Amyloid β oligomers inhibit growth of human cancer cells

English version

Autoři: Bozena Pavliukeviciene ^aff001; Aiste Zentelyte ^aff002; Marija Jankunec ^aff001; Giedre Valiuliene ^aff002; Martynas Talaikis ^aff001; Ruta Navakauskiene ^aff002; Gediminas Niaura ^aff001; Gintaras Valincius ^aff001
Působiště autorů: Department of Bioelectrochemistry and Biospectroscopy, Institute of Biochemistry, Life Sciences Center, Vilnius University, Vilnius, Lithuania ^aff001; Department of Molecular Cell Biology, Institute of Biochemistry, Life Sciences Center, Vilnius University, Vilnius, Lithuania ^aff002
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0221563

Souhrn

Effects of amyloid beta (Aβ) oligomers on viability and function of cell lines such as NB4 (human acute promyelocytic leukemia), A549 (human lung cancer (adenocarcinomic alveolar basal epithelial tumor)) and MCF-7 (human breast cancer (invasive breast ductal carcinoma)) were investigated. Two types of Aβ oligomers were used in the study. The first type was produced in the presence of oligomerization inhibitor, hexafluoroisopropanol (HFIP). The second type of amyloids was assembled in the absence of the inhibitor. The first type preparation was predominantly populated with dimers and trimers, while the second type contained mostly pentadecamers. These amyloid species exhibited different secondary protein structure with considerable amount of antiparallel β sheet structural elements in HFIP oligomerized Aβ mixtures. The effect of the cell growth inhibition, which was stronger in the case of HFIP Aβ oligomers, was observed for all cell lines. Tests aiming at elucidating the effects of the amyloid species on cell cycles showed little differences between amyloid preparations. This prompts us to conclude that the effect on the cancer cell proliferation rate is less specific to the biological processes developing inside the cells during the proliferation. Therefore, cell growth inhibition may involve interactions with the peripheral parts of the cancer cells, such as a phospholipid membrane, and only in case of the NB4 cells, where accumulation of amyloid species inside the cells was detected, one may imply the opposite. In general, cancer cells were much less susceptible to the damaging effects of amyloid oligomers compared to earlier observations in mixed neuronal cell cultures.

Klíčová slova:

Biology and life sciences – Biochemistry – Proteins – Amyloid proteins – Cell biology – Cell processes – Cell cycle and cell division – Cell death – Apoptosis – Cell growth – Physical sciences – Materials science – Materials – Oligomers – Research and analysis methods – Chromatographic techniques – Liquid chromatography – High performance liquid chromatography – Medicine and health sciences – Oncology – Cancer treatment – Mental health and psychiatry – Dementia – Alzheimer's disease – Neurology – Neurodegenerative diseases

Zdroje

1. O’Brien RJ, Wong PC. Amyloid precursor protein processing and Alzheimer's disease. Annu. Rev. Neurosci. 2011; 34: 185–204. doi: 10.1146/annurev-neuro-061010-113613 21456963

2. Sosa LJ, Caceres A, Dupraz S, Oksdath M, Quiroga S, Lorenzo A. The physiological role of the amyloid precursor protein as an adhesion molecule in the developing nervous system. J. Neurochem. 2017; 143: 11–29. doi: 10.1111/jnc.14122 28677143

3. Zhang H, Ma Q, Zhang YW, Xu H. Proteolytic processing of Alzheimer's β-amyloid precursor protein. J. Neurochem. 2012; 120(Suppl 1): 9–21.

4. Voytyuk I, De Strooper B, Chavez-Gutierrez L. Modulation of γ- and β-Secretases as Early Prevention Against Alzheimer's Disease. Biol. Psychiatry. 2018; 83: 320–327.

5. Sanchez-Valle J, Tejero H, Ibanez K, Portero JL, Krallinger M, Al-Shahrour F, et al. A molecular hypothesis to explain direct and inverse co-morbidities between Alzheimer's Disease, Glioblastoma and Lung cancer. Sci. Rep. 2017; 7: 4474. doi: 10.1038/s41598-017-04400-6 28667284

6. Heneka MT, O’Banion MK. Inflammatory processes in Alzheimer’s disease. J. Neuroimmunol. 2007; 184: 69–91.

7. Walsh DM, Selkoe DJ. Oligomers in the brain: the emerging role of soluble protein aggregates in neurodegeneration. Protein Pept. Lett. 2004; 11: 213–228. 15182223

8. Hu X, Crick SL, Bu GJ, Frieden C, Pappu RV, Lee JM. Amyloid seeds formed by cellular uptake, concentration, and aggregation of the amyloid-beta peptide. Proc. Natl. Acad. Sci. U.S.A. 2009; 106: 20324–20329. doi: 10.1073/pnas.0911281106 19910533

9. Wang HM, Ma JF, Tan YY, Wang ZQ, Sheng CY, Chen SD, et al. Amyloid-beta (1–42) Induces Reactive Oxygen Species-Mediated Autophagic Cell Death in U87 and SH-SY5Y Cells. J. Alzheimers Dis. 2010; 21: 597–610. doi: 10.3233/JAD-2010-091207 20571221

10. Pappolla MA, Sos M, Omar RA, Bick RJ, Hickson-Bick DLM, Reiter RJ, et al. Melatonin prevents death of neuroblastoma cells exposed to the Alzheimer amyloid peptide. J. Neurosci. 1997; 17: 1683–1690. 9030627

11. Petkova AT, Leapman RD, Guo Z, Yau WM, Mattson MP, Tycko R. Self-Propagating, Molecular-Level Polymorphism in Alzheimer's beta-Amyloid Fibrils. Science. 2005; 307: 262–265. 15653506

12. Kayed R, Pensalfini A, Margol L, Sokolov Y, Sarsoza F, Head E, et al. Annular Protofibrils Are a Structurally and Functionally Distinct Type of Amyloid Oligomer. J. Biol. Chem. 2009; 284: 4230–4237. doi: 10.1074/jbc.M808591200 19098006

13. Necula M, Kayed R, Milton S, Glabe CG. Small molecule inhibitors of aggregation indicate that amyloid beta oligomerization and fibrillization pathways are independent and distinct. J. Biol. Chem. 2007; 282: 10311–10324. 17284452

14. Lesne S, Koh MT, Kotilinek L, Kayed R, Glabe CG, Yang A, et al. A specific amyloid-beta protein assembly in the brain impairs memory. Nature. 2006; 440: 352–357. 16541076

15. Ferreira ST, Lourenco MV, Oliveira MM, De Felice FG. Soluble amyloid-β oligomers as synaptotoxins leading to cognitive impairment in Alzheimer's disease. Front. Cell. Neurosci. 2015; 9: 191. doi: 10.3389/fncel.2015.00191 26074767

16. Cho MH, Cho K, Kang HJ, Jeon EY, Kim HS, Kwon HJ, et al. Autophagy in microglia degrades extracellular beta-amyloid fibrils and regulates the NLRP3 inflammasome. Autophagy. 2014; 10: 1761–1775. doi: 10.4161/auto.29647 25126727

17. Irvine GB, El-Agnaf OM, Shankar GM, Walsh DM. Protein aggregation in the brain: the molecular basis for Alzheimer's and Parkinson's diseases. Mol. Medi. 2008; 14: 451–464.

18. Stefani M. Structural features and cytotoxicity of amyloid oligomers: implications in Alzheimer's disease and other diseases with amyloid deposits. Prog. Neurobiol. 2012; 99: 226–245. doi: 10.1016/j.pneurobio.2012.03.002 22450705

19. Sponne I, Fifre A, Kriem B, Koziel V, Bihain B, Oster T, et al. Membrane cholesterol interferes with neuronal apoptosis induced by soluble oligomers but not fibrils of the amyloid-beta peptide. FASEB J. 2004; 18: 836–838. 15001562

20. Cizas P, Budvytyte R, Morkuniene R, Moldovan R, Broccio M, Loesche M, et al. Size-dependent neurotoxicity of beta-amyloid oligomers. Arch. Biochem. Biophys. 2010; 496: 84–92.

21. Neniskyte U, Neher JJ, Brown GC. Neuronal death induced by nanomolar amyloid beta is mediated by primary phagocytosis of neurons by microglia. J. Biol. Chem. 2011; 286: 39904–39913. doi: 10.1074/jbc.M111.267583 21903584

22. Valincius G, Heinrich F, Budvytyte R, Vanderah DJ, McGillivray DJ, Sokolov Y, et al. Soluble amyloid ß oligomers affect dielectric membrane properties by bilayer insertion and domain formation: Implications for cell toxicity. Biophys. J. 2008; 95: 4845–4861. doi: 10.1529/biophysj.108.130997 18515395

23. Andreasen M, Lorenzen N, Otzen D. Interactions between misfolded protein oligomers and membranes: A central topic in neurodegenerative diseases? BBA–Biomembranes. 2015; 1848: 1897–1907. doi: 10.1016/j.bbamem.2015.01.018 25666871

24. Canale C, Oropesa-Nunez R, Diaspro A, Dante S. Amyloid and membrane complexity: The toxic interplay revealed by AFM. Semin. Cell Dev. Biol. 2018; 73: 82–94. doi: 10.1016/j.semcdb.2017.08.046 28860102

25. Misiunas A, Talaikyte Z, Niaura G, Razumas V, Nylander T. Thermomyces lanuginosus lipase in the liquid-crystalline phases of aqueous phytantriol: X-ray diffraction and vibrational spectroscopic studies. Biophys. Chem. 2008; 134: 144–156.

26. Jackson M, Mantsh HH. The use and misuse of FTIR spectroscopy in the determination of protein structure. Crit. Rev. Biochem. Mol. Biol. 1995; 30: 95–120. 7656562

27. Kong J, Yu S. Fourier transform infrared spectroscopic analysis of protein secondary structures. Acta Biochim. Biophys. Sin. 2007; 39: 549–559. 17687489

28. Surewicz WK, Mantsch HH, Chapman D. Determination of protein secondary structure by Fourier transform infrared spectroscopy: A critical assessment. Biochemistry 1993; 32: 389–394. 8422346

29. Krimm S, Bandekar J. Vibrational spectroscopy and conformation of peptides, polypeptides, and proteins. Adv. Protein. Chem. 1986; 38: 181–364. 3541539

30. Barth A. Infrared spectroscopy of proteins. BBA–Bioenergetics 2007; 1767: 1073–1101.

31. Rigley DM, Claunch EC, Barone JR. Characterization of large amyloid fibers and tapes with Fourier transform infrared (FT-IR) and Raman spectroscopy. Appl. Spectrosc. 2013; 67: 1417–1426. doi: 10.1366/13-07059 24359656

32. Dousseau F, Pezolet M. Determination of the secondary structure content of proteins in aqueous solutions from their Amide I and Amide II infrared bands. Comparison between classical and partial least-squares methods. Biochemistry 1990; 29: 8771–8779. 2271555

33. Ragaliauskas T, Mickevicius M, Budvytyte R, Niaura G, Carbonnier B, Valincius G. Adsorption of β-amyloid oligomers on octadecanethiol monolayers. J. Colloid Int. Sci. 2014; 425: 159–167.

34. Chirgadze YuN Nevskaya NA. Infrared spectra and resonance interaction of amide-I vibration of the antiparallel-chain pleated sheet. Biopolymers 1976; 15: 637–648. 1252599

35. Zou Y, Li Y, Hao W, Hu X, Ma G. Parallel β-sheet fibril and antiparallel β-sheet oligomer: New insights into amyloid formation of hen egg white lysozyme under heat and acidic condition from FTIR spectroscopy. J. Phys. Chem. B 2013; 117: 4003–4013. doi: 10.1021/jp4003559 23537140

36. Cerf E, Sarroukh R, Tamamizu-Kato S, Breydo L, Derclaye S, Dufrene YF, et al. Antiparallel β-sheet: a signature of the oligomeric amyloid β-peptide. Biochem. J. 2009; 421: 415–423. doi: 10.1042/BJ20090379 19435461

37. Wennmalm S, Chmyrov V, Widengren J, Tjernberg L. Highly sensitive FRET-FCS detects amyloid β-peptide oligomers in solution at physiological concentrations. Anal. Chem. 2015; 87: 11700–11705. doi: 10.1021/acs.analchem.5b02630 26489794

38. Banerjee S, Sun Z, Hayden EY, Teplow DB, Lyubchenko YL. Nanoscale dynamics of amyloid β-42 oligomers as revealed by high-speed atomic force microscopy. ACS Nano. 2017 11: 12202–12209. doi: 10.1021/acsnano.7b05434 29165985

39. Celej MS, Sarroukh R, Goormaghtigh E, Fidelio GD, Ruysschaert JM, Raussens V. Toxic prefibrillar α-synuclein amyloid oligomers adopt a distinctive antiparallel β-sheet structure. Biochem. J. 2012; 443: 719–726.

40. Berthelot K, Ta HP, Gean J, Lecomte S, Cullin C. In vivo and in vitro analyses of toxic mutants of HET-s: FTIR antiparallel signature correlates with amyloid toxicity. J. Mol. Biol. 2011; 412: 137–152.

41. Strouds JC, Liu C, Teng PK, Eisenberg D. Toxic fibrillar oligomers of amyloid-β have cross-β structure. Proc. Natl. Acad. Sci. U.S.A. 2012; 109: 7717–7722. doi: 10.1073/pnas.1203193109 22547798

42. Ferreira ST, Vieira MNN, Felice FG. Soluble protein oligomers as emerging toxins in alzheimer's and other amyloid diseases. IUBMB Life 2007; 59: 332–345. 17505973

43. Irvine GB, El-Agnaf OM, Shankar GM, Walsh DM. Protein Aggregation in the Brain: The Molecular Basis for Alzheimer’s and Parkinson’s Diseases. Mol. Med. 2008; 14: 451–464. doi: 10.2119/2007-00100.Irvine 18368143

44. Head E, Helman AM, Powell D, Schmitt FA. Down syndrome, beta-amyloid and neuroimaging. Free Radic. Biol. Med. 2017; 114: 102–109.

45. Zhang Y, McLaughlin R, Goodyer C, LeBlanc A, Selective cytotoxicity of intracellular amyloid β peptide 1–42 through p53 and Bax in cultured primary human neurons. J. Cell Biol. 2002; 156: 519–529.

46. Michaelis ML, Ansar S, Chen Y, Reiff ER, Seyb KI, Himes RH, et al. β-Amyloid-Induced Neurodegeneration and Protection by Structurally Diverse Microtubule-Stabilizing Agents. J. Pharmacol. Exp. Ther. 2005; 312: 659–668. 15375176

47. Lin CL, Huang WN, Li HH, Huang CN, Hsieh S, Lai C, et al. Hydrogen-rich water attenuates amyloid β-induced cytotoxicity through upregulation of Sirt1-FoxO3a by stimulation of AMP-activated protein kinase in SK-N-MC cells. Chem. Biol. Interact. 2015; 240: 12–21.

48. Ranade DS, Bapat AM, Ramteke SN, Joshi BN, Roussel P, Tomas A, et al. Thiosemicarbazone modification of 3-acetyl coumarin inhibits Aβ peptide aggregation and protect against Aβ-induced cytotoxicity. Eur. J. Med. Chem. 2016; 121: 803–809.

49. Frasca G, Chiechio S, Vancheri C, Nicoletti F, Copani A, Sortino MA. β-Amyloid-activated cell cycle in SH-SY5Y neuroblastoma Cells. J. Mol. Neurosci. 2004; 22: 231–235. 14997017

50. Bhaskar K, Miller M, Chludzinski A, Herrup K, Zagorski M, Lamb BT. The PI3K-Akt-mTOR pathway regulates Aβ oligomer induced neuronal cell cycle events. Mol. Neurodegener. 2009; 4: 14. doi: 10.1186/1750-1326-4-14 19291319

51. Behl C, Davis JB, Klier FG, Schubert D. Amyloid β peptide induces necrosis rather than apoptosis. Brain Res. 1994; 645: 253–264.

52. Li J, McQuade T, Siemer AB, Napetschnig J, Moriwaki K, Hsiao YS, et al. The RIP1/RIP3 necrosome forms a functional amyloid signaling complex required for programmed necrosis. Cell 2012; 150: 339–350. doi: 10.1016/j.cell.2012.06.019 22817896

53. Xue WF, Hellewell AL, Gosal WS, Homans SW, Hewitt EW, Radford SE. Fibril Fragmentation Enhances Amyloid Cytotoxicity. J. Biol. Chem. 2009; 284: 34272–34282. doi: 10.1074/jbc.M109.049809 19808677

54. Pandey P, Sliker B, Peters HL, Tuli A, Herskovitz J, Smits K, et al. Amyloid precursor protein and amyloid precursor-like protein 2 in cancer. Oncotarget. 2016; 7: 19430–19444. doi: 10.18632/oncotarget.7103 26840089

55. Jin WS, Bu XL, Liu YH, Shen LL, Zhuang ZQ, Jiao SS, et al. Plasma Amyloid-Beta Levels in Patients with Different Types of Cancer. Neurotox. Res. 2017; 31: 283–288. doi: 10.1007/s12640-016-9682-9 27913965

56. Frain L, Swanson D, Cho K, Gagnon D, Lu KP, Betensky RA, et al. Association of cancer and Alzheimer's disease risk in a national cohort of veterans. Alzheimers Dement. 2017; 13: 1364–1370. doi: 10.1016/j.jalz.2017.04.012 28711346

57. Musicco M, Adorni F, Di Santo S, Prinelli F, Pettenati C, Caltagirone C, et al. Inverse occurrence of cancer and Alzheimer disease: a population-based incidence study. Neurology. 2013; 81: 322–328. doi: 10.1212/WNL.0b013e31829c5ec1 23843468

58. White RS, Lipton RB, Hall CB, Steinerman JR. Nonmelanoma skin cancer is associated with reduced Alzheimer disease risk. Neurology. 2013; 80: 1966–1972.

Amyloid β oligomers inhibit growth of human cancer cells

Souhrn

Klíčová slova:

Zdroje

PLOS One

INSIGHTS from European Respiratory Congress

Současné pohledy na riziko v parodontologii

Svět praktické medicíny 3/2024 (znalostní test z časopisu)

Kardiologické projevy hypereozinofilií

Střevní příprava před kolonoskopií