Plasticity in rat uterine sympathetic nerves: The role of TrkA and p75 nerve growth factor receptors

Journal of Anatomy

Volumn 207, Issue 2, 2005, Pages 125-134

  Richeri, Analía ^a   Bianchimano, Paola ^a   Mármol, Nelson M ^a   Viettro, Lorena ^a   Cowen, Timothy ^b   Brauer, M Mónica ^a  

^a INSTITUTO DE INVESTIGACIONES BIOLÓGICAS CLEMENTE ESTABLE   (Uruguay)

^b ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

Author keywords

Neurotrophins; Oestrogen; Pregnancy; Puberty

Indexed keywords

ESTRADIOL; ESTROGEN; FLUOROGOLD; NERVE GROWTH FACTOR RECEPTOR; NEUROTROPHIN RECEPTOR; PROTEIN P75; PROTEIN TYROSINE KINASE A;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENSITOMETRY; FEMALE; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; NERVE CELL PLASTICITY; NONHUMAN; PREPUBERTY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SUPERIOR CERVICAL GANGLION; SYMPATHETIC INNERVATION; SYMPATHETIC NERVE; SYMPATHETIC TRUNK; TARGET ORGAN; THIRD TRIMESTER PREGNANCY; UTERUS;

EID: 23344444119     PISSN: 00218782     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1469-7580.2005.00435.x     Document Type: Article

References (68)

1. Alberts KM, Wright DR, Davis BM (1994) Overexpression of nerve growth factor in epidermis of transgenic mice causes hypertrophy of peripheral nervous system. J Neurocytol 14, 1422-1432.
2. Belliveau DJ, Krivko I, Kohn J, et al. (1997) NGF and neurotrophin-3 both activate TrkA on sympathetic neurons but differentially regulate survival and neuritogenesis. J Cell Biol 136, 375-388.
3. Björling DE, Beckman M, Clayton MK, Wang ZY (2002) Modulation of nerve growth factor in peripheral organs by estrogen and progesterone. Neuroscience 110, 155-167.
4. Blaustein JD (2003) Progestin receptors: neuronal integrators of hormonal and environmental stimulation. Ann NY Acad Sci 1007, 238-250.
5. Brauer MM, Lincoln J, Blundell D, Corbacho A (1992) Postnatal development of noradrenaline-containing nerves of the rat uterus. J Autonom Nerv Syst 39, 37-50.
6. Brauer MM, Corbacho A, Burnstock G (1995) Effects of chronic and acute oestrogen treatment on the development of noradrenaline-containing nerves of the rat uterus. Int J Dev Neurosci 13, 791-798.
7. Brauer MM, Burnstock G, Thrasivoulou C, Cowen T (1998) In oculo transplants of myometrium from postpartum guinea pigs fail to support sympathetic reinnervation. J Anat 193, 509-517.
8. Brauer MM, Chávez-Genaro R, Llodrá J, Richeri A, Scorza MC (2000a) Effects of chronic oestrogen treatment are not selective for uterine sympathetic nerves: a transplantation study. J Anat 196, 347-355.
9. Brauer MM, Shockley KP, Chávez R, Richeri A, Cowen T, Crutcher KA (2000b) The role of NGF in pregnancy-induced degeneration and regeneration of sympathetic nerves in the guinea pig uterus. J Autonom Nerv Syst 79, 19-27.
10. Brauer MM, Chávez-Genaro R, Richeri A, et al. (2002) The oestrogenized rat myometrium inhibits organotypic sympathetic reinnervation. Auton Neurosci 101, 13-22.
11. Brennan C, Rivas-Plata K, Landis SC (1999) The p75 neurotrophin receptor influence NT-3 responsiveness of sympathetic neurons in vivo. Nat Neurosci 2, 699-705.
12. Chalar C, Richeri A, Viettro L, et al. (2003) Plasticity in rat uterine sensory nerves: the role of NGF and TrkA. Cell Tissue Res 314, 191-205.
13. Chávez-Genaro R, Crutcher K, Viettro L, et al. (2002) Differential effects of oestrogen on developing and mature uterine sympathetic nerves. Cell Tissue Res 308, 61-73.
14. Cowen T, Thrasivoulou C (1992) A microscopical assay using densitometric application of image analysis to quantify neurotransmitter dynamics. J Neurosci Meth 45, 107-116.
15. Cowen T, Woodhoo A, Sullivan CD, et al. (2003) Reduced age-related plasticity of neurotrophin receptor expression in sympathetic neurons of the rat. Aging Cell 2, 59-69.
16. Dechant G (2001) Molecular interactions between neurotrophin receptors. Cell Tissue Res 305, 229-238.
17. Dobrowsky RT, Werner MH, Castellino AM, Chao MV, Hannun YA (1994) Activation of the sphingomyelin cycle through the low-affinity neurotrophin receptor. Science 265, 1596-1599.
18. Dobrowsky RT, Jenkins GM, Hannun YA (1995) Neurotrophins induce sphingomyelin hydrolysis modulation by co-expressing p75 with Trk receptors. J Cell Chem 270, 22135-22142.
19. Esposito D, Patel P, Stephens RM, et al. (2001) The cytoplasmic and transmembrane domain of the p75 and TrkA receptors regulate high affinity binding to nerve growth factor. J Biol Chem 276, 32687-32695.
20. Frade JM, Barde YA (1998) Nerve growth factor: two receptors, multiple functions. Bioessays 20, 137-145.
21. Gatzinsky KP, Haugland RP, Thrasivoulou C, Orike N, Budi-Santoso AW, Cowen T (2001) p75 and TrkA receptors are both required for uptake of NGF in adult sympathetic neurons: use of a novel fluorescent NGF conjugate. Brain Res 920, 226-238.
22. Gibbs RB, Pfaff DW (1992) Effect of estrogen and fimbria/ fornix transection on p75NGFR and ChAT expression in the medial septum and diagonal band of Broca. Exp Neurol 116, 23-39.
23. Gibbs RB (1998) Levels of trkA and BDNF mRNA, but not NGF mRNA, fluctuate across the estrous cycle and increase in response to acute hormone replacement. Brain Res 787, 259-268.
24. Gruber CJ, Huber JC (2003) Differential effects of progestins on the brain. Maturitas 46S1, S71-S75.
25. Haase EB, Buchman J, Tietz AE, Schramm LP (1997) Pregnancy-induced uterine neuronal degeneration in the rat. Cell Tissue Res 288, 293-306.
26. Hartman DS, McCormack M, Schnubenel R, Hertel C (1992) Multiple trkA proteins in PC12 cells bind NGF with a slow association rate. J Biol Chem 267, 24516-24522.
27. Hempstead BM, Martin-Zanca D, Kaplan DR, Parada LF, Chao MV (1991) High affinity binding requires co-expression of trk proto-oncogen and the low affinity NGF receptor. Nature 350, 678-683.
28. Houdeau E, Rousseau A, Meusnier C, Prud'homme MJ, Rousseau JP (1998) Sympathetic innervation of the upper and lower regions of the uterus and cervix in the rat have different origins and routes. J Comp Neurol 399, 403-412.
29. Jezierski MK, Sohrabji F (2001) Neurotrophin expression in the reproductively senescent forebrain is refractory to estrogen stimulation. Neurobiol Aging 22, 309-319.
30. Katsuda SI, Yoshida M, Watanabe T, et al. (1999) Estrogen receptor mRNA in uteri of normal estrous cycling and ovariectomised rats by in situ hybridization. Proc Soc Exp Biol Med 221, 207-214.
31. Kohn J, Aloyz RS, Toma JG, Haal-Frendsch M, Miller FD (1999) Functionally antagonistic interactions between the TrkA and p75 neurotrophin receptors regulate sympathetic neuron growth and target innervation. J Neurosci 19, 5393-5408.
32. Korsching S, Thoenen H (1983) Nerve growth factor in sympathetic ganglia and corresponding target organs of the rat, correlation with density of sympathetic innervation. Proc Natl Acad Sci USA 80, 3513-3616.
33. Krizsan-Agbas D, Smith PG (2002) Estrogen modulates myometrium-incluced sympathetic neurite formation through actions on target and ganglion. Neuroscience 114, 339-347.
34. Krizsan-Agbas D, Pedchenko T, Hasan W, Smith PG (2003) Oestrogen regulates sympathetic neurite outgrowth by modulating brain derived neurotrophic factor synthesis and release by the rodent uterus. Eur J Neurosci 18, 2760-2768.
35. Lanlua P, Decorti F, Gangula PRR, Chung Taglialatela G, Yallampalli C (2001) Female steroid hormones modulate receptors for nerve growth factor in rat dorsal root ganglia. Biol Reprod 64, 331-338.
36. Levi-Montalcini R (1987) The nerve growth factor 35 years later. Science 237, 1154-1162.
37. Liuzzi FJ, Scoville SA, Bufton SM (1999) Long-term estrogen replacement coordinately decreases trkA and beta-PPT mRNA levels in dorsal root ganglion neurons. Exp Neurol 155, 260-267.
38. Lonstein JS, Blaustein JD (2004) Immunocytochemical investigation of nuclear progestin receptor expression with dopaminergic neurons of the female rat brain. J Neuroendocrinol 16, 534-543.
39. Ma Y, Campenot RB, Miller FD (1992) Concentration-dependent regulation of neuronal gene expression by nerve growth factor. J Cell Biol 117, 135-141.
40. Meakin SO, Shooter EM (1991) Molecular investigations on the high affinity nerve growth factor receptor. Neuron 6, 153-163.
41. Medlock KL, Forrester TM, Sheehan DM (1991) Short-term effects of physiological and pharmacological doses of estradiol on estrogen receptor and uterine growth. J Recept Res 11, 743-756.
42. Melo RCN, Machado RS (1993) Noradrenergic and acetylcholinesterase-positive nerve fibres of the uterus in sexually immature and cycling rats. Histochem J 25, 213-218.
43. Miller FD, Mathew TC, Toma JG (1991) Regulation of nerve growth factor receptor gene expression by nerve growth factor in the developing peripheral nervous system. J Cell Biol 112, 303-312.
44. Miller FD, Speelman A, Mathew TC, et al. (1994) Nerve growth factor derived from terminals selectively increases the ratio p75 to trkA NGF receptors on mature sympathetic neurons. Dev Biol 161, 206-217.
45. Miller FD, Kaplan DR (2001) Neurotrophin signaling pathways regulating neuronal apoptosis. Cell Mol Life Sci 58, 1045-1053.
46. Miranda RC, Sohrabji F, Toran-Allerand CD (1993) Estrogen target neurons co-localize the mRNAs for the neurotrophins and their receptors during development: a basis for the interactions of estrogen and the neurotrophins. Molec Cell Neurosci 4, 510-525.
47. Ojeda SR, Urbanski HF (1994) Puberty in the rat. In The Physiology of Reproduction (eds Knobill E,Neil JD), pp.363-409. New York: Raven Press.
48. Orike N, Thrasivoulou C, Wrigley A, Cowen T (2001a) Differential regulation of survival and growth in adult sympathetic neurons: an in vitro study of neurotrophin responsiveness. J Neurobiol 47, 295-305.
49. Orike N, Middleton G, Borthwick E, Buchman VL, Cowen T, Davis AM (2001 b) Role of PI 3-kinase, Art and BCl-2-related proteins in sustaining the survival of neurotrophic factor-independent adult sympathetic neurons. J Cell Biol 154, 995-1005.
50. Owman C, Stjernquist M (1988) Origin, distribution and functional aspects of aminergic and peptidergic nerves in the male and female genital tracts. In Handbook of Chemical Neuroanatomy, Vol. 6. The Peripheral Nervous System (eds Björklund A, Hökfelt T, Owman C), pp. 445-544. Amsterdam: Elsevier Science Publishers.
51. Posse de Chaves EI, Bussière M, Vance DE, Campenot RB, Vance JE (1997) Elevation of ceramide within distal neurites inhibits neurite growth in cultured rat sympathetic neurons. J Biol Chem 272, 3028-3035.
52. Sohrabji F, Greene LA, Miranda RC, Toran-Allerand CD (1994a) Reciprocal regulation of estrogen and NGF receptors by their ligands in PC12 cells. J Neurobiol 25, 974-988.
53. Sohrabji F, Miranda RC, Toran-Allerand D (1994b) Estrogen differentially regulates estrogen and nerve growth factor receptors mRNAs in adult sensory neurons. J Neurosci 14, 459-471.
54. Sohrabji F, Miranda RC, Toran-Allerand CD (1995) Identification of a putative oestrogen response element in the gene encoding brain-derived neurotrophic factor. Proc Natl Acad Sci USA 92, 11110-11114.
55. Sporrong B, Alm P, Owman Ch, Sjöberg NO, Thorbert G (1981) Pregnancy is associated with extensive adrenergic nerve degeneration in the uterus. An electronmicroscopic study in the guinea pig. Neuroscience 6, 1119-1126.
56. Taleghany N, Sarajari S, DonCarlos LL, Gollapudi L, Oblinger MM (1999) Differential expression of estrogen receptor alpha and beta in rat dorsal root ganglion neurons. J Neurosci Res 57, 603-615.
57. Toran-Allerand CD (2000) Novel sites and mechanisms of oestrogen action in the brain. Novartis Foundation 230. Neuronal and Cognitive Effects of Oestrogen, pp. 56-73. Chichester: John Wiley & Sons.
58. Toran-Allerand CD (2004) Minireview: a plethora of estrogen receptors in the brain: where will it end? Endocrinology 145, 1069-1074.
59. Varol FG, Duchemin AM, Neff HN, Hadjiconstantinou M (2000) Nerve growth factor (NGF) and NGF mRNA change in rat uterus during pregnancy. Neurosci Lett 294, 58-62.
60. Walsh G, Krol KM, Kawaja MD (1999) 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.
61. Xu B, Michalski B, Racine RJ, Fahnestock M (2002) Continuous infusion of neurotrophin-3 triggers sprouting, decreases the levels of TrkA and inhibits epileptogenesis amd activity-dependent axonal growth in adult rats. Neuroscience 115, 1295-1308.
62. Yamada M (1988) Changes in the innervation of the uterus during pregnancy and following parturition: histochemical and electron microscopic observations in the rat and man. Acta Obstet Gynecol Jpn 40, 145-152.
63. Zhou XF, Rush RA (1996a) Functional roles of neurotrophin 3 in the developing and mature sympathetic nervous system. Mol Neurobiol 13, 185-197.
64. Zhou XF, Rush RA (1996b) Endogenous nerve growth factor is required for regulation of the low affinity neurotrophin receptor (p75) in sympathetic but not sensory ganglia. J Comp Neurol 372, 37-48.
65. Zoubina EV, Fan Q, Smith PG (1998) Variation in uterine innervation during the estrous cycle. J Comp Neurol 397, 561-571.
66. Zoubina EV, Smith PG (2000) Axonal degeneration and regeneration in rat uterus during the estrous cycle. Auton Neurosci 84, 176-185.
67. Zoubina EV, Smith PG (2001) Sympathetic hyperinnervation of the uterus in the estrogen receptor alpha knock-out mouse. Neuroscience 103, 237-244.
68. Zoubina EV, Smith PG (2002) Distributions of estrogen receptors alpha and beta in sympathetic neurons of female rats: enriched expression by uterine innervation. J Neurobiol 52, 14-23.