Abnormal sterols in cholesterol-deficiency diseases cause secretory granule malformation and decreased membrane curvature

Journal of Cell Science

Volumn 119, Issue 9, 2006, Pages 1876-1885

  Gondré Lewis, Marjorie C ^a,b   Petrache, Horia I ^a   Wassif, Christopher A ^a   Harries, Daniel ^a   Parsegian, Adrian ^a   Porter, Forbes D ^a   Loh, Y Peng ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b HOWARD UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Cholesterol; Granule biogenesis; Lathosterolosis; Membrane curvature; Regulated secretory pathway; Smith Lemli Opitz syndrome (SLOS)

Indexed keywords

CHOLESTEROL; LATHOSTEROL; STEROL DERIVATIVE;

ACINAR CELL; ADRENAL GLAND; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ARTIFICIAL MEMBRANE; BIOACCUMULATION; BIOGENESIS; CELL BUDDING; CELL FUNCTION; CELL MEMBRANE; CELL SHAPE; CELL STRUCTURE; CHOLESTEROL SYNTHESIS; CONTROLLED STUDY; HOMOZYGOSITY; HYPOPHYSIS; IN VIVO STUDY; METABOLIC DISORDER; MOUSE; NEWBORN; NONHUMAN; PANCREAS; PRECURSOR; PRIORITY JOURNAL; RIGIDITY; SECRETORY GRANULE; SMITH LEMLI OPITZ SYNDROME;

ANIMALS; CELL MEMBRANE; CELLS, CULTURED; CHOLESTEROL; HUMANS; MICE; MICE, KNOCKOUT; MOLECULAR STRUCTURE; OXIDOREDUCTASES ACTING ON CH-CH GROUP DONORS; PANCREAS; SECRETORY VESICLES; SMITH-LEMLI-OPITZ SYNDROME; STEROLS;

ANIMALIA; EUKARYOTA;

EID: 33744512465     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.02906     Document Type: Article

References (46)

1. Arnaoutova, I., Smith, A. M., Coates, L. C., Sharpe, J. C., Dhanvantari, S., Snell, C. R., Birch, N. P. and Loh, Y. P. (2003). The prohormone processing enzyme PC3 is a lipid raft-associated transmembrane protein. Biochemistry 42, 10445-10455.
2. Bloom, M., Evans, E. and Mouritsen, O. G. (1991). Physical properties of the fluid lipid-bilayer component of cell membranes - a perspective. Q. Rev. Biophys. 24, 293-397.
3. Brunetti-Pierri, N., Corso, G., Rossi, M., Ferrari, P., Balli, F., Rivasi, F., Annunziata, I., Ballabio, A., Russo, A. D., Andria, G. et al. (2002). Lathosterolosis, a novel multiple-malformation/mental retardation syndrome due to deficiency of 3beta-hydroxysteroid-delta5-desaturase. Am. J. Hum. Genet. 71, 952-958.
4. Burgoyne, R. D. and Morgan, A. (2003). Secretory granule exocytosis. Physiol. Rev. 83, 581-632.
5. Cherstvoy, E. D., Lazjuk, G. I., Ostrovskaya, T. I., Shved, I. A., Kravtzova, G. I., Lurie, I. W. and Gerasimovich, A. I. (1984). The Smith-Lemli-Opitz syndrome. A detailed pathological study as a clue to a etiological heterogeneity. Virchows Arch. A Plathol. Anat. Histopathol. 404, 413-425.
6. Christian, A. E., Haynes, M. P., Phillips, M. C. and Rothblat, G. H. (1997). Use of cyclodextrins for manipulating cellular cholesterol content. J. Lipid Res. 38, 2264-2272.
7. Churchward, M. A., Rogasevskaia, T., Hofgen, J., Bau, J. and Coorssen, J. R. (2005). Cholesterol facilitates the native mechanism of Ca2+-triggered membrane fusion. J. Cell Sci. 118, 4833-4848.
8. Dhanvantari, S. and Loh, Y. P. (2000). Lipid raft association of carboxypeptidase E is necessary for its function as a regulated secretory pathway sorting receptor. J. Biol. Chem. 275, 29887-29893.
9. Gondré-Lewis, M. C., McGlynn, R. and Walkley, S. U. (2003). Cholesterol accumulation in NPCI-deficient neurons is ganglioside dependent. Curr. Biol. 13, 1324-1329.
10. Harries, D. and Ben-Shaul, A. (1997). Conformational chain statistics in a model lipid bilayer: comparison between mean field and Monte Carlo calculations. J. Chem. Phys. 106, 1609-1619.
11. Helfrich, W. (1978). Steric interaction of fluid membranes in multilayers systems. Z. Naturforsch. 33, 305A-315A.
12. Henriksen, J., Rowat, A. C. and Ipsen, J. H. (2004). Vesicle fluctuation analysis of the effects of sterols on membrane bending rigidity. Eur. Biophys. J. 33, 732-741.
13. Keller, P. and Simons, K. (1998). Cholesterol is required for surface transport of influenza virus hemagglutinin. J. Cell Biol. 140, 1357-1367.
14. Keller, R. K., Arnold, T. P. and Fliesler, S. J. (2004). Formation of 7-dehydrocholesterol-containing membrane rafts in vitro and in vivo, with relevance to the Smith-Lemli-Opitz syndrome. J. Lipid Res. 45, 347-355.
15. Kelley, R. I. and Hennekam, R. C. (2000). The Smith-Lemli-Opitz syndrome. J. Med. Genet. 37, 321-335.
16. Kohler, H. G. (1983). Brief clinical report: familial neonatally lethal syndrome of hypoplastic left heart, absent pulmonary lobation, polydactyly, and talipes, probably Smith-Lemli-Opitz (RSH) syndrome. Am. J. Med. Genet. 14, 423-428.
17. Krakowiak, P. A., Wassif, C. A., Kratz, L., Cozma, D., Kovarova, M., Harris, G., Grinberg, A., Yang, Y., Hunter, A. G., Tsokos, M. et al. (2003). Lathosterolosis: an inborn error of human and murine cholesterol synthesis due to lathosterol 5-desaturase deficiency. Hum. Mol. Genet. 12, 1631-1641.
18. Kurup, S. and Bhonde, R. R. (2002). Analysis and optimization of nutritional set-up for murine pancreatic acinar cells. Jop 3, 8-15.
19. Lachman, M. F., Wright, Y., Whiteman, D. A., Herson, V. and Greenstein, R. M. (1991). Brief clinical report: a 46,XY phenotypic female with Smith-Lemli-Opitz syndrome. Clin. Genet. 39, 136-141.
20. Loh, Y. P., Maldonado, A., Zhang, C., Tam, W. H. and Cawley, N. (2002). Mechanism of sorting proopiomelanocortin and proenkephalin to the regulated secretory pathway of neuroendocrine cells. Ann. N. Y. Acad. Sci. 971, 416-425.
21. Loh, Y. P., Kim, T., Rodriguez, Y. M. and Cawley, N. X. (2004). Secretory granule biogenesis and neuropeptide sorting to the regulated secretory pathway in neuroendocrine cells. J. Mol. Neurosci. 22, 63-71.
22. Lou, H., Kim, S. K., Zaitsev, E., Snell, C. R., Lu, B. and Loh, Y. P. (2005). Sorting and activity-dependent secretion of BDNF require interaction of a specific motif with the sorting receptor carboxypeptidase e. Neuron 45, 245-255.
23. Martinez, G. V., Dykstra, E. M., Lope-Piedrafita, S. and Brown, M. F. (2004). Lanosterol and cholesterol-induced variations in bilayer elasticity probed by H-2 NMR relaxation. Langmuir 20, 1043-1046.
24. Méléard, P., Gerbeaud, C., Pott, T., Fernandez-Puente, L., Bivas, I., Mitov, M. D., Dufourcrcq, J. and Bothorel, P. (1997). Bending elasticities of model membranes: influences of temperature and sterol content. Biophys. J. 72, 2616-2629.
25. Ness, G. C., Lopez, D., Borrego, O. and Gilbert-Barness, E. (1997). Increased expression of low-density lipoprotein receptors in a Smith-Lemli-Opitz infant with elevated bilirubin levels. Am. J. Med. Genet. 68, 294-299.
26. Ohnishi, H., Samuelson, L. C., Yule, D. I., Ernst, S. A. and Williams, J. A. (1997). Overexpression of Rab3D enhances regulated amylase secretion from pancreatic acini of transgenic mice. J. Clin. Invest. 100, 3044-3052.
27. Petrache, H. I., Gouliaev, N., Tristram-Nagle, S., Zhang, R. T., Suter, R. M. and Nagle, J. F. (1998a). Interbilayer interactions from high-resolution x-ray scattering. Phys. Rev. E 57, 7014-7024.
28. Petrache, H. I., Tristram-Nagle, S. and Nagle, J. F. (1998b). Fluid phase structure of EPC and DMPC bilayers. Chem. Phys. Lipids 95, 83-94.
29. Petrache, H. I., Dodd, S. W. and Brown, M. F. (2000). Area per lipid and acyl length distributions in fluid phosphatidylcholines determined by (2)H NMR spectroscopy. Biophys. J. 79, 3172-3192.
30. Porter, F. D. (2000). RSH/Smith-Lemli-Opitz syndrome: a multiple congenital anomaly/mental retardation syndrome due to an inborn error of cholesterol biosynthesis. Mol. Genet. Metab. 71, 163-174.
31. Rand, P., Fuller, N. L., Gruner, S. M. and Parsegian, V. A. (1990). Membrane curvature, lipid segregation. and structural transitions for phospholipid under dual-solvent stress. Biochemistry 29, 76-87.
32. Rawicz, W., Olbrich, K. C., McIntosh, T., Needham, D. and Evans, E. (2000). Effect of chain length and unsaturation on elasticity of lipid bilayers. Biophys. J. 79, 328-339.
33. Schneider, S. W., Sritharan, K. C., Geibel, J. P., Oberleithner, H. and Jena, B. P. (1997). Surface dynamics in living acinar cells imaged by atomic force microscopy: identification of plasma membrane structures involved in exocytosis. Proc. Natl. Acad. Sci. USA 94, 316-321.
34. Schrader, M. (2004). Membrane targeting in secretion. Subcell. Biochem. 37, 391-421.
35. Seddon, J. M. (1990). Structure of the inverted hexagonal (HII) phase, and non-lamellar phase transitions of lipids. Biochim. Biophys. Acta 1031, 1-69.
36. Thiele, C. and Huttner, W. B. (1998). Protein and lipid sorting from the trans-Golgi network to secretory granules-recent developments. Semin. Cell Dev. Biol. 9, 511-516.
37. Tint, G. S., Irons, M., Elias, E. R., Batta, A. K., Frieden, R., Chen, T. S. and Saten, G.(1994). Defective cholesterol biosynthesis associated with the Smith-Lemli-Opitz syndrome. N. Engl. J. Med. 330, 107-113.
38. Tooze, S. A. (1998). Biogenesis of secretory granules in the trans-Golgi network of neuroendocrine and endocrine cells. Biochim. Biophys. Acta 1404, 231-244.
39. van Meer, G. (1993). Transport and sorting of membrane lipids. Curr. Opin. Cell Biol. 5, 661-673.
40. Wang, C. C., Ng, C. P., Lu, L., Atlashkin, V., Zhang, W., Seet, L. F. and Hong, W. (2004). A role of VAMP8/endobrevin in regulated exocytosis of pancreatic acinar cells. Dev. Cell 7, 359-371.
41. Wang, Y., Thiele, C. and Huttner, W. B. (2000). Cholesterol is required for the formation of regulated and constitutive secretory vesicles from the trans-Golgi network. Traffic 1, 952-962.
42. Wassif, C. A., Zhu, P., Kratz, L., Krakowiak, P. A., Battaile, K. P., Weight, F. F., Grinberg, A., Steiner, R. D., Nwokoro, N. A., Kelley, R. I. et al. (2001). Biochemical, phenotypic and neurophysiological characterization of a genetic mouse model of RSH/Smith-Lemli-Opitz syndrome. Hum. Mol. Genet. 10, 555-564.
43. Wassif, C. A., Vied, D., Tsokos, M., Connor, W. E., Steiner, R. D. and Porter, F. D. (2002). Cholesterol storage defect in RSH/ Smith-Lemli-Opitz syndrome fibroblasts. Mol. Genet. Metab. 75, 325-334.
44. Witsch-Baumagartner, M., Ciara, E., Loffler, J., Menzel, H. J., Seedorf, U., Burn, J., Gillessen-Kaesbach, G., Hoffmann, G. F., Fitzky, B. U., Mundy, H. et al. (2001). Frequency gradients of DHCR7 mutations in patients with Smith-Lemli-Opitz syndrome in Europe: evidence for different origins of common mutations. Eur. J. Hum. Genet. 9, 45-50.
45. Xu, X., Bittman, R., Duportail, G., Heissler, D., Vilcheze, C. and London, E. (2001). Effect of the structure of natural sterols and sphingolipids on the formation of ordered sphingolipid/sterol domains (rafts). Comparison of cholesterol to plant, fungal, and disease-associated sterols and comparison of sphingomyelin, cerebrosides, and ceramide. J. Biol. Chem. 276, 33540-33546.
46. Zhang, C. F., Dhanvantari, S., Lou, H. and Loh, Y. P. (2003). Sorting of carboxypeptidase E to the regulated secretory pathway requires interaction of its transmembrane domain with lipid rafts. Biochem. J. 369, 453-460.