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

Silvia A. Ferreira; Meghna S. Motwani; Peter A. Faull; Alexis J. Seymour; Tracy T.L. Yu; Marjan Enayati; Dheraj K. Taheem; Christoph Salzlechner; Tabasom Haghighi; Ewa M. Kania; Oommen P. Oommen; Tarek Ahmed; Sandra Loaiza; Katarzyna Parzych; Francesco Dazzi; Oommen P. Varghese; Frederic Festy; Agamemnon E. Grigoriadis; Holger W. Auner; Ambrosius P. Snijders; Laurent Bozec; Eileen Gentleman

doi:10.1038/s41467-018-06183-4

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

Silvia A. Ferreira
, Meghna S. Motwani
, Peter A. Faull
, Alexis J. Seymour
, Tracy T.L. Yu
, Marjan Enayati
, Dheraj K. Taheem
, Christoph Salzlechner
, Tabasom Haghighi
, Ewa M. Kania
, Oommen P. Oommen
, Tarek Ahmed
, Sandra Loaiza
, Katarzyna Parzych
, Francesco Dazzi
, Oommen P. Varghese
, Frederic Festy
, Agamemnon E. Grigoriadis
, Holger W. Auner
, Ambrosius P. Snijders

Laurent Bozec, Eileen Gentleman^*

^*Tämän työn vastaava kirjoittaja

Tutkimustuotos: Artikkeli › Tieteellinen › vertaisarvioitu

118 Sitaatiot (Scopus)

40 Lataukset (Pure)

Abstrakti

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 have 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.

Alkuperäiskieli	Englanti
Artikkeli	4049
Sivumäärä	12
Julkaisu	Nature Communications
Vuosikerta	9
Numero	1
DOI - pysyväislinkit	https://doi.org/10.1038/s41467-018-06183-4
Tila	Julkaistu - jouluk. 2018
OKM-julkaisutyyppi	A1 Alkuperäisartikkeli tieteellisessä aikakauslehdessä

Rahoitus

hMSC isolation, culture, and characterization. Human samples used in this research project were obtained from the Imperial College Healthcare Tissue Bank (ICHTB, HTA license 12275). ICHTB is supported by the National Institute for Health Research (NIHR) Biomedical Research Centre based at Imperial College Healthcare NHS Trust and Imperial College London. ICHTB is approved by the UK National Research Ethics Service to release human material for research (12/WA/0196), and the samples for this project were issued from sub-collection R16052. Clinical-grade, bone marrow-derived hMSC were generated from bone marrow (BM) aspirates collected from the iliac crest of healthy paediatric donors with informed consent. BM aspirate was collected in 10 mL tubes and cells were plated the same day in CellSTACK® (Corning, UK) culture chambers at 10–25 × 106 per 636 cm2 after establishing the total number of nucleated cells on a Sysmex SE full blood count analyzer. Cells were cultured in αMEM supplemented with 5% human platelet lysate (Stemulate, Cook Medical, USA) and cultured under standard conditions. When cell confluence of 90–100% was achieved (10–14 days), cells were detached with recombinant trypsin (Roche, DE) and reseeded at 5000 cells per cm2. Cells were then routinely expanded in αMEM supplemented with 10% (v/ v) FBS (using 0.05% Trypsin-EDTA, Thermo Fisher Scientific) and used prior to passage 7. Cells were immunophenotyped with a panel of labeled mouse antihuman antibodies and found to express markers CD90, CD105, CD73, and not express haematopoietic markers CD34 and CD4551. Immunophenotyping was performed at passages 0, 1, 4, and 7. hMSC were tested and devoid of mycoplasma contamination before being used in experiments.

Julkaisufoorumi-taso

Jufo-taso 3

!!ASJC Scopus subject areas

Yleinen kemia
Yleinen biokemia, genetiikka ja molekyylibiologia
Yleinen fysiikka ja tähtitiede

Pääsy asiakirjaan

10.1038/s41467-018-06183-4

s41467-018-06183-4
This work is licensed under a Creative Commons Attribution 4.0 International License. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/
Final published version, 2,33 MBLisenssi: CC BY

http://urn.fi/URN:NBN:fi:tty-201811012525

Siteeraa tätä

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

@article{63ea835deb054ca694c73e4953a47324,

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 have 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 S.\} and Faull, \{Peter A.\} and Seymour, \{Alexis J.\} and Yu, \{Tracy T.L.\} and Marjan Enayati and Taheem, \{Dheraj K.\} and Christoph Salzlechner and Tabasom Haghighi and Kania, \{Ewa M.\} and Oommen, \{Oommen P.\} and Tarek Ahmed and Sandra Loaiza and Katarzyna Parzych and Francesco Dazzi and Varghese, \{Oommen P.\} and Frederic Festy and Grigoriadis, \{Agamemnon E.\} and Auner, \{Holger W.\} and Snijders, \{Ambrosius P.\} and Laurent Bozec and Eileen Gentleman",

year = "2018",

month = dec,

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

language = "English",

volume = "9",

journal = "Nature Communications",

issn = "2041-1723",

publisher = "Nature Research",

number = "1",

}

Ferreira, SA, Motwani, MS, Faull, PA, Seymour, AJ, Yu, TTL, Enayati, M, Taheem, DK, Salzlechner, C, Haghighi, T, Kania, EM, Oommen, OP, Ahmed, T, Loaiza, S, Parzych, K, Dazzi, F, Varghese, OP, Festy, F, Grigoriadis, AE, Auner, HW, Snijders, AP, Bozec, L & Gentleman, E 2018, 'Bi-directional cell-pericellular matrix interactions direct stem cell fate', Nature Communications, Vuosikerta 9, Nro 1, 4049. https://doi.org/10.1038/s41467-018-06183-4

TY - JOUR

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

AU - Ferreira, Silvia A.

AU - Motwani, Meghna S.

AU - Faull, Peter A.

AU - Seymour, Alexis J.

AU - Yu, Tracy T.L.

AU - Enayati, Marjan

AU - Taheem, Dheraj K.

AU - Salzlechner, Christoph

AU - Haghighi, Tabasom

AU - Kania, Ewa M.

AU - Oommen, Oommen P.

AU - Ahmed, Tarek

AU - Loaiza, Sandra

AU - Parzych, Katarzyna

AU - Dazzi, Francesco

AU - Varghese, Oommen P.

AU - Festy, Frederic

AU - Grigoriadis, Agamemnon E.

AU - Auner, Holger W.

AU - Snijders, Ambrosius P.

AU - Bozec, Laurent

AU - Gentleman, Eileen

PY - 2018/12

Y1 - 2018/12

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 have 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 have 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.

U2 - 10.1038/s41467-018-06183-4

DO - 10.1038/s41467-018-06183-4

M3 - Article

C2 - 30282987

AN - SCOPUS:85054315213

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

Abstrakti

Rahoitus

Julkaisufoorumi-taso

!!ASJC Scopus subject areas

Pääsy asiakirjaan

Sormenjälki

Siteeraa tätä