AGEs and HMGB1 Increase Inflammatory Cytokine Production from Human Placental Cells, Resulting in an Enhancement of Monocyte Migration

American Journal of Reproductive Immunology

Volumn 75, Issue 5, 2016, Pages 557-568

  Shirasuna, Koumei ^a   Seno, Kotomi ^a   Ohtsu, Ayaka ^a   Shiratsuki, Shogo ^a   Ohkuchi, Akihide ^b   Suzuki, Hirotada ^b   Matsubara, Shigeki ^b   Nagayama, Shiho ^b   Iwata, Hisataka ^a   Kuwayama, Takehito ^a  

^a TOKYO UNIVERSITY OF AGRICULTURE   (Japan)

^b JICHI MEDICAL UNIVERSITY   (Japan)

Author keywords

Advanced glycation end products; High mobility group box 1; Inflammation; Placenta

Indexed keywords

ADVANCED GLYCATION END PRODUCT; ADVANCED GLYCATION END PRODUCT RECEPTOR; HIGH MOBILITY GROUP B1 PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; INTERLEUKIN 8; MONOCYTE CHEMOTACTIC PROTEIN 1; REACTIVE OXYGEN METABOLITE; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; AUTACOID; HMGB1 PROTEIN, HUMAN; TLR4 PROTEIN, HUMAN;

ARTICLE; CELL INTERACTION; CELL MIGRATION; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; HUMAN CELL; HUMORAL IMMUNITY; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; MONOCYTE; PLACENTA DISORDER; PRIORITY JOURNAL; PROTEIN EXPRESSION; TROPHOBLAST; WESTERN BLOTTING; CELL COMMUNICATION; CELL LINE; CELL MOTION; COCULTURE; IMMUNOLOGY; INFLAMMATION; METABOLISM; PHYSIOLOGY; PREGNANCY;

CELL COMMUNICATION; CELL LINE; CELL MOVEMENT; CHEMOKINE CCL2; COCULTURE TECHNIQUES; FEMALE; GLYCOSYLATION END PRODUCTS, ADVANCED; HMGB1 PROTEIN; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; INTERLEUKIN-6; INTERLEUKIN-8; MONOCYTES; PREGNANCY; REACTIVE OXYGEN SPECIES; TOLL-LIKE RECEPTOR 4; TROPHOBLASTS;

EID: 84959874598     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/aji.12506     Document Type: Article

References (56)

1. Mol BW, Roberts CT, Thangaratinam S, Magee LA, de Groot CJ, Hofmeyr GJ: Pre-eclampsia. Lancet 2015; S0140:6736.
2. Redman CW, Sargent IL: Latest advances in understanding preeclampsia. Science 2005; 308:1592-1594.
3. Sacks G, Sargent I, Redman C: An innate view of human pregnancy. Immunol Today 1999; 20:114-118.
4. Faas MM, Spaans F, De Vos P: Monocytes and macrophages in pregnancy and pre-eclampsia. Front Immunol 2014; 5:298.
5. 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.
6. Venkatesha S, Toporsian M, Lam C, Hanai J, Mammoto T, Kim YM, Bdolah Y, Lim KH, Yuan HT, Libermann TA, Stillman IE, Roberts D, D'Amore PA, Epstein FH, Sellke FW, Romero R, Sukhatme VP, Letarte M, Karumanchi SA: Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med 2006; 12:642-649.
7. Sacks GP, Studena K, Sargent K, Redman CW: Normal pregnancy and preeclampsia both produce inflammatory changes in peripheral blood leukocytes akin to those of sepsis. Am J Obstet Gynecol 1998; 179:80-86.
8. Melgert BN, Spaans F, Borghuis T, Klok PA, Groen B, Bolt A, de Vos P, van Pampus MG, Wong TY, van Goor H, Bakker WW, Faas MM: Pregnancy and preeclampsia affect monocyte subsets in humans and rats. PLoS One 2012; 7:e45229.
9. Lau SY, Guild SJ, Barrett CJ, Chen Q, McCowan L, Jordan V, Chamley LW: Tumor necrosis factor-alpha, interleukin-6, and interleukin-10 levels are altered in preeclampsia: a systematic review and meta-analysis. Am J Reprod Immunol 2013; 70:412-427.
10. Mellembakken JR, Aukrust P, Hestdal K, Ueland T, Abyholm T, Videm V: Chemokines and leukocyte activation in the fetal circulation during preeclampsia. Hypertension 2001; 38:394-398.
11. Mor G, Cardenas I, Abrahams V, Guller S: Inflammation and pregnancy: the role of the immune system at the implantation site. Ann N Y Acad Sci 2011; 1221:80-87.
12. Laresgoiti-Servitje E: A leading role for the immune system in the pathophysiology of preeclampsia. J Leukoc Biol 2013; 94:247-257.
13. John WG, Lamb EJ: The Maillard or browning reaction in diabetes. Eye (Lond) 1993; 7(Pt 2):230-237.
14. Lotze MT, Tracey KJ: High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat Rev Immunol 2005; 5:331-342.
15. Chekir C, Nakatsuka M, Noguchi S, Konishi H, Kamada Y, Sasaki A, Hao L, Hiramatsu Y: Accumulation of advanced glycation end products in women with preeclampsia: possible involvement of placental oxidative and nitrative stress. Placenta 2006; 27:225-233.
16. Naruse K, Sado T, Noguchi T, Tsunemi T, Yoshida S, Akasaka J, Koike N, Oi H, Kobayashi H: Peripheral RAGE (receptor for advanced glycation endproducts)-ligands in normal pregnancy and preeclampsia: novel markers of inflammatory response. J Reprod Immunol 2012; 93:69-74.
17. Ibrahim ZA, Armour CL, Phipps S, Sukkar MB: RAGE and TLRs: relatives, friends or neighbours? Mol Immunol 2013; 56:739-744.
18. 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.
19. Wang B, Koga K, Osuga Y, Hirata T, Saito A, Yoshino O, Hirota Y, Harada M, Takemura Y, Fujii T, Taketani Y: High mobility group box 1 (HMGB1) levels in the placenta and in serum in preeclampsia. Am J Reprod Immunol 2011; 66:143-148.
20. Arck PC, Hecher K: Fetomaternal immune cross-talk and its consequences for maternal and offspring's health. Nat Med 2013; 19:548-556.
21. Cupurdija K, Azzola D, Hainz U, Gratchev A, Heitger A, Takikawa O, Goerdt S, Wintersteiger R, Dohr G, Sedlmayr P: Macrophages of human first trimester decidua express markers associated to alternative activation. Am J Reprod Immunol 2004; 51:117-122.
22. Medeiros LT, Peracoli JC, Bannwart-Castro CF, Romao M, Weel IC, Golim MA, de Oliveira LG, Kurokawa CS, Medeiros Borges VT, Peracoli MT: Monocytes from pregnant women with pre-eclampsia are polarized to a M1 phenotype. Am J Reprod Immunol 2014; 72:5-13.
23. Straszewski-Chavez SL, Abrahams VM, Alvero AB, Aldo PB, Ma Y, Guller S, Romero R, Mor G: The isolation and characterization of a novel telomerase immortalized first trimester trophoblast cell line, Swan 71. Placenta 2009; 30:939-948.
24. Fest S, Aldo PB, Abrahams VM, Visintin I, Alvero A, Chen R, Chavez SL, Romero R, Mor G: Trophoblast-macrophage interactions: a regulatory network for the protection of pregnancy. Am J Reprod Immunol 2007; 57:55-66.
25. Holmberg JC, Haddad S, Wunsche V, Yang Y, Aldo PB, Gnainsky Y, Granot I, Dekel N, Mor G: An in vitro model for the study of human implantation. Am J Reprod Immunol 2012; 67:169-178.
26. Liu J, Zhao S, Tang J, Li Z, Zhong T, Liu Y, Chen D, Zhao M, Li Y, Gong X, Deng P, Wang JH, Jiang Y: Advanced glycation end products and lipopolysaccharide synergistically stimulate proinflammatory cytokine/chemokine production in endothelial cells via activation of both mitogen-activated protein kinases and nuclear factor-kappaB. FEBS J 2009; 276:4598-4606.
27. Jin X, Yao T, Zhou Z, Zhu J, Zhang S, Hu W, Shen C: Advanced glycation end products enhance macrophages polarization into M1 phenotype through activating RAGE/NF-kappaB pathway. Biomed Res Int 2015; 2015:732450.
28. Huang QT, Zhang M, Zhong M, Yu YH, Liang WZ, Hang LL, Gao YF, Huang LP, Wang ZJ: Advanced glycation end products as an upstream molecule triggers ROS-induced sFlt-1 production in extravillous trophoblasts: a novel bridge between oxidative stress and preeclampsia. Placenta 2013; 34:1177-1182.
29. Chen YJ, Sheu ML, Tsai KS, Yang RS, Liu SH: Advanced glycation end products induce peroxisome proliferator-activated receptor gamma down-regulation-related inflammatory signals in human chondrocytes via Toll-like receptor-4 and receptor for advanced glycation end products. PLoS One 2013; 8:e66611.
30. He Q, You H, Li XM, Liu TH, Wang P, Wang BE: HMGB1 promotes the synthesis of pro-IL-1beta and pro-IL-18 by activation of p38 MAPK and NF-kappaB through receptors for advanced glycation end-products in macrophages. Asian Pac J Cancer Prev 2012; 13:1365-1370.
31. Nativel B, Marimoutou M, Thon-Hon VG, Gunasekaran MK, Andries J, Stanislas G, Planesse C, Da Silva CR, Cesari M, Iwema T, Gasque P, Viranaicken W: Soluble HMGB1 is a novel adipokine stimulating IL-6 secretion through RAGE receptor in SW872 preadipocyte cell line: contribution to chronic inflammation in fat tissue. PLoS One 2013; 8:e76039.
32. Qin YH, Dai SM, Tang GS, Zhang J, Ren D, Wang ZW, Shen Q: HMGB1 enhances the proinflammatory activity of lipopolysaccharide by promoting the phosphorylation of MAPK p38 through receptor for advanced glycation end products. J Immunol 2009; 183:6244-6250.
33. Choi HJ, Jang HJ, Chung TW, Jeong SI, Cha J, Choi JY, Han CW, Jang YS, Joo M, Jeong HS, Ha KT: Catalpol suppresses advanced glycation end-products-induced inflammatory responses through inhibition of reactive oxygen species in human monocytic THP-1 cells. Fitoterapia 2013; 86:19-28.
34. Brasier AR: The nuclear factor-kappaB-interleukin-6 signalling pathway mediating vascular inflammation. Cardiovasc Res 2010; 86:211-218.
35. Luo H, Wang J, Qiao C, Ma N, Liu D, Zhang W: Pycnogenol attenuates atherosclerosis by regulating lipid metabolism through the TLR4-NF-kappaB pathway. Exp Mol Med 2015; 47:e191.
36. Bredeson S, Papaconstantinou J, Deford JH, Kechichian T, Syed TA, Saade GR, Menon R: HMGB1 promotes a p38MAPK associated non-infectious inflammatory response pathway in human fetal membranes. PLoS One 2014; 9:e113799.
37. Pradervand PA, Clerc S, Frantz J, Rotaru C, Bardy D, Waeber B, Liaudet L, Vial Y, Feihl F: High mobility group box 1 protein (HMGB-1): a pathogenic role in preeclampsia? Placenta 2014; 35:784-786.
38. Zhu L, Zhang Z, Zhang L, Shi Y, Qi J, Chang A, Gao J, Feng Y, Yang X: HMGB1-RAGE signaling pathway in severe preeclampsia. Placenta 2015; 36:1148-1152.
39. Yan JY, Jiang LL: Expression of advanced glycation end products in placenta and concentration in maternal and umbilical serum in pre-eclampsia. J Obstet Gynaecol Res 2015; 41:843-849.
40. Kalinderis M, Papanikolaou A, Kalinderi K, Ioannidou E, Giannoulis C, Karagiannis V, Tarlatzis BC: Elevated serum levels of interleukin-6, interleukin-1beta and human chorionic gonadotropin in pre-eclampsia. Am J Reprod Immunol 2011; 66:468-475.
41. Lappas M, Permezel M, Rice GE: Advanced glycation endproducts mediate pro-inflammatory actions in human gestational tissues via nuclear factor-kappaB and extracellular signal-regulated kinase 1/2. J Endocrinol 2007; 193:269-277.
42. Feng L, Zhu MM, Zhang MH, Wang RS, Tan XB, Song J, Ding SM, Jia XB, Hu SY: Protection of glycyrrhizic acid against AGEs-induced endothelial dysfunction through inhibiting RAGE/NF-kappaB pathway activation in human umbilical vein endothelial cells. J Ethnopharmacol 2013; 148:27-36.
43. Fan J, Li Y, Levy RM, Fan JJ, Hackam DJ, Vodovotz Y, Yang H, Tracey KJ, Billiar TR, Wilson MA: Hemorrhagic shock induces NAD(P)H oxidase activation in neutrophils: role of HMGB1-TLR4 signaling. J Immunol 2007; 178:6573-6580.
44. Ott C, Jacobs K, Haucke E, Navarrete Santos A, Grune T, Simm A: Role of advanced glycation end products in cellular signaling. Redox Biol 2014; 2:411-429.
45. Venereau E, Ceriotti C, Bianchi ME: DAMPs from cell death to new life. Front Immunol 2015; 6:422.
46. Konishi H, Nakatsuka M, Chekir C, Noguchi S, Kamada Y, Sasaki A, Hiramatsu Y: Advanced glycation end products induce secretion of chemokines and apoptosis in human first trimester trophoblasts. Hum Reprod 2004; 19:2156-2162.
47. Lee JJ, Wang PW, Yang IH, Wu CL, Chuang JH: Amyloid-beta mediates the receptor of advanced glycation end product-induced pro-inflammatory response via toll-like receptor 4 signaling pathway in retinal ganglion cell line RGC-5. Int J Biochem Cell Biol 2015; 64:1-10.
48. Prins JR, Faas MM, Melgert BN, Huitema S, Timmer A, Hylkema MN, Erwich JJ: Altered expression of immune-associated genes in first-trimester human decidua of pregnancies later complicated with hypertension or foetal growth restriction. Placenta 2012; 33:453-455.
49. Matias ML, Romao M, Weel IC, Ribeiro VR, Nunes PR, Borges VT, Araujo JP Jr, Peracoli JC, de Oliveira L, Peracoli MT: Endogenous and uric acid-induced activation of NLRP3 inflammasome in pregnant women with preeclampsia. PLoS One 2015; 10:e0129095.
50. Kauma S, Takacs P, Scordalakes C, Walsh S, Green K, Peng T: Increased endothelial monocyte chemoattractant protein-1 and interleukin-8 in preeclampsia. Obstet Gynecol 2002; 100:706-714.
51. Haucke E, Navarrete Santos A, Simm A, Henning C, Glomb MA, Gurke J, Schindler M, Fischer B, Navarrete Santos A: Accumulation of advanced glycation end products in the rabbit blastocyst under maternal diabetes. Reproduction 2014; 148:169-178.
52. Jinno M, Takeuchi M, Watanabe A, Teruya K, Hirohama J, Eguchi N, Miyazaki A: Advanced glycation end-products accumulation compromises embryonic development and achievement of pregnancy by assisted reproductive technology. Hum Reprod 2011; 26:604-610.
53. Hao L, Noguchi S, Kamada Y, Sasaki A, Matsuda M, Shimizu K, Hiramatsu Y, Nakatsuka M: Adverse effects of advanced glycation end products on embryonal development. Acta Med Okayama 2008; 62:93-99.
54. Bhutada S, Basak T, Savardekar L, Katkam RR, Jadhav G, Metkari SM, Chaudhari UK, Kumari D, Kholkute SD, Sengupta S, Sachdeva G: High mobility group box 1 (HMGB1) protein in human uterine fluid and its relevance in implantation. Hum Reprod 2014; 29:763-780.
55. Boog G: Chronic villitis of unknown etiology. Eur J Obstet Gynecol Reprod Biol 2008; 136:9-15.
56. Derricott H, Jones RL, Heazell AE: Investigating the association of villitis of unknown etiology with stillbirth and fetal growth restriction - a systematic review. Placenta 2013; 34:856-862.