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Intrathecal Triamcinolone Acetonide Exerts Anti-Inflammatory Effects on Lewis Rat Experimental Autoimmune Neuritis and Direct An

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Intrathecal Triamcinolone Acetonide Exerts Anti-Inflammatory Effects on Lewis Rat Experimental Autoimmune Neuritis and Direct An Pitarokoili et al. Journal of Neuroinflammation (2019) 16:58 https://doi.org/10.1186/s12974-019-1445-0 RESEARCH Open Access Intrathecal triamcinolone acetonide exerts anti-inflammatory effects on Lewis rat experimental autoimmune neuritis and direct anti-oxidative effects on Schwann cells Kalliopi Pitarokoili*, Melissa Sgodzai, Thomas Grüter, Hussein Bachir, Jeremias Motte, Björn Ambrosius, Xiomara Pedreiturria, Min-Suk Yoon and Ralf Gold Abstract Background: Corticosteroids dominate in the treatment of chronic autoimmune neuropathies although long-term use is characterized by devastating side effects. Methods: We introduce the intrathecal application of the synthetic steroid triamcinolone (TRIAM) as a novel therapeutic option in experimental autoimmune neuritis in Lewis rats Results: After immunization with neuritogenic P2 peptide, we show a dose-dependent therapeutic effect of one intrathecal injection of 0.3 or 0.6 mg/kg TRIAM on clinical and electrophysiological parameters of neuritis with a lower degree of inflammatory infiltrates (T cells and macrophages) and demyelination in the sciatic nerve. In vitro studies in Schwann cell cultures showed an increased expression of IL-1 receptor antagonist and reduced expression of Toll-like receptor 4 after incubation with TRIAM as well as a protective effect of TRIAM against oxidative stress after H2O2 exposure. Conclusion: Intrathecal TRIAM application could be a novel immunomodulatory and potentially neuroprotective option for autoimmune neuropathies with a direct effect on Schwann cells. Keywords: Autoimmune neuropathies, Triamcinolone, Experimental autoimmune neuritis, Autoimmunity, Inflammation, Immunotherapy Introduction sustained release TRIAM (40–80 mg every other day for Triamcinolone acetonide (TRIAM) is an intermediate one to three injections) is performed since the 1970s in -acting synthetic glucocorticoid, which as a sustained-re- specialized centers in Germany for primary and second- lease crystal suspension is suitable for sub-lesional injec- ary progressive multiple sclerosis patients and improves, tions for isolated psoriasis or discoid lupus according to observational trials in up to 161 patients, erythematosus, intra-articular injections for the treat- the maximum walking distance, spasticity, and occupa- ment of chronic inflammatory joint diseases, and intra- tional deficits of the upper extremities [3–9]. Three vitreal applications as it reduces macular edema and months after repeated application of TRIAM in the cere- angiogenesis in eyes with artificial lenses [1, 2]. brospinal fluid (CSF), an elevated steroid level could still Regarding autoimmune diseases of the central nervous be found. Although data from large-scale clinical trials system (CNS), repeated intrathecal application of the are missing, intrathecal TRIAM application is still used from specialized centers as an off-label treatment [4]. * Correspondence: [email protected] Department of Neurology, St. Josef Hospital, Ruhr-University Bochum, Gudrunstr. 56, 44791 Bochum, Germany © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Pitarokoili et al. Journal of Neuroinflammation (2019) 16:58 Page 2 of 12 Our group has previously shown that intrathecal Materials and methods therapeutic application of human immunoglobulins in Antigens the context of experimental autoimmune neuritis The neuritogenic P2 peptide, corresponding to amino (EAN), the animal model of dysimmune neuropathies acids 53–78 of rat myelin P2 protein, was synthesized by such as Guillain-Barré syndrome (GBS), or the Dr. Rudolf Volkmer from Charité Universitätsmedizin chronic inflammatory demyelinating polyradiculo- (Berlin, Germany). neuropathy (CIDP) achieves a dose-dependent im- provement of clinical signs, which correlate with a Triamcinolone histological reduction of inflammatory infiltrates in Triamcinolone acetonide (Volon A, Bristol-Meyers the sciatic nerves and of complement activation in Squibb, New York, NY, USA, active ingredient thesciaticnerve[10]. 16a.17-Dimethyl- Corticosteroids are used as first-line therapy in the methylendioxy-9-fluor-11b.21-dihydroxy-1.4-pregnadien form of pulsed intravenous methylprednisolone or oral - 3.20-dion) supplied in sodium chloride solution long-term prednisolone treatment for patients with equivalent to 10 mg TRIAM/ml or 40 mg TRIAM/ml CIDP and improve sensory symptoms and painful was used for all experiments. paresthesia. Unfortunately, their therapeutic benefits are limited by side effects such as osteoporosis, abdominal Study design—disease induction and clinical score obesity, glaucoma, diabetes mellitus, and hypertension assessment (Cushing’s syndrome) [2]. A total of 45 female Lewis rats were randomized for the Intrathecal application route has not yet been investi- therapeutic concept as described in the following section. gated for TRIAM in autoimmune diseases of the peripheral The rats were 6–8 weeks old; they were purchased from nervous system (PNS) although the first sites of inflamma- Charles River Co. (Sulzfeld, Germany) and weighed 160– tion and increase of blood-nerve barrier permeability are 180 g when used for the following experiments. They were the proximal nerve roots, as indicated by the early intra- anesthetized by 1.5–2.0% halothane in oxygen. They were thecal protein increase found in these patients [11, 12]. immunized by subcutaneous injection of 250 μgP253–78 According to the published literature, TRIAM mediates peptide in phosphate-buffered saline (PBS) into the root a combination of anti-inflammatory, anti-oedematous, of the tail, emulsified in an equal volume of complete anti-proliferative, anti-angiogenetic, and neuroprotective Freund’s adjuvant (CFA) containing Mycobacterium tuber- effects, which could be very crucial for autoimmune dis- culosis (1 mg/ml) H37RA (Difco, Detroit, MI, USA). Ani- eases of the PNS. The anti-inflammatory effects of mals were weighted and scored for disease severity daily TRIAM have been widely investigated and are mediated by two independent, blinded investigators. Disease severity after binding to the glucocorticoid (GR) nuclear receptors, was assessed clinically employing a scale ranging from 0 which is widely expressed in neurons and Schwann cells. to 10 originally described by Enders et al. [16]: 0, normal; Upon binding TRIAM, the receptors undergo a conform- 1, less lively; 2, impaired righting/limb tail; 3, absent right- ational change and translocate in the nucleus to mediate ing; 4, atactic gait, abnormal position; 5, mild paraparesis; gene transcription and induce an anti-inflammatory po- 6, moderate paraparesis; 7, severe paraplegia; 8, tetrapar- tential for example through inhibiting cytokine release esis; 9, moribund; 10, death. All experiments were (e.g., TNFα and IL-1β). GR can also signal through nonge- reviewed and approved by the North-Rhine-Westphalia, nomic pathways which occur rapidly and do not require Germany authorities for animal experimentation (TVA transcriptional changes [13, 14]. 84-02.04.2017-A023). Intrathecal TRIAM was also suggested to have neu- roprotective efficacy on infarction volume in acute Intrathecal treatment with triamcinolone and dosage focal cerebral ischemia in rats. Compared with con- rationale trols (18.2%), infarction volume was significantly re- The animals were anesthetized by 1.5–2.0% halothane in duced using TRIAM injection into the cisterna magna oxygen, and triamcinolone was injected intrathecally (13.4%) [15]. slowly within 4 s with a microsyringe in the following con- In this study, we describe for the first time the im- centrations: 0.3 mg/kg, 0.6 mg/kg once (n = 5/group) on munomodulatory effects of triamcinolone in vivo ap- day 11 post-immunization (p.i.) in a volume of 5 μl, as plied intrathecally in the Lewis rat model of EAN. control NaCl 0.9% in a volume of 5 μl was used (n =5). Moreover, this study describes indirect neuroprotec- The injection was performed with a 30-G needle into the tive mechanisms in vitro in the context of Schwann four to five lumbar intervertebral space, and the correct cell culture. Therefore, we present the first report of placement of the injection was confirmed by a movement an effective and dose-saving route of administration of the tail (“tail flick”) as described by Fairbanks and col- of TRIAM for dysimmune neuropathies. leagues [17]. The experiments were repeated twice. Pitarokoili et al. Journal of Neuroinflammation (2019) 16:58 Page 3 of 12 The dosages described above were calculated accord- maintain a low rate of fibroblast contamination, we ing to previous experiments from Goericke et al. who used Miltenyi’s MACS technology to achieve efficient showed a reduction of the volume of infarction after an separation of SCs and Thy-1-positive fibroblasts (nega- injection of 0.0012–0.3 mg/kg TRIAM in the cisterna tive selection) as described by the manufacturer’s protocol. magna in a rat model of cerebral infarction [15]. Then, the purified SCs (purification of 90% SOX10-positive
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