Differential changes of fat-soluble vitamins and pollutants during lactation in northern elephant seal mother-pup pairs

Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology

Volumn 162, Issue 4, 2012, Pages 323-330

  Debier, Cathy ^a   Crocker, Daniel E ^b   Houser, Dorian S ^b,c   Vanden Berghe, Marie ^a   Fowler, Melinda ^d   Mignolet, Eric ^a   de Tillesse, Tanguy ^e   Rees, Jean François ^a   Thomé, Jean Pierre ^f   Larondelle, Yvan ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b SONOMA STATE UNIVERSITY   (United States)

^c Biomimetica   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e Faune et Biotopes   (Belgium)

^f UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

Biomarkers; DDT; Dynamics; Lactation; PCBs; Seal; Vitamin A; Vitamin E

Indexed keywords

1,1 DICHLORO 2,2 BIS(4 CHLOROPHENYL)ETHANE; 1,1 DICHLORO 2,2 BIS(4 CHLOROPHENYL)ETHYLENE; ALPHA TOCOPHEROL; CHLORPHENOTANE; POLYCHLORINATED BIPHENYL; RETINOL;

ARTICLE; BLOOD SAMPLING; CONTAMINATION; ELEPHANT SEAL; FEMALE; LACTATION; MILK; NONHUMAN; POLLUTANT; SEAL;

MAMMALIA; MIROUNGA ANGUSTIROSTRIS;

EID: 84861532152     PISSN: 10956433     EISSN: 15314332     Source Type: Journal    
DOI: 10.1016/j.cbpa.2012.04.001     Document Type: Article

References (61)

1. Barbas C., Herrera E. Lipid composition and vitamin E content in human colostrum and mature milk. J. Physiol. Biochem. 1998, 54:167-173.
2. Bellovino D., Apreda M., Gragnoli S., Massimi M., Gaetani S. Vitamin A transport: in vitro models for the study of RBP secretion. Mol. Aspects Med. 2003, 24:411-420.
3. Best N.J., Bradshaw C.J.A., Hindell M.A., Nichols P.D. Vertical stratification of fatty acids in the blubber of southern elephant seals (Mirounga leonina): implications for diet analysis. Comp. Biochem. Physiol. A 2003, 134:253-263.
4. Boersma E.R., Offringa P.J., Muskiet F.A., Chase W.M., Simmons I.J. Vitamin E, lipid fractions, and fatty acid composition of colostrum, transitional milk, and mature milk: an international comparative study. Am. J. Clin. Nutr. 1991, 53:1197-1204.
5. Brouwer A., Morse D.C., Lans M.C., Gerlienke Schuur A., Murk A.J., Klasson-Wehler E., Bergman Ã.k., Visser T.J. Interactions of persistent environmental organohalogens with the thyroid hormone system: mechanisms and possible consequences for animal and human health. Toxicol. Ind. Health 1998, 14:59-84.
6. Calderon B., Chauveau-Duriot B., Martin B., Graulet B., Doreau M., Nozière P. Variations in carotenoids, vitamins A and E, and color in cow's plasma and milk during late pregnancy and the first 3 months of lactation. J. Dairy Sci. 2007, 90:2335-2346.
7. Crocker D.E., Williams J.D., Costa D.P., Le Boeuf B.J. Maternal traits and reproductive effort in northern elephant seals. Ecology 2001, 82:3541-3555.
8. Debier C., Kovacs K.M., Lydersen C., Mignolet E., Larondelle Y. Vitamin E, vitamin A contents, fatty acids profiles, and gross composition of harp and hooded seal milk through lactation. Can. J. Zool. 1999, 77:952-958.
9. Debier C., Pomeroy P.P., Baret P.V., Mignolet E., Larondelle Y. Vitamin E status and the dynamics of its transfer between mother and pup during lactation in grey seals (Halichoerus grypus). Can. J. Zool. 2002, 80:727-737.
10. Debier C., Pomeroy P.P., Van Wouwe N., Mignolet E., Baret P.V., Larondelle Y. Dynamics of vitamin A in grey seal (Halichoerus grypus) mothers and pups throughout lactation. Can. J. Zool. 2002, 80:1262-1273.
11. Debier C., Pomeroy P.P., Dupont C., Joiris C., Comblin V., Le Boulenge E., Larondelle Y., Thome J.P. Quantitative dynamics of PCB transfer from mother to pup during lactation in UK grey seals Halichoerus grypus. Mar. Ecol. Prog. Ser. 2003, 247:237-248.
12. Debier C., Pomeroy P.P., Thome J.P., Mignolet E., de Tillesse T., Larondelle Y. An unexpected parallelism between vitamin A and PCBs in seal milk. Aquat. Toxicol. 2004, 68:179-183.
13. Debier C., Larondelle Y. Vitamins A and E: metabolism, roles and transfer to offspring. Br. J. Nutr. 2005, 93:153-174.
14. Debier C., Ylitalo G.M., Weise M., Gulland F., Costa D.P., Le Boeuf B.J., de Tillesse T., Larondelle Y. PCBs and DDT in the serum of juvenile California sea lions: associations with vitamins A and E and thyroid hormones. Environ. Pollut. 2005, 134:323-332.
15. Debier C., Le Bœuf B.J., Ikonomou M.G., de Tillesse T., Larondelle Y., Ross P.S. Polychlorinated biphenyls, dioxins and furans in weaned, free-ranging northern elephant seal pups from central California. USA. Environ. Toxicol. Chem. 2005, 24:629-633.
16. Debier C., Chalon C., Le Boeuf B.J., de Tillesse T., Larondelle Y., Thomé J.-P. Mobilization of PCBs from blubber to blood in northern elephant seals (Mirounga angustirostris) during the post-weaning fast. Aquat. Toxicol. 2006, 80:149-157.
17. Debier C. Vitamin E during pre- and postnatal periods. Vitamins and Hormones 2007, vol. 76:357-373. Elsevier, Amsterdam.
18. Hennig B., Slim R., Toborek M., Robertson L.W. Linoleic acid amplifies polychlorinated biphenyl-mediated dysfunction of endothelial cells. J. Biochem. Mol. Toxicol. 1998, 13:83-91.
19. Käkelä R., Hyvärinen H., Käkelä A. Vitamins A1 (retinol), A2 (3,4-didehydroretinol) and E (α-tocopherol) in the liver and blubber of lacustrine and marine ringed seals (Phoca hispida sp.). Comp. Biochem. Physiol. B 1997, 116:27-33.
20. Käkelä A., Käkela R., Hyvärinen H. Importance of the kidneys in metabolism of vitamins A1 and A2 and their fatty acyl esters in mink feeding on fish-based diets and exposed to Aroclor 1242. Toxicol. Appl. Pharmacol. 2003, 187:118-127.
21. Koopman H.N., Iverson S.J., Gaskin D.E. Stratification and age-related differences in blubber fatty acids of the male harbour porpoise (Phocoena phocoena). J. Comp. Physiol. 1996, 165:628-639.
22. Le Boeuf B.J., Ortiz C.L. Composition of elephant seal milk. J. Mammal. 1977, 58:684-685.
23. Le Boeuf B.J., Giesy J.P., Kannan K., Kajiwara N., Tanabe S., Debier C. Organochloride pesticides in California sea lions revisited. BioMed Central Ecol. 2002, 2(11):8.
24. Letcher R.J., Bustnes J.O., Dietz R., Jenssen B.M., Jørgensen E.H., Sonne C., Verreault J., Vijayan M.M., Gabrielsen G.W. Exposure and effects assessment of persistent organohalogen contaminants in arctic wildlife and fish. Sci. Total. Environ. 2010, 408:2995-3043.
25. Macias C., Schweigert F.J. Changes in the concentrations of carotenoids, vitamin A, alpha-tocopherol and total lipids in human milk throughout early lactation. Ann. Nutr. Metab. 2001, 45:82-85.
26. Martinez S., Barbas C., Herrera E. Uptake of alpha-tocopherol by the mammary gland but not by white adipose tissue is dependent on lipoprotein lipase activity around parturition and during lactation in the rat. Metab. Clin. Exp. 2002, 51:1444-1451.
27. Mos L., Ross P.S. Vitamin A physiology in the precocious harbour seal (Phoca vitulina): a tissue-based biomarker approach. Can. J. Zool. 2002, 80:1511-1519.
28. Mos L., Tabuchi M., Dangerfield N., Jeffries S.J., Koop B.F., Ross P.S. Contaminant-associated disruption of vitamin A and its receptor (retinoic acid receptor [alpha]) in free-ranging harbour seals (Phoca vitulina). Aquat. Toxicol. 2007, 81:319-328.
29. Novák J., Benísek M., Hilscherová K. Disruption of retinoid transport, metabolism and signaling by environmental pollutants. Environ. Int. 2008, 34:898-913.
30. Nyman M., Bergknut M., Fant M.L., Raunio H., Jestoi M., Bengs C., Murk A., Koistinen J., Backman C., Pelkonen O., Tysklind M., Hirvi T., Helle E. Contaminant exposure and effects in Baltic ringed and grey seals as assessed by biomarkers. Mar. Environ. Res. 2003, 55:73-99.
31. Ortiz C.L., Le Boeuf B.J., Costa D.P. Milk intake of elephant seal pups: an index of parental investment. Am. Nat. 1984, 124:416-422.
32. Palace V.P., Klaverkamp J.F., Lockhart W.L., Metner D.O., Muir D.C.G., Brown S.B. Mixed function oxidase enzyme activity and oxidative stress in lake trout (Salvelinus namaycush) exposed to 3,3',4,4',5-pentachlorobiphenyl (PCB-126). Environ. Toxicol. Chem. 1996, 15:955-960.
33. Piantedosi R., Ghyselink N., Blaner W.S., Vogel S. Cellular retinol binding protein type III is needed for retinoid incorporation into milk. J. Biol. Chem. 2005, 280:24286-24292.
34. Pomeroy P.P., Green N., Hall A.J., Walton M., Jones K., Harwood J. Congener-specific exposure of grey seal (Halichoerus grypus) pups to chlorinated biphenyls during lactation. Can. J. Fish. Aquat. Sci. 1996, 53:1526-1534.
35. Raclot T. Selective mobilization of fatty acids from adipose tissue triacylglycerols. Prog. Lipid Res. 2003, 42:257-288.
36. Reijnders P.J.H. Reproductive failure in common seals feeding on fish from polluted coastal waters. Nature 1986, 324:456-457.
37. Rolland R.M. A review of chemically-induced alterations in thyroid and vitamin A status from field studies of wildlife and fish. J. Wildl. Dis. 2000, 615-635.
38. Routti H., Arukwe A., Jenssen B.M., Letcher R.J., Nyman M., Bäckman C., Gabrielsen G.W. Comparative endocrine disruptive effects of contaminants in ringed seals (Phoca hispida) from Svalbard and the Baltic Sea. Comp. Biochem. Physiol. C 2010, 152:306-312.
39. Routti H., Jenssen B.M., Lydersen C., Bäckman C., Arukwe A., Nyman M., Kovacs K.M., Gabrielsen G.W. Hormone, vitamin and contaminant status during the moulting/fasting period in ringed seals (Pusa [Phoca] hispida) from Svalbard. Comp. Biochem. Physiol. A 2010, 155:70-76.
40. Ross P.S. Marine mammals as sentinels in ecological risk assessment. Hum. Ecol. Risk Assess. 2000, 6:29-46.
41. Ross A.C., Pasatiempo A.M.G., Green M.H. Chylomicron margination, lipolysis and vitamin A uptake in the lactating rat mammary gland: implications for milk retinoid content. Exp. Biol. Med. 2004, 229:46-55.
42. Saito M. Polychlorinated biphenyls-induced lipid peroxidation as measured by thiobarbituric acid-reactive substances in liver subcellular fractions of rats. Biochim. Biophys. Acta 1990, 1046:301-308.
43. Schweigert F.J., Stobo W.T., Zucker H. Vitamin A status in the grey seal (Halichoerus grypus) on Sable Island. Int. J. Vitam. Nutr. Res. 1987, 57:239-245.
44. Schweigert F.J., Stobo W.T. Transfer of fat-soluble vitamins and PCBs from mothers to pups in grey seals (Halichoerus grypus). Comp. Biochem. Physiol. C 1994, 109:111-117.
45. Schweigert F.J., Luppertz M., Stobo W.T. Fasting and lactation effect fat-soluble vitamin A and E levels in blood and their distribution in tissue of grey seals (Halichoerus grypus). Comp. Biochem. Physiol. A 2002, 131:901-908.
46. Schweigert F.J., Bathe K., Chen F., Buscher U., Dudenhausen J.W. Effect of the stage of lactation in humans on carotenoid levels in milk, blood plasma and plasma lipoprotein fractions. Eur. J. Nutr. 2004, 43:39-44.
47. Simms W., Ross P.S. Developmental changes in circulatory vitamin A (retinol) and its transport proteins in free-ranging harbour seal (Phoca vitulina) pups. Can. J. Zool. 2000, 78:1862-1868.
48. Simms W., Jeffries S., Ikonomou M., Ross P.S. Contaminant-related disruption of vitamin A dynamics in free-ranging harbor seal (Phoca vitulina) pups from British Columbia, Canada, and Washington State, USA. Environ. Toxicol. Chem. 2000, 19:2844-2849.
49. Slim R., Toborek M., Robertson L.W., Hennig B. Antioxidant protection against PCB-mediated endothelial cell activation. Toxicol. Sci. 1999, 52:232-239.
50. Spector R., Johanson C. Vitamin transport and homeostasis in mammalian brain: focus on vitamins B and E. J. Neurochem. 2007, 103:425-438.
51. Strandberg U., Käkelä A., Lydersen C., Kovacs K.M., Grahl-Nielsen O., Hyvärinen H., Käkelä R. Stratification, composition, and function of marine mammal blubber: the ecology of fatty acids in marine mammals. Physiol. Biochem. Zool. 2008, 81:473-485.
52. Tachikawa M., Okayasu S., Hosoya K. Functional involvement of scavenger receptor class B type I in the uptake of alpha-tocopherol using cultured rat retinal capillary endothelial cells. Mol. Vis. 2007, 13:2041-2047.
53. Takada T., Suzuki H. Molecular mechanisms of membrane transport of vitamin E. Mol. Nutr. Food Res. 2010, 54:616-622.
54. Toborek M., Barger S.W., Mattson M.P., Espandiari P., Robertson L.W., Hennig B. Exposure to polychlorinated biphenyls causes endothelial cell dysfunction. J. Biochem. Toxicol. 1995, 10:219-226.
55. Tsutsumi C., Okuno M., Tannous L., Piantedosi R., Allan M., Goodman D.S., Blaner W.S. Retinoids and retinoid-binding protein expression in rat adipocytes. J. Biol. Chem. 1992, 267:1805-1810.
56. Van Bennekum A.M., Kako Y., Weinstock P.H., Harrison E.H., Deckelbaum R.J., Glodberg I.J., Blaner W.S. Lipoprotein lipase expression level influences tissue clearance of chylomicron retinyl ester. J. Lipid Res. 1999, 40:565-574.
57. Vanden Berghe M., Mat A., Arriola A., Polain S., Stekke V., Thomé J.-P., Gaspart F., Pomeroy P., Larondelle Y., Debier C. Relationships between vitamin A and PCBs in grey seal mothers and pups during lactation. Environ. Pollut. 2010, 158:1570-1575.
58. Wheatley K.E., Nichols P.D., Hindell M.A., Harcourt R.G., Bradshaw C.J.A. Differential mobilization of blubber fatty acids in lactating Weddell seals: evidence for selective use. Physiol. Biochem. Zool. 2008, 81:651-662.
59. Wolkers H., Hammill M.O., van Bavel B. Tissue-specific accumulation and lactational transfer of polychlorinated biphenyls, chlorinated pesticides, and brominated flame retardants in hooded seals (Cistophora cristata) from the Gulf of St. Lawrence: applications for monitoring. Environ. Pollut. 2006, 142:476-486.
60. Ylitalo G.M., Stein J.E., Hom T., Johnson L.L., Tilbury K.L., Hall A.J., Rowles T., Greig D., Lowenstine L.J., Gulland F.M. The role of organochlorines in cancer-associated mortality in California sea lions (Zalophus californianus). Mar. Pollut. Bull. 2005, 50:30-39.
61. Zile M.H. Vitamin A homeostasis endangered by environmental pollutants. Proc. Soc. Exp. Biol. Med. 1992, 141-153.