Live imaging of axon stretch growth in embryonic and adult neurons

Journal of Neurotrauma

Volumn 28, Issue 11, 2011, Pages 2389-2403

  Loverde, Joseph R ^a,b   Ozoka, Vivian C ^a   Aquino, Robert ^a   Lin, Ling ^a   Pfister, Bryan J ^a  

^a NEW JERSEY INSTITUTE OF TECHNOLOGY   (United States)

^b UNIVERSITY OF MEDICINE AND DENTISTRY OF NEW JERSEY   (United States)

Author keywords

axon stretch; bioreactor; development; live imaging; nerve growth

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOREACTOR; EMBRYO; IMAGING; MITOCHONDRION; NERVE CELL; NERVE CELL CULTURE; NERVE FIBER GROWTH; NERVE REGENERATION; NONHUMAN; RAT; SPINAL GANGLION; TENSION;

AGE FACTORS; ANIMALS; AXONS; CELL CULTURE TECHNIQUES; CELLS, CULTURED; EMBRYONIC STEM CELLS; NEURONS; RATS; TIME-LAPSE IMAGING;

EID: 80355148800     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2010.1598     Document Type: Article

References (67)

1. Anderson, D.K., Howland, D.R., and Reier, P.J.1995).Fetal neural grafts and repair of the injured spinal cord. Brain Pathol. 5, 451-457.
2. Bareyre, F.M., Kerschensteiner, M., Raineteau, O., Mettenleiter, T.C., Weinmann, O., and Schwab, M.E.2004).The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats. Nat. Neurosci. 7, 269-277.
3. Battiston, B, Buffoli, P, Vigasio, A, Brunelli, G., and Antonini, L.1992).The effects of lengthening on nerves. Ital. J. Orthop. Traumatol. 18, 79-86.
4. Blight, A.R.2004).Just one word: Plasticity. Nat. Neurosci. 7, 206-208.
5. Bray, D.1984).Axonal growth in response to experimentally applied mechanical tension. Dev. Biol. 102, 379-389.
6. Bunge, M.B.2001).Bridging areas of injury in the spinal cord. Neuroscientist 7, 325-339.
7. Bunge, M.B., and Pearse, D.D.2003).Transplantation strategies to promote repair of the injured spinal cord. J. Rehabil. Res. Dev. 40, 55-62.
8. Dagg, A.I., and Foster, J.B.1982).The Giraffe. Its Biology, Behavior, and Ecology. Krieger Publishing Company: Malabar, FL. David, S., and Aguayo, A.J.1981).Axonal elongation into peripheral nervous system "bridges" after central nervous system injury in adult rats. Science 214, 931-933.
9. David, S, and Lacroix, S.2003).Molecular approaches to spinal cord repair. Annu. Rev. Neurosci. 26, 411-440.
10. De Filippo, R.E., and Atala, A.2002).Stretch and growth: The molecular and physiologic influences of tissue expansion. Plast. Reconstr. Surg. 109, 2450-2462.
11. Del Frari, B., Pulzl, P., Schoeller, T., Widschwendter, M., and Wechselberger, G.2004).Pregnancy as a tissue expander in the correction of a scar deformity. Am. J. Obstet. Gynecol. 190, 579-580.
12. Dennerll, T.J., Lamoureux, P., Buxbaum, R.E., and Heidemann, S.R.1989).The cytomechanics of axonal elongation and retraction. J. Cell Biol. 109, 3073-3083.
13. Dickson, B.J.2002).Molecular mechanisms of axon guidance. Science 298, 1959-1964.
14. Dodla, M.C., and Bellamkonda, R.V.2008).Differences between the effect of anisotropic and isotropic laminin and nerve growth factor presenting scaffolds on nerve regeneration across long peripheral nerve gaps. Biomaterials 29, 33-46.
15. Elwood, E.T., Ingram, W.L., and Carlson, G.W.2000).Pregnancy as a tissue expander in the repair of a massive ventral hernia. Ann. Plast. Surg. 45, 431-433.
16. Evans, G.R.2001).Peripheral nerve injury: A reviewand approach to tissue engineered constructs. Anat. Rec. 263, 396-404.
17. Fawcett, J.2002).Repair of spinal cord injuries: where are we, where are we going? Spinal Cord 40, 615-623.
18. Fry, E.J.2001).Central nervous system regeneration: mission impossible? Clin. Exp. Pharmacol. Physiol. 28, 253-258.
19. Geller, H.M., and Fawcett, J.W.2002).Building a bridge: engineering spinal cord repair. Exp. Neurol. 174, 125-136.
20. Hall, S.2001).Nerve repair: A neurobiologist's view. J. Hand Surg. [Br.] 26, 129-136.
21. Heidemann, S.R., and Buxbaum, R.E.1990).Tension as a regulator and integrator of axonal growth. Cell Motil. Cytoskeleton 17, 6-10.
22. Heidemann, S.R., and Buxbaum, R.E.1994).Mechanical tension as a regulator of axonal development. Neurotoxicology 15, 95-107.
23. Heidemann, S.R., Lamoureux, P., and Buxbaum, R.E.1995).Cytomechanics of axonal development. Cell Biochem. Biophys. 27, 135-155.
24. Houle, J.D., and Tessler, A.2003).Repair of chronic spinal cord injury. Exp. Neurol. 182, 247-260.
25. Houle, J.D., Tom, V.J., Mayes, D., Wagoner, G., Phillips, N., and Silver, J.2006).Combining an autologous peripheral nervous system "bridge" and matrix modification by chondroitinase allows robust, functional regeneration beyond a hemisection lesion of the adult rat spinal cord. J. Neurosci. 26, 7405-7415.
26. Hu, J., Tang, Z., Wang, D., and Buckley, M.J.2001).Changes in the inferior alveolar nerve after mandibular lengthening with different rates of distraction. J. Oral Maxillofac. Surg. 59, 1041- 1045; discussion 1046.
27. Huang, J.H., Zager, E.L., Zhang, J., Groff, R.F., Pfister, B.J., Cohen, A.S., Grady, M.S., Maloney-Wilensky, E., and Smith, D.H.2008).Harvested human neurons engineered as live nervous tissue constructs: implications for transplantation. Laboratory investigation. J. Neurosurg. 108, 343-347.
28. Hudson, T.W., Evans, G.R., and Schmidt, C.E.1999).Engineering strategies for peripheral nerve repair. Clin. Plast. Surg. 26, 617-628, ix.
29. Hulsebosch, C.E.2002).Recent advances in pathophysiology and treatment of spinal cord injury. Adv. Physiol. Educ. 26, 238-255.
30. Imaizumi, T., Lankford, K.L., and Kocsis, J.D.2000).Transplantation of olfactory ensheathing cells or Schwann cells restores rapid and secure conduction across the transected spinal cord. Brain Res. 854, 70-78.
31. Iwahira, Y., and Maruyama, Y.1993).Combined tissue expansion: Clinical attempt to decrease pain and shorten placement time. Plast. Reconstr. Surg. 91, 408-415.
32. Jain, A., Kim, Y.T., McKeon, R.J., and Bellamkonda, R.V.2006).In situ gelling hydrogels for conformal repair of spinal cord defects, and local delivery of BDNF after spinal cord injury. Biomaterials 27, 497-504.
33. Johnson, T.M., Lowe, L., Brown, M.D., Sullivan, M.J., and Nelson, B.R.1993).Histology and physiology of tissue expansion. J. Dermatol. Surg. Oncol. 19, 1074-1078.
34. Kroeber, M.W., Diao, E., Hida, S., and Liebenberg, E.2001).Peripheral nerve lengthening by controlled isolated distraction: A new animal model. J. Orthop. Res. 19, 70-77.
35. Lamoureux, P., Heidemann, S.R., Martzke, N.R., and Miller, K.E.2010).Growth and elongation within and along the axon. Dev. Neurobiol. 70, 135-149.
36. Lee, S.K., and Wolfe, S.W.2000).Peripheral nerve injury and repair. J. Am. Acad. Orthop. Surg. 8, 243-252.
37. Loverde, J.R., Tolentino, R.E., and Pfister, B.J.2011).Axon stretch growth: The mechanotrasduction of neuronal growth. J. Visualized Experiments. 54.
38. Malis, D.J., MacMillan, J.G., Kelley, J.L., and McGath, J.H.1995).Tissue expansion of the facial nerve in an animal model. Ear Nose Throat J. 74, 261-270.
39. McDonald, J.W.1999).Repairing the damaged spinal cord. Sci. Am. 281, 64-73.
40. McDonald, J.W, Liu, X.Z, Qu, Y., Liu, S., Mickey, S.K., Turetsky, D., Gottlieb, D.I., and Choi, D.W.1999).Transplanted embryonic stem cells survive, differentiate and promote recovery in injured rat spinal cord. Nat. Med. 5, 1410-1412.
41. McKerracher, L.2001).Spinal cord repair: strategies to promote axon regeneration. Neurobiol. Dis. 8, 11-18.
42. Miller, K.E., and Sheetz, M.P.2006).Direct evidence for coherent low velocity axonal transport of mitochondria. J. Cell Biol. 173, 373-381.
43. Miya, D., Giszter, S., Mori, F., Adipudi, V., Tessler, A., and Murray, M.1997).Fetal transplants alter the development of function after spinal cord transection in newborn rats. J. Neurosci. 17, 4856-4872.
44. O'Toole, M., Lamoureux, P., and Miller, K.E.2008).A physical model of axonal elongation: force, viscosity, and adhesions govern the mode of outgrowth. Biophys. J. 94, 2610-2620.
45. Park, B.W., Kim, J.R., Lee, J.H., and Byun, J.H.2006).Expression of nerve growth factor and vascular endothelial growth factor in the inferior alveolar nerve after distraction osteogenesis. Int. J. Oral Maxillofac. Surg. 35, 624-630.
46. Park, K.I., Liu, S., Flax, J.D., Nissim, S., Stieg, P.E., and Snyder, E.Y.1999).Transplantation of neural progenitor and stem cells: Developmental insights may suggest new therapies for spinal cord and other CNS dysfunction. J. Neurotrauma 16, 675-687.
47. Pfister, B.J., Bonislawski, D.P., Smith, D.H., and Cohen, A.S.2006a).Stretch-grown axons retain the ability to transmit active electrical signals. FEBS Lett. 580, 3525-3531.
48. Pfister, B.J., Gordon, T., Loverde, J.R., Kochar, A.S., Mackinnon, S.E., and Cullen, D.K.2011).Biomedical engineering strategies for peripheral nerve repair: Surgical applications, state of the art, and future challenges. Crit. Rev. Biomed. Engineering, 39, 81-124.
49. Pfister, B.J., Iwata, A., Meaney, D.F., and Smith, D.H.2004).Extreme stretch-growth of integrated axons. J. Neurosci. 24, 7978-7983.
50. Pfister, B.J., Iwata, A., Taylor, A.G., Wolf, J.A., Meaney, D.F., and Smith, D.H.2006b).Development of transplantable nervous tissue constructs comprised of stretch-grown axons. J. Neurosci. Methods 153, 95-103.
51. Ramon-Cueto, A., Cordero, M.I., Santos-Benito, F.F., and Avila, J.2000).Functional recovery of paraplegic rats and motor axon regeneration in their spinal cords by olfactory ensheathing glia. Neuron 25, 425-435.
52. Riordan, C., Budny, P., and Regan, P.2003).Pregnancy as an autologous tissue expander for closure of an abdominal-wall defect. Br. J. Plast. Surg. 56, 64-66.
53. Schmidt, C.E., and Leach, J.B.2003).Neural tissue engineering: strategies for repair and regeneration. Annu. Rev. Biomed. Eng. 5, 293-347.
54. Smith, D.H., Wolf, J.A., and Meaney, D.F.2001).A new strategy to produce sustained growth of central nervous system axons: Continuous mechanical tension. Tissue Eng. 7, 131-139.
55. Stichel, C.C., and Muller, H.W.1998).Experimental strategies to promote axonal regeneration after traumatic central nervous system injury. Prog. Neurobiol. 56, 119-148.
56. Swanson, N.A., and Argenta, L.C.1988).Tissue expansion. Adv. Dermatol. 3, 243-258.
57. Takei, T., Mills, I., Arai, K., and Sumpio, B.E.1998).Molecular basis for tissue expansion: Clinical implications for the surgeon. Plast. Reconstr. Surg. 102, 247-258.
58. Tang, Z.L., Hu, J., Li, J.H., and Zou, S.J.2004).Effect of nerve growth factor and Schwann cells on axon regeneration of distracted inferior alveolar nerve following mandibular lengthening. Chin. J. Traumatol. 7, 81-86.
59. Tessier-Lavigne, M., and Goodman, C.S.1996).The molecular biology of axon guidance. Science 274, 1123-1133.
60. Tom, V.J., and Houle, J.D.2008).Intraspinal microinjection of chondroitinase ABC following injury promotes axonal regeneration out of a peripheral nerve graft bridge. Exp. Neurol. 211, 315-319.
61. Vekris, M.D., Bates, M., and Terzis, J.K.1999).Optimal time for distraction osteogenesis in limbs with nerve repairs: experimental study in the rat. J. Reconstr. Microsurg. 15, 191-201.
62. Whitesides, L.M., and Meyer, R.A.2004).Effect of distraction osteogenesis on the severely hypoplastic mandible and inferior alveolar nerve function. J. Oral Maxillofac. Surg. 62, 292-297.
63. Wood, F.M., and McMahon, S.B.1989).The response of the peripheral nerve field to controlled soft tissue expansion. Br. J. Plast. Surg. 42, 682-686.
64. Yu, T.W., and Bargmann, C.I.2001).Dynamic regulation of axon guidance. Nat. Neurosci. 4 (Suppl.), 1169-1176.
65. Zeng, Y.J., Xu, C.Q., Yang, J., Sun, G.C., and Xu, X.H.2003). Biomechanical comparison between conventional and rapid expansion of skin. Br. J. Plast. Surg. 56, 660-666.
66. Zheng, J., Lamoureux, P., Santiago, V., Dennerll, T., Buxbaum, R.E., and Heidemann, S.R.1991).Tensile regulation of axonal elongation and initiation. J. Neurosci. 11, 1117-1125.
67. Zompa, E.A., Cain, L.D., Everhart, A.W., Moyer, M.P., and Hulsebosch, C.E.1997).Transplant therapy: Recovery of function after spinal cord injury. J. Neurotrauma 14, 479-506.