期刊论文详细信息
BMC Medical Genomics
Circadian transcriptome analysis in human fibroblasts from Hunter syndrome and impact of iduronate-2-sulfatase treatment
Maurizio Scarpa5  Manlio Vinciguerra4  Francesco Giuliani2  Massimo Francavilla2  Valerio Pazienza6  Alessandra Zanetti3  Laura Rigon3  Marika Salvalaio3  Francesca D’Avanzo3  Tommaso Mazza1  Rosella Tomanin3  Gianluigi Mazzoccoli7 
[1] Bioinformatics Unit, IRCCS Scientific Institute and Regional General Hospital “Casa Sollievo della Sofferenza”, S.Giovanni Rotondo (FG), Italy;Computing Unit, IRCCS Scientific Institute and Regional General Hospital “Casa Sollievo della Sofferenza”, S.Giovanni Rotondo (FG), Italy;Laboratory of Diagnosis and Therapy of Lysosomal Disorders, Department of Women’s and Children’s Health, University of Padova, Padova, Italy;Institute for Liver and Digestive Health, Division of Medicine, Royal Free Campus, University College London, London, UK;Centre for Rare Disorders, IRCCS Scientific Institute and Regional General Hospital “Casa Sollievo della Sofferenza”, S.Giovanni Rotondo (FG), Italy;Research Laboratory of Gastroenterology Unit, IRCCS Scientific Institute and Regional General Hospital “Casa Sollievo della Sofferenza”, S.Giovanni Rotondo (FG), Italy;Department of Medical Sciences, Division of Internal Medicine and Chronobiology Unit, IRCCS Scientific Institute and Regional General Hospital “Casa Sollievo della Sofferenza”, S.Giovanni Rotondo (FG), Italy
关键词: Circadian rhythm;    Lysosomal storage disease;    Hunter syndrome;    Clock gene;   
Others  :  1091949
DOI  :  10.1186/1755-8794-6-37
 received in 2013-06-11, accepted in 2013-09-19,  发布年份 2013
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【 摘 要 】

Background

Hunter syndrome (HS) is a lysosomal storage disease caused by iduronate-2-sulfatase (IDS) deficiency and loss of ability to break down and recycle the glycosaminoglycans, heparan and dermatan sulfate, leading to impairment of cellular processes and cell death. Cell activities and functioning of intracellular organelles are controlled by the clock genes (CGs), driving the rhythmic expression of clock controlled genes (CCGs). We aimed to evaluate the expression of CGs and downstream CCGs in HS, before and after enzyme replacement treatment with IDS.

Methods

The expression levels of CGs and CCGs were evaluated by a whole transcriptome analysis through Next Generation Sequencing in normal primary human fibroblasts and fibroblasts of patients affected by HS before and 24 h/144 h after IDS treatment. The time related expression of CGs after synchronization by serum shock was also evaluated by qRT-PCR before and after 24 hours of IDS treatment.

Results

In HS fibroblasts we found altered expression of several CGs and CCGs, with dynamic changes 24 h and 144 h after IDS treatment. A semantic hypergraph-based analysis highlighted five gene clusters significantly associated to important biological processes or pathways, and five genes, AHR, HIF1A, CRY1, ITGA5 and EIF2B3, proven to be central players in these pathways. After synchronization by serum shock and 24 h treatment with IDS the expression of ARNTL2 at 10 h (p = 0.036), PER1 at 4 h (p = 0.019), PER2 at 10 h (p = 0.041) and 16 h (p = 0.043) changed in HS fibroblasts.

Conclusion

CG and CCG expression is altered in HS fibroblasts and IDS treatment determines dynamic modifications, suggesting a direct involvement of the CG machinery in the physiopathology of cellular derangements that characterize HS.

【 授权许可】

   
2013 Mazzoccoli et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Lampe C, Bellettato CM, Karabul N, Scarpa M: Mucopolysaccharidoses and other lysosomal storage diseases. Rheum Dis Clin North Am 2013, 39:431-455.
  • [2]Scarpa M, Almássy Z, Beck M, Bodamer O, Bruce IA, De Meirleir L, Guffon N, Guillén-Navarro E, Hensman P, Jones S, Kamin W, Kampmann C, Lampe C, Lavery CA, Teles EL, Link B, Lund AM, Malm G, Pitz S, Rothera M, Stewart C, Tylki-Szymańska A, van der Ploeg A, Walker R, Zeman J, Wraith JE: Hunter Syndrome European Expert Council: Mucopolysaccharidosis type II: European recommendations for the diagnosis and multidisciplinary management of a rare disease. Orphanet J Rare Dis 2011, 6:72. BioMed Central Full Text
  • [3]Lowrey PL, Takahashi JS: Genetics of the mammalian circadian system: photic entrainment, circadian pacemaker mechanisms, and posttranslational regulation. Annu Rev Genet 2000, 34:533-562.
  • [4]Mazzoccoli G: The timing clockwork of life. J Biol Regul Homeost Agents 2011, 25:137-143.
  • [5]Bass J: Circadian topology of metabolism. Nature 2012, 491:348-356.
  • [6]Schibler U, Sassone-Corsi P: A web of circadian pacemakers. Cell 2002, 111:919-922.
  • [7]Reyes BA, Pendergast JS, Yamazaki S: Mammalian peripheral circadian oscillators are temperature compensated. J Biol Rhythms 2008, 23:95-98.
  • [8]Hastings MH, Reddy AB, Maywood ES: A clockwork web: circadian timing in brain and periphery, in health and disease. Nat Rev Neurosci 2003, 4:649-661.
  • [9]Houben T, Deboer T, van Oosterhout F, Meijer JH: Correlation with behavioral activity and rest implies circadian regulation by SCN neuronal activity levels. J Biol Rhythms 2009, 24:477-487.
  • [10]Pezuk P, Mohawk JA, Yoshikawa T, Sellix MT, Menaker M: Circadian organization is governed by extra-SCN pacemakers. J Biol Rhythms 2010, 25:432-441.
  • [11]Nagoshi E, Saini C, Bauer C, Laroche T, Naef F, Schibler U: Circadian gene expression in individual fibroblasts: cell-autonomous and self-sustained oscillators pass time to daughter cells. Cell 2004, 119:693-705.
  • [12]Eide EJ, Vielhaber EL, Hinz WA, Virshup DM: The circadian regulatory proteins BMAL1 and Cryptochromes are substrates of Casein Kinase Iϵ. J Biol Chem 2002, 277:17248-17254.
  • [13]Cho H, Zhao X, Hatori M, Yu RT, Barish GD, Lam MT, Chong LW, DiTacchio L, Atkins AR, Glass CK, Liddle C, Auwerx J, Downes M, Panda S, Evans RM: Regulation of circadian behaviour and metabolism by REV-ERB-α and REV-ERB-β. Nature 2012, 485:123-127.
  • [14]Mazzoccoli G, Cai Y, Liu S, Francavilla M, Giuliani F, Piepoli A, Pazienza V, Vinciguerra M, Yamamoto T, Takumi T: REV-ERBα and the clock gene machinery in mouse peripheral tissues: a possible role as a synchronizing hinge. J Biol Regul Homeost Agents 2012, 26:265-276.
  • [15]Asher G, Schibler U: Crosstalk between components of circadian and metabolic cycles in mammals. Cell Metab 2011, 13:125-137.
  • [16]Unsal-Kaçmaz K, Chastain PD, Qu PP, Minoo P, Cordeiro-Stone M, Sancar A, Kaufmann WK: The human Tim/Tipin complex coordinates an Intra-S checkpoint response to UV that slows replication fork displacement. Mol Cell Biol 2007, 27:3131-3142.
  • [17]Smith KD, Fu MA, Brown EJ: Tim-Tipin dysfunction creates an indispensible reliance on the ATR-Chk1 pathway for continued DNA synthesis. J Cell Biol 2009, 5:15-23.
  • [18]Yang X, Wood PA, Hrushesky WJ: Mammalian TIMELESS is required for ATM-dependent CHK2 activation and G2/M checkpoint control. J Biol Chem 2010, 285:3030-3034.
  • [19]Kemp MG, Akan Z, Yilmaz S, Grillo M, Smith-Roe SL, Kang TH, Cordeiro-Stone M, Kaufmann WK, Abraham RT, Sancar A, Unsal-Kaçmaz K: Tipin-replication protein A interaction mediates Chk1 phosphorylation by ATR in response to genotoxic stress. J Biol Chem 2010, 285:16562-16571.
  • [20]Matsuo T, Yamaguchi S, Mitsui S, Emi A, Shimoda F, Okamura H: Control mechanism of the circadian clock for timing of cell division in vivo. Science 2003, 302:255-259.
  • [21]Filipski E, King VM, Etienne MC, Li XM, Claustrat B, Granda TG: Persistent twenty-four hour changes in liver and bone marrow despite suprachiasmatic nuclei ablation in mice. Am J Physiol Regul Integr Comp Physiol 2004, 287:R844-R851.
  • [22]Hunt T, Sassone-Corsi P: Riding tandem: circadian clocks and the cell cycle. Cell 2007, 129:461-464.
  • [23]Ma D, Panda S, Lin JD: Temporal orchestration of circadian autophagy rhythm by C/EBPβ. EMBO J 2011, 30:4642-4651.
  • [24]Mazzoccoli G, Sothern RB, Greco A, Pazienza V, Vinciguerra M, Liu S, Cai Y: Time-related dynamics of variation in core clock gene expression levels in tissues relevant to the immune system. Int J Immunopathol Pharmacol 2011, 24:869-879.
  • [25]Vinciguerra M, Borghesan M, Pazienza V, Piepoli A, Palmieri O, Tarquini R, Tevy MF, De Cata A, Mazzoccoli G: The transcriptional regulators, the circadian clock and the immune system. J Biol Regul Homeost Agents 2013, 27:9-22.
  • [26]Tevy MF, Giebultowicz J, Pincus Z, Mazzoccoli G, Vinciguerra M: Aging signaling pathways and circadian clock-dependent metabolic derangements. Trends Endocrinol Metab 2013, 24:229-237.
  • [27]Panda S, Antoch MP, Miller BH, Su AI, Schook AB, Straume M, Schultz PG, Kay SA, Takahashi JS, Hogenesch JB: Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 2002, 109:307-320.
  • [28]Hughes ME, DiTacchio L, Hayes KR, Vollmers C, Pulivarthy S, Baggs JE, Panda S, Hogenesch JB: Harmonics of circadian gene transcription in mammals. PLoS Genet 2009, 5:e1000442.
  • [29]Bozek K, Relógio A, Kielbasa SM, Heine M, Dame C, Kramer A, Herzel H: Regulation of clock-controlled genes in mammals. PLoS One 2009, 4:e4882.
  • [30]Sukumaran S, Almon RR, DuBois DC, Jusko WJ: Circadian rhythms in gene expression: Relationship to physiology, disease, drug disposition and drug action. Adv Drug Deliv Rev 2010, 62:904-917.
  • [31]Carstea ED, Morris JA, Coleman KG, Loftus SK, Zhang D, Cummings C, Gu J, Rosenfeld MA, Pavan WJ, Krizman DB, Nagle J, Polymeropoulos MH, Sturley SL, Ioannou YA, Higgins ME, Comly M, Cooney A, Brown A, Kaneski CR, Blanchette-Mackie EJ, Dwyer NK, Neufeld EB, Chang TY, Liscum L, Strauss JF 3rd, Ohno K, Zeigler M, Carmi R, Sokol J, Markie D, O'Neill RR, van Diggelen OP, Elleder M, Patterson MC, Brady RO, Vanier MT, Pentchev PG, Tagle DA: Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis. Science 1997, 277:228-231.
  • [32]Harzer K, Massenkeil G, Frohlich E: Concurrent increase of cholesterol, sphingomyelin and glucosylceramide in the spleen from non-neurologic Niemann-Pick type C patients but also patients possibly affected with other lipid trafficking disorders. FEBS Lett 2003, 537:177-181.
  • [33]Pizarro A, Hayer K, Lahens NF, Hogenesch JB: CircaDB: a database of mammalian circadian gene expression profiles. Nucleic Acids Res 2013, 41:D1009-D1013.
  • [34]Balsalobre A, Damiola F, Schibler U: A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell 1998, 93:929-937.
  • [35]Castellana S, Mazza T: Congruency in the prediction of pathogenic missense mutations: state-of-the-art web-based tools. Brief Bioinform 2013. [Epub ahead of print]
  • [36]Castellana S, Romani M, Valente EM, Mazza T: A solid quality-control analysis of AB SOLiD short-read sequencing data. Brief Bioinform 2012. [Epub ahead of print]
  • [37]Wasserman S, Faust K: Social Network Analysis: Methods and Applications. Cambridge, UK: Cambridge University Press; 1994.
  • [38]Mazza T, Romanel A, Jordán J: Estimating the divisibility of complex biological networks by sparseness indices. Brief Bioinformatics 2010, 11:364-374.
  • [39]Mazza T, Ballarini P, Guido R, Prandi D: The relevance of topology in parallel simulation of biological networks. IEEE/ACM Trans Comput Biol Bioinform (TCBB) 2012, 9:911-923.
  • [40]Mazzoccoli G, Pazienza V, Vinciguerra M: Clock genes and clock controlled genes in the regulation of metabolic rhythms. Chronobiol Int 2012, 29:227-251.
  • [41]Kondratov RV, Antoch MP: Circadian proteins in the regulation of cell cycle and genotoxic stress responses. Trends Cell Biol 2007, 17:311-317.
  • [42]Doi M, Hirayama J, Sassone-Corsi P: Circadian regulator CLOCK is a histone acetyltransferase. Cell 2006, 125:497-508.
  • [43]Ukai-Tadenuma M, Yamada RG, Xu H, Ripperger JA, Liu AC, Ueda HR: Delay in feedback repression by cryptochrome 1 is required for circadian clock function. Cell 2011, 144:268-281.
  • [44]Fustin JM, O'Neill JS, Hastings MH, Hazlerigg DG, Dardente H: Cry1 circadian phase in vitro: wrapped up with an E-box. J Biol Rhythms 2009, 24:16-24.
  • [45]Agostino PV, Harrington ME, Ralph MR, Golombek DA: Casein kinase-1-epsilon (CK1epsilon) and circadian photic responses in hamsters. Chronobiol Int 2009, 26:126-133.
  • [46]Burris TP: Nuclear hormone receptors for heme: REV-ERBalpha and REV-ERBbeta are ligand-regulated components of the mammalian clock. Mol Endocrinol 2008, 22:1509-1520.
  • [47]Tahara Y, Otsuka M, Fuse Y, Hirao A, Shibata S: Refeeding after fasting elicits insulin-dependent regulation of Per2 and Rev-erbα with shifts in the liver clock. J Biol Rhythms 2011, 26:230-240.
  • [48]Raspe’ E, Duez H, Mansen A, Fontaine C, Fievet C, Fruchart JC, Vennstrom B, Staels B: Identification of Rev-erb alpha as a physiological repressor of apoC-III gene transcription. J Lipid Res 2002, 43:2172-2179.
  • [49]Asher G, Gatfield D, Stratmann M, Reinke H, Dibner C, Kreppel F, Mostoslavsky R, Alt FW, Schibler U: SIRT1 regulates circadian clock gene expression through PER2 Deacetylation. Cell 2008, 134:317-328.
  • [50]Guarente L, Franklin H: Epstein lecture: Sirtuins, aging, and medicine. N Engl J Med 2011, 364:2235-2244.
  • [51]Zhao W, Kruse JP, Tang Y, Jung SY, Qin J, Gu W: Negative regulation of the deacetylase SIRT1 by DBC1. Nature 2008, 451:587-590.
  • [52]Brooks CL, Gu W: How does SIRT1 affect metabolism, senescence and cancer? Nat Rev Cancer 2009, 9:123-128.
  • [53]Schoenhard JA, Smith LH, Painter CA, Eren M, Johnson CH, Vaughan DE: Regulation of the PAI-1 promoter by circadian clock components: differential activation by BMAL1 and BMAL2. J Mol Cell Cardiol 2003, 35:473-481.
  • [54]Cermakian N, Lange T, Golombek D, Sarkar D, Nakao A, Shibata S, Mazzoccoli G: Crosstalk between the circadian clock circuitry and the immune system. Chronobiol Int 2013, 1-19. DOI: 10.3109/07420528.2013.782315
  • [55]Lindsey S, Papoutsakis ET: The evolving role of the aryl hydrocarbon receptor (AHR) in the normophysiology of hematopoiesis. Stem Cell Rev 2012, 8:1223-1235.
  • [56]Narasimamurthy R, Hatori M, Nayak SK, Liu F, Panda S, Verma IM: Circadian clock protein cryptochrome regulates the expression of proinflammatory cytokines. Proc Natl Acad Sci USA 2012, 109:12662-12667.
  • [57]Chu TJ, Peters DG: Serial analysis of the vascular endothelial transcriptome under static and shear stress conditions. Physiol Genomics 2008, 34:185-192.
  • [58]Anderson G, Beischlag TV, Vinciguerra M, Mazzoccoli G: The circadian clock circuitry and the AHR signaling pathway in physiology and pathology. Biochem Pharmacol 2013. doi:pii: S0006-2952(13)00126-3. 10.1016/j.bcp.2013.02.022. [Epub ahead of print]
  • [59]Zhang N, Walker MK: Crosstalk between the aryl hydrocarbon receptor and hypoxia on the constitutive expression of cytochromeP4501A1 mRNA. Cardiovasc Toxicol 2007, 7:282-290.
  • [60]Chilov D, Hofer T, Bauer C, Wenger RH, Gassmann M: Hypoxia affects expression of circadian genes PER1 and CLOCK in mouse brain. FASEB J 2001, 15:2613-2622.
  • [61]Santilli G, Lamorte G, Carlessi L, Ferrari D, Rota Nodari L, Binda E, Delia D, Vescovi AL, De Filippis L: Mild hypoxia enhances proliferation and multipotency of human neural stem cells. PLoS One 2010, 5:e8575.
  • [62]Oliveira SA, Li YJ, Noureddine MA, Zuchner S, Qin X, Pericak-Vance MA, Vance JM: Identification of risk and age-at-onset genes on chromosome 1p in Parkinson disease. Am J Hum Genet 2005, 77:252-264.
  • [63]Ohlenbusch A, Henneke M, Brockmann K, Goerg M, Hanefeld F, Kohlschütter A, Gärtner J: Identification of ten novel mutations in patients with eIF2B-related disorders. Hum Mutat 2005, 25:411.
  • [64]Scali O, Di Perri C, Federico A: The spectrum of mutations for the diagnosis of vanishing white matter disease. Neurol Sci 2006, 27:271-277.
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