Proteomic and functional annotation analysis of injured peripheral nerves reveals ApoE as a protein upregulated by injury that is modulated by metformin treatment

Molecular Pain

Volumn 9, Issue 1, 2013, Pages

  Melemedjian, Ohannes K ^a   Yassine, Hussein N ^a,c   Shy, Adia ^a   Price, Theodore J ^a,b  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN E; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; METFORMIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CLICK CHEMISTRY; CONTROLLED STUDY; FUNCTIONAL PROTEOMICS; MALE; MOUSE; NONHUMAN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; RAT; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ALGORITHMS; ANIMALS; APOLIPOPROTEINS E; MALE; METFORMIN; MICE; MICE, INBRED ICR; MOLECULAR SEQUENCE ANNOTATION; PROTEOMICS; RATS; RATS, SPRAGUE-DAWLEY; SCIATIC NERVE; UP-REGULATION;

EID: 84875340734     PISSN: None     EISSN: 17448069     Source Type: Journal    
DOI: 10.1186/1744-8069-9-14     Document Type: Article

References (56)

1. Baron R, Binder A, Wasner G. Neuropathic pain: diagnosis, pathophysiological mechanisms, and treatment. Lancet Neurol 2010, 9(8):807-819. 10.1016/S1474-4422(10)70143-5, 20650402.
2. Verma P, Chierzi S, Codd AM, Campbell DS, Meyer RL, Holt CE, Fawcett JW. Axonal protein synthesis and degradation are necessary for efficient growth cone regeneration. J Neurosci 2005, 25(2):331-342. 10.1523/JNEUROSCI.3073-04.2005, 15647476.
3. Willis DE, Twiss JL. The evolving roles of axonally synthesized proteins in regeneration. Curr Opin Neurobiol 2006, 16(1):111-118. 10.1016/j.conb.2006.01.002, 16418002.
4. Zheng JQ, Kelly TK, Chang B, Ryazantsev S, Rajasekaran AK, Martin KC, Twiss JL. A functional role for intra-axonal protein synthesis during axonal regeneration from adult sensory neurons. J Neurosci 2001, 21(23):9291-9303.
5. Geranton SM, Jimenez-Diaz L, Torsney C, Tochiki KK, Stuart SA, Leith JL, Lumb BM, Hunt SP. A rapamycin-sensitive signaling pathway is essential for the full expression of persistent pain states. J Neurosci 2009, 29(47):15017-15027. 10.1523/JNEUROSCI.3451-09.2009, 2830115, 19940197.
6. Jimenez-Diaz L, Geranton SM, Passmore GM, Leith JL, Fisher AS, Berliocchi L, Sivasubramaniam AK, Sheasby A, Lumb BM, Hunt SP. Local translation in primary afferent fibers regulates nociception. PLoS One 2008, 3(4):e1961. 10.1371/journal.pone.0001961, 2276314, 18398477.
7. Melemedjian OK, Asiedu MN, Tillu DV, Sanoja R, Yan J, Lark A, Khoutorsky A, Johnson J, Peebles KA, Lepow T. Targeting adenosine monophosphate-activated protein kinase (AMPK) in preclinical models reveals a potential mechanism for the treatment of neuropathic pain. Mol Pain 2011, 7:70. 10.1186/1744-8069-7-70, 3186752, 21936900.
8. Price TJ, Rashid MH, Millecamps M, Sanoja R, Entrena JM, Cervero F. Decreased nociceptive sensitization in mice lacking the fragile X mental retardation protein: role of mGluR1/5 and mTOR. J Neurosci 2007, 27(51):13958-13967. 10.1523/JNEUROSCI.4383-07.2007, 2206543, 18094233.
9. Zoncu R, Efeyan A, Sabatini DM. MTOR: from growth signal integration to cancer, diabetes and ageing. Nat Rev Mol Cell Biol 2011, 12(1):21-35. 10.1038/nrm3025, 3390257, 21157483.
10. Huang HL, Cendan CM, Roza C, Okuse K, Cramer R, Timms JF, Wood JN. Proteomic profiling of neuromas reveals alterations in protein composition and local protein synthesis in hyper-excitable nerves. Mol Pain 2008, 4:33. 10.1186/1744-8069-4-33, 2525634, 18700027.
11. Lai J, Gold MS, Kim CS, Bian D, Ossipov MH, Hunter JC, Porreca F. Inhibition of neuropathic pain by decreased expression of the tetrodotoxin-resistant sodium channel, NaV1.8. Pain 2002, 95(1-2):143-152.
12. Joshi SK, Mikusa JP, Hernandez G, Baker S, Shieh CC, Neelands T, Zhang XF, Niforatos W, Kage K, Han P. Involvement of the TTX-resistant sodium channel Nav 1.8 In inflammatory and neuropathic, but not post-operative, pain states. Pain 2006, 123(1-2):75-82.
13. Dong XW, Goregoaker S, Engler H, Zhou X, Mark L, Crona J, Terry R, Hunter J, Priestley T. Small interfering RNA-mediated selective knockdown of Na(V)1.8 Tetrodotoxin-resistant sodium channel reverses mechanical allodynia in neuropathic rats. Neuroscience 2007, 146(2):812-821. 10.1016/j.neuroscience.2007.01.054, 17367951.
14. McGaraughty S, Chu KL, Scanio MJ, Kort ME, Faltynek CR, Jarvis MF. A selective Nav1.8 Sodium channel blocker, a-803467 [5-(4-chlorophenyl-N-(3,5-dimethoxyphenyl)furan-2-carboxamide], attenuates spinal neuronal activity in neuropathic rats. J Pharmacol Exp Ther 2008, 324(3):1204-1211.
15. Akopian AN, Sivilotti L, Wood JN. A tetrodotoxin-resistant voltage-gated sodium channel expressed by sensory neurons. Nature 1996, 379(6562):257-262. 10.1038/379257a0, 8538791.
16. Okuse K, Chaplan SR, McMahon SB, Luo ZD, Calcutt NA, Scott BP, Akopian AN, Wood JN. Regulation of expression of the sensory neuron-specific sodium channel SNS in inflammatory and neuropathic pain. Mol Cell Neurosci 1997, 10(3-4):196-207.
17. Akopian AN, Souslova V, England S, Okuse K, Ogata N, Ure J, Smith A, Kerr BJ, McMahon SB, Boyce S. The tetrodotoxin-resistant sodium channel SNS has a specialized function in pain pathways. Nat Neurosci 1999, 2(6):541-548. 10.1038/9195, 10448219.
18. Thakor DK, Lin A, Matsuka Y, Meyer EM, Ruangsri S, Nishimura I, Spigelman I. Increased peripheral nerve excitability and local NaV1.8 MRNA up-regulation in painful neuropathy. Mol Pain 2009, 5:14. 10.1186/1744-8069-5-14, 2667430, 19320998.
19. Schicho R, Florian W, Liebmann I, Holzer P, Lippe IT. Increased expression of TRPV1 receptor in dorsal root ganglia by acid insult of the rat gastric mucosa. Eur J Neurosci 2004, 19(7):1811-1818. 10.1111/j.1460-9568.2004.03290.x, 15078554.
20. Chen Y, Geis C, Sommer C. Activation of TRPV1 contributes to morphine tolerance: involvement of the mitogen-activated protein kinase signaling pathway. J Neurosci 2008, 28(22):5836-5845. 10.1523/JNEUROSCI.4170-07.2008, 18509045.
21. Nadeau S, Filali M, Zhang J, Kerr BJ, Rivest S, Soulet D, Iwakura Y, de Rivero Vaccari JP, Keane RW, Lacroix S. Functional recovery after peripheral nerve injury is dependent on the pro-inflammatory cytokines IL-1beta and TNF: implications for neuropathic pain. J Neurosci 2011, 31(35):12533-12542. 10.1523/JNEUROSCI.2840-11.2011, 21880915.
22. Morin N, Owolabi SA, Harty MW, Papa EF, Tracy TF, Shaw SK, Kim M, Saab CY. Neutrophils invade lumbar dorsal root ganglia after chronic constriction injury of the sciatic nerve. J Neuroimmunol 2007, 184(1-2):164-171.
23. Abbadie C, Lindia JA, Cumiskey AM, Peterson LB, Mudgett JS, Bayne EK, DeMartino JA, MacIntyre DE, Forrest MJ. Impaired neuropathic pain responses in mice lacking the chemokine receptor CCR2. Proc Natl Acad Sci U S A 2003, 100(13):7947-7952. 10.1073/pnas.1331358100, 164693, 12808141.
24. Ignatius MJ, Gebicke-Harter PJ, Skene JH, Schilling JW, Weisgraber KH, Mahley RW, Shooter EM. Expression of apolipoprotein E during nerve degeneration and regeneration. Proc Natl Acad Sci U S A 1986, 83(4):1125-1129. 10.1073/pnas.83.4.1125, 323024, 2419900.
25. Schirmer EC, Yates JR, Gerace L. MudPIT: a powerful proteomics tool for discovery. Discovery Med 2003, 3(18):38-39.
26. Skene JH, Shooter EM. Denervated sheath cells secrete a new protein after nerve injury. Proc Natl Acad Sci U S A 1983, 80(13):4169-4173. 10.1073/pnas.80.13.4169, 394222, 6575401.
27. Mahley RW. Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Science 1988, 240(4852):622-630. 10.1126/science.3283935, 3283935.
28. Handelmann GE, Boyles JK, Weisgraber KH, Mahley RW, Pitas RE. Effects of apolipoprotein E, beta-very low density lipoproteins, and cholesterol on the extension of neurites by rabbit dorsal root ganglion neurons in vitro. J Lipid Res 1992, 33(11):1677-1688.
29. Li FQ, Fowler KA, Neil JE, Colton CA, Vitek MP. An apolipoprotein E-mimetic stimulates axonal regeneration and remyelination after peripheral nerve injury. J Pharmacol Exp Ther 2010, 334(1):106-115. 10.1124/jpet.110.167882, 2912037, 20406857.
30. Kim J, Basak JM, Holtzman DM. The role of apolipoprotein E in Alzheimer's disease. Neuron 2009, 63(3):287-303. 10.1016/j.neuron.2009.06.026, 3044446, 19679070.
31. Teter B, Xu PT, Gilbert JR, Roses AD, Galasko D, Cole GM. Human apolipoprotein E isoform-specific differences in neuronal sprouting in organotypic hippocampal culture. J Neurochem 1999, 73(6):2613-2616.
32. Genis L, Chen Y, Shohami E, Michaelson DM. Tau hyperphosphorylation in apolipoprotein E-deficient and control mice after closed head injury. J Neurosci Res 2000, 60(4):559-564. 10.1002/(SICI)1097-4547(20000515)60:4<559::AID-JNR15>3.0.CO;2-K, 10797559.
33. Pola R, Gaetani E, Flex A, Aprahamian T, Proia AS, Bosch-Marce M, Smith RC, Pola P. Peripheral nerve ischemia: apolipoprotein E deficiency results in impaired functional recovery and reduction of associated intraneural angiogenic response. Exp Neurol 2003, 184(1):264-273. 10.1016/S0014-4886(03)00260-7, 14637097.
34. Osada N, Kosuge Y, Kihara T, Ishige K, Ito Y. Apolipoprotein E-deficient mice are more vulnerable to ER stress after transient forebrain ischemia. Neurochem Int 2009, 54(7):403-409. 10.1016/j.neuint.2009.01.010, 19428781.
35. Aono M, Bennett ER, Kim KS, Lynch JR, Myers J, Pearlstein RD, Warner DS, Laskowitz DT. Protective effect of apolipoprotein E-mimetic peptides on N-methyl-D-aspartate excitotoxicity in primary rat neuronal-glial cell cultures. Neuroscience 2003, 116(2):437-445. 10.1016/S0306-4522(02)00709-1, 12559098.
36. McAdoo JD, Warner DS, Goldberg RN, Vitek MP, Pearlstein R, Laskowitz DT. Intrathecal administration of a novel apoE-derived therapeutic peptide improves outcome following perinatal hypoxic-ischemic injury. Neurosci Lett 2005, 381(3):305-308. 10.1016/j.neulet.2005.02.036, 15896489.
37. Laskowitz DT, McKenna SE, Song P, Wang H, Durham L, Yeung N, Christensen D, Vitek MP. COG1410, A novel apolipoprotein E-based peptide, improves functional recovery in a murine model of traumatic brain injury. J Neurotrauma 2007, 24(7):1093-1107. 10.1089/neu.2006.0192, 17610350.
38. Hoane MR, Kaufman N, Vitek MP, McKenna SE. COG1410 Improves cognitive performance and reduces cortical neuronal loss in the traumatically injured brain. J Neurotrauma 2009, 26(1):121-129. 10.1089/neu.2008.0565, 2749004,2749004, 19119914.
39. Tukhovskaya EA, Yukin AY, Khokhlova ON, Murashev AN, Vitek MP. COG1410, A novel apolipoprotein-E mimetic, improves functional and morphological recovery in a rat model of focal brain ischemia. J Neurosci Res 2009, 87(3):677-682. 10.1002/jnr.21874, 2752425, 18803296.
40. Kaufman NA, Beare JE, Tan AA, Vitek MP, McKenna SE, Hoane MR. COG1410, An apolipoprotein E-based peptide, improves cognitive performance and reduces cortical loss following moderate fluid percussion injury in the rat. Behav Brain Res 2010, 214(2):395-401. 10.1016/j.bbr.2010.06.017, 2936242, 20600347.
41. Ali K, Middleton M, Pure E, Rader DJ. Apolipoprotein E suppresses the type I inflammatory response in vivo. Circ Res 2005, 97(9):922-927. 10.1161/01.RES.0000187467.67684.43, 16179587.
42. Kato N, Nemoto K, Arino H, Fujikawa K. Treatment of the chronic inflammation in peripheral target tissue improves the crushed nerve recovery in the rat: histopathological assessment of the nerve recovery. J Neurol Sci 2002, 202(1-2):69-74.
43. Thacker MA, Clark AK, Marchand F, McMahon SB. Pathophysiology of peripheral neuropathic pain: immune cells and molecules. Anesth Analg 2007, 105(3):838-847. 10.1213/01.ane.0000275190.42912.37, 17717248.
44. Price TJ, Geranton SM. Translating nociceptor sensitivity: the role of axonal protein synthesis in nociceptor physiology. Eur J Neurosci 2009, 29(12):2253-2263. 10.1111/j.1460-9568.2009.06786.x, 2914561, 19490023.
45. Abe N, Borson SH, Gambello MJ, Wang F, Cavalli V. Mammalian target of rapamycin (mTOR) activation increases axonal growth capacity of injured peripheral nerves. J Biol Chem 2010, 285(36):28034-28043. 10.1074/jbc.M110.125336, 2934668, 20615870.
46. Larsson O, Morita M, Topisirovic I, Alain T, Blouin MJ, Pollak M, Sonenberg N. Distinct perturbation of the translatome by the antidiabetic drug metformin. Proc Natl Acad Sci U S A 2012, 109(23):8977-8982. 10.1073/pnas.1201689109, 3384216, 22611195.
47. Tillu DV, Melemedjian OK, Asiedu MN, Qu N, De Felice M, Dussor G, Price TJ. Resveratrol engages AMPK to attenuate ERK and mTOR signaling in sensory neurons and inhibits incision-induced acute and chronic pain. Mol Pain 2012, 8(1):5. 10.1186/1744-8069-8-5, 3284441, 22269797.
48. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 1994, 53(1):55-63. 10.1016/0165-0270(94)90144-9, 7990513.
49. Kim SH, Chung JM. An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 1992, 50(3):355-363. 10.1016/0304-3959(92)90041-9, 1333581.
50. Bourquin AF, Suveges M, Pertin M, Gilliard N, Sardy S, Davison AC, Spahn DR, Decosterd I. Assessment and analysis of mechanical allodynia-like behavior induced by spared nerve injury (SNI) in the mouse. Pain 2006, 122(1-2):14 e11-14.
51. Combs TP, Wagner JA, Berger J, Doebber T, Wang WJ, Zhang BB, Tanen M, Berg AH, O'Rahilly S, Savage DB. Induction of adipocyte complement-related protein of 30 kilodaltons by PPARgamma agonists: a potential mechanism of insulin sensitization. Endocrinology 2002, 143(3):998-1007. 10.1210/en.143.3.998, 11861525.
52. Andon NL, Hollingworth S, Koller A, Greenland AJ, Yates JR, Haynes PA. Proteomic characterization of wheat amyloplasts using identification of proteins by tandem mass spectrometry. Proteomics 2002, 2(9):1156-1168. 10.1002/1615-9861(200209)2:9<1156::AID-PROT1156>3.0.CO;2-4, 12362334.
53. Hunter TC, Andon NL, Koller A, Yates JR, Haynes PA. The functional proteomics toolbox: methods and applications. J Chromatogr B, Anal Technol Biomed Life Sci 2002, 782(1-2):165-181.
54. Wolters DA, Washburn MP, Yates JR. An automated multidimensional protein identification technology for shotgun proteomics. Anal Chem 2001, 73(23):5683-5690. 10.1021/ac010617e, 11774908.
55. da Huang W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4(1):44-57.
56. da Huang W, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 2009, 37(1):1-13. 10.1093/nar/gkn923, 2615629, 19033363.