Diabetes-induced myelin abnormalities are associated with an altered lipid pattern: Protective effects of LXR activation

Journal of Lipid Research

Volumn 53, Issue 2, 2012, Pages 300-310

  Cermenati, Gaia ^a   Abbiati, Federico ^a   Cermenati, Solei ^a   Brioschi, Elisabetta ^a   Volonterio, Alessandro ^b   Cavaletti, Guido ^c   Saez, Enrique ^d   De Fabiani, Emma ^a   Crestani, Maurizio ^a   Garcia Segura, Luis M ^e   Melcangi, Roberto C ^a   Caruso, Donatella ^a   Mitro, Nico ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b POLITECNICO DI MILANO   (Italy)

^c UNIVERSITY OF MILANO BICOCCA   (Italy)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

^e INSTITUTO CAJAL   (Spain)

Author keywords

Diabetic neuropathy; Fatty acid synthesis; Liver X receptor; Myelin composition; Peripheral nerve; Sterol regulatory element binding factor 1c

Indexed keywords

3 [3 [[2 CHLORO 3 (TRIFLUOROMETHYL)BENZYL](2 DIPHENYLETHYL)AMINO]PROPOXY]PHENYLACETIC ACID; CHOLESTEROL; FATTY ACID; LIPID; LIVER X RECEPTOR; MYELIN; MYELIN PROTEIN; MYELIN PROTEIN ZERO; PHOSPHOLIPID; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIABETIC NEUROPATHY; DRUG MECHANISM; GENE EXPRESSION; LIPID ANALYSIS; LIPID COMPOSITION; MALE; MEMBRANE FLUIDITY; NERVE CONDUCTION; NONHUMAN; PAIN THRESHOLD; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; RAT; SCIATIC NERVE;

ANIMALS; CHOLESTEROL; DIABETES MELLITUS, EXPERIMENTAL; GENE EXPRESSION REGULATION; LIPIDS; MALE; MYELIN P0 PROTEIN; MYELIN SHEATH; ORPHAN NUCLEAR RECEPTORS; PHOSPHOLIPIDS; PROTEIN KINASES; RATS; RATS, SPRAGUE-DAWLEY; SCIATIC NERVE; STEAROYL-COA DESATURASE; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; STREPTOZOCIN;

EID: 84855697856     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M021188     Document Type: Article

References (49)

1. ADA. 2007. Standards of medical care in diabetes-2007. Diabetes Care. 30 (Suppl.) : 4-41.
2. Gordois, A., P. Scuffham, A. Shearer, A. Oglesby, and J. A. Tobian. 2003. The health care costs of diabetic peripheral neuropathy in the US. Diabetes Care. 26: 1790-1795. (Pubitemid 36929121)
3. Herman, W. H. 2007. Diabetes epidemiology: guiding clinical and public health practice: the Kelly West Award Lecture, 2006. Diabetes Care. 30: 1912-1919. (Pubitemid 47036382)
4. Sugimoto, K., Y. Murakawa, and A. A. Sima. 2000. Diabetic neuropathy-a continuing enigma. Diabetes Metab. Res. Rev. 16: 408-433.
5. Vinik, A. I., T. S. Park, K. B. Stansberry, and G. L. Pittenger. 2000. Diabetic neuropathies. Diabetologia. 43: 957-973. (Pubitemid 30655714)
6. Sima, A. A., and T. Brismar. 1985. Reversible diabetic nerve dysfunction: structural correlates to electrophysiological abnormalities. Ann. Neurol. 18: 21-29. (Pubitemid 15025409)
7. Eckersley, L. 2002. Role of the Schwann cell in diabetic neuropathy. Int. Rev. Neurobiol. 50: 293-321.
8. Malik, R. A., S. Tesfaye, P. G. Newrick, D. Walker, S. M. Rajbhandari, I. Siddique, A. K. Sharma, A. J. Boulton, R. H. King, P. K. Thomas, et al. 2005. Sural nerve pathology in diabetic patients with minimal but progressive neuropathy. Diabetologia. 48: 578-585. (Pubitemid 40487306)
9. Valls-Canals, J., M. Povedano, J. Montero, and J. Pradas. 2002. Diabetic polyneuropathy. Axonal or demyelinating? Electromyogr. Clin. Neurophysiol. 42: 3-6. (Pubitemid 34130156)
10. Yagihashi, S. 1997. Nerve structural defects in diabetic neuropathy: do animals exhibit similar changes? Neurosci. Res. Commun. 21: 25-32. (Pubitemid 27336349)
11. Biessels, G. J., N. A. Cristino, G. J. Rutten, F. P. Hamers, D. W. Erkelens, and W. H. Gispen. 1999. Neurophysiological changes in the central and peripheral nervous system of streptozotocin-diabetic rats. Course of development and effects of insulin treatment. Brain. 122: 757-768.
12. Dyck, P. J., B. R. Zimmerman, T. H. Vilen, S. R. Minnerath, J. L. Karnes, J. K. Yao, and J. F. Poduslo. 1988. Nerve glucose, fructose, sorbitol, myo-inositol, and fiber degeneration and regeneration in diabetic neuropathy. N. Engl. J. Med. 319: 542-548.
13. Veiga, S., E. Leonelli, M. Beelke, L. M. Garcia-Segura, and R. C. Melcangi. 2006. Neuroactive steroids prevent peripheral myelin alterations induced by diabetes. Neurosci. Lett. 402: 150-153. (Pubitemid 43766443)
14. Garbay, B., A. M. Heape, F. Sargueil, and C. Cassagne. 2000. Myelin synthesis in the peripheral nervous system. Prog. Neurobiol. 61: 267-304. (Pubitemid 30155722)
15. Waxman, S. G., and J. M. Ritchie. 1993. Molecular dissection of the myelinated axon. Ann. Neurol. 33: 121-136. (Pubitemid 23039921)
16. Norton, W. T., and S. E. Poduslo. 1973. Myelination in rat brain: changes in myelin composition during brain maturation. J. Neurochem. 21: 759-773.
17. Norton, W. T., and S. E. Poduslo. 1973. Myelination in rat brain: method of myelin isolation. J. Neurochem. 21: 749-757.
18. Detering, N. K., and M. A. Wells. 1976. The non-synchronous synthesis of myelin components during early stages of myelination in the rat optic nerve. J. Neurochem. 26: 253-257.
19. Nussbaum, J. L., N. Neskovic, and P. Mandel. 1969. A study of lipid components in brain of the 'Jimpy' mouse, a mutant with myelin deficiency. J. Neurochem. 16: 927-934.
20. de Preux, A. S., K. Goosen, W. Zhang, A. A. Sima, H. Shimano, D. M. Ouwens, M. Diamant, J. L. Hillebrands, J. Rozing, G. Lemke, et al. 2007. SREBP-1c expression in Schwann cells is affected by diabetes and nutritional status. Mol. Cell. Neurosci. 35: 525-534. (Pubitemid 47176898)
21. Verheijen, M. H., N. Camargo, V. Verdier, K. Nadra, A. S. de Preux Charles, J. J. Medard, A. Luoma, M. Crowther, H. Inouye, H. Shimano, et al. 2009. SCAP is required for timely and proper myelin membrane synthesis. Proc. Natl. Acad. Sci. USA. 106: 21383-21388.
22. Zuvic-Butorac, M., J. Kriz, A. Simonic, and M. Schara. 2001. Fluidity of the myelin sheath in the peripheral nerves of diabetic rats. Biochim. Biophys. Acta. 1537: 110-116. (Pubitemid 32885612)
23. Coste, T. C., A. Gerbi, P. Vague, J. M. Maixent, G. Pieroni, and D. Raccah. 2004. Peripheral diabetic neuropathy and polyunsaturated fatty acid supplementations: natural sources or biotechnological needs? Cell. Mol. Biol. (Noisy-le-grand). 50: 845-853.
24. Cermenati, G., S. Giatti, G. Cavaletti, R. Bianchi, O. Maschi, M. Pesaresi, F. Abbiati, A. Volonterio, E. Saez, D. Caruso, et al. 2010. Activation of the liver X receptor increases neuroactive steroid levels and protects from diabetes-induced peripheral neuropathy. J. Neurosci. 30: 11896-11901.
25. Caruso, D., S. Scurati, O. Maschi, L. De Angelis, I. Roglio, S. Giatti, L. M. Garcia-Segura, and R. C. Melcangi. 2008. Evaluation of neuroactive steroid levels by liquid chromatography-tandem mass spectrometry in central and peripheral nervous system: effect of diabetes. Neurochem. Int. 52: 560-568.
26. Pesaresi, M., O. Maschi, S. Giatti, L. M. Garcia-Segura, D. Caruso, and R. C. Melcangi. 2010. Sex differences in neuroactive steroid levels in the nervous system of diabetic and non-diabetic rats. Horm. Behav. 57: 46-55.
27. Roglio, I., S. Giatti, M. Pesaresi, R. Bianchi, G. Cavaletti, G. Lauria, L. M. Garcia-Segura, and R. C. Melcangi. 2008. Neuroactive steroids and peripheral neuropathy. Brain Res. Rev. 57: 460-469. (Pubitemid 351381761)
28. Leonelli, E., R. Bianchi, G. Cavaletti, D. Caruso, D. Crippa, L. M. Garcia-Segura, G. Lauria, V. Magnaghi, I. Roglio, and R. C. Melcangi. 2007. Progesterone and its derivatives are neuroprotective agents in experimental diabetic neuropathy: a multimodal analysis. Neuroscience. 144: 1293-1304. (Pubitemid 46123820)
29. Kalaany, N. Y., and D. J. Mangelsdorf. 2006. LXRS and FXR: the yin and yang of cholesterol and fat metabolism. Annu. Rev. Physiol. 68: 159-191.
30. Schultz, J. R., H. Tu, A. Luk, J. J. Repa, J. C. Medina, L. Li, S. Schwendner, S. Wang, M. Thoolen, D. J. Mangelsdorf, et al. 2000. Role of LXRs in control of lipogenesis. Genes Dev. 14: 2831-2838.
31. Melcangi, R. C., F. Celotti, P. Castano, and L. Martini. 1992. Is the 5 alpha-reductase-3 alpha-hydroxysteroid dehydrogenase complex associated with the myelin in the peripheral nervous system of young and old male rats? Endocr. Regul. 26: 119-125. (Pubitemid 23208625)
32. Taguchi, R., and M. Ishikawa. 2010. Precise and global identification of phospholipid molecular species by an Orbitrap mass spectrometer and automated search engine Lipid Search. J. Chromatogr. A. 1217: 4229-4239.
33. Mayhew, T. M., and A. K. Sharma. 1984. Sampling schemes for estimating nerve fibre size. I. Methods for nerve trunks of mixed fascicularity. J. Anat. 139: 45-58. (Pubitemid 14052315)
34. Mayhew, T. M., and A. K. Sharma. 1984. Sampling schemes for estimating nerve fibre size. II. Methods for unifascicular nerve trunks. J. Anat. 139: 59-66. (Pubitemid 14052316)
35. Arbuthnott, E. R., I. A. Boyd, and K. U. Kalu. 1980. Ultrastructural dimensions of myelinated peripheral nerve fibres in the cat and their relation to conduction velocity. J. Physiol. 308: 125-157. (Pubitemid 11252745)
36. Arbuthnott, E. R., K. J. Ballard, I. A. Boyd, and K. U. Kalu. 1980. Quantitative study of the non-circularity of myelinated peripheral nerve fibres in the cat. J. Physiol. 308: 99-123. (Pubitemid 11252744)
37. Chrast, R., G. Saher, K. A. Nave, and M. H. Verheijen. 2011. Lipid metabolism in myelinating glial cells: lessons from human inherited disorders and mouse models. J. Lipid Res. 52: 419-434.
38. Garbay, B., F. Boiron-Sargueil, M. Shy, T. Chbihi, H. Jiang, J. Kamholz, and C. Cassagne. 1998. Regulation of oleoyl-CoA synthesis in the peripheral nervous system: demonstration of a link with myelin synthesis. J. Neurochem. 71: 1719-1726. (Pubitemid 28443046)
39. Shimomura, I., Y. Bashmakov, and J. D. Horton. 1999. Increased levels of nuclear SREBP-1c associated with fatty livers in two mouse models of diabetes mellitus. J. Biol. Chem. 274: 30028-30032.
40. Wang, X., R. Sato, M. S. Brown, X. Hua, and J. L. Goldstein. 1994. SREBP-1, a membrane-bound transcription factor released by sterol-regulated proteolysis. Cell. 77: 53-62.
41. Toth, J. I., S. Datta, J. N. Athanikar, L. P. Freedman, and T. F. Osborne. 2004. Selective coactivator interactions in gene activation by SREBP-1a and -1c. Mol. Cell. Biol. 24: 8288-8300. (Pubitemid 39167476)
42. Jeon, T. I., B. Zhu, J. L. Larson, and T. F. Osborne. 2008. SREBP-2 regulates gut peptide secretion through intestinal bitter taste receptor signaling in mice. J. Clin. Invest. 118: 3693-3700.
43. Kawashima, R., H. Kojima, K. Nakamura, A. Arahata, Y. Fujita, Y. Tokuyama, T. Saito, S. Furudate, T. Kurihara, S. Yagishita, et al. 2007. Alterations in mRNA expression of myelin proteins in the sciatic nerves and brains of streptozotocin-induced diabetic rats. Neurochem. Res. 32: 1002-1010. (Pubitemid 46726019)
44. Azcoitia, I., E. Leonelli, V. Magnaghi, S. Veiga, L. M. Garcia-Segura, and R. C. Melcangi. 2003. Progesterone and its derivatives dihydroprogesterone and tetrahydroprogesterone reduce myelin fiber morphological abnormalities and myelin fiber loss in the sciatic nerve of aged rats. Neurobiol. Aging. 24: 853-860. (Pubitemid 37288858)
45. Lee, A. G. 2003. Lipid-protein interactions in biological membranes: a structural perspective. Biochim. Biophys. Acta. 1612: 1-40. (Pubitemid 36555684)
46. Chen, G., G. Liang, J. Ou, J. L. Goldstein, and M. S. Brown. 2004. Central role for liver X receptor in insulin-mediated activation of Srebp-1c transcription and stimulation of fatty acid synthesis in liver. Proc. Natl. Acad. Sci. USA. 101: 11245-11250. (Pubitemid 39038332)
47. Melcangi, R. C., I. T. Cavarretta, M. Ballabio, E. Leonelli, A. Schenone, I. Azcoitia, L. Miguel Garcia-Segura, and V. Magnaghi. 2005. Peripheral nerves: a target for the action of neuroactive steroids. Brain Res. Brain Res. Rev. 48: 328-338. (Pubitemid 40585763)
48. Makoukji, J., G. Shackleford, D. Meffre, J. Grenier, P. Liere, J. M. Lobaccaro, M. Schumacher, and C. Massaad. 2011. Interplay between LXR and Wnt/{beta}-catenin signaling in the negative regulation of peripheral myelin genes by oxysterols. J. Neurosci. 31: 9620-9629.
49. Krarup, C. 2003. An update on electrophysiological studies in neuropathy. Curr. Opin. Neurol. 16: 603-612. (Pubitemid 37290091)