STAT3-mediated IGF-2 secretion in the tumour microenvironment elicits innate resistance to anti-IGF-1R antibody

Nature Communications

Volumn 6, Issue , 2015, Pages

  Lee, Ji Sun ^a   Kang, Ju Hee ^b   Boo, Hye Jin ^a   Hwang, Su Jung ^c   Hong, Sungyoul ^a   Lee, Su Chan ^a   Park, Young Jun ^a   Chung, Tae Moon ^d   Youn, Hyewon ^d   Mi Lee, Seung ^a,e   Jae Kim, Byoung ^a,e   Chung, June Key ^d   Chung, Yeonseok ^a   William, William N ^f   Kee Shin, Young ^a   Lee, Hyo Jong ^c   Oh, Seung Hyun ^g   Lee, Ho Young ^a  

^a Seoul National University   (South Korea)

^b National Cancer Center   (South Korea)

^c Inje University   (South Korea)

^d Seoul National University Hospital   (South Korea)

^e Seoul National University Boramae Hospital   (South Korea)

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

^g Gachon University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; CANCER; CELLS AND CELL COMPONENTS; DRUG RESISTANCE; GENE EXPRESSION; RODENT; SECRETION; TUMOR;

MUS;

ANTI-IGF-1R ANTIBODY A12; INTERLEUKIN 8; MONOCLONAL ANTIBODY; SOMATOMEDIN B; SOMATOMEDIN B RECEPTOR; SOMATOMEDIN C RECEPTOR; STAT3 PROTEIN;

ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; DRUG RESISTANCE; HUMAN; METABOLISM; MOUSE; NEOPLASMS, EXPERIMENTAL; NEOVASCULARIZATION (PATHOLOGY); NONOBESE DIABETIC MOUSE; NUCLEAR REPROGRAMMING; NUDE MOUSE; PARACRINE SIGNALING; SCID MOUSE; SECRETION (PROCESS); TUMOR CELL LINE; TUMOR INVASION; TUMOR MICROENVIRONMENT; UMBILICAL VEIN ENDOTHELIAL CELL;

ANIMALS; ANTIBODIES, MONOCLONAL; CELL LINE, TUMOR; CELLULAR REPROGRAMMING; DRUG RESISTANCE, NEOPLASM; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INSULIN-LIKE GROWTH FACTOR II; INTERLEUKIN-8; MICE; MICE, INBRED BALB C; MICE, INBRED NOD; MICE, NUDE; MICE, SCID; NEOPLASM INVASIVENESS; NEOPLASMS, EXPERIMENTAL; NEOVASCULARIZATION, PATHOLOGIC; PARACRINE COMMUNICATION; RECEPTOR, IGF TYPE 1; RECEPTOR, IGF TYPE 2; STAT3 TRANSCRIPTION FACTOR; TUMOR MICROENVIRONMENT;

EID: 84944474771     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms9499     Document Type: Article

References (67)

1. Gombos, A., Metzger-Filho, O., Dal Lago, L., Awada-Hussein, A. Clinical development of insulin-like growth factor receptor-1 (IGF-1R) inhibitors: at the crossroad? Invest. New Drugs 30, 2433-2442 (2012).
2. Gao, J., Chang, Y. S., Jallal, B., Viner, J. Targeting the insulin-like growth factor axis for the development of novel therapeutics in oncology. Cancer Res. 72, 3-12 (2012).
3. Patel, S. et al. A SARC global collaborative phase II trial of R1507, a recombinant human monoclonal antibody to the insulin-like growth factor-1 receptor (IGF1R) in patients with recurrent or refractory sarcomas. J. Clin. Oncol. 27, 15s 2009 (suppl; abstr 10503) (2009).
4. Malempati, S. 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. 30, 256-262 (2012).
5. Juergens, H. et al. Preliminary efficacy of the anti-insulin-like growth factor type 1 receptor antibody figitumumab in patients with refractory Ewing sarcoma. J. Clin. Oncol. 29, 4534-4540 (2011).
6. Ramalingam, S. S. et al. Randomized phase II study of erlotinib in combination with placebo or R1507, a monoclonal antibody to insulin-like growth factor-1 receptor, for advanced-stage non-small-cell lung cancer. J. Clin. Oncol. 29, 4574-4580 (2011).
7. Garofalo, C. et al. Efficacy of and resistance to anti-IGF-1R therapies in Ewing's sarcoma is dependent on insulin receptor signaling. Oncogene 30, 2730-2740 (2011).
8. Ulanet, D. B., Ludwig, D. L., Kahn, C. R., Hanahan, D. Insulin receptor functionally enhances multistage tumor progression and conveys intrinsic resistance to IGF-1R targeted therapy. Proc. Natl Acad. Sci. USA 107, 10791-10798 (2010).
9. Huang, F. et al. Differential mechanisms of acquired resistance to insulin-like growth factor-i receptor antibody therapy or to a small-molecule inhibitor, BMS-754807, in a human rhabdomyosarcoma model. Cancer Res. 70, 7221-7231 (2010).
10. Abraham, J. et al. Evasion mechanisms to Igf1r inhibition in rhabdomyosarcoma. Mol. Cancer Ther. 10, 697-707 (2011).
11. McKian, K. P., Haluska, P. Cixutumumab. Expert Opin. Invest. Drugs 18, 1025-1033 (2009).
12. Bissell, M. J., Hines, W. C. Why don't we get more cancer? A proposed role of the microenvironment in restraining cancer progression. Nat. Med. 17, 320-329 (2011).
13. Meads, M. B., Gatenby, R. A., Dalton, W. S. Environment-mediated drug resistance: a major contributor to minimal residual disease. Nat. Rev. Cancer 9, 665-674 (2009).
14. Straussman, R. et al. Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion. Nature 487, 500-504 (2012).
15. Wilson, T. R. et al. Widespread potential for growth-factor-driven resistance to anticancer kinase inhibitors. Nature 487, 505-509 (2012).
16. Joyce, J. A., Pollard, J. W. Microenvironmental regulation of metastasis. Nat. Rev. Cancer 9, 239-252 (2009).
17. Kalluri, R., Zeisberg, M. Fibroblasts in cancer. Nat. Rev. Cancer 6, 392-401 (2006).
18. Huang, W. H. et al. Mesenchymal stem cells promote growth and angiogenesis of tumors in mice. Oncogene 32, 4343-4354 (2013).
19. Karp LGP-A, D. D. et al. High activity of the anti-IGF-IR antibody CP-751,871 in combination with paclitaxel and carboplatin in squamous NSCLC. J. Clin. Oncol. (Meeting Abstracts) 26, 8015 (2008).
20. Schmitz, S. et al. Phase II study of figitumumab in patients with recurrent and/or metastatic squamous cell carcinoma of the head and neck: clinical activity and molecular response (GORTEC 2008-02). Ann. Oncol. 23, 2153-2161 (2012).
21. Ma, C. X. et al. A phase I trial of the IGF-1R antibody Cixutumumab in combination with temsirolimus in patients with metastatic breast cancer. Breast Cancer Res. Treat. 139, 145-153 (2013).
22. Okada, S., Harada, H., Ito, T., Saito, T., Suzu, S. Early development of human hematopoietic and acquired immune systems in new born NOD/Scid/Jak3null mice intrahepatic engrafted with cord blood-derived CD34 \+ cells. Int. J. Hematol. 88, 476-482 (2008).
23. Singh, A., Settleman, J. EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene 29, 4741-4751 (2010).
24. Voulgari, A., Pintzas, A. Epithelial-mesenchymal transition in cancer metastasis: mechanisms, markers and strategies to overcome drug resistance in the clinic. Biochim. Biophys. Acta 1796, 75-90 (2009).
25. Polyak, K., Weinberg, R. A. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat. Rev. Cancer 9, 265-273 (2009).
26. Mani, S. A. et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133, 704-715 (2008).
27. Paranjape, A. N. et al. Introduction of SV40ER and hTERT into mammospheres generates breast cancer cells with stem cell properties. Oncogene 31, 1896-1909 (2012).
28. Cirri, P., Chiarugi, P. Cancer-associated-fibroblasts and tumour cells: a diabolic liaison driving cancer progression. Cancer Metastasis Rev. 31, 195-208 (2012).
29. Bremnes, R. M. et al. The role of tumor stroma in cancer progression and prognosis: emphasis on carcinoma-associated fibroblasts and non-small cell lung cancer. J. Thorac. Oncol. 6, 209-217 (2011).
30. Weis, S. M., Cheresh, D. A. Tumor angiogenesis: molecular pathways and therapeutic targets. Nat. Med. 17, 1359-1370 (2011).
31. Kerbel, R. S. Tumor angiogenesis: past, present and the near future. Carcinogenesis 21, 505-515 (2000).
32. Wang, Y. H. et al. Vascular endothelial cells facilitated HCC invasion and metastasis through the Akt and NF-kappaB pathways induced by paracrine cytokines. J. Exp. Clin. Cancer Res. 32, 51 (2013).
33. Bid, H. K., Zhan, J., Phelps, D. A., Kurmasheva, R. T., Houghton, P. J. Potent inhibition of angiogenesis by the IGF-1 receptor-targeting antibody SCH717454 is reversed by IGF-2. Mol. Cancer Ther. 11, 649-659 (2012).
34. Shin, D. H. et al. Combating resistance to anti-IGFR antibody by targeting the integrin beta3-Src pathway. J. Natl Cancer Inst. 105, 1558-1570 (2013).
35. Singh, P., Dai, B., Given, R. L., Lu, X., Holthuizen, P. E. Differential activation of IGF-II promoters P3 and P4 in Caco-2 cells during growth and differentiation. Gastroenterology 114, 1221-1229 (1998).
36. von Horn, H. et al. GH is a regulator of IGF2 promoter-specific transcription in human liver. J. Endocrinol. 172, 457-465 (2002).
37. Garcia, R. et al. Constitutive activation of Stat3 by the Src and JAK tyrosine kinases participates in growth regulation of human breast carcinoma cells. Oncogene 20, 2499-2513 (2001).
38. Mitra, S. K., Hanson, D. A., Schlaepfer, D. D. Focal adhesion kinase: in command and control of cell motility. Nat. Rev. Mol. Cell Biol. 6, 56-68 (2005).
39. Lazennec, G., Richmond, A. Chemokines and chemokine receptors: new insights into cancer-related inflammation. Trends Mol. Med. 16, 133-144 (2010).
40. Heidemann, J. et al. Angiogenic effects of interleukin 8 (CXCL8) in human intestinal microvascular endothelial cells are mediated by CXCR2. J. Biol. Chem. 278, 8508-8515 (2003).
41. Hill, K.S. et al. Met receptor tyrosine kinase signaling induces secretion of the angiogenic chemokine interleukin-8/CXCL8 in pancreatic cancer. PLoS ONE 7, e40420 (2012).
42. Matsuo, Y. et al. CXCL8/IL-8 and CXCL12/SDF-1alpha co-operatively promote invasiveness and angiogenesis in pancreatic cancer. Int. J. Cancer 124, 853-861 (2009).
43. Wislez, M. et al. High expression of ligands for chemokine receptor CXCR2 in alveolar epithelial neoplasia induced by oncogenic kras. Cancer Res. 66, 4198-4207 (2006).
44. Maxwell, P. J., Neisen, J., Messenger, J., Waugh, D. J. Tumor-derived CXCL8 signaling augments stroma-derived CCL2-promoted proliferation and CXCL12-mediated invasion of PTEN-deficient prostate cancer cells. Oncotarget 5, 4895-4908 (2014).
45. Gales, D., Clark, C., Manne, U., Samuel, T. The chemokine CXCL8 in carcinogenesis and drug response. ISRN Oncol. 2013, 859154 (2013).
46. Agarwal, A. et al. Identification of a metalloprotease-chemokine signaling system in the ovarian cancer microenvironment: implications for antiangiogenic therapy. Cancer Res. 70, 5880-5890 (2010).
47. Li, A., Dubey, S., Varney, M. L., Dave, B. J., Singh, R. K. IL-8 directly enhanced endothelial cell survival, proliferation, and matrix metalloproteinases production and regulated angiogenesis. J. Immunol. 170, 3369-3376 (2003).
48. Qian, B. Z. et al. CCL2 recruits inflammatory monocytes to facilitate breasttumour metastasis. Nature 475, 222-225 (2011).
49. Hazlehurst, L. A., Landowski, T. H., Dalton, W. S. Role of the tumor microenvironment in mediating de novo resistance to drugs and physiological mediators of cell death. Oncogene 22, 7396-7402 (2003).
50. Shree, T. et al. Macrophages and cathepsin proteases blunt chemotherapeutic response in breast cancer. Genes Dev. 25, 2465-2479 (2011).
51. Sun, Y. et al. Treatment-induced damage to the tumor microenvironment promotes prostate cancer therapy resistance through WNT16B. Nat. Med. 18, 1359-1368 (2012).
52. Chung, A. S. et al. An interleukin-17-mediated paracrine network promotes tumor resistance to anti-angiogenic therapy. Nat. Med. 19, 1114-1123 (2013).
53. Langer, C. J. et al. Randomized, phase III trial of first-line figitumumab in combination with paclitaxel and carboplatin versus paclitaxel and carboplatin alone in patients with advanced non-small-cell lung cancer. J. Clin. Oncol. 32, 2059-2066 (2014).
54. Blouin, S., Basle, M. F., Chappard, D. Interactions between microenvironment and cancer cells in two animal models of bone metastasis. Br. J. Cancer 98, 809-815 (2008).
55. Zanella, E. R. et al. IGF2 is an actionable target that identifies a distinct subpopulation of colorectal cancer patients with marginal response to anti-EGFR therapies. Sci. Transl. Med. 7, 272-212 (2015).
56. Miller, M. D., Krangel, M. S. Biology and biochemistry of the chemokines: a family of chemotactic and inflammatory cytokines. Crit. Rev. Immunol. 12, 17-46 (1992).
57. Maeng, Y. S. et al. Endothelial progenitor cell homing: prominent role of the IGF2-IGF2R-PLCbeta2 axis. Blood 113, 233-243 (2009).
58. Groskopf, J. C., Syu, L. J., Saltiel, A. R., Linzer, D. I. Proliferin induces endothelial cell chemotaxis through a G protein-coupled, mitogen-activated protein kinase-dependent pathway. Endocrinology 138, 2835-2840 (1997).
59. Hawkes, C., Amritraj, A., Macdonald, R. G., Jhamandas, J. H., Kar, S. Heterotrimeric G proteins and the single-transmembrane domain IGF-II/M6P receptor: functional interaction and relevance to cell signaling. Mol. Neurobiol. 35, 329-345 (2007).
60. Matsunaga, H. et al. Activation of a calcium-permeable cation channel by insulin-like growth factor II in BALB/c 3T3 cells. Am. J. Physiol. 255, C442-C446 (1988).
61. Zhang, Q. et al. Insulin-like growth factor II signaling through the insulin-like growth factor II/mannose-6-phosphate receptor promotes exocytosis in insulin-secreting cells. Proc. Natl Acad. Sci. USA 94, 6232-6237 (1997).
62. Minniti, C. P. et al. The insulin-like growth factor II (IGF-II)/mannose 6-phosphate receptor mediates IGF-II-induced motility in human rhabdomyosarcoma cells. J. Biol. Chem. 267, 9000-9004 (1992).
63. El-Shewy, H. M. et al. Phospholipase C and protein kinase C-beta 2 mediate insulin-like growth factor II-dependent sphingosine kinase 1 activation. Mol. Endocrinol. 25, 2144-2156 (2011).
64. Waugh, D. J., Wilson, C. The interleukin-8 pathway in cancer. Clin. Cancer Res. 14, 6735-6741 (2008).
65. Douglas, I. S., Nicolls, M. R. Chemokine-mediated angiogenesis: an essential link in the evolution of airway fibrosis? J. Clin. Invest. 115, 1133-1136 (2005).
66. Sparmann, A., Bar-Sagi, D. Ras-induced interleukin-8 expression plays a critical role in tumor growth and angiogenesis. Cancer Cell 6, 447-458 (2004).
67. Wang, X., Crowe, P. J., Goldstein, D., Yang, J. L. STAT3 inhibition, a novel approach to enhancing targeted therapy in human cancers (review). Int. J. Oncol. 41, 1181-1191 (2012).