Login Register Cart 0
Generic placeholder image

Current Protein & Peptide Science

Editor-in-Chief

ISSN (Print): 1389-2037
ISSN (Online): 1875-5550

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Research Article

Effective Reduction of Tau Amyloid Aggregates in the Presence of Cyclophilin from Platanus orientalis Pollens; An Alternative Mechanism of Action of the Allergen

Author(s): Masomeh Mehrabi, Nooshin Bijari*, Vali Akbari, Samira Ranjbar, Saeed Karima, Mojtaba Sankian, Sara Ojaghi and Reza Khodarahmi*

Volume 24, Issue 6, 2023

Published on: 21 June, 2023

Page: [518 - 532] Pages: 15

DOI: 10.2174/1389203724666230530143704

Price: $65

Abstract

Background: A hallmark pathology of Alzheimer's disease (AD) is the construction of neurofibrillary tangles, which are made of hyperphosphorylated Tau. The cis-proline isomer of the pThr/Ser-Pro sequence has been suggested to act as an aggregation precursor according to the ‘Cistauosis’ hypothesis; however, this aggregation scheme is not yet completely approved. Various peptidyl-prolyl isomerases (PPIases) may specifically isomerize cis/trans-proline bonds and restitute Tau's ability to attach microtubules and may control Tau amyloid aggregation in AD.

Methods: In this study, we provided experimental evidence for indicating the effects of the plant Cyclophilin (P-Cyp) from Platanus orientalis pollens on the Tau aggregation by various spectroscopic techniques.

Results: Our findings disclosed that the rate/extent of amyloid formation in the Tau sample which is incubated with P-Cyp decreased and these observations do not seem to be due to the macromolecular crowding effect. Also, as proven that 80% of the prolines in the unfolded protein are in the trans conformation, urea-induced unfolding analyses confirmed this conclusion and showed that the aggregation rate/extent of urea-treated Tau samples decreased compared with those of the native protein. Also, XRD analysis indicated the reduction of scattering intensities and beta structures of amyloid fibrils in the presence of P-Cyp. Therefore, the ability of P-Cyp to suppress Tau aggregation probably depends on cis to trans isomerization of proline peptide bonds (X-Pro) and decreasing cis isomers in vitro.

Conclusion: The findings of the current study may inspire possible protective/detrimental effects of various types of cyclophilins on AD onset/progression through direct regulation of intracellular Tau molecules and provides evidence that a protein from a plant source is able to enter the cell cytoplasm and may affect the behavior of cytoplasmic proteins.

« Previous
Graphical Abstract

[1]
Kosik, K.S.; Duffy, L.K.; Dowling, M.M.; Abraham, C.; McCluskey, A.; Selkoe, D.J. Microtubule-associated protein 2: monoclonal antibodies demonstrate the selective incorporation of certain epitopes into Alzheimer neurofibrillary tangles. Proc. Natl. Acad. Sci. USA, 1984, 81(24), 7941-7945.
[http://dx.doi.org/10.1073/pnas.81.24.7941] [PMID: 6083566]
[2]
Hardy, J. The relationship between amyloid and tau. J. Mol. Neurosci., 2003, 20(2), 203-206.
[http://dx.doi.org/10.1385/JMN:20:2:203] [PMID: 12794314]
[3]
McKee, A.C.; Stein, T.D.; Nowinski, C.J.; Stern, R.A.; Daneshvar, D.H.; Alvarez, V.E.; Lee, H.S.; Hall, G.; Wojtowicz, S.M.; Baugh, C.M.; Riley, D.O.; Kubilus, C.A.; Cormier, K.A.; Jacobs, M.A.; Martin, B.R.; Abraham, C.R.; Ikezu, T.; Reichard, R.R.; Wolozin, B.L.; Budson, A.E.; Goldstein, L.E.; Kowall, N.W.; Cantu, R.C. The spectrum of disease in chronic traumatic encephalopathy. Brain, 2013, 136(1), 43-64.
[http://dx.doi.org/10.1093/brain/aws307] [PMID: 23208308]
[4]
Wang, Y.; Mandelkow, E. Tau in physiology and pathology. Nat. Rev. Neurosci., 2016, 17(1), 22-35.
[http://dx.doi.org/10.1038/nrn.2015.1] [PMID: 26631930]
[5]
Ballatore, C.; Lee, V.M.Y.; Trojanowski, J.Q. Tau-mediated neurodegeneration in Alzheimer’s disease and related disorders. Nat. Rev. Neurosci., 2007, 8(9), 663-672.
[http://dx.doi.org/10.1038/nrn2194] [PMID: 17684513]
[6]
Akbari, V; Mohammadi, S; Mehrabi, M; Ghobadi, S; Farrokhi, A; Khodarahmi, RJ 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, 1100-1111.
[7]
Ramachandran, G.; Udgaonkar, J.B. Understanding the kinetic roles of the inducer heparin and of rod-like protofibrils during amyloid fibril formation by Tau protein. J. Biol. Chem., 2011, 286(45), 38948-38959.
[http://dx.doi.org/10.1074/jbc.M111.271874] [PMID: 21931162]
[8]
Pallo, S.P.; Johnson, G.V.W. Tau facilitates Aβ-induced loss of mitochondrial membrane potential independent of cytosolic calcium fluxes in mouse cortical neurons. Neurosci. Lett., 2015, 597, 32-37.
[http://dx.doi.org/10.1016/j.neulet.2015.04.021] [PMID: 25888814]
[9]
Jangholi, A; Ashrafi-Kooshk, MR; Arab, SS; Riazi, G; Mokhtari, F; Poorebrahim, M; Mahdiuni, H; Kurganov, BI; Moosavi-Movahedi, A.A.; Khodarahmi, R 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.
[10]
Lu, K.P.; Liou, Y.C.; Vincent, I. Proline-directed phosphorylation and isomerization in mitotic regulation and in Alzheimer’s Disease. BioEssays, 2003, 25(2), 174-181.
[http://dx.doi.org/10.1002/bies.10223] [PMID: 12539244]
[11]
Dolan, P.J.; Johnson, G.V. The role of tau kinases in Alzheimer’s disease. Curr. Opin. Drug Discov. Devel., 2010, 13(5), 595-603.
[PMID: 20812151]
[12]
Nakamura, K.; Greenwood, A.; Binder, L.; Bigio, E.H.; Denial, S.; Nicholson, L.; Zhou, X.Z.; Lu, K.P. Proline isomer-specific antibodies reveal the early pathogenic tau conformation in Alzheimer’s disease. Cell, 2012, 149(1), 232-244.
[http://dx.doi.org/10.1016/j.cell.2012.02.016] [PMID: 22464332]
[13]
Lu, K.P.; Kondo, A.; Albayram, O.; Herbert, M.K.; Liu, H.; Zhou, X.Z. 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), 1356-1362.
[http://dx.doi.org/10.1001/jamaneurol.2016.2027] [PMID: 27654282]
[14]
Yaffe, M.B.; Schutkowski, M.; Shen, M.; Zhou, X.Z.; Stukenberg, P.T.; Rahfeld, J.U.; Xu, J.; Kuang, J.; Kirschner, M.W.; Fischer, G.; Cantley, L.C.; Lu, K.P. Sequence-specific and phosphorylation-dependent proline isomerization: a potential mitotic regulatory mechanism. Science, 1997, 278(5345), 1957-1960.
[http://dx.doi.org/10.1126/science.278.5345.1957] [PMID: 9395400]
[15]
Lu, K.P. Pinning down cell signaling, cancer and Alzheimer’s disease. Trends Biochem. Sci., 2004, 29(4), 200-209.
[http://dx.doi.org/10.1016/j.tibs.2004.02.002] [PMID: 15082314]
[16]
Lu, K.P.; Finn, G.; Lee, T.H.; Nicholson, L.K. Prolyl cis-trans isomerization as a molecular timer. Nat. Chem. Biol., 2007, 3(10), 619-629.
[http://dx.doi.org/10.1038/nchembio.2007.35] [PMID: 17876319]
[17]
Lu, P.J.; Wulf, G.; Zhou, X.Z.; Davies, P.; Lu, K.P. The prolyl isomerase Pin1 restores the function of Alzheimer-associated phosphorylated tau protein. Nature, 1999, 399(6738), 784-788.
[http://dx.doi.org/10.1038/21650] [PMID: 10391244]
[18]
Liou, Y.C.; Sun, A.; Ryo, A.; Zhou, X.Z.; Yu, Z.X.; Huang, H.K.; Uchida, T.; Bronson, R.; Bing, G.; Li, X.; Hunter, T.; Lu, K.P. Role of the prolyl isomerase Pin1 in protecting against age-dependent neurodegeneration. Nature, 2003, 424(6948), 556-561.
[http://dx.doi.org/10.1038/nature01832] [PMID: 12891359]
[19]
Lim, J.; Balastik, M.; Lee, T.H.; Nakamura, K.; Liou, Y.C.; Sun, A.; Finn, G.; Pastorino, L.; Lee, V.M.Y.; Lu, K.P. Pin1 has opposite effects on wild-type and P301L tau stability and tauopathy. J. Clin. Invest., 2008, 118(5), 1877-1889.
[http://dx.doi.org/10.1172/JCI34308] [PMID: 18431510]
[20]
Kondo, A.; Shahpasand, K.; Mannix, R.; Qiu, J.; Moncaster, J.; Chen, C.H.; Yao, Y.; Lin, Y.M.; Driver, J.A.; Sun, Y.; Wei, S.; Luo, M.L.; Albayram, O.; Huang, P.; Rotenberg, A.; Ryo, A.; Goldstein, L.E.; Pascual-Leone, A.; McKee, A.C.; Meehan, W.; Zhou, X.Z.; Lu, K.P. Antibody against early driver of neurodegeneration cis P-tau blocks brain injury and tauopathy. Nature, 2015, 523(7561), 431-436.
[http://dx.doi.org/10.1038/nature14658] [PMID: 26176913]
[21]
Zhou, X.Z.; Kops, O.; Werner, A.; Lu, P.J.; Shen, M.; Stoller, G.; Küllertz, G.; Stark, M.; Fischer, G.; Lu, K.P. Pin1-dependent prolyl isomerization regulates dephosphorylation of Cdc25C and tau proteins. Mol. Cell, 2000, 6(4), 873-883.
[http://dx.doi.org/10.1016/S1097-2765(05)00083-3] [PMID: 11090625]
[22]
Hamdane, M.; Dourlen, P.; Bretteville, A.; Sambo, A.V.; Ferreira, S.; Ando, K.; Kerdraon, O.; Bégard, S.; Geay, L.; Lippens, G.; Sergeant, N.; Delacourte, A.; Maurage, C.A.; Galas, M.C.; Buée, L. Pin1 allows for differential Tau dephosphorylation in neuronal cells. Mol. Cell. Neurosci., 2006, 32(1-2), 155-160.
[http://dx.doi.org/10.1016/j.mcn.2006.03.006] [PMID: 16697218]
[23]
Janus, C.; Pearson, J.; McLaurin, J.; Mathews, P.M.; Jiang, Y.; Schmidt, S.D.; Chishti, M.A.; Horne, P.; Heslin, D.; French, J.; Mount, H.T.J.; Nixon, R.A.; Mercken, M.; Bergeron, C.; Fraser, P.E.; St George-Hyslop, P.; Westaway, D. Aβ peptide immunization reduces behavioural impairment and plaques in a model of Alzheimer’s disease. Nature, 2000, 408(6815), 979-982.
[http://dx.doi.org/10.1038/35050110] [PMID: 11140685]
[24]
Pastorino, L.; Sun, A.; Lu, P.J.; Zhou, X.Z.; Balastik, M.; Finn, G.; Wulf, G.; Lim, J.; Li, S.H.; Li, X.; Xia, W.; Nicholson, L.K.; Lu, K.P. The prolyl isomerase Pin1 regulates amyloid precursor protein processing and amyloid-β production. Nature, 2006, 440(7083), 528-534.
[http://dx.doi.org/10.1038/nature04543] [PMID: 16554819]
[25]
Lu, K.P.; Zhou, X.Z. The prolyl isomerase PIN1: A pivotal new twist in phosphorylation signalling and disease. Nat. Rev. Mol. Cell Biol., 2007, 8(11), 904-916.
[http://dx.doi.org/10.1038/nrm2261] [PMID: 17878917]
[26]
Chen, C.H.; Li, W.; Sultana, R.; You, M.H.; Kondo, A.; Shahpasand, K.; Kim, B.M.; Luo, M.L.; Nechama, M.; Lin, Y.M.; Yao, Y.; Lee, T.H.; Zhou, X.Z.; Swomley, A.M.; Butterfield, D.A.; Zhang, Y.; Lu, K.P. Pin1 cysteine-113 oxidation inhibits its catalytic activity and cellular function in Alzheimer’s disease. Neurobiol. Dis., 2015, 76, 13-23.
[http://dx.doi.org/10.1016/j.nbd.2014.12.027] [PMID: 25576397]
[27]
Davies, P. Characterization and use of monoclonal antibodies to tau and paired helical filament tau. Alzheimer’s Disease; Springer, 2000, pp. 361-373.
[28]
Ge, Y.S.; Teng, W.Y.; Zhang, C.D. Protective effect of cyclophilin A against Alzheimer’s amyloid beta-peptide (25-35)-induced oxidative stress in PC12 cells. Chin. Med. J. (Engl.), 2009, 122(6), 716-724.
[PMID: 19323941]
[29]
Kaur, G.; Singh, S.; Dutta, T.; Kaur, H.; Singh, B.; Pareek, A.; Singh, P. The peptidyl-prolyl cis-trans isomerase activity of the wheat cyclophilin, TaCypA-1, is essential for inducing thermotolerance in Escherichia coli. Biochim. Open, 2016, 2, 9-15.
[http://dx.doi.org/10.1016/j.biopen.2015.11.003] [PMID: 29632833]
[30]
Zeronian, MR; Doulkeridou, S Structural insights into the noninhibitory mechanism of the anti-EGFR EgB4 nanobody. BMC Mol. Cell. Biol., 2022, 23(1), 12.
[31]
Theillet, F-X; Kalmar, L; Tompa, P; Han, K-H; Selenko, P; Dunker, AK; Daughdrill, GW; Uversky, VN The alphabet of intrinsic disorder: I. Act like a Pro: On the abundance and roles of proline residues in intrinsically disordered proteins. Intrinsically Disord. Proteins, 2013, 1(1), e24360.
[32]
Favretto, F; Baker, JD; Strohäker, T; Andreas, LB; Blair, LJ; Becker, S; Zweckstetter, M The molecular basis of the interaction of Cyclophilin A with α‐Synuclein. Angew. Chem. Int. Ed. Engl., 2020, 59(14), 5643-5646.
[33]
Pazouki, N.; Sankian, M.; Nejadsattari, T.; Khavari-Nejad, R-A.; Varasteh, A-R. Eds.;. Oriental plane pollen allergy: Identification of allergens and cross-reactivity between relevant species. Allergy and Asthma Proceedings; OceanSide Publications, 2008.
[34]
Pazouki, N; Sankian, M; Leung, PT; Nejadsattari, T; Khavari-Nejad, R-A Identification of cyclophilin as a novel allergen from Platanus orientalis pollens by mass spectrometry. J. Biosci. Bioeng., 2009, 107(2), 215-217.
[35]
Ojaghi, S.; Mohammadi, S.; Amani, M.; Ghobadi, S.; Bijari, N.; Esmaeili, S.; Khodarahmi, R. 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.
[http://dx.doi.org/10.1016/j.bioorg.2020.104123] [PMID: 32781343]
[36]
Sankian, M.; Vahedi, F.; Pazouki, N.; Moghadam, M.; Jabbari Azad, F.; Varasteh, A-R. Cloning and expression of cyclophilin from Platanus orientalis pollens in Escherichia coli. Rep. Biochem. Mol. Biol., 2012, 1(1), 25-29.
[PMID: 26989705]
[37]
Khademi, F; Hamzehee, K; Mostafaie, A; Hajihossaini, RJ Purification of three major forms of β-hCG from urine and production of polyclonal antibodies against them. Clin. Biochem., 2009, 42(13-14), 1476-1482.
[38]
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.
[http://dx.doi.org/10.1016/0167-4838(84)90285-1] [PMID: 6498206]
[39]
Xue, C.; Lin, T.Y.; 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.
[http://dx.doi.org/10.1098/rsos.160696] [PMID: 28280572]
[40]
Kofron, J.L.; Kuzmic, P.; Kishore, V.; Colón-Bonilla, E.; Rich, D.H. Determination of kinetic constants for peptidyl prolyl cis-trans isomerases by an improved spectrophotometric assay. Biochemistry, 1991, 30(25), 6127-6134.
[http://dx.doi.org/10.1021/bi00239a007] [PMID: 2059621]
[41]
Compton, L.A.; Davis, J.M.; MacDonald, J.R.; Bächinger, H.P. Structural and functional characterization of Escherichia coli peptidyl-prolyl cis-trans isomerases. Eur. J. Biochem., 1992, 206(3), 927-934.
[http://dx.doi.org/10.1111/j.1432-1033.1992.tb17002.x] [PMID: 1606970]
[42]
Shen, L.; Liu, C.C.; An, C.Y.; Ji, H.F. How does curcumin work with poor bioavailability? Clues from experimental and theoretical studies. Sci. Rep., 2016, 6(1), 20872.
[http://dx.doi.org/10.1038/srep20872] [PMID: 26887346]
[43]
Chiti, F.; Dobson, C.M. Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem., 2006, 75(1), 333-366.
[http://dx.doi.org/10.1146/annurev.biochem.75.101304.123901] [PMID: 16756495]
[44]
Relini, A.; De Stefano, S.; Torrassa, S.; Cavalleri, O.; Rolandi, R.; Gliozzi, A.; Giorgetti, S.; Raimondi, S.; Marchese, L.; Verga, L.; Rossi, A.; Stoppini, M.; Bellotti, V. Heparin strongly enhances the formation of β2-microglobulin amyloid fibrils in the presence of type I collagen. J. Biol. Chem., 2008, 283(8), 4912-4920.
[http://dx.doi.org/10.1074/jbc.M702712200] [PMID: 18056266]
[45]
Umemoto, A.; Yagi, H.; So, M.; Goto, Y. High-throughput analysis of ultrasonication-forced amyloid fibrillation reveals the mechanism underlying the large fluctuation in the lag time. J. Biol. Chem., 2014, 289(39), 27290-27299.
[http://dx.doi.org/10.1074/jbc.M114.569814] [PMID: 25118286]
[46]
Dinkel, P.D.; Holden, M.R.; Matin, N.; Margittai, M. RNA binds to tau fibrils and sustains template-assisted growth. Biochemistry, 2015, 54(30), 4731-4740.
[http://dx.doi.org/10.1021/acs.biochem.5b00453] [PMID: 26177386]
[47]
Jangholi, A.; Ashrafi-Kooshk, M.R.; Arab, S.S.; Karima, S.; Poorebrahim, M.; Ghadami, S.A.; Moosavi-Movahedi, A.A.; Khodarahmi, R. Can any “non-specific charge modification within microtubule binding domains of Tau” be a prerequisite of the protein amyloid aggregation? An in vitro study on the 1N4R isoform. Int. J. Biol. Macromol., 2018, 109, 188-204.
[http://dx.doi.org/10.1016/j.ijbiomac.2017.12.071] [PMID: 29248553]
[48]
Lim, S.; Haque, M.M.; Kim, D.; Kim, D.J.; Kim, Y.K. Cell-based models to investigate Tau aggregation. Comput. Struct. Biotechnol. J., 2014, 12(20-21), 7-13.
[http://dx.doi.org/10.1016/j.csbj.2014.09.011] [PMID: 25505502]
[49]
Carlson, S.W.; Branden, M.; Voss, K.; Sun, Q.; Rankin, C.A.; Gamblin, T.C. A complex mechanism for inducer mediated tau polymerization. Biochemistry, 2007, 46(30), 8838-8849.
[http://dx.doi.org/10.1021/bi700403a] [PMID: 17608454]
[50]
von Bergen, M.; Barghorn, S.; Müller, S.A.; Pickhardt, M.; Biernat, J.; Mandelkow, E.M.; Davies, P.; Aebi, U.; Mandelkow, E. The core of tau-paired helical filaments studied by scanning transmission electron microscopy and limited proteolysis. Biochemistry, 2006, 45(20), 6446-6457.
[http://dx.doi.org/10.1021/bi052530j] [PMID: 16700555]
[51]
Zhu, H.L.; Fernández, C.; Fan, J.B.; Shewmaker, F.; Chen, J.; Minton, A.P.; Liang, Y. Quantitative characterization of heparin binding to Tau protein: Implication for inducer-mediated Tau filament formation. J. Biol. Chem., 2010, 285(6), 3592-3599.
[http://dx.doi.org/10.1074/jbc.M109.035691] [PMID: 19959468]
[52]
Sibille, N.; Sillen, A.; Leroy, A.; Wieruszeski, J.M.; Mulloy, B.; Landrieu, I.; Lippens, G. Structural impact of heparin binding to full-length Tau as studied by NMR spectroscopy. Biochemistry, 2006, 45(41), 12560-12572.
[http://dx.doi.org/10.1021/bi060964o] [PMID: 17029411]
[53]
Congdon, E.E.; Kim, S.; Bonchak, J.; Songrug, T.; Matzavinos, A.; Kuret, J. Nucleation-dependent tau filament formation: The importance of dimerization and an estimation of elementary rate constants. J. Biol. Chem., 2008, 283(20), 13806-13816.
[http://dx.doi.org/10.1074/jbc.M800247200] [PMID: 18359772]
[54]
Fichou, Y.; Vigers, M.; Goring, A.K.; Eschmann, N.A.; Han, S. Heparin-induced tau filaments are structurally heterogeneous and differ from Alzheimer’s disease filaments. Chem. Commun., 2018, 54(36), 4573-4576.
[http://dx.doi.org/10.1039/C8CC01355A] [PMID: 29664486]
[55]
Lira-De León, K.I.; García-Gutiérrez, P.; Serratos, I.N.; Palomera-Cárdenas, M.; Figueroa-Corona, M.P.; Campos-Peña, V.; Meraz-Ríos, M.A. Molecular mechanism of tau aggregation induced by anionic and cationic dyes. J. Alzheimers Dis., 2013, 35(2), 319-334.
[http://dx.doi.org/10.3233/JAD-121765] [PMID: 23435411]
[56]
Chen, H. Recent advances in azo dye degrading enzyme research. Curr. Protein Pept. Sci., 2006, 7(2), 101-111.
[http://dx.doi.org/10.2174/138920306776359786] [PMID: 16611136]
[57]
Lee, T.H.; Pastorino, L.; Lu, K.P. Peptidyl-prolyl cis-trans isomerase Pin1 in ageing, cancer and Alzheimer disease. Expert Rev. Mol. Med., 2011, 13, e21.
[http://dx.doi.org/10.1017/S1462399411001906] [PMID: 21682951]
[58]
Hamelberg, D; McCammon, JA Mechanistic insight into the role of transition-state stabilization in cyclophilin A. J. Am. Chem. Soc., 2009, 131(1), 147-152.
[59]
Cho, K-i; Patil, H; Senda, E; Wang, J; Yi, H Qiu, S Differential loss of prolyl isomerase or chaperone activity of Ran-binding protein 2 (Ranbp2) unveils distinct physiological roles of its cyclophilin domain in proteostasis. J. Biol. Chem., 2014, 289(8), 4600-4625.
[60]
Banerjee, S.; Maity, S.; Chakraborti, A.S. Methylglyoxal-induced modification causes aggregation of myoglobin. Spectrochim. Acta A Mol. Biomol. Spectrosc., 2016, 155, 1-10.
[http://dx.doi.org/10.1016/j.saa.2015.10.022] [PMID: 26554310]
[61]
Morris, K.L.; Serpell, L.C. X-ray fibre diffraction studies of amyloid fibrils. Amyloid Proteins; Springer, 2012, pp. 121-135.
[62]
Naeem, A.; Amani, S. Deciphering structural intermediates and genotoxic fibrillar aggregates of albumins: A molecular mechanism underlying for degenerative diseases. PLoS One, 2013, 8(1), e54061.
[http://dx.doi.org/10.1371/journal.pone.0054061] [PMID: 23342075]
[63]
Makin, O.S.; Serpell, L.C. X-ray diffraction studies of amyloid structure. Amyloid Proteins; Springer, 2005, pp. 67-80.
[64]
Bijari, N.; Ghobadi, S.; Mahdiuni, H.; Khodarahmi, R.; Ghadami, S.A. Spectroscopic and molecular modeling studies on binding of dorzolamide to bovine and human carbonic anhydrase II. Int. J. Biol. Macromol., 2015, 80, 189-199.
[http://dx.doi.org/10.1016/j.ijbiomac.2015.06.028] [PMID: 26093313]
[65]
Jeganathan, S.; von Bergen, M.; Mandelkow, E.M.; Mandelkow, E. The natively unfolded character of tau and its aggregation to Alzheimer-like paired helical filaments. Biochemistry, 2008, 47(40), 10526-10539.
[http://dx.doi.org/10.1021/bi800783d] [PMID: 18783251]
[66]
Khodarahmi, R.; Soori, H.; Amani, M. Study of cosolvent-induced α-chymotrypsin fibrillogenesis: Does protein surface hydrophobicity trigger early stages of aggregation reaction? Protein J., 2009, 28(7-8), 349-361.
[http://dx.doi.org/10.1007/s10930-009-9200-5] [PMID: 19768527]
[67]
Osváth, S.; Gruebele, M. Proline can have opposite effects on fast and slow protein folding phases. Biophys. J., 2003, 85(2), 1215-1222.
[http://dx.doi.org/10.1016/S0006-3495(03)74557-3] [PMID: 12885665]
[68]
Schindler, T.; Mayr, L.M.; Landt, O.; Hahn, U.; Schmid, F.X. The role of a trans-proline in the folding mechanism of ribonuclease T1. Eur. J. Biochem., 1996, 241(2), 516-524.
[http://dx.doi.org/10.1111/j.1432-1033.1996.00516.x] [PMID: 8917450]
[69]
Herning, T.; Yutani, K.; Taniyama, Y.; Kikuchi, M. Effects of proline mutations on the unfolding and refolding of human lysozyme: the slow refolding kinetic phase does not result from proline cis-trans isomerization. Biochemistry, 1991, 30(41), 9882-9891.
[http://dx.doi.org/10.1021/bi00105a011] [PMID: 1911779]
[70]
Taler-Verčič, A.; Hasanbašić, S.; Berbić, S.; Stoka, V.; Turk, D.; Žerovnik, E. Proline residues as switches in conformational changes leading to amyloid fibril formation. Int. J. Mol. Sci., 2017, 18(3), 549.
[http://dx.doi.org/10.3390/ijms18030549] [PMID: 28272335]
[71]
Park, MH; Jin, HK Potential therapeutic target for aging and age-related neurodegenerative diseases: the role of acid sphingomyelinase. Exp. Mol. Med., 2020, 52(3), 380-389.
[72]
Idris, M; Idris, M; Adeola, F Mensah Sedzro, DJIJBBMB Cyclophilins: The structure and functions of an important peptidyl-prolyl isomerase. Int. J. Biochem. Mol. Biol., 2019, 4(1), 1.
[73]
Colgan, J; Asmal, M; Neagu, M; Yu, B; Schneidkraut, J; Lee, Y; Sokolskaja, E; Andreotti, A; Luban, J Cyclophilin A regulates TCR signal strength in CD4+ T cells via a proline-directed conformational switch in Itk. Immunity., 2004, 21(2), 189-201.
[74]
Brazin, KN; Mallis, RJ; Fulton, DB; Andreotti, AHJ Regulation of the tyrosine kinase Itk by the peptidyl-prolyl isomerase cyclophilin A. Proc. Natl. Acad. Sci. U S A, 2002, 99(4), 1899-1904.
[75]
Kim, N; Wang, B; Koikawa, K; Nezu, Y; Qiu, C; Lee, TH Inhibition of death-associated protein kinase 1 attenuates cis P-tau and neurodegeneration in traumatic brain injury. Prog. Neurobiol., 2021, 203, 102072.
[http://dx.doi.org/10.1016/j.pneurobio.2021.102072]
[76]
Vasudevan, D; Gopalan, G; Kumar, A; Garcia, VJ; Luan, S Swaminathan, KJ Plant immunophilins: A review of their structure function relationship. Biochim. Biophys. Acta., 2015, 1850(10), 2145-2158.
[77]
Favretto, F; Flores, D; Baker, JD; Strohäker, T; Andreas, LB; Blair, LJ; Becker, S; Zweckstetter, M Catalysis of proline isomerization and molecular chaperone activity in a tug-of-war. Nat. Commun., 2020, 11(1), 6046.
[http://dx.doi.org/10.1038/s41467-020-19844-0]
[78]
Saphire, AC; Bobardt, MD Gallay, PA Host cyclophilin A mediates HIV-1 attachment to target cells via heparans. EMBO J., 1999, 18(23), 6771-6785.
[http://dx.doi.org/10.1093/emboj/18.23.6771]
[79]
Baker, J.D.; Shelton, L.B.; Zheng, D.; Favretto, F.; Nordhues, B.A.; Darling, A.; Sullivan, L.E.; Sun, Z.; Solanki, P.K.; Martin, M.D.; Suntharalingam, A.; Sabbagh, J.J.; Becker, S.; Mandelkow, E.; Uversky, V.N.; Zweckstetter, M.; Dickey, C.A.; Koren, J.; Blair, L.J. Human cyclophilin 40 unravels neurotoxic amyloids. PLoS Biol., 2017, 15(6), e2001336.
[http://dx.doi.org/10.1371/journal.pbio.2001336]
[80]
Grass, GD Toole, BPJBR How, with whom and when: An overview of CD147-mediated regulatory networks influencing matrix metalloproteinase activity. Biosci. Rep., 2015, 36(1), e00283.
[http://dx.doi.org/10.1042/BSR20150256]
[81]
Yurchenko, V; Zybarth, G; O’Connor, M; Dai, WW; Franchin, G; Hao, T Active site residues of cyclophilin A are crucial for its signaling activity via CD147. J. Biol. Chem., 2002, 277(25), 22959-22965.
[http://dx.doi.org/10.1074/jbc.M201593200]
[82]
Pushkarsky, T; Yurchenko, V; Vanpouille, C; Brichacek, B; Vaisman, I; Hatakeyama, S; Nakayama, KI; Sherry, B; Bukrinsky, MI I Cell surface expression of CD147/EMMPRIN is regulated by cyclophilin 60. J. Biol. Chem., 2005, 280(30), 27866-27871.
[83]
Hosoki, K; Boldogh, I; Sur, S Innate responses to pollen allergens. Curr. Opin. Allergy Clin. Immunol., 2015, 15(1), 79-88.
[84]
Noirey, N; Rougier, N; André, C; Schmitt, D; Vincent, C Langerhans-like dendritic cells generated from cord blood progenitors internalize pollen allergens by macropinocytosis, and part of the molecules are processed and can activate autologous naive T lymphocytes. J. Allergy Clin. Immunol., 2000, 105(6 Pt 1), 1194-1201.

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy