Depletion of phosphatidylcholine in yeast induces shortening and increased saturation of the lipid acyl chains: Evidence for regulation of intrinsic membrane curvature in a eukaryote

被引:89
作者
Boumann, HA
Gubbens, J
Koorengevel, MC
Oh, CS
Martin, CE
Heck, AJR
Patton-Vogt, J
Henry, SA
de Kruijff, B
de Kroon, AIPM [1 ]
机构
[1] Univ Utrecht, Bijvoet Inst, Dept Biochem Membranes, NL-3584 CH Utrecht, Netherlands
[2] Univ Utrecht, Inst Biomembranes, NL-3584 CH Utrecht, Netherlands
[3] Rutgers State Univ, Dept Cell Biol & Neurosci, Piscataway, NJ 08854 USA
[4] Bijvoet Ctr Biomol Res, Dept Biomol Mass Specttrometry, NL-3584 CA Utrecht, Netherlands
[5] Inst Pharmaceut Sci, NL-3584 CA Utrecht, Netherlands
[6] Duquesne Univ, Dept Biol Sci, Pittsburgh, PA 15282 USA
[7] Cornell Univ, Dept Mol Biol & Genet, Ithaca, NY 14853 USA
关键词
D O I
10.1091/mbc.E05-04-0344
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
To study the consequences of depleting the major membrane phospholipid phosphatidylcholine (PC), exponentially growing cells of a yeast cho2opi3 double deletion mutant were transferred from medium containing choline to choline-free medium. Cell growth did not cease until the PC level had dropped below 2% of total phospholipids after four to five generations. Increasing contents of phosphatidylethanolamine (PE) and phosphatidylinositol made up for the loss of PC. During PC depletion, the remaining PC was subject to acyl chain remodeling with monounsaturated species replacing diunsaturated species, as shown by mass spectrometry. The remodeling of PC did not require turnover by the SPO14-encoded phospholipase D. The changes in the PC species profile were found to reflect an overall shift in the cellular acyl chain composition that exhibited a 40% increase in the ratio of C16 over C18 acyl chains, and a 10% increase in the degree of saturation. The shift was stronger in the phospholipid than in the neutral lipid fraction and strongest in the species profile of PE. The shortening and increased saturation of the PE acyl chains were shown to decrease the nonbilayer propensity of PE. The results point to a regulatory mechanism in yeast that maintains intrinsic membrane curvature in an optimal range.
引用
收藏
页码:1006 / 1017
页数:12
相关论文
共 68 条
  • [1] ATKINSON K, 1980, J BIOL CHEM, V255, P6653
  • [2] Modulation of CTP:phosphocholine cytidylyltransferase by membrane curvature elastic stress
    Attard, GS
    Templer, RH
    Smith, WS
    Hunt, AN
    Jackowski, S
    [J]. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2000, 97 (16) : 9032 - 9036
  • [3] Roles of phosphatidylethanolamine and of its several biosynthetic pathways in Saccharomyces cerevisiae
    Birner, R
    Bürgermeister, M
    Schneiter, R
    Daum, G
    [J]. MOLECULAR BIOLOGY OF THE CELL, 2001, 12 (04) : 997 - 1007
  • [4] BLIGH EG, 1959, CAN J BIOCHEM PHYS, V37, P911
  • [5] The yeast phospholipid N-methyltransferases catalyzing the synthesis of phosphatidylcholine preferentially convert Di-C16:1 Substrates both in vivo and in vitro
    Boumann, HA
    Chin, PTK
    Heck, AJR
    de Kruijff, B
    de Kroon, AIPM
    [J]. JOURNAL OF BIOLOGICAL CHEMISTRY, 2004, 279 (39) : 40314 - 40319
  • [6] The two biosynthetic routes leading to phosphatidylcholine in yeast produce different sets of molecular species. Evidence for lipid remodeling
    Boumann, HA
    Damen, MJA
    Versluis, C
    Heck, AJR
    de Kruijff, B
    de Kroon, AIPM
    [J]. BIOCHEMISTRY, 2003, 42 (10) : 3054 - 3059
  • [7] Nonbilayer lipids affect peripheral and integral membrane proteins via changes in the lateral pressure profile
    Brink-van der Laan, EV
    Killian, JA
    de Kruijff, B
    [J]. BIOCHIMICA ET BIOPHYSICA ACTA-BIOMEMBRANES, 2004, 1666 (1-2): : 275 - 288
  • [8] Phospholipid biosynthesis in the yeast Saccharomyces cerevisiae and interrelationship with other metabolic processes
    Carman, GM
    Henry, SA
    [J]. PROGRESS IN LIPID RESEARCH, 1999, 38 (5-6) : 361 - 399
  • [9] The membrane proteins, Spt23p and Mga2p, play distinct roles in the activation of Saccharomyces cerevisiae OLE1 gene expression -: Fatty acid-mediated regulation of Mga2p activity is independent of its proteolytic processing into a soluble transcription activator
    Chellappa, R
    Kandasamy, P
    Oh, CS
    Jiang, Y
    Vemula, M
    Martin, CE
    [J]. JOURNAL OF BIOLOGICAL CHEMISTRY, 2001, 276 (47) : 43548 - 43556
  • [10] Phosphatidylcholine and N-methylated phospholipids are nonessential in Saccharomyces cerevisiae
    Choi, JY
    Martin, WE
    Murphy, RC
    Voelker, DR
    [J]. JOURNAL OF BIOLOGICAL CHEMISTRY, 2004, 279 (40) : 42321 - 42330