Role of PIN1 in human pathology: Cellular regulation, pathogenesis and therapeutic implications (Review)
- Authors:
- Julian Maggio
- Romina Gabriela Armando
- Lara Balcone
- Román Nicolás Vilarullo
- Maria Del Pilar Casco
- Diego Luis Mengual Gomez
- Daniel Eduardo Gomez
-
Affiliations: Molecular Oncology Unit, Center of Molecular and Translational Oncology, Quilmes National University, Bernal B1876BXD, Argentina - Published online on: December 21, 2023 https://doi.org/10.3892/wasj.2023.220
- Article Number: 5
-
Copyright : © Maggio et al. This is an open access article distributed under the terms of Creative Commons Attribution License [CC BY 4.0].
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|
Liou YC, Zhou XZ and Lu KP: Prolyl isomerase Pin1 as a molecular switch to determine the fate of phosphoproteins. Trends Biochem Sci. 36:501–514. 2011.PubMed/NCBI View Article : Google Scholar | |
|
Alvarez E, Northwood IC, Gonzalez FA, Latour DA, Seth A, Abate C, Curran T and Davis RJ: Pro-Leu-Ser/Thr-Pro is a consensus primary sequence for substrate protein phosphorylation. Characterization of the phosphorylation of c-myc and c-jun proteins by an epidermal growth factor receptor threonine 669 protein kinase. J Biol Chem. 266:15277–15285. 1991.PubMed/NCBI | |
|
Gurung D, Danielson JA, Tasnim A, Zhang JT, Zou Y and Liu JY: Proline Isomerization: From the chemistry and biology to therapeutic opportunities. Biology (Basel). 12(1008)2023.PubMed/NCBI View Article : Google Scholar | |
|
Lu KP, Hanes SD and Hunter T: A human peptidyl-prolyl isomerase essential for regulation of mitosis. Nature. 380:544–547. 1996.PubMed/NCBI View Article : Google Scholar | |
|
El Boustani M, De Stefano L, Caligiuri I, Mouawad N, Granchi C, Canzonieri V, Tuccinardi T, Giordano A and Rizzolio F: A Guide to PIN1 function and mutations across cancers. Front Pharmacol. 9(1477)2018.PubMed/NCBI View Article : Google Scholar | |
|
Rustighi A, Tiberi L, Soldano A, Napoli M, Nuciforo P, Rosato A, Kaplan F, Capobianco A, Pece S, Di Fiore PP and Del Sal G: The prolyl-isomerase Pin1 is a Notch1 target that enhances Notch1 activation in cancer. Nat Cell Biol. 11:133–142. 2009.PubMed/NCBI View Article : Google Scholar | |
|
Ryo A, Liou YC, Wulf G, Nakamura M, Lee SW and Lu KP: PIN1 is an E2F target gene essential for Neu/Ras-induced transformation of mammary epithelial cells. Mol Cell Biol. 22:5281–5295. 2002.PubMed/NCBI View Article : Google Scholar | |
|
MacLachlan TK, Somasundaram K, Sgagias M, Shifman Y, Muschel RJ, Cowan KH and El-Deiry WS: BRCA1 effects on the cell cycle and the DNA damage response are linked to altered gene expression. J Biol Chem. 275:2777–2785. 2000.PubMed/NCBI View Article : Google Scholar | |
|
Luo ML, Gong C, Chen CH, Lee DY, Hu H, Huang P, Yao Y, Guo W, Reinhardt F, Wulf G, et al: Prolyl isomerase Pin1 acts downstream of miR200c to promote cancer stem-like cell traits in breast cancer. Cancer Res. 74:3603–3616. 2014.PubMed/NCBI View Article : Google Scholar | |
|
Eckerdt F, Yuan J, Saxena K, Martin B, Kappel S, Lindenau C, Kramer A, Naumann S, Daum S, Fischer G, et al: Polo-like kinase 1-mediated phosphorylation stabilizes Pin1 by inhibiting its ubiquitination in human cells. J Biol Chem. 280:36575–36583. 2005.PubMed/NCBI View Article : Google Scholar | |
|
Chen CH, Chang CC, Lee TH, Luo M, Huang P, Liao PH, Wei S, Li FA, Chen RH, Zhou XZ, et al: SENP1 deSUMOylates and regulates Pin1 protein activity and cellular function. Cancer Res. 73:3951–3962. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Hamdane M, Dourlen P, Bretteville A, Sambo AV, Ferreira S, Ando K, Kerdraon O, Bégard S, Geay L, Lippens G, et al: Pin1 allows for differential Tau dephosphorylation in neuronal cells. Mol Cell Neurosci. 32:155–160. 2006.PubMed/NCBI View Article : Google Scholar | |
|
Liou YC, Sun A, Ryo A, Zhou XZ, Yu ZX, Huang HK, Uchida T, Bronson R, Bing G, Li X, et al: Role of the prolyl isomerase Pin1 in protecting against age-dependent neurodegeneration. Nature. 424:556–561. 2003.PubMed/NCBI View Article : Google Scholar | |
|
Fahed G, Aoun L, Bou Zerdan M, Allam S, Bou Zerdan M, Bouferraa Y and Assi HI: Metabolic Syndrome: Updates on pathophysiology and management in 2021. Int J Mol Sci. 23(786)2022.PubMed/NCBI View Article : Google Scholar | |
|
Saltiel AR: Insulin signaling in health and disease. J Clin Invest. 131(e142241)2021.PubMed/NCBI View Article : Google Scholar | |
|
Nakatsu Y, Mori K, Matsunaga Y, Yamamotoya T, Ueda K, Inoue Y, Mitsuzaki-Miyoshi K, Sakoda H, Fujishiro M, Yamaguchi S, et al: The prolyl isomerase Pin1 increases β-cell proliferation and enhances insulin secretion. J Biol Chem. 292:11886–11895. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Inoue MK, Nakatsu Y, Yamamotoya T, Hasei S, Kanamoto M, Naitou M, Matsunaga Y, Sakoda H, Fujishiro M, Ono H, et al: Pin1 plays essential roles in NASH development by modulating multiple target proteins. Cells. 8(1545)2019.PubMed/NCBI View Article : Google Scholar | |
|
Han Y, Lee SH, Bahn M, Yeo CY and Lee KY: Pin1 enhances adipocyte differentiation by positively regulating the transcriptional activity of PPARγ. Mol Cell Endocrinol. 436:150–158. 2016.PubMed/NCBI View Article : Google Scholar | |
|
Nakatsu Y and Asano T: Prolyl isomerase Pin1 impacts on metabolism in muscle and adipocytes. Yakugaku Zasshi. 142:449–456. 2022.PubMed/NCBI View Article : Google Scholar : (In Japanese). | |
|
Kanna M, Nakatsu Y, Yamamotoya T, Kushiyama A, Fujishiro M, Sakoda H, Ono H, Arihiro K and Asano T: Hepatic Pin1 expression, particularly in nuclei, is increased in NASH patients in accordance with evidence of the role of Pin1 in lipid accumulation shown in hepatoma cell lines. Int J Mol Sci. 24(8847)2023.PubMed/NCBI View Article : Google Scholar | |
|
Azeez TA: Osteoporosis and cardiovascular disease: A review. Mol Biol Rep. 50:1753–1763. 2023.PubMed/NCBI View Article : Google Scholar | |
|
Xu J, Yu L, Liu F, Wan L and Deng Z: The effect of cytokines on osteoblasts and osteoclasts in bone remodeling in osteoporosis: A review. Front Immunol. 14(1222129)2023.PubMed/NCBI View Article : Google Scholar | |
|
Islam R, Yoon WJ and Ryoo HM: Pin1, the master orchestrator of bone cell differentiation. J Cell Physiol. 232:2339–2347. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Park KR, Kim S, Cho M, Kang SW and Yun HM: Effects of PIN on osteoblast differentiation and matrix mineralization through runt-related transcription factor. Int J Mol Sci. 21(9579)2020.PubMed/NCBI View Article : Google Scholar | |
|
Kurakula K, Hagdorn QAJ, van der Feen DE, Vonk Noordegraaf A, Ten Dijke P, de Boer RA, Bogaard HJ, Goumans MJ and Berger RMF: Inhibition of the prolyl isomerase Pin1 improves endothelial function and attenuates vascular remodelling in pulmonary hypertension by inhibiting TGF-β signalling. Angiogenesis. 25:99–112. 2022.PubMed/NCBI View Article : Google Scholar | |
|
Shin HR, Bae HS, Kim BS, Yoon HI, Cho YD, Kim WJ, Choi KY, Lee YS, Woo KM, Baek JH and Ryoo HM: PIN1 is a new therapeutic target of craniosynostosis. Hum Mol Genet. 27:3827–3839. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Lee SH, Jeong HM, Han Y, Cheong H, Kang BY and Lee KY: Prolyl isomerase Pin1 regulates the osteogenic activity of Osterix. Mol Cell Endocrinol. 400:32–40. 2015.PubMed/NCBI View Article : Google Scholar | |
|
Cho E, Lee JK, Lee JY, Chen Z, Ahn SH, Kim ND, Kook MS, Min SH, Park BJ and Lee TH: BCPA {N, N'-1,4-Butanediylbis[3-(2-chlorophenyl)acrylamide]} Inhibits Osteoclast Differentiation through Increased Retention of Peptidyl-Prolyl cis-trans Isomerase Never in Mitosis A-Interacting 1. Int J Mol Sci. 19(3436)2018.PubMed/NCBI View Article : Google Scholar | |
|
Gao Y, Chen N, Fu Z and Zhang Q: Progress of wnt signaling pathway in osteoporosis. Biomolecules. 13(483)2023.PubMed/NCBI View Article : Google Scholar | |
|
Li S, Cui Y, Li M, Zhang W, Sun X, Xin Z and Li J: Acteoside derived from cistanche improves glucocorticoid-induced osteoporosis by activating PI3K/AKT/mTOR pathway. J Invest Surg. 36(2154578)2023.PubMed/NCBI View Article : Google Scholar | |
|
Zhao P, Xiao L, Peng J, Qian YQ and Huang CC: Exosomes derived from bone marrow mesenchymal stem cells improve osteoporosis through promoting osteoblast proliferation via MAPK pathway. Eur Rev Med Pharmacol Sci. 22:3962–3970. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Yoshida G, Kawabata T, Takamatsu H, Saita S, Nakamura S, Nishikawa K, Fujiwara M, Enokidani Y, Yamamuro T, Tabata K, et al: Degradation of the NOTCH intracellular domain by elevated autophagy in osteoblasts promotes osteoblast differentiation and alleviates osteoporosis. Autophagy. 18:2323–2332. 2022.PubMed/NCBI View Article : Google Scholar | |
|
Vazgiourakis VM, Zervou MI, Papageorgiou L, Chaniotis D, Spandidos DA, Vlachakis D, Eliopoulos E and Goulielmos GN: Association of endometriosis with cardiovascular disease: Genetic aspects (Review). Int J Mol Med. 51(29)2023.PubMed/NCBI View Article : Google Scholar | |
|
Sarmah N, Nauli AM, Ally A and Nauli SM: Interactions among endothelial nitric oxide synthase, cardiovascular system, and nociception during physiological and pathophysiological states. Molecules. 27(2835)2022.PubMed/NCBI View Article : Google Scholar | |
|
Fagiani F, Vlachou M, Di Marino D, Canobbio I, Romagnoli A, Racchi M, Govoni S and Lanni C: Pin1 as molecular switch in vascular endothelium: Notes on its putative role in age-associated vascular diseases. Cells. 10(3287)2021.PubMed/NCBI View Article : Google Scholar | |
|
Kennard S, Ruan L, Buffett RJ, Fulton D and Venema RC: TNFα reduces eNOS activity in endothelial cells through serine 116 phosphorylation and Pin1 binding: Confirmation of a direct, inhibitory interaction of Pin1 with eNOS. Vascul Pharmacol. 81:61–68. 2016.PubMed/NCBI View Article : Google Scholar | |
|
Liu M, Yu P, Jiang H, Yang X, Zhao J, Zou Y and Ge J: TThe essential role of Pin1 via NF-κB signaling in vascular inflammation and atherosclerosis in ApoE-/-Mice. Int J Mol Sci. 18(644)2017.PubMed/NCBI View Article : Google Scholar | |
|
Liang G, Wang S, Shao J, Jin YJ, Xu L, Yan Y, Günther S, Wang L and Offermanns S: Tenascin-X mediates Flow-induced suppression of EndMT and atherosclerosis. Circ Res. 130:1647–1659. 2022.PubMed/NCBI View Article : Google Scholar | |
|
Huminiecki L, Goldovsky L, Freilich S, Moustakas A, Ouzounis C and Heldin CH: Emergence, development and diversification of the TGF-beta signalling pathway within the animal kingdom. BMC Evol Biol. 9(28)2009.PubMed/NCBI View Article : Google Scholar | |
|
Gentile C, Muise-Helmericks RC and Drake CJ: VEGF-mediated phosphorylation of eNOS regulates angioblast and embryonic endothelial cell proliferation. Dev Biol. 373:163–175. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Rai N, Sydykov A, Kojonazarov B, Wilhelm J, Manaud G, Veeroju S, Ruppert C, Perros F, Ghofrani HA, Weissmann N, et al: Targeting peptidyl-prolyl isomerase 1 in experimental pulmonary arterial hypertension. Eur Respir J. 60(2101698)2022.PubMed/NCBI View Article : Google Scholar | |
|
Kim MR, Choi HS, Heo TH, Hwang SW and Kang KW: Induction of vascular endothelial growth factor by peptidyl-prolyl isomerase Pin1 in breast cancer cells. Biochem Biophys Res Commun. 369:547–553. 2008.PubMed/NCBI View Article : Google Scholar | |
|
Toko H, Konstandin MH, Doroudgar S, Ormachea L, Joyo E, Joyo AY, Din S, Gude NA, Collins B, Völkers M, et al: Regulation of cardiac hypertrophic signaling by prolyl isomerase Pin1. Circ Res. 112:1244–1252. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Chen Y, Wu YR, Yang HY, Li XZ, Jie MM, Hu CJ, Wu YY, Yang SM and Yang YB: Prolyl isomerase Pin1: A promoter of cancer and a target for therapy. Cell Death Dis. 9(883)2018.PubMed/NCBI View Article : Google Scholar | |
|
Hanahan D and Weinberg RA: Hallmarks of cancer: The next generation. Cell. 144:646–674. 2011.PubMed/NCBI View Article : Google Scholar | |
|
Chuang HH, Zhen YY, Tsai YC, Chuang CH, Huang MS, Hsiao M and Yang CJ: Targeting Pin1 for modulation of cell motility and cancer therapy. Biomedicines. 9(359)2021.PubMed/NCBI View Article : Google Scholar | |
|
Hanahan D: Hallmarks of cancer: New dimensions. Cancer Discov. 12:31–46. 2022.PubMed/NCBI View Article : Google Scholar | |
|
Wu W, Xue X, Chen Y, Zheng N and Wang J: Targeting prolyl isomerase Pin1 as a promising strategy to overcome resistance to cancer therapies. Pharmacol Res. 184(106456)2022.PubMed/NCBI View Article : Google Scholar | |
|
Cohn GM, Liefwalker DF, Langer EM and Sears RC: PIN1 provides dynamic control of MYC in response to extrinsic signals. Front Cell Dev Biol. 8(224)2020.PubMed/NCBI View Article : Google Scholar | |
|
Nashaat S, Henen MA, El-Messery SM and Eisa H: New benzimidazoles targeting breast cancer: Synthesis, Pin1 inhibition, 2D NMR binding, and computational studies. Molecules. 27(5245)2022.PubMed/NCBI View Article : Google Scholar | |
|
Ueda K, Nakatsu Y, Yamamotoya T, Ono H, Inoue Y, Inoue MK, Mizuno Y, Matsunaga Y, Kushiyama A, Sakoda H, et al: Prolyl isomerase Pin1 binds to and stabilizes acetyl CoA carboxylase 1 protein, thereby supporting cancer cell proliferation. Oncotarget. 10:1637–1648. 2019.PubMed/NCBI View Article : Google Scholar | |
|
Tan X, Zhou F, Wan J, Hang J, Chen Z, Li B, Zhang C, Shao K, Jiang P, Shi S, et al: Pin1 expression contributes to lung cancer: Prognosis and carcinogenesis. Cancer Biol Ther. 9:111–119. 2010.PubMed/NCBI View Article : Google Scholar | |
|
Kim G, Bhattarai PY and Choi HS: Peptidyl-prolyl cis/trans isomerase NIMA-interacting 1 as a molecular target in breast cancer: A therapeutic perspective of gynecological cancer. Arch Pharm Res. 42:128–139. 2019.PubMed/NCBI View Article : Google Scholar | |
|
Chen Y, Wu Y, Yu S, Yang H, Wang X, Zhang Y, Zhu S, Jie M, Liu C, Li X, et al: Deficiency of microRNA-628-5p promotes the progression of gastric cancer by upregulating PIN1. Cell Death Dis. 11(559)2020.PubMed/NCBI View Article : Google Scholar | |
|
Chen M, Xia Y, Tan Y, Jiang G, Jin H and Chen Y: Downregulation of microRNA-370 in esophageal squamous-cell carcinoma is associated with cancer progression and promotes cancer cell proliferation via upregulating PIN1. Gene. 661:68–77. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Kuramochi J, Arai T, Ikeda S, Kumagai J, Uetake H and Sugihara K: High Pin1 expression is associated with tumor progression in colorectal cancer. J Surg Oncol. 94:155–160. 2006.PubMed/NCBI View Article : Google Scholar | |
|
Wang T, Liu Z, Shi F and Wang J: Pin1 modulates chemo-resistance by up-regulating FoxM1 and the involvements of Wnt/β-catenin signaling pathway in cervical cancer. Mol Cell Biochem. 413:179–187. 2016.PubMed/NCBI View Article : Google Scholar | |
|
Kim G, Bhattarai PY, Lim SC, Kim JY and Choi HS: PIN1 facilitates ubiquitin-mediated degradation of serine/threonine kinase 3 and promotes melanoma development via TAZ activation. Cancer Lett. 499:164–174. 2021.PubMed/NCBI View Article : Google Scholar | |
|
Maggio J, Cardama GA, Armando RG, Balcone L, Sobol NT, Gomez DE and Mengual Gómez DL: Key role of PIN1 in telomere maintenance and oncogenic behavior in a human glioblastoma model. Oncol Rep. 49(91)2023.PubMed/NCBI View Article : Google Scholar | |
|
Li Q, Dong Z, Lin Y, Jia X, Li Q, Jiang H, Wang L and Gao Y: The rs2233678 polymorphism in PIN1 promoter region reduced cancer risk: A meta-analysis. PLoS One. 8(e68148)2013.PubMed/NCBI View Article : Google Scholar | |
|
Wulf G, Garg P, Liou YC, Iglehart D and Lu KP: Modeling breast cancer in vivo and ex vivo reveals an essential role of Pin1 in tumorigenesis. EMBO J. 23:3397–3407. 2004.PubMed/NCBI View Article : Google Scholar | |
|
Takahashi K, Akiyama H, Shimazaki K, Uchida C, Akiyama-Okunuki H, Tomita M, Fukumoto M and Uchida T: Ablation of a peptidyl prolyl isomerase Pin1 from p53-null mice accelerated thymic hyperplasia by increasing the level of the intracellular form of Notch1. Oncogene. 26:3835–3845. 2007.PubMed/NCBI View Article : Google Scholar | |
|
Girardini JE, Napoli M, Piazza S, Rustighi A, Marotta C, Radaelli E, Capaci V, Jordan L, Quinlan P, Thompson A, et al: A Pin1/mutant p53 axis promotes aggressiveness in breast cancer. Cancer Cell. 20:79–91. 2011.PubMed/NCBI View Article : Google Scholar | |
|
Zucchi D, Silvagni E, Elefante E, Signorini V, Cardelli C, Trentin F, Schilirò D, Cascarano G, Valevich A, Bortoluzzi A and Tani C: Systemic lupus erythematosus: One year in review 2023. Clin Exp Rheumatol. 41:997–1008. 2023.PubMed/NCBI View Article : Google Scholar | |
|
Baek WY, Choi YS, Lee SW, Son IO, Jeon KW, Choi SD and Suh CH: Toll-like receptor signaling inhibitory peptide improves inflammation in animal model and human systemic lupus erythematosus. Int J Mol Sci. 22(12764)2021.PubMed/NCBI View Article : Google Scholar | |
|
Khoryati L, Augusto JF, Shipley E, Contin-Bordes C, Douchet I, Mitrovic S, Truchetet ME, Lazaro E, Duffau P, Couzi L, et al: IgE inhibits Toll-like receptor 7- and Toll-like receptor 9-mediated expression of interferon-α by plasmacytoid dendritic cells in patients with systemic lupus erythematosus. Arthritis Rheumatol. 68:2221–2231. 2016.PubMed/NCBI View Article : Google Scholar | |
|
Salloum R and Niewold TB: Interferon regulatory factors in human lupus pathogenesis. Transl Res. 157:326–331. 2011.PubMed/NCBI View Article : Google Scholar | |
|
Tun-Kyi A, Finn G, Greenwood A, Nowak M, Lee TH, Asara JM, Tsokos GC, Fitzgerald K, Israel E, Li X, et al: Essential role for the prolyl isomerase Pin1 in Toll-like receptor signaling and type I interferon-mediated immunity. Nat Immunol. 12:733–741. 2011.PubMed/NCBI View Article : Google Scholar | |
|
Wei S, Yoshida N, Finn G, Kozono S, Nechama M, Kyttaris VC, Zhen Zhou X, Tsokos GC and Ping Lu K: Pin1-Targeted therapy for systemic lupus erythematosus. Arthritis Rheumatol. 68:2503–2513. 2016.PubMed/NCBI View Article : Google Scholar | |
|
Jacob N and Stohl W: Cytokine disturbances in systemic lupus erythematosus. Arthritis Res Ther. 13(228)2011.PubMed/NCBI View Article : Google Scholar | |
|
Ding J, Su S, You T, Xia T, Lin X, Chen Z and Zhang L: Serum interleukin-6 level is correlated with the disease activity of systemic lupus erythematosus: A meta-analysis. Clinics (Sao Paulo). 75(e1801)2020.PubMed/NCBI View Article : Google Scholar | |
|
Tackey E, Lipsky PE and Illei GG: Rationale for interleukin-6 blockade in systemic lupus erythematosus. Lupus. 13:339–343. 2004.PubMed/NCBI View Article : Google Scholar | |
|
Takeno M, Gunn J, Suzuki JT, Kim NP, Kang J, Finn TB, Vazirpour M, Martin W and Leung CJ: A novel role of peptidyl-prolyl isomerase-1 as inducer of IL-6 expression in systemic lupus erythematosus. Am J BioMedicine. 3:439–450. 2015. | |
|
Jang S, Kwon EJ and Lee JJ: Rheumatoid arthritis: Pathogenic roles of diverse immune cells. Int J Mol Sci. 23(905)2022.PubMed/NCBI View Article : Google Scholar | |
|
Nagaoka A, Takizawa N, Takeuchi R, Inaba Y, Saito I, Nagashima Y, Saito T and Aoki I: Possible involvement of peptidylprolyl isomerase Pin1 in rheumatoid arthritis. Pathol Int. 61:59–66. 2011.PubMed/NCBI View Article : Google Scholar | |
|
Makarov SS: NF-kappa B in rheumatoid arthritis: A pivotal regulator of inflammation, hyperplasia, and tissue destruction. Arthritis Res. 3:200–206. 2001.PubMed/NCBI View Article : Google Scholar | |
|
Araki Y and Mimura T: Matrix metalloproteinase gene activation resulting from disordred epigenetic mechanisms in rheumatoid arthritis. Int J Mol Sci. 18(905)2017.PubMed/NCBI View Article : Google Scholar | |
|
Li X and Makarov SS: An essential role of NF-kappaB in the ‘tumor-like’ phenotype of arthritic synoviocytes. Proc Natl Acad Sci USA. 103:17432–17437. 2006.PubMed/NCBI View Article : Google Scholar | |
|
Ma Y, Hong FF and Yang SL: Role of prostaglandins in rheumatoid arthritis. Clin Exp Rheumatol. 39:162–172. 2021.PubMed/NCBI View Article : Google Scholar | |
|
Kondo N, Kuroda T and Kobayashi D: Cytokine networks in the pathogenesis of rheumatoid arthritis. Int J Mol Sci. 22(10922)2021.PubMed/NCBI View Article : Google Scholar | |
|
Jeong HG, Pokharel YR, Lim SC, Hwang YP, Han EH, Yoon JH, Ahn SG, Lee KY and Kang KW: Novel role of Pin1 induction in type II collagen-mediated rheumatoid arthritis. J Immunol. 183:6689–6697. 2009.PubMed/NCBI View Article : Google Scholar | |
|
M'Koma AE: Inflammatory bowel disease: Clinical diagnosis and pharmaceutical management. Med Res Arch. 11(10)2023.PubMed/NCBI View Article : Google Scholar | |
|
Matsunaga Y, Hasei S, Yamamotoya T, Honda H, Kushiyama A, Sakoda H, Fujishiro M, Ono H, Ito H, Okabe T, et al: Pathological role of Pin1 in the development of DSS-Induced colitis. Cells. 10(1230)2021.PubMed/NCBI View Article : Google Scholar | |
|
Shao BZ, Wang SL, Pan P, Yao J, Wu K, Li ZS, Bai Y and Linghu EQ: Targeting NLRP3 inflammasome in inflammatory bowel disease: Putting out the fire of inflammation. Inflammation. 42:1147–1159. 2019.PubMed/NCBI View Article : Google Scholar | |
|
Dong R, Xue Z, Fan G, Zhang N, Wang C, Li G and Da Y: Pin1 promotes NLRP3 inflammasome activation by phosphorylation of p38 MAPK pathway in septic shock. Front Immunol. 12(620238)2021.PubMed/NCBI View Article : Google Scholar | |
|
Dagenais A, Villalba-Guerrero C and Olivier M: Trained immunity: A ‘new’ weapon in the fight against infectious diseases. Front Immunol. 14(1147476)2023.PubMed/NCBI View Article : Google Scholar | |
|
Kanna M, Nakatsu Y, Yamamotoya T, Encinas J, Ito H, Okabe T, Asano T and Sakaguchi T: Roles of peptidyl prolyl isomerase Pin1 in viral propagation. Front Cell Dev Biol. 10(1005325)2022.PubMed/NCBI View Article : Google Scholar | |
|
Stroh LJ and Krey T: Structural insights into hepatitis C virus neutralization. Curr Opin Virol. 60(101316)2023.PubMed/NCBI View Article : Google Scholar | |
|
Lim YS, Tran HT, Park SJ, Yim SA and Hwang SB: Peptidyl-prolyl isomerase Pin1 is a cellular factor required for hepatitis C virus propagation. J Virol. 85:8777–8788. 2011.PubMed/NCBI View Article : Google Scholar | |
|
Jeng WJ, Papatheodoridis GV and Lok ASF: Hepatitis B. Lancet. 401:1039–1052. 2023.PubMed/NCBI View Article : Google Scholar | |
|
Kojima Y and Ryo A: Pinning down viral proteins: A new prototype for virus-host cell interaction. Front Microbiol. 1(107)2010.PubMed/NCBI View Article : Google Scholar | |
|
Pang R, Lee TK, Poon RT, Fan ST, Wong KB, Kwong YL and Tse E: Pin1 interacts with a specific serine-proline motif of hepatitis B virus X-protein to enhance hepatocarcinogenesis. Gastroenterology. 132:1088–1103. 2007.PubMed/NCBI View Article : Google Scholar | |
|
Shang S, Hua F and Hu ZW: The regulation of β-catenin activity and function in cancer: Therapeutic opportunities. Oncotarget. 8:33972–33989. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Ao R, Zhang DR, Du YQ and Wang Y: Expression and significance of Pin1, β-catenin and cyclin D1 in hepatocellular carcinoma. Mol Med Rep. 10:1893–1898. 2014.PubMed/NCBI View Article : Google Scholar | |
|
Nishi M, Miyakawa K, Matsunaga S, Khatun H, Yamaoka Y, Watashi K, Sugiyama M, Kimura H, Wakita T and Ryo A: Prolyl Isomerase Pin1 regulates the stability of hepatitis B virus core protein. Front Cell Dev Biol. 8(26)2020.PubMed/NCBI View Article : Google Scholar | |
|
Kwon H, Kim J, Song C, Sajjad MA, Ha J, Jung J, Park S, Shin HJ and Kim K: Peptidyl-prolyl cis/trans isomerase Pin1 interacts with hepatitis B virus core particle, but not with HBc protein, to promote HBV replication. Front Cell Infect Microbiol. 13(1195063)2023.PubMed/NCBI View Article : Google Scholar | |
|
Womack J and Jimenez M: Common questions about infectious mononucleosis. Am Fam Physician. 91:372–376. 2015.PubMed/NCBI | |
|
Hutcheson RL, Chakravorty A and Sugden B: Burkitt lymphomas evolve to escape dependencies on Epstein-Barr virus. Front Cell Infect Microbiol. 10(606412)2020.PubMed/NCBI View Article : Google Scholar | |
|
Narita Y, Murata T, Ryo A, Kawashima D, Sugimoto A, Kanda T, Kimura H and Tsurumi T: Pin1 interacts with the Epstein-Barr virus DNA polymerase catalytic subunit and regulates viral DNA replication. J Virol. 87:2120–2127. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Chang ET, Ye W, Zeng YX and Adami HO: The evolving epidemiology of nasopharyngeal carcinoma. Cancer Epidemiol Biomarkers Prev. 30:1035–1047. 2021.PubMed/NCBI View Article : Google Scholar | |
|
Xu M, Cheung CC, Chow C, Lun SW, Cheung ST and Lo KW: Overexpression of PIN1 enhances cancer growth and aggressiveness with cyclin D1 induction in EBV-Associated nasopharyngeal carcinoma. PLoS One. 11(e0156833)2016.PubMed/NCBI View Article : Google Scholar | |
|
Yu JH, Im CY and Min SH: Function of PIN1 in cancer development and its inhibitors as cancer therapeutics. Front Cell Dev Biol. 8(120)2020.PubMed/NCBI View Article : Google Scholar | |
|
Letafati A, Soheili R, Norouzi M, Soleimani P and Mozhgani SH: Therapeutic approaches for HTLV-1-associated adult T-cell leukemia/lymphoma: A comprehensive review. Med Oncol. 40(295)2023.PubMed/NCBI View Article : Google Scholar | |
|
Ernzen KJ and Panfil AR: Regulation of HTLV-1 transformation. Biosci Rep. 42(BSR20211921)2022.PubMed/NCBI View Article : Google Scholar | |
|
Peloponese JM Jr, Yasunaga J, Kinjo T, Watashi K and Jeang KT: Peptidylproline cis-trans-isomerase Pin1 interacts with human T-cell leukemia virus type 1 tax and modulates its activation of NF-kappaB. J Virol. 83:3238–3248. 2009.PubMed/NCBI View Article : Google Scholar | |
|
Jeong SJ, Ryo A and Yamamoto N: The prolyl isomerase Pin1 stabilizes the human T-cell leukemia virus type 1 (HTLV-1) Tax oncoprotein and promotes malignant transformation. Biochem Biophys Res Commun. 381:294–299. 2009.PubMed/NCBI View Article : Google Scholar | |
|
Mesnard JM, Barbeau B, Cesaire R and Peloponese JM: Roles of HTLV-1 basic zip factor (HBZ) in viral chronicity and leukemic transformation. Potential new therapeutic approaches to prevent and treat HTLV-1-related diseases. Viruses. 7:6490–6505. 2015.PubMed/NCBI View Article : Google Scholar | |
|
Szymonowicz KA and Chen J: Biological and clinical aspects of HPV-related cancers. Cancer Biol Med. 17:864–878. 2020.PubMed/NCBI View Article : Google Scholar | |
|
Fowler JR, Maani EV, Dunton CJ and Jack BW: Cervical Cancer. In: StatPearls. Treasure Island (FL) ineligible companies. Disclosure: Elizabeth Maani declares no relevant financial relationships with ineligible companies. Disclosure: Charles Dunton declares no relevant financial relationships with ineligible companies. Disclosure: Brian Jack declares no relevant financial relationships with ineligible companies, 2023. | |
|
McBride AA: The papillomavirus E2 proteins. Virology. 445:57–79. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Hareza DA, Wilczynski JR and Paradowska E: Human papillomaviruses as infectious agents in gynecological cancers. Oncogenic properties of viral proteins. Int J Mol Sci. 23(1818)2022.PubMed/NCBI View Article : Google Scholar | |
|
Prabhavathy D, Vijayalakshmi R, Kanchana MP and Karunagaran D: HHPV16 E2 enhances the expression of NF-κB and STAT3 target genes and potentiates NF-κB activation by inflammatory mediators. Cell Immunol. 292:70–77. 2014.PubMed/NCBI View Article : Google Scholar | |
|
Masenga SK, Mweene BC, Luwaya E, Muchaili L, Chona M and Kirabo A: HIV-Host Cell Interactions. Cells. 12(1351)2023.PubMed/NCBI View Article : Google Scholar | |
|
Sarkar S, Balakrishnan K, Chintala K, Chintala K, Mohareer K, Luedde T, Vasudevan AAJ, Münk C and Banerjee S: Tough Way In, Tough Way Out: The complex interplay of host and viral factors in nucleocytoplasmic trafficking during HIV-1 infection. Viruses. 14(2503)2022.PubMed/NCBI View Article : Google Scholar | |
|
Watashi K, Khan M, Yedavalli VR, Yeung ML, Strebel K and Jeang KT: Human immunodeficiency virus type 1 replication and regulation of APOBEC3G by peptidyl prolyl isomerase Pin1. J Virol. 82:9928–9936. 2008.PubMed/NCBI View Article : Google Scholar | |
|
Saleh S, Lu HK, Evans V, Harisson D, Zhou J, Jaworowski A, Sallmann G, Cheong KY, Mota TM, Tennakoon S, et al: HIV integration and the establishment of latency in CCL19-treated resting CD4(+) T cells require activation of NF-κB. Retrovirology. 13(49)2016.PubMed/NCBI View Article : Google Scholar | |
|
Dochi T, Nakano T, Inoue M, Takamune N, Shoji S, Sano K and Misumi S: Phosphorylation of human immunodeficiency virus type 1 capsid protein at serine 16, required for peptidyl-prolyl isomerase-dependent uncoating, is mediated by virion-incorporated extracellular signal-regulated kinase 2. J Gen Virol. 95:1156–1166. 2014.PubMed/NCBI View Article : Google Scholar | |
|
Rossi E, Meuser ME, Cunanan CJ and Cocklin S: Structure, function, and interactions of the HIV-1 Capsid Protein. Life (Basel). 11(100)2021.PubMed/NCBI View Article : Google Scholar | |
|
Bao Q and Zhou J: Various strategies for developing APOBEC3G protectors to circumvent human immunodeficiency virus type 1. Eur J Med Chem. 250(115188)2023.PubMed/NCBI View Article : Google Scholar | |
|
Hu B, Guo H, Zhou P and Shi ZL: Characteristics of SARS-CoV-2 and COVID-19. Nat Rev Microbiol. 19:141–154. 2021.PubMed/NCBI View Article : Google Scholar | |
|
Yamamotoya T, Nakatsu Y, Kanna M, Hasei S, Ohata Y, Encinas J, Ito H, Okabe T, Asano T and Sakaguchi T: Prolyl isomerase Pin1 plays an essential role in SARS-CoV-2 proliferation, indicating its possibility as a novel therapeutic target. Sci Rep. 11(18581)2021.PubMed/NCBI View Article : Google Scholar | |
|
Ino Y, Nishi M, Yamaoka Y, Miyakawa K, Jeremiah SS, Osada M, Kimura Y and Ryo A: Phosphopeptide enrichment using Phos-tag technology reveals functional phosphorylation of the nucleocapsid protein of SARS-CoV-2. J Proteomics. 255(104501)2022.PubMed/NCBI View Article : Google Scholar | |
|
Ye H, Robak LA, Yu M, Cykowski M and Shulman JM: Genetics and pathogenesis of Parkinson's syndrome. Annu Rev Pathol. 18:95–121. 2023.PubMed/NCBI View Article : Google Scholar | |
|
Hallacli E, Kayatekin C, Nazeen S, Wang XH, Sheinkopf Z, Sathyakumar S, Sarkar S, Jiang X, Dong X, Di Maio R, et al: The Parkinson's disease protein alpha-synuclein is a modulator of processing bodies and mRNA stability. Cell. 185:2035–2056 e2033. 2022.PubMed/NCBI View Article : Google Scholar | |
|
Gao V, Briano JA, Komer LE and Burre J: Functional and Pathological Effects of α-Synuclein on Synaptic SNARE Complexes. J Mol Biol. 435(167714)2023.PubMed/NCBI View Article : Google Scholar | |
|
Carvajal-Oliveros A, Dominguez-Baleon C, Sanchez-Diaz I, Zambrano-Tipan D, Hernández-Vargas R, Campusano JM, Narváez-Padilla V and Reynaud E: Parkinsonian phenotypes induced by Synphilin-1 expression are differentially contributed by serotonergic and dopaminergic circuits and suppressed by nicotine treatment. PLoS One. 18(e0282348)2023.PubMed/NCBI View Article : Google Scholar | |
|
Ghosh A, Saminathan H, Kanthasamy A, Anantharam V, Jin H, Sondarva G, Harischandra DS, Qian Z, Rana A and Kanthasamy AG: The peptidyl-prolyl isomerase Pin1 up-regulation and proapoptotic function in dopaminergic neurons: Relevance to the pathogenesis of Parkinson disease. J Biol Chem. 288:21955–21971. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Ryo A, Togo T, Nakai T, Hirai A, Nishi M, Yamaguchi A, Suzuki K, Hirayasu Y, Kobayashi H, Perrem K, et al: Prolyl-isomerase Pin1 accumulates in lewy bodies of parkinson disease and facilitates formation of alpha-synuclein inclusions. J Biol Chem. 281:4117–4125. 2006.PubMed/NCBI View Article : Google Scholar | |
|
Weller J and Budson A: Current understanding of Alzheimer's disease diagnosis and treatment. F1000Res 7: Faculty Rev-1161, 2018. | |
|
Karran E and De Strooper B: The amyloid hypothesis in Alzheimer disease: New insights from new therapeutics. Nat Rev Drug Discov. 21:306–318. 2022.PubMed/NCBI View Article : Google Scholar | |
|
Ma C, Hong F and Yang S: Amyloidosis in Alzheimer's Disease: Pathogeny, etiology, and related therapeutic directions. Molecules. 27(1210)2022.PubMed/NCBI View Article : Google Scholar | |
|
Bianchi M and Manco M: Pin1 modulation in physiological status and neurodegeneration. Any contribution to the pathogenesis of type 3 diabetes? Int J Mol Sci. 19(2319)2018.PubMed/NCBI View Article : Google Scholar | |
|
Wang SC, Hu XM and Xiong K: The regulatory role of Pin1 in neuronal death. Neural Regen Res. 18:74–80. 2023.PubMed/NCBI View Article : Google Scholar | |
|
Fagiani F, Govoni S, Racchi M and Lanni C: The Peptidyl-prolyl Isomerase Pin1 in neuronal Signaling: From neurodevelopment to neurodegeneration. Mol Neurobiol. 58:1062–1073. 2021.PubMed/NCBI View Article : Google Scholar | |
|
Palaiogeorgou AM, Papakonstantinou E, Golfinopoulou R, Sigala M, Mitsis T, Papageorgiou L, Diakou I, Pierouli K, Dragoumani K, Spandidos DA, et al: Recent approaches on Huntington's disease (Review). Biomed Rep. 18(5)2023.PubMed/NCBI View Article : Google Scholar | |
|
D'Egidio F, Castelli V, Cimini A and d'Angelo M: Cell rearrangement and oxidant/antioxidant imbalance in huntington's disease. Antioxidants (Basel). 12(571)2023.PubMed/NCBI View Article : Google Scholar | |
|
Pereira CAS, Medaglia NC, Ureshino RP, Bincoletto C, Antonioli M, Fimia GM, Piacentini M, Pereira GJDS, Erustes AG and Smaili SS: NAADP-Evoked Ca2+ signaling leads to mutant huntingtin aggregation and autophagy impairment in murine astrocytes. Int J Mol Sci. 24(5593)2023.PubMed/NCBI View Article : Google Scholar | |
|
Sap KA, Geijtenbeek KW, Schipper-Krom S, Guler AT and Reits EA: Ubiquitin-modifying enzymes in Huntington's disease. Front Mol Biosci. 10(1107323)2023.PubMed/NCBI View Article : Google Scholar | |
|
Napoli M, Girardini JE, Piazza S and Del Sal G: Wiring the oncogenic circuitry: Pin1 unleashes mutant p53. Oncotarget. 2:654–656. 2011.PubMed/NCBI View Article : Google Scholar | |
|
Steger M, Murina O, Hühn D, Ferretti LP, Walser R, Hänggi K, Lafranchi L, Neugebauer C, Paliwal S, Janscak P, et al: Prolyl isomerase PIN1 regulates DNA double-strand break repair by counteracting DNA end resection. Mol Cell. 50:333–343. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Ulugut H and Pijnenburg YAL: Frontotemporal dementia: Past, present, and future. Alzheimers Dement. 19:5253–5263. 2023.PubMed/NCBI View Article : Google Scholar | |
|
Thorpe JR, Mosaheb S, Hashemzadeh-Bonehi L, Cairns NJ, Kay JE, Morley SJ and Rulten SL: Shortfalls in the peptidyl-prolyl cis-trans isomerase protein Pin1 in neurons are associated with frontotemporal dementias. Neurobiol Dis. 17:237–249. 2004.PubMed/NCBI View Article : Google Scholar | |
|
Cataldo AM, Peterhoff CM, Troncoso JC, Gomez-Isla T, Hyman BT and Nixon RA: Endocytic pathway abnormalities precede amyloid beta deposition in sporadic Alzheimer's disease and Down syndrome: Differential effects of APOE genotype and presenilin mutations. Am J Pathol. 157:277–286. 2000.PubMed/NCBI View Article : Google Scholar | |
|
Husseman JW, Nochlin D and Vincent I: Mitotic activation: A convergent mechanism for a cohort of neurodegenerative diseases. Neurobiol Aging. 21:815–828. 2000.PubMed/NCBI View Article : Google Scholar | |
|
Mead RJ, Shan N, Reiser HJ, Marshall F and Shaw PJ: Amyotrophic lateral sclerosis: A neurodegenerative disorder poised for successful therapeutic translation. Nat Rev Drug Discov. 22:185–212. 2023.PubMed/NCBI View Article : Google Scholar | |
|
Iridoy MO, Zubiri I, Zelaya MV, Martinez L, Ausín K, Lachen-Montes M, Santamaría E, Fernandez-Irigoyen J and Jericó I: Neuroanatomical quantitative proteomics reveals common pathogenic biological routes between amyotrophic lateral sclerosis (ALS) and frontotemporal dementia (FTD). Int J Mol Sci. 20(4)2018.PubMed/NCBI View Article : Google Scholar | |
|
Perrot R and Eyer J: Neuronal intermediate filaments and neurodegenerative disorders. Brain Res Bull. 80:282–295. 2009.PubMed/NCBI View Article : Google Scholar | |
|
Kesavapany S, Patel V, Zheng YL, Pareek TK, Bjelogrlic M, Albers W, Amin N, Jaffe H, Gutkind JS, Strong MJ, et al: Inhibition of Pin1 reduces glutamate-induced perikaryal accumulation of phosphorylated neurofilament-H in neurons. Mol Biol Cell. 18:3645–3655. 2007.PubMed/NCBI View Article : Google Scholar | |
|
Chao SH, Greenleaf AL and Price DH: Juglone, an inhibitor of the peptidyl-prolyl isomerase Pin1, also directly blocks transcription. Nucleic Acids Res. 29:767–773. 2001.PubMed/NCBI View Article : Google Scholar | |
|
Xi L, Wang Y, He Q, Zhang Q and Du L: Interaction between Pin1 and its natural product inhibitor epigallocatechin-3-gallate by spectroscopy and molecular dynamics simulations. Spectrochim Acta A Mol Biomol Spectrosc. 169:134–143. 2016.PubMed/NCBI View Article : Google Scholar | |
|
Bayer E, Thutewohl M, Christner C, Tradler T, Osterkamp F, Waldmann H and Bayer P: Identification of hPin1 inhibitors that induce apoptosis in a mammalian Ras transformed cell line. Chem Commun (Camb). 516–518. 2005.PubMed/NCBI View Article : Google Scholar | |
|
Jiang B and Pei D: A selective, cell-permeable nonphosphorylated bicyclic peptidyl inhibitor against Peptidyl-Prolyl isomerase Pin1. J Med Chem. 58:6306–6312. 2015.PubMed/NCBI View Article : Google Scholar | |
|
He S, Li L, Jin R and Lu X: Biological function of Pin1 in vivo and its inhibitors for preclinical study: Early development, current strategies, and future directions. J Med Chem. 66:9251–9277. 2023.PubMed/NCBI View Article : Google Scholar | |
|
Guo C, Hou X, Dong L, Dagostino E, Greasley S, Ferre R, Marakovits J, Johnson MC, Matthews D, Mroczkowski B, et al: Structure-based design of novel human Pin1 inhibitors (I). Bioorg Med Chem Lett. 19:5613–5616. 2009.PubMed/NCBI View Article : Google Scholar | |
|
Russo Spena C, De Stefano L, Poli G, Granchi C, El Boustani M, Ecca F, Grassi G, Grassi M, Canzonieri V, Giordano A, et al: Virtual screening identifies a PIN1 inhibitor with possible antiovarian cancer effects. J Cell Physiol. 234:15708–15716. 2019.PubMed/NCBI View Article : Google Scholar | |
|
Campaner E, Rustighi A, Zannini A, Cristiani A, Piazza S, Ciani Y, Kalid O, Golan G, Baloglu E, Shacham S, et al: A covalent PIN1 inhibitor selectively targets cancer cells by a dual mechanism of action. Nat Commun. 8(15772)2017.PubMed/NCBI View Article : Google Scholar | |
|
Liu L, Zhu R, Li J, Pei Y, Wang S, Xu P, Wang M, Wen Y, Zhang H, Du D, et al: Computational and structure-based development of high potent cell-active covalent inhibitor targeting the Peptidyl-Prolyl isomerase NIMA-Interacting-1 (Pin1). J Med Chem. 65:2174–2190. 2022.PubMed/NCBI View Article : Google Scholar | |
|
Born A, Henen MA and Vogeli B: Activity and Affinity of Pin1 Variants. Molecules. 25:2019.PubMed/NCBI View Article : Google Scholar | |
|
Lu PJ, Zhou XZ, Liou YC, Noel JP and Lu KP: Critical role of WW domain phosphorylation in regulating phosphoserine binding activity and Pin1 function. J Biol Chem. 277:2381–2384. 2002.PubMed/NCBI View Article : Google Scholar | |
|
Verdecia MA, Bowman ME, Lu KP, Hunter T and Noel JP: Structural basis for phosphoserine-proline recognition by group IV WW domains. Nat Struct Biol. 7:639–643. 2000.PubMed/NCBI View Article : Google Scholar | |
|
Wang JZ, Xi L, Lin T, Wang Y, Zhu GF and Du LF: The structural and functional role of the three tryptophan residues in Pin1. J Photochem Photobiol B. 146:58–67. 2015.PubMed/NCBI View Article : Google Scholar | |
|
Li K, Li L, Wang S, Li X, Ma T, Liu D, Jing Y and Zhao L: Design and synthesis of novel 2-substituted 11-keto-boswellic acid heterocyclic derivatives as anti-prostate cancer agents with Pin1 inhibition ability. Eur J Med Chem. 126:910–919. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Maggio J, Cabrera M, Armando R, Chinestrad P, Pifano M, Menna PL, Gomez DE and Gómez DLM: Rational design of PIN1 inhibitors for cancer treatment based on conformational diversity analysis and docking based virtual screening. J Biomol Struct Dyn. 40:5858–5867. 2022.PubMed/NCBI View Article : Google Scholar |
