Effects of Bax gene deletion on muscle and motoneuron degeneration in a sexually dimorphic neuromuscular system

Journal of Neuroscience

Volumn 25, Issue 23, 2005, Pages 5638-5644

  Jacob, Dena A ^a   Bengston, C Lynn ^a   Forger, Nancy G ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

Androgen; Bax; Levator ani; Motoneuron; Neuromuscular; Sex difference; Spinal nucleus of the bulbocavernosus (SNB)

Indexed keywords

FLUORESCENT DYE; PROTEIN BAX;

ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; CELL COUNT; CELL SUBPOPULATION; CONTROLLED STUDY; FEMALE; GENE DELETION; GENE DISRUPTION; LEVATOR ANI MUSCLE; MOUSE; MUSCLE ATROPHY; NERVE CELL NECROSIS; NERVE DEGENERATION; NERVE FIBER; NEUROMUSCULAR SYSTEM; NONHUMAN; PRIORITY JOURNAL; SEX DIFFERENCE;

ANIMALS; ANTIBODIES, MONOCLONAL; BCL-2-ASSOCIATED X PROTEIN; CELL COUNT; CELL DEATH; CELL SIZE; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR NEURONS; MUSCLE, SKELETAL; NERVE DEGENERATION; SEX CHARACTERISTICS; SPINAL CORD;

EID: 20444402211     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1200-05.2005     Document Type: Article

References (45)

1. Adams JM, Cory S (2001) Life-or-death decisions by the Bcl-2 protein family. Trends Biochem Sci 26:61-66.
2. Arai Y, Sekine Y, Murakami S (1996) Estrogen and apoptosis in the developing sexually dimorphic preoptic area in female rats. Neurosci Res 25:403-407.
3. Bar-Peled O, Knudson M, Korsmeyer SJ, Rothstein JD (1999) Motor neuron degeneration is attenuated in bax-defident neurons in vitro. J Neurosci Res 55:542-556.
4. Breedlove SM, Arnold AP (1981) Sexually dimorphic motor nucleus in the rat lumbar spinal cord: response to adult hormone manipulation, absence in androgen-insensitive rats. Brain Res 225:297-307.
5. Breedlove SM, Arnold AP (1983) Hormonal control of a developing neuromuscular system. I. Complete demasculinization of the male rat spinal nucleus of the bulbocavernosus using the anti-androgen flutamide. J Neurosci 3:417-423.
6. Cihak R, Gutmann E, Hanzlikova V (1970) Involution and hormone-induced persistence of the M. sphincter (levator) ani in female rats. J Anat 106:93-110.
7. Deckwerth TL, Elliott JL, Knudson CM, Johnson Jr EM, Snider WD, Korsmeyer SJ (1996) BAX is required for neuronal death after trophic factor deprivation and during development. Neuron 17:401-411.
8. Dominov JA, Houlihan-Kawamoto A, Swap CJ, Miller JB (2001) Pro- and anti-apoptotic members of the Bcl-2 family in skeletal muscle: a distinct role for Bcl-2 in later stages of myogenesis. Dev Dyn 220:18-26.
9. Forger NG, Breedlove SM (1986) Sexual dimorphism in human and canine spinal cord: role of early androgen. Proc Natl Acad Sci USA 83:7527-7531.
10. Forger NG, Roberts SL, Wong V, Breedlove SM (1993) Ciliary neurotrophic factor maintains motoneurons and their target muscles in developing rats. J Neurosci 13:4720-4726.
11. Forger NG, Frank LG, Breedlove SM, Glickman SE (1996) Sexual dimorphism of perineal muscles and motoneurons in spotted hyenas. J Comp Neurol 375:333-343.
12. Forger NG, Howell ML, Bengston L, MacKenzie L, DeChiara TM, Yancopoulos GD (1997) Sexual dimorphism in the spinal cord is absent in mice lacking the ciliary neurotrophic factor receptor. J Neurosci 15:9605-9612.
13. Forger NG, Rosen GJ, Waters EM, Jacob D, Simerly RB, De Vries GJ (2004) Deletion of Bax eliminates sex differences in the mouse forebrain. Proc Natl Acad Sci USA 101:13666-13671.
14. Freeman LM, Watson NV, Breedlove SM (1996) Androgen spares androgen-insensitive motoneurons from apoptosis in the spinal nucleus of the bulbocavernosus in rats. Horm Behav 30:424-433.
15. Girgenrath M, Dominov JA, Kostek CA, Miller JB (2004) Inhibition of apoptosis improves outcome in a model of congenital muscular dystrophy. J Clin Invest 114:1635-1639.
16. Grieshammer U, Lewandoski M, Prevette D, Oppenheim RW, Martin GR (1998) Muscle-specific cell ablation conditional upon Cre-mediated DNA recombination in transgenic mice leads to massive spinal and cranial motoneuron loss. Dev Biol 197:234-247.
17. Hamson DK, Hu JH, Krieger C, Watson NV (2002) Lumbar motoneuron fate in a mouse model of amyotrophic lateral sclerosis. NeuroReport 13:2291-2294.
18. Hollyday M, Hamburger V (1976) Reduction of the naturally occurring motoneuron loss by enlargement of the periphery. J Comp Neurol 170:311-320.
19. Jordan CL, Breedlove SM, Arnold AP (1982) Sexual dimorphism and the influence of neonatal androgen in the dorsolateral motor nucleus of the rat lumbar spinal cord. Brain Res 249:309-314.
20. Joubert Y, Tobin C (1989) Satellite cell proliferation and increase in the number of myonuclei induced by testosterone in the levator ani muscle of the adult female rat. Dev Biol 131:550-557.
21. Knudson CM, Tung KS, Tourtellotte WG, Brown GA, Korsmeyer SJ (1995) Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 270:96-99.
22. Lindsten T, Ross AJ, King A, Zong W-X, Rathmell JC, Shiels HA, Ulrich E, Waymire KG, Mhar P, Frauwirth K, Chen Y, Wei M, Eng VM, Adelman DM, Simon MC, Ma A, Golden JA, Evan G, Korsmeyer SJ, MacGregor GR, et al. (2000) The combined functions of proapoptotic Bcl-2 family members Bak and Bax are essential for normal development of multiple tissues. Mol Cell 6:1389-1399.
23. Mannen T, Iwata M, Toyokura Y, Nagashima K (1982) The Onuf's nucleus and the external anal sphincter muscles in amyotrophic lateral sclerosis and Shy-Drager's syndrome. Acta Neuropathol 58:255-260.
24. McKenna KE, Nadelhaft I (1986) The organization of the pudendal nerve in the male and female rat. J Comp Neurol 248:532-549.
25. Merry DE, Korsmeyer SJ (1997) Bcl-2 gene family in the nervous system. Annu Rev Neurosci 20:245-267.
26. Nicolopoulos-Stournaras S, Iles JF (1983) Motor neuron columns in the lumbar spinal cord of the rat. J Comp Neurol 217:75-85.
27. Nordeen EJ, Nordeen KW, Sengelaub DR, Arnold AP (1985) Androgens prevent normally occurring cell death in a sexually dimorphic spinal nucleus. Science 229:671-673.
28. ARF, or p53 and is accelerated by inactivation of Bax. BMC Cell Biol 5:1-14.
29. Oppenheim RW (1991) Cell death during development of the nervous system. Annu Rev Neurosci 14:453-501.
30. Park JJ, Howell M, Winseck A, Forger NG (1999) Effects of testosterone on the development of a sexually dimorphic neuromuscular system in ciliary neurotrophic factor receptor knockout mice. J Neurobiol 41:317-325.
31. Schroder HD (1980) Organization of the motoneurons innervating the pelvic muscles of the male rats. J Comp Neurol 192:567-587.
32. Siegford JM, Hadi Mansouri S, Ulibarri C (2003) Normal ontogeny of perineal muscles and testosterone levels in Mongolian gerbils; response to testosterone in developing females. Anat Rec 275A:997-1008.
33. Simerly RB, Zee MC, Pendleton JW, Lubahn DB, Korach KS (1997) Estrogen receptor-dependent sexual differentiation of dopaminergic neurons in the preoptic region of the mouse. Proc Natl Acad Sci USA 94:14077-14082.
34. Sun W, Oppenheim RW (2003) Response of motoneurons to neonatal sciatic nerve axotomy in Bax-knockout mice. Mol Cell Neurosci 24:875-876.
35. Sun W, Gould TW, Vinsant S, Prevette D, Oppenheim RW (2003) Neuromuscular development after the prevention of naturally occurring neuronal death by Bax deletion. J Neurosci 23:7298-7310.
36. Sun YF, Yu LY, Saarma M, Timmusk T, Arumae U (2001) Neuron-specific Bcl-2 homology 3 domain-only splice variant of Bak is anti-apoptotic in neurons, but pro-apoptotic in non-neuronal cells. J Biol Chem 276:16240-16247.
37. Tobin C, Joubert Y (1988) The levator ani of the female rat: a suitable model for studying the effects of testosterone on the development of mammalian muscles. Biol Struct Morphog 1:28-33.
38. Uo T, Kinoshita Y, Morrison RS (2004) Neurons exclusively express N-BAK, a BH3 domain-only BAK isoform that promotes neuronal apoptosis. J Biol Chem 280:9065-9073.
39. Venable JH (1966) Constant cell populations in normal, testosterone-deprived and testosterone-stimulated levator ani muscles. Am J Anat 119:263-270.
40. Wagner CK, Clemens LG (1989) Perinatal modification of a sexually dimorphic motor nucleus in the spinal cord of the B6D2F1 house mouse. Physiol Behav 45:831-835.
41. Wainman P, Shipounoff GC (1941) The effects of castration and testosterone propionate on the striated perineal musculature in the rat. Endocrinology 29:975-978.
42. Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, Ross AJ, Roth KA, MacGregor GR, Thompson CB, Korsmeyer SJ (2001) Pro-apoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction. Science 292:727-730.
43. White FA, Keller-Peck CR, Knudson CM, Korsmeyer SJ, Snider WD (1998) Widespread elimination of naturally occurring neuronal death in Bax-deficient mice. J Neurosci 18:1428-1439.
44. Xu J, Gingras KM, Bengston CL, DiMarco A, Forger NG (2001) Blockade of endogenous neurotrophic factors prevents the androgenic rescue of rat spinal motoneurons. J Neurosci 21:4366-4372.
45. Zup SL, Carrier H, Waters EM, Tabor A, Bengston L, Rosen GJ, Simerly RB, Forger NG (2003) Overexpression of Bcl-2 reduces sex differences in neuron number in the brain and spinal cord. J Neurosci 23:2357-2362.