Regulation of hypoxia-inducible factor-1α, vascular endothelial growth factor, and angiogenesis by an insulin-like growth factor-I receptor autocrine loop in human pancreatic cancer

American Journal of Pathology

Volumn 163, Issue 3, 2003, Pages 1001-1011

  Stoeltzing, Oliver ^a   Liu, Wenbiao ^a   Reinmuth, Niels ^a   Fan, Fan ^a   Parikh, Alexander A ^a   Bucana, Corazon D ^a   Evans, Douglas B ^a   Semenza, Gregg L ^b   Ellis, Lee M ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MITOGEN ACTIVATED PROTEIN KINASE 1; SOMATOMEDIN C RECEPTOR; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOCRINE EFFECT; CANCER CELL CULTURE; CANCER GRAFT; CONTROLLED STUDY; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

EID: 0042926509     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0002-9440(10)63460-8     Document Type: Article

References (56)

1. Xie Y, Skytting B, Nilsson G, Brodin B, Larsson O: Expression of insulin-like growth factor-1 receptor in synovial sarcoma: association with an aggressive phenotype. Cancer Res 1999, 59:3588-3591
2. Hakam A, Yeatman TJ, Lu L, Mora L, Marcet G, Nicosia SV, Karl RC, Coppola D: Expression of insulin-like growth factor-1 receptor in human colorectal cancer. Hum Pathol 1999, 30:1128-1133
3. Long L, Rubin R, Brodt P: Enhanced invasion and liver colonization by lung carcinoma cells overexpressing the type 1 insulin-like growth factor receptor. Exp Cell Res 1998, 238:116-121
4. Bergmann U, Funatomi H, Yokoyama M, Beger HG, Korc M: Insulin-like growth factor I overexpression in human pancreatic cancer: evidence for autocrine and paracrine roles. Cancer Res 1995, 55:2007-2011
5. Basso D, Plebani M, Fogar P, Panozzo MP, Meggiato T, De Paoli M, Del Favero G: Insulin-like growth factor-I, interleukin-1 alpha and beta in pancreatic cancer: role in tumor invasiveness and associated diabetes. Int J Clin Lab Res 1995, 25:40-43
6. Parisot JP, Hu XF, DeLuise M, Zalcberg JR: Altered expression of the IGF-1 receptor in a tamoxifen-resistant human breast cancer cell line. Br J Cancer 1999, 79:693-700
7. Burtscher I, Compagni A, Lamm GM, Christofori G: An insulin-like growth factor-mediated, phosphatidylinositol 3′ kinase-independent survival signaling pathway in beta tumor cells. Cancer Res 1999, 59:3923-3926
8. Tanno S, Mitsuuchi Y, Altomare DA, Xiao GH, Testa JR: AKT activation up-regulates insulin-like growth factor I receptor expression and promotes invasiveness of human pancreatic cancer cells. Cancer Res 2001, 61:589-593
9. Baserga R, Hongo A, Rubini M, Prisco M, Valentinis B: The IGF-I receptor in cell growth, transformation and apoptosis. Biochim Biophys Acta 1997, 1332:F105-F126
10. Werner H, Le Roith D: The insulin-like growth factor-I receptor signaling pathways are important for tumorigenesis and inhibition of apoptosis. Crit Rev Oncog 1997, 8:71-92
11. Liu ZZ, Wada J, Alvares K, Kumar A, Wallner EI, Kanwar YS: Distribution and relevance of insulin-like growth factor-I receptor in metanephric development. Kidney Int 1993, 44:1242-1250
12. Steller MA, Delgado CH, Bartels CJ, Woodworth CD, Zou Z: Overexpression of the insulin-like growth factor-1 receptor and autocrine stimulation in human cervical cancer cells. Cancer Res 1996, 56:1761-1765
13. Cullen KJ, Yee D, Sly WS, Perdue J, Hampton B, Lippman ME, Rosen N: Insulin-like growth factor receptor expression and function in human breast cancer. Cancer Res 1990, 50:48-53
14. Ohmura E, Okada M, Onoda N, Kamiya Y, Murakami H, Tsushima T, Shizume K: Insulin-like growth factor I and transforming growth factor alpha as autocrine growth factors in human pancreatic cancer cell growth. Cancer Res 1990, 50:103-107
15. Freeman JW, Mattingly CA, Strodel WE: Increased tumorigenicity in the human pancreatic cell line MIA PaCa-2 is associated with an aberrant regulation of an IGF-1 autocrine loop and lack of expression of the TGF-beta type RII receptor. J Cell Physiol 1995, 165:155-163
16. Flossmann-Kast BB, Jehle PM, Hoeflich A, Adler G, Lutz MP: Src stimulates insulin-like growth factor I (IGF-I)-dependent cell proliferation by increasing IGF-I receptor number in human pancreatic carcinoma cells. Cancer Res 1998, 58:3551-3554
17. Nair PN, De Armond DT, Adamo ML, Strodel WE, Freeman JW: Aberrant expression and activation of insulin-like growth factor-1 receptor (IGF-1R) are mediated by an induction of IGF-1R promoter activity and stabilization of IGF-1R mRNA and contributes to growth factor independence and increased survival of the pancreatic cancer cell line MIA PaCa-2. Oncogene 2001, 20:8203-8214
18. Murphy LO, Abdel-Wahab YH, Wang QJ, Knezetic JA, Permnert J, Larsson J, Hollingsworth AM, Adrian TE: Receptors and ligands for autocrine growth pathways are up-regulated when pancreatic cancer cells are adapted to serum-free culture. Pancreas 2001, 22:293-298
19. Reinmuth N, Fan F, Liu W, Parikh AA, Stoeltzing O, Jung YD, Bucana CD, Radinsky R, Gallick GE, Ellis LM: Impact of insulin-like growth factor receptor-I function on angiogenesis, growth, and metastasis of colon cancer. Lab Invest 2002, 82:1377-1389
20. Reinmuth N, Liu W, Fan F, Jung YD, Ahmad SA, Stoeltzing O, Bucana CD, Radinsky R, Ellis LM: Blockade of insulin-like growth factor I receptor function inhibits growth and angiogenesis of colon cancer. Clin Cancer Res 2002, 8:3259-3269
21. Akagi Y, Liu W, Zebrowski B, Xie K, Ellis LM: Regulation of vascular endothelial growth factor expression in human colon cancer by insulin-like growth factor-I. Cancer Res 1998, 58:4008-4014
22. Warren RS, Yuan H, Matli MR, Ferrara N, Donner DB: Induction of vascular endothelial growth factor by insulin-like growth factor 1 in colorectal carcinoma. J Biol Chem 1996, 271:29483-29488
23. Wu Y, Yakar S, Zhao L, Hennighausen L, LeRoith D: Circulating insulin-like growth factor-I levels regulate colon cancer growth and metastasis. Cancer Res 2002, 62:1030-1035
24. Grant MB, Mames RN, Fitzgerald C, Ellis EA, Aboufriekha M, Guy J: Insulin-like growth factor I acts as an angiogenic agent in rabbit cornea and retina: comparative studies with basic fibroblast growth factor. Diabetologia 1993, 36:282-291
25. Smith LE, Shen W, Perruzzi C, Soker S, Kinose F, Xu X, Robinson G, Driver S, Bischoff J, Zhang B, Schaeffer JM, Senger DR: Regulation of vascular endothelial growth factor-dependent retinal neovascularization by insulin-like growth factor-1 receptor. Nat Med 1999, 5:1390-1395
26. Ellis LM, Fidler IJ: Angiogenesis and metastasis. Eur J Cancer 1996, 32A:2451-2460
27. Folkman J: The role of angiogenesis in tumor growth. Semin Cancer Biol 1992, 3:65-71
28. Fidler IJ, Ellis LM: The implications of angiogenesis for the biology and therapy of cancer metastasis. Cell 1994, 79:185-188
29. Tsuzuki Y, Mouta Carreira C, Bockhorn M, Xu L, Jain RK, Fukumura D: Pancreas microenvironment promotes VEGF expression and tumor growth: novel window models for pancreatic tumor angiogenesis and microcirculation. Lab Invest 2001, 81:1439-1451
30. Bruns CJ, Shrader M, Harbison MT, Portera C, Solorzano CC, Jauch KW, Hicklin DJ, Radinsky R, Ellis LM: Effect of the vascular endothelial growth factor receptor-2 antibody DC101 plus gemcitabine on growth, metastasis and angiogenesis of human pancreatic cancer growing orthotopically in nude mice. Int J Cancer 2002, 102:101-108
31. Solorzano CC, Baker CH, Bruns CJ, Killion JJ, Ellis LM, Wood J, Fidler IJ: Inhibition of growth and metastasis of human pancreatic cancer growing in nude mice by PTK 787/ZK222584, an inhibitor of the vascular endothelial growth factor receptor tyrosine kinases. Cancer Biother Radiopharm 2001, 16:359-370
32. Bruns CJ, Harbison MT, Kuniyasu H, Eue I, Fidler IJ: In vivo selection and characterization of metastatic variants from human pancreatic adenocarcinoma by using orthotopic implantation in nude mice. Neoplasia 1999, 1:50-62
33. Prager D, Yamasaki H, Weber MM, Gebremedhin S, Melmed S: Human insulin-like growth factor I receptor function in pituitary cells is suppressed by a dominant negative mutant. J Clin Invest 1992, 90:2117-2122
34. Prager D, Li HL, Asa S, Melmed S: Dominant negative inhibition of tumorigenesis in vivo by human insulin-like growth factor I receptor mutant. Proc Natl Acad Sci USA 1994, 91:2181-2185
35. Quinn KA, Treston AM, Unsworth EJ, Miller MJ, Vos M, Grimley C, Battey J, Mulshine JL, Cuttitta F: Insulin-like growth factor expression in human cancer cell lines. J Biol Chem 1996, 271:11477-11483
36. Jung YD, Liu W, Reinmuth N, Ahmad SA, Fan F, Galick GE, Ellis LM: Vascular endothelial growth factor is upregulated by interleukin-1 beta in human vascular smooth muscle cells via the P38 mitogen-activated protein kinase pathway. Angiogenesis 2001, 4:155-162
37. Ahmad SA, Liu W, Jung YD, Fan F, Wilson M, Reinmuth N, Shaheen RM, Bucana CD, Ellis LM: The effects of angiopoietin-1 and -2 on tumor growth and angiogenesis in human colon cancer. Cancer Res 2001, 61:1255-1259
38. Jung YD, Fan F, McConkey DJ, Jean ME, Liu W, Reinmuth N, Stoeltzing O, Ahmad SA, Parikh AA, Mukaida N, Ellis LM: Role of P38 MAPK, AP-1, and NF-kappaB in interleukin-1beta induced IL-8 expression in human vascular smooth muscle cells. Cytokine 2002, 18:206-213
39. Fukuda R, Hirota K, Fan F, Jung YD, Ellis LM, Semenza GL: Insulin-like growth factor 1 induces hypoxia-inducible factor 1-mediated vascular endothelial growth factor expression, which is dependent on MAP kinase and phosphatidylinositol 3-kinase signaling in colon cancer cells. J Biol Chem 2002, 277:38205-38211
40. Baker CH, Solorzano CC, Fidler IJ: Blockade of vascular endothelial growth factor receptor and epidermal growth factor receptor signaling for therapy of metastatic human pancreatic cancer. Cancer Res 2002, 62:1996-2003
41. Bruns CJ, Solorzano CC, Harbison MT, Ozawa S, Tsan R, Fan D, Abbruzzese J, Traxler P, Buchdunger E, Radinsky R, Fidler IJ: Blockade of the epidermal growth factor receptor signaling by a novel tyrosine kinase inhibitor leads to apoptosis of endothelial cells and therapy of human pancreatic carcinoma. Cancer Res 2000, 60:2926-2935
42. Fujiwaki R, Iida K, Kanasaki H, Ozaki T, Hata K, Miyazaki K: Cyclooxygenase-2 expression in endometrial cancer: correlation with microvessel count and expression of vascular endothelial growth factor and thymidine phosphorylase. Hum Pathol 2002, 33:213-219
43. Rubin R, Baserga R: Insulin-like growth factor-I receptor. Its role in cell proliferation, apoptosis, and tumorigenicity. Lab Invest 1995, 73:311-331
44. Oh JS, Kucab JE, Bushel PR, Martin K, Bennett L, Collins J, DiAugustine RP, Barrett JC, Afshari CA, Dunn SE: Insulin-like growth factor-1 inscribes a gene expression profile for angiogenic factors and cancer progression in breast epithelial cells. Neoplasia 2002, 4:204-217
45. Bermont L, Lamielle F, Fauconnet S, Esumi H, Weisz A, Adessi GL: Regulation of vascular endothelial growth factor expression by insulin-like growth factor-I in endometrial adenocarcinoma cells. Int J Cancer 2000, 85:117-123
46. Coppola D, Ferber A, Miura M, Sell C, D'Ambrosio C, Rubin R, Baserga R: A functional insulin-like growth factor I receptor is required for the mitogenic and transforming activities of the epidermal growth factor receptor. Mol Cell Biol 1994, 14:4588-4595
47. Bruns CJ, Harbison MT, Davis DW, Portera CA, Tsan R, McConkey DJ, Evans DB, Abbruzzese JL, Hicklin DJ, Radinsky R: Epidermal growth factor receptor blockade with C225 plus gemcitabine results in regression of human pancreatic carcinoma growing orthotopically in nude mice by antiangiogenic mechanisms. Clin Cancer Res 2000, 6:1936-1948
48. Zhong H, De Marzo AM, Laughner E, Lim M, Hilton DA, Zagzag D, Buechler P, Isaacs WB, Semenza GL, Simons JW: Overexpression of hypoxia-inducible factor 1alpha in common human cancers and their metastases. Cancer Res 1999, 59:5830-5835
49. Birner P, Gatterbauer B, Oberhuber G, Schindl M, Rossler K, Prodinger A, Budka H, Hainfellner JA: Expression of hypoxia-inducible factor-1 alpha in oligodendrogliomas: its impact on prognosis and on neoangiogenesis. Cancer 2001, 92:165-171
50. Carmeliet P, Dor Y, Herbert JM, Fukumura D, Brusselmans K, Dewerchin M, Neeman M, Bono F, Abramovitch F, Maxwell P, Koch CJ, Ratcliffe P, Moons L, Jain RK, Collen D, Keshert E, Keshet E: Role of HIF-1alpha in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature 1998, 394:485-490
51. Buchler P, Reber HA, Buchler M, Shrinkante S, Buchler MW, Friess H, Semenza GL, Hines OJ: Hypoxia-inducible factor 1 regulates vascular endothelial growth factor expression in human pancreatic cancer. Pancreas 2003, 26:56-64
52. Akakura N, Kobayashi M, Horiuchi I, Suzuki A, Wang J, Chen J, Niizeki H, Kawamura K, Hosokawa M, Asaka M: Constitutive expression of hypoxia-inducible factor-1alpha renders pancreatic cancer cells resistant to apoptosis induced by hypoxia and nutrient deprivation. Cancer Res 2001, 61:6548-6554
53. Feldser D, Agani F, Iyer NV, Pak B, Ferreira G, Semenza GL: Reciprocal positive regulation of hypoxia-inducible factor 1alpha and insulin-like growth factor 2. Cancer Res 1999, 59:3915-3918
54. Kim KW, Bae SK, Lee OH, Bae MH, Lee MJ, Park BC: Insulin-like growth factor II induced by hypoxia may contribute to angiogenesis of human hepatocellular carcinoma. Cancer Res 1998, 58:348-351
55. Ritter MR, Dorrell MI, Edmonds J, Friedlander SF, Friedlander M: Insulin-like growth factor 2 and potential regulators of hemangioma growth and involution identified by large-scale expression analysis. Proc Natl Acad Sci USA 2002, 99:7455-7460
56. Gallo O, Franchi A, Magnelli L, Sardi I, Vannacci A, Boddi V, Chiarugi V, Masini E: Cyclooxygenase-2 pathway correlates with VEGF expression in head and neck cancer Implications for tumor angiogenesis and metastasis. Neoplasia 2001, 3:53-61