Proteomic analysis of lymphoblastoid cells from Nasu-Hakola patients: A step forward in our understanding of this neurodegenerative disorder

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Giuliano, Serena ^a,b   Agresta, Anna Maria ^c   De Palma, Antonella ^c   Viglio, Simona ^a   Mauri, Pierluigi ^c   Fumagalli, Marco ^a   Iadarola, Paolo ^a   Montalbetti, Lorenza ^a   Salvini, Roberta ^a   Bardoni, Anna ^a  

^a UNIVERSITY OF PAVIA   (Italy)

^b Laboratory of Excellence in Ion Channel Science and Therapeutics   (France)

^c CNR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL DEHYDROGENASE; ALPHA ENOLASE; BETA ACTIN; BIOLOGICAL MARKER; CHAPERONIN CONTAINING TCP1; COPROPORPHYRINOGEN OXIDASE; CYSTATIN B; ELONGATION FACTOR 1; FRUCTOSE BISPHOSPHATE ALDOLASE; FRUCTOSE BISPHOSPHATE ALDOLASE A; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HEAT SHOCK PROTEIN 70; IMMUNOGLOBULIN; PHOSPHATASE; PHOSPHOGLYCERATE KINASE; PHOSPHOGLYCERATE MUTASE; PHOSPHOGLYCERATE MUTASE 1; PYRIDOXAL PHOSPHATE PHOSPHATASE; TREM2 PROTEIN; UBIQUITIN THIOLESTERASE; UNCLASSIFIED DRUG; VOLTAGE DEPENDENT ANION CHANNEL 2; IMMUNOGLOBULIN RECEPTOR; MEMBRANE PROTEIN; PROTEIN; TREM2 PROTEIN, HUMAN;

ADULT; AGED; ARTICLE; BONE DYSPLASIA; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; DEGENERATIVE DISEASE; DISEASE MARKER; FEMALE; GENE AMPLIFICATION; GLUCOSE METABOLISM; HUMAN; ITALY; LEUKOENCEPHALOPATHY; LIQUID CHROMATOGRAPHY; LYMPHOBLASTOID CELL; MALE; MIDDLE AGED; NANOLIQUID CHROMATOGRAPHY; NASU HAKOLA DISEASE; POLYMERASE CHAIN REACTION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEOMICS; REVERSE TRANSCRIPTION; RNA PURIFICATION; TANDEM MASS SPECTROMETRY; TWO DIMENSIONAL ELECTROPHORESIS; VALIDATION PROCESS; WESTERN BLOTTING; YOUNG ADULT; CASE CONTROL STUDY; CHONDRODYSPLASIA; GENE EXPRESSION REGULATION; GENETICS; LIPODYSTROPHY; LYMPHOCYTE; METABOLISM; PATHOLOGY; PEDIGREE; PROCEDURES; SUBACUTE SCLEROSING PANENCEPHALITIS; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ADULT; AGED; CASE-CONTROL STUDIES; CHROMATOGRAPHY, LIQUID; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FEMALE; GENE EXPRESSION REGULATION; HUMANS; ITALY; LIPODYSTROPHY; LYMPHOCYTES; MALE; MEMBRANE GLYCOPROTEINS; MIDDLE AGED; OSTEOCHONDRODYSPLASIAS; PEDIGREE; PROTEINS; PROTEOMICS; RECEPTORS, IMMUNOLOGIC; SUBACUTE SCLEROSING PANENCEPHALITIS; TANDEM MASS SPECTROMETRY; YOUNG ADULT;

EID: 84916228931     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0110073     Document Type: Article

References (100)

1. Nasu T, Tsukahara Y, Terayama K (1973) A lipid metabolic disease- "membranous lipodystrophy"- an autopsyase demonstrating numerous peculiar membrane structures composed of compound lipid in bone and bone marrow and various adipose tissues. Acta Path Jap 23: 539-559.
2. Hakola HPA, Järvi OH, Sourander P (1970) Osteodysplasia polycystica hereditaria combined with sclerosing leucoencephalopathy. Acta Neurol Scand Suppl 43: 79-80.
3. Verloes A, Maquet P, Sadzot B, Vivario M, Thiry A, et al. (1997) Nasu-Hakola syndrome: polycystic lipomembranous osteodysplasia with sclerosing leucoencephalopathy and presenile dementia. J Med Genet 34: 753-757.
4. Hakola HPA (1972) Neuropsychiatric and genetic aspects of a new hereditary disease characterized by progressive dementia and lipomembranous polycystic osteodysplasia. Acta Neuropsych Scand Suppl 232: 1-173.
5. Paloneva J, KestiläM, Wu J, Salminen A, Böhling T, et al. (2000) Loss-of-function mutations in TYROBP (DAP12) result in a presenile dementia with bone cysts. Nat Genet 25: 357-361.
6. Paloneva J, Manninen T, Christman G, Hovanes K, Mandelin J, et al. (2002) Mutations in two genes encoding different subunits of a receptor signaling complex result in an identical disease phenotype. Am J Hum Genet 71: 656-662.
7. Nakano-Yokomizo T, Tahara-Hanaoka S, Nakahashi-Oda C, Nabekura T, Tchao NK, et al. (2011) The immunoreceptor adapter protein DAP12 suppresses B lymphocyte-driven adaptive immune responses. J Exp Med 208: 1661-1671.
8. Hamerman JA, Lanier LL (2006) Inhibition of immune responses by ITAM-bearing receptors. Sci STKE 2006: re1.
9. Turnbull IR, Gilfillan S, Cella M, Aoshi T, Miller M, et al. (2006) Cutting edge: TREM-2 attenuates macrophage activation. J Immunol 177: 3520-3524.
10. Lehnardt S (2010) Innate immunity and neuroinflammation in the CNS: the role of microglia in Toll-like receptor-mediated neuronal injury. Glia 58: 253-263.
11. Mila S, Albo AG, Corpillo D, Giraudo S, Zibetti M, et al. (2009) Lymphocyte proteomics of Parkinson's disease patients reveals cytoskeletal protein dysregulation and oxidative stress. Biomark Med 3: 117-128.
12. Fiszer U (2001) Does Parkinson's disease have an immunological basis? The evidence and its therapeutic implications. BioDrugs 15: 351-355.
13. Colonna M (2003) TREMs in the immune system and beyond. Nat Rev Immunol 3: 445-453.
14. Sharif O, Knapp S (2008) From expression to signaling: roles of TREM-1 and TREM-2 in innate immunity and bacterial infection. Immunobiology 213: 701-713.
15. Bouchon A, Hernández-Munain C, Cella M, Colonna MA (2001) DAP12-mediated pathway regulates expression of CC chemokine receptor 7 and maturation of human dendritic cells. J Exp Med 194 1111-1122.
16. Bianchin MM, Capella HM, Chaves DL, Steindel M, Grisard EC, et al. (2004) Nasu-Hakola disease (polycystic lipomembranous osteodysplasia with sclerosing leukoencephalopathy-PLOSL): a dementia associated with bone cystic lesions From clinical to genetic and molecular aspects. Cell Mol Neurobiol 24: 1-24.
17. Soragna D, Papi L, Ratti MT, Sestini R, Tupler R, et al. (2003) An Italian family affected by Nasu- Hakola disease with a novel genetic mutation in the TREM2 gene. J Neurol Neurosurg Psychiatry 74: 825-826.
18. Montalbetti L, Soragna D, Ratti MT, Bini P, Buscone S, et al. (2004) Nasu-Hakola disease: a rare entity in Italy Critical review of the literature. Funct Neurol 19: 171-179.
19. Neumann H, Takahashi K (2007) Essential role of the microglial triggering receptor expressed on myeloid cells-2 (TREM2) for central nervous tissue immune homeostasis. J Neuroimmunol 84: 92-99.
20. Linnartz B, Wang Y, Neumann H (2010) Microglial immunoreceptor tyrosine-based activation and inhibition motif signaling in neuroinflammation. Int J Alzheimers Dis 2010: pii 587463.
21. Surinova S, Schiess R, Hü ttenhain R, Cerciello F, Wollscheid B, et al. (2011) On the development of plasma protein biomarkers. J Proteome Res 10: 5-16.
22. Salonen JM, Valmu L, Rönnholm G, Kalkkinen N, Vihinen M (2006) Proteome analysis of B-cell maturation. Proteomics 6: 5152-5168.
23. Drabik A, Bierczynska-Krzysik A, Bodzon-Kulakowska A, Suder P, Kotlinska J, et al. (2007) Proteomics in neurosciences. Mass Spectrom Rev 26: 432-450.
24. Tosato G, Cohen JI (2007) Generation of Epstein-Barr Virus (EBV)-immortalized B cell lines. Curr Protoc Immunol Chapter 7: Unit 722.
25. Candiano G, Bruschi M, Musante L, Santucci L, Ghiggeri GM, et al. (2004) Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 25: 1327-1333.
26. Toda T, Sugimoto M (2003) Proteome analysis of Epstein-Barr virus-transformed B-lymphoblasts and the proteome database. J Chromatogr B Analyt Technol Biomed Life Sci 787: 197-206.
27. Caron M, Imam-Sghiouar N, Poirier F, Le Caer JP, Labas V, et al. (2002) Proteomic map and database of lymphoblastoid proteins. J Chromatogr B 771: 197-209.
28. Ford JW, McVicar DW (2009) TREM and TREM-like receptors in inflammation and disease. Curr Opin Immunol 21: 38-46.
29. Martínez A, Dalfó E, Muntané G, Ferrer I (2008) Glycolitic enzymes are targets of oxidation in aged human frontal cortex and oxidative damage of these proteins is increased in progressive supranuclear palsy. J Neural Transm 115: 59-66.
30. Castegna A, Aksenov M, Aksenova M, Thongboonkerd V, Klein JB, et al. (2002) Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain Part I: creatine kinase BB glutamine synthase and ubiquitin carboxy-terminal hydrolase L-1. Free Radic Biol Med 33: 562-571.
31. Korolainen MA, Goldsteins G, Nyman TA, Alafuzoff I, Koistinaho J, et al. (2006) Oxidative modification of proteins in the frontal cortex of Alzheimer's disease brain Neurobiol Aging 27: 42-53.
32. Bigl M, Apelt J, Eschrich K, Schliebs R (2003) Cortical glucose metabolism is altered in aged transgenic Tg2576 mice that demonstrate Alzheimer plaque pathology. J Neural Transm 110: 77-94.
33. Boyd-Kimball D, Poon HF, Lynn BC, Cai J, Pierce WM Jr, et al. (2006) Proteomic identification of proteins specifically oxidized in Caenorhabditis elegans expressing human Abeta(1-42): implications for Alzheimer's disease. Neurobiol Aging 27: 1239-1249.
34. Sultana R, Newman SF, Abdul HM, Cai J, Pierce WM, et al. (2006) Protective effect of D609 against amyloid-beta1-42-induced oxidative modification of neuronal proteins: redox proteomics study. J Neurosci Res 84: 409-417.
35. Chen W, Ji J Ru B (2005) Proteomic analysis of corticobasal degeneration: a case study of corticobasal degeneration at the proteome level. J Neuropsychiatry Clin Neurosci 17: 364-371.
36. Gong B, Cao Z, Zheng P, Vitolo OV, Liu S, et al. (2006) Ubiquitin hydrolase Uch-L1 rescues betaamyloid- induced decreases in synaptic function and contextual memory. Cell 126: 775-788.
37. Castegna A, Aksenov M, Aksenova M, Thongboonkerd V, Klein JB, et al. (2002) Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain Part I: creatine kinase BB glutamine synthase and ubiquitin carboxy-terminal hydrolase L-1. Free Radic Biol Med 33: 562-571.
38. Choi J, Levey AI, Weintraub ST, Rees HD, Gearing M, et al. (2004) Oxidative modifications and downregulation of ubiquitin carboxyl-terminal hydrolase L1 associated with idiopathic Parkinson's and Alzheimer's diseases. J Biol Chem 279: 13256-13264.
39. Leroy E, Boyer R, Auburger G, Leube B, Ulm G, et al. (1998) The ubiquitin pathway in Parkinson's disease Nature 395: 451-452.
40. Liu J, Jiang Y, Huang C, Fang H, Fang H, et al. (2010) Proteomic analysis reveals changes in the hippocampus protein pattern of rats exposed to dietary zinc deficiency. Electrophoresis 31: 1302-1310.
41. Sultana R, Boyd-Kimball D, Cai J, Pierce WM, Klein JB, et al. (2007) Proteomics analysis of the Alzheimer's disease hippocampal proteome. J Alzheimers Dis 11: 153-164.
42. Furuchi T, Sakurako K, Katane M, Sekine M, Homma H (2010) The role of protein L-isoaspartyl/Daspartyl O-methyltransferase (PIMT) in intracellular signal transduction. Chem Biodivers 7: 1337-1348.
43. Yamamoto A, Takagi H, Kitamura D, Tatsuoka H, Nakano H, et al. (1998) Deficiency in protein Lisoaspartyl methyltransferase results in a fatal progressive epilepsy. J Neurosci 18: 2063-2074.
44. Desrosiers RR, Fanélus I (2011) Damaged proteins bearing L-isoaspartyl residues and aging: a dynamic equilibrium between generation of isomerized forms and repair by PIMT. Curr Aging Sci 4: 8-18.
45. Chuang DM, Hough C, Senatorov VV (2005) Glyceraldehyde-3-phosphate dehydrogenase apoptosis and neurodegenerative diseases. Annu Rev Pharmacol Toxicol 45: 269-290.
46. Butterfield DA, Hardas SS, Lange ML (2010) Oxidatively modified glyceraldehyde-3-phosphate dehydrogenase (GAPDH) and Alzheimer's disease: many pathways to neurodegeneration. J Alzheimers Dis 20: 369-393.
47. Shalova IN, Cechalova K, Rehakova Z, Dimitrova P, Ognibene E, et al. (2007) Decrease of dehydrogenase activity of cerebral glyceraldehyde-3-phosphate dehydrogenase in different animal models of Alzheimer's disease. Biochim Biophys Acta 1770: 826-832.
48. Pierce A, Mirzaei H, Muller F, De Waal E, Taylor AB, et al. (2008) GAPDH is conformationally and functionally altered in association with oxidative stress in mouse models of amyotrophic lateral sclerosis. J Mol Biol 382: 1195-1210.
49. Gómez A, Ferrer I (2009) Increased oxidation of certain glycolysis and energy metabolism enzymes in the frontal cortex in Lewy body diseases. J Neurosci Res 87: 1002-1013.
50. Alberio T, Pippione AC, Comi C, Olgiati S, Cecconi D, et al. (2012) Dopaminergic therapies modulate the T-CELL proteome of patients with Parkinson's disease. IUBMB Life 64: 846-852.
51. Castegna A, Aksenov M, Thongboonkerd V, Klein JB, Pierce WM, et al. (2002) Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part II: dihydropyrimidinaserelated protein 2 alpha-enolase and heat shock cognate 71. J Neurochem 82: 1524-1532.
52. Takano M, Yamashita T, Nagano K, Otani M, Maekura K, et al. (2013) Proteomic analysis of the hippocampus in Alzheimer's disease model mice by using two-dimensional fluorescence difference in gel electrophoresis. Neurosci Lett 534: 85-89.
53. Parihar MS, Brewer GJ (2010) Amyloid-b as a modulator of synaptic plasticity. J Alzheimers Dis 22: 741-763.
54. Yao J, Du H, Yan S, Fang F, Wang C, et al. (2011) Inhibition of amyloid-beta (Abeta) peptide-binding alcohol dehydrogenase-Abeta interaction reduces Abeta accumulation and improves mitochondrial function in a mouse model of Alzheimer's disease. J Neurosci 31: 2313-2320.
55. Borger E, Aitken L, Du H, Zhang W, Gunn-Moore FJ, et al. (2013) Is amyloid binding alcohol dehydrogenase a drug target for treating Alzheimer's disease? Curr Alzheimer Res 10: 21-29.
56. Lyon RC, Li D, McGarvie G, Ellis EM (2013) Aldo-keto reductases mediate constitutive and inducible protection against aldehyde toxicity in human neuroblastoma SH-SY5Y cells. Neurochem Int 62: 113-121.
57. Furukawa A, Oikawa S, Hasegawa-Ishii S, Chiba Y, Kawamura N, et al. (2010) Proteomic analysis of aging brain in SAMP10 mouse: a model of age-related cerebral degeneration. Mech Ageing Dev 131: 379-388.
58. Kim JE, Kim DW, Kwak SE, Kwon OS, Choi SY, et al. (2008) Potential role of pyridoxal-59-phosphate phosphatase/chronopin in epilepsy. Exp Neurol 211: 128-140.
59. Tsai YC, Lee YM, Lam KK, Lin JF, Wang JJ, et al. (2013) The role of heat shock protein 70 in the protective effect of YC-1 on β-amyloid-induced toxicity in differentiated PC12 cells. PLoS One 8: e69320.
60. Di Domenico F, Sultana R, Tiu GF, Scheff NN, Perluigi M, et al. (2010) Protein levels of heat shock proteins 27 32 60 70 90 and thioredoxin-1 in amnestic mild cognitive impairment: an investigation on the role of cellular stress response in the progression of Alzheimer disease. Brain Res 1333: 72-81.
61. Perez N, Sugar J, Charya S, Johnson G, Merril C, et al. (1991) Increased synthesis and accumulation of heat shock 70 proteins in Alzheimer's disease. Brain Res Mol Brain Res 11: 249-254.
62. Yoo BC, Kim SH, Cairns N, Fountoulakis M, Lubec G (2001) Deranged expression of molecular chaperones in brains of patients with Alzheimer's disease. Biochem Biophys Res Commun 280: 249-258.
63. Hargreaves GA, Quinn H, Kashem MA, Matsumoto I, McGregor IS (2009) Proteomic analysis demonstrates adolescent vulnerability to lasting hippocampal changes following chronic alcohol consumption. Alcohol Clin Exp Res 33: 86-94.
64. Komatsubara AT, Asano T, Tsumoto H, Shimizu K, Nishiuchi T, et al. (2012) Proteomic analysis of Snitrosylation induced by 1-methyl-4-phenylpyridinium (MPP+). Proteome Sci 10: 74.
65. Yoon S, Cong WT, Bang Y, Lee SN, Yoon CS, et al. (2009) Proteome response to ochratoxin A-induced apoptotic cell death in mouse hippocampal HT22 cells. Neurotoxicology 30: 666-676.
66. Wu H, Shi Y, Lin Y, Qian W, Yu Y, et al. (2011) Eukaryotic translation elongation factor 1 delta inhibits the ubiquitin ligase activity of SIAH-1. Mol Cell Biochem 357: 209-215.
67. Zhang D, Yu W, Geisbrecht BV, Gould SJ, Sprecher H, et al. (2002) Functional characterization of Delta3 Delta2-enoyl-CoA isomerases from rat liver. J Biol Chem 277: 9127-9132.
68. Whetstone H, Lingwood C (2002) 39Sulfogalactolipid binding specifically inhibits Hsp70 ATPase activity in vitro. Biochemistry 42: 1611-1617.
69. Stewart JM, Blakely JA (2000) Long chain fatty acids inhibit and medium chain fatty acids activate mammalian cardiac hexokinase Biochim Biophys Acta 1484: 278-286.
70. Antikainen J, Kuparinen V, Lähteenmäki K, Korhonen TK (2007) pH-dependent association of enolase and glyceraldehyde-3-phosphate dehydrogenase of Lactobacillus crispatus with the cell wall and lipoteichoic acids J Bacteriol 189: 4539-4543.
71. van Tuyll van Serooskerken AM, de Rooij FW, Edixhoven A, Bladergroen RS, Baron JM, et al. (2011) Digenic inheritance of mutations in the coproporphyrinogen oxidase and protoporphyrinogen oxidase genes in a unique type of porphyria. J Invest Dermatol 131: 2249-2254.
72. Bekenstein U, Soreq H (2013) Heterogeneous nuclear ribonucleoprotein A1 in health and neurodegenerative disease: from structural insights to post-transcriptional regulatory roles. Mol Cell Neurosci 56: 436-446.
73. Turk V, Stoka V, Turk D (2008) Cystatins: biochemical and structural properties and medical relevance Front Biosci 13: 5406-5420.
74. Lehtinen MK, Tegelberg S, Schipper H, Su H, Zukor H, et al. (2009) Cystatin B deficiency sensitizes neurons to oxidative stress in progressive myoclonus epilepsy EPM1. J Neurosci 29: 5910-5915.
75. Zerovnik E (2009) The emerging role of cystatins in Alzheimer's disease. Bioessays 31: 597-599.
76. De Pinto V, Messina A, Accardi R, Aiello R, Guarino F, et al. (2003) New functions of an old protein: the eukaryotic porin or voltage dependent anion selective channel (VDAC). Ital J Biochem 52: 17-24.
77. Hemachandra Reddy P (2013) Is the mitochondrial outmembrane protein VDAC1 therapeutic target for Alzheimer's disease? Biochim Biophys Acta 1832: 67-75.
78. Krauskopf A, Eriksson O, Craigen WJ, Forte MA, Bernardi P (2006) Properties of the permeability transition in VDAC1(2/2) mitochondria. Biochim Biophys Acta 1757: 590-595.
79. Raghavan A, Sheiko T, Graham BH, Craigen WJ (2012) Voltage-dependant anion channels: novel insights into isoform function through genetic models. Biochim Biophys Acta 1818: 1477-1485.
80. Devi L, Prabhu BM, Galati DF, Avadhani NG, Anandatheerthavarada HK (2006) Accumulation of amyloid precursor protein in the mitochondrial import channels of human Alzheimer's disease brain is associated with mitochondrial dysfunction. J Neurosci 26: 9057-9068.
81. Manczak M, Calkins MJ, Reddy PH (2011) Impaired mitochondrial dynamics and abnormal interaction of amyloid beta with mitochondrial protein Drp1 in neurons from patients with Alzheimer's disease: implications for neuronal damage. Hum Mol Genet 20: 2495-2509.
82. Hansson Petersen CA, Alikhani N, Behbahani H, Wiehager B, Pavlov PF, et al. (2008) The amyloid beta-peptide is imported into mitochondria via the TOM import machinery and localized to mitochondrial cristae. Proc Natl Acad Sci USA 105: 13145-13150.
83. Yoo BC, Fountoulakis M, Cairns N, Lubec G (2001) Changes of voltage-dependent anion-selective channel proteins VDAC1 and VDAC2 brain levels in patients with Alzheimer's disease and Down syndrome. Electrophoresis 22: 172-179.
84. Cuadrado-Tejedor M, Vilariño M, Cabodevilla F, Del Río J, Frechilla D, et al. (2011) Enhanced expression of the voltage-dependent anion channel 1 (VDAC1) in Alzheimer's disease transgenic mice: an insight into the pathogenic effects of amyloid-b. J Alzheimers Dis 23: 195-206.
85. Manczak M, Reddy PH (2012) Abnormal interaction of VDAC1 with amyloid beta and phosphorylated tau causes mitochondrial dysfunction in Alzheimer's disease. Hum Mol Genet 21: 5131-5146.
86. Lawen A, Ly JD, Lane DJ, Zarschler K, Messina A, et al. (2005) Voltage-dependent anion-selective channel 1 (VDAC1)-a mitochondrial protein rediscovered as a novel enzyme in the plasma membrane. Int J Biochem Cell Biol 37: 277-282.
87. Ohgidani M, Kato TA, Setoyama D, Sagata N, Hashimoto R, et al. (2014) Direct induction of ramified microglial-like cells from human monocytes: dynamic microglial dysfunction in Nasu-Hakola disease. Sci Rep 4: 4957-4963.
88. Mostfavi S, Ray D, Warde-Farley D, Grouis C, Morris Q (2008) GeneMANIA: a real-time multiple association network integration algorithm for predicting gene function. Genome Biol 9: S4.
89. United States National Library of Medicine (2014) Genes, Genetics Home Reference, GPI gene. Available from: ghr.nlm.nih.gov/gene/GPI.
90. Seigle JL, Celotto AM, Palladino MJ (2008) Degradation of functional triose phosphate isomerase protein underlies sugarkill pathology. Genetics 179: 855-892.
91. United States National Library of Medicine (2014) Genes, Genetics Home Reference, LDHA gene. Available: ghr.nlm.nih.gov/gene/LDHA.
92. Donn RP, Ray DW (2004) Macrophage migration inhibitory factor: molecular cellular and genetic aspects of a key neuroendocrine molecule. J Endocrinol 182: 1-9.
93. Klesney-Tait J, Turnbull IR, Colonna M (2006) The TREM receptor family and signal integration. Nature Immunology 7, 1266-1273.
94. Ivashkiv LB (2008) A signal-switch hypothesis for cross-regulation of cytokine and TRL signaling pathways. Nat Rev Immunol 8, 816-822.
95. Kim JM, Jeong D, Kang HK, Jung SY, Kang SS, et al. (2007) Osteoclast precursors display dynamic metabolic shifts toward accelerated glucose metabolism at an early stage of RANKL-stimulated osteoclast differentiation. Cell Physiol Biochem 20, 935-946.
96. Dodds RA, Gowen M, Bradbeer JN (1994) Microcytophotometric analysis of human osteoclast metabolism: lack of activity in certain oxidative pathways indicates inability to sustain biosynthesis during resorption. J Histochem Cytochem 42, 599-606.
97. Lu M, Holliday LS, Zhang L, Dunn WA Jr, Gluck SL (2001) Interaction between aldolase and vacuolar H+-ATPase: evidence for direct coupling of glycolysis to the ATP-hydrolyzing proton pump. J Biol Chem 276, 30407-30413.
98. Stevens TH, Forgac M (1997) Structure, function and regulation of the vacuolar (H+)-ATPase. Annu Rev Cell Dev Biol 13, 779-808.
99. Orphanet (2014) The portal for rare diseases and orphan drugs. Nasu Hakola disease. Available: www.orpha.net.
100. Bock V, Botturi A, Gaviani P, Lamperti E, Maccagnano C, et al. (2013) Polycystic Lipomembranous Osteodysplasia with Sclerosing Leukoencephalopathy (PSOSL): A new report of an Italian woman and review of the literature. J Neurol Sci 326: 115-119.