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Topical Application of Rehmannia Glutinosa Extract Inhibits Mite Allergen-Induced Atopic Dermatitis in NC/Nga Mice

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Topical Application of Rehmannia Glutinosa Extract Inhibits Mite Allergen-Induced Atopic Dermatitis in NC/Nga Mice Journal of Ethnopharmacology 134 (2011) 37–44 Contents lists available at ScienceDirect Journal of Ethnopharmacology journal homepage: www.elsevier.com/locate/jethpharm Topical application of Rehmannia glutinosa extract inhibits mite allergen-induced atopic dermatitis in NC/Nga mice Yoon-Young Sung a, Taesook Yoon a,∗, Ja Young Jang a, Sang-Joon Park b, Ho Kyoung Kim a a Center of Herbal Resources Research, Korea Institute of Oriental Medicine, Daejeon 305-811, Republic of Korea b Department of Veterinary Histology, College of Veterinary Medicine, Kyungpook National University, Daegu 702-701, Republic of Korea article info abstract Article history: Aim of the study: Rehmannia glutinosa is known in Asia as a traditional herbal medicine with anti- Received 5 July 2010 inflammatory properties. Atopic dermatitis (AD) is an inflammatory skin disease associated with Received in revised form enhanced T-helper 2 (Th2) lymphocyte responses to allergens that results in elevated serum IgE lev- 11 November 2010 els and leukocyte infiltration. Although some studies have shown that Rehmannia glutinosa extract (RGE) Accepted 19 November 2010 has anti-inflammatory and anti-allergic activities, these properties have not been demonstrated in AD. Available online 1 December 2010 This study investigated the effectiveness of RGE as a therapeutic candidate in an AD model as well as its underlying mechanism of action. Keywords: Adhesion molecule Materials and methods: The effects of RGE on mite allergen (Dermatophagoides farinae)-treated NC/Nga Anti-allergic effect mice were evaluated by skin symptom severity, ear thickness, production of serum IgE and histamine, Chemokine and expression of cytokines, chemokines, and adhesion molecules in the ear lesions. In addition, the Keratinocyte levels of thymus and activation-regulated chemokine (TARC), macrophage-derived chemokine (MDC), Rehmannia glutinosa and regulated on activation, normal T cell expressed and secreted (RANTES) produced in both TNF-␣- TNF-␣ and IFN-␥-stimulated human keratinocytes were investigated by enzyme-linked immunosorbent assay (ELISA). Results: RGE treatment of NC/Nga mice significantly reduced dermatitis scores, ear thicknesses, and serum histamine levels. Histological analyses demonstrated decreased thickening of the epidermis/dermis as well as dermal infiltration by inflammatory cells. In the ear lesions, mRNA expression levels of IL-4, TNF- ␣, VCAM-1, and ICAM-1 were inhibited by RGE treatment. RGE also suppressed the production of TARC, MDC, and RANTES in both the ear lesions and keratinocytes. Conclusions: RGE inhibits the development of AD in NC/Nga mice by suppressing the expression of cytokines, chemokines, and adhesion molecules. © 2010 Elsevier Ireland Ltd. All rights reserved. 1. Introduction IFN-␥-producing Th1 cells are highly expressed and contribute to pathogenesis during the chronic phase (Vestergaard et al., 1999). Atopic dermatitis (AD) is a chronic inflammatory skin disease Topical glucocorticoids are very effective remedies for the that is occurring in infants and children with an increasing inci- treatment of AD. However, it is well known that long-term use dence (Spergel and Paller, 2003). In AD, the clinical symptoms are of glucocorticoids frequently causes significant adverse effects characterized by pruritic and relapsing eczematous skin lesions, (Barnetson and White, 1992; Leung and Barber, 2003). Tacrolimus, which are distinguished by the infiltration of inflammatory cells, an immunosuppressant, has been evaluated for AD treatment in such as lymphocytes, macrophage, eosinophils, and granulated ointment form (Nakagawa et al., 1994; Bieber, 1998; Inagaki et al., mast cells (Soter, 1989; Leung and Bieber, 2003). T-helper 2 (Th2) 2006; Rustin, 2007). The effect of tacrolimus ointment in a dust cells, producing IL-4, IL-5, and IL-10, play major roles in the onset mite allergen-induced AD model was investigated in NC/Nga mice and development of AD (Leung et al., 2004; Homey et al., 2006). (Sasakawa et al., 2004; Oshio et al., 2009). Recently, results from Although Th2 cells are dominant during the acute phase of AD, several studies indicated that AD patients might benefit from herbal Oriental medicine therapy (Gao et al., 2005; Lee et al., 2006; Park et al., 2007; Kim et al., 2008; Makino et al., 2008). Rehmannia glutinosa, which belongs to the family of Scrophular- ∗ Corresponding author at: Center of Herbal Resources Research, Korea Institute iaceae, is a traditional, medicinal herb. It is believed that Rehmannia of Oriental Medicine, 483 Expo-ro, Yuseong-gu, Daejeon 305-811, Republic of Korea. Tel.: +82 42 868 9529. glutinosa possesses the effects of hemostasis, activation of blood cir- E-mail address: [email protected] (T. Yoon). culation, and improvement of kidney function (Zhang et al., 2008). 0378-8741/$ – see front matter © 2010 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.jep.2010.11.050 38 Y.-Y. Sung et al. / Journal of Ethnopharmacology 134 (2011) 37–44 A steamed root of Rehmannia glutinosa, known as ‘Sook-Ji-Whang’ 2.3. Induction of dermatitis in Korean, has been used in traditional Oriental medicine for treat- ing the allergic inflammatory disease (Huang, 1993). An aqueous Mice were anesthetized with ether, and the hair on the upper extract from a steamed root of Rehmannia glutinosa (RGAE) inhibits back of each animal was shaved with a clipper and a shaver 1 day the secretion of both TNF-␣ and IL-1 from mouse astrocytes, indi- before the experiments. The exposed dorsal region was treated cating that RGAE has anti-inflammatory effects on the central with ointment (Biostir-AD, Biostir, Kobe, Japan) prepared from a nervous system (Kim et al., 1999). In addition, RGAE has been shown crude extract of house dust mite Dermatophagoides farinae (DfE) as to inhibit both compound 48/80-induced systemic allergic and pas- described previously (Yamamoto et al., 2007). The DfE (mite extract, sive cutaneous anaphylaxis (PCA) reactions, two typical models of lyophilized) was mixed in ointment base (hydrophilic petrolatum) immediate-type allergic reaction (Kim et al., 1998). In a veterinary to make a 0.5% solution, referred to as DfE ointment. The oint- study, a mixture of plant extracts (Rehmannia glutinosa, Paeonia ment base (hydrophilic petrolatum) was applied to normal mice lactiflora and Glycyrrhiza uralensis) reduced erythema and pruri- instead of DfE ointment. For topical application, barrier disrup- tus in canine AD (Ferguson et al., 2006). Chemically, Rehmannia tion was achieved using 150 ␮l of a 4% sodium dodecyl sulfate glutinosa was found to contain iridoid glycosides such as catalpol, (SDS) treatment on the shaved dorsal skin and both surfaces of aucubin and ajugol (Oshio and Inouye, 1982). Aucubin inhibits each ear 3 h before DfE ointment application. One hundred micro- 12-O-tetradecanoylphorbol- 13-acetate (TPA)-induced mouse ear grams of DfE ointment were then applied on the shaved dorsal edema and production of TNF-␣ and IL-6 in mast cells (Recio et al., skin twice a week for 3 weeks. SDS treatment was repeatedly 1994; Jeong et al., 2002). Recently, it has been reported that beta- performed prior to each DfE ointment application. Protopic oint- sitosterol, one of the major constituents of Rehmannia glutinosa ment containing 0.1% tacrolimus in ointment base (Astellas Pharma (Ni et al., 1992), inhibits ovalbumin-induced airway inflammation Inc., Deerfield, IL, USA) was used as a positive control for treat- in a guinea pig asthma model (Mahajan and Mehta, 2011). These ing AD. Mice were randomly divided into four groups: (1) normal results suggest that Rehmannia glutinosa might be beneficial in the group without DfE application (8 mice); (2) control group with treatment of human allergic disorders. DfE application (100 mg/mouse) (8 mice); (3) RGE-treated group Therefore, this study investigated the effects of Rehmannia gluti- (400 ␮g/mouse) with DfE application (7 mice); and (4) protopic- nosa extract (RGE) on AD using NC/Nga mice exposed to dust mite treated group (100 ␮g/mouse) with DfE application (7 mice). The allergens as an AD model. We also determined the effects of RGE on lyophilized RGE powder was dissolved in an acetone/olive oil (4:1) chemokine production in the human keratinocyte cell line, HaCaT, mixture for topical application. The same volume of acetone/olive to examine a possible mechanism for the anti-allergic effects of oil vehicle was applied to normal and control group instead of RGE RGE. solution. On the day of fourth DfE application (day 11), RGE treat- ment was started. RGE was treated daily for 23 days. Following the last application of RGE (day 33), the mice were killed to investigate immunological and histological changes (day 34). Ear thickness was 2. Materials and methods measured twice a week using a micrometer (Mitutoyo Corporation, Kanagawa, Japan). 2.1. Preparation of Rehmannia glutinosa extract (RGE) 2.4. Evaluation of skin severity The steamed root of Rehmannia glutinosa as a dried herb was purchased from Omniherb Co. (Yeoungcheon, Korea) and authenti- Severity of dermatitis on the ear and back regions was evalu- cated based on its macroscopic characteristics by the Classification ated twice a week. The development of (1) erythema/hemorrhage, and Identification Committee of the Korea Institute of Oriental (2) scarring/dryness, (3) edema, and (4) excoriation/erosion was Medicine (KIOM). The committee was composed of nine experts scored as 0 (none), 1 (mild), 2 (moderate), or 3 (severe). The sum in the fields of plant taxonomy, botany, pharmacognosy, and her- of the individual scores comprised the dermatitis score (Matsuda bology. A voucher specimen (KIOM 79081) was deposited in the et al., 1997). herbarium of the Department of Herbal Resources Research at KIOM. The dried herb (50 g) was extracted twice with 70% ethanol 2.5. Measurement of serum total IgE and histamine levels (with a 2-h reflux), and the extract was then concentrated under reduced pressure. The decoction was filtered, lyophilized, and After blood was collected from the mice after sacrifice, serum serially stored at 4 ◦C.
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