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Untiring Researches for Alternative Resources of Rhizoma Paridis

  • Xu-Jie Qin 1,  
  • Wei Ni 1,  
  • Chang-Xiang Chen 1,  
  • Hai-Yang Liu 1
    •     
Received date: 18 April 2018; Accepted: 2 July 2018; Published online: 4 July 2018

Abstract

Rhizoma Paridis (RP, 重楼), a traditional Chinese medicine, is the rhizoma of Paris polyphylla var. yunnanensis (PPY) or P. polyphylla var. chinensis which are widely used as important raw materials for several Chinese patent drugs. However, the wild resources of these herbs have become less and less due to their slow-growing characteristics and previously excessive excavation. This review covers untiring investigations on alternative resources of RP by our research group over the past decades, including non-medicinal parts of PPY as well as other plants of Liliaceae and Liliflorae families. The arial parts of PPY and the whole plants of Trillium kamtschaticum might be alternative resources for RP based on the fact that they shared the same or similar saponins and bioactivities.

Keywords

Rhizoma Paridis    Paris polyphylla    Alternative resources    Steroidal saponins    Bioactivities    
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1 Introduction

The genus Paris (Liliaceae) comprises approximately 32 plant species throughout the world and with 26 species found in Southwest China. [1-7]. Among them, the dried rhizoma of Paris polyphylla var. yunnanensis (PPY) and P. polyphylla var. chinensis (PPC), both called Rhizoma Paridis (RP) in China, have long been recorded in Chinese Pharmacopoeia as a traditional Chinese medicine to treat furuncle, snakebite, injuries from falls and convulsion, epilepsy, and sore throat [8]. Because of their remarkable medicinal functions, PPY and PPC have been a hot topic within the medicinal chemistry and drug discovery community since the 1970s. Previous studies revealed that PPY and PPC were rich sources of spirostanol (diosgenin and pennogenin) saponins [9-24] responsible for various pharmacological effects, such as cytotoxic and antitumor [13-20], antifungal [21, 22], and haemostatic bioactivities [23, 24]. The available supplies of PPY and PPC are facing increasing shortage based on the fact that their rhizomes can only be harvested until they have grown more than 7 years and the consumption by the pharmaceutical industry of these herbs have increased sharply in recent years. Thus, it is really imperative to search for other saponins or resources that might be substitutes for RP. Over the past 34 years, in order to find valid and alternative resources of RP, our research group have made great effort to phytochemically investigated on the non-medicinal parts of PPY as well as other plants of Liliaceae and Liliflorae families according to their genetic and phylogenetic relationships, which led to the isolation of identical or similar bioactive constituents with those of RP. As a result, a total of 184 saponins and including 120 new ones were obtained and identified, some of which showed interesting bioactive effects as those of RP. This paper mainly describes our untiring researches that can provide active ingredients for alternative resources of RP.

2 Steroidal Sapogenins and Saponins

According to the fact that the steroidal saponins are the bioactive constituents of RP, the steroidal sapogenins and saponins of non-medicinal parts of PPY and other Paris, Ypsilandra, Trillium, and Tacca plants have been investigated, which led to the isolation of 17 new steroidal sapogenins and 103 steroidal saponins, along with 64 known analogues.

2.1 Non-medicinal Parts of PPY and Other Paris Species (Liliaceae)

Although the renewable aerial parts of PPY yearly have not been used as medicinal materials, in order to clarify the difference of chemical constituents between medicinal and non-medicinal parts (the stems and leaves) of PPY and to improve the efficiency of resources usage, our systematically phytochemical investigations on the non-medical parts of PPY led to the isolation of 22 new steroidal saponins (Fig. 1; Table 1), named chonglouosides SL-1-SL-20 (1-20) [25-27], polyphyllosides Ⅲ (21) and Ⅳ (22) [28], as well as two new steroidal sapogenins, named 27-hydroxylpennogenin (23) and 27, 23β-dihydroxylpennogenin (24) [29]. In addition, three new pennogenin saponins (25-27) [30, 31], three new spirostanol saponins (28-30) and one new cholestane saponin (31) [32], and two new highly oxygenated spirostanol saponins (32 and 33) [33] were isolated from P. axialis (rhizomes), P. verticillata (aerial parts), and P. polyphylla var. stenophylla (rhizomes), respectively (Fig. 1). It was worth noting that saponins 7 and 8 were C22-steroidal lactone saponins which were isolated from genus Paris for the first time, while 9-15 were rare nuatigenin saponins with a furan ring that firstly obtained from species of Liliaceae family.

Fig. 1

New steroidal sapogenins and saponins from non-medicinal parts of PPY and other Paris species

Table 1

New steroidal sapogenins and saponins from non-medicinal parts of PPY and other Paris species

Nos Names Species Parts References
1 Chonglouoside SL-1 PPY Stems and leaves [25]
2 Chonglouoside SL-2 PPY Stems and leaves [25]
3 Chonglouoside SL-3 PPY Stems and leaves [25]
4 Chonglouoside SL-4 PPY Stems and leaves [25]
5 Chonglouoside SL-5 PPY Stems and leaves [25]
6 Chonglouoside SL-6 PPY Stems and leaves [25]
7 Chonglouoside SL-7 PPY Stems and leaves [26]
8 Chonglouoside SL-8 PPY Stems and leaves [26]
9 Chonglouoside SL-9 PPY Stems and leaves [27]
10 Chonglouoside SL-10 PPY Stems and leaves [27]
11 Chonglouoside SL-11 PPY Stems and leaves [27]
12 Chonglouoside SL-12 PPY Stems and leaves [27]
13 Chonglouoside SL-13 PPY Stems and leaves [27]
14 Chonglouoside SL-14 PPY Stems and leaves [27]
15 Chonglouoside SL-15 PPY Stems and leaves [27]
16 Chonglouoside SL-16 PPY Stems and leaves [27]
17 Chonglouoside SL-17 PPY Stems and leaves [27]
18 Chonglouoside SL-18 PPY Stems and leaves [27]
19 Chonglouoside SL-19 PPY Stems and leaves [27]
20 Chonglouoside SL-20 PPY Stems and leaves [27]
21 Polyphylloside Ⅲ PPY Aerial parts [28]
22 Polyphylloside Ⅳ PPY Aerial parts [28]
23 27-Hydroxyl-pennogenin PPY Aerial parts [29]
24 27, 23β-Dihydroxyl-pennogenin PPY Aerial parts [29]
25 Pennogenin-3-O-β-D-glucopyranosyl-(1→3)-[α-L-rhamnopyranosyl(1→2)]-β-D-glucopyranoside P. axialis Rhizomes [30]
26 24α-Hydroxyl-pennogenin-3-O-β-D-glucopyranosyl-(1→3)-[α-L-rhamnopyranosyl(1→2)]-β-D-glucopyranoside P. axialis Rhizomes [30]
27 24α-Hydroxyl-pennogenin-3-O-α-L-rhamnopyranosyl-(1→2)-[α-L-arabinofuranosyl(1→4)]-β-D-glucopyranoside P. axialis Rhizomes [31]
28 Parisverticoside A P. verticillata Aerial parts [32]
29 Parisverticoside B P. verticillata Aerial parts [32]
30 Parisverticoside C P. verticillata Aerial parts [32]
31 Parisverticoside D P. verticillata Aerial parts [32]
32 Paristenoside A P. polyphylla var. stenophylla Rhizomes [33]
33 Paristenoside B P. polyphylla var. stenophylla Rhizomes [33]

2.2 Ypsilandra Species (Liliaceae)

Ypsilandra (Liliaceae), a small genus including only five species, is widely distributed in Southwest China and Myanmar [34]. We speculate that Ypsilandra species should produce similar steroidal derivatives as those of Paris due to their genetic and phylogenetic relationships. Although Y. thibetica has been used as a folk medicine for treating uterine bleeding and traumatic hemorrhage [35, 36], the chemical constituents of Ypsilandra species have not been studied before our investigations. A total of two new sapogenins and 38 saponins (Fig. 2; Table 2) have been reported from the whole plants of Y. thibetica, Y. parviflora, and Y. yunnanensis up to 2017 by our research group, namely, isoypsilandrogenin (34), isoypsilandrosides A (35) and B (36), ypsilandrosides A (37) and B (38) [37], ypsilandrosides C-G (39-43) [38], ypsilandrosides H-L (44-48) [39], ypsilandrosides M-O (49-51) [40], ypsiparosides A-G (52-58) [41], ypsilanogenin (59), ypsilanogenin 3-O-β-D-glucopyranoside (60), 4′-acetylypsilanogenin 3-O-β-D-glucopyranoside (61) [42], ypsilandrosides P-R (62-64) [43], ypsilandrosides S (65) and T (66) [44], ypsiyunnosides A-E (67-71) [45], and ypsilactosides A (71) and B (72) [46]. These new saponins were usually the oxygenated derivatives at C-6, C-7, C-11, and C-12 of those known analogues and some of these isolates had unpredicted aglycones. To be more specific, saponins 44 and 45 represented the first example with a novel 5(6→7) abeo-steroidal aglycone, whereas 59-61 were unusual 23-spirocholestane derivatives and 67 possessed a rare 6/6/6/5/5 fused-rings cholestanol skeleton.

Fig. 2

New steroidal sapogenins and saponins from Ypsilandra species

Table 2

New steroidal sapogenins and saponins from Ypsilandra species (Liliaceae)

Nos. Names Species Parts References
34 Isoypsilandrogenin Y. thibetica Whole plants [37]
35 Isoypsilandroside A Y. thibetica Whole plants [37]
36 Isoypsilandroside B Y. thibetica Whole plants [37]
37 Ypsilandroside A Y. thibetica Whole plants [37]
38 Ypsilandroside B Y. thibetica Whole plants [37]
39 Ypsilandroside C Y. thibetica Whole plants [38]
40 Ypsilandroside D Y. thibetica Whole plants [38]
41 Ypsilandroside E Y. thibetica Whole plants [38]
42 Ypsilandroside F Y. thibetica Whole plants [38]
43 Ypsilandroside G Y. thibetica Whole plants [38]
44 Ypsilandroside H Y. thibetica Whole plants [39]
45 Ypsilandroside I Y. thibetica Whole plants [39]
46 Ypsilandroside J Y. thibetica Whole plants [39]
47 Ypsilandroside K Y. thibetica Whole plants [39]
48 Ypsilandroside L Y. thibetica Whole plants [39]
49 Ypsilandroside M Y. thibetica Whole plants [40]
50 Ypsilandroside N Y. thibetica Whole plants [40]
51 Ypsilandroside O Y. thibetica Whole plants [40]
52 Ypsiparoside A Y. parviflora Whole plants [40]
53 Ypsiparoside B Y. parviflora Whole plants [41]
54 Ypsiparoside C Y. parviflora Whole plants [41]
55 Ypsiparoside D Y. parviflora Whole plants [41]
56 Ypsiparoside E Y. parviflora Whole plants [41]
57 Ypsiparoside F Y. parviflora Whole plants [41]
58 Ypsiparoside G Y. parviflora Whole plants [41]
59 Ypsilanogenin Y. thibetica Whole plants [42]
60 Ypsilanogenin 3-O-β-D-glucopyranoside Y. thibetica Whole plants [42]
61 4′-Acetylypsilanogenin 3-O-β-D-glucopyranoside Y. thibetica Whole plants [42]
62 Ypsilandroside P Y. thibetica Whole plants [43]
63 Ypsilandroside Q Y. thibetica Whole plants [43]
64 Ypsilandroside R Y. thibetica Whole plants [43]
65 Ypsilandroside S Y. thibetica Whole plants [44]
66 Ypsilandroside T Y. thibetica Whole plants [44]
67 Ysiyunnoside A Y. yunnanensis Whole plants [45]
68 Ysiyunnoside B Y. yunnanensis Whole plants [45]
69 Ysiyunnoside C Y. yunnanensis Whole plants [45]
70 Ysiyunnoside D Y. yunnanensis Whole plants [45]
71 Ysiyunnoside E Y. yunnanensis Whole plants [45]
72 Ypsilactoside A Y. thibetica Whole plants [46]
73 Ypsilactoside B Y. thibetica Whole plants [46]

2.3 Trillium Species (Liliaceae)

The Trillium genus consists of approximately 49 species throughout the world. However, only three species, T. kamtschaticum, T. tschonoskii, and T. govanianum, are found in Hubei, Sichuan, Yunnan, and Xizang Provinces of China. The rhizomes of T. kamtschaticum, called "Toudingyikezhu" in Chinese, have been traditionally use by Chinese minorities (Tujia and Miao people) for the treatment of traumatic hemorrhage [47, 48]. In addition, some pennogenin saponins have been reported from Trillium species [49, 50] and the crude extract of the whole plants of T. kamtschaticum displayed significant induced-platelet aggregation activity at a concentration of 1.5 mg/mL as revealed by our initiatory test. All these information strongly inspired us to investigated the hemostatic constituents of the whole plats of T. kamtschaticum, resulting in the isolation of 18 new steroidal saponins (Fig. 3; Table 3), named trillikamtosides A-R (74-91) [51, 52]. Interestingly, some of them were determined to have rare aglycone moieties. For instance, the aglycones of 73-75 had unique 3β, 17α-dihydroxyspirostanes featuring a double bond between C-4 and C-5, 76 and 77 represented a rare class of spirostanol saponins which possess a 5(6-7) abeo-steroidal aglycone, and 83 possessed a rare aglycone with a 16-oxaandrost-5-en-3-ol-17-one moiety. Moreover, saponins 84 and 86 were schizolytic derivatives of those furanstanols and 89-91 were new trillenogenin saponins being only found in Trillium plants. The relevant researches of the other Trillium species are going on in our laboratory.

Fig. 3

New steroidal saponins from Trillium species

Table 3

New steroidal saponins from the whole plants of T. kamtschaticum

No. Name Species References
74 Trillikamtoside A T. kamtschaticum [51]
75 Trillikamtoside B T. kamtschaticum [51]
76 Trillikamtoside C T. kamtschaticum [51]
77 Trillikamtoside D T. kamtschaticum [51]
78 Trillikamtoside E T. kamtschaticum [51]
79 Trillikamtoside F T. kamtschaticum [51]
80 Trillikamtoside G T. kamtschaticum [51]
81 Trillikamtoside H T. kamtschaticum [51]
82 Trillikamtoside I T. kamtschaticum [51]
83 Trillikamtoside J T. kamtschaticum [51]
84 Trillikamtoside K T. kamtschaticum [52]
85 Trillikamtoside L T. kamtschaticum [52]
86 Trillikamtoside M T. kamtschaticum [52]
87 Trillikamtoside N T. kamtschaticum [52]
88 Trillikamtoside O T. kamtschaticum [52]
89 Trillikamtoside P T. kamtschaticum [52]
90 Trillikamtoside Q T. kamtschaticum [52]
91 Trillikamtoside R T. kamtschaticum [52]

2.4 Tacca Species (Taccaceae)

Compared with the genera of Liliaceae family, the Tacca plants are very limited. In order to discuss/explore whether the Tacca species possess the same steroidal constituents as that of RP, our group investigated the phytochemicals of two Tacca species (T. plantaginea and T. subflabellata). The results led to the structural characterization of eight new spirostane saponins, named taccaosides E-L (92-99) [53], taccaoside C (100) [54], taccasubosides B (103) and C (104) [55], three furostanol saponins, named taccaoside D (101) [54], taccaosides A (106) and B (107) [56], a new C21 steroidal saponin, taccasuboside D (105) [55], and 13 new withanolides, named taccasuboside A (102) [55], plantagiolides A-E (108-112) [57], plantagiolide F (113) [58], plantagiolides K-N (114-117) [59], and taccalonolides W-Y (118-120) [60] (Fig. 4; Table 4). Although withanolides 108-117 and taccalonolides 118-120 were also steroidal derivatives with 28 carbons, they may be the taxonomic markers of Tacca species.

Fig. 4

New steroidal sapogenins and saponins from Tacca species

Table 4

New steroidal sapogenins and saponins from Tacca species

Nos. Names Species Parts References
92 Taccaoside E T. plantaginea Whole plants [53]
93 Taccaoside F T. plantaginea Whole plants [53]
94 Taccaoside G T. plantaginea Whole plants [53]
95 Taccaoside H T. plantaginea Whole plants [53]
96 Taccaoside I T. plantaginea Whole plants [53]
97 Taccaoside J T. plantaginea Whole plants [53]
98 Taccaoside K T. plantaginea Whole plants [53]
99 Taccaoside L T. plantaginea Whole plants [53]
100 Taccaoside C T. plantaginea Whole plants [54]
101 Taccaoside D T. plantaginea Whole plants [54]
102 Taccasuboside A T. subflabellata Whole plants [55]
103 Taccasuboside B T. subflabellata Whole plants [55]
104 Taccasuboside C T. subflabellata Whole plants [55]
105 Taccasuboside D T. subflabellata Whole plants [55]
106 Taccaoside A T. plantaginea Rhizomes [56]
107 Taccaoside B T. plantaginea Rhizomes [56]
108 Plantagiolide A T. plantaginea Whole plants [57]
109 Plantagiolide B T. plantaginea Whole plants [57]
110 Plantagiolide C T. plantaginea Whole plants [57]
111 Plantagiolide D T. plantaginea Whole plants [57]
112 Plantagiolide E T. plantaginea Whole plants [57]
113 Plantagiolide F T. plantaginea Whole plants [58]
114 Plantagiolide K T. plantaginea Whole plants [59]
115 Plantagiolide L T. plantaginea Whole plants [59]
116 Plantagiolide M T. plantaginea Whole plants [59]
117 Plantagiolide N T. plantaginea Whole plants [59]
118 Taccalonolide W T. plantaginea Whole plants [60]
119 Taccalonolide X T. plantaginea Whole plants [60]
120 Taccalonolide Y T. plantaginea Whole plants [60]

2.5 Known Sapogenin and Saponins Obtained from the Non-medicinal Parts of PPY and Other Paris, Ypsilandra, Trillium, and Tacca Plants

Apart from the above mentioned new saponins, 1 known sapogenin and 63 known saponins were also identified from the aforementioned species (Fig. 5; Table 5). Compared with those new isolates, these known compounds usually shared the aglycones with lower oxidation degrees.

Fig. 5

Known steroidal sapogenins and saponins

Table 5

Known steroidal sapogenins and saponins

Nos. Names Species Parts References
121 Diosgenin PPY Stems and leaves [25]
122 Polyphyllin A PPY Stems and leaves [25]
123 Paris saponin Ⅴ PPY Stems and leaves [25]
P. axialis rhizomes [31]
P. delavayi Rhizomes [31]
Y. thibetica Whole plants [38]
124 Sansevierin A PPY Stems and leaves [25]
125 Progenin Ⅱ PPY Stems and leaves [25]
126 Disoseptemloside D PPY Stems and leaves [25]
127 Diosgenin-3-O-β-D-glucopyranosyl-(1→3)-[α-L-rhamnopyranosyl(1→2)]-β-D-glucopyranoside P. axialis Rhizomes [30]
128 Taccaoside T. plantaginea Whole plants [53]
T. chanteraeri Rhizomes [66]
129 Dioscin PPY Stems and leaves [25]
Y. thibetica Whole plants [38]
T. plantaginea Whole plants [53]
130 Disoseptemloside E PPY Stems and leaves [25]
131 Paris saponin Ⅰ P. axialis Rhizomes [31]
P. delavayi Rhizomes [31]
P. dunniana Rhizomes [31]
P. luquanensis Rhizomes [62]
132 Diosgenin-3-O-α-L-rhamnopyranosyl-(1→4)-α-L-rhamnopyranosyl(1→4)-β-D-glucopyranoside PPY Stems and leaves [27]
P. verticillata Aerial parts [32]
Y. thibetica Whole plants [38]
133 Paris saponin Ⅱ PPY Stems and leaves [25]
Y. thibetica Whole plants [38]
Y. parviflora Whole plants [41]
134 Pennogenin 3-O-β-D-glucopyranoside T. kamtschaticum Whole plants [51]
135 Paris saponin Ⅵ PPY Stems and leaves [25]
P. axialis Rhizomes [31]
P. delavayi Rhizomes [31]
T. kamtschaticum Whole plants [51]
136 Floribundasaponin B Y. thibetica Whole plants [38]
T. kamtschaticum Whole plants [51]
137 Pennogenin 3-O-β-D-glucopyranosyl-(1→3)-[α-L-rhamnopyranosyl(1→2)]-β-D-glucopyranoside P. axialis Rhizomes [31]
138 Pennogenin 3-O-β-chacotrioside PPY Aerial parts [64]
T. kamtschaticum Whole plants [51]
Y. thibetica Whole plants [38]
Y. parviflora Whole plants [41]
139 Paris saponin H P. axialis Rhizomes [31]
P. delavayi Rhizomes [31]
P. dunniana Rhizomes [31]
P. luquanensis Rhizomes [62]
140 Pennogenin 3-O-α-L-rhamnopyranosyl-(1→4)-α-L-rhamnopyranosyl-(1→4)-β-D-glucopyranoside PPY Stems and leaves [25]
P. verticillata Aerial parts [32]
T. kamtschaticum Whole plants [51]
Y. parviflora Whole plants [48]
141 Paris saponin Ⅶ PPY Stems and leaves [25]
P. verticillata Aerial parts [32]
P. luquanensis Rhizomes [62]
PPY Seeds [63]
T. kamtschaticum Whole plants [51]
Y. parviflora Whole plants [41]
Y. thibetica Whole plants [39]
142 Isonuatigenin 3-O-α-L-rhamnopyranosyl-(1-2)-β-D-glucopyranoside PPY Stems and leaves [25]
143 Disoseptemloside H PPY Stems and leaves [25]
144 Pennogenin 3-O-α-L-rhamnopyranosyl-(1→2)-[α-L-rhamnopyranosyl(1→4)]-β-D-glucopyranoside PPY Aerial parts [65]
145 Nuatigenin 3-O-α-L-rhamnopyranosyl-(1→2)-β-D-glucopyranoside PPY Stems and leaves [27]
146 26-O-β-D-glucopyranosyl nuatigenin 3-O-α-L-rhamnopyranosyl-(1→2)-β-D-glucopyranoside PPY Stems and leaves [27]
147 26-O-β-D-glucopyranosyl nuatigenin 3-O-α-L-rhamnopyranosyl-(1→4)-β-D-glucopyranoside PPY Stems and leaves [27]
148 26-O-β-D-glucopyranosyl nuatigenin 3-O-α-L-rhamnopyranosyl-(1→2)-[α-L-rhamnopyranosyl-(1→4)]-β-D-glucopyranoside PPY Aerial parts [65]
149 Abutiloside L PPY Stems and leaves [27]
150 Borassoside B PPY Stems and leaves [27]
151 (24S, 25R)-spirost-5-en-3β, 24-diol-3-O-α-L-rhamnopyranosyl-(1→2)-[α-L-rhamnopyranosyl(1→3)]-β-D-glucopyranoside T. plantaginea Whole plants [53]
152 (25S)-spirost-5-en-3β-ol-3-O-α-L-rhamnopyranosyl-(1→2)-[β-D-glucopyranosyl-(1→4)-α-L-rhamnopyranosyl-(1→3)]-β-D-glucopyranoside T. plantaginea Whole plants [53]
153 Spiroconazole A T. plantaginea Whole plants [53]
154 Diosbulbiside A T. plantaginea Whole plants [53]
155 Diosbulbiside B T. plantaginea Whole plants [53]
156 (25S)-27-hydroxypennogenin 3-O-β-D-glucopyranoside T. kamtschaticum Whole plants [51]
157 (25S)-27-hydroxypennogenin-3-O-α-L-rhamnopyranosyl-(1→2)-β-D-glucopyranoside T. kamtschaticum Whole plants [51]
158 Trikamsteroside A T. kamtschaticum Whole plants [51]
159 Ophiopogonin B T. kamtschaticum Whole plants [51]
160 Trikamsteroside E T. kamtschaticum Whole plants [52]
161 Diosbulbiside E T. plantaginea Whole plants [53]
162 Aethioside A T. kamtschaticum Whole plants [52]
163 Parispseudoside A P. verticillata Aerial parts [32]
Y. parviflora Whole plants [41]
Y. thibetica Whole plants [43]
164 Protoprogenin Ⅱ Y. thibetica Whole plants [43]
165 26-O-β-D-glucopyranosyl-(25S)-3β, 22ξ, 26-triol-furost-5-ene 3-O-α-L-rhamnopyranosyl-(1→2) -[α-L-rhamnopyranosyl(1→3)]-β-D-glucopyranoside T. plantaginea Whole plants [54]
T. subflabellata Whole plants [55]
166 Proto-dioscin PPY Stems and leaves [25]
167 Methylprotodioscin PPY Stems and leaves [25]
168 Proto-paris saponin Ⅱ P. verticillata Aerial parts [32]
Y. parviflora Whole plants [41]
Y. thibetica Whole plants [43]
169 26-O-β-D-glucopyranosyl-22-methoxy-3β, 26-dihydroxy-(25R)-furost-5-en-3-O-α-L-rhamnopyranosyl-(1→2)-[α-L-rhamnopyranosyl-(1→4)-α-L-rhamnopyranosyl-(1→3)]-β-D-glucopyranoside P. verticillata Aerial parts [32]
170 Proto-paris saponin Ⅶ P. verticillata Aerial parts [32]
Y. thibetica Whole plants [43]
171 26-O-β-D-glucopyranosyl-3β, 20α, 26-triol-(25R)-5, 22-dienofurostan 3-O-α-L-rhamnopyranosyl-(1→2)-[α-L-rhamnopyranosyl(1→4)]-β-D-glucopyranoside PPY Stems and leaves [25]
172 Smilaxchinoside B P. verticillata Aerial parts [32]
Y. thibetica Whole plants [43]
173 26-O-β-D-glucopyranosyl-17(20)-dehydrokryptogenin-3-O-α-L-rhamnopyranosyl-(1→2)-β-D-glucopyranoside T. kamtschaticum Whole plants [52]
174 Pseudoproto Pb P. verticillata Aerial parts [32]
Y. parviflora Whole plants [41]
Y. thibetica Whole plants [43]
175 Parispseudoside C P. verticillata Aerial parts [32]
Y. thibetica Whole plants [43]
Y. yunnanensis Whole plants [45]
176 26-O-β-D-glucopyranosyl-3β, 26-dihydroxy-20, 22-seco-25(R)-furost-5-en-20, 22-dione 3-O-α-L-rhamnopyranosyl-(1→4)-α-L-rhamnopyranosyl-(1→4)-[α-L-rhamnopyranosyl-(1→2)]-β-D-glucopyranoside Y. thibetica Whole plants [43]
177 7α-Hydroxystigmasterol-3-O-β-D-glucopyranoside PPY Stems and leaves [27]
178 7α-Hydroxysitosterol-3-O-β-D-glucopyranoside PPY Stems and leaves [27]
179 Dumoside PPY Stems and leaves [26]
180 Hypoglaucin H PPY Stems and leaves [25]
PPY Aerial parts [64]
181 21-Methoxyl pregna-5, 16-dien-3β-ol-20-one 3-O-α-L-rhamnopyranosyl-(1→2)-[α-L-rhamnopyranosyl(1→4)]-β-D-glucopyranoside PPY Stems and leaves [25]
182 Pregna-5, 16-dien-3β-ol-20-one 3-O-α-L-rhamnopyranosyl-(1→2)-[α-L-rhamnopyranosyl(1→4)-α-L-rhamnopyranosyl(1→4)]-β-D-glucopyranoside P. verticillata Aerial parts [32]
Y. thibetica Whole plants [43]
PPY Aerial parts [64]
183 Chantriolide A T. subflabellata Whole plants [55]
T. plantaginea Whole plants [57]
184 Chantriolide B T. subflabellata Whole plants [55]

3 Bioactivities

Based on the fact that RP is traditionally used as hemostatic, antimicrobial, and antitumor agents, the hemostatic, antimicrobial, and cytotoxic activities of obtained compounds were evaluated to initially confirm that whether the plants could be alternative resources of RP. Our studies revealed that most of the bioactive compounds were spirostanol saponins with only one sugar chain at OH-3.

3.1 Hemostatic Effect

Both the total steroidal saponin moieties and purified saponins of PPY and T. kamtschaticum exhibited hemostatic effects. The 70% EtOH eluted fraction of T. kamtschaticum crude extract obtained from a macroporous resin column showed 76% maximal platelet aggregation rate at a concentration of 1.5 mg/mL [51]. Subsequently, three pennogenin-type saponins, paris saponin Ⅵ (135), pennogenin 3-O-β-chacotrioside (138), and paris saponin Ⅶ (141) were obtained and further proved to display maximal induced platelet aggregation rates (MPARs) of 72, 71, and 62% with EC50 values of 0.49, 0.20, and 0.11 mM, respectively [51]. The results also suggested that the hydroxy group at C-17 in pennogenin saponins was indispensable for their hemostatic effects, whereas the introduction of different functional groups in the A, B, or F-ring of pennogenin glycosides could make the hemostatic effect weak or disappear. Interestingly, the total saponin moieties from the above-ground parts and the rhizomes of PPY showed equivalent maximal platelet aggregation rates of 45 and 43% at a concentration of 1.5 mg/mL, respectively [61]. This indicated that the above-ground parts can be an alternative and more sustainable sources for RP. Additionally, two diosgenin-type saponins, ypsilandroside M (49), ypsiparoside C (54), and paris saponin Ⅱ (133) isolated from Y. parviflora, exhibited MPARs of 43, 44 and 55% at the concentration of 0.3 mg/mL, respectively [41]. This indicated that the carbonyl group at C-12 or the sole α-L-rhamnopyranosyl-(1→4)-α-L-rhamnopyranosyl-(1→4)-[α-L-rhamnopyranosyl-(1→2)]-β-D-glucopyranosyl moiety at OH-3 was essential for the hemostatic effect of diosgenin saponins.

3.2 Cytotoxic Effect

A number of saponins were proved to have cytotoxicity against various human tumor cells. Two Trillium saponis with a double bond between C-13 and 14 isolated from T. kamtschaticum, trillikamtosides P (89) and R (91), showed cytotoxic effect against HCT116 (colorectal carcinoma) cells with the MIC values of 4.92 and 5.84 μM, respectively [52]. Ypsilandroside G (43) obtained from Y. thibetica displayed cytotoxic effect against K562 (leukemia) cells with an MIC value of 4.7 μM, and paris saponin Ⅶ (141) identified from the same species was cytotoxic towards SPC-A-1 (lung carcinoma) and BGC-823 (gastric carcinoma) with the IC50 values of 2.6 and 4.0 μM, respectively [38]. Nuatigenin 3-O-α-L-rhamnopyranosyl-(1→2)-β-D-glucopyranoside isolated from the stems and leaves of PPY exhibited cytotoxicity against HepG2 (hepatoma) and HEK293 (renal carcinoma) cell lines with IC50 values of 2.9 and 5.0 μM, respectively [27]. Taccaoside (128), a saponin obtained from T. plantaginea, exhibited significant cytotoxicity against HepG2 and HEK293 cell lines with IC50 values of 1.2 and 1.7 μM, respectively [53]. Compared with the positive control drug cisplatin (DDP), a furostanol saponin isolated from T. subflabellata, 26-O-β-D-glucopyranosyl-(25S)-3β, 22ξ, 26-triol-furost-5-ene 3-O-α-L-rhamnopyranosyl(1→2)-[α-L-rhamnopyranosyl(1→3)]-β-D-glucopyranoside (165) showed significant cytotoxicity against HL-60 (leukemic), SMMC-7721 (hepatoma), A549 (lung carcinoma), MCF-7 (breast carcinoma), and SW480 (colon carcinoma) cells with the IC50 values of 4.63, 4.34, 3.00, 11.13, and 2.68 μM, respectively [55]. Ypsilandroside P (62), a furostanol saponin obtained from Y. thibetica, showed inhibition ratio of 86.4 and 75.9% to A549 and HL-60 cells at the concentration of 10.0 μM, respectively [43]. Moreover, the total saponin moieties from the both rhizomes and above-ground parts of PPY showed cytotoxicities against HL-60, A549, SMMC-7721, MCF-7, and SW480 cells [61]. To be more specific, the former displayed cytotoxicities against above-mentioned cancer cells with IC50 values of 1.77, 1.75, 5.23, 6.62, and 3.49 μM, whereas the latter was less cytotoxic with IC50 values of 9.54, 9.30, 12.61, 8.12, and 11.25 μM, respectively.

3.3 Antimicrobial Effect

Ypsilandroside G (43) obtained from Y. thibetica showed moderate inhibitory effect on Candida albicans with an MIC value of 10 μg/mL [38]. Compared with that of fluconazole (MIC=52.3 μM), five saponins isolated from T. kamtschaticum, named paris saponin Ⅵ (135), floribundasaponin B (136), pennogenin 3-O-β-chacotrioside (138), paris saponin Ⅴ (123), and ophiopogonin B (159), displayed significant antifungal activity against C. albicans with the MIC values of 21.1, 10.6, 8.8, 21.6, and 11.0 μM, respectively [51]. Chonglouoside SL-6 (6), progenin Ⅱ (125), and dumoside (179), three steroidal saponins isolated from the stems and leaves, exhibited good antibacterial activity with the MIC values of 3.9, 7.8, and 3.9 μg/mL, respectively [25, 26]. All three spirostanol saponins identified from PPY, paris saponin Ⅴ (123), dioscin (129), and paris saponin Ⅱ (133), were revealed to show significant antifungal activities against C. albicans 5314 and C. albicans Y0109 with an MIC value of 1.95 μg/mL [61]. Also, the total saponin moieties from both the above-ground parts and the rhizomes of PPY exhibited remarkable antifungal activities against C. albicans Y0109 with MIC values of 10.3 and 5.15 μg/mL, respectively, compared with that the positive control voriconazole (MIC=15.63 μg/mL) [61].

4 Conclusion

In summary, our continuous effort to search for alternative resources of RP led to the isolation of 184 steroidal derivatives, including 120 new ones. More importantly, several compounds of them displayed remarkable hemostatic, cytotoxic, and antimicrobial effects. Our studies disclosed that the non-medicinal parts of PPY, as well as other plants of Paris, Ypsilandra, Trillium, and Taccaceae family are also resources rich of steroidal saponins similar to those of RP, especially those recorded in Chinese Pharmacopoeia, namely, paris saponins Ⅰ (131), Ⅱ (133), Ⅵ (135), and Ⅶ (141). However, the investigations on the total content of these saponins, the related bioactivities of total saponin moieties of the studied species compared with those of RP, and their security capability are quite indispensable to confirm that whether the non-medicinal parts of PPY and other species from Paris, Ypsilandra, and Tacca genera could be safe and dependable alternative resources of RP. The arial parts of PPY and the whole plants of T. kamtschaticum might be alternative resources for RP based on the fact that they shared the same or similar saponins and bioactivities. The continuous studies on the saponin constituents of non-medicinal parts of RP and other plants will be carried out in our laboratory which may led to the discovery of more alternative resources for RP.

Notes

Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (Nos. 31570363, 31770391, and 31600283), the Natural Science Foundation of Yunnan Province (2015FA031 and 2017FB128), the Science and Technology Research Program (Grant No. KIB2016001) of Kunming Institute of Botany, CAS, Guiding Program of Interdisciplinary Studies from Kunming Institute of Botany, CAS (Grant No. KIB2017004), and the Foundation of State Key Laboratory of Phytochemistry and Plant Resources in West China (P2017-ZZ04), Kunming Institute of Botany, Chinese Academy of Sciences.

Compliance with Ethical Standards

Conflict of interest

All authors declare no conflict of interest.

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Authors and Affiliations

  • Xu-Jie Qin
    • 1
  • Wei Ni
    • 1
  • Chang-Xiang Chen
    • 1
  • Hai-Yang Liu
    • 1
    •     
  1. 1. State Key Laboratory of Phytochemistry and Plant Resources in West China, Kunming Institute of Botany, Chinese Academy of Sciences, and Yunnan Key Laboratory of Medicinal Chemistry, Kunming 650201, People's Republic of China
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