IGFBP-3 activates TGF-β receptors and directly inhibits growth in human intestinal smooth muscle cells

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 287, Issue 4 50-4, 2004, Pages

  Kuemmerle, John F ^a,b   Murthy, Karnam S ^a   Bowers, Jennifer G ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

Insulin like growth factor I; Short interfering RNA; Smad2

Indexed keywords

IODINE 125; SERINE; SMAD2 PROTEIN; SMALL INTERFERING RNA; SOMATOMEDIN BINDING PROTEIN 3; SOMATOMEDIN C; THYMIDINE; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2; TRANSFORMING GROWTH FACTOR BETA RECEPTOR V; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

AFFINITY LABELING; ARTICLE; AUTOCRINE EFFECT; CARCINOMA CELL; CELL GROWTH; CELL PROLIFERATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; INTESTINE MUSCLE; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RECEPTOR UPREGULATION; STIMULATION;

ACTIVIN RECEPTORS, TYPE I; AUTOCRINE COMMUNICATION; CELL DIVISION; CELLS, CULTURED; DNA-BINDING PROTEINS; HUMANS; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 3; INTESTINES; IODINE RADIOISOTOPES; MYOCYTES, SMOOTH MUSCLE; PHOSPHORYLATION; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; RNA, SMALL INTERFERING; SMAD2 PROTEIN; TRANS-ACTIVATORS;

EID: 4644235820     PISSN: 01931857     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpgi.00009.2004     Document Type: Article

References (42)

1. Baxter RC. Signalling pathways involved in antiproliferative effects of IGFBP-3: a review. Mol Pathol 54: 145-148, 2001.
2. Bushman TL and Kuemmerle JF. IGFBP-3 and IGFBP-5 production by human intestinal muscle: reciprocal regulation by endogenous TGF-β1. Am J Physiol Gastrointest Liver Physiol 275: G1282-G1290, 1998.
3. Cheifetz S, Like B, and Massague J. Cellular distribution of type I and type II receptors for transforming growth factor-β. J Biol Chem 261: 9972-9978, 1986.
4. Cohen P, Lamson G, Okajima T, and Rosenfeld RG. Transfection of the human insulin-like growth factor binding protein-3 gene into Balb/c fibroblasts inhibits cellular growth. Mol Endocrinol 7: 380-386, 1993.
5. Derynck R and Zhang YE. Smad-dependent and Smad-independent pathways in TGF-β family signalling. Nature 425: 577-584, 2003.
6. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, and TuschI T. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411: 494-498, 2001.
7. Fanayan S, Firth SM, and Baxter RC. Signaling through the Smad pathway by insulin-like growth factor-binding protein-3 in breast cancer cells. Relationship to transforming growth factor-β 1 signaling. J Biol Chem 277: 7255-7261, 2002.
8. Fanayan S, Firth SM, Butt AJ, and Baxter RC. Growth inhibition by insulin-like growth factor-binding protein-3 in T47D breast cancer cells requires transforming growth factor-β3 (TGF-β) and the type II TGF-β receptor. J Biol Chem 275: 39146-39151, 2000.
9. Hsieh T, Gordon RE, Clemmons DR, Busby WH Jr, and Duan C. Regulation of vascular smooth muscle cell responses to insulin-like growth factor (IGF)-I by local IGF-binding proteins. J Biol Chem 278: 42886-42892, 2003.
10. Huang SS, Ling TY, Tseng WF, Huang YH, Tang FM, Leal SM, and Huang JS. Cellular growth inhibition by IGFBP-3 and TGF-β1 requires LRP-1. FASEB J 17: 2068-2081, 2003.
11. Kansra S, Ewton DZ, Wang J, and Friedman E. IGFBP-3 mediates TGF-β1 proliferative response in colon cancer cells. Int J Cancer 87: 373-378, 2000.
12. Katsanos KH, Tsatsoulis A, Christodoulou D, Challa A, Katsaraki A, and Tsianos EV. Reduced serum insulin-like growth factor-1 (IGF-1) and IGF-binding protein-3 levels in adults with inflammatory bowel disease. Growth Hormone IGF Res 11: 364-367, 2001.
13. Kelley KM, Oh Y, Gargosky SE, Gucev Z, Matsumoto T, Hwa V, Ng L, Simpson DM, and Rosenfeld RG. Insulin-like growth factor-binding proteins (IGFBPs) and their regulatory dynamics. Int J Biochem Cell Biol 28: 619-637, 1996.
14. Kuemmerle JF. Autocrine regulation of growth in cultured human intestinal muscle by growth factors. Gastroenterology 113: 817-824, 1997.
15. Kuemmerle JF. Endogenous IGF-I regulates IGF binding protein production in human intestinal smooth muscle cells. Am J Physiol Gastrointest Liver Physiol 278: G710-G717, 2000.
16. Kuemmerle JF. Endogenous IGF-I inhibits GSK-3 activity and promotes cell survival (Abstract). Gastroenterology 122: A-380, 2002.
17. Kuemmerle JF and Bushman TL. IGF-I stimulates intestinal muscle cell growth by activating distinct PI3-kinase and MAP kinase pathways. Am J Physiol Gastrointest Liver Physiol 275: G151-G158, 1998.
18. i2 in human intestinal smooth muscle. Gβγ-dependent mitogen-activated protein kinase activation and growth. J Biol Chem 276: 7187-7194, 2001.
19. Kuemmerle JF and Teng B. Regulation of IGFBP-4 levels in human intestinal muscle by an IGF-I-activated, confluence-dependent protease. Am J Physiol Gastrointest Liver Physiol 279: G975-G982, 2000.
20. Kuemmerle JF and Zhou H. Insulin-like growth factor-binding protein-5 (IGFBP-5) stimulates growth and IGF-I secretion in human intestinal smooth muscle by Ras-dependent activation of p38 MAP kinase and Erk1/2 pathways. J Biol Chem 277: 20563-20571, 2002.
21. Kuemmerle JF, Zhou H, and Bowers JG. IGF-I stimulates human intestinal smooth muscle cell growth by regulation of G1 phase cell cycle proteins. Am J Physiol Gastrointest Liver Physiol 286: G412-G419, 2004.
22. Lawrance IC, Maxwell L, and Doe W. Inflammation location, but not type, determines the increase in TGF-β1 and IGF-I expression and collagen deposition in IBD intestine. Inflamm Bowel Dis 7: 16-26, 2001.
23. Leal SM, Huang SS, and Huang JS. Interactions of high affinity insulin-like growth factor-binding proteins with the type V transforming growth factor-β receptor in mink lung epithelial cells. J Biol Chem 274: 6711-6717, 1999.
24. Leal SM, Liu Q, Huang SS, and Huang JS. The type V transforming growth factor-β receptor is the putative insulin-like growth factor-binding protein 3 receptor. J Biol Chem 272: 20572-20576, 1997.
25. Li W, Fawcett J, Widmer HR, Fielder PJ, Rabkin R, and Keller GA. Nuclear transport of insulin-like growth factor-I and insulin-like growth factor binding protein-3 in opossum kidney cells. Endocrinology 138: 1763-1766, 1997.
26. Oh Y, Muller HL, Lamson G, and Rosenfeld RG. Insulin-like growth factor (IGF)-independent action of IGF-binding protein-3 in Hs578T human breast cancer cells. Cell surface binding and growth inhibition. J Biol Chem 268: 14964-14971, 1993.
27. Perks CM, McCaig C, Clarke JB, Clemmons DR, and Holly JM. A non-IGF binding mutant of IGFBP-3 modulates cell function in breast epithelial cells. Biochem Biophys Res Commun 294: 988-994, 2002.
28. Rajah R, Valentinis B, and Cohen P. Insulin-like growth factor (IGF)-binding protein-3 induces apoptosis and mediates the effects of transforming growth factor-β1 on programmed cell death through a p53- and IGF-independent mechanism. J Biol Chem 272: 12181-12188, 1997.
29. Schedlich LJ, Le Page SL, Firth SM, Briggs LJ, Jans DA, and Baxter RC. Nuclear import of insulin-like growth factor-binding protein-3 and -5 is mediated by the importin β-subunit. J Biol Chem 275: 23462-23470, 2000.
30. Schedlich LJ, Young TF, Firth SM, and Baxter RC. Insulin-like growth factor-binding protein (IGFBP)-3 and IGFBP-5 share a common nuclear transport pathway in T47D human breast carcinoma cells. J Biol Chem 273: 18347-18352, 1998.
31. Shi Y and Massague J. Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell 113: 685-700, 2003.
32. Shimasaki S and Ling N. Identification and molecular characterization of insulin-like growth factor binding proteins (IGFBP-1, -2, -3, -4, -5 and -6). Prog Growth Factor Res 3: 243-266, 1991.
33. Sjogren K, Liu JL, Blad K, Skrtic S, Vidal O, Wallenius V, LeRoith D, Tornell J, Isaksson OG, Jansson JO, and Ohlsson C. Liver-derived insulin-like growth factor I (IGF-I) is the principal source of IGF-I in blood but is not required for postnatal body growth in mice. Proc Natl Acad Sci USA 96: 7088-7092, 1999.
34. 467 in the C terminus of Smad2 mediates interaction with Smad4 and is required for transforming growth factor-β signaling. J Biol Chem 272: 28107-28115, 1997.
35. Spagnoli A, Hwa V, Horton WA, Lunstrum GP, Roberts CT Jr, Chiarelli F, Torello M, and Rosenfeld RG. Antiproliferative effects of insulin-like growth factor-binding protein-3 in mesenchymal chondrogenic cell line RCJ3.1C518 relationship to differentiation stage. J Biol Chem 276: 5533-5540, 2001.
36. Takenoshita S, Mogi A, Nagashima M, Yang K, Yagi K, Hanyu A, Nagamachi Y, Miyazono K, and Hagiwara K. Characterization of the MADH2/Smad2 gene, a human Mad homolog responsible for the transforming growth factor-β and activin signal transduction pathway. Genomics 48: 1-11, 1998.
37. Teng B, Murthy KS, Kuemmerle JF, Grider JR, and Makhlouf GM. Selective expression of vasoactive intestinal peptide (VIP)2/pituitary adenylate cyclase-activating polypeptide (PACAP)3 receptors in rabbit and guinea pig gastric and tenia coli smooth muscle cells. Regul Pept 77: 127-134, 1998.
38. Teng B, Murthy KS, Kuemmerle JF, Grider JR, Sase K, Michel T, and Makhlouf GM. Expression of endothelial nitric oxide synthase in human and rabbit gastrointestinal smooth muscle cells. Am J Physiol Gastrointest Liver Physiol 275: G342-G351, 1998.
39. Williams KL, Fuller CR, Fagin J, and Lund PK. Mesenchymal IGF-I overexpression: paracrine effects in the intestine, distinct from endocrine actions. Am J Physiol Gastrointest Liver Physiol 283: G875-G885, 2002.
40. Wu HB, Kumar A, Tsai WC, Mascarenhas D, Healey J, and Rechler MM. Characterization of the inhibition of DNA synthesis in proliferating mink lung epithelial cells by insulin-like growth factor binding protein-3. J Cell Biochem 77: 288-297, 2000.
41. Yakar S, Liu JL, Stannard B, Butler A, Accili D, Sauer B, and LeRoith D. Normal growth and development in the absence of hepatic insulin-like growth factor I. Proc Natl Acad Sci USA 96: 7324-7329, 1999.
42. Zimmermann EJ, Li L, Hou YT, Mohapatra NK, and Pucilowska JB. Insulin-like growth factor I and insulin-like growth factor binding protein 5 in Crohn's disease. Am J Physiol Gastrointest Liver Physiol 280: G1022-G1029, 2001.