RNA interference in Lepidoptera: An overview of successful and unsuccessful studies and implications for experimental design

Olle Terenius; Alexie Papanicolaou; Jennie S. Garbutt; Ioannis Eleftherianos; Hanneke Huvenne; Sriramana Kanginakudru; Merete Albrechtsen; Chunju An; Jean Luc Aymeric; Andrea Barthel; Piotr Bebas; Kavita Bitra; Alejandra Bravo; François Chevalier; Derek P. Collinge; Cristina M. Crava; Ruud A. de Maagd; Bernard Duvic; Martin Erlandson; Ingrid Faye; Gabriella Felföldi; Haruhiko Fujiwara; Ryo Futahashi; Archana S. Gandhe; Heather S. Gatehouse; Laurence N. Gatehouse; Jadwiga M. Giebultowicz; Isabel Gómez; Cornelis J.P. Grimmelikhuijzen; Astrid T. Groot; Frank Hauser; David G. Heckel; Dwayne D. Hegedus; Steven Hrycaj; Lihua Huang; J. Joe Hull; Kostas Iatrou; Masatoshi Iga; Michael R. Kanost; Joanna Kotwica; Changyou Li; Jianghong Li; Jisheng Liu; Magnus Lundmark; Shogo Matsumoto; Martina Meyering-Vos; Peter J. Millichap; Antónia Monteiro; Nirotpal Mrinal; Teruyuki Niimi; Daniela Nowara; Atsushi Ohnishi; Vicencio Oostra; Katsuhisa Ozaki; Maria Papakonstantinou; Aleksandar Popadic; Manchikatla V. Rajam; Suzanne Saenko; Robert M. Simpson; Mario Soberón; Michael R. Strand; Shuichiro Tomita; Umut Toprak; Ping Wang; Choon Wei Wee; Steven Whyard; Wenqing Zhang; Javaregowda Nagaraju; Richard H. ffrench-Constant; Salvador Herrero; Karl Gordon; Luc Swevers; Guy Smagghe

doi:10.1016/j.jinsphys.2010.11.006

RNA interference in Lepidoptera: An overview of successful and unsuccessful studies and implications for experimental design

Olle Terenius^*, Alexie Papanicolaou, Jennie S. Garbutt, Ioannis Eleftherianos, Hanneke Huvenne, Sriramana Kanginakudru, Merete Albrechtsen, Chunju An, Jean Luc Aymeric, Andrea Barthel, Piotr Bebas, Kavita Bitra, Alejandra Bravo, François Chevalier, Derek P. Collinge, Cristina M. Crava, Ruud A. de Maagd, Bernard Duvic, Martin Erlandson, Ingrid FayeGabriella Felföldi, Haruhiko Fujiwara, Ryo Futahashi, Archana S. Gandhe, Heather S. Gatehouse, Laurence N. Gatehouse, Jadwiga M. Giebultowicz, Isabel Gómez, Cornelis J.P. Grimmelikhuijzen, Astrid T. Groot, Frank Hauser, David G. Heckel, Dwayne D. Hegedus, Steven Hrycaj, Lihua Huang, J. Joe Hull, Kostas Iatrou, Masatoshi Iga, Michael R. Kanost, Joanna Kotwica, Changyou Li, Jianghong Li, Jisheng Liu, Magnus Lundmark, Shogo Matsumoto, Martina Meyering-Vos, Peter J. Millichap, Antónia Monteiro, Nirotpal Mrinal, Teruyuki Niimi, Daniela Nowara, Atsushi Ohnishi, Vicencio Oostra, Katsuhisa Ozaki, Maria Papakonstantinou, Aleksandar Popadic, Manchikatla V. Rajam, Suzanne Saenko, Robert M. Simpson, Mario Soberón, Michael R. Strand, Shuichiro Tomita, Umut Toprak, Ping Wang, Choon Wei Wee, Steven Whyard, Wenqing Zhang, Javaregowda Nagaraju, Richard H. ffrench-Constant, Salvador Herrero, Karl Gordon, Luc Swevers, Guy Smagghe

^*Corresponding author for this work

Research output: Contribution to journal › Review article › peer-review

701 Citations (Scopus)

Abstract

Gene silencing through RNA interference (RNAi) has revolutionized the study of gene function, particularly in non-model insects. However, in Lepidoptera (moths and butterflies) RNAi has many times proven to be difficult to achieve. Most of the negative results have been anecdotal and the positive experiments have not been collected in such a way that they are possible to analyze. In this review, we have collected detailed data from more than 150 experiments including all to date published and many unpublished experiments. Despite a large variation in the data, trends that are found are that RNAi is particularly successful in the family Saturniidae and in genes involved in immunity. On the contrary, gene expression in epidermal tissues seems to be most difficult to silence. In addition, gene silencing by feeding dsRNA requires high concentrations for success. Possible causes for the variability of success in RNAi experiments in Lepidoptera are discussed. The review also points to a need to further investigate the mechanism of RNAi in lepidopteran insects and its possible connection to the innate immune response. Our general understanding of RNAi in Lepidoptera will be further aided in the future as our public database at http://insectacentral.org/RNAi will continue to gather information on RNAi experiments.

Original language	English
Pages (from-to)	231-245
Number of pages	15
Journal	Journal of Insect Physiology
Volume	57
Issue number	2
DOIs	https://doi.org/10.1016/j.jinsphys.2010.11.006
Publication status	Published - Feb 2011

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10.1016/j.jinsphys.2010.11.006

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Terenius, O., Papanicolaou, A., Garbutt, J. S., Eleftherianos, I., Huvenne, H., Kanginakudru, S., Albrechtsen, M., An, C., Aymeric, J. L., Barthel, A., Bebas, P., Bitra, K., Bravo, A., Chevalier, F., Collinge, D. P., Crava, C. M., de Maagd, R. A., Duvic, B., Erlandson, M., ... Smagghe, G. (2011). RNA interference in Lepidoptera: An overview of successful and unsuccessful studies and implications for experimental design. Journal of Insect Physiology, 57(2), 231-245. https://doi.org/10.1016/j.jinsphys.2010.11.006

@article{12517b3a98fd4c00b205d8e55373f00e,

title = "RNA interference in Lepidoptera: An overview of successful and unsuccessful studies and implications for experimental design",

abstract = "Gene silencing through RNA interference (RNAi) has revolutionized the study of gene function, particularly in non-model insects. However, in Lepidoptera (moths and butterflies) RNAi has many times proven to be difficult to achieve. Most of the negative results have been anecdotal and the positive experiments have not been collected in such a way that they are possible to analyze. In this review, we have collected detailed data from more than 150 experiments including all to date published and many unpublished experiments. Despite a large variation in the data, trends that are found are that RNAi is particularly successful in the family Saturniidae and in genes involved in immunity. On the contrary, gene expression in epidermal tissues seems to be most difficult to silence. In addition, gene silencing by feeding dsRNA requires high concentrations for success. Possible causes for the variability of success in RNAi experiments in Lepidoptera are discussed. The review also points to a need to further investigate the mechanism of RNAi in lepidopteran insects and its possible connection to the innate immune response. Our general understanding of RNAi in Lepidoptera will be further aided in the future as our public database at http://insectacentral.org/RNAi will continue to gather information on RNAi experiments.",

keywords = "Delivery methods, DsRNA properties, Gene function, Lepidoptera, RNA interference, Tissue uptake",

author = "Olle Terenius and Alexie Papanicolaou and Garbutt, {Jennie S.} and Ioannis Eleftherianos and Hanneke Huvenne and Sriramana Kanginakudru and Merete Albrechtsen and Chunju An and Aymeric, {Jean Luc} and Andrea Barthel and Piotr Bebas and Kavita Bitra and Alejandra Bravo and Fran{\c c}ois Chevalier and Collinge, {Derek P.} and Crava, {Cristina M.} and {de Maagd}, {Ruud A.} and Bernard Duvic and Martin Erlandson and Ingrid Faye and Gabriella Felf{\"o}ldi and Haruhiko Fujiwara and Ryo Futahashi and Gandhe, {Archana S.} and Gatehouse, {Heather S.} and Gatehouse, {Laurence N.} and Giebultowicz, {Jadwiga M.} and Isabel G{\'o}mez and Grimmelikhuijzen, {Cornelis J.P.} and Groot, {Astrid T.} and Frank Hauser and Heckel, {David G.} and Hegedus, {Dwayne D.} and Steven Hrycaj and Lihua Huang and Hull, {J. Joe} and Kostas Iatrou and Masatoshi Iga and Kanost, {Michael R.} and Joanna Kotwica and Changyou Li and Jianghong Li and Jisheng Liu and Magnus Lundmark and Shogo Matsumoto and Martina Meyering-Vos and Millichap, {Peter J.} and Ant{\'o}nia Monteiro and Nirotpal Mrinal and Teruyuki Niimi and Daniela Nowara and Atsushi Ohnishi and Vicencio Oostra and Katsuhisa Ozaki and Maria Papakonstantinou and Aleksandar Popadic and Rajam, {Manchikatla V.} and Suzanne Saenko and Simpson, {Robert M.} and Mario Sober{\'o}n and Strand, {Michael R.} and Shuichiro Tomita and Umut Toprak and Ping Wang and Wee, {Choon Wei} and Steven Whyard and Wenqing Zhang and Javaregowda Nagaraju and ffrench-Constant, {Richard H.} and Salvador Herrero and Karl Gordon and Luc Swevers and Guy Smagghe",

year = "2011",

month = feb,

doi = "10.1016/j.jinsphys.2010.11.006",

language = "English",

volume = "57",

pages = "231--245",

journal = "Journal of Insect Physiology",

issn = "0022-1910",

publisher = "Elsevier Ltd.",

number = "2",

}

Terenius, O, Papanicolaou, A, Garbutt, JS, Eleftherianos, I, Huvenne, H, Kanginakudru, S, Albrechtsen, M, An, C, Aymeric, JL, Barthel, A, Bebas, P, Bitra, K, Bravo, A, Chevalier, F, Collinge, DP, Crava, CM, de Maagd, RA, Duvic, B, Erlandson, M, Faye, I, Felföldi, G, Fujiwara, H, Futahashi, R, Gandhe, AS, Gatehouse, HS, Gatehouse, LN, Giebultowicz, JM, Gómez, I, Grimmelikhuijzen, CJP, Groot, AT, Hauser, F, Heckel, DG, Hegedus, DD, Hrycaj, S, Huang, L, Hull, JJ, Iatrou, K, Iga, M, Kanost, MR, Kotwica, J, Li, C, Li, J, Liu, J, Lundmark, M, Matsumoto, S, Meyering-Vos, M, Millichap, PJ, Monteiro, A, Mrinal, N, Niimi, T, Nowara, D, Ohnishi, A, Oostra, V, Ozaki, K, Papakonstantinou, M, Popadic, A, Rajam, MV, Saenko, S, Simpson, RM, Soberón, M, Strand, MR, Tomita, S, Toprak, U, Wang, P, Wee, CW, Whyard, S, Zhang, W, Nagaraju, J, ffrench-Constant, RH, Herrero, S, Gordon, K, Swevers, L & Smagghe, G 2011, 'RNA interference in Lepidoptera: An overview of successful and unsuccessful studies and implications for experimental design', Journal of Insect Physiology, vol. 57, no. 2, pp. 231-245. https://doi.org/10.1016/j.jinsphys.2010.11.006

TY - JOUR

T1 - RNA interference in Lepidoptera

T2 - An overview of successful and unsuccessful studies and implications for experimental design

AU - Terenius, Olle

AU - Papanicolaou, Alexie

AU - Garbutt, Jennie S.

AU - Eleftherianos, Ioannis

AU - Huvenne, Hanneke

AU - Kanginakudru, Sriramana

AU - Albrechtsen, Merete

AU - An, Chunju

AU - Aymeric, Jean Luc

AU - Barthel, Andrea

AU - Bebas, Piotr

AU - Bitra, Kavita

AU - Bravo, Alejandra

AU - Chevalier, François

AU - Collinge, Derek P.

AU - Crava, Cristina M.

AU - de Maagd, Ruud A.

AU - Duvic, Bernard

AU - Erlandson, Martin

AU - Faye, Ingrid

AU - Felföldi, Gabriella

AU - Fujiwara, Haruhiko

AU - Futahashi, Ryo

AU - Gandhe, Archana S.

AU - Gatehouse, Heather S.

AU - Gatehouse, Laurence N.

AU - Giebultowicz, Jadwiga M.

AU - Gómez, Isabel

AU - Grimmelikhuijzen, Cornelis J.P.

AU - Groot, Astrid T.

AU - Hauser, Frank

AU - Heckel, David G.

AU - Hegedus, Dwayne D.

AU - Hrycaj, Steven

AU - Huang, Lihua

AU - Hull, J. Joe

AU - Iatrou, Kostas

AU - Iga, Masatoshi

AU - Kanost, Michael R.

AU - Kotwica, Joanna

AU - Li, Changyou

AU - Li, Jianghong

AU - Liu, Jisheng

AU - Lundmark, Magnus

AU - Matsumoto, Shogo

AU - Meyering-Vos, Martina

AU - Millichap, Peter J.

AU - Monteiro, Antónia

AU - Mrinal, Nirotpal

AU - Niimi, Teruyuki

AU - Nowara, Daniela

AU - Ohnishi, Atsushi

AU - Oostra, Vicencio

AU - Ozaki, Katsuhisa

AU - Papakonstantinou, Maria

AU - Popadic, Aleksandar

AU - Rajam, Manchikatla V.

AU - Saenko, Suzanne

AU - Simpson, Robert M.

AU - Soberón, Mario

AU - Strand, Michael R.

AU - Tomita, Shuichiro

AU - Toprak, Umut

AU - Wang, Ping

AU - Wee, Choon Wei

AU - Whyard, Steven

AU - Zhang, Wenqing

AU - Nagaraju, Javaregowda

AU - ffrench-Constant, Richard H.

AU - Herrero, Salvador

AU - Gordon, Karl

AU - Swevers, Luc

AU - Smagghe, Guy

PY - 2011/2

Y1 - 2011/2

N2 - Gene silencing through RNA interference (RNAi) has revolutionized the study of gene function, particularly in non-model insects. However, in Lepidoptera (moths and butterflies) RNAi has many times proven to be difficult to achieve. Most of the negative results have been anecdotal and the positive experiments have not been collected in such a way that they are possible to analyze. In this review, we have collected detailed data from more than 150 experiments including all to date published and many unpublished experiments. Despite a large variation in the data, trends that are found are that RNAi is particularly successful in the family Saturniidae and in genes involved in immunity. On the contrary, gene expression in epidermal tissues seems to be most difficult to silence. In addition, gene silencing by feeding dsRNA requires high concentrations for success. Possible causes for the variability of success in RNAi experiments in Lepidoptera are discussed. The review also points to a need to further investigate the mechanism of RNAi in lepidopteran insects and its possible connection to the innate immune response. Our general understanding of RNAi in Lepidoptera will be further aided in the future as our public database at http://insectacentral.org/RNAi will continue to gather information on RNAi experiments.

AB - Gene silencing through RNA interference (RNAi) has revolutionized the study of gene function, particularly in non-model insects. However, in Lepidoptera (moths and butterflies) RNAi has many times proven to be difficult to achieve. Most of the negative results have been anecdotal and the positive experiments have not been collected in such a way that they are possible to analyze. In this review, we have collected detailed data from more than 150 experiments including all to date published and many unpublished experiments. Despite a large variation in the data, trends that are found are that RNAi is particularly successful in the family Saturniidae and in genes involved in immunity. On the contrary, gene expression in epidermal tissues seems to be most difficult to silence. In addition, gene silencing by feeding dsRNA requires high concentrations for success. Possible causes for the variability of success in RNAi experiments in Lepidoptera are discussed. The review also points to a need to further investigate the mechanism of RNAi in lepidopteran insects and its possible connection to the innate immune response. Our general understanding of RNAi in Lepidoptera will be further aided in the future as our public database at http://insectacentral.org/RNAi will continue to gather information on RNAi experiments.

KW - Delivery methods

KW - DsRNA properties

KW - Gene function

KW - Lepidoptera

KW - RNA interference

KW - Tissue uptake

UR - http://www.scopus.com/inward/record.url?scp=78651424115&partnerID=8YFLogxK

U2 - 10.1016/j.jinsphys.2010.11.006

DO - 10.1016/j.jinsphys.2010.11.006

M3 - Review article

SN - 0022-1910

VL - 57

SP - 231

EP - 245

JO - Journal of Insect Physiology

JF - Journal of Insect Physiology

IS - 2

ER -

RNA interference in Lepidoptera: An overview of successful and unsuccessful studies and implications for experimental design

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