Mitochondrial iron supply is required for the developmental pulse of ecdysone biosynthesis that initiates metamorphosis in Drosophila melanogaster

详细信息    查看全文

• 作者：Jose V. Llorens ; Christoph Metzendorf…
• 关键词：Development ; Insect ; Mitochondria ; Mitoferrin ; Cholesterol
• 刊名：Journal of Biological Inorganic Chemistry
• 出版年：2015
• 出版时间：December 2015
• 年：2015
• 卷：20
• 期：8
• 页码：1229-1238
• 全文大小：740 KB
• 参考文献：1.Sheftel AD, Mason AB, Ponka P (2012) Biochim Biophys Acta 1820:161-87PubMedCentral CrossRef PubMed
  2.Crichton RR (2001) Inorganic biochemistry of iron metabolism: from molecular mechanisms to clinical consequences, 2nd edn. Wiley, ChichesterCrossRef
  3.Lane DJ, Merlot AM, Huang ML, Bae DH, Jansson PJ, Sahni S, Kalinowski DS, Richardson DR (2015) Biochim Biophys Acta 1853:1130-144CrossRef PubMed
  4.Lill R, Dutkiewicz R, Freibert SA, Heidenreich T, Mascarenhas J, Netz DJ, Paul VD, Pierik AJ, Richter N, Stümpfig M, Srinivasan V, Stehling O, Mühlenhoff U (2015) Eur J Cell Biol 94:280-91CrossRef PubMed
  5.Brazzolotto X, Pierrel F, Pelosi L (2014) Biochem J 460:79-9CrossRef PubMed
  6.Foury F, Roganti T (2002) J Biol Chem 277:24475-4483CrossRef PubMed
  7.Li L, Kaplan J (2004) J Biol Chem 279:33653-3661CrossRef PubMed
  8.Muhlenhoff U, Stadler JA, Richhardt N, Seubert A, Eickhorst T, Schweyen RJ, Lill R, Wiesenberger G (2003) J Biol Chem 278:40612-0620CrossRef PubMed
  9.Zhang Y, Lyver ER, Knight SA, Lesuisse E, Dancis A (2005) J Biol Chem 280:19794-9807CrossRef PubMed
  10.Shaw GC, Cope JJ, Li L, Corson K, Hersey C, Ackermann GE, Gwynn B, Lambert AJ, Wingert RA, Traver D, Trede NS, Barut BA, Zhou Y, Minet E, Donovan A, Brownlie A, Balzan R, Weiss MJ, Peters LL, Kaplan J, Zon LI, Paw BH (2006) Nature 440:96-00CrossRef PubMed
  11.Troadec MB, Warner D, Wallace J, Thomas K, Spangrude GJ, Phillips J, Khalimonchuk O, Paw BH, Ward DM, Kaplan J (2011) Blood 117:5494-502PubMedCentral CrossRef PubMed
  12.Ren Y, Yang S, Tan G, Ye W, Liu D, Qian X, Ding Z, Zhong Y, Zhang J, Jiang D, Zhao Y, Lu J (2012) PLoS ONE 7:e29666PubMedCentral CrossRef PubMed
  13.Paradkar PN, Zumbrennen KB, Paw BH, Ward DM, Kaplan J (2009) Mol Cell Biol 29:1007-016PubMedCentral CrossRef PubMed
  14.Kunji ER (2004) FEBS Lett 564:239-44CrossRef PubMed
  15.Froschauer EM, Schweyen RJ, Wiesenberger G (2009) Biochim Biophys Acta 1788:1044-050CrossRef PubMed
  16.Metzendorf C, Wu W, Lind MI (2009) Biochem J 421:463-71CrossRef PubMed
  17.Metzendorf C, Lind MI (2010) BMC Dev Biol 10:68PubMedCentral CrossRef PubMed
  18.Navarro JA, Botella JA, Metzendorf C, Lind MI, Schneuwly S (2015) Free Radic Biol Med 85:71-2CrossRef PubMed
  19.Massie HR, Aiello VR, Williams TR (1985) Mech Ageing Dev 29:215-20CrossRef PubMed
  20.Palandri A, L’Hote D, Cohen-Tannoudji J, Tricoire H, Monnier V (2015) Hum Mol Genet 24:2615-626CrossRef PubMed
  21.Anderson PR, Kirby K, Hilliker AJ, Phillips JP (2005) Hum Mol Genet 14:3397-405CrossRef PubMed
  22.Llorens JV, Navarro JA, Martínez-Sebastián MJ, Baylies MK, Schneuwly S, Botella JA, Moltó MD (2007) FASEB J 21:333-44CrossRef PubMed
  23.Uhrigshardt H, Rouault TA, Missirlis F (2013) J Biol Inorg Chem 18:441-49PubMedCentral CrossRef PubMed
  24.Sekeris CE, Karlson P (1964) Arch Biochem Biophys 105:483-87CrossRef PubMed
  25.Ashburner M (1975) Sov J Dev Biol 5:97-07PubMed
  26.Thummel CS (1995) Cell 83:871-77CrossRef PubMed
  27.Ono H (2014) Dev Biol 391:32-2CrossRef PubMed
  28.Mirth CK, Tang HY, Makohon-Moore SC, Salhadar S, Gokhale RH, Warner RD, Koyama T, Riddiford LM, Shingleton AW (2014) Proc Natl Acad Sci USA 111:7018-023PubMedCentral CrossRef PubMed
  29.Sarraf-Zadeh L, Christen S, Sauer U, Cognigni P, Miguel-Aliaga I, Stocker H, Kohler K, Hafen E (2013) Dev Biol 381:97-06CrossRef PubMed
  30.Gundner AL, Hahn I, Sendscheid O, Aberle H, Hoch M (2014) PLoS ONE 9:e97332PubMedCentral CrossRef PubMed
  31.Koyama T, Rodrigues MA, Athanasiadis A, Shingleton AW, Mirth CK (2014) Elife 3:e03091PubMedCentral CrossRef
  32.Jaszczak JS, Wolpe JB, Dao AQ, Halme A (2015) Genetics 200:1219-228CrossRef PubMed
  33.Ohhara Y, Shimada-Niwa Y, Niwa R, Kayashima Y, Hayashi Y, Akagi K, Ueda H, Yamakawa-Kobayashi K, Kobayashi S (2015) Proc Natl Acad Sci USA 112:1452-457PubMedCentral CrossRef PubMed
  34.Moeller ME, Danielsen ET, Herder R, O’Connor MB, Rewitz KF (2013) Development 140:4730-739PubMedCentral CrossRef PubMed
  35.Parvy JP, Wang P, Garrido D, Maria A, Blais C, Poidevin M, Montagne J (2014) Development 141:3955-965CrossRef PubMed
  36.Warren JT, Petryk A, Marques G, Jarcho M, Parvy JP, Dauphin-Villemant C, O’Connor MB, Gilbert LI (2002) Proc Natl Acad Sci USA 99:11043-1048PubMedCentral CrossRef PubMed
  37.Rewitz KF, Rybczynski R, Warren JT, Gilbert LI (2006) Biochem Soc Trans 34:1256-260CrossRef PubMed
  38.Danielsen ET, Moeller ME, Dorry E, Komura-Kawa T, Fujimoto Y, Troelsen JT, Herder R, O’Connor MB, Niwa R, Rewitz KF (2014) PLoS Genet 10:e1004343PubMedCentral CrossRef PubMed
  39.Chung H, Sztal T, Pasricha S, Sridhar M, Batterham P, Daborn PJ (2009) Proc Natl Acad Sci USA 106:5731-736PubMedCentral CrossRef PubMed
  40.Yoshiyama T, Namiki T, Mita K, Kataoka H, Niwa R (2006) Development 133:2565-574CrossRef PubMed
  41.Lang M, Murat S, Clark AG, Couppil G, Blais C, Matzkin LM, Guittard E, Yoshiyama-Yanagawa T, Kata
• 作者单位：Jose V. Llorens (1)
  Christoph Metzendorf (2)
  Fanis Missirlis (3)
  Maria I. Lind (1)
  
  1. Department of Comparative Physiology, Uppsala University, Norbyv?gen 18A, Uppsala, Sweden
  2. Heidelberg University Biochemistry Center (BZH), University of Heidelberg, Im Neuenheimer Feld 328, Heidelberg, Germany
  3. Departamento de Fisiología, Biofísica y Neurociencias, Centro de Investigación y de Estudios Avanzados, Av. IPN 2508, Mexico City, Mexico
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Biochemistry
  Microbiology
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1432-1327

文摘

Synthesis of ecdysone, the key hormone that signals the termination of larval growth and the initiation of metamorphosis in insects, is carried out in the prothoracic gland by an array of iron-containing cytochrome P450s, encoded by the halloween genes. Interference, either with iron-sulfur cluster biogenesis in the prothoracic gland or with the ferredoxins that supply electrons for steroidogenesis, causes a block in ecdysone synthesis and developmental arrest in the third instar larval stage. Here we show that mutants in Drosophila mitoferrin (dmfrn), the gene encoding a mitochondrial carrier protein implicated in mitochondrial iron import, fail to grow and initiate metamorphosis under dietary iron depletion or when ferritin function is partially compromised. In mutant dmfrn larvae reared under iron replete conditions, the expression of halloween genes is increased and 20-hydroxyecdysone (20E), the active form of ecdysone, is synthesized. In contrast, addition of an iron chelator to the diet of mutant dmfrn larvae disrupts 20E synthesis. Dietary addition of 20E has little effect on the growth defects, but enables approximately one-third of the iron-deprived dmfrn larvae to successfully turn into pupae and, in a smaller percentage, into adults. This partial rescue is not observed with dietary supply of ecdysone’s precursor 7-dehydrocholesterol, a precursor in the ecdysone biosynthetic pathway. The findings reported here support the notion that a physiological supply of mitochondrial iron for the synthesis of iron-sulfur clusters and heme is required in the prothoracic glands of insect larvae for steroidogenesis. Furthermore, mitochondrial iron is also essential for normal larval growth. Keywords Development Insect Mitochondria Mitoferrin Cholesterol