---
_id: '10713'
abstract:
- lang: eng
  text: Cells migrate through crowded microenvironments within tissues during normal
    development, immune response, and cancer metastasis. Although migration through
    pores and tracks in the extracellular matrix (ECM) has been well studied, little
    is known about cellular traversal into confining cell-dense tissues. We find that
    embryonic tissue invasion by Drosophila macrophages requires division of an epithelial
    ectodermal cell at the site of entry. Dividing ectodermal cells disassemble ECM
    attachment formed by integrin-mediated focal adhesions next to mesodermal cells,
    allowing macrophages to move their nuclei ahead and invade between two immediately
    adjacent tissues. Invasion efficiency depends on division frequency, but reduction
    of adhesion strength allows macrophage entry independently of division. This work
    demonstrates that tissue dynamics can regulate cellular infiltration.
acknowledged_ssus:
- _id: Bio
acknowledgement: 'We thank J. Friml, C. Guet, T. Hurd, M. Fendrych and members of
  the laboratory for comments on the manuscript; the Bioimaging Facility of IST Austria
  for excellent support and T. Lecuit, E. Hafen, R. Levayer and A. Martin for fly
  strains. This work was supported by a grant from the Austrian Science Fund FWF:
  Lise Meitner Fellowship M2379-B28 to M.A and D.S., and internal funding from IST
  Austria to D.S. and EMBL to S.D.R.'
article_processing_charge: No
article_type: original
author:
- first_name: Maria
  full_name: Akhmanova, Maria
  id: 3425EC26-F248-11E8-B48F-1D18A9856A87
  last_name: Akhmanova
  orcid: 0000-0003-1522-3162
- first_name: Shamsi
  full_name: Emtenani, Shamsi
  id: 49D32318-F248-11E8-B48F-1D18A9856A87
  last_name: Emtenani
  orcid: 0000-0001-6981-6938
- first_name: Daniel
  full_name: Krueger, Daniel
  last_name: Krueger
- first_name: Attila
  full_name: György, Attila
  id: 3BCEDBE0-F248-11E8-B48F-1D18A9856A87
  last_name: György
  orcid: 0000-0002-1819-198X
- first_name: Mariana
  full_name: Pereira Guarda, Mariana
  id: 6de81d9d-e2f2-11eb-945a-af8bc2a60b26
  last_name: Pereira Guarda
- first_name: Mikhail
  full_name: Vlasov, Mikhail
  last_name: Vlasov
- first_name: Fedor
  full_name: Vlasov, Fedor
  last_name: Vlasov
- first_name: Andrei
  full_name: Akopian, Andrei
  last_name: Akopian
- first_name: Aparna
  full_name: Ratheesh, Aparna
  id: 2F064CFE-F248-11E8-B48F-1D18A9856A87
  last_name: Ratheesh
- first_name: Stefano
  full_name: De Renzis, Stefano
  last_name: De Renzis
- first_name: Daria E
  full_name: Siekhaus, Daria E
  id: 3D224B9E-F248-11E8-B48F-1D18A9856A87
  last_name: Siekhaus
  orcid: 0000-0001-8323-8353
citation:
  ama: Akhmanova M, Emtenani S, Krueger D, et al. Cell division in tissues enables
    macrophage infiltration. <i>Science</i>. 2022;376(6591):394-396. doi:<a href="https://doi.org/10.1126/science.abj0425">10.1126/science.abj0425</a>
  apa: Akhmanova, M., Emtenani, S., Krueger, D., György, A., Pereira Guarda, M., Vlasov,
    M., … Siekhaus, D. E. (2022). Cell division in tissues enables macrophage infiltration.
    <i>Science</i>. American Association for the Advancement of Science. <a href="https://doi.org/10.1126/science.abj0425">https://doi.org/10.1126/science.abj0425</a>
  chicago: Akhmanova, Maria, Shamsi Emtenani, Daniel Krueger, Attila György, Mariana
    Pereira Guarda, Mikhail Vlasov, Fedor Vlasov, et al. “Cell Division in Tissues
    Enables Macrophage Infiltration.” <i>Science</i>. American Association for the
    Advancement of Science, 2022. <a href="https://doi.org/10.1126/science.abj0425">https://doi.org/10.1126/science.abj0425</a>.
  ieee: M. Akhmanova <i>et al.</i>, “Cell division in tissues enables macrophage infiltration,”
    <i>Science</i>, vol. 376, no. 6591. American Association for the Advancement of
    Science, pp. 394–396, 2022.
  ista: Akhmanova M, Emtenani S, Krueger D, György A, Pereira Guarda M, Vlasov M,
    Vlasov F, Akopian A, Ratheesh A, De Renzis S, Siekhaus DE. 2022. Cell division
    in tissues enables macrophage infiltration. Science. 376(6591), 394–396.
  mla: Akhmanova, Maria, et al. “Cell Division in Tissues Enables Macrophage Infiltration.”
    <i>Science</i>, vol. 376, no. 6591, American Association for the Advancement of
    Science, 2022, pp. 394–96, doi:<a href="https://doi.org/10.1126/science.abj0425">10.1126/science.abj0425</a>.
  short: M. Akhmanova, S. Emtenani, D. Krueger, A. György, M. Pereira Guarda, M. Vlasov,
    F. Vlasov, A. Akopian, A. Ratheesh, S. De Renzis, D.E. Siekhaus, Science 376 (2022)
    394–396.
date_created: 2022-02-01T11:23:18Z
date_published: 2022-04-22T00:00:00Z
date_updated: 2023-08-02T14:06:15Z
day: '22'
department:
- _id: DaSi
doi: 10.1126/science.abj0425
external_id:
  isi:
  - '000788553700039'
  pmid:
  - '35446632'
intvolume: '       376'
isi: 1
issue: '6591'
language:
- iso: eng
license: https://creativecommons.org/licenses/by-nc-nd/4.0/
main_file_link:
- open_access: '1'
  url: https://doi.org/10.1101/2021.04.19.438995
month: '04'
oa: 1
oa_version: Preprint
page: 394-396
pmid: 1
project:
- _id: 264CBBAC-B435-11E9-9278-68D0E5697425
  call_identifier: FWF
  grant_number: M02379
  name: Modeling epithelial tissue mechanics during cell invasion
publication: Science
publication_identifier:
  issn:
  - 0036-8075
publication_status: published
publisher: American Association for the Advancement of Science
quality_controlled: '1'
status: public
title: Cell division in tissues enables macrophage infiltration
tmp:
  image: /images/cc_by_nc_nd.png
  legal_code_url: https://creativecommons.org/licenses/by-nc-nd/4.0/legalcode
  name: Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International
    (CC BY-NC-ND 4.0)
  short: CC BY-NC-ND (4.0)
type: journal_article
user_id: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 376
year: '2022'
...
---
_id: '10918'
abstract:
- lang: eng
  text: Cellular metabolism must adapt to changing demands to enable homeostasis.
    During immune responses or cancer metastasis, cells leading migration into challenging
    environments require an energy boost, but what controls this capacity is unclear.
    Here, we study a previously uncharacterized nuclear protein, Atossa (encoded by
    CG9005), which supports macrophage invasion into the germband of Drosophila by
    controlling cellular metabolism. First, nuclear Atossa increases mRNA levels of
    Porthos, a DEAD-box protein, and of two metabolic enzymes, lysine-α-ketoglutarate
    reductase (LKR/SDH) and NADPH glyoxylate reductase (GR/HPR), thus enhancing mitochondrial
    bioenergetics. Then Porthos supports ribosome assembly and thereby raises the
    translational efficiency of a subset of mRNAs, including those affecting mitochondrial
    functions, the electron transport chain, and metabolism. Mitochondrial respiration
    measurements, metabolomics, and live imaging indicate that Atossa and Porthos
    power up OxPhos and energy production to promote the forging of a path into tissues
    by leading macrophages. Since many crucial physiological responses require increases
    in mitochondrial energy output, this previously undescribed genetic program may
    modulate a wide range of cellular behaviors.
acknowledged_ssus:
- _id: Bio
acknowledgement: "We thank the DGRC (NIH grant 2P40OD010949-10A1) for plasmids, the
  BDSC (NIH grant P40OD018537) and the VDRC for fly stocks, FlyBase for essential
  genomic information, the BDGP in situ database for data (Tomancak et al, 2007),
  the IST Austria Bioimaging facility for support, the VBC Core Facilities for RNA
  sequencing and analysis, and C. Guet, C. Navarro, C. Desplan, T. Lecuit, I. Miguel-Aliaga,
  and Siekhaus group members for comments on the manuscript. The VBCF Metabolomics
  Facility is funded by the City of Vienna through the Vienna Business Agency. This
  work was supported by the Marie Curie CIG 334077/IRTIM (DES), Austrian Science Fund
  (FWF) Lise Meitner Fellowship M2379-B28 (MA and DES), Austrian Science Fund (FWF)
  grant ASI_FWF01_P29638S (DES), NIH/NIGMS (R01GM111779-06 (PR), RO1GM135628-01 (PR),
  European Research Council (ERC) grant no. 677006 “CMIL” (AB), and Natural Sciences
  and Engineering Research Council of Canada\r\n(RGPIN-2019-06766) (TRH). "
article_number: e109049
article_processing_charge: Yes (via OA deal)
article_type: original
author:
- first_name: Shamsi
  full_name: Emtenani, Shamsi
  id: 49D32318-F248-11E8-B48F-1D18A9856A87
  last_name: Emtenani
  orcid: 0000-0001-6981-6938
- first_name: Elliot T
  full_name: Martin, Elliot T
  last_name: Martin
- first_name: Attila
  full_name: György, Attila
  id: 3BCEDBE0-F248-11E8-B48F-1D18A9856A87
  last_name: György
  orcid: 0000-0002-1819-198X
- first_name: Julia
  full_name: Bicher, Julia
  id: 3CCBB46E-F248-11E8-B48F-1D18A9856A87
  last_name: Bicher
- first_name: Jakob-Wendelin
  full_name: Genger, Jakob-Wendelin
  last_name: Genger
- first_name: Thomas
  full_name: Köcher, Thomas
  last_name: Köcher
- first_name: Maria
  full_name: Akhmanova, Maria
  id: 3425EC26-F248-11E8-B48F-1D18A9856A87
  last_name: Akhmanova
  orcid: 0000-0003-1522-3162
- first_name: Mariana
  full_name: Pereira Guarda, Mariana
  id: 6de81d9d-e2f2-11eb-945a-af8bc2a60b26
  last_name: Pereira Guarda
- first_name: Marko
  full_name: Roblek, Marko
  id: 3047D808-F248-11E8-B48F-1D18A9856A87
  last_name: Roblek
  orcid: 0000-0001-9588-1389
- first_name: Andreas
  full_name: Bergthaler, Andreas
  last_name: Bergthaler
- first_name: Thomas R
  full_name: Hurd, Thomas R
  last_name: Hurd
- first_name: Prashanth
  full_name: Rangan, Prashanth
  last_name: Rangan
- first_name: Daria E
  full_name: Siekhaus, Daria E
  id: 3D224B9E-F248-11E8-B48F-1D18A9856A87
  last_name: Siekhaus
  orcid: 0000-0001-8323-8353
citation:
  ama: Emtenani S, Martin ET, György A, et al. Macrophage mitochondrial bioenergetics
    and tissue invasion are boosted by an Atossa-Porthos axis in Drosophila. <i>The
    Embo Journal</i>. 2022;41. doi:<a href="https://doi.org/10.15252/embj.2021109049">10.15252/embj.2021109049</a>
  apa: Emtenani, S., Martin, E. T., György, A., Bicher, J., Genger, J.-W., Köcher,
    T., … Siekhaus, D. E. (2022). Macrophage mitochondrial bioenergetics and tissue
    invasion are boosted by an Atossa-Porthos axis in Drosophila. <i>The Embo Journal</i>.
    Embo Press. <a href="https://doi.org/10.15252/embj.2021109049">https://doi.org/10.15252/embj.2021109049</a>
  chicago: Emtenani, Shamsi, Elliot T Martin, Attila György, Julia Bicher, Jakob-Wendelin
    Genger, Thomas Köcher, Maria Akhmanova, et al. “Macrophage Mitochondrial Bioenergetics
    and Tissue Invasion Are Boosted by an Atossa-Porthos Axis in Drosophila.” <i>The
    Embo Journal</i>. Embo Press, 2022. <a href="https://doi.org/10.15252/embj.2021109049">https://doi.org/10.15252/embj.2021109049</a>.
  ieee: S. Emtenani <i>et al.</i>, “Macrophage mitochondrial bioenergetics and tissue
    invasion are boosted by an Atossa-Porthos axis in Drosophila,” <i>The Embo Journal</i>,
    vol. 41. Embo Press, 2022.
  ista: Emtenani S, Martin ET, György A, Bicher J, Genger J-W, Köcher T, Akhmanova
    M, Pereira Guarda M, Roblek M, Bergthaler A, Hurd TR, Rangan P, Siekhaus DE. 2022.
    Macrophage mitochondrial bioenergetics and tissue invasion are boosted by an Atossa-Porthos
    axis in Drosophila. The Embo Journal. 41, e109049.
  mla: Emtenani, Shamsi, et al. “Macrophage Mitochondrial Bioenergetics and Tissue
    Invasion Are Boosted by an Atossa-Porthos Axis in Drosophila.” <i>The Embo Journal</i>,
    vol. 41, e109049, Embo Press, 2022, doi:<a href="https://doi.org/10.15252/embj.2021109049">10.15252/embj.2021109049</a>.
  short: S. Emtenani, E.T. Martin, A. György, J. Bicher, J.-W. Genger, T. Köcher,
    M. Akhmanova, M. Pereira Guarda, M. Roblek, A. Bergthaler, T.R. Hurd, P. Rangan,
    D.E. Siekhaus, The Embo Journal 41 (2022).
date_created: 2022-03-24T13:23:09Z
date_published: 2022-03-23T00:00:00Z
date_updated: 2023-08-03T06:13:14Z
day: '23'
ddc:
- '570'
department:
- _id: DaSi
- _id: LoSw
doi: 10.15252/embj.2021109049
ec_funded: 1
external_id:
  isi:
  - '000771957000001'
file:
- access_level: open_access
  checksum: dba48580fe0fefaa4c63078d1d2a35df
  content_type: application/pdf
  creator: siekhaus
  date_created: 2022-03-24T13:22:41Z
  date_updated: 2022-03-24T13:22:41Z
  file_id: '10919'
  file_name: Macrophage mitochondrial bioenergetics and tissue invasion are boosted
    by an Atossa-Porthos axis in Drosopila.pdf
  file_size: 4344585
  relation: main_file
file_date_updated: 2022-03-24T13:22:41Z
has_accepted_license: '1'
intvolume: '        41'
isi: 1
language:
- iso: eng
month: '03'
oa: 1
oa_version: Published Version
project:
- _id: 2536F660-B435-11E9-9278-68D0E5697425
  call_identifier: FP7
  grant_number: '334077'
  name: Investigating the role of transporters in invasive migration through junctions
- _id: 264CBBAC-B435-11E9-9278-68D0E5697425
  call_identifier: FWF
  grant_number: M02379
  name: Modeling epithelial tissue mechanics during cell invasion
- _id: 253B6E48-B435-11E9-9278-68D0E5697425
  call_identifier: FWF
  grant_number: P29638
  name: Drosophila TNFa´s Funktion in Immunzellen
publication: The Embo Journal
publication_identifier:
  eissn:
  - 1460-2075
publication_status: published
publisher: Embo Press
quality_controlled: '1'
scopus_import: '1'
status: public
title: Macrophage mitochondrial bioenergetics and tissue invasion are boosted by an
  Atossa-Porthos axis in Drosophila
tmp:
  image: /images/cc_by.png
  legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
  name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
  short: CC BY (4.0)
type: journal_article
user_id: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 41
year: '2022'
...
---
_id: '7180'
abstract:
- lang: eng
  text: Arabidopsis PIN2 protein directs transport of the phytohormone auxin from
    the root tip into the root elongation zone. Variation in hormone transport, which
    depends on a delicate interplay between PIN2 sorting to and from polar plasma
    membrane domains, determines root growth. By employing a constitutively degraded
    version of PIN2, we identify brassinolides as antagonists of PIN2 endocytosis.
    This response does not require de novo protein synthesis, but involves early events
    in canonical brassinolide signaling. Brassinolide-controlled adjustments in PIN2
    sorting and intracellular distribution governs formation of a lateral PIN2 gradient
    in gravistimulated roots, coinciding with adjustments in auxin signaling and directional
    root growth. Strikingly, simulations indicate that PIN2 gradient formation is
    no prerequisite for root bending but rather dampens asymmetric auxin flow and
    signaling. Crosstalk between brassinolide signaling and endocytic PIN2 sorting,
    thus, appears essential for determining the rate of gravity-induced root curvature
    via attenuation of differential cell elongation.
article_number: '5516'
article_processing_charge: No
article_type: original
author:
- first_name: Katarzyna
  full_name: Retzer, Katarzyna
  last_name: Retzer
- first_name: Maria
  full_name: Akhmanova, Maria
  id: 3425EC26-F248-11E8-B48F-1D18A9856A87
  last_name: Akhmanova
  orcid: 0000-0003-1522-3162
- first_name: Nataliia
  full_name: Konstantinova, Nataliia
  last_name: Konstantinova
- first_name: Kateřina
  full_name: Malínská, Kateřina
  last_name: Malínská
- first_name: Johannes
  full_name: Leitner, Johannes
  last_name: Leitner
- first_name: Jan
  full_name: Petrášek, Jan
  last_name: Petrášek
- first_name: Christian
  full_name: Luschnig, Christian
  last_name: Luschnig
citation:
  ama: Retzer K, Akhmanova M, Konstantinova N, et al. Brassinosteroid signaling delimits
    root gravitropism via sorting of the Arabidopsis PIN2 auxin transporter. <i>Nature
    Communications</i>. 2019;10. doi:<a href="https://doi.org/10.1038/s41467-019-13543-1">10.1038/s41467-019-13543-1</a>
  apa: Retzer, K., Akhmanova, M., Konstantinova, N., Malínská, K., Leitner, J., Petrášek,
    J., &#38; Luschnig, C. (2019). Brassinosteroid signaling delimits root gravitropism
    via sorting of the Arabidopsis PIN2 auxin transporter. <i>Nature Communications</i>.
    Springer Nature. <a href="https://doi.org/10.1038/s41467-019-13543-1">https://doi.org/10.1038/s41467-019-13543-1</a>
  chicago: Retzer, Katarzyna, Maria Akhmanova, Nataliia Konstantinova, Kateřina Malínská,
    Johannes Leitner, Jan Petrášek, and Christian Luschnig. “Brassinosteroid Signaling
    Delimits Root Gravitropism via Sorting of the Arabidopsis PIN2 Auxin Transporter.”
    <i>Nature Communications</i>. Springer Nature, 2019. <a href="https://doi.org/10.1038/s41467-019-13543-1">https://doi.org/10.1038/s41467-019-13543-1</a>.
  ieee: K. Retzer <i>et al.</i>, “Brassinosteroid signaling delimits root gravitropism
    via sorting of the Arabidopsis PIN2 auxin transporter,” <i>Nature Communications</i>,
    vol. 10. Springer Nature, 2019.
  ista: Retzer K, Akhmanova M, Konstantinova N, Malínská K, Leitner J, Petrášek J,
    Luschnig C. 2019. Brassinosteroid signaling delimits root gravitropism via sorting
    of the Arabidopsis PIN2 auxin transporter. Nature Communications. 10, 5516.
  mla: Retzer, Katarzyna, et al. “Brassinosteroid Signaling Delimits Root Gravitropism
    via Sorting of the Arabidopsis PIN2 Auxin Transporter.” <i>Nature Communications</i>,
    vol. 10, 5516, Springer Nature, 2019, doi:<a href="https://doi.org/10.1038/s41467-019-13543-1">10.1038/s41467-019-13543-1</a>.
  short: K. Retzer, M. Akhmanova, N. Konstantinova, K. Malínská, J. Leitner, J. Petrášek,
    C. Luschnig, Nature Communications 10 (2019).
date_created: 2019-12-15T23:00:43Z
date_published: 2019-12-01T00:00:00Z
date_updated: 2023-09-06T14:08:21Z
day: '01'
ddc:
- '570'
department:
- _id: DaSi
doi: 10.1038/s41467-019-13543-1
external_id:
  isi:
  - '000500508100001'
  pmid:
  - '31797871'
file:
- access_level: open_access
  checksum: 77e8720a8e0f3091b98159f85be40893
  content_type: application/pdf
  creator: dernst
  date_created: 2019-12-16T07:37:50Z
  date_updated: 2020-07-14T12:47:52Z
  file_id: '7184'
  file_name: 2019_NatureComm_Retzer.pdf
  file_size: 5156533
  relation: main_file
file_date_updated: 2020-07-14T12:47:52Z
has_accepted_license: '1'
intvolume: '        10'
isi: 1
language:
- iso: eng
month: '12'
oa: 1
oa_version: Published Version
pmid: 1
project:
- _id: 264CBBAC-B435-11E9-9278-68D0E5697425
  call_identifier: FWF
  grant_number: M02379
  name: Modeling epithelial tissue mechanics during cell invasion
publication: Nature Communications
publication_identifier:
  eissn:
  - '20411723'
publication_status: published
publisher: Springer Nature
quality_controlled: '1'
scopus_import: '1'
status: public
title: Brassinosteroid signaling delimits root gravitropism via sorting of the Arabidopsis
  PIN2 auxin transporter
tmp:
  image: /images/cc_by.png
  legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
  name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
  short: CC BY (4.0)
type: journal_article
user_id: c635000d-4b10-11ee-a964-aac5a93f6ac1
volume: 10
year: '2019'
...
