Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Oncology Letters
      • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Biomedical Reports
      • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • Information for Authors
    • Information for Reviewers
    • Information for Librarians
    • Information for Advertisers
    • Conferences
  • Language Editing
Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • For Authors
    • For Reviewers
    • For Librarians
    • For Advertisers
    • Conferences
  • Language Editing
Login Register Submit
  • This site uses cookies
  • You can change your cookie settings at any time by following the instructions in our Cookie Policy. To find out more, you may read our Privacy Policy.

    I agree
Search articles by DOI, keyword, author or affiliation
Search
Advanced Search
presentation
Oncology Reports
Join Editorial Board Propose a Special Issue
Print ISSN: 1021-335X Online ISSN: 1791-2431
Journal Cover
September-2017 Volume 38 Issue 3

Full Size Image

Sign up for eToc alerts
Recommend to Library

Journals

International Journal of Molecular Medicine

International Journal of Molecular Medicine

International Journal of Molecular Medicine is an international journal devoted to molecular mechanisms of human disease.

International Journal of Oncology

International Journal of Oncology

International Journal of Oncology is an international journal devoted to oncology research and cancer treatment.

Molecular Medicine Reports

Molecular Medicine Reports

Covers molecular medicine topics such as pharmacology, pathology, genetics, neuroscience, infectious diseases, molecular cardiology, and molecular surgery.

Oncology Reports

Oncology Reports

Oncology Reports is an international journal devoted to fundamental and applied research in Oncology.

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine is an international journal devoted to laboratory and clinical medicine.

Oncology Letters

Oncology Letters

Oncology Letters is an international journal devoted to Experimental and Clinical Oncology.

Biomedical Reports

Biomedical Reports

Explores a wide range of biological and medical fields, including pharmacology, genetics, microbiology, neuroscience, and molecular cardiology.

Molecular and Clinical Oncology

Molecular and Clinical Oncology

International journal addressing all aspects of oncology research, from tumorigenesis and oncogenes to chemotherapy and metastasis.

World Academy of Sciences Journal

World Academy of Sciences Journal

Multidisciplinary open-access journal spanning biochemistry, genetics, neuroscience, environmental health, and synthetic biology.

International Journal of Functional Nutrition

International Journal of Functional Nutrition

Open-access journal combining biochemistry, pharmacology, immunology, and genetics to advance health through functional nutrition.

International Journal of Epigenetics

International Journal of Epigenetics

Publishes open-access research on using epigenetics to advance understanding and treatment of human disease.

Medicine International

Medicine International

An International Open Access Journal Devoted to General Medicine.

Journal Cover
September-2017 Volume 38 Issue 3

Full Size Image

Sign up for eToc alerts
Recommend to Library

  • Article
  • Citations
    • Cite This Article
    • Download Citation
    • Create Citation Alert
    • Remove Citation Alert
    • Cited By
  • Similar Articles
    • Related Articles (in Spandidos Publications)
    • Similar Articles (Google Scholar)
    • Similar Articles (PubMed)
  • Download PDF
  • Download XML
  • View XML
Article

Royal jelly lipophilic fraction induces antiproliferative effects on SH-SY5Y human neuroblastoma cells

  • Authors:
    • Angelo Gismondi
    • Eleonora Trionfera
    • Lorena Canuti
    • Gabriele Di Marco
    • Antonella Canini
  • View Affiliations / Copyright

    Affiliations: Department of Biology, University of Rome ‘Tor Vergata’, I-00133 Rome, Italy
  • Pages: 1833-1844
    |
    Published online on: July 24, 2017
       https://doi.org/10.3892/or.2017.5851
  • Expand metrics +
Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )
Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )
Cited By (CrossRef): 0 citations Loading Articles...

This article is mentioned in:



Abstract

Royal jelly (RJ) is one the most important bee product because it strongly influences the larval development in the hive, including the queen bee. In literature, RJ is known for its antioxidant, immunoregulatory, antifungal, antibiotical, erythropoietic, hypoglycemic, anticholesteremic, antithyroidic, anti-osteoporotic and estrogenic properties. However, it is surprising how rare the scientific evidence about RJ antineoplastic capacity are. That being said, we investigated, for the first time, the in vitro bioactivity of six different RJs on the growth of three different mammalian cell lines: immortalized murine myoblasts (C2C12), human prostate cancer (PC3) and human neuroblastoma (SH-SY5Y). These studies were performed treating the cells with the only lipophilic, or hydrophilic, fraction of the RJs, a scientific approach never performed before. Moreover, chemical and protein profiles of all RJs were finely characterized, in qualitative and quantitative terms, by GC-MS and 1D-SDS-PAGE, respectively, in order to give a complete framework to the research. Despite the deep differences we found in the composition of each sample, unexpectedly, RJs showed comparable or very similar biological effects. In particular, our attention was captured by the extraordinary antiproliferative activity of the lipophilic extract of all RJs against SH-SY5Y cells, suggesting a potential medical application of this bee product to prevent the onset and slow down the growth of human neuroblastoma.
View Figures

Figure 1

Figure 2

Figure 3

Figure 4

View References

1 

Haydak MH: Honey bee nutrition. Annu Rev Entomol. 15:143–156. 1970. View Article : Google Scholar

2 

Contessi A: Le api biologia, allevamento, prodotti. 4th. Edagricole, Bologna: 2016, (In Italian).

3 

Nagai T and Inoue R: Preparation and functional properties of water and alkaline extract of royal jelly. Food Chem. 84:181–186. 2004. View Article : Google Scholar

4 

Hanes J and Simúth J: Identification and partial characterization of major royal jelly protein of honeybee (Apis mellifera). J Apic Res. 31:22–26. 1992. View Article : Google Scholar

5 

Schmitzová J, Klaudiny J, Albert S, Schröder W, Schreckengost W, Hanes J, Júdová J and Simúth J: A family of major royal jelly proteins of the honeybee Apis mellifera L. Cell Mol Life Sci. 54:1020–1030. 1998. View Article : Google Scholar : PubMed/NCBI

6 

Boselli E, Caboni MF, Sabatini AG, Marcazzan GL and Lercker G: Determination and changes of free amino acids in royal jelly during storage. Apidologie (Celle). 34:129–137. 2003. View Article : Google Scholar

7 

Fujita T, Kozuka-Hata H, Ao-Kondo H, Kunieda T, Oyama M and Kubo T: Proteomic analysis of the royal jelly and characterization of the functions of its derivation glands in the honeybee. J Proteome Res. 12:404–411. 2013. View Article : Google Scholar : PubMed/NCBI

8 

Lercker G, Savioli S, Vecchi MA, Sabatini AG, Nanetti A and Piana L: Carbohydrate determination of royal jelly by high resolution gas chromatography (HRGC). Food Chem. 19:255–264. 1986. View Article : Google Scholar

9 

Lercker G, Capella P, Conte LS, Ruini F and Giordani G: Components of royal jelly: I. Identification of the organic acids. Lipids. 16:912–919. 1981. View Article : Google Scholar

10 

Caboni MF, Sabatini AG and Lercker G: La gelatina reale: origine, proprietà e composizione/Royal jelly:origin, properties and composition. APOidea. 1:72–79. 2004.

11 

Melliou E and Chinou I: Chemistry and bioactivity of royal jelly from Greece. J Agric Food Chem. 53:8987–8992. 2005. View Article : Google Scholar : PubMed/NCBI

12 

Gómez-Caravaca AM, Gómez-Romero M, Arráez-Román D, Segura-Carretero A and Fernández-Gutiérrez A: Advances in the analysis of phenolic compounds in products derived from bees. J Pharm Biomed Anal. 41:1220–1234. 2006. View Article : Google Scholar : PubMed/NCBI

13 

Mohamed AA, Galal AA and Elewa YH: Comparative protective effects of royal jelly and cod liver oil against neurotoxic impact of tartrazine on male rat pups brain. Acta Histochem. 117:649–658. 2015. View Article : Google Scholar : PubMed/NCBI

14 

Viuda-Martos M, Ruiz-Navajas Y, Fernández-López J and Pérez-Alvarez JA: Functional properties of honey, propolis, and royal jelly. J Food Sci. 73:R117–R124. 2008. View Article : Google Scholar : PubMed/NCBI

15 

Guo H, Saiga A, Sato M, Miyazawa I, Shibata M, Takahata Y and Morimatsu F: Royal jelly supplementation improves lipoprotein metabolism in humans. J Nutr Sci Vitaminol (Tokyo). 53:345–348. 2007. View Article : Google Scholar : PubMed/NCBI

16 

Münstedt K, Bargello M and Hauenschild A: Royal jelly reduces the serum glucose levels in healthy subjects. J Med Food. 12:1170–1172. 2009. View Article : Google Scholar : PubMed/NCBI

17 

Cihangir E, Orhan D, Ercument O and Yasam B: The effects of royal jelly on autoimmunity in Grave's disease. Endocrinologia. 30:175–183. 2006.

18 

Majtán J, Kovácová E, Bíliková K and Simúth J: The immunostimulatory effect of the recombinant apalbumin 1-major honeybee royal jelly protein-on TNFalpha release. Int Immunopharmacol. 6:269–278. 2006. View Article : Google Scholar : PubMed/NCBI

19 

Bincoletto C, Eberlin S, Figueiredo CA, Luengo MB and Queiroz ML: Effects produced by Royal Jelly on haematopoiesis: Relation with host resistance against Ehrlich ascites tumour challenge. Int Immunopharmacol. 5:679–688. 2005. View Article : Google Scholar : PubMed/NCBI

20 

Hidaka S, Okamoto Y, Uchiyama S, Nakatsuma A, Hashimoto K, Ohnishi ST and Yamaguchi M: Royal jelly prevents osteoporosis in rats: Beneficial effects in ovariectomy model and in bone tissue culture model. Evid Based Complement Alternat Med. 3:339–348. 2006. View Article : Google Scholar : PubMed/NCBI

21 

Yatsunami K and Echigo T: Antibacterial action of royal jelly. Bull Fac Agric Tamagawa Univ. 25:13–22. 1985.

22 

Fujiwara S, Imai J, Fujiwara M, Yaeshima T, Kawashima T and Kobayashi K: A potent antibacterial protein in royal jelly. Purification and determination of the primary structure of royalisin. J Biol Chem. 265:11333–11337. 1990.PubMed/NCBI

23 

Taniguchi Y, Kohno K, Inoue S, Koya-Miyata S, Okamoto I, Arai N, Iwaki K, Ikeda M and Kurimoto M: Oral administration of royal jelly inhibits the development of atopic dermatitis-like skin lesions in NC/Nga mice. Int Immunopharmacol. 3:1313–1324. 2003. View Article : Google Scholar : PubMed/NCBI

24 

Shirzad M, Kordyazdi R, Shahinfard N and Nikokar M: Does Royal jelly affect tumor cells. J HerbMed Pharmacol. 2:45–48. 2013.

25 

Tamura T, Fujii A and Kuboyama N: Antitumor effects of royal jelly (RJ). Nippon Yakurigaku Zasshi. 89:73–80. 1987.(In Japanese). View Article : Google Scholar : PubMed/NCBI

26 

Isidorov VA, Bakier S and Grzech I: Gas chromatographic-mass spectrometric investigation of volatile and extractable compounds of crude royal jelly. J Chromatogr B Analyt Technol Biomed Life Sci. 885–886:109–116. 2012. View Article : Google Scholar

27 

Gismondi A, Canuti L, Grispo M and Canini A: Biochemical composition and antioxidant properties of Lavandula angustifolia Miller essential oil are shielded by propolis against UV radiations. Photochem Photobiol. 90:702–708. 2014. View Article : Google Scholar : PubMed/NCBI

28 

Giovannini D, Gismondi A, Basso A, Canuti L, Braglia R, Canini A, Mariani F and Cappelli G: Lavandula angustifolia Mill. essential oil exerts antibacterial and anti-inflammatory effect in macrophage mediated immune response to Staphylococcus aureus. Immunol Invest. 45:11–28. 2016. View Article : Google Scholar : PubMed/NCBI

29 

Li J, Wang T, Zhang Z and Pan Y: Proteomic analysis of royal jelly from three strains of western honeybees (Apis mellifera). J Agric Food Chem. 55:8411–8422. 2007. View Article : Google Scholar : PubMed/NCBI

30 

Bradford MM: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 72:248–254. 1976. View Article : Google Scholar : PubMed/NCBI

31 

Gismondi A, Lentini A, Tabolacci C, Provenzano B and Beninati S: Transglutaminase-dependent antiproliferative and differentiative properties of nimesulide on B16-F10 mouse melanoma cells. Amino Acids. 38:257–262. 2010. View Article : Google Scholar : PubMed/NCBI

32 

Scarselli R, Donadio E, Giuffrida MG, Fortunato D, Conti A, Balestreri E, Felicioli R, Pinzauti M, Sabatini AG and Felicioli A: Towards royal jelly proteome. Proteomics. 5:769–776. 2005. View Article : Google Scholar : PubMed/NCBI

33 

Howe SR, Dimick PS and Benton AW: Composition of freshly harvested and commercial royal jelly. J Apic Res. 24:52–61. 1985. View Article : Google Scholar

34 

Kodai T, Umebayashi K, Nakatani T, Ishiyama K and Noda N: Compositions of royal jelly II. Organic acid glycosides and sterols of the royal jelly of honeybees (Apis mellifera). Chem Pharm Bull (Tokyo). 55:1528–1531. 2007. View Article : Google Scholar : PubMed/NCBI

35 

Bogdanov S: Royal Jelly, Bee Brood: Composition, Health, Medicine: A Review. Bee Product Sci. 1–36. 2011.

36 

Antinelli JF, Zeggane S, Ico R Dav, Rognone C, Faucon JP and Lizzani L: Evaluation of (E)-10-hydroxydec-2-enoic acid as a freshness parameter for royal jelly. Food Chem. 80:85–89. 2003. View Article : Google Scholar

37 

Matsuka M: Content of benzoic acid in royal jelly and propolis. Mitsubachi Kagaku. 14:79–80. 1993.

38 

Rizwan K, Zubair M, Rasool N, Riaz M, Zia-Ul-Haq M and de Feo V: Phytochemical and biological studies of Agave attenuata. Int J Mol Sci. 13:6440–6451. 2012. View Article : Google Scholar : PubMed/NCBI

39 

Klaudiny J, Hanes J, Kulifajová J, Albert Š and Šimúth J: Molecular cloning of two cDNAs from the head of the nurse honeybee (Apis mellifera L.) for coding related proteins of royal jelly. J Apic Res. 33:105–111. 1994.doi: 10.1080/00218839.1994.11100857. View Article : Google Scholar

40 

Hashimoto M, Kanda M, Ikeno K, Hayashi Y, Nakamura T, Ogawa Y, Fukumitsu H, Nomoto H and Furukawa S: Oral administration of royal jelly facilitates mRNA expression of glial cell line-derived neurotrophic factor and neurofilament H in the hippocampus of the adult mouse brain. Biosci Biotechnol Biochem. 69:800–805. 2005. View Article : Google Scholar : PubMed/NCBI

41 

Hattori N, Nomoto H, Fukumitsu H, Mishima S and Furukawa S: Royal jelly and its unique fatty acid, 10-hydroxy-trans-2-decenoic acid, promote neurogenesis by neural stem/progenitor cells in vitro. Biomed Res. 28:261–266. 2007. View Article : Google Scholar : PubMed/NCBI

Related Articles

  • Abstract
  • View
  • Download
  • Twitter
Copy and paste a formatted citation
Spandidos Publications style
Gismondi A, Trionfera E, Canuti L, Di Marco G and Canini A: Royal jelly lipophilic fraction induces antiproliferative effects on SH-SY5Y human neuroblastoma cells. Oncol Rep 38: 1833-1844, 2017.
APA
Gismondi, A., Trionfera, E., Canuti, L., Di Marco, G., & Canini, A. (2017). Royal jelly lipophilic fraction induces antiproliferative effects on SH-SY5Y human neuroblastoma cells. Oncology Reports, 38, 1833-1844. https://doi.org/10.3892/or.2017.5851
MLA
Gismondi, A., Trionfera, E., Canuti, L., Di Marco, G., Canini, A."Royal jelly lipophilic fraction induces antiproliferative effects on SH-SY5Y human neuroblastoma cells". Oncology Reports 38.3 (2017): 1833-1844.
Chicago
Gismondi, A., Trionfera, E., Canuti, L., Di Marco, G., Canini, A."Royal jelly lipophilic fraction induces antiproliferative effects on SH-SY5Y human neuroblastoma cells". Oncology Reports 38, no. 3 (2017): 1833-1844. https://doi.org/10.3892/or.2017.5851
Copy and paste a formatted citation
x
Spandidos Publications style
Gismondi A, Trionfera E, Canuti L, Di Marco G and Canini A: Royal jelly lipophilic fraction induces antiproliferative effects on SH-SY5Y human neuroblastoma cells. Oncol Rep 38: 1833-1844, 2017.
APA
Gismondi, A., Trionfera, E., Canuti, L., Di Marco, G., & Canini, A. (2017). Royal jelly lipophilic fraction induces antiproliferative effects on SH-SY5Y human neuroblastoma cells. Oncology Reports, 38, 1833-1844. https://doi.org/10.3892/or.2017.5851
MLA
Gismondi, A., Trionfera, E., Canuti, L., Di Marco, G., Canini, A."Royal jelly lipophilic fraction induces antiproliferative effects on SH-SY5Y human neuroblastoma cells". Oncology Reports 38.3 (2017): 1833-1844.
Chicago
Gismondi, A., Trionfera, E., Canuti, L., Di Marco, G., Canini, A."Royal jelly lipophilic fraction induces antiproliferative effects on SH-SY5Y human neuroblastoma cells". Oncology Reports 38, no. 3 (2017): 1833-1844. https://doi.org/10.3892/or.2017.5851
Follow us
  • Twitter
  • LinkedIn
  • Facebook
About
  • Spandidos Publications
  • Careers
  • Cookie Policy
  • Privacy Policy
How can we help?
  • Help
  • Live Chat
  • Contact
  • Email to our Support Team