Transgenerational inheritance of increased fat depot size, stem cell reprogramming, and hepatic steatosis elicited by prenatal exposure to the obesogen tributyltin in mice

Environmental Health Perspectives

Volumn 121, Issue 3, 2013, Pages 359-366

  Chamorro García, Raquel ^a   Sahu, Margaret ^a   Abbey, Rachelle J ^a   Laude, Jhyme ^a   Pham, Nhieu ^a   Blumberg, Bruce ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Adipogenesis; Endocrine disruption; MSCs; NAFLD; Nonalcoholic fatty liver disease; Obesogen; PPAR ; TBT; Transgenerational; Tributyltin

Indexed keywords

ACYL COENZYME A OXIDASE; ALKALINE PHOSPHATASE; FATTY ACID BINDING PROTEIN 4; FATTY ACID SYNTHASE; FATTY ACID TRANSPORTER; GLYCEROL KINASE; LIPOPROTEIN LIPASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA 2; ROSIGLITAZONE; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; TRIBUTYLTIN; ZINC FINGER PROTEIN;

ADIPOCYTE; ADIPOGENESIS; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CELL ISOLATION; CONTROLLED STUDY; DNA ISOLATION; FATTY LIVER; FEMALE; GENE EXPRESSION; GERM CELL; HISTOLOGY; INBREEDING; INHERITANCE; LIPID STORAGE; MALE; MESENCHYMAL STEM CELL; NONALCOHOLIC FATTY LIVER; NONHUMAN; PRENATAL DRUG EXPOSURE; PRIORITY JOURNAL; PROGENY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WHITE ADIPOSE TISSUE;

ADIPOCYTES; ADIPOSE TISSUE; ANIMALS; CELL LINEAGE; DRINKING WATER; FATTY LIVER; FEMALE; MALE; MICE; MICE, INBRED C57BL; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STEM CELLS; TRIALKYLTIN COMPOUNDS;

EID: 84874625478     PISSN: 00916765     EISSN: 15529924     Source Type: Journal    
DOI: 10.1289/ehp.1205701     Document Type: Article

References (73)

1. Abdelmegeed MA, Yoo SH, Henderson LE, Gonzalez FJ, Woodcroft KJ, Song BJ. 2011. PPARα expression protects male mice from high fat-induced nonalcoholic fatty liver. J Nutr 141:603-610.
2. Airaksinen R, Rantakokko P, Turunen AW, Vartiainen T, VuorinenPJ, Lappalainen A, etal. 2010. Organotin intake through fish consumption in finland. Environ Res 110:544-547.
3. Anway MD, Cupp AS, Uzumcu M, Skinner MK. 2005. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308:1466-1469.
4. Anway MD, Rekow SS, Skinner MK. 2008. Transgenerational epigenetic programming of the embryonic testis transcriptome. Genomics 91:30-40.
5. Anway MD, Skinner MK. 2006. Epigenetic transgenerational actions of endocrine disruptors. Endocrinology 147 (6 suppl):S43-S49.
6. Barker DJ. 2007. The origins of the developmental origins theory. J Intern Med 261:412-417.
7. Beresford JN, Bennett JH, Devlin C, Leboy PS, Owen ME. 1992. Evidence for an inverse relationship between the differentiation of adipocytic and osteogenic cells in rat marrow stromal cell cultures. J Cell Sci 102(pt 2):341-351.
8. Blatt J, Van Le L, Weiner T, Sailer S. 2003. Ovarian carcinoma in an adolescent with transgenerational exposure to diethylstilbestrol. J Pediatr Hematol Oncol 25:635-636.
9. Braun JE, Severson DL. 1992. Regulation of the synthesis, processing and translocation of lipoprotein lipase. Biochem J 287(pt 2):337-347.
10. Burris TP, Pelton PD, Zhou L, Osborne MC, Cryan E, DemarestKT. 1999. A novel method for analysis of nuclear receptor function at natural promoters: peroxisome proliferator-activated receptor γ agonist actions on aP2 gene expression detected using branched DNA messenger RNA quantitation. Mol Endocrinol 13:410-417.
11. Cawley J, Meyerhoefer C. 2012. The medical care costs of obesity: an instrumental variables approach. J Health Econ 31:219-230.
12. Chamorro-García R, Kirchner S, Li X, Janesick A, Casey SC, ChowC, etal. 2012. Bisphenol A diglycidyl ether induces adipogenic differentiation of multipotent stromal stem cells through a peroxisome proliferator-activated receptor gamma-independent mechanism. Environ Health Perspect 120:984-989.
13. Danielzik S, Langnase K, Mast M, Spethmann C, Muller MJ. 2002. Impact of parental BMI on the manifestation of overweight 5-7 year old children. Eur J Nutr 41:132-138.
14. de Ferranti S, Mozaffarian D. 2008. The perfect storm: obesity, adipocyte dysfunction, and metabolic consequences. Clin Chem 54:945-955.
15. Diamanti-Kandarakis E, Bourguignon JP, Giudice LC, HauserR, Prins GS, Soto AM, etal. 2009. Endocrine-disrupting chemi-cals: an Endocrine Society scientific statement. Endocr Rev 30:293-342.
16. Flegal KM, Carroll MD, Ogden CL, Curtin LR. 2010. Prevalence and trends in obesity among US adults, 1999-2008. JAMA 303:235-241.
17. Fristachi A, Xu Y, Rice G, Impellitteri CA, Carlson-Lynch H, LittleJC. 2009. Using probabilistic modeling to evaluate human exposure to organotin in drinking water transported by polyvinyl chloride pipe. Risk Anal 29:1615-1628.
18. Garruti G, Cotecchia S, Giampetruzzi F, Giorgino F, Giorgino R. 2008. Neuroendocrine deregulation of food intake, adipose tissue and the gastrointestinal system in obesity and metabolic syndrome. J Gastrointestin Liver Dis 17:193-198.
19. Gastaldelli A, Cusi K, Pettiti M, Hardies J, Miyazaki Y, BerriaR, etal. 2007. Relationship between hepatic/visceral fat and hepatic insulin resistance in nondiabetic and type 2 diabetic subjects. Gastroenterology 133:496-506.
20. Gimble JM, Zvonic S, Floyd ZE, Kassem M, Nuttall ME. 2006. Playing with bone and fat. J Cell Biochem 98:251-266.
21. Godfrey KM, Sheppard A, Gluckman PD, Lillycrop KA, BurdgeGC, McLean C, etal. 2011. Epigenetic gene promoter methylation at birth is associated with child's later adiposity. Diabetes 60:1528-1534.
22. Goncalves CR, Cunha RW, Barros DM, Martinez PE. 2010. Effects of prenatal and postnatal exposure to a low dose of bisphenol A on behavior and memory in rats. Environ Toxicol Pharmacol 30:195-201.
23. Grün F, Watanabe H, Zamanian Z, Maeda L, Arima K, Cubacha R, et al. 2006. Endocrine-disrupting organotin compounds are potent inducers of adipogenesis in vertebrates. Mol Endocrinol 20:2141-2155.
24. Gupta RK, Arany Z, Seale P, Mepani RJ, Ye L, Conroe HM, et al. 2010. Transcriptional control of preadipocyte determination by Zfp423. Nature 464:619-623.
25. Hall AM, Brunt EM, Chen Z, Viswakarma N, Reddy JK, WolinsNE, etal. 2009. Dynamic and differential regulation of proteins that coat lipid droplets in fatty liver dystrophic mice. J Lipid Res 51:554-563.
26. Heindel JJ. 2011. The obesogen hypothesis of obesity: overview and human evidence. In: Obesity Before Birth: Maternal and Prenatal Influences on the Offspring (Lustig RH, ed). New York:Springer Verlag, 355-366.
27. Herbert A. 2008. The fat tail of obesity as told by the genome. Curr Opin Clin Nutr Metab Care 11:366-370.
28. Hill JO, Peters JC. 1998. Environmental contributions to the obesity epidemic. Science 280:1371-1374.
29. Ibrahimi A, Teboul L, Gaillard D, Amri EZ, Ailhaud G, Young P, etal. 1994. Evidence for a common mechanism of action for fatty acids and thiazolidinedione antidiabetic agents on gene expression in preadipose cells. Mol Pharmacol 46:1070-1076.
30. Janesick A, Blumberg B. 2011. Endocrine disrupting chemicals and the developmental programming of adipogenesis and obesity. Birth Defects Res C Embryo Today 93:34-50.
31. Jirtle RL, Skinner MK. 2007. Environmental epigenomics and disease susceptibility. Nat Rev Genet 8:253-262.
32. Kanayama T, Kobayashi N, Mamiya S, Nakanishi T, NishikawaJ. 2005. Organotin compounds promote adipocyte differentiation as agonists of the peroxisome proliferator-activated receptor γ/retinoid X receptor pathway. Mol Pharmacol 67:766-774.
33. Kannan K, Senthilkumar K, Giesy JP. 1999. Occurrence of butyltin compounds in human blood. Environ Sci Technol 33:1776-1779.
34. Kannan K, Takahashi S, Fujiwara N, Mizukawa H, TanabeS. 2010. Organotin compounds, including butyltins and octyltins, in house dust from Albany, New York, USA. Arch Environ Contam Toxicol 58:901-907.
35. Kanno J, Aisaki K, Igarashi K, Nakatsu N, Ono A, KodamaY, etal. 2006. "Per cell" normalization method for mRNA measurement by quantitative PCR and microarrays. BMC Genomics 7:64; doi:10.1186/1471-2164-7-64 [Online 29March 2006].
36. Kirchner S, Kieu T, Chow C, Casey S, Blumberg B. 2010. Prenatal exposure to the environmental obesogen tributyltin pre-disposes multipotent stem cells to become adipocytes. Mol Endocrinol 24:526-539.
37. Klimentidis YC, Beasley TM, Lin HY, Murati G, Glass GE, GuytonM, et al. 2011. Canaries in the coal mine: a cross-species analysis of the plurality of obesity epidemics. Proc Biol Sci 278:1626-1632.
38. Koebnick C, Smith N, Coleman KJ, Getahun D, Reynolds K, QuinnVP, etal. 2010. Prevalence of extreme obesity in a multiethnic cohort of children and adolescents. J Pediatr 157:26-31.
39. La Merrill M, Birnbaum LS. 2011. Childhood obesity and environmental chemicals. Mt Sinai J Med 78:22-48.
40. Li X, Pham HT, Janesick AS, Blumberg B. 2012. Triflumizole is an obesogen in mice that acts through peroxisome proliferator activated receptor gamma (PPARγ). Environ Health Perspect 120:1720-1726.
41. Li X, Ycaza J, Blumberg B. 2011. The environmental obesogen tributyltin chloride acts via peroxisome proliferator activated receptor gamma to induce adipogenesis in murine 3T3-L1 preadipocytes. J Steroid Biochem Mol Biol 127:9-15.
42. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402-408.
43. Lusis AJ, Attie AD, Reue K. 2008. Metabolic syndrome: from epidemiology to systems biology. Nat Rev Genet 9:819-830.
44. Manikkam M, Guerrero-Bosagna C, Tracey R, Haque MM, Skinner MK. 2012. Transgenerational actions of environmental compounds on reproductive disease and identification of epigenetic biomarkers of ancestral exposures. PLoS One 7:e31901; doi:10.1371/journal.pone.0031901 [Online 28 February 2012].
45. McCormick DP, Sarpong K, Jordan L, Ray LA, Jain S. 2010. Infant obesity: are we ready to make this diagnosis? J Pediatr157:15-19.
46. Mencin AA, Lavine JE. 2011. Nonalcoholic fatty liver disease in children. Curr Opin Clin Nutr Metab Care 14:151-157.
47. Newbold RR, Padilla-Banks E, Jefferson WN. 2009. Environmental estrogens and obesity. Mol Cell Endocrinol 304:84-89.
48. Nilsson E, Larsen G, Manikkam M, Guerrero-Bosagna C, Savenkova MI, Skinner MK. 2012. Environmentally induced epigenetic transgenerational inheritance of ovarian disease. PLoS One 7:e36129; doi:10.1371/journal.pone.0036129 [Online 3 May 2012].
49. Paulauskis JD, Sul HS. 1989. Hormonal regulation of mouse fatty acid synthase gene transcription in liver. J Biol Chem 264:574-577.
50. Perseghin G. 2011. Lipids in the wrong place: visceral fat and nonalcoholic steatohepatitis. Diabetes Care 34(suppl 2):S367-S370.
51. Pettinelli P, Videla LA. 2011. Up-regulation of PPAR-γ mRNA expression in the liver of obese patients: an additional reinforcing lipogenic mechanism to SREBP-1c induction. J Clin Endocrinol Metab 96:1424-1430.
52. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, DouglasR, Mosca JD, etal. 1999. Multilineage potential of adult human mesenchymal stem cells. Science 284:143-147.
53. Power C, Jefferis BJ. 2002. Fetal environment and subsequent obesity: a study of maternal smoking. Int J Epidemiol 31:413-419.
54. Power C, Lake JK, Cole TJ. 1997. Body mass index and height from childhood to adulthood in the 1958 British born cohort. Am J Clin Nutr 66:1094-1101.
55. Rantakokko P, Turunen A, Verkasalo PK, Kiviranta H, Mannisto S, Vartiainen T. 2008. Blood levels of organotin compounds and their relation to fish consumption in Finland. Sci Total Environ 399:90-95.
56. Reaven GM. 1993. Role of insulin resistance in human disease (syndromeX): an expanded definition. Annu Rev Med 44:121-131.
57. Reddy JK, Rao MS. 2006. Lipid metabolism and liver inflammation. II. Fatty liver disease and fatty acid oxidation. Am J Physiol Gastrointest Liver Physiol 290:G852-G858.
58. Rippe JM, Hess S. 1998. The role of physical activity in the prevention and management of obesity. J Am Diet Assoc 98:S31-S38.
59. Rozen S, Skaletsky H. 2000. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365-386.
60. Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671-675.
61. Skinner MK. 2008. What is an epigenetic transgenerational phenotype? F3 or F2. Reprod Toxicol 25:2-6.
62. Skinner MK. 2011a. Environmental epigenetic transgenerational inheritance and somatic epigenetic mitotic stability. Epigenetics 6:838-842.
63. Skinner MK. 2011b. Role of epigenetics in developmental biology and transgenerational inheritance. Birth Defects Res C Embryo Today 93:51-55.
64. Sul HS, Smas C, Mei B, Zhou L. 2000. Function of pref-1 as an inhibitor of adipocyte differentiation. Int J Obes Relat Metab Disord 24(suppl 4):S15-S19.
65. Takada I, Kouzmenko AP, Kato S. 2009. Wnt and PPARγ signaling in osteoblastogenesis and adipogenesis. Nat Rev Rheumatol 5:442-447.
66. Tang-Peronard JL, Andersen HR, Jensen TK, Heitmann BL. 2011. Endocrine-disrupting chemicals and obesity development in humans: a review. Obes Rev 12:622-636.
67. Taveras EM, Rifas-Shiman SL, Belfort MB, Kleinman KP, OkenE, Gillman MW. 2009. Weight status in the first 6months of life and obesity at 3 years of age. Pediatrics 123:1177-1183.
68. Tontonoz P, Spiegelman BM. 2008. Fat and beyond: the diverse biology of PPARγ. Annu Rev Biochem 77:289-312.
69. Vos JG, De Klerk A, Krajnc EI, Van Loveren H, Rozing J. 1990. Immunotoxicity of bis(tri-n-butyltin)oxide in the rat: effects on thymus-dependent immunity and on nonspecific resistance following long-term exposure in young versus aged rats. Toxicol Appl Pharmacol 105:144-155.
70. Widhalm K, Ghods E. 2010. Nonalcoholic fatty liver disease: a challenge for pediatricians. Int J Obes (Lond) 34:1451-1467.
71. Wolstenholme JT, Edwards M, Shetty SR, Gatewood JD, TaylorJA, Rissman EF, etal. 2012. Gestational exposure to bisphenol A produces transgenerational changes in behaviors and gene expression. Endocrinology 153:3828-3838.
72. Zambrano E, Martinez-Samayoa PM, Bautista CJ, Deas M, GuillenL, Rodriguez-Gonzalez GL, etal. 2005. Sex differences in transgenerational alterations of growth and metabolism in progeny (F2) of female offspring (F1) of rats fed a low protein diet during pregnancy and lactation. JPhysiol 566:225-236.
73. Zuo Z, Chen S, Wu T, Zhang J, Su Y, Chen Y, etal. 2011. Tributyltin causes obesity and hepatic steatosis in male mice. Environ Toxicol 26:79-85.