Maintenance of the enteric stem cell niche by bacterial lipopolysaccharides? Evidence and perspectives

Journal of Cellular and Molecular Medicine

Volumn 18, Issue 7, 2014, Pages 1429-1443

  Schuster, Anne ^a   Klotz, Markus ^a   Schwab, Tanja ^a   Di Liddo, Rosa ^b   Bertalot, Thomas ^b   Schrenk, Sandra ^a   Martin, Monika ^a   Nguyen, The Duy ^a   Nguyen, Thi Nha Quyen ^a   Gries, Manuela ^c   Faßbender, Klaus ^c   Conconi, Maria Teresa ^b   Parnigotto, Pier Paolo ^d   Schäfer, Karl Herbert ^a,e  

^a UNIVERSITY OF APPLIED SCIENCES KAISERSLAUTERN   (Germany)

^b UNIVERSITY OF PADOVA   (Italy)

^c SAARLAND UNIVERSITY   (Germany)

^d TES Tissue Engineering and Signaling   (Italy)

^e UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Enteric nervous system; Inflammation; LPS; Neural stem progenitor cells; Stem cell niche

Indexed keywords

LIPOPOLYSACCHARIDE; MESSENGER RNA; NESTIN; TLR4 PROTEIN, MOUSE; TOLL LIKE RECEPTOR 4;

ANIMAL; BACTERIUM; BAGG ALBINO MOUSE; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECTS; ENZYME IMMUNOASSAY; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; INTESTINE INNERVATION; METABOLISM; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL NICHE; WESTERN BLOTTING;

ANIMALS; BACTERIA; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; ENTERIC NERVOUS SYSTEM; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOENZYME TECHNIQUES; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED BALB C; NESTIN; NEURAL STEM CELLS; NEUROGENESIS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; STEM CELL NICHE; TOLL-LIKE RECEPTOR 4;

EID: 84904874580     PISSN: 15821838     EISSN: 15824934     Source Type: Journal    
DOI: 10.1111/jcmm.12292     Document Type: Article

References (71)

1. Hagl CI, Heumüller-Klug S, Wink E, et al. The human gastrointestinal tract, a potential autologous neural stem cell source. PLoS ONE. 2013; 8: e72948.
2. Kruger GM, Mosher JT, Bixby S, et al. Neural crest stem cells persist in the adult gut but undergo changes in self-renewal, neuronal subtype potential, and factor responsiveness. Neuron. 2002; 35: 657-69.
3. Heanue TA, Pachnis V. Prospective identification and isolation of enteric nervous system progenitors using Sox2. Stem Cells. 2011; 29: 128-40.
4. Schäfer KH, Van Ginneken C, Copray S. Plasticity and neural stem cells in the enteric nervous system. Anat Rec (Hoboken). 2009; 292: 1940-52.
5. Rauch U, Hänsgen A, Hagl C, et al. 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: 554-9.
6. Metzger M, Caldwell C, Barlow AJ, et al. Enteric nervous system stem cells derived from human gut mucosa for the treatment of aganglionic gut disorders. Gastroenterology. 2009; 136: 2214-25 e1-3.
7. Azan G, Low WC, Wendelschafer-Crabb G, et al. Evidence for neural progenitor cells in the human adult enteric nervous system. Cell Tissue Res. 2011; 344: 217-25.
8. Hagl CI, Klotz M, Wink E, et al. Temporal and regional morphological differences as a consequence of FGF-2 deficiency are mirrored in the myenteric proteome. Pediatr Surg Int. 2007; 24: 49-60.
9. Sharkey KA, Kroese AB. Consequences of intestinal inflammation on the enteric nervous system: neuronal activation induced by inflammatory mediators. Anat Rec. 2001; 262: 79-90.
10. Giaroni C, De Ponti F, Cosentino M, et al. Plasticity in the enteric nervous system. Gastroenterology. 1999; 117: 1438-58.
11. Turrin NP, Gayle D, Ilyin SE, et al. Pro-inflammatory and anti-inflammatory cytokine mRNA induction in the periphery and brain following intraperitoneal administration of bacterial lipopolysaccharide. Brain Res Bull. 2001; 54: 443-53.
12. Shaw KN, Commins S, O'Mara SM. Lipopolysaccharide causes deficits in spatial learning in the watermaze but not in BDNF expression in the rat dentate gyrus. Behav Brain Res. 2001; 124: 47-54.
13. Terrazzino S, Bauleo A, Baldan A, et al. Peripheral LPS administrations up-regulate Fas and FasL on brain microglial cells: a brain protective or pathogenic event? J Neuroimmunol. 2002; 124: 45-53.
14. von Boyen GB, Steinkamp M. Die enterische Glia und neurotrophe Faktoren. Z Gastroenterol. 2006; 44: 985-90.
15. Eggesbo JB, Hjermann I, Lund PK, et al. LPS-induced release of IL-1 beta, IL-6, IL-8, TNF-alpha and sCD14 in whole blood and PBMC from persons with high or low levels of HDL-lipoprotein. Cytokine. 1994; 6: 521-9.
16. Erridge C, Bennett-Guerrero E, Poxton IR. Structure and function of lipopolysaccharides. Microbes Infect. 2002; 4: 837-51.
17. Ekdahl CT. Inflammation is detrimental for neurogenesis in adult brain. PNAS. 2003; 100: 13632-7.
18. Monje ML. Inflammatory blockade restores adult hippocampal neurogenesis. Science. 2003; 302: 1760-5.
19. von Boyen GBT. Proinflammatory cytokines increase glial fibrillary acidic protein expression in enteric glia. Gut. 2004; 53: 222-8.
20. Rumio C, Besusso D, Arnaboldi F, et al. Activation of smooth muscle and myenteric plexus cells of jejunum via toll-like receptor 4. J Cell Physiol. 2006; 208: 47-54.
21. Medert R, Schuster A, Schwarz LK, et al. Spiking rate of myenteric neurons recorded from multi-electrode arrays depending on local microenvironment. Phys Status Solidi (c). 2013; 10: 877-81.
22. Yamaguchi M, Saito H, Suzuki M, et al. Visualization of neurogenesis in the central nervous system using nestin promoter-GFP transgenic mice. NeuroReport. 2000; 11: 1991-6.
23. Schäfer KH, Saffrey MJ, Burnstock G, et al. A new method for the isolation of myenteric plexus from the newborn rat gastrointestinal tract. Brain Res Brain Res Protoc. 1997; 1: 109-13.
24. Schäfer KH, Hagl CI, Rauch U. Differentiation of neurospheres from the enteric nervous system. Pediatr Surg Int. 2003; 19: 340-4.
25. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001; 29: e45.
26. Covacu R, Arvidsson L, Andersson A, et al. TLR activation induces TNF-alpha production from adult neural stem/progenitor cells. J Immunol. 2009; 182: 6889-95.
27. Suárez-Rodríguez 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: 1373-85.
28. Estrada-Mondaca S, Carreón-Rodríguez A, Belkind-Gerson J. Biology of the adult enteric neural stem cell. Dev Dyn. 2007; 236: 20-32.
29. Gage FH. Mammalian neural stem cells. Science. 2000; 287: 1433-8.
30. Shivraj Sohur U, Emsley JG, Mitchell BD, et al. Adult neurogenesis and cellular brain repair with neural progenitors, precursors and stem cells. Philos Trans R Soc B Biol Sci. 2006; 361: 1477-97.
31. Bondurand N. Neuron and glia generating progenitors of the mammalian enteric nervous system isolated from foetal and postnatal gut cultures. Development. 2003; 130: 6387-400.
32. Bondurand N. Maintenance of mammalian enteric nervous system progenitors by SOX10 and endothelin 3 signalling. Development. 2006; 133: 2075-86.
33. Richardson WD, Young KM, Tripathi RB, et al. NG2-glia as multipotent neural stem cells: fact or fantasy? Neuron. 2011; 70: 661-73.
34. Potolicchio I, Carven GJ, Xu X, et al. Proteomic analysis of microglia-derived exosomes: metabolic role of the aminopeptidase CD13 in neuropeptide catabolism. J Immunol. 2005; 175: 2237-43.
35. Paul G, Ozen I, Christophersen NS, et al. The adult human brain harbors multipotent perivascular mesenchymal stem cells. PLoS ONE. 2012; 7: e35577.
36. Chambers I, Colby D, Robertson M, et al. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell. 2003; 113: 643-55.
37. Komitova M, Eriksson PS. Sox-2 is expressed by neural progenitors and astroglia in the adult rat brain. Neurosci Lett. 2004; 369: 24-7.
38. Ruhl A, Franzke S, Collins SM, et al. Interleukin-6 expression and regulation in rat enteric glial cells. Am J Physiol Gastrointest Liver Physiol. 2001; 280: G1163-71.
39. von Boyen GB, Steinkamp M, Geerling I, et al. Proinflammatory cytokines induce neurotrophic factor expression in enteric glia: a key to the regulation of epithelial apoptosis in Crohn's disease. Inflamm Bowel Dis. 2006; 12: 346-54.
40. Barajon I, Serrao G, Arnaboldi F, et al. Toll-like receptors 3, 4, and 7 are expressed in the enteric nervous system and dorsal root ganglia. J Histochem Cytochem. 2009; 57: 1013-23.
41. Schneider J, Jehle EC, Starlinger MJ, et al. Neurotransmitter coding of enteric neurones in the submucous plexus is changed in non-inflamed rectum of patients with Crohn's disease. Neurogastroenterol Motil. 2001; 13: 255-64.
42. Cario E, Podolsky DK. Differential alteration in intestinal epithelial cell expression of toll-like receptor 3 (TLR3) and TLR4 in inflammatory bowel disease. Infect Immun. 2000; 68: 7010-7.
43. Sanai N, Tramontin AD, Quinones-Hinojosa A, et al. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature. 2004; 427: 740-4.
44. Wolf SA, Steiner B, Wengner A, et al. Adaptive peripheral immune response increases proliferation of neural precursor cells in the adult hippocampus. FASEB J. 2009; 23: 3121-8.
45. Ceyhan GO, Demir IE, Rauch U, et al. Pancreatic neuropathy results in "neural remodeling" and altered pancreatic innervation in chronic pancreatitis and pancreatic cancer. Am J Gastroenterol. 2009; 104: 2555-65.
46. Hagl CI, Rauch U, Klotz M, et al. The microenvironment in the Hirschsprung's disease gut supports myenteric plexus growth. Int J Colorectal Dis. 2012; 27: 817-29.
47. von Boyen GBT, Schulte N, Pfluger C, et al. Distribution of enteric glia and GDNF during gut inflammation. BMC Gastroenterol. 2011; 11: 3.
48. Villanacci V, Bassotti G, Nascimbeni R, et al. Enteric nervous system abnormalities in inflammatory bowel diseases. Neurogastroenterol Motil. 2008; 20: 1009-16.
49. Bernardini N, Segnani C, Ippolito C, et al. Immunohistochemical analysis of myenteric ganglia and interstitial cells of Cajal in ulcerative colitis. J Cell Mol Med. 2012; 16: 318-27.
50. da Silveira AB, Freitas MA, de Oliveira EC, et al. Glial fibrillary acidic protein and S-100 colocalization in the enteroglial cells in dilated and nondilated portions of colon from chagasic patients. Hum Pathol. 2009; 40: 244-51.
51. Kriegstein A, Alvarez-Buylla A. The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci. 2009; 32: 149-84.
52. Joseph NM, He S, Quintana E, et al. Enteric glia are multipotent in culture but primarily form glia in the adult rodent gut. J Clin Invest. 2011; 121: 3398-411.
53. Anitha M, Vijay-Kumar M, Sitaraman SV, et al. Gut microbial products regulate murine gastrointestinal motility via Toll-like receptor 4 signaling. Gastroenterology. 2012; 143: 1006-16.
54. Gomes FC, Paulin D, Moura Neto V. Glial fibrillary acidic protein (GFAP): modulation by growth factors and its implication in astrocyte differentiation. Braz J Med Biol Res. 1999; 32: 619-31.
55. Menezes JR, Luskin MB. Expression of neuron-specific tubulin defines a novel population in the proliferative layers of the developing telencephalon. J Neurosci. 1994; 14: 5399-416.
56. Liu MT, Kuan YH, Wang J, et al. 5-HT4 receptor-mediated neuroprotection and neurogenesis in the enteric nervous system of adult mice. J Neurosci. 2009; 29: 9683-99.
57. Kim J, Lo L, Dormand E, et al. SOX10 maintains multipotency and inhibits neuronal differentiation of neural crest stem cells. Neuron. 2003; 38: 17-31.
58. Schneider A, Krüger C, Steigleder T, et al. The hematopoietic factor G-CSF is a neuronal ligand that counteracts programmed cell death and drives neurogenesis. J Clin Invest. 2005; 115: 2083-98.
59. Schuster A, Schwab T, Lilischkis R, et al. Neurogenesis: granulocyte colony-stimulating factor facilitates neural stem cell differentiation. Neurogastroenterol Motil. 2012; 24: 46.
60. Kahn MA, De Vellis J. Regulation of an oligodendrocyte progenitor cell line by the interleukin-6 family of cytokines. Glia. 1994; 12: 87-98.
61. Wagner JA. Is IL-6 both a cytokine and a neurotrophic factor? J Exp Med. 1996; 183: 2417-9.
62. Schäfer KH, Mestres P, Marz P, et al. The IL-6/sIL-6R fusion protein hyper-IL-6 promotes neurite outgrowth and neuron survival in cultured enteric neurons. J Interferon Cytokine Res. 1999; 19: 527-32.
63. Go HS, Shin CY, Lee SH, et al. Increased proliferation and gliogenesis of cultured rat neural progenitor cells by lipopolysaccharide-stimulated astrocytes. NeuroImmunoModulation. 2009; 16: 365-76.
64. Ohbayashi N, Ikeda O, Taira N, et al. LIF- and IL-6-induced acetylation of STAT3 at Lys-685 through PI3K/Akt activation. Biol Pharm Bull. 2007; 30: 1860-4.
65. Levy DE, Lee CK. What does Stat3 do? J Clin Invest. 2002; 109: 1143-8.
66. Suzuki A, Raya A, Kawakami Y, et al. Nanog binds to Smad1 and blocks bone morphogenetic protein-induced differentiation of embryonic stem cells. Proc Natl Acad Sci USA. 2006; 103: 10294-9.
67. Gough NM, Williams RL, Hilton DJ, et al. LIF: a molecule with divergent actions on myeloid leukaemic cells and embryonic stem cells. Reprod Fertil Dev. 1989; 1: 281-8.
68. Lintz M, Booz KH, Schäfer KH. Combined effect of various neurotrophic factors upon dissociated rat myenteric plexus in vitro. Neurosci Res Commun. 1999; 25: 89-96.
69. Hagl C, Heumüller S, Wink E, et al. The appendix, a suitable and autologeous neural stem cell source. Neurogastroenterol Motil. 2012; 24: 24.
70. Hagl CI, Heumüller S, Klotz M, et al. Smooth muscle proteins from Hirschsprung's disease facilitates stem cell differentiation. Pediatr Surg Int. 2011; 28: 135-42.
71. Almond S, Lindley RM, Kenny SE, et al. Characterisation and transplantation of enteric nervous system progenitor cells. Gut. 2007; 56: 489-96.