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Enteric Glia Regulate Gastrointestinal Motility but are not Required for Maintenance of the Epithelium in Mice.

Abstract When the glial fibrillary acidic protein (GFAP) promoter is used to express cellular toxins that eliminate glia in mice, intestinal epithelial permeability and proliferation increase; this led to the concept that glia are required for maintenance of the gastrointestinal epithelium. Many enteric glia, however, particularly in the mucosa, do not express GFAP. In contrast, virtually all enteric glia express proteolipid protein 1 (PLP1). We investigated whether elimination of PLP1-expressing cells compromises epithelial maintenance or gastrointestinal motility.
PMID
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Authors

Mayor MeshTerms
Keywords

enteric nervous system

epithelial barrier

sex differences

Journal Title gastroenterology
Publication Year Start




PMID- 28711628
OWN - NLM
STAT- Publisher
DA  - 20170716
LR  - 20170716
IS  - 1528-0012 (Electronic)
IS  - 0016-5085 (Linking)
DP  - 2017 Jul 12
TI  - Enteric Glia Regulate Gastrointestinal Motility but are not Required for
      Maintenance of the Epithelium in Mice.
LID - S0016-5085(17)35867-5 [pii]
LID - 10.1053/j.gastro.2017.07.002 [doi]
AB  - BACKGROUND & AIMS: When the glial fibrillary acidic protein (GFAP) promoter is
      used to express cellular toxins that eliminate glia in mice, intestinal
      epithelial permeability and proliferation increase; this led to the concept that 
      glia are required for maintenance of the gastrointestinal epithelium. Many
      enteric glia, however, particularly in the mucosa, do not express GFAP. In
      contrast, virtually all enteric glia express proteolipid protein 1 (PLP1). We
      investigated whether elimination of PLP1-expressing cells compromises epithelial 
      maintenance or gastrointestinal motility. METHODS: We generated mice that express
      tamoxifen-inducible Cre recombinase under control of the Plp1 promoter and carry 
      the diptheria toxin subunit A (DTA) transgene in the Rosa26 locus
      (Plp1CreER;Rosa26DTA mice). In these mice, PLP1-expressing glia are selectively
      eliminated without affecting neighboring cells. We measured epithelial barrier
      function and gastrointestinal motility in these mice and littermate controls, and
      analyzed epithelial cell proliferation and ultrastructure from their intestinal
      tissues. To compare our findings with those from previous studies, we also
      eliminated glia with ganciclovir in GfapHSV-TK mice. RESULTS: Expression of DTA
      in PLP1-expressing cells selectively eliminated enteric glia from the small and
      large intestines, but caused no defects in epithelial proliferation, barrier
      integrity, or ultrastructure. In contrast, administration of ganciclovir to
      GfapHSV-TK mice eliminated fewer glia but caused considerable non-glial toxicity 
      and epithelial cell death. Elimination of PLP1-expressing cells did not reduce
      survival of neurons in the intestine, but altered gastrointestinal motility in
      female, but not male, mice. CONCLUSIONS: Using the Plp1 promoter to selectively
      eliminate glia in mice, we found that enteric glia are not required for
      maintenance of the intestinal epithelium but are required for regulation of
      intestinal motility in females. Previous observations supporting the concept that
      maintenance of the intestinal epithelium requires enteric glia can be attributed 
      to non-glial toxicity in GfapHSV-TK mice and epithelial-cell expression of GFAP. 
      Contrary to widespread notions, enteric glia are therefore not required for
      epithelial homeostasis. However, they regulate intestinal motility in a
      sex-dependent manner.
CI  - Copyright (c) 2017 AGA Institute. Published by Elsevier Inc. All rights reserved.
FAU - Rao, Meenakshi
AU  - Rao M
AD  - Department of Pediatrics, Columbia University Medical Center, New York, NY, USA. 
      Electronic address: [email protected]
FAU - Rastelli, Daniella
AU  - Rastelli D
AD  - Department of Pediatrics, Columbia University Medical Center, New York, NY, USA.
FAU - Dong, Lauren
AU  - Dong L
AD  - Department of Pediatrics, Columbia University Medical Center, New York, NY, USA.
FAU - Chiu, Sophia
AU  - Chiu S
AD  - Institute of Human Nutrition, Columbia University.
FAU - Setlik, Wanda
AU  - Setlik W
AD  - Department of Pathology and Cell Biology, Columbia University.
FAU - Gershon, Michael D
AU  - Gershon MD
AD  - Department of Pathology and Cell Biology, Columbia University.
FAU - Corfas, Gabriel
AU  - Corfas G
AD  - Department of Otolaryngology-Head and Neck Surgery, Kresge Hearing Research
      Institute, Ann Arbor, MI, USA.
LA  - eng
PT  - Journal Article
DEP - 20170712
PL  - United States
TA  - Gastroenterology
JT  - Gastroenterology
JID - 0374630
OTO - NOTNLM
OT  - enteric nervous system
OT  - epithelial barrier
OT  - sex differences
EDAT- 2017/07/18 06:00
MHDA- 2017/07/18 06:00
CRDT- 2017/07/17 06:00
PHST- 2017/05/11 [received]
PHST- 2017/06/30 [revised]
PHST- 2017/07/04 [accepted]
AID - S0016-5085(17)35867-5 [pii]
AID - 10.1053/j.gastro.2017.07.002 [doi]
PST - aheadofprint
SO  - Gastroenterology. 2017 Jul 12. pii: S0016-5085(17)35867-5. doi:
      10.1053/j.gastro.2017.07.002.