Protein composition and movements of membrane swellings associated with primary cilia

Ashraf M. Mohieldin, Hanan S. Haymour, Shao T. Lo, Wissam A. Aboualaiwi, Kimberly F. Atkinson, Christopher J. Ward, Min Gao, Oliver Wessely, Surya M. Nauli

Research output: Contribution to journalArticle

12 Citations (Scopus)

Abstract

Abstract Dysfunction of many ciliary proteins has been linked to a list of diseases, from cystic kidney to obesity and from hypertension to mental retardation. We previously proposed that primary cilia are unique communication organelles that function as microsensory compartments that house mechanosensory molecules. Here we report that primary cilia exhibit membrane swellings or ciliary bulbs, which based on their unique ultrastructure and motility, could be mechanically regulated by fluid-shear stress. Together with the ultrastructure analysis of the swelling, which contains monosialodihexosylganglioside (GM3), our results show that ciliary bulb has a distinctive set of functional proteins, including GM3 synthase (GM3S), bicaudal-c1 (Bicc1), and polycystin-2 (PC2). In fact, results from our cilia isolation demonstrated for the first time that GM3S and Bicc1 are members of the primary cilia proteins. Although these proteins are not required for ciliary membrane swelling formation under static condition, fluid-shear stress induced swelling formation is partially modulated by GM3S. We therefore propose that the ciliary bulb exhibits a sensory function within the mechano-ciliary structure. Overall, our studies provided an important step towards understanding the ciliary bulb function and structure.

Original languageEnglish (US)
Article number1838
Pages (from-to)2415-2429
Number of pages15
JournalCellular and Molecular Life Sciences
Volume72
Issue number12
DOIs
StatePublished - Jun 26 2015
Externally publishedYes

Fingerprint

Cilia
Membranes
Proteins
Cystic Kidney Diseases
Intellectual Disability
Organelles
Obesity
Communication
Hypertension
haematoside synthetase

Keywords

  • Bicc-1
  • Ciliary bulb
  • Ciliary membrane swelling
  • Fluid-shear stress
  • GM3S
  • PC2
  • Primary cilia

ASJC Scopus subject areas

  • Cell Biology
  • Molecular Biology
  • Molecular Medicine
  • Pharmacology
  • Cellular and Molecular Neuroscience

Cite this

Mohieldin, A. M., Haymour, H. S., Lo, S. T., Aboualaiwi, W. A., Atkinson, K. F., Ward, C. J., ... Nauli, S. M. (2015). Protein composition and movements of membrane swellings associated with primary cilia. Cellular and Molecular Life Sciences, 72(12), 2415-2429. [1838]. https://doi.org/10.1007/s00018-015-1838-x

Protein composition and movements of membrane swellings associated with primary cilia. / Mohieldin, Ashraf M.; Haymour, Hanan S.; Lo, Shao T.; Aboualaiwi, Wissam A.; Atkinson, Kimberly F.; Ward, Christopher J.; Gao, Min; Wessely, Oliver; Nauli, Surya M.

In: Cellular and Molecular Life Sciences, Vol. 72, No. 12, 1838, 26.06.2015, p. 2415-2429.

Research output: Contribution to journalArticle

Mohieldin, AM, Haymour, HS, Lo, ST, Aboualaiwi, WA, Atkinson, KF, Ward, CJ, Gao, M, Wessely, O & Nauli, SM 2015, 'Protein composition and movements of membrane swellings associated with primary cilia', Cellular and Molecular Life Sciences, vol. 72, no. 12, 1838, pp. 2415-2429. https://doi.org/10.1007/s00018-015-1838-x
Mohieldin AM, Haymour HS, Lo ST, Aboualaiwi WA, Atkinson KF, Ward CJ et al. Protein composition and movements of membrane swellings associated with primary cilia. Cellular and Molecular Life Sciences. 2015 Jun 26;72(12):2415-2429. 1838. https://doi.org/10.1007/s00018-015-1838-x
Mohieldin, Ashraf M. ; Haymour, Hanan S. ; Lo, Shao T. ; Aboualaiwi, Wissam A. ; Atkinson, Kimberly F. ; Ward, Christopher J. ; Gao, Min ; Wessely, Oliver ; Nauli, Surya M. / Protein composition and movements of membrane swellings associated with primary cilia. In: Cellular and Molecular Life Sciences. 2015 ; Vol. 72, No. 12. pp. 2415-2429.
@article{bd82906df75d4e6d9179267a5a43b1cf,
title = "Protein composition and movements of membrane swellings associated with primary cilia",
abstract = "Abstract Dysfunction of many ciliary proteins has been linked to a list of diseases, from cystic kidney to obesity and from hypertension to mental retardation. We previously proposed that primary cilia are unique communication organelles that function as microsensory compartments that house mechanosensory molecules. Here we report that primary cilia exhibit membrane swellings or ciliary bulbs, which based on their unique ultrastructure and motility, could be mechanically regulated by fluid-shear stress. Together with the ultrastructure analysis of the swelling, which contains monosialodihexosylganglioside (GM3), our results show that ciliary bulb has a distinctive set of functional proteins, including GM3 synthase (GM3S), bicaudal-c1 (Bicc1), and polycystin-2 (PC2). In fact, results from our cilia isolation demonstrated for the first time that GM3S and Bicc1 are members of the primary cilia proteins. Although these proteins are not required for ciliary membrane swelling formation under static condition, fluid-shear stress induced swelling formation is partially modulated by GM3S. We therefore propose that the ciliary bulb exhibits a sensory function within the mechano-ciliary structure. Overall, our studies provided an important step towards understanding the ciliary bulb function and structure.",
keywords = "Bicc-1, Ciliary bulb, Ciliary membrane swelling, Fluid-shear stress, GM3S, PC2, Primary cilia",
author = "Mohieldin, {Ashraf M.} and Haymour, {Hanan S.} and Lo, {Shao T.} and Aboualaiwi, {Wissam A.} and Atkinson, {Kimberly F.} and Ward, {Christopher J.} and Min Gao and Oliver Wessely and Nauli, {Surya M.}",
year = "2015",
month = "6",
day = "26",
doi = "10.1007/s00018-015-1838-x",
language = "English (US)",
volume = "72",
pages = "2415--2429",
journal = "Cellular and Molecular Life Sciences",
issn = "1420-682X",
publisher = "Birkhauser Verlag Basel",
number = "12",

}

TY - JOUR

T1 - Protein composition and movements of membrane swellings associated with primary cilia

AU - Mohieldin, Ashraf M.

AU - Haymour, Hanan S.

AU - Lo, Shao T.

AU - Aboualaiwi, Wissam A.

AU - Atkinson, Kimberly F.

AU - Ward, Christopher J.

AU - Gao, Min

AU - Wessely, Oliver

AU - Nauli, Surya M.

PY - 2015/6/26

Y1 - 2015/6/26

N2 - Abstract Dysfunction of many ciliary proteins has been linked to a list of diseases, from cystic kidney to obesity and from hypertension to mental retardation. We previously proposed that primary cilia are unique communication organelles that function as microsensory compartments that house mechanosensory molecules. Here we report that primary cilia exhibit membrane swellings or ciliary bulbs, which based on their unique ultrastructure and motility, could be mechanically regulated by fluid-shear stress. Together with the ultrastructure analysis of the swelling, which contains monosialodihexosylganglioside (GM3), our results show that ciliary bulb has a distinctive set of functional proteins, including GM3 synthase (GM3S), bicaudal-c1 (Bicc1), and polycystin-2 (PC2). In fact, results from our cilia isolation demonstrated for the first time that GM3S and Bicc1 are members of the primary cilia proteins. Although these proteins are not required for ciliary membrane swelling formation under static condition, fluid-shear stress induced swelling formation is partially modulated by GM3S. We therefore propose that the ciliary bulb exhibits a sensory function within the mechano-ciliary structure. Overall, our studies provided an important step towards understanding the ciliary bulb function and structure.

AB - Abstract Dysfunction of many ciliary proteins has been linked to a list of diseases, from cystic kidney to obesity and from hypertension to mental retardation. We previously proposed that primary cilia are unique communication organelles that function as microsensory compartments that house mechanosensory molecules. Here we report that primary cilia exhibit membrane swellings or ciliary bulbs, which based on their unique ultrastructure and motility, could be mechanically regulated by fluid-shear stress. Together with the ultrastructure analysis of the swelling, which contains monosialodihexosylganglioside (GM3), our results show that ciliary bulb has a distinctive set of functional proteins, including GM3 synthase (GM3S), bicaudal-c1 (Bicc1), and polycystin-2 (PC2). In fact, results from our cilia isolation demonstrated for the first time that GM3S and Bicc1 are members of the primary cilia proteins. Although these proteins are not required for ciliary membrane swelling formation under static condition, fluid-shear stress induced swelling formation is partially modulated by GM3S. We therefore propose that the ciliary bulb exhibits a sensory function within the mechano-ciliary structure. Overall, our studies provided an important step towards understanding the ciliary bulb function and structure.

KW - Bicc-1

KW - Ciliary bulb

KW - Ciliary membrane swelling

KW - Fluid-shear stress

KW - GM3S

KW - PC2

KW - Primary cilia

UR - http://www.scopus.com/inward/record.url?scp=84926467684&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84926467684&partnerID=8YFLogxK

U2 - 10.1007/s00018-015-1838-x

DO - 10.1007/s00018-015-1838-x

M3 - Article

C2 - 25650235

AN - SCOPUS:84926467684

VL - 72

SP - 2415

EP - 2429

JO - Cellular and Molecular Life Sciences

JF - Cellular and Molecular Life Sciences

SN - 1420-682X

IS - 12

M1 - 1838

ER -