Expression of the splicing factor gene SFRS10 is reduced in human obesity and contributes to enhanced lipogenesis

Cell Metabolism

Volumn 14, Issue 2, 2011, Pages 208-218

  Pihlajamäki, Jussi ^a,c   Lerin, Carles ^a,d   Itkonen, Paula ^c   Boes, Tanner ^a   Floss, Thomas ^e   Schroeder, Joshua ^a   Dearie, Farrell ^a   Crunkhorn, Sarah ^a   Burak, Furkan ^a   Jimenez Chillaron, Josep C ^a   Kuulasmaa, Tiina ^c   Miettinen, Pekka ^c   Park, Peter J ^b   Nasser, Imad ^a   Zhao, Zhenwen ^f   Zhang, Zhaiyi ^g   Xu, Yan ^f   Wurst, Wolfgang ^e,h   Ren, Hongmei ^g   Morris, Andrew J ^g   Stamm, Stefan ^g   Goldfine, Allison B ^a   Laakso, Markku ^c   Patti, Mary Elizabeth ^a   more..

^a HARVARD MEDICAL SCHOOL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c UNIVERSITY OF EASTERN FINLAND   (Finland)

^d INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^e TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^f INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g UNIVERSITY OF KENTUCKY   (United States)

^h MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN LPIN1; REGULATOR PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; LIPOGENESIS; LIVER CELL; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OBESITY; PHENOTYPE; PRIORITY JOURNAL; RNA PROCESSING; SFFRS10 GENE; SKELETAL MUSCLE;

ADULT; AGED; ANIMALS; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION REGULATION; HUMANS; LIPIDS; LIPOGENESIS; LIVER; MALE; MICE; MICE, INBRED ICR; MICE, TRANSGENIC; MIDDLE AGED; MUSCLE, SKELETAL; NERVE TISSUE PROTEINS; OBESITY; PHOSPHATIDATE PHOSPHATASE; RNA SPLICING; RNA-BINDING PROTEINS;

MUS;

EID: 79960961204     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2011.06.007     Document Type: Article

References (59)

1. Agarwal, A.K., and Garg, A. (2006). Genetic disorders of adipose tissue development, differentiation, and death. Annu. Rev. Genomics Hum. Genet. 7, 175-199.
2. Biddinger, S.B., Hernandez-Ono, A., Rask-Madsen, C., Haas, J.T., Alemán, J.O., Suzuki, R., Scapa, E.F., Agarwal, C., Carey, M.C., Stephanopoulos, G., et al. (2008). Hepatic insulin resistance is sufficient to produce dyslipidemia and susceptibility to atherosclerosis. Cell Metab. 7, 125-134. (Pubitemid 351168555)
3. Bland, C.S., Wang, E.T., Vu, A., David, M.P., Castle, J.C., Johnson, J.M., Burge, C.B., and Cooper, T.A. (2010). Global regulation of alternative splicing during myogenic differentiation. Nucleic Acids Res. 38, 7651-7664.
4. Blencowe, B.J. (2006). Alternative splicing: new insights from global analyses. Cell 126, 37-47.
5. Bou Khalil, M., Sundaram, M., Zhang, H.Y., Links, P.H., Raven, J.F., Manmontri, B., Sariahmetoglu, M., Tran, K., Reue, K., Brindley, D.N., and Yao, Z. (2009). The level and compartmentalization of phosphatidate phosphatase- 1 (lipin-1) control the assembly and secretion of hepatic VLDL. J. Lipid Res. 50, 47-58.
6. Bou Khalil, M., Blais, A., Figeys, D., and Yao, Z. (2010). Lipin - The bridge between hepatic glycerolipid biosynthesis and lipoprotein metabolism. Biochim. Biophys. Acta 1801, 1249-1259.
7. Browning, J.D., and Horton, J.D. (2004). Molecular mediators of hepatic steatosis and liver injury. J. Clin. Invest. 114, 147-152.
8. Chen, Z., Gropler, M.C., Norris, J., Lawrence, J.C., Jr., Harris, T.E., and Finck, B.N. (2008). Alterations in hepatic metabolism in fld mice reveal a role for lipin 1 in regulating VLDL-triacylglyceride secretion. Arterioscler. Thromb. Vasc. Biol. 28, 1738-1744.
9. Cheung, C.Y., Tso, A.W., Cheung, B.M., Xu, A., Ong, K.L., Fong, C.H., Wat, N.M., Janus, E.D., Sham, P.C., and Lam, K.S. (2010). Obesity susceptibility genetic variants identified from recent genome-wide association studies: implications in a chinese population. J. Clin. Endocrinol. Metab. 95, 1395-1403.
10. Cléry, A., Jayne, S., Benderska, N., Dominguez, C., Stamm, S., and Allain, F.H. (2011). Molecular basis of purine-rich RNA recognition by the human SR-like protein Tra2-b1. Nat. Struct. Mol. Biol. 18, 443-450.
11. Croce, M.A., Eagon, J.C., LaRiviere, L.L., Korenblat, K.M., Klein, S., and Finck, B.N. (2007). Hepatic lipin 1beta expression is diminished in insulin-resistant obese subjects and is reactivated by marked weight loss. Diabetes 56, 2395-2399. (Pubitemid 47358247)
12. Csaki, L.S., and Reue, K. (2010). Lipins: multifunctional lipid metabolism proteins. Annu. Rev. Nutr. 30, 257-272.
13. Donkor, J., Sariahmetoglu, M., Dewald, J., Brindley, D.N., and Reue, K. (2007). Three mammalian lipins act as phosphatidate phosphatases with distinct tissue expression patterns. J. Biol. Chem. 282, 3450-3457.
14. Donkor, J., Sparks, L.M., Xie, H., Smith, S.R., and Reue, K. (2008). Adipose tissue lipin-1 expression is correlated with peroxisome proliferator-activated receptor alpha gene expression and insulin sensitivity in healthy young men. J. Clin. Endocrinol. Metab. 93, 233-239.
15. Faustino, N.A., and Cooper, T.A. (2003). Pre-mRNA splicing and human disease. Genes Dev. 17, 419-437. (Pubitemid 36258756)
16. Finck, B.N., Gropler, M.C., Chen, Z., Leone, T.C., Croce, M.A., Harris, T.E., Lawrence, J.C., Jr., and Kelly, D.P. (2006). Lipin 1 is an inducible amplifier of the hepatic PGC-1alpha/PPARalpha regulatory pathway. Cell Metab. 4, 199-210. (Pubitemid 44283957)
17. Ghosh, N., Patel, N., Jiang, K., Watson, J.E., Cheng, J., Chalfant, C.E., and Cooper, D.R. (2007). Ceramide-activated protein phosphatase involvement in insulin resistance via Akt, serine/arginine-rich protein 40, and ribonucleic acid splicing in L6 skeletal muscle cells. Endocrinology 148, 1359-1366.
18. Gibbons, G.F., Khurana, R., Odwell, A., and Seelaender, M.C. (1994). Lipid balance in HepG2 cells: active synthesis and impaired mobilization. J. Lipid Res. 35, 1801-1808. (Pubitemid 24331282)
19. Glatz, D.C., Rujescu, D., Tang, Y., Berendt, F.J., Hartmann, A.M., Faltraco, F., Rosenberg, C., Hulette, C., Jellinger, K., Hampel, H., et al. (2006). The alternative splicing of tau exon 10 and its regulatory proteins CLK2 and TRA2-BETA1 changes in sporadic Alzheimer's disease. J. Neurochem. 96, 635-644.
20. Goren, A., Kim, E., Amit, M., Bochner, R., Lev-Maor, G., Ahituv, N., and Ast, G. (2008). Alternative approach to a heavy weight problem. Genome Res. 18, 214-220. (Pubitemid 351240731)
21. Guo, S., Copps, K.D., Dong, X., Park, S., Cheng, Z., Pocai, A., Rossetti, L., Sajan, M., Farese, R.V., and White, M.F. (2009). The Irs1 branch of the insulin signaling cascade plays a dominant role in hepatic nutrient homeostasis. Mol. Cell. Biol. 29, 5070-5083.
22. Han, G.S., and Carman, G.M. (2010). Characterization of the human LPIN1- encoded phosphatidate phosphatase isoforms. J. Biol. Chem. 285, 14628-14638.
23. Han, G.S., Wu, W.I., and Carman, G.M. (2006). The Saccharomyces cerevisiae Lipin homolog is a Mg2+-dependent phosphatidate phosphatase enzyme. J. Biol. Chem. 281, 9210-9218.
24. Huang, H., Gao, Q., Peng, X., Choi, S.Y., Sarma, K., Ren, H., Morris, A.J., and Frohman, M.A. (2011). piRNA-associated germline nuage formation and spermatogenesis require MitoPLD profusogenic mitochondrial-surface lipid signaling. Dev. Cell 20, 376-387.
25. Jacob, S., Machann, J., Rett, K., Brechtel, K., Volk, A., Renn, W., Maerker, E., Matthaei, S., Schick, F., Claussen, C.D., and Häring, H.U. (1999). Association of increased intramyocellular lipid content with insulin resistance in lean nondiabetic offspring of type 2 diabetic subjects. Diabetes 48, 1113-1119. (Pubitemid 29226360)
26. Jiang, K., Patel, N.A., Watson, J.E., Apostolatos, H., Kleiman, E., Hanson, O., Hagiwara, M., and Cooper, D.R. (2009). Akt2 regulation of Cdc2-like kinases (Clk/Sty), serine/arginine-rich (SR) protein phosphorylation, and insulin-induced alternative splicing of PKCbetaII messenger ribonucleic acid. Endocrinology 150, 2087-2097.
27. Karni, R., de Stanchina, E., Lowe, S.W., Sinha, R., Mu, D., and Krainer, A.R. (2007). The gene encoding the splicing factor SF2/ASF is a proto-oncogene. Nat. Struct. Mol. Biol. 14, 185-193.
28. Kishore, S., and Stamm, S. (2006). The snoRNA HBII-52 regulates alternative splicing of the serotonin receptor 2C. Science 311, 230-232. (Pubitemid 43108188)
29. Kotronen, A., Westerbacka, J., Bergholm, R., Pietiläinen, K.H., and Yki- Järvinen, H. (2007). Liver fat in the metabolic syndrome. J. Clin. Endocrinol. Metab. 92, 3490-3497.
30. Lee, G.H., Proenca, R., Montez, J.M., Carroll, K.M., Darvishzadeh, J.G., Lee, J.I., and Friedman, J.M. (1996). Abnormal splicing of the leptin receptor in diabetic mice. Nature 379, 632-635. (Pubitemid 26053452)
31. Lefai, E., Roques, M., Vega, N., Laville, M., and Vidal, H. (2001). Expression of the splice variants of the p85alpha regulatory subunit of phosphoinositide 3-kinase in muscle and adipose tissue of healthy subjects and type 2 diabetic patients. Biochem. J. 360, 117-126.
32. Liu, G.H., Qu, J., Carmack, A.E., Kim, H.B., Chen, C., Ren, H., Morris, A.J., Finck, B.N., and Harris, T.E. (2010). Lipin proteins form homo- and heterooligomers. Biochem. J. 432, 65-76.
33. Mende, Y., Jakubik, M., Riessland, M., Schoenen, F., Rossbach, K., Kleinridders, A., Köhler, C., Buch, T., and Wirth, B. (2010). Deficiency of the splicing factor Sfrs10 results in early embryonic lethality in mice and has no impact on full-length SMN/Smn splicing. Hum. Mol. Genet. 19, 2154-2167.
34. Nayler, O., Cap, C., and Stamm, S. (1998). Human transformer-2-beta gene (SFRS10): complete nucleotide sequence, chromosomal localization, and generation of a tissue-specific isoform. Genomics 53, 191-202. (Pubitemid 28496609)
35. Nilsen, T.W., and Graveley, B.R. (2010). Expansion of the eukaryotic proteome by alternative splicing. Nature 463, 457-463.
36. Patel, N.A., Kaneko, S., Apostolatos, H.S., Bae, S.S., Watson, J.E., Davidowitz, K., Chappell, D.S., Birnbaum, M.J., Cheng, J.Q., and Cooper, D.R. (2005). Molecular and genetic studies imply Akt-mediated signaling promotes protein kinase CbetaII alternative splicing via phosphorylation of serine/arginine-rich splicing factor SRp40. J. Biol. Chem. 280, 14302-14309.
37. Péterfy, M., Phan, J., Xu, P., and Reue, K. (2001). Lipodystrophy in the fld mouse results from mutation of a new gene encoding a nuclear protein, lipin. Nat. Genet. 27, 121-124.
38. Péterfy, M., Phan, J., and Reue, K. (2005). Alternatively spliced lipin isoforms exhibit distinct expression pattern, subcellular localization, and role in adipogenesis. J. Biol. Chem. 280, 32883-32889.
39. Phan, J., and Reue, K. (2005). Lipin, a lipodystrophy and obesity gene. Cell Metab. 1, 73-83. (Pubitemid 43960586)
40. Pihlajamaki, J., Boes, T., Kim, E.Y., Dearie, F., Kim, B.W., Schroeder, J., Mun, E., Nasser, I., Park, P.J., Bianco, A.C., et al. (2009). Thyroid Hormone-Related Regulation of Gene Expression in Human Fatty Liver. J. Clin. Endocrinol. Metab. 94, 3521-3529.
41. Ren, H., Federico, L., Huang, H., Sunkara, M., Drennan, T., Frohman, M.A., Smyth, S.S., and Morris, A.J. (2010). A phosphatidic acid binding/nuclear localization motif determines lipin1 function in lipid metabolism and adipogenesis. Mol. Biol. Cell 21, 3171-3181.
42. Ryu, D., Oh, K.J., Jo, H.Y., Hedrick, S., Kim, Y.N., Hwang, Y.J., Park, T.S., Han, J.S., Choi, C.S., Montminy, M., and Koo, S.H. (2009). TORC2 regulates hepatic insulin signaling via a mammalian phosphatidic acid phosphatase, LIPIN1. Cell Metab. 9, 240-251.
43. Salomonis, N., Schlieve, C.R., Pereira, L., Wahlquist, C., Colas, A., Zambon, A.C., Vranizan, K., Spindler, M.J., Pico, A.R., Cline, M.S., et al. (2010). Alternative splicing regulates mouse embryonic stem cell pluripotency and differentiation. Proc. Natl. Acad. Sci. USA 107, 10514-10519.
44. Sesti, G., Marini, M.A., Tullio, A.N., Montemurro, A., Borboni, P., Fusco, A., Accili, D., and Lauro, R. (1991). Altered expression of the two naturally occurring human insulin receptor variants in isolated adipocytes of non-insulindependent diabetes mellitus patients. Biochem. Biophys. Res. Commun. 181, 1419-1424.
45. Stamm, S., Ben-Ari, S., Rafalska, I., Tang, Y., Zhang, Z., Toiber, D., Thanaraj, T.A., and Soreq, H. (2005). Function of alternative splicing. Gene 344, 1-20. (Pubitemid 40126788)
46. Stoilov, P., Daoud, R., Nayler, O., and Stamm, S. (2004). Human tra2-beta1 autoregulates its protein concentration by influencing alternative splicing of its pre-mRNA. Hum. Mol. Genet. 13, 509-524.
47. Stoss, O., Stoilov, P., Hartmann, A.M., Nayler, O., and Stamm, S. (1999). The in vivo minigene approach to analyze tissue-specific splicing. Brain Res. Brain Res. Protoc. 4, 383-394.
48. Subramanian, A., Tamayo, P., Mootha, V.K., Mukherjee, S., Ebert, B.L., Gillette, M.A., Paulovich, A., Pomeroy, S.L., Golub, T.R., Lander, E.S., and Mesirov, J.P. (2005). Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 102, 15545-15550.
49. Suviolahti, E., Reue, K., Cantor, R.M., Phan, J., Gentile, M., Naukkarinen, J., Soro-Paavonen, A., Oksanen, L., Kaprio, J., Rissanen, A., et al. (2006). Cross-species analyses implicate Lipin 1 involvement in human glucose metabolism. Hum. Mol. Genet. 15, 377-386.
50. Thorleifsson, G., Walters, G.B., Gudbjartsson, D.F., Steinthorsdottir, V., Sulem, P., Helgadottir, A., Styrkarsdottir, U., Gretarsdottir, S., Thorlacius, S., Jonsdottir, I., et al. (2009). Genome-wide association yields new sequence variants at seven loci that associate with measures of obesity. Nat. Genet. 41, 18-24.
51. Venables, J.P. (2004). Aberrant and alternative splicing in cancer. Cancer Res. 64, 7647-7654.
52. Wang, E.T., Sandberg, R., Luo, S., Khrebtukova, I., Zhang, L., Mayr, C., Kingsmore, S.F., Schroth, G.P., and Burge, C.B. (2008). Alternative isoform regulation in human tissue transcriptomes. Nature 456, 470-476. (Pubitemid 352759009)
53. Xiao, Y., Chen, Y., Kennedy, A.Q., Belinson, J., and Xu, Y. (2000). Evaluation of plasma lysophospholipids for diagnostic significance using electrospray ionization mass spectrometry (ESI-MS) analysis. Ann. N.Y. Acad. Science 905, 242-259.
54. Yao-Borengasser, A., Rasouli, N., Varma, V., Miles, L.M., Phanavanh, B., Starks, T.N., Phan, J., Spencer, H.J., 3rd, McGehee, R.E., Jr., Reue, K., and Kern, P.A. (2006). Lipin expression is attenuated in adipose tissue of insulinresistant human subjects and increases with peroxisome proliferator-activated receptor gamma activation. Diabetes 55, 2811-2818. (Pubitemid 44923681)
55. Yechoor, V.K., Patti, M.E., Saccone, R., and Kahn, C.R. (2002). Coordinated patterns of gene expression for substrate and energy metabolism in skeletal muscle of diabetic mice. Proc. Natl. Acad. Sci. USA 99, 10587-10592.
56. Yechoor, V.K., Patti, M.E., Ueki, K., Laustsen, P.G., Saccone, R., Rauniyar, R., and Kahn, C.R. (2004). Distinct pathways of insulin-regulated versus diabetesregulated gene expression: An in vivo analysis in MIRKO mice. Proc. Natl. Acad. Sci. USA 101, 16525-16530.
57. Zeharia, A., Shaag, A., Houtkooper, R.H., Hindi, T., de Lonlay, P., Erez, G., Hubert, L., Saada, A., de Keyzer, Y., Eshel, G., et al. (2008). Mutations in LPIN1 cause recurrent acute myoglobinuria in childhood. Am. J. Hum. Genet. 83, 489-494.
58. Zhang, W., Patil, S., Chauhan, B., Guo, S., Powell, D.R., Le, J., Klotsas, A., Matika, R., Xiao, X., Franks, R., et al. (2006). FoxO1 regulates multiple metabolic pathways in the liver: effects on gluconeogenic, glycolytic, and lipogenic gene expression. J. Biol. Chem. 281, 10105-10117.
59. Zhong, X.Y., Wang, P., Han, J., Rosenfeld, M.G., and Fu, X.D. (2009). SR proteins in vertical integration of gene expression from transcription to RNA processing to translation. Mol. Cell 35, 1-10.