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Apicomplexan Protozoonlarda Apicoplast

Year 2017, Volume: 14 Issue: 1, 49 - 59, 15.04.2017

Abstract

Apicomplexa subphylumunda bulunan
protistan türleri fotosentetik olmayan apicoplast adı verilen ikincil bir
plastide sahiptirler. Apicoplast;
Plasmodium,
Eimeria, Toxoplasma, Sarcocystis
, Theileria
ve
Babesia gibi bazı apicomplexan
protozoonlarda bulunan buna karşılık
Cryptosporidium
spp ve
Gregarina niphandrodes’de
bulunmayan bir plastiddir. Apicoplastın sekonder endosimbiyoz ile bir algden (kırmızı
ya da yeşil alg) evrimleştiğine inanılmaktadır. Apicoplast, endomembran
sisteminin en dış bölümü içinde dört membran tarafından çevrelenmiştir. Apicomplexan
parazitlerinin büyümesi ve replikasyonu için gerekli son derece özelleşmiş bir
organel olan apicoplastın bakterilerde varolan yağ asidi sentezi, hem pathwayi
ve isoprenoid biyosentezine sahip olduğu bilinmektedir. Bu organelin
yıkımlanması bu parazitlerde ölüme yol açmaktadır. Bu durum, ilaç endüstrisinin
protozoonlara karşı ilaç geliştirme çalışmalarında odak noktasını
oluşturmuştur. Bu yüzden ilaç endüstrisi araştırmalarını bu organele ait gen
bölgeleri üzerine yoğunlaştırmıştır. Bununla birlikte apicoplastın işlevleri
hakkındaki bilgiler henüz yeterli olmayıp bu konuda çeşitli hipotezler
mevcuttur. Bu derlemede apicoplasta dikkat çekilmesi ve bazı fonksiyonları
hakkında üretilen bilgilerin paylaşılması amaçlanmıştır.

References

  • Abrahamsen MS, Templeton TJ, Enomoto S, Abrahante JE, Zhu G, Lancto CA, DengM, Liu C,Widmer G, Tzipori S, Buck GA, Xu P, Bankier AT, Dear PH, Konfortov BA, Spriggs HF, Iyer L, Anantharaman V, Aravind L, Kapur V. Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science 2004; 304(5669): 441-5.
  • 2. Adl SM, Leander BS, Simpson AG, Archibald JM, Anderson OR, Bass D, Bowser SS, Brugerolle G, Farmer MA, Karpov S, Kolisko M, Lane CE, Lodge DJ, Mann DG, Meisterfeld R, Mendoza L, Moestrup O, Mozley-Standridge SE, Smirnov AV, Spiegel F. Diversity, nomenclature, and taxonomy of protists. Syst Biol 2007; 56(4): 684-9.
  • 3. Adl SM, Simpson AG, Farmer MA, Andersen RA, Anderson OR, Barta JR, Bowser SS, Brugerolle G, Fensome RA, Fredericq S, James TY, Karpov S, Kugrens P, Krug J, Lane CE, Lewis LA, Lodge J, Lynn DH, Mann DG, McCourt RM, Mendoza L, Moestrup O, Mozley-Standridge SE, Nerad TA, Shearer CA, Smirnov AV, Spiegel FW, Taylor MF .The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol 2005; 52(5): 399-451.
  • 4. Apt KE, Clendennen SK, Powers DA, Grossman AR. The gene family encoding the fucoxanthin chlorophyll proteins from the brown alga Macrocystis pyrifera. Mol Gen Genet 1995; 246(4): 455-64.
  • 5. Blatter E, Ross W, Tang H, Gourse R, Ebright R. Domain organization of RNA polymerase a subunit: C-terminal 85 amino acids constitute a domain capable of dimerization and DNA binding. Cell 1994; 78(5): 889-96.
  • 6. Bolte K, Bullmann L, Hempel F, Bozarth A, Zauner S, Maier UG. Protein targeting into secondary plastids. J Eukaryot Microbiol 2009; 56(1): 9-15.
  • 7. Brayton KA, Lau AO, Herndon DR, Hannick L, Kappmeyer LS, Berens SJ, Bidwell SL, Brown WC, Crabtree J, Fadrosh D, Feldblum T, Forberger HA, Haas BJ, Howell JM, Khouri H, Koo H, Mann DJ, Norimine J, Paulsen IT, Radune D, Ren Q, Smith RK Jr, Suarez CE, White O, Wortman JR, Knowles DP Jr, McElwain TF, Nene VM. Genome sequence of Babesia bovis and comparative analysis of apicomplexan hemoprotozoa. PLoS Pathog 2007; 3(10): 1401-13.
  • 8. Cai X, Fuller AL, McDougald LR, Zhu G. Apicoplast genome of the coccidian Eimeria tenella Gene 2003; 4(321): 39-46.
  • 9. Clastre M, Goubard A, Prel A, Mincheva Z, Viaud-Massuart MC, Bout D, Rideau M, Velge-Roussel F, Laurent F. The methylerythritol phosphate pathway for isoprenoid biosynthesis in coccidia: presence and sensitivity to fosmidomycin. Exp Parasitol 2007; 116(4): 375-84.
  • 10. Denny P, Preiser P, Williamson D, Wilson I. Evidence for a single origin of the 35 kb plastid DNA in apicomplexans. Protist 1998; 149: 51-59.
  • Hopkins J, Fowler R, Krishna S, Wilson I, Mitchell G, Bannister L. The plastid in Plasmodium falciparum asexual blood stages: a three-dimensional ultrastructural analysis. Protist 1999; 150(3): 283-95.
  • 22. Igarashi K, Ishihama A. Bipartite functional map of the E. coli RNA polymerase a subunit: involvement of the C-terminal region in transcription activation by cAMP-CRP. Cell 1991; 65(6): 1015-22.
  • 23. Janouskovec J, Horak A, Obornik M, Lukes J, Keeling PJ A common red algal origin of the apicomplexan, dinoflagellate, and heterokont plastids. Proc Natl Acad Sci USA 2010; 107: 10949-54.
  • 24. Jomaa H, Wiesner J, Sanderbrand S, Altincicek B, Weidemeyer C, Hintz M, Turbachova I, Eberl M, Zeidler J, Lichtenthaler HK, Soldati D, Beck E. Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs. Science 1999; 285(5433): 1573-6.
  • 25. Kalanon M, Tonkin CJ, McFadden GI. Characterization of two putative protein translocation components in the apicoplast of Plasmodium falciparum. Eukaryot Cell 2009; 8(8): 1146-54.
  • 26. Kilejian A. Circular mitochondrial DNA from the avian malarial parasite Plasmodium lophurae. Biochim Biophys Acta 1975; 390(3): 276-84.
  • 27. Kobayashi T, Sato S, Takamiya S, Komaki-Yasuda K, Yano K,Hirata A, Onitsuka I, Hata M, Mi-ichi F, Tanaka T, Hase T, Miyajima A, Kawazu S, Watanabe Y, Kita K. Mitochondriaand apicoplast of Plasmodium falciparum: Behaviouron subcellular fractionation and the implication. Mitochondrion 2007; 7(1-2): 125-32.
  • 28. Köhler S, Delwiche CF, Denny PW, Tilney LG, Webster P, Wilson RJM, Palmer JD, Roos DS. A plastid of probable green algal origin in apicomplexan parasites. Science 1997; 275 (5305): 1485-89.
  • 29. Lang M, Apt KE, Kroth PG. Protein transport into ‘‘complex’’ diatom plastids utilizes two different targeting signals. J Biol Chem 1998; 273(47): 30973-8.
  • 30. Lang-Unnasch N, Reith ME, Munholland J, Barta JR. Plastids are widespread and ancient in parasites of the phylum Apicomplexa. Int J Parasitol 1998; 28(11): 1743-54.
  • Pain A, Renauld H, Berriman M, Murphy L, Yeats CA, Weir W, Kerhornou A, Aslett M, Bishop R, Bouchier C, Cochet M, Coulson RM, Cronin A, de Villiers EP, Fraser A, Fosker N, Gardner M,Goble A, Griffiths-Jones S, Harris DE, Katzer F, Larke N, Lord A, Maser P, McKellar S, Mooney P, Morton F, Nene V, O’Neil S, Price C, Quail MA, Rabbinowitsch E, Rawlings ND, Rutter S, Saunders D, Seeger K, Shah T, Squares R, Squares S, Tivey A, Walker AR, Woodward J, Dobbelaere DA, Langsley G, Rajandream MA, McKeever D, Shiels B, Tait A, Barrell B, Hall N. Genome of the host-cell transforming parasite Theileria annulata compared with T. parva. Science 2005; 309(5731): 131-3.
  • 42. Perkins FO, Barta JR, Clopton RE, Peirce MA, Upton SJ. Phylum Apicomplexa. Lee JJ, Leedale GF, Bradbury P. eds. In: An Illustrated Guİde to the Protozoa. Kansas: Society of Protozoologists, 2000; pp. 190.
  • 43. Ralph SA, Van Dooren GG, Waller RF, Crawford MJ, Fraunholz MJ, Foth BJ, Tonkin CJ, Roos DS, McFadden GI. Tropical infectious diseases: metabolic maps and functions of the Plasmodium falciparum apicoplast. Nat Rev Microbiol 2004; 2(3): 203-16.
  • 44. Ram EV, Naik R, Ganguli M, Habib S. DNA organization by the apicoplast-targeted bacterial histone-like protein of Plasmodium falciparum. Nucleic Acids Res 2008; 36(15): 5061-73.
  • 45. Reiff SB, Vaishnava S, Striepena B. The HU Protein is important for apicoplast genome maintenance and ınheritance in Toxoplasma gondii. Eukaryotic Cell 2012; 11( 7): 905-15.
  • 46. Richter S, Lamppa GK. A chloroplast processing enzyme functions as the general stromal processing peptidase. Proc Natl Acad Sci USA 1998; 95(13): 7463-8.
  • 47. Roos DS, Crawford MJ, Donald RG, Fraunholz M, Harb OS, He CY, Kissinger JC, Shaw MK, Striepen B. Mining the plasmodium genome database to define organellar function: hat does the apicoplast do? Philos Trans R Soc Lond B Biol Sci 2002; 357(1417): 35-46.
  • 48. Sasaki N, Hirai M, Maeda K, Yui R, Itoh K, Namiki S, Morita T, Hata M, Murakami-Murofushi K, Matsuoka H, Kita K, Sato S. The plasmodium HU homolog, which binds the plastid DNA sequence-independent manner, is essential for the parasite’s survival. FEBS Lett 2009; 583(9): 1446-50.
  • 49. Sato N, Terasawa K, Miyajima K, Kabeya Y. Organization, developmental dynamics, and evolution of plastid nucleoids. Int Rev Cytol 2003 232:217-62.
  • 50. Sato S, Clough B, Coates L, Wilson RJM. Enzymes for heme biosynthesis are found in both the mitochondrion and plastid of the malaria parasite Plasmodium falciparum. Protist 2004; 155(1): 117-25.
  • Tomova C, Geerts WJ, Muller-Reichert T, Entzeroth R, Humbel BM. New comprehension of the apicoplast of Sarcocystis by transmission electron tomography. Biol Cell 2006; 98(9) :535-45.
  • 62. Tomova C, Humbel BM, Geerts WJ, Entzeroth R, Holthuis JC, Verkleij AJ. Membrane contact sites between apicoplast and ER in Toxoplasma gondii revealed by electron tomography. Traffic 2009; 10(10): 1471-80.
  • 63. Tonkin CJ, Struck NS, Mullin KA, Stimmler LM, McFadden GI. Evidence for Golgi-independent transport from the early secretory pathway to the plastid in malaria parasites. Mol Microbiol 2006; 61(3): 614-30.
  • 64. Toso MA, Omoto CK. Gregarina niphandrodes may lack both a plastid genome and organelle. J Eukaryot Microbiol 2007; 54(1): 66-72.
  • 65. Waller RF, Keeling PJ. Alveolate and chlorophycean mitochondrial cox2 genes split twice independently. Gene 2006; 383: 33-7.
  • 66. Waller RF, Keeling PJ, Donald RG, Striepen B, Handman E, Lang-Unnasch N, Cowman AF, Besra GS, Roos DS, McFadden GI. Nuclear-encoded proteins target to the plastid in Toxoplasma gondii and Plasmodium falciparum. Proc Natl Acad Sci USA 1998; 95(21): 12352–7.
  • 67. Waller RF, Keeling PJ, van Dooren GG, McFadden GI. Comment on “A green algal apicoplast ancestor”. Science 2003; 301(5629): 49.
  • 68. Waller RF, Reed MB, Cowman AF, McFadden GI. Protein trafficking to the plastid of Plasmodium falciparum is via the secretory pathway. EMBO J 2000; 19(8): 1794-1802.
  • 69. Waller RF, Ralph SA, Reed MB, Su V, Douglas JD, Minnikin DE, Cowman AF, Besra GS, McFadden GI. A type II pathway for fatty acid biosynthesis presents drug targets in Plasmodium falciparum. Antimicrob Agents Chemother 2003b; 47(1): 297-301.
  • 70. Williamson DH, Denny PW, Moore PW, Sato S, McCready S, Wilson RJM. The in vivo conformation of the plastid DNA of Toxoplasma gondii: İmplications for replication. J Mol Biol 2001; 306(2):159-68.

Apicoplast in Apicomplexan Protozoon

Year 2017, Volume: 14 Issue: 1, 49 - 59, 15.04.2017

Abstract

Protistan species belonging to the subphylum
apicomplexa have a non-photosynthetic secondary plastid structure also called apicoplast. 
This organel is found in most parasitic genera
of apicomplexan protozoans like
Plasmodium,
Eimeria, Toxoplasma, Sarcocystis
, Theileria
and
Babesia spp., but not in the
ohers such as
Cryptosporidium spp.
and
Gregarina niphandrodes. It is
believed that the apicoplast is originated from an alga (red or green alga) through
secondary endosymbiosis. The apicoplast is surrounded by fourfold membrane
within the outer most part of the endomembrane system. The apicoplast which is
a highly specialized organelle that mediates required functions in the growth
and replication of apicomplexan parasites contains an ensemble of bacteria-like
pathways to replicate and express its genome plus an anabolic capacity
generating fatty acids, heme and isoprenoid precursors. Destroying this organel
usually results in parasite death, thus making apicoplast metabolism an
attractive target for drugs. However, the data about the functions of the
apicoplast are limited and there are some hyppotehesis about this subject. In
this review, it was aimed to point out the apicoplast and to s hare the data
about some functions of this organel.

References

  • Abrahamsen MS, Templeton TJ, Enomoto S, Abrahante JE, Zhu G, Lancto CA, DengM, Liu C,Widmer G, Tzipori S, Buck GA, Xu P, Bankier AT, Dear PH, Konfortov BA, Spriggs HF, Iyer L, Anantharaman V, Aravind L, Kapur V. Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science 2004; 304(5669): 441-5.
  • 2. Adl SM, Leander BS, Simpson AG, Archibald JM, Anderson OR, Bass D, Bowser SS, Brugerolle G, Farmer MA, Karpov S, Kolisko M, Lane CE, Lodge DJ, Mann DG, Meisterfeld R, Mendoza L, Moestrup O, Mozley-Standridge SE, Smirnov AV, Spiegel F. Diversity, nomenclature, and taxonomy of protists. Syst Biol 2007; 56(4): 684-9.
  • 3. Adl SM, Simpson AG, Farmer MA, Andersen RA, Anderson OR, Barta JR, Bowser SS, Brugerolle G, Fensome RA, Fredericq S, James TY, Karpov S, Kugrens P, Krug J, Lane CE, Lewis LA, Lodge J, Lynn DH, Mann DG, McCourt RM, Mendoza L, Moestrup O, Mozley-Standridge SE, Nerad TA, Shearer CA, Smirnov AV, Spiegel FW, Taylor MF .The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol 2005; 52(5): 399-451.
  • 4. Apt KE, Clendennen SK, Powers DA, Grossman AR. The gene family encoding the fucoxanthin chlorophyll proteins from the brown alga Macrocystis pyrifera. Mol Gen Genet 1995; 246(4): 455-64.
  • 5. Blatter E, Ross W, Tang H, Gourse R, Ebright R. Domain organization of RNA polymerase a subunit: C-terminal 85 amino acids constitute a domain capable of dimerization and DNA binding. Cell 1994; 78(5): 889-96.
  • 6. Bolte K, Bullmann L, Hempel F, Bozarth A, Zauner S, Maier UG. Protein targeting into secondary plastids. J Eukaryot Microbiol 2009; 56(1): 9-15.
  • 7. Brayton KA, Lau AO, Herndon DR, Hannick L, Kappmeyer LS, Berens SJ, Bidwell SL, Brown WC, Crabtree J, Fadrosh D, Feldblum T, Forberger HA, Haas BJ, Howell JM, Khouri H, Koo H, Mann DJ, Norimine J, Paulsen IT, Radune D, Ren Q, Smith RK Jr, Suarez CE, White O, Wortman JR, Knowles DP Jr, McElwain TF, Nene VM. Genome sequence of Babesia bovis and comparative analysis of apicomplexan hemoprotozoa. PLoS Pathog 2007; 3(10): 1401-13.
  • 8. Cai X, Fuller AL, McDougald LR, Zhu G. Apicoplast genome of the coccidian Eimeria tenella Gene 2003; 4(321): 39-46.
  • 9. Clastre M, Goubard A, Prel A, Mincheva Z, Viaud-Massuart MC, Bout D, Rideau M, Velge-Roussel F, Laurent F. The methylerythritol phosphate pathway for isoprenoid biosynthesis in coccidia: presence and sensitivity to fosmidomycin. Exp Parasitol 2007; 116(4): 375-84.
  • 10. Denny P, Preiser P, Williamson D, Wilson I. Evidence for a single origin of the 35 kb plastid DNA in apicomplexans. Protist 1998; 149: 51-59.
  • Hopkins J, Fowler R, Krishna S, Wilson I, Mitchell G, Bannister L. The plastid in Plasmodium falciparum asexual blood stages: a three-dimensional ultrastructural analysis. Protist 1999; 150(3): 283-95.
  • 22. Igarashi K, Ishihama A. Bipartite functional map of the E. coli RNA polymerase a subunit: involvement of the C-terminal region in transcription activation by cAMP-CRP. Cell 1991; 65(6): 1015-22.
  • 23. Janouskovec J, Horak A, Obornik M, Lukes J, Keeling PJ A common red algal origin of the apicomplexan, dinoflagellate, and heterokont plastids. Proc Natl Acad Sci USA 2010; 107: 10949-54.
  • 24. Jomaa H, Wiesner J, Sanderbrand S, Altincicek B, Weidemeyer C, Hintz M, Turbachova I, Eberl M, Zeidler J, Lichtenthaler HK, Soldati D, Beck E. Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs. Science 1999; 285(5433): 1573-6.
  • 25. Kalanon M, Tonkin CJ, McFadden GI. Characterization of two putative protein translocation components in the apicoplast of Plasmodium falciparum. Eukaryot Cell 2009; 8(8): 1146-54.
  • 26. Kilejian A. Circular mitochondrial DNA from the avian malarial parasite Plasmodium lophurae. Biochim Biophys Acta 1975; 390(3): 276-84.
  • 27. Kobayashi T, Sato S, Takamiya S, Komaki-Yasuda K, Yano K,Hirata A, Onitsuka I, Hata M, Mi-ichi F, Tanaka T, Hase T, Miyajima A, Kawazu S, Watanabe Y, Kita K. Mitochondriaand apicoplast of Plasmodium falciparum: Behaviouron subcellular fractionation and the implication. Mitochondrion 2007; 7(1-2): 125-32.
  • 28. Köhler S, Delwiche CF, Denny PW, Tilney LG, Webster P, Wilson RJM, Palmer JD, Roos DS. A plastid of probable green algal origin in apicomplexan parasites. Science 1997; 275 (5305): 1485-89.
  • 29. Lang M, Apt KE, Kroth PG. Protein transport into ‘‘complex’’ diatom plastids utilizes two different targeting signals. J Biol Chem 1998; 273(47): 30973-8.
  • 30. Lang-Unnasch N, Reith ME, Munholland J, Barta JR. Plastids are widespread and ancient in parasites of the phylum Apicomplexa. Int J Parasitol 1998; 28(11): 1743-54.
  • Pain A, Renauld H, Berriman M, Murphy L, Yeats CA, Weir W, Kerhornou A, Aslett M, Bishop R, Bouchier C, Cochet M, Coulson RM, Cronin A, de Villiers EP, Fraser A, Fosker N, Gardner M,Goble A, Griffiths-Jones S, Harris DE, Katzer F, Larke N, Lord A, Maser P, McKellar S, Mooney P, Morton F, Nene V, O’Neil S, Price C, Quail MA, Rabbinowitsch E, Rawlings ND, Rutter S, Saunders D, Seeger K, Shah T, Squares R, Squares S, Tivey A, Walker AR, Woodward J, Dobbelaere DA, Langsley G, Rajandream MA, McKeever D, Shiels B, Tait A, Barrell B, Hall N. Genome of the host-cell transforming parasite Theileria annulata compared with T. parva. Science 2005; 309(5731): 131-3.
  • 42. Perkins FO, Barta JR, Clopton RE, Peirce MA, Upton SJ. Phylum Apicomplexa. Lee JJ, Leedale GF, Bradbury P. eds. In: An Illustrated Guİde to the Protozoa. Kansas: Society of Protozoologists, 2000; pp. 190.
  • 43. Ralph SA, Van Dooren GG, Waller RF, Crawford MJ, Fraunholz MJ, Foth BJ, Tonkin CJ, Roos DS, McFadden GI. Tropical infectious diseases: metabolic maps and functions of the Plasmodium falciparum apicoplast. Nat Rev Microbiol 2004; 2(3): 203-16.
  • 44. Ram EV, Naik R, Ganguli M, Habib S. DNA organization by the apicoplast-targeted bacterial histone-like protein of Plasmodium falciparum. Nucleic Acids Res 2008; 36(15): 5061-73.
  • 45. Reiff SB, Vaishnava S, Striepena B. The HU Protein is important for apicoplast genome maintenance and ınheritance in Toxoplasma gondii. Eukaryotic Cell 2012; 11( 7): 905-15.
  • 46. Richter S, Lamppa GK. A chloroplast processing enzyme functions as the general stromal processing peptidase. Proc Natl Acad Sci USA 1998; 95(13): 7463-8.
  • 47. Roos DS, Crawford MJ, Donald RG, Fraunholz M, Harb OS, He CY, Kissinger JC, Shaw MK, Striepen B. Mining the plasmodium genome database to define organellar function: hat does the apicoplast do? Philos Trans R Soc Lond B Biol Sci 2002; 357(1417): 35-46.
  • 48. Sasaki N, Hirai M, Maeda K, Yui R, Itoh K, Namiki S, Morita T, Hata M, Murakami-Murofushi K, Matsuoka H, Kita K, Sato S. The plasmodium HU homolog, which binds the plastid DNA sequence-independent manner, is essential for the parasite’s survival. FEBS Lett 2009; 583(9): 1446-50.
  • 49. Sato N, Terasawa K, Miyajima K, Kabeya Y. Organization, developmental dynamics, and evolution of plastid nucleoids. Int Rev Cytol 2003 232:217-62.
  • 50. Sato S, Clough B, Coates L, Wilson RJM. Enzymes for heme biosynthesis are found in both the mitochondrion and plastid of the malaria parasite Plasmodium falciparum. Protist 2004; 155(1): 117-25.
  • Tomova C, Geerts WJ, Muller-Reichert T, Entzeroth R, Humbel BM. New comprehension of the apicoplast of Sarcocystis by transmission electron tomography. Biol Cell 2006; 98(9) :535-45.
  • 62. Tomova C, Humbel BM, Geerts WJ, Entzeroth R, Holthuis JC, Verkleij AJ. Membrane contact sites between apicoplast and ER in Toxoplasma gondii revealed by electron tomography. Traffic 2009; 10(10): 1471-80.
  • 63. Tonkin CJ, Struck NS, Mullin KA, Stimmler LM, McFadden GI. Evidence for Golgi-independent transport from the early secretory pathway to the plastid in malaria parasites. Mol Microbiol 2006; 61(3): 614-30.
  • 64. Toso MA, Omoto CK. Gregarina niphandrodes may lack both a plastid genome and organelle. J Eukaryot Microbiol 2007; 54(1): 66-72.
  • 65. Waller RF, Keeling PJ. Alveolate and chlorophycean mitochondrial cox2 genes split twice independently. Gene 2006; 383: 33-7.
  • 66. Waller RF, Keeling PJ, Donald RG, Striepen B, Handman E, Lang-Unnasch N, Cowman AF, Besra GS, Roos DS, McFadden GI. Nuclear-encoded proteins target to the plastid in Toxoplasma gondii and Plasmodium falciparum. Proc Natl Acad Sci USA 1998; 95(21): 12352–7.
  • 67. Waller RF, Keeling PJ, van Dooren GG, McFadden GI. Comment on “A green algal apicoplast ancestor”. Science 2003; 301(5629): 49.
  • 68. Waller RF, Reed MB, Cowman AF, McFadden GI. Protein trafficking to the plastid of Plasmodium falciparum is via the secretory pathway. EMBO J 2000; 19(8): 1794-1802.
  • 69. Waller RF, Ralph SA, Reed MB, Su V, Douglas JD, Minnikin DE, Cowman AF, Besra GS, McFadden GI. A type II pathway for fatty acid biosynthesis presents drug targets in Plasmodium falciparum. Antimicrob Agents Chemother 2003b; 47(1): 297-301.
  • 70. Williamson DH, Denny PW, Moore PW, Sato S, McCready S, Wilson RJM. The in vivo conformation of the plastid DNA of Toxoplasma gondii: İmplications for replication. J Mol Biol 2001; 306(2):159-68.
There are 40 citations in total.

Details

Journal Section Articles
Authors

Abdullah İnci

Gözde Şahingöz Demirpolat This is me

Alparslan Yıldırım

Önder Düzlü

Publication Date April 15, 2017
Submission Date April 3, 2017
Acceptance Date April 5, 2016
Published in Issue Year 2017 Volume: 14 Issue: 1

Cite

APA İnci, A., Şahingöz Demirpolat, G., Yıldırım, A., Düzlü, Ö. (2017). Apicomplexan Protozoonlarda Apicoplast. Erciyes Üniversitesi Veteriner Fakültesi Dergisi, 14(1), 49-59.
AMA İnci A, Şahingöz Demirpolat G, Yıldırım A, Düzlü Ö. Apicomplexan Protozoonlarda Apicoplast. Erciyes Üniv Vet Fak Derg. April 2017;14(1):49-59.
Chicago İnci, Abdullah, Gözde Şahingöz Demirpolat, Alparslan Yıldırım, and Önder Düzlü. “Apicomplexan Protozoonlarda Apicoplast”. Erciyes Üniversitesi Veteriner Fakültesi Dergisi 14, no. 1 (April 2017): 49-59.
EndNote İnci A, Şahingöz Demirpolat G, Yıldırım A, Düzlü Ö (April 1, 2017) Apicomplexan Protozoonlarda Apicoplast. Erciyes Üniversitesi Veteriner Fakültesi Dergisi 14 1 49–59.
IEEE A. İnci, G. Şahingöz Demirpolat, A. Yıldırım, and Ö. Düzlü, “Apicomplexan Protozoonlarda Apicoplast”, Erciyes Üniv Vet Fak Derg, vol. 14, no. 1, pp. 49–59, 2017.
ISNAD İnci, Abdullah et al. “Apicomplexan Protozoonlarda Apicoplast”. Erciyes Üniversitesi Veteriner Fakültesi Dergisi 14/1 (April 2017), 49-59.
JAMA İnci A, Şahingöz Demirpolat G, Yıldırım A, Düzlü Ö. Apicomplexan Protozoonlarda Apicoplast. Erciyes Üniv Vet Fak Derg. 2017;14:49–59.
MLA İnci, Abdullah et al. “Apicomplexan Protozoonlarda Apicoplast”. Erciyes Üniversitesi Veteriner Fakültesi Dergisi, vol. 14, no. 1, 2017, pp. 49-59.
Vancouver İnci A, Şahingöz Demirpolat G, Yıldırım A, Düzlü Ö. Apicomplexan Protozoonlarda Apicoplast. Erciyes Üniv Vet Fak Derg. 2017;14(1):49-5.