Open Access

Screening of Korean medicinal plants for possible osteoclastogenesis effects in vitro

  • Yu Na Youn1,
  • Erang Lim1,
  • Nari Lee3,
  • Young Seop Kim2,
  • Min Seon Koo3 and
  • Soon Young Choi1Email author
Genes & Nutrition20072:62

https://doi.org/10.1007/s12263-007-0062-1

Published: 16 November 2007

Abstract

Bone undergoes continuous remodeling through bone formation and resorption, and maintaining the balance for skeletal rigidity. Bone resorption and loss are generally attributed to osteoclasts. Differentiation of osteoclasts is regulated by receptor activator of nuclear factor NF-kB ligand (RANKL), a member of tumor necrosis factor family. When the balance is disturbed, pathological bone abnormality ensues. Through the screening of traditional Korean medicinal plants, the effective molecules for inhibition and stimulation of RANKL-induced osteoclast differentiation in mouse bone marrow macrophages were identified. Among 222 methanol extracts, of medicinal plants, 10 samples exhibited ability to induce osteoclast differentiation. These include Dryobalanops aromatica, Euphoria longana, Lithospermum erythrorhizon, Prunus mume, Prunus nakaii, and Polygonatum odoratum. In contrast, Ailanthus altissima, Curcuma longa, Solanum nigrum, Taraxacum platycarpa, Trichosanthes kirilowii, and Daphne genkwa showed inhibitory effects in RANKL-induced osteoclast differentiation.

Keywords

BoneMedicinal plantsOsteoclastOsteoclastogenesisTRAP assay

Introduction

Bone destruction is observed in advanced cases of rheumatoid arthritis and the neoplastic diseases, osteoporosis, and periodontitis. The balance between bone formation and resorption is tightly regulated by osteoblast and osteoclast, respectively, to maintain the homeostasis of our skeleton. Osteoclasts are sole bone-resorptive multinucleated cells (MNCs) that derived from hematopoietic cells. Excessive osteoclastogenesis or activation of mature osteoclasts causes the bone destruction which is implicated in rheumatoid arthritis, osteoporosis, multiple myeloma and bone metastasis.

Bone mineral density (BMD) and bone metabolism are affected by genetic, endocrine, mechanical and nutritional factors, with interactions among the different factors [1]. Bone mass in adult humans decreases with age, leading to an increased risk of fractures. Osteoporosis occurs frequently in postmenopausal women due to decrease in estrogen levels. Despite its positive effects on the bone physiology, estrogen replacement therapy is no longer recommended as the first choice therapy for the prevention and treatment of the postmenopausal osteoporosis because it increases the risks of cardiovascular, thromboembolic, and breast cancer [2]. As an alternative way to the hormone therapy, the use of phytoestrogens has attracted attention [3]. Nutritional factors are of particular importance to bone health because they are modifiable [4].

Treating perimenopausal and postmenopausal women with 40 g/day soy protein isolate providing 80–90 mg/day of isoflavones attenuated the loss of bone mineral density in the spine but not in other sites [58]. Onion and mixtures of vegetables, salads and herbs inhibit the bone resorption when metabolic acid is completely buffered with potassium citrate [9, 10]. Sage, rosemary and thyme, which are the herbs rich in essential oil, also strongly inhibit bone resorption. There is a long history in the use of essential oils as medical applications for the relief of head and chest colds as well as pain [10]. Natural products of plant origin are still a major part of traditional medicinal systems in Korea. Korean herbal formulations, such as Yukmi-jihang-tang and Dae-bo-won-chun, were reported for their preventive effect on the progress of bone loss in the rats [11, 12].

To examine the inhibitory effects of Korean traditional medicinal plant extracts on the bone resorption in the mouse macrophage cells, we have screened the inhibitory activities. Here, we report that the methanol extracts of Ailanthus ltissima, Curcuma longa, Solanum nigrum, Taraxacum platycarpa, Trichosanthes kirilowii and Daphne genkwa inhibit osteoclastogenesis.

Materials and methods

Reagents

The methanol extract was of medicinal plants provided by Dr. Young Seop Kim (Korea Research Institute of Chemical Technology, South Korea). Minimal essential medium alpha modification (α-MEM), fetal bovine serum (FBS), and antibiotics were purchased from Well Gene (Dae gu, South Korea). Macrophage colony stimulation factor(M-CSF) were purchased from R&D Systems. TRANCE was provided by Dr. Lee (University of Ewha Women’s University, Korea). TRAP staining kit (Leukocyte acid phosphatase kit) was obtained from Sigma (St. Louis, Miss., USA).

Culture of mouse bone marrow mononuclear cells

The bone marrow cells were isolated from the long bones of 4-week-old C57BL/6 male mice, and cultured with α-MEM/10% FBS/1% antibiotics with M-CSF (25 ng/ml) in a humidified incubator (5% CO2 in air) at 37°C. After 24 h of cultures, the non-adherent cells were collected and centrifuged to obtain the bone marrow macrophage (BMM) cells which were the depleted stromal cells. For the osteoclast differentiation experiments, the BMM cells were cultured in 96-well plates (3 × 104/well) with M-CSF (50 ng/ml), TRANCE (400 ng/ml) and stimuli for 6–9 days.

Tartrate-resistant acid phosphatase (TRAP) assay

To determine the characteristics of osteoclast differentiation, cells were fixed with 3.7% formaldehyde for 10 min and then washed with distilled water. Then the cells were stained for TRAP with 0.1 M acetate solution containing 6.76 mM sodium tartrate, 0.12 mg/ml naphthol AS-MX phosphate, and 0.07 mg/ml of fast Garnet GBC solution as described in the manufacturer’s instructions (Leukocyte acid phosphatase kit) for 30 min at room temperature.

Results and discussion

The screening of 222 specimens of Korean traditional medicinal plants for possible tartrate-resistant acid phosphatase inhibitory and stimulatory effects was performed (Table 1). The methanol extracts of Dryobalanops aromatica, Euphoria longana, Lithospermum erythrorhizon, Prunus mume, Prunus nakaii, Polygonatum odoratum, Alpinia oxyphylla, and Sambucus williamsii var.coreana showed stimulatory effects for osteoclast differentiation by TRAP assay (Fig. 1b; Table 2). However, Ailanthus altissima, Curcuma longa, Solanum nigrum, Taraxacum platycarpa, Trichosanthes kirilowii, Daphne genkwa, Gleditsia japonica, Picrasma quassioides, Sanguisorba officinalis, Citrus aurantium, Cnidium officinale, Lindera strychnifolia, Melandrium firmum, Phaseolus angularis, Rheum undulatum and Taraxacum platycarpa suppressed the osteoclastogenesis (Fig. 1c; Table 3).
Table 1

Korean medicinal plants for possible osteoclastogenesis in this experiment

Body

Flower

Seed

Root

Other

Agrimonia pilosa

Althaea rosea

Allium tuberosum

Aconitum carmichaeli

Boswellia carterii

Akebia quinata

Chrysanthemum indicum

Alpinia katsumadai

Aconitum ciliare

Dryobalanops aromatica

Albizzia julibrissin

Daphne genkwa

Alpinia oxyphylla

Aconitum koreanum

Flammulina velutipes

Artemisia apiace

Eugenia caryophyllata

Amomum tsao-ko

Aconium carmichaeli

Ganoderma lucidum

Artemisia asiatica

Lonicera japonica

Arctium lappa

Acyranthes japonica

Lygodium japonica

Artemisia capillaris

Pinus densiflora

Brassica chinensis var.oleifera

Adenophora remotiflorus

Lyophyllum ulmarium

Biota orientalis

Pueraria thunbergiana

Brassica juncea

Adenophora triphylla

Phyllostachys bambusoides

Cassia angustifolia

Tussilago farfar

Broussonetia kazinoki

Ailanthus altissima

Phyllostachys nigra var.henonis

Cephalonoplos segetum

Typha orientalis

Cannabis sativa

Alisma orientale

Pinus densiflora

Chelidonium majus

Zea mays

Capsicum annuum

Allium macrostemon

Pleurotus eryngii

Chrysanthemum sibiricum

 

Carpesium abrotanoides

Alpinia officinarum

Polyporus umbellatus

Cinnamomum cassia

 

Carthamus tinctorius

Anemarrhena asphodeloides

Poria cocos

Circium japonicum

 

Cassia tora

Anthriscus sylvestris

 

Eclipta prostrata

 

Celosia argentea

Arisaema amurense

 

Elsholtzia ciliata

 

Castanea crenata

Aristolochia cordata

 

Epimedium koreanum

 

Citrus aurantium

Asiasarum sieboldi

 

Equisetum hiemale

 

Citrus unshiu

Asparagus cochinchinensis

 

Eriocaulon sieboldianum

 

Coix lachryma-jobi

Aster tataricus

 

Eugenia aromatica

 

Croton tiglium

Atractylodes japonica

 

Gallus domesticus

 

Cucumis melo

Bretilla striata

 

Geranium thunbergii

 

Cuscusta chinensis

Caragana sinica

 

Ginkgo biloba

 

Dianthus chinensis

Cistanche deserticola

 

Gleditsia japonica

 

Draba nemorosa

Clematis mandshurica

 

Houttuynia cordata

 

Euphorbia lathyris

Cnidium officinale

 

Kalopanax pictus

 

Euphoria longana

Cocculus trilobus

 

Lonicera japonica

 

Euryale ferox

Codonopsis pilosula

 

Lophatherum gracile

 

Evodia officinalis

Coptis japonica

 

Loranthus parasiticus

 

Foeniculum vulgare

Cremastra variabilis

 

Lycopus coreanus

 

Gardenia jasminoides

Curcuma longa

 

Melandrium firmum

 

Gleditsia japonica

Cynanchum wilfordii

 

Melia azedarach var.japonica

 

Glycine max

Cyperus rotundus

 

Mucuna birdwoodiana

 

Gossypium nanking

Dalbergia odorifera

 

Nelumbo nucifera

 

Hordeum vulgare

Dioscorea japonica

 

Nepeta japonica

 

Hovenia dulcis

Drynaria fortunei

 

Orostachys japonicus

 

Juglans sinensis

Erucibe obtusifolia

 

Persicaria tinctoria

 

Kochia scoparia

Dryopteris crassirhizoma

 

Phyllostachys nigra

 

Luffa cylindrical

Euphorbia kansui

 

Polygonum aviculare

 

Lycium chinense

Euphorbia pekinensis

 

Portulaca oleracea

 

Lycopodium clavatum

Gastrodia elata

 

Pterocarpus santalinus

 

Phaseolus angularis

Gentiana macrophylla

 

Rhus verniciflua

 

Phaseolus radiatus

Gentiana scabra

 

Sambucus williamsii var.coreana

 

Pinus koraiensis

Glycyrrhiza glabra

 

Sargassum fusiforme

 

Piper longum

Isatis tinctoria

 

Saururus chinensis

 

Piper nigrum

Laminaria japonica

 

Selaginella tamariscina

 

Plantago asiatica

Lindera strychnifolia

 

Solanum nigrum

 

Polygonatum odoratum

Liriope platyphylla

 

Taraxacum platycarpa

 

Prunus armeniaca

Lithospermum erythrorhizon

 

Tetrapanax papyriferus

 

Prunus mume

Lycium chinense

 

Ulmus macrocarpa

 

Prunus nakaii

Morinda officinalis

 

Uncaria senensis

 

Psoralea corylifolia

Nardostachys chinensis

 

Vitis vinifera

 

Ricinus communis

Paeonia albiflora

 
  

Rosa multiflorsa

Paeonia japonica

 
  

Sesamum indicum

Paeonia moutan

 
  

Siegesbeckia pubescens

Paeonia obovata

 
  

Terminaria chebula

Panax ginseng

 
  

Torreya nucifera

Panax notoginseng

 
  

Tribulus terrestris

Patrinia villosa

 
  

Trigonella foenum- graecum

Pinellia ternate

 
  

Ulmus macrocarpa

Platycodon grandiflorum

 
  

Xanthium strumarium

Polygonatum sibiricum

 
   

Polygonum cuspidatum

 
   

Polygonum multiflorum

 
   

Rehmania glutinosa var.purpurea

 
   

Rheum palmatum

 
   

Rheum undulatum

 
   

Rubia alkane

 
   

Sanguisorba officinalis

 
   

Scrophularia buergeriana

 
   

Scutellaria baicalensis

 
   

Smilax china

 
   

Trichosanthes kirilowii

 
   

Zingiber officinale

 
Fig. 1

The effects of the extracts in osteoclastogenesis of mouse macrophage by TRAP staining. a Control. b Lithospermum erythrorhizon stimulate osteoclastogenesis. c Shows suppression effects of Gleditsia japonica in osteoclastogenesis

Table 2

The positive effects of the crude compounds in osteoclastogenesis

Botanical name

Part used

Effect

0.1 mg/ml

0.2 mg/ml

Alpinia oxyphylla

Seed

Staining

Differentiation

Dryobalanops aromatica

Resin

Differentiation

Differentiation

Euphoria longana

Seed

Differentiation

Differentiation

Lithospermum erythrorhizon

Root

Differentiation

Differentiation

Plantago asiatica

Seed

Differentiation

Toxic

Polygonatum odoratum

Seed

Differentiation

Differentiation

Prunus mume

Seed

Differentiation

Differentiation

Prunus nakaii

Seed

Differentiation

Differentiation

Sambucus williamsii var.coreana

Body

Staining

Differentiation

Zea mays

Flower

Differentiation

Suppression

Table 3

The negative effects of the crude compounds in osteoclastogenesis

Botanical name

Part used

Effect

0.1 mg/ml

0.2 mg/ml

Ailanthus altissima

Root

Suppression

Suppression

Citrus aurantium

Seed

Suppression

Toxic

Cnidium officinale

Root

Suppression

Toxic

Curcuma longa

Root

Suppression

Suppression

Daphne genkwa

Flower

Suppression

Suppression

Eugenia caryophyllata

Flower

Suppression

Suppression

Gleditsia japonica

Thorn

Staining

Suppression

Lindera strychnifolia

Root

Suppression

Toxic

Melandrium firmum

Body

Suppression

Toxic

Orostachys japonicus

Body

Suppression

Staining

Phaseolus angularis

Seed

Suppression

Soxic

Picrasma quassioides

Body

Staining

Suppression

Rheum undulatum

Root

Suppression

Toxic

Sanguisorba officinalis

Root

Staining

Suppression

Solanum nigrum

Body

Suppression

Suppression

Taraxacum platycarpa

Body

Suppression

Toxic

Trichosanthes kirilowii

Root

Suppression

Suppression

The positive effects of nutritional supplement with herbal formulation extracts on bone mineral density and height in prepubescent children were reported [13].

The methanol extract and its major bioactive compound, gallic acid of Orostachys japonicus, greatly enhanced the activities of hepatic alcohol dehydrogenase, the microsomal ethanol-oxidizing enzyme, and aldehyde dehydrogenase in a dose dependent manner [14]. In additions, the inhibitory effects on the formation of carcinogenic N-nitrosodimethylamine were observed [15].

The main root of Aconitum carmichaelli has been used in Chinese herbal medications mainly for the treatment of musculoskeletal disorders, and the herbal formulations containing it have been used for the treatment of rheumatism and heart failure as well as improvement of the immune system and retarding aging [16, 17]. The plant contained the highly toxic C19 diterpenoid alkaloids of aconitine, mesaconitine and hypaconitine. A. altissima (synonym A. glandulosa) has been used to treat cold, gastric diseases, and cancer. From the bioassay-oriented study, it is reported that it has cytotoxicity and antiproliferative activities. It contains quassinoids, indole and β-carboline alkaloids. These compounds are reported for antitubercular, antimalarial, and inhibitory effects against Epstein-Barr virus [18]. Furthermore, other Ailanthus species have anti-cancer agents [18]. Curcuma longa has been in use for centuries as a dye and also as a component of curry powder [19]. Daphne genkwa has an antitumor activity. The anti-tumor constituent, daphnodorin complex, was reported to have inhibitory effects on tumor growth and metastasis by protecting host immunocyte viability and proliferation potential, thus selectively inhibiting tumor cell proliferation [20]. Daphnane diterpene esters from flower buds induced apoptosis in human pro-myelocytic leukemia HL-60 cells. This esters were found to have suppressed the growth of Lewis lung carcinomas (LLC) inoculated into mice [21]. An anticoagulant purified from Taraxacum platycarpum has been used as an inflammatory agent to treat colitis and ulcer. In addition, this anticoagulant protein, when treated to the murine macrophage cell line RAW 264.7, induced expression of cyclooxygenase-2 (COX-2) and nitric oxide synthase, and production of anti-tumor necrosis factor-α [22]. The rhizome extract of Rheum undulatum was reported to have vasorelaxant, anti-allergic and anti-platelet aggregation activities [23, 24]. The methanolic extract of the cortex of Eugenia caryophyllata exerted the COX-2 inhibitor activity in RAW264.7 cells [25].

Eugenol is a major component of essential oil isolated from the E. caryophyllata, which was reported as an anti-cancer agent [26]. The root tuber protein of Richosanthes kirilowii suppressed the HSV-1 infection by targeting the mitogen-activated protein kinase (MAPK) family pathway [27]. Water extract of the root of Lindera strychnifolia slowed down the progression of diabetic nephropathy in db/db mice [28]. Citrus fruits were found to be a potentially important source of anti-inflammatory flavonoids in the human diet [29]. The peel of citrus fruits is a rich source of flavones. Nitric oxide (NO) has been implicated in a variety of pathophysiological conditions, including inflammation, carcinogenesis, and atherosclerosis [29]. The ethyl acetate soluble fraction of Cnidium officinale MAKINO inhibited neuronal cell death by reducing excessive NO production in LPS-treated rat hippocampal slice cultures and microglia cells [30]. The extract of Phaeseolus angularis (Adzuki bean) exhibited estrogen-like activities [31] but in different ways from Phaseolus lunatus L.

Some medicinal plants showed stimulatory effects on osteoclast differentiation. The aqueous extract from the medicinal plant Dryobalanops aromatica specifically inhibited catecholamine secretion that is important in stressful states and emotional behavior [32]. The kaempferol derived from Polygonatum odoratum has been used for the treatment of chronic airway diseases [33]. Euphoria longana and Prunus mume fruit was reported to have an anti-cancer effects [34, 35]. The naphthoquinone pigment, shikonin, isolated from Lithospermum erythrorhizon, has several therapeutic potential including anti-inflammatory and anti-tumor effects [36].

From these results, we found several compounds with stimulatory or inhibitory effects on osteoclastogenesis (Tables 2, 3). There were several medicinal plants that showed strong effects on osteoclast differentiation (Table 2), even though we could not find a relationship through these results in osteoclastogenesis. The next step will be a study with single compounds purified from 30 verified plants.

Declarations

Acknowledgments

This work was supported by the Project of Bio-Food Research from the Korea Science and Engineering Foundation (KOSEF) under the Ministry of Science and Technology in Korea, and also supported by grant No. R01-2006-000-10515-0 from the Basic Research Program of the Korea Science & Engineering Foundation.

Authors’ Affiliations

(1)
Department of Biology, Sookmyung Women’s University
(2)
Korea Research Institute of Chemical Technology
(3)
Korea Food Research Institute

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