Early systemic granulocyte-colony stimulating factor treatment attenuates neuropathic pain after peripheral nerve injury

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Chao, Po Kuan ^a   Lu, Kwok Tung ^a   Lee, Yun Lin ^b   Chen, Jin Chung ^c   Wang, Hung Li ^c   Yang, Yi Ling ^d   Cheng, Mei Yun ^b   Liao, Ming Feng ^b   Ro, Long Sun ^b  

^a NATIONAL TAIWAN NORMAL UNIVERSITY   (Taiwan)

^b CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

^c CHANG GUNG UNIVERSITY   (Taiwan)

^d NATIONAL CHIAYI UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

17 METHYLNALOXONE; FIGRASTIM; INTERLEUKIN 6; MESSENGER RNA; OPIATE; OPIATE RECEPTOR; RECOMBINANT GRANULOCYTE COLONY STIMULATING FACTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ALLODYNIA; ANALGESIC ACTIVITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HYPERALGESIA; MALE; MICROGLIA; NEUROPATHIC PAIN; NONHUMAN; PERIPHERAL NERVE INJURY; POLYMORPHONUCLEAR CELL; RAT; SINGLE DRUG DOSE; SPINAL CORD DORSAL HORN; SPINAL GANGLION; UPREGULATION;

ANIMALS; GANGLIA, SPINAL; GRANULOCYTE COLONY-STIMULATING FACTOR; HYPERALGESIA; INTERLEUKIN-6; MALE; NEURALGIA; PAIN MEASUREMENT; PAIN THRESHOLD; PERIPHERAL NERVE INJURIES; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84865291091     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0043680     Document Type: Article

References (55)

1. Marchand F, Perretti M, McMahon SB, (2005) Role of the immune system in chronic pain. Nat Rev Neurosci 6: 521-532.
2. Fecho K, Manning EL, Maixner W, Schmitt CP, (2007) Effects of carrageenan and morphine on acute inflammation and pain in Lewis and Fischer rats. Brain Behav Immun 21: 68-78.
3. Finley MJ, Happel CM, Kaminsky DE, Rogers TJ, (2008) Opioid and nociceptin receptors regulate cytokine and cytokine receptor expression. Cell Immunol 252: 146-154.
4. Berrios I, Castro C, Kuffler DP, (2008) Morphine: axon regeneration, neuroprotection, neurotoxicity, tolerance, and neuropathic pain. P R Health Sci J 27: 119-128.
5. Ugolini G, Marinelli S, Covaceuszach S, Cattaneo A, Pavone F, (2007) The function neutralizing anti-TrkA antibody MNAC13 reduces inflammatory and neuropathic pain. Proc Natl Acad Sci U S A 104: 2985-2990.
6. Stein C, Schafer M, Machelska H, (2003) Attacking pain at its source: new perspectives on opioids. Nat Med 9: 1003-1008.
7. Busch-Dienstfertig M, Stein C, (2010) Opioid receptors and opioid peptide-producing leukocytes in inflammatory pain-basic and therapeutic aspects. Brain Behav Immun 24: 683-694.
8. Binder W, Mousa SA, Sitte N, Kaiser M, Stein C, et al. (2004) Sympathetic activation triggers endogenous opioid release and analgesia within peripheral inflamed tissue. Eur J Neurosci 20: 92-100.
9. Labuz D, Schmidt Y, Schreiter A, Rittner HL, Mousa SA, et al. (2009) Immune cell-derived opioids protect against neuropathic pain in mice. J Clin Invest 119: 278-286.
10. Stein C, Hassan AH, Przewlocki R, Gramsch C, Peter K, et al. (1990) Opioids from immunocytes interact with receptors on sensory nerves to inhibit nociception in inflammation. Proc Natl Acad Sci U S A 87: 5935-5939.
11. Cabot PJ, Carter L, Schafer M, Stein C, (2001) Methionine-enkephalin-and Dynorphin A-release from immune cells and control of inflammatory pain. Pain 93: 207-212.
12. Brack A, Rittner HL, Machelska H, Leder K, Mousa SA, et al. (2004) Control of inflammatory pain by chemokine-mediated recruitment of opioid-containing polymorphonuclear cells. Pain 112: 229-238.
13. Mousa SA, Shakibaei M, Sitte N, Schafer M, Stein C, (2004) Subcellular pathways of beta-endorphin synthesis, processing, and release from immunocytes in inflammatory pain. Endocrinology 145: 1331-1341.
14. Rittner HL, Brack A, Stein C, (2008) The other side of the medal: how chemokines promote analgesia. Neurosci Lett 437: 203-208.
15. Labuz D, Schreiter A, Schmidt Y, Brack A, Machelska H, (2010) T lymphocytes containing beta-endorphin ameliorate mechanical hypersensitivity following nerve injury. Brain Behav Immun 24: 1045-1053.
16. Rittner HL, Mousa SA, Labuz D, Beschmann K, Schafer M, et al. (2006) Selective local PMN recruitment by CXCL1 or CXCL2/3 injection does not cause inflammatory pain. J Leukoc Biol 79: 1022-1032.
17. Hoggatt J, Pelus LM, (2011) Many mechanisms mediating mobilization: an alliterative review. Curr Opin Hematol 18: 231-238.
18. Roberts AW, (2005) G-CSF: a key regulator of neutrophil production, but that's not all! Growth Factors. 23: 33-41.
19. Touw IP, van de Geijn GJ, (2007) Granulocyte colony-stimulating factor and its receptor in normal myeloid cell development, leukemia and related blood cell disorders. Front Biosci 12: 800-815.
20. Cabot PJ, Carter L, Gaiddon C, Zhang Q, Schafer M, et al. (1997) Immune cell-derived beta-endorphin. Production, release, and control of inflammatory pain in rats. J Clin Invest 100: 142-148.
21. Cabot PJ, (2001) Immune-derived opioids and peripheral antinociception. Clin Exp Pharmacol Physiol 28: 230-232.
22. Rittner HL, Labuz D, Schaefer M, Mousa SA, Schulz S, et al. (2006) Pain control by CXCR2 ligands through Ca2+-regulated release of opioid peptides from polymorphonuclear cells. FASEB J 20: 2627-2629.
23. Bennett GJ, Xie YK, (1988) A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33: 87-107.
24. Wang F, Shen X, Guo X, Peng Y, Liu Y, et al. (2010) Spinal macrophage migration inhibitory factor contributes to the pathogenesis of inflammatory hyperalgesia in rats. Pain 148: 275-283.
25. Zhang YQ, Guo N, Peng G, Wang X, Han M, et al. (2009) Role of SIP30 in the development and maintenance of peripheral nerve injury-induced neuropathic pain. Pain 146: 130-140.
26. Nguyen HX, Galvan MD, Anderson AJ, (2008) Characterization of early and terminal complement proteins associated with polymorphonuclear leukocytes in vitro and in vivo after spinal cord injury. J Neuroinflammation 5: 26.
27. Lloyd CM, Phillips AR, Cooper GJ, Dunbar PR, (2008) Three-colour fluorescence immunohistochemistry reveals the diversity of cells staining for macrophage markers in murine spleen and liver. J Immunol Methods 334: 70-81.
28. Rittner HL, Brack A, Machelska H, Mousa SA, Bauer M, et al. (2001) Opioid peptide-expressing leukocytes: identification, recruitment, and simultaneously increasing inhibition of inflammatory pain. Anesthesiology 95: 500-508.
29. Mousa SA, Machelska H, Schafer M, Stein C, (2002) Immunohistochemical localization of endomorphin-1 and endomorphin-2 in immune cells and spinal cord in a model of inflammatory pain. J Neuroimmunol 126: 5-15.
30. Machelska H, Heppenstall PA, Stein C, (2003) Breaking the pain barrier. Nat Med 9: 1353-1354.
31. Hagiwara S, Iwasaka H, Hasegawa A, Noguchi T, (2008) Pre-Irradiation of blood by gallium aluminum arsenide (830 nm) low-level laser enhances peripheral endogenous opioid analgesia in rats. Anesth Analg 107: 1058-1063.
32. Leanez S, Hervera A, Pol O, (2009) Peripheral antinociceptive effects of micro- and delta-opioid receptor agonists in NOS2 and NOS1 knockout mice during chronic inflammatory pain. Eur J Pharmacol 602: 41-49.
33. Becker PS, Wagle M, Matous S, Swanson RS, Pihan G, et al. (1997) Spontaneous splenic rupture following administration of granulocyte colony-stimulating factor (G-CSF): occurrence in an allogeneic donor of peripheral blood stem cells. Biol Blood Marrow Transplant 3: 45-49.
34. Semerad CL, Poursine-Laurent J, Liu F, Link DC, (1999) A role for G-CSF receptor signaling in the regulation of hematopoietic cell function but not lineage commitment or differentiation. Immunity 11: 153-161.
35. Takemoto Y, Wada H, Takatsuka H, Okamoto T, Kakishita E, (2000) Mobilization of peripheral blood stem cells by granulocyte-colony stimulating factors: comparison of a standard dose of glycosylated and mutated granulocyte-colony stimulating factor in non-Hodgkin's lymphoma patients following CHOP therapy. Drugs Exp Clin Res 26: 1-5.
36. Eyles JL, Hickey MJ, Norman MU, Croker BA, Roberts AW, et al. (2008) A key role for G-CSF-induced neutrophil production and trafficking during inflammatory arthritis. Blood 112: 5193-5201.
37. Brack A, Rittner HL, Machelska H, Beschmann K, Sitte N, et al. (2004) Mobilization of opioid-containing polymorphonuclear cells by hematopoietic growth factors and influence on inflammatory pain. Anesthesiology 100: 149-157.
38. Brack A, Rittner HL, Machelska H, Shaqura M, Mousa SA, et al. (2004) Endogenous peripheral antinociception in early inflammation is not limited by the number of opioid-containing leukocytes but by opioid receptor expression. Pain 108: 67-75.
39. Kapitzke D, Vetter I, Cabot PJ, (2005) Endogenous opioid analgesia in peripheral tissues and the clinical implications for pain control. Ther Clin Risk Manag 1: 279-297.
40. Nilsson A, Moller K, Dahlin L, Lundborg G, Kanje M, (2005) Early changes in gene expression in the dorsal root ganglia after transection of the sciatic nerve; effects of amphiregulin and PAI-1 on regeneration. Brain Res Mol Brain Res 136: 65-74.
41. White FA, Jung H, Miller RJ, (2007) Chemokines and the pathophysiology of neuropathic pain. Proc Natl Acad Sci U S A 104: 20151-20158.
42. Zhang RX, Liu B, Wang L, Ren K, Qiao JT, et al. (2005) Spinal glial activation in a new rat model of bone cancer pain produced by prostate cancer cell inoculation of the tibia. Pain 118: 125-136.
43. Lazarini F, Tham TN, Casanova P, Arenzana-Seisdedos F, Dubois-Dalcq M, (2003) Role of the alpha-chemokine stromal cell-derived factor (SDF-1) in the developing and mature central nervous system. Glia 42: 139-148.
44. Hathway GJ, Vega-Avelaira D, Moss A, Ingram R, Fitzgerald M, (2009) Brief, low frequency stimulation of rat peripheral C-fibres evokes prolonged microglial-induced central sensitization in adults but not in neonates. Pain 144: 110-118.
45. Schweizerhof M, Stosser S, Kurejova M, Njoo C, Gangadharan V, et al. (2009) Hematopoietic colony-stimulating factors mediate tumor-nerve interactions and bone cancer pain. Nat Med 15: 802-807.
46. Liou JT, Lui PW, Liu FC, Lai YS, Day YJ, (2011) Exogenous granulocyte colony-stimulating factor exacerbate pain-related behaviors after peripheral nerve injury. J Neuroimmunol 232: 83-93.
47. Mousa SA, Bopaiah CP, Richter JF, Yamdeu RS, Schafer M, (2007) Inhibition of inflammatory pain by CRF at peripheral, spinal and supraspinal sites: involvement of areas coexpressing CRF receptors and opioid peptides. Neuropsychopharmacology 32: 2530-2542.
48. Dale CS, Pagano Rde L, Rioli V, (2005) Hemopressin: a novel bioactive peptide derived from the alpha1-chain of hemoglobin. Mem Inst Oswaldo Cruz 100 (Suppl 1):: 105-106.
49. Poisbeau P, Patte-Mensah C, Keller AF, Barrot M, Breton JD, et al. (2005) Inflammatory pain upregulates spinal inhibition via endogenous neurosteroid production. J Neurosci 25: 11768-11776.
50. Iwasaka H, Kitano T, Miyakawa H, Unoshima M, Shinguu C, et al. (2001) Neutrophilia and granulocyte colony-stimulating factor levels after cardiopulmonary bypass. Can J Anaesth 48: 81-84.
51. Brack A, Rittner HL, Stein C, (2004) Neurogenic painful inflammation. Curr Opin Anaesthesiol 17: 461-464.
52. Rutella S, (2007) Granulocyte colony-stimulating factor for the induction of T-cell tolerance. Transplantation 84: S26-30.
53. Solaroglu I, Jadhav V, Zhang JH, (2007) Neuroprotective effect of granulocyte-colony stimulating factor. Front Biosci 12: 712-724.
54. Tsai RK, Chang CH, Wang HZ, (2008) Neuroprotective effects of recombinant human granulocyte colony-stimulating factor (G-CSF) in neurodegeneration after optic nerve crush in rats. Exp Eye Res 87: 242-250.
55. Pollari E, Savchenko E, Jaronen M, Kanninen K, Malm T, et al. (2011) Granulocyte colony stimulating factor attenuates inflammation in a mouse model of amyotrophic lateral sclerosis. J Neuroinflammation 8: 74.