#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

3D analysis of human islet amyloid polypeptide crystalline structures in Drosophila melanogaster


Autoři: Ling Xie aff001;  Xiaohong Gu aff002;  Kenta Okamoto aff003;  Gunilla T. Westermark aff002;  Klaus Leifer aff001
Působiště autorů: Department of Engineering Sciences, Applied Materials Sciences, Uppsala University, Uppsala, Sweden aff001;  Department of Medical Cell Biology, Uppsala University, Uppsala, Sweden aff002;  Department of Biology Physics, Uppsala University, Uppsala, Sweden aff003
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0223456

Souhrn

Expression of the Alzheimer’s disease associated polypeptide Aβ42 and the human polypeptide hormon islet amyloid polypeptide (hIAPP) and the prohormone precursor (hproIAPP) in neurons of Drosophila melanogaster leads to the formation of protein aggregates in the fat body tissue surrounding the brain. We determined the structure of these membrane-encircled protein aggregates using transmission electron microscopy (TEM) and observed the dissolution of protein aggregates after starvation. Electron tomography (ET) as an extension of transmission electron microscopy revealed that these aggregates were comprised of granular subunits having a diameter of 20 nm aligned into highly ordered structures in all three dimensions. The three dimensional (3D) lattice of hIAPP granules were constructed of two unit cells, a body centered tetragonal (BCT) and a triclinic unit cell. A 5-fold twinned structure was observed consisting of the cyclic twinning of the BCT and triclinic unit cells. The interaction between the two nearest hIAPP granules in both unit cells is not only governed by the van der Waals forces and the dipole-dipole interaction but potentially also by filament-like structures that can connect the nearest neighbors. Hence, our 3D structural analysis provides novel insight into the aggregation process of hIAPP in the fat body tissue of Drosophila melanogaster.

Klíčová slova:

Amyloid proteins – Crystal structure – Drosophila melanogaster – Fats – Protein structure – Protein structure comparison – Transmission electron microscopy – Nutrient and storage proteins


Zdroje

1. Benson MD, Buxbaum JN, Eisenberg DS, Merlini G, Saraiva MJM, Sekijima Y, et al. Amyloid nomenclature 2018: recommendations by the International Society of Amyloidosis (ISA) nomenclature committee. Amyloid. 2018;25:215–219. doi: 10.1080/13506129.2018.1549825 30614283

2. Crowther DC, Page R, Chandraratna D, Lomas DA. A Drosophila model of Alzheimer's disease. Methods Enzymol. 2006;412:234–255. doi: 10.1016/S0076-6879(06)12015-7 17046662

3. Pokrzywa M, Dacklin I, Hultmark D, Lundgren E. Misfolded transthyretin causes behavioral changes in a Drosophila model for transthyretin-associated amyloidosis. Eur J Neurosci. 2007;26:913–924. doi: 10.1111/j.1460-9568.2007.05728.x 17714186

4. Berg I, Thor S, Hammarstrom P. Modeling familial amyloidotic polyneuropathy (Transthyretin V30M) in Drosophila melanogaster. Neurodegener Dis. 2009;6:127–138. doi: 10.1159/000213761 19372706

5. Brand AH, Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development. 1993;118:401–145. 8223268

6. Schultz SW, Nilsson KP, Westermark GT. Drosophila melanogaster as a model system for studies of islet amyloid polypeptide aggregation. PLoS One. 2011;6:e20221. doi: 10.1371/journal.pone.0020221 21695120

7. Arrese EL, Soulages JL. Insect fat body: energy, metabolism, and regulation. Ann Rev Entomol. 2010;55:207–225.

8. Haunerland N, Shirk P. Regional and functional differentiation in the insect fatbody. Ann Rev Entomol. 1995;40:121–145.

9. Chapman R. Fat Body. In: Simpson S, Douglas A, editors. The Insects: Structure and Function. Cambridge University Press; 2013. p. 132–144.

10. Butterworth FM, Emerson L, Rasch EM. Maturation and degeneration of the fat body in the Drosophila larva and pupa as revealed by morphometric analysis. Tissue Cell. 1988;20:255–268. doi: 10.1016/0040-8166(88)90047-x 3136556

11. Hoshizaki DK, Lunz R, Ghosh M, Johnson W. Identification of fat-cell enhancer activity in Drosophila melanogaster using P-element enhancer traps. Genome. 1995;38:497–506. doi: 10.1139/g95-065 7557362

12. Gaudecker B. Über den Formwechsel einiger Zellorganelle bei der Bildung der Reservestoffe im Fettkörper von Drosophila-Larven. Z Zellforscnung. 1963;61:56–95.

13. Locke M, Collins JV. Protein uptake into multivesicular bodies and storage granules in the fat body of an insect. J Cell Biol. 1968;36:453–483. doi: 10.1083/jcb.36.3.453 5645544

14. Tojo S, Betchaku T, Ziccardi VJ, Wyatt GR. Fat body protein granules and storage proteins in the silkmoth, Hyalophora cecropia. J Cell Biol. 1978;78:823–838. doi: 10.1083/jcb.78.3.823 701361

15. Pokrzywa M, Dacklin I, Vestling M, Hultmark D, Lundgren E, Cantera R. Uptake of aggregating transthyretin by fat body in a Drosophila model for TTR-associated amyloidosis. PLoS One. 2010;5:e14343. doi: 10.1371/journal.pone.0014343 21179560

16. Doye J, Poon W. Protein crystallisation in vivo. Curr Opin Colloid Interface Sci. 2006;11:40–46.

17. Hofmeister H. Fivefoled twinned nanoparticles. In: Nalwa S, editor. Encyclopedia of Nanoscience and Nanotechnology 3. Valencia: American Scientific Publishers; 2004. p. 432–452.

18. Nir S, Andersen M. Van der Waals interactions between cell surfaces. J Membr Biol. 1977;31:1–18. doi: 10.1007/bf01869396 839528

19. Olins DE, Olins AL, Levy HA, Durfee RC, Margle SM, Tinnel EP, et al. Electron microscope tomography: transcription in three dimensions. Science. 1983;220:498–500. doi: 10.1126/science.6836293 6836293

20. Skoglund U, Andersson K, Strandberg B, Daneholt B. Three-dimensional structure of a specific pre-messenger RNP particle established by electron microscope tomography. Nature. 1986;319:560–564. doi: 10.1038/319560a0 3945344

21. Roma GC, Bueno OC, Camargo-Mathias MI. Morpho-physiological analysis of the insect fat body: a review. Micron. 2010;41:395–401. doi: 10.1016/j.micron.2009.12.007 20206534

22. Rizki TM, Rizki RM. Larval adipose tissue of homoeotic bithorax mutants of Drosophila. Dev Biol. 1978;65:476–482. doi: 10.1016/0012-1606(78)90042-8 98371

23. Raman C. Electron microscopy and immunogold labelling analysis of smart nanoparticles in insects. In: Méndez-Vilas A, editor. Current microscopy contributions to advances in science and technology. 1. Spain: Formatex publisher; 2012. p. 168–178.

24. Butterworth FM, Bownes M, Burde VS. Genetically modified yolk proteins precipitate in the adult Drosophila fat body. J Cell Biol. 1991;112:727–737. doi: 10.1083/jcb.112.4.727 1899669

25. Neumann W, Komrska J, Hofmeister H, Heydenreich J. Interpretation of the shape of electron diffraction spots from small polyhedral crystals by means of the crystal shape amplitude. Acta Crystallographica Section A. 1988;44:890–897.

26. Smit J, Ogbum F, Bechtoldt C. Multiple Twin Structures in Electrodeposited Silver Dendrites. J Electrochem Soc. 1968;115:371–374.

27. Walz J, Tamura T, Tamura N, Grimm R, Baumeister W, Koster AJ. Tricorn protease exists as an icosahedral supermolecule in vivo. Mol Cell. 1997;1:59–65. doi: 10.1016/s1097-2765(00)80007-6 9659903

28. Otzen DE, Oliveberg M. Transient formation of nano-crystalline structures during fibrillation of an Abeta-like peptide. Protein Sci. 2004;13:1417–1421. doi: 10.1110/ps.03538904 15096642

29. Crowther DC, Kinghorn KJ, Miranda E, Page R, Curry JA, Duthie FA, et al. Intraneuronal Abeta, non-amyloid aggregates and neurodegeneration in a Drosophila model of Alzheimer's disease. Neuroscience. 2005;132:123–135. doi: 10.1016/j.neuroscience.2004.12.025 15780472

30. Momma K, Izumi F. VESTA 3 for three-dimensional visualization of crystal, volumetric and morphology data. J Appl Crystallogr 2011;44:1272–1276.

31. Mastronarde DN. Automated electron microscope tomography using robust prediction of specimen movements. J Struct Biol. 2005;152:36–51. doi: 10.1016/j.jsb.2005.07.007 16182563

32. Kremer JR, Mastronarde DN, McIntosh JR. Computer visualization of three-dimensional image data using IMOD. J Struct Biol. 1996;116:71–76. doi: 10.1006/jsbi.1996.0013 8742726

33. Mastronarde DN. Dual-axis tomography: An approach with alignment methods that preserve resolution. J Struct Biol. 1997;120:343–352. doi: 10.1006/jsbi.1997.3919 9441937

34. Norlin N, Hellberg M, Filippov A, Sousa AA, Grobner G, Leapman RD, et al. Aggregation and fibril morphology of the Arctic mutation of Alzheimer's A beta peptide by CD, TEM, STEM and in situ AFM. J Struct Biol. 2012;180:174–189. doi: 10.1016/j.jsb.2012.06.010 22750418

35. Tang G, Peng L, Baldwin PR, Mann DS, Jiang W, Rees I, et al. EMAN2: An extensible image processing suite for electron microscopy. J Struct Biol. 2007;157:38–46. doi: 10.1016/j.jsb.2006.05.009 16859925

36. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, et al. UCSF chimera—A visualization system for exploratory research and analysis. J Comput Chem. 2004;25:1605–1612. doi: 10.1002/jcc.20084 15264254


Článek vyšel v časopise

PLOS One


2019 Číslo 10
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

KOST
Koncepce osteologické péče pro gynekology a praktické lékaře
nový kurz
Autoři: MUDr. František Šenk

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková

Hypertenze a hypercholesterolémie – synergický efekt léčby
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Svět praktické medicíny 5/2023 (znalostní test z časopisu)

Imunopatologie? … a co my s tím???
Autoři: doc. MUDr. Helena Lahoda Brodská, Ph.D.

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#