Primary cilia utilize glycoprotein-dependent adhesion mechanisms to stabilize long-lasting cilia-cilia contacts

Cilia

Jennifer Lippincott-Schwartz¹  Prabuddha Sengupta¹  Christine Insinna³  Suh Young Jeong²  Natalie Elia¹  Carolyn Ott¹ 

[1] Cell Biology and Metabolism Program, National Institute of Child Health and Human Development, Bethesda, MD, USA;Molecular Medicine Program, National Institute of Child Health and Human Development, Bethesda, MD, USA;Department of Ophthalmology and Vision Science, University of California, Davis, CA, USA

关键词: Glycoprotein;    Direct sensing;    Adhesion;    Contact;    Primary cilia;   

Others  :  793785
DOI  :  10.1186/2046-2530-1-3

 received in 2011-10-26, accepted in 2012-04-25,  发布年份 2012

【 摘 要 】

Background

The central tenet of cilia function is sensing and transmitting information. The capacity to directly contact extracellular surfaces would empower primary cilia to probe the environment for information about the nature and location of nearby surfaces. It has been well established that flagella and other motile cilia perform diverse cellular functions through adhesion. We hypothesized that mammalian primary cilia also interact with the extracellular environment through direct physical contact.

Methods

We identified cilia in rod photoreceptors and cholangiocytes in fixed mouse tissues and examined the structures that these cilia contact in vivo. We then utilized an MDCK cell culture model to characterize the nature of the contacts we observed.

Results

In retina and liver tissue, we observed that cilia from nearby cells touch one another. Using MDCK cells, we found compelling evidence that these contacts are stable adhesions that form bridges between two cells, or networks between many cells. We examined the nature and duration of the cilia-cilia contacts and discovered primary cilia movements that facilitate cilia-cilia encounters. Stable adhesions form as the area of contact expands from a single point to a stretch of tightly bound, adjacent cilia membranes. The cilia-cilia contacts persisted for hours and were resistant to several harsh treatments such as proteases and DTT. Unlike many other cell adhesion mechanisms, calcium was not required for the formation or maintenance of cilia adhesion. However, swainsonine, which blocks maturation of N-linked glycoproteins, reduced contact formation. We propose that cellular control of adhesion maintenance is active because cilia adhesion did not prevent cell division; rather, contacts dissolved during mitosis as cilia were resorbed.

Conclusions

The demonstration that mammalian primary cilia formed prolonged, direct, physical contacts supports a novel paradigm: that mammalian primary cilia detect features of the extracellular space, not just as passive antennae, but also through direct physical contact. We present a model for the cycle of glycoprotein-dependent contact formation, maintenance, and termination, and discuss the implications for potential physiological functions of cilia-cilia contacts.

【 授权许可】

   
2012 Ott et al; licensee BioMed Central Ltd.

【 图 表 】

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