Lack of adenylate cyclase 1 (AC1): Consequences on corticospinal tract development and on locomotor recovery after spinal cord injury

Brain Research

Volumn 1549, Issue , 2014, Pages 1-10

  Nait Taleb Ali, H ^a,b,c   Morel, M P ^c   Doulazmi, M ^c   Scotto Lomassese, S ^b,c   Gaspar, P ^b,c   Dusart, I ^c   Bennis, M ^a  

^a FACULTÉ DES SCIENCES SEMLALIA   (Morocco)

^b INSTITUT DU FER À MOULIN   (France)

^c SORBONNE UNIVERSITÉ   (France)

Author keywords

Adenylate cyclase 1; Barrelless mice; Corticospinal tract; Spinal cord injury

Indexed keywords

ADENYLATE CYCLASE; ADENYLATE CYCLASE 1; FLUOROGOLD; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DENSITY; CERVICAL SPINAL CORD; CONTROLLED STUDY; GENE INACTIVATION; GENE MUTATION; LOCOMOTION; MOTOR CORTEX; MOTOR PERFORMANCE; MOTOR SYSTEM; MOUSE; NERVE FIBER; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; PYRAMIDAL TRACT; SPINAL CORD INJURY; SPINAL CORD MOTONEURON; TRANSGENIC MOUSE;

ANIMALIA; MUS;

ADENYLATE CYCLASE 1; BARRELLESS MICE; CORTICOSPINAL TRACT; SPINAL CORD INJURY;

ADENYLATE CYCLASE; ANIMALS; LOCOMOTION; MALE; MICE; MICE, MUTANT STRAINS; MOTOR NEURONS; PYRAMIDAL TRACTS; SPINAL CORD INJURIES;

EID: 84893983730     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2014.01.001     Document Type: Article

References (54)

1. R.M. Abdel-Majid, W.L. Leong, L.C. Schalkwyk, D.S. Smal lman, S.T. Wong, D.R. Storm, A. Fine, M.J. Dobson, D.L. Guernsey, and P.E Neumann Loss of adenylyl cyclase I activity disrupts patterning of mouse somatosensory cortex Nat. Genet. 19 1998 289 291
2. F.M. Bareyre, M. Kerschensteiner, O. Raineteau, T.C. Mettenleiter, O. Weinmann, and ME. Schwab The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats Nat. Neurosci. 7 2004 269 277
3. D.M. Basso, L.C. Fisher, A.J. Anderson, L.B. Jakeman, D.M. McTigue, and P.G. Popovich Basso Mouse Scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains J. Neurotrauma 23 2006 635 659
4. C. Brösamle, and M.E. Schwab Cells of origin, course, and termination patterns of the ventral, uncrossed component of the mature rat corticospinal tract J. Comp. Neurol. 386 1997 293 303
5. D. Cai, J. Qiu, Z. Cao, M. McAtee, B.S. Bregman, and M.T. Filbin Neuronal cyclic AMP controls the developmental loss in ability of axons to regenerate J. Neurosci. 21 2001 4731 4739
6. E. Camand, M.P. Morel, A. Faissner, C. Sotelo, and I. Dusart Long-term changes in the molecular composition of the glial scar and progressive increase of serotoninergic fibre sprouting after hemisection of the mouse spinal cord Eur. J. Neurosci. 20 2004 1161 1176
7. R.G. Corredor, E.F. Trakhtenberg, W. Pita-Thomas, X. Jin, Y. Hu, and J.L. Goldberg Soluble adenylyl cyclase activity is necessary for retinal ganglion cell survival and axon growth J. Neurosci. 32 2012 7734 7744
8. Q. Cui, and K.F. So Involvement of cAMP in neuronal survival and axonal regeneration Anat. Sci. Int. 79 2004 209 212
9. M. Dottori, L. Hartley, M. Galea, G. Paxinos, M. Polizzotto, T. Kilpatrick, P.F. Bartlett, M. Murphy, F. Kontgen, and A.W. Boyd EphA4 (Sek1) receptor tyrosine kinase is required for the development of the corticospinal tract Proc. Nat. Acad. Sci. U.S.A. 95 1998 13248 13253
10. R.L. Faulkner, L.K. Low, X.B. Liu, J. Coble, E.G. Jones, and H.J. Cheng Dorsal turning of motor corticospinal axons at the pyramidal decussation requires plexin signaling Neural Dev. 3 2008 21
11. G.D. Ferguson, and D.R. Storm Why calcium-stimulated adenylyl cyclases? Physiology (Bethesda) 19 2004 271 276
12. I. Ferrer, E. Soriano, J.A. Del Rio, S. Alcantara, and C. Auladell Cell death and removal in the cerebral cortex during development Prog. Neurobiol. 39 1992 1 43
13. J.H. Finger, R.T. Bronson, B. Harris, K. Johnson, S.A. Przyborski, and S.L. Ackerman The netrin 1 receptors Unc5h3 and Dcc are necessary at multiple choice points for the guidance of corticospinal tract axons J. Neurosci. 22 2002 10346 10356
14. K. Fouad, A. Krajacic, and W. Tetzlaff Spinal cord injury and plasticity: opportunities and challenges Brain Res. Bull. 84 2011 337 342
15. C. Haupt, J. Langhoff, and A.B. Huber Adenylate Cyclase 1 modulates peripheral nerve branching patterns Mol. Cell. Neurosci. 45 2010 439 448
16. D. Heumann, and G. Leuba Neuronal death in the development and aging of the cerebral cortex of the mouse Neuropathol. Appl. Neurobiol. 9 1983 297 311
17. D. Heumann, G. Leuba, and T. Rabinowicz Postnatal development of the mouse cerebral neocortex. IV. Evolution of the total cortical volume, of the population of neurons and glial cells J. Hirnforsch. 19 1978 385 393
18. L.B. Jakeman, Y. Chen, K.M. Lucin, and D.M. McTigue Mice lacking L1 cell adhesion molecule have deficits in locomotion and exhibit enhanced corticospinal tract sprouting following mild contusion injury to the spinal cord Eur. J. Neurosci. 23 2006 1997 2011
19. T. Kamiyama, N. Yoshioka, and M. Sakurai Synapse Elimination in the Corticospinal Projection during the early postnatal period J. Neurophysiol. 95 2006 2304 (-231)
20. K. Kullander, S.D. Croll, M. Zimmer, L. Pan, J. McClain, V. Hughes, S. Zabski, T.M. DeChiara, R. Klein, G.D. Yancopoulos, and N.W. Gale Ephrin-B3 is the midline barrier that prevents corticospinal tract axons from recrossing, allowing for unilateral motor control Genes Dev. 15 2001 877 888
21. H.C. Lu, W.C. She, D.T. Plas, P.E. Neumann, R. Janz, and M.C. Crair Adenylyl cyclase I regulates AMPA receptor trafficking during mouse cortical 'barrel' map development Nat. Neurosci. 6 2003 939 947
22. L. Luo, and D.D. O'Leary Axon retraction and degeneration in development and disease Annu. Rev. Neurosci. 28 2005 127 156
23. M. Ma, D.M. Basso, P. Walters, B.T. Stokes, and L.B. Jakeman Behavioral and histological outcomes following graded spinal cord contusion injury in the C57Bl/6 mouse Exp. Neurol. 169 2001 239 254
24. J.H. Martin, M. Choy, S. Pullman, and Z. Meng Corticospinal system development depends on motor experience J. Neurosci. 24 2004 2122 2132
25. A. Meyer-Franke, M.R. Kaplan, F.W. Pfrieger, and B.A. Barres Characterization of the signaling interactions that promote the survival and growth of developing retinal ganglion cells in culture Neuron 15 1995 805 819
26. X. Nicol, M. Bennis, Y. Ishikawa, G. Chan, D. Storm, and P. Gaspar The role of calcium modulated cyclases in the development of the retinal projections Eur. J. Neurosci. 24 2006 3401 3414
27. X. Nicol, A. Muzerelle, I. Bachy, A. Ravary, and P. Gaspar Spatiotemporal localization of the calcium-stimulated adenylate cyclases, AC1 and AC8, during mouse brain development J. Comp. Neurol. 486 2005 281 294
28. X. Nicol, A. Muzerelle, J.P. Rio, C. Metin, and P. Gaspar Requirement of adenylate cyclase 1 for the ephrin-A5-dependent retraction of exuberant retinal axons J. Neurosci. 26 2006 862 872
29. X. Nicol, S. Voyatzis, A. Muzerelle, N. Narboux-Nême, T.C. Südhof, R. Miles, and P. Gaspar cAMP oscillations and retinal activity are permissive for ephrin signaling during the establishment of the retinotopic map Nat. Neurosci. 10 2007 340 347
30. E. Nikulina, J.L. Tidwell, H.N. Dai, B.S. Bregman, and M.T. Filbin The phosphodiesterase inhibitor rolipram delivered after a spinal cord lesion promotes axonal regeneration and functional recovery Proc. Nat. Acad. Sci. U.S.A. 101 2004 8786 8790
31. T. Ohno, H. Maeda, and M. Sakurai Regionally specific distribution of corticospinal synapses because of activity-dependent synapse elimination in vitro J. Neurosci. 24 2004 1377 1384
32. T. Ohno, and M. Sakurai Critical period for activity-dependent elimination of Corticospinal synapses in vitro Neuroscience 132 2005 917 922
33. G. Paxinos, and K.B.J. Franklin The Mouse Brain in Stereotaxic Coordinates 2001 Academic Press San Diego
34. A.G. Peace, and D.A. Shewan New perspectives in cyclic AMP-mediated axon growth and guidance: the emerging epoch of Epac Brain Res. Bull. 84 2011 280 288
35. D.D. Pearse, F.C. Pereira, A.E. Marcillo, M.L. Bates, Y.A. Berrocal, M.T. Filbin, and M.B. Bunge cAMP and Schwann cells promote axonal growth and functional recovery after spinal cord injury Nat. Med. 10 2004 610 616
36. A. Ravary, A. Muzerelle, D. Herve, V. Pascoli, K.N. Ba-Charvet, J.A. Girault, E. Welker, and P. Gaspar Adenylate cyclase 1 as a key actor in the refinement of retinal projection maps J. Neurosci. 23 2003 2228 2238
37. M. Repici, X. Chen, M.P. Morel, M. Doulazmi, A. Sclip, V. Cannaya, P. Veglianese, R. Kraftsik, J. Mariani, T. Borsello, and I. Dusart Specific inhibition of the JNK pathway promotes locomotor recovery and neuroprotection after mouse spinal cord injury Neurobiol. Dis. 46 2012 710 721
38. B. Rolf, M. Bastmeyer, M. Schachner, and U. Bartsch Pathfinding errors of corticospinal axons in neural cell adhesion molecule-deficient mice J. Neurosci. 22 2002 8357 8362
39. E.S. Rosenzweig, J.H. Brock, M.D. Culbertson, P. Lu, R. Moseanko, V.R. Edgerton, L.A. Havton, and M.H. Tuszynski Extensive spinal decussation and bilateral termination of cervical corticospinal projections in rhesus monkeys J. Comp. Neurol. 513 2009 151 163
40. A.E. Rünker, G.E. Little, F. Suto, H. Fujisawa, and K.J. Mitchell Semaphorin-6A controls guidance of corticospinal tract axons at multiple choice points Neural Dev. 3 2008 34
41. S.M. Schaal, M.S. Garg, M. Ghosh, L. Lovera, M. Lopez, M. Patel, J. Louro, S. Patel, L. Tuesta, W.M. Chan, and D.D. Pearse The therapeutic profile of rolipram, PDE target and mechanism of action as a neuroprotectant following spinal cord injury PLoS One 7 9 2012 e43634
42. D. Shewan, A. Dwivedy, R. Anderson, and C.E. Holt Age-related changes underlie switch in netrin-1 responsiveness as growth cones advance along visual pathway Nat. Neurosci. 5 2002 955 962
43. P. Schucht, O. Raineteau, M.E. Schwab, and K. Fouad Anatomical correlates of locomotor recovery following dorsal and ventral lesions of the rat spinal cord Exp. Neurol. 176 2002 143 153
44. H. Song, G. Ming, Z. He, M. Lehmann, L. McKerracher, M. Tessier-Lavigne, and M. Poo Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides Science 281 1998 1515 1518
45. R. Spreafico, C. Frassoni, P. Arcelli, M. Selvaggio, and S. De Biasi In situ labeling of apoptotic cell death in the cerebral cortex and thalamus of rats during development J. Comp. Neurol. 363 1995 281 295
46. R.K. Sunahara, and R. Taussig Isoforms of mammalian adenylyl cyclase: multiplicities of signaling Mol. Interventions 2 2002 168 184
47. H. Takuma, M. Sakurai, and I. Kanazawa In vitro formation of corticospinal synapses in an organotypic slice co-culture Neuroscience 109 2002 359 370
48. C. Verney, T. Takahashi, P.G. Bhide, R.S. Nowakowski, and V.S. Caviness Jr. Independent controls for neocortical neuron production and histogenetic cell death Dev. Neurosci. 22 2000 125 138
49. A. Visel, G. Alvarez-Bolado, C. Thaller, and G. Eichele Comprehensive analysis of the expression patterns of the adenylate cyclase gene family in the developing and adult mouse brain J. Comp. Neurol. 496 2006 684 697
50. J.T. Voyvodic Cell death in cortical development: how much? Why? So what? Neuron 16 1996 693 696
51. E Welker, M. Armstrong-James, G. Bronchti, W. Ourednik, F. Gheorghita-Baechler, R. Dubois, D.L. Guernsey, H. Van der Loos, and P.E. Neumann Altered sensory processing in the somatosensory cortex of the mouse mutant barrelless Science 271 1996 1864 1867
52. D. Willoughby, and D.M. Cooper Organization and Ca2+ regulation of adenylyl cyclases in cAMP microdomains Physiol. Rev. 87 2007 965 1010
53. Z.L. Wu, S.A. Thomas, E.C. Villacres, Z. Xia, M.L. Simmons, C. Chavkin, R.D. Palmiter, and D.R. Storm Altered behavior and long-term potentiation in type I adenylyl cyclase mutant mice Proc. Nat. Acad. Sci. U.S.A. 92 1995 220 224
54. P. Yang, and Z. Yang Enhancing intrinsic growth capacity promotes adult CNS regeneration J. Neurol. Sci. 312 2012 1 6