Cytosolic functions of MORC2 in lipogenesis and adipogenesis

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1843, Issue 2, 2014, Pages 316-326

  Sánchez Solana, Beatriz ^a   Li, Da Qiang ^a   Kumar, Rakesh ^a  

^a GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

ACLY; Adipogenesis; Lipogenesis; MORC2; Protein protein interaction

Indexed keywords

ADENOSINE TRIPHOSPHATE; MICRORCHIDIA PROTEIN; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

ADIPOGENESIS; ARTICLE; BREAST CANCER; CHOLESTEROL SYNTHESIS; CYTOSOL; DNA DAMAGE; HOMEOSTASIS; HUMAN; HUMAN CELL; LIPOGENESIS; MAMMARY GLAND; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION;

3-HYDROXYL-3-METHYLGLUTARYL-COA REDUCTASE; 3-ISOBUTYL-1-METHYLXANTHINE; ACC; ACETYL-COA CARBOXYLASE; ACLY; ADENOSINE TRIPHOSPHATE; ADIPOGENESIS; ATP; ATP CITRATE LYASE; CAMP-DEPENDENT PROTEIN KINASE; FAS; FATTY ACID SYNTHASE; GLUTATHIONE-S-TRANSFERASE; GLYCOGEN SYNTHASE KINASE-3; GSK-3; GST; HMGCR; IBMX; IMMUNOPRECIPITATION; IP; LIPOGENESIS; MALATE DEHYDROGENASE; MDH; MICRORCHIDIA FAMILY CW-TYPE ZINC FINGER 2; MORC2; PKA; PROTEIN-PROTEIN INTERACTION; RADIO-IMMUNOPRECIPITATION ASSAY; RIPA; ZF; ZINC FINGER;

3T3-L1 CELLS; ADIPOGENESIS; ANIMALS; ATP CITRATE (PRO-S)-LYASE; CELL DIFFERENTIATION; CYTOSOL; ENZYME ACTIVATION; FATTY ACIDS; HUMANS; LIPOGENESIS; MCF-7 CELLS; MEVALONIC ACID; MICE; MODELS, BIOLOGICAL; PROTEIN BINDING; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84890289988     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.11.012     Document Type: Article

References (56)

1. Inoue N., Hess K.D., Moreadith R.W., Richardson L.L., Handel M.A., Watson M.L., Zinn A.R. New gene family defined by MORC, a nuclear protein required for mouse spermatogenesis. Hum. Mol. Genet. 1999, 8:1201-1207.
2. Iyer L.M., Abhiman S., Aravind L. MutL homologs in restriction-modification systems and the origin of eukaryotic MORC ATPases. Biol. Direct 2008, 3:8.
3. Dutta R., Inouye M. GHKL, an emergent ATPase/kinase superfamily. Trends Biochem. Sci. 2000, 25:24-28.
4. Platani M., Goldberg I., Lamond A.I., Swedlow J.R. Cajal body dynamics and association with chromatin are ATP-dependent. Nat. Cell Biol. 2002, 4:502-508.
5. Hu X., Machius M., Yang W. Monovalent cation dependence and preference of GHKL ATPases and kinases. FEBS Lett. 2003, 544:268-273.
6. Perry J., Zhao Y. The CW domain, a structural module shared amongst vertebrates, vertebrate-infecting parasites and higher plants. Trends Biochem. Sci. 2003, 28:576-580.
7. Watson M.L., Zinn A.R., Inoue N., Hess K.D., Cobb J., Handel M.A., Halaban R., Duchene C.C., Albright G.M., Moreadith R.W. Identification of morc (microrchidia), a mutation that results in arrest of spermatogenesis at an early meiotic stage in the mouse. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:14361-14366.
8. Takahashi K., Yoshida N., Murakami N., Kawata K., Ishizaki H., Tanaka-Okamoto M., Miyoshi J., Zinn A.R., Shime H., Inoue N. Dynamic regulation of p53 subnuclear localization and senescence by MORC3. Mol. Biol. Cell 2007, 18:1701-1709.
9. Liggins A.P., Cooper C.D., Lawrie C.H., Brown P.J., Collins G.P., Hatton C.S., Pulford K., Banham A.H. MORC4, a novel member of the MORC family, is highly expressed in a subset of diffuse large B-cell lymphomas. Br. J. Haematol. 2007, 138:479-486.
10. Moissiard G., Cokus S.J., Cary J., Feng S., Billi A.C., Stroud H., Husmann D., Zhan Y., Lajoie B.R., McCord R.P., Hale C.J., Feng W., Michaels S.D., Frand A.R., Pellegrini M., Dekker J., Kim J.K., Jacobsen S.E. MORC family ATPases required for heterochromatin condensation and gene silencing. Science 2012, 336:1448-1451.
11. Shao Y., Li Y., Zhang J., Liu D., Liu F., Zhao Y., Shen T., Li F. Involvement of histone deacetylation in MORC2-mediated down-regulation of carbonic anhydrase IX. Nucleic Acids Res. 2010, 38:2813-2824.
12. Li D.Q., Nair S.S., Ohshiro K., Kumar A., Nair V.S., Pakala S.B., Reddy S.D., Gajula R.P., Eswaran J., Aravind L., Kumar R. MORC2 signaling integrates phosphorylation-dependent, ATPase-coupled chromatin remodeling during the DNA damage response. Cell Rep. 2012, 2:1657-1669.
13. Watson J.A., Fang M., Lowenstein J.M. Tricarballylate and hydroxycitrate: substrate and inhibitor of ATP:citrate oxaloacetate lyase. Arch. Biochem. Biophys. 1969, 135:209-217.
14. Takahashi H., McCaffery J.M., Irizarry R.A., Boeke J.D. Nucleocytosolic acetyl-coenzyme a synthetase is required for histone acetylation and global transcription. Mol. Cell 2006, 23:207-217.
15. Wellen K.E., Hatzivassiliou G., Sachdeva U.M., Bui T.V., Cross J.R., Thompson C.B. ATP-citrate lyase links cellular metabolism to histone acetylation. Science 2009, 324:1076-1080.
16. Beigneux A.P., Kosinski C., Gavino B., Horton J.D., Skarnes W.C., Young S.G. ATP-citrate lyase deficiency in the mouse. J. Biol. Chem. 2004, 279:9557-9564.
17. Migita T., Narita T., Nomura K., Miyagi E., Inazuka F., Matsuura M., Ushijima M., Mashima T., Seimiya H., Satoh Y., Okumura S., Nakagawa K., Ishikawa Y. ATP citrate lyase: activation and therapeutic implications in non-small cell lung cancer. Cancer Res. 2008, 68:8547-8554.
18. Yancy H.F., Mason J.A., Peters S., Thompson C.E., Littleton G.K., Jett M., Day A.A. Metastatic progression and gene expression between breast cancer cell lines from African American and Caucasian women. J. Carcinog. 2007, 6:8.
19. Yahagi N., Shimano H., Hasegawa K., Ohashi K., Matsuzaka T., Najima Y., Sekiya M., Tomita S., Okazaki H., Tamura Y., Iizuka Y., Nagai R., Ishibashi S., Kadowaki T., Makuuchi M., Ohnishi S., Osuga J., Yamada N. Co-ordinate activation of lipogenic enzymes in hepatocellular carcinoma. Eur. J. Cancer 2005, 41:1316-1322.
20. Varis A., Wolf M., Monni O., Vakkari M.L., Kokkola A., Moskaluk C., Frierson H., Powell S.M., Knuutila S., Kallioniemi A., El-Rifai W. Targets of gene amplification and overexpression at 17q in gastric cancer. Cancer Res. 2002, 62:2625-2629.
21. Turyn J., Schlichtholz B., Dettlaff-Pokora A., Presler M., Goyke E., Matuszewski M., Kmiec Z., Krajka K., Swierczynski J. Increased activity of glycerol 3-phosphate dehydrogenase and other lipogenic enzymes in human bladder cancer. Horm. Metab. Res. 2003, 35:565-569.
22. Szutowicz A., Kwiatkowski J., Angielski S. Lipogenetic and glycolytic enzyme activities in carcinoma and nonmalignant diseases of the human breast. Br. J. Cancer 1979, 39:681-687.
23. 13C NMR spectroscopy. Magn. Reson. Med. 1988, 7:384-411.
24. Hatzivassiliou G., Zhao F., Bauer D.E., Andreadis C., Shaw A.N., Dhanak D., Hingorani S.R., Tuveson D.A., Thompson C.B. ATP citrate lyase inhibition can suppress tumor cell growth. Cancer Cell 2005, 8:311-321.
25. Bauer D.E., Hatzivassiliou G., Zhao F., Andreadis C., Thompson C.B. ATP citrate lyase is an important component of cell growth and transformation. Oncogene 2005, 24:6314-6322.
26. MacDonald M.J., Longacre M.J., Langberg E.C., Tibell A., Kendrick M.A., Fukao T., Ostenson C.G. Decreased levels of metabolic enzymes in pancreatic islets of patients with type 2 diabetes. Diabetologia 2009, 52:1087-1091.
27. Chu K.Y., Lin Y., Hendel A., Kulpa J.E., Brownsey R.W., Johnson J.D. ATP-citrate lyase reduction mediates palmitate-induced apoptosis in pancreatic beta cells. J. Biol. Chem. 2010, 285:32606-32615.
28. Pearce N.J., Yates J.W., Berkhout T.A., Jackson B., Tew D., Boyd H., Camilleri P., Sweeney P., Gribble A.D., Shaw A., Groot P.H. The role of ATP citrate-lyase in the metabolic regulation of plasma lipids. Hypolipidaemic effects of SB-204990, a lactone prodrug of the potent ATP citrate-lyase inhibitor SB-201076. Biochem. J. 1998, 334(Pt. 1):113-119.
29. Wang Q., Jiang L., Wang J., Li S., Yu Y., You J., Zeng R., Gao X., Rui L., Li W., Liu Y. Abrogation of hepatic ATP-citrate lyase protects against fatty liver and ameliorates hyperglycemia in leptin receptor-deficient mice. Hepatology 2009, 49:1166-1175.
30. Melnick J.Z., Srere P.A., Elshourbagy N.A., Moe O.W., Preisig P.A., Alpern R.J. Adenosine triphosphate citrate lyase mediates hypocitraturia in rats. J. Clin. Invest. 1996, 98:2381-2387.
31. Dignam J.D., Lebovitz R.M., Roeder R.G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983, 11:1475-1489.
32. Linn T.C., Srere P.A. Identification of ATP citrate lyase as a phosphoprotein. J. Biol. Chem. 1979, 254:1691-1698.
33. Oskouian B. Overexpression of fatty acid synthase in SKBR3 breast cancer cell line is mediated via a transcriptional mechanism. Cancer Lett. 2000, 149:43-51.
34. Nieva C., Marro M., Santana-Codina N., Rao S., Petrov D., Sierra A. The lipid phenotype of breast cancer cells characterized by Raman microspectroscopy: towards a stratification of malignancy. PloS One 2012, 7:e46456.
35. Sun T., Hayakawa K., Bateman K.S., Fraser M.E. Identification of the citrate-binding site of human ATP-citrate lyase using X-ray crystallography. J. Biol. Chem. 2010, 285:27418-27428.
36. Murzin A.G. Structural classification of proteins: new superfamilies. Curr. Opin. Struct. Biol. 1996, 6:386-394.
37. Joyce M.A., Fraser M.E., Brownie E.R., James M.N., Bridger W.A., Wolodko W.T. Probing the nucleotide-binding site of Escherichia coli succinyl-CoA synthetase. Biochemistry 1999, 38:7273-7283.
38. Pierce M.W., Palmer J.L., Keutmann H.T., Avruch J. ATP-citrate lyase. Structure of a tryptic peptide containing the phosphorylation site directed by glucagon and the cAMP-dependent protein kinase. J. Biol. Chem. 1981, 256:8867-8870.
39. Ramakrishna S., D'Angelo G., Benjamin W.B. Sequence of sites on ATP-citrate lyase and phosphatase inhibitor 2 phosphorylated by multifunctional protein kinase (a glycogen synthase kinase 3 like kinase). Biochemistry 1990, 29:7617-7624.
40. Berwick D.C., Hers I., Heesom K.J., Moule S.K., Tavare J.M. The identification of ATP-citrate lyase as a protein kinase B (Akt) substrate in primary adipocytes. J. Biol. Chem. 2002, 277:33895-33900.
41. Lord K.A., Wang X.M., Simmons S.J., Bruckner R.C., Loscig J., O'Connor B., Bentley R., Smallwood A., Chadwick C.C., Stevis P.E., Ciccarelli R.B. Variant cDNA sequences of human ATP:citrate lyase: cloning, expression, and purification from baculovirus-infected insect cells. Protein Expr. Purif. 1997, 9:133-141.
42. Potapova I.A., El-Maghrabi M.R., Doronin S.V., Benjamin W.B. Phosphorylation of recombinant human ATP:citrate lyase by cAMP-dependent protein kinase abolishes homotropic allosteric regulation of the enzyme by citrate and increases the enzyme activity. Allosteric activation of ATP:citrate lyase by phosphorylated sugars. Biochemistry 2000, 39:1169-1179.
43. Srere P.A. The citrate cleavage enzyme. I. Distribution and purification. J. Biol. Chem. 1959, 234:2544-2547.
44. Bernlohr D.A., Angus C.W., Lane M.D., Bolanowski M.A., Kelly T.J. Expression of specific mRNAs during adipose differentiation: identification of an mRNA encoding a homologue of myelin P2 protein. Proc. Natl. Acad. Sci. U. S. A. 1984, 81:5468-5472.
45. Zaidi N., Swinnen J.V., Smans K. ATP-citrate lyase: a key player in cancer metabolism. Cancer Res. 2012, 72:3709-3714.
46. Davidson M.H. Safety profiles for the HMG-CoA reductase inhibitors: treatment and trust. Drugs 2001, 61:197-206.
47. Sarjeant K., Stephens J.M. Adipogenesis. Cold Spring Harb. Perspect. Biol. 2012, 4:a008417.
48. Anderson S.M., Rudolph M.C., McManaman J.L., Neville M.C. Key stages in mammary gland development. Secretory activation in the mammary gland: it's not just about milk protein synthesis!. Breast Cancer Res. 2007, 9:204.
49. Hughes K., Ramakrishna S., Benjamin W.B., Woodgett J.R. Identification of multifunctional ATP-citrate lyase kinase as the alpha-isoform of glycogen synthase kinase-3. Biochem. J. 1992, 288(Pt. 1):309-314.
50. Pierce M.W., Palmer J.L., Keutmann H.T., Hall T.A., Avruch J. The insulin-directed phosphorylation site on ATP-citrate lyase is identical with the site phosphorylated by the cAMP-dependent protein kinase in vitro. J. Biol. Chem. 1982, 257:10681-10686.
51. Yu K.T., Benjamin W.B., Ramakrishna S., Khalaf N., Czech M.P. An insulin-sensitive cytosolic protein kinase accounts for the regulation of ATP citrate-lyase phosphorylation. Biochem. J. 1990, 268:539-545.
52. Rosen E.D., Walkey C.J., Puigserver P., Spiegelman B.M. Transcriptional regulation of adipogenesis. Genes Dev. 2000, 14:1293-1307.
53. Galic S., Oakhill J.S., Steinberg G.R. Adipose tissue as an endocrine organ. Mol. Cell Endocrinol. 2010, 316:129-139.
54. Porstmann T., Santos C.R., Lewis C., Griffiths B., Schulze A. A new player in the orchestra of cell growth: SREBP activity is regulated by mTORC1 and contributes to the regulation of cell and organ size. Biochem. Soc. Trans. 2009, 37:278-283.
55. Demoulin J.B., Ericsson J., Kallin A., Rorsman C., Ronnstrand L., Heldin C.H. Platelet-derived growth factor stimulates membrane lipid synthesis through activation of phosphatidylinositol 3-kinase and sterol regulatory element-binding proteins. J. Biol. Chem. 2004, 279:35392-35402.
56. Menendez J.A., Lupu R. Fatty acid synthase and the lipogenic phenotype in cancer pathogenesis. Nature reviews. Cancer 2007, 7:763-777.