Distribution and neurochemical identification of pancreatic afferents in the mouse

Journal of Comparative Neurology

Volumn 509, Issue 1, 2008, Pages 42-52

  Fasanella, Kenneth E ^a   Christianson, Julie A ^a   Chanthaphavong, R Savanh ^a   Davis, Brian M ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

CGRP; Dorsal root ganglion; Immunohistochemistry; Nodose ganglia; Retrograde labeling; TRPV1; Visceral pain

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR RECEPTOR; VANILLOID RECEPTOR 1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONFOCAL MICROSCOPY; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NEUROCHEMISTRY; NOCICEPTION; NODOSE GANGLION; NONHUMAN; PANCREAS; PRIORITY JOURNAL; SENSORY NERVE; SPINAL GANGLION; VISCERAL PAIN;

AFFERENT PATHWAYS; ANIMALS; MALE; MICE; MICE, INBRED C57BL; NEURONS, AFFERENT; PANCREAS;

EID: 45349095446     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21736     Document Type: Article

References (54)

1. Averill S, McMahon SB, Clary DO, Reichardt LF, Priestley JV. 1995. Immunocytochemical localization of trkA receptors in chemically identified subgroups of adult rat sensory neurons. Eur J Neurosci 7:1484-1494.
2. Bahns E, Halsband U, Janig W. 1987. Responses of sacral visceral afferents from the lower urinary tract, colon and anus to mechanical stimulation. Pflugers Arch 410:296-303.
3. Baloh RH, Tansey MG, Lampe PA, Fahrner TJ, Enomoto H, Simburger KS, Leitner ML, Araki T, Johnson EM Jr, Milbrandt J. 1998. Artemin, a novel member of the GDNF ligand family, supports peripheral and central neurons and signals through the GFRalpha3-RET receptor complex. Neuron 21:1291-1302.
4. Bennett DL, Dmietrieva N, Priestley JV, Clary D, McMahon SB. 1996. trkA, CGRP and IB4 expression in retrogradely labelled cutaneous and visceral primary sensory neurones in the rat. Neurosci Lett 206:33-36.
5. Berkley KJ, Hotta H, Robbins A, Sato Y. 1990. Functional properties of afferent fibers supplying reproductive and other pelvic organs in pelvic nerve of female rat. J Neurophysiol 63:256-272.
6. Bielefeldt K and Davis B. 2008. Differential effects of ASIC3 and TRPV1 deletion on gastroesophageal sensation in mice. Am J Physiol Gastrointest Liver Physiol 294:G103-G108.
7. Bielefeldt K, Zhong F, Koerber HR, Davis BM. 2006. Phenotypic characterization of gastric sensory neurons in mice. Am J Physiol Gastrointest Liver Physiol 291:G987-997.
8. Blackshaw LA, Page AJ, Partosoedarso ER. 2000. Acute effects of capsaicin on gastrointestinal vagal afferents. Neuroscience 96:407-416.
9. Bookman DE, Buchler M, Malfertheiner P, Beger HG. 1988. Analysis of nerves in chronic pancreatitis. Gastroenterology 94:1459-1469.
10. Brierley SM, Carter R, Jones W 3rd, Xu L, Robinson DR, Hicks GA, Gebhart GF, Blackshaw LA. 2005. Differential chemosensory function and receptor expression of splanchnic and pelvic colonic afferents in mice. J Physiol 567:267-281.
11. Carlsten JA, Kothary R, Wright DE. 2001. Glial cell line-derived neurotrophic factor-responsive and neurotrophin-3-responsive neurons require the cytoskeletal linker protein dystonin for postnatal survival. J Comp Neurol 432:155-168.
12. Carobi C. 1987. Capsaicin-sensitive vagal afferent neurons innervating the rat pancreas. Neurosci Lett 77:5-9.
13. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D. 1997. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389:816-824.
14. Ceyhan GO, Bergmann F, Kadihasanoglu M, Erkan M, Park W, Hinz U, Giese T, Muller MW, Buchler MW, Giese NA, Friess H. 2007. The neurotrophic factor artemin influences the extent of neural damage and growth in chronic pancreatitis. Gut 56:534-544.
15. Christiansen JA, McIlwrath SL, Koerber HR, Davis BM. 2006a. Transient receptor potential vanilloid 1-immunopositive neurons in the mouse are more prevalent within colon afferents compared to skin and muscle afferents. Neuroscience 140:247-257.
16. Christianson JA, Traub RJ, Davis BM. 2006b. Differences in spinal distribution and neurochemical phenotype of colonic afferents in mouse and rat. J Comp Neurol 494:246-259.
17. Christianson JA, Liang R, Ustinova EE, Davis BM, Fraser MO, Pezzone MA. 2007. Convergence of bladder and colon sensory innervation occurs at the primary afferent level. Pain 128:235-243.
18. Davis JB, Gray J, Gunthorpe MJ, Hatcher JP, Davey PT, Overend P, Harries MH, Latcham J, Clapham C, Atkinson K, Hughes SA, Rance K, Grau E, Harper AJ, Pugh PL, Rogers DC, Bingham S, Randall A, Sheardown SA. 2000. Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 405:183-187.
19. Di Sebastiano P, di Mola FF, Buchler MW, Friess H. 2004. Pathogenesis of pain in chronic pancreatitis. Dig Dis 22:267-272.
20. Elitt CM, McIlwrath SL, Lawson JJ, Malin SA, Molliver DC, Cornuet PK, Koerber HR, Davis BM, Albers KM. 2006. Artemin overexpression in skin enhances expression of TRPV1 and TRPA1 in cutaneous sensory neurons and leads to behavioral sensitivity to heat and cold. J Neurosci 26:8578-8587.
21. Forrest SL, Keast JR. 2008. Expression of receptors for glial cell line-derived neurotrophic factor family ligands in sacral spinal cord reveals separate targets of pelvic afferent fibers. J Comp Neurol 506:989-1002.
22. Friess H, Zhu ZW, di Mola FF, Kulli C, Graber HU, Andren-Sandberg A, Zimmermann A, Korc M, Reinshagen M, Buchler MW. 1999. Nerve growth factor and its high-affinity receptor in chronic pancreatitis. Ann Surg 230:615-624.
23. Friess H, Shrikhande S, Shrikhande M, Martignoni M, Kulli C, Zimmermann A, Kappeler A, Ramesh H, Buchler M. 2002. Neural alterations in surgical stage chronic pancreatitis are independent of the underlying aetiology. Gut 50:682-686.
24. Goldstein IJ, Winter HG. 1999. The Griffonia simplicifolia I-B4 isolectin. A probe for alpha-D-galactosyl end groups. Subcell Biochem 32:127-141.
25. Grundy D. 2002. Neuroanatomy of visceral nociception: vagal and splanchnic afferent. Gut 51(suppl 1):i2-5.
26. Kirchgessner AL, Gershon MD. 1990. Innervation of the pancreas by neurons in the gut. J Neurosci 10:1626-1642.
27. Liddle RA. 2007. The role of transient receptor potential vanilloid 1 (TRPV1) channels in pancreatitis. Biochim Biophys Acta 1772:869-878.
28. Lindsay TH, Halvorson KG, Peters CM, Ghilardi JR, Kuskowski MA, Wong GY, Mantyh PW. 2006. A quantitative analysis of the sensory and sympathetic innervation of the mouse pancreas. Neuroscience 137:1417-1426.
29. Ma W, Quirion R. 2007. Inflammatory mediators modulating the transient receptor potential vanilloid 1 receptor: therapeutic targets to treat inflammatory and neuropathic pain. Expert Opin Ther Targets 11:307-320.
30. Malin SA, Molliver DC, Koerber HR, Cornuet P, Frye R, Albers KM, Davis BM. 2006. Glial cell line-derived neurotrophic factor family members sensitize nociceptors in vitro and produce thermal hyperalgesia in vivo. J Neurosci 26:8588-8599.
31. Malykhina AP, Qin C, Greenwood-van Meerveld B, Foreman RD, Lupu F, Akbarali HI. 2006. Hyperexcitability of convergent colon and bladder dorsal root ganglion neurons after colonic inflammation: mechanism for pelvic organ cross-talk. Neurogastroenterol Motil 18:936-948.
32. Mizushima T, Obata K, Yamanaka H, Dai Y, Fukuoka T, Tokunaga A, Mashimo T, Noguchi K. 2005. Activation of p38 MAPK in primary afferent neurons by noxious stimulation and its involvement in the development of thermal hyperalgesia. Pain 113:51-60.
33. Molliver DC, Wright DE, Leitner ML, Parsadanian AS, Doster K, Wen D, Yan Q, Snider WD. 1997. IB4-binding DRG neurons switch from NGF to GDNF dependence in early postnatal life. Neuron 19:849-861.
34. Noble MD, Romac J, Wang Y, Hsu J, Humphrey JE, Liddle RA. 2006. Local disruption of the celiac ganglion inhibits substance P release and ameliorates caerulein-induced pancreatitis in rats. Am J Physiol Gastrointest Liver Physiol 291:G128-134.
35. Orozco OE, Walsh L, Sah DW, Pepinsky RB, Sanicola M. 2001. GFRα3 is expressed predominantly in nociceptive sensory neurons. Eur S Neurosci 13:2177-2182.
36. Pakkenberg B, Gundersen HJ. 1988. Total number of neurons and glial cells in human brain nuclei estimated by the disector and the fractionator. J Microsc 150:1-20.
37. Peeters PJ, Aerssens J, de Hoogt R, Stanisz A, Gohlmann HW, Hillsley K, Meulemans A, Grundy D, Stead RH, Coulie B. 2006. Molecular profiling of murine sensory neurons in the nodose and dorsal root ganglia labeled from the peritoneal cavity. Physiol Genomics 24:252-263.
38. Robinson DR, McNaughton PA, Evans ML, Hicks GA. 2004. Characterization of the primary spinal afferent innervation of the mouse colon using retrograde labelling. Neurogastroenterol Motil 16:113-124.
39. Sengupta JN. 2000. An overview of esophageal sensory receptors. Am J Med 108(suppl 4a):87S-89S.
40. Sharkey KA, Williams RG. 1983. Extrinsic innervation of the rat pancreas: demonstration of vagal sensory neurones in the rat by retrograde tracing. Neurosci Lett 42:131-135.
41. Sharkey KA, Williams RG, Dockray GJ. 1984. Sensory substance P innervation of the stomach and pancreas. Demonstration of capsaicin-sensitive sensory neurons in the rat by combined immunohistochemistry and retrograde tracing. Gastroenterology 87:914-921.
42. Sternini C, De Giorgio R, Furness JB. 1992. Calcitonin gene-related peptide neurons innervating the canine digestive system. Regul Pept 42:15-26.
43. Tamura S, Morikawa Y, Senba E. 2005. TRPV2, a capsaicin receptor homologue, is expressed predominantly in the neurotrophin-3-dependent subpopulation of primary sensory neurons. Neuroscience 130:223-228.
44. Toma H, Winston J, Micci MA, Shenoy M, Pasricha PJ. 2000. Nerve growth factor expression is up-regulated in the rat model of L-arginine-induced acute pancreatitis. Gastroenterology 119:1373-1381.
45. Toma H, Winston JH, Micci MA, Li H, Hellmich HL, Pasricha PJ. 2002. Characterization of the neurotrophic response to acute pancreatitis. Pancreas 25:31-38.
46. Ustinova EE, Fraser MO, Pezzone MA. 2006. Colonic irritation in the rat sensitizes urinary bladder afferents to mechanical and chemical stimuli: an afferent origin of pelvic organ cross-sensitization. Am J Physiol Renal Physiol 290:F1478-1487.
47. Wang HF, Shortland P, Park MJ, Grant G. 1998. Retrograde and transganglionic transport of horseradish peroxidase-conjugated cholera toxin B subunit, wheatgerm agglutinin and isolectin B4 from Griffonia simplicifolia I in primary afferent neurons innervating the rat urinary bladder. Neuroscience 87:275-288.
48. Wang S, Davis BM, Zwick M, Waxman SG, Albers KM. 2006. Reduced thermal sensitivity and Nav1.8 and TRPV1 channel expression in sensory neurons of aged mice. Neurobiology of aging 27:895-903.
49. Wick EC, Hoge SG, Grahn SW, Kim E, Divino LA, Grady EF, Bunnett NW, Kirkwood KS. 2006. Transient receptor potential vanilloid 1, calcitonin gene-related peptide, and substance P mediate nociception in acute pancreatitis. Am J Physiol Gastrointest Liver Physiol 290:G959-969.
50. Winston JH, He ZJ, Shenoy M, Xiao SY, Pasricha PJ. 2005. Molecular and behavioral changes in nociception in a novel rat model of chronic pancreatitis for the study of pain. Pain 117:214-222.
51. Won MH, Park HS, Jeong YG, Park HJ. 1998. Afferent innervation of the rat pancreas: retrograde tracing and immunohistochemistry in the dorsal root ganglia. Pancreas 16:80-87.
52. Xu GY, Winston JH, Shenoy M, Yin H, Pendyala S, Pasricha PJ. 2007. Transient receptor potential vanilloid 1 mediates hyperalgesia and is up-regulated in rats with chronic pancreatitis. Gastroenterology 133:1282-1292.
53. Zhong F, Christianson JA, Davis BM, Bielefeldt K. 2008. Dichotomizing axons in spinal and vagal afferents of the mouse stomach. Dig Dis Sci 53:194-203.
54. Zhu ZW, Friess H, Wang L, Zimmermann A, Buchler MW. 2001. Brain-derived neurotrophic factor (BDNF) is upregulated and associated with pain in chronic pancreatitis. Dig Dis Sci 46:1633-1639.