High Levels of Prebiotic Resistant Starch in Diet Modulate a Specific Pattern of miRNAs Expression Profile Associated to a Better Overall Survival in Pancreatic Cancer
Abstract
:1. Introduction
2. Materials and Methods
2.1. Animal Study
2.2. RNA Extraction
2.3. MicroRNAs and mRNA Analysis
2.4. Prediction of miRNAs Targets and Functional Enrichment Analysis
2.5. Immunoblotting
2.6. Survival and Statistical Analyses
3. Results
3.1. Differential miRNAs and miRNAs Target Genes’ Expression in PC Xenograft Mice under RS Diet
3.2. Biological Function and Pathway Enrichment Analysis of miRNA-Target Genes
3.3. ERSD Influence on PI3K/AKT Signaling
3.4. Expression of Four miRNAs in ERSD Predicts Survival of Pancreatic Cancer Patients
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Vincent, A.; Herman, J.; Schulick, R.; Hruban, R.H.; Goggins, M. Pancreatic cancer. Lancet 2011, 378, 607–620. [Google Scholar] [CrossRef]
- Yachida, S.; Jones, S.; Bozic, I.; Antal, T.; Leary, R.; Fu, B.; Kamiyama, M.; Hruban, R.H.; Eshleman, J.R.; Nowak, M.A.; et al. Distant metastasis occurs late during the genetic evolution of pancreatic cancer. Nature 2010, 467, 1114–1117. [Google Scholar] [CrossRef] [Green Version]
- Wiseman, M. Nutrition and cancer: Prevention and survival. Br. J. Nutr. 2018, 122, 481–487. [Google Scholar] [CrossRef] [Green Version]
- Gianotti, L.; Besselink, M.G.; Sandini, M.; Hackert, T.; Conlon, K.; Gerritsen, A.; Griffin, O.; Fingerhut, A.; Probst, P.; Abu Hilal, M.; et al. Nutritional support and therapy in pancreatic surgery: A position paper of the International Study Group on Pancreatic Surgery (ISGPS). Surgery 2018, 164, 1035–1048. [Google Scholar] [CrossRef]
- Tajan, M.; Vousden, K.H. Dietary Approaches to Cancer Therapy. Cancer Cell 2020, 37, 767–785. [Google Scholar] [CrossRef]
- Arends, J.; Bachmann, P.; Baracos, V.; Barthelemy, N.; Bertz, H.; Bozzetti, F.; Fearon, K.; Hutterer, E.; Isenring, E.; Kaasa, S.; et al. ESPEN guidelines on nutrition in cancer patients. Clin. Nutr. 2017, 36, 11–48. [Google Scholar] [CrossRef] [Green Version]
- Lévesque, S.; Pol, J.G.; Ferrere, G.; Galluzzi, L.; Zitvogel, L.; Kroemer, G. Trial watch: Dietary interventions for cancer therapy. OncoImmunology 2019, 8, e1591878. [Google Scholar] [CrossRef]
- Panebianco, C.; Potenza, A.; Pazienza, V. Fasting and engineered diets as powerful tool in the medical practice: An old approach in the new era. Ann. Transl. Med. 2017, 5, 429. [Google Scholar] [CrossRef]
- Cairns, R.A.; Harris, I.S.; Mak, T.W. Regulation of cancer cell metabolism. Nat. Rev. Cancer 2011, 11, 85–95. [Google Scholar] [CrossRef] [Green Version]
- Birt, D.F.; Boylston, T.; Hendrich, S.; Jane, J.-L.; Hollis, J.; Li, L.; McClelland, J.; Moore, S.; Phillips, G.J.; Rowling, M.; et al. Resistant Starch: Promise for Improving Human Health. Adv. Nutr. 2013, 4, 587–601. [Google Scholar] [CrossRef] [Green Version]
- Nugent, A.P. Health properties of resistant starch. Nutr. Bull. 2005, 30, 27–54. [Google Scholar] [CrossRef]
- Hu, Y.; Le Leu, R.K.; Christophersen, C.T.; Somashekar, R.; Conlon, M.A.; Meng, X.Q.; Winter, J.M.; Woodman, R.J.; McKinnon, R.; Young, G.P. Manipulation of the gut microbiota using resistant starch is associated with protection against colitis-associated colorectal cancer in rats. Carcinogenesis 2016, 37, 366–375. [Google Scholar] [CrossRef] [PubMed]
- Hijova, E.; Szabadosova, V.; Strojny, L.; Bomba, A. Changes chemopreventive markers in colorectal cancer development after inulin supplementation. Bratisl. Lek. List. 2014, 115, 76–79. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Toden, S.; Lockett, T.J.; Topping, D.L.; Scherer, B.L.; Watson, E.-J.L.; Southwood, J.G.; Clarke, J.M. Butyrylated starch affects colorectal cancer markers beneficially and dose-dependently in genotoxin-treated rats. Cancer Biol. Ther. 2014, 15, 1515–1523. [Google Scholar] [CrossRef] [Green Version]
- Malcomson, F.C.; Willis, N.D.; Mathers, J.C. Is resistant starch protective against colorectal cancer via modulation of the WNT signalling pathway? Proc. Nutr. Soc. 2015, 74, 282–291. [Google Scholar] [CrossRef] [Green Version]
- Van Munster, I.P.; Tangerman, A.; Nagengast, F.M. Effect of resistant starch on colonic fermentation, bile acid metabolism, and mucosal proliferation. Dig. Dis. Sci. 1994, 39, 834–842. [Google Scholar] [CrossRef]
- Le Leu, R.K.; Winter, J.M.; Christophersen, C.T.; Young, G.P.; Humphreys, K.J.; Hu, Y.; Gratz, S.W.; Miller, R.B.; Topping, D.L.; Bird, A.R.; et al. Butyrylated starch intake can prevent red meat-induced O6-methyl-2-deoxyguanosine adducts in human rectal tissue: A randomised clinical trial. Br. J. Nutr. 2015, 114, 220–230. [Google Scholar] [CrossRef] [Green Version]
- Burn, J.; Bishop, D.T.; Chapman, P.D.; Elliott, F.; Bertario, L.; Dunlop, M.G.; Eccles, D.; Ellis, A.; Evans, D.G.; Fodde, R.; et al. International CAPP consortium: A randomized placebo-controlled prevention trial of aspirin and/or resistant starch in young people with familial adenomatous polyposis. Cancer Prev. Res. 2011, 4, 655–665. [Google Scholar] [CrossRef] [Green Version]
- Burn, J.; Bishop, D.T.; Mecklin, J.P.; Macrae, F.; Möslein, G.; Olschwang, S.; Bisgaard, M.L.; Ramesar, R.; Eccles, D.; Maher, E.R.; et al. CAPP2 Investigators: Effect of aspirin or resistant starch on colorectal neoplasia in the Lynch syndrome. N. Engl. J. Med. 2008, 359, 2567–2578. [Google Scholar] [CrossRef] [Green Version]
- Quintanilha, B.J.; Reis, B.Z.; Silva, G.B.; Cozzolino, S.M.F.; Rogero, M.M. Nutrimiromics: Role of microRNAs and Nutrition in Modulating Inflammation and Chronic Diseases. Nutrients 2017, 9, 1168. [Google Scholar] [CrossRef]
- Humphreys, K.J.; Conlon, M.A.; Young, G.P.; Topping, D.L.; Hu, Y.; Winter, J.M.; Bird, A.R.; Cobiac, L.; Kennedy, N.A.; Michael, M.Z.; et al. Dietary Manipulation of Oncogenic MicroRNA Expression in Human Rectal Mucosa: A Randomized Trial. Cancer Prev. Res. 2014, 7, 786–795. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nielsen, T.S.; Bendiks, Z.A.; Thomsen, B.; Wright, M.E.; Theil, P.K.; Scherer, B.L.; Marco, M.L. High-Amylose Maize, Potato, and Butyrylated Starch Modulate Large Intestinal Fermentation, Microbial Composition, and Oncogenic miRNA Expression in Rats Fed A High-Protein Meat Diet. Int. J. Mol. Sci. 2019, 20, 2137. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Panebianco, C.; Adamberg, K.; Adamberg, S.; Saracino, C.; Jaagura, M.; Kolk, K.; Di Chio, A.G.; Graziano, P.; Vilu, R.; Pazienza, V. Engineered Resistant-Starch (ERS) Diet Shapes Colon Microbiota Profile in Parallel with the Retardation of Tumor Growth in In Vitro and In Vivo Pancreatic Cancer Models. Nutrients 2017, 9, 331. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Panebianco, C.; Villani, A.; Pazienza, V. High Levels of Prebiotic Resistant Starch in Diet Modulate Gene Expression and Metabolomic Profile in Pancreatic Cancer Xenograft Mice. Nutrients 2019, 11, 709. [Google Scholar] [CrossRef] [Green Version]
- Badea, L.; Herlea, V.; Dima, S.O.; Dumitrascu, T.; Popescu, I. Combined gene expression analysis of whole-tissue and microdissected pancreatic ductal adenocarcinoma identifies genes specifically overexpressed in tumor epithelia. Hepatogastroenterology 2008, 55, 2016–2027. [Google Scholar]
- Panebianco, C.; Adamberg, K.; Jaagura, M.; Copetti, M.; Fontana, A.; Adamberg, S.; Kolk, K.; Vilu, R.; Andriulli, A.; Pazienza, V. Influence of gemcitabine chemotherapy on the microbiota of pancreatic cancer xenografted mice. Cancer Chemother. Pharmacol. 2018, 81, 773–782. [Google Scholar] [CrossRef]
- Hu, J.; Li, L.; Chen, H.; Zhang, G.; Liu, H.; Kong, R.; Chen, H.; Wang, Y.; Li, Y.; Tian, F.; et al. MiR-361-3p regulates ERK1/2-induced EMT via DUSP2 mRNA degradation in pancreatic ductal adenocarcinoma. Cell Death Dis. 2018, 9, 807. [Google Scholar] [CrossRef] [Green Version]
- Liu, H.; Xu, X.-F.; Zhao, Y.; Tang, M.-C.; Zhou, Y.-Q.; Lu, J.; Gao, F.-H. MicroRNA-191 promotes pancreatic cancer progression by targeting USP10. Tumor Biol. 2014, 35, 12157–12163. [Google Scholar] [CrossRef]
- Lu, Y.; Wu, X.; Wang, J. Correlation of miR-425-5p and IL-23 with pancreatic cancer. Oncol. Lett. 2019, 17, 4595–4599. [Google Scholar] [CrossRef]
- Mazza, T.; Gioffreda, D.; Fontana, A.; Biagini, T.; Carella, M.; Palumbo, O.; Maiello, E.; Bazzocchi, F.; Andriulli, A.; Tavano, F. Clinical Significance of Circulating miR-1273g-3p and miR-122-5p in Pancreatic Cancer. Front. Oncol. 2020, 10, 44. [Google Scholar] [CrossRef] [Green Version]
- Calatayud, D.; Dehlendorff, C.; Boisen, M.K.; Hasselby, J.P.; Schultz, N.A.; Werner, J.; Immervoll, H.; Molven, A.; Hansen, C.P.; Johansen, J.S. Tissue MicroRNA profiles as diagnostic and prognostic biomarkers in patients with resectable pancreatic ductal adenocarcinoma and periampullary cancers. Biomark. Res. 2017, 5, 8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gui, Z.; Luo, F.; Yang, Y.; Shen, C.; Li, S.; Xu, J. Oridonin inhibition and miR-200b-3p/ZEB1 axis in human pancreatic cancer. Int. J. Oncol. 2017, 50, 111–120. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Idichi, T.; Seki, N.; Kurahara, H.; Fukuhisa, H.; Toda, H.; Shimonosono, M.; Okato, A.; Arai, T.; Kita, Y.; Mataki, Y.; et al. Molecular pathogenesis of pancreatic ductal adenocarcinoma: Impact of passenger strand of pre-miR-148a on gene regulation. Cancer Sci. 2018, 109, 2013–2026. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Karihtala, P.; Porvari, K.; Soini, Y.; Eskelinen, M.; Juvonen, P.; Haapasaari, K.-M. Expression Levels of microRNAs miR-93 and miR-200a in Pancreatic Adenocarcinoma with Special Reference to Differentiation and Relapse-Free Survival. Oncology 2018, 96, 164–170. [Google Scholar] [CrossRef] [PubMed]
- Ma, M.-Z.; Kong, X.; Weng, M.; Cheng, K.; Gong, W.; Quan, Z.-W.; Peng, C.-H. Candidate microRNA biomarkers of pancreatic ductal adenocarcinoma: Meta-analysis, experimental validation and clinical significance. J. Exp. Clin. Cancer Res. 2013, 32, 71. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pan, L.; Zhou, L.; Yin, W.; Bai, J.; Liu, R. miR-125a induces apoptosis, metabolism disorder and migrationimpairment in pancreatic cancer cells by targeting Mfn2-related mitochondrial fission. Int. J. Oncol. 2018, 53, 124–136. [Google Scholar] [CrossRef]
- Shi, S.; Lu, Y.; Qin, Y.; Li, W.; Cheng, H.; Xu, Y.; Xu, J.; Long, J.; Liu, L.; Liu, C.; et al. miR-1247 is correlated with prognosis of pancreatic cancer and inhibits cell proliferation by targeting neuropilins. Curr. Mol. Med. 2014, 14, 316–327. [Google Scholar] [CrossRef]
- Zhou, J.; Song, S.; Cen, J.; Zhu, D.; Li, D.; Zhang, Z. MicroRNA-375 Is Downregulated in Pancreatic Cancer and Inhibits Cell Proliferation In Vitro. Oncol. Res. Featur. Preclin. Clin. Cancer Ther. 2012, 20, 197–203. [Google Scholar] [CrossRef]
- Edgar, R.; Domrachev, M.; Lash, A.E. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002, 30, 207–210. [Google Scholar] [CrossRef] [Green Version]
- Liu, B.; Yang, H.; Taher, L.; Denz, A.; Grützmann, R.; Pilarsky, C.; Weber, G.F. Identification of Prognostic Biomarkers by Combined mRNA and miRNA Expression Microarray Analysis in Pancreatic Cancer. Transl. Oncol. 2018, 11, 700–714. [Google Scholar] [CrossRef]
- Parsons, C.M.; Muilenburg, D.; Bowles, T.L.; Virudachalam, S.; Bold, R.J. The role of Akt activation in the response to chemotherapy in pancreatic cancer. Anticancer Res. 2010, 30, 3279–3289. [Google Scholar]
- Klement, R.J.; Pazienza, V. Impact of Different Types of Diet on Gut Microbiota Profiles and Cancer Prevention and Treatment. Medicina 2019, 55, 84. [Google Scholar] [CrossRef] [Green Version]
- Quagliani, D.; Felt-Gunderson, P. Closing America’s Fiber Intake Gap: Communication Strategies from a Food and Fiber Summit. Am. J. Lifestyle Med. 2016, 11, 80–85. [Google Scholar] [CrossRef]
- Kohler, L.N.; Garcia, D.O.; Harris, R.B.; Oren, E.; Roe, D.J.; Jacobs, E.T. Adherence to Diet and Physical Activity Cancer Prevention Guidelines and Cancer Outcomes: A Systematic Review. Cancer Epidemiol. Biomark. Prev. 2016, 25, 1018–1028. [Google Scholar] [CrossRef] [Green Version]
- Lin, S.; Wang, X.; Huang, C.; Liu, X.; Zhao, J.; Yu, I.T.; Christiani, D.C. Consumption of salted meat and its interactions with alcohol drinking and tobacco smoking on esophageal squamous-cell carcinoma. Int. J. Cancer 2015, 137, 582–589. [Google Scholar] [CrossRef]
- Haub, M.D.; Hubach, K.L.; Al-Tamimi, E.K.; Ornelas, S.; Seib, P.A. Different Types of Resistant Starch Elicit Different Glucose Reponses in Humans. J. Nutr. Metab. 2010, 2010, 1–4. [Google Scholar] [CrossRef] [Green Version]
- Robertson, M.D. Dietary-resistant starch and glucose metabolism. Curr. Opin. Clin. Nutr. Metab. Care 2012, 15, 362–367. [Google Scholar] [CrossRef]
- Zhang, Z.; Pan, B.; Lv, S.; Ji, Z.; Wu, Q.; Lang, R.; He, Q.; Zhao, X. Integrating MicroRNA Expression Profiling Studies to Systematically Evaluate the Diagnostic Value of MicroRNAs in Pancreatic Cancer and Validate Their Prognostic Significance with the Cancer Genome Atlas Data. Cell. Physiol. Biochem. 2018, 49, 678–695. [Google Scholar] [CrossRef]
- Liang, L.; Wei, D.; Li, J.; Luo, D.; Chen, G.; Dang, Y.; Cai, X. Prognostic microRNAs and their potential molecular mechanism in pancreatic cancer: A study based on The Cancer Genome Atlas and bioinformatics investigation. Mol. Med. Rep. 2018, 17, 939–951. [Google Scholar] [CrossRef] [Green Version]
- Wu, X.; Wu, G.; Wu, Z.; Yao, X.; Li, G. MiR-200a Suppresses the Proliferation and Metastasis in Pancreatic Ductal Adenocarcinoma through Downregulation of DEK Gene. Transl. Oncol. 2016, 9, 25–31. [Google Scholar] [CrossRef] [Green Version]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Trivieri, N.; Panebianco, C.; Villani, A.; Pracella, R.; Latiano, T.P.; Perri, F.; Binda, E.; Pazienza, V. High Levels of Prebiotic Resistant Starch in Diet Modulate a Specific Pattern of miRNAs Expression Profile Associated to a Better Overall Survival in Pancreatic Cancer. Biomolecules 2021, 11, 26. https://doi.org/10.3390/biom11010026
Trivieri N, Panebianco C, Villani A, Pracella R, Latiano TP, Perri F, Binda E, Pazienza V. High Levels of Prebiotic Resistant Starch in Diet Modulate a Specific Pattern of miRNAs Expression Profile Associated to a Better Overall Survival in Pancreatic Cancer. Biomolecules. 2021; 11(1):26. https://doi.org/10.3390/biom11010026
Chicago/Turabian StyleTrivieri, Nadia, Concetta Panebianco, Annacandida Villani, Riccardo Pracella, Tiziana Pia Latiano, Francesco Perri, Elena Binda, and Valerio Pazienza. 2021. "High Levels of Prebiotic Resistant Starch in Diet Modulate a Specific Pattern of miRNAs Expression Profile Associated to a Better Overall Survival in Pancreatic Cancer" Biomolecules 11, no. 1: 26. https://doi.org/10.3390/biom11010026
APA StyleTrivieri, N., Panebianco, C., Villani, A., Pracella, R., Latiano, T. P., Perri, F., Binda, E., & Pazienza, V. (2021). High Levels of Prebiotic Resistant Starch in Diet Modulate a Specific Pattern of miRNAs Expression Profile Associated to a Better Overall Survival in Pancreatic Cancer. Biomolecules, 11(1), 26. https://doi.org/10.3390/biom11010026