Download PDF
Planta Medica International Open 2016; 3(02): e39-e42
DOI: 10.1055/s-0042-108808
Letter
Georg Thieme Verlag KG Stuttgart · New York

Lipopolysaccharide-Induced Nitric Oxide and Prolyl Oligopeptidase – Inhibitory Activities of Triterpenoids from Sanguisorba officinalis

Hongyu Ma
School of Traditional Chinese Materia Medica, Shenyang Pharmaceutical University, Shenyang, Peopleʼs Republic of China
,
Xizhe Li
School of Traditional Chinese Materia Medica, Shenyang Pharmaceutical University, Shenyang, Peopleʼs Republic of China
,
Yuchen Zhang
School of Traditional Chinese Materia Medica, Shenyang Pharmaceutical University, Shenyang, Peopleʼs Republic of China
,
Guangsong Chu
School of Traditional Chinese Materia Medica, Shenyang Pharmaceutical University, Shenyang, Peopleʼs Republic of China
,
Zhong Yuan
School of Traditional Chinese Materia Medica, Shenyang Pharmaceutical University, Shenyang, Peopleʼs Republic of China
› Author Affiliations
Further Information

Publication History

received 22 September 2015
revised 02 March 2016

accepted 13 May 2016

Publication Date:
15 August 2016 (online)

   Permissions and Reprints

Abstract

Lipopolysaccharide-induced nitric oxide and the protease prolyl oligopeptidase (EC 3.4.21.26) have been proposed as targets for the treatment of cognitive disturbances such as dementia. In this study, nine triterpenoids isolated from the roots of Sanguisorba officinalis, including arjunic acid (1), rosamultic acid (2), haptadienic acid (3), 1β-hydroxyeuscaphic acid (4), euscaphic acid (5), tormentic acid (6), pomolic acid (7), ursolic acid (8), and oleanolic acid (9), were tested in vitro for their inhibitory activities on lipopolysaccharide-induced nitric oxide in N9 microglia cells and on prolyl oligopeptidase. Among them, 7 exhibited the strongest inhibitory activity on lipopolysaccharide-induced nitric oxide (IC50, 21.9 µM), while 8 and 9 exhibited a significant prolyl oligopeptidase inhibitory activity (IC50 18.1 and 24.0 µM, respectively). The results could provide a clue that these triterpenoids are responsible for the reported neuro-protective effect of S. officinalis.

Key words

Sanguisorba officinalis - Rosaceae - triterpenoids - lipopolysaccharide-induced nitric oxide - prolyl oligopeptidase
 

  • References

  • 1 Amor EC, Villaseñor IM, Yasin A, Choudhary MI. Prolyl endopeptidase inhibitors from Syzygium samarangense (Blume) Merr. & L. M. Perry. Z Naturforsch C 2004; 59: 86-92
    CrossrefPubMedSearch in Google Scholar
  • 2 Yu T, Lee YJ, Yang HM, Han S, Kim JH, Lee Y, Kim C, Han MH, Kim MY, Lee J, Cho JY. Inhibitory effect of Sanguisorba officinalis ethanol extract on NO and PGE2 production is mediated by suppression of NF-κB and AP-1 activation signaling cascade. J Ethnopharmacol 2011; 138: 11-17
    PubMedSearch in Google Scholar
  • 3 Da Rocha MD, Viegas FP, Campos HC, Nicastro PC, Fossaluzza PC, Fraga CA, Barreiro EJ, Viegas Jr. C. The role of natural products in the discovery of new drug candidates for the treatment of neurodegenerative disorders II: Alzheimerʼs disease. CNS Neurol Disord Drug Targets 2011; 10: 251-270
    CrossrefPubMedSearch in Google Scholar
  • 4 Katsube N, Sunaga K, Aishita H, Chuang DM, Ishitani R. ONO-1603, a potential antidementia drug, delays age-induced apoptosis and suppresses overexpression of glyceraldehyde-3-phosplhate dehydrogenase in cultured central nervous system neurons. J Pharmacol Exp Ther 1999; 288: 6-13
    PubMedSearch in Google Scholar
  • 5 Liu X, Cui Y, Yu Q, Yu B. Triterpenoids from Sanguisorba officinalis . Phytochemistry 2005; 66: 1671-1679
    CrossrefPubMedSearch in Google Scholar
  • 6 Zhang PY, Qin SH, Zhao HX, Wang FL, Guo HJ, Bai H. A new triterpenoid saponin from Sanguisorba officinalis . J Asian Nat Prod Res 2012; 14: 607-611
    CrossrefPubMedSearch in Google Scholar
  • 7 Hu J, Li H, Yang BS, Mao X, Shi XD. Nordammarane triterpenoids from Sanguisorba officinalis . Helv Chim Acta 2015; 2: 273-278
    PubMedSearch in Google Scholar
  • 8 Liu X, Shi B, Yu B. Four new dimeric triterpene glucosides from Sanguisorba officinalis . Tetrahedron 2004; 60: 11647-11654
    CrossrefPubMedSearch in Google Scholar
  • 9 Lue LF, Kuo YM, Beach T, Walker DG. Microglia activation and anti-inflammatory regulation in Alzheimerʼs disease. Mol Neurobiol 2010; 41: 115-128
    CrossrefPubMedSearch in Google Scholar
  • 10 Gu JH, Ge JB, Li M, Wu F, Zhang W, Qin ZH. Inhibition of NF-κB activation is associated with anti-inflammatory and anti-apoptotic effects of ginkgolide B in a mouse model of cerebral ischemia/reperfusion injury. Eur J Pharm Sci 2012; 47: 652-660
    CrossrefPubMedSearch in Google Scholar
  • 11 Hagberg H, Gressens P, Mallard C. Inflammation during fetal and neonatal life: Implications for neurologic and neuropsychiatric disease in children and adults. Ann Neurol 2012; 71: 444-457
    CrossrefPubMedSearch in Google Scholar
  • 12 Hao Y, Yang JY, Wu CF, Wu MF. Pseudoginsenoside-F11 decreases morphine-induced behavioral sensitization and extracellular glutamate levels in the medial prefrontal cortex in mice. Pharmacol Biochem Behav 2007; 86: 660-666
    CrossrefPubMedSearch in Google Scholar
  • 13 Polgár L. The prolyl oligopeptidase family. Cell Mol Life Sci 2002; 59: 349-362
    CrossrefPubMedSearch in Google Scholar
  • 14 Taylor WL, Dixon JE. Catabolism of neuropeptides by a brain proline endopeptidase. Biochem Biophys Res Commun 1980; 94: 9-15
    CrossrefPubMedSearch in Google Scholar
  • 15 Schneider JS, Giardiniere M, Morain P. Effects of the prolyl endopeptidase inhibitor S 17092 on cognitive deficits in chronic low dose MPTP-treated monkeys. Neuropsychopharmacology 2002; 26: 176-182
    CrossrefPubMedSearch in Google Scholar
  • 16 Portevin B, Benoist A, Rémond G, Hervé Y, Vincent M, Lepagnol J, De Nanteuil G. New prolyl endopeptidase inhibitors: in vitro and in vivo activities of azabicyclo[2.2.2]octane, azabicyclo[2.2.1]heptane, and perhydroin-dole derivatives. J Med Chem 1996; 39: 2379-2391
    CrossrefPubMedSearch in Google Scholar
  • 17 Yoshimoto T, Kado K, Matsubara F, Koriyama N, Kaneto H, Tsura D. Specific inhibitors for prolyl endopeptidase and their anti-amnesic effect. J Pharmacobiodyn 1987; 10: 730-735
    CrossrefPubMedSearch in Google Scholar
  • 18 Park DH, Park SJ, Kim JM, Jung WY, Ryu JH. Subchronic administration of rosmarinic acid, a natural prolyl oligopeptidase inhibitor, enhances cognitive performances. Fitoterapia 2010; 81: 644-648
    CrossrefPubMedSearch in Google Scholar
  • 19 Morain P, Robin JL, De Nanteuil G, Jochemsen R, Heidet V, Guez D. Pharmacodynamic and pharmacokinetic profile of S 17092, a new orally active prolyl endopeptidase inhibitor, in elderly healthy volunteers. A phase I study. Br J Clin Pharmacol 2000; 50: 350-359
    CrossrefPubMedSearch in Google Scholar
  • 20 Sultanova N, Makhmoor T, Yasin A, Abilov ZA, Omurkamzinova VB, Atta-ur-Rahman. Choudhary MI. Isotamarixen – a new antiodant and prolyl endopeptidase-inhibiting triterpenoid from Tamarix hipida . Planta Med 2004; 70: 65-67
    Thieme ConnectPubMedSearch in Google Scholar
  • 21 Park YS, Jang HJ, Paik YS. Prolyl endopeptidase inhibitory activity of ursolic and oleanolic acids from Corni Fructus. Agric Chem Biotechnol 2005; 48: 207-212
    PubMedSearch in Google Scholar
  • 22 Marques MR, Stüker C, Kichik N, Tarragó T, Giralt E, Morel AF, Dalcol II. Flavonoids with prolyl oligopeptidase inhibitory activity isolated from Scutellaria racemosa Pers. Fitoterapia 2010; 81: 552-556
    CrossrefPubMedSearch in Google Scholar
  • 23 Wang H, Yuan Z. Triterpenes of Sanguisorba officinalis L. Chin J Med Chem 2009; 19: 52-62
    PubMedSearch in Google Scholar
  • 24 Turkmen Z, Klymchenko AS, Oncul S, Duportail G, Topcu G, Demchenko AP. A triterpene oleanolic acid conjugate with 3-hydroxyflavone derivative as a new membrane probe with two-color ratiometric response. J Biochem Biophys Methods 2005; 64: 1-18
    CrossrefPubMedSearch in Google Scholar
  • 25 Meng XL, Yang JY, Chen GL, Wang LH, Zhang LJ, Wang S, Li J, Wu CF. Effects of resveratrol and its derivatives on lipopolysaccharide-induced microglial activation and their structure-activity relationships. Chem Biol Interact 2008; 17: 451-459
    PubMedSearch in Google Scholar
  • 26 Iribarren P, Chen KQ, Hu JY, Zhang X, Gong WH, Wang JM. IL-4 inhibits the expression of mouse formyl peptide receptor 2, a receptor for amyloid beta1-42, in TNF-α-activated microglia. J Immunol 2005; 175: 6100-6106
    CrossrefPubMedSearch in Google Scholar
  • 27 Lee HJ, Maeng K, Dang HT, Kang GJ, Ryou C, Jung JH, Kang HK, Prchal JT, Yoo ES, Yoon D. Anti-inflammatory effect of methyl dehydrojasmonate (J2) is mediated by the NF-κB pathway. J Mol Med (Berl) 2011; 89: 83-90
    CrossrefPubMedSearch in Google Scholar
  • 28 Chen X, Choi IY, Chang TS, Noh YH, Shin CY, Wu CF, Ko KH, Kim WK. Pretreatment with interferon-gprotects microglia from oxidative stress via up-regulation of Mn-SOD. Free Radic Biol Med 2009; 46: 1204-1210
    CrossrefPubMedSearch in Google Scholar
  • 29 Wallén EA, Christiaans JA, Saarinen TJ, Jarho EM, Forsberg MM, Venäläinen JI, Männistö PT, Gynther J. Conformationally rigid N-acyl-5-alkyl-L-prolyl-pyrrolidines as prolyl oligopeptidase inhibitors. Bioorg Med Chem 2003; 11: 3611-3619
    CrossrefPubMedSearch in Google Scholar
  • 30 Wallén EA, Christiaans JA, Forsberg MM, Venäläinen JI, Männistö PT, Gynther J. Dicarboxylic acid bis(L-prolyl-pyrroldine) amides as prolyl oligopeptidase inhibitors. J Med Chem 2002; 45: 4581-4584
    CrossrefPubMedSearch in Google Scholar