Reduced levels of miRNAs 449 and 34 in sperm of mice and men exposed to early life stress

Translational Psychiatry

Volumn 8, Issue 1, 2018, Pages

  Dickson, David A ^a   Paulus, Jessica K ^b   Mensah, Virginia ^c   Lem, Janis ^b   Saavedra Rodriguez, Lorena ^d   Gentry, Adrienne ^e   Pagidas, Kelly ^e   Feig, Larry A ^a,d  

^a TUFTS UNIVERSITY   (United States)

^b TUFTS MEDICAL CENTER   (United States)

^c BROWN UNIVERSITY   (United States)

^d TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e University of Louisville School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 34; MICRORNA 449; UNCLASSIFIED DRUG; MIRN34 MICRORNA, HUMAN; MIRN34 MICRORNA, MOUSE; MIRN449 MICRORNA, HUMAN; MIRN449 MICRORNA, MOUSE;

ADOLESCENT; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; BRAIN DEVELOPMENT; CHRONIC STRESS; CONTROLLED STUDY; DYSFUNCTIONAL FAMILY; EARLY LIFE STRESS; EMBRYO; FEMALE; MALE; MATING; MOUSE; NONHUMAN; PERSONAL EXPERIENCE; PROGENY; SPERM; SPERMATOGENESIS; ANIMAL; CAUCASIAN; CHILDHOOD TRAUMA SURVIVOR; HUMAN; MENTAL STRESS; METABOLISM; SPERMATOZOON;

ADULT; ADULT SURVIVORS OF CHILD ADVERSE EVENTS; ANIMALS; EUROPEAN CONTINENTAL ANCESTRY GROUP; HUMANS; MALE; MICE; MICRORNAS; SPERMATOZOA; STRESS, PSYCHOLOGICAL;

EID: 85047406530     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/s41398-018-0146-2     Document Type: Article

References (40)

1. Kalmakis, K. A. & Chandler, G. E. Health consequences of adverse childhood experiences: a systematic review. J. Am. Assoc. Nurse Pract. 27, 457-465 (2015).
2. Chapman, D. P. et al. Adverse childhood experiences and the risk of depressive disorders in adulthood. J. Affect. Disord. 82, 217-225 (2004).
3. Dube, S. R. et al. Childhood abuse, household dysfunction, and the risk of attempted suicide throughout the life span: findings from the Adverse Childhood Experiences Study. JAMA 286, 3089-3096 (2001).
4. Waite, R., Gerrity, P. & Arango, R. Assessment for and response to adverse childhood experiences. J. Psychosoc. Nurs. Ment. Health Serv. 48, 51-61 (2010).
5. Kalmakis, K. A., Chandler, G. E., Roberts, S. J. & Leung, K. Nurse practitioner screening for childhood adversity among adult primary care patients: a mixed-method study. J. Am. Assoc. Nurse Pract. 29, 35-45 (2017).
6. McGuinness, T. M. & Waldrop, J. R. Adverse childhood experiences and the mental health of veterans. J. Psychosoc. Nurs. Ment. Health Serv. 53, 23-26 (2015).
7. LeardMann, C. A., Smith, B. & Ryan, M. A. Do adverse childhood experiences increase the risk of postdeployment posttraumatic stress disorder in US Marines? BMC Public. Health 10, 437 (2010).
8. Phillips, C. J., Leardmann, C. A., Gumbs, G. R. & Smith, B. Risk factors for posttraumatic stress disorder among deployed US male marines. BMC Psychiatry 10, 52 (2010).
9. Santavirta, T., Santavirta, N. & Gilman, S. E. Association of the World War II finnish evacuation of children with psychiatric hospitalization in the next generation. JAMA Psychiatry 75, 21-27 (2018).
10. Bohacek, J. & Mansuy, I. M. Molecular insights into transgenerational non-genetic inheritance of acquired behaviours. Nat. Rev. Genet. 16, 641-652 (2015).
11. Rodgers, A. B. & Bale, T. L. Germ cell origins of posttraumatic stress disorder risk: the transgenerational impact of parental stress experience. Biol. Psychiatry 78, 307-314 (2015).
12. Dietz, D. M. et al. Paternal transmission of stress-induced pathologies. Biol. Psychiatry 70, 408-414 (2011).
13. He, N. et al. Parental life events cause behavioral difference among offspring: adult pre-gestational restraint stress reduces anxiety across generations. Sci. Rep. 6, 39497 (2016).
14. Rodgers, A. B., Morgan, C. P., Bronson, S. L., Revello, S. & Bale, T. L. Paternal stress exposure alters sperm microRNA content and reprograms offspring HPA stress axis regulation. J. Neurosci. 33, 9003-9012 (2013).
15. Saavedra-Rodriguez, L. & Feig, L. A. Chronic social instability induces anxiety and defective social interactions across generations. Biol. Psychiatry 73, 44-53 (2013).
16. Franklin, T. B. et al. Epigenetic transmission of the impact of early stress across generations. Biol. Psychiatry 68, 408-415 (2010).
17. Jodar, M., Selvaraju, S., Sendler, E., Diamond, M. P. & Krawetz, S. A. The presence, role and clinical use of spermatozoal RNAs. Hum. Reprod. Update 19, 604-624 (2013).
18. Ostermeier, G. C., Miller, D., Huntriss, J. D., Diamond, M. P. & Krawetz, S. A. Reproductive biology: delivering spermatozoan RNA to the oocyte. Nature 429, 154 (2004).
19. Sendler, E. et al. Stability, delivery and functions of human sperm RNAs at fertilization. Nucleic Acids Res. 41, 4104-4117 (2013).
20. Gapp, K. et al. Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice. Nat. Neurosci. 17, 667-669 (2014).
21. Rodgers, A. B., Morgan, C. P., Leu, N. A. & Bale, T. L. Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress. Proc. Natl Acad. Sci. USA 112, 13699-13704 (2015).
22. Wu, J. et al. Two miRNA clusters, miR-34b/c and miR-449, are essential for normal brain development, motile ciliogenesis, and spermatogenesis. Proc. Natl Acad. Sci. USA 111, E2851-E2857 (2014).
23. Fededa, J. P. et al. MicroRNA-34/449 controls mitotic spindle orientation during mammalian cortex development. EMBO J. 35, 2386-2398 (2016).
24. Andolina, D., Di Segni, M. & Ventura, R. MiRNA-34 and stress response. Oncotarget 8, 5658-5659 (2017).
25. Haramati, S. et al. MicroRNA as repressors of stress-induced anxiety: the case of amygdalar miR-34. J. Neurosci. 31, 14191-14203 (2011).
26. Andolina, D. et al. Effects of lack of microRNA-34 on the neural circuitry underlying the stress response and anxiety. Neuropharmacology 107, 305-316 (2016).
27. Kaneko, S. et al. Purification of human sperm by a discontinuous Percoll density gradient with an innercolumn. Biol. Reprod. 35, 1059-1063 (1986).
28. Check, J. H., Adelson, H. G., Schubert, B. R. & Bollendorf, A. Evaluation of sperm morphology using Kruger's strict criteria. Arch. Androl. 28, 15-17 (1992).
29. Campbell, J. A., Walker, R. J. & Egede, L. E. Associations between adverse childhood experiences, high-risk behaviors, and morbidity in adulthood. Am. J. Prev. Med. 50, 344-352 (2016).
30. Marczylo, E. L., Amoako, A. A., Konje, J. C., Gant, T. W. & Marczylo, T. H. Smoking induces differential miRNA expression in human spermatozoa: a potential transgenerational epigenetic concern? Epigenetics 7, 432-439 (2012).
31. Williamson, D. F., Thompson, T. J., Anda, R. F., Dietz, W. H. & Felitti, V. Body weight and obesity in adults and self-reported abuse in childhood. Int. J. Obes. Relat. Metab. Disord. 26, 1075-1082 (2002).
32. Donkin, I. et al. Obesity and bariatric surgery drive epigenetic variation of spermatozoa in humans. Cell Metab. 23, 369-378 (2016).
33. Schmidt, M. V. et al. Persistent neuroendocrine and behavioral effects of a novel, etiologically relevant mouse paradigm for chronic social stress during adolescence. Psychoneuroendocrinology 32, 417-429 (2007).
34. Yuan, S. et al. Sperm-borne miRNAs and endo-siRNAs are important for fertilization and preimplantation embryonic development. Development 143, 635-647 (2016).
35. Reuben, A. et al. Lest we forget: comparing retrospective and prospective assessments of adverse childhood experiences in the prediction of adult health. J. Child. Psychol. Psychiatry 57, 1103-1112 (2016).
36. Abu-Halima, M. et al. Altered microRNA expression profiles of human spermatozoa in patients with different spermatogenic impairments. Fertil. Steril. 99, 1249-1255 e1216 (2013).
37. Cui, L., Fang, L., Shi, B., Qiu, S. & Ye, Y. Spermatozoa micro ribonucleic acid-34c level is correlated with intracytoplasmic sperm injection outcomes. Fertil. Steril. 104, 312-317 e311 (2015).
38. Wang, M. et al. Sperm-borne miR-449b influences cleavage, epigenetic reprogramming and apoptosis of SCNT embryos in bovine. Sci. Rep. 7, 13403 (2017).
39. Merrick, M. T., Leeb, R. T. & Lee, R. D. Examining the role of safe, stable, and nurturing relationships in the intergenerational continuity of child maltreatment - introduction to the special issue. J. Adolesc. Health 53, S1-S3 (2013).
40. Holman, D. M. et al. The association between adverse childhood experiences and risk of cancer in adulthood: a systematic review of the literature. Pediatrics 138, S81-S91 (2016).