Combination therapies prevent the neuropathic, proinflammatory characteristics of bone marrow in streptozotocin-induced diabetic rats

Diabetes

Volumn 64, Issue 2, 2015, Pages 643-653

  Dominguez, James M ^a   Yorek, Mark A ^b,c   Grant, Maria B ^d  

^a UNIVERSITY OF FLORIDA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c UNIVERSITY OF IOWA   (United States)

^d INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

8 HYDROXYDEOXYGUANOSINE; ALDEHYDE REDUCTASE; ANTIOXIDANT; CALCITONIN GENE RELATED PEPTIDE; COLONY STIMULATING FACTOR 1; FIDARESTAT; GELATINASE A; GLUCOSE; GLYCOSYLATED HEMOGLOBIN; GRANULOCYTE COLONY STIMULATING FACTOR; HEMOGLOBIN A1C; I KAPPA B; I KAPPA B1 PROTEIN; ILEPATRIL; INDUCIBLE NITRIC OXIDE SYNTHASE; INSULIN; INTERLEUKIN 1BETA; MEMBRANE METALLOENDOPEPTIDASE; MENHADEN OIL; NEUROPEPTIDE Y; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; SOMATOSTATIN; THIOCTIC ACID; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG; ANTIDIABETIC AGENT; CYBB PROTEIN, RAT; CYTOKINE; FISH OIL; FUSED HETEROCYCLIC RINGS; IMIDAZOLIDINE DERIVATIVE; MEMBRANE PROTEIN; MESSENGER RNA; NOS2 PROTEIN, RAT; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; STREPTOZOCIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; BONE MARROW NEUROPATHY; BONE MARROW PROGENITOR CELL; CONTROLLED STUDY; DIABETIC NEUROPATHY; ENZYME INHIBITION; EXPERIMENTAL NEUROPATHY; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INFLAMMATION; INSULIN TREATMENT; LIMIT OF QUANTITATION; MALE; MOTOR NERVE CONDUCTION; NERVE CONDUCTION; NEUROPROTECTION; NOCICEPTIVE STIMULATION; NONHUMAN; OBESITY; PERIPHERAL NEUROPATHY; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT; REAL TIME POLYMERASE CHAIN REACTION; SENSORY NERVE CONDUCTION; STREPTOZOTOCIN-INDUCED DIABETIC NEUROPATHY; ADIPOSE TISSUE; ANIMAL; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEUROPATHIES; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PAIN MEASUREMENT; PATHOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT; STEM CELL;

ADIPOSE TISSUE; ANIMALS; BONE MARROW; CYTOKINES; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEUROPATHIES; FISH OILS; GENE EXPRESSION REGULATION; HETEROCYCLIC COMPOUNDS, 3-RING; HYPOGLYCEMIC AGENTS; IMIDAZOLIDINES; INFLAMMATION; INSULIN; MALE; MEMBRANE GLYCOPROTEINS; NADPH OXIDASE; NEUROPEPTIDE Y; NITRIC OXIDE SYNTHASE TYPE II; PAIN MEASUREMENT; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SOMATOSTATIN; STEM CELLS; STREPTOZOCIN; THIOCTIC ACID; TYROSINE 3-MONOOXYGENASE;

EID: 84921902298     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db14-0433     Document Type: Article

References (64)

1. Centers for Disease Control and Prevention. National Diabetes Statistics Report: Estimates of Diabetes and its Burden in the United States, 2014. Atlanta, GA, U. S. Department of Health and Human Services, 2014
2. Ziegler-Graham K, MacKenzie EJ, Ephraim PL, Travison TG, Brookmeyer R. Estimating the prevalence of limb loss in the United States: 2005 to 2050. Arch Phys Med Rehabil 2008;89:422-429
3. Judzewitsch RG, Jaspan JB, Polonsky KS, et al. Aldose reductase inhibition improves nerve conduction velocity in diabetic patients. N Engl J Med 1983;308:119-125
4. Davidson EP, Kleinschmidt TL, Oltman CL, Lund DD, Yorek MA. Treatment of streptozotocin-induced diabetic rats with AVE7688, a vasopeptidase inhibitor: effect on vascular and neural disease. Diabetes 2007;56:355-362
5. Coppey LJ, Gellett JS, Davidson EP, Dunlap JA, Yorek MA. Effect of treating streptozotocin-induced diabetic rats with sorbinil, myo-inositol or aminoguanidine on endoneurial blood flow, motor nerve conduction velocity and vascular function of epineurial arterioles of the sciatic nerve. Int J Exp Diabetes Res 2002;3:21-36
6. Gonzalez AM, Sochor M, McLean P. The effect of an aldose reductase inhibitor (Sorbinil) on the level of metabolites in lenses of diabetic rats. Diabetes 1983;32:482-485
7. Busse E, Zimmer G, Schopohl B, Kornhuber B. Influence of alpha-lipoic acid on intracellular glutathione in vitro and in vivo. Arzneimittelforschung 1992;42:829-831
8. Low PA, Nickander KK, Tritschler HJ. The roles of oxidative stress and antioxidant treatment in experimental diabetic neuropathy. Diabetes 1997;46(Suppl. 2):S38-S42
9. Nagamatsu M, Nickander KK, Schmelzer JD, et al. Lipoic acid improves nerve blood flow, reduces oxidative stress, and improves distal nerve conduction in experimental diabetic neuropathy. Diabetes Care 1995;18:1160-1167
10. Sola S, Mir MQ, Cheema FA, et al. Irbesartan and lipoic acid improve endothelial function and reduce markers of inflammation in the metabolic syndrome: results of the Irbesartan and Lipoic Acid in Endothelial Dysfunction (ISLAND) study. Circulation 2005;111:343-348
11. De Caterina R, Madonna R, Bertolotto A, Schmidt EB. n-3 fatty acids in the treatment of diabetic patients: biological rationale and clinical data. Diabetes Care 2007;30:1012-1026
12. Katayama Y, Battista M, Kao WM, et al. Signals from the sympathetic nervous system regulate hematopoietic stem cell egress from bone marrow. Cell 2006;124:407-421
13. Hazra S, Jarajapu YP, Stepps V, et al. Long-term type 1 diabetes influences haematopoietic stem cells by reducing vascular repair potential and increasing inflammatory monocyte generation in a murine model. Diabetologia 2013;56:644-653
14. Busik JV, Tikhonenko M, Bhatwadekar A, et al. Diabetic retinopathy is associated with bone marrow neuropathy and a depressed peripheral clock. J Exp Med 2009;206:2897-2906
15. Hu P, Thinschmidt JS, Yan Y, et al. CNS inflammation and bone marrow neuropathy in type 1 diabetes. Am J Pathol 2013;183:1608-1620
16. Coppey LJ, Holmes A, Davidson EP, Yorek MA. Partial replacement with menhaden oil improves peripheral neuropathy in high-fat-fed low-dose streptozotocin type 2 diabetic rat. J Nutr Metab 2012;2012:950517
17. Nagatsu T, Levitt M, Udenfriend S. Tyrosine hydroxylase. The initial step in norepinephrine biosynthesis. J Biol Chem 1964;239:2910-2917
18. Chalazonitis A, Zigmond RE. Effects of synaptic and antidromic stimulation on tyrosine hydroxylase activity in the rat superior cervical ganglion. J Physiol 1980;300:525-538
19. Armani C, Catalani E, Balbarini A, Bagnoli P, Cervia D. Expression, pharmacology, and functional role of somatostatin receptor subtypes 1 and 2 in human macrophages. J Leukoc Biol 2007;81:845-855
20. Lundberg P, Allison SJ, Lee NJ, et al. Greater bone formation of Y2 knockout mice is associated with increased osteoprogenitor numbers and altered Y1 receptor expression. J Biol Chem 2007;282:19082-19091
21. Magavi SS, Leavitt BR, Macklis JD. Induction of neurogenesis in the neocortex of adult mice. Nature 2000;405:951-955
22. Parent JM, Yu TW, Leibowitz RT, Geschwind DH, Sloviter RS, Lowenstein DH. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 1997;17:3727-3738
23. Seo JY, Kim H, Kim KH. Transcriptional regulation by thiol compounds in Helicobacter pylori-induced interleukin-8 production in human gastric epithelial cells. Ann N Y Acad Sci 2002;973:541-545
24. Ramana KV, Willis MS, White MD, et al. Endotoxin-induced cardiomyopathy and systemic inflammation in mice is prevented by aldose reductase inhibition. Circulation 2006;114:1838-1846
25. Morcos M, Borcea V, Isermann B, et al. Effect of alpha-lipoic acid on the progression of endothelial cell damage and albuminuria in patients with diabetes mellitus: an exploratory study. Diabetes Res Clin Pract 2001;52:175-183
26. Matsumoto M, Sata M, Fukuda D, et al. Orally administered eicosapentaenoic acid reduces and stabilizes atherosclerotic lesions in ApoE-deficient mice. Atherosclerosis 2008;197:524-533
27. Sorgi CA, Rose S, Court N, et al. GM-CSF priming drives bone marrowderived macrophages to a pro-inflammatory pattern and downmodulates PGE2 in response to TLR2 ligands. PLoS One 2012;7:e40523
28. Lacey DC, Achuthan A, Fleetwood AJ, et al. Defining GM-CSF- and macrophage-CSF-dependent macrophage responses by in vitro models. J Immunol 2012;188:5752-5765
29. Fleetwood AJ, Lawrence T, Hamilton JA, Cook AD. Granulocyte-macrophage colony-stimulating factor (CSF) and macrophage CSF-dependent macrophage phenotypes display differences in cytokine profiles and transcription factor activities: implications for CSF blockade in inflammation. J Immunol 2007;178:5245-5252
30. Agro A, Jordana M, Chan KH, et al. Synoviocyte derived granulocyte macrophage colony stimulating factor mediates the survival of human lymphocytes. J Rheumatol 1992;19:1065-1069
31. Alvaro-Gracia JM, Zvaifler NJ, Brown CB, Kaushansky K, Firestein GS. Cytokines in chronic inflammatory arthritis. VI. Analysis of the synovial cells involved in granulocyte-macrophage colony-stimulating factor production and gene expression in rheumatoid arthritis and its regulation by IL-1 and tumor necrosis factor-alpha. J Immunol 1991;146:3365-3371
32. Guzik TJ, Mussa S, Gastaldi D, et al. Mechanisms of increased vascular superoxide production in human diabetes mellitus: role of NAD (P) H oxidase and endothelial nitric oxide synthase. Circulation 2002;105:1656-1662
33. Hink U, Li H, Mollnau H, et al. Mechanisms underlying endothelial dysfunction in diabetes mellitus. Circ Res 2001;88:E14-E22
34. Nagareddy PR, Xia Z, McNeill JH, MacLeod KM. Increased expression of iNOS is associated with endothelial dysfunction and impaired pressor responsiveness in streptozotocin-induced diabetes. Am J Physiol Heart Circ Physiol 2005;289:H2144-H2152
35. Gunnett CA, Lund DD, Chu Y, Brooks RM 2nd, Faraci FM, Heistad DD. NO-dependent vasorelaxation is impaired after gene transfer of inducible NO-synthase. Arterioscler Thromb Vasc Biol 2001;21:1281-1287
36. Gunnett CA, Heistad DD, Faraci FM. Gene-targeted mice reveal a critical role for inducible nitric oxide synthase in vascular dysfunction during diabetes. Stroke 2003;34:2970-2974
37. Ito K, Hirao A, Arai F, et al. Reactive oxygen species act through p38 MAPK to limit the lifespan of hematopoietic stem cells. Nat Med 2006;12:446-451
38. Urao N, Inomata H, Razvi M, et al. Role of nox2-based NADPH oxidase in bone marrow and progenitor cell function involved in neovascularization induced by hindlimb ischemia. Circ Res 2008;103:212-220
39. Jang YY, Sharkis SJ. A low level of reactive oxygen species selects for primitive hematopoietic stem cells that may reside in the low-oxygenic niche. Blood 2007;110:3056-3063
40. Piccoli C, D'Aprile A, Ripoli M, et al. Bone-marrow derived hematopoietic stem/progenitor cells express multiple isoforms of NADPH oxidase and produce constitutively reactive oxygen species. Biochem Biophys Res Commun 2007;353:965-972
41. Tack CJ, Van Gurp PJ, Holmes C, Goldstein DS. Local sympathetic denervation in painful diabetic neuropathy. Diabetes 2002;51:3545-3553
42. Britland ST, Young RJ, Sharma AK, Clarke BF. Association of painful and painless diabetic polyneuropathy with different patterns of nerve fiber degeneration and regeneration. Diabetes 1990;39:898-908
43. Korsching S, Thoenen H. Developmental changes of nerve growth factor levels in sympathetic ganglia and their target organs. Dev Biol 1988;126:40-46
44. Fehér E, Batbayar B, Vér A, Zelles T. Changes of the different neuropeptidecontaining nerve fibers and immunocells in the diabetic rat's alimentary tract. Ann N Y Acad Sci 2006;1084:280-295
45. Donnerer J, Schuligoi R, Stein C. Increased content and transport of substance P and calcitonin gene-related peptide in sensory nerves innervating inflamed tissue: evidence for a regulatory function of nerve growth factor in vivo. Neuroscience 1992;49:693-698
46. Schmidt RE, Dorsey DA, Beaudet LN, Parvin CA, Zhang W, Sima AA. Experimental rat models of types 1 and 2 diabetes differ in sympathetic neuroaxonal dystrophy. J Neuropathol Exp Neurol 2004;63:450-460
47. Schmidt RE, Dorsey DA, Beaudet LN, Peterson RG. Analysis of the Zucker Diabetic Fatty (ZDF) type 2 diabetic rat model suggests a neurotrophic role for insulin/IGF-I in diabetic autonomic neuropathy. Am J Pathol 2003;163:21-28
48. Tan AM, Samad OA, Fischer TZ, Zhao P, Persson AK, Waxman SG. Maladaptive dendritic spine remodeling contributes to diabetic neuropathic pain. J Neurosci 2012;32:6795-6807
49. Oomen SP, Van Hennik PB, Antonissen C, et al. Somatostatin is a selective chemoattractant for primitive (CD34 (+)) hematopoietic progenitor cells. Exp Hematol 2002;30:116-125
50. Solomou K, Ritter MA, Palmer DB. Somatostatin is expressed in the murine thymus and enhances thymocyte development Eur J Immunol 2002;32:1550-1559
51. Talme T, Ivanoff J, Sundqvist KG. Somatostatin is a specific inhibitor of SDF-1alpha-induced T cell infiltration. Clin Exp Immunol 2004;135:434-439
52. Lambert GW, Straznicky NE, Lambert EA, Dixon JB, Schlaich MP. Sympathetic nervous activation in obesity and the metabolic syndrome-causes, consequences and therapeutic implications. Pharmacol Ther 2010;126:159-172
53. Bedoui S, Miyake S, Lin Y, et al. Neuropeptide Y (NPY) suppresses experimental autoimmune encephalomyelitis: NPY1 receptor-specific inhibition of autoreactive Th1 responses in vivo. J Immunol 2003;171:3451-3458
54. Singer K, Morris DL, Oatmen KE, et al. Neuropeptide Y is produced by adipose tissue macrophages and regulates obesity-induced inflammation. PLoS One 2013;8:e57929
55. Wheway J, Herzog H, Mackay F. The Y1 receptor for NPY: a key modulator of the adaptive immune system. Peptides 2007;28:453-458
56. Garrett NE, Malcangio M, Dewhurst M, Tomlinson DR. alpha-Lipoic acid corrects neuropeptide deficits in diabetic rats via induction of trophic support. Neurosci Lett 1997;222:191-194
57. Ahmad T, Ugarph-Morawski A, Li J, et al. Bone and joint neuropathy in rats with type-2 diabetes. Regul Pept 2004;119:61-67
58. Krings A, Rahman S, Huang S, Lu Y, Czernik PJ, Lecka-Czernik B. Bone marrow fat has brown adipose tissue characteristics, which are attenuated with aging and diabetes. Bone 2012;50:546-552
59. Gimble JM, Nuttall ME. Bone and fat: old questions, new insights. Endocrine 2004;23:183-188
60. Lecka-Czernik B. Marrow fat metabolism is linked to the systemic energy metabolism. Bone 2012;50:534-539
61. Naveiras O, Nardi V, Wenzel PL, Hauschka PV, Fahey F, Daley GQ. Bonemarrow adipocytes as negative regulators of the haematopoietic microenvironment. Nature 2009;460:259-263
62. Gimble JM, Nuttall ME. The relationship between adipose tissue and bone metabolism. Clin Biochem 2012;45:874-879
63. Omatsu Y, Sugiyama T, Kohara H, et al. The essential functions of adipoosteogenic progenitors as the hematopoietic stem and progenitor cell niche. Immunity 2010;33:387-399
64. Belaid-Choucair Z, Lepelletier Y, Poncin G, et al. Human bone marrow adipocytes block granulopoiesis through neuropilin-1-induced granulocyte colony-stimulating factor inhibition. Stem Cells 2008;26:1556-1564