Durability of Aligned Microtubules Dependent on Persistence Length Determines Phase Transition and Pattern Formation in Collective Motion

Collective motion is a ubiquitous phenomenon in nature. The collective motion of cytoskeleton filaments results mainly from dynamic collisions and alignments; however, the detailed mechanism of pattern formation still needs to be clarified. In particular, the influence of persistence length, which i...

Full description

Saved in:
Bibliographic Details
Published in:ACS nano Vol. 16; no. 9; pp. 14765 - 14778
Main Authors: Zhou, Hang, Jung, Wonyeong, Farhana, Tamanna Ishrat, Fujimoto, Kazuya, Kim, Taeyoon, Yokokawa, Ryuji
Format: Journal Article
Language:English
Published: United States American Chemical Society 27-09-2022
Subjects:
Online Access:Get full text
Tags: Add Tag
No Tags, Be the first to tag this record!
Abstract Collective motion is a ubiquitous phenomenon in nature. The collective motion of cytoskeleton filaments results mainly from dynamic collisions and alignments; however, the detailed mechanism of pattern formation still needs to be clarified. In particular, the influence of persistence length, which is a measure of filament flexibility, on collective motion is still unclear and lacks experimental verifications although it is likely to directly affect the orientational flexibility of filaments. Here, we investigated the collective motion of microtubules with different persistence lengths using a microtubule–kinesin motility system. We showed that local interactions between microtubules significantly vary depending on their persistence length. We demonstrated that the bundling of microtubules is enhanced by more durable alignment, rather than by greater likelihood of alignment. An agent-based computational model confirmed that the rigidity-dependent durability of microtubule alignment dominates their collective behavior.
AbstractList Collective motion is a ubiquitous phenomenon in nature. The collective motion of cytoskeleton filaments results mainly from dynamic collisions and alignments; however, the detailed mechanism of pattern formation still needs to be clarified. In particular, the influence of persistence length, which is a measure of filament flexibility, on collective motion is still unclear and lacks experimental verifications although it is likely to directly affect the orientational flexibility of filaments. Here, we investigated the collective motion of microtubules with different persistence lengths using a microtubule–kinesin motility system. We showed that local interactions between microtubules significantly vary depending on their persistence length. We demonstrated that the bundling of microtubules is enhanced by more durable alignment, rather than by greater likelihood of alignment. An agent-based computational model confirmed that the rigidity-dependent durability of microtubule alignment dominates their collective behavior.
Author Jung, Wonyeong
Kim, Taeyoon
Fujimoto, Kazuya
Yokokawa, Ryuji
Zhou, Hang
Farhana, Tamanna Ishrat
AuthorAffiliation Department of Micro Engineering
Weldon School of Biomedical Engineering
AuthorAffiliation_xml – name: Department of Micro Engineering
– name: Weldon School of Biomedical Engineering
Author_xml – sequence: 1
  givenname: Hang
  orcidid: 0000-0003-0158-2244
  surname: Zhou
  fullname: Zhou, Hang
  organization: Department of Micro Engineering
– sequence: 2
  givenname: Wonyeong
  surname: Jung
  fullname: Jung, Wonyeong
  organization: Weldon School of Biomedical Engineering
– sequence: 3
  givenname: Tamanna Ishrat
  orcidid: 0000-0001-8445-2642
  surname: Farhana
  fullname: Farhana, Tamanna Ishrat
  organization: Department of Micro Engineering
– sequence: 4
  givenname: Kazuya
  surname: Fujimoto
  fullname: Fujimoto, Kazuya
  organization: Department of Micro Engineering
– sequence: 5
  givenname: Taeyoon
  orcidid: 0000-0002-5588-8532
  surname: Kim
  fullname: Kim, Taeyoon
  organization: Weldon School of Biomedical Engineering
– sequence: 6
  givenname: Ryuji
  orcidid: 0000-0002-6306-2693
  surname: Yokokawa
  fullname: Yokokawa, Ryuji
  email: yokokawa.ryuji.8c@kyoto-u.ac.jp
  organization: Department of Micro Engineering
BackLink https://www.ncbi.nlm.nih.gov/pubmed/36098647$$D View this record in MEDLINE/PubMed
BookMark eNp1kE1LxDAQhoMofp-9SY6CrCZpm7ZH2fULVtyDgreSpFONtJM1SQV_gv_a6K7ePM0wed4X8uyRTXQIhBxxdsaZ4OfKBFTozoRhRVFnG2SX15mcsEo-bf7tBd8heyG8MlaUVSm3yU4mWV3JvNwln7PRK217Gz-o6-hFb58RWnpnjXdx1GMPgc5gCdgCRuqQLsAHGyKgAToHfI4v6T2CHywmdPGiAtAHrzDYaBOusKULFROA9Mr5Qf1cLdKp63sw0b4DvXPfxwOy1ak-wOF67pPHq8uH6c1kfn99O72YT1TOqzipmSk0g7KWotWlEbkUBqqs6mRpCiMybVoDqu4qwXPG6kKYWncyIVybUug82ycnq96ld28jhNgMNhjoe4XgxtCIMgVlnuwm9HyFJhkheOiapbeD8h8NZ823_2btv1n7T4njdfmoB2j_-F_hCThdASnZvLrRY_rrv3VfMU2V7A
CitedBy_id crossref_primary_10_1103_PhysRevResearch_6_023319
Cites_doi 10.1039/D0SM01036G
10.1016/j.physrep.2012.03.004
10.1038/s41598-022-06941-x
10.1002/jemt.20829
10.1038/nature11591
10.1002/smll.200801388
10.1016/S0006-3495(01)76223-6
10.1529/biophysj.103.038877
10.1073/pnas.1219961110
10.1103/PhysRevLett.75.1226
10.1016/j.jbiomech.2009.09.005
10.1016/S1046-5928(03)00218-3
10.1038/s41467-018-05666-8
10.1038/nature10874
10.1103/PhysRevLett.75.176
10.1126/sciadv.aaw9975
10.1103/PhysRevE.77.011920
10.1021/ja901538n
10.1021/nl071696y
10.1038/nature22321
10.3389/fphy.2018.00075
10.1002/bit.21874
10.1103/PhysRevLett.117.197801
10.1088/0953-8984/23/37/374104
10.1371/journal.pone.0002736
10.1016/S0092-8674(00)81285-4
10.1073/pnas.0704169105
10.1186/s12951-021-00960-y
10.1021/bm501573v
10.1103/PhysRevLett.106.128101
10.1103/PhysRevLett.104.184502
10.1103/PhysRevLett.120.198101
10.1126/science.1059758
10.1074/jbc.M302186200
10.1103/PhysRevLett.96.258103
10.1364/AO.30.001369
10.1103/PhysRevE.54.1791
10.1140/epjst/e2016-60066-8
10.1016/S0006-3495(98)74029-9
10.1038/s41467-017-00035-3
10.1039/C8SM01877D
10.1038/nature09312
10.1016/j.bbagen.2014.01.012
10.1126/scirobotics.aan4882
10.2142/biophysico.16.0_1
10.1039/C8SM00282G
10.1039/C6RA27449H
10.1103/PhysRevLett.93.098103
10.1021/acs.macromol.7b01024
10.5685/plmorphol.29.15
10.1021/nl050586t
10.1038/s41467-019-12674-9
10.1039/C5NR02213D
10.1038/nmat4396
10.1371/journal.pcbi.1009394
10.1021/acs.langmuir.0c01002
10.1109/CVPRW50498.2020.00020
10.1529/biophysj.105.070458
10.1038/nature08908
10.1103/PhysRevE.77.046113
10.1103/PhysRevLett.74.330
10.1039/C7SM02298K
10.1016/0092-8674(94)90060-4
ContentType Journal Article
Copyright 2022 American Chemical Society
Copyright_xml – notice: 2022 American Chemical Society
DBID CGR
CUY
CVF
ECM
EIF
NPM
AAYXX
CITATION
7X8
DOI 10.1021/acsnano.2c05593
DatabaseName Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
CrossRef
MEDLINE - Academic
DatabaseTitle MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
CrossRef
MEDLINE - Academic
DatabaseTitleList
MEDLINE
Database_xml – sequence: 1
  dbid: ECM
  name: MEDLINE
  url: https://search.ebscohost.com/login.aspx?direct=true&db=cmedm&site=ehost-live
  sourceTypes: Index Database
DeliveryMethod fulltext_linktorsrc
Discipline Engineering
EISSN 1936-086X
EndPage 14778
ExternalDocumentID 10_1021_acsnano_2c05593
36098647
c02861023
Genre Research Support, Non-U.S. Gov't
Journal Article
GroupedDBID ---
.K2
23M
4.4
55A
5GY
5VS
6J9
7~N
AABXI
ABFRP
ABMVS
ABUCX
ACGFO
ACGFS
ACS
ADHLV
AEESW
AENEX
AFEFF
AHGAQ
ALMA_UNASSIGNED_HOLDINGS
AQSVZ
CS3
EBS
ED~
F5P
GGK
GNL
IH9
IHE
JG~
P2P
RNS
ROL
UI2
VF5
VG9
W1F
XKZ
YZZ
AAHBH
ABJNI
ABQRX
ACBEA
BAANH
CGR
CUPRZ
CUY
CVF
ECM
EIF
NPM
AAYXX
CITATION
7X8
ID FETCH-LOGICAL-a418t-90c5b0e7962db7c2462ce838f67c5c23bcdcea9f821400952c9bf6ce81bc72b43
IEDL.DBID ACS
ISSN 1936-0851
IngestDate Sat Aug 17 02:11:06 EDT 2024
Fri Aug 23 02:51:58 EDT 2024
Sat Sep 28 08:17:05 EDT 2024
Thu Sep 29 04:36:30 EDT 2022
IsDoiOpenAccess false
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 9
Keywords collective motion
self-organization
microtubules
active matter
persistence length
Language English
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-a418t-90c5b0e7962db7c2462ce838f67c5c23bcdcea9f821400952c9bf6ce81bc72b43
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
ORCID 0000-0001-8445-2642
0000-0002-5588-8532
0000-0002-6306-2693
0000-0003-0158-2244
OpenAccessLink https://repository.kulib.kyoto-u.ac.jp/dspace/bitstream/2433/277228/1/acsnano.2c05593.pdf
PMID 36098647
PQID 2714064021
PQPubID 23479
PageCount 14
ParticipantIDs proquest_miscellaneous_2714064021
crossref_primary_10_1021_acsnano_2c05593
pubmed_primary_36098647
acs_journals_10_1021_acsnano_2c05593
PublicationCentury 2000
PublicationDate 2022-09-27
PublicationDateYYYYMMDD 2022-09-27
PublicationDate_xml – month: 09
  year: 2022
  text: 2022-09-27
  day: 27
PublicationDecade 2020
PublicationPlace United States
PublicationPlace_xml – name: United States
PublicationTitle ACS nano
PublicationTitleAlternate ACS Nano
PublicationYear 2022
Publisher American Chemical Society
Publisher_xml – name: American Chemical Society
References ref9/cit9
ref45/cit45
ref3/cit3
ref27/cit27
ref63/cit63
ref56/cit56
ref16/cit16
ref52/cit52
ref23/cit23
ref8/cit8
ref31/cit31
ref59/cit59
ref2/cit2
ref34/cit34
ref37/cit37
ref20/cit20
ref48/cit48
ref60/cit60
ref17/cit17
ref10/cit10
ref35/cit35
ref53/cit53
ref19/cit19
ref21/cit21
ref42/cit42
ref46/cit46
ref49/cit49
ref13/cit13
ref61/cit61
ref24/cit24
ref38/cit38
ref50/cit50
ref64/cit64
ref54/cit54
ref6/cit6
ref18/cit18
ref65/cit65
ref11/cit11
ref25/cit25
ref29/cit29
Wang H. (ref36/cit36) 2020
ref32/cit32
ref39/cit39
ref14/cit14
ref57/cit57
ref5/cit5
ref51/cit51
ref43/cit43
ref28/cit28
ref40/cit40
ref26/cit26
ref55/cit55
ref12/cit12
ref15/cit15
ref62/cit62
ref41/cit41
ref58/cit58
ref22/cit22
ref33/cit33
ref4/cit4
ref30/cit30
ref47/cit47
ref1/cit1
ref44/cit44
ref7/cit7
References_xml – ident: ref31/cit31
  doi: 10.1039/D0SM01036G
– ident: ref1/cit1
  doi: 10.1016/j.physrep.2012.03.004
– ident: ref47/cit47
  doi: 10.1038/s41598-022-06941-x
– ident: ref64/cit64
  doi: 10.1002/jemt.20829
– ident: ref7/cit7
  doi: 10.1038/nature11591
– ident: ref49/cit49
  doi: 10.1002/smll.200801388
– ident: ref48/cit48
  doi: 10.1016/S0006-3495(01)76223-6
– ident: ref33/cit33
  doi: 10.1529/biophysj.103.038877
– ident: ref55/cit55
  doi: 10.1073/pnas.1219961110
– ident: ref24/cit24
  doi: 10.1103/PhysRevLett.75.1226
– ident: ref32/cit32
  doi: 10.1016/j.jbiomech.2009.09.005
– ident: ref59/cit59
  doi: 10.1016/S1046-5928(03)00218-3
– ident: ref11/cit11
  doi: 10.1038/s41467-018-05666-8
– ident: ref16/cit16
  doi: 10.1038/nature10874
– ident: ref52/cit52
  doi: 10.1103/PhysRevLett.75.176
– ident: ref30/cit30
  doi: 10.1126/sciadv.aaw9975
– ident: ref26/cit26
  doi: 10.1103/PhysRevE.77.011920
– ident: ref17/cit17
  doi: 10.1021/ja901538n
– ident: ref20/cit20
  doi: 10.1021/nl071696y
– ident: ref4/cit4
  doi: 10.1038/nature22321
– ident: ref39/cit39
  doi: 10.3389/fphy.2018.00075
– ident: ref60/cit60
  doi: 10.1002/bit.21874
– ident: ref22/cit22
  doi: 10.1103/PhysRevLett.117.197801
– ident: ref50/cit50
  doi: 10.1088/0953-8984/23/37/374104
– ident: ref53/cit53
  doi: 10.1371/journal.pone.0002736
– ident: ref9/cit9
  doi: 10.1016/S0092-8674(00)81285-4
– ident: ref21/cit21
  doi: 10.1073/pnas.0704169105
– ident: ref35/cit35
  doi: 10.1186/s12951-021-00960-y
– ident: ref18/cit18
  doi: 10.1021/bm501573v
– ident: ref25/cit25
  doi: 10.1103/PhysRevLett.106.128101
– ident: ref27/cit27
  doi: 10.1103/PhysRevLett.104.184502
– ident: ref2/cit2
  doi: 10.1103/PhysRevLett.120.198101
– ident: ref10/cit10
  doi: 10.1126/science.1059758
– ident: ref43/cit43
  doi: 10.1074/jbc.M302186200
– ident: ref28/cit28
  doi: 10.1103/PhysRevLett.96.258103
– ident: ref65/cit65
– ident: ref62/cit62
  doi: 10.1364/AO.30.001369
– ident: ref5/cit5
  doi: 10.1103/PhysRevE.54.1791
– ident: ref58/cit58
  doi: 10.1140/epjst/e2016-60066-8
– ident: ref61/cit61
  doi: 10.1016/S0006-3495(98)74029-9
– ident: ref37/cit37
  doi: 10.1038/s41467-017-00035-3
– ident: ref14/cit14
  doi: 10.1088/0953-8984/23/37/374104
– ident: ref12/cit12
  doi: 10.1039/C8SM01877D
– ident: ref13/cit13
  doi: 10.1038/nature09312
– ident: ref44/cit44
  doi: 10.1016/j.bbagen.2014.01.012
– ident: ref19/cit19
  doi: 10.1126/scirobotics.aan4882
– ident: ref63/cit63
  doi: 10.2142/biophysico.16.0_1
– ident: ref29/cit29
  doi: 10.1039/C8SM00282G
– ident: ref40/cit40
  doi: 10.1039/C6RA27449H
– ident: ref3/cit3
  doi: 10.1103/PhysRevLett.93.098103
– ident: ref23/cit23
  doi: 10.1021/acs.macromol.7b01024
– ident: ref38/cit38
  doi: 10.5685/plmorphol.29.15
– ident: ref46/cit46
  doi: 10.1021/nl050586t
– ident: ref8/cit8
  doi: 10.1038/s41467-019-12674-9
– ident: ref15/cit15
  doi: 10.1039/C5NR02213D
– ident: ref34/cit34
  doi: 10.1038/nmat4396
– ident: ref56/cit56
  doi: 10.1371/journal.pcbi.1009394
– ident: ref51/cit51
  doi: 10.1021/acs.langmuir.0c01002
– start-page: 111
  volume-title: 2020 IEEE/CVF Conference on Computer Vision and Pattern Recognition Workshops (CVPRW)
  year: 2020
  ident: ref36/cit36
  doi: 10.1109/CVPRW50498.2020.00020
  contributor:
    fullname: Wang H.
– ident: ref42/cit42
  doi: 10.1529/biophysj.105.070458
– ident: ref6/cit6
  doi: 10.1038/nature08908
– ident: ref57/cit57
  doi: 10.1103/PhysRevE.77.046113
– ident: ref45/cit45
  doi: 10.1103/PhysRevLett.74.330
– ident: ref41/cit41
  doi: 10.1039/C7SM02298K
– ident: ref54/cit54
  doi: 10.1016/0092-8674(94)90060-4
SSID ssj0057876
Score 2.4609149
Snippet Collective motion is a ubiquitous phenomenon in nature. The collective motion of cytoskeleton filaments results mainly from dynamic collisions and alignments;...
SourceID proquest
crossref
pubmed
acs
SourceType Aggregation Database
Index Database
Publisher
StartPage 14765
SubjectTerms Cytoskeleton
Kinesins
Microtubules
Motion
Phase Transition
Title Durability of Aligned Microtubules Dependent on Persistence Length Determines Phase Transition and Pattern Formation in Collective Motion
URI http://dx.doi.org/10.1021/acsnano.2c05593
https://www.ncbi.nlm.nih.gov/pubmed/36098647
https://search.proquest.com/docview/2714064021
Volume 16
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://sdu.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwlV1LS8QwEA66XvTg-7G-iLAHPVTb9JH0KO4ue1ARVsFbyavugqRi24M_wX_tJO0uiizopZeGEDIzmW8yk28Q6slIB7kvqAcf34sYzz0ec-X5Ooq0jtM8lPYqezSm98-sP7A0ORcLMvgkuOKyNNwUl0T6gH7DZbRCKOAEi4JuxrND1-pd0iSQIUAGFDFn8fk1gXVDsvzphhZgS-djhhv_WN0mWm-BJL5uJL-FlrTZRmvf6AV30Ge_fm9ouD9wkePr1-kLHKr4ztbgVbWoX3WJ-20T3AoXBttyeCt2UAR8q81LNYH_TbkMDH2YgMfDzrm5Oi_MjcIPjp_T4OHsESSeGuxuI9xBiu9cl6Bd9DQcPN6MvLb1gsejgFVe6stY-JqmCVGCShIlRGoWsjyhMpYkFFJJzdOcEQjQAKURmYo8gSGBkJSIKNxDHVMYfYCwAgtnue3SriA6EiyNY6VTUJAgUYxFoot6sIlZazpl5rLiJMjanc3ane2i85nAsreGiGPx0LOZQDMwFpsB4UYXdZkRS0-YQMgcdNF-I-n5ZGHiW6p6evi39RyhVWJfQtgEFT1Gneq91idouVT1qdPMLzgF4Y0
link.rule.ids 315,782,786,2769,27085,27933,27934,56747,56797
linkProvider American Chemical Society
linkToHtml http://sdu.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwlV3JTuQwEC2xHIADMAxLs8wYicNcAomTOM4R0bQaTTdCgpHmFsVLAAk5iCQHPoG_puwkLEJIcMnBsSzLVXa9cpVfARzISAeFLxIPP74X8bzw8jhXnq-jSOs4LUJpr7LHl8n5fz48tTQ5fv8WBidR4UiVC-K_sgsER9hmclMeUukjCA5nYT5mCIUtGDq57M9eq36sjSOjn4xg4oXM58MA1hrJ6r01-gRiOlMzWvn-JFdhuYOV5LjVgx8wo80aLL0hG_wJT8PmoSXlfiRlQY7vbq_xiCVTm5FXN6K50xUZdiVxa1IaYpPjrRKgWpCJNtf1Df5vk2ew68UN2j_iTJ3L-iK5UeTCsXUaMuqfRJJbQ9zdhDtWydTVDFqHf6PTq5Ox1xVi8PIo4LWX-jIWvk5SRpVIJI0YlZqHvGCJjCUNhVRS52nBKbpriNmoTEXBsEsgZEJFFG7AnCmN3gKicL_zwtZsV-grCZ7GsdIpqkvAFOeRGMABLmLWbaQqczFyGmTdymbdyg7gTy-37L6l5fi8634v1wy3jo2H5EaXTZVRS1bI0IEOBrDZCvxlsJD5lrg-2f7afH7DwvhqOskmZ-d_d2CR2jcSNnSV7MJc_dDoPZitVPPLKesz5_rp-g
linkToPdf http://sdu.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1La9wwEB7ygNIe2jR9ZNumVSCHXtzasizJxyWbJaFJWEgLvRnrlQSCHGL7kJ_Qf92RbIeWEii5-CAPQkjz1Iy-AdjXzGYuVSLBT5owWbukLmqTpJYxa4vS5TpcZR-di7OfcnEYYHLY9BYGF9HiTG1M4gepvjFuRBjIvuK4r33zheoUHeF8HTYLLsoQcs0Pzif9G1iQD7lkjJXRobgH9PlngmCRdPu3RXrAzYzmZvnicQvdgueje0nmAz-8hDXrt-HZH6CDr-DXor8dwLnvSOPI_PrqAlUtOQ2VeV2v-mvbksXYGrcjjSehSD4wA7IHObH-orvE_0MRDZKuLtEOkmjyYvUXqb0hq4ja6clyehpJrjyJdxRRvZLT2DvoNfxYHn4_OErGhgxJzTLZJWWqC5VaUXJqlNCUcaqtzKXjQhea5kobbevSSYphG_puVJfKcSTJlBZUsfwNbPjG2x0gBuVeutC73WDMpGRZFMaWyDYZN1IyNYN93MRqFKi2irlymlXjzlbjzs7g83R21c0Az_Ew6d50thWKUMiL1N42fVvRAFrIMZDOZvB2OPT7yXKeBgB78e7_1vMJnqwWy-rk-Ozbe3hKw1OJkMESH2Cju-3tLqy3pv8Y-fU3g5jsfQ
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Durability+of+Aligned+Microtubules+Dependent+on+Persistence+Length+Determines+Phase+Transition+and+Pattern+Formation+in+Collective+Motion&rft.jtitle=ACS+nano&rft.au=Zhou%2C+Hang&rft.au=Jung%2C+Wonyeong&rft.au=Farhana%2C+Tamanna+Ishrat&rft.au=Fujimoto%2C+Kazuya&rft.date=2022-09-27&rft.eissn=1936-086X&rft.volume=16&rft.issue=9&rft.spage=14765&rft.epage=14778&rft_id=info:doi/10.1021%2Facsnano.2c05593&rft.externalDBID=NO_FULL_TEXT
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1936-0851&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1936-0851&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1936-0851&client=summon