Heparan sulfate proteoglycans mediate internalization and propagation of specific proteopathic seeds

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 33, 2013, Pages

  Holmes, Brandon B ^a   DeVos, Sarah L ^a   Kfoury, Najla ^a   Li, Mei ^b   Jacks, Rachel ^a   Yanamandra, Kiran ^a   Ouidja, Mohand O ^c   Brodsky, Frances M ^d   Marasa, Jayne ^a   Bagchi, Devika P ^a   Kotzbauer, Paul T ^a   Miller, Timothy M ^a   Papy Garcia, Dulce ^c   Diamond, Marc I ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITÉ PARIS EST CRÉTEIL   (France)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Alzheimer's disease; Macropinocytosis; Neurodegeneration; Prion like mechanisms

Indexed keywords

ALPHA SYNUCLEIN; HUNTINGTIN; PROTEOHEPARAN SULFATE; TAU PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DEGENERATIVE DISEASE; HUMAN; HUMAN CELL; INTERNALIZATION; MALE; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PINOCYTOSIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN TRANSPORT; TAUOPATHY;

ALZHEIMER'S DISEASE; MACROPINOCYTOSIS; NEURODEGENERATION; PRION-LIKE MECHANISMS;

ACTINS; AMYLOID; ANIMALS; FLOW CYTOMETRY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEK293 CELLS; HEPARAN SULFATE PROTEOGLYCANS; HUMANS; IMMUNOHISTOCHEMISTRY; INDOLES; MALE; MICE; MICE, INBRED C57BL; MICROSCOPY, FLUORESCENCE; NEURAL STEM CELLS; PINOCYTOSIS; TAU PROTEINS;

EID: 84882306577     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1301440110     Document Type: Article

References (55)

1. Seeley WW, Crawford RK, Zhou J, Miller BL, Greicius MD (2009) Neurodegenerative diseases target large-scale human brain networks. Neuron 62(1):42-52.
2. Zhou J, Gennatas ED, Kramer JH, Miller BL, Seeley WW (2012) Predicting regional neurodegeneration from the healthy brain functional connectome. Neuron 73(6):1216-1227.
3. Braak H, Braak E (1997) Diagnostic criteria for neuropathologic assessment of Alzheimer's disease. Neurobiol Aging 18(4, suppl):S85-S88.
4. Raj A, Kuceyeski A, Weiner M (2012) A network diffusion model of disease progression in dementia. Neuron 73(6):1204-1215.
5. Braak H, Braak E (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82(4):239-259.
6. Frost B, Jacks RL, Diamond MI (2009) Propagation of tau misfolding from the outside to the inside of a cell. J Biol Chem 284(19):12845-12852.
7. Clavaguera F, et al. (2009) Transmission and spreading of tauopathy in transgenic mouse brain. Nat Cell Biol 11(7):909-913.
8. Liu L, et al. (2012) Trans-synaptic spread of tau pathology in vivo. PLoS ONE 7(2): e31302.
9. de Calignon A, et al. (2012) Propagation of tau pathology in a model of early Alzheimer's disease. Neuron 73(4):685-697.
10. Guo JL, Lee VMY (2011) Seeding of normal Tau by pathological Tau conformers drives pathogenesis of Alzheimer-like tangles. J Biol Chem 286(17):15317-15331.
11. Iba M, et al. (2013) Synthetic tau fibrils mediate transmission of neurofibrillary tangles in a transgenic mouse model of Alzheimer's-like tauopathy. J Neurosci 33(3):1024-1037.
12. Kfoury N, Holmes BB, Jiang H, Holtzman DM, Diamond MI (2012) Trans-cellular propagation of Tau aggregation by fibrillar species. J Biol Chem 287(23): 19440-19451.
13. Schonberger O, et al. (2003) Novel heparan mimetics potently inhibit the scrapie prion protein and its endocytosis. Biochem Biophys Res Commun 312(2):473-479.
14. Horonchik L, et al. (2005) Heparan sulfate is a cellular receptor for purified infectious prions. J Biol Chem 280(17):17062-17067.
15. Mercer J, Helenius A (2009) Virus entry by macropinocytosis. Nat Cell Biol 11(5): 510-520.
16. Kaplan IM, Wadia JS, Dowdy SF (2005) Cationic TAT peptide transduction domain enters cells by macropinocytosis. J Control Release 102(1):247-253.
17. Wadia JS, Stan RV, Dowdy SF (2004) Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nat Med 10(3): 310-315.
18. Nakase I, et al. (2004) Cellular uptake of arginine-rich peptides: roles for macropinocytosis and actin rearrangement. Mol Ther 10(6):1011-1022.
19. Nakase I, et al. (2007) Interaction of arginine-rich peptides with membrane-associated proteoglycans is crucial for induction of actin organization and macropinocytosis. Biochemistry 46(2):492-501.
20. Chang HC, Samaniego F, Nair BC, Buonaguro L, Ensoli B (1997) HIV-1 Tat protein exits from cells via a leaderless secretory pathway and binds to extracellular matrixassociated heparan sulfate proteoglycans through its basic region. AIDS 11(12): 1421-1431.
21. Tyagi M, Rusnati M, Presta M, Giacca M (2001) Internalization of HIV-1 tat requires cell surface heparan sulfate proteoglycans. J Biol Chem 276(5):3254-3261.
22. Rusnati M, et al. (1997) Interaction of HIV-1 Tat protein with heparin. Role of the backbone structure, sulfation, and size. J Biol Chem 272(17):11313-11320.
23. Liu Y, et al. (2000) Uptake of HIV-1 tat protein mediated by low-density lipoprotein receptor-related protein disrupts the neuronal metabolic balance of the receptor ligands. Nat Med 6(12):1380-1387.
24. Console S, Marty C, García-Echeverría C, Schwendener R, Ballmer-Hofer K (2003) Antennapedia and HIV transactivator of transcription (TAT) protein transduction domains promote endocytosis of high molecular weight cargo upon binding to cell surface glycosaminoglycans. J Biol Chem 278(37):35109-35114.
25. Goedert M, et al. (1996) Assembly of microtubule-associated protein tau into Alzheimer-like filaments induced by sulphated glycosaminoglycans. Nature 383(6600): 550-553.
26. Kanekiyo T, et al. (2011) Heparan sulphate proteoglycan and the low-density lipoprotein receptor-related protein 1 constitute major pathways for neuronal amyloid-beta uptake. J Neurosci 31(5):1644-1651.
27. Conrad EH (1998) Heparin-Binding Proteins (Academic, San Diego).
28. Lidholt K, et al. (1992) A single mutation affects both N-acetylglucosaminyltransferase and glucuronosyltransferase activities in a Chinese hamster ovary cell mutant defective in heparan sulfate biosynthesis. Proc Natl Acad Sci USA 89(6):2267-2271.
29. Tong M, et al. (2008) RGTA OTR 4120, a heparan sulfate proteoglycan mimetic, increases wound breaking strength and vasodilatory capability in healing rat fullthickness excisional wounds. Wound Repair Regen 16(2):294-299.
30. Ouidja MO, et al. (2007) Structure-activity studies of heparan mimetic polyanions for anti-prion therapies. Biochem Biophys Res Commun 363(1):95-100.
31. Desplats P, et al. (2009) Inclusion formation and neuronal cell death through neuron-to-neuron transmission of alpha-synuclein. Proc Natl Acad Sci USA 106(31): 13010-13015.
32. Hansen C, et al. (2011) ?-Synuclein propagates from mouse brain to grafted dopaminergic neurons and seeds aggregation in cultured human cells. J Clin Invest 121(2):715-725.
33. Luk KC, et al. (2009) Exogenous alpha-synuclein fibrils seed the formation of Lewy body-like intracellular inclusions in cultured cells. Proc Natl Acad Sci USA 106(47): 20051-20056.
34. Trevino RS, et al. (2012) Fibrillar structure and charge determine the interaction of polyglutamine protein aggregates with the cell surface. J Biol Chem 287(35): 29722-29728.
35. Ren PH, et al. (2009) Cytoplasmic penetration and persistent infection of mammalian cells by polyglutamine aggregates. Nat Cell Biol 11(2):219-225.
36. Münch C, O'Brien J, Bertolotti A (2011) Prion-like propagation of mutant superoxide dismutase-1 misfolding in neuronal cells. Proc Natl Acad Sci USA 108(9):3548-3553.
37. Wadia JS, Schaller M, Williamson RA, Dowdy SF (2008) Pathologic prion protein infects cells by lipid-raft dependent macropinocytosis. PLoS ONE 3(10):e3314.
38. Lee HJ, et al. (2008) Assembly-dependent endocytosis and clearance of extracellular alpha-synuclein. Int J Biochem Cell Biol 40(9):1835-1849.
39. de Planque MR, et al. (2007) beta-Sheet structured beta-amyloid(1-40) perturbs phosphatidylcholine model membranes. J Mol Biol 368(4):982-997.
40. Blumenthal R, Seth P, Willingham MC, Pastan I (1986) pH-dependent lysis of liposomes by adenovirus. Biochemistry 25(8):2231-2237.
41. Chandran K, Farsetta DL, Nibert ML (2002) Strategy for nonenveloped virus entry: A hydrophobic conformer of the reovirus membrane penetration protein micro 1 mediates membrane disruption. J Virol 76(19):9920-9933.
42. Conner SD, Schmid SL (2003) Regulated portals of entry into the cell. Nature 422(6927):37-44.
43. Flach K, et al. (2012) Tau oligomers impair artificial membrane integrity and cellular viability. J Biol Chem 287(52):43223-43233.
44. Vieira TCRG, et al. (2011) Heparin binding by murine recombinant prion protein leads to transient aggregation and formation of RNA-resistant species. J Am Chem Soc 133(2):334-344.
45. Watson DJ, Lander AD, Selkoe DJ (1997) Heparin-binding properties of the amyloidogenic peptides Abeta and amylin. Dependence on aggregation state and inhibition by Congo red. J Biol Chem 272(50):31617-31624.
46. Cohlberg JA, Li J, Uversky VN, Fink AL (2002) Heparin and other glycosaminoglycans stimulate the formation of amyloid fibrils from alpha-synuclein in vitro. Biochemistry 41(5):1502-1511.
47. Yamada K, et al. (2011) In vivo microdialysis reveals age-dependent decrease of brain interstitial fluid tau levels in P301S human tau transgenic mice. J Neurosci 31(37): 13110-13117.
48. Okada M, Nadanaka S, Shoji N, Tamura J, Kitagawa H (2010) Biosynthesis of heparan sulfate in EXT1-deficient cells. Biochem J 428(3):463-471.
49. Broekelmann TJ, et al. (2005) Tropoelastin interacts with cell-surface glycosaminoglycans via its COOH-terminal domain. J Biol Chem 280(49):40939-40947.
50. Lee S, Kim W, Li Z, Hall GF (2012) Accumulation of vesicle-associated human tau in distal dendrites drives degeneration and tau secretion in an in situ cellular tauopathy model. Int J Alzheimers Dis 2012:172837.
51. Doh-ura K, et al. (2004) Treatment of transmissible spongiform encephalopathy by intraventricular drug infusion in animal models. J Virol 78(10):4999-5006.
52. Goedert M, Jakes R (1990) Expression of separate isoforms of human tau protein: correlation with the tau pattern in brain and effects on tubulin polymerization. EMBO J 9(13):4225-4230.
53. Pollitt SK, et al. (2003) A rapid cellular FRET assay of polyglutamine aggregation identifies a novel inhibitor. Neuron 40(4):685-694.
54. Desai UA, et al. (2006) Biologically active molecules that reduce polyglutamine aggregation and toxicity. Hum Mol Genet 15(13):2114-2124.
55. Shao J, Welch WJ, Diamond MI (2008) ROCK and PRK-2 mediate the inhibitory effect of Y-27632 on polyglutamine aggregation. FEBS Lett 582(12):1637-1642.