Muscle ciliary neurotrophic factor receptor α promotes axonal regeneration and functional recovery following peripheral nerve lesion

Journal of Comparative Neurology

Volumn 521, Issue 13, 2013, Pages 2947-2965

  Lee, Nancy ^a   Spearry, Rachel P ^a   Leahy, Kendra M ^a   Robitz, Rachel ^a   Trinh, Dennis S ^a   Mason, Carter O ^a   Zurbrugg, Rebekah J ^a   Batt, Myra K ^a   Paul, Richard J ^a   Maclennan, A John ^a  

^a UNIVERSITY OF CINCINNATI   (United States)

Author keywords

Cre recombinase; Mlc1f Cre; Mouse; Muscle CNTF receptor ; Sciatic

Indexed keywords

CILIARY NEUROTROPHIC FACTOR RECEPTOR ALPHA; CRE RECOMBINASE; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CILIARY NEUROTROPHIC FACTOR RECEPTOR ALPHA GENE; CONTROLLED STUDY; CONVALESCENCE; CRE RECOMBINASE GENE; EXTENSOR DIGITORUM LONGUS MUSCLE; FEMALE; GENE; GENE CONSTRUCT; GENE DISRUPTION; GENE EXPRESSION; GENE INSERTION; GENE LOCUS; IN VITRO STUDY; IN VIVO STUDY; MALE; MOLECULAR INTERACTION; MOTONEURON; MOTOR PERFORMANCE; MOUSE; MYOSIN LIGHT CHAIN 1F GENE; NERVE CRUSH; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NERVE SPROUTING; NEUROANATOMICAL TRACT TRACING; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; SCIATIC NERVE INJURY; SOLEUS MUSCLE; SYNAPTOSOME; TIBIALIS ANTERIOR MUSCLE; WEIGHT CHANGE;

CRE RECOMBINASE; MLC1F-CRE; MOUSE; MUSCLE CNTF RECEPTOR Α; SCIATIC;

ANALYSIS OF VARIANCE; ANIMALS; AXONS; BACTERIAL PROTEINS; BODY WEIGHT; CELL SURVIVAL; CILIARY NEUROTROPHIC FACTOR RECEPTOR ALPHA SUBUNIT; DISEASE MODELS, ANIMAL; FUNCTIONAL LATERALITY; GENE EXPRESSION REGULATION; LUMINESCENT PROTEINS; MICE; MICE, TRANSGENIC; MOTOR NEURONS; MUSCLE CONTRACTION; MUSCLE FIBERS, SKELETAL; NERVE REGENERATION; NEUROMUSCULAR JUNCTION; RECEPTORS, CHOLINERGIC; RECOVERY OF FUNCTION; RNA, MESSENGER; SCIATIC NEUROPATHY; STILBAMIDINES; WALKING;

EID: 84880600760     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23324     Document Type: Article

References (77)

1. ALS CNTF Treatment Study (ACTS) Phase I-II Study Group. 1995. A phase I study of recombinant human ciliary neurotrophic factor (rHCNTF) in patients with amyotrophic lateral sclerosis. Clin Neuropharmacol 18:515-532.
2. ALS CNTF Treatment Study Group. 1996. A double-blind placebo-controlled clinical trial of subcutaneous recombinant human ciliary neurotrophic factor (rHCNTF) in amyotrophic lateral sclerosis. Neurology 46:1244-1249.
3. Bain JR, Mackinnon SE, Hunter DA. 1988. Functional evaluation of complete sciatic, peroneal, and posterior tibial nerve lesions in the rat. Plast Reconstr Surg 82:1052-1066.
4. Bervar M. 2000. Video analysis of standing-an alternative footprint analysis to assess functional loss following injury to the rat sciatic nerve. J Neurosci Methods 102:109-116.
5. Bothe GWM, Haspel JA, Smith CL, Wiener HH, Burden SJ. 2000. Selective expression of Cre recombinase in skeletal muscle fibers. Genesis 26:165-166.
6. Carson NE, Gu J, Ianuzzo CD. 1998. Detection of myosin heavy chain in skeletal muscles using monoclonal antibodies on formalin fixed, paraffin embedded tissue sections. J Histotechnol 21:19-24.
7. Crawford K, Flick R, Close L, Shelly D, Paul RJ, Bove K, Kumar A, Lessard J. 2002. Mice lacking skeletal muscle actin show reduced muscle strength and growth deficits and die during the neonatal period. Mol Cell Biol 22:5887-5896.
8. Dadon-Nachum M, Melamed E, Offen D. 2011. The "dying back" phenomenon of motor neurons in ALS. J Mol Neurosci 43:470-477.
9. Davis S, Aldrich TH, Ip NY, Stahl N, Scherer S, Farruggella T, DiStefano PS, Curtis R, Panayotatos N, Gascan H, Chevalier S, Yancopoulos GD. 1993a. Released form of CNTF receptor α component is a soluble mediator of CNTF responses. Science 259:1736-1739.
10. Davis S, Aldrich TH, Stahl N, Pan L, Taga T, Kishimoto T, Ip NY, Yancopoulos GD. 1993b. LIFRβ and gp130 as heterodimerizing signal transducers of the tripartite CNTF receptor. Science 260:1805-1808.
11. DeChiara TM, Vejsada R, Poueymirou WT, Acheson A, Suri C, Conover JC, Friedman B, McClain J, Pan L, Stahl N, Ip NY, Kato A, Yancopoulos GD. 1995. Mice lacking the CNTF receptor, unlike mice lacking CNTF, exhibit profound motor neuron deficits at birth. Cell 83:313-322.
12. De Medinaceli L, Freed WJ, Wyatt RJ. 1982. An index of the functional condition of rat sciatic nerve based on measurements made from walking tracks. Exp Neurol 77:634-643.
13. Derouet D, Rousseau F, Alfonsi F, Froger J, Hermann J, Barbier F, Perret D, Diveu C, Guillet C, Preisser L, Dumont A, Barbado M, Morel A, deLapeyriere O, Gascan H, Chevalier S. 2004. Neuropoietin, a new IL-6-related cytokine signaling through the ciliary neurotrophic factor receptor. Proc Natl Acad Sci U S A 101:4827-4832.
14. Dijkstra JR, Meek MF, Robinson PH, Gramsbergen A. 2000. Methods to evaluate functional nerve recovery in adult rats: walking track analysis, video analysis and the withdrawal reflex. J Neurosci Methods 96:89-96.
15. Elson GCA, Lelievre E, Guillet C, Chevalier S, Plun-Favreau H, Froger J, Suard I, Benoit de Coignac A, Delneste Y, Bonnefoy J-Y, Gauchat J-F, Gascan H. 2000. CLF associates with CLC to form a functional heteromeric ligand for the CNTF receptor complex. Nat Neurosci 3:867-872.
16. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, Nerbonne JM, Lichtman JW, Sanes JR. 2000. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28:41-51.
17. Forger NG, Prevette D, deLapeyriere O, de Bovis B, Wang S, Bartlett P, Oppenheim RW. 2003. Cardiotrophin-like cytokine/cytokine-like factor 1 is an essential trophic factor for lumbar and facial motoneurons in vivo. J Neurosci 23:8854-8858.
18. Fraysse B, Guillet C, Huchet-Cadiou C, Conte Camerino D, Gascan H, Leoty C. 2000. Ciliary neurotrophic factor prevents unweighting-induced functional changes in rat soleus muscle. J Appl Physiol 88:1623-1630.
19. Gould TW, Buss RR, Vinsant S, Prevette D, Sun W, Knudson CM, Milligan CE, Oppenheim RW. 2006. Complete dissociation of motor neuron death from motor dysfunction by Bax deletion in a mouse model of ALS. J Neurosci 26:8774-8786.
20. Guillet C, Auguste P, Mayo W, Kreher P, Gascan H. 1999. Ciliary neurotrophic factor is a regulator of muscular strength in aging. J Neurosci 19:1257-1262.
21. Gurney ME, Yamamoto H, Kwon Y. 1992. Induction of motor neuron sprouting in vivo by ciliary neurotrophic factor and basic fibroblast growth factor. J Neurosci 12:3241-3247.
22. Hare GM, Evans PJ, Mackinnon SE, Best TJ, Midha R, Szalai JP, Hunter DA. 1993. Walking track analysis: utilization of individual footprint parameters. Ann Plast Surg 30:147-153.
23. Harris J, Ayyub C, Shaw G. 1991. A molecular dissection of the carboxyterminal tails of the major neurofilament subunits NF-M and NF-H. J Neurosci Res 30:47-62.
24. Hatton WJ, Von Bartheld CS. 1999. Analysis of cell death in the trochlear nucleus of the chick embryo: calibration of the optical dissector counting method reveals systematic bias. J Comp Neurol 409:169-186.
25. Havenith MG, Visser R, Schrijvers-van Schendel JM, Bosman FT. 1990. Muscle fiber typing in routinely processed skeletal muscle with monoclonal antibodies. Histochemistry 93:497-499.
26. He S, Shelly DA, Moseley AE, James PF, James JH, Paul RJ, Lingrel JB. 2001. The alpha(1)- and alpha(2)-isoforms of Na-K-ATPase play different roles in skeletal muscle contractility. Am J Physiol Regul Integr Comp Physiol 281:R917-R925.
27. Helgren ME, Squinto SP, Davis HL, Parry DJ, Boulton TG, Heck CS, Zhu Y, Yancopoulos GD, Lindsay RM, DiStefano PS. 1994. Trophic effect of ciliary neurotrophic factor on denervated skeletal muscle. Cell 76:493-504.
28. Hosaka Y, Yokota T, Miyagoe-Suzuki Y, Yuasa K, Imamura M, Matsuda R, Ikemoto T, Kameya S, Takeda S. 2002. α1-Syntrophin-deficient skeletal muscle exhibits hypertrophy and aberrant formation of neuromuscular junctions during regeneration. J Cell Biol 158:1097-1107.
29. Huang S, Wang F, Hong G, Wan S, Kang H. 2002. Protective effects of ciliary neurotrophic factor on denervated skeletal muscle. J Tongji Med Univ 22:148-151.
30. Hughes SM, Cho M, Karsch-Mizrachi I, Travis M, Silberstein L, Leinwand LA, Blau HM. 1993. Three slow myosin heavy chains sequentially expressed in developing mammalian skeletal muscle. Dev Biol 158:183-199.
31. Hyman BT, Gomez-Isla T, Irizarry MC. 1998. Stereology: A practical primer for neuropathology. J Neuropathol Exp Neurol 57:305-310.
32. Ikeda K, Wong V, Holmlund TH, Greene T, Cedarbaum JM, Lindsay RM, Mitsumoto H. 1995. Histometric effects of ciliary neurotrophic factor in wobbler mouse motor neuron disease. Ann Neurol 37:47-54.
33. Ip NY, Yancopoulos GD. 1992. Ciliary neurotrophic factor and its receptor complex. Prog Growth Factor Res 4:139-155.
34. Itoh S, Fujimori KE, Uyeda A, Matsuda A, Kobayashi H, Shinomiya K, Tanaka J, Taguchi T. 2005. Long-term effects of muscle-derived protein with molecular mass of 77 kDa (MDP77) on nerve regeneration. J Neurosci Res 81:730-738.
35. Janjua MZ, Leong SK. 1984. Organization of neurons forming the femoral, sciatic, common peroneal and tibial nerves in rats and monkeys. Brain Res 310:311-323.
36. Klover P, Chen W, Zhu B-M, Hennighausen L. 2009. Skeletal muscle growth and fiber composition in mice are regulated through the transcription factors STAT5a/b: linking growth hormone to the androgen receptor. FASEB J 23:3140-3148.
37. Kokoeva MV, Yin H, Flier JS. 2005. Neurogenesis in the hypothalamus of adult mice: potential role in energy balance. Science 310:679-683.
38. Kwon YW, Gurney ME. 1994. Systemic injections of ciliary neurotrophic factor induce sprouting by adult motor neurons. Neuroreport 5:789-792.
39. Lambert PD, Anderson KD, Sleeman MW, Wong V, Tan J, Hijarunguru A, Corcoran TL, Murray JD, Thabet KE, Yancopoulos GD, Wiegand SJ. 2001. Ciliary neurotrophic factor activates leptin-like pathways and reduces body fat, without cachexia or rebound weight gain, even in leptin-resistant obesity. Proc Natl Acad Sci U S A 98:4652-4657.
40. Lee N, Robitz R, Zurbrugg RJ, Karpman AM, Mahler AM, Cronier SA, Vesey R, Spearry RP, Zolotukhin S, MacLennan AJ. 2008. Conditional, genetic disruption of ciliary neurotrophic factor receptors reveals a role in adult motor neuron survival. Eur J Neurosci 27:2830-2837.
41. Lee S-B, Beak SK, Park SH, Waterhouse BD, Lee HS. 2009. Collateral projection from the locus coeruleus to whisker-related sensory and motor brain regions of the rat. J Comp Neurol 514:387-402.
42. Li M, Sendtner M, Smith A. 1995. Essential function of LIF receptor in motor neurons. Nature 378:724-727.
43. Lucas CA, Kang LHD, Hoh JFY. 2000. Monospecific antibodies against the three mammalian fast limb myosin heavy chains. Biochem Biophys Res Comm 272:303-308.
44. Lyons GE, Ontell M, Cox R, Sassoon D, Buckingham M. 1990. The expression of myosin genes in developing skeletal muscle in the mouse embryo. J Cell Biol 111:1465-1476.
45. MacLennan AJ, Vinson EN, Marks L, McLaurin DL, Pfeifer M, Lee N. 1996. Immunohistochemical localization of ciliary neurotrophic factor receptor α expression in the rat nervous system. J Neurosci 16:621-630.
46. McCabe KL, Gunther EC, Reh TA. 1999. The development of the pattern of retinal ganglion cells in the chick retina: mechanisms that control differentiation. Development 126:5713-5724.
47. Miller RG, Bryan WW, Dietz MA, Munsat TL, Petajan JH, Smith SA, Goodpasture JC. 1996. Toxicity and tolerability of recombinant human ciliary neurotrophic factor in patients with amyotrophic lateral sclerosis. Neurology 47:1329-1331.
48. Mitsumoto H, Ikeda K, Holmlund T, Greene T, Cedarbaum JM, Wong V, Lindsay RM. 1994. The effects of ciliary neurotrophic factor on motor dysfunction in wobbler mouse motor neuron disease. Ann Neurol 36:142-148.
49. Nguyen QT, Son Y-J, Sanes JR, Lichtman JW. 2000. Nerve terminals form but fail to mature when postsynaptic differentiation is blocked: in vivo analysis using mammalian nerve-muscle chimeras. J Neurosci 20:6077-6086.
50. Okuno H, Kishimoto KN, Hatori M, Itoi E. 2012. 1α, 25-Dihydroxyvitamin D3 enhances fast-myosin heavy chain expression in differentiated C2C12 myoblasts. Cell Biol Int 36:441-447.
51. Oppenheim RW, Prevette D, Qin-Wei Y, Collins F, MacDonald J. 1991. Control of embryonic motoneuron survival in vivo by ciliary neurotrophic factor. Science 251:1616-1618.
52. Poea S, Guyon T, Lavasseur P, Berrih-Aknin S. 2001. Expression of ciliary neurotrophic factor receptor in myasthenia gravis. J Neuroimmunol 120:180-189.
53. Pun S, Santos AF, Saxena S, Xu L, Caroni P. 2006. Selective vulnerability and pruning of phasic motoneuron axons in motoneuron disease alleviated by CNTF. Nat Neurosci 9:408-19.
54. Robinson GA, Madison RD. 2009. Influence of terminal nerve branch size on motor neuron regeneration accuracy. Exp Neurol 215:228-235.
55. Rojiani AM, Cho ES. 1998. Neuropathologic applications of immunohistochemical fiber typing in the non-neoplastic muscle biopsy. Mod Pathol 11:334-338.
56. Saggio I, Gloaguen I, Poiana G, Laufer R. 1995. CNTF variants with increased biological potency and receptor selectivity define a functional site of receptor interaction. EMBO J 14:3045-3054.
57. Sahenk Z, Seharaseyon J, Mendell JR. 1994. CNTF potentiates peripheral nerve regeneration. Brain Res 655:246-250.
58. Schuettauf F, Zurakowski D, Quinto K, Varde MA, Besch D, Laties A, Anderson R, Wen R. 2005. Neuroprotective effects of cardiotropin-like cytokine on retinal ganglion cells. Graefes Arch Clin Exp Ophthalmol 243:1036-1042.
59. Sendtner M, Kreutzberg GW, Thoenen H. 1990. Ciliary neurotrophic factor prevents the degeneration of motor neurons after axotomy. Nature 345:440-441.
60. Sendtner M, Schmalbruch H, Stockli KA, Carroll P, Kreutzberg GW, Thoenen H. 1992a. Ciliary neurotrophic factor prevents degeneration of motor neurons in mouse mutant progressive motor neuronopathy. Nature 358:502-504.
61. Sendtner M, Stockli KA, Thoenen H. 1992b. Synthesis and localization of ciliary neurotrophic factor in the sciatic nerve of the adult rat after lesion and during regeneration. J Cell Biol 118:139-148.
62. Siegel SG, Patton B, English AW. 2000. Ciliary neurotrophic factor is required for motoneuron sprouting. Exp Neurol 166:205-212.
63. Smerdu V, Soukup T. 2008. Demonstration of myosin heavy chain isoforms in rat and humans: the specificity of seven available monoclonal antibodies used in immunohistochemical and immunoblotting methods. Eur J Histochem 52:179-190.
64. Soriano P. 1999. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21:70-71.
65. Swett JE, Torigoe Y, Elie VR, Bourassa CM, Miller PG. 1991. Sensory neurons of the rat sciatic nerve. Exp Neurol 114:82-103.
66. Tarabal O, Caldero J, Esquerda JE. 1996. Intramuscular nerve sprouting induced by CNTF is associated with increases in CGRP content in mouse motor nerve terminals. Neurosci Lett 219:60-64.
67. Wang M-S, Zeleny-Pooley M, Gold BG. 1997. Comparative dose-dependence study of FK506 and cyclosporin A on the rate of axonal regeneration in the rat sciatic nerve. J Pharm Exp Therap 282:1084-1093.
68. Watt MJ, Dzamko N, Thomas WG, Rose-John S, Ernst M, Carling D, Kemp BE, Febbraio MA, Steinberg GR. 2006. CNTF reverses obesity-induced insulin resistance by activating skeletal muscle AMPK. Nature Med 12:541-548.
69. Wattler S, Kelly M, Nehls M. 1999. Construction of gene targeting vectors from lKOS genomic libraries. BioTechniques 26:1150-1160.
70. Weis J, Lie DC, Ragoss U, Zuchner SL, Schroder JM, Karpati G, Farruggella T, Stahl N, Yancopoulos GD, DiStefano PS. 1998. Increased expression of CNTF receptor α in denervated human skeletal muscle. J Neuropathol Exp Neurol 57:850-857.
71. Wredenberg A, Wibom R, Wilhelmsson H, Graff C, Wiener HH, Burden SJ, Oldfors A, Westereblad H, Larsson N-G. 2002. Increased mitochondrial mass in mitochondrial myopathy mice. Proc Natl Acad Sci U S A 99:15066-15071.
72. Wright MC, Son Y-J, 2007. Ciliary neurotrophic factor is not required for terminal sprouting and compensatory reinnervation of neuromuscular synapses: reevaluation of CNTF null mice. Exp Neurol 205:437-448.
73. Wright MC, Cho W-J, Son Y-J. 2007. Distinct patterns of motor nerve terminal sprouting induced by ciliary neurotrophic factor vs. botulinum toxin. J Comp Neurol 504:1-16.
74. Yao M, Moir MS, Wang MZ, To MP, Terris DJ. 1999. Peripheral nerve regeneration in CNTF knockout mice. Laryngoscope 109:1263-1268.
75. Yumoto N, Kim N, Burden SJ. 2012. Lrp4 is a retrograde signal for presynaptic differentiation at neuromuscular synapses. Nature 489:438-442.
76. Zhou CJ, Kawabuchi M, Wang S, Liu WT, Hirata K. 2002. Age differences in morphological patterns of axonal sprouting and multiple innervation of neuromuscular junctions during muscle reinnervation following nerve crush injury. Ann Anat 184:461-472.
77. Zou X, Bolon B, Pretorius JK, Kurahara C, McCabe J, Christiansen KA, Sun N, Duryea D, Foreman O, Senaldi G, Itano AA, Siu G. 2009. Neonatal death in mice lacking cardiotropin-like cytokine is associated with multifocal neuronal hypoplasia. Vet Pathol 46:514-519.