Targeting insulin-like growth factor-I and insulin-like growth factor-binding protein-3 signaling pathways: A novel therapeutic approach for asthma

American Journal of Respiratory Cell and Molecular Biology

Volumn 50, Issue 4, 2014, Pages 667-677

  Lee, Hyun ^a   Kim, So Ri ^a   Oh, Youngman ^b   Cho, Seong Ho ^c   Schleimer, Robert P ^c   Lee, Yong Chul ^a  

^a Chonbuk National University Medical School   (South Korea)

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

^c NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Asthma; Insulin like growth factor binding protein 3; Insulin like growth factor I

Indexed keywords

1 [4 [(5 CYCLOPROPYL 1H PYRAZOL 3 YL)AMINO]PYRROLO[2,1 F][1,2,4]TRIAZIN 2 YL] N (6 FLUORO 3 PYRIDINYL) 2 METHYL 2 PYRROLIDINECARBOXAMIDE; AMG A 12; AUTACOID; CASPASE; CIXUTUMUMAB; DALOTUZUMAB; DUSIGITUMAB; GANITUMAB; HYPOXIA INDUCIBLE FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; NORDIHYDROGUAIARETIC ACID; SOMATOMEDIN B; SOMATOMEDIN B RECEPTOR; SOMATOMEDIN BINDING PROTEIN 1; SOMATOMEDIN BINDING PROTEIN 2; SOMATOMEDIN BINDING PROTEIN 3; SOMATOMEDIN BINDING PROTEIN 4; SOMATOMEDIN BINDING PROTEIN 5; SOMATOMEDIN BINDING PROTEIN 6; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; UNCLASSIFIED DRUG; VASCULOTROPIN;

ASTHMA; ENZYME ACTIVATION; HUMAN; IMMUNOPATHOGENESIS; NONHUMAN; PROTEIN TARGETING; REGULATORY MECHANISM; RESPIRATORY SYSTEM; RESPIRATORY TRACT ALLERGY; RESPIRATORY TRACT INFLAMMATION; REVIEW; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; ANTI-ASTHMATIC AGENTS; ASTHMA; DRUG DESIGN; HUMANS; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 3; INSULIN-LIKE GROWTH FACTOR I; LUNG; MOLECULAR TARGETED THERAPY; RECEPTOR, IGF TYPE 1; RECEPTORS, CELL SURFACE; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION;

EID: 84898755074     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2013-0397TR     Document Type: Review

References (135)

1. Barnes PJ, Jonsson B, Klim JB. The costs of asthma. Eur Respir J 1996;9:636-642. (Pubitemid 26167864)
2. American Thoracic Society. Proceedings of the ATS workshop on refractory asthma: current understanding, recommendations, and unanswered questions. Am J Respir Crit Care Med 2000;162:2341-2351.
3. Caramori G, Groneberg D, Ito K, Casolari P, Adcock IM, Papi A. New drugs targeting Th2 lymphocytes in asthma. J Occup Med Toxicol 2008;3:S6.
4. Hoshino M, Nakamura Y, Sim JJ, Yamashiro Y, Uchida K, Hosaka K, Isogai S. Inhaled corticosteroid reduced lamina reticularis of the basement membrane by modulation of insulin-like growth factor (IGF)-I expression in bronchial asthma. Clin Exp Allergy 1998;28:568-577. (Pubitemid 28238271)
5. Rajah R, Nachajon RV, Collins MH, Hakonarson H, Grunstein MM, Cohen P. Elevated levels of the IGF-binding protein protease MMP-1 in asthmatic airway smooth muscle. Am J Respir Cell Mol Biol 1999;20:199-208. (Pubitemid 129504879)
6. Yamashita N, Tashimo H, Ishida H, Matsuo Y, Arai H, Nagase H, Adachi T, Ohta K. Role of insulin-like growth factor-I in allergen-induced airway inflammation and remodeling. Cell Immunol 2005;235:85-91. (Pubitemid 41597471)
7. Veraldi KL, Gibson BT, Yasuoka H, Myerburg MM, Kelly EA, Balzar S, Jarjour NN, Pilewski JM, Wenzel SE, Feghali-Bostwick CA. Role of insulin-like growth factor binding protein-3 in allergic airway remodeling. Am J Respir Crit Care Med 2009;180:611-617.
8. Lee YC, Jogie-Brahim S, Lee DY, Han J, Harada A, Murphy LJ, Oh Y. Insulin-like growth factor-binding protein-3 (IGFBP-3) blocks the effects of asthma by negatively regulating NF-κB signaling through IGFBP-3R-mediated activation of caspases. J Biol Chem 2011;286:17898-17909.
9. Kim SR, Lee KS, Lee KB, Lee YC. Recombinant IGFBP-3 inhibits allergic lung inflammation, VEGF production, and vascular leak in a mouse model of asthma. Allergy 2012;67:869-877.
10. Jogie-Brahim S, Feldman D, Oh Y. Unraveling insulin-like growth factor binding protein-3 actions in human disease. Endocr Rev 2009;30:417-437.
11. Ingermann AR, Yang YF, Han J, Mikami A, Garza AE, Mohanraj L, Fan L, Idowu M, Ware JL, Kim HS, et al. Identification of a novel cell death receptor mediating IGFBP-3-induced anti-tumor effects in breast and prostate cancer. J Biol Chem 2010;285:30233-30246.
12. Spiess J, Rivier J, Vale W. Characterization of rat hypothalamic growth hormone-releasing factor. Nature 1983;303:532-535. (Pubitemid 13054622)
13. Kojima M, Hosoda H, Date Y, Nakazato M, Matsuo H, Kangawa K. Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 1999;402:656-660. (Pubitemid 129516334)
14. Butler AA, Le Roith D. Control of growth by the somatropic axis: growth hormone and the insulin-like growth factors have related and independent roles. Annu Rev Physiol 2001;63:141-164. (Pubitemid 32304315)
15. Brazeau P, Vale W, Burgus R, Ling N, Butcher M, Rivier J, Guillemin R. Hypothalamic polypeptide that inhibits the secretion of immunoreactive pituitary growth hormone. Science 1973;179:77-79.
16. Rinderknecht E, Humbel RE. The amino acid sequence of human insulin-like growth factor I and its structural homology with proinsulin. J Biol Chem 1978;253:2769-2776. (Pubitemid 8326483)
17. Bayne ML, Applebaum J, Underwood D, Chicchi GG, Green BG, Hayes NS, Cascieri MA. The C region of human insulin-like growth factor (IGF) I is required for high affinity binding to the type 1 IGF receptor. J Biol Chem 1989;264:11004-11008. (Pubitemid 19168823)
18. Brissenden JE, Ullrich A, Francke U. Human chromosomal mapping of genes for insulin-like growth factors I and II and epidermal growth factor. Nature 1984;310:781-784. (Pubitemid 14057658)
19. Smith TJ. Insulin-like growth factor-I regulation of immune function: a potential therapeutic target in autoimmune diseases? Pharmacol Rev 2010;62:199-236.
20. Adams TE, Epa VC, Garrett TP, Ward CW. Structure and function of the type 1 insulin-like growth factor receptor. Cell Mol Life Sci 2000;57:1050-1093. (Pubitemid 30598754)
21. LeRoith D, Werner H, Beitner-Johnson D, Roberts CT Jr. Molecular and cellular aspects of the insulin-like growth factor I receptor. Endocr Rev 1995;16:143-163.
22. Siddle K, Ursø B, Niesler CA, Cope DL, Molina L, Surinya KH, Soos MA. Specificity in ligand binding and intracellular signalling by insulin and insulin-like growth factor receptors. BiochemSoc Trans 2001;29:513-525. (Pubitemid 32783649)
23. Kato H, Faria TN, Stannard B, Roberts CT Jr, LeRoith D. Role of tyrosine kinase activity in signal transduction by the insulin-like growth factor-I (IGF-I) receptor: characterization of kinase-deficient IGF-I receptors and the action of an IGF-I-mimetic antibody (alpha IR-3). J Biol Chem 1993;268:2655-2661. (Pubitemid 23057892)
24. Craparo A, O'Neill TJ, Gustafson TA. Non-SH2 domains within insulin receptor substrate-1 and SHC mediate their phosphotyrosine-dependent interaction with the NPEY motif of the insulin-like growth factor I receptor. J Biol Chem 1995;270:15639-15643.
25. Dey BR, Frick K, Lopaczynski W, Nissley SP, Furlanetto RW. Evidence for the direct interaction of the insulin-like growth factor I receptor with IRS-1, Shc, and Grb10. Mol Endocrinol 1996;10:631-641. (Pubitemid 26176271)
26. Egan SE, Giddings BW, Brooks MW, Buday L, Sizeland AM, Weinberg RA. Association of Sos Ras exchange protein with Grb2 is implicated in tyrosine kinase signal transduction and transformation. Nature 1993;363:45-51. (Pubitemid 23144959)
27. Kecha O, Brilot F, Martens H, Franchimont N, Renard C, Greimers R, Defresne MP, Winkler R, Geenen V. Involvement of insulin-like growth factors in early T cell development: a study using fetal thymic organ cultures. Endocrinology 2000;141:1209-1217. (Pubitemid 32260464)
28. Myers MG Jr, Backer JM, Sun XJ, Shoelson S, Hu P, Schlessinger J, Yoakim M, Schaffhausen B, White MF. IRS-1 activates phosphatidylinositol 3′-kinase by associating with src homology 2 domains of p85. Proc Natl Acad Sci USA 1992;89:10350-10354.
29. Datta SR, Brunet A, Greenberg ME. Cellular survival: a play in three Akts. Genes Dev 1999;13:2905-2927.
30. Keegan AD, Nelms K, White M, Wang LM, Pierce JH, Paul WE. An IL-4 receptor region containing an insulin receptor motif is important for IL-4-mediated IRS-1 phosphorylation and cell growth. Cell 1994;76:811-820. (Pubitemid 24085319)
31. Sun XJ, Pons S, Wang LM, Zhang Y, Yenush L, Burks D, Myers MG Jr, Glasheen E, Copeland NG, Jenkins NA, et al. The IRS-2 gene on murine chromosome 8 encodes a unique signaling adapter for insulin and cytokine action. Mol Endocrinol 1997;11:251-262. (Pubitemid 27057438)
32. Zhou MM, Huang B, Olejniczak ET, Meadows RP, Shuker SB, Miyazaki M, Trüb T, Shoelson SE, Fesik SW. Structural basis for IL-4 receptor phosphopeptide recognition by the IRS-1 PTB domain. Nat Struct Biol 1996;3:388-393.
33. Braulke T. Type-2 IGF receptor: a multi-ligand binding protein. Horm Metab Res 1999;31:242-246. (Pubitemid 29169502)
34. Domené HM, Bengolea SV, Jasper HG, Boisclair YR. Acid-labile subunit deficiency: phenotypic similarities and differences between human and mouse. J Endocrinol Invest 2005;28(5 Suppl):43-46. (Pubitemid 46211840)
35. Twigg SM, Baxter RC. Insulin-like growth factor (IGF)-binding protein 5 forms an alternative ternary complex with IGFs and the acid-labile subunit. J Biol Chem 1998;273:6074-6079. (Pubitemid 28144686)
36. Baxter RC. Insulin-like growth factor binding proteins in the human circulation: a review. Horm Res 1994;42:140-144. (Pubitemid 24336141)
37. Wetterau LA, Moore MG, Lee KW, Shim ML, Cohen P. Novel aspects of the insulin-like growth factor binding proteins. Mol Genet Metab 1999;68:161-181. (Pubitemid 29501088)
38. Jones JI, Clemmons DR. Insulin-like growth factors and their binding proteins: biological actions. Endocr Rev 1995;16:3-34.
39. Fu P, Thompson JA, Bach LA. Promotion of cancer cell migration: an insulin-like growth factor (IGF)-independent action of IGF-binding protein-6. J Biol Chem 2007;282:22298-22306. (Pubitemid 47267353)
40. Granata R, Trovato L, Garbarino G, Taliano M, Ponti R, Sala G, Ghidoni R, Ghigo E. Dual effects of IGFBP-3 on endothelial cell apoptosis and survival: involvement of the sphingolipid signaling pathways. FASEB J 2004;18:1456-1458. (Pubitemid 39561613)
41. Kim JH, Choi DS, Lee OH, Oh SH, Lippman SM, Lee HY. Antiangiogenic antitumor activities of IGFBP-3 are mediated by IGF-independent suppression of Erk1/2 activation and Egr-1-mediated transcriptional events. Blood 2011;118:2622-2631.
42. Chang KH, Chan-Ling T, McFarland EL, Afzal A, Pan H, Baxter LC, Shaw LC, Caballero S, Sengupta N, Li Calzi S, et al. IGF binding protein-3 regulates hematopoietic stem cell and endothelial precursor cell function during vascular development. Proc Natl Acad Sci USA 2007;104:10595-10600. (Pubitemid 47185710)
43. Lofqvist C, Chen J, Connor KM, Smith AC, Aderman CM, Liu N, Pintar JE, Ludwig T, Hellstrom A, Smith LE. IGFBP3 suppresses retinopathy through suppression of oxygen-induced vessel loss and promotion of vascular regrowth. Proc Natl Acad Sci USA 2007;104:10589-10594. (Pubitemid 47185709)
44. Veraldi KL, Feghali-Bostwick CA. Insulin-like growth factor binding proteins-3 and -5: central mediators of fibrosis and promising new therapeutic targets. Open Rheumatol J 2012;6:140-145.
45. Allander SV, Bajalica S, Larsson C, Luthman H, Powell DR, Stern I, Weber G, Zazzi H, Ehrenborg E. Structure and chromosomal localization of human insulin-like growth factor-binding protein genes. Growth Regul 1993;3:3-5. (Pubitemid 23131718)
46. Imai Y, Moralez A, Andag U, Clarke JB, Busby WH Jr, Clemmons DR. Substitutions for hydrophobic amino acids in the N-terminal domains of IGFBP-3 and -5 markedly reduce IGF-I binding and alter their biologic actions. J Biol Chem 2000;275:18188-18194. (Pubitemid 30414770)
47. Buckway CK, Wilson EM, Ahlsén M, Bang P, Oh Y, Rosenfeld RG. Mutation of three critical amino acids of the N-terminal domain of IGF-binding protein-3 essential for high affinity IGF binding. J Clin Endocrinol Metab 2001;86:4943-4950. (Pubitemid 33020546)
48. Lalou C, Lassarre C, Binoux M. A proteolytic fragment of insulin-like growth factor (IGF) binding protein-3 that fails to bind IGFs inhibits the mitogenic effects of IGF-I and insulin. Endocrinology 1996;137:3206-3212. (Pubitemid 26250165)
49. Salahifar H, Firth SM, Baxter RC, Martin JL. Characterization of an amino-terminal fragment of insulin-like growth factor binding protein-3 and its effects in MCF-7 breast cancer cells. Growth Horm IGF Res 2000;10:367-377. (Pubitemid 32125108)
50. Firth SM, Baxter RC. Cellular actions of the insulin-like growth factor binding proteins. Endocr Rev 2002;23:824-854. (Pubitemid 35454590)
51. Spencer EM, Chan K. A 3-dimensional model for the insulin-like growth factor binding proteins (IGFBPs); supporting evidence using the structural determinants of the IGF binding site on IGFBP-3. Prog Growth Factor Res 1995;6:209-214.
52. Ho PJ, Baxter RC. Characterization of truncated insulin-like growth factor-binding protein-2 in human milk. Endocrinology 1997;138:3811-3818. (Pubitemid 27351934)
53. Devi GR, Yang DH, Rosenfeld RG, Oh Y. Differential effects of insulin-like growth factor (IGF)-binding protein-3 and its proteolytic fragments on ligand binding, cell surface association, and IGF-I receptor signaling. Endocrinology 2000;141:4171-4179.
54. Campbell PG, Durham SK, Hayes JD, Suwanichkul A, Powell DR. Insulin-like growth factor-binding protein-3 binds fibrinogen and fibrin. J Biol Chem 1999;274:30215-30221.
55. Campbell PG, Durham SK, Suwanichkul A, Hayes JD, Powell DR. Plasminogen binds the heparin-binding domain of insulin-like growth factor-binding protein-3. Am J Physiol 1998;275:E321-E331.
56. Fowlkes JL, Serra DM. Characterization of glycosaminoglycan-binding domains present in insulin-like growth factor-binding protein-3. J Biol Chem 1996;271:14676-14679.
57. Smith EP, Lu L, Chernausek SD, Klein DJ. Insulin-like growth factor-binding protein-3 (IGFBP-3) concentration in rat Sertoli cell-conditioned medium is regulated by a pathway involving association of IGFBP-3 with cell surface proteoglycans. Endocrinology 1994;135:359-364. (Pubitemid 24203838)
58. Zhu W, Shiojima I, Ito Y, Li Z, Ikeda H, Yoshida M, Naito AT, Nishi J, Ueno H, Umezawa A, et al. IGFBP-4 is an inhibitor of canonical Wnt signalling required for cardiogenesis. Nature 2008;454:345-349.
59. Schedlich LJ, Le Page SL, Firth SM, Briggs LJ, Jans DA, Baxter RC. Nuclear import of insulin-like growth factor-binding protein-3 and -5 is mediated by the importin beta subunit. J Biol Chem 2000;275:23462-23470. (Pubitemid 30624626)
60. Singh B, Charkowicz D, Mascarenhas D. Insulin-like growth factor-independent effects mediated by a C-terminal metal-binding domain of insulin-like growth factor binding protein-3. J Biol Chem 2004;279:477-487. (Pubitemid 38044849)
61. Liao L, Dearth RK, Zhou S, Britton OL, Lee AV, Xu J. Liver-specific overexpression of the insulin-like growth factor-I enhances somatic growth and partially prevents the effects of growth hormone deficiency. Endocrinology 2006;147:3877-3888. (Pubitemid 44079393)
62. DiGirolamo DJ, Mukherjee A, Fulzele K, Gan Y, Cao X, Frank SJ, Clemens TL. Mode of growth hormone action in osteoblasts. J Biol Chem 2007;282:31666-31674. (Pubitemid 350044902)
63. Phillips LS, Pao CI, Villafuerte BC. Molecular regulation of insulin-like growth factor-I and its principal binding protein, IGFBP-3. Prog Nucleic Acid Res Mol Biol 1998;60:195-265.
64. Albiston AL, Saffery R, Herington AC. Cloning and characterization of the promoter for the rat insulin-like growth factor-binding protein-3 gene. Endocrinology 1995;136:696-704.
65. Olivecrona H, Hilding A, Ekström C, Barle H, Nyberg B, Möller C, Delhanty PJ, Baxter RC, Angelin B, Ekström TJ, et al. Acute and short-term effects of growth hormone on insulin-like growth factors and their binding proteins: serum levels and hepatic messenger ribonucleic acid responses in humans. J Clin Endocrinol Metab 1999;84:553-560. (Pubitemid 29075683)
66. Paolisso G, Ammendola S, Del Buono A, Gambardella A, Riondino M, Tagliamonte MR, Rizzo MR, Carella C, Varricchio M. Serum levels of insulin-like growth factor-I (IGF-I) and IGF-binding protein-3 in healthy centenarians: relationship with plasma leptin and lipid concentrations, insulin action, and cognitive function. J Clin Endocrinol Metab 1997;82:2204-2209. (Pubitemid 27287585)
67. Marzullo P, Di Somma C, Pratt KL, Khosravi J, Diamandis A, Lombardi G, Colao A, Rosenfeld RG. Usefulness of different biochemical markers of the insulin-like growth factor (IGF) family in diagnosing growth hormone excess and deficiency in adults. J Clin Endocrinol Metab 2001;86:3001-3008. (Pubitemid 32673456)
68. Arosio M, Garrone S, Bruzzi P, Faglia G, Minuto F, Barreca A. Diagnostic value of the acid-labile subunit in acromegaly: evaluation in comparison with insulin-like growth factor (IGF) I, and IGF-binding protein-1, -2, and -3. J Clin Endocrinol Metab 2001;86:1091-1098. (Pubitemid 32322987)
69. Kanzaki S, Baxter RC, Knutsen R, Baylink DJ, Mohan S. Evidence that human bone cells in culture secrete insulin-like growth factor (IGF)-II and IGF binding protein-3 but not acid-labile subunit both under basal and regulated conditions. J Bone Miner Res 1995;10:854-858.
70. Olney RC, Wilson DM, Mohtai M, Fielder PJ, Smith RL. Interleukin-1 and tumor necrosis factor-alpha increase insulin-like growth factor-binding protein-3 (IGFBP-3) production and IGFBP-3 protease activity in human articular chondrocytes. J Endocrinol 1995;146:279-286.
71. Besset V, Le Magueresse-Battistoni B, Collette J, Benahmed M. Tumor necrosis factor alpha stimulates insulin-like growth factor binding protein 3 expression in cultured porcine Sertoli cells. Endocrinology 1996;137:296-303.
72. Oh Y, Müller HL, Ng L, Rosenfeld RG. Transforming growth factor-beta-induced cell growth inhibition in human breast cancer cells is mediated through insulin-like growth factor-binding protein-3 action. J Biol Chem 1995;270:13589-13592.
73. Gucev ZS, Oh Y, Kelley KM, Rosenfeld RG. Insulin-like growth factor binding protein 3 mediates retinoic acid- and transforming growth factor beta2-induced growth inhibition in human breast cancer cells. Cancer Res 1996;56:1545-1550. (Pubitemid 26104017)
74. Martin JL, Ballesteros M, Baxter RC. Insulin-like growth factor-I (IGF-I) and transforming growth factor-beta 1 release IGF-binding protein-3 from human fibroblasts by different mechanisms. Endocrinology 1992;131:1703-1710.
75. Conover CA, Clarkson JT, Bale LK. Effect of glucocorticoid on insulin-like growth factor (IGF) regulation of IGF-binding protein expression in fibroblasts. Endocrinology 1995;136:1403-1410.
76. Nickerson T, Huynh H. Vitamin D analogue EB1089-induced prostate regression is associated with increased gene expression of insulin-like growth factor binding proteins. J Endocrinol 1999;160:223-229. (Pubitemid 29074692)
77. Huynh H, Yang X, Pollak M. Estradiol and antiestrogens regulate a growth inhibitory insulin-like growth factor binding protein 3 autocrine loop in human breast cancer cells. J Biol Chem 1996;271:1016-1021. (Pubitemid 26034960)
78. Nickerson T, Pollak M. Bicalutamide (Casodex)-induced prostate regression involves increased expression of genes encoding insulin-like growth factor binding proteins. Urology 1999;54:1120-1125.
79. Buckbinder L, Talbott R, Velasco-Miguel S, Takenaka I, Faha B, Seizinger BR, Kley N. Induction of the growth inhibitor IGF-binding protein 3 by p53. Nature 1995;377:646-649.
80. Yi HK, Kim SY, Hwang PH, Kim CY, Yang DH, Oh Y, Lee DY. Impact of PTEN on the expression of insulin-like growth factors (IGFs) and IGF-binding proteins in human gastric adenocarcinoma cells. Biochem Biophys Res Commun 2005;330:760-767. (Pubitemid 40462152)
81. Tomii K, Tsukuda K, Toyooka S, Dote H, Hanafusa T, Asano H, Naitou M, Doihara H, Kisimoto T, Katayama H, et al. Aberrant promoter methylation of insulin-like growth factor binding protein-3 gene in human cancers. Int J Cancer 2007;120:566-573. (Pubitemid 44969028)
82. Wiley A, Katsaros D, Fracchioli S, Yu H. Methylation of the insulin-like growth factor binding protein-3 gene and prognosis of epithelial ovarian cancer. Int J Gynecol Cancer 2006;16:210-218.
83. Ibanez de Caceres I, Dulaimi E, Hoffman AM, Al-Saleem T, Uzzo RG, Cairns P. Identification of novel target genes by an epigenetic reactivation screen of renal cancer. Cancer Res 2006;66:5021-5028. (Pubitemid 43844922)
84. Hanafusa T, Yumoto Y, Nouso K, Nakatsukasa H, Onishi T, Fujikawa T, Taniyama M, Nakamura S, Uemura M, Takuma Y, et al. Reduced expression of insulin-like growth factor binding protein-3 and its promoter hypermethylation in human hepatocellular carcinoma. Cancer Lett 2002;176:149-158. (Pubitemid 34136014)
85. Harada A, Jogie-Brahim S, Oh Y. Tobacco specific carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone suppresses a newly identified anti-tumor IGFBP-3/IGFBP-3R system in lung cancer cells. Lung Cancer 2013;80:270-277.
86. Walker GE, Wilson EM, Powell D, Oh Y. Butyrate, a histone deacetylase inhibitor, activates the human IGF binding protein-3 promoter in breast cancer cells: molecular mechanism involves an Sp1/Sp3 multiprotein complex. Endocrinology 2001;142:3817-3827. (Pubitemid 32802652)
87. Chun SY, Chen F, Washburn JG, MacDonald JW, Innes KL, Zhao R, Cruz-Correa MR, Dang LH, Dang DT. CDX2 promotes anchorage-independent growth by transcriptional repression of IGFBP-3. Oncogene 2007;26:4725-4729. (Pubitemid 47067405)
88. Prieur A, Tirode F, Cohen P, Delattre O. EWS/FLI-1 silencing and gene profiling of Ewing cells reveal downstream oncogenic pathways and a crucial role for repression of insulin-like growth factor binding protein 3. Mol Cell Biol 2004;24:7275-7283. (Pubitemid 39014452)
89. Benini S, Zuntini M, Manara MC, Cohen P, Nicoletti G, Nanni P, Oh Y, Picci P, Scotlandi K. Insulin-like growth factor binding protein 3 as an anticancer molecule in Ewing's sarcoma. Int J Cancer 2006;119:1039-1046. (Pubitemid 44116910)
90. Conover CA, Powell DR. Insulin-like growth factor (IGF)-binding protein-3 blocks IGF-I-induced receptor down-regulation and cell desensitization in cultured bovine fibroblasts. Endocrinology 1991;129:710-716.
91. Martin JL, Weenink SM, Baxter RC. Insulin-like growth factor-binding protein-3 potentiates epidermal growth factor action in MCF-10A mammary epithelial cells: involvement of p44/42 and p38 mitogen-activated protein kinases. J Biol Chem 2003;278:2969-2976. (Pubitemid 36801203)
92. Butt AJ, Martin JL, Dickson KA, McDougall F, Firth SM, Baxter RC. Insulin-like growth factor binding protein-3 expression is associated with growth stimulation of T47D human breast cancer cells: the role of altered epidermal growth factor signaling. J Clin Endocrinol Metab 2004;89:1950-1956. (Pubitemid 38507956)
93. Pilewski JM, Liu L, Henry AC, Knauer AV, Feghali-Bostwick CA. Insulin-like growth factor binding proteins 3 and 5 are overexpressed in idiopathic pulmonary fibrosis and contribute to extracellular matrix deposition. Am J Pathol 2005;166:399-407. (Pubitemid 40189037)
94. Chan SS, Schedlich LJ, Twigg SM, Baxter RC. Inhibition of adipocyte differentiation by insulin-like growth factor-binding protein-3. Am J Physiol Endocrinol Metab 2009;296:E654-E663.
95. Mohanraj L, Kim HS, Li W, Cai Q, Kim KE, Shin HJ, Lee YJ, Lee WJ, Kim JH, Oh Y. IGFBP-3 inhibits cytokine-induced insulin resistance and early manifestations of atherosclerosis. PLoS ONE 2013;8:e55084.
96. Han J, Jogie-Brahim S, Harada A, Oh Y. Insulin-like growth factor-binding protein-3 suppresses tumor growth via activation of caspase-dependent apoptosis and cross-talk with NF-κB signaling. Cancer Lett 2011;307:200-210.
97. Lee KS, Park SJ, Kim SR, Min KH, Lee KY, Choe YH, Hong SH, Lee YR, Kim JS, Hong SJ, et al. Inhibition of VEGF blocks TGF-beta1 production through a PI3K/Akt signalling pathway. Eur Respir J 2008;31:523-531.
98. Cohen P, Noveral JP, Bhala A, Nunn SE, Herrick DJ, Grunstein MM. Leukotriene D4 facilitates airway smooth muscle cell proliferation via modulation of the IGF axis. Am J Physiol 1995;269:L151-L157.
99. Noveral JP, Bhala A, Hintz RL, Grunstein MM, Cohen P. Insulin-like growth factor axis in airway smooth muscle cells. Am J Physiol 1994;267:L761-L765.
100. Gosens R, Schaafsma D, Grootte Bromhaar MM, Vrugt B, Zaagsma J, Meurs H, Nelemans SA. Growth factor-induced contraction of human bronchial smooth muscle is Rho-kinase-dependent. Eur J Pharmacol 2004;494:73-76. (Pubitemid 38759833)
101. Rajah R, Nunn SE, Herrick DJ, Grunstein MM, Cohen P. Leukotriene D4 induces MMP-1, which functions as an IGFBP protease in human airway smooth muscle cells. Am J Physiol 1996;271:L1014-L1022.
102. Kawaguchi M, Fujita J, Kokubu F, Ohara G, Huang SK, Matsukura S, Ishii Y, Adachi M, Satoh H, Hizawa N. Induction of insulin-like growth factor-I by interleukin-17F in bronchial epithelial cells. Clin Exp Allergy 2010;40:1036-1043.
103. Kim SR, Lee KS, Park SJ, Min KH, Lee KY, Choe YH, Lee YR, Kim JS, Hong SJ, Lee YC. PTEN down-regulates IL-17 expression in a murine model of toluene diisocyanate-induced airway disease. J Immunol 2007;179:6820-6829.
104. Park SJ, Lee KS, Kim SR, Min KH, Choe YH, Moon H, Chae HJ, Yoo WH, Lee YC. Peroxisome proliferator-activated receptor gamma agonist down-regulates IL-17 expression in a murine model of allergic airway inflammation. J Immunol 2009;183:3259-3267.
105. H-Zadeh AM, Collard TJ, Malik K, Hicks DJ, Paraskeva C, Williams AC. Induction of apoptosis by the 16-kDa amino-terminal fragment of the insulin-like growth factor binding protein 3 in human colonic carcinoma cells. Int J Oncol 2006;29:1279-1286.
106. Williams AC, Smartt H, H-Zadeh AM, Macfarlane M, Paraskeva C, Collard TJ. Insulin-like growth factor binding protein 3 (IGFBP-3) potentiates TRAIL-induced apoptosis of human colorectal carcinoma cells through inhibition of NF-kappaB. Cell Death Differ 2007;14:137-145. (Pubitemid 44911901)
107. Lee CG, Link H, Baluk P, Homer RJ, Chapoval S, Bhandari V, Kang MJ, Cohn L, Kim YK, McDonald DM, et al. Vascular endothelial growth factor (VEGF) induces remodeling and enhances Th2-mediated sensitization and inflammation in the lung. Nat Med 2004;10:1095-1103. (Pubitemid 39424871)
108. Holgate ST, Lackie PM, Howarth PH, Roche WR, Puddicombe SM, Richter A, Wilson SJ, Holloway JW, Davies DE. Invited lecture: activation of the epithelial mesenchymal trophic unit in the pathogenesis of asthma. Int Arch Allergy Immunol 2001;124:253-258. (Pubitemid 32304819)
109. Roudabush FL, Pierce KL, Maudsley S, Khan KD, Luttrell LM. Transactivation of the EGF receptor mediates IGF-1-stimulated shc phosphorylation and ERK1/2 activation in COS-7 cells. J Biol Chem 2000;275:22583-22589. (Pubitemid 30621851)
110. Takeyama K, Dabbagh K, Lee HM, Agustí C, Lausier JA, Ueki IF, Grattan KM, Nadel JA. Epidermal growth factor system regulates mucin production in airways. Proc Natl Acad Sci USA 1999;96:3081-3086. (Pubitemid 29148847)
111. Young HW, Williams OW, Chandra D, Bellinghausen LK, Pérez G, Suárez A, Tuvim MJ, Roy MG, Alexander SN, Moghaddam SJ, et al. Central role of Muc5ac expression in mucous metaplasia and its regulation by conserved 59 elements. Am J Respir Cell Mol Biol 2007;37:273-290. (Pubitemid 350067607)
112. Wan H, Kaestner KH, Ang SL, Ikegami M, Finkelman FD, Stahlman MT, Fulkerson PC, Rothenberg ME, Whitsett JA. Foxa2 regulates alveolarization and goblet cell hyperplasia. Development 2004;131:953-964. (Pubitemid 38263209)
113. Desbois-Mouthon C, Cadoret A, Blivet-Van Eggelpoël MJ, Bertrand F, Cherqui G, Perret C, Capeau J. Insulin and IGF-1 stimulate the beta-catenin pathway through two signalling cascades involving GSK-3beta inhibition and Ras activation. Oncogene 2001;20:252-259. (Pubitemid 32150270)
114. Mucenski ML, Nation JM, Thitoff AR, Besnard V, Xu Y, Wert SE, Harada N, Taketo MM, Stahlman MT, Whitsett JA. Beta-catenin regulates differentiation of respiratory epithelial cells in vivo. Am J Physiol Lung Cell Mol Physiol 2005;289:L971-L979. (Pubitemid 41681332)
115. Lee YC, Lee HK. Vascular endothelial growth factor in patients with acute asthma. J Allergy Clin Immunol 2001;107:1106-1108.
116. Asai K, Kanazawa H, Otani K, Shiraishi S, Hirata K, Yoshikawa J. Imbalance between vascular endothelial growth factor and endostatin levels in induced sputum from asthmatic subjects. J Allergy Clin Immunol 2002;110:571-575. (Pubitemid 35178791)
117. Lee KY, Lee KS, Park SJ, Kim SR, Min KH, Choe YH, Lee YC. Clinical significance of plasma and serum vascular endothelial growth factor in asthma. J Asthma 2008;45:735-739.
118. Lee KS, Min KH, Kim SR, Park SJ, Park HS, Jin GY, Lee YC. Vascular endothelial growth factor modulates matrix metalloproteinase-9 expression in asthma. Am J Respir Crit Care Med 2006;174:161-170.
119. Kim SR, Lee KS, Park SJ, Jeon MS, Lee YC. Inhibition of p38 MAPK reduces expression of vascular endothelial growth factor in allergic airway disease. J Clin Immunol 2012;32:574-586.
120. Kim SR, Lee KS, Park HS, Park SJ, Min KH, Moon H, Puri KD, Lee YC. HIF-1α inhibition ameliorates an allergic airway disease via VEGF suppression in bronchial epithelium. Eur J Immunol 2010;40:2858-2869.
121. Lee KS, Kim SR, Park SJ, Min KH, Lee KY, Choe YH, Park SY, Chai OH, Zhang X, Song CH, et al. Mast cells can mediate vascular permeability through regulation of the PI3K-HIF-1α-VEGF axis. Am J Respir Crit Care Med 2008;178:787-797.
122. Lee KS, Kim SR, Park SJ, Park HS, Min KH, Lee MH, Jin SM, Jin GY, Yoo WH, Lee YC. Hydrogen peroxide induces vascular permeability via regulation of vascular endothelial growth factor. Am J Respir Cell Mol Biol 2006;35:190-197. (Pubitemid 44175318)
123. Ozkan EE. Plasma and tissue insulin-like growth factor-I receptor (IGF-IR) as a prognostic marker for prostate cancer and anti-IGF-IR agents as novel therapeutic strategy for refractory cases: a review. Mol Cell Endocrinol 2011;344:1-24.
124. Yee D. Insulin-like growth factor receptor inhibitors: baby or the bathwater? J Natl Cancer Inst 2012;104:975-981.
125. Gao J, Chesebrough JW, Cartlidge SA, Ricketts SA, Incognito L, Veldman-Jones M, Blakey DC, Tabrizi M, Jallal B, Trail PA, et al. Dual IGF-I/II-neutralizing antibody MEDI-573 potently inhibits IGF signaling and tumor growth. Cancer Res 2011;71:1029-1040.
126. Scagliotti GV, Novello S. The role of the insulin-like growth factor signaling pathway in non-small cell lung cancer and other solid tumors. Cancer Treat Rev 2012;38:292-302.
127. Youngman O. Patent application: methods and compositions for the treatment of metabolic syndrome, obstructive respiratory disorders, cancer and related diseases (WO/2012/166158). Richmond, VA: Biocure Pharma, LLC; 2012. PCT/US2011/043061.
128. Wittman MD, Carboni JM, Yang Z, Lee FY, Antman M, Attar R, Balimane P, Chang C, Chen C, Discenza L, et al. Discovery of a 2,4-disubstituted pyrrolo[1,2-f][1,2,4]triazine inhibitor (BMS-754807) of insulin-like growth factor receptor (IGF-1R) kinase in clinical development. J Med Chem 2009;52:7360-7363.
129. Carboni JM, Wittman M, Yang Z, Lee F, Greer A, Hurlburt W, Hillerman S, Cao C, Cantor GH, Dell-John J, et al. BMS-754807, a small molecule inhibitor of insulin-like growth factor-1R/IR. Mol Cancer Ther 2009;8:3341-3349.
130. Tolcher AW, Sarantopoulos J, Patnaik A, Papadopoulos K, Lin CC, Rodon J, Murphy B, Roth B, McCaffery I, Gorski KS, et al. Phase I, pharmacokinetic, and pharmacodynamic study of AMG 479, a fully human monoclonal antibody to insulin-like growth factor receptor 1. J Clin Oncol 2009;27:5800-5807.
131. Murakami H, Doi T, Yamamoto N, Watanabe J, Boku N, Fuse N, Yoshino T, Ohtsu A, Otani S, Shibayama K, et al. Phase 1 study of ganitumab (AMG 479), a fully human monoclonal antibody against the insulin-like growth factor receptor type I (IGF1R), in Japanese patients with advanced solid tumors. Cancer Chemother Pharmacol 2012;70:407-414.
132. Naing A, Kurzrock R, Burger A, Gupta S, Lei X, Busaidy N, Hong D, Chen HX, Doyle LA, Heilbrun LK, et al. Phase I trial of cixutumumab combined with temsirolimus in patients with advanced cancer. Clin Cancer Res 2011;17:6052-6060.
133. Malempati S, Weigel B, Ingle AM, Ahern CH, Carroll JM, Roberts CT, Reid JM, Schmechel S, Voss SD, Cho SY, et al. Phase I/II trial and pharmacokinetic study of cixutumumab in pediatric patients with refractory solid tumors and Ewing sarcoma: a report from the Children's Oncology Group. J Clin Oncol 2012;30:256-262.
134. Weickhardt A, Doebele R, Oton A, Lettieri J, Maxson D, Reynolds M, Brown A, Jackson MK, Dy G, Adjei A, et al. A phase I/II study of erlotinib in combination with the anti-insulin-like growth factor-1 receptor monoclonal antibody IMC-A12 (cixutumumab) in patients with advanced non-small cell lung cancer. J Thorac Oncol 2012;7:419-426.
135. Naing A, LoRusso P, Fu S, Hong DS, Anderson P, Benjamin RS, Ludwig J, Chen HX, Doyle LA, Kurzrock R. Insulin growth factor-receptor (IGF-1R) antibody cixutumumab combined with the mTOR inhibitor temsirolimus in patients with refractory Ewing's sarcoma family tumors. Clin Cancer Res 2012;18:2625-2631.