NRAGE, a p75NTR adaptor protein, is required for developmental apoptosis in vivo

Cell Death and Differentiation

Volumn 15, Issue 12, 2008, Pages 1921-1929

  Bertrand, M J M ^a,b,c   Kenchappa, R S ^d   Andrieu, D ^e   Leclercq Smekens, M ^a   Nguyen, H N T ^a   Carter, B D ^d   Muscatelli, F ^e   Barker, P A ^c   De Backer, O ^a,b  

^a UNIVERSITY OF NAMUR   (Belgium)

^b LUDWIG INSTITUTE FOR CANCER RESEARCH   (Belgium)

^c MCGILL UNIVERSITY   (Canada)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MELANOMA ANTIGEN 1; NEUROTROPHIN INTERACTING MAGE HOMOLOGUE; NEUROTROPHIN RECEPTOR P75; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; GENE DELETION; GENE EXPRESSION REGULATION; GENE LOCATION; HAIR FOLLICLE; IN VIVO STUDY; KNOCKOUT MOUSE; MALE; MOTONEURON; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SYMPATHETIC NERVE CELL;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; APOPTOSIS; FERTILITY; GENE TARGETING; HAIR FOLLICLE; MICE; MICE, KNOCKOUT; MOTOR NEURONS; MUTATION; NEOPLASM PROTEINS; RECEPTOR, NERVE GROWTH FACTOR; SYMPATHETIC NERVOUS SYSTEM; TRIGEMINAL GANGLION;

ANIMALIA; MUS;

EID: 56349161988     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2008.127     Document Type: Article

References (45)

1. Roux PP, Barker PA. Neurotrophin signaling through the p75 neurotrophin receptor. Prog Neurobiol 2002; 67: 203-233.
2. Nykjaer A, Willnow TE, Petersen CM. p75NTR - live or let die. Curr Opin Neurobiol 2005; 15: 49-57.
3. Teng KK, Hempstead BL. Neurotrophins and their receptors: Signaling trios in complex biological systems. Cell Mol Life Sci 2004; 61 35-48.
4. Beattie MS, Harrington AW, Lee R, Kim JY, Boyce SL, Longo FM et al ProNGF induces p75-mediated death of oligodendrocytes following spinal cord injury. Neuron 2002; 36: 375-386.
5. Bhakar AL, Howell JL, Paul CE, Salehi AH, Becker EB, Said F et al. Apoptosis induced by p75NTR overexpression requires Jun kinase-dependent phosphorylation of Bad. J Neurosci 2003; 23: 11373-11381.
6. Harrington AW, Leiner B, Blechschmitt C, Arevalo JC, Lee R, Morl K et al. Secreted proNGF is a pathophysiological death-inducing ligand after adult CNS injury. Proc Natl Acad Sci USA 2004; 101: 6226-6230.
7. Wang X, Bauer JH, Li Y, Shao Z, Zetoune FS, Cattaneo E et al. Characterization of a p75(NTR) apoptotic signaling pathway using a novel cellular model. J Biol Chem 2001; 276: 33812-33820.
8. Kuwako K, Taniura H, Yoshikawa K. Necdin-related MAGE proteins differentially interact with the E2F1 transcription factor and the p75 neurotrophin receptor. J Biol Chem 2004; 279: 1703-1712.
9. Salehi AH, Roux PP, Kubu CJ, Zeindler C, Bhakar A, Tannis LL et al NRAGE, a novel MAGE protein, interacts with the p75 neurotrophin receptor and facilitates nerve growth factor-dependent apoptosis. Neuron 2000; 27: 279-288.
10. Tcherpakov M, Bronfman FC, Conticello SG, Vaskovsky A, Levy Z, Niinobe M et al. The p75 neurotrophin receptor interacts with multiple MAGE proteins. J Biol Chem 2002; 277: 49101-49104.
11. Salehi AH, Xanthoudakis S, Barker PA. NRAGE, a p75 neurotrophin receptor-interacting protein, induces caspase activation and cell death through a JNK-dependent mitochondrial pathway. J Biol Chem 2002; 277: 48043-48050.
12. Xue B, Wen C, Shi Y, Zhao D, Li C. Human NRAGE disrupts E-cadherin/ beta-catenin regulated homotypic cell-cell adhesion. Biochem Biophys Res Commun 2005; 336: 247-251.
13. Masuda Y, Sasaki A, Shibuya H, Ueno N, Ikeda K, Watanabe K. Dlxin-1, a novel protein that binds Dlx5 and regulates its transcriptional function. J Biol Chem 2001; 276: 5331-5338.
14. Kuwajima T, Taniura H, Nishimura I, Yoshikawa K. Necdin interacts with the Msx2 homeodomain protein via MAGE-D1 to promote myogenic differentiation of C2C12 cells. J Biol Chem 2004; 279: 40484-40493.
15. Chomez P, De Backer O, Bertrand M, De Plaen E, Boon T, Lucas S. An overview of the MAGE gene family with the identification of all human members of the family. Cancer Res 2001; 61: 5544-5551.
16. Muller-Rover S, Handjiski B, van der Veen C, Eichmuller S, Foitzik K, McKay IA et al. A comprehensive guide for the accurate classification of murine hair follicles in distinct hair cycle stages. J Invest Dermatol 2001; 117: 3-15.
17. Peters EM, Stieglitz MG, Liezman C, Overall RW, Nakamura M, Hagen E et al. p75 Neurotrophin receptor-mediated signaling promotes human hair follicle regression (Catagen). Am J Pathol 2006; 168: 221-234.
18. Botchkarev VA, Botchkareva NV, Albers KM, Chen LH, Welker P, Paus R. A role for p75 neurotrophin receptor in the control of apoptosis-driven hair follicle regression. FASEB J 2000; 14: 1931-1942.
19. Bertrand M, Huijbers I, Chomez P, De Backer O. Comparative expression analysis of the MAGED genes during embryogenesis and brain development. Dev Dyn 2004; 230: 325-334.
20. Bamji SX, Majdan M, Pozniak CD, Belliveau DJ, Aloyz R, Kohn J et al The p75 neurotrophin receptor mediates neuronal apoptosis and is essential for naturally occurring sympathetic neuron death. J Cell Biol 1998; 140: 911-923.
21. Kenchappa RS, Zampieri N, Chao MV, Barker PA, Teng HK, Hempstead BL et al. Ligand- dependent cleavage of the P75 neurotrophin receptor is necessary for NRIF nuclear translocation and apoptosis in sympathetic neurons. Neuron 2006; 50: 219-232.
22. Deppmann CD, Mihalas S, Sharma N, Lonze BE, Niebur E, Ginty DD. A model for neuronal competition during development. Science 2008; 320 369-373.
23. Bergmann I, Priestley JV, McMahon SB, Brocker EB, Toyka KV, Koltzenburg M. Analysis of cutaneous sensory neurons in transgenic mice lacking the low affinity neurotrophin receptor p75. Eur J Neurosci 1997; 9 18-28.
24. Yamashita T, Tucker KL, Barde YA. Neurotrophin binding to the p75 receptor modulates Rho activity and axonal outgrowth. Neuron 1999; 24: 585-593.
25. Lee K-L, Bachman K, Landis S, Jaenisch R. Dependence on p75 for innervation of some sympathetic targets. Science 1994; 263: 1447-1449.
26. Ernfors P, Henschen A, Olson L, Persson H. Expression of nerve growth factor receptor mRNA is developmentally regulated and increased after axotomy in rat spinal cord motoneurons. Neuron 1989; 2: 1605-1613.
27. Wiese S, Metzger F, Holtmann B, Sendtner M. The role of p75NTR in modulating neurotrophin survival effects in developing motoneurons. Eur J Neurosci 1999; 11: 1668-1676.
28. Sedel F, Bechade C, Triller A. Nerve growth factor (NGF) induces motoneuron apoptosis in rat embryonic spinal cord in vitro. Eur J Neurosci 1999; 11: 3904-3912.
29. Murray SS, Bartlett PF, Cheema SS. Differential loss of spinal sensory but not motor neurons in the p75NTR knockout mouse. Neurosci Lett 1999; 267: 45-48.
30. Yamamoto W, Henderson CE. Patterns of programmed cell death in populations of developing spinal motoneurons in chicken, mouse, and rat. Dev Biol 1999; 1999: 60-71.
31. Barker PA, Salehi A. The MAGE proteins: Emerging roles in cell cycle progression, apoptosis, and neurogenetic disease. J Neurosci Res 2002; 67: 705-712.
32. Bischof JM, Ekker M, Wevrick R. A MAGE/NDN-like gene in zebrafish. Dev Dyn 2003; 228: 475-479.
33. Lopez-Sanchez N, Gonzalez-Fernandez Z, Niinobe M, Yoshikawa K, Frade JM. Single mage gene in the chicken genome encodes CMage, a protein with functional similarities to mammalian type II Mage proteins. Physiol Genomics 2007; 30: 156-171.
34. Sasaki A, Masuda Y, Iwai K, Ikeda K, Watanabe K. A RING finger protein Praja1 regulates Dlx5-dependent transcription through its ubiquitin ligase activity for the Dlx/Msx-interacting MAGE/Necdin family protein, Dlxin-1. J Biol Chem 2002; 277: 22541-22546.
35. Wen CJ, Xue B, Qin WX, Yu M, Zhang MY, Zhao DH et al. hNRAGE, a human neurotrophin receptor interacting MAGE homologue, regulates p53 transcriptional activity and inhibits cell proliferation. FEBS Lett 2004; 564: 171-176.
36. Kendall SE, Goldhawk DE, Kubu C, Barker PA, Verdi JM. Expression analysis of a novel p75(NTR) signaling protein, which regulates cell cycle progression and apoptosis. Mech Dev 2002; 117: 187-200.
37. Kendall SE, Battelli C, Irwin S, Mitchell JG, Glackin CA, Verdi JM. NRAGE mediates p38 activation and neural progenitor apoptosis via the bone morphogenetic protein signaling cascade. Mol Cell Biol 2005; 25: 7711-7724.
38. Salehi AH, Roux PP, Kubu CJ, Zeindler C, Bhakar A, Tannis LL et al NRAGE, a novel MAGE protein, interacts with the p75 neurotrophin receptor and facilitates nerve growth factor-dependent apoptosis. Neuron 2000; 27: 279-288.
39. Botchkareva NV, Botchkarev VA, Chen LH, Lindner G, Paus R. A role for p75 neurotrophin receptor in the control of hair follicle morphogenesis. Dev Biol 1999; 216: 135-153.
40. Peters EM, Hendrix S, Golz G, Klapp BF, Arck PC, Paus R. Nerve growth factor and its precursor differentially regulate hair cycle progression in mice. J Histochem Cytochem 2006; 54: 275-288.
41. Pehar M, Cassina P, Vargas MR, Castellanos R, Viera L, Beckman JS et al. Astrocytic production of nerve growth factor in motor neuron apoptosis: Implications for amyotrophic lateral sclerosis. J Neurochem 2004; 89: 464-473.
42. Williams ME, Strickland P, Watanabe K, Hinck L. UNC5H1 induces apoptosis via its juxtamembrane region through an interaction with NRAGE. J Biol Chem 2003; 278: 17483-17490.
43. Williams ME, Lu X, McKenna WL, Washington R, Boyette A, Strickland P et al. UNC5A promotes neuronal apoptosis during spinal cord development independent of netrin-1. Nat Neurosci 2006; 9: 996-998.
44. Lee K-F, Li E, Huber J, Landis SC, Sharpe AH, Chao MV et al. Targeted mutation of the gene encoding the low affinity NGF receptor leads to deficits in the peripheral sensory nervous system. Cell 1992; 69: 737-749.
45. Palmada M, Kanwal S, Rutkoski NJ, Gustafson-Brown C, Johnson RS, Wisdom R et al. c-jun is essential for sympathetic neuronal death induced by NGF withdrawal but not by p75 activation. J Cell Biol 2002; 158: 453-461.