Conditional genetic deletion of PTEN after a spinal cord injury enhances regenerative growth of CST axons and motor function recovery in mice

Experimental Neurology

Volumn 266, Issue , 2015, Pages 147-160

  Danilov, Camelia A ^a   Steward, Oswald ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Axon regeneration; Axonal growth; Corticospinal tract; CRE mediated recombination; CST; Motor system; Mouse; Recovery of function; Spinal cord injury; Sprouting

Indexed keywords

PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PTEN PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CONVALESCENCE; DISEASE SEVERITY; FEMALE; FIRST CERVICAL VERTEBRA; FORELIMB; FUNCTIONAL ASSESSMENT; GENE DELETION; GENETIC MANIPULATION; GRIP STRENGTH; LIMB MOVEMENT; MOTOR PERFORMANCE; MOUSE; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NONHUMAN; PRIORITY JOURNAL; PTEN GENE; PYRAMIDAL TRACT; SENSORIMOTOR CORTEX; SPINAL CORD INJURY; TASK PERFORMANCE; VOLUNTARY MOVEMENT; ANIMAL; CONTUSION; GENETICS; HAND STRENGTH; KNOCKOUT MOUSE; LOCOMOTION; NERVE FIBER; NERVE REGENERATION; PATHOLOGY;

ANIMALS; AXONS; CONTUSIONS; FEMALE; HAND STRENGTH; LOCOMOTION; MICE; MICE, KNOCKOUT; NERVE REGENERATION; PTEN PHOSPHOHYDROLASE; PYRAMIDAL TRACTS; RECOVERY OF FUNCTION; SPINAL CORD INJURIES;

EID: 84925638795     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2015.02.012     Document Type: Article

References (38)

1. Aguilar R.M., Steward O. A bilateral cervical contusion injury model in mice: assessment of gripping strength as a measure of forelimb motor function. Exp. Neurol. 2010, 221(1):38-53.
2. Anderson K.D., Gunawan A., Steward O. Quantitative assessment of forelimb motor function after cervical spinal cord injury in rats: relationship to corticospinal tract. Exp. Neurol. 2005, 194(1):161-174.
3. Anderson K.D., Sharp K.G., Steward O. Bilateral cervical contusion spinal cord injury rats. Exp. Neurol. 2009, 220(1):9-22.
4. Blanco J.E., Anderson K.D., Steward O. Recovery of forepaw gripping ability and reorganization of cortical motor control following cervical spinal cord injuries in mice. Exp. Neurol. 2007, 203(2):333-348.
5. Cafferty W.B., Duffy P., Huebner E., Strittmater S.M. MAG and OMgp synergize with Nogo-A to restrict axonal growth and neurological recovery after spinal cord trauma. J. Neurosci. 2010, 30(20):6825-6837. (19).
6. Cai D., Qiu J., Cao Z., McAtee M., Bregman B.S., Filbin M.T. Neuronal cyclic AMP controls the developmental loss in ability of neurons to regenerate. J. Neurosci. 2001, 21(13):4731-4739. (1).
7. Dang D.T., Pevsner J., Yang V.W. The biology of the mammalian Kruppel-like family of transcription factors. Int. J. Biochem. Cell Biol. 2000, 32:1103-1121. (Review).
8. Diener P.S., Bregman B.S. Fetal spinal cord transplants support the development of target reaching and coordinated postural adjustments after neonatal cervical spinal cord injury. J. Neurosci. 1998, 18(2):763-778.
9. Goldberg J.L. Intrinsic neuronal regulation of axon and dendrite growth. Curr. Opin. Neurobiol. 2004, 14(5):551-557. (Review).
10. Hellstrom M., Muhling J., Ehlert E.M., Verhaagen J., Pollett M.A., Hu Y., Harvey A.R. Negative impact of rAAV2 mediated expression of SOCS3 on the regulation of adult retinal ganglion cell axons. Mol. Cell. Neurosci. 2011, 46(2):507-515.
11. Kalil K., Schneider G.E. Retrograde cortical and axonal changes following lesions of the pyramidal tract. Brain Res. 1975, 89(1):15-27. (16).
12. Kanagal S.G., Muir G.D. The differential effects of cervical and thoracic dorsal funiculus lesions in rats. Behav. Brain Res. 2008, 187(2):379-386. (5).
13. Kartje-Tilllotson G., O'Donoghue D.L., Dauzvardis M.F., Castro A.J. Pyramidotomy abolishes the abnormal movements evoked by intracortical microstimulation in adult rats that sustained neonatal cortical lesions. Brain Res. 1987, 415(1):172-177. (7).
14. Lewandowski G., Steward O. AAVshRNA-mediated suppression of PTEN in adult rats in combination with salmon fibrin administration enables regenerative growth of corticospinal axons and enhances recovery of voluntary motor function after cervical spinal cord injury. J. Neurosci. 2014, 34:9951-9962.
15. Liu K., Lu Y., Lee J.K., Samara R., Willenberg R., Sears-Kraxberger I., Tedeski A., Park K.K., Jin D., Cai B., Xu B., Connolly L., Steward O., Zheng B., He Z. PTEN deletion enhances the regenerative ability of adult corticospinal neurons. Nat. Neurosci. 2010, 13(9):1075-1081.
16. Ma X.M., Blenis J. Molecular mechanisms of mTOR mediated translational control. Nat. Rev. Mol. Cell Biol. 2009, 10(5):307-318.
17. Moore D.L., Apara A., Goldberg J.L. Kruppel-like transcription factors in the nervous system: novel players in neurite outgrowth and axon regeneration. Mol. Cell. Neurosci. 2011, 47(4):233-243.
18. Muir G.D., Webb A.A., Kanagal S., Taylor L. Dorsolateral cervical spinal injury differentially affects forelimb and hindlimb action in rats. Eur. J. Neurosci. 2007, 25(5):1501-1510.
19. Ohtake Y., Park D., Abdule-Muneer P.M., Li H., Xu B., Sharma K., Smith G.M., Selzer M.E., Li S. The effect of systemic PTEN antagonist peptides on axon growth and functional recovery after spinal cord injury. Biomaterials 2014, 35:4610-4626.
20. Park K.K., Liu K., Hu Y., Smith P.D., Wang C., Cai B., Xu B., Connolly L., Kramvis I., Sahin M., He Z. Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science 2008, 322(5903):963-966.
21. Rodger J., Goto H., Cui Q., Chen P.B., Harvey A.R. cAMP regulates axon outgrowth and guidance during optic nerve regeneration in goldfish. Mol. Cell. Neurosci. 2005, 30(3):452-464.
22. Sabatini D.M. mTOR and cancer: insights into a complex relationship. Nat. Rev. Cancer 2006, 6(9):729-734.
23. Schieber M.H., Rivlis G. Partial reconstruction of muscle activity from a pruned network of diverse motor cortex neurons. J. Neurophysiol. 2007, 97(1):70-82.
24. Schrimsher G.W., Reier P.J. Forelimb motor performance following dorsal column, dorsolateral funiculi, or ventrolateral funiculi lesions of the cervical spinal cord in the rat. Exp. Neurol. 1993, 120(2):264-276.
25. Selzer M.E. Promotion of axon regeneration in the injured CNS. Lancet Neurol. 2003, 2(3):157-166.
26. Smith P.D., Sun F., Park K.K., Cai B., Wang C., Kuwako K., Martinez-Carrasco I., Connolly L., He Z. Socs3 deletion promotes optic nerve regeneration in vivo. Neuron 2009, 64:617-623.
27. Steward O., Zheng B., Ho C., Anderson K., Tessier-Lavigne M. The dorsolateral corticospinal trct in mice: an alternative route for corticospinal input to caudal segments following dorsal column lesions. J. Comp. Neurol. 2004, 472(4):463-477. (10).
28. Strong M.K., Blanco J.E., Anderson K.D., Lewandowski G., Steward O. An investigation of the cortical control of forepaw gripping after cervical hemisection injuries in rats. Exp. Neurol. 2009, 217(1):96-107.
29. Sun F., He Z. Neuronal intrinsic barriers for axon regeneration in the adult CNS. Curr. Opin. Neurobiol. 2010, 20(4):510-518.
30. Sun F., Park K.K., Belin S., Wang D., Lu T., Chen G., Zhang K., Yeung C., Feng G., Yankner B.A., He Z. Sustained axon regeneration induced by co-deletion of PTEN and SOCS3. Nature 2011, 480:372-375.
31. Tang X., Davies J.E., Davies S.J.A. Changes in distribution, cell associations, and protein expression levels of NG2, neurocan, phosphocan, brevican, versicanV2, and tenascin-C during acute to chronic maturation of spinal cord scar tissue. J. Neurosci. Res. 2003, 71(3):427-444. (1).
32. Thallmair M., Metz G.A., Z'Graggen W.J., Raineteau O., Kartje G.L., Schwab M.E. Neurite growth inhibitors restrict plasticity and functional recovery following corticospinal tract lesions. Nat. Neurosci. 1998, 1(2):124-131.
33. Verma P., Chierzi S., Codd A.M., Campbell D.S., Meyer R.L., Holt C.E., Fawcett J.W. Axonal protein synthesis and degradation are necessary for efficient growth cone regeneration. J. Neurosci. 2005, 25(2):331-342. (12).
34. Wanner I.B., Deik A., Torres M., Rosendahl A., Neary J.T., Lemmon V.P., Bixby J.L. A new in vitro model of the glial scar inhibits axon growth. Glia 2008, 56(15):1691-1709. (15).
35. Whishaw I.Q., Metz G.A. Absence of impairments or recovery mediated by the uncrossed pyramidal tract in the rat versus enduring deficits produced by the crossed pyramidal tract. Behav. Brain Res. 2002, 134(1-2):323-336.
36. Whishaw I.Q., Pellis S.M., Pellis V.C. A behavioral study of the contribution of cells and fibers of passage in the red nucleus of the rat to postural righting, skilled movements, and learning. Behav. Brain Res. 1992, 52(1):29-44. (30).
37. Whishaw I.Q., Sarna J.R., Pellis S.M. Evidence for rodent-common and species typical limb and digit use in eating, derived from a comparative analysis of ten rodent species. Behav. Brain Res. 1998, 96(1-2):79-91.
38. Zukor K., Belin S., Wang C., Keelan N., Wang X., He Z. Short hairpin RNA against PTEN enhances regenerative growth of corticospinal tract axons after spinal cord injury. J. Neurosci. 2013, 33(39):15350-15361. (25).