PKC Activation in Niemann Pick C1 Cells Restores Subcellular Cholesterol Transport

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Tamari, Farshad ^a,b   Chen, Fannie W ^a   Li, Chunlei ^a   Chaudhari, Jagrutiben ^a   Ioannou, Yiannis A ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b KINGSBOROUGH COMMUNITY COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIAZOXIDE; FATTY ACID; ISOENZYME; ISOPROTEIN; PROTEIN KINASE C; PROTEIN KINASE C ALPHA; PROTEIN KINASE C BETA; PROTEIN KINASE C BETA II; PROTEIN KINASE C EPSILON; UNCLASSIFIED DRUG; VIMENTIN; CELL EXTRACT; CHOLESTEROL; RAB PROTEIN; RAB9A PROTEIN, HUMAN; SPHINGOLIPID;

ANIMAL CELL; ARTICLE; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; DRUG TARGETING; ENDOSOME; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME SUBSTRATE; HUMAN; HUMAN CELL; LIPID STORAGE; NIEMANN PICK DISEASE; NONHUMAN; PATHOGENESIS; PHENOTYPE; PROTEIN EXPRESSION; SOLUBILIZATION; ANIMAL; CHO CELL LINE; CRICETULUS; DRUG EFFECTS; ENZYMOLOGY; ESTERIFICATION; HAMSTER; METABOLISM; SOLUBILITY; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; CELL EXTRACTS; CHO CELLS; CHOLESTEROL; CRICETINAE; CRICETULUS; ENZYME ACTIVATION; ESTERIFICATION; FATTY ACIDS; NIEMANN-PICK DISEASE, TYPE C; PHENOTYPE; PROTEIN KINASE C; RAB GTP-BINDING PROTEINS; SOLUBILITY; SPHINGOLIPIDS; VIMENTIN;

EID: 84881585586     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0074169     Document Type: Article

References (37)

1. Mellor H, Parker PJ, (1998) The extended protein kinase C superfamily. Biochem J 332(2):: 281-292. PubMed: 9601053.
2. Azzi A, Boscoboinik D, Hensey C, (1992) The protein kinase C family. Eur J Biochem 208: 547-557. doi:10.1111/j.1432-1033.1992.tb17219.x. PubMed: 1396661.
3. Cloud-Heflin BA, McMasters RA, Osborn MT, Chambers TC, (1996) Expression, subcellular distribution and response to phorbol esters of protein kinase C (PKC) isozymes in drug-sensitive and multidrug-resistant KB cells evidence for altered regulation of PKC-alpha. Eur J Biochem 239: 796-804. doi:10.1111/j.1432-1033.1996.0796u.x. PubMed: 8774728.
4. Mochly-Rosen D, Das K, Grimes KV, (2012) Protein kinase C, an elusive therapeutic target? Nat Rev Drug Discov 11: 937-957. doi:10.1038/nrd3871. PubMed: 23197040.
5. Walter M, Chen FW, Tamari F, Wang R, Ioannou YA, (2009) Endosomal lipid accumulation in NPC1 leads to inhibition of PKC, hypophosphorylation of vimentin and Rab9 entrapment. Biol Cell 101: 141-152. doi:10.1042/BC20070171. PubMed: 18681838.
6. Shen WJ, Zaidi SK, Patel S, Cortez Y, Ueno M, et al. (2012) Ablation of vimentin results in defective steroidogenesis. Endocrinology 153: 3249-3257. doi:10.1210/en.2012-1048. PubMed: 22535769.
7. Styers ML, Kowalczyk AP, Faundez V, (2005) Intermediate filaments and vesicular membrane traffic: the odd couple's first dance? Traffic 6: 359-365. doi:10.1111/j.1600-0854.2005.00286.x. PubMed: 15813746.
8. Perlson E, Hanz S, Ben-Yaakov K, Segal-Ruder Y, Seger R, et al. (2005) Vimentin-dependent spatial translocation of an activated MAP kinase in injured nerve. Neuron 45: 715-726. doi:10.1016/j.neuron.2005.01.023. PubMed: 15748847.
9. Toda M, Kuo CH, Borman SK, Richardson RM, Inoko A, et al. (2012) Evidence that formation of vimentin mitogen-activated protein kinase (MAPK) complex mediates mast cell activation following FcepsilonRI/CC chemokine receptor 1 cross-talk. J Biol Chem 287: 24516-24524. doi:10.1074/jbc.M111.319624. PubMed: 22613718.
10. Ivaska J, Vuoriluoto K, Huovinen T, Izawa I, Inagaki M, et al. (2005) PKCepsilon-mediated phosphorylation of vimentin controls integrin recycling and motility. EMBO J 24: 3834-3845. doi:10.1038/sj.emboj.7600847. PubMed: 16270034.
11. Sarria AJ, Panini SR, Evans RM, (1992) A functional role for vimentin intermediate filaments in the metabolism of lipoprotein-derived cholesterol in human SW-13 cells. J Biol Chem 267: 19455-19463. PubMed: 1527066.
12. Eriksson JE, He T, Trejo-Skalli AV, Härmälä-Braskén AS, Hellman J, et al. (2004) Specific in vivo phosphorylation sites determine the assembly dynamics of vimentin intermediate filaments. J Cell Sci 117: 919-932. doi:10.1242/jcs.00906. PubMed: 14762106.
13. Klymkowsky MW, (1995) Intermediate filament organization, reorganization, and function in the clawed frog Xenopus. Curr Top Dev Biol 31: 455-486. PubMed: 8746673.
14. Mor-Vaknin N, Punturieri A, Sitwala K, Markovitz DM, (2003) Vimentin is secreted by activated macrophages. Nat Cell Biol 5: 59-63. PubMed: 12483219.
15. Mangoura D, Sogos V, Dawson G, (1995) Phorbol esters and PKC signaling regulate proliferation, vimentin cytoskeleton assembly and glutamine synthetase activity of chick embryo cerebrum astrocytes in culture. Brain Res Dev Brain Res 87: 1-11. doi:10.1016/0165-3806(95)00046-G. PubMed: 7554227.
16. Spudich A, Meyer T, Stryer L, (1992) Association of the beta isoform of protein kinase C with vimentin filaments. Cell Motil Cytoskeleton 22: 250-256. doi:10.1002/cm.970220405. PubMed: 1516148.
17. Szalay J, Bruno P, Bhati R, Adjodha J, Schueler D, et al. (2001) Associations of PKC isoforms with the cytoskeleton of B16F10 melanoma cells. J Histochem Cytochem 49: 49-66. doi:10.1177/002215540104900106. PubMed: 11118478.
18. Bertrand F, Veissiere D, Hermelin B, Paul A, Capeau J, et al. (1994) Phosphorylation of vimentin is an intermediate step in protein kinase C-mediated glycoconjugate secretion. Am J Physiol 266: C611-C621. PubMed: 7513122.
19. Walter M, Davies JP, Ioannou YA, (2003) Telomerase immortalization upregulates Rab9 expression and restores LDL cholesterol egress from Niemann-Pick C1 late endosomes. J Lipid Res 44: 243-253. doi:10.1194/jlr.M200230-JLR200. PubMed: 12576506.
20. Disatnik MH, Buraggi G, Mochly-Rosen D, (1994) Localization of protein kinase C isozymes in cardiac myocytes. Exp Cell Res 210: 287-297. doi:10.1006/excr.1994.1041. PubMed: 8299726.
21. Millard EE, Srivastava K, Traub LM, Schaffer JE, Ory DS, (2000) Niemann-pick type C1 (NPC1) overexpression alters cellular cholesterol homeostasis. J Biol Chem 275: 38445-38451. doi:10.1074/jbc.M003180200. PubMed: 10964915.
22. Pentchev PG, Boothe AD, Kruth HS, Weintroub H, Stivers J, et al. (1984) A genetic storage disorder in BALB/C mice with a metabolic block in esterification of exogenous cholesterol. J Biol Chem 259: 5784-5791. PubMed: 6325448.
23. Bolard J, (1986) How do the polyene macrolide antibiotics affect the cellular membrane properties? Biochim Biophys Acta 864: 257-304. doi:10.1016/0304-4157(86)90002-X. PubMed: 3539192.
24. Khan WA, Blobe G, Halpern A, Taylor W, Wetsel WC, et al. (1993) Selective regulation of protein kinase C isoenzymes by oleic acid in human platelets. J Biol Chem 268: 5063-5068. PubMed: 8444883.
25. Kanno T, Yamamoto H, Yaguchi T, Hi R, Mukasa T, et al. (2006) The linoleic acid derivative DCP-LA selectively activates PKC-epsilon, possibly binding to the phosphatidylserine binding site. J Lipid Res 47: 1146-1156. doi:10.1194/jlr.M500329-JLR200. PubMed: 16520488.
26. Tanaka A, Nishizaki T, (2003) The newly synthesized linoleic acid derivative FR236924 induces a long-lasting facilitation of hippocampal neurotransmission by targeting nicotinic acetylcholine receptors. Bioorg Med Chem Lett 13: 1037-1040. doi:10.1016/S0960-894X(03)00089-1 PubMed: 12643906.
27. Chen FW, Gordon RE, Ioannou YA, (2005) NPC1 late endosomes contain elevated levels of non-esterified ('free') fatty acids and an abnormally glycosylated form of the NPC2 protein. Biochem J 390: 549-561. doi:10.1042/BJ20050236. PubMed: 15896196.
28. Nishizuka Y, (1992) Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C. Science 258: 607-614. doi:10.1126/science.1411571. PubMed: 1411571.
29. Kim MY, Kim MJ, Yoon IS, Ahn JH, Lee SH, et al. (2006) Diazoxide acts more as a PKC-epsilon activator, and indirectly activates the mitochondrial K(ATP) channel conferring cardioprotection against hypoxic injury. Br J Pharmacol 149: 1059-1070. PubMed: 17043673.
30. Puri V, Watanabe R, Dominguez M, Sun X, Wheatley CL, et al. (1999) Cholesterol modulates membrane traffic along the endocytic pathway in sphingolipid-storage diseases. Nat Cell Biol 1: 386-388. doi:10.1038/14084. PubMed: 10559968.
31. Goldin E, Roff CF, Miller SP, Rodriguez-Lafrasse C, Vanier MT, et al. (1992) Type C Niemann-Pick disease: a murine model of the lysosomal cholesterol lipidosis accumulates sphingosine and sphinganine in liver. Biochim Biophys Acta 1127: 303-311. doi:10.1016/0005-2760(92)90236-O. PubMed: 1324734.
32. Rodriguez-Lafrasse C, Rousson R, Valla S, Antignac P, Louisot P, et al. (1997) Modulation of protein kinase C by endogenous sphingosine: inhibition of phorbol dibutyrate binding in Niemann-Pick C fibroblasts. Biochem J 325(3):: 787-791. PubMed: 9271101.
33. Leventhal AR, Leslie CC, Tabas I, (2004) Suppression of macrophage eicosanoid synthesis by atherogenic lipoproteins is profoundly affected by cholesterol-fatty acyl esterification and the Niemann-Pick C pathway of lipid trafficking. J Biol Chem 279: 8084-8092. PubMed: 14638686.
34. Garver WS, Hossain GS, Winscott MM, Heidenreich RA, (1999) The Npc1 mutation causes an altered expression of caveolin-1, annexin II and protein kinases and phosphorylation of caveolin-1 and annexin II in murine livers. Biochim Biophys Acta 1453: 193-206. doi:10.1016/S0925-4439(98)00101-X. PubMed: 10036317.
35. Ioannou YA, (2004) Defects in transmembrane proteins. In: SUWeds., FM Platt. Lysosomal disorders of the brain. New York: Oxford University Press. pp. pp. 206-228.
36. Ioannou YA, Zeidner KM, Gordon RE, Desnick RJ, (2001) Fabry disease: preclinical studies demonstrate the effectiveness of alpha-galactosidase A replacement in enzyme-deficient mice. Am J Hum Genet 68: 14-25. doi:10.1086/316953. PubMed: 11115376.
37. Higgins ME, Davies JP, Chen FW, Ioannou YA, (1999) Niemann-Pick C1 is a late endosome-resident protein that transiently associates with lysosomes and the trans-Golgi network. Mol Genet Metab 68: 1-13. doi:10.1006/mgme.1999.2882. PubMed: 10479477.