C30F12.4 influences oogenesis, fat metabolism, and lifespan in C. elegans
Received date: 20 Apr 2016
Accepted date: 19 Jul 2016
Published date: 24 Oct 2016
Copyright
Reproduction, fat metabolism, and longevity are intertwined regulatory axes; recent studies in C. elegans have provided evidence that these processes are directly coupled. However, the mechanisms by which they are coupled and the reproductive signals modulating fat metabolism and lifespan are poorly understood. Here, we find that an oogenesis-enriched gene, c30f12.4, is specifically expressed and located in germ cells and early embryos; when the gene is knocked out, oogenesis is disrupted and brood size is decreased. In addition to the reproductive phenotype, we find that the loss of c30f12.4alters fat metabolism, resulting in decreased fat storage and smaller lipid droplets. Meanwhile, c30f12.4mutant worms display a shortened lifespan. Our results highlight an important role for c30f12.4in regulating reproduction, fat homeostasis, and aging in C. elegans, which helps us to better understand the relationship between these processes.
Key words： C30F12.4; oogenesis; fat metabolism; lifespan
Lu Wang , Fei Xu , Guishuan Wang , Xiaorong Wang , Ajuan Liang , Hefeng Huang , Fei Sun . C30F12.4 influences oogenesis, fat metabolism, and lifespan in C. elegans[J]. Protein & Cell, 2016 , 7(10) : 714 -721 . DOI: 10.1007/s13238-016-0308-z
| 1 |
Berman JR, Kenyon C (2006) Germ-cell loss extends C. elegans life span through regulation of DAF-16 by kri-1 and lipophilichormone signaling. Cell 124:1055–1068
|
| 2 |
Chen X, Xu F, Zhu C, Ji J, Zhou X, Feng X, Guang S (2014) Dual sgRNA-directed gene knockout using CRISPR/Cas9 technology in Caenorhabditis elegans. Sci Rep 4:7581
|
| 3 |
Claycomb JM, Batista PJ, Pang KM, Gu W, Vasale JJ, van Wolfswinkel JC, Chaves DA, Shirayama M, Mitani S, Ketting RF
|
| 4 |
Corona G, Mannucci E, Forti G, Maggi M (2009) Hypogonadism, ED, metabolic syndrome and obesity: a pathological link supporting cardiovascular diseases. Int J Androl 32:587–598
|
| 5 |
Dernburg AF, McDonald K, Moulder G, Barstead R, Dresser M, Villeneuve AM (1998) Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 94:387–398
|
| 6 |
Friedland AE, Tzur YB, Esvelt KM, Colaiácovo MP, Church GM, Calarco JA (2013) Heritable genome editing in C. elegansvia a CRISPR-Cas9 system. Nat Methods 10:741–743
|
| 7 |
Frokjaer-Jensen C, Davis MW, Sarov M, Taylor J, Flibotte S, LaBella M, Pozniakovsky A, Moerman DG, Jorgensen EM (2014) Random and targeted transgene insertion in Caenorhabditis elegansusing a modified Mos1 transposon. Nat Methods 11:529–534
|
| 8 |
Gems D, Sutton AJ, Sundermeyer ML, Albert PS, King KV, Edgley ML, Larsen PL, Riddle DL (1998) Two pleiotropic classes of daf-2 mutation affect larval arrest, adult behavior, reproduction and longevity in Caenorhabditis elegans. Genetics 150:129–155
|
| 9 |
Goudeau J, Bellemin S, Toselli-Mollereau E, Shamalnasab M, Chen Y, Aguilaniu H (2011) Fatty acid desaturation links germ cell loss to longevity through NHR-80/HNF4 in C. elegans. PLoS Biol 9: e1000599
|
| 10 |
Green RA, Kao HL, Audhya A, Arur S, Mayers JR, Fridolfsson HN, Schulman M, Schloissnig S, Niessen S, Laband K
|
| 11 |
Hamilton B, Dong Y, Shindo M, Liu W, Odell I, Ruvkun G, Lee SS (2005) A systematic RNAi screen for longevity genes in C. elegans. Genes Dev 19:1544–1555
|
| 12 |
Hansen M, Flatt T, Aguilaniu H (2013) Reproduction, fat metabolism, and life span: what is the connection? Cell Metab 17:10–19
|
| 13 |
Herndon LA, Schmeissner PJ, Dudaronek JM, Brown PA, Listner KM, Sakano Y, Paupard MC, Hall DH, Driscoll M (2002) Stochastic and genetic factors influence tissue-specific decline in ageing C. elegans. Nature 419:808–814
|
| 14 |
Hsin H, Kenyon C (1999) Signals from the reproductive system regulate the lifespan of C. elegans. Nature 399:362–366
|
| 15 |
Jia K, Albert PS, Riddle DL (2002) DAF-9, a cytochrome P450 regulating C. eleganslarval development and adult longevity. Development 129:221–231
|
| 16 |
Judd ET, Wessels FJ, Drewry MD, Grove M, Wright K, Hahn DA, Hatle JD (2011) Ovariectomy in grasshoppers increases somatic storage, but proportional allocation of ingested nutrients to somatic tissues is unchanged. Aging Cell 10:972–979
|
| 17 |
Kalis AK, Kroetz MB, Larson KM, Zarkower D (2010) Functional genomic identification of genes required for male gonadal differentiation in Caenorhabditis elegans. Genetics 185:523–535
|
| 18 |
Kenyon CJ (2010) The genetics of ageing. Nature 464:504–512
|
| 19 |
Kenyon C, Chang J, Gensch E, Rudner A, Tabtiang R (1993) A C. elegansmutant that lives twice as long as wild type. Nature 366:461–464
|
| 20 |
Khanna A, Johnson DL, Curran SP (2014) Physiological roles for mafr-1 in reproduction and lipid homeostasis. Cell Rep 9:2180–2191
|
| 21 |
Klemm RW, Norton JP, Cole RA, Li CS, Park SH, Crane MM, Li L, Jin D, Boye-Doe A, Liu TY
|
| 22 |
Lin K, Dorman JB, Rodan A, Kenyon C (1997) daf-16: An HNF-3/forkhead family member that can function to double the lifespan of Caenorhabditis elegans. Science 278:1319–1322
|
| 23 |
McCormick M, Chen K, Ramaswamy P, Kenyon C (2012) New genes that extend Caenorhabditis elegans’ lifespan in response to reproductive signals. Aging Cell 11:192–202
|
| 24 |
Ni Z, Ebata A, Alipanahiramandi E, Lee SS (2012) Two SET domain containing genes link epigenetic changes and aging in Caenorhabditis elegans. Aging Cell 11:315–325
|
| 25 |
Pang S, Lynn DA, Lo JY, Paek J, Curran SP (2014) SKN-1 and Nrf2 couples proline catabolism with lipid metabolism during nutrient deprivation. Nat Commun 5:5048
|
| 26 |
Pino EC, Webster CM, Carr CE, Soukas AA (2013) Biochemical and high throughput microscopic assessment of fat mass in Caenorhabditis elegans. J Vis Exp 73(2013):e50180–e50180
|
| 27 |
Spencer WC, Zeller G,Watson JD, Henz SR,Watkins KL, McWhirter RD, Petersen S, Sreedharan VT, Widmer C, Jo J
|
| 28 |
Wang MC, O’Rourke EJ, Ruvkun G (2008) Fat metabolism links germline stem cells and longevity in C. elegans. Science 322:957–960
|
| 29 |
Wang L, Liu W, Zhao W, Song G, Wang G, Wang X, Sun F (2014) Phosphorylation of CDK2 on threonine 160 influences silencing of sex chromosome during male meiosis. Biol Reprod 90:138
|
| 30 |
Wiedenheft B, Sternberg SH, Doudna JA (2012) RNA-guided genetic silencing systems in bacteria and archaea. Nature 482:331–338
|
| 31 |
Wollam J, Magner DB, Magomedova L, Rass E, Shen Y, Rottiers V, Habermann B, Cummins CL, Antebi A (2012) A novel 3-hydroxysteroid dehydrogenase that regulates reproductive development and longevity. PLoS Biol 10:e1001305
|
| 32 |
Xu N, Zhang SO, Cole RA, McKinney SA, Guo F, Haas JT, Bobba S, Farese RV Jr, Mak HY (2012) The FATP1-DGAT2 complex facilitates lipid droplet expansion at the ER-lipid droplet interface. J Cell Biol 198:895–911
|
/
| 〈 |
|
〉 |