Exendin-4 Induces Cell Adhesion and Differentiation and Counteracts the Invasive Potential of Human Neuroblastoma Cells

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Luciani, Paola ^a   Deledda, Cristiana ^a   Benvenuti, Susanna ^a   Squecco, Roberta ^b   Cellai, Ilaria ^a   Fibbi, Benedetta ^a   Marone, Ilaria Maddalena ^a   Giuliani, Corinna ^a   Modi, Giulia ^a   Francini, Fabio ^b   Vannelli, Gabriella Barbara ^b   Peri, Alessandro ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

^b UNIVERSITY OF FLORENCE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MARKER; EXENDIN 4; VITRONECTIN;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL ADHESION; CELL DIFFERENTIATION; CELL MIGRATION; CELL STRAIN; CELL STRAIN SH SY5Y; CELL STRAIN SK N AS; CONTROLLED STUDY; CULTURE TECHNIQUE; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NEURITE; NEUROBLASTOMA CELL; PHENOTYPE;

CALCIUM CHANNELS; CELL ADHESION; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL MOVEMENT; CELL SURVIVAL; CELLS, CULTURED; GENE EXPRESSION; HUMANS; HYPOGLYCEMIC AGENTS; MEMBRANE POTENTIALS; MICROTUBULE-ASSOCIATED PROTEINS; NEOPLASM INVASIVENESS; NEUROBLASTOMA; PEPTIDES; PROTEIN BINDING; RECEPTORS, GLUCAGON; RECEPTORS, UROKINASE PLASMINOGEN ACTIVATOR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SYNAPTOPHYSIN; TAU PROTEINS; VENOMS; VITRONECTIN;

EID: 84882745517     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0071716     Document Type: Article

References (44)

1. Kolterman OG, Kim DD, Shen L, Ruggles JA, Nielsen LL, et al. (2005) Pharmacokinetics, pharmacodynamics, and safety of exenatide in patients with type 2 diabetes mellitus. Am J Health Syst Pharm 62: 173-181.
2. Göke R, Larsen PJ, Mikkelsen JD, Sheikh SP, (1995) Distribution of GLP-1 binding sites in the rat brain: evidence that exendin-4 is a ligand of brain GLP-1 binding sites. Eur J Neurosci 7: 2294-2300.
3. Baggio LL, Drucker DJ, (2007) Biology of incretins: GLP-1 and GIP. Gastroenterology 132: 2131-2157.
4. During MJ, Cao L, Zuzga DS, Francis JS, Fitzsimons HL, et al. (2003) Glucagon-like peptide-1 receptor is involved in learning and neuroprotection. Nat. Med. 9: 1173-1179.
5. Perry T, Lahiri DK, Chen D, Zhou J, Shaw KT, et al. (2002) A novel neurotrophic property of glucagon-like peptide 1: a promoter of nerve growth factor-mediated differentiation in PC12 cells. J Pharmacol Exp Ther 300: 958-966.
6. Perry T, Lahiri DK, Sambamurti K, Chen D, Mattson MP, et al. (2003) Glucagon-like peptide-1 decreases endogenous amyloid-beta peptide (Abeta) levels and protects hippocampal neurons from death induced by Abeta and iron. J Neurosci Res 72: 603-612.
7. Körner M, Stöckli M, Waser B, Reubi JC, (2007) GLP-1 receptor expression in human tumors and human normal tissues: potential for in vivo targeting. J Nucl Med 48: 736-743.
8. Koehler JA, Kain T, Drucker DJ, (2011) Glucagon-like peptide-1 receptor activation inhibits growth and augments apoptosis in murine CT26 colon cancer cells. Endocrinology 152: 3362-3372.
9. Ligumsky H, Wolf I, Israeli S, Haimsohn M, Ferber S, et al. (2012) The peptide-hormone glucagon-like peptide-1 activates cAMP and inhibits growth of breast cancer cells. Breast Cancer Res Treat 132: 449-461.
10. Uchiyama A, Mukai M, Fujiwara Y, Kobayashi S, Kawai N, et al. (2007) Inhibition of transcellular tumor cell migration and metastasis by novel carba-derivatives of cyclic phosphatidic acid. Biochim Biophys Acta 1771: 103-112.
11. Lee M, Hadi M, Halldén G, Aponte GW, (2005) Peptide YY and neuropeptide Y induce villin expression, reduce adhesion, and enhance migration in small intestinal cells through the regulation of CD63, matrix metalloproteinase-3, and Cdc42 activity. J Biol Chem 280: 125-136.
12. Johnston JA, Taub DD, Lloyd AR, Conlon K, Oppenheim JJ, et al. (1994) Human T lymphocyte chemotaxis and adhesion induced by vasoactive intestinal peptide. J Immunol 153: 1762-1768.
13. Cheng HC, Abdel-Ghany M, Elble RC, Pauli BU, (1998) Lung endothelial dipeptidyl peptidase IV promotes adhesion and metastasis of rat breast cancer cells via tumor cell surface-associated fibronectin. J Biol Chem 273: 24207-24215.
14. Shingu K, Helfritz A, Zielinska-Skowronek M, Meyer-Olson D, Jacobs R, et al. (2003) CD26 expression determines lung metastasis in mutant F344 rats: involvement of NK cell function and soluble CD26. Cancer Immunol Immunother 52: 546-554.
15. Havre PA, Abe M, Urasaki Y, Ohnuma K, Morimoto C, et al. (2009) CD26 expression on T cell lines increases SDF-1-alpha-mediated invasion. Br J Cancer 101: 983-991.
16. Maris JM, Hogarty MD, Bagatell R, Cohn SL, (2007) Neuroblastoma. Lancet 369: 2106-2120.
17. Luciani P, Deledda C, Benvenuti S, Cellai I, Monici M, et al. (2010) Differentiating effects of the glucagon-like peptide-1 analogue exendin-4 in a human neuronal cell model. Cell Mol Life Sci 67: 3711-3723.
18. Vannelli GB, Ensoli F, Zonefrati R, Kubota Y, Arcangeli A, et al. (1995) Neuroblast long-term cell cultures from human fetal olfactory epithelium respond to odors J Neurosci. 15: 4382-4394.
19. Benvenuti S, Saccardi R, Luciani P, Urbani S, Deledda C, et al. (2006) Neuronal differentiation of human mesenchymal stem cells: changes in the expression of the Alzheimer's disease-related gene seladin-1. Exp Cell Res 312: 2592-2604.
20. Giannini S, Benvenuti S, Luciani P, Manuelli C, Cellai I, et al. (2008) Intermittent high glucose concentrations reduce neuronal precursor survival by altering the IGF system: the involvement of the neuroprotective factor DHCR24 (Seladin-1). J Endocrinol 198: 523-532.
21. Cellai I, Benvenuti S, Luciani P, Galli A, Ceni E, et al. (2006) Published online 2006 Antineoplastic effects of rosiglitazone and PPARγ transactivation in neuroblastoma cells. Br J Cancer 95: 879-888.
22. Formigli L, Francini F, Tani A, Squecco R, Nosi D, et al. (2005) Morphofunctional integration between skeletal myoblasts and adult cardiomyocytes in coculture is favored by direct cell-cell contacts and relaxin treatment. Am J Physiol Cell Physiol 288: 795-804.
23. Formigli L, Sassoli C, Squecco R, Bini F, Martinesi M, et al. (2009) Regulation of transient receptor potential canonical channel (TRPC1) by sphingosine 1-phosphate in C2C12 myoblasts and its relevance for a role of mechanotransduction in skeletal muscle differentiation. J Cell Sci 122: 1322-1333.
24. Krause S, Maffini MV, Soto AM, Sonnenschein C, (2008) A novel 3D in vitro culture model to study stromal-epithelial interactions in the mammary gland. Tissue Eng Part C Methods 14: 261-271.
25. Sbrana F, Sassoli C, Meacci E, Nosi D, Squecco R, et al. (2008) Role for stress fiber contraction in surface tension development and stretch-activated channel regulation in C2C12 myoblasts. Am J Physiol Cell Physiol 295: C160-C172.
26. Ma M, Ye JY, Deng R, Dee CM, Chan GC, (2001) Mesenchymal stromal cells may enhance metastasis of neuroblastoma via SDF-1/CXCR4 and SDF1/CXCR7 signalling. Cancer Lett 31: 1-10.
27. Meyer A, van Golen CM, Kim B, van Golen KL, Feldman EL, (2004) Integrin expression regulates neuroblastoma attachment and migration. Neoplasia 6: 332-342.
28. Pola S, Cattaneo MG, Vicentini LM, (2003) Anti-migratory and anti-invasive effect of somatostatin in human neuroblastoma cells: involvement of Rac and MAP kinase activity. J Biol Chem 278: 40601-40606.
29. O'Neill GM, (2009) The coordination between actin filaments and adhesion in mesenchymal migration. Cell Adh Migr 3: 355-357.
30. Gladson CL, Dennis C, Rotolo TC, Kelly DR, Grammer JR, (1997) Vitronectin expression in differentiating neuroblastic tumors: integrin alpha v beta 5 mediates vitronectin-dependent adhesion of retinoic-acid-differentiated neuroblastoma cells. Am J Pathol. 150: 1631-1646.
31. Li P, Gao Y, Ji Z, Zhang X, Xu Q, et al. (2004) Role of urokinase plasminogen activator and its receptor in metastasis and invasion of neuroblastoma. J Pediatr Surg 39: 1512-1519.
32. Geminder H, Sagi-Assif O, Goldberg L, Meshel T, Rechavi G, et al. (2001) A possible role for CXCR4 and its ligand, the CXC chemokine stromal cell-derived factor-1, in the development of bone marrow metastases in neuroblastoma. J Immunol 167: 4747-4757.
33. Marx N, Burgmaier M, Heinz P, Ostertag M, Hausauer A, et al. (2010) Glucagon-like peptide-1(1-37) inhibits chemokine-induced migration of human CD4-positive lymphocytes. Cell Mol Life Sci 67: 3549-3555.
34. Lam WA, Cao L, Umesh V, Keung AJ, Sen S, et al. (2010) Extracellular matrix rigidity modulates neuroblastoma cell differentiation and N-myc expression. Mol Cancer 9: 35.
35. Chambaut-Guerin AM, Herigault H, Rouet-Benzineb P, Rouher C, Lafuma C, (2000) Induction of matrix metalloproteinase MMP-9 (92-kDa gelatinase) by retinoic acid in human neuroblastoma SKNBE cells: relevance to neuronal differentiation. J Neurochem 74: 508-517.
36. Nordstrom LA, Lochner J, Yeung W, Ciment G, (1995) The metalloproteinase stromelysin-1 (transin) mediates PC12 cell growth cone invasiveness through basal laminae. Mol Cell Neurosci 6: 56-68.
37. Joshi S, Guleria RS, Pan J, Dipette D, Singh US, (2007) Heterogeneity in retinoic acid signaling in neuroblastomas: Role of matrix metalloproteinases in retinoic acid-induced differentiation. Biochim Biophys Acta 1772: 1093-1102.
38. Wang LH, (2004) Molecular signaling regulating anchorage-independent growth of cancer cells. Mt Sinai J Med 71: 361-367.
39. Ross RA, Biedler JL, Spengler BA, (2003) A role for distinct cell types in determining malignancy in human neuroblastoma cell lines and tumors. Cancer Lett 197: 35-39.
40. Cheung BB, Marshall GM, (2011) Targeting ATP7A to increase the sensitivity of neuroblastoma cells to retinoid therapy. Curr Cancer Drug Targets 11: 826-836.
41. Crespel A, De Boisvilliers F, Gros L, Kervran A, (1996) Effects of glucagon and glucagon-like peptide-1-(7-36) amide on C cells from rat thyroid and medullary thyroid carcinoma CA-77 cell line. Endocrinology 137: 3674-3680.
42. Bjerre Knudsen L, Madsen LW, Andersen S, Almholt K, de Boer AS, et al. (2010) Glucagon-like Peptide-1 receptor agonists activate rodent thyroid C-cells causing calcitonin release and C-cell proliferation. Endocrinology 151: 1473-1486.
43. Elashoff M, Matveyenko AV, Gier B, Elashoff R, Butler PC, (2011) Pancreatitis, pancreatic, and thyroid cancer with glucagon-like peptide-1-based therapies. Gastroenterology 141: 150-156.
44. Alves C, Batel-Marques F, Macedo AF, (2012) A meta-analysis of serious adverse events reported with exenatide and liraglutide: acute pancreatiris and cancer. Diabetes Res Clin Pract 98: 271-284.