Lysosomal-associated membrane protein 2 isoforms are differentially affected in early Parkinson's disease

Movement Disorders

Volumn 30, Issue 12, 2015, Pages 1639-1647

  Murphy, Karen E ^a,b   Gysbers, Amanda M ^a   Abbott, Sarah K ^c,d   Spiro, Adena S ^c,d   Furuta, Akiko ^e,g   Cooper, Antony ^b,f   Garner, Brett ^c,d   Kabuta, Tomohiro ^e   Halliday, Glenda M ^a,b  

^a NEUROSCIENCE RESEARCH AUSTRALIA   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c ILLAWARRA HEALTH AND MEDICAL RESEARCH INSTITUTE   (Australia)

^d UNIVERSITY OF WOLLONGONG   (Australia)

^e NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

^f GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^g JUNTENDO UNIVERSITY   (Japan)

Author keywords

Chaperone mediated autophagy (CMA); LAMP2; Nucleic acid autophagy; Parkinson's disease; synuclein

Indexed keywords

ALPHA SYNUCLEIN; BRAIN EXTRACT; CHOLESTEROL; HEAT SHOCK COGNATE PROTEIN 70; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; MESSENGER RNA; HEAT SHOCK PROTEIN 70; ISOPROTEIN;

ARTICLE; BRAIN REGION; CHAPERONE-MEDIATED AUTOPHAGY; CONTROLLED STUDY; HUMAN; LIPIDOMICS; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; WESTERN BLOTTING; AGED; BRAIN; FEMALE; GENETICS; LIPID METABOLISM; MALE; METABOLISM; MIDDLE AGED; NONPARAMETRIC TEST; PATHOLOGY; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ALPHA-SYNUCLEIN; BRAIN; CHOLESTEROL; FEMALE; HSP70 HEAT-SHOCK PROTEINS; HUMANS; LIPID METABOLISM; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 2; MALE; MIDDLE AGED; PARKINSON DISEASE; PROTEIN ISOFORMS; RNA, MESSENGER; STATISTICS, NONPARAMETRIC;

EID: 84929705440     PISSN: 08853185     EISSN: 15318257     Source Type: Journal    
DOI: 10.1002/mds.26141     Document Type: Article

References (53)

1. Saftig P, Klumperman J. Lysosome biogenesis and lysosomal membrane proteins: trafficking meets function. Nat Rev Mol Cell Biol 2009;10:623-635.
2. Saftig P, Schroder B, Blanz J. Lysosomal membrane proteins: life between acid and neutral conditions. Biochem Soc Trans 2010;38:1420-1423.
3. Gough NR, Hatem CL, Fambrough DM. The family of LAMP-2 proteins arises by alternative splicing from a single gene: characterization of the avian LAMP-2 gene and identification of mammalian homologs of LAMP-2b and LAMP-2c. DNA Cell Biol 1995;14:863-867.
4. Kaushik S, Massey AC, Cuervo AM. Lysosome membrane lipid microdomains: novel regulators of chaperone-mediated autophagy. EMBO J 2006;25:3921-3933.
5. Kaushik S, Kiffin R, Cuervo AM. Chaperone-mediated autophagy and aging: a novel regulatory role of lipids revealed. Autophagy 2007;3:387-389.
6. Kiffin R, Kaushik S, Zeng M, et al. Altered dynamics of the lysosomal receptor for chaperone-mediated autophagy with age. J Cell Sci 2007;120:782-791.
7. Koga H, Cuervo AM. Chaperone-mediated autophagy dysfunction in the pathogenesis of neurodegeneration. Neurobiol Dis 2011;43:29-37.
8. Li W, Yang Q, Mao Z. Chaperone-mediated autophagy: machinery, regulation and biological consequences. Cell Mol Life Sci 2011;68:749-763.
9. Cuervo AM, Dice JF. A receptor for the selective uptake and degradation of proteins by lysosomes. Science 1996;273:501-503.
10. Bandyopadhyay U, Kaushik S, Varticovski L, Cuervo AM. The chaperone-mediated autophagy receptor organizes in dynamic protein complexes at the lysosomal membrane. Mol Cell Biol 2008;28:5747-5763.
11. Fujiwara Y, Furuta A, Kikuchi H, et al. Discovery of a novel type of autophagy targeting RNA. Autophagy 2013;9:403-409.
12. Fujiwara Y, Kikuchi H, Aizawa S, et al. Direct uptake and degradation of DNA by lysosomes. Autophagy 2013;9:1167-1171.
13. Mijaljica D, Prescott M, Devenish RJ. Microautophagy in mammalian cells: revisiting a 40-year-old conundrum. Autophagy 2011;7:673-682.
14. Dickson DW, Braak H, Duda JE, et al. Neuropathological assessment of Parkinson's disease: refining the diagnostic criteria. Lancet Neurol 2009;8:1150-1157.
15. Chu Y, Dodiya H, Aebischer P, Olanow CW, Kordower JH. Alterations in lysosomal and proteasomal markers in Parkinson's disease: relationship to alpha-synuclein inclusions. Neurobiol Dis 2009;35:385-398.
16. Crews L, Spencer B, Desplats P, et al. Selective molecular alterations in the autophagy pathway in patients with Lewy body disease and in models of alpha-synucleinopathy. PLoS One 2010;5:e9313.
17. Dehay B, Bove J, Rodriguez-Muela N, et al. Pathogenic lysosomal depletion in Parkinson's disease. J Neurosci 2010;30:12535-12544.
18. Murphy KE, Gysbers AM, Abbott SK, et al. Reduced glucocerebrosidase is associated with increased alpha-synuclein in sporadic Parkinson's disease. Brain 2014;137:834-848.
19. Alvarez-Erviti L, Rodriguez-Oroz MC, Cooper JM, et al. Chaperone-mediated autophagy markers in Parkinson disease brains. Arch Neurol 2010;67:1464-1472.
20. Cuervo AM, Stefanis L, Fredenburg R, Lansbury PT, Sulzer D. Impaired degradation of mutant alpha-synuclein by chaperone-mediated autophagy. Science 2004;305:1292-1295.
21. Vogiatzi T, Xilouri M, Vekrellis K, Stefanis L. Wild type alpha-synuclein is degraded by chaperone-mediated autophagy and macroautophagy in neuronal cells. J Biol Chem 2008;283:23542-23556.
22. Spillantini MG, Schmidt ML, Lee VM, Trojanowski JQ, Jakes R, Goedert M. Alpha-synuclein in Lewy bodies. Nature 1997;388:839-840.
23. Murphy KE, Cottle L, Gysbers AM, Cooper AA, Halliday GM. ATP13A2 (PARK9) protein levels are reduced in brain tissue of cases with Lewy bodies. Acta Neuropathol Comm 2013;1:11.
24. Zhou J, Broe M, Huang Y, et al. Changes in the solubility and phosphorylation of alpha-synuclein over the course of Parkinson's disease. Acta Neuropathol 2011;121:695-704.
25. Abbott SK, Jenner AM, Mitchell TW, Brown SH, Halliday GM, Garner B. An improved high-throughput lipid extraction method for the analysis of human brain lipids. Lipids 2013;48:307-318.
26. Houseley J, Tollervey D. The many pathways of RNA degradation. Cell 2009;136:763-776.
27. Cuervo AM, Hu W, Lim B, Dice JF. IkappaB is a substrate for a selective pathway of lysosomal proteolysis. Mol Biol Cell 1998;9:1995-2010.
28. Yang Q, She H, Gearing M, et al. Regulation of neuronal survival factor MEF2D by chaperone-mediated autophagy. Science 2009;323:124-127.
29. Lue LF, Walker DG, Adler CH, et al. Biochemical increase in phosphorylated alpha-synuclein precedes histopathology of Lewy-type synucleinopathies. Brain Pathol 2012;22:745-756.
30. Hatem CL, Gough NR, Fambrough DM. Multiple mRNAs encode the avian lysosomal membrane protein LAMP-2, resulting in alternative transmembrane and cytoplasmic domains. J Cell Sci 1995;108:2093-2100.
31. Furuta K, Yang XL, Chen JS, Hamilton SR, August JT. Differential expression of the lysosome-associated membrane proteins in normal human tissues. Arch Biochem Biophys 1999;365:75-82.
32. Konecki DS, Foetisch K, Zimmer KP, Schlotter M, Lichter-Konecki U. An alternatively spliced form of the human lysosome-associated membrane protein-2 gene is expressed in a tissue-specific manner. Biochem Biophys Res Commun 1995;215:757-767.
33. Alvarez-Erviti L, Seow Y, Schapira AH, Rodriguez-Oroz MC, Obeso JA, Cooper JM. Influence of microRNA deregulation on chaperone-mediated autophagy and alpha-synuclein pathology in Parkinson's disease. Cell Death Dis 2013;4:e545.
34. Huang J, Xu J, Pang S, Bai B, Yan B. Age-related decrease of the LAMP-2 gene expression in human leukocytes. Clin Biochem 2012;45:1229-1232.
35. Wu G, Wang X, Feng X, et al. Altered expression of autophagic genes in the peripheral leukocytes of patients with sporadic Parkinson's disease. Brain Res 2011;1394:105-111.
36. Pang S, Chen D, Zhang A, Qin X, Yan B. Genetic analysis of the LAMP-2 gene promoter in patients with sporadic Parkinson's disease. Neurosci Lett 2012;526:63-67.
37. Sala G, Stefanoni G, Arosio A, et al. Reduced expression of the chaperone-mediated autophagy carrier hsc70 protein in lymphomonocytes of patients with Parkinson's disease. Brain Res 2014;1546:46-52.
38. Sardiello M, Palmieri M, di Ronza A, et al. A gene network regulating lysosomal biogenesis and function. Science 2009;325:473-477.
39. Settembre C, Di Malta C, Polito VA, et al. TFEB links autophagy to lysosomal biogenesis. Science 2011;332:1429-1433.
40. Anguiano J, Garner TP, Mahalingam M, Das BC, Gavathiotis E, Cuervo AM. Chemical modulation of chaperone-mediated autophagy by retinoic acid derivatives. Nat Chem Biol 2013;9:374-382.
41. Cuervo AM, Dice JF. Age-related decline in chaperone-mediated autophagy. J Biol Chem 2000;275:31505-31513.
42. Agarraberes FA, Terlecky SR, Dice JF. An intralysosomal hsp70 is required for a selective pathway of lysosomal protein degradation. J Cell Biol 1997;137:825-834.
43. Cuervo AM, Mann L, Bonten EJ, d'Azzo A, Dice JF. Cathepsin A regulates chaperone-mediated autophagy through cleavage of the lysosomal receptor. EMBO J 2003;22:47-59.
44. Gai WP, Yuan HX, Li XQ, Power JT, Blumbergs PC, Jensen PH. In situ and in vitro study of colocalization and segregation of alpha-synuclein, ubiquitin, and lipids in Lewy bodies. Exp Neurol 2000;166:324-333.
45. Bosco DA, Fowler DM, Zhang Q, et al. Elevated levels of oxidized cholesterol metabolites in Lewy body disease brains accelerate alpha-synuclein fibrilization. Nat Chem Biol 2006;2:249-253.
46. Bar-On P, Crews L, Koob AO, et al. Statins reduce neuronal alpha-synuclein aggregation in in vitro models of Parkinson's disease. J Neurochem 2008;105:1656-1667.
47. Mak SK, McCormack AL, Manning-Bog AB, Cuervo AM, Di Monte DA. Lysosomal degradation of alpha-synuclein in vivo. J Biol Chem 2010;285:13621-13629.
48. Fantini J, Carlus D, Yahi N. The fusogenic tilted peptide (67-78) of alpha-synuclein is a cholesterol binding domain. Biochim Biophys Acta 2011;1808:2343-2351.
49. Xilouri M, Brekk OR, Landeck N, et al. Boosting chaperone-mediated autophagy in vivo mitigates alpha-synuclein-induced neurodegeneration. Brain 2013;136:2130-2146.
50. Rodriguez-Navarro JA, Kaushik S, Koga H, et al. Inhibitory effect of dietary lipids on chaperone-mediated autophagy. Proc Natl Acad Sci U S A 2012;109:E705-E714.
51. Braak H, Del Tredici K, Rub U, de Vos RA, Jansen Steur EN, Braak E. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging 2003;24:197-211.
52. Consensus recommendations for the postmortem diagnosis of Alzheimer's disease. The National Institute on Aging, and Reagan Institute Working Group on Diagnostic Criteria for the Neuropathological Assessment of Alzheimer's Disease. Neurobiol Aging 1997;18(4 Suppl):S1-S2.
53. Morris JC. Clinical dementia rating: a reliable and valid diagnostic and staging measure for dementia of the Alzheimer type. Int Psychogeriatr 1997;9(Suppl 1):173-176; discussion, 177-178.