A mutant Ahr allele protects the embryonic kidney from hydrocarbon-induced deficits in fetal programming

Environmental Health Perspectives

Volumn 119, Issue 12, 2011, Pages 1745-1753

  Nanez, Adrian ^a   Ramos, Irma N ^a   Ramos, Kenneth S ^a  

^a UNIVERSITY OF LOUISVILLE   (United States)

Author keywords

Aryl hydrocarbon receptor; Benzo(a)pyrene; Fetal programming; Nephrogenesis; WT1

Indexed keywords

BENZO[A]PYRENE; EPIDERMAL GROWTH FACTOR RECEPTOR; HOMEODOMAIN PROTEIN; LIM HOMEOBOX PROTEIN 1; MESSENGER RNA; RETINOIC ACID RECEPTOR ALPHA; SECRETED FRIZZLED RELATED PROTEIN 1; SOMATOMEDIN C RECEPTOR; SYNDECAN 1; TRANSCRIPTION FACTOR PAX2; UNCLASSIFIED DRUG; UVOMORULIN; WNT4 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CELL DIFFERENTIATION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DOWN REGULATION; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; FETUS; FETUS DEVELOPMENT; GENE EXPRESSION REGULATION; GENE FREQUENCY; GENE FUNCTION; GENE TARGETING; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GESTATIONAL AGE; KIDNEY DEVELOPMENT; KIDNEY DYSFUNCTION; LIGAND BINDING; MOUSE; NEPHRON; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROGENY; RNA SPLICING; TUMOR SUPPRESSOR GENE; WILM TUMOR SUPPRESSOR GENE;

EID: 82755177626     PISSN: 00916765     EISSN: 15529924     Source Type: Journal    
DOI: 10.1289/ehp.1103692     Document Type: Article

References (67)

1. Avner ED. 1993 Renal developmental diseases. Semin Nephrol 13:427-435.
2. Barbaux S, Niaudet P, Gubler M-C, Grünfeld J-P, Jaubert F, Kuttenn F, et al. 1997. Donor splice-site mutations in WT1 are responsible for Frasier syndrome. Nat Genet 17:467-470.
3. Barker DJP. 2004. The developmental origins of adult disease. J Am Coll Nutr 23(suppl 6):588S-595S.
4. Barnes JD, Crosby JL, Jones CM, Wright CVE, Hogan BLM. 1994. Embryonic expression of Lim-1, the mouse homolog of Xenopus XLim-1, suggests a role in lateral mesoderm differentiation and neurogenesis. Dev Biol 161:168-178.
5. Bertazzi PA, Pesatori AC, Zocchetti C, Latocca R. 1989. Mortality study of cancer risk among oil refinery workers. Int Arch Occup Environ Health 61(4):261-270.
6. Bowes RC, Ramos KS. 1994. Responses of vascular smooth muscle cells to toxic insult: cellular and molecular perspectives for environmental toxicants. Toxicol In Vitro 8:1151-1160.
7. Celsi G, Kistner A, Aizman R, Eklof AC, Ceccatelli S, de Santiago A, et al. 1998. Prenatal dexamethasone causes oligonephronia, sodium retention, and higher blood pressure in the offspring. Pediatr Res 44(3):317-322.
8. Cho EA, Patterson LT, Brookhiser WT, Mah S, Kintner C, Dressler GR. 1998. Differential expression and function of cadherin-6 during renal epithelium development. Development 125:803-812.
9. Cohen HT, Bossone SA, Zhu G, McDonald GA, Sukhatme VP. 1997. Sp1 is a critical regulator of the Wilms' tumor-1 gene. J Biol Chem 272:2901-2913.
10. Denison MS, Nagy SR. 2003. Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals. Annu Rev Pharmacol Toxicol 43:309-334.
11. Duong Van Huyen JP, Amri K, Bélair MF, Vilar J, Merlet-Bénichou C, Bruneval P, et al. 2003. Spatiotemporal distribution of insulin-like growth factor receptors during nephrogenesis in fetuses from normal and diabetic rats. Cell Tissue Res 314(3):367-379.
12. Englert C, Vidal M, Maheswaran S, Ge Y, Ezzell R, Isselbacher K, et al. 1995 Truncated WT1 mutants alter the subnuclear localization of the wild-type protein. Proc Natl Acad Sci USA 92:11960-11964.
13. Everson RB, Randerath E, Santella RM, Avitts TA, Weinstein IB, Randerath K. 1988. Quantitative associations between DNA damage in human placenta and maternal smoking and birth weight. J Natl Cancer Inst 80:567-576.
14. Falahatpisheh MH, Ramos KS. 2003. Ligand-activated Ahr signaling leads to disruption of nephrogenesis and altered Wilms' tumor suppressor mRNA splicing. Oncogene 22:2160-2171.
15. Falkenberg FW, Hildebrand H, Lutte L, Schwengberg S, Henke B, Greshake D, et al. 1996. Urinary antigens as markers of papillary toxicity. I. Identification and characterization of rat kidney papillary antigens with monoclonal antibodies. Arch Toxicol 71(1-2):80-92.
16. Feld S, Hirschberg R. 1996. Growth hormone, the insulin-like growth factor system, and the kidney. Endocr Rev 17:423-480.
17. Fernandez-Salguero P, Pineau T, Hilbert DM, McPhail T, Lee SS, Kimura S, et al. 1995. Immune system impairment and hepatic fibrosis in mice lacking the dioxin-binding Ah receptor. Science 5211:722-726.
18. Hammes A, Guo J-K, Lutsch G, Leheste J-R, Landrock D, Ziegler U, et al. 2001. Two splice variants of the Wilms' tumor 1 gene have distinct functions during sex determination and nephron formation. Cell 106:319-329.
19. Hara M, Yanagihara T, Kihara I. 2001. Urinary podocytes in primary focal segmental glomerulosclerosis. Nephron 89(3):342-347.
20. Hastie ND. 2001. Life, sex, and WT1 isoforms-three amino acids can make all the difference. Cell 106:391-394.
21. Hayden MR, Whaley-Connell A, Sowers JR. 2005. Renal redox stress and remodeling in metabolic syndrome, type 2 diabetes mellitus, and diabetic nephropathy: paying homage to the podocyte. Am J Nephrol 25(6):553-569.
22. Henry EC, Gasiewicz TA. 2003. Agonist but not antagonist ligands induce conformational change in the mouse AHR as detected by partial proteolysis. Mol Pharmacol 63:392-400.
23. Hildebrand H, Rinke M, Schluter G, Bomhard E, Falkenberg FW. 1999. Urinary antigens as markers of papillary toxicity. II: Application of monoclonal antibodies for the determination of papillary antigens in rat urine. Arch Toxicol 73(4-5):233-245.
24. Hosono S, Luo X, Hyink DP, Schnapp LM, Wilson PD, Burrow CR, et al. 1999. WT1 expression induces features of renal epithelial differentiation in mesenchymal fibroblasts. Oncogene 18:417-427.
25. Hricik DE, Chung-Park M, Sedor JR. 1998. Glomerulonephritis. N Engl J Med 339(13):888-899.
26. Iben S, Royer-Pokora B. 1999. Analysis of native WT1 protein from frozen human kidney and Wilms' tumors. Oncogene 18:2533-2536.
27. Karavanov AA, Karavanova I, Perantoni A, Dawid IB. 1998. Expression pattern of the rat Lim-1 homeobox gene suggests a dual role during kidney development. Int J Dev Biol 42:61-66.
28. Kilty C, Doyle S, Hassett B, Manning F. 1998. Glutathione S-transferases as biomarkers of organ damage: applications of rodent and canine GST enzyme immunoassays. Chem Bio Interact 111-112:123-135.
29. Kim YH, Goyal M, Kurnit D, Wharram B, Wiggins J, Holzman L, et al. 2001. Podocyte depletion and glomerulosclerosis have a direct relationship in the PAN-treated rat. Kidney Int 60(3):957-968.
30. Knutti D, Kressler D, Kralli A. 2001. Regulation of the transcriptional coactivator PGC-1 via MAPK-sensitive interaction with a repressor. Proc Natl Acad Sci USA 98:9713-9718.
31. Kreidberg JA, Sariola H, Loring JM, Maeda M, Pelletier J, Housman D, et al. 1993. WT-1 is required for early kidney development. Cell 74:679-691.
32. Lahvis GP, Pyzalski RW, Glover E, Pitot HC, McElwee MK, Bradfield CA. 2005. The AHR is required for developmental closure of the ductus venosus in the neonatal mouse. Mol Pharmacol 67:714-720.
33. Lee TH, Lwu S, Kim J, Pelletier J. 2002. Inhibition of Wilms tumor 1 transactivation by BMZF2, a nevel transcriptional repressor. J Biol Chem 227:44826-44837.
34. Lummus ZL, Henningsen G. 1995. Modulation of T-cell ontogeny by transplacental BaP. Int J Immunopharmacol 17(4):339-350.
35. Lund AK, Goens MB, Kanagy NL, Walker MK. 2003. Cardiac hypertrophy in AHR null mice is correlated with elevated angiotensin II, endothelin-1, and mean arterial blood pressure. Toxicol Appl Pharmacol 193:177-187.
36. Lund AK, Goens MB, Nunez BA, Walker MK. 2006. Characterizing the role of endothelin-1 in the progression of cardiac hypertrophy in AHR (AhR) null mice. Toxicol Appl Pharmacol 212:127-135.
37. MacKenzie KM, Angevine DM. 1981. Infertility in mice exposed in utero to benzo[a]pyrene. Biol Reprod 24:183-191.
38. Mah SP, Saueressig H, Goulding M, Kintner C, Dressler GR. 2000. Kidney development in cadherin-6 mutants: delayed mesenchyme-to-epithelial conversion and loss of nephrons. Dev Biol 223:38-53.
39. Marlowe J, Puga A. 2010. Novel AHR interactions. In: Comprehensive Toxicology, Vol 2 (McQueen CA, Bond J, Ramos K, Lamb J, Guengerich FP, Lawrence D, et al., eds). 2nd ed. Kidlington, UK:Elsevier, 93-115.
40. McMillan BJ, Bradfield CA. 2007. The AHR sans xenobiotics: endogenous function in genetic model systems. Mol Pharmacol 72:487-498.
41. Menke AL, van der Eb AJ, Jochemsen AG. 1998. The Wilms' tumor 1 gene: oncogene or tumor suppressor gene? Int Rev Cytol 181:151-212.
42. Menzie CA, Potocki BB, Santodonato J. 1992. Exposure to carcinogenic PAHs in the environment. Environ Sci Technol 26(7):1278-1284.
43. Moriguchi T, Motohashi H, Hosaya T, Nakajima O, Takahashi S, Ohsako S, et al. 2003. Distinct response to dioxin in an arylhydrocarbon receptor (AHR)-humanized mouse. Proc Natl Acad Sci USA 100:5652-5657.
44. Nanez A, Ramos KS. 2010. Introduction and overview of receptor systems. In: Comprehensive Toxicology, Vol 2 (McQueen CA, Bond J, Ramos K, Lamb J, Guengerich FP, Lawrence D, et al., eds). 2nd ed. Kidlington, UK:Elsevier, 71-80.
45. Nelson E, Goubet-Wiemers C, Guo Y, Jodscheit K. 1999. Maternal passive smoking during pregnancy and fetal developmental toxicity. Part 2: histological changes. Hum Exp Toxicol 18:257-264.
46. Nwagwu MO, Cook A, Langley-Evans SC. 2000. Evidence of progressive deterioration of renal function in rats exposed to a maternal low-protein diet in utero. Br J Nutr 83:79-85.
47. Ohtake F, Baba A, Takada I, Okada M, Iwasaki K, Miki H, et al. 2007. Dioxin receptor is a ligand-dependent E3 ubiquitin ligase. Nature 446:562-566.
48. Pinto-Sietsma S, Mulder J, Janssen W, Hillege H, de Zeeuw D, de Jong P. 2000. Smoking is related to albuminuria and abnormal renal function in nondiabetic persons. Ann Intern Med 133:585-591.
49. Poland A, Palen D, Glover E. 1994. Analysis of the four alleles of the murine AHR. Mol Pharmacol 46:915-921.
50. Rebagliato M, Florey CV, Bolumar F. 1995. Exposure to environmental tobacco smoke in nonsmoking pregnant women in relation to birth weight. Am J Epidemiol 142(5):531-537.
51. Roberts BJ, Whitelaw ML. 1999. Degradation of the basic helix-loop-helix/Per-ARNT-Sim homology domain dioxin receptor via the ubiquitin/proteasome pathway. J Biol Chem 274:36351-36356.
52. Rodriquez JW, Kirlin WG, Wirsiy YG, Matheravidathu S, Hodge TW, Urso P. 1999. Maternal exposure to BaP alters development of T lymphocytes in offspring. Immunopharmacol Immunotoxicol 21(2):379-396.
53. Roquer JM, Figueras F, Botet F, Jimenez R. 1995. Influence on fetal growth of exposure to tobacco smoke during pregnancy. Acta Paediatr 84:118-121.
54. Sanders MW, Fazzi GE, Janssen GMJ, Blanco CE, De Mey JGR. 2005. High sodium intake increases blood pressure and alters renal function in intrauterine growth-retarded rats. Hypertension 46(1):71-75.
55. Sasaki S, Kondo T, Sata F, Saijo Y, Katoh S, Nakajima S, et al. 2006. Maternal smoking during pregnancy and genetic polymorphisms in the Ah receptor, CYP1A1 and GSTM1 affect infant birth size in Japanese subjects. Mol Hum Reprod 12:77-83.
56. Schmidt JV, Su GH-T, Reddy JK, Simon MC, Bradfield CA. 1996. Characterization of a murine Ahr null allele: involvement of the Ah receptor in hepatic growth and development. Proc Natl Acad Sci USA 93:6731-6736.
57. Shawlot W, Behringer RR. 1995. Requirement for Lim1 in head-organizer function. Nature 374:425-430.
58. Song Z, Pollenz RS. 2002. Ligand-dependent and independent modulation of AHR localization, degradation, and gene regulation. Mol Pharmacol 62:806-816.
59. Stark K, Vainio S, Vassileva G, McMahon AP. 1994. Epithelial transformation of metanephric mesenchyme in the developing kidney regulated by Wnt-4. Nature 372:679-683.
60. Vainio SJ, Itäranta PV, Peräsaari JP, Uusitalo MS. 1999. Wnts as kidney tubule inducing factors. Int J Dev Biol 43:419-423.
61. Wang ZY, Qiu QQ, Gurrieri M, Huang J, Deuel TF. 1995. WT1, the Wilm's tumor suppressor gene product, represses transcription through an interactive nuclear protein. Oncogene 10:1243-1247.
62. Wells PG, Kim PM, Laposa RR, Nicol CJ, Parman T, Winn LM. 1997. Oxidative damage in chemical teratogenesis. Mutat Res 396:65-78.
63. Wiggins RC. 2007. The spectrum of podocytopathies: a unifying view of glomerular diseases. Kidney Int 71(12):1205-1214.
64. Winn LM, Wells PG. 1997. Evidence for embryonic prostaglandin H synthase-catalyzed bioactivation and reactive oxygen species-mediated oxidation of cellular macromolecules in phenytoin and benzo[a]pyrene teratogenesis. Free Radic Biol Med. 22(4):607-621.
65. Wolf G, Chen S, Ziyadeh FN. 2005. From the periphery of the glomerular capillary wall toward the center of disease: podocyte injury comes of age in diabetic nephropathy. Diabetes 54(6):1626-1634.
66. Yoshino K, Rubin JS, Higinbotham KG, Üren A, Anest V, Plisov SY, et al. 2001. Secreted Frizzled-related proteins can regulate metanephric development. Mech Dev 102:45-55.
67. Zandi-Nejad K, Luyckx VA, Brenner BM. 2006. Adult hypertension and kidney disease: the role of fetal programming. Hypertension 47(3):502-508.