Axon regeneration in the absence of growth cones: Acceleration by cyclic AMP

Journal of Comparative Neurology

Volumn 515, Issue 3, 2009, Pages 295-312

  Jin, Li Qing ^a   Zhang, Guixin ^a   Jamison Jr , Curtis ^a   Takano, Hajime ^a   Haydon, Philip G ^a   Selzer, Michael E ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

2 photon microscopy; Actin; Lamprey; Microtubule; Neurofilament; Spinal cord injury

Indexed keywords

CYCLIC AMP; F ACTIN; ACTIN;

ANIMAL TISSUE; ARTICLE; CELL MOTION; CELL STRUCTURE; CONTROLLED STUDY; FLUORESCENCE ANALYSIS; GROWTH CONE; IMMUNOREACTIVITY; LAMPREY; MICROSCOPY; MICROTUBULE; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NEUROFILAMENT; NONHUMAN; PRIORITY JOURNAL; ANIMAL; CELL CULTURE; CYTOLOGY; DRUG EFFECT; METABOLISM; MICROFILAMENT; NERVE FIBER; NERVE REGENERATION; PATHOLOGY; PHYSIOLOGY; PSEUDOPODIUM; SPINAL CORD; ULTRASTRUCTURE;

ACTINS; ANIMALS; AXONS; CELLS, CULTURED; CYCLIC AMP; GROWTH CONES; LAMPREYS; MICROFILAMENTS; MICROTUBULES; NERVE REGENERATION; PSEUDOPODIA; SPINAL CORD;

EID: 67650120384     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22057     Document Type: Article

References (101)

1. Banker GA, Cowan WM. 1977. Rat hippocampal neurons in dispersed cell culture. Brain Res 126:397-342.
2. Bauer RJ, Swiatek KR, Robins RK, Simon LN. 1971. Adenosine 3′,5′-cyclic monosphate derivatives. II. Biological activity of some 8-substituted analogs. Biochem Biophys Res Commun 45:526-531.
3. Beattie MS, Bresnahan JC, Lopate G. 1990. Metamorphosis alters the response to spinal cord transection in Xenopus laevis frogs. J Neurobiol 21:1108-1122.
4. Bhatt DH, Otto SJ, Depoister B, Fetcho JR. 2004. Cyclic AMP-induced repair of zebrafish spinal circuits. Science 305:254-258.
5. Blesch A, Uy HS, Grill RJ, Cheng JG, Patterson PH, Tuszynski MH. 1999. Leukemia inhibitory factor augments neurotrophin expression and corticospinal axon growth after adult CNS injury. J Neurosci 19:3556-3566.
6. Bloom O, Evergren E, Tomilin N, Kjaerulff O, Low P, Brodin L, Pieribone VA, Greengard P, Shupliakov O. 2003. Colocalization of synapsin and actin during synaptic vesicle recycling. J Cell Biol 161:737-747.
7. Blose SH, Meltzer DI, Feramisco JR. 1984. 10-nm filaments are induced to collapse in living cells microinjected with monoclonal and polyclonal antibodies against tubulin. J Cell Biol 98:847-858.
8. Brown J, Bridgman PC. 2003. Role of myosin II in axon outgrowth. J Histochem Cytochem 51:421-428.
9. Buchli AD, Schwab ME. 2005. Inhibition of Nogo: a key strategy to increase regeneration, plasticity and functional recovery of the lesioned central nervous system. Ann Med 37:556-567.
10. Cafferty WB, Gardiner NJ, Gavazzi I, Powell J, McMahon SB, Heath JK, Munson J, Cohen J, Thompson SW. 2001. Leukemia inhibitory factor determines the growth status of injured adult sensory neurons. J Neurosci 21:7161-7170.
11. Cai D, Qiu J, Cao Z, McAtee M, Bregman BS, Filbin MT. 2001. Neuronal cyclic AMP controls the developmental loss in ability of axons to regenerate. J Neurosci 21:4731-4739.
12. Cai D, Deng K, Mellado W, Lee J, Ratan RR, Filbin MT. 2002. Arginase I and polyamines act downstream from cyclic AMP in overcoming inhibition of axonal growth MAG and myelin in vitro. Neuron 35:711-719.
13. Cao Z, Gao Y, Bryson JB, Hou J, Chaudhry N, Siddiq M, Martinez J, Spencer T, Carmel J, Hart RB, Filbin MT. 2006. The cytokine interleukin-6 is sufficient but not necessary to mimic the peripheral conditioning lesion effect on axonal growth. J Neurosci 26:5565-5573.
14. Chan WK, Dickerson A, Ortiz D, Pimenta AF, Moran CM, Motil J, Snyder SJ, Malik K, Pant HC, Shea TB. 2004. Mitogen-activated protein kinase regulates neurofilament axonal transport. J Cell Sci 117:4629-4642.
15. Cui Q, Pollett MA, Symons NA, Plant GW, Harvey AR. 2003. A new approach to CNS repair using chimeric peripheral nerve grafts. J Neurotrauma 20:17-31.
16. Dergham P, Ellezam B, Essagian C, Avedissian H, Lubell WD, McKerracher L. 2002. Rho signaling pathway targeted to promote spinal cord repair. J Neurosci 22:6570-6577.
17. Domeniconi M, Filbin MT. 2005. Overcoming inhibitors in myelin to promote axonal regeneration. J Neurol Sci 233:43-47.
18. Fournier AE, Takizawa BT, Strittmatter SM. 2003. Rho kinase inhibition enhances axonal regeneration in the injured CNS. J Neurosci 23:1416-1423.
19. Gao Y, Deng K, Hou J, Bryson JB, Barco A, Nikulina E, Spencer T, Mellado W, Kandel ER, Filbin MT. 2004. Activated CREB is sufficient to overcome inhibitors in myelin and promote spinal axon regeneration in vivo. Neuron 44:609-621.
20. Glass JD, Schryer BL, Griffin JW. 1994. Calcium-mediated degeneration of the axonal cytoskeleton in the Ola mouse. J Neurochem 62:2472-2475.
21. Gocht A, Löhler J. 1993. Microenvironmental changes during axonal regrowth in the optic nerve of the myelin deficient rat. Immunocytochemical and ultrastructural observations. J Neurocytol 22:461-479.
22. GrandPre T, Li S, Strittmatter SM. 2002. Nogo-66 receptor antagonist peptide promotes axonal regeneration. Nature 417:547-551.
23. Hall GF, Lee VM. 1995. Neurofilament sidearm proteolysis is a prominent early effect of axotomy in lamprey giant central neurons. J Comp Neurol 353:38-49.
24. Hall GF, Lee VM, Kosik KS. 1991. Microtubule destabilization and neurofilament phosphorylation precede dendritic sprouting after close axotomy of lamprey central neurons. Proc Natl Acad Sci U S A 88:5016-5020.
25. Hall GF, Yao J, Selzer ME, Kosik KS. 1997. Cytoskeletal changes correlated with the loss of neuronal polarity in axotomized lamprey central neurons. J Neurocytol 26:733-753.
26. Han PJ, Shukla S, Subramanian PS, Hoffman PN. 2004. Cyclic AMP elevates tubulin expression without increasing intrinsic axon growth capacity.[see comment]. Exp Neurol 189:293-302.
27. Hannila SS, Filbin MT. 2008. The role of cyclic AMP signaling in promoting axonal regeneration after spinal cord injury. Exp Neurol 209:321-332.
28. He Z, Koprivica V. 2004. The Nogo signaling pathway for regeneration block. Annu Rev Neurosci 27:341-368.
29. Hisanaga S, Gonda Y, Inagaki M, Ikai A, Hirokawa N. 1990. Effects of phosphorylation of the neurofilament L protein on filamentous structures. Cell Regul 1:237-248.
30. Hisanaga S, Kusubata M, Okumura E, Kishimoto T. 1991. Phosphorylation of neurofilament H subunit at the tail domain by CDC2 kinase dissociates the association to microtubules. J Biol Chem 266:21798-21803.
31. Ivins JK, Parry MK, Long DA. 2004. A novel cAMP-dependent pathway activates neuronal integrin function in retinal neurons. J Neurosci 24:1212-1216.
32. Jacobs AJ, Swain GP, Snedeker JA, Pijak DS, Gladstone LJ, Selzer ME. 1997. Recovery of neurofilament expression selectively in regenerating reticulospinal neurons. J Neurosci 17:5206-5220.
33. Jin LQ, Zhang G, Selzer ME. 2005. Lamprey neurofilaments contain a previously unreported 50-kDa protein. J Comp Neurol 483:403-414.
34. Jones SL, Selzer ME, Gallo G. 2006. Developmental regulation of sensory axon regeneration in the absence of growth cones. J Neurobiol 66: 1630-1645.
35. Khodair MA, Zarbin MA, Townes-Anderson E. 2005. Cyclic AMP prevents retraction of axon terminals in photoreceptors prepared for transplantation: an in vitro study. Invest Ophthalmol Vis Sci 46:967-973.
36. Kim JE, Li S, GrandPre T, Qiu D, Strittmatter SM. 2003. Axon regeneration in young adult mice lacking Nogo-A/B [see Comment]. Neuron 38:187-199.
37. Kim JE, Liu BP, Park JH, Strittmatter SM. 2004. Nogo-66 receptor prevents raphespinal and rubrospinal axon regeneration and limits functional recovery from spinal cord injury. Neuron 44:439-451.
38. Lanners HN, Grafstein B. 1980. Effect of a conditioning lesion on regeneration of goldfish optic axons: ultrastructural evidence of enhanced outgrowth and pinocytosis. Brain Res 196:547-553.
39. Leterrier JF, Kas J, Hartwig J, Vegners R, Janmey PA. 1996. Mechanical effects of neurofilament cross-bridges. Modulation by phosphorylation, lipids, and interactions with F-actin. J Biol Chem 271:15687-15694.
40. Letourneau PC, Shattuck TA, Ressler AH. 1987. "Pull" and "push" in neurite elongation: observations on the effects of different concentrations of cytochalasin B and taxol. Cell Motil Cytoskeleton 8:193-209.
41. Lewis SE, Nixon RA. 1988. Multiple phosphorylated variants of the high molecular mass subunit of neurofilaments in axons of retinal cell neurons: characterization and evidence for their differential association with stationary and moving neurofilaments. J Cell Biol 107:2689-2701.
42. Li S, Kim JE, Budel S, Hampton TG, Strittmatter SM. 2005. Transgenic inhibition of Nogo-66 receptor function allows axonal sprouting and improved locomotion after spinal injury. Mol Cell Neurosci 29:26-39.
43. Lindsay RM. 1988. Nerve growth factors (NGF, BDNF) enhance axonal regeneration but are not required for survival of adult sensory neurons. J Neurosci 8:2394-2405.
44. Liu HH, Brady ST. 2004. cAMP, tubulin, axonal transport, and regeneration [Comment]. Exp Neurol 189:199-203.
45. Lu P, Yang H, Jones LL, Filbin MT, Tuszynski MH. 2004. Combinatorial therapy with neurotrophins and cAMP promotes axonal regeneration beyond sites of spinal cord injury. J Neurosci 24:6402-6409.
46. Lurie DI, Pijak DS, Selzer ME. 1994. Structure of reticulospinal axon growth cones and their cellular environment during regeneration in the lamprey spinal cord. J Comp Neurol 344:559-580.
47. Marsh L, Letourneau PC. 1984. Growth of neurites without filopodial or lamellipodial activity in the presence of cytochalasin B. J Cell Biol 99:2041-2047.
48. Mason CA, Wang LC. 1997. Growth cone form is behavior-specific and, consequently, position-specific along the retinal axon pathway. J Neurosci 17:1086-1100.
49. McGee AW, Strittmatter SM. 2003. The Nogo-66 receptor: focusing myelin inhibition of axon regeneration. Trends Neurosci 26:193-198.
50. McHale MK, Hall GF, Cohen MJ. 1995. Early cytoskeletal changes following injury of giant spinal axons in the lamprey. J Comp Neurol 353:25-37.
51. McKerracher L, Vidal-Sanz M, Aguayo AJ. 1990. Slow transport rates of cytoskeletal proteins change during regeneration of axotomized retinal neurons in adult rats. J Neurosci 10:641-648.
52. McKerracher L, Selzer ME. 2006. Intraneuronal determinants of regeneration. In: Selzer ME, Clarke S, Cohen LG, Duncan PW, Gage FH, editors. Textbook of neural repair and rehabilitation: neural repair and plasticity. Cambridge, UK: Cambridge University Press. p 421-442.
53. Merrick SE, Pleasure SJ, Lurie DI, Pijak DS, Selzer ME, Lee VM. 1995. Glial cells of the lamprey nervous system contain keratin-like proteins. J Comp Neurol 355:199-210.
54. Monsul NT, Geisendorfer AR, Han PJ, Banik R, Pease ME, Skolasky RL Jr, Hoffman PN. 2004. Intraocular injection of dibutyryl cyclic AMP promotes axon regeneration in rat optic nerve. Exp Neurol 186:124-133.
55. Neumann S, Woolf CJ. 1999. Regeneration of dorsal column fibers into and beyond the lesion site following adult spinal cord injury [see Comment]. Neuron 23:83-91.
56. Neumann S, Bradke F, Tessier-Lavigne M, Basbaum AI. 2002. Regeneration of sensory axons within the injured spinal cord induced by intraganglionic cAMP elevation. Neuron 34:885-893.
57. Neumann S, Skinner K, Basbaum AI. 2005. Sustaining intrinsic growth capacity of adult neurons promotes spinal cord regeneration. Proc Natl Acad Sci U S A 102:16848-16852.
58. Nikulina E, Tidwell JL, Dai HN, Bregman BS, Filbin MT. 2004. The phosphodiesterase inhibitor rolipram delivered after a spinal cord lesion promotes axonal regeneration and functional recovery. Proc Natl Acad Sci U S A 101:8786-8790.
59. Nordlander RH. 1987. Axonal growth cones in the developing amphibian spinal cord. J Comp Neurol 263:485-496.
60. O'Connor TP, Bentley D. 1993. Accumulation of actin in subsets of pioneer growth cone filopodia in response to neural and epithelial guidance cues in situ. J Cell Biol 123:935-948.
61. Pant HC, Gallant PE, Gould R, Gainer H. 1982. Distribution of calcium-activated protease activity and endogenous substrates in the squid nervous system. J Neurosci 2:1578-1587.
62. Pant HC, Veeranna, Grant P. 2000. Regulation of axonal neurofilament phosphorylation. Curr Top Cell Regul 36:133-150.
63. Park K, Luo JM, Hisheh S, Harvey AR, Cui Q. 2004. Cellular mechanisms associated with spontaneous and ciliary neurotrophic factor-cAMP-induced survival and axonal regeneration of adult retinal ganglion cells. J Neurosci 24:10806-10815.
64. Pearse DD, Pereira FC, Marcillo AE, Bates ML, Berrocal YA, Filbin MT, Bunge MB. 2004. cAMP and Schwann cells promote axonal growth and functional recovery after spinal cord injury. Nat Med 10:610-616.
65. Pijak DS, Hall GF, Tenicki PJ, Boulos AS, Lurie DI, Selzer ME. 1996. Neurofilament spacing, phosphorylation, and axon diameter in regenerating and uninjured lamprey axons. J Comp Neurol 368:569-581.
66. Pleasure SJ, Selzer ME, Lee VM. 1989. Lamprey neurofilaments combine in one subunit the features of each mammalian NF triplet protein but are highly phosphorylated only in large axons. J Neurosci 9:698-709.
67. Posternak T. 1974. Cyclic AMP and cyclic GMP. Annu Rev Pharmacol 14:23-33.
68. Qiu J, Cai D, Dai H, McAtee M, Hoffman PN, Bregman BS, Filbin MT. 2002. Spinal axon regeneration induced by elevation of cyclic AMP. Neuron 34:895-903.
69. Richardson PM, Issa VM. 1984. Peripheral injury enhances central regeneration of primary sensory neurones. Nature 309:791-793.
70. Richardson PM, Verge VM. 1987. Axonal regeneration in dorsal spinal roots is accelerated by peripheral axonal transection. Brain Res 411: 406-408.
71. Roederer E, Goldberg NH, Cohen MJ. 1983. Modification of retrograde degeneration in transected spinal axons of the lamprey by applied DC current. J Neurosci 3:153-160.
72. Sah DW, Frank E. 1984. Regeneration of sensory-motor synapses in the spinal cord of the bullfrog. J Neurosci 4:2784-2791.
73. Schlaepfer WW, Hasler MB. 1979. Characterization of the calcium-induced disruption of neurofilaments in rat peripheral nerve. Brain Res 168: 299-309.
74. Schnell L, Schwab ME. 1990. Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors. Nature 343:269-272.
75. Selzer ME. 2003. Promotion of axonal regeneration in the injured CNS. Lancet Neurol 2:157-166.
76. Shifman MI, Selzer ME. 2000a. Expression of the netrin receptor UNC-5 in lamprey brain: modulation by spinal cord transection. Neurorehabil Neural Repair 14:49-58.
77. Shifman MI, Selzer ME. 2000b. In situ hybridization in wholemounted lamprey spinal cord: localization of netrin mRNA expression. J Neurosci Methods 104:19-25.
78. Shifman MI, Selzer ME. 2006. Semaphorins and their receptors in lamprey CNS: cloning, phylogenetic analysis, and developmental changes during metamorphosis. J Comp Neurol 497:115-132.
79. Shifman MI, Selzer ME. 2007. Differential expression of class 3 and 4 semaphorins and netrin in the lamprey spinal cord during regeneration. J Comp Neurol 501:631-646.
80. Shifman MI, Yumul RE, Laramore C, Selzer ME. 2009. Expression of the repulsive guidance molecule RGM and its receptor neogenin after spinal cord injury in sea lamprey. Exp Neurol, March 5. DOI:1016/ jexpneurol.2009.02.011.
81. Sicotte M, Tsatas O, Jeong SY, Cai CQ, He Z, David S. 2003. Immunization with myelin or recombinant Nogo-66/MAG in alum promotes axon regeneration and sprouting after corticospinal tract lesions in the spinal cord. Mol Cell Neurosci 23:251-263.
82. Sihag RK, Nixon RA. 1989. In vivo phosphorylation of distinct domains of the 70-kilodalton neurofilament subunit involves different protein kinases. J Biol Chem 264:457-464 [erratum J Biol Chem 1989;264: 4264].
83. Simonen M, Pedersen V, Weinmann O, Schnell L, Buss A, Ledermann B, Christ F, Sansig G, van der Putten H, Schwab ME. 2003. Systemic deletion of the myelin-associated outgrowth inhibitor Nogo-A improves regenerative and plastic responses after spinal cord injury. Neuron 38:201-211.
84. Spencer T, Domeniconi M, Filbin MT. 2006. Inhibitors of axonal regeneration. In: Selzer ME, Clarke S, Cohen LG, Duncan PW, Gage FH, editors. Textbook of neural repair and rehabilitation: neural repair and plasticity. Cambridge, UK: Cambridge University Press. p 365-389.
85. Sperry RW. 1944. Optic nerve regeneration with return of vision in anurans. J Neurophysiol 7:57-69.
86. Strautman AF, Cork RJ, Robinson KR. 1990. The distribution of free calcium in transected spinal axons and its modulation by applied electrical fields. J Neurosci 10:3564-3575.
87. Tang D, Selzer ME. 1979. Projections of lamprey spinal neurons determined by the retrograde axonal transport of horseradish peroxidase. J Comp Neurol 188:629-645.
88. Teng FY, Tang BL. 2006. Axonal regeneration in adult CNS neurons - signaling molecules and pathways. J Neurochem 96:1501-1508.
89. Tesser P, Jones PS, Schechter N. 1986. Elevated levels of retinal neurofilament mRNA accompany optic nerve regeneration. J Neurochem 47:1235-1243.
90. Vossler MR, Yao H, York RD, Pan MG, Rim CS, Stork PJ. 1997. cAMP activates MAP kinase and Elk-1 through a B-Raf-and Rap1-dependent pathway. Cell 89:73-82.
91. Wahl S, Barth H, Ciossek T, Aktories K, Mueller BK. 2000. Ephrin-A5 induces collapse of growth cones by activating Rho and Rho kinase. J Cell Biol 149:263-270.
92. Wang Q, Zheng JQ. 1998. cAMP-mediated regulation of neurotrophin-induced collapse of nerve growth cones. J Neurosci 18:4973-4984.
93. Wang KC, Koprivica V, Kim JA, Sivasankaran R, Guo Y, Neve RL, He Z. 2002. Oligodendrocyte-myelin glycoprotein is a Nogo receptor ligand that inhibits neurite outgrowth. Nature 417:941-944.
94. Wang H, Guo Z, Wu F, Long F, Cao X, Liu B, Zhu Z, Yao X. 2005. PKA-mediated protein phosphorylation protects ezrin from calpain I cleavage. Biochem Biophys Res Commun 333:496-501.
95. Wu D, Zhang Y, Bo X, Huang W, Xiao F, Zhang X, Miao T, Magoulas C, Subang MC, Richardson PM. 2007. Actions of neuropoietic cytokines and cyclic AMP in regenerative conditioning of rat primary sensory neurons. Exp Neurol 204:66-76.
96. Wujek JR, Lasek RJ. 1983. Correlation of axonal regeneration and slow component B in two branches of a single axon. J Neurosci 3:243-251.
97. Yin HS, Selzer ME. 1983. Axonal regeneration in lamprey spinal cord. J Neurosci 3:1135-1144.
98. Zhang G, Jin LQ, Sul JY, Haydon PG, Selzer ME. 2005. Live imaging of regenerating lamprey spinal axons. Neurorehabil Neural Repair 19:46-57.
99. Zheng B, Ho C, Li S, Keirstead H, Steward O, Tessier-Lavigne M. 2003. Lack of enhanced spinal regeneration in Nogo-deficient mice [see Comment]. Neuron 38:213-224.
100. Zheng B, Atwal J, Ho C, Case L, He XL, Garcia KC, Steward O, Tessier-Lavigne M. 2005. Genetic deletion of the Nogo receptor does not reduce neurite inhibition in vitro or promote corticospinal tract regeneration in vivo. Proc Natl Acad Sci U S A 102:1205-1210.
101. Zimmerman UJ, Schlaepfer WW. 1982. Characterization of a brain calcium-activated protease that degrades neurofilament proteins. Biochemistry 21:3977-3982.