1. Koob G, Kreek MJ. Stress, dysregulation of drug reward
pathways, and the transition to drug dependence. Am
J Psychiatry. 2007;164(8):1149-59. doi: 10.1176/appi.
ajp.2007.05030503.
2. Koob GF. Neurobiology of opioid addiction: opponent process,
hyperkatifeia, and negative reinforcement. Biol Psychiatry.
2020;87(1):44-53. doi: 10.1016/j.biopsych.2019.05.023.
3. Merikangas KR, Stolar M, Stevens DE, Goulet J, Preisig
MA, Fenton B, et al. Familial transmission of substance use
disorders. Arch Gen Psychiatry. 1998;55(11):973-9. doi:
10.1001/archpsyc.55.11.973.
4. Agrawal A, Lynskey MT. Are there genetic influences on
addiction: evidence from family, adoption and twin studies.
Addiction. 2008;103(7):1069-81. doi: 10.1111/j.1360-
0443.2008.02213.x.
5. Mistry CJ, Bawor M, Desai D, Marsh DC, Samaan Z. Genetics
of opioid dependence: a review of the genetic contribution to
opioid dependence. Curr Psychiatry Rev. 2014;10(2):156-67.
doi: 10.2174/1573400510666140320000928.
6. Zheng B, Fletcher J, Zheng F, Lu Q. Gene-by-peerenvironment interaction effects on cigarette, alcohol, and
marijuana use among US high school students of European
ancestry. Soc Sci Med. 2022;309:115249. doi: 10.1016/j.
socscimed.2022.115249.
7. Zhang H, Khan A, Rzhetsky A. Gene-environment interactions
explain a substantial portion of variability of common
neuropsychiatric disorders. Cell Rep Med. 2022;3(9):100736.
doi: 10.1016/j.xcrm.2022.100736.
8. Zhu C, Liang M, Li Y, Feng X, Hong J, Zhou R. Involvement
of epigenetic modifications of GABAergic interneurons in
basolateral amygdala in anxiety-like phenotype of prenatally
stressed mice. Int J Neuropsychopharmacol. 2018;21(6):570-
81. doi: 10.1093/ijnp/pyy006.
9. Browne CJ, Godino A, Salery M, Nestler EJ. Epigenetic
mechanisms of opioid addiction. Biol Psychiatry.
2020;87(1):22-33. doi: 10.1016/j.biopsych.2019.06.027.
10. Martins SS, Fenton MC, Keyes KM, Blanco C, Zhu H, Storr
CL. Mood and anxiety disorders and their association with
non-medical prescription opioid use and prescription
opioid-use disorder: longitudinal evidence from the
National Epidemiologic Study on Alcohol and Related
Conditions. Psychol Med. 2012;42(6):1261-72. doi: 10.1017/
s0033291711002145.
11. Raghav R, Jain R, Jacob TG, Dhawan A, Roy TS. Coadministration of nalbuphine attenuates the morphine-induced
anxiety and dopaminergic alterations in morphine-withdrawn
rats. Psychopharmacology (Berl). 2021;238(4):1193-211. doi:
10.1007/s00213-021-05765-3.
12. Vassoler FM, Byrnes EM. Transgenerational effects on anxietylike behavior following adolescent morphine exposure
in female rats. Behav Brain Res. 2021;406:113239. doi:
10.1016/j.bbr.2021.113239.
13. Akbarabadi A, Sadat-Shirazi MS, Kabbaj M, Nouri ZadehTehrani S, Khalifeh S, Pirri F, et al. Effects of morphine and
maternal care on behaviors and protein expression of male
offspring. Neuroscience. 2021;466:58-76. doi: 10.1016/j.
neuroscience.2021.04.011.
14. Sabzevari S, Rohbani K, Sadat-Shirazi MS, Babhadi-Ashar
N, Shakeri A, Ashabi G, et al. Morphine exposure before
conception affects anxiety-like behavior and CRF level (in the
CSF and plasma) in the adult male offspring. Brain Res Bull.
2019;144:122-31. doi: 10.1016/j.brainresbull.2018.11.022.
15. Ashabi G, Sadat-Shirazi MS, Akbarabadi A, Vousooghi N,
Kheiri Z, Toolee H, et al. Is the nociception mechanism
altered in offspring of morphine-abstinent rats? J Pain.
2018;19(5):529-41. doi: 10.1016/j.jpain.2017.12.268.
16. Ahmadian-Moghadam H, Akbarabadi A, Toolee H, SadatShirazi MS, Khalifeh S, Niknamfar S, et al. Correlation among
the behavioral features in the offspring of morphine-abstinent
rats. Addict Health. 2019;11(4):262-75. doi: 10.22122/ahj.
v11i4.253.
17. Sadat-Shirazi MS, Nouri Zadeh-Tehrani S, Akbarabadi A, Mokri
A, Taleb Zadeh Kasgari B, Zarrindast MR. Exercise can restore
behavioural and molecular changes of intergenerational
morphine effects. Addict Biol. 2022;27(2):e13122. doi:
10.1111/adb.13122.
18. Sadat-Shirazi MS, Karimi F, Kaka G, Ashabi G, Ahmadi I,
Akbarabadi A, et al. Parental morphine exposure enhances
morphine (but not methamphetamine) preference and
increases monoamine oxidase-B level in the nucleus
accumbens. Behav Pharmacol. 2019;30(5):435-45. doi:
10.1097/fbp.0000000000000465.
19. Goldman D, Oroszi G, Ducci F. The genetics of addictions:
uncovering the genes. Nat Rev Genet. 2005;6(7):521-32. doi:
10.1038/nrg1635.
20. Nestler EJ. Molecular basis of long-term plasticity underlying
addiction. Nat Rev Neurosci. 2001;2(2):119-28. doi:
10.1038/35053570.
21. Sadat-Shirazi MS, Sadeghi-Adl M, Akbarabadi A, Ashabi G,
Mokri A, Zarrindast MR. Inter/transgenerational effects of
drugs of abuse: a scoping review. CNS Neurol Disord Drug
Targets. 2023;22(4):512-38. doi: 10.2174/18715273216662
20429122819.
22. Dickson DA, Stohn P, Saavedra Rodriguez L, Hernandez A,
Harrington A, Liaw L, et al. Involvement of early embryonic
miR-409-3p in the establishment of anxiety levels in female
mice. Dev Neurobiol. 2020;80(5-6):160-7. doi: 10.1002/
dneu.22756.
Sabzevari et al
176 Addict Health. Volume 15, Number 3, 2023
23. Gapp K, Jawaid A, Sarkies P, Bohacek J, Pelczar P, Prados
J, et al. Implication of sperm RNAs in transgenerational
inheritance of the effects of early trauma in mice. Nat
Neurosci. 2014;17(5):667-9. doi: 10.1038/nn.3695.
24. Di Emidio G, D’Aurora M, Placidi M, Franchi S, Rossi
G, Stuppia L, et al. Pre-conceptional maternal exposure
to cyclophosphamide results in modifications of DNA
methylation in F1 and F2 mouse oocytes: evidence for
transgenerational effects. Epigenetics. 2019;14(11):1057-64.
doi: 10.1080/15592294.2019.1631111.
25. López-Rodríguez D, Aylwin CF, Delli V, Sevrin E, Campanile
M, Martin M, et al. Multi- and transgenerational outcomes of
an exposure to a mixture of endocrine-disrupting chemicals
(EDCs) on puberty and maternal behavior in the female rat.
Environ Health Perspect. 2021;129(8):87003. doi: 10.1289/
ehp8795.
26. Khan N, Peters RA, Richardson E, Robert KA. Maternal
corticosterone exposure has transgenerational effects on
grand-offspring. Biol Lett. 2016;12(11):20160627. doi:
10.1098/rsbl.2016.0627.
27. Nazeri M, Nezhadi A, Shabani M. Role of opioid system
in empathy-like behaviours in rats. Addict Health.
2019;11(4):216-22. doi: 10.22122/ahj.v11i4.243.
28. Miladi-Gorji H, Rashidy-Pour A, Fathollahi Y. Anxiety
profile in morphine-dependent and withdrawn rats: effect of
voluntary exercise. Physiol Behav. 2012;105(2):195-202. doi:
10.1016/j.physbeh.2011.08.010.
29. Byrnes EM. Transgenerational consequences of adolescent
morphine exposure in female rats: effects on anxiety-like
behaviors and morphine sensitization in adult offspring.
Psychopharmacology (Berl). 2005;182(4):537-44. doi:
10.1007/s00213-005-0122-4.
30. Li CQ, Luo YW, Bi FF, Cui TT, Song L, Cao WY, et al.
Development of anxiety-like behavior via hippocampal IGF2 signaling in the offspring of parental morphine exposure:
effect of enriched environment. Neuropsychopharmacology.
2014;39(12):2777-87. doi: 10.1038/npp.2014.128.
31. Farah Naquiah MZ, James RJ, Suratman S, Lee LS, Mohd
Hafidz MI, Salleh MZ, et al. Transgenerational effects of
paternal heroin addiction on anxiety and aggression behavior
in male offspring. Behav Brain Funct. 2016;12(1):23. doi:
10.1186/s12993-016-0107-y.
32. Vassoler FM, Johnson-Collins NL, Carini LM, Byrnes EM. Next
generation effects of female adolescent morphine exposure:
sex-specific alterations in response to acute morphine emerge
before puberty. Behav Pharmacol. 2014;25(2):173-81. doi:
10.1097/fbp.0000000000000032.