Uterine Immunity and Microbiota: A Shifting Paradigm

The female reproductive tract harbors distinct microbial communities, as in the vagina, cervical canal, uterus, and fallopian tubes. The nature of the vaginal microbiota is well-known; in contrast, the upper reproductive tract remains largely unexplored. Alteration in the uterine microbiota, which i...

Full description

Saved in:
Bibliographic Details
Published inFrontiers in immunology Vol. 10; p. 2387
Main Authors Agostinis, Chiara, Mangogna, Alessandro, Bossi, Fleur, Ricci, Giuseppe, Kishore, Uday, Bulla, Roberta
Format Journal Article
LanguageEnglish
Published Switzerland Frontiers Media S.A 17.10.2019
Subjects
Online AccessGet full text
ISSN1664-3224
1664-3224
DOI10.3389/fimmu.2019.02387

Cover

Abstract The female reproductive tract harbors distinct microbial communities, as in the vagina, cervical canal, uterus, and fallopian tubes. The nature of the vaginal microbiota is well-known; in contrast, the upper reproductive tract remains largely unexplored. Alteration in the uterine microbiota, which is dependent on the nutrients and hormones available to the uterus, is likely to play an important role in uterine-related diseases such as hysteromyoma, adenomyosis, and endometriosis. Uterine mucosa is an important tissue barrier whose main function is to offer protection against pathogens and other toxic factors, while maintaining a symbiotic relationship with commensal microbes. These characteristics are shared by all the mucosal tissues; however, the uterine mucosa is unique since it changes cyclically during the menstrual cycle as well as pregnancy. The immune system, besides its role in the defense process, plays crucial roles in reproduction as it ensures local immune tolerance to fetal/paternal antigens, trophoblast invasion, and vascular remodeling. The human endometrium contains a conspicuous number of immune cells, mainly Natural Killers (NK) cells, which are phenotypically distinct from peripheral cytotoxic NK, cells and macrophages. The endometrium also contains few lymphoid aggregates comprising B cell and CD8 T cells. The number and the phenotype of these cells change during the menstrual cycle. It has become evident in recent years that the immune cell phenotype and function can be influenced by microbiota. Immune cells can sense the presence of microbes through their pattern recognition receptors, setting up host-microbe interaction. The microbiota exerts an appropriately controlled defense mechanism by competing for nutrients and mucosal space with pathogens. It has recently been considered that uterus is a non-sterile compartment since it seems to possess its own microbiota. There has been an increasing interest in characterizing the nature of microbial colonization within the uterus and its apparent impact on fertility and pregnancy. This review will examine the potential relationship between the uterine microbiota and the immune cells present in the local environment.
AbstractList The female reproductive tract harbors distinct microbial communities, as in the vagina, cervical canal, uterus, and fallopian tubes. The nature of the vaginal microbiota is well-known; in contrast, the upper reproductive tract remains largely unexplored. Alteration in the uterine microbiota, which is dependent on the nutrients and hormones available to the uterus, is likely to play an important role in uterine-related diseases such as hysteromyoma, adenomyosis, and endometriosis. Uterine mucosa is an important tissue barrier whose main function is to offer protection against pathogens and other toxic factors, while maintaining a symbiotic relationship with commensal microbes. These characteristics are shared by all the mucosal tissues; however, the uterine mucosa is unique since it changes cyclically during the menstrual cycle as well as pregnancy. The immune system, besides its role in the defense process, plays crucial roles in reproduction as it ensures local immune tolerance to fetal/paternal antigens, trophoblast invasion, and vascular remodeling. The human endometrium contains a conspicuous number of immune cells, mainly Natural Killers (NK) cells, which are phenotypically distinct from peripheral cytotoxic NK, cells and macrophages. The endometrium also contains few lymphoid aggregates comprising B cell and CD8 T cells. The number and the phenotype of these cells change during the menstrual cycle. It has become evident in recent years that the immune cell phenotype and function can be influenced by microbiota. Immune cells can sense the presence of microbes through their pattern recognition receptors, setting up host-microbe interaction. The microbiota exerts an appropriately controlled defense mechanism by competing for nutrients and mucosal space with pathogens. It has recently been considered that uterus is a non-sterile compartment since it seems to possess its own microbiota. There has been an increasing interest in characterizing the nature of microbial colonization within the uterus and its apparent impact on fertility and pregnancy. This review will examine the potential relationship between the uterine microbiota and the immune cells present in the local environment.
The female reproductive tract harbors distinct microbial communities, as in the vagina, cervical canal, uterus, and fallopian tubes. The nature of the vaginal microbiota is well-known; in contrast, the upper reproductive tract remains largely unexplored. Alteration in the uterine microbiota, which is dependent on the nutrients and hormones available to the uterus, is likely to play an important role in uterine-related diseases such as hysteromyoma, adenomyosis, and endometriosis. Uterine mucosa is an important tissue barrier whose main function is to offer protection against pathogens and other toxic factors, while maintaining a symbiotic relationship with commensal microbes. These characteristics are shared by all the mucosal tissues; however, the uterine mucosa is unique since it changes cyclically during the menstrual cycle as well as pregnancy. The immune system, besides its role in the defense process, plays crucial roles in reproduction as it ensures local immune tolerance to fetal/paternal antigens, trophoblast invasion, and vascular remodeling. The human endometrium contains a conspicuous number of immune cells, mainly Natural Killers (NK) cells, which are phenotypically distinct from peripheral cytotoxic NK, cells and macrophages. The endometrium also contains few lymphoid aggregates comprising B cell and CD8 + T cells. The number and the phenotype of these cells change during the menstrual cycle. It has become evident in recent years that the immune cell phenotype and function can be influenced by microbiota. Immune cells can sense the presence of microbes through their pattern recognition receptors, setting up host-microbe interaction. The microbiota exerts an appropriately controlled defense mechanism by competing for nutrients and mucosal space with pathogens. It has recently been considered that uterus is a non-sterile compartment since it seems to possess its own microbiota. There has been an increasing interest in characterizing the nature of microbial colonization within the uterus and its apparent impact on fertility and pregnancy. This review will examine the potential relationship between the uterine microbiota and the immune cells present in the local environment.
The female reproductive tract harbors distinct microbial communities, as in the vagina, cervical canal, uterus, and fallopian tubes. The nature of the vaginal microbiota is well-known; in contrast, the upper reproductive tract remains largely unexplored. Alteration in the uterine microbiota, which is dependent on the nutrients and hormones available to the uterus, is likely to play an important role in uterine-related diseases such as hysteromyoma, adenomyosis, and endometriosis. Uterine mucosa is an important tissue barrier whose main function is to offer protection against pathogens and other toxic factors, while maintaining a symbiotic relationship with commensal microbes. These characteristics are shared by all the mucosal tissues; however, the uterine mucosa is unique since it changes cyclically during the menstrual cycle as well as pregnancy. The immune system, besides its role in the defense process, plays crucial roles in reproduction as it ensures local immune tolerance to fetal/paternal antigens, trophoblast invasion, and vascular remodeling. The human endometrium contains a conspicuous number of immune cells, mainly Natural Killers (NK) cells, which are phenotypically distinct from peripheral cytotoxic NK, cells and macrophages. The endometrium also contains few lymphoid aggregates comprising B cell and CD8+ T cells. The number and the phenotype of these cells change during the menstrual cycle. It has become evident in recent years that the immune cell phenotype and function can be influenced by microbiota. Immune cells can sense the presence of microbes through their pattern recognition receptors, setting up host-microbe interaction. The microbiota exerts an appropriately controlled defense mechanism by competing for nutrients and mucosal space with pathogens. It has recently been considered that uterus is a non-sterile compartment since it seems to possess its own microbiota. There has been an increasing interest in characterizing the nature of microbial colonization within the uterus and its apparent impact on fertility and pregnancy. This review will examine the potential relationship between the uterine microbiota and the immune cells present in the local environment.The female reproductive tract harbors distinct microbial communities, as in the vagina, cervical canal, uterus, and fallopian tubes. The nature of the vaginal microbiota is well-known; in contrast, the upper reproductive tract remains largely unexplored. Alteration in the uterine microbiota, which is dependent on the nutrients and hormones available to the uterus, is likely to play an important role in uterine-related diseases such as hysteromyoma, adenomyosis, and endometriosis. Uterine mucosa is an important tissue barrier whose main function is to offer protection against pathogens and other toxic factors, while maintaining a symbiotic relationship with commensal microbes. These characteristics are shared by all the mucosal tissues; however, the uterine mucosa is unique since it changes cyclically during the menstrual cycle as well as pregnancy. The immune system, besides its role in the defense process, plays crucial roles in reproduction as it ensures local immune tolerance to fetal/paternal antigens, trophoblast invasion, and vascular remodeling. The human endometrium contains a conspicuous number of immune cells, mainly Natural Killers (NK) cells, which are phenotypically distinct from peripheral cytotoxic NK, cells and macrophages. The endometrium also contains few lymphoid aggregates comprising B cell and CD8+ T cells. The number and the phenotype of these cells change during the menstrual cycle. It has become evident in recent years that the immune cell phenotype and function can be influenced by microbiota. Immune cells can sense the presence of microbes through their pattern recognition receptors, setting up host-microbe interaction. The microbiota exerts an appropriately controlled defense mechanism by competing for nutrients and mucosal space with pathogens. It has recently been considered that uterus is a non-sterile compartment since it seems to possess its own microbiota. There has been an increasing interest in characterizing the nature of microbial colonization within the uterus and its apparent impact on fertility and pregnancy. This review will examine the potential relationship between the uterine microbiota and the immune cells present in the local environment.
The female reproductive tract harbors distinct microbial communities, as in the vagina, cervical canal, uterus, and fallopian tubes. The nature of the vaginal microbiota is well-known; in contrast, the upper reproductive tract remains largely unexplored. Alteration in the uterine microbiota, which is dependent on the nutrients and hormones available to the uterus, is likely to play an important role in uterine-related diseases such as hysteromyoma, adenomyosis, and endometriosis. Uterine mucosa is an important tissue barrier whose main function is to offer protection against pathogens and other toxic factors, while maintaining a symbiotic relationship with commensal microbes. These characteristics are shared by all the mucosal tissues; however, the uterine mucosa is unique since it changes cyclically during the menstrual cycle as well as pregnancy. The immune system, besides its role in the defense process, plays crucial roles in reproduction as it ensures local immune tolerance to fetal/paternal antigens, trophoblast invasion, and vascular remodeling. The human endometrium contains a conspicuous number of immune cells, mainly Natural Killers (NK) cells, which are phenotypically distinct from peripheral cytotoxic NK, cells and macrophages. The endometrium also contains few lymphoid aggregates comprising B cell and CD8+ T cells. The number and the phenotype of these cells change during the menstrual cycle. It has become evident in recent years that the immune cell phenotype and function can be influenced by microbiota. Immune cells can sense the presence of microbes through their pattern recognition receptors, setting up host-microbe interaction. The microbiota exerts an appropriately controlled defense mechanism by competing for nutrients and mucosal space with pathogens. It has recently been considered that uterus is a non-sterile compartment since it seems to possess its own microbiota. There has been an increasing interest in characterizing the nature of microbial colonization within the uterus and its apparent impact on fertility and pregnancy. This review will examine the potential relationship between the uterine microbiota and the immune cells present in the local environment.
Author Bulla, Roberta
Ricci, Giuseppe
Kishore, Uday
Bossi, Fleur
Mangogna, Alessandro
Agostinis, Chiara
AuthorAffiliation 3 Department of Medical, Surgical and Health Science, University of Trieste , Trieste , Italy
1 Institute for Maternal and Child Health, IRCCS (Istituto di Ricovero e Cura a Carattere Scientifico) Burlo Garofolo , Trieste , Italy
4 Biosciences, College of Health and Life Sciences, Brunel University London , Uxbridge , United Kingdom
2 Department of Life Sciences, University of Trieste , Trieste , Italy
AuthorAffiliation_xml – name: 1 Institute for Maternal and Child Health, IRCCS (Istituto di Ricovero e Cura a Carattere Scientifico) Burlo Garofolo , Trieste , Italy
– name: 4 Biosciences, College of Health and Life Sciences, Brunel University London , Uxbridge , United Kingdom
– name: 2 Department of Life Sciences, University of Trieste , Trieste , Italy
– name: 3 Department of Medical, Surgical and Health Science, University of Trieste , Trieste , Italy
Author_xml – sequence: 1
  givenname: Chiara
  surname: Agostinis
  fullname: Agostinis, Chiara
– sequence: 2
  givenname: Alessandro
  surname: Mangogna
  fullname: Mangogna, Alessandro
– sequence: 3
  givenname: Fleur
  surname: Bossi
  fullname: Bossi, Fleur
– sequence: 4
  givenname: Giuseppe
  surname: Ricci
  fullname: Ricci, Giuseppe
– sequence: 5
  givenname: Uday
  surname: Kishore
  fullname: Kishore, Uday
– sequence: 6
  givenname: Roberta
  surname: Bulla
  fullname: Bulla, Roberta
BackLink https://www.ncbi.nlm.nih.gov/pubmed/31681281$$D View this record in MEDLINE/PubMed
BookMark eNp1kc1r3DAQxUVJadI0956Kj73sVtLI8riHQgj9WEhoIOlZyNZoo2BLqawt5L-vdzcNSSG6SIze_GZ47y07iCkSY-8FXwJg-8mHcdwsJRftkkvA5hU7ElqrBUipDp68D9nJNN3y-agWAOo37BCERiFRHDH1q1AOkarVDIuh3Fc2uuoi9Dl1IRX7uTqtrm6CLyGuq0ubrQvr8R177e0w0cnDfcyuv329PvuxOP_5fXV2er7oa4ll4S2RkgoVAhGqhpzmHFH3jjQ5Dpa8bUG5pnMtknC640haC9FID1TDMVvtsS7ZW3OXw2jzvUk2mF0h5bWxuYR-INMRAu-85xo7BUhINWqplKyhaetGz6wve9bdphvJ9RRLtsMz6POfGG7MOv0xs1GiFjgDPj4Acvq9oamYMUw9DYONlDaTkSBEK1VTb_f-8HTW45B_rs8CvhfMLk9TJv8oEdxsszW7bM02W7PLdm7R_7X0odgS0nbbMLzc-BcmHqi5
CitedBy_id crossref_primary_10_1111_aji_13798
crossref_primary_10_5937_arhfarm74_46612
crossref_primary_10_17116_repro20202606115
crossref_primary_10_1002_ijgo_15357
crossref_primary_10_1089_ten_teb_2021_0062
crossref_primary_10_3389_fphys_2022_1050690
crossref_primary_10_4081_reumatismo_2024_1764
crossref_primary_10_1016_j_jri_2022_103494
crossref_primary_10_1186_s12934_025_02662_8
crossref_primary_10_3390_agriculture10060232
crossref_primary_10_1016_j_compbiolchem_2024_108216
crossref_primary_10_3390_biology13030150
crossref_primary_10_1093_humrep_deaa372
crossref_primary_10_15407_microbiolj85_03_032
crossref_primary_10_1016_j_jvacx_2024_100501
crossref_primary_10_3390_ijms242015233
crossref_primary_10_1111_brv_13145
crossref_primary_10_1152_physrev_00050_2021
crossref_primary_10_3389_fcimb_2021_790627
crossref_primary_10_3390_life13122269
crossref_primary_10_1016_j_jri_2023_103925
crossref_primary_10_17116_rosakush20232302153
crossref_primary_10_3389_fimmu_2022_928475
crossref_primary_10_1007_s41974_022_00219_w
crossref_primary_10_1038_s41598_020_65299_0
crossref_primary_10_3390_ijerph20043762
crossref_primary_10_3390_antibiotics11101331
crossref_primary_10_3390_ani13040554
crossref_primary_10_3389_fcimb_2022_767693
crossref_primary_10_1016_j_jbc_2022_101874
crossref_primary_10_17116_rosakush20252501125
crossref_primary_10_1016_j_placenta_2023_10_002
crossref_primary_10_3390_nu15153359
crossref_primary_10_1186_s43043_025_00214_z
crossref_primary_10_3389_fcimb_2020_609488
crossref_primary_10_12677_jcpm_2024_32084
crossref_primary_10_1097_GCO_0000000000000709
crossref_primary_10_1016_j_jri_2024_104325
crossref_primary_10_17816_JOWD88921
crossref_primary_10_21886_2219_8075_2023_14_3_5_15
crossref_primary_10_33549_physiolres_935036
crossref_primary_10_1186_s12967_023_04113_7
crossref_primary_10_3389_fmicb_2022_864720
crossref_primary_10_3390_ijms232416019
crossref_primary_10_1186_s12916_024_03500_1
crossref_primary_10_1016_j_fsigen_2023_102978
crossref_primary_10_1093_humupd_dmad013
crossref_primary_10_1093_humrep_dead194
crossref_primary_10_1186_s12905_023_02697_2
crossref_primary_10_1155_2021_8844346
crossref_primary_10_1016_j_yhbeh_2023_105411
crossref_primary_10_3892_br_2023_1626
crossref_primary_10_1007_s10787_022_01032_9
crossref_primary_10_3389_fmicb_2022_998813
crossref_primary_10_1038_s41598_022_12095_7
crossref_primary_10_1016_j_intimp_2023_110023
crossref_primary_10_3389_fimmu_2023_1169232
crossref_primary_10_3390_diagnostics13091557
crossref_primary_10_31083_j_ceog5005093
crossref_primary_10_1071_RD24162
crossref_primary_10_1111_apm_13288
crossref_primary_10_3390_biom10040593
crossref_primary_10_1007_s42977_022_00134_3
crossref_primary_10_3390_futurepharmacol2040039
crossref_primary_10_1016_j_jri_2023_103973
crossref_primary_10_3390_ani14223337
crossref_primary_10_62486_agsalud2025187
crossref_primary_10_15789_2220_7619_IBE_17808
crossref_primary_10_1016_j_lfs_2025_123427
crossref_primary_10_3389_fcimb_2022_884272
crossref_primary_10_1016_j_toxlet_2020_11_008
crossref_primary_10_3390_medicina60121920
crossref_primary_10_3390_ijms24032995
crossref_primary_10_1016_j_psj_2022_102008
crossref_primary_10_3389_fcell_2021_693267
crossref_primary_10_3389_fcimb_2022_814668
crossref_primary_10_3390_jpm11060546
crossref_primary_10_3390_biomedicines12122801
crossref_primary_10_1111_aji_70022
crossref_primary_10_21518_2079_701X_2020_3_17_23
crossref_primary_10_3390_diagnostics11081434
crossref_primary_10_3390_life12111867
crossref_primary_10_1128_JVI_00417_21
crossref_primary_10_1016_j_repbio_2023_100852
crossref_primary_10_17116_repro202228061159
crossref_primary_10_1007_s12088_023_01062_z
crossref_primary_10_1186_s12866_024_03379_1
crossref_primary_10_1016_j_plefa_2024_102619
crossref_primary_10_1186_s12917_023_03845_4
crossref_primary_10_3390_ijms25063362
crossref_primary_10_1055_s_0043_1778017
crossref_primary_10_17116_rosakush20222202171
crossref_primary_10_3390_ijms242115896
crossref_primary_10_1016_j_ecoenv_2023_114711
crossref_primary_10_1016_j_addr_2021_113955
crossref_primary_10_3390_microorganisms12081647
crossref_primary_10_3390_microorganisms12081641
crossref_primary_10_5327_DST_2177_8264_201931406
crossref_primary_10_1097_GCO_0000000000000627
crossref_primary_10_1093_humrep_deae190
crossref_primary_10_1111_aji_70019
crossref_primary_10_1016_j_molmed_2022_04_006
crossref_primary_10_3390_vetsci11070324
crossref_primary_10_33073_pjm_2021_043
crossref_primary_10_3389_fimmu_2022_857299
crossref_primary_10_1210_clinem_dgaa951
crossref_primary_10_3389_fendo_2024_1365602
crossref_primary_10_1111_aji_13384
crossref_primary_10_3390_pharmaceutics16111475
crossref_primary_10_1186_s13244_024_01708_6
crossref_primary_10_3389_fimmu_2022_984356
crossref_primary_10_3389_fimmu_2023_1110001
crossref_primary_10_3389_fimmu_2021_758281
crossref_primary_10_3390_microorganisms12030547
crossref_primary_10_12717_DR_2022_26_4_135
crossref_primary_10_11603_1681_2727_2023_4_14163
crossref_primary_10_3389_fnut_2023_1166929
crossref_primary_10_3390_vetsci10060370
crossref_primary_10_1155_2024_5582151
crossref_primary_10_3389_fonc_2022_975201
crossref_primary_10_1128_spectrum_02732_23
Cites_doi 10.1016/S0165-0378(02)00011-6
10.1093/humupd/6.1.28
10.1002/jnr.20881
10.1038/nrmicro2538
10.1016/j.it.2018.01.007
10.1016/j.immuni.2017.04.008
10.1016/j.immuni.2013.02.010
10.1155/2014/248963
10.3389/fimmu.2018.02396
10.1016/j.immuni.2011.12.020
10.1111/aji.12252
10.1186/s13073-016-0368-y
10.1093/humupd/4.6.891
10.1016/j.coi.2018.08.003
10.1007/s00441-005-1127-3
10.3109/00016349509008942
10.1093/humrep/13.4.1036
10.4049/jimmunol.1602085
10.1038/srep36748
10.1111/j.1600-065X.2007.00551.x
10.1016/S0002-9378(16)34549-5
10.1084/jem.20051615
10.1111/j.1600-0897.2004.00237.x
10.1128/IAI.01049-16
10.3389/fimmu.2018.00208
10.1111/j.1365-2567.2006.02339.x
10.1093/humrep/13.1.44
10.1111/imcb.12273
10.1038/nri3819
10.1038/nri3365
10.1093/humrep/den030
10.1016/j.ajog.2015.05.032
10.1097/00006254-199505000-00026
10.1016/j.addr.2017.10.014
10.4110/in.2015.15.1.16
10.1016/S0165-0378(99)00002-9
10.1093/humupd/6.1.16
10.1096/fj.07-8189com
10.1111/aogs.12296
10.4049/jimmunol.1001637
10.1016/0165-0378(93)90025-D
10.1007/s10815-015-0614-z
10.1046/j.1365-2141.2001.03202.x
10.1016/j.cell.2018.07.017
10.1093/humupd/dmy012
10.1016/j.ajog.2016.09.075
10.1210/jc.2012-1102
10.1016/S0015-0282(16)38890-2
10.1371/journal.pone.0110152
10.4049/jimmunol.1401813
10.1002/jcp.21221
10.7717/peerj.1602
10.1093/humupd/4.5.702
10.1146/annurev-physiol-021115-105238
10.1038/ni.2604
10.1038/ni.2131
10.1016/j.fertnstert.2018.04.041
10.4049/jimmunol.160.10.5145
10.3389/fimmu.2018.01874
10.1073/pnas.0611098104
10.1016/0020-7292(92)90974-N
10.1111/j.8755-8920.2000.430405.x
10.1046/j.1365-2567.2001.01199.x
10.1038/s41467-017-00901-0
10.3389/fimmu.2015.00646
10.4049/jimmunol.1500689
10.1006/cimm.1997.1199
10.4049/jimmunol.149.9.2872
10.1016/S0002-9378(11)90589-4
10.1038/372190a0
10.1095/biolreprod53.2.312
10.4049/jimmunol.0904192
10.1111/aji.12198
10.1016/j.ajog.2014.11.043
10.1189/jlb.0712327
ContentType Journal Article
Copyright Copyright © 2019 Agostinis, Mangogna, Bossi, Ricci, Kishore and Bulla.
Copyright © 2019 Agostinis, Mangogna, Bossi, Ricci, Kishore and Bulla. 2019 Agostinis, Mangogna, Bossi, Ricci, Kishore and Bulla
Copyright_xml – notice: Copyright © 2019 Agostinis, Mangogna, Bossi, Ricci, Kishore and Bulla.
– notice: Copyright © 2019 Agostinis, Mangogna, Bossi, Ricci, Kishore and Bulla. 2019 Agostinis, Mangogna, Bossi, Ricci, Kishore and Bulla
DBID AAYXX
CITATION
NPM
7X8
5PM
DOA
DOI 10.3389/fimmu.2019.02387
DatabaseName CrossRef
PubMed
MEDLINE - Academic
PubMed Central (Full Participant titles)
DOAJ Directory of Open Access Journals
DatabaseTitle CrossRef
PubMed
MEDLINE - Academic
DatabaseTitleList PubMed

MEDLINE - Academic

Database_xml – sequence: 1
  dbid: DOA
  name: DOAJ Directory of Open Access Journals
  url: https://www.doaj.org/
  sourceTypes: Open Website
– sequence: 2
  dbid: NPM
  name: PubMed
  url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
DeliveryMethod fulltext_linktorsrc
Discipline Biology
EISSN 1664-3224
ExternalDocumentID oai_doaj_org_article_be830bff068b438e8e58624425379576
PMC6811518
31681281
10_3389_fimmu_2019_02387
Genre Research Support, Non-U.S. Gov't
Journal Article
Review
GroupedDBID 53G
5VS
9T4
AAFWJ
AAKDD
AAYXX
ACGFO
ACGFS
ACXDI
ADBBV
ADRAZ
AENEX
AFPKN
ALMA_UNASSIGNED_HOLDINGS
AOIJS
BAWUL
BCNDV
CITATION
DIK
EBS
EMOBN
GROUPED_DOAJ
GX1
HYE
KQ8
M48
M~E
OK1
PGMZT
RNS
RPM
IPNFZ
NPM
RIG
7X8
5PM
ID FETCH-LOGICAL-c528t-faee4248483ee847ed600886cde6ed03aefa934d7bd98e1d6b08e661172f3e53
IEDL.DBID M48
ISSN 1664-3224
IngestDate Wed Aug 27 01:24:18 EDT 2025
Thu Aug 21 18:40:45 EDT 2025
Thu Sep 04 22:45:00 EDT 2025
Thu Apr 03 07:03:02 EDT 2025
Tue Jul 01 00:39:48 EDT 2025
Thu Apr 24 23:03:33 EDT 2025
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Keywords microbiota
immune cells
uterus
cellular immunity
menstruation
pregnancy
Language English
License Copyright © 2019 Agostinis, Mangogna, Bossi, Ricci, Kishore and Bulla.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c528t-faee4248483ee847ed600886cde6ed03aefa934d7bd98e1d6b08e661172f3e53
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
ObjectType-Review-3
content type line 23
This article was submitted to Mucosal Immunity, a section of the journal Frontiers in Immunology
Edited by: Nicoletta Disimone, Agostino Gemelli University Polyclinic, Italy
Reviewed by: Gerard Chaouat, INSERM U976 Immunologie, Dermatologie, Oncologie, France; Julia Szekeres-Bartho, University of Pécs, Hungary
OpenAccessLink http://journals.scholarsportal.info/openUrl.xqy?doi=10.3389/fimmu.2019.02387
PMID 31681281
PQID 2311924755
PQPubID 23479
ParticipantIDs doaj_primary_oai_doaj_org_article_be830bff068b438e8e58624425379576
pubmedcentral_primary_oai_pubmedcentral_nih_gov_6811518
proquest_miscellaneous_2311924755
pubmed_primary_31681281
crossref_primary_10_3389_fimmu_2019_02387
crossref_citationtrail_10_3389_fimmu_2019_02387
ProviderPackageCode CITATION
AAYXX
PublicationCentury 2000
PublicationDate 2019-10-17
PublicationDateYYYYMMDD 2019-10-17
PublicationDate_xml – month: 10
  year: 2019
  text: 2019-10-17
  day: 17
PublicationDecade 2010
PublicationPlace Switzerland
PublicationPlace_xml – name: Switzerland
PublicationTitle Frontiers in immunology
PublicationTitleAlternate Front Immunol
PublicationYear 2019
Publisher Frontiers Media S.A
Publisher_xml – name: Frontiers Media S.A
References Jeziorska (B50) 1995; 53
Belkaid (B18) 2013; 14
Salamonsen (B41) 2000; 6
Heyborne (B59) 1992; 149
Wira (B12) 2014; 72
King (B39) 2000; 6
Bonatz (B67) 1992; 37
Kodama (B66) 1998; 13
Miller (B33) 2018; 9
Belkaid (B3) 2017; 46
Brubaker (B14) 2015; 213
Moller (B20) 1995; 74
Chen (B23) 2017; 8
Rami (B44) 2014; 2014
Salamonsen (B45) 1999; 44
Moghissi (B71) 1972; 23
Netter (B6) 2019
Cousins (B46) 2016; 6
Monticelli (B36) 2011; 12
Schnupf (B4) 2018; 54
Franasiak (B16) 2016; 33
Haddad (B49) 1997; 181
Halim (B35) 2012; 36
Fuchs (B31) 2013; 38
Wallach (B70) 1994
Ribatti (B51) 2001; 115
Robertson (B74) 2005; 322
Vivier (B28) 2018; 174
Bartemes (B37) 2018; 200
Vassiliadou (B61) 1998; 13
Wira (B5) 2015; 15
Flynn (B64) 2000; 43
Cepek (B32) 1994; 372
McGuckin (B2) 2011; 9
Trifonova (B11) 2014; 71
Doisne (B29) 2015; 195
Song (B43) 1995; 50
Yeaman (B62) 2001; 102
Baker (B69) 2018; 9
Drake (B8) 2015
Fallon (B34) 2006; 203
Moreno (B77) 2018; 110
Schulke (B53) 2008; 23
Fahl (B57) 2014; 193
Montaldo (B30) 2015; 6
Salamonsen (B47) 2002; 57
Clark (B80) 2004; 52
Zhou (B1) 2018; 39
Hill (B60) 1992; 166
Lee (B26) 2010; 185
Jones (B65) 1998; 4
Taherali (B68) 2018; 124
Brunelli (B72) 2007; 21
Ansbacher (B19) 1967; 99
Prieto (B54) 2006; 118
Mitchell (B21) 2015; 212
Ueno (B52) 2007; 219
Altmae (B24) 2018; 9
Keck (B75) 1998; 4
Walther-Antonio (B78) 2016; 8
Carlino (B40) 2012; 97
Tai (B56) 2008; 214
Moreno (B22) 2016; 215
Male (B38) 2010; 185
Keskin (B63) 2007; 104
Benner (B25) 2018; 24
Hall (B9) 2016
Verstraelen (B15) 2016; 4
Thiruchelvam (B42) 2013; 93
Hansen (B73) 2014; 93
Polanczyk (B55) 2006; 84
Haller (B58) 1993; 23
Spits (B27) 2013; 13
Lee (B10) 2015; 15
Dickson (B13) 2016; 78
Weng (B76) 2014; 9
Standring (B7) 2016
McCoy (B79) 2019; 97
Laniewski (B17) 2017; 85
Yeaman (B48) 1998; 160
References_xml – volume: 57
  start-page: 95
  year: 2002
  ident: B47
  article-title: Leukocyte networks and human endometrial remodelling
  publication-title: J Reprod Immunol.
  doi: 10.1016/S0165-0378(02)00011-6
– volume: 6
  start-page: 28
  year: 2000
  ident: B39
  article-title: Uterine leukocytes and decidualization
  publication-title: Hum Reprod Update.
  doi: 10.1093/humupd/6.1.28
– volume: 84
  start-page: 370
  year: 2006
  ident: B55
  article-title: Estrogen-mediated immunomodulation involves reduced activation of effector T cells, potentiation of Treg cells, and enhanced expression of the PD-1 costimulatory pathway
  publication-title: J Neurosci Res.
  doi: 10.1002/jnr.20881
– volume: 9
  start-page: 265
  year: 2011
  ident: B2
  article-title: Mucin dynamics and enteric pathogens
  publication-title: Nat Rev Microbiol.
  doi: 10.1038/nrmicro2538
– volume: 39
  start-page: 302
  year: 2018
  ident: B1
  article-title: Immunology of uterine and vaginal mucosae
  publication-title: Trends Immunol.
  doi: 10.1016/j.it.2018.01.007
– volume: 46
  start-page: 562
  year: 2017
  ident: B3
  article-title: Homeostatic immunity and the microbiota
  publication-title: Immunity.
  doi: 10.1016/j.immuni.2017.04.008
– volume: 38
  start-page: 769
  year: 2013
  ident: B31
  article-title: Intraepithelial type 1 innate lymphoid cells are a unique subset of IL-12- and IL-15-responsive IFN-gamma-producing cells
  publication-title: Immunity.
  doi: 10.1016/j.immuni.2013.02.010
– volume: 2014
  start-page: 248963
  year: 2014
  ident: B44
  article-title: The first trimester gravid serum regulates procalcitonin expression in human macrophages skewing their phenotype in vitro
  publication-title: Mediators Inflamm.
  doi: 10.1155/2014/248963
– volume: 9
  start-page: 2396
  year: 2018
  ident: B33
  article-title: Innate lymphoid cells in the maternal and fetal compartments
  publication-title: Front Immunol.
  doi: 10.3389/fimmu.2018.02396
– volume: 36
  start-page: 451
  year: 2012
  ident: B35
  article-title: Lung natural helper cells are a critical source of Th2 cell-type cytokines in protease allergen-induced airway inflammation
  publication-title: Immunity.
  doi: 10.1016/j.immuni.2011.12.020
– volume: 72
  start-page: 236
  year: 2014
  ident: B12
  article-title: Regulation of mucosal immunity in the female reproductive tract: the role of sex hormones in immune protection against sexually transmitted pathogens
  publication-title: Am J Reprod Immunol.
  doi: 10.1111/aji.12252
– volume: 8
  start-page: 122
  year: 2016
  ident: B78
  article-title: Potential contribution of the uterine microbiome in the development of endometrial cancer
  publication-title: Genome Med.
  doi: 10.1186/s13073-016-0368-y
– volume: 4
  start-page: 891
  year: 1998
  ident: B75
  article-title: Seminal tract infections: impact on male fertility and treatment options
  publication-title: Hum Reprod Update.
  doi: 10.1093/humupd/4.6.891
– volume: 54
  start-page: 137
  year: 2018
  ident: B4
  article-title: Modulation of the gut microbiota to improve innate resistance
  publication-title: Curr Opin Immunol.
  doi: 10.1016/j.coi.2018.08.003
– volume: 322
  start-page: 43
  year: 2005
  ident: B74
  article-title: Seminal plasma and male factor signalling in the female reproductive tract
  publication-title: Cell Tissue Res.
  doi: 10.1007/s00441-005-1127-3
– volume: 74
  start-page: 216
  year: 1995
  ident: B20
  article-title: Sterility of the uterine cavity
  publication-title: Acta Obstet Gynecol Scand.
  doi: 10.3109/00016349509008942
– volume: 13
  start-page: 1036
  year: 1998
  ident: B66
  article-title: Characteristic changes of large granular lymphocytes that strongly express CD56 in endometrium during the menstrual cycle and early pregnancy
  publication-title: Hum Reprod.
  doi: 10.1093/humrep/13.4.1036
– volume: 200
  start-page: 229
  year: 2018
  ident: B37
  article-title: IL-33-responsive group 2 innate lymphoid cells are regulated by female sex hormones in the uterus
  publication-title: J Immunol.
  doi: 10.4049/jimmunol.1602085
– volume: 6
  start-page: 36748
  year: 2016
  ident: B46
  article-title: Evidence for a dynamic role for mononuclear phagocytes during endometrial repair and remodelling
  publication-title: Sci Rep.
  doi: 10.1038/srep36748
– volume: 219
  start-page: 118
  year: 2007
  ident: B52
  article-title: Dendritic cell subsets in health and disease
  publication-title: Immunol Rev.
  doi: 10.1111/j.1600-065X.2007.00551.x
– start-page: xvi
  volume-title: Gray's Atlas of Anatomy
  year: 2015
  ident: B8
– volume: 99
  start-page: 394
  year: 1967
  ident: B19
  article-title: Sterility of the uterine cavity
  publication-title: Am J Obstet Gynecol.
  doi: 10.1016/S0002-9378(16)34549-5
– volume: 203
  start-page: 1105
  year: 2006
  ident: B34
  article-title: Identification of an interleukin (IL)-25-dependent cell population that provides IL-4, IL-5, and IL-13 at the onset of helminth expulsion
  publication-title: J Exp Med.
  doi: 10.1084/jem.20051615
– volume: 52
  start-page: 370
  year: 2004
  ident: B80
  article-title: Ecology of danger-dependent cytokine-boosted spontaneous abortion in the CBA x DBA/2 mouse model. I. Synergistic effect of LPS and (TNF-alpha + IFN-gamma) on pregnancy loss
  publication-title: Am J Reprod Immunol.
  doi: 10.1111/j.1600-0897.2004.00237.x
– volume: 85
  start-page: e01049
  year: 2017
  ident: B17
  article-title: Human three-dimensional endometrial epithelial cell model to study host interactions with vaginal bacteria and Neisseria gonorrhoeae
  publication-title: Infect Immun.
  doi: 10.1128/IAI.01049-16
– volume: 9
  start-page: 208
  year: 2018
  ident: B69
  article-title: Uterine microbiota: residents, tourists, or invaders?
  publication-title: Front Immunol.
  doi: 10.3389/fimmu.2018.00208
– volume-title: Atlas of Human Anatomy
  year: 2019
  ident: B6
– volume: 118
  start-page: 58
  year: 2006
  ident: B54
  article-title: Oestradiol potentiates the suppressive function of human CD4 CD25 regulatory T cells by promoting their proliferation
  publication-title: Immunology.
  doi: 10.1111/j.1365-2567.2006.02339.x
– volume: 13
  start-page: 44
  year: 1998
  ident: B61
  article-title: Characterization of endometrial T lymphocyte subpopulations in spontaneous early pregnancy loss
  publication-title: Hum Reprod.
  doi: 10.1093/humrep/13.1.44
– volume: 97
  start-page: 625
  year: 2019
  ident: B79
  article-title: The microbiome and immune memory formation
  publication-title: Immunol Cell Biol.
  doi: 10.1111/imcb.12273
– volume: 15
  start-page: 217
  year: 2015
  ident: B5
  article-title: The role of sex hormones in immune protection of the female reproductive tract
  publication-title: Nat Rev Immunol.
  doi: 10.1038/nri3819
– volume: 13
  start-page: 145
  year: 2013
  ident: B27
  article-title: Innate lymphoid cells–a proposal for uniform nomenclature
  publication-title: Nat Rev Immunol.
  doi: 10.1038/nri3365
– volume: 23
  start-page: 1574
  year: 2008
  ident: B53
  article-title: Endometrial dendritic cell populations during the normal menstrual cycle
  publication-title: Hum Reprod.
  doi: 10.1093/humrep/den030
– volume: 213
  start-page: 644
  year: 2015
  ident: B14
  article-title: The new world of the urinary microbiota in women
  publication-title: Am J Obstet Gynecol.
  doi: 10.1016/j.ajog.2015.05.032
– volume: 50
  start-page: 385
  year: 1995
  ident: B43
  article-title: Effects of progestogens on human endometrium
  publication-title: Obstet Gynecol Surv.
  doi: 10.1097/00006254-199505000-00026
– volume: 124
  start-page: 16
  year: 2018
  ident: B68
  article-title: A slippery slope: on the origin, role and physiology of mucus
  publication-title: Adv Drug Deliv Rev.
  doi: 10.1016/j.addr.2017.10.014
– volume: 15
  start-page: 16
  year: 2015
  ident: B10
  article-title: Immune cells in the female reproductive tract
  publication-title: Immune Netw.
  doi: 10.4110/in.2015.15.1.16
– volume: 44
  start-page: 1
  year: 1999
  ident: B45
  article-title: Menstruation: induction by matrix metalloproteinases and inflammatory cells
  publication-title: J Reprod Immunol.
  doi: 10.1016/S0165-0378(99)00002-9
– volume: 6
  start-page: 16
  year: 2000
  ident: B41
  article-title: Endometrial leukocytes and menstruation
  publication-title: Hum Reprod Update.
  doi: 10.1093/humupd/6.1.16
– volume: 21
  start-page: 3872
  year: 2007
  ident: B72
  article-title: Globular structure of human ovulatory cervical mucus
  publication-title: FASEB J.
  doi: 10.1096/fj.07-8189com
– volume: 93
  start-page: 102
  year: 2014
  ident: B73
  article-title: The cervical mucus plug inhibits, but does not block, the passage of ascending bacteria from the vagina during pregnancy
  publication-title: Acta Obstet Gynecol Scand.
  doi: 10.1111/aogs.12296
– volume: 185
  start-page: 3913
  year: 2010
  ident: B38
  article-title: Immature NK cells, capable of producing IL-22, are present in human uterine mucosa
  publication-title: J Immunol.
  doi: 10.4049/jimmunol.1001637
– volume: 23
  start-page: 41
  year: 1993
  ident: B58
  article-title: An immunohistochemical study of leucocytes in human endometrium, first and third trimester basal decidua
  publication-title: J Reprod Immunol.
  doi: 10.1016/0165-0378(93)90025-D
– volume: 33
  start-page: 129
  year: 2016
  ident: B16
  article-title: Endometrial microbiome at the time of embryo transfer: next-generation sequencing of the 16S ribosomal subunit
  publication-title: J Assist Reprod Genet.
  doi: 10.1007/s10815-015-0614-z
– volume: 115
  start-page: 514
  year: 2001
  ident: B51
  article-title: The role of mast cells in tumour angiogenesis
  publication-title: Br J Haematol.
  doi: 10.1046/j.1365-2141.2001.03202.x
– volume: 174
  start-page: 1054
  year: 2018
  ident: B28
  article-title: Innate lymphoid cells: 10 years on
  publication-title: Cell.
  doi: 10.1016/j.cell.2018.07.017
– volume: 24
  start-page: 393
  year: 2018
  ident: B25
  article-title: How uterine microbiota might be responsible for a receptive, fertile endometrium
  publication-title: Hum Reprod Update.
  doi: 10.1093/humupd/dmy012
– volume: 215
  start-page: 684
  year: 2016
  ident: B22
  article-title: Evidence that the endometrial microbiota has an effect on implantation success or failure
  publication-title: Am J Obstet Gynecol.
  doi: 10.1016/j.ajog.2016.09.075
– volume: 97
  start-page: 3603
  year: 2012
  ident: B40
  article-title: Chemerin regulates NK cell accumulation and endothelial cell morphogenesis in the decidua during early pregnancy
  publication-title: J Clin Endocrinol Metab.
  doi: 10.1210/jc.2012-1102
– volume: 23
  start-page: 295
  year: 1972
  ident: B71
  article-title: The function of the cervix in fertility
  publication-title: Fertil Steril.
  doi: 10.1016/S0015-0282(16)38890-2
– volume: 9
  start-page: e110152
  year: 2014
  ident: B76
  article-title: Bacterial communities in semen from men of infertile couples: metagenomic sequencing reveals relationships of seminal microbiota to semen quality
  publication-title: PLoS ONE.
  doi: 10.1371/journal.pone.0110152
– volume: 193
  start-page: 4289
  year: 2014
  ident: B57
  article-title: Origins of gammadelta T cell effector subsets: a riddle wrapped in an enigma
  publication-title: J Immunol.
  doi: 10.4049/jimmunol.1401813
– volume: 214
  start-page: 456
  year: 2008
  ident: B56
  article-title: Induction of regulatory T cells by physiological level estrogen
  publication-title: J Cell Physiol.
  doi: 10.1002/jcp.21221
– volume: 4
  start-page: e1602
  year: 2016
  ident: B15
  article-title: Characterisation of the human uterine microbiome in non-pregnant women through deep sequencing of the V1-2 region of the 16S rRNA gene
  publication-title: PeerJ.
  doi: 10.7717/peerj.1602
– volume: 4
  start-page: 702
  year: 1998
  ident: B65
  article-title: Phenotypic and functional studies of leukocytes in human endometrium and endometriosis
  publication-title: Hum Reprod Update.
  doi: 10.1093/humupd/4.5.702
– volume: 78
  start-page: 481
  year: 2016
  ident: B13
  article-title: The microbiome and the respiratory tract
  publication-title: Annu Rev Physiol.
  doi: 10.1146/annurev-physiol-021115-105238
– start-page: xix
  volume-title: Guyton and Hall Textbook of Medical Physiology
  year: 2016
  ident: B9
– volume: 14
  start-page: 646
  year: 2013
  ident: B18
  article-title: Compartmentalized and systemic control of tissue immunity by commensals
  publication-title: Nat Immunol.
  doi: 10.1038/ni.2604
– volume: 12
  start-page: 1045
  year: 2011
  ident: B36
  article-title: Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus
  publication-title: Nat Immunol.
  doi: 10.1038/ni.2131
– volume: 110
  start-page: 337
  year: 2018
  ident: B77
  article-title: Relevance of assessing the uterine microbiota in infertility
  publication-title: Fertil Steril.
  doi: 10.1016/j.fertnstert.2018.04.041
– volume: 160
  start-page: 5145
  year: 1998
  ident: B48
  article-title: IFN-gamma is produced by polymorphonuclear neutrophils in human uterine endometrium and by cultured peripheral blood polymorphonuclear neutrophils
  publication-title: J Immunol.
  doi: 10.4049/jimmunol.160.10.5145
– volume: 9
  start-page: 1874
  year: 2018
  ident: B24
  article-title: Commentary: uterine microbiota: residents, tourists, or invaders?
  publication-title: Front Immunol.
  doi: 10.3389/fimmu.2018.01874
– volume: 104
  start-page: 3378
  year: 2007
  ident: B63
  article-title: TGFbeta promotes conversion of CD16+ peripheral blood NK cells into CD16- NK cells with similarities to decidual NK cells
  publication-title: Proc Natl Acad Sci USA.
  doi: 10.1073/pnas.0611098104
– volume: 37
  start-page: 29
  year: 1992
  ident: B67
  article-title: Macrophage- and lymphocyte-subtypes in the endometrium during different phases of the ovarian cycle
  publication-title: Int J Gynaecol Obstet.
  doi: 10.1016/0020-7292(92)90974-N
– volume: 43
  start-page: 209
  year: 2000
  ident: B64
  article-title: Menstrual cycle dependent fluctuations in NK and T-lymphocyte subsets from non-pregnant human endometrium
  publication-title: Am J Reprod Immunol.
  doi: 10.1111/j.8755-8920.2000.430405.x
– start-page: xvi
  volume-title: Reproductive Medicine and Surgery
  year: 1994
  ident: B70
– volume: 102
  start-page: 434
  year: 2001
  ident: B62
  article-title: CD8+ T cells in human uterine endometrial lymphoid aggregates: evidence for accumulation of cells by trafficking
  publication-title: Immunology.
  doi: 10.1046/j.1365-2567.2001.01199.x
– volume: 8
  start-page: 875
  year: 2017
  ident: B23
  article-title: The microbiota continuum along the female reproductive tract and its relation to uterine-related diseases
  publication-title: Nat Commun.
  doi: 10.1038/s41467-017-00901-0
– volume: 6
  start-page: 646
  year: 2015
  ident: B30
  article-title: Unique Eomes(+) NK cell subsets are present in uterus and decidua during early pregnancy
  publication-title: Front Immunol.
  doi: 10.3389/fimmu.2015.00646
– volume: 195
  start-page: 3937
  year: 2015
  ident: B29
  article-title: Composition, development, and function of uterine innate lymphoid cells
  publication-title: J Immunol.
  doi: 10.4049/jimmunol.1500689
– start-page: xviii
  volume-title: Gray's Anatomy : The Anatomical Basis of Clinical Practice
  year: 2016
  ident: B7
– volume: 181
  start-page: 68
  year: 1997
  ident: B49
  article-title: Role of interferon-gamma in the priming of decidual macrophages for nitric oxide production and early pregnancy loss
  publication-title: Cell Immunol.
  doi: 10.1006/cimm.1997.1199
– volume: 149
  start-page: 2872
  year: 1992
  ident: B59
  article-title: Characterization of gamma delta T lymphocytes at the maternal-fetal interface
  publication-title: J Immunol.
  doi: 10.4049/jimmunol.149.9.2872
– volume: 166
  start-page: 1044
  year: 1992
  ident: B60
  article-title: Evidence of embryo- and trophoblast-toxic cellular immune response(s) in women with recurrent spontaneous abortion
  publication-title: Am J Obstet Gynecol.
  doi: 10.1016/S0002-9378(11)90589-4
– volume: 372
  start-page: 190
  year: 1994
  ident: B32
  article-title: Adhesion between epithelial cells and T lymphocytes mediated by E-cadherin and the alpha E beta 7 integrin
  publication-title: Nature.
  doi: 10.1038/372190a0
– volume: 53
  start-page: 312
  year: 1995
  ident: B50
  article-title: Mast cell and eosinophil distribution and activation in human endometrium throughout the menstrual cycle
  publication-title: Biol Reprod.
  doi: 10.1095/biolreprod53.2.312
– volume: 185
  start-page: 756
  year: 2010
  ident: B26
  article-title: Fluctuation of peripheral blood T, B, and NK cells during a menstrual cycle of normal healthy women
  publication-title: J Immunol.
  doi: 10.4049/jimmunol.0904192
– volume: 71
  start-page: 252
  year: 2014
  ident: B11
  article-title: Distribution of immune cells in the human cervix and implications for HIV transmission
  publication-title: Am J Reprod Immunol.
  doi: 10.1111/aji.12198
– volume: 212
  start-page: 611 e1
  year: 2015
  ident: B21
  article-title: Colonization of the upper genital tract by vaginal bacterial species in nonpregnant women
  publication-title: Am J Obstet Gynecol.
  doi: 10.1016/j.ajog.2014.11.043
– volume: 93
  start-page: 217
  year: 2013
  ident: B42
  article-title: The importance of the macrophage within the human endometrium
  publication-title: J Leukoc Biol.
  doi: 10.1189/jlb.0712327
SSID ssj0000493335
Score 2.5593288
SecondaryResourceType review_article
Snippet The female reproductive tract harbors distinct microbial communities, as in the vagina, cervical canal, uterus, and fallopian tubes. The nature of the vaginal...
SourceID doaj
pubmedcentral
proquest
pubmed
crossref
SourceType Open Website
Open Access Repository
Aggregation Database
Index Database
Enrichment Source
StartPage 2387
SubjectTerms cellular immunity
immune cells
Immunology
menstruation
microbiota
pregnancy
uterus
SummonAdditionalLinks – databaseName: DOAJ Directory of Open Access Journals
  dbid: DOA
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV1LS8QwEA4iCF7Et-uLCl481O1umjbxpqKosCKo4C0kzUQrbhXtHvz3zjS7y66IXry2CUm_STrfMC_G9j1eMNVFswSU8zHeRBVLZV2ceSm8T1xHWUoU7l1nF_fp1YN4mGj1RTFhoTxwAK5tQfLE4rRM2pRLkCAopwGPGs8VkmX6-yYqmTCmngPv5ZyL4JdEK0y1fdnvDyiUSx2Smsqn9FBTrv8njvk9VHJC95wvsoUhaYyOw2aX2AxUy2wutJH8XGHpfd0k8UWXTbJH_RmZykW9MtRYqs1RdBzdPpWeIpyjG_NuXPnYX2V352d3pxfxsBtCXIiurGNvANJuKlPJAVCngEOuImVWOMjAJdyAN4qnLrdOSei4zCYSUPsiQ_EcBF9js9VrBRsssjkkAOAL2ymQjwnThcwZ6jpc4CJctFh7BI0uhpXCqWHFi0aLgcDUDZiawNQNmC12MJ7xFqpk_DL2hNAej6P61s0DlLoeSl3_JfUW2xvJSuN9ICeHqeB18KGRr5JNmQv8jPUgu_FS1KSLPIctlk9JdWov02-q8qmpuY0TkRvJzf_Y_BabJzhIA3bybTZbvw9gB6lNbXebU_wFvrn2Vw
  priority: 102
  providerName: Directory of Open Access Journals
Title Uterine Immunity and Microbiota: A Shifting Paradigm
URI https://www.ncbi.nlm.nih.gov/pubmed/31681281
https://www.proquest.com/docview/2311924755
https://pubmed.ncbi.nlm.nih.gov/PMC6811518
https://doaj.org/article/be830bff068b438e8e58624425379576
Volume 10
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwjV1Lb9QwELZKKyQuFZRHl0cVJC4c0iZrx7GRECqoD5CKkOhKe7PseNym6mZhm5XYf8-Mky4sWlVcckicOB7PZL7JvBh7E1DA9BDNEtA-pCiJOlXa-VQGVYSQ-Vw7ShQ--ypPR-LLuBj_SY_uCXiz1rSjflKj2fX-r5-LDyjw78niRH17EOrJZE5RWnqfNFB5j21FbxEF8vVg_6rDwpzHjpu5lCJFThad33LtQ1b0VCznvw6D_htK-ZduOn7ItntQmRx2XPCIbUCzw-53bSYXj5kYtTHJL_kck0HaRWIbn5zVXQ2m1r5LDpPvl3WgCOjkm51ZX19MnrDz46PzT6dp3y0hrYqhatNgAcRQKKE4AOoc8IhllJKVBwk-4xaC1Vz40nmtIPfSZQpQOyOCCRwK_pRtNtMGdlniSsgAIFQurxCvFXYI0lvqSlzhJLwYsINb0piqryRODS2uDVoUREwTiWmImCYSc8DeLu_40VXRuGPsR6L2chzVv44nprML04uTcaB45pCZpHKCK1BQUKYLfoB4qdGEGrDXt3tlUF7ICWIbmM5vDOJZsjnLApfxrNu75VTUxIs8iwNWruzqyrusXmnqy1iTG29E7KSe_8e8L9gDWi0pwLx8yTbb2RxeIbJp3V78I4DHk3G-F5n3N6Qi-IM
linkProvider Scholars Portal
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Uterine+Immunity+and+Microbiota%3A+A+Shifting+Paradigm&rft.jtitle=Frontiers+in+immunology&rft.au=Agostinis%2C+Chiara&rft.au=Mangogna%2C+Alessandro&rft.au=Bossi%2C+Fleur&rft.au=Ricci%2C+Giuseppe&rft.date=2019-10-17&rft.issn=1664-3224&rft.eissn=1664-3224&rft.volume=10&rft.spage=2387&rft_id=info:doi/10.3389%2Ffimmu.2019.02387&rft.externalDBID=NO_FULL_TEXT
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1664-3224&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1664-3224&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1664-3224&client=summon