The peptidyl-prolyl isomerase pin1 up-regulation and proapoptotic function in dopaminergic neurons: Relevance to the pathogenesis of parkinson disease

Journal of Biological Chemistry

Volumn 288, Issue 30, 2013, Pages 21955-21971

  Ghosh, Anamitra ^a   Saminathan, Hariharan ^a   Kanthasamy, Arthi ^a   Anantharam, Vellareddy ^a   Jin, Huajun ^a   Sondarva, Gautam ^b   Harischandra, Dilshan S ^a   Qian, Ziqing ^c   Rana, Ajay ^b,d   Kanthasamy, Anumantha G ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b LOYOLA UNIVERSITY CHICAGO   (United States)

^c OHIO STATE UNIVERSITY   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL MODEL; DOPAMINERGIC NEURONS; PARKINSON DISEASE; PEPTIDE BONDS; PEPTIDYL-PROLYL ISOMERASE; PRO-APOPTOTIC FUNCTION; SIGNALING PROTEINS; UP-REGULATION;

CELL CULTURE;

NEURONS;

1 METHYL 4 PHENYLPYRIDINIUM; 1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; ALPHA SYNUCLEIN; CASPASE 3; DOPAMINE; JUGLONE; MESSENGER RNA; PEPTIDYLPROLYL ISOMERASE PIN1; PROTEIN INHIBITOR; PROTEIN INHIBITOR F; PROTEIN INHIBITOR PIB; SIGNAL PEPTIDE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BEHAVIOR DISORDER; BRAIN TISSUE; CELL CULTURE; CELL LOSS; CIS TRANS ISOMERISM; CONTROLLED STUDY; DISEASE MODEL; DNA FRAGMENTATION; DOPAMINERGIC NERVE CELL; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME LOCALIZATION; ENZYME REGULATION; ENZYME REPRESSION; HUMAN; HUMAN TISSUE; MOTOR DYSFUNCTION; MOUSE; NERVE DEGENERATION; NEUROPROTECTION; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PARKINSON DISEASE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN EXPRESSION; SUBSTANTIA NIGRA; UPREGULATION;

CASPASE-3; DOPAMINE; JUGLONE; MPTP; NEUROBIOLOGY; NEURODEGENERATIVE DISEASES; NEUROPROTECTION; PARKINSON DISEASE; PIN1;

1-METHYL-4-PHENYL-1,2,3,6-TETRAHYDROPYRIDINE; 1-METHYL-4-PHENYLPYRIDINIUM; ANIMALS; APOPTOSIS; BRAIN; CELLS, CULTURED; DOPAMINERGIC NEURONS; GENE EXPRESSION; HUMANS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; NAPHTHOQUINONES; NEUROTOXINS; PARKINSON DISEASE; PARKINSON DISEASE, SECONDARY; PEPTIDYLPROLYL ISOMERASE; RNA INTERFERENCE; RNA-DIRECTED DNA POLYMERASE; SUBSTANTIA NIGRA; UP-REGULATION;

EID: 84881224985     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.444224     Document Type: Article

References (66)

1. Lees, A. J., Hardy, J., and Revesz, T. (2009) Parkinson disease. Lancet 373, 2055-2066
2. Dauer, W., and Przedborski, S. (2003) Parkinson's disease. Mechanisms and models. Neuron 39, 889-909
3. Dunnett, S. B., and Björklund, A. (1999) Prospects for new restorative and neuroprotective treatments in Parkinson's disease. Nature 399, A32-A39
4. Ghosh, A., Roy, A., Matras, J., Brahmachari, S., Gendelman, H. E., and Pahan, K. (2009) Simvastatin inhibits the activation of p21ras and prevents the loss of dopaminergic neurons in a mouse model of Parkinson's disease. J. Neurosci. 29, 13543-13556
5. Chaudhuri, K. R., and Schapira, A. H. (2009) Non-motor symptoms of Parkinson's disease. Dopaminergic pathophysiology and treatment. Lancet Neurol. 8, 464-474
6. Martinez-Martin, P., Rodriguez-Blazquez, C., Abe, K., Bhattacharyya, K. B., Bloem, B. R., Carod-Artal, F. J., Prakash, R., Esselink, R. A., Falup-Pecurariu, C., Gallardo, M., Mir, P., Naidu, Y., Nicoletti, A., Sethi, K., Tsuboi, Y., van Hilten, J. J., Visser, M., Zappia, M., and Chaudhuri, K. R. (2009) International study on the psychometric attributes of the nonmotor symptoms scale in Parkinson's disease. Neurology 73, 1584-1591
7. Göthel, S. F., and Marahiel, M. A. (1999) Peptidyl-prolyl cis-trans isomerases, a superfamily of ubiquitous folding catalysts. Cell Mol. Life Sci. 55, 423-436
8. Lu, K. P., Finn, G., Lee, T. H., and Nicholson, L. K. (2007) Prolyl cis-trans isomerization as a molecular timer. Nat. Chem. Biol. 3, 619-629
9. Shaw, P. E. (2007) Peptidyl-prolyl cis/trans isomerases and transcription. Is there a twist in the tail? EMBO Rep. 8, 40-45
10. Joseph, J. D., Yeh, E. S., Swenson, K. I., Means, A. R., and Winkler (2003) The peptidyl-prolyl isomerase Pin1. Prog. Cell Cycle Res. 5, 477-487
11. Lu, K. P. (2003) Prolyl isomerase Pin1 as a molecular target for cancer diagnostics and therapeutics. Cancer Cell 4, 175-180
12. Atchison, F. W., and Means, A. R. (2004) A role for Pin1 in mammalian germ cell development and spermatogenesis. Front. Biosci. 9, 3248-3256
13. Braithwaite, A. W., Del Sal, G., and Lu, X. (2006) Some p53-binding proteins that can function as arbiters of life and death. Cell Death Differ. 13, 984-993
14. Akiyama, H., Shin, R. W., Uchida, C., Kitamoto, T., and Uchida, T. (2005) Pin1 promotes production of Alzheimer's amyloid α from-cleaved amyloid precursor protein. Biochem. Biophys. Res. Commun. 336, 521-529
15. Maruszak, A., Safranow, K., Gustaw, K., Kijanowska-Haładyna, B., Jakubowska, K., Olszewska, M., Styczyńska, M., Berdyński, M., Tysarowski, A., Chlubek, D., Siedlecki, J., Barcikowska, M., and Zekanowski, C. (2009) PIN1 gene variants in Alzheimer's disease. BMC Med. Genet. 10, 115
16. Esnault, S., Shen, Z. J., and Malter, J. S. (2008) Pinning down signaling in the immune system. The role of the peptidyl-prolyl isomerase Pin1 in immune cell function. Crit. Rev. Immunol. 28, 45-60
17. Shen, Z. J., Esnault, S., Rosenthal, L. A., Szakaly, R. J., Sorkness, R. L., Westmark, P. R., Sandor, M., and Malter, J. S. (2008) Pin1 regulates TGF-α1 production by activated human and murine eosinophils and contributes to allergic lung fibrosis. J. Clin. Invest. 118, 479-490
18. Hutton, M., Lewis, J., Dickson, D., Yen, S. H., and McGowan, E. (2001) Analysis of tauopathies with transgenic mice. Trends Mol. Med. 7, 467-470
19. Lee, V. M., Goedert, M., and Trojanowski, J. Q. (2001) Neurodegenerative tauopathies. Annu. Rev. Neurosci. 24, 1121-1159
20. Li, H., Wang, S., Zhu, T., Zhou, J., Xu, Q., Lu, Y., and Ma, D. (2006) Pin1 contributes to cervical tumorigenesis by regulating cyclin D1 expression. Oncol. Rep. 16, 491-496
21. Becker, E. B., and Bonni, A. (2006) Pin1 mediates neural-specific activation of the mitochondrial apoptotic machinery. Neuron 49, 655-662
22. Lu, P. J., Wulf, G., Zhou, X. Z., Davies, P., and Lu, K. P. (1999) The prolyl isomerase Pin1 restores the function of Alzheimer-associated phosphorylated tau protein. Nature 399, 784-788
23. Becker, E. B., and Bonni, A. (2007) Pin1 in neuronal apoptosis. Cell Cycle 6, 1332-1335
24. Ryo, A., Togo, T., Nakai, T., Hirai, A., Nishi, M., Yamaguchi, A., Suzuki, K., Hirayasu, Y., Kobayashi, H., Perrem, K., Liou, Y. C., and Aoki, I. (2006) Prolyl-isomerase Pin1 accumulates in lewy bodies of Parkinson disease and facilitates formation of-synuclein inclusions. J. Biol. Chem. 281, 4117-4125
25. Rangasamy, V., Mishra, R., Sondarva, G., Das, S., Lee, T. H., Bakowska, J. C., Tzivion, G., Malter, J. S., Rana, B., Lu, K. P., Kanthasamy, A., and Rana, A. (2012) Mixed-lineage kinase 3 phosphorylates prolyl-isomerase Pin1 to regulate its nuclear translocation and cellular function. Proc. Natl. Acad. Sci. U.S.A. 109, 8149-8154
26. Liu, T., Liu, Y., Kao, H. Y., and Pei, D. (2010) Membrane permeable cyclic peptidyl inhibitors against human peptidylprolyl isomerase Pin1. J. Med. Chem. 53, 2494-2501
27. Choi, H. K., Won, L. A., Kontur, P. J., Hammond, D. N., Fox, A. P., Wainer, B. H., Hoffmann, P. C., and Heller, A. (1991) Immortalization of embryonic mesencephalic dopaminergic neurons by somatic cell fusion. Brain Res. 552, 67-76
28. Sun, F., Anantharam, V., Latchoumycandane, C., Kanthasamy, A., and Kanthasamy, A. G. (2005) Dieldrin induces ubiquitin-proteasome dysfunction in-synuclein overexpressing dopaminergic neuronal cells and enhances susceptibility to apoptotic cell death. J. Pharmacol. Exp. Ther. 315, 69-79
29. Anantharam, V., Kaul, S., Song, C., Kanthasamy, A., and Kanthasamy, A. G. (2007) Pharmacological inhibition of neuronalNADPHoxidase protects against 1-methyl-4-phenylpyridinium (MPP-)-induced oxidative stress and apoptosis in mesencephalic dopaminergic neuronal cells. Neurotoxicology 28, 988-997
30. Song, C., Kanthasamy, A., Anantharam, V., Sun, F., and Kanthasamy, A. G. (2010) Environmental neurotoxic pesticide increases histone acetylation to promote apoptosis in dopaminergic neuronal cells. Relevance to epigenetic mechanisms of neurodegeneration. Mol. Pharmacol. 77, 621-632
31. Zhang, D., Anantharam, V., Kanthasamy, A., and Kanthasamy, A. G. (2007) Neuroprotective effect of protein kinase C delta inhibitor rottlerin in cell culture and animal models of Parkinson's disease. J. Pharmacol. Exp. Ther. 322, 913-922
32. Ghosh, A., Kanthasamy, A., Joseph, J., Anantharam, V., Srivastava, P., Dranka, B. P., Kalyanaraman, B., and Kanthasamy, A. G. (2012) Antiinflammatory and neuroprotective effects of an orally active apocynin derivative in pre-clinical models of Parkinson's disease. J. Neuroinflammation 9, 241
33. Ghosh, A., Chandran, K., Kalivendi, S. V., Joseph, J., Antholine, W. E., Hillard, C. J., Kanthasamy, A., Kanthasamy, A., and Kalyanaraman, B. (2010) Neuroprotection by a mitochondria-targeted drug in a Parkinson's disease model. Free Radic. Biol. Med. 49, 1674-1684
34. Roy, A., Ghosh, A., Jana, A., Liu, X., Brahmachari, S., Gendelman, H. E., and Pahan, K. (2012) Sodium phenylbutyrate controls neuroinflammatory and antioxidant activities and protects dopaminergic neurons in mouse models of Parkinson's disease. PloS ONE 7, e38113
35. Hu, X., Weng, Z., Chu, C. T., Zhang, L., Cao, G., Gao, Y., Signore, A., Zhu, J., Hastings, T., Greenamyre, J. T., and Chen, J. (2011) Peroxiredoxin-2 protects against 6-hydroxydopamine-induced dopaminergic neurodegeneration via attenuation of the apoptosis signal-regulating kinase (ASK1) signaling cascade. J. Neurosci. 31, 247-261
36. Castro, D. S., Hermanson, E., Joseph, B., Wallén, A., Aarnisalo, P., Heller, A., and Perlmann, T. (2001) Induction of cell cycle arrest and morphological differentiation by Nurr1 and retinoids in dopamine MN9D cells. J. Biol. Chem. 276, 43277-43284
37. Hirsch, E., Graybiel, A. M., and Agid, Y. A. (1988) Melanized dopaminergic neurons are differentially susceptible to degeneration in Parkinson's disease. Nature 334, 345-348
38. Kastner, A., Hirsch, E. C., Lejeune, O., Javoy-Agid, F., Rascol, O., and Agid, Y. (1992) Is the vulnerability of neurons in the substantia nigra of patients with Parkinson's disease related to their neuromelanin content? J. Neurochem. 59, 1080-1089
39. Uchida, T., Takamiya, M., Takahashi, M., Miyashita, H., Ikeda, H., Terada, T., Matsuo, Y., Shirouzu, M., Yokoyama, S., Fujimori, F., and Hunter, T. (2003) Pin1 and Par14 peptidyl prolyl isomerase inhibitors block cell proliferation. Chem. Biol. 10, 15-24
40. Rudrabhatla, P., and Pant, H. C. (2010) Phosphorylation-specific peptidylprolyl isomerization of neuronal cytoskeletal proteins by Pin1. Implications for therapeutics in neurodegeneration. J. Alzheimers Dis. 19, 389-403
41. Butterfield, D. A., Abdul, H. M., Opii, W., Newman, S. F., Joshi, G., Ansari, M. A., and Sultana, R. (2006) Pin1 in Alzheimer's disease. J. Neurochem. 98, 1697-1706
42. Sultana, R., Boyd-Kimball, D., Poon, H. F., Cai, J., Pierce, W. M., Klein, J. B., Markesbery, W. R., Zhou, X. Z., Lu, K. P., and Butterfield, D. A. (2006) Oxidative modification and down-regulation of Pin1 in Alzheimer's disease hippocampus. A redox proteomics analysis. Neurobiol. Aging 27, 918-925
43. Kesavapany, S., Patel, V., Zheng, Y. L., Pareek, T. K., Bjelogrlic, M., Albers, W., Amin, N., Jaffe, H., Gutkind, J. S., Strong, M. J., Grant, P., and Pant, H. C. (2007) Inhibition of Pin1 reduces glutamate-induced perikaryal accumulation of phosphorylated neurofilament-H in neurons. Mol. Biol. Cell 18, 3645-3655
44. Rudrabhatla, P., Albers, W., and Pant, H. C. (2009) Peptidyl-prolyl isomerase 1 regulates protein phosphatase 2A-mediated topographic phosphorylation of neurofilament proteins. J. Neurosci. 29, 14869-14880
45. Lou, H., Montoya, S. E., Alerte, T. N., Wang, J., Wu, J., Peng, X., Hong, C. S., Friedrich, E. E., Mader, S. A., Pedersen, C. J., Marcus, B. S., McCormack, A. L., Di Monte, D. A., Daubner, S. C., and Perez, R. G. (2010) Serine 129 phosphorylation reduces the ability of-synuclein to regulate tyrosine hydroxylase and protein phosphatase 2A in vitro and in vivo. J. Biol. Chem. 285, 17648-17661
46. Mbefo, M. K., Paleologou, K. E., Boucharaba, A., Oueslati, A., Schell, H., Fournier, M., Olschewski, D., Yin, G., Zweckstetter, M., Masliah, E., Kahle, P. J., Hirling, H., and Lashuel, H. A. (2010) Phosphorylation of synucleins by members of the Polo-like kinase family. J. Biol. Chem. 285, 2807-2822
47. Machiya, Y., Hara, S., Arawaka, S., Fukushima, S., Sato, H., Sakamoto, M., Koyama, S., and Kato, T. (2010) Phosphorylated-synuclein at Ser-129 is targeted to the proteasome pathway in a ubiquitin-independent manner. J. Biol. Chem. 285, 40732-40744
48. Pronin, A. N., Morris, A. J., Surguchov, A., and Benovic, J. L. (2000) Synucleins are a novel class of substrates for G protein-coupled receptor kinases. J. Biol. Chem. 275, 26515-26522
49. Sakamoto, M., Arawaka, S., Hara, S., Sato, H., Cui, C., Machiya, Y., Koyama, S., Wada, M., Kawanami, T., Kurita, K., and Kato, T. (2009) Contribution of endogenous G-protein-coupled receptor kinases to Ser-129 phosphorylation of-synuclein in HEK293 cells. Biochem. Biophys. Res. Commun. 384, 378-382
50. Okochi, M., Walter, J., Koyama, A., Nakajo, S., Baba, M., Iwatsubo, T., Meijer, L., Kahle, P. J., and Haass, C. (2000) Constitutive phosphorylation of the Parkinson's disease associated-synuclein. J. Biol. Chem. 275, 390-397
51. Inglis, K. J., Chereau, D., Brigham, E. F., Chiou, S. S., Schöbel, S., Frigon, N. L., Yu, M., Caccavello, R. J., Nelson, S., Motter, R., Wright, S., Chian, D., Santiago, P., Soriano, F., Ramos, C., Powell, K., Goldstein, J. M., Babcock, M., Yednock, T., Bard, F., Basi, G. S., Sham, H., Chilcote, T. J., McConlogue, L., Griswold-Prenner, I., and Anderson, J. P. (2009) Pololike kinase 2 (PLK2) phosphorylates-synuclein at serine 129 in central nervous system. J. Biol. Chem. 284, 2598-2602
52. Lee, K. W., Chen, W., Junn, E., Im, J. Y., Grosso, H., Sonsalla, P. K., Feng, X., Ray, N., Fernandez, J. R., Chao, Y., Masliah, E., Voronkov, M., Braithwaite, S. P., Stock, J. B., and Mouradian, M. M. (2011) Enhanced phosphatase activity attenuates-synucleinopathy in a mouse model. J. Neurosci. 31, 6963-6971
53. Ai, Z., Zhang, W., Luo, W., Huang, L., and Pan, Y. (2009) Expression of Pin1 mRNA in non-small-cell lung cancer patients. Asian Cardiovasc. Thorac. Ann. 17, 157-161
54. Miyashita, H., Mori, S., Motegi, K., Fukumoto, M., and Uchida, T. (2003) Pin1 is overexpressed in oral squamous cell carcinoma and its levels correlate with cyclin D1 overexpression. Oncol. Rep. 10, 455-461
55. Lv, L., Zhou, Z., Huang, X., Zhao, Y., Zhang, L., Shi, Y., Sun, M., and Zhang, J. (2010) Inhibition of peptidyl-prolyl cis/trans isomerase Pin1 induces cell cycle arrest and apoptosis in vascular smooth muscle cells. Apoptosis 15, 41-54
56. Shen, Z. J., Esnault, S., Schinzel, A., Borner, C., and Malter, J. S. (2009) The peptidyl-prolyl isomerase Pin1 facilitates cytokine-induced survival of eosinophils by suppressing Bax activation. Nat. Immunol. 10, 257-265
57. Li, Q. M., Tep, C., Yune, T. Y., Zhou, X. Z., Uchida, T., Lu, K. P., and Yoon, S. O. (2007) Opposite regulation of oligodendrocyte apoptosis by JNK3 and Pin1 after spinal cord injury. J. Neurosci. 27, 8395-8404
58. Barone, M. C., Desouza, L. A., and Freeman, R. S. (2008) Pin1 promotes cell death in NGF-dependent neurons through a mechanism requiring c-Jun activity. J. Neurochem. 106, 734-745
59. Esnault, S., Rosenthal, L. A., Shen, Z. J., Sedgwick, J. B., Szakaly, R. J., Sorkness, R. L., and Malter, J. S. (2007) A critical role for Pin1 in allergic pulmonary eosinophilia in rats. J. Allergy Clin. Immunol. 120, 1082-1088
60. Jeong, H. G., Pokharel, Y. R., Lim, S. C., Hwang, Y. P., Han, E. H., Yoon, J. H., Ahn, S. G., Lee, K. Y., and Kang, K. W. (2009) Novel role of Pin1 induction in type II collagen-mediated rheumatoid arthritis. J. Immunol. 183, 6689-6697
61. Hennig, L., Christner, C., Kipping, M., Schelbert, B., Rücknagel, K. P., Grabley, S., Küllertz, G., and Fischer, G. (1998) Selective inactivation of parvulin-like peptidyl-prolyl cis/trans isomerases by juglone. Biochemistry 37, 5953-5960
62. Ryo, A., Liou, Y. C., Wulf, G., Nakamura, M., Lee, S. W., and Lu, K. P. (2002) PIN1 is an E2F target gene essential for Neu/Ras-induced transformation of mammary epithelial cells. Mol. Cell. Biol. 22, 5281-5295
63. Lee, K. Y., Lee, J. W., Nam, H. J., Shim, J. H., Song, Y., and Kang, K. W. (2011) PI3-kinase/p38 kinase-dependent E2F1 activation is critical for Pin1 induction in tamoxifen-resistant breast cancer cells. Mol. Cells 32, 107-111
64. Ryo, A., Suizu, F., Yoshida, Y., Perrem, K., Liou, Y. C., Wulf, G., Rottapel, R., Yamaoka, S., and Lu, K. P. (2003) Regulation of NF-κB signaling by Pin1-dependent prolyl isomerization and ubiquitin-mediated proteolysis of p65/RelA. Mol. Cell 12, 1413-1426
65. Mantovani, F., Tocco, F., Girardini, J., Smith, P., Gasco, M., Lu, X., Crook, T., and Del Sal, G. (2007) The prolyl isomerase Pin1 orchestrates p53 acetylation and dissociation from the apoptosis inhibitor iASPP. Nat. Struct. Mol. Biol. 14, 912-920
66. Wulf, G. M., Liou, Y. C., Ryo, A., Lee, S. W., and Lu, K. P. (2002) Role of Pin1 in the regulation of p53 stability and p21 transactivation and cell cycle checkpoints in response to DNA damage. J. Biol. Chem. 277, 47976-47979