Pathological roles of the VEGF/SphK pathway in Niemann-Pick type C neurons

Nature Communications

Volumn 5, Issue , 2014, Pages

  Lee, Hyun ^a,b   Lee, Jong Kil ^a,c   Park, Min Hee ^a,c   Hong, Yu Ri ^a,b   Marti, Hugo H ^d   Kim, Hyongbum ^e   Okada, Yohei ^f   Otsu, Makoto ^g   Seo, Eul Ju ^h   Park, Jae Hyung ⁱ   Bae, Jae Hoon ⁱ   Okino, Nozomu ^j   He, Xingxuan ^k   Schuchman, Edward H ^k   Bae, Jae Sung ^a,c   Jin, Hee Kyung ^a,b  

^a Kyungpook National University   (South Korea)

^b Cell and Matrix Research Institute   (South Korea)

^c Department of Physiology   (South Korea)

^d UNIVERSITY OF HEIDELBERG   (Germany)

^e Hanyang University   (South Korea)

^f KEIO UNIVERSITY   (Japan)

^g THE UNIVERSITY OF TOKYO   (Japan)

^h University of Ulsan College of Medicine   (South Korea)

ⁱ Keimyung University   (South Korea)

^j KYUSHU UNIVERSITY   (Japan)

^k MOUNT SINAI SCHOOL OF MEDICINE   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

BETA N ACETYLHEXOSAMINIDASE; CURCUMIN; LACTATE DEHYDROGENASE; SPHINGOSINE KINASE; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2; VATALANIB; CARRIER PROTEIN; MEMBRANE PROTEIN; MICROSPHERE; NPC1 PROTEIN, HUMAN; PHTHALAZINE DERIVATIVE; PROTEIN KINASE INHIBITOR; PYRIDINE DERIVATIVE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SKIP PROTEIN, HUMAN; SMALL INTERFERING RNA; SPHINGOSINE; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN; VEGFR2 PROTEIN, MOUSE;

CELL ORGANELLE; DISEASE PREVALENCE; GROWTH; NEUROLOGY; PATHOGENICITY; PATHOLOGY; RODENT;

ANIMAL CELL; ARTICLE; AUTOLYSOSOME; AUTOPHAGOSOME; AUTOPHAGY; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; CELL SURVIVAL; CELLULAR DISTRIBUTION; CEREBELLUM; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FIBROBLAST; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; LASER CAPTURE MICRODISSECTION; LIPID STORAGE; LYSOSOME; MALE; MOUSE; NIEMANN PICK DISEASE; NONHUMAN; PATHOGENESIS; PLURIPOTENT STEM CELL; PROTEIN EXPRESSION; PURKINJE CELL; SIGNAL TRANSDUCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; BIOSYNTHESIS; BONE MARROW CELL; CELL LINE; CYTOLOGY; GENETICS; MESENCHYMAL STROMA CELL; METABOLISM; RNA INTERFERENCE; SCID MOUSE; TRANSGENIC MOUSE;

MUS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; AUTOPHAGY; BONE MARROW CELLS; CARRIER PROTEINS; CELL LINE; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MALE; MEMBRANE GLYCOPROTEINS; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED BALB C; MICE, SCID; MICE, TRANSGENIC; MICROSPHERES; NIEMANN-PICK DISEASE, TYPE C; PHTHALAZINES; PROTEIN KINASE INHIBITORS; PURKINJE CELLS; PYRIDINES; RNA INTERFERENCE; RNA, SMALL INTERFERING; SPHINGOSINE; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84923358519     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6514     Document Type: Article

References (45)

1. Vanier, M. T. & Millat, G. Niemann-Pick disease type C. Clin. Genet. 64, 269-281 (2003).
2. Vanier, M. T. Lipid changes in Niemann-Pick disease type C brain: personal experience and review of the literature. Neurochem. Res. 24, 481-489 (1999).
3. Blom, T., Li, Z., Bittman, R., Somerharju, P. & Ikonen, E. Tracking sphingosine metabolism and transport in sphingolipidoses: NPC1 deficiency as a test case. Traffic 13, 1234-1243 (2012).
4. 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).
5. Bae, J. S. et al. Bone marrow-derived mesenchymal stem cells promote neuronal networks with functional synaptic transmission after transplantation into mice with neurodegeneration. Stem Cells 25, 1307-1316 (2007).
6. Bae, J. S. et al. Neurodegeneration augments the ability of bone marrow-derived mesenchymal stem cells to fuse with Purkinje neurons in Niemann-Pick type C mice. Hum. Gene Ther. 16, 1006-1011 (2005).
7. Lee, H. et al. 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 28, 821-831 (2010).
8. Le Stunff, H., Peterson, C., Liu, H., Milstien, S. & Spiegel, S. Sphingosine-1- phosphate and lipid phosphohydrolases. Biochim. Biophys. Acta 1582, 8-17 (2002).
9. Shu, X., Wu, W., Mosteller, R. D. & Broek, D. Sphingosine kinase mediates vascular endothelial growth factor-induced activation of ras and mitogenactivated protein kinases. Mol. Cell. Biol. 22, 7758-7768 (2002).
10. Xia, P. et al. Tumor necrosis factor-alpha induces adhesion molecule expression through the sphingosine kinase pathway. Proc. Natl Acad. Sci. USA 95, 14196-14201 (1998).
11. Olivera, A. & Spiegel, S. Sphingosine-1-phosphate as second messenger in cell proliferation induced by PDGF and FCS mitogens. Nature 365, 557-560 (1993).
12. Edsall, L. C., Pirianov, G. G. & Spiegel, S. Involvement of sphingosine 1-phosphate in nerve growth factor-mediated neuronal survival and differentiation. J. Neurosci. 17, 6952-6960 (1997).
13. Spiegel, S. & Milstien, S. Sphingosine-1-phosphate: an enigmatic signalling lipid. Nat. Rev. Mol. Cell Biol. 4, 397-407 (2003).
14. Wang, Y. et al. VEGF overexpression induces post-ischaemic neuroprotection, but facilitates haemodynamic steal phenomena. Brain 128, 52-63 (2005).
15. Olsson, A. K., Dimberg, A., Kreuger, J. & Claesson-Welsh, L. VEGF receptor signalling - in control of vascular function. Nat. Rev. Mol. Cell Biol. 7, 359-371 (2006).
16. Cvetanovic, M., Patel, J. M., Marti, H. H., Kini, A. R. & Opal, P. Vascular endothelial growth factor ameliorates the ataxic phenotype in a mouse model of spinocerebellar ataxia type 1. Nat. Med. 17, 1445-1447 (2011).
17. Wood, J. M. et al. PTK787/ZK 222584, a novel and potent inhibitor of vascular endothelial growth factor receptor tyrosine kinases, impairs vascular endothelial growth factor-induced responses and tumor growth after oral administration. Cancer Res. 60, 2178-2189 (2000).
18. Foraker, J. E. et al. Cross-talk between human mesenchymal stem/progenitor cells (MSCs) and rat hippocampal slices in LPS-stimulated cocultures: the MSCs are activated to secrete prostaglandin E2. J. Neurochem. 119, 1052-1063 (2011).
19. Ruiz de Almodovar, C. et al. Matrix-binding vascular endothelial growth factor (VEGF) isoforms guide granule cell migration in the cerebellum via VEGF receptor Flk1. J. Neurosci. 30, 15052-15066 (2010).
20. Sentilhes, L. et al. Vascular endothelial growth factor and its high-affinity receptor (VEGFR-2) are highly expressed in the human forebrain and cerebellum during development. J. Neuropathol. Exp. Neurol. 69, 111-128 (2010).
21. Folkman, J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat. Med. 1, 27-31 (1995).
22. Ko, D. C. et al. Cell-autonomous death of cerebellar purkinje neurons with autophagy in Niemann-Pick type C disease. PLoS Genet. 1, 81-95 (2005).
23. Rubinsztein, D. C. et al. In search of an 'autophagomometer'. Autophagy 5, 585-589 (2009).
24. Settembre, C. et al. TFEB links autophagy to lysosomal biogenesis. Science 332, 1429-1433 (2011).
25. Pankiv, S. et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 282, 24131-24145 (2007).
26. Bilmen, J. G., Khan, S. Z., Javed, M. H. & Michelangeli, F. Inhibition of the SERCA Ca2+ pumps by curcumin. Curcumin putatively stabilizes the interaction between the nucleotide-binding and phosphorylation domains in the absence of ATP. Eur. J. Biochem. 268, 6318-6327 (2001).
27. Chen, F. W., Li, C. & Ioannou, Y. A. Cyclodextrin induces calcium-dependent lysosomal exocytosis. PLoS ONE 5, e15054 (2010).
28. Trilck, M. et al. Niemann-Pick type C1 patient-specific induced pluripotent stem cells display disease specific hallmarks. Orphanet J. Rare Dis. 8, 144 (2013).
29. Maetzel, D. et al. Genetic and chemical correction of cholesterol accumulation and impaired autophagy in hepatic and neural cells derived from Niemann- Pick Type C patient-specific iPS cells. Stem Cell Rep. 2, 866-880 (2014).
30. Yu, D. et al. Niemann-Pick disease type C: induced pluripotent stem cellderived neuronal cells for modeling neural disease and evaluating drug efficacy. J. Biomol. Screen. 19, 1164-1173 (2014).
31. Liscum, L. & Faust, J. R. Low density lipoprotein (LDL)-mediated suppression of cholesterol synthesis and LDL uptake is defective in Niemann-Pick type C fibroblasts. J. Biol. Chem. 262, 17002-17008 (1987).
32. Griffin, L. D., Gong, W., Verot, L. & Mellon, S. H. Niemann-Pick type C disease involves disrupted neurosteroidogenesis and responds to allopregnanolone. Nat. Med. 10, 704-711 (2004).
33. Meske, V., Erz, J., Priesnitz, T. & Ohm, T. G. The autophagic defect in Niemann-Pick disease type C neurons differs from somatic cells and reduces neuronal viability. Neurobiol. Dis. 64, 88-97 (2014).
34. Liao, G. et al. Cholesterol accumulation is associated with lysosomal dysfunction and autophagic stress in Npc1-/- mouse brain. Am. J. Pathol. 171, 962-975 (2007).
35. Panyam, J. & Labhasetwar, V. Biodegradable nanoparticles for drug and gene delivery to cells and tissue. Adv. Drug Deliv. Rev. 55, 329-347 (2003).
36. Aebischer, P. & Ridet, J. Recombinant proteins for neurodegenerative diseases: the delivery issue. Trends Neurosci. 24, 533-540 (2001).
37. Loftus, S. K. et al. Murine model of Niemann-Pick C disease: mutation in a cholesterol homeostasis gene. Science 277, 232-235 (1997).
38. Takahashi, K. et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861-872 (2007).
39. Billich, A. & Ettmayer, P. Fluorescence-based assay of sphingosine kinases. Anal. Biochem. 324, 114-119 (2004).
40. Miyoshi, H., Blomer, U., Takahashi, M., Gage, F. H. & Verma, I. M. Development of a self-inactivating lentivirus vector. J. Virol. 72, 8150-8157 (1998).
41. Kim, T. K. & Burgess, D. J. Pharmacokinetic characterization of 14C-vascular endothelial growth factor controlled release microspheres using a rat model. J. Pharm. Pharmacol. 54, 897-905 (2002).
42. Okita, K., Ichisaka, T. & Yamanaka, S. Generation of germline-competent induced pluripotent stem cells. Nature 448, 313-317 (2007).
43. Okabe, M. et al. Definitive proof for direct reprogramming of hematopoietic cells to pluripotency. Blood 114, 1764-1767 (2009).
44. Okada, Y. et al. Spatiotemporal recapitulation of central nervous system development by murine embryonic stem cell-derived neural stem/progenitor cells. Stem Cells 26, 3086-3098 (2008).
45. Imaizumi, Y. et al. Mitochondrial dysfunction associated with increased oxidative stress and alpha-synuclein accumulation in PARK2 iPSC-derived neurons and postmortem brain tissue. Mol. Brain 5, 35 (2012).