Activation profile of dorsal root ganglia Iba-1 (+) macrophages varies with the type of lesion in rats

Acta Histochemica

Volumn 115, Issue 8, 2013, Pages 840-850

  Ton, Bich Hoai Thi ^a,b   Chen, Qingmin ^c   Gaina, Gisela ^a   Tucureanu, Catalin ^d   Georgescu, Adriana ^e   Strungaru, Carmen ^a   Flonta, Maria Luiza ^a   Sah, Dinah ^c   Ristoiu, Violeta ^a  

^a UNIVERSITY OF BUCHAREST   (Romania)

^b VINH UNIVERSITY   (Viet Nam)

^c ALNYLAM PHARMACEUTICALS   (United States)

^d CANTACUZINO INSTITUTE   (Romania)

^e INSTITUTE OF CELLULAR BIOLOGY AND PATHOLOGY NICOLAE SIMIONESCU   (Romania)

Author keywords

Diabetic neuropathy; Dorsal root ganglia; Iba 1; Macrophages; Neuropathic pain; Rat; Spinal nerve ligation

Indexed keywords

GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; IONIZED CALCIUM BINDING ADAPTOR MOLECULE 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MELANOMA GROWTH STIMULATORY ACTIVITY FACTOR; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; ACTIN BINDING PROTEIN; AIF1 PROTEIN, RAT; CALCIUM BINDING PROTEIN;

ADULT ANIMAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ACTIVATION; CELL POPULATION; CELL STRUCTURE; CONTROLLED STUDY; DIABETIC NEUROPATHY; ENZYME ACTIVATION; ENZYME RELEASE; IMMUNOHISTOCHEMISTRY; MACROPHAGE; MALE; MICROGLIA; NERVE LIGATION; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SATELLITE CELL; SPINAL CORD; SPINAL GANGLION; SPINAL NERVE; STREPTOZOCIN DIABETES; UPREGULATION; ANIMAL; METABOLISM; PATHOLOGY; SPRAGUE DAWLEY RAT;

RATTUS;

ANIMALS; CALCIUM-BINDING PROTEINS; GANGLIA, SPINAL; MACROPHAGES; MALE; MICROFILAMENT PROTEINS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84887210041     PISSN: 00651281     EISSN: 16180372     Source Type: Journal    
DOI: 10.1016/j.acthis.2013.04.007     Document Type: Article

References (62)

1. Beggs S., Salter M.W. Stereological and somatotopic analysis of the spinal microglial response to peripheral nerve injury. Brain Behav Immun 2007, 21:624-633.
2. Bich-Hoai T.T., Marin A., Dinu C., Banciu D., Maria-Luiza F., Ristoiu V. Hypoxia and high glucose activate tetrodotoxin-resistant Na(+) currents through PKA and PKC. Acta Neurobiol Exp (Wars) 2010, 70:351-361.
3. Bishnoi M., Bosgraaf C.A., Abooj M., Zhong L., Premkumar L.S. Streptozotocin-induced early thermal hyperalgesia is independent of glycemic state of rats: role of transient receptor potential vanilloid 1(TRPV1) and inflammatory mediators. Mol Pain 2011, 7:52.
4. Chatzigeorgiou A., Harokopos V., Mylona-Karagianni C., Tsouvalas E., Aidinis V., Kamper E.F. The pattern of inflammatory/anti-inflammatory cytokines and chemokines in type 1 diabetic patients over time. Ann Med 2010, 42:426-438.
5. Cheng X.P., Wang B.R., Liu H.L., You S.W., Huang W.J., Jiao X.Y., et al. Phosphorylation of extracellular signal-regulated kinases 1/2 is predominantly enhanced in the microglia of the rat spinal cord following dorsal root transection. Neuroscience 2003, 119:701-712.
6. Clark A.K., Yip P.K., Grist J., Gentry C., Staniland A.A., Marchand F., et al. Inhibition of spinal microglial cathepsin S for the reversal of neuropathic pain. Proc Natl Acad Sci USA 2007, 104:10655-10660.
7. Conti G., Scarpini E., Baron P., Livraghi S., Tiriticco M., Bianchi R., et al. Macrophage infiltration and death in the nerve during the early phases of experimental diabetic neuropathy: a process concomitant with endoneurial induction of IL-1beta and p75NTR. J Neurol Sci 2002, 195:35-40.
8. Daulhac L., Mallet C., Courteix C., Etienne M., Duroux E., Privat A.M., et al. Diabetes-induced mechanical hyperalgesia involves spinal mitogen-activated protein kinase activation in neurons and microglia via N-methyl-d-aspartate-dependent mechanisms. Mol Pharmacol 2006, 70:1246-1254.
9. Drozina G., Kohoutek J., Nishiya T., Peterlin B.M. Sequential modifications in class II transactivator isoform 1 induced by lipopolysaccharide stimulate major histocompatibility complex class II transcription in macrophages. J Biol Chem 2006, 281:39963-39970.
10. Dubovy P., Jancalek R., Klusakova I., Svizenska I., Pejchalova K. Intra- and extraneuronal changes of immunofluorescence staining for TNF-alpha and TNFR1 in the dorsal root ganglia of rat peripheral neuropathic pain models. Cell Mol Neurobiol 2006, 26:1205-1217.
11. Feng G.J., Goodridge H.S., Harnett M.M., Wei X.Q., Nikolaev A.V., Higson A.P., et al. Extracellular signal-related kinase (ERK) and p38 mitogen-activated protein (MAP) kinases differentially regulate the lipopolysaccharide-mediated induction of inducible nitric oxide synthase and IL-12 in macrophages: Leishmania phosphoglycans subvert macrophage IL-12 production by targeting ERK MAP kinase. J Immunol 1999, 163:6403-6412.
12. Gosselin R.D., Suter M.R., Ji R.R., Decosterd I. Glial cells and chronic pain. Neuroscientist 2010, 16:519-531.
13. Hanani M. Satellite glial cells in sensory ganglia: from form to function. Brain Res Brain Res Rev 2005, 48:457-476.
14. Hatashita S., Sekiguchi M., Kobayashi H., Konno S., Kikuchi S. Contralateral neuropathic pain and neuropathology in dorsal root ganglion and spinal cord following hemilateral nerve injury in rats. Spine (Phila Pa 1976) 2008, 33:1344-1351.
15. Hu P., McLachlan E.M. Macrophage and lymphocyte invasion of dorsal root ganglia after peripheral nerve lesions in the rat. Neuroscience 2002, 112:23-38.
16. Hu P., McLachlan E.M. Distinct functional types of macrophage in dorsal root ganglia and spinal nerves proximal to sciatic and spinal nerve transections in the rat. Exp Neurol 2003, 184:590-605.
17. Hu P., Bembrick A.L., Keay K.A., McLachlan E.M. Immune cell involvement in dorsal root ganglia and spinal cord after chronic constriction or transection of the rat sciatic nerve. Brain Behav Immun 2007, 21:599-616.
18. Hunt J.L., Winkelstein B.A., Rutkowski M.D., Weinstein J.N., DeLeo J.A. Repeated injury to the lumbar nerve roots produces enhanced mechanical allodynia and persistent spinal neuroinflammation. Spine (Phila Pa 1976) 2001, 26:2073-2079.
19. Ji R.R., Kawasaki Y., Zhuang Z.Y., Wen Y.R., Zhang Y.Q. Protein kinases as potential targets for the treatment of pathological pain. Handb Exp Pharmacol 2007, 177:359-389.
20. Jin S.X., Zhuang Z.Y., Woolf C.J., Ji R.R. p38 mitogen-activated protein kinase is activated after a spinal nerve ligation in spinal cord microglia and dorsal root ganglion neurons and contributes to the generation of neuropathic pain. J Neurosci 2003, 23:4017-4022.
21. Kawamura N., Dyck P.J., Schmeichel A.M., Engelstad J.K., Low P.A. Inflammatory mediators in diabetic and non-diabetic lumbosacral radiculoplexus neuropathy. Acta Neuropathol (Berl) 2008, 115:231-239.
22. Kim S.H., Chung J.M. An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 1992, 50:355-363.
23. Kim C.F., Moalem-Taylor G. Detailed characterization of neuro-immune responses following neuropathic injury in mice. Brain Res 2011, 1405:95-108.
24. Li H., Xie W., Strong J.A., Zhang J.M. Systemic antiinflammatory corticosteroid reduces mechanical pain behavior, sympathetic sprouting, and elevation of proinflammatory cytokines in a rat model of neuropathic pain. Anesthesiology 2007, 107:469-477.
25. Liu T., van Rooijen N., Tracey D.J. Depletion of macrophages reduces axonal degeneration and hyperalgesia following nerve injury. Pain 2000, 86:25-32.
26. Luo M.C., Chen Q., Ossipov M.H., Rankin D.R., Porreca F., Lai J. Spinal dynorphin and bradykinin receptors maintain inflammatory hyperalgesia. J Pain 2008, 9:1096-1105.
27. Ma W., Quirion R. Increased calcitonin gene-related peptide in neuroma and invading macrophages is involved in the up-regulation of interleukin-6 and thermal hyperalgesia in a rat model of mononeuropathy. J Neurochem 2006, 98:180-192.
28. Machelska H. Dual peripheral actions of immune cells in neuropathic pain. Arch Immunol Ther Exp (Warsz) 2011, 59:11-24.
29. Menge T., Jander S., Stoll G. Induction of the proinflammatory cytokine interleukin-18 by axonal injury. J Neurosci Res 2001, 65:332-339.
30. Mert T., Gunay I., Ocal I., Guzel A.I., Inal T.C., Sencar L., et al. Macrophage depletion delays progression of neuropathic pain in diabetic animals. Naunyn Schmiedebergs Arch Pharmacol 2009, 379:445-452.
31. Miyoshi K., Obata K., Kondo T., Okamura H., Noguchi K. Interleukin-18-mediated microglia/astrocyte interaction in the spinal cord enhances neuropathic pain processing after nerve injury. J Neurosci 2008, 28:12775-12787.
32. Mizisin A.P., Weerasuriya A. Homeostatic regulation of the endoneurial microenvironment during development, aging and in response to trauma, disease and toxic insult. Acta Neuropathol (Berl) 2011, 121:291-312.
33. Mueller M., Wacker K., Ringelstein E.B., Hickey W.F., Imai Y., Kiefer R. Rapid response of identified resident endoneurial macrophages to nerve injury. Am J Pathol 2001, 159:2187-2197.
34. Mueller M., Leonhard C., Wacker K., Ringelstein E.B., Okabe M., Hickey W.F., et al. Macrophage response to peripheral nerve injury: the quantitative contribution of resident and hematogenous macrophages. Lab Invest 2003, 83:175-185.
35. Muller M., Wacker K., Getts D., Ringelstein E.B., Kiefer R. Further evidence for a crucial role of resident endoneurial macrophages in peripheral nerve disorders: lessons from acrylamide-induced neuropathy. Glia 2008, 56:1005-1016.
36. Myers R.R., Sekiguchi Y., Kikuchi S., Scott B., Medicherla S., Protter A., et al. Inhibition of p38 MAP kinase activity enhances axonal regeneration. Exp Neurol 2003, 184:606-614.
37. Nimmerjahn A., Kirchhoff F., Helmchen F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 2005, 308:1314-1318.
38. Obata K., Katsura H., Mizushima T., Sakurai J., Kobayashi K., Yamanaka H., et al. Roles of extracellular signal-regulated protein kinases 5 in spinal microglia and primary sensory neurons for neuropathic pain. J Neurochem 2007, 102:1569-1584.
39. Ochodnicka E., Ochdnicky M., Belej K., Fusekova E., Bosel'ova L. Quantitative analysis of myelinated nerve fibers of peripheral nerve in streptozotocin-induced diabetes mellitus. Mol Chem Neuropathol 1995, 25:225-233.
40. Ohsawa K., Imai Y., Kanazawa H., Sasaki Y., Kohsaka S. Involvement of Iba1 in membrane ruffling and phagocytosis of macrophages/microglia. J Cell Sci 2000, 113:3073-3084.
41. Pabreja K., Dua K., Sharma S., Padi S.S., Kulkarni S.K. Minocycline attenuates the development of diabetic neuropathic pain: possible anti-inflammatory and anti-oxidant mechanisms. Eur J Pharmacol 2011, 661:15-21.
42. Richardson S.J., Willcox A., Bone A.J., Morgan N.G., Foulis A.K. Immunopathology of the human pancreas in type-I diabetes. Semin Immunopathol 2011, 33:9-21.
43. Rio-Hortega P.D. Cytology and cellular pathology of the nervous system 1932, P.B. Hoeber, Inc., New York.
44. Romanovsky D., Hastings S.L., Stimers J.R., Dobretsov M. Relevance of hyperglycemia to early mechanical hyperalgesia in streptozotocin-induced diabetes. J Peripher Nerv Syst 2004, 9:62-69.
45. Rossini A.A., Like A.A., Chick W.L., Appel M.C., Cahill G.F. Studies of streptozotocin-induced insulitis and diabetes. Proc Natl Acad Sci USA 1977, 74:2485-2489.
46. Saijo K., Glass C.K. Microglial cell origin and phenotypes in health and disease. Nat Rev Immunol 2011, 11:775-787.
47. Schafers M., Sorkin L.S., Geis C., Shubayev V.I. Spinal nerve ligation induces transient upregulation of tumor necrosis factor receptors 1 and 2 in injured and adjacent uninjured dorsal root ganglia in the rat. Neurosci Lett 2003, 347:179-182.
48. Scholz J., Woolf C.J. The neuropathic pain triad: neurons, immune cells and glia. Nat Neurosci 2007, 10:1361-1368.
49. Scholz J., Abele A., Marian C., Haussler A., Herbert T.A., Woolf C.J., et al. Low-dose methotrexate reduces peripheral nerve injury-evoked spinal microglial activation and neuropathic pain behavior in rats. Pain 2008, 138:130-142.
50. Skundric D.S., Lisak R.P. Role of neuropoietic cytokines in development and progression of diabetic polyneuropathy: from glucose metabolism to neurodegeneration. Exp Diabesity Res 2003, 4:303-312.
51. Suzuki N., Hasegawa-Moriyama M., Takahashi Y., Kamikubo Y., Sakurai T., Inada E. Lidocaine attenuates the development of diabetic-induced tactile allodynia by inhibiting microglial activation. Anesth Analg 2011, 113:941-946.
52. Sweitzer S.M., Medicherla S., Almirez R., Dugar S., Chakravarty S., Shumilla J.A., et al. Antinociceptive action of a p38alpha MAPK inhibitor, SD-282, in a diabetic neuropathy model. Pain 2004, 109:409-419.
53. Thacker M.A., Clark A.K., Marchand F., McMahon S.B. Pathophysiology of peripheral neuropathic pain: immune cells and molecules. Anesth Analg 2007, 105:838-847.
54. Thornton P.D., Gerke M.B., Plenderleith M.B. Histochemical localisation of a galactose-containing glycoconjugate expressed by sensory neurons innervating different peripheral tissues in the rat. J Peripher Nerv Syst 2005, 10:47-57.
55. Tsuda M., Ueno H., Kataoka A., Tozaki-Saitoh H., Inoue K. Activation of dorsal horn microglia contributes to diabetes-induced tactile allodynia via extracellular signal-regulated protein kinase signaling. Glia 2008, 56:378-386.
56. Vallejo R., Tilley D.M., Vogel L., Benyamin R. The role of glia and the immune system in the development and maintenance of neuropathic pain. Pain Pract 2010, 10:167-184.
57. Vega-Avelaira D., Geranton S.M., Fitzgerald M. Differential regulation of immune responses and macrophage/neuron interactions in the dorsal root ganglion in young and adult rats following nerve injury. Mol Pain 2009, 5:70.
58. Vinik A.I., Bril V., Litchy W.J., Price K.L., Bastyr E.J. Sural sensory action potential identifies diabetic peripheral neuropathy responders to therapy. Muscle Nerve 2005, 32:619-625.
59. Wodarski R., Clark A.K., Grist J., Marchand F., Malcangio M. Gabapentin reverses microglial activation in the spinal cord of streptozotocin-induced diabetic rats. Eur J Pain 2009, 13:807-811.
60. Xu J.T., Xin W.J., Wei X.H., Wu C.Y., Ge Y.X., Liu Y.L., et al. p38 activation in uninjured primary afferent neurons and in spinal microglia contributes to the development of neuropathic pain induced by selective motor fiber injury. Exp Neurol 2007, 204:355-365.
61. 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.
62. Ziegler D., Muhlen H., Dannehl K., Gries F.A. Tibial nerve somatosensory evoked potentials at various stages of peripheral neuropathy in insulin dependent diabetic patients. J Neurol Neurosurg Psychiatry 1993, 56:58-64.