Phosphatidylinositol 3-Kinase Mediates the Ability of Retinol to Decrease Colorectal Cancer Cell Invasion

REFERENCES

• Freemantle SJ, Spinella MJ, and Dmitrovsky E: Retinoids in cancer therapy and chemoprevention: promise meets resistance. Oncogene, 22, 7305–7315, 2003.
   PubMed Web of Science ®Google Scholar
• Vogel S, Gamble MV, and Blaner WS: Biosynthesis, absorption, metabolism and transport of retinoids. In: Retinoids: the biochemical and molecular basis of vitamin A and retinoid action, H. Nau, and W. S. Blaner (eds.). Berlin, Springer-Verlag, 1999, pp. 31–95.
   Google Scholar
• Park EY, Pinali D, Lindley K, and Lane MA: Hepatic vitamin A preloading reduces colorectal cancer metastatic multiplicity in a mouse xenograft model. Nutr Cancer 64, 732–740, 2012.
   PubMed Web of Science ®Google Scholar
• Garcia AL, Ruhl R, and Schweigert FJ: Retinoid concentrations in the mouse during postnatal development and after maternal vitamin A supplementation. Ann Nutr Metab 49, 333–341, 2005.
   PubMed Web of Science ®Google Scholar
• Liu L, Tang XH, and Gudas LJ: Homeostasis of retinol in lecithin: retinol acyltransferase gene knockout mice fed a high retinol diet. Biochem Pharmacol 75, 2316–2324, 2008.
   PubMed Web of Science ®Google Scholar
• Park EY, Wilder ET, and Lane MA: Retinol inhibits the invasion of retinoic acid-resistant colon cancer cells in vitro and decreases matrix metalloproteinase mRNA, protein, and activity levels. Nutr Cancer 57, 66–77, 2007.
   PubMed Web of Science ®Google Scholar
• Qiu Q, Yang M, Tsang BK, and Gruslin A: EGF-induced trophoblast secretion of MMP-9 and TIMP-1 involves activation of both PI3K and MAPK signalling pathways. Reproduction 128, 355–363, 2004.
   PubMed Web of Science ®Google Scholar
• Kadri Z, Maouche-Chretien L, Rooke HM, Orkin SH, Romeo PH, et al.: Phosphatidylinositol 3-kinase/Akt induced by erythropoietin renders the erythroid differentiation factor GATA-1 competent for TIMP-1 gene transactivation. Mol Cell Biol 25, 7412–7422, 2005.
   PubMed Web of Science ®Google Scholar
• Park EY, Wilder ET, Chipuk JE, and Lane MA: Retinol decreases phosphatidylinositol 3-kinase activity in colon cancer cells. Mol Carcinog 47, 264–274, 2008.
   PubMed Web of Science ®Google Scholar
• Stephens L, Williams R, and Hawkins P: Phosphoinositide 3-kinases as drug targets in cancer. Curr Opin Pharmacol 5, 357–365, 2005.
   PubMed Web of Science ®Google Scholar
• Chen JS, Wang Q, Fu XH, Huang XH, Chen XL, et al.: Involvement of PI3K/PTEN/AKT/mTOR pathway in invasion and metastasis in hepatocellular carcinoma: Association with MMP-9. Hepatol Res 39, 177–186, 2009.
   PubMedGoogle Scholar
• Kim D, Kim S, Koh H, Yoon SO, Chung AS, et al.: Akt/PKB promotes cancer cell invasion via increased motility and metalloproteinase production. FASEB J 15, 1953–1962, 2001.
   PubMed Web of Science ®Google Scholar
• Cheng JC, Chou CH, Kuo ML, and Hsieh CY: Radiation-enhanced hepatocellular carcinoma cell invasion with MMP-9 expression through PI3K/Akt/NF-kappaB signal transduction pathway. Oncogene 25, 7009–7018, 2006.
   PubMed Web of Science ®Google Scholar
• Bernhard EJ, Gruber SB, and Muschel RJ: Direct evidence linking expression of matrix metalloproteinase 9 (92-kDa gelatinase/collagenase) to the metastatic phenotype in transformed rat embryo cells. Proc Natl Acad Sci U S A 91, 4293–4297, 1994.
   PubMed Web of Science ®Google Scholar
• Bergers G, Brekken R, McMahon G, Vu TH, Itoh T, et al.: Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol 2, 737–744, 2000.
   PubMed Web of Science ®Google Scholar
• McCawley LJ and Matrisian LM: Matrix metalloproteinases: they’re not just for matrix anymore! Curr Opin Cell Biol 13, 534–540, 2001.
   PubMed Web of Science ®Google Scholar
• Huang S, Van Arsdall M, Tedjarati S, McCarty M, Wu W, et al.: Contributions of stromal metalloproteinase-9 to angiogenesis and growth of human ovarian carcinoma in mice. J Natl Cancer Inst 94, 1134–1142, 2002.
   PubMed Web of Science ®Google Scholar
• Legrand C, Gilles C, Zahm JM, Polette M, Buisson AC, et al.: Airway epithelial cell migration dynamics. MMP-9 role in cell-extracellular matrix remodeling. J Cell Biol 146, 517–529, 1999.
   PubMed Web of Science ®Google Scholar
• Heslin MJ, Yan J, Johnson MR, Weiss H, Diasio RB, et al.: Role of matrix metalloproteinases in colorectal carcinogenesis. Ann Surg 233, 786–792, 2001.
   PubMed Web of Science ®Google Scholar
• Zeng ZS and Guillem JG: Colocalisation of matrix metalloproteinase-9-mRNA and protein in human colorectal cancer stromal cells. Br J Cancer 74, 1161–1167, 1996.
   PubMed Web of Science ®Google Scholar
• Roeb E, Dietrich CG, Winograd R, Arndt M, Breuer B, et al.: Activity and cellular origin of gelatinases in patients with colon and rectal carcinoma differential activity of matrix metalloproteinase-9. Cancer 92, 2680–2691, 2001.
   PubMed Web of Science ®Google Scholar
• Herszenyi L, Sipos F, Galamb O, Solymosi N, Hritz I, et al.: Matrix metalloproteinase-9 expression in the normal mucosa-adenoma-dysplasia-adenocarcinoma sequence of the colon. Pathol Oncol Res 14, 31–37, 2008.
   PubMed Web of Science ®Google Scholar
• Dutta A, Sen T, and Chatterjee A: All-trans retinoic acid (ATRA) downregulates MMP-9 by modulating its regulatory molecules. Cell Adh Migr 4, 409–418, 2010.
   PubMed Web of Science ®Google Scholar
• Lateef H, Stevens MJ, and Varani J: All-trans-retinoic acid suppresses matrix metalloproteinase activity and increases collagen synthesis in diabetic human skin in organ culture. Am J Pathol 165, 167–174, 2004.
   PubMed Web of Science ®Google Scholar
• Liu H, Zang C, Fenner MH, Possinger K, and Elstner E: PPARgamma ligands and ATRA inhibit the invasion of human breast cancer cells in vitro. Breast Cancer Res Treatment 79, 63–74, 2003.
   PubMed Web of Science ®Google Scholar
• Hornebeck W, Lambert E, Petitfrère E, and Bernard P: Beneficial and detrimental influences of tissue inhibitor of metalloproteinase-1 (TIMP-1) in tumor progression. Biochimie. 87, 377–383, 2005.
   PubMed Web of Science ®Google Scholar
• Gomez DE, Alonso DF, Yoshiji H, and Thorgeirsson UP: Tissue inhibitors of metalloproteinases: structure, regulation and biological functions. Eur J Cell Biol 74, 111–122, 1997.
   PubMed Web of Science ®Google Scholar
• Guruvayoorappan C and Kuttan G: 13 cis-retinoic acid regulates cytokine production and inhibits angiogenesis by disrupting endothelial cell migration and tube formation. J Exp Ther Oncol 7, 173–182, 2008.
   PubMedGoogle Scholar
• Samuels Y, Diaz LA Jr., Schmidt-Kittle, O, Cummin, JM, Delong L, et al.: Mutant PIK3CA promotes cell growth and invasion of human cancer cells. Cancer Cell 7, 561–573, 2005.
   PubMed Web of Science ®Google Scholar
• National Research Council: Nutrient Requirements of Laboratory Animals, 4th ed. Washington, DC: National Academy Press, 1995, p. 92.
   Google Scholar
• Wildi S, Kleeff J, Maruyama H, Maurer CA, Friess H, et al.: Characterization of cytokeratin 20 expression in pancreatic and colorectal cancer. Clin Cancer Res 5, 2840–2847, 1999.
   PubMed Web of Science ®Google Scholar
• West KA, Castillo SS, and Dennis PA: Activation of the PI3K/Akt pathway and chemotherapeutic resistance. Drug Resist Updat 5, 234–248, 2002.
   PubMed Web of Science ®Google Scholar
• Herrera F, Chen Q, and Schubert D: Synergistic effect of retinoic acid and cytokines on the regulation of glial fibrillary acidic protein expression. J Biol Chem 285, 38915–38922, 2010.
   Google Scholar
• Kim JS, Kim BS, Kim J, Park CS, and Chung IY: The phosphoinositide-3-kinase/Akt pathway mediates the transient increase in Nanog expression during differentiation of F9 cells. Arch Pharm Res 33, 1117–1125, 2010.
   Google Scholar
• Yan TD, Wu H, Zhang HP, Lu N, Ye P, et al.: Oncogenic potential of retinoic acid receptor-gamma in hepatocellular carcinoma. Cancer Res 70, 2285–2295, 2010.
   PubMed Web of Science ®Google Scholar
• Day RM, Lee YH, Park AM, and Suzuki YJ: Retinoic acid inhibits airway smooth muscle cell migration. Am J Respir Cell Mol Biol 34, 695–703, 2006.
   PubMed Web of Science ®Google Scholar
• del Rincon SV, Rousseau C, Samanta R, and Miller WH Jr.: Retinoic acid-induced growth arrest of MCF-7 cells involves the selective regulation of the IRS-1/PI 3-kinase/AKT pathway. Oncogene 22, 3353–3360, 2003.
   PubMed Web of Science ®Google Scholar
• Bastien, J, Plassat, JL, Payrastre, B, and Rochette-Egly, C: The phosphoinositide 3-kinase/Akt pathway is essential for the retinoic acid-induced differentiation of F9 cells. Oncogene 25, 2040–2047, 2006.
   PubMed Web of Science ®Google Scholar
• Sonneveld E, van den Brink CE, van der Leede BM, Schulkes R, Petkovich M, et al.: Human retinoic acid (RA) 4-hydroxylase (CYP26) is highly specific for all-trans-RA and can be induced through RA receptors in human breast and colon carcinoma cells. Cell Growth Differ 9, 629–637, 1998.
   PubMedGoogle Scholar
• Park EY, Dillard A, Williams EA, Wilder ET, Pepper MR, et al.: Retinol inhibits the growth of all-trans-retinoic acid-sensitive and all-trans-retinoic acid-resistant colon cancer cells through a retinoic acid receptor-independent mechanism. Cancer Res 65, 9923–9933, 2005.
   PubMed Web of Science ®Google Scholar
• Chen L and Khillan JS: A novel signaling by vitamin A/retinol promotes self renewal of mouse embryonic stem cells by activating PI3K/Akt signaling pathway via insulin-like growth factor-1 receptor. Stem Cells 28, 57–63, 2010.
   PubMed Web of Science ®Google Scholar
• Lackey DE and Hoag KA: Vitamin A upregulates matrix metalloproteinase-9 activity by murine myeloid dendritic cells through a nonclassical transcriptional mechanism. J Nutr 140, 1502–1508, 2008.
   Web of Science ®Google Scholar
• Qin YH, Lei FY, Hu P, Pei J, Feng ZB, et al.: Effect of all-trans retinoic acid on renal expressions of matrix metalloproteinase-2, matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-1 in rats with glomerulosclerosis. Pediatr Nephrol 24, 1477–1486, 2009.
   PubMed Web of Science ®Google Scholar
• Darmanin S, Chen J, Zhao S, Cui H, Shirkoohi R, et al.: All-trans retinoic acid enhances murine dendritic cell migration to draining lymph nodes via the balance of matrix metalloproteinases and their inhibitors. J Immunol 179, 4616–4625, 2007.
   PubMed Web of Science ®Google Scholar
• Lee TF, Mak KM, Rackovsky O, Lin YL, Kwong AJ, et al.: Downregulation of hepatic stellate cell activation by retinol and palmitate mediated by adipose differentiation-related protein (ADRP). J Cell Physiol 223, 648–657, 2010.
   PubMed Web of Science ®Google Scholar
• Vorotnikova E, Tries M, and Braunhut S: Retinoids and TIMP1 prevent radiation-induced apoptosis of capillary endothelial cells. Radiat Res 161, 174–184, 2004.
   PubMed Web of Science ®Google Scholar
• Jette C, Peterson PW, Sandoval IT, Manos EJ, Hadley E, et al.: The tumor suppressor adenomatous polyposis coli and caudal related homeodomain protein regulate expression of retinol dehydrogenase L. J Biol Chem 279, 34397–34405, 2004.
   PubMed Web of Science ®Google Scholar
• Weinzweig J, Tattini C, Lynch S, Zienowicz R, Weinzweig N, et al.: Investigation of the growth and metastasis of malignant melanoma in a murine model: the role of supplemental vitamin A. Plastic Reconstr Surg 112, 152–158, 2003.
   PubMed Web of Science ®Google Scholar
• Delage B, Groubet R, Pallet V, Bairras C, Higueret P, et al.: Vitamin A prevents high fat diet-induced ACF development and modifies the pattern of expression of peroxisome proliferator and retinoic acid receptor mRNA. Nutr Cancer 48, 28–36, 2004.
   PubMed Web of Science ®Google Scholar
• Penniston K and Tanumihardjo S: The acute and chronic toxic effects of vitamin A. Am J Clin Nutr 83, 191–201, 2006.
   PubMed Web of Science ®Google Scholar
• Guo XN, Rajput A, Rose R, Hauser J, Beko A, et al.: Mutant PIK3CA-bearing colon cancer cells display increased metastasis in an orthotopic model. Cancer Res 67, 5851–5858, 2007.
   PubMed Web of Science ®Google Scholar