Diabetic retinopathy is associated with bone marrow neuropathy and a depressed peripheral clock

Journal of Experimental Medicine

Volumn 206, Issue 13, 2009, Pages 2897-2906

  Busik, Julia V ^a   Tikhonenko, Maria ^a   Bhatwadekar, Ashay ^c   Opreanu, Madalina ^a,b   Yakubova, Nafissa ^a   Caballero, Sergio ^c   Player, Danny ^d   Nakagawa, Takahiko ^d   Afzal, Aqeela ^c   Kielczewski, Jennifer ^c   Sochacki, Andrew ^a   Hasty, Stephanie ^a   Li Calzi, Sergio ^c   Kim, Sungjin ^b   Duclas, Shane K ^e   Segal, Mark S ^d   Guberski, Dennis L ^e   Esselman, Walter J ^b   Boulton, Michael E ^c   Grant, Maria B ^c  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b University of Florida ^*  (United States)

^c UNIVERSITY OF FLORIDA   (United States)

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

^e Biomedical Research Models Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR CLOCK; NORADRENALIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW NEUROPATHY; CELL COUNT; CIRCADIAN RHYTHM; CONTROLLED STUDY; DENERVATION; DIABETIC RETINOPATHY; DISEASE ASSOCIATION; DISEASE DURATION; ENDOTHELIUM CELL; FEMALE; GENE EXPRESSION REGULATION; MOUSE; NERVE ENDING; NEUROPATHY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RETINA CAPILLARY; STEM CELL; TISSUE STRUCTURE; ADRENERGIC SYSTEM; ANIMAL; BLOOD; BONE MARROW; C57BL MOUSE; DIABETIC NEUROPATHY; GENETICS; HEMATOPOIETIC STEM CELL; INNERVATION; PHYSIOLOGY;

ANIMALS; BONE MARROW; CIRCADIAN RHYTHM; CLOCK PROTEINS; DENERVATION; DIABETIC NEUROPATHIES; DIABETIC RETINOPATHY; FEMALE; HEMATOPOIETIC STEM CELLS; MICE; MICE, INBRED C57BL; NOREPINEPHRINE; RATS; SYMPATHETIC NERVOUS SYSTEM;

EID: 73949157202     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20090889     Document Type: Article

References (23)

1. Asahara, T., T. Murohara, A. Sullivan, M. Silver, R. van der Zee, T. Li, B. Witzenbichler, G. Schatteman, and J.M. Isner. 1997. Isolation of putative progenitor endothelial cells for angiogenesis. Science. 275:964-967. doi:10.1126/science.275.5302.964
2. Ellis, E.A., M.B. Grant, F.T. Murray, M.B. Wachowski, D.L. Guberski, P.S. Kubilis, and G.A. Lutty. 1998. Increased NADH oxidase activity in the retina of the BBZ/Wor diabetic rat. Free Radic. Biol. Med. 24:111-120. doi:10.1016/S0891-5849(97)00202-5
3. Ellis, E.A., D.L. Guberski, M. Somogyi-Mann, and M.B. Grant. 2000. Increased H2O2, vascular endothelial growth factor and receptors in the retina of the BBZ/Wor diabetic rat. Free Radic. Biol. Med. 28:91-101. doi:10.1016/S0891-5849(99)00216-6
4. Grant, M.B., W.S. May, S. Caballero, G.A. Brown, S.M. Guthrie, R.N. Mames, B.J. Byrne, T. Vaught, P.E. Spoerri, A.B. Peck, and E.W. Scott. 2002. Adult hematopoietic stem cells provide functional hemangioblast activity during retinal neovascularization. Nat. Med. 8:607-612. doi:10.1038/nm0602-607
5. Ikeda, H., Q. Yong, T. Kurose, T. Todo, W. Mizunoya, T. Fushiki, Y. Seino, and Y. Yamada. 2007. Clock gene defect disrupts light-dependency of autonomic nerve activity. Biochem. Biophys. Res. Commun. 364:457-463. doi:10.1016/j.bbrc.2007.10.058
6. Katayama, Y., M. Battista, W.M. Kao, A. Hidalgo, A.J. Peired, S.A. Thomas, and P.S. Frenette. 2006. Signals from the sympathetic nervous system regulate hematopoietic stem cell egress from bone marrow. Cell. 124:407-421. doi:10.1016/j.cell.2005.10.041
7. Kohsaka, A., A.D. Laposky, K.M. Ramsey, C. Estrada, C. Joshu, Y. Kobayashi, F.W. Turek, and J. Bass. 2007. High-fat diet disrupts behavioral and molecular circadian rhythms in mice. Cell Metab. 6:414-421. doi:10.1016/j.cmet.2007.09.006
8. Loomans, C.J., H. Wan, R. de Crom, R. van Haperen, H.C. de Boer, P.J. Leenen, H.A. Drexhage, T.J. Rabelink, A.J. van Zonneveld, and F.J. Staal. 2006. Angiogenic murine endothelial progenitor cells are derived from a myeloid bone marrow fraction and can be identified by endothelial NO synthase expression. Arterioscler. Thromb. Vasc. Biol. 26:1760-1767. doi:10.1161/01.ATV. 0000229243.49320.c9
9. Méndez-Ferrer, S., D. Lucas, M. Battista, and P.S. Frenette. 2008. Haematopoietic stem cell release is regulated by circadian oscillations. Nature. 452:442-447. doi:10.1038/nature06685
10. Mizutani, M., T.S. Kern, and M. Lorenzi. 1996. Accelerated death of retinal microvascular cells in human and experimental diabetic retinopathy. J. Clin. Invest. 97:2883-2890. doi:10.1172/JCI118746
11. Peichev, M., A.J. Naiyer, D. Pereira, Z. Zhu, W.J. Lane, M. Williams, M.C. Oz, D.J. Hicklin, L. Witte, M.A. Moore, and S. Rafii. 2000. Expression of VEGFR-2 and AC133 by circulating human CD34(+) cells identifies a population of functional endothelial precursors. Blood. 95:952-958.
12. Peschke, E. 2008. Melatonin, endocrine pancreas and diabetes. J. Pineal Res. 44:26-40.
13. Ruiter, M., R.M. Buijs, and A. Kalsbeek. 2006. Hormones and the autonomic nervous system are involved in suprachiasmatic nucleus modulation of glucose homeostasis. Curr. Diabetes Rev. 2:213-226. doi:10.2174/ 157339906776818596
14. Said, G. 2007. Focal and multifocal diabetic neuropathies. Arq. Neuropsiquiatr. 65:1272-1278.
15. Schatteman, G.C., M. Dunnwald, and C. Jiao. 2007. Biology of bone marrow-derived endothelial cell precursors. Am. J. Physiol. Heart Circ. Physiol. 292:H1-H18. doi:10.1152/ajpheart.00662.2006
16. Segal, M.S., R. Shah, A. Afzal, C.M. Perrault, K. Chang, A. Schuler, E. Beem, L.C. Shaw, S. Li Calzi, J.K. Harrison, et al. 2006. Nitric oxide cytoskeletal-induced alterations reverse the endothelial progenitor cell migratory defect associated with diabetes. Diabetes. 55:102-109. doi:10.2337/diabetes.55.01.06.db05-0803
17. Serre, C.M., D. Farlay, P.D. Delmas, and C. Chenu. 1999. Evidence for a dense and intimate innervation of the bone tissue, including glutamate-containing fibers. Bone. 25:623-629. doi:10.1016/S8756-3282(99) 00215-X
18. Su, W., Z. Guo, D.C. Randall, L. Cassis, D.R. Brown, and M.C. Gong. 2008. Hypertension and disrupted blood pressure circadian rhythm in type 2 diabetic db/db mice. Am. J. Physiol. Heart Circ. Physiol. 295:H1634-H1641. doi:10.1152/ajpheart.00257.2008
19. Thomas, H.E., R. Redgrave, M.S. Cunnington, P. Avery, B.D. Keavney, and H.M. Arthur. 2008. Circulating endothelial progenitor cells exhibit diurnal variation. Arterioscler. Thromb. Vasc. Biol. 28:e21-e22. doi:10.1161/ATVBAHA.107.160317
20. Tirabassi, R.S., J.F. Flanagan, T. Wu, E.H. Kislauskis, P.J. Birckbichler, and D.L. Guberski. 2004. The BBZDR/Wor rat model for investigating the complications of type 2 diabetes mellitus. ILAR J. 45:292-302.
21. Wang, C.Y., M.S. Wen, H.W. Wang, I.C. Hsieh, Y. Li, P.Y. Liu, F.C. Lin, and J.K. Liao. 2008. Increased vascular senescence and impaired endothelial progenitor cell function mediated by mutation of circadian gene Per2. Circulation. 118:2166-2173. doi:10.1161/CIRCULATIONAHA.108.790469
22. Weber, F. 2009. Remodeling the clock: coactivators and signal transduction in the circadian clockworks. Naturwissenschaften. 96:321-337. doi:10.1007/s00114-008-0474-9
23. Weston, P.J., and G.V. Gill. 1999. Is undetected autonomic dysfunction responsible for sudden death in Type 1 diabetes mellitus? The 'dead in bed' syndrome revisited. Diabet. Med. 16:626-631. doi:10.1046/j.1464-5491. 1999.00121.x