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Celastrol: a Spectrum of Treatment Opportunities in Chronic Diseases

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Celastrol: a Spectrum of Treatment Opportunities in Chronic Diseases REVIEW published: 15 June 2017 doi: 10.3389/fmed.2017.00069 Celastrol: A Spectrum of Treatment Opportunities in Chronic Diseases Rita Cascão1, João E. Fonseca1,2* and Luis F. Moita3 1 Instituto de Medicina Molecular, Faculdade de Medicina, Universidade de Lisboa, Lisbon, Portugal, 2 Rheumatology Department, Centro Hospitalar de Lisboa Norte, EPE, Hospital de Santa Maria, Lisbon Academic Medical Centre, Lisbon, Portugal, 3 Instituto Gulbenkian de Ciência, Oeiras, Portugal The identification of new bioactive compounds derived from medicinal plants with significant therapeutic properties has attracted considerable interest in recent years. Such is the case of the Tripterygium wilfordii (TW), an herb used in Chinese medicine. Clinical trials performed so far using its root extracts have shown impressive therapeutic properties but also revealed substantial gastrointestinal side effects. The most promising bioactive compound obtained from TW is celastrol. During the last decade, an increasing number of studies were published highlighting the medicinal usefulness of celastrol in diverse clinical areas. Here we systematically review the mechanism of action and the therapeutic properties of celastrol in inflammatory diseases, namely, rheumatoid arthritis, systemic lupus erythematosus, inflammatory bowel diseases, osteoarthritis and allergy, Edited by: as well as in cancer, neurodegenerative disorders and other diseases, such as diabetes, Peter S. Steyger, Oregon Health & Science University, obesity, atherosclerosis, and hearing loss. We will also focus in the toxicological profile United States and limitations of celastrol formulation, namely, solubility, bioavailability, and dosage Reviewed by: issues that still limit its further clinical application and usefulness. Imtiaz Ahmad Siddiqui, University of Wisconsin-Madison, Keywords: celastrol, inflammation, cancer, neurodegenerative diseases, toxicity, treatment, clinical trials United States Carole Guillonneau, Centre national de la recherche Abbreviations: T W, Tripterygium wilfordii; RA, rheumatoid arthritis; CD, Crohn’s disease; CRP, C-reactive protein; ACR, scientifique (CNRS), France American College of Rheumatology; DMARD, disease-modifying antirheumatic drug; MTX, methotrexate; DM, diabetes mellitus; LPS, lipopolysaccharide; IL, interleukin; PEG2, prostaglandin E2; SCW, Streptococcus cell wall-induced arthritis; *Correspondence: CIA, collagen-induced arthritis; AIA, adjuvant-induced arthritis; TNF, tumor necrosis factor; NO, nitric oxide; iNOS, inducible João E. Fonseca nitric oxide synthase; COX, cyclooxygenase; NF-kB, nuclear factor kappa B; AP-1, activator protein 1; IFN-γ, interferon gamma; [email protected] LN, lymph node; SA, spleen adherent; STAT3, signal transducer and activator of transcription 3; RORγ, RAR-related orphan receptor gamma; Th, T helper; MMP, metalloproteinase; ERK, extracellular signal-regulated kinase; VEGF, vascular endothelial Specialty section: growth factor; Anti-CCP, anti-cyclic citrullinated peptide; RANTES, regulated on activation, normal T cell expressed and This article was submitted to secreted; MCP-1, monocyte chemoattractant protein-1; GRO/KC, chemokine ligand 1; MIP-1α, macrophage inflammatory Translational Medicine, protein 1-alpha; CCR1, C-C chemokine receptor type 1; MD2, lymphocyte antigen 96; TLR, Toll-like receptor; FLS, fibroblasts; MyD88, myeloid differentiation primary response gene 88; HIF, hypoxia-inducible factor; CXCR, C-X-C chemokine receptor; a section of the journal NET, extracellular trap; SYK, spleen tyrosine kinase; MEK, serine/tyrosine/threonine kinase; IkBα, nuclear factor of kappa light Frontiers in Medicine polypeptide gene enhancer in B-cells inhibitor, alpha; SIC, synovium-infiltrating cells; Treg, T regulatory; RANKL, receptor Received: 13 March 2017 activator of nuclear factor kappa-B ligand; M-CSF, Macrophage colony-stimulating factor; TAK1, transforming growth factor Accepted: 19 May 2017 beta-activated kinase 1; OPG, osteoprotegerin; Trap, tartrate-resistant acid phosphatase; Ctsk, Cathepsin k; NFATc1, nuclear Published: 15 June 2017 factor of activated T-cells 1; MAPK, mitogen-activated protein kinase; PTH, parathyroid hormone; TRACP5b, tartrate-resistant acid phosphatase 5b; CTX-I, cross-linked C-telopeptide of type I collagen; DPD, deoxypyridinoline; AS, ankylosing spondylitis; Citation: PI3K, phosphoinositide 3-kinase; Akt, protein kinase B; CB2, cannabinoid receptor-2; SLE, systemic lupus erythematosus; UC, Cascão R, Fonseca JE and Moita LF ulcerative colitis; PBMCs, peripheral blood mononuclear cells; NLRP3, NLR family pyrin domain containing 3; RIP3, receptor- (2017) Celastrol: A Spectrum of interacting serine-threonine kinase 3; MLKL, mixed lineage kinase domain-like pseudokinase; LITAF, LPS-induced-TNF-α- Treatment Opportunities in Chronic factor; mTOR, mechanistic target of rapamycin; PCNA, proliferating cell nuclear antigen; EMT, mesenchymal transition; SCD1, Diseases. stearoyl-CoA desaturase-1; OA, osteoarthritis; HSP, heat shock protein; TIMP, inhibitor of metalloproteinase; FcεRI, Fc epsilon Front. Med. 4:69. receptor I; PKC, protein kinase C; ROS, reactive oxygen species; JNK, c-Jun N-terminal kinases; AR, androgen receptor; TRAIL, doi: 10.3389/fmed.2017.00069 TNF-related apoptosis-inducing ligand; MRC, mitochondrial respiratory chain; AMPK, AMP-activated protein kinase; ErbB2, Frontiers in Medicine | www.frontiersin.org 1 June 2017 | Volume 4 | Article 69 Cascão et al. Celastrol: Potential and Limitations Erb-B2 receptor tyrosine kinase 2; AML, acute myelogenous leukemia; JAK, Janus kinase; ER, endoplasmic reticulum; PERK, ER stress; eIF2, eukaryotic initiation factor 2; ATF, activating transcription factor; CHOP, C/EBP homology protein; GSK3β, glycogen synthase kinase 3 beta; IP3R, inositol trisphosphate receptor; EGFR, epidermal growth factor receptor; PARP, poly (ADP-ribose) polymerase; IKK, IkappaB kinase; HSF, heat shock transcription factor; NEMO, NF-kappa-B essential modula- tor; TRAF, TNF receptor associated factor; BACE-1, β-site amyloid precursor protein cleaving enzyme 1; EAE, experimental autoimmune encephalomyelitis; PGC1α, peroxisome proliferator-activated receptor gamma coactivator 1-alpha; Sirt3, NAD- dependent deacetylase sirtuin-3; CCL2, chemokine (C-C motif) ligand 2; POMC, pro-opiomelanocortin; AgRP, Agouti-related protein; NPY, Neuropeptide Y; LDL, low-density lipoprotein; apoE, apolipoprotein E; LOX-1, lectin-like oxidized low-density lipoprotein receptor-1; EPC, endothelial progenitor cell; LD, lethal dose. INTRODUCTION CLINICAL EXPERIENCE WITH THE USE OF TW The identification of bioactive compounds derived from medici- nal plants has attracted considerable interest in recent years Clinical trials using TW plant extracts have already been con- for their strong and in some cases unique, anti-inflammatory, ducted in inflammatory diseases. anticancer, and neuroprotective properties. One representa- TW is generally used in the treatment of Crohn’s disease tive example is the Tripterygium wilfordii (TW) plant, used in (CD) in China. Its therapeutic benefits have been explored in Chinese medicine to treat an array of immunological disorders, an open-label clinical trial conducted in 20 CD patients treated including rheumatoid arthritis (RA), with promising results in a with TW tablets (120 mg daily) for a period of 12 weeks. series of clinical trials. TW is a perennial vine of the Celastraceae CD Activity Index diminished during the first 8 weeks, and family, also called Thunder God Vine or “lei gong teng” (Chinese the endoscopic improvement was observed after 12 weeks. name). This plant is poisonous but its root pulp contains several Inflammatory parameters, including c-reactive protein (CRP), therapeutic compounds, including terpenoids, alkaloids, and also decreased (2). In addition, two placebo-controlled trials steroids. The chemical structure of its purified compounds and one prospective single-blind clinical trial have studied the has been determined by nuclear magnetic resonance and mass therapeutic potential of polyglycoside TW (1 mg/kg daily) in the spectroscopy. More than 46 diterpenoids (such as triptolide), prevention of postsurgical relapses in patients with CD. Results 20 triterpenoids (e.g., celastrol), 21 alkaloids (like euonine), from these studies suggest that this is an effective and well- and other small molecules have been identified from TW. The tolerated drug (3–5). Recently, a randomized clinical trial has most abundant and promising bioactive compound derived shown that TW (1.5 mg/kg/day) was comparable to azathioprine from the root of this plant is celastrol, also called tripterine, to prevent postoperative clinical recurrence of CD, although less which possess a broad range of biological activities. Celastrol efficient in preserving endoscopic remission at week 52 (6). An (3-hydroxy-9β,13α-dimethyl-2-oxo-24,25,26-trinoroleana- additional clinical trial enrolled 198 patients with CD, which 1(10),3,5,7-tetraen-29-oic acid) is a pentacyclic triterpenoid were randomized to receive mesalazin (3 g/day), low-dose (Figure 1) that belongs to a small category of natural products TW (1.5 mg/kg/day) or high-dose TW (2.0 mg/kg/day) over of triterpene quinine methides. a 52-week period (7). Importantly, data have shown that less Here, we systematically review the therapeutic properties of patients in the high-dose group (7/71) had clinical recurrence celastrol in chronic diseases and its toxicological profile, illustrat- in comparison with patients in the
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