Adult enteric nervous system in health is maintained by a dynamic balance between neuronal apoptosis and neurogenesis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 114, Issue 18, 2017, Pages E3709-E3718

  Kulkarni, Subhash ^a   Micci, Maria Adelaide ^b   Leser, Jenna ^a   Shin, Changsik ^c   Tang, Shiue Cheng ^d   Fu, Ya Yuan ^a   Liu, Liansheng ^a   Li, Qian ^a   Saha, Monalee ^a   Li, Cuiping ^a   Enikolopov, Grigori ^e,f   Becker, Laren ^g   Rakhilin, Nikolai ^h,i   Anderson, Michael ^a   Shen, Xiling ^h,i   Dong, Xinzhong ^a   Butte, Manish J ^j   Song, Hongjun ^a   Southard Smith, E Michelle ^k   Kapur, Raj P ^l   Bogunovic, Milena ^c   Pasricha, Pankaj J ^a   more..

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b University of Texas Medical Branch School of Medicine   (United States)

^c PENN STATE COLLEGE OF MEDICINE   (United States)

^d NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^e Simons Center for Quantitative Biology   (United States)

^f STONY BROOK UNIVERSITY   (United States)

^g STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h Duke University   (United States)

ⁱ Cornell University   (United States)

^j UNIVERSITY OF CALIFORNIA   (United States)

^k VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^l SEATTLE CHILDREN S HOSPITAL   (United States)

more..

Author keywords

Adult neurogenesis; Enteric neural precursor cells; Enteric neurons; Nestin; Neuronal apoptosis

Indexed keywords

NESTIN; NERVE GROWTH FACTOR RECEPTOR; NES PROTEIN, MOUSE; SOX10 PROTEIN, MOUSE; TNFRSF16 PROTEIN, MOUSE; TRANSCRIPTION FACTOR SOX;

APOPTOSIS; ARTICLE; CELL DIVISION; CELL FUNCTION; CELL LOSS; CELL PROLIFERATION; GANGLION; GANGLIONEUROMA; GLIA; HOMEOSTASIS; HUMAN; IN VITRO STUDY; INTESTINE INNERVATION; MACROPHAGE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; PHENOTYPE; PRIORITY JOURNAL; SMALL INTESTINE; STEM CELL; TURNOVER TIME; ANIMAL; GENETICS; METABOLISM; MOUSE; TRANSGENIC MOUSE;

ANIMALS; APOPTOSIS; ENTERIC NERVOUS SYSTEM; HUMANS; MICE; MICE, TRANSGENIC; NESTIN; NEUROGENESIS; RECEPTORS, NERVE GROWTH FACTOR; SOXE TRANSCRIPTION FACTORS;

EID: 85018784856     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1619406114     Document Type: Article

References (75)

1. Furness JB (2012) The enteric nervous system and neurogastroenterology. Nat Rev Gastroenterol Hepatol 9:286-294.
2. Ouyang A, Locke GR, 3rd (2007) Overview of neurogastroenterology-gastrointestinal motility and functional GI disorders: Classification, prevalence, and epidemiology. Gastroenterol Clin North Am 36:485-498, vii.
3. Mazzuoli-Weber G, Schemann M (2015) Mechanosensitivity in the enteric nervous system. Front Cell Neurosci 9:408.
4. Anitha M, et al. (2016) Intestinal dysbiosis contributes to the delayed gastrointestinal transit in high-fat diet fed mice. Cell Mol Gastroenterol Hepatol 2:328-339.
5. Gabella G (1971) Neuron size and number in the myenteric plexus of the newborn and adult rat. J Anat 109:81-95.
6. Thrasivoulou C, et al. (2006) Reactive oxygen species, dietary restriction and neurotrophic factors in age-related loss of myenteric neurons. Aging Cell 5:247-257.
7. Joseph NM, et al. (2011) Enteric glia are multipotent in culture but primarily form glia in the adult rodent gut. J Clin Invest 121:3398-3411.
8. Laranjeira C, et al. (2011) Glial cells in the mouse enteric nervous system can undergo neurogenesis in response to injury. J Clin Invest 121:3412-3424.
9. Liu MT, Kuan YH, Wang J, Hen R, Gershon MD (2009) 5-HT4 receptor-mediated neuroprotection and neurogenesis in the enteric nervous system of adult mice. J Neurosci 29:9683-9699.
10. Pham TD, Gershon MD, Rothman TP (1991) Time of origin of neurons in the murine enteric nervous system: Sequence in relation to phenotype. J Comp Neurol 314:789-798.
11. Almond S, Lindley RM, Kenny SE, Connell MG, Edgar DH (2007) Characterisation and transplantation of enteric nervous system progenitor cells. Gut 56:489-496.
12. Becker L, Kulkarni S, Tiwari G, Micci MA, Pasricha PJ (2012) Divergent fate and origin of neurosphere-like bodies from different layers of the gut. Am J Physiol Gastrointest Liver Physiol 302:G958-G965.
13. Bixby S, Kruger GM, Mosher JT, Joseph NM, Morrison SJ (2002) Cell-intrinsic differences between stem cells from different regions of the peripheral nervous system regulate the generation of neural diversity. Neuron 35:643-656.
14. Bondurand N, Natarajan D, Thapar N, Atkins C, Pachnis V (2003) Neuron and glia generating progenitors of the mammalian enteric nervous system isolated from foetal and postnatal gut cultures. Development 130:6387-6400.
15. Heanue TA, Pachnis V (2010) Prospective identification and isolation of enteric nervous system progenitors using SOX2. Stem Cells 29:128-40.
16. Lo L, Anderson DJ (1995) Postmigratory neural crest cells expressing c-RET display restricted developmental and proliferative capacities. Neuron 15:527-539.
17. Metzger M (2010) Neurogenesis in the enteric nervous system. Arch Ital Biol 148: 73-83.
18. Metzger M, et al. (2009) Expansion and differentiation of neural progenitors derived from the human adult enteric nervous system. Gastroenterology 137: 2063-2073 e2064.
19. Metzger M, Caldwell C, Barlow AJ, Burns AJ, Thapar N (2009) Enteric nervous system stem cells derived from human gut mucosa for the treatment of aganglionic gut disorders. Gastroenterology 136:2214-2225.e1-3.
20. Natarajan D, Grigoriou M, Marcos-Gutierrez CV, Atkins C, Pachnis V (1999) Multipotential progenitors of the mammalian enteric nervous system capable of colonising aganglionic bowel in organ culture. Development 126:157-168.
21. Rauch U, Hänsgen A, Hagl C, Holland-Cunz S, Schäfer KH (2006) 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 21:554-559.
22. Suárez-Rodríguez R, Belkind-Gerson J (2004) Cultured nestin-positive cells from postnatal mouse small bowel differentiate ex vivo into neurons, glia, and smooth muscle. Stem Cells 22:1373-1385.
23. Schäfer KH, Hagl CI, Rauch U (2003) Differentiation of neurospheres from the enteric nervous system. Pediatr Surg Int 19:340-344.
24. Puig I, et al. (2009) Deletion of Pten in the mouse enteric nervous system induces ganglioneuromatosis and mimics intestinal pseudoobstruction. J Clin Invest 119: 3586-3596.
25. Sanno H, et al. (2010) Control of postnatal apoptosis in the neocortex by RhoAsubfamily GTPases determines neuronal density. J Neurosci 30:4221-4231.
26. Nezami BG, et al. (2014) MicroRNA 375 mediates palmitate-induced enteric neuronal damage and high-fat diet-induced delayed intestinal transit in mice. Gastroenterology 146:473-483 e473.
27. Becker L, et al. (2017) Age-dependent shift in macrophage polarisation causes inflammation-mediated degeneration of enteric nervous system. Gut, 10.1136/gutjnl-2016-312940.
28. Hristov G, et al. (2014) SHOX triggers the lysosomal pathway of apoptosis via oxidative stress. Hum Mol Genet 23:1619-1630.
29. Hussain ST, Attilo A, Bigotte L, Cesarini K, Olsson Y (1985) Cytofluorescence localization of propidium iodide injected intravenously into the nervous system of the mouse. Acta Neuropathol 66:62-67.
30. Unal Cevik I, Dalkara T (2003) Intravenously administered propidium iodide labels necrotic cells in the intact mouse brain after injury. Cell Death Differ 10:928-929.
31. Brana C, Benham C, Sundstrom L (2002) A method for characterising cell death in vitro by combining propidium iodide staining with immunohistochemistry. Brain Res Brain Res Protoc 10:109-114.
32. Rakhilin N, et al. (2016) Simultaneous optical and electrical in vivo analysis of the enteric nervous system. Nat Commun 7:11800.
33. Margolis KG, Gershon MD, Bogunovic M (2016) Cellular organization of neuroimmune interactions in the gastrointestinal tract. Trends Immunol 37:487-501.
34. Muller PA, et al. (2014) Crosstalk between muscularis macrophages and enteric neurons regulates gastrointestinal motility. Cell 158:300-313.
35. Gautron L, et al. (2013) Neuronal and nonneuronal cholinergic structures in the mouse gastrointestinal tract and spleen. J Comp Neurol 521:3741-3767.
36. Heng TS, Painter MW; Immunological Genome Project Consortium (2008) The Immunological Genome Project: Networks of gene expression in immune cells. Nat Immunol 9:1091-1094.
37. Steinert PM, et al. (1999) A high molecular weight intermediate filament-associated protein in BHK-21 cells is Nestin, a type VI intermediate filament protein. Limited coassembly in vitro to form heteropolymers with type III vimentin and type IV alphainternexin. J Biol Chem 274:9881-9890.
38. Mignone JL, et al. (2007) Neural potential of a stem cell population in the hair follicle. Cell Cycle 6:2161-2170.
39. Mignone JL, Kukekov V, Chiang AS, Steindler D, Enikolopov G (2004) Neural stem and progenitor cells in nestin-GFP transgenic mice. J Comp Neurol 469:311-324.
40. Becker L, Peterson J, Kulkarni S, Pasricha PJ (2013) Ex vivo neurogenesis within enteric ganglia occurs in a PTEN dependent manner. PLoS One 8:e59452.
41. Birbrair A, Wang ZM, Messi ML, Enikolopov GN, Delbono O (2011) Nestin-GFP transgene reveals neural precursor cells in adult skeletal muscle. PLoS One 6:e16816.
42. Bonaguidi MA, et al. (2011) In vivo clonal analysis reveals self-renewing and multipotent adult neural stem cell characteristics. Cell 145:1142-1155.
43. Fu YY, Peng SJ, Lin HY, Pasricha PJ, Tang SC (2013) 3-D imaging and illustration of mouse intestinal neurovascular complex. Am J Physiol Gastrointest Liver Physiol 304: G1-G11.
44. Corpening JC, et al. (2011) Isolation and live imaging of enteric progenitors based on Sox10-Histone2BVenus transgene expression. Genesis 49:599-618.
45. Uesaka T, Nagashimada M, Enomoto H (2015) Neuronal differentiation in Schwann cell lineage underlies postnatal neurogenesis in the enteric nervous system. J Neurosci 35:9879-9888.
46. Wilm B, Ipenberg A, Hastie ND, Burch JB, Bader DM (2005) The serosal mesothelium is a major source of smooth muscle cells of the gut vasculature. Development 132: 5317-5328.
47. Shimada A, Shibata T, Komatsu K, Nifuji A (2008) Improved methods for immunohistochemical detection of BrdU in hard tissue. J Immunol Methods 339:11-16.
48. Kimoto M, Yura Y, Kishino M, Toyosawa S, Ogawa Y (2008) Label-retaining cells in the rat submandibular gland. J Histochem Cytochem 56:15-24.
49. 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.
50. Rao M, et al. (2015) Enteric glia express proteolipid protein 1 and are a transcriptionally unique population of glia in the mammalian nervous system. Glia 63: 2040-2057.
51. Azan G, Low WC, Wendelschafer-Crabb G, Ikramuddin S, Kennedy WR (2011) Evidence for neural progenitor cells in the human adult enteric nervous system. Cell Tissue Res 344:217-225.
52. Lindley RM, et al. (2008) Human and mouse enteric nervous system neurosphere transplants regulate the function of aganglionic embryonic distal colon. Gastroenterology 135:205-216.e6.
53. Hotta R, et al. (2013) Transplanted progenitors generate functional enteric neurons in the postnatal colon. J Clin Invest 123:1182-1191.
54. Belkind-Gerson J, et al. (2015) Colitis induces enteric neurogenesis through a 5-HT4-dependent mechanism. Inflamm Bowel Dis 21:870-878.
55. Cook RD, Burnstock G (1976) The altrastructure of Auerbach's plexus in the guineapig. I. Neuronal elements. J Neurocytol 5:171-194.
56. Anitha M, et al. (2006) GDNF rescues hyperglycemia-induced diabetic enteric neuropathy through activation of the PI3K/Akt pathway. J Clin Invest 116:344-356.
57. Gianino S, Grider JR, Cresswell J, Enomoto H, Heuckeroth RO (2003) GDNF availability determines enteric neuron number by controlling precursor proliferation. Development 130:2187-2198.
58. Stenkamp-Strahm CM, Kappmeyer AJ, Schmalz JT, Gericke M, Balemba O (2013) Highfat diet ingestion correlates with neuropathy in the duodenum myenteric plexus of obese mice with symptoms of type 2 diabetes. Cell Tissue Res 354:381-394.
59. Kristiansen M, Ham J (2014) Programmed cell death during neuronal development: The sympathetic neuron model. Cell Death Differ 21:1025-1035.
60. Gershon MD (2011) Behind an enteric neuron there may lie a glial cell. J Clin Invest 121:3386-3389.
61. Taylor CR, Montagne WA, Eisen JS, Ganz J (2016) Molecular fingerprinting delineates progenitor populations in the developing zebrafish enteric nervous system. Dev Dyn 245:1081-1096.
62. Bai X, et al. (2013) Genetic background affects human glial fibrillary acidic protein promoter activity. PLoS One 8:e66873.
63. Mandyam CD, Harburg GC, Eisch AJ (2007) Determination of key aspects of precursor cell proliferation, cell cycle length and kinetics in the adult mouse subgranular zone. Neuroscience 146:108-122.
64. Gabella G (1989) Fall in the number of myenteric neurons in aging guinea pigs. Gastroenterology 96:1487-1493.
65. Garcia SB, et al. (2002) No reduction with ageing of the number of myenteric neurons in benzalkonium chloride treated rats. Neurosci Lett 331:66-68.
66. Spencer NJ (2016) Motility patterns in mouse colon: Gastrointestinal dysfunction induced by anticancer chemotherapy. Neurogastroenterol Motil 28:1759-1764.
67. Ro S, Hwang SJ, MutoM, Jewett WK, Spencer NJ (2006) Anatomic modifications in the enteric nervous system of piebald mice and physiological consequences to colonic motor activity. Am J Physiol Gastrointest Liver Physiol 290:G710-G718.
68. Kabouridis PS, et al. (2015) Microbiota controls the homeostasis of glial cells in the gut lamina propria. Neuron 85:289-295.
69. Crosnier C, Stamataki D, Lewis J (2006) Organizing cell renewal in the intestine: Stem cells, signals and combinatorial control. Nat Rev Genet 7:349-359.
70. McQuade RM, et al. (2016) Gastrointestinal dysfunction and enteric neurotoxicity following treatment with anticancer chemotherapeutic agent 5-fluorouracil. Neurogastroenterol Motil 28:1861-1875.
71. Soares A, Beraldi EJ, Ferreira PE, Bazotte RB, Buttow NC (2015) Intestinal and neuronal myenteric adaptations in the small intestine induced by a high-fat diet in mice. BMC Gastroenterol 15:3.
72. Molofsky AV, et al. (2006) Increasing p16INK4a expression decreases forebrain progenitors and neurogenesis during ageing. Nature 443:448-452.
73. Gown AM, Willingham MC (2002) Improved detection of apoptotic cells in archival paraffin sections: Immunohistochemistry using antibodies to cleaved caspase 3. J Histochem Cytochem 50:449-454.
74. Shirasawa S, et al. (1997) Enx (Hox11L1)-deficient mice develop myenteric neuronal hyperplasia and megacolon. Nat Med 3:646-650.
75. Kuo YM, et al. (2010) Extensive enteric nervous system abnormalities in mice transgenic for artificial chromosomes containing Parkinson disease-associated alphasynuclein gene mutations precede central nervous system changes. Hum Mol Genet 19:1633-1650.