Recent advances in the biomedical applications of fumaric acid and its ester derivatives: The multifaceted alternative therapeutics

Yang, 2011 Goldberg, 2006, Organic acids: old metabolites, new themes, J Chem Technol Biotechnol, 8, 1601, 10.1002/jctb.1590 Rohokale, 2014, Natural organic acids promoted Beckmann rearrangement: green and expeditious synthesis of amides under solvent-free conditions, Chem Pap, 68, 575, 10.2478/s11696-013-0481-y Temenoff, 2007 www.fda.gov/NewsEvents/Newsroom/PressAnnouncements/ucm345528.htm [accessed 30.06.15]. Gniadecki, 1998, Regulation of keratinocyte proliferation, Gen Pharmac, 30, 619, 10.1016/S0306-3623(97)00419-9 Cai, 2012, New insights of T cells in the pathogenesis of psoriasis, Cell Mol Immunol, 9, 302, 10.1038/cmi.2012.15 Ghoreschi, 2007, Immunopathogenesis and role of T cells in psoriasis, Clin Dermatol, 25, 574, 10.1016/j.clindermatol.2007.08.012 Nestle, 2009, Psoriasis, Engl J Med, 361, 496, 10.1056/NEJMra0804595 Leonardi, 2008, Efficacy and safety of ustekinumab, a human interleukin-12/23 monoclonal antibody, in patients with psoriasis: 76-week results from a randomised, double-blind, placebo-controlled trial (PHOENIX 1), Lancet, 371, 1665, 10.1016/S0140-6736(08)60725-4 Belge, 2014, Advances in treating psoriasis, F1000Prim Rep, 6, 1 Schweckendiek, 1959, Psoriasis, Med Monatsschr, 13, 103 Cathcart, 1990, 351 Mrowietz, 2005, Dimethylfumarate for psoriasis: more than a dietary curiosity, Trends Mol Med, 11, 43, 10.1016/j.molmed.2004.11.003 Altmeyer, 1994, Antipsoriatic effect of fumaric acid derivatives. Results of a multicenter double-blind study in 100 patients, J Am Acad Dermatol, 30, 977, 10.1016/S0190-9622(94)70121-0 Mrowietz, 1998, Treatment of psoriasis with fumaric acid esters: results of a prospective multicenter study, Br J Dermatol, 138, 456, 10.1046/j.1365-2133.1998.02124.x Kolbach, 1992, Fumaric acid therapy in psoriasis. Results and side-effects of 2 years of treatment, J Am Acad Dermatol, 27, 769, 10.1016/S0190-9622(08)80228-9 Thio, 1995, Long-term systemic therapy with dimethylfumarate and monoethylfumarate (Fumaderm) in psoriasis, J Eur Acad Dermatol Venereol, 4, 35, 10.1016/0926-9959(94)00056-6 Hoefnagel, 2003, Long-term safety aspects of systemic therapy with fumaric acid esters in severe psoriasis, Brit J Dermatol, 149, 363, 10.1046/j.1365-2133.2003.05433.x Brewer, 2007, Fumaric acid esters in the management of severe psoriasis, Clin Exp Dermatol, 32, 246, 10.1111/j.1365-2230.2007.02389.x Reich, 2009, Efficacy and safety of fumaric acid esters in the long-term treatment of psoriasis – a retrospective study (FUTURE), J Dtsch Dermatol Ges, 7, 603 Wain, 2010, Treatment of severe, recalcitrant, chronic plaque psoriasis with fumaric acid esters: a prospective study, Br J Dermatol, 162, 427, 10.1111/j.1365-2133.2009.09267.x Harries, 2005, Fumaric acid esters for severe psoriasis: a retrospective review of 58 cases, Br J Dermatol, 153, 549, 10.1111/j.1365-2133.2005.06728.x Ismail, 2014, Drug survival of fumaric acid esters for psoriasis: a retrospective study, Br J Dermatol, 171, 397, 10.1111/bjd.12849 Ockenfels, 1998, The antipsoriatic agent dimethylfumarate immunomodulates T-cell cytokines and inhibits cytokines of the psoriatic cytokine network, Br J Dermatol, 139, 390, 10.1046/j.1365-2133.1998.02400.x Jong, 1996, Selective stimulation of T helper 2 cytokine responses by the antipsoriasis agent monomethyl-fumarate, Eur J Immunol, 26, 2067, 10.1002/eji.1830260916 Litjens, 2003, Beneficial effects of fumarate therapy in psoriasis vulgaris patients coincide with downregulation of type 1 cytokines, Br J Dermatol, 148, 444, 10.1046/j.1365-2133.2003.05153.x Sebok, 1994, Antiproliferative and cytotoxic profiles of antipsoriatic fumaric acid derivatives in keratinocyte cultures, Eur J Pharmacol, 270, 79 Sebok, 1994, IL-1 alpha-induced expression of ICAM-1on cultured hyperproliferative keratinocytes: suppression by antipsoriatic dimethyl-fumarate, Int J Dermatol, 33, 367, 10.1111/j.1365-4362.1994.tb01070.x Stühlinger, 1990, The nephrotoxic effect of therapy with fumaric acid esters in psoriasis, Dtsch Med Wochenschr, 115, 1712, 10.1055/s-2008-1065215 Haring, 2011, Early detection of renal damage caused by fumaric acid ester therapy by determination of urinary β2-microglobulin, Br J Dermatol, 164, 648 Fliegner, 1992, Osteomalacia as an apparently rare side effect of oral fumaric acid therapy Secondary DeToni-Debré Fanconi syndrome in the adult, Hautarzt, 43, 554 Raschka, 1999, Long term treatment of psoriasis using fumaric acid preparations can be associated with severe proximal tubular damage, Hum Exp Toxicol, 18, 738, 10.1191/096032799678839662 Clanet, 2008, Jean-Martin Charcot. 1825 to 1893, Int MS J, 15, 59 Compston, 2002, Multiple sclerosis, Lancet, 359, 1221, 10.1016/S0140-6736(02)08220-X Compston, 2008, Multiple sclerosis, Lancet, 372, 1502, 10.1016/S0140-6736(08)61620-7 www.msif.org/global-ms-news [accessed 22.06.15]. Schimrigk, 2006, Oral fumaric acid esters for the treatment of active multiple sclerosis: an open-label, baseline-controlled pilot study, Eur J Neurol, 13, 604, 10.1111/j.1468-1331.2006.01292.x Schilling, 2006, Fumaric acid esters are effective in chronic experimental autoimmune encephalomyelitis and suppress macrophage infiltration, Clin Exp Immunol, 145, 101, 10.1111/j.1365-2249.2006.03094.x Anon., 2005, BG 12: BG 00012, BG 12/Oral Fumarate, FAG–201, second-generation fumarate derivative – Fumapharm/Biogen Idec, Drugs R D, 6, 229, 10.2165/00126839-200506040-00005 Wakkee, 2007, Drug evaluation: BG-12, an immunomodulatory dimethylfumarate, Curr Opin Invest Drugs, 8, 955 Moharregh-Khiabani, 2009, Fumaric acid and its esters: an emerging treatment for multiple sclerosis, Curr Neuropharm, 7, 60, 10.2174/157015909787602788 www.biogenidec.com/press_release_details.aspx?ID=14712&M=News&PID=61997&NewsID=1809 [accessed 22.06.15]. Ermis, 2013, PML in a patient treated with fumaric acid, N Engl J Med, 368, 1657, 10.1056/NEJMc1211805 van Oosten, 2013, PML in a patient treated with dimethyl fumarate from a compounding pharmacy, N Engl J Med, 368, 1658, 10.1056/NEJMc1215357 Rosenkranz, 2015, PML in a patient with lymphocytopenia treated with dimethyl fumarate, N Engl J Med, 372, 1476, 10.1056/NEJMc1415408 Khatri, 2015, The effect of dimethyl fumarate (Tecfidera™) on lymphocyte counts: A potential contributor to progressive multifocal Leukoencephalopathy risk, Mult Scler Relat Disord, 4, 377, 10.1016/j.msard.2015.05.003 Spencer, 2015, Reduction of CD8(+) T lymphocytes in multiple sclerosis patients treated with dimethyl fumarate, Neurol Neuroimmunol Neuroinflamm, 2, e76, 10.1212/NXI.0000000000000076 Xu, 2014, Dimethyl fumarate for multiple sclerosis, Cochr Database Syst Rev, 10.1002/14651858.CD011076 www.myocarditisfoundation.org/about-myocarditis/ [accessed 22.06.15]. Loewe, 2011, Dimethylfumarate inhibits tumor-necrosis-factor-induced CD62E expression in an NF-kB-dependent manner, J Invest Dermatol, 117, 1363 Loewe, 2002, Dimethylfumarate inhibits TNF-Induced Nuclear Entry of NF-κB/p65 in human endothelial cells, J Immunol, 168, 4781, 10.4049/jimmunol.168.9.4781 Milenkovic, 2008, Beneficial effects of dimethyl fumarate on experimental autoimmune myocarditis, Arch Med Res, 39, 639, 10.1016/j.arcmed.2008.07.003 Kis, 2003, Role of nuclear factor-kappa B activation in acute ischaemia–reperfusion injury in myocardium, Br J Pharmacol, 138, 894, 10.1038/sj.bjp.0705108 Meili-Butz, 2008, Dimethyl fumarate, a small molecule drug for psoriasis, inhibits Nuclear Factor-κB and reduces myocardial infarct size in rats, Eur J Pharmacol, 586, 251, 10.1016/j.ejphar.2008.02.038 Cross, 2011, Dimethyl fumarate, an immune modulator and inducer of the antioxidant response, suppresses HIV replication and macrophage-mediated neurotoxicity: a novel candidate for HIV neuroprotection, J Immunol, 187, 5015, 10.4049/jimmunol.1101868 Gill, 2013, Dimethyl fumarate modulation of immune and antioxidant responses: application to HIV therapy, Crit Rev Immunol, 33, 307, 10.1615/CritRevImmunol.2013007247 Gill, 2014, Heme oxygenase-1 deficiency accompanies neuropathogenesis of HIV-associated neurocognitive disorders, J Clin Invest, 124, 4459, 10.1172/JCI72279 Schmidt, 2007, Reactivity of dimethyl fumarate and methylhydrogen fumarate towards glutathione and N-acetyl-l-cysteine – preparation of S-substituted thiosuccinic acid esters, Bioorg Med Chem, 15, 333, 10.1016/j.bmc.2006.09.053 Linker, 2011, Fumaric acid esters exert neuroprotective effects in neuroinflammation via activation of the Nrf2 antioxidant pathway, Brain, 134, 678, 10.1093/brain/awq386 Wiesner, 2013, Fumaric acid esters stimulate astrocytic VEGF expression through HIF-1α and Nrf2, PLOS ONE, 8, e76670, 10.1371/journal.pone.0076670 Zhu, 2001, Inhibition of dendritic cell differentiation by fumaric acid esters, J Invest Dermatol, 116, 203, 10.1046/j.1523-1747.2001.01159.x Nibbering, 1993, Effects of Monomethylfumarate on human granulocytes, J Invest Dermatol, 101, 37, 10.1111/1523-1747.ep12358715 Stoof, 2001, The antipsoriatic drug dimethylfumarate strongly suppresses chemokine production in human keratinocytes and peripheral blood mononuclear cells, Br J Dermatol, 144, 1114, 10.1046/j.1365-2133.2001.04220.x Hanson, 2012, Role of HCA2 (GPR109A) in nicotinic acid and fumaric acid ester-induced effects on the skin, Pharmacol Ther, 136, 1, 10.1016/j.pharmthera.2012.06.003 Heiligenhaus, 2005, Improvement of herpetic stromal keratitis with fumaric acid derivate is associated with systemic induction of T helper 2 cytokines, Clin Exp Immunol, 142, 180, 10.1111/j.1365-2249.2005.02896.x Venten, 2006, Treatment of therapy-resistant alopecia areata with fumaric acid esters, Eur J Med Res, 11, 300 Wang, 2006, Bone tissue-engineering material poly(propylene fumarate): correlation between molecular weight, chain dimensions, and physical properties, Biomacromolecules, 7, 1976, 10.1021/bm060096a Elfick, 2002, Poly(e-caprolactone) as a potential material for a temporary joint spacer, Biomaterials, 23, 4463, 10.1016/S0142-9612(02)00163-1 Peter, 1998, In vivo degradation of a poly(propylene fumarate)/beta-tricalcium phosphate injectable composite scaffold, J Biomed Mater Res, 41, 1, 10.1002/(SICI)1097-4636(199807)41:1<1::AID-JBM1>3.0.CO;2-N Horch, 2004, Nanoreinforcement of poly(propylene fumarate)-based networks with surface modified alumoxane nanoparticles for bone tissue engineering, Biomacromolecules, 5, 1990, 10.1021/bm049768s Farshid, 2013, Cytotoxicity of polypropylene fumarate nanocomposites used in bone tissue engineering Christenson, 2007, Biodegradable fumarate-based PolyHIPEs as tissue engineering scaffolds, Biomacromolecules, 8, 3806, 10.1021/bm7007235 Lee, 2007, Poly(propylene fumarate) bone tissue engineering scaffold fabrication using stereolithography: effects of resin formulations and laser parameters, Biomacromolecules, 8, 1077, 10.1021/bm060834v Lan, 2009, Development of 3D PPF/DEF scaffolds using micro-stereolithography and surface modification, J Mater Sci: Mater Med, 20, 271 Fisher, 2002, Photocrosslinking characteristics and mechanical properties of diethyl fumarate/poly(propylene fumarate) biomaterials, Biomaterials, 23, 4333, 10.1016/S0142-9612(02)00178-3 Domb, 1996, Biodegradable bone cement compositions based on acrylate and epoxide terminated poly(propylene fumarate) oligomers and calcium salt compositions, Biomaterials, 17, 411, 10.1016/0142-9612(96)89657-8 Chang, 2010, A poly(propylene fumarate) – calcium phosphate based angiogenic injectable bone cement for femoral head osteonecrosis, Biomaterials, 31, 4048, 10.1016/j.biomaterials.2010.01.124 Cai, 2010, Poly(ethylene glycol)-grafted poly(propylene fumarate) networks and parabolic dependence of MC3T3 cell behavior on the network composition, Biomaterials, 31, 4457, 10.1016/j.biomaterials.2010.02.020 Timmer, 2003, Fabrication of poly(propylene fumarate)-based orthopedic implants by photo-crosslinking through transparent silicone molds, Biomaterials, 24, 4707, 10.1016/S0142-9612(03)00364-8 Timmer, 2003, In vitro degradation of polymeric networks of poly(propylene fumarate) and the crosslinking macromer poly(propylene fumarate)-diacrylate, Biomaterials, 24, 571, 10.1016/S0142-9612(02)00368-X Payne, 2002, Development of an injectable, in situ crosslinkable, degradable polymeric carrier for osteogenic cell populations. Part 2. Viability of encapsulated marrow stromal osteoblasts cultured on crosslinking poly(propylene fumarate), Biomaterials, 23, 4373, 10.1016/S0142-9612(02)00185-0 Payne, 2002, Development of an injectable, in situ crosslinkable, degradable polymeric carrier for osteogenic cell populations. Part 3. Proliferation and differentiation of encapsulated marrow stromal osteoblasts cultured on crosslinking poly(propylene fumarate), Biomaterials, 23, 4381, 10.1016/S0142-9612(02)00186-2 He, 2000, Injectable biodegradable polymer composites based on poly(propylene fumarate) crosslinked with poly(ethylene glycol)-dimethacrylate, Biomaterials, 21, 2389, 10.1016/S0142-9612(00)00106-X Jayabalan, 2001, Polypropylene fumarate/phloroglucinol triglycidyl methacrylate blend for use as partially biodegradable orthopaedic cement, Biomaterials, 22, 2749, 10.1016/S0142-9612(01)00018-7 Hedberga, 2005, In vitro degradation of porous poly(propylene fumarate)/poly(dl-lactic-co-glycolic acid) composite scaffolds, Biomaterials, 26, 3215, 10.1016/j.biomaterials.2004.09.012 Suggs, 1999, Platelet adhesion on a bioresorbable poly(propylene fumarate-co-ethylene glycol) copolymer, Biomaterials, 20, 683, 10.1016/S0142-9612(98)00226-9 Childers, 2015, 3D printing of resorbable poly(propylene fumarate) tissue engineering scaffolds, Mat Res Soc Bull, 40, 119, 10.1557/mrs.2015.2 Runge, 2010, The development of electrically conductive polycaprolactone fumarate-polypyrrole composite materials for nerve regeneration, Biomaterials, 31, 5916, 10.1016/j.biomaterials.2010.04.012 Farokhi, 2012, Porous crosslinked poly(e-caprolactone fumarate)/nanohydroxyapatite composites for bone tissue engineering, J Biomed Mater Res A, 100, 1051, 10.1002/jbm.a.33241 Shafieyan, 2011, Biocompatible composite based on poly(e-caprolactone fumarate) and hydroxyapatite, Polym Adv Technol, 22, 2182, 10.1002/pat.1743 Wang, 2006, Synthesis and characterizations of biodegradable and crosslinkable poly(e-caprolactone fumarate), poly(ethylene glycol fumarate), and their amphiphilic copolymer, Biomaterials, 27, 832, 10.1016/j.biomaterials.2005.07.013 Desai, 2013, Synthesis and characterization of fumaric acid functionalized AgCl/titania nanocomposite with enhanced antibacterial activity, J Nanosci Nanotechnol, 13, 2826, 10.1166/jnn.2013.7370 Ueda, 2007, Injectable, in situ forming poly(propylene fumarate)-based ocular drug delivery systems, J Biomed Mater Res A, 83, 656, 10.1002/jbm.a.31226 Shokri, 2011, Preparation and characterization of crosslinked and non-crosslinked polycaprolactone fumarate (PCLF) NPs as carriers for doxorubicin HCl, Afr J Pharm Pharmacol, 5, 797 Jansen, 2010, Rapid photo-crosslinking of fumaric acid monoethyl ester-functionalized poly(trimethylene carbonate) oligomers for drug delivery applications, J Control Release, 147, 54, 10.1016/j.jconrel.2010.06.031 Chickering, 1996, Poly(fumaric-co-sebacic). Microspheres as oral drug delivery systems, Biotechnol Bioeng, 52, 96, 10.1002/(SICI)1097-0290(19961005)52:1<96::AID-BIT9>3.0.CO;2-U Mrowietz, 1999, Treatment of severe psoriasis with fumaric acid esters: scientific background and guidelines for therapeutic use, Br J Dermatol, 141, 424, 10.1046/j.1365-2133.1999.03034.x Werdenberg, 2003, Presystemic metabolism and intestinal absorption of antipsoriatic fumaric acid esters, Biopharm Drug Dispos, 24, 259, 10.1002/bdd.364 Litjens, 2004, In vitro pharmacokinetics of anti-psoriatic fumaric acid esters, BMC Pharmacol, 4, 22, 10.1186/1471-2210-4-22 Litjens, 2004, Pharmacokinetics of oral fumarates in healthy subjects, Br J Clin Pharm, 58, 429, 10.1111/j.1365-2125.2004.02145.x Rostami-Yazdi, 2009, Detection of metabolites of fumaric acid esters in human urine: implications for their mode of action, J Invest Dermatol, 129, 231, 10.1038/jid.2008.197 Rostami-Yazdi, 2010, Pharmacokinetics of anti-psoriatic fumaric acid esters in psoriasis patients, Arch Dermatol Res, 302, 531, 10.1007/s00403-010-1061-4 Kuroda, 1976, Inhibitory effect of Capsella bursa pastoris extract on growth of Ehrlich solid tumor in mice, Cancer Res, 36, 1900 Kuroda, 1981, Antitumor anti-intoxication activities of fumaric acid in cultured cells, Gan, 72, 777 Kuroda, 1982, Inhibitory effect of fumaric acid on forestomach and lung carcinogenesis by a 5-nitrofuran naphthyridine derivative in mice, J Natl Cancer Inst, 69, 1317 Kuroda, 1986, Fumaric acid enhances DNA synthesis of rat hepatocytes by counteracting the toxicities of mitomycin C and aflatoxin B1, Jpn J Cancer Res, 77, 750 Akao, 1990, Inhibitory effect of fumaric acid on hepatocarcinogenesis by thioacetamide in mice, Chem Pharm Bull (Tokyo), 38, 2012, 10.1248/cpb.38.2012 Bespalov, 1992, The anticarcinogenic effects of fumaric acid on models of carcinogenesis in the esophagus, nervous system and kidney, Voprosy, Onkologii, 38, 956 Tsubaki, 2014, Dimethyl fumarate induces apoptosis of hematopoietic tumor cells via inhibition of NF-kB nuclear translocation and down-regulation of Bcl-xL and XIAP, Biomed Pharmacother, 68, 999, 10.1016/j.biopha.2014.09.009 Roa Engel, 2008, Fumaric acid production by fermentation, Appl Microbiol Biotechnol, 78, 379, 10.1007/s00253-007-1341-x Launert, 1989 Sharma, 2012, Hepatoprotective activity of fumaria officinalis against CCl4-induced liver damage in rats, Pharmacologia, 3, 9, 10.5567/pharmacologia.2012.9.14