Bi-directional cell-pericellular matrix interactions direct stem cell fate

Silvia A Ferreira; Meghna Suresh Motwani; Peter A. Faull; Alexis Jane Seymour; Tong Yu; Marjan Enayati; Dheraj Kumar Taheem; Ewa Monika Kania; Oommen P Oommen; Tarek Ahmed; Sandra Loaiza; Katarzyna Parzych; Francesco Dazzi; H. W. Auner; Oommen P. Varghese; Frederic Festy; Agamemnon Emil Grigoriadis; Ambrosius P. Snijders; Laurent Bozec; Eileen Deirdre Gentleman

doi:10.1038/s41467-018-06183-4

Bi-directional cell-pericellular matrix interactions direct stem cell fate

Silvia A Ferreira, Meghna Suresh Motwani, Peter A. Faull, Alexis Jane Seymour, Tong Yu, Marjan Enayati, Dheraj Kumar Taheem, Ewa Monika Kania, Oommen P Oommen, Tarek Ahmed, Sandra Loaiza, Katarzyna Parzych, Francesco Dazzi, H. W. Auner, Oommen P. Varghese, Frederic Festy, Agamemnon Emil Grigoriadis, Ambrosius P. Snijders, Laurent Bozec, Eileen Deirdre Gentleman

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Abstract

Modifiable hydrogels have revealed tremendous insight into how physical characteristics of cells’ 3D environment drive stem cell lineage specification. However, in native tissues, cells do not passively receive signals from their niche. Instead they actively probe and modify their pericellular space to suit their needs, yet the dynamics of cells’ reciprocal interactions with their pericellular environment when encapsulated within hydrogels remains relatively unexplored. Here, we show that human bone marrow stromal cells (hMSC) encapsulated within hyaluronic acid-based hydrogels modify their surroundings by synthesizing, secreting and arranging proteins pericellularly or by degrading the hydrogel. hMSC’s interactions with this local environment play a role in regulating hMSC fate, with a secreted proteinaceous pericellular matrix associated with adipogenesis, and degradation with osteogenesis. Our observations suggest that hMSC participate in a bi-directional interplay between the properties of their 3D milieu and their own secreted pericellular matrix, and that this combination of interactions drives fate.

Original language	English
Article number	4049
Number of pages	12
Journal	Nature Communications
Volume	9
Issue number	1
Early online date	3 Oct 2018
DOIs	https://doi.org/10.1038/s41467-018-06183-4
Publication status	Published - 3 Oct 2018

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Ferreira, S. A., Motwani, M. S., Faull, P. A., Seymour, A. J., Yu, T., Enayati, M., Taheem, D. K., Kania, E. M., Oommen, O. P., Ahmed, T., Loaiza, S., Parzych, K., Dazzi, F., Auner, H. W., Varghese, O. P., Festy, F., Grigoriadis, A. E., Snijders, A. P., Bozec, L., & Gentleman, E. D. (2018). Bi-directional cell-pericellular matrix interactions direct stem cell fate. Nature Communications, 9(1), Article 4049. https://doi.org/10.1038/s41467-018-06183-4

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title = "Bi-directional cell-pericellular matrix interactions direct stem cell fate",

abstract = "Modifiable hydrogels have revealed tremendous insight into how physical characteristics of cells{\textquoteright} 3D environment drive stem cell lineage specification. However, in native tissues, cells do not passively receive signals from their niche. Instead they actively probe and modify their pericellular space to suit their needs, yet the dynamics of cells{\textquoteright} reciprocal interactions with their pericellular environment when encapsulated within hydrogels remains relatively unexplored. Here, we show that human bone marrow stromal cells (hMSC) encapsulated within hyaluronic acid-based hydrogels modify their surroundings by synthesizing, secreting and arranging proteins pericellularly or by degrading the hydrogel. hMSC{\textquoteright}s interactions with this local environment play a role in regulating hMSC fate, with a secreted proteinaceous pericellular matrix associated with adipogenesis, and degradation with osteogenesis. Our observations suggest that hMSC participate in a bi-directional interplay between the properties of their 3D milieu and their own secreted pericellular matrix, and that this combination of interactions drives fate. ",

author = "Ferreira, {Silvia A} and Motwani, {Meghna Suresh} and Faull, {Peter A.} and Seymour, {Alexis Jane} and Tong Yu and Marjan Enayati and Taheem, {Dheraj Kumar} and Kania, {Ewa Monika} and Oommen, {Oommen P} and Tarek Ahmed and Sandra Loaiza and Katarzyna Parzych and Francesco Dazzi and Auner, {H. W.} and Varghese, {Oommen P.} and Frederic Festy and Grigoriadis, {Agamemnon Emil} and Snijders, {Ambrosius P.} and Laurent Bozec and Gentleman, {Eileen Deirdre}",

year = "2018",

month = oct,

day = "3",

doi = "10.1038/s41467-018-06183-4",

language = "English",

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Ferreira, SA , Motwani, MS, Faull, PA, Seymour, AJ , Yu, T , Enayati, M , Taheem, DK , Kania, EM, Oommen, OP, Ahmed, T, Loaiza, S, Parzych, K, Dazzi, F, Auner, HW, Varghese, OP, Festy, F, Grigoriadis, AE, Snijders, AP, Bozec, L & Gentleman, ED 2018, 'Bi-directional cell-pericellular matrix interactions direct stem cell fate', Nature Communications, vol. 9, no. 1, 4049. https://doi.org/10.1038/s41467-018-06183-4

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T1 - Bi-directional cell-pericellular matrix interactions direct stem cell fate

AU - Ferreira, Silvia A

AU - Motwani, Meghna Suresh

AU - Faull, Peter A.

AU - Seymour, Alexis Jane

AU - Yu, Tong

AU - Enayati, Marjan

AU - Taheem, Dheraj Kumar

AU - Kania, Ewa Monika

AU - Oommen, Oommen P

AU - Ahmed, Tarek

AU - Loaiza, Sandra

AU - Parzych, Katarzyna

AU - Dazzi, Francesco

AU - Auner, H. W.

AU - Varghese, Oommen P.

AU - Festy, Frederic

AU - Grigoriadis, Agamemnon Emil

AU - Snijders, Ambrosius P.

AU - Bozec, Laurent

AU - Gentleman, Eileen Deirdre

PY - 2018/10/3

Y1 - 2018/10/3

N2 - Modifiable hydrogels have revealed tremendous insight into how physical characteristics of cells’ 3D environment drive stem cell lineage specification. However, in native tissues, cells do not passively receive signals from their niche. Instead they actively probe and modify their pericellular space to suit their needs, yet the dynamics of cells’ reciprocal interactions with their pericellular environment when encapsulated within hydrogels remains relatively unexplored. Here, we show that human bone marrow stromal cells (hMSC) encapsulated within hyaluronic acid-based hydrogels modify their surroundings by synthesizing, secreting and arranging proteins pericellularly or by degrading the hydrogel. hMSC’s interactions with this local environment play a role in regulating hMSC fate, with a secreted proteinaceous pericellular matrix associated with adipogenesis, and degradation with osteogenesis. Our observations suggest that hMSC participate in a bi-directional interplay between the properties of their 3D milieu and their own secreted pericellular matrix, and that this combination of interactions drives fate.

AB - Modifiable hydrogels have revealed tremendous insight into how physical characteristics of cells’ 3D environment drive stem cell lineage specification. However, in native tissues, cells do not passively receive signals from their niche. Instead they actively probe and modify their pericellular space to suit their needs, yet the dynamics of cells’ reciprocal interactions with their pericellular environment when encapsulated within hydrogels remains relatively unexplored. Here, we show that human bone marrow stromal cells (hMSC) encapsulated within hyaluronic acid-based hydrogels modify their surroundings by synthesizing, secreting and arranging proteins pericellularly or by degrading the hydrogel. hMSC’s interactions with this local environment play a role in regulating hMSC fate, with a secreted proteinaceous pericellular matrix associated with adipogenesis, and degradation with osteogenesis. Our observations suggest that hMSC participate in a bi-directional interplay between the properties of their 3D milieu and their own secreted pericellular matrix, and that this combination of interactions drives fate.

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DO - 10.1038/s41467-018-06183-4

M3 - Article

SN - 2041-1723

VL - 9

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 4049

ER -

Bi-directional cell-pericellular matrix interactions direct stem cell fate

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