Insulin and insulin-like growth factor signalling in neoplasia

Pollak, Michael

doi:10.1038/nrc2536

Cited by 2,059Growth Hormone and Insulin-like Growth FactorsMetabolism, Diabetes, and CancerCancer, Lipids, and Metabolism

Insulin and insulin-like growth factor signalling in neoplasia

Pollak, Michael·2008·Nature Reviews Cancer

DOI 10.1038/nrc2536

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Abstract

Insulin and insulin-like growth factors (IGFs) are well known as key regulators of energy metabolism and growth. There is now considerable evidence that these hormones and the signal transduction networks they regulate have important roles in neoplasia. Epidermiological, clinical and laboratory research methods are being used to investigate novel cancer prevention and treatment strategies related to insulin and IGF signalling. Pharmacological strategies under study include the use of novel receptor-specific antibodies, receptor kinase inhibitors and AMP-activated protein kinase activators such as metformin. There is evidence that insulin and IGF signalling may also be relevant to dietary and lifestyle factors that influence cancer risk and cancer prognosis. Recent results are encouraging and have justified the expansion of many translational research programmes.

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Neoplastic cells may express the receptors for some rejuvenating agents, which could promote tumor growth.
“neoplastic cells might also express receptors resulting in tumor growth (115).”
From Causes, consequences, and reversal of immune system aging (2013) · cites this paper as [115]
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“Some of these mechanisms may be through inhibition of cell growth [148], IGF-1 signaling [149], inhibition of the mTOR pathway [150], reduction of human epidermal growth factor receptor type 2 (HER-2) expression (a major driver of proliferation in breast cancer) [151], inhibition of angiogenesis and inflammation [152], induction of apoptosis and protein 53 (p53) activation [153], cell cycle arrest”
From Metformin: An Old But Still the Best Treatment for Type 2 Diabetes (2013) · cites this paper as [149]
Insulin and IGF receptors form a complex network of cell surface receptors; homodimers and heterodimers have been described, and all function to mediate insulin and IGF responses.
“Insulin and insulin-like growth factor (IGF) receptors form a complex network of cell surface receptors; homodimers and heterodimers have been described, and all function to mediate insulin and IGF responses (49).”
From Diabetes and Cancer (2010) · cites this paper as [49]
Human tumors commonly over-express insulin, IGF-I, and hybrid receptors.
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From Diabetes and Cancer (2010) · cites this paper as [49]
IGF-I could act as a growth stimulus in preneoplastic and neoplastic cells that express insulin, IGF-I, and hybrid receptors.
“IGF-I has more potent mitogenic and anti-apoptotic activities than insulin (58) and could act as a growth stimulus in preneoplastic and neoplastic cells that express insulin, IGF-I, and hybrid receptors (49).”
From Diabetes and Cancer (2010) · cites this paper as [49]

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Self-reported birth weight and subsequent risk of colorectal cancer.
Sandhu, M. S., Luben, R., Day, N., & Khaw, K. (2002) · PubMed · Cited by 63 · see citing works
Plasma Insulin-like Growth Factors, Insulin-like Binding Protein-3, and Outcome in Metastatic Colorectal Cancer: Results from Intergroup Trial N9741
Fuchs, C. S., Goldberg, R. M., Sargent, D. J., Meyerhardt, J. A., Wolpin, B. M., Green, E. M., Pitot, H. C., & Pollak, M. (2008) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-08-0480 · Cited by 60 · see citing works
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Effects of Energy Balance on Cancer in Genetically Altered Mice
Patel, A. C., Núñez, N. P., Perkins, S. N., Barrett, J. C., & Hursting, S. D. (2004) · Journal of Nutrition · doi:10.1093/jn/134.12.3394s · Cited by 57 · see citing works
Cell proliferation induced by insulin in organ culture of rat mammary carcinoma
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An Antibody Targeting the Type I Insulin-like Growth Factor Receptor Enhances the Castration-Induced Response in Androgen-Dependent Prostate Cancer
Plymate, S. R., Haugk, K. H., Coleman, I. M., Woodke, L. B., Vessella, R. L., Nelson, P. S., Montgomery, B., Ludwig, D. L., & Wu, J. D. (2007) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-0648 · Cited by 57 · see citing works
A germ line mutation that delays prostate cancer progression and prolongs survival in a murine prostate cancer model
Majeed, N., Blouin, M., Kaplan‐Lefko, P. J., Barry-Shaw, J., Greenberg, N. M., Gaudreau, P., Bismar, T. A., & Pollak, M. (2005) · Oncogene · doi:10.1038/sj.onc.1208572 · Cited by 56 · see citing works
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A phase I, pharmacokinetic (PK) and pharmacodynamic (PD) study of weekly (qW) MK-0646, an insulin-like growth factor-1 receptor (IGF1R) monoclonal antibody (MAb) in patients (pts) with advanced solid tumors
Atzori, F., Tabernero, J. M., Cervantes, A. M. R., et al. (2008) · Journal of Clinical Oncology · doi:10.1200/jco.2008.26.15_suppl.3519 · Cited by 56 · see citing works
The aromatase inhibitor letrozole and inhibitors of insulin-like growth factor I receptor synergistically induce apoptosis in in vitro models of estrogen-dependent breast cancer
Lisztwan, J. H., Pornon, A., Chen, B., et al. (2008) · Breast Cancer Research · doi:10.1186/bcr2113 · Cited by 54 · see citing works
Inhaled insulin's last gasp?
Kling, J. (2008) · Nature Biotechnology · doi:10.1038/nbt0508-479 · Cited by 52 · see citing works
Insulin resistance, estimated by serum C-peptide level, is associated with reduced event-free survival for postmenopausal women in NCIC CTG MA.14 adjuvant breast cancer trial
Pollak, M., Chapman, J. W., Shepherd, L. E., Meng, D., Richardson, P. M., Wilson, C., Orme, B., & Pritchard, K. I. (2006) · Journal of Clinical Oncology · doi:10.1200/jco.2006.24.18_suppl.524 · Cited by 51 · see citing works
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Influence of Caloric Intake on Experimental Carcinogenesis: A Review
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High activity of the anti-IGF-IR antibody CP-751,871 in combination with paclitaxel and carboplatin in squamous NSCLC
Karp, D. D., Paz-Ares, L. G., Novello, S., et al. (2008) · Journal of Clinical Oncology · doi:10.1200/jco.2008.26.15_suppl.8015 · Cited by 49 · see citing works
Novel role for insulin as an autocrine growth factor for malignant brain tumour cells
Arcaro, A., Doepfner, K. T., Boller, D., et al. (2007) · Biochemical Journal · doi:10.1042/bj20070309 · Cited by 48 · see citing works
A phase I study of MK-0646, a humanized monoclonal antibody against the insulin-like growth factor receptor type 1 (IGF1R) in advanced solid tumor patients in a q2 wk schedule
Hidalgo, M., Gomez, M. T., Lewis, N. L., et al. (2008) · Journal of Clinical Oncology · doi:10.1200/jco.2008.26.15_suppl.3520 · Cited by 47 · see citing works
A phase I study of q3W R1507, a human monoclonal antibody IGF-1R antagonist in patients with advanced cancer
Rodon, J. A., Patnaik, A., Stein, M. N., et al. (2007) · Journal of Clinical Oncology · doi:10.1200/jco.2007.25.18_suppl.3590 · Cited by 46 · see citing works
Implications for Prostate Cancer of Insulin-Like Growth Factor-I (IGF-I) Genetic Variation and Circulating IGF-I Levels
Johansson, M., McKay, J., Wiklund, F. E., et al. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-0887 · Cited by 45 · see citing works
The level of insulin growth factor-1 receptor expression is directly correlated with the tumor uptake of 111In-IGF-1(E3R) in vivo and the clonogenic survival of breast cancer cells exposed in vitro to trastuzumab (Herceptin)
Cornelissen, B. T., McLarty, K., Kersemans, V., et al. (2008) · Nuclear Medicine and Biology · doi:10.1016/j.nucmedbio.2008.05.010 · Cited by 42 · see citing works
Secular changes in body height and weight of Portuguese boys over one century
Cardoso, H. F. V. (2008) · American Journal of Human Biology · doi:10.1002/ajhb.20710 · Cited by 41 · see citing works
Safety, pharmacokinetics and preliminary activity of the anti-IGF-IR antibody CP-751,871 in patients with sarcoma
Olmos, D., Okuno, S., Schuetze, S. M., et al. (2008) · Journal of Clinical Oncology · doi:10.1200/jco.2008.26.15_suppl.10501 · Cited by 41 · see citing works
Optimization of Whole-Body Positron Emission Tomography Imaging by Using Delayed 2-Deoxy-2-[F-18]fluoro-d-glucose Injection Following I.V. Insulin in Diabetic Patients
Turcotte, É. E., Leblanc, M., Carpentier, A. C., & Bénard, F. (2006) · Molecular Imaging and Biology · doi:10.1007/s11307-006-0064-1 · Cited by 40 · see citing works
Cancer and aging: More puzzles, more promises?
Blagosklonny, M., & Campisi, J. (2008) · Cell Cycle · doi:10.4161/cc.7.17.6626 · Cited by 40 · see citing works
Antixenograft tumor activity of a humanized anti-insulin-like growth factor-I receptor monoclonal antibody is associated with decreased AKT activation and glucose uptake
Shang, Y., Mao, Y. V., Batson, J., et al. (2008) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-07-2401 · Cited by 37 · see citing works
A phase I study of AVE1642, a humanized monoclonal antibody IGF-1R (insulin like growth factor1 receptor) antagonist, in patients(pts) with advanced solid tumor(ST)
Tolcher, A. W., Patnaik, A., Till, E., et al. (2008) · Journal of Clinical Oncology · doi:10.1200/jco.2008.26.15_suppl.3582 · Cited by 32 · see citing works
Therapeutic metformin/AMPK activation promotes the angiogenic phenotype in the ERα negative MDA-MB-435 breast cancer model
Hadad, S. M., Appleyard, V. C. L., & Thompson, A. M. (2008) · Breast Cancer Research and Treatment · doi:10.1007/s10549-008-0016-3 · Cited by 31 · see citing works
A phase IB study of AMG 479, a type 1 insulin-like growth factor receptor (IGF1R) antibody, in combination with panitumumab (P) or gemcitabine (G)
Sarantopoulos, J., Mita, A., Mulay, M., et al. (2008) · Journal of Clinical Oncology · doi:10.1200/jco.2008.26.15_suppl.3583 · Cited by 31 · see citing works
Phase I Study of AVE1642 Anti IGF-1R Monoclonal Antibody in Patients with Advanced Multiple Myeloma.
Moreau, P., Hulin, C., Facon, T. T. F., et al. (2007) · Blood · doi:10.1182/blood.v110.11.1166.1166 · Cited by 31 · see citing works
Doctors seek to prevent breast cancer recurrence by lowering insulin levels.
Hede, K. (2008) · Journal of the National Cancer Institute · doi:10.1093/jnci/djn119 · Cited by 27 · see citing works
AMP-activated protein kinase is essential for survival in chronic hypoxia
Borger, D. R., Gavrilescu, L. C., Bucur, M. C., Ivan, M., & DeCaprio, J. A. (2008) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2008.03.056 · Cited by 26 · see citing works
Balancing oral exposure with Cyp3A4 inhibition in benzimidazole-based IGF-IR inhibitors
Zimmermann, K., Wittman, M. D., Saulnier, M. G., Velaparthi, U., Langley, D. R., Sang, X., Frennesson, D. B., Carboni, J. M., Li, A., Greer, A. L., et al. (2008) · Bioorganic & Medicinal Chemistry Letters · doi:10.1016/j.bmcl.2008.05.104 · Cited by 25 · see citing works
IGF1 is a modifier of disease risk in hereditary non‐polyposis colorectal cancer
Reeves, S. G., Rich, D., Meldrum, C. J., et al. (2008) · International Journal of Cancer · doi:10.1002/ijc.23668 · Cited by 25 · see citing works
LKB1: a sweet side to Peutz–Jeghers syndrome?
Carling, D. (2006) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2006.02.003 · Cited by 25 · see citing works
Characterization of NSCLC patients responding to anti-IGF-IR therapy
Gualberto, A., Melvin, C. L., Dean, A., Ang, A. L., Reynolds, J. M., Lee, A., Terstappen, L. W. M. M., Haluska, P., Lipton, A., & Karp, D. D. (2008) · Journal of Clinical Oncology · doi:10.1200/jco.2008.26.15_suppl.8000 · Cited by 24 · see citing works
Correspondence re: Giovannucci et al., A prospective study of plasma insulin-like growth factor-1 and binding protein-3 and risk of colorectal neoplasia in women. Cancer Epidemiol. Biomark. Prev., 9: 345-349, 2000.
Kaaks, R., Rinaldi, S., Lukanova, A., Akhmedkhanov, A., Zeleniuch‐Jacquotte, A., & Toniolo, P. G. (2001) · PubMed · Cited by 19 · see citing works
Phase I dose-escalation study of the anti-IGF-IR recombinant human IgG1 monoclonal antibody (Mab) IMC-A12, administered every other week to patients with advanced solid tumors
Rothenberg, M. L., Poplin, E. A., Sandler, A., et al. (2007) · Molecular Cancer Therapeutics · Cited by 19 · see citing works
Commercial interest waxes for IGF-1 blockers
Osborne, R. (2008) · Nature Biotechnology · doi:10.1038/nbt0708-719 · Cited by 18 · see citing works
NCIC-CTG MA14 Trial: Tamoxifen (tam) vs. tam + octreotide (oct) for adjuvant treatment of stage I or II postmenopausal breast cancer
Pollak, M., Chapman, J. W., Pritchard, K. I., et al. (2008) · Journal of Clinical Oncology · doi:10.1200/jco.2008.26.15_suppl.532 · Cited by 13 · see citing works
Self-citation
Annual Zoledronic Acid: Is Less More?
Higano, C. S. (2007) · Journal of Clinical Oncology · doi:10.1200/jco.2006.08.8146 · Cited by 12 · see citing works
The effects of metformin on pathologic complete response (pCR) rates in diabetic breast cancer (BC) patients receiving neoadjuvant systemic therapy (NST)
Jiralerspong, S., Giordano, S. H., Meric‐Bernstam, F., Barnett, C., Kau, S., Hung, M., Hortobágyi, G. N., & Gonzalez-Angulo, A. M. (2008) · Journal of Clinical Oncology · doi:10.1200/jco.2008.26.15_suppl.528 · Cited by 12 · see citing works
Commentary: Implications of the frequent occurrence of occult carcinoma of the prostate
Miller, A. (2007) · International Journal of Epidemiology · doi:10.1093/ije/dym052 · Cited by 11 · see citing works
A mysterious something: The discovery of insulin and the 1923 Nobel Prize for Frederick G. Banting (1891–1941) and John J.R. Macleod (1876–1935)
Raju, T. N. K. (2006) · Acta Paediatrica · doi:10.1080/08035250600930328 · Cited by 9 · see citing works
A phase I study of the recombinant human IgG1 anti-IGF-IR monoclonal antibody (Mab) IMC-A12, administered on a weekly basis to patients with advanced solid tumors: Interim analysis
Higano, C. S., LoRusso, P. A., Gordon, M. A., et al. (2007) · Molecular Cancer Therapeutics · Cited by 9 · see citing works
Population pharmacokinetics of CP-751,871, a monoclonal antibody against IGF-I receptor, in patients with multiple myeloma or solid tumors
Yin, D., Paccagnella, M. L., Lacy, M. Q., et al. (2008) · Journal of Clinical Oncology · doi:10.1200/jco.2008.26.15_suppl.2524 · Cited by 8 · see citing works
Notes of some cases illustrating peculiarity of type in enteric fever
Armstron, H. E. (1895) · Public Health · doi:10.1016/s0033-3506(05)82553-3 · Cited by 1 · see citing works

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Understanding the Warburg Effect: The Metabolic Requirements of Cell Proliferation
Vander Heiden, M. G., Cantley, L. C., & Thompson, C. B. (2009) · Science · doi:10.1126/science.1160809 · Cited by 16,197 · see citing works
Epithelial-Mesenchymal Transitions in Development and Disease
Thiery, J. P., Acloque, H., Huang, R. Y. J., & Nieto, M. A. (2009) · Cell · doi:10.1016/j.cell.2009.11.007 · Cited by 9,931 · see citing works
A Chromatin-Mediated Reversible Drug-Tolerant State in Cancer Cell Subpopulations
Sharma, S. V., Lee, D. Y., Li, B., Quinlan, M. P., Takahashi, F., Maheswaran, S., McDermott, U., Azizian, N., Zou, L., Fischbach, M. A., et al. (2010) · Cell · doi:10.1016/j.cell.2010.02.027 · Cited by 2,770 · see citing works
Diabetes and Cancer
Giovannucci, E., Harlan, D. M., Archer, M. C., Bergenstal, R. M., Gapstur, S. M., Habel, L. A., Pollak, M., Regensteiner, J. G., & Yee, D. (2010) · Diabetes Care · doi:10.2337/dc10-0666 · Cited by 2,366 · see citing works
Self-citation
The LKB1-AMPK pathway: metabolism and growth control in tumour suppression
Shackelford, D. B., & Shaw, R. J. (2009) · Nature Reviews Cancer · doi:10.1038/nrc2676 · Cited by 1,943 · see citing works
Diabetes and cancer
Vigneri, P., Frasca, F., Sciacca, L., Pandini, G., & Vigneri, R. (2009) · Endocrine Related Cancer · doi:10.1677/erc-09-0087 · Cited by 1,009 · see citing works
Causes, consequences, and reversal of immune system aging
Montecino-Rodriguez, E., Berent-Maoz, B., & Dorshkind, K. (2013) · Journal of Clinical Investigation · doi:10.1172/jci64096 · Cited by 793 · see citing works
Glycemic index, glycemic load and glycemic response: An International Scientific Consensus Summit from the International Carbohydrate Quality Consortium (ICQC)
Augustin, L. S. A., Kendall, C. W. C., Jenkins, D. J. A., Willett, W. C., Astrup, A., Barclay, A. W., Björck, I., Brand-Miller, J. C., Brighenti, F., Buyken, A. E., et al. (2015) · Nutrition, Metabolism and Cardiovascular Diseases · doi:10.1016/j.numecd.2015.05.005 · Cited by 707 · see citing works
Understanding resistance to EGFR inhibitors—impact on future treatment strategies
Wheeler, D. L., Dunn, E. F., & Harari, P. M. (2010) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2010.97 · Cited by 683 · see citing works
Insulin resistance and cancer risk: An overview of the pathogenetic mechanisms
Arcidiacono, B., Iiritano, S., Nocera, A., Possidente, K., Nevolo, M. T., Ventura, V., Foti, D., Chiefari, E., & Brunetti, A. (2012) · Experimental Diabetes Research · doi:10.1155/2012/789174 · Cited by 606 · see citing works
Metformin: An Old But Still the Best Treatment for Type 2 Diabetes
Rojas, L. B. A., & Gomes, M. B. (2013) · Diabetology & Metabolic Syndrome · doi:10.1186/1758-5996-5-6 · Cited by 567 · see citing works
Mechanisms of drug release in nanotherapeutic delivery systems
Wong, P. T., & Choi, S. K. (2015) · Chemical Reviews · doi:10.1021/cr5004634 · Cited by 507 · see citing works
Metformin in cancer therapy: a new perspective for an old antidiabetic drug?
Ben Sahra, I., Le Marchand-Brustel, Y., Tanti, J.-F., & Bost, F. (2010) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-09-1186 · Cited by 493 · see citing works
Signalling by insulin and IGF receptors: supporting acts and new players
Siddle, K. (2011) · Journal of Molecular Endocrinology · doi:10.1530/jme-11-0022 · Cited by 456 · see citing works
Metformin reduces endogenous reactive oxygen species and associated DNA damage
Algire, C., Moiseeva, O., Deschênes-Simard, X., Amrein, L., Petruccelli, L., Birman, E., Viollet, B., Ferbeyre, G., & Pollak, M. N. (2012) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-11-0536 · Cited by 372 · see citing works
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Dietary patterns and cancer risk
Steck, S. E., & Murphy, E. A. (2020) · Nature Reviews Cancer · doi:10.1038/s41568-019-0227-4 · Cited by 292 · see citing works
Insulin–PI3K signalling: an evolutionarily insulated metabolic driver of cancer
Hopkins, B. D., Goncalves, M. D., & Cantley, L. C. (2020) · Nature Reviews Endocrinology · doi:10.1038/s41574-020-0329-9 · Cited by 288 · see citing works
A randomized crossover trial on the effect of plant-based compared with animal-based meat on trimethylamine-N-oxide and cardiovascular disease risk factors in generally healthy adults: Study With Appetizing Plantfood-Meat Eating Alternative Trial (SWAP-MEAT).
Crimarco, A., Springfield, S., Petlura, C., Streaty, T., Cunanan, K., Lee, J., Fielding-Singh, P., Carter, M. M., Topf, M. A., Wastyk, H. C., et al. (2020) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqaa203 · Cited by 286 · see citing works
Repurposing metformin: an old drug with new tricks in its binding pockets
Pryor, R., & Cabreiro, F. (2015) · Biochemical Journal · doi:10.1042/bj20150497 · Cited by 280 · see citing works
Exercise-induced muscle-derived cytokines inhibit mammary cancer cell growth
Hojman, P., Dethlefsen, C., Brandt, C., Hansen, J., Pedersen, L., & Pedersen, B. K. (2011) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00520.2010 · Cited by 259 · see citing works
Insulin-Like Growth Factor 1 (IGF-1) Signaling in Glucose Metabolism in Colorectal Cancer
Kasprzak, A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22126434 · Cited by 248 · see citing works
Visceral adiposity, insulin resistance and cancer risk
Donohoe, C. L., Doyle, S. L., & Reynolds, J. V. (2011) · Diabetology & Metabolic Syndrome · doi:10.1186/1758-5996-3-12 · Cited by 247 · see citing works
Hyperinsulinaemia in cancer
Gallagher, E. J., & LeRoith, D. (2020) · Nature Reviews Cancer · doi:10.1038/s41568-020-0295-5 · Cited by 241 · see citing works
Metformin and Other Biguanides in Oncology: Advancing the Research Agenda
Pollak, M. (2010) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-10-0175 · Cited by 240 · see citing works
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Insulin receptor functionally enhances multistage tumor progression and conveys intrinsic resistance to IGF-1R targeted therapy
Ulanet, D. B., Ludwig, D. L., Kahn, C. R., & Hanahan, D. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0914076107 · Cited by 235 · see citing works
Metformin and rapamycin have distinct effects on the AKT pathway and proliferation in breast cancer cells
Zakikhani, M., Blouin, M.-J., Piura, E., & Pollak, M. N. (2010) · Breast Cancer Research and Treatment · doi:10.1007/s10549-010-0763-9 · Cited by 213 · see citing works
Self-citation
Development and validation of anthropometric prediction equations for lean body mass, fat mass and percent fat in adults using the National Health and Nutrition Examination Survey (NHANES) 1999–2006
Lee, D. H., Keum, N., Hu, F. B., Orav, E. J., Rimm, E. B., Sun, Q., Willett, W. C., & Giovannucci, E. L. (2017) · British Journal of Nutrition · doi:10.1017/s0007114517002665 · Cited by 191 · see citing works
Metformin downregulates the insulin/IGF-I signaling pathway and inhibits different uterine serous carcinoma (USC) cells proliferation and migration in p53-dependent or -independent manners
Sarfstein, R., Friedman, Y., Attias-Geva, Z., Fishman, A., Bruchim, I., & Werner, H. (2013) · PLoS ONE · doi:10.1371/journal.pone.0061537 · Cited by 150 · see citing works
Metformin Targets Multiple Signaling Pathways in Cancer
Lei, Y., Yi, Y., Liu, Y., Liu, X., Keller, E. T., Qian, C.-N., Zhang, J., & Lu, Y. (2017) · Chinese Journal of Cancer · doi:10.1186/s40880-017-0184-9 · Cited by 152 · see citing works
A new link between diabetes and cancer: enhanced WNT/β-catenin signaling by high glucose
García-Jiménez, C., García-Martínez, J. M., Chocarro-Calvo, A., & De la Vieja, A. (2014) · Journal of Molecular Endocrinology · doi:10.1530/jme-13-0152 · Cited by 151 · see citing works
The metabolic landscape of lung cancer: New insights in a disturbed glucose metabolism
Vanhove, K., Graulus, G.-J., Mesotten, L., Thomeer, M., Derveaux, E., Noben, J.-P., Guedens, W., & Adriaensens, P. (2019) · Frontiers in Oncology · doi:10.3389/fonc.2019.01215 · Cited by 147 · see citing works
Regulation of muscle atrophy in aging and disease
Vinciguerra, M., Musaro, A., & Rosenthal, N. (2010) · Advances in experimental medicine and biology · doi:10.1007/978-1-4419-7002-2_15 · Cited by 149 · see citing works
Diabetes and Pancreatic Cancer: Chicken or Egg?
Magruder, J. T., Elahi, D., & Andersen, D. K. (2011) · Pancreas · doi:10.1097/mpa.0b013e318209e05d · Cited by 140 · see citing works
Changes in Insulin Receptor Signaling Underlie Neoadjuvant Metformin Administration in Breast Cancer: A Prospective Window of Opportunity Neoadjuvant Study
Dowling, R. J., Niraula, S., Chang, M. C., Done, S. J., Ennis, M., McCready, D. R., Leong, W. L., Escallon, J. M., Reedijk, M., Goodwin, P. J., et al. (2015) · Breast Cancer Research · doi:10.1186/s13058-015-0540-0 · Cited by 117 · see citing works
Abdominal obesity and gastroesophageal cancer risk: Systematic review and meta-analysis of prospective studies
Du, X., Hidayat, K., & Shi, B.-M. (2017) · Bioscience Reports · doi:10.1042/bsr20160474 · Cited by 98 · see citing works
The impact of type 2 diabetes mellitus on cancer‐specific survival: A follow‐up study in sweden
Liu, X., Ji, J., Sundquist, K., Sundquist, J., & Hemminki, K. (2012) · Cancer · doi:10.1002/cncr.26420 · Cited by 97 · see citing works
Targeting the insulin growth factor receptor 1
Arnaldez, F. I., & Helman, L. J. (2012) · Hematology/Oncology Clinics of North America · doi:10.1016/j.hoc.2012.01.004 · Cited by 88 · see citing works
Inhibition of lung tumorigenesis by metformin is associated with decreased plasma IGF-I and diminished receptor tyrosine kinase signaling
Quinn, B. J., Dallos, M., Kitagawa, H., Kunnumakkara, A. B., Memmott, R. M., Hollander, M. C., Gills, J. J., & Dennis, P. A. (2013) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-13-0058-t · Cited by 85 · see citing works
Is There a Role for IGF1R and c-MET Pathways in Resistance to Cetuximab in Metastatic Colorectal Cancer?
Inno, A., Di Salvatore, M., Cenci, T., Martini, M., Orlandi, A., Strippoli, A., Ferrara, A. M., Bagalà, C., Cassano, A., Larocca, L. M., et al. (2011) · Clinical Colorectal Cancer · doi:10.1016/j.clcc.2011.03.028 · Cited by 83 · see citing works
Cellular Senescence as a Therapeutic Target for Age-Related Diseases: A Review
Amaya-Montoya, M., Pérez-Londoño, A., Guatibonza-García, V., Vargas-Villanueva, A., & Mendivil, C. O. (2020) · Advances in Therapy · doi:10.1007/s12325-020-01287-0 · Cited by 82 · see citing works
Thiazolidinedione use and cancer incidence in type 2 diabetes: A systematic review and meta-analysis
Colmers, I. N., Bowker, S. L., & Johnson, J. A. (2012) · Diabetes & Metabolism · doi:10.1016/j.diabet.2012.06.003 · Cited by 81 · see citing works
Endogenous hormones and risk of invasive breast cancer in pre- and post-menopausal women: findings from the UK Biobank
Tin Tin, S., Reeves, G. K., & Key, T. J. (2021) · British Journal of Cancer · doi:10.1038/s41416-021-01392-z · Cited by 71 · see citing works
Repositioning chloroquine and metformin to eliminate cancer stem cell traits in pre-malignant lesions
Vazquez-Martin, A., López-Bonetc, E., Cufí, S., Oliveras-Ferraros, C., Del Barco, S., Martin-Castillo, B., & Menendez, J. A. (2011) · Drug Resistance Updates · doi:10.1016/j.drup.2011.04.003 · Cited by 66 · see citing works
Identifying hyperinsulinaemia in the absence of impaired glucose tolerance: An examination of the Kraft database
Crofts, C., Schofield, G., Zinn, C., Wheldon, M., & Kraft, J. (2016) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2016.06.007 · Cited by 53 · see citing works
Somatotropic-Testicular Axis: A Crosstalk Between GH/IGF-I and Gonadal Hormones During Development, Transition, and Adult Age
Tenuta, M., Carlomagno, F., Cangiano, B., Kanakis, G., Pozza, C., Sbardella, E., Isidori, A. M., Krausz, C., & Gianfrilli, D. (2021) · Andrology · doi:10.1111/andr.12918 · Cited by 49 · see citing works
Regulation of insulin-like growth factor signaling by metformin in endometrial cancer cells
XIE, Y., WANG, J.-L., JI, M., YUAN, Z.-F., PENG, Z., ZHANG, Y., WEN, J.-G., & SHI, H.-R. (2014) · Oncology Letters · doi:10.3892/ol.2014.2466 · Cited by 46 · see citing works
Neuregulin 1-HER axis as a key mediator of hyperglycemic memory effects in breast cancer
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Authors: Pollak, M.
Venue: Nature Reviews Cancer
Publisher: Springer Science and Business Media LLC
Published: 2008-12
Volume: 8
Issue: 12
Pages: 915-928
ISSN: 1474-175X (ISSN-L)
1474-1768
DOI: 10.1038/nrc2536
OpenAlex: W2089171551
Cited by: 2,059
References: 199
Citations by year: 2026: 70 · 2025: 68 · 2024: 64 · 2023: 103 · 2022: 76 · 2021: 105 · 2020: 98 · 2019: 102 · 2018: 84 · 2017: 110 · 2016: 101 · 2015: 153 · 2014: 153 · 2013: 152 · 2012: 176
FWCI: 20.47
Type: journal article
Language: en
Update notices: erratum (2009-01-30)
Open access: closed
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature reviews. Cancer (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Growth Hormone and Insulin-like Growth Factors
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Lipids, and Metabolism
Keywords: insulin signaling, insulin-like growth factor, cancer, cancer prevention, cancer therapy, metformin, AMPK, energy metabolism, lifestyle factors, cancer risk, cancer prognosis, signal transduction
MeSH terms: Cell Division, Cell Physiological Phenomena, Diabetes Mellitus, Glucose, Humans, Insulin, Insulin-Like Growth Factor I, Insulin-Like Growth Factor II, Neoplasms, Receptor, Insulin, Somatomedins, Signal Transduction, Receptor, IGF Type 1, Insulin-Like Growth Factor Binding Proteins

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