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The Impact of Host Diet on Titer in


Many invertebrate organisms carry bacterial endosymbionts within their cells. In many cases, this ensures host access to resources provided by the endosymbionts, and reciprocally, a rich source of host-supplied nutrients supports bacterial growth and reproduction. However if bacterial reproduction is uncontrolled, an over-abundance of bacteria will ultimately destroy the host cell. Here we explore the factors that regulate endosymbiont abundance in host cells. We focused on Wolbachia endosymbionts that are carried naturally in the germ cells of fruit flies. Specifically, we determined whether dietary nutrients affect the amount of Wolbachia bacteria carried by female flies. We found that yeast-enriched diets strongly depleted Wolbachia in fly ovarian cells. By contrast, sucrose-enriched diets doubled the amount of Wolbachia in ovarian cells. In addition, we found that this response to diet is mediated through highly conserved TORC1 and insulin signaling pathways in the fly. Recent studies have revealed that host diet dramatically influences the types and abundance of gut microbes. Our study informs how host diet affects endosymbiotic bacteria housed within specific types of host cells.


Vyšlo v časopise: The Impact of Host Diet on Titer in. PLoS Pathog 11(3): e32767. doi:10.1371/journal.ppat.1004777
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004777

Souhrn

Many invertebrate organisms carry bacterial endosymbionts within their cells. In many cases, this ensures host access to resources provided by the endosymbionts, and reciprocally, a rich source of host-supplied nutrients supports bacterial growth and reproduction. However if bacterial reproduction is uncontrolled, an over-abundance of bacteria will ultimately destroy the host cell. Here we explore the factors that regulate endosymbiont abundance in host cells. We focused on Wolbachia endosymbionts that are carried naturally in the germ cells of fruit flies. Specifically, we determined whether dietary nutrients affect the amount of Wolbachia bacteria carried by female flies. We found that yeast-enriched diets strongly depleted Wolbachia in fly ovarian cells. By contrast, sucrose-enriched diets doubled the amount of Wolbachia in ovarian cells. In addition, we found that this response to diet is mediated through highly conserved TORC1 and insulin signaling pathways in the fly. Recent studies have revealed that host diet dramatically influences the types and abundance of gut microbes. Our study informs how host diet affects endosymbiotic bacteria housed within specific types of host cells.


Zdroje

1. Davy SK, Allemand D, Weis VM (2012) Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol Mol Biol Rev 76: 229–261. doi: 10.1128/MMBR.05014-11 22688813

2. Feldhaar H, Straka J, Krischke M, Berthold K, Stoll S, et al. (2007) Nutritional upgrading for omnivorous carpenter ants by the endosymbiont Blochmannia. BMC Biol 5: 48. 17971224

3. Gibson KE, Kobayashi H, Walker GC (2008) Molecular Determinants of a Symbiotic Chronic Infection. Annual Review of Genetics 42: 413–441. doi: 10.1146/annurev.genet.42.110807.091427 18983260

4. Hosokawa T, Koga R, Kikuchi Y, Meng XY, Fukatsu T (2010) Wolbachia as a bacteriocyte-associated nutritional mutualist. Proc Natl Acad Sci U S A 107: 769–774. doi: 10.1073/pnas.0911476107 20080750

5. Johnson MD (2011) The acquisition of phototrophy: adaptive strategies of hosting endosymbionts and organelles. Photosynthesis Research 107: 117–132. doi: 10.1007/s11120-010-9546-8 20405214

6. Nakabachi A, Ishikawa H (1999) Provision of riboflavin to the host aphid, Acyrthosiphon pisum, by endosymbiotic bacteria, Buchnera. J Insect Physiol 45: 1–6. 12770389

7. Nogge G (1981) Significance of Symbionts for the Maintenance of an Optimal Nutritional State for Successful Reproduction in Hematophagous Arthropods. Parasitology 82: 101–104.

8. Oldroyd GED (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nature Reviews Microbiology 11: 252–263. doi: 10.1038/nrmicro2990 23493145

9. Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nature Reviews Microbiology 6: 763–775. doi: 10.1038/nrmicro1987 18794914

10. Puchta O (1955) Experimentelle Untersuchungen uber die Bedeutung der Symbiose der Kleiderlaus Pediculus vestimenti Burm. Z Parasitenk 17. 13312506

11. Sabree ZL, Huang CY, Okusu A, Moran NA, Normark BB (2013) The nutrient supplying capabilities of Uzinura, an endosymbiont of armoured scale insects. Environ Microbiol 15: 1988–1999. doi: 10.1111/1462-2920.12058 23279075

12. Sabree ZL, Kambhampati S, Moran NA (2009) Nitrogen recycling and nutritional provisioning by Blattabacterium, the cockroach endosymbiont. Proc Natl Acad Sci U S A 106: 19521–19526. doi: 10.1073/pnas.0907504106 19880743

13. Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H (2000) Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407: 81–86. 10993077

14. Stambler N (2011) Zooxanthellae: The yellow symbionts inside animals. In: Dubinsy Z, Stambler N, editors. Coral reefs: an ecosystem in transition. New York: Springer. pp. 87–106.

15. Snyder AK, McLain C, Rio RVM (2012) The Tsetse Fly Obligate Mutualist Wigglesworthia morsitans Alters Gene Expression and Population Density via Exogenous Nutrient Provisioning. Applied and Environmental Microbiology 78: 7792–7797. doi: 10.1128/AEM.02052-12 22904061

16. Snyder AK, Deberry JW, Runyen-Janecky L, Rio RV (2010) Nutrient provisioning facilitates homeostasis between tsetse fly (Diptera: Glossinidae) symbionts. Proc Biol Sci 277: 2389–2397. doi: 10.1098/rspb.2010.0364 20356887

17. Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6: 741–751. doi: 10.1038/nrmicro1969 18794912

18. Serbus LR, Casper-Lindley C, Landmann F, Sullivan W (2008) The Genetics and Cell Biology of Wolbachia-Host Interactions. Annual Review of Genetics 42: 683–707. doi: 10.1146/annurev.genet.41.110306.130354 18713031

19. Zug R, Hammerstein P (2012) Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PLoS One 7: e38544. doi: 10.1371/journal.pone.0038544 22685581

20. Ashburner M (1989) Drosophila, a Laboratory Handbook. New York: Cold Spring Harbor Laboratory Press. 1331 p.

21. Snook RR, Cleland SY, Wolfner MF, Karr TL (2000) Offsetting effects of Wolbachia infection and heat shock on sperm production in Drosophila simulans: analyses of fecundity, fertility and accessory gland proteins. Genetics 155: 167–178. 10790392

22. Bressac C, Rousset F (1993) The reproductive incompatibility system in Drosophila simulans: DAPI-staining analysis of the Wolbachia symbionts in sperm cysts. J Invertebr Pathol 61: 226–230. 7689622

23. Clark ME, Veneti Z, Bourtzis K, Karr TL (2002) The distribution and proliferation of the intracellular bacteria Wolbachia during spermatogenesis in Drosophila. Mech Dev 111: 3–15. 11804774

24. Hoffmann AA, Hercus M, Dagher H (1998) Population dynamics of the Wolbachia infection causing cytoplasmic incompatibility in Drosophila melanogaster. Genetics 148: 221–231. 9475734

25. Turelli M, Hoffmann AA (1995) Cytoplasmic incompatibility in Drosophila simulans: dynamics and parameter estimates from natural populations. Genetics 140: 1319–1338. 7498773

26. Ashburner M (1989) Developmental Biology. Drosophila, a Laboratory Handbook. Cold Spring Harbor: Cold Spring Harbor Laboratory Press. pp. 139–204.

27. King RC (1970) Ovarian development in Drosophila melanogaster. New York: Academic Press. 227 p.

28. Spradling AC (1993) Developmental Genetics of Oogenesis. In: Bate M, Arias AM, editors. The Development of Drosophila melanogaster. New York: Cold Spring Harbor Laboratory Press. pp. 1–70.

29. Kugler JM, Lasko P (2009) Localization, anchoring and translational control of oskar, gurken, bicoid and nanos mRNA during Drosophila oogenesis. Fly (Austin) 3: 15–28. 19182536

30. Hudson AM, Cooley L (2014) Methods for studying oogenesis. Methods.

31. Ferree PM, Frydman HM, Li JM, Cao J, Wieschaus E, et al. (2005) Wolbachia utilizes host microtubules and Dynein for anterior localization in the Drosophila oocyte. PLoS Pathog 1: e14. 16228015

32. Serbus L, Ferreccio A, Zhukova M, McMorris C, Kiseleva E, et al. (2011) A feedback loop between Wolbachia and the Drosophila gurken mRNP complex influences Wolbachia titer. J Cell Sci 124: 4299–4308. doi: 10.1242/jcs.092510 22193955

33. Casper-Lindley C, Kimura S, Saxton DS, Essaw Y, Simpson I, et al. (2011) Rapid Fluorescence-Based Screening for Wolbachia Endosymbionts in Drosophila Germ Line and Somatic Tissues. Applied and Environmental Microbiology 77: 4788–4794. doi: 10.1128/AEM.00215-11 21622788

34. Fast EM, Toomey ME, Panaram K, Desjardins D, Kolaczyk ED, et al. (2011) Wolbachia Enhance Drosophila Stem Cell Proliferation and Target the Germline Stem Cell Niche. Science 334: 990–992. doi: 10.1126/science.1209609 22021671

35. Toomey ME, Panaram K, Fast EM, Beatty C, Frydman HM (2013) Evolutionarily conserved Wolbachia-encoded factors control pattern of stem-cell niche tropism in Drosophila ovaries and favor infection. Proceedings of the National Academy of Sciences of the United States of America 110: 10788–10793. doi: 10.1073/pnas.1301524110 23744038

36. Frydman HM, Li JM, Robson DN, Wieschaus E (2006) Somatic stem cell niche tropism in Wolbachia. Nature 441: 509–512. 16724067

37. Veneti Z, Clark ME, Karr TL, Savakis C, Bourtzis K (2004) Heads or tails: host-parasite interactions in the Drosophila-Wolbachia system. Appl Environ Microbiol 70: 5366–5372. 15345422

38. Serbus LR, Sullivan W (2007) A Cellular Basis for Wolbachia Recruitment to the Host Germline. PLoS Pathog 3: e190. 18085821

39. Hadfield SJ, Axton JM (1999) Germ cells colonized by endosymbiotic bacteria. Nature 402: 482. 10591206

40. Anagnostou C, Dorsch M, Rohlfs M (2010) Influence of dietary yeasts on Drosophila melanogaster life-history traits. Entomol Exp Appl 136: 1–11.

41. Begon M (1982) Yeasts and Drosophila. In: Ashburner M, Carson HL, Thompson JN Jr., editors. The Genetics and Biology of Drosophila. San Francisco: Academic Press. pp. 345–384.

42. Shorrocks B (1982) The Breeding Sites of Temperate Woodland Drosophila. In: Ashburner M, Carson HL, Thompson JN Jr., editors. The Genetics and Biology and Biology of Drosophila. San Francisco: Academic Press. pp. 385–428.

43. Brncic D (1983) Ecology of Flower-Breeding Drosophila. In: Ashburner M, Carson HL, Thompson JN Jr., editors. The Genetics and Biology of Drosophila. San Francisco: Academic Press. pp. 333–382.

44. Kukor JJ, Martin MM (1987) Nutritional Ecology of Fungus-feeding Arthropods. In: Slansky F Jr., Rodriguez JG, editors. Nutritional Ecology of Insects, Mites, Spiders, and Related Invertebrates. New York: John Wiley and Sons. pp. 791–836.

45. Coluccio AE, Rodriguez RK, Kernan MJ, Neiman AM (2008) The yeast spore wall enables spores to survive passage through the digestive tract of Drosophila. PLoS One 3: e2873. doi: 10.1371/journal.pone.0002873 18682732

46. Teleman AA (2010) Molecular mechanisms of metabolic regulation by insulin in Drosophila. Biochemical Journal 425: 13–26. doi: 10.1042/BJ20091181 20001959

47. Colombani J, Raisin S, Pantalacci S, Radimerski T, Montagne J, et al. (2003) A nutrient sensor mechanism controls Drosophila growth. Cell 114: 739–749. 14505573

48. Colombani J, Raisin S, Pantalacci S, Radimerski T, Montagne J, et al. (2003) Amino acids and the humoral regulation of growth: fat bodies use Slimfast (vol 114, pg 656, 2003). Cell 115: 123–123.

49. Choi JW, Chen J, Schreiber SL, Clardy J (1996) Structure of the FKBP12-rapamycin complex interacting with the binding domain of human FRAP. Science 273: 239–242. 8662507

50. Chen J, Zheng XF, Brown EJ, Schreiber SL (1995) Identification of an 11-Kda Fkbp12-Rapamycin-Binding Domain within the 289-Kda Fkbp12-Rapamycin-Associated Protein and Characterization of a Critical Serine Residue. Proceedings of the National Academy of Sciences of the United States of America 92: 4947–4951. 7539137

51. Guertin DA, Sabatini DM (2009) The Pharmacology of mTOR Inhibition. Science Signaling 2.

52. Yip CK, Murata K, Walz T, Sabatini DM, Kang SA (2010) Structure of the Human mTOR Complex I and Its Implications for Rapamycin Inhibition. Molecular Cell 38: 768–774. doi: 10.1016/j.molcel.2010.05.017 20542007

53. Gonzalez IM, Martin PM, Burdsal C, Sloan JL, Mager S, et al. (2012) Leucine and arginine regulate trophoblast motility through mTOR-dependent and independent pathways in the preimplantation mouse embryo. Developmental Biology 361: 286–300. doi: 10.1016/j.ydbio.2011.10.021 22056783

54. Wang YX, Zhang LL, Zhou GL, Liao ZY, Ahmad H, et al. (2012) Dietary L-arginine supplementation improves the intestinal development through increasing mucosal Akt and mammalian target of rapamycin signals in intra-uterine growth retarded piglets. British Journal of Nutrition 108: 1371–1381. doi: 10.1017/S0007114511006763 22217383

55. Xi PB, Jiang ZY, Dai ZL, Li XL, Yao K, et al. (2010) Regulation of protein turnover in porcine intestinal cells by L-glutamine (Gln). Faseb Journal 24.

56. Yao K, Yin YL, Chu WY, Li ZQ, Deng D, et al. (2008) Dietary arginine supplementation increases mTOR signaling activity in skeletal muscle of neonatal pigs. Journal of Nutrition 138: 867–872. 18424593

57. Atherton PJ, Smith K, Etheridge T, Rankin D, Rennie MJ (2010) Distinct anabolic signalling responses to amino acids in C2C12 skeletal muscle cells. Amino Acids 38: 1533–1539. doi: 10.1007/s00726-009-0377-x 19882215

58. Norton LE, Layman DK, Bunpo P, Anthony TG, Brana DV, et al. (2009) The Leucine Content of a Complete Meal Directs Peak Activation but Not Duration of Skeletal Muscle Protein Synthesis and Mammalian Target of Rapamycin Signaling in Rats. Journal of Nutrition 139: 1103–1109. doi: 10.3945/jn.108.103853 19403715

59. Dibble CC, Elis W, Menon S, Qin W, Klekota J, et al. (2012) TBC1D7 Is a Third Subunit of the TSC1-TSC2 Complex Upstream of mTORC1. Molecular Cell 47: 535–546. doi: 10.1016/j.molcel.2012.06.009 22795129

60. Stocker H, Radimerski T, Schindelholz B, Wittwer F, Belawat P, et al. (2003) Rheb is an essential regulator of S6K in controlling cell growth in Drosophila. Nature Cell Biology 5: 559–565. 12766775

61. Saucedo LJ, Gao XS, Chiarelli DA, Li L, Pan D, et al. (2003) Rheb promotes cell growth as a component of the insulin/TOR signalling network. Nature Cell Biology 5: 566–571. 12766776

62. Inoki K, Li Y, Zhu TQ, Wu J, Guan KL (2002) TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nature Cell Biology 4: 648–657. 12172553

63. Cai SL, Tee AR, Short JD, Bergeron JM, Kim J, et al. (2006) Activity of TSC2 is inhibited by AKT-mediated phosphorylation and membrane partitioning. Journal of Cell Biology 173: 279–289. 16636147

64. Ito N, Rubin GM (1999) Gigas, a Drosophila homolog of tuberous sclerosis gene product-2, regulates the cell cycle. Cell 96: 529–539. 10052455

65. Huang JX, Manning BD (2009) A complex interplay between Akt, TSC2 and the two mTOR complexes. Biochemical Society Transactions 37: 217–222. doi: 10.1042/BST0370217 19143635

66. Inoki K, Guan KL (2009) Tuberous sclerosis complex, implication from a rare genetic disease to common cancer treatment. Human Molecular Genetics 18: R94–R100. doi: 10.1093/hmg/ddp032 19297407

67. Tapon N, Ito N, Dickson BJ, Treisman JE, Hariharan IK (2001) The Drosophila tuberous sclerosis complex gene homologs restrict cell growth and cell proliferation. Cell 105: 345–355. 11348591

68. Gao XS, Pan DJ (2001) TSC1 and TSC2 tumor suppressors antagonize insulin signaling in cell growth. Genes & Development 15: 1383–1392.

69. Ni JQ, Zhou R, Czech B, Liu LP, Holderbaum L, et al. (2011) A genome-scale shRNA resource for transgenic RNAi in Drosophila. Nat Methods 8: 405–407. doi: 10.1038/nmeth.1592 21460824

70. Ni JQ, Markstein M, Binari R, Pfeiffer B, Liu LP, et al. (2008) Vector and parameters for targeted transgenic RNA interference in Drosophila melanogaster. Nat Methods 5: 49–51. 18084299

71. Wodarz A, Hinz U, Engelbert M, Knust E (1995) Expression of crumbs confers apical character on plasma membrane domains of ectodermal epithelia of Drosophila. Cell 82: 67–76. 7606787

72. Petrella LN, Smith-Leiker T, Cooley L (2007) The Ovhts polyprotein is cleaved to produce fusome and ring canal proteins required for Drosophila oogenesis. Development 134: 702–712.

73. Broughton SJ, Piper MDW, Ikeya T, Bass TM, Jacobson J, et al. (2005) Longer lifespan, altered metabolism, and stress resistance in Drosophila from ablation of cells making insulin-like ligands. Proceedings of the National Academy of Sciences of the United States of America 102: 3105–3110. 15708981

74. Haselton A, Sharmin E, Schrader J, Sah M, Poon P, et al. (2010) Partial ablation of adult Drosophila insulin-producing neurons modulates glucose homeostasis and extends life span without insulin resistance. Cell Cycle 9: 3063–3071. doi: 10.4161/cc.9.15.12458 20699643

75. Pasco MY, Leopold P (2012) High sugar-induced insulin resistance in Drosophila relies on the lipocalin Neural Lazarillo. PLoS One 7: e36583. doi: 10.1371/journal.pone.0036583 22567167

76. Morris SN, Coogan C, Chamseddin K, Fernandez-Kim SO, Kolli S, et al. (2012) Development of diet-induced insulin resistance in adult Drosophila melanogaster. Biochim Biophys Acta 1822: 1230–1237. doi: 10.1016/j.bbadis.2012.04.012 22542511

77. Yang Q, Graham TE, Mody N, Preitner F, Peroni OD, et al. (2005) Serum retinol binding protein 4 contributes to insulin resistance in obesity and type 2 diabetes. Nature 436: 356–362. 16034410

78. Graham TE, Yang Q, Bluher M, Hammarstedt A, Ciaraldi TP, et al. (2006) Retinol-binding protein 4 and insulin resistance in lean, obese, and diabetic subjects. N Engl J Med 354: 2552–2563. 16775236

79. Norseen J, Hosooka T, Hammarstedt A, Yore MM, Kant S, et al. (2012) Retinol-binding protein 4 inhibits insulin signaling in adipocytes by inducing proinflammatory cytokines in macrophages through a c-Jun N-terminal kinase- and toll-like receptor 4-dependent and retinol-independent mechanism. Mol Cell Biol 32: 2010–2019. doi: 10.1128/MCB.06193-11 22431523

80. Bohni R, Riesgo-Escovar J, Oldham S, Brogiolo W, Stocker H, et al. (1999) Autonomous control of cell and organ size by CHICO, a Drosophila homolog of vertebrate IRS1-4. Cell 97: 865–875. 10399915

81. Ogawa W, Matozaki T, Kasuga M (1998) Role of binding proteins to IRS-1 in insulin signalling. Molecular and Cellular Biochemistry 182: 13–22. 9609110

82. Werz C, Kohler K, Hafen E, Stocker H (2009) The Drosophila SH2B family adaptor Lnk acts in parallel to chico in the insulin signaling pathway. PLoS Genet 5: e1000596. doi: 10.1371/journal.pgen.1000596 19680438

83. Drummond-Barbosa D, Spradling AC (2001) Stem cells and their progeny respond to nutritional changes during Drosophila oogenesis. Dev Biol 231: 265–278. 11180967

84. Tatar M, Kopelman A, Epstein D, Tu MP, Yin CM, et al. (2001) A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 292: 107–110. 11292875

85. Richard DS, Rybczynski R, Wilson TG, Wang Y, Wayne ML, et al. (2005) Insulin signaling is necessary for vitellogenesis in Drosophila melanogaster independent of the roles of juvenile hormone and ecdysteroids: female sterility of the chico1 insulin signaling mutation is autonomous to the ovary. J Insect Physiol 51: 455–464. 15890189

86. LaFever L, Drummond-Barbosa D (2005) Direct control of germline stem cell division and cyst growth by neural insulin in Drosophila. Science 309: 1071–1073. 16099985

87. Ikeya T, Broughton S, Alic N, Grandison R, Partridge L (2009) The endosymbiont Wolbachia increases insulin/IGF-like signalling in Drosophila. Proceedings of the Royal Society B-Biological Sciences 276: 3799–3807. doi: 10.1098/rspb.2009.0778 19692410

88. LaFever L, Feoktistov A, Hsu HJ, Drummond-Barbosa D (2010) Specific roles of Target of rapamycin in the control of stem cells and their progeny in the Drosophila ovary (vol 137, pg 2117, 2010). Development 137: 2451–2451.

89. Gronke S, Clarke DF, Broughton S, Andrews TD, Partridge L (2010) Molecular Evolution and Functional Characterization of Drosophila Insulin-Like Peptides. Plos Genetics 6.

90. Hsu HJ, Drummond-Barbosa D (2009) Insulin levels control female germline stem cell maintenance via the niche in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 106: 1117–1121. doi: 10.1073/pnas.0809144106 19136634

91. Hsu HJ, LaFever L, Drummond-Barbosa D (2008) Diet controls normal and tumorous germline stem cells via insulin-dependent and-independent mechanisms in Drosophila. Developmental Biology 313: 700–712. 18068153

92. Heifetz Y, Tram U, Wolfner MF (2001) Male contributions to egg production: the role of accessory gland products and sperm in Drosophila melanogaster. Proc Biol Sci 268: 175–180. 11209888

93. Soller M, Bownes M, Kubli E (1997) Mating and sex peptide stimulate the accumulation of yolk in oocytes of Drosophila melanogaster. Eur J Biochem 243: 732–738. 9057839

94. Soller M, Bownes M, Kubli E (1999) Control of oocyte maturation in sexually mature Drosophila females. Dev Biol 208: 337–351. 10191049

95. King RC, Sang JH (1959) Oogenesis in adult Drosophila melanogaster. VIII. The role of folic acid in oogenesis. Growth 23: 37–53. 13672469

96. Carvalho GB, Kapahi P, Anderson DJ, Benzer S (2006) Allocrine modulation of feeding behavior by the Sex Peptide of Drosophila. Curr Biol 16: 692–696. 16581515

97. Landmann F, Bain O, Martin C, Uni S, Taylor M, et al. (2012) Both asymmetric mitotic segregation and cell-to-cell invasion are required for stable germline transmission of Wolbachia in filarial nematodes. Biology Open 00: 1–12.

98. Pierce A, Gillette D, Jones PG (2011) Escherichia coli cold shock protein CsdA effects an increase in septation and the resultant formation of coccobacilli at low temperature. Arch Microbiol 193: 373–384. doi: 10.1007/s00203-011-0682-0 21359956

99. Frenkiel-Krispin D, Minsky A (2006) Nucleoid organization and the maintenance of DNA integrity in E. coli, B. subtilis and D. radiodurans. J Struct Biol 156: 311–319. 16935006

100. Min KT, Benzer S (1997) Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proceedings of the National Academy of Sciences of the United States of America 94: 10792–10796. 9380712

101. Albertson R, Tan V, Leads RR, Reyes M, Sullivan W, et al. (2013) Mapping Wolbachia distributions in the adult Drosophila brain. Cellular Microbiology 15: 1527–1544. doi: 10.1111/cmi.12136 23490256

102. Wu M, Sun LV, Vamathevan J, Riegler M, Deboy R, et al. (2004) Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol 2: E69. 15024419

103. Caragata EP, Rances E, O'Neill SL, McGraw EA (2014) Competition for amino acids between Wolbachia and the mosquito host, Aedes aegypti. Microb Ecol 67: 205–218. doi: 10.1007/s00248-013-0339-4 24337107

104. Markov AV, Zakharov IA (2006) The parasitic bacterium Wolbachia and the origin of the eukaryotic cell. Paleontological Journal 40: 115–124.

105. Ponton F, Wilson K, Holmes A, Raubenheimer D, Robinson KL, et al. (2015) Macronutrients mediate the functional relationship between Drosophila and Wolbachia. Proc Biol Sci 282.

106. Ikeya T, Broughton S, Alic N, Grandison R, Partridge L (2009) The endosymbiont Wolbachia increases insulin/IGF-like signalling in Drosophila. Proc Biol Sci 276: 3799–3807. doi: 10.1098/rspb.2009.0778 19692410

107. Matilainen O, Arpalahti L, Rantanen V, Hautaniemi S, Holmberg CI (2013) Insulin/IGF-1 signaling regulates proteasome activity through the deubiquitinating enzyme UBH-4. Cell Rep 3: 1980–1995. doi: 10.1016/j.celrep.2013.05.012 23770237

108. Blakesley VA, Koval AP, Stannard BS, Scrimgeour A, LeRoith D (1998) Replacement of tyrosine 1251 in the carboxyl terminus of the insulin-like growth factor-I receptor disrupts the actin cytoskeleton and inhibits proliferation and anchorage-independent growth. J Biol Chem 273: 18411–18422. 9660809

109. Coletta DK, Mandarino LJ (2011) Mitochondrial dysfunction and insulin resistance from the outside in: extracellular matrix, the cytoskeleton, and mitochondria. Am J Physiol Endocrinol Metab 301: E749–755. doi: 10.1152/ajpendo.00363.2011 21862724

110. Hwang H, Bowen BP, Lefort N, Flynn CR, De Filippis EA, et al. (2010) Proteomics analysis of human skeletal muscle reveals novel abnormalities in obesity and type 2 diabetes. Diabetes 59: 33–42. doi: 10.2337/db09-0214 19833877

111. Abe Y, Yoon SO, Kubota K, Mendoza MC, Gygi SP, et al. (2009) p90 ribosomal S6 kinase and p70 ribosomal S6 kinase link phosphorylation of the eukaryotic chaperonin containing TCP-1 to growth factor, insulin, and nutrient signaling. J Biol Chem 284: 14939–14948. doi: 10.1074/jbc.M900097200 19332537

112. Huang J, Brumell JH (2014) Bacteria-autophagy interplay: a battle for survival. Nat Rev Microbiol 12: 101–114. doi: 10.1038/nrmicro3160 24384599

113. Steele S, Brunton J, Ziehr B, Taft-Benz S, Moorman N, et al. (2013) Francisella tularensis harvests nutrients derived via ATG5-independent autophagy to support intracellular growth. PLoS Pathog 9: e1003562. doi: 10.1371/journal.ppat.1003562 23966861

114. Yu HB, Croxen MA, Marchiando AM, Ferreira RB, Cadwell K, et al. (2014) Autophagy facilitates Salmonella replication in HeLa cells. MBio 5: e00865–00814. doi: 10.1128/mBio.00865-14 24618251

115. Voronin D, Cook DAN, Steven A, Taylor MJ (2012) Autophagy regulates Wolbachia populations across diverse symbiotic associations. Proceedings of the National Academy of Sciences of the United States of America 109: E1638–E1646. doi: 10.1073/pnas.1203519109 22645363

116. Hedges LM, Brownlie JC, O'Neill SL, Johnson KN (2008) Wolbachia and virus protection in insects. Science 322: 702. doi: 10.1126/science.1162418 18974344

117. Teixeira L, Ferreira A, Ashburner M (2008) The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol 6: e2. doi: 10.1371/journal.pbio.1000002 19222304

118. Rainey SM, Shah P, Kohl A, Dietrich I (2014) Understanding the Wolbachia-mediated inhibition of arboviruses in mosquitoes: progress and challenges. J Gen Virol 95: 517–530. doi: 10.1099/vir.0.057422-0 24343914

119. Kriesner P, Hoffmann AA, Lee SF, Turelli M, Weeks AR (2013) Rapid sequential spread of two Wolbachia variants in Drosophila simulans. PLoS Pathog 9: e1003607. doi: 10.1371/journal.ppat.1003607 24068927

120. Hoffmann AA, Montgomery BL, Popovici J, Iturbe-Ormaetxe I, Johnson PH, et al. (2011) Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 476: 454–457. doi: 10.1038/nature10356 21866160

121. Walker T, Johnson PH, Moreira LA, Iturbe-Ormaetxe I, Frentiu FD, et al. (2011) The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature 476: 450–453. doi: 10.1038/nature10355 21866159

122. Chrostek E, Marialva MSP, Esteves SS, Weinert LA, Martinez J, et al. (2013) Wolbachia Variants Induce Differential Protection to Viruses in Drosophila melanogaster: A Phenotypic and Phylogenomic Analysis. Plos Genetics 9.

123. Lu P, Bian G, Pan X, Xi Z (2012) Wolbachia induces density-dependent inhibition to dengue virus in mosquito cells. PLoS Negl Trop Dis 6: e1754. doi: 10.1371/journal.pntd.0001754 22848774

124. Osborne SE, Iturbe-Ormaetxe I, Brownlie JC, O'Neill SL, Johnson KN (2012) Antiviral protection and the importance of Wolbachia density and tissue tropism in Drosophila simulans. Appl Environ Microbiol 78: 6922–6929. doi: 10.1128/AEM.01727-12 22843518

125. Osborne SE, Leong YS, O'Neill SL, Johnson KN (2009) Variation in antiviral protection mediated by different Wolbachia strains in Drosophila simulans. PLoS Pathog 5: e1000656. doi: 10.1371/journal.ppat.1000656 19911047

126. Chrostek E, Marialva MS, Yamada R, O'Neill SL, Teixeira L (2014) High anti-viral protection without immune upregulation after interspecies Wolbachia transfer. PLoS One 9: e99025. doi: 10.1371/journal.pone.0099025 24911519

127. Bloomington_Drosophila_Stock_Center http://flystocks.bio.indiana.edu/Fly_Work/media-recipes/bloomfood.htm.

128. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45. 11328886

129. R_Development_Core_Team (2011) A language and Environment for Statistical Computing. Vienna, Austrria: The R Foundation for Statistical Computing. doi: 10.1016/j.neuroimage.2011.01.013 21238596

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Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

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PLOS Pathogens


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