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Antiproliferative Effects of St. John's Wort, Its Derivatives, and Other Hypericum Species in Hematologic Malignancies

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Antiproliferative Effects of St. John's Wort, Its Derivatives, and Other Hypericum Species in Hematologic Malignancies International Journal of Molecular Sciences Review Antiproliferative Effects of St. John’s Wort, Its Derivatives, and Other Hypericum Species in Hematologic Malignancies Alessandro Allegra 1,* , Alessandro Tonacci 2 , Elvira Ventura Spagnolo 3, Caterina Musolino 1 and Sebastiano Gangemi 4 1 Division of Hematology, Department of Human Pathology in Adulthood and Childhood “Gaetano Barresi”, University of Messina, 98125 Messina, Italy; [email protected] 2 Clinical Physiology Institute, National Research Council of Italy (IFC-CNR), 56124 Pisa, Italy; [email protected] 3 Section of Legal Medicine, Department of Health Promotion Sciences, Maternal and Infant Care, Internal Medicine and Medical Specialties (PROMISE), University of Palermo, Via del Vespro, 129, 90127 Palermo, Italy; [email protected] 4 School and Operative Unit of Allergy and Clinical Immunology, Department of Clinical and Experimental Medicine, University of Messina, 98125 Messina, Italy; [email protected] * Correspondence: [email protected]; Tel.: +39-090-221-2364 Abstract: Hypericum is a widely present plant, and extracts of its leaves, flowers, and aerial elements have been employed for many years as therapeutic cures for depression, skin wounds, and respiratory and inflammatory disorders. Hypericum also displays an ample variety of other biological actions, such as hypotensive, analgesic, anti-infective, anti-oxidant, and spasmolytic abilities. However, recent investigations highlighted that this species could be advantageous for the cure of other pathological situations, such as trigeminal neuralgia, as well as in the treatment of cancer. This review focuses on the in vitro and in vivo antitumor effects of St. John’s Wort (Hypericum perforatum), its derivatives, and other Hypericum species in hematologic malignancies. Hypericum induces apoptosis in both myeloid and lymphoid cells. Other Hypericum targets include matrix metalloproteinase-2, vascular Citation: Allegra, A.; Tonacci, A.; endothelial growth factor, and matrix metalloproteinase-9, which are mediators of cell migration Spagnolo, E.V.; Musolino, C.; Gangemi, and angiogenesis. Hypericum also downregulates the expression of proteins that are involved in S. Antiproliferative Effects of St. John’s the resistance of leukemia cells to chemotherapeutic agents. Finally, Hypericum and its derivatives Wort, Its Derivatives, and Other Hypericum Species in Hematologic appear to have photodynamic effects and are candidates for applications in tumor photodynamic Malignancies. Int. J. Mol. Sci. 2021, 22, therapy. Although the in vitro studies appear promising, controlled in vivo studies are necessary 146. https://dx.doi.org/10.3390/ before we can hypothesize the introduction of Hypericum and its derivatives into clinical practice for ijms22010146 the treatment of hematologic malignancies. Received: 4 November 2020 Keywords: Hypericum; St. John’s wort; hypericin; hyperforin; leukemia; lymphoma; apoptosis; Accepted: 24 December 2020 multidrug resistance; photodynamic therapy Published: 25 December 2020 Publisher’s Note: MDPI stays neu- tral with regard to jurisdictional claims 1. Introduction in published maps and institutional affiliations. The Hypericum genus is broadly allocated and is presently believed to include over 500 species. The Mediterranean region is a hot spot for Hypericum spp.; however, several species are present in America and Asia, and many are endemic species [1]. Among the multitude of Hypericum species, H. perforatum L. (Clusiaceae), generally named St. John’s Copyright: © 2020 by the authors. Li- wort (SJW), is one of the most relevant and notorious species. Hypericum perforatum L. censee MDPI, Basel, Switzerland. This is a perennial plant. It is widely planted in Europe, and extracts of its leaves, flowers, article is an open access article distributed and aerial elements have been employed for many years as therapeutic cures for depres- under the terms and conditions of the sion, skin wounds, and respiratory and inflammatory disorders (Figure1)[ 2–4]. It also Creative Commons Attribution (CC BY) displays an ample variety of other different biological actions, such as hypotensive, anal- license (https://creativecommons.org/ gesic, anti-infective, anti-oxidant, and spasmolytic abilities (Figure1)[ 3–7]. However, licenses/by/4.0/). Int. J. Mol. Sci. 2021, 22, 146. https://dx.doi.org/10.3390/ijms22010146 https://www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2021, 22, x Int.FOR J. PEER Mol. Sci. REVIEW2021, 22 , 146 2 of 16 2 of 15 infective, anti-oxidant,recent and investigations spasmolytic highlighted abilities (Figure that this 1) [3–7]. species However, could be advantageousrecent investi- for the cure of gations highlightedother that pathological this species situations,could be advantageous such as trigeminal for the neuralgia cure of [8 other,9], and patho- in the treatment of logical situations, suchcancer as [trigeminal10,11]. neuralgia [8,9], and in the treatment of cancer [10,11]. FigureFigure 1. 1.Therapeutic Therapeutic usefulness usefulness (red ()red and) and ascertained ascertained beneficial benefi propertiescial properties in (green in )(green of Hypericum) of Hyperi- perforatum L. cum perforatum L. The genus Hypericum includes other species utilized as medicine in diverse regions of The genus Hypericumthe world. includes Relevant other therapeutic species applicationsutilized as medicine have been in reported diverse for regionsH. polyanthemum, H. of the world. Relevantdrumondii, therapeutic H. mysorense, applications H. patulum have, and been numerous reported other for H. components polyanthemum, of the genus Hyper- H. drumondii, H. mysorense,icum as well H. patulum as several, and of theirnumerous phytocomponents other components [12–15]. of In the fact, genus to date, Hy- more than 900 pericumas well as severalchemical of elementstheir phytocomponent have been recognizeds [12–15]. from In fact,Hypericum to date,species, more than comprising 900 phloroglu- cinol products, naphthodianthrones, xanthones (principally represented by hypericin chemical elements have been recognized from Hypericum species, comprising phloroglu- and pseudohypericin as well as protohypericin and protopseudohypericin), flavonoids cinol products, naphthodianthrones, xanthones (principally represented by hypericin and (such as astilbin, rutin, miquelianin, hyperoside, quercetin, quercitrin, isoquercitrin, and pseudohypericin asI3,II8-biapigenin), well as protohypericin a group and of phloroglucinolprotopseudohypericin), derivatives flavonoids (such as hyperforin, (such adhyper- as astilbin, rutin, miquelianin,forin, hyperfirin, hyperoside, and adhyperfirin), quercetin, and quercitrin, other phenolic isoquercitrin, elements and (such I3,II8- as chlorogenic acid, biapigenin), a group3-O-coumaroylquinic of phloroglucinol deriva acid, andtives terpenoids) (such as hyperforin, [16–20]. adhyperforin, hy- perfirin, and adhyperfirin),Hypericin and other has been pheno recognizedlic elements among (such the as most chlorogenic effective acid, elements. 3-O- Both in vitro coumaroylquinic acid,and inand vivo terpenoids)studies demonstrated [16–20]. that the red-colored pigment hypericin was primarily Hypericin hasresponsible been recognized for the among therapeutic the actionsmost effective of Hypericum elements.[21,22 Both]. Hypericin in vitro operatesand as an anti- in vivo studies demonstrateddepressant drug that through the red- variouscolored systems, pigment such hyperi as 5-hydroxytryptamine1cin was primarily re- receptor and g- sponsible for the therapeuticaminobutyric actions acid A of receptor Hypericum binding, [21,22]. the inhibition Hypericin of glutamateoperates as release, an anti- and the reduction depressant drug throughof dopamine- variousb-hydroxylase systems, such [23 ].as This 5-hydroxytryptamine1 substance operates by receptor decreasing and the γ viral- infectivity aminobutyric acid andA receptor proliferation binding, [24]. the Hypericin inhibition is also of glutamate a multi-layered release, participant and the reduc- in cell signaling [25]. tion of dopamine-βHypericin-hydroxylase reduces [23]. the This amounts substance of epidermal operates growth by decreasing factor receptor the tyrosineviral in- kinase, insulin receptors, and protein kinase C, abolishes the phorbol-12-myristate-13-acetate and tumor fectivity and proliferation [24]. Hypericin is also a multi-layered participant in cell signal- necrosis factor a (TNF-a)-caused stimulation of nuclear factor k-light-chain-enhancer of ing [25]. Hypericin reduces the amounts of epidermal growth factor receptor tyrosine ki- activated B cells (NF-kB), and inhibits the synthesis of prostaglandin-E2 and interleukin nase, insulin receptors,6 [26– and28]. protein kinase C, abolishes the phorbol-12-myristate-13-ace- tate and tumor necrosisFinally, factor as α mentioned(TNF-α)-caused before, stimulation the antiproliferative of nuclear capacities factor κ of-light-Hypericum species chain-enhancer of andactivated their derivativesB cells (NF- haveκB), beenand assessedinhibits the in several synthesis cancer of prostaglandin- cell lines, presenting data on E2 and interleukinthe 6 [26–28]. bioactivity of single component and combinations, such as petrol, methanol, ethanol, Finally, as mentioneddichloromethane, before, the ethyl antiproliferative acetate, and petrol capacities ether extracts.of Hypericum species and their derivatives have Thebeen purpose assessed of in this several review cancer is to analyzecell lines, the presenting data present
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