Overexpression of nerve growth factor by murine smooth muscle cells: Role of the p75 neurotrophin receptor on sympathetic and sensory sprouting

Journal of Comparative Neurology

Volumn 521, Issue 11, 2013, Pages 2621-2643

  Petrie, Casey N ^a   Smithson, Laura J ^a   Crotty, Anne Marie ^b   Michalski, Bernadeta ^c   Fahnestock, Margaret ^c   Kawaja, Michael D ^a,b  

^a QUEEN S UNIVERSITY   (Canada)

^b QUEEN S UNIVERSITY   (Canada)

^c MCMASTER UNIVERSITY   (Canada)

Author keywords

Colon; Nerve growth factor; P75; Transgene; Urinary bladder

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; NERVE GROWTH FACTOR; NEUROTROPHIN RECEPTOR P75; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLADDER; CELL DENSITY; CONTROLLED STUDY; DESCENDING COLON; FEMALE; GENE OVEREXPRESSION; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NERVE CELL; NERVE SPROUTING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SENSORY GANGLION; SENSORY NERVE; SENSORY NERVE CELL; SMOOTH MUSCLE FIBER; SYMPATHETIC NERVE;

ANIMALS; AXONS; BLOTTING, WESTERN; CELL COUNT; COLON; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; MICE; MICE, TRANSGENIC; MUSCLE, SMOOTH; NERVE FIBERS; NERVE GROWTH FACTOR; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, NERVE GROWTH FACTOR; SENSORY RECEPTOR CELLS; SYMPATHETIC NERVOUS SYSTEM; URINARY BLADDER;

EID: 84878641305     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23302     Document Type: Article

References (85)

1. Albers KM, Wright DE, Davis BM. 1994. Overexpression of nerve growth factor in epidermis of transgenic mice causes hypertrophy of the peripheral nervous system. J Neurosci 14: 1422-1432.
2. Alexander JM, Hsu D, Penchuk L, Heinrich G. 1989. Cell-specfic and developmental regulation of a nerve growth factor-huan growth hormone fusion gene in transgenic mice. Neuron 3: 133-139.
3. Allsopp TE, Robinson M, Wyatt S, Davies AM. 1993. Ectopic trkA expression mediates a NGF survival response in NGF-independent sensory neurons but not in parasympathetic neurons. J Cell Biol 123: 1555-1566.
4. Aloe L, Mugnaini E, Levi-Montalcini R. 1975. Light and electron microscopic studies on the excessive growth of sympathetic ganglia in rats injected daily from birth with 6-OHDA and NGF. Arch Ital Biol 113: 326-353.
5. Barada KA, Mourad FH, Sawah SI, Khoury C, Safieh-Garabedian B, Nassar CF, Tawil A, Jurjus A, Saade NE. 2007. Up-regulation of nerve growth factor and interleukin-10 in inflamed and non-inflamed intestinal segments in rats with experimental colitis. Cytokine 37: 236-245.
6. Barde YA. 1994. Neurotrophins: a family of proteins supporting the survival of neurons. Prog Clin Biol Res 390: 45-56.
7. Bergmann I, Priestley JV, McMahon SB, Brocker EB, Toyka KV, Koltzenburg M. 1997. Analysis of cutaneous sensory neurons in transgenic mice lacking the low affinity neurotrophin receptor p75. Eur J Neurosci 9: 18-28.
8. Bibel M, Hoppe E, Barde YA. 1999. Biochemical and functional interactions between the neurotrophin receptors trk and p75NTR. EMBO J 18: 616-622.
9. Brown A, Ricci MJ, Weaver LC. 2007. NGF mRNA is expressed in the dorsal root ganglia after spinal cord injury in the rat. Exp Neurol 205: 283-286.
10. Brumovsky P, Villar MJ, Hökfelt T. 2006. Tyrosine hydroxylase is expressed in a subpopulation of small dorsal root ganglion neurons in the adult mouse. Exp Neurol 200: 153-165.
11. Christianson JA, Liang R, Ustinova EE, Davis BM, Fraser MO, Pezzone MA. 2007. Convergence of bladder and colon sensory innervation occurs at the primary afferent level. Pain 128: 235-243.
12. Chun LL, Patterson PH. 1977. Role of nerve growth factor in the development of rat sympathetic neurons in vitro. I. Survival, growth, and differentiation of catecholamine production. J Cell Biol 75: 694-704.
13. Coome GE, Elliott J, Kawaja MD. 1998. Sympathetic and sensory axons invade the brains of nerve growth factor transgenic mice in the absence of p75NTR expression. Exp Neurol 149: 284-294.
14. Coughlin MD, Boyer DM, Black IB. 1977. Embryologic development of a mouse sympathetic ganglion in vivo and in vitro. Proc Natl Acad Sci U S A 74: 3438-3442.
15. Counts SE, Mufson EJ. 2005. The role of nerve growth factor receptors in cholinergic basal forebrain degeneration in prodromal Alzheimer disease. J Neuropathol Exp Neurol 64: 263-272.
16. Crowley C, Spencer SD, Nishimura MC, Chen KS, Pitts-Meek S, Armanini MP, Ling LH, McMahon SB, Shelton DL, Levinson AD. 1994. Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons. Cell 76: 1001-1011.
17. Davis BM, Albers KM, Seroogy KB, Katz DM. 1994. Overexpression of nerve growth factor in transgenic mice induces novel sympathetic projections to primary sensory neurons. J Comp Neurol 349: 464-474.
18. Davis BM, Goodness TP, Soria A, Albers KM. 1998. Over-expression of NGF in skin causes formation of novel sympathetic projections to trkA-positive sensory neurons. Neuroreport 9: 1103-1107.
19. Delafoy L, Gelot A, Ardid D, Eschalier A, Bertrand C, Doherty AM, Diop L. 2006. Interactive involvement of brain derived neurotrophic factor, nerve growth factor, and calcitonin gene related peptide in colonic hypersensitivity in the rat. Gut 55: 940-945.
20. Dhanoa NK, Krol KM, Jahed A, Crutcher KA, Kawaja MD. 2006. Null mutations for exon III and exon IV of the p75 neurotrophin receptor gene enhance sympathetic sprouting in response to elevated levels of nerve growth factor in transgenic mice. Exp Neurol 198: 416-426.
21. Diamond J, Coughlin M, Macintyre L, Holmes M, Visheau B. 1987. Evidence that endogenous beta nerve growth factor is responsible for the collateral sprouting, but not the regeneration, of nociceptive axons in adult rats. Proc Natl Acad Sci U S A 84: 6596-6600.
22. Edwards RH, Rutter WJ, Hanahan D. 1989. Directed expression of NGF to pancreatic beta cells in transgenic mice leads to selective hyperinnervation of the islets. Cell 58: 161-170.
23. Elliott J, MacLellan A, Saini JK, Chan J, Scott S, Kawaja MD. 2009. Transgenic mice expressing nerve growth factor in smooth muscle cells. Neuroreport 20: 223-227.
24. Fahnestock M, Michalski B, Xu B, Coughlin MD. 2001. The precursor pro-nerve growth factor is the predominant form of nerve growth factor in brain and is increased in Alzheimer's disease. Mol Cell Neurosci 18: 210-220.
25. Ghasemlou N, Krol KM, Macdonald DR, Kawaja MD. 2004. Comparison of target innervation by sympathetic axons in adult wild type and heterozygous mice for nerve growth factor or its receptor trkA. J Pineal Res 37: 230-240.
26. Gorin PD, Johnson EM. 1979. Experimental autoimmune model of nerve growth factor deprivation: effects on developing peripheral sympathetic and sensory neurons. Proc Natl Acad Sci U S A 76: 5382-5386.
27. Greene LA, Kaplan DR. 1995. Early events in neurotrophin signalling via Trk and p75 receptors. Curr Opin Neurobiol 5: 579-587.
28. Grimes ML, Zhou J, Beattie EC, Yuen EC, Hall DE, Valletta JS, Topp KS, LaVail JH, Bunnett NW, Mobley WC. 1996. Endocytosis of activated TrkA: evidence that nerve growth factor induces formation of signaling endosomes. J Neurosci 16: 7950-7964.
29. Hannila SS, Kawaja MD. 1999. Nerve growth factor-induced growth of sympathetic axons into the optic tract of mature mice is enhanced by an absence of p75NTR expression. J Neurobiol 39: 51-66.
30. Hannila SS, Kawaja MD. 2003. Distribution of central sensory axons in transgenic mice overexpressing nerve growth factor and lacking functional p75 neurotrophin receptor expression. Eur J Neurosci 18: 312-322.
31. Hannila SS, Kawaja MD. 2005. Nerve growth factor-mediated collateral sprouting of central sensory axons into deafferentated regions of the dorsal horn is enhanced in the absence of the p75 neurotrophin receptor. J Comp Neurol 486: 331-343.
32. Hannila SS, Lawrance GM, Ross GM, Kawaja MD. 2004. TrkA and mitogen-activated protein kinase phosphorylation are enhanced in sympathetic neurons lacking functional p75 neurotrophin receptor expression. Eur J Neurosci 19: 2903-2908.
33. Hassankhani A, Steinhelper ME, Soonpaa MH, Katz EB, Taylor DA, Andrade-Rozental A, Factor SM, Steinberg JJ, Field LJ, Federoff HJ. 1995. Overexpression of NGF within the heart of transgenic mice causes hyperinnervation, cardiac enlargement, and hyperplasia of ectopic cells. Dev Biol 169: 309-321.
34. Hoyle GW, Mercer EH, Palmiter RD, Brinster RL. 1993. Expression of NGF in sympathetic neurons leads to excessive axon outgrowth from ganglia but decreased terminal innervation within tissues. Neuron 10: 1019-1034.
35. Huber LJ, Chao MV. 1995. Mesenchymal and neuronal cell expression of the p75 neurotrophin receptor gene occur by different mechanisms. Dev Biol 167: 227-238.
36. Hughes IE, Kirk JA, Kneen B, Large BJ. 1973. An assessment of sympathetic function in isolated tissues from mice given nerve-growth-factor antiserum and 6-hydroxydopamine. Br J Pharmacol 47: 748-759.
37. Isaacson LG, Saffran BN, Crutcher KA. 1990. Intracerebral NGF infusion induces hyperinnervation of cerebral blood vessels. Neurobiol Aging 11: 51-55.
38. Jacobs BL, Smaldone MC, Tyagi V, Philips BJ, Jackman SV, Leng WW, Tyagi P. 2010. Increased nerve growth factor in neurogenic overactive bladder and interstitial cystitis patients. Can J Urol 17: 4989-4994.
39. Jahed A, Kawaja MD. 2005. The influences of p75 neurotrophin receptor and brain-derived neurotrophic factor in the sympathetic innervation of target tissues during murine postnatal development. Auton Neurosci 118: 32-42.
40. Johnson EMJr, Yip HK. 1985. Central nervous system and peripheral nerve growth factor provide trophic support critical to mature sensory neuronal survival. Nature 314: 751-752.
41. Kaplan DR, Martin-Zanca D, Parada LF. 1991a. Tyrosine phosphorylation and tyrosine kinase activity of the trk proto-oncogene product induced by NGF. Nature 350: 158-160.
42. Kaplan DR, Hempstead BL, Martin-Zanca D, Chao MV, Parada LF. 1991b. The trk proto-oncogene product: a signal transducing receptor for nerve growth factor. Science 252: 554-558.
43. Kawaja MD. 1998. Sympathetic and sensory innervation of the extracerebral vasculature: roles for p75NTR neuronal expression and nerve growth factor. J Neurosci Res 52: 295-306.
44. Kawaja MD, Crutcher KA. 1997. Sympathetic axons invade the brains of mice overexpressing nerve growth factor. J Comp Neurol 383: 60-72.
45. Klein R. 1994. Role of neurotrophins in mouse neuronal development. FASEB J 8: 738-744.
46. Klein R, Jing SQ, Nanduri V, O'Rourke E, Barbacid M. 1991. The trk proto-oncogene encodes a receptor for nerve growth factor. Cell 65: 189-197.
47. Krol KM, Stein EJ, Elliott J, Kawaja MD. 2001. TrkA-expressing trigeminal sensory neurons display both neurochemical and structural plasticity despite a loss of p75NTR function: responses to normal and elevated levels of nerve growth factor. Eur J Neurosci 13: 35-47.
48. Lee KF, Li E, Huber LJ, Landis SC, Sharpe AH, Chao MV, Jaenisch R. 1992. Targeted mutation of the gene encoding the low affinity NGF receptor p75 leads to deficits in the peripheral sensory nervous system. Cell 69: 737-749.
49. Levi-Montalcini R. 1987. The nerve growth factor 35 years later. Science 237: 1154-1162.
50. Levi-Montalcini R, Skaper SD, Dal Toso R, Petrelli L, Leon A. 1996. Nerve growth factor: from neurotrophin to neurokine. Trends Neurosci 19: 514-520.
51. Liao J, Xu X, Wargovich MJ. 2000. Direct reprobing with anti-beta-actin antibody as an internal control for Western blotting analysis. Biotechniques 28: 216-218.
52. Liu HT, Chen CY, Kuo HC. 2010. Urinary nerve growth factor levels in overactive bladder syndrome and lower urinary tract disorders. J Formosa Med Assoc 109: 862-878.
53. Liu HT, Lin H, Kuo HC. 2011. Increased serum nerve growth factor levels in patients with overactive bladder syndrome refractory to antimuscarinic therapy. Neurourol Urodyn 30: 1525-1529.
54. Ma W, Ribeiro-da-Silva A, Noel G, Julien JP, Cuello AC. 1995. Ectopic substance P and calcitonin gene-related peptide immunoreactive fibres in the spinal cord of transgenic mice over-expressing nerve growth factor. Eur J Neurosci 7: 2021-2035.
55. Majdan M, Lachance C, Gloster A, Aloyz R, Zeindler C, Bamji S, Bhakar A, Belliveau D, Fawcett J, Miller FD, Barker PA. 1997. Transgenic mice expressing the intracellular domain of the p75 neurotrophin receptor undergo neuronal apoptosis. J Neurosci 17: 6988-6998.
56. Majdan M, Walsh GS, Aloyz R, Miller FD. 2001. TrkA mediates developmental sympathetic neuron survival in vivo by silencing an ongoing p75NTR-mediated death signal. J Cell Biol 155: 1275-1285.
57. Manni L, Lundeberg T, Tirassa P, Aloe L. 2002. Role of cholecystokinin-8 in nerve growth factor and nerve growth factor mRNA expression in carrageenan-induced joint inflammation in adult rats. Rheumatology 41: 787-792.
58. Meakin SO, Shooter EM. 1991. Molecular investigations on the high-affinity nerve growth factor receptor. Neuron 6: 153-163.
59. Mearow KM, Kril Y, Diamond J. 1993. Increased NGF mRNA expression in denervated rat skin. Neuroreport 4: 351-354.
60. Miller FD, Speelman A, Matthew TC, Fabian J, Pozniac C, Toma JG. 1994. Nerve growth factor derived from terminals selectively selectively increases the ratio of p75 to TrkA NGF receptors on mature sympathetic neurons. Dev Biol 161: 206-217.
61. Oppenheim RW, Maderdrut JL, Wells DJ. 1982. Reduction of naturally occurring cell death in the thoraco-lumbar preganglionic cell column of the chick embryo by nerve growth factor and hemicholinium-3. Brain Res 255: 134-139.
62. Otten U, Goedert M, Schwab M, Thibault J. 1979. Immunization of adult rats against 2.5 S NGF: effects on the peripheral sympathetic nervous system. Brain Res 176: 79-90.
63. Price J, Mudge AW. 1983. A subpopulation of rat dorsal root ganglion neurones is catecholaminergic. Nature 301: 241-243.
64. Qiao LY, Grider JR. 2010. Colitis elicits differential changes in the expression levels of receptor tyrosine kinase TrkA and TrkB in colonic afferent neurons: a possible involvement of axonal transport. Pain 151: 117-127.
65. Quarcoo D, Schulte-Herbruggen O, Lommatzsch M, Schierhorn K, Hoyle GW, Renz H, Braun A. 2004. Nerve growth factor induces increased airway inflammation via a neuropeptide-dependent mechanism in a transgenic animal model of allergic airway inflammation. Clin Exp Allergy 34: 1146-1151.
66. Saffran BN, Crutcher KA. 1990. NGF-induced remodeling of mature uninjured axon collaterals. Brain Res 13; 525: 11-20.
67. Saffran BN, Woo JE, Mobley WC, Crutcher KA. 1989. Intraventricular NGF infusion in the mature rat brain enhances sympathetic innervation of cerebrovascular targets but fails to elicit sympathetic ingrowth. Brain Res 492: 245-254.
68. Saragovi HU, Zheng W, Maliartchouk S, DiGugliemo GM, Mawal YR, Kamen A, Woo SB, Cuello AC, Debeir T, Neet KE. 1998. A TrkA-selective, fast internalizing nerve growth factor-antibody complex induces trophic but not neuritogenic signals. J Biol Chem 273: 34933-34940.
69. Schnegelsberg B, Sun TT, Cain G, Bhattacharya A, Nunn PA, Ford AP, Vizzard MA, Cockayne DA. 2010. Overexpression of NGF in mouse urothelium leads to neuronal hyperinnervation, pelvic sensitivity, and changes in urinary bladder function. Am J Physiol Regul Integr Comp Physiol 298: R534-R547.
70. Sebert ME, Shooter EM. 1993. Expression of mRNA for neurotrophic factors and their receptors in the rat dorsal root ganglion and sciatic nerve following nerve injury. J Neurosci Res 36: 357-367.
71. Smeyne RJ, Klein R, Schnapp A, Long LK, Bryant S, Lewin A, Lira SA, Barbacid M. 1994. Severe sensory and sympathetic neuropathies in mice carrying a disrupted Trk/NGF receptor gene. Nature 368: 246-249.
72. Stanzel RD, Lourenssen S, Blennerhassett MG. 2008. Inflammation causes expression of NGF in epithelial cells of the rat colon. Exp Neurol 211: 203-213.
73. Straznicky C, Rush RA. 1985. The effect of nerve growth factor on developing primary sensory neurons of the trigeminal nerve in chick embryos. Anat Embryol 171: 91-95.
74. Thoenen H. 1991. The changing scene of neurotrophic factors. Trends Neurosci 14: 165-170.
75. Vega JA, Amenta F, Hernandez LC, del Valle ME. 1991. Presence of catecholamine-related enzymes in a subpopulation of primary sensory neurons in dorsal root ganglia of the rat. Cell Mol Biol 37: 519-530.
76. Vetter ML, Martin-Zanca D, Parada LF, Bishop JM, Kaplan DR. 1991. Nerve growth factor rapidly stimulates tyrosine phosphorylation of phospholipase C-gamma 1 by a kinase activity associated with the product of the trk protooncogene. Proc Natl Acad Sci U S A 88: 5650-5654.
77. Vizzard MA. 2000. Changes in urinary bladder neurotrophic factor mRNA and NGF protein following urinary bladder dysfunction. Exp Neurol 161: 273-284.
78. von Schack D, Casademunt E, Schweigreiter R, Meyer M, Bibel M, Dechant G. 2001. Complete ablation of the neurotrophin receptor p75NTR causes defects both in the nervous and the vascular system. Nat Neurosci 4: 977-978.
79. Walsh GS, Petruccelli K, Kawaja MD. 1998. p75-Deficient sensory axons are immunoreactive for the glycoprotein L1 in mice overexpressing nerve growth factor. Brain Res 798: 184-194.
80. Walsh GS, Krol KM, Kawaja MD. 1999a. Absence of the p75 neurotrophin receptor alters the pattern of sympathosensory sprouting in the trigeminal ganglia of mice overexpressing nerve growth factor. J Neurosci 19: 258-273.
81. Walsh GS, Krol KM, Crutcher KA, Kawaja MD. 1999b. Enhanced neurotrophin-induced axon growth in myelinated portions of the CNS in mice lacking the p75 neurotrophin receptor. J Neurosci 19: 4155-4168.
82. Wehrman T, He X, Raab B, Dukipatti A, Blau H, Garcia KC. 2007. Structural and mechanistic insights into nerve growth factor interactions with the TrkA and p75 receptors. Neuron 53: 25-38.
83. White FA, Silos-Santiago I, Molliver DC, Nishimura M, Phillips H, Barbacid M, Snider WD. 1996. Synchronous onset of NGF and TrkA survival dependence in developing dorsal root ganglia. J Neurosci 16: 4662-4672.
84. Woodbury CJ, Kullmann FA, McIlwrath SL, Koerber HR. 2008. Identity of myelinated cutaneous sensory neurons projecting to nocireceptive laminae following nerve injury in adult mice. J Comp Neurol 508: 500-509.
85. Yip HK, Rich KM, Lampe PA, Johnson EMJr. 1984. The effects of nerve growth factor and its antiserum on the postnatal development and survival after injury of sensory neurons in rat dorsal root ganglia. J Neurosci 4: 2986-2992.