Prenatal ethanol exposure induces the osteoarthritis-like phenotype in female adult offspring rats with a post-weaning high-fat diet and its intrauterine programming mechanisms of cholesterol metabolism

Toxicology Letters

Volumn 238, Issue 2, 2015, Pages 117-125

  Ni, Qubo ^a,d   Wang, Linlong ^a   Wu, Yunpeng ^a   Shen, Lang ^b   Qin, Jun ^a   Liu, Yansong ^a   Magdalou, Jacques ^c   Chen, Liaobin ^a,d   Wang, Hui ^b,d  

^a ZHONGNAN HOSPITAL OF WUHAN UNIVERSITY   (China)

^b WUHAN UNIVERSITY   (China)

^c UNIVERSITÉ DE LORRAINE   (France)

^d HUBEI PROVINCIAL KEY LABORATORY OF DEVELOPMENTALLY ORIGINATED DISEASE   (China)

Author keywords

Ethanol; Intrauterine growth retardation; Intrauterine programming alteration; Osteoarthritis; Serum cholesterol

Indexed keywords

ABC TRANSPORTER A1; ALCOHOL; CHOLESTEROL; COLLAGENASE 3; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LIVER X RECEPTOR; LOW DENSITY LIPOPROTEIN CHOLESTEROL; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; SOMATOMEDIN C; STROMELYSIN; ABCA1 PROTEIN, RAT; CHOLESTEROL INTAKE; INSULIN-LIKE GROWTH FACTOR-1, RAT; MATRIX METALLOPROTEINASE; ORPHAN NUCLEAR RECEPTOR;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ARTICULAR CARTILAGE; BODY WEIGHT; CARTILAGE CELL; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL METABOLISM; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; EXPERIMENTAL MODEL; FEMALE; FETUS; GENE EXPRESSION; GROWTH RATE; HISTOLOGY; INTRAUTERINE GROWTH RETARDATION; LIPID DIET; NONHUMAN; OSTEOARTHRITIS; PHENOTYPE; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; RAT; TIBIA; WEANING; ADVERSE EFFECTS; AGE; ANIMAL; CARTILAGE; CHEMICALLY INDUCED; CHOLESTEROL INTAKE; DRUG EFFECTS; METABOLISM; PREGNANCY; WISTAR RAT;

RATTUS;

AGE FACTORS; ANIMALS; ATP BINDING CASSETTE TRANSPORTER 1; BODY WEIGHT; CARTILAGE; CHOLESTEROL, DIETARY; CHONDROCYTES; DIET, HIGH-FAT; ETHANOL; FEMALE; FETAL GROWTH RETARDATION; INSULIN-LIKE GROWTH FACTOR I; MATRIX METALLOPROTEINASES; ORPHAN NUCLEAR RECEPTORS; OSTEOARTHRITIS; PHENOTYPE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS, WISTAR; TIBIA;

EID: 84940179460     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2015.07.017     Document Type: Article

References (55)

1. Agrogiannis G.D., Sifakis S., Patsouris E.S., Konstantinidou A.E. Insulin-like growth factors in embryonic and fetal growth and skeletal development (review). Mol. Med. Rep. 2014, 10:579-584.
2. Al-Arfaj A.S. Radiographic osteoarthritis and serum cholesterol. Saudi Med. J. 2003, 24:745-747.
3. Alfadhli E. Cholesterol deposition around small joints of the hands in familial hypercholesterolemia mimicking "Bouchard's and Heberden's nodes" of osteoarthritis. Intern. Med. 2010, 49:1675-1676.
4. Boyan B.D., Tosi L., Coutts R., Enoka R., Hart D.A., Nicolella D.P., Berkley K., Sluka K., Kwoh K., O'Connor M.I., Kohrt W. Sex differences in osteoarthritis of the knee. J. Am. Acad. Orthop. Surg. 2012, 20:668-669.
5. Brunner A.M., Henn C.M., Drewniak E.I., Lesieur-Brooks A., Machan J., Crisco J.J., Ehrlich M.G. High dietary fat and the development of osteoarthritis in a rabbit model. Osteoarthritis Cartilage 2012, 20:584-592.
6. Burr D.B., Radin E.L. Microfractures and microcracks in subchondral bone: are they relevant to osteoarthrosis?. Rheum. Dis. Clin. North Am. 2003, 29:675-685.
7. Carames B., Kiosses W.B., Akasaki Y., Brinson D.C., Eap W., Koziol J., Lotz M.K. Glucosamine activates autophagy in vitro and in vivo. Arthritis Rheum. 2013, 65:1843-1852.
8. Carbone D.L., Zuloaga D.G., Hiroi R., Foradori C.D., Legare M.E., Handa R.J. Prenatal dexamethasone exposure potentiates diet-induced hepatosteatosis and decreases plasma IGF-I in a sex-specific fashion. Endocrinology 2012, 153:295-306.
9. Chen L., Nyomba B.L. Effects of prenatal alcohol exposure on glucose tolerance in the rat offspring. Metabolism 2003, 52:454-462.
10. Cicuttini F.M., Baker J.R., Spector T.D. The association of obesity with osteoarthritis of the hand and knee in women: a twin study. J. Rheumatol. 1996, 23:1221-1226.
11. Endres M., Toso L., Roberson R., Park J., Abebe D., Poggi S., Spong C.Y. Prevention of alcohol-induced developmental delays and learning abnormalities in a model of fetal alcohol syndrome. Am. J. Obstet. Gynecol 2005, 193:1028-1034.
12. Engelbregt M.J., van Weissenbruch M.M., Popp-Snijders C., Lips P., Delemarre-van de Waal H.A. Body mass index, body composition, and leptin at onset of puberty in male and female rats after intrauterine growth retardation and after early postnatal food restriction. Pediatr. Res. 2001, 50:474-478.
13. Fitzgerald M.L., Moore K.J., Freeman M.W. Nuclear hormone receptors and cholesterol trafficking: the orphans find a new home. J. Mol. Med. 2002, 80:271-281.
14. Forsyth C.B., Cole A., Murphy G., Bienias J.L., Im H.J., Loeser R.F. Increased matrix metalloproteinase-13 production with aging by human articular chondrocytes in response to catabolic stimuli. J. Gerontol. A: Biol. Sci. Med. Sci. 2005, 60:1118-1124.
15. Gkretsi V., Simopoulou T., Tsezou A. Lipid metabolism and osteoarthritis: lessons from atherosclerosis. Prog. lipid Res. 2011, 50:133-140.
16. Griffin T.M., Huebner J.L., Kraus V.B., Yan Z., Guilak F. Induction of osteoarthritis and metabolic inflammation by a very high-fat diet in mice: effects of short-term exercise. Arthritis Rheum. 2012, 64:443-453.
17. Grotle M., Hagen K.B., Natvig B., Dahl F.A., Kvien T.K. Obesity and osteoarthritis in knee, hip and/or hand: an epidemiological study in the general population with 10 years follow-up. BMC musculoskelet. Disord. 2008, 9:132.
18. Hart D.J., Doyle D.V., Spector T.D. Association between metabolic factors and knee osteoarthritis in women: the Chingford Study. J. Rheumatol. 1995, 22:1118-1123.
19. Iliopoulos D., Malizos K.N., Oikonomou P., Tsezou A. Integrative microRNA and proteomic approaches identify novel osteoarthritis genes and their collaborative metabolic and inflammatory networks. PLoS ONE 2008, 3:e3740.
20. Kajantie E. Early-life events. Effects on aging. Hormones 2008, 7:101-113.
21. Katz J.D., Agrawal S., Velasquez M. Getting to the heart of the matter: osteoarthritis takes its place as part of the metabolic syndrome. Curr. Opin. Rheumatol. 2010, 22:512-519.
22. Kim S.P., Ha J.M., Yun S.J., Kim E.K., Chung S.W., Hong K.W., Kim C.D., Bae S.S. Transcriptional activation of peroxisome proliferator-activated receptor-gamma requires activation of both protein kinase A and Akt during adipocyte differentiation. Biochem. Biophys. Res. Commun. 2010, 399:55-59.
23. Las Heras F., Gahunia H.K., Pritzker K.P. Articular cartilage development: a molecular perspective. Orthop. Clin. North Am. 2012, 43:155-171.
24. Lawrence R.C., Felson D.T., Helmick C.G., Arnold L.M., Choi H., Deyo R.A., Gabriel S., Hirsch R., Hochberg M.C., Hunder G.G., Jordan J.M., Katz J.N., Kremers H.M., Wolfe F., National Arthritis Data W. Estimates of the prevalence of arthritis and other rheumatic conditions in the United States. Part II. Arthritis Rheum. 2008, 58:26-35.
25. Liang G., Chen M., Pan X.L., Zheng J., Wang H. Ethanol-induced inhibition of fetal hypothalamic-pituitary-adrenal axis due to prenatal overexposure to maternal glucocorticoid in mice. Exp. Toxicol. Pathol. 2011, 63:607-611.
26. Mankin H.J., Dorfman H., Lippiello L., Zarins A. Biochemical and metabolic abnormalities in articular cartilage from osteo-arthritic human hips. II. Correlation of morphology with biochemical and metabolic data. J. Bone Joint Surg. Am. 1971, 53:523-537.
27. Meaney M.J., Szyf M., Seckl J.R. Epigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health. Trends Mol. Med. 2007, 13:269-277.
28. Morrison J.L., Duffield J.A., Muhlhausler B.S., Gentili S., McMillen I.C. Fetal growth restriction, catch-up growth and the early origins of insulin resistance and visceral obesity. Pediatr. Nephrol. 2010, 25:669-677.
29. Nammi S., Dembele K., Nyomba B.L. Increased 11beta-hydroxysteroid dehydrogenase type-1 and hexose-6-phosphate dehydrogenase in liver and adipose tissue of rat offspring exposed to alcohol in utero. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 292:R1101-R1109.
30. Neuhold L.A., Killar L., Zhao W., Sung M.L., Warner L., Kulik J., Turner J., Wu W., Billinghurst C., Meijers T., Poole A.R., Babij P., DeGennaro L.J. Postnatal expression in hyaline cartilage of constitutively active human collagenase-3 (MMP-13) induces osteoarthritis in mice. J. Clin. Invest. 2001, 107:35-44.
31. O'Conor C.J., Griffin T.M., Liedtke W., Guilak F. Increased susceptibility of Trpv4-deficient mice to obesity and obesity-induced osteoarthritis with very high-fat diet. Ann. Rheum. Dis. 2013, 72:300-304.
32. Oliveria S.A., Felson D.T., Cirillo P.A., Reed J.I., Walker A.M. Body weight, body mass index, and incident symptomatic osteoarthritis of the hand, hip, and knee. Epidemiology 1999, 10:161-166.
33. Price M.D., Herndon J.H. Gender differences in osteoarthritis. Menopause 2009, 16:624-625.
34. Rai A.J., Kamath R.M., Gerald W., Fleisher M. Analytical validation of the GeXP analyzer and design of a workflow for cancer-biomarker discovery using multiplexed gene-expression profiling. Anal. Bioanal. Chem. 2009, 393:1505-1511.
35. Sayer A.A., Poole J., Cox V., Kuh D., Hardy R., Wadsworth M., Cooper C. Weight from birth to 53 years: a longitudinal study of the influence on clinical hand osteoarthritis. Arthritis Rheum. 2003, 48:1030-1033.
36. Shen J., Li J., Wang B., Jin H., Wang M., Zhang Y., Yang Y., Im H.J., O'Keefe R., Chen D. Deletion of the transforming growth factor beta receptor type II gene in articular chondrocytes leads to a progressive osteoarthritis-like phenotype in mice. Arthritis Rheum. 2013, 65:3107-3119.
37. Shen L., Liu Z., Gong J., Zhang L., Wang L., Magdalou J., Chen L., Wang H. Prenatal ethanol exposure programs an increased susceptibility of non-alcoholic fatty liver disease in female adult offspring rats. Toxicol. Appl. Pharmacol. 2014, 274:263-273.
38. Silberberg R., Aufdermaur M., Hasler M. Ultrastructural changes in articular chondrocytes of mice fed a lard-enriched diet. Anat. Rec. 1970, 166:447-467.
39. Simpson M.E., Duggal S., Keiver K. Prenatal ethanol exposure has differential effects on fetal growth and skeletal ossification. Bone 2005, 36:521-532.
40. Sowers M., Karvonen-Gutierrez C.A., Palmieri-Smith R., Jacobson J.A., Jiang Y., Ashton-Miller J.A. Knee osteoarthritis in obese women with cardiometabolic clustering. Arthritis Rheum. 2009, 61:1328-1336.
41. Staal B., Williams B.O., Beier F., Vande Woude G.F., Zhang Y.W. Cartilage-specific deletion of Mig-6 results in osteoarthritis-like disorder with excessive articular chondrocyte proliferation. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:2590-2595.
42. Sturmer T., Sun Y., Sauerland S., Zeissig I., Gunther K.P., Puhl W., Brenner H. Serum cholesterol and osteoarthritis. The baseline examination of the Ulm Osteoarthritis Study. J. Rheumatol. 1998, 25:1827-1832.
43. Tabas I. Free cholesterol-induced cytotoxicity a possible contributing factor to macrophage foam cell necrosis in advanced atherosclerotic lesions. Trends Cardiovasc. Med. 1997, 7:256-263.
44. Tan Y., Liu J., Deng Y., Cao H., Xu D., Cu F., Lei Y., Magdalou J., Wu M., Chen L., Wang H. Caffeine-induced fetal rat over-exposure to maternal glucocorticoid and histone methylation of liver IGF-1 might cause skeletal growth retardation. Toxicol. Lett. 2012, 214:279-287.
45. Tosh D.N., Fu Q., Callaway C.W., McKnight R.A., McMillen I.C., Ross M.G., Lane R.H., Desai M. Epigenetics of programmed obesity: alteration in IUGR rat hepatic IGF1 mRNA expression and histone structure in rapid vs. delayed postnatal catch-up growth. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 299:G1023-G1029.
46. Tsezou A., Iliopoulos D., Malizos K.N., Simopoulou T. Impaired expression of genes regulating cholesterol efflux in human osteoarthritic chondrocytes. J. Orthop. Res. 2010, 28:1033-1039.
47. Valsamakis G., Kanaka-Gantenbein C., Malamitsi-Puchner A., Mastorakos G. Causes of intrauterine growth restriction and the postnatal development of the metabolic syndrome. Ann. N.Y. Acad. Sci. 2006, 1092:138-147.
48. van der Sluijs J.A., Geesink R.G., van der Linden A.J., Bulstra S.K., Kuyer R., Drukker J. The reliability of the Mankin score for osteoarthritis. J. Orthop. Res 1992, 10:58-61.
49. Veje K., Hyllested J.L., Ostergaard K. Osteoarthritis. Pathogenesis, clinical features and treatment. Ugeskr. Laeger 2002, 164:3173-3179.
50. Wang L., Shen L., Ping J., Zhang L., Liu Z., Wu Y., Liu Y., Huang H., Chen L., Wang H. Intrauterine metabolic programming alteration increased susceptibility to non-alcoholic adult fatty liver disease in prenatal caffeine-exposed rat offspring. Toxicol. Lett. 2014, 224:311-318.
51. Welberg L.A., Seckl J.R. Prenatal stress, glucocorticoids and the programming of the brain. J. Neuroendocrinol. 2001, 13:113-128.
52. Wu Q., Kim K.O., Sampson E.R., Chen D., Awad H., O'Brien T., Puzas J.E., Drissi H., Schwarz E.M., O'Keefe R.J., Zuscik M.J., Rosier R.N. Induction of an osteoarthritis-like phenotype and degradation of phosphorylated Smad3 by Smurf2 in transgenic mice. Arthritis Rheum. 2008, 58:3132-3144.
53. Xia L.P., Shen L., Kou H., Zhang B.J., Zhang L., Wu Y., Li X.J., Xiong J., Yu Y., Wang H. Prenatal ethanol exposure enhances the susceptibility to metabolic syndrome in offspring rats by HPA axis-associated neuroendocrine metabolic programming. Toxicol. Lett. 2014, 226:98-105.
54. Zanotti I., Favari E., Bernini F. Cellular cholesterol efflux pathways: impact on intracellular lipid trafficking and methodological considerations. Curr. Pharm. Biotechnol. 2012, 13:292-302.
55. Zhuo Q., Yang W., Chen J., Wang Y. Metabolic syndrome meets osteoarthritis. Nat. Rev. Rheumatol. 2012, 8:729-737.