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Pharmanutrition Cannflavins from Hemp Sprouts, a Novel Cannabinoid-Free Hemp Food Product, Target Microsomal Prostaglandin E

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Pharmanutrition Cannflavins from Hemp Sprouts, a Novel Cannabinoid-Free Hemp Food Product, Target Microsomal Prostaglandin E PharmaNutrition 2 (2014) 53–60 Contents lists available at ScienceDirect PharmaNutrition j o u r n a l h o m e p a g e : w w w . e l s e v i e r . c o m / l o c a t e / p h a n u Cannflavins from hemp sprouts, a novel cannabinoid-free hemp food product, target microsomal prostaglandin E 2 synthase-1 and 5-lipoxygenase Oliver Werz a,*, Julia Seegers b, Anja Maria Schaible a, Christina Weinigel a, Dagmar Barz c, Andreas Koeberle a, Gianna Allegrone d, Federica Pollastro d, Lorenzo Zampieri d, Gianpaolo Grassi e, Giovanni Appendino d,* aDepartment of Pharmaceutical / Medicinal Chemistry, Institute of Pharmacy, University of Jena, Philosophenweg 14, D-07743 Jena, Germany bDepartment for Pharmaceutical Analytics, Pharmaceutical Institute, University of T ubingen,¨ Auf der Morgenstelle 8, D-72076 Tuebingen, Germany cInstitute of Transfusion Medicine, Jena University Hospital, 07743 Jena, Germany dDipartimento di Scienze del Farmaco, Universit a` del Piemonte Orientale, Largo Donegani 2, 28100 Novara, Italy eConsiglio per le Ricerca e la sperimentazione in Agricoltura, Centro di Ricerca per le Colture Industriali, CRA, CIN, Viale G. Amendola 82, 45100 Rovigo, Italy a r t i c l e i n f o a b s t r a c t Article history: Hemp seeds are of great nutritional value, containing all essential amino acids and fatty acids in sufficient Received 8 April 2014 amount and ratio to meet the dietary human demand. Hemp seeds do not contain cannabinoids, and because Received in revised form 12 May 2014 of their high contents of ω -3 fatty acids, are enjoying a growing popularity as a super-food to beneficially Accepted 12 May 2014 affect chronic inflammation. Seeds also lack the typical phenolics of hemp leaves and inflorescences, but we found that sprouting, while not triggering the production of cannabinoids, could nevertheless induce the Keywords: Hemp production of the anti-inflammatory prenylflavonoids cannflavins A and B. This effect was especially marked Plant-derived food in Ermo, a cannabinoid-free variety of Cannabis sativa L. Microsomal prostaglandin E2 synthase (mPGES-1) Cannflavins and 5-lipoxygenase (5-LO) were identified as the molecular targets of cannflavins A and B, solving an almost Inflammation three-decade old uncertainty on the mechanism of their the anti-inflammatory activity. No change on the Microsomal prostaglandin E2 synthase fatty acid profile was observed during sprouting, and the presence of lipophilic flavonoids combines with the 1 high concentration of ω -3 essential acids to qualify sprouts from Ermo as a novel anti-inflammatory hemp 5-Lipoxygenase food product worth considering for mass production and commercial development. c 2014 Elsevier B.V. All rights reserved. 1. Introduction contents that would perform very poorly as sources of drug mate- rial [ 1 ]. Currently, hemp seeds are mostly used as staple in certain The nutritional virtues of hemp seeds can hardly be underesti- animals, and especially for some birds too, but hemp seed products mated, since, virtually unique between food plants, they contain all (whole or dehulled hemp grains, hemp oil, hemp flour, hemp protein essential amino acids and fatty acids in sufficient amount and ratio powder, hemp substitute milk, hemp tofu, hemp butter) are enjoying to meet the human demand [ 1 ]. Unsurprisingly, hemp was one of the a growing popularity in human nutrition, where they have attained first “grain” plants domesticated by man [ 2 ], and, starting from the na- a super-food status because of a combination of healthy fatty acids tive Central Asia, hemp cultivation spread all over the world because composition, high contents of proteins (20–25%) and vitamins, and, of its multipurpose use as a source of nutrition and fiber as well as a last but not least, they have a pleasant nutty taste also [ 3 ]. Hemp medicinal / ritual plant [ 2 ]. Per se , hemp seeds do not contain cannabi- seeds contain up to 35% of oil, with an 80% concentration of polyun- noids, but, just like the seeds from poppy or peppers, their surface can saturated acids, and a ca. 3:1 ratio between linoleic (LA, ω -6)- and be contaminated by compounds present in the plant matrix in which α-linolenic (ALA, ω -3) acids [ 3 ]. Hemp oil is one of the very few edi- they are hosted, eventually becoming a source of trace amounts of ble oils that contains significant amounts (up to 7%) of γ-linolenic acid them (alkaloids for poppy seeds, capsaicinoids for hot pepper seeds, (GLA) and stearidonic acid (SDA, 18:4n3) (up to 1.5%). GLA and SDA cannabinoids for hemp seeds) [ 1 ]. Because of regulatory limits on the attenuate the formation of inflammatory prostanoids from arachi- contents of psychoactive cannabinoids in hemp products, hemp seeds donic acid [ 4 ], overall making hemp oil unique in terms of capacity to are produced from strains bred for low tetrahydrocannabinol (THC) increase tissue concentration of n -3 polyunsaturated fatty acids and to decrease the production of inflammatory eicosanoids. Because of the anti-inflammatory profile of their fatty acid composition, hemp seed food products could therefore beneficially affect pathological * Corresponding authors. E-mail addresses: [email protected] (O. Werz) conditions characterized by chronic inflammation, as suggested, for [email protected] (G. Appendino). 2213-4344/ $ - see front matter c 2014 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.phanu.2014.05.001 54 O. Werz et al. / PharmaNutrition 2 (2014) 53–60 instance, by a clinical study on atopic dermatitis [ 5 ], and various anec- 2.3. Production of sprouts dotal reports [ 5 ]. By decreasing platelet aggregation, hemp seed oil could also reduce cardiovascular risk [ 6 ]. Seeds (50 g) were washed in running water, sterilized with a short In the context of hemp seed food, little attention has been given (5 min) treatment with hydrogen peroxide, and then rinsed with to sprouts, despite their possibility to expand the nutritional use of running water. Germination was carried out in a VitaSeed domestic hemp not only in culinary terms, but also phytochemically, exploit- equipment for 5 days under dark, with changing the water every day. ing the expression of new metabolic pathways induced by germina- The sprouted seeds were washed, and, after removing their tegument tion. Germination-associated changes in the phytochemical profile of manually, were dried in an oven at 50 ◦C for 2 days. seeds are well documented [ 7 ], and have spurred the commercial de- velopment of sprouts enriched in specific phytochemicals, as shown 2.4. Isolation of cannflavin A from C. sativa var. Ermo by sulforaphane-rich broccoli sprouts [ 8 ]. Quantitative changes in the amount of specific phytochemicals have also been reported, as well Powdered dried plant material (900 g) was twice extracted with as a general remodeling of the whole profile of specific secondary acetone (ratio plant–solvent 1:9), to afford, after evaporation 32 g metabolites. Thus, the triterpenoid profile of pumpkin seeds is com- (3.5%) of a dark oil, that was dissolved in the minimal amount of pletely changed by sprouting, with the replacement of multiflorane methanol and adsorbed on a bed of RP18 silica gel (160 g). Vacuum- p -aminobenzoate triterpenoid esters with bryonolic acid [ 9 ], a potent filtration with methanol afforded a de-pigmented and de-waxed frac- triterpene inducer of anti-inflammatory and antioxidant genes [ 10 ]. tion (12 g) as a brownish gum, next purified by gravity column chro- Since the production of cannabinoid is associated with the presence matography on silica gel using petroleum ether–EtOAc as eluent (from of specific glandular hairs typical of foliar and floral hemp tissues [ 11 ], 7:3 to 5:5). A first crop of CFA( 1 ) (80 mg) was obtained from the more sprouting was unlikely to induce their synthesis or accumulation. On polar fractions of the column. The mother liquors (880 mg) were fur- the other hand, hemp is a prolific producer of structurally unique ther purified by flash-chromatography on silica gel, using petroleum phenolics (cannflavins, cannabispiranes, canniprenes), present in the ether–EtOAc 6:4 as eluent to afford a fraction that crystallized to pro- leaves and flowers, but absent in the seeds [ 12 ]. Since beneficial prop- vide 15 further mg of CFA( 1 ). The mother liquors (280 mg) contained erties have been associated to these compounds [ 13 ], the induction additional amounts of CFA( 1 ) that, however, could not be induced of their production by sprouting might, in principle, adds value to the to crystallize and were impure for the presence of other phenolics, product. including CFB( 2 ). The overall yield of crystalline CFA( 1 ) was 95 mg In this context, we have focused on cannflavin A (CVA, 1 ) and (0.011% on dried plant material). By NMR-inspection of the mother B (CVB, 2 ), a pair of prenylated flavonoids unique to hemp [ 14 ]. liquors, an estimated similar amount of CFA( 1 ) was present in the Inhibition of prostanoid formation has previously been demonstrated mother liquors. for cannflavins [ 15 ], implying anti-inflammatory activity that might nicely complement one of the ω -3 fatty acids present in the seeds, 2.5. Synthesis of cannflavin B and overall increasing the value of hemp seed products as an anti-inflammatory nutritional support. Critical to this project was The published protocol [ 14 ] was used without any significant mod- also the clarification of the mechanism(s) by which cannflavins ification. inhibit prostanoid synthesis, an issue that, despite almost three- decade of studies on these compounds [ 15 ], is still unresolved. 2.6. Determination of the lipid contents of seeds and sprouts The overall amounts of lipids was estimated by exhaustive hexane extraction. Oven-dried (heating in a ventilated oven at 50 ◦C for 48 h) powdered seeds and sprouts (10 g each) were extracted with hexane at room temperature (3 × 100 mL).
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