Clinical and immunopathologic alterations in rhesus macaques affected with globoid cell leukodystrophy

American Journal of Pathology

Volumn 172, Issue 1, 2008, Pages 98-111

  Borda, Juan T ^a   Alvarez, Xavier ^a   Mohan, Mahesh ^a   Ratterree, Marion S ^a   Phillippi Falkenstein, Kathrine ^a   Lackner, Andrew A ^a   Bunnell, Bruce A ^a,b,c  

^a TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

^b TULANE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^c TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD163 ANTIGEN; CD68 ANTIGEN; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUCOSE TRANSPORTER 5; HLA DR3 ANTIGEN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; ATAXIA; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DEMYELINATION; FEMALE; GENE EXPRESSION; GLIOSIS; GLOBOID CELL LEUKODYSTROPHY; HISTOCHEMISTRY; HISTOPATHOLOGY; HYPERMETROPIA; IMMUNOHISTOLOGY; IMMUNOPHENOTYPING; LIMB TREMOR; LUNG DISEASE; MACROPHAGE; MALE; MICROGLIA; MONOCYTE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RHESUS MONKEY; TREMOR; WHITE MATTER;

EID: 38749109232     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.2353/ajpath.2008.070404     Document Type: Article

References (74)

1. Wenger DA, Rafi MA, Luzi P: Molecular genetics of Krabbe disease (globoid cell leukodystrophy): diagnostic and clinical implications. Hum Mutat 1997, 10:268-279
2. Suzuki K: Twenty five years of the "psychosine hypothesis": a personal perspective of its history and present status. Neurochem Res 1998, 23:251-259
3. Suzuki K: Globoid cell leukodystrophy (Krabbe disease): update. J Child Neurol 2003, 18:595-603
4. Wenger DA: Murine, canine and non-human primate models of Krabbe disease. Mol Med Today 2000, 6:449-451
5. Wenger DA, Sattler M, Hiatt W: Globoid cell leukodystrophy: deficiency of lactosyl ceramide beta-galactosidase, Proc Natl Acad Sci USA 1974, 71:854-857
6. Wenger DA, Victoria T, Rafi MA, Luzi P, Vanier MT, Vite C, Patterson DF, Haskins MH: Globoid cell leukodystrophy in Cairn and West Highland white terriers. J Hered 1999, 90:138-142
7. Wenger DA, Suzuki K, Suzuki Y, Suzuki, K: Galactosylceramide lipidosis: globoid cell leukodystrophy (Krabbe disease). The Metabolic and Molecular Bases of Inherited Disease. Edited by Scriver CR, Beaudet AL, Sly WS, Valle D, Childs B, Kinzler KW, Vogelstein B. New York, McGraw-Hill, 2001, pp 3669-3687
8. Jesionek-Kupnicka D, Majchrowska A, Krawczyk J, Wendorff J, Barcikowska M, Lukaszek S, Liberski PP: Krabbe disease: an ultrastructural study of globoid cells and reactive astrocytes at the brain and optic nerves. Folia Neuropathol 1997, 35:155-162
9. Luzi P, Rafi MA, Victoria T, Baskin GB, Wenger DA: Characterization of the rhesus monkey galactocerebrosidase (GALC) cDNA and gene and identification of the mutation causing globoid cell leukodystrophy (Krabbe disease) in this primate. Genomics 1997, 42:319-324
10. Giri S, Jatana M, Rattan R, Won JS, Singh I, Singh AK: Galactosylsphingosine (psychosine)-induced expression of cytokine-mediated inducible nitric oxide synthases via AP-1 and C/EBP: implications for Krabbe disease. FASEB J 2002, 16:661-672
11. Sigurdson CJ, Basaraba RJ, Mazzaferro EM, Gould DH: Globoid cell-like leukodystrophy in a domestic longhaired cat. Vet Pathol 2002, 39:494-496
12. D'Agostino AN, Sayre GP, Hayles AB: Krabbe's disease. Globoid cell type of leukodystrophy, Arch Neurol 1963, 8:82-96
13. Gullotta F, Pavone L, Mollica F, Grasso S, Valenti C: Krabbe's disease with unusual clinical and morphological features. Neuropadiatrie 1979, 10:395-400
14. Hagberg B, Sourander P, Svennerholm L: Diagnosis of Krabbe's infantile leucodystrophy. J Neurol Neurosurg Psychiatry 1963, 26:195-198
15. Suzuki K, Suzuki K: The twitcher mouse. A model of human globoid cell leukodystrophy (Krabbe's disease). Am J Pathol 1983, 111:394-397
16. Suzuki K, Suzuki Y: Galactosylceramide lipidosis: Globoid cell leukodystrophy (Krabbe disease). The Metabolic Basis of Inherited Disease. Edited by Stanbury JW, Wyngaarden JB, Fredrickson DS, Goldstein JI, Brown MS. New York, McGraw Hill, 1983, pp 857-880
17. Suzuki K: Genetic galactosylceramidase deficiency (globoid cell leukodystrophy). Krabbe disease in different mammalian species. Neurochem Pathol 1985, 3:53-68
18. Kobayashi S, Chiu FC, Katayama M, Sacchi RS, Suzuki K: Expression of glial fibrillary acidic protein in the CNS and PNS of murine globoid cell leukodystrophy, the twitcher. Am J Pathol 1986, 125:227-243
19. Suzuki K: The twitcher mouse: a model for Krabbe disease and for experimental therapies. Brain Pathol 1995, 5:249-258
20. Baskin GB, Ratterree M, Davison BB, Falkenstein KP, Clarke MR, England JD, Vanier MT, Luzi P, Rafi MA, Wenger DA: Genetic galactocerebrosidase deficiency (globoid cell leukodystrophy, Krabbe disease) in rhesus monkeys (Macaca mulatta). Lab Anim Sci 1998, 48:476-482
21. Victoria T, Rafi MA, Wenger DA: Cloning of the canine GALC cDNA and identification of the mutation causing globoid cell leukodystrophy in West Highland White and Cairn terriers. Genomics 1996, 33:457-462
22. Weimer MB, Gutierrez A, Baskin GB, Borda JT, Veazey RS, Myers L, Phillippi-Falkenstein KM, Bunnell BA, Ratterree MS, England JD: Serial electrophysiologic studies in rhesus monkeys with Krabbe disease. Muscle Nerve 2005, 32:185-190
23. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, Cooper NR, Eikelenboom P, Emmerling M, Fiebich BL, Finch CE, Frautschy S, Griffin WS, Hampel H, Hull M, Landreth G, Lue L, Mrak R, Mackenzie IR, McGeer PL, O'Banion MK, Pachter J, Pasinetti G, Plata-Salaman C, Rogers J, Rydel R, Shen Y, Streit W, Strohmeyer R, Tooyoma I, Van Muiswinkel FL, Veerhuis R, Walker D, Webster S, Wegrzyniak B, Wenk G, Wyss-Coray T: Inflammation and Alzheimer's disease. Neurobiol Aging 2000, 21:383-421
24. Akiyama H, Arai T, Kondo H, Tanno E, Haga C, Ikeda K: Cell mediators of inflammation in the Alzheimer disease brain, Alzheimer Dis Assoc Disord 2000, 14 Suppl 1:S47-S53
25. Frautschy SA, Yang F, Irrizarry M, Hyman B, Saido TC, Hsiao K, Cole GM: Microglial response to amyloid plaques in APPsw transgenic mice. Am J Pathol 1998, 152:307-317
26. Stoll G, Jander S: The role of microglia and macrophages in the pathophysiology of the CNS. Prog Neurobiol 1999, 58:233-247
27. Streit WJ, Conde JR, Harrison JK: Chemokines and Alzheimer's disease. Neurobiol Aging 2001, 22:909-913
28. Streit WJ: Microglia and Alzheimer's disease pathogenesis. J Neurosci Res 2004, 77:1-8
29. Pocock JM, Liddle AC: Microglial signalling cascades in neurodegenerative disease. Prog Brain Res 2001, 132:555-565
30. Streit WJ, Walter SA, Pennell NA: Reactive microgliosis. Prog Neurobiol 1999, 57:563-581
31. Williams K, Bar-Or A, Ulvestad E, Olivier A, Antel JP, Yong VW: Biology of adult human microglia in culture: comparisons with peripheral blood monocytes and astrocytes. J Neuropathol Exp Neurol 1992, 51:538-549
32. Ulvestad E, Williams K, Mork S, Antel J, Nyland H: Phenotypic differences between human monocytes/macrophages and microglial cells studied in situ and in vitro. J Neuropathol Exp Neurol 1994, 53:492-501
33. Ulvestad E, Williams K, Bjerkvig R, Tiekotter K, Antel J, Matre R: Human microglial cells have phenotypic and functional characteristics in common with both macrophages and dendritic antigen-presenting cells. J Leukoc Biol 1994, 56:732-740
34. Becher B, Antel JP: Comparison of phenotypic and functional properties of immediately ex vivo and cultured human adult microglia. Glia 1996, 18:1-10
35. Sedgwick JD, Schwender S, Imrich H, Dorries R, Butcher GW, ter Meulen V: Isolation and direct characterization of resident microglial cells from the normal and inflamed central nervous system, Proc Natl Acad Sci USA 1991, 88:7438-7442
36. Williams KC, Corey S, Westmoreland SV, Pauley D, Knight H, deBakker C, Alvarez X, Lackner AA: Perivascular macrophages are the primary cell type productively infected by simian immunodeficiency virus in the brains of macaques: implications for the neuropathogenesis of AIDS. J Exp Med 2001, 193:905-915
37. Champoux M, DeGregorio G, Schneider ML, Suomi SJ: Inanimate environmental enrichment for group-housed rhesus macaque infants. Am J Primatol 1990, 22:61-67
38. Schneider ML, Suomi SJ: The effect of mild stress during pregnancy on birthweight and neuromotor maturation in rhesus monkey infants (M. mulatta). Infant Behav Dev 1992, 15:389-403
39. Schneider ML, Suomi SJ: Neurobehavioral assessment in rhesus monkey neonates (Macaca mulatta): developmental changes, behavioral stability, and early experience. Infant Behav Dev 1992, 15:155-177
40. Borda JT, Alvarez X, Kondova I, Aye P, Simon MA, Desrosiers RC, Lackner AA: Cell tropism of simian immunodeficiency virus in culture is not predictive of in vivo tropism or pathogenesis. Am J Pathol 2004, 165:2111-2122
41. Babcock AM, Standing D, Bullshields K, Schwartz E, Paden CM, Poulsen DJ: In vivo inhibition of hippocampal Ca2+/calmodulin-dependent protein kinase II by RNA interference. Mol Ther 2005, 11:899-905
42. Mathew JS, Westmoreland S, Alvarez X, Simon MA, Pauley DR, MacKey JJ, Lackner AA: Expression of peripherin in the brain of macaques (Macaca mulatta and M. fascicularis) occurs in astrocytes rather than neurons and is associated with encephalitis. Neuropathol Appl Neurobiol 2001, 27:434-443
43. Friedenstein AJ, Deriglasova UF, Kulagina NN, Panasuk AF, Rudakowa SF, Luria EA, Ruadkow IA: Precursors for fibroblasts in different populations of hematopoietic cells as detected by the in vitro colony assay method. Exp Hematol 1974, 2:83-92
44. Williams K, Schwartz A, Corey S, Orandle M, Kennedy W, Thompson B, Alvarez X, Brown C, Gartner S, Lackner A: Proliferating cellular nuclear antigen expression as a marker of perivascular macrophages in simian immunodeficiency virus encephalitis. Am J Pathol 2002, 161:575-585
45. Horikoshi Y, Sasaki A, Taguchi N, Maeda M, Tsukagoshi H, Sato K, Yamaguchi H: Human GLUT5 immunolabeling is useful for evaluating microglial status in neuropathological study using paraffin sections. Acta Neuropathol (Berl) 2003, 105:157-162
46. Imai Y, Ibata I, Ito D, Ohsawa K, Kohsaka S: A novel gene iba1 in the major histocompatibility complex class III region encoding an EF hand protein expressed in a monocytic lineage. Biochem Biophys Res Commun 1996, 224:855-862
47. Nathan C: Inducible nitric oxide synthase: what difference does it make? J Clin Invest 1997, 100:2417-2423
48. Laroux FS, Pavlick KP, Hines IN, Kawachi S, Harada H, Bharwani S, Hoffman JM, Grisham MB: Role of nitric oxide in inflammation. Acta Physiol Scand 2001, 173:113-118
49. Conant K, Garzino-Demo A, Nath A, McArthur JC, Halliday W, Power C, Gallo RC, Major EO: Induction of monocyte chemoattractant protein-1 in HIV-1 Tat-stimulated astrocytes and elevation in AIDS dementia. Proc Natl Acad Sci USA 1998, 95:3117-3121
50. Van Der Voorn P, Tekstra J, Beelen RH, Tensen CP, Van Der Valk P, De Groot CJ: Expression of MCP-1 by reactive astrocytes in demyelinating multiple sclerosis lesions. Am J Pathol 1999, 154:45-51
51. Persidsky Y, Ghorpade A, Rasmussen J, Limoges J, Liu XJ, Stins M, Fiala M, Way D, Kim KS, Witte MH, Weinand M, Carhart L, Gendelman HE: Microglial and astrocyte chemokines regulate monocyte migration through the blood-brain barrier in human immunodeficiency virus-1 encephalitis. Am J Pathol 1999, 155:1599-1611
52. Alroy J, Warren CD, Raghavan SS, Kolodny EH: Animal models for lysosomal storage diseases: their past and future contribution. Hum Pathol 1989, 20:823-826
53. Itoh M, Hayashi M, Fujioka Y, Nagashima K, Morimatsu Y, Matsuyama H: Immunohistological study of globoid cell leukodystrophy. Brain Dev 2002, 24:284-290
54. Im DS, Heise CE, Nguyen T, O'Dowd BF, Lynch KR: Identification of a molecular target of psychosine and its role in globoid cell formation. J Cell Biol 2001, 153:429-434
55. Boyle EA, McGeer PL: Cellular immune response in multiple sclerosis plaques. Am J Pathol 1990, 137:575-584
56. McGeer PL, Kawamata T, Walker DG, Akiyama H, Tooyama I, McGeer EG: Microglia in degenerative neurological disease. Glia 1993, 7:84-92
57. Ulvestad E, Williams K, Vedeler C, Antel J, Nyland H, Mork S, Matre R: Reactive microglia in multiple sclerosis lesions have an increased expression of receptors for the Fc part of IgG. J Neurol Sci 1994, 121:125-131
58. Williams K, Ulvestad E, Waage A, Antel JP, McLaurin J: Activation of adult human derived microglia by myelin phagocytosis in vitro. J Neurosci Res 1994, 38:433-443
59. Sloane JA, Hollander W, Moss MB, Rosene DL, Abraham CR: Increased microglial activation and protein nitration in white matter of the aging monkey. Neurobiol Aging 1999, 20:395-405
60. Nathan C, Calingasan N, Nezezon J, Ding A, Lucia MS, La Perle K, Fuortes M, Lin M, Ehrt S, Kwon NS, Chen J, Vodovotz Y, Kipiani K, Beal MF: Protection from Alzheimer's-like disease in the mouse by genetic ablation of inducible nitric oxide synthase. J Exp Med 2005, 202:1163-1169
61. LeVine SM, Brown DC: IL-6 and TNFalpha expression in brains of twitcher, quaking and normal mice. J Neuroimmunol 1997, 73:47-56
62. Pedchenko TV, LeVine SM: IL-6 deficiency causes enhanced pathology in Twitcher (globoid cell leukodystrophy) mice. Exp Neurol 1999, 158:459-468
63. Merrill JE, Ignarro LJ, Sherman MP, Melinek J, Lane TE: Microglial cell cytotoxicity of oligodendrocytes is mediated through nitric oxide. J Immunol 1993, 151:2132-2141
64. Mitrovic B, Ignarro LJ, Montestruque S, Smoll A, Merrill JE: Nitric oxide as a potential pathological mechanism in demyelination: its differential effects on primary glial cells in vitro. Neuroscience 1994, 61:575-585
65. Mitrovic B, Ignarro LJ, Vinters HV, Akers MA, Schmid I, Uittenbogaart C, Merrill JE: Nitric oxide induces necrotic but not apoptotic cell death in oligodendrocytes. Neuroscience 1995, 65:531-539
66. Hisahara S, Shoji S, Okano H, Miura M: ICE/CED-3 family executes oligodendrocyte apoptosis by tumor necrosis factor. J Neurochem 1997, 69:10-20
67. Louis JC, Magal E, Takayama S, Varon S: CNTF protection of oligodendrocytes against natural and tumor necrosis factor-induced death. Science 1993, 259:689-692
68. Wing MG, Zajicek J, Seilly DJ, Compston DA, Lachmann PJ: Oligodendrocytes lack glycolipid anchored proteins which protect them against complement lysis. Restoration of resistance to lysis by incorporation of CD59, Immunology 1992, 76:140-145
69. Suarez I, Bodega G, Rubio M, Felipo V, Fernandez B: Neuronal and inducible nitric oxide synthase expression in the rat cerebellum following portacaval anastomosis. Brain Res 2005, 1047:205-213
70. Suarez I, Bodega G, Arilla E, Felipo V, Fernandez B: The expression of nNOS, iNOS and nitrotyrosine is increased in the rat cerebral cortex in experimental hepatic encephalopathy. Neuropathol Appl Neurobiol 2006, 32:594-604
71. Boje KM, Jaworowicz D, Jr., Raybon JJ: Neuroinflammatory role of prostaglandins during experimental meningitis: evidence suggestive of an in vivo relationship between nitric oxide and prostaglandins. J Pharmacol Exp Ther 2003, 304:319-325
72. Murphy S, Simmons ML, Agullo L, Garcia A, Feinstein DL, Galea E, Reis DJ, Minc-Golomb D, Schwartz JP: Synthesis of nitric oxide in CNS glial cells. Trends Neurosci 1993, 16:323-328
73. Dubowitz DJ, Bernheim KA, Chen DY, Bradley Jr WG, Andersen RA: Enhancing fMRI contrast in awake-behaving primates using intravascular magnetite dextran nanopartieles. Neuroreport 2001, 12:2335-2340
74. Hackett TA, Preuss TM, Kaas JH: Architectonic identification of the core region in auditory cortex of macaques, chimpanzees, and humans. J Comp Neurol 2001, 441:197-222