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PMID: 16971520 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Blocking soluble tumor necrosis factor signaling with dominant-negative tumor necrosis factor inhibitor attenuates loss of dopaminergic neurons in models of Parkinson's disease.

McCoy MK, Martinez TN, Ruhn KA, Szymkowski DE, Smith CG, Botterman BR, Tansey KE, Tansey MG

Abstract

The mechanisms that trigger or contribute to loss of dopaminergic (DA) neurons in Parkinson's disease (PD) remain unclear and controversial. Elevated levels of tumor necrosis factor (TNF) in CSF and postmortem brains of PD patients and animal models of PD implicate this proinflammatory cytokine in the pathophysiology of the disease; but a role for TNF in mediating loss of DA neurons in PD has not been clearly demonstrated. Here, we report that neutralization of soluble TNF (solTNF) in vivo with the engineered dominant-negative TNF compound XENP345 (a PEGylated version of the TNF variant A145R/I97T) reduced by 50% the retrograde nigral degeneration induced by a striatal injection of the oxidative neurotoxin 6-hydroxydopamine (6-OHDA). XENP345 was neuroprotective only when infused into the nigra, not the striatum. XENP345/6-OHDA rats displayed attenuated amphetamine-induced rotational behavior, indicating preservation of striatal dopamine levels. Similar protective effects were observed with chronic in vivo coinfusion of XENP345 with bacterial lipopolysaccharide (LPS) into the substantia nigra, confirming a role for solTNF-dependent neuroinflammation in nigral degeneration. In embryonic rat midbrain neuron/glia cell cultures exposed to LPS, even delayed administration of XENP345 prevented selective degeneration of DA neurons despite sustained microglia activation and secretion of solTNF. XENP345 also attenuated 6-OHDA-induced DA neuron toxicity in vitro. Collectively, our data demonstrate a role for TNF in vitro and in vivo in two models of PD, and raise the possibility that delaying the progressive degeneration of the nigrostriatal pathway in humans is therapeutically feasible with agents capable of blocking solTNF in early stages of PD.

MeSH Terms
Amphetamine/pharmacology Animals Cell Death/drug effects,genetics Cells, Cultured Coculture Techniques Disease Models, Animal Dopamine/metabolism Female Gliosis/drug therapy,physiopathology,prevention & control Inflammation Mediators/antagonists & inhibitors Motor Activity/drug effects,physiology Nerve Degeneration/drug therapy,physiopathology,prevention & control Neurons/drug effects,metabolism,pathology Neurotoxins/antagonists & inhibitors Oxidopamine/antagonists & inhibitors Parkinsonian Disorders/drug therapy,metabolism,physiopathology Rats Rats, Inbred F344 Rats, Sprague-Dawley Signal Transduction/drug effects,genetics Substantia Nigra/drug effects,metabolism,physiopathology Treatment Outcome Tumor Necrosis Factor-alpha/antagonists & inhibitors,genetics,metabolism
Chemicals
Inflammation Mediators Neurotoxins Tumor Necrosis Factor-alpha Oxidopamine Amphetamine Dopamine
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
McCoy Melissa K
Department of Physiology, University of Texas Southwestern Medical Center, Dallas, Texas 75390, USA.
Martinez Terina N
Ruhn Kelly A
Szymkowski David E
Smith Christine G
Botterman Barry R
Tansey Keith E
Tansey Malú G
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Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2006-09-13
Pages
9365-75
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC3707118
Subset
IM
Grants
NINDS NIH HHS · R01 NS049433 · United States
NINDS NIH HHS · R01 NS049433-02 · United States
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