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IGF-1 and IGFBP-3: Risk of prostate cancer among men in the Prostate, Lung, Colorectal and Ovarian Cancer Screening Trial

  1. Jocelyn M. Weiss1,†,*,
  2. Wen-Yi Huang1,
  3. Sabina Rinaldi2,
  4. Thomas R. Fears1,
  5. Nilanjan Chatterjee1,
  6. David Chia3,
  7. E. David Crawford4,
  8. Rudolf Kaaks2,
  9. Richard B. Hayes1

Article first published online: 27 JUN 2007

DOI: 10.1002/ijc.22921

Issue

International Journal of Cancer

International Journal of Cancer

Volume 121, Issue 10, pages 2267–2273, 15 November 2007

Additional Information

How to Cite

Weiss, J. M., Huang, W.-Y., Rinaldi, S., Fears, T. R., Chatterjee, N., Chia, D., Crawford, E. D., Kaaks, R. and Hayes, R. B. (2007), IGF-1 and IGFBP-3: Risk of prostate cancer among men in the Prostate, Lung, Colorectal and Ovarian Cancer Screening Trial. Int. J. Cancer, 121: 2267–2273. doi: 10.1002/ijc.22921

Author Information

  1. 1

    Division of Cancer Epidemiology and Genetics, NCI/NIH, Bethesda, MD

  2. 2

    International Agency for Research on Cancer, Lyon, France

  3. 3

    UCLA Immunogenetics Center, Los Angeles, CA

  4. 4

    University of Colorado Health Sciences Center, Denver, CO

  1. †

    Fax: +301-402-1819.

*Division of Cancer Epidemiology and Genetics, NCI, Occupational and Environmental Epidemiology Branch, 6120 Executive Boulevard, EPS 8123, MSC 7240, Bethesda, MD 20892, USA

Publication History

  1. Issue published online: 25 SEP 2007
  2. Article first published online: 27 JUN 2007
  3. Manuscript Accepted: 9 MAY 2007
  4. Manuscript Received: 16 MAR 2007

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References

  • 1
    American Cancer Society. Cancer facts and figures. Atlanta, GA: American Cancer Society, 2007.
  • 2
    Bostwick DG, Burke HB, Djakiew D, Euling S, Ho SM, Landolph J, Morrison H, Sonawane B, Shifflett T, Waters DJ, Timms B. Human prostate cancer risk factors. Cancer 2004; 101: 2371–490.
    Direct Link:
  • 3
    Chan JM, Gann PH, Giovannucci EL. Role of diet in prostate cancer development and progression. J Clin Oncol 2005; 23: 8152–60.
  • 4
    Freedland SJ, Aronson WJ. Obesity and prostate cancer. Urology 2005; 65: 433–9.
  • 5
    Wolk A. Diet, lifestyle and risk of prostate cancer. Acta Oncol 2005; 44: 277–81.
  • 6
    Hsing AW, Chokkalingam AP. Prostate cancer epidemiology. Front Biosci 2006; 11: 1388–413.
  • 7
    Cancel-Tassin G, Cussenot O. Genetic susceptibility to prostate cancer. BJU Int 2005; 96: 1380–5.
    Direct Link:
  • 8
    Chan JM, Stampfer MJ, Giovannucci E, Gann PH, Ma J, Wilkinson P, Hennekens CH, Pollak M. Plasma insulin-like growth factor-I and prostate cancer risk: a prospective study. Science 1998; 279: 563–6.
  • 9
    Chan JM, Stampfer MJ, Ma J, Gann P, Gaziano JM, Pollak M, Giovannucci E. Insulin-like growth factor-I (IGF-I) and IGF binding protein-3 as predictors of advanced-stage prostate cancer. J Natl Cancer Inst 2002; 94: 1099–106.
  • 10
    Chen C, Lewis SK, Voigt L, Fitzpatrick A, Plymate SR, Weiss NS. Prostate carcinoma incidence in relation to prediagnostic circulating levels of insulin-like growth factor I, insulin-like growth factor binding protein 3, and insulin. Cancer 2005; 103: 76–84.
    Direct Link:
  • 11
    Chokkalingam AP, Pollak M, Fillmore CM, Gao YT, Stanczyk FZ, Deng J, Sesterhenn IA, Mostofi FK, Fears TR, Madigan MP, Ziegler RG, Fraumeni JF,Jr, et al. Insulin-like growth factors and prostate cancer: a population-based case-control study in China. Cancer Epidemiol Biomarkers Prev 2001; 10: 421–7.
  • 12
    Finne P, Auvinen A, Koistinen H, Zhang WM, Maattanen L, Rannikko S, Tammela T, Seppala M, Hakama M, Stenman UH. Insulin-like growth factor I is not a useful marker of prostate cancer in men with elevated levels of prostate-specific antigen. J Clin Endocrinol Metab 2000; 85: 2744–7.
  • 13
    Harman SM, Metter EJ, Blackman MR, Landis PK, Carter HB. Serum levels of insulin-like growth factor I (IGF-I), IGF-II, IGF-binding protein-3, and prostate-specific antigen as predictors of clinical prostate cancer. J Clin Endocrinol Metab 2000; 85: 4258–65.
  • 14
    Ismail AH, Pollak M, Behlouli H, Tanguay S, Begin LR, Aprikian AG. Insulin-like growth factor-1 and insulin-like growth factor binding protein-3 for prostate cancer detection in patients undergoing prostate biopsy. J Urol 2002; 168: 2426–30.
  • 15
    Lacey JV,Jr, Hsing AW, Fillmore CM, Hoffman S, Helzlsouer KJ, Comstock GW. Null association between insulin-like growth factors, insulin-like growth factor-binding proteins, and prostate cancer in a prospective study. Cancer Epidemiol Biomarkers Prev 2001; 10: 1101–2.
  • 16
    Li L, Yu H, Schumacher F, Casey G, Witte JS. Relation of serum insulin-like growth factor-I (IGF-I) and IGF binding protein-3 to risk of prostate cancer (United States). Cancer Causes Control 2003; 14: 721–6.
  • 17
    Mantzoros CS, Tzonou A, Signorello LB, Stampfer M, Trichopoulos D, Adami HO. Insulin-like growth factor 1 in relation to prostate cancer and benign prostatic hyperplasia. Br J Cancer 1997; 76: 1115–8.
  • 18
    Meyer F, Galan P, Douville P, Bairati I, Kegle P, Bertrais S, Czernichow S, Hercberg S. A prospective study of the insulin-like growth factor axis in relation with prostate cancer in the SU.VI.MAX trial. Cancer Epidemiol Biomarkers Prev 2005; 14: 2269–72.
  • 19
    Morris JK, George LM, Wu T, Wald NJ. Insulin-like growth factors and cancer: no role in screening. Evidence from the BUPA study and meta-analysis of prospective epidemiological studies. Br J Cancer 2006; 95: 112–7.
  • 20
    Oliver SE, Gunnell D, Donovan J, Peters TJ, Persad R, Gillatt D, Pearce A, Neal DE, Hamdy FC, Holly J. Screen-detected prostate cancer and the insulin-like growth factor axis: results of a population-based case-control study. Int J Cancer 2004; 108: 887–92.
    Direct Link:
  • 21
    Platz EA, Pollak MN, Leitzmann MF, Stampfer MJ, Willett WC, Giovannucci E. Plasma insulin-like growth factor-1 and binding protein-3 and subsequent risk of prostate cancer in the PSA era. Cancer Causes Control 2005; 16: 255–62.
  • 22
    Stattin P, Bylund A, Rinaldi S, Biessy C, Dechaud H, Stenman UH, Egevad L, Riboli E, Hallmans G, Kaaks R. Plasma insulin-like growth factor-I, insulin-like growth factor-binding proteins, and prostate cancer risk: a prospective study. J Natl Cancer Inst 2000; 92: 1910–17.
  • 23
    Stattin P, Rinaldi S, Biessy C, Stenman UH, Hallmans G, Kaaks R. High levels of circulating insulin-like growth factor-I increase prostate cancer risk: a prospective study in a population-based nonscreened cohort. J Clin Oncol 2004; 22: 3104–12.
  • 24
    Wolk A, Mantzoros CS, Andersson SO, Bergstrom R, Signorello LB, Lagiou P, Adami HO, Trichopoulos D. Insulin-like growth factor 1 and prostate cancer risk: a population-based, case-control study. J Natl Cancer Inst 1998; 90: 911–15.
  • 25
    Woodson K, Tangrea JA, Pollak M, Copeland TD, Taylor PR, Virtamo J, Albanes D. Serum insulin-like growth factor I: tumor marker or etiologic factor? A prospective study of prostate cancer among Finnish men. Cancer Res 2003; 63: 3991–4.
  • 26
    Severi G, Morris HA, MacInnis RJ, English DR, Tilley WD, Hopper JL, Boyle P, Giles GG. Circulating insulin-like growth factor-I and binding protein-3 and risk of prostate cancer. Cancer Epidemiol Biomarkers Prev 2006; 15: 1137–41.
  • 27
    Meinbach DS, Lokeshwar BL. Insulin-like growth factors and their binding proteins in prostate cancer: cause or consequence. Urol Oncol 2006; 24: 294–306.
  • 28
    Gennigens C, Menetrier-Caux C, Droz JP. Insulin-Like Growth Factor (IGF) family and prostate cancer. Crit Rev Oncol Hematol 2006; 58: 124–45.
  • 29
    Kaplan PJ, Mohan S, Cohen P, Foster BA, Greenberg NM. The insulin-like growth factor axis and prostate cancer: lessons from the transgenic adenocarcinoma of mouse prostate (TRAMP) model. Cancer Res 1999; 59: 2203–9.
  • 30
    Papatsoris AG, Karamouzis MV, Papavassiliou AG. Novel insights into the implication of the IGF-1 network in prostate cancer. Trends Mol Med 2005; 11: 52–5.
  • 31
    Baserga R, Peruzzi F, Reiss K. The IGF-1 receptor in cancer biology. Int J Cancer 2003; 107: 873–7.
    Direct Link:
  • 32
    Pollak MN, Schernhammer ES, Hankinson SE. Insulin-like growth factors and neoplasia. Nat Rev Cancer 2004; 4: 505–18.
  • 33
    Rajaram S, Baylink DJ, Mohan S. Insulin-like growth factor-binding proteins in serum and other biological fluids: regulation and functions. Endocr Rev 1997; 18: 801–31.
  • 34
    Angelloz-Nicoud P, Harel L, Binoux M. Recombinant human insulin-like growth factor (IGF) binding protein-3 stimulates prostate carcinoma cell proliferation via an IGF-dependent mechanism. Role of serine proteases. Growth Regul 1996; 6: 130–6.
  • 35
    Rajah R, Khare A, Lee PD, Cohen P. Insulin-like growth factor-binding protein-3 is partially responsible for high-serum-induced apoptosis in PC-3 prostate cancer cells. J Endocrinol 1999; 163: 487–94.
  • 36
    Macinnis RJ, English DR. Body size and composition and prostate cancer risk: systematic review and meta-regression analysis. Cancer Causes Control 2006; 17: 989–1003.
  • 37
    Rodriguez C, Freedland SJ, Deka A, Jacobs EJ, McCullough ML, Patel AV, Thun MJ, Calle EE. Body mass index, weight change, and risk of prostate cancer in the Cancer Prevention Study II Nutrition Cohort. Cancer Epidemiol Biomarkers Prev 2007; 16: 63–9.
  • 38
    Wright ME, Chang SC, Schatzkin A, Albanes D, Kipnis V, Mouw T, Hurwitz P, Hollenbeck A, Leitzmann MF. Prospective study of adiposity and weight change in relation to prostate cancer incidence and mortality. Cancer 2007; 109: 675–84.
    Direct Link:
  • 39
    Calle EE, Rodriguez C, Walker-Thurmond K, Thun MJ. Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N Engl J Med 2003; 348: 1625–38.
  • 40
    Snowdon DA, Phillips RL, Choi W. Diet, obesity, and risk of fatal prostate cancer. Am J Epidemiol 1984; 120: 244–50.
  • 41
    Hall K, Hilding A, Thoren M. Determinants of circulating insulin-like growth factor-I. J Endocrinol Invest 1999; 22: 48–57.
  • 42
    Luque RM, Kineman RD. Impact of obesity on the growth hormone axis: evidence for a direct inhibitory effect of hyperinsulinemia on pituitary function. Endocrinology 2006; 147: 2754–63.
  • 43
    Kaklamani VG, Linos A, Kaklamani E, Markaki I, Mantzoros C. Age, sex, and smoking are predictors of circulating insulin-like growth factor 1 and insulin-like growth factor-binding protein 3. J Clin Oncol 1999; 17: 813–17.
  • 44
    Morimoto LM, Newcomb PA, White E, Bigler J, Potter JD. Variation in plasma insulin-like growth factor-1 and insulin-like growth factor binding protein-3: personal and lifestyle factors (United States). Cancer Causes Control 2005; 16: 917–27.
  • 45
    Thissen JP, Ketelslegers JM, Underwood LE. Nutritional regulation of the insulin-like growth factors. Endocr Rev 1994; 15: 80–101.
  • 46
    Yu H, Rohan T. Role of the insulin-like growth factor family in cancer development and progression. J Natl Cancer Inst 2000; 92: 1472–89.
  • 47
    Harrela M, Koistinen H, Kaprio J, Lehtovirta M, Tuomilehto J, Eriksson J, Toivanen L, Koskenvuo M, Leinonen P, Koistinen R, Seppala M. Genetic and environmental components of interindividual variation in circulating levels of IGF-I, IGF-II, IGFBP-1, and IGFBP-3. J Clin Invest 1996; 98: 2612–15.
  • 48
    Hong Y, Pedersen NL, Brismar K, Hall K, de Faire U. Quantitative genetic analyses of insulin-like growth factor I (IGF-I), IGF-binding protein-1, and insulin levels in middle-aged and elderly twins. J Clin Endocrinol Metab 1996; 81: 1791–7.
  • 49
    Argente J, Caballo N, Barrios V, Pozo J, Munoz MT, Chowen JA, Hernandez M. Multiple endocrine abnormalities of the growth hormone and insulin-like growth factor axis in prepubertal children with exogenous obesity: effect of short- and long-term weight reduction. JClin Endocrinol Metab 1997; 82: 2076–83.
  • 50
    Frystyk J, Vestbo E, Skjaerbaek C, Mogensen CE, Orskov H. Free insulin-like growth factors in human obesity. Metabolism 1995; 44: 37–44.
  • 51
    Nam SY, Lee EJ, Kim KR, Cha BS, Song YD, Lim SK, Lee HC, Huh KB. Effect of obesity on total and free insulin-like growth factor (IGF)-1, and their relationship to IGF-binding protein (BP)-1, IGFBP-2, IGFBP-3, insulin, and growth hormone. Int J Obes Relat Metab Disord 1997; 21: 355–9.
  • 52
    Weaver JU, Holly JM, Kopelman PG, Noonan K, Giadom CG, White N, Virdee S, Wass JA. Decreased sex hormone binding globulin (SHBG) and insulin-like growth factor binding protein (IGFBP-1) in extreme obesity. Clin Endocrinol (Oxf) 1990; 33: 415–22.
    Direct Link:
  • 53
    Tannenbaum GS, Guyda HJ, Posner BI. Insulin-like growth factors: a role in growth hormone negative feedback and body weight regulation via brain. Science 1983; 220: 77–9.
  • 54
    Gohagan JK, Prorok PC, Hayes RB, Kramer BS. The Prostate, Lung, Colorectal and Ovarian (PLCO) Cancer Screening Trial of the National Cancer Institute: history, organization, and status. Control Clin Trials 2000; 21: 251S–272S.
  • 55
    Hayes RB, Sigurdson A, Moore L, Peters U, Huang WY, Pinsky P, Reding D, Gelmann EP, Rothman N, Pfeiffer RM, Hoover RN, Berg CD. Methods for etiologic and early marker investigations in the PLCO trial. Mutat Res 2005; 592: 147–54.
  • 56
    Andriole GL, Levin DL, Crawford ED, Gelmann EP, Pinsky PF, Chia D, Kramer BS, Reding D, Church TR, Grubb RL, Izmirlian G, Ragard LR, et al. Prostate Cancer Screening in the Prostate, Lung, Colorectal and Ovarian (PLCO) Cancer Screening Trial: findings from the initial screening round of a randomized trial. J Natl Cancer Inst 2005; 97: 433–8.
  • 57
    Fleming ID, Cooper JS, Henson DE, Hutter RVP, Kennedy BJ, Murphy GP. American Joint Committee on Cancer staging manual. 5th editon. Philadelphia: J.B. Lippincott 1997; 219–22.
  • 58
    Beahrs OH, Henson DE, Hutter RVP, Kennedy BJ. American Joint Committee on Cancer staging manual. 4th editon. Philadelphia: J.B. Lippincott 1992; 181–6.
  • 59
    Rothman KJ, Greenland S. Modern epidemiology. Philadelphia, PA: Lippincott Raven, 1998.
  • 60
    Harrell FE,Jr. Missing data. Regression modeling strategies: with applications to linear models, logistic regression, and survival analysis. New York: Springer-Verlag; 2001; 41–52.
  • 61
    Stolzenberg-Solomon RZ, Limburg P, Pollak M, Taylor PR, Virtamo J, Albanes D. Insulin-like growth factor (IGF)-1, IGF-binding protein-3, and pancreatic cancer in male smokers. Cancer Epidemiol Biomarkers Prev 2004; 13: 438–44.
  • 62
    Calle EE, Kaaks R. Overweight, obesity and cancer: epidemiological evidence and proposed mechanisms. Nat Rev Cancer 2004; 4: 579–91.
  • 63
    Presti JC,Jr. Obesity and prostate cancer. Curr Opin Urol 2005; 15: 13–6.
  • 64
    Onuma M, Bub JD, Rummel TL, Iwamoto Y. Prostate cancer cell-adipocyte interaction: leptin mediates androgen-independent prostate cancer cell proliferation through c-Jun NH2-terminal kinase. J Biol Chem 2003; 278: 42660–7.
  • 65
    Cohen P, Peehl DM, Lamson G, Rosenfeld RG. Insulin-like growth factors (IGFs), IGF receptors, and IGF-binding proteins in primary cultures of prostate epithelial cells. J Clin Endocrinol Metab 1991; 73: 401–7.
  • 66
    Rinaldi S, Kaaks R, Zeleniuch-Jacquotte A, Arslan AA, Shore RE, Koenig KL, Dossus L, Riboli E, Stattin P, Lukanova A, Toniolo P. Insulin-like growth factor-I, IGF binding protein-3, and breast cancer in young women: a comparison of risk estimates using different peptide assays. Cancer Epidemiol Biomarkers Prev 2005; 14: 48–52.
  • 67
    Diamandi A, Mistry J, Krishna RG, Khosravi J. Immunoassay of insulin-like growth factor-binding protein-3 (IGFBP-3): new means to quantifying IGFBP-3 proteolysis. J Clin Endocrinol Metab 2000; 85: 2327–33.
  • 68
    Baillargeon J, Pollock BH, Kristal AR, Bradshaw P, Hernandez J, Basler J, Higgins B, Lynch S, Rozanski T, Troyer D, Thompson I. The association of body mass index and prostate-specific antigen in a population-based study. Cancer 2005; 103: 1092–5.
    Direct Link:
  • 69
    Barqawi AB, Golden BK, O'Donnell C, Brawer MK, Crawford ED. Observed effect of age and body mass index on total and complexed PSA: analysis from a national screening program. Urology 2005; 65: 708–12.
  • 70
    Kristal AR, Chi C, Tangen CM, Goodman PJ, Etzioni R, Thompson IM. Associations of demographic and lifestyle characteristics with prostate-specific antigen (PSA) concentration and rate of PSA increase. Cancer 2006; 106: 320–8.
    Direct Link:
  • 71
    Ku JH, Kim ME, Lee NK, Park YH, Ahn JO. Influence of age, anthropometry, and hepatic and renal function on serum prostate-specific antigen levels in healthy middle-age men. Urology 2003; 61: 132–6.
  • 72
    Werny DM, Thompson T, Saraiya M, Freedman D, Kottiri BJ, German RR, Wener M. Obesity is negatively associated with prostate-specific antigen in U.S. men, 2001–2004. Cancer Epidemiol Biomarkers Prev 2007; 16: 70–6.
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