Adipogenic Histone Mark Regulation by Matrix Metalloproteinase 14 in Collagen-Rich Microenvironments

Sato-Kusubata, Kaori; Yi-bin, Jiang; Ueno, Yoko; Chun, Tae Hwa

doi:10.1210/me.2010-0429

Cited by 18 publications

(16 citation statements)

References 43 publications

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“…The lobules of adipocytes are enwrapped by a dense network of collagen fibers, particularly in subcutaneous adipose tissues (Chun et al, 2006). Type I collagen fibers are suppressive to adipogenic histone modifications, which precede adipocyte gene expression (Sato-Kusubata et al, 2011). Therefore, the collagen-rich environment may restrain the full adipogenic potential of ASCs in subcutaneous adipose tissues in vivo .…”

Section: Discussionmentioning

confidence: 99%

“…Adipogenesis was induced by adding 10 μg/ml porcine insulin, 0.5 mM 3-Isobutyl-1-Methyxathine, and 0.25 μM dexamethasone (all from Sigma) as described before (Sato-Kusubata et al, 2011). The lipid droplets were visualized using BODIPY 493/503 (Molecular Probe) (Listenberger and Brown, 2001).…”

Section: Methodsmentioning

confidence: 99%

“…Fluoresceinated collagen degradation assay was performed as described previously (Chun and Inoue, 2014; Sato-Kusubata et al, 2011). Type I collagen was extracted from aged rat tails and lyophilized.…”

Section: Methodsmentioning

confidence: 99%

“…While subcutaneous Sca1 high cells exerted slow and focused collagenolysis mediated by membrane-bound collagenases (MMP14-MMP2 axis), visceral Sca1 high cells displayed rapid, bulk collagenolysis, which is partly mediated by secreted collagenases, i.e., MMP8 or MMP13. (Sabeh et al, 2009; Sato-Kusubata et al, 2011) and a MMP-independent mechanism.…”

Section: Introductionmentioning

confidence: 99%

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Fat depot-specific gene signature and ECM remodeling of Sca1high adipose-derived stem cells

Tokunaga¹,

Inoue²,

Yi-bin³

et al. 2014

Matrix Biology

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Stem Cell Antigen-1 (Sca1 or Ly6A/E) is a cell surface marker that is widely expressed in mesenchymal stem cells, including adipose-derived stem cells (ASCs). We hypothesized that the fat depot-specific gene signature of Sca1high ASCs may play the major role in defining adipose tissue function and extracellular matrix (ECM) remodeling in a depot-specific manner. Herein we aimed to characterize the unique gene signature and ECM remodeling of Sca1high ASCs isolated from subcutaneous (inguinal) and visceral (epididymal) adipose tissues. Sca1high ASCs are found in the adventitia and perivascular area of adipose tissues. Sca1high ASCs purified with magnetic-activated cell sorting (MACS) demonstrate dendrite or round shape with the higher expression of cytokines and chemokines (e.g., Il6, Cxcl1) and the lower expression of a glucose transporter (Glut1). Subcutaneous and visceral fat-derived Sca1high ASCs particularly differ in the gene expressions of adhesion and ECM molecules. While the expression of the major membrane-type collagenase (MMP14) is comparable between the groups, the expressions of secreted collagenases (MMP8 and MMP13) are higher in visceral Sca1high ASCs than subcutaneous ASCs. Consistently, slow but focal MMP-dependent collagenolysis was observed with subcutaneous Sca1high ASCs, whereas rapid and bulk collagenolysis was observed with visceral Sca1high ASCs in MMP-dependent and –independent manners. These results suggest that the fat depot-specific gene signatures of ASCs may contribute to the distinct patterns of ECM remodeling and adipose function in different fat depots.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Fat depot-specific gene signature and ECM remodeling of Sca1high adipose-derived stem cells

Tokunaga¹,

Inoue²,

Yi-bin³

et al. 2014

Matrix Biology

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“…One is that during adipogenesis the ECM develops from a fibrillar to laminar structure as cells move from commitment to growth and triglyceride storage (Mariman and Wang, 2010). In addition, adipogenesis tends to proceed in a collagen-rich ECM environment (Sato-Kusubata et al, 2011). Further, mature adipocytes invest a substantial amount of energy on ECM maintenance (Mariman and Wang, 2010).…”

Section: Marbling Physiology and Developmentmentioning

confidence: 99%

Longitudinal muscle gene expression patterns associated with differential intramuscular fat in cattle

Hudson

Reverter

Greenwood

et al. 2015

Animal

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Intramuscular fat (IMF) can improve meat product quality through its impact on flavour and juiciness. High marbling cuts can command premium prices in some countries and grading systems, but there is substantial cost involved in choosing to grain feed animals in an effort to deposit more IMF. There would be value in developing methods to predict predisposition to 'marble' well. Unfortunately, the biological mechanisms underpinning marbling remain a mystery: the key adipocyte cell populations have not been defined, there are no reliable DNA markers, no known (if any) causal mutations and gene expression analyses in the main have tended to characterise increases in expression of end-point fat metabolism proteins such as the fatty acid-binding proteins. To shed light on expression-based markers of marbling potential, we contrasted LD gene expression in high IMF Wagyu cross animals with a low IMF Piedmontese cross at various time points. The expected divergence in the fat metabolism genes FABP4, THRSP, CIDEC and ACACA between the breeds occurs surprisingly late in postnatal development at about 20 months. On the other hand, divergent expression of WISP2, RAI14 and CYP4F2 was discovered in animals at or before 12 months of age, suggesting these genes may have potential as earlier predictors of marbling potential. In line with other researchers, we found intriguing links between IMF development and connective tissue remodelling. WISP2 -a novel adipokine highly expressed and secreted by adipose precursor cells and an inhibitor of the pro-fibrotic connective tissue growth factor -emerges as a particularly attractive candidate. It is relatively upregulated in high marbling Wagyu before admission to feedlotting, somewhere between 7 and 12 months. This difference is subsequently maintained until 25 months, but not thereafter. RAI14, thought to play a role in porcine adipocyte differentiation and with links to retinoic acid metabolism, has an unusual expression profile. Its expression level increases monotonically with postnatal development, and is always higher in Wagyu than Piedmontese. Strong, sustained upregulation of the anti-inflammatory CYP4F2 in Piedmontese is consistent with Wagyu adiposity being a pro-inflammatory state. Application of regulatory impact factor analysis, a network method for identifying causal effector molecules, suggests marbling roles for transcription factors previously implicated in (1) the formation of liposarcoma (unconstrained fatty masses) (YEATS4, MDM2), (2) adipogenesis (CREBL2, SP1, STAT1) and (3) inflammation (ISGF3G, HOXB13, PML).

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Inhibition of MMP-13 prevents diet-induced obesity in mice and suppresses adipogenesis in 3T3-L1 preadipocytes

Shih

Ajuwon

2015

Mol Biol Rep

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Adipose tissue remodeling by the matrix metalloproteases (MMPs) is critical for tissue hypertrophy and obesity. MMP-13 is an important protein that is highly expressed in adipose tissue but whose potential role in adipose tissue expansion is poorly characterized. We investigated the effect of pharmacological inhibition of MMP-13 with a selective inhibitor, CP-544439, on adipose tissue mass in mice on a high fat diet, and determined the effect of the inhibitor during in vitro adipocyte differentiation of 3T3-L1 cells. CP-544439 was administered for 6 weeks to mice on a high fat diet. Body adiposity and glucose tolerance was determined. Differentiating 3T3-L1 adipocytes were also treated with the inhibitor for a maximum of 8 days and adipogenesis assessed. Treatment of mice with the inhibitor resulted in reduction in body adiposity and improvement in glucose clearance. Histological examination of epididymal adipose showed reduced adipocyte hypertrophy accompanied by increased staining for collagen in the inhibitor treated mice. Treatment of differentiating 3T3-L1 cells with the inhibitor resulted in reduced adipocyte differentiation. Knockdown of MMP-13 using small interfering RNA in differentiating 3T3-L1 cells reduced adipocyte differentiation indicated by reduced expression of PPARγ. These results suggest that MMP-13 may play a major role in adipose development and its inhibition could be a potential strategy to prevent obesity.

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Adipogenic Histone Mark Regulation by Matrix Metalloproteinase 14 in Collagen-Rich Microenvironments

Cited by 18 publications

References 43 publications

Fat depot-specific gene signature and ECM remodeling of Sca1high adipose-derived stem cells

Fat depot-specific gene signature and ECM remodeling of Sca1high adipose-derived stem cells

Longitudinal muscle gene expression patterns associated with differential intramuscular fat in cattle

Inhibition of MMP-13 prevents diet-induced obesity in mice and suppresses adipogenesis in 3T3-L1 preadipocytes

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