Impact of air pollution exposure on cytokines and histone modification profiles at single-cell levels during pregnancy

Youn Soo Jung; Juan Aguilera; Abhinav Kaushik; Ji Won Ha; Stuart Cansdale; Emily Yang; Rizwan Ahmed; Fred Lurmann; Liza Lutzker; S Katherine Hammond; John Balmes; Elizabeth Noth; Trevor D Burt; Nima Aghaeepour; Anne R Waldrop; Purvesh Khatri; Paul J Utz; Yael Rosenburg-Hasson; Rosemarie DeKruyff; Holden T Maecker; Mary M Johnson; Kari C Nadeau

doi:10.1126/sciadv.adp5227

Impact of air pollution exposure on cytokines and histone modification profiles at single-cell levels during pregnancy

Sci Adv. 2024 Nov 29;10(48):eadp5227. doi: 10.1126/sciadv.adp5227. Epub 2024 Nov 29.

Authors

Youn Soo Jung¹, Juan Aguilera², Abhinav Kaushik¹, Ji Won Ha^{3

4}, Stuart Cansdale⁴, Emily Yang³, Rizwan Ahmed³, Fred Lurmann^{5

6}, Liza Lutzker⁵, S Katherine Hammond⁵, John Balmes^{5

7

8}, Elizabeth Noth⁵, Trevor D Burt⁹, Nima Aghaeepour¹⁰, Anne R Waldrop¹¹, Purvesh Khatri¹², Paul J Utz³, Yael Rosenburg-Hasson¹³, Rosemarie DeKruyff⁴, Holden T Maecker¹³, Mary M Johnson¹, Kari C Nadeau^{1

14}

Affiliations

¹ Harvard T.H. Chan School of Public Health, Harvard University, Boston, MA, USA.
² School of Public Health, The University of Texas Health Science Center at Houston, Houston, TX, USA.
³ Division of Immunology and Rheumatology, Stanford University, Palo Alto, CA, USA.
⁴ Sean N. Parker Center for Allergy and Asthma Research, Stanford University, Palo Alto, CA, USA.
⁵ School of Public Health, University of California, Berkeley, Berkeley, CA, USA.
⁶ Sonoma Technology Inc., Petaluma, CA, USA.
⁷ Department of Medicine, University of California, San Francisco, San Francisco, CA, USA.
⁸ California Air Resources Board, Riverside, CA, USA.
⁹ Department of Pediatrics, Division of Neonatology, Duke University School of Medicine, Durham, NC, USA.
¹⁰ Department of Medicine, Stanford University, Palo Alto, CA, USA.
¹¹ Department of Obstetrics and Gynecology, Stanford University, Palo Alto, CA, USA.
¹² Department of Medicine, Institute for Immunity, Transplantation, and Infection, Stanford University, Palo Alto, CA, USA.
¹³ Department of Microbiology and Immunology, Stanford University, Palo Alto, CA, USA.
¹⁴ Beth Israel Deaconess Medical Center, Boston, MA, USA.

Abstract

Fine particulate matter (PM_2.5) exposure can induce immune system pathology via epigenetic modification, affecting pregnancy outcomes. Our study investigated the association between PM_2.5 exposure and immune response, as well as epigenetic changes using high-dimensional epigenetic landscape profiling using cytometry by time-of-flight (EpiTOF) at the single cell. We found statistically significant associations between PM_2.5 exposure and levels of certain cytokines [interleukin-1RA (IL-1RA), IL-8/CXCL8, IL-18, and IL-27)] and histone posttranslational modifications (HPTMs) in immune cells (HPTMs: H3K9ac, H3K23ac, H3K27ac, H2BK120ub, H4K20me1/3, and H3K9me1/2) among pregnant and nonpregnant women. The cord blood of neonates with high maternal PM_2.5 exposure showed lower IL-27 than those with low exposure. Furthermore, PM_2.5 exposure affects the co-modification profiles of cytokines between pregnant women and their neonates, along with HPTMs in each immune cell type between pregnant and nonpregnant women. These modifications in specific histones and cytokines could indicate the toxicological mechanism of PM_2.5 exposure in inflammation, inflammasome pathway, and pregnancy complications.

MeSH terms

Adult
Air Pollutants
Air Pollution* / adverse effects
Cytokines* / metabolism
Epigenesis, Genetic
Female
Histone Code
Histones* / metabolism
Humans
Infant, Newborn
Maternal Exposure / adverse effects
Particulate Matter* / adverse effects
Pregnancy
Protein Processing, Post-Translational
Single-Cell Analysis

Substances

Cytokines
Particulate Matter
Histones
Air Pollutants