized by an acute inflammation gene expression signature. by Haddad (2006)
10.1095/biolreprod.108.069260 / Biol. Reprod. / Region-specific gene expression profiling: novel evidence for biological heterogeneity of the human amnion. by Han (2008)
10.1016/S0002-9378(00)70501-1 / Am. J. Obstet. Gynecol. / Fetal membrane distention: determination of the intrauterine surface area and distention of the fetal membranes preterm and at term. by Millar (2000)
10.1093/molehr/gam086 / Mol. Hum. Reprod. / Prostaglandin H synthase-2 gene regulation in the amnion at labour: histone acetylation and nuclear factor kappa B binding to the promoter in vivo. by Mitchell (2008)
10.1016/0090-6980(89)90028-2 / Prostaglandins / Interleukin-1 stimulates prostaglandin biosynthesis by human amnion. by Romero (1989)
10.1016/S0090-6980(97)00144-5 / Prostaglandins / Tumor necrosis factor-alpha promotes sustained cyclooxygenase-2 expression: attenuation by dexamethasone and NSAIDs. by Perkins (1997)
10.1002/jcp.1041530107 / J. Cell. Physiol. / Amnion cell biosynthesis of interleukin-8: regulation by inflammatory cytokines. by Trautman (1992)
10.1016/j.jri.2008.04.002 / J. Reprod. Immunol. / Inflammatory processes in preterm and term parturition. by Christiaens (2008)
{'key': '2023010202372280800_r9', 'first-page': 'L354', 'article-title': 'Characterization of mRNA transcripts and organization of human SP-A1 and SP-A2 genes.', 'volume': '266', 'author': 'McCormick', 'year': '1994', 'journal-title': 'Am. J. Physiol.'} / Am. J. Physiol. / Characterization of mRNA transcripts and organization of human SP-A1 and SP-A2 genes. by McCormick (1994)
{'key': '2023010202372280800_r10', 'first-page': 'L177', 'article-title': 'Differential regulation of SP-A1 and SP-A2 genes by cAMP, glucocorticoids, and insulin.', 'volume': '274', 'author': 'Kumar', 'year': '1998', 'journal-title': 'Am. J. Physiol.'} / Am. J. Physiol. / Differential regulation of SP-A1 and SP-A2 genes by cAMP, glucocorticoids, and insulin. by Kumar (1998)
10.1016/j.molimm.2005.08.004 / Mol. Immunol. / Surfactant proteins SP-A and SP-D: structure, function and receptors. by Kishore (2006)
10.1111/j.1462-5822.2007.00953.x / Cell. Microbiol. / Pulmonary collectins in innate immunity of the lung. by Kuroki (2007)
10.1165/rcmb.2002-0274OC / Am. J. Respir. Cell Mol. Biol. / Expression and localization of lung surfactant protein A in human tissues. by Madsen (2003)
10.1111/j.1365-2567.2004.01782.x / Immunology / Surfactant protein A, an innate immune factor, is expressed in the vaginal mucosa and is present in vaginal lavage fluid. by MacNeill (2004)
10.1210/jc.2006-1472 / J. Clin. Endocrinol. Metab. / Induction of surfactant protein A expression by cortisol facilitates prostaglandin synthesis in human chorionic trophoblasts. by Sun (2006)
10.1002/path.2131 / J. Pathol. / Surfactant protein-A mRNA expression by human fetal membranes is increased in histological chorioamnionitis but not in spontaneous labour at term. by Han (2007)
10.1203/00006450-199112000-00023 / Pediatr. Res. / Ontogeny of surfactant proteins A and B in human amniotic fluid as indices of fetal lung maturity. by Pryhuber (1991)
10.1016/0005-2760(94)90233-X / Biochim. Biophys. Acta / Surfactant proteins A (SP-A) and D (SP-D): levels in human amniotic fluid and localization in the fetal membranes. by Miyamura (1994)
10.1073/pnas.0401124101 / Proc. Natl. Acad. Sci. U.S.A. / Surfactant protein secreted by the maturing mouse fetal lung acts as a hormone that signals the initiation of parturition. by Condon (2004)
10.1016/j.jsbmb.2004.12.027 / J. Steroid Biochem. Mol. Biol. / New insights into the molecular endocrinology of parturition. by Mendelson (2005)
10.1016/j.ajog.2006.06.052 / Am. J. Obstet. Gynecol. / Fetal macrophages are not present in the myometrium of women with labor at term. by Kim (2006)
10.1177/1933719107309646 / Reprod. Sci. / Vascular and myometrial changes in the human uterus at term. by Leong (2008)
10.1080/14767050802215193 / J. Matern. Fetal Neonatal Med. / The concentration of surfactant protein-A in amniotic fluid decreases in spontaneous human parturition at term. by Chaiworapongsa (2008)
10.4049/jimmunol.171.1.417 / J. Immunol. / Direct binding of Toll-like receptor 2 to zymosan, and zymosan-induced NF-kappa B activation and TNF-alpha secretion are down-regulated by lung collectin surfactant protein A. by Sato (2003)
10.4049/jimmunol.168.12.5989 / J. Immunol. / Cutting edge: the immunostimulatory activity of the lung surfactant protein-A involves Toll-like receptor 4. by Guillot (2002)
10.1016/j.ajog.2004.07.009 / Am. J. Obstet. Gynecol. / Toll-like receptor-2 and -4 in the chorioamniotic membranes in spontaneous labor at term and in preterm parturition that are associated with chorioamnionitis. by Kim (2004)
10.1016/S0092-8674(03)00758-X / Cell / By binding SIRPalpha or calreticulin/CD91, lung collectins act as dual function surveillance molecules to suppress or enhance inflammation. by Gardai (2003)
10.1093/biostatistics/4.2.249 / Biostatistics / Exploration, normalization, and summaries of high density oligonucleotide array probe level data. by Irizarry (2003)
10.1007/0-387-29362-0_23 / Bioinformatics and Computational Biology Solutions using R and Bioconductor. / Limma: linear models for microarray data by Smyth (2005)
10.1111/j.2517-6161.1995.tb02031.x / J. R. Stat. Soc., B / Controlling the false discovery rate: a practical and powerful approach to multiple testing. by Benjamini (1995)
10.1007/978-3-7908-2656-2_13 / Compstat 2004 Proceedings in Computational Statistics. / Using GO for statistical analyses by Gentleman (2004)
10.1101/gr.6202607 / Genome Res. / A systems biology approach for pathway level analysis. by Draghici (2007)
10.1093/bioinformatics/btn577 / Bioinformatics / A novel signaling pathway impact analysis. by Tarca (2009)
10.1016/S0022-1759(98)00160-4 / J. Immunol. Methods / A novel method of purifying lung surfactant proteins A and D from the lung lavage of alveolar proteinosis patients and from pooled amniotic fluid. by Strong (1998)
10.1002/pmic.200390013 / Proteomics / Proteomic analysis of human bronchoalveolar lavage fluid: expression profiling of surfactant-associated protein A isomers derived from human pulmonary alveolar proteinosis using immunoaffinity detection. by He (2003)
10.1038/labinvest.3700749 / Lab. Invest. / Coexpression of myofibroblast and macrophage markers: novel evidence for an in vivo plasticity of chorioamniotic mesodermal cells of the human placenta. by Kim (2008)
10.1074/jbc.M410266200 / J. Biol. Chem. / Role of the degree of oligomerization in the structure and function of human surfactant protein A. by Sánchez-Barbero (2005)
{'key': '2023010202372280800_r38', 'first-page': '393', 'article-title': 'Macrophage populations in the human placenta and amniochorion.', 'volume': '57', 'author': 'Bulmer', 'year': '1984', 'journal-title': 'Clin. Exp. Immunol.'} / Clin. Exp. Immunol. / Macrophage populations in the human placenta and amniochorion. by Bulmer (1984)
10.1111/j.1749-6632.1998.tb10104.x / Ann. N. Y. Acad. Sci. / Formation of the placenta and extraembryonic membranes. by Cross (1998)
{'key': '2023010202372280800_r40', 'first-page': 'L546', 'article-title': 'Murine pulmonary surfactant SP-A gene: cloning, sequence, and transcriptional activity.', 'volume': '263', 'author': 'Korfhagen', 'year': '1992', 'journal-title': 'Am. J. Physiol.'} / Am. J. Physiol. / Murine pulmonary surfactant SP-A gene: cloning, sequence, and transcriptional activity. by Korfhagen (1992)
10.1378/chest.128.3.1611 / Chest / Association of polymorphisms in pulmonary surfactant protein A1 and A2 genes with high-altitude pulmonary edema. by Saxena (2005)
10.1016/S0925-4439(98)00075-1 / Biochim. Biophys. Acta / Surfactant protein A (SP-A) gene targeted mice. by Korfhagen (1998)
10.1152/ajplung.00125.2002 / Am. J. Physiol. Lung Cell. Mol. Physiol. / Surfactant protein A differentially regulates peripheral and inflammatory neutrophil chemotaxis. by Schagat (2003)
10.1164/ajrccm.163.1.2005084 / Am. J. Respir. Crit. Care Med. / Surfactant protein A recruits neutrophils into the lungs of ventilated preterm lambs. by Kramer (2001)
10.1093/ajcp/87.1.37 / Am. J. Clin. Pathol. / Immunocytochemical characterization of amniotic fluid macrophages in cases of fetal neural tube defects. by Polgar (1987)
10.1111/j.1600-0897.1988.tb00240.x / Am. J. Reprod. Immunol. Microbiol. / Neutral-red uptake and expression of monocytic antigens in amniotic-fluid mononuclear phagocytes: evaluation of a novel approach for prenatal diagnosis of neural-tube defects. by Polgár (1988)
10.1093/humrep/14.1.229 / Hum. Reprod. / Leukocytes infiltrate the myometrium during human parturition: further evidence that labour is an inflammatory process. by Thomson (1999)
10.4049/jimmunol.181.2.1470 / J. Immunol. / Monocyte chemoattractant protein-1 (CCL-2) integrates mechanical and endocrine signals that mediate term and preterm labor. by Shynlova (2008)
10.1095/biolreprod61.4.879 / Biol. Reprod. / Macrophage trafficking in the uterus and cervix precedes parturition in the mouse. by Mackler (1999)
10.4049/jimmunol.165.7.3934 / J. Immunol. / Distinct effects of surfactant protein A or D deficiency during bacterial infection on the lung. by LeVine (2000)
10.1152/ajplung.00427.2002 / Am. J. Physiol. Lung Cell. Mol. Physiol. / Surfactant protein A inhibits alveolar macrophage cytokine production by CD14-independent pathway. by Alcorn (2004)
10.4049/jimmunol.172.11.6866 / J. Immunol. / Pulmonary surfactant protein a inhibits macrophage reactive oxygen intermediate production in response to stimuli by reducing NADPH oxidase activity. by Crowther (2004)
10.4049/jimmunol.180.12.7847 / J. Immunol. / Pulmonary surfactant protein A regulates TLR expression and activity in human macrophages. by Henning (2008)
10.1002/(SICI)1097-4652(199903)178:3<379::AID-JCP12>3.0.CO;2-C / J. Cell. Physiol. / SP-A as a cytokine: surfactant protein-A-regulated transcription of surfactant proteins and other genes. by Korutla (1999)

Dates

Type	When
Created	15 years, 3 months ago (May 3, 2010, 10:37 p.m.)
Deposited	6 months ago (Feb. 20, 2025, 9:17 a.m.)
Indexed	5 months ago (March 22, 2025, 5:20 a.m.)
Issued	15 years, 2 months ago (June 1, 2010)
Published	15 years, 2 months ago (June 1, 2010)
Published Online	15 years, 2 months ago (June 1, 2010)
Published Print	15 years, 2 months ago (June 1, 2010)

Funders 0

None

BibTeX

@article{Lee_2010, title={Surfactant Protein-A as an Anti-Inflammatory Component in the Amnion: Implications for Human Pregnancy}, volume={184}, ISSN={1550-6606}, url={http://dx.doi.org/10.4049/jimmunol.0903867}, DOI={10.4049/jimmunol.0903867}, number={11}, journal={The Journal of Immunology}, publisher={Oxford University Press (OUP)}, author={Lee, Deug-Chan and Romero, Roberto and Kim, Chong Jai and Chaiworapongsa, Tinnakorn and Tarca, Adi L. and Lee, JoonHo and Suh, Yeon-Lim and Mazaki-Tovi, Shali and Vaisbuch, Edi and Mittal, Pooja and Draghici, Sorin and Erez, Offer and Kusanovic, Juan Pedro and Hassan, Sonia S. and Kim, Jung-Sun}, year={2010}, month=jun, pages={6479–6491} }

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      "volume": "195",
      "author": "Haddad",
      "year": "2006",
      "journal-title": "Am. J. Obstet. Gynecol."
    },
    {
      "key": "2023010202372280800_r2",
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      "first-page": "954",
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      "article-title": "Region-specific gene expression profiling: novel evidence for biological heterogeneity of the human amnion.",
      "volume": "79",
      "author": "Han",
      "year": "2008",
      "journal-title": "Biol. Reprod."
    },
    {
      "key": "2023010202372280800_r3",
      "doi-asserted-by": "crossref",
      "first-page": "128",
      "DOI": "10.1016/S0002-9378(00)70501-1",
      "article-title": "Fetal membrane distention: determination of the intrauterine surface area and distention of the fetal membranes preterm and at term.",
      "volume": "182",
      "author": "Millar",
      "year": "2000",
      "journal-title": "Am. J. Obstet. Gynecol."
    },
    {
      "key": "2023010202372280800_r4",
      "doi-asserted-by": "crossref",
      "first-page": "53",
      "DOI": "10.1093/molehr/gam086",
      "article-title": "Prostaglandin H synthase-2 gene regulation in the amnion at labour: histone acetylation and nuclear factor kappa B binding to the promoter in vivo.",
      "volume": "14",
      "author": "Mitchell",
      "year": "2008",
      "journal-title": "Mol. Hum. Reprod."
    },
    {
      "key": "2023010202372280800_r5",
      "doi-asserted-by": "crossref",
      "first-page": "13",
      "DOI": "10.1016/0090-6980(89)90028-2",
      "article-title": "Interleukin-1 stimulates prostaglandin biosynthesis by human amnion.",
      "volume": "37",
      "author": "Romero",
      "year": "1989",
      "journal-title": "Prostaglandins"
    },
    {
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      "doi-asserted-by": "crossref",
      "first-page": "727",
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      "volume": "54",
      "author": "Perkins",
      "year": "1997",
      "journal-title": "Prostaglandins"
    },
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      "DOI": "10.1002/jcp.1041530107",
      "article-title": "Amnion cell biosynthesis of interleukin-8: regulation by inflammatory cytokines.",
      "volume": "153",
      "author": "Trautman",
      "year": "1992",
      "journal-title": "J. Cell. Physiol."
    },
    {
      "key": "2023010202372280800_r8",
      "doi-asserted-by": "crossref",
      "first-page": "50",
      "DOI": "10.1016/j.jri.2008.04.002",
      "article-title": "Inflammatory processes in preterm and term parturition.",
      "volume": "79",
      "author": "Christiaens",
      "year": "2008",
      "journal-title": "J. Reprod. Immunol."
    },
    {
      "key": "2023010202372280800_r9",
      "first-page": "L354",
      "article-title": "Characterization of mRNA transcripts and organization of human SP-A1 and SP-A2 genes.",
      "volume": "266",
      "author": "McCormick",
      "year": "1994",
      "journal-title": "Am. J. Physiol."
    },
    {
      "key": "2023010202372280800_r10",
      "first-page": "L177",
      "article-title": "Differential regulation of SP-A1 and SP-A2 genes by cAMP, glucocorticoids, and insulin.",
      "volume": "274",
      "author": "Kumar",
      "year": "1998",
      "journal-title": "Am. J. Physiol."
    },
    {
      "key": "2023010202372280800_r11",
      "doi-asserted-by": "crossref",
      "first-page": "1293",
      "DOI": "10.1016/j.molimm.2005.08.004",
      "article-title": "Surfactant proteins SP-A and SP-D: structure, function and receptors.",
      "volume": "43",
      "author": "Kishore",
      "year": "2006",
      "journal-title": "Mol. Immunol."
    },
    {
      "key": "2023010202372280800_r12",
      "doi-asserted-by": "crossref",
      "first-page": "1871",
      "DOI": "10.1111/j.1462-5822.2007.00953.x",
      "article-title": "Pulmonary collectins in innate immunity of the lung.",
      "volume": "9",
      "author": "Kuroki",
      "year": "2007",
      "journal-title": "Cell. Microbiol."
    },
    {
      "key": "2023010202372280800_r13",
      "doi-asserted-by": "crossref",
      "first-page": "591",
      "DOI": "10.1165/rcmb.2002-0274OC",
      "article-title": "Expression and localization of lung surfactant protein A in human tissues.",
      "volume": "29",
      "author": "Madsen",
      "year": "2003",
      "journal-title": "Am. J. Respir. Cell Mol. Biol."
    },
    {
      "key": "2023010202372280800_r14",
      "doi-asserted-by": "crossref",
      "first-page": "91",
      "DOI": "10.1111/j.1365-2567.2004.01782.x",
      "article-title": "Surfactant protein A, an innate immune factor, is expressed in the vaginal mucosa and is present in vaginal lavage fluid.",
      "volume": "111",
      "author": "MacNeill",
      "year": "2004",
      "journal-title": "Immunology"
    },
    {
      "key": "2023010202372280800_r15",
      "doi-asserted-by": "crossref",
      "first-page": "4988",
      "DOI": "10.1210/jc.2006-1472",
      "article-title": "Induction of surfactant protein A expression by cortisol facilitates prostaglandin synthesis in human chorionic trophoblasts.",
      "volume": "91",
      "author": "Sun",
      "year": "2006",
      "journal-title": "J. Clin. Endocrinol. Metab."
    },
    {
      "key": "2023010202372280800_r16",
      "doi-asserted-by": "crossref",
      "first-page": "489",
      "DOI": "10.1002/path.2131",
      "article-title": "Surfactant protein-A mRNA expression by human fetal membranes is increased in histological chorioamnionitis but not in spontaneous labour at term.",
      "volume": "211",
      "author": "Han",
      "year": "2007",
      "journal-title": "J. Pathol."
    },
    {
      "key": "2023010202372280800_r17",
      "doi-asserted-by": "crossref",
      "first-page": "597",
      "DOI": "10.1203/00006450-199112000-00023",
      "article-title": "Ontogeny of surfactant proteins A and B in human amniotic fluid as indices of fetal lung maturity.",
      "volume": "30",
      "author": "Pryhuber",
      "year": "1991",
      "journal-title": "Pediatr. Res."
    },
    {
      "key": "2023010202372280800_r18",
      "doi-asserted-by": "crossref",
      "first-page": "303",
      "DOI": "10.1016/0005-2760(94)90233-X",
      "article-title": "Surfactant proteins A (SP-A) and D (SP-D): levels in human amniotic fluid and localization in the fetal membranes.",
      "volume": "1210",
      "author": "Miyamura",
      "year": "1994",
      "journal-title": "Biochim. Biophys. Acta"
    },
    {
      "key": "2023010202372280800_r19",
      "doi-asserted-by": "crossref",
      "first-page": "4978",
      "DOI": "10.1073/pnas.0401124101",
      "article-title": "Surfactant protein secreted by the maturing mouse fetal lung acts as a hormone that signals the initiation of parturition.",
      "volume": "101",
      "author": "Condon",
      "year": "2004",
      "journal-title": "Proc. Natl. Acad. Sci. U.S.A."
    },
    {
      "key": "2023010202372280800_r20",
      "doi-asserted-by": "crossref",
      "first-page": "113",
      "DOI": "10.1016/j.jsbmb.2004.12.027",
      "article-title": "New insights into the molecular endocrinology of parturition.",
      "volume": "93",
      "author": "Mendelson",
      "year": "2005",
      "journal-title": "J. Steroid Biochem. Mol. Biol."
    },
    {
      "key": "2023010202372280800_r21",
      "doi-asserted-by": "crossref",
      "first-page": "829",
      "DOI": "10.1016/j.ajog.2006.06.052",
      "article-title": "Fetal macrophages are not present in the myometrium of women with labor at term.",
      "volume": "195",
      "author": "Kim",
      "year": "2006",
      "journal-title": "Am. J. Obstet. Gynecol."
    },
    {
      "key": "2023010202372280800_r22",
      "doi-asserted-by": "crossref",
      "first-page": "59",
      "DOI": "10.1177/1933719107309646",
      "article-title": "Vascular and myometrial changes in the human uterus at term.",
      "volume": "15",
      "author": "Leong",
      "year": "2008",
      "journal-title": "Reprod. Sci."
    },
    {
      "key": "2023010202372280800_r23",
      "doi-asserted-by": "crossref",
      "first-page": "652",
      "DOI": "10.1080/14767050802215193",
      "article-title": "The concentration of surfactant protein-A in amniotic fluid decreases in spontaneous human parturition at term.",
      "volume": "21",
      "author": "Chaiworapongsa",
      "year": "2008",
      "journal-title": "J. Matern. Fetal Neonatal Med."
    },
    {
      "key": "2023010202372280800_r24",
      "doi-asserted-by": "crossref",
      "first-page": "417",
      "DOI": "10.4049/jimmunol.171.1.417",
      "article-title": "Direct binding of Toll-like receptor 2 to zymosan, and zymosan-induced NF-kappa B activation and TNF-alpha secretion are down-regulated by lung collectin surfactant protein A.",
      "volume": "171",
      "author": "Sato",
      "year": "2003",
      "journal-title": "J. Immunol."
    },
    {
      "key": "2023010202372280800_r25",
      "doi-asserted-by": "crossref",
      "first-page": "5989",
      "DOI": "10.4049/jimmunol.168.12.5989",
      "article-title": "Cutting edge: the immunostimulatory activity of the lung surfactant protein-A involves Toll-like receptor 4.",
      "volume": "168",
      "author": "Guillot",
      "year": "2002",
      "journal-title": "J. Immunol."
    },
    {
      "key": "2023010202372280800_r26",
      "doi-asserted-by": "crossref",
      "first-page": "1346",
      "DOI": "10.1016/j.ajog.2004.07.009",
      "article-title": "Toll-like receptor-2 and -4 in the chorioamniotic membranes in spontaneous labor at term and in preterm parturition that are associated with chorioamnionitis.",
      "volume": "191",
      "author": "Kim",
      "year": "2004",
      "journal-title": "Am. J. Obstet. Gynecol."
    },
    {
      "key": "2023010202372280800_r27",
      "doi-asserted-by": "crossref",
      "first-page": "13",
      "DOI": "10.1016/S0092-8674(03)00758-X",
      "article-title": "By binding SIRPalpha or calreticulin/CD91, lung collectins act as dual function surveillance molecules to suppress or enhance inflammation.",
      "volume": "115",
      "author": "Gardai",
      "year": "2003",
      "journal-title": "Cell"
    },
    {
      "key": "2023010202372280800_r28",
      "doi-asserted-by": "crossref",
      "first-page": "249",
      "DOI": "10.1093/biostatistics/4.2.249",
      "article-title": "Exploration, normalization, and summaries of high density oligonucleotide array probe level data.",
      "volume": "4",
      "author": "Irizarry",
      "year": "2003",
      "journal-title": "Biostatistics"
    },
    {
      "key": "2023010202372280800_r29",
      "doi-asserted-by": "crossref",
      "first-page": "397",
      "DOI": "10.1007/0-387-29362-0_23",
      "article-title": "Limma: linear models for microarray data",
      "volume-title": "Bioinformatics and Computational Biology Solutions using R and Bioconductor.",
      "author": "Smyth",
      "year": "2005"
    },
    {
      "key": "2023010202372280800_r30",
      "doi-asserted-by": "crossref",
      "first-page": "289",
      "DOI": "10.1111/j.2517-6161.1995.tb02031.x",
      "article-title": "Controlling the false discovery rate: a practical and powerful approach to multiple testing.",
      "volume": "57",
      "author": "Benjamini",
      "year": "1995",
      "journal-title": "J. R. Stat. Soc., B"
    },
    {
      "key": "2023010202372280800_r31",
      "doi-asserted-by": "crossref",
      "first-page": "171",
      "DOI": "10.1007/978-3-7908-2656-2_13",
      "article-title": "Using GO for statistical analyses",
      "volume-title": "Compstat 2004 Proceedings in Computational Statistics.",
      "author": "Gentleman",
      "year": "2004"
    },
    {
      "key": "2023010202372280800_r32",
      "doi-asserted-by": "crossref",
      "first-page": "1537",
      "DOI": "10.1101/gr.6202607",
      "article-title": "A systems biology approach for pathway level analysis.",
      "volume": "17",
      "author": "Draghici",
      "year": "2007",
      "journal-title": "Genome Res."
    },
    {
      "key": "2023010202372280800_r33",
      "doi-asserted-by": "crossref",
      "first-page": "75",
      "DOI": "10.1093/bioinformatics/btn577",
      "article-title": "A novel signaling pathway impact analysis.",
      "volume": "25",
      "author": "Tarca",
      "year": "2009",
      "journal-title": "Bioinformatics"
    },
    {
      "key": "2023010202372280800_r34",
      "doi-asserted-by": "crossref",
      "first-page": "139",
      "DOI": "10.1016/S0022-1759(98)00160-4",
      "article-title": "A novel method of purifying lung surfactant proteins A and D from the lung lavage of alveolar proteinosis patients and from pooled amniotic fluid.",
      "volume": "220",
      "author": "Strong",
      "year": "1998",
      "journal-title": "J. Immunol. Methods"
    },
    {
      "key": "2023010202372280800_r35",
      "doi-asserted-by": "crossref",
      "first-page": "87",
      "DOI": "10.1002/pmic.200390013",
      "article-title": "Proteomic analysis of human bronchoalveolar lavage fluid: expression profiling of surfactant-associated protein A isomers derived from human pulmonary alveolar proteinosis using immunoaffinity detection.",
      "volume": "3",
      "author": "He",
      "year": "2003",
      "journal-title": "Proteomics"
    },
    {
      "key": "2023010202372280800_r36",
      "doi-asserted-by": "crossref",
      "first-page": "365",
      "DOI": "10.1038/labinvest.3700749",
      "article-title": "Coexpression of myofibroblast and macrophage markers: novel evidence for an in vivo plasticity of chorioamniotic mesodermal cells of the human placenta.",
      "volume": "88",
      "author": "Kim",
      "year": "2008",
      "journal-title": "Lab. Invest."
    },
    {
      "key": "2023010202372280800_r37",
      "doi-asserted-by": "crossref",
      "first-page": "7659",
      "DOI": "10.1074/jbc.M410266200",
      "article-title": "Role of the degree of oligomerization in the structure and function of human surfactant protein A.",
      "volume": "280",
      "author": "S\u00e1nchez-Barbero",
      "year": "2005",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023010202372280800_r38",
      "first-page": "393",
      "article-title": "Macrophage populations in the human placenta and amniochorion.",
      "volume": "57",
      "author": "Bulmer",
      "year": "1984",
      "journal-title": "Clin. Exp. Immunol."
    },
    {
      "key": "2023010202372280800_r39",
      "doi-asserted-by": "crossref",
      "first-page": "23",
      "DOI": "10.1111/j.1749-6632.1998.tb10104.x",
      "article-title": "Formation of the placenta and extraembryonic membranes.",
      "volume": "857",
      "author": "Cross",
      "year": "1998",
      "journal-title": "Ann. N. Y. Acad. Sci."
    },
    {
      "key": "2023010202372280800_r40",
      "first-page": "L546",
      "article-title": "Murine pulmonary surfactant SP-A gene: cloning, sequence, and transcriptional activity.",
      "volume": "263",
      "author": "Korfhagen",
      "year": "1992",
      "journal-title": "Am. J. Physiol."
    },
    {
      "key": "2023010202372280800_r41",
      "doi-asserted-by": "crossref",
      "first-page": "1611",
      "DOI": "10.1378/chest.128.3.1611",
      "article-title": "Association of polymorphisms in pulmonary surfactant protein A1 and A2 genes with high-altitude pulmonary edema.",
      "volume": "128",
      "author": "Saxena",
      "year": "2005",
      "journal-title": "Chest"
    },
    {
      "key": "2023010202372280800_r42",
      "doi-asserted-by": "crossref",
      "first-page": "296",
      "DOI": "10.1016/S0925-4439(98)00075-1",
      "article-title": "Surfactant protein A (SP-A) gene targeted mice.",
      "volume": "1408",
      "author": "Korfhagen",
      "year": "1998",
      "journal-title": "Biochim. Biophys. Acta"
    },
    {
      "key": "2023010202372280800_r43",
      "doi-asserted-by": "crossref",
      "first-page": "L140",
      "DOI": "10.1152/ajplung.00125.2002",
      "article-title": "Surfactant protein A differentially regulates peripheral and inflammatory neutrophil chemotaxis.",
      "volume": "284",
      "author": "Schagat",
      "year": "2003",
      "journal-title": "Am. J. Physiol. Lung Cell. Mol. Physiol."
    },
    {
      "key": "2023010202372280800_r44",
      "doi-asserted-by": "crossref",
      "first-page": "158",
      "DOI": "10.1164/ajrccm.163.1.2005084",
      "article-title": "Surfactant protein A recruits neutrophils into the lungs of ventilated preterm lambs.",
      "volume": "163",
      "author": "Kramer",
      "year": "2001",
      "journal-title": "Am. J. Respir. Crit. Care Med."
    },
    {
      "key": "2023010202372280800_r45",
      "doi-asserted-by": "crossref",
      "first-page": "37",
      "DOI": "10.1093/ajcp/87.1.37",
      "article-title": "Immunocytochemical characterization of amniotic fluid macrophages in cases of fetal neural tube defects.",
      "volume": "87",
      "author": "Polgar",
      "year": "1987",
      "journal-title": "Am. J. Clin. Pathol."
    },
    {
      "key": "2023010202372280800_r46",
      "doi-asserted-by": "crossref",
      "first-page": "81",
      "DOI": "10.1111/j.1600-0897.1988.tb00240.x",
      "article-title": "Neutral-red uptake and expression of monocytic antigens in amniotic-fluid mononuclear phagocytes: evaluation of a novel approach for prenatal diagnosis of neural-tube defects.",
      "volume": "18",
      "author": "Polg\u00e1r",
      "year": "1988",
      "journal-title": "Am. J. Reprod. Immunol. Microbiol."
    },
    {
      "key": "2023010202372280800_r47",
      "doi-asserted-by": "crossref",
      "first-page": "229",
      "DOI": "10.1093/humrep/14.1.229",
      "article-title": "Leukocytes infiltrate the myometrium during human parturition: further evidence that labour is an inflammatory process.",
      "volume": "14",
      "author": "Thomson",
      "year": "1999",
      "journal-title": "Hum. Reprod."
    },
    {
      "key": "2023010202372280800_r48",
      "doi-asserted-by": "crossref",
      "first-page": "1470",
      "DOI": "10.4049/jimmunol.181.2.1470",
      "article-title": "Monocyte chemoattractant protein-1 (CCL-2) integrates mechanical and endocrine signals that mediate term and preterm labor.",
      "volume": "181",
      "author": "Shynlova",
      "year": "2008",
      "journal-title": "J. Immunol."
    },
    {
      "key": "2023010202372280800_r49",
      "doi-asserted-by": "crossref",
      "first-page": "879",
      "DOI": "10.1095/biolreprod61.4.879",
      "article-title": "Macrophage trafficking in the uterus and cervix precedes parturition in the mouse.",
      "volume": "61",
      "author": "Mackler",
      "year": "1999",
      "journal-title": "Biol. Reprod."
    },
    {
      "key": "2023010202372280800_r50",
      "doi-asserted-by": "crossref",
      "first-page": "3934",
      "DOI": "10.4049/jimmunol.165.7.3934",
      "article-title": "Distinct effects of surfactant protein A or D deficiency during bacterial infection on the lung.",
      "volume": "165",
      "author": "LeVine",
      "year": "2000",
      "journal-title": "J. Immunol."
    },
    {
      "key": "2023010202372280800_r51",
      "doi-asserted-by": "crossref",
      "first-page": "L129",
      "DOI": "10.1152/ajplung.00427.2002",
      "article-title": "Surfactant protein A inhibits alveolar macrophage cytokine production by CD14-independent pathway.",
      "volume": "286",
      "author": "Alcorn",
      "year": "2004",
      "journal-title": "Am. J. Physiol. Lung Cell. Mol. Physiol."
    },
    {
      "key": "2023010202372280800_r52",
      "doi-asserted-by": "crossref",
      "first-page": "6866",
      "DOI": "10.4049/jimmunol.172.11.6866",
      "article-title": "Pulmonary surfactant protein a inhibits macrophage reactive oxygen intermediate production in response to stimuli by reducing NADPH oxidase activity.",
      "volume": "172",
      "author": "Crowther",
      "year": "2004",
      "journal-title": "J. Immunol."
    },
    {
      "key": "2023010202372280800_r53",
      "doi-asserted-by": "crossref",
      "first-page": "7847",
      "DOI": "10.4049/jimmunol.180.12.7847",
      "article-title": "Pulmonary surfactant protein A regulates TLR expression and activity in human macrophages.",
      "volume": "180",
      "author": "Henning",
      "year": "2008",
      "journal-title": "J. Immunol."
    },
    {
      "key": "2023010202372280800_r54",
      "doi-asserted-by": "crossref",
      "first-page": "379",
      "DOI": "10.1002/(SICI)1097-4652(199903)178:3<379::AID-JCP12>3.0.CO;2-C",
      "article-title": "SP-A as a cytokine: surfactant protein-A-regulated transcription of surfactant proteins and other genes.",
      "volume": "178",
      "author": "Korutla",
      "year": "1999",
      "journal-title": "J. Cell. Physiol."
    }
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