Neurotrophic actions initiated by proNGF in adult sensory neurons may require peri-somatic glia to drive local cleavage to NGF

Journal of Neurochemistry

Volumn 122, Issue 3, 2012, Pages 523-536

  Kalous, Adrianna ^a   Nangle, Matthew R ^a   Anastasia, Agustin ^b   Hempstead, Barbara L ^b   Keast, Janet R ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

dorsal root ganglion; Neurotrophin; nociceptor; p75; satellite cells; sortilin

Indexed keywords

MATRIX METALLOPROTEINASE; NERVE GROWTH FACTOR; NERVE GROWTH FACTOR PRECURSOR; NEUROTROPHIN RECEPTOR P75; PROTEIN PRECURSOR; PROTEIN TYROSINE KINASE A; SORTILIN; UNCLASSIFIED DRUG;

ADULT ANIMAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; CELL ISOLATION; CONTROLLED STUDY; ENZYME ACTIVATION; GLIA CELL; GROWTH CONE; IN VIVO STUDY; INTRACELLULAR SIGNALING; MALE; MOUSE; NERVE CELL CULTURE; NERVE FIBER GROWTH; NEUROCHEMISTRY; NEUROTROPISM; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SENSORY NERVE CELL; SOMATIC CELL; SPINAL GANGLION;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; ANTIBODIES; CALCITONIN GENE-RELATED PEPTIDE; CARBAZOLES; CELLS, CULTURED; ENZYME INHIBITORS; GANGLIA, SPINAL; GLIAL FIBRILLARY ACIDIC PROTEIN; INDOLE ALKALOIDS; MALE; MICE; MICE, INBRED C57BL; NERVE GROWTH FACTOR; NEURITES; NEUROGLIA; PROTEIN PRECURSORS; RECEPTOR, TRKA; SENSORY RECEPTOR CELLS; SIGNAL TRANSDUCTION; TIME FACTORS; TUBULIN; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84863723497     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2012.07799.x     Document Type: Article

References (52)

1. Al-Shawi R., Hafner A., Olson J., Chun S., Raza S., Thrasivoulou C., Lovestone S., Killick R., Simons P., and, Cowen T., (2008) Neurotoxic and neurotrophic roles of proNGF and the receptor sortilin in the adult and ageing nervous system. Eur. J. Neurosci. 27, 2103-14.
2. Althaus H. H., and, Kloppner S., (2006) Mature pig oligodendrocytes rapidly process human recombinant pro-nerve growth factor and do not undergo cell death. J. Neurochem. 98, 506-17.
3. Arnett M. G., Ryals J. M., and, Wright D. E., (2007) Pro-NGF, sortilin, and p75NTR: potential mediators of injury-induced apoptosis in the mouse dorsal root ganglion. Brain Res. 1183, 32-42.
4. Averill S., McMahon S. B., Clary D. O., Reichardt L. F., and, Priestley J. V., (1995) Immunocytochemical localization of trkA receptors in chemically identified subgroups of adult rat sensory neurons. Eur. J. Neurosci. 7, 1484-94.
5. Barbacid M., (1994) The Trk family of neurotrophin receptors. J. Neurobiol. 25, 1386-403.
6. Bierl M. A., Jones E. E., Crutcher K. A., and, Isaacson L. G., (2005) 'Mature' nerve growth factor is a minor species in most peripheral tissues. Neurosci. Lett. 380, 133-7.
7. Boutilier J., Ceni C., Pagdala P. C., Forgie A., Neet K. E., and, Barker P. A., (2008) Proneurotrophins require endocytosis and intracellular proteolysis to induce TrkA activation. J. Biol. Chem. 283, 12709-16.
8. Buttigieg H., Kawaja M. D., and, Fahnestock M., (2007) Neurotrophic activity of proNGF in vivo. Exp. Neurol. 204, 832-5.
9. Campenot R. B., (1994) NGF and the local control of nerve terminal growth. J. Neurobiol. 25, 599-611.
10. Chen Z. L., Yu W. M., and, Strickland S., (2007) Peripheral regeneration. Annu. Rev. Neurosci. 30, 209-33.
11. Clewes O., Fahey M. S., Tyler S. J., Watson J. J., Seok H., Catania C., Cho K., Dawbarn D., and, Allen S. J., (2008) Human ProNGF: biological effects and binding profiles at TrkA, P75NTR and sortilin. J. Neurochem. 107, 1124-35.
12. Connolly J. L., Seeley P. J., and, Greene L. A., (1987) Rapid regulation of neuronal growth cone shape and surface morphology by nerve growth factor. Neurochem. Res. 12, 861-8.
13. Domeniconi M., Hempstead B. L., and, Chao M. V., (2007) Pro-NGF secreted by astrocytes promotes motor neuron cell death. Mol. Cell. Neurosci. 34, 271-9.
14. Ernsberger U., (2009) Role of neurotrophin signalling in the differentiation of neurons from dorsal root ganglia and sympathetic ganglia. Cell Tissue Res. 336, 349-84.
15. Fahnestock M., Michalski B., Xu B., and, Coughlin M. D., (2001) The precursor pro-nerve growth factor is the predominant form of nerve growth factor in brain and is increased in Alzheimer's disease. Mol. Cell. Neurosci. 18, 210-20.
16. Fahnestock M., Yu G., Michalski B., Mathew S., Colquhoun A., Ross G. M., and, Coughlin M. D., (2004) The nerve growth factor precursor proNGF exhibits neurotrophic activity but is less active than mature nerve growth factor. J. Neurochem. 89, 581-92.
17. Fiorentini C., Guerra N., Facchetti M., Finardi A., Tiberio L., Schiaffonati L., Spano P., and, Missale C., (2002) Nerve growth factor regulates dopamine D(2) receptor expression in prolactinoma cell lines via p75(NGFR)-mediated activation of nuclear factor-kappaB. Mol. Endocrinol. 16, 353-66.
18. Fukazawa H., and, Uehara Y., (2000) U0126 reverses Ki-ras-mediated transformation by blocking both mitogen-activated protein kinase and p70 S6 kinase pathways. Cancer Res. 60, 2104-7.
19. Harrington A. W., Leiner B., Blechschmitt C., Arevalo J. C., Lee R., Morl K., Meyer M., Hempstead B. L., Yoon S. O., and, Giehl K. M., (2004) Secreted proNGF is a pathophysiological death-inducing ligand after adult CNS injury. Proc. Natl Acad. Sci. USA 101, 6226-30.
20. Hu P., and, McLachlan E. M., (2003) Selective reactions of cutaneous and muscle afferent neurons to peripheral nerve transection in rats. J. Neurosci. 23, 10559-67.
21. Huang E. J., and, Reichardt L. F., (2001) Neurotrophins: roles in neuronal development and function. Annu. Rev. Neurosci. 24, 677-736.
22. Huang B., Zhao X., Zheng L. B., Zhang L., Ni B., and, Wang Y. W., (2011) Different expression of tissue inhibitor of metalloproteinase family members in rat dorsal root ganglia and their changes after peripheral nerve injury. Neuroscience 193, 421-8.
23. Jansen P., Giehl K., Nyengaard J. R., et al. (2007) Roles for the pro-neurotrophin receptor sortilin in neuronal development, aging and brain injury. Nat. Neurosci. 10, 1449-57.
24. Kalous A., and, Keast J. R., (2010) Conditioning lesions enhance growth state only in sensory neurons lacking calcitonin gene-related peptide and isolectin B4-binding. Neuroscience 166, 107-21.
25. Kaplan D. R., and, Miller F. D., (2000) Neurotrophin signal transduction in the nervous system. Curr. Opin. Neurobiol. 10, 381-91.
26. Kawasaki Y., Xu Z. Z., Wang X., et al. (2008) Distinct roles of matrix metalloproteases in the early- and late-phase development of neuropathic pain. Nat. Med. 14, 331-6.
27. Kim T., and, Hempstead B. L., (2009) NRH2 is a trafficking switch to regulate sortilin localization and permit proneurotrophin-induced cell death. EMBO J. 28, 1612-23.
28. Kozai T., Yamanaka H., Dai Y., Obata K., Kobayashi K., Mashimo T., and, Noguchi K., (2007) Tissue type plasminogen activator induced in rat dorsal horn astrocytes contributes to mechanical hypersensitivity following dorsal root injury. Glia 55, 595-603.
29. Lee R., Kermani P., Teng K. K., and, Hempstead B. L., (2001) Regulation of cell survival by secreted proneurotrophins. Science 294, 1945-8.
30. Lewin G. R., and, Barde Y. A., (1996) Physiology of the neurotrophins. Annu. Rev. Neurosci. 19, 289-317.
31. Markus A., Zhong J., and, Snider W. D., (2002) Raf and akt mediate distinct aspects of sensory axon growth. Neuron 35, 65-76.
32. Masoudi R., Ioannou M. S., Coughlin M. D., Pagadala P., Neet K. E., Clewes O., Allen S. J., Dawbarn D., and, Fahnestock M., (2009) Biological activity of nerve growth factor precursor is dependent upon relative levels of its receptors. J. Biol. Chem. 284, 18424-33.
33. Meyers R., and, Cantley L. C., (1997) Cloning and characterization of a wortmannin-sensitive human phosphatidylinositol 4-kinase. J. Biol. Chem. 272, 4384-90.
34. Nykjaer A., Lee R., Teng K. K., et al. (2004) Sortilin is essential for proNGF-induced neuronal cell death. Nature 427, 843-8.
35. Obata K., Katsura H., Sakurai J., Kobayashi K., Yamanaka H., Dai Y., Fukuoka T., and, Noguchi K., (2006) Suppression of the p75 neurotrophin receptor in uninjured sensory neurons reduces neuropathic pain after nerve injury. J. Neurosci. 26, 11974-86.
36. Paveliev M., Lume M., Velthut A., Phillips M., Arumae U., and, Saarma M., (2007) Neurotrophic factors switch between two signaling pathways that trigger axonal growth. J. Cell Sci. 120, 2507-16.
37. Pezet S., and, McMahon S. B., (2006) Neurotrophins: mediators and modulators of pain. Annu. Rev. Neurosci. 29, 507-38.
38. Purves-Tyson T. D., and, Keast J. R., (2004) Rapid actions of estradiol on cyclic amp response-element binding protein phosphorylation in dorsal root ganglion neurons. Neuroscience 129, 629-37.
39. Reinshagen M., Geerling I., Eysselein V. E., Adler G., Huff K. R., Moore G. P., and, Lakshmanan J., (2000) Commercial recombinant human beta-nerve growth factor and adult rat dorsal root ganglia contain an identical molecular species of nerve growth factor prohormone. J. Neurochem. 74, 2127-33.
40. Riccio A., Ahn S., Davenport C. M., Blendy J. A., and, Ginty D. D., (1999) Mediation by a CREB family transcription factor of NGF-dependent survival of sympathetic neurons. Science 286, 2358-61.
41. Rivera S., Khrestchatisky M., Kaczmarek L., Rosenberg G. A., and, Jaworski D. M., (2010) Metzincin proteases and their inhibitors: foes or friends in nervous system physiology? J. Neurosci. 30, 15337-57.
42. Segal R. A., (2003) Selectivity in neurotrophin signaling: theme and variations. Annu. Rev. Neurosci. 26, 299-330.
43. Seidah N. G., Benjannet S., Pareek S., Savaria D., Hamelin J., Goulet B., Laliberte J., Lazure C., Chretien M., and, Murphy R. A., (1996) Cellular processing of the nerve growth factor precursor by the mammalian pro-protein convertases. Biochem. J. 314, 951-60.
44. Teng K. K., Felice S., Kim T., and, Hempstead B. L., (2010) Understanding proneurotrophin actions: recent advances and challenges. Dev. Neurobiol. 70, 350-9.
45. Tucker B. A., Rahimtula M., and, Mearow K. M., (2008) Src and FAK are key early signalling intermediates required for neurite growth in NGF-responsive adult DRG neurons. Cell. Signal. 20, 241-57.
46. Volosin M., Song W., Almeida R. D., Kaplan D. R., Hempstead B. L., and, Friedman W. J., (2006) Interaction of survival and death signaling in basal forebrain neurons: roles of neurotrophins and proneurotrophins. J. Neurosci. 26, 7756-66.
47. Wright D. E., and, Snider W. D., (1995) Neurotrophin receptor mRNA expression defines distinct populations of neurons in rat dorsal root ganglia. J. Comp. Neurol. 351, 329-38.
48. Yamanaka H., Obata K., Fukuoka T., Dai Y., Kobayashi K., Tokunaga A., and, Noguchi K., (2004) Tissue plasminogen activator in primary afferents induces dorsal horn excitability and pain response after peripheral nerve injury. Eur. J. Neurosci. 19, 93-102.
49. Yamanaka H., Obata K., Fukuoka T., Dai Y., Kobayashi K., Tokunaga A., and, Noguchi K., (2005) Induction of plasminogen activator inhibitor-1 and -2 in dorsal root ganglion neurons after peripheral nerve injury. Neuroscience 132, 183-91.
50. Yong V. W., Power C., Forsyth P., and, Edwards D. R., (2001) Metalloproteinases in biology and pathology of the nervous system. Nat. Rev. Neurosci. 2, 502-11.
51. Yune T. Y., Lee J. Y., Jung G. Y., Kim S. J., Jiang M. H., Kim Y. C., Oh Y. J., Markelonis G. J., and, Oh T. H., (2007) Minocycline alleviates death of oligodendrocytes by inhibiting pro-nerve growth factor production in microglia after spinal cord injury. J. Neurosci. 27, 7751-61.
52. Zhou X. F., Rush R. A., and, McLachlan E. M., (1996) Differential expression of the p75 nerve growth factor receptor in glia and neurons of the rat dorsal root ganglia after peripheral nerve transection. J. Neurosci. 16, 2901-11.