Lysosomal and mitochondrial liaisons in Niemann-Pick disease

Frontiers in Physiology

Volumn 8, Issue NOV, 2017, Pages

  Torres, Sandra ^a,b   Balboa, Elisa ^c   Zanlungo, Silvana ^c   Enrich, Carlos ^d   Garcia Ruiz, Carmen ^a,b,e   Fernandez Checa, Jose C ^a,b,e  

^a CSIC   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^d UNIVERSITY OF BARCELONA   (Spain)

^e Southern California Research Center for ALPD and Cirrhosis   (United States)

Author keywords

Acid sphingomyelinase; Cholesterol; Intracellular trafficking; Lysosomal disorders; Lysosomes; Mitochondria; Sphingolipids

Indexed keywords

BIOACCUMULATION; CELL MIGRATION; CHOLESTEROL TRANSPORT; DETERIORATION; DISEASE COURSE; DISEASE SEVERITY; ENDOLYSOSOME; ENDOPLASMIC RETICULUM; HOMEOSTASIS; HUMAN; INNER MITOCHONDRIAL MEMBRANE; LIVER CELL; LYSOSOME; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NERVE CELL; NIEMANN PICK DISEASE; NONHUMAN; OUTER MITOCHONDRIAL MEMBRANE; OXIDATIVE PHOSPHORYLATION; PATHOGENESIS; QUALITY CONTROL; REVIEW;

EID: 85035328749     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2017.00982     Document Type: Review

References (138)

1. Acín-Pérez, R., Carrascoso, I., Baixauli, F., Roche-Molina, M., Latorre-Pellicer, A., Fernández-Silva, P., et al. (2014). ROS-triggered phosphorylation of complex II by Fgr kinase regulates cellular adaptation to fuel use. Cell Metab. 19, 1020-1033. doi: 10.1016/j.cmet.2014.04.015
2. Acuña, M., Castro-Fernández, V., Latorre, M., Castro, J., Schuchman, E. H., Guixé, V., et al. (2016a). Structural and functional analysis of the ASM p.Ala359Asp mutant that causes acid sphingomyelinase deficiency. Biochem. Biophys. Res. Commun. 479, 496-501. doi: 10.1016/j.bbrc.2016.09.096
3. Acuña, M., Martínez, P., Moraga, C., He, X., Moraga, M., Hunter, B., et al. (2016b). Epidemiological, clinical and biochemical characterization of the p.(Ala359Asp) SMPD1 variant causing Niemann-Pick disease type B. Eur. J. Hum. Genet. 24, 208-213. doi: 10.1038/ejhg.2015.89
4. Alam, M. S., Getz, M., and Haldar, K. (2016). Chronic administration of an HDAC inhibitor treats both neurological and systemic Niemann-Pick type C disease in a mouse model. Sci. Transl. Med. 8:326ra23. doi: 10.1126/scitranslmed.aad9407
5. Almeida, A., Almeida, J., Bolaños, J. P., and Moncada, S. (2001). Different responses of astrocytes and neurons to nitric oxide: the role of glycolytically generated ATP in astrocyte protection. Proc. Natl. Acad. Sci. U.S.A. 98, 15294-15299. doi: 10.1073/pnas.261560998
6. Alpy, F., and Tomasetto, C. (2006). MLN64 and MENTHO, two mediators of endosomal cholesterol transport. Biochem. Soc. Trans. 34, 343-345. doi: 10.1042/BST0340343
7. Alpy, F., Legueux, F., Bianchetti, L., and Tomasetto, C. (2009). START domain-containing proteins: a review of their role in lipid transport exchange. Med. Sci. 25, 181-191. doi: 10.1051/medsci/2009252181
8. Alpy, F., Rousseau, A., Schwab, Y., Legueux, F., Stoll, I., Wendling, C., et al. (2013). STARD3 or STARD3NL and VAP form a novel molecular tether between late endosomes and the ER. J. Cell Sci. 126, 5500-5512. doi: 10.1242/jcs.139295
9. Alpy, F., Stoeckel, M. E., Dierich, A., Escola, J. M., Wendling, C., Chenard, M. P., et al. (2001). The steroidogenic acute regulatory protein homolog MLN64, a late endosomal cholesterol-binding protein. J. Biol. Chem. 276, 4261-4269. doi: 10.1074/jbc.M006279200
10. Baixauli, F., Acín-Pérez, R., Villarroya-Beltrí, C., Mazzeo, C., Nuñez-Andrade, N., Gabandé-Rodriguez, E., et al. (2015). Mitochondrial respiration controls lysosomal function during inflammatory T cell responses. Cell Metab. 22, 485-498. doi: 10.1016/j.cmet.2015.07.020
11. Baker, M. J., Palmer, C. S., and Stojanovski, D. (2014). Mitochondrial protein quality control in health and disease. Br. J. Pharmacol. 171, 1870-1889. doi: 10.1111/bph.12430
12. Balboa, E., Castro, J., Pinochet, M.-J., Cancino, G. I., Matías, N., José Sáez, P., et al. (2017). MLN64 induces mitochondrial dysfunction associated with increased mitochondrial cholesterol content. Redox Biol. 12, 274-284. doi: 10.1016/j.redox.2017.02.024
13. Baulies, A., Ribas, V., Núñez, S., Torres, S., Alarcón-Vila, C., Martínez, L., et al. (2015). Lysosomal cholesterol accumulation sensitizes to acetaminophen hepatotoxicity by impairing mitophagy. Sci. Rep. 5:18017. doi: 10.1038/srep18017
14. Blom, T. S., Linder, M. D., Snow, K., Pihko, H., Hess, M. W., Jokitalo, E., et al. (2003). Defective endocytic trafficking of NPC1 and NPC2 underlying infantile Niemann-Pick type C disease. Hum. Mol. Genet. 12, 257-272. doi: 10.1093/hmg/ddg025
15. Calderon-Dominguez, M., Gil, G., Medina, M. A., Pandak, W. M., and Rodríguez-Agudo, D. (2014). The StarD4 subfamily of steroidogenic acute regulatory-related lipid transfer (START) domain proteins: new players in cholesterol metabolism. Int. J. Biochem. Cell Biol. 49, 64-68. doi: 10.1016/j.biocel.2014.01.002
16. Canonico, B., Cesarini, E., Salucci, S., Luchetti, F., Falcieri, E., Di Sario, G., et al. (2016). Defective Autophagy, mitochondrial clearance and lipophagy in Niemann-Pick type B lymphocytes. PLoS ONE 11:e0165780. doi: 10.1371/journal.pone.0165780
17. Caron, K. M., Soo, S. C., Wetsel, W. C., Stocco, D. M., Clark, B. J., and Parker, K. L. (1997). Targeted disruption of the mouse gene encoding steroidogenic acute regulatory protein provides insights into congenital lipoid adrenal hyperplasia. Proc. Natl. Acad. Sci. U.S.A. 94, 11540-11545. doi: 10.1073/pnas.94.21.11540
18. Carstea, E. D., Morris, J. A., Coleman, K. G., Loftus, S. K., Zhang, D., Cummings, C., et al. (1997). Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis. Science 277, 228-231. doi: 10.1126/science.277.5323.228
19. Carstea, E. D., Polymeropoulos, M. H., Parker, C. C., Detera-Wadleigh, S. D., O'Neill, R. R., Patterson, M. C., et al. (1993). Linkage of Niemann-Pick disease type C to human chromosome 18. Proc. Natl. Acad. Sci. U.S.A. 90, 2002-2004
20. Cassiman, D., Packman, S., Bembi, B., Turkia, H. B., Al-Sayed, M., Schiff, M., et al. (2016). Cause of death in patients with chronic visceral and chronic neurovisceral acid sphingomyelinase deficiency (Niemann-Pick disease type B and B variant): literature review and report of new cases. Mol. Genet. Metab. 118, 206-213. doi: 10.1016/j.ymgme.2016.05.001
21. Chan, D. C. (2006). Mitochondria: dynamic organelles in disease, aging, and development. Cell 125, 1241-1252. doi: 10.1016/j.cell.2006.06.010
22. Charman, M., Kennedy, B. E., Osborne, N., and Karten, B. (2010). MLN64 mediates egress of cholesterol from endosomes to mitochondria in the absence of functional Niemann-Pick Type C1 protein. J. Lipid Res. 51, 1023-1034. doi: 10.1194/jlr.M002345
23. Charruyer, A., Grazide, S., Bezombes, C., Müller, S., Laurent, G., and Jaffrézou, J.-P. (2005). UV-C light induces raft-associated acid sphingomyelinase and JNK activation and translocation independently on a nuclear signal. J. Biol. Chem. 280, 19196-19204. doi: 10.1074/jbc.M412867200
24. Chen, G., Li, H.-M., Chen, Y.-R., Gu, X.-S., and Duan, S. (2007). Decreased estradiol release from astrocytes contributes to the neurodegeneration in a mouse model of Niemann-Pick disease type C. Glia 55, 1509-1518. doi: 10.1002/glia.20563
25. Chow, C. K., Ibrahim, W., Wei, Z., and Chan, A. C. (1999). Vitamin E regulates mitochondrial hydrogen peroxide generation. Free Radic. Biol. Med. 27, 580-587. doi: 10.1016/S0891-5849(99)00121-5
26. Colell, A., García-Ruiz, C., Lluis, J. M., Coll, O., Mari, M., and Fernández-Checa, J. C. (2003). Cholesterol impairs the adenine nucleotide translocator-mediated mitochondrial permeability transition through altered membrane fluidity. J. Biol. Chem. 278, 33928-33935. doi: 10.1074/jbc.M210943200
27. Contreras, P. S., Gonzalez-Zuñiga, M., González-Hódar, L., Yáñez, M., Dulcey, A., Marugan, J., et al. (2016). Neuronal gene repression in Niemann-Pick type C models is mediated by the c-Abl/HDAC2 signaling pathway. Biochim. Biophys. Acta 1859, 269-279. doi: 10.1016/j.bbagrm.2015.11.006
28. Daniele, T., and Schiaffino, M. V. (2016). Lipid transfer and metabolism across the endolysosomal-mitochondrial boundary. Biochim. Biophys. Acta 1861, 880-894. doi: 10.1016/j.bbalip.2016.02.001
29. Davies, J. P., and Ioannou, Y. A. (2000). Topological analysis of Niemann-Pick C1 protein reveals that the membrane orientation of the putative sterol-sensing domain is identical to those of 3-hydroxy-3-methylglutaryl-CoA reductase and sterol regulatory element binding protein cleavage-activating protein. J. Biol. Chem. 275, 24367-24374. doi: 10.1074/jbc.M002184200
30. Detmer, S. A., and Chan, D. C. (2007). Functions and dysfunctions of mitochondrial dynamics. Nat. Rev. Mol. Cell Biol. 8, 870-879. doi: 10.1038/nrm2275
31. Diogo, C. V., Yambire, K. F., Fernández Mosquera, L., Branco, F. T., and Raimundo, N. (2017). Mitochondrial adventures at the organelle society. Biochem. Biophys. Res. Commun. doi: 10.1016/j.bbrc.2017.04.124. [Epub ahead of print]
32. Echegoyen, S., Oliva, E. B., Sepulveda, J., Díaz-Zagoya, J. C., Espinosa-García, M. T., Pardo, J. P., et al. (1993). Cholesterol increase in mitochondria: its effect on inner-membrane functions, submitochondrial localization and ultrastructural morphology. Biochem. J. 289(Pt 3), 703-708. doi: 10.1042/bj2890703
33. Elbaz-Alon, Y. (2017). Mitochondria-organelle contact sites: the plot thickens. Biochem. Soc. Trans. 45, 477-488. doi: 10.1042/BST20160130
34. Elrick, M. J., Yu, T., Chung, C., and Lieberman, A. P. (2012). Impaired proteolysis underlies autophagic dysfunction in Niemann-Pick type C disease. Hum. Mol. Genet. 21, 4876-4887. doi: 10.1093/hmg/dds324
35. Elustondo, P., Martin, L. A., and Karten, B. (2017). Mitochondrial cholesterol import. Biochim. Biophys. Acta 1862, 90-101. doi: 10.1016/j.bbalip.2016.08.012
36. Enrich, C., Rentero, C., Hierro, A., and Grewal, T. (2015). Role of cholesterol in SNARE-mediated trafficking on intracellular membranes. J. Cell Sci. 128, 1071-1081. doi: 10.1242/jcs.164459
37. Falcone, S., Perrotta, C., De Palma, C., Pisconti, A., Sciorati, C., Capobianco, A., et al. (2004). Activation of acid sphingomyelinase and its inhibition by the nitric oxide/cyclic guanosine 3',5'-monophosphate pathway: key events in Escherichia coli-elicited apoptosis of dendritic cells. J. Immunol. 173, 4452-4463. doi: 10.4049/jimmunol.173.7.4452
38. Farmer, T., Reinecke, J. B., Xie, S., Bahl, K., Naslavsky, N., and Caplan, S. (2017). Control of mitochondrial homeostasis by endocytic regulatory proteins. J. Cell Sci. 130, 2359-2370. doi: 10.1242/jcs.204537
39. Fernandez, A., Matias, N., Fucho, R., Ribas, V., Von Montfort, C., Nuño, N., et al. (2013). ASMase is required for chronic alcohol induced hepatic endoplasmic reticulum stress and mitochondrial cholesterol loading. J. Hepatol. 59, 805-813. doi: 10.1016/j.jhep.2013.05.023
40. Ferrante, A., De Nuccio, C., Pepponi, R., Visentin, S., Martire, A., Bernardo, A., et al. (2016). Stimulation of adenosine A2A receptors reduces intracellular cholesterol accumulation and rescues mitochondrial abnormalities in human neural cell models of Niemann-Pick C1. Neuropharmacology 103, 155-162. doi: 10.1016/j.neuropharm.2015.11.022
41. Freeman, D. A., Romero, A., and Choi, Y. S. (1998). Plasma membrane steroidogenic cholesterol: the relative importance of membrane internalization rate and cholesterol extraction rate of internalized membrane. Endocr. Res. 24, 619-622. doi: 10.3109/07435809809032657
42. Friedland, N., Liou, H.-L., Lobel, P., and Stock, A. M. (2003). Structure of a cholesterol-binding protein deficient in Niemann-Pick type C2 disease. Proc. Natl. Acad. Sci. U.S.A. 100, 2512-2517. doi: 10.1073/pnas.0437840100
43. Fu, R., Wassif, C. A., Yanjanin, N. M., Watkins-Chow, D. E., Baxter, L. L., Incao, A., et al. (2013). Efficacy of N-acetylcysteine in phenotypic suppression of mouse models of Niemann-Pick disease, type C1. Hum. Mol. Genet. 22, 3508-3523. doi: 10.1093/hmg/ddt206
44. Fucho, R., Martínez, L., Baulies, A., Torres, S., Tarrats, N., Fernandez, A., et al. (2014). ASMase regulates autophagy and lysosomal membrane permeabilization and its inhibition prevents early stage non-alcoholic steatohepatitis. J. Hepatol. 61, 1126-1134. doi: 10.1016/j.jhep.2014.06.009
45. Futerman, A. H., and van Meer, G. (2004). The cell biology of lysosomal storage disorders. Nat. Rev. Mol. Cell Biol. 5, 554-565. doi: 10.1038/nrm1423
46. Garcia-Ruiz, C., Mari, M., Colell, A., Morales, A., Caballero, F., Montero, J., et al. (2009). Mitochondrial cholesterol in health and disease. Histol. Histopathol. 24, 117-132. doi: 10.14670/HH-24.117
47. Girard, M., Larivière, R., Parfitt, D. A., Deane, E. C., Gaudet, R., Nossova, N., et al. (2012). Mitochondrial dysfunction and Purkinje cell loss in autosomal recessive spastic ataxia of Charlevoix-Saguenay (ARSACS). Proc. Natl. Acad. Sci. U.S.A. 109, 1661-1666. doi: 10.1073/pnas.1113166109
48. Gocze, P. M., and Freeman, D. A. (1993). Plasma membrane cholesterol is utilized as steroidogenic substrate in Y-1 mouse adrenal tumor cells and normal sheep adrenal cells. Exp. Cell Res. 209, 21-25. doi: 10.1006/excr.1993.1279
49. Gorelik, A., Illes, K., Heinz, L. X., Superti-Furga, G., and Nagar, B. (2016). Crystal structure of mammalian acid sphingomyelinase. Nat. Commun. 7:12196. doi: 10.1038/ncomms12196
50. Guo, H., Zhao, M., Qiu, X., Deis, J. A., Huang, H., Tang, Q.-Q., et al. (2016). Niemann-Pick type C2 deficiency impairs autophagy-lysosomal activity, mitochondrial function, and TLR signaling in adipocytes. J. Lipid Res. 57, 1644-1658. doi: 10.1194/jlr.M066522
51. Hatefi, Y. (1985). The mitochondrial electron transport and oxidative phosphorylation system. Annu. Rev. Biochem. 54, 1015-1069. doi: 10.1146/annurev.bi.54.070185.005055
52. Huang, J., and Feigenson, G. W. (1999). A microscopic interaction model of maximum solubility of cholesterol in lipid bilayers. Biophys. J. 76, 2142-2157. doi: 10.1016/S0006-3495(99)77369-8
53. Ikonen, E. (2008). Cellular cholesterol trafficking and compartmentalization. Nat. Rev. Mol. Cell Biol. 9, 125-138. doi: 10.1038/nrm2336
54. Iyer, L. M., Koonin, E. V., and Aravind, L. (2001). Adaptations of the helix-grip fold for ligand binding and catalysis in the START domain superfamily. Proteins 43, 134-144. doi: 10.1002/1097-0134(20010501)43:2<134::AID-PROT1025>3.0.CO;2-I
55. Jennings, J. J., Zhu, J.-H., Rbaibi, Y., Luo, X., Chu, C. T., and Kiselyov, K. (2006). Mitochondrial aberrations in mucolipidosis Type IV. J. Biol. Chem. 281, 39041-39050. doi: 10.1074/jbc.M607982200
56. Johri, A., and Beal, M. F. (2012). Mitochondrial dysfunction in neurodegenerative diseases. J. Pharmacol. Exp. Ther. 342, 619-630. doi: 10.1124/jpet.112.192138
57. Kasumu, A., and Bezprozvanny, I. (2012). Deranged calcium signaling in Purkinje cells and pathogenesis in spinocerebellar ataxia 2 (SCA2) and other ataxias. Cerebellum Lond. Engl. 11, 630-639. doi: 10.1007/s12311-010-0182-9
58. Kennedy, B. E., Charman, M., and Karten, B. (2012). Niemann-Pick Type C2 protein contributes to the transport of endosomal cholesterol to mitochondria without interacting with NPC1. J. Lipid Res. 53, 2632-2642. doi: 10.1194/jlr.M029942
59. Kennedy, B. E., Madreiter, C. T., Vishnu, N., Malli, R., Graier, W. F., and Karten, B. (2014). Adaptations of energy metabolism associated with increased levels of mitochondrial cholesterol in Niemann-Pick type C1-deficient cells. J. Biol. Chem. 289, 16278-16289. doi: 10.1074/jbc.M114.559914
60. Kim, S. J., Lee, B. H., Lee, Y. S., and Kang, K. S. (2007). Defective cholesterol traffic and neuronal differentiation in neural stem cells of Niemann-Pick type C disease improved by valproic acid, a histone deacetylase inhibitor. Biochim. Biophys. Res. Commun. 360, 593-599. doi: 10.1016/j.bbrc.2007.06.116
61. Kiselyov, K., and Muallem, S. (2008). Mitochondrial Ca2+ homeostasis in lysosomal storage diseases. Cell Calcium 44, 103-111. doi: 10.1016/j.ceca.2007.12.005
62. Kishida, T., Kostetskii, I., Zhang, Z., Martinez, F., Liu, P., Walkley, S. U., et al. (2004). Targeted mutation of the MLN64 START domain causes only modest alterations in cellular sterol metabolism. J. Biol. Chem. 279, 19276-19285. doi: 10.1074/jbc.M400717200
63. Klein, A. D., Alvarez, A., and Zanlungo, S. (2014). The unique case of the Niemann-Pick type C cholesterol storage disorder. Pediatr. Endocrinol. Rev. 12(Suppl. 1), 166-175
64. Klein, A., Mosqueira, M., Martínez, G., Robledo, F., González, M., Caballero, B., et al. (2011). Lack of activation of the unfolded protein response in mouse and cellular models of Niemann-Pick type C disease. Neurodegener. Dis. 8, 124-128. doi: 10.1159/000316540
65. Kraemer, F. B., Shen, W.-J., and Azhar, S. (2017). SNAREs and cholesterol movement for steroidogenesis. Mol. Cell. Endocrinol. 441, 17-21. doi: 10.1016/j.mce.2016.07.034
66. Kwon, H. J., Abi-Mosleh, L., Wang, M. L., Deisenhofer, J., Goldstein, J. L., Brown, M. S., et al. (2009). Structure of N-terminal domain of NPC1 reveals distinct subdomains for binding and transfer of cholesterol. Cell 137, 1213-1224. doi: 10.1016/j.cell.2009.03.049
67. Lange, Y., Steck, T. L., Ye, J., Lanier, M. H., Molugu, V., and Ory, D. (2009). Regulation of fibroblast mitochondrial 27-hydroxycholesterol production by active plasma membrane cholesterol. J. Lipid Res. 50, 1881-1888. doi: 10.1194/jlr.M900116-JLR200
68. Lapuente-Brun, E., Moreno-Loshuertos, R., Acín-Pérez, R., Latorre-Pellicer, A., Colás, C., Balsa, E., et al. (2013). Supercomplex assembly determines electron flux in the mitochondrial electron transport chain. Science 340, 1567-1570. doi: 10.1126/science.1230381
69. Lavigne, P., Najmanivich, R., and Lehoux, J.-G. (2010). Mammalian StAR-related lipid transfer (START) domains with specificity for cholesterol: structural conservation and mechanism of reversible binding. Subcell. Biochem. 51, 425-437. doi: 10.1007/978-90-481-8622-8_15
70. Lee, H., Lee, J. K., Park, M. H., Hong, Y. R., Marti, H. H., Kim, H., et al. (2014). Pathological roles of the VEGF/SphK pathway in Niemann-Pick type C neurons. Nat. Commun. 5:5514. doi: 10.1038/ncomms6514
71. Lee, J. E., Westrate, L. M., Wu, H., Page, C., and Voeltz, G. K. (2016). Multiple dynamin family members collaborate to drive mitochondrial division. Nature 540, 139-143. doi: 10.1038/nature20555
72. Létourneau, D., Lefebvre, A., Lavigne, P., and LeHoux, J.-G. (2015). The binding site specificity of STARD4 subfamily: breaking the cholesterol paradigm. Mol. Cell. Endocrinol. 408, 53-61. doi: 10.1016/j.mce.2014.12.016
73. Leventhal, A. R., Chen, W., Tall, A. R., and Tabas, I. (2001). Acid sphingomyelinase-deficient macrophages have defective cholesterol trafficking and efflux. J. Biol. Chem. 276, 44976-44983. doi: 10.1074/jbc.M106455200
74. Lidove, O., Sedel, F., Charlotte, F., Froissart, R., and Vanier, M. T. (2015). Cirrhosis and liver failure: expanding phenotype of Acid sphingomyelinase-deficient Niemann-Pick disease in adulthood. JIMD Rep. 15, 117-121. doi: 10.1007/8904_2014_306
75. Lieberman, A. P., Puertollano, R., Raben, N., Slaugenhaupt, S., Walkley, S. U., and Ballabio, A. (2012). Autophagy in lysosomal storage disorders. Autophagy 8, 719-730. doi: 10.4161/auto.19469
76. Lin, D., Sugawara, T., Strauss, J. F., Clark, B. J., Stocco, D. M., Saenger, P., et al. (1995). Role of steroidogenic acute regulatory protein in adrenal and gonadal steroidogenesis. Science 267, 1828-1831. doi: 10.1126/science.7892608
77. Liu, J., Rone, M. B., and Papadopoulos, V. (2006). Protein-protein interactions mediate mitochondrial cholesterol transport and steroid biosynthesis. J. Biol. Chem. 281, 38879-38893. doi: 10.1074/jbc.M608820200
78. Lloyd-Evans, E., Morgan, A. J., He, X., Smith, D. A., Elliot-Smith, E., Sillence, D. J., et al. (2008). Niemann-Pick disease type C1 is a sphingosine storage disease that causes deregulation of lysosomal calcium. Nat. Med. 14, 1247-1255. doi: 10.1038/nm.1876
79. Lucki, N. C., Li, D., Bandyopadhyay, S., Wang, E., Merril, A. H., and Sewer, M. B. (2012). Acid ceramidase (ASAH1) represses steroidogenic factor 1-dependent gene transcription in H295R human adrenocortical cells by binding to the receptor. Mol. Cell. Biol. 32, 4419-4431. doi: 10.1128/MCB.00378-12
80. Luzio, J. P., Pryor, P. R., and Bright, N. A. (2007). Lysosomes: fusion and function. Nat. Rev. Mol. Cell Biol. 8, 622-632. doi: 10.1038/nrm2217
81. Marí, M., Caballero, F., Colell, A., Morales, A., Caballeria, J., Fernandez, A., et al. (2006). Mitochondrial free cholesterol loading sensitizes to TNF-and Fas-mediated steatohepatitis. Cell Metab. 4, 185-198. doi: 10.1016/j.cmet.2006.07.006
82. Marí, M., Morales, A., Colell, A., García-Ruiz, C., and Fernández-Checa, J. C. (2009). Mitochondrial glutathione, a key survival antioxidant. Antioxid. Redox Signal. 11, 2685-2700. doi: 10.1089/ars.2009.2695
83. Marín, T., Contreras, P., Castro, J. F., Chamorro, D., Balboa, E., Bosch-Morató, M., et al. (2014). Vitamin E dietary supplementation improves neurological symptoms and decreases c-Abl/p73 activation in Niemann-Pick C mice. Nutrients 6, 3000-3017. doi: 10.3390/nu6083000
84. McGovern, M. M., Dionisi-Vici, C., Giugliani, R., Hwu, P., Lidove, O., Lukacs, Z., et al. (2017). Consensus recommendation for a diagnostic guideline for acid sphingomyelinase deficiency. Genet. Med. 19, 967-974. doi: 10.1038/gim.2017.7
85. McGovern, M. M., Lippa, N., Bagiella, E., Schuchman, E. H., Desnick, R. J., and Wasserstein, M. P. (2013). Morbidity and mortality in type B Niemann-Pick disease. Genet. Med. 15, 618-623. doi: 10.1038/gim.2013.4
86. McLelland, G.-L., Lee, S. A., McBride, H. M., and Fon, E. A. (2016). Syntaxin-17 delivers PINK1/parkin-dependent mitochondrial vesicles to the endolysosomal system. J. Cell Biol. 214, 275-291. doi: 10.1083/jcb.201603105
87. Miller, W. L. (1997). Congenital lipoid adrenal hyperplasia: the human gene knockout for the steroidogenic acute regulatory protein. J. Mol. Endocrinol. 19, 227-240. doi: 10.1677/jme.0.0190227
88. Moles, A., Tarrats, N., Fernández-Checa, J. C., and Marí, M. (2012). Cathepsin B overexpression due to acid sphingomyelinase ablation promotes liver fibrosis in Niemann-Pick disease. J. Biol. Chem. 287, 1178-1188. doi: 10.1074/jbc.M111.272393
89. Morohaku, K., Pelton, S. H., Daugherty, D. J., Butler, W. R., Deng, W., and Selvaraj, V. (2014). Translocator protein/peripheral benzodiazepine receptor is not required for steroid hormone biosynthesis. Endocrinology 155, 89-97. doi: 10.1210/en.2013-1556
90. Munkacsi, A. B., Hammond, N., Schneider, R. T., Senannayake, D. S., Higaki, K., Lagutin, K., Bloor, S. J., et al. (2017). Normalization of hepatic homeostasis in the Npc1nmf164 mouse model of Niemann-Pick type C diseases treated wth the histone deacetylase inhibitor vorinostat. J. Biol. Chem. 292, 4395-4410. doi: 10.1074/jbc.M116.770578
91. Naureckiene, S., Sleat, D. E., Lackland, H., Fensom, A., Vanier, M. T., Wattiaux, R., et al. (2000). Identification of HE1 as the second gene of Niemann-Pick C disease. Science 290, 2298-2301. doi: 10.1126/science.290.5500.2298
92. Ordonez, M. P. (2012). Defective mitophagy in human Niemann-Pick Type C1 neurons is due to abnormal autophagy activation. Autophagy 8, 1157-1158. doi: 10.4161/auto.20668
93. Ordonez, M. P., Roberts, E. A., Kidwell, C. U., Yuan, S. H., Plaisted, W. C., and Goldstein, L. S. B. (2012). Disruption and therapeutic rescue of autophagy in a human neuronal model of Niemann Pick type C1. Hum. Mol. Genet. 21, 2651-2662. doi: 10.1093/hmg/dds090
94. Osellame, L. D., and Duchen, M. R. (2014). Quality control gone wrong: mitochondria, lysosomal storage disorders and neurodegeneration. Br. J. Pharmacol. 171, 1958-1972. doi: 10.1111/bph.12453
95. Osellame, L. D., Rahim, A. A., Hargreaves, I. P., Gegg, M. E., Richard-Londt, A., Brandner, S., et al. (2013). Mitochondria and quality control defects in a mouse model of Gaucher disease-links to Parkinson's disease. Cell Metab. 17, 941-953. doi: 10.1016/j.cmet.2013.04.014
96. Patterson, M. C., and Walkley, S. U. (2017). Niemann-Pick disease, type C and Roscoe Brady. Mol. Genet. Metab. 120, 34-37. doi: 10.1016/j.ymgme.2016.11.008
97. Patterson, M. C., Hendriksz, C. J., Walterfang, M., Sedel, F., Vanier, M. T., Wijburg, F., et al. (2012). Recommendations for the diagnosis and management of Niemann-Pick disease type C: an update. Mol. Genet. Metab. 106, 330-344. doi: 10.1016/j.ymgme.2012.03.012
98. Pentchev, P. G., Boothe, A. D., Kruth, H. S., Weintroub, H., Stivers, J., and Brady, R. O. (1984). A genetic storage disorder in BALB/C mice with a metabolic block in esterification of exogenous cholesterol. J. Biol. Chem. 259, 5784-5791
99. Pipalia, N. H., Cosner, C. C., Huang, A., Chatterjee, A., Bourbon, P., Farley, N., et al. (2011). Histone deacetylase inhibitor treatment dramatically reduces cholesterol accumulation in Niemann-Pick type C1 mutant human fibroblasts. Proc. Natl. Acad. Sci. U.S.A. 108, 5620-5625. doi: 10.1073/pnas.1014890108
100. Platt, F. M., Boland, B., and van der Spoel, A. C. (2012). The cell biology of disease: lysosomal storage disorders: the cellular impact of lysosomal dysfunction. J. Cell Biol. 199, 723-734. doi: 10.1083/jcb.201208152
101. Plotegher, N., and Duchen, M. R. (2017). Mitochondrial dysfunction and neurodegeneration in lysosomal storage disorders. Trends Mol. Med. 23, 116-134. doi: 10.1016/j.molmed.2016.12.003
102. Ponting, C. P., and Aravind, L. (1999). START: a lipid-binding domain in StAR, HD-ZIP and signalling proteins. Trends Biochem. Sci. 24, 130-132. doi: 10.1016/S0968-0004(99)01362-6
103. Radhakrishnan, A., Anderson, T. G., and McConnell, H. M. (2000). Condensed complexes, rafts, and the chemical activity of cholesterol in membranes. Proc. Natl. Acad. Sci. U.S.A. 97, 12422-12427. doi: 10.1073/pnas.220418097
104. Raimundo, N., Fernández-Mosquera, L., Yambire, K. F., and Diogo, C. V. (2016). Mechanisms of communication between mitochondria and lysosomes. Int. J. Biochem. Cell Biol. 79, 345-349. doi: 10.1016/j.biocel.2016.08.020
105. Ridgway, N. D. (2000). Interactions between metabolism and intracellular distribution of cholesterol and sphingomyelin. Biochim. Biophys. Acta 1484, 129-141. doi: 10.1016/S1388-1981(00)00006-8
106. Rodriguez-Lafrasse, C., Rousson, R., Pentchev, P. G., Louisot, P., and Vanier, M. T. (1994). Free sphingoid bases in tissues from patients with type C Niemann-Pick disease and other lysosomal storage disorders. Biochim. Biophys. Acta 1226, 138-144. doi: 10.1016/0925-4439(94)90021-3
107. Rone, M. B., Fan, J., and Papadopoulos, V. (2009). Cholesterol transport in steroid biosynthesis: role of protein-protein interactions and implications in disease states. Biochim. Biophys. Acta 1791, 646-658. doi: 10.1016/j.bbalip.2009.03.001
108. Rowland, A. A., and Voeltz, G. K. (2012). Endoplasmic reticulum-mitochondria contacts: function of the junction. Nat. Rev. Mol. Cell Biol. 13, 607-625. doi: 10.1038/nrm3440
109. Saffari, A., Kölker, S., Hoffmann, G. F., and Ebrahimi-Fakhari, D. (2017). Linking mitochondrial dysfunction to neurodegeneration in lysosomal storage diseases. J. Inherit. Metab. Dis. doi: 10.1007/s10545-017-0048-0. [Epub ahead of print]
110. Saftig, P., and Klumperman, J. (2009). Lysosome biogenesis and lysosomal membrane proteins: trafficking meets function. Nat. Rev. Mol. Cell Biol. 10, 623-635. doi: 10.1038/nrm2745
111. Schrader, M., Godinho, L. F., Costello, J. L., and Islinger, M. (2015). The different facets of organelle interplay-an overview of organelle interactions. Front. Cell Dev. Biol. 3:56. doi: 10.3389/fcell.2015.00056
112. Schuchman, E. H., and Desnick, R. J. (2014). "Niemann-Pick disease types A and B: acid sphingomyelinase deficiencies," in The Online Metabolic and Molecular Bases of Inherited Disease, McGraw-Hill Medical. Chapter 144, ed D. Valle (New York, NY: McGraw-Hill), OMMBID (Accessed December 6, 2015)
113. Schuchman, E. H., and Desnick, R. J. (2017). Types A and B Niemann-Pick disease. Mol. Genet. Metab. 120, 27-33. doi: 10.1016/j.ymgme.2016.12.008
114. Settembre, C., Fraldi, A., Medina, D. L., and Ballabio, A. (2013). Signals from the lysosome: a control centre for cellular clearance and energy metabolism. Nat. Rev. Mol. Cell Biol. 14, 283-296. doi: 10.1038/nrm3565
115. Shen, D., Wang, X., Li, X., Zhang, X., Yao, Z., Dibble, S., et al. (2012). Lipid storage disorders block lysosomal trafficking by inhibiting a TRP channel and lysosomal calcium release. Nat. Commun. 3:731. doi: 10.1038/ncomms1735
116. Shen, W.-J., Patel, S., Natu, V., Hong, R., Wang, J., Azhar, S., et al. (2003). Interaction of hormone-sensitive lipase with steroidogenic acute regulatory protein: facilitation of cholesterol transfer in adrenal. J. Biol. Chem. 278, 43870-43876. doi: 10.1074/jbc.M303934200
117. Sheng, Z.-H., and Cai, Q. (2012). Mitochondrial transport in neurons: impact on synaptic homeostasis and neurodegeneration. Nat. Rev. Neurosci. 13, 77-93. doi: 10.1038/nrn3156
118. Slotte, J. P. (1999). Sphingomyelin-cholesterol interactions in biological and model membranes. Chem. Phys. Lipids 102, 13-27. doi: 10.1016/S0009-3084(99)00071-7
119. Smith, E. L., and Schuchman, E. H. (2008). The unexpected role of acid sphingomyelinase in cell death and the pathophysiology of common diseases. FASEB J. 22, 3419-3431. doi: 10.1096/fj.08-108043
120. Soubannier, V., McLelland, G.-L., Zunino, R., Braschi, E., Rippstein, P., Fon, E. A., et al. (2012). A vesicular transport pathway shuttles cargo from mitochondria to lysosomes. Curr. Biol. 22, 135-141. doi: 10.1016/j.cub.2011.11.057
121. Stocco, D. M. (2001). StAR protein and the regulation of steroid hormone biosynthesis. Annu. Rev. Physiol. 63, 193-213. doi: 10.1146/annurev.physiol.63.1.193
122. Stojkovski, V., Hadzi-Petrushev, N., Ilieski, V., Sopi, R., Gjorgoski, I., Mitrov, D., et al. (2013). Age and heat exposure-dependent changes in antioxidant enzymes activities in rat's liver and brain mitochondria: role of alpha-tocopherol. Physiol. Res. 62, 503-510
123. Tang, F.-L., Liu, W., Hu, J.-X., Erion, J. R., Ye, J., Mei, L., et al. (2015). VPS35 deficiency or mutation causes dopaminergic neuronal loss by impairing mitochondrial fusion and function. Cell Rep. 12, 1631-1643. doi: 10.1016/j.celrep.2015.08.001
124. Taylor, R. W., and Turnbull, D. M. (2005). Mitochondrial DNA mutations in human disease. Nat. Rev. Genet. 6, 389-402. doi: 10.1038/nrg1606
125. Thurberg, B. L., Wasserstein, M. P., Schiano, T., O'Brien, F., Richards, S., Cox, G. F., et al. (2012). Liver and skin histopathology in adults with acid sphingomyelinase deficiency (Niemann-Pick disease type B). Am. J. Surg. Pathol. 36, 1234-1246. doi: 10.1097/PAS.0b013e31825793ff
126. Torres, S., Baulies, A., Fucho, R., Garcia-Ruiz, C., and Fernandez-Checa, J. C. (2016). StARD1 overexpression through ACDase downregulation contributes to hepatic mitochondria cholesterol-mediated GSH depletion and liver injury in Niemann-Pick C disease. Hepatology 64:361A
127. Torres, S., Matías, N., Baulies, A., Nuñez, S., Alarcon-Vila, C., Martinez, L., et al. (2017). Mitochondrial GSH replenishment as a potential therapeutic approach for Niemann Pick type C disease. Redox Biol. 11, 60-72. doi: 10.1016/j.redox.2016.11.010
128. Tu, L. N., Morohaku, K., Manna, P. R., Pelton, S. H., Butler, W. R., Stocco, D. M., et al. (2014). Peripheral benzodiazepine receptor/translocator protein global knock-out mice are viable with no effects on steroid hormone biosynthesis. J. Biol. Chem. 289, 27444-27454. doi: 10.1074/jbc.M114.578286
129. Vanier, M. T. (2013). Niemann-Pick diseases. Handb. Clin. Neurol. 113, 1717-1721. doi: 10.1016/B978-0-444-59565-2.00041-1
130. Vázquez, M. C., Balboa, E., Alvarez, A. R., and Zanlungo, S. (2012). Oxidative stress: a pathogenic mechanism for Niemann-Pick type C disease. Oxid. Med. Cell Longev. 2012:205713. doi: 10.1155/2012/205713
131. Visentin, S., De Nuccio, C., Bernardo, A., Pepponi, R., Ferrante, A., Minghetti, L., et al. (2013). The stimulation of adenosine A2A receptors ameliorates the pathological phenotype of fibroblasts from Niemann-Pick type C patients. J. Neurosci. 33, 15388-15393. doi: 10.1523/JNEUROSCI.0558-13.2013
132. Watari, H., Arakane, F., Moog-Lutz, C., Kallen, C. B., Tomasetto, C., Gerton, G. L., et al. (1997). MLN64 contains a domain with homology to the steroidogenic acute regulatory protein (StAR) that stimulates steroidogenesis. Proc. Natl. Acad. Sci. U.S.A. 94, 8462-8467. doi: 10.1073/pnas.94.16.8462
133. Wos, M., Szczepanowska, J., Pikula, S., Tylki-Szymanska, A., Zablocki, K., and Bandorowicz-Pikula, J. (2016). Mitochondrial dysfunction in fibroblasts derived from patients with Niemann-Pick type C disease. Arch. Biochem. Biophys. 593, 50-59. doi: 10.1016/j.abb.2016.02.012
134. Xiong, Z.-J., Huang, J., Poda, G., Pomès, R., and Privé, G. G. (2016). Structure of human acid sphingomyelinase reveals the role of the saposin domain in activating substrate hydrolysis. J. Mol. Biol. 428, 3026-3042. doi: 10.1016/j.jmb.2016.06.012
135. Youle, R. J., and Narendra, D. P. (2011). Mechanisms of mitophagy. Nat. Rev. Mol. Cell Biol. 12, 9-14. doi: 10.1038/nrm3028
136. Yu, W., Gong, J.-S., Ko, M., Garver, W. S., Yanagisawa, K., and Michikawa, M. (2005). Altered cholesterol metabolism in Niemann-Pick type C1 mouse brains affects mitochondrial function. J. Biol. Chem. 280, 11731-11739. doi: 10.1074/jbc.M412898200
137. Zampieri, S., Filocamo, M., Pianta, A., Lualdi, S., Gort, L., Coll, M. J., et al. (2016). SMPD1 mutation update: database and comprehensive analysis of published and novel variants. Hum. Mutat. 37, 139-147. doi: 10.1002/humu.22923
138. Zhang, M., Liu, P., Dwyer, N. K., Christenson, L. K., Fujimoto, T., Martinez, F., et al. (2002). MLN64 mediates mobilization of lysosomal cholesterol to steroidogenic mitochondria. J. Biol. Chem. 277, 33300-33310. doi: 10.1074/jbc.M200003200