PMID- 37058409 OWN - NLM STAT- MEDLINE DCOM- 20231004 LR - 20240217 IS - 2211-1247 (Electronic) VI - 42 IP - 4 DP - 2023 Apr 25 TI - Maternal diet alters long-term innate immune cell memory in fetal and juvenile hematopoietic stem and progenitor cells in nonhuman primate offspring. PG - 112393 LID - S2211-1247(23)00404-7 [pii] LID - 10.1016/j.celrep.2023.112393 [doi] AB - Maternal overnutrition increases inflammatory and metabolic disease risk in postnatal offspring. This constitutes a major public health concern due to increasing prevalence of these diseases, yet mechanisms remain unclear. Here, using nonhuman primate models, we show that maternal Western-style diet (mWSD) exposure is associated with persistent pro-inflammatory phenotypes at the transcriptional, metabolic, and functional levels in bone marrow-derived macrophages (BMDMs) from 3-year-old juvenile offspring and in hematopoietic stem and progenitor cells (HSPCs) from fetal and juvenile bone marrow and fetal liver. mWSD exposure is also associated with increased oleic acid in fetal and juvenile bone marrow and fetal liver. Assay for transposase-accessible chromatin with sequencing (ATAC-seq) profiling of HSPCs and BMDMs from mWSD-exposed juveniles supports a model in which HSPCs transmit pro-inflammatory memory to myeloid cells beginning in utero. These findings show that maternal diet alters long-term immune cell developmental programming in HSPCs with proposed consequences for chronic diseases featuring altered immune/inflammatory activation across the lifespan. CI - Copyright (c) 2023 The Authors. Published by Elsevier Inc. All rights reserved. FAU - Nash, Michael J AU - Nash MJ AD - Department of Pediatrics, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA. FAU - Dobrinskikh, Evgenia AU - Dobrinskikh E AD - Department of Pediatrics, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA. FAU - Soderborg, Taylor K AU - Soderborg TK AD - Department of Pediatrics, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA. FAU - Janssen, Rachel C AU - Janssen RC AD - Harold Hamm Diabetes Center, University of Oklahoma Health Sciences Center, Oklahoma City, OK 73104, USA. FAU - Takahashi, Diana L AU - Takahashi DL AD - Division of Cardiometabolic Health, Oregon National Primate Research Center, Oregon Health & Science University, Beaverton, OR 97006, USA. FAU - Dean, Tyler A AU - Dean TA AD - Division of Cardiometabolic Health, Oregon National Primate Research Center, Oregon Health & Science University, Beaverton, OR 97006, USA. FAU - Varlamov, Oleg AU - Varlamov O AD - Division of Cardiometabolic Health, Oregon National Primate Research Center, Oregon Health & Science University, Beaverton, OR 97006, USA. FAU - Hennebold, Jon D AU - Hennebold JD AD - Division of Reproductive and Developmental Sciences, Oregon National Primate Research Center, Oregon Health & Science University, Beaverton, OR 97006, USA. FAU - Gannon, Maureen AU - Gannon M AD - Department of Medicine, Division of Diabetes, Endocrinology, and Metabolism, Vanderbilt University Medical Center, Nashville, TN 37235, USA. FAU - Aagaard, Kjersti M AU - Aagaard KM AD - Department of Obstetrics and Gynecology, Division of Maternal-Fetal Medicine, Baylor College of Medicine, Houston, TX 77030, USA. FAU - McCurdy, Carrie E AU - McCurdy CE AD - Department of Human Physiology, University of Oregon, Eugene, OR 97403, USA. FAU - Kievit, Paul AU - Kievit P AD - Division of Cardiometabolic Health, Oregon National Primate Research Center, Oregon Health & Science University, Beaverton, OR 97006, USA. FAU - Bergman, Bryan C AU - Bergman BC AD - Department of Medicine, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA. FAU - Jones, Kenneth L AU - Jones KL AD - Department of Physiology, University of Oklahoma Health Sciences Center, Oklahoma City, OK 73104, USA. FAU - Pietras, Eric M AU - Pietras EM AD - Department of Medicine, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA. FAU - Wesolowski, Stephanie R AU - Wesolowski SR AD - Department of Pediatrics, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USA. FAU - Friedman, Jacob E AU - Friedman JE AD - Harold Hamm Diabetes Center, University of Oklahoma Health Sciences Center, Oklahoma City, OK 73104, USA; Department of Physiology, University of Oklahoma Health Sciences Center, Oklahoma City, OK 73104, USA. Electronic address: jed-friedman@ouhsc.edu. LA - eng GR - P51 OD011092/OD/NIH HHS/United States GR - P30 DK048520/DK/NIDDK NIH HHS/United States GR - P30 NS048154/NS/NINDS NIH HHS/United States GR - R01 DK119394/DK/NIDDK NIH HHS/United States GR - R01 DK108910/DK/NIDDK NIH HHS/United States GR - F30 DK122672/DK/NIDDK NIH HHS/United States GR - R24 DK090964/DK/NIDDK NIH HHS/United States GR - P50 HD071836/HD/NICHD NIH HHS/United States GR - R01 DK128416/DK/NIDDK NIH HHS/United States GR - R01 DK128187/DK/NIDDK NIH HHS/United States GR - P30 DK116073/DK/NIDDK NIH HHS/United States GR - P30 CA225520/CA/NCI NIH HHS/United States PT - Journal Article PT - Research Support, N.I.H., Extramural DEP - 20230413 PL - United States TA - Cell Rep JT - Cell reports JID - 101573691 SB - IM MH - Humans MH - Animals MH - Female MH - *Hematopoietic Stem Cells MH - *Bone Marrow MH - Diet, Western/adverse effects MH - Primates MH - Immunity, Innate PMC - PMC10570400 MID - NIHMS1897947 OTO - NOTNLM OT - CP: Immunology OT - DoHaD OT - Western-style diet OT - epigenetics OT - fatty acid OT - glycolysis OT - hematopoiesis OT - inflammation OT - macrophage OT - obesity COIS- Declaration of interests The authors declare no competing interests. EDAT- 2023/04/15 06:00 MHDA- 2023/10/04 06:43 PMCR- 2023/10/23 CRDT- 2023/04/14 12:36 PHST- 2022/12/12 00:00 [received] PHST- 2023/01/30 00:00 [revised] PHST- 2023/03/30 00:00 [accepted] PHST- 2023/10/04 06:43 [medline] PHST- 2023/04/15 06:00 [pubmed] PHST- 2023/04/14 12:36 [entrez] PHST- 2023/10/23 00:00 [pmc-release] AID - S2211-1247(23)00404-7 [pii] AID - 10.1016/j.celrep.2023.112393 [doi] PST - ppublish SO - Cell Rep. 2023 Apr 25;42(4):112393. doi: 10.1016/j.celrep.2023.112393. Epub 2023 Apr 13.