Novel activities of pro-IGF-I E peptides: Regulation of morphological differentiation and anchorage-independent growth in human neuroblastoma cells

Experimental Cell Research

Volumn 280, Issue 1, 2002, Pages 75-89

  Kuo, Ya Huei ^a   Chen, Thomas T ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

Growth and differentiation; Neuroblastoma cells; Pro IGF I E peptide

Indexed keywords

BIOLOGICAL MARKER; MICROTUBULE ASSOCIATED PROTEIN 2; MITOGEN ACTIVATED PROTEIN KINASE 1; NEUROPEPTIDE Y; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN; PROTEIN HEA; PROTEIN HEB; PROTEIN RTEA4; SIGNAL PEPTIDE; SOMATOMEDIN; TAURINE; UNCLASSIFIED DRUG;

ARTICLE; CELL ANCHORAGE; CELL DIFFERENTIATION; CELL GROWTH; COLONY FORMING CELL; CONTROLLED STUDY; GENETIC CODE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; MOLECULAR BIOLOGY; MOLECULAR CLONING; NERVE FIBER GROWTH; NEUROBLASTOMA CELL; NEUROFILAMENT; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

EID: 0036031802     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1006/excr.2002.5628     Document Type: Article

References (68)

1. Shamblott, M. J., and Chen, T. T. (1993). Age-related and tissue-specific levels of five forms of insulin-like growth factor mRNA in a teleost. Mol. Mar. Biol. Biotechnol. 2, 351-361.
2. Rotwein, P., Pollock, K. M., Didier, D. K., and Krivi, G. G. (1986). Organization and sequence of the human insulin-like growth factor I gene. Alternative RNA processing produces two insulin-like growth factor I precursor peptides. J. Biol. Chem. 261, 4828-4832.
3. Rotwein, P. (1986). Two insulin-like growth factor I messenger RNAs are expressed in human liver. Proc. Natl. Acad. Sci. USA 83, 77-81.
4. Shimatsu, A., and Rotwein, P. (1987). Mosaic evolution of the insulin-like growth factors. Organization, sequence, and expression of the rat insulin-like growth factor I gene. J. Biol. Chem. 262, 7894-7900.
5. Chew, S. L., Lavender, P., Clark, A. J., and Ross, R. J. (1995). An alternatively spliced human insulin-like growth factor-I transcript with hepatic tissue expression that diverts away from the mitogenic IBE1 peptide. Endocrinology 136, 1939-1944.
6. Foyt, H. L., and Roberts, C. T., Jr. (1991). In "Insulin-Like Growth Factors: Molecular and Cellular Aspects" (D., LeRoith, Ed.), pp. 1-16. CRC Press, Boca Raton, FL.
7. Forst, T., Kunt, T., Pohlmann, T., Goitom, K., Engelbach, M., Beyer, J., and Pfutzner, A. (1998). Biological activity of C-peptide on the skin microcirculation in patients with insulin-dependent diabetes mellitus. J. Clin. Invest. 101, 2036-2041.
8. Ido, Y., Vindigni, A., Chang, K., Stramm, L., Chance, R., Heath, W. F., DiMarchi, R. D., Di Cera, E., and Williamson, J. R. (1997). Prevention of vascular and neural dysfunction in diabetic rats by C-peptide. Science 277, 563-566.
9. Sjoquist, M., Huang, W., and Johansson, B. L. (1998). Effects of C-peptide on renal function at the early stage of experimental diabetes. Kidney Int. 54, 758-764.
10. Rigler, R., Pramanik, A., Jonasson, P., Kratz, G., Jansson, O. T., Nygren, P., Stahl, S., Ekberg, K., Johansson, B., Uhlen, S., Uhlen, M., Jornvall, H., and Wahren, J. (1999). Specific binding of proinsulin C-peptide to human cell membranes. Proc. Natl. Acad. Sci. USA 96, 13318-13323.
11. Lin, W. W., and Oberbauer, A. M. (1998). Alternative splicing of insulin-like growth factor I mRNA is developmentally regulated in the rat and mouse with preferential exon 2 usage in the mouse. Growth Horm. IGF Res. 8, 225-233.
12. Lin, W. W., and Oberbauer, A. M. (1999). Spatiotemporal expression of alternatively spliced IGF-I mRNA in the rat costochondral growth plate. J. Endocrinol. 160, 461-467.
13. Greene, M. W., and Chen, T. T. (1997). Temporal expression pattern of insulin-like growth factor mRNA during embryonic development in a teleost, rainbow trout (Onchorynchus mykiss). Mol. Mar. Biol. Biotechnol. 6, 144-151.
14. Duguay, S. J., Swanson, P., and Dickhoff, W. W. (1994). Differential expression and hormonal regulation of alternatively spliced IGF-I mRNA transcripts in salmon. J. Mol. Endocrinol. 12, 25-37.
15. Duguay, S. J., Lai-Zhang, J., and Steiner, D. F. (1995). Mutational analysis of the insulin-like growth factor I prohormone processing site. J. Biol. Chem. 270, 17566-17574.
16. Hylka, V. W., and Straus, D. S. (1990). The E-domain peptide of rat pro-insulin-like growth factor II (proIGF-II): Properties of the peptide in serum and production by rat cell lines. Biochim. Biophys. Acta 1051, 6-13.
17. Hylka, V. W., Teplow, D. B., Kent, S. B., and Straus, D. S. (1985). Identification of a peptide fragment from the carboxyl-terminal extension region (E-domain) of rat proinsulin-like growth factor-II. J. Biol. Chem. 260, 14417-14420.
18. Straus, D. S., and Takemoto, C. D. (1988). Amino acid limitation negatively regulates insulin-like growth factor-II mRNA levels and E-domain peptide secretion at a post-transcriptional step in BRL-3A rat liver cells. J. Biol. Chem. 263, 18404-18410.
19. Yang, Y. W., Romanus, J. A., Liu, T. Y., Nissley, S. P., and Rechler, M. M. (1985). Biosynthesis of rat insulin-like growth factor II. I. Immunochemical demonstration of a approximately 20-kilodalton biosynthetic precursor of rat insulin-like growth factor II in metabolically labeled BRL-3A rat liver cells. J. Biol. Chem. 260, 2570-2577.
20. Siegfried, J. M., Kasprzyk, P. G., Treston, A. M., Mulshine, J. L., Quinn, K. A., and Cuttitta, F. (1992). A mitogenic peptide amide encoded within the E peptide domain of the insulin-like growth factor IB prohormone. Proc. Natl. Acad. Sci. USA 89, 8107-8111.
21. Tian, X. C., Chen, M. J., Pantschenko, A. G., Yang, T. J., and Chen, T. T. (1999). Recombinant E-peptides of pro-IGF-I have mitogenic activity. Endocrinology 140, 3387-3390.
22. Chen, M. J., Kuo, Y.-H., and Chen, T. T. (2002). Novel biological activities of the pro-IGF-I E-peptides: Studies on effects of pro-IGF-I E-peptide on morphological change, anchorage-independent cell division, and invasiveness in tumor cells. Gen. Comp. Endocrinol. 126, 342-351.
23. Encinas, M., Iglesias, M., Llecha, N., and Comella, J. X. (1999). Extracellular-regulated kinases and phosphatidylinositol 3-kinase are involved in brain-derived neurotrophic factor-mediated survival and neuritogenesis of the neuroblastoma cell line SH-SY5Y. J. Neurochem. 73, 1409-1421.
24. Perez-Juste, G., and Aranda, A. (1999). Differentiation of neuroblastoma cells by phorbol esters and insulin-like growth factor 1 is associated with induction of retinoic acid receptor beta gene expression. Oncogene 18, 5393-5402.
25. Turco, A., Scarpa, S., Coppa, A., Baccheschi, G., Palumbo, C., Leonetti, C., Zupi, G., and Colletta, G. (2000) Increased TGF-beta type II receptor expression suppresses the malignant phenotype and induces differentiation of human neuroblastoma cells. Exp. Cell Res. 255, 77-85.
26. Fagerstrom, S., Pahlman, S., Gestblom, C., and Nanberg, E. (1996). Protein kinase C-epsilon is implicated in neurite out-growth in differentiating human neuroblastoma cells. Cell Growth Differ. 7, 775-785.
27. Garcia-Perez, J., Avila, J., and Diaz-Nido, J. (1999). Lithium induces morphological differentiation of mouse neuroblastoma cells. J. Neurosci. Res. 57, 261-270.
28. Morrione, A., Romano, G., Navarro, M., Reiss, K., Valentinis, B., Dews, M., Eves, E., Rosner, M. R., and Baserga, R. (2000). Insulin-like growth factor I receptor signaling in differentiation of neuronal H19-7 cells. Cancer Res. 60, 2263-2272.
29. Macpherson, I. (1973). In "Tissue Culture Methods and Applications" (Kruse, P. F. and Petterson, M.K. Jr, Ed.), pp. 276-280. Academic Press, New York.
30. Chomczynski, P., and Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159.
31. Voigt, A., Hartmann, P., and Zintl, F. (2000). Differentiation, proliferation and adhesion of human neuroblastoma cells after treatment with retinoic acid. Cell Adhes. Commun. 7, 423-440.
32. Chambaut-Guerin, A. M., Herigault, S., Rouet-Benzineb, P., Rouher, C., and 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.
33. Tieu, K., Zuo, D. M., and Yu, P. H. (1999). Differential effects of staurosporine and retinoic acid on the vulnerability of the SH-SY5Y neuroblastoma cells: Involvement of bcl-2 and p53 proteins. J. Neurosci. Res. 58, 426-435.
34. Arnold, S. E., and Trojanowski, J. Q. (1996). Human fetal hippocampal development: II. The neuronal cytoskeleton. J. Comp. Neurol. 367, 293-307.
35. Kosik, K. S., and Finch, E. A. (1987). MAP2 and tau segregate into dendritic and axonal domains after the elaboration of morphologically distinct neurites: An immunocytochemical study of cultured rat cerebrum. J. Neurosci. 7, 3142-3153.
36. Andersson, G., Pahlman, S., Parrow, V., Johansson, I., and Hammerling, U. (1994). Activation of the human NPY gene during neuroblastoma cell differentiation: Induced transcriptional activities of AP-1 and AP-2. Cell Growth Differ. 5, 27-36.
37. Perron, J. C., and Bixby, J. L. (1999). Distinct neurite out-growth signaling pathways converge on ERK activation. Mol. Cell. Neurosci. 13, 362-378.
38. Sarner, S., Kozma, R., Ahmed, S., and Lim, L. (2000). Phosphatidylinositol 3-kinase, Cdc42, and Rac1 act downstream of Ras in integrin-dependent neurite outgrowth in N1E-115 neuroblastoma cells. Mol. Cell. Biol. 20, 158-172.
39. Vlahos, C. J., Matter, W. F., Hui, K. Y., and Brown, R. F. (1994). A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J. Biol. Chem. 269, 5241-5248.
40. Thelen, M., Wymann, M. P., and Langen, H. (1994). Wortmannin binds specifically to 1-phosphatidylinositol 3-kinase while inhibiting guanine nucleotide-binding protein-coupled receptor signaling in neutrophil leukocytes. Proc. Natl. Acad. Sci. USA 91, 4960-4964.
41. Alessi, D. R., Cuenda, A., Cohen, P., Dudley, D. T., and Saltiel, A. R. (1995). PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo. J. Biol. Chem. 270, 27489-27494.
42. Blenis, J. (1993). Signal transduction via the MAP kinases: Proceed at your own RSK. Proc. Natl. Acad. Sci. USA 90, 5889-5892.
43. Payne, D. M., Rossomando, A. J., Martino, P., Erickson, A. K., Her, J. H., Shabanowitz, J., Hunt, D. F., Weber, M. J., and Sturgill, T. W. (1991). Identification of the regulatory phosphorylation sites in pp42/mitogen-activated protein kinase (MAP kinase). EMBO J. 10, 885-892.
44. Aplin, A. E., Howe, A., Alahari, S. K., and Juliano, R. L. (1998). Signal transduction and signal modulation by cell adhesion receptors: The role of integrins, cadherins, immunoglobulin-cell adhesion molecules, and selectins. Pharmacol. Rev. 50, 197-263.
45. Adams, J. C., and Watt, F. M. (1993). Regulation of development and differentiation by the extracellular matrix. Development 117, 1183-1198.
46. Lee, Y. J., and Streuli, C. H. (1999). Extracellular matrix selectively modulates the response of mammary epithelial cells to different soluble signaling ligands. J. Biol. Chem. 274, 22401-22408.
47. Bonfoco, E., Chen, W., Paul, R., Cheresh, D. A., and Cooper, N. R. (2000). beta1 integrin antagonism on adherent, differentiated human neuroblastoma cells triggers an apoptotic signaling pathway. Neuroscience 101, 1145-1152.
48. Reiske, H. R., Zhao, J., Han, D. C., Cooper, L. A., and Guan, J. (2000). Analysis of FAK-associated signaling pathways in the regulation of cell cycle progression. FEBS Lett. 486, 275-280.
49. Matus, A. (1991). Microtubule-associated proteins and neuronal morphogenesis. J. Cell Sci. Suppl. 15, 61-67.
50. Maccioni, R. B., and Cambiazo, V. (1995). Role of microtubule-associated proteins in the control of microtubule assembly. Physiol. Rev. 75, 835-864.
51. Caceres, A., Banker, G. A., and Binder, L. (1986). Immunocytochemical localization of tubulin and microtubule-associated protein 2 during the development of hippocampal neurons in culture. J. Neurosci. 6, 714-722.
52. Ferreira, A., Busciglio, J., and Caceres, A. (1989). Microtubule formation and neurite growth in cerebellar macroneurons which develop in vitro: Evidence for the involvement of the microtubule-associated proteins, MAP-1a, HMW-MAP2 and Tau. Brain Res. Dev. Brain Res. 49, 215-228.
53. Falconer, M. M., Vielkind, U., and Brown, D. L. (1989) Association of acetylated microtubules, vimentin intermediate filaments, and MAP 2 during early neural differentiation in EC cell culture. Biochem. Cell. Biol. 67, 537-544.
54. Saragoni, L., Hernandez, P., and Maccioni, R. B. (2000). Differential association of tau with subsets of microtubules containing posttranslationally modified tubulin variants in neuroblastoma cells. Neurochem. Res. 25, 59-70.
55. Li, B. S., Zhang, L., Gu, J., Amin, N. D., and Pant, H. C. (2000). Integrin alpha(1) beta(1)-mediated activation of cyclin-dependent kinase 5 activity is involved in neurite outgrowth and human neurofilament protein H Lys-Ser-Pro tail domain phosphorylation. J. Neurosci. 20, 6055-6062.
56. Brugg, B., and Matus, A. (1991). Phosphorylation determines the binding of microtubule-associated protein 2 (MAP2) to microtubules in living cells. J. Cell Biol. 114, 735-743.
57. Avila, J., Dominguez, J., and Diaz-Nido, J. (1994). Regulation of microtubule dynamics by microtubule-associated protein expression and phosphorylation during neuronal development. Int. J. Dev. Biol. 38, 13-25.
58. Drewes, G., Ebneth, A., and Mandelkow, E. M. (1998). MAPs, MARKs and microtubule dynamics. Trends Biochem. Sci. 23, 307-311.
59. Zamora-Leon, S. P., Lee, G., Davies, P., and Shafit-Zagardo, B. (2001). Binding of Fyn to MAP-2c through an SH3 binding domain: regulation of the interaction by ERK2. J. Biol. Chem. 23, 23.
60. Singh, M., Setalo, G., Jr., Guan, X., Warren, M., and Toran-Allerand, C. D. (1999). Estrogen-induced activation of mitogen-activated protein kinase in cerebral cortical explants: Convergence of estrogen and neurotrophin signaling pathways. J. Neurosci. 19, 1179-1188.
61. Sanchez, C., Tompa, P., Szucs, K., Friedrich, P., and Avila, J. (1996). Phosphorylation and dephosphorylation in the proline-rich C-terminal domain of microtubule-associated protein 2. Eur. J. Biochem. 241, 765-771.
62. Sanchez, C., Diaz-Nido, J., and Avila, J. (1995). Variations in in vivo phosphorylation at the proline-rich domain of the microtubule-associated protein 2 (MAP2) during rat brain development. Biochem. J. 306, 481-487.
63. Veeranna, Amin, N. D., Ahn, N. G., Jaffe, H., Winters, C. A., Grant, P., and Pant, H. C. (1998). Mitogen-activated protein kinases (Erk1,2) phosphorylate Lys-Ser-Pro (KSP) repeats in neurofilament proteins NF-H and NF-M. J. Neurosci. 18, 4008-4021.
64. Vaillant, A. R., Mazzoni, I., Tudan, C., Boudreau, M., Kaplan, D. R., and Miller, F. D. (1999). Depolarization and neurotrophins converge on the phosphatidylinositol 3-kinase-Akt pathway to synergistically regulate neuronal survival. J. Cell Biol. 146, 955-966.
65. Leevers, S. J., Vanhaesebroeck, B., and Waterfield, M. D. (1999). Signalling through phosphoinositide 3-kinases: The lipids take centre stage. Curr. Opin. Cell Biol. 11, 219-225.
66. Wahren, J., Ekberg, K., Johansson, J., Henriksson, M., Pramanik, A., Johansson, B. L., Rigler, R., and Jornvall, H. (2000). Role of C-peptide in human physiology. Am. J. Physiol. Endocrinol. Metab. 278, E759-768.
67. Johansson, B. L., Sjoberg, S., and Wahren, J. (1992). The influence of human C-peptide on renal function and glucose utilization in type 1 (insulin-dependent) diabetic patients. Diabetologia 35, 121-128.
68. Johansson, B. L., Linde, B., and Wahren, J. (1992). Effects of C-peptide on blood flow, capillary diffusion capacity and glucose utilization in the exercising forearm of type 1 (insulin-dependent) diabetic patients. Diabetologia 35, 1151-1158.