Joshua Robinson, PhD

Associate Professor
Ob/Gyn, Reproductive Sciences
+1 415 476-4509

During human pregnancy, the embryo/fetus is exposed to thousands of unique environmental chemicals with unknown consequences. My research aims to determine the potential effects of these compounds and to identify the mechanistic links between environmental exposures in utero and adverse developmental outcomes (e.g., neurodevelopmental disorders, neural tube defects, placental diseases). To study these relationships, we employ three model systems: human embryonic stem cells, rodent whole embryo culture, and primary human trophoblasts. We combine classical molecular, genomic, morphological/imaging, and in silico based approaches to conduct in-depth chemical assessments and to determine modes of action. Our current investigations are focused on evaluating the effects of polybrominated diphenyl ethers (PBDEs)—commonly used flame retardants—and their alternatives on human pregnancy (in vitro). Additional research projects in the lab include: 1) establishing alternative model systems for developmental toxicology; 2) identifying human biomarkers of response; 3) developing strategies to integrate diverse toxicogenomic data; and 4) characterizing age-dependent differences in human xenobiotic metabolism. We anticipate that this research—which coalesces elements of developmental toxicology, genomics, and risk assessment—will lead to the discovery of gene-environment interactions underlying toxicity, and future prevention of specific chemical exposures that occur during human pregnancy.

Publications: 

Gravidity influences distinct transcriptional profiles of maternal and fetal placental macrophages at term.

Frontiers in immunology

Ozarslan N, Robinson JF, Buarpung S, Kim MY, Ansbro MR, Akram J, Montoya DJ, Kamya MR, Kakuru A, Dorsey G, Rosenthal PJ, Cheng G, Feeney ME, Fisher SJ, Gaw SL

RosetteArray ® Platform for Quantitative High-Throughput Screening of Human Neurodevelopmental Risk.

bioRxiv : the preprint server for biology

Lundin BF, Knight GT, Fedorchak NJ, Krucki K, Iyer N, Maher JE, Izban NR, Roberts A, Cicero MR, Robinson JF, Iskandar BJ, Willett R, Ashton RS

Rapid identification of reproductive toxicants among environmental chemicals using an in vivo evaluation of gametogenesis in budding yeast Saccharomyces cerevisiae.

Reproductive toxicology (Elmsford, N.Y.)

Kumar R, Oke A, Rockmill B, de Cruz M, Verduzco R, Shodhan A, Woodruff-Madeira X, Abrahamsson DP, Varshavsky J, Lam J, Robinson JF, Allard P, Woodruff TJ, Fung JC

Analyzing high-throughput assay data to advance the rapid screening of environmental chemicals for human reproductive toxicity.

bioRxiv : the preprint server for biology

Varshavsky JR, Lam J, Cooper C, Allard P, Fung J, Oke A, Kumar R, Robinson JF, Woodruff TJ

Placental Malaria Induces a Unique Placental Methylation Profile Associated with Fetal Growth Restriction.

bioRxiv : the preprint server for biology

Ozarslan N, Mong C, Ategeka J, Li L, Buarpung S, Robinson JF, Kizza J, Kakuru A, Kamya MR, Dorsey G, Rosenthal PJ, Gaw SL

Screening and characterization of 133 physiologically-relevant environmental chemicals for reproductive toxicity.

Reproductive toxicology (Elmsford, N.Y.)

Ulaganathan G, Jiang H, Canio N, Oke A, Armstrong SS, Abrahamsson D, Varshavsky JR, Lam J, Cooper C, Robinson JF, Fung JC, Woodruff TJ, Allard P

High rates of placental inflammation among samples collected by the Multi-Omics for Mothers and Infants consortium.

American journal of obstetrics and gynecology

Robinson JF, Das S, Khan W, Khanam R, Price JT, Rahman A, Ahmed S, Ali SM, Deb S, Deveale B, Dutta A, Gormley M, Hall SC, Hasan ASMT, Hotwani A, Juma MH, Kasaro MP, Khalid J, Kshetrapal P, McMaster MT, Mehmood U, Nisar I, Pervin J, Rahman S, Raqib R, San A, Sarker P, Tuomivaara ST, Zhang G, Zhou Y, Aktar S, Baqui AH, Jehan F, Sazawal S, Stringer JSA, Fisher SJ

Screening and characterization of 133 physiologically-relevant environmental chemicals for reproductive toxicity.

bioRxiv : the preprint server for biology

Ulaganathan G, Jiang H, Canio N, Oke A, Armstrong SS, Abrahamsson D, Varshavsky JR, Lam J, Cooper C, Robinson JF, Fung JC, Woodruff TJ, Allard P

Perfluorooctanoic Acid Induces Transcriptomic Alterations in 2nd Trimester Human Cytotrophoblasts.

Toxicological sciences : an official journal of the Society of Toxicology

Chen H, Kapidzic M, Gantar D, Aksel S, Levan J, Abrahamsson DP, Jigmeddagva U, Basrai S, San A, Gaw SL, Woodruff TJ, Fisher SJ, Robinson JF

Distinct transcriptional profiles of maternal and fetal placental macrophages at term are associated with gravidity.

bioRxiv : the preprint server for biology

Ozarslan N, Robinson JF, Buarpung S, Kim MY, Ansbro MR, Akram J, Montoya DJ, Kamya MR, Kakuru A, Dorsey G, Rosenthal PJ, Cheng G, Feeney ME, Fisher SJ, Gaw SL

Proteomic analyses of primary human villous trophoblasts exposed to flame retardant BDE-47 using SWATH-MS.

Toxicology

Chen H, Williams KE, Kwan EY, Kapidzic M, Puckett KA, San A, Fisher SJ, Robinson JF

Retrospective analysis of wildfire smoke exposure and birth weight outcomes in the San Francisco Bay Area of California.

Environmental research, health : ERH

Fernández ACG, Basilio E, Benmarhnia T, Roger J, Gaw SL, Robinson JF, Padula AM

Society for Birth Defects Research and Prevention 2022-2027 strategic plan.

Birth defects research

Makris SL, Beyer BK, DeLise A, Williams AL, Roberts LG, Hardy JR, Robinson JF, Feldkamp ML

Minimal mRNA uptake and inflammatory response to COVID-19 mRNA vaccine exposure in human placental explants.

medRxiv : the preprint server for health sciences

Gonzalez V, Li L, Buarpung S, Prahl M, Robinson JF, Gaw SL

A science-based agenda for health-protective chemical assessments and decisions: overview and consensus statement.

Environmental health : a global access science source

Woodruff TJ, Rayasam SDG, Axelrad DA, Koman PD, Chartres N, Bennett DH, Birnbaum LS, Brown P, Carignan CC, Cooper C, Cranor CF, Diamond ML, Franjevic S, Gartner EC, Hattis D, Hauser R, Heiger-Bernays W, Joglekar R, Lam J, Levy JI, MacRoy PM, Maffini MV, Marquez EC, Morello-Frosch R, Nachman KE, Nielsen GH, Oksas C, Abrahamsson DP, Patisaul HB, Patton S, Robinson JF, Rodgers KM, Rossi MS, Rudel RA, Sass JB, Sathyanarayana S, Schettler T, Shaffer RM, Shamasunder B, Shepard PM, Shrader-Frechette K, Solomon GM, Subra WA, Vandenberg LN, Varshavsky JR, White RF, Zarker K, Zeise L

Current practice and recommendations for advancing how human variability and susceptibility are considered in chemical risk assessment.

Environmental health : a global access science source

Varshavsky JR, Rayasam SDG, Sass JB, Axelrad DA, Cranor CF, Hattis D, Hauser R, Koman PD, Marquez EC, Morello-Frosch R, Oksas C, Patton S, Robinson JF, Sathyanarayana S, Shepard PM, Woodruff TJ

Gestational age-dependent decrease in fetal Hofbauer cells in placentas from pregnancies exposed to wildfire smoke in California.

medRxiv : the preprint server for health sciences

Basilio E, Ozarslan N, Buarpung S, Benmarhnia T, Padula AM, Robinson JF, Gaw SL

Wildfire Smoke Exposure during Pregnancy: A Review of Potential Mechanisms of Placental Toxicity, Impact on Obstetric Outcomes, and Strategies to Reduce Exposure.

International journal of environmental research and public health

Basilio E, Chen R, Fernandez AC, Padula AM, Robinson JF, Gaw SL

Modeling the transplacental transfer of small molecules using machine learning: a case study on per- and polyfluorinated substances (PFAS).

Journal of exposure science & environmental epidemiology

Abrahamsson D, Siddharth A, Robinson JF, Soshilov A, Elmore S, Cogliano V, Ng C, Khan E, Ashton R, Chiu WA, Fung J, Zeise L, Woodruff TJ

Associations of per- and polyfluoroalkyl substances (PFAS) and their mixture with oxidative stress biomarkers during pregnancy.

Environment international

Taibl KR, Schantz S, Aung MT, Padula A, Geiger S, Smith S, Park JS, Milne GL, Robinson JF, Woodruff TJ, Morello-Frosch R, Eick SM

Neutralizing antibody activity against SARS-CoV-2 variants in gestational age-matched mother-infant dyads after infection or vaccination.

JCI insight

Matsui Y, Li L, Prahl M, Cassidy AG, Ozarslan N, Golan Y, Gonzalez VJ, Lin CY, Jigmeddagva U, Chidboy MA, Montano M, Taha TY, Khalid MM, Sreekumar B, Hayashi JM, Chen PY, Kumar GR, Warrier L, Wu AH, Song D, Jegatheesan P, Rai DS, Govindaswami B, Needens J, Rincon M, Myatt L, Asiodu IV, Flaherman VJ, Afshar Y, Jacoby VL, Murtha AP, Robinson JF, Ott M, Greene WC, Gaw SL

Integrated analysis of transcriptomic datasets to identify placental biomarkers of spontaneous preterm birth.

Placenta

Sobhani NC, Mernoff R, Abraha M, Okorie CN, Marquez-Magana L, Gaw SL, Robinson JF

Global proteomic analyses of human cytotrophoblast differentiation/invasion.

Development (Cambridge, England)

Chen H, Williams KE, Kwan EY, Kapidzic M, Puckett KA, Aburajab RK, Robinson JF, Fisher SJ

Organophosphate Flame Retardants, Highly Fluorinated Chemicals, and Biomarkers of Placental Development and Disease During Mid-Gestation.

Toxicological sciences : an official journal of the Society of Toxicology

Varshavsky JR, Robinson JF, Zhou Y, Puckett KA, Kwan E, Buarpung S, Aburajab R, Gaw SL, Sen S, Gao S, Smith SC, Park JS, Zakharevich I, Gerona RR, Fisher SJ, Woodruff TJ

Human placental cytotrophoblast epigenome dynamics over gestation and alterations in placental disease.

Developmental cell

Zhang B, Kim MY, Elliot G, Zhou Y, Zhao G, Li D, Lowdon RF, Gormley M, Kapidzic M, Robinson JF, McMaster MT, Hong C, Mazor T, Hamilton E, Sears RL, Pehrsson EC, Marra MA, Jones SJM, Bilenky M, Hirst M, Wang T, Costello JF, Fisher SJ

Cytotrophoblast extracellular vesicles enhance decidual cell secretion of immune modulators via TNFα.

Development (Cambridge, England)

Taylor SK, Houshdaran S, Robinson JF, Gormley MJ, Kwan EY, Kapidzic M, Schilling B, Giudice LC, Fisher SJ

Differences in cytochrome p450 enzyme expression and activity in fetal and adult tissues.

Placenta

Robinson JF, Hamilton EG, Lam J, Chen H, Woodruff TJ

Racial/ethnic and geographic differences in polybrominated diphenyl ether (PBDE) levels across maternal, placental, and fetal tissues during mid-gestation.

Scientific reports

Varshavsky JR, Sen S, Robinson JF, Smith SC, Frankenfield J, Wang Y, Yeh G, Park JS, Fisher SJ, Woodruff TJ

Up-regulated cytotrophoblast DOCK4 contributes to over-invasion in placenta accreta spectrum.

Proceedings of the National Academy of Sciences of the United States of America

McNally L, Zhou Y, Robinson JF, Zhao G, Chen LM, Chen H, Kim MY, Kapidzic M, Gormley M, Hannibal R, Fisher SJ

Association of polybrominated diphenyl ether (PBDE) levels with biomarkers of placental development and disease during mid-gestation.

Environmental health : a global access science source

Varshavsky JR, Robinson JF, Zhou Y, Puckett KA, Kwan E, Buarpung S, Aburajab R, Gaw SL, Sen S, Smith SC, Frankenfield J, Park JS, Fisher SJ, Woodruff TJ

Trisomy 21 is Associated with Caspase-2 Upregulation in Cytotrophoblasts at the Maternal-Fetal Interface.

Reproductive sciences (Thousand Oaks, Calif.)

Leon-Martinez D, Robinson JF, Zdravkovic T, Genbacev O, Gormley M, Mcmaster M, Fisher SJ, Bianco K

Circulating Monocytes, Tissue Macrophages, and Malaria.

Journal of tropical medicine

Ozarslan N, Robinson JF, Gaw SL

Using a Multi-Stage hESC Model to Characterize BDE-47 Toxicity during Neurogenesis.

Toxicological sciences : an official journal of the Society of Toxicology

Chen H, Seifikar H, Larocque N, Kim Y, Khatib I, Fernandez CJ, Abello N, Robinson JF

Genomic Profiling of BDE-47 Effects on Human Placental Cytotrophoblasts.

Toxicological sciences : an official journal of the Society of Toxicology

Robinson JF, Kapidzic M, Hamilton EG, Chen H, Puckett KW, Zhou Y, Ona K, Parry E, Wang Y, Park JS, Costello JF, Fisher SJ

Convergence of placenta biology and genetic risk for schizophrenia.

Nature medicine

Ursini G, Punzi G, Chen Q, Marenco S, Robinson JF, Porcelli A, Hamilton EG, Mitjans M, Maddalena G, Begemann M, Seidel J, Yanamori H, Jaffe AE, Berman KF, Egan MF, Straub RE, Colantuoni C, Blasi G, Hashimoto R, Rujescu D, Ehrenreich H, Bertolino A, Weinberger DR

Transcriptional Dynamics of Cultured Human Villous Cytotrophoblasts.

Endocrinology

Robinson JF, Kapidzic M, Gormley M, Ona K, Dent T, Seifikar H, Hamilton EG, Fisher SJ

A genomics-based framework for identifying biomarkers of human neurodevelopmental toxicity.

Reproductive toxicology (Elmsford, N.Y.)

Robinson JF, Gormley MJ, Fisher SJ

Rbpj links uterine transformation and embryo orientation.

Cell research

Robinson JF, Fisher SJ

Valproic acid-induced gene expression responses in rat whole embryo culture and comparison across in vitro developmental and non-developmental models.

Reproductive toxicology (Elmsford, N.Y.)

Tonk EC, Robinson JF, Verhoef A, Theunissen PT, Pennings JL, Piersma AH

Toxicogenomic approaches in developmental toxicology testing.

Methods in molecular biology (Clifton, N.J.)

Robinson JF, Piersma AH

Complementary detection of embryotoxic properties of substances in the neural and cardiac embryonic stem cell tests.

Toxicological sciences : an official journal of the Society of Toxicology

Theunissen PT, Pennings JL, van Dartel DA, Robinson JF, Kleinjans JC, Piersma AH

Dose-response analysis of phthalate effects on gene expression in rat whole embryo culture.

Toxicology and applied pharmacology

Robinson JF, Verhoef A, van Beelen VA, Pennings JL, Piersma AH

Dose response analysis of monophthalates in the murine embryonic stem cell test assessed by cardiomyocyte differentiation and gene expression.

Reproductive toxicology (Elmsford, N.Y.)

Schulpen SH, Robinson JF, Pennings JL, van Dartel DA, Piersma AH

Triazole induced concentration-related gene signatures in rat whole embryo culture.

Reproductive toxicology (Elmsford, N.Y.)

Robinson JF, Tonk EC, Verhoef A, Piersma AH

Compound-specific effects of diverse neurodevelopmental toxicants on global gene expression in the neural embryonic stem cell test (ESTn).

Toxicology and applied pharmacology

Theunissen PT, Robinson JF, Pennings JL, van Herwijnen MH, Kleinjans JC, Piersma AH

A comparison of gene expression responses in rat whole embryo culture and in vivo: time-dependent retinoic acid-induced teratogenic response.

Toxicological sciences : an official journal of the Society of Toxicology

Robinson JF, Verhoef A, Pennings JL, Pronk TE, Piersma AH

Transcriptomic analysis of neurulation and early organogenesis in rat embryos: an in vivo and ex vivo comparison.

Toxicological sciences : an official journal of the Society of Toxicology

Robinson JF, Verhoef A, Piersma AH

A review of toxicogenomic approaches in developmental toxicology.

Methods in molecular biology (Clifton, N.J.)

Robinson JF, Pennings JL, Piersma AH

Transcriptomic concentration-response evaluation of valproic acid, cyproconazole, and hexaconazole in the neural embryonic stem cell test (ESTn).

Toxicological sciences : an official journal of the Society of Toxicology

Theunissen PT, Robinson JF, Pennings JL, de Jong E, Claessen SM, Kleinjans JC, Piersma AH

Comparison of MeHg-induced toxicogenomic responses across in vivo and in vitro models used in developmental toxicology.

Reproductive toxicology (Elmsford, N.Y.)

Robinson JF, Theunissen PT, van Dartel DA, Pennings JL, Faustman EM, Piersma AH

Time-response evaluation by transcriptomics of methylmercury effects on neural differentiation of murine embryonic stem cells.

Toxicological sciences : an official journal of the Society of Toxicology

Theunissen PT, Pennings JL, Robinson JF, Claessen SM, Kleinjans JC, Piersma AH

Gene set assembly for quantitative prediction of developmental toxicity in the embryonic stem cell test.

Toxicology

Pennings JL, van Dartel DA, Robinson JF, Pronk TE, Piersma AH

Cadmium induced p53-dependent activation of stress signaling, accumulation of ubiquitinated proteins, and apoptosis in mouse embryonic fibroblast cells.

Toxicological sciences : an official journal of the Society of Toxicology

Yu X, Sidhu JS, Hong S, Robinson JF, Ponce RA, Faustman EM

Discriminating classes of developmental toxicants using gene expression profiling in the embryonic stem cell test.

Toxicology letters

van Dartel DA, Pennings JL, Robinson JF, Kleinjans JC, Piersma AH

Integrating genetic and toxicogenomic information for determining underlying susceptibility to developmental disorders.

Birth defects research. Part A, Clinical and molecular teratology

Robinson JF, Port JA, Yu X, Faustman EM

Arsenic- and cadmium-induced toxicogenomic response in mouse embryos undergoing neurulation.

Toxicology and applied pharmacology

Robinson JF, Yu X, Moreira EG, Hong S, Faustman EM

Embryotoxicant-specific transcriptomic responses in rat postimplantation whole-embryo culture.

Toxicological sciences : an official journal of the Society of Toxicology

Robinson JF, van Beelen VA, Verhoef A, Renkens MF, Luijten M, van Herwijnen MH, Westerman A, Pennings JL, Piersma AH

A systems-based approach to investigate dose- and time-dependent methylmercury-induced gene expression response in C57BL/6 mouse embryos undergoing neurulation.

Birth defects research. Part B, Developmental and reproductive toxicology

Robinson JF, Guerrette Z, Yu X, Hong S, Faustman EM

Methylmercury induced toxicogenomic response in C57 and SWV mouse embryos undergoing neural tube closure.

Reproductive toxicology (Elmsford, N.Y.)

Robinson JF, Griffith WC, Yu X, Hong S, Kim E, Faustman EM

Toxicogenomic profiling in maternal and fetal rodent brains following gestational exposure to chlorpyrifos.

Toxicology and applied pharmacology

Moreira EG, Yu X, Robinson JF, Griffith W, Hong SW, Beyer RP, Bammler TK, Faustman EM

Embryonic toxicokinetic and dynamic differences underlying strain sensitivity to cadmium during neurulation.

Reproductive toxicology (Elmsford, N.Y.)

Robinson JF, Yu X, Hong S, Zhou C, Kim N, DeMasi D, Faustman EM

Cadmium-induced differential toxicogenomic response in resistant and sensitive mouse strains undergoing neurulation.

Toxicological sciences : an official journal of the Society of Toxicology

Robinson JF, Yu X, Hong S, Griffith WC, Beyer R, Kim E, Faustman EM

Research Area: 
Clinical Research