The differential axonal degradation of ret accounts for cell-type-specific function of glial cell line-derived neurotrophic factor as a retrograde survival factor

Journal of Neuroscience

Volumn 30, Issue 15, 2010, Pages 5149-5158

  Tsui, Cynthia C ^a   Pierchala, Brian A ^b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN SCHOOL OF DENTISTRY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; PROTEASOME; PROTEIN RET;

ANIMAL CELL; ARTICLE; CELL SURVIVAL; CELL TYPE; CONTROLLED STUDY; EMBRYO; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SENSORY NERVE CELL; SPINAL GANGLION; SYMPATHETIC NERVE CELL;

ANIMALS; AXONS; BIOLOGICAL TRANSPORT, ACTIVE; CELL CULTURE TECHNIQUES; CELL SURVIVAL; CELLS, CULTURED; GANGLIA, SPINAL; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; MICE; MICE, INBRED BALB C; NEURONS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN ISOFORMS; PROTO-ONCOGENE PROTEINS C-RET; RATS; RATS, SPRAGUE-DAWLEY; SENSORY RECEPTOR CELLS; SUPERIOR CERVICAL GANGLION; TIME FACTORS;

EID: 77950994645     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5246-09.2010     Document Type: Article

References (49)

1. Albers KM, Woodbury CJ, Ritter AM, Davis BM, Koerber HR (2006) Glial cell line-derived neurotrophic factor expression in skin alters the mechanical sensitivity of cutaneous nociceptors. J Neurosci 26:2981-2990.
2. Arenas E, Trupp M, Akerud P, Ibáñez CF (1995) GDNF prevents degeneration and promotes the phenotype of brain noradrenergic neurons in vivo. Neuron 15:1465-1473. (Pubitemid 26005383)
3. Baloh RH, Tansey MG, Lampe PA, Fahrner TJ, Enomoto H, Simburger KS, Leitner ML, Araki T, Johnson EM Jr, Milbrandt J (1998) Artemin, a novel member of the GDNF ligand family, supports peripheral and central neurons and signals through the GFRalpha3-RET receptor complex. Neuron 21:1291-1302. (Pubitemid 29022532)
4. Buj-Bello A, Buchman VL, Horton A, Rosenthal A, Davies AM (1995) GDNF is an age-specific survival factor for sensory and autonomic neurons. Neuron 15:821-828.
5. Cacalano G, Fariñas I, Wang LC, Hagler K, Forgie A, Moore M, Armanini M, Phillips H, Ryan AM, Reichardt LF, Hynes M, Davies A, Rosenthal A (1998) GFRalpha1 is an essential receptor component for GDNF in the developing nervous system and kidney. Neuron 21:53-62. (Pubitemid 28355691)
6. Coulpier M, Ibáñez CF (2004) Retrograde propagation of GDNF-mediated signals in sympathetic neurons. Mol Cell Neurosci 27:132-139. (Pubitemid 39370095)
7. Deckwerth TL, Johnson EM Jr (1993) Temporal analysis of events associated with programmed cell death (apoptosis) of sympathetic neurons deprived of nerve growth factor. J Cell Biol 123:1207-1222.
8. Durbec P, Marcos-Gutierrez CV, Kilkenny C, Grigoriou M, Wartiowaara K, Suvanto P, Smith D, Ponder B, Costantini F, Saarma M, Sariola H, Pachnis V (1996) GDNF signalling through the Ret receptor tyrosine kinase. Nature 381:789-793. (Pubitemid 26243119)
9. Enomoto H, Heuckeroth RO, Golden JP, Johnson EM, Milbrandt J (2000) Development of cranial parasympathetic ganglia requires sequential actions of GDNF and neurturin. Development 127:4877-4889.
10. Garcès A, Haase G, Airaksinen MS, Livet J, Filippi P, deLapeyrière O (2000) GFRα1 is required for development of distinct subpopulations of motoneuron. J Neurosci 20:4992-5000.
11. Haase G, Dessaud E, Garcès A, de Bovis B, Birling M, Filippi P, Schmalbruch H, Arber S, deLapeyrière O (2002) GDNF acts through PEA3 to regulate cell body positioning and muscle innervation of specific motor neuron pools. Neuron 35:893-905.
12. Henderson CE, Phillips HS, Pollock RA, Davies AM, Lemeulle C, Armanini M, Simmons L, Moffet B, Vandlen RA, Simpson LC (1994) GDNF: a potent survival factor for motoneurons present in peripheral nerve and muscle. Science [Erratum (1995) 267:777] 266:1062-1064. (Pubitemid 24373728)
13. Honma Y, Araki T, Gianino S, Bruce A, Heuckeroth R, Johnson E, Milbrandt J (2002) Artemin is a vascular-derived neurotrophic factor for developing sympathetic neurons. Neuron 35:267-282. (Pubitemid 34876730)
14. Jain S, Naughton CK, Yang M, Strickland A, Vij K, Encinas M, Golden J, Gupta A, Heuckeroth R, Johnson EM Jr, Milbrandt J (2004) Mice expressing a dominant-negative Ret mutation phenocopy human Hirschsprung disease and delineate a direct role of Ret in spermatogenesis. Development 131:5503-5513. (Pubitemid 39562192)
15. Jing S, Wen D, Yu Y, Holst PL, Luo Y, Fang M, Tamir R, Antonio L, Hu Z, Cupples R, Louis JC, Hu S, Altrock BW, Fox GM (1996) GDNF-induced activation of the ret protein tyrosine kinase is mediated by GDNFR-alpha, a novel receptor for GDNF. Cell 85:1113-1124. (Pubitemid 26231176)
16. Kotzbauer PT, Lampe PA, Heuckeroth RO, Golden JP, Creedon DJ, Johnson EM Jr, Milbrandt J (1996) Neurturin, a relative of glial-cell-line-derived neurotrophic factor. Nature 384:467-470.
17. Kramer ER, Knott L, Su F, Dessaud E, Krull CE, Helmbacher F, Klein R (2006) Cooperation between GDNF/Ret and ephrinA/EphA4 signals for motor-axon pathway selection in the limb. Neuron 50:35-47.
18. Kuruvilla R, Zweifel LS, Glebova NO, Lonze BE, Valdez G, Ye H, Ginty DD (2004) A neurotrophin signaling cascade coordinates sympathetic neuron development through differential control of TrkA trafficking and retrograde signaling. Cell 118:243-255. (Pubitemid 38962579)
19. Leitner ML, Molliver DC, Osborne PA, Vejsada R, Golden JP, Lampe PA, Kato AC, Milbrandt J, Johnson EM Jr (1999) Analysis of the retrograde transport of glial cell line-derived neurotrophic factor (GDNF), neurturin, and persephin suggests that in vivo signaling for the GDNF family is GFRα coreceptor specific. J Neurosci 19:9322-9331.
20. Levi-Montalcini R (1987) The nerve growth factor 35 years later. Science 237:1154-1162. (Pubitemid 17124912)
21. Li L, Wu W, Lin LF, Lei M, Oppenheim RW, Houenou LJ (1995) Rescue of adult mouse motoneurons from injury-induced cell death by glial cell line-derived neurotrophic factor. Proc Natl Acad Sci U S A 92:9771-9775.
22. Lin LF, Doherty DH, Lile JD, Bektesh S, Collins F (1993) GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science 260:1130-1132. (Pubitemid 23186789)
23. Luo W, Wickramasinghe SR, Savitt JM, Griffin JW, Dawson TM, Ginty DD (2007) A hierarchical NGF signaling cascade controls Ret-dependent and Ret-independent events during development of nonpeptidergic DRG neurons. Neuron 54:739-754. (Pubitemid 46843519)
24. Meng X, Lindahl M, Hyvönen ME, Parvinen M, de Rooij DG, Hess MW, Raatikainen-Ahokas A, Sainio K, Rauvala H, Lakso M, Pichel JG, Westphal H, Saarma M, Sariola H (2000) Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science 287:1489-1493. (Pubitemid 30127143)
25. Milbrandt J, de Sauvage FJ, Fahrner TJ, Baloh RH, Leitner ML, Tansey MG, Lampe PA, Heuckeroth RO, Kotzbauer PT, Simburger KS, Golden JP, Davies JA, Vejsada R, Kato AC, Hynes M, Sherman D, Nishimura M, Wang LC, Vandlen R, Moffat B, Klein RD, Poulsen K, Gray C, Garces A, Johnson EM Jr (1998) Persephin, a novel neurotrophic factor related to GDNF and neurturin. Neuron 20:245-253. (Pubitemid 28125069)
26. Molliver DC, Wright DE, Leitner ML, Parsadanian AS, Doster K, Wen D, Yan Q, Snider WD (1997) IB4-binding DRG neurons switch from NGF to GDNF dependence in early postnatal life. Neuron 19:849-861. (Pubitemid 27471389)
27. Moore MW, Klein RD, Fariñas I, Sauer H, Armanini M, Phillips H, Reichardt LF, Ryan AM, Carver-Moore K, Rosenthal A (1996) Renal and neuronal abnormalities in mice lacking GDNF. Nature 382:76-79. (Pubitemid 26243361)
28. Mount HT, Dean DO, Alberch J, Dreyfus CF, Black IB (1995) Glial cell line-derived neurotrophic factor promotes the survival and morphologic differentiation of Purkinje cells. Proc Natl Acad Sci U S A 92:9092-9096.
29. Oppenheim RW, Houenou LJ, Johnson JE, Lin LF, Li L, Lo AC, Newsome AL, Prevette DM, Wang S (1995) Developing motor neurons rescued from programmed and axotomy-induced cell death by GDNF. Nature 373:344-346.
30. Oppenheim RW, Houenou LJ, Parsadanian AS, Prevette D, Snider WD, Shen L (2000) Glial cell line-derived neurotrophic factor and developing mammalian motoneurons: regulation of programmed cell death among motoneuron subtypes. J Neurosci 20:5001-5011. (Pubitemid 30421704)
31. Paratcha G, Ledda F, Ibáñez CF (2003) The neural cell adhesion molecule NCAM is an alternative signaling receptor for GDNF family ligands. Cell 113:867-879. (Pubitemid 36792031)
32. Pichel JG, Shen L, Sheng HZ, Granholm AC, Drago J, Grinberg A, Lee EJ, Huang SP, Saarma M, Hoffer BJ, Sariola H, Westphal H (1996) Defects in enteric innervation and kidney development in mice lacking GDNF. Nature 382:73-76. (Pubitemid 27257993)
33. Pierchala BA, Milbrandt J, Johnson EM Jr (2006) Glial cell line-derived neurotrophic factor-dependent recruitment of Ret into lipid rafts enhances signaling by partitioning Ret from proteasome-dependent degradation. J Neurosci 26:2777-2787. (Pubitemid 43357861)
34. Poteryaev D, Titievsky A, Sun YF, Thomas-Crusells J, Lindahl M, Billaud M, Arumäe U, Saarma M (1999) GDNF triggers a novel ret-independent Src kinase family-coupled signaling via a GPI-linked GDNF receptor alpha1. FEBS Lett 463:63-66. (Pubitemid 30001719)
35. Pozas E, Ibáñez CF (2005) GDNF and GFRalpha1 promote differentiation and tangential migration of cortical GABAergic neurons. Neuron 45:701-713. (Pubitemid 40320705)
36. Rosenblad C, Grønborg M, Hansen C, Blom N, Meyer M, Johansen J, Dagø L, Kirik D, Patel UA, Lundberg C, Trono D, Björklund A, Johansen TE (2000) In vivo protection of nigral dopamine neurons by lentiviral gene transfer of the novel GDNF-family member neublastin/artemin. Mol Cell Neurosci 15:199-214.
37. Sánchez MP, Silos-Santiago I, Frisén J, He B, Lira SA, Barbacid M (1996) Renal agenesis and the absence of enteric neurons in mice lacking GDNF. Nature 382:70-73. (Pubitemid 26243359)
38. Sanicola M, Hession C, Worley D, Carmillo P, Ehrenfels C, Walus L, Robinson S, Jaworski G, Wei H, Tizard R, Whitty A, Pepinsky RB, Cate RL (1997) Glial cell line-derived neurotrophic factor-dependent RET activation can be mediated by two different cell-surface accessory proteins. Proc Natl Acad Sci U S A 94:6238-6243. (Pubitemid 27270668)
39. Scott RP, Eketjäll S, Aineskog H, Ibáñez CF (2005) Distinct turnover of alternatively spliced isoforms of the RET kinase receptor mediated by differential recruitment of the Cbl ubiquitin ligase. J Biol Chem 280:13442-13449.
40. Treanor JJ, Goodman L, de Sauvage F, Stone DM, Poulsen KT, Beck CD, Gray C, Armanini MP, Pollock RA, Hefti F, Phillips HS, Goddard A, Moore MW, Buj-Bello A, Davies AM, Asai N, Takahashi M, Vandlen R, Henderson CE, Rosenthal A (1996) Characterization of a multicomponent receptor for GDNF. Nature 382:80-83.
41. Trupp M, Rydén M, Jörnvall H, Funakoshi H, Timmusk T, Arenas E, Ibáñez CF (1995) Peripheral expression and biological activities of GDNF, a new neurotrophic factor for avian and mammalian peripheral neurons. J Cell Biol 130:137-148.
42. Trupp M, Scott R, Whittemore SR, Ibáñez CF (1999) Ret-dependent and -independent mechanisms of glial cell line-derived neurotrophic factor signaling in neuronal cells. J Biol Chem 274:20885-20894. (Pubitemid 129519586)
43. Tsui-Pierchala BA, Ginty DD (1999) Characterization of an NGF-P-TrkA retrograde-signaling complex and age-dependent regulation of TrkA phosphorylation in sympathetic neurons. J Neurosci 19:8207-8218.
44. Tsui-Pierchala BA, Milbrandt J, Johnson EM Jr (2002a) NGF utilizes c-Ret via a novel GFL-independent, inter-RTK signaling mechanism to maintain the trophic status of mature sympathetic neurons. Neuron 33:261-273. (Pubitemid 34127758)
45. Tsui-Pierchala BA, Ahrens RC, Crowder RJ, Milbrandt J, Johnson EM Jr (2002b) The long and short isoforms of Ret function as independent signaling complexes. J Biol Chem 277:34618-34625.
46. Vega QC, Worby CA, Lechner MS, Dixon JE, Dressler GR (1996) Glial derived neurotrophic factor is a ligand for RET and promotes kidney morphogenesis. Proc Natl Acad Sci U S A 93:10657-10661.
47. Whitehead J, Keller-Peck C, Kucera J, Tourtellotte WG (2005) Glial cell-line derived neurotrophic factor-dependent fusimotor neuron survival during development. Mech Dev 122:27-41. (Pubitemid 39593743)
48. Wright DE, Snider WD (1996) Focal expression of glial cell line-derived neurotrophic factor in developing mouse limb bud. Cell Tissue Res 286:209-217.
49. Yan Q, Matheson C, Lopez OT (1995) In vivo neurotrophic effects of GDNF on neonatal and adult facial motor neurons. Nature 373:341-344.