Skip to main content
Log in

Linking Stress, Catecholamine Autotoxicity, and Allostatic Load with Neurodegenerative Diseases: A Focused Review in Memory of Richard Kvetnansky

  • Review Paper
  • Published:
Cellular and Molecular Neurobiology Aims and scope Submit manuscript

Abstract

In this Focused Review, we provide an update about evolving concepts that may link chronic stress and catecholamine autotoxicity with neurodegenerative diseases such as Parkinson’s disease. Richard Kvetnansky’s contributions to the field of stress and catecholamine systems inspired some of the ideas presented here. We propose that coordination of catecholaminergic systems mediates adjustments maintaining health and that senescence-related disintegration of these systems leads to disorders of regulation and to neurodegenerative diseases such as Parkinson’s disease. Chronically repeated episodes of stress-related catecholamine release and reuptake, with attendant increases in formation of the toxic dopamine metabolite 3,4-dihydroxyphenylacetaldehyde, might accelerate this process.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Acosta SA, Tajiri N, de la Pena I, Bastawrous M, Sanberg PR, Kaneko Y, Borlongan CV (2015) Alpha-synuclein as a pathological link between chronic traumatic brain injury and Parkinson’s disease. J Cell Physiol 230(5):1024–1032. doi:10.1002/jcp.24830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson DG, Florang VR, Schamp JH, Buettner GR, Doorn JA (2016) Antioxidant-mediated modulation of protein reactivity for 3,4-dihydroxyphenylacetaldehyde, a toxic dopamine metabolite. Chem Res Toxicol 29(7):1098–1107. doi:10.1021/acs.chemrestox.5b00528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Axelrod J, Kopin IJ (1969) The uptake, storage, release and metabolism of noradrenaline in sympathetic nerves. Prog Brain Res 31:21–32

    Article  CAS  PubMed  Google Scholar 

  • Betarbet R, Sherer TB, MacKenzie G, Garcia-Osuna M, Panov AV, Greenamyre JT (2000) Chronic systemic pesticide exposure reproduces features of Parkinson’s disease. Nat Neurosci 3(12):1301–1306

    Article  CAS  PubMed  Google Scholar 

  • Bezard E, Jaber M, Gonon F, Boireau A, Bloch B, Gross CE (2000) Adaptive changes in the nigrostriatal pathway in response to increased 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced neurodegeneration in the mouse. Eur J Neurosci 12(8):2892–2900

    Article  CAS  PubMed  Google Scholar 

  • Bisaglia M, Mammi S, Bubacco L (2007) Kinetic and structural analysis of the early oxidation products of dopamine: analysis of the interactions with alpha-synuclein. J Biol Chem 282(21):15597–15605. doi:10.1074/jbc.M610893200

    Article  CAS  PubMed  Google Scholar 

  • Brimijoin S, Molinoff PB (1971) Effects of 6-hydroxydopamine on the activity of tyrosine hydroxylase and dopamine-beta -hydroxylase in sympathetic ganglia of the rat. J Pharmacol Exp Ther 178(3):417–424

    CAS  PubMed  Google Scholar 

  • Bronstein J, Carvey P, Chen H, Cory-Slechta D, DiMonte D, Duda J, English P, Goldman S, Grate S, Hansen J, Hoppin J, Jewell S, Kamel F, Koroshetz W, Langston JW, Logroscino G, Nelson L, Ravina B, Rocca W, Ross GW, Schettler T, Schwarzschild M, Scott B, Seegal R, Singleton A, Steenland K, Tanner CM, Van Den Eeden S, Weisskopf M (2009) Meeting report: consensus statement-Parkinson’s disease and the environment: collaborative on health and the environment and Parkinson’s Action Network (CHE PAN) conference 26-28 June 2007. Environ Health Perspect 117(1):117–121. doi:10.1289/ehp.11702

    Article  PubMed  Google Scholar 

  • Burke WJ, Li SW, Williams EA, Nonneman R, Zahm DS (2003) 3,4-Dihydroxyphenylacetaldehyde is the toxic dopamine metabolite in vivo: implications for Parkinson’s disease pathogenesis. Brain Res 989(2):205–213

    Article  CAS  PubMed  Google Scholar 

  • Burke WJ, Kumar VB, Pandey N, Panneton WM, Gan Q, Franko MW, O’Dell M, Li SW, Pan Y, Chung HD, Galvin JE (2008) Aggregation of alpha-synuclein by DOPAL, the monoamine oxidase metabolite of dopamine. Acta Neuropathol 115(2):193–203. doi:10.1007/s00401-007-0303-9

    Article  CAS  PubMed  Google Scholar 

  • Cai H, Liu G, Sun L, Ding J (2014) Aldehyde Dehydrogenase 1 making molecular inroads into the differential vulnerability of nigrostriatal dopaminergic neuron subtypes in Parkinson’s disease. Transl Neurodegener 3:27. doi:10.1186/2047-9158-3-27

    Article  PubMed  PubMed Central  Google Scholar 

  • Cannon WB (1929) Organization for physiological homeostasis. Physiol Rev 9:399–431

    Article  Google Scholar 

  • Cannon WB (1939) The wisdom of the body. W.W. Norton, New York

    Google Scholar 

  • Caudle WM, Richardson JR, Wang MZ, Taylor TN, Guillot TS, McCormack AL, Colebrooke RE, Di Monte DA, Emson PC, Miller GW (2007) Reduced vesicular storage of dopamine causes progressive nigrostriatal neurodegeneration. J Neurosci 27(30):8138–8148. doi:10.1523/JNEUROSCI.0319-07.2007

    Article  CAS  PubMed  Google Scholar 

  • Chase A (2015) Parkinson disease: traumatic brain injury increases the risk of Parkinson disease. Nat Rev Neurol 11(4):184. doi:10.1038/nrneurol.2015.39

    Article  PubMed  Google Scholar 

  • Chiu CC, Yeh TH, Lai SC, Wu-Chou YH, Chen CH, Mochly-Rosen D, Huang YC, Chen YJ, Chen CL, Chang YM, Wang HL, Lu CS (2015) Neuroprotective effects of aldehyde dehydrogenase 2 activation in rotenone-induced cellular and animal models of parkinsonism. Exp Neurol 263:244–253. doi:10.1016/j.expneurol.2014.09.016

    Article  CAS  PubMed  Google Scholar 

  • Chu Y, Morfini GA, Langhamer LB, He Y, Brady ST, Kordower JH (2012) Alterations in axonal transport motor proteins in sporadic and experimental Parkinson’s disease. Brain 135(Pt 7):2058–2073. doi:10.1093/brain/aws133

    Article  PubMed  PubMed Central  Google Scholar 

  • Crane PK, Gibbons LE, Dams-O’Connor K, Trittschuh E, Leverenz JB, Keene CD, Sonnen J, Montine TJ, Bennett DA, Leurgans S, Schneider JA, Larson EB (2016) Association of traumatic brain injury with late-life neurodegenerative conditions and neuropathologic findings. JAMA Neurol 73(9):1062–1069. doi:10.1001/jamaneurol.2016.1948

    Article  PubMed  PubMed Central  Google Scholar 

  • Cubells JF, Baker H, Volpe BT, Smith GP, Das SS, Joh TH (1995) Innervation-independent changes in the mRNAs encoding tyrosine hydroxylase and the norepinephrine transporter in rat adrenal medulla after high-dose reserpine. Neurosci Lett 193:189–192

    Article  CAS  PubMed  Google Scholar 

  • Djamshidian A, Lees AJ (2014) Can stress trigger Parkinson’s disease? J Neurol Neurosurg Psychiatry 85(8):878–881. doi:10.1136/jnnp-2013-305911

    Article  PubMed  Google Scholar 

  • Dronjak S, Jezova D, Kvetnansky R (2004) Different effects of novel stressors on sympathoadrenal system activation in rats exposed to long-term immobilization. Ann N Y Acad Sci 1018:113–123. doi:10.1196/annals.1296.013

    Article  CAS  PubMed  Google Scholar 

  • Fitzmaurice AG, Rhodes SL, Lulla A, Murphy NP, Lam HA, O’Donnell KC, Barnhill L, Casida JE, Cockburn M, Sagasti A, Stahl MC, Maidment NT, Ritz B, Bronstein JM (2013) Aldehyde dehydrogenase inhibition as a pathogenic mechanism in Parkinson disease. Proc Natl Acad Sci USA 110(2):636–641. doi:10.1073/pnas.1220399110

    Article  CAS  PubMed  Google Scholar 

  • Florang VR, Rees JN, Brogden NK, Anderson DG, Hurley TD, Doorn JA (2007) Inhibition of the oxidative metabolism of 3,4-dihydroxyphenylacetaldehyde, a reactive intermediate of dopamine metabolism, by 4-hydroxy-2-nonenal. Neurotoxicology 28(1):76–82. doi:10.1016/j.neuro.2006.07.018

    Article  CAS  PubMed  Google Scholar 

  • Folkow B (1990) “Structural factor” in primary and secondary hypertension. Hypertension 16(1):89–101

    Article  CAS  PubMed  Google Scholar 

  • Follmer C, Coelho-Cerqueira E, Yatabe-Franco DY, Araujo GD, Pinheiro AS, Domont GB, Eliezer D (2015) Oligomerization and membrane-binding properties of covalent adducts formed by the interaction of alpha-synuclein with the toxic dopamine metabolite 3,4-dihydroxyphenylacetaldehyde (DOPAL). J Biol Chem 290(46):27660–27679. doi:10.1074/jbc.M115.686584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fornstedt B, Rosengren E, Carlsson A (1986) Occurrence and distribution of 5-S-cysteinyl derivatives of dopamine, dopa and dopac in the brains of eight mammalian species. Neuropharmacology 25(4):451–454

    Article  CAS  PubMed  Google Scholar 

  • Frank SM, Raja SN, Bulcao C, Goldstein DS (2000) Age-related thermoregulatory differences during core cooling in humans. Am J Physiol 279(1):R349–R354

    CAS  Google Scholar 

  • Fumagalli F, Gainetdinov RR, Wang YM, Valenzano KJ, Miller GW, Caron MG (1999) Increased methamphetamine neurotoxicity in heterozygous vesicular monoamine transporter 2 knock-out mice. J Neurosci 19(7):2424–2431

    CAS  PubMed  Google Scholar 

  • Gardner RC, Burke JF, Nettiksimmons J, Goldman S, Tanner CM, Yaffe K (2015) Traumatic brain injury in later life increases risk for Parkinson disease. Ann Neurol 77(6):987–995. doi:10.1002/ana.24396

    Article  PubMed  PubMed Central  Google Scholar 

  • Gaugler MN, Genc O, Bobela W, Mohanna S, Ardah MT, El-Agnaf OM, Cantoni M, Bensadoun JC, Schneggenburger R, Knott GW, Aebischer P, Schneider BL (2012) Nigrostriatal overabundance of alpha-synuclein leads to decreased vesicle density and deficits in dopamine release that correlate with reduced motor activity. Acta Neuropathol 123(5):653–669. doi:10.1007/s00401-012-0963-y

    Article  CAS  PubMed  Google Scholar 

  • German DC, Liang CL, Manaye KF, Lane K, Sonsalla PK (2000) Pharmacological inactivation of the vesicular monoamine transporter can enhance 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced neurodegeneration of midbrain dopaminergic neurons, but not locus coeruleus noradrenergic neurons. Neuroscience 101(4):1063–1069

    Article  CAS  PubMed  Google Scholar 

  • Goldstein DS (2006) Adrenaline and the inner world: an introduction to scientific integrative medicine. The Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Goldstein DS (2011) Stress, allostatic load, catecholamines, and other neurotransmitters in neurodegenerative diseases. Endocr Regul 45(2):91–98

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goldstein DS (2012) Stress, allostatic load, catecholamines, and other neurotransmitters in neurodegenerative diseases. Cell Mol Neurobiol 32(5):661–666. doi:10.1007/s10571-011-9780-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goldstein DS (2013) Concepts of scientific integrative medicine applied to the physiology and pathophysiology of catecholamine systems. Compr Physiol 3:1569–1610

    Article  PubMed  PubMed Central  Google Scholar 

  • Goldstein DS, Li ST, Kopin IJ (2001) Sympathetic neurocirculatory failure in Parkinson disease: evidence for an etiologic role of alpha-synuclein. Ann Intern Med 135(11):1010–1011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goldstein DS, Holmes C, Patronas N, Kopin IJ (2003a) Cerebrospinal fluid levels of catechols in patients with neurogenic orthostatic hypotension. Clin Sci 104(6):649–654. doi:10.1042/CS20020315

    Article  CAS  PubMed  Google Scholar 

  • Goldstein DS, Holmes C, Sharabi Y, Brentzel S, Eisenhofer G (2003b) Plasma levels of catechols and metanephrines in neurogenic orthostatic hypotension. Neurology 60(8):1327–1332

    Article  CAS  PubMed  Google Scholar 

  • Goldstein DS, Holmes C, Kopin IJ, Sharabi Y (2011a) Intra-neuronal vesicular uptake of catecholamines is decreased in patients with Lewy body diseases. J Clin Inv 121:3320–3330

    Article  CAS  Google Scholar 

  • Goldstein DS, Sullivan P, Holmes C, Kopin IJ, Basile MJ, Mash DC (2011b) Catechols in post-mortem brain of patients with Parkinson disease. Eur J Neurol 18:703–710. doi:10.1111/j.1468-1331.2010.03246.x

    Article  CAS  PubMed  Google Scholar 

  • Goldstein DS, Sullivan P, Cooney A, Jinsmaa Y, Sullivan R, Gross DJ, Holmes C, Kopin IJ, Sharabi Y (2012) Vesicular uptake blockade generates the toxic dopamine metabolite 3,4-dihydroxyphenylacetaldehyde in PC12 Cells: relevance to the pathogenesis of Parkinson disease. J Neurochem 123(6):932–943. doi:10.1111/j.1471-4159.2012.07924.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goldstein DS, Sullivan P, Holmes C, Miller GW, Alter S, Strong R, Mash DC, Kopin IJ, Sharabi Y (2013) Determinants of buildup of the toxic dopamine metabolite DOPAL in Parkinson’s disease. J Neurochem 126(5):591–603. doi:10.1111/jnc.12345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goldstein DS, Kopin IJ, Sharabi Y (2014a) Catecholamine autotoxicity. Implications for pharmacology and therapeutics of Parkinson disease and related disorders. Pharmacol Ther 144(3):268–282. doi:10.1016/j.pharmthera.2014.06.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goldstein DS, Sullivan P, Holmes C, Miller GW, Sharabi Y, Kopin IJ (2014b) A vesicular sequestration to oxidative deamination shift in myocardial sympathetic nerves in Parkinson disease. J Neurochem 131:219–228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goldstein DS, Holmes C, Sullivan P, Mash DC, Sidransky E, Stefani A, Kopin IJ, Sharabi Y (2015a) Deficient vesicular storage: a common theme in catecholaminergic neurodegeneration. Parkinsonism Relat Disord 21(9):1013–1022. doi:10.1016/j.parkreldis.2015.07.009

    Article  PubMed  PubMed Central  Google Scholar 

  • Goldstein DS, Sullivan P, Cooney A, Jinsmaa Y, Kopin IJ, Sharabi Y (2015b) Rotenone decreases intracellular aldehyde dehydrogenase activity: implications for the pathogenesis of Parkinson’s disease. J Neurochem 133(1):14–25. doi:10.1111/jnc.13042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goldstein DS, Sullivan P, Holmes C, Kopin IJ, Sharabi Y, Mash DC (2015c) Decreased vesicular storage and aldehyde dehydrogenase activity in multiple system atrophy. Parkinsonism Relat Disord 21(6):567–572. doi:10.1016/j.parkreldis.2015.03.006

    Article  PubMed  PubMed Central  Google Scholar 

  • Goldstein DS, Jinsmaa Y, Sullivan P, Holmes C, Kopin IJ, Sharabi Y (2016) Comparison of monoamine oxidase inhibitors in decreasing production of the autotoxic dopamine metabolite 3,4-dihydroxyphenylacetaldehyde in PC12 cells. J Pharmacol Exp Ther 356(2):484–493. doi:10.1124/jpet.115.230201

    Article  CAS  Google Scholar 

  • Goldstein DS, Sullivan P, Holmes C, Mash DC, Kopin IJ, Sharabi Y (2017) Determinants of denervation-independent depletion of putamen dopamine in Parkinson’s disease and multiple system atrophy. Parkinsonism Relat Disord 35:88–91. doi:10.1016/j.parkreldis.2016.12.011

    Article  PubMed  Google Scholar 

  • Grunblatt E, Riederer P (2014) Aldehyde dehydrogenase (ALDH) in Alzheimer’s and Parkinson’s disease. J Neural Transm. doi:10.1007/s00702-014-1320-1

    Google Scholar 

  • Grunblatt E, Riederer P (2016) Aldehyde dehydrogenase (ALDH) in Alzheimer’s and Parkinson’s disease. J Neural Transm 123(2):83–90. doi:10.1007/s00702-014-1320-1

    Article  CAS  PubMed  Google Scholar 

  • Guillot TS, Miller GW (2009) Protective actions of the vesicular monoamine transporter 2 (VMAT2) in monoaminergic neurons. Mol Neurobiol 39(2):149–170. doi:10.1007/s12035-009-8059-y

    Article  CAS  PubMed  Google Scholar 

  • Guillot TS, Shepherd KR, Richardson JR, Wang MZ, Li Y, Emson PC, Miller GW (2008) Reduced vesicular storage of dopamine exacerbates methamphetamine-induced neurodegeneration and astrogliosis. J Neurochem 106(5):2205–2217. doi:10.1111/j.1471-4159.2008.05568.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo JT, Chen AQ, Kong Q, Zhu H, Ma CM, Qin C (2008) Inhibition of vesicular monoamine transporter-2 activity in alpha-synuclein stably transfected SH-SY5Y cells. Cell Mol Neurobiol 28(1):35–47. doi:10.1007/s10571-007-9227-0

    Article  CAS  PubMed  Google Scholar 

  • Herrera A, Munoz P, Steinbusch HW, Segura-Aguilar J (2017) Are dopamine oxidation metabolites involved in the loss of dopaminergic neurons in the nigrostriatal system in Parkinson’s disease? ACS Chem Neurosci. doi:10.1021/acschemneuro.7b00034

    PubMed  Google Scholar 

  • Hertting G, Axelrod J (1961) Fate of tritiated noradrenaline at sympathetic nerve endings. Nature 192:172–173

    Article  CAS  PubMed  Google Scholar 

  • Holz RW (1978) Evidence that catecholamine transport into chromaffin vesicles is coupled to vesicle membrane potential. Proc Natl Acad Sci USA 75(10):5190–5194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Impellizzeri D, Campolo M, Bruschetta G, Crupi R, Cordaro M, Paterniti I, Cuzzocrea S, Esposito E (2016) Traumatic brain injury leads to development of Parkinson’s disease related pathology in mice. Front Neurosci 10:458. doi:10.3389/fnins.2016.00458

    Article  PubMed  PubMed Central  Google Scholar 

  • Isingrini E, Perret L, Rainer Q, Sagueby S, Moquin L, Gratton A, Giros B (2016) Selective genetic disruption of dopaminergic, serotonergic and noradrenergic neurotransmission: insights into motor, emotional and addictive behaviour. J Psychiatry Neurosci 41(3):169–181

    Article  PubMed  Google Scholar 

  • Ito S, Nakaso K, Imamura K, Takeshima T, Nakashima K (2010) Endogenous catecholamine enhances the dysfunction of unfolded protein response and alpha-synuclein oligomerization in PC12 cells overexpressing human alpha-synuclein. Neurosci Res 66(1):124–130. doi:10.1016/j.neures.2009.10.005

    Article  CAS  PubMed  Google Scholar 

  • Jafari S, Etminan M, Aminzadeh F, Samii A (2013) Head injury and risk of Parkinson disease: a systematic review and meta-analysis. Mov Disord 28(9):1222–1229. doi:10.1002/mds.25458

    Article  PubMed  Google Scholar 

  • Janakiraman U, Manivasagam T, Justin Thenmozhi A, Dhanalakshmi C, Essa MM, Song BJ, Guillemin GJ (2017) Chronic mild stress augments MPTP induced neurotoxicity in a murine model of Parkinson’s disease. Physiol Behav 173:132–143. doi:10.1016/j.physbeh.2017.01.046

    Article  CAS  PubMed  Google Scholar 

  • Kish SJ, Shannak K, Hornykiewicz O (1988) Uneven pattern of dopamine loss in the striatum of patients with idiopathic Parkinson’s disease. Pathophysiologic and clinical implications. N Engl J Med 318:876–880

    Article  CAS  PubMed  Google Scholar 

  • Koeslag JH, Saunders PT, Terblanche E (2003) A reappraisal of the blood glucose homeostat which comprehensively explains the type 2 diabetes mellitus–syndrome X complex. J Physiol 549:333–346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kvetnansky R (2004) Stressor specificity and effect of prior experience on catecholamine biosynthetic enzyme phenylethanolamine N-methyltransferase. Ann N Y Acad Sci 1032:117–129. doi:10.1196/annals.1314.009

    Article  CAS  PubMed  Google Scholar 

  • Kvetnansky R, Mikulaj L (1970) Adrenal and urinary catecholamines in rat during adaptation to repeated immobilization stress. Endocrinology 87:738–743

    Article  CAS  PubMed  Google Scholar 

  • Kvetnansky R, Weise VK, Kopin IJ (1970) Elevation of adrenal tyrosine hydroxylase and phenylethanolamine-N-methyl transferase by repeated immobilization of rats. Endocrinology 87:744–749

    Article  CAS  PubMed  Google Scholar 

  • Kvetnansky R, Gewirtz GP, Weise VK, Kopin IJ (1971a) Enhanced synthesis of adrenal dopamine beta-hydroxylase induced by repeated immobilization in rats. Mol Pharmacol 7:81–86

    CAS  PubMed  Google Scholar 

  • Kvetnansky R, Weise VK, Gewirtz GP, Kopin IJ (1971b) Synthesis of adrenal catecholamines in rats during and after immobilization stress. Endocrinology 89:46–49

    Article  CAS  PubMed  Google Scholar 

  • Kvetnansky R, Sun CL, Lake CR, Thoa N, Torda T, Kopin IJ (1978) Effect of handling and forced immobilization on rat plasma levels of epinephrine, norepinephrine, and dopamine-beta-hydroxylase. Endocrinology 103(5):1868–1874

    Article  CAS  PubMed  Google Scholar 

  • Kvetnansky R, Armando I, Weise VK, Holmes C, Fukuhara K, Deka-Starosta A, Kopin IJ, Goldstein DS (1992a) Plasma dopa responses during stress: dependence on sympathoneural activity and tyrosine hydroxylation. J Pharmacol Exp Ther 261(3):899–909

    CAS  PubMed  Google Scholar 

  • Kvetnansky R, Goldstein DS, Weise VK, Holmes C, Szemeredi K, Bagdy G, Kopin IJ (1992b) Effects of handling or immobilization on plasma levels of 3,4-dihydroxyphenylalanine, catecholamines, and metabolites in rats. J Neurochem 58(6):2296–2302

    Article  CAS  PubMed  Google Scholar 

  • Kvetnansky R, Fukuhara K, Pacak K, Cizza G, Goldstein DS, Kopin IJ (1993) Endogenous glucocorticoids restrain catecholamine synthesis and release at rest and during immobilization stress in rats. Endocrinology 133:1411–1419

    Article  CAS  PubMed  Google Scholar 

  • Kvetnansky R, Pacak K, Fukuhara K, Viskupic E, Hiremagalur B, Nankova B, Goldstein DS, Sabban EL, Kopin IJ (1995) Sympathoadrenal system in stress. Interaction with the hypothalamic-pituitary-adrenocortical system. Ann N Y Acad Sci 771:131–158

    Article  CAS  PubMed  Google Scholar 

  • Kvetnansky R, Pacak K, Sabban EL, Kopin IJ, Goldstein DS (1998) Stressor specificity of peripheral catecholaminergic activation. Adv Pharmacol 42:556–560

    Article  CAS  PubMed  Google Scholar 

  • Kvetnansky R, Sabban EL, Palkovits M (2009) Catecholaminergic systems in stress: structural and molecular genetic approaches. Physiol Rev 89(2):535–606. doi:10.1152/physrev.00042.2006

    Article  CAS  PubMed  Google Scholar 

  • Lamensdorf I, Eisenhofer G, Harvey-White J, Hayakawa Y, Kirk K, Kopin IJ (2000a) Metabolic stress in PC12 cells induces the formation of the endogenous dopaminergic neurotoxin, 3,4-dihydroxyphenylacetaldehyde. J Neurosci Res 60(4):552–558

    Article  CAS  PubMed  Google Scholar 

  • Lamensdorf I, Eisenhofer G, Harvey-White J, Nechustan A, Kirk K, Kopin IJ (2000b) 3,4-Dihydroxyphenylacetaldehyde potentiates the toxic effects of metabolic stress in PC12 cells. Brain Res 868(2):191–201

    Article  CAS  PubMed  Google Scholar 

  • Li SW, Lin TS, Minteer S, Burke WJ (2001) 3,4-Dihydroxyphenylacetaldehyde and hydrogen peroxide generate a hydroxyl radical: possible role in Parkinson’s disease pathogenesis. Brain Res Mol Brain Res 93(1):1–7

    Article  CAS  PubMed  Google Scholar 

  • Lohr KM, Stout KA, Dunn AR, Wang M, Salahpour A, Guillot TS, Miller GW (2015) Increased vesicular monoamine transporter 2 (VMAT2; Slc18a2) protects against methamphetamine toxicity. ACS Chem Neurosci 6(5):790–799. doi:10.1021/acschemneuro.5b00010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lotharius J, Barg S, Wiekop P, Lundberg C, Raymon HK, Brundin P (2002) Effect of mutant alpha-synuclein on dopamine homeostasis in a new human mesencephalic cell line. J Biol Chem 277(41):38884–38894

    Article  CAS  PubMed  Google Scholar 

  • Lundblad M, Decressac M, Mattsson B, Bjorklund A (2012) Impaired neurotransmission caused by overexpression of alpha-synuclein in nigral dopamine neurons. Proc Natl Acad Sci USA 109(9):3213–3219. doi:10.1073/pnas.1200575109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma S, Mifflin SW, Cunningham JT, Morilak DA (2008) Chronic intermittent hypoxia sensitizes acute hypothalamic-pituitary-adrenal stress reactivity and Fos induction in the rat locus coeruleus in response to subsequent immobilization stress. Neuroscience 154(4):1639–1647. doi:10.1016/j.neuroscience.2008.04.068

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marchitti SA, Deitrich RA, Vasiliou V (2007) Neurotoxicity and metabolism of the catecholamine-derived 3,4-dihydroxyphenylacetaldehyde and 3,4-dihydroxyphenylglycolaldehyde: the role of aldehyde dehydrogenase. Pharmacol Rev 59:125–150

    Article  CAS  PubMed  Google Scholar 

  • Mazzulli JR, Mishizen AJ, Giasson BI, Lynch DR, Thomas SA, Nakashima A, Nagatsu T, Ota A, Ischiropoulos H (2006) Cytosolic catechols inhibit alpha-synuclein aggregation and facilitate the formation of intracellular soluble oligomeric intermediates. J Neurosci 26(39):10068–10078. doi:10.1523/JNEUROSCI.0896-06.2006

    Article  CAS  PubMed  Google Scholar 

  • Modell H, Cliff W, Michael J, McFarland J, Wenderoth MP, Wright A (2015) A physiologist’s view of homeostasis. Adv Physiol Educ 39:259–266

    Article  PubMed  PubMed Central  Google Scholar 

  • Mooslehner KA, Chan PM, Xu W, Liu L, Smadja C, Humby T, Allen ND, Wilkinson LS, Emson PC (2001) Mice with very low expression of the vesicular monoamine transporter 2 gene survive into adulthood: potential mouse model for parkinsonism. Mol Cell Biol 21(16):5321–5331. doi:10.1128/MCB.21.16.5321-5331.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morgan DG, Marcusson JO, Nyberg P, Wester P, Winblad B, Gordon MN, Finch CE (1987) Divergent changes in D-1 and D-2 dopamine binding sites in human brain during aging. Neurobiol Aging 8(3):195–201

    Article  CAS  PubMed  Google Scholar 

  • Mosharov EV, Staal RG, Bove J, Prou D, Hananiya A, Markov D, Poulsen N, Larsen KE, Moore CM, Troyer MD, Edwards RH, Przedborski S, Sulzer D (2006) Alpha-synuclein overexpression increases cytosolic catecholamine concentration. J Neurosci 26(36):9304–9311. doi:10.1523/JNEUROSCI.0519-06.2006

    Article  CAS  PubMed  Google Scholar 

  • Pacak K, Armando I, Fukuhara K, Kvetnansky R, Palkovits M, Kopin IJ, Goldstein DS (1992) Noradrenergic activation in the paraventricular nucleus during acute and chronic immobilization stress in rats: an in vivo microdialysis study. Brain Res 589:91–96

    Article  CAS  PubMed  Google Scholar 

  • Pacak K, Kvetnansky R, Palkovits M, Fukuhara K, Yadid G, Kopin IJ, Goldstein DS (1993a) Adrenalectomy augments in vivo release of norepinephrine in the paraventricular nucleus during immobilization stress. Endocrinology 133:1404–1410

    Article  CAS  PubMed  Google Scholar 

  • Pacak K, Palkovits M, Kvetnansky R, Fukuhara K, Armando I, Kopin IJ, Goldstein DS (1993b) Effects of single or repeated immobilization on release of norepinephrine and its metabolites in the central nucleus of the amygdala in conscious rats. Neuroendocrinology 57:626–633

    Article  CAS  PubMed  Google Scholar 

  • Pacak K, Baffi JS, Kvetnansky R, Goldstein DS, Palkovits M (1998a) Stressor-specific activation of catecholaminergic systems: implications for stress-related hypothalamic-pituitary-adrenocortical responses. Adv Pharmacol 42:561–564

    Article  CAS  PubMed  Google Scholar 

  • Pacak K, Palkovits M, Yadid G, Kvetnansky R, Kopin IJ, Goldstein DS (1998b) Heterogeneous neurochemical responses to different stressors: a test of Selye’s doctrine of nonspecificity. Am J Physiol 275:R1247–R1255

    Article  CAS  PubMed  Google Scholar 

  • Panneton WM, Kumar VB, Gan Q, Burke WJ, Galvin JE (2010) The neurotoxicity of DOPAL: behavioral and stereological evidence for its role in Parkinson disease pathogenesis. PLoS One 5(12):e15251. doi:10.1371/journal.pone.0015251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Picard M, Juster RP, McEwen BS (2014) Mitochondrial allostatic load puts the ‘gluc’ back in glucocorticoids. Nat Rev Endocrinol 10(5):303–310. doi:10.1038/nrendo.2014.22

    Article  CAS  PubMed  Google Scholar 

  • Pifl C, Rajput A, Reither H, Blesa J, Cavada C, Obeso JA, Rajput AH, Hornykiewicz O (2014) Is Parkinson’s disease a vesicular dopamine storage disorder? Evidence from a study in isolated synaptic vesicles of human and nonhuman primate striatum. J Neurosci 34(24):8210–8218. doi:10.1523/JNEUROSCI.5456-13.2014

    Article  PubMed  CAS  Google Scholar 

  • Plotegher N, Berti G, Ferrari E, Tessari I, Zanetti M, Lunelli L, Greggio E, Bisaglia M, Veronesi M, Girotto S, Dalla Serra M, Perego C, Casella L, Bubacco L (2017) DOPAL derived alpha-synuclein oligomers impair synaptic vesicles physiological function. Sci Rep 7:40699. doi:10.1038/srep40699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Polymeropoulos MH, Lavedan C, Leroy E, Ide SE, Dehejia A, Dutra A, Pike B, Root H, Rubenstein J, Boyer R, Stenroos ES, Chandrasekharappa S, Athanassiadou A, Papapetropoulos T, Johnson WG, Lazzarini AM, Duvoisin RC, Di Iorio G, Golbe LI, Nussbaum RL (1997) Mutation in the alpha-synuclein gene identified in families with Parkinson’s disease. Science 276:2045–2047

    Article  CAS  PubMed  Google Scholar 

  • Rilstone JJ, Alkhater RA, Minassian BA (2013) Brain dopamine-serotonin vesicular transport disease and its treatment. N Engl J Med 368(6):543–550. doi:10.1056/NEJMoa1207281

    Article  CAS  PubMed  Google Scholar 

  • Sai Y, Wu Q, Le W, Ye F, Li Y, Dong Z (2008) Rotenone-induced PC12 cell toxicity is caused by oxidative stress resulting from altered dopamine metabolism. Toxicol In Vitr 22(6):1461–1468. doi:10.1016/j.tiv.2008.04.019

    Article  CAS  Google Scholar 

  • Selye H (1936) A syndrome produced by diverse nocuous agents. Nature 138:32

    Article  Google Scholar 

  • Selye H (1950) The physiology and pathology of exposure to stress. A treatise based on the concepts of the general-adaptation syndrome and the diseases of adaptation. Acta, Inc., Montreal

    Google Scholar 

  • Selye H (1956) The stress of life. McGraw-Hill, New York

    Google Scholar 

  • Selye H (1974) Stress without distress. New American Library, New York

    Google Scholar 

  • Selye H (1976) Stress without distress. Psychopathology of human adaptation. Springer, New York

    Google Scholar 

  • Sherer TB, Kim JH, Betarbet R, Greenamyre JT (2003) Subcutaneous rotenone exposure causes highly selective dopaminergic degeneration and alpha-synuclein aggregation. Exp Neurol 179(1):9–16

    Article  CAS  PubMed  Google Scholar 

  • Singleton AB, Farrer M, Johnson J, Singleton A, Hague S, Kachergus J, Hulihan M, Peuralinna T, Dutra A, Nussbaum R, Lincoln S, Crawley A, Hanson M, Maraganore D, Adler C, Cookson MR, Muenter M, Baptista M, Miller D, Blancato J, Hardy J, Gwinn-Hardy K (2003) α-Synuclein locus triplication causes Parkinson’s disease. Science 302(5646):841

    Article  CAS  PubMed  Google Scholar 

  • Singleton A, Gwinn-Hardy K, Sharabi Y, Li ST, Holmes C, Dendi R, Hardy J, Crawley A, Goldstein DS (2004) Association between cardiac denervation and parkinsonism caused by alpha-synuclein gene triplication. Brain 127(Pt 4):768–772

    Article  PubMed  Google Scholar 

  • Snyder GL, Keller RW Jr, Zigmond MJ (1990) Dopamine efflux from striatal slices after intracerebral 6-hydroxydopamine: evidence for compensatory hyperactivity of residual terminals. J Pharmacol Exp Ther 253(2):867–876

    CAS  PubMed  Google Scholar 

  • Spencer JP, Whiteman M, Jenner P, Halliwell B (2002) 5-s-Cysteinyl-conjugates of catecholamines induce cell damage, extensive DNA base modification and increases in caspase-3 activity in neurons. J Neurochem 81(1):122–129

    Article  CAS  PubMed  Google Scholar 

  • Spillantini MG, Schmidt ML, Lee VM, Trojanowski JQ, Jakes R, Goedert M (1997) Alpha-synuclein in Lewy bodies. Nature 388(6645):839–840. doi:10.1038/42166

    Article  CAS  PubMed  Google Scholar 

  • Staal RG, Sonsalla PK (2000) Inhibition of brain vesicular monoamine transporter (VMAT2) enhances 1-methyl-4-phenylpyridinium neurotoxicity in vivo in rat striata. J Pharmacol Exp Ther 293(2):336–342

    CAS  PubMed  Google Scholar 

  • Sterling P, Eyer J (1988) Allostasis: a new paradigm to explain arousal pathology. In: Fisher J, Reason J (eds) Handbook of life stress, cognition, and health. Wiley, New York, pp 629–649

    Google Scholar 

  • Sugama S, Sekiyama K, Kodama T, Takamatsu Y, Takenouchi T, Hashimoto M, Bruno C, Kakinuma K (2016) Chronic restraint stress triggers dopaminergic and noradrenergic: possible role of chronic stress in the onset of Parkinson’s disease. Brain Behav Immun 51:39–46

    Article  CAS  PubMed  Google Scholar 

  • Sun M, Kong L, Wang X, Holmes C, Gao Q, Zhang GR, Pfeilschifter J, Goldstein DS, Geller AI (2004) Coexpression of tyrosine hydroxylase, GTP cyclohydrolase I, aromatic amino acid decarboxylase, and vesicular monoamine transporter 2 from a helper virus-free herpes simplex virus type 1 vector supports high-level, long-term biochemical and behavioral correction of a rat model of Parkinson’s disease. Hum Gene Ther 15(12):1177–1196. doi:10.1089/hum.2004.15.1177

    Article  PubMed  PubMed Central  Google Scholar 

  • Taylor TN, Alter SP, Wang M, Goldstein DS, Miller GW (2014) Reduced vesicular storage of catecholamines causes progressive degeneration in the locus ceruleus. Neuropharmacology 76(Pt A):97–105

    Article  CAS  PubMed  Google Scholar 

  • Verbalis JG, Baldwin EF, Robinson AG (1986) Osmotic regulation of plasma vasopressin and oxytocin after sustained hyponatremia. Am J Physiol 250(3 Pt 2):R444–R451

    CAS  PubMed  Google Scholar 

  • Vergo S, Johansen JL, Leist M, Lotharius J (2007) Vesicular monoamine transporter 2 regulates the sensitivity of rat dopaminergic neurons to disturbed cytosolic dopamine levels. Brain Res 1185:18–32. doi:10.1016/j.brainres.2007.09.028

    Article  CAS  PubMed  Google Scholar 

  • Wakabayashi K, Yoshimoto M, Tsuji S, Takahashi H (1998) Alpha-synuclein immunoreactivity in glial cytoplasmic inclusions in multiple system atrophy. Neurosci Lett 249(2–3):180–182

    Article  CAS  PubMed  Google Scholar 

  • Walsh MJ, Davis VE, Yamanaka Y (1970) Tetrahydropapaveroline: an alkaloid metabolite of dopamine in vitro. J Pharmacol Exp Ther 174:388–400

    CAS  PubMed  Google Scholar 

  • Watabe M, Nakaki T (2008) Mitochondrial complex I inhibitor rotenone inhibits and redistributes vesicular monoamine transporter 2 via nitration in human dopaminergic SH-SY5Y cells. Mol Pharmacol 74(4):933–940. doi:10.1124/mol.108.048546

    Article  CAS  PubMed  Google Scholar 

  • Werner CJ, Heyny-von Haussen R, Mall G, Wolf S (2008) Proteome analysis of human substantia nigra in Parkinson’s disease. Proteome Sci 6:8. doi:10.1186/1477-5956-6-8

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wey M, Fernandez E, Martinez PA, Sullivan P, Goldstein DS, Strong R (2012) Neurodegeneration and motor dysfunction in mice lacking cytosolic and mitochondrial aldehyde dehydrogenases: implications for Parkinson’s disease. PLoS One 7:e31522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williams GC (1957) Pleiotropy, natural selection, and the evolution of senescence. Evolution 11(4):398–411

    Article  Google Scholar 

  • Winner B, Jappelli R, Maji SK, Desplats PA, Boyer L, Aigner S, Hetzer C, Loher T, Vilar M, Campioni S, Tzitzilonis C, Soragni A, Jessberger S, Mira H, Consiglio A, Pham E, Masliah E, Gage FH, Riek R (2011) In vivo demonstration that alpha-synuclein oligomers are toxic. Proc Natl Acad Sci USA 108(10):4194–4199. doi:10.1073/pnas.1100976108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zarow C, Lyness SA, Mortimer JA, Chui HC (2003) Neuronal loss is greater in the locus coeruleus than nucleus basalis and substantia nigra in Alzheimer and Parkinson diseases. Arch Neurol 60:337–341

    Article  PubMed  Google Scholar 

Download references

Acknowledgement

The research reported here was supported (in part) by the Division of Intramural Research, NINDS.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David S. Goldstein.

Ethics declarations

Conflict of interest

The authors declare that they have no competing of interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Goldstein, D.S., Kopin, I.J. Linking Stress, Catecholamine Autotoxicity, and Allostatic Load with Neurodegenerative Diseases: A Focused Review in Memory of Richard Kvetnansky. Cell Mol Neurobiol 38, 13–24 (2018). https://doi.org/10.1007/s10571-017-0497-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10571-017-0497-x

Keywords

Navigation