Early gene expression during natural spinal cord regeneration in the salamander Ambystoma mexicanum

Journal of Neurochemistry

Volumn 101, Issue 1, 2007, Pages 27-40

  Monaghan, James R ^a   Walker, John A ^a   Page, Robert B ^a   Putta, Srikrishna ^a   Beachy, Christopher K ^b   Voss, S Randal ^a,c  

^a UNIVERSITY OF KENTUCKY   (United States)

^b MINOT STATE UNIVERSITY   (United States)

^c NONE   (United States)

Author keywords

Axolotl; In situ hybridization; Microarray; Regeneration; Salamander; Spinal cord

Indexed keywords

AMBYSTOMA MEXICANUM; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA MICROARRAY; DOWN REGULATION; EXTRACELLULAR MATRIX; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; IMMUNOHISTOCHEMISTRY; NERVE REGENERATION; NEUROCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; SALAMANDER; SPINAL CORD; SPINAL CORD INJURY; STATISTICAL SIGNIFICANCE; UPREGULATION;

AMBYSTOMA; ANIMALS; DOWN-REGULATION; EXTRACELLULAR MATRIX PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; NERVE REGENERATION; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; NEURONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RATS; RNA, MESSENGER; SPECIES SPECIFICITY; SPINAL CORD; SPINAL CORD INJURIES; STEM CELLS; UP-REGULATION;

AMBYSTOMA MEXICANUM; MAMMALIA; RATTUS; SALAMANDROIDEA;

EID: 33947202652     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.04344.x     Document Type: Article

References (65)

1. Aimone J. B., Leasure J. L., Perreau V. M. and Thallmair M. (2004) Spatial and temporal gene expression profiling of the contused rat spinal cord. The Christopher Reeve Paralysis Foundation Research Consortium. Exp. Neurol. 189, 204-211.
2. Bareyre F. M. and Schwab M. E. (2003) Inflammation, degeneration and regeneration in the injured spinal cord: insights from DNA microarrays. Trends Neurosci. 26, 555-563.
3. Bauer J. A. (1998) Hydroxocobalamins as biologically compatible donors of nitric oxide implicated in the acceleration of wound healing. Med. Hypotheses 51, 65-67.
4. Beck C. W., Christen B. and Slack J. M. (2003) Molecular pathways needed for regeneration of spinal cord and muscle in a vertebrate. Dev. Cell 5, 429-439.
5. Benjamini Y. and Hochberg Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Royal Stat. Soc. Ser. B 57, 289-300.
6. Bolstad B., Irizarry R., Gautier L. and Wu Z. (2005a) Preprocessing high-density oligonucleotide arrays, in Bioinformatics and Computational Biology Solutions Using R and Bioconductor (Gentleman R., Carey V., Huber W., Irizarry R. and Dudoit S., eds.), pp. 13-32. Springer, New York.
7. Bolstad B., Collin F., Brettschneider J., Simpson K., Cope L., Irizarry R. A. and Speed T. P. (2005b) Quality assessment of Affymetrix GeneChip data, in Bioinformatics and Computational Biology Solutions Using R and Bioconductor (Gentleman R., Carey V., Huber W., Irizarry R. and Dudoit S., eds.), pp. 33-47. Springer, New York.
8. Borgnon J., Djamouri F., Lorand I., Rico V. D., Loux N., Pages J. C., Franco D., Capron F. and Weber A. (2005) Follistatin allows efficient retroviral-mediated gene transfer into rat liver. Biochem. Biophys. Res. Commun. 328, 937.
9. Carlson M. R., Bryant S. V. and Gardiner D. M. (1998) Expression of Msx-2 during development, regeneration, and wound healing in axolotl limbs. J. Exp. Zool. 282, 715-723.
10. Carlson M. R. J., Komine Y., Bryant S. V. and Gardiner D. M. (2001) Expression of Hoxb13 and Hoxc10 in developing and regenerating axolotl limbs and tails. Dev. Biol. 229, 396-406.
11. Carmel J. B., Galante A., Soteropoulos P., Tolias P., Recce M., Young W. and Hart R. P. (2001) Gene expression profiling of acute spinal cord injury reveals spreading inflammatory signals and neuron loss. Physiol. Genomics 7, 201-213.
12. Caubit X., Nicolas S. and Le Parco Y. (1997) Possible roles for Wnt genes in growth and axial patterning during regeneration of the tail in urodele amphibians. Dev. Dyn. 210, 1-10.
13. Chernoff E. A., O'Hara C. M., Bauerle D. and Bowling M. (2000) Matrix metalloproteinase production in regenerating axolotl spinal cord. Wound Repair and Regeneration 8, 282-291.
14. Choe S. E., Boutros M., Michelson A. M., Church G. M. and Halfon M. S. (2005) Preferred analysis methods for Affymetrix GeneChips revealed by a wholly defined control dataset. Genome Biol. 6, R16.
15. Christensen R. N., Weinstein M. and Tassava R. A. (2002) Expression of fibroblast growth factors 4, 8, and 10 in limbs, flanks, and blastemas of Ambystoma. Dev. Dyn. 223, 193-203.
16. Corcoran J. P. and Ferretti P. (1997) Keratin 8 and 18 expression in mesenchymal progenitor cells of regenerating limbs is associated with cell proliferation and differentiation. Dev. Dyn. 210, 355-370.
17. Cui X., Hwang J. T., Qiu J., Blades N. J. and Churchill G. A. (2005) Improved statistical tests for differential gene expression by shrinking variance components estimates. Biostatistics 6, 59-75.
18. De Biase A., Knoblach S. M., Di Giovanni S., Fan C., Molon A., Hoffman E. P. and Faden A. I. (2005) Gene expression profiling of experimental traumatic spinal cord injury as a function of distance from impact site and injury severity. Physiol. Genomics 22, 368-381.
19. Di Giovanni S., Knoblach S. M., Brandoli C., Aden S. A., Hoffman E. P. and Faden A. I. (2003) Gene profiling in spinal cord injury shows role of cell cycle in neuronal death. Ann. Neurol. 53, 454-468.
20. Draghici S., Khatri P., Eklund A. C. and Szallasi Z. (2006) Reliability and reproducibility issues in DNA microarray measurements. Trends Genet. 22, 101-109.
21. Egar M. and Singer M. (1972) The role of ependyma in spinal cord regeneration in the urodele, Titurus. Exp. Neurol. 37, 422-430.
22. Hay E. and Fischman D. (1961) Origin of the blastema in regenerating limbs of the newt Triturus viridescens. An autoradiographic study using tritiated thymidine to follow cell proliferation and migration. Dev. Biol. 3, 26-59.
23. Hirota S., Ito A., Morii E., Wanaka A., Tohyama M., Kitamura Y. and Nomura S. (1992) Localization of mRNA for c-kit receptor and its ligand in the brain of adult rats: an analysis using in situ hybridization histochemistry. Brain Res. Mol. Brain Res. 1, 47-54.
24. Horimoto M., Fulop P., Derdak Z., Wands J. R. and Baffy G. (2004) Uncoupling protein-2 deficiency promotes oxidant stress and delays liver regeneration in mice. Hepatology 39, 386-392.
25. Irizarry R. A., Hobbs B., Collin F., Beazer-Barclay Y. D., Antonellis K. J., Scherf U. and Speed T. P. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249-264.
26. Iten L. E. and Bryant S. V. (1976) Stages of tail regeneration in the adult newt, Notophthalmus viridescens. J. Exp. Zool. 196, 283-292.
27. Jones J. and Corwin J. (1993) Replacement of lateral line sensory organs during tail regeneration in salamanders: Identification of progenitor cells and analysis of leukocyte activity. J. Neurosci. 13, 1022-1034.
28. Kawano Y. and Kypta R. (2003) Secreted antagonists of the Wnt signaling pathway. J. Cell Sci. 116, 2627-2634.
29. Kikkawa Y., Mochizuki Y., Miner J. H. and Mitaka T. (2005) Transient expression of laminin alpha1 chain in regenerating murine liver: restricted localization of laminin chains and nidogen-1. Exp. Cell Res. 305, 99-109.
30. Koussoulakos S., Margaritis L. H. and Anton H. J. (1999) Origin of renewed spinal ganglia during tail regeneration in urodeles. Dev. Neurosci. 21, 134-139.
31. Lee K. J. and Jessell T. M. (1999) The specification of dorsal cell fates in the vertebrate central nervous system. Ann. Rev. of Neurosci. 22, 261-294.
32. Lo D. C., Allen F. and Brockes J. P. (1993) Reversal of muscle differentiation during urodele limb regeneration. PNAS 90, 7230-7234.
33. Millenaar F. F., Okyere J., May S. T., van Zanten M., Voesenek L. A. and Peeters A. J. (2006) How to decide? Different methods of calculating gene expression from short oligonucleotide array data will give different results. BMC Bioinformatics 7, 137.
34. Müller H. (1864) Ueber regeneration der wirbelsäule und des rückenmarks bei Tritonen und Eidechsen. Abhandl. d. Senckenbergischen nature-forsch. Gesellsch 5, 113-136.
35. Myohara M., Niva C. C. and Lee J. M. (2006) Molecular approach to annelid regeneration: cDNA subtraction cloning reveals various novel genes that are upregulated during the large-scale regeneration of the oligochaete, Enchytraeus japonensis. Dev. Dyn. 235, 2051-2070.
36. Niemann C. (2006) Controlling the stem cell niche: right time, right place, right strength. BioEssays 28, 1-5.
37. Noble L. J., Donovan F., Igarashi T., Goussev S. and Werb Z. (2002) Matrix metalloproteinases limit functional recovery after spinal cord injury by modulation of early vascular events. J. Neurosci. 22, 7526-7535.
38. Nordlander R. H. and Singer M. (1978) The role of ependyma in regeneration of the spinal cord in the urodele amphibian tail. J. Comp. Neur. 180, 349-374.
39. O'Hara C. M. and Chernoff E. A. (1994) Growth factor modulation of injury-reactive ependymal cell proliferation and migration. Tissue Cell 26, 599-611.
40. Ohtake Y., Maruko A., Abe S., Fukumoto M. and Ohkubo Y. (2006) Effect of retinoic acid-induced transglutaminase on cell growth in regenerating liver. Biomed. Res. 27, 75-80.
41. Padhi B. K., Joly L., Tellis P., Smith A., Nanjappa P., Chevrette M., Ekker M. and Akimenko M. A. (2004) Screen for genes differentially expressed during regeneration of the zebrafish caudal fin. Dev. Dyn. 231, 527-541.
42. Page R. B., Monaghan J. R., Samuels A. K., Smith J. J., Beachy C. K. and Voss S. R. (2006) Microarray analysis identifies keratin loci as sensitive biomarkers for thyroid hormone disruption in salamanders (Ambystoma). Comp. Biochem. Physiol. Part C doi:10.1016/j.cbpc.2006.06.003.
43. Pfaffl M. W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucl. Acids Res. 29, e45.
44. Piatt J. (1955) Regeneration of the spinal cord in the salamander. J. Exp. Zool. 129, 177-207.
45. Profyris C., Cheema S. S., Zang D., Azari M. F., Boyle K. and Petratos S. (2004) Degenerative and regenerative mechanisms governing spinal cord injury. Neurobiol. Dis. 15, 415-436.
46. Putta S., Smith J. J., Walker J. A. et al. (2004) From biomedicine to natural history research: EST resources for ambystomatid salamanders. BMC Genomics 5, 54.
47. Rozen S. and Skaletsky H. (2000) Primer3 on the WWW for general users and for biologist programmers, in Bioinformatics Methods and Protocols: Methods in Molecular Biology (Krawetz S. and Misener S., eds.), pp. 365-386. Humana Press, Totowa, NJ.
48. Schnapp E., Kragl M., Rubin L. and Tanaka E. M. (2005) Hedgehog signaling controls dorsoventral patterning, blastema cell proliferation and cartilage induction during axolotl tail regeneration. Development 132, 3243-3253.
49. Song G., Cechvala C., Resnick D. K., Dempsey R. J. and Rao V. L. (2001) GeneChip® analysis after acute spinal cord injury in rat. J. Neurochem. 79, 804-815.
50. Spallanzani L. (1769) Prodromo di un opera da imprimersi sopra la riproduzioni animal: (An essay on animal reproduction), in Mati M. translation. T. Becket and de Hondt, London.
51. Stensaas L. J. (1983) Regeneration in the spinal cord of the newt Notopthalmus (Titurus) pyrrhogaster, in Spinal Cord Reconstruction (Kao C. C. and Reier P. J., eds.), pp. 121-150. Raven Press, New York.
52. Tassi E., Al-Attar A., Aigner A., Swift M. R., McDonnell K., Karavanov A. and Wellstein A. (2001) Enhancement of fibroblast growth factor (FGF) activity by an FGF-binding protein. J. Biol. Chem. 276, 40 247-40 253.
53. Teshigawara M., Matsumoto S., Tsuboi S. and Ohmori S. (1995) Changes in levels of glutathione and related compounds and activities of glutathione-related enzymes during rat liver regeneration. Res. Exp. Med. (Berl) 195, 55-60.
54. Torok M. A., Gardiner D. M., Izpisua-Belmonte J. C. and Bryant S. V. (1999) Sonic Hedgehog (shh) expression in developing and regenerating axolotl limbs. J. Exp. Zool. 284, 197-206.
55. Tsai J., Sultana R., Lee Y., Pertea G., Karamycheva S., Antonescu V., Cho J., Parvizi B., Cheung F. and Quackenbush J. (2001) RESOURCERER: a database for annotating and linking microarray resources within and across species. Genome Biol. 2, software0002.1-0002.4.
56. Vance J. E., Campenot R. B. and Vance D. E. (2000) The synthesis and transport of lipids for axonal growth and nerve regeneration. Biochim. Biophys. Acta 1486, 84-96.
57. Vazquez-Chona F. R., Khan A. N., Chan C. K. et al. (2005) Genetic networks controlling retinal injury. Mol. Vis. 11, 958-970.
58. Vergara M. N., Arsenijevic Y. and Del Rio-Tsonis K. (2005) CNS regeneration: a morphogen's tale. J. Neurobiol. 64, 491-507.
59. Vinarsky V., Atkinson D. L., Stevenson T. J., Keating M. T. and Odelberg S. J. (2005) Normal newt limb regeneration requires matrix metalloproteinase function. Dev. Biol. 279, 86-98.
60. Wells J. E. A., Rice T. K., Nuttall R. K., Edwards D. R., Zekki H. and Rivest S. (2003) An adverse role for matrix metalloproteinase 12 after spinal cord injury in mice. J. Neurosci. 23, 10 107-10 115.
61. Whitehead G. G., Makino S., Lien C. L. and Keating M. T. (2005) fgf20 Is Essential for Initiating Zebrafish Fin Regeneration. Science 310, 1957-1960.
62. Yang E. V., Gardiner D. M., Carlson M. R., Nugas C. A. and Bryant S. V. (1999) Expression of Mmp-9 and related matrix metalloproteinase genes during axolotl limb regeneration. Dev. Dyn. 216, 2-9.
63. Zhang F., Clarke J. and Ferretti P. (2000) FGF-2 Up-regulation and proliferation of neural progenitors in the regenerating amphibian spinal cord in vivo. Dev. Biol. 225, 381-391.
64. Zhang F., Clarke J., Santos-Ruiz L. and Ferretti P. (2002) Differential regulation of fibroblast growth factor receptors in the regenerating amphibian spinal cord in vivo. Neuroscience 114, 837-848.
65. Zhang F., Ferretti P. and Clarke J. (2003) Recruitment of postmitotic neurons into the regenerating spinal cord of urodeles. Dev. Dyn. 226, 341-348.