Molecular architecture of myelinated peripheral nerves is supported by calorie restriction with aging

Aging Cell

Volumn 8, Issue 2, 2009, Pages 178-191

  Rangaraju, Sunitha ^a   Hankins, David ^a   Madorsky, Irina ^a   Madorsky, Evgenia ^a   Lee, Wei Hua ^a   Carter, Christy S ^b   Leeuwenburgh, Christiaan ^b   Notterpek, Lucia ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

Autophagy; Chaperones; Heat shock protein; Myelin; Peripheral nerve; Schwann cell

Indexed keywords

HEAT SHOCK PROTEIN; MYELIN PROTEIN;

AGING; ANIMAL CELL; ARTICLE; AUTOPHAGY; CALORIC RESTRICTION; CELL DIFFERENTIATION; CELL FUNCTION; CELL ISOLATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; GLIA CELL; HOMEOSTASIS; IN VIVO STUDY; LYSOSOME; MALE; MYELINATION; NONHUMAN; PERIPHERAL NERVE; PERIPHERAL NERVOUS SYSTEM; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RANVIER NODE; RAT; SCHWANN CELL; SCIATIC NERVE;

AGING; ANIMALS; ANIMALS, NEWBORN; AUTOPHAGY; CALORIC RESTRICTION; CELL DIFFERENTIATION; CELLS, CULTURED; FOOD DEPRIVATION; MALE; MOLECULAR CHAPERONES; MYELIN PROTEINS; MYELIN SHEATH; PERIPHERAL NERVES; PERIPHERAL NERVOUS SYSTEM DISEASES; RATS; RATS, INBRED F344; SCHWANN CELLS;

ANIMALIA; RATTUS;

EID: 63549138319     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/j.1474-9726.2009.00460.x     Document Type: Article

References (81)

1. Adinolfi AM, Yamuy J, Morales FR, Chase MH (1991) Segmental demyelination in peripheral nerves of old cats. Neurobiol. Aging. 12, 175-179.
2. Amici SA, Dunn WA Jr, Notterpek L (2007) Developmental abnormalities in the nerves of peripheral myelin protein 22-deficient mice. J. Neurosci. Res. 85, 238-249.
3. Aquino DA, Lopez C, Farooq M (1996) Antisense oligonucleotide to the 70-kDa heat shock cognate protein inhibits synthesis of myelin basic protein. Neurochem. Res. 21, 417-422.
4. + inactivation. Eur. Biophys. J. 25, 189-200.
5. Bergamini E, Cavallini G, Donati A, Gori Z (2003) The anti-ageing effects of caloric restriction may involve stimulation of macroautophagy and lysosomal degradation, and can be intensified pharmacologically. Biomed. Pharmacother. 57, 203-208.
6. Bergamini E, Cavallini G, Donati A, Gori Z (2004) The role of macroautophagy in the ageing process, anti-ageing intervention and age-associated diseases. Int. J. Biochem. Cell Biol. 36, 2392-2404.
7. Blommaart EF, Luiken JJ, Blommaart PJ, van Woerkom GM, Meijer AJ (1995) Phosphorylation of ribosomal protein S6 is inhibitory for autophagy in isolated rat hepatocytes. J. Biol. Chem. 270, 2320-2326.
8. Boulton M, Rozanowska M, Rozanowski B, Wess T (2004) The photoreactivity of ocular lipofuscin. Photochem. Photobiol. Sci. 3, 759-764.
9. Byun Y, Chen F, Chang R, Trivedi M, Green KJ, Cryns VL (2001) Caspase cleavage of vimentin disrupts intermediate filaments and promotes apoptosis. Cell Death. Differ. 8, 443-450.
10. Calabrese V, Scapagnini G, Ravagna A, Colombrita C, Spadaro F, Butterfield DA, Giuffrida Stella AM (2004) Increased expression of heat shock proteins in rat brain during aging: Relationship with mitochondrial function and glutathione redox state. Mech. Ageing. Dev. 125, 325-335.
11. Cristofalo VJ, Lorenzini A, Allen RG, Torres C, Tresini M (2004) Replicative senescence: A critical review. Mech. Ageing. Dev. 125, 827-848.
12. Cuervo AM, Bergamini E, Brunk UT, Droge W, Ffrench M, Terman A (2005) Autophagy and aging: The importance of maintaining 'clean' cells. Autophagy 1, 131-140.
13. Everitt AV, Hilmer SN, Brand-Miller JC, Jamieson HA, Truswell AS, Sharma AP, Mason RS, Morris BJ, Le Couteur DG (2006) Dietary approaches that delay age-related diseases. Clin. Interv Aging 1, 11-31.
14. Feuers RJ, Duffy PH, Leakey JA, Turturro A, Mittelstaedt RA, Hart RW (1989) Effect of chronic caloric restriction on hepatic enzymes of intermediary metabolism in the male Fischer 344 rat. Mech. Ageing. Dev. 48, 179-189.
15. Fortun J, Dunn WA Jr, Joy S, Li J, Notterpek L (2003) Emerging role for autophagy in the removal of aggresomes in Schwann cells. J. Neurosci. 23, 10672-10680.
16. Fortun J, Verrier JD, Go JC, Madorsky I, Dunn WA, Notterpek L (2007) The formation of peripheral myelin protein 22 aggregates is hindered by the enhancement of autophagy and expression of cytoplasmic chaperones. Neurobiol. Dis. 25, 252-265.
17. Frydman J (2001) Folding of newly translated proteins in vivo: The role of molecular chaperones. Annu. Rev. Biochem. 70, 603-647.
18. Fusek M, Vetvicka V (2005) Dual role of cathepsin D: Ligand and protease. Biomed. Pap. Med. Fac. Univ. Palacky. Olomouc. Czech. Repub. 149, 43-50.
19. Garbay B, Heape AM, Sargueil F, Cassagne C (2000) Myelin synthesis in the peripheral nervous system. Prog. Neurobiol. 61, 267-304.
20. Gregson NA, Hall SM (1973) A quantitative analysis of the effects of the intraneural injection of lysophosphatidyl choline. J. Cell Sci. 13, 257-277.
21. Grover-Johnson N, Spencer PS (1981) Peripheral nerve abnormalities in aging rats. J. Neuropathol. Exp. Neurol. 40, 155-165.
22. Grune T, Merker K, Jung T, Sitte N, Davies KJ (2005) Protein oxidation and degradation during postmitotic senescence. Free Radic Biol. Med. 39, 1208-1215.
23. Heydari AR, You S, Takahashi R, Gutsmann A, Sarge KD, Richardson A (1996) Effect of caloric restriction on the expression of heat shock protein 70 and the activation of heat shock transcription factor 1. Dev Genet 18, 114-124.
24. Heydari AR, You S, Takahashi R, Gutsmann-Conrad A, Sarge KD, Richardson A (2000) Age-related alterations in the activation of heat shock transcription factor 1 in rat hepatocytes. Exp. Cell. Res. 256, 83-93.
25. Hinman JD, Peters A, Cabral H, Rosene DL, Hollander W, Rasband MN, Abraham CR (2006) Age-related molecular reorganization at the node of Ranvier. J. Comp. Neurol. 495, 351-362.
26. Homma S, Jin X, Wang G, Tu N, Min J, Yanasak N, Mivechi NF (2007) Demyelination, astrogliosis, and accumulation of ubiquitinated proteins, hallmarks of CNS disease in hsf1-deficient mice. J. Neurosci. 27, 7974-7986.
27. Hori N, Hirotsu I, Davis PJ, Carpenter DO (1992) Long-term potentiation is lost in aged rats but preserved by calorie restriction. Neuroreport 3, 1085-1088.
28. Ingram DK, Young J, Mattison JA (2007) Calorie restriction in nonhuman primates: Assessing effects on brain and behavioral aging. Neuroscience 145, 1359-1364.
29. Jessen KR, Mirsky R (2005) The origin and development of glial cells in peripheral nerves. Nat. Rev. Neurosci. 6, 671-682.
30. Johnson JB, Laub DR, John S (2006) The effect on health of alternate day calorie restriction: Eating less and more than needed on alternate days prolongs life. Med. Hypotheses. 67, 209-211.
31. Jolly CA (2004) Dietary restriction and immune function. J. Nutr. 134, 1853-1856.
32. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19, 5720-5728.
33. Keller JN, Dimayuga E, Chen Q, Thorpe J, Gee J, Ding Q (2004) Autophagy, proteasomes, lipofuscin, and oxidative stress in the aging brain. Int. J. Biochem. Cell Biol. 36, 2376-2391.
34. Klionsky DJ, Meijer AJ, Codogno P (2005) Autophagy and p70S6 kinase. Autophagy 1, 59-60; discussion 60-51.
35. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, Baba M, Baehrecke EH, Bahr BA, Ballabio A, Bamber BA, Bassham DC, Bergamini E, Bi X, Biard-Piechaczyk M, Blum JS, Bredesen DE, Brodsky JL, Brumell JH, Brunk UT, Bursch W, Camougrand N, Cebollero E, Cecconi F, Chen Y, Chin LS, Choi A, Chu CT, Chung J, Clarke PG, Clark RS, Clarke SG, Clave C, Cleveland JL, Codogno P, Colombo MI, Coto-Montes A, Cregg JM, Cuervo AM, Debnath J, Demarchi F, Dennis PB, Dennis PA, Deretic V, Devenish RJ, Di Sano F, Dice JF, Difiglia M, Dinesh-Kumar S, Distelhorst CW, Djavaheri-Mergny M, Dorsey FC, Droge W, Dron M, Dunn WA Jr, Duszenko M, Eissa NT, Elazar Z, Esclatine A, Eskelinen EL, Fesus L, Finley KD, Fuentes JM, Fueyo J, Fujisaki K, Galliot B, Gao FB, Gewirtz DA, Gibson SB, Gohla A, Goldberg AL, Gonzalez R, Gonzalez-Estevez C, Gorski S, Gottlieb RA, Haussinger D, He YW, Heidenreich K, Hill JA, Hoyer-Hansen M, Hu X, Huang WP, Iwasaki A, Jaattela M, Jackson WT, Jiang X, Jin S, Johansen T, Jung JU, Kadowaki M, Kang C, Kelekar A, Kessel DH, Kiel JA, Kim HP, Kimchi A, Kinsella TJ, Kiselyov K, Kitamoto K, Knecht E et al. (2008) Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy. 4, 151-175.
36. Lund BT, Chakryan Y, Ashikian N, Mnatsakanyan L, Bevan CJ, Aguilera R, Gallaher T, Jakowec MW (2006) Association of MBP peptides with Hsp70 in normal appearing human white matter. J. Neurol. Sci. 249, 122-134.
37. Macario AJ, Conway de Macario E (2002) Sick chaperones and ageing: A perspective. Ageing. Res. Rev. 1, 295-311.
38. Marzetti E, Lawler JM, Hiona A, Manini T, Seo AY, Leeuwenburgh C (2008) Modulation of age-induced apoptotic signaling and cellular remodeling by exercise and calorie restriction in skeletal muscle. Free Radic Biol. Med. 44, 160-168.
39. Mattson MP, Magnus T (2006) Ageing and neuronal vulnerability. Nat. Rev. Neurosci. 7, 278-294.
40. Mattson MP, Duan W, Lee J, Guo Z (2001) Suppression of brain aging and neurodegenerative disorders by dietary restriction and environmental enrichment: Molecular mechanisms. Mech. Ageing. Dev. 122, 757-778.
41. Melcangi RC, Magnaghi V, Cavarretta I, Martini L, Piva F (1998a) Age-induced decrease of glycoprotein Po and myelin basic protein gene expression in the rat sciatic nerve. Repair by steroid derivatives. Neuroscience 85, 569-578.
42. Melcangi RC, Magnaghi V, Cavarretta I, Riva MA, Piva F, Martini L (1998b) Effects of steroid hormones on gene expression of glial markers in the central and peripheral nervous system: Variations induced by aging. Exp. Gerontol. 33, 827-836.
43. Melcangi RC, Magnaghi V, Martini L (2000) Aging in peripheral nerves: regulation of myelin protein genes by steroid hormones. Prog. Neurobiol. 60, 291-308.
44. Mizushima N, Yoshimori T (2007) How to interpret LC3 immunoblotting. Autophagy 3, 542-545.
45. Nave KA, Trapp BD (2008) Axon-glial signaling and the glial support of axon function. Annu. Rev. Neurosci. 31, 535-561.
46. Noebels JL, Marcom PK, Jalilian-Tehrani MH (1991) Sodium channel density in hypomyelinated brain increased by myelin basic protein gene deletion. Nature 352, 431-434.
47. Norris CM, Korol DL, Foster TC (1996) Increased susceptibility to induction of long-term depression and long-term potentiation reversal during aging. J. Neurosci. 16, 5382-5392.
48. Notterpek L, Shooter EM, Snipes GJ (1997) Upregulation of the endosomal-lysosomal pathway in the trembler-J neuropathy. J. Neurosci. 17, 4190-4200.
49. Notterpek L, Snipes GJ, Shooter EM (1999) Temporal expression pattern of peripheral myelin protein 22 during in vivo and in vitro myelination. Glia 25, 358-369.
50. + channel distribution in the nervous system. Trends Neurosci. 24, 473-478.
51. Ohtsuka K, Suzuki T (2000) Roles of molecular chaperones in the nervous system. Brain Res. Bull. 53, 141-146.
52. Pareek S, Notterpek L, Snipes GJ, Naef R, Sossin W, Laliberte J, Iacampo S, Suter U, Shooter EM, Murphy RA (1997) Neurons promote the translocation of peripheral myelin protein 22 into myelin. J Neurosci 17, 7754-7762.
53. Parhad IM, Scott JN, Cellars LA, Bains JS, Krekoski CA, Clark AW (1995) Axonal atrophy in aging is associated with a decline in neurofilament gene expression. J. Neurosci. Res. 41, 355-366.
54. Pirkkala L, Nykanen P, Sistonen L (2001) Roles of the heat shock transcription factors in regulation of the heat shock response and beyond. FASEB J. 15, 1118-1131.
55. Pitsikas N, Algeri S (1992) Deterioration of spatial and nonspatial reference and working memory in aged rats: Protective effect of life-long calorie restriction. Neurobiol. Aging. 13, 369-373.
56. Plakidou-Dymock S, McGivan JD (1994) Amino acid deprivation-induced stress response in the bovine renal epithelial cell line NBL-1: induction of HSP 70 by phenylalanine. Biochim. Biophys. Acta 1224, 189-197.
57. Rangaraju S, Madorsky I, Pileggi JG, Kamal A, Notterpek L (2008) Pharmacological induction of the heat shock response improves myelination in a neuropathic model. Neurobiol Dis 32, 105-115.
58. Rattan SI (2004) Hormetic mechanisms of anti-aging and rejuvenating effects of repeated mild heat stress on human fibroblasts in vitro. Rejuvenation. Res. 7, 40-48.
59. Ribalta T, McCutcheon IE, Aldape KD, Bruner JM, Fuller GN (2004) The mitosis-specific antibody anti-phosphohistone-H3 (PHH3) facilitates rapid reliable grading of meningiomas according to WHO 2000 criteria. Am. J. Surg. Pathol. 28, 1532-1536.
60. Rocca A, Lamaze C, Subtil A, Dautry-Varsat A (2001) Involvement of the ubiquitin/proteasome system in sorting of the interleukin 2 receptor beta chain to late endocytic compartments. Mol. Biol. Cell 12, 1293-1301.
61. Ryan MC, Shooter EM, Notterpek L (2002) Aggresome formation in neuropathy models based on peripheral myelin protein 22 mutations. Neurobiol. Dis. 10, 109-118.
62. Saito H, Kobayashi K, Mochizuki H, Ishii T (1990) Axonal degeneration of the peripheral nerves and postganglionic anhidrosis in a patient with multiple sclerosis. Tohoku J. Exp. Med. 162, 279-291.
63. Samarel AM, Ferguson AG, Decker RS, Lesch M (1989) Effects of cysteine protease inhibitors on rabbit cathepsin D maturation. Am. J. Physiol. 257, C1069-C1079.
64. Selsby JT, Judge AR, Yimlamai T, Leeuwenburgh C, Dodd SL (2005) Life long calorie restriction increases heat shock proteins and proteasome activity in soleus muscles of Fisher 344 rats. Exp. Gerontol. 40, 37-42.
65. Sharma AK, Bajada S, Thomas PK (1980) Age changes in the tibial and plantar nerves of the rat. J. Anat. 130, 417-428.
66. Sherman MY, Goldberg AL (2001) Cellular defenses against unfolded proteins: A cell biologist thinks about neurodegenerative diseases. Neuron 29, 15-32.
67. Sitte N, Merker K, Von Zglinicki T, Davies KJ, Grune T (2000) Protein oxidation and degradation during cellular senescence of human BJ fibroblasts: Part II -aging of nondividing cells. FASEB J. 14, 2503-2510.
68. Squier TC (2001) Oxidative stress and protein aggregation during biological aging. Exp. Gerontol. 36, 1539-1550.
69. Stadtman ER (2001) Protein oxidation in aging and age-related diseases. Ann. N. Y. Acad. Sci. 928, 22-38.
70. Toth C, Shim SY, Wang J, Jiang Y, Neumayer G, Belzil C, Liu WQ, Martinez J, Zochodne D, Nguyen MD (2008) Ndel1 promotes axon regeneration via intermediate filaments. PLoS ONE. 3, e2014.
71. Uchida A, Brown A (2004) Arrival, reversal, and departure of neurofilaments at the tips of growing axons. Mol. Biol. Cell 15, 4215-4225.
72. Uchida A, Tashiro T, Komiya Y, Yorifuji H, Kishimoto T, Hisanaga S (2004) Morphological and biochemical changes of neurofilaments in aged rat sciatic nerve axons. J. Neurochem. 88, 735-745.
73. Vabnick I, Messing A, Chiu SY, Levinson SR, Schachner M, Roder J, Li C, Novakovic S, Shrager P (1997) Sodium channel distribution in axons of hypomyelinated and MAG null mutant mice. J. Neurosci. Res. 50, 321-336.
74. Verdu E, Ceballos D, Vilches JJ, Navarro X (2000) Influence of aging on peripheral nerve function and regeneration. J. Peripher. Nerv. Syst. 5, 191-208.
75. Voellmy R, Boellmann F (2007) Chaperone regulation of the heat shock protein response. Adv. Exp. Med. Biol. 594, 89-99.
76. Weissman L, de Souza-Pinto NC, Stevnsner T, Bohr VA (2007) DNA repair, mitochondria, and neurodegeneration. Neuroscience 145, 1318-1329.
77. Westenbroek RE, Noebels JL, Catterall WA (1992) Elevated expression of type II Na+ channels in hypomyelinated axons of shiverer mouse brain. J. Neurosci. 12, 2259-2267.
78. Wohlgemuth SE, Julian D, Akin DE, Fried J, Toscano K, Leeuwenburgh C, Dunn WA Jr (2007) Autophagy in the heart and liver during normal aging and calorie restriction. Rejuvenation. Res. 10, 281-292.
79. Xu J, Knutson MD, Carter CS, Leeuwenburgh C (2008) Iron accumulation with age, oxidative stress and functional decline. PLoS ONE 3, e2865.
80. Zanazzi G, Einheber S, Westreich R, Hannocks MJ, Bedell-Hogan D, Marchionni MA, Salzer JL (2001) Glial growth factor/neuregulin inhibits Schwann cell myelination and induces demyelination. J. Cell Biol. 152, 1289-1299.
81. Zwerling SJ, Cohen SA, Barchi RL (1991) Analysis of protease-sensitive regions in the skeletal muscle sodium channel in vitro and implications for channel tertiary structure. J. Biol. Chem. 266, 4574-4580.