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Developmental biology - Brain

Dad's smoking may cause problems in his children

While women have long been warned about the dangers of smoking during pregnancy, far less is known about risks for the children of men who smoke...


A new study in mice by the Florida State University College of Medicine produced results that suggest nicotine exposure in men could lead to cognitive deficits in their children and grandchildren. Further studies will be required to know if the same outcomes seen in mice apply to humans.
"Our data raises the possibility that some of the cognitive disabilities found in today's generation of children and adults may be attributable to adverse environmental insults suffered a generation or two ago. Cigarette smoking was more common and more readily accepted by the population in the 1940s, '50s and '60s compared to today. That exposure could be revealing itself as a marked rise in the diagnoses of neuro-developmental disorders such as ADHD and autism?"

Pradeep G. Bhide PhD, Center for Brain Repair, Department of Biomedical Sciences, Florida State University College of Medicine, Tallahassee, Florida, United States of America.

The results are published in the open-access journal PLOS Biology.

The study found changes in a father's sperm which are attributed to exposure to nicotine and led to problems in his genes problems that play a role in his children's memory and learning. These epigenetic, outside the gene plan, changes are believed to be temporary, although some could be long-lasting. More research is needed to understand how long these changes last, says Bhide.

Bhide and College of Medicine colleagues Deirdre McCarthy and Cynthia Vied, recently received a three-year National Institutes of Health grant to support additional work on molecular mechanisms underlying paternal transmission of nicotine exposure. Nicotine's harmful effects on cells in the lungs and brain are part of the evidence given by doctors to avoid smoking. However, absent in the conversation is the research demonstrating how nicotine affects germ cells and/or changes DNA in sperm.

Nicotine exposure for women is recognized as a significant risk factor for behavioral disorders such as ADHD. With men, there was not enough evidence previously to separate genetic risk from environmental influence.
"Doctors may not warn men that their own smoking could be harming their unborn child even if the mother never smoked. I believe our study brings this to the forefront."

Pradeep G. Bhide PhD, Center for Brain Repair, Department of Biomedical Sciences, Florida State University College of Medicine, Tallahassee, Florida, United States of America.

McCarthy exposed males to low-dose nicotine in their drinking water during the developmental stage when they produce sperm. The mice were then bred with female mice never exposed to nicotine. Though these fathers displayed normal behavioral tendencies, both their male and female pups displayed hyperactivity with attention deficit and cognitive inflexibility.
"In analyzing spermatozoa from the father we found multiple genes with epigenetic changes. This includes the dopamine D2 gene, which has an important role in brain development and learning. This is the likely source for the cognitive deficits found in their descendants."

Deirdre M. McCarthy PhD, Center for Brain Repair, Department of Biomedical Sciences, Florida State University College of Medicine, Tallahassee, Florida, United States of America.

While the study was done in mice, previous studies on maternal nicotine exposure were consistent whether performed in mice or in women and children. "I believe the findings from our study can be extrapolated to humans," adds Bhide.

Abstract
Use of tobacco products is injurious to health in men and women. However, tobacco use by pregnant women receives greater scrutiny because it can also compromise the health of future generations. More men smoke cigarettes than women. Yet the impact of nicotine use by men upon their descendants has not been as widely scrutinized. We exposed male C57BL/6 mice to nicotine (200 ug/mL in drinking water) for 12 wk and bred the mice with drug-nave females to produce the F1 generation. Male and female F1 mice were bred with drug-nave partners to produce the F2 generation. We analyzed spontaneous locomotor activity, working memory, attention, and reversal learning in male and female F1 and F2 mice. Both male and female F1 mice derived from the nicotine-exposed males showed significant increases in spontaneous locomotor activity and significant deficits in reversal learning. The male F1 mice also showed significant deficits in attention, brain monoamine content, and dopamine receptor mRNA expression. Examination of the F2 generation showed that male F2 mice derived from paternally nicotine-exposed female F1 mice had significant deficits in reversal learning. Analysis of epigenetic changes in the spermatozoa of the nicotine-exposed male founders (F0) showed significant changes in global DNA methylation and DNA methylation at promoter regions of the dopamine D2 receptor gene. Our findings show that nicotine exposure of male mice produces behavioral changes in multiple generations of descendants. Nicotine-induced changes in spermatozoal DNA methylation are a plausible mechanism for the transgenerational transmission of the phenotypes. These findings underscore the need to enlarge the current focus of research and public policy targeting nicotine exposure of pregnant mothers by a more equitable focus on nicotine exposure of the mother and the father.

Author summary
Use of tobacco products is a major public health concern throughout the world. Cigarette smoking by pregnant women receives significant attention by scientific, public health, and public policy experts because it poses health risks for the mother and her children. Although more men smoke cigarettes than women, the health consequences of paternal smoking for their descendants are much less explored. Using a mouse model, we show that the offspring of nicotine-exposed males have hyperactivity, attention deficit, and cognitive inflexibility. These behavioral phenotypes are associated with attention deficit hyperactivity disorder (ADHD) and autism spectrum disorder in humans. Cognitive inflexibility persists into the third (F2) generation. The neurotransmitters dopamine and noradrenaline and their receptors, critically implicated in neurodevelopmental disorders, are also altered in the offsprings brains. The nicotine-exposed males show significant alterations in spermatozoal DNA methylation patterns, especially at dopamine receptor gene promoter regions, implicating epigenetic modification of germ cell DNA as a mechanism for the transgenerational transmission of the behavioral and neurotransmitter phenotypes. The impact of nicotine on germ cells and the neurobehavioral impairments in multiple subsequent generations call for renewed focus of research and public policy on tobacco use by men and its consequences for their descendants.

Authors
Deirdre M. McCarthy, Thomas J. Morgan Jr., Sarah E. Lowe, Matthew J. Williamson, Thomas J. Spencer, Joseph Biederman and Pradeep G. Bhide.


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Oct 22, 2018   Fetal Timeline   Maternal Timeline   News   News Archive




Although more men smoke cigarettes than women, the health consequences of paternal smoking for their descendants are much less explored. Using a mouse model, we show that the offspring of nicotine-exposed males have hyperactivity, attention deficit, and cognitive inflexibility. Credit: FreePix.com


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