Endoplasmic reticulum stress is increased after spontaneous labor in human fetal membranes and myometrium where it regulates the expression of prolabor mediators

Biology of Reproduction

Volumn 91, Issue 3, 2014, Pages

  Liong, Stella ^a,b   Lappas, Martha ^a,b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b MERCY HOSPITAL FOR WOMEN   (Australia)

Author keywords

Endoplasmic reticulum stress; Fetal membranes; Human labor; Inflammation; Myometrium; Preterm labor

Indexed keywords

4 PHENYLBUTYRIC ACID; BILE ACID; CYCLOOXYGENASE 2; ENDOTOXIN; GELATINASE A; GELATINASE B; GLUCOSE REGULATED PROTEIN 78; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; PROSTAGLANDIN E2; PROTEIN IRE1; TAUROURSODEOXYCHOLIC ACID; TUMOR NECROSIS FACTOR; X BOX BINDING PROTEIN 1; 4-PHENYLBUTYRIC ACID; ARYLBUTYRIC ACID DERIVATIVE; BIOLOGICAL MARKER; DNA BINDING PROTEIN; ERN1 PROTEIN, HUMAN; HEAT SHOCK PROTEIN; MOLECULAR CHAPERONE GRP78; PROTEIN SERINE THREONINE KINASE; REGULATORY FACTOR X TRANSCRIPTION FACTORS; RIBONUCLEASE; TAUROCHENODEOXYCHOLIC ACID; TRANSCRIPTION FACTOR; UTERUS SPASMOLYTIC AGENT;

ADULT; ARTICLE; CHORIOAMNIONITIS; CLINICAL ARTICLE; CLINICAL ASSESSMENT; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE ASSOCIATION; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; FEMALE; FETUS MEMBRANE; GENE EXPRESSION; HUMAN; INFECTION COMPLICATION; INFLAMMATORY DISEASE; LABOR INDUCTION; MYOMETRIUM; PREMATURE LABOR; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN SECRETION; UNFOLDED PROTEIN RESPONSE; VAGINAL DELIVERY; ALTERNATIVE RNA SPLICING; CESAREAN SECTION; DRUG EFFECTS; EMBRYO MEMBRANE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; LABOR; METABOLISM; PATHOLOGY; PREGNANCY; TISSUE CULTURE TECHNIQUE; UPREGULATION;

BACTERIA (MICROORGANISMS);

ADULT; ALTERNATIVE SPLICING; BIOLOGICAL MARKERS; CESAREAN SECTION; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM STRESS; ENDORIBONUCLEASES; EXTRAEMBRYONIC MEMBRANES; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEAT-SHOCK PROTEINS; HUMANS; LABOR, OBSTETRIC; MYOMETRIUM; OBSTETRIC LABOR, PREMATURE; PHENYLBUTYRATES; PREGNANCY; PROTEIN-SERINE-THREONINE KINASES; TAUROCHENODEOXYCHOLIC ACID; TISSUE CULTURE TECHNIQUES; TOCOLYTIC AGENTS; TRANSCRIPTION FACTORS; UNFOLDED PROTEIN RESPONSE; UP-REGULATION;

EID: 84929510263     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.114.120741     Document Type: Article

References (105)

1. March of Dimes, PMNCH, Save the Children, WHO. Born too soon: the global action report on preterm birth. Howson CP, Kinney MV, Lawn JE (eds.). Geneva: World Health Organization; 2012.
2. Liu L, Johnson HL, Cousens S, Perin J, Scott S, Lawn JE, Rudan I, Campbell H, Cibulskis R, Li M, Mathers C, Black RE, et al. Global, regional, and national causes of child mortality: an updated systematic analysis for 2010 with time trends since 2000. Lancet 2012; 379:2151-2161.
3. Lawn JE, Cousens S, Zupan J, Lancet Neonatal Survival Steering Team. 4 million neonatal deaths: When? Where? Why? Lancet 2005; 365:891-900.
4. Lawn JE, Kerber K, Enweronu-Laryea C, Cousens S. 3.6 million neonatal deaths-what is progressing and what is not? Semin Perinatol 2010; 34:371-386.
5. Mwaniki MK, Atieno M, Lawn JE, Newton CR. Long-term neurodevelopmental outcomes after intrauterine and neonatal insults: a systematic review. Lancet 2012; 379:445-452.
6. National Research Council. Preterm birth: causes, consequences, and prevention. Behrman RE, Butler AS (eds.). Washington, DC: The National Academies Press; 2007.
7. Romero R, Mazor M, Munoz H, Gomez R, Galasso M, Sherer DM. The preterm labor syndrome. Ann N Y Acad Sci 1994; 734:414-429.
8. Bowen JM, Chamley L, Mitchell MD, Keelan JA. Cytokines of the placenta and extra-placental membranes: biosynthesis, secretion and roles in establishment of pregnancy in women. Placenta 2002; 23:239-256.
9. Christiaens I, Zaragoza DB, Guilbert L, Robertson SA, Mitchell BF, Olson DM. Inflammatory processes in preterm and term parturition. J Reprod Immunol 2008; 79:50-57.
10. Olson DM. The role of prostaglandins in the initiation of parturition. Best Pract Res Clin Obstet Gynaecol 2003; 17:717-730.
11. Weiss A, Goldman S, Shalev E. The matrix metalloproteinases (MMPS) in the decidua and fetal membranes. Front Biosci 2007; 12:649-659.
12. Goldenberg RL, Culhane JF, Iams JD, Romero R. Epidemiology and causes of preterm birth. Lancet 2008; 371:75-84.
13. Hotamisligil GS. Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 2010; 140:900-917.
14. Garg AD, Kaczmarek A, Krysko O, Vandenabeele P, Krysko DV, Agostinis P. ER stress-induced inflammation: does it aid or impede disease progression? Trends Mol Med 2012; 18:589-598.
15. Verfaillie T, Garg AD, Agostinis P. Targeting ER stress induced apoptosis and inflammation in cancer. Cancer Lett 2013; 332:249-264.
16. McGuckin MA, Eri RD, Das I, Lourie R, Florin TH. ER stress and the unfolded protein response in intestinal inflammation. Am J Physiol Gastrointest Liver Physiol 2010; 298:G820-G832.
17. Li J, Wang JJ, Yu Q, Wang M, Zhang SX. Endoplasmic reticulum stress is implicated in retinal inflammation and diabetic retinopathy. FEBS Lett 2009; 583:1521-1527.
18. Bird L. ER stress induces systemic inflammation. Nat Rev Immunol 2006; 6:170-171.
19. Bertolotti A, Zhang Y, Hendershot LM, Harding HP, Ron D. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2000; 2:326-332.
20. Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007; 8:519-529.
21. Schroder M, Kaufman RJ. The mammalian unfolded protein response. Annu Rev Biochem 2005; 74:739-789.
22. Patil C, Walter P. Intracellular signaling from the endoplasmic reticulum to the nucleus: the unfolded protein response in yeast and mammals. Curr Opin Cell Biol 2001; 13:349-356.
23. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA, Yuan J. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 2000; 403:98-103.
24. Gargalovic PS, Gharavi NM, Clark MJ, Pagnon J, Yang WP, He AQ, Truong A, Baruch-Oren T, Berliner JA, Kirchgessner TG, Lusis AJ. The unfolded protein response is an important regulator of inflammatory genes in endothelial cells. Arterioscler Thromb Vasc Biol 2006; 26:2490-2496.
25. Martinon F, Chen X, Lee AH, Glimcher LH. TLR activation of the transcription factor XBP1 regulates innate immune responses in macrophages. Nat Immunol 2010; 11:411-U471.
26. Deng J, Lu PD, Zhang Y, Scheuner D, Kaufman RJ, Sonenberg N, Harding HP, Ron D. Translational repression mediates activation of nuclear factor kappa B by phosphorylated translation initiation factor 2. Mol Cell Biol 2004; 24:10161-10168.
27. Hu P, Han Z, Couvillon AD, Kaufman RJ, Exton JH. Autocrine tumor necrosis factor alpha links endoplasmic reticulum stress to the membrane death receptor pathway through IRE1 alpha-mediated NF-kappa B activation and down-regulation of TRAF2 expression. Mol Cell Biol 2006; 26:3071-3084.
28. Yamazaki H, Hiramatsu N, Hayakawa K, Tagawa Y, Okamura M, Ogata R, Huang T, Nakajima S, Yao J, Paton AW, Paton JC, Kitamura M. Activation of the Akt-NF-kappa B pathway by subtilase cytotoxin through the ATF6 branch of the unfolded protein response. J Immunol 2009; 183:1480-1487.
29. Bonizzi G, Karin M. The two NF-kappa B activation pathways and their role in innate and adaptive immunity. Trends Immunol 2004; 25:280-288.
30. Kaneko M, Niinuma Y, Nomura Y. Activation signal of nuclear factor-kappa B in response to endoplasmic reticulum stress is transduced via IRE1 and tumor necrosis factor receptor-associated factor 2. Biol Pharm Bull 2003; 26:931-935.
31. Zhang KZ, Shen XH, Wu J, Sakaki K, Saunders T, Rutkowski DT, Back SH, Kaufman RJ. Endoplasmic reticulum stress activates cleavage of CREBH to induce a systemic inflammatory response. Cell 2006; 124:587-599.
32. Yung HW, Calabrese S, Hynx D, Hemmings BA, Cetin I, Charnock-Jones DS, Burton GJ. Evidence of placental translation inhibition and endoplasmic reticulum stress in the etiology of human intrauterine growth restriction. Am J Pathol 2008; 173:451-462.
33. 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 oset preeclampsia. Placenta 2009; 30:S43-S48.
34. Yung HW, Hemberger M, Watson ED, Senner CE, Jones CP, Kaufman RJ, Charnock-Jones DS, Burton GJ. Endoplasmic reticulum stress disrupts placental morphogenesis: implications for human intrauterine growth restriction. J Pathol 2012; 228:554-564.
35. Lappas M, Rice GE. Transcriptional regulation of the processes of human labour and delivery. Placenta 2009; 30(suppl A):S90-S95.
36. Lamont RF, Sawant SR. Infection in the prediction and antibiotics in the prevention of spontaneous preterm labour and preterm birth. Minerva Ginecol 2005; 57:423-433.
37. Goldenberg RL, Hauth JC, Andrews WW. Intrauterine infection and preterm delivery. N Engl J Med 2000; 342:1500-1507.
38. Dulay AT, Buhimschi CS, Zhao G, Oliver EA, Mbele A, Jing S, Buhimschi IA. Soluble TLR2 is present in human amniotic fluid and modulates the intraamniotic inflammatory response to infection. J Immunol 2009; 182:7244-7253.
39. Benjamin DK, DeLong E, Cotten CM, Garges HP, Steinbach WJ, Clark RH. Mortality following blood culture in premature infants: increased with gram-negative bacteremia and candidemia, but not gram-positive bacteremia. J Perinatol 2004; 24:175-180.
40. Stoll BJ, Hansen N, Fanaroff AA, Wright LL, Carlo WA, Ehrenkranz RA, Lemons JA, Donovan EF, Stark AR, Tyson JE, Oh W, Bauer CR, et al. Changes in pathogens causing early-onset sepsis in very-low-birthweight infants. N Engl J Med 2002; 347:240-247.
41. Lirussi F, O'Brien M, Wendremaire M, Goirand F, Sagot P, Dumas M, Morrison JJ, Bardou M. SAR150640, a selective beta3-adrenoceptor agonist, prevents human myometrial remodelling and activation of matrix metalloproteinase in an in vitro model of chorioamnionitis. Br J Pharmacol 2010; 159:1354-1366.
42. Hutchinson JL, Rajagopal SP, Yuan M, Norman JE. Lipopolysaccharide promotes contraction of uterine myocytes via activation of Rho/ROCK signaling pathways. FASEB J 2014; 28:94-105.
43. Welch WJ, Brown CR. Influence of molecular and chemical chaperones on protein folding. Cell Stress Chaperones 1996; 1:109-115.
44. Kawasaki N, Asada R, Saito A, Kanemoto S, Imaizumi K. Obesity-induced endoplasmic reticulum stress causes chronic inflammation in adipose tissue. Sci Rep 2012; 2:799.
45. Basseri S, Lhotak S, Sharma AM, Austin RC. The chemical chaperone 4-phenylbutyrate inhibits adipogenesis by modulating the unfolded protein response. J Lipid Res 2009; 50:2486-2501.
46. Ozcan U, Yilmaz E, Ozcan L, Furuhashi M, Vaillancourt E, Smith RO, Gorgun CZ, Hotamisligil GS. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 2006; 313:1137-1140.
47. Ozcan L, Ergin AS, Lu A, Chung J, Sarkar S, Nie D, Myers MG, Ozcan U. Endoplasmic reticulum stress plays a central role in development of leptin resistance. Cell Metab 2009; 9:35-51.
48. Qi X, Hosoi T, Okuma Y, Kaneko M, Nomura Y. Sodium 4-phenylbutyrate protects against cerebral ischemic injury. Mol Pharmacol 2004; 66:899-908.
49. Ryu H, Smith K, Camelo SI, Carreras I, Lee J, Iglesias AH, Dangond F, Cormier KA, Cudkowicz ME, Brown RH, Ferrante RJ. Sodium phenylbutyrate prolongs survival and regulates expression of anti-apoptotic genes in transgenic amyotrophic lateral sclerosis mice. J Neurochem 2005; 93:1087-1098.
50. Miller SDW, Greene CM, McLean C, Lawless MW, Taggart CC, O'Neill SJ, McElvaney NG. Tauroursodeoxycholic acid inhibits apoptosis induced by Z alpha-1 antitrypsin via inhibition of Bad. Hepatology 2007; 46:496-503.
51. Kim HJ, Jeong JS, Kim SR, Park SY, Chae HJ, Lee YC. Inhibition of endoplasmic reticulum stress alleviates lipopolysaccharide-induced lung inflammation through modulation of NF-kappaB/HIF-1alpha signaling pathway. Sci Rep 2013; 3:1142.
52. Mosbah IB, Alfany-Fernandez I, Martel C, Zaouali MA, Bintanel-Morcillo M, Rimola A, Rodes J, Brenner C, Rosello-Catafau J, Peralta C. Endoplasmic reticulum stress inhibition protects steatotic and nonsteatotic livers in partial hepatectomy under ischemia-reperfusion. Cell Death Dis 2010; 1:e52.
53. Lappas M, Odumetse TL, Riley C, Reti NG, Holdsworth-Carson SJ, Rice GE, Permezel M. Pre-labour fetal membranes overlying the cervix display alterations in inflammation and NF-kappaB signalling pathways. Placenta 2008; 29:995-1002.
54. Lappas M, Mitton A, Lim R, Barker G, Riley C, Permezel M. SIRT1 is a novel regulator of key pathways of human labor. Biol Reprod 2011; 84:167-178.
55. Lappas M. Caspase-1 activation is increased with human labour in foetal membranes and myometrium and mediates infection-induced interleukin-1beta secretion. Am J Reprod Immunol 2014; 71:189-201.
56. Lappas M. NOD1 and NOD2 regulate proinflammatory and prolabor mediators in human fetal membranes and myometrium via nuclear factor-kappa B. Biol Reprod 2013; 89:14.
57. Lim R, Barker G, Riley C, Lappas M. Apelin is decreased with human preterm and term labor and regulates prolabor mediators in human primary amnion cells. Reprod Sci 2013; 20:957-967.
58. Lappas M. Forkhead box O1 (FOXO1) in pregnant human myometrial cells: a role as a pro-inflammatory mediator in human parturition. J Reprod Immunol 2013; 99:24-32.
59. Lim R, Morwood CJ, Barker G, Lappas M. Effect of silibinin in reducing inflammatory pathways in in vitro and in vivo models of infection-induced preterm birth. PLoS One 2014; 9:e92505.
60. Lappas M, Permezel M, Rice GE. N-Acetyl-cysteine inhibits phospholipid metabolism, proinflammatory cytokine release, protease activity, and nuclear factor-kappaB deoxyribonucleic acid-binding activity in human fetal membranes in vitro. J Clin Endocrinol Metab 2003; 88:1723-1729.
61. Lim R, Barker G, Lappas M. SIRT6 is decreased with preterm labor and regulates key terminal effector pathways of human labor in fetal membranes. Biol Reprod 2013; 88:17.
62. Lim R, Barker G, Wall CA, Lappas M. Dietary phytophenols curcumin, naringenin and apigenin reduce infection-induced inflammatory and contractile pathways in human placenta, foetal membranes and myometrium. Mol Hum Reprod 2013; 19:451-462.
63. Chu ZL, McKinsey TA, Liu L, Gentry JJ, Malim MH, Ballard DW. Suppression of tumor necrosis factor-induced cell death by inhibitor of apoptosis c-IAP2 is under NF-kappaB control. Proc Natl Acad Sci U S A 1997; 94:10057-10062.
64. Holdsworth-Carson SJ, Permezel M, Rice GE, Lappas M. Preterm and infection-driven preterm labor: the role of peroxisome proliferator-activated receptors and retinoid X receptor. Reproduction 2009; 137:1007-1015.
65. Flamment M, Hajduch E, Ferre P, Foufelle F. New insights into ER stress-induced insulin resistance. Trends Endocrinol Metab 2012; 23:381-390.
66. Bartoszewski R, Rab A, Jurkuvenaite A, Mazur M, Wakefield J, Collawn JF, Bebok Z. Activation of the unfolded protein response by deltaF508 CFTR. Am J Respir Cell Mol Biol 2008; 39:448-457.
67. Carrasco DR, Sukhdeo K, Protopopova M, Sinha R, Enos M, Carrasco DE, Zheng M, Mani M, Henderson J, Pinkus GS, Munshi N, Horner J, et al. The differentiation and stress response factor XBP-1 drives multiple myeloma pathogenesis. Cancer Cell 2007; 11:349-360.
68. Jamora C, Dennert G, Lee AS. Inhibition of tumor progression by suppression of stress protein GRP78/BiP induction in fibrosarcoma B/C10ME. Proc Natl Acad Sci U S A 1996; 93:7690-7694.
69. Kaser A, Lee AH, Franke A, Glickman JN, Zeissig S, Tilg H, Nieuwenhuis EE, Higgins DE, Schreiber S, Glimcher LH, Blumberg RS. XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell 2008; 134:743-756.
70. Norwitz ER, Robinson JN, Challis JR. The control of labor. N Engl J Med 1999; 341:660-666.
71. Slater D, Allport V, Bennett P. Changes in the expression of the type-2 but not the type-1 cyclo-oxygenase enzyme in chorion-decidua with the onset of labour. Br J Obstet Gynaecol 1998; 105:745-748.
72. Belt AR, Baldassare JJ, Molnar M, Romero R, Hertelendy F. The nuclear transcription factor NF-kappaB mediates interleukin-1beta-induced expression of cyclooxygenase-2 in human myometrial cells. Am J Obstet Gynecol 1999; 181:359-366.
73. Kovacs JJ, Murphy PJ, Gaillard S, Zhao X, Wu JT, Nicchitta CV, Yoshida M, Toft DO, Pratt WB, Yao TP. HDAC6 regulates Hsp90 acetylation and chaperone-dependent activation of glucocorticoid receptor. Mol Cell 2005; 18:601-607.
74. Sola S, Ma X, Castro RE, Kren BT, Steer CJ, Rodrigues CM. Ursodeoxycholic acid modulates E2F-1 and p53 expression through a caspase-independent mechanism in transforming growth factor beta1-induced apoptosis of rat hepatocytes. J Biol Chem 2003; 278:48831-48838.
75. Sola S, Castro RE, Laires PA, Steer CJ, Rodrigues CM. Tauroursodeoxycholic acid prevents amyloid-beta peptide-induced neuronal death via a phosphatidylinositol 3-kinase-dependent signaling pathway. Mol Med 2003; 9:226-234.
76. Kim SR, Kim DI, Kang MR, Lee KS, Park SY, Jeong JS, Lee YC. Endoplasmic reticulum stress influences bronchial asthma pathogenesis by modulating nuclear factor kappaB activation. J Allergy Clin Immunol 2013; 132:1397-1408.
77. Anderson CD, Upadhya G, Conzen KD, Jia J, Brunt EM, Tiriveedhi V, Xie Y, Ramachandran S, Mohanakumar T, Davidson NO, Chapman WC. Endoplasmic reticulum stress is a mediator of posttransplant injury in severely steatotic liver allografts. Liver Transpl 2011; 17:189-200.
78. Lappas M, Rice GE. The role and regulation of the nuclear factor kappa B signalling pathway in human labour. Placenta 2007; 28:543-556.
79. Kim S, Joe Y, Jeong SO, Zheng M, Back SH, Park SW, Ryter SW, Chung HT. Endoplasmic reticulum stress is sufficient for the induction of IL-1beta production via activation of the NF-kappaB and inflammasome pathways. Innate Immun (in press). Published online before print 11 November 2013; DOI: 10.1177/1753425913508593.
80. Sadowsky DW, Adams KM, Gravett MG, Witkin SS, Novy MJ. Preterm labor is induced by intraamniotic infusions of interleukin-1beta and tumor necrosis factor-alpha but not by interleukin-6 or interleukin-8 in a nonhuman primate model. Am J Obstet Gynecol 2006; 195:1578-1589.
81. Baggia S, Gravett MG, Witkin SS, Haluska GJ, Novy MJ. Interleukin-1 beta intra-amniotic infusion induces tumor necrosis factor-alpha, prostaglandin production, and preterm contractions in pregnant rhesus monkeys. J Soc Gynecol Investig 1996; 3:121-126.
82. Martey CA, Pollock SJ, Turner CK, O'Reilly KM, Baglole CJ, Phipps RP, Sime PJ. Cigarette smoke induces cyclooxygenase-2 and microsomal prostaglandin E2 synthase in human lung fibroblasts: implications for lung inflammation and cancer. Am J Physiol Lung Cell Mol Physiol 2004; 287:L981-L991.
83. Kelsen SG, Duan XB, Ji R, Perez O, Liu C, Merali S. Cigarette smoke induces an unfolded protein response in the human lung-a proteomic approach. Am J Respir Cell Mol Biol 2008; 38:541-550.
84. Jorgensen E, Stinson A, Shan L, Yang J, Gietl D, Albino AP. Cigarette smoke induces endoplasmic reticulum stress and the unfolded protein response in normal and malignant human lung cells. BMC Cancer 2008; 8:229.
85. Tagawa Y, Hiramatsu N, Kasai A, Hayakawa K, Okamura M, Yao J, Kitamura M. Induction of apoptosis by cigarette smoke via ROS-dependent endoplasmic reticulum stress and CCAAT/enhancer-binding protein-homologous protein (CHOP). Free Radic Biol Med 2008; 45:50-59.
86. Allport VC, Pieber D, Slater DM, Newton R, White JO, Bennett PR. Human labour is associated with nuclear factor-kappaB activity which mediates cyclo-oxygenase-2 expression and is involved with the "functional progesterone withdrawal." Mol Hum Reprod 2001; 7:581-586.
87. Cindrova-Davies T, Yung HW, Johns J, Spasic-Boskovic O, Korolchuk S, Jauniaux E, Burton GJ, Charnock-Jones DS. Oxidative stress, gene expression, and protein changes induced in the human placenta during labor. Am J Pathol 2007; 171:1168-1179.
88. Cullinan SB, Diehl JA. Coordination of ER and oxidative stress signaling: the PERK/Nrf2 signaling pathway. Int J Biochem Cell Biol 2006; 38:317-332.
89. Salminen A, Kauppinen A, Suuronen T, Kaarniranta K, Ojala J. ER stress in Alzheimer's disease: a novel neuronal trigger for inflammation and Alzheimer's pathology. J Neuroinflammation 2009; 6:41.
90. Ito H, Iwamoto I, Inaguma Y, Takizawa T, Nagata K, Asano T, Kato K. Endoplasmic reticulum stress induces the phosphorylation of small heat shock protein, Hsp27. J Cell Biochem 2005; 95:932-941.
91. Marcu MG, Doyle M, Bertolotti A, Ron D, Hendershot L, Neckers L. Heat shock protein 90 modulates the unfolded protein response by stabilizing IRE1alpha. Mol Cell Biol 2002; 22:8506-8513.
92. Ota A, Wang Y. Cdc37/Hsp90 protein-mediated regulation of IRE1alpha protein activity in endoplasmic reticulum stress response and insulin synthesis in INS-1 cells. J Biol Chem 2012; 287:6266-6274.
93. Dafforn TR, Della M, Miller AD. The molecular interactions of heat shock protein 47 (Hsp47) and their implications for collagen biosynthesis. J Biol Chem 2001; 276:49310-49319.
94. Kumar D, Fung W, Moore RM, Pandey V, Fox J, Stetzer B, Mansour JM, Mercer BM, Redline RW, Moore JJ. Proinflammatory cytokines found in amniotic fluid induce collagen remodeling, apoptosis, and biophysical weakening of cultured human fetal membranes. Biol Reprod 2006; 74:29-34.
95. Bryant-Greenwood GD, Yamamoto SY. Control of peripartal collage-nolysis in the human chorion-decidua. Am J Obstet Gynecol 1995; 172:63-70.
96. Facchinetti F, Venturini P, Blasi I, Giannella L. Changes in the cervical competence in preterm labour. BJOG 2005; 112(suppl 1):23-27.
97. Park B, Lee S, Kim E, Cho K, Riddell SR, Cho S, Ahn K. Redox regulation facilitates optimal peptide selection by MHC class I during antigen processing. Cell 2006; 127:369-382.
98. Osman I, Young A, Ledingham MA, Thomson AJ, Jordan F, Greer IA, Norman JE. Leukocyte density and pro-inflammatory cytokine expression in human fetal membranes, decidua, cervix and myometrium before and during labour at term. Mol Hum Reprod 2003; 9:41-45.
99. Steenport M, Khan KM, Du B, Barnhard SE, Dannenberg AJ, Falcone DJ. Matrix metalloproteinase (MMP)-1 and MMP-3 induce macrophage MMP-9: evidence for the role of TNF-alpha and cyclooxygenase-2. J Immunol 2009; 183:8119-8127.
100. Choi SJ, Oh Sy, Kim JH, Roh CR. Changes of nuclear factor kappa B (NF-kappaB), cyclooxygenase-2 (COX-2) and matrix metalloproteinase-9 (MMP-9) in human myometrium before and during term labor. Eur J Obstet Gynecol Reprod Biol 2007; 132:182-188.
101. Roh CR, Oh WJ, Yoon BK, Lee JH. Up-regulation of matrix metalloproteinase-9 in human myometrium during labour: a cytokine-mediated process in uterine smooth muscle cells. Mol Hum Reprod 2000; 6:96-102.
102. Mitchell MD, Branch DW, Lundin-Schiller S, Romero RJ, Daynes RA, Dudley DJ. Immunologic aspects of preterm labor. Semin Perinatol 1991; 15:210-224.
103. Romero R, Wu YK, Mazor M, Oyarzun E, Hobbins JC, Mitchell MD. Amniotic fluid arachidonate lipoxygenase metabolites in preterm labor. Prostaglandins Leukot Essent Fatty Acids 1989; 36:69-75.
104. Enns GM, Berry SA, Berry GT, Rhead WJ, Brusilow SW, Hamosh A. Survival after treatment with phenylacetate and benzoate for urea-cycle disorders. N Engl J Med 2007; 356:2282-2292.
105. Beuers U. Drug insight: mechanisms and sites of action of ursodeoxycholic acid in cholestasis. Nat Clin Pract Gastroenterol Hepatol 2006; 3:318-328.