Molecular Pain | |
Secretagogin is expressed in sensory CGRP neurons and in spinal cord of mouse and complements other calcium-binding proteins, with a note on rat and human | |
Tomas Hökfelt5  Tibor Harkany6  Mathias Uhlén1  Anna Josephson5  Ludwig Wagner2  Kaj Fried7  Jan Mulder3  Henrik Hammarberg4  Giuseppe Tortoriello6  Ming-Dong Zhang7  Qiong Xiang5  Tie-Jun Sten Shi7  | |
[1] Science for Life Laboratory, Albanova University Center, Royal Institute of Technology (KTH), Stockholm, Sweden;Department of Medicine III, Medical University of Vienna, Vienna, Austria;Department of Neuroscience, Science for Life Laboratory, Karolinska Institutet, Stockholm, Sweden;Department of Clinical Science and Education, Södersjukhuset (The Southern Hospital), Karolinska Institutet, Stockholm, Sweden;Department of Neuroscience, Karolinska Institutet, Stockholm, Sweden;European Neuroscience Institute, University of Aberdeen, Aberdeen, UK;Department of Dental Medicine, Karolinska Institutet, Stockholm, Sweden | |
关键词: Trigeminal ganglion; Parvalbumin; Nerve injury; Dorsal root ganglion; Dorsal horn; Calretinin; Calbindin D-28k; | |
Others : 863338 DOI : 10.1186/1744-8069-8-80 |
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received in 2011-10-13, accepted in 2012-10-10, 发布年份 2012 | |
【 摘 要 】
Background
Secretagogin (Scgn), a member of the EF-hand calcium-binding protein (CaBP) superfamily, has recently been found in subsets of developing and adult neurons. Here, we have analyzed the expression of Scgn in dorsal root ganglia (DRGs) and trigeminal ganglia (TGs), and in spinal cord of mouse at the mRNA and protein levels, and in comparison to the well-known CaBPs, calbindin D-28k, parvalbumin and calretinin. Rat DRGs, TGs and spinal cord, as well as human DRGs and spinal cord were used to reveal phylogenetic variations.
Results
We found Scgn mRNA expressed in mouse and human DRGs and in mouse ventral spinal cord. Our immunohistochemical data showed a complementary distribution of Scgn and the three CaBPs in mouse DRG neurons and spinal cord. Scgn was expressed in ~7% of all mouse DRG neuron profiles, mainly small ones and almost exclusively co-localized with calcitonin gene-related peptide (CGRP). This co-localization was also seen in human, but not in rat DRGs. Scgn could be detected in the mouse sciatic nerve and accumulated proximal to its constriction. In mouse spinal cord, Scgn-positive neuronal cell bodies and fibers were found in gray matter, especially in the dorsal horn, with particularly high concentrations of fibers in the superficial laminae, as well as in cell bodies in inner lamina II and in some other laminae. A dense Scgn-positive fiber network and some small cell bodies were also found in the superficial dorsal horn of humans. In the ventral horn, a small number of neurons were Scgn-positive in mouse but not rat, confirming mRNA distribution. Both in mouse and rat, a subset of TG neurons contained Scgn. Dorsal rhizotomy strongly reduced Scgn fiber staining in the dorsal horn. Peripheral axotomy did not clearly affect Scgn expression in DRGs, dorsal horn or ventral horn neurons in mouse.
Conclusions
Scgn is a CaBP expressed in a subpopulation of nociceptive DRG neurons and their processes in the dorsal horn of mouse, human and rat, the former two co-expressing CGRP, as well as in dorsal horn neurons in all three species. Functional implications of these findings include the cellular refinement of sensory information, in particular during the processing of pain.
【 授权许可】
2012 Shi et al.; licensee BioMed Central Ltd.
【 预 览 】
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【 参考文献 】
- [1]Celio RC, Pauls T, Schwaller B: Guidebook to the calcium-binding proteins. New York: Oxford University Press; 1996.
- [2]Celio MR: Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 1990, 35:375-475.
- [3]Freund TF, Buzsaki G: Interneurons of the hippocampus. Hippocampus 1996, 6:347-470.
- [4]Celio MR, Heizmann CW: Calcium-binding protein parvalbumin as a neuronal marker. Nature 1981, 293:300-302.
- [5]Andressen C, Blumcke I, Celio MR: Calcium-binding proteins: selective markers of nerve cells. Cell Tissue Res 1993, 271:181-208.
- [6]Kretsinger RH: Crystallographic studies of calmodulin and homologs. Ann N Y Acad Sci 1980, 356:14-19.
- [7]Kretsinger RH: Structure and evolution of calcium-modulated proteins. CRC Crit Rev Biochem 1980, 8:119-174.
- [8]Wagner L, Oliyarnyk O, Gartner W, Nowotny P, Groeger M, Kaserer K, Waldhausl W, Pasternack MS: Cloning and expression of secretagogin, a novel neuroendocrine- and pancreatic islet of Langerhans-specific Ca2+−binding protein. J Biol Chem 2000, 275:24740-24751.
- [9]Wagner L, Templ E, Reining G, Base W, Weissel M, Nowotny P, Kaserer K, Waldhausl W: Culture of human insulinoma cells: development of a neuroendocrine tumor cell- and human pancreatic islet cell-specific monoclonal antibody. J Endocrinol 1998, 156:469-476.
- [10]Attems J, Ittner A, Jellinger K, Nitsch RM, Maj M, Wagner L, Gotz J, Heikenwalder M: Reduced secretagogin expression in the hippocampus of P301L tau transgenic mice. J Neural Transm 2011.
- [11]Attems J, Preusser M, Grosinger-Quass M, Wagner L, Lintner F, Jellinger K: Calcium-binding protein secretagogin-expressing neurones in the human hippocampus are largely resistant to neurodegeneration in Alzheimer's disease. Neuropathol Appl Neurobiol 2008, 34:23-32.
- [12]Attems J, Quass M, Gartner W, Nabokikh A, Wagner L, Steurer S, Arbes S, Lintner F, Jellinger K: Immunoreactivity of calcium binding protein secretagogin in the human hippocampus is restricted to pyramidal neurons. Exp Gerontol 2007, 42:215-222.
- [13]Gartner W, Vila G, Daneva T, Nabokikh A, Koc-Saral F, Ilhan A, Majdic O, Luger A, Wagner L: New functional aspects of the neuroendocrine marker secretagogin based on the characterization of its rat homolog. Am J Physiol Endocrinol Metab 2007, 293:E347-E354.
- [14]Maj M, Gartner W, Ilhan A, Neziri D, Attems J, Wagner L: Expression of TAU in insulin-secreting cells and its interaction with the calcium-binding protein secretagogin. J Endocrinol 2010, 205:25-36.
- [15]Mulder J, Spence L, Tortoriello G, Dinieri JA, Uhlen M, Shui B, Kotlikoff MI, Yanagawa Y, Aujard F, Hökfelt T, Hurd YL, Harkany T: Secretagogin is a Ca2+−binding protein identifying prospective extended amygdala neurons in the developing mammalian telencephalon. Eur J Neurosci 2010, 31:2166-2177.
- [16]Mulder J, Zilberter M, Spence L, Tortoriello G, Uhlen M, Yanagawa Y, Aujard F, Hokfelt T, Harkany T: Secretagogin is a Ca2+−binding protein specifying subpopulations of telencephalic neurons. Proc Natl Acad Sci USA 2009, 106:22492-22497.
- [17]Rogstam A, Linse S, Lindqvist A, James P, Wagner L, Berggard T: Binding of calcium ions and SNAP-25 to the hexa EF-hand protein secretagogin. Biochem J 2007, 401:353-363.
- [18]Bark IC, Wilson MC: Regulated vesicular fusion in neurons: snapping together the details. Proc Natl Acad Sci USA 1994, 91:4621-4624.
- [19]Liu Y, Ma Q: Generation of somatic sensory neuron diversity and implications on sensory coding. Curr Opin Neurobiol 2011, 21:52-60.
- [20]Marmigere F, Ernfors P: Specification and connectivity of neuronal subtypes in the sensory lineage. Nat Rev Neurosci 2007, 8:114-127.
- [21]Li Y, Li H, Kaneko T, Mizuno N: Local circuit neurons showing calbindin D28k-immunoreactivity in the substantia gelatinosa of the medullary dorsal horn of the rat. An immunohistochemical study combined with intracellular staining in slice preparation. Brain Res 1999, 840:179-183.
- [22]Li YN, Sakamoto H, Kawate T, Cheng CX, Li YC, Shimada O, Atsumi S: An immunocytochemical study of calbindin-D28K in laminae I and II of the dorsal horn and spinal ganglia in the chicken with special reference to the relation to substance P-containing primary afferent neurons. Arch Histol Cytol 2005, 68:57-70.
- [23]Philippe E, Droz B: Calbindin-immunoreactive sensory neurons of dorsal root ganglion project to skeletal muscle in the chick. J Comp Neurol 1989, 283:153-160.
- [24]Morona R, Moreno N, Lopez JM, Gonzalez A: Immunohistochemical localization of calbindin-D28k and calretinin in the spinal cord of Xenopus laevis. J Comp Neurol 2006, 494:763-783.
- [25]Morona R, Lopez JM, Dominguez L, Gonzalez A: Immunohistochemical and hodological characterization of calbindin-D28k-containing neurons in the spinal cord of the turtle, Pseudemys scripta elegans. Microsc Res Tech 2007, 70:101-118.
- [26]Levanti MB, Montalbano G, Laura R, Ciriaco E, Cobo T, Garcia-Suarez O, Germana A, Vega JA: Calretinin in the peripheral nervous system of the adult zebrafish. J Anat 2008, 212:67-71.
- [27]Chang IY, Kim SW, Lee KJ, Yoon SP: Calbindin D-28k, parvalbumin and calcitonin gene-related peptide immunoreactivity in the canine spinal cord. Anat Histol Embryol 2008, 37:446-451.
- [28]Kobayashi M, Hjerling-Leffler J, Ernfors P: Increased progenitor proliferation and apoptotic cell death in the sensory lineage of mice overexpressing N-myc. Cell Tissue Res 2006, 323:81-90.
- [29]Alvarez FJ, Jonas PC, Sapir T, Hartley R, Berrocal MC, Geiman EJ, Todd AJ, Goulding M: Postnatal phenotype and localization of spinal cord V1 derived interneurons. J Comp Neurol 2005, 493:177-192.
- [30]Nakamura S, Senzaki K, Yoshikawa M, Nishimura M, Inoue K, Ito Y, Ozaki S, Shiga T: Dynamic regulation of the expression of neurotrophin receptors by Runx3. Development 2008, 135:1703-1711.
- [31]Ninomiya T, Barakat-Walter I, Droz B: Neuronal phenotypes in mouse dorsal root ganglion cell cultures: enrichment of substance P and calbindin D-28k expressing neurons in a defined medium. Int J Dev Neurosci 1994, 12:99-106.
- [32]Ringstedt T, Kucera J, Lendahl U, Ernfors P, Ibanez CF: Limb proprioceptive deficits without neuronal loss in transgenic mice overexpressing neurotrophin-3 in the developing nervous system. Development 1997, 124:2603-2613.
- [33]Barakat-Walter I, Kraftsik R, Kuntzer T, Bogousslavsky J, Magistretti P: Differential effect of thyroid hormone deficiency on the growth of calretinin-expressing neurons in rat spinal cord and dorsal root ganglia. J Comp Neurol 2000, 426:519-533.
- [34]Yamamoto T, Carr PA, Baimbridge KG, Nagy JI: Parvalbumin- and calbindin D28k-immunoreactive neurons in the superficial layers of the spinal cord dorsal horn of rat. Brain Res Bull 1989, 23:493-508.
- [35]Antal M, Freund TF, Polgar E: Calcium-binding proteins, parvalbumin- and calbindin-D 28k-immunoreactive neurons in the rat spinal cord and dorsal root ganglia: a light and electron microscopic study. J Comp Neurol 1990, 295:467-484.
- [36]Heppelmann B, Emson PC: Distribution of calretinin mRNA in rat spinal cord and dorsal root ganglia: a study using non-radioactive in situ hybridization histochemistry. Brain Res 1993, 624:312-316.
- [37]Carr PA, Yamamoto T, Karmy G, Baimbridge KG, Nagy JI: Parvalbumin is highly colocalized with calbindin D28k and rarely with calcitonin gene-related peptide in dorsal root ganglia neurons of rat. Brain Res 1989, 497:163-170.
- [38]Carr PA, Yamamoto T, Karmy G, Baimbridge KG, Nagy JI: Analysis of parvalbumin and calbindin D28k-immunoreactive neurons in dorsal root ganglia of rat in relation to their cytochrome oxidase and carbonic anhydrase content. Neuroscience 1989, 33:363-371.
- [39]Ichikawa H, Jacobowitz DM, Sugimoto T: Calretinin-immunoreactive neurons in the trigeminal and dorsal root ganglia of the rat. Brain Res 1993, 617:96-102.
- [40]Ren K, Ruda MA: A comparative study of the calcium-binding proteins calbindin-D28K, calretinin, calmodulin and parvalbumin in the rat spinal cord. Brain Res Brain Res Rev 1994, 19:163-179.
- [41]Ichikawa H, Deguchi T, Fujiyoshi Y, Nakago T, Jacobowitz DM, Sugimoto T: Calbindin-D28k-immunoreactivity in the trigeminal ganglion neurons and molar tooth pulp of the rat. Brain Res 1996, 715:71-78.
- [42]Ichikawa H, Deguchi T, Nakago T, Jacobowitz DM, Sugimoto T: Parvalbumin, calretinin and carbonic anhydrase in the trigeminal and spinal primary neurons of the rat. Brain Res 1994, 655:241-245.
- [43]Ichikawa H, Jacobowitz DM, Sugimoto T: S100 protein-immunoreactive primary sensory neurons in the trigeminal and dorsal root ganglia of the rat. Brain Res 1997, 748:253-257.
- [44]Ichikawa H, Jin HW, Terayama R, Yamaai T, Jacobowitz DM, Sugimoto T: Calretinin-containing neurons which co-express parvalbumin and calbindin D-28k in the rat spinal and cranial sensory ganglia; triple immunofluorescence study. Brain Res 2005, 1061:118-123.
- [45]Papka RE, Collins J, Copelin T, Wilson K: Calretinin-immunoreactive nerves in the uterus, pelvic autonomic ganglia, lumbosacral dorsal root ganglia and lumbosacral spinal cord. Cell Tissue Res 1999, 298:63-74.
- [46]Shimizu T, Suzuki N, Takao M, Koto A, Fukuuchi Y: Calbindin-D28k in cerebrovascular extrinsic innervation system of the rat. Auton Neurosci 2000, 84:130-139.
- [47]Yamashita N, Ilg EC, Schafer BW, Heizmann CW, Kosaka T: Distribution of a specific calcium-binding protein of the S100 protein family, S100A6 (calcyclin), in subpopulations of neurons and glial cells of the adult rat nervous system. J Comp Neurol 1999, 404:235-257.
- [48]Antal M, Polgar E, Chalmers J, Minson JB, Llewellyn-Smith I, Heizmann CW, Somogyi P: Different populations of parvalbumin- and calbindin-D28k-immunoreactive neurons contain GABA and accumulate 3H-D-aspartate in the dorsal horn of the rat spinal cord. J Comp Neurol 1991, 314:114-124.
- [49]Honda CN: Differential distribution of calbindin-D28k and parvalbumin in somatic and visceral sensory neurons. Neuroscience 1995, 68:883-892.
- [50]Ichikawa H, Mo Z, Xiang M, Sugimoto T: Effect of Brn-3a deficiency on parvalbumin-immunoreactive primary sensory neurons in the dorsal root ganglion. Brain Res Dev Brain Res 2004, 150:41-45.
- [51]McMahon SB, Priestley JV: Nociceptor plasticity. In The Neurobiology of Pain. Edited by Hunt SP, Koltzenburg M. Oxford Univ Press; 35-64.
- [52]Snider WD, McMahon SB: Tackling pain at the source: new ideas about nociceptors. Neuron 1998, 20:629-632.
- [53]Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D: The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 1997, 389:816-824.
- [54]McDonald TJ, Jornvall H, Tatemoto K, Mutt V: Identification and characterization of variant forms of the gastrin-releasing peptide (GRP). FEBS Lett 1983, 156:349-356.
- [55]Panula P, Hadjiconstantinou M, Yang HY, Costa E: Immunohistochemical localization of bombesin/gastrin-releasing peptide and substance P in primary sensory neurons. J Neurosci 1983, 3:2021-2029.
- [56]Sun YG, Chen ZF: A gastrin-releasing peptide receptor mediates the itch sensation in the spinal cord. Nature 2007, 448:700-703.
- [57]Malmberg AB, Chen C, Tonegawa S, Basbaum AI: Preserved acute pain and reduced neuropathic pain in mice lacking PKCgamma. Science 1997, 278:279-283.
- [58]Xiang Q, Mulder J, Harkany T, Uhlen M, Hökfelt T, Shi TJ: Expression of the calcium-binding protein secretagogin in mouse and human dorsal root ganglia and spinal cord. Montreal: Abstract, 13 World Congress on Pain; 2010.
- [59]Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, Bernard A, Boe AF, Boguski MS, Brockway KS, Byrnes EJ, Chen L, Chen TM, Chin MC, Chong J, Crook BE, Czaplinska A, Dang CN, Datta S, Dee NR, Desaki AL, Desta T, Diep E, Dolbeare TA, Donelan MJ, Dong HW, Dougherty JG, Duncan BJ, Ebbert AJ, Eichele G, Estin LK, Faber C, Facer BA, Fields R, Fischer SR, Fliss TP, Frensley C, Gates SN, Glattfelder KJ, Halverson KR, Hart MR, Hohmann JG, Howell MP, Jeung DP, Johnson RA, Karr PT, Kawal R, Kidney JM, Knapik RH, Kuan CL, Lake JH, Laramee AR, Larsen KD, Lau C, Lemon TA, Liang AJ, Liu Y, Luong LT, Michaels J, Morgan JJ, Morgan RJ, Mortrud MT, Mosqueda NF, Ng LL, Ng R, Orta GJ, Overly CC, Pak TH, Parry SE, Pathak SD, Pearson OC, Puchalski RB, Riley ZL, Rockett HR, Rowland SA, Royall JJ, Ruiz MJ, Sarno NR, Schaffnit K, Shapovalova NV, Sivisay T, Slaughterbeck CR, Smith SC, Smith KA, Smith BI, Sodt AJ, Stewart NN, Stumpf KR, Sunkin SM, Sutram M, Tam A, Teemer CD, Thaller C, Thompson CL, Varnam LR, Visel A, Whitlock RM, Wohnoutka PE, Wolkey CK, Wong VY, Wood M, Yaylaoglu MB, Young RC, Youngstrom BL, Yuan XF, Zhang B, Zwingman TA, Jones AR: Genome-wide atlas of gene expression in the adult mouse brain. Nature 2007, 445:168-176.
- [60]Mulder J, Bjorling E, Jonasson K, Wernerus H, Hober S, Hokfelt T, Uhlen M: Tissue profiling of the mammalian central nervous system using human antibody-based proteomics. Mol Cell Proteomics 2009, 8:1612-1622.
- [61]Gibson SJ, Polak JM, Bloom SR, Sabate IM, Mulderry PM, Ghatei MA, McGregor GP, Morrison JF, Kelly JS, Evans RM, et al.: Calcitonin gene-related peptide immunoreactivity in the spinal cord of man and of eight other species. J Neurosci 1984, 4:3101-3111.
- [62]Giuffrida R, Rustioni A: Dorsal root ganglion neurons projecting to the dorsal column nuclei of rats. J Comp Neurol 1992, 316:206-220.
- [63]Yoshida S, Senba E, Kubota Y, Hagihira S, Yoshiya I, Emson PC, Tohyama M: Calcium-binding proteins calbindin and parvalbumin in the superficial dorsal horn of the rat spinal cord. Neuroscience 1990, 37:839-848.
- [64]Heizmann CW, Braun K: Changes in Ca(2+)-binding proteins in human neurodegenerative disorders. Trends Neurosci 1992, 15:259-264.
- [65]Gotz J, Schonrock N, Vissel B, Ittner LM: Alzheimer's disease selective vulnerability and modeling in transgenic mice. J Alzheimers Dis 2009, 18:243-251.
- [66]Hof PR, Cox K, Young WG, Celio MR, Rogers J, Morrison JH: Parvalbumin-immunoreactive neurons in the neocortex are resistant to degeneration in Alzheimer's disease. J Neuropathol Exp Neurol 1991, 50:451-462.
- [67]Ferrer I, Isamat F, Lopez-Obarrio L, Conesa G, Rimbau J, Alcantara S, Espanol I, Zujar MJ: Parvalbumin and calbindin D-28K immunoreactivity in central ganglioglioma and dysplastic gangliocytoma of the cerebellum. Report of two cases. J Neurosurg 1993, 78:133-137.
- [68]Iacopino A, Christakos S, German D, Sonsalla PK, Altar CA: Calbindin-D28K-containing neurons in animal models of neurodegeneration: possible protection from excitotoxicity. Brain Res Mol Brain Res 1992, 13:251-261.
- [69]Mattson MP, Rychlik B, Chu C, Christakos S: Evidence for calcium-reducing and excito-protective roles for the calcium-binding protein calbindin-D28k in cultured hippocampal neurons. Neuron 1991, 6:41-51.
- [70]Nicotera P, Bellomo G, Orrenius S: Calcium-mediated mechanisms in chemically induced cell death. Annu Rev Pharmacol Toxicol 1992, 32:449-470.
- [71]Nitsch C, Scotti A, Sommacal A, Kalt G: GABAergic hippocampal neurons resistant to ischemia-induced neuronal death contain the Ca2(+)-binding protein parvalbumin. Neurosci Lett 1989, 105:263-268.
- [72]Sloviter RS: Calcium-binding protein (calbindin-D28k) and parvalbumin immunocytochemistry: localization in the rat hippocampus with specific reference to the selective vulnerability of hippocampal neurons to seizure activity. J Comp Neurol 1989, 280:183-196.
- [73]Chard PS, Bleakman D, Christakos S, Fullmer CS, Miller RJ: Calcium buffering properties of calbindin D28k and parvalbumin in rat sensory neurones. J Physiol 1993, 472:341-357.
- [74]Gibbons SJ, Brorson JR, Bleakman D, Chard PS, Miller RJ: Calcium influx and neurodegeneration. Ann N Y Acad Sci 1993, 679:22-33.
- [75]Ponsati B, Carreno C, Curto-Reyes V, Valenzuela B, Duart MJ, Van Den Nest W, Cauli O, Beltran B, Fernandez J, Borsini F, Caprioli A, Di Serio S, Veretchy M, Baamonde A, Menendez L, Barros F, de la Pena P, Borges R, Felipo V, Planells-Cases R, Ferrer-Montiel A: An Inhibitor of Neuronal Exocytosis (DD04107) Displays Long-Lasting In Vivo Activity against Chronic Inflammatory and Neuropathic Pain. J Pharmacol Exp Ther 2012, 341:634-645.
- [76]Shi TJ, Tandrup T, Bergman E, Xu ZQ, Ulfhake B, Hokfelt T: Effect of peripheral nerve injury on dorsal root ganglion neurons in the C57 BL/6J mouse: marked changes both in cell numbers and neuropeptide expression. Neuroscience 2001, 105:249-263.
- [77]Hjerling-Leffler J, Marmigere F, Heglind M, Cederberg A, Koltzenburg M, Enerback S, Ernfors P: The boundary cap: a source of neural crest stem cells that generate multiple sensory neuron subtypes. Development 2005, 132:2623-2632.
- [78]Shi TJ, Cui JG, Meyerson BA, Linderoth B, Hokfelt T: Regulation of galanin and neuropeptide Y in dorsal root ganglia and dorsal horn in rat mononeuropathic models: possible relation to tactile hypersensitivity. Neuroscience 1999, 93:741-757.
- [79]Pease PC: Buffered formaldehyde as a killing agent and primary fixative for electron microscopy. Anat Rec 1962, 142:342.
- [80]Zamboni I, De Martino C: Buffered picric acid formaldehyde. A new rapid fixative for electron microscopy. J Cell Biol 1967, 35:148A.
- [81]Orazzo C, Pieribone VA, Ceccatelli S, Terenius L, Hökfelt T: CGRP-like immunoreactivity in A11 dopamine neurons projecting to the spinal cord and a note on CGRP-CCK cross-reactivity. Brain Res 1993, 600:39-48.
- [82]Wang H, Rivero-Melian C, Robertson B, Grant G: Transganglionic transport and binding of the isolectin B4 from Griffonia simplicifolia I in rat primary sensory neurons. Neuroscience 1994, 62:539-551.
- [83]Johnson GD, Nogueira Araujo GM: A simple method of reducing the fading of immunofluorescence during microscopy. J Immunol Methods 1981, 43:349-350.
- [84]Platt JL, Michael AF: Retardation of fading and enhancement of intensity of immunofluorescence by p-phenylenediamine. J Histochem Cytochem 1983, 31:840-842.
- [85]Shi TJ, Huang P, Mulder J, Ceccatelli S, Hokfelt T: Expression of p-Akt in sensory neurons and spinal cord after peripheral nerve injury. Neurosignals 2009, 17:203-212.
- [86]Dubovy P, Svizenska I, Vega JA: Non-specific cholinesterase activity in mouse spinal ganglia. The usefulness of histochemical study and image analysis for simple characterization of neuron subclasses. Cell Mol Biol 1990, 36:23-40.