Antiproliferative activity and apoptotic effects of Filipendula ulmaria pollen against C26 mice colon tumour cells

Open access


Honeybee collected pollen exhibits high nutritional and pharmaceutical benefits for the human diet and medicine. Pollen’s antioxidant, anti-ageing, anti-inflammatory, anti-atherosclerosis, and cardioprotective activity, depending on the floral origin, are well known. Recent studies proposed that pollen may also be an excellent cancer-fighting candidate, as pollen harbours high amounts of phenolic substances. In our study, Filipendula ulmaria pollen (bee collected) was methanol-water extracted and used to verify its in vitro pharmacological activities on C26 mice cancer tumour cells. Three different concentrations of the extract were tested in antitumour assays. Monitoring was done after 6, 12, 24, and 48 hours. Promising results were obtained for antiproliferative and apoptotic activity of the pollen extracts, with high efficiency for the highest concentration (1 mg/mL). For both activities, time and concentration-dependent effects were observed. Pollen extracts or bee collected pollen has a high potential as an antitumour agent for use in human medicine, because they are both rich in bioactive compounds.

Aulino, P., Berardi, E., Cardillo, V.M., Rizzuto, E., Perniconi, B., Ramina, C., Padula, F., Spugnini, E.P., Baldi, A., Faiola, F., Adamo, S., Coletti, D. (2010). Molecular, cellular and physiological characterization of the cancer cachexia-inducing C26 colon carcinoma in mouse. BMC Cancer, 10, 363.

Bogdanov, S. (2004). Quality and standards of pollen and beeswax. Apiacta, 38, 334-341.

Campos, M., Markham, K.R., Mitchell, K.A., da Cunha, A.P. (1997). An approach to the characterization of bee pollens via their flavonoid/phenolic profiles. Phytochemical Analysis, 8(4), 181-185.<181::AIDPCA359>3.0.CO;2-A

Campos, M.G., Webby, R.F., Markham, K.R., Mitchell, K.A., da Cunha, A.P. (2003). Age-induced diminution of free radical scavenging capacity in bee pollens and the contribution of constituent flavonoids. Journal of Agriculture and Food Chemistry, 51(3), 742-745.

Campos, M.G.R., Bogdanov, S., de Almeida-Muradian, L.B., Szczesna, T., Mancebo, Y., Frigerio, C., Ferreira, F. (2008). Pollen composition and standardization of analytical methods. Journal of Apicultural Research, 47(2), 156-163.

Cárdenas, M., Marder, M., Blank, V.C., Roguin, L.P. (2006). Antitumor activity of some natural flavonoids and synthetic derivatives on various human and murine cancer cell lines. Bioorganic & Medicinal Chemistry, 14(9), 2966-2971.

Carpes, S.T., Begnini, R., Matias de Alencar, S., Masson, M.L. (2007). Study of preparations of bee pollen extracts, antioxidant and antibacterial activity. Ciência e Agrotecnologia, 31(6), 1818-1825.

Catchpole, O., Mitchell, K., Bloor, S., Davis, P., Suddes, A. (2015). Antiproliferative activity of New Zealand propolis and phenolic compounds vs human colorectal adenocarcinoma cells. Fitoterapia, 106, 167-74.

Chu, H.L., Mao, H., Feng, W., Liu, J.W., Geng, Y. (2013). Effects of sulfated polysaccharide from Masson pine (Pinus massoniana) pollen on the proliferation and cell cycle of HepG2 cells. International Journal of Biological Macromolecules, 55, 104-8.

Dezmirean, G.I., Mărghitaş, L.A., Bobiş, O., Dezmirean, D.S., Bonta, V., Erler, S. (2012). Botanical origin causes changes in nutritional profile and antioxidant activity of fermented products obtained from honey. Journal of Agricultural and Food Chemistry, 60(32), 8028-8035.

Duda, S.D., Mărghitaş, L.A., Dezmirean, D., Duda, M., Mărgăoan, R., Bobiş, O. (2015). Changes in major bioactive compounds with antioxidant activity of Agastache foeniculum, Lavandula angustifolia, Melissa officinalis and Nepeta cataria: Effect of harvest time and plant species. Industrial Crops and Products, 77, 499-507.

Eraslan, G., Kanbur, M., & Silici, S. (2009). Effect of carbaryl on some biochemical changes in rats: the ameliorative effect of bee pollen. Food and Chemical Toxicology, 47(1), 86-91.

Erler, S., & Moritz, R.F.A. (2015). Pharmacophagy and pharmacophory: mechanisms of self-medication and disease prevention in the honeybee colony (Apis mellifera). Apidologie, (early online).

Furusawa, A.E., Chou, S.C., Hirazumi, A., Melera, A. (1995). Antitumour potential of pollen extract on lewis lung carcinoma implaned intraperitoneally in syngeneic mice. Phytotherapy Research, 9(4), 255-259.

Hisada, M., Yoshimoto, T., Kamiya, S., Magami, Y., Miyaji, H., Yoneto, T., Tamada, K., Aoki, T., Koyanagi, Y., Mizuguchi, J. (2004). Synergistic antitumor effect by coexpression of chemokine CCL21/SLC and costimulatory molecule LIGHT. Cancer Gene Therapy, 11, 280-288.

Komosinska-Vassev, K., Olczyk, P., Kaźmierczak, J., Mencner, L., Olczyk, K. (2015). Pollen: chemical composition and therapeutic application. Evidence- Based Complementary and Alternative Medicine, 2015, 297425.

Kroyer, G., & Hegedus, N. (2001). Evaluation of bioactive properties of pollen extracts as functional dietary food supplements. Innovative Food Science and Emerging Technologies, 2(3), 171-174.

Kustiawan, P.M., Puthong, S., Arung, E.T., Chanchao, C. (2014). In vitro cytotoxicity of Indonesian stingless bee products against human cancer cell lines. Asian Pacific Journal of Tropical Biomedicine, 4(7), 549-56.

LeBlanc, B.W., Davis, O.K., Boue, S., DeLucca, A., Deeby, T. (2009). Antioxidant activity of Sonoran Desert bee pollen. Food Chemistry, 115(4), 1299-1305.

Leng, J., Zhang, L., Yao, H., Cao, X. (2003). Antitumor effects of interleukin-18 gene-modified hepatocyte cell line on implanted liver carcinoma. Chinese Medical Journal, 116(10), 1475-1479.

Lopes, J., Stanciu, O.G., Campos, M.G., Almaraz-Abarca, N., Almeida-Muradian, L.B., Marghitas, L.A. (2011). Bee pollen antioxidant activity - a review: achievements and further challenges. Journal of Pharmacognosy, 2(2), 25-38.

Louveaux, J., Maurizio, A., & Vorwohl, G. (1978). Methods of melissopalynology. Bee World, 59(4), 139-157.

Mărgăoan, R., Mărghitaş, L.A., Dezmirean, D., Dulf, F.V., Bunea, A., Socaci, S.A., Bobiş, O. (2014). Predominant and secondary pollen botanical origins influence the carotenoid and fatty acid profile in fresh honeybee-collected pollen. Journal of Agricultural and Food Chemistry, 62(27), 6306-6316.

Mărghitaş, L.A., Stanciu, O.G., Dezmirean, D.S., Bobiş, O., Popescu, O., Bogdanov, S., Campos, M.G. (2009). In vitro antioxidant capacity of honeybee-collected pollen of selected floral origin harvested from Romania. Food Chemistry, 115(3), 878-883.

Markiewicz-Żukowska, R., Naliwajko, S.K., Bartosiuk, E., Moskwa, J., Isidorov, V., Soroczyńska, J., Borawska, M.H. (2013). Chemical composition and antioxidant activity of beebread, and its influence on the glioblastoma cell line (U87MG). Journal of Apicultural Science, 57(2), 147-157.

Morais, M., Moreira, L., Feas, X., Estevinho, L.M. (2011). Honeybee-collected pollen from five Portuguese natural Parks: Palynological origin, phenolic content, antioxidant properties and antimicrobial activity. Food and Chemical Toxicology, 49(5), 1096-1101.

Newman, D.J., & Cragg, G.M. (2007). Natural products as sources of new drugs over the 30 years from 1981 to 2010. Journal of Natural Products, 75(3), 311-335.

Pascoal, A., Rodrigues, S., Teixeira, A., Feás, X., Estevinho, L.M. (2014). Biological activities of commercial bee pollens: antimicrobial, antimutagenic, antioxidant and anti-inflammatory. Food and Chemical Toxicology, 63, 233-239.

Pavel, C.I., Mărghitaş, L.A., Dezmirean, D.S., Tomoş, L.I., Bonta, V., Şapcaliu, A., Buttstedt, A. (2014). Comparison between local and commercial royal jelly - use of antioxidant activity and 10-hydroxy-2-decenoic acid as quality parameter. Journal of Apicultural Research, 53(1), 116-123.

Rzepecka-Stojko, A., Stojko, J., Kurek-Górecka, A., Górecki, M., Kabała-Dzik, A., Kubina, R., Moździerz, A., Buszman, E. (2015). Polyphenols from bee pollen: structure, absorption, metabolism and biological activity. Molecules, 20(12), 21732-21749.

Serra Bonvehí, J., Soliva Torrentó, M., Centelles Lorente, E. (2001). Evaluation of polyphenolic and flavonoid compounds in honeybee-collected pollen produced in Spain. Journal of Agricultural and Food Chemistry, 49(4), 1848-53.

Stanciu, O.G., Mărghitaş, L.A., Dezmirean, D., Tămaş, M. (2011). Flavonoid content of unifloral bee pollen harvested from Transylvania, evaluated spectrophotometricaly by ZrOCl2 reagent. Economics, Management, and Financial Markets, 6(1), 1222-1227.

STATISTICA, Version 8.0. StatSoft, Tulsa, Oklahoma, USA

Szczęsna, T. (2007). Study on the sugar composition of honeybee-collected pollen. Journal of Apicultural Science, 51(1), 15-21.

Wu, Y.D., & Lou, Y.J. (2007). A steroid fraction of chloroform extract from bee pollen of Brassica campestris induces apoptosis in human prostate cancer PC-3 cells. Phytotherapy Research, 21(11), 1087-91.

Journal of Apicultural Science

The Journal of Research Institute of Horticulture and Apicultural Research Association

Journal Information

IMPACT FACTOR 2017: 0.75
5-year IMPACT FACTOR: 1.007

CiteScore 2017: 0.92

SCImago Journal Rank (SJR) 2017: 0.345
Source Normalized Impact per Paper (SNIP) 2017: 0.461

Cited By


All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 247 247 16
PDF Downloads 109 109 6