Lipid storage disorders block lysosomal trafficking by inhibiting a TRP channel and lysosomal calcium release

Dongbiao Shen; Xiang Wang; Xiaoli Zhang; Zepeng Yao; Shannon Dibble; Xian-Ping Dong; Ting Yu; Andrew P. Lieberman; Hollis D. Showalter; Haoxing Xu

doi:10.1038/ncomms1735

journal article Mar 13, 2012

Lipid storage disorders block lysosomal trafficking by inhibiting a TRP channel and lysosomal calcium release

Dongbiao Shen Xiang Wang

Xiaoli Zhang

Zepeng Yao Shannon Dibble Xian-Ping Dong Ting Yu

Andrew P. Lieberman Hollis D. Showalter Haoxing Xu

Nature Communications Vol. 3 No. 1 · Springer Science and Business Media LLC

View at Publisher Save 10.1038/ncomms1735

Topics

No keywords indexed for this article. Browse by subject →

References

39

[1]

de Duve, C. The lysosome turns fifty. Nat. Cell Biol. 7, 847–849 (2005). 10.1038/ncb0905-847

[2]

Parkinson-Lawrence, E. J. et al. Lysosomal storage disease: revealing lysosomal function and physiology. Physiology (Bethesda) 25, 102–115 (2010).

[3]

Schuchman, E. H. Acid sphingomyelinase, cell membranes and human disease: lessons from Niemann-Pick disease. FEBS Lett. 584, 1895–1900 (2010). 10.1016/j.febslet.2009.11.083

[4]

Rosenbaum, A. I. & Maxfield, F. R. Niemann-Pick type C disease: molecular mechanisms and potential therapeutic approaches. J. Neurochem. 116, 789–795 (2011). 10.1111/j.1471-4159.2010.06976.x

[5]

Vitner, E. B., Platt, F. M. & Futerman, A. H. Common and uncommon pathogenic cascades in lysosomal storage diseases. J. Biol. Chem. 285, 20423–20427 (2010). 10.1074/jbc.r110.134452

[6]

Puri, V. et al. Cholesterol modulates membrane traffic along the endocytic pathway in sphingolipid-storage diseases. Nat. Cell Biol. 1, 386–388 (1999). 10.1038/14084

[7]

Kiselyov, K., Yamaguchi, S., Lyons, C. W. & Muallem, S. Aberrant Ca2+ handling in lysosomal storage disorders. Cell Calcium 47, 103–111 (2010). 10.1016/j.ceca.2009.12.007

[8]

Pryor, P. R., Reimann, F., Gribble, F. M. & Luzio, J. P. Mucolipin-1 is a lysosomal membrane protein required for intracellular lactosylceramide traffic. Traffic 7, 1388–1398 (2006). 10.1111/j.1600-0854.2006.00475.x

[9]

Vergarajauregui, S. & Puertollano, R. Two di-leucine motifs regulate trafficking of mucolipin-1 to lysosomes. Traffic 7, 337–353 (2006). 10.1111/j.1600-0854.2006.00387.x

[10]

Thompson, E. G., Schaheen, L., Dang, H. & Fares, H. Lysosomal trafficking functions of mucolipin-1 in murine macrophages. BMC Cell Biol. 8, 54 (2007). 10.1186/1471-2121-8-54

[11]

Dong, X. P. et al. The type IV mucolipidosis-associated protein TRPML1 is an endolysosomal iron release channel. Nature 455, 992–996 (2008). 10.1038/nature07311

[12]

Venkatachalam, K. et al. Motor deficit in a Drosophila model of mucolipidosis type IV due to defective clearance of apoptotic cells. Cell 135, 838–851 (2008). 10.1016/j.cell.2008.09.041

[13]

Cheng, X., Shen, D., Samie, M. & Xu, H. Mucolipins: intracellular TRPML1-3 channels. FEBS Lett. 584, 2013–2021 (2010). 10.1016/j.febslet.2009.12.056

[14]

Dong, X. P. et al. PI(3,5)P(2) controls membrane traffic by direct activation of mucolipin Ca release channels in the endolysosome. Nat. Commun. 1, 38 (2010). 10.1038/ncomms1037

[15]

Shen, D., Wang, X. & Xu, H. Pairing phosphoinositides with calcium ions in endolysosomal dynamics: phosphoinositides control the direction and specificity of membrane trafficking by regulating the activity of calcium channels in the endolysosomes. Bioessays 33, 448–457 (2011). 10.1002/bies.201000152

[16]

Bargal, R. et al. Identification of the gene causing mucolipidosis type IV. Nat. Genet. 26, 118–123 (2000). 10.1038/79095

[17]

Bassi, M. T. et al. Cloning of the gene encoding a novel integral membrane protein, mucolipidin-and identification of the two major founder mutations causing mucolipidosis type IV. Am. J. Hum. Genet. 67, 1110–1120 (2000). 10.1016/s0002-9297(07)62941-3

[18]

Sun, M. et al. Mucolipidosis type IV is caused by mutations in a gene encoding a novel transient receptor potential channel. Hum. Mol. Genet. 9, 2471–2478 (2000). 10.1093/hmg/9.17.2471

[19]

Grimm, C. et al. A helix-breaking mutation in TRPML3 leads to constitutive activity underlying deafness in the varitint-waddler mouse. Proc. Natl Acad. Sci. USA 104, 19583–19588 (2007). 10.1073/pnas.0709846104

[20]

Xu, H., Delling, M., Li, L., Dong, X. & Clapham, D. E. Activating mutation in a mucolipin transient receptor potential channel leads to melanocyte loss in varitint-waddler mice. Proc. Natl Acad. Sci. USA 104, 18321–18326 (2007). 10.1073/pnas.0709096104

[21]

Grimm, C. et al. Small molecule activators of TRPML3. Chem. Biol. 17, 135–148 (2010). 10.1016/j.chembiol.2009.12.016

[22]

Zhang, Y. et al. Loss of Vac14, a regulator of the signaling lipid phosphatidylinositol 3,5-bisphosphate, results in neurodegeneration in mice. Proc. Natl Acad. Sci. USA 104, 17518–17523 (2007). 10.1073/pnas.0702275104

[23]

Abe, K. & Puertollano, R. Role of TRP channels in the regulation of the endosomal pathway. Physiology (Bethesda) 26, 14–22 (2011).

[24]

Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators

Lin Tian, S Andrew Hires, Tianyi Mao et al.

Nature Methods 2009 10.1038/nmeth.1398

[25]

Lloyd-Evans, E. et al. Niemann-Pick disease type C1 is a sphingosine storage disease that causes deregulation of lysosomal calcium. Nat. Med. 14, 1247–1255 (2008). 10.1038/nm.1876

[26]

Cadigan, K. M., Spillane, D. M. & Chang, T. Y. Isolation and characterization of Chinese hamster ovary cell mutants defective in intracellular low density lipoprotein-cholesterol trafficking. J. Cell Biol. 110, 295–308 (1990). 10.1083/jcb.110.2.295

[27]

Cruz, J. C., Sugii, S., Yu, C. & Chang, T. Y. Role of Niemann-Pick type C1 protein in intracellular trafficking of low density lipoprotein-derived cholesterol. J. Biol. Chem. 275, 4013–4021 (2000). 10.1074/jbc.275.6.4013

[28]

Liscum, L. & Faust, J. R. The intracellular transport of low density lipoprotein-derived cholesterol is inhibited in Chinese hamster ovary cells cultured with 3-beta-[2-(diethylamino)ethoxy]androst-5-en-17-one. J. Biol. Chem. 264, 11796–11806 (1989). 10.1016/s0021-9258(18)80136-3

[29]

Lloyd-Evans, E. & Platt, F. M. Lipids on trial: the search for the offending metabolite in Niemann-Pick type C disease. Traffic 11, 419–428 (2010). 10.1111/j.1600-0854.2010.01032.x

[30]

Hurwitz, R., Ferlinz, K. & Sandhoff, K. The tricyclic antidepressant desipramine causes proteolytic degradation of lysosomal sphingomyelinase in human fibroblasts. Biol. Chem. Hoppe Seyler 375, 447–450 (1994). 10.1515/bchm3.1994.375.7.447

[31]

Kornhuber, J. et al. Identification of new functional inhibitors of acid sphingomyelinase using a structure-property-activity relation model. J. Med. Chem. 51, 219–237 (2008). 10.1021/jm070524a

[32]

Pagano, R. E. & Chen, C. S. Use of BODIPY-labeled sphingolipids to study membrane traffic along the endocytic pathway. Ann. N Y Acad. Sci. 845, 152–160 (1998). 10.1111/j.1749-6632.1998.tb09668.x

[33]

Kolter, T. & Sandhoff, K. Lysosomal degradation of membrane lipids. FEBS Lett. 584, 1700–1712 (2010). 10.1016/j.febslet.2009.10.021

[34]

Devlin, C. et al. Improvement in lipid and protein trafficking in Niemann-Pick C1 cells by correction of a secondary enzyme defect. Traffic 11, 601–615 (2010). 10.1111/j.1600-0854.2010.01046.x

[35]

Chen, C. S., Bach, G. & Pagano, R. E. Abnormal transport along the lysosomal pathway in mucolipidosis, type IV disease. Proc. Natl Acad. Sci. USA 95, 6373–6378 (1998). 10.1073/pnas.95.11.6373

[36]

Chen, C. S., Patterson, M. C., Wheatley, C. L., O'Brien, J. F. & Pagano, R. E. Broad screening test for sphingolipid-storage diseases. Lancet 354, 901–905 (1999). 10.1016/s0140-6736(98)10034-x

[37]

Venugopal, B. et al. Neurologic, gastric, and opthalmologic pathologies in a murine model of mucolipidosis type IV. Am. J. Hum. Genet. 81, 1070–1083 (2007). 10.1086/521954

[38]

Link, T. M. et al. TRPV2 has a pivotal role in macrophage particle binding and phagocytosis. Nat. Immunol. 11, 232–239 (2010). 10.1038/ni.1842

[39]

Calcraft, P. J. et al. NAADP mobilizes calcium from acidic organelles through two-pore channels. Nature 459, 596–600 (2009). 10.1038/nature08030

Cited By

443

Hyperosmotic Stress Promotes the Nuclear Translocation of TFEB in Tubular Epithelial Cells Depending on Intracellular Ca2+ Signals via TRPML Channels

Takashi Miyano, Atsushi Suzuki · 2025

Cellular and Molecular Bioengineeri...

Activation of lysosomal Ca2+ channels mitigates mitochondrial damage and oxidative stress

Xinghua Feng, Weijie Cai · 2024

The Journal of cell biology

Podocyte Lysosome Dysfunction in Chronic Glomerular Diseases

Guangbi Li, Jason Kidd · 2020

International Journal of Molecular...

The aging lysosome: An essential catalyst for late-onset neurodegenerative diseases

Ralph A. Nixon · 2020

Biochimica et Biophysica Acta (BBA)...

TRP Channels Regulation of Rho GTPases in Brain Context and Diseases

Boris Lavanderos, Ian Silva · 2020

Frontiers in Cell and Developmental...

Control of lysosomal TRPML1 channel activity and exosome release by acid ceramidase in mouse podocytes

Guangbi Li, Dandan HUANG · 2019

American Journal of Physiology-Cell...

Lysosomal Physiology

Haoxing Xu, Dejian Ren · 2015

Annual Review of Physiology

Metrics

443

Citations

39

References

Details

Published: Mar 13, 2012
Vol/Issue: 3(1)
License: View

Authors

Cite This Article

Dongbiao Shen, Xiang Wang, Xiaoli Zhang, et al. (2012). Lipid storage disorders block lysosomal trafficking by inhibiting a TRP channel and lysosomal calcium release. Nature Communications, 3(1). https://doi.org/10.1038/ncomms1735

Lipid storage disorders block lysosomal trafficking by inhibiting a TRP channel and lysosomal calcium release

You May Also Like