- Professor
Biography
- Professor, College of Arts & Sciences, School of Biological Sciences
- Faculty, Neuroscience Program within the College of Veterinary Medicine, Department of Integrative Physiology and Neuroscience
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Education
PhD, Biochemistry, Washington State University
Research Interests
Environmentally Induced Epigenetic Transgenerational Inheritance of Disease and Evolution; and Molecular and Cellular Control of Testis and Ovary Development and Biology
General interest is in mammalian reproduction and environmental epigenetics on a systems biology level. The laboratory has had a long standing research program to study gonadal development and function on a molecular, cellular and physiological level (systems biology). More recently, the ability of environmental factors to act on gonadal development has been shown to cause the epigenetic transgenerational inheritance of disease and phenotypic variation which impacts areas of biology such as medicine or evolution. This non-genetic form of inheritance has now become a predominant research program in the lab.
Basic reproductive biology research projects involve the investigation of how different cell types in a tissue interact and communicate to regulate cellular growth and differentiation, with emphasis in the area of reproductive biology. The cells of interest and specific interactions investigated have an integral role in controlling the development of the spermatozoa and oocyte. Our observations indicate that the mesenchymal cells of both the testis and ovary produce inducer substances that alter the differentiation and function of adjacent epithelial cells. Information obtained from these studies is necessary before novel therapeutic agents can be designed and targeted at reproductive cells for the prevention of infertility or to act as contraceptives. The research is designed to understand testis and ovary development and function on a systems biology level.
Previously we have found that environmental toxicants (e.g. endocrine disruptors) have the ability to modify local cell-cell interactions in the testis and ovary during fetal development that influences epigenetic programming of the germline. If gestating females are exposed to environmental toxicants at the time of fetal gonadal sex determination, a number of adult onset diseases develop. Interestingly this phenotype is transgenerational, such that what your pregnant great grandmother was exposed to may cause disease in you with no subsequent exposure. This has been termed epigenetic transgenerational inheritance. An epigenetic effect on the programming of the germ-line was observed and is the causal factor in this epigenetic transgenerational effect of environmental toxicants. In addition to effects on reproduction, numerous other adult onset disease sates are observed including cancer, prostate disease, kidney disease, obesity, immune abnormalities and behavior effects. Further characterization of this phenomena and its impact on disease etiology and evolutionary biology is in progress. Further information is available at www.skinner.wsu.edu.
Representative Publications:
- Skinner MK. (2024) Epigenetic biomarkers for disease susceptibility and preventative medicine. Cell Metabolism. 36(2):263-277.
- Ben Maamar M, Wang Y, Nilsson EE, Beck D, Yan W, Michael K Skinner MK (2023) Transgenerational sperm DMRs escape DNA methylation erasure during embryonic development and epigenetic inheritance. Environ Epigenet. 2023 Jun 3;9(1):dvad003 (1-15).
- Nilsson E, McBirney M, De Santos S, King SE, Beck D, Greeley C, Holder LB, Skinner MK (2023) Multiple Generation Distinct Toxicant Exposures Induce Epigenetic-Transgenerational-Inheritance of Enhanced Pathology and Obesity. Environmental Epigenetics 9(1) dvad006 (1-19).
- Winchester P, Nilsson E, Beck D, Skinner MK. (2022) Premature Birth Buccal Cell Epigenetic Biomarkers to Facilitate Preventative Medicine. Scientific Reports 12, 3361.
- Nilsson E, Ben Maamar M, Skinner MK. (2022) Role of Epigenetic Transgenerational Inheritance in Generational Toxicology. Environmental Epigenetics 16;8(1):1-9, dvac001.
- Ben Maamar M, Beck D, Sadler-Riggleman I, Nilsson E, McCarrey JR, Skinner MK (2022) Developmental Alterations in DNA Methylation During Gametogenesis from Primordial Germ Cells to Sperm. iScience. 2022 Jan 19;25(2):103786.
- Nilsson E, Sadler-Riggleman I, Beck D, Skinner MK (2021) Differential DNA Methylation in Somatic and Sperm cells of Hatchery versus Wild (Natural-Origin) Steelhead Trout Population. Environmental Epigenetics. 7(1):1-17, dvab002.
- Beck D, Ben Maamar M, Skinner MK (2021) Integration of Sperm ncRNA Directed DNA Methylation and DNA Methylation Directed Histone Retention in Epigenetic Transgenerational Inheritance. Epigenetics & Chromatin 14(1):6.
- Garrido N, Cruz F, Rivera Egea R, Simon C, Sadler-Riggleman I, Beck D, Nilsson E, Skinner MK (2021) Sperm DNA Methylation Epimutation Biomarker for Paternal Offspring Autism Susceptibility. Clinical Epigenetics 13(1):6.
- Ben Maamar M, Beck D, Thorson JLM, Nilsson E, Kubsad D, Skinner MK (2020) Glyphosate Induced Transgenerational DNA Methylation and Histone Retention Sperm Epigenetic Biomarkers for Disease. Epigenetics. 9:1-18.
- Ben Maamar M, King S, Nilsson E, Sadler-Riggleman I, Beck D, Skinner MK (2020) Epigenetic Transgenerational Inheritance of Parent-of-Origin Allelic Transmission of Outcross Pathology and Sperm Epimutations. Developmental Biology 458(1):106-119.
- King SE, Skinner MK (2020) Epigenetic Transgenerational Inheritance of Obesity. Trends in Endocrinology & Metabolism Vol. 31, No. 7 pp 478-49.
- Luján S, Caroppo E, Niederberger C, Arce JC, Sadler-Riggleman I, Beck D, Nilsson E, Skinner MK (2019) Sperm DNA Methylation Epimutation Biomarkers for Male Infertility and FSH Therapeutic Responsiveness. Scientific Reports (2019) 9:16786.
- Ben Maamar M, Sadler-Riggleman I, Beck D, McBirney M, Nilsson E, Klukovich R, Xie Y, Tang C, Yan W, Skinner MK (2018) Alterations in sperm DNA Methylation, Non-Coding RNA expression, and histone retention mediate Vinclozolin induced epigenetic transgenerational inheritance of disease. Environmental Epigenetics 4(2):1-19, dvy101.
- McNew S, Beck D, Sadler-Riggleman I, Knutie SA, Koop JAH, Clayton DH, Skinner MK (2017) Epigenetic variation between urban and rural populations of Darwin’s finches. BMC Evolutionary Biology 17:183.
- Skinner MK (2015) Environmental Epigenetics and a Unified Theory of the Molecular Aspects of Evolution: A Neo-Lamarckian Concept that Facilitates Neo-Darwinian Evolution. Genome Biol Evol 7(5): 1296-1302.
- Skinner MK (2014) A New Kind of Inheritance. Scientific American 311(2)41-45.
- Skinner MK, Guerrero-Bosagna C, Haque M, Knutie S, Koop J, and Clayton D (2014) Epigenetics and the Speciation and Evolution of Darwin’s Finches. Genome Biology & Evolution 24;6(8):1972-89.
- Skinner MK, Manikkam M, Tracey R, Nilsson E, Haque Md. M, and Guerrero-Bosagna C (2013) Ancestral DDT Exposure Promotes Epigenetic Transgenerational Inheritance of Obesity. BMC Medicine 11:228.
- Crews D, Gillette R, Manikkam M, Savenkova M and Skinner MK (2012) Epigenetic transgenerational inheritance of altered stress responses. PNAS 5;109(23):9143-8.
- Skinner MK (2010) Metabolic Disorders: Fathers’ nutritional legacy. Nature. 21;467(7318):922-3.
- Anway M, Cupp AS, Uzumcu M and Skinner MK (2005) Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308:1466-1469.