Schwann cell LRP1 regulates Remak bundle ultrastructure and axonal interactions to prevent neuropathic pain

Journal of Neuroscience

Volumn 33, Issue 13, 2013, Pages 5590-5602

  Orita, Sumihisa ^a,b   Henry, Kenneth ^a   Mantuano, Elisabetta ^a   Yamauchi, Kazuyo ^a,b   De Corato, Alice ^a,c   Ishikawa, Tetsuhiro ^a,b   Feltri, M Laura ^d   Wrabetz, Lawrence ^d   Gaultier, Alban ^a   Pollack, Melanie ^a   Ellisman, Mark ^a   Takahashi, Kazuhisa ^b   Gonias, Steven L ^a   Campana, W Marie ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CHIBA UNIVERSITY   (Japan)

^c CATHOLIC UNIVERSITY   (Italy)

^d UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN;

ALLODYNIA; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CRUSH TRAUMA; IMMUNOBLOTTING; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MICROGLIA; MOTOR PERFORMANCE; MOUSE; MYELINATION; NERVE DEGENERATION; NERVE FIBER; NERVE INJURY; NEUROPATHIC PAIN; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REMYELINIZATION; SCHWANN CELL; SCIATIC NERVE; SPINAL CORD; TRANSGENIC MOUSE; TRANSMISSION ELECTRON MICROSCOPY;

ACTINS; ANALYSIS OF VARIANCE; ANIMALS; ANTIGENS, CD11B; AXONS; CYTOPLASM; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; HYPERALGESIA; IN SITU NICK-END LABELING; INDOLES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, ELECTRON, TRANSMISSION; MOVEMENT DISORDERS; MYELIN BASIC PROTEIN; NERVE DEGENERATION; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PAIN MEASUREMENT; PHOSPHORYLATION; POSTERIOR HORN CELLS; RECEPTORS, LDL; S100 PROTEINS; SCHWANN CELLS; SCIATICA; SENSATION DISORDERS; SPINAL CORD; TUMOR SUPPRESSOR PROTEINS;

EID: 84875477283     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3342-12.2013     Document Type: Article

References (64)

1. Akassoglou K, Kombrinck KW, Degen JL, Strickland S (2000) Tissue plasminogen activator-mediated fibrinolysis protects against axonal degeneration and demyelination after sciatic nerve injury. J Cell Biol 149:1157-1166. CrossRef Medline
2. Azzouz M, Kenel PF, Warter JM, Poindron P, Borg J (1996) Enhnacement of mouse sciatic nerve regeneration by the long chain fatty alcohol, N-Hexacosanol. Exp Neurol 138:189-197. CrossRef Medline
3. Bolis A, Coviello S, Bussini S, Dina G, Pardini C, Previtali SC, Malaguti M, Morana P, Del Carro U, Feltri ML, Quattrini A, Wrabetz L, Bolino A (2005) Loss of Mtmr2 phosphatase in Schwann cells but not in motor neurons causes Cahrcot-Marie-Tooth type 4B1 neuropathy with myelin outfoldings. J Neurosci 25:8567-8577. CrossRef Medline
4. Bunge MB, Pearse DD (2003) Transplantation strategies to promote repair of the injured spinal cord. J Rehabil Res Dev 40:55-62. CrossRef Medline
5. Campana WM, Myers RR (2001) Erythropoietin and erythropoietin receptors in the peripheral nervous system: changes after nerve injury. FASEB J 15:1804-1806. Medline
6. Campana WM, Li X, Dragojlovic N, Janes J, Gaultier A, Gonias SL (2006a) The low-density lipoprotein receptor-related protein is a pro-survival receptor in Schwann cells: possible implications in peripheral nerve injury. J Neurosci 26:11197-11207. CrossRef Medline
7. Campana WM, Li X, Shubayev VI, Angert M, Cai K, Myers RR (2006b) Erythropoietin reduces Schwann cell TNF-alpha, Wallerian degeneration and pain-related behaviors after peripheral nerve injury. Eur J Neurosci 23:617-626. CrossRef Medline
8. Carter GT, Jensen MP, Galer BS, Kraft GH, Crabtree LD, Beardsley RM, Abresch RT, Bird TD (1998) Neuropathic pain in Charcot-Marie-Tooth disease. Arch Phys Med Rehabil 79:1560-1564. CrossRef Medline
9. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL (1994) Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53:55-63. CrossRef Medline
10. Chasman DI, Schurks M, Anttila V, de Vries B, Schminke U, Launer LJ, Terwindt GM, van den Maagdenberg AM, Fendrich K, Völzke H, Ernst F, Griffiths LR, Buring JE, Kallela M, Freilinger T, Kubisch C, Ridker PM, Palotie A, Ferrari MD, Hoffmann W, et al. (2011) Genome-wide association study reveals three susceptibility loci for common migraine in the general population. Nat Genet 43:695-698. CrossRef Medline
11. Chen S, Rio C, Ji RR, Dikkes P, Coggeshall RE, Woolf CJ, Corfas G (2003) Disruption of ErbB receptor signaling in adult non-myelinating Schwann cells causes progressive sensory loss. Nat Neurosci 6:1186-1193. CrossRef Medline
12. Chen ZL, Yu WM, Strickland S (2007) Peripheral regeneration. Annu Rev Neurosci 30:209-233. CrossRef Medline
13. Devor M, Govrin-Lippmann R, Angelides K (1993) Na+ channel immunolocalization in peripheral mammalian axons and changes following nerve injury and neuroma formation. J Neurosci 13:1976-1992. Medline
14. Dixon WJ (1980) Efficient analysis of experimental observations. Annu Rev Pharmacol Toxicol 20:441-462. CrossRef Medline
15. Feltri ML, D'Antonio M, Previtali S, Fasolini M, Messing A, Wrabetz L (1999) P0-Cre transgenic mice for inactivation of adhesion molecules in Schwann cells. Ann N Y Acad Sci 883:116-123. CrossRef Medline
16. Feltri ML, Graus Porta D, Previtali SC, Nodari A, Migliavacca B, Cassetti A, Littlewood-Evans A, Reichardt LF, Messing A, Quattrini A, Mueller U, Wrabetz L (2002) Conditional disruption of beta 1 integrin in Schwann cells impedes interactions with axons. J Cell Biol 156:199-209. CrossRef Medline
17. Fujita R, Kiguchi N, Ueda H (2007) LPA-mediated demyelination in ex vivo culture of dorsal root. Neurochem Internat 50:351-355. CrossRef
18. Gaultier A, Arandjelovic S, Li X, Janes J, Dragojlovic N, Zhou GP, Dolkas J, Myers RR, Gonias SL, Campana WM (2008) A shed form of LDL receptor-related protein-1 regulates peripheral nerve injury and neuropathic pain in rodents. J Clin Invest 118:161-172. CrossRef Medline
19. Goldberg DS, McGee SJ (2011) Pain as a global public health priority. BMC Public Health 11:770-775. CrossRef Medline
20. Gorovoy M, Gaultier A, Campana WM, Firestein GS, Gonias SL (2010) Inflammatory mediators promote production of shed LRP1/CD91, which regulates cell signaling and cytokine expression by macrophages. J Leukoc Biol 88:769-778. CrossRef Medline
21. Griffin JW, Thompson WJ (2008) Biology and pathology of nonmyelinating Schwann cells. Glia 56:1518-1531. CrossRef Medline
22. Grinspan JB, Marchionni MA, Reeves M, Coulaloglou M, Scherer SS (1996) Axonal interactions regulate Schwann cell apoptosis in developing peripheral nerve: neuregulin receptors and the role of neuregulins. J Neurosci 16:6107-6118. Medline
23. Hathway GJ, Vega-Avelaira D, Moss A, Ingram R, Fitzgerald M (2009) Brief, low frequency stimulation of rat peripheral C-fibres evokes prolonged microglial-induced central sensitization in adults but not in neonates. Pain 144:110-118. CrossRef Medline
24. Herz J, Clouthier DE, Hammer RE (1992) LDL receptor-related protein internalizes and degrades uPA-PAI-1 complexes and is essential for embryo implantation. Cell 71:411-421. CrossRef Medline
25. Ide C (1996) Peripheral nerve regeneration. Neurosci Res 25:101-121. CrossRef Medline
26. Jessen KR, Mirsky R (1999) Schwann cells and their precursors emerge as major regulators of nerve development. Trends Neurosci 22:402-410. CrossRef Medline
27. Jessen KR, Mirsky R (2005) The origin and development of glial cells in peripheral nerves. Nat Rev Neurosci 6:671-682. CrossRef Medline
28. Ji RR, Suter MR (2007) p38 MAPK, microglial signaling, and neuropathic pain. Mol Pain 3:33. CrossRef Medline
29. La Fleur M, Underwood JL, Rappolee DA, Werb Z (1996) Basement membrane and repair of injury to peripheral nerve: defining a potential role for macrophages, matrix metalloproteinases, and tissue inhibitor of metalloproteinases-1. J Exp Med 184:2311-2326. CrossRef Medline
30. Ledeboer A, Sloane EM, Milligan ED, Frank MG, Mahony JH, Maier SF, Watkins LR (2005) Minocycline attenuates mechanical allodynia and proinflammatory cytokine expression in rat models of pain facilitation. Pain 115:71-83. CrossRef Medline
31. Lillis AP, Van Duyn LB, Murphy-Ullrich JE, Strickland DK (2008) LDL receptor related protein 1: unique tissue specific functions revealed by selective gene knockout studies. Physiol Rev 88:887-918. CrossRef Medline
32. Liu Q, Zhang J, Tran H, Verbeek MM, Reiss K, Estus S, Bu G (2009) LRP1 shedding in human brain: roles of ADAM10 and ADAM17. Mol Neurodegener 4:17. CrossRef Medline
33. 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. CrossRef Medline
34. Mantuano E, Jo M, Gonias SL, Campana WM (2010) Low density lipoprotein receptor-related protein (LRP1) regulats Rac1 and RhoA recipricoally to control Schwann cell adhesion and migration. J Biol Chem 285: 14259-14266. CrossRef Medline
35. Mantuano E, Henry K, Yamauchi T, Hiramatsu N, Yamauchi K, Orita S, Takahashi K, Lin JH, Gonias SL, Campana WM (2011) The unfolded protein response is a major mechanism by which LRP1 regulates Schwann cell survival after injury. J Neurosci 31:13376-13385. CrossRef Medline
36. Meier C, Parmantier E, Brennan A, Mirsky R, Jessen KR (1999) Developing Schwann cells acquire the ability to survive without axons by establishing an autocrine circuit involving insulin-like growth factor, neurotrophin-3, and platelet-derived growth factor-BB. J Neurosci 19:3847-3859. Medline
37. Melendez-Vasquez CV, Einheber S, Salzer JL (2004) Rho kinase regulates schwann cell myelination and formation of associated axonal domains. J Neurosci 24:3953-3963. CrossRef Medline
38. 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 25:1179-1187. CrossRef Medline
39. Nachemson AK, Bennett GJ (1993) Does pain damage spinal cord neurons? Transsynaptic degeneration in rat following a surgical incision. Neurosci Lett 162:78-80. CrossRef Medline
40. Ohara S, Ikuta F (1988) Schwann cell resonses during regeneration after one or more crush injuries to myelinated nerve fibres. Neuropath Appl Neurobiol 14:229-245. CrossRef
41. Overton CD, Yancey PG, Major AS, Linton MF, Fazio S (2007) Deletion of macrophage LDL receptor-related protein increases atherogenesis in the mouse. Circ Res 100:670-677. CrossRef Medline
42. Pentland B, Donald SM (1994) Pain in the Guillain-Barre syndrome: a clinical review. Pain 59:159-164. CrossRef Medline
43. Raghavendra V, Tanga FY, DeLeo JA (2004) Attenuation of morphine tolerance, withdrawal-induced hyperalgesia, and associated spinal inflammatory immune responses by propentofylline in rats. Neuropsychopharmacology 29:327-334. CrossRef Medline
44. Rogawski MA, Löscher W (2004) The neurobiology of antiepileptic drugs for the treatment of nonepileptic conditions. Nat Med 10:685-692. CrossRef Medline
45. Rohlmann A, Gotthardt M, Willnow TE, Hammer RE, Herz J (1996) Sustained somatic gene inactivation by viral transfer of Cre recombinase. Nat Biotechnol 14:1562-1565. CrossRef Medline
46. Sadjadpour K (1975) Postfacial palsy phenomena: faulty nerve regeneration or ephaptic transmission? Brain Res 95:403-406. CrossRef Medline
47. Salicioni AM, Gaultier A, Brownlee C, Cheezum MK, Gonias SL (2004) Low density lipoprotein receptor-related protein-1 promotes beta1 integrin maturation and transport to the cell surface. J Biol Chem 279:10005-10012. Medline
48. Schäfers M, Lee DH, Brors D, Yaksh TL, Sorkin LS (2003) Increased sensitivity of injured and adjacent uninjured rat primary sensory neurons to exogenous tumor necrosis factor-alpha after spinal nerve ligation. J Neurosci 23:3028-3038. Medline
49. Seltzer Z, Dubner R, Shir Y (1990) A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury. Pain 43: 205-218. CrossRef Medline
50. Shi Y, Mantuano E, Inoue G, Campana WM, Gonias SL (2009) Ligand binding to LRP1 transactivates Trk receptors by a Src family kinase-dependent pathway. Sci Signal 2: ra18. Medline
51. Shir Y, Seltzer Z (1990) A-fibers mediate mechanical hyperesthesia and allodynia and C-fibers mediate thermal hyperalgesia in a new model of causalgiform pain disorders in rats. Neurosci Lett 115:62-67. CrossRef Medline
52. Strickland DK, Ashcom JD, Williams S, Burgess WH, Migliorini M, Argraves WS (1990) Sequence identity between the alpha 2-macroglobulin receptor and low density lipoprotein receptor-related protein suggests that this molecule is a multifunctional receptor. J Biol Chem 265:17401-17404. Medline
53. Strickland DK, Gonias SL, Argraves WS (2002) Diverse roles for the LDL receptor family. Trends Endocrinol Metab 13:66-74. CrossRef Medline
54. Svensson C, Medicherla S, Malkmus S, Jiang Y, Ma JY, Kerr I, Brainin-Mattos J, Powell HC, Luo ZD, Chakravarty S, Dugar S, Higgins LS, Protter AA, Yaksh TL (2008) Role of p38 mitogen activated protein kinase in a model of osteosarcoma-induced pain. Pharmacol Biochem Behav 90:664-675. Medline
55. Taveggia C, Salzer JL (2007) PARsing the events of myelination. Nat Neurosci 10:17-18. CrossRef Medline
56. Thomas PK (1970) The cellular responses to nerve injury. J Anat 106:463-470. Medline
57. Ueda H (2006) Molecular mechanisms of neuropathic pain-phenotypic switch and initiation mechanisms. Pharmacol Ther 109:57-77. CrossRef Medline
58. Ueda H (2008) Peripheral mechanisms of neuropathic paininvolvement of lysophosphatidic acid receptor-mediated demyelination. Mol Pain 4:11. CrossRef Medline
59. Ueda H (2011) Lysophosphadic acid as the initiator of neuropathic pain. Biol Pharm Bull 34:1154-1158. CrossRef Medline
60. Ulmann L, Hatcher JP, Hughes JP, Chaumont S, Green PJ, Conquet F, Buell GN, Reeve AJ, Chessell IP, Rassendren F (2008) Up-regulation of P2X4 receptors in spinal microglia after peripheral nerve injury mediates BDNF release and neuropathic pain. J Neurosci 28:11263-11268. CrossRef Medline
61. Witt A, Brady ST (2000) Unwrapping new layers of complexity in axon/glial relationships. Glia 29:112-117. CrossRef Medline
62. Wu G, Ringkamp M, Murinson BB, Pogatzki EM, Hartke TV, Weerahandi HM, Campbell JN, Griffin JW, Meyer RA (2002) Degeneration of myelinated efferent fibers induces spontaneous activity in uninjured C-fiber afferents. J Neurosci 22:7746-7753. Medline
63. Yu WM, Yu H, Chen ZL (2007) Laminins in peripheral nerve development and muscular dystrophy. Mol Neurobiol 35:288-297. CrossRef Medline
64. Zhang H, Nei H, Dougherty PM (2010) A p38 mitogen-activated protein kinase-dependent mechanism of disinhibition in spinal synaptic transmission induced by tumor necrosis factor-alpha. J Neurosci 30:12844-12855. CrossRef Medline