Skip to main content
SpringerLink
Log in

Developmental Origins of Breast Cancer: A Paternal Perspective

  • Protocol
  • First Online:
Investigations of Early Nutrition Effects on Long-Term Health

Part of the book series: Methods in Molecular Biology ((MIMB,volume 1735))

Abstract

The developmental origins of breast cancer have been considered predominantly from a maternal perspective. Although accumulating evidence suggests a paternal programming effect on metabolic diseases, the potential impact of fathers’ experiences on their daughters’ breast cancer risk has received less attention. In this chapter, we focus on the developmental origins of breast cancer and examine the emerging evidence for a role of fathers’ experiences.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 79.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 99.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 129.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Oeffinger KC, Fontham ET, Etzioni R, Herzig A, Michaelson JS, Shih YC et al (2015) Breast cancer screening for women at average risk. JAMA 314:1599–1614

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M et al (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136:E359–E386

    Article  CAS  PubMed  Google Scholar 

  3. Lee BL, Liedke PE, Barrios CH, Simon SD, Finkelstein DM, Goss PE (2012) Breast cancer in Brazil: present status and future goals. Lancet Oncol 13:e95–102

    Article  PubMed  Google Scholar 

  4. Colditz GA, Bohlke K, Berkey CS (2014) Breast cancer risk accumulation starts early: prevention must also. Breast Cancer Res Treat 145:567–579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Hilakivi-Clarke L (2007) Nutritional modulation of terminal end buds: its relevance to breast cancer prevention. Curr Cancer Drug Targets 7:465–474

    Article  CAS  PubMed  Google Scholar 

  6. Oakes SR, Gallego-Ortega D, Ormandy CJ (2014) The mammary cellular hierarchy and breast cancer. Cell Mol Life Sci 71:4301–4324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Russo J (2015) Significance of rat mammary tumors for human risk assessment. Toxicol Pathol 43:145–170

    Article  CAS  PubMed  Google Scholar 

  8. Hilakivi-Clarke L, de Assis S (2006) Fetal origins of breast cancer. Trends Endocrinol Metab 17:340–348

    Article  CAS  PubMed  Google Scholar 

  9. de Assis S, Wang M, Jin L, Bouker KB, Hilakivi-Clarke LA (2013) Exposure to excess estradiol or leptin during pregnancy increases mammary cancer risk and prevents parity-induced protective genomic changes in rats. Cancer Prev Res 6:1194–1211

    Article  Google Scholar 

  10. de Oliveira Andrade F, Fontelles CC, Rosim MP, de Oliveira TF, de Melo Loureiro AP, Mancini-Filho J et al (2014) Exposure to lard-based high-fat diet during fetal and lactation periods modifies breast cancer susceptibility in adulthood in rats. J Nutr Biochem 25:613–622

    Article  PubMed  PubMed Central  Google Scholar 

  11. Soto AM, Brisken C, Schaeberle C, Sonnenschein C (2013) Does cancer start in the womb? Altered mammary gland development and predisposition to breast cancer due to in utero exposure to endocrine disruptors. J Mammary Gland Biol Neoplasia 18:199–208

    Article  PubMed  PubMed Central  Google Scholar 

  12. Osborne G, Rudel R, Schwarzman M (2015) Evaluating chemical effects on mammary gland development: a critical need in disease prevention. Reprod Toxicol 54:148–155

    Article  CAS  PubMed  Google Scholar 

  13. Barker DJ, Gluckman PD, Godfrey KM, Harding JE, Owens JA, Robinson JS (1993) Fetal nutrition and cardiovascular disease in adult life. Lancet 341:938–941

    Article  CAS  PubMed  Google Scholar 

  14. Trichopoulos D (1990) Is breast cancer initiated in utero? Epidemiology 1:95–96

    Article  CAS  PubMed  Google Scholar 

  15. Hilakivi-Clarke L, Clarke R, Onojafe I, Raygada M, Cho E, Lippman M (1997) 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 94:9372–9377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Hilakivi-Clarke L, Clarke R, Lippman M (1999) The influence of maternal diet on breast cancer risk among female offspring. Nutrition15:392–401

    Google Scholar 

  17. de Assis S, Hilakivi-Clarke L (2006) Timing of dietary estrogenic exposures and breast cancer risk. Ann N Y Acad Sci 1089:14–35

    Article  PubMed  Google Scholar 

  18. Troisi R, Potischman N, Hoover RN (2007) Exploring the underlying hormonal mechanisms of prenatal risk factors for breast cancer: a review and commentary. Cancer Epidemiol Biomark Prev 16:1700–1712

    Article  CAS  Google Scholar 

  19. Hill J, Hodsdon W (2014) In utero exposure and breast cancer development: an epigenetic perspective. J Environ Pathol Toxicol Oncol 33:239–245

    Article  PubMed  Google Scholar 

  20. Bukowski R, Chlebowski RT, Thune I, Furberg AS, Hankins GD, Malone FD et al (2012) Birth weight, breast cancer and the potential mediating hormonal environment. PLoS One 7(7):e40199. https://doi.org/10.1371/journal.pone.0040199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Swerdlow AJ, De Stavola BL, Swanwick MA, Maconochie NE (1997) Risks of breast and testicular cancers in young adult twins in England and Wales: evidence on prenatal and genetic aetiology. Lancet 350:1723–1728

    Article  CAS  PubMed  Google Scholar 

  22. Xue F, Michels KB (2007) Intrauterine factors and risk of breast cancer: a systematic review and meta-analysis of current evidence. Lancet Oncol 8:1088–1100

    Article  PubMed  Google Scholar 

  23. Palmer JR, Wise LA, Hatch EE, Troisi R, Titus-Ernstoff L, Strohsnitter W et al (2006) Prenatal diethylstilbestrol exposure and risk of breast cancer. Cancer Epidemiol Biomark Prev 15:1509–1514

    Article  CAS  Google Scholar 

  24. Cohn BA, La Merrill M, Krigbaum NY, Yeh G, Park JS, Zimmermann L et al (2015) DDT exposure in utero and breast cancer. J Clin Endocrinol Metab 100:2865–2872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Hilakivi-Clarke L (2014) Maternal exposure to diethylstilbestrol during pregnancy and increased breast cancer risk in daughters. Breast Cancer Res 16:208

    Article  PubMed  PubMed Central  Google Scholar 

  26. MacLennan M, Ma DW (2010) Role of dietary fatty acids in mammary gland development and breast cancer. Breast Cancer Res 12:211

    Article  PubMed  PubMed Central  Google Scholar 

  27. de Assis S, Khan G, Hilakivi-Clarke L (2006) High birth weight increases mammary tumorigenesis in rats. Int J Cancer 119:1537–1546

    Article  PubMed  Google Scholar 

  28. Fernandez-Twinn DS, Ekizoglou S, Gusterson BA, Luan J, Ozanne SE (2007) Compensatory mammary growth following protein restriction during pregnancy and lactation increases early-onset mammary tumor incidence in rats. Carcinogenesis 28:545–552

    Article  CAS  PubMed  Google Scholar 

  29. Fernandez-Twinn DS, Ekizoglou S, Martin-Gronert MS, Tarry-Adkins J, Wayman AP, Warner MJ et al (2010) Poor early growth and excessive adult calorie intake independently and additively affect mitogenic signaling and increase mammary tumor susceptibility. Carcinogenesis 31:1873–1881

    Article  CAS  PubMed  Google Scholar 

  30. de Assis S, Wang M, Goel S, Foxworth A, Helferich W, Hilakivi-Clarke L et al (2006) Excessive weight gain during pregnancy increases carcinogen-induced mammary tumorigenesis in Sprague-Dawley and lean and obese Zucker rats. J Nutr 136:998–1004

    Article  PubMed  Google Scholar 

  31. de Oliveira Andrade F, de Assis S, Jin L, Fontelles CC, Barbisan LF, Purgatto E et al (2015) Lipidomic fatty acid profile and global gene expression pattern in mammary gland of rats that were exposed to lard-based high fat diet during fetal and lactation periods associated to breast cancer risk in adulthood. Chem Biol Interact 239:118–128

    Article  Google Scholar 

  32. Ferguson-Smith AC, Patti ME (2011) You are what your dad ate. Cell Metab 13:115–117

    Article  CAS  PubMed  Google Scholar 

  33. Lane M, Robker RL, Robertson SA (2014) Parenting from before conception. Science 345:756–760

    Article  CAS  PubMed  Google Scholar 

  34. Soubry A, Hoyo C, Jirtle RL, Murphy SK (2014) A paternal environmental legacy: evidence for epigenetic inheritance through the male germ line. BioEssays 36:359–371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Hur SS, Cropley JE, Suter CM (2017) Paternal epigenetic programming: evolving metabolic disease risk. J Mol Endocrinol 58:R159–R168

    Article  CAS  PubMed  Google Scholar 

  36. Carrell DT, Hammoud SS (2010) The human sperm epigenome and its potential role in embryonic development. Mol Hum Reprod 16:37–47

    Article  CAS  PubMed  Google Scholar 

  37. de Mateo S, Sassone-Corsi P (2014) Regulation of spermatogenesis by small non-coding RNAs: role of the germ granule. Semin Cell Dev Biol 29:84–92

    Article  PubMed  PubMed Central  Google Scholar 

  38. van der Heijden GW, Derijck AA, Ramos L, Giele M, van der Vlag J, de Boer P (2006) Transmission of modified nucleosomes from the mouse male germline to the zygote and subsequent remodeling of paternal chromatin. Dev Biol 298:458–469

    Article  PubMed  Google Scholar 

  39. Lane N, Dean W, Erhardt S, Hajkova P, Surani A, Walter J et al (2003) Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis 35:88–93

    Article  CAS  PubMed  Google Scholar 

  40. Barlow DP, Bartolomei MS (2014) Genomic imprinting in mammals. Cold Spring Harb Perspect Biol 6(2):–pii:a018382. https://doi.org/10.1101/cshperspect.a018382

  41. Gill ME, Erkek S, Peters AH (2012) Parental epigenetic control of embryogenesis: a balance between inheritance and reprogramming? Curr Opin Cell Biol 24:387–396

    Article  CAS  PubMed  Google Scholar 

  42. Carrell DT (2012) Epigenetics of the male gamete. Fertil Steril 97:267–274

    Article  CAS  PubMed  Google Scholar 

  43. Stuppia L, Franzago M, Ballerini P, Gatta V, Antonucci I (2015) Epigenetics and male reproduction: the consequences of paternal lifestyle on fertility, embryo development, and children lifetime health. Clin Epigenetics 7:120. https://doi.org/10.1186/s13148-015-0155-4

    Article  PubMed  PubMed Central  Google Scholar 

  44. Ong TP, Ozanne SE (2015) Developmental programming of type 2 diabetes: early nutrition and epigenetic mechanisms. Curr Opin Clin Nutr Metab Care 18:354–360

    Article  CAS  PubMed  Google Scholar 

  45. Ly L, Chan D, Trasler JM (2015) Developmental windows of susceptibility for epigenetic inheritance through the male germline. Semin Cell Dev Biol 43:96–105

    Article  CAS  PubMed  Google Scholar 

  46. Kaati G, Bygren LO, Edvinsson S (2002) Cardiovascular and diabetes mortality determined by nutrition during parents’ and grandparents’ slow growth period. Eur J Hum Genet 10:682–688

    Article  CAS  PubMed  Google Scholar 

  47. Pembrey ME, Bygren LO, Kaati G, Edvinsson S, Northstone K, Sjöström M et al (2006) Sex-specific, male-line transgenerational responses in humans. Eur J Hum Genet 14:159–166

    Article  PubMed  Google Scholar 

  48. Pembrey M, Saffery R, Bygren LO (2014) Human transgenerational responses to early-life experience: potential impact on development, health and biomedical research. J Med Genet 51:563–572

    Article  PubMed  PubMed Central  Google Scholar 

  49. Linn T, Loewk E, Schneider K, Federlin K (1993) Spontaneous glucose intolerance in the progeny of low dose streptozotocin-induced diabetic mice. Diabetologia 36:1245–1251

    Article  CAS  PubMed  Google Scholar 

  50. Anderson LM, Riffle L, Wilson R (2006) Preconceptional fasting of fathers alters serum glucose in offspring of mice. Nutrition 22:327–331

    Article  CAS  PubMed  Google Scholar 

  51. Ng SF, Lin RC, Laybutt DR, Barres R, Owens JA, Morris MJ (2010) Chronic high-fat diet in fathers programs β-cell dysfunction in female rat offspring. Nature 467:963–966

    Article  CAS  PubMed  Google Scholar 

  52. Carone BR, Fauquier L, Habib N, Shea JM, Hart CE, Li R et al (2010) Paternally-induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 143:1084–1096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Mitchell M, Bakos HW, Lane M (2011) Paternal diet-induced obesity impairs embryo development and implantation in the mouse. Fertil Steril 95:1349–1353

    Article  PubMed  Google Scholar 

  54. Dunn GA, Bale TL (2011) Maternal high-fat diet effects on third-generation female body size via the paternal lineage. Endocrinology 152:2228–2236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Harrison M, Langley-Evans SC (2009) Intergenerational programming of impaired nephrogenesis and hypertension in rats following maternal protein restriction during pregnancy. Br J Nutr 101:1020–1030

    Article  CAS  PubMed  Google Scholar 

  56. Ly L, Chan D, Aarabi M, Landry M, Behan NA, AJ MF et al (2017) Intergenerational impact of paternal lifetime exposures to both folic acid deficiency and supplementation on reproductive outcomes and imprinted gene methylation. Mol Hum Reprod. https://doi.org/10.1093/molehr/gax029

  57. Wei Y, Yang CR, Wei YP, Zhao ZA, Hou Y, Schatten H et al (2014) Paternally induced transgenerational inheritance of susceptibility to diabetes in mammals. Proc Natl Acad Sci U S A 111:1873–1878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Radford EJ, Ito M, Shi H, Corish JA, Yamazawa K, Isganaitis E et al (2014) In utero undernourishment perturbs the adult sperm methylome and intergenerational metabolism. Science 345:1255903. https://doi.org/10.1126/science.1255903

    Article  PubMed  PubMed Central  Google Scholar 

  59. Martínez D, Pentinat T, Ribó S, Daviaud C, Bloks VW, Cebrià J et al (2014) In utero undernutrition in male mice programs liver lipid metabolism in the second-generation offspring involving altered LXRa DNA methylation. Cell Metab 19:941–951

    Article  PubMed  Google Scholar 

  60. Soubry A, Schildkraut JM, Murtha A, Wang F, Huang Z, Bernal A et al (2013) Paternal obesity is associated with IGF2 hypomethylation in newborns: results from a Newborn Epigenetics Study (NEST) cohort. BMC Med 11:29. https://doi.org/10.1186/1741-7015-11-29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Soubry A, Murphy SK, Wang F, Huang Z, Vidal AC, Fuemmeler BF et al (2015) Newborns of obese parents have altered DNA methylation patterns at imprinted genes. Int J Obes 39:650–657

    Article  CAS  Google Scholar 

  62. Sermondade N, Faure C, Fezeu L, Shayeb AG, Bonde JP, Jensen TK et al (2013) BMI in relation to sperm count: an updated systematic review and collaborative meta-analysis. Hum Reprod Update 19:221–231

    Article  CAS  PubMed  Google Scholar 

  63. Fariello RM, Pariz JR, Spaine DM, Cedenho AP, Bertolla RP, Fraietta R (2012) Association between obesity and alteration of sperm DNA integrity and mitochondrial activity. BJU Int 110:863–867

    Article  CAS  PubMed  Google Scholar 

  64. Soubry A, Guo L, Huang Z, Hoyo C, Romanus S, Price T et al (2016) Obesity-related DNA methylation at imprinted genes in human sperm: results from the TIEGER study. Clin Epigenetics 8:51. https://doi.org/10.1186/s13148-016-0217-2

    Article  PubMed  PubMed Central  Google Scholar 

  65. Donkin I, Versteyhe S, Ingerslev LR, Qian K, Mechta M, Nordkap L et al (2016) Obesity and bariatric surgery drive epigenetic variation of spermatozoa in humans. Cell Metab 23:369–378

    Article  CAS  PubMed  Google Scholar 

  66. Aarabi M, San Gabriel MC, Chan D, Behan NA, Caron M, Pastinen T et al (2015) High-dose folic acid supplementation alters the human sperm methylome and is influenced by the MTHFR C677T polymorphism. Hum Mol Genet 24:6301–6313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Chan D, McGraw S, Klein K, Wallock LM, Konermann C, Plass C et al (2017) Stability of the human sperm DNA methylome to folic acid fortification and short-term supplementation. Hum Reprod 32:272–283

    Article  CAS  PubMed  Google Scholar 

  68. Ong TP, Moreno FS, Ross SA (2011) Targeting the epigenome with bioactive food components for cancer prevention. J Nutrigenet Nutrigenomics 4:275–292

    Article  CAS  PubMed  Google Scholar 

  69. Ostermeier GC, Miller D, Huntriss JD, Diamond MP, Krawetz SA (2004) Reproductive biology: delivering spermatozoan RNA to the oocyte. Nature 429:154. https://doi.org/10.1038/429154a

    Article  CAS  PubMed  Google Scholar 

  70. Gapp K, Jawaid A, Sarkies P, Bohacek J, Pelczar P, Prados J et al (2014) Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice. Nat Neurosci 17:667–669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Rassoulzadegan M, Cuzin F (2015) Epigenetic heredity: RNA-mediated modes of phenotypic variation. Ann N Y Acad Sci 1341:172–175

    Article  CAS  PubMed  Google Scholar 

  72. McPherson NO, Fullston T, Aitken RJ, Lane M (2014) Paternal obesity, interventions, and mechanistic pathways to impaired health in offspring. Ann Nutr Metab 64:231–238

    Google Scholar 

  73. Fullston T, Ohlsson Teague EM, Palmer NO, DeBlasio MJ, Mitchell M, Corbett M et al (2013) Paternal obesity initiates metabolic disturbances in two generations of mice with incomplete penetrance to the F2 generation and alters the transcriptional profile of testis and sperm microRNA content. FASEB J 27:4226–4243

    Article  CAS  PubMed  Google Scholar 

  74. Sharma U, Conine CC, Shea JM, Boskovic A, Derr AG, Bing XY et al (2016) Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals. Science 351:391–396

    Article  CAS  PubMed  Google Scholar 

  75. Chen Q, Yan M, Cao Z, Li X, Zhang Y, Shi J et al (2016) Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder. Science 351:397–400

    Article  CAS  PubMed  Google Scholar 

  76. McPherson NO, Owens JA, Fullston T, Lane M (2015) Preconception diet or exercise intervention in obese fathers normalizes sperm microRNA profile and metabolic syndrome in female offspring. Am J Phys 308:E805–E821

    Google Scholar 

  77. Choi JY, Lee KM, Park SK, Noh DY, Ahn SH, Yoo KY et al (2005) Association of paternal age at birth and the risk of breast cancer in offspring: a case control study. BMC Cancer 5:143. https://doi.org/10.1186/1471-2407-5-143

    Article  PubMed  PubMed Central  Google Scholar 

  78. Titus-Ernstoff L, Egan KM, Newcomb PA, Ding J, Trentham-Dietz A, Greenberg ER et al (2002) Early life factors in relation to breast cancer risk in postmenopausal women. Cancer Epidemiol Biomark Prev 11:207–210

    Google Scholar 

  79. Fontelles CC, Carney E, Clarke J, Nguyen NM, Yin C, Jin L et al (2016) Paternal overweight is associated with increased breast cancer risk in daughters in a mouse model. Sci Rep 6:28602. https://doi.org/10.1038/srep28602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Fontelles CC, Guido LN, Rosim MP, Andrade Fde O, Jin L, Inchauspe J et al (2016) Paternal programming of breast cancer risk in daughters in a rat model: opposing effects of animal- and plant-based high-fat diets. Breast Cancer Res 18:71. https://doi.org/10.1186/s13058-016-0729-x

    Article  PubMed  PubMed Central  Google Scholar 

  81. Guido LN, Fontelles CC, Rosim MP, Pires VC, Cozzolino SM, Castro IA et al (2016) Paternal selenium deficiency but not supplementation during preconception alters mammary gland development and 7,12-dimethylbenz[a]anthracene-induced mammary carcinogenesis in female rat offspring. Int J Cancer:139, 1873–1882

    Google Scholar 

  82. McPherson NO, Fullston T, Kang WX, Sandeman LY, Corbett MA, Owens JA et al (2016) Paternal under-nutrition programs metabolic syndrome in offspring which can be reversed by antioxidant/vitamin food fortification in fathers. Sci Rep 6:27010. https://doi.org/10.1038/srep27010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Masuyama H, Mitsui T, Eguchi T, Tamada S, Hiramatsu Y (2016) The effects of paternal high-fat diet exposure on offspring metabolism with epigenetic changes in the mouse adiponectin and leptin gene promoters. Am J Physiol Endocrinol Metab 311:E236–E245

    Article  PubMed  Google Scholar 

  84. Troisi R, Stephansson O, Jacobsen J, Tretli S, Sørensen HT, Gissler M et al (2014) Perinatal characteristics and bone cancer risk in offspring – a Scandinavian population-based study. Acta Oncol 53:830–838

    Article  PubMed  Google Scholar 

  85. Lagiou P, Samoli E, Okulicz W, Xu B, Lagiou A, Lipworth L et al (2011) Maternal and cord blood hormone levels in the United States and China and the intrauterine origin of breast cancer. Ann Oncol 22:1102–1108

    Article  CAS  PubMed  Google Scholar 

  86. Qiu L, Low HP, Chang CI, Strohsnitter WC, Anderson M, Edmiston K et al (2012) Novel measurements of mammary stem cells in human umbilical cord blood as prospective predictors of breast cancer susceptibility in later life. Ann Oncol 23:245–250

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

C. C. F. was a recipient of a PhD scholarship from the Brazilian National Council for Scientific and Technological Development (CNPq; Proc. 153478/2012-8). T. P. O. is the recipient of a researcher fellowship from CNPq (Proc.307910/2016-4) and is supported by grants from CNPq (Proc. 448501/2014-7), the Food Research Center (FoRC), and the São Paulo State Research Funding Agency (Proc.2013/07914-8).

Author information

Authors and Affiliations

  1. Department of Food and Experimental Nutrition, Food Research Center (FoRC), Faculty of Pharmaceutical Sciences, University of São Paulo, São Paulo, Brazil

    Camile Castilho Fontelles & Thomas Prates Ong

  2. Georgetown University Lombardi Comprehensive Cancer Center, Washington, DC, USA

    Camile Castilho Fontelles, Raquel Santana da Cruz, Leena Hilakivi-Clarke & Sonia de Assis

Authors
  1. Camile Castilho Fontelles
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Raquel Santana da Cruz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Leena Hilakivi-Clarke
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sonia de Assis
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Thomas Prates Ong
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Thomas Prates Ong .

Editor information

Editors and Affiliations

  1. Debden, Essex, United Kingdom

    Paul C. Guest

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Science+Business Media, LLC

About this protocol

Check for updates. Verify currency and authenticity via CrossMark

Cite this protocol

Fontelles, C.C., da Cruz, R.S., Hilakivi-Clarke, L., de Assis, S., Ong, T.P. (2018). Developmental Origins of Breast Cancer: A Paternal Perspective. In: Guest, P. (eds) Investigations of Early Nutrition Effects on Long-Term Health. Methods in Molecular Biology, vol 1735. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-7614-0_5

Download citation

  • DOI: https://doi.org/10.1007/978-1-4939-7614-0_5

  • Published:

  • Publisher Name: Humana Press, New York, NY

  • Print ISBN: 978-1-4939-7613-3

  • Online ISBN: 978-1-4939-7614-0

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics

Search

Navigation