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Maternal Energetics and the Developmental Origins of Prostate Cancer in Offspring

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Murine Models, Energy Balance, and Cancer

Part of the book series: Energy Balance and Cancer ((EBAC,volume 10))

Abstract

In 2014, Prostate cancer was the most commonly diagnosed cancer in men in the Western world, but few modifiable risk factors exist for this disease. Many studies have examined the association between obesity and prostate cancer incidence, producing conflicting results. However, maternal energetics during periconception and gestation has barely been considered as a potential risk factor, despite the fact that prostate tissue patterning and early development occur in utero. Maternal diabetes and obesity dramatically affect health at the time of pregnancy, and rodent and human studies demonstrate that the effects manifest in a variety of noncommunicable conditions in offspring, including early initiation of mammary tumors. Importantly, maternal diabetes and obesity directly alter the health of the early embryo and the maternal germ cell, or oocyte. Obesity-exposed oocytes exhibit alterations in size, gene expression, chromosome structure, and metabolism, and adult offspring present with defects including hyperplastic prostate tissues. We propose here that maternal obesity alters epigenetic and metabolic functions in the oocyte, which are passed to offspring, sensitizing them to precancerous conditions. Such an in utero environment could provide a “first hit” for prostate cancer development and should be considered when making dietary recommendations for expectant mothers.

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References

  1. Kleinsmith LJ, Kerrigan D, Kelly J, Hollen B. What is Cancer? National Cancer Institute. 2009. http://www.cancer.gov/cancertopics/understandingcancer/cancer/page1. Accessed 10 June 2014.

  2. Howlader N, Noone A, Krapcho M, Garshell J, Neyman N, Altekruse SF, Kosary CL, Yu M, Ruhl J, Tatalovich Z, Cho H, Mariotto A, Lewis DR, Chen HS, Feuer EJ, Cronin KA. SEER Cancer Statistics Review, 1975–2011. National Cancer Institute. 2014. http://seer.cancer.gov/csr/1975_2011/. Accessed 20 April 2014.

  3. Cancer Trends Progress Report—2011/2012. Update National Cancer Institute, NIH, DHHS. 2012. http://progressreport.cancer.gov.

  4. Klein EA, Thompson IM Jr, Tangen CM, Crowley JJ, Lucia MS, Goodman PJ, Minasian LM, Ford LG, Parnes HL, Gaziano JM, Karp DD, Lieber MM, Walther PJ, Klotz L, Parsons JK, Chin JL, Darke AK, Lippman SM, Goodman GE, Meyskens FL Jr, Baker LH. Vitamin E and the risk of prostate cancer: the Selenium and Vitamin E Cancer Prevention Trial (SELECT). JAMA. 2011;306(14):1549–56.

    CAS  PubMed Central  PubMed  Google Scholar 

  5. Figueiredo JC, Grau MV, Haile RW, Sandler RS, Summers RW, Bresalier RS, Burke CA, McKeown-Eyssen GE, Baron JA. Folic acid and risk of prostate cancer: results from a randomized clinical trial. J Natl Cancer Inst. 2009;101(6):432–5.

    CAS  PubMed Central  PubMed  Google Scholar 

  6. Rycyna KJ, Bacich DJ, O’Keefe DS. Opposing roles of folate in prostate cancer. Urology. 2013;82(6):1197–203.

    PubMed  Google Scholar 

  7. Chan JM, Giovannucci EL. Dairy products, calcium, and vitamin D and risk of prostate cancer. Epidemiol Rev. 2001;23(1):87–92.

    CAS  PubMed  Google Scholar 

  8. Skinner HG, Schwartz GG. Serum calcium and incident and fatal prostate cancer in the National Health and Nutrition Examination Survey. Cancer Epidemiol Biomarkers Prev (a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology). 2008;17(9):2302–5.

    CAS  PubMed Central  PubMed  Google Scholar 

  9. Van Hemelrijck M, Hermans R, Michaelsson K, Melvin J, Garmo H, Hammar N, Jungner I, Walldius G, Holmberg L. Serum calcium and incident and fatal prostate cancer in the Swedish AMORIS study. Cancer Causes Control. 2012;23(8):1349–58.

    PubMed  Google Scholar 

  10. Wynder EL. Nutrition and cancer. Fed Proc. 1976;35(6):1309–15.

    CAS  PubMed  Google Scholar 

  11. Holmberg L. Obesity, nutrition, and prostate cancer: insights and issues. Eur Urol. 2013;63(5):821–2.

    PubMed  Google Scholar 

  12. Discacciati A, Orsini N, Wolk A. Body mass index and incidence of localized and advanced prostate cancer—a dose-response meta-analysis of prospective studies. Ann Oncol. 2012;23(7):1665–71.

    CAS  PubMed  Google Scholar 

  13. Hsing AW, Sakoda LC, Chua S Jr. Obesity, metabolic syndrome, and prostate cancer. Am J Clin Nutr. 2007;86(3):843–57.

    Google Scholar 

  14. Cao Y, Ma J. Body mass index, prostate cancer-specific mortality, and biochemical recurrence: a systematic review and meta-analysis. Cancer Prev Res. 2011;4(4):486–501.

    CAS  Google Scholar 

  15. Hu MB, Xu H, Bai PD, Jiang HW, Ding Q. Obesity has multifaceted impact on biochemical recurrence of prostate cancer: a dose-response meta-analysis of 36,927 patients. Med Oncol. 2014;31(2):829.

    PubMed  Google Scholar 

  16. Allott EH, Masko EM, Freedland SJ. Obesity and prostate cancer: weighing the evidence. Eur Urol. 2013;63(5):800–9.

    CAS  PubMed Central  PubMed  Google Scholar 

  17. Humphrey PA. Prostate pathology. Chicago: American society for clinical pathology; 2003. pp. 1–13.

    Google Scholar 

  18. Abate-Shen C, Shen MM. Molecular genetics of prostate cancer. Genes Dev. 2000;14(19):2410–34.

    CAS  PubMed  Google Scholar 

  19. Moller E, Adami HO, Mucci LA, Lundholm C, Bellocco R, Johansson JE, Gronberg H, Balter K. Lifetime body size and prostate cancer risk in a population-based case-control study in Sweden. Cancer Causes Control. 2013;24(12):2143–55.

    PubMed  Google Scholar 

  20. Sutcliffe S, Colditz GA. Prostate cancer: is it time to expand the research focus to early-life exposures? Nature Rev Cancer 2013;13(3):208–518.

    CAS  Google Scholar 

  21. Barker DJ. The fetal and infant origins of adult disease. BMJ. 1990;301(6761):1111.

    CAS  PubMed Central  PubMed  Google Scholar 

  22. Drake AJ, Reynolds RM. Impact of maternal obesity on offspring obesity and cardiometabolic disease risk. Reproduction. 2010;140(3):387–98.

    CAS  PubMed  Google Scholar 

  23. Ma RC, Chan JC, Tam WH, Hanson MA, Gluckman PD. Gestational diabetes, maternal obesity, and the NCD burden. Clin Obstet Gynecol. 2013;56(3):633–41.

    PubMed  Google Scholar 

  24. Galliano D, Bellver J. Female obesity: short- and long-term consequences on the offspring. Gynecol Endocrinol. 2013;29(7):626–31.

    PubMed  Google Scholar 

  25. Williams L, Seki Y, Vuguin PM, Charron MJ. Animal models of in utero exposure to a high fat diet: a review. Biochim Biophys Acta. 2014;1842(3):507–19.

    CAS  PubMed Central  PubMed  Google Scholar 

  26. Waddington CH. Epigenetics and evolution. Symp Soc Exp Biol. 1953;7:186–99.

    Google Scholar 

  27. Fukushige S, Horii A. DNA methylation in cancer: a gene silencing mechanism and the clinical potential of its biomarkers. Tohoku J Exp Med. 2013;229(3):173–85.

    CAS  PubMed  Google Scholar 

  28. Baylin SB, Jones PA. A decade of exploring the cancer epigenome—biological and translational implications. Nature Rev Cancer. 2011;11(10):726–34.

    CAS  Google Scholar 

  29. Holliday R, Pugh JE. DNA modification mechanisms and gene activity during development. Science. 1975;187(4173):226–32.

    CAS  PubMed  Google Scholar 

  30. Schapira F. DNA methylation and gene expression. Biomed Pharmacother. 1983;37(4):173–5.

    CAS  PubMed  Google Scholar 

  31. Christman JK, Price P, Pedrinan L, Acs G. Correlation between hypomethylation of DNA and expression of globin genes in Friend erythroleukemia cells. Eur J Biochem. 1977;81(1):53–61.

    CAS  PubMed  Google Scholar 

  32. Robertson KD. DNA methylation and human disease. Nature Rev Genet. 2005;6(8):597–610.

    CAS  PubMed  Google Scholar 

  33. Waterland RA, Jirtle RL. Early nutrition, epigenetic changes at transposons and imprinted genes, and enhanced susceptibility to adult chronic diseases. Nutrition. 2004;20(1):63–8.

    CAS  PubMed  Google Scholar 

  34. Williams K, Christensen J, Helin K. DNA methylation: TET proteins-guardians of CpG islands? EMBO Rep. 2012;13(1):28–35.

    CAS  PubMed Central  Google Scholar 

  35. Liu R, Leslie KL, Martin KA. Epigenetic regulation of smooth muscle cell plasticity. Biochim Biophys Acta. 2014;1849:448–53.

    PubMed  Google Scholar 

  36. Campbell NA, Reece JB. Biology. 6th edn. San Francisco: Benjamin Cummings; 2002. p. 87, 94–95, 125–7, 160, 172, 363–4, 984–92.

    Google Scholar 

  37. Bannister AJ, Kouzarides T. Regulation of chromatin by histone modifications. Cell Res. 2011;21(3):381–95.

    CAS  PubMed Central  PubMed  Google Scholar 

  38. Jenuwein T, Allis CD. Translating the histone code. Science. 2001;293(5532):1074–80.

    CAS  PubMed  Google Scholar 

  39. Song N, Liu J, An S, Nishino T, Hishikawa Y, Koji T. Immunohistochemical analysis of histone H3 modifications in germ cells during mouse spermatogenesis. Acta Histochem Cytochem. 2011;44(4):183–90.

    CAS  PubMed Central  PubMed  Google Scholar 

  40. Kouzarides T. Chromatin modifications and their function. Cell. 2007;128(4):693–705.

    CAS  PubMed  Google Scholar 

  41. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K. High-resolution profiling of histone methylations in the human genome. Cell. 2007;129(4):823–37.

    CAS  PubMed  Google Scholar 

  42. Strahl BD, Allis CD. The language of covalent histone modifications. Nature. 2000;403(6765):41–5.

    CAS  PubMed  Google Scholar 

  43. He L, Hannon GJ. MicroRNAs: small RNAs with a big role in gene regulation. Nature Rev Genet. 2004;5(7):522–31.

    CAS  PubMed  Google Scholar 

  44. Morozova N, Zinovyev A, Nonne N, Pritchard LL, Gorban AN, Harel-Bellan A. Kinetic signatures of microRNA modes of action. RNA. 2012;18(9):1635–55.

    CAS  PubMed Central  PubMed  Google Scholar 

  45. Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM, Castle J, Bartel DP, Linsley PS, Johnson JM. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature. 2005;433(7027):769–73.

    CAS  PubMed  Google Scholar 

  46. Yao B, Jin P. Unlocking epigenetic codes in neurogenesis. Genes Dev. 2014;28(12):1253–71.

    CAS  PubMed Central  PubMed  Google Scholar 

  47. Joh RI, Palmieri CM, Hill IT, Motamedi M. Regulation of histone methylation by noncoding RNAs. Biochim Biophys Acta. 2014;1839:1385–94.

    Google Scholar 

  48. Fall CH. Fetal programming and the risk of noncommunicable disease. Ind J Pediatr. 2013;80(Suppl 1):13–20.

    Google Scholar 

  49. Edwards TM, Myers JP. Environmental exposures and gene regulation in disease etiology. Environ Health Perspect. 2007;115(9):1264–70.

    CAS  PubMed Central  PubMed  Google Scholar 

  50. Plasschaert RN, Bartolomei MS. Genomic imprinting in development, growth, behavior and stem cells. Development. 2014;141(9):1805–13.

    CAS  PubMed Central  PubMed  Google Scholar 

  51. Reynolds EH. The neurology of folic acid deficiency. Handb Clin Neurol. 2014;120:927–43.

    CAS  PubMed  Google Scholar 

  52. Zhang S, Rattanatray L, McMillen IC, Suter CM, Morrison JL. Periconceptional nutrition and the early programming of a life of obesity or adversity. Prog Biophysics Mol Biol. 2011;106(1):307–14.

    CAS  Google Scholar 

  53. Damaschke NA, Yang B, Bhusari S, Svaren JP, Jarrard DF. Epigenetic susceptibility factors for prostate cancer with aging. Prostate. 2013;73(16):1721–30.

    CAS  PubMed Central  PubMed  Google Scholar 

  54. Bergman D, Halje M, Nordin M, Engstrom W. Insulin-like growth factor 2 in development and disease: a mini-review. Gerontology. 2013;59(3):240–49.

    CAS  PubMed  Google Scholar 

  55. Grindler NM, Moley KH. Maternal obesity, infertility and mitochondrial dysfunction: potential mechanisms emerging from mouse model systems. Mol Hum Reprod. 2013;19(8):486–94.

    CAS  Google Scholar 

  56. Hartil K, Vuguin PM, Kruse M, Schmuel E, Fiallo A, Vargas C, Warner MJ, Durand JL, Jelicks LA, Charron MJ. Maternal substrate utilization programs the development of the metabolic syndrome in male mice exposed to high fat in utero. Pediatr Res. 2009;66(4):368–73.

    CAS  PubMed Central  PubMed  Google Scholar 

  57. Barbour LA. Changing perspectives in pre-existing diabetes and obesity in pregnancy: maternal and infant short and long-term outcomes. Curr Opin Endocrinol Diabetes Obes. 2014;21:257–63.

    Google Scholar 

  58. Klimek P, Leitner M, Kautzky-Willer A, Thurner S. Effect of fetal and infant malnutrition on metabolism in older age. Gerontology. 2014;60:502–7.

    Google Scholar 

  59. Li CC, Young PE, Maloney CA, Eaton SA, Cowley MJ, Buckland ME, Preiss T, Henstridge DC, Cooney GJ, Febbraio MA, Martin DI, Cropley JE, Suter CM. Maternal obesity and diabetes induces latent metabolic defects and widespread epigenetic changes in isogenic mice. Epigenetics. 2013;8(6):602–11.

    CAS  PubMed Central  PubMed  Google Scholar 

  60. Heerwagen MJ, Miller MR, Barbour LA, Friedman JE. Maternal obesity and fetal metabolic programming: a fertile epigenetic soil. Am J Physiol Regul Integr Comp Physiol. 2010;299(3):R711–22.

    CAS  PubMed Central  PubMed  Google Scholar 

  61. Turdi S, Ge W, Hu N, Bradley KM, Wang X, Ren J. Interaction between maternal and postnatal high fat diet leads to a greater risk of myocardial dysfunction in offspring via enhanced lipotoxicity, IRS-1 serine phosphorylation and mitochondrial defects. J Mol Cell Cardiol. 2013;55:117–29.

    CAS  PubMed  Google Scholar 

  62. Hoile SP, Irvine NA, Kelsall CJ, Sibbons C, Feunteun A, Collister A, Torrens C, Calder PC, Hanson MA, Lillycrop KA, Burdge GC. Maternal fat intake in rats alters 20:4n-6 and 22:6n-3 status and the epigenetic regulation of Fads2 in offspring liver. J Nutr Biochem. 2013;24(7):1213–20.

    CAS  PubMed Central  PubMed  Google Scholar 

  63. Masuyama H, Hiramatsu Y. Effects of a high-fat diet exposure in utero on the metabolic syndrome-like phenomenon in mouse offspring through epigenetic changes in adipocytokine gene expression. Endocrinology. 2012;153(6):2823–30.

    CAS  PubMed  Google Scholar 

  64. Wang Q, Ratchford AM, Chi MM, Schoeller E, Frolova A, Schedl T, Moley KH. Maternal diabetes causes mitochondrial dysfunction and meiotic defects in murine oocytes. Mol Endocrinol. 2009;23(10):1603–12.

    CAS  PubMed Central  PubMed  Google Scholar 

  65. Phelan S. Smoking cessation in pregnancy. Obstet Gynecol Clin North Am. 2014;41(2):255–66.

    PubMed  Google Scholar 

  66. Bhattacharya S, Campbell DM, Liston WA, Bhattacharya S. Effect of body mass index on pregnancy outcomes in nulliparous women delivering singleton babies. BMC Public Health. 2007;7:168.

    PubMed Central  PubMed  Google Scholar 

  67. Watkins ML, Rasmussen SA, Honein MA, Botto LD, Moore CA. Maternal obesity and risk for birth defects. Pediatrics. 2003;111(5 Pt 2):1152–58.

    PubMed  Google Scholar 

  68. Odell LD, Mengert WF. The overweight obstetric patient. JAMA. 1945;128(2):87–90.

    Google Scholar 

  69. Aune D, Saugstad OD, Henriksen T, Tonstad S. Maternal body mass index and the risk of fetal death, stillbirth, and infant death: a systematic review and meta-analysis. JAMA. 2014;311(15):1536–46.

    CAS  PubMed  Google Scholar 

  70. Rasmussen KM, Yaktine AL, editors. Weight gain during pregnancy: reexamining the guidelines. The National Academies Collection: Reports funded by National Institutes of Health. Washington, DC. 2009.

    Google Scholar 

  71. James WP. WHO recognition of the global obesity epidemic. Int J Obes. 2008;32(Suppl 7):120–6.

    Google Scholar 

  72. American College of Obstetricians and Gynecologists. ACOG Committee opinion no. 549: obesity in pregnancy. Obstet Gynecol. 2013;121(1):213–7.

    Google Scholar 

  73. Prevention CfDCa. Pregnancy complications. 2014. http://www.cdc.gov/reproductivehealth/maternalinfanthealth/pregcomplications.htm. Accessed 05 April 2014.

  74. Thompson ML, Ananth CV, Jaddoe VW, Miller RS, Williams MA. The association of maternal adult weight trajectory with preeclampsia and gestational diabetes mellitus. Paediatr Prenat Epidemiol. 2014;28(4):287–96.

    Google Scholar 

  75. Elhddad AS, Fairlie F, Lashen H. Impact of gestational weight gain on fetal growth in obese normoglycemic mothers: a comparative study. Acta Obstet Gynecol Scand. 2014;98:771–7.

    Google Scholar 

  76. Lashen H, Fear K, Sturdee DW. Obesity is associated with increased risk of first trimester and recurrent miscarriage: matched case-control study. Hum Reprod. 2004;19(7):1644–6.

    CAS  PubMed  Google Scholar 

  77. Sebire NJ, Jolly M, Harris JP, Wadsworth J, Joffe M, Beard RW, Regan L, Robinson S. Maternal obesity and pregnancy outcome: a study of 287,213 pregnancies in London. Int J Obes Relat Metab Disord. 2001;25(8):1175–82.

    CAS  PubMed  Google Scholar 

  78. Li R, Jewell S, Grummer-Strawn L. Maternal obesity and breast-feeding practices. Am J Clin Nutr. 2003;77(4):931–6.

    CAS  PubMed  Google Scholar 

  79. Tenenbaum-Gavish K, Hod M. Impact of maternal obesity on fetal health. Fetal Diagn Ther. 2013;34(1):1–7.

    PubMed  Google Scholar 

  80. Walsh JM, McAuliffe FM. Prediction and prevention of the macrosomic fetus. Eur J Obstet Gynecol Reprod Biol. 2012;162(2):125–30.

    PubMed  Google Scholar 

  81. Stothard KJ, Tennant PW, Bell R, Rankin J. Maternal overweight and obesity and the risk of congenital anomalies: a systematic review and meta-analysis. JAMA. 2009;301(6):636–50.

    CAS  PubMed  Google Scholar 

  82. Matthews TJ, MacDorman MF. Infant mortality statistics from the 2010 period linked birth/infant death data set. Natl Vital Stat Rep (from the Centers for Disease Control and Prevention, National Center for Health Statistics, National Vital Statistics System). 2013;62(8):1–26.

    CAS  Google Scholar 

  83. Patro B, Liber A, Zalewski B, Poston L, Szajewska H, Koletzko B. Maternal and paternal body mass index and offspring obesity: a systematic review. Ann Nutr Metab. 2013;63(1–2):32–41.

    CAS  PubMed  Google Scholar 

  84. Catalano PM, McIntyre HD, Cruickshank JK, McCance DR, Dyer AR, Metzger BE, Lowe LP, Trimble ER, Coustan DR, Hadden DR, Persson B, Hod M, Oats JJ, Group HSCR. The hyperglycemia and adverse pregnancy outcome study: associations of GDM and obesity with pregnancy outcomes. Diabetes Care. 2012;35(4):780–6.

    CAS  PubMed Central  PubMed  Google Scholar 

  85. Gaillard R, Steegers EA, Duijts L, Felix JF, Hofman A, Franco OH, Jaddoe VW. Childhood cardiometabolic outcomes of maternal obesity during pregnancy: the Generation R Study. Hypertension. 2014;63(4):683–91.

    CAS  PubMed  Google Scholar 

  86. Brumbaugh DE, Tearse P, Cree-Green M, Fenton LZ, Brown M, Scherzinger A, Reynolds R, Alston M, Hoffman C, Pan Z, Friedman JE, Barbour LA. Intrahepatic fat is increased in the neonatal offspring of obese women with gestational diabetes. J Pediatr. 2013;162(5):930–6.e1.

    CAS  PubMed Central  PubMed  Google Scholar 

  87. Guenard F, Tchernof A, Deshaies Y, Cianflone K, Kral JG, Marceau P, Vohl MC. Methylation and expression of immune and inflammatory genes in the offspring of bariatric bypass surgery patients. J Obes. 2013;2013:492170.

    PubMed Central  PubMed  Google Scholar 

  88. Desai M, Gayle D, Han G, Ross MG. Programmed hyperphagia due to reduced anorexigenic mechanisms in intrauterine growth-restricted offspring. Reprod Sci. 2007;14(4):329–37.

    PubMed  Google Scholar 

  89. Taylor PD, Samuelsson AM, Poston L. Maternal obesity and the developmental programming of hypertension: a role for leptin. Acta Physiol. 2014;210(3):508–23.

    CAS  Google Scholar 

  90. Bird A. Perceptions of epigenetics. Nature. 2007;447(7143):396–8.

    CAS  PubMed  Google Scholar 

  91. Ge ZJ, Zhang CL, Schatten H, Sun QY. Maternal diabetes mellitus and the origin of non-communicable diseases in offspring: the role of epigenetics. Biol Reprod. 2014;90:139.

    Google Scholar 

  92. Ruchat SM, Houde AA, Voisin G, St-Pierre J, Perron P, Baillargeon JP, Gaudet D, Hivert MF, Brisson D, Bouchard L. Gestational diabetes mellitus epigenetically affects genes predominantly involved in metabolic diseases. Epigenetics. 2013;8(9):935–43.

    CAS  PubMed Central  PubMed  Google Scholar 

  93. Robinson S, Yardy K, Carter V. A narrative literature review of the development of obesity in infancy and childhood. J Child Health Care. 2012;16(4):339–54.

    PubMed  Google Scholar 

  94. Sullivan EL, Nousen EK, Chamlou KA. Maternal high fat diet consumption during the perinatal period programs offspring behavior. Physiol Behav. 2014;123:236–42.

    CAS  PubMed  Google Scholar 

  95. Breton C. The hypothalamus-adipose axis is a key target of developmental programming by maternal nutritional manipulation. J Endocrinol. 2013;216(2):R19–31.

    CAS  PubMed  Google Scholar 

  96. Lukaszewski MA, Eberle D, Vieau D, Breton C. Nutritional manipulations in the perinatal period program adipose tissue in offspring. Am J Physiol Endocrinol Metab. 2013;305 (10):E1195–207.

    CAS  PubMed  Google Scholar 

  97. O’Reilly JR, Reynolds RM. The risk of maternal obesity to the long-term health of the offspring. Clin Endocrinol. 2013;78(1):9–16.

    Google Scholar 

  98. Suburu J, Chen YQ. Lipids and prostate cancer. Prostaglandins Other Lipid Mediat. 2012;98(1–2):1–10.

    CAS  PubMed Central  PubMed  Google Scholar 

  99. Sanderson M, Williams MA, Malone KE, Stanford JL, Emanuel I, White E, Daling JR. Perinatal factors and risk of breast cancer. Epidemiology. 1996;7(1):34–7.

    CAS  PubMed  Google Scholar 

  100. Sanderson M, Williams MA, Daling JR, Holt VL, Malone KE, Self SG, Moore DE. Maternal factors and breast cancer risk among young women. Paediatr Perinat Epidemiol. 1998;12(4):397–407.

    CAS  PubMed  Google Scholar 

  101. Wilson KM, Willett WC, Michels KB. Mothers’ pre-pregnancy BMI and weight gain during pregnancy and risk of breast cancer in daughters. Breast Cancer Res Treat. 2011;130(1):273–9.

    PubMed Central  PubMed  Google Scholar 

  102. Michels KB, Trichopoulos D, Robins JM, Rosner BA, Manson JE, Hunter DJ, Colditz GA, Hankinson SE, Speizer FE, Willett WC. Birthweight as a risk factor for breast cancer. Lancet. 1996;348(9041):1542–46.

    CAS  PubMed  Google Scholar 

  103. Park SK, Kang D, McGlynn KA, Garcia-Closas M, Kim Y, Yoo KY, Brinton LA. Intrauterine environments and breast cancer risk: meta-analysis and systematic review. Breast Cancer Res. 2008;10(1):R8.

    PubMed Central  PubMed  Google Scholar 

  104. Yenbutr P, Hilakivi-Clarke L, Passaniti A. Hypomethylation of an exon I estrogen receptor CpG island in spontaneous and carcinogen-induced mammary tumorigenesis in the rat. Mech Ageing Dev. 1998;106(1–2):93–102.

    CAS  PubMed  Google Scholar 

  105. La Merrill M, Harper R, Birnbaum LS, Cardiff RD, Threadgill DW. Maternal dioxin exposure combined with a diet high in fat increases mammary cancer incidence in mice. Environ Health Perspect. 2010;118(5):596–601.

    PubMed Central  PubMed  Google Scholar 

  106. Hilakivi-Clarke L, Clarke R, Onojafe I, Raygada M, Cho E, Lippman M. A maternal diet high in n−6 polyunsaturated fats alters mammary gland development, puberty onset, and breast cancer risk among female rat offspring. Proc Natl Acad Sci U S A. 1997;94(17):9372–7.

    CAS  PubMed Central  PubMed  Google Scholar 

  107. de Assis S, Warri A, Cruz MI, Laja O, Tian Y, Zhang B, Wang Y, Huang TH, Hilakivi-Clarke L. High-fat or ethinyl-oestradiol intake during pregnancy increases mammary cancer risk in several generations of offspring. Nat Commun. 2012;3:1053.

    PubMed Central  PubMed  Google Scholar 

  108. Lo CY, Hsieh PH, Chen HF, Su HM. A maternal high-fat diet during pregnancy in rats results in a greater risk of carcinogen-induced mammary tumors in the female offspring than exposure to a high-fat diet in postnatal life. Int J Cancer. 2009;125(4):767–73.

    CAS  PubMed  Google Scholar 

  109. Su HM, Hsieh PH, Chen HF. A maternal high n-6 fat diet with fish oil supplementation during pregnancy and lactation in rats decreases breast cancer risk in the female offspring. J Nutr Biochem. 2010;21(11):1033–7.

    CAS  PubMed  Google Scholar 

  110. de Oliveira Andrade F, Fontelles CC, Rosim MP, de Oliveira TF, de Melo Loureiro AP, Mancini-Filho J, Rogero MM, Moreno FS, de Assis S, Barbisan LF, Hilakivi-Clarke L, Ong TP. Exposure to lard-based high-fat diet during fetal and lactation periods modifies breast cancer susceptibility in adulthood in rats. J Nutr Biochem 2014;25(6):613–22.

    PubMed  Google Scholar 

  111. Montales MT, Melnyk SB, Simmen FA, Simmen RC. Maternal metabolic perturbations elicited by high-fat diet promote Wnt-1-induced mammary tumor risk in adult female offspring via long-term effects on mammary and systemic phenotypes. Carcinogenesis. 2014;35:2012–12.

    Google Scholar 

  112. Kerdivel G, Flouriot G, Pakdel F. Modulation of estrogen receptor alpha activity and expression during breast cancer progression. Vitam Horm. 2013;93:135–60.

    CAS  PubMed  Google Scholar 

  113. Burton A, Martin R, Galobardes B, Davey Smith G, Jeffreys M. Young adulthood body mass index and risk of cancer in later adulthood: historical cohort study. Cancer Causes Control. 2010;21(12):2069–77.

    PubMed  Google Scholar 

  114. Dal Maso L, Zucchetto A, La Vecchia C, Montella M, Conti E, Canzonieri V, Talamini R, Tavani A, Negri E, Garbeglio A, Franceschi S. Prostate cancer and body size at different ages: an Italian multicentre case-control study. Br J Cancer. 2004;90(11):2176–80.

    CAS  PubMed  Google Scholar 

  115. Schuurman AG, Goldbohm RA, Dorant E, van den Brandt PA. Anthropometry in relation to prostate cancer risk in the Netherlands cohort study. Am J Epidemiol. 2000;151(6):541–9.

    CAS  PubMed  Google Scholar 

  116. Giovannucci E, Rimm EB, Stampfer MJ, Colditz GA, Willett WC. Height, body weight, and risk of prostate cancer. Cancer Epidemiol Biomarkers Prev (a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology). 1997;6(8):557–63.

    CAS  PubMed  Google Scholar 

  117. Robinson WR, Stevens J, Gammon MD, John EM. Obesity before age 30 years and risk of advanced prostate cancer. Am J Epidemiol. 2005;161(12):1107–14.

    PubMed  Google Scholar 

  118. Discacciati A, Orsini N, Andersson SO, Andren O, Johansson JE, Wolk A. Body mass index in early and middle-late adulthood and risk of localised, advanced and fatal prostate cancer: a population-based prospective study. Br J Cancer. 2011;105(7):1061–68.

    CAS  PubMed Central  PubMed  Google Scholar 

  119. Barker DJ, Osmond C, Thornburg KL, Kajantie E, Eriksson JG. A possible link between the pubertal growth of girls and prostate cancer in their sons. Am J Hum Biol. 2012;24(4):406–10.

    PubMed Central  PubMed  Google Scholar 

  120. Ekstrom S, Magnusson J, Kull I, Lind T, Almqvist C, Melen E, Bergstrom A. Maternal BMI in early pregnancy and offspring asthma, rhinitis and eczema up to 16 years of age. Clin Exp Allergy. 2014;45:283–91.

    Google Scholar 

  121. Ekbom A, Hsieh CC, Lipworth L, Wolk A, Ponten J, Adami HO, Trichopoulos D. Perinatal characteristics in relation to incidence of and mortality from prostate cancer. BMJ. 1996;13(7053):337–41.

    Google Scholar 

  122. Ikeda Y, Cho YM, Takahashi S, Tang M, Asamoto M, Ogawa K, Shirai T. Equivocal impact of transplacental and lactational exposure to a food-derived carcinogen, 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine, on prostate and colon lesion development in F344 rats. Cancer Lett. 2005;224(1):23–30.

    CAS  PubMed  Google Scholar 

  123. Kondo Y, Homma Y, Aso Y, Kakizoe T. Promotional effect of two-generation exposure to a high-fat diet on prostate carcinogenesis in ACI/Seg rats. Cancer Res. 1994;54(23):6129–32.

    CAS  PubMed  Google Scholar 

  124. Tobisu K, Kakizoe T, Tanaka Y, Takai K, Shirai T. Influence of dietary fat and total calorie intake on the incidence of spontaneous prostatic cancer. Proceeding of the First Workshop on Prostatic Cancer; 1990; Shalom Co., Tokyo.

    Google Scholar 

  125. Benesh EC, Humphrey PA, Wang Q, Moley KH. Maternal high-fat diet induces hyperproliferation and alters Pten/Akt signaling in prostates of offspring. Sci Rep. 2013;3:3466.

    PubMed Central  PubMed  Google Scholar 

  126. Rinaldi JC, Justulin LA Jr, Lacorte LM, Sarobo C, Boer PA, Scarano WR, Felisbino SL. Implications of intrauterine protein malnutrition on prostate growth, maturation and aging. Life Sci. 2013;92(13):763–74.

    CAS  PubMed  Google Scholar 

  127. Ramos Cda F, Babinski MA, Costa WS, Sampaio FJ. The prostate of weaned pups is altered by maternal malnutrition during lactation in rats. Asian J Androl. 2010;12(2):180–5.

    PubMed  Google Scholar 

  128. Eriksson JG, Sandboge S, Salonen MK, Kajantie E, Osmond C. Long-term consequences of maternal overweight in pregnancy on offspring later health: findings from the Helsinki Birth Cohort Study. Ann Med. 2014;46:434–8.

    Google Scholar 

  129. Walker BE. Tumors in female offspring of control and diethylstilbestrol-exposed mice fed high-fat diets. J Natl Cancer Inst. 1990;82(1):50–4.

    CAS  PubMed  Google Scholar 

  130. Simmen FA, Simmen RC. The maternal womb: a novel target for cancer prevention in the era of the obesity pandemic? Eur J Cancer Prev (the official journal of the European Cancer Prevention Organisation). 2011;20(6):539–48.

    PubMed Central  PubMed  Google Scholar 

  131. Colton SA, Pieper GM, Downs SM. Altered meiotic regulation in oocytes from diabetic mice. Biol Reprod. 2002;67(1):220–31.

    CAS  PubMed  Google Scholar 

  132. Luzzo KM, Wang Q, Purcell SH, Chi M, Jimenez PT, Grindler N, Schedl T, Moley KH. High fat diet induced developmental defects in the mouse: oocyte meiotic aneuploidy and fetal growth retardation/brain defects. PloS One. 2012;7(11):e49217.

    CAS  PubMed Central  PubMed  Google Scholar 

  133. Minge CE, Bennett BD, Norman RJ, Robker RL. Peroxisome proliferator-activated receptor-gamma agonist rosiglitazone reverses the adverse effects of diet-induced obesity on oocyte quality. Endocrinology. 2008;149(5):2646–56.

    CAS  PubMed  Google Scholar 

  134. Cunningham FG, Williams JW. Williams obstetrics. 21st edn. New York: McGraw-Hill; 2001. p. 86–89, 130–134.

    Google Scholar 

  135. Racki WJ, Richter JD. CPEB controls oocyte growth and follicle development in the mouse. Development. 2006;133(22):4527–37.

    CAS  PubMed  Google Scholar 

  136. Behringer R. Manipulating the mouse embryo: a laboratory manual. 4th edn. New York: Cold Spring Harbor Laboratory Press, Cold Spring Harbor; 2014.

    Google Scholar 

  137. Chang AS, Dale AN, Moley KH. Maternal diabetes adversely affects preovulatory oocyte maturation, development, and granulosa cell apoptosis. Endocrinology. 2005;146(5):2445–53.

    CAS  PubMed  Google Scholar 

  138. Diamond MP, Moley KH, Pellicer A, Vaughn WK, DeCherney AH. Effects of streptozotocin- and alloxan-induced diabetes mellitus on mouse follicular and early embryo development. J Reprod Fertil. 1989;86(1):1–10.

    CAS  PubMed  Google Scholar 

  139. Moley KH, Vaughn WK, DeCherney AH, Diamond MP. Effect of diabetes mellitus on mouse pre-implantation embryo development. J Reprod Fertil. 1991;93(2):325–32.

    CAS  PubMed  Google Scholar 

  140. Moley KH, Vaughn WK, Diamond MP. Manifestations of diabetes mellitus on mouse preimplantation development: effect of elevated concentration of metabolic intermediates. Hum Reprod. 1994;9(1):113–21.

    CAS  PubMed  Google Scholar 

  141. Ratchford AM, Chang AS, Chi MM, Sheridan R, Moley KH. Maternal diabetes adversely affects AMP-activated protein kinase activity and cellular metabolism in murine oocytes. Am J Physiol Endocrinol Metab. 2007;293(5):E1198–206.

    CAS  PubMed  Google Scholar 

  142. Chi MM, Hoehn A, Moley KH. Metabolic changes in the glucose-induced apoptotic blastocyst suggest alterations in mitochondrial physiology. Am J Physiol Endocrinol Metab. 2002;283(2):E226–32.

    CAS  PubMed  Google Scholar 

  143. Moley KH, Chi MM, Knudson CM, Korsmeyer SJ, Mueckler MM. Hyperglycemia induces apoptosis in pre-implantation embryos through cell death effector pathways. Nature Med. 1998;4(12):1421–4.

    CAS  PubMed  Google Scholar 

  144. Moley KH, Chi MM, Mueckler MM. Maternal hyperglycemia alters glucose transport and utilization in mouse preimplantation embryos. Am J Physiol. 1998;275(1 Pt 1):E38–47.

    CAS  Google Scholar 

  145. Wyman A, Pinto AB, Sheridan R, Moley KH. One-cell zygote transfer from diabetic to nondiabetic mouse results in congenital malformations and growth retardation in offspring. Endocrinology. 2008;149(2):466–9.

    CAS  PubMed Central  PubMed  Google Scholar 

  146. Wang Q, Frolova AI, Purcell S, Adastra K, Schoeller E, Chi MM, Schedl T, Moley KH. Mitochondrial dysfunction and apoptosis in cumulus cells of type I diabetic mice. PloS One. 2010;5(12):e15901.

    CAS  PubMed Central  PubMed  Google Scholar 

  147. Wang Q, Chi MM, Moley KH. Live imaging reveals the link between decreased glucose uptake in ovarian cumulus cells and impaired oocyte quality in female diabetic mice. Endocrinology. 2012;153(4):1984–9.

    CAS  PubMed Central  PubMed  Google Scholar 

  148. Wang Q, Chi MM, Schedl T, Moley KH. An intercellular pathway for glucose transport into mouse oocytes. Am J Physiol Endocrinol Metab. 2012;302(12):E1511–8.

    CAS  PubMed Central  PubMed  Google Scholar 

  149. Jungheim ES, Schoeller EL, Marquard KL, Louden ED, Schaffer JE, Moley KH. Diet-induced obesity model: abnormal oocytes and persistent growth abnormalities in the offspring. Endocrinology. 2010;151(8):4039–46.

    CAS  PubMed Central  PubMed  Google Scholar 

  150. Bermejo-Alvarez P, Rosenfeld CS, Roberts RM. Effect of maternal obesity on estrous cyclicity, embryo development and blastocyst gene expression in a mouse model. Hum Reprod. 2012;27(12):3513–22.

    CAS  PubMed Central  PubMed  Google Scholar 

  151. Igosheva N, Abramov AY, Poston L, Eckert JJ, Fleming TP, Duchen MR, McConnell J. Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes. PloS One. 2012;5(4):e10074.

    Google Scholar 

  152. Shankar K, Zhong Y, Kang P, Lau F, Blackburn ML, Chen JR, Borengasser SJ, Ronis MJ, Badger TM. Maternal obesity promotes a proinflammatory signature in rat uterus and blastocyst. Endocrinology. 2011;152(11):4158–70.

    CAS  PubMed Central  PubMed  Google Scholar 

  153. Jungheim ES, Louden ED, Chi MM, Frolova AI, Riley JK, Moley KH. Preimplantation exposure of mouse embryos to palmitic acid results in fetal growth restriction followed by catch-up growth in the offspring. Biol Reprod. 2011;85(4):678–83.

    CAS  PubMed Central  PubMed  Google Scholar 

  154. Bernal AB, Vickers MH, Hampton MB, Poynton RA, Sloboda DM. Maternal undernutrition significantly impacts ovarian follicle number and increases ovarian oxidative stress in adult rat offspring. PloS One. 2010;5(12):e15558.

    CAS  PubMed Central  PubMed  Google Scholar 

  155. Luke B, Brown MB, Missmer SA, Bukulmez O, Leach R, Stern JE, Society for Assisted Reproductive Technology writing group. The effect of increasing obesity on the response to and outcome of assisted reproductive technology: a national study. Fertil Steril. 2011;96(4):820–85.

    PubMed  Google Scholar 

  156. Jungheim ES, Schon SB, Schulte MB, DeUgarte DA, Fowler SA, Tuuli MG. IVF outcomes in obese donor oocyte recipients: a systematic review and meta-analysis. Hum Reprod. 2013;28(10):2720–7.

    CAS  PubMed Central  PubMed  Google Scholar 

  157. Machtinger R, Combelles CM, Missmer SA, Correia KF, Fox JH, Racowsky C. The association between severe obesity and characteristics of failed fertilized oocytes. Hum Reprod. 2012;27(11):3198–207.

    CAS  PubMed  Google Scholar 

  158. Hilakivi-Clarke L, Cho E, deAssis S, Olivo S, Ealley E, Bouker KB, Welch JN, Khan G, Clarke R, Cabanes A. Maternal and prepubertal diet, mammary development and breast cancer risk. J Nutr. 2001;131(1):154S–7S.

    Google Scholar 

  159. Zadra G, Photopoulos C, Loda M. The fat side of prostate cancer. Biochim Biophys Acta. 2013;1831(10):1518–32.

    CAS  PubMed Central  PubMed  Google Scholar 

  160. Chiam K, Ricciardelli C, Bianco-Miotto T. Epigenetic biomarkers in prostate cancer: current and future uses. Cancer Lett. 2014;342(2):248–56.

    CAS  PubMed  Google Scholar 

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Acknowledgements

K.H.M. and E.C.B. were supported by the Washington University Transdisciplinary Research in Energetics and Cancer Program Grant (NCI; U54 CA 155496). E.C.B. was funded by the Washington University Department of Pathology Training Grant (5T32 DK 7296-33) and the Washington University Institute of Clinical and Translational Sciences grant UL1 TR000448 from the National Center for Advancing Translational Sciences. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institute of Health (NIH). We thank Dr. Deborah Frank for suggestions on the manuscript and Michaela Reid for assistance with bibliography generation.

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Benesh, E., Moley, K. (2015). Maternal Energetics and the Developmental Origins of Prostate Cancer in Offspring. In: Berger, N. (eds) Murine Models, Energy Balance, and Cancer. Energy Balance and Cancer, vol 10. Springer, Cham. https://doi.org/10.1007/978-3-319-16733-6_11

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