The effects of exercise on synaptic stripping require androgen receptor signaling

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Liu, Caiyue ^a   Ward, Patricia J ^b   English, Arthur W ^b  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; FLUTAMIDE; GLUTAMATE DECARBOXYLASE 67; VESICULAR GLUTAMATE TRANSPORTER 1;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL LABELING; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FEMALE; IMMUNOREACTIVITY; MALE; MOTONEURON; MOUSE; NERVE FIBER REGENERATION; NERVE FIBER TRANSECTION; NEUROLOGICAL AND SENSORIAL PROCEDURES; NONHUMAN; REST; SCIATIC NERVE; SEX DIFFERENCE; SIGNAL TRANSDUCTION; SYNAPTIC STRIPPING; SYNAPTIC TRANSMISSION; TREADMILL EXERCISE; WALKING SPEED; ANIMAL; C57BL MOUSE; METABOLISM; PHYSIOLOGY; SURGERY; SYNAPSE;

ANIMALS; FEMALE; MALE; MICE; MICE, INBRED C57BL; PHYSICAL CONDITIONING, ANIMAL; RECEPTORS, ANDROGEN; SCIATIC NERVE; SIGNAL TRANSDUCTION; SYNAPSES;

EID: 84902340881     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0098633     Document Type: Article

References (63)

1. Frostick SP, Yin Q, Kemp GJ (1998) Schwann cells, neurotrophic factors, and peripheral nerve regeneration. Microsurgery 18: 397-405. (Pubitemid 29014397)
2. Scholz T, Krichevsky A, Sumarto A, Jaffurs D, Wirth GA, et al. (2009) Peripheral nerve injuries: an international survey of current treatments and future perspectives. J Reconstr Microsurg 25: 339-344.
3. Alvarez FJ, Titus-Mitchell HE, Bullinger KL, Kraszpulski M, Nardelli P, et al. (2011) Permanent central synaptic disconnection of proprioceptors after nerve injury and regeneration. I. Loss of VGLUT1/IA synapses on motoneurons. J Neurophysiol 106: 2450-2470.
4. Todd AJ, Hughes DI, Polgar E, Nagy GG, Mackie M, et al. (2003) The expression of vesicular glutamate transporters VGLUT1 and VGLUT2 in neurochemically defined axonal populations in the rat spinal cord with emphasis on the dorsal horn. Eur J Neurosci 17: 13-27. (Pubitemid 36104205)
5. Alvarez FJ, Villalba RM, Zerda R, Schneider SP (2004) Vesicular glutamate transporters in the spinal cord, with special reference to sensory primary afferent synapses. J Comp Neurol 472: 257-280. (Pubitemid 38420368)
6. Cope TC, Clark BD (1993) Motor-unit recruitment in self-reinnervated muscle. J Neurophysiol 70: 1787-1796. (Pubitemid 23351021)
7. Sabatier MJ, Redmon N, Schwartz G, English AW (2008) Treadmill training promotes axon regeneration in injured peripheral nerves. Exp Neurol 211: 489-493.
8. Wood K, Wilhelm JC, Sabatier MJ, English AW (2012) Sex differences in the effects of treadmill training on axon regeneration in cut peripheral nerves. Dev Neurobiol 72: 688-698.
9. English AW, Wilhelm JC, Sabatier MJ (2011) Enhancing recovery from peripheral nerve injury using treadmill training. Ann Anat 193: 354-361.
10. Brown T, Khan T, Jones K (1999) Androgen induced acceleration of functional recovery after rat sciatic nerve injury. Restor Neurol Neurosci 15: 289-295. (Pubitemid 30056184)
11. Brown T, Storer P, Oblinger M, Jones K (2001) Androgenic enhancement of betaII-tubulin mRNA in spinal motoneurons following sciatic nerve injury. Restor Neurol Neurosci 18: 191-198. (Pubitemid 34258572)
12. Jones K, Storer P, Drengler S, Oblinger M (1999) Differential regulation of cytoskeletal gene expression in hamster facial motoneurons: effects of axotomy and testosterone treatment. J Neurosci Res 57: 817-823. (Pubitemid 29416111)
13. Fargo KN, Alexander TD, Tanzer L, Poletti A, Jones KJ (2008) Androgen regulates neuritin mRNA levels in an in vivo model of steroid-enhanced peripheral nerve regeneration. J Neurotrauma 25: 561-566. (Pubitemid 351685491)
14. Brown TJ, Pittman AL, Monaco GN, Benscoter BJ, Mantravadi AV, et al. (2013) Androgen treatment and recovery of function following recurrent laryngeal nerve injury in the rat. Restor Neurol Neurosci 31: 169-176.
15. Jones KJ, Durica TE, Jacob SK (1997) Gonadal steroid preservation of central synaptic input to hamster facial motoneurons following peripheral axotomy. J Neurocytol 26: 257-266. (Pubitemid 27261231)
16. Matsumoto A (2005) Testosterone prevents synaptic loss in the perineal motoneuron pool in the spinal cord in male rats exposed to chronic stress. Stress 8: 133-140.
17. Kujawa KA, Tanzer L, Jones KJ (1995) Inhibition of the accelerative effects of testosterone on hamster facial nerve regeneration by the antiandrogen flutamide. Exp Neurol 133: 138-143.
18. Thompson NJ, Sengelaub DR, English AW (2014) Enhancement of peripheral nerve regeneration due to treadmill training and electrical stimulation is dependent on androgen receptor signaling. Dev Neurobiol 74: 531-540.
19. Lenth RV (2006) Java Applets for Power and Sample Size [Computer software]. Retrieved 01/10/2013, from http://www.stat.uiowa.edu/~rlenth/Power.
20. Oliveira A, Thams S, Lidman O, Piehl F, Hökfelt T, et al. (2008) A role for MHC class I molecules in synaptic plasticity and regeneration of neurons after axotomy. Proc Natl Acad Sci U S A 101: 17843-17848.
21. Al-Majed AA, Neumann CM, Brushart TM, Gordon T (2000) Brief electrical stimulation promotes the speed and accuracy of motor axonal regeneration. J Neurosci 20: 2602-2608. (Pubitemid 30220347)
22. Funakoshi H, Frisen J, Barbany G, Timmusk T, Zachrisson O, et al. (1993) Differential expression of mRNAs for neurotrophins and their receptors after axotomy of the sciatic nerve. J Cell Biol 123: 455-465. (Pubitemid 23313968)
23. Griesbeck O, Parsadanian AS, Sendtner M, Thoenen H (1995) Expression of neurotrophins in skeletal muscle: quantitative comparison and significance for motoneuron survival and maintenance of function. J Neurosci Res 42: 21-33.
24. Jones SL, Ismail N, King L, Pfaus JG (2012) The effects of chronic administration of testosterone propionate with or without estradiol on the sexual behavior and plasma steroid levels of aged female rats. Endocrinology 153: 5928-5939.
25. Smith E, Damassa D, Davidson J (1977) Hormone Administration: Peripheral and Intracranial Implants. In: RD M, editor. Methods Psychobiol. New York: Academic Press. pp. 259-279.
26. McLean IW, Nakane PK (1974) Periodate-lysate-paraformaldehyde fixative. A new fixative for immunoelectron microscopy. J Histochem Cytochem 22: 1077-1083.
27. Hughes DI, Mackie M, Nagy GG, Riddell JS, Maxwell DJ, et al. (2005) P boutons in lamina IX of the rodent spinal cord express high levels of glutamic acid decarboxylase-65 and originate from cells in deep medial dorsal horn. Proc Natl Acad Sci U S A 102: 9038-9043. (Pubitemid 40881074)
28. Wang Y, Pillai S, Wolpaw JR, Chen XY (2006) Motor learning changes GABAergic terminals on spinal motoneurons in normal rats. Eur J Neurosci 23: 141-150.
29. Rotterman TM, Nardelli P, Cope TC, Alvarez FJ (2014) Normal distribution of VGLUT1 synapses on spinal motoneuron dendrites and their reorganization after nerve injury. J Neurosci 34: 3475-3492.
30. De Bono JP, Adlam D, Paterson DJ, Channon KM (2006) Novel quantitative phenotypes of exercise training in mouse models. Am J Physiol Regul Integr Comp Physiol 290: R926-934.
31. Hoke A (2013) Experimental neurology and state of preclinical research. Exp Neurol 239: A1.
32. Udina E, Puigdemasa A, Navarro X (2011) Passive and active exercise improve regeneration and muscle reinnervation after peripheral nerve injury in the rat. Muscle & Nerve 43: 500-509.
33. Blinzinger K, Kreutzberg G (1968) Displacement of synaptic terminals from regenerating motoneurons by microglial cells. Z Zellforsch 85: 145-157.
34. Graeber M, Kreutzberg G (1986) Astrocytes increase in glial fibrillary acidic protein during retrograde changes of facial motor neurons. J Neurocytol 15: 363-373. (Pubitemid 16065168)
35. Aldskogius H, Liu L, Svensson M (1999) Glial responses to synaptic damage and plasticity. J Neurosci Res 58: 33-41. (Pubitemid 29463691)
36. Zelano J, Berg A, Thams S, Hailer NP, Cullheim S (2009) SynCAM1 expression correlates with restoration of central synapses on spinal motoneurons after two different models of peripheral nerve injury. J Comp Neurol 517: 670-682.
37. Perry VH, O'Connor V (2010) The role of microglia in synaptic stripping and synaptic degeneration: a revised perspective. ASN Neuro 2: e00047.
38. Berg A, Zelano J, Thams S, Cullheim S (2013) The extent of synaptic stripping of motoneurons after axotomy is not correlated to activation of surrounding glia or downregulation of postsynaptic adhesion molecules. PLoS ONE 8: e59647.
39. Oliveira AL, Thams S, Lidman O, Piehl F, Hokfelt T, et al. (2004) A role for MHC class I molecules in synaptic plasticity and regeneration of neurons after axotomy. Proc Natl Acad Sci U S A 101: 17843-17848. (Pubitemid 40051974)
40. Berg A, Zelano J, Stephan A, Thams S, Barres BA, et al. (2012) Reduced removal of synaptic terminals from axotomized spinal motoneurons in the absence of complement C3. Exp Neurol 237: 8-17.
41. Thams S, Oliveira A, Cullheim S (2008) MHC class I expression and synaptic plasticity after nerve lesion. Brain Res Rev 57: 265-269. (Pubitemid 350218165)
42. Moreno-Lopez B, Sunico CR, Gonzalez-Forero D (2011) NO orchestrates the loss of synaptic boutons from adult "sick" motoneurons: modeling a molecular mechanism. Mol Neurobiol 43: 41-66.
43. Jovanovic JN, Benfenati F, Siow YL, Sihra TS, Sanghera JS, et al. (1996) Neurotrophins stimulate phosphorylation of synapsin I by MAP kinase and regulate synapsin I-actin interactions. Proc Natl Acad Sci U S A 93: 3679-3683. (Pubitemid 26127596)
44. Sunico CR, Portillo F, Gonzalez-Forero D, Moreno-Lopez B (2005) Nitric-oxide-directed synaptic remodeling in the adult mammal CNS. J Neurosci 25: 1448-1458. (Pubitemid 40250721)
45. Sunico CR, Gonzalez-Forero D, Dominguez G, Garcia-Verdugo JM, Moreno-Lopez B (2010) Nitric oxide induces pathological synapse loss by a protein kinase G-, Rho kinase-dependent mechanism preceded by myosin light chain phosphorylation. J Neurosci 30: 973-984.
46. Montero F, Sunico CR, Liu B, Paton JF, Kasparov S, et al. (2010) Transgenic neuronal nitric oxide synthase expression induces axotomy-like changes in adult motoneurons. J Physiol 588: 3425-3443.
47. Wilhelm JC, Cucoranu D, Xu M, Chmielewski S, Holmes T, et al. (2012) Cooperative roles of BDNF expression in neurons and Schwann cells are modulated by exercise to facilitate nerve regeneration. J Neurosci 32: 5002-5009.
48. Krakowiak JR, Wilhelm JC, English AW (2010) Effect of treadmill training on synaptic stripping of axotomized mouse motoneurons. Abstr Soc Neurosci.
49. Gordon T (2009) The role of neurotrophic factors in nerve regeneration. Neurosurg Focus 26: E3.
50. Davis-Lopez de Carrizosa M, Morado-Diaz C, Tena J, Benitez-Temino B, Pecero M, et al. (2009) Complimentary actions of BDNF and Neurotrophin-3 on the firing patterns and synaptic composition of motoneurons. J Neurosci 29: 575-587.
51. Gomez-Pinilla F, Ying Z, Opazo P, Roy RR, Edgerton VR (2001) Differential regulation by exercise of BDNF and NT-3 in rat spinal cord and skeletal muscle. Eur J Neurosci 13: 1078-1084. (Pubitemid 32275744)
52. Hong EJ, McCord AE, Greenberg ME (2008) A biological function for the neuronal activity-dependent component of Bdnf transcription in the development of cortical inhibition. Neuron 60: 610-624.
53. Gomez-Pinilla F, Ying Z, Roy RR, Molteni R, Edgerton VR (2002) Voluntary exercise induces a BDNF-mediated mechanism that promotes neuroplasticity. J Neurophysiol 88: 2187-2195. (Pubitemid 35346024)
54. Sharma N, Marzo SJ, Jones KJ, Foecking EM (2010) Electrical stimulation and testosterone differentially enhance expression of regeneration-associated genes. Exp Neurol 223: 183-191.
55. Kujawa KA, Kinderman NB, Jones KJ (1989) Testosterone-induced acceleration of recovery from facial paralysis following crush axotomy of the facial nerve in male hamsters. Exp Neurol 105: 80-85. (Pubitemid 19198880)
56. Turgeon JL, Carr MC, Maki PM, Mendelsohn ME, Wise PM (2006) Complex actions of sex steroids in adipose tissue, the cardiovascular system, and brain: Insights from basic science and clinical studies. Endocrine Rev 27: 575-605. (Pubitemid 44582052)
57. Coirini H, Gouezou M, Liere P, Delespierre B, Pianos A, et al. (2002) 3 Beta-hydroxysteroid dehydrogenase expression in rat spinal cord. Neuroscience 113: 883-891. (Pubitemid 35245257)
58. Rakotoarivelo C, Petite D, Lambard S, Fabre C, Rouleau C, et al. (2004) Receptors to steroid hormones and aromatase are expressed by cultured motoneurons but not by glial cells derived from rat embryo spinal cord. Neuroendocrinology 80: 284-297. (Pubitemid 40470237)
59. Gottfried-Blackmore A, Sierra A, Jellinck PH, McEwen BS, Bulloch K (2008) Brain microglia express steroid-converting enzymes in the mouse. J Steroid Biochem 109: 96-107.
60. Garcia-Ovejero D, Azcoitia I, Doncarlos LL, Melcangi RC, Garcia-Segura LM (2005) Glia-neuron crosstalk in the neuroprotective mechanisms of sex steroid hormones. Brain Res Brain Res Rev 48: 273-286. (Pubitemid 40585759)
61. Saldanha CJ, Duncan KA, Walters BJ (2009) Neuroprotective actions of brain aromatase. Front Neuroendocrin 30: 106-118.
62. Patte-Mensah C, Penning TM, Mensah-Nyagan AG (2004) Anatomical and cellular localization of neuroactive 5 alpha/3 alpha-reduced steroid-synthesizing enzymes in the spinal cord. J Comp Neurol 477: 286-299. (Pubitemid 39136235)
63. Aizawa K, Iemitsu M, Otsuki T, Maeda S, Miyauchi T, et al. (2008) Sex differences in steroidogenesis in skeletal muscle following a single bout of exercise in rats. J Appl Physiol 104: 67-74.