Molecular Mechanisms of Drosophila Hematopoiesis

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Abstract

As а model organism, the fruit fly (Drosophila melanogaster) has assumed a leading position in modern biological research. The Drosophila genetic system has a number of advantages making it a key model in investigating the molecular mechanisms of metazoan developmental processes. Over the past two decades, significant progress has been made in understanding the molecular mechanisms regulating Drosophila hematopoiesis. This review discusses the major advances in investigating the molecular mechanisms involved in maintaining the population of multipotent progenitor cells and their differentiation into mature hemocytes in the hematopoietic organ of the Drosophila larva. The use of the Drosophila hematopoietic organ as a model system for hematopoiesis has allowed to characterize the complex interactions between signaling pathways and transcription factors in regulating the maintenance and differentiation of progenitor cells through the signals from the hematopoietic niche, autocrine and paracrine signals, and the signals emanated by differentiated cells.

About the authors

S. A. Sinenko

Institute of Cytology Russian Academy of Sciences

Author for correspondence.
Email: s.sinenko@incras.ru
Russian Federation, St. Petersburg, 194064

References

  1. Morgan T.H. // Sci. Mon. 1935. V. 41. № 1. P. 5–18.
  2. Morgan T.H. // Am. Nat. 1917. V. 51. № 609. P. 513–544.
  3. Nefedova L.N. // Russ. J. Dev. Biol. 2020. V. 51. № 4. P. 201–211.
  4. Osadchiy I.S., Kamalyan S.O., Tumashova K.Y., Georgiev P.G., Maksimenko O.G. // Acta Naturae. 2023. V. 15. № 2. P. 70–74.
  5. Brand A.H., Perrimon N. // Development. 1993. V. 118. № 2. P. 401–415.
  6. Evans C.J., Olson J.M., Ngo K.T., Kim E., Lee N.E., Kuoy E., Patananan A.N., Sitz D., Tran P., Do M.-T. et al. // Nat. Meth. 2009. V. 6. № 8. P. 603–605.
  7. Hu Y., Comjean A., Rodiger J., Liu Y., Gao Y., Chung V., Zirin J., Perrimon N., Mohr S. E. // Nucleic Acids Res. 2021. V. 49. № D1. P. D908–D915.
  8. Cooley L., Kelley R., Spradling A. // Science. 1988. V. 239. № 4844. P. 1121–1128.
  9. Bokel C. // Methods Mol. Biol. 2008. V. 420. P. 119–138.
  10. Braun A., Lemaitre B., Lanot R., Zachary D., Meister M. // Genetics. 1997. V. 147. № 2. P. 623–634.
  11. Nemudryi A.A., Valetdinova K.R., Medvedev S.P., Zakian S.M. // Acta Naturae. 2014. V. 6. № 3. P. 19–40.
  12. Friedman A., Perrimon N. // Curr. Opin. Genet. Dev. 2004. V. 14. № 5. P. 470–476.
  13. Sinenko S.A., Kim E.K., Wynn R., Manfruelli P., Ando I., Wharton K.A., Perrimon N., Mathey-Prevot B. // Dev. Biol. 2004. V. 273. № 1. P. 48–62.
  14. Kaufman T. C. // Genetics. 2017. V. 206. № 2. P. 665–689.
  15. St Johnston D. // Nat. Rev. Genet. 2002. V. 3. № 3. P. 176–188.
  16. Reitman Z.J., Sinenko S.A., Spana E.P., Yan H. // Blood. 2015. V. 125. № 2. P. 336–345.
  17. Sinenko S.A., Hung T., Moroz T., Tran Q.M., Sidhu S., Cheney M.D., Speck N.A., Banerjee U. // Blood. 2010. V. 116. № 22. P. 4612–4620.
  18. Hales K.G., Korey C.A., Larracuente A.M., Roberts D.M. // Genetics. 2015. V. 201. № 3. P. 815–842.
  19. Schneider D. // Nat. Rev. Genet. 2000. V. 1. № 3. P. 218–226.
  20. Perrimon N. // Proc. Natl. Acad. Sci. USA. 1998. V. 95. № 17. P. 9716–9717.
  21. Celniker S.E., Rubin G.M. // Annu. Rev. Genomics Hum. Genet. 2003. V. 4. P. 89–117.
  22. Sinenko S.A. // Oncotarget. 2017. V. 8. № 41. P. 70452–70462.
  23. Yang C.S., Sinenko S.A., Thomenius M.J., Robeson A.C., Freel C.D., Horn S.R., Kornbluth S. // Cell Death Differ. 2014. V. 21. № 4. P. 604–611.
  24. Shrestha R., Gateff E. // Dev. Growth. Differ. 1982. V. 24. № 1. P. 65–82.
  25. Mathey-Prevot B., Perrimon N. // Cell. 1998. V. 92. № 6. P. 697–700.
  26. Lanot R., Zachary D., Holder F., Meister M. // Dev. Biol. 2001. V. 230. № 2. P. 243–257.
  27. Evans C.J., Hartenstein V., Banerjee U. // Dev. Cell. 2003. V. 5. № 5. P. 673–690.
  28. Millar D.A., Ratcliffe N.A. // Endeavour. 1989. V. 13. № 2. P. 72–77.
  29. Evans C.J., Sinenko S.A., Mandal L., MartinezAgosto J.A., Hartenstein V., Banerjee U., Rolf B. Genetic Dissection of Hematopoiesis Using Drosophila as a Model System // Advances in Developmental Biology: Elsevier, 2007. P. 259.
  30. Honti V., Csordas G., Kurucz E., Markus R., Ando I. // Dev. Comp. Immunol. 2014. V. 42. № 1. P. 47–56.
  31. Koranteng F., Cho B., Shim J. // Mol. Cells. 2022. V. 45. № 3. P. 101–108.
  32. Banerjee U., Girard J.R., Goins L.M., Spratford C.M. // Genetics. 2019. V. 211. № 2. P. 367–417.
  33. Morin-Poulard I., Tian Y., Vanzo N., Crozatier M. // Front. Immunol. 2021. V. 12. P. 719349.
  34. Kharrat B., Csordas G., Honti V. // Int. J. Mol. Sci. 2022. V. 23. № 14. P. 7767.
  35. Tepass U., Fessler L.I., Aziz A., Hartenstein V. // Development. 1994. V. 120. № 7. P. 1829–1837.
  36. Holz A., Bossinger B., Strasser T., Janning W., Klapper R. // Development. 2003. V. 130. № 20. P. 4955–4962.
  37. Honti V., Csordas G., Markus R., Kurucz E., Jankovics F., Ando I. // Mol. Immunol. 2010. V. 47. № 11–12. P. 1997–2004.
  38. Ghosh S., Singh A., Mandal S., Mandal L. // Dev. Cell. 2015. V. 33. № 4. P. 478–488.
  39. Srdić Ž., Reinhardt C. // Science. 1980. V. 207. № 4437. P. 1375–1377.
  40. Gateff E. // Science. 1978. V. 200. № 4349. P. 1448–1459.
  41. Jung S.H., Evans C.J., Uemura C., Banerjee U. // Development. 2005. V. 132. № 11. P. 2521–2533.
  42. Rugendorff A., Younossi-Hartenstein A., Hartenstein V. // Rouxs Arch. Dev. Biol. 1994. V. 203. № 5. P. 266–280.
  43. Cho B., Yoon S.H., Lee D., Koranteng F., Tattikota S.G., Cha N., Shin M., Do H., Hu Y., Oh S. Y., et al. // Nat. Commun. 2020. V. 11. № 1. P. 4483.
  44. Cattenoz P.B., Monticelli S., Pavlidaki A., Giangrande A. // Front. Cell Dev. Biol. 2021. V. 9. P. 643712.
  45. Fu Y., Huang X., Zhang P., van de Leemput J., Han Z. // J. Genet. Genomics. 2020. V. 47. № 4. P. 175–186.
  46. Cattenoz P.B., Sakr R., Pavlidaki A., Delaporte C., Riba A., Molina N., Hariharan N., Mukherjee T., Giangrande A. // EMBO J. 2020. V. 39. № 12. P. e104486.
  47. Tattikota S.G., Cho B., Liu Y., Hu Y., Barrera V., Steinbaugh M.J., Yoon S.H., Comjean A., Li F., Dervis F., et al. // Elife. 2020. V. 9. P. e54818.
  48. Russo J., Dupas S., Frey F., Carton Y., Brehelin M. // Parasitology. 1996. V. 112 (Pt 1). P. 135–142.
  49. Brehelin M. // Cell Tissue. Res. 1982. V. 221. № 3. P. 607– 615.
  50. Charroux B., Royet J. // Proc. Natl. Acad. Sci. USA. 2009. V. 106. № 24. P. 9797–9802.
  51. Kurucz E., Vaczi B., Markus R., Laurinyecz B., Vilmos P., Zsamboki J., Csorba K., Gateff E., Hultmark D., Ando I. // Acta Biol. Hung. 2007. V. 58 Suppl. P. 95–111.
  52. Franc N.C., Heitzler P., Ezekowitz R.A., White K. // Science. 1999. V. 284. № 5422. P. 1991–1994.
  53. Kocks C., Cho J. H., Nehme N., Ulvila J., Pearson A. M., Meister M., Strom C., Conto S. L., Hetru C., Stuart L. M., et al. // Cell. 2005. V. 123. № 2. P. 335–346.
  54. Bretscher A.J., Honti V., Binggeli O., Burri O., Poidevin M., Kurucz E., Zsamboki J., Ando I., Lemaitre B. // Biol. Open. 2015. V. 4. № 3. P. 355–363.
  55. Irving P., Ubeda J.M., Doucet D., Troxler L., Lagueux M., Zachary D., Hoffmann J.A., Hetru C., Meister M. // Cell. Microbiol. 2005. V. 7. № 3. P. 335–350.
  56. Kurucz E., Markus R., Zsamboki J., Folkl-Medzihradszky K., Darula Z., Vilmos P., Udvardy A., Krausz I., Lukacsovich T., Gateff E. et al. // Curr. Biol. 2007. V. 17. № 7. P. 649–654.
  57. Balandin S., Ovchinnikova T. // Russ. J. Bioorganic Chem. 2016. V. 42. № 3. P. 229–248.
  58. Olofsson B., Page D.T. // Dev. Biol. 2005. V. 279. № 1. P. 233–243.
  59. Bunt S., Hooley C., Hu N., Scahill C., Weavers H., Skaer H. // Dev. Cell. 2010. V. 19. № 2. P. 296–306.
  60. Nelson R.E., Fessler L.I., Takagi Y., Blumberg B., Keene D.R., Olson P.F., Parker C.G., Fessler J.H. // EMBO J. 1994. V. 13. № 15. P. 3438–3447.
  61. Defaye A., Evans I., Crozatier M., Wood W., Lemaitre B., Leulier F. // J. Innate Immun. 2009. V. 1. № 4. P. 322–334.
  62. Sears H.C., Kennedy C.J., Garrity P.A. // Development. 2003. V. 130. № 15. P. 3557–3565.
  63. Guillou A., Troha K., Wang H., Franc N.C., Buchon N. // PLoS Pathog. 2016. V. 12. № 10. P. e1005961.
  64. Shia A.K., Glittenberg M., Thompson G., Weber A.N., Reichhart J.M., Ligoxygakis P. // J. Cell Sci. 2009. V. 122. № 24. P. 4505–4515.
  65. Binggeli O., Neyen C., Poidevin M., Lemaitre B. // PLoS Pathog. 2014. V. 10. № 5. P. e1004067.
  66. Dudzic J.P., Kondo S., Ueda R., Bergman C.M., Lemaitre B. // BMC Biol. 2015. V. 13. P. 81.
  67. Tang H., Kambris Z., Lemaitre B., Hashimoto C. // J. Biol. Chem. 2006. V. 281. № 38. P. 28097–28104.
  68. Nam H.J., Jang I.H., You H., Lee K.A., Lee W.J. // EMBO J. 2012. V. 31. № 5. P. 1253–1265.
  69. Nappi A.J., Vass E., Frey F., Carton Y. // Eur. J. Cell. Biol. 1995. V. 68. № 4. P. 450–456.
  70. Ramet M., Manfruelli P., Pearson A., Mathey-Prevot B., Ezekowitz R.A. // Nature. 2002. V. 416. № 6881. P. 644–648.
  71. Galko M.J., Krasnow M.A. // PLoS Biol. 2004. V. 2. № 8. P. E239.
  72. Neyen C., Binggeli O., Roversi P., Bertin L., Sleiman M.B., Lemaitre B. // Dev. Comp. Immunol. 2015. V. 50. № 2. P. 166–174.
  73. Rizki T.M., Rizki R.M. // Dev. Comp. Immunol. 1992. V. 16. № 2–3. P. 103–110.
  74. Shrestha R., Gateff E. // Development, Growth and Differentiation. 1982. V. 24. № 1. P. 83–98.
  75. Anderl I., Vesala L., Ihalainen T.O., Vanha-Aho L.M., Ando I., Ramet M., Hultmark D. // PLoS Pathog. 2016. V. 12. № 7. P. e1005746.
  76. Nam H.J., Jang I.H., Asano T., Lee W.J. // Mol. Cells. 2008. V. 26. № 6. P. 606–610.
  77. Honti V., Kurucz E., Csordas G., Laurinyecz B., Markus R., Ando I. // Immunol. Lett. 2009. V. 126. № 1–2. P. 83–84.
  78. Tokusumi T., Shoue D.A., Tokusumi Y., Stoller J.R., Schulz R.A. // Genesis. 2009. V. 47. № 11. P. 771–774.
  79. Evans C.J., Liu T., Banerjee U. // Methods. 2014. V. 68. № 1. P. 242–251.
  80. Rus F., Kurucz E., Markus R., Sinenko S.A., Laurinyecz B., Pataki C., Gausz J., Hegedus Z., Udvardy A., Hultmark D., et al. // Gene Expr. Patterns. 2006. V. 6. № 8. P. 928–934.
  81. Sinenko S.A., Mathey-Prevot B. // Oncogene. 2004. V. 23. № 56. P. 9120–9128.
  82. Semenova N.Y., Bessmel’tsev S.S., Rugal’ V.I. // Klin. Onkogematol. 2014. V. 7. № 4. P. 501–510.
  83. Charbord P., Pouget C., Binder H., Dumont F., Stik G., Levy P., Allain F., Marchal C., Richter J., Uzan B., et al. // Cell Stem Cell. 2014. V. 15. № 3. P. 376–391.
  84. Belyavsky A., Petinati N., Drize N. // Int. J. Mol. Sci. 2021. V. 22. № 17. P. 9231.
  85. Comazzetto S., Shen B., Morrison S. J. // Dev. Cell. 2021. V. 56. № 13. P. 1848–1860.
  86. Morrison S.J., Spradling A.C. // Cell. 2008. V. 132. № 4. P. 598–611.
  87. Fuller M.T., Spradling A.C. // Science. 2007. V. 316. № 5823. P. 402–404.
  88. Homem C.C., Knoblich J.A. // Development. 2012. V. 139. № 23. P. 4297–4310.
  89. Micchelli C.A., Perrimon N. // Nature. 2006. V. 439. № 7075. P. 475–479.
  90. Minakhina S., Steward R. // Development. 2010. V. 137. № 1. P. 27–31.
  91. Dey N.S., Ramesh P., Chugh M., Mandal S., Mandal L. // Elife. 2016. V. 5. P. e18295.
  92. Ho K.Y.L., Carr R.L., Dvoskin A.D., Tanentzapf G. // Elife. 2023. V. 12. P. e84085.
  93. Girard J.R., Goins L.M., Vuu D.M., Sharpley M.S., Spratford C.M., Mantri S.R., Banerjee U. // Elife. 2021. V. 10. P. e67516.
  94. Mandal L., Banerjee U., Hartenstein V. // Nat. Genet. 2004. V. 36. № 9. P. 1019–1023.
  95. Medvinsky A., Dzierzak E. // Cell. 1996. V. 86. № 6. P. 897–906.
  96. Mandal L., Martinez-Agosto J.A., Evans C.J., Hartenstein V., Banerjee U. // Nature. 2007. V. 446. № 7133. P. 320–324.
  97. Crozatier M., Ubeda J.M., Vincent A., Meister M. // PLoS Biol. 2004. V. 2. № 8. P. E196.
  98. Rodrigues D., Renaud Y., VijayRaghavan K., Waltzer L., Inamdar M. S. // Elife. 2021. V. 10. P. e61409.
  99. Sinenko S.A., Mandal L., Martinez-Agosto J.A., Banerjee U. // Dev. Cell. 2009. V. 16. № 5. P. 756–763.
  100. Owusu-Ansah E., Banerjee U. // Nature. 2009. V. 461. № 7263. P. 537–541.
  101. Crozatier M., Meister M. // Cell. Microbiol. 2007. V. 9. № 5. P. 1117–1126.
  102. Krzemien J., Dubois L., Makki R., Meister M., Vincent A., Crozatier M. // Nature. 2007. V. 446. № 7133. P. 325–328.
  103. Mondal B.C., Mukherjee T., Mandal L., Evans C.J., Sinenko S.A., Martinez-Agosto J. A., Banerjee U. // Cell. 2011. V. 147. № 7. P. 1589–1600.
  104. Tokusumi Y., Tokusumi T., Shoue D.A., Schulz R.A. // PLoS One. 2012. V. 7. № 7. P. e41604.
  105. Lebestky T., Jung S.H., Banerjee U. // Genes Dev. 2003. V. 17. № 3. P. 348–353.
  106. Krzemien J., Oyallon J., Crozatier M., Vincent A. // Dev. Biol. 2010. V. 346. № 2. P. 310–319.
  107. Mohammad K., Dakik P., Medkour Y., Mitrofanova D., Titorenko V.I. // Int. J. Mol. Sci. 2019. V. 20. № 9. P. 2158.
  108. Hombria J.C., Brown S., Hader S., Zeidler M.P. // Dev. Biol. 2005. V. 288. № 2. P. 420–433.
  109. Benmimoun B., Polesello C., Haenlin M., Waltzer L. // Proc. Natl. Acad. Sci. USA. 2015. V. 112. № 29. P. 9052–9057.
  110. Oyallon J., Vanzo N., Krzemien J., Morin-Poulard I., Vincent A., Crozatier M. // PLoS One. 2016. V. 11. № 2. P. e0148978.
  111. Grigorian M., Liu T., Banerjee U., Hartenstein V. // Dev. Biol. 2013. V. 384. № 2. P. 301–312.
  112. Makhijani K., Alexander B., Tanaka T., Rulifson E., Bruckner K. // Development. 2011. V. 138. № 24. P. 5379–5391.
  113. Goto A., Kadowaki T., Kitagawa Y. // Dev. Biol. 2003. V. 264. № 2. P. 582–591.
  114. Mukherjee T., Kim W. S., Mandal L., Banerjee U. // Science. 2011. V. 332. № 6034. P. 1210–1213.
  115. Terriente-Felix A., Li J., Collins S., Mulligan A., Reekie I., Bernard F., Krejci A., Bray S. // Development. 2013. V. 140. № 4. P. 926–937.
  116. Lebestky T., Chang T., Hartenstein V., Banerjee U. // Science. 2000. V. 288. № 5463. P. 146–149.
  117. Tokusumi T., Sorrentino R.P., Russell M., Ferrarese R., Govind S., Schulz R. A. // PLoS One. 2009. V. 4. № 7. P. e6429.
  118. Spratford C.M., Goins L.M., Chi F., Girard J.R., Macias S.N., Ho V.W., Banerjee U. // Development. 2021. V. 148. № 24. P. 200216.
  119. Ferguson G.B., Martinez-Agosto J.A. // Dev. Biol. 2017. V. 425. № 1. P. 21–32.
  120. Shim J., Mukherjee T., Mondal B.C., Liu T., Young G.C., Wijewarnasuriya D.P., Banerjee U. // Cell. 2013. V. 155. № 5. P. 1141–1153.
  121. Baldeosingh R., Gao H., Wu X., Fossett N. // Dev. Biol. 2018. V. 441. № 1. P. 132–145.
  122. Benmimoun B., Polesello C., Waltzer L., Haenlin M. // Development. 2012. V. 139. № 10. P. 1713–1717.
  123. Pennetier D., Oyallon J., Morin-Poulard I., Dejean S., Vincent A., Crozatier M. // Proc. Natl. Acad. Sci. USA. 2012. V. 109. № 9. P. 3389–3394.
  124. Khadilkar R.J., Rodrigues D., Mote R.D., Sinha A.R., Kulkarni V., Magadi S.S., Inamdar M.S. // Proc. Natl. Acad. Sci. USA. 2014. V. 111. № 13. P. 4898–4903.
  125. Destalminil-Letourneau M., Morin-Poulard I., Tian Y., Vanzo N., Crozatier M. // Elife. 2021. V. 10. P. e64672.
  126. Morin-Poulard I., Sharma A., Louradour I., Vanzo N., Vincent A., Crozatier M. // Nat. Commun. 2016. V. 7. P. 11634.
  127. Ramesh P., Dey N. S., Kanwal A., Mandal S., Mandal L. // Elife. 2021. V. 10. P. e67158.
  128. Ho K.Y.L., An K., Carr R.L., Dvoskin A.D., Ou A.Y.J., Vogl W., Tanentzapf G. // Proc. Natl. Acad. Sci. USA. 2023. V. 120. № 45. P. e2303018120.
  129. Sinenko S.A., Shim J., Banerjee U. // EMBO Rep. 2012. V. 13. № 1. P. 83–89.
  130. Louradour I., Sharma A., Morin-Poulard I., Letourneau M., Vincent A., Crozatier M., Vanzo N. // Elife. 2017. V. 6. P. e25496.
  131. Gao H., Wu X., Fossett N. // Molecular and Cellular Biology. 2009. V. 29. № 22. P. 6086–6096.
  132. Zhang C.U., Cadigan K.M. // Development. 2017. V. 144. № 13. P. 2415–2427.
  133. Zhang C.U., Blauwkamp T.A., Burby P.E., Cadigan K.M. // PLoS Genet. 2014. V. 10. № 8. P. e1004509.
  134. Goins L.M., Girard J.R., Mondal B.C., Buran S., Su C.C., Tang R., Biswas T., Banerjee U. // bioRxiv. 2023. 10.1101/2023.06.29.547151. P. 2023.2006.2029.547151.
  135. Dragojlovic-Munther M., Martinez-Agosto J.A. // Dev. Biol. 2013. V. 384. № 2. P. 313–330.
  136. Zhang W., Wang D., Si J., Jin L. H., Hao Y. // Cells. 2023. V. 12. № 4. P. 661.
  137. Makki R., Meister M., Pennetier D., Ubeda J.M., Braun A., Daburon V., Krzemien J., Bourbon H.M., Zhou R., Vincent A., et al. // PLoS Biol. 2010. V. 8. № 8. P. e1000441.
  138. Flaherty M.S., Salis P., Evans C. J., Ekas L. A., Marouf A., Zavadil J., Banerjee U., Bach E.A. // Dev. Cell. 2010. V. 18. № 4. P. 556–568.
  139. Minakhina S., Tan W., Steward R. // Dev. Biol. 2011. V. 352. № 2. P. 308–316.
  140. Gao H., Wu X., Fossett N. // PLoS One. 2013. V. 8. № 9. P. e74684.
  141. Kulkarni V., Khadilkar R.J., Magadi S.S., Inamdar M.S. // PLoS One. 2011. V. 6. № 11. P. e27667.
  142. Sinha A., Khadilkar R.J., S V.K., Roychowdhury Sinha A., Inamdar M. S. // Cell Rep. 2013. V. 4. № 4. P. 649–658.
  143. Sinenko S.A., Starkova T.Y., Kuzmin A.A., Tomilin A.N. // Front. Cell Dev. Biol. 2021. V. 9. P. 714370.
  144. Lennicke C., Cocheme H.M. // Mol. Cell. 2021. V. 81. № 18. P. 3691–3707.
  145. Gao H., Wu X., Simon L., Fossett N. // PLoS One. 2014. V. 9. № 9. P. e107768.
  146. Cho B., Shin M., Chang E., Son S., Shin I., Shim J. // Dev. Cell. 2024. V. 59. № 8. P. 1075–1090.
  147. Dolezal T., Dolezelova E., Zurovec M., Bryant P. J. // PLoS Biol. 2005. V. 3. № 7. P. e201.
  148. Bajgar A., Dolezal T. // PLoS Pathog. 2018. V. 14. № 4. P. e1007022.
  149. Belenkaya T.Y., Han C., Yan D., Opoka R.J., Khodoun M., Liu H., Lin X. // Cell. 2004. V. 119. № 2. P. 231–244.
  150. Hao Y., Jin L.H. // Elife. 2017. V. 6. P. e25094.
  151. Khadilkar R.J., Vogl W., Goodwin K., Tanentzapf G. // Elife. 2017. V. 6. P. e28081.
  152. Labrosse C., Eslin P., Doury G., Drezen J.M., Poirie M. // J. Insect Physiol. 2005. V. 51. № 2. P. 161–170.
  153. Nassel D.R., Liu Y., Luo J. // Gen. Comp. Endocrinol. 2015. V. 221. P. 255–266.
  154. Dragojlovic-Munther M., Martinez-Agosto J.A. // Development. 2012. V. 139. № 20. P. 3752–3763.

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