LDL and cAMP cooperate to regulate the functional expression of the LRP in rat ovarian granulosa cells

Journal of Lipid Research

Volumn 47, Issue 11, 2006, Pages 2538-2550

  Azhar, Salman ^a,b   Medicherla, Satyanarayana ^a,c   Shen, Wen Jun ^a   Fujioka, Yoshio ^b   Fong, Loren G ^b,d   Reaven, Eve ^a   Cooper, Allen D ^b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c SCIOS INC   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Adenosine 3 ,5 cyclic monophosphate; Low density lipoprotein; Low density lipoprotein receptor related protein

Indexed keywords

ALPHA 2 MACROGLOBULIN; CHYLOMICRON; CYCLIC AMP; GESTAGEN; LIPOPROTEIN RECEPTOR; LOW DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; N2,O2' DIBUTYRYL ADENOSINE 3',5' CYCLIC MONOPHOSPHATE; VERY LOW DENSITY LIPOPROTEIN;

ANIMAL CELL; ARTICLE; CELL CULTURE; CONTROLLED STUDY; FEMALE; GRANULOSA CELL; HORMONAL REGULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; RAT; STEROIDOGENESIS;

ALPHA-MACROGLOBULINS; ANIMALS; CELLS, CULTURED; CYCLIC AMP; FEMALE; GENE EXPRESSION REGULATION; GRANULOSA CELLS; HUMANS; LIPOPROTEINS, LDL; OVARY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, LDL; SCAVENGER RECEPTORS, CLASS B; STEROIDS;

EID: 33845583493     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M600349-JLR200     Document Type: Article

References (67)

1. Azhar, S., and E. Reaven. 2002. Scavenger receptor class BI and selective cholesteryl ester uptake: partners in the regulation of steroidogenesis. Mol. Cell. Endocrinol. 195: 1-26.
2. Azhar, S., S. Leers-Sucheta, and E. Reaven. 2003. Cholesterol uptake in adrenal and gonadal tissues: the SR-BI and 'selective' pathway connection. Front. Biosci. 8 (Suppl.): 998-1029.
3. Connelly, M. A., and D. L. Williams. 2003. SR-BI and cholesterol uptake into steroidogenic cells. Trends Endocrinol. Metab. 14: 467-472.
4. Rigotti, A., H. E. Miettin, and M. Krieger. 2003. The role of the high-density lipoprotein receptor SR-BI in the lipid metabolism of endocrine and other tissues. Endocr. Rev. 24: 357-387.
5. Reaven, E., L. Tsai, M. Spicher, L. Shilo, M. Philip, A. D. Cooper, and S. Azhar. 1994. Enhanced expression of granulosa cell low density lipoprotein receptor activity in response to in vitro culture conditions. J. Cell. Physiol. 161: 449-462.
6. Medicherla, S., S. Azhar, A. Cooper, and E. Reaven. 1996. Regulation of cholesterol responsive genes in ovary cells: impact of cholesterol delivery systems. Biochemistry. 35: 6243-6250.
7. Hussain, M. M., D. K. Strickland, and A. Bakillah. 1999. The mammalian low-density lipoprotein receptor family. Annu. Rev. Nutr. 19: 141-172.
8. Herz, J., and D. K. Strickland. 2001. LRP: a multifunctional scavenger and signaling receptor. J. Clin. Invest. 108: 779-784.
9. Strickland, D. K., S. L. Gonias, and W. S. Argraves. 2002. Diverse roles for the LDL receptor family. Trends Endocrinol. Metab. 13: 66-74.
10. Bu, G. 2001. The roles of receptor-associated protein (RAP) as a molecular chaperone for members of the LDL receptor family. Int. Rev. Cytol. 209: 70-116.
11. 2-macroglobulin receptor/low density lipoprotein receptor-related protein in human tissues. Cell Tissue Res. 269: 375-382.
12. Kounnas, M. Z., C. C. Haudenschild, D. K. Strickland, and W. S. Argraves. 1994. Immunological localization of glycoprotein 330, low density lipoprotein receptor related protein and 39 kDa receptor associated protein in embryonic mouse tissues. In Vivo. 8: 343-351.
13. 2MR, and the receptor-associated protein (RAP). J. Histochem. Cytochem. 42: 531-542.
14. Watanabe, Y., T. Inaba, H. Shimano, T. Gotoda, K. Yamamoto, H. Mokuno, H. Sato, Y. Yazaki, and N. Yamada. 1994. Induction of LDL receptor-related protein during the differentiation of monocyte-macrophages: possible involvement in the atherosclerotic process. Arterioscler. Thromb. 14: 1000-1006.
15. Hussaini, I. M., J. LaMarre, J. J. Lysiak, L. R. Karns, S. R. VandenBerg, and S. L. Gonias. 1996. Transcriptional regulation of LDL receptor-related protein by IFN-gamma and the antagonistic activity of TGF-beta(1) in the RAW 264.7 macrophage-like cell line. J. Leukoc. Biol. 59: 733-739.
16. 2- macroglobulin receptor and its receptor-associated protein in late stages of cutaneous tumor progression. Cancer Res. 56: 1432-1439.
17. Kancha, R. K., and M. M. Hussain. 1996. Up-regulation of the low density lipoprotein receptor-related protein by dexamethasone in HepG2 cells. Biochim. Biophys. Acta. 1301: 213-220.
18. Misra, U. K., G. Gwadi, M. Gonzalez-Gronow, and S. V. Pizzo. 1999. Coordinate regulation of the alpha (2)-macroglobulin signaling receptor and the low density lipoprotein receptor-related protein/alpha (2)-macroglobulin receptor by insulin. J. Biol. Chem. 274: 25785-25791.
19. Noguchi, T., M. Noguchi, H. Masubuchi, T. Seki, and T. Ariga. 2001. IL-1beta down-regulates tissue-type plasminogen activator by up-regulating low-density lipoprotein receptor-related protein in AML 12 cells. Biochem. Biophys. Res. Commun. 288: 42-48.
20. Jo, I., H. M. Im, H. J. Shin, C. K. Won, M. Jung, S. D. Kim, J. Jeong, and J. S. Ahn. 2002. Serum deprivation increases the expression of low density lipoprotein receptor-related protein in primary cultured rat astrocytes. Biochem. Biophys. Res. Commun. 299: 102-108.
21. Llorente-Cortés, V., M. Otero-Viñas, S. Sánchez, C. Rodríguez, and L. Badimon. 2002. Low-density lipoprotein upregulates low-density lipoprotein receptor-related protein expression in vascular smooth muscle cells: possible involvement of sterol regulatory element binding protein-2-dependent mechanism. Circulation. 106: 3104-3110.
22. Gauthier, A., G. Vassiliou, F. Benoist, and R. McPherson. 2003. Adipocyte low density lipoprotein receptor-related gene expression and function is regulated by peroxisome proliferator-activated receptor gamma. J. Biol. Chem. 278: 11945-11953.
23. Hollborn, M., G. Birkenmeier, A. Saalbach, I. Iandiev, A. Reichenbach, P. Wiedemann, and L. Kohen. 2004. Expression of LRP1 in retinal pigment epithelial cells and its regulation by growth factors. Invest. Ophthalmol. Vis. Sci. 45: 2033-2038.
24. Kim, C., and N. D. Vaziri. 2005. Down-regulation of hepatic LDL receptor-related protein (LRP) in chronic renal failure. Kidney Int. 67: 1028-1032.
25. Kim, S., C. M. Kim, and N. D. Vaziri. 2005. Upregulation of hepatic LDL receptor-related protein in nephritic syndrome: response to statin therapy. Am. J. Physiol. Endocrinol. Metab. 288: E813-E817.
26. Beisiegel, U., W. Weber, G. Ihrke, J. Herz, and K. K. Stanley. 1989. The LDL-receptor-related protein, LRP, is an apolipoprotein E-binding protein. Nature. 341: 162-164.
27. Kowal, R. C., J. Herz, K. H. Weisgraber, R. W. Mahley, M. S. Brown, and J. L. Goldstein. 1990. Opposing effects of apolipoproteins E and C on lipoprotein binding to low density lipoprotein receptor-related protein. J. Biol. Chem. 265: 10771-10779.
28. Kowal, R. C., J. Herz, J. L. Goldstein, V. Esser, and M. S. Brown. 1989. Low density lipoprotein receptor-related protein mediates uptake cholesteryl esters derived from apoprotein E-enriched lipoproteins. Proc. Natl. Acad. Sci. USA. 86: 5810-5814.
29. Havel, R. J. 1998. Receptor and non-receptor mediated uptake of chylomicron remnants by the liver. Atherosclerosis. 141 (Suppl.): 1-7.
30. Mahley, R. W., and Z. S. Ji. 1999. Remnant lipoprotein metabolism: key pathways involving cell-surface heparin sulfate proteoglycans and lipoprotein E. J. Lipid Res. 40: 1-16.
31. Yu, K. C., and A. D. Cooper. 2001. Postprandial lipoproteins and atherosclerosis. Front. Biosci. 6: D332-D354.
32. Azhar, S., L. Tsai, and E. Reaven. 1990. Uptake and utilization of lipoprotein cholesteryl esters by rat granulosa cells. Biochim. Biophys. Acta. 1047: 148-160.
33. Reaven, E., L. Tsai, and S. Azhar. 1995. Cholesterol uptake by the 'selective' pathway of ovarian granulosa cells: early intracellular events. J. Lipid Res. 36: 1602-1617.
34. Reaven, E., L. Tsai, and S. Azhar. 1996. Intracellular events in the "selective" transport of lipoprotein-derived cholesteryl esters. J. Biol. Chem. 271: 16208-16217.
35. Azhar, S., A. Nomoto, S. Leers-Sucheta, and E. Reaven. 1998. Simultaneous induction of an HDL receptor protein (SR-BI) and the selective uptake of HDL-cholesteryl esters in a physiologically relevant steroidogenic cell model. J. Lipid Res. 39: 1616-1628.
36. 2-macroglobulin receptor. J. Biol. Chem. 266: 21232-21238.
37. Fong, L. G., E. Bonney, J. C. Kosek, and A. D. Cooper. 1989. Immunohistochemical localization of low density lipoprotein receptors in adrenal gland, liver, and intestine. J. Clin. Invest. 84: 847-856.
38. Bu, G., E. A. Maksymovitch, J. M. Nerbonne, and A. L. Schwartz. 1994. Expression and function of the low density lipoprotein receptor-related protein (LRP) in mammalian central neurons. J. Biol. Chem. 269: 18521-18528.
39. Hansen, M. B., S. E. Nielsen, and K. Berg. 1989. Re-examination and further development of a precise and rapid dye method for measuring cell growth/cell kill. J. Immunol. Methods. 119: 203-210.
40. Reaven, E., X-Y. Shi, and S. Azhar. 1990. Interaction of lipoproteins with isolated ovary plasma membranes. J. Biol. Chem. 265: 19100-19111.
41. 2-macroglobulin receptor in chylomicron remnant removal in the mouse in vivo. J. Biol. Chem. 268: 15804-15811.
42. de Faria, E., L. G. Fong, M. Komaromy, and A. D. Cooper. 1996. Relative roles of the LDL receptor, the LDL receptor-like protein, and hepatic lipase in chylomicron remnant removal by the liver. J. Lipid Res. 37: 197-209.
43. 2- macroglobulin. J. Biol. Chem. 256: 8134-8139.
44. Harada, K., W-J. Shen, S. Patel, V. Natu, J. Wang, J. Osuga, S. Ishibashi, and F. Kraemer. 2003. Resistance to high fat diet-induced obesity associated with altered expression of adipose specific genes in hormone-sensitive lipase deficient mice. Am. J. Physiol. Endocrinol. Metab. 285: E1182-E1195.
45. West, D. C., A. Sattar, and S. Kumar. 1985. A simplified in situ solubilization procedure for the determination of DNA and cell number in tissue cultured mammalian cells. Anal. Biochem. 147: 289-295.
46. Markwell, M. A. K., S. M. Haas, L. L. Bieber, and N. E. Tolbert. 1978. A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal. Biochem. 87: 206-210.
47. Peterson, G. L. 1977. A simplification of the protein assay method of Lowry et al which is more generally applicable. Anal. Biochem. 83: 346-356.
48. Tercyak, A. M. 1991. Determination of cholesterol and cholesterol esters. J. Nutr. Biochem. 2: 281-292.
49. Brown, M. S., and J. L. Goldstein. 1986. A receptor-mediated pathway for cholesterol homeostasis. Science. 232: 34-47.
50. Horton, J. D., J. L. Goldstein, and M. S. Brown. 2002. SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J. Clin. Invest. 109: 1125-1131.
51. May, P., J. Herz, and H. H. Bock. 2005. Molecular mechanisms of lipoprotein receptor signaling. Cell. Mol. Life Sci. 62: 2325-2338.
52. Attardi, B., and S. J. Winters. 1993. Decay of follicle-stimulating hormone-beta messenger RNA in the presence of transcription inhibitors and/or inhibin, activin, or follistatin. Mol. Endocrinol. 7: 668-680.
53. Tano, M., T. Minegishi, K. Nakamura, S. Karino, Y. Ibuki, and K. Miyamoto. 1997. Transcription and post-transcriptional regulation of FSH receptor in rat granulosa cells by cyclic AMP and activin. J. Endocrinol. 153: 465-473.
54. Rohlman, A., M. Gotthardt, R. E. Hammer, and J. Herz. 1998. Inducible inactivation of hepatic LRP gene Cre-mediated recombination confirms role of LRP in clearance of chylomicron remnants. J. Clin. Invest. 101: 689-695.
55. Beisiegel, U. 1998. Lipoprotein metabolism. Eur. Heart J. 19 (Suppl. A): 20-23.
56. Ji, Z. S., H. L. Dichek, R. D. Miranda, and R. W. Mahley. 1997. Heparan sulfate proteoglycans participate in hepatic lipase and apolipoprotein E-mediated binding and uptake of plasma lipoproteins, including high density lipoproteins. J. Biol. Chem. 272: 31285-31292.
57. Reaven, E., Y. Lua, A. Nomoto, R. Temel, D. L. Williams, D. R. van der Westhuyzen, and S. Azhar. 1999. The selective pathway and a high-density lipoprotein receptor (SR-BI) in ovarian granulosa cells of the mouse. Biochim. Biophys. Acta. 1436: 565-576.
58. Stocco, D. L. 2000. Intramitochondrial cholesterol transfer. Biochim. Biophys. Acta. 1486: 184-197.
59. Argov, N., and D. Sklan. 2004. Expression of mRNA of lipoprotein receptor related protein 8, low density lipoprotein receptor, and very low density lipoprotein receptor in bovine ovarian cells during follicular development and corpus luteum formation and regression. Mol. Reprod. Dev. 68: 169-175.
60. Fayad, T., V. Lévesque, J. Sirois, D. W. Silversides, and J. G. Lussier. 2004. Gene expression profiling of differentially expressed genes in granulosa cells of bovine dominant follicles using suppression subtractive hybridization. Biol. Reprod. 70: 523-533.
61. Herz, J., and R. V. Fareese, Jr. 1999. The LDL receptor gene family, apolipoprotein B and cholesterol receptor family. J. Nutr. 129 (Suppl.): 473-475.
62. Kutt, H., J. Herz, and K. K. Stanley. 1989. Structure of the low-density lipoprotein receptor-related protein (LRP) promoter. Biochim. Biophys. Acta. 1009: 229-236.
63. Gaeta, B. A., I. Borthwick, and K. K. Stanley. 1994. The 5′-flanking region of the alpha 2MR/LRP gene contains an enhancer-like cluster of SP1 binding sites. Biochim. Biophys. Acta. 1219: 307-313.
64. Swarnakar, S., J. Beers, D. K. Strickland, S. Azhar, and D. L. Williams. 2001. The apolipoprotein E-dependent low density lipoprotein cholesteryl ester selective uptake pathway in murine adrenocortical cells involves chondroitin sulfate proteoglycans and an alpha 2-macroglobulin receptor. J. Biol. Chem. 276: 21121-21128.
65. Vassiliou, G., F. Benoist, P. Lau, G. N. Kavaslar, and R. McPherson. 2001. The low density lipoprotein receptor-related protein contributes to selective uptake of high density lipoprotein cholesteryl esters by SW872 liposarcoma cells and primary human adipocytes. J. Biol. Chem. 276: 48823-48830.
66. Zhu, H., Y. Takahashi, W. Xu, H. Kawajiri, T. Murakami, M. Yamamoto, S. Iseki, T. Iwassaki, H. Hattori, and T. Yoshimoto. 2003. Low density lipoprotein receptor-related protein-mediated membrane translocation of 12/15-lipoxygenase is required for oxidation of low density lipoprotein by macrophages. J. Biol. Chem. 278: 13350-13355.
67. Wilsie, L. C., and R. A. Orlando. 2003. The low density lipoprotein receptor-related protein complexes with cell surface heparan sulfate proteoglycans to regulate proteoglycan-mediated lipoprotein catabolism. J. Biol. Chem. 278: 15758-15764.