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Seasonal variation of pheophorbide a and flavonoid in different organs of two Carpinus species and its correlation with immunosuppressive activity

  • Qianqian Sheng
  • Xianying Fang
  • Zunling ZhuEmail author
  • Wei XiaoEmail author
  • Zhenzhong Wang
  • Gang Ding
  • Linguo Zhao
  • Yujian Li
  • Ping Yu
  • Zhibin Ding
  • Qinru Sun
Article

Abstract

The genus Carpinus of Betulaceae is the most widely distributed in the European landscape. This study reports a comparative study based on the pheophorbide a and flavonoid content from the two main species of the genus Carpinus, Carpinus betulus and Carpinus turczaninowii, respectively, in Nanjing, China. The pheophorbide a and flavonoid content depends on the organ, species, and season. HPLC analysis showed that the pheophorbide a and flavonoid levels were the highest in May and June, respectively, from the leaves of C. betulus ‘Fastigiata.’ In contrast, the content of pheophorbide a and flavonoid in the stems of C. betulus ‘Fastigiata’ or in other species was low. The immunosuppressive effects of the ethyl acetate extracts and methanol extracts from the two Carpinus species were also evaluated. The ethyl acetate extracts of C. betulus ‘Fastigiata’ in May and the methanol extracts of C. betulus ‘Fastigiata’ in June showed better immunosuppressive activity than in other seasons, which coincided with the content of pheophorbide a and flavonoid, respectively. Our findings indicated that C. betulus ‘Fastigiata’ can serve as a medicinal plant against inflammation because of its pheophorbide a and flavonoid content.

Keywords

Carpinus Pheophorbide a Flavonoid Immunosuppressive 

Notes

Acknowledgments

This work was supported by The Open Fund of Jiangsu Key Lab of Biomass-based Green Fuels and Chemicals (JSBGFC14013), Jiangsu Province Engineering Technology Research Center Projects (BM2013478), Jiangsu Province Six Big Talent Peak Project (NY-029), and the Fourth Stage Funded Research Projects of 333 in Jiangsu Province. Animal welfare and experimental procedures were carried out strictly in accordance with the guide for the care and use of laboratory animals and the related ethical regulations of Nanjing Forestry University. All efforts were made to minimize animal’s suffering and to reduce the number of animals used.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Alejandro GM (1996) Kinetic model for chlorophyll degradation in green tissue. Pheophorbide degradation to colorless compounds. J Agric Food Chem 44:3735–3740CrossRefGoogle Scholar
  2. Anelise SNF, Candida ALK, Frederico FN et al (2013) The flavonoid content and antiproliferative, hypoglycaemic, anti-inflammatory and free radical scavenging activities of Annona dioica St. Hill. BMC Complement Altern Med 13:14CrossRefGoogle Scholar
  3. Anna JK, Tomasz W (1990) Species deletion in Potentillo albae-Quercetum phytocoenoses reversed by the removal of Carpinus betulus. Vegetatio 87:115–126CrossRefGoogle Scholar
  4. Bono L, Visˇnja S, Dejan P et al (2014) Correlation between 13C NMR chemical shifts and antiradical activity of flavonoids. Monatsh Chem 145:457–463CrossRefGoogle Scholar
  5. Cartaxana P, Jesus B, Brotas V (2003) Pheophorbide and pheophytin a-like pigments as useful markers for intertidal microphytobenthos grazing by Hydrobia ulvae. Estuar Coast Shelf Sci 58:293–297CrossRefGoogle Scholar
  6. Changwei H, Juyun C, Tenghsu W et al (2014) Hypoglycaemic effects of Ajuga extract in vitro and in vivo. J Funct Foods 6:224–230CrossRefGoogle Scholar
  7. Chingyun H, Chiming Y, Chiaoming C et al (2005) Effects of chlorophyll-related compounds on hydrogen peroxide induced DNA damage within human lymphocytes. J Agric Food Chem 53:2746–2750CrossRefGoogle Scholar
  8. Chinsung C, Jeong IJ (2004) Foliar flavonoids of the most primitive group, sect. Distegocarpus within the genus Carpinus. Biochem Syst Ecol 32:35–44CrossRefGoogle Scholar
  9. Christian S, Patrick P, Gero B, Ju¨rgen B (2012) Biomass equations for sessile oak (Quercus petraea (Matt.) Liebl.) and hornbeam (Carpinus betulus L.) in aged coppiced forests in southwest Germany. biomass and bioenergy 46: 722-730.Google Scholar
  10. Eisen HN, Orris L, Belman S (1952) Elicitation of delayed allergic skin reactions with haptens; the dependence of elicitation on hapten combination with protein. J Exp Med 95:473–487CrossRefPubMedPubMedCentralGoogle Scholar
  11. Els C, Sabine VG, Remy JP et al (2005) Range wide versus local patterns of genetic diversity in hornbeam (Carpinus betulus L.). Conserv Genet 6:259–273CrossRefGoogle Scholar
  12. Ewa C, Luc A, Thierry G et al (2012) Potential anticancer activity of young Carpinus betulus leaves. Phytomedicine 19:278–283CrossRefGoogle Scholar
  13. Flax MH, Caulfield JB (1963) Cellular and vascular components of allergic contact dermatitis. Am J Pathol 43:1031–1053PubMedPubMedCentralGoogle Scholar
  14. Gamal AM, Sabrin RMI, Nawal MA, Samir AR (2014) New anti-inflammatory flavonoids from Cadaba glandulosa Forssk. Arch Pharm Res 37:459–466CrossRefGoogle Scholar
  15. Gomah N (2013) Antimicrobial activity of Calotropis procera Ait. (Asclepiadaceae) and isolation of four flavonoid glycosides as the active constituents. World J Microbiol Biotechnol 29:1255–1262CrossRefGoogle Scholar
  16. Grabbe S, Schwarz T (1998) Immunoregulatory mechanisms involved in elicitation of allergic contact hypersensitivity. Immunol Today 19:37–44CrossRefPubMedGoogle Scholar
  17. Gyeoungjin K, Najin K, Sangchul H et al (2012) The chloroform fraction of carpinus tschonoskii leaves inhibits the production of inflammatory mediators in HaCaT keratinocytes and RAW264.7 macrophages. Toxicol Res 28(4):255–262CrossRefGoogle Scholar
  18. Ha NK, Taeheon O, Jong SB et al (2013) Anti-inflammatory activities for the extracts and carpinontriols from branches of carpinus turczaninowii. Int J Pharmacol 9(2):157–163CrossRefGoogle Scholar
  19. Haoyu Y, Wenshuang W, Zhuowei L et al (2014) Bioactivity-guided isolation of anti-inflammation flavonoids from the stems of Millettia dielsiana Harms. Fitoterapia 95:154–159CrossRefGoogle Scholar
  20. Hongjie Z, Ghee TT, Vu DH et al (2003) Natural anti-HIV agents. Part IV. Anti-HIV constituents from Vatica cinerea. J Nat Prod 66:263–268CrossRefGoogle Scholar
  21. Inhyeok O, Hyun SM, Li L et al (2013) Cancer cell-specific photoactivity of pheophorbide a-glycol chitosan nanoparticles for photodynamic therapy in tumor-bearing mice. Biomaterials 34:6454–6463CrossRefGoogle Scholar
  22. Jeong IJ, Chinsung C, Zhiduan C, Tae YP (2007) Systematic aspects of foliar flavonoids in subsect. Carpinus (Carpinus, Betulaceae). Biochem Syst Ecol 35:606–613CrossRefGoogle Scholar
  23. Jungeun K, Hyejin H, Vivek BM et al (2012) Inhibitory effects of Carpinus tschonoskii leaves extract on Cpg-stimulated pro-inflammatory cytokine production in murine bone marrow-derived macrophages and dendritic cells. In Vitro Cell Dev Biol Animal 48:197–202CrossRefGoogle Scholar
  24. Kwang HC, Hee JL, Song YK et al (2010) Optimization of pressurized liquid extraction of carotenoids and chlorophylls from chlorella vulgaris. J Agric Food Chem 58:793–797CrossRefGoogle Scholar
  25. Lai CS, Mas RN, Mansor SM et al (2010) Chemical constituents and in vitro anticancer activity of Typhonium flagelliforme (Araceae). J Ethnopharmacol 127:486–494CrossRefPubMedGoogle Scholar
  26. Lalou C, Basak A, Mishrab P et al (2013) Inhibition of tumor cells proliferation and migration by the flavonoid furin inhibitor isolated from oroxylum indicum. Curr Med Chem 20:583–591PubMedGoogle Scholar
  27. Lamjed B, Kyoko H, JungBum L et al (2011) Potent virucidal effect of pheophorbide a and pyropheophorbide a on enveloped viruses. J Nat Med 65:229–233CrossRefGoogle Scholar
  28. Le DMG, Havill DC (1998) Competition between Quercus petraea and Carpinus betulus in an ancient wood in England. seedling survivorship. J Veg Sci 9:873–880CrossRefGoogle Scholar
  29. Mohammed KH, Hye YC, Jaeseon H et al (2014) Antiviral activity of 3, 4’-dihydroxyflavone on influenza a virus. J Microbiol 52(6):521–526CrossRefGoogle Scholar
  30. Mohan S, Nandhakumar L (2014) Role of various flavonoids: hypotheses on novel approach to treat diabetes. J Med Hypotheses Ideas 8:1–6CrossRefGoogle Scholar
  31. Namyi C (2011) Annual variation of soil respiration and precipitation in a temperate forest (Quercus serrata and carpinus laxiflora) under East Asian monsoon climate. J Plant Biol 54:101–111CrossRefGoogle Scholar
  32. Parida Y, Takako O, Hideyuki S et al (2012) Inhibitory effect of tannins from galls of Carpinus tschonoskii on the degranulation of RBL-2H3 Cells. Cytotechnology 64:349–356CrossRefGoogle Scholar
  33. Pengfei W, Zunlai S, Qiang H et al (2014) Enrichment and purification of total flavonoids from Flos Populi extracts with macroporous resins and evaluation of antioxidant activities in vitro. J Chromatogr B 946:68–74Google Scholar
  34. Sungha K, Jungeun K, Hyejin H et al (2012) Anti-inflammatory activity of carpinus tschonoskii leaves extract in R848-stimulated bone marrow-derived macrophages and dendritic cells. J Bacteriol Virol 42(1):256–263Google Scholar
  35. Uoshimasa N, Akira M, Koichi K, Hajime O (1996) Cancer Lett 108:247–255CrossRefGoogle Scholar
  36. Valentina R, Sonia Z, Marina Z et al (2013) The PDT activity of free and pegylated pheophorbide a against an amelanotic melanoma transplanted in C57/BL6 mice. Investig New Drugs 31:192–199CrossRefGoogle Scholar
  37. Wajirou S (2000) Germination traits and adaptive regeneration strategies of the three carpinus species. J For Res 5:181–185CrossRefGoogle Scholar
  38. Woongsoon J, Christopher RK, Jonghwan L (2013) Application of mathematical models in the spatial analysis of early tree seedling distribution patterns within a treefall gap at gwangneung experimental forest, Korea. J Plant Biol 56:283–289CrossRefGoogle Scholar
  39. Yu W, Ping C, Changyun T et al (2014) Antinociceptive and anti-inflammatory activities of extract and two isolated flavonoids of Carthamus tinctorius L. J Ethnopharmacol 151(2):944–950CrossRefGoogle Scholar
  40. Zahra T, Parina A, Saied G et al (2014) Potent cytotoxic flavonoids from Iranian Securigera securidaca. Med Chem Res 23:1718–1724CrossRefGoogle Scholar
  41. Zhishen J, Mengcheng T, Jianming W (1999) The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem 64(4):55–59CrossRefGoogle Scholar

Copyright information

© The Society for In Vitro Biology 2016

Authors and Affiliations

  • Qianqian Sheng
    • 1
  • Xianying Fang
    • 2
  • Zunling Zhu
    • 1
    • 3
    Email author
  • Wei Xiao
    • 4
    Email author
  • Zhenzhong Wang
    • 4
  • Gang Ding
    • 4
  • Linguo Zhao
    • 2
  • Yujian Li
    • 1
  • Ping Yu
    • 1
  • Zhibin Ding
    • 1
  • Qinru Sun
    • 1
  1. 1.College of Landscape ArchitectureNanjing Forestry UniversityNanjingChina
  2. 2.College of Chemical EngineeringNanjing Forestry UniversityNanjingChina
  3. 3.College of Art & DesignNanjing Forestry UniversityNanjingChina
  4. 4.Jiangsu Kanion Pharmaceutical Co., Ltd.LianyungangChina

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