Lysosomal Ca2+ homeostasis: Role in pathogenesis of lysosomal storage diseases

Cell Calcium

Volumn 50, Issue 2, 2011, Pages 200-205

  Lloyd Evans, Emyr ^a   Platt, Frances M ^b  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Lysosomal calcium; Lysosomal storage disease; MLIV; Mucolipidosis type IV; NAADP; Niemann Pick; NPC1

Indexed keywords

CALCIUM CHANNEL; MEMBRANE PROTEIN; NICOTINIC ACID ADENINE DINUCLEOTIDE PHOSPHATE; TRPML1 PROTEIN; UNCLASSIFIED DRUG;

CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CALCIUM TRANSPORT; CHEDIAK HIGASHI SYNDROME; ENDOCYTOSIS; GENE MUTATION; HUMAN; LIPID STORAGE; LYSOSOME; LYSOSOME STORAGE DISEASE; MUCOLIPIDOSIS; MUCOLIPIDOSIS TYPE 4; NIEMANN PICK DISEASE; PRIORITY JOURNAL; REVIEW;

EID: 80051470524     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2011.03.010     Document Type: Review

References (60)

1. Galione A., Morgan A.J., Arredouani A., Davis L.C., Rietdorf K., Ruas M., Parrington J. NAADP as an intracellular messenger regulating lysosomal calcium-release channels. Biochem. Soc. Trans. 2010, 38:1424-1431.
2. Lloyd-Evans E., Waller-Evans H., Peterneva K., Platt F.M. Endolysosomal calcium regulation and disease. Biochem. Soc. Trans. 2010, 38:1458-1464.
3. Patel S., Docampo R. Acidic calcium stores open for business: expanding the potential for intracellular Ca2+ signaling. Trends Cell Biol. 2010, 20:277-286.
4. Christensen K.A., Myers J.T., Swanson J.A. pH-dependent regulation of lysosomal calcium in macrophages. J. Cell. Sci. 2002, 115:599-607.
5. 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., Platt F.M. Niemann-Pick disease type C1 is a sphingosine storage disease that causes deregulation of lysosomal calcium. Nat. Med. 2008, 14:1247-1255.
6. Churchill G.C., Okada Y., Thomas J.M., Genazzani A.A., Patel S., Galione A. NAADP mobilizes Ca(2+) from reserve granules, lysosome-related organelles, in sea urchin eggs. Cell 2002, 111:703-708.
7. Brailoiu E., Churamani D., Cai X., Schrlau M.G., Brailoiu G.C., Gao X., Hooper R., Boulware M.J., Dun N.J., Marchant J.S., Patel S. Essential requirement for two-pore channel 1 in NAADP-mediated calcium signaling. J. Cell Biol. 2009, 186:201-209.
8. Brailoiu E., Hooper R., Cai X., Brailoiu G.C., Keebler M.V., Dun N.J., Marchant J.S., Patel S. An ancestral deuterostome family of two-pore channels mediates nicotinic acid adenine dinucleotide phosphate-dependent calcium release from acidic organelles. J. Biol. Chem. 2010, 285:2897-2901.
9. Calcraft P.J., Ruas M., Pan Z., Cheng X., Arredouani A., Hao X., Tang J., Rietdorf K., Teboul L., Chuang K.T., Lin P., Xiao R., Wang C., Zhu Y., Lin Y., Wyatt C.N., Parrington J., Ma J., Evans A.M., Galione A., Zhu M.X. NAADP mobilizes calcium from acidic organelles through two-pore channels. Nature 2009, 459:596-600.
10. Ruas M., Rietdorf K., Arredouani A., Davis L.C., Lloyd-Evans E., Koegel H., Funnell T.M., Morgan A.J., Ward J.A., Watanabe K., Cheng X., Churchill G.C., Zhu M.X., Platt F.M., Wessel G.M., Parrington J., Galione A. Purified TPC isoforms form NAADP receptors with distinct roles for Ca(2+) signaling and endolysosomal trafficking. Curr. Biol. 2010.
11. Pryor P.R., Mullock B.M., Bright N.A., Gray S.R., Luzio J.P. The role of intraorganellar Ca(2+) in late endosome-lysosome heterotypic fusion and in the reformation of lysosomes from hybrid organelles. J. Cell Biol. 2000, 149:1053-1062.
12. Gerasimenko J.V., Tepikin A.V., Petersen O.H., Gerasimenko O.V. Calcium uptake via endocytosis with rapid release from acidifying endosomes. Curr. Biol. 1998, 8:1335-1338.
13. Adachi T., Arai K., Ohkuma S. A comparative study of (Ca(2+)-Mg2+)-ATPase on the lysosomal membrane and ecto-ATPase on the plasma membrane from rat liver. Biol. Pharm. Bull. 1996, 19:1291-1297.
14. Ezaki J., Himeno M., Kato K. Purification and characterization of (Ca2+-Mg2+)-ATPase in rat liver lysosomal membranes. J. Biochem. (Tokyo) 1992, 112:33-39.
15. Lemons R.M., Thoene J.G. Mediated calcium transport by isolated human fibroblast lysosomes. J. Biol. Chem. 1991, 266:14378-14382.
16. Styrt B., Pollack C.R., Klempner M.S. An abnormal calcium uptake pump in Chediak-Higashi neutrophil lysosomes. J. Leukoc. Biol. 1988, 44:130-135.
17. Bach G. Mucolipin 1: endocytosis and cation channel-a review. Pflugers Arch. 2005, 451:313-317.
18. Lloyd-Evans E., Peterneva K., Lewis A., Churchill G., Platt F. Abnormal lysosomal calcium homeostasis in mucolipidosis type IV. Mol. Genet. Metab. 2008, 93:S29-S30.
19. Lloyd-Evans E., Platt F.M. Lipids on trial: the search for the offending metabolite in Niemann-Pick type C disease. Traffic 2010, 11:419-428.
20. Vanier M.T. Lipid changes in Niemann-Pick disease type C brain: personal experience and review of the literature. Neurochem. Res. 1999, 24:481-489.
21. Ko D.C., Gordon M.D., Jin J.Y., Scott M.P. Dynamic movements of organelles containing Niemann-Pick C1 protein: NPC1 involvement in late endocytic events. Mol. Biol. Cell 2001, 12:601-614.
22. Huwiler A., Kolter T., Pfeilschifter J., Sandhoff K. Physiology and pathophysiology of sphingolipid metabolism and signaling. Biochim. Biophys. Acta 2000, 1485:63-99.
23. Kagedal K., Zhao M., Svensson I., Brunk U.T. Sphingosine-induced apoptosis is dependent on lysosomal proteases. Biochem. J. 2001, 359:335-343.
24. Colina C., Cervino V., Benaim G. Ceramide and sphingosine have an antagonistic effect on the plasma-membrane Ca2+-ATPase from human erythrocytes. Biochem. J. 2002, 362:247-251.
25. Bottega R., Epand R.M., Ball E.H. Inhibition of protein kinase C by sphingosine correlates with the presence of positive charge. Biochem. Biophys. Res. Commun. 1989, 164:102-107.
26. Shearman M.S., Sekiguchi K., Nishizuka Y. Modulation of ion channel activity: a key function of the protein kinase C enzyme family. Pharmacol. Rev. 1989, 41:211-237.
27. Rodriguez-Lafrasse C., Rousson R., Valla S., Antignac P., Louisot P., Vanier M.T. Modulation of protein kinase C by endogenous sphingosine: inhibition of phorbol dibutyrate binding in Niemann-Pick C fibroblasts. Biochem. J. 1997, 325(Pt 3):787-791.
28. Naylor E., Arredouani A., Vasudevan S.R., Lewis A.M., Parkesh R., Mizote A., Rosen D., Thomas J.M., Izumi M., Ganesan A., Galione A., Churchill G.C. Identification of a chemical probe for NAADP by virtual screening. Nat. Chem. Biol. 2009, 5:220-226.
29. Mayran N., Parton R.G., Gruenberg J. Annexin II regulates multivesicular endosome biogenesis in the degradation pathway of animal cells. EMBO J. 2003, 22:3242-3253.
30. Masson M., Spezzatti B., Chapman J., Battisti C., Baumann N. Calmodulin antagonists chlorpromazine and W-7 inhibit exogenous cholesterol esterification and sphingomyelinase activity in human skin fibroblast cultures. Similarities between drug-induced and Niemann-Pick type C lipidoses. J. Neurosci. Res. 1992, 31:84-88.
31. Artalejo C.R., Elhamdani A., Palfrey H.C. Calmodulin is the divalent cation receptor for rapid endocytosis, but not exocytosis, in adrenal chromaffin cells. Neuron 1996, 16:195-205.
32. Lee H., Lee J.K., Min W.K., Bae J.H., He X., Schuchman E.H., Bae J.S., Jin H.K. Bone marrow-derived mesenchymal stem cells prevent the loss of Niemann-Pick type C mouse Purkinje neurons by correcting sphingolipid metabolism and increasing sphingosine-1-phosphate. Stem Cells 2010, 28:821-831.
33. Shiflett S.L., Kaplan J., Ward D.M. Chediak-Higashi syndrome: a rare disorder of lysosomes and lysosome related organelles. Pigment Cell Res. 2002, 15:251-257.
34. Burgess A., Mornon J.P., de Saint-Basile G., Callebaut I. A concanavalin A-like lectin domain in the CHS1/LYST protein, shared by members of the BEACH family. Bioinformatics 2009, 25:1219-1222.
35. Huizing M., Helip-Wooley A., Westbroek W., Gunay-Aygun M., Gahl W.A. Disorders of lysosome-related organelle biogenesis: clinical and molecular genetics. Annu. Rev. Genomics Hum. Genet. 2008, 9:359-386.
36. Huynh C., Roth D., Ward D.M., Kaplan J., Andrews N.W. Defective lysosomal exocytosis and plasma membrane repair in Chediak-Higashi/beige cells. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:16795-16800.
37. Lopez J.J., Redondo P.C., Salido G.M., Pariente J.A., Rosado J.A. Two distinct Ca2+ compartments show differential sensitivity to thrombin, ADP and vasopressin in human platelets. Cell. Signal. 2006, 18:373-381.
38. Shiraishi M., Kawashima S., Moroi M., Shin Y., Morita T., Horii Y., Ikeda M., Ito K. A defect in collagen receptor-Ca2+ signaling system in platelets from cattle with Chediak-Higashi syndrome. Thromb. Haemost. 2002, 87:334-341.
39. Altarescu G., Sun M., Moore D.F., Smith J.A., Wiggs E.A., Solomon B.I., Patronas N.J., Frei K.P., Gupta S., Kaneski C.R., Quarrell O.W., Slaugenhaupt S.A., Goldin E., Schiffmann R. The neurogenetics of mucolipidosis type IV. Neurology 2002, 59:306-313.
40. Bach G. Mucolipidosis type IV. Mol. Genet. Metab. 2001, 73:197-203.
41. Chen C.S., Bach G., Pagano R.E. Abnormal transport along the lysosomal pathway in mucolipidosis, type IV disease. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:6373-6378.
42. Thompson E.G., Schaheen L., Dang H., Fares H. Lysosomal trafficking functions of mucolipin-1 in murine macrophages. BMC Cell Biol. 2007, 8:54.
43. Luzio J.P., Pryor P.R., Gray S.R., Gratian M.J., Piper R.C., Bright N.A. Membrane traffic to and from lysosomes. Biochem. Soc. Symp. 2005, 77-86.
44. Piper R.C., Luzio J.P. Cuppling calcium to lysosomal biogenesis. Trends Cell Biol. 2004, 14:471-473.
45. Dong X.P., Cheng X., Mills E., Delling M., Wang F., Kurz T., Xu H. The type IV mucolipidosis-associated protein TRPML1 is an endolysosomal iron release channel. Nature 2008, 455:992-996.
46. LaPlante J.M., Falardeau J., Sun M., Kanazirska M., Brown E.M., Slaugenhaupt S.A., Vassilev P.M. Identification and characterization of the single channel function of human mucolipin-1 implicated in mucolipidosis type IV, a disorder affecting the lysosomal pathway. FEBS Lett. 2002, 532:183-187.
47. Raychowdhury M.K, Gonzalez-Perrett S., Montalbetti N., Timpanaro G.A., Chasan B., Goldmann W.H., Stahl S., Cooney A., Goldin E., Cantiello H.F. Molecular pathophysiology of mucolipidosis type IV: pH dysregulation of the mucolipin-1 cation channel. Hum. Mol. Genet. 2004, 13:617-627.
48. Bach G., Chen C.S., Pagano R.E. Elevated lysosomal pH in mucolipidosis type IV cells. Clin. Chim. Acta 1999, 280:173-179.
49. Pryor P.R., Reimann F., Gribble F.M., Luzio J.P. Mucolipin-1 is a lysosomal membrane protein required for intracellular lactosylceramide traffic. Traffic 2006, 7:1388-1398.
50. Soyombo A.A., Tjon-Kon-Sang S., Rbaibi Y., Bashllari E., Bisceglia J., Muallem S., Kiselyov K. TRP-ML1 regulates lysosomal pH and acidic lysosomal lipid hydrolytic activity. J. Biol. Chem. 2006, 281:7294-7301.
51. Pitt S.J., Funnell T.M., Sitsapesan M., Venturi E., Rietdorf K., Ruas M., Ganesan A., Gosain R., Churchill G.C., Zhu M.X., Parrington J., Galione A., Sitsapesan R. TPC2 is a novel NAADP-sensitive Ca2+ release channel, operating as a dual sensor of luminal pH and Ca2+. J. Biol. Chem. 2010, 285:35039-35046.
52. Zhang F., Jin S., Yi F., Li P.L. TRP-ML1 functions as a lysosomal NAADP-sensitive Ca2+ release channel in coronary arterial myocytes. J. Cell. Mol. Med. 2009, 13:3174-3185.
53. Dickinson G.D., Churchill G.C., Brailoiu E., Patel S. Deviant nicotinic acid adenine dinucleotide phosphate (NAADP)-mediated Ca2+ signaling upon lysosome proliferation. J. Biol. Chem. 2010, 285:13321-13325.
54. Jeyakumar M., Dwek R.A., Butters T.D., Platt F.M. Storage solutions: treating lysosomal disorders of the brain. Nat. Rev. Neurosci. 2005, 6:713-725.
55. Sulem P., Gudbjartsson D.F., Stacey S.N., Helgason A., Rafnar T., Jakobsdottir M., Steinberg S., Gudjonsson S.A., Palsson A., Thorleifsson G., Palsson S., Sigurgeirsson B., Thorisdottir K., Ragnarsson R., Benediktsdottir K.R., Aben K.K., Vermeulen S.H., Goldstein A.M., Tucker M.A., Kiemeney L.A., Olafsson J.H., Gulcher J., Kong A., Thorsteinsdottir U., Stefansson K. Two newly identified genetic determinants of pigmentation in Europeans. Nat. Genet. 2008, 40:835-837.
56. Khan S.Y., Riazuddin S., Tariq M., Anwar S., Shabbir M.I., Riazuddin S.A., Khan S.N., Husnain T., Ahmed Z.M., Friedman T.B. Autosomal recessive nonsyndromic deafness locus DFNB63 at chromosome 11q13.2-q13.3. Hum. Genet. 2007, 120:789-793.
57. Zeigler M., Bargal R., Suri V., Meidan B., Bach G. Mucolipidosis type IV: accumulation of phospholipids and gangliosides in cultured amniotic cells. A tool for prenatal diagnosis. Prenat. Diagn. 1992, 12:1037-1042.
58. Bargal R., Bach G. Phospholipids accumulation in mucolipidosis IV cultured fibroblasts. J. Inherit. Metab. Dis. 1988, 11:144-150.
59. Bach G., Zeigler M., Kohn G. Biochemical investigations of cultured amniotic fluid cells in mucolipidosis type IV. Clin. Chim. Acta 1980, 106:121-128.
60. Goldin E., Blanchette-Mackie E.J., Dwyer N.K., Pentchev P.G., Brady R.O. Cultured skin fibroblasts derived from patients with mucolipidosis 4 are auto-fluorescent. Pediatr. Res. 1995, 37:687-692.