Enteric neuroplasticity in seawater-adapted European eel (Anguilla anguilla)

Journal of Anatomy

Volumn 224, Issue 2, 2014, Pages 180-191

  Sorteni, C ^a   Clavenzani, P ^a   De Giorgio, R ^a   Portnoy, O ^a   Sirri, R ^b   Mordenti, O ^b   Di Biase, A ^b   Parmeggiani, A ^b   Menconi, V ^a   Chiocchetti, R ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

Enteric neuroplasticity; Immunohistochemistry; Neurogenesis; Neuronal migration

Indexed keywords

FRESH WATER; HYPOPHYSIS EXTRACT; SEA WATER;

ADAPTATION; ANGUILLA ANGUILLA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTONOMIC NERVOUS SYSTEM; CELL DENSITY; CELL SIZE; CONTROLLED STUDY; FEMALE; GLIA CELL; HABITAT; HOMEOSTASIS; IMMUNOHISTOCHEMISTRY; INTESTINE CELL; INTESTINE INNERVATION; LAGOON; MALE; MYENTERIC PLEXUS; NERVE CELL PLASTICITY; NONHUMAN; POPULATION MIGRATION; PRIORITY JOURNAL; SALINITY; SALT STRESS; SEXUAL MATURITY; STARVATION;

ANGUILLA ANGUILLA; ANGUILLIDAE; CYPRINIDAE;

ENTERIC NEUROPLASTICITY; IMMUNOHISTOCHEMISTRY; NEUROGENESIS; NEURONAL MIGRATION;

ACCLIMATIZATION; ADAPTATION, PHYSIOLOGICAL; ANGUILLA; ANIMAL MIGRATION; ANIMALS; CRYOULTRAMICROTOMY; ENTERIC NERVOUS SYSTEM; FEMALE; FRESH WATER; IMMUNOHISTOCHEMISTRY; INTESTINES; LIFE CYCLE STAGES; MALE; MUSCLE, SMOOTH; NEUROGLIA; NEURONAL PLASTICITY; NEURONS; SEAWATER;

EID: 84892541884     PISSN: 00218782     EISSN: 14697580     Source Type: Journal    
DOI: 10.1111/joa.12131     Document Type: Article

References (61)

1. Akamatsu W, Okano HJ, Osumi N, et al. (1999) Mammalian ELAV-like neuronal RNA-binding proteins HuB and HuC promote neuronal development in both the central and the peripheral nervous systems. Proc Natl Acad Sci U S A 96, 9885-9890.
2. Akamatsu W, Fujihara H, Mitsuhashi T, et al. (2005) The RNA-binding protein HuD regulates neuronal cell identity and maturation. Proc Natl Acad Sci U S A 102, 4625-4630.
3. Ando M (1980) Chloride-dependent sodium and water transport in the seawater eel intestine. J Comp Physiol 138B, 87-91.
4. Ando M, Kobayashi M (1978) Effects of stripping of the outer layers of the eel intestine on salt and water transport. Comp Biochem Physiol 61A, 497-501.
5. Ando M, Mukuda T, Kozaka T (2003) Water metabolism in the eel acclimated to sea water: from mouth to intestine. Comp Biochem Physiol B Biochem Mol Biol 136, 621-633.
6. Barami K, Iversen K, Furneaux H, et al. (1995) Hu protein as an early marker of neuronal phenotypic differentiation by subependymal zone cells of the adult songbird forebrain. J Neurobiol 28, 82-101.
7. Bernardos RL, Raymond PA (2006) GFAP transgenic zebrafish. Gene Expr Patterns 6, 1007-1013.
8. Bixby S, Kruger GM, Mosher JT, et al. (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.
9. Boëtius I, Boëtius J (1967) Studies in the European eel, Anguilla anguilla (L.). Experimental induction of the male sexual cycle, its relation to temperature and other factors. Meddr Danm Fisk Havunders NS 4, 339-405.
10. Bondurand N, Natarajan D, Thapar N, et al. (2003) Neuron and glia generating progenitors of the mammalian enteric nervous system isolated from fetal and postnatal gut cultures. Development 130, 6387-6400.
11. Chiocchetti R, Grandis A, Bombardi C, et al. (2004) Characterisation of neurons expressing calbindin immunoreactivity in the ileum of the unweaned and mature sheep. Cell Tissue Res 318, 289-303.
12. Chung-Davidson YW, Rees CB, Bryan MB, et al. (2008) Neurogenic and neuroendocrine effects of goldfish pheromones. J Neurosci 28, 14492-14499.
13. Clarke AJ, Witcomb DM (1980) A study of the histology and morphology of the digestive tract of the common eel (Anguilla Anguilla). J Fish Biol 16, 159-170.
14. Cooke HJ (1989) Role of the 'little brain' in the gut in water and electrolyte homeostasis. FASEB J 3, 127-138.
15. De Leo GA, Gatto M (1996) Trends in vital rates of the European eel: evidence for density dependence? Ecol Appl 6, 1281-1294.
16. Deschênes-Furry J, Perrone-Bizzozero N, Jasmin BJ (2006) The RNA-binding protein HuD: a regulator of neuronal differentiation, maintenance and plasticity. Bioessays 28, 822-833.
17. Ezeasor DN (1979) Ultrastractural observations on the submucous plexus of the large intestine of the rainbow trout (Salmo gairdneri, Rich.). Z Mikrosk Anat Forsch 93, 803-812.
18. Fairman CL, Clagett-Dame M, Lennon VA, et al. (1995) Appearance of neurons in the developing chick gut. Dev Dyn 204, 192-201.
19. Filogamo G, Cracco C (1995) Models of neuronal plasticity and repair in the enteric nervous system. Ital J Anat Embryo 100, 185-195.
20. Fowler CD, Liu Y, Wang Z (2008) Estrogen and adult neurogenesis in the amygdala and hypothalamus. Brain Res Rev 57, 342-351.
21. Gisbert E, Fernández I, Alvarez-González CA (2011) Prolonged feed deprivation does not permanently compromise digestive function in migrating European glass eels Anguilla anguilla. J Fish Biol 78, 580-592.
22. Grosell M (2006) Intestinal anion exchange in marine fish osmoregulation. J Exp Biol 209, 2813-2827.
23. Hanani M, Ledder O, Yutkin V, et al. (2003) Regeneration of myenteric plexus in the mouse colon after experimental denervation with benzalkonium chloride. J Comp Neurol 462, 315-327.
24. Harder W (1975) Anatomy of Fishes. Stuttgart:Schweizerbart'sche Verlagsbuchhandlung, pp. 136-159, 364-406.
25. Hirano T, Utida S (1968) Effects of ACTH and cortisol on water movement in isolated intestine of the eel, Anguilla japonica. Gen Comp Endocrinol 11, 373-380.
26. Hirano T, Utida S (1971) Plasma cortisol concentration and the rate of intestinal water absorption in the eel, Anguilla japonica. Endocrinol Jpn 17, 47-52.
27. Hoff S, Zeller F, von Weyhern CW, et al. (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.
28. Holtkamp K, Bühren K, Ponath G, et al. (2008) Serum levels of S100B are decreased in chronic starvation and normalize with weight gain. J Neural Transm 115, 937-940.
29. Honma Y, Matsui I (1972) Histological observation on a specimen of the Japanese eel, Anguilla japonica, under the long-term starvation. J Shimonoseki Univ Fish 21, 15-23.
30. Inman MV, Levy S, Mock BA, et al. (1998) Gene organization and chromosome location of the neural-specific RNA binding protein Elavl4. Gene 208, 139-145.
31. Karila P, Holmgren S (1995) Enteric reflexes and nitric oxide in the fish intestine. J Exp Biol 198, 2405-2411.
32. Kim YK, Ideuchi H, Watanabe S, et al. (2008) Rectal water absorption in seawater-adapted Japanese eel Anguilla japonica. Comp Biochem Physiol A Mol Integr Physiol 151, 533-541.
33. Kruger G, Mosher J, Bixby S, 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.
34. Laranjeira C, Sandgren K, Kessaris N, et al. (2011) Glial cells in the mouse enteric nervous system can undergo neurogenesis in response to injury. J Clin Invest 121, 3412-3424.
35. Laverty G, Skadhauge E (2012) Adaptation of teleosts to very high salinity. Comp Biochem Physiol A Mol Integr Physiol 163, 1-6.
36. Li J, Siegel M, Yuan M, et al. (2011) Estrogen enhances neurogenesis and behavioral recovery after stroke. J Cereb Blood Flow Metab 31, 413-425.
37. Lieberwirth C, Wang Z (2012) The social environment and neurogenesis in the adult Mammalian brain. Front Hum Neurosci 6, 118.
38. Liu MT, Kuan YH, Wang J, et al. (2009) 5-HT4 receptor-mediated neuroprotection and neurogenesis in the enteric nervous system of adult mice. J Neurosci 29, 9683-9699.
39. MacKay WC, Janicki R (1978) Changes in the eel intestine during seawater adaptation. Comp Biochem Physiol 62A, 757-761.
40. Marusich MF, Furneaux HM, Henion PD, et al. (1994) Hu neuronal proteins are expressed in proliferating neurogenic cells. J Neurobiol 25, 143-155.
41. Mordenti O, Di Biase A, Sirri R, et al. (2012a) Induction of sexual maturation in wild female European eel (Anguilla anguilla) in darkness and light. Isr J Aquac - Bamidgeh IJA_64.2012.726, 9.
42. Mordenti O, Di Biase A, Bastone G, et al. (2012b) Controlled reproduction in the wild European eel (Anguilla anguilla): Two populations compared. Acquac Int 21, 1045-1063.
43. Moreira NM, Hermes C, Almeida CS, et al. (2008) Quantitative analysis of the neurons from the myenteric plexus in the ileum of rats submitted to severe protein deficiency. Arq Neuropsiquiatr 66, 242-245.
44. Natali MRM, Miranda-Neto MH, Orsi AM (2003) Morphometry and quantification of the myenteric neurons of the duodenum of adult rats fed with hypoproteic chow. Int J Morphol 21, 273-277.
45. Okano HJ, Darnell RB (1997) A hierarchy of Hu RNA binding proteins in developing and adult neurons. J Neurosci 17, 3024-3037.
46. Olsson C (2009) Autonomic innervation of the fish gut. Acta Histochem 111, 185-195.
47. Olsson C (2011a) Calbindin-immunoreactive cells in the fish enteric nervous system. Auton Neurosci 159, 7-14.
48. Olsson C (2011b) Calbindin immunoreactivity in the enteric nervous system of larval and adult zebrafish (Danio rerio). Cell Tissue Res 344, 31-40.
49. Olsson C, Holmberg A, Holmgren S (2008) Development of enteric and vagal innervation of the zebrafish (Danio rerio) gut. J Comp Neurol 508, 756-770.
50. Pankhurst NW, Sorensen PW (1983) Degeneration of the alimentary tract in sexually maturing European Anguilla anguilla (L.) and American eels Anguilla rostrata (LeSueur). Can J Zool 62, 1143-1149.
51. Perrone-Bizzozero N, Bolognani F (2002) Role of HuD and other RNA binding proteins in neural development and plasticity. J Neurosci Res 68, 121-126.
52. Redi F (1684) Osservazioni intorno agli animali viventi che si trovano negli animali viventi: Life-history of the eel. Florence, 253.
53. Shochina M, Belai A, Toole L, et al. (1997) Neurochemical coding in the myenteric plexus of the upper gastrointestinal tract of hibernating hamsters. Int J Dev Neurosci 15, 353-362.
54. da Silva PG, Bertaglia Pereira JN, Tibúrcio VG, et al. (2012) Effect of caloric restriction on myenteric neuroplasticity in the rat duodenum during aging. Auton Neurosci 168, 43-47.
55. Sørensen C, Bohlin LC, Øverli Ø, et al. (2011) Cortisol reduces cell proliferation in the telencephalon of rainbow trout (Oncorhynchus mykiss). Physiol Behav 102, 518-523.
56. Sørensen C, Nilsson GE, Summers CH, et al. (2012) Social stress reduces forebrain cell proliferation in rainbow trout (Oncorhynchus mykiss). Behav Brain Res 227, 311-318.
57. Toole L, Belai A, Shochina M, et al. (1999) The effects of hibernation on the myenteric plexus of the golden hamster small and large intestine. Cell Tissue Res 296, 479-487.
58. Vasina V, Barbara G, Talamonti L, et al. (2006) Enteric neuroplasticity evoked by inflammation. Auton Neurosci 126-127, 264-272.
59. Wallace KN, Akhter S, Smith EM, et al. (2005) Intestinal growth and differentiation in zebrafish. Mech Dev 122, 157-173.
60. Waters MJ, Blackmore DG (2011) Growth hormone (GH), brain development and neural stem cells. Pediatr Endocrinol Rev 9, 549-553.
61. Yamamoto M, Hirano T (1978) Morphological changes in the esophageal epithelium of the eel, Anguilla japonica, during adaptation to seawater. Cell Tissue Res 192, 25-38.