RNA sequencing of the human milk fat layer transcriptome reveals distinct gene expression profiles at three stages of lactation

Aware of the important benefits of human milk, most U.S. women initiate breastfeeding but difficulties with milk supply lead some to quit earlier than intended. Yet, the contribution of maternal physiology to lactation difficulties remains poorly understood. Human milk fat globules, by enveloping ce...

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Published inPloS one Vol. 8; no. 7; p. e67531
Main Authors Lemay, Danielle G, Ballard, Olivia A, Hughes, Maria A, Morrow, Ardythe L, Horseman, Nelson D, Nommsen-Rivers, Laurie A
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 05.07.2013
Public Library of Science (PLoS)
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Abstract Aware of the important benefits of human milk, most U.S. women initiate breastfeeding but difficulties with milk supply lead some to quit earlier than intended. Yet, the contribution of maternal physiology to lactation difficulties remains poorly understood. Human milk fat globules, by enveloping cell contents during their secretion into milk, are a rich source of mammary cell RNA. Here, we pair this non-invasive mRNA source with RNA-sequencing to probe the milk fat layer transcriptome during three stages of lactation: colostral, transitional, and mature milk production. The resulting transcriptomes paint an exquisite portrait of human lactation. The resulting transcriptional profiles cluster not by postpartum day, but by milk Na:K ratio, indicating that women sampled during similar postpartum time frames could be at markedly different stages of gene expression. Each stage of lactation is characterized by a dynamic range (10(5)-fold) in transcript abundances not previously observed with microarray technology. We discovered that transcripts for isoferritins and cathepsins are strikingly abundant during colostrum production, highlighting the potential importance of these proteins for neonatal health. Two transcripts, encoding β-casein (CSN2) and α-lactalbumin (LALBA), make up 45% of the total pool of mRNA in mature lactation. Genes significantly expressed across all stages of lactation are associated with making, modifying, transporting, and packaging milk proteins. Stage-specific transcripts are associated with immune defense during the colostral stage, up-regulation of the machinery needed for milk protein synthesis during the transitional stage, and the production of lipids during mature lactation. We observed strong modulation of key genes involved in lactose synthesis and insulin signaling. In particular, protein tyrosine phosphatase, receptor type, F (PTPRF) may serve as a biomarker linking insulin resistance with insufficient milk supply. This study provides the methodology and reference data set to enable future targeted research on the physiological contributors of sub-optimal lactation in humans.
AbstractList Aware of the important benefits of human milk, most U.S. women initiate breastfeeding but difficulties with milk supply lead some to quit earlier than intended. Yet, the contribution of maternal physiology to lactation difficulties remains poorly understood. Human milk fat globules, by enveloping cell contents during their secretion into milk, are a rich source of mammary cell RNA. Here, we pair this non-invasive mRNA source with RNA-sequencing to probe the milk fat layer transcriptome during three stages of lactation: colostral, transitional, and mature milk production. The resulting transcriptomes paint an exquisite portrait of human lactation. The resulting transcriptional profiles cluster not by postpartum day, but by milk Na:K ratio, indicating that women sampled during similar postpartum time frames could be at markedly different stages of gene expression. Each stage of lactation is characterized by a dynamic range (10 5 -fold) in transcript abundances not previously observed with microarray technology. We discovered that transcripts for isoferritins and cathepsins are strikingly abundant during colostrum production, highlighting the potential importance of these proteins for neonatal health. Two transcripts, encoding β-casein (CSN2) and α-lactalbumin (LALBA), make up 45% of the total pool of mRNA in mature lactation. Genes significantly expressed across all stages of lactation are associated with making, modifying, transporting, and packaging milk proteins. Stage-specific transcripts are associated with immune defense during the colostral stage, up-regulation of the machinery needed for milk protein synthesis during the transitional stage, and the production of lipids during mature lactation. We observed strong modulation of key genes involved in lactose synthesis and insulin signaling. In particular, protein tyrosine phosphatase, receptor type, F (PTPRF) may serve as a biomarker linking insulin resistance with insufficient milk supply. This study provides the methodology and reference data set to enable future targeted research on the physiological contributors of sub-optimal lactation in humans.
Aware of the important benefits of human milk, most U.S. women initiate breastfeeding but difficulties with milk supply lead some to quit earlier than intended. Yet, the contribution of maternal physiology to lactation difficulties remains poorly understood. Human milk fat globules, by enveloping cell contents during their secretion into milk, are a rich source of mammary cell RNA. Here, we pair this non-invasive mRNA source with RNA-sequencing to probe the milk fat layer transcriptome during three stages of lactation: colostral, transitional, and mature milk production. The resulting transcriptomes paint an exquisite portrait of human lactation. The resulting transcriptional profiles cluster not by postpartum day, but by milk Na:K ratio, indicating that women sampled during similar postpartum time frames could be at markedly different stages of gene expression. Each stage of lactation is characterized by a dynamic range (10.sup.5 -fold) in transcript abundances not previously observed with microarray technology. We discovered that transcripts for isoferritins and cathepsins are strikingly abundant during colostrum production, highlighting the potential importance of these proteins for neonatal health. Two transcripts, encoding [beta]-casein (CSN2) and [alpha]-lactalbumin (LALBA), make up 45% of the total pool of mRNA in mature lactation. Genes significantly expressed across all stages of lactation are associated with making, modifying, transporting, and packaging milk proteins. Stage-specific transcripts are associated with immune defense during the colostral stage, up-regulation of the machinery needed for milk protein synthesis during the transitional stage, and the production of lipids during mature lactation. We observed strong modulation of key genes involved in lactose synthesis and insulin signaling. In particular, protein tyrosine phosphatase, receptor type, F (PTPRF) may serve as a biomarker linking insulin resistance with insufficient milk supply. This study provides the methodology and reference data set to enable future targeted research on the physiological contributors of sub-optimal lactation in humans.
Aware of the important benefits of human milk, most U.S. women initiate breastfeeding but difficulties with milk supply lead some to quit earlier than intended. Yet, the contribution of maternal physiology to lactation difficulties remains poorly understood. Human milk fat globules, by enveloping cell contents during their secretion into milk, are a rich source of mammary cell RNA. Here, we pair this non-invasive mRNA source with RNA-sequencing to probe the milk fat layer transcriptome during three stages of lactation: colostral, transitional, and mature milk production. The resulting transcriptomes paint an exquisite portrait of human lactation. The resulting transcriptional profiles cluster not by postpartum day, but by milk Na:K ratio, indicating that women sampled during similar postpartum time frames could be at markedly different stages of gene expression. Each stage of lactation is characterized by a dynamic range (105-fold) in transcript abundances not previously observed with microarray technology. We discovered that transcripts for isoferritins and cathepsins are strikingly abundant during colostrum production, highlighting the potential importance of these proteins for neonatal health. Two transcripts, encoding β-casein (CSN2) and α-lactalbumin (LALBA), make up 45% of the total pool of mRNA in mature lactation. Genes significantly expressed across all stages of lactation are associated with making, modifying, transporting, and packaging milk proteins. Stage-specific transcripts are associated with immune defense during the colostral stage, up-regulation of the machinery needed for milk protein synthesis during the transitional stage, and the production of lipids during mature lactation. We observed strong modulation of key genes involved in lactose synthesis and insulin signaling. In particular, protein tyrosine phosphatase, receptor type, F (PTPRF) may serve as a biomarker linking insulin resistance with insufficient milk supply. This study provides the methodology and reference data set to enable future targeted research on the physiological contributors of sub-optimal lactation in humans.
Aware of the important benefits of human milk, most U.S. women initiate breastfeeding but difficulties with milk supply lead some to quit earlier than intended. Yet, the contribution of maternal physiology to lactation difficulties remains poorly understood. Human milk fat globules, by enveloping cell contents during their secretion into milk, are a rich source of mammary cell RNA. Here, we pair this non-invasive mRNA source with RNA-sequencing to probe the milk fat layer transcriptome during three stages of lactation: colostral, transitional, and mature milk production. The resulting transcriptomes paint an exquisite portrait of human lactation. The resulting transcriptional profiles cluster not by postpartum day, but by milk Na:K ratio, indicating that women sampled during similar postpartum time frames could be at markedly different stages of gene expression. Each stage of lactation is characterized by a dynamic range (10(5)-fold) in transcript abundances not previously observed with microarray technology. We discovered that transcripts for isoferritins and cathepsins are strikingly abundant during colostrum production, highlighting the potential importance of these proteins for neonatal health. Two transcripts, encoding β-casein (CSN2) and α-lactalbumin (LALBA), make up 45% of the total pool of mRNA in mature lactation. Genes significantly expressed across all stages of lactation are associated with making, modifying, transporting, and packaging milk proteins. Stage-specific transcripts are associated with immune defense during the colostral stage, up-regulation of the machinery needed for milk protein synthesis during the transitional stage, and the production of lipids during mature lactation. We observed strong modulation of key genes involved in lactose synthesis and insulin signaling. In particular, protein tyrosine phosphatase, receptor type, F (PTPRF) may serve as a biomarker linking insulin resistance with insufficient milk supply. This study provides the methodology and reference data set to enable future targeted research on the physiological contributors of sub-optimal lactation in humans.
Audience Academic
Author Ballard, Olivia A
Morrow, Ardythe L
Hughes, Maria A
Nommsen-Rivers, Laurie A
Lemay, Danielle G
Horseman, Nelson D
AuthorAffiliation University of Arkansas for Medical Sciences, United States of America
3 College of Medicine, University of Cincinnati, Cincinnati, Ohio, United States of America
2 Department of Pediatrics, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio, United States of America
1 Genome Center, University of California Davis, Davis, California, United States of America
AuthorAffiliation_xml – name: 2 Department of Pediatrics, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio, United States of America
– name: University of Arkansas for Medical Sciences, United States of America
– name: 3 College of Medicine, University of Cincinnati, Cincinnati, Ohio, United States of America
– name: 1 Genome Center, University of California Davis, Davis, California, United States of America
Author_xml – sequence: 1
  givenname: Danielle G
  surname: Lemay
  fullname: Lemay, Danielle G
  organization: Genome Center, University of California Davis, Davis, California, USA
– sequence: 2
  givenname: Olivia A
  surname: Ballard
  fullname: Ballard, Olivia A
– sequence: 3
  givenname: Maria A
  surname: Hughes
  fullname: Hughes, Maria A
– sequence: 4
  givenname: Ardythe L
  surname: Morrow
  fullname: Morrow, Ardythe L
– sequence: 5
  givenname: Nelson D
  surname: Horseman
  fullname: Horseman, Nelson D
– sequence: 6
  givenname: Laurie A
  surname: Nommsen-Rivers
  fullname: Nommsen-Rivers, Laurie A
BackLink https://www.ncbi.nlm.nih.gov/pubmed/23861770$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright COPYRIGHT 2013 Public Library of Science
2013 Lemay et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
2013 Lemay et al 2013 Lemay et al
Copyright_xml – notice: COPYRIGHT 2013 Public Library of Science
– notice: 2013 Lemay et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
– notice: 2013 Lemay et al 2013 Lemay et al
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content type line 23
Conceived and designed the experiments: LAN-R ALM NDH. Performed the experiments: LAN-R OAB MAH. Analyzed the data: LAN-R DGL. Wrote the paper: DGL LAN-R. Development of the Bioinformatics analysis plan: DGL LAN-R. Bioinformatics analysis: DGL. qPCR experimental design: DGL NDH MAH LAN-R. Design and execution of the milk fat globule processing experiments and identification of intact cells within the milk fat layer: OAB ALM NDH LAN-R. Constructive feedback on each draft of the manuscript: OAB ALM MAH NDH.
Competing Interests: The authors have declared that no competing interests exist.
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Snippet Aware of the important benefits of human milk, most U.S. women initiate breastfeeding but difficulties with milk supply lead some to quit earlier than...
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SubjectTerms Adult
Bioindicators
Bioinformatics
Biology
Biomarkers
Biosynthetic Pathways
Breast feeding
Breast milk
Breastfeeding & lactation
Casein
Cathepsins
Cluster Analysis
Colostrum
DNA microarrays
Female
Gene expression
Gene Expression Profiling
Gene Expression Regulation
Gene Regulatory Networks
Gene sequencing
Genes
Genomes
Genomics
Globules
Hospitals
Humans
Immune system
Insulin
Insulin - metabolism
Insulin resistance
Insulin Resistance - genetics
Lactalbumin
Lactation
Lactation - genetics
Lactation - metabolism
Lactose
Lactose - biosynthesis
Lipids
Medicine
Messenger RNA
Milk
Milk fat globule membranes
Milk production
Milk, Human
Neonates
Oils & fats
Packaging
Pediatrics
Physiology
Postpartum
Pregnancy
Protein biosynthesis
Protein synthesis
Protein-tyrosine-phosphatase
Proteins
Receptor-Like Protein Tyrosine Phosphatases, Class 2 - genetics
Reproducibility of Results
Ribonucleic acid
RNA
RNA probes
RNA sequencing
RNA, Messenger - genetics
Rodents
Signal Transduction
Signaling
Transcription
Transcriptome
Tyrosine
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Title RNA sequencing of the human milk fat layer transcriptome reveals distinct gene expression profiles at three stages of lactation
URI https://www.ncbi.nlm.nih.gov/pubmed/23861770
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http://dx.doi.org/10.1371/journal.pone.0067531
Volume 8
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