The serine protease inhibitor SerpinA3N attenuates neuropathic pain by inhibiting T cell-derived leukocyte elastase

Nature Medicine

Volumn 21, Issue 5, 2015, Pages 518-523

  Vicuña, Lucas ^a   Strochlic, David E ^b   Latremoliere, Alban ^b,c   Bali, Kiran Kumar ^a   Simonetti, Manuela ^a   Husainie, Dewi ^a   Prokosch, Sandra ^d   Riva, Priscilla ^c   Griffin, Robert S ^e   Njoo, Christian ^a   Gehrig, Stefanie ^a   Mall, Marcus A ^a   Arnold, Bernd ^d   Devor, Marshall ^f   Woolf, Clifford J ^b,c   Liberles, Stephen D ^b   Costigan, Michael ^b,c   Kuner, Rohini ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^e HOSPITAL FOR SPECIAL SURGERY   (United States)

^f HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ACUTE PHASE PROTEIN; ENZYME INHIBITOR; LEUKOCYTE ELASTASE; SERINE PROTEINASE INHIBITOR; SERPINA3N PROTEIN, MOUSE; SERPINA3N PROTEIN, RAT;

ANIMAL; ANTAGONISTS AND INHIBITORS; CELL SEPARATION; CYTOLOGY; DEPENDOPARVOVIRUS; DNA MICROARRAY; FEMALE; GENETICS; HYPERALGESIA; IN SITU HYBRIDIZATION; MALE; METABOLISM; MOUSE; NERVE CELL; NEURALGIA; PAIN; PATHOPHYSIOLOGY; PHENOTYPE; POLYMERASE CHAIN REACTION; RAT; SPINAL GANGLION; T LYMPHOCYTE; TRANSGENIC MOUSE; UPREGULATION;

ACUTE-PHASE PROTEINS; ANIMALS; CELL SEPARATION; DEPENDOVIRUS; ENZYME INHIBITORS; FEMALE; GANGLIA, SPINAL; HYPERALGESIA; IN SITU HYBRIDIZATION; LEUKOCYTE ELASTASE; MALE; MICE; MICE, TRANSGENIC; NEURALGIA; NEURONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PAIN; PHENOTYPE; POLYMERASE CHAIN REACTION; RATS; SERPINS; T-LYMPHOCYTES; UP-REGULATION;

EID: 84929151078     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.3852     Document Type: Article

References (55)

1. Costigan, M. et al. Multiple chronic pain states are associated with a common amino acid-changing allele in KCNS1. Brain 133, 2519-2527 (2010).
2. Nissenbaum, J. et al. Susceptibility to chronic pain following nerve injury is genetically affected by CACNG2. Genome Res. 20, 1180-1190 (2010).
3. Sorge, R.E. et al. Genetically determined P2X7 receptor pore formation regulates variability in chronic pain sensitivity. Nat. Med. 18, 595-599 (2012).
4. Tegeder, I. et al. GTP cyclohydrolase and tetrahydrobiopterin regulate pain sensitivity and persistence. Nat. Med. 12, 1269-1277 (2006).
5. Persson, A.K. et al. Correlational analysis for identifying genes whose regulation contributes to chronic neuropathic pain. Mol. Pain 5, 7 (2009).
6. Devor, M. & Raber, P. Heritability of symptoms in an experimental model of neuropathic pain. Pain 42, 51-67 (1990).
7. Ziv-Sefer, S., Raber, P., Barbash, S. & Devor, M. Unity vs. diversity of neuropathic pain mechanisms: allodynia and hyperalgesia in rats selected for heritable predisposition to spontaneous pain. Pain 146, 148-157 (2009).
8. Seijffers, R., Mills, C.D. & Woolf, C.J. ATF3 increases the intrinsic growth state of DRG neurons to enhance peripheral nerve regeneration. J. Neurosci. 27, 7911-7920 (2007).
9. Horvath, A.J. et al. The murine orthologue of human antichymotrypsin: a structural paradigm for clade A3 serpins. J. Biol. Chem. 280, 43168-43178 (2005).
10. Sipione, S. et al. Identification of a novel human granzyme B inhibitor secreted by cultured sertoli cells. J. Immunol. 177, 5051-5058 (2006).
11. Gettins, P.G. Serpin structure, mechanism, and function. Chem. Rev. 102, 4751-4804 (2002).
12. Lee, W.L. & Downey, G.P. Leukocyte elastase: physiological functions and role in acute lung injury. Am. J. Respir. Crit. Care Med. 164, 896-904 (2001).
13. Pham, C.T. Neutrophil serine proteases: specific regulators of inflammation. Nat. Rev. Immunol. 6, 541-550 (2006).
14. García, P.S., Gulati, A. & Levy, J.H. The role of thrombin and protease-activated receptors in pain mechanisms. Thromb. Haemost. 103, 1145-1151 (2010).
15. Kawasaki, Y. et al. Distinct roles of matrix metalloproteases in the early- and late-phase development of neuropathic pain. Nat. Med. 14, 331-336 (2008).
16. Ferry, G. et al. Activation of MMP-9 by neutrophil elastase in an in vivo model of acute lung injury. FEBS Lett. 402, 111-115 (1997).
17. Jackson, P.L. et al. Human neutrophil elastase-mediated cleavage sites of MMP-9 and TIMP-1: implications to cystic fibrosis proteolytic dysfunction. Mol. Med. 16, 159-166 (2010).
18. Kawabata, K. et al. ONO-5046, a novel inhibitor of human neutrophil elastase. Biochem. Biophys. Res. Commun. 177, 814-820 (1991).
19. McMahon, S.B. & Malcangio, M. Current challenges in glia-pain biology. Neuron 64, 46-54 (2009).
20. Scholz, J. & Woolf, C.J. The neuropathic pain triad: neurons, immune cells and glia. Nat. Neurosci. 10, 1361-1368 (2007).
21. 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. 21, 599-616 (2007).
22. Kim, C.F. & Moalem-Taylor, G. Detailed characterization of neuro-immune responses following neuropathic injury in mice. Brain Res. 1405, 95-108 (2011).
23. Gehrig, S., Mall, M.A. & Schultz, C. Spatially resolved monitoring of neutrophil elastase activity with ratiometric fluorescent reporters. Angew. Chem. Int. Edn Engl. 51, 6258-6261 (2012).
24. Costigan, M. et al. T-cell infiltration and signaling in the adult dorsal spinal cord is a major contributor to neuropathic pain-like hypersensitivity. J. Neurosci. 29, 14415-14422 (2009).
25. Irving, J.A., Pike, R.N., Lesk, A.M. & Whisstock, J.C. Phylogeny of the serpin superfamily: implications of patterns of amino acid conservation for structure and function. Genome Res. 10, 1845-1864 (2000).
26. Irving, J.A. et al. Serpins in prokaryotes. Mol. Biol. Evol. 19, 1881-1890 (2002).
27. Alam, S.R., Newby, D.E. & Henriksen, P.A. Role of the endogenous elastase inhibitor, elafin, in cardiovascular injury: from epithelium to endothelium. Biochem. Pharmacol. 83, 695-704 (2012).
28. Reardon, C. et al. Thymic stromal lymphopoetin-induced expression of the endogenous inhibitory enzyme SLPI mediates recovery from colonic inflammation. Immunity 35, 223-235 (2011).
29. Belaaouaj, A. et al. Mice lacking neutrophil elastase reveal impaired host defense against Gram-negative bacterial sepsis. Nat. Med. 4, 615-618 (1998).
30. Griffin, R.S. et al. Complement induction in spinal cord microglia results in anaphylatoxin C5a-mediated pain hypersensitivity. J. Neurosci. 27, 8699-8708 (2007).
31. Bolstad, B.M., Irizarry, R.A., Astrand, M. & Speed, T.P. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19, 185-193 (2003).
32. Irizarry, R.A. et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249-264 (2003).
33. Gentleman, R.C. et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5, R80 (2004).
34. Díaz, E. et al. Molecular analysis of gene expression in the developing pontocerebellar projection system. Neuron 36, 417-434 (2002).
35. Decosterd, I. & Woolf, C.J. Spared nerve injury: an animal model of persistent peripheral neuropathic pain. Pain 87, 149-158 (2000).
36. Luo, C. et al. Presynaptically localized cyclic GMP-dependent protein kinase 1 is a key determinant of spinal synaptic potentiation and pain hypersensitivity. PLoS Biol. 10, e1001283 (2012).
37. Costigan, M. et al. Replicate high-density rat genome oligonucleotide microarrays reveal hundreds of regulated genes in the dorsal root ganglion after peripheral nerve injury. BMC Neurosci. 3, 16 (2002).
38. Blackshaw, S. & Snyder, S.H. Parapinopsin, a novel catfish opsin localized to the parapineal organ, defines a new gene family. J. Neurosci. 17, 8083-8092 (1997).
39. Montmayeur, J.P., Liberles, S.D., Matsunami, H. & Buck, L.B. A candidate taste receptor gene near a sweet taste locus. Nat. Neurosci. 4, 492-498 (2001).
40. Schaeper, U. et al. Distinct requirements for Gab1 in Met and EGF receptor signaling in vivo. Proc. Natl. Acad. Sci. USA 104, 15376-15381 (2007).
41. Lu, J. et al. Pain in experimental autoimmune encephalitis: a comparative study between different mouse models. J. Neuroinflammation 9, 233 (2012).
42. Basso, A.S. et al. Reversal of axonal loss and disability in a mouse model of progressive multiple sclerosis. J. Clin. Invest. 118, 1532-1543 (2008).
43. Kim, C.F. & Moalem-Taylor, G. Detailed characterization of neuro-immune responses following neuropathic injury in mice. Brain Res. 1405, 95-108 (2011).
44. Jiang, P. et al. hESC-derived Olig2+ progenitors generate a subtype of astroglia with protective effects against ischaemic brain injury. Nat. Commun. 4, 2196 (2013).
45. Gangadharan, V. et al. A novel biological role for the phospholipid lysophosphatidylinositol in nociceptive sensitization via activation of diverse G protein signalling pathways in sensory nerves in vivo. Pain 154, 2801-2812 (2013).
46. Xu, Q. et al. In vivo gene knockdown in rat dorsal root ganglia mediated by self-complementary adeno-associated virus serotype 5 following intrathecal delivery. PLoS ONE 7, e32581 (2012).
47. Wang, Z. et al. Differentiation of neuronal cells from NIH/3T3 fibroblasts under defined conditions. Dev. Growth Differ. 53, 357-365 (2011).
48. Hirota, Y. et al. Roles of planar cell polarity signaling in maturation of neuronal precursor cells in the postnatal mouse olfactory bulb. Stem Cells 30, 1726-1733 (2012).
49. Chiang, H.S. et al. GEF-H1 controls microtubule-dependent sensing of nucleic acids for antiviral host defenses. Nat. Immunol. 15, 63-71 (2014).
50. Allman, D., Li, J. & Hardy, R.R. Commitment to the B lymphoid lineage occurs before DH-JH recombination. J. Exp. Med. 189, 735-740 (1999).
51. Ko, S.Y. et al. alpha-Galactosylceramide can act as a nasal vaccine adjuvant inducing protective immune responses against viral infection and tumor. J. Immunol. 175, 3309-3317 (2005).
52. Charles, N., Hardwick, D., Daugas, E., Illei, G.G. & Rivera, J. Basophils and the T helper 2 environment can promote the development of lupus nephritis. Nat. Med. 16, 701-707 (2010).
53. Andoniou, C.E. et al. Interaction between conventional dendritic cells and natural killer cells is integral to the activation of effective antiviral immunity. Nat. Immunol. 6, 1011-1019 (2005).
54. Papatriantafyllou, M. et al. Dickkopf-3, an immune modulator in peripheral CD8 T-cell tolerance. Proc. Natl. Acad. Sci. USA 109, 1631-1636 (2012).
55. Gehrig, S., Mall, M.A. & Schultz, C. Spatially resolved monitoring of neutrophil elastase activity with ratiometric fluorescent reporters. Angew. Chem. Int. Edn Engl. 51, 6258-6261 (2012).