A mechanosensory system governs myosin II accumulation in dividing cells

Yee Seir Kee, Yixin Ren, Danielle Dorfman, Miho Iijima, Richard Firtel, Pablo A Iglesias, Douglas Robinson

Research output: Contribution to journalArticle

Abstract

The mitotic spindle is generally considered the initiator of furrow ingression. However, recent studies suggest that furrows can form without spindles, particularly during asymmetric cell division. In Dictyostelium, the mechanoenzyme myosin II and the actin crosslinker cortexillin I form a mechanosensor that responds to mechanical stress, which could account for spindle-independent contractile protein recruitment. Here we show that the regulatory and contractility network composed of myosin II, cortexillin I, IQGAP2, kinesin-6 (kif12), and inner centromeric protein (INCENP) is a mechanical stress-responsive system. Myosin II and cortexillin I form the core mechanosensor, and mechanotransduction is mediated by IQGAP2 to kif12 and INCENP. In addition, IQGAP2 is antagonized by IQGAP1 to modulate the mechanoresponsiveness of the system, suggesting a possible mechanism for discriminating between mechanical and biochemical inputs. Furthermore, IQGAP2 is important for maintaining spindle morphology and kif12 and myosin II cleavage furrow recruitment. Cortexillin II is not directly involved in myosin II mechanosensitive accumulation, but without cortexillin I, cortexillin II's role in membrane-cortex attachment is revealed. Finally, the mitotic spindle is dispensable for the system. Overall, this mechanosensory system is structured like a control system characterized by mechanochemical feedback loops that regulate myosin II localization at sites of mechanical stress and the cleavage furrow.

Original languageEnglish (US)
Pages (from-to)1510-1523
Number of pages14
JournalMolecular Biology of the Cell
Volume23
Issue number8
DOIs
StatePublished - Apr 15 2012

Fingerprint

Myosin Type II
Mechanical Stress
Spindle Apparatus
Asymmetric Cell Division
Contractile Proteins
Kinesin
Dictyostelium
Actins
Proteins
Membranes

ASJC Scopus subject areas

  • Molecular Biology
  • Cell Biology

Cite this

A mechanosensory system governs myosin II accumulation in dividing cells. / Kee, Yee Seir; Ren, Yixin; Dorfman, Danielle; Iijima, Miho; Firtel, Richard; Iglesias, Pablo A; Robinson, Douglas.

In: Molecular Biology of the Cell, Vol. 23, No. 8, 15.04.2012, p. 1510-1523.

Research output: Contribution to journalArticle

Kee, Yee Seir ; Ren, Yixin ; Dorfman, Danielle ; Iijima, Miho ; Firtel, Richard ; Iglesias, Pablo A ; Robinson, Douglas. / A mechanosensory system governs myosin II accumulation in dividing cells. In: Molecular Biology of the Cell. 2012 ; Vol. 23, No. 8. pp. 1510-1523.
@article{b6cb73dec20142ba95b4ecadb13421e2,
title = "A mechanosensory system governs myosin II accumulation in dividing cells",
abstract = "The mitotic spindle is generally considered the initiator of furrow ingression. However, recent studies suggest that furrows can form without spindles, particularly during asymmetric cell division. In Dictyostelium, the mechanoenzyme myosin II and the actin crosslinker cortexillin I form a mechanosensor that responds to mechanical stress, which could account for spindle-independent contractile protein recruitment. Here we show that the regulatory and contractility network composed of myosin II, cortexillin I, IQGAP2, kinesin-6 (kif12), and inner centromeric protein (INCENP) is a mechanical stress-responsive system. Myosin II and cortexillin I form the core mechanosensor, and mechanotransduction is mediated by IQGAP2 to kif12 and INCENP. In addition, IQGAP2 is antagonized by IQGAP1 to modulate the mechanoresponsiveness of the system, suggesting a possible mechanism for discriminating between mechanical and biochemical inputs. Furthermore, IQGAP2 is important for maintaining spindle morphology and kif12 and myosin II cleavage furrow recruitment. Cortexillin II is not directly involved in myosin II mechanosensitive accumulation, but without cortexillin I, cortexillin II's role in membrane-cortex attachment is revealed. Finally, the mitotic spindle is dispensable for the system. Overall, this mechanosensory system is structured like a control system characterized by mechanochemical feedback loops that regulate myosin II localization at sites of mechanical stress and the cleavage furrow.",
author = "Kee, {Yee Seir} and Yixin Ren and Danielle Dorfman and Miho Iijima and Richard Firtel and Iglesias, {Pablo A} and Douglas Robinson",
year = "2012",
month = "4",
day = "15",
doi = "10.1091/mbc.E11-07-0601",
language = "English (US)",
volume = "23",
pages = "1510--1523",
journal = "Molecular Biology of the Cell",
issn = "1059-1524",
publisher = "American Society for Cell Biology",
number = "8",

}

TY - JOUR

T1 - A mechanosensory system governs myosin II accumulation in dividing cells

AU - Kee, Yee Seir

AU - Ren, Yixin

AU - Dorfman, Danielle

AU - Iijima, Miho

AU - Firtel, Richard

AU - Iglesias, Pablo A

AU - Robinson, Douglas

PY - 2012/4/15

Y1 - 2012/4/15

N2 - The mitotic spindle is generally considered the initiator of furrow ingression. However, recent studies suggest that furrows can form without spindles, particularly during asymmetric cell division. In Dictyostelium, the mechanoenzyme myosin II and the actin crosslinker cortexillin I form a mechanosensor that responds to mechanical stress, which could account for spindle-independent contractile protein recruitment. Here we show that the regulatory and contractility network composed of myosin II, cortexillin I, IQGAP2, kinesin-6 (kif12), and inner centromeric protein (INCENP) is a mechanical stress-responsive system. Myosin II and cortexillin I form the core mechanosensor, and mechanotransduction is mediated by IQGAP2 to kif12 and INCENP. In addition, IQGAP2 is antagonized by IQGAP1 to modulate the mechanoresponsiveness of the system, suggesting a possible mechanism for discriminating between mechanical and biochemical inputs. Furthermore, IQGAP2 is important for maintaining spindle morphology and kif12 and myosin II cleavage furrow recruitment. Cortexillin II is not directly involved in myosin II mechanosensitive accumulation, but without cortexillin I, cortexillin II's role in membrane-cortex attachment is revealed. Finally, the mitotic spindle is dispensable for the system. Overall, this mechanosensory system is structured like a control system characterized by mechanochemical feedback loops that regulate myosin II localization at sites of mechanical stress and the cleavage furrow.

AB - The mitotic spindle is generally considered the initiator of furrow ingression. However, recent studies suggest that furrows can form without spindles, particularly during asymmetric cell division. In Dictyostelium, the mechanoenzyme myosin II and the actin crosslinker cortexillin I form a mechanosensor that responds to mechanical stress, which could account for spindle-independent contractile protein recruitment. Here we show that the regulatory and contractility network composed of myosin II, cortexillin I, IQGAP2, kinesin-6 (kif12), and inner centromeric protein (INCENP) is a mechanical stress-responsive system. Myosin II and cortexillin I form the core mechanosensor, and mechanotransduction is mediated by IQGAP2 to kif12 and INCENP. In addition, IQGAP2 is antagonized by IQGAP1 to modulate the mechanoresponsiveness of the system, suggesting a possible mechanism for discriminating between mechanical and biochemical inputs. Furthermore, IQGAP2 is important for maintaining spindle morphology and kif12 and myosin II cleavage furrow recruitment. Cortexillin II is not directly involved in myosin II mechanosensitive accumulation, but without cortexillin I, cortexillin II's role in membrane-cortex attachment is revealed. Finally, the mitotic spindle is dispensable for the system. Overall, this mechanosensory system is structured like a control system characterized by mechanochemical feedback loops that regulate myosin II localization at sites of mechanical stress and the cleavage furrow.

UR - http://www.scopus.com/inward/record.url?scp=84859709754&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84859709754&partnerID=8YFLogxK

U2 - 10.1091/mbc.E11-07-0601

DO - 10.1091/mbc.E11-07-0601

M3 - Article

C2 - 22379107

AN - SCOPUS:84859709754

VL - 23

SP - 1510

EP - 1523

JO - Molecular Biology of the Cell

JF - Molecular Biology of the Cell

SN - 1059-1524

IS - 8

ER -