The role of ERK1, 2, and 5 in dopamine neuron survival during aging

Neurobiology of Aging

Volumn 35, Issue 3, 2014, Pages 669-679

  Parmar, Mayur S ^a   Jaumotte, Juliann D ^b   Wyrostek, Stephanie L ^b   Zigmond, Michael J ^b   Cavanaugh, Jane E ^a  

^a DUQUESNE UNIVERSITY   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Aging; Brain; ERK1 2; ERK5; Fischer 344xBrown Norway F1 hybrids (F344xBN F1); MAP kinases; Striatum; Substantia nigra; Ventral tegmental area

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE 7;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; FEMALE; HUMAN; HUMAN CELL; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SUBSTANTIA NIGRA; VENTRAL TEGMENTUM;

AGING; BRAIN; ERK1/2; ERK5; FISCHER-344XBROWN NORWAY F1 HYBRIDS (F344XBN F1); MAP KINASES; STRIATUM; SUBSTANTIA NIGRA; VENTRAL TEGMENTAL AREA;

AGING; ANIMALS; CELL SURVIVAL; CELLS, CULTURED; CORPUS STRIATUM; DOPAMINE; MALE; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MITOGEN-ACTIVATED PROTEIN KINASE 7; NEURONS; PHOSPHORYLATION; RATS; RATS, INBRED BN; RATS, INBRED F344; SUBSTANTIA NIGRA; VENTRAL TEGMENTAL AREA;

EID: 84889564798     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2013.09.031     Document Type: Article

References (58)

1. Allen E., Carlson K.M., Zigmond M.J., Cavanaugh J.E. L-DOPA reverses motor deficits associated with normal aging in mice. Neurosci. Lett. 2011, 489:1-4.
2. Barros J.C., Marshall C.J. Activation of either ERK1/2 or ERK5 MAP kinase pathways can lead to disruption of the actin cytoskeleton. J.Cell. Sci. 2005, 118:1663-1671.
3. Bennett D.A., Beckett L.A., Murray A.M., Shannon K.M., Goetz C.G., Pilgrim D.M., Evans D.A. Prevalence of parkinsonian signs and associated mortality in a community population of older people. N.Engl. J. Med. 1996, 334:71-76.
4. Biedler J.L., Helson L., Spengler B.A. Morphology and growth, tumorigenicity, and cytogenetics of human neuroblastoma cells in continuous culture. Cancer Res. 1973, 33:2643-2652.
5. Boger H., Middaugh L., Huang P., Zaman V., Smith A., Hoffer B., Tomac A., Granholm A. Apartial GDNF depletion leads to earlier age-related deterioration of motor function and tyrosine hydroxylase expression in the substantia nigra. Exp. Neurol. 2006, 202:336-347.
6. Carlsson T., Schindler F.R., Höllerhage M., Depboylu C., Arias-Carrión O., Schnurrbusch S., Rösler T.W., Wozny W., Schwall G.P., Groebe K. Systemic administration of neuregulin-1β1 protects dopaminergic neurons in a mouse model of Parkinson's disease. J.Neurochem. 2011, 117:1066-1074.
7. Carlsson A., Winblad B. Influence of age and time interval between death and autopsy on dopamine and 3-methoxytyramine levels in human basal ganglia. J.Neural Transm. 1976, 38:271-276.
8. Cavanaugh J.E. Role of extracellular signal regulated kinase 5 in neuronal survival. Eur. J. Biochem. 2004, 271:2056-2059.
9. Cavanaugh J.E., Ham J., Hetman M., Poser S., Yan C., Xia Z. Differential regulation of mitogen-activated protein kinases ERK1/2 and ERK5 by neurotrophins, neuronal activity, and cAMP in neurons. J.Neurosci. 2001, 21:434-443.
10. Cavanaugh J.E., Jaumotte J.D., Lakoski J.M., Zigmond M.J. Neuroprotective role of ERK1/2 and ERK5 in a dopaminergic cell line under basal conditions and in response to oxidative stress. J.Neurosci. Res. 2006, 84:1367-1375.
11. Cheung Y., Lau W.K., Yu M., Lai C.S., Yeung S., So K., Chang R.C. Effects of all-trans-retinoic acid on human SH-SY5Y neuroblastoma as invitro model in neurotoxicity research. Neurotoxicology 2009, 30:127-135.
12. Di Benedetto B., Hitz C., Holter S.M., Kuhn R., Vogt Weisenhorn D.M., Wurst W. Differential mRNA distribution of components of the ERK/MAPK signalling cascade in the adult mouse brain. J.Comp. Neurol. 2007, 500:542-556.
13. Dickerson, J.W., 2010. Neuroprotective and neurorestorative effects of neuregulins in the injured and aged dopaminergic nigrostriatal system. Electronic Thesis or Dissertation. University of Cincinnati, 2010. OhioLINK Electronic Theses and Dissertations Center. Retrieved from http://https://etd.ohiolink.edu/.
14. Dickerson J.W., Hemmerle A.M., Numan S., Lundgren K.H., Seroogy K.B. Decreased expression of ErbB4 and tyrosine hydroxylase mRNA and protein in the ventral midbrain of aged rats. Neuroscience 2009, 163:482-489.
15. Ding Y.M., Jaumotte J.D., Signore A.P., Zigmond M.J. Effects of 6-hydroxydopamine on primary cultures of substantia nigra: specific damage to dopamine neurons and the impact of glial cell line-derived neurotrophic factor. J.Neurochem. 2004, 89:776-787.
16. Dwivedi Y., Rizavi H.S., Teppen T., Sasaki N., Chen H., Zhang H., Roberts R.C., Conley R.R., Pandey G.N. Aberrant extracellular signal-regulated kinase (ERK) 5 signaling in hippocampus of suicide subjects. Neuropsychopharmacology 2007, 32:2338-2350.
17. Eriksen N., Stark A.K., Pakkenberg B. Age and Parkinson's disease-related neuronal death in the substantia nigra pars compacta. J.Neural Transm. Suppl. 2009, 73:203-213.
18. Esparis-Ogando A., Diaz-Rodriguez E., Montero J.C., Yuste L., Crespo P., Pandiella A. Erk5 participates in neuregulin signal transduction and is constitutively active in breast cancer cells overexpressing ErbB2. Mol. Cell. Biol. 2002, 22:270-285.
19. Fearnley J.M., Lees A.J. Ageing and Parkinson's disease: substantia nigra regional selectivity. Brain 1991, 114:2283-2301.
20. Finegan K.G., Wang X., Lee E.J., Robinson A.C., Tournier C. Regulation of neuronal survival by the extracellular signal-regulated protein kinase 5. Cell Death Differ. 2009, 16:674-683.
21. Fox C.M., Gash D.M., Smoot M.K., Cass W.A. Neuroprotective effects of GDNF against 6-OHDA in young and aged rats. Brain Res. 2001, 896:56-63.
22. Gerhardt G.A., Cass W.A., Henson M., Zhang Z., Ovadia A., Hoffer B.J., Gash D.M. Age-related changes in potassium-evoked overflow of dopamine in the striatum of the rhesus monkey. Neurobiol. Aging 1995, 16:939-946.
23. Hayashi Y., Iwashita T., Murakamai H., Kato Y., Kawai K., Kurokawa K., Tohnai I., Ueda M., Takahashi M. Activation of BMK1 via tyrosine 1062 in RET by GDNF and MEN2A mutation. Biochem. Biophys. Res. Commun. 2001, 281:682-689.
24. Hidalgo-Figueroa M., Bonilla S., Gutiérrez F., Pascual A., López-Barneo J. GDNF is predominantly expressed in the PV neostriatal interneuronal ensemble in normal mouse and after injury of the nigrostriatal pathway. J. Neurosci. 2012, 32:864-872.
25. Hou J.G., Cohen G., Mytilineou C. Basic fibroblast growth factor stimulation of glial cells protects dopamine neurons from 6-hydroxydopamine toxicity: involvement of the glutathione system. J.Neurochem. 1997, 69:76-83.
26. Irwin I., DeLanney L.E., McNeill T., Chan P., Forno L.S., Murphy G.M., Di Monte D.A., Sandy M.S., Langston J.W. Aging and the nigrostriatal dopamine system: a non-human primate study. Neurodegeneration 1994, 3:251-265.
27. Jenner P., Olanow C.W. Understanding cell death in Parkinson's disease. Ann. Neurol. 1998, 44:S72-S84.
28. Kamakura S., Moriguchi T., Nishida E. Activation of the protein kinase ERK5/BMK1 by receptor tyrosine kinases: identification and characterization of a signaling pathway to the nucleus. J.Biol. Chem. 1999, 274:26563-26571.
29. Kim S.R., Chen X., Oo T.F., Kareva T., Yarygina O., Wang C., During M., Kholodilov N., Burke R.E. Dopaminergic pathway reconstruction by Akt/Rheb-induced axon regeneration. Ann. Neurol. 2011, 70:110-120.
30. Kramer E.R., Aron L., Ramakers G.M., Seitz S., Zhuang X., Beyer K., Smidt M.P., Klein R. Absence of Ret signaling in mice causes progressive and late degeneration of the nigrostriatal system. PLOS Biol. 2007, 5:616-628.
31. Lindgren N., Leak R.K., Carlson K.M., Smith A.D., Zigmond M.J. Activation of the extracellular signal-regulated kinases 1 and 2 by glial cell line-derived neurotrophic factor and its relation to neuroprotection in a mouse model of Parkinson's disease. J.Neurosci. Res. 2008, 86:2039-2049.
32. Liu L., Cavanaugh J.E., Wang Y., Sakagami H., Mao Z., Xia Z. ERK5 activation of MEF2-mediated gene expression plays a critical role in BDNF-promoted survival of developing but not mature cortical neurons. Proc. Natl. Acad. Sci. U.S.A 2003, 100:8532-8537.
33. Liu L., Cundiff P., Abel G., Wang Y., Faigle R., Sakagami H., Xu M., Xia Z. Extracellular signal-regulated kinase (ERK) 5 is necessary and sufficient to specify cortical neuronal fate. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:9697-9702.
34. McGeer P.L., McGeer E.G., Suzuki J.S. Aging and extrapyramidal function. Arch. Neurol. 1977, 34:33.
35. Mo L., Ren Q., Duchemin A.M., Neff N.H., Hadjiconstantinou M. GM1 and ERK signaling in the aged brain. Brain Res. 2005, 1054:125-134.
36. Mody N., Leitch J., Armstrong C., Dixon J., Cohen P. Effects of MAP kinase cascade inhibitors on the MKK5/ERK5 pathway. FEBS Lett. 2001, 502:21-24.
37. Mogi M., Togari A., Kondo T., Mizuno Y., Komure O., Kuno S., Ichinose H., Nagatsu T. Brain-derived growth factor and nerve growth factor concentrations are decreased in the substantia nigra in Parkinson's disease. Neurosci. Lett. 1999, 270:45-48.
38. Morgan D.G., May P.C., Finch C.E. Dopamine and serotonin systems in human and rodent brain: effects of age and neurodegenerative disease. J.Am. Geriatr. Soc. 1987, 35:334-345.
39. National Research Council (US) Committee for the Update of the Guide for the Care and Use of Laboratory Animals NIH Care and Use of Laboratory Animals 2011, National Academies Press, Washington, D.C. eighth ed.
40. Obara Y., Yamauchi A., Takehara S., Nemoto W., Takahashi M., Stork P.J., Nakahata N. ERK5 activity is required for nerve growth factor-induced neurite outgrowth and stabilization of tyrosine hydroxylase in PC12 cells. J.Biol. Chem. 2009, 284:23564-23573.
41. Obara Y., Nemoto W., Kohno S., Murata T., Kaneda N., Nakahata N. Basic fibroblast growth factor promotes glial cell-derived neurotrophic factor gene expression mediated by activation of ERK5 in rat C6 glioma cells. Cell. Signal. 2011, 23:666-672.
42. Oyarce A.M., Fleming P.J. Multiple forms of human dopamine β-hydroxylase in SH-SY5Y neuroblastoma cells. Arch. Biochem. Biophys. 1991, 290:503-510.
43. Pan Y.W., Zou J., Wang W., Sakagami H., Garelick M.G., Abel G., Kuo C.T., Storm D.R., Xia Z. Inducible and conditional deletion of extracellular signal-regulated kinase 5 disrupts adult hippocampal neurogenesis. J.Biol. Chem. 2012, 287:23307-23317.
44. Pascual A., Hidalgo-Figueroa M., Piruat J.I., Pintado C.O., Gómez-Díaz R., López-Barneo J. Absolute requirement of GDNF for adult catecholaminergic neuron survival. Nat. Neurosci. 2008, 11:755-761.
45. Pruett B.S., Salvatore M.F. GFR alpha-1 receptor expression in the aging nigrostriatal and mesoaccumbens pathways. J.Neurochem. 2010, 115:707-715.
46. Satoh Y., Kobayashi Y., Takeuchi A., Pagès G., Pouysségur J., Kazama T. Deletion of ERK1 and ERK2 in the CNS causes cortical abnormalities and neonatal lethality: Erk1 deficiency enhances the impairment of neurogenesis in Erk2-deficient mice. J. Neurosci. 2011, 31:1149-1155.
47. Siegel G.J., Chauhan N.B. Neurotrophic factors in Alzheimer's and Parkinson's disease brain. Brain Res. Rev. 2000, 33:199-227.
48. Shalizi A., Lehtinen M., Gaudilliere B., Donovan N., Han J., Konishi Y., Bonni A. Characterization of a neurotrophin signaling mechanism that mediates neuron survival in a temporally specific pattern. J.Neurosci. 2003, 23:7326-7336.
49. Song G.Y., Kang J.S., Lee S.Y., Myung C.S. Region-specific reduction of Gbeta4 expression and induction of the phosphorylation of PKB/Akt and ERK1/2 by aging in rat brain. Pharmacol. Res. 2007, 56:295-302.
50. Tatake R.J., O'Neill M.M., Kennedy C.A., Wayne A.L., Jakes S., Wu D., Kugler S.Z., Kashem M.A., Kaplita P., Snow R.J. Identification of pharmacological inhibitors of the MEK5/ERK5 pathway. Biochem. Biophys. Res. Commun. 2008, 377:120-125.
51. Watson F.L., Heerssen H.M., Bhattacharyya A., Klesse L., Lin M.Z., Segal R.A. Neurotrophins use the Erk5 pathway to mediate a retrograde survival response. Nat. Neurosci. 2001, 4:981-988.
52. Xia Z., Dickens M., Raingeaud J., Davis R.J., Greenberg M.E. Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 1995, 270:1326-1331.
53. Xie H., Hu L., Li G. SH-SY5Y human neuroblastoma cell line: invitro cell model of dopaminergic neurons in Parkinson's disease. Chin. Med. J. 2010, 123:1086-1092.
54. Yoon S.C., Ahn Y.M., Jun S.J., Kim Y., Kang U.G., Park J., Kim Y.S. Region-specific phosphorylation of ERK5-MEF2C in the rat frontal cortex and hippocampus after electroconvulsive shock. Prog. Neuropsychopharmacol. Biol. Psychiatry 2005, 29:749-753.
55. Yue F., Zeng S., Wu D., Yi D., Zhang Y.A., Chan P. Age-related decline in motor behavior and striatal dopamine transporter in cynomolgus monkeys. J.Neural Transm 2012, 119:943-952.
56. Yurek D.M., Fletcher-Turner A. Differential expression of GDNF, BDNF, and NT-3 in the aging nigrostriatal system following a neurotoxic lesion. Brain Res. 2001, 891:228-235.
57. Yurek D.M., Hipkens S.B., Hebert M.A., Gash D.M., Gerhardt G.A. Age-related decline in striatal dopamine release and motoric function in brown Norway/Fischer 344 hybrid rats. Brain Res. 1998, 791:246-256.
58. Zou J., Pan Y.W., Wang Z., Chang S.Y., Wang W., Wang X., Tournier C., Storm D.R., Xia Z. Targeted deletion of ERK5 MAP kinase in the developing nervous system impairs development of GABAergic interneurons in the main olfactory bulb and behavioral discrimination between structurally similar odorants. J.Neurosci. 2012, 32:4118-4132.