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Sulforaphane and related mustard oils in focus of cancer prevention and therapy

Sulforaphan und verwandte Senföle im Fokus der Prävention und Therapie von Krebs

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Summary

The plant family Brassicaceae, formerly Cruciferae, contains mustard oil glycosides, from which mustard oils are enzymatically hydrolyzed. Mustard oils offer protection from pests, microorganisms and fungi. More than 120 different mustard oils with various biological functions are known. Since ancient times, these substances are used as natural antibiotics, antiviral drugs and antimycotics. The antioxidative effect of mustard oils contributes to protection from DNA damage. Epidemiological and experimental studies have shown preventive and therapeutic effects of crucifers or isolated substances thereof. Particularly well studied is the mustard oil sulforaphane, which is contained in high concentrations in broccoli and its sprouts. As has been shown in mice recently, sulforaphane also targets the most malignant cancer stem cells, which are not affected by conventional cancer treatments. Based on these promising results, the first prospective clinical studies with cancer patients and sulforaphane-enriched broccoli sprouts have now been initiated in the United States.

Zusammenfassung

Die Pflanzenfamilie Brassicaceae, mit älterem Namen Cruciferae, enthält Senfölglykoside, woraus durch enzymatische Hydrolyse Senföle entstehen, welche Schutz vor Fraßfeinden, Mikroorganismen und Pilzen bieten. Über 120 verschiedene Senföle mit vielfältigen biologischen Funktionen sind bekannt. Seit der Antike kommen diese Substanzen in der Heilkunde als natürliche Antibiotika, Virostatika und Anti-Mykotika zum Einsatz. Der antioxidative Effekt von Senfölen trägt zum Schutz vor DNA-Schäden bei. Epidemiologische und experimentelle Studien belegen eine präventive und therapeutische Wirkung von Gemüse der Kreuzblütlerfamilie und isolierter Substanzen daraus. Besonders gut untersucht ist das Senföl Sulforaphan, das in hoher Konzentration in Brokkoli und seinen Sprossen enthalten ist. Wie an Mäusen nun gezeigt wurde, greift Sulforaphan sogar die besonders bösartigen Krebsstammzellen an, denen konventionelle Tumortherapien nichts anhaben. Aufgrund dieser vielversprechenden Ergebnisse sind nun in den USA erste prospektive Klinische Studien mit Sulforaphan-angereicherten Brokkolisprossen bei Krebspatienten angelaufen.

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References

  1. Fenwick GR, Heaney RK, Mullin WJ. Glucosinolates and their breakdown products in food and food plants. Crit Rev Food Sci Nutr. 1983;18:123–48.

    PubMed  CAS  Google Scholar 

  2. Beliveau R, Gingras D. Krebszellen mögen keine Himbeeren. Nahrungsmittel gegen Krebs. 13th ed. München: Kösel; 2007.

    Google Scholar 

  3. Pechatschek H. Kohlblatt: Ein großes Geschenk der Natur. 13th ed. Steyr: Ennsthaler; 1987/2009.

    Google Scholar 

  4. Rosa EAS, Heaney RK, Fenwick GR, et al. Glucosinolates in crop plants. Hortic Rev. 1997;19:99–215.

    CAS  Google Scholar 

  5. Juge N, Mithen RF, Traka M. Molecular basis for chemoprevention by sulforaphane: a comprehensive review. Cell Mol Life Sci. 2007;64:1105–27.

    Article  PubMed  CAS  Google Scholar 

  6. Joseph MA, Moysich KB, Freudenheim JL, et al. Cruciferous vegetables, genetic polymorphisms in glutathione S-transferases M1 and T1, and prostate cancer risk. Nutr Cancer. 2004;50:206–13.

    Article  PubMed  CAS  Google Scholar 

  7. Hayes JD, Kelleher MO, Eggleston IM. The cancer chemopreventive actions of phytochemicals derived from glucosinolates. Eur J Nutr. 2008;47 Suppl 2:73–88.

    Article  PubMed  CAS  Google Scholar 

  8. Higdon JV, Delage B, Williams DE, et al. Cruciferous vegetables and human cancer risk: epidemiologic evidence and mechanistic basis. Pharmacol Res. 2007;55:224–36.

    Article  PubMed  CAS  Google Scholar 

  9. Keum YS, Jeong WS, Kong AN. Chemopreventive functions of isothiocyanates. Drug News Perspect. 2005;18:445–51.

    Article  PubMed  CAS  Google Scholar 

  10. Fahey JW, Zalcmann AT, Talalay P. The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry. 2001;56:5–51.

    Article  PubMed  CAS  Google Scholar 

  11. Ratzka A, Vogel H, Kliebenstein DJ, et al. Disarming the mustard oil bomb. Proc Natl Acad Sci U S A. 2002;99:11223–8.

    Article  PubMed  CAS  Google Scholar 

  12. Halkier BA, Gershenzon J. Biology and biochemistry of glucosinolates. Annu Rev Plant Biol. 2006;57:303–33.

    Article  PubMed  CAS  Google Scholar 

  13. Griffiths DW, Birch ANE, Hillman JR. Antinutritional compounds in the brassicaceae: analysis, biosynthesis, chemistry and dietary effects. J Hort Sci Biotech. 1998;73:1–18.

    Article  CAS  Google Scholar 

  14. Engel E, Baty C, Le Corre D, et al. Flavor-active compounds potentially implicated in cooked cauliflower acceptance. J Agric Food Chem. 2002;50:6459–67.

    Article  PubMed  CAS  Google Scholar 

  15. Shin IS, Masuda H, Naohide K. Bactericidal activity of wasabi (wasabia japonica) against Helicobacter pylori. Int J Food Microbiol. 2004;94:255–61.

    Article  PubMed  Google Scholar 

  16. Romanowski F, Klenk H. Thiocyanates and isothiocyanates, organic. Weinheim: Wiley-VCH; 2005.

    Google Scholar 

  17. Schilcher H, Kammerer S, Wegener T. Leitfaden Phytotherapie. 4th ed. München: Urban & Fischer; 2010.

    Google Scholar 

  18. Conrad A, Kolberg T, Engels I, et al. In-vitro-Untersuchungen zur antibakteriellen Wirksamkeit einer Kombination aus Kapuzinerkressenkraut (Tropaeoli majoris herb a) und Meerrettichwurzel (Armoraciae rusticaneae radix). Arzneimittelforschung. 2006;56:842–9.

    PubMed  CAS  Google Scholar 

  19. Stingl W. Influenza-Viren mit Phytotherapie bekämpfen. Ärzte Zeitung.de. 2010 Oct 16.

  20. Winter AG, Willeke L. Untersuchungen über den Einfluss von Senfölen auf die Vermehrung des Influenza-Virus im exembryonierten Hühnerei. Arch Mikrobiol. 1958;31:311–8.

    Article  Google Scholar 

  21. Singh SV, Kim SH, Sehrawat A, et al. Biomarkers of phenethyl isothiocyanate-mediated mammary cancer chemoprevention in a clinically relevant mouse model. J Natl Cancer Inst. 2012;104:1228–39.

    Article  PubMed  CAS  Google Scholar 

  22. Verhoeven DT, Goldbohm RA, van Poppel G, et al. Epidemiological studies on brassica vegetables and cancer risk. Cancer Epidemiol Biomarkers Prev. 1996;5:733–48.

    PubMed  CAS  Google Scholar 

  23. Herr I, Büchler MW. Dietary constituents of broccoli and other cruciferous vegetables: implications for prevention and therapy of cancer. Cancer Treat Rev. 2010;36:377–83.

    Article  PubMed  CAS  Google Scholar 

  24. Forman D, Burley V, Cade J, et al. The associations between food, nutrition and physical activity and the risk of pancreatic cancer and underlying mechanisms. In: World Cancer Research Fund. Food, nutrition, physical activity, and the prevention of cancer: a global perspective. Washington, DC: AICR; 2007

    Google Scholar 

  25. Silverman DT, Swanson CA, Gridley G, et al. Dietary and nutritional factors and pancreatic cancer: a case-control study based on direct interviews. J Natl Cancer Inst. 1998;90:1710–9.

    Article  PubMed  CAS  Google Scholar 

  26. Kirsh VA, Peters U, Mayne ST, et al. Prospective study of fruit and vegetable intake and risk of prostate cancer. J Natl Cancer Inst. 2007;99:1200–9.

    Article  PubMed  Google Scholar 

  27. Richman EL, Carroll PR, Chan JM. Vegetable and fruit intake after diagnosis and risk of prostate cancer progression. Int J Cancer. 2012;131(1):201–10.

    Article  PubMed  CAS  Google Scholar 

  28. Hoelzl C, Lorenz O, Haudek V, et al. Proteome alterations induced in human white blood cells by consumption of Brussels sprouts: results of a pilot intervention study. Proteomics Clin Appl. 2008;2:108–17.

    Article  PubMed  CAS  Google Scholar 

  29. Prochazka Z. Isolation of sulforaphane from hoary cress. Collet Czech Chem Commun. 1959;24:2429–30.

    CAS  Google Scholar 

  30. Fahey JW, Talalay P. Antioxidant functions of sulforaphane: a potent inducer of Phase II detoxication enzymes. Food Chem Toxicol. 1999;37:973–9.

    Article  PubMed  CAS  Google Scholar 

  31. Zhang Y, Talalay P, Cho CG, et al. A major inducer of anticarcinogenic protective enzymes from broccoli: isolation and elucidation of structure. Proc Natl Acad Sci U S A. 1992;89:2399–403.

    Article  PubMed  CAS  Google Scholar 

  32. Fahey JW, Zhang Y, Talalay P. Broccoli sprouts: an exceptionally rich source of inducers of enzymes that protect against chemical carcinogens. Proc Natl Acad Sci U S A. 1997;94:10367–72.

    Article  PubMed  CAS  Google Scholar 

  33. Prochazka Z, Komersova I. Isolation of sulforaphane from Cardaria draba and its antimicrobial effect. Cesk Farm. 1959;8:373–6.

    Google Scholar 

  34. Dornberger K, Böckel V, Heyer J, et al. Untersuchungen über die Isothiocyanate Erysolin und Sulforaphan aus Cardaria draba L. Pharmazie. 1975;30:792–6.

    PubMed  CAS  Google Scholar 

  35. Shishu, Singla AK, Kaur IP. Inhibition of mutagenicity of food-derived heterocyclic amines by sulphoraphene-an isothiocyanate isolated from radish. Planta Med. 2003;69:184–6.

    Article  PubMed  CAS  Google Scholar 

  36. Herr I, Büchler MW. Glukosinolate der Kreuzblütlerfamilie in Prävention und Therapie maligner Tumore. Dtsch Z Onkol. 2009;41:109–14.

    Article  Google Scholar 

  37. Bertl E, Bartsch H, Gerhauser C. Inhibition of angiogenesis and endothelial cell functions are novel sulforaphane-mediated mechanisms in chemoprevention. Mol Cancer Ther. 2006;5:575–85.

    Article  PubMed  CAS  Google Scholar 

  38. Myzak MC, Dashwood RH. Chemoprotection by sulforaphane: keep one eye beyond Keap1. Cancer Lett. 2006;233:208–18.

    Article  PubMed  CAS  Google Scholar 

  39. Kallifatidis G, Rausch V, Baumann B, et al. Sulforaphane targets pancreatic tumour-initiating cells by NF-kappaB-induced antiapoptotic signalling. Gut. 2009;58:949–63.

    Article  PubMed  CAS  Google Scholar 

  40. Abbott A. Cancer: the root of the problem. Nature. 2006;442:742–3.

    Article  PubMed  CAS  Google Scholar 

  41. Kallifatidis G, Labsch S, Rausch V, et al. Sulforaphane increases drug-mediated cytotoxicity towards cancer stem-like cells of pancreas and prostate. Mol Ther. 2011;19:188–95.

    Article  PubMed  CAS  Google Scholar 

  42. Rausch V, Liu L, Kallifatidis G, et al. Synergistic activity of sorafenib and sulforaphane abolishes pancreatic cancer stem cell characteristics. Cancer Res. 2010;70:5004–13.

    Article  PubMed  CAS  Google Scholar 

  43. Li Y, Zhang T, Korkaya H, et al. Sulforaphane, a dietary component of broccoli/broccoli sprouts, inhibits breast cancer stem cells. Clin Cancer Res. 2010;16:2580–90.

    Article  PubMed  CAS  Google Scholar 

  44. Li Y, Wicha MS, Schwartz SJ, et al. Implications of cancer stem cell theory for cancer chemoprevention by natural dietary compounds. J Nutr Biochem. 2011;22:799–806.

    Article  PubMed  CAS  Google Scholar 

  45. Reagan-Shaw S, Nihal M, Ahmad N. Dose translation from animal to human studies revisited. FASEB J. 2008;22:659–61.

    Article  PubMed  CAS  Google Scholar 

  46. Sasaki K, Neyazaki M, Shindo K, et al. Quantitative profiling of glucosinolates by LC-MS analysis reveals several cultivars of cabbage and kale as promising sources of sulforaphane. J Chromatogr B Analyt Technol Biomed Life Sci. 2012;903:171–6.

    Article  PubMed  CAS  Google Scholar 

  47. Meyer M, Adam ST. Comparison of glucosinolate levels in commercial broccoli and red cabbage from conventional and exological farming. Eur Food Res Technol. 2008;226:1429–37.

    Article  CAS  Google Scholar 

  48. Sarikamis G, Marquez J, MacCormack R, et al. High glucosinolate broccoli: a delivery system for sulforaphane. Mol Breeding. 2006;18:219–28.

    Article  CAS  Google Scholar 

  49. Conaway CC, Getahun SM, Liebes LL, et al. Disposition of glucosinolates and sulforaphane in humans after ingestion of steamed and fresh broccoli. Nutr Cancer. 2000;38:168–178.

    Article  PubMed  CAS  Google Scholar 

  50. Li F, Hullar MA, Beresford SA, et al. Variation of glucoraphanin metabolism in vivo and ex vivo by human gut bacteria. Br J Nutr. 2011;106:408–16.

    Article  PubMed  CAS  Google Scholar 

  51. Farnham MW, Stephenson KK, Fahey JW. Glucoraphanin level in broccoli seed is largely determined by genotype. HortScience. 2005;40:50–3.

    CAS  Google Scholar 

  52. Kensler TW, Chen JG, Egner PA, et al. Effects of glucosinolate-rich broccoli sprouts on urinary levels of aflatoxin-DNA adducts and phenanthrene tetraols in a randomized clinical trial in He Zuo township, Qidong, People’s Republic of China. Cancer Epidemiol Biomarkers Prev. 2005;14:2605–13.

    Article  PubMed  CAS  Google Scholar 

  53. Rychlik M, Adam ST. Glucosinolate and folate content in sprouted broccoli seeds. Eur Food Res Technol. 2008;226:1057–64.

    Article  CAS  Google Scholar 

  54. Galan MV, Kishan AA, Silverman AL. Oral broccoli sprouts for the treatment of Helicobacter pylori infection: a preliminary report. Dig Dis Sci. 2004;49:1088–90.

    Article  PubMed  Google Scholar 

  55. Yanaka A, Fahey JW, Fukumoto A, et al. Dietary sulforaphane-rich broccoli sprouts reduce colonization and attenuate gastritis in Helicobacter pylori-infected mice and humans. Cancer Prev Res (Phila Pa). 2009;2:353–60.

    Article  CAS  Google Scholar 

  56. Egner PA, Chen JG, Wang JB, et al. Bioavailability of Sulforaphane from two broccoli sprout beverages: results of a short-term, cross-over clinical trial in Qidong, China. Cancer Prev Res (Phila). 2011;4:384–95.

    Article  CAS  Google Scholar 

  57. Yuan GF, Sun B, Yuan J, et al. Effects of different cooking methods on health-promoting compounds of broccoli. J Zhejiang Univ Sci B. 2009;10:580–8.

    Article  PubMed  Google Scholar 

  58. Lopez-Berenguer C, Carvajal M, Moreno DA, et al. Effects of microwave cooking conditions on bioactive compounds present in broccoli inflorescences. J Agric Food Chem. 2007;55:10001–7.

    Article  PubMed  CAS  Google Scholar 

  59. Moreno DA, Lopez-Berenguer C, Garcia-Viguera C. Effects of stir-fry cooking with different edible oils on the phytochemical composition of broccoli. J Food Sci. 2007;72:S064–8.

    Article  PubMed  Google Scholar 

  60. Shapiro TA, Fahey JW, Dinkova-Kostova AT, et al. Safety, tolerance, and metabolism of broccoli sprout glucosinolates and isothiocyanates: a clinical phase I study. Nutr Cancer. 2006;55:53–62.

    Article  PubMed  CAS  Google Scholar 

  61. Shapiro TA, Fahey JW, Wade KL, et al. Chemoprotective glucosinolates and isothiocyanates of broccoli sprouts: metabolism and excretion in humans. Cancer Epidemiol Biomarkers Prev. 2001;10:501–8.

    PubMed  CAS  Google Scholar 

  62. Shapiro TA, Fahey JW, Wade KL, et al. Human metabolism and excretion of cancer chemoprotective glucosinolates and isothiocyanates of cruciferous vegetables. Cancer Epidemiol Biomarkers Prev. 1998;7:1091–100.

    PubMed  CAS  Google Scholar 

  63. Lawenda BD, Kelly KM, Ladas EJ, et al. Should supplemental antioxidant administration be avoided during chemotherapy and radiation therapy? J Natl Cancer Inst. 2008;100:773–83.

    Article  PubMed  CAS  Google Scholar 

  64. D’Andrea GM. Use of antioxidants during chemotherapy and radiotherapy should be avoided. CA Cancer J Clin. 2005;55:319–21.

    Article  PubMed  Google Scholar 

  65. Zhou W, Kallifatidis G, Baumann B, et al. Dietary polyphenol quercetin targets pancreatic cancer stem cells. Int J Oncol. 2010;37:551–61.

    PubMed  CAS  Google Scholar 

  66. Verhoeven DT, Verhagen H, Goldbohm RA, et al. A review of mechanisms underlying anticarcinogenicity by brassica vegetables. Chem Biol Interact. 1997;103:79–129.

    Article  PubMed  CAS  Google Scholar 

  67. Adikrisna R, Tanaka S, Muramatsu S, et al. Identification of pancreatic cancer stem cells and selective toxicity of chemotherapeutic agents. Gastroenterology. 2012;143:234–45.e7.

    Article  PubMed  CAS  Google Scholar 

  68. Rosen CJ. Clinical practice. Vitamin D insufficiency. N Engl J Med. 2011;364:248–54.

    Article  PubMed  CAS  Google Scholar 

  69. Wolpin BM, Ng K, Bao Y, et al. Plasma 25-hydroxyvitamin D and risk of pancreatic cancer. Cancer Epidemiol Biomarkers Prev. 2012;21:82–91.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This manuscript was supported by grants from the German Cancer Aid (Deutsche Krebshilfe 109362), German Research Community (DFG HE 3186/11-1) and German-Israeli Foundation for Scientific Research and Development (GIF 1058-7.11/2008).

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Authors and Affiliations

  1. Molecular OncoSurgery Group, Im Neuenheimer Feld 365, 69120, Heidelberg, Germany

    Ingrid Herr PhD

  2. Department of General Surgery, University of Heidelberg and German Cancer Research Center-G403, Heidelberg, Germany

    Vladimir Lozanovski, Philipp Houben, Peter Schemmer & Markus W. Büchler

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  1. Ingrid Herr PhD
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Herr, I., Lozanovski, V., Houben, P. et al. Sulforaphane and related mustard oils in focus of cancer prevention and therapy. Wien Med Wochenschr 163, 80–88 (2013). https://doi.org/10.1007/s10354-012-0163-3

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