Association between insulin-like growth factor-1 receptor (IGF1R) negativity and poor prognosis in a cohort of women with primary breast cancer

BMC Cancer

Volumn 14, Issue 1, 2014, Pages

  Aaltonen, Kristina E ^a   Rosendahl, Ann H ^a,b   Olsson, Hans ^c,d   Malmström, Per ^a,b   Hartman, Linda ^a,e   Fernö, Mårten ^a  

^a LUND UNIVERSITY   (Sweden)

^b LUND UNIVERSITY HOSPITAL   (Sweden)

^c Ostergotland County Council   (Sweden)

^d LINKÖPING UNIVERSITY   (Sweden)

^e South Swedish Regional   (Sweden)

Author keywords

Estrogen receptor; Insulin like growth factor 1 receptor; Primary breast cancer; Prognosis; Tamoxifen

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR; KI 67 ANTIGEN; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN S6; SOMATOMEDIN C RECEPTOR; TAMOXIFEN; BIOLOGICAL MARKER; TARGET OF RAPAMYCIN KINASE;

ADULT; ARTICLE; BREAST CANCER; CANCER PROGNOSIS; CANCER STAGING; CANCER SURVIVAL; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE FREE INTERVAL; DISTANT DISEASE FREE INTERVAL; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MIDDLE AGED; POSTMENOPAUSE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TISSUE MICROARRAY; TREATMENT DURATION; TUMOR VOLUME; AGED; BREAST NEOPLASMS; FOLLOW UP; INTRACELLULAR SPACE; LYMPH NODE METASTASIS; METABOLISM; MORTALITY; PATHOLOGY; PROGNOSIS; PROTEIN TRANSPORT;

ADULT; AGED; BIOLOGICAL MARKERS; BREAST NEOPLASMS; COHORT STUDIES; FEMALE; FOLLOW-UP STUDIES; HUMANS; INTRACELLULAR SPACE; LYMPHATIC METASTASIS; MIDDLE AGED; PROGNOSIS; PROTEIN TRANSPORT; RECEPTOR, IGF TYPE 1; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TUMOR BURDEN;

EID: 84920811592     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-14-794     Document Type: Article

References (42)

1. Osborne CK, Schiff R: Mechanisms of endocrine resistance in breast cancer. Annu Rev Med 2011, 62:233-237.
2. Mitsiades CS, Mitsiades NS, McMullan CJ, Poulaki V, Shringarpure R, Akiyama M, Hideshima T, Chauhan D, Joseph M, Libermann TA, Garcia-Echeverria C, Pearson MA, Hofmann F, Anderson KC, Kung AL: Inhibition of the insulin-like growth factor receptor-1 tyrosine kinase activity as a therapeutic strategy for multiple myeloma, other hematologic malignancies, and solid tumors. Cancer Cell 2004, 5:221-230.
3. Maor SB, Abramovitch S, Erdos MR, Brody LC, Werner H: BRCA1 suppresses insulin-like growth factor-I receptor promoter activity: potential interaction between BRCA1 and Sp1. Mol Genet Metab 2000, 69:130-136.
4. Levine AJ, Feng Z, Mak TW, You H, Jin S: Coordination and communication between the p53 and IGF-1-AKT-TOR signal transduction pathways. Genes Dev 2006, 20:267-275.
5. Werner H, Karnieli E, Rauscher FJ, LeRoith D: Wild-type and mutant p53 differentially regulate transcription of the insulin-like growth factor I receptor gene. Proc Natl Acad Sci U S A 1996, 93:8318-8323.
6. Lee AV, Jackson JG, Gooch JL, Hilsenbeck SG, Coronado-Heinsohn E, Osborne CK, Yee D: Enhancement of insulin-like growth factor signaling in human breast cancer: estrogen regulation of insulin receptor substrate-1 expression in vitro and in vivo. Mol Endocrinol 1999, 13:787-796.
7. Stewart AJ, Johnson MD, May FE, Westley BR: Role of insulin-like growth factors and the type I insulin-like growth factor receptor in the estrogenstimulated proliferation of human breast cancer cells. J Biol Chem 1990, 265:21172-21178.
8. Maruani DM, Spiegel TN, Harris EN, Shachter AS, Unger HA, Herrero-Gonzalez S, Holz MK: Estrogenic regulation of S6K1 expression creates a positive regulatory loop in control of breast cancer cell proliferation. Oncogene 2012, 31:5073-5080.
9. Fagan DH, Yee D: Crosstalk between IGF1R and estrogen receptor signaling in breast cancer. J Mammary Gland Biol Neoplasia 2008, 13:423-429.
10. Magnuson B, Ekim B, Fingar DC: Regulation and function of ribosomal protein S6 kinase (S6K) within mTOR signalling networks. Biochem J 2012, 441:1-21.
11. Chakraborty A, Welsh A, DiGiovanna M: Co-targeting the insulin-like growth factor I receptor enhances growth-inhibitory and pro-apoptotic effects of anti-estrogens in human breast cancer cell lines. Breast Cancer Res Treat 2010, 120:327-335.
12. Cavazzoni A, Bonelli MA, Fumarola C, La Monica S, Airoud K, Bertoni R, Alfieri RR, Galetti M, Tramonti S, Galvani E, Harris AL, Martin L-A, Andreis D, Bottini A, Generali D, Petronini PG: Overcoming acquired resistance to letrozole by targeting the PI3K/AKT/mTOR pathway in breast cancer cell clones. Cancer Lett 2012, 323:77-87.
13. Baselga J, Campone M, Piccart M, Burris HA, Rugo HS, Sahmoud T, Noguchi S, Gnant M, Pritchard KI, Lebrun F, Beck JT, Ito Y, Yardley D, Deleu I, Perez A, Bachelot T, Vittori L, Xu Z, Mukhopadhyay P, Lebwohl D, Hortobagyi GN: Everolimus in postmenopausal hormone-receptor-positive advanced breast cancer. N Engl J Med 2012, 366:520-529.
14. Bachelot T, Bourgier C, Cropet C, Ray-Coquard I, Ferrero JM, Freyer G, Abadie-Lacourtoisie S, Eymard JC, Debled M, Spaeth D, Legouffe E, Allouache D, El Kouri C, Pujade-Lauraine E: Randomized phase II trial of everolimus in combination with tamoxifen in patients with hormone receptor-positive, human epidermal growth factor receptor 2-negative metastatic breast cancer with prior exposure to aromatase inhibitors: a GINECO study. J Clin Oncol 2012, 30:2718-2724.
15. Ma CX, Suman VJ, Goetz M, Haluska P, Moynihan T, Nanda R, Olopade O, Pluard T, Guo Z, Chen HX, Erlichman C, Ellis MJ, Fleming GF: A phase I trial of the IGF-1R antibody Cixutumumab in combination with temsirolimus in patients with metastatic breast cancer. Breast Cancer Res Treat 2013, 139:145-153.
16. Law JH, Habibi G, Hu K, Masoudi H, Wang MYC, Stratford AL, Park E, Gee JMW, Finlay P, Jones HE, Nicholson RI, Carboni J, Gottardis M, Pollak M, Dunn SE: Phosphorylated insulin-like growth factor-I/Insulin receptor is present in all breast cancer subtypes and is related to poor survival. Cancer Res 2008, 68:10238-10246.
17. Peiro G, Adrover E, Sanchez-Tejada L, Lerma E, Planelles M, Sanchez-Paya J, Aranda FI, Giner D, Gutierrez-Avino FJ: Increased insulin-like growth factor-1 receptor mRNA expression predicts poor survival in immunophenotypes of early breast carcinoma. Mod Pathol 2011, 24:201-208.
18. Henriksen KL, Rasmussen BB, Lykkesfeldt AE, Møller S, Ejlertsen B, Mouridsen HT: An ER activity profile including ER, PR, Bcl-2 and IGF-IR may have potential as selection criterion for letrozole or tamoxifen treatment of patients with advanced breast cancer. Acta Oncol 2009, 48:522-531.
19. Yerushalmi R, Gelmon K, Leung S, Gao D, Cheang M, Pollak M, Turashvili G, Gilks B, Kennecke H: Insulin-like growth factor receptor (IGF-1R) in breast cancer subtypes. Breast Cancer Res Treat 2012, 132:131-142.
20. Kim JH, Cho YH, Park YL, Sohn JH, Kim HS: Prognostic significance of insulin growth factor-I receptor and insulin growth factor binding protein-3 expression in primary breast cancer. Oncol Rep 2010, 23:989-995.
21. Fu P, Ibusuki M, Yamamoto Y, Hayashi M, Murakami K, Zheng S, Iwase H: Insulin-like growth factor-1 receptor gene expression is associated with survival in breast cancer: a comprehensive analysis of gene copy number, mRNA and protein expression. Breast Cancer Res Treat 2011, 130:307-317.
22. Bakarakos P, Theohari I, Nomikos A, Mylona E, Papadimitriou C, Dimopoulos A-M, Nakopoulou L: Immunohistochemical study of PTEN and phosphorylated mTOR proteins in familial and sporadic invasive breast carcinomas. Histopathology 2010, 56:876-882.
23. Bose S, Chandran S, Mirocha JM, Bose N: The Akt pathway in human breast cancer: a tissue-array-based analysis. Mod Pathol 2005, 19:238-245.
24. Zhou X, Tan M, Stone Hawthorne V, Klos KS, Lan K-H, Yang Y, Yang W, Smith TL, Shi D, Yu D: Activation of the Akt/Mammalian target of rapamycin/ 4E-BP1 pathway by ErbB2 overexpression predicts tumor progression in breast cancers. Clin Cancer Res 2004, 10:6779-6788.
25. Bostner J, Karlsson E, Pandiyan MJ, Westman H, Skoog L, Fornander T, Nordenskjold B, Stal O: Activation of Akt, mTOR, and the estrogen receptor as a signature to predict tamoxifen treatment benefit. Breast Cancer Res Treat 2013, 137:397-406.
26. McShane L, Altman D, Sauerbrei W, Taube S, Gion M, Clark G: Reporting recommendations for tumor MARKer prognostic studies (REMARK). Breast Cancer Res Treat 2006, 100:229-235.
27. Rydén L, Jönsson P-E, Chebil G, Dufmats M, Fernö M, Jirström K, Källström A-C, Landberg G, Stål O, Thorstenson S, Nordenskjöld B: Two years of adjuvant tamoxifen in premenopausal patients with breast cancer: a randomised, controlled trial with long-term follow-up. Eur J Cancer 2005, 41:256-264.
28. Swedish Breast Cancer Cooperative Group: Randomized trial of two versus five years of adjuvant tamoxifen for postmenopausal early stage breast cancer. J Natl Cancer Inst 1996, 88:1543-1549.
29. Chebil G, Bendahl P-O, Idvall I, Fernö M: Comparison of immunohistochemical and biochemical assay of steroid receptors in primary breast cancer. Acta Oncol 2003, 42:719-725.
30. Strand C, Bak M, Borgquist S, Chebil G, Falck AK, Fjallskog ML, Grabau D, Hedenfalk I, Jirstrom K, Klintman M, Malmstrom P, Olsson H, Ryden L, Stal O, Bendahl PO, Ferno M: The combination of Ki67, histological grade and estrogen receptor status identifies a low-risk group among 1,854 chemo-naive women with N0/N1 primary breast cancer. Springerplus 2013, 2:111.
31. Gruvberger-Saal SK, Bendahl P-O, Saal LH, Laakso M, Hegardt C, Edén P, Peterson C, Malmström P, Isola J, Borg Å, Fernö M: Estrogen receptor β expression is associated with tamoxifen response in ERa-negative breast carcinoma. Clin Cancer Res 2007, 13:1987-1994.
32. Malmström P, Bendahl P-O, Boiesen P, Brünner N, Idvall I, Fernö M, Group SSBC: S-Phase fraction and urokinase plasminogen activator are better markers for distant recurrences than nottingham prognostic index and histologic grade in a prospective study of premenopausal lymph node-negative breast cancer. J Clin Oncol 2001, 19:2010-2019.
33. Klintman M, Bendahl PO, Grabau D, Lovgren K, Malmstrom P, Ferno M: The prognostic value of Ki67 is dependent on estrogen receptor status and histological grade in premenopausal patients with node-negative breast cancer. Mod Pathol 2010, 23:251-259.
34. Goldhirsch A, Winer EP, Coates AS, Gelber RD, Piccart-Gebhart M, Thurlimann B, Senn HJ: Personalizing the treatment of women with early breast cancer: highlights of the St Gallen International expert consensus on the primary therapy of early breast cancer 2013. Ann Oncol 2013, 24:2206-2223.
35. Elston CW, Ellis IO: Pathological prognostic factors in breast cancer. I. the value of histological grade in breast cancer: experience from a large study with long-term follow-up. Histopathology 1991, 19:403-441.
36. Nielsen TO, Andrews HN, Cheang M, Kucab JE, Hsu FD, Ragaz J, Gilks CB, Makretsov N, Bajdik CD, Brookes C, Neckers LM, Evdokimova V, Huntsman DG, Dunn SE: Expression of the insulin-like growth factor i receptor and urokinase plasminogen activator in breast cancer is associated with poor survival. Cancer Res 2004, 64:286-291.
37. Fagan DH, Uselman RR, Sachdev D, Yee D: Acquired resistance to tamoxifen is associated with loss of the type I insulin-like growth factor receptor (IGF1R): implications for breast cancer treatment. Cancer Res 2012, 72:3372-3380.
38. Brockdorff BL, Heiberg I, Lykkesfeldt AE: Resistance to different antiestrogens is caused by different multi-factorial changes and is associated with reduced expression of IGF receptor Ialpha. Endocr-Relat Cancer 2003, 10:579-590.
39. Pinhel IF, Macneill FA, Hills MJ, Salter J, Detre S, A'Hern R, Nerurkar A, Osin P, Smith IE, Dowsett M: Extreme loss of immunoreactive p-Akt and p-Erk1/2 during routine fixation of primary breast cancer. Breast Cancer Res 2010, 12:R76.
40. Jones RA, Moorehead RA: The impact of transgenic IGF-IR overexpression on mammary development and tumorigenesis. J Mammary Gland Biol Neoplasia 2008, 13:407-413.
41. Pennisi PA, Barr V, Nunez NP, Stannard B, Le Roith D: Reduced expression of insulin-like growth factor I receptors in MCF-7 breast cancer cells leads to a more metastatic phenotype. Cancer Res 2002, 62:6529-6537.
42. Montero JC, Esparis-Ogando A, Re-Louhau MF, Seoane S, Abad M, Calero R, Ocana A, Pandiella A: Active kinase profiling, genetic and pharmacological data define mTOR as an important common target in triple-negative breast cancer. Oncogene 2014, 33:148-156.