Cited by 9Alzheimer's disease research and treatmentsCell death mechanisms and regulationPancreatic and Hepatic Oncology Research

Inhibition of Pancreatic Cancer Cells by Different Amyloid Proteins Reveals an Inverse Relationship between Neurodegenerative Diseases and Cancer

Open access
Tang, Yijing, Zhang, Dong, Robinson, Sarah, Zheng, Jie·2023·Advanced Biology

Abstract

Neurodegenerative diseases and cancers are considered to be two families of diseases caused by completely opposite cell‐death mechanisms: the former caused by premature cell death, with the latter due to the increased resistance to cell death. Growing epidemiologic evidence appear to suggest an inverse correlation between neurodegenerative diseases and cancers. However, pathological links, particularly from a protein‐cell interaction perspective, between these two families of diseases remains to be proven. Here, a fundamental study investigates the effects of three amyloid proteins of Aβ (associated with AD), hIAPP (associated with T2D), and hCT (associated with MTC) on pancreatic cancer (PANC‐1) cells. Collective results demonstrate a general inhibitory activity of all of three amyloid proteins on cancer cell proliferation, but inhibition efficiencies are strongly dependent on amyloid sequence (Aβ, hIAPP, hCT), concentration (IC25, IC50, IC75), and aggregation states (monomers, oligomers). Amyloid proteins exhibit two pathways against cancer cells: amyloid monomer‐induced ROS production to inhibit cell growth and amyloid oligomer‐induced membrane disruption to kill cells. Collectively, the results demonstrate a general inhibition function of amyloid proteins to induce cancer cell death by preventing cell proliferation, suppressing cell migration, promoting reactive oxygen species production, and disrupting cell membranes.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1002/adbi.202300070

Cites

2 of 2 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 63

  1. C. Lanni, M. Masi, M. Racchi, S. Govoni, Mol. Psychiatry 2021, 26, 280.
  2. Y. Takamatsu, G. Ho, M. Hashimoto, Trends Cancer 2020, 6, 624.
  3. J. A. Driver, Biogerontology 2014, 15, 547.
  4. J. Seo, M. Park, Cell. Mol. Life Sci. 2020, 77, 2659.
  5. H. Plun-Favreau, P. A. Lewis, J. Hardy, L. M. Martins, N. W. Wood, PLoS Genet. 2010, 6, e1001257.
  6. Y. Tang, D. Zhang, Y. Chang, J. Zheng, ACS Chem. Neurosci. 2023, 14, 312.
  7. R. C. Brown, A. H. Lockwood, B. R. Sonawane, Environ. Health Per- spect. 2005, 113, 1250.
  8. T. Farooqui, A. A. Farooqui, Mech. Ageing Dev. 2009, 130, 203.
  9. A. Fumia, N. Cicero, M. Gitto, N. Nicosia, A. Alesci, Nat. Prod. Res. 2022, 36, 5916.
  10. Y. Tang, D. Zhang, Y. Zhang, Y. Liu, Y. Miller, K. Gong, J. Zheng, Com- mun. Biol. 2022, 5, 417.
  11. V. N. Anisimov, Cancer Control 2007, 14, 23.
  12. C. E. DeSantis, K. D. Miller, W. Dale, S. G. Mohile, H. J. Cohen, C. R. Leach, A. G. Sauer, A. Jemal, R. L. Siegel, Ca-Cancer J. Clin. 2019, 69, 452.
  13. R. L. Siegel, K. D. Miller, H. E. Fuchs, A. Jemal, Ca-Cancer J. Clin. 2022, 72, 7.
  14. S. Pilleron, D. Sarfati, M. Janssen-Heijnen, J. Vignat, J. Ferlay, F. Bray, I. Soerjomataram, Int. J. Cancer 2019, 144, 49.
  15. A. L. Houck, S. Seddighi, J. A. Driver, Curr. Aging Sci. 2018, 11, 77.
  16. M. Ospina-Romero, M. M. Glymour, E. Hayes-Larson, E. R. Mayeda, R. E. Graff, W. D. Brenowitz, S. F. Ackley, J. S. Witte, L. C. Kobayashi, JAMA Netw Open 2020, 3, e2025515.
  17. S. Majd, J. Power, Z. Majd, Front. Neurosci. 2019, 13, 155.
  18. J. A. Driver, A. Beiser, R. Au, B. E. Kreger, G. L. Splansky, T. Kurth, D. P. Kiel, K. P. Lu, S. Seshadri, P. A. Wolf, BMJ 2012, 344, e1442.
  19. M. Ejma, N. Madetko, A. Brzecka, K. Guranski, P. Alster, M. Misiuk- Hojło, S. G. Somasundaram, C. E. Kirkland, G. Aliev, Biomedicines 2020, 8, 416.
  20. B. Jansson, J. Jankovic, Ann. Neurol. 1985, 17, 505.
  21. M. I. Behrens, C. Lendon, C. M. Roe, Curr. Alzheimer Res. 2009, 6, 196.
  22. S. A. Sørensen, K. Fenger, J. H. Olsen, Cancer 1999, 86, 1342.
  23. H. N. Lee, M. S. Jeong, S. B. Jang, Int. J. Mol. Sci. 2021, 22, 4999.
  24. K. Takagi, S. Ito, T. Miyazaki, Y. Miki, Y. Shibahara, T. Ishida, M. Watan- abe, S. Inoue, H. Sasano, T. Suzuki, Cancer Sci. 2013, 104, 1532.
  25. J. Y. S. Tsang, M. A. Lee, T. H. Chan, J. Li, Y. B. Ni, Y. Shao, S. K. Chan, S. Y. Cheungc, K. F. Lau, G. M. K. Tse, eBioMedicine 2018, 38, 89.
  26. H. Qin, T. Cui, Z. Liu, Y. Zhou, J. Niu, J. Ren, X. Qu, Nano Lett. 2021, 21, 7379.
  27. B. Pavliukeviciene, A. Zentelyte, M. Jankunec, G. Valiuliene, M. Ta- laikis, R. Navakauskiene, G. Niaura, G. Valincius, PLoS One 2019, 14, e0221563.
  28. S. Luo, J. Feng, L. Xiao, L. Guo, L. Deng, Z. Du, Y. Xue, X. Song, X. Sun, Z. Zhang, Y. Fu, T. Gong, Biomaterials 2020, 249, 120055.
  29. D.-C. Chan, C.-J. Chen, H.-C. Chu, W.-K. Chang, J.-C. Yu, Y.-J. Chen, L.- L. Wen, S.-C. Huang, C.-H. Ku, Y.-C. Liu, J. H. Chen, Ann. Surg. Oncol. 2007, 14, 84.
  30. W. C. S. Cho, T. T. Yip, W. W. Cheng, J. S. K. Au, Br. J. Cancer 2010, 102, 1731.
  31. E. Cocco, S. Bellone, K. El-Sahwi, M. Cargnelutti, N. Buza, F. A. Tavas- soli, P. E. Schwartz, T. J. Rutherford, S. Pecorelli, A. D. Santin, Cancer 2010, 116, 843.
  32. G. Zhang, X. Sun, H. Lv, X. Yang, X. Kang, Oncol. Lett. 2012, 3, 940.
  33. L. Le, K. Chi, S. Tyldesley, S. Flibotte, D. L. Diamond, M. A. Kuzyk, M. D. Sadar, Clin. Chem. 2005, 51, 695.
  34. C. Soto, S. Pritzkow, Nat. Neurosci. 2018, 21, 1332.
  35. J. Gandhi, A. C. Antonelli, A. Afridi, S. Vatsia, G. Joshi, V. Romanov, I. V. Murray, S. A. Khan, Rev. Neurosci. 2019, 30, 339.
  36. A. Gámez, P. Yuste-Checa, S. Brasil, Á. Briso-Montiano, L. R. Desviat, M. Ugarte, C. Pérez-Cerdá, B. Pérez, Clin. Genet. 2018, 93, 450.
  37. X. Yi, Y. Zhang, M. Gong, X. Yu, N. Darabedian, J. Zheng, F. Zhou, Biochemistry 2015, 54, 6323.
  38. M. G. Iadanza, M. P. Jackson, E. W. Hewitt, N. A. Ranson, S. E. Rad- ford, Nat. Rev. Mol. Cell Biol. 2018, 19, 755.
  39. F. Chiti, C. M. Dobson, Annu. Rev. Biochem. 2006, 75, 333.
  40. A. Saha, S. Mohapatra, P. Kurkute, B. Jana, P. Mondal, D. Bhunia, S. Ghosh, S. Ghosh, Chem. Commun. 2015, 51, 2249.
  41. V. S. Ramasamy, M. I. Islam, M. A. Haque, S. Y. Shin, I.-S. Park, Biochim. Biophys. Acta 2016, 1863, 1189.
  42. D. Paris, K. Townsend, A. Quadros, J. Humphrey, J. Sun, S. Brem, M. Wotoczek-Obadia, A. DelleDonne, N. Patel, D. F. Obregon, Angiogen- esis 2004, 7, 75.
  43. H. Dillekås, M. S. Rogers, O. Straume, Cancer Med. 2019, 8, 5574.
  44. C. L. Chaffer, R. A. Weinberg, Science 2011, 331, 1559.
  45. G. P. Gupta, J. Massagué, Cell 2006, 127, 679.
  46. J. E. Lee, D. Kim, J. H. Lee, Dementia Neurocognit. Disord. 2018, 17, 137.
  47. S.-M. Ou, Y.-J. Lee, Y.-W. Hu, C.-J. Liu, T.-J. Chen, J.-L. Fuh, S.-J. Wang, Neuroepidemiology 2013, 40, 42.
  48. J.-H. Park, D.-H. Kim, Y.-G. Park, D.-Y. Kwon, M. Choi, J.-H. Jung, K. Han, Eur. J. Cancer B Oral Oncol. 2019, 117, 5.
  49. J. Wang, B. J. Gu, C. L. Masters, Y.-J. Wang, Nat. Rev. Neurol. 2017, 13, 612.
  50. Y. Zhang, Y. Liu, Y. Tang, D. Zhang, H. He, J. Wu, J. Zheng, Chem. Sci. 2021, 12, 9124.
  51. Y. Tang, D. Zhang, X. Gong, J. Zheng, Chem. Sci. 2022, 13, 7143.
  52. M. Zhang, J. Zhao, J. Zheng, Soft Matter 2014, 10, 7425.
  53. D. Javadrashid, A. Baghbanzadeh, A. Derakhshani, P. Leone, N. Sil- vestris, V. Racanelli, A. G. Solimando, B. Baradaran, Biomedicines 2021, 9, 373.
  54. S. H. Kiaie, M. J. Sanaei, M. Heshmati, Z. Asadzadeh, I. Azimi, S. Hadidi, R. Jafari, B. Baradaran, Acta Pharm. Sin. B 2021, 11, 1083.
  55. C. Sinthuvanich, A. S. Veiga, K. Gupta, D. Gaspar, R. Blumenthal, J. P. Schneider, J. Am. Chem. Soc. 2012, 134, 6210.
  56. X. Dong, Q. Qiao, Z. Qian, G. Wei, Biochim. Biophys. Acta, Biomembr. 2018, 1860, 1826.
  57. A. Quist, I. Doudevski, H. Lin, R. Azimova, D. Ng, B. Frangione, B. Kagan, J. Ghiso, R. Lal, Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 10427.
  58. Y. Sokolov, J. A. Kozak, R. Kayed, A. Chanturiya, C. Glabe, J. E. Hall, J. Gen. Physiol. 2006, 128, 637.
  59. R. Kayed, Y. Sokolov, B. Edmonds, T. M. McIntire, S. C. Milton, J. E. Hall, C. G. Glabe, J. Biol. Chem. 2004, 279, 46363.
  60. R. Capone, F. G. Quiroz, P. Prangkio, I. Saluja, A. M. Sauer, M. R. Bautista, R. S. Turner, J. Yang, M. Mayer, Neurotoxic. Res. 2009, 16, 1.
  61. J. R. Brender, U. H. Durr, D. Heyl, M. B. Budarapu, A. Ramamoorthy, Bioch. Biophys. Acta 2007, 1768, 2026.
  62. M. K. Siddiqi, S. Malik, N. Majid, P. Alam, R. H. Khan, Adv. Protein Chem. Struct. Biol. 2019, 118, 333.
  63. T. A. Mirzabekov, M. C. Lin, B. L. Kagan, J. Biol. Chem. 1996, 271, 1988.

Cited by

Sorted by citations

Authors
Tang, Y., Zhang, D., Robinson, S., & Zheng, J.
Affiliations
University of Akron (US)
Corresponding author
Zheng, Jie
Venue
Advanced Biology
Publisher
Wiley
Published
2023-04-20
Volume
7
Issue
8
Pages
e2300070-e2300070
ISSN
2701-0198 (ISSN-L)
OpenAlex
W4366465258
Cited by
9
References
2
Citations by year
2026: 3 · 2025: 4 · 2024: 1 · 2023: 1
FWCI
1.59
Type
journal article
Language
en
Open access
Locations
  • Advanced Biology (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • National Science Foundation (2107619)
  • Division of Chemical, Bioengineering, Environmental, and Transport Systems (2107619, CBET-2107619)
Topics
  • Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
  • Health Sciences › Medicine › Oncology › Pancreatic and Hepatic Oncology Research
Keywords
pancreatic cancer, amyloid proteins, human islet amyloid polypeptide, cancer cell proliferation inhibition, reactive oxygen species, membrane damage, amyloid oligomers, PANC-1 cells, cell migration
MeSH terms
Amyloid, Humans, Pancreatic Hormones, Pancreatic Neoplasms, Neurodegenerative Diseases, Amyloidogenic Proteins, Islet Amyloid Polypeptide

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review