p75 neurotrophin receptor regulates tissue fibrosis through inhibition of plasminogen activation via a PDE4/cAMP/PKA pathway

Journal of Cell Biology

Volumn 177, Issue 6, 2007, Pages 1119-1132

  Sachs, Benjamin D ^a   Baillie, George S ^b   McCall, Julianne R ^a   Passino, Melissa A ^a   Schachtrup, Christian ^a   Wallace, Derek A ^b   Dunlop, Allan J ^b   MacKenzie, Kirsty F ^b   Klussmann, Enno ^c   Lynch, Martin J ^b   Sikorski, Shoana L ^a   Nuriel, Tal ^a,d,e   Tsigelny, Igor ^a   Zhang, Jin ^a,f   Houslay, Miles D ^b   Chao, Moses V ^d   Akassoglou, Katerina ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

^d NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e WEILL CORNELL MEDICAL COLLEGE   (United States)

^f JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; NEUROTROPHIN RECEPTOR; P75 NEUROTROPHIN RECEPTOR; PHOSPHODIESTERASE IV; PHOSPHODIESTERASE V; PLASMINOGEN ACTIVATOR INHIBITOR; PLASMINOGEN ACTIVATOR INHIBITOR 1; SERINE PROTEINASE; TISSUE PLASMINOGEN ACTIVATOR; TUMOR NECROSIS FACTOR RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; FIBRINOLYSIS; FIBROSIS; HUMAN; HUMAN CELL; IN VIVO STUDY; LUNG FIBROSIS; MOUSE; NONHUMAN; PATHOGENESIS; PERIPHERAL NERVE INJURY; PLASMINOGEN ACTIVATION; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN DEGRADATION; PROTEIN FAMILY; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SCAR FORMATION; SCIATIC NERVE; UPREGULATION;

3',5'-CYCLIC-NUCLEOTIDE PHOSPHODIESTERASE; ANIMALS; CICATRIX; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; FIBRINOLYSIS; FIBROSIS; GENE EXPRESSION REGULATION; MICE; MICE, KNOCKOUT; PLASMINOGEN ACTIVATOR INHIBITOR 1; RECEPTOR, NERVE GROWTH FACTOR; SCIATIC NERVE; TISSUE PLASMINOGEN ACTIVATOR; WOUNDS AND INJURIES;

MUS;

EID: 34250732324     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200701040     Document Type: Article

References (73)

1. Adams, R.A., M. Passino, B.D. Sachs, T. Nuriel, and K. Akassoglou. 2004. Fibrin mechanisms and functions in nervous system pathology. Mol. Interv. 4:163-176.
2. Akassoglou, K., K.W. Kombrinck, J.L. Degen, and S. Strickland. 2000. Tissue plasminogen activator-mediated fibrinolysis protects against axonal degeneration and demyelination after sciatic nerve injury. J. Cell Biol. 149:1157-1166.
3. Akassoglou, K., W.-M. Yu, P. Akpinar, and S. Strickland. 2002. Fibrin inhibits peripheral nerve regeneration by arresting Schwann cell differentiation. Neuron. 33:861-875.
4. Allen, M.D., and J. Zhang. 2006. Subcellular dynamics of protein kinase A activity visualized by FRET-based reporters. Biochem. Biophys. Res. Commun. 348:716-721.
5. Barber, R., G.S. Baillie, R. Bergmann, M.C. Shepherd, R. Sepper, M.D. Houslay, and G.V. Heeke. 2004. Differential expression of PDE4 cAMP phosphodiesterase isoforms in inflammatory cells of smokers with COPD, smokers without COPD, and nonsmokers. Am. J. Physiol. Lung Cell. Mol. Physiol. 287:L332-L343.
6. Baron, P., E. Scarpini, S. Pizzul, F. Zotti, G. Conti, D. Pleasure, and G. Scarlato. 1997. Immunocytochemical expression of human muscle cell p75 neurotrophin receptor is down-regulated by cyclic adenosine 3′,5′- monophosphate. Neurosci. Lett. 234:79-82.
7. Beattie, M.S., A.W. Harrington, R. Lee, J.Y. Kim, S.L. Boyce, F.M. Longo, J.C. Bresnahan, B.L. Hempstead, and S.O. Yoon. 2002. ProNGF induces p75-mediated death of oligodendrocytes following spinal cord injury. Neuron. 36:375-386.
8. Beavo, J.A., and D.H. Reifsnyder. 1990. Primary sequence of cyclic nucleotide phosphodiesterase isozymes and the design of selective inhibitors. Trends Pharmacol. Sci. 11:150-155.
9. Bolger, G.B., G.S. Baillie, X. Li, M.J. Lynch, P. Herzyk, A. Mohamed, L.H. Mitchell, A. McCahill, C. Hundsrucker, E. Klussmann, et al. 2006. Scanning peptide array analyses identify overlapping binding sites for the signalling scaffold proteins, beta-arrestin and RACK1, in cAMP-specific phosphodiesterase PDE4D5. Biochem. J. 398:23-36.
10. Brunton, L.L. 2003. PDE4: arrested at the border. Sci. STKE. 2003:PE44.
11. Bugge, T.H., K.W. Kombrinck, M.J. Flick, C.C. Daugherty, M.J. Danton, and J.L. Degen. 1996. Loss of fibrinogen rescues mice from the pleiotropic effects of plasminogen deficiency. Cell. 87:709-719.
12. Carmeliet, P., L. Schoonjans, L. Kieckens, B. Ream, J. Degen, R. Bronson, R. De Vos, J.J. van den Oord, D. Collen, and R.C. Mulligan. 1994. Physiological consequences of loss of plasminogen activator gene function in mice. Nature. 368:419-424.
13. Chao, M.V. 2003. Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat. Rev. Neurosci. 4:299-309.
14. Chen, D., K. Giannopoulos, P.G. Shiels, Z. Webster, J.H. McVey, G. Kemball-Cook, E. Tuddenham, M. Moore, R. Lechler, and A. Dorling. 2004. Inhibition of intravascular thrombosis in murine endotoxemia by targeted expression of hirudin and tissue factor pathway inhibitor analogs to activated endothelium. Blood. 104:1344-1349.
15. Cherry, J.A., and R.L. Davis. 1999. Cyclic AMP phosphodiesterases are localized in regions of the mouse brain associated with reinforcement, movement, and affect. J. Comp. Neurol. 407:287-301.
16. Cosgaya, J.M., J.R. Chan, and E.M. Shooter. 2002. The neurotrophin receptor p75NTR as a positive modulator of myelination. Science. 298:1245-1248.
17. Degen, J.L., A.F. Drew, J.S. Palumbo, K.W. Kombrinck, J.A. Bezerra, M.J. Danton, K. Holmback, and T.T. Suh. 2001. Genetic manipulation of fibrinogen and fibrinolysis in mice. Ann. N. Y. Acad. Sci. 936:276-290.
18. Dowling, P., X. Ming, S. Raval, W. Husar, P. Casaccia-Bonnefil, M. Chao, S. Cook, and B. Blumberg. 1999. Up-regulated p75NTR neurotrophin receptor on glial cells in MS plaques. Neurology. 53:1676-1682.
19. Filbin, M.T. 2003. Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat. Rev. Neurosci. 4:703-713.
20. Fiumelli, H., D. Jabaudon, P.J. Magistretti, and J.-L. Martin. 1999. BDNF stimulates expression, activity and release of tissue-type plasminogen activator in mouse cortical neurons. Eur. J. Neurosci. 11:1639-1646.
21. Frank, R. 2002. The SPOT-synthesis technique. Synthetic peptide arrays on membrane supports-principles and applications. J. Immunol. Methods. 267:13-26.
22. Gao, Y., E. Nikulina, W. Mellado, and M.T. Filbin. 2003. Neurotrophins elevate cAMP to reach a threshold required to overcome inhibition by MAG through extracellular signal-regulated kinase-dependent inhibition of phosphodiesterase. J. Neurosci. 23:11770-11777.
23. Gretarsdottir, S., G. Thorleifsson, S.T. Reynisdottir, A. Manolescu, S. Jonsdottir, T. Jonsdottir, T. Gudmundsdottir, S.M. Bjarnadottir, O.B. Einarsson, H.M. Gudjonsdottir, et al. 2003. The gene encoding phosphodiesterase 4D confers risk of ischemic stroke. Nat. Genet. 35:131-138.
24. Herrmann, J.L., D.G. Menter, J. Hamada, D. Marchetti, M. Nakajima, and G.L. Nicolson. 1993. Mediation of NGF-stimulated extracellular matrix invasion by the human melanoma low-affinity p75 neurotrophin receptor: melanoma p75 functions independently of trkA. Mol. Biol. Cell. 4:1205-1216.
25. Higuchi, H., T. Yamashita, H. Yoshikawa, and M. Tohyama. 2003. PKA phosphorylates the p75 receptor and regulates its localization to lipid rafts. EMBO J. 22:1790-1800.
26. Houslay, M.D., and D.R. Adams. 2003. PDE4 cAMP phosphodiesterases: modular enzymes that orchestrate signalling cross-talk, desensitization and compartmentalization. Biochem. J. 370:1-18.
27. Houslay, M.D., P. Schafer, and K.Y. Zhang. 2005. Keynote review: phosphodiesterase-4 as a therapeutic target. Drug Discov. Today. 10:1503-1519.
28. Hsu, K.C., and M.V. Chao. 1993. Differential expression and ligand binding properties of tumor necrosis factor receptor chimeric mutants. J. Biol. Chem. 268:16430-16436.
29. Idell, S. 2003. Coagulation, fibrinolysis, and fibrin deposition in acute lung injury. Crit. Care Med. 31:S213-S220.
30. Kawasaki, T., M. Dewerchin, H.R. Lijnen, I. Vreys, J. Vermylen, and M.F. Hoylaerts. 2001. Mouse carotid artery ligation induces platelet-leukocyte- dependent luminal fibrin, required for neointima development. Circ. Res. 88:159-166.
31. Khursigara, G., J.R. Orlinick, and M.V. Chao. 1999. Association of the p75 neurotrophin receptor with TRAF6. J. Biol. Chem. 274:2597-2600.
32. Khursigara, G., J. Bertin, H. Yano, H. Moffett, P.S. DiStefano, and M.V. Chao. 2001. A prosurvival function for the p75 receptor death domain mediated via the caspase recruitment domain receptor-interacting protein 2. J. Neurosci. 21:5854-5863.
33. Kraemer, R. 2002. Reduced apoptosis and increased lesion development in the flow-restricted carotid artery of p75(NTR)-null mutant mice. Circ. Res. 91:494-500.
34. Lansink, M., P. Koolwijk, V. van Hinsbergh, and T. Kooistra. 1998. Effect of steroid hormones and retinoids on the formation of capillary-like tubular structures of human microvascular endothelial cells in fibrin matrices is related to urokinase expression. Blood. 92:927-938.
35. Lee, K.F., E. Li, L.J. Huber, S.C. Landis, A.H. Sharpe, M.V. Chao, and R. Jaenisch. 1992. Targeted mutation of the gene encoding the low affinity NGF receptor p75 leads to deficits in the peripheral sensory nervous system. Cell. 69:737-749.
36. Lee, R., P. Kermani, K.K. Teng, and B.L. Hempstead. 2001. Regulation of cell survival by secreted proneurotrophins. Science. 294:1945-1948.
37. Lehnart, S.E., X.H. Wehrens, S. Reiken, S. Warrier, A.E. Belevych, R.D. Harvey, W. Richter, S.L. Jin, M. Conti, and A.R. Marks. 2005. Phosphodiesterase 4D deficiency in the ryanodine-receptor complex promotes heart failure and arrhythmias. Cell. 123:25-35.
38. Lemke, G., and M. Chao. 1988. Axons regulate Schwann cell expression of the major myelin and NGF receptor genes. Development. 102:499-504.
39. Lijnen, H.R. 2001. Elements of the fibrinolytic system. Ann. N. Y. Acad. Sci. 936:226-236.
40. Ling, Q., A.T. Jacovina, A. Deora, M. Febbraio, R. Simantov, R.L. Silverstein, B. Hempstead, W.H. Mark, and K.A. Hajjar. 2004. Annexin II regulates fibrin homeostasis and neoangiogenesis in vivo. J. Clin. Invest. 113:38-48.
41. Livak, K.J., and T.D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 25:402-408.
42. Lomen-Hoerth, C., and E.M. Shooter. 1995. Widespread neurotrophin receptor expression in the immune system and other nonneuronal rat tissues. J. Neurochem. 64:1780-1789.
43. McPhee, I., S.J. Yarwood, G. Scotland, E. Huston, M.B. Beard, A.H. Ross, E.S. Houslay, and M.D. Houslay. 1999. Association with the SRC family tyrosyl kinase LYN triggers a conformational change in the catalytic region of human cAMP-specific phosphodiesterase HSPDE4A4B. Consequences for rolipram inhibition. J. Biol. Chem. 274:11796-11810.
44. Medcalf, R.L., M. Ruegg, and W.D. Schleuning. 1990. A DNA motif related to the cAMP-responsive element and an exon-located activator protein-2 binding site in the human tissue-type plasminogen activator gene promoter cooperate in basal expression and convey activation by phorbol ester and cAMP. J. Biol. Chem. 265:14618-14626.
45. Millar, J.K., B.S. Pickard, S. Mackie, R. James, S. Christie, S.R. Buchanan, M.P. Malloy, J.E. Chubb, E. Huston, G.S. Baillie, et al. 2005. DISC1 and PDE4B are interacting genetic factors in schizophrenia that regulate cAMP signaling. Science. 310:1187-1191.
46. Miotla, J.M., M.M. Teixeira, and P.G. Hellewell. 1998. Suppression of acute lung injury in mice by an inhibitor of phosphodiesterase type 4. Am. J. Respir. Cell Mol. Biol. 18:411-420.
47. Nikulina, E., J.L. Tidwell, H.N. Dai, B.S. Bregman, and M.T. Filbin. 2004. The phosphodiesterase inhibitor rolipram delivered after a spinal cord lesion promotes axonal regeneration and functional recovery. Proc. Natl. Acad. Sci. USA. 101:8786-8790.
48. O'Connell, J.C., J.F. McCallum, I. McPhee, J. Wakefield, E.S. Houslay, W. Wishart, G. Bolger, M. Frame, and M.D. Houslay. 1996. The SH3 domain of Src tyrosyl protein kinase interacts with the N-terminal splice region of the PDE4A cAMP-specific phosphodiesterase RPDE-6 (RNPDE4A5). Biochem. J. 318(Pt 1):255-261.
49. Park, J.A., J.Y. Lee, T.A. Sato, and J.Y. Koh. 2000. Co-induction of p75NTR and p75NTR-associated death executor in neurons after zinc exposure in cortical culture or transient ischemia in the rat. J. Neurosci. 20:9096-9103.
50. Passino, M.A., R.A. Adams, S.L. Sikorski, and K. Akassoglou. 2007. Regulation of hepatic stellate cell differentiation by the neurotrophin receptor p75NTR. Science. 315:1853-1856.
51. Perry, S.J., G.S. Baillie, T.A. Kohout, I. McPhee, M.M. Magiera, K.L. Ang, W.E. Miller, A.J. McLean, M. Conti, M.D. Houslay, and R.J. Lefkowitz. 2002. Targeting of cyclic AMP degradation to beta 2-adrenergic receptors by beta-arrestins. Science. 298:834-836.
52. Qian, Z., M.E. Gilbert, M.A. Colicos, E.R. Kandel, and D. Kuhl. 1993. Tissue-plasminogen activator is induced as an immediate-early gene during seizure, kindling and long-term potentiation. Nature. 361:453-457.
53. Rabizadeh, S., J. Oh, L.T. Zhong, J. Yang, C.M. Bitler, L.L. Butcher, and D.E. Bredesen. 1993. Induction of apoptosis by the low-affinity NGF receptor. Science. 261:345-348.
54. Reichardt, L.F. 2006. Neurotrophin-regulated signalling pathways. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361:1545-1564.
55. Renz, H., S. Kerzel, and W.A. Nockher. 2004. The role of neurotrophins in bronchial asthma: contribution of the pan-neurotrophin receptor p75. Prog. Brain Res. 146:325-333.
56. Ricci, A., L. Felici, S. Mariotta, F. Mannino, G. Schmid, C. Terzano, G. Cardillo, F. Amenta, and E. Bronzetti. 2004. Neurotrophin and neurotrophin receptor protein expression in the human lung. Am. J. Respir. Cell Mol. Biol. 30:12-19.
57. Roux, P.P., A.L. Bhakar, T.E. Kennedy, and P.A. Barker. 2001. The p75 neurotrophin receptor activates Akt (protein kinase B) through a phosphatidylinositol 3-kinase-dependent pathway. J. Biol. Chem. 276:23097-23104.
58. Samson, A.L., and R.L. Medcalf. 2006. Tissue-type plasminogen activator: a multifaceted modulator of neurotransmission and synaptic plasticity. Neuron. 50:673-678.
59. Santell, L., and E. Levin. 1988. Cyclic AMP potentiates phorbol ester stimulation of tissue plasminogen activator release and inhibits secretion of plasminogen activator inhibitor-1 from human endothelial cells. J. Biol. Chem. 263:16802-16808.
60. Savov, J.D., D.M. Brass, K.G. Berman, E. McElvania, and D.A. Schwartz. 2003. Fibrinolysis in LPS-induced chronic airway disease. Am. J. Physiol. Lung Cell. Mol. Physiol. 285:L940-L948.
61. Siconolfi, L.B., and N.W. Seeds. 2001. Mice lacking tPA, uPA, or plasminogen genes showed delayed functional recovery after sciatic nerve crush. J. Neurosci. 21:4348-4355.
62. Song, X.Y., F.H. Zhou, J.H. Zhong, L.L. Wu, and X.F. Zhou. 2006. Knockout of p75(NTR) impairs re-myelination of injured sciatic nerve in mice. J. Neurochem. 96:833-842.
63. Syroid, D.E., P.J. Maycox, M. Soilu-Hanninen, S. Petratos, T. Bucci, P. Burrola, S. Murray, S. Cheema, K.F. Lee, G. Lemke, and T.J. Kilpatrick. 2000. Induction of postnatal Schwann cell death by the low-affinity neurotrophin receptor in vitro and after axotomy. J. Neurosci. 20:5741-5747.
64. Taniuchi, M., H.B. Clark, and E.M. Johnson Jr. 1986. Induction of nerve growth factor receptor in Schwann cells after axotomy. Proc. Natl. Acad. Sci. USA. 83:4094-4098.
65. Teng, K.K., and B.L. Hempstead. 2004. Neurotrophins and their receptors: signaling trios in complex biological systems. Cell. Mol. Life Sci. 61:35-48.
66. Walikonis, R.S., and J.F. Poduslo. 1998. Activity of cyclic AMP phosphodiesterases and adenylyl cyclase in peripheral nerve after crush and permanent transection injuries. J. Biol. Chem. 273:9070-9077.
67. Wang, S., P. Bray, T. McCaffrey, K. March, B.L. Hempstead, and R. Kraemer. 2000. p75(NTR) mediates neurotrophin-induced apoptosis of vascular smooth muscle cells. Am. J. Pathol. 157:1247-1258.
68. Yamamoto, K., and D.J. Loskutoff. 1996. Fibrin deposition in tissues from endotoxin-treated mice correlates with decreases in the expression of urokinase-type but not tissue-type plasminogen activator. J. Clin. Invest. 97:2440-2451.
69. Yamashita, T., and M. Tohyama. 2003. The p75 receptor acts as a displacement factor that releases Rho from Rho-GDI. Nat. Neurosci. 6:461-467.
70. Yamashita, T., K.L. Tucker, and Y.A. Barde. 1999. Neurotrophin binding to the p75 receptor modulates Rho activity and axonal outgrowth. Neuron. 24:585-593.
71. Yarwood, S.J., M.R. Steele, G. Scotland, M.D. Houslay, and G.B. Bolger. 1999. The RACK1 signaling scaffold protein selectively interacts with the cAMP-specific phosphodiesterase PDE4D5 isoform. J. Biol. Chem. 274:14909-14917.
72. Zhang, J., C.J. Hupfeld, S.S. Taylor, J.M. Olefsky, and R.Y. Tsien. 2005. Insulin disrupts beta-adrenergic signalling to protein kinase A in adipocytes. Nature. 437:569-573.
73. Zorick, T.S., and G. Lemke. 1996. Schwann cell differentiation. Curr. Opin. Cell Biol. 8:870-876.