Enteric glia express proteolipid protein 1 and are a transcriptionally unique population of glia in the mammalian nervous system

GLIA

Volumn 63, Issue 11, 2015, Pages 2040-2057

  Rao, Meenakshi ^a,b   Nelms, Bradlee D ^a   Dong, Lauren ^b   Salinas Rios, Viviana ^a   Rutlin, Michael ^b   Gershon, Michael D ^b   Corfas, Gabriel ^a,c,d  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b Howard Hughes Medical Institute   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Enteric nervous system; Gastrointestinal tract; Neuroglia; RNA Seq

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; MOLECULAR MARKER; PROTEIN S100B; PROTEOLIPID PROTEIN; PROTEOLIPID PROTEIN 1; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL STRUCTURE; CELL SUBPOPULATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENTERIC GLIA; FEMALE; GENE EXPRESSION; GENETIC TRANSCRIPTION; GLIA; INTESTINE; INTESTINE INNERVATION; MALE; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA SEQUENCE; SEQUENCE ANALYSIS;

EID: 84941189827     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22876     Document Type: Article

References (62)

1. Aube AC, Cabarrocas J, Bauer J, Philippe D, Aubert P, Doulay F, Liblau R, Galmiche JP, Neunlist M. 2006. Changes in enteric neurone phenotype and intestinal functions in a transgenic mouse model of enteric glia disruption. Gut 55:630-637.
2. Boesmans W, Lasrado R, Vanden Berghe P, Pachnis V. 2015. Heterogeneity and phenotypic plasticity of glial cells in the mammalian enteric nervous system. Glia 63:229-241.
3. Bohorquez DV, Samsa LA, Roholt A, Medicetty S, Chandra R, Liddle RA. 2014. An enteroendocrine cell-enteric glia connection revealed by 3D electron microscopy. PLoS One 9:e89881.
4. Braun N, Sevigny J, Robson SC, Hammer K, Hanani M, Zimmermann H. 2004. Association of the ecto-ATPase NTPDase2 with glial cells of the peripheral nervous system. Glia 45:124-132.
5. Buchstaller J, Sommer L, Bodmer M, Hoffmann R, Suter U, Mantei N. 2004. Efficient isolation and gene expression profiling of small numbers of neural crest stem cells and developing Schwann cells. J Neurosci 24:2357-2365.
6. Bush TG, Savidge TC, Freeman TC, Cox HJ, Campbell EA, Mucke L, Johnson MH, Sofroniew MV. 1998. Fulminant jejuno-ileitis following ablation of enteric glia in adult transgenic mice. Cell 93:189-201.
7. Cahoy JD, Emery B, Kaushal A, Foo LC, Zamanian JL, Christopherson KS, Xing Y, Lubischer JL, Krieg PA, Krupenko SA, et al. 2008. A transcriptome database for astrocytes, neurons, and oligodendrocytes: A new resource for understanding brain development and function. J Neurosci 28:264-278.
8. Carpenter AE, Jones TR, Lamprecht MR, Clarke C, Kang IH, Friman O, Guertin DA, Chang JH, Lindquist RA, Moffat J, et al. 2006. CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol 7:R100.
9. Clairembault T, Kamphuis W, Leclair-Visonneau L, Rolli-Derkinderen M, Coron E, Neunlist M, Hol EM, Derkinderen P. 2014. Enteric GFAP expression and phosphorylation in Parkinson's disease. J Neurochem 130:805-815.
10. Cook RD, Burnstock G. 1976. The ultrastructure of Auerbach's plexus in the guinea-pig. II. Non-neuronal elements. J Neurocytol 5:195-206.
11. Deber CM, Reynolds SJ. 1991. Central nervous system myelin: Structure, function, and pathology. Clin Biochem 24:113-134.
12. Doerflinger NH, Macklin WB, Popko B. 2003. Inducible site-specific recombination in myelinating cells. Genesis 35:63-72.
13. Duregotti E, Negro S, Scorzeto M, Zornetta I, Dickinson BC, Chang CJ, Montecucco C, Rigoni M. 2015. Mitochondrial alarmins released by degenerating motor axon terminals activate perisynaptic Schwann cells. Proc Natl Acad Sci USA 112:E497-505.
14. el Marjou F, Janssen KP, Chang BH, Li M, Hindie V, Chan L, Louvard D, Chambon P, Metzger D, Robine S. 2004. Tissue-specific and inducible Cre-mediated recombination in the gut epithelium. Genesis 39:186-193.
15. Engreitz JM, Daigle BJ Jr., Marshall JJ, Altman RB. 2010. Independent component analysis: Mining microarray data for fundamental human gene expression modules. J Biomed Inform 43:932-944.
16. Furness JB. 2006. The enteric nervous system. Malden, Mass.: Blackwell Pub. xiii, p 274.
17. Gabella G. 1971. Glial cells in the myenteric plexus. Z Naturforsch B 26:244-245.
18. Gabella G. 1972. Fine structure of the myenteric plexus in the guinea-pig ileum. J Anat 111:69-97.
19. Galau GA, Klein WH, Britten RJ, Davidson EH. 1977. Significance of rare mRNA sequences in liver. Arch Biochem Biophys 179:584-599.
20. Garbay B, Heape AM, Sargueil F, Cassagne C. 2000. Myelin synthesis in the peripheral nervous system. Prog Neurobiol 61:267-304.
21. Garcia SB, Stopper H, Kannen V. 2014. The contribution of neuronal-glial-endothelial-epithelial interactions to colon carcinogenesis. Cell Mol Life Sci 71:3191-3197.
22. Gershon MD, Rothman TP. 1991. Enteric glia. Glia 4:195-204.
23. Gomez-Casati ME, Murtie J, Taylor B, Corfas G. 2010. Cell-specific inducible gene recombination in postnatal inner ear supporting cells and glia. J Assoc Res Otolaryngol 11:19-26.
24. Gulbransen BD, Sharkey KA. 2012. Novel functional roles for enteric glia in the gastrointestinal tract. Nat Rev Gastroenterol Hepatol 9:625-632.
25. Hanani M, Reichenbach A. 1994. Morphology of horseradish peroxidase (HRP)-injected glial cells in the myenteric plexus of the guinea-pig. Cell Tissue Res 278:153-160.
26. Harauz G, Boggs JM. 2013. Myelin management by the 18.5-kDa and 21.5-kDa classic myelin basic protein isoforms. J Neurochem 125:334-361.
27. Hawrylycz MJ, Lein ES, Guillozet-Bongaarts AL, Shen EH, Ng L, Miller JA, van de Lagemaat LN, Smith KA, Ebbert A, Riley ZL, et al. 2012. An anatomically comprehensive atlas of the adult human brain transcriptome. Nature 489:391-399.
28. Henning SJ. 1981. Postnatal development: Coordination of feeding, digestion, and metabolism. Am J Physiol 241:G199-214.
29. Hoff S, Zeller F, von Weyhern CW, Wegner M, Schemann M, Michel K, Ruhl A. 2008. Quantitative assessment of glial cells in the human and guinea pig enteric nervous system with an anti-Sox8/9/10 antibody. J Comp Neurol 509:356-371.
30. Jessen KR, Mirsky R. 1980. Glial cells in the enteric nervous system contain glial fibrillary acidic protein. Nature 286:736-737.
31. Jessen KR, Mirsky R. 1983. Astrocyte-like glia in the peripheral nervous system: an immunohistochemical study of enteric glia. J Neurosci 3:2206-2218.
32. Jessen KR, Mirsky R. 2005. The origin and development of glial cells in peripheral nerves. Nat Rev Neurosci 6:671-682.
33. Karim SA, Barrie JA, McCulloch MC, Montague P, Edgar JM, Kirkham D, Anderson TJ, Nave KA, Griffiths IR, McLaughlin M. 2007. PLP overexpression perturbs myelin protein composition and myelination in a mouse model of Pelizaeus-Merzbacher disease. Glia 55:341-351.
34. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357-359.
35. Laranjeira C, Sandgren K, Kessaris N, Richardson W, Potocnik A, Vanden Berghe P, Pachnis V. 2011. Glial cells in the mouse enteric nervous system can undergo neurogenesis in response to injury. J Clin Invest 121:3412-3424.
36. Lavoie EG, Gulbransen BD, Martin-Satue M, Aliagas E, Sharkey KA, Sevigny J. 2011. Ectonucleotidases in the digestive system: Focus on NTPDase3 localization. Am J Physiol Gastrointest Liver Physiol 300:G608-G620.
37. Li L, Rutlin M, Abraira VE, Cassidy C, Kus L, Gong S, Jankowski MP, Luo W, Heintz N, Koerber HR, et al. 2011. The functional organization of cutaneous low-threshold mechanosensory neurons. Cell 147:1615-1627.
38. Liu YA, Chung YC, Pan ST, Shen MY, Hou YC, Peng SJ, Pasricha PJ, Tang SC. 2013. 3-D imaging, illustration, and quantitation of enteric glial network in transparent human colon mucosa. Neurogastroenterol Motil 25:e324-e338.
39. Lottaz C, Yang X, Scheid S, Spang R. 2006. OrderedList-a bioconductor package for detecting similarity in ordered gene lists. Bioinformatics 22:2315-2316.
40. Lukk M, Kapushesky M, Nikkila J, Parkinson H, Goncalves A, Huber W, Ukkonen E, Brazma A. 2010. A global map of human gene expression. Nat Biotechnol 28:322-324.
41. Madisen L, Zwingman TA, Sunkin SM, Oh SW, Zariwala HA, Gu H, Ng LL, Palmiter RD, Hawrylycz MJ, Jones AR, et al. 2010. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci 13:133-140.
42. Mallon BS, Shick HE, Kidd GJ, Macklin WB. 2002. Proteolipid promoter activity distinguishes two populations of NG2-positive cells throughout neonatal cortical development. J Neurosci 22:876-885.
43. Maudlej N, Hanani M. 1992. Modulation of dye coupling among glial cells in the myenteric and submucosal plexuses of the guinea pig. Brain Res 578:94-98.
44. Miyamoto Y, Torii T, Tanoue A, Yamauchi J. 2012. Pelizaeus-Merzbacher disease-associated proteolipid protein 1 inhibits oligodendrocyte precursor cell differentiation via extracellular-signal regulated kinase signaling. Biochem Biophys Res Commun 424:262-268.
45. Morris JK, Maklad A, Hansen LA, Feng F, Sorensen C, Lee KF, Macklin WB, Fritzsch B. 2006. A disorganized innervation of the inner ear persists in the absence of ErbB2. Brain Res 1091:186-199.
46. Mundell NA, Plank JL, LeGrone AW, Frist AY, Zhu L, Shin MK, Southard-Smith EM, Labosky PA. 2012. Enteric nervous system specific deletion of Foxd3 disrupts glial cell differentiation and activates compensatory enteric progenitors. Dev Biol 363:373-387.
47. Nasser Y, Fernandez E, Keenan CM, Ho W, Oland LD, Tibbles LA, Schemann M, MacNaughton WK, Ruhl A, Sharkey KA. 2006a. Role of enteric glia in intestinal physiology: effects of the gliotoxin fluorocitrate on motor and secretory function. Am J Physiol Gastrointest Liver Physiol 291:G912-G927.
48. Nasser Y, Ho W, Sharkey KA. 2006b. Distribution of adrenergic receptors in the enteric nervous system of the guinea pig, mouse, and rat. J Comp Neurol 495:529-553.
49. Neunlist M, Van Landeghem L, Mahe MM, Derkinderen P, des Varannes SB, Rolli-Derkinderen M. 2013. The digestive neuronal-glial-epithelial unit: A new actor in gut health and disease. Nat Rev Gastroenterol Hepatol 10:90-100.
50. Savidge TC, Newman P, Pothoulakis C, Ruhl A, Neunlist M, Bourreille A, Hurst R, Sofroniew MV. 2007. Enteric glia regulate intestinal barrier function and inflammation via release of S-nitrosoglutathione. Gastroenterology 132:1344-1358.
51. Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671-675.
52. Silver J, Miller JH. 2004. Regeneration beyond the glial scar. Nat Rev Neurosci 5:146-156.
53. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, et al. 2005. Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 102:15545-15550.
54. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L. 2012. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7:562-578.
55. Wilson AJ, Furness JB, Costa M. 1981. The fine structure of the submucous plexus of the guinea-pig ileum. I. The ganglia, neurons, Schwann cells and neuropil. J Neurocytol 10:759-784.
56. Wink MR, Braganhol E, Tamajusuku AS, Lenz G, Zerbini LF, Libermann TA, Sevigny J, Battastini AM, Robson SC. 2006. Nucleoside triphosphate diphosphohydrolase-2 (NTPDase2/CD39L1) is the dominant ectonucleotidase expressed by rat astrocytes. Neuroscience 138:421-432.
57. Yang X, Bentink S, Scheid S, Spang R. 2006. Similarities of ordered gene lists. J Bioinform Comput Biol 4:693-708.
58. Young HM, Bergner AJ, Muller T. 2003. Acquisition of neuronal and glial markers by neural crest-derived cells in the mouse intestine. J Comp Neurol 456:1-11.
59. Zhang Y, Chen K, Sloan SA, Bennett ML, Scholze AR, O'Keeffe S, Phatnani HP, Guarnieri P, Caneda C, Ruderisch N, et al. 2014. An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. J Neurosci 34:11929-11947.
60. Zheng-Bradley X, Rung J, Parkinson H, Brazma A. 2010. Large scale comparison of global gene expression patterns in human and mouse. Genome Biol 11:R124.
61. Zhu Y, Davis S, Stephens R, Meltzer PS, Chen Y. 2008. GEOmetadb: Powerful alternative search engine for the Gene Expression Omnibus. Bioinformatics 24:2798--2800.
62. Zilliox MJ, Irizarry RA. 2007. A gene expression bar code for microarray data. Nat Methods 4:911-913.