Enteric glia are multipotent in culture but primarily form glia in the adult rodent gut

Journal of Clinical Investigation

Volumn 121, Issue 9, 2011, Pages 3398-3411

  Joseph, Nancy M ^a   He, Shenghui ^a   Quintana, Elsa ^a   Kim, Yun Gi ^b   Núñez, Gabriel ^b   Morrison, Sean J ^a  

^a Life Sciences Institute   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA2 INTEGRIN; BENZALKONIUM CHLORIDE; GLIAL FIBRILLARY ACIDIC PROTEIN; NEUROTROPHIN RECEPTOR P75; PROTEIN S100B; TRANSCRIPTION FACTOR SOX10;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CYCLE PROGRESSION; CELL DIFFERENTIATION; CELL FUNCTION; CELL ISOLATION; CELL PROLIFERATION; CELL STRUCTURE; CELLULAR DISTRIBUTION; CENTRAL NERVOUS SYSTEM; DIET; EXERCISE; GLIA CELL; HYPERGLYCEMIA; INFLAMMATION; INTESTINE INJURY; INTESTINE INNERVATION; INTESTINE STENOSIS; MOUSE; MULTIPOTENT STEM CELL; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEURAL CREST CELL; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; DIET; ENTERIC NERVOUS SYSTEM; FEMALE; GASTROINTESTINAL TRACT; HUMANS; MICE; MICE, INBRED C57BL; MULTIPOTENT STEM CELLS; NEURAL CREST; NEUROGENESIS; NEUROGLIA; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY;

EID: 80052381647     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI58186     Document Type: Article

References (55)

1. Altman J., Das G.D. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol. 1965;124(3):319-335.
2. Altman J., Das G.D. Autoradiographic and histological studies of postnatal neurogenesis. J Comp Neurol. 1966;126(3):337-390.
3. Altman J. Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J Comp Neurol. 1969;137(4):433-458.
4. Luskin M.B. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron. 1993; 11(1):173-189. (Pubitemid 23222544)
5. Seki T., Arai Y. Highly polysialylated neural cell adhesion molecule (NCAM-H) is expressed by newly generated granule cells in the dentate gyrus of the adult rat. J Neurosci. 1993;13(6):2351-2358. (Pubitemid 23151752)
6. Lois C., Alvarez-Buylla A. Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc Natl Acad Sci U S A. 1993;90(5):2074-2077. (Pubitemid 23070000)
7. Kuhn H.G., Dickinson-Anson H., Gage F.H. Neurogenesis in the dentate gyrus of the adult rat: Agerelated decrease of neuronal progenitor proliferation. J NeuroSci. 1996;16(6):2027-2033. (Pubitemid 26144015)
8. Gould E., Tanapat P., McEwen B.S., Flugge G., Fuchs E. Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. PNAS USA. 1998;95(6):3168-3171. (Pubitemid 28135873)
9. Gould E., Reeves A.J., Fallah M., Tanapat P., Gross C.G., Fuchs E. Hippocampal neurogenesis in adult old world primates. Proc Natl Acad Sci U S A. 1999; 96(9):5263-5267. (Pubitemid 29214571)
10. Eriksson P.S., et al. Neurogenesis in the adult human hippocampus. Nat Med. 1998;4(11):1313-1317. (Pubitemid 28512114)
11. Kornack D.R., Rakic P. Cell proliferation without neurogenesis in adult primate neocortex. Science. 2001;294(5549):2127-2130. (Pubitemid 33150663)
12. Doetsch F., Caille I., Lim D.A., Garcia-Verdugo J.M., Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell. 1999;97(6):703-716. (Pubitemid 29278045)
13. Palmer T.D., Takahashi J., Gage F.H. The adult rat hippocampus contains primordial neural stem cells. Mol Cell Neurosci. 1997;8(6):389-404. (Pubitemid 127796477)
14. Reynolds B.A., Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science. 1992; 255(5052):1707-1710.
15. Lois C., Alvarez-Buylla A. Long-distance neuronal migration in the adult mammalian brain. Science. 1994;264(5162):1145-1148. (Pubitemid 24210676)
16. Rosselli-Austin L., Williams J. Enriched neonatal odor exposure leads to increased numbers of olfactory bulb mitral and granule cells. Brain Res Dev Brain Res. 1990;51(1):135-137. (Pubitemid 20035463)
17. Rochefort C., Gheusi G., Vincent J.D., Lledo P.M. Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J Neurosci. 2002; 22(7):2679-2689. (Pubitemid 37465817)
18. Van Praag H., Kempermann G., Gage F.H. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat NeuroSci. 1999;2(3):266-270. (Pubitemid 30491298)
19. Parent J.M., Yu T.W., Leibowitz R.T., Geschwind D.H., Sloviter R.S., Lowenstein D.H. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci. 1997;17(10):3727-3738. (Pubitemid 27200597)
20. Gould E., Tanapat P. Lesion-induced proliferation of neuronal progenitors in the dentate gyrus of the adult rat. NeuroScience. 1997;80(2):427-436. (Pubitemid 27334592)
21. Liu J., Solway K., Messing R.O., Sharp F.R. Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils. J Neurosci. 1998; 18(19):7768-7778. (Pubitemid 28441018)
22. Shingo T., et al. Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science. 2003;299(5603):117-120. (Pubitemid 36042416)
23. Zhang C.L., Zou Y., He W., Gage F.H., Evans R.M. A role for adult TLX-positive neural stem cells in learning and behaviour. Nature. 2008;451(7181):1004-1007. (Pubitemid 351301727)
24. Shors T.J., Miesegaes G., Beylin A., Zhao M., Rydel T., Gould E. Neurogenesis in the adult is involved in the formation of trace memories. Nature. 2001; 410(6826):372-376. (Pubitemid 32246054)
25. Magavi S.S., Leavitt B.R., Macklis J.D. Induction of neurogenesis in the neocortex of adult mice. Nature. 2000;405(6789):951-955. (Pubitemid 30435051)
26. Nakatomi H., et al. Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell. 2002;110(4):429-441. (Pubitemid 35232287)
27. Barnea A., Nottebohm F. Recruitment and replacement of hippocampal neurons in young and adult chickadees: An addition to the theory of hippocampal learning. Proc Natl Acad Sci U S A. 1996; 93(2):714-718. (Pubitemid 26041155)
28. Gheusi G., Cremer H., McLean H., Chazal G., Vincent J-D, Lledo P-M. Importance of newly generated neurons in the adult olfactory bulb for odor discrimination. Proc Natl Acad Sci U S A. 2000;97(4):1823-1828. (Pubitemid 30118527)
29. Pardal R., Ortega-Saenz P., Duran R., Lopez-Barneo J. Glia-like stem cells sustain physiologic neurogenesis in the adult mammalian carotid body. Cell. 2007;131(2):364-377. (Pubitemid 47576136)
30. Le Douarin N.M. The Neural Crest. Cambridge, Massachusetts, USA: Cambridge University Press; 1999.
31. Morrison S.J., White P.M., Zock C., Anderson D.J. Prospective identification, isolation by flow cytometry, and in vivo self-renewal of multipotent mammalian neural crest stem cells. Cell. 1999;96(5):737-749. (Pubitemid 29122815)
32. Bixby S., Kruger G.M., Mosher J.T., Joseph N.M., Morrison S.J. Cell-intrinsic differences between stem cells from different regions of the peripheral nervous system regulate the generation of neural diversity. Neuron. 2002;35(4):643-656. (Pubitemid 35223025)
33. Kruger G.M., Mosher J.T., Bixby S., Joseph N., Iwashita T., Morrison S.J. Neural crest stem cells persist in the adult gut but undergo changes in self-renewal, neuronal subtype potential, and factor responsiveness. Neuron. 2002;35(4):657-669. (Pubitemid 35223026)
34. Molofsky A.V., Pardal R., Iwashita T., Park I.K., Clarke M.F., Morrison S.J. Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature. 2003;425(6961):962-967. (Pubitemid 37376927)
35. Molofsky A.V., et al. Increasing p16INK4a expression decreases forebrain progenitors and neurogenesis during ageing. Nature. 2006;443(7110):448-452. (Pubitemid 44477280)
36. Bondurand N., Natarajan D., Thapar N., Atkins C., Pachnis V. Neuron and glia generating progenitors of the mammalian enteric nervous system isolated from foetal and postnatal gut cultures. Development. 2003;130(25):6387-6400. (Pubitemid 38016177)
37. Suarez-Rodriguez R., Belkind-Gerson J. Cultured nestin-positive cells from postnatal mouse small bowel differentiate ex vivo into neurons, glia, and smooth muscle. Stem Cells. 2004;22(7):1373-1385. (Pubitemid 39636412)
38. Rauch U., Hansgen A., Hagl C., Holland-Cunz S., Schafer K.H. Isolation and cultivation of neuronal precursor cells from the developing human enteric nervous system as a tool for cell therapy in dysganglionosis. Int J Colorectal Dis. 2006;21(6):554-559. (Pubitemid 44111284)
39. Metzger M., et al. Expansion and differentiation of neural progenitors derived from the human adult enteric nervous system. Gastroenterology. 2009; 137(6):2063-2073.
40. Kondo T., Raff M. Oligodendrocyte precursor cells reprogrammed to become multipotential CNS stem cells. Science. 2000;289(5485):1754-1757.
41. Gabay L., Lowell S., Rubin L.L., Anderson D.J. Deregulation of dorsoventral patterning by FGF confers trilineage differentiation capacity on CNS stem cells in vitro. Neuron. 2003;40(3):485-499. (Pubitemid 37494699)
42. Cracco C., Filogamo G. Mesenteric neurons in the adult rat are responsive to ileal treatment with benzalkonium chloride. Int J Dev Neurosci. 1993; 11(1):49-61. (Pubitemid 23110653)
43. Hanani M., et al. Regeneration of myenteric plexus in the mouse colon after experimental denervation with benzalkonium chloride. J Comp Neurol. 2003;462(3):315-327. (Pubitemid 36736714)
44. Geuna S., Borrione P., Filogamo G. Postnatal histogenesis in the peripheral nervous system. Int J Dev Neurosci. 2002;20(6):475-479. (Pubitemid 35254151)
45. Pham T.D., Gershon M.D., Rothman T.P. Time of origin of neurons in the murine enteric nervous system: Sequence in relation to phenotype. J Comp Neurol. 1991;314(4):789-798.
46. Liu M.T., Kuan Y.H., Wang J., Hen R., Gershon M.D. 5-HT4 receptor-mediated neuroprotection and neurogenesis in the enteric nervous system of adult mice. J Neurosci. 2009;29(31):9683-9699.
47. Stemple D.L., Anderson D.J. Isolation of a stem cell for neurons and glia from the mammalian neural crest. Cell. 1992;71(6):973-985.
48. Molofsky A.V., He S., Bydon M., Morrison S.J., Pardal R. Bmi-1 promotes neural stem cell self-renewal and neural development but not mouse growth and survival by repressing the p16Ink4a and p19Arf senescence pathways. Genes Dev. 2005;19(12):1432-1437. (Pubitemid 41003009)
49. Srinivasan S., Stevens M., Wiley J.W. Diabetic peripheral neuropathy - Evidence for apoptosis and associated mitochondrial dysfunctions. Diabetes. 2000; 49(11):1932-1938.
50. Parr E.J., Sharkey K.A. Multiple mechanisms contribute to myenteric plexus ablation induced by benzalkonium chloride in the guinea-pig ileum. Cell Tissue Res. 1997;289(2):253-264. (Pubitemid 27326649)
51. Bush T.G., et al. Fulminant jejuno-ileitis following ablation of enteric glia in adult transgenic mice. Cell. 1998;93(2):189-201. (Pubitemid 28180853)
52. Zhuo L., Theis M., Alvarez-Maya I., Brenner M., Willecke K., Messing A. hGFAP-cre transgenic mice for manipulation of glial and neuronal function in vivo. Genesis. 2001;31(2):85-94. (Pubitemid 33064319)
53. Hirrlinger P.G., Scheller A., Braun C., Hirrlinger J., Kirchhoff F. Temporal control of gene recombination in astrocytes by transgenic expression of the tamoxifen-inducible DNA recombinase variant CreERT2. Glia. 2006;54(1):11-20. (Pubitemid 43980030)
54. Srinivas S., et al. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol. 2001;1:4.
55. Laranjeira C., et al. Glial cells in the mouse enteric nervous system can undergo neurogenesis in response to injury. J Clin Invest. doi:10.1172/ JCI58200.