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  5. Physiological Mechanisms Regulating Development of Marbling
PROJECT SUMMARY

Phase II - Physiological Mechanisms Regulating the Coordinated Development of Marbling and Muscle in Stocker Cattle

Principle Investigator(s):
Clint Krehbiel1, Udaya DeSilva1, Gerald Horn1, Jessica Starkey2, and Phillip Lancaster1 
Institution(s):
      1Oklahoma State University
2Texas Tech University
Completion Date:
May 2012
Background

Marbling, or intramuscular fat, is the primary determinant of quality grades for beef, and has a strong relationship with palatability such that improvements in marbling development could enhance consumer demand for beef. Marbling deposition is a lifetime event and pre-feedlot nutrition has a significant impact on marbling deposition indicating that the stocker phase of production is critical to improving marbling development. In addition, 76% of the yearly calf crop enters a backgrounding/stocker program prior to finishing; thus, there is tremendous opportunity to improve carcass quality attributes by influencing adipose tissue development during the backgrounding/stocker phase of production.

One of the primary objectives of the backgrounding/stocker phase is to enhance muscle development of young calves. Marbling deposits develop in close association with muscle fibers, and one of the primary objectives of the backgrounding/stocker phase is to enhance muscle development of young calves. Marbling deposits develop in close association with muscle fibers, and marbling score is related to measures of energy metabolism and vascular development in longissimus muscle. Proliferation and differentiation of satellite cells during postnatal muscle growth is regulated by many growth factors such as insulin-like growth factor-I and myostatin, which influence adipocyte differentiation. Thus, muscle growth and metabolism could have a significant influence on marbling development, but little research has evaluated the physiological mechanisms regulating muscle and marbling development. Our central hypothesis is that stocker cattle production systems can be manipulated to enhance marbling development through changes in intercellular signaling between muscle and marbling promoting adipocyte differentiation. The objective of this study was to further investigate how altering beef stocker cattle rate of gain produces changes in metabolism and intercellular signaling mechanisms in skeletal muscle that stimulate differentiation of preadipocytes and initiate development of marbling deposits.


Methodology

Longissimus muscle (LM) samples previously collected from steers grazing wheat pasture to produce either a low (LGW) or high (HGW) rate of gain (3 steers/treatment) in 2 consecutive years were dissected and sorted into immature, intermediate, and mature intramuscular fat deposits along with the associated longissimus muscle tissue. Samples in year 1 were collected from steers at similar age, whereas samples in year 2 were collected at similar BW. Expression of genes involved in vascular development and growth factors involved in intercellular signaling between skeletal muscle and intramuscular fat were measured to determine physiological mechanisms involved in coordinated development of muscle and intramuscular fat.

Bovine satellite cells (BSC) were previously isolated from longissimus muscle of steers in year 2 from 4 stocker production systems: 1) grazing winter wheat pasture at a low stocking density (1.1 steers/ha) to produce a high rate of gain (HGW); 2) grazing winter wheat pasture at a high stocking density (2.2 steers/ha) to produce a moderate rate of gain (LGW); 3) grazing dormant winter native range supplemented with corn/cottonseed meal at 1% of BW followed by short season grazing on summer pasture (CORN); and 4) grazing dormant winter native range supplemented with cottonseed meal at 1.0 kg•steer-1•d-1 followed by season-long grazing on summer pasture (CON). Conditioned medium was collected from proliferating and differentiating bovine satellite cells and applied to cultures of mouse preadipocytes. Expression of genes involved in adipocyte differentiation in mouse preadipocytes and staining of preadipocytes for lipid droplets was used to determine effects of satellite cells on preadipocyte differentiation.

Two meta-analyses were conducted to evaluate nutritional and management practices during the stocker/backgrounding phase on carcass characteristics. The first meta-analysis used previous studies in our lab to evaluate the relationships of marbling score and rib fat thickness with rate of gain and carcass weight at the end of the stocker phase. Regression analysis was used to determine relationships between carcass traits and stocker cattle performance. The second meta-analysis used previously published studies in the literature to evaluate the level of starch in backgrounding diets on final carcass characteristics.


Findings

This study has yielded a number of significant observations for known flavor precursors and volatile flavor compounds. Differences were observed among lipid fractions and USDA-quality grades which may be contributing to volatile flavor compounds. Polar lipid fatty acids were found to be degraded differently during cooking compared with neutral lipid fatty acids.  Among Low Choice and Standard quality grade amino acids, greater concentrations of Strecker aldehyde forming amino acids were found. Additionally, cooking increased the concentration of all free amino acids except cysteine. Quality grade was found to have no effect on many important reducing sugars. However, cooking dramatically decreased the concentration of reducing sugars. Ribose was found to be more affected by cooking in Low Choice and Standard quality grade steaks, than Prime steaks.

Among nucleotide compounds, it was found that raw Standard steaks possessed greater amounts of taste contributing compounds than Low Choice and Prime graded steaks. Cooking was found to dramatically increase adenosine-5-monophosphate, which when degraded may ultimately provide the reducing sugar, ribose. In addition, thiamin was found to not be affected by quality grade and decreased with cooking.

Specific volatile compounds were identified, which have previously been shown to contribute to beef flavor. Many of the determined compounds are known to be the results of degradation or interactions of precursor compounds. Regardless, positive flavor contributing compounds were observed to be greater among Prime quality grade steaks.    

Implications

Marbling is an important attribute of beef that influences palatability and consumer demand. However, methods to improve marbling relative to other fat depots have been difficult to develop.  One of the possible reasons for this may be the influence the muscle environment has on marbling, but not on other fat depots. Results of this study indicate a highly coordinated mechanism between longissimus muscle and intramuscular adipose tissue regulating the early stages of intramuscular adipose tissue development, and that bovine satellite cells with greater proliferative capability inhibit the differentiation of preadipocytes. These results suggest that skeletal muscle exerts significant control over development of new intramuscular fat deposits, which may explain why different stocker and backgrounding programs have little effect on the final marbling score when cattle are finished with similar genetic potential for muscle growth.  

Photos

  • Figure 1.  Relationship of marbling score with ADG during the grazing phase (A) and HCW at intermediate harvest (B) or the relationship of 12th-rib fat with ADG during the grazing phase (C) and HCW at intermediate harvest (D) when steers are harvested at similar age (♦) or BW (■) prior to finishing.
  • A) Marbling score at similar age (solid line) = 106.17 + 170.96*ADG; R2 = 0.723; RMSE = 50.70. Marbling score at similar BW (dashed line) = 167.12 + 98.2041*ADG; R2 = 0.271; RMSE = 60.07.  
  • B) Marbling score at similar age (solid line) = -163.14 + 2.0208*HCW; R2 = 0.783; RMSE = 43.90. Marbling score at similar BW (dashed line) = -206.34 + 2.1283*HCW; R2 = 0.352; RMSE = 56.79. 
  • C) 12th-rib fat thickness at similar age (solid line) = -0.0472 + 0.2123*ADG + 0.4456*ADG2; R2 = 0.856; RMSE = 0.163. 12th-rib fat thickness at similar BW (dashed line) = -0.02499 + 0.4706*ADG; R2 = 0.434; RMSE = 0.201. 
  • D) 12th-rib fat thickness at similar age (solid line) = 1.2005 – 0.01883*HCW + 0.000073*HCW2; R2 = 0.737; RMSE = 0.219. 12th-rib fat thickness at similar BW (dashed line) = -1.5807 + 0.009096*HCW; R2 = 0.450; RMSE = 0.197. 

Figure 2. Photographs representing different stages of intramuscular adipose tissue development using a dissecting microscope and camera; A) initial stage, B) intermediate stage, and C) late stage of development of intramuscular adipose tissue between muscle bundles in steer #511. 

Graphs/Tables

Table 1. Relative mRNA expression of genes evaluated in intramuscular adipose tissue of different  stages of maturity in steers in year 1 and 2. 

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  • 1 G3PDH= Glycerol-3- phosphate dehydrogenase; FASN= Fatty acid synthase; FABP4= Adipocyte fatty acid binding protein; DLK1= Delta-like 1- pre-adipocyte factor-1; PPARγ= Peroxisome proliferator-activated receptor gamma; ACVR2B= Activin A receptor IIB; FST= Follistatin; ANGPT1= Angiopoietin-1: ANGPT2= Angiopoietin-2; VEGFA= Vascular endothelial growth factor; IGF1R= Insulin-like growth factor 1 receptor; IGFBP6= Insulin-like growth factor binding protein 6; IGFBP2= Insulin- like growth factor binding protein 2; IGFBP5= Insulin- like growth factor binding protein 5; IGFBP3= Insulin-like growth factor binding protein 3; IGFBP4= Insulin-like growth factor binding protein 4; IGFBP1= Insulin-like growth factor binding protein 1; ADIPOQ= Adiponectin
  • 2MM = immature intramuscular fat; ME = intermediate intramuscular fat; MA = mature  intramuscular fat. 
  • abLSmeans within a row and year with unlike superscripts differ (P < 0.05).
Graphs/Tables

Table 2. Relative mRNA expression of genes evaluated in longissimus muscle associated with intramuscular fat in steers grazing wheat pasture in year 1 and 2. 

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  • 1ND2= NADH dehydrogenase subunit 2; COX3= Cytochrome c oxidase subunit III; VEGFA= Vascular endothelial growth factor A; ANGPT1= Angiopoietin-1; ANGPT2= Angiopoietin-2; MSTN= Myostatin; IGF-I= Insulin-like growth factor 1; ADIPOR1= Adiponectin receptor 1; ADIPOR2 = Adiponectin receptor 2. 
  • 2NF = longissimus muscle not associated with intramuscular fat; MM = longissimus muscle associated with immature intramuscular fat; ME = longissimus muscle associated with intermediate intramuscular fat; MA = longissimus muscle associated with mature intramuscular fat
  • abLSmeans within a row and year with unlike superscripts differ (P < 0.05).

Table 3. Correlations of angiogenic gene expression in longissimus muscle with gene expression in  corresponding immature, intermediate, and mature intramuscular adipose tissue (IM). 

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  • 1VEGFA = vascular endothelial growth factor A; ANGPT1 = angiopoietin 1; ANGPT2 = angiopoietin 2; FASN = fatty acid synthase; PPARγ = peroxisome proliferator activated receptor gamma; ADIPOQ = adiponectin. 
  • *Correlations are significantly different from zero (P < 0.05).

Table 4. Expression of genes (relative fold change) involved in adipogenic differentiation of 3T3-L1  preadipocytes exposed to conditioned media from mitotically active skeletal muscle satellite cells (96 h  in culture) of stocker cattle from different production systems at the conclusion of the stocker and  finishing phases1 

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  • 1Values are least squares means ± SEM. 
  • 2CON = season-long grazing production system (n = 4).
  • 3CORN = short-season grazing production system (n = 4).
  • 4LGW = low-gain wheat pasture production system (n = 4).
  • 5HGW = high-gain wheat pasture production system (n = 4).
  • 6Lipid Accumulation = percent of total cells positive for Oil Red O staining.
  • a,bMeans within a row lacking a common superscript letter differ (P ≤ 0.05).

Table 5. Meta-analysis of carcass traits from steers fed high- versus medium- or high- versus low-starch  growing diets prior to finishing. 

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  • 1HCW = hot carcass weight, KPH = kidney, pelvic and heart fat. 
  • 2Marbling grid: Slight00=300, Small00=400, Modest00=500.