Skip to main content
Log in

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

  • Published:
In Vitro Cellular & Developmental Biology - Animal Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1.
Figure 2.
Figure 3.

Similar content being viewed by others

References

  • Alejandro GM (1996) Kinetic model for chlorophyll degradation in green tissue. Pheophorbide degradation to colorless compounds. J Agric Food Chem 44:3735–3740

    Article  Google Scholar 

  • 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 13:14

    Article  Google Scholar 

  • Anna JK, Tomasz W (1990) Species deletion in Potentillo albae-Quercetum phytocoenoses reversed by the removal of Carpinus betulus. Vegetatio 87:115–126

    Article  Google Scholar 

  • Bono L, Visˇnja S, Dejan P et al (2014) Correlation between 13C NMR chemical shifts and antiradical activity of flavonoids. Monatsh Chem 145:457–463

    Article  Google Scholar 

  • 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 58:293–297

    Article  CAS  Google Scholar 

  • Changwei H, Juyun C, Tenghsu W et al (2014) Hypoglycaemic effects of Ajuga extract in vitro and in vivo. J Funct Foods 6:224–230

    Article  Google Scholar 

  • 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 53:2746–2750

    Article  Google Scholar 

  • Chinsung C, Jeong IJ (2004) Foliar flavonoids of the most primitive group, sect. Distegocarpus within the genus Carpinus. Biochem Syst Ecol 32:35–44

    Article  Google Scholar 

  • 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.

  • 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 95:473–487

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Els C, Sabine VG, Remy JP et al (2005) Range wide versus local patterns of genetic diversity in hornbeam (Carpinus betulus L.). Conserv Genet 6:259–273

    Article  Google Scholar 

  • Ewa C, Luc A, Thierry G et al (2012) Potential anticancer activity of young Carpinus betulus leaves. Phytomedicine 19:278–283

    Article  Google Scholar 

  • Flax MH, Caulfield JB (1963) Cellular and vascular components of allergic contact dermatitis. Am J Pathol 43:1031–1053

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gamal AM, Sabrin RMI, Nawal MA, Samir AR (2014) New anti-inflammatory flavonoids from Cadaba glandulosa Forssk. Arch Pharm Res 37:459–466

    Article  Google Scholar 

  • Gomah N (2013) Antimicrobial activity of Calotropis procera Ait. (Asclepiadaceae) and isolation of four flavonoid glycosides as the active constituents. World J Microbiol Biotechnol 29:1255–1262

    Article  Google Scholar 

  • Grabbe S, Schwarz T (1998) Immunoregulatory mechanisms involved in elicitation of allergic contact hypersensitivity. Immunol Today 19:37–44

    Article  CAS  PubMed  Google Scholar 

  • 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):255–262

    Article  Google Scholar 

  • 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):157–163

    Article  Google Scholar 

  • Haoyu Y, Wenshuang W, Zhuowei L et al (2014) Bioactivity-guided isolation of anti-inflammation flavonoids from the stems of Millettia dielsiana Harms. Fitoterapia 95:154–159

    Article  Google Scholar 

  • Hongjie Z, Ghee TT, Vu DH et al (2003) Natural anti-HIV agents. Part IV. Anti-HIV constituents from Vatica cinerea. J Nat Prod 66:263–268

    Article  Google Scholar 

  • 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 34:6454–6463

    Article  Google Scholar 

  • Jeong IJ, Chinsung C, Zhiduan C, Tae YP (2007) Systematic aspects of foliar flavonoids in subsect. Carpinus (Carpinus, Betulaceae). Biochem Syst Ecol 35:606–613

    Article  Google Scholar 

  • 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 48:197–202

    Article  Google Scholar 

  • 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 58:793–797

    Article  Google Scholar 

  • Lai CS, Mas RN, Mansor SM et al (2010) Chemical constituents and in vitro anticancer activity of Typhonium flagelliforme (Araceae). J Ethnopharmacol 127:486–494

    Article  CAS  PubMed  Google Scholar 

  • 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 20:583–591

    CAS  PubMed  Google Scholar 

  • Lamjed B, Kyoko H, JungBum L et al (2011) Potent virucidal effect of pheophorbide a and pyropheophorbide a on enveloped viruses. J Nat Med 65:229–233

    Article  Google Scholar 

  • Le DMG, Havill DC (1998) Competition between Quercus petraea and Carpinus betulus in an ancient wood in England. seedling survivorship. J Veg Sci 9:873–880

    Article  Google Scholar 

  • Mohammed KH, Hye YC, Jaeseon H et al (2014) Antiviral activity of 3, 4’-dihydroxyflavone on influenza a virus. J Microbiol 52(6):521–526

    Article  Google Scholar 

  • Mohan S, Nandhakumar L (2014) Role of various flavonoids: hypotheses on novel approach to treat diabetes. J Med Hypotheses Ideas 8:1–6

    Article  CAS  Google Scholar 

  • 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 54:101–111

    Article  Google Scholar 

  • 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 64:349–356

    Article  Google Scholar 

  • 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 946:68–74

    Google Scholar 

  • 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):256–263

    Google Scholar 

  • Uoshimasa N, Akira M, Koichi K, Hajime O (1996) Cancer Lett 108:247–255

    Article  Google Scholar 

  • 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 31:192–199

    Article  Google Scholar 

  • Wajirou S (2000) Germination traits and adaptive regeneration strategies of the three carpinus species. J For Res 5:181–185

    Article  Google Scholar 

  • 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 56:283–289

    Article  Google Scholar 

  • 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):944–950

    Article  Google Scholar 

  • Zahra T, Parina A, Saied G et al (2014) Potent cytotoxic flavonoids from Iranian Securigera securidaca. Med Chem Res 23:1718–1724

    Article  Google Scholar 

  • 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):55–59

    Article  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Zunling Zhu or Wei Xiao.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Editor: Tetsuji Okamoto

Qianqian Sheng and Xianying Fang contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sheng, Q., Fang, X., Zhu, Z. et al. Seasonal variation of pheophorbide a and flavonoid in different organs of two Carpinus species and its correlation with immunosuppressive activity. In Vitro Cell.Dev.Biol.-Animal 52, 654–661 (2016). https://doi.org/10.1007/s11626-016-0041-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11626-016-0041-1

Keywords

Navigation