Digestion products of the PH20 hyaluronidase inhibit remyelination

Annals of Neurology

Volumn 73, Issue 2, 2013, Pages 266-280

  Preston, Marnie ^a   Gong, Xi ^b   Su, Weiping ^a   Matsumoto, Steven G ^a,c   Banine, Fatima ^a   Winkler, Clayton ^a   Foster, Scott ^a   Xing, Rubing ^a   Struve, Jaime ^a   Dean, Justin ^b   Baggenstoss, Bruce ^d   Weigel, Paul H ^d   Montine, Thomas J ^e   Back, Stephen A ^b,f   Sherman, Larry S ^a,c  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

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

^e UNIVERSITY OF WASHINGTON   (United States)

^f OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYALURONIDASE;

ANIMAL CELL; ARTICLE; CELL MATURATION; CONTROLLED STUDY; ENZYME ACTIVITY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NEURAL STEM CELL; NONHUMAN; OLIGODENDROCYTE PROGENITOR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REMYELINIZATION;

ACTION POTENTIALS; ANIMALS; CELL ADHESION MOLECULES; CELL DIFFERENTIATION; CELLS, CULTURED; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; ENZYME INHIBITORS; FEMALE; HYALURONIC ACID; HYALURONOGLUCOSAMINIDASE; LYSOPHOSPHATIDYLCHOLINES; MICE; MICE, INBRED C57BL; MYELIN SHEATH; NERVE REGENERATION; NEURAL STEM CELLS; OLIGODENDROGLIA;

EID: 84875417448     PISSN: 03645134     EISSN: 15318249     Source Type: Journal    
DOI: 10.1002/ana.23788     Document Type: Article

References (55)

1. Franklin RJ, Ffrench-Constant C,. Remyelination in the CNS: from biology to therapy. Nat Rev Neurosci 2008; 9: 839-855.
2. Wolswijk G,. Chronic stage multiple sclerosis lesions contain a relatively quiescent population of oligodendrocyte precursor cells. J Neurosci 1998; 18: 601-609.
3. Scolding N, Franklin R, Stevens S, et al. Oligodendrocyte progenitors are present in the normal adult human CNS and in the lesions of multiple sclerosis. Brain 1998; 121 (pt 12): 2221-2228.
4. Chang A, Nishiyama A, Peterson J, et al. NG2-positive oligodendrocyte progenitor cells in adult human brain and multiple sclerosis lesions. J Neurosci 2000; 20: 6404-6412.
5. Maeda Y, Solanky M, Menonna J, et al. Platelet-derived growth factor-alpha receptor-positive oligodendroglia are frequent in multiple sclerosis lesions. Ann Neurol 2001; 49: 776-785.
6. Chang A, Tourtellotte WW, Rudick R, Trapp BD,. Premyelinating oligodendrocytes in chronic lesions of multiple sclerosis. N Engl J Med 2002; 346: 165-173.
7. Wolswijk G,. Oligodendrocyte precursor cells in the demyelinated multiple sclerosis spinal cord. Brain 2000; 125 (pt 2): 338-349.
8. Kotter MR, Stadelmann C, Hartung HP,. Enhancing remyelination in disease-can we wrap it up? Brain 2011; 134 (pt 7): 1882-1900.
9. Kremer D, Aktas O, Hartung HP, Küry P,. The complex world of oligodendroglial differentiation inhibitors. Ann Neurol 2011; 69: 602-618.
10. Sherman LS, Back SA,. A 'GAG' reflex prevents repair of the damaged CNS. Trends Neurosci 2008; 31: 44-52.
11. Preston M, Sherman LS,. Neural stem cell niches: roles for the hyaluronan-based extracellular matrix. Front Biosci (Schol Ed) 2011; 3: 1165-1179.
12. Back SA, Tuohy TM, Chen H, et al. Hyaluronan accumulates in demyelinated lesions and inhibits oligodendrocyte progenitor maturation. Nat Med 2005; 11: 966-972.
13. Struve J, Maher PC, Li YQ, et al. Disruption of the hyaluronan-based extracellular matrix in spinal cord promotes astrocyte proliferation. Glia 2005; 52: 16-24.
14. Buser JR, Maire J, Riddle A, et al. Arrested pre-oligodendrocyte maturation contributes to myelination failure in premature infants. Ann Neurol 2012; 71: 93-109.
15. Back SA, Kroenke CD, Sherman LS, et al. White matter lesions defined by diffusion tensor imaging in older adults. Ann Neurol 2011; 70: 465-476.
16. Cargill R, Kohama SG, Struve J, et al. Astrocytes in aged nonhuman primate brain gray matter synthesize excess hyaluronan. Neurobiol Aging 2012; 33: 830.e13-830.e24.
17. Jiang D, Liang J, Noble PW,. Hyaluronan as an immune regulator in human diseases. Physiol Rev 2001; 91: 221-264.
18. Soltés L, Mendichi R, Kogan G, et al. Degradative action of reactive oxygen species on hyaluronan. Biomacromolecules 2006; 7: 659-668.
19. Al'Qteishat A, Gaffney J, Krupinski J, et al. Changes in hyaluronan production and metabolism following ischaemic stroke in man. Brain 2006; 129 (pt 8): 2158-2176.
20. Sloane JA, Batt C, Ma Y, et al. Hyaluronan blocks oligodendrocyte progenitor maturation and remyelination through TLR2. Proc Natl Acad Sci U S A 2010; 107: 11555-11560.
21. Marret S, Delpech B, Delpech A, et al. Expression and effects of hyaluronan and of the hyaluronan-binding protein hyaluronectin in newborn rat brain glial cell cultures. J Neurochem 1994; 62: 1285-1295.
22. Lee HG, Cowman MK,. An agarose gel electrophoretic method for analysis of hyaluronan molecular weight distribution. Anal Biochem 1994; 219: 278-287.
23. Botzki A, Rigden DJ, Braun S, et al. L-Ascorbic acid 6-hexadecanoate, a potent hyaluronidase inhibitor. X-ray structure and molecular modeling of enzyme-inhibitor complexes. J Biol Chem 2004; 279: 45990-45997.
24. Baggenstoss BA, Weigel PH,. Size exclusion chromatography-multiangle laser light scattering analysis of hyaluronan size distributions made by membrane-bound hyaluronan synthase. Anal Biochem 2006; 352: 243-251.
25. Dissen GA, Lomniczi A, Neff TL, et al. In vivo manipulation of gene expression in non-human primates using lentiviral vectors as delivery vehicles. Methods 2009; 49: 70-77.
26. Atmuri V, Martin DC, Hemming R, et al. Hyaluronidase 3 (HYAL3) knockout mice do not display evidence of hyaluronan accumulation. Matrix Biol 2008; 27: 653-660.
27. Zhang SC, Lundberg C, Lipsitz D, et al. Generation of oligodendroglial progenitors from neural stem cells. J Neurocytol 1998; 27: 475-489.
28. Meyer MF, Kreil G, Aschauer H,. The soluble hyaluronidase from bull testes is a fragment of the membrane-bound PH-20 enzyme. FEBS Lett 1997; 413: 385-388.
29. Phelps B, Myles DG,. The guinea pig sperm plasma membrane protein, PH-20, reaches the surface via two transport pathways and becomes localized to a domain after an initial uniform distribution. Dev Biol 1987; 123: 63-72.
30. Jones MH, Davey PM, Aplin H, Affara NA,. Expression analysis, genomic structure, and mapping to 7q31 of the human sperm adhesion molecule gene SPAM1. Genomics 1995; 29: 796-800.
31. Jones R, Ma A, Hou ST, et al. Testicular biosynthesis and epididymal endoproteolytic processing of rat sperm surface antigen 2B1. J Cell Sci 1996; 109 (pt 10): 2561-2570.
32. Zheng Y, Martin-DeLeon PA,. The mouse Spam1 gene: RNA expression pattern and lower steady-state level associated with the Rb(6.16) translocation. Mol Reprod Dev 1997; 46: 252-257.
33. Wang H, Zhan Y, Xu L, et al. Use of suppression subtractive hybridization for differential gene expression in stroke: discovery of CD44 gene expression and localization in permanent focal stroke in rats. Stroke 2011; 32: 1020-1027.
34. Jenkins HG, Bachelard HS,. Developmental and age-related changes in rat brain glycosaminoglycans. J Neurochem 1988; 51: 1634-1640.
35. Jenkins HG, Bachelard HS,. Glycosaminoglycans in cortical autopsy samples from Alzheimer brain. J Neurochem 1988; 51: 1641-1645.
36. Suzuki K, Katzman R, Korey SR,. Chemical studies on Alzheimer's disease. J Neuropathol Exp Neurol 1965; 24: 211-224.
37. Contreras EG, Gaete M, Sánchez N, et al. Early requirement of hyaluronan for tail regeneration in Xenopus tadpoles. Development 2009; 136: 2987-2996.
38. Fancy SP, Baranzini SE, Zhao C, et al. Dysregulation of the Wnt pathway inhibits timely myelination and remyelination in the mammalian CNS. Genes Dev 2009; 23: 1571-1585.
39. Feigenson K, Reid M, See J, et al. Wnt signaling is sufficient to perturb oligodendrocyte maturation. Mol Cell Neurosci 2009; 42: 255-265.
40. Azim K, Butt AM,. GSK3β negatively regulates oligodendrocyte differentiation and myelination in vivo. Glia 2011; 59: 540-553.
41. Tawk M, Makoukji J, Belle M, et al. Wnt/beta-catenin signaling is an essential and direct driver of myelin gene expression and myelinogenesis. J Neurosci 2011; 31: 3729-3742.
42. Termeer C, Benedix F, Sleeman J, et al. Oligosaccharides of hyaluronan activate dendritic cells via toll-like receptor 4. J Exp Med 2002; 195: 99-111.
43. Taylor KR, Trowbridge JM, Rudisill JA, et al. Hyaluronan fragments stimulate endothelial recognition of injury through TLR4. J Biol Chem 2004; 279: 17079-17084.
44. Jiang D, Liang J, Fan Y, et al. Regulation of lung injury and repair by Toll-like receptors and hyaluronan. Nat Med 2005; 11: 1173-1179.
45. Scheibner KA, Lutz MA, Boodoo S, et al. Hyaluronan fragments act as an endogenous danger signal by engaging TLR2. J Immunol 2006; 177: 1272-1281.
46. Shimada M, Yanai Y, Okazaki T, et al. Hyaluronan fragments generated by sperm-secreted hyaluronidase stimulate cytokine/chemokine production via the TLR2 and TLR4 pathway in cumulus cells of ovulated COCs, which may enhance fertilization. Development 2008; 135: 2001-2011.
47. Kim JS, Yeo S, Shin DG, et al. Glycogen synthase kinase 3beta and beta-catenin pathway is involved in toll-like receptor 4-mediated NADPH oxidase 1 expression in macrophages. FEBS J 2010; 277: 2830-2837.
48. Zhang P, Katz J, Michalek SM,. Glycogen synthase kinase-3beta (GSK3beta) inhibition suppresses the inflammatory response to Francisella infection and protects against tularemia in mice. Mol Immunol 2009; 46: 677-687.
49. Wang Y, Cheng X, He Q, et al. Astrocytes from the contused spinal cord inhibit oligodendrocyte differentiation of adult oligodendrocyte precursor cells by increasing the expression of bone morphogenetic proteins. J Neurosci 2011; 31: 6053-6058.
50. Mi S, Hu B, Hahm K, et al. LINGO-1 antagonist promotes spinal cord remyelination and axonal integrity in MOG-induced experimental autoimmune encephalomyelitis. Nat Med 2007; 13: 1228-1233.
51. Stern R, Jedrzejas MJ,. Hyaluronidases: their genomics, structures, and mechanisms of action. Chem Rev 2006; 106: 818-839.
52. Martin DC, Atmuri V, Hemming RJ, et al. A mouse model of human mucopolysaccharidosis IX exhibits osteoarthritis. Hum Mol Genet 2008; 17: 1904-1915.
53. Triggs-Raine B, Salo TJ, Zhang H, et al. Mutations in HYAL1, a member of a tandemly distributed multigene family encoding disparate hyaluronidase activities, cause a newly described lysosomal disorder, mucopolysaccharidosis IX. Proc Natl Acad Sci U S A 1999; 96: 6296-6300.
54. Jadin L, Wu X, Ding H, et al. Skeletal and hematological anomalies in HYAL2-deficient mice: a second type of mucopolysaccharidosis IX? FASEB J 2008; 22: 4316-4326.
55. Baba D, Kashiwabara S, Honda A, et al. Mouse sperm lacking cell surface hyaluronidase PH-20 can pass through the layer of cumulus cells and fertilize the egg. J Biol Chem 2002; 277: 30310-30314.