Disease progression in a mouse model of amyotrophic lateral sclerosis: The influence of chronic stress and corticosterone

FASEB Journal

Volumn 25, Issue 12, 2011, Pages 4369-4377

  Fidler, Jonathan A ^a   Treleaven, Christopher M ^a   Frakes, Ashley ^b,c   Tamsett, Thomas J ^a   McCrate, Mary ^b,c   Cheng, Seng H ^a   Shihabuddin, Lamya S ^a   Kaspar, Brian K ^b,c   Dodge, James C ^a  

^a GENZYME CORPORATION   (United States)

^b NATIONWIDE CHILDREN S HOSPITAL   (United States)

^c THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Allostasis; ALS; Cacostasis; Glucocorticoid; MND; Motor neuron disease

Indexed keywords

CORTICOSTERONE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTOSIS; CELL ACTIVATION; CHRONIC STRESS; CIRCADIAN RHYTHM; CONTROLLED STUDY; DISEASE COURSE; FEMALE; HORMONE BLOOD LEVEL; MICROGLIA; MOUSE; MUSCLE WEAKNESS; NONHUMAN; PRIORITY JOURNAL; SURVIVAL RATE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; CORTICOSTERONE; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FEMALE; HUMANS; MALE; MICE; MICE, MUTANT STRAINS; MICE, TRANSGENIC; MODELS, BIOLOGICAL; MUTANT PROTEINS; RESTRAINT, PHYSICAL; STRESS, PHYSIOLOGICAL; SUPEROXIDE DISMUTASE;

EID: 82655173728     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-190819     Document Type: Article

References (56)

1. Czaplinski, A., Yen, A. A., Simpson, E. P., and Appel, S. H. (2006) Slower disease progression and prolonged survival in contemporary patients with amyotrophic lateral sclerosis: is the natural history of amyotrophic lateral sclerosis changing? Arch. Neurol. 63, 1139-1143 (Pubitemid 44232321)
2. Hunter, M. D., Robinson, I. C., and Neilson, S. (1993) The functional and psychological status of patients with amyotrophic lateral sclerosis: some implications for rehabilitation. Disabil. Rehabil. 15, 119-126 (Pubitemid 23243660)
3. McDonald, E. R., Wiedenfeld, S. A., Hillel, A., Carpenter, C. L., and Walter, R. A. (1994) Survival in amyotrophic lateral sclerosis. The role of psychological factors. Arch. Neurol. 51, 17-23 (Pubitemid 24020167)
4. Chio, A., Benzi, G., Dossena, M., Mutani, R., and Mora, G. (2005) Severely increased risk of amyotrophic lateral sclerosis among Italian professional football players. Brain 128, 472-476 (Pubitemid 40380183)
5. Weisskopf, M. G., O'Reilly, E. J., McCullough, M. L., Calle, E. E., Thun, M. J., Cudkowicz, M., and Ascherio, A. (2005) Prospective study of military service and mortality from ALS. Neurology 64, 32-37 (Pubitemid 40082933)
6. Chrousos, G. P. (2009) Stress and disorders of the stress system. Nat. Rev. Endocrinol. 5, 374-381
7. McEwen, B. S. (1998) Stress, adaptation, and disease. Allostasis and allostatic load. Ann. N. Y. Acad. Sci. 840, 33-44
8. Sapolsky, R. M. (2000) Stress hormones: good and bad. Neurobiol. Dis. 7, 540-542
9. Charmandari, E., Tsigos, C., and Chrousos, G. (2005) Endocrinology of the stress response. Annu. Rev. Physiol. 67, 259-284 (Pubitemid 40409509)
10. Sapolsky, R. M., Krey, L. C., and McEwen, B. S. (1986) The neuroendocrinology of stress and aging: the glucocorticoid cascade hypothesis. Endocr. Rev. 7, 284-301
11. Patacchioli, F. R., Monnazzi, P., Scontrini, A., Tremante, E., Caridi, I., Brunetti, E., Buttarelli, F. R., and Pontieri, F. E. (2003) Adrenal dysregulation in amyotrophic lateral sclerosis. J. Endocrinol. Invest. 26, RC23-RC25 (Pubitemid 38324729)
12. Ziegler, M. G., Brooks, B. R., Lake, C. R., Wood, J. H., and Enna, S. J. (1980) Norepinephrine and gamma-aminobutyric acid in amyotrophic lateral sclerosis. Neurology 30, 98-101 (Pubitemid 10160225)
13. Bertel, O., Malessa, S., Sluga, E., and Hornykiewicz, O. (1991) Amyotrophic lateral sclerosis: changes of noradrenergic and serotonergic transmitter systems in the spinal cord. Brain Res. 566, 54-60
14. Ohno, T., Shimizu, T., Kato, S., Hayashi, H., and Hirai, S. (2001) Effect of tamsulosin hydrochloride on sympathetic hyperactivity in amyotrophic lateral sclerosis. Auton. Neurosci. 88, 94-98 (Pubitemid 32273493)
15. Bouteloup, C., Desport, J. C., Clavelou, P., Guy, N., Derumeaux-Burel, H., Ferrier, A., and Couratier, P. (2009) Hypermetabolism in ALS patients: an early and persistent phenomenon. J. Neurol. 256, 1236-1242
16. Pradat, P. F., Bruneteau, G., Gordon, P. H., Dupuis, L., Bonnefont-Rousselot, D., Simon, D., Salachas, F., Corcia, P., Frochot, V., Lacorte, J. M., Jardel, C., Coussieu, C., Forestier, N. L., Lacomblez, L., Loeffler, J. P., and Meininger, V. (2009) Impaired glucose tolerance in patients with amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. 11, 166-171
17. Morselli, L. L., Bongioanni, P., Genovesi, M., Licitra, R., Rossi, B., Murri, L., Rossi, G., Martino, E., and Gasperi, M. (2006) Growth hormone secretion is impaired in amyotrophic lateral sclerosis. Clin. Endocrinol. (Oxf.) 65, 385-388
18. Wilczak, N., de Vos, R. A., and De Keyser, J. (2003) Free insulin-like growth factor (IGF)-I and IGF binding proteins 2, 5, and 6 in spinal motor neurons in amyotrophic lateral sclerosis. Lancet 361, 1007-1011 (Pubitemid 36355935)
19. Sato, Y., Honda, Y., Asoh, T., Kikuyama, M., and Oizumi, K. (1997) Hypovitaminosis D and decreased bone mineral density in amyotrophic lateral sclerosis. Eur. Neurol. 37, 225-229 (Pubitemid 27212030)
20. Toepfer, M., Folwaczny, C., Klauser, A., Riepl, R. L., Muller-Felber, W., and Pongratz, D. (1999) Gastrointestinal dysfunction in amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. Other Motor Neuron Disord. 1, 15-19
21. Kimura, K., Tachibana, N., Kimura, J., and Shibasaki, H. (1999) Sleep-disordered breathing at an early stage of amyotrophic lateral sclerosis. J. Neurol. Sci. 164, 37-43 (Pubitemid 29256071)
22. Vignola, A., Guzzo, A., Calvo, A., Moglia, C., Pessia, A., Cavallo, E., Cammarosano, S., Giacone, S., Ghiglione, P., and Chio, A. (2008) Anxiety undermines quality of life in ALS patients and caregivers. Eur. J. Neurol. 15, 1231-1236
23. McElhiney, M. C., Rabkin, J. G., Gordon, P. H., Goetz, R., and Mitsumoto, H. (2009) Prevalence of fatigue and depression in ALS patients and change over time. J. Neurol. Neurosurg. Psychiatry 80, 1146-1149
24. Wheaton, M. W., Salamone, A. R., Mosnik, D. M., McDonald, R. O., Appel, S. H., Schmolck, H. I., Ringholz, G. M., and Schulz, P. E. (2007) Cognitive impairment in familial ALS. Neurology 69, 1411-1417 (Pubitemid 47511462)
25. Rosen, D. R. (1993) Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 364, 362
26. Gurney, M. E., Pu, H., Chiu, A. Y., Dal Canto, M. C., Polchow, C. Y., Alexander, D. D., Caliendo, J., Hentati, A., Kwon, Y. W., Deng, H. X., Deng, H. X., Chen, W., Zhai, P., Sufit, R. L., and Siddique, T. (1994) Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 264, 1772-1775 (Pubitemid 24227760)
27. Kim, K. S., and Han, P. L. (2006) Optimization of chronic stress paradigms using anxiety- and depression-like behavioral parameters. J. Neurosci. Res. 83, 497-507
28. Dodge, J. C., Haidet, A. M., Yang, W., Passini, M. A., Hester, M., Clarke, J., Roskelley, E. M., Treleaven, C. M., Rizo, L., Martin, H., Kim, S. H., Kaspar, R., Taksir, T. V., Griffiths, D. A., Cheng, S. H., Shihabuddin, L. S., and Kaspar, B. K. (2008) Delivery of AAV-IGF-1 to the CNS extends survival in ALS mice through modification of aberrant glial cell activity. Mol. Ther. 16, 1056-1064 (Pubitemid 351737070)
29. Dodge, J. C., Treleaven, C. M., Fidler, J. A., Hester, M., Haidet, A., Handy, C., Rao, M., Eagle, A., Matthews, J. C., Taksir, T. V., Cheng, S. H., Shihabuddin, L. S., and Kaspar, B. K. (2010) AAV4-mediated expression of IGF-1 and VEGF within cellular components of the ventricular system improves survival outcome in familial ALS mice. Mol. Ther. 18, 2075-2084
30. Ray, J., and Gage, F. H. (2006) Differential properties of adult rat and mouse brain-derived neural stem/progenitor cells. Mol. Cell. Neurosci. 31, 560-573 (Pubitemid 43358027)
31. Bruijn, L. I., Miller, T. M., and Cleveland, D. W. (2004) Unraveling the mechanisms involved in motor neuron degeneration in ALS. Annu. Rev. Neurosci. 27, 723-749 (Pubitemid 39050419)
32. Magnus, T., Carmen, J., Deleon, J., Xue, H., Pardo, A. C., Lepore, A. C., Mattson, M. P., Rao, M. S., and Maragakis, N. J. (2008) Adult glial precursor proliferation in mutant SOD1G93A mice. Glia 56, 200-208 (Pubitemid 350292312)
33. Raps, D., Barthe, P. L., and Desaulles, P. A. (1971) Plasma and adrenal corticosterone levels during the different phases of the sexual cycle in normal female rats. Experientia 27, 339-340
34. Esposito, P., Gheorghe, D., Kandere, K., Pang, X., Connolly, R., Jacobson, S., and Theoharides, T. C. (2001) Acute stress increases permeability of the blood-brain-barrier through activation of brain mast cells. Brain Res. 888, 117-127 (Pubitemid 32056268)
35. Garbuzova-Davis, S., Haller, E., Saporta, S., Kolomey, I., Nicosia, S. V., and Sanberg, P. R. (2007) Ultrastructure of blood-brain barrier and blood-spinal cord barrier in SOD1 mice modeling ALS. Brain Res. 1157, 126-137 (Pubitemid 46935078)
36. Zhong, Z., Deane, R., Ali, Z., Parisi, M., Shapovalov, Y., O'Banion, M. K., Stojanovic, K., Sagare, A., Boillee, S., Cleveland, D. W., and Zlokovic, B. V. (2008) ALS-causing SOD1 mutants generate vascular changes prior to motor neuron degeneration. Nat. Neurosci. 11, 420-422 (Pubitemid 351441888)
37. Kaufer, D., Friedman, A., Seidman, S., and Soreq, H. (1998) Acute stress facilitates long-lasting changes in cholinergic gene expression. Nature 393, 373-377 (Pubitemid 28269711)
38. Tateno, M., Kato, S., Sakurai, T., Nukina, N., Takahashi, R., and Araki, T. (2009) Mutant SOD1 impairs axonal transport of choline acetyltransferase and acetylcholine release by sequestering KAP3. Hum. Mol. Genet. 18, 942-955
39. Nagao, M., Misawa, H., Kato, S., and Hirai, S. (1998) Loss of cholinergic synapses on the spinal motor neurons of amyotrophic lateral sclerosis. J. Neuropathol. Exp. Neurol. 57, 329-333 (Pubitemid 28182630)
40. Gonzalez Deniselle, M. C., Gonzalez, S., Piroli, G., Ferrini, M., Lima, A. E., and De Nicola, A. F. (1997) Glucocorticoid receptors and actions in the spinal cord of the Wobbler mouse, a model for neurodegenerative diseases. J. Steroid Biochem. Mol. Biol. 60, 205-213 (Pubitemid 27229775)
41. Dupuis, L., Oudart, H., Rene, F., Gonzalez de Aguilar, J. L., and Loeffler, J. P. (2004) Evidence for defective energy homeostasis in amyotrophic lateral sclerosis: benefit of a high-energy diet in a transgenic mouse model. Proc. Natl. Acad. Sci. U. S. A. 101, 11159-11164 (Pubitemid 38989600)
42. Mastorakos, G., Pavlatou, M., Diamanti-Kandarakis, E., and Chrousos, G. P. (2005) Exercise and the stress system. Hormones (Athens) 4, 73-89
43. Paccotti, P., Minetto, M., Terzolo, M., Ventura, M., Ganzit, G. P., Borrione, P., Termine, A., and Angeli, A. (2005) Effects of high-intensity isokinetic exercise on salivary cortisol in athletes with different training schedules: relationships to serum cortisol and lactate. Int. J. Sports Med. 26, 747-755 (Pubitemid 41658609)
44. O'Connor, P. J., Morgan, W. P., Raglin, J. S., Barksdale, C. M., and Kalin, N. H. (1989) Mood state and salivary cortisol levels following overtraining in female swimmers. Psychoneuroendocrinology 14, 303-310 (Pubitemid 19248226)
45. Kraemer, W. J., Fry, A. C., Warren, B. J., Stone, M. H., Fleck, S. J., Kearney, J. T., Conroy, B. P., Maresh, C. M., Weseman, C. A., Triplett, N. T., and Gordon, S. E. (1992) Acute hormonal responses in elite junior weightlifters. Int. J. Sports Med. 13, 103-109
46. Kraemer, W. J., Patton, J. F., Gordon, S. E., Harman, E. A., Deschenes, M. R., Reynolds, K., Newton, R. U., Triplett, N. T., and Dziados, J. E. (1995) Compatibility of high-intensity strength and endurance training on hormonal and skeletal muscle adaptations. J. Appl. Physiol. 78, 976-989
47. Iellamo, F., Pigozzi, F., Parisi, A., Di Salvo, V., Vago, T., Norbiato, G., Lucini, D., and Pagani, M. (2003) The stress of competition dissociates neural and cortisol homeostasis in elite athletes. J. Sports Med. Phys. Fitness 43, 539-545 (Pubitemid 38220367)
48. Perna, F. M., and McDowell, S. L. (1995) Role of psychological stress in cortisol recovery from exhaustive exercise among elite athletes. Int. J. Behav. Med. 2, 13-26
49. Tanskanen, M. M., Kyrolainen, H., Uusitalo, A. L., Huovinen, J., Nissila, J., Kinnunen, H., Atalay, M., and Hakkinen, K. (2011) Serum sex hormone-binding globulin and cortisol concentrations are associated with overreaching during strenuous military training. J. Strength Cond. Res. 25, 787-797
50. Morgan, C. A., 3rd, Wang, S., Mason, J., Southwick, S. M., Fox, P., Hazlett, G., Charney, D. S., and Greenfield, G. (2000) Hormone profiles in humans experiencing military survival training. Biol. Psychiatry 47, 891-901 (Pubitemid 30243177)
51. Nelson, J. F., Karelus, K., Bergman, M. D., and Felicio, L. S. (1995) Neuroendocrine involvement in aging: evidence from studies of reproductive aging and caloric restriction. Neurobiol Aging 16, 837-843; discussion 855-836
52. Hamadeh, M. J., Rodriguez, M. C., Kaczor, J. J., and Tarnopolsky, M. A. (2005) Caloric restriction transiently improves motor performance but hastens clinical onset of disease in the Cu/Zn-superoxide dismutase mutant G93A mouse. Muscle Nerve 31, 214-220 (Pubitemid 40189843)
53. Patel, B. P., Safdar, A., Raha, S., Tarnopolsky, M. A., and Hamadeh, M. J. (2010) Caloric restriction shortens lifespan through an increase in lipid peroxidation, inflammation and apoptosis in the G93A mouse, an animal model of ALS. PLoS One 5, e9386
54. Sorrells, S. F., and Sapolsky, R. M. (2007) An inflammatory review of glucocorticoid actions in the CNS. Brain Behav. Immun. 21, 259-272 (Pubitemid 46199119)
55. Yang, W. W., Sidman, R. L., Taksir, T. V., Treleaven, C. M., Fidler, J. A., Cheng, S. H., Dodge, J. C., and Shihabuddin, L. S. (2011) Relationship between neuropathology and disease progression in the SOD1(G93A) ALS mouse. Exp. Neurol. 227, 287-295
56. Dumas, T. C., Gillette, T., Ferguson, D., Hamilton, K., and Sapolsky, R. M. (2010) Anti-glucocorticoid gene therapy reverses the impairing effects of elevated corticosterone on spatial memory, hippocampal neuronal excitability, and synaptic plasticity. J. Neurosci. 30, 1712-1720