Neighborhood and Family Environment of Expectant Mothers May Influence Prenatal Programming of Adult Cancer Risk: Discussion and an Illustrative DNA Methylation Example

Biodemography and Social Biology

Volumn 62, Issue 1, 2016, Pages 87-104

  King, Katherine E ^a   Kane, Jennifer B ^b   Scarbrough, Peter ^c   Hoyo, Cathrine ^d   Murphy, Susan K ^c,e  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA AT CHAPEL HILL   (United States)

^c DUKE CANCER INSTITUTE   (United States)

^d NORTH CAROLINA STATE UNIVERSITY   (United States)

^e DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LONG UNTRANSLATED RNA; MEG3 NON-CODING RNA, HUMAN;

ADULT; DEMOGRAPHY; DNA METHYLATION; FAMILY SIZE; FEMALE; GENETICS; HUMAN; MARRIAGE; MENTAL STRESS; NORTH CAROLINA; PHYSIOLOGY; PREGNANCY; PREGNANT WOMAN; SOCIAL ENVIRONMENT; STATISTICS AND NUMERICAL DATA; YOUNG ADULT;

ADULT; DNA METHYLATION; FAMILY CHARACTERISTICS; FEMALE; HUMANS; MARITAL STATUS; NORTH CAROLINA; PREGNANCY; PREGNANT WOMEN; RESIDENCE CHARACTERISTICS; RNA, LONG NONCODING; SOCIAL ENVIRONMENT; STRESS, PSYCHOLOGICAL; YOUNG ADULT;

EID: 84963795261     PISSN: 19485565     EISSN: 19485573     Source Type: Journal    
DOI: 10.1080/19485565.2015.1126501     Document Type: Review

References (116)

1. Albrecht, S. L., and M. K. Miller. 1996. Hispanic subgroup differences in prenatal care. Social Biology 43:38-58.
2. Anwar, S. L., T. Krech, B. Hasemeier, E. Schipper, N. Schweitzer, A. Vogel, and U. Lehmann. 2012. Loss of imprinting and allelic switching at the DLK1-MEG3 locus in human hepatocellular carcinoma. PLoS One 7 (11):e49462. doi:10.1371/journal.pone.0049462.
3. Averett, S., H. Corman, and N. E. Reichman. 2013. Effects of overweight on risky sexual behavior of adolescent girls. Economic Inquiry 51 (1):605-19. doi:10.1111/ecin.2013.51.issue-1.
4. Barker, D. J. 1995. Fetal origins of coronary heart disease. British Medical Journal 311 (6998):171-74. doi:10.1136/bmj.311.6998.171.
5. Barker, D. J. 2004. The developmental origins of adult disease. Journal of the American College of Nutrition 23 (sup6):588S-595S. doi:10.1080/07315724.2004.10719428.
6. Benetatos, L., A. Dasoula, E. Hatzimichael, I. Georgiou, M. Syrrou, and K. L. Bourantas. 2008. Promoter hypermethylation of the MEG3 (DLK1/MEG3) imprinted gene in multiple myeloma. Clinical Lymphoma and Myeloma 8 (3):171-75. doi:10.3816/CLM.2008.n.021.
7. Benetatos, L., G. Vartholomatos, and E. Hatzimichael. 2011. MEG3 imprinted gene contribution in tumorigenesis. International Journal of Cancer 129 (4):773-79. doi:10.1002/ijc.26052.
8. Borugian, M. J., J. J. Spinelli, Z. Abanto, C. L. Xu, and R. Wilkins. 2011. Breast cancer incidence and neighbourhood income. Health Reports 22 (2):7-13.
9. Boynton-Jarrett, R., J. W. Rich-Edwards, H.-J. Jun, E. N. Hibert, and R. J. Wright. 2011. Abuse in childhood and risk of uterine leiomyoma: The role of emotional support in biologic resilience. Epidemiology 22 (1):6-14. doi:10.1097/EDE.0b013e3181ffb172.
10. Braconi, C., T. Kogure, N. Valeri, N. Huang, G. Nuovo, S. Costinean, and T. Patel. 2011. Microrna-29 can regulate expression of the long non-coding RNA gene MEG3 in hepatocellular cancer. Oncogene 30 (47):4750-56. doi:10.1038/onc.2011.193.
11. Breton, C., H. Byun, M. Wenten, F. Pan, A. Yang, and F. Gilliland. 2009. Prenatal tobacco smoke exposure affects global and gene-specific DNA methylation. American Journal of Respiratory and Critical Care Medicine 180 (5):642-47.
12. Brown, D. W., R. F. Anda, V. J. Felitti, V. J. Edwards, A. M. Malarcher, J. B. Croft, and W. H. Giles. 2010. Adverse childhood experiences are associated with the risk of lung cancer: A prospective cohort study. BMC Public Health 10:20. doi:10.1186/1471-2458-10-20.
13. Buckles, K., and J. Price. 2013. Selection and the marriage premium for infant health. Demography 50 (4):1315-39. doi:10.1007/s13524-013-0211-7.
14. Buka, S., R. Brennan, J. Rich-Edwards, S. W. Raudenbush, and F. Earls. 2003. Neighborhood support and the birth weight of urban infants. American Journal of Epidemiology 157:1-8. doi:10.1093/aje/kwf170.
15. Champagne, F. A., and J. P. Curley. 2011. Epigenetic influence of the social environment. In Brain, behavior and epigenetics, ed. A. Petronis, and J. Mill, 185-208. Berlin and Heidelberg: Springer-Verlag.
16. Clark, L., H. Beesley, C. Holcombe, and P. Salmon. 2011. The influence of childhood abuse and adult attachment style on clinical relationships in breast cancer care. General Hospital Psychiatry 33 (6):579-86. doi:10.1016/j.genhosppsych.2011.07.007.
17. Clarke, P., J. Morenoff, M. Debbink, E. Golberstein, M. R. Elliott, and P. M. Lantz. 2013. Cumulative exposure to neighborhood context: Consequences for health transitions over the adult life course. Research on Aging 36 (1):115-42. doi:10.1177/0164027512470702.
18. Colditz, G. A., and E. K. Wei. 2012. Preventability of cancer: The relative contributions of biologic and social and physical environmental determinants of cancer mortality. Annual Review of Public Health 33:137-56. doi:10.1146/annurev-publhealth-031811-124627.
19. Cole, S. W., J. M. Arevalo, R. Takahashi, E. K. Sloan, S. K. Lutgendorf, A. K. Sood, J. F. Sheridan, and T. E. Seeman. 2010. Computational identification of gene-social environment interaction at the human IL6 locus. Proceedings of the National Academy of Sciences 107 (12):5681-86. doi:10.1073/pnas.0911515107.
20. Copper, R., R. Goldenberg, A. Das., N. Elder, M. Swain, G. Norman, R. Ramsey, et al. 1996. The preterm prediction study: Maternal stress is associated with spontaneous preterm birth at less than thirty-five weeks gestation. American Journal of Obstetrics and Gynecology 175:1286-92. doi:10.1016/S0002-9378(96)70042-X.
21. Culhane, J. F., and I. T. Elo. 2005. Neighborhood context and reproductive health. American Journal of Obstetrics and Gynecology 192 (5):S22-S29. doi:10.1016/j.ajog.2005.01.071.
22. Cunningham, S. A., I. T. Elo, K. Herbst, and V. Hosegood. 2010. Prenatal development in rural South Africa: Relationship between birth weight and access to fathers and grandparents. Population Studies 64 (3):229-46. doi:10.1080/00324728.2010.510201.
23. Dawson, M. A., and T. Kouzarides. 2012. Cancer epigenetics: From mechanism to therapy. Cell 150 (1):12-27. doi:10.1016/j.cell.2012.06.013.
24. Farley, T., K. Mason, J. Rice, J. Habel, R. Scribner, and D. Cohen. 2006. The relationship between the neighbourhood environment and adverse birth outcomes. Paediatric and Perinatal Epidemiology 20:188-200. doi:10.1111/ppe.2006.20.issue-3.
25. Fraser, H., L. Lam, S. Neumann, and M. Kobor. 2012. Population-specificity of human DNA methylation. Genome Biology 13 (2):R8. doi:10.1186/gb-2012-13-2-r8.
26. Fuller-Thomson, E., and S. Brennenstuhl. 2009. Making a link between childhood physical abuse and cancer. Cancer 115 (14):3341-50. doi:10.1002/cncr.24372.
27. Galea, S., M. Uddin, and K. Koenen. 2011. The urban environment and mental disorders: Epigenetic links. Epigenetics 6 (4):400-04. doi:10.4161/epi.6.4.14944.
28. Ghosh, J. K. C., J. E. Heck, M. Cockburn, J. Su, M. Jerrett, and B. Ritz. 2013. Prenatal exposure to traffic-related air pollution and risk of early childhood cancers. American Journal of Epidemiology 178 (8):1233-39. doi:10.1093/aje/kwt129.
29. Goldenberg, R. L., J. Culhane, J. Iams, and R. Romero. 2008. Epidemiology and causes of preterm birth. Lancet 371 (9606):75-84. doi:10.1016/S0140-6736(08)60074-4.
30. Goldsmith, R. E., L. Jandorf, H. Valdimarsdottir, K. L. Amend, B. G. Stoudt, C. Rini, and D. H. Bovbjerg. 2010. Traumatic stress symptoms and breast cancer: The role of childhood abuse. Child Abuse & Neglect 34 (6):465-70. doi:10.1016/j.chiabu.2009.10.007.
31. Gritz, E. C., and V. Bhandari. 2015. The human neonatal gut microbiome: A brief review. Frontiers in Pediatrics 3:17. doi:10.3389/fped.2015.00017.
32. Gudsnuk, K., and F. A. Champagne. 2012. Epigenetic influence of stress and the social environment. ILAR Journal 53 (3-4):279-88. doi:10.1093/ilar.53.3-4.279.
33. Haggarty, P., G. Hoad, D. Campbell, G. Horgan, C. Piyathilake, and G. McNeill. 2013. Folate in pregnancy and imprinted gene and repeat element methylation in the offspring. American Journal of Clinical Nutrition 97 (1):94-99. doi:10.3945/ajcn.112.042572.
34. Heijmans, B. T., E. W. Tobi, A. D. Stein, H. Putter, G. J. Blauw, E. S. Susser, and L. H. Lumey. 2008. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proceedings of the National Academy of Sciences 105 (44):17046-49. doi:10.1073/pnas.0806560105.
35. Hiatt, R. A., and N. Breen. 2008. The social determinants of cancer: A challenge for transdisciplinary science. American Journal of Preventive Medicine 35 (2):S141-S150. doi:10.1016/j.amepre.2008.05.006.
36. Hoffmann, A., and D. Spengler. 2012. The lasting legacy of social stress on the epigenome of the hypothalamic-pituitary-adrenal axis. Epigenomics 4 (4):431-44. doi:10.2217/epi.12.34.
37. Hoyo, C., A. P. Murtha, J. M. Schildkraut, M. R. Forman, B. Calingaert, W. Demark-Wahnefried, and S. K. Murphy. 2011. Folic acid supplementation before and during pregnancy in the Newborn Epigenetics STudy (NEST). BMC Public Health 11:46. doi:10.1186/1471-2458-11-46.
38. Hoyo, C., A. P. Murtha, J. M. Schildkraut, R. L. Jirtle,W. Demark-Wahnefried, M. R. Forman, and S. K. Murphy. 2011. Methylation variation at IGF2 differentially methylated regions and maternal folic acid use before and during pregnancy. Epigenetics 6 (7):928-36. doi:10.4161/epi.6.7.16263.
39. Isles, A. R., W. Davies, and L. S. Wilkinson. 2006. Genomic imprinting and the social brain. Philosophical Transactions of the Royal Society B: Biological Sciences 361 (1476):2229-37. doi:10.1098/rstb.2006.1942.
40. Janssen, B., L. Godderis, N. Pieters, K. Poels, M. Kicinski, A. Cuypers, and T. Nawrot. 2013. Placental DNA hypomethylation in association with particulate air pollution in early life. Particle and Fibre Toxicology 10 (1):22. doi:10.1186/1743-8977-10-22.
41. Joubert, B. R., S. E. Haberg, R. M. Nilsen, X. Wang, S. E. Vollset, S. K. Murphy, and S. J. London. 2012. 450K epigenome-wide scan identifies differential DNA methylation in newborns related to maternal smoking during pregnancy. Environmental Health Perspectives 120 (10):1425-31. doi:10.1289/ehp.1205412.
42. Kaati, G., L. O. Bygren, M. Pembrey, and M. Sjostrom. 2007. Transgenerational response to nutrition, early life circumstances and longevity. European Journal of Human Genetics 15 (7):784-90. doi:10.1038/sj.ejhg.5201832.
43. Kalantaridou, S. N., A. Makrigiannakis, E. Zoumakis, and G. P. Chrousos. 2004. Stress and the female reproductive system. Journal of Reproductive Immunology 62 (1-2):61-68. doi:10.1016/j.jri.2003.09.004.
44. Kane, J. B. (2012). The "marriage advantage" in infant health outcomes: Evidence of selection or risky behavior? Paper presented at the Population Association of America, San Francisco, CA.
45. Kane, J. B., and M. L. Frisco. 2013. Obesity, school obesity prevalence, and adolescent childbearing among US young women. Social Science & Medicine 88:108-15. doi:10.1016/j.socscimed.2013.04.005.
46. Kapoor, A., E. Dunn, A. Kostaki, M. H. Andrews, and S. G. Matthews. 2006. Fetal programming of hypothalamo-pituitary-adrenal function: Prenatal stress and glucocorticoids. Journal of Physiology 572 (1):31-44. doi:10.1113/jphysiol.2006.105254.
47. Kawakami, T., T. Chano, K. Minami, H. Okabe, Y. Okada, and K. Okamoto. 2006. Imprinted DLK1 is a putative tumor suppressor gene and inactivated by epimutation at the region upstream of GTL2 in human renal cell carcinoma. Human Molecular Genetics 15 (6):821-30. doi:10.1093/hmg/ddl001.
48. Kelly-Irving, M., B. Lepage, D. Dedieu, R. Lacey, N. Cable, M. Bartley, and C. Delpierre. 2013. Childhood adversity as a risk for cancer: Findings from the 1958 British Birth Cohort Study. BMC Public Health 13 (1):767. doi:10.1186/1471-2458-13-767.
49. Kile, M. L., A. Baccarelli, L. Tarantini, E. Hoffman, R. O. Wright, and D. C. Christiani. 2010. Correlation of global and gene-specific DNA methylation in maternal-infant pairs. PLoS One 5 (10):e13730. doi:10.1371/journal.pone.0013730.
50. Kimbro, R. T. 2008. Together forever? Romantic relationship characteristics and prenatal health behaviors. Journal of Marriage and Family 70 (3):745-57. doi:10.1111/jomf.2008.70.issue-3.
51. King, K., J. Morenoff, and J. House. 2011. Neighborhood socioeconomic characteristics and social disparities in cumulative biological risk factors. Psychosomatic Medicine 73 (7):572-79. doi:10.1097/PSY.0b013e318227b062.
52. King, K., S. Murphy, and C. Hoyo. 2015. Epigenetic regulation of newborns' imprinted genes related to gestational growth: Patterning by parental race/ethnicity and maternal socioeconomic status. Journal of Epidemiology & Community Health 69:639-47. doi:10.1136/jech-2014-204781.
53. Landale, N. S., and R. Oropresa. 2001. Migration, social support and perinatal health: An origindestination analysis of Puerto Rican women. Journal of Health and Social Behavior 42 (2):166-183.
54. Liu, Y., S. K. Murphy, A. P. Murtha, B. F. Fuemmeler, J. Schildkraut, Z. Huang, and C. Hoyo. 2012. Depression in pregnancy, infant birth weight and DNA methylation of imprint regulatory elements. Epigenetics 7 (7):735-46. doi:10.4161/epi.20734.
55. Lobel, M., C. Dunkerl-Schetter, and S. Scrimshaw. 1992. Prenatal maternal stress and prematurity: A prospective study of socioeconomically disadvantaged women. Health Psychology 11:32-40. doi:10.1037/0278-6133.11.1.32.
56. Lutgendorf, S. K., K. DeGeest, L. Dahmoush, D. Farley, F. Penedo, D. Bender, and S.W. Cole. 2011. Social isolation is associated with elevated tumor norepinephrine in ovarian carcinoma patients. Brain Behavior and Immunity 25 (2):250-55. doi:10.1016/j.bbi.2010.10.012.
57. Maccari, S., and S. Morley-Fletcher. 2007. Effects of prenatal restraint stress on the hypothalamus-pituitary-adrenal axis and related behavioural and neurobiological alterations. Psychoneuroendocrinology 32:S10-S15. doi:10.1016/j.psyneuen.2007.06.005.
58. Markunas, C. A., Z. Xu, S. Harlid, P. A. Wade, R. T. Lie, J. A. Taylor, and A. J. Wilcox. 2014. Identification of DNA methylation changes in newborns related to maternal smoking during pregnancy. Environmental Health Perspectives 122 (10):1147-53.
59. Maynard, M., D. Gunnell, P. Emmett, S. Frankel, and G. Davey Smith. 2003. Fruit, vegetables, and antioxidants in childhood and risk of adult cancer: The Boyd Orr cohort. Journal of Epidemiology & Community Health 57 (3):218-25. doi:10.1136/jech.57.3.218.
60. McEwen, B. S., L. Eiland, R. Hunter, and M. Miller. 2012. Stress and anxiety: Structural plasticity and epigenetic regulation as a consequence of stress. Neuropharmacology 62 (1):3-12. doi:10.1016/j.neuropharm.2011.07.014.
61. McGowan, P. O., A. Sasaki, A. C. D'Alessio, S. Dymov, B. Labonte, M. Szyf, and M. J. Meaney. 2009. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nature Neuroscience 12 (3):342-48. doi:10.1038/nn.2270.
62. McGowan, P. O., and M. Szyf. 2010. Environmental epigenomics: Understanding the effects of parental care on the epigenome. Essays in Biochemistry 48 (1):275-87. doi:10.1042/bse0480275.
63. McRae, A. F., J. E. Powell, A. K. Henders, L. Bowdler, G. Hemani, S. Shah, and G.W. Montgomery. 2014. Contribution of genetic variation to transgenerational inheritance of DNA methylation. Genome Biology 15 (5):R73. doi:10.1186/gb-2014-15-5-r73.
64. Mehta, D., T. Klengel, K. N. Conneely, A. K. Smith, A. Altmann, T. W. Pace, and E. B. Binder. 2013. Childhood maltreatment is associated with distinct genomic and epigenetic profiles in posttraumatic stress disorder. Proceedings of the National Academy of Sciences 110 (20):8302-07. doi:10.1073/pnas.1217750110.
65. Meijer, M., K. Bloomfield, and G. Engholm. 2013. Neighbourhoods matter too: The association between neighbourhood socioeconomic position, population density and breast, prostate and lung cancer incidence in Denmark between 2004 and 2008. Journal of Epidemiology & Community Health 67 (1):6-13. doi:10.1136/jech-2011-200192.
66. Messer, L. C., J. S. Kaufman, N. Dole, D. A. Savitz, and B. A. Laraia. 2006. Neighborhood crime, deprivation, and preterm birth. Annals of Epidemiology 16 (6):455-62. doi:10.1016/j.annepidem.2005.08.006.
67. Metwally, M., T. C. Li, and W. L. Ledger. 2007. The impact of obesity on female reproductive function. Obesity Reviews 8 (6):515-23. doi:10.1111/obr.2007.8.issue-6.
68. Miller, G. E., and E. Chen. 2010. Harsh family climate in early life presages the emergence of a proinflammatory phenotype in adolescence. Psychological Science 21 (6):848-56. doi:10.1177/0956797610370161.
69. Miller, G., E. Chen, and S. W. Cole. 2009. Health psychology: Developing biologically plausible models linking the social world and physical health. Annual Review of Psychology 60:501-24. doi:10.1146/annurev.psych.60.110707.163551.
70. Miller, G. E., E. Chen, and K. J. Parker. 2011. Psychological stress in childhood and susceptibility to the chronic diseases of aging: Moving toward a model of behavioral and biological mechanisms. Psychological Bulletin 137 (6):959-97. doi:10.1037/a0024768.
71. Montgomery, S. M., A. G. Ehlin, P. Sparen, B. Bjorksten, and A. Ekbom. 2002. Childhood indicators of susceptibility to subsequent cervical cancer. British Journal of Cancer 87 (9):989-93. doi:10.1038/sj.bjc.6600585.
72. Moreno-Smith, M., S. K. Lutgendorf, and A. K. Sood. 2010. Impact of stress on cancer metastasis. Future Oncology 6 (12):1863-81. doi:10.2217/fon.10.142.
73. Morton, P. M., M. H. Schafer, and K. F. Ferraro. 2012. Does childhood misfortune increase cancer risk in adulthood? Journal of Aging and Health 24 (6):948-84. doi:10.1177/0898264312449184.
74. Mueller, B. R., and T. L. Bale. 2008. Sex-specific programming of offspring emotionality after stress early in pregnancy. Journal of Neuroscience 28 (36):9055-65. doi:10.1523/jneurosci.1424-08.2008.
75. Murphy, S. K., A. Adigun, Z. Huang, F. Overcash, F. Wang, R. L. Jirtle, and C. Hoyo. 2012. Genderspecific methylation differences in relation to prenatal exposure to cigarette smoke. Gene 494 (1):36-43. doi:10.1016/j.gene.2011.11.062.
76. Murphy, S. K., Z. Huang, and C. Hoyo. 2012. Differentially methylated regions of imprinted genes in prenatal, perinatal and postnatal human tissues. PLoS One 7 (7):e40924. doi:10.1371/journal.pone.0040924.
77. Nesset, K. A., A. M. Perri, and C. R. Mueller. 2014. Frequent promoter hypermethylation and expression reduction of the glucocorticoid receptor gene in breast tumors. Epigenetics 9 (6):851-59. doi:10.4161/epi.28484.
78. Olden, K., H. A. Olden, and Y.-S. Lin, Eds. 2015. The role of the epigenome in translating neighborhood disadvantage into health disparities. Current Environmental Health Reports 2 (2):163-170.
79. Radtke, K. M., M. Ruf, H. M. Gunter, K. Dohrmann, M. Schauer, A. Meyer, and T. Elbert. 2011. Transgenerational impact of intimate partner violence on methylation in the promoter of the glucocorticoid receptor. Translational Psychiatry 1:e21. doi:10.1038/tp.2011.21.
80. Redshaw, M., and J. Henderson. 2013. Fathers' engagement in pregnancy and childbirth: Evidence from a national survey. BMC Pregnancy and Childbirth 13:70. doi:10.1186/1471-2393-13-70.
81. Reichman, N. E., J. O. Teitler, and E. R. Hamilton. 2009. Effects of neighborhood racial composition on birthweight. Health & Place 15 (3):814-21. doi:10.1016/j.healthplace.2009.01.001.
82. Reynolds, P., J. Von Behren, R. B. Gunier, D. E. Goldberg, A. Hertz, and D. Smith. 2002. Traffic patterns and childhood cancer incidence rates in California, United States. Cancer Causes Control 13 (7):665-73. doi:10.1023/A:1019579430978.
83. Richardson, S. S., C. R. Daniels, M. W. Gillman, J. Golden, R. Kukla, C. Kuzawa, and J. Rich-Edwards. 2014. Society: Don't blame the mothers. Nature 512 (7513):131-32. doi:10.1038/512131a.
84. Salim, S., G. Chugh, and M. Asghar. 2012. Inflammation in anxiety. Advances in Protein Chemistry and Structural Biology 88:1-25. doi:10.1016/b978-0-12-398314-5.00001-5.
85. Sampson, R. J., S.W. Raudenbush, and F. Earls. 1997. Neighborhoods and violent crime: A multilevel study of collective efficacy. Science 277:918-24. doi:10.1126/science.277.5328.918.
86. Sandler, D. P., R. B. Everson, A. J. Wilcox, and J. P. Browder. 1985. Cancer risk in adulthood from early life exposure to parents' smoking. American Journal of Public Health 75 (5):487-92. doi:10.2105/AJPH.75.5.487.
87. Sanna, L., A. L. Stuart, J. A. Pasco, F. N. Jacka, M. Berk, M. Maes, and L. J. Williams. 2013. Atopic disorders and depression: Findings from a large, population-based study. Journal of Affective Disorders. doi:10.1016/j.jad.2013.11.009.
88. Schempf, A. H., J. S. Kaufman, L. C. Messer, and P. Mendola. 2011. The neighborhood contribution to black-white perinatal disparities: An example from two North Carolina counties, 1999-2001. American Journal of Epidemiology 174 (6):744-52. doi:10.1093/aje/kwr128.
89. Schootman, M., M. Lian, A. D. Deshpande, E. A. Baker, S. L. Pruitt, R. Aft, and D. B. Jeffe. 2010. Temporal trends in area socioeconomic disparities in breast-cancer incidence and mortality, 1988-2005. Breast Cancer Research and Treatment 122 (2):533-43. doi:10.1007/s10549-009-0729-y.
90. Schuler, L. A., and A. P. Auger. 2010. Psychosocially influenced cancer: Diverse early-life stress experiences and links to breast cancer. Cancer Prevention Research 3 (11):1365-70. doi:10.1158/1940-6207.CAPR-10-0238.
91. Sear, R., and R. Mace. 2008. Who keeps children alive? A review of the effects of kin on child survival. Evolution and Human Behavior 29 (1):1-18. doi:10.1016/j.evolhumbehav.2007.10.001.
92. Sharkey, P. 2008. The intergenerational transmission of context. American Journal of Sociology 113:931-69. doi:10.1086/517893.
93. Sheng, X., J. Li, L. Yang, Z. Chen, Q. Zhao, L. Tan, and Y. Zhou. 2014. Promoter hypermethylation influences the suppressive role of maternally expressed 3, a long non-coding RNA, in the development of epithelial ovarian cancer. Oncology Reports 32 (1):277-85. doi:10.3892/or.2014.3208.
94. Smedby, K. E., H. Hjalgrim, E. T. Chang, K. Rostgaard, B. Glimelius, H.-O. Adami, and M. Melbye. 2007. Childhood social environment and risk of non-Hodgkin lymphoma in adults. Cancer Research 67 (22):11074-82. doi:10.1158/0008-5472.can-07-1751.
95. Snijders, T. A. B., and R. J. Bosker. 1999. Multilevel analysis: An introduction to basic and advanced multilevel modeling. London: Sage Publishers.
96. Sobrinho, L. G., J. S. Duarte, I. Paiva, L. Gomes, V. Vicente, and P. Aguiar. 2012. Paternal deprivation prior to adolescence and vulnerability to pituitary adenomas. Pituitary 15 (2):251-57. doi:10.1007/s11102-011-0324-1.
97. Soubry, A., S. Murphy, Z. Huang, A. Murtha, J. Schildkraut, R. Jirtle, C. Wang, et al. 2011. The effects of depression and use of antidepressive medicines during pregnancy on the methylation status of the IGF2 imprinted control regions in the offspring. Clinical Epigenetics 3 (1):2. doi:10.1186/1868-7083-3-2.
98. Soubry, A., S. K. Murphy, F. Wang, Z. Huang, A. C. Vidal, B. F. Fuemmeler, J. Kurtzberg, A. Murtha, R. L. Jirtle, J. M. Schildkraut, and C. Hoyo. 2013. Newborns of obese parents have altered DNA methylation patterns at imprinted genes. International Journal of Obesity (2005). doi:10.1038/ijo.2013.193.
99. Soubry, A., J. M. Schildkraut, A. Murtha, F. Wang, Z. Huang, A. Bernal, J. Kurtzberg, R. L. Jirtle, S. K. Murphy, and C. Hoyo. 2013. Paternal obesity is associated with IGF2 hypomethylation in newborns: Results from a Newborn Epigenetics STudy (NEST) cohort. BMC Medicine. doi:10.1186/1741-7015-11-29.
100. StataCorp. 2011. Stata statistical software: Release 12. College Station, TX: StataCorp LP.
101. Stieb, D. M., L. Chen, M. Eshoul, and S. Judek. 2012. Ambient air pollution, birth weight and preterm birth: A systematic review and meta-analysis. Environmental Research 117:100-11. doi:10.1016/j.envres.2012.05.007.
102. Szyf, M., I.Weaver, and M. Meaney. 2007. Maternal care, the epigenome and phenotypic differences in behavior. Reproductive Toxicology 24:9-19. doi:10.1016/j.reprotox.2007.05.001.
103. Tang, W.W.C., Dietmann S., Irie N., Leitch H.G., Floros V.I., Bradshaw C.R., Hackett J.A. Chinnery, and M. A. Surani. 2015. A unique gene regulatory network resets the human germline epigenome for development. Cell 161 (6):1453-1467.
104. Vidal, A. C., A. P. Murtha, S. K. Murphy, K. Fortner, F. Overcash, N. Henry, and C. Hoyo. 2013. Maternal BMI, IGF-I levels, and birth weight in African American and white infants. International Journal of Pediatrics 7. doi:10.1155/2013/191472. Available at http://www.hindawi.com/journals/ ijpedi/2013/191472/cta/
105. Volden, P. A., E. L. Wonder, M. N. Skor, C. M. Carmean, F. N. Patel, H. Ye, and S. D. Conzen. 2013. Chronic social isolation is associated with metabolic gene expression changes specific to mammary adipose tissue. Cancer Prevention Research 6 (7):634-45. doi:10.1158/1940-6207.capr-12-0458.
106. Weaver, I. C., F. A. Champagne, S. E. Brown, S. Dymov, S. Sharma, M. J. Meaney, and M. Szyf. 2005. Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: Altering epigenetic marking later in life. Journal of Neuroscience 25 (47):11045-54. doi:10.1523/jneurosci.3652-05.2005.
107. Weaver, I. C., M. J. Meaney, and M. Szyf. 2006. Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood. Proceedings of the National Academy of Sciences 103 (9):3480-85. doi:10.1073/pnas.0507526103.
108. Welberg, L. A. M., and J. R. Seckl. 2001. Prenatal stress, glucocorticoids and the programming of the brain. Journal of Neuroendocrinology 13 (2):113-28. doi:10.1111/j.1365-2826.2001.00601.x.
109. Williams, D. R., E. Z. Kontos, K. Viswanath, J. S. Haas, C. S. Lathan, L. E. MacConaill, and J. Z. Ayanian. 2012. Integrating multiple social statuses in health disparities research: The case of lung cancer. Health Services Research 47 (3pt2):1255-77. doi:10.1111/j.1475-6773.2012.01404.x.
110. Yang, B. Z., H. Zhang,W. Ge, N.Weder, H. Douglas-Palumberi, F. Perepletchikova, and J. Kaufman. 2013. Child abuse and epigenetic mechanisms of disease risk. American Journal of Preventive Medicine 44 (2):101-07. doi:10.1016/j.amepre.2012.10.012.
111. Ying, L., Y. Huang, H. Chen, Y.Wang, L. Xia, Y. Chen, and F. Qiu. 2013. Downregulated MEG3 activates autophagy and increases cell proliferation in bladder cancer. Molecular Biosystems 9 (3):407-11. doi:10.1039/c2mb25386k.
112. Zhang, X., R. Gejman, A. Mahta, Y. Zhong, K. A. Rice, Y. Zhou, and A. Klibanski. 2010. Maternally expressed gene 3, an imprinted noncoding RNA gene, is associated with meningioma pathogenesis and progression. Cancer Research 70 (6):2350-58. doi:10.1158/0008-5472.can-09-3885.
113. Zhao, J., X. Zhang, Y. Zhou, P. J. Ansell, and A. Klibanski. 2006. Cyclic AMP stimulates MEG3 gene expression in cells through a cAMP-response element (CRE) in the MEG3 proximal promoter region. International Journal of Biochemistry & Cell Biology 38 (10):1808-20. doi:10.1016/j.biocel.2006.05.004.
114. Zhou, Y., X. Zhang, and A. Klibanski. 2012. MEG3 noncoding RNA: A tumor suppressor. Journal of Molecular Endocrinology 48 (3):R45-53. doi:10.1530/JME-12-0008.
115. Zhou, Y., Y. Zhong, Y.Wang, X. Zhang, D. L. Batista, R. Gejman, and A. Klibanski. 2007. Activation of p53 by MEG3 non-coding RNA. Journal of Biological Chemistry 282 (34):24731-42. doi:10.1074/jbc.M702029200.
116. Zonderman, A. B., P. T. Costa, and R. R. McCrae. 1989. Depression as a risk for cancer morbidity and mortality in a nationally representative sample. JAMA 262 (9):1191-95. doi:10.1001/jama.1989.03430090053032.