"Cyclophilin A" Enzymatic Effect on the Aggregation Behavior of 1N4R Tau Protein: An Overlooked Crucial Determinant that should be Re-considered in Alzheimer's Disease Pathogenesis


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Background:Neurodegenerative disorders like Alzheimer's disease (AD) involve the abnormal aggregation of tau protein, which forms toxic oligomers and amyloid deposits. The structure of tau protein is influenced by the conformational states of distinct proline residues, which are regulated by peptidyl-prolyl isomerases (PPIases). However, there has been no research on the impact of human cyclophilin A (CypA) as a PPIase on (non-phosphorylated) tau protein aggregation.

Methods:On the basis of these explanations, we used various spectroscopic techniques to explore the effects of CypA on tau protein aggregation behavior.

Results:We demonstrated the role of the isomerization activity of CypA in promoting the formation of tau protein amyloid fibrils with well-defined and highly ordered cross-β structures. According to the \"cistauosis hypothesis,\" CypA's ability to enhance tau protein fibril formation in AD is attributed to the isomerization of specific proline residues from the trans to cis configuration. To corroborate this theory, we conducted refolding experiments using lysozyme as a model protein. The presence of CypA increased lysozyme aggregation and impeded its refolding process. It is known that proper refolding of lysozyme relies on the correct (trans) isomerization of two critical proline residues.

Conclusion:Thus, our findings confirmed that CypA induces the trans-to-cis isomerization of specific proline residues, ultimately leading to increased aggregation. Overall, this study highlights the emerging role of isomerization in tau protein pathogenesis in AD.

作者简介

Samira Ranjbar

Medical Biology Research Center, Health Technology Institute, Kermanshah University of Medical Sciences

Email: info@benthamscience.net

Masomeh Mehrabi

Medical Biology Research Center, Health Technology Institute, Kermanshah University of Medical Sciences

编辑信件的主要联系方式.
Email: info@benthamscience.net

Vali Akbari

Department of Biology, Faculty of Basic Sciences, Lorestan University

Email: info@benthamscience.net

Somayeh Pashaei

Medical Biology Research Center, Health Technology Institute, Kermanshah University of Medical Sciences

Email: info@benthamscience.net

Reza Khodarahmi

Medical Biology Research Center, Health Technology Institute, Kermanshah University of Medical Sciences

编辑信件的主要联系方式.
Email: info@benthamscience.net

参考

  1. McKhann GM, Knopman DS, Chertkow H, et al. The diagnosis of dementia due to Alzheimer’s disease: Recommendations from the National Institute on Aging‐Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimers Dement 2011; 7(3): 263-9. doi: 10.1016/j.jalz.2011.03.005 PMID: 21514250
  2. Fazelinejad H, Zahedi E, Nazarian S, et al. Neuroprotective effect of Bis(Indolyl)phenylmethane in Alzheimer’s disease rat model through inhibition of hen Lysozyme amyloid fibril-induced neurotoxicity. J Indian Chem Soc 2023; 20(3): 551-62. doi: 10.1007/s13738-022-02692-8
  3. Akbari V, Bahramikia S, Jalalvand AR, Mehrabi M, Ezati M, Khodarahmi R. The induction of tau aggregation is restricted by sulfamethoxazole and provides new information regarding the use of the drug. J Biomol Struct Dyn 2023; 19: 1-15. doi: 10.1080/07391102.2023.2273433 PMID: 37878050
  4. Ballatore C, Lee VMY, Trojanowski JQ. Tau-mediated neurodegeneration in Alzheimer’s disease and related disorders. Nat Rev Neurosci 2007; 8(9): 663-72. doi: 10.1038/nrn2194 PMID: 17684513
  5. Akbari V, Mohammadi S, Mehrabi M, Ghobadi S, Farrokhi A, Khodarahmi R. Investigation of the role of prolines 232/233 in RTPPK motif in tau protein aggregation: An in vitro study. Int J Biol Macromol 2022; 219: 1100-11. doi: 10.1016/j.ijbiomac.2022.08.160 PMID: 36049563
  6. Lu KP, Liou YC, Vincent I. Proline‐directed phosphorylation and isomerization in mitotic regulation and in Alzheimer’s Disease. BioEssays 2003; 25(2): 174-81. doi: 10.1002/bies.10223 PMID: 12539244
  7. Hamano T, Enomoto S, Shirafuji N, et al. Autophagy and tau protein. Int J Mol Sci 2021; 22(14): 7475. doi: 10.3390/ijms22147475 PMID: 34299093
  8. Dolan PJ, Johnson GV. The role of tau kinases in Alzheimer’s disease. Curr Opin Drug Discov Devel 2010; 13(5): 595-603. PMID: 20812151
  9. Nakamura K, Greenwood A, Binder L, et al. Proline isomer-specific antibodies reveal the early pathogenic tau conformation in Alzheimer’s disease. Cell 2012; 149(1): 232-44. doi: 10.1016/j.cell.2012.02.016 PMID: 22464332
  10. Lu KP, Kondo A, Albayram O, Herbert MK, Liu H, Zhou XZ. Potential of the antibody against cis–phosphorylated tau in the early diagnosis, treatment, and prevention of Alzheimer disease and brain injury. JAMA Neurol 2016; 73(11): 1356-62. doi: 10.1001/jamaneurol.2016.2027 PMID: 27654282
  11. Yaffe MB, Schutkowski M, Shen M, et al. Sequence-specific and phosphorylation-dependent proline isomerization: a potential mitotic regulatory mechanism. Science 1997; 278(5345): 1957-60. doi: 10.1126/science.278.5345.1957 PMID: 9395400
  12. Lu KP. Pinning down cell signaling, cancer and Alzheimer’s disease. Trends Biochem Sci 2004; 29(4): 200-9. doi: 10.1016/j.tibs.2004.02.002 PMID: 15082314
  13. Lu KP, Finn G, Lee TH, Nicholson LK. Prolyl cis-trans isomerization as a molecular timer. Nat Chem Biol 2007; 3(10): 619-29. doi: 10.1038/nchembio.2007.35 PMID: 17876319
  14. Zeronian MR, Doulkeridou S, van Bergen en Henegouwen PMP, Janssen BJC. Structural insights into the non-inhibitory mechanism of the anti-EGFR EgB4 nanobody. BMC Mol Cell Biol 2022; 23(1): 12. doi: 10.1186/s12860-022-00412-x PMID: 35232398
  15. Blair LJ, Baker JD, Sabbagh JJ, Dickey CA. The emerging role of peptidyl‐prolyl isomerase chaperones in tau oligomerization, amyloid processing, and Alzheimer’s disease. J Neurochem 2015; 133(1): 1-13. doi: 10.1111/jnc.13033 PMID: 25628064
  16. Šimić G, Babić Leko M, Wray S, et al. Tau protein hyperphosphorylation and aggregation in Alzheimer’s disease and other tauopathies, and possible neuroprotective strategies. Biomolecules 2016; 6(1): 6. doi: 10.3390/biom6010006 PMID: 26751493
  17. Chen ZJ, Vetter M, Chang GD, et al. Cyclophilin A functions as an endogenous inhibitor for membrane-bound guanylate cyclase-A. Hypertension 2004; 44(6): 963-8. doi: 10.1161/01.HYP.0000145859.94894.23 PMID: 15466660
  18. Song J, Lu YC, Yokoyama K, Rossi J, Chiu R. Cyclophilin A is required for retinoic acid-induced neuronal differentiation in p19 cells. J Biol Chem 2004; 279(23): 24414-9. doi: 10.1074/jbc.M311406200 PMID: 15047706
  19. Göldner FM, Patrick JW. Neuronal localization of the cyclophilin A protein in the adult rat brain. J Comp Neurol 1996; 372(2): 283-93. doi: 10.1002/(SICI)1096-9861(19960819)372:23.0.CO;2-# PMID: 8863131
  20. Ojaghi S, Mohammadi S, Amani M, et al. Sunset yellow degradation product, as an efficient water-soluble inducer, accelerates 1N4R Tau amyloid oligomerization: In vitro preliminary evidence against the food colorant safety in terms of "Triggered Amyloid Aggregation". Bioorg Chem 2020; 103: 104123. doi: 10.1016/j.bioorg.2020.104123 PMID: 32781343
  21. Mehrabi M, Bijari N, Akbari V, et al. Effective reduction of tau amyloid aggregates in the presence of cyclophilin from Platanus orientalis pollens; An alternative mechanism of action of the allergen. Curr Protein Pept Sci 2023; 24(6): 518-32. doi: 10.2174/1389203724666230530143704 PMID: 37259218
  22. Lowry O, Rosebrough N, Farr AL, Randall R. Protein measurement with the Folin phenol reagent. J Biol Chem 1951; 193(1): 265-75. doi: 10.1016/S0021-9258(19)52451-6 PMID: 14907713
  23. Khademi F, Hamzehee K, Mostafaie A, Hajihossaini R. Purification of three major forms of β-hCG from urine and production of polyclonal antibodies against them. Clin Biochem 2009; 42(13-14): 1476-82. doi: 10.1016/j.clinbiochem.2009.05.019 PMID: 19501580
  24. Farina B, Di Sorbo G, Chambery A, et al. Structural and biochemical insights of CypA and AIF interaction. Sci Rep 2017; 7(1): 1138. doi: 10.1038/s41598-017-01337-8 PMID: 28442737
  25. Sambrook, J.; Russell, D.W. Molecular Cloning: Ch. 8. In Vitro amplification of DNA by the polymerase chain reaction. Vol. 2. Cold Spring Harbor Laboratory Press 2001.
  26. Song F, Zhang X, Ren XB, et al. Cyclophilin A (CyPA) induces chemotaxis independent of its peptidylprolyl cis-trans isomerase activity: direct binding between CyPA and the ectodomain of CD147. J Biol Chem 2011; 286(10): 8197-203. doi: 10.1074/jbc.C110.181347 PMID: 21245143
  27. Moparthi SB, Hammarström P, Carlsson U. A nonessential role for Arg 55 in cyclophilin18 for catalysis of proline isomerization during protein folding. Protein Sci 2009; 18(2): 475-9. doi: 10.1002/pro.28 PMID: 19185003
  28. Fischer G, Bang H, Berger E, Schellenberger A. Conformational specificity of chymotrypsin toward proline-containing substrates. Biochim Biophys Acta Protein Struct Mol Enzymol 1984; 791(1): 87-97. doi: 10.1016/0167-4838(84)90285-1 PMID: 6498206
  29. Hudson SA, Ecroyd H, Kee TW, Carver JA. The thioflavin T fluorescence assay for amyloid fibril detection can be biased by the presence of exogenous compounds. FEBS J 2009; 276(20): 5960-72. doi: 10.1111/j.1742-4658.2009.07307.x PMID: 19754881
  30. Xue C, Lin TY, Chang D, Guo Z. Thioflavin T as an amyloid dye: fibril quantification, optimal concentration and effect on aggregation. R Soc Open Sci 2017; 4(1): 160696. PMID: 28280572
  31. Jangholi A, Ashrafi-Kooshk MR, Arab SS, et al. Appraisal of role of the polyanionic inducer length on amyloid formation by 412-residue 1N4R Tau protein: A comparative study. Arch Biochem Biophys 2016; 609: 1-19. doi: 10.1016/j.abb.2016.09.004 PMID: 27638048
  32. Khodarahmi R, Beyrami M, Soori H. Appraisal of casein’s inhibitory effects on aggregation accompanying carbonic anhydrase refolding and heat-induced ovalbumin fibrillogenesis. Arch Biochem Biophys 2008; 477(1): 67-76. doi: 10.1016/j.abb.2008.04.028 PMID: 18485276
  33. Hur S, Bruice TC. The mechanism of cis-trans isomerization of prolyl peptides by cyclophilin. J Am Chem Soc 2002; 124(25): 7303-13. doi: 10.1021/ja020222s PMID: 12071739
  34. Li G, Cui Q. What is so special about Arg 55 in the catalysis of cyclophilin A? insights from hybrid QM/MM simulations. J Am Chem Soc 2003; 125(49): 15028-38. doi: 10.1021/ja0367851 PMID: 14653737
  35. Inouye H, Sharma D, Goux WJ, Kirschner DA. Structure of core domain of fibril-forming PHF/Tau fragments. Biophys J 2006; 90(5): 1774-89. doi: 10.1529/biophysj.105.070136 PMID: 16339876
  36. Lührs T, Ritter C, Adrian M, et al. 3D structure of Alzheimer’s amyloid-β(1–42) fibrils. Proc Natl Acad Sci USA 2005; 102(48): 17342-7. doi: 10.1073/pnas.0506723102 PMID: 16293696
  37. Brown NR, Noble MEM, Endicott JA, Johnson LN. The structural basis for specificity of substrate and recruitment peptides for cyclin-dependent kinases. Nat Cell Biol 1999; 1(7): 438-43. doi: 10.1038/15674 PMID: 10559988
  38. Zhou XZ, Kops O, Werner A, et al. Pin1-dependent prolyl isomerization regulates dephosphorylation of Cdc25C and tau proteins. Mol Cell 2000; 6(4): 873-83. doi: 10.1016/S1097-2765(05)00083-3 PMID: 11090625
  39. Lim J, Balastik M, Lee TH, et al. Pin1 has opposite effects on wild-type and P301L tau stability and tauopathy. J Clin Invest 2008; 118(5): 1877-89. doi: 10.1172/JCI34308 PMID: 18431510
  40. Poppek D, Keck S, Ermak G, et al. Phosphorylation inhibits turnover of the tau protein by the proteasome: influence of RCAN1 and oxidative stress. Biochem J 2006; 400(3): 511-20. doi: 10.1042/BJ20060463 PMID: 16939415
  41. Lu PJ, Wulf G, Zhou XZ, Davies P, Lu KP. The prolyl isomerase Pin1 restores the function of Alzheimer-associated phosphorylated tau protein. Nature 1999; 399(6738): 784-8. doi: 10.1038/21650 PMID: 10391244
  42. Luna-Muñoz J, Chávez-Macías L, García-Sierra F, Mena R. Earliest stages of tau conformational changes are related to the appearance of a sequence of specific phospho-dependent tau epitopes in Alzheimer’s disease. J Alzheimers Dis 2007; 12(4): 365-75. doi: 10.3233/JAD-2007-12410 PMID: 18198423
  43. Kondo A, Shahpasand K, Mannix R, et al. Antibody against early driver of neurodegeneration cis P-tau blocks brain injury and tauopathy. Nature 2015; 523(7561): 431-6. doi: 10.1038/nature14658 PMID: 26176913
  44. Colgan J, Asmal M, Neagu M, et al. Cyclophilin A regulates TCR signal strength in CD4+ T cells via a proline-directed conformational switch in Itk. Immunity 2004; 21(2): 189-201. doi: 10.1016/j.immuni.2004.07.005 PMID: 15308100
  45. Brazin KN, Mallis RJ, Fulton DB, Andreotti AH. Regulation of the tyrosine kinase Itk by the peptidyl-prolyl isomerase cyclophilin A. Proc Natl Acad Sci USA 2002; 99(4): 1899-904. doi: 10.1073/pnas.042529199 PMID: 11830645
  46. Harrison RK, Stein RL. Substrate specificities of the peptidyl prolyl cis-trans isomerase activities of cyclophilin and FK-506 binding protein: evidence for the existence of a family of distinct enzymes. Biochemistry 1990; 29(16): 3813-6. doi: 10.1021/bi00468a001 PMID: 1693856
  47. Baker JD, Shelton LB, Zheng D, et al. Human cyclophilin 40 unravels neurotoxic amyloids. PLoS Biol 2017; 15(6): e2001336. doi: 10.1371/journal.pbio.2001336 PMID: 28654636
  48. Zhao Y, Ke H. Crystal structure implies that cyclophilin predominantly catalyzes the trans to cis isomerization. Biochemistry 1996; 35(23): 7356-61. doi: 10.1021/bi9602775 PMID: 8652511
  49. Barron SE. Misfolded forms of hen egg white lysozyme. United Kingdom: University of Glasgow 2001.
  50. Rajan R, Ahmed S, Sharma N, Kumar N, Debas A, Matsumura K. Review of the current state of protein aggregation inhibition from a materials chemistry perspective: special focus on polymeric materials. Materials Advances 2021; 2(4): 1139-76. doi: 10.1039/D0MA00760A
  51. Limorenko G, Lashuel HA. Revisiting the grammar of Tau aggregation and pathology formation: how new insights from brain pathology are shaping how we study and target Tauopathies. Chem Soc Rev 2022; 51(2): 513-65. doi: 10.1039/D1CS00127B PMID: 34889934
  52. Favretto F, Flores D, Baker JD, et al. Catalysis of proline isomerization and molecular chaperone activity in a tug-of-war. Nat Commun 2020; 11(1): 6046. doi: 10.1038/s41467-020-19844-0 PMID: 33247146
  53. Hill SE, Esquivel AR, Ospina SR, Rahal LM, Dickey CA, Blair LJ. Chaperoning activity of the cyclophilin family prevents tau aggregation. Protein Sci 2022; 31(11): e4448. doi: 10.1002/pro.4448 PMID: 36305768
  54. Maeda S, Sato Y, Takashima A. Frontotemporal dementia with Parkinsonism linked to chromosome-17 mutations enhance tau oligomer formation. Neurobiol Aging 2018; 69: 26-32. doi: 10.1016/j.neurobiolaging.2018.04.014 PMID: 29852407

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