Characteristics and Functional Relevance of Apolipoprotein-A1 and Cholesterol Binding in Mammary Gland Tissues and Epithelial Cells

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Ontsouka, Edgar Corneille ^a   Huang, Xiao ^a   Stieger, Bruno ^a,b   Albrecht, Christiane ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN A1; CHOLESTEROL; PROBUCOL;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BREAST EPITHELIUM; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; COW; DISSOCIATION CONSTANT; MAMMARY GLAND; MEMBRANE VESICLE; NONHUMAN;

ANIMALS; ANTICHOLESTEREMIC AGENTS; APOLIPOPROTEIN A-I; ATP BINDING CASSETTE TRANSPORTER 1; BIOLOGICAL TRANSPORT; CATTLE; CELL LINE; CELL MEMBRANE; CELLS, CULTURED; CHOLESTEROL; EPITHELIAL CELLS; FEMALE; HUMANS; IODINE RADIOISOTOPES; KINETICS; MAMMARY GLANDS, ANIMAL; MICROSCOPY, ELECTRON, TRANSMISSION; PROBUCOL; PROTEIN BINDING; TRANSPORT VESICLES; TRITIUM;

EID: 84881184124     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0070407     Document Type: Article

References (49)

1. Rochow N, Möller S, Fusch G, Drogies T, Fusch C, (2010) Levels of lipids in preterm infants fed breast milk. Clin Nutr 29: 94-99. doi:10.1016/j.clnu.2009.07.002. PubMed: 19666201.
2. Rudnicka AR, Owen CG, Strachan DP, (2007) The effect of breastfeeding on cardiorespiratory risk factors in adult life. Pediatrics 119: e1107-1115. PubMed: 17473082.
3. Albrecht C, Huang X, Ontsouka EC, (In press) Cholesterol transporters in lactating and non-lactating human mammary tissue. In Dietary and nutritional aspects of human breast milk. Wageningen Academic Publishers.
4. Ohlsson L, (2010) Dairy products and plasma cholesterol levels. Foods Nutr Res 54([MedlinePgn:]) PubMed: 20806084.
5. Turck D, (2011) [Childhood diet and cardiovascular risk factors]. Bull Acad Natl Med 195: 487-498. PubMed: 22292299.
6. Nikitina L, Wenger F, Baumann M, Surbek D, Körner M, et al. (2011) Expression and localization pattern of ABCA1 in diverse human placental primary cells and tissues. Placenta 32: 420-430. doi:10.1016/j.placenta.2011.03.003. PubMed: 21501868.
7. Yamamoto S, Tanigawa H, Li X, Komaru Y, Billheimer JT, et al. (2011) Pharmacologic suppression of hepatic ATP-binding cassette transporter 1 activity in mice reduces high-density lipoprotein cholesterol levels but promotes reverse cholesterol transport. Circulation 124: 1382-1390. doi:10.1161/CIRCULATIONAHA.110.009704. PubMed: 21859969.
8. Lee J, Shirk A, Oram JF, Lee SP, Kuver R, (2002) Polarized cholesterol and phospholipid efflux in cultured gall-bladder epithelial cells: evidence for an ABCA1-mediated pathway. Biochem J 364: 475-484. doi:10.1042/BJ20011493. PubMed: 12023891.
9. Nagao K, Takahashi K, Azuma Y, Takada M, Kimura Y, et al. (2012) ATP hydrolysis-dependent conformational changes in the extracellular domain of ABCA1 are associated with apoA-I binding. J Lipid Res 53: 126-136. doi:10.1194/jlr.M019976. PubMed: 22028339.
10. Wang N, Tall AR, (2003) Regulation and mechanisms of ATP-binding cassette transporter A1-mediated cellular cholesterol efflux. Arterioscler Thromb Vasc Biol 23: 1178-1184. doi:10.1161/01.ATV.0000075912.83860.26. PubMed: 12738681.
11. Hassan HH, Denis M, Lee DY, Iatan I, Nyholt D, et al. (2007) Identification of an ABCA1-dependent phospholipid-rich plasma membrane apolipoprotein A-I binding site for nascent HDL formation: implications for current models of HDL biogenesis. J Lipid Res 48: 2428-2442. doi:10.1194/jlr.M700206-JLR200. PubMed: 17656736.
12. Vedhachalam C, Ghering AB, Davidson WS, Lund-Katz S, Rothblat GH, et al. (2007) ABCA1-induced cell surface binding sites for ApoA-I. Arterioscler Thromb Vasc Biol 27: 1603-1609. doi:10.1161/ATVBAHA.107.145789. PubMed: 17478755.
13. Iatan I, Bailey D, Ruel I, Hafiane A, Campbell S, et al. (2011) Membrane microdomains modulate oligomeric ABCA1 function: impact on apoAI-mediated lipid removal and phosphatidylcholine biosynthesis. J Lipid Res 52: 2043-2055. doi:10.1194/jlr.M016196. PubMed: 21846716.
14. Mendez AJ, Lin G, Wade DP, Lawn RM, Oram JF, (2001) Membrane lipid domains distinct from cholesterol/sphingomyelin-rich rafts are involved in the ABCA1-mediated lipid secretory pathway. J Biol Chem 276: 3158-3166. doi:10.1074/jbc.M007717200. PubMed: 11073951.
15. Orlowski S, Coméra C, Tercé F, Collet X, (2007) Lipid rafts: dream or reality for cholesterol transporters? Eur Biophys J 36: 869-885. doi:10.1007/s00249-007-0193-8. PubMed: 17576551.
16. Bodzioch M, Orsó E, Klucken J, Langmann T, Böttcher A, et al. (1999) The gene encoding ATP-binding cassette transporter 1 is mutated in Tangier disease. Nat Genet 22: 347-351. doi:10.1038/11914. PubMed: 10431237.
17. Brooks-Wilson A, Marcil M, Clee SM, Zhang LH, Roomp K, et al. (1999) Mutations in ABC1 in Tangier disease and familial high-density lipoprotein deficiency. Nat Genet 22: 336-345. doi:10.1038/11905. PubMed: 10431236.
18. Yvan-Charvet L, Ranalletta M, Wang N, Han S, Terasaka N, et al. (2007) Combined deficiency of ABCA1 and ABCG1 promotes foam cell accumulation and accelerates atherosclerosis in mice. J Clin Invest 117: 3900-3908. PubMed: 17992262.
19. Francone OL, Royer L, Boucher G, Haghpassand M, Freeman A, et al. (2005) Increased cholesterol deposition, expression of scavenger receptors, and response to chemotactic factors in Abca1-deficient macrophages. Arterioscler Thromb Vasc Biol 25: 1198-1205. doi:10.1161/01.ATV.0000166522.69552.99. PubMed: 15831807.
20. Oram JF, Heinecke JW, (2005) ATP-binding cassette transporter A1: a cell cholesterol exporter that protects against cardiovascular disease. Physiol Rev 85: 1343-1372. doi:10.1152/physrev.00005.2005. PubMed: 16183915.
21. Mani O, Körner M, Ontsouka CE, Sorensen MT, Sejrsen K, et al. (2011) Identification of ABCA1 and ABCG1 in milk fat globules and mammary cells--implications for milk cholesterol secretion. J Dairy Sci 94: 1265-1276. doi:10.3168/jds.2010-3521. PubMed: 21338792.
22. Schimanski S, Wild PJ, Treeck O, Horn F, Sigruener A, et al. (2010) Expression of the lipid transporters ABCA3 and ABCA1 is diminished in human breast cancer tissue. Horm Metab Res 42: 102-109. doi:10.1055/s-0029-1241859. PubMed: 19902402.
23. Mani O, Körner M, Sorensen MT, Sejrsen K, Wotzkow C, et al. (2010) Expression, localization, and functional model of cholesterol transporters in lactating and nonlactating mammary tissues of murine, bovine, and human origin. Am J Physiol Regul Integr Comp Physiol 299: R642-R654. doi:10.1152/ajpregu.00723.2009. PubMed: 20445153.
24. Mani O, Sorensen MT, Sejrsen K, Bruckmaier RM, Albrecht C, (2009) Differential expression and localization of lipid transporters in the bovine mammary gland during the pregnancy-lactation cycle. J Dairy Sci 92: 3744-3756. doi:10.3168/jds.2009-2063. PubMed: 19620656.
25. Fong BY, Norris CS, MacGibbon AKH, (2007) Protein and lipid composition of bovine milk-fat-globule membrane. Int Dairy J 17: 275-288. doi:10.1016/j.idairyj.2006.05.004.
26. Reinhardt TA, Lippolis JD, (2006) Bovine milk fat globule membrane proteome. J Dairy Res 73: 406-416. doi:10.1017/S0022029906001889. PubMed: 16834814.
27. Wang Y, Baumrucker CR, (2010) Retinoids, retinoid analogs, and lactoferrin interact and differentially affect cell viability of 2 bovine mammary cell types in vitro. Domest Anim Endocrinol 39: 10-20. doi:10.1016/j.domaniend.2009.12.001. PubMed: 20434866.
28. Carron J, Morel C, Hammon HM, Blum JW, (2005) Ontogenetic development of mRNA levels and binding sites of hepatic beta-adrenergic receptors in cattle. Domest Anim Endocrinol 28: 320-330. doi:10.1016/j.domaniend.2004.12.002. PubMed: 15760672.
29. Ontsouka EC, Bruckmaier RM, Steiner A, Blum JW, Meylan M, (2007) Messenger RNA levels and binding sites of muscarinic acetylcholine receptors in gastrointestinal muscle layers from healthy dairy cows. J Recept Signal Transduct Res 27: 147-166. doi:10.1080/10799890701417741. PubMed: 17613726.
30. Ontsouka EC, Niederberger M, Steiner A, Bruckmaier RM, Meylan M, (2010) Binding sites of muscarinic and adrenergic receptors in gastrointestinal tissues of dairy cows suffering from left displacement of the abomasum. Vet J 186: 328-337. doi:10.1016/j.tvjl.2009.08.029. PubMed: 19796972.
31. Lin PH, Selinfreund R, Wakshull E, Wharton W, (1987) Rapid and efficient purification of plasma membrane from cultured cells: characterization of epidermal growth factor binding. Biochemistry 26: 731-736. doi:10.1021/bi00377a012. PubMed: 3567146.
32. Schenkman JB, Cinti DL, (1978) Preparation of microsomes with calcium. Methods Enzymol 52: 83-89. doi:10.1016/S0076-6879(78)52008-9. PubMed: 672658.
33. Kamath SA, Rubin E, (1972) Interaction of calcium with microsomes: a modified method for the rapid isolation of rat liver microsomes. Biochem Biophys Res Commun 49: 52-59. doi:10.1016/0006-291X(72)90008-3. PubMed: 4342728.
34. Mühlfeld C, Rothen-Rutishauser B, Vanhecke D, Blank F, Gehr P, et al. (2007) Visualization and quantitative analysis of nanoparticles in the respiratory tract by transmission electron microscopy. Part Fibres Toxicol 4: 11. doi:10.1186/1743-8977-4-11. PubMed: 17996124.
35. Greenwood FC, Hunter WM, (1963) Preparation of 131i-Labelled Human Growth Hormone of High Specific Radioactivity. Biochem J 89: 114-123& PubMed: 14097352.
36. Osborne JC Jr., Schaefer EJ, Powell GM, Lee NS, Zech LA, (1984) Molecular properties of radioiodinated apolipoprotein A-I. J Biol Chem 259: 347-353. PubMed: 6423628.
37. Favari E, Zanotti I, Zimetti F, Ronda N, Bernini F, et al. (2004) Probucol inhibits ABCA1-mediated cellular lipid efflux. Arterioscler Thromb Vasc Biol 24: 2345-2350. doi:10.1161/01.ATV.0000148706.15947.8a. PubMed: 15514211.
38. Wu CA, Tsujita M, Hayashi M, Yokoyama S, (2004) Probucol inactivates ABCA1 in the plasma membrane with respect to its mediation of apolipoprotein binding and high density lipoprotein assembly and to its proteolytic degradation. J Biol Chem 279: 30168-30174. doi:10.1074/jbc.M403765200. PubMed: 15140889.
39. Baumrucker CR, Deemer KP, Walsh R, Riss TL, Akers RM, (1988) Primary culture of bovine mammary acini on a collagen matrix. Tissue Cell 20: 541-554. doi:10.1016/0040-8166(88)90056-0. PubMed: 3238687.
40. Low H, Hoang A, Sviridov D, (2012) Cholesterol efflux assay. J Vis Exp: pp. e3810. PubMed: 22414908.
41. Vaziri ND, Yuan J, Norris K, (2013) Role of urea in intestinal barrier dysfunction and disruption of epithelial tight junction in chronic kidney disease. Am J Nephrol 37: 1-6. doi:10.1159/000345969. PubMed: 23258127.
42. Hidalgo IJ, Raub TJ, Borchardt RT, (1989) Characterization of the human colon carcinoma cell line (Caco-2) as a model system for intestinal epithelial permeability. Gastroenterology 96: 736-749. PubMed: 2914637.
43. Yoo JW, Kim YS, Lee SH, Lee MK, Roh HJ, et al. (2003) Serially passaged human nasal epithelial cell monolayer for in vitro drug transport studies. Pharmacol Res 20: 1690-1696. doi:10.1023/A:1026112107100. PubMed: 14620527.
44. Fitzgerald ML, Morris AL, Rhee JS, Andersson LP, Mendez AJ, et al. (2002) Naturally occurring mutations in the largest extracellular loops of ABCA1 can disrupt its direct interaction with apolipoprotein A-I. J Biol Chem 277: 33178-33187. doi:10.1074/jbc.M204996200. PubMed: 12084722.
45. Shepherd J, Gotto AM Jr., Taunton OD, Caslake MJ, Farish E, (1977) The in vitro interaction of human apolipoprotein A-I and high density lipoproteins. Biochim Biophys Acta 489: 486-501. doi:10.1016/0005-2760(77)90169-2. PubMed: 22350.
46. Fitzgerald ML, Morris AL, Chroni A, Mendez AJ, Zannis VI, et al. (2004) ABCA1 and amphipathic apolipoproteins form high-affinity molecular complexes required for cholesterol efflux. J Lipid Res 45: 287-294. PubMed: 14617740.
47. Tsujita M, Wu CA, Abe-Dohmae S, Usui S, Okazaki M, et al. (2005) On the hepatic mechanism of HDL assembly by the ABCA1/apoA-I pathway. J Lipid Res 46: 154-162. PubMed: 15520446.
48. Patterson BW, Lee AM, (1986) Self-association and phospholipid binding properties of iodinated apolipoprotein A-I. Biochemistry 25: 4953-4957. doi:10.1021/bi00365a035. PubMed: 3094578.
49. Sankaranarayanan S, Kellner-Weibel G, de la Llera-Moya M, Phillips MC, Asztalos BF, et al. (2011) A sensitive assay for ABCA1-mediated cholesterol efflux using BODIPY-cholesterol. J Lipid Res 52: 2332-2340. doi:10.1194/jlr.D018051. PubMed: 21957199.