Placental Regulation of Inflammation and Hypoxia after TNF-α Infusion in Mice

American Journal of Reproductive Immunology

Volumn 74, Issue 5, 2015, Pages 407-418

  Bobek, Gabriele ^a   Surmon, Laura ^a   Mirabito, Katrina M ^b   Makris, Angela ^a,c,d   Hennessy, Annemarie ^a,c  

^a UNIVERSITY OF WESTERN SYDNEY   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c UNIVERSITY OF SYDNEY   (Australia)

^d LIVERPOOL HOSPITAL   (Australia)

Author keywords

Cytokines; HIF 1; Mouse; Placenta; Pre eclampsia; Toll like receptor

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; PROTEIN TYROSINE KINASE; SODIUM CHLORIDE; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN RECEPTOR 1; FLT1 PROTEIN, MOUSE; HIF1A PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HYPOXIA; IMMUNOREGULATION; INFLAMMATION; MATERNAL HYPERTENSION; MEAN ARTERIAL PRESSURE; MOUSE; NONHUMAN; PLACENTA; PLACENTA DEVELOPMENT; PREECLAMPSIA; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEINURIA; UPREGULATION; ANIMAL; ANOXIA; BLOOD; DISEASE MODEL; DRUG EFFECTS; HYPERTENSION; METABOLISM; PATHOLOGY; PREGNANCY;

ANIMALS; ANOXIA; DISEASE MODELS, ANIMAL; FEMALE; HYPERTENSION; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INFLAMMATION; MICE; PLACENTA; PRE-ECLAMPSIA; PREGNANCY; TOLL-LIKE RECEPTOR 3; TOLL-LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR-ALPHA; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1;

EID: 84944172972     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/aji.12417     Document Type: Article

References (69)

1. Kanasaki K, Kalluri R: The biology of preeclampsia. Kidney Int 2009; 76:831-837.
2. Redman CW, Sargent IL: Placental stress and pre-eclampsia: a revised view. Placenta 2009; 30(Suppl A):S38-S42.
3. Maynard SE, Min JY, Merchan J, Lim KH, Li J, Mondal S, Libermann TA, Morgan JP, Sellke FW, Stillman IE, Epstein FH, Sukhatme VP, Karumanchi SA: Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest 2003; 111:649-658.
4. LaMarca B: Endothelial dysfunction. An important mediator in the pathophysiology of hypertension during pre-eclampsia. Minerva Ginecol 2012; 64:309-320.
5. Burton GJ, Yung HW, Cindrova-Davies T, Charnock-Jones DS: Placental endoplasmic reticulum stress and oxidative stress in the pathophysiology of unexplained intrauterine growth restriction and early onset preeclampsia. Placenta 2009; 30(Suppl A):S43-S48.
6. Roberts JM, Hubel CA: The two stage model of preeclampsia: variations on the theme. Placenta 2009; 30:32-37.
7. Huppertz B: Placental origins of preeclampsia: challenging the current hypothesis. Hypertension 2008; 51:970-975.
8. Saito S, Shiozaki A, Nakashima A, Sakai M, Sasaki Y: The role of the immune system in preeclampsia. Mol Aspects Med 2007; 28:192-209.
9. Ahn H, Park J, Gilman-Sachs A, Kwak-Kim J: Immunologic characteristics of preeclampsia, a comprehensive review. Am J Reprod Immunol 2011; 65:377-394.
10. Hsu P, Nanan RKH: Innate and adaptive immune interactions at the fetal-maternal interface in healthy human pregnancy and pre-eclampsia. Front Immunol 2014; 5:125.
11. Saito S, Sakai M, Sasaki Y, Nakashima A, Shiozaki A: Inadequate tolerance induction may induce pre-eclampsia. J Reprod Immunol 2007; 76:30-39.
12. Leber A, Teles A, Zenclussen AC: Regulatory T cells and their role in pregnancy. Am J Reprod Immunol 2010; 63:445-459.
13. Goldman-Wohl D, Yagel S: NK cells and pre-eclampsia. Reprod Biomed online 2008; 16:227-231.
14. Chakraborty D, Rumi MAK, Soares MJ: NK cells, hypoxia and trophoblast cell differentiation. Cell Cycle 2012; 11:2427-2430.
15. Sargent IL, Borzychowski AM, Redman CW: Immunoregulation in normal pregnancy and pre-eclampsia: an overview. Reprod Biomed online 2006; 13:680-686.
16. Schiff E, Friedman SA, Baumann P, Sibai BM, Romero R: Tumor necrosis factor-alpha in pregnancies associated with preeclampsia or small-for-gestational-age newborns. Am J Obstet Gynecol 1994; 170:1224-1229.
17. Wang Y, Walsh SW: TNF alpha concentrations and mRNA expression are increased in preeclamptic placentas. J Reprod Immunol 1996; 32:157-169.
18. Hennessy A, Pilmore HL, Simmons LA, Painter DM: A deficiency of placental IL-10 in preeclampsia. J Immunol 1999; 163:3491-3495.
19. Chatterjee P, Weaver LE, Doersch KM, Kopriva SE, Chiasson VL, Allen SJ, Narayanan AM, Young KJ, Jones KA, Kuehl TJ, Mitchell BM: Placental toll-like receptor 3 and toll-like receptor 7/8 activation contributes to preeclampsia in humans and mice. PLoS ONE 2012; 7:e41884.
20. Sado T, Naruse K, Noguchi T, Haruta S, Yoshida S, Tanase Y, Kitanaka T, Oi H, Kobayashi H: Inflammatory pattern recognition receptors and their ligands: Factors contributing to the pathogenesis of preeclampsia. Inflamm Res 2011; 60:509-520.
21. Koga K, Izumi G, Mor G, Fujii T, Osuga Y: Toll-like receptors at the maternal-fetal interface in normal pregnancy and pregnancy complications. Am J Reprod Immunol 2014; 72:192-205.
22. Kim YM, Romero R, Oh SY, Kim CJ, Kilburn BA, Armant DR, Nien JK, Gomez R, Mazor M, Saito S, Abrahams VM, Mor G: Toll-like receptor 4: a potential link between "danger signals", the innate immune system, and preeclampsia? Am J Obstet Gynecol 2005; 193:921-927.
23. Pineda A, Verdin-Terán SL, Camacho A, Moreno-Fierros L: Expression of toll-like receptor TLR-2, TLR-3, TLR-4 and TLR-9 is increased in placentas from patients with preeclampsia. Arch Med Res 2011; 42:382-391.
24. Mathis D, Shoelson SE: Immunometabolism: an emerging frontier. Nat Rev Immunol 2011; 11:81.
25. Shapiro H, Lutaty A, Ariel A: Macrophages, meta-inflammation, and immuno-metabolism. ScientificWorldJournal 2011; 11:2509-2529.
26. Nizet V, Johnson RS: Interdependence of hypoxic and innate immune responses. Nat Rev Immunol 2009; 9:609-617.
27. Sharma S, Norris WE, Kalkunte S: Beyond the threshold: an etiological bridge between hypoxia and immunity in preeclampsia. J Reprod Immunol 2010; 85:112-116.
28. Rodesch F, Simon P, Donner C, Jauniaux E: Oxygen measurements in endometrial and trophoblastic tissues during early pregnancy. Obstet Gynecol 1992; 80:283-285.
29. Jauniaux E, Watson AL, Hempstock J, Bao YP, Skepper JN, Burton GJ: Onset of maternal arterial blood flow and placental oxidative stress. A possible factor in human early pregnancy failure. Am J Pathol 2000; 157:2111-2122.
30. Genbacev O, Zhou Y, Ludlow JW, Fisher SJ: Regulation of human placental development by oxygen tension. Science 1997; 277:1669-1672.
31. Semenza G: Signal transduction to hypoxia-inducible factor 1. Biochem Pharmacol 2002; 64:993-998.
32. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME, Wykoff CC, Pugh CW, Maher ER, Ratcliffe PJ: The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 1999; 399:271-275.
33. Pouysségur J, Dayan F, Mazure NM: Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 2006; 441:437-443.
34. Patel J, Landers K, Mortimer RH, Richard K: Regulation of hypoxia inducible factors (HIF) in hypoxia and normoxia during placental development. Placenta 2010; 31:951-957.
35. Caniggia I, Winter JL: Adriana and Luisa Castellucci Award Lecture 2001 Hypoxia Inducible Factor-1: oxygen regulation of trophoblast differentiation in normal and pre-eclamptic pregnancies - A review. Placenta 2002; 23:S47-S57.
36. Imtiyaz HZ, Simon MC: Hypoxia-inducible factors as essential regulators of inflammation. Curr Top Microbiol Immunol 2010; 345:105-120.
37. Tsapournioti S, Mylonis I, Hatziefthimiou A, Ioannou MG, Stamatiou R, Koukoulis GK, Simos G, Molyvdas PA, Paraskeva E: TNFalpha induces expression of HIF-1alpha mRNA and protein but inhibits hypoxic stimulation of HIF-1 transcriptional activity in airway smooth muscle cells. J Cell Physiol 2013; 228:1745-1753.
38. Zhou J, Callapina M, Goodall GJ, Brune B: Functional integrity of nuclear factor kappaB, phosphatidylinositol 3′-kinase, and mitogen-activated protein kinase signaling allows tumor necrosis factor alpha-evoked Bcl-2 expression to provoke internal ribosome entry site-dependent translation of hypoxia-inducible factor 1alpha. Cancer Res 2004; 64:9041-9048.
39. Frede S, Stockmann C, Freitag P, Fandrey J: Bacterial lipopolysaccharide induces HIF-1 activation in human monocytes via p44/42 MAPK and NF-kappaB. Biochem J 2006; 396:517-527.
40. Kim HY, Kim YH, Nam BH, Kong HJ, Kim HH, Kim YJ, An WG, Cheong J: HIF-1α expression in response to lipopolysaccaride mediates induction of hepatic inflammatory cytokine TNFα. Exp Cell Res 2007; 313:1866-1876.
41. Zenclussen AC, Fest S, Joachim R, Klapp BF, Arck PC: Introduction a mouse model for pre-eclampsia: adoptive transfer of activated Th1 cells leads to pre-eclampsia-like symptoms exclusively in pregnant mice. Eur J Immunol 2004; 34:377-387.
42. Sunderland NS, Thomson SE, Heffernan SJ, Lim S, Thompson J, Ogle R, McKenzie P, Kirwan PJ, Makris A, Hennessy A: Tumor necrosis factor α induces a model of preeclampsia in pregnant baboons (Papio hamadryas). Cytokine 2011; 56:192-199.
43. Alexander BT, Cockrell KL, Massey MB, Bennett WA, Granger JP: Tumor necrosis factor-alpha-induced hypertension in pregnant rats results in decreased renal neuronal nitric oxide synthase expression. Am J Hypertens 2002; 15:170-175.
44. Faas MM, Schuiling GA, Baller JF, Visscher CA, Bakker WW: A new animal model for human preeclampsia: ultra-low-dose endotoxin infusion in pregnant rats. Am J Obstet Gynecol 1994; 171:158-164.
45. Tinsley JH, Chiasson VL, Mahajan A, Young KJ, Mitchell BM: Toll-like receptor 3 activation during pregnancy elicits preeclampsia-like symptoms in rats. Am J Hypertens 2009; 22:1314-1319.
46. Chatterjee P, Chiasson VL, Kopriva SE, Young KJ, Chatterjee V, Jones KA, Mitchell BM: Interleukin 10 deficiency exacerbates toll-like receptor 3-induced preeclampsia-like symptoms in mice. Hypertension 2011; 58:489-496.
47. Huckle WR, Roche RI: Post-transcriptional control of expression of sFlt-1, an endogenous inhibitor of vascular endothelial growth factor. J Cell Biochem 2004; 93:120-132.
48. Chiu CL, Morgan CT, Lupton SJ, Lind JM: Parent of origin influences the cardiac expression of vascular endothelial growth factor (Vegfa). BMC Med Genet 2013; 14:43.
49. Surmon L, Bobek G, Chiu CL, Young S, Makris A, Lind JM, Hennessy A: The expression of placental soluble fms-like tyrosine kinase 1 in mouse placenta varies significantly across different litters from normal pregnant mice. Hypertens Pregnancy 2014; 33:371-374.
50. Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JA: Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 2007; 35:W71-W74.
51. Livak KJ, Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25:402-408.
52. Carpenter S, Ricci EP, Mercier BC, Moore MJ, Fitzgerald KA: Post-transcriptional regulation of gene expression in innate immunity. Nat Rev Immunol 2014; 14:361-376.
53. Schuetz P, Jones AE, Aird WC, Shapiro NI: Endothelial cell activation in emergency department patients with sepsis-related and non-sepsis-related hypotension. Shock 2011; 36:104-108.
54. Zamudio S, Kovalenko O, Echalar L, Torricos T, Al-Khan A, Alvarez M, Illsley NP: Evidence for extraplacental sources of circulating angiogenic growth effectors in human pregnancy. Placenta 2013; 34:1170-1176.
55. Levine RJ, Maynard SE, Qian C, Lim KH, England LJ, Yu KF, Schisterman EF, Thadhani R, Sachs BP, Epstein FH, Sibai BM, Sukhatme VP, Karumanchi SA: Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 2004; 350:672-683.
56. Makris A, Thornton C, Thompson J, Thomson S, Martin R, Ogle R, Waugh R, McKenzie P, Kirwan P, Hennessy A: Uteroplacental ischemia results in proteinuric hypertension and elevated sFLT-1. Kidney Int 2007; 71:977-984.
57. Zhou CC, Ahmad S, Mi T, Xia L, Abbasi S, Hewett PW, Sun C, Ahmed A, Kellems RE, Xia Y: Angiotensin II induces soluble fms-Like tyrosine kinase-1 release via calcineurin signaling pathway in pregnancy. Circ Res 2007; 100:88-95.
58. Nevo O, Soleymanlou N, Wu Y, Xu J, Kingdom J, Many A, Zamudio S, Caniggia I: Increased expression of sFlt-1 in in vivo and in vitro models of human placental hypoxia is mediated by HIF-1. Am J Physiol Regul Integr Comp Physiol 2006; 291:R1085-R1093.
59. Sumbayev VV, Nicholas SA: Hypoxia-inducible factor 1 as one of the "signaling drivers" of Toll-like receptor-dependent and allergic inflammation. Archivum immunologiae et therapiae experimentalis 2010; 58:287-294.
60. Wenger RH, Kvietikova I, Rolfs A, Gassmann M, Marti HH: Hypoxia-inducible factor-1 alpha is regulated at the post-mRNA level. Kidney Int 1997; 51:560-563.
61. Olmos G, Conde I, Arenas I, Del Peso L, Castellanos C, Landazuri MO, Lucio-Cazana J: Accumulation of hypoxia-inducible factor-1alpha through a novel electrophilic, thiol antioxidant-sensitive mechanism. Cell Signal 2007; 19:2098-2105.
62. Wiener CM, Booth G, Semenza GL: In vivo expression of mRNAs encoding hypoxia-inducible factor 1. Biochem Biophys Res Commun 1996; 225:485-488.
63. Lang KJD, Kappel A, Goodall GJ: Hypoxia-inducible factor-1α mRNA contains an internal ribosome entry site that allows efficient translation during normoxia and hypoxia. Mol Biol Cell 2002; 13:1792-1801.
64. Mortaz E, Redegeld FA, Nijkamp FP, Wong HR, Engels F: Acetylsalicylic acid-induced release of HSP70 from mast cells results in cell activation through TLR pathway. Exp Hematol 2006; 34:8-18.
65. Koga K, Aldo PB, Mor G: Toll-like receptors and pregnancy: trophoblast as modulators of the immune response. J Obstet Gynaecol Res 2009; 35:191-202.
66. Redman CW, Sargent IL, Staff AC: IFPA senior award lecture: making sense of pre-eclampsia - Two placental causes of preeclampsia? Placenta 2014; 35:S20-S25.
67. Huebener P, Schwabe RF: Regulation of wound healing and organ fibrosis by toll-like receptors. Biochim Biophys Acta 2013; 1832:1005-1017.
68. Tal R: The role of hypoxia and hypoxia-inducible factor-1Alpha in preeclampsia pathogenesis. Biol Reprod 2012; 87:134.
69. Young KC, Hussein SM, Dadiz R, deMello D, Devia C, Hehre D, Suguihara C: Toll-like receptor 4-deficient mice are resistant to chronic hypoxia-induced pulmonary hypertension. Exp Lung Res 2010; 36:111-119.