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Molecular cloning, sequence characterization, and tissue expression analysis of chicken sphingomyelin synthase 1 (SMS1)

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Abstract

Sphingomyelin synthase 1 (SMS1) is an important cytoplasmic protein which may have functions that go beyond housekeeping function of sphingomyelin (SM) synthesis. In this study, a Hi-Line Brown chicken SMS1 gene was cloned, sequenced, and characterized. The SMS1 full-length coding sequence (CDS) consisted of 1242 nt and encoded 413 amino acids with a molecular weight of 48.54 kDa. The N-terminal sterile alpha motif (SAM) was well conserved between chicken and other animals. The 3D structure of the SMS1 (1-78AA) by homology modeling was similar to that of mouse phosphatidyl ceramide cholinephosphotransferase 1 (2d8c Chain: A (1-97)). The phylogenetic tree analysis revealed that chicken SMS1 had closer genetic relationship with that of land mammals. RT-PCR analysis showed that the SMS1 transcripts were constitutively expressed in 11 tissues tested. Several microRNA target sites were predicted in the CDS of chicken SMS1 mRNA. These data serve as a foundation for further insight into the chicken SMS1 gene.

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Abbreviations

AA:

Amino acid

CDS:

Coding sequence

SAM:

Sterile alpha motif

TNF-a:

Tumor necrosis factor-a

SM:

Sphingomyelin

PC:

Phosphatidylcholine

DAG:

Diacylglycerol

ROS:

Reactive oxygen species

bFGF:

Basic fibroblast growth factor

NF-κB:

Nuclear factor-kappa B

MHC:

Major histocompatibility complex

SV40:

Simian virus 40

3D:

Three dimensional

References

  1. Merrill AH, Jones DD (1990) An update of the enzymology and regulation of sphingomyelin metabolism. Biochim Biophys Acta 1044:1–12

    PubMed  CAS  Google Scholar 

  2. Huitema K, van den Dikkenberg J, Brouwers JF, Holthuis JC (2004) Identification of a family of animal sphingomyelin synthases. EMBO J 23:33–44

    Article  PubMed  CAS  Google Scholar 

  3. Ding T, Li Z, Hailemariam T, Mukherjee S, Maxfield FR, Wu M-P, Jiang X-C (2008) SMS overexpression and knockdown: impact on cellular sphingomyelin and diacylglycerol metabolism, and cell apoptosis. J Lipid Res 49:376–385

    Article  PubMed  CAS  Google Scholar 

  4. Li Z, Hailemariam TK, Zhou H, Li Y, Duckworth DC, Peake DA, Zhang Y, Kuo MS, Cao G, Jiang XC (2007) Inhibition of sphingomyelin synthase (SMS) affects intracellular sphingomyelin accumulation and plasma membrane lipid organization. Biochim Biophys Acta 1771:1186–1194

    PubMed  CAS  Google Scholar 

  5. Miro-Obradors M-J, Osada J, Aylagas H, Sanchez-Vegazo I, Palacios-Alaiz E (1993) Microsomal sphingomyelin accumulation in thioacetamide-injured regenerating rat liver: involvement of sphingomyelin synthase activity. Carcinogenesis 14:941–946

    Article  PubMed  CAS  Google Scholar 

  6. Riboni L, Viani P, Bassi R, Giussani P, Tettamanti G (2001) Basic fibroblast growth factor-induced proliferation of primary astrocytes: evidence for the involvement of sphingomyelin biosynthesis. J Biol Chem 276:12797–12804

    Article  PubMed  CAS  Google Scholar 

  7. Yamaoka S, Miyaji M, Kitano T, Umehara H, Okazaki T (2004) Expression cloning of a human cDNA restoring sphingomyelin synthesis and cell growth in sphingomyelin synthase-defective lymphoid cells. J Biol Chem 279:18688–18693

    Article  PubMed  CAS  Google Scholar 

  8. Separovic D, Hanada K, Maitah MYA, Nagy B, Hang I, Tainsky MA, Kraniak JM, Bielawski J (2007) Sphingomyelin synthase 1 suppresses ceramide production and apoptosis post-photodamage. Biochem Biophys Res Commun 358:196–202

    Article  PubMed  CAS  Google Scholar 

  9. Yano M, Watanabe K, Yamamoto T, Ikeda K, Senokuchi T, Lu M, Kadomatsu T, Tsukano H, Ikawa M, Okabe M, Yamaoka S, Okazaki T, Umehara H, Gotoh T, Song WJ, Node K, Taguchi R, Yamagata K, Oike Y (2011) Mitochondrial dysfunction and increased reactive oxygen species impair insulin secretion in sphingomyelin synthase 1-null mice. J Biol Chem 286:3992–4002

    Article  PubMed  CAS  Google Scholar 

  10. Van der Luit AH, Budde M, Zerp S, Caan W, Klarenbeek JB, Verheij M, Van Blitterswijk WJ (2007) Resistance to alkyl-lysophospholipid-induced apoptosis due to downregulated sphingomyelin synthase 1 expression with consequent sphingomyelin-and cholesterol-deficiency in lipid rafts. Biochem J 401:541–549

    Article  PubMed  Google Scholar 

  11. Van der Luit AH, Vink SR, Klarenbeek JB, Perrissoud D, Solary E, Verheij M, van Blitterswijk WJ (2007) A new class of anticancer alkylphospholipids uses lipid rafts as membrane gateways to induce apoptosis in lymphoma cells. Mol Cancer Ther 6:2337–2345

    Article  PubMed  Google Scholar 

  12. Tafesse FG, Huitema K, Hermansson M, van der Poel S, van den Dikkenberg J, Uphoff A, Somerharju P, Holthuis JC (2007) Both sphingomyelin synthases SMS1 and SMS2 are required for sphingomyelin homeostasis and growth in human HeLa cells. J Biol Chem 282:17537–17547

    Article  PubMed  CAS  Google Scholar 

  13. Bourteele S, Hausser A, Doppler H, Horn-Muller J, Ropke C, Schwarzmann G, Pfizenmaier K, Muller G (1998) Tumor necrosis factor induces ceramide oscillations and negatively controls sphingolipid synthases by caspases in apoptotic Kym-1 cells. J Biol Chem 273:31245–31251

    Article  PubMed  CAS  Google Scholar 

  14. Watanabe M, Kitano T, Kondo T, Yabu T, Taguchi Y, Tashima M, Umehara H, Domae N, Uchiyama T, Okazaki T (2004) Increase of nuclear ceramide through caspase-3-dependent regulation of the “sphingomyelin cycle” in Fas-induced apoptosis. Cancer Res 64:1000–1007

    Article  PubMed  CAS  Google Scholar 

  15. Separovic D, Semaan L, Tarca AL, Awad Maitah MY, Hanada K, Bielawski J, Villani M, Luberto C (2008) Suppression of sphingomyelin synthase 1 by small interference RNA is associated with enhanced ceramide production and apoptosis after photodamage. Exp Cell Res 314:1860–1868

    Article  PubMed  CAS  Google Scholar 

  16. Luberto C, Yoo DS, Suidan HS, Bartoli GM, Hannun YA (2000) Differential effects of sphingomyelin hydrolysis and resynthesis on the activation of NF-κB in normal and SV40-transformed human fibroblasts. J Biol Chem 275:14760–14766

    Article  PubMed  CAS  Google Scholar 

  17. Linn SC, Kim HS, Keane EM, Andras LM, Wang E, Merrill AH (2001) Regulation of de novo sphingolipid biosynthesis and the toxic consequences of its disruption. Biochem Soc Trans 29:831–855

    Article  PubMed  CAS  Google Scholar 

  18. Miyaji M, Jin ZX, Yamaoka S, Amakawa R, Fukuhara S, Sato SB, Kobayashi T, Domae N, Mimori T, Bloom ET, Okazaki T, Umehara H (2005) Role of membrane sphingomyelin and ceramide in platform formation for Fas-mediated apoptosis. J Exp Med 202:249–259

    Article  PubMed  CAS  Google Scholar 

  19. Simons K, Ikonen E (1997) Functional rafts in cell membranes. Nature 387:569–572

    Article  PubMed  CAS  Google Scholar 

  20. Simons K, van Meer G (1988) Lipid sorting in epithelial cells. Biochemistry 27:6197–6202

    Article  PubMed  CAS  Google Scholar 

  21. Cherukuri A, Dykstra M, Pierce SK (2001) Floating the raft hypothesis: lipid rafts play a role in immune cell activation. Immunity 14:657–660

    Article  PubMed  CAS  Google Scholar 

  22. Alonso MA, Millan J (2001) The role of lipid rafts in signalling and membrane trafficking in T lymphocytes. J Cell Sci 114:3957–3965

    PubMed  CAS  Google Scholar 

  23. Munro S (2003) Lipid rafts: elusive or illusive? Cell 115:377–388

    Article  PubMed  CAS  Google Scholar 

  24. Kindt TJ, Goldsby RA, Osborne BA, Kuby J (2007) Kuby immunology. Macmillan, New Delhi

    Google Scholar 

  25. Jin ZX, Huang CR, Dong L, Goda S, Kawanami T, Sawaki T, Sakai T, Tong XP, Masaki Y, Fukushima T, Tanaka M, Mimori T, Tojo H, Bloom ET, Okazaki T, Umehara H (2008) Impaired TCR signaling through dysfunction of lipid rafts in sphingomyelin synthase1 (SMS1)-knockdown T cells. Int Immunol 20:1427–1437

    Article  PubMed  CAS  Google Scholar 

  26. Wan F, Lenardo MJ (2010) The nuclear signaling of NF-kappaB: current knowledge, new insights, and future perspectives. Cell Res 20:24–33

    Article  PubMed  CAS  Google Scholar 

  27. Lenardo MJ, Baltimore D (1989) NF-kappa B: a pleiotropic mediator of inducible and tissue-specific gene control. Cell 58:227–229

    Article  PubMed  CAS  Google Scholar 

  28. Hayden MS, Ghosh S (2004) Signaling to NF-kappaB. Genes Dev 18:2195–2224

    Article  PubMed  CAS  Google Scholar 

  29. Hayden MS, Ghosh S (2008) Shared principles in NF-kappaB signaling. Cell 132:344–362

    Article  PubMed  CAS  Google Scholar 

  30. Vallabhapurapu S, Karin M (2009) Regulation and function of Nf-kappaB transcription factors in the immune system. Annu Rev Immunol 27:693–733

    Article  PubMed  CAS  Google Scholar 

  31. Kang SM, Tran AC, Grilli M, Lenardo MJ (1992) NF-kappa B subunit regulation in nontransformed CD4+ T lymphocytes. Science 256:1452–1456

    Article  PubMed  CAS  Google Scholar 

  32. Su H, Bidère N, Zheng L, Cubre A, Sakai K, Dale J, Salmena L, Hakem R, Straus S, Lenardo M (2005) Requirement for caspase-8 in NF-kappaB activation by antigen receptor. Science 307:1465–1468

    Article  PubMed  CAS  Google Scholar 

  33. Bidère N, Ngo VN, Lee J, Collins C, Zheng L, Wan F, Davis RE, Lenz G, Anderson DE, Arnoult D, Vazquez A, Sakai K, Zhang J, Meng Z, Veenstra TD, Staudt LM, Lenardo MJ (2009) Casein kinase 1alpha governs antigen-receptor-induced NF-kappaB activation and human lymphoma cell survival. Nature 458:92–96

    Article  PubMed  Google Scholar 

  34. Kim JA, Wei Y, Sowers JR (2008) Role of mitochondrial dysfunction in insulin resistance. Circ Res 102:401–414

    Article  PubMed  CAS  Google Scholar 

  35. Maasen JA (2008) Mitochondria, body fat and type 2 diabetes: hat is the connection. Minerva Med 99:241–251

    PubMed  CAS  Google Scholar 

  36. Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODEL Workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22:195–201

    Article  PubMed  CAS  Google Scholar 

  37. Schwede T, Kopp J, Guex N, Peitsch MC (2003) SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res 31:3381–3385

    Article  PubMed  CAS  Google Scholar 

  38. Guex N, Peitsch MC (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modelling. Electrophoresis 18:2714–2723

    Article  PubMed  CAS  Google Scholar 

  39. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297

    Article  PubMed  CAS  Google Scholar 

  40. Zeng Y, Yi R, Cullen BR (2003) MicroRNAs and small interfering RNAs can inhibit mRNA expression by similar mechanisms. Proc Natl Acad Sci USA 100:9779–9784

    Article  PubMed  CAS  Google Scholar 

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Acknowledgment

This study was supported by foundation for Young Scholars of Harbin Normal University (10KXQ-06).

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Authors and Affiliations

  1. College of Life Science and Technology, Harbin Normal University, No. 1 South of Shida RD Limin Development Zone, Harbin City, 150025, Heilongjiang Province, People’s Republic of China

    Chaolai Man & Jongeun Lee

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  1. Chaolai Man
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  2. Jongeun Lee
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Correspondence to Chaolai Man.

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Man, C., Lee, J. Molecular cloning, sequence characterization, and tissue expression analysis of chicken sphingomyelin synthase 1 (SMS1). Mol Cell Biochem 357, 353–361 (2011). https://doi.org/10.1007/s11010-011-0906-2

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