Lipopolysaccharide exposure during pregnancy leads to aortic dysfunction in offspring rats

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Zhao, Shanyu ^a   Zhang, Haigang ^a   Cao, Dayan ^a   Liu, Ya ^a   Li, Xiaohui ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CONNEXIN 37; CONNEXIN 40; CONNEXIN 43; CONNEXIN 45; I KAPPA B ALPHA; I KAPPA B BETA; LIPOPOLYSACCHARIDE; MESSENGER RNA; PYRROLIDINE DITHIOCARBAMATE; SODIUM CHLORIDE; TRANSCRIPTION FACTOR RELA; GAP JUNCTION PROTEIN; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA DISEASE; ARTICLE; CARDIOVASCULAR DISEASE; CONTROLLED STUDY; DISEASE PREDISPOSITION; FEMALE; GESTATION PERIOD; HISTOPATHOLOGY; IMMUNOFLUORESCENCE; MALE; NONHUMAN; PREGNANCY; PRENATAL EXPOSURE; PROGENY; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; VASCULAR RING; ADVERSE EFFECTS; ANIMAL; AORTA; CARDIOVASCULAR DISEASES; DISEASE MODEL; ENVIRONMENTAL EXPOSURE; GENETICS; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHOSPHORYLATION; ULTRASTRUCTURE;

ANIMALS; AORTA; CARDIOVASCULAR DISEASES; CONNEXINS; DISEASE MODELS, ANIMAL; FEMALE; I-KAPPA B PROTEINS; LIPOPOLYSACCHARIDES; MATERNAL EXPOSURE; NF-KAPPA B; PHOSPHORYLATION; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS;

EID: 84904261245     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0102273     Document Type: Article

References (50)

1. Daviglus ML, Lloyd-Jones DM, Pirzada A (2006) Preventing cardiovascular disease in the 21st century: therapeutic and preventive implications of current evidence. Am J Cardiovasc Drugs 6:87-101.
2. Barker DJ (2000) In utero programming of cardiovascular disease. Theriogenology 53: 555-74.
3. Eriksson JG, Forsén T, Tuomilehto J, Osmond C, Barker DJ (2001) Early growth and coronary heart disease in later life: longitudinal study. BMJ 322:949-53. (Pubitemid 32374683)
4. Tsukuda K, Mogi M, Iwanami J, Min LJ, Jing F, et al. (2012) Influence of angiotensin II type 1 receptor-associated protein on prenatal development and adult hypertension after maternal dietary protein restriction during pregnancy. J Am Soc Hypertens 6:324-30.
5. O'Regan D, Kenyon CJ, Seckl JR, Holmes MC (2004) Glucocorticoid exposure in late gestation in the rat permanently programs gender-specific differences in adult cardiovascular and metabolic physiology. Am J Physiol Endocrinol Metab 287:E863-70. (Pubitemid 39382921)
6. Bol VV, Delattre AI, Reusens B, Raes M, Remacle C (2009) Forced catch-up growth after fetal protein restriction alters the adipose tissue gene expression program leading to obesity in adult mice. Am J Physiol Regul Integr Comp Physiol 297:R291-9.
7. Samuelsson AM, Matthews PA, Argenton M, Christie MR, McConnell JM, et al. (2008) Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance: a novel murine model of developmental programming. Hypertension 51:383-92. (Pubitemid 351159954)
8. Wei YL, Li XH, Zhou JZ (2007) Prenatal exposure to lipopolysaccharide results in increases in blood pressure and body weight in rats. Acta Pharmacol Sin 28:651-6.
9. Liao W, Wei Y, Yu C, Zhou J, Li S, et al. (2008) Prenatal exposure to zymosan results in hypertension in adult offspring rats. Clin Exp Pharmacol Physiol 35:1413-8.
10. He XY, Deng YC, Li SH, Wei YL, Hao LY, et al. (2011) Prenatal exposure to lipopolysaccharide results in vascular renin-angiotensin system dysfunction in offspring rats. Zhonghua Xin Xue Guan Bing Za Zhi 39:853-6.
11. Hao XQ, Zhang HG, Li SH, Jia Y, Liu Y, et al. (2010) Prenatal exposure to inflammation induced by zymosan results in activation of intrarenal renin-angiotensin system in adult offspring rats. Inflammation 33:408-14.
12. Keelan JA, Khan S, Yosaatmadja F, Mitchell MD (2009) Prevention of inflammatory activation of human gestational membranes in an ex vivo model using a pharmacological NF-kappaB inhibitor. J Immunol 183:5270-8.
13. Palinski W, Napoli C (2008) Impaired fetal growth, cardiovascular disease, and the need to move on. Circulation 117:341-3.
14. Palinski W, Nicolaides E, Liguori A, Napoli C (2009) Influence of maternal dysmetabolic conditions during pregnancy on cardiovascular disease. J Cardiovasc Transl Res 2:277-85.
15. Yzydorczyk C, Comte B, Cambonie G, Lavoie JC, Germain N, et al. (2008) Neonatal oxygen exposure in rats leads to cardiovascular and renal alterations in adulthood. Hypertension 52:889-95.
16. Singh RR, Cullen-McEwen LA, Kett MM, Boon WM, Dowling J, et al. (2007) Prenatal corticosterone exposure results in altered AT1/AT2, nephron deficit and hypertension in the rat offspring. J Physiol 579:503-13.
17. van Vliet LS, Poelmann RE, Havekes LM, Willems van Dijk K, DeRuiter MC (2007) Intrauterine exposure to maternal atherosclerotic risk factors increases the susceptibility to atherosclerosis in adult life. Arterioscler Thromb Vasc Biol 27:2228-35.
18. Rogers LK, Velten M (2011) Maternal inflammation, growth retardation, and preterm birth: insights into adult cardiovascular disease. Life Sci 89:417-21.
19. Velten M, Hutchinson KR, Gorr MW, Wold LE, Lucchesi PA, et al. (2011) Systemic maternal inflammation and neonatal hyperoxia induces remodeling and left ventricular dysfunction in mice. PLoS One 6:e24544.
20. Bevan JA, Osher JV (1972) A direct method for recording tension changes in the wall of small blood vessels in vitro. Agents Actions 2:257-60.
21. Hampton T (2004) Fetal environment may have profound long-term consequences for health. JAMA 292:1285-6.
22. Kohmura Y, Kirikae T, Kirikae F, Nakano M, Sato I (2000) Lipopolysaccharide (LPS)-induced intra-uterine fetal death (IUFD) in mice is principally due to maternal cause but not fetal sensitivity to LPS. Microbiol Immunol 44:897-904. (Pubitemid 32000939)
23. Salminen A, Paananen R, Vuolteenaho R, Metsola J, Ojaniemi M, et al. (2008) Maternal endotoxin-induced preterm birth in mice: fetal responses in toll-like receptors, collectins, and cytokines. Pediatr Res 63:280-6. (Pubitemid 351301457)
24. Zhou J, Zhang X, Zhang H, Jia Y, Liu Y, et al. (2013) Use of data mining to determine changes in the gene expression profiles of rat embryos following prenatal exposure to inflammatory stimulants. Mol Med Rep 8:95-102.
25. Nijdam ME, Plantinga Y, Hulsen HT, Bos WJ, Grobbee DE, et al. (2008) Pulse pressure amplification and risk of cardiovascular disease. Am J Hypertens 21:388-92. (Pubitemid 351450859)
26. Chobanian AV, Bakris GL, Black HR, Cushman WC, Green LA, et al. (2003) The Seventh Report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure: the JNC 7 report. JAMA 289:2560-72. (Pubitemid 37430158)
27. Zhao SY, Liu Y, Li XH (2014) Effect of Maternal LPS exposure during pregnancy on vascular structure in neonatal offspring rats. Zhonghua Xin Xue Guan Bing Za Zhi.42 (Epub ahead of print)
28. Weisbrod RM, Shiang T, Al Sayah L, Fry JL, Bajpai S, et al. (2013) Arterial stiffening precedes systolic hypertension in diet-induced obesity. Hypertension 62:1105-10.
29. Olzinski AR, McCafferty TA, Zhao SQ, Behm DJ, Eybye ME, et al. (2005) Hypertensive target organ damage is attenuated by a p38 MAPK inhibitor: role of systemic blood pressure and endothelial protection. Cardiovasc Res 66:170-8. (Pubitemid 40357880)
30. Christ GJ, Spray DC, el-Sabban M, Moore LK, Brink PR (1996) Gap junctions in vascular tissues. Evaluating the role of intercellular communication in the modulation of vasomotor tone. Circ Res 79:631-46. (Pubitemid 26317811)
31. Yeh HI, Chang HM, Lu WW, Lee YN, Ko YS, et al. (2000) Age-related alteration of gap junction distribution and connexin expression in rat aortic endothelium. J Histochem Cytochem 48:1377-89.
32. Simon AM, McWhorter AR (2003) Decreased intercellular dye-transfer and downregulation of non-ablated connexins in aortic endothelium deficient in connexin37 or connexin40. J Cell Sci 116:2223-6.
33. Figueroa XF, Duling BR (2009) Gap junctions in the control of vascular function. Antioxid Redox Signal 11:251-66.
34. Haefliger JA, Meda P, Formenton A, Wiesel P, Zanchi A, et al. (1999) Aortic connexin43 is decreased during hypertension induced by inhibition of nitric oxide synthase. Arterioscler Thromb Vasc Biol 19:1615-22. (Pubitemid 29323819)
35. Jobs A, Schmidt K, Schmidt VJ, Lübkemeier I, van Veen TA, et al. (2012) Defective Cx40 maintains Cx37 expression but intact Cx40 is crucial for conducted dilations irrespective of hypertension. Hypertension 60:1422-9.
36. Wagner C, Jobs A, Schweda F, Kurtz L, Kurt B, et al. (2010) Selective deletion of Connexin 40 in renin-producing cells impairs renal baroreceptor function and is associated with arterial hypertension. Kidney Int 78:762-8.
37. Tang EH, Vanhoutte PM (2008) Gap junction inhibitors reduce endothelium-dependent contractions in the aorta of spontaneously hypertensive rats. J Pharmacol Exp Ther 327:148-53.
38. Alonso F, Boittin FX, Bény JL, Haefliger JA (2010) Loss of connexin40 is associated with decreased endothelium-dependent relaxations and eNOS levels in the mouse aorta. Am J Physiol Heart Circ Physiol 299:H1365-73.
39. McKinnon RL, Lidington D, Bolon M, Ouellette Y, Kidder GM, et al. (2006) Reduced arteriolar conducted vasoconstriction in septic mouse cremaster muscle is mediated by nNOS-derived NO. Cardiovasc Res 69:236-44. (Pubitemid 41814825)
40. Isakson BE, Kronke G, Kadl A, Leitinger N, Duling BR (2006) Oxidized phospholipids alter vascular connexin expression, phosphorylation, and heterocellular communication. Arterioscler Thromb Vasc Biol 26:2216-21. (Pubitemid 44465714)
41. Wong CW, Christen T, Roth I, Chadjichristos CE, Derouette JP, et al. (2006) Connexin37 protects against atherosclerosis by regulating monocyte adhesion. Nat Med 12:950-4. (Pubitemid 44175148)
42. Plum A, Hallas G, Magin T, Dombrowski F, Hagendorff A, et al. (2000) Unique and shared functions of different connexins in mice. Curr Biol 10:1083-91.
43. Liu J, Zhao S, Tang J, Li Z, Zhong T, et al. (2009) 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 276:4598-4606.
44. Csiszar A, Wang M, Lakatta EG, Ungvari Z (2008) Inflammation and endothelial dysfunction during aging: role of NF-kappaB. J Appl Physiol 105:1333-41.
45. Elks CM, Mariappan N, Haque M, Guggilam A, Majid DS, et al. (2009) Chronic NF-{kappa}B blockade reduces cytosolic and mitochondrial oxidative stress and attenuates renal injury and hypertension in SHR. Am J Physiol Renal Physiol 296:F298-305.
46. Muller DN, Dechend R, Mervaala EM, Park JK, Schmidt F, et al. (2000) NF-kappaB inhibition ameliorates angiotensin II-induced inflammatory damage in rats. Hypertension 35:193-201. (Pubitemid 30054172)
47. Hao XQ, Zhang HG, Yuan ZB, Yang DL, Hao LY, et al. (2010) Prenatal exposure to lipopolysaccharide alters the intrarenal renin-angiotensin system and renal damage in offspring rats. Hypertens Res 33:76-82.
48. Pfenniger A, Derouette JP, Verma V, Lin X, Foglia B, et al. (2010) Gap junction protein Cx37 interacts with endothelial nitric oxide synthase in endothelial cells. Arterioscler Thromb Vasc Biol 30:827-34.
49. Tsai SH, Huang PH, Peng YJ, Chang WC, Tsai HY, et al. (2013) Zoledronate attenuates angiotensin II-induced abdominal aortic aneurysm through inactivation of Rho/ROCK-dependent JNK and NF-kB pathway. Cardiovasc Res 100:501-10.
50. Takahashi M, Suzuki E, Takeda R, Oba S, Nishimatsu H, et al. (2008) Angiotensin II and tumor necrosis factor-alpha synergistically promote monocyte chemoattractant protein-1 expression: roles of NF-kappaB, p38, and reactive oxygen species. Am J Physiol Heart Circ Physiol 294:H2879-88. China