Role of Acid Sphingomyelinase in Shifting the Balance between Proinflammatory and Reparative Bone Marrow Cells in Diabetic Retinopathy

Stem Cells

Volumn 34, Issue 4, 2016, Pages 972-983

  Chakravarthy, Harshini ^a   Navitskaya, Svetlana ^a   O'Reilly, Sandra ^a   Gallimore, Jacob ^a   Mize, Hannah ^a   Beli, Eleni ^b   Wang, Qi ^a   Kady, Nermin ^a   Huang, Chao ^a   Blanchard, Gary J ^a   Grant, Maria B ^b   Busik, Julia V ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b INDIANA UNIVERSITY   (United States)

Author keywords

Bone marrow transplantation; Diabetic retinopathy; Dyslipidemias; Sphingolipids; Vascular system injuries

Indexed keywords

CERAMIDE; CYTOKINE; SPHINGOMYELIN; SPHINGOMYELIN PHOSPHODIESTERASE; ACID SPHINGOMYELINASE-1; SPHINGOLIPID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CELL ACTIVATION; CELL HOMING; CELL MEMBRANE; CELL MEMBRANE FLUIDITY; CELL MIGRATION; CIRCULATING ANGIOGENIC CELL; CONTROLLED STUDY; DIABETIC RETINOPATHY; ENZYME INHIBITION; MALE; MEMBRANE VESICLE; MICROGLIA; MONOCYTE; MOUSE; NONHUMAN; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; DIABETES MELLITUS, EXPERIMENTAL; DISEASE MODEL; ENDOTHELIUM CELL; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; INFLAMMATION; METABOLISM; PATHOLOGY; RETINA; RETINA BLOOD VESSEL;

ANIMALS; BONE MARROW CELLS; CERAMIDES; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC RETINOPATHY; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; HUMANS; INFLAMMATION; MICE; MONOCYTES; RETINA; RETINAL VESSELS; SPHINGOLIPIDS; SPHINGOMYELIN PHOSPHODIESTERASE;

EID: 84953242795     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.2259     Document Type: Article

References (58)

1. Antonetti DA, Klein R, Gardner TW,. Diabetic retinopathy. N Engl J Med 2012; 366: 1227-1239.
2. Kern TS,. Contributions of inflammatory processes to the development of the early stages of diabetic retinopathy. Exp Diabetes Res 2007; 2007: 95103.
3. Mohr S,. Potential new strategies to prevent the development of diabetic retinopathy. Expert Opin Investig Drugs 2004; 13: 189-198.
4. Busik JV, Mohr S, Grant MB,. Hyperglycemia-induced reactive oxygen species toxicity to endothelial cells is dependent on paracrine mediators. Diabetes 2008; 57: 1952-1965.
5. Abcouwer SF,. Angiogenic factors and cytokines in diabetic retinopathy. J Clin Cell Immunol 2013;(suppl 1).
6. Li G, Veenstra AA, Talahalli RR, et al., Marrow-derived cells regulate the development of early diabetic retinopathy and tactile allodynia in mice. Diabetes 2012; 61: 3294-3303.
7. Schroder S, Palinski W, Schmid-Schonbein GW,. Activated monocytes and granulocytes, capillary nonperfusion, and neovascularization in diabetic retinopathy. Am J Pathol 1991; 139: 81-100.
8. Hinze A, Stolzing A,. Differentiation of mouse bone marrow derived stem cells toward microglia-like cells. BMC Cell Biol 2011; 12: 35.
9. Soulet D, Rivest S,. Bone-marrow-derived microglia: Myth or reality? Curr Opin Pharmacol 2008; 8: 508-518.
10. 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.
11. 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.
12. Loomans CJ, de Koning EJ, Staal FJ, et al., Endothelial progenitor cell dysfunction: A novel concept in the pathogenesis of vascular complications of type 1 diabetes. Diabetes 2004; 53: 195-199.
13. Tikhonenko M, Lydic TA, Opreanu M, et al., N-3 polyunsaturated fatty acids prevent diabetic retinopathy by inhibition of retinal vascular damage and enhanced endothelial progenitor cell reparative function. PLoS One 2013; 8: e55177.
14. Segal MS, Shah R, Afzal A, et al., Nitric oxide cytoskeletal-induced alterations reverse the endothelial progenitor cell migratory defect associated with diabetes. Diabetes 2006; 55: 102-109.
15. Shaw LC, Neu MB, Grant MB,. Cell-based therapies for diabetic retinopathy. Curr Diabetes Rep 2011; 11: 265-274.
16. Kim C, Schneider G, Abdel-Latif A, et al., Ceramide-1-phosphate regulates migration of multipotent stromal cells (MSCs) and endothelial progenitor cells (EPCs)-Implications for tissue regeneration. Stem Cells 2013; 31: 500-510.
17. Tongers J, Roncalli JG, Losordo DW,. Therapeutic angiogenesis for critical limb ischemia: Microvascular therapies coming of age. Circulation 2008; 118: 9-16.
18. Lyons TJ, Jenkins AJ, Zheng D, et al., Diabetic retinopathy and serum lipoprotein subclasses in the DCCT/EDIC cohort. Invest Ophthalmol Vis Sci 2004; 45: 910-918.
19. Chew EY, Ambrosius WT, Davis MD, et al., Effects of medical therapies on retinopathy progression in type 2 diabetes. New Engl J Med 2010; 363: 233-244.
20. Opreanu M, Tikhonenko M, Bozack S, et al., The unconventional role of acid sphingomyelinase in regulation of retinal microangiopathy in diabetic human and animal models. Diabetes 2011; 60: 2370-2378.
21. Fox TE, Bewley MC, Unrath KA, et al., Circulating sphingolipid biomarkers in models of type 1 diabetes. J Lipid Res 2011; 52: 509-517.
22. Fox TE, Han X, Kelly S, et al., Diabetes alters sphingolipid metabolism in the retina: A potential mechanism of cell death in diabetic retinopathy. Diabetes 2006; 55: 3573-3580.
23. Busik JV, Esselman WJ, Reid GE,. Examining the role of lipid mediators in diabetic retinopathy. Clin Lipidol 2012; 7: 661-675.
24. Maines LW, French KJ, Wolpert EB, et al., Pharmacologic manipulation of sphingosine kinase in retinal endothelial cells: Implications for angiogenic ocular diseases. Invest Ophthalmol Vis Sci 2006; 47: 5022-5031.
25. Opreanu M, Lydic TA, Reid GE, et al., Inhibition of cytokine signaling in human retinal endothelial cells through downregulation of sphingomyelinases by docosahexaenoic acid. Invest Ophthalmol Vis Sci 2010; 51: 3253-3263.
26. Kielczewski JL, Calzi SL, Shaw LC, et al., Free Insulin-like growth factor binding protein-3 (IGFBP-3) reduces retinal vascular permeability in association with a reduction of acid sphingomyelinase (ASMase). Invest Ophthalmol Vis Sci 2011; 52: 8278-8286.
27. Medina RJ, O'Neill CL, O'Doherty TM, et al., Myeloid angiogenic cells act as alternative M2 macrophages and modulate angiogenesis through interleukin-8. Mol Med 2011; 17: 1045-1055.
28. Lapinski MM, Blanchard GJ,. Interrogating the role of liposome size in mediating the dynamics of a chromophore in the acyl chain region of a phospholipid bilayer. Chem Phys Lipids 2008; 153: 130-137.
29. Lydic TA, Busik JV, Reid GE,. A monophasic extraction strategy for the simultaneous lipidome analysis of polar and nonpolar retina lipids. J Lipid Res 2014; 55: 1797-1809.
30. Rungger-Brandle E, Dosso AA, Leuenberger PM,. Glial reactivity, an early feature of diabetic retinopathy. Invest Ophthalmol Vis Sci 2000; 41: 1971-1980.
31. Zeng XX, Ng YK, Ling EA,. Neuronal and microglial response in the retina of streptozotocin-induced diabetic rats. Vis Neurosci 2000; 17: 463-471.
32. Barber AJ, Antonetti DA, Kern TS, et al., The Ins2Akita mouse as a model of early retinal complications in diabetes. Invest Ophthalmol Vis Sci 2005; 46: 2210-2218.
33. Martin PM, Roon P, Van Ells TK, et al., Death of retinal neurons in streptozotocin-induced diabetic mice. Invest Ophthalmol Vis Sci 2004; 45: 3330-3336.
34. Feit-Leichman RA, Kinouchi R, Takeda M, et al., Vascular damage in a mouse model of diabetic retinopathy: Relation to neuronal and glial changes. Invest Ophthalmol Vis Sci 2005; 46: 4281-4287.
35. Catapano ER, Arriaga LR, Espinosa G, et al., Solid character of membrane ceramides: A surface rheology study of their mixtures with sphingomyelin. Biophys J 2011; 101: 2721-2730.
36. Hla T,. Physiological and pathological actions of sphingosine 1-phosphate. Semin Cell Dev Biol 2004; 15: 513-520.
37. Boulgaropoulos B, Rappolt M, Sartori B, et al., Lipid sorting by ceramide and the consequences for membrane proteins. Biophys J 2012; 102: 2031-2038.
38. Dannhausen K, Karlstetter M, Caramoy A, et al., Acid sphingomyelinase (aSMase) deficiency leads to abnormal microglia behavior and disturbed retinal function. Biochem Biophys Res Commun 2015; 464: 434-440.
39. Horinouchi K, Erlich S, Perl DP, et al., Acid sphingomyelinase deficient mice: A model of types A and B Niemann-Pick disease. Nat Genet 1995; 10: 288-293.
40. Tang J, Kern TS,. Inflammation in diabetic retinopathy. Prog Retin Eye Res 2011; 30: 343-358.
41. Marchetti V, Yanes O, Aguilar E, et al., Differential macrophage polarization promotes tissue remodeling and repair in a model of ischemic retinopathy. Sci Rep 2011; 1: 76.
42. Caballero S, Sengupta N, Afzal A, et al., Ischemic vascular damage can be repaired by healthy, but not diabetic, endothelial progenitor cells. Diabetes 2007; 56: 960-967.
43. Said G,. Focal and multifocal diabetic neuropathies. Arq neuro-psiquiatr. 2007; 65: 1272-1278.
44. 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.
45. Li Calzi S, Purich DL, Chang KH, et al., Carbon monoxide and nitric oxide mediate cytoskeletal reorganization in microvascular cells via vasodilator-stimulated phosphoprotein phosphorylation: Evidence for blunted responsiveness in diabetes. Diabetes 2008; 57: 2488-2494.
46. Jarajapu YP, Hazra S, Segal M, et al., Vasoreparative dysfunction of CD34 + cells in diabetic individuals involves hypoxic desensitization and impaired autocrine/paracrine mechanisms. PLoS One 2014; 9: e93965.
47. Golan K, Vagima Y, Ludin A, et al., S1P promotes murine progenitor cell egress and mobilization via S1P1-mediated ROS signaling and SDF-1 release. Blood 2012; 119: 2478-2488.
48. Kim CH, Wu W, Wysoczynski M, et al., Conditioning for hematopoietic transplantation activates the complement cascade and induces a proteolytic environment in bone marrow: A novel role for bioactive lipids and soluble C5b-C9 as homing factors. Leukemia 2012; 26: 106-116.
49. Ginhoux F, Lim S, Hoeffel G, et al., Origin and differentiation of microglia. Front Cell Neurosci 2013; 7: 45.
50. Ajami B, Bennett JL, Krieger C, et al., Local self-renewal can sustain CNS microglia maintenance and function throughout adult life. Nat Neurosci 2007; 10: 1538-1543.
51. Bianco F, Perrotta C, Novellino L, et al., Acid sphingomyelinase activity triggers microparticle release from glial cells. EMBO J 2009; 28: 1043-1054.
52. Garcia-Barros M, Paris F, Cordon-Cardo C, et al., Tumor response to radiotherapy regulated by endothelial cell apoptosis. Science 2003; 300: 1155-1159.
53. Kolesnick R, Fuks Z,. Radiation and ceramide-induced apoptosis. Oncogene 2003; 22: 5897-5906.
54. Stancevic B, Kolesnick R,. Ceramide-rich platforms in transmembrane signaling. FEBS Lett 2010; 584: 1728-1740.
55. Grassme H, Riethmuller J, Gulbins E,. Biological aspects of ceramide-enriched membrane domains. Prog Lipid Res 2007; 46: 161-170.
56. Pfeiffer A, Bottcher A, Orso E, et al., Lipopolysaccharide and ceramide docking to CD14 provokes ligand-specific receptor clustering in rafts. Eur J Immunol 2001; 31: 3153-3164.
57. Goni FM, Alonso A,. Biophysics of sphingolipids I. Membrane properties of sphingosine, ceramides and other simple sphingolipids. Biochim Biophys Acta 2006; 1758: 1902-1921.
58. Song J, Waugh RE,. Bending rigidity of SOPC membranes containing cholesterol. Biophys J 1993; 64: 1967-1970.