Small regulators, major consequences-Ca2+ and cholesterol at the endosome-ER interface

Journal of Cell Science

Volumn 127, Issue 5, 2014, Pages 929-938

  Van Der Kant, Rik ^a   Neefjes, Jacques ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

Ca2+; Cholesterol; Endoplasmic reticulum; Endosome; Lysosome; Membrane contact site

Indexed keywords

CALCIUM ION; CHOLESTEROL; EPIDERMAL GROWTH FACTOR RECEPTOR; ESCRT PROTEIN; GRANULOCYTE COLONY STIMULATING FACTOR RECEPTOR; LOW DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR; PHOSPHATIDYLINOSITOL; PRESENILIN 1; PROTEIN TYROSINE PHOSPHATASE 1B; STEROIDOGENIC ACUTE REGULATORY PROTEIN; STEROL REGULATORY ELEMENT BINDING PROTEIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL;

ARTICLE; CELL COMMUNICATION; CELL FREE SYSTEM; CELL FUNCTION; CELL INTERACTION; CELL MATURATION; CELLULAR DISTRIBUTION; CHOLESTEROL TRANSPORT; CONFORMATIONAL TRANSITION; ELECTRON MICROSCOPY; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENDOSOME; EXTRACELLULAR FLUID; HUMAN; LYSOSOME; MICROSCOPY; MULTIVESICULAR BODY; NEURONAL CEROID LIPOFUSCINOSIS; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION;

CA2+; CHOLESTEROL; ENDOPLASMIC RETICULUM; ENDOSOME; LYSOSOME; MEMBRANE CONTACT SITE;

CALCIUM; CALCIUM SIGNALING; CHOLESTEROL; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENDOSOMES; HUMANS; RAB GTP-BINDING PROTEINS;

EID: 84896819965     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.137539     Document Type: Article

References (83)

1. Alpy, F. and Tomasetto, C. (2005). Give lipids a START: the StAR-related lipid transfer (START) domain in mammals. J. Cell Sci. 118, 2791-2801.
2. Alpy, F., Rousseau, A., Schwab, Y., Legueux, F., Stoll, I., Wendling, C., Spiegelhalter, C., Kessler, P., Mathelin, C., Rio, M. 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.
3. Amini-Bavil-Olyaee, S., Choi, Y. J., Lee, J. H., Shi, M., Huang, I. C., Farzan, M. and Jung, J. U. (2013). The antiviral effector IFITM3 disrupts intracellular cholesterol homeostasis to block viral entry. Cell Host Microbe 13, 452-464.
4. Annaert, W. G., Levesque, L., Craessaerts, K., Dierinck, I., Snellings, G., Westaway, D., George-Hyslop, P. S., Cordell, B., Fraser, P. and De Strooper, B. (1999). Presenilin 1 controls gamma-secretase processing of amyloid precursor protein in pre-golgi compartments of hippocampal neurons. J. Cell Biol. 147, 277-294.
5. Bargal, R. and Bach, G. (1997). Mucolipidosis type IV: abnormal transport of lipids to lysosomes. J. Inherit. Metab. Dis. 20, 625-632.
6. Berridge, M. J., Lipp, P. and Bootman, M. D. (2000). The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell Biol. 1, 11-21.
7. Bissig, C., Lenoir, M., Velluz, M. C., Kufareva, I., Abagyan, R., Overduin, M. and Gruenberg, J. (2013). Viral infection controlled by a calcium-dependent lipid-binding module in ALIX. Dev. Cell 25, 364-373.
8. Brown, M. S. and Goldstein, J. L. (1999). A proteolytic pathway that controls the cholesterol content of membranes, cells, and blood. Proc. Natl. Acad. Sci. USA 96, 11041-11048.
9. Cantalupo, G., Alifano, P., Roberti, V., Bruni, C. B. and Bucci, C. (2001). Rabinteracting lysosomal protein (RILP): the Rab7 effector required for transport to lysosomes. EMBO J. 20, 683-693.
10. Cataldo, A. M., Peterhoff, C. M., Troncoso, J. C., Gomez-Isla, T., Hyman, B. T. and Nixon, R. A. (2000). Endocytic pathway abnormalities precede amyloid beta deposition in sporadic Alzheimer's disease and Down syndrome: differential effects of APOE genotype and presenilin mutations. Am. J. Pathol. 157, 277-286.
11. Christensen, K. A., Myers, J. T. and Swanson, J. A. (2002). pH-dependent regulation of lysosomal calcium in macrophages. J. Cell Sci. 115, 599-607.
12. Churchill, G. C., Okada, Y., Thomas, J. M., Genazzani, A. A., Patel, S. and Galione, A. (2002). NAADP mobilizes Ca(2+) from reserve granules, lysosomerelated organelles, in sea urchin eggs. Cell 111, 703-708.
13. Cianciola, N. L., Greene, D. J., Morton, R. E. and Carlin, C. R. (2013). Adenovirus RIDa uncovers a novel pathway requiring ORP1L for lipid droplet formation independent of NPC1. Mol. Biol. Cell 24, 3309-3325.
14. Clapper, D. L.,Walseth, T. F., Dargie, P. J. and Lee, H. C. (1987). Pyridine nucleotide metabolites stimulate calcium release from sea urchin egg microsomes desensitized to inositol trisphosphate. J. Biol. Chem. 262, 9561-9568.
15. Coen, K., Flannagan, R. S., Baron, S., Carraro-Lacroix, L. R., Wang, D., Vermeire, W., Michiels, C., Munck, S., Baert, V., Sugita, S. et al. (2012). Lysosomal calcium homeostasis defects, not proton pump defects, cause endo-lysosomal dysfunction in PSEN-deficient cells. J. Cell Biol. 198, 23-35.
16. Colombo, M. I., Beron, W. and Stahl, P. D. (1997). Calmodulin regulates endosome fusion. J. Biol. Chem. 272, 7707-7712.
17. Courtney, S. C., Di, H., Stockman, B. M., Liu, H., Scherbik, S. V. and Brinton, M. A. (2012). Identification of novel host cell binding partners of Oas1b, the protein conferring resistance to flavivirus-induced disease in mice. J. Virol. 86, 7953-7963.
18. Dong, X. P., Shen, D., Wang, X., Dawson, T., Li, X., Zhang, Q., Cheng, X., Zhang, Y., Weisman, L. S., Delling, M. et al. (2010). PI(3,5)P(2) controls membrane trafficking by direct activation of mucolipin Ca(2+) release channels in the endolysosome. Nat. Commun. 1, 38.
19. Du, X., Kumar, J., Ferguson, C., Schulz, T. A., Ong, Y. S., Hong, W., Prinz, W. A., Parton, R. G., Brown, A. J. and Yang, H. (2011). A role for oxysterolbinding protein-related protein 5 in endosomal cholesterol trafficking. J. Cell Biol. 192, 121-135.
20. Du, X., Kazim, A. S., Brown, A. J. and Yang, H. (2012). An essential role of Hrs/ Vps27 in endosomal cholesterol trafficking. Cell Reports 1, 29-35.
21. Eden, E. R., White, I. J., Tsapara, A. and Futter, C. E. (2010). Membrane contacts between endosomes and ER provide sites for PTP1B-epidermal growth factor receptor interaction. Nat. Cell Biol. 12, 267-272.
22. Eden, E. R., Burgoyne, T., Edgar, J. R., Sorkin, A. and Futter, C. E. (2012). The relationship between ER-multivesicular body membrane contacts and the ESCRT machinery. Biochem. Soc. Trans. 40, 464-468.
23. Elbaz, Y. and Schuldiner, M. (2011). Staying in touch: the molecular era of organelle contact sites. Trends Biochem. Sci. 36, 616-623.
24. Fairn, G. D. and Grinstein, S. (2012). How nascent phagosomes mature to become phagolysosomes. Trends Immunol. 33, 397-405.
25. Friedman, J. R., Dibenedetto, J. R., West, M., Rowland, A. A. and Voeltz, G. K. (2013). Endoplasmic reticulum-endosome contact increases as endosomes traffic and mature. Mol. Biol. Cell 24, 1030-1040.
26. Futter, C. E., Felder, S., Schlessinger, J., Ullrich, A. and Hopkins, C. R. (1993). Annexin I is phosphorylated in the multivesicular body during the processing of the epidermal growth factor receptor. J. Cell Biol. 120, 77-83.
27. Gerasimenko, J. V., Tepikin, A. V., Petersen, O. H. and Gerasimenko, O. V. (1998). Calcium uptake via endocytosis with rapid release from acidifying endosomes. Curr. Biol. 8, 1335-1338.
28. 2+ signalling to membrane dynamics. Nat. Rev. Mol. Cell Biol. 6, 449-461.
29. Getty, A. L. and Pearce, D. A. (2011). Interactions of the proteins of neuronal ceroid lipofuscinosis: clues to function. Cell. Mol. Life Sci. 68, 453-474.
30. Hölttä-Vuori, M., Alpy, F., Tanhuanpää , K., Jokitalo, E., Mutka, A. L. and Ikonen, E. (2005). MLN64 is involved in actin-mediated dynamics of late endocytic organelles. Mol. Biol. Cell 16, 3873-3886.
31. Huotari, J. and Helenius, A. (2011). Endosome maturation. EMBO J. 30, 3481-3500.
32. Huynh, K. K., Gershenzon, E. and Grinstein, S. (2008). Cholesterol accumulation by macrophages impairs phagosome maturation. J. Biol. Chem. 283, 35745-35755.
33. Ikonen, E. (2008). Cellular cholesterol trafficking and compartmentalization. Nat. Rev. Mol. Cell Biol. 9, 125-138.
34. Israel, M. A., Yuan, S. H., Bardy, C., Reyna, S. M., Mu, Y., Herrera, C., Hefferan, M. P., Van Gorp, S., Nazor, K. L., Boscolo, F. S. et al. (2012). Probing sporadic and familial Alzheimer's disease using induced pluripotent stem cells. Nature 482, 216-220.
35. Johansson, M., Lehto, M., Tanhuanpää , K., Cover, T. L. and Olkkonen, V. M. (2005). The oxysterol-binding protein homologue ORP1L interacts with Rab7 and alters functional properties of late endocytic compartments. Mol. Biol. Cell 16, 5480-5492.
36. Johansson, M., Rocha, N., Zwart, W., Jordens, I., Janssen, L., Kuijl, C., Olkkonen, V. M. and Neefjes, J. (2007). Activation of endosomal dynein motors by stepwise assembly of Rab7-RILP-p150Glued, ORP1L, and the receptor betalll spectrin. J. Cell Biol. 176, 459-471.
37. Jordens, I., Fernandez-Borja, M., Marsman, M., Dusseljee, S., Janssen, L., Calafat, J., Janssen, H., Wubbolts, R. and Neefjes, J. (2001). The Rab7 effector protein RILP controls lysosomal transport by inducing the recruitment of dynein-dynactin motors. Curr. Biol. 11, 1680-1685.
38. Jovic, M., Sharma, M., Rahajeng, J. and Caplan, S. (2010). The early endosome: a busy sorting station for proteins at the crossroads. Histol. Histopathol. 25, 99-112.
39. Kaiser, S. E., Brickner, J. H., Reilein, A. R., Fenn, T. D., Walter, P. and Brunger, A. T. (2005). Structural basis of FFAT motif-mediated ER targeting. Structure 13, 1035-1045.
40. 2+ signals. J. Cell Sci. 126, 60-66.
41. Ko, D. C., Gordon, M. D., Jin, J. Y. and Scott, M. P. (2001). Dynamic movements of organelles containing Niemann-Pick C1 protein: NPC1 involvement in late endocytic events. Mol. Biol. Cell 12, 601-614.
42. Kobuna, H., Inoue, T., Shibata, M., Gengyo-Ando, K., Yamamoto, A., Mitani, S. and Arai, H. (2010). Multivesicular body formation requires OSBP-related proteins and cholesterol. PLoS Genet. 6, e1001055.
43. Lange, Y., Ye, J. and Chin, J. (1997). The fate of cholesterol exiting lysosomes. J. Biol. Chem. 272, 17018-17022.
44. 2+-release channel in beta cells. Sci. Signal. 2, ra23.
45. 2+/calmodulin in Early Endosome Antigen-1 localization. Mol. Biol. Cell 14, 2935-2945.
46. Lelouvier, B. and Puertollano, R. (2011). Mucolipin-3 regulates luminal calcium, acidification, and membrane fusion in the endosomal pathway. J. Biol. Chem. 286, 9826-9832.
47. Li, Y., Zhao, Y., Hu, J., Xiao, J., Qu, L., Wang, Z., Ma, D. and Chen, Y. (2013). A novel ER-localized transmembrane protein, EMC6, interacts with RAB5A and regulates cell autophagy. Autophagy 9, 150-163.
48. Liapis, A., Chen, F. W., Davies, J. P., Wang, R. and Ioannou, Y. A. (2012). MLN64 transport to the late endosome is regulated by binding to 14-3-3 via a non-canonical binding site. PLoS ONE 7, e34424.
49. Lloyd-Evans, E., Morgan, A. J., He, X., Smith, D. A., Elliot-Smith, E., Sillence, D. J., Churchill, G. C., Schuchman, E. H., Galione, A. and Platt, F. M. (2008). Niemann-Pick disease type C1 is a sphingosine storage disease that causes deregulation of lysosomal calcium. Nat. Med. 14, 1247-1255.
50. Loewen, C. J. and Levine, T. P. (2005). A highly conserved binding site in vesicleassociated membrane protein-associated protein (VAP) for the FFAT motif of lipid-binding proteins. J. Biol. Chem. 280, 14097-14104.
51. Loewen, C. J., Roy, A. and Levine, T. P. (2003). A conserved ER targeting motif in three families of lipid binding proteins and in Opi1p binds VAP. EMBO J. 22, 2025-2035.
52. 2+ released from the endoplasmic reticulum. J. Cell Sci. 126, 289-300.
53. Mayran, N., Parton, R. G. and Gruenberg, J. (2003). Annexin II regulates multivesicular endosome biogenesis in the degradation pathway of animal cells. EMBO J. 22, 3242-3253.
54. Möbius, W., van Donselaar, E., Ohno-Iwashita, Y., Shimada, Y., Heijnen, H. F., Slot, J. W. and Geuze, H. J. (2003). Recycling compartments and the internal vesicles of multivesicular bodies harbor most of the cholesterol found in the endocytic pathway. Traffic 4, 222-231.
55. 2+ signaling occurs between the endoplasmic reticulum and acidic organelles. J. Cell Biol. 200, 789-805.
56. Mukherjee, S. and Maxfield, F. R. (2004). Lipid and cholesterol trafficking in NPC. Biochim. Biophys. Acta 1685, 28-37.
57. Neefjes, J. and van der Kant, R., (2014). Stuck in traffic; an emerging theme in diseases of the nervous system. Trends Neurosci. 37, 66-76.
58. Neufeld, E. B., Cooney, A. M., Pitha, J., Dawidowicz, E. A., Dwyer, N. K., Pentchev, P. G. and Blanchette-Mackie, E. J. (1996). Intracellular trafficking of cholesterol monitored with a cyclodextrin. J. Biol. Chem. 271, 21604-21613.
59. Ordonez, M. P., Roberts, E. A., Kidwell, C. U., Yuan, S. H., Plaisted, W. C. and Goldstein, L. S. (2012). Disruption and therapeutic rescue of autophagy in a human neuronal model of Niemann Pick type C1. Hum. Mol. Genet. 21, 2651-2662.
60. Palande, K., Roovers, O., Gits, J., Verwijmeren, C., Iuchi, Y., Fujii, J., Neel, B. G., Karisch, R., Tavernier, J. and Touw, I. P. (2011). Peroxiredoxincontrolled G-CSF signalling at the endoplasmic reticulum-early endosome interface. J. Cell Sci. 124, 3695-3705.
61. Passantino, R., Cascio, C., Deidda, I., Galizzi, G., Russo, D., Spedale, G. and Guarneri, P. (2013). Identifying protein partners of CLN8, an ER-resident protein involved in neuronal ceroid lipofuscinosis. Biochim. Biophys. Acta 1833, 529-540.
62. 2+ signals by NAADP-gated two-pore channels: a role for membrane contact sites? Biochem. Soc. Trans. 40, 153-157.
63. 2+ signaling. Trends Cell Biol. 20, 277-286.
64. Pridgeon, J. W., Webber, E. A., Sha, D., Li, L. and Chin, L. S. (2009). Proteomic analysis reveals Hrs ubiquitin-interacting motif-mediated ubiquitin signaling in multiple cellular processes. FEBS J. 276, 118-131.
65. Pryor, P. R., Mullock, B. M., Bright, N. A., Gray, S. R. and Luzio, J. P. (2000). The role of intraorganellar Ca(2+) in late endosome-lysosome heterotypic fusion and in the reformation of lysosomes from hybrid organelles. J. Cell Biol. 149, 1053-1062.
66. Rocha, N., Kuijl, C., van der Kant, R., Janssen, L., Houben, D., Janssen, H., Zwart, W. and Neefjes, J. (2009). Cholesterol sensor ORP1L contacts the ER protein VAP to control Rab7-RILP-p150 Glued and late endosome positioning. J. Cell Biol. 185, 1209-1225.
67. Shen, D., Wang, X., Li, X., Zhang, X., Yao, Z., Dibble, S., Dong, X. P., Yu, T., Lieberman, A. P., Showalter, H. D. et al. (2012). Lipid storage disorders block lysosomal trafficking by inhibiting a TRP channel and lysosomal calcium release. Nat. Commun. 3, 731.
68. Sherwood, M. W., Prior, I. A., Voronina, S. G., Barrow, S. L., Woodsmith, J. D., Gerasimenko, O. V., Petersen, O. H. and Tepikin, A. V. (2007). Activation of trypsinogen in large endocytic vacuoles of pancreatic acinar cells. Proc. Natl. Acad. Sci. USA 104, 5674-5679.
69. 2+ flux through individual ion channels: theoretical considerations and limits to resolution. Cell Calcium 37, 283-299.
70. Stenmark, H. (2009). Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol. 10, 513-525.
71. Stuible, M., Abella, J. V., Feldhammer, M., Nossov, M., Sangwan, V., Blagoev, B., Park, M. and Tremblay, M. L. (2010). PTP1B targets the endosomal sorting machinery: dephosphorylation of regulatory sites on the endosomal sorting complex required for transport component STAM2. J. Biol. Chem. 285, 23899-23907.
72. Subramanian, K. and Balch, W. E. (2008). NPC1/NPC2 function as a tag team duo to mobilize cholesterol. Proc. Natl. Acad. Sci. USA 105, 15223-15224.
73. Sun, M., Goldin, E., Stahl, S., Falardeau, J. L., Kennedy, J. C., Acierno, J. S., Jr, Bove, C., Kaneski, C. R., Nagle, J., Bromley, M. C. et al. (2000). Mucolipidosis type IV is caused by mutations in a gene encoding a novel transient receptor potential channel. Hum. Mol. Genet. 9, 2471-2478.
74. Tang, N. and Marshall, W. F. (2012). Centrosome positioning in vertebrate development. J. Cell Sci. 125, 4951-4961.
75. Teuling, E., Ahmed, S., Haasdijk, E., Demmers, J., Steinmetz, M. O., Akhmanova, A., Jaarsma, D. and Hoogenraad, C. C. (2007). Motor neuron disease-associated mutant vesicle-associated membrane protein-associated protein (VAP) B recruits wild-type VAPs into endoplasmic reticulum-derived tubular aggregates. Neuroscience 27, 9801-9815.
76. 2+ leak channels, a function disrupted by familial Alzheimer's disease-linked mutations. Cell 126, 981-993.
77. Uusi-Rauva, K., Kyttä lä , A., van der Kant, R., Vesa, J., Tanhuanpää , K., Neefjes, J., Olkkonen, V. M. and Jalanko, A. (2012). Neuronal ceroid lipofuscinosis protein CLN3 interacts with motor proteins and modifies location of late endosomal compartments. Cell. Mol. Life Sci. 69, 2075-2089.
78. van der Kant, R., Zondervan, I., Janssen, L. and Neefjes, J. (2013a). Cholesterol-binding molecules MLN64 and ORP1L mark distinct late endosomes with transporters ABCA3 and NPC1. J. Lipid Res. 54, 2153-2165.
79. van der Kant, R., Fish, A., Janssen, L., Janssen, H., Krom, S., Ho, N., Brummelkamp, T., Carette, J., Rocha, N. and Neefjes, J. (2013b). Late endosomal transport and tethering are coupled processes controlled by RILP and the cholesterol sensor ORP1L. J. Cell Sci. 126, 3462-3474.
80. Vihervaara, T., Uronen, R. L., Wohlfahrt, G., Björkhem, I., Ikonen, E. and Olkkonen, V. M. (2011). Sterol binding by OSBP-related protein 1L regulates late endosome motility and function. Cell. Mol. Life Sci. 68, 537-551.
81. Wang, X., Zhang, X., Dong, X. P., Samie, M., Li, X., Cheng, X., Goschka, A., Shen, D., Zhou, Y., Harlow, J. et al. (2012). TPC proteins are phosphoinositideactivated sodium-selective ion channels in endosomes and lysosomes. Cell 151, 372-383.
82. Yip, S. C., Saha, S. and Chernoff, J. (2010). PTP1B: a double agent in metabolism and oncogenesis. Trends Biochem. Sci. 35, 442-449.
83. Zhang, M., Liu, P., Dwyer, N. K., Christenson, L. K., Fujimoto, T., Martinez, F., Comly, M., Hanover, J. A., Blanchette-Mackie, E. J. and Strauss, J. F., 3rd (2002). MLN64 mediates mobilization of lysosomal cholesterol to steroidogenic mitochondria. J. Biol. Chem. 277, 33300-33310.