The BMP coreceptor RGMb promotes while the endogenous BMP antagonist noggin reduces neurite outgrowth and peripheral nerve regeneration by modulating BMP signaling

Journal of Neuroscience

Volumn 31, Issue 50, 2011, Pages 18391-18400

  Ma, Chi H E ^a,f   Brenner, Gary J ^b   Omura, Takao ^a   Samad, Omar A ^c   Costigan, Michael ^a   Inquimbert, Perrine ^a   Niederkofler, Vera ^d   Salie, Rishard ^d   Sun, Chia Chi ^b   Lin, Herbert Y ^b   Arber, Silvia ^c   Coppola, Giovanni ^e   Woolf, Clifford J ^a   Samad, Tarek A ^g  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF BASEL   (Switzerland)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f CITY UNIVERSITY OF HONG KONG   (Hong Kong)

^g PFIZER INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN RECEPTOR; MEMBRANE PROTEIN; NOGGIN; REPULSIVE GUIDANCE MOLECULE B; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXPLANT; FEMALE; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; KNOCKOUT MOUSE; MALE; MOUSE; NERVE FIBER GROWTH; NERVE INJURY; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; SCIATIC NERVE; SIGNAL TRANSDUCTION; SPINAL GANGLION; WESTERN BLOTTING;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CARRIER PROTEINS; CELLS, CULTURED; GANGLIA, SPINAL; MICE; MICE, KNOCKOUT; NERVE CRUSH; NERVE REGENERATION; NERVE TISSUE PROTEINS; NEURITES; NEURONS; PHOSPHORYLATION; SCIATIC NERVE; SIGNAL TRANSDUCTION;

EID: 83455199106     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4550-11.2011     Document Type: Article

References (48)

1. Abdel Samad O, Liu Y, Yang FC, Kramer I, Arber S, Ma Q (2010) Characterization of two Runx1-dependent nociceptor differentiation programs necessary for inflammatory versus neuropathic pain. Mol Pain 6:45.
2. Ai X, Cappuzzello J, Hall AK (1999) Activin and bone morphogenetic proteins induce calcitonin gene-related peptide in embryonic sensory neurons in vitro. Mol Cell Neurosci 14:506-518
3. Babitt JL, Huang FW, Wrighting DM, Xia Y, Sidis Y, Samad TA, Campagna JA, Chung RT, Schneyer AL, Woolf CJ, Andrews NC, Lin HY (2006) Bone morphogenetic protein signaling by hemojuvelin regulates hepcidin expression. Nat Genet 38:531-539
4. Balemans W, Van Hul W (2002) Extracellular regulation of BMP signaling in vertebrates: a cocktail of modulators. Dev Biol 250:231-250
5. Benn SC, Perrelet D, Kato AC, Scholz J, Decosterd I, Mannion RJ, Bakowska JC, Woolf CJ (2002) Hsp27 upregulation and phosphorylation is required for injured sensory and motor neuron survival. Neuron 36:45-56
6. Blackshaw S, Snyder SH (1997) Parapinopsin, a novel catfish opsin localized to the parapineal organ, defines a new gene family. J Neurosci 17:8083-8092
7. Brenner GJ, Ji RR, Shaffer S, Woolf CJ (2004) Peripheral noxious stimulation induces phosphorylation of the NMDA receptor NR1 subunit at the PKC-dependent site, serine-896, in spinal cord dorsal horn neurons. Eur J Neurosci 20:375-384
8. Conrad S, Genth H, Hofmann F, Just I, Skutella T (2007) Neogenin-RGMa signaling at the growth cone is bone morphogenetic protein-independent and involves RhoA, ROCK, and PKC. J Biol Chem 282:16423-16433
9. Conrad S, Stimpfle F, Montazeri S, Oldekamp J, Seid K, Alvarez-Bolado G, Skutella T (2010) RGMb controls aggregation and migration of Neogeninpositive cells in vitro and in vivo. Mol Cell Neurosci 43:222-231
10. Court FA, Sherman DL, Pratt T, Garry EM, Ribchester RR, Cottrell DF, Fleetwood-Walker SM, Brophy PJ (2004) Restricted growth of Schwann cells lacking Cajal bands slows conduction in myelinated nerves. Nature 431:191-195
11. Hata K, Fujitani M, Yasuda Y, Doya H, Saito T, Yamagishi S, Mueller BK, Yamashita T (2006) RGMa inhibition promotes axonal growth and recovery after spinal cord injury. J Cell Biol 173:47-58
12. Hocking JC, Hehr CL, Bertolesi G, Funakoshi H, Nakamura T, McFarlane S (2009) LIMK1 acts downstream of BMP signaling in developing retinal ganglion cell axons but not dendrites. Dev Biol 330:273-285
13. Hodge LK, Klassen MP, Han BX, Yiu G, Hurrell J, Howell A, Rousseau G, Lemaigre F, Tessier-Lavigne M, Wang F (2007) Retrograde BMP signaling regulates trigeminal sensory neuron identities and the formation of precise face maps. Neuron 55:572-586
14. Koeberle PD, Tura A, Tassew NG, Schlichter LC, Monnier PP (2010) The repulsive guidance molecule, RGMa, promotes retinal ganglion cell survival in vitro and in vivo. Neuroscience 169:495-504
15. Lewis SE, Mannion RJ, White FA, Coggeshall RE, Beggs S, Costigan M, Martin JL, Dillmann WH, Woolf CJ (1999) A role for HSP27 in sensory neuron survival. J Neurosci 19:8945-8953
16. Liu A, Niswander LA (2005) Bone morphogenetic protein signalling and vertebrate nervous system development. Nat Rev Neurosci 6:945-954
17. Liu X, Hashimoto M, Horii H, Yamaguchi A, Naito K, Yamashita T (2009) Repulsive guidance molecule b inhibits neurite growth and is increased after spinal cord injury. Biochem Biophys Res Commun 382:795-800
18. Ma CH, Omura T, Cobos EJ, Latrémolière A, Ghasemlou N, Brenner GJ, van Veen E, Barrett L, Sawada T, Gao F, Coppola G, Gertler F, Costigan M, Geschwind D, Woolf CJ (2011) Accelerating axonal growth promotes motor recovery after peripheral nerve injury in mice. J Clin Invest 121:4332-4347
19. Ma Q, Sommer L, Cserjesi P, Anderson DJ (1997) Mash1 and neurogenin1 expression patterns define complementary domains of neuroepithelium in the developing CNS and are correlated with regions expressing notch ligands. J Neurosci 17:3644-3652
20. Matsunaga E, Nakamura H, Chédotal A (2006) Repulsive guidance molecule plays multiple roles in neuronal differentiation and axon guidance. J Neurosci 26:6082-6088
21. Matsuura I, Endo M, Hata K, Kubo T, Yamaguchi A, Saeki N, Yamashita T (2007) BMP inhibits neurite growth by a mechanism dependent on LIM-kinase. Biochem Biophys Res Commun 360:868-873
22. Matsuura I, Taniguchi J, Hata K, Saeki N, Yamashita T (2008) BMP inhibition enhances axonal growth and functional recovery after spinal cord injury. J Neurochem 105:1471-1479
23. Mills CD, Bitler JL, Woolf CJ (2005) Role of the peripheral benzodiazepine receptor in sensory neuron regeneration. Mol Cell Neurosci 30:228-237
24. Mills CD, Allchorne AJ, Griffin RS, Woolf CJ, Costigan M (2007) GDNF selectively promotes regeneration of injury-primed sensory neurons in the lesioned spinal cord. Mol Cell Neurosci 36:185-194
25. Moon JI, Birren SJ (2008) Target-dependent inhibition of sympathetic neuron growth via modulation of a BMP signaling pathway. Dev Biol 315:404-417
26. Niederkofler V, Salie R, Sigrist M, Arber S (2004) Repulsive guidance molecule (RGM) gene function is required for neural tube closure but not retinal topography in the mouse visual system. J Neurosci 24:808-818
27. Niederkofler V, Salie R, Arber S (2005) Hemojuvelin is essential for dietary iron sensing, and its mutation leads to severe iron overload. J Clin Invest 115:2180-2186
28. Oldekamp J, Krämer N, Alvarez-Bolado G, Skutella T (2004) Expression pattern of the repulsive guidance molecules RGM A-C during mouse development. Gene Expr Patterns 4:283-288
29. Oldham MC, Horvath S, Geschwind DH (2006) Conservation and evolution of gene coexpression networks in human and chimpanzee brains. Proc Natl Acad Sci U S A 103:17973-17978
30. Oldham MC, Konopka G, Iwamoto K, Langfelder P, Kato T, Horvath S, Geschwind DH (2008) Functional organization of the transcriptome in human brain. Nat Neurosci 11:1271-1282
31. Rosen V (2006) BMP and BMP inhibitors in bone. Ann N Y Acad Sci 1068:19-25
32. Samad TA, Srinivasan A, Karchewski LA, Jeong SJ, Campagna JA, Ji RR, Fabrizio DA, Zhang Y, Lin HY, Bell E, Woolf CJ (2004) DRAGON: a member of the repulsive guidance molecule-related family of neuronaland muscle-expressed membrane proteins is regulated by DRG11 and has neuronal adhesive properties. J Neurosci 24:2027-2036
33. Samad TA, Rebbapragada A, Bell E, Zhang Y, Sidis Y, Jeong SJ, Campagna JA, Perusini S, Fabrizio DA, Schneyer AL, Lin HY, Brivanlou AH, Attisano L, Woolf CJ (2005) DRAGON, a bone morphogenetic protein coreceptor. J Biol Chem 280:14122-14129
34. Sánchez-Camacho C, Bovolenta P (2009) Emerging mechanisms in morphogen-mediated axon guidance. Bioessays 31:1013-1025
35. Schwab JM, Monnier PP, Schluesener HJ, Conrad S, Beschorner R, Chen L, Meyermann R, Mueller BK (2005) Central nervous system injuryinduced repulsive guidance molecule expression in the adult human brain. Arch Neurol 62:1561-1568
36. Seijffers R, Allchorne AJ, Woolf CJ (2006) The transcription factor ATF-3 promotes neurite outgrowth. Mol Cell Neurosci 32:143-154
37. Seijffers R, Mills CD, Woolf CJ (2007) ATF3 increases the intrinsic growth state of DRG neurons to enhance peripheral nerve regeneration. J Neurosci 27:7911-7920
38. Severyn CJ, Shinde U, Rotwein P (2009) Molecular biology, genetics and biochemistry of the repulsive guidance molecule family. Biochem J 422:393-403
39. Sjöberg J, Kanje M (1990) The initial period of peripheral nerve regeneration and the importance of the local environment for the conditioning lesion effect. Brain Res 529:79-84
40. Smith WC (1999) TGF beta inhibitors. New and unexpected requirements in vertebrate development. Trends Genet 15:3-5
41. Tsujii M, Akeda K, Iino T, Uchida A (2009) Are BMPs involved in normal nerve and following transection?: a pilot study. Clin Orthop Relat Res 467:3183-3189
42. Wu MY, Hill CS (2009) Tgf-beta superfamily signaling in embryonic development and homeostasis. Dev Cell 16:329-343
43. Xia Y, Sidis Y, Mukherjee A, Samad TA, Brenner G, Woolf CJ, Lin HY, Schneyer A (2005) Localization and action of Dragon (repulsive guidance molecule b), a novel bone morphogenetic protein coreceptor, throughout the reproductive axis. Endocrinology 146:3614-3621
44. Xia Y, Babitt JL, Bouley R, Zhang Y, Da Silva N, Chen S, Zhuang Z, Samad TA, Brenner GJ, Anderson JL, Hong CC, Schneyer AL, Brown D, Lin HY (2010) Dragon enhances BMP signaling and increases transepithelial resistance in kidney epithelial cells. J Am Soc Nephrol 21:666-677
45. Xia Y, Cortez-Retamozo V, Niederkofler V, Salie R, Chen S, Samad TA, Hong CC, Arber S, Vyas JM, Weissleder R, Pittet MJ, Lin HY (2011) Dragon (repulsive guidance molecule B) inhibits IL-6 expression in macrophages. J Immunol 186:1369-1376
46. Xiao Q, Du Y, Wu W, Yip HK (2010) Bone morphogenetic proteins mediate cellular response and, together with Noggin, regulate astrocyte differentiation after spinal cord injury. Exp Neurol 221:353-366
47. Zhao GQ (2003) Consequences of knocking out BMP signaling in the mouse. Genesis 35:43-56
48. Zou H, Ho C, Wong K, Tessier-Lavigne M (2009) Axotomy-induced Smad1 activation promotes axonal growth in adult sensory neurons. J Neurosci 29:7116-7123