Prenatal lipopolysaccharide exposure results in dysfunction of the renal dopamine D1 receptor in offspring

Free Radical Biology and Medicine

Volumn 76, Issue , 2014, Pages 242-250

  Wang, Xinquan ^a,b   Luo, Hao ^a,b   Chen, Caiyu ^a,b   Chen, Ken ^a,b   Wang, Jialiang ^a,b   Cai, Yue ^a,b   Zheng, Shuo ^a,b   Yang, Xiaoli ^a,b   Zhou, Lin ^a,b   Jose, Pedro A ^c   Zeng, Chunyu ^a,b  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

^b Chongqing Institute of Cardiology   (China)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

D dopamine receptor; Fetal programming; G protein coupledreceptorkinase; Hypertension; Lipopolysaccharide; Oxidativestress; TEMPOL

Indexed keywords

DOPAMINE 1 RECEPTOR; G PROTEIN COUPLED RECEPTOR KINASE 2; G PROTEIN COUPLED RECEPTOR KINASE 4; LIPOPOLYSACCHARIDE; REACTIVE OXYGEN METABOLITE; TEMPOL; ADRBK1 PROTEIN, RAT; AMINE OXIDE; ANTIOXIDANT; GPRK2L PROTEIN, RAT; PROTEIN KINASE C; SPIN LABELING;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE REGULATION; CONTROLLED STUDY; DIURESIS; ELEVATED BLOOD PRESSURE; FEMALE; FETUS; GESTATIONAL AGE; HYPERTENSION; KIDNEY FUNCTION; MALE; NATRIURESIS; NONHUMAN; OXIDATIVE STRESS; PRENATAL EXPOSURE; PROGENY; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; SODIUM URINE LEVEL; ANIMAL; BLOOD PRESSURE; CHEMICALLY INDUCED; DRUG EFFECTS; IMMUNOBLOTTING; KIDNEY PROXIMAL TUBULE; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PREGNANCY; SPIN LABELING; SPRAGUE DAWLEY RAT;

ANIMALS; ANTIOXIDANTS; BLOOD PRESSURE; CYCLIC N-OXIDES; DIURESIS; FEMALE; G-PROTEIN-COUPLED RECEPTOR KINASE 2; G-PROTEIN-COUPLED RECEPTOR KINASE 4; HYPERTENSION; IMMUNOBLOTTING; KIDNEY TUBULES, PROXIMAL; LIPOPOLYSACCHARIDES; NATRIURESIS; OXIDATIVE STRESS; PHOSPHORYLATION; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PROTEIN KINASE C; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; RECEPTORS, DOPAMINE D1; SPIN LABELS;

EID: 84908173997     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2014.08.010     Document Type: Article

References (64)

1. I.C. McMillen, and J.S. Robinson Developmental origins of the metabolic syndrome: prediction, plasticity, and programming Physiol. Rev. 85 2005 571 633
2. E. Ritz, K. Amann, N. Koleganova, and K. Benz Prenatal programming-effects on blood pressure and renal function Nat. Rev. Nephrol. 7 2011 137 144
3. K. Zandi-Nejad, V.A. Luyckx, and B.M. Brenner Adult hypertension and kidney disease: the role of fetal programming Hypertension 47 2006 502 508
4. D.J. Barker The fetal and infant origins of adult disease BMJ 301 1990 1111
5. D.J. Barker The intrauterine environment and adult cardiovascular disease (discussion 10-16) Ciba Found. Symp. 156 1991 3 10
6. R.S. Gibbs The relationship between infections and adverse pregnancy outcomes: an overview Ann. Periodontol. 6 2001 153 163
7. P.H. Patterson Maternal infection and immune involvement in autism Trends Mol. Med. 17 2011 389 394
8. G.M. Khandaker, J. Zimbron, G. Lewis, and P.B. Jones Prenatal maternal infection, neurodevelopment and adult schizophrenia: a systematic review of population-based studies Psychol. Med. 43 2013 239 257
9. A.S. Brown, and E.J. Derkits Prenatal infection and schizophrenia: a review of epidemiologic and translational studies Am. J. Psychiatry 167 2010 261 280
10. M. Huleihel, H. Golan, and M. Hallak Intrauterine infection/inflammation during pregnancy and offspring brain damages: possible mechanisms involved Reprod. Biol. Endocrinol. 2 2004 17
11. D.X. Xu, Y.H. Chen, H. Wang, L. Zhao, J.P. Wang, and W. Wei Effect of N-acetylcysteine on lipopolysaccharide-induced intra-uterine fetal death and intra-uterine growth retardation in mice Toxicol. Sci. 88 2005 525 533
12. N. Quan, E.L. Stern, M.B. Whiteside, and M. Herkenham Induction of pro-inflammatory cytokine mRNAs in the brain after peripheral injection of subseptic doses of lipopolysaccharide in the rat J. Neuroimmunol. 93 1999 72 80
13. A. Urakubo, L.F. Jarskog, J.A. Lieberman, and J.H. Gilmore Prenatal exposure to maternal infection alters cytokine expression in the placenta, amniotic fluid, and fetal brain Schizophr. Res. 47 2001 27 36
14. X.Q. Hao, H.G. Zhang, Z.B. Yuan, D.L. Yang, L.Y. Hao, and X.H. Li Prenatal exposure to lipopolysaccharide alters the intrarenal renin-angiotensin system and renal damage in offspring rats Hypertens. Res. 33 2010 76 82
15. Y.L. Wei, X.H. Li, and J.Z. Zhou Prenatal exposure to lipopolysaccharide results in increases in blood pressure and body weight in rats Acta Pharmacol. Sin. 28 2007 651 656
16. C. Zeng, and P.A. Jose Dopamine receptors: important antihypertensive counterbalance against hypertensive factors Hypertension 57 2011 11 17
17. V. Pinto, M.J. Pinho, and P. Soares-da-Silva Renal amino acid transport systems and essential hypertension FASEB J. 27 2013 2927 2938
18. R.M. Carey Theodore Cooper Lecture. Renal dopamine system: paracrine regulator of sodium homeostasis and blood pressure Hypertension 38 2001 297 302
19. R.C. Harris, and M.Z. Zhang Dopamine, the kidney, and hypertension Curr. Hypertens. Rep. 14 2012 138 143
20. L.J. Salomone, N.L. Howell, H.E. McGrath, B.A. Kemp, S.R. Keller, J.J. Gildea, R.A. Felder, and R.M. Carey Intrarenal dopamine D1-like receptor stimulation induces natriuresis via an angiotensin type-2 receptor mechanism Hypertension 49 2007 155 161
21. A. Nishi, A.C. Eklof, A.M. Bertorello, and A. Aperia Dopamine regulation of renal Na+, K(+)-ATPase activity is lacking in Dahl salt-sensitive rats Hypertension 21 1993 767 771
22. H. Watanabe, J. Xu, C. Bengra, P.A. Jose, and R.A. Felder Desensitization of human renal D1 dopamine receptors by G protein-coupled receptor kinase 4 Kidney Int. 62 2002 790 798
23. G. Chugh, M.F. Lokhandwala, and M. Asghar Altered functioning of both renal dopamine D1 and angiotensin II type 1 receptors causes hypertension in old rats Hypertension 59 2012 1029 1036
24. M. Asghar, A.A. Banday, R.Z. Fardoun, and M.F. Lokhandwala Hydrogen peroxide causes uncoupling of dopamine D1-like receptors from G proteins via a mechanism involving protein kinase C and G-protein-coupled receptor kinase 2 Free Radic. Biol. Med. 40 2006 13 20
25. R.Z. Fardoun, M. Asghar, and M. Lokhandwala Role of nuclear factor kappa B (NF-kappaB) in oxidative stress-induced defective dopamine D1 receptor signaling in the renal proximal tubules of Sprague-Dawley rats Free Radic. Biol. Med. 42 2007 756 764
26. R.Z. Fardoun, M. Asghar, and M. Lokhandwala Role of oxidative stress in defective renal dopamine D1 receptor-G protein coupling and function in old Fischer 344 rats Am. J. Physiol. Renal Physiol. 291 2006 F945 F951
27. A.A. Banday, A. Marwaha, L.S. Tallam, and M.F. Lokhandwala Tempol reduces oxidative stress, improves insulin sensitivity, decreases renal dopamine D1 receptor hyperphosphorylation, and restores D1 receptor-G-protein coupling and function in obese Zucker rats Diabetes 54 2005 2219 2226
28. A. Marwaha, and M.F. Lokhandwala Tempol reduces oxidative stress and restores renal dopamine D1-like receptor- G protein coupling and function in hyperglycemic rats Am. J. Physiol. Renal Physiol. 291 2006 F58 F66
29. C.A. Ladines, C. Zeng, L.D. Asico, X. Sun, F. Pocchiari, C. Semeraro, J. Pisegna, S. Wank, I. Yamaguchi, G.M. Eisner, and P.A. Jose Impaired renal D(1)-like and D(2)-like dopamine receptor interaction in the spontaneously hypertensive rat Am. J. Physiol. Regul. Integr. Comp. Physiol. 281 2001 R1071 R1078
30. H. Yamada, T. Arai, N. Endo, K. Yamashita, K. Fukuda, M. Sasada, and T. Uchiyama LPS-induced ROS generation and changes in glutathione level and their relation to the maturation of human monocyte-derived dendritic cells Life Sci. 78 2006 926 933
31. R.A. Felder, M.G. Seikaly, P. Cody, G.M. Eisner, and P.A. Jose Attenuated renal response to dopaminergic drugs in spontaneously hypertensive rats Hypertension 15 1990 560 569
32. S.H. Padia, B.A. Kemp, N.L. Howell, S.R. Keller, J.J. Gildea, and R.M. Carey Mechanisms of dopamine D(1) and angiotensin type 2 receptor interaction in natriuresis Hypertension 59 2012 437 445
33. T. Nehiri, V.H.J. Duong, M. Viltard, C. Fassot, D. Heudes, N. Freund, G. Deschenes, P. Houillier, P. Bruneval, and M. Lelievre-Pegorier Exposure to maternal diabetes induces salt-sensitive hypertension and impairs renal function in adult rat offspring Diabetes 57 2008 2167 2175
34. V.M. Vehaskari, D.H. Aviles, and J. Manning Prenatal programming of adult hypertension in the rat Kidney Int. 59 2001 238 245
35. V.M. Vehaskari, and L.L. Woods Prenatal programming of hypertension: lessons from experimental models J. Am. Soc. Nephrol. 16 2005 2545 2556
36. M. Xu, Z.L. Sulkowski, P. Parekh, A. Khan, T. Chen, S. Midha, T. Iwasaki, N. Shimokawa, N. Koibuchi, A.M. Zavacki, and E.M. Sajdel-Sulkowska Effects of perinatal lipopolysaccharide (LPS) exposure on the developing rat brain; modeling the effect of maternal infection on the developing human CNS Cerebellum 12 2013 572 586
37. H. Fukui, B. Brauner, J.C. Bode, and C. Bode Plasma endotoxin concentrations in patients with alcoholic and non-alcoholic liver disease: reevaluation with an improved chromogenic assay J. Hepatol. 12 1991 162 169
38. S.J. Fortunato, R.P. Menon, K.F. Swan, and R. Menon Inflammatory cytokine (interleukins 1, 6 and 8 and tumor necrosis factor-alpha) release from cultured human fetal membranes in response to endotoxic lipopolysaccharide mirrors amniotic fluid concentrations (discussion 1861-1852) Am. J. Obstet. Gynecol. 174 1996 1855 1861
39. M. Baharnoori, S.K. Bhardwaj, and L.K. Srivastava Effect of maternal lipopolysaccharide administration on the development of dopaminergic receptors and transporter in the rat offspring PLoS One 8 2013 e54439
40. M.H. Kaufman The atlas of mouse development 1992 Academic Press, Edinburgh University UK 6 26
41. A. Ornoy, and G. Altshuler Maternal endotoxemia, fetal anomalies, and central nervous system damage: a rat model of a human problem Am. J. Obstet. Gynecol. 124 1976 196 204
42. X.Q. Hao, J.X. Du, Y. Li, M. Li, and S.Y. Zhang Prenatal exposure to lipopolysaccharide combined with pre- and postnatal high-fat diet result in lowered blood pressure and insulin resistance in offspring rats PLoS One 9 2014 e88127
43. M.P. Blaustein, and J.M. Hamlyn Signaling mechanisms that link salt retention to hypertension: endogenous ouabain, the Na(+) pump, the Na(+)/Ca(2+) exchanger and TRPC proteins Biochim. Biophys. Acta 1802 2010 1219 1229
44. S.H. Alwasel, I. Kaleem, V. Sahajpal, and N. Ashton Maternal protein restriction reduces angiotensin II AT(1) and AT(2) receptor expression in the fetal rat kidney Kidney Blood Press Res. 33 2010 251 259
45. J.E. Hall, J.P. Granger, J.M. do Carmo, A.A. da Silva, J. Dubinion, E. George, S. Hamza, J. Speed, and M.E. Hall Hypertension: physiology and pathophysiology Comprehens. Physiol. 2 2012 2393 2442
46. A.A. Banday, and M.F. Lokhandwala Dopamine receptors and hypertension Curr. Hypertens. Rep. 10 2008 268 275
47. H. Sanada, J. Yatabe, S. Midorikawa, T. Katoh, S. Hashimoto, T. Watanabe, J. Xu, Y. Luo, X. Wang, C. Zeng, I. Armando, R.A. Felder, and P.A. Jose Amelioration of genetic hypertension by suppression of renal G protein-coupled receptor kinase type 4 expression Hypertension 47 2006 1131 1139
48. R. Gros, J.L. Benovic, C.M. Tan, and R.D. Feldman G-protein-coupled receptor kinase activity is increased in hypertension J. Clin. Invest. 99 1997 2087 2093
49. R.A. Felder, H. Sanada, J. Xu, P.Y. Yu, Z. Wang, H. Watanabe, L.D. Asico, W. Wang, S. Zheng, I. Yamaguchi, S.M. Williams, J. Gainer, N.J. Brown, D. Hazen-Martin, L.J. Wong, J.E. Robillard, R.M. Carey, G.M. Eisner, and P.A. Jose G protein-coupled receptor kinase 4 gene variants in human essential hypertension Proc. Natl. Acad. Sci. USA 99 2002 3872 3877
50. C. Zeng, V.A. Villar, G.M. Eisner, S.M. Williams, R.A. Felder, and P.A. Jose G protein-coupled receptor kinase 4: role in blood pressure regulation Hypertension 51 2008 1449 1455
51. R.A. Felder, and P.A. Jose Mechanisms of disease: the role of GRK4 in the etiology of essential hypertension and salt sensitivity Nat. Clin. Pract. Nephrol. 2 2006 637 650
52. M. Trivedi, and M.F. Lokhandwala Rosiglitazone restores renal D1A receptor-Gs protein coupling by reducing receptor hyperphosphorylation in obese rats Am. J. Physiol. Renal Physiol. 289 2005 F298 F304
53. M.L. Rankin, P.S. Marinec, D.M. Cabrera, Z. Wang, P.A. Jose, and D.R. Sibley The D1 dopamine receptor is constitutively phosphorylated by G protein-coupled receptor kinase 4 Mol. Pharmacol. 69 2006 759 769
54. P.A. Jose, P. Soares-da-Silva, G.M. Eisner, and R.A. Felder Dopamine and G protein-coupled receptor kinase 4 in the kidney: role in blood pressure regulation Biochim. Biophys. Acta 1802 2010 1259 1267
55. N.E. Taylor, P. Glocka, M. Liang, and A.W. Cowley Jr. NADPH oxidase in the renal medulla causes oxidative stress and contributes to salt-sensitive hypertension in Dahl S rats Hypertension 47 2006 692 698
56. S. Meng, G.W. Cason, A.W. Gannon, L.C. Racusen, and R.D. Manning Jr. Oxidative stress in Dahl salt-sensitive hypertension Hypertension 41 2003 1346 1352
57. A.C. Montezano, and R.M. Touyz Oxidative stress, Noxs, and hypertension: experimental evidence and clinical controversies Ann. Med. 44 Suppl. 1 2012 S2 S16
58. M.J. Bell, J.M. Hallenbeck, and V. Gallo Determining the fetal inflammatory response in an experimental model of intrauterine inflammation in rats Pediatr. Res. 56 2004 541 546
59. K. Ejima, T. Koji, H. Nanri, M. Kashimura, and M. Ikeda Expression of thioredoxin and thioredoxin reductase in placentae of pregnant mice exposed to lipopolysaccharide Placenta 20 1999 561 566
60. A.P. Bautista, K. Meszaros, J. Bojta, and J.J. Spitzer Superoxide anion generation in the liver during the early stage of endotoxemia in rats J. Leukoc. Biol. 48 1990 123 128
61. P. Yu, W. Han, V.A. Villar, Y. Yang, Q. Lu, H. Lee, F. Li, M.T. Quinn, J.J. Gildea, R.A. Felder, and P.A. Jose Unique role of NADPH oxidase 5 in oxidative stress in human renal proximal tubule cells Redox Biol. 2 2014 570 579
62. S. Cuevas, V.A. Villar, P.A. Jose, and I. Armando Renal dopamine receptors, oxidative stress, and hypertension Int. J. Mol. Sci 14 9 2013 17553 17572
63. G. Chugh, M.F. Lokhandwala, and M. Asghar Oxidative stress alters renal D1 and AT1 receptor functions and increases blood pressure in old rats Am. J. Physiol. Renal Physiol. 300 2011 F133 F138
64. A.A. Banday, F.R. Fazili, and M.F. Lokhandwala Oxidative stress causes renal dopamine D1 receptor dysfunction and hypertension via mechanisms that involve nuclear factor-kappaB and protein kinase C J. Am. Soc. Nephrol. 18 2007 1446 1457