Neurotrophin selectivity in organizing topographic regeneration of nociceptive afferents

Experimental Neurology

Volumn 271, Issue , 2015, Pages 262-278

  Kelamangalath, Lakshmi ^a   Tang, Xiaoqing ^a   Bezik, Kathleen ^a   Sterling, Noelle ^a   Son, Young Jin ^a   Smith, George M ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Artemin; Axonal guidance; Regeneration; Sensory system

Indexed keywords

ARTEMIN; CALCITONIN GENE RELATED PEPTIDE; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR RECEPTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR RECEPTOR ALPHA 1; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR RECEPTOR ALPHA 3; ISOLECTIN B4; LENTIVIRUS VECTOR; NERVE GROWTH FACTOR; NEUROTROPHIN; PROTEIN C FOS; PROTEIN RET; UNCLASSIFIED DRUG; ARTN PROTEIN, RAT; CHOLERA TOXIN; IMMUNOLOGICAL ADJUVANT; LECTIN; NERVE PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CRUSH TRAUMA; DORSAL ROOT; FEMALE; GENE EXPRESSION; MECHANICAL HYPERALGESIA; NERVE REGENERATION; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; PROPRIOCEPTION; RAT; SCIATIC NERVE; SENSORY NERVE; SPINAL CORD DORSAL HORN; SPINAL CORD INJURY; ANIMAL; DISEASE MODEL; DRUG EFFECTS; GENETIC TRANSDUCTION; HYPERALGESIA; METABOLISM; PAIN MEASUREMENT; PAIN RECEPTOR; PAIN THRESHOLD; PATHOLOGY; PATHOPHYSIOLOGY; PERIPHERAL NERVE INJURIES; PSYCHOMOTOR PERFORMANCE; SPINAL GANGLION; SPRAGUE DAWLEY RAT;

ADJUVANTS, IMMUNOLOGIC; AFFERENT PATHWAYS; ANIMALS; CALCITONIN GENE-RELATED PEPTIDE; CHOLERA TOXIN; DISEASE MODELS, ANIMAL; FEMALE; GANGLIA, SPINAL; HYPERALGESIA; LECTINS; NERVE GROWTH FACTOR; NERVE REGENERATION; NERVE TISSUE PROTEINS; NOCICEPTORS; PAIN MEASUREMENT; PAIN THRESHOLD; PERIPHERAL NERVE INJURIES; PSYCHOMOTOR PERFORMANCE; RATS; RATS, SPRAGUE-DAWLEY; TRANSDUCTION, GENETIC;

EID: 84934988254     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2015.06.007     Document Type: Article

References (71)

1. Albers K.M., Zhang X.L., Diges C.M., Schwartz E.S., Yang C.I., Davis B.M., Gold M.S. Artemin growth factor increases nicotinic cholinergic receptor subunit expression and activity in nociceptive sensory neurons. Mol. Pain 2014, 10:31.
2. Baloh R.H., Tansey M.G., Lampe P.A., Fahrner T.J., Enomoto H., Simburger K.S., Leitner M.L., Araki T., Johnson E.M., Milbrandt J. Artemin, a novel member of the GDNF ligand family, supports peripheral and central neurons and signals through the GFRalpha3-RET receptor complex. Neuron 1998, 21:1291-1302.
3. Bennett D.L.H., Boucher T.J., Armanini M.P., Poulsen K.T., Michael G.J., Priestley J.V., Phillips H.S., McMahon S.B., Shelton D.L. The glial cell line-derived neurotrophic factor family receptor components are differentially regulated within sensory neurons after nerve injury. J. Neurosci. 2000, 20:427-437.
4. Blesch A., Lu P., Tuszynski M.H. Neurotrophic factors, gene therapy, and neural stem cells for spinal cord repair. Brain Res. Bull. 2002, 57:833-838.
5. Boucher T.J., Okuse K., Bennett D.L., Munson J.B., Wood J.N., McMahon S.B. Potent analgesic effects of GDNF in neuropathic pain states. Science 2000, 290:124-147.
6. Brown A., Ricci M.J., Weaver L.C. NGF message and protein distribution in the injured rat spinal cord. Exp. Neurol. 2004, 188:115-127.
7. Cajal Ramon y Bull. N. Y. Acad. Med. 1929, 5.
8. Campenot R.B. Development of sympathetic neurons in compartmentalized cultures: II. Local control of neurite survival by nerve growth factor. Dev. Biol. 1982, 93:13-21.
9. Carlstedt T. Regenerating axons form nerve-terminals at astrocytes. Brain Res. 1985, 347:188-191.
10. Chaplan S.R., Pogrel J.W., Yaksh T.L. Role of voltage-dependent calcium channel subtypes in experimental tactile allodynia. J. Pharmacol. Exp. Ther. 1994, 269:1117-1123.
11. Christensen M.D., Hulsebosch C.E. Spinal cord injury and anti-NGF treatment results in changes in CGRP density and distribution in the dorsal horn in the rat. Exp. Neurol. 1997, 147:463-475.
12. Coggeshall R.E. Fos, nociception and the dorsal horn. Prog. Neurobiol. 2005, 77:299-352.
13. Crone S.A., Lee K.F. The bound leading the bound: target-derived receptors act as guidance cues. Neuron 2002, 36:333-335.
14. Devor M., Govrin-Lippmann R. Selective regeneration of sensory fibers following nerve crush injury. Exp. Neurol. 1979, 65:243-254.
15. Diamond J., Coughlin M., Macintyre L. Evidence that endogenous beta-nerve growth factor is responsible for the collateral sprouting, but not the regeneration, of nociceptive axons in adult-rats. Proc. Natl. Acad. Sci. U. S. A. 1985, 84:6596-6600.
16. Diamond J., Holmes M., Coughlin M. Endogenous Ngf and nerve impulses regulate the collateral sprouting of sensory axons in the skin of the adult-rat. J. Neurosci. 1992, 12:1454-1466.
17. Dixon W.J. Efficient analysis of experimental observations. Annu. Rev. Pharmacol. Toxicol. 1980, 20:441-462.
18. Doubleday B., Robinson P.P. The role of nerve growth-factor in collateral reinnervation by cutaneous C-fibers in the rat. Brain Res. 1992, 593:179-184.
19. Doucette R., Diamond J. Normal and precocious sprouting of heat nociceptors in the skin of adult rats. J. Comp. Neurol. 1987, 261:592-603.
20. Eggers R., de Winter F., Hoyng S.A., Roet K.C., Ehlert E.M., Malessy M.J., Verhaagen J., Tannemaat M.R. Lentiviral vector-mediated gradients of GDNF in the injured peripheral nerve: effects on nerve coil formation, Schwann cell maturation and myelination. PLoS One 2013, 8:e71076.
21. Elitt C.M., McIlwrath S.L., Lawson J.J., Malin S.A., Molliver D.C., Cornuet P.K., Koerber H.R., Davis B.M., Albers K.M. 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. 2006, 26:8578-8587.
22. Fouad K., Pedersen V., Schwab M.E., Brosamle C. Cervical sprouting of corticospinal fibers after thoracic spinal cord injury accompanies shifts in evoked motor responses. Curr. Biol. 2001, 11:1766-1770.
23. Gallo G., Letourneau P.C. Localized sources of neurotrophins initiate axon collateral sprouting. J. Neurosci. 1998, 18:5403-5414.
24. Gardell L.R., et al. Multiple actions of systemic artemin in experimental neuropathy. Nat. Med. 2003, 9:1383-1389.
25. Hancock M.L., Nowakowski D.W., Role L.W., Talmage D.A., Flanagan J.G. Type III neuregulin 1 regulates pathfinding of sensory axons in the developing spinal cord and periphery. Development 2011, 138:4887-4898.
26. Hannila S.S., Kawaja M.D. Nerve growth factor-mediated collateral sprouting of central sensory axons into deafferentated regions of the dorsal horn is enhanced in the absence of the p75 neurotrophin receptor. J. Comp. Neurol. 2005, 486:331-343.
27. Hargreaves K., Dubner R., Brown F., Flores C., Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 1988, 32:77-88.
28. Harper S.J., Buchman V.L., Owen D. Denervation of the skin following section of the inferior alveolar nerve leads to increased NGF accumulation without change in NGF mRNA expression. Exp. Neurol. 1999, 155:327-330.
29. Harris J.A. Using c-Fos as a neural marker of pain. Brain Res. Bull. 1998, 45:1-8.
30. Harvey P., Gong B., Rossomando A.J., Frank E. Topographically specific regeneration of sensory axons in the spinal cord. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:11585-11590.
31. Hunt S.P., Pini A., Evan G. Induction of c-Fos-like protein in spinal cord neurons following sensory stimulation. Nature 1987, 328:632-634.
32. Jankowski M.P., Rau K.K., Soneji D.J., Anderson C.E., Koerber H.R. Enhanced artemin/GFRα3 levels regulate mechanically insensitive, heat-sensitive C-fiber recruitment after axotomy and regeneration. J. Neurosci. 2010, 30:16272-16283.
33. Ketschek A., Gallo G. Nerve growth factor induces axonal filopodia through localized microdomains of phosphoinositide 3-kinase activity that drive the formation of cytoskeletal precursors to filopodia. J. Neurosci. 2010, 30:12185-12197.
34. Kim B.G., Dai H.N., McAtee M., Vicini S., Bregman B.S. Remodeling of synaptic structures in the motor cortex following spinal cord injury. Exp. Neurol. 2006, 198:401-415.
35. Kimpinski K., Campenot R.B., Mearow K. Effects of the neurotrophins nerve growth factor, neurotrophin-3, and brain-derived neurotrophic factor (BDNF) on neurite growth from adult sensory neurons in compartmented cultures. J. Neurobiol. 1997, 33:395-410.
36. Krenz N.R., Weaver L.C. Nerve growth factor in glia and inflammatory cells of the injured rat spinal cord. J. Neurochem. 2000, 74:730-739.
37. Leclere P.G., Norman E., Groutsi F., Coffin R., Mayer U., Pizzey J., Tonge D. Impaired axonal regeneration by isolectin B4-binding dorsal root ganglion neurons in vitro. J. Neurosci. 2007, 27:1190-1199.
38. Ledda F., Paratcha G., Ibanez C.F. Target-derived GFR alpha 1 as an attractive guidance signal for developing sensory and sympathetic axons via activation of Cdk5. Neuron 2002, 36:387-401.
39. Ledda F., Paratcha G., Sandoval-Guzman T., Ibanez C.F. GDNF and GFR alpha 1 promote formation of neuronal synapses by ligand-induced cell adhesion. Nat. Neurosci. 2007, 10:293-300.
40. Lewin G.R., Rueff A., Mendell L.M. Peripheral and central mechanisms of Ngf-induced hyperalgesia. Eur. J. Neurosci. 1994, 6:1903-1912.
41. Lin C.-L., Heron P., Hamann S.R., Smith G.M. Functional distinction between NGF-mediated plasticity and regeneration of nociceptive axons within the spinal cord. Neuroscience 2014, 272.
42. Lippoldt E.K., Elmes R.R., McCoy D.D., Knowlton W.M., McKemy D.D. Artemin, a glial cell line-derived neurotrophic factor family member, induces TRPM8-dependent cold pain. J. Neurosci. 2013, 33:12543-12552.
43. Malin S.A., Davis B.M. Postnatal roles of GDNF family members in nociceptors plasticity. Sheng Li Xue Bao 2008, 60:571-578.
44. Malin S.A., Molliver D.C., Koerber H.R., Cornuet P., Frye R., Albers K.M., Davis B.M. Glial cell line-derived neurotrophic factor family members sensitize nociceptors in vitro and produce thermal hyperalgesia in vivo. J. Neurosci. 2006, 26:8588-8599.
45. Marr R.A., Guan H., Rockenstein E., Kindy M., Gage F.H., Verma I., Masliah E., Hersh L.B. Neprilysin regulates amyloid Beta peptide levels. J. Mol. Neurosci. 2004, 22:5-11.
46. O'Donnell M., Chance R.K., Bashaw G.J. Axon growth and guidance: receptor regulation and signal transduction. Annu. Rev. Neurosci. 2009, 32:383-412.
47. Orozco O.E., L W, Sah D.W., Pepinsky R.B., M S GFRalpha3 is expressed predominantly in nociceptive sensory neurons. Eur. J. Neurosci. 2001, 13:2177-2182.
48. Paratcha G., Ledda F. GDNF and GFR alpha: a versatile molecular complex for developing neurons. Trends Neurosci. 2008, 31:384-391.
49. Paratcha G., Ledda F., Baars L., Coulpier M., Besset V., Anders J., Scott R., Ibanez C.F. Released GFR alpha 1 potentiates downstream signaling, neuronal survival, and differentiation via a novel mechanism of recruitment of c-Ret to lipid rafts. Neuron 2001, 29:171-184.
50. Pezet S., Krzyzanowska A., Wong L.F., Grist J., Mazarakis N.D., Georgievska B., McMahon S.B. Reversal of neurochemical changes and pain-related behavior in a model of neuropathic pain using modified lentiviral vectors expressing GDNF. Mol. Ther. 2006, 13:1101-1109.
51. Ramer M.S., Priestley J.V., McMahon S.B. Functional regeneration of sensory axone into the adult spinal cord. Nature 2000, 403:312-316.
52. Ramer M.S., Duraisingam I., Priestley J.V., McMahon S.B. Two-tiered inhibition of axon regeneration at the dorsal root entry zone. J. Neurosci. 2001, 21:2651-2660.
53. Randall L.O., Selitto J.J. A method for measurement of analgesic activity on inflamed tissue. Arch. Int. Pharmacodyn. Ther. 1957, 111:409-419.
54. Robertson B., Grant G. A comparison between wheat-germ agglutinin horseradish and choleragenoid-horseradish peroxidase as anterogradely transported markers in central branches of primary sensory neurons in the rat with some observations in the cat. Neuroscience 1985, 14:895-905.
55. Romero M.I., Rangappa N., Li L., Lightfoot E., Garry M.G., Smith G.M. Extensive sprouting of sensory afferents and hyperalgesia induced by conditional expression of nerve growth factor in the adult spinal cord. J. Neurosci. 2000, 20:4435-4445.
56. Romero M.I., Rangappa N., Garry M.G., Smith G.M. Functional regeneration of chronically injured sensory afferents into adult spinal cord after neurotrophin gene therapy. J. Neurosci. 2001, 21:8408-8416.
57. Salio C., Ferrini F., Muthuraju S., Merighi A. Presynaptic modulation of spinal nociceptive transmission by glial cell line-derived neurotrophic factor (GDNF). J. Neurosci. 2014, 34:13819-13833.
58. Sanes J.R., Yamagata M. Formation of lamina-specific synaptic connections. Curr. Opin. Neurobiol. 1999, 9:79-87.
59. Santoro M.I., Melillo R.M., Carlomagno F., Vecchio G., Fusco A. Minireview: RET: normal and abnormal functions. Endocrinology 2004, 145:5448-5451.
60. Snider W.D., McMahon S.B. Tackling pain at the source: new ideas about nociceptors. Neuron 1998, 20:629-632.
61. Tang X.Q., Tanelian D.L., Smith G.M. Semaphorin3A inhibits nerve growth factor-induced sprouting of nociceptive afferents in adult rat spinal cord. J. Neurosci. 2004, 24:819-827.
62. Tang X.Q., Heron P., Mashburn C., Smith G.M. Targeting sensory axon regeneration in adult spinal cord. J. Neurosci. 2007, 27:6068-6078.
63. Tarpley J.W., Kohler M.G., Martin W.J. The behavioral and neuroanatomical effects of IB4-saporin treatment in rat models of nociceptive and neuropathic pain. Brain Res. 2004, 1029:65-76.
64. Trafton J.A., Abbadie C., Marchand S., Mantyh P.W., Basbaum A.I. Spinal opioid analgesia: how critical is the regulation of substance P signaling?. J. Neurosci. 1999, 19:9642-9653.
65. Vulchanova L., Olson T.H., Stone L.S., Riedl M.S., Elde R., Honda C.N. Cytotoxic targeting of isolectin IB4-binding sensory neurons. Neuroscience 2001, 108:143-155.
66. Wang R., King T., Ossipov M.H., Rossomando A.J., Vanderah T.W., Harvey P., Cariani P., Frank E., Sah D.W., Porreca F. Persistent restoration of sensory function by immediate or delayed systemic artemin after dorsal root injury. Nat. Neurosci. 2008, 11:488-496.
67. Widenfalk J., Tomac A., Lindqvist E., Hoffer B., Olson L. GFR alpha-3, a protein related to GFR alpha-1, is expressed in developing peripheral neurons and ensheathing cells. Eur. J. Neurosci. 1998, 10:1508-1517.
68. Worley D.S., Pisano J.M., Choi E.D., Walus L., Hession C.A., Cate R.L., Sanicola M., Birren S.J. Developmental regulation of GDNF response and receptor expression in the enteric nervous system. Development 2000, 127:4383-4393.
69. Zhang J., Cavanaugh D.J., Nemenov M.I., Basbaum A.I. The modality-specific contribution of peptidergic and non-peptidergic nociceptors is manifest at the level of dorsal horn nociresponsive neurons. J. Physiol. 2013, 591:1097-1110.
70. Zhang C., Jin Y., Ziemba K.S., Fletcher A.M., Ghosh B., Truit E., Yurek D.M., Smith G.M. Long distance directional growth of dopaminergic axons along pathways of netrin-1 and GDNF. Exp. Neurol. 2013, 250:156-164.
71. Zhou F.-Q., Snider W.D. Intracellular control of developmental and regenerative axon growth. Philos. Trans. R. Soc., B 2006, 361:1575-1592.