Skip to main content

Advertisement

SpringerLink
Log in

Identification and gene expression profile analysis of a major type of lipoprotein lipase in adult medaka Oryzias latipes

  • Original Article
  • Chemistry and Biochemistry
  • Published:
Fisheries Science Aims and scope Submit manuscript

Abstract

Lipoprotein lipase (LPL) plays a critical role in the metabolism of circulating triacylglycerols (TAGs) packaged in lipoproteins. Fish have two LPL genes, encoding the LPL1 and LPL2 enzymes, but their functions are not yet clearly understood. To provide a basis for further investigation, we cloned a cDNA encoding LPL from the liver of adult medaka Oryzias latipes. The cloned LPL gene was found to share a high identity with LPL1 genes from several fish species and was denoted medaka LPL1. Screening against publicly available medaka expressed sequence tag (EST) databases revealed that LPL1 transcripts are abundant in ESTs from various developmental stages and tissues. The EST screening also identified a second LPL-like gene, denoted medaka LPL2, the transcripts of which were found exclusively in EST libraries from embryonic stages. The LPL1 cDNA obtained by a combination of 3′ and 5′ rapid amplification of cDNA ends was 2,259 bp, with an open reading frame of 1,551 bp encoding 516 amino acids. Quantitative real-time PCR further confirmed the ubiquitous distribution of LPL1 transcripts, with high levels in the liver and visceral adipose tissue, and the lowest level in the intestine. A relatively high expression of the LPL1 gene was also found in the brain, suggesting the potential function of LPL1 in this organ.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Smith LC, Pownall HJ, Gotto AM Jr (1978) The plasma lipoproteins: structure and metabolism. Annu Rev Biochem 47:751–777

    Article  PubMed  CAS  Google Scholar 

  2. Rogie A, Skinner RE (1985) The roles of the intestine and liver in the biosynthesis of plasma lipoproteins in the rainbow trout, Salmo gairdnerii Richardson. Comp Biochem Physiol B 81:285–289

    Google Scholar 

  3. Nilsson-Ehle P, Garfinkel AS, Schotz MC (1980) Lipolytic enzymes and plasma lipoprotein metabolism. Annu Rev Biochem 49:667–693

    Article  PubMed  CAS  Google Scholar 

  4. Mahley RW, Innerarity TL, Rall SC Jr, Weisgraber KH (1984) Plasma lipoproteins: apolipoprotein structure and function. J Lipid Res 25:1277–1294

    PubMed  CAS  Google Scholar 

  5. Goldberg IJ (1996) Lipoprotein lipase and lipolysis: central roles in lipoprotein metabolism and atherogenesis. J Lipid Res 37:693–707

    PubMed  CAS  Google Scholar 

  6. Wang H, Eckel RH (2009) Lipoprotein lipase: from gene to obesity. Am J Physiol Endocrinol Metab 297:E271–E288

    Article  PubMed  CAS  Google Scholar 

  7. Beigneux AP, Davies BS, Gin P, Weinstein MM, Farber E, Qiao X, Peale F, Bunting S, Walzem RL, Wong JS, Blaner WS, Ding ZM, Melford K, Wongsiriroj N, Shu X, de Sauvage F, Ryan RO, Fong LG, Bensadoun A, Young SG (2007) Glycosylphosphatidylinositol-anchored high-density lipoprotein-binding protein 1 plays a critical role in the lipolytic processing of chylomicrons. Cell Metab 5:279–291

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  8. Berryman DE, Bensadoun A (1995) Heparan sulfate proteoglycans are primarily responsible for the maintenance of enzyme activity, binding, and degradation of lipoprotein lipase in Chinese hamster ovary cells. J Biol Chem 270:24525–24531

    Article  PubMed  CAS  Google Scholar 

  9. Rumsey SC, Obunike JC, Arad Y, Deckelbaum RJ, Goldberg IJ (1992) Lipoprotein lipase-mediated uptake and degradation of low density lipoproteins by fibroblasts and macrophages. J Clin Invest 90:1504–1512

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  10. Fernández-Borja M, Bellido D, Vilella E, Olivecrona G, Vilaró S (1996) Lipoprotein lipase-mediated uptake of lipoprotein in human fibroblasts: evidence for an LDL receptor-independent internalization pathway. J Lipid Res 37:464–481

    PubMed  Google Scholar 

  11. Weinstock PH, Bisgaier CL, Aalto-Setala K, Radner H, Ramakrishnan R, Levak-Frank S, Essenburg AD, Zechner R, Breslow JL (1995) Severe hypertriglyceridemia, reduced high density lipoprotein, and neonatal death in lipoprotein lipase knockout mice—mild hypertriglyceridemia with impaired very low density lipoprotein clearance in heterozygotes. J Clin Invest 96:2555–2568

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  12. Gotoda T, Senda M, Gamou T, Furuichi Y, Oka K (1989) Nucleotide sequence of human cDNA coding for a lipoprotein lipase (LPL) cloned from placental cDNA library. Nucleic Acids Res 17:2351

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  13. Semenkovich CF, Chen SH, Wims M, Luo CC, Li WH, Chan L (1989) Lipoprotein lipase and hepatic lipase mRNA tissue specific expression, developmental regulation, and evolution. J Lipid Res 30:423–431

    PubMed  CAS  Google Scholar 

  14. Kirchgessner TG, Svenson KL, Lusis AJ, Schotz MC (1987) The sequence of cDNA encoding lipoprotein lipase. A member of a lipase gene family. J Biol Chem 262:8463–8466

    PubMed  CAS  Google Scholar 

  15. Senda M, Oka K, Brown WV, Qasba PK, Furuichi Y (1987) Molecular cloning and sequence of a cDNA coding for bovine lipoprotein lipase. Proc Natl Acad Sci USA 84:4369–4373

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  16. Lindberg A, Olivecrona G (2002) Lipoprotein lipase from rainbow trout differs in several respects from the enzyme in mammals. Gene 292:213–223

    Article  PubMed  CAS  Google Scholar 

  17. Saera-Vila A, Calduch-Giner JA, Gomez-Requeni P, Medale F, Kaushik S, Perez-Sanchez J (2005) Molecular characterization of gilthead sea bream (Sparus aurata) lipoprotein lipase. Transcriptional regulation by season and nutritional condition in skeletal muscle and fat storage tissues. Comp Biochem Physiol B 142:224–232

    Article  PubMed  CAS  Google Scholar 

  18. Merkel M, Eckel RH, Goldberg IJ (2002) Lipoprotein lipase: genetics, lipid uptake, and regulation. J Lipid Res 43:1997–2006

    Article  PubMed  CAS  Google Scholar 

  19. Zechner R (1997) The tissue-specific expression of lipoprotein lipase: implications for energy and lipoprotein metabolism. Curr Opin Lipidol 8:77–88

    Article  PubMed  CAS  Google Scholar 

  20. Vilaró S, Llobera M, Bengtsson-Olivecrona G, Olivecrona T (1988) Synthesis of lipoprotein lipase in the liver of newborn rats and localization of the enzyme by immunofluorescence. Biochem J 249:549–556

    PubMed Central  PubMed  Google Scholar 

  21. Gimenez-Llort L, Vilanova J, Skottova N, Bengtsson-Olivecrona G, Llobera M, Robert MQ (1991) Lipoprotein lipase enables triacylglycerol hydrolysis by perfused newborn rat liver. Am J Physiol 261:G641–G647

    PubMed  CAS  Google Scholar 

  22. Cheng HL, Sun SP, Peng YX, Shi XY, Shen X, Meng XP, Dong ZG (2010) cDNA sequence and tissues expression analysis of lipoprotein lipase from common carp (Cyprinus carpio Var. Jian). Mol Biol Rep 37:2665–2673

    Article  PubMed  CAS  Google Scholar 

  23. Cheng HL, Wang X, Peng YX, Meng XP, Sun SP, Shi XY (2009) Molecular cloning and tissue distribution of lipoprotein lipase full-length cDNA from Pengze crucian carp (Carassius auratusvar. Pengze). Comp Biochem Physiol B 153:109–115

    Article  PubMed  CAS  Google Scholar 

  24. Oku H, Koizumi N, Okumura T, Kobayashi T, Umino T (2006) Molecular characterization of lipoprotein lipase, hepatic lipase and pancreatic lipase genes: effects of fasting and refeeding on their gene expression in red sea bream Pagrus major. Comp Biochem Physiol B 145:168–178

    Article  PubMed  CAS  Google Scholar 

  25. Kaneko G, Yamada T, Han Y, Hirano Y, Khieokhajonkhet A, Shirakami H, Nagasaka R, Kondo H, Hirono I, Ushio H, Watabe S (2013) Differences in lipid distribution and expression of peroxisome proliferator-activated receptor gamma and lipoprotein lipase genes in torafugu and red seabream. Gen Comp Endocrinol 184:51–60

    Article  PubMed  CAS  Google Scholar 

  26. Wittbrodt J, Shima A, Schartl M (2002) Medaka—a model organism from the far East. Nat Rev Genet 3:53–64

    Article  PubMed  CAS  Google Scholar 

  27. Kinoshita M, Toyohara H, Sakaguchi M, Inoue K, Yamashita S, Satake M, Wakamatsu Y, Ozato K (1996) A stable line of transgenic medaka (Oryzias latipes) carrying the CAT gene. Aquaculture 143:267–276

    Article  Google Scholar 

  28. Ono Y, Kinoshita S, Ikeda D, Watabe S (2010) Early development of medaka Oryzias latipes muscles as revealed by transgenic approaches using embryonic and larval types of myosin heavy chain genes. Dev Dyn 239:1807–1817

    Article  PubMed  CAS  Google Scholar 

  29. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  30. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  31. Zhang ZB, Hu JY (2007) Development and validation of endogenous reference genes for expression profiling of medaka (Oryzias latipes) exposed to endocrine disrupting chemicals by quantitative real-time RT-PCR. Toxicol Sci 95:356–368

    Article  PubMed  CAS  Google Scholar 

  32. Cardin AD, Weintraub HJ (1989) Molecular modeling of protein–glycosaminoglycan interactions. Arteriosclerosis 9:21–32

    Article  PubMed  CAS  Google Scholar 

  33. Dugi KA, Dichek HL, Santamarina-Fojo S (1995) Human hepatic and lipoprotein lipase: the loop covering the catalytic site mediates lipase substrate specificity. J Biol Chem 270:25396–25401

    Article  PubMed  CAS  Google Scholar 

  34. van Tilbeurgh H, Roussel A, Lalouel JM, Cambillau C (1994) Lipoprotein lipase. Molecular model based on the pancreatic lipase x-ray structure: consequences for heparin binding and catalysis. J Biol Chem 269:4626–4633

    PubMed  Google Scholar 

  35. Wang CS, Hartsuck J, McConathy WJ (1992) Structure and functional properties of lipoprotein lipase. Biochim Biophys Acta 1123:1–17

    Article  PubMed  CAS  Google Scholar 

  36. Wong H, Davis RC, Thuren T, Goers JW, Nikazy J, Waite M, Schotz MC (1994) Lipoprotein lipase domain function. J Biol Chem 269:10319–10323

    PubMed  CAS  Google Scholar 

  37. Henderson HE, Ma Y, Liu MS, Clark-Lewis I, Maeder DL, Kastelein JJ, Brunzell JD, Hayden MR (1993) Structure-function relationships of lipoprotein lipase: mutation analysis and mutagenesis of the loop region. J Lipid Res 34:1593–1602

    PubMed  CAS  Google Scholar 

  38. Wong H, Davis RC, Nikazy J, Seebart KE, Schotz MC (1991) Domain exchange: characterization of a chimeric lipase of hepatic lipase and lipoprotein lipase. Proc Natl Acad Sci USA 88:11290–11294

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  39. Hata A, Ridinger DN, Sutherland S, Emi M, Shuhua Z, Myers RL, Ren K, Cheng T, Inoue I, Wilson DE et al (1993) Binding of lipoprotein lipase to heparin. Identification of five critical residues in two distinct segments of the amino-terminal domain. J Biol Chem 268:8447–8457

    PubMed  CAS  Google Scholar 

  40. Ma Y, Henderson HE, Liu MS, Zhang H, Forsythe IJ, Clarke-Lewis I, Hayden MR, Brunzell JD (1994) Mutagenesis in four candidate heparin binding regions (residues 279–282, 291–304, 390–393, and 439–448) and identification of residues affecting heparin binding of human lipoprotein lipase. J Lipid Res 35:2049–2059

    PubMed  CAS  Google Scholar 

  41. Williams SE, Inoue I, Tran H, Fry GL, Pladet MW, Iverius PH, Lalouel JM, Chappell DA, Strickland DK (1994) The carboxyl-terminal domain of lipoprotein lipase binds to the low density lipoprotein receptor-related protein/alpha 2-macroglobulin receptor (LRP) and mediates binding of normal very low density lipoproteins to LRP. J Biol Chem 269:8653–8658

    PubMed  CAS  Google Scholar 

  42. Krapp A, Zhang HF, Ginzinger D, Liu MS, Lindberg A, Olivecrona G, Hayden MR, Beisiegel U (1995) Structural features in lipoprotein lipase necessary for the mediation of lipoprotein uptake into cells. J Lipid Res 36:2362–2373

    PubMed  CAS  Google Scholar 

  43. Lo JY, Smith LC, Chan L (1995) Lipoprotein lipase: role of intramolecular disulfide bonds in enzyme catalysis. Biochem Biophys Res Commun 206:266–271

    Article  PubMed  CAS  Google Scholar 

  44. Keiper T, Schneider JG, Dugi KA (2001) Novel site in lipoprotein lipase (LPL415-438) essential for substrate interaction and dimer stability. J Lipid Res 42:1180–1186

    PubMed  CAS  Google Scholar 

  45. Raisonnier A, Etienne J, Arnault F, Brault D, Noe L, Chuat JC, Galibert F (1995) Comparison of the cDNA and amino acid sequences of lipoprotein lipase in eight species. Comp Biochem Physiol B 111:385–398

    Article  PubMed  CAS  Google Scholar 

  46. Bessesen DH, Richards CL, Etienne J, Goers JW, Eckel RH (1993) Spinal cord of the rat contains more lipoprotein lipase than other brain regions. J Lipid Res 34:229–238

    PubMed  CAS  Google Scholar 

  47. Ben-Zeev O, Doolittle MH, Singh N, Chang CH, Schotz MC (1990) Synthesis and regulation of lipoprotein lipase in the hippocampus. J Lipid Res 31:1307–1313

    PubMed  CAS  Google Scholar 

  48. Vilaro S, Camps L, Reina M, Perez-Clausell J, Llobera M, Olivecrona T (1990) Localization of lipoprotein lipase to discrete areas of the guinea pig brain. Brain Res 506:249–253

    Article  PubMed  CAS  Google Scholar 

  49. Gong H, Dong W, Rostad SW, Marcovina SM, Albers JJ, Brunzell JD, Vuletic S (2013) Lipoprotein lipase (LPL) is associated with neurite pathology and its levels are markedly reduced in the dentate gyrus of Alzheimer’s disease brains. J Histochem Cytochem 61:857–868

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  50. Koch S, Donarski N, Goetze K, Kreckel M, Stuerenburg HJ, Buhmann C, Beisiegel U (2001) Characterization of four lipoprotein classes in human cerebrospinal fluid. J Lipid Res 42:1143–1151

    PubMed  CAS  Google Scholar 

  51. Brecher P, Kuan HT (1979) Lipoprotein lipase and acid lipase activity in rabbit brain microvessels. J Lipid Res 20:464–471

    PubMed  CAS  Google Scholar 

  52. Wang H, Astarita G, Taussig MD, Bharadwaj KG, DiPatrizio NV, Nave KA, Piomelli D, Goldberg IJ, Eckel RH (2011) Deficiency of lipoprotein lipase in neurons modifies the regulation of energy balance and leads to obesity. Cell Metab 13:105–113

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  53. Goti D, Balazs Z, Panzenboeck U, Hrzenjak A, Reicher H, Wagner E, Zechner R, Malle E, Sattler W (2002) Effects of lipoprotein lipase on uptake and transcytosis of low density lipoprotein (LDL) and LDL-associated α-tocopherol in a porcine in vitro blood-brain barrier model. J Biol Chem 277:28537–28544

    Article  PubMed  CAS  Google Scholar 

  54. Xian X, Liu T, Yu J, Wang Y, Miao Y, Zhang J, Yu Y, Ross C, Karasinska JM, Hayden MR, Liu G, Chui D (2009) Presynaptic defects underlying impaired learning and memory function in lipoprotein lipase-deficient mice. J Neurosci 29:4681–4685

    Article  PubMed  CAS  Google Scholar 

  55. Nuñez M, Peinado-Onsurbe J, Vilaró S, Llobera M (1995) Lipoprotein lipase activity in developing rat brain areas. Biol Neonate 68:119–127

    Article  PubMed  Google Scholar 

  56. Blain JF, Paradis E, Gaudreault SB, Champagne D, Richard D, Poirier J (2004) A role for lipoprotein lipase during synaptic remodeling in the adult mouse brain. Neurobiol Dis 15:510–519

    Article  PubMed  CAS  Google Scholar 

  57. Paradis E, Clement S, Julien P, Ven Murthy MR (2003) Lipoprotein lipase affects the survival and differentiation of neural cells exposed to very low density lipoprotein. J Biol Chem 278:9698–9705

    Article  PubMed  CAS  Google Scholar 

  58. Bundgaard M, Abbott NJ (2008) All vertebrates started out with a glial blood–brain barrier 4–500 million years ago. Glia 56:699–708

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We acknowledge the National Institute for Basic Biology for the medaka EST data. This work was partly supported by a grant from the Scientific Technique Research Promotion Program for Agriculture, Forestry, Fisheries and Food industry and by a Grant-in-Aid for Scientific Research from the Japan Society for the Promotion of Science.

Author information

Authors and Affiliations

  1. Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1 Yayoi, 113-8657, Bunkyo, Tokyo, Japan

    Lu Wang, Gen Kaneko, Shin-Ichiro Takahashi, Shugo Watabe & Hideki Ushio

  2. School of Marine Biosciences, Kitasato University, 252-0373, Sagamihara, Kanagawa, Japan

    Shugo Watabe

Authors
  1. Lu Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gen Kaneko
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shin-Ichiro Takahashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shugo Watabe
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hideki Ushio
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gen Kaneko.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PPTX 196 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, L., Kaneko, G., Takahashi, SI. et al. Identification and gene expression profile analysis of a major type of lipoprotein lipase in adult medaka Oryzias latipes . Fish Sci 81, 163–173 (2015). https://doi.org/10.1007/s12562-014-0826-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12562-014-0826-7

Keywords

Search

Navigation