nach oben

Acta Neuropathologica

Erschienen in:

01.11.2015 | Review

Role of macrophages in Wallerian degeneration and axonal regeneration after peripheral nerve injury

verfasst von: Peiwen Chen, Xianhua Piao, Paolo Bonaldo

Erschienen in: Acta Neuropathologica | Ausgabe 5/2015

Einloggen, um Zugang zu erhalten

Abstract

The peripheral nervous system (PNS) has remarkable regenerative abilities after injury. Successful PNS regeneration relies on both injured axons and non-neuronal cells, including Schwann cells and immune cells. Macrophages are the most notable immune cells that play key roles in PNS injury and repair. Upon peripheral nerve injury, a large number of macrophages are accumulated at the injury sites, where they not only contribute to Wallerian degeneration, but also are educated by the local microenvironment and polarized to an anti-inflammatory phenotype (M2), thus contributing to axonal regeneration. Significant progress has been made in understanding how macrophages are educated and polarized in the injured microenvironment as well as how they contribute to axonal regeneration. Following the discussion on the main properties of macrophages and their phenotypes, in this review, we will summarize the current knowledge regarding the mechanisms of macrophage infiltration after PNS injury. Moreover, we will discuss the recent findings elucidating how macrophages are polarized to M2 phenotype in the injured PNS microenvironment, as well as the role and underlying mechanisms of macrophages in peripheral nerve injury, Wallerian degeneration and regeneration. Furthermore, we will highlight the potential application by targeting macrophages in treating peripheral nerve injury and peripheral neuropathies.

Arthur-Farraj PJ, Latouche M, Wilton DK, Quintes S, Chabrol E, Banerjee A, Woodhoo A, Jenkins B, Rahman M, Turmaine M, Wicher GK, Mitter R, Greensmith L, Behrens A, Raivich G, Mirsky R, Jessen KR (2012) c-Jun reprograms Schwann cells of injured nerves to generate a repair cell essential for regeneration. Neuron 75:633–647PubMedCentralPubMedCrossRef

Avellino AM, Dailey AT, Harlan JM, Sharar SR, Winn RK, McNutt LD, Kliot M (2004) Blocking of up-regulated ICAM-1 does not prevent macrophage infiltration during Wallerian degeneration of peripheral nerve. Exp Neurol 187:430–444PubMedCrossRef

Baitsch D, Bock HH, Engel T, Telgmann R, Müller-Tidow C, Varga G, Bot M, Herz J, Robenek H, von Eckardstein A, Nofer JR (2011) Apolipoprotein E induces antiinflammatory phenotype in macrophages. Arterioscler Thromb Vasc Biol 31:1160–1168PubMedCentralPubMedCrossRef

Barrette B, Hébert MA, Filali M, Lafortune K, Vallières N, Gowing G, Julien JP, Lacroix S (2008) Requirement of myeloid cells for axon regeneration. J Neurosci 28:9363–9376PubMedCrossRef

Bendszus M, Stoll G (2003) Caught in the act: in vivo mapping of macrophage infiltration in nerve injury by magnetic resonance imaging. J Neurosci 23:10892–10896PubMed

Benowitz LI, Popovich PG (2011) Inflammation and axon regeneration. Curr Opin Neurol 24:577–583PubMedCrossRef

Beuche W, Friede RL (1986) Myelin phagocytosis in Wallerian degeneration of peripheral nerves depends on silica-sensitive, bg/bg-negative and Fc-positive monocytes. Brain Res 378:97–106PubMedCrossRef

Bianco C, Gotze O, Cohn ZA (1979) Regulation of macrophage migration by products of the complement system. Proc Natl Acad Sci USA 76:888–891PubMedCentralPubMedCrossRef

Boivin A, Pineau I, Barrette B, Filali M, Vallières N, Rivest S, Lacroix S (2007) Toll-like receptor signaling is critical for Wallerian degeneration and functional recovery after peripheral nerve injury. J Neurosci 27:12565–12576PubMedCrossRef

10.

Brown BN, Ratner BD, Goodman SB, Amar S, Badylak SF (2012) Macrophage polarization: an opportunity for improved outcomes in biomaterials and regenerative medicine. Biomaterials 33:3792–3802PubMedCentralPubMedCrossRef

11.

Brown HC, Castaño A, Fearn S, Townsend M, Edwards G, Streuli C, Perry VH (1997) Adhesion molecules involved in macrophage responses to Wallerian degeneration in the murine peripheral nervous system. Eur J Neurosci 9:2057–2063PubMedCrossRef

12.

Bruck W (1997) The role of macrophages in Wallerian degeneration. Brain Pathol 7:741–752PubMedCrossRef

13.

Bruck W, Bruck Y, Friede RL (1992) TNF-alpha suppresses CR3-mediated myelin removal by macrophages. J Neuroimmunol 38:9–17PubMedCrossRef

14.

Bruck W, Friede RL (1991) The role of complement in myelin phagocytosis during PNS wallerian degeneration. J Neurol Sci 103:182–187PubMedCrossRef

15.

Bruck W, Friede RL (1990) Anti-macrophage CR3 antibody blocks myelin phagocytosis by macrophages in vitro. Acta Neuropathol 80:415–418PubMedCrossRef

16.

Camara-Lemarroy CR, Guzman-de la Garza FJ, Fernandez-Garza NE (2010) Molecular inflammatory mediators in peripheral nerve degeneration and regeneration. Neuroimmunomodulation 17:314–324PubMedCrossRef

17.

Castano A, Bell MD, Perry VH (1996) Unusual aspects of inflammation in the nervous system: Wallerian degeneration. Neurobiol Aging 17:745–751PubMedCrossRef

18.

Cattin AL, Burden JJ, Van Emmenis L, Mackenzie FE, Hoving JJ, Garcia Calavia N, Guo Y, McLaughlin M, Rosenberg LH, Quereda V, Jamecna D, Napoli I, Parrinello S, Enver T, Ruhrberg C, Lloyd AC (2015) Macrophage-induced blood vessels guide schwann cell-mediated regeneration of peripheral nerves. Cell 162:1127–1139PubMedCentralPubMedCrossRef

19.

Chen P, Bonaldo P (2013) Role of macrophage polarization in tumor angiogenesis and vessel normalization: implications for new anticancer therapies. Int Rev Cell Mol Biol 301:1–35PubMedCrossRef

20.

Chen P, Cescon M, Megighian A, Bonaldo P (2014) Collagen VI regulates peripheral nerve myelination and function. FASEB J 28:1145–1156PubMedCrossRef

21.

Chen P, Cescon M, Zuccolotto G, Nobbio L, Colombelli C, Filaferro M, Vitale G, Feltri ML, Bonaldo P (2015) Collagen VI regulates peripheral nerve regeneration by modulating macrophage recruitment and polarization. Acta Neuropathol 129:97–113PubMedCrossRef

22.

Chen ZL, Yu WM, Strickland S (2007) Peripheral regeneration. Annu Rev Neurosci 30:209–233PubMedCrossRef

23.

Chernov AV, Dolkas J, Hoang K, Angert M, Srikrishna G, Vogl T, Baranovskaya S, Strongin AY, Shubayev VI (2015) The Calcium-binding proteins S100A8 and S100A9 initiate the early inflammatory program in injured peripheral nerves. J Biol Chem 290:11771–11784PubMedCrossRef

24.

Cote SC, Pasvanis S, Bounou S, Dumais N (2009) CCR7-specific migration to CCL19 and CCL21 is induced by PGE(2) stimulation in human monocytes: involvement of EP(2)/EP(4) receptors activation. Mol Immunol 46:2682–2693PubMedCrossRef

25.

Dailey AT, Avellino AM, Benthem L, Silver J, Kliot M (1998) Complement depletion reduces macrophage infiltration and activation during Wallerian degeneration and axonal regeneration. J Neurosci 18:6713–6722PubMed

26.

de Jonge RR, van Schaik IN, Vreijling JP, Troost D, Baas F (2004) Expression of complement components in the peripheral nervous system. Hum Mol Genet 13:295–302PubMedCrossRef

27.

Dessing MC, Tammaro A, Pulskens WP, Teske GJ, Butter LM, Claessen N, van Eijk M, van der Poll T, Vogl T, Roth J, Florquin S, Leemans JC (2015) The calcium-binding protein complex S100A8/A9 has a crucial role in controlling macrophage-mediated renal repair following ischemia/reperfusion. Kidney Int 87:85–94PubMedCrossRef

28.

Diaz-Munoz MD, Osma-Garcia IC, Iniguez MA, Fresno M (2013) Cyclooxygenase-2 deficiency in macrophages leads to defective p110gamma PI3K signaling and impairs cell adhesion and migration. J Immunol 191:395–406PubMedCrossRef

29.

Doulatov S, Notta F, Eppert K, Nguyen LT, Ohashi PS, Dick JE (2010) Revised map of the human progenitor hierarchy shows the origin of macrophages and dendritic cells in early lymphoid development. Nat Immunol 11:585–593PubMedCrossRef

30.

Dubovy P (2011) Wallerian degeneration and peripheral nerve conditions for both axonal regeneration and neuropathic pain induction. Ann Anat 193:267–275PubMedCrossRef

31.

Ehrchen JM, Sunderkotter C, Foell D, Vogl T, Roth J (2009) The endogenous Toll-like receptor 4 agonist S100A8/S100A9 (calprotectin) as innate amplifier of infection, autoimmunity, and cancer. J Leukoc Biol 86:557–566PubMedCrossRef

32.

Ferrante CJ, Leibovich SJ (2012) Regulation of macrophage polarization and wound healing. Adv Wound Care (New Rochelle) 1:10–16CrossRef

33.

Ferrante CJ, Pinhal-Enfield G, Elson G, Cronstein BN, Hasko G, Outram S, Leibovich SJ (2013) The adenosine-dependent angiogenic switch of macrophages to an M2-like phenotype is independent of interleukin-4 receptor alpha (IL-4Ralpha) signaling. Inflammation 36:921–931PubMedCentralPubMedCrossRef

34.

Francesco-Lisowitz A, Lindborg JA, Niemi JP, Zigmond RE (2015) The neuroimmunology of degeneration and regeneration in the peripheral nervous system. Neuroscience 302:174–203CrossRef

35.

Franco R, Fernandez-Suarez D (2015) Alternatively activated microglia and macrophages in the central nervous system. Prog Neurobiol 131:65–86PubMedCrossRef

36.

Galli SJ, Borregaard N, Wynn TA (2011) Phenotypic and functional plasticity of cells of innate immunity: macrophages, mast cells and neutrophils. Nat Immunol 12:1035–1044PubMedCentralPubMedCrossRef

37.

Gaudet AD, Leung M, Poirier F, Kadoya T, Horie H, Ramer MS (2009) A role for galectin-1 in the immune response to peripheral nerve injury. Exp Neurol 220:320–327PubMedCrossRef

38.

Gaudet AD, Popovich PG, Ramer MS (2011) Wallerian degeneration: gaining perspective on inflammatory events after peripheral nerve injury. J Neuroinflammation 8:110PubMedCentralPubMedCrossRef

39.

Gomez PE, Klapproth K, Schulz C, Busch K, Azzoni E, Crozet L, Garner H, Trouillet C, de Bruijn MF, Geissmann F, Rodewald HR (2015) Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors. Nature 518:547–551CrossRef

40.

Gordon S, Taylor PR (2005) Monocyte and macrophage heterogeneity. Nat Rev Immunol 5:953–964PubMedCrossRef

41.

Gray M, Palispis W, Popovich PG, van Rooijen N, Gupta R (2007) Macrophage depletion alters the blood–nerve barrier without affecting Schwann cell function after neural injury. J Neurosci Res 85:766–777PubMedCrossRef

42.

Griffin JW, George R, Ho T (1993) Macrophage systems in peripheral nerves. A review. J Neuropathol Exp Neurol 52:553–560PubMedCrossRef

43.

Hack CE, Wolbink GJ, Schalkwijk C, Speijer H, Hermens WT, van den Bosch H (1997) A role for secretory phospholipase A2 and C-reactive protein in the removal of injured cells. Immunol Today 18:111–115PubMedCrossRef

44.

Hikawa N, Takenaka T (1996) Myelin-stimulated macrophages release neurotrophic factors for adult dorsal root ganglion neurons in culture. Cell Mol Neurobiol 16:517–528PubMedCrossRef

45.

Hiratsuka S, Watanabe A, Aburatani H, Maru Y (2006) Tumour-mediated upregulation of chemoattractants and recruitment of myeloid cells predetermines lung metastasis. Nat Cell Biol 8:1369–1375PubMedCrossRef

46.

Hiratsuka S, Watanabe A, Sakurai Y, Akashi-Takamura S, Ishibashi S, Miyake K, Shibuya M, Akira S, Aburatani H, Maru Y (2008) The S100A8-serum amyloid A3-TLR4 paracrine cascade establishes a pre-metastatic phase. Nat Cell Biol 10:1349–1355PubMedCrossRef

47.

Horie H, Kadoya T, Hikawa N, Sango K, Inoue H, Takeshita K, Asawa R, Hiroi T, Sato M, Yoshioka T, Ishikawa Y (2004) Oxidized galectin-1 stimulates macrophages to promote axonal regeneration in peripheral nerves after axotomy. J Neurosci 24:1873–1880PubMedCrossRef

48.

Huang JK, Phillips GR, Roth AD, Pedraza L, Shan W, Belkaid W, Mi S, Fex-Svenningsen A, Florens L, Yates JR 3rd, Colman DR (2005) Glial membranes at the node of Ranvier prevent neurite outgrowth. Science 310:1813–1817PubMedCrossRef

49.

Jang SY, Shin YK, Lee HY, Park JY, Suh DJ, Kim JK, Bae YS, Park HT (2012) Local production of serum amyloid a is implicated in the induction of macrophage chemoattractants in Schwann cells during wallerian degeneration of peripheral nerves. Glia 60:1619–1628PubMedCrossRef

50.

Kallenborn-Gerhardt W, Hohmann SW, Syhr KM, Schröder K, Sisignano M, Weigert A, Lorenz JE, Lu R, Brüne B, Brandes RP, Geisslinger G, Schmidtko A (2014) Nox2-dependent signaling between macrophages and sensory neurons contributes to neuropathic pain hypersensitivity. Pain 155:2161–2170PubMedCrossRef

51.

Keilhoff G, Langnaese K, Wolf G, Fansa H (2007) Inhibiting effect of minocycline on the regeneration of peripheral nerves. Dev Neurobiol 67:1382–1395PubMedCrossRef

52.

Kiguchi N, Kobayashi Y, Saika F, Kishioka S (2013) Epigenetic upregulation of CCL2 and CCL3 via histone modifications in infiltrating macrophages after peripheral nerve injury. Cytokine 64:666–672PubMedCrossRef

53.

Kiguchi N, Kobayashi Y, Saika F, Sakaguchi H, Maeda T, Kishioka S (2015) Peripheral interleukin-4 ameliorates inflammatory macrophage-dependent neuropathic pain. Pain 156:684–693PubMedCrossRef

54.

Kim D, You B, Lim H, Lee SJ (2011) Toll-like receptor 2 contributes to chemokine gene expression and macrophage infiltration in the dorsal root ganglia after peripheral nerve injury. Mol Pain 7:74PubMedCentralPubMedCrossRef

55.

Kim Y, Remacle AG, Chernov AV, Liu H, Shubayev I, Lai C, Dolkas J, Shiryaev SA, Golubkov VS, Mizisin AP, Strongin AY, Shubayev VI (2012) The MMP-9/TIMP-1 axis controls the status of differentiation and function of myelin-forming Schwann cells in nerve regeneration. PLoS One 7:e33664PubMedCentralPubMedCrossRef

56.

Konofaos P, Terzis JK (2013) FK506 and nerve regeneration: past, present, and future. J Reconstr Microsurg 29:141–148PubMedCrossRef

57.

Kvist M, Danielsen N, Dahlin LB (2003) Effects of FK506 on regeneration and macrophages in injured rat sciatic nerve. J Peripher Nerv Syst 8:251–259PubMedCrossRef

58.

Lauber K, Bohn E, Krober SM, Xiao YJ, Blumenthal SG, Lindemann RK, Marini P, Wiedig C, Zobywalski A, Baksh S, Xu Y, Autenrieth IB, Schulze-Osthoff K, Belka C, Stuhler G, Wesselborg S (2003) Apoptotic cells induce migration of phagocytes via caspase-3-mediated release of a lipid attraction signal. Cell 113:717–730PubMedCrossRef

59.

Lee HK, Shin YK, Jung J, Seo SY, Baek SY, Park HT (2009) Proteasome inhibition suppresses Schwann cell dedifferentiation in vitro and in vivo. Glia 57:1825–1834PubMedCrossRef

60.

Lee HY, Kim MK, Park KS, Shin EH, Jo SH, Kim SD, Jo EJ, Lee YN, Lee C, Baek SH, Bae YS (2006) Serum amyloid A induces contrary immune responses via formyl peptide receptor-like 1 in human monocytes. Mol Pharmacol 70:241–248PubMedCrossRef

61.

Lee HY, Kim SD, Shim JW, Lee SY, Lee H, Cho KH, Yun J, Bae YS (2008) Serum amyloid A induces CCL2 production via formyl peptide receptor-like 1-mediated signaling in human monocytes. J Immunol 181:4332–4339PubMedCrossRef

62.

Liou JT, Lee CM, Lin YC, Chen CY, Liao CC, Lee HC, Day YJ (2013) P-selectin is required for neutrophils and macrophage infiltration into injured site and contributes to generation of behavioral hypersensitivity following peripheral nerve injury in mice. Pain 154:2150–2159PubMedCrossRef

63.

Liou JT, Liu FC, Mao CC, Lai YS, Day YJ (2011) Inflammation confers dual effects on nociceptive processing in chronic neuropathic pain model. Anesthesiology 114:660–672PubMedCrossRef

64.

Liu T, van Rooijen N, Tracey DJ (2000) Depletion of macrophages reduces axonal degeneration and hyperalgesia following nerve injury. Pain 86:25–32PubMedCrossRef

65.

Lu X, Richardson PM (1993) Responses of macrophages in rat dorsal root ganglia following peripheral nerve injury. J Neurocytol 22:334–341PubMedCrossRef

66.

Malik RK, Ghurye RR, Lawrence-Watt DJ, Stewart HJ (2009) Galectin-1 stimulates monocyte chemotaxis via the p44/42 MAP kinase pathway and a pertussis toxin-sensitive pathway. Glycobiology 19:1402–1407PubMedCrossRef

67.

Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 25:677–686PubMedCrossRef

68.

Mantovani A, Sozzani S, Locati M, Allavena P, Sica A (2002) Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol 23:549–555PubMedCrossRef

69.

Martinez FO, Gordon S (2014) The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep 6:13PubMedCentralPubMedCrossRef

70.

Martinez FO, Sica A, Mantovani A, Locati M (2008) Macrophage activation and polarization. Front Biosci 13:453–461PubMedCrossRef

71.

Martini R, Fischer S, Lopez-Vales R, David S (2008) Interactions between Schwann cells and macrophages in injury and inherited demyelinating disease. Glia 56:1566–1577PubMedCrossRef

72.

Moalem G, Tracey DJ (2006) Immune and inflammatory mechanisms in neuropathic pain. Brain Res Rev 51:240–264PubMedCrossRef

73.

Mokarram N, Merchant A, Mukhatyar V, Patel G, Bellamkonda RV (2012) Effect of modulating macrophage phenotype on peripheral nerve repair. Biomaterials 33:8793–8801PubMedCentralPubMedCrossRef

74.

Mueller M, Leonhard C, Wacker K, Ringelstein EB, Okabe M, Hickey WF, Kiefer R (2003) Macrophage response to peripheral nerve injury: the quantitative contribution of resident and hematogenous macrophages. Lab Invest 83:175–185PubMedCrossRef

75.

Mueller M, Wacker K, Ringelstein EB, Hickey WF, Imai Y, Kiefer R (2001) Rapid response of identified resident endoneurial macrophages to nerve injury. Am J Pathol 159:2187–2197PubMedCentralPubMedCrossRef

76.

Murinson BB, Archer DR, Li Y, Griffin JW (2005) Degeneration of myelinated efferent fibers prompts mitosis in Remak Schwann cells of uninjured C-fiber afferents. J Neurosci 25:1179–1187PubMedCrossRef

77.

Myers RR, Heckman HM, Rodriguez M (1996) Reduced hyperalgesia in nerve-injured WLD mice: relationship to nerve fiber phagocytosis, axonal degeneration, and regeneration in normal mice. Exp Neurol 141:94–101PubMedCrossRef

78.

Nadeau S, Filali M, Zhang J, Kerr BJ, Rivest S, Soulet D, Iwakura Y, de Rivero Vaccari JP, Keane RW, Lacroix S (2011) Functional recovery after peripheral nerve injury is dependent on the pro-inflammatory cytokines IL-1beta and TNF: implications for neuropathic pain. J Neurosci 31:12533–12542PubMedCrossRef

79.

Namikawa K, Fukushima M, Murakami K, Suzuki A, Takasawa S, Okamoto H, Kiyama H (2005) Expression of Reg/PAP family members during motor nerve regeneration in rat. Biochem Biophys Res Commun 332:126–134PubMedCrossRef

80.

Namikawa K, Okamoto T, Suzuki A, Konishi H, Kiyama H (2006) Pancreatitis-associated protein-III is a novel macrophage chemoattractant implicated in nerve regeneration. J Neurosci 26:7460–7467PubMedCrossRef

81.

Napoli I, Noon LA, Ribeiro S, Kerai AP, Parrinello S, Rosenberg LH, Collins MJ, Harrisingh MC, White IJ, Woodhoo A, Lloyd AC (2012) A central role for the ERK-signaling pathway in controlling Schwann cell plasticity and peripheral nerve regeneration in vivo. Neuron 73:729–742PubMedCrossRef

82.

Nicol LS, Dawes JM, La RF, Didangelos A, Clark AK, Gentry C, Grist J, Davies JB, Malcangio M, McMahon SB (2015) The role of G-protein receptor 84 in experimental neuropathic pain. J Neurosci 35:8959–8969PubMedCentralPubMedCrossRef

83.

Niemi JP, Francesco-Lisowitz A, Roldan-Hernandez L, Lindborg JA, Mandell D, Zigmond RE (2013) A critical role for macrophages near axotomized neuronal cell bodies in stimulating nerve regeneration. J Neurosci 33:16236–16248PubMedCentralPubMedCrossRef

84.

Painter MW, Brosius LA, Cheng YC, Latremoliere A, Duong K, Miller CM, Posada S, Cobos EJ, Zhang AX, Wagers AJ, Havton LA, Barres B, Omura T, Woolf CJ (2014) Diminished Schwann cell repair responses underlie age-associated impaired axonal regeneration. Neuron 83:331–343PubMedCentralPubMedCrossRef

85.

Parrinello S, Napoli I, Ribeiro S, Wingfield Digby P, Fedorova M, Parkinson DB, Doddrell RD, Nakayama M, Adams RH, Lloyd AC (2010) EphB signaling directs peripheral nerve regeneration through Sox2-dependent Schwann cell sorting. Cell 143:145–155PubMedCrossRef

86.

Perrin FE, Lacroix S, viles-Trigueros M, David S (2005) Involvement of monocyte chemoattractant protein-1, macrophage inflammatory protein-1alpha and interleukin-1beta in Wallerian degeneration. Brain 128:854–866PubMedCrossRef

87.

Perry VH, Brown MC (1992) Role of macrophages in peripheral nerve degeneration and repair. BioEssays 14:401–406PubMedCrossRef

88.

Perry VH, Brown MC, Gordon S (1987) The macrophage response to central and peripheral nerve injury. A possible role for macrophages in regeneration. J Exp Med 165:1218–1223PubMedCrossRef

89.

Popiolek-Barczyk K, Kolosowska N, Piotrowska A, Makuch W, Rojewska E, Jurga AM, Pilat D, Mika J (2015) Parthenolide relieves pain and promotes M2 microglia/macrophage polarization in rat model of neuropathy. Neural Plast 2015:676473PubMedCentralPubMed

90.

Potas JR, Haque F, Maclean FL, Nisbet DR (2015) Interleukin-10 conjugated electrospun polycaprolactone (PCL) nanofibre scaffolds for promoting alternatively activated (M2) macrophages around the peripheral nerve in vivo. J Immunol Methods 420:38–49PubMedCrossRef

91.

Prinz M, Priller J (2014) Microglia and brain macrophages in the molecular age: from origin to neuropsychiatric disease. Nat Rev Neurosci 15:300–312PubMedCrossRef

92.

Pyonteck SM, Akkari L, Schuhmacher AJ, Bowman RL, Sevenich L, Quail DF, Olson OC, Quick ML, Huse JT, Teijeiro V, Setty M, Leslie CS, Oei Y, Pedraza A, Zhang J, Brennan CW, Sutton JC, Holland EC, Daniel D, Joyce JA (2013) CSF-1R inhibition alters macrophage polarization and blocks glioma progression. Nat Med 19:1264–1272PubMedCrossRef

93.

Qian BZ, Pollard JW (2010) Macrophage diversity enhances tumor progression and metastasis. Cell 141:39–51PubMedCrossRef

94.

Ramaglia V, Wolterman R, de Kok M, Vigar MA, Wagenaar-Bos I, King RH, Morgan BP, Baas F (2008) Soluble complement receptor 1 protects the peripheral nerve from early axon loss after injury. Am J Pathol 172:1043–1052PubMedCentralPubMedCrossRef

95.

Ristoiu V (2013) Contribution of macrophages to peripheral neuropathic pain pathogenesis. Life Sci 93:870–881PubMedCrossRef

96.

Rolny C, Mazzone M, Tugues S, Laoui D, Johansson I, Coulon C, Squadrito ML, Segura I, Li X, Knevels E, Costa S, Vinckier S, Dresselaer T, Åkerud P, De Mol M, Salomäki H, Phillipson M, Wyns S, Larsson E, Buysschaert I, Botling J, Himmelreich U, Van Ginderachter JA, De Palma M, Dewerchin M, Claesson-Welsh L, Carmeliet P (2011) HRG inhibits tumor growth and metastasis by inducing macrophage polarization and vessel normalization through downregulation of PlGF. Cancer Cell 19:31–44PubMedCrossRef

97.

Rosenberg AF, Wolman MA, Franzini-Armstrong C, Granato M (2012) In vivo nerve-macrophage interactions following peripheral nerve injury. J Neurosci 32:3898–3909PubMedCentralPubMedCrossRef

98.

Rotshenker S (2011) Wallerian degeneration: the innate-immune response to traumatic nerve injury. J Neuroinflammation 8:109PubMedCentralPubMedCrossRef

99.

Ruffell B, Coussens LM (2015) Macrophages and therapeutic resistance in cancer. Cancer Cell 27:462–472PubMedCrossRef

100.

Saada A, Dunaevsky-Hutt A, Aamar A, Reichert F, Rotshenker S (1995) Fibroblasts that reside in mouse and frog injured peripheral nerves produce apolipoproteins. J Neurochem 64:1996–2003PubMedCrossRef

101.

Scheidt P, Friede RL (1987) Myelin phagocytosis in Wallerian degeneration. Properties of millipore diffusion chambers and immunohistochemical identification of cell populations. Acta Neuropathol 75:77–84PubMedCrossRef

102.

Schiopu A, Cotoi OS (2013) S100A8 and S100A9: DAMPs at the crossroads between innate immunity, traditional risk factors, and cardiovascular disease. Mediators Inflamm 2013:828354PubMedCentralPubMedCrossRef

103.

Schreiber RC, Krivacic K, Kirby B, Vaccariello SA, Wei T, Ransohoff RM, Zigmond RE (2001) Monocyte chemoattractant protein (MCP)-1 is rapidly expressed by sympathetic ganglion neurons following axonal injury. NeuroReport 12:601–606PubMedCrossRef

104.

Schreiber RC, Shadiack AM, Bennett TA, Sedwick CE, Zigmond RE (1995) Changes in the macrophage population of the rat superior cervical ganglion after postganglionic nerve injury. J Neurobiol 27:141–153PubMedCrossRef

105.

Schuh CD, Pierre S, Weigert A, Weichand B, Altenrath K, Schreiber Y, Ferreiros N, Zhang DD, Suo J, Treutlein EM, Henke M, Kunkel H, Grez M, Nüsing R, Brüne B, Geisslinger G, Scholich K (2014) Prostacyclin mediates neuropathic pain through interleukin 1beta-expressing resident macrophages. Pain 155:545–555PubMedCrossRef

106.

Schulz C, Schafer A, Stolla M, Kerstan S, Lorenz M, von Brühl ML, Schiemann M, Bauersachs J, Gloe T, Busch DH, Gawaz M, Massberg S (2007) Chemokine fractalkine mediates leukocyte recruitment to inflammatory endothelial cells in flowing whole blood: a critical role for P-selectin expressed on activated platelets. Circulation 116:764–773PubMedCrossRef

107.

Seitz RJ, Reiners K, Himmelmann F, Heininger K, Hartung HP, Toyka KV (1989) The blood-nerve barrier in Wallerian degeneration: a sequential long-term study. Muscle Nerve 12:627–635PubMedCrossRef

108.

Semple JW, Freedman J (2010) Platelets and innate immunity. Cell Mol Life Sci 67:499–511PubMedCrossRef

109.

Shamash S, Reichert F, Rotshenker S (2002) The cytokine network of Wallerian degeneration: tumor necrosis factor-alpha, interleukin-1alpha, and interleukin-1beta. J Neurosci 22:3052–3060PubMed

110.

Siebert H, Dippel N, Mader M, Weber F, Weber F, Brück W (2001) Matrix metalloproteinase expression and inhibition after sciatic nerve axotomy. J Neuropathol Exp Neurol 60:85–93PubMedCrossRef

111.

Siebert H, Sachse A, Kuziel WA, Maeda N, Bruck W (2000) The chemokine receptor CCR2 is involved in macrophage recruitment to the injured peripheral nervous system. J Neuroimmunol 110:177–185PubMedCrossRef

112.

Sierra-Filardi E, Nieto C, Dominguez-Soto A, Barroso R, Sanchez-Mateos P, Puig-Kroger A, Lopez-Bravo M, Joven J, Ardavin C, Rodríguez-Fernandez JL, Sanchez-Torres C, Mellado M, Corbi AL (2014) CCL2 shapes macrophage polarization by GM-CSF and M-CSF: identification of CCL2/CCR2-dependent gene expression profile. J Immunol 192:3858–3867PubMedCrossRef

113.

Smythies LE, Sellers M, Clements RH, Mosteller-Barnum M, Meng G, Benjamin WH, Orenstein JM, Smith PD (2005) Human intestinal macrophages display profound inflammatory anergy despite avid phagocytic and bacteriocidal activity. J Clin Invest 115:66–75PubMedCentralPubMedCrossRef

114.

Snipes GJ, McGuire CB, Norden JJ, Freeman JA (1986) Nerve injury stimulates the secretion of apolipoprotein E by nonneuronal cells. Proc Natl Acad Sci USA 83:1130–1134PubMedCentralPubMedCrossRef

115.

Sommer C, Schafers M (1998) Painful mononeuropathy in C57BL/Wld mice with delayed wallerian degeneration: differential effects of cytokine production and nerve regeneration on thermal and mechanical hypersensitivity. Brain Res 784:154–162PubMedCrossRef

116.

Stoll G, Muller HW (1999) Nerve injury, axonal degeneration and neural regeneration: basic insights. Brain Pathol 9:313–325PubMedCrossRef

117.

Tanaka T, Minami M, Nakagawa T, Satoh M (2004) Enhanced production of monocyte chemoattractant protein-1 in the dorsal root ganglia in a rat model of neuropathic pain: possible involvement in the development of neuropathic pain. Neurosci Res 48:463–469PubMedCrossRef

118.

Taskinen HS, Roytta M (1997) The dynamics of macrophage recruitment after nerve transection. Acta Neuropathol 93:252–259PubMedCrossRef

119.

Tchernychev B, Furie B, Furie BC (2003) Peritoneal macrophages express both P-selectin and PSGL-1. J Cell Biol 163:1145–1155PubMedCentralPubMedCrossRef

120.

Toews AD, Barrett C, Morell P (1998) Monocyte chemoattractant protein 1 is responsible for macrophage recruitment following injury to sciatic nerve. J Neurosci Res 53:260–267PubMedCrossRef

121.

Tofaris GK, Patterson PH, Jessen KR, Mirsky R (2002) Denervated Schwann cells attract macrophages by secretion of leukemia inhibitory factor (LIF) and monocyte chemoattractant protein-1 in a process regulated by interleukin-6 and LIF. J Neurosci 22:6696–6703PubMed

122.

Uhlar CM, Whitehead AS (1999) Serum amyloid A, the major vertebrate acute-phase reactant. Eur J Biochem 265:501–523PubMedCrossRef

123.

Van SJ, Auvynet C, Sapienza A, Reaux-Le Goazigo A, Combadiere C, Melik Parsadaniantz S (2015) Stromal cell-derived CCL2 drives neuropathic pain states through myeloid cell infiltration in injured nerve. Brain Behav Immun 45:198–210CrossRef

124.

Vargas ME, Watanabe J, Singh SJ, Robinson WH, Barres BA (2010) Endogenous antibodies promote rapid myelin clearance and effective axon regeneration after nerve injury. Proc Natl Acad Sci USA 107:11993–11998PubMedCentralPubMedCrossRef

125.

Vougioukas VI, Roeske S, Michel U, Bruck W (1998) Wallerian degeneration in ICAM-1-deficient mice. Am J Pathol 152:241–249PubMedCentralPubMed

126.

Yang J, Gu Y, Huang X, Shen A, Cheng C (2011) Dynamic changes of ICAM-1 expression in peripheral nervous system following sciatic nerve injury. Neurol Res 33:75–83PubMedCrossRef

127.

Ydens E, Cauwels A, Asselbergh B, Goethals S, Peeraer L, Lornet G, Almeida-Souza L, Van Ginderachter JA, Timmerman V, Janssens S (2012) Acute injury in the peripheral nervous system triggers an alternative macrophage response. J Neuroinflammation 9:176PubMedCentralPubMedCrossRef

128.

Zhang L, Johnson D, Johnson JA (2013) Deletion of Nrf2 impairs functional recovery, reduces clearance of myelin debris and decreases axonal remyelination after peripheral nerve injury. Neurobiol Dis 54:329–338PubMedCentralPubMedCrossRef

Titel: Role of macrophages in Wallerian degeneration and axonal regeneration after peripheral nerve injury
verfasst von: Peiwen Chen
Xianhua Piao
Paolo Bonaldo
Publikationsdatum: 01.11.2015
Verlag: Springer Berlin Heidelberg
Erschienen in: Acta Neuropathologica / Ausgabe 5/2015
Print ISSN: 0001-6322
Elektronische ISSN: 1432-0533
DOI: https://doi.org/10.1007/s00401-015-1482-4

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Neu im Fachgebiet Neurologie

23.04.2024 | Demenz | Nachrichten

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Live-Webinar: Aktuelle Leitlinien bei Herz-Kreislauf-Erkrankungen

Springer Medizin

Role of macrophages in Wallerian degeneration and axonal regeneration after peripheral nerve injury

Abstract

Leitlinien kompakt für die Neurologie

Neu im Fachgebiet Neurologie

Demenzkranke durch Antipsychotika vielfach gefährdet

Parkinson-Therapie im Wandel – aktuelle Leitlinie im Fokus

Auf diese Krankheiten bei Geflüchteten sollten Sie vorbereitet sein

Hustenstiller lindert Agitation bei Alzheimer

Update Neurologie

Live-Webinar: Aktuelle Leitlinien bei Herz-Kreislauf-Erkrankungen

Springer Medizin

Abstract

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 5/2015

PDCD10 (CCM3) regulates brain endothelial barrier integrity in cerebral cavernous malformation type 3: role of CCM3-ERK1/2-cortactin cross-talk

Comparing the efficacy and neuroinflammatory potential of three anti-abeta antibodies

Functional recovery in new mouse models of ALS/FTLD after clearance of pathological cytoplasmic TDP-43

Abeta targets of the biosimilar antibodies of Bapineuzumab, Crenezumab, Solanezumab in comparison to an antibody against N-truncated Abeta in sporadic Alzheimer disease cases and mouse models

Short-term suppression of A315T mutant human TDP-43 expression improves functional deficits in a novel inducible transgenic mouse model of FTLD-TDP and ALS

Rab1-dependent ER–Golgi transport dysfunction is a common pathogenic mechanism in SOD1, TDP-43 and FUS-associated ALS

Leitlinien kompakt für die Neurologie

Neu im Fachgebiet Neurologie

Demenzkranke durch Antipsychotika vielfach gefährdet

Parkinson-Therapie im Wandel – aktuelle Leitlinie im Fokus

Auf diese Krankheiten bei Geflüchteten sollten Sie vorbereitet sein

Hustenstiller lindert Agitation bei Alzheimer

Update Neurologie