In Vivo transplantation of neurosphere-like bodies derived from the human postnatal and adult enteric nervous system: A pilot study

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Hetz, Susan ^a,b   Acikgoez, Ali ^c   Voss, Ulrike ^a   Nieber, Karen ^a   Holland, Heidrun ^a   Hegewald, Cindy ^a   Till, Holger ^d   Metzger, Roman ^e   Metzger, Marco ^a,f  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b FRAUNHOFER INSTITUTE FOR CELL THERAPY AND IMMUNOLOGY   (Germany)

^c Klinikum St Georg   (Germany)

^d MEDICAL UNIVERSITY OF GRAZ   (Austria)

^e Salzburg County Hospital   (Austria)

^f FRAUNHOFER INSTITUTE FOR INTERFACIAL ENGINEERING AND BIOTECHNOLOGY IGB   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BENZALKONIUM CHLORIDE; GLIAL FIBRILLARY ACIDIC PROTEIN; NITRIC OXIDE SYNTHASE; SERUM AMYLOID P; SMOOTH MUSCLE ACTIN; PRIMER DNA;

ADULT STEM CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL TRANSPLANTATION; CONTROLLED STUDY; ELECTROSTIMULATION; FLUORESCENCE IN SITU HYBRIDIZATION; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPERTROPHY; HYPOGANGLIONOSIS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; IN VIVO STUDY; INTESTINE CELL; MOUSE; NERVE CELL; NEURAL STEM CELL; NEUROLOGIC DISEASE; NEUROSPHERE LIKE BODY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PILOT STUDY; POLYMERASE CHAIN REACTION; TELOMERE; ADOLESCENT; ADULT; AGED; ANIMAL; CHILD; CYTOLOGY; FEMALE; INFANT; INTESTINE INNERVATION; MALE; MIDDLE AGED; VERY ELDERLY; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ANIMALS; BASE SEQUENCE; CELL TRANSPLANTATION; CHILD; DNA PRIMERS; ENTERIC NERVOUS SYSTEM; FEMALE; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; INFANT; MALE; MICE; MIDDLE AGED; PILOT PROJECTS; POLYMERASE CHAIN REACTION; YOUNG ADULT;

EID: 84899435238     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0093605     Document Type: Article

References (46)

1. De GR, Guerrini S, Barbara G, Cremon C, Stanghellini V, et al. (2004) New insights into human enteric neuropathies. Neurogastroenterol Motil 16 Suppl 1: 143-7.: 143-147.
2. Di NG, Blandizzi C, Volta U, Colucci R, Stanghellini V, et al. (2008) Review article: molecular, pathological and therapeutic features of human enteric neuropathies. Aliment Pharmacol Ther 28: 25-42. (Pubitemid 351782813)
3. Micci MA, Pasricha PJ (2007) Neural stem cells for the treatment of disorders of the enteric nervous system: strategies and challenges. Dev Dyn 236: 33-43. 10.1002/dvdy.20975 [doi]. (Pubitemid 46095077)
4. Hotta R, Natarajan D, Burns AJ, Thapar N (2011) Stem cells for GI motility disorders. Curr Opin Pharmacol 11: 617-623. S1471-4892(11)00171-8 [pii]; 10.1016/j.coph.2011.09.004 [doi].
5. Kulkarni S, Becker L, Pasricha PJ (2012) Stem cell transplantation in neurodegenerative disorders of the gastrointestinal tract: future or fiction? Gut 61: 613-621. gut.2010.235614 [pii]; 10.1136/gut.2010.235614 [doi].
6. Hotta R, Natarajan D, Thapar N (2009) Potential of cell therapy to treat pediatric motility disorders. Semin Pediatr Surg 18: 263-273. S1055-8586(09)00046-8 [pii]; 10.1053/j.sempedsurg.2009.07.008 [doi].
7. Gershon MD (2007) Transplanting the enteric nervous system: a step closer to treatment for aganglionosis. Gut 56: 459-461. 56/4/459 [pii]; 10.1136/gut.2006.107748 [doi].
8. Schafer KH, Micci MA, Pasricha PJ (2009) Neural stem cell transplantation in the enteric nervous system: roadmaps and roadblocks. Neurogastroenterol Motil 21: 103-112. NMO1257 [pii]; 10.1111/j.1365-2982.2008.01257.x [doi].
9. Estrada-Mondaca S, Carreon-Rodriguez A, Belkind-Gerson J (2007) Biology of the adult enteric neural stem cell. Dev Dyn 236: 20-32. 10.1002/dvdy.20954 [doi]. (Pubitemid 46095076)
10. Burns AJ, Pasricha PJ, Young HM (2004) Enteric neural crest-derived cells and neural stem cells: biology and therapeutic potential. Neurogastroenterol Motil 16 Suppl 1: 3-7. 10.1111/j.1743-3150.2004.00466.x [doi];NMO466 [pii].
11. Young HM (2005) Neural stem cell therapy and gastrointestinal biology. Gastroenterology 129: 2092-2095. S0016-5085(05)02192-X [pii]; 10.1053/j.gastro.2005.10.033 [doi].
12. Metzger M (2010) Neurogenesis in the enteric nervous system. Arch Ital Biol 148: 73-83.
13. Geisbauer CL, Wu BM, Dunn JC (2012) Transplantation of enteric cells into the aganglionic rodent small intestines. J Surg Res 176: 20-28. S0022-4804(11)00453-7 [pii]; 10.1016/j.jss.2011.05.014 [doi].
14. Pan WK, Zheng BJ, Gao Y, Qin H, Liu Y (2011) Transplantation of neonatal gut neural crest progenitors reconstructs ganglionic function in benzalkonium chloride-treated homogenic rat colon. J Surg Res 167: e221-e230. S0022-4804(11)00013-8 [pii]; 10.1016/j.jss.2011.01.016 [doi].
15. Tsai YH, Murakami N, Gariepy CE (2011) Postnatal intestinal engraftment of prospectively selected enteric neural crest stem cells in a rat model of Hirschsprung disease. Neurogastroenterol Motil 23: 362-369. 10.1111/j.1365-2982. 2010.01656.x [doi].
16. Martucciello G, Brizzolara A, Favre A, Lombardi L, Bocciardi R, et al. (2007) Neural crest neuroblasts can colonise aganglionic and ganglionic gut in vivo. Eur J Pediatr Surg 17: 34-40. 10.1055/s-2007-964952 [doi]. (Pubitemid 47262136)
17. Anitha M, Joseph I, Ding X, Torre ER, Sawchuk MA, et al. (2008) Characterization of fetal and postnatal enteric neuronal cell lines with improvement in intestinal neural function. Gastroenterology 134: 1424-1435. (Pubitemid 351615361)
18. Hanani M, Ledder O, Yutkin V, Abu-Dalu R, Huang TY, et al. (2003) Regeneration of myenteric plexus in the mouse colon after experimental denervation with benzalkonium chloride. J Comp Neurol 462: 315-327. (Pubitemid 36736714)
19. Dong YL, Liu W, Gao YM, Wu RD, Zhang YH, et al. (2008) Neural stem cell transplantation rescues rectum function in the aganglionic rat. Transplant Proc 40: 3646-3652.
20. Metzger M, Bareiss PM, Danker T, Wagner S, Hennenlotter J, et al. (2009) Expansion and differentiation of neural progenitors derived from the human adult enteric nervous system. Gastroenterology 137: 2063-2073.
21. Hegewald C, Alt R, Hetz S, Cross M, Acikgoez A, et al. (2011) Reduced oxygen stress promotes propagation of murine postnatal enteric neural progenitors in vitro. Neurogastroenterol Motil 23: e412-e424. 10.1111/j.1365-2982.2011.01761.x [doi].
22. Holland H, Ahnert P, Koschny R, Kirsten H, Bauer M, et al. (2012) Detection of novel genomic aberrations in anaplastic astrocytomas by GTG-banding, SKY, locus-specific FISH, and high density SNP-array. Pathol Res Pract 208: 325-330. S0344-0338(12)00102-1 [pii]; 10.1016/j.prp.2012.03.010 [doi].
23. Just L, Timmer M, Tinius J, Stahl F, Deiwick A, et al. (2003) Identification of human cells in brain xenografts and in neural co-cultures of rat by in situ hybridisation with Alu probe. J Neurosci Methods 126: 69-77. S0165027003000657 [pii].
24. Wallace AS, Barlow AJ, Navaratne L, Delalande JM, Tauszig-Delamasure S, et al. (2009) Inhibition of cell death results in hyperganglionosis: implications for enteric nervous system development. Neurogastroenterol Motil 21: 768-e49. NMO1309 [pii]; 10.1111/j.1365-2982.2009.01309.x [doi].
25. Brothman AR, Persons DL, Shaffer LG (2009) Nomenclature evolution: Changes in the ISCN from the 2005 to the 2009 edition. Cytogenet Genome Res 127: 1-4. 000279442 [pii]; 10.1159/000279442 [doi].
26. 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. (Pubitemid 36043638)
27. Heanue TA, Pachnis V (2011) Prospective identification and isolation of enteric nervous system progenitors using Sox2. Stem Cells 29: 128-140. 10.1002/stem.557 [doi].
28. Kruger GM, Mosher JT, Bixby S, Joseph N, Iwashita T, et al. (2002) Neural crest stem cells persist in the adult gut but undergo changes in self-renewal, neuronal subtype potential, and factor responsiveness. Neuron 35: 657-669. (Pubitemid 35223026)
29. 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. 10.1007/s00441-011-1130-9 [doi].
30. Cracco C, Filogamo G (1997) Neuronal and non-neuronal plasticity in the rat following myenteric denervation. Adv Exp Med Biol 429: 159-69.: 159-169.
31. Poli E, Lazzaretti M, Grandi D, Pozzoli C, Coruzzi G (2001) Morphological and functional alterations of the myenteric plexus in rats with TNBS-induced colitis. Neurochem Res 26: 1085-1093. (Pubitemid 33021434)
32. 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. (Pubitemid 38016177)
33. Silva AT, Wardhaugh T, Dolatshad NF, Jones S, Saffrey MJ (2008) Neural progenitors from isolated postnatal rat myenteric ganglia: expansion as neurospheres and differentiation in vitro. Brain Res 1218: 47-53. S0006-8993(08)00979-7 [pii]; 10.1016/j.brainres.2008.04.051 [doi].
34. Suarez-Rodriguez 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. (Pubitemid 39636412)
35. 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.
36. Rauch U, Hansgen A, Hagl C, Holland-Cunz S, Schafer 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. (Pubitemid 44111284)
37. Almond S, Lindley RM, Kenny SE, Connell MG, Edgar DH (2007) Characterisation and transplantation of enteric nervous system progenitor cells. Gut 56: 489-496. (Pubitemid 46580503)
38. Lindley RM, Hawcutt DB, Connell MG, Almond SN, Vannucchi MG, et al. (2008) Human and mouse enteric nervous system neurosphere transplants regulate the function of aganglionic embryonic distal colon. Gastroenterology 135: 205-216.
39. 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.
40. Thapar N (2009) New frontiers in the treatment of Hirschsprung disease. J Pediatr Gastroenterol Nutr 48 Suppl 2: S92-4.: S92-S94.
41. Amiel J, Lyonnet S (2001) Hirschsprung disease, associated syndromes, and genetics: a review. J Med Genet 38: 729-739. (Pubitemid 33032927)
42. Suslov ON, Kukekov VG, Ignatova TN, Steindler DA (2002) Neural stem cell heterogeneity demonstrated by molecular phenotyping of clonal neurospheres. Proc Natl Acad Sci U S A 99: 14506-14511. 10.1073/pnas.212525299 [doi]; 212525299 [pii].
43. Singec I, Knoth R, Meyer RP, Maciaczyk J, Volk B, et al. (2006) Defining the actual sensitivity and specificity of the neurosphere assay in stem cell biology. Nat Methods 3: 801-806. nmeth926 [pii]; 10.1038/nmeth926 [doi].
44. Hanani M, Ledder O, Yutkin V, Abu-Dalu R, Huang TY, et al. (2003) Regeneration of myenteric plexus in the mouse colon after experimental denervation with benzalkonium chloride. J Comp Neurol 462: 315-327. 10.1002/cne.10721 [doi]. (Pubitemid 36736714)
45. Liu W, Wu RD, Dong YL, Gao YM (2007) Neuroepithelial stem cells differentiate into neuronal phenotypes and improve intestinal motility recovery after transplantation in the aganglionic colon of the rat. Neurogastroenterol Motil 19: 1001-1009. (Pubitemid 350198316)
46. Hotta R, Anderson RB, Kobayashi K, Newgreen DF, Young HM (2010) Effects of tissue age, presence of neurones and endothelin-3 on the ability of enteric neurone precursors to colonize recipient gut: implications for cell-based therapies. Neurogastroenterol Motil 22: 331-e86. NMO1411 [pii]; 10.1111/j.1365-2982.2009.01411.x [doi].