A novel function for proSAAS as an amyloid anti-aggregant in Alzheimer's disease

Journal of Neurochemistry

Volumn 128, Issue 3, 2014, Pages 419-430

  Hoshino, Akina ^a   Helwig, Michael ^a   Rezaei, Sina ^b   Berridge, Casey ^b   Eriksen, Jason L ^b   Lindberg, Iris ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF HOUSTON   (United States)

Author keywords

Alzheimer's disease; chaperone; proSAAS; protein aggregation

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-42]; PROTEIN PROSAAS; RECOMBINANT PROTEIN; SECRETORY PROTEIN; UNCLASSIFIED DRUG; AMYLOID; AMYLOID BETA PROTEIN (1 42); AMYLOID BETA-PROTEIN (1-42); CHAPERONE; NERVE PROTEIN; PCSK1N PROTEIN, MOUSE; PEPTIDE FRAGMENT; SMALL INTERFERING RNA;

AGED; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CASE REPORT; CONTROLLED STUDY; HUMAN; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NERVE CELL; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; ANIMAL; CELL LINE; CELL SURVIVAL; CHEMISTRY; DRUG ANTAGONISM; DRUG EFFECT; ELECTRON MICROSCOPY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; IMMUNOPRECIPITATION; LENTIVIRINAE; PATHOLOGY; PHYSIOLOGY; PROSAAS; TISSUE FIXATION; TRANSGENIC MOUSE; WESTERN BLOTTING;

MUS;

ALZHEIMER'S DISEASE; CHAPERONE; PROSAAS; PROTEIN AGGREGATION;

AGED; ALZHEIMER DISEASE; AMYLOID; AMYLOID BETA-PEPTIDES; ANIMALS; BLOTTING, WESTERN; CELL LINE; CELL SURVIVAL; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOPRECIPITATION; LENTIVIRUS; MALE; MICE; MICE, TRANSGENIC; MICROSCOPY, ELECTRON; MOLECULAR CHAPERONES; NERVE TISSUE PROTEINS; PEPTIDE FRAGMENTS; RECOMBINANT PROTEINS; RNA, SMALL INTERFERING; TISSUE FIXATION;

EID: 84897018530     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12454     Document Type: Article

References (44)

1. Abdi F., Quinn J. F., Jankovic J., et al,. (2006) Detection of biomarkers with a multiplex quantitative proteomic platform in cerebrospinal fluid of patients with neurodegenerative disorders. J. Alzheimer's Dis. 9, 293-348.
2. Ali Y. O., Kitay B. M., and, Zhai R. G., (2010) Dealing with misfolded proteins: examining the neuroprotective role of molecular chaperones in neurodegeneration. Molecules 15, 6859-6887.
3. Atkins N., Jr, Mitchell J. W., Romanova E. V., Morgan D. J., Cominski T. P., Ecker J. L., Pintar J. E., Sweedler J. V., and, Gillette M. U., (2010) Circadian integration of glutamatergic signals by little SAAS in novel suprachiasmatic circuits. PLoS ONE 5, e12612.
4. Benilova I., Karran E., and, De Strooper B., (2012) The toxic Abeta oligomer and Alzheimer's disease: an emperor in need of clothes. Nat. Neurosci. 15, 349-357.
5. Braks J. A. M., and, Martens G. J. M., (1994) 7B2 is a neuroendocrine chaperone that transiently interacts with prohormone convertase PC2 in the secretory pathway. Cell 78, 263-273.
6. Cameron A., Fortenberry Y., and, Lindberg I., (2000) The SAAS granin exhibits structural and functional homology to 7B2 and contains a highly potent hexapeptide inhibitor of PC1. FEBS Lett. 473, 135-138.
7. Chaudhuri B., Stephen C., Huijbregts R., and, Martens G., (1995) The neuroendocrine protein 7B2 acts as a molecular chaperone in the in vitro folding of human insulin-like growth factor-1 secreted from yeast. Biochem. Biophys. Res. Commun. 211, 417-425.
8. Davidsson P., Sjogren M., Andreasen N., Lindbjer M., Nilsson C. L., Westman-Brinkmalm A., and, Blennow K., (2002) Studies of the pathophysiological mechanisms in frontotemporal dementia by proteome analysis of CSF proteins. Brain Res. Mol. Brain Res. 109, 128-133.
9. Emmanouilidou E., Melachroinou K., Roumeliotis T., Garbis S. D., Ntzouni M., Margaritis L. H., Stefanis L., and, Vekrellis K., (2010) Cell-produced alpha-synuclein is secreted in a calcium-dependent manner by exosomes and impacts neuronal survival. J. Neurosci. 30, 6838-6851.
10. Feng Y., Reznik S. E., and, Fricker L. D., (2001) Distribution of proSAAS-derived peptides in rat neuroendocrine tissues. Neuroscience 105, 469-478.
11. Finehout E. J., Franck Z., Choe L. H., Relkin N., and, Lee K. H., (2007) Cerebrospinal fluid proteomic biomarkers for Alzheimer's disease. Ann. Neurol. 61, 120-129.
12. Fortenberry Y., Hwang J. R., Apletalina E. V., and, Lindberg I., (2002) Functional characterization of ProSAAS: similarities and differences with 7B2. J. Biol. Chem. 277, 5175-5186.
13. Fricker L. D., McKinzie A. A., Sun J., et al,. (2000) Identification and characterization of proSAAS, a granin-like neuroendocrine peptide precursor that inhibits prohormone processing. J. Neurosci. 20, 639-648.
14. Guest P. C., Abdel-Halim S. M., Gross D. J., Clark A., Poitout V., Amaria R., Ostenson C. G., and, Hutton J. C., (2002) Proinsulin processing in the diabetic Goto-Kakizaki rat. J. Endocrinol. 175, 637-647.
15. Haass C., Lemere C. A., Capell A., Citron M., Seubert P., Schenk D., Lannfelt L., and, Selkoe D. J., (1995) The Swedish mutation causes early-onset Alzheimer's disease by beta-secretase cleavage within the secretory pathway. Nat. Med. 1, 1291-1296.
16. Harper J. D., Lieber C. M., and, Lansbury P. T., Jr, (1997) Atomic force microscopic imaging of seeded fibril formation and fibril branching by the Alzheimer's disease amyloid-beta protein. Chem. Biol. 4, 951-959.
17. Hatcher N. G., Atkins N. J., Annangudi S. P., Forbes A. J., Kelleher N. L., Gillette M. U., and, Sweedler J. V., (2008) Mass spectrometry-based discovery of circadian peptides. Proc. Natl Acad. Sci. USA 105, 12527-12532.
18. Helwig M., Hoshino A., Berridge C., Lee S. N., Lorenzen N., Otzen D. E., Eriksen J. L., and, Lindberg I., (2012) The neuroendocrine protein 7B2 suppresses the aggregation of neurodegenerative disease-related proteins. J. Biol. Chem. 288, 1114-1124.
19. Hu X., Crick S. L., Bu G., Frieden C., Pappu R. V., and, Lee J. M., (2009) Amyloid seeds formed by cellular uptake, concentration, and aggregation of the amyloid-beta peptide. Proc. Natl Acad. Sci. USA 106, 20324-20329.
20. Jahn H., Wittke S., Zurbig P., et al,. (2011) Peptide fingerprinting of Alzheimer's disease in cerebrospinal fluid: identification and prospective evaluation of new synaptic biomarkers. PLoS ONE 6, e26540.
21. Jankowsky J. L., Fadale D. J., Anderson J., et al,. (2004) Mutant presenilins specifically elevate the levels of the 42 residue beta-amyloid peptide in vivo: evidence for augmentation of a 42-specific gamma secretase. Hum. Mol. Genet. 13, 159-170.
22. Kikuchi K., Arawaka S., Koyama S., et al,. (2003) An N-terminal fragment of ProSAAS (a granin-like neuroendocrine peptide precursor) is associated with tau inclusions in Pick's disease. Biochem. Biophys. Res. Commun. 308, 646-654.
23. Lambert M. P., Barlow A. K., Chromy B. A., et al,. (1998) Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc. Natl Acad. Sci. USA 95, 6448-6453.
24. Lanoue E., and, Day R., (2001) Coexpression of proprotein convertase SPC3 and the neuroendocrine precursor proSAAS. Endocrinology 142, 4141-4149.
25. Lee S. N., and, Lindberg I., (2008) 7B2 prevents unfolding and aggregation of prohormone convertase 2. Endocrinology 149, 4116-4127.
26. Lin M. S., Chen L. Y., Tsai H. T., Wang S. S., Chang Y., Higuchi A., and, Chen W. Y., (2008) Investigation of the mechanism of beta-amyloid fibril formation by kinetic and thermodynamic analyses. Langmuir 24, 5802-5808.
27. Liu X. D., Zeng B. F., Xu J. G., Zhu H. B., and, Xia Q. C., (2006) Proteomic analysis of the cerebrospinal fluid of patients with lumbar disk herniation. Proteomics 6, 1019-1028.
28. Mannini B., Cascella R., Zampagni M., et al,. (2012) Molecular mechanisms used by chaperones to reduce the toxicity of aberrant protein oligomers. Proc. Natl Acad. Sci. USA 109, 12479-12484.
29. Mohamed A., and, Posse de Chaves E., (2011) Abeta internalization by neurons and glia. Int. J. Alzheimer's Dis. 2011, 127984.
30. Morgan D. J., Mzhavia N., Peng B., Pan H., Devi L. A., and, Pintar J. E., (2005) Embryonic gene expression and pro-protein processing of proSAAS during rodent development. J. Neurochem. 93, 1454-1462.
31. Morgan D. J., Wei S., Gomes I., Czyzyk T., Mzhavia N., Pan H., Devi L. A., Fricker L. D., and, Pintar J. E., (2010) The propeptide precursor proSAAS is involved in fetal neuropeptide processing and body weight regulation. J. Neurochem. 113, 1275-1284.
32. Mzhavia N., Qian Y., Feng Y., Che F. Y., Devi L. A., and, Fricker L. D., (2002) Processing of proSAAS in neuroendocrine cell lines. Biochem. J. 361, 67-76.
33. Qian Y., Devi L. A., Mzhavia N., Munzer S., Seidah N. G., and, Fricker L. D., (2000) The C-terminal region of proSAAS is a potent inhibitor of prohormone convertase 1. J. Biol. Chem. 275, 23596-23601.
34. Rekas A., Adda C. G., Andrew Aquilina J., et al,. (2004) Interaction of the molecular chaperone alphaB-crystallin with alpha-synuclein: effects on amyloid fibril formation and chaperone activity. J. Mol. Biol. 340, 1167-1183.
35. Sayah M., Fortenberry Y., Cameron A., and, Lindberg I., (2001) Tissue distribution and processing of proSAAS by proprotein convertases. J. Neurochem. 76, 1833-1841.
36. Shammas S. L., Waudby C. A., Wang S., et al,. (2011) Binding of the molecular chaperone alphaB-crystallin to Abeta amyloid fibrils inhibits fibril elongation. Biophys. J. 101, 1681-1689.
37. Stine W. B., Jungbauer L., Yu C., and, LaDu M. J., (2011) Preparing synthetic Abeta in different aggregation states. Methods Mol. Biol. 670, 13-32.
38. Takuma K., Fang F., Zhang W., et al,. (2009) RAGE-mediated signaling contributes to intraneuronal transport of amyloid-beta and neuronal dysfunction. Proc. Natl Acad. Sci. USA 106, 20021-20026.
39. Terry R. D., Masliah E., Salmon D. P., Butters N., DeTeresa R., Hill R., Hansen L. A., and, Katzman R., (1991) Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann. Neurol. 30, 572-580.
40. Volpicelli-Daley L. A., Luk K. C., Patel T. P., Tanik S. A., Riddle D. M., Stieber A., Meaney D. F., Trojanowski J. Q., and, Lee V. M., (2011) Exogenous alpha-synuclein fibrils induce Lewy body pathology leading to synaptic dysfunction and neuron death. Neuron 72, 57-71.
41. Wada M., Ren C. H., Koyama S., et al,. (2004) A human granin-like neuroendocrine peptide precursor (proSAAS) immunoreactivity in tau inclusions of Alzheimer's disease and parkinsonism-dementia complex on Guam. Neurosci. Lett. 356, 49-52.
42. Walsh D. M., Lomakin A., Benedek G. B., Condron M. M., and, Teplow D. B., (1997) Amyloid beta-protein fibrillogenesis. Detection of a protofibrillar intermediate. J. Biol. Chem. 272, 22364-22372.
43. Wardman J. H., Berezniuk I., Di S., Tasker J. G., and, Fricker L. D., (2011) ProSAAS-derived peptides are colocalized with neuropeptide Y and function as neuropeptides in the regulation of food intake. PLoS ONE 6, e28152.
44. Yerbury J. J., Poon S., Meehan S., Thompson B., Kumita J. R., Dobson C. M., and, Wilson M. R., (2007) The extracellular chaperone clusterin influences amyloid formation and toxicity by interacting with prefibrillar structures. FASEB J. 21, 2312-2322.