Involvement of placental growth factor in Wallerian degeneration

GLIA

Volumn 59, Issue 3, 2011, Pages 379-396

  Chaballe, Linda ^a   Close, Pierre ^a   Sempels, Maxime ^a   Delstanche, Stéphanie ^a   Fanielle, Julien ^a   Moons, Lieve ^b   Carmeliet, Peter ^c,d   Schoenen, Jean ^a   Chariot, Alain ^a   Franzen, Rachelle ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b SKELETAL BIOLOGY AND ENGINEERING RESEARCH CENTER   (Belgium)

^c DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^d UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Cytokine; Inflammation; NF B; PNS injury; Schwann cell

Indexed keywords

CYTOKINE; GELATINASE B; I KAPPA B; INTERSTITIAL COLLAGENASE; PLACENTAL GROWTH FACTOR; SYNAPTOTAGMIN I;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; MACROPHAGE; NERVE DEGENERATION; NERVE TRANSECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MICROARRAY; SCHWANN CELL; SCIATIC NERVE; WILD TYPE;

ANIMALS; CELLS, CULTURED; CYTOKINES; DISEASE MODELS, ANIMAL; FEMALE; MICE; MICE, KNOCKOUT; MOLECULAR DYNAMICS SIMULATION; NERVE FIBERS, MYELINATED; PREGNANCY PROTEINS; SCHWANN CELLS; SCIATIC NEUROPATHY; WALLERIAN DEGENERATION;

EID: 78751681442     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.21108     Document Type: Article

References (78)

1. Anton ES, Weskamp G, Reichardt LF, Matthew WD. 1994. Nerve growth factor and its low-affinity receptor promote Schwann cell migration. Proc Natl Acad Sci USA 91: 2795-2799.
2. Autiero M, Luttun A, Tjwa M, Carmeliet P. 2003a. Placental growth factor and its receptor, vascular endothelial growth factor receptor-1: Novel targets for stimulation of ischemic tissue revascularization and inhibition of angiogenic and inflammatory disorders. J Thromb Haemost 1: 1356-1370.
3. Autiero M, Waltenberger J, Communni D, Kranz A, Moons L, Lambrechts D, Kroll J, Plaisance S, De Mol M, Bono F, Kliche S, Fellbrich G, Ballmer-Hofer K, Maglione D, Mayr-Beyrle U, Dewerchin M, Dombrowski S, Stanimirovic D, Van Hummelen P, Dehio C, Hicklin DJ, Persico G, Herbert JM, Communi D, Shibuya M, Collen D, Conway EM, Carmeliet P. 2003b. Role of PlGF in the intra- and inter-molecular cross talk between the VEGF receptors Flt1 and Flk1. Nat Med 9: 936-943.
4. Bae DG, Kim TD, Li G, Yoon WH, Chae CB. 2005. Anti-flt1 peptide, a vascular endothelial growth factor receptor 1-specific hexapeptide, inhibits tumor growth and metastasis. Clin Cancer Res 11: 2651-2661.
5. Bannerman P, Ara J, Hahn A, Hong L, Mc Cauley E, Friesen K, Pleasure D. 2008. Peripheral nerve regeneration is delayed in neuropilin 2-deficient mice. J Neurosci Res 86: 3163-3169.
6. 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: 9363-9376.
7. Beck H, Acker T, Puschel AW, Fujisawa H, Carmeliet P, Plate KH. 2002. Cell type-specific expression of neuropilins in an MCA-occlusion model in mice suggests a potential role in post-ischemic brain remodelling. J Neuropathol Exp Neurol 61: 339-350.
8. Bolin LM, Verity AN, Silver JE, Shooter EM, Abrams JS. 1995. Interleukin-6 production by Schwann cells and induction in sciatic nerve injury. J Neurochem 64: 850-858.
9. Borsani E, Albertini R, Labanca M, Lonati C, Rezzani R, Rodella LF. 2010. Peripheral purinergic receptor modulation influences the trigeminal ganglia nitroxodergic system in an experimental murine model of inflammatory orofacial pain. J Neurosci Res 88: 2715-2726.
10. Bottomley MJ, Webb NJ, Watson CJ, Holt L, Bukhari M, Denton J, Freemont AJ, Brenchley PE. 2000. Placenta growth factor (PlGF) induces vascular endothelial growth factor (VEGF) secretion from mononuclear cells and is co-expressed with VEGF in synovial fluid. Clin Exp Immunol 119: 182-188.
11. Bouquet C, Ravaille-Veron M, Propst F, Nothias F. 2007. MAP1B coordinates microtubule and actin filament remodeling in adult mouse Schwann cell tips and DRG neuron growth cones. Mol Cell Neurosci 36: 235-247.
12. Carmeliet P, Moons L, Luttun A, Vincneti V, Compernolle V, De Mol M, Wu Y, Bono F, Devy L, Beck H, Scholz D, Acker T, DiPalma T, Dewerchin M, Noel A, Stalmans I, Barra A, Blacher S, Vandendriessche T, Ponten A, Eriksson U, Plate KH, Foidart JM, Schaper W, Charnock-Jones DS, Hicklin DJ, Herbert JM, Collen D, Persico MG. 2001. Synergism between vascular endothelial growth factor and placental growth factor contributes to angogenesis and plasma extravasion in pathological conditions. Nat Med 7: 575-583.
13. Chattopadhyay S, Shubayev V. 2009. MMP-9 controls Schwann cell proliferation and phenotypic remodelling via IGF-1 and ErbB receptor-mediated activation of MEK/ERK pathway. GLIA 57: 1316-1325.
14. Chen Y, Li X, Tian L, Lui VC, Dallman MJ, Lamb JR, Tam PK. 2007. Inhibition of sonic hedgehog signaling reduces chronic rejection and prolongs allograft survival in a rat orthotopic small bowel transplantation model. Transplantation 83: 1351-1357.
15. Clauss M, Weich H, Breier G, Knies U, Röckl W, Waltenberger J, Risau W. 1996. The vascular growth factor receptor Flt-1 mediates biological activities: Implications for a functional role of placenta growth factor in monocyte activation and chemotaxis. J Biol Chem 27: 17629-17634.
16. Cramer M, Nagy I, Murphy BJ, Gassman M, Hottiger MO, Georgiev O, Schaffner W. 2005. NF-kB contributes to transcription of placental growth factor and interacts with metal responsive transcription factor-1 in hypoxic human cells. Biol Chem 386: 865-872.
17. D'Antonio M, Droggiti A, Feltri ML, Roes J, Wrabetz L, Mirsky R, Jessen KR. 2006. TGFbeta type II receptor signaling controls Schwann cell death and proliferation in developing nerves. J Neurosci 26: 8417-8427.
18. De Falco S, Gigante B, Persico MG. 2002. Structure and function of placental growth factor. Trends Cardiovasc Med 12: 241-246.
19. De Girolamo LA, Billett EE, Hargreaves AJ. 2000. Effects of 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine on differentiating mouse N2a neuroblastoma cells. J Neurochem 75: 133-140.
20. DiPalma T, Tucci M, Russo G, Maglione D, Lago CT, Romano A, Saccone S, Della Valle G, De Gregorio L, Dragani TA, Viglietto G, Persico MG. 1996. The placenta growth factor gene of the mouse. Mamm Genome 7: 6-12.
21. Dray C, Rougon G, Debarbieux F. 2009. Quantitative analysis by in vivo imaging of the dynamics of vascular and axonal networks in injured mouse spinal cord. Proc Natl Acad Sci USA 106: 9459-9464.
22. Failla CM, Odorisio T, Cianfarani F, Schietroma C, Puddu P, Zambruno G. 2000. Placenta growth factor is induced in human keratinocytes during wound healing. J Invest Dermatol 115: 388-395.
23. Fu ES, Zhang YP, Sagen J, Candiotti KA, Morton PD, Liebl DJ, Bethea JR, Brambilla R. 2010. Transgenic inhibition of glial NF-kappa B reduces pain behavior and inflammation after peripheral nerve injury. Pain 148: 509-518.
24. Funakoshi H, Frisén J, Barbany G, Timmusk T, Zachrisson O. 1993. Differential expression of mRNAs for neurotrophins and their receptors after axotomy of sciatic nerve. J Cell Biol 123: 455-465.
25. George LT, Myckatyn TM, Jensen JN, Hunter DA, Mackinnon SE. 2003. Functional recovery and histomorphometric assessment following tibial nerve injury in the mouse. J Reconstr Microsurg 19: 41-48.
26. Giraud SN, Caron CM, Pham-Dinh D, Kitabgi P, Nicot AB. 2010. Estradiol inhibits ongoing autoimmune neuroinflammation and NF{kappa}B-dependent CCL2 expression in reactive astrocytes. Proc Natl Acad Sci USA 107: 8416-8421.
27. Gould VE, Moll R, Moll I, Lee I, Schwechheimer K, Franke WW. 1986. The intermediate filament complement of the spectrum of nerve sheath neoplasms. Lab Invest 55: 463-474.
28. Green CJ, Lichtlen P, Huynh NT, Yanovsky M, Laderoute KR, Schaffner W, Murphy BJ. 2001. Placenta growth factor gene expression is induced by hypoxia in fibroblasts: A central role for metal transcription factor-1. Cancer Res 61: 2696-703.
29. Grove M, Plumb M. 1993. C/EBP, NF-kappa B, and c-Ets family members and transcriptional regulation of the cell-specific and inducible macrophage inflammatory protein 1 alpha immediate-early gene. Mol Cell Biol 13: 5276-5289.
30. Haddad O, Chotard-Ghodsnia R, Verdier C, Duperray A. 2010. Tumor cell/endothelial cell tight contact upregulates endothelial adhesion molecule expression mediated by NFkappaB: Differential role of the shear stress. Exp Cell Res. 316: 615-626.
31. Hattori K, Heissig B, Wu Y, Dias S, Tejada R, Ferris B, Hicklin DJ, Zhu Z, Bohlen P, Witte L, Hendrikx J, Hackett NR, Crystal RG, Moore MA, Werb Z, Lyden D, Rafii S. 2002. Placental growth factor reconstitutes hematopoiesis by recruiting VEGFR1(+) stem cells from bone marrow microenvironment. Nat Med 8: 841-849.
32. Hnia K, Gayraud J, Hugon G, Ramonatxo M, De La Porte S, Matecki S, Mornet D. 2008. L-arginine decreases inflammation and modulates the nuclear factor-kappaB/matrix metalloproteinase cascade in mdx muscle fibers. Am J Pathol 172: 1509-1519.
33. Hobson MI, Green CJ, Terenghi G. 2000. VEGF enhances intraneural angiogenesis and improves nerve regeneration after axotomy. J Anat 197: 591-605.
34. Höke A, Sun HS, Gordon T, Zochodne DW. 2001. Do denervated peripheral nerve trunks become ischemic? The impact of chronic denervation on vasa nervorum. Exp Neurol 172: 398-406.
35. Hollborn M, Tenckhoff S, Seifert M, Köhler S, Wiedemann P, Bringmann A, Kohen L. 2006. Human retinal epithelium produces and responds to placenta growth factor. Graefes Arch Clin Exp Ophthalmol 244: 732-741.
36. Krum JM, Mani N, Rosenstein JM. 2008. Roles of the endogenous VEGF receptors flt-1 and flk-1 in astroglial and vascular remodeling after brain injury. Exp Neurol 212: 108-117.
37. Kwon YK, Bhattacharyya A, Alberta JA, Giannobile WV, Cheon K, Stiles CD, Pomeroy SL. 1997. Activation of ErbB2 during Wallerian degeneration of sciatic nerve. J Neurosci 17: 8293-8299.
38. Lauffenburger DA, Horwitz, AF. 1996. Cell Migration: A physically integrated molecular process. Cell 84: 359-369.
39. Lawson LJ, Frost L, Risbridger J, Fearn, S, Perry VH. 1994. Quantification of the mononuclear phagocyte response to Wallerian degeneration of the optic nerve. J Neurocytol 23: 729-744.
40. Ledeboer A, Gamanos M, Lai W, Martin D, Maier SF, Watkins LR, Quan N. 2005. Involvement of spinal cord nuclear factor kappaB activation in rat models of proinflammatory cytokine-mediated pain facilitation. Eur J Neurosci 22: 1977-1986.
41. Leonardi A, Chariot A, Claudio E, Cunningham K, Siebenlist U. 2000. CIKS, a connection to Ikappa B kinase and stress-activated protein kinase. Proc Natl Acad Sci USA 97: 10494-10499.
42. Li X, Gonias SL, Campana WM. 2005. Schwann cells express erythropoietin receptor and represent a major target for Epo in peripheral nerve injury. GLIA 51: 254-265.
43. Li B, Sharpe EE, Maupin AB, Teleron AA, Pyle AL, Carmeliet P, Young PP. 2006. VEGF and PlGF promote adult vasculogenesis by enhancing EPC recruitment and vessel formation at the site of tumor neovascularization. FASEB J 20: 1495-1497.
44. Liu H, Honmou O, Harada K, Nakamura K, Houkin K, Hamada H, Kocsis JD. 2006. Neuroprotection by PlGF gene-modified human mesenchymal stem cells after cerebral ischaemia. Brain 129: 2734-2745.
45. Luttun A, Tjwa M, Moons L, Wu Y, Angelillo-Scherrer A, Liao F, Nagy JA, Hooper A, Priller J, De Klerck B, Compernolle V, Daci E, Bohlen P, Dewerchin M, Herbert JM, Fava R, Matthys P, Carmeliet G, Collen D, Dvorak HF, Hicklin DJ, Carmeliet P. 2002. Revascularization of ischemic tissues by PlGF treatment, and inhibition of tumor angiogenesis, arthritis and atherosclerosis by anti-Flt1. Nat Med 8: 831-840.
46. Maglione D, Guerriero V, Viglietto G, Delli Bovi P, Persico MG. 1991. Isolation of a human placenta cDNA coding for a protein related to the vascular permeability factor. Proc Natl Acad Sci USA 88: 9267-9271.
47. Mani N, Khaibullina A, Krum JM, Rosenstein JM. 2005. Astrocyte growth effects of vascular endothelial growth factor (VEGF) application to perinatal neocortical explants: Receptor mediation and signal transduction pathways. Exp Neurol 192: 394-406.
48. Mani N, Khaibullina A, Krum JM, Rosenstein JM. 2010. Vascular endothelial growth factor enhances migration of astroglial cells in subventricular zone neurosphere cultures. J Neurosci Res 88: 248-257.
49. Mantuano E, Inoue G, Li X, Takahashi K, Gaultier A, Gonias SL, Campana, WM. 2008. The hemopexin domain of matrix metalloproteinase-9 activates cell signaling and promotes migration of schwann cells by binding to low-density lipoprotein receptor-related protein. J Neurosci 28: 11571-11582.
50. Moynagh PN, Williams DC, O'Neill LA. 1994. Activation of NF-kappa B and induction of vascular cell adhesion molecule-1 and intracellular adhesion molecule-1 expression in human glial cells by IL-1. Modulation by antioxidants. J Immunol 153: 2681-2690.
51. Ogata T, Yamamoto S, Nakamura K, Tanaka, S. 2006. Signaling axis in schwann cell proliferation and differentiation. Mol Neurobiol 33: 51-62.
52. Perrin FE, Lacroix S, Avilès-Trigueros M, David S. 2005. Involvement of monocyte chemoattractant protein-1, macrophage inflammatory protein-1α and interleukin-1β in Wallerian degeneration. Brain 128: 854-66.
53. 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: 1218-1223.
54. Persico MG, Vincenti V, Di Palma T. 1999. Structure, expression and receptor-binding properties of placenta growth factor (PlGF). Curr Top Microbiol Immunol 237: 31-40.
55. Perelman N, Selvaraj SK, Batra S, Luck LR, Erdreich-Epstein A, Coates TD, Kalra VK, Malik P. 2003. Placenta growth factor activates monocytes and correlates with sickle cell disease severity. Blood 102: 1506-1514.
56. Rhee JW, Lee KW, Kim D, Lee Y, Jeon OH, Kwon HJ, Kim DS. 2007. NF-kappaB-dependent regulation of matrix metalloproteinase-9 gene expression by lipopolysaccharide in a macrophage cell line RAW 264.7. J Biochem Mol Biol 40: 88-94.
57. Ribatti D. 2008. The discovery of the placental growth factor and its role in angiogenesis: A historical review. Angiogenesis 11: 215-221.
58. Rogister B, Delrée P, Leprince P, Martin D, Sadzot C, Malgrange B, Munaut C, Rigo JM, Lefebvre PP, Octave J-N, Schoenen J, Moonen G. 1993. Transforming growth factor β as a neuronoglial signal during peripheral nervous system response to injury. J Neurosci Res 34: 32-43.
59. Runyan SA, Phelps PE. 2009. Mouse olfactory ensheathing glia enhance axon outgrowth on a myelin substrate in vitro. Exp Neurol 216: 95-104.
60. Scarlato M, Ara J, Bannerman P, Scherer S, Pleasure D. 2003. Induction of neuroplins-1 and -2 and their ligands, Sema3A, Sema3F, and VEGF, during Wallerian degeneration in the peripheral nervous system. Exp Neurol 183: 489-498.
61. Schratzberger P, Schratzberger G, Silver M, Curry C, Kearney M, Magner M, Alroy J, Adelman LS, Weinberg DH, Ropper AH, Isner JM. 2000. Favorable effect of VEGF gene transfer on ischemic peripheral neuropathy. Nat Med 6: 405-413.
62. Selvaraj SK, Giri RK, Perelman N, Johnson C, Malik P, Kalra VK. 2003. Mechanism of monocyte activation and expression of proinflammatory cytochemokines by placenta growth factor. Blood 102: 1515-1524.
63. Shamash S, Reichert F, Rotshenker S. 2002. The cytokine network of Wallerian degeneration: Tumor necrosis factor-α, interleukin-1α and interleukin-1β. J Neurosci 22: 3052-3060.
64. Siebert H, Sachse A, Kuziel WA, Maeda N, Brück W. 2000. The chemokine receptor CCR2 is involved in macrophage recruitment to the injured peripheral nervous system. J Neuroimmunol 110: 177-185.
65. Slobodov U, Reichert F, Mirski R, Rotshenker S. 2001. Distinct inflammatory stimuli induce different patterns of myelin phagocytosis and degradation in recruited macrophages. Exp Neurol 167: 401-409.
66. Springer T, Galfré G, Secher DS, Milstein C. 1979. Mac-1: A macrophage differentiation antigen identified by monoclonal antibody. Eur J Immunol 9: 301-306.
67. Stoll G, Griffin JW, Li CY, Trapp BD. 1989. Wallerian degeneration in the peripheral nervous system: Participation of both Schwann cells and macrophages in myelin degradation. J Neurocytol 18: 671-683.
68. Subang MC, Richardson PM. 2001. Influence of injury and cytokines on synthesis of monocyte chemoattractant protein-1 mRNA in peripheral nervous tissue. Eur J Neurosci 13: 521-528.
69. Takeda Y, Uemura S, Iwama H, Imagawa K, Nishida T, Onoue K, Takemoto Y, Soeda T, Okayama S, Somekawa S, Ishigami K, Takaoka M, Kawata H, Kubo A, Horii M, Nakajima T, Saito Y. 2009. Treatment with recombinant placental growth factor (PlGF) enhances both angiogenesis and arteriogenesis and improves survival after myocardial infarction. Circ J 73: 1674-1682.
70. Taskinen HS, Röyttä M. 2000. Increased expression of chemokines (MCP-1, MIP-1alpha, RANTES) after peripheral nerve transection. JPeripher Nerv Syst 5: 75-81.
71. Taniuchi M, Clark HB, Schweitzer JB, Johnson EM. 1988. Expression of Nerve growth factor receptors by Schwann cells of axotomized peripheral nerves: Ultrastructural location, suppression by axonal contact, and binding properties. J Neurosci 8: 664-681.
72. Taylor AP, Goldenberg DM. 2007. Role of placenta growth factor in malignancy and evidence that an antagonistic PlGF/Flt-1 peptide inhibits the growth and metastasis of human breast cancer xenografts. Mol Cancer Ther 6: 524-531;
73. Toews A, Barrett C, Morell P. 1998. Monocyte chemoattractant protein 1 is responsible for macrophage recruitment following injury to sciatic nerve. J Neurosci Res 53: 260-267.
74. Tofaris G, 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 process regulated by interleukin-6 and LIF. J Neurosci 22: 6696-6703.
75. Vallabhapurapu S, Karin M. 2009. Regulation and function of NF-kappaB transcription factors in the immune system. Annu Rev Immunol 27: 693-733.
76. Vargas ME, Barres BA. 2007. Why is Wallerian degeneration in the CNS so slow? Annu Rev Neurosci 30: 153-179.
77. Waller A. 1850. Experiments on the section of the glossopharyngeal and hypoglossal nerves of the frog, and observations of the alterations produced thereby in the structure of their primitive fibres. Philos Trans R Soc Lond 140: 423-429.
78. Yin X, Wright J, Wall T, Grammas P. 2010. Brain endothelial cells synthesize neurotoxic thrombin in Alzheimer's disease. Am J Pathol 176: 1600-1606.