Signaling proteins in spinal parenchyma and dorsal root ganglion in rat with spinal injury-induced spasticity

Journal of Proteomics

Volumn 91, Issue , 2013, Pages 41-57

  Kupcova Skalnikova, Helena ^a   Navarro, Roman ^b   Marsala, Silvia ^b   Hrabakova, Rita ^a   Vodicka, Petr ^a,c   Gadher, Suresh Jivan ^d   Kovarova, Hana ^a   Marsala, Martin ^b,e  

^a INSTITUTE OF ANIMAL PHYSIOLOGY AND GENETICS   (Czech Republic)

^b University of California   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d Life Technologies Inc   (United States)

^e Slovak Academy of Sciences   (Singapore)

Author keywords

Dorsal root ganglia; Hyper reflexia; Proteomic profiling; Spasticity; Spinal cord trauma; Spinal gray matter

Indexed keywords

ABELSON KINASE; ANGIOPOIETIN 1; ATM PROTEIN; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE IV; CASEIN KINASE II; CASPASE 3; CASPASE 7; CASPASE 9; CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE 2; DEATH ASSOCIATED PROTEIN KINASE; FOCAL ADHESION KINASE; HEAT SHOCK PROTEIN 27; INITIATION FACTOR 4G; INTEGRIN LINKED KINASE; MACROPHAGE ACTIVATING FACTOR; MITOGEN ACTIVATED PROTEIN KINASE 12; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE 4; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN KINASE C DELTA; PROTEIN KINASE LCK; PROTEIN KINASE ZAP 70; PROTEIN SH2; PROTEIN TYROSINE PHOSPHATASE SHP 2; SOMATOMEDIN RECEPTOR; STRESS ACTIVATED PROTEIN KINASE 1; TAU PROTEIN;

AMINO ACID SEQUENCE; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DOWN REGULATION; GENE SILENCING; GRAY MATTER; IMMUNOFLUORESCENCE; MALE; MICROARRAY ANALYSIS; MUSCLE STRETCHING; NERVE DEGENERATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; QUALITY OF LIFE; RAT; SIGNAL TRANSDUCTION; SPASTICITY; SPINAL CORD VENTRAL HORN; SPINAL GANGLION; SPINE INJURY; TRANSLATIONAL RESEARCH; UPREGULATION; WESTERN BLOTTING;

AMPA; ANGIOPOIETIN-1 RECEPTOR-TYROSINE KINASE; C-JUN N-TERMINAL KINASE; CALCIUM/CALMODULIN-DEPENDENT PROTEIN-SERINE KINASE; CAMK; CAMP RESPONSE ELEMENT BINDING PROTEIN; CASEIN PROTEIN-SERINE KINASE; CASP; CK; CREB; DORSAL ROOT GANGLIA; DORSAL ROOT GANGLION; DRG; EIF4G; ELECTROMYOGRAPHY; EMG; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ENOS; ERK; EUKARYOTIC TRANSLATION INITIATION FACTOR 4 GAMMA; EXTRACELLULAR SIGNAL-REGULATED KINASE; FAK; FGFR; FIBROBLAST GROWTH FACTOR RECEPTOR; FOCAL ADHESION PROTEIN-TYROSINE KINASE; GABA; GAMMA-AMINOBUTYRIC ACID; HYPER-REFLEXIA; I2D; IGFR; INDUCIBLE NITRIC OXIDE SYNTHASE; INOS; INSULIN-LIKE GROWTH FACTOR RECEPTOR; INTEROLOGOUS INTERACTION DATABASE; JNK; LCK; LONG-TERM POTENTIATION; LTP; LYMPHOCYTE-SPECIFIC PROTEIN-TYROSINE KINASE; MACROPHAGE-STIMULATING PROTEIN; MACROPHAGE-STIMULATING PROTEIN RECEPTOR ALPHA CHAIN; MAPK; MAPK/ERK KINASE KINASE 4; MEKK4; MITOGEN-ACTIVATED PROTEIN KINASE; MSP; N-METHYL D-ASPARTATE; NMDA; PK; PRO-CASPASE; PROTEIN KINASE; PROTEOMIC PROFILING; RONΑ; SCI; SPASTICITY; SPINAL CORD INJURY; SPINAL CORD TRAUMA; SPINAL GRAY MATTER; TEK/TIE2; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR; VEGFR; Α-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID;

ANIMALS; ANTIBODIES; GANGLIA, SPINAL; GENE EXPRESSION REGULATION; MALE; MICROARRAY ANALYSIS; NEOVASCULARIZATION, PATHOLOGIC; NEURODEGENERATIVE DISEASES; PHOSPHORYLATION; PROTEIN INTERACTION MAPPING; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; SPINAL CORD; SPINAL INJURIES;

EID: 84881489360     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2013.06.028     Document Type: Article

References (73)

1. Lance J.W. Spasticity: disordered motor control. Symposium synopsis 1980, 485-494. Year Book Medical Publishers, Chicago. R.G. Feldman, R.R. Young, W.P. Koella (Eds.).
2. Maurice V., Allan H.R., Raymond D.A. Adams & Victor's principles of neurology 2001, McGraw-Hill Companies. 7th ed.
3. Thuret S., Moon L.D., Gage F.H. Therapeutic interventions after spinal cord injury. Nat Rev Neurosci 2006, 7:628-643.
4. Elbasiouny S.M., Moroz D., Bakr M.M., Mushahwar V.K. Management of spasticity after spinal cord injury: current techniques and future directions. Neurorehabil Neural Repair 2010, 24:23-33.
5. Nielsen J.B., Crone C., Hultborn H. The spinal pathophysiology of spasticity-from a basic science point of view. Acta Physiol (Oxf) 2007, 189:171-180.
6. Noreau L., Proulx P., Gagnon L., Drolet M., Laramee M.T. Secondary impairments after spinal cord injury: a population-based study. Am J Phys Med Rehabil 2000, 79:526-535.
7. Boulenguez P., Liabeuf S., Bos R., Bras H., Jean-Xavier C., Brocard C., et al. Down-regulation of the potassium-chloride cotransporter KCC2 contributes to spasticity after spinal cord injury. Nat Med 2010, 16:302-307.
8. Li Y., Gorassini M.A., Bennett D.J. Role of persistent sodium and calcium currents in motoneuron firing and spasticity in chronic spinal rats. J Neurophysiol 2004, 91:767-783.
9. Marsala M., Hefferan M.P., Kakinohana O., Nakamura S., Marsala J., Tomori Z. Measurement of peripheral muscle resistance in rats with chronic ischemia-induced paraplegia or morphine-induced rigidity using a semi-automated computer-controlled muscle resistance meter. J Neurotrauma 2005, 22:1348-1361.
10. Siddall P., Xu C.L., Cousins M. Allodynia following traumatic spinal cord injury in the rat. Neuroreport 1995, 6:1241-1244.
11. Eide P.K., Stubhaug A., Stenehjem A.E. Central dysesthesia pain after traumatic spinal cord injury is dependent on N-methyl-d-aspartate receptor activation. Neurosurgery 1995, 37:1080-1087.
12. Katz R. Presynaptic inhibition in humans: a comparison between normal and spastic patients. J Physiol Paris 1999, 93:379-385.
13. Mazzocchio R., Rossi A. Involvement of spinal recurrent inhibition in spasticity. Further insight into the regulation of Renshaw cell activity. Brain 1997, 120(Pt 6):991-1003.
14. Boorman G.I., Lee R.G., Becker W.J., Windhorst U.R. Impaired "natural reciprocal inhibition" in patients with spasticity due to incomplete spinal cord injury. Electroencephalogr Clin Neurophysiol 1996, 101:84-92.
15. Remy-Neris O., Barbeau H., Daniel O., Boiteau F., Bussel B. Effects of intrathecal clonidine injection on spinal reflexes and human locomotion in incomplete paraplegic subjects. Exp Brain Res 1999, 129:433-440.
16. Krach L.E. Pharmacotherapy of spasticity: oral medications and intrathecal baclofen. J Child Neurol 2001, 16:31-36.
17. Kamen L., Henney H.R., Runyan J.D. A practical overview of tizanidine use for spasticity secondary to multiple sclerosis, stroke, and spinal cord injury. Curr Med Res Opin 2008, 24:425-439.
18. ElBasiouny S.M., Schuster J.E., Heckman C.J. Persistent inward currents in spinal motoneurons: important for normal function but potentially harmful after spinal cord injury and in amyotrophic lateral sclerosis. Clin Neurophysiol 2010, 121:1669-1679.
19. Hefferan M.P., Kucharova K., Kinjo K., Kakinohana O., Sekerkova G., Nakamura S., et al. Spinal astrocyte glutamate receptor 1 overexpression after ischemic insult facilitates behavioral signs of spasticity and rigidity. J Neurosci 2007, 27:11179-11191.
20. Oshiro M., Hefferan M.P., Kakinohana O., Lukacova N., Sugahara K., Yaksh T.L., et al. Suppression of stretch reflex activity after spinal or systemic treatment with AMPA receptor antagonist NGX424 in rats with developed baclofen tolerance. Br J Pharmacol 2010, 161:976-985.
21. Gao Y.J., Ji R.R. Chemokines, neuronal-glial interactions, and central processing of neuropathic pain. Pharmacol Ther 2010, 126:56-68.
22. Cruz C.D., Cruz F. The ERK 1 and 2 pathway in the nervous system: from basic aspects to possible clinical applications in pain and visceral dysfunction. Curr Neuropharmacol 2007, 5:244-252.
23. Ji R.R., RWt Gereau, Malcangio M., Strichartz G.R. MAP kinase and pain. Brain Res Rev 2009, 60:135-148.
24. Wang Y., Wu J., Lin Q., Nauta H., Yue Y., Fang L. Effects of general anesthetics on visceral pain transmission in the spinal cord. Mol Pain 2008, 4:50.
25. Willis W.D. Role of neurotransmitters in sensitization of pain responses. Ann N Y Acad Sci 2001, 933:142-156.
26. Aimone J.B., Leasure J.L., Perreau V.M., Thallmair M. Spatial and temporal gene expression profiling of the contused rat spinal cord. Exp Neurol 2004, 189:204-221.
27. Bareyre F.M., Schwab M.E. Inflammation, degeneration and regeneration in the injured spinal cord: insights from DNA microarrays. Trends Neurosci 2003, 26:555-563.
28. Ding Q., Wu Z., Guo Y., Zhao C., Jia Y., Kong F., et al. Proteome analysis of up-regulated proteins in the rat spinal cord induced by transection injury. Proteomics 2006, 6:505-518.
29. Chen A., McEwen M.L., Sun S., Ravikumar R., Springer J.E. Proteomic and phosphoproteomic analyses of the soluble fraction following acute spinal cord contusion in rats. J Neurotrauma 2010, 27:263-274.
30. Kang S.K., So H.H., Moon Y.S., Kim C.H. Proteomic analysis of injured spinal cord tissue proteins using 2-DE and MALDI-TOF MS. Proteomics 2006, 6:2797-2812.
31. Kunz S., Tegeder I., Coste O., Marian C., Pfenninger A., Corvey C., et al. Comparative proteomic analysis of the rat spinal cord in inflammatory and neuropathic pain models. Neurosci Lett 2005, 381:289-293.
32. Yan X., Liu J., Luo Z., Ding Q., Mao X., Yan M., et al. Proteomic profiling of proteins in rat spinal cord induced by contusion injury. Neurochem Int 2010, 56:971-983.
33. Mann M., Ong S.E., Gronborg M., Steen H., Jensen O.N., Pandey A. Analysis of protein phosphorylation using mass spectrometry: deciphering the phosphoproteome. Trends Biotechnol 2002, 20:261-268.
34. Pelech S., Jelinkova L., Susor A., Zhang H., Shi X., Pavlok A., et al. Antibody microarray analyses of signal transduction protein expression and phosphorylation during porcine oocyte maturation. J Proteome Res 2008, 7:2860-2871.
35. Pelech S., Zhang H. Plasticity of the kinomes in monkey and rat tissues. Sci STKE 2002, 2002:pe50.
36. Skalnikova H., Vodicka P., Pelech S., Motlik J., Gadher S.J., Kovarova H. Protein signaling pathways in differentiation of neural stem cells. Proteomics 2008, 8:4547-4559.
37. Thomas P.D., Campbell M.J., Kejariwal A., Mi H., Karlak B., Daverman R., et al. PANTHER: a library of protein families and subfamilies indexed by function. Genome Res 2003, 13:2129-2141.
38. Brown K.R., Jurisica I. Online predicted human interaction database. Bioinformatics 2005, 21:2076-2082.
39. Zhang H., Pelech S. Using protein microarrays to study phosphorylation-mediated signal transduction. Semin Cell Dev Biol 2012, 23:872-882.
40. Nakao-Hayashi J., Ito H., Kanayasu T., Morita I., Murota S. Stimulatory effects of insulin and insulin-like growth factor I on migration and tube formation by vascular endothelial cells. Atherosclerosis 1992, 92:141-149.
41. Wang M.H., Zhou Y.Q., Chen Y.Q. Macrophage-stimulating protein and RON receptor tyrosine kinase: potential regulators of macrophage inflammatory activities. Scand J Immunol 2002, 56:545-553.
42. Lance J.W. The control of muscle tone, reflexes, and movement: Robert Wartenberg Lecture. Neurology 1980, 30:1303-1313.
43. Barolat G., Myklebust J.B., Wenninger W. Effects of spinal cord stimulation on spasticity and spasms secondary to myelopathy. Appl Neurophysiol 1988, 51:29-44.
44. Arroyo R., Vila C., Clissold S. Retrospective observational study of the management of multiple sclerosis patients with resistant spasticity in Spain: the '5E' study. Expert Rev Pharmacoecon Outcomes Res 2011, 11:205-213.
45. Ashworth N.L., Satkunam L.E., Deforge D. Treatment for spasticity in amyotrophic lateral sclerosis/motor neuron disease. Cochrane Database Syst Rev 2006, CD004156.
46. Botte M.J., Nickel V.L., Akeson W.H. Spasticity and contracture. Physiologic aspects of formation. Clin Orthop 1988, 7-18.
47. Dabney K.W., Lipton G.E., Miller F. Cerebral palsy. Curr Opin Pediatr 1997, 9:81-88.
48. Abbott R., Forem S.L., Johann M. Selective posterior rhizotomy for the treatment of spasticity: a review. Childs Nerv Syst 1989, 5:337-346.
49. Barolat G. Surgical management of spasticity and spasms in spinal cord injury: an overview. J Am Paraplegia Soc 1988, 11:9-13.
50. Strack V., Krutzfeldt J., Kellerer M., Ullrich A., Lammers R., Haring H.U. The Protein-tyrosine-phosphatase SHP2 is phosphorylated on serine residues 576 and 591 by protein kinase C isoforms alpha, beta 1, beta 2, and eta. Biochemistry 2002, 41:603-608.
51. Beattie M.S., Bresnahan J.C., Komon J., Tovar C.A., Van Meter M., Anderson D.K., et al. Endogenous repair after spinal cord contusion injuries in the rat. Exp Neurol 1997, 148:453-463.
52. Kawabe J., Koda M., Hashimoto M., Fujiyoshi T., Furuya T., Endo T., et al. Neuroprotective effects of granulocyte colony-stimulating factor and relationship to promotion of angiogenesis after spinal cord injury in rats: laboratory investigation. J Neurosurg Spine 2011, 15:414-421.
53. Esper R.M., Loeb J.A. Neurotrophins induce neuregulin release through protein kinase Cdelta activation. J Biol Chem 2009, 284:26251-26260.
54. Andratsch M., Mair N., Constantin C.E., Scherbakov N., Benetti C., Quarta S., et al. A key role for gp130 expressed on peripheral sensory nerves in pathological pain. J Neurosci 2009, 29:13473-13483.
55. Yang L., Jones N.R., Blumbergs P.C., Van Den Heuvel C., Moore E.J., Manavis J., et al. Severity-dependent expression of pro-inflammatory cytokines in traumatic spinal cord injury in the rat. J Clin Neurosci 2005, 12:276-284.
56. Wen J., Ribeiro R., Zhang Y. Specific PKC isoforms regulate LPS-stimulated iNOS induction in murine microglial cells. J Neuroinflammation 2011, 8:38.
57. Tasci N., Ankarali S., Demir S. Further evidence for enhancing effects of NO on monosynaptic and polysynaptic spinal reflexes in cats. Brain Res 2003, 980:109-116.
58. Sorkin L.S. NMDA evokes an L-NAME sensitive spinal release of glutamate and citrulline. Neuroreport 1993, 4:479-482.
59. Kohno T., Wang H., Amaya F., Brenner G.J., Cheng J.K., Ji R.R., et al. Bradykinin enhances AMPA and NMDA receptor activity in spinal cord dorsal horn neurons by activating multiple kinases to produce pain hypersensitivity. J Neurosci 2008, 28:4533-4540.
60. Zhuang Z.Y., Gerner P., Woolf C.J., Ji R.R. ERK is sequentially activated in neurons, microglia, and astrocytes by spinal nerve ligation and contributes to mechanical allodynia in this neuropathic pain model. Pain 2005, 114:149-159.
61. Crown E.D., Ye Z., Johnson K.M., Xu G.Y., McAdoo D.J., Hulsebosch C.E. Increases in the activated forms of ERK 1/2, p38 MAPK, and CREB are correlated with the expression of at-level mechanical allodynia following spinal cord injury. Exp Neurol 2006, 199:397-407.
62. Obata K., Yamanaka H., Kobayashi K., Dai Y., Mizushima T., Katsura H., et al. Role of mitogen-activated protein kinase activation in injured and intact primary afferent neurons for mechanical and heat hypersensitivity after spinal nerve ligation. J Neurosci 2004, 24:10211-10222.
63. Kobayashi A., Shinoda M., Sessle B.J., Honda K., Imamura Y., Hitomi S., et al. Mechanisms involved in extraterritorial facial pain following cervical spinal nerve injury in rats. Mol Pain 2011, 7:12.
64. Anderson K.A., Noeldner P.K., Reece K., Wadzinski B.E., Means A.R. Regulation and function of the calcium/calmodulin-dependent protein kinase IV/protein serine/threonine phosphatase 2A signaling complex. J Biol Chem 2004, 279:31708-31716.
65. Wayman G.A., Lee Y.S., Tokumitsu H., Silva A.J., Soderling T.R. Calmodulin-kinases: modulators of neuronal development and plasticity. Neuron 2008, 59:914-931.
66. Toyoda H., Zhao M.G., Mercaldo V., Chen T., Descalzi G., Kida S., et al. Calcium/calmodulin-dependent kinase IV contributes to translation-dependent early synaptic potentiation in the anterior cingulate cortex of adult mice. Mol Brain 2010, 3:27.
67. Fang L., Wu J., Lin Q., Willis W.D. Calcium-calmodulin-dependent protein kinase II contributes to spinal cord central sensitization. J Neurosci 2002, 22:4196-4204.
68. Wang Y., Cheng X., Xu J., Liu Z., Wan Y., Ma D. Anti-hyperalgesic effect of CaMKII inhibitor is associated with downregulation of phosphorylated CREB in rat spinal cord. J Anesth 2011, 25:87-92.
69. Wayman G.A., Tokumitsu H., Davare M.A., Soderling T.R. Analysis of CaM-kinase signaling in cells. Cell Calcium 2011, 50:1-8.
70. Xie W.R., Deng H., Li H., Bowen T.L., Strong J.A., Zhang J.M. Robust increase of cutaneous sensitivity, cytokine production and sympathetic sprouting in rats with localized inflammatory irritation of the spinal ganglia. Neuroscience 2006, 142:809-822.
71. Shafit-Zagardo B., Sharma N., Berman J.W., Bornstein M.B., Brosnan C.F. CSF-1 expression is upregulated in astrocyte cultures by IL-1 and TNF and affects microglial proliferation and morphology in organotypic cultures. Int J Dev Neurosci 1993, 11:189-198.
72. Takeuchi A., Miyaishi O., Kiuchi K., Isobe K. Macrophage colony-stimulating factor is expressed in neuron and microglia after focal brain injury. J Neurosci Res 2001, 65:38-44.
73. Franzen R., Bouhy D., Schoenen J. Nervous system injury: focus on the inflammatory cytokine 'granulocyte-macrophage colony stimulating factor'. Neurosci Lett 2004, 361:76-78.