Maslinic Acid-Enriched Diet Decreases Intestinal Tumorigenesis in ApcMin/+ Mice through Transcriptomic and Metabolomic Reprogramming

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Sánchez Tena, Susana ^a   Reyes Zurita, Fernando J ^b   Díaz Moralli, Santiago ^a   Vinardell, Maria Pilar ^a   Reed, Michelle ^c   García García, Francisco ^d,e   Dopazo, Joaquín ^d,e   Lupiáñez, José A ^b   Günther, Ulrich ^c   Cascante, Marta ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b UNIVERSITY OF GRANADA   (Spain)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^d CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

^e CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE ENFERMEDADES RARAS CIBERER   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

APC PROTEIN; MASLINIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER PREVENTION; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL SURVIVAL; COLON CANCER; CONTROLLED STUDY; DIET SUPPLEMENTATION; ENERGY METABOLISM; GENE EXPRESSION PROFILING; GENETIC PREDISPOSITION; INFLAMMATION; INTESTINE POLYP; INTESTINE TUMOR; METABOLOMICS; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTOMICS;

ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; DIETARY SUPPLEMENTS; GENE EXPRESSION PROFILING; GENES, APC; INTESTINAL POLYPS; MALE; MICE; MICE, INBRED STRAINS; MICROARRAY ANALYSIS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRITERPENES;

EID: 84875063952     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0059392     Document Type: Article

References (53)

1. Su LK, Kinzler KW, Vogelstein B, Preisinger AC, Moser AR, et al. (1992) Multiple intestinal neoplasia caused by a mutation in the murine homolog of the APC gene. Science 256: 668-670.
2. Xu HX, Zeng FQ, Wan M, Sim KY, (1996) Anti-HIV triterpene acids from Geum japonicum. Journal of natural products 59: 643-645.
3. Fernandez-Navarro M, Peragon J, Amores V, De La Higuera M, Lupianez JA, (2008) Maslinic acid added to the diet increases growth and protein-turnover rates in the white muscle of rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol C Toxicol Pharmacol 147: 158-167.
4. Parra A, Rivas F, Martin-Fonseca S, Garcia-Granados A, Martinez A, (2011) Maslinic acid derivatives induce significant apoptosis in b16f10 murine melanoma cells. European journal of medicinal chemistry 46: 5991-6001.
5. Lin CC, Huang CY, Mong MC, Chan CY, Yin MC, (2011) Antiangiogenic potential of three triterpenic acids in human liver cancer cells. Journal of agricultural and food chemistry 59: 755-762.
6. Martin R, Carvalho-Tavares J, Ibeas E, Hernandez M, Ruiz-Gutierrez V, et al. (2007) Acidic triterpenes compromise growth and survival of astrocytoma cell lines by regulating reactive oxygen species accumulation. Cancer research 67: 3741-3751.
7. Reyes FJ, Centelles JJ, Lupianez JA, Cascante M, (2006) (2Alpha,3beta)-2,3-dihydroxyolean-12-en-28-oic acid, a new natural triterpene from Olea europea, induces caspase dependent apoptosis selectively in colon adenocarcinoma cells. FEBS letters 580: 6302-6310.
8. Garcia-Granados A, Lopez PE, Melguizo E, Moliz JN, Parra A, et al. (2003) Epoxides, cyclic sulfites, and sulfate from natural pentacyclic triterpenoids: theoretical calculations and chemical transformations. The Journal of organic chemistry 68: 4833-4844.
9. Bolstad BM, Irizarry RA, Astrand M, Speed TP, (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19: 185-193.
10. Smyth GK, (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Statistical applications in genetics and molecular biology 3: Article3.
11. Benjamini Y, Drai D, Elmer G, Kafkafi N, Golani I, (2001) Controlling the false discovery rate in behavior genetics research. Behavioural brain research 125: 279-284.
12. Gunther RW, Neuerburg J, Mossdorf A, Pfeffer J, Hoj AR, et al. (2005) New optional IVC filter for percutaneous retrieval-in vitro evaluation of embolus capturing efficiency. Rofo 177: 632-636.
13. Gunther UL, Ludwig C, Ruterjans H, (2000) NMRLAB-Advanced NMR data processing in matlab. J Magn Reson 145: 201-208.
14. Liu J, Sun H, Duan W, Mu D, Zhang L, (2007) Maslinic acid reduces blood glucose in KK-Ay mice. Biological & pharmaceutical bulletin 30: 2075-2078.
15. Corpet DE, Pierre F, (2003) Point: From animal models to prevention of colon cancer. Systematic review of chemoprevention in min mice and choice of the model system. Cancer Epidemiol Biomarkers Prev 12: 391-400.
16. Iwuchukwu OF, Nagar S, (2008) Resveratrol (trans-resveratrol, 3,5,4′-trihydroxy-trans-stilbene) glucuronidation exhibits atypical enzyme kinetics in various protein sources. Drug metabolism and disposition: the biological fate of chemicals 36: 322-330.
17. Tessitore L, Davit A, Sarotto I, Caderni G, (2000) Resveratrol depresses the growth of colorectal aberrant crypt foci by affecting bax and p21(CIP) expression. Carcinogenesis 21: 1619-1622.
18. Phelps RA, Chidester S, Dehghanizadeh S, Phelps J, Sandoval IT, et al. (2009) A two-step model for colon adenoma initiation and progression caused by APC loss. Cell 137: 623-634.
19. Ban JO, Kwak DH, Oh JH, Park EJ, Cho MC, et al. (2010) Suppression of NF-kappaB and GSK-3beta is involved in colon cancer cell growth inhibition by the PPAR agonist troglitazone. Chemico-biological interactions 188: 75-85.
20. Min HJ, Koh SS, Cho IR, Srisuttee R, Park EH, et al. (2009) Inhibition of GSK-3beta enhances reovirus-induced apoptosis in colon cancer cells. International journal of oncology 35: 617-624.
21. Colakoglu T, Yildirim S, Kayaselcuk F, Nursal TZ, Ezer A, et al. (2008) Clinicopathological significance of PTEN loss and the phosphoinositide 3-kinase/Akt pathway in sporadic colorectal neoplasms: is PTEN loss predictor of local recurrence? American journal of surgery 195: 719-725.
22. Qiu W, Carson-Walter EB, Kuan SF, Zhang L, Yu J, (2009) PUMA suppresses intestinal tumorigenesis in mice. Cancer research 69: 4999-5006.
23. Shiou SR, Datta PK, Dhawan P, Law BK, Yingling JM, et al. (2006) Smad4-dependent regulation of urokinase plasminogen activator secretion and RNA stability associated with invasiveness by autocrine and paracrine transforming growth factor-beta. The Journal of biological chemistry 281: 33971-33981.
24. Castets M, Broutier L, Molin Y, Brevet M, Chazot G, et al. (2011) DCC constrains tumour progression via its dependence receptor activity. Nature 482: 534-537.
25. Liu J, Yao F, Wu R, Morgan M, Thorburn A, et al. (2002) Mediation of the DCC apoptotic signal by DIP13 alpha. The Journal of biological chemistry 277: 26281-26285.
26. Reyes-Zurita FJ, Pachon-Pena G, Lizarraga D, Rufino-Palomares EE, Cascante M, et al. (2011) The natural triterpene maslinic acid induces apoptosis in HT29 colon cancer cells by a JNK-p53-dependent mechanism. BMC cancer 11: 154.
27. Koizumi F, Shimoyama T, Taguchi F, Saijo N, Nishio K, (2005) Establishment of a human non-small cell lung cancer cell line resistant to gefitinib. International journal of cancer 116: 36-44.
28. Tan Y, Ruan H, Demeter MR, Comb MJ, (1999) p90(RSK) blocks bad-mediated cell death via a protein kinase C-dependent pathway. The Journal of biological chemistry 274: 34859-34867.
29. Wu KK, Liou JY, (2009) Cyclooxygenase inhibitors induce colon cancer cell apoptosis Via PPARdelta ->14-3-3epsilon pathway. Methods in molecular biology 512: 295-307.
30. Franklin RA, McCubrey JA, (2000) Kinases: positive and negative regulators of apoptosis. Leukemia 14: 2019-2034.
31. Brudvik KW, Paulsen JE, Aandahl EM, Roald B, Tasken K, (2011) Protein kinase A antagonist inhibits beta-catenin nuclear translocation, c-Myc and COX-2 expression and tumor promotion in ApcMin/+ mice. Molecular cancer 10: 149.
32. Ballabeni A, Park IH, Zhao R, Wang W, Lerou PH, et al. (2011) Cell cycle adaptations of embryonic stem cells. Proceedings of the National Academy of Sciences of the United States of America 108: 19252-19257.
33. Li C, Yang Z, Zhai C, Qiu W, Li D, et al. (2010) Maslinic acid potentiates the anti-tumor activity of tumor necrosis factor alpha by inhibiting NF-kappaB signaling pathway. Molecular cancer 9: 73.
34. Roberti A, Rizzolio F, Lucchetti C, de Leval L, Giordano A, (2011) Ubiquitin-mediated protein degradation and methylation-induced gene silencing cooperate in the inactivation of the INK4/ARF locus in Burkitt lymphoma cell lines. Cell cycle 10: 127-134.
35. Dehan E, Bassermann F, Guardavaccaro D, Vasiliver-Shamis G, Cohen M, et al. (2009) betaTrCP- and Rsk1/2-mediated degradation of BimEL inhibits apoptosis. Molecular cell 33: 109-116.
36. Ougolkov A, Zhang B, Yamashita K, Bilim V, Mai M, et al. (2004) Associations among beta-TrCP, an E3 ubiquitin ligase receptor, beta-catenin, and NF-kappaB in colorectal cancer. Journal of the National Cancer Institute 96: 1161-1170.
37. Hsum YW, Yew WT, Hong PL, Soo KK, Hoon LS, et al. (2011) Cancer Chemopreventive Activity of Maslinic Acid: Suppression of COX-2 Expression and Inhibition of NF-kappaB and AP-1 Activation in Raji Cells. Planta medica 77: 152-157.
38. Eichhorn PJ, Creyghton MP, Bernards R, (2009) Protein phosphatase 2A regulatory subunits and cancer. Biochimica et biophysica acta 1795: 1-15.
39. Zhang W, Yang J, Liu Y, Chen X, Yu T, et al. (2009) PR55 alpha, a regulatory subunit of PP2A, specifically regulates PP2A-mediated beta-catenin dephosphorylation. The Journal of biological chemistry 284: 22649-22656.
40. Honda K, Yamada T, Hayashida Y, Idogawa M, Sato S, et al. (2005) Actinin-4 increases cell motility and promotes lymph node metastasis of colorectal cancer. Gastroenterology 128: 51-62.
41. Rosano L, Spinella F, Di Castro V, Dedhar S, Nicotra MR, et al. (2006) Integrin-linked kinase functions as a downstream mediator of endothelin-1 to promote invasive behavior in ovarian carcinoma. Molecular cancer therapeutics 5: 833-842.
42. Park YS, Huh JW, Lee JH, Kim HR, (2012) shRNA against CD44 inhibits cell proliferation, invasion and migration. Oncology reports 27: 339-346.
43. Abuzeid WM, Jiang X, Shi G, Wang H, Paulson D, et al. (2009) Molecular disruption of RAD50 sensitizes human tumor cells to cisplatin-based chemotherapy. The Journal of clinical investigation 119: 1974-1985.
44. Zamarron BF, Chen W, (2011) Dual roles of immune cells and their factors in cancer development and progression. International journal of biological sciences 7: 651-658.
45. McClellan JL, Davis JM, Steiner JL, Day SD, Steck SE, et al. (2012) Intestinal inflammatory cytokine response in relation to tumorigenesis in the Apc(Min/+) mouse. Cytokine 57: 113-119.
46. Huang L, Guan T, Qian Y, Huang M, Tang X, et al. (2011) Anti-inflammatory effects of maslinic acid, a natural triterpene, in cultured cortical astrocytes via suppression of nuclear factor-kappa B. European journal of pharmacology. 672: 169-174.
47. Furci L, Tolazzi M, Sironi F, Vassena L, Lusso P, (2012) Inhibition of HIV-1 Infection by Human alpha-Defensin-5, a Natural Antimicrobial Peptide Expressed in the Genital and Intestinal Mucosae. PloS one 7: e45208.
48. Parra A, Rivas F, Lopez PE, Garcia-Granados A, Martinez A, et al. (2009) Solution- and solid-phase synthesis and anti-HIV activity of maslinic acid derivatives containing amino acids and peptides. Bioorganic & medicinal chemistry 17: 1139-1145.
49. Zhang M, Kimura A, Saltiel AR, (2003) Cloning and characterization of Cbl-associated protein splicing isoforms. Molecular medicine 9: 18-25.
50. Guan T, Qian Y, Tang X, Huang M, Huang L, et al. (2011) Maslinic acid, a natural inhibitor of glycogen phosphorylase, reduces cerebral ischemic injury in hyperglycemic rats by GLT-1 up-regulation. Journal of neuroscience research 89: 1829-1839.
51. Hussain Shaik A, Rasool SN, Abdul Kareem M, Krushna GS, Akhtar PM, et al. (2012) Maslinic acid protects against isoproterenol-induced cardiotoxicity in albino Wistar rats. Journal of medicinal food 15: 741-746.
52. Mutoh M, Teraoka N, Takasu S, Takahashi M, Onuma K, et al. (2011) Loss of adiponectin promotes intestinal carcinogenesis in Min and wild-type mice. Gastroenterology 140: 2000-2008, 2008 e2001-2002.
53. Erbach M, Mehnert H, Schnell O, (2012) Diabetes and the risk for colorectal cancer. Journal of diabetes and its complications 26: 50-55.